PAN-AMERICAN JOURNAL OF AQUATIC SCIENCES

Transcription

PAN-AMERICAN JOURNAL OF AQUATIC SCIENCES - PANAMJAS
Executive Editor: Maria Cristina Oddone
Scientific Editors: Gonzalo Velasco, Ana Cecília Giacometti Mai, Pablo Muniz, Ronaldo Angelini,
Danilo Calliari, and Samantha Eslava G. Martins
Honorary members: Jorge P. Castello, Omar Defeo, and Kirk Winemiller.
Advisory committee: Júlio N. Araújo, André S. Barreto, Sylvia Bonilla S., Francisco S. C.
Buchmann, Adriana Carvalho, Marta Coll M., César S. B. Costa, Karen Diele, Ruth Durán G.,
Gisela M. Figueiredo, Sergio R. Floeter, Alexandre M. Garcia, Ricardo M. Geraldi, Denis
Hellebrandt, David J. Hoeinghaus, Simone Libralato, Luis O. Lucifora, Paul G. Kinas, Monica G.
Mai, Rodrigo S. Martins, Manuel Mendoza C., Aldo Montecinos, Walter A. Norbis, Enir G. Reis,
Getúlio Rincon Fo., Marcelo B. Tesser, João P. Vieira, and Michael M. Webster.
PanamJAS is a non-profit Journal supported by researchers from several scientific institutions.
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PAN-AMERICAN JOURNAL OF AQUATIC SCIENCES
2006, 1-2
2009, 4 (2)
Quarterly Journal
ISSN 1809-9009 (On Line Version)
CDU 570
Cover photo of this issue: A male of Hippocampus reidi (Teleostei, Syngnathidae) after releasing their newborns into
the environment. The article reporting this event is available on page 154 of this issue. Picture captured by Ana C. G.
Mai in the mangrove region of Rio Camurupim River, state of Piauí, Brazil.
Pan-American Journal of Aquatic Sciences
Research articles
Richness of common names of Brazilian reef fishes.
FREIRE, K. M. F. & CARVALHO FILHO, A. ..........................................................................................96
Evolution and state of the art of fishing capacity management in Peru: The case of the anchoveta
fishery.
ARANDA, M. …………………………………………………….……………………………….146
Size and number of newborn juveniles in wild Hippocampus reidi broods.
MAI, A. C. G. & LOEBMANN, D. …..……………………………………………………………… 154
Cortisol and Glucose: Reliable indicators of fish stress?
MARTINÉZ-PORCHAS, M., MARTÍNEZ-CÓRDOVA, L. R. & RAMOS-ENRIQUEZ, R. ............................158
Aspectos biológicos do peixe-olhudo-dentinho, Synagrops bellus (Actinopterygii: Acropomatidae),
da plataforma externa e talude superior do estado de São Paulo, Brasil.
VASKE JÚNIOR, R., TEIXEIRA, A. F. & GADIG, O. B. F. ………………………………………… 179
First confirmed record of the blunthead puffer, Sphoeroides pachygaster (Osteichthyes:
Tetraodontidae) off the Algerian coast (south-western Mediterranean).
HEMIDA, F., BEN AMOR, M. M. & CAPAPÉ, C. .................................................................................188
A fauna de peixes na bacia do Rio Jucuruçu, leste de Minas Gerais e extremo Sul da Bahia.
SARMENTO-SOARES, L. M., MAZZONI, R. & MARTINS-PINHEIRO, R. F. .......................................... 193
Occurrence of the white anglerfish, Lophiodes beroe Caruso, 1981 (Lophiiformes: Lophiidae), in
Brazilian waters.
ROTUNDO, M. M. & VASKE JÚNIOR, T. …………………………………………………………... 208
A mutton hamlet Alphestes afer (Bloch, 1793) reproductive event in northeast Brazil.
MEDEIROS, D. V., NUNES, J. A. C. C. & SAMPAIO, C. L. S. ………………………………………. 212
New record of the alien mollusc Rapana venosa (Valenciennes 1846) in the Uruguayan coastal zone
of Río de la Plata.
LANFRANCONI, A., HUTTON, M., BRUGNOLI, E. & MUNIZ, P. ..........................................................216
Biofouling of the golden mussel Limnoperna fortunei (Dunker, 1857) over the Anomura crab Aegla
platensis Schmitt, 1942.
LOPES, M. N., VIEIRA, J. P. & BURNS, M. D. M. ..............................................................................222
Pan-American Journal of Aquatic Sciences (2009) 4 (2): 96-250
Zooplankton (Cladocera and Rotifera) variations along a horizontal salinity gradient and during two
seasons (dry and rainy) in a tropical inverse estuary (Northeast Brazil).
SILVA, A. M. A., BARBOSA, J. E. L., MEDEIROS, P. R., ROCHA, R. M., LUCENA-FILHO, M. A. &
SILVA, D. F. ………………………………………………………………………………………. 226
Larval fish assemblage in a tropical estuary in relation to tidal cycles, day/night and seasonal
variations.
BONECKER, F. T., CASTRO, M. S. & BONECKER, A. C. T. ………………………………………… 239
Gametogenesis in the mangrove mussel Mytella guyanensis from northern Brazil.
GOMES, C. P., BEASLEY, C. R., PEROTE, S. M. O., FAVACHO, A. S., TAGLIARO, C. H., FERREIRA,
M. A. P. & ROCHA, R. M. .................................................................................................................247
Diffusion Material - Do not cite
Original scientific photographs
PANDYA, P. J. & VACHHRAJANI, K. D. ………………………………………………………………I
Original scientific photographs
LIRA, S. M. A., AMARAL, F. M. D. & FARRAPEIRA, C. M. R. .............................................................. II
Pan-American Journal of Aquatic Sciences (2009) 4 (2): 96-250
Richness of common names of Brazilian reef fishes
KÁTIA MEIRELLES FELIZOLA FREIRE1 & ALFREDO CARVALHO FILHO2
1
Universidade Federal do Rio Grande do Norte, Departamento de Oceanografia, Praia de Mãe Luíza S/N, Mãe Luíza,
Natal-Rio Grande do Norte, Brazil, 59014-100. Email: kfreire2006@yahoo.com.br
2
Fish Bizz Ltda., Rua Moncorvo Filho 51, São Paulo, Brazil, 05424-070. Email: alfie@telnet.com.br
Abstract. The richness of common names of Brazilian reef fishes is high (7.2 names per species)
and mostly so if the species are commercially important. The high richness of names for easily
seen species such as reef fishes represents one of the Berlin’s attributes leading to the naming
process of living things. The attribute ‘size’ was also tested and indicated that species of
intermediate size receive more names than smaller or larger ones. These names have several
origins, but come mainly from Latin or native languages (Tupi/Tupi-Guarani). Several categories
of words are used in these names as core or modifiers: non-fish animals, morphology, plants,
persons, color pattern, behavior, taste/smell, habitat/ecology, size, and locality/area. A list of
unique common names is proposed for all 547 reef fish species found in Brazil based on the
available array of names. We suggest these names are used whenever cited in a national context.
Key words: common name, folk nomenclature, Berlin’s attributes
Resumo. Riqueza de nomes comuns de peixes recifais brasileiros. A riqueza de nomes comuns
de peixes recifais brasileiros é elevada (7,2 nomes por espécie), principalmente para espécies que
são comercialmente importantes. A elevada riqueza de nomes de espécies facilmente visíveis
como as de peixes recifais representa um dos atributos de Berlin que leva ao processo de
atribuição de nomes às coisas vivas. O atributo ‘tamanho’ foi também testado e indicou que
espécies de tamanho intermediário recebem mais nomes do que espécies menores ou maiores.
Estes nomes têm várias origens, mas vêm principalmente do Latim ou de línguas nativas
(Tupi/Tupi-Guarani). Muitas categorias de palavras são usadas nestes nomes, como núcleo ou
como modificadores: outro animal que não peixe, morfologia, planta, pessoa, padrão de cor,
comportamento, sabor/cheiro, habitat/ecologia, tamanho e localidade/área. Uma lista de nomes
comuns únicos é proposta para todas as 547 espécies de peixes recifais encontradas no Brasil
baseada nos nomes disponíveis. Sugerimos que esses nomes sejam usados sempre que forem
citados em um contexto nacional.
Palavras-Chave: nome comum, nomenclatura popular, atributos de Berlin
Introduction
The first main effort to standardize scientific
names of living beings according to the binomial
nomenclature introduced by Linneaus goes back to
1842 with the production of the Strickland Code
(Minelli 1999). Since then several documents were
produced, culminating, for animals, with the fourth
edition of the International Code of Zoological
Nomenclature in 2000. This represents an attempt to
decrease the incidence of synonymy (two or more
names for the same species) and homonymy (same
name for more than one species). For fishes, the
main effort to update scientific nomenclature is by
William N. Eschmeyer in his three volumes
published in 1998, which have been continuously
updated online (Eschmeyer 2008).
Even though the scientific nomenclature is
intended to facilitate communication among
different cultures and languages, it is almost
restricted to the academic realm. Common names
are used by local communities, commercial and
recreational fishers, divers, in restaurants, by
aquarists, in fisheries statistics, and in legislation, in
some cases in association with the corresponding
scientific names, but most of the times as a standing
alone identification. These different groups may use
Pan-American Journal of Aquatic Sciences (2009), 4(2): 96-145
97
different common names that also reflect local
culture. This poses some problems when dealing
with species at a national level.
North America recognized the importance of
dealing with standard common names a long time
ago, and published the first list of standardized
English names of fishes for that region in 1948.
Since then, there has been a continuous effort on this
matter, culminating with the sixth edition of
common and scientific names of North American
fishes, extending the coverage to include species
occurring in Mexican waters (Nelson et al. 2004).
Similar effort was undertaken in Portugal, leading to
a list of common and scientific names for aquatic
organisms found in Portuguese waters (Sanches
1989). The Food and Agriculture Organization
(FAO) has also put some effort into the
standardization of common names of commercial
species around the world in its three official
languages (English, French and Spanish) (Garibaldi
& Busilacchi 2002).
Brazil is well known for its cultural diversity
and this is also reflected in the richness of common
names of fishes. This richness called the attention of
William A. Gosline in the 1940s (Gerald R. Smith,
Univ. Michigan, Museum of Zoology, MI, USA,
pers. comm.) and has been constantly cited in
several sources (see, e.g.,Welcomme et al. 1979). It
was not until Freire & Pauly (2003) that a
quantification for this richness was made available
in a national scale, indicating that in average six
names are used for each marine fish species in
Brazil, with a maximum of 31 names used for one
species. Homonymy is also common. Freire (2006)
also found a high richness of common names for
freshwater fish species in Brazil (three common
names per species, based on a smaller database of
names), with a maximum of 30 names for one
species. There has been no known initiative to
standardize the common names of Brazilian fishes
using the variety available.
The growing concern with biodiversity loss
and the effect of anthropogenic activities on
biodiversity stress the importance of assessing
taxonomic adequacy (Vecchione et al. 2000). The
bad effect of the misidentification associated with
common names recorded in national fishery
statistics should also not be underestimated (Freire
& Pauly 2005). This work presents an assessment of
the richness of common names for reef and reefassociated fish species, and will provide an initial
list of unique common names for these species.
Hopefully this initiative will trigger a more
comprehensive movement towards the use of similar
process for all other fish species in Brazil.
Materials and Methods
All names compiled in the database
(NAMEDAT) presented here originate from 43 local
lists of common names of fishes extending from the
state of Pará to the state of Rio Grande do Sul, and
for more than 50 years (from 1953 to 2004): FAO
(1953), Barcellos (1962), Brandão (1964), Ihering
(1968), Eskinazi-Leça (1967), Mutti Pedreira
(1971), Anon. (1976), SUDENE (1976), Carvalho &
Branco (1977), CEPA-MA (1978), Figueiredo
(1977), Figueiredo & Menezes (1978), Lima &
Oliveira (1978), Rosa (1980), Menezes &
Figueiredo (1980), Figueiredo & Menezes (1980),
Chao et al. (1982), Paiva (1981), Santos (1982),
Nomura (1984), Menezes & Figueiredo (1985),
Suzuki (1986), Godoy (1987), Martins-Juras (1987),
Soares (1988), Begossi (1989), Lopes (1989),
Begossi & Figueiredo (1995), Ferreira et al. (1998),
Santos et al. (1998), Carvalho-Filho (1999), Ferreira
(1999), Rocha & Costa (1999), CEPENE (2000),
Figueiredo & Menezes (2000), Szpilman (2000),
Ferreira & Cava (2001), Ávila da Silva & Carneiro
(2003),
Ramires
&
Barrella
(2003),
UNIVALI/CTTMar (2004), Sampaio & Nottingham
(2008), Mário Barletta (pers. comm., Universidade
Federal de Pernambuco, Brazil), and Cláudio
Sampaio (pers. comm., Museu de Zoologia da
Universidade Federal da Bahia, Brazil). This
database is based on an extension of a previous work
by the first author for marine and estuarine fishes in
Brazil (Freire & Pauly 2005) that currently includes
a total of 4,649 common names referring to 734
marine and estuarine species (63%) of a total of
1,168 listed in FishBase, a global electronic
encyclopedia of fishes (Froese & Pauly 2008).
A total of 547 reef or reef-associated fish
species (here after referred only as ‘reef species’) are
recorded to date in Brazilian waters. Within the
context of this study, reef is defined as any and all
formation built-up of consolidated bottoms, of
organic or inorganic origin, and which top is no
deeper than 30 m from the surface in the lowest tide
known for that geographic area. For the fish fauna
named as “reef fish”, the ecological niche also
includes the sandy and/or rubble bottom
immediately adjacent to a distance of 20 m from the
ecotone. Thus, any fish species that uses the reef or
its adjacencies for any activity, including shelter,
feeding, reproduction, growth, cleaning or passage,
is considered as reef fish.
The richness of common names for all reef
species was calculated in terms of synonyms
(number of common names for each species). An
indication of the degree in which one fish species
shares the same name (homonyms) was also given.
FREIRE & CARVALHO FILHO
98
For comparison purposes, this analysis was
performed for all reef or reef-associated fish species
and compared with other fish species.
The analysis of the common names included
origin of names, descriptors used in the core of the
name and as first and second modifiers, relation to
commercial importance and size. The origin of the
names was defined based on Tibiriçá (1984), Bueno
(1998), Ferreira (1999), and Cunha (2001).
Information on habitat, fish size, and English
common name was obtained from FishBase (Froese
& Pauly 2008) and local commercial importance
from Carvalho-Filho (1999), Szpilman (2000),
FISHTEC (2003), Espírito Santo (2005), Gasparini
et al. (2005), and SEAP/PROZEE/IBAMA (2006).
Commercial importance was defined based on the
interest for food consumption and/or for aquarists.
Catch data were obtained from an extension of the
database compiled by Freire (2003), based on
national bulletins, and represent an average for the
period from 1995 to 2000.
For the standardization of common names, a
unique name was chosen using an initial list of
species with only one name available. Then, we
dealt first with species having increasingly higher
richness of common names, i.e., with species with
only 2 common names, 3, 4, and so on. Emphasis
was given in the first stage to species of commercial
importance, which would contribute to improvement
in the recording system of catch statistics. In cases
where names were not available, they were
borrowed from the list of Portuguese names
assembled by Sanches (1989), translated from other
languages to Portuguese, or created based on the
criteria used for existing names. We also made use
of criteria defined in Robins et al. (1991) for North
American fishes (updated in Nelson et al. 2004).
Preference was given to simple and descriptive
names. Names tied to scientific names, the ones that
include the word ‘common’, and names that honour
people or were offensive were avoided. The spelling
available in the most widely used Portuguese
dictionary in Brazil – Aurélio (Ferreira 1999) was
used. Two additional criteria were used: no inclusion
of hyphens (to avoid different spellings) and
capitalization of the first letter of the common name.
Names that have been cited in more publications and
used in more Brazilian states were given priority.
Finally, the diversity of origin languages was kept as
much as possible, including native and African
languages.
Results
Quantifying the richness of the common
names. No common name was found for 175 out of
the 547 fish species recognized as reef or reefassociated. It is worth pointing out that about 41% of
those were not associated with any English name,
according to FishBase. Many of the unamed species
were criptic (76 out of 117 criptic species) or
nocturnal (6 out of 10).
The degree of synonymy among reef species
was very high, with 7.2 names per species in average
(excluding those unnamed species). This degree will
probably get higher the more sources of names are
used in the database. Reef species had a higher
degree of synonymy as evidenced by a higher
number of species with more names and lesser
number of species with only one name (Fig. 1). For
criptic species, the degree of synonymy was much
lower: 2.8 names per species in average. One has to
consider that these mean values actually represent
minimum averages of names’ richness, as they will
probably increase the more sources are incorporated
in the names’ database.
a) 140
Reef
Others
120
100
80
60
40
20
0
0
5
10
15 20 25 30 35
Number of common names
40
b) 10000
45
50
Reefs
Others
1000
100
10
1
0
2
4
6
8
10 12 14
Number of species
16
18
20
Figure 1. Nomenclatural richness of Brazilian marine
fishes (reef and other non-reef species): a) frequency of
scientific species that have one to forty-six common
names (synonymy); b) frequency of common names that
correspond to one to twenty scientific species
(homonymy).
Three species presented 30 or more common
names: Opisthonema oglinum (38), Carangoides
crysos (34), and Bathygobius soporator (30). Details
on the complexity of names (and synonymy) are
presented for one species, C. crysos (Fig. 2). Note
that some of these names are only different spellings
of the same word: garujuba, guarajuba, and
99
garajuba; guaraçu and guaracu; guaraçuma,
guarassuma, and guaraxuma; and xarelete, xalerete,
xerelete, xererete, and xereleté. Nine of these
common names were associated with records in
fishery statistics (according with the database
compiled by Freire, 2003): garajuba, graçainha,
guaricema, guaracema, xaréu, taguara, xerelete,
Non-commercial names
Cavaca [0]
Carapau [11]
Cavaco [1]
Oligoplites saurus {15}
xixarro, and solteira (Fig. 2). Twenty-five of them
were not associated with any catch record. Sixteen
out of the 34 names were related to no other species
than C. crysos: cavaca, chumberga, garajuba preta,
garujuba, guaraçu, guaracu, guarainha, guaraxuma,
xalerete, graçainha, taguara, xaréu dourado, xaréu
pequeno, xererete, xereleté, and xumberga.
Commercial names
Carangoides crysos {34}
Garajuba (1854) [4]
Aspistor luniscutis {36}
Graçainha (2) [0]
Guaricema (802) [3]
Chumberga [0]
Guaracema (289) [2]
Garajuba preta [0]
Carangoides bartholomaei {3}
Xaréu (3195) [4]
Carangoides ruber {3}
Garujuba [0]
Chloroscombrus chrysurus {16}
Guarajuba [3]
Guaraçu [0]
Caranx latus {16}
Taguara (9) [0]
Xerelete (1992) [2]
Guaracu [0]
Xixarro (2860) [7]
Selar crumenophthalmus {10}
Solteira (85) [5]
Guarainha [0]
Trachurus lathami {6}
Oligoplites saliens {11}
Guaraçuma [1]
Decapterus macarellus {11}
Guarassuma [1]
Decapterus punctatus {7}
Xarelete [3]
Eucinostomus gula {13}
Trachinotus carolinus {19}
Thyrsitops lepidopoides {4}
Trachinotus marginatus {2}
Guaraxuma [0]
Xalerete [0]
Caranx lugubris {7}
Parona signata {14}
Xaréu dourado [0]
Caranx hippos {21}
Xaréu pequeno [0]
Manezinho [1]
Xaréu branco [4]
Oligoplites saurus {15}
Hemicaranx amblyrhynchus {7}
Alectis ciliaris {23}
Xererete [0]
Xereleté [0]
Pseudocaranx dentex {2}
Xaréu amarelo [1]
Xaréu xixá [1]
Xixarro pintado [1]
Xumberga [0]
Figure 2. Portuguese common names associated with Carangoides crysos in Brazil. Names associated with catch
records are presented in the top-right. Mean annual catches (only for years with positive record) for commercial names
are presented in parentheses (tonnes).The number of additional species associated with each common name is presented
in brackets. The number of common names associated with each species (besides the ones shown) is presented in
braces. Gray boxes indicate common names not related to any species other than C. crysos.
Origin of the common names. The highest
number of common names used to describe
Brazilian reef or reef-associated fishes come from
Latin (37%), followed by Tupi/Tupi-Guarani (30%),
and Brazilianism (15%) (Table I). Brazilianism is
defined as ‘word created by Brazilians’ (Ferreira
1999). Spanish, Greek, Arabic, and African together
represent 15% of all names. Native languages
correspond to 1% of all names and may include
Tupi/Tupi-Guarani. However, the sources used did
not indicate the specific language. One should
consider that there are about 187 living native
languages in Brazil, some of them spoken by only a
dozen of people (SIL International, 2008). The
influence of African languages in this field is very
low compared to other fields.
Table I. Origin of the common names of reef
Brazilian fishes.
Origin
Count
%
Latin
898
37
Tupi/Tupi-Guarani
717
30
Brazilianism
329
14
Spanish
121
5
Greek
114
5
Arabic
79
3
African
48
2
Native
29
1
Others
84
3
Total
2419
100
Descriptors used for the names. Names of
Brazilian fishes are formed by a single word or by a
100
composite of up to four words. The first word (or
core) represents mainly primary lexemes, followed
by non-fish animal, morphology, plant, person
(generic), color pattern, behavior, and person
(specific) (Fig. 3). Taste/smell, habitat/ecology, size,
and locality/area are not commonly used as core.
Core
Modifier 1
40
Modifier 2
30
20
mod. for abundance
locality/area
size
habitat/ecology
taste/smell
person (specific)
behavior
color pattern
other
person (generic)
plant
inanimate object
primary lexeme
0
morphology
10
non-fish animal
Relative frequency (%)
50
Figure 3. Relative frequency of each descriptor used in the core, modifier 1 and modifier 2 for reef and reef-associated
Brazilian fishes.
Effect of commercial importance and
size. Species of commercial interest had an average
of 8.2 common names per species and noncommercial species had a lower synonymy rate
(4.6). Figure 4 indicated that species of no
commercial interest were usually small and had less
than 15 names per species (with Bathygobius
soporator being an exception, with 30 common
names). Species of commercial interest were larger
and had a wider range of names. Many species had
more than 15 names, with a maximum of 38 names
for Opisthonema oglinum. It is interesting to point
out that very large species had few names resulting
in an asymmetry in the relationship between degree
of synonymy and size. A total of 68% of the species
with no common name for which size information
was available were smaller than 0.20 m. Only seven
species with no name were larger than 1 m:
Callechelys bilinearis, Channomuraena vittata,
Himantura schmardae, Mobula japonica,
Mobula
tarapacana, Mobula thurstoni, and Muraena
melanotis.
No. of common names
40
30
20
10
0
0
1
2
3
4
5
6
7
8
Total length (m)
Figure 4. Relationship between the number of common names and the maximum size of each reef species. Closed
diamonds indicate species of no commercial interest and open squares indicate commercial species (food or aquarium
trade). Note that one non-commercial species 20 m long (with three common names) was removed from the graph to
better represent the remaining species (Rhincodon typus) .
101
A total of 87 species included in this
database are in the ornamental trade. These species
were associated to a mean number of 4.8 common
names, which was smaller than the average of
7.2 for reef species in general. These species were
mainly smaller than 1 m and those species with
no common name were very small (6-10 cm;
Fig. 5).
No. of common names
25
20
15
10
5
0
0
50
100
150
200
250
300
Total length (cm)
Figure 5: Relationship between the number of common names and the maximum size of each reef fish species for
ornamental trade.
Standardization of common names. Only
seven species of Brazilian reef fishes had a
unique common name that refers to no other
species in the database compiled here (Table II).
The remaining species had more than one
common name or shared the same name with
other species. To overcome this confusion, a list
was created containing all names linked to
each species and a unique common name was
proposed for each one of the 547 reef species
occurring in Brazil (Table III). These unique
names indicate that only one common name was
used for each species and that name was not shared
with any other species.
Table II. List of reef species presenting one unique common name in Brazil, based in the sources presented
here and included on NAMEDAT.
Species
Carcharhinus signatus
Conger triporiceps
Dactyloscopus tridigittatus
Entomacrodus vomerinus
Haemulon chrysargyreum
Muraena retifera
Negaprion brevirostris
Portuguese name
Cação noturno
Congro dentão
Tanduju mirim
Macaco pérola
Cocoroca boquinha
Moréia de roseta
Cação limão
Discussion
The degree of synonymy was high among
reef species in Brazil. This corroborates one of the
Berlin’s principles: species that are more visible
(such as reef species) are more prone to be named
(Berlin 1992). However, several reef species had no
name, which indicates that not only the habitat,
associated to the ease of access, is important in the
naming process. Other factors also play a role and
are discussed below.
Commercial importance has been stated
as one of the Berlin’s attributes leading to the
English name
Night shark
Manytooth conger
Sand stargazer
―
Smallmouth grunt
Reticulate moray
Lemon shark
naming process of plants and animals (Berlin
1992). It is related to the utilitarian concept
defended by Hunn (1982), and was demonstrated
for Philippines fishes by Palomares & Pauly
(1999) and for Brazilian marine fishes by
Freire & Pauly (2005). We analyzed the influence
of the commercial importance on the richness
of common names of reef fish species occurring
in Brazil and found that the degree of synonymy
is much higher for commercialspecies (8.2
names per species) than for non-commercial
species (4.6).
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
1
Ablennes hians
Agulha, Agulha fita, Agulha pintada, Carapiá, Zambaia taba
Carapiá
Carvalho-Filho (1999)
2
Abudefduf saxatilis
Acará da pedra, Camisa de meia, Camiseta, Cará das pedras, Sargento
Carapiaçaba, Carapicu, Castanheta, Maria mole, Oá, Palhaço, Peixe
sargento, Querê querê, Querquerê, Saberé, Saberê, Salema feiticeira,
Sargento, Sinhá rosa, Soldado moura, Tinhuma, Tinhuna, Viuvinha
3
Acanthistius brasilianus Badejo, Garoupa, Garoupa senhor de engenho, Mero, Senhor de engenho, Senhor de engenho
Serigado focinhudo, Serigado mero
4
Acanthistius
patachonicus
5
Acanthocybium solandri Aimpim, Cavala, Cavala aimpim, Cavala aipi, Cavala aipim, Cavala Cavala aipim
empinge, Cavala impim, Cavala pim, Cavala wahoo, Guarapicu,
Guarapucu, Wahoo
6
Acanthostracion
polygonia
Baiacu caixão, Cofre, Peixe cofre, Peixe cofre colméia, Peixe vaca
7
Acanthostracion
quadricornis
Baiacu caixão, Baiacú chifrudo, Baiacu de chifre, Chifrudo, Cofre de Cofre de chifre
chifre, Peixe boi, Peixe cofre, Peixe cofre riscado, Peixe vaca, Taoca,
Taóca, Toaca
8
Acanthurus bahianus
Acaraúna azul e preta, Bahianus, Barbeiro, Cirurgião, Lanceta, Peixe Acaraúna cinza
cirurgião
Freire, pers. comm.
9
Acanthurus chirurgus
Acaraúna, Acaraúna preta, Barbeiro, Barbeiro comum, Carauna, Caraúna, Acaraúna preta
Caraúna preta, Cirurgião, Lanceta, Peixe cirurgião, Peixe doutor
Nomura (1984)
10
Acanthurus coeruleus
Acara úna, Acaraúna azul, Acaraúna azul e preta, Acaraúna preta, Acaraúna azul
Barbeiro, Barbeiro azul, Caraúna azul, Cirurgião azul, Lanceta, Peixe
cirurgião, Peixe doutor
Nomura (1984)
11
Acanthurus monroviae
NENHUM
12
Achirus lineatus
Aramaçá, Aramaçá tapa, Linguado, Maraçapeba, Sôia, Solha, Solha Aramaçá tapa
redonda, Tapa
Badejo argentino, Badejo do sul
Badejo do sul
Peixe cofre colméia
102
Table III. List of all common names associated with Brazilian reef fish species and their unique name chosen according to the source presented.
Nomura (1984)
Nomura (1984)
IBAMA Inst. Normativa
14/2004
Anon. (1976)
Cirurgião de espinho Rangel, pers. comm.**
amarelo
Nº SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
13 Acyrtops beryllina
NENHUM
Ventosa esmeralda
Rangel & CarvalhoFilho, pers. comm.
14 Acyrtus pauciradiatus NENHUM
15 Aetobatus narinari
Limpa vidro de noronha Sampaio, pers.
comm.***
Ajeru, Ajuru, Arraia morcego, Arraia pintada, Cação anjo, Narinari, Raia chita
Papagaio, Pintada, Raia chita, Raia leopardo, Raia pintada
Enguia, Moréia, Muriongo
Muriongo amarelo
Mod. from CarvalhoFilho (1999)
17 Albula nemoptera
Ubarana, Ubarana focinho de rato
Juruna mirim
18 Albula vulpes
Álbula, Arabaiana boca de rato, Bicudo, Focinho de rato, Juruma, Juruna, Juruna açú
Obarana, Obarana focinho de rato, Obarana rato, Parati mico, Peixe rato,
Ratão, Robalo da pedra, Tubarana, Ubarana, Ubarana boca de rato,
Ubarana do norte, Ubarana focinho de rato, Ubarana mirim, Ubarana
rato, Ubarana roliça, Urubaiana boca de rato
Carvalho-Filho, pers.
comm.
Mod. from Nomura
(1984)
19 Alectis ciliaris
Abacataia, Abacatina, Abacatuaia, Abacatuia, Abacatúxia, Abacutaia, Xaréu branco
Aleto, Aracaguira, Aracambé, Aracanguira, Aracangüira, Aranguira,
Galo, Galo bandeira, Galo de capacho, Galo do alto, Galo fita, Galo
pluma, Galo rabudo, Peixe galo, Peixe galo do Brasil, Xaréu bandeira,
Xaréu branco, Xaréu penacho
20 Alopias vulpinus
Cação macaco, Cação pena, Cação raposa, Rabilongo, Rabudo, Raposa, Tubarão raposa comum Mod. from Suzuki (1986)
Tubarão raposa
21 Alphestes afer
Aruçapeba, Badejo, Cerigado vermelho, Garaçapé, Garoupa, Garoupa Pirapiranga
gato, Garoupa rajada, Gato, Peixe gato, Pira piranga, Pirá piranga,
Pirapiranga, Ruçapeba, Sapa, Sapá, Sapé, Sapé pintado, Sapê pintado,
Serigado vermelho, Sulalepa, Sulapeba
Nomura (1984)
22 Aluterus heudelotii
Peixe porco
Carvalho Filho & Freire,
pers. comm.
23 Aluterus monoceros
Cangulo, Cângulo, Cangulo comum, Gudunho, Peixe porco, Peixe rato, Gudunho comum
Perua, Pirá acá
Gudunho serrilhado
Mod. from Nomura
(1984)
103
16 Ahlia egmontis
Table III. List of all common names associated with Brazilian reef fish species and their unique name chosen according to the source presented (cont.).
Nº SPECIES
COMMON NAMES
24 Aluterus schoepfii
Peixe porco, Peixe lixa, Peixe rato, Peroá pena, Porco lixa, Raquet Gudunho galhudo
laranja
Cangulo de areia, Cangulo pavão, Cangulo velho, Peixe porco, Peixe Cangulo pavão
rato, Raquete listrado
Peixe gavião, Pinos, Sarampinho
Pinos
pers. comm.
Carvalho-Filho, pers. comm.
Mod. from Nomura (1984)
using FishBase
25 Aluterus scriptus
26 Amblycirrhitus pinos
UNIQUE NAME
SOURCE
27 Amphichthys
cryptocentrus
28 Anarchias similis
Cuíca, Mamangá liso, Pacamão, Pacamon, Peixe sapo, Pucumã
Pacamão bocon
NENHUM
Moréia lobo
29 Anarchopterus tectus
NENHUM
Peixe cachimbo ilhéu Carvalho-Filho, pers. comm.
30 Anchoa cubana
Manjuba
Manjuba cubana
31 Anchoa filifera
Manjuba
Manjuba de fita
32 Anchoa lyolepis
Enchoveta, Manjuba, Manjuba boca de rato
Manjuba boca de rato Begossi & Figueiredo (1995)
33 Anchoa tricolor
Enchova, Enchoveta, Irico, Manjuba, Manjuba branca, Tungão
Manjuba branca
34 Anchoviella
lepidentostole
Don don, Manjuba, Manjuba de Iguape, Manjubinha, Sardinha, Manjuba de Iguape
Sardinha selvagem
35 Anisotremus moricandi Avô do pirambú, Fumeiro
38 Antennarius
multiocellatus
39 Antennarius striatus
Lima & Oliveira (1978)
Avila da Silva & Carneiro
(2003)
Mod. Ferreira & Cava (2001)
Beiçudo, Perambu, Pirambu, Pirambú, Salema, Salema açu, Salgo, Sargo verdadeiro
Salgo de beiço, Sargo, Sargo beiçudo, Sargo de beiço, Zumbi
Ferrugem, Frade, Mercador, Par de leme, Salema, Salema branca, Salema
Salema de freio, Sambuari, Selumixira
Aniquim, Antenarius, Peixe sapo
Peixe sapo de recife
Antenarius, Guaperva, Peixe pescador, Peixe pescador riscado, Peixe Peixe pescador
sapo
riscado
Sampaio
(2008)
40 Anthias salmopunctatus Antias de São Pedro e São Paulo
Canário do mar
Nomura (1984)
Mod. from Szpilman (2000)
&
Nottingham
36 Anisotremus
surinamensis
37 Anisotremus virginicus
Avô do pirambu
104
COMMON NAMES
UNIQUE NAME
SOURCE
41 Apogon americanus
Apogon, Apogon brasileiro, Cardeal fogo, Olhão, Totó vermelho
Totó vermelho
42 Apogon planifrons
NENHUM
Totó rosa
comm.
43 Apogon pseudomaculatus Apogon, Apogon de duas manchas, Gordinho, Leopoldina, Totó
Totó leopoldina
Begossi & Figueiredo
(1995)
44 Apogon quadrisquamatus NENHUM
Totó dourado
comm.
45 Apogon robbyi
NENHUM
Totó listrado
46 Archosargus
probatocephalus
47 Archosargus
rhomboidalis
Sargento, Sargo, Sargo de dente, Sargo do mar, Sorgo
Sargo de dente
comm.
Nomura (1984)
48 Ariosoma balearicum
49 Ariosoma
opistophthalmus
50 Arothron firmamentum
Caicanha, Canhanha, Caranha, Frade, Guatucupajuba, Mercador, Canhanha
Salema, Salema branca, Salema da pedra, Salema feiticeira, Sambuio,
Sambulho, Sargo, Sargo de dente, Choupa, Canhanda, Frade,
Mercador, Guatucupa-Juba
NENHUM
Congro das baleares
Nomura (1984)
NENHUM
Congrinho olhão
NENHUM
Baiacu de estrela
comm.
comm.
comm.
comm.
Barletta (2002)*
51 Astrapogon puncticulatus Apogon bangai
Totó pintadinho
52 Astrapogon stellatus
NENHUM
Totó de concha
53 Astroscopus y-graecum
Aniquim, Bacalhau, Mira céu, Miracéu, Pomboca, Tanduju
Pomboca
54 Atherinella blackburni
Mamarreis, Papa boba
Papa boba
55 Atherinella brasiliensis
Charuto, João duro, Mamarreis, Manjuba, Manjuba verde, Papa boba, Manjuba verde
Peixe rei, Peixe reis, Piaba dura, Piquitinga, Pititinga, Varapau
Sanches (1989)
Sampaio & Nottingham
(2008)
105
Nº SPECIES
Nº SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
56 Atherinomorus stipes
Mamarreis
Mamarreis cabeçuda
Mod. from Szpilman
(2000)
57 Aulostomus strigosus
Peixe trombeta, Peixe trompete
Corneta
58 Auxis rochei
Bonito, Bonito cachorro, Cavala
Bonito cachorro
comm.
Szpilman (2000)
59 Balistes capriscus
Acará fuso, Acará mocó, Acaramuçu, Acarapicu, Acarapucu, Peixe porco verdadeiro
Cangulo, Cangulo branco, Cangulo da parede, Cangulo de Fernando,
Cangulo papo amarelo, Cangurro, Capado, Capão, Fantasma,
Maracuguara, Peixe porco, Peroá, Peroatinga, Perua, Peruá, Pirá acá,
Piraaca, Piruá, Porco, Porquinho
Mod. from Nomura
(1984)
60 Balistes vetula
Cangulo, Cangulo do alto, Cangulo fernande, Cangulo papo amarelo, Cangulo rei
Cangulo real, Cangulo rei, Cangulo verdadeiro, Cangurro, Capado,
Capão, Gatilho rainha, Lírio, Peixe gatilho, Peixe porco, Peroá, Peruá,
Piruá, Vetula
(2008)
61 Barbulifer ceuthoecus
Peixe ventosa, Pregador
Rangel & CarvalhoFilho, pers. comm.
comm.
comm.
Ventosa barbuda
62 Bascanichthys paulensis NENHUM
Miroró paulista
63 Bathygobius mystacium NENHUM
Amoré baiano
Aimoré, Amboré, Amborê, Amoré, Amorê, Amoré guaçu, Amoreia, Amoré de buzo
Amoréia, Aramaré, Babosa, Candunga, Cunduda, Emborê, Florete,
Imborê, Macaco, Maiuíra, Maria da toca, Moré, Moré de buzo, Moré
garoupa, Moré preto, Moreia, Moréia, Mucurungo, Muçurungo, Muré,
Mussurungo, Peixe capim, Peixe flor, Peixe macaco, Tajacica
65 Bodianus insularis
Bodião, Bodião oceânico
66 Bodianus pulchellus
Bodião, Bodião do fundo, Bodião vermelho, Budião, Budião arara, Budião fogueira
Budião batata, Budião branco, Budião vermelho, Budião fogueira,
Gudião, Papagaio, Pitubeiro, Pulchelus
Budião oceânico
Mod. from Lima &
Oliveira (1978)
(2008)
Begossi & Figueiredo
(1995)
64 Bathygobius soporator
106
67 Bodianus rufus
Bigodeiro, Bodião, Bodião azul, Bodião judite, Bodião papagaio, Budião, Budião papagaio
Budião batata, Budião papagaio, Budião rufus, Gudião, Papagaio,
verdadeiro
Paratucaro, Pretucano, Rufus
68 Boridia grossidens
69 Bothus lunatus
Cocoroca sargo, Corcoroca, Corcoroca sargo, Peixe pedra, Roncador, Cocoroca sargo
Sargo, Sargo de beiço
Linguadinho pavão, Linguado, Linguado ocelado, Solha, Tapa
Linguadinho pavão
70 Bothus maculiferus
NENHUM
71 Bothus ocellatus
72 Bothus robinsi
Aramaçá, Aramaçã, Linguadinho ocelado, Linguado, Linguado arco-íris, Linguado arco íris
Maraçapeba, Sôia, Solha, Tapa
Solha duas pintas
Linguado, Solha
73 Brotula barbata
NENHUM
Brótula barbuda
74 Bryx dunckeri
Peixe cachimbo
75 Calamus bajonado
Pargo pena, Pena salgo
Peixe cachimbo de
nariz curto
Pena salgo
Nomura (1984)
76 Calamus calamus
Peixe pena, Salgo
Peixe pena olhão
Mod. from Suzuki (1986)
77 Calamus mu
Pargo pena, Peixe pena
Peixe pena brasileiro Mod. from Nomura (1984)
78 Calamus penna
79 Calamus pennatula
Caratinga, Pampo pena, Pargo, Pargo pena, Peixe pena, Pena, Pena Peixe pena branco
branco
Pargo pena, Peixe pena, Pena
Peixe pena amarelo
80 Callechelys bilinearis
NENHUM
Miroró de duas listras FishBase****
81 Callionymus bairdi
Peixe pau, Dragãozinho
Dragãozinho
Cangulo das índias
83 Cantherhines
macrocerus
84 Cantherhines pullus
Solha manchada
Cangulo, Macrocerus, Peixe porco, Peixe porco de pintas brancas, Porco Porquinho pintado
pintado, Porquinho pintado
Cangulho velho, Cangulo, Cangulo bastardo, Cangulo da pedra, Cangulo Cangulo de pedra
de pedra, Cangulo Fernando, Cangulo pavão, Peixe porco, Peixe porco de
pintas laranjas, Porco pintado, Pullus
Sampaio & Nottingham (2008)
Mod. from FishBase
Mod. from Soares (1988)
Mod from Nomura (1984)
Carvalho & Branco (1977)
107
COMMON NAMES
82 Cantherhines dumerili NENHUM
UNIQUE NAME
SOURCE
Nº SPECIES
Nº SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
85 Canthidermis maculata
NENHUM
Cangulo oceânico
pintado
FishBase
86 Canthidermis sufflamen
Peixe porco, Peroá do alto
Peroá do alto
Sampaio, pers. comm.
87 Canthigaster figueiredoi Baiacu, Baiacu de recife, Cantigaster
Baiacu de recife mirim Mod. from IBAMA Inst.
Normativa 14/2004
88 Caralophia loxochila
NENHUM
Miroró ilhéu
89 Carangoides
bartholomaei
Carapau, Garajuba, Guaraiúba, Guarajuba, Xarelete amarelo, Xarelete Xarelete amarelo
azul, Xaréu, Xaréu amarelo, Xerelete amarelo
90 Carangoides crysos
Carapau, Cavaca, Cavaco, Chumberga, Garaçuma, Garajuba, Garajuba Carapau verdadeiro
preta, Garujuba, Graçainha, Guaracema, Guaracu, Guaraçu, Guaraçuma,
Guarainha, Guarajuba, Guarassuma, Guaraxuma, Guaricema, Manezinho,
Solteira, Taguara, Xalerete, Xarelete, Xaréu, Xaréu amarelo, Xaréu
branco, Xaréu dourado, Xaréu pequeno, Xaréu xixá, Xerelete, Xereleté,
Xererete, Xixarro, Xixarro pintado, Xumberga
91 Carangoides ruber
Algodão, Carapau, Garajuba, Guaricema, Guaricema branca, Xarelete Xarelete azul
azul
Aracimbora, Cabeçudo, Carango, Cáranx, Carimbamba, Cavala, Xaréu verdadeiro
Corimbamba, Durão, Guaracema, Guaracimbora, Guaricema, Guiará,
Guiaru, Manezinho, Olhudo, Papaterra, Xarelete, Xaréu, Xaréu branco,
Xaréu cabeçudo, Xaréu preto, Xaréu roncador, Xaréu vaqueiro, Xaréu
verdadeiro, Xarso, Xerelete, Xeréu, Xexém
93 Caranx latus
Arachimbóia, Aracimbora, Araximbora, Carapau, Caraximbora, Guarajuba
Garacimbora,
Garaximbora,
Graçaim,
Graçarim,
Guaracema,
Guaracimbora, Guaraiúba, Guarajuba, Guarambá, Guarassuma,
Guaraximbora, Guaricema, Olhudo, Xarelete, Xaréu, Xaréu graçarim,
Xaréu olhudo, Xaréu preto, Xaréu xaralete, Xaréu xixá, Xerelete, Xixarro
Nomura (1984)
94 Caranx lugubris
Ferreiro, Fumeiro, Pargo ferreiro, Xarelete, Xaréu branco, Xaréu cabeça Xaréu preto
preta, Xaréu preto, Xeréu preto
Nomura (1984)
92 Caranx hippos
108
comm.
Rocha & Costa (1999)
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
95
Carapus bermudensis
Sarapó, Tira faca
Sarapó de pepino
Mod. from Szpilman
(2000)
96
Carcharhinus acronotus
Cação, Cação lombo preto, Corta garoupa, Lombo preto, Cação de Cação de focinho preto Carvalho-Filho, pers.
comm.
focinho preto, Cação flamengo, Marracho
97
Carcharhinus brevipinna Cação, Cação agulha preta, Cação galha preta, Galha preta, Machote, Galha preta
Serra garoupa, Sucuri de ponta petra
98
Carcharhinus falciformis Cação, Cação de cima d'água, Cação lombo preto, Cação seda, Lombo preto
Focinhudo, Lombo preto, Negrinho, Tubarão de lombo preto
comm.
99
Carcharhinus
galapagensis
comm.
100 Carcharhinus leucas
Cabeça chata, Cação, Cação baiacu, Cação branco, Cação de rio, Cabeça chata
Cação do raso, Cação fidalgo, Cação flamengo, Pirarara, Sicuri
branco, Tubarão, Tubarão de água doce, Tubarão touro
Nomura (1984)
101 Carcharhinus limbatus
Cação, Cação de fundo, Cação do fundo, Cação galha preta, Cação Serra garoupa
peru, Cação ponta preta, Cação sicuri, Corta garoupa, Galha preta,
Machote, Serra garoupa, Sicuri, Sicuri de galha preta, Sicuri de ponta
preta, Sucuri da galha preta, Tubarão galha preta
Nomura (1984)
102 Carcharhinus longimanus Estrangeiro, Galha branca
Galha branca
Nomura (1984)
103 Carcharhinus perezi
Bico fino, Cabeça chata, Cação, Cação da pedra, Cação coralino, Olho Olho branco
branco, Tubarão caribenho, Tubarão dos corais, Tubarão dos recifes
comm.
104 Carcharhinus signatus
Cação noturno
Szpilman (2000)
105 Carcharias taurus
Cação da areia, Cação de areia, Cação galhudo, Cação macho, Cação Mangona
magonga, Caçoa, Magonga
Suzuki (1986)
106 Caulolatilus chrysops
Batata, Batata da pedra, Michola, Peixe batata
Nomura (1984)
107 Centropomus ensiferus
Camorim cabo de machado, Camorim espora, Camorim peba, Robalo branco
Camorim sovela, Camuri, Camurim, Camurim branco, Camurim
sovela, Camuripeba, Robalete, Robalito, Robalo, Robalo corcunda,
Robalo espora, Robalo galhudo
Cação noturno
Batata da pedra
Mod. from Lima &
Oliveira (1978)
109
Cação baia, Cação do alto, Cação de fora, Tubarão do alto, Tubarão Cação do alto
dos Galápagos, Cabeça de cesto
Nº SPECIES
COMMON NAMES
108 Centropomus mexicanus Robalo
UNIQUE NAME
SOURCE
Robalo de escama grande Carvalho-Filho (1999)
109 Centropomus parallelus Cambriaçu, Camburiapeva, Camorim corcunda, Camorim peba, Robalo peba
Camorim pena, Camorim tapa, Camuri, Camurim, Camurim amarelo,
Camurim apuá, Camurim branco, Camurim corcunda, Camurim peva,
Camuripeba, Camurupeba, Cangoropeba, Cangurupeba, Robalo,
Robalo peba, Robalo peva
110 Centropomus
Bicudo, Cambriaçu, Camburiaçu, Camorim, Camorim açu, Camuri, Robalo verdadeiro
undecimalis
Camurim, Camurim açu, Camurim açú, Camurim branco, Camurim
cabo de machado, Camurim preto, Camurimpema, Camuripeba,
Camuripema, Cangoropeba, Canjurupeba, Escalho, Robalão, Robalo,
Robalo bicudo, Robalo branco, Robalo camurim, Robalo de galha,
Robalo estoque, Robalo flecha, Robalo flexa, Rolão
Suzuki (1986)
111 Centropyge aurantanota Centropige, Centropige dorso de fogo
Mod. from IBAMA Inst.
Normativa 14/2004
Nomura (1984)
Anjo dorso de fogo
Carvalho & Branco
(1977)
112 Cephalopholis fulva
Caraúna, Catoá, Catuá, Garoupa, Garoupa chita, Garoupa diamante, Piraúna
Garoupa pintada da Bahia, Garoupinha, Garoupinha vermelha, Jabu,
Jabú, Pirauna, Piraúna, Praúna
113 Cerdale fasciata
NENHUM
114 Chaetodipterus faber
Enxada, Paru, Parú, Paru branco, Parú enxada, Paru jandaia, Paru Enxada
preto, Parum, Parum branco, Parum enxada, Parum rajado, Peixe
enxada, Tareira
Nomura (1984)
115 Chaetodon ocellatus
Beija moça, Bicudinha, Bicudo, Borboleta, Borboleta amarelo, Borboleta ocelado
Borboleta ocelado, Caco de prato, Jandaia, Namorado, Parum
amarelo, Parum bicudo, Saberé, Viuvinha
(2008)
116 Chaetodon sedentarius
Bicudo, Borboleta, Borboleta dos recifes, Borboleta namorada, Moca, Borboleta namorada
Namorado bicudo, Sedentarius
Beijo de moça, Boca de moça, Borboleta, Borboleta listrada, Borboleta listrada
Borboleta listrado, Carapiaçaba, Castanhola, Freire, Paru, Paru
mulato, Parum, Peixe borboleta, Quebra prato, Striatus, Tinhuna frade
Peixe lombriga listrado
comm.
117 Chaetodon striatus
110
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
118
Channomuraena vittata
Caramuru malha de jibóia
Caramuru malha de jibóia Sampaio & Nottingham
(2008)
119
Cheilopogon cyanopterus Peixe voador, Voador, Voador de fernando, Voador holandês
120
Cheilopogon exsiliens
121
Cheilopogon melanurus
122
123
124
NENHUM
SOURCE
Voador de fernando
Nomura (1984)
Voador de asa listrada
FishBase
125
Chilomycterus spinosus
NENHUM
Baiacu espinho comum
comm.
126
Chilorhinus suensonii
Cobrinha, Congro mirim
Congro mirim
127
Chloroscombrus
chrysurus
Arriba saia, Caico, Caracaxá, Carapau, Favinha, Favoleta, Folha, Palombeta
Folha de mangue, Garapau, Juva, Juvá, Palombeta, Palometa,
Pilombeta, Polombeta, Saia rôta, Vento leste
128
Chromis enchrysura
NENHUM
Donzela de rabo amarelo FishBase
129
Chromis flavicauda
Donzela, Donzela rabo amarelo
Donzela cobalto
Mod. from Szpilman
(2000 )
130
Chromis jubauna
NENHUM
Donzela jubauna
131
Chromis multilineata
Chromis, Cromis, Cromis tesoura, Donzela, Donzela marrom
Mulata
comm.
132
Chromis scotti
NENHUM
Donzela roxa
FishBase
133
Citharichthys arenaceus
Linguado, Solha
Linguado de areia costeiro Freire, pers. comm.
111
Peixe voador, Pirabebe, Tainhota, Tainhota voadeira, Voador, Voador preto
comm.
Voador cascudo, Voador do alto
Chilomycterus antennatus Baiacu espinho, Baiacu espinho antenado
Baiacu espinho antenado Sampaio & Nottingham
(2008)
Chilomycterus antillarum Baiacu de espinho, baiacu espinho rendado
Baiacu espinho rendado Sampaio & Nottingham
(2008)
Chilomycterus reticulatus Baiacu de espinho
Baiacu espinho pintado Carvalho-Filho, pers.
comm.
Nº SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
134 Citharichthys macrops
Linguado
Linguado onça
135 Clepticus brasiliensis
Clepticus brasileiro, Budião fantasma, Peixe fantasma
Budião fantasma
(2008)
136 Conger orbignyanus
Cobra do mar, Côngrio, Congro, Congro preto, Congro verdadeiro, Congro preto
Enguia
Univali (2004)
137 Conger triporiceps
Congro dentão
Szpilman (2000)
138 Cookeolus japonicus
Cassumba de mero, Olho de boi, Olho de cão, Olho de vidro, Olho de vidro
Piranema do fundo
139 Corniger spinosus
Mariquita vovó, Olho de vidro, Talhão, Vovó
Talhão
Nomura (1984)
140 Coryphaena equiselis
Dourado, Dourado de Santo Antônio, Dourado palombeta
Dourado palombeta
Szpilman (2000)
141 Coryphaena hippurus
142 Coryphopterus dicrus
Dalfinho, Dourado, Dourado de alto mar, Dourado do mar, Dourado
Graçapé, Grassapé, Guaraçapé, Guaraçapema, Macaco, Peixe
tábua, Sapé
Amoré dois pontos
NENHUM
143 Coryphopterus eidolon
NENHUM
Amoré pálido
Rangel, pers. comm.
144 Coryphopterus
glaucofraenum
Gobi de areia, Gobi de vidro, Gobião de freio, Maria da toca
Amoré vidro
Mod. from Sampaio &
Nottingham (2008)
145 Coryphopterus thrix
NENHUM
Amoré pintado
Rangel, pers. comm.
146 Cosmocampus albirostris
Cachimbo, Peixe cachimbo, Peixe cachimbo de focinho branco
147 Cryptotomus roseus
Batata, Bodião batata, Budião
Peixe cachimbo de
focinho branco
Periquito
(2008)
148 Ctenogobius boleosoma
Maria da toca, Rondom, Amoré de garça
Amoré de garça
149 Ctenogobius saepepallens NENHUM
Amoré vírgula
150 Ctenogobius stigmaticus
Amoré rondom
Rangel & Carvalho-Filho,
pers. comm.
Mod. from Lima & Oliveira
(1978)
Nomura (1984)
Rangel, pers. comm.
Amoré, Rondom
Congro dentão
112
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
151
Cyclopsetta chittendeni
Linguado, Linguado mexicano, Linguado pintado, Rodovalho
Linguado pintado
152
Cyclopsetta fimbriata
Linguado, Tapa
FishBase
153
Cypselurus comatus
Voador holandês
Linguado de nadadeira
pintada
Voador holandês
154
Dactylopterus volitans
155
Dactyloscopus crossotus
Cabra bode, Cajaleó, Cajaléu, Coió, Falso voador, Peixe Coió
Nomura (1984)
voador, Pirabebe, Pirapebebe, Voador, Voador cascudo, Voador
coió, Voador das pedras, Voador de fundo, Voador de pedra,
Voador de pedras, Voador Santo Antônio
NENHUM
Miracéu de olho grande FishBase
156
Dactyloscopus foraminosus NENHUM
Miracéu malhado
157
Dactyloscopus tridigittatus Tanduju mirim
Miracéu de areia
158
Dasyatis americana
159
Dasyatis centroura
160
Dasyatis guttata
161
Dasyatis hipostigma
Arraia, Raia, Raia cravadora, Raia lixa, Raia manteiga, Raia Aiereba
prego, Aiereba, Arraia branca, Arraia de prato, Arraia
Aireba, Arraia, Arraia prego, Raia, Raia manteiga, Raia prego Raia prego de cauda
áspera
Arraia, Arraia bico de remo, Arraia bicuda, Arraia branca, Raia branca
Arraia lixa, Jabebiretê, Jabiretê, Raia, Raia branca, Raia lixa,
Raia lixo, Raia prego
NENHUM
Raia manteiga lisa
162
Dasyatis marianae
Arraia de prato, Raia mariquita
163
Decapterus macarellus
Carapau, Cavalinha, Cavalinha de reis, Cavalinha do reis, Chicharro alamarim
Chicharro, Chicharro alamarim, Chicharro calabar, Chicharro
cavala, Garapau, Xixarro, Xixarro branco, Xixarro calabar,
Xixarro cavala
Carvalho & Branco
(1977)
164
Decapterus punctatus
Mod. from CarvalhoFilho (1999)
165
Decapterus tabl
Carapau, Chicharro, Chicharro branco, Chicharro de olho Chicharro pintado
grande, Chicharro pintado, Peixe rei, Xixarro, Xixarro branco,
Xixarro de olho grande, Xixarro pintado
Chicharro roliço
Xixarro roliço
Raia mariquita
Szpilman (2000)
comm.
comm.
Freire, pers. comm.
Nomura (1984)
Ciência Hoje
Gomes et al. (2000)
Mod. from Sampaio,
pers. comm.
113
Nº
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
166
Decodon puellaris
Ministro
Ministro
Sampaio, pers. comm.
167
Dermatolepis inermis
Garoupa gostosa, Gostosa, Piranema, Piranema pintado, Sapé da Piranema pintada
pedra
Nomura (1984)
168
Diapterus auratus
Carapeba, Carapeba branca, Carapeva, Carapicu, Caratinga, Peixe Carapeba branca
prata, Tinga
Nomura (1984)
169
Diapterus rhombeus
Acarapeba, Acarapeva, Carapeba, Carapeba branca, Carapeva, Caratingaitê
Caratinga, Caratingaitê, Peixe prata
Barletta (2002)
170
Diodon holocanthus
171
Diodon hystrix
(2008)
Nomura (1984)
172
Diplectrum bivittatum
Baiacu, Baiacu de espinho, Baicu espinho, Baiacu espinho Baiacu espinho
manchado, Peixe ouriço
manchado
Baiacu de espinho, Baiacu espinho pintalgado, Baiacu graviola, Baiacu graviola
Graviola, Peixe ouriço
Michole de areia anão
Jacundá, Michole da areia
173
Diplectrum formosum
Canguito, Jacundá, Margarida, Michole, Michole da areia, Michole Michole de areia listrado Sampaio & Nottingham
(2008)
de areia, Michole de areia listrado, Michóli, Mixole, Mixole da
areia, Mixole de areia
174
Diplectrum radiale
Jacundá, Margarida, Michole, Michóle, Michole da areia, Michole Michole aipim
de areia, Michole de areia costeiro, Mixole, Mixole da pedra, Papa
terra, Peixe aipim
175
Diplobatis picta
NENHUM
176
Diplodus argenteus
Chinelão, Maímbá, Maria chinelo, Marimbá, Marimbá chinelo, Marimbá
Marimbau, Pargo branco, Pinta no cabo, Sargo
Nomura (1984)
177
Doratonotus megalepis
Budião, Gudião, Folha verde, Peixe dragão, Sabonete anão
Folha verde
178
Dules auriga
Jacundá, Mariquita, Mariquita de penacho, Vovó
Mariquita de penacho
Mod. from Sampaio &
Nottingham (2008)
179
Echeneis naucrates
Agarrador, Pegador, Peixe pegador, Peixe piolho, Piolho, Piolho de Pegador listrado
cação, Piolho de tubarão, Piraquiba, Rêmora, Rêmora de listra
Mod. from Nomura
(1984)
180
Echidna catenata
Camuflada, Caramuru de listra, Moréia, Moréia listada, Moréia Moréia zebra
zebra
Freire, pers. comm.
Raia elétrica pintada
114
Mod. from Ferreira
(1999)
Freire, pers. comm.
FishBase
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
181
Echiopsis intertinctus
Cobra pintada, Congro, Enguia, Miroró, Moréia
Miroró leopardo
182
Echiophis punctifer
NENHUM
Miroró sarampo
Mod. from Carvalho-Filho
(1999)
183
Elacatinus figaro
Néon, Neon goby
Amoré neon
(1999)
184
Elacatinus pridisi
NENHUM
Neón de trindade
Rangel, pers. comm.
185
Elacatinus phthripophagus NENHUM
Neón de Noronha
186
Elagatis bipinnulata
Arabaiana, Arabaiana azul, Arabaiana norte, Camisa de meia, Arabaiana azul
Enxova, Guaxum, Guaxumba, Olhete, Peixe rei, Xixarro salmão
187
Elops saurus
Albarana, Barana, Baranda, Obarana, Oiá, Robalo da pedra, Ubarana
Tijubarana, Tubarana, Ubarama, Ubarana, Ubarana açu,
Ubarana cabo de machado, Ubaranaçu, Urubaiana, Urubaiana
pau, Urubaiana verdadeira, Urubarana
Nomura (1984)
188
Emblemaria australis
NENHUM
Macaquinho do
cascalho
189
Emblemariopsis
occidentalis
NENHUM
Macaquinho bandeira
FishBase
190
Emblemariopsis signifera
Cabeça preta, Macaquinho
Macaquinho cabeça
preta
(1999)
191
Emmelichthys ruber
NENHUM
Chicharro vermelho
192
Enchelycore anatina
Caramuru cachorro, Caramuru de dente, Moréia, Moréia Moréia víbora
cachorro, Moréia de dente
193
Enchelycore carychroa
Caramuru cachorro, Caramuru preto, Caramuru vinagre, Moréia vinagre
Moréia, Moréia cachorro, Moréia negra, Moréia vampiro
194
Enchelycore nigricans
Caramuru cachorro, Caramuru de dente, Caramuru preto, Moréia cachorro
Caramuru vinagre, Moréia, Moréia negra, Moréia cachorro,
Moréia vampiro, Moréia vinagre
195
Enneanectes altivelis
NENHUM
Macaquinho parati
115
Nº
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
196
Enneanectes smithi
NENHUM
Macaquinho dos
penedos
Carvalho-Filho & Freire,
pers. comm.
197
Entomacrodus vomerinus
Macaco pérola
Macaco pérola
198
Epinephelus adscensionis
199
Epinephelus flavolimbatus
Badejo, Badejo pintado, Garoupa chita, Garoupa gato, Garoupa Garoupa gato
pintada, Gato, Mero gato, Peixe gato, Piragica, Pirapiranga
Cherne, Cherne amarelo, Cherne claro, Cherne galha amarela
Cherne galha amarela Cepene (2000)
200
Epinephelus itajara
201
Epinephelus marginatus
202
Epinephelus morio
Garoupa, Garoupa bichada, Garoupa de São Tomé, Garoupa de Garoupa São Tomé
segunda, Garoupa São Tomé, Garoupa verdadeira, Garoupa
vermelha, Garoupa vermelha de abrolhos, Garoupa vermelha dos
Abrolhos, Piragia
Suzuki (1986)
203
Epinephelus mystacinus
Cherne escuro, Cherne listrado, Piraroba
204
Epinephelus nigritus
205
Epinephelus niveatus
Cherne, Cherne negro, Cherne queimado, Chernete, Chernote, Cherne queimado
Garoupa, Mero, Mero negro, Mero preto, Piraroba, Serigado
h
Badejo branco, Cerigado cherne, Cerigado tapoã, Cherna, Cherna Cherne claro
preta, Cherna preto, Cherne, Cherne claro, Cherne pintado, Cherne
tapoan, Cherne verdadeiro, Chernete, Chernote, Garoupa, Mero
preto, Serigado cherne, Serigado tapoan, Xerne
206
Equetus lanceolatus
Bacalhau, Bilro, Cabeça de coco, Cavaleiro de bandoleira, Bilro listrado
Equetos, Maria nagô, Maria negra
comm.
207
Equetus punctatus
Bacalhau
Bilro pintado
208
Eucinostomus argenteus
Carapeba, Carapicu, Carapicú, Carapicu pena, Carapipiacuaçu, Carapicu pena
Escrivão
comm.
Nomura (1984)
Canapu, Canapú, Canapu guaçu, Canapuguaçu, Cunapu guaçu, Mero verdadeiro
Merete, Mero, Mero canapu, Mero canapum, Mero preto, Merote,
Mirete, Nero
Galinha do mar, Garoupa, Garoupa barriga amarela, Garoupa Garoupa verdadeira
crioula, Garoupa preta, Garoupa verdadeira, Piracuca
Cherne listrado
116
Carvalho & Branco
(1977)
Nomura (1984)
Nº
SPECIES
209 Eucinostomus gula
COMMON NAMES
UNIQUE NAME
Acarapicu, Cacundo, Carapau, Carapeba, Carapicu, Carapicu açu, Carapicu branco
Carapicu branco, Carapicu sem dente, Carapicupeba, Carapim,
Carataí, Escrivão, Primituma, Riscador
SOURCE
Ferreira (1999)
210 Eucinostomus harengulus Carapicu açu
Carapicu açu
Suzuki (1986)
211 Eucinostomus lefroyi
Carapicu, Carapim
Carapicu manchado
212 Eucinostomus
melanopterus
Cacundo, Carapeba, Carapicu, Carapicu açu, Carapicu branco, Carapicu bandeira
Escrivão, Riscador
213 Eugerres brasilianus
Acará tinga, Carapeba, Carapeba branca, Carapeba de lista, Caratinga vivóca
Carapeba de listra, Carapeba listada, Carapeba listrada, Carapeba
rajada, Carapeva, Carapitanga, Carapitinga, Caratinga, Caratinga
i ó
Albacora, Bonito, Bonito cachorro, Bonito pintado, Bonito rajado, Bonito pintado
Curuatá pinima, Merma
Barletta (2002)
214 Euthynnus alleteratus
Cajaleo, Cajaleó, Coió, Holandês, Peixe voador, Pirabebe, Santo Voador verdadeiro
Antônio, Tainhota, Voador, Voador cascudo, Voador de pedra,
Voador do fundo, Voador verdadeiro
216 Fistularia petimba
Agulhão trombeta, Timbáli, Trombeta
217 Fistularia tabacaria
Agulhão trombeta, Agulheta, Cachimbau, Cachimbo, Catimbau, Cachimbau azul
Peixe cachimbo, Peixe corneta, Peixe trombeta, Petimbo,
Petimbuaba, Trombeta, Trombeta pintada
Cação, Cação cabeça chata, Cação jaguara, Cação jaguará, Cação Tubarão tigre
tigre, Cação tintureiro, Gata, Gatinha, Jaguara, Jaguará, Tigre,
Tintureira, Tintureiro, Tubarão tigre, Tubarão tintureira
Bagre, Bagre amarelo, Bagre branco, Bagre curiaçu, Bagre de Bagre urutu
manta, Bagre do Natal, Bagre guri, Bagre guriaçu, Bagre guru,
Bagre leilão, Bagre mandi, Bagre mandim, Bagre pararê, Bagre
urutu, Bagre veludo, Beiçudo, Cabeçote, Guriaçu, Pareré
218 Galeocerdo cuvier
219 Genidens genidens
Nomura (1984)
Brandão (1964)
Cachimbau vermelho Carvalho-Filho, pers. comm.
Suzuki (1986)
Nomura (1984)
220 Gerres cinereus
Carapeba, Carapicu açú
Carapicu listrado
221 Gillellus greyae
NENHUM
Miracéu seta
FishBase
117
215 Exocoetus volitans
225
Gobiesox punctulatus
NENHUM
Peixe ventosa pintado
Freire, pers. comm.
226
Gobiosoma
hemigymnum
Amboré zebra
Amoré zebra
(1999)
227
Gobiosoma nudum
NENHUM
Amoré mirim
228
Gobulus myersi
NENHUM
Amoré de dorso pálido
FishBase
229
Gonioplectrus hispanus Bandeira espanhola, Jabu do fundo
Bandeira espanhola
230
Gramma brasiliensis
Grama, Camarolete
Camarolete
231
Gymnachirus nudus
Aramaçã, Linguado zebra, Solha, Solha zebra
Aramaçá zebra
232
Gymnothorax funebris
233
Gymnothorax miliaris
234
Gymnothorax moringa
Amoréia verde, Camburú marrom, Caramuru, Caramuru verde, Moréia verde
Moréia, Moréia verde
Caramuru banana, Caramuru bombóia, Caramuru dourado, Moréia banana
Caramuru jibóia, Caramuru mulato, Caramuru pinima, Moréia,
Moréia amarela, Moréia banana, Moréia de rabo amarelo, Moréia
dourada, Moréia rabo dourado
Aimoré, Amoréia pintada, Camburú pintado, Caramuru, Caramuru Moréia pintada
pinima, Caramuru pintado, Enguia, Miroró, Moréia, Moréia
americana, Moréia pintada, Moréia verde, Morongo, Mororó,
Mussulina, Mutuca, Mututuca, Sangrador, Tororó, Totoró
235
Gymnothorax ocellatus Amoréia, Amorepinima, Caramuru, Caramuru de areia, Caramuru Moréia de areia
pinima, Miroró, Moréia, Moréia amarela, Moréia de areia, Moréia
de pedra, Moréia ocelada, Moréia pintada, Mutuca, Mututuca
118
SOURCE
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
Nomura (1984)
222 Ginglymostoma
Barroso, Cação arumaru, Cação lixa, Lambaru, Lixa, Peixe anjo,
Cação lixa
cirratum
Tubarão enfermeira, Tubarão lixa, Tubarão pajem, Urumaru, Gata,
Cação-Arumaru, Urumaru, Uaromaru.
FishBase
223 Gnatholepis thompsoni NENHUM
Amoré de mancha
dourada
Limpa vidro, Peixe ventosa, Pregador
224 Gobiesox barbatulus
Peixe ventosa de bigode Carvalho-Filho, pers. comm.
Suzuki (1986)
COMMON NAMES
UNIQUE NAME
SOURCE
Moréia bombóia
comm.
SPECIES
236
Gymnothorax polygonius NENHUM
237
Gymnothorax vicinus
Caramuru, Caramuru mulato, Caramuru pinima, Moréia, Moréia Moréia preta
amarela, Moréia boca preta, Moréia preta
comm.
238
Gymnura altavela
Arraia, Arraia borboleta, Arraia manteiga, Arraia parati, Borboleta, Raia borboleta de
espinho
Raia, Raia amarela, Raia borboleta, Raia gererera, Raia manteiga
Mod. from Carvalho
(1999)
239
Gymnura micrura
Arraia, Arraia baté, Arraia borboleta, Arraia caã, Arraia comum, Raia borboleta lisa
Arraia manteiga, Borboleta, Carapiaçava, Raia borboleta, Raia
manteiga, Raia mariquita, Raia olho de ovelha, Raia olhuda
Mod. from Nomura
(1984)
240
Haemulon album
Arrebenta panela, Cocoroca branca, Corcoroca, Pirambu
241
Haemulon aurolineatum
Corcoroca, Cotinga, Quatinga, Sapuruna, Sapuruna branca, Xira, Xira dourada
Xira branca, Xira dourada
242
Haemulon
chrysargyreum
Cocoroca boquinha
Szpilman (2000)
243
Haemulon melanurum
244
Haemulon parra
Sapurana, Sapurana de lista, Sapuruna preta, Supuruna de listra, Sapuruna preta
Xirão
Biquara, Cambuba, Cancan, Cancanhe, Carrapato, Cocoroca, Cancanhe
Cocoroca mulata, Corcoroca mulata, Macassa, Negramina,
Pirambu, Pirambú, Xira branca
245
Haemulon plumieri
Abiquara, Biquara, Boca de fogo, Boca de velha, Cambuba, Cocoroca boca velha
Capiúma, Capiúna, Cocoroca, Cocoroca mulata, Corcoroca,
Corcoroca boca de velha, Corcoroca mulata, Corocoroca,
Corocoroca boca de fogo, Corocoroca mulata, Crocoroca, Macaca,
Negra mina, Negramina, Pirambu, Sapuruna, Uribaco, Xira
246
Haemulon squamipinna
Quatinga amarela, Xira, Xira amarela
247
Haemulon steindachneri Cambuba, Carrapato, Cocoroca boca larga, Corcoroca boca de Cocoroca boca larga
fogo, Corcoroca boca larga, Corcoroca de boca larga, Corcoroca
sargo, Farofa, Macassa, Macasso, Quatinga, Xirão
Cocoroca branca
Cocoroca boquinha
Xira amarela
Szpilman (2000)
Ferreira & Cava (2001)
Szpilman (2000)
119
Nº
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
248
Haemulon striatum
Cocoroca listrada, Xira
Cocoroca listrada
Szpilman (2000)
249
Halichoeres bathiphillus Budião de Fundo
Budião de fundo
250
Halichoeres bivittatus
Budião, Gudião vermelho, Punheta, Sabonete listrado
Budião sabonete
251
Halichoeres
brasiliensis
Budião azul, Budião sipica, Budião verde, Mangarueira, Radiatus, Budião verde
Sabonete brasileiro
252
Halichoeres dimidiatus
253
Halichoeres penrosei
Budião papagaio, Budião azul, Bodião dourado, Cianocéfalo, Budião azul
Ministro, Peixe rei, Sabonete cara amarela brasileiro
Budião ocelado
Budião, Maculipina, Mangarueira, Sabonete ocelado
254
Halichoeres poeyi
255
Mod. from Sampaio &
Nottingham (2008)
Halichoeres radiatus
Bindalo, Bodião, Bodião rei, Budião, Budião puxê, Budião verde, Budião puxê
Gudião, Peixe rei, Poei, Poei verde, Punheta, Sabonete verde,
Verdugo
Bindalo, Bodião bindaló
Budião bindalo
256
Halieuticthys aculeatus
NENHUM
257
Harengula clupeola
258
Harengula jaguana
Sardinha, Sardinha casca dura, Sardinha cascuda, Sardinha lage, Sardinha lage
Savelha
Sardinha, Sardinha cascuda, Savelha cascuda
Sardinha cascuda
259
Hemicaranx
amblyrhynchus
Hemiramphus balao
Cabeça dura, Cabeçudo, Cara de gato, Catarro, Palombeta do alto, Vento leste
Vento leste, Vento leste do verão, Xixarro
Agulha, Agulhinha, Panaguaiú
Agulha azul
261
Hemiramphus
brasiliensis
Agulha, Agulha crioula, Agulha preta, Agulhinha, Farnangaio, Agulha preta
Farnangalho, Peixe agulha, Tarangalho
Nomura (1984)
262
Heteroconger
camelopardalis
Heteroconger
longissimus
NENHUM
Heteropriacanthus
cruentatus
Imperador, Olho de cão, Olho de cão das pedras, Olho de vidro, Olho de fogo
Olho de fogo, Piranema
260
264
NENHUM
Enguia de jardim
manchada
Enguia de jardim
marrom
Sazima et al. (in press)
Barletta (2002)
Nomura (1984)
Freire, pers. comm.
Anon. (1976)
263
Cacuá do alto
120
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
265
Himantura schmardae
NENHUM
Raia raspadora
Freire, pers. comm.
266
Hippocampus erectus
267
268
Hippocampus
patagonicus
Hippocampus reidi
269
Hirundichthys affinis
Cavalo marinho pintado Mod. from Nomura
(1984)
Cavalo marinho mirim Carvalho-Filho, pers.
NENHUM
comm.
Cavalinho, Cavalinho do mar, Cavalinho marinho, Cavalo marinho, Cavalo marinho de
Cavalo marinho de focinho longo
focinho longo
(2008)
Holandês, Peixe voador, Voador, Voador comum, Voador holandes
Voador comum
Brandão (1964)
270
Histrio histrio
Peixe doutor, Peixe pescador, Peixe sargaço
271
Holacanthus ciliaris
272
Holacanthus tricolor
Anjo rainha, Borboleta, Ciliaris, Enxada, Papu, Paru branco, Paru Peixe anjo rainha
rajado, Parum amarelo, Parum dourado, Parum jandaia, Peixe anjo,
Peixe anjo rainha, Peixe borboleta
Enxada, Paru de pedra, Paru fumaça, Paru papagaio, Paru soldado, Paru fumaça
Parum dourado, Parum jandaia, Peixe borboleta, Peixe soldado,
Soldado, Tambuatá, Tamuatá, Tricolor, Vigário
273
Holocentrus
adscensionis
Cachaça, Jaguaraçá, Jaguareça, Jaguareçá, Jaguarica, Jaguariça, Jaguareçá açú
Jaguariçá, Jaguaruça, Jaguaruçá, Jaguriçá, João cachaça, João guriçá,
Juguriçá, Mariquita, Mariquita olhão, Olho de vidro, Realito, Tararaca
Nomura (1984)
274
Holocentrus rufus
275
Hypleurochilus
fissicornis
Hypleurochilus
pseudoaequipinnis
Hyporhamphus roberti
Jaguareçá, Jaguariçá, Jaguariçá, Jaguaruçá, João cachaça, Juguriçá, Tararaca
Mariquita, Tararaca
Macaco de chifre
Macaco, Maria da toca
276
277
Cavalinho, Cavalinho do mar, Cavalo marinho, Hipocampo
Peixe sargasso
Carvalho & Freire, pers.
comm
(2008)
Carvalho & Branco
(1977)
NENHUM
Macaco ostra
comm.
comm.
Freire, pers. comm.
Agulha, Agulhinha, Panaguaiu, Panaguaiú
Agulha fina
FishBase
278
Hyporhamphus
unifasciatus
Agulha, Agulha branca, Farnangalho, Panaguaiú, Peixe agulha, Agulha branca
Tarangalho
279
Hypsoblennius
invemar
Macaquinho pavão, Sarampinho
Sarampinho
Nomura (1984)
comm.
121
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
280
Ichthyapus ophioneus
NENHUM
Enguia bicuda
281
Inermia vittata
NENHUM
Chicharro listrado
282
Istiophorus platypterus
Agulhão, Agulhão bandeira, Agulhão de vela, Agulhão vela, Agulhão vela
Bacho, Basho, Bicudo, Espadim azul, Guebo, Guebucu,
Guebuçu, Guebuçú, Sailfish
Nomura (1984)
283
Kaupichthys hyoproroides
NENHUM
284
Kyphosus incisor
Pijirica, Pirabanha, Piraboca, Piragica, Pirajica, Piranjica, Pirajica amarelada
Quará, Salema do alto, Salema preta
285
Kyphosus sectatrix
Pirabanha, Piraboca, Piragica, Pirajica, Piramboca, Pirangica, Pirajica preta
Pirangica amarela, Pirangica comum, Piranjica, Quara, Salema
açú, Salema do alto, Salema preta
Mod. from Menezes &
Figueiredo (1985)
286
Labrisomus cricota
Garrião
Maria da toca cricota
287
Labrisomus kalisherae
Garrião, Guavina
Maria da toca olhão
288
Labrisomus nuchipinnis
Folha seca, Garguelo, Garrião, Garrião de papo vermelho, Maria da toca garrião
Garrião guloso, Garrião macaco, Guavina, Guloso, Imborê,
Imborê de chio, Imborê folha seca, Macaco, Maria da toca,
Mariongo, Moré, Peixe macaco, Quatro olhos
(1999)
289
Lachnolaimus maximus
NENHUM
Budião porco
290
Lactophrys bicaudalis
Baiacu caixão, Peixe cofre
Baiacu caixão pintado
291
Lactophrys trigonus
Baiacú, Baiacu caixão, Baiacu chifrudo, Baiacu cofre, Baiacu Baiacu caixão búfalo
sem chifre, Baiacu sem espinhos, Cofre, Ostracião, Peixe cofre,
Peixe vaca, Taoca, Vaca sem chifre
292
Lactophrys triqueter
Baiacu, Baiacu caixão, Baiacu cofre, Baiacu sem espinho, Guamaiacu apé
Cofre, Guamaiacu apé, Ostracião, Peixe cofre, Peixe vaca,
Taoca, Toaca, Vaca sem chifre
Santos (1982)
Falsa moréia marrom
Nº
122
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
293 Letharchus aliculatus
NENHUM
Miroró baiano
294 Liopropoma carmabi
NENHUM
Mariquita arlequim
295 Lobotes surinamensis
Brejereba, Cará do mar, Chancharrona, Crauaçu, Croaçu, Prejereba
Dorminhoco, Frejereba, Frejereva, Gereba, Peixe folha, Peixe
sono, Pejereba, Pijareba, Piraca, Piracá, Piráca, Pirajeva, Prejereba,
Prejereva, Xancarona, Xancarrona, Xanxarrona
Baúna, Caranha de mangue, Carapitanga, Pargo mulato
Baúna
Nomura (1984)
Ariocó, Caranha, Caranha vermelha, Caranho, Caranho verdadeiro, Cioba
Caranho vermelho, Carapitanga, Ceoba, Chioba, Cioba, Cioba
verdadeira, Ciobinha, Cioquira, Guaiúba, Rabo aberto, Sioba,
Siquira, Sirioba, Siriúba, Vermelho caranha, Vermelho cioba,
Vermelho de fundo
Boca negra, Pargo, Pargo boca negra, Pargo boca preta, Saçupema, Vermelho boca negra
Saçupema boca preta, Vermelho, Vermelho boca negra, Vermelho
de fundo, Vermelho do fundo
Caúba, Ceoba, Cioba, Cioba mulata, Gaiero, Goiúba, Guaiuba, Guaiúba
Guaiúba, Guaiúva, Guajuba, Mulata, Rabo aberto, Rabo amarelo,
Saioba, Sarmão, Saúba, Sioba, Siova, Sirioba
Nomura (1984)
300 Lutjanus cyanopterus
Caranha, Caranha do fundo, Caranho, Vermelho caranho
301 Lutjanus jocu
Baúna, Baúna de fogo, Baúna do alto, Baúna fogo, Caranha, Dentão
Carapitanga, Chiova, Cioba, Cioquira, Dentão, Pirá siririca, Sioba,
Siobinha, Siririca, Vermelho, Vermelho dentão, Vermelho siriúba
Acará aia, Acaraaia, Acarapitanga, Acarapuã, Caranha, Pargo verdadeiro
Carapitanga, Caraputanga, Cherne vermelho, Dentão, Pargo, Pargo
cachucho, Pargo olho de vidro, Pargo real, Pargo verdadeiro,
Sacupema, Saçupema, Vermelho, Vermelho dentão, Vermelho do
fundo
Areiacó, Areocó, Ariacó, Aricó, Ariocó, Baúna, Caranho, Caranho Ariocó
verdadeiro, Caranho vermelho, Carapitanga, Ciobinha, Dentão,
Oriocó, Siobinha, Siuquira, Vermelho, Vermelho aricó, Vermelho
ariocó, Vermelho henrique, Vermelho verdadeiro, Vermelho xióva
296 Lutjanus alexandrei
297 Lutjanus analis
299 Ocyurus chrysurus
302 Lutjanus purpureus
303 Lutjanus synagris
Caranha do fundo
Nomura (1984)
Nomura (1984)
Cepene (2000)
Nomura (1984)
123
298 Lutjanus bucanella
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
304 Lutjanus vivanus
Acará aia, Acarapitanga, Carapitanga, Cherne vermelho, Vermelho olho amarelo Rocha & Costa (1999)
Dentão, Olho de vidro, Papaterra estrela, Pargo olho de
vidro, Vermelho, Vermelho de olho amarelo, Vermelho do
fundo, Vermelho olho amarelo, Vidrado
305 Lythrypnus brasiliensis
NENHUM
306 Makaira nigricans
Agulhão, Agulhão azul, Agulhão negro, Agulhão preto, Agulhão negro
Espadarte preto, Kurokawa, Marlim azul, Marlim azul do
Atlântico, Marlin, Marlin azul, Merlim
307 Malacanthus plumieri
308 Malacoctenus delalandei
Bom nome, Peixe da rainha, Peixe pica, Pirá
Macaquinho
309 Manta birostris
Arraia boca de gaveta, Arraia duas cabeças, Diabo do mar, Jamanta gigante
Jamanta, Manta, Morcego do mar, Peixe diabo, Raia jamanta
310 Megalops atlanticus
Camaripim, Camarupi, Camarupim, Camarupim tarpão, Camurupim
Camburupu,
Camorubi,
Camorupim,
Camuripema,
Camuripi, Camuripim, Camurupi, Camurupim, Camurupim
pema, Cangôa, Cangurupi, Cangurupim, Canjurupi,
Canjurupim, Conjurupi, Parapema, Pema, Perapema,
Pirapema, Pomboca, Tarpão
Nomura (1984)
311 Melichthys niger
Cangulo, Cangulo fernande, Cangulo francês, Cangulo Cangulo preto
negro, Cangulo preto, Me pega por favor, Niger, Peixe
porco, Peroá preto
312 Microdesmus bahianus
NENHUM
Peixe lombriga baiano
Freire, pers. comm.
313 Microdesmus longipinnis
NENHUM
Peixe lombriga rosa
FishBase
314 Micrognathus crinitus
Agulha do mar, Peixe cachimbo
Peixe cachimbo preto
315 Micrognathus erugatus
316 Microgobius carri
NENHUM
NENHUM
Peixe cachimbo estrela Carvalho-Filho, pers. comm.
Amoré de listra amarela FishBase
Amoré arlequim
Pirá
Macaquinho comum
124
Cepene (2000)
Nomura (1984)
(1999)
(1999)
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
317
Microphis brachyurus
Peixe cachimbo, Sabiá
Peixe sabiá
318
Microspathodon chrysurus Chrysurus, Crisurus, Donzela azul, Jóia
Donzela azul
319
Mobula hypostoma
Arraia boca de gaveta, Jamanta, Jamanta mirim
Jamanta mirim
320
Mobula japanica
Arraia boca de gaveta
Jamanta de cauda
espinhosa
FishBase
321
Mobula tarapacana
Jamanta chilena
FishBase
322
Mobula thurstoni
Jamanta de cauda lisa
FishBase
323
Mola mola
Lua, Peixe lua, Peixe roda, Sol
Peixe lua
Nomura (1984)
324
Monacanthus ciliatus
Cangulo, Cangulo de fernando, Peixe porco, Peruá, Pirá aca, Porquinho de franja
Piraaca, Porquinho
325
Moringua edwardsi
NENHUM
FishBase
326
Mugil curema
Caíca, Mondego, Parati, Paratí, Parati guaçú, Parati olho de Tainha pratiqueira
fogo, Paratibu, Paratiguera, Pratiqueira, Pratiquera, Sassaiuba,
Saúna, Saúna olho de fogo, Solé, Tainha, Tainha de olho
amarelo, Tainha do olho amarelo, Tainha do olho preto, Tainha
parati, Tainha pitiu, Tainha sajuba, Tainha verdadeira
327
Mulloidichthys martinicus
Salmonete, Saramonete, Saramunete, Trilha, Trilha amarela
Saramonete amarelo
Mod. from Ferreira & Cava
(2001)
328
Muraena melanotis
NENHUM
Moréia colméia
FishBase
329
Muraena pavonina
Caramuru de chifre, Moréia de pintas brancas, Moréia pavão, Moréia pavão
Moréia pintada
330
Muraena retifera
Moréia de roseta
331
Mycteroperca acutirostris
Badejete, Badejo mira, Badejo saltão, Mira, Miracelo, Saltão, Badejo mira
Serigado tapoã
Nomura (1984)
332
Mycteroperca bonaci
Badejo, Badejo ferro, Badejo preto, Badejo quadrado, Cerigado Badejo quadrado
preto, Quadradinho, Serigado, Serigado preto, Sirigado
Enguia macarrão
Moréia de roseta
125
Nº
Nº SPECIES
333 Mycteroperca interstitialis
334 Mycteroperca microlepis
335 Mycteroperca tigris
336 Mycteroperca venenosa
337 Myrichthys breviceps
338 Myrichthys ocellatus
339 Myripristis jacobus
340 Myrophis platyrhynchus
341 Myrophis punctatus
COMMON NAMES
Água fria, Badejo, Badejo amarelo, Cabra, Cabrinha, Mané
nego, Pirambeba, Serigado, Sirigado
Badejo, Badejo bicudo, Badejo branco, Badejo brando,
Badejo da areia, Badejo de areia, Badejo saltão, Badejo
sapateiro, Garoupa, Serigado badejo
Badejo, Badejo mira, Badejo tigre, Serigado, Sirigado
UNIQUE NAME
Badejo amarelo
SOURCE
Szpilman (2000)
Badejo de areia
Suzuki (1986)
Badejo tigre
Szpilman (2000)
Badejo, Badejo ferro, Badejo serigado, Badejo vermelho,
Piragia, Piragira, Pirangira, Serigado ferro, Sirigado,
Sirigado panã
Miriquitis, Miroró, Miroró pintado, Murucutuca pintada,
Mutuca
Miriquitis amarela, Moréia, Muriongo, Murucutuca ocelada,
Mutuca, Mututuca
Fogueira, Juguaraçá, Mariquita, Mariquita do alto, Mariquita
olhão, Miripristis, Olho de vidro, Peixe gato, Pirapiranga,
Vovó de mariquita
Badejo ferro
Suzuki (1986)
Miroró de pintas brancas Carvalho-Filho, pers. comm.
Mututuca
Fogueira
Muriongo narigudo
NENHUM
Congro, Enguia, Moréia, Muriongo, Muriongo mirim, Muriongo mirim
Miroró de rio
Treme treme do norte
NENHUM
343 Narcine brasiliensis
Arraia, Arraia elétrica, Emplasto, Raia elétrica, Raia Treme treme do sul
emplasto, Raia treme treme, Treme treme, Tremelga
344 Naucrates ductor
Camisa de meia, Ductor, Peixe piloto, Piloto, Remeiro, Peixe piloto
Romeiro
Tubarão limão
Cação limão
Nomura (1984)
342 Narcine bancrofti
346
347
348
349
Neoconger mucronatus
Nicholsina usta
Odontaspis ferox
Odontoscion dentex
NENHUM
Budião, Budião batata, Budião sabonete
NENHUM
Corvina dos recifes, Dentudo, Maria mole, Pescada, Pescada
cambucu, Pescada canguçu, Pescada cascuda, Pescada de
pedra, Pescada dentuça, Pescada dentuda, Pirucaia
Enguia de crista
Papagaio esmeralda
Mangona lisa
Pescada de pedra
FishBase
345 Negaprion brevirostris
126
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
350
351
352
353
Ogcocephalus declivirostris
Ogcocephalus nasutus
Ogcocephalus notatus
Ogcocephalus vespertilio
Bacacuá
Batimbau
Cacuá
Peixe morcego
verdadeiro
Cepa (1978)
354
Oligoplites palometa
Peixe morcego, cacuá, bacacuá
Batimbau, Peixe morcego
Cacuá, Peixe morcego, Pirá andirá
Bacacuá, Cachimbo, Cacuá, Guacari, Guacu cuia, Guacucuia,
Oncocéfalo, Peixe cachimbo, Peixe morcego, Peixe morcego do
focinho longo, Pirá andirá
Gaivira, Guaibira, Guaivira, Salteira, Tibiro, Tibiro amarelo,
Tibiro de couro
Guaivira amarela
355
Oligoplites saliens
Gaivira, Guaivira, Guajuvira, Guarivira, Guavira, Guivira, Guaivira salteira
Salteira, Solteira, Táboa, Tibiro, Tibiro saltador, Xaveia, Xavéia
356
Oligoplites saurus
Cavaco, Gaivira, Goivira, Guaibira, Guaivira, Guajuvira, Guaivira branca
Guaravira, Guarivira, Guavira, Pamparrona, Salteira, Solteira,
Tábua, Tibiro, Tibiro branco, Tiburo
357
Omobranchus punctatus
NENHUM
Mod. from FishBase
358
Ophichthus cylindroideus
Cobra do mar, Jucutuca, Moréia, Muçum, Muçum do mar, Porongo
Rosa (1980)
359
Ophichthus ophis
Muçum pintado, Muriongo
Miroró pintado
360
Ophidion holbrooki
Congro, Congro rosa, Falso congro, Miro
Miro
361
Ophioblennius trinitatis
Blênio, Macaco de rabo vermelho, Maria da toca oceânico
Macaco de rabo
vermelho
362
Opisthonema oglinum
Caiçara, Maçambê, Manjuba, Manjuba lombo azul, Manjubão, Sardinha bandeira
Moromba, Sardinha, Sardinha azul, Sardinha baleia, Sardinha
bandeira, Sardinha barriga larga, Sardinha branca rio ribeira,
Sardinha chata, Sardinha da lage, Sardinha de galha, Sardinha de
gato, Sardinha de penacho, Sardinha do alto, Sardinha facão,
Sardinha falcão, Sardinha gaia, Sardinha galho, Sardinha gato,
Sardinha gulosa, Sardinha lage, Sardinha lais, Sardinha laje,
Sardinha larga, Sardinha lombo azul, Sardinha maromba,
Sardinha penacho, Sardinha peú, Sardinha preta, Sardinha roliça,
Sardinha verdadeira, Sardinha verde, Sargo, Xangó
Macaco de mordaça
Nomura (1984)
127
Nº
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
363
Opistognathus brasiliensis NENHUM
Bocão do alto
364
Opistognathus cuvieri
NENHUM
Bocão da boca amarela
365
Opistognathus lonchurus
NENHUM
Bocão bigode
FishBase
366
Opsanus beta
NENHUM
Pacamão estrangeiro
367
Orthopristis ruber
368
Ostichthys trachypoma
Cambuba, Canguito, Cocoroca, Cocoroca comum, Cocoroca jurumirim
Cocoroca jumirim, Cocoroca jurumin, Cocoroca jurumiri,
Cocoroca jurumirim, Cocoroca verdadeira, Corcoroca,
Corcoroca da pedra, Corcoroca jurumim, Corcoroca
jurumiri, Corcoroca jurumirim, Corcoroca legítima,
Corcoroca verdadeira, Coró de pedra, Cotinga, Sapuruna,
Uribaco
NENHUM
Soldado do olho grande
369
Otophidium chickcharney
NENHUM
Congro fantasma
370
Otophidium dormitator
NENHUM
Congro dorminhoco
371
Oxyurichthys
stigmalophius
NENHUM
Amoré nadadeira pintada FishBase
372
Pagrus pagrus
Pagro, Palgo, Pargo, Pargo amarelo, Pargo liso, Pargo Pargo rosa
olho de vidro, Pargo rosa, Pargo róseo, Pargo vermelho
Cepene (2000)
373
Parablennius marmoreus
Blênio, Maria da toca das algas
Normativa 14/2004
374
Parablennius pilicornis
Blênio, Macaco, Maria da toca, Maria da toca das pedras Macaco das pedras
Normativa 14/2004
375
Paraclinus arcanus
Macaquinho de mancha verde
Macaquinho de mancha
verde
376
Paraclinus rubicundus
Macaco verde
Macaquinho verde
Normativa 14/2004
Szpilman (2000)
From English (Carvalho
Filho, 1999)
FishBase
pers. comm.
Macaco das algas
128
Table III. List of all common names associated with Brazilian reef fish species and their unique name chosen according to the source presented
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
377
Paraclinus spectator
NENHUM
Macaquinho de vela
378
Paralabrax dewegeri
Mané velho
Mané velho
379
Paralichthys brasiliensis
380
Paralichthys isosceles
Catraio, Lenguado, Lenguado de praia, Linguado, Linguado Linguado de praia
aramaçá, Linguado de praia, Linguado preto, Rodovalho,
Solha, Solha aramaçá
Linguado, Linguado areia, Linguado de areia, Linguado Linguado transparente
transparente
381
Paralichthys patagonicus
Linguado, Linguado branco
Linguado branco
(2003)
382
Paralichthys tropicus
Linguado, Solha
Linguado tropical
FishBase
383
Paranthias furcifer
Boquinha, Esquentamento, Namorado, Pargo mirim, Pargo Pargo mirim
pincel, Peixe santo
Nomura (1984)
384
Pareques acuminatus
Anteninha, Bandeirinha, Bilró, Cabeça de coco, Doutor, Maria nagô
Equetos, Equetus, Maria nagô, Obispo, Submarino
Nomura (1984)
385
Parexocoetus brachypterus
Peixe voador, Voador
Do inglês (Carvalho Filho,
1999)
386
Pempheris schomburgki
387
Phaenomonas longissima
Machadinha, Manteiga, Olhudo, Papudinha, Pelada, Piaba Piaba do mar
do mar, Sardinha barriguda, Sardinha do mar brabo,
Sardinha gorda, Sardinha ouro
Muriongo comprido
NENHUM
388
Phaeoptyx pigmentaria
Apogon pintado, Cardeal pintado, Olhão, Totó, Totó chita, Totó chita
Totó pintadinho
389
Pinguipes brasilianus
Nomura (1984)
390
Platybelone argalus
Batata, Michole quati, Mixole coati, Mixole quati, Michole quati
Namorado
Agulha, Agulhão
Agulha rabo de quilha
391
Platygillellus brasiliensis
NENHUM
Tanduju tigre
392
Plectrypops retrospinis
Fusquinha, Plectripops, Plic ploc, Soldado
Fusquinha
Voador vela
Univali (2004)
FishBase
129
Nº
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
393
Polydactylus oligodon
394
Polydactylus virginicus
Barbudinho, Barbudo, Parati barbado, Parati barbudo,
Barbudo piraguaba
Piracuaba, Piraguá, Piraguaba, Tainha barbuda
Barbado, Barbudo, Barbudo amarelo, Parati barbado, Parati Barbudo amarelo
barbudo, Parati de barba, Piracuaba, Piraguaba
395
Pomacanthus arcuatus
Arcuatus, Enxada, Frade, Frade cinza, Gordinho, Jandaia, Paru beija moça
Mercador, Paru, Paru beija moça, Paru bordado, Paru branco,
Paru cinza, Paru da pedra, Parú da pedra, Paru dourado, Paru
frade, Paru fumaça, Paru listrado, Paru preto, Parum dourado,
Parumbeba, Peixe frade, Perambeba, Sambuio
Nomura (1984)
396
Pomacanthus paru
Suzuki (1986)
397
Pomadasys corvinaeformis
Enxada, Frade, Frede, Jandaia, Paru, Parú, Paru da pedra, Paru Frade
de pedra, Paru frade, Paru listrado, Paru preto, Parum dourado,
Peixe anjo
Abiquara, Arrebenta panela, Biquara, Cocoroca, Cocoroca Coró boca roxa
legítima, Corcoroca, Corcoroca legítima, Corcoroca verdadeira,
Coró, Coró boca roxa, Coró branco, Coroque branco, Juquiri
branco, Roncador
398
Pomatomus saltatrix
Anchova, Anchoveta, Anchovinha, Anxova, Enchova, Enchova Enchova
baeta, Enchoveta, Enchoveta baeta, Enchovinha, Enxova,
Enxoveta, Marisqueira, Perna de moça, Piquitinga
Nomura (1984)
399
Porichthys kymosemeum
Beatinha, Beatriz, Biatriz, Mamangá liso, Mamangava
Rosa (1980)
400
Porichthys porosissimus
Aniquim de areia, Bacalhau, Bagre sapo, Magangá, Mamangá Mangangá liso
liso, Mamangava, Mangangá, Mangangá liso, Monaguaba,
Niquim, Peixe fosforescente, Peixe sapo, Piramangaba
Figueiredo & Menezes
(1978)
401
Priacanthus arenatus
Cantador, Figueira, Fogueira, Imperador, Mirassol, Olhão, Olho Olho de cão
de boi, Olho de cão, Olho de fogo, Olho de vidro, Olho do
diabo, Piranema, Pirapema
Nomura (1984)
402
Priolepis dawsoni
NENHUM
Amoré pijama
403
Priolepis hipoliti
NENHUM
Amoré ferrugem
Freire & Carvalho-Filho,
pers. comm.
Beatriz
130
SOURCE
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
404
Prionace glauca
405
Prionotus punctatus
Azul, Bico doce, Cação azul, Cação focinhudo, Cação mole Tubarão azul
mole, Focinhudo, Lombo preto, Mole mole, Tubarão azul,
Cabra, Cabrinha, Cascudo, Peixe cabra, Voador bico de Cabrinha Santo Antônio
pato, Voador de pedra, Voador Santo Antônio
406
Pristigenys alta
407
SOURCE
Suzuki (1986)
Pristipomoides aquilonaris Vermelho voraz
Vermelho voraz
408
Prognathodes brasiliensis Borboleta, Borboleta bicuda, Borboleta trombeta
Borboleta bicuda
409
Prognathodes guyannensis NENHUM
Borboleta de fundo
410
Prognathodes
obliquus
Borboleta dos penedos
Mod. from Sampaio &
Nottingham (2008)
411
Prognichthys occidentalis Voador, Peixe voador
Voador do raso
412
NENHUM
Língua de lixa
413
Pronotogrammus
duplicidentatus
Pseudocaranx dentex
414
Pseudogramma gregoryi
NENHUM
Sabaõzinho do alto
415
Pseudopercis numida
Namorado, Namorado verdadeiro
Namorado verdadeiro
416
Pseudopercis
semifasciatus
Namorado, Namorado listrado
Namorado listrado
417
Pseudupeneus maculatus
418
Psilotris batrachodes
Beija moça, Canaiú, Pirametara, Sabonete, Salamonete, Saramonete pintado
Salmão pequeno, Salmonejo, Salmonete, Salmonete da
pedra, Saramonete, Saramunete, Trilha
Amoré sapo
NENHUM
419
Psilotris celsus
NENHUM
Peixe borboleta de São Pedro e São Paulo
Falsa guarajuba, Garapoá, Guaracimbora, Pracumandá, Garapoá
Xaréu, Xaréu branco
Nomura (1984)
FishBase
Amoré de espinho grande FishBase
131
Piranema do fundo
Cassumba de mero, Olhão, Piranema, Piranema do fundo
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
420
Ptereleotris randalli
NENHUM
Linha azul
421
422
Quassiremus ascensionis
Rachycentron canadum
NENHUM
Miroró de pintas pretas
Beijo pirá, Beijupirá, Beiupirá, Bejupirá, Bijupirá, Biupirá, Bijupirá
Cação de escama, Cação de escamas, Canado, Chancarona,
Parabiju, Parambeju, Parambiju, Parambijú, Paramiju,
Parandiju, Peixe rei, Pirá biju, Pirabeju, Pirabiju, Pirambiju,
Pirapiju
423
Raneya brasiliensis
Congro, Lagarto do mar
Congrinho de praia
424
Remora australis
Rêmora
Rêmora de baleia
425
Remora remora
426
Remorina albescens
Agarrador, Pegador, Peixe pegador, Peixe piolho, Piolho de Rêmora comum
cação, Piolho de tubarão, Piraquiba, Rémora, Rêmora
Rêmora branca
Pegador, Rêmora
427
Rhincodon typus
Cação estrela, Pintadinho, Tubarão baleia
Tubarão baleia
Suzuki (1986)
428
Rhinobatos horkeli
Arraia viola, Cação viola, Raia viola, Viola
Raia viola brasileira
429
430
Rhinobatos lentiginosus
Rhinobatos percellens
NENHUM
Arraia viola, Cação viola, Guitarra, Raia viola, Viola
Raia viola do Atlântico
Raia viola do sul
FishBase
431
Rhinoptera bonasus
Arraia cabocla, Arraia moitão, Raia, Raia focinho de vaca, Raia Ticonha
sapo, Raia ticonha, Ticonha, Raia-Boi, Arraia-de-duas-cabeças,
Arraia-jamborana
Nomura (1984)
432
Rhinoptera brasiliensis
Arraia ticonha, Raia boi, Ticonha
433
Rhizoprionodon lalandii
Bico de surela, Bico de suvela, Bico fino, Bicudinho, Caçonete, Cação alecrim
Cação aipim, Cação alecrim, Cação alegrim, Cação anjo, Cação
babaqueiro, Cação bicudo, Cação de bico doce, Cação fidalgo,
Cação frango, Cação frango olhudo, Cação babaqueiro, Cação
rabo seco, Cor de enxofre, Cucuri, Fecha venda, Frango,
Figuinho, lauê, Lustroso, Rabo seco, Sicuri, Sucuri, Tubarão
frango, Tubarão frango olhudo
Nomura (1984)
Raia boi
132
UNIQUE NAME
SOURCE
SPECIES
COMMON NAMES
434
Rhizoprionodon porosus
Cação, Cação alecrim, Cação bicudo, Cação de praia, Cação Cação frango
fidalgo, Cação frango, Cação rabo seco, Caçonete, Cucuri,
Fecha venda, Figuinho, Frango
435
Rhomboplites aurorubens
Arcoco, Areocó, Caranha, Carapitanga, Chioba, Chiova, Cioba, Realito
Ciova, Mulata, Paramirim, Pargo pinanga, Pargo piranga,
Piranga, Realito, Sioba, Siobinha, Vermelha do ar,
Vermelhinho, Vermelho, Vermelho olho mole, Vermelho
paramirim, Vermelho piranga, Xióva
436
Ribeiroclinus
eigenmanni
NENHUM
Macaquinho do sul
437
Risor rubber
NENHUM
Amoré de esponja
438
Rypticus bistrispinus
Badejo sabão, Badejo sabão pintalgado, Sabão
Badejo sabão mirim
Rangel & Freire, pers.
comm.
439
Rypticus randalli
Badejo sabão, Peixe sabão
Badejo sabão marrom
440
Rypticus saponaceus
Badejo, Badejo sabão, Badejo sabão comum, Cerigado sabão, Badejo sabão comum
Peixe sabão, Sabão, Sabonete, Saramonete, Serigado sabão
441
Rypticus subbifrenatus
Badejo sabão
Badejo sabão pintado
442
Sarda sarda
Bonito serrinha
443
Sardinella aurita
Sardinha charuto
(2003)
Nomura (1984)
444
Sardinella janeiro
Sardinha verdadeira
Nomura (1984)
445
Sargocentron bullisi
Baquara, Bonito, Bonito atlântico, Bonito serrinha, Cavala,
Sarda, Sarrajão, Serra, Serra comum, Serra de escama, Serra
Alacha, Maromba, Sardinha, Sardinha charuto, Sardinha de lata,
Sardinha legítima, Sardinha maromba, Sardinha verdadeira,
Sardinha verdadeira grande, Sardinha verdadeira pequena
Biribiri, Boca torta, Charuto, Escamuda, Manjuvão, Maromba,
Sardinha, Sardinha azul, Sardinha charuto, Sardinha de galha,
Sardinha do reino, Sardinha legítima, Sardinha maromba,
Sardinha verdadeira
NENHUM
Jaguareçá listrado
(2008)
133
Nº
UNIQUE NAME
SOURCE
Nº
SPECIES
COMMON NAMES
446
Scartella cristata
447
Scartella poiti
Mod. from Nomura (1984) &
Macaco, Macaco verde, Marachomba, Maria da toca, Peixe Marachomba verde
macaco
NENHUM
Marachomba de trindade Carvalho-Filho, pers. comm.
448
Scarus trispinosus
449
Scarus zelindae
450
Scomber colias
451
Scomberomorus
brasiliensis
452
Scomberomorus
cavalla
453
Scomberomorus
regalis
454
Bico verde, Budião, Budião azul, Budião preto, Budião Papagaio azul
roxo, Budião una, Peixe papagaio, Papagaio preto,
Papagaio una
Budião banana, Peixe papagaio zelinda, Scarus banana
Papagaio banana
Szpilman (2000)
Cavala, Cavala de reino, Cavala do reino, Cavala
sardinheira, Cavalinha, Muzundo, Muzundu, Muzundum,
Periquito, Serra de escama, Sororoca
Caroroca, Cavala, Cavala pintada, Escalda mar, Sarda,
Serra, Serrá, Serra pima, Serra pininga, Serrapinima,
Serrinha, Sororoca, Sororóca
Cavala, Cavala aipim, Cavala branca, Cavala impingem,
Cavala perna de moça, Cavala preta, Cavala sardinheira,
Cavala verdadeira, Perna de moça, Serra, Sororoca
Cavala, Cavala boca larga, Cavala branca, Cavala canguçu,
Cavala pintada, Cavala sardinheira, Cavala serra, Serra,
Serra penincho, Serra pininga, Sororoca, Sororoca pinima
Cavala sardinheira
Nomura (1984)
Serra
Nomura (1984)
Cavala
Nomura (1984)
Serra pininga
Scorpaena bergi
NENHUM
Mangangá cabeça de
ganso
FishBase
455
Scorpaena
brasiliensis
456
Scorpaena calcarata
Beatinha, Beatinha pintada, Beatriz, Mamangá, Mangangá, Mangangá vermelho
Mangangá pintado, Mangangá vermelho, Niquim, Niquim
da pedra, Niquim de pedra, Peixe escorpião, Peixe
Mangangá cabeça lisa
Mangangá
457
Scorpaena dispar
Mangangá, Moriati
458
Scorpaena
grandicornis
Beatinha, Beatriz, Mangangá, Mangangá de espinho, Mangangá de pluma
Niquim da pedra, Niquim de pedra, Peixe escorpião,
Mangangá de chifres
Mod. from Ferreira & Cava (2001)
Mod. from Carvalho & Branco
(1977)
Mod. from Rocha & Costa (1999)
Mangangá corcunda
134
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
459
Scorpaena inermis
NENHUM
Mangangá cogumelo
FishBase
460
Scorpaena isthmensis
Beatriz, Mamangá, Mangangá, Mangangá cara lisa, Moréia Mangangá cara lisa
ati cara lisa, Peixe pedra
461
Scorpaena mellissi
NENHUM
462
Scorpaena plumieri
463
Scorpaenodes caribbaeus
Anequim, Aniquim, Aniquim beatriz, Aniquim de pedra, Mangangá axila roxa
Baetinha, Beatinha, Beatinha axila rocha, Beatriz, Biriati,
Briati, Mamangá, Mangangá, Mangangá axila roxa, Moreiati,
Moriati, Niquim, Niquim da pedra, Niquim de pedra, Peixe
escorpião, Peixe pedra, Sarrão
Beatinha colorada
Beatriz, Mangangá
464
Scorpaenodes insularis
NENHUM
Beatinha dos penedos
465
Scorpaenodes
tredecimspinosus
Mangangá
Beatinha de recife
466
Selar crumenophthalmus
Carapau, Chicharro, Chicharro olho grande, Garajuba, Chicharro olho grande
Garapau, Guarajuba, Gurapau, Gurapu, Manequinho, Olhão,
Olhudo, Xixarro olho de boi, Xixarro, Xixarro olho grande,
Xixarro olhudo
467
Selene brownii
Galo, Peixe galo
468
Selene vomer
Abatucaia, Alfaquim, Aracaguira, Aracanguira, Capão, Galo, Galo de penacho
Galo bandeira, Galo da costa, Galo de fita, Galo de penacho,
Galo do alto, Galo do morro, Galo fita, Galo proa de bote,
Galo verdadeiro, Peixe galo, Peixe galo de penacho, Testudo
469
Seriola dumerili
Arabaiana, Arabaiana pintada, Olhete, Olho de boi, Pitangola, Olho de boi
Tapiranga, Tapireca, Tapireçá, Urubaiana
470
Seriola fasciata
Arabaiana, Olhete, Olhete listrado, Olho de boi, Pitangola, Olhete listrado
Urubaiana
Szpilman (2000)
471
Seriola lalandi
Arabaiana, Arabaiana pintada, Olhete, Olho de boi, Pitangola, Olhete comum
Tapiranga, Tapireça, Tapireçá, Urubaiana
(2008)
Mangangá dos penedos Carvalho-Filho, pers. comm.
Galo de recife
(2008)
135
Nº
UNIQUE NAME
SOURCE
Nº
SPECIES
COMMON NAMES
472
Seriola rivoliana
Arabaiana, Fumeiro, Olhete bacamarte, Olho de boi, Olho de Olhete bacamarte
boi fumeiro, Piloto, Remeiro
473
Serranus annularis
NENHUM
Mariquita de dorso laranja
FishBase
474
Serranus atrobranchus
Jacundá
Mariquita de orelha negra
FishBase
475
Serranus baldwini
Badejinho lanterna, Mariquita pintada, Mero, Peixe gato, Mariquita pintada
Serranus laranja
476
Serranus chionaraia
NENHUM
477
Serranus flaviventris
Jacundá, Mariquita, Pirucaia, Serigado xerne, Serrano, Mariquita pirucaia
Serranus barriga branca, Traíra, Traíra das pedras, Vovó
478
Serranus phoebe
Jacundá, Sete fundão
Sete fundão
IBAMA Inst. Normativa
14/2004
479
Serranus tabacarius
Jacundá
Mariquita fumo
Mod. from FishBase
480
Sparisoma amplum
Batata, Bobó, Budião, Budião bandeira, Budião batata, Papagaio de recife
Budião comum, Budião de recifes, Budião papagaio, Budião
vermelho, Papagaio bandeira, Papagaio espelho, Peixe
papagaio, Peixe papagaio dos recifes
Mod. from Ferreira & Cava
(2001)
481
Sparisoma axillare
Batata, Bobó, Budião, Budião batata, Budião caranha, Papagaio cinza
Budião cinza, Budião verde, Papagaio verde, Peixe
papagaio, Peixe papagaio cinzento
482
Sparisoma frondosum
Batata, Bobó, Bodião roxo, Budião, Budião agassiz, Budião Papagaio sinaleiro
barriga azul, Budião enxofrado, Budião verde, Papagaio,
Papagaio aquarela, Peixe papagaio, Peixe papagaio sinaleiro
Mod. from Sampaio &
Nottingham (2008)
483
Sparisoma radians
Batata, Bobó, Bodião verde, Budião, Peixe papagaio dentuço Papagaio verde dentuço
484
Sparisoma tuiupiranga
NENHUM
485
Sphoeroides greeleyi
Baiacu, Baiacu areia, Baiacu mirim, Baiacu pinima, Baiacu Baiacu areia
pintado, Baiacu verde
Mariquita arlequim
Ihering (1968)
Freire, pers. comm.
Martins-Juras (1987)
Papagaio vermelho
136
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
486
Sphoeroides pachygaster
Baiacu, Guima das paredes
Baiacu gigante
487
Sphoeroides spengleri
Baiacu, Baiacú, Baiacu mirin, Baiacu pinima
Baiacu pinima
488
Sphoeroides testudineus
Baiacu, Baiacú, Baiacu de croa, Baiacu dondon, Baiacu Baiacu quadriculado
franguinho, Baiacu mirim, Baiacu pininga, Baiacu pintado,
Baicu quadriculado, Guamaiacu mirim
489
Sphoeroides tyleri
Baiacu
490
Sphyraena barracuda
Bacuda, Barracuda, Bicuda, Bicuda cachorra, Bicuda de corso, Barracuda
Carama, Carana, Corama, Gaviana, Goirana, Gorana, Guarana,
Pescada, Pescada bicuda, Pescada goiva
491
Sphyraena borealis
Bicuda, Barracuda, Bicuda de corso, Bicuda goirana
492
Sphyraena guachancho
Barracuda, Bicuda, Bicuda branca, Bicuda goirana, Bicudinha, Bicuda branca
Corama, Coroma, Goirana, Gorana, Pescada bicuda, Pescada
goirana, Pescadinha bicuda
493
Sphyraena tome
Bicuda, Pescada bicuda
494
Sphyrna lewini
Cação cornudo, Cação martelo, Cação rudela, Cambeva, Cambeva preta
Cambeva preta, Cornudo, Martelo, Peixe martelo, Rudela,
Suzuki (1986)
495
Sphyrna mokarran
Cação martelo, Cação panã, Cambeva, Martelo, Panã, Peixe Martelo gigante
martelo
Mod. from Carvalho &
Branco (1977)
496
Sphyrna tiburo
Cação, Cação campeba, Cação chapéu, Cação martelo, Cação Cambeva pata
panã, Cação pata, Cação rodela, Cação rudela, Cambeva pata,
Chapéu armado, Martelo, Pata, Peixe martelo, Rodela, Rudela,
Tubarão panã
497
Squatina punctata
Cação anjo, Tubarão anjo espinhudo, Anjo, Anjo do mar
Anjo da pedra
498
Starksia brasiliensis
NENHUM
Maria da toca malhada
499
Starksia multilepis
NENHUM
Maria da toca escamosa FishBase
Baiacu de cavanhaque
Bicuda goirana
Bicuda pescada
(2008)
Nomura (1984)
Mod. from Rocha & Costa
(1999)
137
Nº
UNIQUE NAME
SOURCE
Nº
SPECIES
COMMON NAMES
500
Stegastes fuscus
501
Stegastes pictus
Café torrado, Castanheta, Donzela, Donzela escura,
Saberé café torrado
Donzelinha, Maria mole, Maria preta, Querê querê, Saberê
Cará, Castanheta, Donzela bicolor, Gregório, Saberé, Saberé bicolor
Saberê, Saberê bicolor
Mod. From Carvalho-Filho
(1999)
(1999)
502
Stegastes rocasensis
Donzela, Saberé
Saberé de Rocas
503
Stegastes sanctipauli
Donzela de São Pedro e São Paulo
Donzela de São Pedro
504
Stegastes trindadensis
NENHUM
Donzela de Trindade
Mod. from Sampaio &
Nottingham (2008)
Freire, pers. comm.
505
Stegastes uenfi
Donzela cinza, Gregório, Maria preta
Donzela cinza
506
Stegastes variabilis
Anjo, Cará, Castanheta, Donzela, Donzela amarela, Donzela Saberé amarelo
cacau, Donzelinha amarela, Saberê, Saberê amarelo
507
Stephanolepis hispidus
Cangulo, Cangulo Fernando, Esfaldado, Esfalfado, Porquinho de pedra
Gudunho, Negro mina, Peixe porco, Peixe porco de pedra,
Peroazinho, Peruá, Piraaca, Piruá, Porquinho, Porquinho de
fronte reta
(1999)
508
Stephanolepis setifer
Cangulo, Peixe porco, Peixe porco de pedra, Peruá, Pirá aça, Porquinho de penacho
Porquinho de penacho
(2008)
509
Storrsia olsoni
NENHUM
Tanduju de Rocas
510
Strongylura marina
Agulha, Agulhão, Agulhinha
Agulha do Atlântico
Mod. from Godoy (1987)
511
Strongylura timucu
512
Stygnobrotula latebricola
Acarapindá, Agulha, Agulhão, Agulhão roliço, Carapiá, Timucu
Peixe agulha, Petimbuaba, Timbucú, Timicu, Timucu,
Timucú, Timuçu
Brótula negra, Latebrícola, Viúva negra
Viúva negra
513
Syacium micrurum
Linguado, Linguado da areia, Linguado dáreia, Solha, Tapa
514
Syacium papillosum
(2008)
Mod. from Figueiredo &
Menezes (2000)
Aramaçá, Aramaçã, Linguado, Linguado da areia, Linguado Linguado do olho riscado Carvalho-Filho (1999)
dáreia, Linguado de areia, Linguado do olho riscado, Solha,
Solha de dente
Linguado de canal
138
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
515
Symphurus diomedeanus
Língua de mulata, Língua de mulato, Solha
Língua de mulata de
nadadeira pintada
Szpilman (2000)/FishBase
516
Symphurus plagusia
Língua, Língua de mulata, Língua de mulato, Língua de vaca, Língua de mulata de
bochecha escura
Linguado, Linguado mulato, Solha, Solha linguado
517
Symphurus rhytisma
Língua de mulata
518
Synodus foetens
Bonome, Coió, Jacaré, Lagartixa, Lagarto, Lagarto do mar, Lagarto papo branco
Peixe lagartixa, Peixe lagarto, Peixe lagarto costeiro, Tira vira,
Tiravira, Traíra, Traíra do bico fino, Traíra do mar, Traíra do
papo branco, Traíra papo branco
Mod. from Carvalho &
Branco (1977)
519
Synodus intermedius
Calango, Lagartixa, Lagarto do mar, Peixe lagarto, Peixe Lagarto do raso
lagarto de areia, Tira vira, Traíra, Traíra branca, Traíra das
pedras, Traíra de água salgada, Traíra do mar, Traíra preta
520
Synodus saurus
NENHUM
521
Synodus synodus
Bom nome, Peixe lagarto, Peixe lagarto vermelho, Calango, Lagarto vermelho
Lagarto do mar, Peixe pica, Traíra do mar
522
Thalassoma noronhanum Budião de Noronha, Sabonete das ilhas, Talassoma azul
523
Thalassophryne
montevidensis
524
Thalassophryne nattereri Aniquim, Aniquim da lama, Moreiatim, Niqui, Niquim, Niquim Niquim do mar
comum, Niquim da areia, Niquim do mar
Nomura (1984)
525
Thalassophryne punctata Moreiatim, Niquim, Pacamão
Szpilman (2000)
526
Thunnus albacares
Albacora, Albacora da lage, Albacora da laje, Albacora de lage, Albacora laje
Albacora de laje, Albacora lage, Albacora laje, Albacora lajeira,
Alvacora, Alvacora lajeira, Atum, Atum amarelo, Atum galha
amarela, Kihada, Kimeji, Kiwada, Lageira
527
Thunnus atlanticus
Albacora, Albacora preta, Albacora rabo seco, Albacorinha, Albacorinha
Atum, Atum negro, Atum preto, Binta
Nomura (1984)
Língua de mulata do
rabo preto
Lagarto azul
Budião de Noronha
Caboza, Mangangá, Niquim, Niquim barrado, Niquim do sul, Tumi tumi
Tumi tumi
Moreiatim
Normativa 14/2004
Sazima et al. (2003)
139
Nº
SPECIES
COMMON NAMES
UNIQUE NAME
SOURCE
528
Tomicodon australis
NENHUM
Peixe ventosa mirim
529
Trachinocephalus
myops
Peixe cobra, Peixe lagarto, Traíra, Traíra branca, Traíra das Traíra do mar
pedras, Traíra de água salgada, Traíra do alto, Traíra do mar
530
Trachinotus carolinus
Cangueiro, Enxova, Palombeta, Palometa, Palumbeta, Pampo cabeça mole
Pampano, Pamplo, Pampo, Pampo amarelo, Pampo cabeça
mole, Pampo da espinha mole, Pampo de cabeça mole, Pampo
real, Pampo verdadeiro, Pereroba, Pirabora, Piraroba,
Samenduara, Semenduara, Solteira
Nomura (1984)
531
Trachinotus falcatus
Arabebéu. Aracanguira, Arebebéu, Arecangura, Aribebéu, Pampo garabebéu
Cernambiguara, Garabebel, Garabebéu, Pampo, Pampo
arabebéu, Pampo galhudo, Pampo garabebéu, Pampo gigante,
Pampo verdadeiro, Rombudo, Sangue de boi, Sernambiguara,
Sernambiquara, Tambó
532
Trachinotus goodei
Aracanguito, Aratobaia, Aratubaia, Galhuda, Galhudinho, Pampo galhudo
Galhudo, Jiriquiti, Pampino, Pampo, Pampo aracanguira,
Pampo de espinha mole, Pampo espinha mole, Pampo galhudo,
Pampo listado, Pampo listrado, Pampo malhado, Pampo mirim,
Pampo riscado, Sargento, Sernambiquara
Nomura (1984)
533
Trachurus lathami
Carapau, Chicharro, Garaçuma, Surel argentino, Xinxarro, Chicharro lombo preto
Xixarro, Xixarro de lombo preto, Xixarro do lombo preto
534
Trichiurus lepturus
Catana, Embira, Espada, Guaravira, Imbira, Peixe espada, Peixe Espada
fita
Nomura (1984)
535
Tylosurus acus
Agulhão, Agulhão bebé, Agulhão bebeu, Agulhão lambaio, Agulhão lambaio
Timbale
Szpilman (2000)
536
Tylosurus crocodilus
Agulhão, Agulhão bebé, Agulhão bebeu, Agulhão verde, Zamboque
Zambaio roliço, Zamboque
Nº
140
SPECIES
COMMON NAMES
UNIQUE NAME
537
Umbrina coroides
Betara, Cabeça seca, Castanha, Castanha riscada, Chora Castanha riscada
chora, Corcoroca da areia branca, Coró branco, Corvina,
Corvina branca, Corvina de linha, Corvina listada, Corvina
nova, Corvina rajada, Corvina riscada, Cururuca lavrada,
Cururuca riscada, Embetara, Embitara, Juruna, Mbetara,
Ombrino, Papa terra, Papaterra de dentes, Roncador,
Roncador taboca, Sargento, Tametara, Tembetara
Nomura (1984)
538
Upeneus parvus
Saramonete, Trilha, Trilha pena
Trilha anã
Mod. from Ávila da Silva &
Carneiro (2003)
539
Uraspis secunda
Boca de algodão, Cara de gato, Língua de algodão, Sabão
Cara de gato
540
Uropterygius macularius
NENHUM
Moréia manchada
541
Urotrygon microphthalmum
Raia, Raia de fogo
Raia de fogo
542
Xanthichthys ringens
Cangulo mirim, Cangulo rei, Cangulo do alto, Gatilho preto
Cangulo mirim
543
Xyrichthys incandescens
NENHUM
Curuá fogo
544
Xyrichtys martinicensis
NENHUM
Curuá rosado
FishBase
545
Xyrichtys novacula
Bodião curuá, Budião, Budião de areia, Gudião, Peixe Budião curuá
dragão
Nomura (1984)
546
Xyrichtys splendens
547
Zapteryx brevirostris
Budião curuá, Curuá verde, Peixe dragão, Peixe dragão Curuá verde
verde
Raia, Viola, Viola de cara curta
Viola de cara curta
SOURCE
Nomura (1984)
* Barletta (2002) corresponds to Mário Barletta (pers. comm., Universidade Federal de Pernambuco, Brazil); ** Rangel, pers. comm. (Carlos Rangel, Universidade
Federal Fluminense, Centro de Estudos Gerais, Departamento de Biologia Marinha, Brazil); *** Sampaio, pers. comm. (Cláudio Sampaio, Museu de Zoologia da
Universidade Federal da Bahia, Brazil); ****FishBase indicates common names translated and/or modified from www.fishbase.org
141
Nº
142
Thus, there is an impact of the diversity of names
when trying to assess how fisheries affect the
resources (see, p. ex., Freire & Pauly 2005). Species
commercialized among aquarists were associated to
4.8 common names each, which was smaller than
the average of 7.2 for reef species in general. This
probably occurs because these species are mainly
exported (Monteiro-Neto et al. 2003) and their
English names are commonly used in the
international market.
Size is another factor leading to the richness
of fish names (one of the Berlin’s attributes).
According to Hunn (1999), larger species have more
names. The author presented evidence for several
groups: mammals, birds, fishes and even plants.
However, his evidence was based on rather poor
regression fits. We showed here that species of
intermediate size are more prone to be named and
the richness of names decrease for the largest
species.
Even though the richness of names is
important from the cultural point of view, it poses
problems when dealing with regional or national
scales. Problems are similar to the evidenced by the
use of synonyms of scientific names and raise from
the fact that we do not know what we are referring to
(see, p.ex., Minelli 1999). The correct identification
of species is a sine qua non condition to proper
assess the effect of fishing on the local biodiversity.
The use of the national official list of common
names proposed here would be appropriate
whenever species are dealt with in a national context
(in scientific publications or reports), in catch
statistics, and/or in legislation, just to represent the
species with a name more accessible to the general
public than the scientific name. For those cases
where the species are dealt in a more local context,
their local names should be used as usual and thus,
the original richness of names is kept. The proposed
unique names are not intended to replace local
names, which reflect all the knowledge local
communities have about their local resources, but
represent only names to be used at a national scale,
chosen based on well-established criteria from the
array of existing names. The same procedure could
be used for all the other marine and freshwater
species.
Acknowledgements
We would like to thank all those who kindly
sent their publications with common names; to those
who suggested common names for species with no
known published name; to D. Pauly who introduced
the first author to the ‘world’ of common names; and
to Cláudio Sampaio and two anonymous referees for
their valuable corrections and suggestions.
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Received October 2008
Accepted February 2009
Published online April 2009
Evolution and state of the art of fishing capacity management in Peru:
The case of the anchoveta fishery
MARTIN ARANDA1
1
AZTI Tecnalia, Technological Institute for Fisheries and Food. Marine Research Division. Herrera Kaia - Portualdea,
z/g; E-20110. Spain. E-mail: maranda@pas.azti.es
Abstract. The Peruvian anchoveta fishery began in the early 1950s and has become one of the
most important fisheries in the world in terms of landings and fishmeal production. Fisheries
management in Peru has evolved from regulated open access to recently introduced individual
vessel quota management. This paper aims to examine the evolution of fishing capacity
management and identify the management actions that have determined the current levels of
fishing overcapacity. A lack of a solid policy to stop fishing capacity accumulation together with
management susceptibility to industry pressure are likely the main causes of the historical levels
of overcapacity, which has recently encouraged a drastic change in the management system.
Key words: Peruvian anchoveta, fishing capacity, regulated open access, IVQs, ITQs
Resumen. Evolución y situación de la gestión de la capacidad de pesca en Perú: El caso de la
pesquería de anchoveta. La pesquería de anchoveta peruana se inició a principios de los años
cincuenta y se ha convertido en una de las pesquerías más importantes del mundo en términos de
desembarques y producción de harina de pescado. La gestión de la pesquería ha evolucionado
desde un acceso abierto regulado a un sistema de cuotas individuales por embarcación. Este
artículo tiene como objetivo revisar la evolución de la gestión de la capacidad de pesca e
identificar las decisiones que han determinado los niveles actuales de sobrecapacidad. La falta de
una política sólida para impedir la acumulación de la capacidad de pesca junto con una gestión
susceptible a la presión de la industria serian las causas principales de los niveles históricos de
sobrecapacidad que han demandado un cambio drástico en la gestión de la pesquería.
Palabras clave: Anchoveta peruana, capacidad de pesca, acceso abierto regulado, IVQs, ITQs
Introduction
Fishing overcapacity is an acute problem
that threatens marine fisheries due to over-fishing
while producing significant economic waste (FAO
1999). One notable case of capacity accumulation is
that of the Peruvian pelagic fishery. The fishery
focuses on the exploitation of anchoveta (Engraulins
ringens) for fish meal production. Other pelagics are
mainly utilised in canning and freezing (Fig. 1). The
anchoveta fishery is managed using a ‘top-down’
approach where the management authority attempts
to enforce a Total Allowable Catch (TAC).
High abundance of anchoveta and historical
management
decisions
have
allowed
the
development of a large fleet (Fig. 2). Throughout the
history of the fishery, capacity accumulation has
been considered detrimental to its sustainability.
Overcapacity tends to be more dangerous due to the
continuous threat of El Niño. The collapse of the
anchoveta fishery in early 1970s shows how a
natural phenomenon together with over-fishing, can
drive a resource to exhaustion (Boerema & Gulland
1973, Tsukuyama 1983). The crash of the anchoveta
fishery has become a paradigmatic case for study
and is analysed in several academic texts e.g.
Hilborn & Walters (1992).
Currently, high levels of capacity are being
suggested as the cause of the race for fish a situation
where 1200 vessels competing for the TAC have
reduced the fishing season to 50 days (Fig. 3). The
government has recently passed Law 1084 which
advocates the implementation a new system to
manage the fleet through individual vessel quotas
(IVQs). This paper reviews the theoretical concepts
Evolution and state of the art of fishing capacity management in Peru
behind overcapacity and the race for fish; examines
the diverse management measures undertaken by the
Peruvian government, from the early times of the
fishery to the recently introduced management
decisions; and assesses the new management scheme
as a tool to reduce fishing capacity.
Theoretic background. It is widely
recognised that pure and regulated open access are
the main causes of overcapacity. Pure open access is
defined as the state where access rights do not exist
or are poorly defined. In a regulated open access,
access rights are weakly defined and the
management system attempts unsuccessfully to
enforce a Total Allowable Catch (TAC). Due to the
common pool characteristic of resource exploitation,
individuals have the incentive of taking a bigger
share of the TAC. This race for fish encourages
fishers to invest in larger and more modern vessels
to ensure larger individual shares (Grevobal &
Munro 1999). Consequently, resources are gradually
depleted and the fishing season becomes shorter.
Because of rent dissipation, the fishery becomes
vulnerable to adverse economic and resource shocks.
In this context, fishers may press the government to
provide subsidies to alleviate economic distress,
increase the TAC or lengthen the fishing season.
Other factors that may lead to overcapacity
are inter alia the evolution of competitive fishing
industries, the rapid development of harvesting
technology and the expansion of fish markets
(Cunningham & Grévobal 2001). The traditional
management of resources that stipulate input (i.e.
limits on fishing effort, closed seasons and fishing
gear) and output restrictions (i.e. TACs) may not
control capacity efficiently. On the contrary, they
may induce redistribution of effort across fisheries
or accumulation of capacity (Grévobal & Munro
1999).
Among the management measures to
counteract capacity building, Ward and Metzner
(2002) outline two types of strategies: incentive
blocking measures and incentive adjusting measures.
The former measures aim at blocking fleet capacity
building. They include limited license programs,
vessel buyback schemes, gear and vessel
restrictions, individual vessel quotas (IVQs), TACs,
and individual effort quotas. The main difficulty in
implementing these measures is ensuring
compliance. Should a fisher be prevented from
increasing profits by a certain regulation, he will
have the incentive to circumvent that regulation;
hence he will find the means to increase capacity by
increasing or substituting inputs. This fact is prone
to occur where penalties and mechanisms of
enforcement are not strong enough to prevent non-
147
compliance.
On the other hand, incentive adjusting
measures offer long-term strategies to control
overcapacity by creating a sense of ownership, thus
the race for fish may be eliminated by fishers
themselves through capacity reduction. Even though
incentive adjusting measures are the most effective
solutions to counteract overcapacity, they are hard to
implement since they require a drastic change in the
management apparatus. These measures comprise
territorial use rights (TURFs), individual
transferable quotas (ITQs) and collective fishing
rights (Ward & Metzner 2002).
Early fishing capacity management. The
production of fishmeal started in Peru in 1950.
Landings of Peruvian anchoveta increased rapidly
from 1200 tons in 1951 to more than 6.6 million tons
in 1963 converting the Peruvian fishmeal industry
into the largest in the world (Christy & Scott 1967,
Bottemanne 1972). In 1963, the scientific authority,
IMARPE (“Instituto del Mar del Perú”) was
founded. In 1965, scientists recommended the first
TAC of 7 million tons and the first closed season to
deter heavy exploitation (IMARPE 1965, Clark
1976). Due to resource abundance and high demand
for fishmeal, the fishing fleet experienced fast
growth. In 1951, 25 vessels were registered. In 1964,
the fleet had expanded to 1744 boats.
This frenzy of shipbuilding persisted
throughout the 1960s and early 1970s (see Fig. 2).
The fleet was built without clear and strong
restrictions since management rules were poorly
defined. The administration and formulation of the
Peruvian fishery policy was spread amongst diverse
ministries, none of which had fisheries management
as their main task (Hammergren 1981). In 1965,
IMARPE reported that there was evidence of
overexploitation and recommended measures to
deter the escalating rate of fleet building (IMARPE
1965). In 1969, the military government created the
Ministry of Fisheries and empowered it as the
national management authority (Guerra 1972). Only
restrictions to fishmeal plant installation were
devised (Montoya 2003), however, and in 1971,
landings reached 12.3 million tons which is the
highest level ever experienced for a single-species
fishery in the world (see Fig. 1). Then, in 1972, the
industry was hit by a particularly strong El Niño
event. During 1972-73, the anchoveta population
was seriously depressed (Tsukuyama 1983).
Two major causes may have produced the
collapse of anchoveta: the El Niño event and overfishing (Boerema & Gulland 1973). Since 1965
IMARPE recommended TACs but in practice,
catches exceeded the scientifically recommended
M. ARANDA
148
denationalized the fishing fleet due to the
impossibility of subsidizing the fleet during years of
poor catches (Glantz 1979).
In early 1980s, the anchoveta stock
apparently began to recover but was hit again by the
strong El Niño 1982-83 (Tsukuyama 1983). The
population of anchoveta was again seriously
reduced. Throughout the rest of the 1980s, the
stock did not recover to former levels. In this period,
few management measures were undertaken in
relation to fleet size. One of the most notable
measures was the export of idle purse seiners to
other countries in Latin-America (Sueiro 1996). The
effect of the 1980s crisis was reflected in
deterioration and age of the fleet. In late 1980s, 80%
of the 373 boats that composed the industrial fleet
were poorly equipped and older than 20 years
(Garcia Mesinas 1993).
quota. It was obvious that the enforcement system
was not strong enough to ensure compliance with
the TACs. Because of the fleet size, adherence to a
TAC of 7.5 million tons required a shorter fishing
season. Few boat owners could afford to tie up their
boats due to fishmeal plants demanding raw material
to satisfy the high international demand (Laws
1997). After the catastrophic El Niño, the military
government nationalised the industry with the aim of
rationalizing the activity and preserving the resource
(Glantz 1979).
The government created the state owned
Pesca-Peru. This large company started its activities
with 1154 fishing vessels and 99 fishmeal plants.
The government decided to apply corrective
measures such as a drastic reduction of the fleet and
a moratorium on vessel licensing and construction
(Laws 1997). In 1976, the government
14,000
anchovy
12,000
sardine
mackerel & jack mackerel
total
Thousands tons
10,000
8,000
6,000
4,000
2,000
0
2006
2004
2002
2000
1998
1996
1994
1992
1990
1988
1986
1984
1982
1980
1978
1976
1974
1972
1970
1968
1966
1964
1962
1960
1958
1956
1954
1952
1950
Figure 1. Evolution of the Peruvian pelagic fisheries 1950-2006. Data source: PRODUCE.
The 1990s: a new era of capacity
building. Throughout the period 1990-1995 and
1995-2000, a new democratic government adopted
neo-liberal economic policies. The most important
action was the privatisation of Pesca-Peru. The new
policies and the recovery of anchoveta stocks
offered an optimal environment for the industry to
invest in fleet and processing capacity. Industry’s
investment in the period 1991-1995 was estimated at
$ 400 million. (Aguilar et al. 2000). Consequently,
the fleet experienced a sharp increase in capacity. In
1990, the fleet consisted of 386 vessels and by 1996
it had increased to 727.
In December 1992, the current General Law
of Fisheries (Gobierno del Perú 1992) was
promulgated and forms the backbone of fisheries
management in Peru. The General Law devised
measures to prevent capacity building. Article 24,
for example, required new vessel entries to be
balanced by decommissioning older boats. Many
firms were authorised to build vessels only for the
human consumption fishery. These firms found,
however, means to divert effort to the anchoveta
fishery (Thorpe et al. 2000). Consequently,
overcapacity levels were again reached.
In 1998, the government passed Law 26920
(Gobierno del Peru 1998) which authorises owners
of boats larger than 30 m3 of fish-hold capacity to
harvest anchoveta for the fish meal industry. This
segment is known locally as the ‘Viking’ fleet due to
the wide shape of the hull. Law 26920 has partially
alleviated the economic needs of a sector of the
artisanal fleet but has substantially increased fleet
size up to 1200 purse seiners (see Fig. 1).
Currently, the pelagic industrial fleet
comprises two clearly differentiated segments: the
large-scale fleet and the wooden fleet. This fleet
sector is comprised mainly of steel vessels, larger
than 120 m3 carrying capacity. It is composed of 608
vessels with a combined fish-hold capacity of circa
180000 m3. The small-scale fleet ranges from 30 m3
to 119 m3 carrying capacity and comprises 592 purse
seiners with a combined fish-hold capacity of circa
32000 m3.
During recent years, great concern has arisen
regarding the fishing activities of the latter sector
due to the fact that part of the fleet lacks the
mandatory satellite-tracking devices. This renders
them prone to committing illegal fishing of
anchoveta for industrial purposes within 5 nautical
miles of the coast. By law, this zone is reserved for
artisanal fishing. Both segments of the fleet supply
raw material to 140 fishmeal plants scattered along
the Peruvian littoral.
Local researchers have realised that the
overcapacity of the industrial fleet generates a race
for fish behaviour that shortens fishing seasons and
increases running costs (Chavez 2000).
Overcapacity has also been a concern for the
stakeholders. In 1998, the National Society of
Fisheries, the most influential association of fishing
companies,
proposed
a
decommissioning
programme where firms wishing to stay in the
fishery had to buy out 25000 m3 from those firms
wishing to leave the trade. They suggested the
creation of a fund contributed to by fishmeal
producers with a fee of 10 dollars per tone of
fishmeal exported (Anon 1998). In 2007 the
association of boat owners, which represents the
small-scale operators, suggested to the government
to buy back capacity from boat owners wishing to
leave the activity. They suggest the creation of a
fund contributed to by all boat owners with a fee of
2 dollars per landed anchovy (PRODUCE 2007).
Since 2006 the levels of capacity exhibit
strong dynamics associated with changes in
ownership and the concentration of capacity by the
largest operators. For example, the seven largest
companies concentrate 50% of fish-hold capacity
(Arroyo 2007). As recently as 2007, fishing
149
companies invested $ 800 million dollars in buying
out fishing capacity to increase their participation in
the fishery (Anon. 2007).
Implementation of IVQs to enhance
capacity control. Incentive-adjusting measures to
counteract overcapacity such as Individual
Transferable Quotas (ITQs) were first proposed by
the World Bank in 1992 (Hidalgo 2002). In 2002,
the Vice-ministry of Production (former Ministry of
Fisheries) proposed the introduction of an ITQ
system in the fishery for anchoveta and sardine. In
June 2003, a new fisheries administration confirmed
to the local media the government’s willingness to
implement an ITQ scheme from 2004 (Anon 2003).
The proposal was finally shelved.
These measures have proven to be difficult
to implement due to strong opposition by certain
factions of fishermen and politicians due to their
belief that they will be detrimental to the social
fabric. Indeed, theoretically, ITQs may produce a
concentration of wealth in a few efficient hands by
expelling less efficient agents from the fishing
activity (del Valle et al. 2006).
In June 2008, the Presidency of the Republic
enacted Law 1084 (Gobierno del Perú 2008) entitled
‘Maximum Catch Limits per Vessel’. This new
management instrument can be categorised as an
incentive-blocking capacity measure which utilises
IVQs. It aims to control capacity and deter the race
for fish. The decision to introduce individual quotas
is a potential turning point in the management of this
fishery and has been welcomed by the National
Society of Fisheries, despite having faced opposition
from the Association of Boat Owners of the 26920
(PRODUCE 2007). The recently launched Peruvian
IVQ system is described in Aranda (2009).
The large-scale and the small-scale fleets are
eligible for initial allocation of a share of the Total
Allowable Catch (TAC). The rights allocation is
based on the best years of landings since 2004.
Rights allocation is carried out on a temporary basis;
the validity period of an allocated right is 10 years.
Rights are attached to the vessel itself and the
fishing license. Should a boat be withdrawn, its
remaining rights can be accumulated to other boats
belonging to the same boat owner. Should a boat not
fully utilise its rights in a given season, it cannot
carry over the remaining rights into the following
season.
The IVQ scheme assures rights-holders that
the management system will not changeby devising
the Contract of Permanence of the Management
System. This legal instrument may enhance security
and provide stakeholders incentives to invest in
modernisation of fleets and plants.The government
M. ARANDA
150
relies on such incentives to motivate stakeholders to
eliminate redundant capacity.
2,000
14,000
1,800
Vessels
12,000
anchovy
1,600
Fleet size
1,200
8,000
1,000
6,000
800
600
4,000
Anchovy landings (1,000 tons)
10,000
1,400
400
2,000
200
2006
2004
2002
2000
1998
1996
1994
1992
1990
1988
1986
1984
1982
1980
1978
1976
1974
1972
1970
1968
1966
1964
1962
1960
1958
1956
1954
1952
0
1950
0
Figure 2. Comparison between fleet size and anchovy landings 1950-2006. Data source: PRODUCE.
1,400
300
Vessels
Days
1,200
250
1,000
800
150
600
Fishing season
Fleet size
200
100
400
50
200
2006
2005
2004
2003
2002
2001
2000
1999
1998
1997
1996
1995
1994
1993
1992
1991
0
1990
0
Figure 3.Comparison between fleet size and the length of the fishing season. Source: PRODUCE
The IVQ system enhances the monitoring,
control and surveillance system (MCS) by
mandatory installation of satellite-tracking devices
(VMS) in every single vessel. Costs of the improved
MCS are to be recovered from the stakeholders. The
new management instrument also devises a variety
of provisions to counteract the social distress that
may arise from the IVQ approach, such as voluntary
retirement of crews and measures to provide labour
opportunities for crews outside the fishing activity.
The Peruvian IVQ model aims at stopping the race
for fish without allowing the full transferability of
rights and thus concentration of wealth amongst a
few operators. The choice of non-transferability,
however, may not substantially cut down
overcapacity (Arnason 2000).
Conclusions and final considerations
Due to the failure of regulated open access,
the management of fishing capacity in Peru has been
characterised by the implementation of measures
aimed at correcting rather then preventing capacity
accumulation. Throughout five decades of history,
managers have been unable to deter capacity
building in a fishery where resource abundance and
high international demand for fishmeal have
encouraged investment. In addition, governments in
the 1990s allowed capacity building to both support
the re-emergence of the industry and alleviate
distress in the small-scale fisheries. Due to these
measures the fleet has expanded to a size similar to
that prior to the big crash in the 1970s (Fig. 2). A
lack of a solid policy on the prevention of capacity
accumulation and the feeblenesses of the system to
withstand pressure from fishers are likely the main
causes of capacity accumulation throughout the
history of the fishery.
The introduction of the IVQ system is a
breakthrough in the management process and
establishes a well defined platform for the control of
capacity as it allocates rights only to licensed vessels
and does not allow new entries. It does not,
however, make provisions for voluntary or
mandatory withdrawal of redundant capacity either.
So, capacity levels may remain fairly constant or
only be reduced smoothly if stakeholders decide to
withdraw less viable units in order to reduce costs.
The provisions allowing the accumulation of
rights in cases of withdrawals of given boats may
result in some boat owners deciding to harvest their
quotas using fewer vessels. However, this fishery is
economically attractive. Large investments in
capacity building prove this point. Since the
purchase of vessels is the only way outsiders may
enter the fishery, it is likely that vessels and their
associated rights and licenses will attain high prices.
Thus it would be an incentive for rights holders to
not decommission their fishing vessels. In this
context, if the strict system of control of individual
catches fails, it could give raise to a new race for
fish.
The fear of the concentration of rights has
determined the non-transferability of the new
system. However, concentration is a phenomenon
that has taken place in the fishery anyway, especially
during the last 3 years. Complementary measures to
allow a certain degree of transferability among boat
owners may speed up fleet reduction since more
efficient agents will buy out rights and eliminate less
viable vessels. The case of the Icelandic
management system is a good example of this
phenomenon (Arnason 2008). Transferability also
151
provides flexibility to compensate surpasses in the
use of individual quotas since boat owners may buy
or rent quotas to compensate quota overshooting and
thus avoid discarding.
International examples such as the
Norwegian IVQ system show that boat owners try to
incorporate missing transferability (Hersoug et al.
2000). Hence, clear rules should be established to
allow accountable transferability. In addition,
incentives to decommission and even scrap less
viable vessels should be provided to permanently
eliminate the threat of a latent race for fish.
Acknowledgments
The author wishes to express his gratitude to
one anonymous reviewer and to his colleague Israel
Montoya at the Universidad Nacional Federico
Villarreal del Peru for his valuable aid in supplying
key information. The author is also indebted with
AZTI Tecnalia for its support in the writing of this
manuscript and with Paul de Bruyn for the revision
of the English. Any error remains the sole
responsibility of the author.
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Received September 2008
Size and number of newborn juveniles in wild
Hippocampus reidi broods
ANA CECÍLIA GIACOMETTI MAI1 & DANIEL LOEBMANN2
1
Laboratório de Ictiologia, Universidade Federal do Rio Grande - FURG, Av Itália km 8, CEP 96201-900, Rio Grande,
RS, Brazil. E-mail: anacecilia_mai@yahoo.com.br
2
UNESP, Rio Claro – SP, Instituto de Biociências, Laboratório de Herpetologia. Av. 24A, 1515, Bairro Bela Vista,
CEP 13506-900 Rio Claro, SP, Brazil. E-mail: contato@danielloebmann.com
Abstract. Four births of Hippocampus reidi Ginsburg, 1933 were monitored for the first time
under natural conditions. This study provides the fish estimate of fecundity in the wild, which is
an important parameter for assessing population dynamics and management strategies.
Key words: Seahorse, reproduction, fecundity, newborn size.
Resumo. Número e tamanho dos recém-nascidos de Hippocampus reidi em ambiente natural.
Quatro eventos de nascimento de Hippocampus reidi Ginsburg, 1933 foram acompanhados pela
primeira vez em ambiente natural. Este estudo traz a estimativa da fecundidade da espécie em
ambiente natural, que é um importante parâmetro para avaliar a dinâmica populacional e
estratégias de manejo.
Palavras-chave: Cavalo-marinho, reprodução, fecundidade, tamanho dos recém-nascidos.
Total reproductive success, ideally defined
as the lifetime total offspring to reach maturity (i.e.
to be able to breed), is the product of fecundity
(number of offspring produced per mating event),
number of mating events per season, adult
reproductive life span and offspring survival
(Clutton-Brock 1988). For seahorses, underwater
surveys and catch data has been recently utilized in
models to estimate the duration of the reproductive
season, female spawning frequency, male brooding
frequency, and batch fecundity (Curtis 2007).
In general, in most of the seahorses species,
the males release about 100 - 300 young per
pregnancy, but brood size can range from as few as
five, for the small species H. zosterae, to
approximately 2000 young by a single H. ingens
male (Foster & Vincent 2004). The present study
measures the number and size of juvenile H. reidi
under natural conditions.
During the period of December 2006 to
March 2007, throughout visual search method in the
borders of the Camurupim River estuary, Piauí state,
Brazil (UTM 0230727, 9676724; 24 M zone; Datum
WGS 84), males found with distended pouch were
encaged and monitored daily, until the offspring
birth. The cage was rectangular with dimensions of
30 x 30 x 45 cm, covered with mesh of 0.5 mm, and
containing an artificial holdfast for the male to
grasp. The algae Caulerpa sertularioides or
Enteromorpha sp. (and its associated fauna) were
offered in order to complement the diet of the
seahorses. Also, the cage was cleaned daily to avoid
the mesh clogging by micro algae and sediment.
This research was authorized by Brazilian Institute
of Environment and Renewable Natural Resources
(IBAMA - license number 10682-1).
From each male studied, the following
parameters were taken: the height of the individuals
measured according to Curtis & Vincent (2006) and
the size of the brood pouch. After giving birth, the
male was released to the same place where it had
been found. Simultaneously, the total number of
newborns was recorded. Ten individuals per brood
were randomly chosen and photographed with
Digital Machine (Cannon A620). The photographs
were analyzed with the software Image Tools for
Windows v. 3.0, making it possible to record the
size of newborns. After this procedure, the offspring
Size and number of newborn juveniles in wild Hippocampus reidi broods
were released in the environment.
During this study, three pregnant males were
monitored. In order to avoid pseudo-replication,
only the first brood recorded for each male was
included in the analysis, recognized by the presence
155
of nature tags. The monitored males ranged in height
from 15.1 to 16.5 cm (mean 15.6 cm) and the
newborns from 0.44 to 0.66 cm (mean 0.54 ± 0.051
cm; n= 30). Offspring number ranged from 202 to
652 (mean 375 ± 242.4; n= 3) (Table I).
Table I. Morphometric data of Hippocampus reidi from each reproductive male and their respective
offspring, birth date, and captivity period of the males in the cage.
A
A
B
C
Height (mm)
151
152
140
165
Pouch length (mm)
31.1
31.3
30.3
35.6
Birth date (month/day/year)
12/29/2006
02/09/2007
01/06/2006
03/15/2007
Days in the cage
3
1
6
6
Offspring number
202
274
652
271
Mean offspring height (mm)
5.4
4.9
5.1
5.8
Standard deviation in offspring height
0.38
0.61
0.41
0.56
Range in offspring height (mm)
5-5.9
4.1-6.1
4.4-5.7
5-6.6
There is no published data which describes
the reproduction of H. reidi in the wild (Rosa et al.
2002). On laboratorial conditions the number of
offspring ranged from 1000 to 1536 and measured
approximated 0.7 cm for H. reidi samples from
latitude 13oN (Vincent 1990). So, the fecundity and
the mean height of the newborns found in this study
are lower to those previously recorded. It is expected
a relationship between latitude and several lifehistory variables, mainly because environmental
factors such as temperature and photoperiod that
vary with latitude are known to affect the
physiological function in many species (Thresher
1988). According to Foster & Vincent (2004) the
size of the adults, eggs, and young increase with
increasing latitude, although brood size does not.
The male A had two events of pregnancy
monitored, with a number of 202 and 274 offspring
respectively, and showed a time interval of 42 days
between each born. The breeding season of H. reidi
extends for at least eight months (Vincent 1990). In
most study sites from Brazil H. reidi has been
reported as a species reproductively active yearround, however, peaked from October to February
(summer months) (Rosa et al. 2007). According to
Silveira (2000), which studied this species under
laboratorial conditions, a male is able to mate two
days after the birth of offspring and its pregnancy
lasted from 12 to 20 days, depending on the water
temperature. In this way, it is not possible to
conclude if the gap of 42 days between the
pregnancies of male A could characterize a
consecutive pregnancy.
The morphometric comparison of an adult
male with a newborn (Fig. 1a, b) shows that
although embryos and adults are similar in the
external aspect, some measurements showed an
expected and pronounced non-proportionality. For
example, although the newborns were 26 times
smaller than adults in height, juvenile head length,
and snout diameter were on average only 18 and 11
times smaller, respectively (Table II). This nonproportionality of newborn is important once it
allows the capture of bigger prey from the
mesoplancton (0.2-20 mm), as can be seen for many
other fish species.
Table II. Length relationships of adults and
newborns Hippocampus reidi. All measurements are
in millimeters.
Adult Newborn Adult/newborn
Height
136
5.14
26
Head length
32.8
1.86
18
Trunk length
56.1
1.66
34
Tail length
69.4
2.46
28
Snout diameter
4.6
0.42
11
Evidence suggests that many seahorse
populations are declining due to unsustainable
exploitation and more seahorse species have been
included in the World Conservation Union red list of
threatened species (IUCN 2007). Also, the genus
Hippocampus was listed by the Convention on
International Trade in Endangered Species of Wild
Fauna e Flora (CITES 2004). To the date, the
conservation status of Hippocampus reidi is
considered as ‘data deficient’ for IUCN’s red list.
For this reason, these findings may contribute to the
development of effective fisheries management
strategies for this species.
A. C. G. MAI & D. LOEBMANN
156
Figure 1. Specimens of Hippocampus reidi: a) brooding male and, b) newborn.
Acknowledgments
We are very thankful to Maria Cristina
Oddone (Secretaria Especial de Aqüicultura e Pesca
(SEAP), Brasília, DF) and Mônica G. Mai
(Universidade Federal de São Carlos) for revising
and improving the grammar and style of the
manuscript. To unidentified referees for valuated
suggestions on earlier versions of the manuscript.
This study was support for financial recourses from
PADI-Foundation. ACGM was supported by master
degree scholarship from the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior
(CAPES) and DL is supported by doctoral
scholarship from the Conselho Nacional de Pesquisa
e Desenvolvimento (CNPq).
References
Clutton-Brock, T. H. 1988. Reproductive success.
Studies of individual variation in contrasting
breeding systems. Chicago, IL: The
University of Chicago Press, 548 p.
Curtis, J. M. R. 2007. Validation of a method for
estimating realized annual fecundity in a
multiple spawner, the long-snouted seahorse
(Hippocampus guttulatus), using underwater
visual census. Fishery Bulletin, 105(3): 327-
336.
Curtis, J. M. R. & Vincent, A. C. J. 2006. Life
history of an unusual marine fish: survival,
growth
and
movement
patterns
of
Hippocampus guttulatus Curvier 1829.
Journal of Fish Biology, 68: 707-733.
CITES, 2004. Convention on International Trade
in Endangered Species of Wild Fauna e
Flora. Meeting of the nomenclature
committee Geneva (Switzerland), 19 August
2003. Project Seahorse, 5 p.
Foster, S. J. & Vincent, A. C. J. 2004. Life history
and ecology of seahorses: implications for
conservation and management. Journal of
Fish Biology, 65: 1-61.
IUCN, 2007. IUCN Red List of Threatened
Species - World Wide Web electronic
publication,
accessible
at
www.iucnredlist.org. (Accessed 07/19/2007).
Rosa, I. L., Oliveira, T. P. R., Castro, A. L. C.,
Moraes, L. E. S., Xavier, J. H. A.,
Nottingham, M. C., Dias, T. L. P., BrunoCosta, L. V., Araújo, M. E., Birolo, A. B.,
Mai, A. C. G. & Monteiro-Neto, C. 2007.
Population characteristics, space use and
habitat associations of Hippocampus reidi.
Size and number of newborn juveniles in wild Hippocampus reidi broods
Neotropical Ichthyology, 5(3): 405-414.
Silveira, R. B. 2000. Comportamento reprodutivo e
desenvolvimento inicial de Hippocampus
reidi Ginsburg, 1933 em laboratório.
Biociências, 8(1): 115-122.
Thresher, R. E. 1988. Latitudinal variation in egg
157
sizes of tropical and. sub-tropical North
Atlantic shore fishes. Environmental
Biology of Fishes, 21: 17-25.
Vincent, A. C. J. 1990. Reproductive ecology of
seahorses. PhD. Thesis. University of
Cambridge, Cambridge, 101 p.
Received February 2008
MARCEL MARTÍNEZ-PORCHAS1, LUIS RAFAEL MARTÍNEZ-CÓRDOVA2 & ROGELIO
RAMOS-ENRIQUEZ3
1
Centro de Investigaciones Científicas y de Educación Superior de Ensenada. CICESE. Departamento de Acuicultura.
Km. 107 Carretera Tijuana–Ensenada. 22860. Ensenada Baja California, México. Email: marcelmp_6@hotmail.com
2
Universidad de Sonora. Departamento de Investigaciones Científicas y Tecnológicas de la Universidad de Sonora.
DICTUS. Bldv. Luis Donaldo Colosio. 83000. Hermosillo, Sonora
3
Universidad de Sonora. Laboratorio de Análisis Clínicos e Investigación de la Universidad de Sonora. LACIUS. Bldv.
Luis Donaldo Colosio. 83000. Hermosillo, Sonora.
Abstract. Stress in fish has been widely studied. Cortisol and glucose are two of the most
common stress indicators. In spite of the extended use of these indicators and their acceptance,
some inconsistencies have been reported in the results of several experimental studies, much of
them associated to undefined and uncontrolled variables which may alter the response in secretion
of cortisol and glucose into the bloodstream. Most of those factors are not considered as direct
stressors but have an effect on the intensity of the response which makes them a source of error.
Some of those factors are related to metabolic changes in the organisms as an adaptation or
acclimation mechanism; other are extrinsic to the fishes; other sources of error are caused
unconsciously by the researcher during manipulation or due to inadequate control of variables, and
may lead to intrinsic changes. The present paper is a contribution on the review of the most
evident factors that may affect results when using cortisol and/or glucose as fish stress indicators.
Some suggestions to avoid or minimize erroneous results in such investigations are also presented.
Keywords: Blood chemistry, blood parameters, blood sugar, biochemical responses, corticoids,
stress indicators.
Resumen. ¿Cortisol y glucosa: fiables indicadores de estrés de los peces? El estrés en los peces
ha sido ampliamente estudiado. El cortisol y la glucosa son dos de los indicadores de estrés más
comunes. A pesar del extenso uso de estos indicadores y su aceptación, se han reportado algunas
inconsistencias en los resultados de muchos experimentos, algunos de ellos asociados a variables
que no son controladas, las cuales pueden alterar la respuesta de secreción de cortisol y glucosa.
Muchos de esos factores no son considerados estresores directos, pero tienen un efecto en la
intensidad de respuesta, lo cual los vuelve una fuente de error. Algunos de esos factores están
relacionados con cambios metabólicos en los organismos, como un mecanismo de aclimatación o
adaptación; otros son extrínsecos a los peces y otros más son causados inconscientemente por el
investigador mediante la manipulación o inadecuado control de variables, lo cual puede provocar
cambios intrínsecos. El presente manuscrito es una contribución en la revisión de los factores más
evidentes que pueden afectar los resultados cuando se usa cortisol y/o glucosa como indicadores
de estrés en peces y a su vez se mencionan algunas sugerencias para evitar o minimizar resultados
erróneos.
Palabras clave: Azúcar sanguínea, corticoides, indicadores de estrés, parámetros sanguíneos,
química sanguínea, respuestas bioquímicas.
Introduction
In recent years the concept of stress as
applied to fish has awaked the interest among
scientists dedicated to the research of environmental
influences on health (Barreto et al. 2006).
There are discrepancies from the different
authors about the stress definition. One of the most
accepted is described as chemical and physical
factors causing body reactions that may contribute to
disease and-or death (Rottmann et al. 1992). Stress
is also known as “the nonspecific response of the
body to any demand made upon it” (Selye 1973).
Although there are several definitions, most of them
refer to an “altered state” which increases the energy
demand. According to Selye (1985) stress should be
divided into two phases: “eustress” or the healthy
stress and “distress” or bad stress. Eustress occur as
a response of the organism undergoing situations
that provoke physiological changes that optimize its
biological performance, for example exercise.
Distress occurs when certain factor promotes
physiological changes into an organism that may
compromise organism’s integrity. Major part of
stress research is focused on distress phase.
The response to stress in fish is
characterized by the stimulation of the
hypothalamus, which results in the activation of the
neuroendocrine system and a subsequent cascade of
metabolic and physiological changes (Wedemeyer
1990, Lowe & Davison 2005). These changes
enhance the tolerance of an organism to face an
environmental variation or an adverse situation
while maintaining a homeostasis status (Mazeaud et
al. 1977, Pickering, 1981).
Under conditions of stress, the body of the
fish emits immediate responses recognized as
primary and secondary responses. The primary
response is the perception of an altered state by the
central nervous system (CNS) and the release of the
stress hormones, cortisol and catecholamines
(adrenaline and epinephrine) into the bloodstream by
the endocrine system (Randall & Perry 1992).
Secondary responses occur as a consequence of the
released stress hormones (Barton & Iwama 1991),
causing changes in the blood and tissue chemistry,
e.g. an increase of plasma glucose (Barton 1997,
Begg & Pankhurst 2004). This entire metabolic
pathway produces a burst of energy to prepare the
fish for an emergency situation (Rottmann et al.
1992).
Some plasma chemicals may be useful tools
to evaluate the health and/or stress condition of the
fishes (Sadler et al. 2000a, Campbell 2004, Wagner
& Congleton 2004). Because stress has been
reported to elevate plasma cortisol (Pottiner &
Mosuwe 1994, Wendelaar-Bonga 1997, Pottinger et
al. 2003, Haukenes et al. 2008) and glucose levels
(Silbergeld 1974, Wedemeyer & Yasutake 1977,
David et al. 2005), many researchers consider as a
“rule of thumb” that fishes undergoing stressful
situations exhibit plasmatic increases of cortisol and
glucose (Hattingh 1977, Balm et al. 1989, Barcellos
159
et al. 1999). In spite of the extensive use of cortisol
and glucose levels as stress indicators, there are
some inconsistencies in the results of various
experiments that in some cases would be attributed
to unknown situations.
This is a review on the effectiveness of
glucose and cortisol as stress indicators in fish and
we attempt to identify possible errors within
different
scenarios
and
make
some
recommendations.
Cortisol.
Cortisol is the principal glucocorticoid
secreted by the interrenal tissue (steroidogenic cells)
located in the head-kidney of teleost fish (Iwama et
al. 1999). This hormone is released by the activation
of the hypothalamus-pituitary-interrenal axis (HPI
axis) (Mommsen et al. 1999). When an organism
undergoes stress conditions, the hypothalamus
releases corticotropin-releasing factor (CRF) toward
blood circulation. This polypeptide further
stimulates secretion of adrenocorticotrophic
hormone (ACTH) from the anterior pituitary gland
(Fryer & Lederis 1986) which finally activates the
release of cortisol by the interrenal tissue
(Mommsen et al. 1999).
Cholesterol is the precursor of cortisol; this
sterol is transformed to pregnenolone by the action
of the enzyme P450 side chain cleavage (P450SCC)
in the inner mitochondrial membrane. Then
pregnenolone is further converted into 11deoxycortisol by steroidogenic enzymes and this
product is finally converted to cortisol by enzyme
11b-hydroxylase (Miller 1998, Castillo et al. 2008).
The secretion of cortisol is slower than
catecholamines, but its effects are more prolonged
(Gamperl et al. 1994a, b; Waring et al. 1996),
combining mineral and glucocorticoid actions to
restore homeostasis (Wendelaar-Bonga 1997, Maule
et al. 1993, Colombe et al. 2000). Cortisol activates
glycogenolysis and gluconeogenesis processes in
fish; but also causes that chromaffin cells increase
the release of catecholamines which further increase
glycogenolysis and modulate cardiovascular and
respiratory function (Reid et al. 1992, Reid et al.
1998). This whole process increases the substrate
levels (glucose) to produce enough energy according
with the demand.
Factors that can affect the intensity of
response. The intensity of response is not always
caused by a specific stressor in any experiment;
instead it may be modulated or affected by alien
factors that are not considered as direct stressors
(Frisch & Anderson 2005) but that may further
impact cortisol secretion (Fig. 1). Those factors that
affect/modulate the response may be from intrinsic
MARTINEZ-PORCHAS ET AL.
160
nature when some factors depend basically on the
genotype or phenotype of the organism and from
extrinsic nature when response is affected by
external factors.
Figure 1. Briefly view of the dynamics of cortisol and
catecholamine in the production of glucose. (+) means
positive modulation and (–) means negative modulation.
Intrinsic. Heritability is considered as a
modulator with progeny groups of high response and
low response showing a similar intensity of cortisol
secretion as their ancestors (Pottinger & Carrick
1999). Also age has been identified as one of those
factors (Pottinger & Mosuwe 1994), for example,
Sakakura et al. (2002) reported an increase of
immunoreactive cortisol concentrations during the
transition from larval to juvenile stage of yellowtail
(Seriola quinqueradiata). Pottinger et al. (1995)
identified sexual maturity as a factor related with the
intensity of response in fishes. Gilmour et al. (2005)
mentioned that cortisol response is variable even in
salmonid fishes of the same stock and that
subordinate organisms showed a higher response
than dominant ones; this is in agreement with Doyon
et al. (2003) report, where they documented that
socially subordinate salmonids exhibit enhanced
CRF mRNA in the preoptic area.
Another factor that may affect results is the
fact that in some cases cortisol is rapidly converted
into cortisone (Kime 1978) which is significantly
less immunoreactive than cortisol. Some authors
have reported increases in the concentrations of
plasma cortisone of stressed fishes (Weisbart &
McGowan 1984, Patiño et al. 1987, Pottinger et al.
1992).
Extrinsic. Extrinsic factors may affect a
variety of biochemical functions within the fish
organism such as cortisol biosynthesis and release
rates. Environmental color is reported to have an
effect on cortisol secretion (Van der Salm et al.
2004). A higher intensity of cortisol response is
documented in Pargus pargus acclimated in black
tanks as compared with those in gray and white
tanks when fish were exposed to crowding stress
(Rotllant et al. 2003).
In some species the magnitude of the stress
response varies with respect of a previous thermal
acclimation or acclimatization (Strange et al. 1977,
Stouthart et al. 1998, Lankford et al. 2003). As an
example Koldkjær et al. (2004) reported differences
in plasma cortisol of rainbow trout (Oncorhynchus
mykiss) when comparing results in warm months
versus cold months. Also Stouthart et al. (1998)
hypothesized that the rearing temperature for eggs
and larvae of fish can influence the induction of
cortisol response.
Differences in the intensity of response
might occur in domesticated organisms as compared
with non-domesticated ones (Jentoft et al.
2005). Nutritional status (Pottinger 1998; Pottinger
et al. 2003) is another factor that may affect the
response; for instance, serotonin which is a HPI axis
regulator increases when administered dietary
tryptophan (serotonin precursor) (Lepage et al.
2002, 2003).
Reid et al. (1998) made a review about the
adrenergic response in fish and mentioned that the
regulation in the production of stress hormones is
influenced by adverse internal or external conditions
in the history of the fish (anoxia, pollution, nutritive
stress, physical stress). This last argument can be
explained because those organisms require energy
and necessitate an “alteration in the capacity to
express the adrenergic stress response”.
The rate of cortisol clearance is another step
in the cortisol cycle that may be influenced by
environmental factors. Liver is the key organ for
cortisol disposal with the hepato-biliary system as
the main biochemical pathway for cortisol clearance
(Wilson et al. 1998, Vijayan & Leatherland 1990).
However the efficiency of that process is reported to
be altered by stress, salinity, maturity, nutritional
state, etc (Mommsen et al. 1999).
If a modulator of response is not identified,
experiments may provide erroneous results, thereby
it is indispensable to know cortisol basal levels of
any experimental species. There are species-specific
and stressor-specific cortisol values that may serve
as general guidelines (Barton & Imawa 1991,
Gamperl et al. 1994b, Iwama et al. 2006) to avoid
over or sub estimating the cortisol response (Table
I). We suggest standardizing physiological and
biochemical status off all experimental organisms
previously to the beginning of any experiment. For
instance: a prior acclimation of experimental fishes
to laboratory conditions (temperature, dissolved
oxygen,
water
quality,
nutritional
status,
photoperiod, size, weight, color and shape of
experimental containers); organisms should be from
the same progenies or at least from the same place of
collection. It also has been suggested that high
variability in response from one organism to another
(even from the same species) may be avoided by
using clonal groups of fishes (Plaut & Gordon
1994). However this is a difficult task and would not
be possible in many cases and also clonal groups
may be only useful in specific studies, for example
to test genetically modified organisms.
Although these are common sense
suggestions, sometimes these are not followed,
leading to abnormal results.
To illustrate this, fishes from polluted sites
may have a different response than those acclimated
to laboratory conditions. Organisms accustomed to
the harassing of predators will show a weak stress
response during the experiments as compared with
others that thrive in environments without predators.
There are other several situations that have an effect
on the stress response.
Acute and chronic stress. In experiments
of acute stress, the cortisol response is rapid but
regularly becomes weak or disappears some hours
after the exposure to stress (Davis Jr. & McEntire
2006).
In most fishes, cortisol reaches highest
concentration 1 hour after being stressed, and returns
to basal levels after 6 hours (Iwama et al. 2006).
Cortisol levels of red drum during some handling
procedures grew rapidly, but decreased to the basal
state within 48 hours (Robertson et al. 1987).
Common dentex (Dentex dentex) increased its
glucose and cortisol levels immediately after
handling and then returned to the basal level after 8
hours (Morales et al. 2005). Carp (Cyprinus carpio)
increased plasma cortisol when retained in anglers´
keep nets but returned to basal levels within 4 hours
(Pottinger 1998).
It has been suggested that after stress, the
cortisol levels of fishes return to basal levels to
avoid tissue damage (Wendelaar-Bonga 1997). This
damage has been observed in salmons, where high
levels of cortisol cause death in Pacific salmon
(Oncorhynchus spp) by tissue degeneration and
damage of homeostatic mechanisms (Dickhoff 1989,
Stein-Behrens & Sapolsky 1992). Thus, cortisol test
is a good option in acute stress experiments, but it is
indispensable to measure cortisol immediately after
stress and over time, because a single and/or a late
test will have a high probability to be far from the
real response.
In chronic-stress experiments some fish
showed a weak increase of cortisol (Barton et al.
161
2005, Fast et al. 2008) probably caused by
exhaustion of the endocrine system as a result of
prolonged hyperactivity (Hontela et al. 1992) or an
habituation of the organism to that condition. For
example, when an organism undergoes suboptimal
conditions for a considerable period of time, the
release of cortisol decreases because the interrenal
tissue of stressed fishes becomes less sensitive to the
action of ACTH or other pituitary hormones
(Vijayan and Leatherland 1990, Mommsen et al.
1999). This culminates in less cortisol secretion than
expected. In consonance, Barton et al. (1987)
observed that cortisol levels of juvenile rainbow
trout increased in acute exposure to stress, but
returned to basal after a chronic exposure.
Although there are exceptions (Gil-Barcellos
et al. 2006, Ramsay 2006), because in the absence of
the ACTH some other pituitary hormones can
increase the secretion of cortisol (Wilson et al.
1998).
For instance, different hormones such as
alpha-melanocyte-stimulating hormone (MSH),
endorphin from the pars intermedia (PI) (Lamers et
al. 1992, 1994; Metz et al. 2005) and some
sympathetic nerve fibers (Arends et al. 1999) have
been implicated in cortisol release during the chronic
phase in fishes, functioning as an emergency system.
However if the sub-optimal condition persists this
system may be also depleted.
Therefore, cortisol response would not be a
sufficient but rather a less reliable tool to examine
stress status after chronic stress experiments.
Previous experience to stress conditions
should also be considered as a chronic exposure,
which is another source of error that appears when
the fish has been acclimated to conditions of stress
or was acclimatizated to a certain stress factor in its
environment that the collector did not notice. Barton
et al. (2005) observed a less intense response of fish
acclimated to chronic confinement (70 ng mL-1) than
fish acclimated to low density (139 ng mL-1) when
submitted both to acute handling stress. Rainbow
trout (O. mykiss) submitted to a 6-week exercise
program showed less cortisol concentration than
unexercised trout when both were in rest condition
(Woodward & Smith 1985). Pickering & Pottinger
(1987b) hypothesized an acclimation of the HPI axis
assessed by changes in plasma cortisol levels.
Perhaps this means that the fish used to stress
require a lesser amount of cortisol to reach the same
quantity of energy (glucose).
On the other hand, Selye (1936) reported
that during the first 6-48 hours after an organism
undergoes adverse conditions it suffers changes in
blood chemicals (cortisol increase), which is called
162
Table I. Plasma cortisol values of different species of fishes before and after being stressed.
Cortisol (nmol/l)
Species
Stressor
Prestress
Poststress
Exposure
References
Atlantic char Salvelinus alpinus
Handling
5
449
Acute
Lyytikäinen et al. (2002)
Atlantic salmon Salmo salar
Sea lice challenge
99
339
Chronic
Bowers et al. (2000)
Atlantic salmon (diploid) Salmo salar
Confinement
27
151
Acute
Sadler et al. (2000b)
Atlantic salmon (triploid) Salmo salar
Confinement
27
124
Acute
Sadler et al. (2000b)
Brook trout (diploid) Salvelinus fontinalis
Handling and confinement
19
242
Acute
Benfey & Biron (2000)
Brook trout (triploid) Salvelinus fontinalis
2
146
Acute
Common carp Cyprinus carpio
Density
19
206
Acute
Ruane et al. (2002)
Pallid sturgeon
Confinement
5
16
Acute
Barton et al. (2000)
Pallid sturgeon Scaphirhynchus albus
Handling
5
8
Acute
Rainbow trout Oncorhynchus mykiss
Chemical exposure
49
110
Chronic
Benguira et al. (2002)
Rainbow trout (diploid) Oncorhynchus mykiss
77
698
Acute
Rainbow trout male Oncorhynchus mykiss
Trapping
16
380
Acute
Clements et al. (2002)
Rainbow trout female Oncorhynchus mykiss
Trapping
57
764
Acute
Clements et al. (2002)
Sea bream Sparus aurata
Crowding
13
358
Chronic
Ortuño et al. (2001)
Walleyes Stizostedion vitreum
Capture and transport
33-315
380-480
Acute
Scaphirhynchus albus
BEGINNING OF STRESS EXPOSURE
BIOCHEMICAL PARAMETERS
“general alarm reaction” (GAR). If those conditions
continue, blood chemicals return to normal (general
adaptation syndrome) due to some modifications in
163
the metabolism. But, if the stressful environment
prevails, the GAR symptoms appear again caused by
energy depletion (Fig. 2).
GENERAL ALARM REACTION
GENERAL ALARM REACTION
GENERAL ADAPTATION SYNDROME
EXHAUSTION
TIME
Figure 2. Biochemical responses of fishes undergoing chronic stress (Selye 1936). The responses change with respect
to time; the fish modifies and regulate the biochemical processes to restore the homeostasis (GAR), but the duration of
this mechanism depends on the availability of energy reserves.
When Pickering & Pottinger (1987b)
experimented with salmonids under crowding
conditions, they concluded that changes in cellular
composition were better stress indicators than
plasma cortisol levels. Likewise we agree with those
authors and recommend that cortisol may be a
primary stress indicator in acute rather than chronic
experiments. However cortisol may be reported as
complementary data of chronic experiments.
Chemicals. Several pollutants can stress the
fish, activating alarm reactions producing a primary
and a secondary response (Brown 1993). In Atlantic
salmon (Salmo salar), cortisol and glucose levels
increased after being exposed to high aluminum
concentrations (Ytrestøyl et al. 2001). Roche &
Bogué (1996) argued that one of the most frequent
responses in fish blood to specific chemical
intoxication is cortisolemia.
Nevertheless Wendelaar-Bonga (1997)
explained that “the exposure to chemicals may
directly compromise the stress response by
interfering with specific neuroendocrine control
mechanisms”. Some chemicals affect metabolic
pathways which eventually will influence neural and
interrenal tissue functions. In agreement with this
finding, it has been observed that cortisol secretion
can be affected by environmental contaminants
because xenobiotic chemicals such as DDT are
toxicants targeting multiple sites along the HPI axis,
resulting in secretion of less bioactive ACTH, which
in turn will promote a minor cortisol release from
the interrenal tissue (Aluru et al. 2004; Hontela
1997).
Several studies have corroborated the
impairment in the cortisol synthesis and secretion
due the action of chemicals. Gravel & Vijayan
(2006) studied the impacts of three pharmaceuticals
(acetaminophen, ibuprofen, and salicylic acid) in
rainbow trout and supported the hypothesis that
these pharmaceuticals disrupt steroidogenesis in fish
interrenal tissue. These findings were also tested in
vitro and observed that salicylic acid produced a
depression of ACTH stimulation in cortisol secretion
and a lower gene expression of steroidogenic acute
regulatory (StAR) protein, which is involved in
steroidogenesis of cortisol (Hontela 2006); the same
author also stated that StAR protein may be a
sensitive target of many environmental pollutants,
ranging from pesticides to pharmaceuticals. Also,
the expression of StAR and P450SCC decreased in
fish exposed to xenobiotics because they bind aryl
hydrocarbon–receptor (AhR), a cytosolic ligand-
164
induced transcription factor, with a consequent
depress of steroidogenic enzyme activity and finally
altering the cortisol production and secretion (Aluru
et al. 2005). Therefore many pollutants halt cortisol
secretion and even if the fish is under stress this will
probably not be reflected in cortisol response.
Pickering & Pottinger (1987a) observed that
the exposure of brown trout (Salmo trutta) to poor
quality water resulted in a 50% suppression of the
cortisol release. Brodeur et al. (1997) reported an
impairment of the cortisol stress-response in the
yellow perch (Perca flavescens) from polluted sites.
Langiano & Martínez (2008) did not observed any
change in plasma cortisol of neotropical fish
Prochilodus lineatus when exposed to different
concentrations of a glyphosphate-based herbicide at
different periods, while difference in glucose levels
were assessed.
These results suggest that the interrenal
response may be contaminant specific. Thus the
estimation of cortisol as a toxic stress indicator may
be in doubt, and if no response is observed in fishes
under obvious stressful conditions, then cortisol
should be replaced by more useful tests to evaluate
the effect of any chemical compound on any species.
To mention some examples: medium lethal dose
(LD50) (Sprague 1969), behavior (Sprague 1971),
histopathological indicators (Schwaiger et al. 1997),
blood parameters (Iwama et al. 1995) or enzymatic
activity (oxidative stress enzymes) (Pedrajas et al.
1995, Gorbi & Regoli 2004).
Anesthesia and Sampling. When sampling
cortisol in fishes, it is necessary to handle the
organisms. This handling eventually aware the
organism and provokes an alarm reaction altering
the level of pituitary hormones and thus increases
the possibilities to obtain less precise results.
Anesthetics have been used to reduce pain and
awareness, and thus avoid metabolism enhancement
(increase of cortisol or other parameters) in fish. To
this respect, Small (2003) documented that
anesthetics reduce or block the activation of HPI
axis, so blood chemicals would not be altered at
sampling process.
However, Flodmark et al. (2002) mentioned
that some anesthetics per se (i.e. tricaine and 2phenoxyethanol) are stressful and may raise plasma
cortisol. Similar conclusion was assessed by Barton
& Peter (1982) when observed that 2phenoxiethanol and tricaine increased blood cortisol
in the trout Salmo gairdneri. A possible explanation
for these abnormal results may be that oxygen
concentration in water significantly decreases when
an anesthetic is added and HPI axis is activated
rather than blocked (Bolasina 2006). Palić et al.
(2006) evaluated the effectiveness of three
anesthetics (MS 222, metomidate and enguenol) in
fathead minnows, concluding that MS 222 did not
block the activation of HPI axis, instead they had
better results using metomidate. Although 2phenoxiethanol and tricaine are the two most used
anesthetics, we do not recommend their use for
cortisol and glucose evaluation because of the
possibility of erroneous increased results.
Some anesthetics though have been shown
to halt secretion of cortisol. Clove oil showed to be a
strong blocker of cortisol increase in channel catfish
(Ictalurus punctatus) (Small 2003). In contrast, it
was documented that clove oil did not block cortisol
secretion in stressed sea bream (Pagrus major).
Isoeugenol was shown to diminish 60%
blood cortisol in channel catfish exposed to
confinement, whereas metomidate showed greater
effectiveness in blocking cortisol release under high
ammonium concentrations (Small 2004). Olsen et al.
(1995) intraperinoteally injected ACTH into Atlantic
salmon to promote cortisol secretion; they reported
that metomidate blocked cortisol release, whilst high
cortisol levels were found when using tricaine (MS
222). Metyrapone has also shown successful results
as a cortisol synthesis blocker (Hopkins et al. 1995).
However, metyrapone and etomidate halt cortisol
secretion by inhibiting 11β-hydroxylase, a key
enzyme in the conversion of 11-deoxycortisol to
cortisol (Dang & Trainer 2007). This hindrance in
the biochemical pathway of cortisol generation may
compromise physiological status of organisms
limiting adaptation capacity, and perhaps leading
them to death. In this case, these anesthetics may be
used if a single sample of every fish is required, for
example when fishes are sacrificed while sampling
(heart puncture), such as the case of small size
fishes. But, if more than one sample (from caudal
vein) of every fish is needed or the investigator does
not intend to sacrifice the animal (animal
management ethics), then it is not recommended to
use metyrapone nor isoenguenol, and maybe other
anesthetics constitute better options, perhaps
sacrificing precision for the survival of the
experimental organisms.
Results are very contrasting, the efficacy of
anesthetics seems to be species-specific and prior
tests would be required and report how much of the
cortisol response is due to anesthetic and how much
is due to the stressor.
It is also worth to mention that some of the
above studies only tested a single dose of anesthetic.
Thus it is unknown if the kind of anesthetic per se is
inefficient or the dose was not adequate. In a recent
experiment Welker et al. (2007) tested four
concentrations of MS 222 (0, 90, 120 and 180mg·l-1)
in the channel catfish and reported that the highest
cortisol level was found in the treatment without
anesthetic (0mg·l-1), but the treatment with the
highest level of anesthetic (180mg·l-1) also increased
the cortisol concentrations. The best results were
obtained with the dose of 90mg·l-1. Therefore, prior
tests should consider not only anesthetics
themselves, but also explore the adequate dose. Also
it is important to establish the time at which samples
should be taken, because apparently the time after
applying the anesthetic has an effect on the secretion
of cortisol. Welker et al. (2007) found that the MS
222 effectively blocked cortisol secretion of channel
catfish during the first 20 minutes after
anesthetizing, but the levels tended to increase after
25 minutes.
Water temperature is another point of
concern at the time of administering any anesthetic.
Park et al. (2008) proved the efficacy of clove oil in
anesthetizing fishes and their physiological
responses when administered it at different
concentrations and temperatures, finding that the
optimal dose (lower cortisol and glucose secretion)
decreased at higher temperatures.
Non invasive methods. Non invasive
methods have been used as indirect indicators of
stress. In 1994, Sorensen & Scott found that goldfish
released steroid to the water, and that one of those
steroids was cortisol. After that, the measurement of
cortisol in water to evaluate stress status in fish was
proposed (Scott et al. 2001). Ellis et al. (2004)
measured free cortisol released into water by
rainbow trout. Lower et al. (2005) tagged two
species of fishes, the common carp (Cyprinus
carpio) and the rutilus (Rutilus rutilus) reporting that
cortisol in water increased from 70 to 400 and from
170 to 2000 pg/g/h respectively.
This method has the advantage that fishes
are not stressed up when sampling due to null or
minimal intervention. Moreover there is no necessity
to bleed and hurt the animal to measure cortisol.
However Scott & Ellis (2007) pointed out that in
some cases cortisol in water is too low to be
measured by conventional methods, being necessary
to extract and concentrate cortisol from water,
because the highest proportion of cortisol is
eliminated through hepatic processes, while renal
and branchial routes play a secondary role in steroid
elimination (Idler & Truscott 1972, Butler 1973).
Scott & Ellis also suggested that only free cortisol
and not conjugated steroid fractions (sulphated and
glucuronidated steroids) have to be measured to
evaluate stress response, because “the concentration
of free steroid in the water equates to the
165
concentration of ‘physiologically active’ steroid in
the plasma, which is very close to the moment in
time that the sample is taken.
This method also faces the problem of fish
mass and water flow rate, because cortisol secretion
is in direct proportion to fish biomass and flow rate
modifies cortisol concentration. Thus, very similar
biomasses are required in every experimental unit,
together with calculations considering flow rate (see
Scott & Ellis 2007). Furthermore, the method can
not be used to measure individual cortisol levels,
unless tests of single organisms are carried out.
Despite those related problems, this method emerges
as an interesting alternative to substitute cortisol
measurements in plasma.
Another non invasive method to measure
cortisol is to measure it in feces. This procedure has
been reported by some authors, but with limited
success (Oliveira et al. 1999, Turner et al. 2003).
Also the major part of free cortisol releasing occurs
through the gills (Ellis et al. 2005). Despite the
advantage of being non intrusive, this method does
not have yet the precision of direct evaluations
(plasma cortisol levels; Huntingford et al. 2006) or
water cortisol measurement for what its use is of
limited practical value.
Glucose.
Glucose is a carbohydrate that has a major
role in the bioenergetics of animals, being
transformed to chemical energy (ATP), which in
turn can be expressed as mechanical energy (Lucas
1996).
In suboptimum or stressful conditions
(internal or external) the chromaffin cells release
catecholamine
hormones,
adrenaline
and
noradrenaline toward blood circulation (Reid et al.
1998). Those stress hormones in conjunction with
cortisol mobilize and elevate glucose production in
fish through glucogenesis and glycogenolysis
pathways (Iwama et al. 1999) to cope with the
energy demand produced by the stressor for the
“fight of flight” reaction. This glucose production is
mostly mediated by the action of cortisol which
stimulates liver gluconeogenesis and also halts
peripheral sugar uptake (Wedemeyer et al. 1990).
Glucose is then released (from liver and muscle)
toward blood circulation and enters into cells
through the insulin action (Nelson & Cox 2005).
Regardless of the wide use of glucose as an
indicator of stress, some authors (Mommsen et al.
1999, Flodmark et al. 2001) emphasized that care
has to be taken when using plasma glucose as the
only indicator. It has been reported that glucose
content is a less precise indicator of stress than
cortisol (Wedemeyer et al. 1990, Pottinger 1998).
166
Mommsen et al. (1999) were skeptical about the use
of glucose as a stress indicator, whereas Simontacchi
et al. (2008) stated that glucose and cortisol “cannot
be considered itself as reliable stress indicators”.
Factors that affect the intensity of
response. Similar to cortisol, some factors can
indirectly alter the response of glucose levels in
blood. Vijayan & Moon (1994) suggests that “the
rearing history including nutritional status may
affect the stress response and glucose clearance
rates”. That affirmation is supported by other
authors who concluded that blood glucose results
have to be interpreted with care, taking into account
extrinsic factors such as diet, life stage, time since
last feeding and season of the year, etc., because
they may affect liver glycogen stores (Nakano &
Tomlinson 1967, Barton et al. 1988, McLeay 1977,
Wedemeyer et al. 1990).
Nutritional status is a factor that can have an
effect in the glucose response. The intake of diets
with different lipid and protein content resulted in
different responses of blood glucose of the orangespotted Grouper (Epinephelus coioides) when it was
exposed to cold stress (Cheng et al. 2006). The
channel catfish under fasting conditions evidenced
hyperglycemia after 30 days of experiment (22.8
versus 4.7 ng·ml-1 in the control group) (Peterson &
Small 2004).
Glucose also varies between species and
stage of development (Iwama et al. 2004, Hemre et
al. 2002). Woodward & Strange (1987) observed
that wild rainbow trout experienced a cortisol
increase 3 times greater than hatchery fish when
exposed to net confinement and electroshock. To
avoid erroneous results we also suggest prior
standardization of organisms before any stress
experiment.
On the other hand as previously stated,
stress hormones such as catecholamines, cortisol
and others may be influenced by internal or
external conditions in the history of the fish
(anoxia, pollution, nutritive stress, physical stress)
(Reid et al. 1998). Cortisol is known to increase
blood glucose, herein a disruption in cortisol
secretion may conclude in an altered glucose
response.
However there have been observed increases
in blood glucose whilst cortisol secretion is impaired
(Costas et al. 2008). Some authors suggest that this
increase in glucose may be attributed to a different
mechanism of the action of cortisol, (catecholamine
action for instance) (Vijayan et al. 1991, 1994;
Trenzado et al. 2006). To this respect, it has been
demonstrated that catecholamines itself can increase
sugar levels (Wagner et al. 2003). Catecholamines
promote the phosphorylation of the enzyme
glycogen phosphorylase which results in a
glycogenolysis increase (Vijayan & Moon 1992);
then, if catecholamine production or secretion is
modified also glucose response may be affected.
When Nilsson (1989) exposed crucian carp
(Carassius carassius) to anoxic conditions (76-169
h), a significantly decrease in stored noradrenaline in
kidney head was observed. However Reid et al.
(1998) also concluded that those effects are
reversible under normoxic conditions.
As in the cortisol case it is indispensable to
know basal or pre-stress levels of the species to be
studied (Table II).
Energy demand. As mentioned, sugar
levels increase during stress, however some authors
reported a weak rise of glucose (Davis Jr. &
McEntire 2006), others found no change (Rotllant &
Tort 1997, Jentoft et al. 2005), and even a decrease
(Wood et al. 1990).
Sometimes no significant changes in plasma
glucose may be observed, because under stress the
fish is rapidly consuming the energetic substrates
generated (glucose) since the main function of the
central nervous system (CNS) is to maintain
homeostasis. West et al. (1993) argued that during
peak activity glucose use can increase by almost 30fold. However it is possible that fish exposed to
chronic stress suffer substrate depletion that leads to
a decrease on plasma glucose (Fig. 2).
The freshwater fish rohu (Labeo rohita)
exposed to high fenvalerate (an insecticide)
concentrations, presented the maximum glucose
level in the fourth day of exposure, but the level
began to decrease over time until depleted (David et
al. 2005). From those results, a weak or no change in
plasma glucose may be attributed to a high energy
demand so that glucose cannot be accumulated
(acute experiments) or the organism be habituated
(chronic experiments). A decrease of glucose is
linked to depletion of reserve energy. If it is not part
of the experiment, fishes should not be exercised
during experimental or acclimation period to avoid
an increase in energy demand; this caution will
reduce the risk to obtain abnormal results,
nonetheless glucose response is still more variable
than cortisol response.
Rapid measurements. Normally the
increase of glucose in plasma is not as rapid as for
cortisol. Many researchers documented an increase
of glucose minutes or days after the stress (Pratap &
Wendelaar-Bonga 1990, Hemre & Krogdahl 1996,
Barcellos et al. 1999, Falahatkar & Barton 2007)
because cortisol triggers glucose production.
Measuring glucose just after an acute experiment is
Glucose (mmol/l)
Species
Stressor
Prestress
Poststress
Exposure
References
Atlantic cod Gadus morhua
Nitrite exposure
0.17
0.23
Chronic
Bald notothen Pagothenia borchgrevinki
Temperature
4.5
10
Chronic
Siikavuopio & Sæther
(2006)
Lowe & Davison (2005)
Channel catfish Ictalurus punctatus
Handling
1.7
2.8
Acute
Welker et al. (2007)
Coral trout
Capture and handling
Chronic
Frisch & Anderson (2005)
1.6
7.9
Plectropomus leopardus
1.9
7.4
Emerald rockcod Trematomus bernacchii
Temperature
1.5
7.5
Chronic
Lowe & Davison (2005)
Matrinxã Brycon amazonicus
Handling and transportation
2.8
10
Acute
Urbinati & Carneiro (2006)
Nile tilapia Oreochromis niloticus
Electroshock
2.2
6.4
Acute
Barreto & Volpato (2006)
Nile tilapia
Social stressor
1.9
6.7
Acute
Barreto & Volpato (2006)
Rainbow trout Oncorhynchus mykiss
Pollutant
4.2
9
Acute
Miller et al. (2007)
Rainbow trout
Copper and air exposure
5.1
7.2
Chronic/Acute
Gagnon et al. (2006)
Sunshine bass Morone chrysops x saxatilis
Temperature and confinement
6.1
10.5
Chronic/Acute
Davis & Peterson (2006)
White sturgeon Acipenser transmontanus
Air exposure
1.6
1.7
Acute
Zuccarelli et al. (2008)
167
Plectropomus maculatus
Table II. Plasma glucose values of different species of fishes before and after being stressed. In every line is indicated if the kind of exposure to the
stressor was acute or chronic. When Chronic/Acute appears, it indicates that the fish was first acclimated to any condition and thereafter exposed to an
acute stressor.
168
considered a source of error, because there is the
probability of not measuring any change. For
instance, Perez-Casanova et al. (2008) increased
water temperature of Atlantic cod (Gadus morhua)
at a rate of 2°C·h-1 and measured glucose every 2°C,
not finding statistical differences from 10 to 24°C (a
critical temperature). These results appeared
probably because the change in blood glucose levels
might occurrs minutes, hours or even days later
(Langiano & Martínez 2008). Thus single measures
of glucose are not a real indicator, rather it is
recommended to measure glucose over time as in the
cortisol case.
For chronic experiments, the acclimation
period should be long enough to ensure that in case
of observing a null or weak glucose response, that
response is not caused by the general adaptation
syndrome (Fig. 2). Some authors suggest 3 weeks of
acclimation for laboratory experiments (Houston
1982; Johnsson et al. 2003), however this is not a
rule and may vary among species and stressors. Fast
et al. (2008) did not observe a rise of glucose in the
Atlantic salmon during acute experiments, but
reported an increase when the fish were exposed to
prolonged stress. A 3-week period of crowding
stress elevated cortisol and glucose in gilthead
seabream (Sparus auratus) (Tort et al. 1996).
Therefore, unlike in acute experiments, glucose can
be measured immediately after a chronic exposure to
stressful conditions.
Blood samples can be extracted during the
chronic experiments, but if the experimental units
are limited and all the samples have to be taken from
the same tanks, it is not recommendable to measure
cortisol over time, because the consequent handling
and manipulation of organisms may lead to
erroneous results in the future samples.
Nevertheless, if it is necessary to measure glucose
over time, it is recommended that sampling is not
very frequent, while a limited number of samplings
should be established.
Anesthesia
and
sampling.
Some
irregularities have been reported in glucose response
when anesthetics are used before sampling. The
ideal role of anesthetics is to minimize fish stress
response, prevent any negative impact on
performance and thus measure real values of glucose
or other blood components (Pickering 1998).
Nevertheless, some anesthetics do not fit with that
role. Ortuño et al. (2002) tested four anesthetics (MS
222, benzocaine, 2-phenoxytehanol and quinaldine)
in gilthead seabream and reported that basal glucose
level was 3.6 mmol·l-1 and increased to 5.6, 11.1,
11.9 and 16.4 mmol·l-1 when exposed to MS 222,
benzocaine, 2-phenoxytehanol and quinaldine
respectively; also immune response was depressed
by benzocaine and 2-phenoxyethanol, but not by MS
222 or quinaldine. In another experiment, Iversen et
al. (2003) exposed Atlantic salmon to other four
anesthetics (metomidate, clove oil, Aqui-S™ and
Benzoak®) not finding any increase in plasma
glucose. On the other hand, Velíšek et al. (2005)
reported a significant increase in rainbow trout
glucose when anesthetized with clove oil. Also clove
oil and MS 222 blocked cortisol secretion but
increased glucose in another experiment with
rainbow trout (Wagner et al. 2003). Those
controversial results suggest that perhaps anesthetic
efficacy in halting glucose increase is speciesdependant and also previous tests may be required
(see Anesthesia and sampling in cortisol section).
Other stress indicators.
Previously we documented that many
studies utilized cortisol and glucose as sole stress
indicators of stress in fish; however regarding the
several factors that can affect these responses give
us to consider that cortisol and glucose are not
enough as stress indicators. Iwama et al. (2004)
argued that “none of the current indicators of stress,
including the stress hormones, are 100% suitable in
reflecting stressed states in fish”; in consonance with
that, it is recommendable to complement cortisol
and glucose with other stress indicators to establish a
more complete profile of the experimental organism.
In the case of cortisol it is known that in
some fishes a small increase in plasma cortisol leads
to an alteration in amino acid metabolism (Hopkins
et al. 1995), for this reason it is plausible to consider
that the activity of those enzymes involved in amino
acid metabolism would be a complement or also a
more accurate indicators of stress even if cortisol
response is weak. Glutamine synthase for example,
has been observed to increase with small response of
cortisol (Reid et al. 1998).
Otherwise, it is possible to measure
intermediate enzymes of glycolysis (phosphoenol
pyruvate carboxykinase, fructose 1,6-biphosphate,
glucose 6-phosphatase), since cortisol and
catecholamines positively influence that process. For
instance, Vijayan et al. (2003) exposed rainbow
trout to cortisol treatments and reported an increase
in the abundance of phosphoenolpyruvate
carboxykinase (PEPCK) mRNA. DziewulskaSzwajkowska et al. (2003) documented an increase
of glucose 6-phosphatase when injected a high dose
of cortisol in the common carp.
However, there are other important
parameters that should be taken into account to
study stress. For instance catecholamines are
recognized as a stress indicator; adverse conditions
activates the HPI axis and catecholamines are
released into blood stream (Iwama 2007).
Melanocyte stimulating hormone (α-MSH) is a
peptide produced in the pituitary cells of several
fishes (Kawauchi et al. 1984; Lamers et al. 1991)
and proved to increase in stressful conditions
(Arends et al. 1999, 2000). Lactate is a chemical
compound that plays a role in anaerobic metabolism
of animals, produced from pyruvate via the enzyme
lactate dehydrogenase during exercise and is
considered as a stress indicator in fishes because its
levels are enhanced in under adverse situations
(Thomas et al. 1999; Grutter & Pankhurst 2000).
Eventually, fish also respond at the cellular
level to stressors. This response comprises some
protein changes, for example an enhancement in
heat shock protein (hsps) synthesis (Iwama et al.
1998, 2004). In cells of stressed organisms there is
an increase in the production of hsps which are
required to assist the folding of nascent polypeptide
chains, act as a molecular chaperone and mediate the
repair and degradation of altered or denatured
proteins to maintain homeostasis.
On the other hand, different non-invasive
methods can be used to complement the biochemical
and molecular parameters. The ventilation rate and
oxygen consumption represent an adequate
alternative because they are indicators of the
metabolic rate due to high activity, stress, etc.
However, Alvaenga & Volpato (1995) stated that
metabolic differences derived from social stress
usually show data with high variance, masking
important differences among treatments and that the
oxygen consumption and ventilation rate can
complement the stress studies. This method is very
simple and if the water is clear enough the
measurements can simply be determined visually. It
has been observed that the ventilation rate and
oxygen consumption increase with different
stressors such as, presence of predators, air
exposure, light intensity, etc. (Brown et al. 2005,
Sager et al. 2000, Thompson et al. 2008). However
despite ventilation rate is a very sensitive test, it has
the limitation that the severity of any stimulus or
stressor is not reflected in this parameter (Barreto &
Volpato 2004) and thus, it is only useful to indicate
if the fish is being stressed or not, but not how much.
Other non-invasive methods are the
measurement of the excretion of nitrogenous
compounds such as ammonia and urea, gas
exchange (carbon dioxide) and others (Walsh et al.
1994, Evans et al. 2003). These non-invasive
methods are good candidates to complement the
cortisol and glucose as stress indicators, although
they have the same limitation as the non-invasive
169
methods to measure cortisol (see above).
These suggestions are not a rule of thumb
and may be replaced or complemented with others,
depending on the nature of the stressor. In that
manner, false results obtained by using any
particular stress test may be validated or contrasted
with others.
Conclusions
Cortisol and glucose cannot be eliminated
from the stress indicators list, but due to their high
variability they must be complemented with other
measurements such as other stress hormones, hsps,
blood-cell
counts
(preferably
in
chronic
experiments), non-invasive methods and/or others,
in order to have a more complete profile about the
stress status of any fish.
Cortisol may be useful only in acute stress
experiments and monitored throughout time. To be
used as stress indicator, the physiological status of
organisms should be standardized.
Anesthetics
efficiency
shows
many
inconsistencies and there is controversy about the
convenience to use an effective metabolism blocker
anesthetic or a non harmful anesthetic due to animal
management ethics. It is important, as long as
possible, to select an adequate anesthetic according
to the species, which effectively blocks metabolism
while causing a minimum damage to the animal
integrity. The dose of the anesthetic and the water of
temperature are subjects of concern.
Non invasive methods such as measuring
cortisol in water are a suitable alternative to avoid
anesthetic problems.
Glucose
measurements
show
many
inconsistencies and should be a complement of
stress tests rather than a main indicator. It also can
be used as a tool to provide a point of reference for a
particular species.
Results may be more realistic if
standardization of organisms and experimental
conditions are done, and organisms are not exercised
prior sampling blood.
Repeated glucose measures have to be done
during or after acute exposures, but during chronic
experiments the sampling should not be very
frequent, because the handling and manipulation of
organisms may affect the future measurements.
In using both cortisol and glucose as stress
indicators the researcher needs to be careful to
identify possible situations or factors that may
influence the stress response of the fish as long as
possible and to be certain they are not part of the
experiment. On the other hand, the use of these two
indicators as pollution or toxic stress indicators is
170
not adequate, rather behavior and oxidative stress
tests are recommended.
Finally in the scientific task of monitoring
stress, the reliability of the results may be
significantly increased if adequate and enough
number of tests is carried out.
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Received January 2009
Accepted March 2009
Published online May 2009
Aspectos biológicos do peixe-olhudo-dentinho, Synagrops bellus
(Actinopterygii: Acropomatidae), da plataforma externa e talude
superior do estado de São Paulo, Brasil.
TEODORO VASKE JÚNIOR1, ALINE FREIRE TEIXEIRA2 & OTTO BISMARCK
FAZZANO GADIG2
1
UNESP, Campus Experimental do Litoral Paulista, Praça Infante Dom Henrique s/n CEP: 11330-900 São Vicente SP.
Email: vaske@ig.com.br
2
UNESP, Campus Experimental do Litoral Paulista, Praça Infante Dom Henrique s/n CEP: 11330-900 São Vicente SP.
Resumo. São apresentados aspectos biológicos do peixe-olhudo-dentinho, Synagrops bellus, que
ocorre em regiões de quebra de plataforma e talude superior na costa de São Paulo, sudeste do
Brasil. A espécie representou cerca de 71,6% e 9,7% em número das capturas realizadas com rede
de arrasto de fundo nas isóbatas de 300 m e 500 m, respectivamente. Os tamanhos de 266
exemplares variaram entre 130 e 265 mm de comprimento total, com proporção de 55,9% de
machos e 44,1% de fêmeas, onde a maior parte dos exemplares encontrava-se em maturação.
Foram encontrados 22 itens alimentares com destaque para peixes Myctophidade, camarões
Penaeidea e Caridea, megalopas de Brachyura, estomatópodes, cefalópodes Enoploteuthidae e
Cranchiidae, e pterópodes e tunicados. O quociente intestinal tende a diminuir com o aumento de
tamanho do corpo e o número de rastros branquiais está entre 16 e 17. A relação pesocomprimento foi de PT = 6,0x10 -6 x CT3,12, r 2 = 0,9495. Synagrops bellus é um importante elo de
transferência de energia entre o zooplâncton e micronécton, e os grandes predadores demersais e
pelágicos na quebra de plataforma no sudeste do Brasil.
Palavras-chave: peixe, águas profundas, alimentação, reprodução, relação peso-comprimento,
Abstract. Biological aspects of the blackmouth bass Synagrops bellus (Actinopterygii:
Acropomatidae), from the outer shelf and upper slope of São Paulo State, Brazil. Biological
aspects of the blackmouth bass Synagrops bellus from the outer shelf and upper slope along the
coast of São Paulo, southeastern Brazil, are presented. The species represented about 71.6% and
9.7% in number of the total catch performed by balloom trawl in the isobaths of 300m and 500m
respectively. Body sizes of 266 individuals ranged between 130 and 265mm total length, with sex
ratio of 55.9% males, and 44.1% females, where most individuals were in maturation stage.
Twenty two food items were found, pointing out Myctophidae fishes, Penaeidea and Caridea
shrimps, Brachyuran megalopae, Enoploteuthidae and Cranchiidae cephalopods, pteropods and
tunicates. The intestinal coefficient increases as the body size increase, and the number of gill
rakers ranged between 16 and 17. Length-weight relationship was WT = 6.0x10-6 x TL3.12, r 2 =
0.9495. Synagrops bellus is an important link between zooplankton and micronekton, and
demersal and pelagic predators in the outer shelf and upper slope in southwestern Brazilian coast.
Key words: fish, deep water, feeding, reproduction, length-weight relationship
Introdução
Desde o começo do Programa REVIZEE em
1995, um estudo abrangente dos recursos vivos da
Zona Econômica Exclusiva foi realizado ao longo da
costa brasileira, incluindo regiões de borda de
talude, onde muitas espécies tinham suas ocorrências
desconhecidas. Dentre elas, os peixes do gênero
Synagrops (família Acropomatidae), representado
por onze espécies, duas das quais, S. bellus e S.
spinosus, registradas em águas brasileiras
(Figueiredo & Meneses 1980, Haimovici et al. 1994,
Carvalho Fo 1999, Figueiredo et al. 2002, Perez et
VASKE JUNIOR ET AL.
180
al. 2003, Mincarone et al. 2004, Muto et al. 2005,
Costa et al. 2007), onde costumam ocorrer em águas
profundas na plataforma externa e talude superior.
Synagrops bellus (Fig. 1) é a maior espécie do
gênero atingindo até 30 cm, com distribuição no
Atlântico ocidental, desde o Canadá até o Rio
Grande do Sul (Mejia et al., 2001). Esta espécie
representa entre 29 e 44% do total da captura em
peso de peixes entre 250 m e 350 m no sul do Brasil
(Haimovici et al. 1994).
Figura 1. Peixe-olhudo-dentinho, Synagrops bellus, coletado no talude do estado de São Paulo.
Apenas mais recentemente, foi dada mais
atenção aos recursos de plataforma externa e talude
superior, através dos levantamentos faunísticos
realizados no âmbito do Programa REVIZEE
(Figueiredo et al. 2002, Haimovici et al.
2004, Bernardes et al. 2005, Muto et al. 2005, Costa
et al. 2005). O fundo da plataforma externa
e talude superior ao largo de Santos se
apresentam com predomínio de áreas planas, com
raras protuberâncias, composto basicamente por
areia lamosa e lama arenosa (Figueiredo &
Madureira 2004), que facilitam o arrasto de fundo.
Estudos de alimentação de peixes demersais de
profundidade no sudeste do Brasil ainda são
escassos, entre os quais se destaca uma análise sobre
a
composição
de
dieta
e
comparações
intraespecíficas para nove espécies de peixes (Muto
et al. 2005), e também para outras três espécies
representativas da ictiofauna onde a espécie
congênere S. spinosus foi analisada (Nascimento
2006).
No intuito de dar seguimento aos estudos de
peixes de profundidade da região sudeste, o presente
trabalho analisa dados biológicos de S. bellus da
costa de São Paulo, particularmente a composição
por tamanhos, alimentação, aspectos de maturação
gonadal, e relação peso-comprimento, visando a
obtenção de informações biológicas básicas da
espécie, até então desconhecidas para a costa
brasileira.
Material e Métodos
As amostras foram obtidas em dezembro de
2007 pelo NPq “Soloncy Moura” (CEPSULIBAMA), durante dois arrastos realizados cada um
ao longo das isóbatas de 300 m e 500 m ao largo de
Santos no estado de São Paulo (Fig. 2). Foi utilizada
uma rede de portas para arrasto profundo, do tipo
balloom trawl de 439 malhas, 160 mm na boca e 70
mm no sacador. Os arrastos foram efetuados entre 9
h e 13 h nas posições 26º21’S; 46º23’W e 25º50’S;
46º47’W. Para o propósito deste estudo, os
exemplares coletados nas duas posições foram
analisados em conjunto. A duração de cada arrasto
foi de 30 minutos com velocidade do navio entre
dois e três nós.
Imediatamente após a captura, os peixes
foram congelados a bordo e posteriormente o
comprimento total (CT) de cada peixe foi medido
em milímetros e o peso úmido total (PT) em gramas
em laboratório. Após as tomadas de medidas e peso,
e determinação de sexo, os estômagos foram
removidos e preservados em solução de formalina 4
%. Após o descongelamento das gônadas foi
determinado o estágio de maturação de cada
exemplar, descartando-se os exemplares duvidosos.
Os itens alimentares foram identificados ao menor
táxon possível, contados, medidos em mm e pesados
em centésimos de grama.
O conteúdo estomacal de cada predador
incluiu lista de itens alimentares e grau de repleção
estomacal conforme a seguinte escala: I – vazio; II um quarto preenchido; III - metade preenchido; IV três quartos preenchido; V – cheio.
A importância de cada presa nos conteúdos
estomacais foi obtida através do Índice de Importância
Relativa (IRI) modificado para peso (Pinkas et al.
1971):
IRIi = %FOi x (%Ni + %Pi)
onde:
% FOi - porcentagem da freqüência de ocorrência de
cada item
% Ni - porcentagem em número de cada item
% Pi - porcentagem em peso de cada item
Para o cálculo de IRI não foram
considerados como conteúdo os bicos isolados de
cefalópodes, evitando-se assim a sobrestimativa em
número deste grupo (Vaske & Rincón 1998). No
entanto, para o estudo do tamanho das presas
ingeridas, os bicos foram utilizados para se obter o
comprimento do manto do cefalópode predado. As
equações de regressão utilizadas para se estimar o
manto dos cefalópodes a partir dos bicos foram as
obtidas por Clarke (1986).
Uma
relação
peso-comprimento
foi
determinada para 266 exemplares de ambos os
181
sexos, conforme a equação potencial:
PT = a CT b
onde PT é o peso total úmido (g), CT é o
comprimento total (cm), “a” é a constante, e “b” é o
coeficiente
alométrico.
O
coeficiente
de
2
determinação de Pearson (r ) foi usado para indicar a
qualidade da regressão.
A escala de maturação sexual macroscópica
de Vazoller (1996) foi usada para analisar o grau de
maturação gonadal conforme quarto estágios: A –
imaturo, quando não é possível distinguir
diferenciação de sexo; B – em maturação, com
ovócitos em vitelogênese e produção de
espermatozóides; C – maturo, com gônadas
ocupando 2/3 da cavidade abdominal, gônada fêmea
cilíndica, vascularizada e ovócitos grandes, gônada
macho, esbranquiçada, volumosa; D – desovada, e E
– em repouso, gônadas flácidas e esvaziadas.
O número de rastros branquiais e o
Quociente Intestinal (QI) foram obtidos para se ter
idéia da preferência por determinados tipos de presas
(Zavala-Camin 1996):
QI = CI / CT
onde:
CI = comprimento do intestino (cm)
CT = comprimento total (cm)
Figura 2. Localização (X) da procedência das amostras de Synagrops bellus, na região do talude do estado de São
Paulo..
Resultados
A espécie representou 71,6% em número do
total de peixes capturados no arrasto de 300 m e
9,7% dos peixes de 500 m. Os comprimentos totais
de 266 S. bellus variaram entre 130 e 265 mm, com
uma moda evidente entre 180 e 190 mm (Fig. 3). A
relação peso-comprimento obtida para 266
exemplares com sexos agrupados é apresentada na
Figura 4.
Um total de 201 estômagos foi aproveitado
VASKE JUNIOR ET AL.
182
para análise, onde 22 itens alimentares foram
identificados, dos quais oito representantes de
cefalópodes, dez crustáceos, dois peixes, um
pterópode, e um tunicado (Tabela I). De acordo
com a classificação por IRI, peixes Myctophidae
foram o principal item alimentar de S. bellus,
apesar de peixes terem sido pouco representativos
em diversidade na dieta. A seguir vieram camarões
Penaeidea e Caridea, megalopas de Brachyura,
estomatópodes, os cefalópodes Enoploteuthidae e
Cranchiidae, e os pterópodes e tunicados. Todos
os organismos foram representados por formas
larvais e jovens, com exceção de Brachyscelus
crusculum, Phronima sp., e Cavolinia sp. Houve
uma notável presença de bicos acumulados do
polvo epipelágico Ocythoe tuberculata. Sua
presença nos estômagos se deu na forma de um a
cinco pares de bicos, cujas regressões resultaram em
polvos jovens entre 4,3 e 5,7cm de comprimento de
manto.
n=266 média = 190,3 mm
25
20
15
%
10
5
0
120 130 140 150 160 170 180 190 200 210 220 230 240 250 260 270
Comprimento total (mm)
Figure 3. Distribuição de comprimentos de Synagrops bellus no sudeste do Brasil.
250
n = 266
y = 10 - 6 x 3,12
r2 = 0,9495
Peso total (g)
200
150
100
50
0
0
50
100
150
200
250
300
Comprimento total (mm)
Figure 4. Relação peso-comprimento para Synagrops bellus no sudeste do Brasil.
Em
sete
exemplares
selecionados
aleatoriamente com comprimentos entre 14,5 e 23
cm, foram contados os rastros branquiais que
totalizaram 16 unidades, com exceção de um
exemplar que apresentou 17 rastros. Nos mesmos
sete exemplares o QI apresentou uma tendência de
diminuição a medida que a espécie aumenta de
tamanho (Tabela II).
Os comprimentos corporais dos itens
alimentares variaram entre 5 e 75 mm, sem
tendência clara de preferências por tamanhos
(Fig. 5). Os graus de repleção estomacal de
201 estômagos estiveram representados por
35,8% de estômagos vazios e 64,2% com
presença de alimento (Fig. 6). Para 136 peixes, a
razão sexual foi de 76 fêmeas (55,9%) e 60 machos
(44,1%). Os estágios de maturação gonadal foram
possíveis de se observar em 33 exemplares
machos, com 48,5% no estágio A e 51,5% no
estágio B. Para 29 fêmeas as proporções foram de
27,6% no estágio A, 68,9% no estágio B e 3,5% no
estágio C.
183
Tabela I. Porcentagem em número, peso, e frequência de ocorrência dos itens alimentares de Synagrops
bellus. Os dez itens mais importantes conforme IRI são enumerados de 1 a 10.
Itens alimentares
N
%N
P
%P
FO
%FO
IRI
Enoploteutis anapsis
Enoploteutis leptura
Cranchiidae
Ocythoe tuberculata
Histioteuthidae
Japetella diaphana
Cephalopoda
Argonauta sp.
Cefalópodes
Penaeidae
Brachyura (megalopa)
Caridea
Stomatopoda
Nephropidae
Decapoda
Scyllaridae
Copepoda
Brachyscelus crusculum
Phronima sp.
Crustáceos
Myctophidae
Teleostei
Peixes
Cavolinia sp.
Tunicata
Outros
TOTAL
9
6
8
6
6
2
1
1
39
32
14
11
6
2
3
1
2
2
1
74
40
12
52
2
1
3
168
5,4
3,6
4,8
3,6
3,6
1,2
0,6
0,6
23,40
19
8,3
6,6
3,6
1,2
1,8
0,6
1,2
1,2
0,6
43,90
23,80
7,10
30,90
1,20
0,60
1,80
100
10
6,2
1
13,80
8,60
1,40
0,1
0,10
17,3
9,1
6,1
6,9
1,4
2,5
0,2
2
0,1
1
0,1
29,4
18,8
7
25,8
0,1
0,1
0,2
72,7
23,90
12,50
8,50
9,50
1,90
3,40
0,30
2,70
0,10
1,40
0,10
40,40
25,90
9,60
35,50
0,10
0,10
0,20
100
8
4
6
6
3
2
1
1
6,6
3,3
4,9
4,9
2,5
1,6
0,8
0,8
6
7
8
10
23
12
10
6
2
3
1
2
1
1
18,80
9,80
8,20
4,90
1,60
2,50
0,80
1,60
0,80
0,80
2
4
5
9
35
13
28,70
10,70
1
3
2
1
1,60
0,80
Tabela II. Dados de Quociente Intestinal (QI) e número de rastros branquiais para sete indivíduos de
Synagrops bellus.
Comprimento
CT (cm)
do intestino (cm)
QI
Rastros
14,5
12
82,76
16
15,5
10
64,52
17
17
12
70,59
16
17
12
70,59
16
17,5
13
74,29
16
23
15
65,22
16
23
16
69,57
16
VASKE JUNIOR ET AL.
184
n = 49
média = 37,1 mm
25
20
15
%
10
5
0
10
20
30
40
50
60
70
80
90
100
Comprimento das presas (mm)
Figura 5. Comprimento das presas de Synagrops bellus.
45
40
35
30
25
%
20
15
10
5
0
I
II
III
IV
V
Repleção estomacal
Figura 6. Graus de repleção estomacal de Synagrops bellus.
Discussão
Apesar da representatividade e constância
em arrastos de águas profundas ao longo da costa
sudeste-sul, a espécie não é aproveitada
comercialmente. No entanto, é parte importante no
ecossistema de quebra de talude, evidenciado pelo
espectro alimentar que a caracteriza como predadora
de organismos pelágicos de pequeno porte (dezenas
de mm). Synagrops bellus apresenta corpo robusto,
olhos grandes, dentição forte, e cauda furcada, que
lhe conferem capacidade para investir com
eficiência sobre suas presas na coluna d’água. Por
outro lado, faz parte da dieta de outros predadores
demersais locais como Polymixia lowei e chega a ser
o terceiro item em importância na dieta de Lophius
gastrophysus (Muto et al. 2005). Também é parte
integrante da dieta de grandes predadores pelágicos
do sudeste e sul do Brasil como Thunnus albacares
(Vaske Jr & Castello 1998, Zavala-Camin 1981),
Xiphias gladius (Zavala-Camin 1981, Mello 1992),
Istiophorus platypterus, Tetrapturus albidus
(Zavala-Camin 1981) e Thunnus obesus (Mello
1992), funcionando como um elo de transferência de
energia entre o zooplâncton e micronécton, e os
predadores topo do ecossistema pelágico. O fato de
ser presa constante de grandes predadores evidencia
que S. bellus faz deslocamentos verticais
consideráveis na coluna d’água, o que lhe é
vantajoso para obter um espectro alimentar
heterogêneo como o observado, mas também a torna
presa potencial para grandes predadores.
Nascimento (2006) analisou 953 estômagos
da espécie congênere Synagrops spinosus na mesma
região, dos quais 197 com conteúdo, encontrando
peixes, crustáceos e cefalópodes, onde o item
crustáceo foi estudado mais detalhadamente. A alta
porcentagem de estômagos vazios (66%) encontrada
por Nascimento (2006) foi atribuída a um provável
horário de alimentação mais intensa nas amostras de
período noturno. No presente estudo, a maioria dos
estômagos continha alimento no horário de coleta
diurno, no entanto, para se inferir horários de
alimentação em ambientes entre 300 e 500 m onde a
luz praticamente não faz diferença ao longo do dia,
seriam necessários arrastos em horários definidos,
onde é provável que a disponibilidade de presas
possa estar associada à grande migração vertical
diária do micronécton. Dentre os principais itens
alimentares de S. bellus destacam-se organismos que
realizam grandes migrações verticais diárias em
quebras de plataforma como Myctophidae,
Enoploteuhidae, Cranchiidae, Histioteuthidae, entre
outros. Se a estratégia de S. bellus for de se deslocar
na coluna dágua acompanhando a migração do
micronécton, é provável que os períodos de
alimentação mais intensa sejam entre a madrugada e
crepúsculo, como observado por Nascimento (2006),
para S. spinosus.
Em relação a presença do polvo epipelágico
Ocythoe tuberculata, restrito ao ambiente
epipelágico (0 a 150 m) (Roper & Young 1975), e
comumente encontrado em conteúdos estomacais de
grandes peixes pelágicos, como atuns e agulhões
(Vaske Jr. & Castello 1998, Vaske Jr et al. 2004),
pode-se inferir que S. bellus faz incursões no
epipelágico com certa freqüência, já que S. bellus é
caracterizada como espécie demersal-pelágica
(Haimovici et al. 1994). Dessa forma, se O.
tuberculata é restrito as camadas superficiais, a sua
presença na alimentação de S. bellus é um indicativo
que evidencia a constante migração vertical na
coluna d’água de S. bellus, embora provavelmente se
concentre na maior parte do tempo em águas mais
profundas, como observado em outras capturas
(Haimovici et al. 1994, Mincarone et al. 2004, Muto
et al. 2005). Não foi capturado nenhum exemplar em
outras artes de pesca utilizadas na região e que
trabalham com iscas como pargueiras, espinhel de
fundo e armadilhas (Haimovici et al. 2004, Martins
et al. 2005), devido a uma provável limitação de
tamanho de boca com o tamanho das iscas
empregadas nas artes de pesca.
Pela observação de que intestinos mais
curtos e algumas unidades de rastros branquiais
possam ser indicativos de hábito mais carnívoro
(Zavala-Camin 1996), é provável que na amplitude
de tamanhos aqui estudados, os peixes tenham uma
preferência por presas com maior massa muscular.
Segundo Nascimento (2006), S. spinosus pode ser
considerado como consumidor secundário que
realiza migrações na coluna d’água, onde jovens
preferem se alimentar de pequenos crustáceos no
fundo e adultos preferem mais peixes e cefalópodes
na coluna d’água. Um estudo futuro de QI com
tamanhos mais representativos de larvas, jovens e
adultos, poderá confirmar se o QI é maior nessas
fases em relação às presas encontradas.
A maior parte dos estágios de maturação
observados estava na fase de maturação. De acordo
com Sinque & Muelbert (1997) larvas de Synagrops
sp. são observadas no estuário de Rio Grande (RS)
em períodos de forte entrada de água salgada, o que
pode ser um indício de que indivíduos maturos
desovem em águas de plataforma externa e migrem
nas fases jovens e adultas para a quebra do talude,
185
uma vez que exemplares adultos não são
encontrados em profundidades até 119 m no sul do
Brasil (Haimovici et al. 1996). Dessa maneira, S.
bellus parece ser uma espécie abundante em quebras
de plataforma, sobretudo em torno da isóbata dos
300 m, exercendo papel importante como presa e
predador na transferência de energia nesse
ecossistema.
Agradecimentos
Os autores são gratos à tripulação do NPq
“Soloncy Moura”(CEPSUL-IBAMA), e aos
professores e alunos da UNESP-CLP que
colaboraram nas coletas durante o embarque.
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Accepted March 2009
First confirmed record of the blunthead puffer, Sphoeroides
pachygaster (Osteichthyes: Tetraodontidae) off the Algerian coast
(south-western Mediterranean)
FARID HEMIDA1, MOHAMED MOURAD BEN AMOR2 & CHRISTIAN CAPAPÉ3
1
Ecole Supérieure des Sciences de la Mer et de l’Aménagement du Littoral (ESSMAL), BP 19 Bois des Cars, 16320
Dely Ibrahim, Algiers, Algeria. Email: hemidafarid@yahoo.fr
2
Institut National des Sciences et Technologies de la Mer, port de pêche, 2060 La Goulette, Tunisia. Email:
benamor7@yahoo.fr
3
Laboratoire d’Ichtyologie, Case 104, Université Montpellier 2, Sciences et Techniques du Languedoc, 34095
Montpellier cedex 5, France. Email: capape@univ-montp2.fr
Abstract. A blunthead puffer Sphoeroides pachygaster (Müller & Troschel, 1848) was recorded
for the first time in the Algerian waters, off the eastern region close to the Tunisian border. The
specimen was an adult male; it measured 330 mm in total length and weighed 650 g.
Key words: distribution, migration, Algerian ichthyofauna, Maghreb shore.
Resumo. Primeiro registro confirmado do baiacu Sphoeroides pachygaster (Osteichthyes:
Tetraodontidae) na plataforma argelina (sudoeste do Mediterrâneo). Um exemplar do baiacu
Sphoeroides pachygaster (Müller & Troschel, 1848) foi registrado pela primeira vez em águas
argelinas, águas fora da região leste próximo à fronteira da Tunísia. O espécime foi um macho
adulto, com 330 mm de comprimento total e peso de 650 g.
Palavras-chave: distribuição, migração, ictiofauna argelina, costa de Maghreb.
The
blunthead
puffer
Sphoeroides
pachygaster (Müller & Troschel, 1848) is a relative
deep water species, found between 100 and 500 m
of depth, and distributed circumglobally in tropical
and temperate waters (Shipp 1990, Sampaio et al.
2001). S. pachygaster presents a widespread amphiatlantic distribution, off the western Atlantic, the
species was reported from New England to southern
Brazil (Golani et al. 2002), while off the eastern
Atlantic, the species was recorded from Irish waters
(Wheeler & Van Oijen 1985), the Bay of Biscay
(Quéro et al. 1998, 2003), off Portugal
(Albuquerque 1954-1956). The species is known to
be reported south Strait of Gibraltar, from off
Morocco, Senegal (Séret & Opic 1981) to the Gulf
of Guinea (Blache et al. 1970, Shipp 1990),
southward probably to South Africa (Smith &
Heemstra 1986). The species is also reported from
the Indian Ocean (Golani et al. 2002) and the
Pacific (Hardy 1981).
Sphoeroides pachygaster formed a well
established population in the Mediterranean Sea,
where it was reported to date, at least 26 times
between the first record off Mallorca,
Balearic Islands, which occurred in 1979 (Oliver
1981), and 2004 according to Psomadakis
et al. (2006). Recently, three additional records
were reported by Peristeraki et al. (2006) and
Ligas et al. (2006, 2007). The species was reported
from Adriatic Sea, Aegean Sea, Italian seas,
the eastern Levant Basin and southern Tunisian
coast. Although the ‘core’ of the Mediterranean
population seems to be located off the southeastern
Tunisian coast, especially the Gulf of Gabès
(Bradaï et al. 2004). Golani et al. (2002) wrongly
considered the occurrence of S. pachygaster
as probable off the Algerian coast, due to fact that
no specimen being available for confirmation
despite investigations were regularly conducted
during four decades at Algerian fishing sites
and fish markets.
However, on 22 November 2008, a
First confirmed register of Sphoeroides pachygaster off the Algerian coast
specimen of Sphoeroides pachygaster was trawled
at a depth of approximately 150 m, on sandy-muddy
189
bottom, at about 20 km west to Annaba, in the
eastern region of the Algerian coast (Fig. 1).
Figure 1. Map of the Mediterranean showing the Maghreb coast and capture site (black star) of the specimen of
Sphoeroides pachygaster off the Algerian coast.
The specimen was weighed to the nearest
gram and measured to the nearest millimetre; all
measurements with percents of total length (% of
TL) and counts are summarized in Table I,
following Ragonese et al. (1997). The specimen
was photographed (Fig. 2), preserved in 5%
buffered formaline, and deposited in the
Ichthyological Collection of the University of Bab
Ezzouar
(Algiers),
Faculté
des
Sciences
Biologiques, under the catalogue number FSB/HAL
IV B 12.
Identification was made by skin completely
smooth with total lack of scales, spines and body
plates; one lateral line on each side convoluted;
body inflatable, with large head and snout rounded;
with a beak-like jaws with two large teeth on each
jaw forming a dental plate with entire cutting edge;
eyes big and ovale with a flat interorbital space;
dorsal fin single placed in front of the similar
shaped anal fin, pelvic fin absent and caudal fin
truncated or slightly concave; colour greyish on
dorsal surface with brownish spots, belly whitish
pale grey, caudal fin base dark. Both macroscopic
and microscopic examination allowed to consider
the specimen as a mature adult male, no food was
found in the gut.
Morphology,
colour,
morphometric
measurements and meristic counts of the Algerian
blunthead puffer agree with previous descriptions
(Tortonese 1986, Ragonese et al. 1997, Golani et al.
2002, Psomadakis et al. 2006). Nevertheless, slight
variations were observed when compared with
material from the south-western Atlantic (Sampaio
et al. 2001).
This recent finding is the first welldocumented and confirmed record of S. pachygaster
off the Algerian coast. Consequently, S.
pachygaster could be considered at present as a new
additional species for the Algerian ichthyofauna.
Records of the species generally occurred in
the western and central Mediterranean, suggesting a
migration from the eastern Atlantic through
Gibraltar Strait. However recent findings in the
eastern Mediterranean cannot exclude the
possibility of a lessepsian migration (sensu Por
1978), according to Psomadakis et al. (2006), but
also a more ancient presence of S. pachygaster,
mainly in the south-eastern Mediterranean
according to Relini & Orsi-Relini (1995) who
referred to ancient literature (see Golani et al.
2002). The specimen described in this note was
captured in the eastern area close to the Tunisian
where the species is substantially established, so a
migration from the Tunisian waters where the
species is substantially established cannot be totally
excluded, as it was the case for the filefish
Stephanolepis diaspros Fraser-Brünner, 1940, a
lessepsian migrant. This species develops and
reproduces in the southern Gulf of Gabès (ZouariKtari et al. 2008), it migrated northward in Tunisian
waters and was found in a brackish area the Lagoon
of Bizerte (Fig. 1) by Bdioui et al. (2004) and more
recently off Tabarka, city located close to the
Algerian border (Fig. 1) by Ben Amor & Capapé
HEMIDA ET AL.
190
(2008). Similar pattern could explain the occurrence
of S. pachygaster in Algerian waters, but this
suitable hypothesis needs to be confirmed by
genetic methods prior definitive statement.
Table I. Morphometric measurements and meristic counts carried out on the specimen of Sphoeroides
pachygaster captured off the Algerian coast.
Morphometric measurements
in mm
% of TL
Total length (TL)
330
100
Standard length
295
89.4
Head length
100
30.3
Head width
70
21.2
Head height
60
18.2
Eye horizontal diameter
21
6.4
Eye vertical diameter
21
6.4
Interobital space
30
9.1
Snout length
40
12.1
Postorbital length
35
10.6
Width of pedunculum
35
10.6
Width of gill opening
25
7.6
Predorsal length
215
65.2
Preanal length
225
68.2
Dorsal fin length
25
7.6
Dorsal fin base length
11
3.3
Anal fin length
30
9.1
Anal fin base length
11
3.3
Pectoral fin length
30
9.1
Caudal fin length
38
11.5
Body thickness
90
27.3
Body height
90
27.3
Nostrill greatest diameter
6
1.8
Nostrill lesser diameter
4
1.2
Internarial space
30
9.1
Meristic counts
Dorsal fin rays
Anal fin rays
Pectoral fin rays
Caudal fin rays
Figure 2. Sphoeroides pachygaster captured off the Algerian coast (scale bar = 50 mm).
8
8
15
10
First confirmed register of Sphoeroides pachygaster off the Algerian coast
Acknowledgements
The authors wish to thank two anonymous
referees for helpful and useful comments that
allowed improving the manuscript. They are also
grateful to Si Hadj Aissa, carreau n° 9, at Algiers
Fishery who kindly provided the specimen of
Sphoeroides pachygaster.
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Accepted April 2009
A fauna de peixes na bacia do Rio Jucuruçu, leste de
Minas Gerais e extremo Sul da Bahia
LUISA MARIA SARMENTO-SOARES1, ROSANA MAZZONI2 & RONALDO FERNANDO
MARTINS-PINHEIRO1
1
Museu de Biologia Prof. Mello Leitão. Laboratório de Zoologia. Av. José Ruschi, 4, Centro, Santa Teresa-ES, Brasil.
Email: biobahia@nossacasa.net
2
Universidade do Estado do Rio de Janeiro- UERJ. Depto. Ecologia. Laboratório de Ecologia de Peixes - sala 225,
Av. São Francisco Xavier, 524- Maracanã, 20550-013, Rio de Janeiro- RJ.
Resumo. No presente estudo investigou-se a ictiofauna da bacia do Rio Jucuruçu, localizada no
leste de Minas Gerais e no Extremo Sul da Bahia, Brasil. Através do estudo da composição das
espécies na bacia do Rio Jucuruçu verificaram-se os padrões de distribuição espacial e o
endemismo. Foram investigados catorze pontos amostrais no vale do rio, sendo relacionadas 51
espécies, pertencentes a 30 famílias em 9 ordens. Destas, 21 espécies estão presentes unicamente
no delta do rio. As espécies consideradas constantes foram Astyanax aff. rivularis, Characidium
sp.5 e Geophagus brasiliensis. Foram estimadas a riqueza, a diversidade, a uniformidade e a
dominância. O terço superior do Jucuruçu apresentou baixa diversidade e alta dominância, devido
ao predomínio da Astyanax aff. rivularis. O terço inferior apresentou alta diversidade e baixa
dominância. A diversidade de espécies mudou ao longo do gradiente do rio. Houve aumento na
riqueza de espécies no sentido do terço inferior, devido à presença de espécies marinhas
unicamente nas proximidades da foz. Parte da ictiofauna é substituída ao longo do gradiente do
rio. A redução na disponibilidade de micro-ambientes característicos de áreas vegetadas em
trechos da bacia influencia a ocorrência e distribuição de algumas espécies. Espécies registradas
historicamente estão desaparecendo.
Palavras-Chave: Peixes de riacho, diversidade, água doce, conservação, nordeste do Brasil.
Abstract. The fish fauna of Rio Jucuruçu basin, eastern Minas Gerais and southern Bahia
State. The present study aims to investigate the fishes along the Jucuruçu River basin, in eastern
Minas Gerais and extreme southern Bahia, Brazil. Spatial distribution and endemism of fish
species along the Jucuruçu River was analyzed. Fourteen localities were investigated along the
river valley. There were related 51 species, belonging to 30 families into 9 orders. Between them,
21 species were present only on the river mouth. The species considered constant along river were
Astyanax aff. rivularis, Characidium sp.5 and Geophagus brasiliensis. The richness, the diversity,
the equitability and the dominancy are estimated. The upper stretch is the section with less
diversity and higher dominance, due to the predominance of the species Astyanax aff. rivularis.
The lower stretch had the higher diversity and the less dominance. Species diversity changed
along river gradient. There is increased species richness towards the lower stretch, with many
marine species present uniquely in this section. In spite of the increased fish diversity towards
river mouth, there were observed faunal substitution along river gradient. The low availability of
microhabitats characteristic of vegetated areas in portions of rivers is pointed out as influencing
the occurrence and distribution of some species. Some historically recorded species are nowadays
disappearing.
Key Words: stream fishes, diversity, freshwater, conservation, northeastern Brazil.
SARMENTO-SOARES ET AL.
194
Introdução
O extremo sul da Bahia é uma região de
variados ambientes para peixes de água doce,
entrecortada por diversas bacias hidrográficas de
pequeno e médio porte. A riqueza hídrica contrasta
com o baixo conhecimento de sua fauna ictiológica,
mas iniciativas para se conhecer melhor os peixes de
água doce da região têm revelado a existência de
uma diversificada fauna, especialmente de espécies
endêmicas. A destruição da Floresta Atlântica no
extremo sul da Bahia vem aumentando e no vale do
Rio Jucuruçu existe o agravante de a extensa área de
drenagem fluvial carecer de unidades de
conservação de caráter público. Atualmente,
encontra-se em fase de avaliação a Unidade de
Conservação
Serras
de
Itamarajú
(MMA/SBF/NAPMA, 2006), mas a proposta de área
protegida não inclui as cabeceiras do rio Jucuruçu,
que é crítica para a sobrevivência do próprio rio
(Sarmento-Soares & Pinheiro 2007a).
A maioria das espécies de peixes de água
doce na região inclui animais pequenos, de hábitos
crípticos, que se ocultam entre a vegetação aquática
ou sob rochas submersas. Estes peixes mantêm
íntima associação com a floresta e sua sobrevivência
é dependente da manutenção de áreas vegetadas e da
qualidade e quantidade das águas (Oyakawa et al.
2006). A conservação da biota aquática pode ser
conduzida pela preservação dos sistemas hídricos,
através de sua proteção integral ou de estratégias de
zoneamento de acordo com as atividades praticadas
ao longo do vale do rio (Casatti et al. 2008). Em
razão da paisagem fluvial e do isolamento
geográfico, é intuitivo que tomemos como alvo de
conservação da biota aquática as espécies endêmicas
de peixes de água doce (Casatti et al. 2008). Para
termos melhor compreensão destes endemismos,
precisamos de conhecimento acerca da diversidade
ictiofaunística na área a ser estudada.
No sul da Bahia as informações acerca das
populações naturais de peixes são incompletas,
carecendo de conhecimento detalhado sobre os
padrões de distribuição e biologia populacional da
maioria das espécies. Alguns registros de espécies
amostradas na bacia e/ou depositadas em coleções
científicas aparecem em banco de dados e em
relatório técnico (Sarmento-Soares & MartinsPinheiro 2008). O Projeto BioBahia – “Diversidade,
endemismo e análise biogeográfica de Siluriformes
em sistemas hídricos pouco explorados no Extremo
Sul da Bahia (Osteichthyes: Ostariophysi)”, estuda
os sistemas hídricos, do extremo sul baiano e vem
realizando uma avaliação detalhada desta região. No
presente estudo investigamos a distribuição e
endemismo das comunidades de peixes na bacia do
Rio Jucuruçu.
Material e Métodos
Área de Estudo. O vale do rio Jucuruçu
permaneceu com ocupação indígena desde o século
XVI e até a segunda metade do século XX, passando
por lento e gradual processo de colonização. O ciclo
de exploração madeireira, iniciado na década de 60,
causou mudanças profundas na região e durante
pouco mais de 20 anos modificou sua paisagem,
restando hoje apenas fragmentos florestais, da
cobertura de Floresta Atlântica.
Em decorrência da ocupação do vale por
fazendas, grande parte da mata ciliar dos rios foi
removida, observando-se intenso assoreamento,
facilmente evidenciado pelas baixas profundidades
nos locais de amostragem e qualidade do leito.
As primeiras informações sobre as espécies
de peixes de água doce no Rio Jucuruçu foram
colhidas apenas ao final do século XX, já durante
este processo de remoção das matas nativas e
alteração dramática da paisagem (Sarmento-Soares
& Martins-Pinheiro 2008).
A bacia do Jucuruçu tem área de 5.284,30
2
km (MMA/SRH, 1997). Este rio nasce com o nome
de Córrego da Prata no contraforte ocidental da
Serra dos Aimorés, em Minas Gerais, a cerca de
1000 m de altitude, e cruza o extremo sul da Bahia,
no sentido oeste-leste (Fig. 1), percorrendo a
extensão de 241 km. O terço superior da bacia do
Jucuruçu foi considerada como a área desde as
nascentes até o encontro com o Ribeirão Dois de
Abril no povoado de Dois de Abril (Fig. 2, Tabela I).
Neste trecho as declividades são mais acentuadas, e
a ocorrência de intrusões dos maciços graníticos se
reflete na organização da rede de drenagem do
Jucuruçu,
eventualmente
marcada
por
encachoeiramentos.
O médio Jucuruçu vai até o encontro
com o Córrego Jundiar, nas cercanias de Itamarajú
(Fig. 2, Tabela I). A declividade neste trecho
é mais suave, pela influência do relevo plano
dos Tabuleiros Costeiros. O baixo Jucuruçu
segue das cercanias de Itamarajú até a foz, na cidade
do Prado (Fig. 2, Tabela I). Entre Itamarajú e Prado,
o rio Jucuruçu segue encaixado em uma
falha (Graben sensu Saadi 1998) de baixo curso
fluvial.
Em direção à foz, aparece extensa baixada
com relevo quase plano com inundações periódicas
da planície associadas ao período chuvoso. A
expedição BioBahia, realizada entre Outubro e
Novembro de 2004 (Sarmento-Soares 2005), e
complementada em Dezembro e Janeiro de 2006 e
2007 (Sarmento-Soares 2007) contribuiu para o
A fauna de peixes da bacia do rio Jucuruçu
195
conhecimento da ictiofauna da bacia como um todo.
Foram amostrados 13 trechos do rio Jucuruçu,
somando à avaliação histórica de um 14º trecho (Fig.
2, Tabela I).
Figura 1. Localização do rio Jucuruçu.
Figura 2. Mapa da bacia do rio Jucuruçu indicando os catorze pontos de amostragem recentes e os pontos históricos.
Ponto
UF
Município
Local
Coordenadas
Altitude (m)
Espécies
capturadas
Data
196
Tabela I. Localização geográfica, horário de amostragem, condições da água e substrato do fundo dos pontos na bacia do Rio Jucuruçu.
Característica da água: (T1) Transparente amarelada; (T2) Transparente cor de chá e (T3) Marrom turva. Substrato: (Ae) Areia; (Ai) Argila;
(C) Cascalho; (L) Lodo; (P) Pedra e (R) Rocha.
Profund. (m) Água Substrato
Terço superior
1
MG Palmópolis
Rio Jururuçu
16º44'02"S 40º25'35"W
607
4
26/10/ 2004
1,0 a 2,0
T1
R-Ae
2
MG Palmópolis
Córrego Bananeiras
16º44'48"S 40º25'46"W
605
7
26/10/ 2004
0,3 a 0,5
T3
Ae-Ai
3
MG Palmópolis
Ribeirão Dois de Abril
16º50'19"S 40º24'21"W
400
6
26/10/ 2004
0,3 a 1,0
T3
L
4
MG Palmópolis
Córrego Seco
16º50'55"S 40º24'31"W
442
10
27/10/ 2004
0,3 a 0,5
T3
R-L
5
MG Palmópolis
Córrego das Novas
16º51'12"S 40º23'42"W
432
3
27/10/ 2004
1,0 a 1,5
T3
R-L
6
MG Palmópolis
Rio Dois de Abril
16º50'21"S 40º19'10"W
358
9
26/10/ 2004
0,8 a 1,5
T1
Ae
Terço médio
BA
Jucuruçu
Córrego da Onça
16º49'49"S 40º15'05"W
379
7
26/10/ 2004
0,3 a 0,5
T1
Ae
8
BA
Jucuruçu
Rio Jucuruçu
16º50'10"S 40º08'40"W
138
11
26/10/ 2004
1,0 a 1,2
T1
R-Ae
9
BA
Jucuruçu
Rio Jucuruçu
16º51'06"S 39º53'53"W
119
10
25/10/ 2004
0,5 a 1,0
T1
Ae-C
10
BA
Itamaraju
Córrego São Pedro
16º54'24"S 39º45'15"W
67
10
25/10/ 2004
0,5 a 1,5
T1
R-P
11
BA
Itamaraju
Córrego do Jundiar
17º01'35"S 39º35'57"W
27
10
25/10/ 2004
0,5 a 0,7
T1
Ae-C
Terço inferior
12
BA
Prado
Rio João de Corongo
17º05'42"S 39º27'00"W
14
7
31/12/2006
1,0 a 1,5
T2
Ae
13
BA
Prado
Afluente do Rio Jucuruçu
17º16'15"S 39º17'57"W
6
3
31/12/2006
1,0 a 1,5
T1
Ae-Ai
14
BA
Prado
Foz do Rio Jucuruçu
17º20'34"S 39º13'23"W
0
24
Histórico
1,0 a 5,0
T3
Ae-L
7
197
De acordo com os registros históricos
disponíveis até o ano 2000, a bacia do Rio Jucuruçu
havia sido amostrada em dez localidades (SarmentoSoares & Pinheiro 2008). As amostragens
evidenciadas neste estudo somadas às coletas antigas
se complementam, permitindo uma avaliação mais
homogênea da distribuição das espécies em toda a
bacia.
Amostragem. As atividades de campo
foram realizadas durante o dia, pela manhã até o
crepúsculo, cobrindo três ou quatro localidades por
dia. Cada uma das localidades foi amostrada
percorrendo-se um trecho de aproximadamente 50
metros rio acima. Cada um dos pontos de
amostragem foi localizado por GPS, fotografado e
caracterizado quanto às condições ambientais.
As amostragens foram realizadas com o uso
de tarrafa tipo argola (8 mm de malha e 16 m de
perímetro), rede passaguá (2,5 mm de malha),
picarés (malhas de 2,5 e 5,0 mm), rede de arrasto
tipo Trawl (malha 5 mm; 2,6 m de altura e 10 m de
comprimento), redes de arrastos (malha de 5 mm e 8
mm), tarrafa multifilamento (malha de 8 mm) e
redes de espera (malhas de 15 mm e 25 mm). Casos
em que os métodos convencionais revelaram-se
pouco eficientes, o mergulho livre foi empregado
para localização e captura de exemplares. Em cada
ponto foi usada uma combinação dos recursos de
pesca de forma assegurar uma exaustiva amostragem
de leito, fundo e margem do local amostrado.
Os exemplares coletados foram fotografados
vivos, em aquário de campo, fixados em formalina a
10% e transportados para o laboratório, onde foram
triados, transferidos para conservação em álcool a
70%, identificados e catalogados. A licença de
coleta para a expedição foi solicitada junto ao
Instituto Brasileiro do Meio Ambiente e dos
Recursos Naturais Renováveis - IBAMA (processo
número 02006.002926/06-17), confirmando-se
através do registro #1906091 emitido pelo SISBIO.
Informações históricas acerca da ictiofauna
na região de estudo, foram obtidas a partir de
consulta ao banco de dados do projeto NEODAT
(The
Inter-Institutional
Database
of
Fish
Biodiversity in the Neotropics –NEODAT
Project/NSF) e a partir de relatório técnico
disponível (MMA/SRH, 1999), cujos registros
encontram-se disponibilizados em Sarmento-Soares
& Martins-Pinheiro (2008).
Taxonomia. A classificação taxonômica
dos exemplares seguiu Buckup et al. (2007) para
peixes de água doce e Carvalho Filho (1999) e
Menezes et al. (2003), para peixes marinhos. Em
uma parcela dos indivíduos capturados foram
tomadas informações morfométricas e merísticas
para identificação específica. Dúvidas sobre a
identificação de espécies foram resolvidas através da
avaliação de caracteres anatômicos. Os exemplares
foram catalogados nas coleções ictiológicas do
MBML - Museu de Biologia Professor Mello Leitão
e MNRJ - Museu Nacional, Universidade Federal do
Rio de Janeiro (Sarmento-Soares & MartinsPinheiro 2007b).
Análise de dados. Para a caracterização da
ictiofauna presente na bacia do Rio Jucuruçu, foram
realizadas avaliações de constância, suficiência de
amostragem, rarefação, riqueza, dominância,
diversidade e uniformidade.
Os valores de Constância de Ocorrência (C)
das diferentes espécies foram calculados, segundo
Dajoz (1983), a partir da equação: C=(p÷P)×100;
onde C é o valor de constância da espécie; p é a
quantidade de pontos em que apareceu a espécie e P
o número total de pontos. As espécies foram
consideradas constantes quando apresentaram C ≥
50, acessórias quando 25 ≤ C < 50 e ocasionais
quando C < 25. Foram realizadas estimativas de
espécies com e sem as espécies marinhas periféricas
(Myers, 1938).
As curvas de suficiência da amostragem
foram construídas pelo método Mao Tau (Colwell et
al., 2004). Como estimadores de riqueza foram
usados os índices de riqueza não-paramétricos:
Chao2, Jackknife1, Jackknife2 e Bootstrap. Estes
índices estimam o número de espécies ainda por
serem coletadas, baseados numa quantificação de
raridade. Os estimadores Chao2, Jackknife1,
Jackknife2 e Bootstrap, são baseados em incidência
e utilizam o número de “Uniques” e “Duplicates”,
que são o número de espécies encontradas em
somente uma e/ou duas amostras, respectivamente,
para as estimativas de riqueza (Colwell &
Coddington 1994).
Para a obtenção da riqueza específica foi
utilizado o índice de riqueza de Margalef (M), que
se baseia na relação entre o número de espécies
identificadas e o número total de indivíduos
coletados, calculado da seguinte forma: M=(S-1) ÷
(ln n), onde S é a quantidade de espécies e n é o
número total de indivíduos.
Para estimativa da dominância (D) foi usada
a relação: D=Σ (ni÷n)2; onde ni é a quantidade de
exemplares da espécie i. A dominância varia de 0
(todas as espécies estão igualmente representadas)
até 1 (uma espécie domina a comunidade
completamente).
A estimativa da diversidade foi realizada
utilizando-se o Índice de Shannon-Wiener:
H=-Σ(ni÷n) × (ln (ni÷n)). Este é um índice
de diversidade que leva em conta o número de
198
indivíduos e quantidade de espécies. Varia de 0 para
comunidades com uma única espécie até valores
elevados (acima de 5.0) para comunidade com
muitas espécies e poucos exemplares de cada
espécie (Magurran, 2006).
A
uniformidade
(“equitability”)
foi
calculada usando-se o índice de Pielou (1969):
e=H÷log S.
Para os diferentes índices e curvas foi
utilizado o programa PAST versão 1.90 (Hammer et
al, 2007).
Resultados
Foram amostrados na bacia do Rio Jucuruçu
14 pontos (da cabeceira a foz), sendo 1 histórico e
13 recentes (Tabela I, Fig. 3).
Figura 3. Pontos de amostragem (P) ao longo da bacia do rio Jucuruçu . Terço Superior: P1- rio Jucuruçu em
Palmópolis; P2- córrego Bananeiras; P3- ribeirão Dois de Abril na Fazenda Antonio Gildo; P4- córrego Seco; P5riacho afluente do córrego das Novas; P6- rio Dois de Abril em Dois de Abril.; Terço Médio: P7- córrego da Onça; P8rio Jucuruçu próximo a Jucuruçu. Terço P9- rio Jucuruçu; P10- córrego são Pedro, P11- córrego do Jundiar. Terço
inferior: P12- rio João de Corongo; P13- afluente do rio Jucuruçu; e P14- rio Jucuruçu em Prado.
Na bacia do Jucuruçu foram registradas 51
espécies, pertencentes a 30 famílias em 9 ordens,
considerando-se tanto as amostragens recentes, das
expedições ictiológicas, como as históricas, de
registros de coleções (Tabela II, Fig. 4). Os
Ostariophysi foram maioria com 30 espécies (Fig.
4,a-h), representando 58,8% da riqueza total
registrada na bacia, seguidos pelos Perciformes (Fig.
4, i-j) com 12 espécies que representam 23,5%;
Clupeiformes, com 3 espécies e 5,9%;
Cyprinodontiformes e Pleroneuctiformes, com 2
espécies e 3,9% cada e ainda Lophiiformes e
Gasterosteiformes, com 1 espécie e 2,0% cada.
Dentre os Ostariophysi, os Siluriformes foram os
mais representativos, com 15 espécies (50,0%),
seguidos pelos Characiformes com 14 espécies
(46,7%). O terceiro grupo representativo de
Ostariophysi, Gymnotiformes, foi representado por
uma única espécie (3,3% do total). A lista
taxonômica das espécies de peixes conhecidas para a
bacia, incluindo os registros históricos está
apresentada na Tabela II.
199
Figura 4. Algumas espécies de peixes na bacia do rio Jucuruçu. (a) Leporinus copelandii; (b) Astyanax aff.rivularis; (c)
Mimagoniates microlepis; (d) Imparfinis aff.minutus; (e) Trichomycterus pradensis; (f) Hypostomus cf. affinis; (g)
Parauchenipterus striatulus; (h) Gymnotus carapo; (i) Centropomus parallelus; (j) Awaous tajasica.
Tabela II. Espécies de peixes conhecidas para a Bacia do rio Jucuruçu, suas localidades e
ocorrência. Asteriscos (*) indicam registros históricos.
Localidades
Ordem/ Família
Espécies
(ocorrência)
Clupeiformes
Pristigasteridae
Odontognathus mucronatus (Poey, 1867) (*)
1 (4,3%)
Pellona harroweri Lacepède, 1800 (*)
1 (4,3%)
Clupeidae
Harengula jaguana Poey, 1865 (*)
1 (4,3%)
Characiformes
Curimatidae
Cyphocharax gilbert (Quoy & Gaimard, 1824)
2 (8,7%)
Prochilodontidae
Prochilodus vimboides Kner, 1859 (*)
2 (8,7%)
Anostomidae
Leporinus conirostris Steindachner, 1875
2 (8,7%)
Leporinus copelandii Steindachner, 1875
5 (21,7%)
Leporinus cf. steindachneri
2 (8,7%)
Crenuchidae
Characidium sp.5
15 (65,2%)
Characidae
Astyanax aff. lacustris
12 (43,5%)
Astyanax aff. rivularis
16 (69,6%)
Hyphessobrycon bifasciatus Ellis, 1911
1 (4,3%)
Moenkhausia doceana (Steindachner, 1877) (*)
1 (4,3%)
Oligosarcus acutirostris Menezes, 1987
2 (8,7%)
Mimagoniates microlepis (Steindachner, 1876)
1 (4,3%)
constância de
Constância
de ocorrência
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Constante
Constante
Constante
Ocasional
Ocasional
Ocasional
Ocasional
200
Tabela II. Espécies de peixes conhecidas para a Bacia do rio Jucuruçu, suas localidades e
ocorrência. Asteriscos (*) indicam registros históricos (cont.).
Localidades
Ordem/ Família
Espécies
(ocorrência)
Erythrinidae
Hoplerythrinus unitaeniatus (Agassiz, 1829)
1 (4,3%)
Hoplias malabaricus (Bloch, 1794)
7 (30,4%)
Siluriformes
Trichomycteridae
Trichomycterus pradensis Sarmento-Soares et. al 2005 5 (21,7%)
Callichthyidae
Scleromystax prionotos (Nijssen & Isbrüecker, 1980)
4 (17,4%)
Loricariidae
Neoplecostominae
New genus and species
3 (13,0%)
Hypoptopomatinae
Otothyris travassosi Garavello, Britski & Schaeffer,
4 (17,4%)
1998
Parotocinclus sp.
4 (17,4%)
Hypostomus cf. affinis
7 (30,4%)
Pseudopimelodidae
Microglanis pataxo Sarmento-Soares et al., 2006.
1 (4,3%)
Heptapteridae
Imparfinis aff. minutus
6 (26,1%)
Pimelodella aff. vittata
9 (39,1%)
Rhamdia sp.
7 (30,4%)
Ariidae
Arius phrygiatus Valenciennes 1840 (*)
1 (4,3%)
Bagre bagre (Linnaeus, 1758) (*)
1 (4,3%)
Cathorops spixii (Agassiz, 1829) (*)
1 (4,3%)
Auchenipteridae
Pseudauchenipterus affinis (Steindachner, 1877) (*)
1 (4,3%)
Parauchenipterus striatulus (Steindachner, 1877)
2 (8,7%)
Gymnotiformes
Gymnotidae
Gymnotus carapo Linnaeus, 1758
3 (13,0%)
Lophiiformes
Ogcocephalidae
Ogcocephalus notatus (Linnaeus, 1758)
1 (4,3%)
Cyprinodontiformes
Poeciliidae
Poecilia vivipara Bloch & Schneider, 1801
8 (34,8%)
Poecilia reticulata Peters, 1859
3 (13,0%)
Gasterosteiformes
Syngnathidae
Microphis brachyurus (Bleeker, 1853) (*)
1 (4,3%)
Perciformes
Centropomidae
Centropomus paralellus Poey, 1860 (*)
1 (4,3%)
Serranidae
Rypticus randalli Courtenay, 1967 (*)
1 (4,3%)
Carangidae
Caranx latus Agassis, 1831 (*)
1 (4,3%)
Selene vomer (Linnaeus, 1758)
1 (4,3%)
Trachinotus goodei Jordan & Evermann, 1896 (*)
1 (4,3%)
Haemulidae
Haemulon plumieri (Lacèpede, 1812) (*)
1 (4,3%)
Pomadasys corvinaeformis (Steindachner, 1868) (*)
1 (4,3%)
Sciaenidae
Paralonchurus brasiliensis (Steindachner, 1875) (*)
1 (4,3%)
Umbrina coroides Jordan & Evermann, 1896 (*)
1 (4,3%)
Cichlidae
Geophagus brasiliensis (Quoy & Gaimard, 1824)
13 (56,5%)
Eleotridae
Eleotris pisonis (Gmelin, 1789)
1 (4,3%)
Gobiidae
Awaous tajasica Lichtenstein, 1822
3 (13,0%)
Pleuronectiformes
Paralichthyidae
Citharichthys spilopterus Günther, 1862 (*)
1 (4,3%)
Achiridae
Achirus lineatus (Linnaeus, 1758) (*)
1 (4,3%)
A suficiência de amostragem (Fig.
5a,b) indica maior inclinação para a curva
histórica (Fig. 5a), sugerindo baixa estabilização,
visto que com cerca de metade das localidades
constância de
Constância
de ocorrência
Ocasional
Acessória
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Acessória
Ocasional
Acessória
Acessória
Acessória
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Acessória
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Ocasional
Constante
Ocasional
Ocasional
Ocasional
Ocasional
coletadas
amostradas,
apenas
62%
das
espécies haviam sido amostradas. Em contraste,
com as amostragens recentes, houve tendência
mais acentuada de estabilização, sendo que com
metade
das
aproximadamente
sido registradas
201
localidades
amostradas,
84% das espécies haviam
(Fig. 5b), indicando que
mesmo com o incremento do número de
amostragens, o número de espécies tende a
permanecer igual.
Figura 5. Curvas dos coletores espécie-ponto geradas de acordo com o método Mao Tau. Linhas azuis representam
uma área de confiança de 95%. (a) Coletas históricas. (b) Amostragens recentes. Observa-se uma melhor estabilização
na curva de coletas recentes.
Das espécies coletadas, Microglanis pataxo
Sarmento-Soares et al. (2006) e Trichomycterus
pradensis Sarmento-Soares et al. (2005) foram
descritas como novas. Cinco outras espécies
possuem “status” taxonômico ainda indefinido,
Characidium sp.5, Parotocinclus sp., Hypostomus
cf. affinis, Rhamdia sp., juntamente com um novo
Neoplecostominae. Parotocinclus sp. é espécie
potencialmente nova e está em processo
de descrição. O novo gênero e espécie de
Neoplecostominae foi identificado por R.E. Reis
e E.H.L. Pereira (com. pess.) e vem sendo
estudado pela equipe. As demais espécies não
identificadas em nível específico pertencem a grupos
taxonômicos bastante complexos e podem
representar novos táxons no âmbito de trabalhos de
revisão.
A única espécie exótica registrada para a
bacia do Rio Jucuruçu é o barrigudinho Poecilia
reticulata. Tal espécie é originária do litoral norte da
América do Sul, entre Venezuela e o estado
brasileiro do Amapá (Lucinda & Costa, 2007). É
interessante notar que esta espécie não aparecia nos
registros históricos.
Três
espécies
foram
consideradas
constantes, baseando-se na constância de ocorrência
(C), com presença em mais da metade dos pontos
amostrados; sete foram consideradas acessórias e as
41 restantes foram reconhecidas como ocasionais
(Tabela II).
Na parte alta da bacia não foi registrada
nenhuma espécie da divisão periférica, na parte
média foi registrada apenas Awaous tajasica e na
parte baixa foram registradas 20 espécies periféricas.
O índice Bootstrap mostrou-se menos sensível a
inclusão das espécies periféricas, com estimativas de
9,4% (com as periféricas) a 16,8% (sem as
periféricas) do total de espécies amostradas. Os
demais índices não paramétricos, no entanto,
mostraram-se bastante sensíveis a esta inclusão. O
mais sensível foi o índice Chao 2, 47,8% (com as
periféricas) a 6,8% (sem as periféricas) do total de
espécies amostradas (Tabela III).
A avaliação dos índices paramétricos
considerando os peixes marinhos de estuário
(periféricos); e ainda os mesmos índices caso
excluídas tais espécies marinhas, apresentaram
resultados próximos para os dois grupos; com
exceção do índice de Margalef. O aumento do índice
de Margalef na parte baixa da bacia e na bacia como
um todo, quando se consideram as espécies
periféricas, é devido ao fato destas espécies estarem
em grande número e representadas por poucos
exemplares.
Os valores dos índices de diversidade de
Shannon-Weiner (H’) e de dominância (D) foram
diferentes entre os trechos da bacia (Tabela III). O
terço superior é a seção com menor diversidade e
maior dominância, devido ao predomínio da espécie
Astyanax aff. rivularis. O terço inferior, entretanto,
tem a mais alta diversidade e a menor dominância. O
terço médio, com 26 espécies amostradas,
apresentou valores intermediários de diversidade e
dominância.
A diversidade de espécies mudou ao longo
do gradiente fluvial. Houve um aumento na riqueza
202
de espécies em direção ao terço inferior, com muitas
espécies marinhas periféricas presentes unicamente
naquele trecho. Além do aumento na diversidade em
direção à foz, houve substituição ictiofaunística ao
longo do gradiente fluvial.
Algumas espécies de água doce habitam
apenas rios de grande porte, tais como adultos de
Cyphocharax gilbert, Leporinus cf. steindachneri,
Leporinus conirostris, Prochilodus vimboides e
Pseudauchenipterus affinis, registrados apenas para
o canal principal do rio Jucuruçu e grandes
tributários. As amostragens em pequenos tributários
permitiram a captura das seguintes espécies não
previamente assinaladas para a bacia: Awaous
tajasica,
Gymnotus
carapo,
Hoplerythrinus
unitaeniatus,
Hyphessobrycon
bifasciatus,
Microglanis pataxo, Poecilia reticulata, Rhamdia
sp. e Trichomycterus pradensis.
Sete espécies de pequeno porte, com
tamanho adulto inferior a 50 mm SL, foram
registradas na bacia do Rio Jucuruçu, representadas
pelos ostariofíseos Characidium sp.5, Mimagoniates
microleps, Otothyris travassosi, Parotocinclus sp.,
Microglanis pataxo e ainda pelos poecilídeos
Poecilia vivipara e Poecilia reticulata. A maioria
das espécies de tamanho pequeno pôde ser
encontrada nos terços superior a médio, com menor
incidência no terço inferior, apesar do esforço de
amostragem ter sido equivalente em todos os trechos
fluviais.
Tabela III. Estimativa não-paramétrica de riqueza de espécies e descritores da ictiofauna na Bacia do Rio
Jucuruçu (com e sem a presença dos peixes marinhos da divisão periférica).
TOTAL
SEM MARINHOS
ESTIMADORES
Superior Médio Baixo Bacia Superior Médio Baixo Bacia
19,6
31,2 160,7
97,7
19,6
30,2
42,3
32,2
Chao 2
20,4
33,7
71,6
75,9
20,4
32,7
34,1
35,7
Jackknife 1
22,8
36,6
95,3
94,4
22,8
35,6
42,8
36,0
Jackknife 2
18,0
29,7
53,5
61,3
18,0
28,7
26,6
33,1
Bootstrap
DESCRITORES
Espécies coletadas (S)
Exemplares (n)
Dominância (D)
Diversidade Shannon (H)
Riqueza Margalef (M)
Uniformidade (e)
Superior
16
601
0,20
2,00
2,34
0,72
Médio
26
981
0,16
2,32
3,63
0,71
Baixo
41
191
0,08
2,99
7,62
0,80
Discussão
A predominância dos Ostariophysi repete
um arranjo comum da fauna de água doce das bacias
da região neotropical formada essencialmente por
peixes pertencentes a este grupo (Lowe McConnell,
1999). Entre as 51 espécies registradas na bacia, 26
não foram capturadas durante os trabalhos de campo
ao longo do Jucuruçu. Destas, 18 espécies eram de
peixes marinhos presentes apenas no estuário do rio,
trecho onde as amostragens históricas foram
consideradas suficientes, e 8 eram peixes de água
doce. Apesar de não terem sido localizadas no
Jucuruçu, as espécies C. gilbert, C. paralellus,
Leporinus cf. steindachneri e P. affinis foram
registradas em sistemas hídricos vizinhos, no
extremo sul da Bahia (e.g., Sarmento-Soares et al.,
2007, 2008). Apesar de não terem sido encontradas
na bacia do Jucuruçu, M. doceana, L. conirostris, P.
vimboides e E. pisonis habitam outros rios do
extremo sul, com registro recente no rio Peruípe ou
rio Itanhém (obs. pess).
Bacia
51
1773
0,14
2,58
6,68
0,66
Superior
16
601
0,20
2,00
2,34
0,72
Médio
25
978
0,16
2,31
3,49
0,72
Baixo
21
157
0,12
2,48
3,96
0,81
Bacia
30
1736
0,15
2,48
3,89
0,72
A avaliação comparativa da biota é uma
tarefa imprescindível quando da tomada de decisões
sobre áreas a preservar. Os vários índices de
diversidade calculados indicam uma diversidade
crescente da parte alta do rio para a parte baixa o que
estaria de acordo com o conceito de rio contínuo
(Vannote et al., 1980), o que pode estar associado a
uma progressiva adição de micro-hábitats.
No terço superior predominam córregos de
leito raso e substrato de cascalho e pedras, sendo
gradualmente substituído por fundo de areia e
gramíneas marginais no terço médio, e por grandes
poças, com locas e ramos submersos no terço
inferior.
Não foram registradas espécies com
distribuição exclusiva ao terço superior da bacia,
mas algumas destas tiveram ocorrência limitada
aos terços alto e médio. Esta distribuição se aplica a
Characidium sp.5, T. pradensis, Parotocinclus sp. e
Hypostomus cf. affinis, espécies tipicamente
habitantes das cabeceiras de rios e riachos. Espécies
203
de água doce das planícies fluviais foram
unicamente registradas no terço inferior, tais como
H. bifasciatus, M. microlepis e P. affinis. As
espécies
de
Auchenipteridae
do
gênero
Pseudauchenipterus são peixes de água doce
preferencialmente encontrados próximos ao estuário
de rios (Akama 1999, Sarmento-Soares & MartinsPinheiro 2007c).
A bacia do rio Jucuruçu drena uma região
geologicamente conhecida como Tabuleiros
Costeiros do Grupo Barreiras, caracterizada por
relevo de inclinação moderada a suave, amplamente
distribuída ao longo do norte do Espírito Santo e sul
da Bahia (Braun & Ramalho 1980). A topografia
pode ser considerada um fator de forte influência
sobre a distribuição longitudinal das espécies de
peixes (Caramaschi, 1986), podendo explicar a
ausência de populações de peixes com distribuição
restrita às cabeceiras do Rio Jucuruçu.
As zonas ripárias do Rio Jucuruçu
atualmente encontram-se quase que totalmente
desflorestadas, à exceção da região próxima ao
estuário, onde ainda existem manguezais, isto
contribui para a incidência direta de luz solar sobre o
rio e a elevada temperatura da água compromete a
sobrevivência de certas espécies (Casatti, 2004).
Muitas das espécies de peixes não foram
encontradas
em
trechos
desflorestados,
possivelmente por não tolerarem a intensa
luminosidade e as alterações químicas na
composição da água. As espécies consideradas
constantes como Astyanax aff. lacustris, Astyanax
aff. rivularis, Characidium sp.5, Geophagus
brasiliensis e Pimelodela aff. vittata conseguem
adaptar-se às novas condições dos ambientes
aquáticos.
A bacia do Jucuruçu encontra-se melhor
vegetada nas proximidades das planícies litorâneas,
como exemplificado pelo registro único de certas
espécies. Alguns peixes de pequeno porte dependem
da vegetação marginal para alimentação, como é o
caso de M. microleps (Mazzoni & Iglesias-Rios,
2002). A presença desta espécie unicamente no Rio
João de Corongo, no curso inferior do Jucuruçu,
pode ser decorrência das condições ambientais
naquele local, um dos poucos trechos onde se
observou a presença de mata ciliar em razoável
estado de conservação.
Outra espécie de Characiformes, H.
bifasciatus, foi unicamente encontrada em um
afluente do rio Jucuruçu no terço inferior. Os cinco
exemplares encontrados no local estavam junto à
vegetação submersa. A ocorrência desta espécie em
um único ponto da bacia do Jucuruçu parece indicar
uma baixa tolerância às alterações de cobertura
vegetal observadas em outras localidades mais à
montante. Menezes et al. (1990) ressaltam que certas
espécies de Hyphessobrycon ocupam ambientes
aquáticos restritos, que se alterados ou destruídos
podem levar a seu desaparecimento.
Dentre os Siluriformes, Costa et al. (2004)
assinalaram a presença de uma nova espécie de
Microcambeva para a bacia do Rio Jucuruçu, que se
encontra em processo de descrição (Wilson J.E.M.
Costa, com. pess.). As duas espécies conhecidas de
Microcambeva abrigam peixes pequenos, com
tamanho inferior a 50 mm SL, habitantes de fundos
arenosos de pequenos rios rasos (Costa &
Bockmann, 1994; Oyakawa et al., 2006). No rio
Jucuruçu Microcambeva pode representar uma
espécie rara.
A Serra do Espinhaço, com altas montanhas,
corresponde ao divisor natural das águas entre alto
São Francisco e as drenagens litorâneas. Estas
montanhas, com elevações entre 1.000 a 1.300
metros, aparentemente funciona como uma barreira
biogeográfica eficiente para peixes de água doce,
pois uma considerável parcela da ictiofauna é
diferenciada nos dois sistemas hídricos. Apesar do
isolamento, o alto rio São Francisco, em Minas
Gerais, e as drenagens litorâneas do extremo sul da
Bahia compartilham elementos da ictiofauna, como
Cyphocharax gilbert e Hoplerythrinus unitaeniatus.
Grupos de taxonomia complexa nas drenagens
litorâneas têm sido atribuídos como co-específicos
de peixes do Alto Rio São Francisco. No caso do rio
Jucuruçu, as espécies Astyanax aff. lacustris,
Astyanax aff. rivularis, Imparfinis aff. minutus e
Pimelodella aff. vittata foram associadas aos nomes
de espécies na drenagem do rio das Velhas, um dos
principais contribuintes do Alto São Francisco, em
Minas Gerais.
A diversidade da ictiofauna na drenagem do
rio das Velhas é razoavelmente bem estudada
(Lütken, 2001 e Alves & Pompeu, 2001). No rio
Jucuruçu muitas espécies são potencialmente novas,
porém os nomes para tais peixes ainda estão
indisponíveis, no aguardo de descrição formal. A
semelhança morfológica observada entre os peixes
do Alto São Francisco e das drenagens litorâneas
sugere uma história hidrológica compartilhada em
algum momento.
A delimitação de áreas de endemismo é um
dos principais tópicos na análise biogeográfica
(Crisci et al., 2003). Uma área de endemismo pode
ser reconhecida pela congruência na distribuição de
diferentes taxa (Harold & Mooi, 1994). Congruência
quanto aos padrões de distribuição entre diferentes
espécies de peixes de água doce é observada para as
drenagens costeiras entre o norte do Espírito Santo e
204
o extremo sul da Bahia. A ictiofauna aqui estudada
exemplifica esta situação de endemismo regional,
como pode ser ilustrado pelos padrões de
congruência na distribuição de Oligosarcus
acutirostris e Pseudauchenipterus affinis. Outras
espécies de peixes possuem distribuição similar,
como Mimagoniates sylvicola, reportado por
Sarmento-Soares & Martins-Pinheiro (2006a),
Rachoviscus graciliceps, reportado por SarmentoSoares & Martins-Pinheiro (2006b), Aspidoras
virgulatus reportado por Sarmento-Soares et al.
(2007), Phalloceros ocellatus reportado por Lucinda
(2008) e Simpsonichthys myersi reportado por Costa
(2003). Todas estas espécies de peixes habitam os
rios que cortam os Tabuleiros Costeiros entre o norte
do Espírito Santo e o extremo sul da Bahia.
Áreas são sistemas abertos e muitas vezes
têm histórias múltiplas e complicadas, e assim sendo
não há respostas simples para explicar padrões
biogeográficos (Funk, 2004). A inferência sobre
uma evolução conjunta da ictiofauna de água doce
entre o norte do Espírito Santo e o extremo sul da
Bahia merece ser investigada com maior
profundidade.
Agradecimentos
Agradecemos aos colegas do Setor de
Zoologia, Museu de Biologia Prof. Mello Leitão.
Somos gratos a Gustavo W. Nunan, Marcelo R.
Britto e Paulo A. Buckup pela cooperação junto ao
setor de Ictiologia do Museu Nacional/ UFRJ. Aos
colegas Arion T. Aranda, Carine C. Chamon e
Rogério L.Teixeira pelo empenho e ajuda nos
trabalhos de campo. Agradecemos a Edson H.L.
Pereira, Flavio F.C.T. Lima, Marcelo R. Britto,
Paulo H.F. Lucinda, Roberto E. Reis, Wilson J.E.M.
Costa e Z. Margarete Lucena pela ajuda com as
identificações de espécies e/ou informações sobre os
ambientes. A L. Casatti pelas sugestões e leitura
crítica do manuscrito. Somos gratos a Benevaldo G.
Nunes pela ajuda e incentivo para publicação.
Financiamento para os trabalhos de campo foi dado
pelo
All
Catfish
Species
Inventory
(http://clade.acnatsci.org/allcatfish), com fundos da
National Science Foundation, USA, NSF DEB0315963. Somos gratos ao apoio da UFRJ/ MNRJ
(Universidade Federal do Rio de Janeiro/ Museu
Nacional), pelo veículo utilizado para transporte
durante os trabalhos de campo referentes à primeira
expedição. Agradecemos ao Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renováveis
(IBAMA/ SISBIO) pela licença de coleta regional
para a área de estudo. Ao povo da vila de
Cumuruxatiba, Prado, pela hospitalidade, incentivo e
apoio para realização de nosso trabalho com os
peixes do Extremo Sul da Bahia. A autora principal
recebeu financiamento parcial através de bolsa de
pós-doutorado sênior pelo CNPq (processo #
154358/2006-1).
Material Examinado. Espécies de peixes coletadas
ao longo da bacia do Rio Jucuruçu, com o número
de registro e número de exemplares em cada lote
(em parênteses): Astyanax aff. lacustris: MNRJ
28619(9), MNRJ 28616(1), MNRJ 28611(2), MNRJ
28606(3), MNRJ 28676(2), MNRJ 28599(2), MNRJ
28596(11). Astyanax aff. rivularis: MNRJ 28621(6),
MNRJ 28623(37), MNRJ 28625(19), MNRJ
28620(115), MNRJ 28615(3), MNRJ 28607(38),
MNRJ 28602(47), MNRJ 28600(167), MNRJ
28591(25), MNRJ 32120(16), MBML 1456(6),
MNRJ 32168(10). Awaos tajasica: MNRJ 28339(1),
MNRJ 28337(1), MNRJ 28333(1). Characidium
sp.5: MNRJ 29072(15), MNRJ 29075(62), MNRJ
29068(24), MNRJ 29076(17), MNRJ 29067(52),
MNRJ 29066(33), MNRJ 29064(38), MNRJ
29061(3), MNRJ 29058(39), MNRJ 29056(9).
Geophagus brasiliensis: MNRJ 28346(20), MNRJ
28347(3), MNRJ 28345(3), MNRJ 28343(1), MNRJ
28342(7), MNRJ 28338(5), MNRJ 28335(21),
MNRJ 28334(1), MNRJ 28332(6), MNRJ 32115(3),
MNRJ 32113(5). Gymnotus carapo: MNRJ
28617(9), MNRJ 28597(2), MNRJ 32211(5),
MBML 1452(5). Hoplerythrinus unitaeniatus:
MNRJ 28330(1). Hoplias malabaricus: MNRJ
28348(2), MNRJ 28344(2), MNRJ 28349(1), MNRJ
28341(7), MNRJ 28331(2). Hyphessobrycon
bifasciatus: MNRJ 32103(5), Hypostomus cf. affinis:
MNRJ 29074(5), MNRJ 29069(1), MNRJ 29063(8),
MNRJ 29059(1), MNRJ 29057(1). Imparfinis aff.
minutus: MNRJ 28622(4), MNRJ 28618(52), MNRJ
28612(4), MNRJ 28605(1), MNRJ 28592(11).
Leporinus copelandii: MNRJ 28340(1), MNRJ
29062(3), MNRJ 28336(1). Microglanis pataxo:
MNRJ 28397(10). Mimagoniates microlepis: MNRJ
32213(22), MBML 1452(5), Neoplecostominae
(Nova espécie): MNRJ 28613(1), MNRJ 28609(1),
MNRJ 28601(21). Oligosarcus acutirostris: MNRJ
28604(3). Otothyris travassosi: MNRJ 28614(1),
MNRJ 28593(52), MNRJ 32051(3), MBML
1455(2). Parauchenipterus striatulus: MNRJ
28594(2), MNRJ 28296(24), MNRJ 28295(74).
Pimelodella aff. vittata: MNRJ 29071(2), MNRJ
29073(31), MNRJ 29070(2), MNRJ 29065(4),
MNRJ 29060(1), MNRJ 29055(11). Poecilia
reticulata: MNRJ 28624(3), MNRJ 28626(26),
MNRJ 28610(45). Poecilia vivipara: MNRJ
28608(3), MNRJ 28603(12), MNRJ 28598(1),
MNRJ 28595(2), MNRJ 32041(4), MBML 1453(4).
Rhamdia sp. 1: MNRJ 29114(2), MNRJ 32217(1),
205
MBML 1436(1), MNRJ 29113(12), MNRJ
32195(1), MNRJ 29112(1), MNRJ 29111(3), MNRJ
32073(1). Scleromystax prionotos: MNRJ 28707(1),
MNRJ 28706(15). Trichomycterus pradensis: MNRJ
28489(2), MNRJ 28488(12), MNRJ 28483(20),
MNRJ 28487(9), MNRJ 28486(1).
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Received November 2008
Accepted March 2009
Occurrence of the white anglerfish, Lophiodes beroe Caruso, 1981
(Lophiiformes: Lophiidae), in Brazilian waters.
MATHEUS MARCOS ROTUNDO1 & TEODORO VASKE JÚNIOR2
1
Acervo Zoológico da UNISANTA (AZUSC), Rua Oswaldo Cruz, 266 - Bloco B - 3º andar/ sala B-31A CEP:11045-907,
Santos SP. Email: mmrotundo@unisanta.br
2
Laboratório de Elasmobrânquios, UNESP, Praça Infante Dom Henrique s/n CEP: 11330-900 São Vicente SP Email:
vaske@ig.com.br
Abstract. One specimen of the lophiid white anglerfish, Lophiodes beroe was collected for the
second time in Brazilian waters, which far extends the limit distribution of the species to
southeastern region (25o00’08’’S).
Key Words: New record, ichthyofauna, trawl fishery, upper slope, Southwestern Atlantic
Resumo. Ocorrência do peixe-pescador-branco, Lophiodes beroe Caruso, 1981
(Lophiiformes: Lophiidae), em águas brasileiras. Um espécime do peixe-pescador-branco,
Lophiodes beroe foi coletado pela segunda vez em águas brasileiras, o que amplia o limite de
distribuição da espécie para a região sudeste do Brasil (25o00’08’’S).
Palavras-chave: Novo registro, ictiofauna, pesca de arrasto, talude superior, Atlântico sudoeste
Lophiiformes are known as anglerfishes due
to the illicium and the esca, a pendulous fleshy
structure modified from the first spine of the dorsal
fin that are used as false bait for capture of preys.
With the exception of the Neoceratiidae, all families
of this order show this structure, varying widely in
shape, size, and presence of the esca, among other
characters (Nelson 2006). The Lophiidae is
represented by four genera and twenty five species
(Caruso 1983), where Lophius is the most important
genus due to its commercial value.
In Brazilian waters the main species of the
family, the monkfish, Lophius gastrophysus Miranda
Ribeiro, 1915, recently became a target species of
deep waters fishing fleet in the southern and
southeastern regions (Perez et al. 2002a,b; Perez et
al. 2003a,b; Perez & Wharlich 2005, Valentim et al.
2007, 2008). Lophius gastrophysus occurs from
North Carolina (USA) to Argentina in waters usually
between 40 and 180 m, but also occur up to 660 m
deep (Figueiredo et al. 2002), and is captured by
deepwater gillnet fishery and as bycatch of shrimp
fishery (Wharlich et al. 2004, Valentim et al. 2007).
Another genus, Lophiodes contains 13 species
(Caruso 1985, Froese & Pauly 2009). Costa et al.
(2007) reported about the occurrence of Lophiodes
beroe in Brazilian waters, during a deep exploratoryfishing cruise performed by the R/V Thalassa,
between 11oS and 22oS in 2000, but the authors just
cite its presence without any further explanation.
The main diagnostic characteristics that differs
Lophiodes beroe from the similar L. gastrophysus
are the body slightly narrow than L. gastrophysus,
and the gill openings of Lophiodes that are very
large and extends not only behind the pectoral fin,
but in front of it as well (Caruso 1985) (Fig. 1). In
Lophius gill opening is more restricted, being
located below and behind the pectoral fin. Also, the
pectoral fin shape in Lophiodes is narrow and
paddle-like, with a relatively low number of rays
(14-21), whilst in Lophius the pectoral fin is broad
and fan-like, with a relatively high number of rays
(22-28). In the present report, one specimen was also
captured by the R/V Soloncy Moura (CEPSULIBAMA) in the position 25º00’08’’S;45º27’38’’W
straight ahead Ilha Comprida, São Paulo state,
southeastern-Brazil, 99.5 m deep along the upper
slope coast (Fig. 2). Our specimen measured
Occurrence of the white anglerfish Lophiodes beroe in Brazilian waters
157 mm total length, with 18 pectoral fin rays. In the
description of the species, Caruso (1981) observes
that L. beroe inhabits the Western North Atlantic,
with northern distribution at 24º24’N. According
Caruso et al. (2007), L. beroe attains a maximum
size of 300 mm, commonly observed with 150 mm,
restricted in region between Southeastern USA and
northern coast of South America. The present
sample extends the South American limit of the
species to more than 3500 km in straight line to
25oS, in southeastern Brazil.
209
Although L. beroe attains smaller lengths
than L. gastrophysus, both are similar in shape,
which may cause confusion during identification
onboard by the fishermen, and so, individuals of L.
beroe may be normally included as part of the
commercial catches of L. gastrophysus. In this way,
it is probable that the species range can be even
extended for southernmost waters.
The specimen is stored in the Zoological
collection of Santa Cecília University (UNISANTA)
- AZUSC 2632.
Figure 1. Dorsal view and main differences between one monkfish (A), Lophius gastrophysus (400 mm total length)
and the white anglerfish (B), Lophiodes beroe (AZUSC 2632, 157 mm total length). Arrows indicate the gill openings
that are very large and extends in front of the pectoral fin in L. beroe. The paddle-like shape of the pectoral fin is also
evident in L. beroe.
M. M. ROTUNDO & T. VASKE JUNIOR
210
Figure 2. Distribution of Lophiodes beroe in the Atlantic coast (dashed area). Limit of the northern distribution
(24º24’N); record of the R/V Thalassa (2000) (●); present study (x).
Acknowledgments
The authors are grateful to Dr. Otto
Bismarck Fazzano Gadig who provided support in
the UNESP-CLP laboratories, and to the crew of the
R/V Soloncy Moura (CEPSUL-IBAMA) during
samples.
References
Caruso, J. H. 1981. The systematics and distribution
of the lophiid anglerfishes: I. A revision of the
genus Lophiodes with the description of two
new species. Copeia, 1(3): 522–549.
of the lophiid anglerfishes. II. Revisions of the
genera Lophiomus and Lophius. Copeia, 1:1130.
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Relationships. Copeia, 4: 870-875.
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G. R. 2007. Deep-water chaunacid and lophiid
anglerfishes (Pisces:Lophiiformes) off the
south-eastern United States. Journal of Fish
Biology, 70:1015-1026.
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Nunan, G. W. A., Martins, A. S. & Olavo, G.
2007. Assembléias de teleósteos demersais no
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Schwingel, P. R., Rodrigues-Ribeiro, M. &
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& Ribeiro, M. R. 2002b. Análise da pescaria
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Lopes, F. R. A. 2003a. Estrutura e dinâmica
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gastrophysus no Sudeste e Sul do Brasil.
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Schwingel, P. R., Lopes, F. R. A., &
Rodrigues-Ribeiro, M. 2003b. Deep-sea
fishery off southern Brazil: recent trends of
the Brazilian fishing industry. Journal of the
211
Northwest Atlantic Fisheries Sciences, 31:
1–18.
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2007. Length structure of monkfish, Lophius
gastrophysus (Lophiiformes, Lophiidae),
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2008. Feeding ecology of monkfish Lophius
gastrophysus in the south-western Atlantic
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peixe-sapo (Lophius gastrophysus) com rede
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Boletim do Instituto Pesca, 30: 87–98.
Accepted April 2009
Published online June 2009
A mutton hamlet Alphestes afer (Bloch, 1793) reproductive
event in northeast Brazil
1,2,3
DIEGO VALVERDE MEDEIROS , JOSÉ DE ANCHIETA C. C. NUNES
3,4
& CLÁUDIO L. S. SAMPAIO
3
1
Centro de Pesquisa e Conservação dos Ecossistemas Aquático - BIOTA AQUÁTICA. Email: bolamedeiros@gmail.com
2
Centro de Ecologia e Conservação Animal – ECOA
Grupo de Estudos de Ambientes Recifais da Bahia
4
Museu de Zoologia, Instituto de Biologia, Universidade Federal da Bahia
3
Abstract. We present here the first record of a reproductive event of the mutton hamlet, Alphestes
afer, in Brazilian waters. Four individuals participated in the event, which lasted approximately 30
minutes at dusk.
Keywords: reproductive event, mutton hamlet, Alphestes afer, shallow waters, northeast Brazil
Resumo. Um evento reprodutivo da garoupa-rajada Alphestes afer (Bloch, 1793) no Nordeste
do Brasil. Apresentamos aqui o primeiro registro em águas brasileiras de um evento reprodutivo
da garoupa-rajada, Alphestes afer. Quatro indivíduos participaram do evento que durou
aproximadamente 30 minutos no período do crepúsculo.
Palavras-chave: evento reprodutivo, garoupa-rajada, Alphestes afer, águas rasas, nordeste
brasileiro
The Epinephelidae family is an important
group of carnivorous marine fishes that occur in
tropical and subtropical waters throughout world.
The family was recently revalidated following
molecular and morphologic studies, which separated
some species that were previously part of Serranidae
(Smith & Craig 2007). Along the Brazilian coast
there are probably 25 species of this family,
including groupers and hinds (Carvalho-Filho, pers.
com.).
The mutton hamlet, Alphestes afer, is found
in the southwest Atlantic from Florida (USA) to
Santa Catarina (Brazil), including the Bermuda
Islands, Bahamas and Cuba in the Caribbean Sea
and Western Africa from Guinea, type locality, and
São Tomé and Prince (Craig et al. 2006, Hostim et
al. 2006, Wirtz et al. 2007, Sampaio & Nottingham
2008). It is a relatively small-sized species that
reaches 33 cm of total length (TL). The muttom
hamlet displays solitary and sedentary habits during
the day, sheltering in rocky crevices and above
algae. It feeds mainly on crustaceans at dusk and
after nightfall (Randall 1967, Heemstra & Randall
1993, Sampaio & Nottingham 2008).
We report here a reproductive behaviour of a
small school of mutton hamlet. Our observations
occurred opportunistically in 05 October (2008) in
the rocky reef of Farol da Barra, located at the
entrance of Baía de Todos os Santos – BTS
(northeast of Brazil). We observed the behavior of
the fishes using the focal group method while
snorkeling (Altmann 1974). Photographic records
were obtained with a Sony WPC 4 MP. The
sequence of events occurred at dusk (5:20p.m. to
6p.m.) at two meters in depth, during high tide, with
~3m of horizontal water transparency and at crescent
moon phase. The site where the observation was
made has a sandy bottom, filamentous and foliage
algae and the zoanthid Palythoa sp.
Four grouped individuals were sighted. The
largest individual (A) had ~30 cm TL, apparently a
female, presenting a lighter coloration and big belly,
while the other three had between 20 to 25 cm TL
(B, C, e D) (most likely males) and displayed a
A mutton hamlet Alphestes afer reproductive event in northeast Brazil
darker coloration, typical of courting male
epinephelids (Tresher 1984, DeLoach & Humann
1999). During the observations, individuals B, C,
and D followed A, attempting to approach it.
However, only one fish (B) was able to maintain
direct contact with individual (A). Individual B bit
the back of A and also behaved agonistically when
the other fishes approached. Subsequently,
213
individuals A and B rested laterally to the
substrate (Fig. 1) where they maintained physical
contact between their bellies. The release of their
gametes occurred after a few minutes close to the
substratum. The other two individuals moved away
to a distance of approximately 1 m from the
spawning couple. The episode lasted approximately
30 minutes.
Figure 1. Two individuals of Alphestes afer during a reproductive event. Note the physical contact between the
individuals. Photographed by D.V. Medeiros.
One day before, in same locality and horary
was observed many muttons hamlet closeness,
probably as same individuals the after day; however
no signs of reproduction event were registered.
Reef fish exhibit a great variety of
reproductive strategies, from spawning aggregations
to spawning in pairs (Tresher 1984, Domeier &
Colin 1997, DeLoach & Humann 1999, Krajewski &
Bonaldo 2005). Some groupers make their way to
spawning sites in the beginning of spring and
summer, migrating long distances to a specific
location in order to join with other individuals
(Tresher 1984, Shapiro 1987, Sadovy 1996,
DeLoach & Humann 1999). We believe that because
of the small size and sedentary habits, A. afer was
not pursuing breeding migration.
The majority of marine fish, specially
groupers of the Epinephelidae family, that display
lunar spawning rhythms, reproduce at the new or full
moon (Domeier & Colin 1997), suggesting that there
may be some selective advantages associated with
spawning at spring tide as the tide has greater
amplitude (Johannes 1978). Moreover, the lunar
cycles apparently help to synchronize the spawn
(Lowe-Mcconnell 1999). The event reported here
occurred at the crescent moon, making it difficult to
associate A. afer spawning synchronization with the
lunar cycle. Curiously, non-lunar spawning has been
reported for a few species of epinephelids (Hereu et
al. 2006, Erisman et al. 2007, 2009).
Among the Atlantic marine fish species, the
Epinephelidae, Serranidae and Lutjanidae family
received great research and conservation attention
because of their characteristic of forming spawning
aggregations (Claro & Lindeman 2003, Sadovy &
Domeier 2005). A reproductive aggregation occurs
MEDEIROS ET AL.
214
when one or more species convene at a certain place
and time with a reproductive end. When a large
number of normally dispersed fishes organize in
predetermined areas and times, they become highly
vulnerable to overfishing (Colin et al. 2003, Sadovy
& Cheung 2003, Sadovy & Domeier 2005). Previous
studies have documented that from the original five
historic aggregation sites in the Caiman Island for
Epinephelus striatus, three are inactive or
commercially extinct due to overfishing (Whaylen et
al. 2004).
In Brazil, the goliath grouper Epinephelus
itajara, an endangered species according to IUCN
(The World Conservation Union) (Tak-Chuen &
Ferreira 2006), is known to reproduce during
summer, with reproductive aggregations observed in
December (full moon) and occasionally in January
and February in Babitonga bay, Santa Catarina
(Brazil) (Gerhardinger et al. 2006, 2007). However,
no bibliographic or anecdotal information exists
concerning reproductive aggregations of small and
cryptic epinephelids, such as A. afer. We do not
consider the reproductive event described herein a
spawning aggregation, since only two individuals
spawned simultaneously.
In spite of its relatively small size, A. afer is
captured for consumption and ornamental trade
within BTS (Sampaio & Nottingham 2008). The
only similar feature between the reproduction of
large groupers and the reproductive event of A. afer
reported here was the dusk period (Claro &
Lindeman 2003).
Our observations confirm that mutton
hamlet can spawn in shallow waters. We suggest
that shallow reefs inside the BTS are an important
reproductive site for A. afer. However, future studies
focusing on the periodicity of these events, the
influence of lunar phases, the average size at sexual
maturation and possible occurrence of migration for
reproductive events will elucidate some of the
questions raised in this paper.
Acknowledgements
Dra. Alina Sá Nunes (UCSal/UNIME) the
loan of digital camera, Camilo M. Ferreira (UESC)
and Ericka C.O. Coni (CI do Brasil) for suggestions
on the manuscripts, Leo Dutra (CMAR), Clarice
Lino (Fundação Pró Tamar), and Katie Brennan for
assistance on the English version. Alfredo de
Carvalho Filho (Fish Bizz Ltda.) for valuable
information about the family Epinephelidae. The
Programa Institucional Brasileiro de Iniciação
Científica - Universidade Católica do Salvador Fundação de Amparo à Pesquisa do Estado da Bahia
provided a fellowship to the author senior.
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dermatolepis
(Teleostei:
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Gerhardinger, L.C., Medeiros, R., Marenzi, R.C.,
Bertoncini, A.A & Hostim- Silva, M. 2006.
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Gerhardinger, L.C., Medeiros, R.P., Marenzi, R.C.,
Godoy, E.A., Freitas, M.O., Andrade, A.B. &
Hostim-Silva, M. 2007. Conhecimento
Ecológico Local no Planejamento e Gestão de
Áreas Marinhas Protegidas e na Conservação
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Accepted March 2009
New record of the alien mollusc Rapana venosa (Valenciennes 1846) in
the Uruguayan coastal zone of Río de la Plata.
ANDREA LANFRANCONI*, MARISA HUTTON, ERNESTO BRUGNOLI
& PABLO MUNIZ
Sección Oceanología, Facultad
andrea.lanfranconi@gmail.com
de
Ciencias,
Iguá
4225,
Montevideo
11400,
Uruguay.
*
E-mail:
Abstract. Rapana venosa, an invasive gastropod reported for the Río de la Plata estuary since
1998, represents a serious risk to the shellfish fauna with economic value of the region. In this
contribution new records in the Uruguayan coastal zone of the easternmost distribution limit are
presented. Also are discussed potential impacts of the range expansion over the local biodiversity.
Key words: biological invasion, gastropods, biodiversity, estuary, South-western Atlantic.
Resumen. Nuevo registro del molusco Rapana venosa (Valenciennes 1846) en la zona costera
Uruguaya del Río de la Plata. Rapana venosa, molusco invasor reportado para el Río de la Plata
desde 1998, representa un riesgo para la malacofauna de importancia económica de la zona. Se
presentan resultados sobre su límite este de distribución para la costa uruguaya y se discuten sus
potenciales impactos en la biodiversidad autóctona.
Palabras clave: invasión biológica, gastrópodos, biodiversidad, estuario, Atlántico Sud
Occidental.
As in other areas of the world, the southwestern Atlantic enclose many exotic aquatic species
(Schwindt 2001, Orenzans et al. 2002, Silva &
Souza 2004) and Uruguayan ecosystems are not an
exception of this scenario (Brugnoli et al. 2005,
2006, Muniz et al. 2005). Rapana venosa
(Gastropoda, Muricidae) is a large carnivore whelk
native from Asia (Tsi 1983, Chung et al. 1993). It
has been recorded in the Río de la Plata estuary for
the first time in 1998 by Scarabino et al. (1999) and
Pastorino et al. (2000). This species is frequently
found in surveys carried out in the middle and outer
portions of the estuary (Giberto et al. 2006, Carranza
& Rodríguez 2007, Carranza et al. 2007, Cortelezzi
et al. 2007).
Rapa whelks show wide termohaline
tolerance (Chung et al. 1993, ICES 2004),
fast growth, high fertility (ICES 2004, Harding
et al. 2007a), a planktonic phase ranging from
14 to 80 days (Mann & Harding 2000), tolerance
to water pollution and hypoxia (Zolotarev 1996).
All of these traits made this organism a successful
invader. Furthermore, this voracious predator
of molluscs (Savini et al. 2002) can be considered
one of the most unwelcome invasive species
impacting large native mollusc populations (Drapkin
1963, Zolotarev 1996, Giberto et al. 2006). Despite
its importance as an invasive species little is
known in South America about its distribution,
population structure, and potential ecological
impacts on the native benthic community and on the
trophic web.
Having
highlighted
Rapana
venosa
ecological importance, the present contribution aims
to report the expansion of its distribution range in the
Uruguayan coastal zone, and also to analyze
morphometric variables, sex-ratio and epibionts
coverture of the collected organisms.
The Río de la Plata (34º-36º30’ S, 55º58º30’ W) is a large extension (38,000 km2) and
shallow (5-25 m) coastal plain estuary that according
to salinity can be divided in upper (< 0.4) and outer
(0-33) (Framiñan et al. 1999) zones. This study was
carried out in a coastal area localized in the outer
zone (Fig. 1), characterized by rocky shores and
sandy beaches.
New record of the alien mollusc Rapana venosa in the Uruguayan coastal zone of Río de la Plata
217
Figure 1. South America, and Uruguay with the sampling zone studied in the Uruguayan coastal zone ().
Data was obtained by scuba diving on April
15 of 2006, using an squared sampler (5x5 m)
covering an area of 25 m2 in Playa Hermosa
(34°50´38´´S, 55°18´09´´W) at late afternoon.
Depth, water temperature and salinity were
measured in situ using a field conductimeter and an
echo-sounder (Table I).
Collected specimens of Rapana venosa were
immediately frozen and examined later in the
laboratory. Total shell length (SL) and Total shell
width (SW) were measured using a calliper (0.1
mm) (Fig. 2). Total animal wet weight (TW) was
recorded using a digital scale balance (0.1 g). To
analyze the relationship between SL and other two
variables, regression test were performed using the
four common models (i.e. lineal, logarithmic,
exponential and geometric), verifying with the
determination coefficient the best one. The sex was
determined by the presence of penis and reddishbrown gonads (male) and absence of penis and the
presence of gonopore and yellow gonads (female).
Also we analyzed organisms for signs of imposex
anomalies in the reproductive apparatus, the
imposition of male sexual characters including a
penis and vas deferens onto females under toxic
effects of pollutants (Mann et al. 2006). Coverage
type and percentage of epibionts were also
determined.
Environmental variables measured in the
sampling site are presented in Table I. The total
number of snails recorded was 18 (0.72
individuals/m2). Shell length ranged between 57.3
and 81.2 mm, width between 45.1 and 61.3 mm and
total weight ranged from 41.1 to 91.1 g. The best fit
for Log SL vs. Log SW and Log SL vs. Log TW
relationship was obtained applying a lineal model
(Y= ax+b), with R2 of 0.68 and 0.73 respectively
(Fig. 3). The ratio of males and females was 0.64,
being 39% and 61% mean values of males and
females respectively. The lack of imposex signs in
females of the present study could be interpreted as a
symptom of a healthy population or a signal that this
population had not been exposed enough time to
TBT to develop signs of imposex. In relation to the
epibionts the following taxa were identified:
Coelenterata (Anthozoa: Anemone sp.), Annelida
(Polychaeta: Polydora sp.), Mollusca (Bivalvia:
Ostrea sp.), Arthropoda (Crustacea: not identified
barnacles)
and
Bryozoa
(Cheilostomata:
Membranipora sp.), being the last two the most
abundant. The majority of the specimens (67%)
presented low epibionts cover (0-25% of coverage).
Table I. Tolerance range of Rapana venosa to temperature, salinity, type of sediment and depth at native
regions and other invaded regions, and the data obtained in this work (study area).
Study Area
Native region
Other invaded regions
1.5
ND
up to 40
sand-rock
hard sand
sand -rock
Temp. (°C)
18.5
4-35
7-24
Salinity
16.6
ND
25-32
Depth (m)
Substratum (type)
ND = no data
218
A. LANFRA
ANCONI ET AL.
m
in thhe present stud
dy. SW= totall
Figure 2. Raapana venosa: Ventral and dorsal view, with biometriic variables measures
shell width, SL=
S total shelll length.
Figure 3. Raapana venosa: Relationships between SL vs SW and SL vs TW. Equuation of the bbest model fittted and R2 aree
also presenteed in the figuree.
Eveen though the reducced numberr of
organisms collected in
i this stuudy, the reesults
obtained coould be useeful as an approach too the
potentially problem
p
thatt this invasioon could cauuse in
the Uruguayyan coastal zone.
z
As farr as we know
w the
present daata constitutted the firrst approachh to
population feature
f
in the eastern disstribution lim
mit of
the species in Uruguay.. Figure 4 shhows the advvance
of rapa poppulations sinnce 2005. Thhe abundancce of
rapa individdual here reeported (0.772 individual/m2)
are higher thhan those repported by Saavini et al. (22004)
for the norrthern Adriaatic Sea. Thhe size rangge of
organisms here
h
recordeed and the coommon pressence
of egg masses with liviing larvae, during
d
the auustral
summer (peersonal obseervations of the authors) are
both an inddication thatt R. venosa populationss are
matu
ure and estabblished.
Considering all stuudies perform
med in thiss
regio
on of South America, thhe present distribution off
R. venosa
v
seems to be restrricted exclussively to thee
Río de la Plata estuary (Figure 4). The lack of rapaa
indiv
viduals in the
t Atlantic Ocean coaast could bee
attrib
buted to thee presence oof the nativ
ve gastropodd
Stra
amonita
h
haemastoma
(Linnaeus
1767,,
Murricidae), sincce the environmental ch
haracteristicss
of this
t
zone arre in the raange established for R.
veno
osa. S. haaemastoma could be a possiblee
com
mpetitor that occupies a similar ecological nichee
and is also a larrge active prredator (Rios 1994) thatt
seem
ms to be higghly salinityy dependent and cannott
enteer the estuarry, then, is restricted to
o the oceann
wateers. Howeveer, the questiion about iff rapa whelkk
A
Sciennces (2009), 4(2): 216-221
can outcompete S. haemastona is still open. Since
molluscan invasions in estuaries and marine
ecosystems have hardly altered communities
(Carlton 1999), the need for specific research on this
topic is highlighted as a warning to native
biodiversity loss. The life history and reproductive
strategies of R. venosa, combining characteristics of
both r and K strategies, facilitates its development in
niches that may be available or used in the new
habitats and fruitfully compete with native species
that share habitat requirements (Harding et al.
2007b).
-33
Rapana venosa
-34
Uruguay
N
A
-35
B
Río de la Plata
Argentina
-36
-37
-59
-58
-57
-56
-55
-54
-53
Figure 4. Distribution of Rapana venosa, modified of
Brugnoli et al. 2007. Black dots: distribution at 2005; red
dots, actual range of distribution: A: Playa Hermosa (this
report), B: Punta del Este (unpublished data, collected in
October 2008).
In the Río de la Plata estuary the coexistence
of this predator (R. venosa) with populations of
native bivalves (e.g. Mactra isabelleana, Ostrea
puelchana) could be related to the predation pressure
over this indigenous species (Giberto et al. 2006).
The Uruguayan coastal zone, and particularly the
outer Río de la Plata, has important mussel banks of
the commercially exploitable blue mussel (Mytilus
edulis platensis) which are the first mollusc resource
of the country (Riestra & Defeo 1994). In this sense,
the spread of R. venosa could be a threat for this
natural resource, as stated before by Scarabino et al.
(1999). Moreover, local fishermen reported that rapa
whelks usually are found in the long lines eating
over the baits (dead fish) near the rocky shores
where also mussels are inhabiting (mean depth of 2
m).
Researches on the first stages of invasions
are necessary in order to detect exotic species before
they cause damage to local community and
ecosystems. It is clear that once established in the
new environment, the eradication of exotic species is
not easy (de Poorter 1999). Therefore, only with a
good knowledge of the distribution, ecology, life
history and impacts of alien species it would be
219
possible to improve management and control.
Acknowledgment
Special thanks to EC Incofish Project
Contract 003739 (WP3) for partially supported the
study. Thanks to M. Diaz, F. Scarabino, I. Pereyra,
J.M. Clemente and M. Bessonart for collaboration in
the field sampling. The manuscript was enhanced by
the comments and suggestios of three anonymous
reviewers.
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Accepted May 2009
Biofouling of the golden mussel Limnoperna fortunei (Dunker, 1857)
over the Anomura crab Aegla platensis Schmitt, 1942.
MICHELLE N. LOPES*; JOÃO P. VIEIRA & MARCELO D. M. BURNS
Universidade Federal do Rio Grande, Instituto de Oceanografia, Laboratório de Ictiologia, CP 474, Rio Grande, RS,
Brazil. Phone: +55-53 3233 6539; FAX: +55-53 3233 6602. *Email: michellebiors@yahoo.com.br
Abstract .This note reports the first occurrence of golden mussel Limnoperna fortunei (Dunker,
1857) colonizing (biofouling) the surface body of the anomuran crab Aegla platensis Schmitt,
1942 on the São Gonçalo channel, Mirim Lagoon, Brazil. One live individual of A. platensis (25.5
mm tail to head; 2.8 g) was colleted at São Gonçalo channel carrying 62 individuals (30.4 g) of L.
fortunei, with total length ranging from 7 to 23 mm. The total weight recorded for the crab was 10
times lower than the total weight of the bivalves incrusted, which suggest that this could be a new
factor affecting the preservation of this endemic South America crab that is already in a vulnerable
state of conservation in the Rio Grande do Sul, state. Like A. platensis, other benthic invertebrates
could be also negatively affected by L. fortunei, and further investigation is currently needed to
assess the potential ecological negative effects on the local biodiversity.
Key-words: Biodiversity, biofouling, Limnoperna fortunei, South America.
Resumo. Bioincrustação de mexilhão dourado Limnoperna fortunei (Dunker, 1857) sobre o
caranguejo Anomura Aegla platensis Schmitt, 1942. Esta nota relata a primeira ocorrência da
colonização de mexilhão dourado Limnoperna fortunei (Dunker, 1857) sobre a superfície do corpo
(biofouling) do crustáceo Anomura Aegla platensis Schmitt, 1942 no canal São Gonçalo, Lagoa
Mirim, RS, Brasil. Um exemplar vivo de A. platensis (25,5 milímetros de comprimento total; 2,8 g
de peso) foi coletado no Canal São Gonçalo com 62 indivíduos de L. fortunei (30,4 g) fixados
sobre sua carapaça, com comprimento total variando de 7 a 23 mm. O peso total registrado para o
crustáceo foi aproximadamente 10 vezes menor do que o peso total dos bivalves incrustados, o que
sugere que este fator seria um novo agravante ao estado de conservação destes crustáceos,
endêmicos da América do Sul, que já se encontram em estado vulnerável de conservação na região
do Rio Grande do Sul. Assim como A. platensis, outros invertebrados bentônicos podem estar
sendo ameaçados pelo L. fortunei, sugerindo a necessidade de futuras investigações sobre
bioincrustação no sistema.
Palavras-chave: Biodiversidade, bioincrustação; Limnoperna fortunei, América do Sul.
Although species distribution changes
naturally over time, human activities greatly increase
the rate and the spatial scale of these changes by
accidentally or deliberately moving organisms
across the world (Ricciardi & MacIsaac 2000). The
introduction of invasive species threatens native
biodiversity, ecosystem functioning, animal and
plant health, and human economies.
Limnoperna fortunei (Dunker 1857), the
Asian golden mussel, is an invasive freshwater
species that shares several features with the zebra
mussel Dreissena polymorpha (Pallas 1771),
arguably the most influential animal to ever invade
North American fresh waters (Thorp et al. 1998).
Both have filter-feeding habits, are epifaunal and
attach to hard substrates by means of a byssus and
have fast growth rates (Boltovskoy & Cataldo 1999,
Boltovskoy et al. 2006, Karatayev et al. 2007a). Its
veliger larvae allows a quick dispersal through
several mechanisms including water currents, animal
and ship transport (ballast waters), and fishing
activities (Morton 1977, Garcia & Protogino 2005),
although the attachment to vessels is by far the most
important dispersion mechanism of golden mussel
Biofouling of the golden mussel Limnoperna fortunei over the Anomura crab Aegla platensis
(Boltovskoy et al. 2006, Karatayev et al. 2007b).
The golden mussel was first found in South
America in the coast of Río de la Plata, Buenos
Aires province (Pastorino et al. 1993). Its occurrence
has been reported in the main hydrologic systems of
the region: coastal zones of Río de la Plata
(Darrigran et al. 1998), Paraguay, Paraná, Salado
and Uruguay Rivers (Darrigran & Ezcurra de Drago
2000, Darrigran 2002). It was first recorded in Patos
Lagoon in 1999 by Mansur et al. (1999, 2003) and
in 2005 was found at the adjacent Mirim Lagoon,
probably through a dispersion via the São Gonçalo
channel that connects both lagoons (Langone 2005,
Burns et al. 2006a, 2006b).
The combination of early sexual maturity,
high fecundity, semelparity and wide environmental
tolerance probably allow L. fortunei to be a
successful invader into new environments. The high
densities of golden mussel and their fixation to the
substrate by its byssal threads result in the formation
of a new continuous microenvironment, which
provide a new substrate by some epifaunal species
and, at the same time, can lead to the displacement
of other organisms (Darrigran 2002). Colonization is
not restricted to man-made structures, such as
revetments, piers, rock armors, gabions, boat hulls
and others, since the golden mussel also settles on
biogenic material such as debris, driftwood, reed
roots (Boltovskoy et al. 2006). Among the potential
impacts associated with the presence of this invasive
bivalve, the rapid change produced in benthic
communities should be noted. Since its invasion of
the Plata Basin, L. fortunei has modified the natural
occurrence and abundance of several native
macroinvertebrates species (Martin & Darrigran
1994, Darrigran et al. 1998).
In the area of Guaíba lake at Patos Lagoon
system, Mansur et al. (2003) reported that the
golden mussel attaches to at least 6 species of
mollusks in numbers up to ca. 300 individuals per
host. In several cases this overgrowth may hinder the
host’s normal displacement and valve mobility.
Darrigran et al. (2002), in Argentina, also reported
the settlement of the golden mussel on other bivalve
species, as well as in the anomuran crab Aegla
platensis Schmitt, 1942. The present paper reports
the first occurrence of L. fortunei colonizing the
surface body of A. platensis in the São Gonçalo
channel.
Bottom trawl sampling was carry out in São
Gonçalo channel in waters 3 to 6 m deep (Fig. 1) on
June 13th, 2008. Sampling was conducted using a
fishermen wood boat (10.9 m long, with a 60 Hp
motor). Five minutes sample (approximately 400 m
beginning at 32º7’40.86” S; 52º36’41.91”) were
223
performed using an 10.5 m (head rope) shrimp trawl
(1.3 cm bar mesh wings and body with a 0.5 cm bar
mesh cod end liner, and a pair of weighted outer
doors.
Figure 1. Mirim Lagoon and its drainage basin (62.250
Km2), showing the São Gonçalo channel that connecting
it with the Patos Lagoon. The red dot represent the
location (32º7’40.86” S; 52º36’41.91” O) where A.
platensis was collected. Modified from Machado (2007).
One live individual of A. platensis (25.5 mm
tail to head; 2.8 g) was colleted carrying 62
individuals (30.4 g) of L. fortunei, with total length
(TL) ranging from 7 to 23 mm (Fig. 2). In addition
to the golden mussel, 28 live gastropods (Heleobia
spp.) were also observed trapped into the byssus net.
Figure 2. Specimen collected, showing the fouling of L.
fortunei on A. platensis.
Comparing the size ranges of the golden
mussels with those reported on the literature
(Magara et al. 2001, Maroñas et al. 2003) it is
possible to suggest that the majority of the golden
M. N. LOPES ET AL.
224
mussel individuals found attached to A. platensis can
be considered adults with more than 2 years
(>17mm TL; Fig. 3), suggesting that the
colonization started long time before the sampling
date. The total weight recorded for the crab (2.8 g)
was 10 times lower than the total weight of the
bivalves incrusted (30.4 g), which could suggest that
this infested crab would have more difficulties in
finding shelter and/or avoiding predation and
increased rates of energy consumption.
Figure 3. Size range of L. fortunei observed at A.
platensis.
The aeglids are a peculiar group of
crustaceans because they are the only Anomura that
occurs on fresh waters. They are endemic to South
America and occur in streams, rivers, lakes and
currents. They show nocturnal activity and sheltered
under rocks, leaf litter and plant debris during the
day. They are vulnerable to changes on their habitat,
and they are under serious risks to become extinct
even before they had been properly studied (BondBuckup & Buckup 1994). Thus, the macrofouling of
L. fortunei on A. platensis on São Gonçalo Channel
reported here could be another potential factor
leading to the population decline of this crab, which
is already in a vulnerable conservation state (BondBuckup & Buckup 1994). Like A. platensis, other
benthic invertebrates could be also negatively
affected by L. fortunei. Further investigation is
currently needed to assess the current finding and its
potential ecological negative effects on the local
biodiversity, including eventual indirect effects in
the community structure and local food webs.
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Received March 2009
Accepted April 2009
Zooplankton (Cladocera and Rotifera) variations along a horizontal
salinity gradient and during two seasons (dry and rainy) in a tropical
inverse estuary (Northeast Brazil)
ANA M. A. SILVA1*, JOSÉ E. L. BARBOSA1, PAULO R. MEDEIROS2, RENATO M. ROCHA3,
MILTON A. LUCENA-FILHO3 & DIÓGENES F. SILVA3
1
Departamento de Biologia, Universidade Estadual da Paraíba (UEPB), Av. das Bananeiras, 351, CEP 58109-753,
Campina Grande, PB, Brazil. *ana.maria.bio@gmail.com
2
Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba
(UFPB), Cidade Universitária, Campus I, CEP 58059-900, João Pessoa, PB, Brazil
³Laboratório de Ecologia do Semi-Árido (LABESA), Universidade Federal do Rio Grande do Norte (UFRN), R. José
Evaristo, CEP 59300-000, Caicó, RN, Brazil.
Abstract. The present study investigated the influence of environmental variables on the spatial
and temporal composition of the most abundant zooplankton groups (Cladocera and Rotifera) in a
tropical inverse estuary located in a salt pond-dominated area. Zooplankton and twelve
environmental variables were sampled at nine permanent stations throughout a two-year period
(Sep 2005 to Sep 2007). A total of nineteen species, mostly freshwater dwellers, was detected
throughout the study and ten species accounted for 97% of all individuals. Mean species richness
and abundance were significantly higher at the uppermost stations, but only during the rainy
seasons, when salinity drastically decreased due to freshwater input. According to multiple
regression and canonical correspondence analyses salinity, nutrients, pluviometry, pH,
Chlorophyll-a and transparency were the most important predictors of zooplankton community
structure. The low community diversity and strong dominance of the pollution-tolerant Brachionus
genus (80% of all individuals) support the idea that only plastic species are able to cope with
harsh spatial and seasonal variations such as the ones observed during our observations in the
estuary.
Key words: Brazil, community, estuary, salinity gradient, zooplankton.
Resumo. Variações do zooplâncton (Cladocera e Rotifera) ao longo de um gradiente
horizintal de salinidade e durante duas estações (seca e chuvosa) em um estuário tropical
inverso (Nordeste do Brasil). O presente estudo avaliou a influência de variáveis ambientais na
composição espacial e temporal dos grupos zooplanctônicos mais abundantes (Cladocera e
Rotifera) em um estuário tropical inverso localizado numa área dominada por salinas. O
zooplâncton e doze variáveis ambientais foram amostrados em nove pontos permanentes ao longo
de um período de dois anos (Set 2005 a Set 2007). Um total de dezenove espécies, a maioria
habitante da água doce, foi observado durante o estudo e dez espécies representaram 97% de todos
os indivíduos. As médias de riqueza de espécies e abundância foram significativamente maiores
nos pontos superiores próximos à margem do rio, mas somente durante os períodos chuvosos,
quando a salinidade reduziu-se drasticamente devido ao influxo de água doce. De acordo com as
análises de regressão múltipla e correspondência canônica, salinidade, nutrientes, pluviometria,
pH, Clorofila-a e transparência foram os mais importantes preditores da estrutura da comunidade
do zooplâncton. A baixa diversidade de comunidade e forte dominância do gênero Brachionus,
tolerantes a poluição (80% de todos os indivíduos), suporta a idéia de que somente espécies
plásticas são capazes de suportar variações espaciais e sazonais adversas como as observadas
durante as nossas observações no estuário.
Palavras-chave: Brasil, comunidade, estuário, gradiente de salinidade, zooplâncton.
Zooplankton variation in a tropical inverse estuary (Northeast Brazil)
Introduction
Brackish waters of typical estuarine systems
are the result of a mixture in freshwater and salt
water inputs (Remane & Schlieper 1971, McLusky
& Elliott 2004). Thus, one expects to find a
horizontal gradient of salt concentration in these
estuaries, with freshwater nearby the river border
and salinity increasing seawards to reach typical
oceanic levels. However, some estuaries show the
opposite pattern, with a horizontal gradient of salt
concentration increasing upstream (Hammer 1986,
Simier et al. 2004).
Salinity is amongst the most important
environmental factors with the potential to
significantly influence estuarine communities
(Savenije 2006). Therefore, fluctuations in salinity
and other environmental factors (e.g. temperature,
pH, nutrients and pigments) on both spatial and
seasonal scales, play major ecological roles
promptly controlling the composition and
distribution of estuarine species (Prado-Por &
Lansac-Tôha 1984, Lansac-Tôha & Lima 1993).
This is true, given that only select species are able to
cope with major environmental shifts (Hammer
1993).
The Mossoró River Estuary (MRE) is a 24
km inverse system in which salinity decreases from
the river border towards the sea, with salt
concentrations varying between saline and brackish.
Located in a semi-arid region, the high daily
evaporation rates (~1 cm/m³), low annual rainfall
and consequently low river outflow, are responsible
for this inverse pattern. Although inverse estuaries
are often considered a synonym for hypersaline
estuaries, in some cases such as in the MRE, salt
concentrations rarely exceed 50 g/l, which is stated
by Hammer (1986) as the minimum concentration
for a water body to be classified as hypersaline (see
McLusky & Elliott 2004, Simier et al. 2004).
The salt industry has been exploiting the
MRE for over 300 years and nowadays over 25
ponds for salt extraction are permanently located
along the estuary’s margin. The gross annual salt
production is approximately 2,400,000 tons and the
Rio Grande do Norte State (RN) is responsible for
up to 90% of Brazil’s salt production, with the
highest contribution coming from the MRE. As a
consequence of the long history of unregulated
exploitation, mangrove forests have been submitted
to high levels of impact, currently covering a
substantially smaller area relative to the original.
Atypical environments like the MRE
encompass a very small portion of the inland aquatic
environments of the world (Sassi 1991, Hammer
1993), but are of high scientific and economic
227
interest because of their uniqueness (Hammer 1986,
McLusky & Elliott 2004) and income prospective
(Coetzee et al. 1996, Lamberth & Turpie 2003).
Despite the importance of inverse estuaries,
many ecological processes which take place therein
are still poorly known, and need more thorough
investigations, especially at the community-level
(Hammer 1986, Sassi 1991, Neumann-Leitão et al.
1992, Bos et al. 1996, Williams 1998, Derry et al.
2003). Furthermore, areas which are subject to high
degradation due to human activities are particularly
important since species composition can be altered
throughout the years (Matsumura-Tundisi & Tundisi
2003).
The present study aimed at evaluating
zooplankton community composition spatially
(along a salinity gradient) and temporally
(encompassing dry and rainy seasons). We focused
on Cladocera and Rotifera zooplankton provided
those constitute the more diverse and abundant
metazooplankton groups in the study area. It was
hypothesized that salinity acts as a restraining force
on species abundance, whereas freshwater input (and
its associated nutrients) has a positive effect on the
community.
Material and methods
Study area. The study was carried out at the
Mossoró River Estuary (MRE), located in a
floodplain with an area of 14,276 km² in Rio Grande
do Norte (RN) state, northeastern coast of Brazil
(Fig. 1). The inlet extends for about 24 km from the
lower reach (salinity: ~ 10), nearby the South
Atlantic Ocean, to the uppermost portion (~ 28),
delimited by the river border, yet still influenced by
tidal fluctuation. Salinity increases, however, from
the lower reach of the estuary towards the sea and
typical marine regimes are observed in the ocean. It
has a maximum depth of 10 m with an average of 6
m. The region is under semi-arid climatic influence,
typically receiving low, yet concentrated annual
rainfall (rainy season between Feb and Jun). The
Caatinga, vegetation region dominated by xeric
shrublands and thorn forests, encloses most of the
area, albeit Restinga and Atlantic Forest areas are
also present. In addition, the estuary is under the
influence of constant winds (> 7 km/h during ~ 75%
of the year) and high water temperatures (~ 29ºC)
yearlong.
Sampling design.Monthly samples were
collected during two consecutive years (Sep-05 to
Sep-07) at 9 permanent sampling stations following
a horizontal gradient (~ 24 km) (Fig. 1). Throughout
the study span, 225 samples were collected during
the day (between 0800 and 1600) and at high tides
228
(for standarrdizing samppling). Althoough the verrtical
were
profile waas not invvestigated, samplings
s
A. M. A.
A SILVA ET AL.
standardized andd collected w
within the firsst 2 m of thee
wateer column.
Figure 1. Mossoró
M
Riverr Estuary andd associated zones.
z
Samplling stations indicated by numbers and
d direction off
increasing saalinity gradiennt indicated byy arrows. Insett: location of the
t study areaa in the Northeeastern coast of
o Brazil.
Zoooplankton was
w collectedd using a 600 µm
mesh size plankton
p
net of 25 cm mouth diameteer by
filtering 700 l of water at each sampling
s
staation.
Volume filtered was estimated
e
byy calculatingg the
horizontal tow
t
distancee with regardds to diametter of
mouth apertture area. Thhe collected individuals were
preserved inn 5% formalldehyde satuurated with sugar
s
(Haney andd Hall 19733). Three alliquots (1 ml
m of
volume eaach) were taken from
m each sam
mple
(between 800 and 140 ml
m of volume) and counteed on
a Sedgwickk-Rafter cham
mber. If an aliquot hadd less
than 100 inndividuals annother one was
w examinedd and
the resultss combinedd. The meean numberr of
each
individuals of the threee aliquots represented
r
sample. Quualitative and
a
quantitaative data were
calculated simultaneous
s
sly.
Twelve environmeental variaables weree
asseessed at the same statioons as the zooplankton.
z
.
Tran
nsparency (Secchi diskk), temperatture (digitall
therm
mometer),
salinity
(Fisher
portablee
refraactometer) and
a pH (Hannna portablee membranee
pHm
meter) were measured inn situ. Dissollved oxygenn
was measuredd followingg Winkler``s method..
Nutrrients conceentrations ((ammonia NH
N 3, nitritee
NO2, nitrate NO3 andd total phosphorous)
p
)
weree estimatedd accordingg to the proceduress
desccribed by Rodier
R
(19775), Mackeereth et al.
(197
78) and APHA
A
(19955). Chlorop
phyll-a andd
Pheo
ophytin concentrationns were determinedd
specctrophotomettrically baseed on the proceduress
desccribed in AP
PHA (1995). Pluviometriic rates weree
prov
vided by LA
ABESA (Laaboratory off Semi-Aridd
A
Sciennces (2009), 4(2): 226-238
Ecology) at the margin of estuary nearby each
sampling station.
Ecological indices and data analysis.
Species richness was expressed as the total number
of species in each sample. Additionally, log-based
Shannon`s index (H’) was calculated using Primer 5
software as a measure of community diversity (see
Krebs 1989).
Since data departed from normality, spatial
and seasonal variations were evaluated by
performing, respectively, non-parametric rank-based
Kruskal-Wallis one-way ANOVA and Friedman
ANOVA tests on Statistica 7 software (Sokal &
Rohlf 1995). All comparisons and correlations
(below) were considered significant when p values
were < 0.05.
Stepwise
multiple-regression
analyses
(MRA) were made using Statistica 7 to determine
the proportion of variance in zooplankton numbers
which could be attributed to environmental data
(Sokal & Rohlf 1995). In the regression models,
zooplankton abundances, richness and diversity
(separated by season) were entered as dependent
variables, and the environmental variables as
predictors of their variance. Data from rare species
(i.e., those which contributed < 1% of
total abundance) were excluded from the
individual species correlations, but contributed to
total richness, diversity and abundance. Prior
to the analyses, data was log-transformed (base
10) and linearity between variables and
multicolinearity between independent variables were
tested (Sokal & Rohlf 1995), but data proved to be
non-linear.
In addition to the MRA, a canonical
correspondence analysis (CCA) was performed with
log-transformed data (natural) using CANOCO 4.5
software (ter Braak & Smilauer 1998). For this test,
all species were included, but the downweighting of
rare species option was employed. The Monte-Carlo
randomization test (499 permutations under the
reduced model) was performed to assess the
probability of the observed pattern being due to
chance (see ter Braak 1986).
Results
Environmental
characterization. No
significant spatial variation was observed for
pluviometry (Fig. 2), but significant seasonal
variation was detected (Fig. 3). Salinity values
increased significantly upstream (between stations 1
and 9) (Fig. 2) and were significantly lower during
the rainy seasons (Fig. 3). Water temperature also
229
increased significantly upstream (Fig. 2), with a
trend towards higher values during the second rainy
season (Fig. 3). No significant spatial differences
were observed for pH values (Fig. 2), but lower
values were observed during the second rainy season
(Fig. 3). Water transparency values decreased
significantly upstream (Fig. 2) and showed
significant seasonal variation (Fig. 3). Although
spatial and seasonal differences were detected for
oxygen, no clear spatial patterns were observed and
a small trend towards higher values during the dry
season was detected (Figs. 2 and 3). No spatial
variation was detected for any of the nutrients (Fig.
2). Between seasons, higher values of NO2, NO3 and
total phosphorous were observed during the rainy
seasons (Fig. 3). Chlorophyll-a and Pheophytin
values significantly increased upstream (Fig. 2) and
a significant trend towards higher values during the
first rainy season was observed (Fig. 3). Species
composition and distribution. A total of 157,464
individuals belonging to 16 rotifer species
(Anuraeopsis fissa (Gosse), Brachionus angularis
(Gosse), Brachionus calyciflorus Pallas, Brachionus
caudatus Barrois & Daday, Brachionus falcatus
Zacharias,
Brachionus
leydigi
(Rousselet),
Brachionus patulus (Müller), Brachionus plicatilis
Müller, Brachionus urceolaris (Müller), Epiphanes
macrourus (Barrois & Daday), Filinia longiseta
(Ehrenberg),
Filinia
opoliensis
(Zacharias),
Hexarthra mira (Hudson), Keratella tropica
(Apstein), Keratella valga (Ehrenberg) and
Polyarthra vulgaris Ehrenberg) and 3 cladoceran
species
(Ceriodaphnia
cornuta
(Sars),
Diaphanosoma spinulosum Herbst and Moina
minuta Hansen) were collected throughout the study
span. The ten most abundant species, which
accounted for 97% of all collected individuals, were
(mean ind.l-1; relative abundance): B. urceolaris
(245.7; 35.1%), B. plicatilis (146.5; 20.9%), B.
calyciflorus (79.2; 11.3%), B. leydigi (73.9; 10.6%),
C. cornuta (47.2; 6.7%), E. macrourus (40.4; 5.7%),
H. mira (12.6; 1.8%), K. tropica (12.4; 1.8%), F.
opoliensis (10.1; 1.4%) and B. falcatus (8.6; 1.2%).
Each of the remaining nine species contributed to
less than 1% of all collected individuals.
Species richness significantly increased
upstream (Fig. 4) and community diversity
(Shannon’s index) showed a similar significant
pattern, albeit less marked (Fig. 4). Significant
seasonal fluctuations were observed for species
richness and diversity, which showed higher
values especially during the second rainy season
(Fig. 4).
230
A. M. A.
A SILVA ET AL.
Figure 2. Mean
M
values (±
± SE) of montthly records of
o environmen
ntal variables sampled duriing the 2-yearrs observationn
period at 9 permanent
p
stattions at the Mossoró
M
Riverr Estuary. SE variations specify the temp
mporal variancees of the dataa
within each sampling stattion. KW ANO
OVA results of comparisons among staations indicateed: *significan
nt at p < 0.055
and **signifi
ficant at p < 0.001.
Ressults of spatiaal distributioon of the ten most
abundant species reevealed som
mewhat sim
milar
w
significcant spatiall differences in
patterns, with
the densityy of five sppecies, whichh showed peaks
p
of abundaances betw
ween statioons 6 andd 9
(Fig. 5). Allso, all speciies showed highly
h
signifficant
seasonal vaariation in abundance
a
w
with
clear peaks
p
during the rainy seasoons, particullarly the seecond
one.
Zoooplankton-eenvironmenttal
variaables
associationns. Predictorrs of zooplannkton commuunity
weree fairly diffeerent betweenn the two seaasons (Tablee
I). According
A
to the regresssion modells, the mostt
impo
ortant variaables responnsible for zooplanktonn
variaance were pH, water temperaturee, NO2 andd
Chlo
orophyll-a during
d
the dry seasonss, and totall
phossphorous, waater transparrency, NO3, salinity andd
pH during
d
the raainy seasons.
For the canonical ccorresponden
nce analysis,,
the Monte-Carllo test waas significan
nt (test off
sign
nificance of all canonicaal axes: tracce: 0.65; F-ratio
o: 3.58; p < 0.01). Cum
mulatively, ax
xes 1 and 2
A
Sciennces (2009), 4(2): 226-238
Zooplanktonn variation in a tropical inveerse estuary (N
Northeast Brazzil)
accounted for 63.9% of the total variance, with
zooplanktonn-environmeental variablees correlationns of
0.77 (Axis 1) and 0.53 (Axis 2). Within
W
the biiplot,
two generall, somewhat divergent, groups
g
of species
were distincct. The first group compprised 14 species
whicch correlatted positiveely with
phossphorous, NH
H3, water teemperature,
a, or
o pluviomettry; the secoond group
speccies which correlated positively
transsparency or salinity
s
(Fig.. 6).
231
NO3, totall
ChlorophyllC
comprised
c
5
with waterr
Figure 3. Ennvironmental variables (± SE)
S sampled throughout
t
a 2-year
2
periodd at the Mossooró River Estu
uary averagedd
for the 9 staations. SE varriations speciffy the spatial variances off the data witthin each sam
mpled month. Shaded areass
indicate the rainy seasonss. Friedman ANOVA
A
resuults of comparrisons among months indiccated: **signiificant at p <
0.001.
Pan-Americcan Journal off Aquatic Scieences (2009), 4(2):
4
226-2388
232
A. M. A.
A SILVA ET AL.
Figure 4. Mean
M
values (±
± SE) of twoo ecological indices (richness and Shannnon’s index of diversity) sampled at 9
permanent sttations reflectiing an increassing salinity gradient
g
(left panel),
p
and thrroughout a 2-year period (rright panel) att
the Mossoró River Estuaryy. SE variatioons specify thee temporal vaariances of thee data within eeach sampling
g station (left))
and the spatiial variances of
o the data within each sam
mpled month (right). Shadeed areas indiccate the rainy seasons. KW
W
ANOVA andd Friedman ANOVA
A
resultts of comparissons spatially and temporallly, respectiveely, indicated: **significantt
at p < 0.001.
Figure 5. Mean
M
densities (± SE) of tenn zooplanktonn species sam
mpled at 9 perm
manent statioons reflecting an increasingg
salinity gradient (left paneels), and throuughout a 2-yeear period (rig
ght panels) att the Mossoróó River Estuarry. Data from
m
rare species (i.e. those whhich contribuuted to less thhan 1% of tottal abundancee) were excludded from the analyses. SE
E
variations sppecify the tempporal variancees of the data within each sampling
s
statiion (left) and the spatial vaariances of thee
data within each
e
sampled month (right)). Shaded areaas indicate thee rainy seasonns. KW ANOV
VA and Friedm
man ANOVA
A
results of com
mparisons spaatially and tem
mporally, respectively, indiccated: *signifi
ficant at p < 0..05 and **sign
nificant at p <
0.001.
A
Sciennces (2009), 4(2): 226-238
Discussion
Zooplankton (Cladocera and Rotifera) in the
Mossoró river estuary (MRE) was characterized
mostly by freshwater species with a fairly low
richness compared to other tropical estuaries (e.g.
Rougier et al. 2005). Nevertheless, Lansac-Tôha &
Lima (1993) made monthly collections throughout a
year and detected even lower richness than the
present study, suggesting that our results are
consistent with some estuary-based investigations,
where species richness tend to be lower than
freshwater and marine environments (see Hammer
1986, Neumann-Leitão 1994).
The low richness observed in the present
study clearly reflected the striking spatial and
seasonal fluctuations, particularly of salinity, on
freshwater dwellers. This is a common pattern, as
acknowledged by many authors (e.g. Prado-Por &
Lansac-Tôha 1984, Sassi 1991, Hammer 1993,
Lansac-Tôha & Lima 1993, Keller & Conlin 1994,
Williams 1998, Herbst 2001, Ara 2002, Derry et al.
2003, Toumi et al. 2005) suggesting a large-scale
occurrence of these relationships. Derry et al. (2003)
studying temperate saline lakes discerned patterns of
community composition along a gradient of salt
concentration. In tropical estuaries of Brazil, similar
findings have also been observed (see Prado-Por &
Lansac-Tôha 1984, Lansac-Tôha & Lima 1993,
Lopes 1994, Neumann-Leitão 1994, Magalhães et
al. 2006).
Further, richness and abundance increased
upstream, a seemingly inconsistency with the
observed negative relationship between zooplankton
and salinity, given that salt concentrations increased
likewise. However, species richness and abundance
at the more saline stations were only high during the
rainy seasons, when salt concentration substantially
decreased due to higher freshwater input. This alone
explains the seemingly odd higher richness and
abundance at the more saline stations, but not the
prevailing lower values at the less saline ones.
Seasonal salinity fluctuations due to freshwater
runoff were high at the more saline stations and a
corresponding high fluctuation in species numbers
was also observed. Conversely, both salinity and
species numbers showed very small seasonal
fluctuations at the less saline stations, likely because
the area was not significantly affected by the
freshwater input and was under higher tidal
dynamics. Hence, these stations uphold similar salt
concentrations yearlong, and it is reasonable to
associate the small variation in community
composition at these stations to a lack of seasonal
salinity fluctuation. At the higher stations, however,
233
richness and abundance increased as salinity
decreased. In fact, the majority of the species
identified in our study was exclusively found in the
stations nearby the river and during the second rainy
season (see below).
It is likely, however, that other factors may
have supported the observed higher numbers at these
higher stations, since, despite the proximity to the
river, salinity still remained higher there than at the
lower stations. As detected by some authors (Keller
& Conlin 1994, Herbst 2001), in addition to salinity,
small-scale differences in factors such as ion
composition (Derry et al. 2003), food availability
(Toumi et al. 2005) and predation pressure
(Williams 1998) may significantly alter the structure
of zooplankton communities in saline environments.
These processes need yet to be investigated in the
MRE. Alternatively, the more conspicuous shifts in
community composition at the higher stations may
be related to the rapid freshwater discharge which
displaced the individuals towards the estuary.
Rougier et al. (2005) reported a similar finding
associating higher rotifer richness in the estuary
during the rainy season to a mixing of populations
across the estuarine zone due to fluvial
hydrodynamics. It is not clear, however, if this was a
strictly mechanical passive dislocation or if some
active horizontal movement was made by the
species, since most individuals were alive when
collected, suggesting a tolerance to the conditions.
Whatever factor is involved, freshwater input was a
highly important determinant of species numbers as
previously acknowledged by other authors (e.g.
Osore et al. 1997, Mwaluma et al. 2003, Paranaguá
et al. 2005, Rougier et al. 2005, Magalhães et al.
2006). It is likely that richness and abundance were
higher during the rainy seasons due to more
favorable conditions provided by the rain,
particularly, diluting salt concentration, since most
species identified are typical freshwater dwellers.
The influence of these factors on other groups not
evaluated here, such as copepods (albeit not a
diverse/abundant group in the MRE; author’s
personal observations), may divulge additional
information.
Further, striking differences of richness
and abundance between the two rainy seasons were
observed. Since pluviometric rates were similar
on both rainy seasons, this suggests that other
factors also influenced the species. Higher values
of water temperature, NO3 and total phosphorous
and lower values of pH, salinity, NO2 and
Chlorophyll-a were observed during the second
rainy season.
Dependent variables
Predictors (contribution to total R²)
F
df
P
R²
4.96
−
2.79
3.02
4.9
−
3.74
−
1.86
−
3.64
2.63
5.48
−
5.38
−
4.82
3.7
2.58
3.12
2.54
4.67
7.62
4.49
3.24
3.29
12, 122
−
12, 122
12, 122
12, 122
−
12, 122
−
12, 122
−
12, 122
12, 122
12, 122
−
12, 77
−
12, 77
12, 77
12, 77
12, 77
12, 77
12, 77
12, 77
12, 77
12, 77
12, 77
<0.001
NS
<0.01
<0.001
<0.001
NS
<0.001
NS
<0.05
NS
<0.001
<0.01
<0.001
NS
<0.001
NS
<0.001
<0.001
<0.01
<0.01
<0.01
<0.001
<0.001
<0.001
<0.001
<0.001
0.3
−
0.2
0.2
0.3
−
0.3
−
0.2
−
0.3
0.2
0.4
−
0.5
−
0.4
0.4
0.3
0.3
0.3
0.4
0.5
0.4
0.3
0.3
S
T
pH
-0.2
0.4
Tr
O2
NH3 NO2 NO3
TP
Ch-a
Ph
P
0.29
0.4
0.3
-0.4
0.4
0.26
-0.2
0.2
0.27 0.25
0.2
0.3
0.25
0.4
0.3
0.4
0.22
0.32
-0.2 0.19
0.4
0.3
0.27
-0.4
0.3
0.25
0.3
-0.5
0.5
0.42
-0.4
-0.33
-0.3
-0.26
-0.3
0.3
0.3
0.2
0.2
-0.2 0.23
0.29
0.3
0.3
-0.3
0.29
DS: dry season; RS: rainy season; S: salinity; T: temperature; Tr: water transparency; O2: dissolved oxygen; NH3: ammonia; NO2: nitrite; NO3: nitrate; TP: total
phosphorous; Ch-a: Chlorophyll-a; Ph: Pheophytin; P: pluviometry; NS: non-significant.
A. M. A. SILVA ET AL.
Ceriodaphnia cornuta DS
Brachionus calyciflorus DS
Brachionus leydigi DS
Brachionus urceolaris DS
Brachionus plicatilis DS
Brachionus falcatus DS
Epiphanes macrourus DS
Filinia opoliensis DS
Hexarthra mira DS
Keratella tropica DS
Richness DS
Diversity DS
Abundance DS
Ceriodaphnia cornuta RS
Brachionus calyciflorus RS
Brachionus leydigi RS
Brachionus urceolaris RS
Brachionus plicatilis RS
Brachionus falcatus RS
Epiphanes macrourus RS
Filinia opoliensis RS
Hexarthra mira RS
Keratella tropica RS
Richness RS
DiveRSity RS
Abundance RS
Regression
234
Table I. Stepwise multiple regression analyses between zooplankton richness and abundance (dependent variables) and environmental variables
(predictors) during two seasons (dry and rainy) at the Mossoró River Estuary.
Zooplanktonn variation in a tropical inveerse estuary (N
Northeast Brazzil)
These obsservations confirm the
t
correlaations
observed inn the CCA, where
w
tempeerature, NO3 and
total phospphorous weree strong preedictors of most
species. The positive reelation betweeen zooplankkton,
water tempperature annd high cooncentrationss of
nutrients haas been deteected by maany authors (e.g.
Montú 19880, Nascim
mento-Vieira & Sant'-A
Anna
1989, Neum
mann-Leitãoo et al. 19992, Lopes 1996;
1
Breitburg ett al. 1999; Park
P
& Marshhall 1999). It is a
consensus that
t
an increease in the concentratioon of
2355
nutrrients influennces the topp levels of a food webb
through a cascaade of interaactions (e.g. Seip 1991,,
Forrrester et all. 1999, A
Anderson et al. 2002)..
Therrefore, zoopplankton inndividuals were
w
likelyy
beneefited by thiis increase dduring the second
s
rainyy
seasson in the preesent study. It is not cleaar, however,,
how
w the high vallues of Chlorrophyll-a du
uring the firstt
rainy
y season, which is an indicato
or of highh
phyttoplankton abundance, limited zooplanktonn
abun
ndance.
Figure 6. Orrdination bipllot of 19 zoopplankton speciies (points) an
nd 12 environnmental variabbles (arrows) sampled at 9
permanent sttations througghout a two-yeear period sam
mpling effort at the Mossorró River Estuaary. Cer cor: Ceriodaphniaa
cornuta; Braa cal: Brachioonus calyciflorrus; Bra ley: B. leydigi; Brra urc: B. urcceolaris; Bra pli: B. plicatiilis; Epi Mac::
Epiphanes macrourus;
m
Mooi min: Moinaa minuta; Braa fal: B. falcattus; Bra cau: B.
B caudatus; F
Fil opo: Filin
nia opoliensis;;
Hex mir: Hexxarthra mira; Ker tro: Keraatella tropica; Dia spi: Diap
aphanosoma sppinulosum; Brra pat: B. patu
ulus; Bra ang::
B. angularis;; Anu fis: Anuuraeopsis fissaa; Fil lon: F. longiseta;
l
Kerr val: Keratellla valga; Pol vvul: Polyarthrra vulgaris. S::
salinity; T: teemperature; Tr:
T water transsparency; O2: dissolved ox
xygen; NH3: ammonia;
a
NO2: nitrite; NO3: nitrate; TP::
total phosphoorous; Ch-a: Chlorophyll-a
C
a; Ph: Pheophyytin; P: pluvio
ometry.
Acccording to mean tottal phosphoorous
values, the estuary waas characterizzed as eutroophic
during the dry seasonss and hyperreutrophic duuring
the rainy seasons. Also,
A
accorrding to mean
m
Chlorophylll-a values, thhe estuary was
w characterrized
m
d
during
the drry seasons an
nd eutrophicc
as mesotrophic
during the rainy seasons (Carrlson 1977).
Two sppecies (Epipphanes maccrourus andd
Bracchionus plicaatilis) showeed positive relationships
r
s
with
h salinity. The
T latter sppecies has demonstrated
d
d
Pan-Americcan Journal off Aquatic Scieences (2009), 4(2):
4
226-2388
236
great
resistance
to
salinity
fluctuations
(Madhupratap 1986, Derry et al. 2003) and this may
have also been the case for E. macrourus. In
addition, the genus Brachionus, which is renowned
to tolerate polluted waters (Sampaio et al. 2002,
Dulic et al. 2006, Sousa et al. 2008), accounted for
80% of all individuals collected throughout the study
span, suggesting an ecological plasticity for the
species of this genus and further supporting the
notion that only tolerant species are able to survive
in highly dynamic environments. In extreme
conditions predation and competition pressures
could be reduced, and tolerant species may benefit
by residing at these areas (Madhupratap 1986,
Neumann-Leitão 1994, Herbst 2001).
Acknowledgements
We would like to thank the personnel of
LABESA (Laboratory of Semi-Arid Ecology) and
LEAq (Laboratory of Aquatic Ecology) for field and
lab assistance, the anonymous referees and D.
Calliari, whose comments were of great importance.
We are also indebted to CNPq and CAPES for
providing financial support.
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Received March 2009
Accepted May 2009
Larval fish assemblage in a tropical estuary in relation to tidal cycles,
day/night and seasonal variations
FABIANA TEIXEIRA BONECKER1,2, MÁRCIA SALUSTIANO DE CASTRO1,3 &
ANA CRISTINA TEIXEIRA BONECKER1,4
1
Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia , CCS, Bloco A, Ilha do
Fundão. 21941-590, Rio de Janeiro, Brasil. E-mail: 2 fabianabonecker@gmail.com, 3 mscastro@biologia.ufrj.br,
4
ana@biologia.ufrj.br
Abstract. The Mucuri River estuary is a salt wedge ecosystem located in Northeast Brazil with an
average depth of 4 m in the main channel and wide mangrove vegetation along its margins. This
study aimed to analyze the occurrence and abundance of larval fish in relation to seasonal,
day/night and tidal variations, and to verify the influence of temperature and salinity on this
assemblage. Sampling was conducted at a fixed station located in the entrance of the estuary at
every six hours along one tide cycle every three months from March 2002 to December 2004.
Oblique hauls were done using a bongo net. A total of 7,230 larval fish from 22 families and 33
species were identified. The highest number of taxa was recorded during the flood tide and night
sampling. The highest average densities occurred during the night sampling and in the rainy
period, except by 2004 when the highest mean value was recorded in the dry season at night. The
highest average densities and number of taxa obtained during flood tide suggested an important
contribution of the adjacent coastal zone on the composition of larval assemblage. Larval fish
assemblage did not change significantly between rainy and dry periods and it is also true for
day/night variation. Larval assemblage of the Mucuri River estuary was dominated by
Engraulidae, Gobiidae and Sciaenidae and was mainly influenced by tidal variation.
Keywords: Larval fish assemblage, seasonal variation, day/night variation, tidal variation, Mucuri
estuary, Brazil.
Resumo. Assembléia de larvas de peixes em um estuário tropical em relação aos ciclos de
marés e variações nictemerais e sazonais. O estuário do rio Mucuri é um ecossistema de cunha
salina localizado no nordeste do Brasil, apresentando profundidades médias de 4 m no canal
principal e vasta vegetação de mangue nas suas margens. Este estudo teve como objetivo analisar
a ocorrência e a abundância das larvas de peixes em relação às variações sazonais, nictemerais e
de maré e verificar a influência da temperatura e da salinidade sobre essa assembléia. As coletas
foram trimestrais, em uma estação fixa localizada na entrada do estuário, a cada 6 horas, ao longo
de um ciclo de maré, de março de 2002 a dezembro de 2004.Os arrastos oblíquos foram efetuados
com rede bongô. Foi identificado um total de 7.230 larvas de peixes, incluindo 22 famílias e 33
espécies. O maior número de táxons foi registrado durante a maré enchente, nas amostragens
noturnas. As maiores densidades médias ocorreram nas amostras noturnas na estação chuvosa,
com exceção do ano de 2004 quando a maior densidade média ocorreu na estação seca durante a
noite. As maiores densidades médias e número de táxons obtidas durante a maré enchente sugere
uma importante contribuição da zona costeira adjacente sobre a composição da assembléia de
larvas. A assembléia de larva de peixe não mudou significativamente entre o período chuvoso e o
seco e o mesmo foi observado para a variação dia/noite. A assembléia de larvas do estuário do rio
Mucuri foi dominada por Engraulidae, Gobiidae e Sciaenidae e foi principalmente influenciada
pela variação de maré.
Palavras-chave: Assembléia de larvas de peixes, variação sazonal, variação dia/noite, estuário do
rio Mucuri, Brasil.
F. T. BONECKER ET AL.
240
Introduction
Estuaries have ecological value and have
frequently been referred to as fish nursery areas
(Franco-Gordo et al. 2003, Berasategui et al. 2004)
and sustain many marine fish species mainly
represented by larvae and juveniles (DuffyAnderson et al. 2003, Castro et al. 2005).
Adults and larval fish occurrence and
distribution in an estuary vary according to
environmental changes like: precipitation regime,
estuary morphology that determines the intensity
and distance of the salt wedge inversion, tidal
dynamic, current velocity and the availability of
food resources (Camargo & Isaac 2003, Ré 2005).
Temperature
and
salinity
are
important
environmental factors influencing the occurrence,
density and growth of eggs and larval fish in
estuarine regions (Faria et al. 2006, Ramos et al.
2006a).
Larval fish assemblage can also be
seasonally influenced in an estuarine region (Harris
& Cyrus 2000) and seasonal variations have been
well documented (Morais & Morais 1994, BarlettaBergan et al. 2002, Ré 2005). However, most studies
developed along the Brazilian coast on estuarine
larval fish are limited to the north and south Brazil
and few works developed in the southeast region
(Barletta-Bergan et al. 2002, Joyeux et al. 2004).
The Mucuri River is a salt wedge estuary
with a semi-diurnal regime situated in the Northeast
of Brazil (18°06’02”S and 039°34’0”W). The rainy
season extends from November to April and the dry
period occurs from May to October (Castro &
Bonecker 1996). Although the Mucuri estuary serves
as repository for industrial waste, it is important for
the local population because of the subsistence
fishery activity. There is also a regionally important
artisanal fishery upon blue crabs (Schwamborn &
Bonecker 1996).
Previous studies in this ecosystem have
focused on the zooplankton community variation
(Aben-Athar & Bonecker 1996) and the
meroplankton distribution (Castro & Bonecker 1996,
Schwamborn & Bonecker 1996). However, neither
the relationship between larval fish assemblage and
environmental parameters, nor the short-term
temporal variations on larval fish density have been
studied. Therefore, this study analyzes the
occurrence and abundance of larval fish in the
Mucuri River estuary in relation to seasonal,
day/night and tidal variations and verifies the
influence of temperature and salinity on this
assemblage.
Material and methods
Sampling. Samples were collected at a
fixed point (18°05’45.7”S and 39°33’07.7W”) in the
mouth of Mucuri River estuary (Figure 1). Sampling
was performed at every three months, from March
2002 to December 2004, during the rainy (March
and December) and dry periods (June and
September). In each survey, sampling was
done at every six hours during the flood and ebb
tides.
Figure 1. Sampling station location (*) in Mucuri River estuary.
Larval fish assemblage in a Tropical estuary in relation to tidal cycles, day/night and seasonal variations
Ichthyoplankton was collected through
oblique hauls using a bongo net of 0.6 m diameter
and 2.5 m length with 330 and 500 µm mesh sizes.
Larval fish were more abundant and taxa number
were greater in samples collected with the 500 µm
mesh. Therefore, only samples obtained with this
mesh were used. A flowmeter (General Oceanics
Inc.) was used in order to quantify the volume of
water filtered. Samples were fixed in 4% buffered
seawater-formalin solution.
Temperature and salinity were measured at
the surface, mid-water and bottom using a
thermosalinometer (LabComp). Due to the shallow
depth and low data variation (CV%) the average
values of temperature and salinity were used.
Numerical density was expressed as the number of
specimens per 100 m3. Some yolk-sac and damaged
larvae could not be identified and were not
considered in the analysis. The larval fish list was
based on Nelson (2006).
Data analysis. Analysis of variance
(ANOVA) was applied to verify if the differences
among densities collected during the three years
were significant. Student t test was used to test
differences between samples collected during the
dry and wet seasons, day and night, and in flood and
ebb tides. In these analyses, the statistical program
Statistica 6.0 was used.
One-way analysis of similarity (ANOSIM)
and multidimensional scaling (MDS) were
performed based on a matrix of 45 samples and taxa
that occurred in more than five stations to determine
the significance of seasonality, day/night and tidal
cycle in the structure of the larval fish assemblage
(Clarke & Gorley 2001). Three samples were
excluded from the analyses because there were no
241
larval fish. Density data were transformed to
log(x+1) and the results were considered significant
at significance level <5%.
Similarity percentages analyses (SIMPER)
were used to identify taxon contribution to the factor
that influenced significantly the assemblage
formation. Species that accounted for more than
90% were considered key species. BIO-ENV, a
correlation analysis between abiotic and biotic data,
was employed using the Spearman correlation
coefficient. The biotic matrix was the same used to
ANOSIM and SIMPER and the abiotic matrix was
based on temperature and salinity data. These
analyses were done using the PRIMER 5.0 for
Windows program.
Results
Environmental conditions. Temperature
average values showed a similar pattern both in the
flood and ebb tides, during the day and night
sampling. During the flood tide water temperature
varied between 23.13oC and 28.90oC; while in the
ebb tide it ranged from 24.50oC to 29.70oC. The
highest values were recorded during the rainy season
and the lowest values occurred in the dry period.
Salinity average values varied greatly during
this study especially in ebb tides when most values
were lower than 20. During the flood tide salinity
ranged from 29.35 to 37.63 and in the ebb tide
varied between 0.13 and 27.90. The highest mean
salinity values were recorded in the flood tide, while
the lowest mean values were obtained during
ebb tide (Figure 2). Salinity varied also seasonally
and higher mean values were obtained during
the dry period, both in the ebb and flood tides
(Figure 2).
60
50
40
Salinity
30
20
10
0
-10
Mean
±SD
±1,96*SD
-20
Rainy Ebb
Dry Ebb
Rainy Flood
Dry Flood
Season and tide
Figure 2. Box and whisker diagrams of salinity (seasonality and tide analyses).
242
Larval fish assemblage: Taxonomic
composition and abundance. A total of 7,230
larval fish was identified along the study,
comprising 22 families and 33 species (Table I).
Engraulidae, Anchoa spinifer, Clupeidae,
Syngnathidae, Gerreidae, Sciaenidae, Stellifer
stellifer, Stellifer sp. and Gobiidae were recorded in
all samples (Table I). However, some species
occurred exclusively in one tidal or sampling period
(Table I). The greatest number of taxa (36) was
recorded during the nocturnal flood tide, while the
lowest number of taxa (18) was collected during the
diurnal ebb tide (Table I).
Engraulidae was most abundant in 2002 and
2004, and represented more than 40% of the total
catch. In 2003, Gobiidae dominated and contributed
with more than 30%. Sciaenidae was the third in
abundance (> 8 %) in the study period. Other
families that represented more than 1% in at least
one study year were Clupeidae, Pristigasteridae,
Syngnathidae, Gerreidae, Eleotridae and Achiridae.
ANOVA analysis showed no significant
differences among larval fish densities obtained
along the years (p = 0.5). Therefore, the other
analyses were done considering the three years
together. Average larval densities were significantly
greater in the nocturnal samples than in the diurnal
ones (p = 0.01) and during the flood tide (p << 0.05).
However, there was no significant difference
between dry and rainy season (p = 0.2) in relation to
larval densities.
Larval fish composition in relation to
seasonality, day/night and tidal cycles. The
ANOSIM analysis indicated that larval fish
assemblages during the rainy and dry seasons were
similar to one another (R = 0.032; p = 0.12), as were
during the day and night sampling (R = 0.009; p =
0.56). Significant differences on larval assemblage
were observed during the flood and ebb tides (R =
0.46; p = 0.001) and it was also revealed in MDS
plot (Figure 3).
During the flood tide Engraulidae was the
discriminating taxon representing 41% followed by
Gobiidae (20%) and Sciaenidae (15%); while in the
ebb there was greater contribution of Syngnathidae
(38%), Engraulidae (21%) and Sciaenidae (16%).
According to BIO-ENV analysis, changes on larval
fish assemblages were more correlated with salinity
than with temperature, as was expected since
assemblages in the Mucuri estuary were determined
by tide variation.
Discussion
The Mucuri River estuary is under a
seasonal regime typically tropical, which is defined
by two seasons: rainy (summer), when precipitation
is very frequent and intense; and dry period (winter)
when there is a critical decline of rain (Nimer 1989).
This pattern described in the literature was also
found during the present study. Unsurprisingly, the
salinity pattern varied in accordance to seasonality
being typical of tropical humid regions that are
influenced by precipitation and tide, as previously
reported for other tropical estuaries (Barletta et al.
2005, Castro et al. 2005).
The number of taxa recorded during this
study (45) was higher than the previous study
developed in the same ecosystem (24) (Castro &
Bonecker 1996). Other studies developed in
different estuaries showed a higher taxa number,
e.g. in Lima estuary (50) (Ramos et al. 2006b);
Caeté River estuary (63) (Bartella-Bergan et al.
2002); in the French Guiana (59) (Morais & Morais
1994). However, it is important to stress that
when one compares larval fish assemblages
of estuarine regions one should considerate
the methodology used, sampling effort, the
extension of water bodies and environmental
conditions (Barletta et al. 2005, Ramos et al.
2006b). The greater number of sampling stations
defined in other estuaries listed above and monthly
sampling contributed to increase the number of
taxa collected when compared with the present
study. Probably, the number of taxa would be higher
in Mucuri estuary if larvae were collected in
more than one station and if samples were taken
monthly. The majority of taxa recorded in this study
had already been cited to the Mucuri River estuary
(Castro & Bonecker 1996) except by the
Atherinopsidae (A. brasiliensis), Carangidae (C.
chysurus and Oligoplites sp.) and Haemulidae. Only
Ophichthidae (Myrophis punctatus) that had already
been recorded from this estuary (Castro & Bonecker
1996) was not collected in this study.
The larval fish assemblage of the Mucuri
estuary is composed by few species with high
abundance, like Engraulidae, Gobiidae and
Sciaenidae. According to Joyeux et al. (2004), larval
fish assemblages in Brazilian estuaries are structured
around Gobiidae, Sciaenidae and Engraulidae or
Clupeidae. Dominance of these species was also
recorded in different estuarine and coastal regions
(Grijalva-Chon et al. 1992, Bartella-Bergan et al.
2002, Castro et al. 2005, Faria et al. 2006).
According to the literature the dominance of
engraulids at lower latitudes is common while
clupeids are less abundant (Bartella-Bergan et al.
2002).
243
Table I. Total number and percentage of contribution of family and species of fish larvae collected in flood
and ebb tide, during day and night, along the study period in the Mucuri River estuary.
Flood
Ebb
Taxa
Day
%
Night
%
Day
%
Night
%
Elopidae
Elops sp.
Engraulidae
Anchoa spinifer
Achoviella lepidentostole
Clupeidae
Opisthonema oglinum
Pristigasteridae
Pellona harroweri
Ariidae
Mugilidae
Mugil curema
Atherinopsidae
Atherinella brasiliensis
Hemiramphidae
Hyporhamphus unifasciatus
Syngnathidae
Microphis brachyurus lineatus
Pseudophallus mindii
Syngnathus pelagicus
Scorpaenidae
Carangidae
Chloroscombrus chrysurus
Oligoplites sp.
Gerreidae
Diapterus sp.
Diapterus auratus
Diapterus rhombeus
Haemulidae
Sciaenidae
Cynoscion leiarchus
Macrodon ancylodon
Menticirrhus americanus
Micropogonias furnieri
Stellifer sp.
Stellifer rastrifer
Stellifer stellifer
Ephippidae
Chaetodipterus faber
Blenniidae
Parablennius pilicornis
Gobiidae
Eleotridae
Dormitator maculatus
Microdesmidae
Microdesmus carri
Achiridae
Achirus declives
Achirus lineatus
Trinectes microphthalmus
Trinectes paulistanus
Cynoglossidae
Symphurus plagusia
Tetraodontidae
Sphoeroides greeleyi
11
609
18
3
3
-
1.08
59.53
1.76
0.29
0.29
-
14
2492
225
21
-
0.24
42.84
3.87
0.36
-
43
1
1
22.40
0.52
0.52
3
53
1
3
1
1.49
26.37
0.50
1.49
0.50
1
0.10
63
3
1.09
0.05
2
2
1.04
1.04
1
-
0.50
-
-
-
4
0.07
-
-
2
1.00
-
-
2
0.03
-
-
-
-
2
1
0.20
0.10
1
11
1
1
-
0.02
0.19
0.02
0.02
-
98
2
-
51.04
1.04
-
3
32
2
-
1.49
15.92
1.49
1.00
-
3
49
46
1
67
1
3
0.29
4.79
4.50
0.10
6.55
0.10
0.29
1
4
274
7
1
4
2
161
5
1
25
106
116
241
0.02
0.07
4.71
0.12
0.02
0.07
0.03
2.77
0.09
0.02
0.43
1.82
1.99
4.14
1
2
1
1
11
6
0.52
1.04
0.52
0.52
5.73
3.13
12
1
19
1
2
19
5.97
0.50
9.45
0.50
1.00
9.45
2
0.20
1
59
0.10
5.77
1
1
1537
0.02
0.02
26.42
1
1
17
0.52
0.52
8.85
7
31
3.48
15.42
-
-
16
0.28
-
-
1
0.50
-
-
6
0.10
-
-
-
-
90
51
8.80
4.99
6
241
222
0.10
4.14
3.82
1
0.52
3
-
1.49
-
1
1
0.10
0.10
1
-
0.02
-
1
0.52
1
-
0.50
-
244
Stress: 0,17
Figure 3. MDS ordination showing differences between ebb and flood assemblages. Each individual point represents a
sample. Closed circles: flood; closed triangles: ebb.
According to Mc Lusky (1981) estuaries are
characterized by presence of few species that are
very abundant and many species rare, normality
originated from the adjacent coastal region. In this
study marine-estuarine species were dominants (A.
lepidentostole, P. harroweri, M. ancylodon, M.
americanus, C. leiarchus, M. furnieri, Stellifer
rastrifer, S. stellifer), but were also recorded
amphidromous species (Dormitator maculatus) and
freshwater-estuarine species (Microphis brachyurus
lineatus, Pseudophallus mindii).
Seasonality and day/night variations seem to
play an important role on larval fish abundance and
composition (Sanvicente-Añorve et al. 2000). Many
larval fish studies showed a tendency of higher
densities and taxa number to be recorded during the
hottest months (Ramos et al. 2006b, Faria et al.
2006, Aceves-Medina et al. 2008). Generally, larval
fish peaks are observed during nocturnal sampling in
opposition to lower densities found in diurnal
samples (Ramos et al. 2006b). This was also true for
the Mucuri estuary where larval fish densities were
significantly higher during the night comparing with
daylight sampling. Although, seasonality is an
important factor influencing larval fish, in the
present study larval fish density and composition did
not vary significantly between the rainy and dry
seasons. Different results were obtained by BarlettaBergan et al (2002) in the Caeté River estuary,
where the authors found significant differences in
density of the most abundant species in relation to
season. In Rio da Prata estuary was also observed
strong association between larval fish assemblage
distribution and salinity structure taken with
seasonality (Berasategui et al. 2004).
The significant difference observed in larval
density and composition between assemblages
collected in the flood and ebb tides along this study
stresses the importance of tidal cycles in the
maintenance of larval fish within the Mucuri
estuary. Aben-Athar & Bonecker (1996) attested that
tidal cycles with seasonal variations are the main
factors influencing plankton distribution in the
Mucuri River estuary. Previous studies developed in
the Mucuri River estuary observed higher larval
densities during flood tide (Castro & Bonecker
1996). In Australia the number of species collected
in the flood tide was six times higher than found
during the ebb (Neira & Potter 1992). On the other
hand, a study conducted at the Guanabara Bay
entrance showed that higher densities were obtained
during the ebb tide (Castro et al. 2005).
Low correlation between water temperature
and larval assemblage observed in this study is
probably associated with the tropical climate of this
region. According to Camargo & Isaac (2003), water
temperature in estuarine and coastal ecosystems
located in the north Brazil (tropical climate) does not
change greatly during the year, and is not the main
factor influencing adult fish distribution. Otherwise,
salinity changes along the year in tropical regions
and in this study had the greatest correlation with
larval fish assemblage. In Caeté estuary, situated in
the Brazilian north region, seasonal salinity
variations was the principal factor influencing the
fish assemblage structure (Barletta et al. 2005).
Changes in salinity probably also influenced the
dominance of Engraulidae during the flood tide and
of Syngnathidae in the ebb tide in the Mucuri River
estuary.
The results obtained in this study suggest
that larval assemblage in Mucuri River estuary is
mainly influenced by tidal variance. However,
further works considering sampling stations
distributed along the estuary and adjacent coast, as
discussed earlier, would give more information on
larval assemblage variability and confirm the
importance of this estuary as a nursery area.
Acknowledgments
The authors thank the team of Zooplankton
and Ichthyoplankton Integrated Laboratory of
Universidade Federal do Rio de Janeiro for sorting
the samples. We also thank CEPEMAR for
assistance in field surveys and for providing
environmental data. Thanks to Bahia Sul Celulose
for permission to publish these data. We thank M.
Macedo for the artwork in the map.
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Received December 2008
Accepted May 2009
Gametogenesis in the mangrove mussel Mytella guyanensis from
northern Brazil
CLEIDSON PAIVA GOMES1, COLIN ROBERT BEASLEY1*, SUELLEN MARIA OLIVEIRA
PEROTE1, ALINE SILVA FAVACHO2, CLAUDIA HELENA TAGLIARO3, MARIA
AUXILIADORA PANTOJA FERREIRA2 & ROSSINEIDE MARTINS ROCHA2
1
Laboratório de Moluscos, Universidade Federal do Pará, Campus de Bragança, Alameda Leandro Ribeiro s/n,
Bragança CEP 68.600-000, Pará, Brazil. *Email: beasley@ufpa.br
2
Laboratório de Ultraestrutura Celular, Departamento de Histologia e Embriologia, Centro de Ciências Biológicas,
Universidade Federal do Pará, Campus do Guamá, Belém CEP 66.075-900, Pará, Brazil
3
Laboratório de Conservação e Biologia Evolutiva, Universidade Federal do Pará, Campus de Bragança, Alameda
Leandro Ribeiro s/n, Bragança CEP 68.600-000, Pará, Brazil
Abstract. Gametogenesis was investigated using histological methods, in Mytella guyanensis from
the Caeté mangrove estuary, northern Brazil. The sexes could not be distinguished from
macroscopic observations of color. Histology and cellular organization was similar to that
previously described for this and other species.
Keywords: Mytilidae, reproduction, histology, tropical estuary
Resumo. Gametogênese no mexilhão do mangue Mytella guyanensis do norte do Brasil.
Gametogênese foi investigado usando métodos histológicos, em Mytella guyanensis no mangue do
estuário do rio Caeté, Norte do Brasil. Os sexos não podiam ser distinguidos pelas observações
macroscópicas da cor. A histologia e organização celular foi similar às que foram descritas
anteriormente para esta e outras espécies.
Palavras-chave: Mytilidae, reprodução, histologia, estuário tropical
Mytella guyanensis (Lamarck, 1819) is a
mangrove mussel with a wide distribution in Brazil
(Klappenbach 1965, Rios 1994) and has both
economic and ecological importance (Nishida &
Leonel 1995, Mora & Alpízar 1998, Pereira et al.
2003, Nishida et al. 2006, Pereira et al. 2007). M.
guyanensis is generally dioecious with a sex ratio of
1:1 (Cruz & Villalobos 1993, Carpes-Paternoster
2003) although Sibaja (1986), using both squash
preparations and macroscopic observations of gonad
color, reported sex-ratios biased towards females.
Hermaphrodites are rare, representing only 0.2% of
the
population
(Carpes-Paternoster
2003).
Information on reproductive activity in mussels is
important for their management (Narchi 1976;
Fernandes & Castro 1982) and culture (Marques
1987, Sibaja 1988, Rajagopal et al. 1998) and the
present study aims to describe gametogenetic
activity in Mytella guyanensis from northern Brazil.
The study area, near the Furo do Meio tidal
channel (00°52’14.6’’S, 46°38’57.7’’W), was
located in the Caeté mangrove estuary, along the
northeastern coast of the State of Pará. The mussel
bed (120 m2) occurs in typical fine muddy mangrove
sediment with aerial roots and is regularly flooded
during high tide as it borders a secondary channel
linked to the Furo do Meio. The mean density of the
bed was 6 mussels m-2, somewhat lower than that of
another bed in the same region (11.9 mussels m-2,
Beasley et al. 2005) but similar to the mean density
of M. guyanensis (5.2 mussels m-2) in Paraíba
(Nishida & Leonel 1995).
Between January 2004 and January 2005,
mussels were collected at low tide during the new
moon phase, to standardize the timing of sampling.
In order to obtain sexually mature individuals,
mussels with an anterior-posterior shell length of at
least 20 mm were selected. Mussels were obtained at
C. P. GOMES ET AL.
248
randomly chosen coordinates within the bed. An
initial sample size of 20 individuals was used in the
first two months of the study but from March 2004
onwards, the number of specimens collected was
reduced to 10 to minimize any possible impact of
sampling, such as trampling and/or a reduction in
population size due to the removal of individuals.
A pair of gonads occurs in the dorsal part of
the visceral mass from which ventrally ramified
tubules unite to eventually open into the mantle
cavity to release gametes into the sea water (Cox
1969, Gosling 2003). The gonads in mytilids
develop extensively into the mantle tissue and both
visceral mass and mantle tissue were sampled. The
color of both the gonad and mantle tissue was noted
for each individual. Both visceral mass and mantle
tissue were fixed in Davidson's solution for 24 h
before being stored in 70% alcohol. The material
was dehydrated using a series of alcohol
concentrations, cleared using xylol and embedded in
paraffin wax. Thin sections (5 μm) were obtained
using a microtome, which were subsequently stained
using Haematoxylin and Eosin and mounted on glass
slides for microscopic examination.
Qualitative evaluations of gametogenesis in
both the visceral mass and mantle tissue were
carried out using the criteria of Nascimento (1968)
for reproductive development in the closely related
Mytella falcata (M. charruana (d´Orbigny, 1842)).
Up to 5 consecutive developmental stages were
identified by Nascimento (1968): I (Immature), II
(Maturing), III (Pre-spawning), IV (Total or partial
spawning) and V (Recovery).
From the 150 individuals collected, 72 were
male and 77 female with a single hermaphrodite,
with mostly male reproductive tissue, found in
September. There was no significant difference in
2
the sex ratio during the study period ( χ =10.3,
d.f.=12, n.s.). Male reproductive tissue in the mantle
tended to be darker (light yellow to orange yellow)
than that of females (ivory to light yellow).
However, the degree of overlap in color precluded
conclusive determination of sex in 50% of cases by
macroscopic observation alone.
All individuals examined were sexually
mature and belonged to reproductive stages III to V;
there were no individuals at stages I and II.
Pre-spawning (Stage III) males were characterized
by long tubules with some immature cells close
to the tubule wall and greater numbers of darkly
stained mature spermatozoa in the lumen forming
dense groups of cells (Figure 1a). During spawning
(Stage IV) males are characterized by a reduction
in the number of spermatozoa and the presence
of small numbers of immature cells around the
tubule walls and residual spermatozoa in the lumen
(Figure 1b). In males, tubules in mantle tissue
were almost completely empty in contrast to tubules
in the visceral mass where residual spermatozoa
were common. During recovery (Stage V), the
tubules were packed with immature cells but also
contained lower numbers of spermatozoa (Figure
1c).
Pre-spawning (Stage III) females showed
well developed oval follicles containing a
large quantity of mature oocytes (round in shape
and free in the lumen). Some oocytes were still
attached to the follicle wall by a stalk (Figure 1d).
Spawning (Stage IV) females were characterized
by poorly developed follicles without a definite
shape and containing occasional mature oocytes.
Some degenerating oocytes that had not been
released during spawning were also present
(Figure 1e). In females, follicles were completely
empty in the visceral mass but not in the mantle
tissue. Recovering (Stage V) females contained
many immature oocytes close to the follicle
wall (Figure 1f) but these did not have the oval
shape characteristic of the pre-spawning stage.
The sexes in Mytella guyanensis could not
be accurately distinguished through macroscopic
observation due to wide variation in the colour of the
reproductive tissues, which were darker in males and
lighter in females. This contrasts with other mytilids
where the gonads are usually lighter in colour in
males and darker in females (Nascimento 1968,
Arrieche et al. 2002, Gosling 2003). However, our
results agree with those of Cruz & Villalobos (1993)
whose macroscopic description of gonad colour in
M. guyanensis from Costa Rica varies from light to
dark yellow in females and from light to dark brown
in males.
The histology and cellular organization of
the reproductive tissues of Mytella guyanensis is
similar to what has been previously reported for this
species (Cruz & Villalobos 1993, Carpes-Paternoster
2003), for the closely related Mytella falcata
(Nascimento 1968), and, for other bivalves in
general (Gosling 2003). Mean oocyte size of M.
guyanensis ranged from 26 to 42 µm (maximum
individual observation was 62 µm) in northern
Brazil, similar to the 30-45 µm range described for a
population in Costa Rica (Sibaja 1986). By
comparison, maximum oocyte size is 63.3 µm in M.
falcata (Nascimento 1968) and 70 µm in Mytilus
edulis (Gosling 2003).
Gametogenesis in the mangrove mussel Mytella guyanensis from northern Brazil
249
Figure 1. Photo-microscopy of thin sections of reproductive tissue from male and female Mytella guyanensis. (a) Male,
Stage III, pre-spawning, (b) male, Stage IV, spawning and (c) male, Stage V, recovery. (d) Female, Stage III, prespawning, (e) female, Stage IV, spawning and (f) female, Stage V, recovery. Sp Spermatozoa, Im Immature cells, F
Follicle, Oc 1 primary oocytes, Oc 2 secondary oocytes. Bar is 100 µm.
Acknowledgments
CPG, SMOP were supported by scholarships
from the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq). We also thank the
Secretaria Executiva de Ciência, Tecnologia e Meio
Ambiente, Pará State and Banco da Amazônia, S. A.
for financial support. This study was carried out as
part of the Mangrove Dynamics and Management
(MADAM) Project, a joint German-Brazilian
cooperative scientific program.
References
Arrieche, D., Licet, B., Garcia, N., Lodeiros, C. &
Prieto, A. 2002. Condition index, gonadic
index and yield of the brown mussel Perna
perna (Bivalvia: Mytilidae) from the Morro
de Guarapo, Venezuela. Interciencia, 27:
613-619.
Beasley, C. R., Gomes, C. P., Fernandes, C. M.,
Brito, B. A., Santos, S. M. L. & Tagliaro, C.
H. 2005. Molluscan diversity and abundance
among coastal habitats of northern Brazil.
Ecotropica, 11: 9-20.
Carpes-Paternoster, S. 2003. Ciclo reprodutivo do
marisco-do-mangue
Mytella
guyanensis
(Lamarck, 1819) no manguezal do Rio
Tavares-Ilha de Santa Catarina/SC. M.Sc.
Dissertation. Universidade Federal de Santa
Catarina, Florianópolis, Brazil, 30 p.
Cox, L. R. 1969. General features of Bivalvia. Pp. 2129. In: Moore, R. C. (Eds.). Treatise on
invertebrate paleontology. Part N Mollusca
C. P. GOMES ET AL.
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6 Bivalvia. Geological Society of America,
University of Kansas, Lawrence, Kansas, 489
p.
Cruz, R. A. & Villalobos, C. R. 1993. Shell length at
sexual maturity and spawning cycle of
Mytella guyanensis (Bivalvia: Mytilidae) from
Costa Rica. Revista de Biologia Tropical,
41: 89-92.
Fernandes, L. M. B. & Castro, A. C. 1982.
Caracterização ambiental e prospecção
pesqueira do estuário do rio Cururuca (MA).
Estudos de moluscos, crustáceos e peixes.
Atlântica, 5: 44.
Gosling, E. 2003. Bivalve molluscs. Biology,
ecology and culture. Blackwell Science,
Oxford, 431 p.
Klappenbach, M. A. 1965. Lista preliminar de los
Mytilidae brasileños con claves para su
determinación y notas sobre su distribución.
Anais da Academia Brasileira de Ciências,
37: 327-352.
Marques, H. L. A. 1987. Estudo preliminar sobre a
época de captação de jovens de mexilhão
Perna perna (Linnaeus, 1758) em coletores
artificiais na região de Ubatuba, Estado de
São Paulo, Brasil. Boletim do Instituto de
Pesca, 14: 25-34.
Mora, D. A. & Alpízar, B. M. 1998. Crecimiento de
Mytella guyanensis (Bivalvia: Mytilidae) en
balsas flotantes Revista de Biologia
Tropical, 46: 21-26.
Narchi, W. 1976. Importância do conhecimento dos
ciclos gametogênicos de bivalves comestíveis.
Anais da Academia Brasileira de Ciências,
47: 133-134.
Nascimento, I. 1968. Estudo preliminar da
maturidade do sururu (Mytella falcata,
Orbigny, 1846). Boletim de Estudos de
Pesca, 8: 17-33.
Nishida, A. K. & Leonel, R. M. V. 1995.
Occurrence, population dynamics and habitat
characterization of Mytella guyanensis
(Lamarck, 1819) (Mollusca, Bivalvia) in the
Paraíba do Norte river estuary. Boletim do
Instituto de Oceanografia, 43: 41-49.
Nishida, A., Nordi, N. & da Nóbrega-Alves, R.
2006. Mollusc gathering in northeast Brazil:
an ethnological approach. Human Ecology,
34: 133-144.
Pereira, O., Hilberath, R., Ansarah, P. & Galvão, M.
2003. Estimativa da produção de Mytella
falcata e de M. guyanensis em bancos naturais
do estuário de Ilha Comprida, SP, Brasil.
Boletim do Instituto de Pesca, São Paulo,
29: 139-149.
Pereira, O. M., Galvão, M. S. N., Pimentel, C. M.,
Henriques, M. B. & Machado, I. C. 2007.
Distribuição dos bancos naturais e estimativa
de estoque do gênero Mytella no estuário
de Cananéia, SP, Brasil. Brazilian Journal
of Aquatic Science and Technology, 11: 2129.
Rajagopal, S., Venugopalan, V. P., Nair, K. V. K.,
van de Velde, G., Jenner, H. A. & den Hartog,
C. 1998. Reproduction, growth rate and
culture potential of the green mussel, Perna
viridis (L.) in Edaiyur backwaters, east coast
of India. Aquaculture, 162: 187-202.
Rios, E. 1994. Seashells of Brazil. Editora da
Fundação Universidade do Rio Grande, Rio
Grande, 368 p.
Sibaja, W. 1986. Madurez sexual em el mejillón
chora Mytella guyanensis Lamark, 1819
(Bivalvia: Mytilidae) del manglar en Jicaral,
Puntarenas, Costa Rica. Revista de Biologia
Tropical, 34: 151-155.
Sibaja, W. G. 1988. Fijación larval y crecimiento del
mejillón Mytella guyanensis L. (Bivalvia:
Mytilidae) en Isla Chira, Costa Rica. Revista
de Biologia Tropical, 36: 453-456.
Accepted May 2009
Diffusion material only – Do not cite
Original Scientific Photographs
BY PRANAV J.PANDYA & KAURESH D.VACHHRAJANI
Division of Environment and Toxicology, Department of Zoology, The M. S. University of Baroda, Vadodara – 390002,
Gujarat, India. Email: pranavpandya1@yahoo.com
The Decapoda crab Matuta planipes (Fabricius, 1798) is usually found in marine reaches as well as mouth of estuaries.
It belongs to family Calappidae. It is distributed from Southeast Asia to Australia and westward to India. This crab is
known and reported as predator of flounder fishes. Mostly found in sandy zones and showed typical predatory behavior.
On 27th July 2008 we observed adult M. planipes (Carapace width = 8 cm including lateral spines) predating on other
crab Macrophthalmsus dilatatus (Lancheser, 1900), on the intertidal reach of Mahi river estuary (22º12’52.38” N 72º37’17.89” E), Gujarat, India. The crab partially buries itself under the sandy substrata and predates on the other
inhabitant M. dilatatus abundant in sandy zone. Also, observation and sampling of the area from 2006 to 2008
illustrated that both the predator and prey species were specific in substratum preference and habitat utility (90 -94%
sand and 6-10% silt-clay). Picture characteristics: Canon PowerShot S70; Resolution of 4 megapixels; autofocus;
automatic regulation; Image cropped.
References
Ng, P. K. L., Guinot D. and Davie P. J. F., 2008. Systema Brachyurorum: Part 1: An annotated checklist of extant
brachyuran crabs of the world. The Raffles Bulletin of Zoology., 17: 1-286.
Hossain, M. A. R and Tanaka, M. 2002. Predator-prey interaction between hatchery-reared Japanese flounder juvenile,
Paralichthys olivaceus and sandy shore crab, Matuta lunaris: daily rhythms, anti-predator conditioning and
starvation. J. Exp. Mar. Biol. And Ecol. 26: 1-14.
Fatima, M. 2003. Length weight study of two species of crabs Matuta planipes and Matuta lunaris from Karachi,
Pakistan. Pakistan Journal of Biological Science, 6(4):397-398.
This picture may be used for academic or personal purposes but always accompanied by the author's information
(copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire
about reprints, fees, and licensing, please contact the author via e-mail.
Pan-American Journal of Aquatic Sciences (2009), 4(2): I
Diffusion material only – Do not cite
Original Scientific Photographs
*
BY SIMONE MARIA DE ALBUQUERQUE LIRA , FERNANDA MARIA DUARTE DO AMARAL
& CRISTIANE MARIA ROCHA FARRAPEIRA
Universidade Federal Rural de Pernambuco, Departamento de Biologia, 52.171-900. Recife - PE, Brasil. *Email:
simonealira@gmail.com
A
B
A numerous population of the white sea-urchin Tripneustes ventricosus (Lamarck, 1816) was recorded on long
extensions of the Atalaia Beach, Fernando de Noronha Archipelago, Brazil (3º49’S e 32º24W). The area is home to a
reef environment dominated by this sea-urchin, as shown in pictures A and B made in February 2009 at 3 p.m. local
time. The species is distributed throughout the occidental and oriental Atlantic Ocean and was first recorded for the
archipelago in 1962 (Brito 1962). It was later classified as rare by a study on reef zonation carried out in 1986 (Eston et
al. 1986). Atalaia Beach is part of the Fernando de Noronha National Marine Park and its reef environments suffer from
the impacts caused by the Echinodermata. Sea-urchins are commonly recorded competing for space and food in reef
ecosystems (Hughes 1989, Done 1995). Such competition conspicuously impacts these environments, which includes
the loss of special characteristics of the reef, such as decreasing zones of reefbuilding corals (scleractinians) in a process
known as non-reefbuilding (Done 1995, Done et al. 1996). Considering the area's low insular diversity (Eston et al.
1986, Simberloff 2000), the increasing presence of these organisms may cause local biodiversity to diminish even more
due to interspecific competition. Picture characteristics: Cyber-shot DSC-W90 digital camera; 8.1 megapixels (300 dpi);
2.8 diaphragm opening; 1/40 exposure.
References
Brito, I. M. 1962. Ensaio de catálogo dos equinodermas do Brasil. Faculdade Nacional de Filosofia, Centro de Estudos
Zoológicos, Rio de Janeiro, 13:1-10.
Done, T. J. 1995. Remediation of degraded coral reefs: the need for broad focus. Marine Pollution Bulletin 30: 686-688.
Done, T. J., Ogden, J. C., Wiebe, W. J. & Rosen, B. R. 1996. Biodiversity and ecosystem function of coral reefs. pp. 393-429.
In: Heywood, V. H. (ed) Global biodiversity assessment. Cambridge University Press for United Nations
Environment Programme. 1152 p.
Eston, V. R., Migotto, A. E., Oliveira Filho, E. C., Rodrigues, S. A. & Freitas, J. C. 1986. Vertical distribution of benthic
marine organisms on rocky coasts of the Fernando de Noronha Archipelago (Brazil). Boletim do Instituto
Oceanográfico 34: 37-53.
Hughes, T. P. 1989. Community structure and diversity of coral reefs: the role of history. Ecology 70:275–279.
Simberloff, D. 2000. Extinction-proneness of island species- causes and management implications. The Raffles Bulletin of
Zoology, Singapore, 48 (1): 1-19.
This picture may be used for academic or personal purposes but always accompanied by the author's information
(copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire
about reprints, fees, and licensing, please contact the author via e-mail.
Pan-American Journal of Aquatic Sciences (2009), 4(2): II

PAN-AMERICAN JOURNAL OF AQUATIC SCIENCES

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