Catalogue of algae with high growth rates and energy potential

Transcription

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Produced by:
National Environmental Research Institute (NERI), Aarhus University, Denmark (WP leader)
Central Salt & Marine Chemicals Research Institute (CSMCRI), India (WP leader)
National Interuniversity Consortium for Ocean Sciences (CoNISMa), Italy
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Catalogue of algae species with high growth rates and energy potential
Deliverable 2.1. WP2.
List of contents:
Algae species of interest for BioWalk4Biofuels..................................................................................4
Growth rate ..........................................................................................................................................4
Ulva sp. ................................................................................................................................................6
General description ......................................................................................................................6
Lifecycle.......................................................................................................................................6
Distribution ..................................................................................................................................7
Growth rate ..................................................................................................................................8
Uptake of nutrients and CO2 ........................................................................................................9
Cultivation..................................................................................................................................10
Protoplast technology.................................................................................................................10
Biogas production ......................................................................................................................11
Pros and cons for selecting Ulva for cultivation in Augusta plant.............................................12
Chaetomorpha sp. ..............................................................................................................................13
General description ....................................................................................................................13
Distribution ................................................................................................................................13
Lifecycle.....................................................................................................................................13
Growth and production ..............................................................................................................14
Uptake of nutrients and CO2 ......................................................................................................14
Cultivation..................................................................................................................................14
Pros and cons for selecting Chaetomorpha for cultivation in Augusta plant ............................15
Gracilaria sp. .....................................................................................................................................16
General description ....................................................................................................................16
Lifecycle.....................................................................................................................................16
Distribution ................................................................................................................................17
Growth and production ..............................................................................................................18
Uptake of nutrients and CO2 ......................................................................................................18
Cultivation..................................................................................................................................18
Pros and cons for selecting Gracilaria for cultivation in Augusta plant ...................................20
Literature............................................................................................................................................23
Appendix 1. Note on Caulerpa (CMSCRI)........................................................................................35
Appendix 2. Algae from Augusta Bay (CoNISMA)..........................................................................35
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Algae species of interest for BioWalk4Biofuels
The species described in this catalogue are species suitable for the specific cultivation required in
the cultivation facility at Augusta, Sicily.
The aim of the BioWalk4Biofuel project is to use cultivation of algae to treat and clean biowaste
streams, yielding a biomass usable for energy production in the form of biogas. The algae species
selected for cultivation in the facility needs to fulfil the following criteria:
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Fast growth in order to achieve a high biomass production and efficient waste removal
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Capability to grow on biowaste sources such as flue gas and nitrogen rich wastewater
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Efficient uptake and assimilation of the CO2 and nutrients in the waste streams
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Fairly easy to keep in cultivation
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Efficiently harvestable
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Suitable for biogas production
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Domestic species in Sicilian waters. No invasive species can be introduced at the risk of the
surrounding marine environment.
At the kick-off meeting in Rome (09.04.2010) the WP2 partners agreed on focusing on the
following fast growing species, primarily belonging to the green algae:
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Ulva sp. (chlorophyceae) including the former Enteromorpha sp. (chlorophyceae)*
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Chaetomorpha sp. (chlorophyceae)
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Gracilaria sp. (rhodophyta)
•
Caulerpa sp. (chlorophyceae)
* On the basis of genetic analyses, the genus Enteromorpha has been merged with the Ulva (Hayden et al. 2003) .
The species Caulerpa has since been omitted as subject for cultivation on the basis of its status of
invasive species in the Mediterranean area (Appendix 1. (Note on Caulerpa by CSMCRI).
This catalogue therefore primarily concerns the remaining four species.
Growth rate
Growth rates of algae depend on the environmental conditions such as nutrient concentrations, light
availability, temperature and water turbulence. Many green algae are opportunistic fast growing
species, proliferating at high nutrient concentrations and relatively high incoming light. Certain
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species can under optimal conditions grow into massive populations, so-called “green tides”. This
phenomenon is observed along many coast lines in particular in Europe, South America and China.
Documented growth rates vary not only between species, but also within the species, and growth
rates obtained under optimal conditions in laboratory scale are most likely difficult to achieve in
larger scale experiments or cultivation systems.
In the following growth rates, production potential, nutrient removal capacity, biogas production
potential as well as considerations for cultivation and harvest are described for species within the
three selected genera.
At the end of the report, various data – from own experiments as well as from the existing literature
– are compiled in a table (Table 2) as well as data on biochemical composition of a number of
species is investigated by CSMCRI is included (Table 3).
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Ulva sp.
Chlorophyceae, Ulvaceae.
General description
Ulva sp. is a genus of marine and brackish water green algae. It is edible and often called 'Sea
Lettuce'. Distinction of species of Ulva have traditionally been based on morphological, anatomical
and cytological characteristics such as shape, size, presence or absence of dentation, thickness, cell
dimensions and number of pyrenoids. Many studies have shown that these characteristics can be
highly variable within species, varying with age, reproductive state, wave exposure, tidal factors,
temperature, salinity, light and biological factors such as grazing. In recent years developmental
patterns in culture, reproductive details and the apparent inability of species to interbreed have been
used to evaluate species concepts based on morphological and anatomical characteristics.
Species with hollow, one-layered thalli were formerly included in Enteromorpha, but it is widely
accepted now that such species should be included in Ulva. The thallus of ulvoid species is flat and
blade-like and is composed of two layers of cells. There is no differentiation into tissues; all the
cells of the plant are more or less alike except for the basal cells, which are elongated to form
attachment rhizoids. Each cell contains one nucleus and has a cup-shaped chloroplast with a single
pyrenoid (www.AlgaeBase.org).
Lifecycle
Ulva undergoes a very definite alternation of generations (Figure 1). Biflagellate isogametes are
formed by certain cells of the haploid, gametangial plant. These are liberated and fuse in pairs to
form a diploid zygote which germinates to form a separate diploid plant called the sporophyte; this
resembles the haploid gametangial plant in outward appearance. Certain cells of the sporophyte
undergo meiosis and form zoospores in sporangia; these zoospores are quite different to the gametes
in that they form quadriflagellate zoospores (with 4 flagella). The zoospores are released, swim
around for a time, settle and germinate to form the haploid gametangial thallus. Note that the
haploid gametes are capable of settling and germinating without fusion to form a haploid thallus
directly. Most Ulva populations reproduce by this form of parthenogenesis and sexual reproduction
is not very common.
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In mass cultures of Ulva, sporulation may occur in response to seasonal environmental cues and
reduce the biomass of vegetative thalli by more than half within a few days. It has been attempted to
prevent the uncontrolled mass sporulation by applying “artificial moon-shine” in order to break the
hypothesised semi-lunar sporulation system of Ulva (EU-project SEAPURA report
(www.cbm.ulpgc.es/seapura/SeapuraAnnRepY2PartA.pdf). However, this attempt was not
successful (Lüning et al. 2008). Recently, a swarming inhibitor (SWI) excreted by the algae, was
isolated and described in two of Ulva species (U. lactuca and U. mutabilis) (Wichard and Oertel
2010).
Fig 1. Lifecycle of Ulva
Distribution
Ulva has a cosmopolitan distribution in salt and brackish waters. It is known to form dense mass
populations in shallow nutrient rich areas (green tides), and cause local nuisance, when washed up
and decaying on the beaches. The green tides are described since the 1970’s in Europe and South
America. The washed up material has been attempted to use for compost, ie. (Wosnitza and
Barrantes 2006) as well as biogas, ie. (Charlier et al. 2007). In recent years, reports of massive
green tides are described along the Chinese coast line, particularly in the Qingdao region. The green
tides are caused by nutrient effluents from sewage, agri- and aquaculture.
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Growth rate
Regarding the growth rates of Ulva there are numerous studies from nature as well as from
cultivation experiments on different size scales. The general picture of Ulva species is that they
have relatively high growth rates compared to other algae, in nature as well as in cultivation
facilities. In nature, growth rates of up to 35% have been reported for the Ulva type species
(holotype) U. lactuca (Pedersen and Borum 1996). In the Mediterranean relatively low growth rates
of U. rigida, <10% d-1, are reported from eutrophicated sites (de Casabianca et al. 2002). In
laboratory scale high growth rates have been achieved with several Ulva species i.e.: U. curvata
(Kützing) De Toni, 52% wet wt.day−1 in short-term laboratory studies (Duke et al. 1989a; Duke et
al. 1989b), U. fasciata Delile, 36% wet wt.day−1 (Lapointe and Tenore 1981). Within this project,
experiments for determining the growth rates of selected species of Ulva have been carried out by
CMSCRI (Figure 2): The RGR was 30.2±1.13% for Ulva reticulata, 25.3±0.14% for U. taeniata,
19.6 ± 1.06% for U. fasciata, 25.85±2.31% for U. lactuca and 17.75±1.16% for Monostroma.
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RGR (%d-1)
30
25
20
15
10
5
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Figure 2. Results from growth measurements CMSCRI (Relative growth rates ±SD, n=3).
Robertson-Andersson (2003), showed that there is a decrease in standard growth rate (SGR) when
scaling up tank sizes (Bolton et al. 2009), which is reflected i.e. in the following studies: Pilot scale
cultivation growth rates of up to18.7% d-1 and 9.2 % d-1 are reported for biomass densities of 1 and
4 kg’s, respectively (U. lactuca) (Bruhn et al. 2011). Growth rates for U. fenestrata Postels et
Ruprecht under experimental conditions were 16% wet wt.day−1 (Bjornsater and Wheeler 1990).
This is lower than those obtained for U. lactuca, 18.6% wet wt.day−1 (Neori et al. 1991). In a large
scale cultivation experiment in Japan growth rates of up to 55% d-1 were reported for U. prolifera
cultivated in 500 l tanks with supply of nutrient rich deep sea water. This cultivation method was
based on production of “germling clusters” (Hiraoka and Oka 2008).
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Uptake of nutrients and CO2
There are a number of studies treating the uptake of nutrients of Ulva in nature as well as in
cultivation in connection to integrated multitrophic aquaculture (IMTA) or waste water treatment.
The N removal efficiency of Ulva in co-cultivation with fin fish under different TAN loads (NH3 +
NH4) proved highest under high or medium TAN loads as compared to low or very high loads (up
to 65%), whereas the areal uptake of N was highest under very high TAN loads (up to 7.4 g N m-2
d-1) (Msuya and Neori 2008). Uptake rates of NH4 of 50-390 µmol h-1 g DW-1 are reported (Neori et
al. 1991). In co-cultivation with abalone, Ulva was removing on average 80.8% (between 24.3%
and 99.5%) of the NH4 in the effluent water. However, the NH4 concentrations were relatively low
(<34 µM) (Bolton et al. 2009). In Greece on the island of Ios, experiments using Ulva to remove
phosphate from waste water achieved an average efficiency of 35% phosphate removal with an
average concentration of 100µM P. The algae would take up 2.13 µmol PO43− g−1 DW h−1 in the
day time, with a significantly lower uptake during night (Tsagkamilis et al. 2010). NERI has
initiated experiments with cultivation of U. lactuca on fresh, as well as degassed, liquid pig manure.
The manure was diluted to approximately 300µM NH4 (300-400 times dilution) and both types of
manure supported as high growth rates as inorganic N in the form of NO3 and even higher than NH4
(average of 30-35 % g FW d-1) (Nielsen, et al. in prep).
Generally, there is a co-limitation of growth by light and N, meaning that in order to utilise high N
concentrations and achieve high growth rates, incoming irradiance must be high (Lapointe and
Tenore 1981). Surge uptake of NH4 is reported for many macroalgae including Ulva (Pedersen and
Borum 1997). Thus, addition of NH4 in pulses can give macroalgae an advantage in competition
with fouling microalgae, as well as potentially lowering the evaporisation of NH4.
Various species of Ulva are reported to be able to utilise carbon (C) in the form of CO2 as well as in
the form of HCO3- (Gao and Mckinley 1994). Regarding pH, dissolved inorganic carbon (DIC) and
CO2, the growth rate of Ulva is documented to decline at pH values above 7.5-8 (Frost-Christensen
and Sand-Jensen 1990), and at pH values below 7 (NERI, unpublished). Cultivation of U. lactuca
using flue gas as source of DIC has been carried out by NERI, documenting the capability of Ulva
to utilise the CO2 from the flue gas as C source and increasing growth rates by up to 21% as
compared to aeration with atmospheric air. Addition of flue gas was controlled by the pH of the
growth media, keeping the pH in the range of 7.5 (Bruhn, et al. in prep). This increase in growth
rate by flue gas addition is also demonstrated in one red algae (Gracilaria cornea) and one green
microalgae (Chlorella vulgaris) (Douskova et al. 2009; Israel et al. 2005).
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Cultivation
Ulva has been cultivated successfully for biomass production in connection to aquaculture and
bioenergy purposes (Bruhn et al. 2011; Msuya and Neori 2008; Robertson-Andersson et al. 2008;
Ryther et al. 1984). Several cultivation methods are tested and described ranging from different size
ponds to different size raceways. Also non energy intensive cultivation forms have been tested
(Ryther et al. 1984). Production rates ranging from 74 T DW ha-1 y-1 (18.8 g DW m-2 d-1) for energy
intensive systems to 25 T DW ha-1 y-1 (6.8 g DW m-2 d-1) in non-energy intensive systems are
reported (Ryther et al. 1984). Similar areal yields, and even higher, have been attained in South
Africa in IMTA of U. lactuca and abalone (19.71-26.1 g DW m-2 d-1). Ulva was here cultivated in
raceways (Bolton et al. 2009). In IMTA with fin fish biomass yields of up to 376 g FW m-2 d-1 is
reported from Israel (Msuya and Neori 2008). Annual yields of 45 T DW ha-1 y-1 (up to 38.8 g DW
m-2 d-1) are described for locations as far north as Denmark (Bruhn et al. 2011).
Yields are directly correlated to incoming light with higher irradiance supporting a higher areal
biomass density (Bruhn et al. 2011).
Protoplast technology
There are numerous species within the Ulva genus that have been proven successful for protoplast
propagation as well as for genetic engineering (for review see Reddy et al, 2008). Enzyme based
methods for producing a large number of viable protoplasts has been developed for several Ulva
species and Ulva has successfully been seeded from protoplast cultures onto cultivation nets and
ropes (CSMCRI, unpublished). An alternative cultivation strategy based on cultivation of germling
clusters has been proven successful using the species U. fasciata (Figure 3) (Hiraoka and Oka
2008).
Table 1. Yield of viable protoplasts from various Ulva species (CSMCRI, unpublished).
Species
U. beytensis
U. fasciata
U. lactuca
U. linza
U. ovata
U. reticulata
U. taeniata
Protoplasts yield
(cells /g fresh wt.)
2.47 ± 1.6 ×106
1.85 ± 0.62× 106
4.0 ± 0.45× 108
3.75 ± 1.45 ×106
1.2 ± 1.20 ×105
1.4 ± 0.7× 107
1.4 ± 0.78 ×107
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Fig 3. Illustration of the germling cluster resporduction method used by Hiraoka & Oka (2007) to cultivate U. fasciata
on deep sea water in large landbased tanks (500 l).
Biogas production
Ulva is regarded as a reasonable source of methane (Briand and Morand 1997). Methane yields in
the range of up to 330 m3 T VS-1 are reported (Briand and Morand 1997; Bruhn et al. 2011;
Chynoweth 2002; Habig et al. 1984b) and are documented to depend on the nitrogen content of the
biomass, with highest methane yields from N-deficient biomass (Habig et al. 1984b). This is
equivalent to the yield from cattle manure and land based energy crops, such as grass-clover.
However, the high sulphur content of the sulphated polysaccharides in Ulva (Lahaye and Robic
2007; Robic et al. 2009) may inhibit the methanisation process since the methanogenic
microorganisms are sensitive to the H2S evolved in the first stages of the decay of the Ulva biomass.
Thus, the theoretical biogas yield of Ulva is thought to be higher than what is yet demonstrated.
Direct combustion of U. lactuca biomass is problematic due to a high ash content and a high
content of alkali metals in the ash (Bruhn et al. 2011). This problem is the same for other species of
algae (Ross et al. 2008).
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Pros and cons for selecting Ulva for cultivation in Augusta plant
Positive
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High growth rates in general
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High N removal capacity
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Increase of growth rates by addition of flue gas documented (NERI, in prep)
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High growth rates by addition of manure documented (NERI, in prep)
•
Native species present in Augusta, Sicily (documented by Algaebase and CoNISMA)
•
Vast documentation and experience in cultivation of this genus for biomass production as
well as bioremediation of nutrient rich aquaculture effluent
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Progress in protoplast isolation and regeneration is successful at a very high level
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Good substrate for biogas production
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No reports of major biofouling competition
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High adaptability to varying environmental conditions
Negative
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Sporulation and mass disintegration reported
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Chaetomorpha sp.
Chlorophyceae, Chladophoraceae.
General description
Chaetomorpha sp is also called spaghetti algae. It is build of thin, yet robust, filaments that are
uniseriate and unbranched. The alga is either erect and attached with an elongate, thick-walled,
basal cell, or loose-lying without basal cells. Growth is diffuse or generalized, producing cylindrical
to barrel-shaped to rarely oval cells 20-5000 um in diameter, generally consistent within species.
Cells are as wide as long or up to ten times as long as wide. Chloroplasts are parietal and reticulate,
composed of many segments and generally covering the entire outer surface of the protoplast, with
numerous pyrenoids. Cells are multinucleate with ca. 10 to 1000 nuclei per cell. Nuclear number is
related to cell size. Chaetomorpha is not clearly delimited from Rhizoclonium, although the latter
usually has smaller cells with fewer nuclei, and commonly forms rhizoidal branches.
(www.AlgaeBase.org).
Distribution
Chaetomorpha has a cosmopolitan distribution in shallow marine and brackish waters, where it
commonly forms extensive mats of intertwining filaments. It is common intertidally either as
scattered individuals or as clumps of filaments on exposed rock or in pools, often as understory
species beneath other algae. Some species are commonly found as unattached filaments entangled
with other algae.
Lifecycle
Asexual reproduction by fragmentation of filaments or by quadriflagellate zoospores produced in
large numbers from otherwise undifferentiated vegetative cells. Sexual reproduction isogamous by
means of biflagellate gametes, some gametes parthenogenetic to repeat gametophytic stage. Life
history with isomorphic gametophytic and sporophytic stages.
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Growth and production
In situ growth rates of C. linum has been measured in the range of 1% to 22 % d-1 (Pedersen and
Borum 1996). In laboratory comparable rates of 3% to 15 % d-1 have been found (McGlathery and
Pedersen 1999).
A British strain of C. linum has in the lab been shown to attain maximum growth rates (22% d-1)at
irradiances of 175 µM photons m-2 s-1, temperatures of 20 ºC, a salinity of 27.5 psu, PO4concentration of 30 µM, nitrate concentrations of 800 µM or even higher at ammonium of 80 µM
(Taylor et al. 2001).
C. linum has been demonstrated to take up nitrate at a rate of 25 µmol g DW-1 h-1, and ammonium
surge uptake (first 15 minutes) to reach 125 µmol g DW-1 h-1, with assimilation rates of 50 µmol g
DW-1 h-1 (Pedersen and Borum 1997). Maximum uptake rate of P described is 667 µmol g DW-1 h-1
(Lavery and Mccomb 1991).
Optimal range of pH was shown to be from 6 to 7.5 (Menendez et al. 2002), and DIC was shown to
be limiting for photosynthesis in summer high light and high pH situations.
Cultivation
There are no reports on the cultivation of Chaetomorpha for the production of biomass, however the
biomass potential of “green tide” mats of C. linum and other macroalgae in the Venice lagoon has
been estimated to be approximately 5 kg’s of wet weight m-2 (a decrease from 10-25 kg’s of wet
weight m-2 in the late 1980’s.
Cultivation of C. linum in aerated ponds may be problematic as the filaments tend to break as an
effect of the water movement, and the needle-like fragments are able to leave the systems trough the
filters as opposed to for instance fragments of foliose algae like Ulva (NERI, unpublished).
Regarding the cultivation of Chaetomorpha sp using protoplast technology, only one report on a
biochemical study on the species Chaetomorpha aerea exists. Here regeneration of protoplasts from
extruded cytoplasm and successive development of aplanospores within regenerated cells are
described (Klotchkova et al. 2003).
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Biogas production
There are few specific report on the biogas production on the basis of Chaetomorpha sp. A methane
yield of 125 ml per g VS has been demonstrated from C. linum after a hydrothermal oxidation
pretreatment process (Nielsen et al. 2009). In one review the mixed biomass of Chaetomorpha,
Ulva and Chladophora is reported to yield 480 ml methane g VS-1 (Gunaseelan 1997). (The original
reference is a phd dissertation by Hansson, G., Methane Fermentations: End Product Inhibition
Thermophilic Methane Formation and Production of Methane from Algae. Ph.D. Dissertation,
Dept. of Technical Microbiology, University of Lund, Sweden, 1981). Another study compares the
biooil yield from macroalgae (C. linum) to land based feed stock (Sun flower)(Bastianoni et al.
2008).
Pros and cons for selecting Chaetomorpha for cultivation in Augusta plant
Positive
•
Relatively high growth rates
•
Indication of potential for elevating growth rates with CO2/flue gas addition
•
Native species present in Augusta, Sicily (documented by Algaebase and CoNISMA)
•
Potential for protoplast reproduction
•
•
No sporulation and mass disintegration reported
Negative
•
Not proven suitable for cultivation in ponds with aeration or water circulation by
paddlewheels
•
No existing experience on large scale cultivation
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Gracilaria sp.
Rhodophyta. Gracilariaceae.
General description
Gracilaria sp. is typically branched and forms up to 60 cm long bushes. The thalli is able to grow
attached as well as detached from the substrate, and in natural populations Gracilaria often forms
dense mats in shallow water areas. Thalli range from erect to prostrate and from terete to broadly
flattened. Some species form articulated fronds composed of cylindrical or irregularly shaped units.
The apical structure of the type species has been demonstrated to be uniaxial, although too compact
to be easily interpreted. Procarps, fusion-cell formation, and early gonimoblast development are
typical of the family. Carposporangia occur in chains, and cystocarps are strongly protuberant.
Spermatangia have been reported to form in one of 3 taxonomically important patterns (Bird and
McLachlan 1984), either as a completely superficial continuum or in sori flush with the outer cortex
("Chorda"-type), in shallow sunken patches ("Textorii"-type), or in deep conceptacular pits
("Verrucosa"-type). Tetrasporangia are mostly decussate-cruciate and occur both scattered and in
nemathecia, according to the species (www.AlgaeBase.org).
Lifecycle
Commonly, the genus Gracilaria is characterized by a Polysiphonia-type life history with an
alternation of isomorphic generations of tetrasporophytes and distinct male and female
gametophytes (Figure 4), however deviations from this type of lifecycle has been described for
many species of Gracilaria, including various forms of mixed reproductive phases (see references
in Polifrone et al, 2006).
16
Figure 4. The typical lifecycle of Gracilaria sp.
Distribution
The genus Gracilaria is cosmopolitan with species reported in arctic, tropical and temperate waters
(FAO, 1990). The genus is most abundant in regions where mean water temperatures are 25ºC or
more, with numbers falling off rapidly where three month mean minimum temperatures occur
(Mclachlan and Bird 1984). At least one species is described in Sicily: G. gracilis (Polifrone et al.
2006). In certain north Atlantic regions, i.e. USA and Denmark, the invasive species G.
vermicullophylla is establishing (Thomsen et al. 2007; Wilson Freshwater et al. 2006). Over 150
species have been described, many of them poorly known and with very limited distributions. Some
species long considered to be widely distributed, on the other hand, appear to be complexes of
distinct taxa difficult to separate on habit differences alone.
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Growth and production
The reported growth rates of Gracilaria are generally lower than those of Ulva. In China, growth
rates of G. lichenoides grown under optimal conditions are reported of 16.26% d-1 (Xu et al. 2009)
and for G. lemaneiformis of 13.9% d-1 (Yang et al. 2006), whereas up to 3% d-1 are reported from
laboratory optimisation of the same species (Xu et al. 2010). In Brazil mean and max growth rates
of G. birdiae were found to be 4.3 and 7.45%, respectively (Bezerra and Marinho-Soriano 2010).
From Korea max growth rates of 4.95% d-1 are reported for the species G. verrucosa (Choi et al.
2006).
In intensive cultivation systems, the annual production yield of G. tikvahiae is reported to be up to
127 T DW ha-1 year-1 in Florida (Hanisak and Ryther 1984), and up to 60 T DW ha-1 year-1 in Israel
(Friedlander and Levy 1995). In non-intensive cultivation systems production rates of 18-20 t DW
ha-1 year-1 are reported from Florida (Hanisak and Ryther 1984) and 40 t DW ha-1 year-1 from
Taiwan (Shang 1976).
Low biomass density generally yields the highest growth rate, whereas the maximal production
yield is achieved at 2-4/5 kg fresh weight m-2, depending on the incoming light (Friedlander and
Levy 1995).
Gracilaria sp. has been used for bioremediation of nitrogen rich waste water from shrimp ponds
and is reported to take up 93% of phosphate, 43 % of ammonium and 100 % of nitrate in the
particular system (Marinho-Soriano et al. 2009). G. vermicullophylla has been demonstrated to
perform well in landbased IMTA with fin fish, with tissue concentrations of nitrogen ranging
between 4 and 8% of DW depending on season (Abreu et al. ).
Addition of CO2 rich flue gas to cultivation systems with G. cornea has been reported to increase
growth rates by up to 21% (Israel et al. 2005), also addition of CO2 was found to increase growth of
several species of Gracilaria, in particular in summer, spring and autumn periods, when light was
not the main limiting factor (Friedlander and Levy 1995).
Cultivation
Gracilaria is one of the worlds most cultivated seaweed species. Due to its agar content it is of
major economical importance for the hydrocolloid industry. For this reason there is a long tradition
and much experience in the cultivation of Gracilaria. Various species of Gracilaria has for decades
18
been cultivated in large scale in the developing world, particularly in Asia, Africa, Oceania and
South America, supplying half of the global agar production (Polifrone et al. 2006). In 1990, 30,000
tonnes of dry weight of Gracilaria was harvested, including harvest from natural populations (FAO,
1990).
Gracilaria is cultured by several techniques: Unattached, in ponds (non-intensive) or tanks
(intensive) as part of integrated multi-trophic aquaculture with shrimps or fish (Friedlander and
Levy 1995; Marinho-Soriano et al. 2009), or attached in open water rafts culture on ropes or nets
(FAO, 1990).
Gracilaria has been subject for protoplast cultivation studies and several species are at the stage of
successful protoplast generation, and also plant regeneration from protoplasts. See review by Reddy
et al, 2008.
Biogas production
Various strains of two species of Gracilaria, G. tikvahiae and G. veruucosa, have proven to be
excellent substrates for methane production (Bird et al. 1990). The methane yields of 0.28-0.4 m3
kg VS-1, represented between 58 and 95% of the theoretical methane yield. The methane yield was
positively correlated to the agar content of the biomass, and negatively correlated to the melting
temperature of the agar, as well as to the total carbohydrate content.
Biogas yields of up to 0.54 l biogas g VS-1 (0.36 m3 methane kg VS-1) was demonstrated for G.
tikvahiae (Habig et al. 1984a). It was also shown that the nitrogen content of the seaweed did not
affect the biogas yields, as opposed to the biogas yield of U. lactuca, where low-nitrogen biomass
outperformed the high-nitrogen biomass regarding biogas production per unit volatile solids (Habig
et al. 1984b).
19
Pros and cons for selecting Gracilaria for cultivation in Augusta plant
Positive
•
Solid existing experience in many forms of cultivation of Gracilaria
•
Native species present in Sicily
•
Positive response of growth rate to CO2 addition
•
Positive response of growth rate to biowaste as nutrient source (NH4+ rich effluent from
shrimps/fish)
•
Potential for protoplast reproduction
•
•
Potential for commercial use of the agar
•
No sporulation and mass disintegration reported
Negative
•
Slow growth rate
•
Epiphyte competition
•
White tip disease due to bacterial growth under high temperature, low water exchange and
high nutrient load
20
Table 2. Growth rate and optimal growth condition for selected species (Mean±SD, n=3)
Maximum growth rate
-1
(%d )
Ulva sp.
25.85±2.31 (CMSCRI)
(Bruhn et al. 2011)
18.7
(Pedersen and Borum
35.0
Chaetomorpha linum
(Pedersen and Borum
21.8
1996)
Gracilaria sp.
(Yang et al. 2006)
13.9
Enteromorpha sp.
(Fortes and Luning 1980)
7
G. debilis
(Mathieson and Dawes
1972
E. clathrata
(Shellem and Josselyn 1982)
240
1996)
Optimal light
conditions
-2 -1
(µmol photons m s )
Optimal pH
Light saturated
photosynthetic rate
-1
Pn (µmol CO2 h )
C source (CO2/HCO3 )
30.2±1.13 (CMSCRI)
150
200
(Sand-Jensen 1988)
30-100
unpublished
7.5
(Menendez et al. 2001)
6-7.5
U. rotundata
(Levavasseur
140-288 dm-2
81.9
(Arnold and Murray 1980)
1972
(Mathieson and Dawes
1986)
6-7.5
6.5-8.5
1986)
-1 (Gao et al.
62-108 g fw
1993)
et al. 1991)
E. linza
-1 (Brown and
223 g fw
Tregunna 1967)
CO2 (P) HCO3- (Y)
CO2 (P) HCO3- (Y)
(Drechsler and Beer 1991)
(Gao et
al. 1993)
E. linza
(Brown
CO2 (Y) HCO3-(N)
and Tregunna 1967)
Optimal temperature
(°C)
Optimal N compound
Optimal N
concentration
Maximal N removal
-1 -1
(µmol g DW h )
15
(Ale et al. 2010)
NH4 > NO3
-1 -1
7.4 mg N (gDW d
(Pedersen and Borum 1996)
2002)
(Campbell 1999)
108
Optimal P
concentration ( µM)
Maximal P removal
-1 -1
(µmol g DW h )
Annual yield
(T DW/ha/y)
Lipid content
(% of DW)
Protein content
(% of DW)
Carbohydrate content
(% of DW)
Biogas yield
-1
(ml g VS )
(Hernandez et al.
89.0 NH4
(Mathieson and Dawes 1986)
(Taylor et al. 2001)
G. debilis
(Mathieson and Dawes 1986)
24
15
NH4
-1 -1
2.5 mg N(gDW d
(Pedersen and Borum 1996)
80µM NH4 or 800µM
NO3
25 NO3 and 50 NH4
(120 surge
(Pedersen and Borum
uptake)
21.3 NH4
(Hernandez et al.
2002)
79.5 NH4
(Hernandez et al.
2002)
1997)
(Steffensen 1976)
0.6 g / m3
2.58
45
20
(Tsagkamilis et al. 2010)
30
-1
667 µg g DW h
-1 (Lavery
and Mccomb 1991)
(Bruhn et al. 2011)
0.34-1.94
(de Padua et al.
2004)
3.25
(Ortiz et al. 2006)
27.2
53.31-58.4
2.4 (g/mg WW)
(Bastianoni
14-18.2
(Jadeja and Tewari
2008)
(Martinez-Aragon et al.
2002)
(Manivannan et al. 2008)
3.23
(Briand and Morand 1997)
1.3
6.98
(Habig et al. 1984a)
6.7-15.6
22.32
66.1
2004)
280
94-177 L CH4/kg VS
2.64
(de Padua et al.
(Bruhn et al. 2011)
(Martinez-Aragon et al.
40-127
et al. 2008)
1.25
2002)
125 (methane)
(Nielsen et
al. 2009)
(Habig et al. 1984b)
(Wang et al. 2009)
1.28
(Haroon.A.M. et al.
3.47-4.36
2000)
4.16-15.89
(Haroon.A.M. et
al. 2000)
(Wang et al. 2009)
23.99
(Haroon.A.M. et
29.09-39.81
al. 2000)
23.84
83-430
540
Calorific value
-1
(MJ kg )
Ash (% of DW)
77-560
(Marsham et al. 2007)
15.7
12.54-20.61
(de Padua et al.
2004)
28.1-30.2
13.4
(own data, DTI)
(Givernaud et al. 1999)
29-43
(Mageswaran and
24-38%
Sivasubramanian 1984)
32-36%
(guilera-Morales et al.
2005)
37.09
(Wang et al. 2009)
34.5-47.7
DTI
7.1 (G. longissima,
data
)
21
Table 3. Proximate composition of carbohydrate, protein and lipid in different seaweeds
(Mean±SD, n=3)
S.No
Species
Carbohydrate
Protein
Lipid
Moisture
(% DW)
(% DW)
(% DW)
( %)
Rhodophyta
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Amphiora anceps
Kappaphycus alvarezii
Gelidiella acerosa
Gelidium micropterum
Gracilaria corticata
Gracilaria dura
Gracilaria debilis
Gracilaria fergusonii
Gracilaria salicornia
Laurencia cruciata
Sarconema filiforme
Phaeophyta
41.09±2.84gh
47.42±3.51def
55.55±4.10bc
51.67±3.40cd
48.35±2.56de
58.62±3.17ab
61.63±2.25a
46.56±1.96efg
40.81±0.76hi
31.43±1.89jk
39.69±3.69hi
6.90±0.42n
14.84±1.24d
16.77±0.95bc
12.66±1.14fgh
17.14±1.32bc
7.66±0.25mn
14.76±1.45de
10.82±0.69hijk
10.34±1.47ijkl
16.11±1.30cd
10.57±0.68ijk
1.23±0.15hi
1.50±0.30h
1.47±0.12h
0.91±0.16i
1.97±0.15ef
1.10±0.20i
1.50±0.17h
0.57±0.06j
1.24±0.03hi
1.53±0.06gh
1.47±.06h
77.90±1.73h
88.92±2.96bc
80.13±2.80gh
79.19±2.92h
88.27±1.99bc
88.06±2.31bc
86.78±2.62bcde
85.32±2.46cdef
89.00±2.32bc
93.03±2.69a
83.51±1.57defg
12.
Cystoseira indica
Padina
tetrastromatica
Sargassum swartzii
Sargassum
tenerrimum
Spatoglossum
asperum
Chlorophyta
32.62±2.17jk
12.95±0.34efg
1.23±0.12hi
82.71±1.04fg
87.07±2.76bcd
28.69±2.68k
33.30±3.07j
22.11±2.28a
2.07±0.31de
ghij
11.21±1.43
2.37±0.25cd
30.30±1.55jk
10.75±0.75ijk
13.
14.
15.
16.
17.
18.
19.
20.
21.
Ulva fasciata
Ulva reticulata
Ulva rigida
Caulerpa racemosa
Caulerpa veravelensis
Caulerpa
scalpeliformis
22.
a-n
78.21±3.24h
83.04±3.04efg
2.03±0.35def
86.28±1.69bcdef
21.99±2.64
l
9.89±0.33
jkl
2.50±0.30
c
46.73±2.25efg
57.96±1.75ab
56.07±2.68b
43.50±2.19fgh
33.10±0.95j
14.30±0.95def
16.72±1.29bc
18.57±1.82b
8.68±0.98lmn
9.19±0.40klm
1.83±0.21fg
2.03±0.21def
2.00±0.20ef
2.16±0.17de
2.65±0.17b
36.59±1.34i
12.24±0.63ghi
3.03±0.21a
85.61±2.36cdef
88.42±0.84bc
89.98±0.79ab
86.93±1.14bcd
83.73±2.22defg
89.68±2.14ab
Values in a column without a common superscript are significantly different at p<0.01.
22
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Biomass. 1. Combustion Characteristics of Enteromorpha clathrata and Sargassum natans. Energy
& Fuels, 235173-5178.
Wichard, T. & Oertel, W. (2010). Gametogenesis and gamete release of Ulva mutabilis and Ulva
lactuca (Chlorophyta): Regulatory effects and chemical characterization of the swarming inhibitor.
Journal of Phycology, 46(2), 248-259.
33
Wilson Freshwater, D., Montgomery, F., Greene, J., Hamner, R., Williams, M., & Whitfield, P.
(2006). Distribution and Identification of an Invasive Gracilaria Species that is Hampering
Commercial Fishing Operations in Southeastern North Carolina, USA. Biological Invasions, 8(4),
631-637.
Wosnitza, T. & Barrantes, J. (2006). Utilization of seaweed Ulva sp. in Paracas Bay (Peru):
experimenting with compost. Journal of Applied Phycology, 18(1), 27-31.
Xu, Y. J., Wei, W., & Fang, J. G. (2009). Effects of salinity, light and temperature on growth rates
of two species of Gracilaria (Rhodophyta). Chinese Journal of Oceanology and Limnology, 27(2),
350-355.
Xu, Z. G., Zou, D. H., & Gao, K. S. (2010). Effects of elevated CO2 and phosphorus supply on
growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis
(Rhodophyta). Botanica Marina, 53(2), 123-129.
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http://www.fao.org/docrep/field/003/AB730E/AB730E00.htm
34
Appendix 1. Note on Caulerpa (CMSCRI)
Appendix 2. Algae from Augusta Bay (CoNISMA)
35
A NOTE ON CAULERPACEAN
PLANTS & THEIR TOXICITY
Prepared By
AquAgri Processing Private Limited
New Delhi, INDIA
April - 2010
CONTENTS
1.
Genus Caulerpa
2.
Edible Caulerpa spp.
2.1. Cultivation of C. lentilifera
2.2. Market demand
3.
Toxic Caulerpa spp.
3.1. Toxins and their Chemistry
3.2. Effects on autochthonous species
3.3. Toxic effect on microbial loop
3.4. Toxic Effect on invertebrates
3.5. Toxic effect on flora
3.6. Toxic effect on fish communities
4.
Invasion issue
4.1. Caulerpa taxifolia
4.2. Invasion properties, Reproduction & Nutrition dynamics
4.3. Control Measures, Strategies and Prevention
4.4. Caulerpa and the Law
5.
Caulerpa and bio-fuels
6.
Caulerpa and waster water treatment
7.
Bioactive compounds from Caulerpa
8.
Why Caulerpa in B4B project
9.
References
1. GENUS CAULERPA
Green algae of the family Caulerpaceae, represented by the single genus Caulerpa, are found worldwide, generally in
shallow water tropical and subtropical marine habitats. All species, which are traditionally separated by their distinct
morphologies, possess a rhizome that produces erect blades and rhizoids that penetrate sediments.
Although individual plants are composed of only one cell, Caulerpa has a complex morphology, composed of pseudoorgans that often resemble the roots, shoots and leaves of higher plants. It is one of the most distinctive genera of
seaweeds, making it identifiable solely on the basis of its habit1. It consists of a creeping rhizome that produces tufts of
colourless rhizoids downward and photosynthetic branches (assimilators) upward. The phylogeny of the genus
Caulerpa is given as below.
KINGDOM :
DIVISION/PHYLUM:
CLASS
:
ORDER :
FAMILY :
GENUS :
Protista/planta
Chlorophyta
Chlorophyceae / Bryopsidophyceae
Caulerpales/ Bryopsidales
Caulerpaceae
Caulerpa
Over 100 species of genus Caulerpa are found worldwide. In Indian waters the genus stands second highest in species
diversity recording 22 species and 23 varieties and forma. The species of Caulerpa are widespread in tropical waters
like Atlantic Ocean (West Indies and African coast), the Indian Ocean (Pakistan, Sri Lanka, and north western
Australia), and the Pacific Ocean (Philippines, Indonesia, Japan, New Caledonia, and north eastern Australia).
2. EDIBLE CAULERPA SPECIES
Several species and varieties of this genus are edible and have been used traditionally in the form of fresh vegetable or
salad. C. lentillifera is a tropical food alga and commonly known as ‘green caviar’ or ‘sea grapes’. This species has been
recently rediscovered from Samiani Island (N 22. 29& E 69. 05), West coast of India2, 2004) and has been successfully
cultivated in tanks3.
2.1. Cultivation of C. lentillifera
Pond cultivation: Vegetative fragments of about 100 g fresh weight are inoculated in 1 sq meter area or 1 ton ha-1.
The first harvesting is done after 60 days and subsequent harvests could be achieved at the interval of two weeks
maintaining the initial stocking density in the pond.
Open lagoon cultivation: This type of cultivation is carried out in the lagoons. Bunches of Caulerpa cuttings are buried
at 0.5 meter intervals at the bottom of lagoon. The rest of the cultivation practices and harvesting strategies are similar
to that of pond cultivation.
Cage cultivation: Multistage, cylindrical cages are used. Small bundles of thalli (ca. 10 g), cut in to 10 cm sections, are
tied to the middle of the floor of each stage of the cage, which are then hung in the sea. During harvesting portions of
the thalli projecting out of cage are harvested. Several harvests per month by this method are possible depending on
growth rate of plants. Production of fresh Caulerpa from 112 rafts with 1, 344 cages can reach about 10 tons during the
cultivation season2a.
2.2. Market demand
It has been extensively cultivated in the Philippines and Japan with annual harvest of about 5600 tonnes of fresh4.
(White & M. Ohno). The fresh fronds of Caulerpa are packed in 100-200 g packages for marketing. These will stay
fresh for about 7 days, if kept chilled and moist. Salted and dehydrated Caulerpa, when soaked in fresh water rapidly
swells and recovers its original shape within few minuets and thus have advantage of marketing in ready-to-eat packets.
Seaweed placed in bottle along with seawater will remain fresh for three months under lower temperatures.
Caulerpa lentillifera
In India, Avelin Mary et. al. have
demonstrated the culture of C.
lentilifera in Tanks. 16gm of C.
lentilifera grew to 12.4kg in 6
months3.
Figure 1:
C. lentillifera was cultured in tanks and conventional natural fishing ground, it was found that growth rate was
higher in tank culture as compared to culture done in natural fishing ground5.
Table 1: Tank culture of C. lentillifera and growth rate
Class
No.
Weight at
stat
Harvest Kg
Days
required
Manured
Daily growth
rate %
1
2.1kg/t tank
2.9
7
No
2.00
2
5kg/10t tank
34.0
40
Yes
2.08
3
2kg/20t tank
8
30
No
2.01
2
2kg/20t tank
10.5
30
No
2.39
Table 2: Culture of C. lentillifera in fishing ground and growth rate
A conceptual view of the apparatus
for cultivation of C. lentillifera
Class
No.
Weight at
stat
Harvest Kg
Days
required
Manured
Daily growth
rate %
1
200g/m2
2.5
60
No
1.77
2
200g/m2
1.8
60
No
1.59
3
200g/m2
2.0
62
No
1.72
4
200g/m2
4.0
77
No
1.69
3. TOXIC CAULERPA SPECIES
Many species of Caulerpa, including the Mediterranean “aquarium strain” C.
taxifolia, C. racemosa are toxic to herbivores, fish populations, invertebrates and
seagrass in a region where it is not native. They produce the sesquiterpene
caulerpenyne as a major metabolite. Caulerpenyne concentrations are often 2%
or more of algal dry mass and are higher in the erect blades than in the rhizoids.
Various biological effects including toxicity have been attributed to caulerpenyne.
Whereas, in the tropics, most species of Caulerpa are readily consumed by
herbivorous reef fishes such as rabbitfishes (Siganidae) and surgeonfishes
(Acanthuridae). Crude extracts of several species of Caulerpa as well as
caulerpenyne do not deter feeding by any species of herbivorous fishes against
which they have been tested. A few tropical species of Caulerpa including C.
ashmeadii and C. bikinensis, which produce sesquiterpene aldehydes instead of
caulerpenyne, have chemical defenses against herbivorous reef fishes. Toxicity
and invasion issues of C. taxifolia has beeb extensively reviewed by Pierre MADL
& Maricela6.
Caulerpa taxifolia
Caulerpa racemosa
3.1. Toxins & their chemistry
Mediterranean collections of C. taxifolia produce caulerpenyne, oxytoxins, taxifolials and other terpenes. A woundactivated transformation of caulerpenyne to oxytoxins has been described for Mediterranean C. taxifolia. Caulerpa
taxifolia is unpalatable to generalist herbivores in the Mediterranean (where herbivorous fishes are not present) and
can affect the physiology of sympatric fishes. The chemical defenses of C. taxifolia appear to have facilitated this
biological invasion, which is greatly affecting the benthic community structure in areas where it occurs. The aquaria
strain of C.taxifolia contains higher CYN concentrations than the tropical strain. C.racemosa as a Lessepsian migrant is
likewise a tropical representative, but far less toxic than the C.taxifolia. The mean CYN values were found to be 80x
higher in C. taxifolia than in C.racemosa and are much higher than in other Caulerpa species. CYN in the aquarium
strain of C. taxifolia can account for up to 1.3% of the algal fresh weight or 2% or more of algal dry mass7.
C. taxifolia is native to the tropics thus subject of intense herbivore activity leading to the development of efficient
chemical defense and antifouling capabilities. The cocktail of repellent toxins consists of caulerpenyne (CYN),
oxytoxins, taxifolials and other terpenes. As CYN is the most predominant toxin, it is believed that toxicity is almost
exclusively based on the acetylenic sesquiterpene caulerpenyne with a bis-enol acetate functional group7. Caulerpin,
on the other hand, is a hydrophobic macromolecule containing a cyclo-octatetraene ring pigment8. This molecule is
synthesized in the fronds of the algae, thus concentrations are higher in the erect blades than in the rhizoids, where
they are released into the surrounding sea-water or consumed by herbivores9.
Caulerpenyne
Caulerpin
Caulerpenyne, caulerpin and other metabolites isolated from Caulerpa species
Caulerpa toxicity & Seasons
Caulerpa's toxicity is highly seasonal; the heaviest disturbance occurred in summer and autumn when the size of
C.taxifolia and its terpenoids production peaked at a maximum. Epiphytic and epizootic growth on C.taxifolia is
insignificant except in spring when endotoxin concentration is lowest10. The annual decrease in CYN concentrations,
with the concomitant increase in frond length, under conditions of competition with P.oceanica is a likely result of a
modified metabolism in the alga as the increased energy allocated to growth of fronds would be at the cost of another
function11. Usually during late winter, the cover of C.taxifolia generally decreases with algal fronds much smaller12, only
to pick up again during the warmer months to recuperate lost terrain.
This periodic cycle correlates with its high growth rate, its total substrate occupation, light access, and sedimentation
rates. This oscillation is reflected in the CYN concentration of the alga's frond wet weight: from to 0.2% in spring to 13%
in summer13. CYN is known for its repulsive and antifouling effects14 confirming the presence of highest CYN at the
surface of the alga with a negative gradient in the immediate seawater environment10.
3.2. Effects on autochthonous species and C. taxifolia's toxicity
As C. taxifolia colonizes all types of substrata from the eulittoral down to 100m depth, inducing a homogenization of
microhabitats and a reduction of the architectural complexity of the substratum15, a decrease in diversity and
abundance of motile invertebrates was observed in the C.taxifolia meadows16, as well as a persistent decrease in mean
species richness, density and biomass of fish assemblages15. Relini et al.17 described qualitative and quantitative
changes in fish communities during the replacement of the sea grass Cymodocea nodosa with that of C.taxifolia (at
Imperia, western Ligurian Sea, Italy). In addition to the high fishing pressure (local/coastal fishing industry) and weak
rugosity, they strongly impacted upon density and demographic structure of fish assemblages and ultimately leading
also
to
a
decrease
of
the
abundance
of
larger-sized
fishes.
Also the possible transfer of toxins through the food chain presents a toxicological risk not only for marine organisms
exposed to it but also for man; i.e. certain mollusks feeding on Caulerpa showed a two- to three-fold concentration of
toxic metabolites and became themselves toxic to predators, while human food poisoning resulting from the
consumption of the Mediterranean bream Sarpa salpa has been already observed18.
3.3. Effect on microbial loop
Soft sediment bottoms are not only characterized by a high infauna and epibenthic fauna, but are directly coupled to
the microbial association of the sandy substrate. Particulate organic material and plankton organisms in the surface
water are trapped and accumulate temporarily in shallow soft bottom sediment. Usually some of this carbon is
available for consumption by benthic microbes in the system. However, the presence of an algal mat on otherwise
unvegetated shallow soft bottoms considerably changes its ecosystem structure and functions. Rather than enabling a
healthy microbial association to perform the nutrient conversion and especially under eutrophicated conditions,
C.taxifolia takes over the "recycling activity". The altered nutrient dynamics of the sediment becomes evident in the
net accumulation of organic matter. In the long term however, the organic enrichment leads to higher oxygen
consumption that, together with the reduced water exchange, will result in decreased oxygen levels in both the water
column and the sediment. The reduced oxygenation of the sediment causes the redoxcline to move towards the
sediment surface further reducing the mineralization-capabilities of the microbial loop19.
3.4. Effect on invertebrates
It has been observed that this invasive species suffocates numerous white Gorgonians Eunicella verrucosa at depths
beyond 40m. The numbers of individuals of mollusca, amphipoda and polychaeta in C.taxifolia meadows were greatly
reduced. Aquaria observation revealed that after massive "bleeding" of a large Caulerpa-stand following spontaneous
gametogenesis or mechanical injury, tubeworms behave abnormally. They will crawl half way out of their tube or even
abandon the tube entirely, only to die shortly afterwards20.
It is already known that C.taxifolia has a repulsive effect against various herbivores, and particularly against the
tropical Atlantic urchin Lytechinus variegatus21. It simply means that algal endotoxins disrupt the entire food chain and
biodiversity of the affected ecosystem.
(8) Schröder et al., (4.611998) have shown that multixenobiotic resistance (MXR) membrane pumps - present in marine
organisms - are negatively affected by CYN and caulerpin; i.e. otherwise non-lethal concentrations of environmental toxins in
combination with suppressed MXR mechanism resulted in a strong apoptotic response of target cells21a.
3.5. Effect on flora
The creeping and erect axes of C.taxifolia shade off the light while its rhizoids trap and chemically alter the sediment.
Most autochthonous algae tend to disappear quickly while crustose algae seem to be eliminated latest. The
paucispecific C.taxifolia meadows tend to substitute for all sheltered algal infralittoral phytocoenosis which stands for a
dramatic fall of richness and diversity of the littoral ecosystem. Among the dozens of plants that are found in an intact
Mediterranean ecosystem are the marine phanerogams of Posidonia, Cymodocea or Zostera. Posidonia oceanica is a
dark, gray/green endemic sea grass covering large areas of the seabed at depths between 30-40m22, thus a
fundamental key sea grass for that ecosystem. Posidonia meadows, like the other species of sea grass, not only
bolster and protect the coastline, but it is one of the most important coastal primary producers, act as a refuge, habitat,
substrate for epiphytes, providing food and shelter for a huge variety of fish and invertebrates, and is the spawning
ground and nursery for a countless number of species.
As species-poor meadows of C. taxifolia cover the infralittoral zone, it replaced the rich natural algal populations along
with the disappearance of many of the normally occurring species associated with it, resulting in a drastic reduction in
the richness and diversity of the Mediterranean littoral ecosystem. Due to the synthesis of toxic secondary metabolites
(mono- and sesqui-terpenes) C. taxifolia has another advantage over the native seaweeds and sea-grasses.
3.6. Effect on fish communities
Bottom dwelling species (important commercial fish species) however suffered a severe blow due to the reduction of
sandy seabed by the arrival of C.taxifolia. In another study Francour et al.,23 focused on the color patterns of
individuals of four Mediterranean labrid species, Symphodus ocellatus, Symphodus roissali, Symphodus rostratus, and
Coris julis, living in dense C.taxifolia meadows. They were compared with those of the same species inhabiting their
usual indigenous habitats, the P.oceanica seagrass beds and the shallow rocky areas. In C.taxifolia meadows the
proportion of green morphs observed in S.ocellatus and C.julis was significantly higher, particularly for small fishes.
While S.ocellatus and C.julis settled in C.taxifolia meadows, S.roissali withdrew to shallow waters where C.taxifolia is
not the dominant vegetation24.
4. INVASION ISSUE
4.1. C. taxifolia
The establishment of an aquarium strain of C. taxifolia was first found in the Mediterranean in the 1984. This
seaweed has been a popular plant in the aquarium industry in Europe in 1970s. From its first at the base of the
Monaco aquarium (from where it was accidentally released), it has now spread throughout of the western
Mediterranean Sea. Molecular analysis of the colonies of the seaweed collected in the Mediterranean Sea and
various aquariums are both similar and very different from natural populations, and provides evidence that this strain
is used in the global aquarium trade or exchange in North America, Australia, Japan and elsewhere. Not surprisingly
it acquired negative fame as the "Aquarium-Mediterranean strain" or even publicized as the "Killer Algae".
This is underlined by recent discoveries of Caulerpa taxifolia at the coast of California (USA) and New South Wales
(AUS) raising public concern about the potential danger of a new invasion similar to the one endured by the
Mediterranean Sea over the past decades. Although natural (wind & ocean currents) vectors aid in its distribution, the
main dispersal agent spreading C.taxifolia across the globe is human-mediated. The aquarium trade in particular, is
the most likely source of introduction to the Australia, Oceania, and the Americas.
4.2. Invasion properties, Reproduction Nutrient Dynamics of C.taxifolia
Invasive Properties
Vegetative reproduction is usually the commonest, and often the only method of reproduction; as a result,
i. one viable propagule is sufficient to start a new colony;
ii. vegetative reproduction is prolific;
iii. habitat requirements are flexible;
iv. they tolerate environmental fluctuations and extremes of the invaded habitat
v. there is a similarity between the native and recipient habitat;
vi. they are free from predators and diseases characteristic of their native range;
vii. human influences aid in the in-/direct proliferation through water pollution, toxicants, etc.
Since the launch of the invasion in 1984, the alga's spread continued resulting in coverage indices in the most
affected benthic areas of up to 100% between depths of 1 to 35m. Below this depth, it has been observed - though at
much smaller densities - as far down as 100m. Such depths are unknown for the tropical strain of C.taxifolia: 30m at
Papua-New Guinea, 32m at Tahiti, 50m at New Caledonia, 32m in the tropical Atlantic around Virgin. Potential
invasion sites are first colonized around headlands and were drifting algal fragments can attach. With its ability to
form dense carpets, the aquarium strain is capable of extremely rapid growth resulting in exceptionally dense
meadows. This is in sharp contrast to the tropical strain of C.taxifolia where it occurs in isolated and patchy
aggregations25.
Thus it comes of no surprise that C.taxifolia growing in the Mediterranean sea (with distinct seasons such as summer
and winter) exhibits a corresponding growth rhythm. New sprouts emerge in the spring from the remnants of the
overwintering population. These plants can grow 1-2cm per week (growth in the tropics is much faster). Thus, the
rate of expansion of this invading species as well as the impacts noted upon the environment, along with the feature
of asexual reproduction, assigns this weedy species a catastrophic and property represents a major risk for shallow
underwater ecosystems of the Mediterranean.
Reproduction: Species of the genus Caulerpa can reproduce both sexually and asexually. According to Meinesz,
C.taxifolia is able to disperse a shower of male and female gametes that pair up and fuse to form a zygote (new plant)
under lab-conditions. In the wild, though, the only reproductive cells released are male confirming existing evidence
that all C.taxifolia in the Mediterranean are clones of that single aquarium plant release in 1984.
Genetically, this invasive species shows relatively little variation, thus vegetative reproduction by fragmentation is the
most common mode of proliferation (asexual or clonal propagation). The break-up of thalli (mediated via anchor
damage, fishing gear or storm activity as small as 1cm2) gives rise to new colonies that usually appear in 2 to 10m
deep water during summer and fall when growth rates are highest26.
Nutrient dynamics: C.taxifolia can utilize nutrients and carbon sources from the sediment via uptake through the
rhizoids and associated bacteria (Chisholm et al., 1996), even in eutrophicated, anoxic sediments. Therefore the alga
was shown to be tolerant to shading conditions27 enabling growth in areas where photosynthesis is light-limited as a
result of greater depths or during the darker winter months.
4.3. Control Measures and Prevention
Various attempts that range from manual uprooting, mechanical means (underwater suction devices), physical control
with dry ice, to chemical intervention utilizing household bleach (chlorine) and other chemicals have been tried to halt
the spread of this invasive species. Some selected predators that are able to feed on this particular mutant was also
tried Mediterranean. Some have tried to tear up the patches of algae but one torn leaf that gets away can generate a
whole new outbreak. Divers have used pumps to pull out the plant but it seems to regenerate in the same place at a
rate quicker than its original growth rate. Other eradication methods include poison, smothering the algae with a cover
that lets in no light, and using underwater welding devices to boil the plant.
Manual uprooting has been executed by trained and motivated divers but it is a solution for small algal patches
measuring a few square meters, but even then it is not 100% effective. Sometimes there is re-growth and the operation
has to be repeated. This technique is unfeasible, and tends to be a lost cause from the outset in-depth growth,
guaranteed re-growth and exorbitant cost.
Physico-chemical elimination procedures were considered and tested either in an aquarium or at an experimental
site. These involve certain chemicals, cross-ionic dialysis, vacuum hoses, airlift sediment suckers, suction pumps, dry
ice, ultrasound, hot water jets, etc. Although not very efficient with larger patches, these methods can be applied in
areas with smaller infestations; e.g. being smaller in extension, annual control measures in Croatia have been
implemented by covering isolated colonies with black plastic sheets and removing the alga with a suction pump. Since
these methods do not meet one or more of the criteria (effectiveness, absence of re-growth after one month, nondispersal of cutting, absence of secondary effects on other systems), the only feasible strategy is not one of total
eradication but rather one of slowing down the rate of spread by eradicating small, isolated patches through a
combination of various techniques.
Biocontrol via potential predators of C. taxifolia
Since 1994, the potential use of four ascoglossans (Mollusca: Opisthobranchia) as biological control agents against
C.taxifolia (and C.racemosa) have been examined. These mollusks make incisions on all parts of C.taxifolia. They
perforate the cell wall with its uniserial radula and sucks up a small portion of the algal contents, leaving light colored
markings on the alga. Most ascoglossan sequester secondary metabolites from its diet for their own defense28 thus
storing and using caulerpenyne (CYN) from C.taxifolia as a feeding deterrent.
One of the more unspecific predators is Berthelina chloris. Infestation with this snail over a period of a few months
creates a booming bivalve population that pierce into the thalli and cause the algae to “bleed”. Under such pressure and
within a few days Caulerpa attains a vitreous appearance that triggers collapse of entire sections.
Oxynoe
olivacea
is
a
Mediterranean
ascoglossan
species has become an adapted
feeder on the invading tropical alga
C.taxifolia29.
Oxynoe olivacea
Oxynoe azuropunctata
Lobiger serradifalci, another
shelled species native to the
Mediterranean
that
naturally
feeds on C.prolifera has been
observed to settle and feed on
C.taxifolia.
Lobiger serradifalci
Oxynoe azuropunctata is also
a shelled species feeding
exclusively on Caulerpales and
has a higher feeding rate than
either
O.olivacea
or
L.serradifalci; an individual is
able to destroy a 3-4.5cm of
frond per day30.
Elysia subornata
Elysia subornata, it feeds only on
Caulerpa species by causing incisions
with the radula - incised algal thalli
rapidly become necrotic and die. The
grazing rates correspond to the
destruction of 5-6cm/day of frond at
21°C; this is 2-11 times higher than
those recorded for the Mediterranean
ascoglossan species29.
Preventive Methods: To prevent the spread of C. taxifolia following guidelines were set:
Home-Aquaria: As alternatives are available, every owner of a salt-water aquarium should refrain from using this
seaweed!
Fishing: If any seaweed suspected to be C.taxifolia is found on fishing gear it should be removed, carefully bagged
and definitely not thrown back into the sea, since even a small fragment has the potential to regenerate into a new
plant and reported.
Boat: Long-distance spread should be avoided by informing owners of private vessels of the need to check and clean
their anchors, trailers, rudders, after mooring in contaminated areas.
Water Sports: Sun-lovers, snorkellers, divers, and fishermen should be instructed to inform their local authorities and
environmental services each time they sight new patches or populations of C. taxifolia.
4.4. Caulerpa & the Law
As the aquarium strain of C.taxifolia proofs to be extremely successful under a wide range of environmental
conditions, it has shown to cause major ecological and economic damage in the north-western Mediterranean. C.
taxifolia has proven to be an opportunist whenever an ecosystem is out of balance. Thus, this seaweed showed to
have devastating ecological and economic impacts not only in the Mediterranean but also in other regions where it is
not native. It has formed dense carpets, out-competed native seaweeds and sea-grasses and displaced
invertebrates. Such carpets can also cause sediment anoxia, which affects the infauna. Chemical analyses and
feeding trials have demonstrated that the alga contains toxins that deter herbivores, including fish. Where C. taxifolia
has invaded and established itself successfully, species diversity and abundance is reduced, resulting in substantial
losses in fisheries production. In addition, the presence of C.taxifolia reported has harmed tourism, pleasure boating
as well as recreational diving.
Therefore, any invasion of C. taxifolia into new territory must be tackled promptly and action plans applicated
immediately in order to prevent any further spread. The spread of an aquarium strain of C. taxifolia in the
Mediterranean has led several governments (Australia, France, Spain and USA) to ban its use in the aquarium trade
in order to prevent it from escaping to new geographical areas.
EU: In a decree dated 4th of March 1993, the French Minister for the Environment and the State Undersecretary for the
Sea banned the offering, the sale, buying, use and dumping into the sea of all or parts of the specimens of the algae
Caulerpa taxifolia. Collection and transport of the algae are also subject to a system of authorization granted on
presentation of a well-grounded request.
AUS: The risk of an introduction of non-native C.taxifolia to Australian waters has been recognized by the Australian
Quarantine and Inspection Service with the implementation of an import ban of the species in 1996. The alga was listed
as a Noxious Species by the parliament of New South Wales (NSW) on 1st of October 2000; it cannot be bought, sold,
traded, or kept in an aquarium in NSW
NZ: The New Zealand government put the aquaria strain of C.taxifolia to the list of species on the Plant Pest Accord for
surveillance of retail outlets by Regional Councils.
USA: Assembly Bill 1334 (Harman), signed into law by the Californian Governor in September 2001, prohibits the
possession, sale, and transport of C.taxifolia throughout that state.
5. CAULERPA AND BIOFUELS
A research was carried out on “Cultivation and conversion of Marine macro algae” in search of promising marine algae
for bio-fuel purpose by US govt. in 1984. The work was performed under “Solar Energy Research Institute (SERI)”
Colorado with funds provided by the Biomass Energy Technology Division of the U.S. Department of Energy.
In their study, total extractable lipid content for 20 species of marine algae including Caulerpa species were studied.
The highest lipid content i.e. 80mg/g (freeze-dried) was found with C. verticillata (also contained greater amount of
hydrocarbon), C. prolifera contained 58mg/g, C. mexicana 33mg/g and C. racemosa 30mg.g. Attempt was also taken to
culture C. prolifera in both outdoor & indoor. It would therefore be of interest to investigate the possibility of increasing
its lipid content by nitrogen limitation and /or other manipulation of environmental conditions and culture management
practices, as has been found necessary to increase the lipid fraction of micro algae31.
6. CAULERPA AND WASTE WATER TREATMENT
There are few reports in the literature on the adsorption of capacities of genus Caulerpa. Dyes used in textile industry
are important causes of pollution in aquatic ecosystems. The dyes which are released into the aquatic environment
without treatment inhibit development of aquatic animals and plants by blocking sunlight penetration. Over 7x105
tones of dyes and about 10,000 different types are produced in the world but unfortunately only about 10-15% of the
total produced dyes is released in to the aquatic system without being removed from the effluents. The biosorption
capacity for heavy metals (Cu, Cd, Pb, Zn) by dry C. lentillifera after the pretreatment with NaOH was by Pavasant et
al.32. Alkaline treatment (0.5N) was found to promote the adsorption capacities for Cu and Pb by 16 and 67%
respectively and no pretreatment was found to enhance the adsorption capacities of Cd and Zn.
Marungruneng & Pavasant33 have investigated the adsorption of a dye, astrazon blue FGRL into C. lentillifera from
aqueous solution and adsorption was 49.26mg/g. In another studies C. lentillifera exhibited greater sorption
capacities than activated carbon for some basic dyes such as Astrazon Blue FGRL, Astrazon Red GTLN and
methylene blue34. Dry biomass of C. racemosa var cylindracea was shown to have adsorption capacity for methylene
blue. The adsorption reached equilibrium at 90 min for all studied concentrations (5-100mg/L)35.
7. BIOACTIVE COMPOUNDS FROM CAULERPA
i. Antiproliferative as well as growth-inhibitory effects of sesquiterpene in eight cancer cell lines of human origin have
been reported37,38 and similar results were with in vitro tests of caulerpin by Ayyad & Badria38, 45.
ii. CYN is known to induces neurological disorders (i.e. amnesia, vertigo, and hallucinations, reported by De Haro et
al.39 on patients with food poisoning due to the ingestion of Sarpa salpa that fed on C. taxifolia.
iii. CYN, besides its inhibitory effect on the Na+/K+-ATPase, also affects some other ion channels accounting for
reduced after-hyperpolarization amplitudes and the decrease of cellular membrane resistance36,40.
iv. CYN exhibits antibiotic activity41,42.
v. Sulfated polysacchries isolated from C. racemosa shown anti-herpetic activity. Hot water fractions was a selective
inhibitor of reference strains and TK− acyclovir-resistant strains of herpes simplex virus type 1 (HSV-1) and type 2
(HSV-2) in Vero cells, with antiviral effective concentration 50% (EC50) values in the range of 2.2–4.2 µg/ml and
lacking cytotoxic effects43.
vi. A polysaccharide, CrvpPS, was isolated from C. racemosa var peltata. It was reacted with nano-selenium in distilled
water containing ascorbic acid (Vit C) to form a stable CrvpPS-nano-Se complex. The immunomodulatory effects of
CrvpPS and CrvpPS-nano-Se on T lymphocytes subgroups and NK cells in mice were investigated. After intragastric
administration for 10 days separately, both CrvpPS and CrvpPS-nano-Se showed significant stimulatory functions to
thymus gland of mice. Moreover, the CrvpPS-nano-Se induced the percentage of CD3 +, CD3 +CD4 +, NK cells and
the CD4 +/CD8 + value to increase significantly (P<0.05) when analyzed by flow cytometry, which is better than the
CrvpPS, sucrose-nano-Se, and even the positive drug levamisole44.
vii. Caulerpin and Caulerpicin have been described as toxic constituents of edible species of the green algal genus
Caulerpa, but evidences in later studies indicate that they have no acute toxicity. Caulerpin, which has a structure
related to auxin, promotes plant growth46.
viii. The edible species become peppery to the taste during rainy months in the Philippines, and other species are not
eaten because of the extremely peppery tase. Caulerpicin was reported to be responsible for manifestation of such
toxc symptoms such as mild, anaesthetizing sensation, numbness of tongue, and cold sensation in the feet and
fingers.
8. WHY CAULERPA IN B4B PROJECT
i. It is understood from the literatures that though Caulerpa species like C. taxifolia and C. racemosa are not causing
any adverse effect to their native environment, they are very harmful to non-native marine ecosystem, therefore, these
species will be not recommended for culture or any kind of work for B4B project.
ii. C. lentilifera is an edible alga and can be selected for B4B project
iii. C. lentillifera and C. racemosa var cylindracea are reported to have good adsorbing capacity for heavy metals and
different kinds of dyes, therefore, these species might be useful in waste water treatment.
vi. C. verticillata and other caulerpacean species have been reported to contain high amount of lipids, hence, may be
potential species for biofuels.
vii. In Indian waters about 20 species of Caulerpa including C. taxifolia and C. racemosa are available. Leaving these
two harmful algae, other species can be screened for their methane content / waste water treatment.
9. REFERENCES
1.
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87(10), 1321-1322. 2a. Personnel communication from Mantri, V. A. 2009.
3. Mary, A., Mary, V., Lorella, A., Matias, O. R., Rediscovery of naturally occuring seagrape Caulerpa lentillifera from the Gulf of Mannar
and its mariculture, Current Science, 2009, 97(10), 1418-1420.
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effects of extracts from the marine alga Caulerpa taxifolia and of toxin from Caulerpa racemosa on multixenobiotic resistance in
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Parc Nat. Rég. Corse & GIS Posidonie Edit. Marseille
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ichthyofauna of North-Western Mediterranean sea: preliminary results; Hydrobiologia 300/301:345-353
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Lemée R., Mari X., Molenaar H., Perney L., Venturini A., 1993; Suivi de l'invasion de l'algue tropicale Caulerpa taxifolia devant
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Cd2+, Pb2+ and Zn2+ using dried marine green macro alga Caulerpa lentillifera. Bioresource Technology, 2006, 97, 23212329.
33. Marungrueng, K., Pavasant, P., Removal of basic dye (Astrazon Blue FGRL) using macro alga Caulerpa lentillifera. J.
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Ulva: Sea lettuce
This is a small genus of marine and brackish water green algae. It is edible and is often called 'Sea
Lettuce'. Species with hollow, one-layered thalli were
formerly included in Enteromorpha, but it is widely
accepted now that such species should be included in
Ulva.
The thallus of ulvoid species is flat and blade-like and
is composed of two layers of cells. There is no
differentiation into tissues; all the cells of the plant are
more or less alike except for the basal cells, which are
elongated to form attachment rhizoids. Each cell
contains one nucleus and has a cup-shaped choroplast
with a single pyrenoid.
Ulva undergoes a very definite alternation of
generations. Biflagellate isogametes are formed by
certain cells of the haploid, gametangial plant. These
are liberated and fuse in pairs to form a diploid zygote
which germinates to form a separate diploid plant
called the sporophyte; this resembles the haploid
gametangial plant in outward appearance. Certain cells
of the sporophyte undergo meiosis and form zoospores
in sporangia; these zoospores are quite different to the
gametes in that they form quadriflagellate zoospores (with 4 flagella). These are released, swim
around for a time, settle and germinate to form the haploid gametangial thallus. Note that the
haploid gametes are capable of settling and
germinating without fusion to form a haploid
thallus directly; most Ulva populations reproduce
by this form of parthenogenesis and sexual
reproduction is not very common.
Ulva can be quite a nuisance in areas that are
nutrient enriched from sewage outfalls, where
populations of Ulva may cover large areas of
mudflats in the summer.
Ulva rigida
C. Agardh
Description: The thallus is laminar, pedunculated, with a thick and rigid base
provided with rhizoids. The margin was irregular and indented. Measures up to
30 cm high and 40 wide. The species is typically sessile, but may also be found
free. It can be found all year round, but reaches its greatest development in
the spring and summer. Lives on rocky and muddy bottoms, often in port
areas, polluted and shallow. It needs lots of light and nutrients and tolerate
large variations in temperature, salinity and solar radiation.
Classification:
Empire Eukaryota
Kingdom Plantae
Subkingdom Viridaeplantae
Phylum Chlorophyta
Class Ulvophyceae
Order Ulvales
Family Ulvaceae
Genus Ulva
Pictures:
Ulva rigida C.Agardh Spain, Galicia, Ría de A Coruña, 2009; TS
Publication details
Ulva rigida C.Agardh 1823: 410
Original publication: Agardh, C.A. (1823). Species algarum rite cognitae, cum synonymis,
differentiis specificis et descriptionibus succinctis. Volumen primum pars posterior. pp. [viiviii], [399]-531. Lundae [Lund]: ex officina Berlingiana.
Type species
The type species (holotype) of the genus Ulva is Ulva lactuca Linnaeus.
Status of name
This name is of an entity that is currently accepted taxonomically.
2
Origin of species name
Adjective (Latin), rigid (Stearn 1973).
Homotypic Synonym(s)
Phycoseris rigida (C.Agardh) Kützing 1843
Ulva lactuca var. rigida (C.Agardh) Le Jolis 1863
Heterotypic Synonym(s)
Phycoseris ulva Sonder 1845
Phycoseris gigantea var. perforata Kützing 1849
Ulva australis Areschoug 1854
Letterstedtia petiolata J.Agardh 1883
Ulva thuretii B.Föyn 1955
Ulva petiolata (J.Agardh) Womersley 1956
Ulva spathulata Papenfuss 1960
Ulva scandinavica Bliding 1969
Ulva armoricana P.Dion, B.de Reviers & G.Coat 1998
General environment
This is a marine species.
Type information
Type locality: Cádiz, Spain (Silva, Basson & Moe 1996: 750). Type: LD herb. alg. Agardh,
14449 (Ricker 1987: 41). Notes: Silva et al. recommend consulting Papenfuss (1960: 305) for
further information regarding the type locality of this species. The type locality was given as
Cape of Good Hope by Ricker (1987: 41) and he records that a lectotype has been selected by
R.B. Searles on 10 October 1975. Womersley (1984: 144) gives the herbarium no. 14294.
Detailed distribution with sources
(as Ulva rigida C.Agardh)
Arctic: Canada (Arctic) (Lee 1980).
Ireland: Antrim (Morton 1994), Cork (Guiry 1978), Donegal (Morton 2003), Down (Morton
1994), Galway (Loughnane et al. 2008), Wexford (Norton 1970, Guiry 1978, Loughnane et al.
2008).
Europe: Adriatic (Giaccone 1978, Munda 1979, Ercegović 1980, Gallardo et al. 1993, Curiel et
al.1998), Balearic Islands (Gómez Garreta 1983, Ribera Siguán 1983, Ribera Siguán & Gómez
Garreta 1985, Gallardo et al. 1993), Black Sea (Gallardo et al. 1993), Britain (Burrows 1991,
Hardy & Guiry 2003, Brodie et al. 2007), Bulgaria (Dimitrova-Konaklieva 1981), Faroes (Irvine
1982, Nielsen & Gunnarsson 2001), France (Feldmann 1937, Feldmann 1954, Gallardo et al.
3
1993, Verlaque 2001, Dizerbo & Herpe 2007, Loiseaux-de Goër & Noailles 2008), Greece
(Gerloff & Geissler 1974, Haritonidis & Tsekos 1976, Tsekos & Haritonidis 1977, Athanasiadis
1987, Gallardo et al. 1993), Iceland (Caram & Jónsson 1972), Ireland (Guiry 1978, Burrows
1991, Morton 1994), Italy (Giaccone 1969, Cinelli et al. 1976, Gallardo et al. 1993, Gallardo et
al. 1993, Sfriso 2010), Netherlands (Stegenga & Mol 1983, Stegenga, Kaaremans & Simons
2007), Portugal (Ardré 1970, Araujo et al. 2009, Araújo, Bárbara & Sousa-Pinto in press),
Romania (Caraus 2002), Spain (Ballesteros 1981, Gómez, Ribera & Romero 1981, Ballesteros
& Romero 1982, Pérez-Cirera & Maldonado 1982, Barcelo & Seoane 1982, Gallardo & PérezCirera 1982, Fernández & Niell 1982, Fernández, Niell & Anadón 1983, Boisset & Barceló 1984,
Sierra & Fernández 1984, Gallardo et al. 1985, Anadón & Fernández 1986, Rodriguez Prieto &
Polo Alberti 1988, Silva & Fernández 1988, Soto & Conde 1989, Pérez-Ruzafa 1990, Fernández
& Menéndez 1991, Granja, Cremades & Barbara 1992, Conde Poyales 1992, Gallardo et al.
1993, Flores-Moya et al. 1994, Flores-Moya et al. 1995, Bárbara & Cremades 1996, RodríguezPrieto & Polo, L. 1996, Rodriguez-Prieto et al. 1997, Veiga, Cremades & Bárbara 1998,
Rodriguez-Prieto & Polo Albertí 1998, Calvo & Bárbara 2002, Peña & Bárbara 2002, Valenzuela
Miranda 2002, Sánchez, Fernández & Rico 2003, Gorostiaga et al., 2004, Bárbara et al. 2004,
Hayden & Waaland 2004, Bárbara et al. 2005, Diaz-Tapia & Bárbara 2005, Cabello-Pasini &
Figueroa 2005, Sánchez & Fernández 2005, Pena & Bárbara 2008, Pérez-Ruzafa et al. 2008,
Viejo et al. 2008), Turkey (Europe) (Güner, Aysel, Sukatar & Öztürk 1985, Cirik, Zeybeck,
Aysel & Cirik 1990, Gallardo et al. 1993, Taskin et al. 2008).
Atlantic Islands: Azores (Neto 1994, Tittley & Neto 1994), Canary Islands (Gil-Rodríguez &
Afonso-Carrillo 1980, Sanson, Chacana & Gil-Rodriguez 1990, Febles et al. 1995, Guadalupe et
al. 1995, Lorenzo-Martín, Hernández-González & Gil-Rodriguez 1998, Febles, Arias, GilRodríguez, Hardisson & Sierra López 199?, Haroun et al. 2002, Aldanondo-Aristizábal,
Domínguez-Alvarez & Gil-Rodríguez 2003, Gil-Rodríguez et al. 2003, John et al. 2004,
Hernández-González et al. 2004a, Hernández-González et al. 2004b, Díaz-Villa et al 2005,
Domínguez-Alvarez et al. 2005), Cape Verde Islands (Otero-Schmitt & Sanjuan 1992, John et
al. 2004, Prud'homme van Reine, Haroun & Kostermans 2005), Madeira (Levring 1974, Neto,
Cravo & Haroun 2001, Haroun et al. 2002, John et al. 2004), Salvage Islands (Parente et al.
2000, John et al. 2004), Tristan da Cunha (Baardseth 1941).
North America: Alaska (Lindstrom 1977), California (Abbott & Hollenberg 1976, Stewart 1991),
Florida (Littler, Littler & Hanisak 2008), Georgia (Schneider & Searles 1991), Gulf of California
(Setchell & Gardner 1924, Dawson 1944), Mexico (Aguilar-Rosas et al. 2005), New Hampshire
(Hofman et al. 2010), North Carolina (Schneider & Searles 1991), Texas (Wynne 2009).
Central America: Baja California (Norris 2010), Belize (Littler & Littler 1997), México (Pacific)
(Pedroche et al. 2005).
4
Caribbean Islands: Caribbean (Littler & Littler 2000).
South America: Argentina (Boraso de Zaixso 2004), Chile (Santelices 1989, Ramírez &
Santelices 1991, Hoffmann & Santelices 1997, Hayden & Waaland 2004), Peru (Acleto 1973,
Ramírez & Santelices 1991), Venezuela (Ganesan 1990).
Africa: Algeria (Gallardo et al. 1993), Angola (John et al. 2004), Côte d'Ivoire (Lawson & John
1987, John, Lawson & Ameka, 2003, John et al. 2004), Egypt (Aleem 1993, Gallardo et al.
1993), Ghana (Lawson & John 1987, John, Lawson & Ameka, 2003, John et al. 2004), Kenya
(Silva, Basson & Moe 1996), Liberia (Lawson & John 1987, John, Lawson & Ameka, 2003, John
et al. 2004), Madagascar (Silva, Basson & Moe 1996), Mauritius (Silva, Basson & Moe 1996),
Morocco (Dangeard 1949, Gil-Rodriguez & Socorro Hernández 1986, Gallardo et al. 1993,
Benhissoune, Boudouresque & Verlaque 2001, Benhissoune, Boudouresque & Verlaque 2001),
Mozambique (Silva, Basson & Moe 1996), Namibia (Rull Lluch 2002, John et al. 2004), Senegal
(John et al. 2004), Sierra Leone (Lawson & John 1987, John, Lawson & Ameka, 2003, John et
al. 2004), Somalia (Silva, Basson & Moe 1996), South Africa (Silva, Basson & Moe 1996,
Stegenga, Bolton & Anderson 1997, Coppejans, Leliaert & Verbruggen 2005), Tanzania
(Oliveira, Österlund & Mtolera 2005), Tunisia (Meñez & Mathieson 1981, Ben Maiz,
Boudouresque & Quahchi 1987, Gallardo et al. 1993), Western Sahara (John et al. 2004).
Indian Ocean Islands: Aldabra Islands (Silva, Basson & Moe 1996), Laccadive Islands (Silva,
Basson & Moe 1996), Nicobar Islands (Silva, Basson & Moe 1996), Réunion (Silva, Basson &
Moe 1996), Seychelles (Silva, Basson & Moe 1996).
South-west Asia: India (Silva, Basson & Moe 1996, Sahoo et al. 2001), Israel (Hoffman 2004),
Kuwait (Silva, Basson & Moe 1996), Levant states (Gallardo et al. 1993), Oman (Wynne &
Jupp 1998), Pakistan (Abid et al. 2005), Southeast Arabian coast (Silva, Basson & Moe 1996),
Sri Lanka (Silva, Basson & Moe 1996, Coppejans et al. 2009), Turkey (Asia) (Taskin et al.
2008
, Percot, Yalcin, Aysel, Erdugan, Durral & Guven 2009), Yemen (Silva, Basson & Moe
1996).
South-east Asia: Philippines (Silva, Meñez & Moe 1987).
Australia and New Zealand: Lord Howe Island (Kraft 2000, Kraft 2007), New Zealand (Adams
1994, Heesch et al. 2009), Papua New Guinea (Coppejans et al. 2001), Queensland (Lewis
1987, Phillips 1997, Phillips 2002), South Australia (Womersley 1984), Victoria (Womersley
1984), Western Australia (Huisman & Walker 1990).
Pacific Islands: Hawaiian Islands (Abbott & Huisman, 2004).
5
Antarctic and the subantarctic islands: Antarctica (Papenfuss 1964), Macquarie Island (Ricker
1987).
(as Ulva australis Areschoug)
Australia and New Zealand: New South Wales (Womersley 1984), Queensland (Cribb 1996),
South Australia (Womersley 1984), Tasmania (Womersley 1984), Victoria (Womersley 1984,
Shepherd et al. 2009), Western Australia (Womersley 1984).
(as Ulva lactuca var. rigida (C.Agardh) Le Jolis)
Europe: Balearic Islands (Piccone 1889, Rodríguez y Femenías 1889, Seoane-Camba 1969),
Britain (Newton 1931), Romania (Caraus 2002), Spain (Sauvageau 1897, Seoane-Camba
1957, Fischer-Piette, C. & Seoane Camba, J. (1962), Seoane-Camba 1965).
Atlantic Islands: Canary Islands (Børgesen 1926).
North America: Florida (Taylor 1928, Dawes 1974).
South America: Brazil (Taylor 1930), Chile (Taylor 1939, Silva & Chacana 2005), Falkland
Islands (Taylor 1939).
Africa: Ethiopia (Papenfuss 1968).
South-west Asia: Sri Lanka (Børgesen 1936).
Australia and New Zealand: New Zealand (Chapman 1956).
(as Letterstedtia petiolata J.Agardh)
Australia and New Zealand: New Zealand (Chapman 1956).
(as Ulva spathulata Papenfuss)
Australia and New Zealand: New South Wales (Womersley 1984), New Zealand (Womersley
1984, Adams 1994), South Australia (Womersley 1984), Victoria (Womersley 1984), Western
Australia (Papenfuss 1960, Womersley 1984).
Antarctic and the subantarctic islands: Antarctica (Papenfuss 1964).
(as Ulva scandinavica Bliding)
Ireland: Cork (Loughnane et al. 2008).
Europe: Adriatic (Battelli & Tan 1998), Belgium (Coppejans 1995), Britain (Hayden & Waaland
2004, Loughnane et al. 2008), France (Coppejans 1995, Dizerbo & Herpe 2007), Netherlands
(Stegenga & Mol 1983), Norway (Rueness 1997), Portugal (Araujo et al. 2009, Araújo, Bárbara
6
& Sousa-Pinto in press), Spain (Bárbara & Cremades 1996, Calvo, Bárbara & Cremades 1999,
Calvo & Bárbara 2002, Peña & Bárbara 2002, Gorostiaga et al., 2004, Bárbara et al. 2005,
Diaz-Tapia & Bárbara 2005).
(as Ulva armoricana P.Dion, B.de Reviers & G.Coat)
Europe: France (Loiseaux-de Goër & Noailles 2008, Robic et al. 2009).
Australia and New Zealand: New Zealand (Heesch et al. 2009
).
Taxonomic notes
John et al. (2004) cite Ulva uncialis (Kütz.) Mont. as a synonym of this species.
Nomenclatural notes
Ricker (1987) gives as type locality “Cape of Good Hope, S. Africa.”
Key references
Bliding, C. (1969 '1968'). A critical survey of European taxa in Ulvales, Part II. Ulva, Ulvaria,
Monostroma, Kornmannia. Botaniska Notiser 121: 535-629, 47 figs.
Braune, W. (2008). Meeresalgen. Ein Farbbildführer zu den verbreiteten benthischen GrünBraun- und Rotalgen der Weltmeere. pp. [1]-596, 266 pls. Ruggell: A.R.G. Gantner Verlag.
Dawes, C.J. & Mathieson, A.C. (2008). The seaweeds of Florida. pp. [i]- viii, [1]-591, [592],
pls I-LI. Gainesville, Florida: University Press of Florida.
Hayden, H.S. & Waaland, J.R. (2004). A molecular systematic study of Ulva (Ulvaceae,
Ulvales) from the northeast Pacific. Phycologia 43: 364-382.
Kraft, G.T. (2007). Algae of Australia. Marine benthic algae of Lord Howe Island and the
southern Great Barrier Reef, 1. Green algae. pp. [i-iv], v-vi, 1-347, 110 text-figs; 11 pls.
Canberra & Melbourne: Australian Biological Resources Study & CSIRO Publishing.
Loiseaux-de Goër, S. & Noailles, M.-C. (2008). Algues de Roscoff. pp. [1]-215, col. figs.
Roscoff: Editions de la Station Biologique de Roscoff.
Loughnane, C.J., McIvor, L.M., Rindi, F., Stengel, D.B. & Guiry, M.D. (2008). Morphology, rbcL
phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and
southern Britain. Phycologia 47: 416-429.
Norris, J.N. (2010). Marine algae of the Northern Gulf of California: Chlorophyta and
Phaeophyceae. Smithsonian Contributions to Botany 94: i-x, 1-276.
7
Pedroche, F.F., Silva, P.C., Aguilar-Rosas, L.E., Dreckmann, K.M. & Aguilar-Rosas, R. (2005).
Catálogo de las algas marinas bentónicas del Pacífico de México. I. Chlorophycota. pp. i-viii,
17-146. Ensenada, México: Universidad Autónoma de Baja California.
Smith, G.M. (1944). Marine algae of the Monterey Peninsula. pp. i-ix, 1-622, 98 pls. Stanford:
Stanford University Press.
SAG Cultures
No records have been found on the SAG site.
NCBI Nucleotide Sequences
No sequences have been found on the NCBI site.
Created: 31 March 1996 by M.D. Guiry
Verified by: 26 March 2010 by M.D. Guiry
References
(Please note: only references with the binomials in the title are included. The information is
from the Literature database.)
Altamirano, M., Flores-Moya, A. & Figueroa, F.L. (2000). Long-term effects of natural sunlights
under various ultraviolet radiation conditions on growth and photosynthesis of intertidal Ulva
rigida (Chlorophyceae) cultivated in situ. Botanica Marina 43: 119-126, 5 figs.
Badini, L., Pistocchi, R. & Bagni, N. (1994). Polyamine transport in the seaweed Ulva rigida
(Chlorophyta). Journal of Phycology 30: 599-605, 6 figs, 2 tables.
Björk, M., Haglund, K., Ramazanov, Z., Garcia-Reina, G. & Pedersén, M. (1992). Inorganiccarbon assimilation in the green seaweed Ulva rigida C. Ag. (Chlorophyta). Planta 187: 152156, 3 figs, 1 table.
Björk, M., Gómez-Pinchetti, J., García-Reina, G. & Pedersén, M. (1992). Protoplast isolation
from Ulva rigida (Chlorophyta). British Phycological Journal 27: 401-407, 3 figs, 1 table.
Boubonari, T., Malea, P. & Kevrekidis, T. (2008). The green seaweed Ulva rigida as a
bioindicator of metals (Zn, Cu, Pb and Cd) in a low-salinity coastal environment. Botanica
Marina 51: 472-484.
Cabello-Pasini, A. & Figueroa, F.L. (2005). Effect of nitrate concentration on the relationship
between photosynthetic oxygen evolution and electron transport rate in Ulva rigida
(Chlorophyta). Journal of Phycology 41: 1169-1177.
Collén, J. & Pedersén, M. (1996). Production, scavenging and toxicity of hydrogen peroxide in
the green seaweed Ulva rigida. European Journal of Phycology 31: 265-271, 6 figs, 2 tables.
Corzo, A. & Niell, F.X. (1991). Determination of nitrate reductase activity in Ulva rigida C.
Agardh by the in situ method. J Exp Mer Biol Ecol 146: 181-191.
8
Cuomo, V., Perretti, A., Palomba, I., Verde, A. & Cuomo, A. (1995). Utilization of Ulva rigida
biomass in the Venice Lagoon (Italy): biotansformation in compost. Journal of Applied
Phycology 7: 479-485.
De Casabianca, M.-L. & Posada, F. (1998). Effect of environmental parameters on the growth
of Ulva rigida (Thau Lagoon, France). Botanica Marina 41: 157-165, 9 figs.
del Campo, E., García-Reina, G. & Correa, J.A. (1998). Degradative disease in Ulva rigida
(Chlorophyceae) associated with Acrochaete geniculata (Chlorophyceae). Journal of Phycology
34: 160-166, 22 figs.
Fillit, M. (1995). Seasonal changes in the photosynthetic capacities and pigment content of
Ulva rigida in a Mediterranean coastal lagoon. Botanica Marina 38: 271-280, 8 figs, 2 tables.
Fujita, R.M., Wheeler, P.A. & Edwards, R.L. (1988). Metabolic regulation of ammonium uptake
by Ulva rigida (Chlorophyta). Journal of Phycology 24: 560-566, 4 figs, 2 tables.
Gordillo, F.J.L., Figueroa, F.L. & Niell, F.X. (2003). Photon- and carbon use efficiency in Ulva
rigida at different CO2 and N levels. Planta 218: 315-322.
Jiménez del Rio, M., Ramazanov, Z. & García-Reina, G. (1996). Ulva rigida (Ulvales,
Chlorophyta) tank culture as biofilters for dissolved inorganic nitrogen from fishpond effluents.
Proceedings of the International Seaweed Symposium 15: 61-66.
Lavery, P.S. & Mccomb, A.J. (1991). The nutritional eco-physiology of Chaetomorpha linum
and Ulva rigida in Peel Inlet, western Australia. Botanica Marina 34: 251-260.
López-Figueroa, F. & Niell, F.X. (1989). A possible control by a phytochrome-like photoreceptor
of chlorophyll synthesis in the green alga Ulva rigida. Photochemistry and Photobiology 50:
263-266.
López-Figueroa, F. & Niell, F.X. (1989). Red-light and blue-light photoreceptors controlling
chlorophyll a synthesis in the red alga Porphyra umbilicalis and in the green alga Ulva rigida.
Physiologia Plantarum 76: 391-397.
López-Figueroa, F. & Rudiger, W. (1991). Stimulation of nitrate net uptake and reduction by
red and blue light and reversion by far-red light in the green alga Ulva rigida. Journal of
López-Figueroa, F. & Rüdiger, W. (1990). A possible control by phytochrome and other
photoreceptors of protein accumulation in the green alga Ulva rigida. Phytochemistry and
Phytobiology 52: 111-114.
Pérez-Cirera, J.L. & Gallardo, T. (1981). Notas sobre la vegetación bentónica del litoral de la
Península Ibérica. II. Ulva rigida C. Agardh var. fimbriata J. Agardh en las costas españolas: su
variabilidad morfológica y anatómica. Lazaroa 3: 227-233.
Phillips, J.A. (1990). Life history studies of Ulva rigida C. Ag. and Ulva stenophylla S. et G.
(Ulvaceae, Chlorophyta) in Southern Australia. Botanica Marina 33: 79-84.
Riccardi, N. & Solidoro, C. (1996). The influence of environmental variables onUlva rigida C.Ag.
Growth and production. Botanica Marina 39: 27-32.
Sfriso, A. (1995). Temporal and spatial responses of growth of Ulva rigida C. Ag. to
9
environmental and tissue concentrations of nutrients in the Lagoon of Venice. Botanica Marina
38: 557-573, 6 figs, 3 tables.
Sfriso, A. (2010). Coexistence of Ulva rigida and Ulva laetevirens (Ulvales, Chlorophyta) in
Venice Lagoon and other Italian transitional and marine environments. Botanica marina 53: 918.
Zanvondik, N. (1987). Seasonal variations in the rate of photosynthesis activity and chemical
composition of the littoral seaweeds Ulva rigida and Porphyra leucostica from the North
Adriatic. Botanica Marina 30: 71-82.
10
Ulva prolifera
O.F. Müller
(Enteromorpha prolifera (O.F.Müller) J.Agardh)
Classification:
Empire Eukaryota
Kingdom Plantae
Phylum Chlorophyta
Class Ulvophyceae
Order Ulvales
Family Ulvaceae
Genus Ulva
Publication details
Ulva prolifera O.F.Müller 1778: 7, pl. DCCLXIII: fig. 1
Original publication: Müller, O.F. (1778). Flroa danica. Vol. 5, fasc. 13 pp. 8, Plates 721-780.
Havniae [Copenhagen].
Type species
Status of name
Adjective (Latin), producing offsets, bearing progeny as offshoots (Stearn 1973).
Ulva enteromorpha f. prolifera (O.F.Müller) Van Heurck
Ulva compressa var. prolifera (O.F.Müller) C.Agardh 1823
Enteromorpha compressa var. prolifera (O.F.Müller) Greville 1830
Enteromorpha prolifera (O.F.Müller) J.Agardh 1883
Enteromorpha salina Kützing 1845
Enteromorpha salina var. polyclados Kützing 1845
Enteromorpha compressa var. trichodes Kützing 1845
Enteromorpha polyclados (Kützing) Kützing 1856
General environment
This is a Marine species.
11
Type information
Type locality: "U. p. tubulosa simplex teres, adultior compressiuscula. In fossa ad Nebbelund
Lalandiae" [Lolland, Denmark] Notes: Womersley (1984; 156, 157) reports that the type is
from Lolland, Denmark and that it has been lost. Lolland Island, Denmark (O'Kelly et al. 2010).
(as Ulva prolifera O.F.Müller)
Europe: Britain (Hayden & Waaland 2004, Brodie et al. 2007), Portugal (Araujo et al. 2009),
Slovenia (Rindi & Battelli 2005), Spain (Gorostiaga et al., 2004, Bárbara et al. 2005, DiazTapia & Bárbara 2005), Turkey (Europe) (Taskin et al. 2008).
Atlantic Islands: Canary Islands (John et al. 2004), Madeira (John et al. 2004).
North America: Alaska (Lindeberg & Lindstrom 2010), California (Hayden & Waaland 2004),
Florida (Littler, Littler & Hanisak 2008), Texas (Wynne 2009), Washington (Hayden & Waaland
2004).
Central America: México (Pacific) (Pedroche et al. 2005).
Caribbean Islands: Cuba (Suárez 2005).
Africa: Equatorial Guinea (John et al. 2004), Ghana (John et al. 2004), Mauritania (John et al.
2004), Namibia (John et al. 2004), Senegal (John et al. 2004, John et al. 2004), Western
Sahara (John et al. 2004).
South-west Asia: Israel (Hoffman 2004), Sri Lanka (Coppejans et al. 2009), Turkey (Asia)
(Taskin et al. 2008).
Australia and New Zealand: New Zealand (Heesch et al. 2009).
Pacific Islands: American Samoa (Skelton et al. 2004).
(as Enteromorpha salina Kützing)
Europe: Romania (Caraus 2002).
Atlantic Islands: Bermuda (Taylor 1960).
North America: Florida (Taylor 1928, Taylor 1960), Louisiana (Taylor 1960).
Caribbean Islands: Bahamas (Taylor 1960).
South America: Chile (Ramírez & Santelices 1991).
12
Pacific Islands: Easter Island (Santelices & Abbott 1987).
(as Enteromorpha salina var. polyclados Kützing)
North America: Florida (Taylor 1928, Dawes 1974).
South America: Galápagos Islands (Taylor 1945).
(as Enteromorpha prolifera (O.F.Müller) J.Agardh)
Ireland: Antrim (Guiry 1978, Morton 1994), Clare (Pybus 1977, Guiry 1978, De Valéra et al.
1979), Cork (Guiry 1978), Derry (Morton 1994), Down (Guiry 1978, Morton 1994), Galway
(Pybus 1977, Guiry 1978), Mayo (Cotton 1912, Guiry 1978), Wexford (Norton 1970, Guiry
1978).
Europe: Adriatic (Giaccone 1978, Munda 1979, Gallardo et al. 1993), Balearic Islands (Ribera
Siguán 1983, Ribera Siguán & Gómez Garreta 1985, Gallardo et al. 1993), Baltic Sea (Nielsen
et al. 1995), Black Sea (Gallardo et al. 1993), Britain (Newton 1931, Burrows 1991, Hardy &
Guiry 2003), Bulgaria (Dimitrova-Konaklieva 1981), Corsica (Gallardo et al. 1993), Denmark
(Larsen & Sand-Jensen 2006), E. Greenland (Lund 1959, Pedersen 1976), Faroes (Irvine 1982,
Nielsen & Gunnarsson 2001), France (Feldmann 1954, Gallardo et al. 1993, Coppejans 1995,
Verlaque 2001, Dizerbo & Herpe 2007), Greece (Gerloff & Geissler 1974, Athanasiadis 1987,
Gallardo et al. 1993), Helgoland (Bartsch & Kuhlenkamp 2000), Iceland (Caram & Jónsson
1972), Ireland (Cotton 1912, Pybus 1977, Guiry 1978, De Valéra et al. 1979, Burrows 1991,
Morton 1994), Italy (Edwards et al. 1975, Gallardo et al. 1993, Gallardo et al. 1993, Cecere et
al. 1996, Furnari, Cormaci & Serio 1999, Rindi, Sartoni & Cinelli 2002), Netherlands (Stegenga
& Mol 1983, Stegenga, Kaaremans & Simons 2007), Portugal (Ardré 1970), Romania (Caraus
2002), Spain (Miranda 1931, Miranda 1934, Fischer-Piette, C. & Seoane Camba, J. (1962),
Seoane-Camba 1965, Ballesteros & Romero 1982, Gallardo & Pérez-Cirera 1982, Ballesteros
1983, Gallardo et al. 1985, Alvárez Cobelas & Gallardo 1986, Soto & Conde 1989, PérezRuzafa 1990, Conde, Flores-Moya & Vera 1990, Granja, Cremades & Barbara 1992, Gallardo et
al. 1993, Flores-Moya et al. 1994, Flores-Moya et al. 1995, Bárbara & Cremades 1996,
Rodriguez-Prieto et al. 1997, Veiga, Cremades & Bárbara 1998, Cambra Sánchez, Álvarez
Cobelas & Aboal Sanjurjo 1998, Calvo & Bárbara 2002, Peña & Bárbara 2002), Spitsbergen
(Vinogradova 1995), Sweden (Kylin 1949), Turkey (Europe) (Güven & Öztig 1971, Gallardo et
al. 1993).
Atlantic Islands: Azores (Neto 1994, Tittley & Neto 1994), Bermuda (Taylor 1957, Taylor
1960), Canary Islands (Gil-Rodríguez & Afonso-Carrillo 1980, Haroun et al. 2002, GilRodríguez et al. 2003), Madeira (Levring 1974, Neto, Cravo & Haroun 2001, Haroun et al.
2002), Tristan da Cunha (Baardseth 1941).
13
North America: Alaska (Lindstrom 1977, Scagel et al. 1989), British Columbia (Scagel et al.
1989), California (Abbott & Hollenberg 1976, Silva 1979), Florida (Taylor 1928, Taylor 1960,
Dawes 1974), Georgia (Schneider & Searles 1991), Gulf of California (Setchell & Gardner
1924, Dawson 1944), Maine (Mathieson et al. 2001), New Hampshire (Mathieson & Hehre
1986), North Carolina (Taylor 1960, Schneider & Searles 1991), Oregon (Hansen 1997),
Quebec (Taylor 1957), South Carolina (Taylor 1957, Taylor 1960, Schneider & Searles 1991),
Texas (Taylor 1960), Virginia (Humm 1979), Washington (Scagel et al. 1989).
Central America: Panama (Wysor 2004).
Caribbean Islands: Barbados (Taylor 1960), Caribbean (Littler & Littler 2000), Cuba (Taylor
1960), Jamaica (Taylor 1960), Lesser Antilles (Taylor 1960).
South America: Argentina (Boraso de Zaixso 2004), Brazil (Taylor 1930, Taylor 1960), Chile
(Santelices 1989, Ramírez & Santelices 1991), Peru (Ramírez & Santelices 1991), Uruguay
(Coll & Oliveira 1999), Venezuela (Taylor 1960, Ganesan 1990).
Africa: Egypt (Aleem 1993), Equatorial Guinea (John, Lawson & Ameka, 2003), Ghana (Lawson
& John 1987, John, Lawson & Ameka, 2003), Mauritius (Silva, Basson & Moe 1996), Morocco
(Gallardo et al. 1993, Benhissoune, Boudouresque & Verlaque 2001, Benhissoune,
Boudouresque & Verlaque 2001), Mozambique (Silva, Basson & Moe 1996), Namibia (Rull
Lluch 2002), South Africa (Silva, Basson & Moe 1996, Stegenga, Bolton & Anderson 1997),
Tanzania (Silva, Basson & Moe 1996), Tunisia (Meñez & Mathieson 1981, Ben Maiz,
Boudouresque & Quahchi 1987, Gallardo et al. 1993).
Indian Ocean Islands: Laccadive Islands (Silva, Basson & Moe 1996), Maldives (Silva, Basson
& Moe 1996), Réunion (Silva, Basson & Moe 1996).
South-west Asia: Bangladesh (Silva, Basson & Moe 1996), India (Silva, Basson & Moe 1996,
Sahoo et al. 2001), Iraq (Silva, Basson & Moe 1996), Israel (Einav 2007), Kuwait (Silva,
Basson & Moe 1996), Levant states (Gallardo et al. 1993), Pakistan (Silva, Basson & Moe
1996), Sri Lanka (Silva, Basson & Moe 1996).
Asia: China (Tseng 1984), Commander Islands (Selivanova & Zhigadlova 1997), Japan
(Yoshida, Nakajima & Nakata 1990, Yoshida 1998, Hiraoka 2003), Korea (Lee & Kang 2001,
Lee 2008), Russia (Kozhenkova 2009), Taiwan (Huang 2000).
South-east Asia: Indonesia (Silva, Basson & Moe 1996), Philippines (Silva, Meñez & Moe
1987), Vietnam (Tsutsui et al. 2005).
14
Australia and New Zealand: New Zealand (Adams 1994, Nelson & Phillips 1996), Queensland
(Phillips 1997, Phillips 2002), South Australia (Womersley 1984), Tasmania (Womersley 1984),
Victoria (Womersley 1984).
Pacific Islands: Federated States of Micronesia (Lobban & Tsuda 2003), Fiji (N'Yeurt, South &
Keats 1996, South & Skelton 2003), Hawaiian Islands (Abbott & Huisman, 2004), Samoan
Archipelago (Skelton & South 1999).
Taxonomic notes
John et al. (2004) cite Enteromorpha torta (Mert.) Reinb. as a synonym of this species.
Key references
Brodie, J., Maggs, C.A. & John, D.M. (2007). Green seaweeds of Britain and Ireland. pp. [i-v],
vi-xii, 1-242, 101 figs. London: British Phycological Society.
Leliaert F., Zhang X., Ye N., Malta E.J., Engelen A.E., Mineur F., Verbruggen H. & De Clerck O.
(2009). Identity of the Qingdao algal bloom. Phycological Research 57: 147-151.
Lindeberg, M.R. & Lindstrom, S.C. (2010). Field guide to the seaweeds of Alaska. pp. [i-]iii-iv,
1-188, numerous col. photographs. Fairbanks: Alaska Sea Grant College Program.
SAG Cultures
Created: 27 October 1998 by M.D. Guiry
Verified by: 27 October 2010 by M.D. Guiry
15
Ulva intestinalis
Linnaeus
(Enteromorpha intestinalis (Linnaeus) Nees)
Classification:
Empire Eukaryota
Kingdom Plantae
Phylum Chlorophyta
Class Ulvophyceae
Order Ulvales
Family Ulvaceae
Genus Ulva
Pictures:
Spiddal, Co. Galway, Ireland; plants in extreme high-shore pools; polaroid filter. 24 Sep 2006.
Michael Guiry. © Michael Guiry.
Sotogawa-cho, Choshi, Chiba Prefecture, Japan. Courtesy Chiba University.
Sotogawa-cho, Choshi, Chiba Prefecture, Japan. Courtesy Chiba University.
16
Spiddal, Co. Galway, Ireland; upper-shore pool; plants to about 60 mm long. 26 Mar 2005. Michael
Guiry. © Michael Guiry.
Ulva intestinalis at the Suva market. 16 Aug 2003. Peter Skelton. © ORDA.
KwaZulu-Natal. O. Dargent. © O. Dargent. From: De Clerck, O., Bolton, J.J., Anderson, R.J. &
Coppejans, E. (2005). Guide to the seaweeds of KwaZulu-Natal. Scripta Botanica Belgica 33: 1-294.
Purchase information.
© ABC Taxa. From: Coppejans, E., Leliaert, F., Dargent, O., Gunasekara, R., & De Clerck, O.
(2009). Sri Lankan Seaweeds Methodologies and field guide to the dominant species. Vol. 6 pp. 1265.: ABC Taxa..
Spain, Galicia, Ría de Ortigueira, 1999. Ignacio Bárbara. © Ignacio Bárbara.
17
Carna, Co. Galway, Ireland. Alex Dufort. © Alex Dufort.
Groton, Connecticut, USA; mid intertidal pools. 13 Sep 2007. Courtnay Hermann. © Courtnay
Hermann.
Ulva intestinalis Linnaeus Spiddal, Co. Galway, Ireland; upper-shore pool; plants to about 60 mm long
Publication details
Ulva intestinalis Linnaeus 1753: 1163
Original publication: Linnaeus, C. (1753). Species plantarum, exhibentes plantas rite cognitas,
ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis
natalibus, secundum systema sexuale digestas. Vol. 2 pp. [i], 561-1200, [1-30, index], [i,
err.]. Holmiae [Stockholm]: Impensis Laurentii Salvii.
Type species
Status of name
18
Adjective (Latin), relating to or found in the intestines (Stearn 1973).
Conferva intestinalis (Linnaeus) Roth 1797
Tetraspora intestinalis (Linnaeus) Desvaux 1818
Scytosiphon intestinalis (Linnaeus) Lyngbye 1819
Enteromorpha intestinalis (Linnaeus) Nees 1820
Fistularia intestinalis (Linnaeus) Greville 1824
Solenia intestinalis (Linnaeus) C.Agardh 1824
Ilea intestinalis (Linnaeus) Leiblein 1827
Hydrosolen intestinalis (Linnaeus) Martius 1833
Ulva enteromorpha var. intestinalis (Linnaeus) Le Jolis 1863
Ulva bulbosa var. intestinalis (Linnaeus) Hariot 1889
Enteromorpha compressa var. intestinalis (Linnaeus) Hamel 1931
Scytosiphon intestinalis var. nematodes Wallroth 1833
Enteronia simplex Chevallier 1836
Enteromorpha vulgaris var. lacustris Edmondston 1845
Enteromorpha intestinalis f. maxima J.Agardh 1883
Enteromorpha intestinalis var. maxima (J.Agardh) Lily Newton 1931
General environment
This is a Marine species.
Type information
Type locality: Woolwich, London, England? (Hayden et al. 2003: 289). Lectotype: Dillenius
(1742: pl. 9: fig. 7) (epitype) OXF (Yoshida 1998 Notes: Blomster et al. (1999) select a
lectotype (epitype) of Dillenius (1742: pl. 9: fig. 7); see also Hayden et al. (2003: 289). Type
locality: 'in Mari omni' (South & Skelton, 2003).
(as Ulva intestinalis Linnaeus)
Ireland: Wexford (Tighe 1803).
Europe: Balearic Islands (Weyler 1854), Britain (Hayden & Waaland 2004, Brodie et al. 2007),
France (Loiseaux-de Goër & Noailles 2008), Ireland (Tighe 1803), Portugal (Araujo et al. 2009,
Araújo, Bárbara & Sousa-Pinto in press), Spain (Gorostiaga et al., 2004, Bárbara et al. 2005,
Pérez-Ruzafa et al. 2008, Viejo et al. 2008, de los Santos, Pérez-Lloréns & Vergara 2009,
Mercado et al. 2009), Turkey (Europe) (Taskin et al. 2008).
19
Atlantic Islands: Ascension (John et al. 2004), Cape Verde Islands (John et al. 2004), Madeira
(John et al. 2004), Salvage Islands (John et al. 2004).
North America: Alaska (Hayden & Waaland 2004, Lindeberg & Lindstrom 2010), British
Columbia (Hayden & Waaland 2004), California (Hayden & Waaland 2004), Connecticut (Van
Patten 2009), Florida (Littler, Littler & Hanisak 2008), Texas (Wynne 2009).
Central America: Baja California (Norris 2010), México (Pacific) (Pedroche et al. 2005).
Africa: Eritrea (Ateweberhan & Prud'homme van Reine 2005), Ghana (John et al. 2004),
Guinea-Bissau (John et al. 2004), Namibia (John et al. 2004), South Africa (Coppejans,
Leliaert & Verbruggen 2005).
South-west Asia: Abu Dhabi (John, D.M.), Israel (Hoffman 2004), Pakistan (Shahnaz &
Shameel 2007), Sri Lanka (Coppejans et al. 2009), Turkey (Asia) (Taskin et al. 2008
).
Australia and New Zealand: New Zealand (Taylor et al 2006, Taylor et al 2006, Heesch et al.
2009).
Pacific Islands: American Samoa (Skelton et al. 2004).
(as Enteromorpha intestinalis (Linnaeus) Nees)
Arctic: Canada (Arctic) (Taylor 1957, Lee 1980).
Ireland: Antrim (Adams 1907, Guiry 1978, McMillan & Morton 1979, Morton 1994), Clare
(Pybus 1977, Guiry 1978, De Valéra et al. 1979), Cork (Renouf 1931, Cullinane 1971, Guiry
1978), Derry (Guiry 1978, Morton 1994), Donegal (Guiry 1978, Morton 2003), Down (Guiry
1978, Morton 1994), Dublin (Sanders 1860, Guiry 1978), Galway (Pybus 1977, Guiry 1978),
Kerry (Guiry 1978), Leitrim (Cullinane 1970, Guiry 1978), Limerick (Cullinane 1969, Guiry
1978), Mayo (Cotton 1912, Guiry 1978), Waterford (Guiry 1977), Wexford (Cotton 1913,
Norton 1970, Guiry 1978).
Europe: Adriatic (Giaccone 1978, Munda 1979, Ercegović 1980, Gallardo et al. 1993), Balearic
Islands (Colmeiro, M. 1868, Navarro & Bellón 1945, Gómez Garreta 1983, Ribera Siguán 1983,
Ribera Siguán & Gómez Garreta 1985, Gallardo et al. 1993, Cambra Sánchez, Álvarez Cobelas
& Aboal Sanjurjo 1998), Baltic Sea (Nielsen et al. 1995), Belgium (Coppejans 1995), Black Sea
(Gallardo et al. 1993), Britain (Newton 1931, Burrows 1991, Hardy & Guiry 2003), Bulgaria
(Dimitrova-Konaklieva 1981), Corsica (Gallardo et al. 1993), Denmark (Larsen & Sand-Jensen
2006), E. Greenland (Pedersen 1976), Faroes (Irvine 1982, Nielsen & Gunnarsson 2001),
France (Feldmann 1937, Feldmann 1954, Ben Maiz, Boudouresque, Lauret & Riouall 1988,
Gallardo et al. 1993, Coppejans 1995, Verlaque 2001), Greece (Gerloff & Geissler 1974,
20
Haritonidis & Tsekos 1976, Tsekos & Haritonidis 1977, Athanasiadis 1987, Gallardo et al.
1993), Helgoland (Bartsch & Kuhlenkamp 2000), Iceland (Caram & Jónsson 1972), Ireland
(Adams 1907, Cotton 1912, Cotton 1913, Cullinane 1969, Cullinane 1971, Guiry 1977, Guiry
1978, De Valéra et al. 1979, Burrows 1991, Morton 1994), Italy (Giaccone 1969, Edwards et
al. 1975, Cinelli et al. 1976, Gallardo et al. 1993, Gallardo et al. 1993, Cecere et al. 1996,
Furnari, Cormaci & Serio 1999, Rindi, Sartoni & Cinelli 2002), Malta (Cormaci et al. 1997),
Netherlands (Stegenga & Mol 1983, Stegenga, Kaaremans & Simons 2007), Portugal (Ardré
1970, Araújo et al., 2003), Romania (Caraus 2002), Spain (Lázaro Ibiza 1889, Sauvageau
1897, Hamel 1928, Miranda 1931, Bellón 1942, González Guerrero 1957, Seoane-Camba
1957, Ardré 1957, González Guerrero 1957, Seoane-Camba 1965, Ballesteros 1981,
Ballesteros & Romero 1982, Pérez-Cirera & Maldonado 1982, Barcelo & Seoane 1982, Gallardo
& Pérez-Cirera 1982, Fernández & Niell 1982, Anadón 1983, Aboal & Llimona 1984a, PérezRuzafa & Honrubia 1984, Gallardo et al. 1985, Alvárez Cobelas & Gallardo 1986, Aboal 1988b,
Rodriguez Prieto & Polo Alberti 1988, Soto & Conde 1989, Pérez-Ruzafa 1990, Granja,
Cremades & Barbara 1992, Gallardo et al. 1993, Aboal et al. 1994, Flores-Moya et al. 1994,
Flores-Moya et al. 1995, Bárbara & Cremades 1996, Veiga, Cremades & Bárbara 1998, Cambra
Sánchez, Álvarez Cobelas & Aboal Sanjurjo 1998, Calvo, Bárbara & Cremades 1999, Veiga
Villar 1999, Cantoral Uiza & Aboal Sanjurjo 2001, Moreno et al. 2001, Calvo & Bárbara 2002,
Peña & Bárbara 2002, Pérez-Lorens et al. 2004), Sweden (Kylin 1907, Kylin 1949), Turkey
(Europe) (Güven & Öztig 1971, Güner, Aysel, Sukatar & Öztürk 1985, Cirik, Zeybeck, Aysel &
Cirik 1990, Gallardo et al. 1993).
1960), Canary Islands (Børgesen 1926, Gil-Rodríguez & Afonso-Carrillo 1980, Viera-Rodriguez
et al. 1987, Guadalupe et al. 1995, Haroun et al. 2002, Aldanondo-Aristizábal, DomínguezAlvarez & Gil-Rodríguez 2003, Gil-Rodríguez et al. 2003), Cape Verde Islands (John, Lawson &
Ameka, 2003, Prud'homme van Reine, Haroun & Kostermans 2005), Madeira (Neto, Cravo &
Haroun 2001), Salvage Islands (Audiffred & Weisscher 1984, Parente et al. 2000, Hardy &
Guiry 2003), Tristan da Cunha (Baardseth 1941).
North America: Alaska (Lindstrom 1977, Scagel et al. 1989, Mondragon & Mondragon 2003),
British Columbia (Scagel et al. 1989), California (Abbott & Hollenberg 1976, Silva 1979, Cohen
& Fong 2005), Florida (Taylor 1957, Dawes 1974), Gulf of California (Dawson 1944), Maine
(Mathieson et al. 2001), Mexico (Mondragon & Mondragon 2003), New Hampshire (Mathieson
& Hehre 1986), North Carolina (Taylor 1957, Taylor 1960, Schneider & Searles 1991), Oregon
(Hansen 1997), Quebec (Taylor 1957), Texas (Taylor 1960), Virginia (Humm 1979),
Washington (Scagel et al. 1989).
Caribbean Islands: Caribbean (Littler & Littler 2000), Cuba (Comas González 2008), Jamaica
(Taylor 1960), Lesser Antilles (Taylor 1960), Puerto Rico (Taylor 1960).
21
South America: Argentina (Boraso de Zaixso 2004), Brazil (Taylor 1930, Taylor 1960), Chile
(Santelices 1989, Ramírez & Santelices 1991, Hoffmann & Santelices 1997), Peru (Ramírez &
Santelices 1991), Uruguay (Taylor 1939, Coll & Oliveira 1999), Venezuela (Ganesan 1990).
Africa: Algeria (Gallardo et al. 1993), Egypt (Papenfuss 1968, Mohsen, Kharboush, Khaleafa,
Metwalli & Azab 1975, Aleem 1993, Gallardo et al. 1993), Ghana (Lawson & John 1987, John,
Lawson & Ameka, 2003), Guinea-Bissau (Welten, Audiffred & Prud'homme van Reine 2002,
Welten, Audiffred & Prud'homme van Reine 2002, John, Lawson & Ameka, 2003), Libya
(Gallardo et al. 1993), Morocco (Dangeard 1949, Gil-Rodriguez & Socorro Hernández 1986,
Gallardo et al. 1993, Benhissoune, Boudouresque & Verlaque 2001, Benhissoune,
Boudouresque & Verlaque 2001), Namibia (Rull Lluch 2002), South Africa (Silva, Basson & Moe
1996, Stegenga, Bolton & Anderson 1997), Tunisia (Meñez & Mathieson 1981, Ben Maiz,
Boudouresque & Quahchi 1987, Gallardo et al. 1993).
Indian Ocean Islands: Andaman Islands (Silva, Basson & Moe 1996), Laccadive Islands (Silva,
Basson & Moe 1996), Rodrigues Island (Silva, Basson & Moe 1996), Seychelles (Silva, Basson
& Moe 1996).
South-west Asia: Bahrain (Silva, Basson & Moe 1996), Bangladesh (Silva, Basson & Moe
1996), India (Silva, Basson & Moe 1996, Sahoo et al. 2001), Israel (Einav 2007), Kuwait
(Silva, Basson & Moe 1996), Levant states (Gallardo et al. 1993), Pakistan (Silva, Basson &
Moe 1996), Sri Lanka (Silva, Basson & Moe 1996), Yemen (Silva, Basson & Moe 1996).
Asia: China (Tseng 1984, Hu & Wei 2006), Japan (Yoshida, Nakajima & Nakata 1990, Yoshida
1998), Korea (Lee & Kang 2001, Lee 2008), Taiwan (Huang 2000).
South-east Asia: Indonesia (Verheij & Prud'homme van Reine 1993, Silva, Basson & Moe
1996), Malaysia (Silva, Basson & Moe 1996), Philippines (Silva, Meñez & Moe 1987), Singapore
(Teo & Wee 1983, Silva, Basson & Moe 1996), Vietnam (Pham-Hoàng 1969).
Australia and New Zealand: New Zealand (Adams 1994, Adams 1997), Papua New Guinea
(Coppejans et al. 2001), Queensland (Lewis 1987, Day et al. 1995, Phillips 1997, Phillips
2002), South Australia (Womersley 1984), Tasmania (Womersley 1984), Victoria (Day et al.
1995).
Pacific Islands: Easter Island (Santelices & Abbott 1987), Federated States of Micronesia
(Lobban & Tsuda 2003), Fiji (N'Yeurt, South & Keats 1996, South & Skelton 2003), Hawaiian
Islands (Abbott & Huisman, 2004, Sherwood 2004), Samoan Archipelago (Skelton & South
1999).
22
Antarctic and the subantarctic islands: Antarctica (Papenfuss 1964), Macquarie Island (Ricker
1987), South Shetland Islands (Wiencke & Clayton 2002).
(as Enteromorpha intestinalis f. maxima J.Agardh)
Europe: Britain (Newton 1931).
North America: Alaska (Lindstrom 1977).
(as Enteromorpha compressa var. intestinalis (Linnaeus) Hamel)
Europe: France (Coppejans 1972).
Key references
Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J. & Waaland, J.R. (2003).
Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. European Journal
of Phycology 38: 277-294.
Lindeberg, M.R. & Lindstrom, S.C. (2010). Field guide to the seaweeds of Alaska. pp. [i-]iii-iv,
1-188, numerous col. photographs. Fairbanks: Alaska Sea Grant College Program.
Loiseaux-de Goër, S. & Noailles, M.-C. (2008). Algues de Roscoff. pp. [1]-215, col. figs.
Roscoff: Editions de la Station Biologique de Roscoff.
23
Skelton, P.A. & South, G.R. (2007). The benthic marine algae of the Samoan Archipelago,
South Pacific, with emphasis on the Apia District. Nova Hedwigia Beihefte 132: 1-350.
SAG Cultures
Created: 19 October 1998 by M.D. Guiry
Verified by: 27 October 2010 by M.D. Guiry
References
Barr, N.G., Tijsen, R.J. & Rees, T.A.V. (2004). Contrasting effects of methionine sulfoximine on
uptake and assimiliation of ammonium in Ulva intestinalis (Chlorophyceae). Journal of
Björnsäter, B.R. & Wheeler, P.A. (1983). Effect of nitrogen and phosphorus supply on growth
and tissue composition of Ulva fenestrata and Enteromorpha intestinalis (Ulvales,
Chlorophyta). Journal of Phycology 26: 603-611.
Björnsäter, B.R. & Wheeler, P.A. (1990). Effect of nitrogen and phosphorus supply on growth
and tissue composition of Ulva fenestrata and Enteromrpha intestinalis (Ulvales, Chlorophyta).
Journal of Phycology 26: 603-611, 5 figs, 4 tables.
Kostamo, K., Blomster, J., Korpelainen, H., Kelly, J., Maggs, C.A. & Mineur, F. (2008). New
microsatellite markers for Ulva intestinalis (Chlorophyta) and the transferability of markers
across species Ulvaceae. Phycologia 47: 580-587.
Taylor, M.W., Barr, N.G., Grant, C.M. & Rees, T.A.V. (2006). Changes in amino acid
composition of Ulva intestinalis (Chlorophyceae) following addition of ammonium or nitrate.
Phycologia 45: 270-276.
24
Ulva laetevirens Areschoug
Description: The species has a leaf-like thallus slightly pedunculated, palmate or lobed and
margin without indentations. Can reach widths of 40 cm. It lives in shallow waters and
polluted. Reaches its maximum development in the spring and summer.
Classification:
Empire Eukaryota
Kingdom Plantae
Phylum Chlorophyta
Class Ulvophyceae
Order Ulvales
Family Ulvaceae
Genus Ulva
Pictures:
Photo Cinelli F., Augusta (SR), Italy
25
Photo Cinelli F., Augusta (SR), Italy (U. laetevirens + U. intestinalis)
Photo Cinelli F., Augusta (SR), Italy (U. laetevirens + U. intestinalis)
Publication details
Ulva laetevirens Areschoug 1854: 370
Original publication: Areschoug, J.E. (1854). Phyceae novae et minus cognitae in maribus
extraeuropaeis collectae. Nova Acta Regiae Societatis Scientiarum Upsaliensis, ser. 3 1: 329372.
Type species
Status of name
26
Participle (Latin), light green (Stearn 1973).
Gemina linzoidea V.J.Chapman 1952
General environment
Type information
Type locality: In sinu Port Phillip, South Australia [Port Phillip, Victoria, Australia] (Areschoug
1854: 370).
(as Ulva laetevirens Areschoug)
Europe: Italy (Furnari, Cormaci & Serio 1999, Rindi, Sartoni & Cinelli 2002, Sfriso 2010),
Slovenia (Rindi & Battelli 2005).
South-west Asia: Israel (Einav 2007).
Australia and New Zealand: Western Australia (Silva, Basson & Moe 1996, Huisman &
Borowitzka 2003).
Key references
Adams, N.M. (1994). Seaweeds of New Zealand. An Illustrated Guide. pp. [1-7], 8-360, 116
pls. Christchurch: Canterbury University Press.
SAG Cultures
Created: 11 July 1998 by M.D. Guiry
Verified by: 13 February 2010 by M.D. Guiry
References
27
Sfriso, A. (2010). Coexistence of Ulva rigida and Ulva laetevirens (Ulvales, Chlorophyta) in
Venice Lagoon and other Italian transitional and marine environments. Botanica marina 53: 918.
28
Chaetomorpha linum
(O.F.Müller) Kützing
Classification:
Empire Eukaryota
Kingdom Plantae
Phylum Chlorophyta
Class Ulvophyceae
Order Cladophorales
Family Cladophoraceae
Genus Chaetomorpha
Pictures:
29
From Littler, D.S., M.M. Littler & M.D. Hanisak (2008) Submersed Plants of the Indian River Lagoon.
Purchase information. Diane Littler. © Diane Littler.
Mar Piccolo, Taranto, Italy. Ginnani Felicini. © Ginnani Felicini.
Schilksee, Kiel Bight, Baltic Sea, 2m depth. 06 Dec 2004. Dirk Schories. © dirk.schories@gmx.de.
30
Chaetomorpha linum (O.F.Müller) Kützing Schilksee, Kiel Bight, Baltic Sea, 2m depth
Publication details
Chaetomorpha linum (O.F.Müller) Kützing 1845: 204
Original publication: Kützing, F.T. (1845). Phycologia germanica, d. i. Deutschlands Algen in
bündigen Beschreibungen. Nebst einer Anleitung zum Untersuchen und Bestimmen dieser
Gewächse für Anfänger. pp. i-x, 1-340. Nordhausen: W. Köhne.
Type species
This is the type species (lectotype) of the genus Chaetomorpha.
Status of name
Basionym
Conferva linum O.F.Müller
Type information
Type locality: Nakskov Fjord, Lolland, Denmark (Lipkin & Silva 2002: 55). Notes: According to
Womersley (1984: 176) the type is from Lolland, Denmark and is probably lost. Syntypes:
Nakskov and Rødby, Denmark (Silva et al. 1996). Nakskov is in the Lolland municipality in
Region Sjælland on the western coast of the island of Lolland in south Denmark. Rødby is a
town and a former municipality (Danish, kommune) also on the island of Lolland.
Adjective (Latin), flax (Lewis & Short 1890).
Conferva linum O.F.Müller 1778
Lychaete linum (O.F.Müller)
Areschoug 1851
31
Chaetomorpha sutoria Rabenhorst
Chaetomorpha baltica Kützing
Chaetomorpha surtoria (Berkeley) Kornmann
Chaetomorpha linum f. aerea (Dillwyn) F.S.Collins
Conferva linoides S.F.Gray 1821
Conferva linoides C.Agardh 1822
Conferva crassa C.Agardh 1824
Conferva rigida C.Agardh 1824
Chaetomorpha crassa (C.Agardh) Kützing 1845
Chaetomorpha rigida Kützing 1845
Conferva chlorotica Montagne 1846
Chaetomorpha linoides Kützing 1847
Chaetomorpha chlorotica (Montagne) Kützing 1849
General environment
(as Chaetomorpha surtoria (Berkeley) Kornmann)
Europe: Baltic Sea (Nielsen et al. 1995).
(as Chaetomorpha linum f. aerea (Dillwyn) F.S.Collins)
South America: Brazil (Taylor 1930).
(as Chaetomorpha linum (O.F.Müller) Kützing)
Ireland: Antrim (Morton 1994), Clare (Maggs 1983), Cork (Cullinane 1971, Guiry 1978), Derry
(Morton 1994), Donegal (Morton 2003), Down (Morton 1994), Galway (Guiry 1978, De Valéra
et al. 1979, Maggs 1983), Limerick (Cullinane 1969, Guiry 1978), Louth (Synnott 1969, Guiry
1978), Mayo (Cotton 1912, Guiry 1978), Wexford (Parkes & Scannell 1969, Norton 1970, Guiry
1978).
Europe: Adriatic (Giaccone 1978, Ercegović 1980, Gallardo et al. 1993), Balearic Islands
(Piccone 1889, Rodríguez y Femenías 1889, Navarro & Bellón 1945, Ribera Siguán 1983,
Ribera Siguán & Gómez Garreta 1985, Gallardo et al. 1993, Ribera, Coloreu, Rodriguez Prieto
& Ballesteros 1997, Ribera, Coloreu, Rodriguez Prieto & Ballesteros 1997, Cambra Sánchez,
Álvarez Cobelas & Aboal Sanjurjo 1998), Baltic Sea (Nielsen et al. 1995), Black Sea (Gallardo
et al. 1993), Britain (Newton 1931, Patel 1971, Burrows 1991, John 2002, Hardy & Guiry
2003, Brodie et al. 2007), Bulgaria (Dimitrova-Konaklieva 1981), Corsica (Boudouresque &
32
Perret 1977, Gallardo et al. 1993), Denmark (Larsen & Sand-Jensen 2006), Faroes (Nielsen &
Gunnarsson 2001), France (Feldmann 1937, Ben Maiz, Boudouresque, Lauret & Riouall 1988,
Gallardo et al. 1993, Verlaque 2001, Dizerbo & Herpe 2007), Greece (Diannelidis 1953, Gerloff
& Geissler 1974, Haritonidis & Tsekos 1976, Tsekos & Haritonidis 1977, Athanasiadis 1987,
Gallardo et al. 1993, Tsirika & Haritonidis 2005), Helgoland (Bartsch & Kuhlenkamp 2000),
Ireland (Cotton 1912, Cullinane 1969, Cullinane 1971, Guiry 1978, De Valéra et al. 1979,
Maggs 1983, Burrows 1991, Morton 1994), Italy (Giaccone 1969, Edwards et al. 1975, Cinelli
et al. 1976, Gallardo et al. 1993, Gallardo et al. 1993, Cecere et al. 1996, Furnari, Cormaci &
Serio 1999, Rindi, Sartoni & Cinelli 2002, Serio et al 2006), Mediterranean Sea (Báez et al.
2002), Netherlands (Stegenga & Mol 1983), Norway (Rueness 1997), Portugal (Araújo et al.,
2003, Araujo et al. 2009, Araújo, Bárbara & Sousa-Pinto in press), Romania (Caraus 2002),
Slovenia (Rindi & Battelli 2005), Spain (Hamel 1928, Miranda 1931, Seoane-Camba 1965,
Ballesteros 1981, Ballesteros & Romero 1982, Pérez-Ruzafa & Honrubia 1984, Gallardo et al.
1985, Alvárez Cobelas & Gallardo 1986, Soto & Conde 1989, Pérez-Ruzafa 1990, Granja,
Cremades & Barbara 1992, Gallardo et al. 1993, Flores-Moya et al. 1995, Bárbara & Cremades
1996, Veiga, Cremades & Bárbara 1998, Cambra Sánchez, Álvarez Cobelas & Aboal Sanjurjo
1998, Calvo, Bárbara & Cremades 1999, Cantoral Uiza & Aboal Sanjurjo 2001, Calvo & Bárbara
2002, Valenzuela Miranda 2002, Gorostiaga et al., 2004, Bárbara et al. 2005, Bárbara et al.
2005, Pérez-Ruzafa et al. 2008), Sweden (Kylin 1907, Kylin 1949, Tolstoy & Österlund 2003),
Turkey (Europe) (Güner, Aysel, Sukatar & Öztürk 1985, Cirik, Zeybeck, Aysel & Cirik 1990,
Taskin et al. 2008
).
1960), Canary Islands (Børgesen 1926, Gil-Rodríguez & Afonso-Carrillo 1980, Gil-Rodriguez,
Afonso-Carrillo & Wildpret de la Torre 1987, Haroun et al. 2002, Gil-Rodríguez et al. 2003,
John et al. 2004), Madeira (Levring 1974, Neto, Cravo & Haroun 2001, John et al. 2004),
Salvage Islands (Audiffred & Weisscher 1984, John et al. 2004).
North America: Alaska (Scagel et al. 1989), British Columbia (Scagel et al. 1989), California
(Abbott & Hollenberg 1976), Connecticut (Van Patten 2009), Florida (Taylor 1928, Taylor
1957, Taylor 1960, Dawes 1974, Littler, Littler & Hanisak 2008), Maine (Mathieson et al.
2001), New Hampshire (Mathieson & Hehre 1986, Mathieson & Dawes 2002), New Jersey
(Taylor 1957), North Carolina (Taylor 1957, Taylor 1960), Nova Scotia (Taylor 1957), Oregon
(Hansen 1997), Texas (Wynne 2009), Virginia (Humm 1979), Washington (Scagel et al. 1989).
Central America: Baja California (Norris 2010), Costa Rica (Taylor 1960), México (Pacific)
(Pedroche et al. 2005), Panama (Taylor 1960, Wysor & Kooistra 2003, Wysor 2004).
Caribbean Islands: Bahamas (Taylor 1960), Barbados (Taylor 1960), Caribbean (Littler &
Littler 2000), Cuba (Taylor 1960, Cabrera, Moreira & Suárez 2004, Suárez 2005), Hispaniola
33
(Taylor 1960), Jamaica (Taylor 1960), Lesser Antilles (Taylor 1960, Taylor 1969), Martinique
(Rodríguez-Prieto, Michanek & Ivon 1999), Netherlands Antilles (Taylor 1960), Puerto Rico
(Taylor 1960), Trinidad (Richardson 1975), Trinidad & Tobago (Duncan & Lee Lum 2006),
Virgin Islands (Taylor 1960).
South America: Argentina (Boraso de Zaixso 2004), Brazil (Taylor 1960), Chile (Santelices
1989), Galápagos Islands (Taylor 1945), Venezuela (Ganesan 1990).
Africa: Algeria (Gallardo et al. 1993), Cameroon (Lawson & John 1987, John, Lawson &
Ameka, 2003, John et al. 2004), Côte d'Ivoire (Lawson & John 1987, John, Lawson & Ameka,
2003, John et al. 2004), Egypt (Papenfuss 1968, Aleem 1993, Gallardo et al. 1993), Eritrea
(Lipkin & Silva 2002, Ateweberhan & Prud'homme van Reine 2005), Ethiopia (Papenfuss
1968), Gabon (Lawson & John 1987, John, Lawson & Ameka, 2003, John et al. 2004), Gambia
(John et al. 2004), Ghana (Lawson & John 1987, John, Lawson & Ameka, 2003, John et al.
2004), Kenya (Silva, Basson & Moe 1996), Liberia (John, Lawson & Ameka, 2003, John et al.
2004), Libya (Gallardo et al. 1993), Madagascar (Silva, Basson & Moe 1996), Mauritius
(Børgesen 1946, Silva, Basson & Moe 1996), Morocco (Gallardo et al. 1993, Benhissoune,
Boudouresque & Verlaque 2001, Benhissoune, Boudouresque & Verlaque 2001), Mozambique
(Silva, Basson & Moe 1996), Namibia (Rull Lluch 2002, John et al. 2004), Senegal (John,
Lawson & Ameka, 2003, John et al. 2004, John et al. 2004), Sierra Leone (Lawson & John
1987, John, Lawson & Ameka, 2003, John et al. 2004), South Africa (Silva, Basson & Moe
1996, Stegenga, Bolton & Anderson 1997), Sudan (Papenfuss 1968), Tanzania (Silva, Basson
& Moe 1996), Togo (Lawson & John 1987, John, Lawson & Ameka, 2003, John et al. 2004),
Tunisia (Ben Maiz, Boudouresque & Quahchi 1987, Gallardo et al. 1993), Western Sahara
(John et al. 2004).
Indian Ocean Islands: Diego Garcia Atoll (Silva, Basson & Moe 1996), Laccadive Islands (Silva,
Basson & Moe 1996), Maldives (Silva, Basson & Moe 1996), Nicobar Islands (Silva, Basson &
Moe 1996), Réunion (Silva, Basson & Moe 1996), Seychelles (Silva, Basson & Moe 1996).
South-west Asia: Abu Dhabi (John, D.M.), Bahrain (Silva, Basson & Moe 1996), Bangladesh
(Silva, Basson & Moe 1996), India (Silva, Basson & Moe 1996, Sahoo et al. 2001), Iran (Silva,
Basson & Moe 1996), Kuwait (Silva, Basson & Moe 1996), Levant states (Gallardo et al. 1993),
Pakistan (Silva, Basson & Moe 1996), Saudi Arabia (Silva, Basson & Moe 1996), Sri Lanka
(Silva, Basson & Moe 1996), Turkey (Asia) (Taskin et al. 2008
).
Asia: China (Tseng 1984), Commander Islands (Selivanova & Zhigadlova 1997), Japan
(Yoshida 1998, Hanyuda et al. 2002), Korea (Lee & Kang 2001), Russia (Kozhenkova 2009),
Taiwan (Huang 2000).
34
South-east Asia: Indonesia (Silva, Basson & Moe 1996), Philippines (Silva, Meñez & Moe
1987), Singapore (Teo & Wee 1983, Silva, Basson & Moe 1996), Thailand (Silva, Basson & Moe
1996), Vietnam (Pham-Hoàng 1969).
Australia and New Zealand: New Zealand (Adams 1994), Papua New Guinea (Coppejans et al.
2001, Littler & Littler 2003), Queensland (Lewis 1987, Phillips 1997, Phillips 2002), South
Australia (Womersley 1984, Day et al. 1995), Victoria (Womersley 1984, Day et al. 1995),
Western Australia (Womersley 1984).
Pacific Islands: Easter Island (Santelices & Abbott 1987), Federated States of Micronesia
(Lobban & Tsuda 2003), Fiji (N'Yeurt, South & Keats 1996, South & Skelton 2003), Samoan
Archipelago (Skelton & South 1999), Solomon Islands (Womersley & Bailey 1970).
(as Chaetomorpha crassa (C.Agardh) Kützing)
Ireland: Antrim (Morton 1994), Down (Morton 1994), Dublin (Adams 1908, Guiry 1978), Mayo
(Cotton 1912, Guiry 1978).
Europe: Adriatic (Ercegović 1980, Gallardo et al. 1993), Balearic Islands (Ballesteros 1992,
Gallardo et al. 1993, Cambra Sánchez, Álvarez Cobelas & Aboal Sanjurjo 1998), Black Sea
(Gallardo et al. 1993), Britain (Newton 1931, Hardy & Guiry 2003), Corsica (Gallardo et al.
1993), France (Dizerbo & Herpe 2007), Greece (Gerloff & Geissler 1974, Haritonidis & Tsekos
1976, Tsekos & Haritonidis 1977, Athanasiadis 1987, Gallardo et al. 1993), Ireland (Adams
1908, Cotton 1912, Guiry 1978, Morton 1994), Italy (Giaccone 1969, Gallardo et al. 1993,
Gallardo et al. 1993), Romania (Caraus 2002), Spain (Ballesteros & Romero 1982, Gallardo et
al. 1985, Alvárez Cobelas & Gallardo 1986, Gallardo et al. 1993, Cambra Sánchez, Álvarez
Cobelas & Aboal Sanjurjo 1998).
Atlantic Islands: Azores (Neto 1994), Bermuda (Taylor 1960).
Central America: Belize (Littler & Littler 1997), México (Pacific) (Pedroche et al. 2005).
Caribbean Islands: Caribbean (Littler & Littler 2000), Cuba (Suárez 2005), Lesser Antilles
(Taylor 1960, Taylor 1969), Trinidad (Richardson 1975), Trinidad & Tobago (Duncan & Lee
Lum 2006), Virgin Islands (Taylor 1960).
South America: Brazil (Lourenço et al 2005), Chile (Ramírez & Santelices 1991), Peru (Ramírez
& Santelices 1991), Venezuela (Ganesan 1990).
Africa: Guinea-Bissau (Welten, Audiffred & Prud'homme van Reine 2002, Welten, Audiffred &
Prud'homme van Reine 2002, John, Lawson & Ameka, 2003, John et al. 2004), Kenya (Silva,
Basson & Moe 1996, Leliaert & Coppejans 2004), Madagascar (Silva, Basson & Moe 1996),
35
Mauritius (Silva, Basson & Moe 1996), Mozambique (Silva, Basson & Moe 1996), São Tomé &
Príncipe (Lawson & John 1987, John, Lawson & Ameka, 2003, John et al. 2004), Somalia
(Silva, Basson & Moe 1996), South Africa (Silva, Basson & Moe 1996), Tanzania (Silva, Basson
& Moe 1996, Leliaert & Coppejans 2004, Oliveira, Österlund & Mtolera 2005).
Indian Ocean Islands: Aldabra Islands (Silva, Basson & Moe 1996), Maldives (Silva, Basson &
Moe 1996), Seychelles (Silva, Basson & Moe 1996).
South-west Asia: India (Silva, Basson & Moe 1996, Sahoo et al. 2001), Kuwait (Silva, Basson
& Moe 1996), Pakistan (Silva, Basson & Moe 1996), Sri Lanka (Børgesen 1936, Silva, Basson &
Moe 1996, Coppejans et al. 2009), Turkey (Asia) (Taskin et al. 2008), Yemen (Silva, Basson &
Moe 1996).
Asia: Japan (Yoshida, Nakajima & Nakata 1990, Yoshida 1998, Hanyuda et al. 2002), Korea
(Lee & Kang 2001, Lee 2008), Taiwan (Huang 2000).
South-east Asia: Indonesia (Verheij & Prud'homme van Reine 1993, Silva, Basson & Moe
1996), Philippines (Silva, Meñez & Moe 1987, Leliaert & Coppejans 2004), Singapore (Silva,
Basson & Moe 1996), Vietnam (Pham-Hoàng 1969, Abbott, Fisher & McDermid 2002, Tsutsui
et al. 2005).
Australia and New Zealand: Papua New Guinea (Coppejans et al. 2001), Queensland (Lewis
1987, Phillips 1997, Phillips 2002).
Pacific Islands: Federated States of Micronesia (Lobban & Tsuda 2003), Fiji (N'Yeurt, South &
Keats 1996, South & Skelton 2003), Solomon Islands (Womersley & Bailey 1970).
(as Chaetomorpha rigida Kützing)
Pacific Islands: Federated States of Micronesia (Lobban & Tsuda 2003).
(as Chaetomorpha linoides Kützing)
Atlantic Islands: St Helena (John et al. 2004).
Central America: México (Pacific) (Pedroche et al. 2005).
South America: Chile (Ramírez & Santelices 1991), Venezuela (Ganesan 1990).
Africa: Ghana (John et al. 2004), Mauritania (John et al. 2004), Mauritius (Børgesen 1940,
Silva, Basson & Moe 1996).
Indian Ocean Islands: Réunion (Silva, Basson & Moe 1996).
36
South-west Asia: India (Silva, Basson & Moe 1996, Sahoo et al. 2001).
(as Chaetomorpha chlorotica (Montagne) Kützing)
Europe: Bulgaria (Dimitrova-Konaklieva 1981), Greece (Gerloff & Geissler 1974), Romania
(Caraus 2002).
Taxonomic notes
John et al. (2003) cite Chaetomorpha aerea (Dillwyn) Kütz. as a synonym of this species. John
et al. (2004) cite Chaetomorpha gallica Kützing as a synonym of this species.
Burrows (1991: 140-141) includes this entity in Chaetomorpha mediterranea (Kützing)
Kützing; see Silva, Meñez & Moe (1987: 96) and Silva, Basson & Moe (1996: 936-937) for the
reasons why C. ligustica is the correct name for a species complex that includes C.
mediterranea. A complete revision of the genus Chaetomorpha is required.
Key references
Burrows, E.M. (1991). Seaweeds of the British Isles. Volume 2. Chlorophyta. pp. xi + 238, 60
figs, 9 plates. London: Natural History Museum Publications.
Day, S.A., Wickham, R.P., Entwisle, T.J. & Tyler, P.A. (1995). Bibliographic check-list of nonmarine algae in Australia. Flora of Australia Supplementary Series 4: vii + 276.
Hanyuda, T., Wakana, I., Arai, S., Miyaji, K., Watano, Y. & Ueda, K. (2002). Phylogenetic
relationships within Cladophorales (Ulvophyceae, Chlorophyta) inferred from 18S rRNA gene
sequences with special reference to Aegagropila linnaei. Journal of Phycology 38: 564-571.
John, D.M. (2002). Order Cladophorales (=Siphonocladales). In: The Freshwater Algal Flora of
the British Isles. An identification guide to freshwater and terrestrial algae. (John, D.M.,
Whitton, B.A. & Brook, A.J. Eds), pp. 468-470. Cambridge: Cambridge University Press.
37
Silva, P.C., Basson, P.W. & Moe, R.L. (1996). Catalogue of the benthic marine algae of the
Indian Ocean. University of California Publications in Botany 79: 1-1259.
Skelton, P.A. & South, G.R. (2007). The benthic marine algae of the Samoan Archipelago,
South Pacific, with emphasis on the Apia District. Nova Hedwigia Beihefte 132: 1-350.
SAG Cultures
Created: 06 April 1996 by M.D. Guiry
Verified by: 17 June 2010 by Wendy Guiry
References
Christensen, T. (1957). Chaetomorpha linum in the attached state. Botanisk Tidsskrift 53:
311-316.
Lavery, P.S. & Mccomb, A.J. (1991). The nutritional eco-physiology of Chaetomorpha linum
and Ulva rigida in Peel Inlet, western Australia. Botanica Marina 34: 251-260.
McGlathery, K.J. & Pedersen, M.F. (1999). The effect of growth irradiance on the coupling of
carbon and nitrogen metabolism in Chaetomorpha linum (Chlorophyta). Journal of Phycology
35: 721-731, 9 figs, 2 tables.
McGlathery, K.J., Pedersen, M.F. & Borum, J. (1996). Changes in intracellular nitrogen pools
and feedback controls on nitrogen uptake in Chaetomorpha linum (Chlorophyta). Journal of
Phycology 32: 393-401, 5 figs, 1 table.
Patel, R.J. (1971). Cytotaxonomical studies of British marine species of Chaetomorpha - I
Chaetomorpha linum Kütz., and Chaetomorpha aerea Kütz.. Phykos 10: 127-136.
38

Catalogue of algae with high growth rates and energy potential

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