Determinants of the diversity of intestinal parasite communities in

Determinants of the diversity of intestinal parasite communities
in sympatric New World primates
(Saguinus mystax, Saguinus fuscicollis, Callicebus cupreus)
Britta Müller
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1. Auflage 2007
© 2007 by Verlag: Deutsche Veterinärmedizinische Gesellschaft Service GmbH, Gießen
Printed in Germany
ISBN 978-3-939902-34-8
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Aus dem Deutschen Primatenzentrum Göttingen
__________________________________________________
Determinants of the diversity
of intestinal parasite communities
in sympatric New World primates
(Saguinus mystax, Saguinus fuscicollis, Callicebus cupreus)
INAUGURAL–DISSERTATION
zur Erlangung des Grades einer Doktorin der Veterinärmedizin
(Dr. med. vet.)
durch die Tierärztliche Hochschule Hannover
vorgelegt von
Britta Müller
aus Münster
Hannover 2007
Wissenschaftliche Betreuung:
Univ. Prof. Dr. F.- J. Kaup
PD Dr. E. W. Heymann
1. Gutachter:
Univ. Prof. Dr. F.- J. Kaup
2. Gutachterin:
Univ. Prof. Dr. E. Zimmermann
Tag der mündlichen Prüfung: 05.06.2007
Diese Promotionssarbeit wurde finanziell gefördert
vom Deutschen Akademischen Austauschdienst (DAAD) und
der Deutschen Forschungsgemeinschaft (DFG) (HE 1870/13-[1-3]).
Meiner Familie
TABLE OF CONTENTS
1
INTRODUCTION ...................................................................................................................1
2
LITERATURE REVIEW ..........................................................................................................3
2.1
Parasite diversity and correlates with host ecology ..................................................3
2.1.1
2.1.1.1
Body size ..................................................................................................8
2.1.1.2
Sex............................................................................................................8
2.1.1.3
Age and longevity .....................................................................................9
2.1.1.4
Dominance rank and social status ..........................................................10
2.1.1.5
Reproductive status ................................................................................10
2.1.1.6
Group size and host density ...................................................................11
2.1.1.7
Social and mating system .......................................................................11
2.1.1.8
Strata use................................................................................................12
2.1.1.9
Diet..........................................................................................................12
2.1.1.10
Nutritional status .....................................................................................13
2.1.1.11
Home-range size and geographic distribution ........................................14
2.1.2
Host-extrinsic or habitat factors ......................................................................15
2.1.2.1
Temperature and humidity ......................................................................15
2.1.2.2
Solar radiation.........................................................................................15
2.1.2.3
Soil type ..................................................................................................16
2.1.2.4
Water bodies...........................................................................................16
2.1.2.5
Habitat morphology.................................................................................17
2.1.2.6
Resources for intermediate hosts and vectors........................................17
2.1.2.7
Vegetation type and density....................................................................18
2.1.2.8
Predation.................................................................................................18
2.1.3
2.2
Host-intrinsic factors .........................................................................................8
Seasonality .....................................................................................................18
Intestinal parasite diversity in New World primates ................................................19
2.2.1
Intestinal protozoa ..........................................................................................19
2.2.2
Intestinal helminths .........................................................................................21
2.3
2.2.2.1
Trematoda...............................................................................................21
2.2.2.2
Cestoda...................................................................................................21
2.2.2.3
Nematoda ...............................................................................................22
2.2.2.4
Acanthocephala ......................................................................................22
Study host species .................................................................................................23
2.3.1
Saguinus mystax and Saguinus fuscicollis .....................................................23
2.3.2
Callicebus cupreus .........................................................................................24
2.4
2.4.1
Selection bias .................................................................................................27
2.4.2
Information bias ..............................................................................................27
2.4.3
Confounding bias............................................................................................28
2.5
3
Bias in parasitological studies ................................................................................27
Objectives of this study...........................................................................................28
ANIMALS, MATERIALS AND METHODS .................................................................................33
3.1
Study site................................................................................................................33
3.2
Study animals .........................................................................................................33
3.3
Study period ...........................................................................................................35
3.4
Parasitological analyses .........................................................................................36
3.4.1
Faecal sample collection and preservation.....................................................36
3.4.2
Sedimentation procedure................................................................................38
3.4.3
Microscopic examination ................................................................................38
3.4.4
Intra-observer reliability test............................................................................39
3.4.5
Qualitative and quantitative description of parasite diversity ..........................39
3.4.5.1
Parasite identification..............................................................................39
3.4.5.2
Parasite species richness (PSR) ............................................................41
3.4.5.3
Prevalence ..............................................................................................41
3.4.5.4
Egg or larvae output................................................................................41
3.5
Behavioural observations .......................................................................................42
3.6
Post-mortem examination.......................................................................................44
3.7
Habitat characterization ..........................................................................................45
3.7.1
Drainage .........................................................................................................46
3.7.2
Soil type ..........................................................................................................47
3.7.3
Ground inclination...........................................................................................47
3.7.4
Height of leaf litter...........................................................................................47
3.7.5
Deadwood abundance....................................................................................48
3.7.6
Vegetation density ..........................................................................................48
3.7.7
Understorey density........................................................................................49
3.8
Climate ...................................................................................................................49
3.9
Phenology...............................................................................................................50
3.10
Statistical analyses .................................................................................................50
3.10.1
Parasite morphology.......................................................................................51
4
3.10.2
PSR and prevalence.......................................................................................51
3.10.3
Egg/larvae output............................................................................................53
3.10.4
Behavioural observations and phenology.......................................................54
RESULTS .........................................................................................................................55
4.1
Parasite diversity ....................................................................................................55
4.1.1
Helminths........................................................................................................55
4.1.2
Protozoa .........................................................................................................61
4.2
Parasite ecology .....................................................................................................61
4.3
Variation in parasite species richness (PSR) and prevalence ................................63
4.3.1
4.3.1.1
Host species ...........................................................................................64
4.3.1.2
Host sex ..................................................................................................67
4.3.1.3
Strata use................................................................................................70
4.3.1.4
Diet composition .....................................................................................72
4.3.1.5
Home-range size.....................................................................................76
4.3.1.6
Group size...............................................................................................77
4.3.1.7
Host density ............................................................................................78
4.3.2
Host-extrinsic or habitat factors ......................................................................79
4.3.2.1
Home ranges ..........................................................................................79
4.3.2.2
Habitat use..............................................................................................82
4.3.3
5
Host-intrinsic factors .......................................................................................64
Seasonality .....................................................................................................93
4.3.3.1
PSR and prevalences .............................................................................93
4.3.3.2
Climate....................................................................................................94
4.3.3.3
Phenology ...............................................................................................94
4.3.3.4
Diet..........................................................................................................96
4.4
Variation in egg and larvae output ..........................................................................96
4.5
Post-mortem analyses ..........................................................................................103
4.5.1
Small and large intestine ..............................................................................103
4.5.2
Liver ..............................................................................................................104
4.5.3
Abdominal cavity...........................................................................................105
4.5.4
Further pathological findings.........................................................................106
DISCUSSION ...................................................................................................................107
5.1
Methodological considerations .............................................................................107
5.1.1
Faecal sampling, fixation and concentration technique ................................107
5.1.2
Helminth identification...................................................................................111
5.1.3
Metrics of disease risk ..................................................................................112
5.1.4
Avoiding bias ................................................................................................114
5.2
5.1.4.1
Selection bias........................................................................................114
5.1.4.2
Information bias ....................................................................................115
5.1.4.3
Confounding bias ..................................................................................115
Parasite diversity and host-intrinsic correlates .....................................................116
5.2.1
Host species .................................................................................................118
5.2.2
Host sex........................................................................................................120
5.2.3
Strata use .....................................................................................................122
5.2.4
Diet ...............................................................................................................123
5.2.5
Home-range size ..........................................................................................126
5.2.6
Group size and host density .........................................................................128
5.3
Parasite diversity and host-extrinsic correlates ....................................................131
5.3.1
Ground humidity ...........................................................................................133
5.3.2
Soil type ........................................................................................................134
5.3.3
Habitat morphology.......................................................................................136
5.3.4
Resources for intermediate hosts .................................................................136
5.3.5
Vegetation density ........................................................................................138
5.4
Seasonal variation in parasite diversity ................................................................140
5.4.1
Host susceptibility related to the nutritional status ........................................142
5.4.2
Host exposure...............................................................................................143
5.5
Parasites and their impact on the host’s survival..................................................145
5.6
Conclusions ..........................................................................................................149
6
SUMMARY ......................................................................................................................152
7
ZUSAMMENFASSUNG (GERMAN SUMMARY)......................................................................155
8
RESUMEN (SPANISH SUMMARY) ......................................................................................160
9
REFERENCES .................................................................................................................160
10
APPENDICES ..................................................................................................................190
11
DANKSAGUNG/AGRADECIMIENTOS/ACKNOWLEDGEMENTS ...............................................214
Abbreviations
ANOVA
analysis of variance
°C
degree Celsius
C.c.
Callicebus cupreus
cm
centimetre
DBH
diameter at breast height (of trees)
df
degrees of freedom
DPZ
Deutsches Primatenzentrum (German Primate Center)
e.g.
exempli gratia (for example)
EBQB
field station Estación Biológica Quebrada Blanco
et al.
et alii (and others)
Fig.
Figure
g
gram
g
acceleration due to gravity (standard gravity, 9.80665 m/s2)
GLMM
General Linear Mixed Model
h
hour
H.&E.
haematoxylin-eosin stain
ha
hectare
i.e.
id est (that is)
IQR
interquartile range
km
kilometre
m
metre
max
maximum
min
minimum
ml
millilitre
µl
microlitre
mm
millimetre
µm
micrometre
MWU
Mann-Whitney U-test
N
number
NE
North East
NW
North West
PAS
periodic acid-Schiff reaction
PET
polyethylene terephthalate
POM
point of measurement
PSR
parasite species richness
rpm
rounds per minute
S.f.
Saguinus fuscicollis
S.m.
Saguinus mystax
SD
standard deviation
SE
South East
SEM
scanning electron microscope
SW
South West
syn.
synonymous with
sp.
species (singular)
spp.
species (plural)
Introduction
1
1 INTRODUCTION
Parasites are significant sources of mortality in wild animal populations (HUDSON et
al. 2002; MOORE and WILSON 2002). Thus, it is of basic and applied importance to
assess accurately the patterns of parasitism in wild hosts and to identify host-intrinsic
and environmental factors that determine parasite diversity. From various field and
meta-studies host-intrinsic factors like body size, diet, group size, geographic range
(CÔTÉ and POULIN 1995; MORAND and POULIN 1998; NUNN et al. 2003), as well
as host-extrinsic factors, namely climate or soil moisture (MÜLLER-GRAF et al. 1996;
LILLY et al. 2001), are supposed to affect the composition of parasite communities.
However, there has been no study that examined systematically a comprehensive
set of both host-intrinsic and -extrinsic factors affecting parasite diversity in sympatric
primate host populations.
The primary objectives of this study are to collect baseline data on the intestinal
parasite spectrum of three wild, sympatric New World primate species (Saguinus
mystax, Saguinus fuscicollis and Callicebus cupreus) and characterize the role of
host-intrinsic traits and environmental factors for parasite species richness (PSR) and
parasite prevalences. In order to achieve these goals it was aimed to improve and
standardize methods for parasitological analyses in terms of sample collection,
processing and examination for the needs of primatological field studies. In total, over
2200 faecal samples were collected over a 15 month period from altogether 45 host
individuals of the three study species at the field site Estación Biológica Quebrada
Blanco (EBQB) in Peru. Data on activity patterns, ranging and group composition
was collected to explore the importance of the following host-intrinsic factors on
parasitism: host sex, strata use, diet composition, nutritional status, home-range size,
host density and group size. In order to elucidate environmental factors that may
shape parasite diversity, different habitat variables were measured like ground
humidity, soil type, habitat morphology, resource distribution for intermediate hosts
and vegetation density.
This comprehensive comparative study is a powerful approach for a better
understanding of the factors that determine intestinal parasite diversity. A non-
2
Introduction
invasive year-round study on parasitism of natural host communities provides
essential advantages: by multiple sampling of individually recognized hosts the
information on parasite patterns is highly reliable (MUEHLENBEIN 2005).
Simultaneously, a diverse array of potential factors is considered while the study
animals are in their natural environment and not affected by an anthropogenic impact
(EZENWA et al. 2006; KEESING et al. 2006). By means of standardized
parasitological methods the bias is reduced. A more comprehensive insight into the
seasonal variation of parasite diversity is provided by including data from rainy and
dry season.
The results of this study are also of particular interest for public health concern: the
study host species are commonly kept as pet animals or used for food in rural areas
of Peru and other countries and their parasites are potentially zoonotic (ORIHEL
1970; FLYNN 1973; MICHAUD et al. 2003). Furthermore, the deeper understanding
of host-parasite interaction and habitat influences can be important for conservation
management (STUART and STRIER 1995; GILLESPIE et al. 2004; CHAPMAN et al.
2006).
Literature review
3
2 LITERATURE REVIEW
2.1
Parasite diversity and correlates with host ecology
Parasites can exert an important impact on host population regulation in terms of
reducing fecundity and/or survival of the host individuals (SCOTT and DOBSON
1989; HUDSON et al. 2002). They can even lead to rapid declines of host
populations or host species extinctions (DASZAK 2000; HARVELL et al. 2002).
Parasites are assigned a central role in sexual selection and the evolution of male
secondary sexual characters that advertise their high parasite resistance because
females should benefit from choosing parasite-resistant mates by the means of these
sex traits or honest signals (HAMILTON and ZUK 1982; MØLLER 1990; ZUK 1996).
Since parasites play such an important role it is crucial to investigate factors that
shape the probability of acquiring parasites and the risk of developing pathology
caused by these parasites, the so-called disease risk (NUNN and ALTIZER 2006).
Many different factors are assumed to shape parasite diversity in hosts by
modulating this disease risk at any stage of the potential infection: parasite
encounter, transmission, parasite recruitment, colonization, parasite reproduction or
establishment. Disease risk is difficult to measure in wild host populations, thus
indirect surrogates are needed: parasite species richness (PSR) describes the
number of parasite species encountered per host (MORAND and HARVEY 2000;
NUNN et al. 2003). Parasite intensity is the number of parasite individuals of a
particular species per host (MARGOLIS et al. 1982; BUSH et al. 1997). Parasite
prevalence is the number of hosts infected with a particular parasite as a proportion
of all hosts examined (MARGOLIS et al. 1982; BUSH et al. 1997). In summary, these
three metrics allow to estimate indirectly the disease risk in host populations.
Since in the ecological sense the term “parasite” encompasses a wide range of
organisms like virus, bacteria, fungi, helminths, protozoa and arthropods which
diverge enormously in their mode of replication and transmission, generation times,
elicited immune responses and diseases etc. (HUDSON et al. 2002) it is essential to
specify the studied parasite type. This study focuses on protozoan and helminthic
4
Literature review
parasites mainly dwelling in the intestinal tract. Due to the coprological survey of
parasites this study also includes protozoan and helminthic parasites inhabiting other
sites than the intestine that shed their propagules in the faeces, e.g. parasites that
inhabit the stomach, upper parts of the alimentary tract, pancreas, liver, mesenteric
vessels, lungs or other tissues. For convenience the protozoa and helminths
considered in this study will be simply called intestinal parasites.
As the host represents the well-defined habitat on which the parasite depends
strongly for at least one life-history stage it is of great interest to study host traits in
search of ecological, behavioural and morphological correlates for parasite diversity.
A growing body of studies reveals the importance of host traits for parasite diversity
on the individual, population and species level (CÔTÉ and POULIN 1995;
GREGORY et al. 1996; MORAND and POULIN 1998; ARNEBERG 2002; ALTIZER
et al. 2003; NUNN et al. 2003; EZENWA 2004b; VITONE et al. 2004).
Nevertheless, parasites are also intimately linked to the host’s environment. Although
with few exceptions intestinal parasites are obligatory endoparasites they pass their
propagules into the external environment to reach the next definitive or intermediate
host (ECKERT 2000; BUSH et al. 2001). Parasite diversity cannot be investigated
without considering parasite ecology in terms of life cycle, transmission mode, host
specificity, and host and parasite habitat characteristics. In order to understand hostparasite-interactions knowledge of the parasites’ life cycle is crucial. Direct life cycle
(homoxenous parasites) means that transmission occurs within individuals of one
host species where adult parasites reproduce sexually and release propagules.
However, some of the directly transmitted parasites spend an obligatory period
outside the host, for example in the soil to undergo a development into the infective
stages (soil-transmitted parasites, e.g. Strongyloides sp., Trichuris sp. Ascaris sp.
and hookworms (DUNN et al. 1968; ASH and ORIHEL 1987; BETHONY et al. 2006).
An indirect life cycle (heteroxenous parasites) requires at least one other host
species as intermediate host where asexual reproduction of the parasite can take
place (BUSH et al. 2001; ECKERT et al. 2005). While reasonable knowledge is
available for a number of parasites affecting domestic animals and parasites in
Literature review
5
temperate zones, information on potential intermediate hosts or even life cycles in
complex tropical ecology remains extremely rudimentary.
Other important strategies for parasites to persist in the environment and ensure
transmission are hypobiosis (developmental arrestment) and the use of reservoir
hosts (BUSH et al. 2001; HUDSON et al. 2002). Hypobiosis is a temporary cessation
in development of many nematode species. It is an important adaptation to changing
ecological conditions and can be induced in three ways: by adverse environmental
conditions (e.g. temperature, day length) or by host-intrinsic factors (resistance,
reproductive cycles) or parasite intrinsic factors (density dependent and genetically
based arrestment) (BUSH et al. 2001). A reservoir host comprises one or more
epidemiologically connected populations where the parasite can persist and from
which infection is transmitted to the defined target population (HAYDON et al. 2002;
HUDSON et al. 2002).
Very few studies have examined the habitat influences on parasite diversity, mostly
focussing on human intestinal parasite prevalences and their correlation with climatic
factors, elevation, soil type, vegetation density (AUGUSTINE and SMILLIE 1926;
SORIANO et al. 2001; MABASO et al. 2003; SÁNCHEZ THEVENET et al. 2004;
SAATHOFF et al. 2005a; SAATHOFF et al. 2005b). Most primatological studies on
intestinal parasite diversity detected habitat specific variations as a by-product of
their main research goals (MCGREW et al. 1989b; STUART et al. 1990; STONER
1993; STUART et al. 1993; STUART and STRIER 1995; MÜLLER-GRAF et al. 1996;
STONER 1996; MÜLLER-GRAF et al. 1997).
From this perspective, to get a comprehensive insight into the factors shaping
parasite diversity both host-intrinsic and environmental or habitat factors deserve
closer attention. The potential effects of host-intrinsic (2.1.1) and -extrinsic factors
(2.1.2.) are discussed in chapter 2.1. The chapter titles are underlined if this study
design allows investigating the respective factors. A synopsis of these factors is
depicted in Fig. 2.1. Since it is not possible to unravel the effects of host-intrinsic and
-extrinsic factors on parasite diversity without considering the biology of intestinal
parasites it will be presented shortly in the subsequent section (chapter 2.2). In order
6
Literature review
to achieve a better understanding of the examined host-intrinsic and also -extrinsic
factors, background information on the three study host species will be outlined in
chapter 2.3. Chapter 2.4 outlines some sources of bias that can frequently emerge in
parasitological studies especially in non-invasive surveys on wild host populations. In
chapter 2.5 the main goals of this study and the hypotheses are presented.
Individuum
Groups or populations
Species or metapopulations
HOST
•
•
•
•
•
•
•
•
body size
sex
age, longevity
social status
reproductive status
strata use
diet
nutrional status
• home-range size
• group size
• host density
• social & mating system
• geographic distribution
biotic
abiotic
•
•
•
•
•
•
temperature
humidity
solar radiation
soil type
water bodies
habitat morphology
•
•
•
•
•
Literature review
HABITAT
• resources
• vegetation density
& type
• vector/ intermediate
host abundance
• predation
life cycle
transmission mode
location
host specificity
pathogenicity
PARASITE
7
Fig. 2.1 Host-intrinsic and -extrinsic factors determining parasite diversity. Factors examined in this study are printed in bold letters.
Literature review
8
2.1.1
Host-intrinsic factors
Host-intrinsic factors reflect the conditions offered by the host that affect directly the
habitat of the parasite. Host-intrinsic factors can influence parasite diversity on
different host levels: on an individual (e.g. sex, age), population (population size and
density) or species level (geographic distribution) (Fig. 2.1).
2.1.1.1 Body size
Large body size is correlated with parameters that can influence parasite diversity:
generally, body size is positively correlated with longevity, body surface, home-range
size and metabolic rate (BELL and BURT 1991; WATVE and SUKUMAR 1995;
GREGORY et al. 1996; MORAND and POULIN 1998; MORAND and HARVEY 2000;
NUNN et al. 2003; POULIN and MOUILLOT 2004). As metabolic rate increases with
body size also the food uptake increases, augmenting the probability of food-borne
parasite infection (POULIN 1995a; WATVE and SUKUMAR 1995; GREGORY et al.
1996; MORAND and POULIN 1998; MORAND and HARVEY 2000; ARNEBERG
2002; POULIN and MOUILLOT 2004). Since large hosts have an increased activity
level or mobility and a longer life span, their exposure to infectious stages is longer
and more intense; thus leading to a higher parasite accumulation rate and period
(CÔTÉ and POULIN 1995; MORAND and HARVEY 2000; ARNEBERG 2002;
POULIN and MOUILLOT 2004). Some authors argue that a larger body size can also
be associated with an increasing niche diversity that offers potential habitats for
parasites (GUEGAN and KENNEDY 1993; POULIN 1995a; GREGORY et al. 1996;
MORAND and POULIN 1998; VITONE et al. 2004). Therefore, larger hosts should be
able to accommodate more parasite species and offer them more stable and greater
“habitat islands” (BELL and BURT 1991; POULIN 1995a; POULIN and MOUILLOT
2004).
2.1.1.2 Sex
Adult males of vertebrates, including humans, tend to be more heavily parasitized
than adult females (POULIN 1996; ZUK and MCKEAN 1996; SCHALK and FORBES
1997; KLEIN 2000; HUDSON et al. 2002; MOORE and WILSON 2002). Sex
Literature review
9
differences in morphology, metabolism, endocrine-immune system and behaviour
can result in varying exposure to parasites and/or higher susceptibility (ZUK and
MCKEAN 1996; KLEIN 2000). Sex hormones can have direct effects on growth and
development of parasites but they can also modulate the immune responses and
indirectly affect the parasite colonization (ZUK and MCKEAN 1996). Testosterone is
thought to act as a handicap for males because it is supposed to compromise the
immune system (“immunocompetence handicap” (FOLSTAD and KARTER 1992)). It
has been shown to suppress the cell-mediated and humoral immunity (ZUK and
MCKEAN 1996; SCHALK and FORBES 1997; KLEIN and NELSON 1999; KLEIN
2000; MOUGEOT et al. 2006). In females, oestrogens and prolactin are mostly
considered to enhance immune functions (SCHALK and FORBES 1997; KLEIN and
NELSON 1999; HUDSON et al. 2002). On the other hand, females’ progesterone
and other pregnancy related hormones can play an immunosuppressive role (ZUK
and MCKEAN 1996). Host behaviour is inseparably intertwined with sex and stress
hormones: sex steroids regulate sex-specific behaviour that may expose males to a
higher disease risk, e.g. aggression, competition, territorial defence, mating display,
dispersal, sex-specific habitat use and diet (POULIN 1996; ZUK and MCKEAN 1996;
SCHALK and FORBES 1997; KLEIN 2000; SEIVWRIGHT et al. 2005; MOUGEOT et
al. 2006; NUNN and ALTIZER 2006). Sex-specific behaviour mentioned above
seems to expose males to more stressors that are associated with elevated
corticosteroid levels and thus reduced immune response (ZUK and MCKEAN 1996;
KLEIN and NELSON 1999; BERCOVITCH and ZIEGLER 2002). Taken together, in
this study the males are expected to have a higher parasite diversity and prevalence.
2.1.1.3 Age and longevity
Susceptibility to parasites and exposure risk varies throughout the life history stages:
acquired immunity develops with increasing number of parasite encounters indicating
that the older the host individual is the greater is its immune competence (HUDSON
et al. 2002). However, animals tend to exhibit lower immune defences towards the
end of their life (MORAND and HARVEY 2000). Suckling infants can receive a
passive immunity by colostral antibodies, but generally their immune response is
weak (NUNN and ALTIZER 2006). Longevity should correlate positively with parasite
10
Literature review
diversity and intensity as a consequence of parasite accumulation over the whole life
span (BELL and BURT 1991; MORAND and HARVEY 2000).
2.1.1.4 Dominance rank and social status
The degree of parasitism is influenced by dominance rank or social status (BARTOLI
et al. 2000; ALTIZER et al. 2003; NUNN and ALTIZER 2006). There are conflicting
theories about effects of dominance rank: higher ranking individuals might be more
exposed to parasites because of increased mating behaviour, contact rates with
females and agonistic encounters (KLEIN 2000; NUNN and ALTIZER 2006). They
can be also more susceptible because of alteration in the endocrine-immune system
(higher testosterone levels in males, increased corticosteroid levels leading to an
impairment of the immune defences, see 2.1.1.2) (BERCOVITCH and ZIEGLER
2002). On the other hand, socially subordinate individuals might suffer an increased
disease risk: they might experience elevated stress levels due to intimidation by the
dominant individuals, they are likely to have less access to resources and to occupy
less favourable habitats (BARTOLI et al. 2000; SAPOLSKY 2005; NUNN and
ALTIZER 2006). Dominance rank-related behaviour, e.g. breeding and dispersal,
also influences patterns of parasitism (BARTOLI et al. 2000; ALTIZER et al. 2003).
2.1.1.5 Reproductive status
Disease risk varies with the reproductive status as a consequence of alteration in
energy demands, reproductive effort and in endocrine-immune status. Behaviour
which is tied to the reproductive phase can challenge the metabolism and immune
system (exhaustive courtship displays, increased contact rates, competition, mate
selection, gestation, parturition, lactation or infant care) (GIBBS and BARGER 1986;
FESTA-BIANCHET 1989; GUSTAFSSON et al. 1994; ZUK and MCKEAN 1996;
KLEIN and NELSON 1999; KLEIN 2000; ALTIZER et al. 2003; NUNN and ALTIZER
2006). In conclusion, energetic and social stress might lead to a decrease in immune
functions and increase in parasite prevalence and/or intensity (KLEIN and NELSON
1999; BERCOVITCH and ZIEGLER 2002). Yet, changes in parasite infections
varying with the reproductive cycle can potentially be confounded with seasonal
variations (ZUK and MCKEAN 1996).
Literature review
11
2.1.1.6 Group size and host density
Group or population size and host density is expected to correlate positively with
parasite diversity. The parasite transmission, especially of the directly transmitted
parasites, depends strongly on the number of actually available hosts at a given time
in a given area and on their contact rate (CÔTÉ and POULIN 1995; WATVE and
SUKUMAR 1995; MORAND and POULIN 1998; ARNEBERG 2002; NUNN et al.
2003; BAGGE et al. 2004; POULIN and MOUILLOT 2004; VITONE et al. 2004).
Epidemiological models predict that host density or number of hosts is an important
determinant for the basic parasite reproduction rate (R0) which represents the
capacity of a parasite to invade a susceptible host population and become
established there (ANDERSON and MAY 1991; HUDSON et al. 2002). A minimum
density or threshold density of a population can be derived from this model, below
which a specific parasite cannot persist in this host population. Large groups
therefore can support a large parasite diversity (FREELAND 1979; PRICE 1990;
BELL and BURT 1991; LOEHLE 1995; MORAND and POULIN 1998; BAGGE et al.
2004; EZENWA 2004a; POULIN and MOUILLOT 2004). Thus, larger groups with
higher densities and therefore potentially higher contact rates should exhibit a higher
parasite diversity and prevalence. Parasites that are transmitted by intermediate
hosts, vectors, via contaminated soil and water or by sexual contact should be less
dependent on host density or group size (CÔTÉ and POULIN 1995; ALTIZER et al.
2003).
2.1.1.7 Social and mating system
Not only host density or number of hosts influences contact rates within a group but
also the effective size of a sub-structured group maintained by hierarchy or cohesion.
Thus, the social and mating system is considered an important factor to shape
parasite diversity (LOEHLE 1995; ALTIZER et al. 2003; NUNN et al. 2003). If the
frequency and intensity of interactions within the group members is high, parasite
species richness and prevalence is expected to be high as well. Another important
aspect of the social system is the stability of groups: with more frequent exchange of
group members the contact with diverse parasites increases (CÔTÉ and POULIN
1995; EZENWA 2004a).
12
Literature review
2.1.1.8 Strata use
Terrestrial animals should host more diverse communities of parasites in higher
prevalences than arboreal animals (DUNN 1968; DUNN et al. 1968). Parasite stages
excreted in faeces, urine or other corporal liquids can accumulate on the ground and
consequently disease risk in species showing a higher terrestriality should be
increased (NUNN and ALTIZER 2006). In addition, so-called soil-transmitted
parasites, which strictly require detritus or soil for their larval development, can be
transmitted while the animals frequent the ground (DUNN et al. 1968; ASH and
ORIHEL 1987). On the ground there is also a higher accumulation of generalist
parasites shed by heterospecifics, e.g. rodents (MORERA 1973; SLY et al. 1982;
ASH and ORIHEL 1987; POTKAY 1992; MICHAUD et al. 2003). On the other hand,
one could argue that the use of diverse strata increases the probability to encounter
different parasites (NUNN et al. 2003). Parasites are linked to different strata,
especially to the stratified occurrence of intermediate hosts (DUNN et al. 1968).
2.1.1.9 Diet
The ingestion of food items can influence parasite diversity mainly in three ways:
firstly, hosts can get infected accidentally by the uptake of contaminated food or
water. Secondly, parasites can be recruited by ingestion of animal prey which can
serve as intermediate hosts for heteroxenous parasites (FREELAND 1983;
KENNEDY et al. 1986; GUEGAN and KENNEDY 1993; WATVE and SUKUMAR
1995; NUNN et al. 2003; VITONE et al. 2004). In primate food webs, amphibians,
fish, small reptiles, insects and other arthropods, even mammals or other primates
can serve as intermediate hosts. As a consequence insectivorous, carnivorous or
omnivorous host species should harbour a more diverse parasite community than
folivorous or herbivorous host species (DUNN 1968; KENNEDY et al. 1986; POULIN
1995a). Not only the diet components but also the dietary breadth should influence
parasite diversity: diet generalists are exposed to a wide array of infection sources
leading to a higher diversity in parasite assemblage (DUNN et al. 1968; KENNEDY et
al. 1986; PRICE 1990; POULIN 1995a; GREGORY et al. 1996). Thirdly, parasite
diversity may be negatively influenced by the intake of diet-derived anti-parasitic
plant compounds (NUNN et al. 2003; VITONE et al. 2004): certain secondary plant
Literature review
13
metabolites, such as phenolic or nitrogen-containing metabolites and terpenoids, e.g.
tannins, are thought to possess anti-parasitic effects (COOP and KYRIAZAKIS
2001). Folivorous hosts can reduce parasite intensity by the selective ingestion of
plants with chemical or physical properties of purging intestinal parasites (HUFFMAN
et al. 1997). On the other hand, folivory is also associated with a higher resource
intake and thus a higher parasite exposure risk (NUNN et al. 2003; VITONE et al.
2004; NUNN and ALTIZER 2006). Also the accidental uptake of animal prey could
play a role in folivorous hosts. A confounding factor for diet can be host body size
because body size is positively correlated with food uptake (GREGORY et al. 1996;
VITONE et al. 2004), as described in chapter 2.1.1.1. This study focuses on the
aspect of intermediate host uptake, and therefore it is expected that the proportion of
animal prey in the host’s diet correlates positively with parasite diversity and
prevalence.
2.1.1.10 Nutritional status
Not only quality but also the quantity of the host’s diet has a major effect on parasite
infection. The importance of the host’s nutritional status for the function of the
immune system is generally accepted (BUNDY and GOLDEN 1987; FOLSTAD and
KARTER 1992; HOLMES 1993; BEISEL 1996; COOP and HOLMES 1996; COOP
and KYRIAZAKIS 2001; KOSKI and SCOTT 2001; NELSON and DEMAS 2004). The
nutritional status can influence parasitism mainly in two aspects: firstly, it influences
host defences which regulate parasite colonization, growth and fecundity
(resistance). Secondly, it can affect the capability to cope with the pathophysiological consequences of parasite infection (resilience) (GIBSON 1963;
HOLMES 1993; BEISEL 1996; COOP and HOLMES 1996; COOP and KYRIAZAKIS
2001). Malnutrition which is characterized by a deficiency of total energy and protein
supply leads to a variety of severe immune dysfunctions and an impaired resilience
(GIBSON 1963; BUNDY and GOLDEN 1987; BEISEL 1996; COOP and
KYRIAZAKIS 2001). In seasons with low food availability and/or quality or in
situations of higher energy demands (growth, late pregnancy and lactation),
malnutrition can impair the immune system even more pronounced (COOP and
KYRIAZAKIS 2001). Animals suffering malnourishment combined with parasite
14
Literature review
infection enter a vicious circle: malnutrition enhances parasite infection and intestinal
parasites in turn reduce food uptake and resource utilization and increase protein
loss into the intestinal lumen (GIBSON 1963; KOSKI and SCOTT 2001). In
conclusion, the parasite diversity and prevalence is expected to be higher in hosts of
a poor nutritional status or in a period of food scarcity.
2.1.1.11 Home-range size and geographic distribution
Hosts which are distributed in a large and heterogeneous space should harbour a
greater diversity of parasites than hosts with a uniform and small habitat niche
(KENNEDY et al. 1986; POULIN and MOUILLOT 2004). On a small scale, travel
distances and home-range size, on a larger scale habitat and geographic distribution
determine the area that is sampled by the host. Larger spatial distribution also
implies a higher probability of encounters with conspecific and heterospecific hosts
which can transmit generalist parasites (EZENWA 2003; NUNN et al. 2003; POULIN
and MOUILLOT 2004; VITONE et al. 2004). The higher exposure to different
parasites should translate into higher parasite diversity (PRICE 1990; BELL and
BURT 1991; GUEGAN and KENNEDY 1993; WATVE and SUKUMAR 1995; NUNN
et al. 2003; VITONE et al. 2004). Another aspect of spatial distribution is the host’s
territoriality. Hosts which are confined to a determined area are expected to be
exposed to an increasingly contaminated environment, and thus, to accumulate more
parasites over time. Territorial host species or hosts with smaller home ranges
should exhibit a higher parasite intensity and prevalence compared to non-territorial
host species or hosts with larger home ranges (CÔTÉ and POULIN 1995; EZENWA
2004a). Thus, hosts with larger home ranges should experience a higher PSR but
lower parasite prevalence.
Not only the size and heterogeneity of the habitat but also the latitudinal position of
geographical range plays an important role (POULIN 1995a; BUSH et al. 2001;
NUNN et al. 2005). The higher abundance of intermediate and definitive hosts, the
more favourable environmental conditions in the tropics compared to more temperate
areas may enhance parasite transmission (NUNN et al. 2005). Thus, with closer
proximity to the equator parasite diversity should increase.
Literature review
2.1.2
15
Host-extrinsic or habitat factors
Host-extrinsic or habitat factors lead to variation in disease risk changing the host’s
exposure to parasites also independently from the host susceptibility. Abiotic and
biotic habitat factors are closely interrelated and their complex interaction influences
the assemblage of parasite communities by modifying the conditions for free-living
parasite stages, intermediate hosts or vectors. Besides the above mentioned aspects
of the habitat and the host’s mobility within this habitat, there are numerous hostextrinsic habitat factors that shape parasite diversity.
2.1.2.1 Temperature and humidity
Temperature and humidity are key factors for the survival and development of
parasite stages (WHARTON 1979; UDONSI and ATATA 1987; ROEPSTORFF and
MURRELL 1997; STROMBERG 1997; BUSH et al. 2001; BETHONY et al. 2006).
Temperature and humidity are also determining the abundance of intermediate hosts
especially of arthropods groups (TANAKA and TANAKA 1982; PEARSON and DERR
1986). Depending on the parasites’ morphological features and physiology, some
stages of nematode larvae are particularly vulnerable to climatic conditions
(GORDON 1948; STROMBERG 1997). Some authors pointed out that an optimal
combination of temperature and humidity is crucial for the viability of free-living
stages (GORDON 1948; DIESFELD 1970; UDONSI and ATATA 1987). Deviation
from the optimum can reduce egg hatch rates, longevity, infectivity, larval migration
and desiccation tolerance (WHARTON 1979; ARENE 1986; UDONSI and ATATA
1987). Climatic conditions on a larger geographical scale play an important role but
microclimatic conditions turned out to be of eminent importance (DIESFELD 1970;
SMITH 1990). Therefore, this study aims at examining the influence of ground
humidity on parasite diversity and prevalence. But not only amount and distribution of
precipitation contribute to the local humidity but also soil type, water-retaining leaf
litter and vegetation density (PATZ et al. 2000).
2.1.2.2 Solar radiation
Ultraviolet light causes damages to parasite eggs (STOREY and PHILLIPS 1985;
ROEPSTORFF and MURRELL 1997; SAATHOFF et al. 2005a). In combination with
16
Literature review
higher temperatures, sunlight can reduce longevity and desiccation tolerance
(STOREY and PHILLIPS 1985; UDONSI and ATATA 1987).
2.1.2.3 Soil type
The soil type can modify parasite diversity and prevalence (PATZ et al. 2000; BUSH
et al. 2001). Especially for soil-transmitted parasites it is of major importance
(BUNGIRO and CAPPELLO 2004). The soil is also relevant to parasite stages and
intermediate hosts: its texture, acidity, salinity, mineral content, degree of water
retention and aeration can drive the parasite development and viability (VINAYAK et
al. 1979; PEARSON and DERR 1986; MIZGAJASKA 1993; SÁNCHEZ THEVENET
et al. 2004; SAATHOFF et al. 2005a).
Depending on the soil texture, the size and the ability of active movement of the
parasite stages, they travel into deeper soil layers where they are protected from
adverse environmental condition (STOREY and PHILLIPS 1985; MIZGAJASKA
1993; SAATHOFF et al. 2005b). Soil moisture can be an important parameter for
intermediate host diversity and abundance: it is positively correlated with beetle
species richness (LASSAU et al. 2005). Mineral contents such as calcium in soil
limits the abundance of snails which are important intermediate hosts of trematodes
and some nematodes (BUSH et al. 2001). Soil nutrients and electrolytes can be
essential for larvae to reach infectivity (UDONSI and ATATA 1987). The acidity of soil
has a significant effect on hatch rate of nematode eggs (UDONSI and ATATA 1987).
Clay soils should be conducive to parasite development and intermediate hosts in
terms of the high water retention capacity and moister ground conditions (MABASO
et al. 2003). Additionally, clay soils can impede the vertical washout of parasite
stages into deeper soil layers where they become unavailable for infection
(MIZGAJASKA 1993). This would lead to higher parasite diversity and prevalence in
the hosts spending more time on clay soils.
2.1.2.4 Water bodies
Parasite diversity also depends on types and amounts of water bodies because
these may favour the development of intermediate hosts (PATZ et al. 2000; BUSH et
al. 2001). Especially arthropods, e.g. larva and pupa of mosquitoes (culids) and
Literature review
17
blackflies (Simulidae), crustraceans, but also leeches and intermediate hosts of
trematodes (molluscs) are intimately linked to the presence of water bodies (BUSH et
al. 2001). Size, temperature, acidity, dissolved oxygen, salinity, flow and
sedimentation may play an important role in parasite distribution (BUSH et al. 2001).
2.1.2.5 Habitat morphology
Habitat morphology like terrain inclination indirectly affects the occurrence of water
bodies or flowing water, sun exposure and temperature (PATZ et al. 2000;
SAATHOFF et al. 2005a). On flat terrain parasite diversity and prevalence is
expected to be higher: the chance of horizontal washout of the parasite stages
should be less and soil humidity should be generally higher than in steep terrain.
2.1.2.6 Resources for intermediate hosts and vectors
Deadwood and leaf litter represent important food resources and shelters for a great
variety of arthropods that can serve as intermediate hosts or vectors (HÖFER et al.
1996; GROVE 2002a; KELLY and SAMWAYS 2003). Additionally leaf litter and
deadwood can buffer fluctuations in humidity and temperature (SAYER 2006)
favouring survival and development of parasite stages on the ground. Therefore,
parasite diversity and prevalence should correlate positively with the abundance of
deadwood and leaf litter in the host’s environment.
Animal communities in leaf litter and also soil include a great variety of arthropods
representing all major taxa: arachnids, centi- and millipeds, insects (especially
collembolans, ants, flies, beetles, termites, true bugs), and crustaceans (PFEIFFER
1996; DALY et al. 1998). Additionally soil and plant debris offer a habitat for annelids,
bacteria, fungi and molluscs (DALY et al. 1998). Litter provides habitat for larval
stages of arthropods that later inhabit other forest strata (PFEIFFER 1996).
Deadwood is the essential resource of the saproxylic fauna (organisms that depend
on dead or dying wood (GROVE 2002a)) representing important intermediate host
taxa. Saproxylic organisms comprise all major insect orders (especially beetles and
flies) and account for a high proportion of insects in any natural forest (GROVE
2002a; KELLY and SAMWAYS 2003). But the saproxylic organisms also include
Literature review
18
fungi which are important food resources for numerous insect species (EHNSTRÖM
2001).
2.1.2.7 Vegetation type and density
Vegetation type and density play an important role for the abundance of intermediate
hosts. Vegetation density limits evaporation from the soil surface and reduces
exposure to solar radiation which favours parasite development (ROEPSTORFF and
MURRELL 1997; PATZ et al. 2000; BUSH et al. 2001; SAATHOFF et al. 2005a). The
parasite diversity and prevalence should be associated positively with vegetation
density in the host’s home ranges.
2.1.2.8 Predation
Predation on hosts and parasites directly affects the parasite abundance. Predation
on free-living parasite stages by earthworms, dung beetles, other arthropods, birds or
mammals has a strong impact on the parasite population (FINCHER 1973;
HAUSFATER and MEADE 1982; STOREY and PHILLIPS 1985; STROMBERG
1997; LARSEN and ROEPSTORFF 1999).
Likewise, predation on the hosts has a negative impact on parasite abundance: host
individuals with the highest parasite intensity seem to be more vulnerable to
predation (HUDSON et al. 1992). Host species with high predatory pressure should
therefore develop a higher parasite resistance. Consequently, these species are
expected to harbour a lower parasite diversity (WATVE and SUKUMAR 1995).
However, if predation enables trophic parasite transmission from the intermediate to
the definitive host, parasite populations would increase with higher predation
pressure on intermediate hosts (HOLMES 1995; POULIN 1995b; CEZILLY and
PERROT-MINNOT 2005; THOMAS et al. 2005).
2.1.3
Seasonality
Parasite diversity or prevalence can fluctuate seasonally (ROEPSTORFF and
MURRELL 1997; LARSEN and ROEPSTORFF 1999; PIERANGELI et al. 2003;
SÁNCHEZ THEVENET et al. 2004). Seasonally varying key factors for parasite
diversity may operate on host-intrinsic and -extrinsic factors as well as on the
Literature review
19
parasite itself. Most notably host-extrinsic climatic factors like humidity and
temperature can affect the survival of free-living parasites, the abundance of both
intermediate hosts and vectors and the host’s susceptibility. The viability of free-living
parasite stages is higher under moist and warm conditions (WHARTON 1979;
UDONSI and ATATA 1987; ROEPSTORFF and MURRELL 1997; BUSH et al. 2001;
BETHONY et al. 2006, see 2.1.2.1). The abundance of intermediate hosts, important
groups of arthropods and amphibians, is generally higher in warmer and more humid
seasons (TANAKA and TANAKA 1982; PEARSON and DERR 1986; SHELLY 1988;
FRITH and FRITH 1990; WATLING and DONNELLY 2002). Concerning the
favourable conditions for parasites and the resulting higher exposure risk, parasite
diversity and prevalence in this study should be higher in the rainy season. However,
also host-intrinsic factors can be affected by seasonal changes in temperature, day
length and resource distribution. Food shortage can result in a poorer nutritional
status, higher intra-specific competition which in turn can induce stress and impaired
immune reactions (2.1.1.10). Immune responses can also be modulated by changes
in temperature and photoperiods or reproduction related efforts (KLEIN 2000;
HUDSON et al. 2002; NELSON and DEMAS 2004; NUNN and ALTIZER 2006).
Considering the nutritional status of the studied hosts, parasite diversity and
prevalence should be higher in the dry season when food availability is low.
2.2
Intestinal parasite diversity in New World primates
This chapter reviews some general characteristics of intestinal protozoa and
helminths on life cycle, transmission mode, host specificity, location and
pathogenicity. Detailed descriptions of the spectrum of intestinal parasite species of
the studied New World primates, egg and larvae morphology for identification,
information on their life cycle and pathogenicity, other described host species and
their origin are provided in Appendix A.
2.2.1
Intestinal protozoa
Intestinal protozoa of New World primates belong to three different phyla:
Metamonada (including the genera Giardia, Chilomastix), Axostyla or Parabasala
Literature review
20
(Trichomonas,
Tritrichomonas,
Pentatrichomonas.),
Alveolata
(two
subphyla:
Apicomplexa (e.g. Isospora, Cryptosporidium) and Ciliophora (e.g. Balantidium)), and
Amoebozoa (Entamoeba, Endolimax, Iodamoeba) (TOFT and EBERHARD 1998;
ECKERT et al. 2005; SCHNIEDER and TENTER 2006). The life cycle of most
intestinal protozoa is direct: infective stages (cysts or oocysts) are ingested by
contact with infected hosts or via contaminated water or food items (ECKERT et al.
2005). Insects are reported to serve as transport hosts (TOFT and EBERHARD
1998). Reproduction in intestinal protozoa is usually asexual, only species of the
phyla Apicomplexa and Ciliophora also reproduce sexually involving micro- and
macrogametes or conjugation (ECKERT et al. 2000; BUSH et al. 2001; ECKERT et
al. 2005). Intestinal protozoa can have a broad host spectrum (euryxenous). For
example Giardia intestinalis can infect a great array of species of mammals, birds
and reptiles. Entamoeba histolytica (sensu latu) and Balantidium coli affect diverse
primate species, rats, cats and dogs (SHADDUCK and PAKES 1978; TOFT and
EBERHARD 1998; ECKERT et al. 2005). But some parasite species have very high
host specificity (stenoxenous) like Isospora callimico, Isospora cebi or Isospora
saimiriae affecting one single host species (Callimico goeldii, Cebus albifrons, Saimiri
sciureus respectively) (DUSZYNSKI et al. 1999). They inhabit generally small
(Giardia) or large intestine (Tritrichomonas, Balantidium), but can also dwell stomach
or adjacent organs like bile ducts, pancreatic ducts, gall bladder (Cryptosporidium,
Entamoeba histolytica sensu latu) (TOFT and EBERHARD 1998). Pathogenicity
varies highly across all protozoa taxa and also within one species: Balantidium coli
and Entamoeba dispar are apparently nonpathogenic, while Giardia intestinalis and
Cryptosporidium sp. can cause gastritis or enteritis. Entamoeba histolytica (sensu
latu) infection can be asymptomatic or produce severe diseases in primates (necroulcerative colitis, peritonitis, amoebic abscesses in liver, lung, central nervous
system) depending on multiple factors like parasite strain, host species, host body
condition, intestinal bacterial flora present and environmental factors (KING 1976;
SHADDUCK and PAKES 1978; TOFT and EBERHARD 1998).
Literature review
2.2.2
21
Intestinal helminths
Helminths comprise a very diverse group of metazoan parasites of the phyla
Platyhelmintha (with the digenean Trematoda, monogenean Cercomeromorpha and
Cestodea), Nematoda and Acanthocephala (SCHNIEDER and TENTER 2006).
2.2.2.1 Trematoda
Trematode infections are considered to be very rare and atypical in New World
primates (DUNN 1968; KING 1976). Around 11 species from five families are known
to infect New World monkeys (TOFT and EBERHARD 1998), e.g. Athesmia foxi,
Athesmia heterolecithoides, Zoonorchis goliath, Neodiplostomum tamarini and
Phaneropsolus orbicularis (detailed list see Appendix A). Trematodes exhibit a very
complex life cycle involving at least two hosts: intermediate hosts are usually
molluscs; definitive hosts are vertebrates (KUNTZ 1972; SHADDUCK and PAKES
1978; ECKERT et al. 2005). Trematode species can infect various primate genera
(polyxenous) (DUNN 1968; FLYNN 1973). Adult flukes reside in the intestinal lumen,
liver, bile ducts, gall bladder, mesenteric and other abdominal veins, lungs and rarely
in other organs (TOFT and EBERHARD 1998). Trematode infections with exception
of lung flukes and schistosomes may be less virulent than other helminths (KUNTZ
1972).
2.2.2.2 Cestoda
Cestodes are highly diverse and commonly infect New World monkey species (KING
1976). The characteristic cestodes are of the families Anoplocephalidae and
Davaineidae (DUNN 1968). At least 13 cestode species are identified to infect New
World monkeys (TOFT and EBERHARD 1998), e.g. Atriotaenia megastoma, Bertiella
mucronata,
Railletina
trinitatae,
Hymenolepis
diminuta,
Hymenolepis
nana,
Hymenolepis cebidarum (further information in Appendix A). Generally cestodes are
heteroxenous, except Hymenolepis nana that can also be transmitted indirectly, and
euryxenous (FLYNN 1973; KING 1976; SHADDUCK and PAKES 1978). Adult
cestodes are located in the small intestine but they are usually not very pathogenic
(DUNN 1963; 1968; KING 1976; SHADDUCK and PAKES 1978).
Literature review
22
2.2.2.3 Nematoda
Intestinal nematode diversity in New World monkeys is extremely high: to date,
approximately 68 species from six genera have been identified (TOFT and
EBERHARD 1998). Nematode species of the families Metastrongylidae (lungworms,
e.g. Angiostrongylus costaricensis, Filaroides barretoi), Trichostrongylidea (e.g.
Longistriata dubia, Molineus vexillarius, Molineus torulosus), Strongyloididae (e.g.
Strongyloides
cebus),
Oxyuridae
(pinworms,
e.g.
Trypanoxyuris
tamarini,
Trypanoxyuris callithricis) and Spiruridae (e.g. Trichospirura leptostoma, Spirura
guianensis, Spirura tamarini) are characteristic for Neotropical primates (DUNN
1968). A detailed list on nematode species infecting the study host species can be
found in Appendix A. Nematodes possess the highest variability in life cycles of all
helminths (BUSH et al. 2001). Some intestinal nematodes exhibit a direct life cycle
with diverse transmission strategies (ingestion of eggs, skin penetration, lactogenic
or intrauterine transmission); others have complex life cycles including free-living
generations (TOFT and EBERHARD 1998; BUSH et al. 2001). Regarding their host
specificity some nematodes are stenoxenous (family Oxyuridae), others can infect
various genera of primates (Strongyloides cebus, Longistriata dubia) (HUGOT et al.
1994; TOFT and EBERHARD 1998). The location of the nematodes is diverse as
well: they inhabit the oral cavity, oesophagus, stomach, pancreas (Spiruridae), small
intestine (Trichostrongyloidea, Spirurida), large intestine (Oxyurida, Trichuroidea) and
lungs (Metastrongylidae) (TOFT and EBERHARD 1998). Hence, also pathogenicity
is fairly variable: it can range from asymptomatic to severe pathologies like ulcerative
enteritis (Molineus torulosus) or lung haemorrhages (Filaroides sp., Strongyloides
cebus) (FLYNN 1973; TOFT and EBERHARD 1998).
2.2.2.4 Acanthocephala
Acanthocephalan infections are very characteristic for New World primates (DUNN
1968; KUNTZ and MYERS 1972; TOFT and EBERHARD 1998). Taxonomically it is a
less diverse parasite group represented by only one genus Prosthenorchis (KUNTZ
and MYERS 1972; SCHMIDT 1972; SHADDUCK and PAKES 1978; TOFT and
EBERHARD 1998). Acanthocephalans are heteroxenous: cockroaches and beetles
act as intermediate hosts (STUNKARD 1965b; SCHMIDT 1972; KING 1993;
Literature review
23
GOZALO 2003). They infect various species across most New World genera (DUNN
1968; KUNTZ and MYERS 1972; KIM and WOLF 1980). The adults of
Prosthenorchis sp. inhabit the ileum, caecum and colon (TOFT and EBERHARD
1998). Severe pathologies are associated with infections of Prosthenorchis elegans
(DUNN 1968; SCHMIDT 1972; TOFT and EBERHARD 1998). The adult worms can
provoke inflammation and perforation at the site of attachment resulting in peritonitis
and death (MENSCHEL and STROH 1963; RICHART and BENIRSCHKE 1963;
NELSON et al. 1966; SCHMIDT 1972; KIM and WOLF 1980; KING 1993; ECKERT
et al. 2005).
2.3
Study host species
2.3.1
Saguinus mystax and Saguinus fuscicollis
Saddle-back tamarins (Saguinus fuscicollis, Fig. 2.2 (A)) and moustached tamarins
(Saguinus mystax, Fig. 2.2 (B)) are two out of 15 species of the genus Saguinus
included in the family Callitrichidae (RYLANDS et al. 2000). S. mystax is the largest
member of this genus with a body mass ranging from 360 to 650 g (SOINI and SOINI
1990), and S. fuscicollis is the smallest species of this genus with 290 to 420 g
(HEYMANN 2003a). The geographic distribution of tamarins is in western and central
Amazonia west of Rio Madeira, in the Guyanas and northern Brazil, and in
northwestern Columbia, Panama, and southeastern Costa Rica (RYLANDS et al.
1993; HEYMANN 2003a). The subspecies Saguinus mystax mystax, to which the
study groups belong, ranges between the Río Ucayali in the west and the Rio Juruá
in the east (GROVES 2001). The subspecies Saguinus fuscicollis nigrifrons, to which
the other groups belong, ranges between the Río Ucayali in the west and the Río
Javari in the east, south of the Rio Solimoes as far as the Río Blanco
(HERSHKOVITZ 1977; GROVES 2001). Tamarins mainly occur in high-ground
primary rainforest (“terra firme”) interspersed with patches of secondary vegetation,
but can also range into mixed fruit-plantations (SOINI and SOINI 1990; HEYMANN
2003a). Where two species of tamarins occur sympatrically they commonly live in
stable mixed-species troops with only one other congeneric troop sharing and
Literature review
24
defending the same home range (TERBORGH 1983). S. mystax and S. fuscicollis
are frequently seen together and spend most of their time in such associations
(SMITH 1997; HEYMANN and BUCHANAN-SMITH 2000). Their common home
range comprises around 40 hectares (reviewed in SMITH 1997), but can vary
between 10 and 200 ha according to population (HEYMANN 2003a). The group size
of moustached tamarins varies between two to 12 individuals (SOINI and SOINI
1990; LÖTTKER et al. 2004a) and of saddle-back tamarins between three to 10
individuals, with one to two adults of each sex and their offspring from previous years
(SNOWDON and SOINI 1988; HEYMANN 2003a). Both tamarin species in the study
area exhibit a polyandrous mating system (GOLDIZEN 1989; HEYMANN and
BUCHANAN-SMITH 2000). Moustached and saddle-back tamarins feed on fruits,
insects, other arthropods, small vertebrates, nectar, soil, gums and other exudates
(SNOWDON and SOINI 1988; GARBER 1993; PERES 1993; NICKLE and
HEYMANN 1996; SMITH 1997; KNOGGE 1998; HEYMANN and BUCHANANSMITH 2000; HEYMANN et al. 2000; HEYMANN 2003a). They spend the night in
closed sleeping sites like Jessenia bataua palm trees and tree hollows, dense
epiphyte tangles and crotches (HEYMANN 1995; SMITH 1997). Sleeping sites are
usually changed on a daily basis, but they may also be reused repeatedly
(HEYMANN 1995; SMITH 1997; HEYMANN and BUCHANAN-SMITH 2000).
2.3.2
Callicebus cupreus
The red or coppery titi monkey (Callicebus cupreus, Fig. 2.2 (C)) is one of the 28
species of the genus Callicebus belonging to the Callicebus cupreus-group with five
other species (VAN ROOSMALEN et al. 2002). The genus belongs to its own
subfamily Callicebinae within the family Pitheciidae (RYLANDS et al. 2000; GROVES
2001). The body mass of an adult C. cupreus ranges from 750 to 1000 g (BICCAMARQUES et al. 2002). The geographic distribution of the genus Callicebus ranges
throughout most of the Amazon and Orinoco basin and the Atlantic forest of Eastern
Brazil (HERSHKOVITZ 1990). Callicebus is found in primary, riverine and remnant
forest in low altitudes (under 500 m elevation) (AQUINO and ENCARNACIÓN 1994).
It reaches the highest population densities in open forest areas, riparian forests and
Literature review
25
swamps (KINZEY 1981). Little is known about the species C. cupreus so that we
have to rely on information about other species of the Callicebus genus. Titi monkeys
are reported to range in areas from 0.5 (Callicebus moloch) to 29 ha (Callicebus
torquatus) (KINZEY 1981; ROBINSON et al. 1987). Daily path length of Callicebus
varies between 315 m (C. moloch) and 1500 m (C. torquatus) (KINZEY 1981).
Estimates on population density give three to 24 individuals per km² (KINZEY 1981).
It occupies relatively exclusive and stable home ranges with slight overlaps
(TERBORGH 1983; MAYEAUX et al. 2002). Callicebus is reported to be in frequent
association with tamarins (S. fuscicollis and Saguinus imperator) (KINZEY 1981).
They live in family groups and probably exhibit a monogamous mating system
(KINZEY 1981; TERBORGH 1983; MAYEAUX et al. 2002). In all studied Callicebus
species groups are formed by up to five individuals (KINZEY 1981; AQUINO and
ENCARNACIÓN 1994), exceptionally they were found in larger groups of seven
members (BICCA-MARQUES et al. 2002; MAYEAUX et al. 2002). Callicebus has a
generalized diet including fruits (pulp and seeds), insects, leaves and flowers
(KINZEY 1981; TERBORGH 1983; ROBINSON et al. 1987; AQUINO and
ENCARNACIÓN 1994; TIRADO HERRERA and HEYMANN 2003). They eat
immature leaves from trees and mature and immature leaves from lianas (AQUINO
and ENCARNACIÓN 1994). C. cupreus spends the night in closed microhabitats for
example holes in hollow trees or vine tangles (ROBINSON et al. 1987; NUNN and
HEYMANN 2005).
26
Literature review
Fig. 2.2 (A-C) Study host species A. S. fuscicollis, B. S. mystax, C. C. cupreus, photographed by
J. Diegmann (A, B) and M. Nadjafzadeh (C).
Literature review
2.4
27
Bias in parasitological studies
Scientific studies are almost invariably subject to systematic errors (bias). Biased
samples do not give a representative estimate of a study population and can
therefore be difficult to analyse or even lead to inaccurate results. As many authors
have remarked, errors in selection, processing or measurement of samples can be
important and frequent sources for bias in parasitological studies (e.g. GUEGAN and
KENNEDY 1993; WALTHER et al. 1995; GREGORY et al. 1996; NUNN et al. 2003;
KREIENBROCK and SCHACH 2005). In the following some sources of bias will be
outlined which can lead to essential deviations of parasitological results, especially if
they are based on non-invasive methods (e.g. faecal sampling). Types of bias can be
grouped into three categories: selection, information and confounding bias (GRIMES
and SCHULZ 2002; KREIENBROCK and SCHACH 2005).
2.4.1
Selection bias
This bias occurs during selection of the studied subpopulation resulting in a nonrepresentative conclusion about the target population (GRIMES and SCHULZ 2002;
KREIENBROCK and SCHACH 2005). In studies of wild host populations,
opportunistic sampling or selective sampling of a subset of individuals like road kill,
captured or hunted animals can be sources of selection bias. If in studies on freeranging hosts samples are not assigned to single individuals, prevalences or
individual PSR cannot be calculated accurately. In addition, it is known that sampling
effort correlates positive with parasite species richness (e.g. GUEGAN and
KENNEDY 1993; WALTHER et al. 1995; GREGORY et al. 1996; FELIU et al. 1997;
ARNEBERG 2002; NUNN et al. 2003; MUEHLENBEIN 2005).
2.4.2
Information bias
Information bias, also known as observation, classification, or measurement bias can
arise during processing and measuring the samples (GRIMES and SCHULZ 2002;
KREIENBROCK and SCHACH 2005). In parasitological analyses information bias
can emerge from non-standardized processing, e.g. variation in the concentration
procedure (WARNICK 1992), subjective sample examination, uneven examination
Literature review
28
effort in terms of the observer’s experience, the time budget and sample volume.
This type of bias can also be caused by imprecise measurements of size and number
of parasites.
2.4.3
Confounding bias
Confounders are mostly unknown factors which are associated to both disease
exposure and disease outcome. Confounding factors account for some of the
observed relationship between the two, but they are not affected by the exposure
(GRIMES and SCHULZ 2002; MCNAMEE 2003; KREIENBROCK and SCHACH
2005). Sampling hosts from different geographic regions, in different seasons or
under specific conditions affecting the host’s immune system can lead to confounder
problems. Disregarding confounders can lead to distortion of exposure-disease
relation. Especially in such complex ecosystems as the tropical rainforest, the risk of
neglecting important confounders is high.
2.5
Objectives of this study
In order to contribute to the knowledge of host-parasite interactions this study has
three major goals. Firstly, it aims to collect baseline data on the parasite spectrum of
three sympatric New World monkey species in the wild. Most information available on
the parasite spectrum in general is collected from laboratory or captured animals.
Data on intestinal parasites of S. mystax, S. fuscicollis and C. cupreus is very limited
and refers mostly to captured animals where exact origin and time spent in the
captivity are uncertain (DUNN 1962; 1963; NELSON et al. 1966; COSGROVE et al.
1968; PORTER 1972; KIM and WOLF 1980; HORNA and TANTALEÁN 1990;
TANTALEÁN et al. 1990; MICHAUD et al. 2003). Hitherto, there is only one
parasitological study published on wild S. fuscicollis (PHILLIPS et al. 2004).
Secondly, this study explores systematically the ecological determinants of parasite
diversity of sympatric host species. The influence of host-intrinsic and -extrinsic
factors on parasite species richness (PSR), prevalence and egg or larvae output are
examined on individual, group and host species level. Thirdly, in order to achieve the
two first goals it was aimed to establish standardized methods for parasitological
Literature review
29
analyses in terms of sample collection, processing and examination for the needs of
primatological field studies.
This comparative, year-round study is a potentially powerful approach to understand
the factors that determine parasite diversity for several reasons: a long-term study of
wild host populations with negligible anthropogenic impact is a better model to study
host-parasite interactions than experimental studies. Advantages of laboratory and
field studies can be combined: the complexity of the ecological interactions is not
reduced while the samples can be collected individually because hosts are
individually recognizable, and information about sex, age and life history is available.
Three primate species sharing the same habitat were studied at the same time in
order to control for confounding factors like predator pressure, resource availability,
climatic conditions, and other unknown geographical factors. Especially groups of the
two tamarin species have identical home ranges and spend the majority of their time
in association so that confounding effects can be minimized. The study period
included rainy and dry season which provides a more comprehensive insight into the
seasonal variation of parasite diversity.
This study addresses three main question complexes:
1. Do host-intrinsic factors play a role in determining PSR and prevalence?
The following factors are considered:
ƒ Host species
ƒ Host sex
ƒ Strata use
ƒ Diet composition
ƒ Nutritional status
ƒ Home-range size
ƒ Group size
ƒ Host density
Literature review
30
2. Do host-extrinsic and habitat characteristics influence PSR and prevalence?
The following factors are considered:
ƒ
Ground humidity
ƒ
Soil type
ƒ
Habitat morphology, especially ground inclination
ƒ
Resource distribution for intermediate hosts (e.g. leaf litter, deadwood)
ƒ
Vegetation density
3. What are predictors for variation in egg/larvae output?
ƒ
Does variation show a host-specific pattern?
ƒ
Does variation show a seasonal pattern?
If there is a seasonal pattern, is it correlated with
a) the host’s nutritional status?
b) environmental conditions that favour development and survival
of parasite stages or intermediate hosts?
From the theoretical background outlined in chapter 2.1, the following, not mutually
exclusive hypotheses and predictions are derived for factors that possibly influence
intestinal parasite diversity. For a better understanding the chapters to which the
hypotheses refer are given in parentheses.
A. Hypotheses concerning host-intrinsic factors
A.1 Host species hypothesis: PSR, prevalence and egg/larvae output is dependent
on the host species.
Prediction: PSR, prevalence and egg/larvae output is higher in the host
species that offers more diverse and conducive conditions to parasite
encounter, survival and reproduction.
Literature review
31
A.2 Sex hypothesis (2.1.1.2): The host’s sex has an influence on PSR and
prevalence.
Prediction: Male host individuals harbour more different parasite species
than females and exhibit higher prevalences.
A.3 Strata use hypothesis (2.1.1.8): The strata use of the hosts influences PSR and
prevalence.
Prediction: PSR and prevalence is positively correlated with time hosts
spend on the ground.
A.4 Diet hypothesis (2.1.1.9): The diet composition of the hosts plays a role in
determining PSR and prevalence.
Prediction: PSR and prevalence is positively associated with the proportion
of animal prey in diet.
A.5 Nutritional status hypothesis (2.1.1.10): PSR, prevalence and egg/larvae
output is affected by the nutritional status of the host.
Prediction: PSR, prevalence and egg/larvae output is higher in the season
when the host nutritional status is poor (dry season).
A.6 Home-range size hypothesis (2.1.1.11): PSR and prevalence is determined by
the host’s home-range size.
Prediction: Hosts with larger home ranges exhibit higher PSR, but lower
prevalences.
A.7 Group size hypothesis (2.1.1.6): PSR and prevalence is determined by the
host’s group size.
Prediction: Hosts living in larger groups have higher PSR and higher
prevalences.
A.8 Host density hypothesis (2.1.1.6): PSR and prevalence is determined by the
host’s density.
Prediction: Hosts living at higher densities have higher PSR and higher
prevalences.
Literature review
32
B. Hypotheses concerning host-extrinsic or habitat factors
B.1 Habitat use hypotheses: Habitat characteristics that are more conducive to
parasite stage survival or development and abundance of intermediate hosts shape
PSR and prevalence of the hosts that use this habitat.
Predictions:
(1) Humidity (2.1.2.1): The more time the hosts spend in areas of high
ground humidity the higher PSR and prevalence.
(2) Soil type (2.1.2.3): The time hosts spend on clay soil is positively
correlated with PSR and prevalence.
(3) Habitat morphology (2.1.2.5): The time hosts spend on flat terrain is
positively correlated with PSR and prevalence.
(4) Resources (2.1.2.6): The proportion of time the hosts are in areas of
high abundance of leaf litter and deadwood scales positively with PSR and
prevalence.
(5) Vegetation density (2.1.2.7): The higher the proportion of time the
hosts spend in areas of high vegetation density and dense understorey the
higher PSR and prevalence.
B.2 Environment hypothesis: Egg/larvae output is affected by environmental
conditions in which the parasite stages are excreted.
Prediction: Egg/larvae output is higher in the season where environmental
conditions are more conducive to survival of parasite stages and
abundance of intermediate hosts (rainy season).
Animals, materials and methods
33
3 ANIMALS, MATERIALS AND METHODS
3.1
Study site
The study was conducted at the Estación Biológica Quebrada Blanco (EBQB),
situated approximately 4°21’S and 73°09’ W on the right bank of Quebrada Blanco, a
white water tributary of the Río Tahuayo, in the Amazon lowlands of north-eastern
Peru. The study area is located in “bosque de altura” (ENCARNACIÓN 1985) and is
not subject to annual inundations. Based on its soil texture, nature of water,
geomorphology and dynamics of watercourse this area falls into the subcategories of
“bosque de terraza” and “bosque de colina” (ENCARNACIÓN 1985). Some lower
parts of the study area can be characterized as “palmal alto” or “aguajal de altura”
(ENCARNACIÓN 1985) dominated by palm trees (Mauritia flexuosa, Jessenia
bataua) in swampy areas. For further details see HEYMANN (1995). The study site
comprises approximately 100 ha and contains a grid system. This grid is based on
footpaths every 100 m, in direction from North to South and from East to West (Fig.
3.1).
3.2
Study animals
The subjects of this study were eight wild groups from three species of New World
primates: three groups of moustached tamarins (Saguinus mystax mystax), three
groups of saddle-back tamarins (Saguinus fuscicollis nigrifrons) and two groups of
red titi monkeys (Callicebus cupreus). Each of the three groups of moustached
tamarins lived in a mixed-species troop with a group of saddle-back tamarins. Groups
West of saddle-back and moustached tamarins have been under observation since
May 1999, groups East since January 2000, and groups North since October 2001.
The titi monkey group Casa was habituated when the observations started in October
2002, but had not been under routine observation. Habituation of group Puerto
started in September 2002, but the female of this group died on the 29th of
September 2002, and the remainder of the group disappeared in March 2003. Group
composition is provided in Table 3.1. Changes in group composition over time are
Animals, materials and methods
34
shown in Appendix B. Details of the population dynamics are available for the
moustached tamarins in LÖTTKER et al. (2004a). All group members were known
individually by natural markings (LÖTTKER et al. 2004a). Mean group size was
calculated as the mean number of individuals per group over the study period (Table
3.1). The range use of the study groups is depicted by 95% kernel home ranges
(HARRIS et al. 1990) which represent the area with a 95% probability to encounter
the group. For this purpose, the spatial data on group localization was collected
every 15 minutes during the observation time. The position within the grid system
was determined with a precision of 50 x 50 m. The Animal Movement extension to
ArcView 3.3 was used to perform the home range estimations (HOOGE and
EICHENLAUB 1997). The home ranges of all study groups are illustrated in Fig. 3.1.
Host density was then derived from the mean group size per home range size.
Table 3.1 Study group composition, initial and mean group size over the study period
Adults
Subadults
Juveniles
♀♀
♀♀
Group
♀♀
♂♂
Sf West
2
2
Sm West
1
2
Sf East
1
2
Sm East
1
5
Sf North
2
2
Sm North
2
2
Cc Casa
1
1
Cc Puerto
1
1
♂♂
Initial
group size
♂♂
1
Mean
group size
♀♂
5
5.4
3
3.5
4
5.3
8
6.7
4
4.9
5
5.8
1
3
3.8
1
3
-
1
2
1
Sf: S. fuscicollis, Sm: S. mystax, Cc: C. cupreus; age classification refers to the age when the
individual was first observed, for both Saguinus species the classes are defined by SOINI and SOINI
(1990), for Callicebus cupreus by MAYEAUX et al. (2002) and KINZEY(1981).
Animals, materials and methods
35
N
E
W
S
0
10
200
Camp
Fig. 3.1 Map of the grid system at the field site EBQB and 95% kernel home ranges of the study
groups. Red represents groups East, blue groups North, green groups West, orange Callicebus group
Casa. Dotted line comprises range of S. fuscicollis; solid lines represent S. mystax home ranges.
3.3
Study period
The study was carried out from June 2002 to August 2003. Habitat characterization,
behavioural data and faecal sample collection took place in this period. Callicebus
group Casa and tamarin group West were followed from October 2002 to August
2003. From Callicebus group Puerto faecal samples were collected between
September 2002 and March 2003. During that time unbiased behavioural data could
not be collected due to an insufficient habituation of the group. The other study
groups were followed during the whole study period. Faecal sample collection and
Animals, materials and methods
36
behavioural observation were carried out during the whole activity period of the
primates: from the time that they left their sleeping site (tamarins around 6:00h, titi
monkeys around 5:30 h) to the moment that they entered the next sleeping site in the
afternoon (around 16:00 h and 16:30 h, respectively). The study period included one
rainy and two dry seasons (first dry season: July to October 2002, rainy season:
March to June 2003, second dry season: July to September 2003).
3.4
Parasitological analyses
3.4.1 Faecal sample collection and preservation
Faecal samples of all individuals were collected as often as possible, at least three
times at three different days per rainy and dry season. The samples were put into
PET tubes immediately after defecation, in order to avoid contamination by egg
laying flies, soil or water. By observation of the defecating individuals and immediate
sample collection a correct match of the hosts with the collected faecal samples was
ensured. All vials were individually labelled with date and time of defecation, species,
group and identification of the defecating animal. The samples were weighed on
return to the camp, and then 10% neutral buffered formalin (solution of 10%
formaldehyde and sodium phosphate buffer, pH 7.0) was added to the faecal
material. The samples were stored at ambient temperature at EBQB, and at 4°C after
returning to the DPZ. Each sample was assigned to a specific identification category
(provided in Table 3.2) which describes the degree of accuracy of the individual
identification. Only samples of category “A” were considered for parasitological
analyses. Others were kept as spare samples for further analyses in case essential
samples were missing or preservation or centrifugation techniques failed. In total
2226 faecal samples were collected from the eight study groups. The total number of
faecal samples per study group and species and their proportion of identification
categories are depicted in Table 3.3.
Animals, materials and methods
37
Table 3.2 Identification categories for faecal samples
Identification
Description
category
accurate identification of the defecating individual, precise
A
localization of the faecal sample and immediate sample collection
accurate identification, but imprecise localization or delayed
B
collection of the sample
inaccurate identification, but precise localization and immediate
C
collection
Table 3.3 Faecal sample collection: total number of faecal samples per study group and species
and their proportion of identification categories
Group
Total number of
faecal samples
% of Asamples
% of Bsamples
% of Csamples
S. fuscicollis
West
340
64.4
6.2
29.4
S. fuscicollis
East
416
79.3
5.5
15.2
S. fuscicollis
North
286
81.8
5.3
12.9
Species
TOTAL Sf
1042
S. mystax
West
119
64.7
5.9
29.4
S. mystax
East
368
66.8
4.1
29.1
S. mystax
North
378
76.2
2.1
21.7
TOTAL Sm
865
C. cupreus
Casa
284
49.6
8.1
42.3
C. cupreus
Puerto
35
34.3
11.4
54.3
TOTAL Cc
319
38
Animals, materials and methods
3.4.2 Sedimentation procedure
The formalin-ethyl acetate-sedimentation technique was performed for all faecal
samples. The standard protocol (ASH et al. 1994) was followed except in some
points where adjustment to the special needs of this study was required. Faecal
solutions were homogenized very well before proceeding with the extraction and
analyses. Approximately 5 ml of faecal solution was strained through a polyamide
sieve with standardized mesh size (400 µm) into a 15 ml centrifuge tube. The
remnants were weighed separately for later reference to total faecal mass.
Subsequently more formalin was added to bring the total volume to 10 ml and the
faecal solution was stirred well again. About 3 ml of ethyl acetate was added and the
tube was shaken vigorously for 30 seconds before centrifugation. The power of
centrifugation for this centrifuge was calculated after a nomogram: 2200 rpm was the
equivalent for 500 g as recommended in the standard literature. The centrifugation
time was 10 minutes. Before pouring off the supernatant, the top layer of fat was
detached of the centrifuge tube. The tube was decanted and the layers of fat, debris,
ethyl acetate and formalin were discarded and the sediment with parasite propagules
was transferred into an Eppendorf tube and weighed. A second centrifugation was
not performed as recommended for small faecal amounts (ASH and ORIHEL 1987;
ASH et al. 1994). Given the low weight of the faecal samples (mean weight 1.24 g,
N=2191, SD=0.64, range: 0.12-6.5 g) and the fact that decanting the top layers after
centrifugation bears the risk of losing parasite stages the second centrifugation was
omitted in order to preserve as much faecal material as possible.
3.4.3 Microscopic examination
All microscopic examinations were done in a blind test. This means that all faecal
samples were number coded before starting the sedimentation procedure so that the
identification of the samples was unknown at each step of the parasitological
analysis. The processed samples were examined microscopically by taking 100 µl
sediment of each, and mixing it well with 50 µl of iodine (5%) in order to facilitate the
detection and recognition of cyst stages (ASH and ORIHEL 1987). The sediment was
examined for helminth eggs and larvae as well as protozoan cysts under three
Animals, materials and methods
39
22 mm-square cover slips at a magnification of 100 to 400 or 650. Each slide was
scanned systematically and thoroughly in lanes covering the whole area of the three
cover slips. The examination time was limited to 30-45 minutes per sample
(15 minutes additionally for protozoa). For all individuals three samples of different,
non-consecutive days of each season were examined. Because of the more timeconsuming examination for protozoa the analysis was restricted to a subset of faecal
samples: where possible two females and two males from each group and three
samples for each individual were examined (totally 84 samples of 28 individuals).
3.4.4 Intra-observer reliability test
In order to determine the degree of repeatability and precision of the microscopic
examination, an intra-observer-reliability test was performed: six samples were
selected, and 100 µl sediment of each sample was analysed for three times in a blind
test. All parasitic stages were counted in the same way as described above. Then the
Kendall Coefficient of Concordance (W) was calculated. It is a non-parametric test to
determine the consistency of three or more judgements of a multiple set of rankings
(MARTIN and BATESON 1993). W can range from 0 to 1, with 1 indicating perfect
agreement and 0 indicating total disagreement (MARTIN and BATESON 1993). In
this study, the intra-observer-reliability test revealed a very high agreement in the
three judging processes of the parasitic objects (W=0.95, N=3, p<0.001).
3.4.5 Qualitative and quantitative description of parasite diversity
3.4.5.1 Parasite identification
For identification mean egg size (length, width) was determined from 10 stages of the
same morpho-type per host if eggs were not damaged or deformed. Measurements
were made to the nearest 0.08 µm at a magnification of 400 using an ocular
micrometer fitted to a compound microscope. Egg and larvae morphology was
documented photographically (Axiophot, Olympus Camera DP50, software AnalySIS
3.0). Egg characteristics like shell structure, shape, colour and egg content were also
taken into account. If there was a unimodal distribution of the length and width of the
parasite stages within one host species or parasite sizes were included in the range
40
Animals, materials and methods
of the parasite of the other host species, it was assumed that this morpho-type
belonged to a single morpho-species. For each morpho-species per host species,
minimum and maximum size, median size and interquartile range (IQR) were
recorded. The median size and IQR were chosen to give a more representative
measure for the average when referring to data of a small sample size including
outliers (FOWLER et al. 1998).
The parasite identification is presented at the level of family or genus, because a
more detailed parasite identification based on microscopic examination of eggs,
larvae, cysts and oocysts is often unreliable (ASH and ORIHEL 1987; GILLESPIE et
al. 2005). In the case of the acanthocephalan parasite recovered from the intestine of
a dead female titi monkey, the binocular microscope examination led to identification
up to the species level (see chapter 3.6 and 4.5.1). The adult worm was identified
based on morphological criteria and location cited in the literature (SCHMIDT 1972;
SHADDUCK and PAKES 1978; BRACK 1987). Identification of the parasite from the
abdominal wall was also based on morphological features and location described in
the literature (NELSON et al. 1966; SELF and COSGROVE 1972; TOFT and
EBERHARD 1998), see chapter 3.6 and 4.5.3. Besides morphological characteristics
of the parasite stages recovered from the faecal samples and from the necropsy,
reports on geographical distribution and presence in wild S. mystax, S. fuscicollis and
C. cupreus or related primate species were taken into account. All this information on
possible parasite species was compiled from parasitological standard references
(e.g. BURROWS 1972; KUNTZ 1972; MYERS 1972; ORIHEL and SEIBOLD 1972;
SCHMIDT 1972; FLYNN 1973; SHADDUCK and PAKES 1978; BRACK 1987; TOFT
and EBERHARD 1998; ECKERT et al. 2005; SCHNIEDER 2006) or review articles
(e.g. DUNN 1963; 1968; KUNTZ 1982; YAGI et al. 1988; WOLFF 1990; GOZALO
2003) and specific papers. This list and the cited literature on which the final
identification was based on are provided in Appendix A. Furthermore, helminth
identification was done in collaboration with Prof. Dr. D. W. Büttner, Department of
Helminthology, Bernhard Nocht Institute for Tropical Medicine in Hamburg, Dr. C.
Epe, Department for Infectious Diseases, Institute of Parasitology, Hannover School
of Veterinary Medicine, Dr. M. Tantaleán Vidaurre, Faculty of Biological Sciences,
Animals, materials and methods
41
Universidad Nacional Mayor de San Marcos, Lima, Perú, and Dr. W. Tscherner,
Department of Parasitology, Tierpark Berlin Friedrichsfelde. The taxonomic
classification follows SCHNIEDER and TENTER (2006) if not otherwise noted.
3.4.5.2 Parasite species richness (PSR)
Parasite diversity is expressed as parasite species richness (PSR). This is the
number of different parasite species per host (BUSH et al. 1997). PSR is either given
as total PSR referring to the total number of different parasite species over the entire
study period or as seasonal PSR referring to the total number of different parasite
species in rainy or dry season. All host individuals from which at least three
unambiguous samples were available (category “A”, see Table 3.2) over the whole
study period were included for total PSR. For seasonal PSR only individuals that had
three “A” samples per season were included. If animals were present in two dry
seasons, the second dry season was chosen for which comparable data was also
available on C. cupreus.
3.4.5.3 Prevalence
Prevalence was given as the number of hosts infected with one or more individuals of
a particular parasite species or taxonomic group divided by the number of hosts
examined. It is usually expressed as percentage or proportion (MARGOLIS et al.
1982; BUSH et al. 1997). On the individual level, prevalence was defined either as
the presence or absence of a specific parasite over the whole study period or over a
specific season. The sample selection was conducted in the same way as described
for PSR (3.4.5.2).
3.4.5.4 Egg or larvae output
The total number of parasite stages per 100 µl faecal sediment was given as a
standard unit for egg or larvae output. This refers to the number of eggs or larvae of
one parasite species in the faecal sediment after the removal of feeding residuals
during the sedimentation procedure. If there were more than 200 propagules of one
morpho-species under the first cover slip and the other cover slip areas were similar
in parasite density, the number of counted propagules was multiplied by three as an
estimate. For descriptive statistics all samples prepared by the standardized methods
Animals, materials and methods
42
were taken into account, at maximum three samples per individual per season. For
comparing the seasonal egg or larvae output per parasite species, the mean output
was calculated from exactly three samples of each individual in each season (two dry
and one rainy season).
3.5
Behavioural observations
The tamarin groups were followed for three consecutive days each month.
Observations were carried out on 182 days yielding a total of 1730 contact hours
(Table 3.4). The Callicebus groups were followed for five days per month. In total the
Callicebus group Casa was observed for 47 days yielding 403 contact hours (Table
3.4). For group Puerto no unbiased behavioural data could be collected because they
disappeared from the study area in March 2002 before the process of habituation
had been accomplished.
Table 3.4 Contact time for behavioural observations for all study groups
Species
Group
Overall contact time (in h)
S. fuscicollis
West
230
S. fuscicollis
East
370
S. fuscicollis
North
316
S. mystax
West
160
S. mystax
East
384
S. mystax
North
270
C. cupreus
Casa
403
Behavioural data were recorded by “instantaneous scan sampling” (MARTIN and
BATESON 1993): every 15 minutes the group was scanned and the activity of all
visible individuals, their height in the forest and their location in the grid system were
recorded during the scanning period of two minute duration. Two minutes are an
Animals, materials and methods
43
appropriate scanning period for rather dispersed groups of small-sized primates
(MARTIN and BATESON 1993). A 15 minute-interval generates independent data for
group positions because in this time period the group is potentially able to reach
every point of its home range. The following activity categories were recorded:
locomotion, feeding, foraging, grooming and resting (definitions are provided in Table
3.5). If animals were feeding also the category of the food object was recorded (fruit,
animal prey, exudate, leaf, nectar, seeds, soil, others). The behaviour of dependent
infants was not recorded up to the age of approximately three months.
For each scan all recorded activity categories were taken as a percentage of all
active individuals seen in this specific scan. Across all scans the mean was
calculated per category and per season and entire study period. If animals were
observed feeding, the animals’ food object was expressed as proportion of all food
objects which were consumed in this scan. Again means were computed over all
scans in which feeding activity was recorded. This method was chosen in order to
avoid underestimation of the proportion of consumed animal prey. Feeding on animal
prey is likely to be underestimated because it is an individual activity of short
duration. So if in one scan a single individual is seen ingesting animal prey it
accounts for 100% of feeding activity. By this procedure, it receives the same weight
as if all observed individuals were feeding together on a fruit tree.
Height in forest strata was grouped into nine categories (ground, >0-3 m, >3-6 m, >69 m, >9-12 m, >12-15 m, >15-18 m and >18 m). At each scan the height of all
animals was estimated from the ground and all individuals at the same height
category were summed up. Over all scans the sum of specific height use was
expressed as a percentage of all scan events.
Animals, materials and methods
44
Table 3.5 Description of activity categories applied in the “instantaneous scan sampling” (MARTIN
and BATESON 1993)
Activity
Description
categories
1. Locomotion
movements that result in a displacement of at least two times the body length,
including walking, running, jumping but also movements associated with
playing and scent marking
2. Feeding
manipulation of food items, biting, chewing and swallowing
3. Foraging
searching and hunting for animal prey, e.g. visual inspection and manipulation
of substrates, and investigation of tree holes, bromeliads etc.
4. Grooming
one individual picks through the hair of another individual (allogrooming) or of
itself (autogrooming) with its hands or mouth
5. Resting
3.6
sitting or laying with no activity corresponding to 1.- 4.
Post-mortem examination
A post-mortem examination was performed on a female titi monkey of the Puerto
group immediately after its death. After exenteration the intestinal tract was entirely
opened and washed in formalin to remove the ingesta and parasites. The intestinal
content and any parasite stages were stored separately for subsequent
parasitological analyses. All organs were measured and weighed. The pathological
findings were described and documented photographically. A spectrum of
representative tissue samples was taken from all organ systems and fixed in 10%
buffered formalin.
Further sample processing for histological examinations was conducted at the
Department of Infectious Pathology of the German Primate Centre (DPZ) and the
Department of Helminthology of the Bernhard Nocht Institute for Tropical Medicine.
Tissue samples of brain, liver, kidneys, heart, stomach, small and large intestine,
pancreas, adrenal gland were automatically paraffin-embedded (Hypercenter XP,
Thermo Shandon, Frankfurt/Main, Germany), sectioned at 3 µm and stained with
haematoxylin-eosin (H.&E.). In addition, sections of liver, spleen and intestine were
Animals, materials and methods
45
stained with Ziehl-Neelsen, Grocott, Periodic Acid Schiff reaction (PAS) and Giemsa
for detection of bacterial, fungal and protozoan structures. The sections of the
abdominal cyst were stained with Masson’s Trichrome stain. The histological
analyses were performed by light microscopic examination. Histopathological
findings were recorded in an examination protocol and were documented
photographically (Axiophot, Olympus Camera DP50, software AnalySIS 3.0).
Scanning electron microscope pictures of adult parasites recovered from the intestine
were taken at the Bernhard Nocht Institute for Tropical Medicine.
3.7
Habitat characterization
The term “habitat” is used as the sum of resources and conditions present in an area
that is occupied by certain species (sensu HALL et al. 1997). From the multitude of
biological and physical components some parameters were selected which were
thought to affect parasite diversity. Sampling points (spn) were set covering the home
ranges of all study groups in order to assess the following habitat variables: ground
drainage, soil type, ground inclination, leaf litter height, deadwood abundance,
vegetation and understorey density. For this purpose all sampling points were
arranged systematically along the established grid system. The quadrants of 100 x
100 m were divided into four sub-quadrants and four sampling points were set up at
the centre of each sub-quadrant (Fig. 3.2). From each sampling point (spn) the
surrounding area was divided into four sections by the compass bearing in all four
cardinal directions. Each sampling point describes the habitat variables for an area of
50 by 50 m. All habitat variables were recorded within the rainy season 2003.
Animals, materials and methods
46
NW1
NW2
WN3
N
Sp3
Sp4
N
Sp2
Sp1
WN2
=d
50 m
Fig. 3.2 Setup of the sampling points and point-quarter method for vegetation density
estimation. spn = sampling point; d = distance from sp to the trunk surface, N= North, WN2, NW1 etc.
marked trail from grid system
3.7.1 Drainage
The drainage was estimated at five meters distance to the sampling point in direction
SE, SW, NE and NW. At this point of measurement, in the following referred to as
POM, the drainage was determined as good (1) or poor (0) by considering the
presence of stagnant water and ground humidity. For description of the drainage
Animals, materials and methods
47
properties of one sub-quadrant the values were averaged and grouped into three
categories: poor (0-0.25), intermediate (0.5-0.75) and good (1).
3.7.2 Soil type
At the sampling point the soil type of the superficial layer was determined. The soil
layer was penetrated up to 15 to 20 cm depth. The substrate was described in three
categories according to the soil colour and texture: clay soil, sandy soil and mixed
soil. Sandy soil was considered to be of coarse particles, well separated, free
draining, with a light colour. Clay soil was denominated soil out of very fine particles,
compact, waterlogged, clumped when wet and of a yellowish or reddish tint. Soil
samples with intermediate characteristics between clay and sandy soil were
denominated mixed soil. In areas of stagnant water bodies and accumulation of
decaying material, the soil was denominated swampy.
3.7.3 Ground inclination
The ground inclination was assessed by measuring the height differences from the
sampling point to the four POMs. If there was less than 50 cm of height difference,
the inclination was considered 0-10%, if the difference was 50-100 cm, inclination
was 10-20% and if the difference was greater than 100 cm, inclination was annotated
with >20%. To study the habitat use, values were averaged and categories were built
for the ground inclination of the single sub-quadrant: it was grouped into flat (0-5%),
intermediate (>5-20%) and steep (>20%).
3.7.4 Height of leaf litter
The height of leaf litter and organic debris was measured at the four POMs. The
debris layer was perforated until reaching the forest ground with a sharp pointed
pole. The height was measured in cm, and averaged over the four sections and
sorted into four categories (0-5 cm, 5-10 cm, 10-15 cm, >15 cm).
48
Animals, materials and methods
3.7.5 Deadwood abundance
At each sampling point, the abundance of deadwood was recorded. This was done
according to tree diameter (trees between 30 and 100 cm in diameter account for
one tree unit, trees greater than 100 cm diameter account for two units) and the
number of trees present. Three groups were used to classify the abundance at the
sampling point (0=no tree unit present, 1=one tree unit, 2=more than one unit).
3.7.6 Vegetation density
The point-quarter method was employed to estimate the vegetation density of the
habitat by using distances from the sampling points to the nearest plants (KREBS
1999). In each quarter of the sub-quadrant, the distance from the nearest plant to the
sampling point was measured and recorded whether it was a tree or a palm tree
(description displayed in Fig. 3.2). The following instructions were carried out: plants
were measured that had a diameter at breast height (DBH) of more than 10 cm.
Breast height is defined as 1.30 m from the ground. DBH was calculated from the
stem circumference. To measure the stem circumference a pole was pushed firmly
into the ground. If the tree was buttressed or stilt rooted at 1.30 m height the stem
was measured above the top of the buttress or root. If this was not possible the
circumference was estimated above the buttress or root. Trees that were fluted for
their entire length were measured at breast height. If a tree had multiple stems, all
stems of more than 10 cm DBH were recorded and the mean diameter and distance
of all stems was calculated. In order to compute the vegetation density the following
procedure was applied: tree circumference was transformed into radius r. Since it
was impossible to measure exactly the distance D from the sampling point to the
centre of the trunks, the radius r of the trunk was added to the distance of the
sampling point to the surface of the closest trunk in each section (d1 – d4). Mean
distance D was calculated as shown in equation (1). The mean area where a single
plant occurs is equal to the mean distance D squared (GANZHORN 2003). Thus,
theoretically each plant covers an area mean D². The density of plants (Np) per unit
area (A) is then computed following equation (2). The absolute density of trees is
defined as the number of trees per unit area. Since it is usually expressed as the
Animals, materials and methods
49
number of trees per hectare the values were subsequently transformed into this unit.
In order to compare the habitat use of all study groups the vegetation density was
transformed into the following five categories: very low (<400 trees/ha), low (400-800)
intermediate (800-1200), high (1200-2000) and very high (>2000).
1 N
Mean D = ∑ (d i + ri )
N i =1
Equation (1)
D = distance from the sampling point to the tree centre
d = distance from the sampling point to the tree surface
r = radius of the tree
N = number of trees measured at the sampling point (N=4)
Np =
A
mean D 2
Equation (2)
N p = estimate of tree density at the sampling point
A = sampled area, here sub-quadrant of 2500 m²
3.7.7 Understorey density
The density of the understorey (vegetation less than three meters of height) was
estimated at the POM. The understorey density was ranked according to the relative
visibility of the field assistant. It was assigned four ranks: 0=almost full visibility,
1=half visibility, 2=very limited visibility, 3=no visibility. For the analyses of habitat use
the categories low (density average per sub-quadrant: <1), intermediate (1-1.75) and
high (>2) were employed.
3.8
Climate
Data on precipitation (in mm) was recorded with a rain gauge located on the clearing
of the camp and the minimum and maximum temperature (in °C) by a minimum-
Animals, materials and methods
50
maximum thermometer situated in a shaded place at the camp site. These variables
were recorded daily throughout the study period.
3.9
Phenology
Food abundance was evaluated by the phenological trail method (CHAPMAN and
WRANGHAM 1994; GANZHORN 2003). This method provides a relative measure of
food productivity of the forest and food availability for the primates (CHAPMAN 1992;
STEVENSON et al. 1998). Since trapping of the study animals would have been
incompatible with behavioural observations and faecal sampling the seasonal food
availability was used as a surrogate for the nutritional status of the host individuals.
The abundance of dietary plant parts was monitored, such as fruit, flowers and young
leaves of 220 plant individuals belonging to 113 different species of key feeding trees
of the three primate species. Phenological data on the feeding trees were recorded
by an experienced field assistant once per month during two consecutive days, on a
regular basis throughout the whole study period. The feeding plants had been
selected previously as a representative subset of feeding plants of all three primate
species. The abundance of leaves, fruit and flowers was ranked on a relative scale
from 0 to 3 modified from HEIDUCK (1997) (0=none, 1=few, 2=moderate,
3=abundant). Fruit, flower or leaf availability per month was calculated as the sum of
the assigned abundance ranks of the specific food item divided by the total number
of monitored trees in this period (GANZHORN 2003).
3.10
Statistical analyses
All statistical analyses were done using SPSS 12.0 (SPSS Inc.) except the
nonparametric repeated measures analysis of variance (ANOVA) and the ranked ttest for unequal variances (Satterthwaite) which were performed in SAS (version
9.1). Parametric tests were conducted whenever possible. If tests showed that data
did not meet the required assumptions, equivalent non-parametric tests were
performed. All tests were two-tailed and significance levels were set to α=0.05. The
Animals, materials and methods
51
p-values in multiple comparisons were adjusted by the Bonferroni procedure to
control for type I error.
3.10.1 Parasite morphology
Differences in sizes of the parasite morpho-species over the host species were
tested by using the Kruskal-Wallis test or Mann-Whitney U-test, respectively. Length
and width of parasite taxa varied significantly between host species in the case of
small spirurids and strongylids (Appendix C). Since the maximum variance was less
than 7% of the medians and/or less than reported in the references (Appendix A), the
morpho-types were grouped into one single species.
3.10.2 PSR and prevalence
In order to detect the general effects on parasite species richness (PSR) a nonparametric repeated measures analysis of variance (ANOVA) was conducted. Host
species, season and home range entered the model as independent variables and
their main effects and interaction effects were analysed. Firstly, all tamarin groups
and titi monkey group Casa were included. The C. cupreus group Puerto was
excluded because it was only present in one season. Since in the home range of
group Casa no other host species than C. cupreus occurred, the influence of host
species and home range could not be disentangled in this case. Thus, a second
ANOVA was conducted including the tamarin species that formed mixed-species
troops in the three home ranges. In case a significant effect was detected, a ranked ttest for unequal variances was conducted as a post-hoc test. Since PSR considers
only the number of different parasite taxa in the following the differences in
prevalence of all parasite species were examined separately: to analyse prevalence
differences between the species, home ranges or groups, Chi square (χ²) test or a
Fisher’s Exact test (extension by Freeman and Halton for more than two categories)
was conducted. In order to detect differences in parasite prevalences over the
seasons, a McNemar’s test for paired samples was performed using binomial data on
parasite presence/absence.
52
Animals, materials and methods
Sex differences in PSR were examined by using the Mann-Whitney U-test. To
analyse differences in parasite prevalence between the sexes a Fisher’s Exact test
was performed. To determine the extent of sex bias in prevalence, the prevalence of
females was subtracted from the prevalence of males for each parasite taxon and
host species separately. A one sample t-test was used to test if the mean value of
sex bias over all parasite taxa differed from zero (meaning no sex bias).
In order to explore factors that can cause possible differences of PSR/prevalence
over the host species or home ranges, data of all host species was examined by
using the Spearman rank correlation calculations. The hypotheses presented before
(chapter 2.5) predict specific relationships between host-intrinsic/-extrinsic variables
and PSR/prevalence that should be primarily similar for the studied host species
belonging all to the New World primates. Thus, even though species might be
expected to differ in the magnitude of relationships, there is no a-priori reason why
species should differ fundamentally in the direction of the relationship. Hence, the
examined host-intrinsic variables are expected to have a similar outcome on the
exposed individuals, independent from their species. Data of all species was
therefore analysed together. Since there were no significant effects of the host
groups within all host species on PSR (ANOVA F2,27=1.17, p=0.307, see chapter 4.3,
Table 4.4 and 4.5) the same effects of host-intrinsic and –extrinsic traits on parasite
diversity were expected for all host individuals. The same should be true for habitat
use: since the results revealed no significant effects of three different home ranges
(West, East, North; ANOVA F2,36=1.23, p=0.312, chapter 4.3, Table 4.4) or significant
interactive effects of home range and species (ANOVA F2,36=0.44, p=0.633, see
Results, Table 4.4) on PSR, there was no reason to expect diverging effects of
habitat use in different home ranges at the field site. In order to assure this pattern
found in the first analyses, in a second step the rank correlation coefficients were
determined by excluding the Callicebus species. Since for the second group of
Callicebus group no data could be collected, the analyses were repeated without this
species to exclude the possibility that general patterns were driven by nonrepresentative data from one host species. The second analysis excluding the
Callicebus further allowed drawing conclusions about consistency of the observed
Animals, materials and methods
53
pattern within phylogenetically closely related hosts (genus Saguinus). Since the
tamarin species shared all recovered parasite taxa and many socio-ecological and
immunological traits which might have an impact on their parasite diversity examining
an association of parasite diversity and host-intrinsic and habitat factors with a
balanced number of host individuals of both species can strengthen the detected
patterns.
In order to analyse the relationship between PSR/ parasite prevalences and the hostintrinsic factors the Spearman's Rank Correlation Coefficient (rs) was calculated. The
following independent variables were examined: strata use (percent of time hosts
spent on the ground), diet (proportion of animal prey), mean group size, home-range
size and host density. Of these independent variables proportion of animal prey and
home-range size (N=42, rs=0.71, p<0.001) showed a strong intercorrelation (a table
of correlations between independent variables is provided in Appendix D).
To examine the relationship between PSR, parasite prevalences and habitat use a
Spearman's Rank Correlation was conducted. The Correlation Coefficient (rs) was
calculated for PSR, parasite prevalence and the time the hosts stayed in areas of the
following habitat characteristics: dense vegetation (more than 1200 trees per ha),
high understorey density, high leaf litter layer (more than 10 cm), clay soil, poor
drainage (score 0-0.25), flat terrain (0-5% inclination) and high deadwood abundance
(one and more tree units per sampling point). The frequency of use of some habitat
characteristics showed a strong multicollinearity (results are displayed in Appendix
D).
3.10.3 Egg/larvae output
Data on mean parasite stages per season were log (n+1)–transformed to meet
criteria of normality. A General Linear Mixed Model (GLMM) was used to analyse the
effects of categorical variables (species and season) on a dependent continuous
variable (mean egg or larvae output) of each individual. T-tests for independent
samples (in case of comparing species) or dependent samples (in case of
comparison between seasons) were employed as post hoc tests.
54
Animals, materials and methods
3.10.4 Behavioural observations and phenology
Wilcoxon’s test for matched pairs was employed to study the differences of diet
composition over both seasons for all host species. Comparison of the relative food
availability in rainy and dry season was carried out by the t-test for dependent
samples.
Results
55
4 RESULTS
4.1
Parasite diversity
Saguinus fuscicollis and Saguinus mystax harboured seven intestinal parasite taxa
while Callicebus cupreus harboured four (see Table 4.1). Nematodes, cestodes and
acanthocephalans were found in both Saguinus species. In C. cupreus cestodes
were lacking. Trematodes and intestinal protozoa were not detected in either of the
studied host species. Nematodes were dominant among the intestinal helminth fauna
of the three studied primate species. Adult acanthocephalan parasites of the species
Prosthenorchis elegans, and a pentastomid larva were found incidentally at the
necropsy of a female C. cupreus (see chapter 3.6 and 4.5). The pentastomid is not
an intestinal parasite of the studied primates and thus was excluded from the
analyses. The other recovered parasite taxa are described more detailed in the
following chapters.
4.1.1
Helminths
Seven different helminth taxa were recovered from altogether 432 faecal samples of
45 host individuals: one acanthocephalan species, two cestode species and four
nematode species (Table 4.1). The helminth taxa were identified as follows: the
acanthocephalan species was Prosthenorchis elegans. One cestode taxon belonged
to the family Hymenolepididae, it probably was Hymenolepis cebidarum. The
identification of the other cestode species remained uncertain (in the following simply
referred to as cestode sp. #2). The nematode taxa were represented by four morphospecies: two taxa of the order Spirurida: a large spirurid, probably Gongylonema sp.
or Trichospirura leptostoma and a small spirurid which could not be determined
further. Nematode eggs belonging to the polyphyletic group of the “strongylids” were
found. “Strongylids” comprise the orders Rhabditida and Tylenchida (Strongylida).
The morpho-species was narrowed down to Molineus sp. and Strongyloides cebus.
The detected nematode larvae belong either to the group of “strongylids”, probably of
the genus Strongyloides, or to the superfamily Metastrongyloidea (genus Filaroides
or Angiostrongylus). For convenience this taxon was referred to as nematode larvae.
The identification of the recovered helminth taxa, their taxonomy and the study host
56
Results
species from which they were recovered, are summarized in Table 4.1. The
information on which the parasite identification is based on (morphological
characteristics, description of potential host species and their origin) including
references is given in Appendix A. The descriptive statistics of length and width for
each parasite morpho-species are presented in Table 4.2. Nematode larvae are not
included in this table because their identification was not primarily based on size but
on other morphological features. Results of the statistical comparisons of the parasite
sizes are provided in Appendix C. Light microscopical photographs of all parasite
taxa are presented in Fig. 4.1 (A-F) and 4.2 (A,B). Fig. 4.3 shows a scanning electron
microscope (SEM) picture of an adult P. elegans.
Results
57
Fig. 4.1 (A-F) Light microscope pictures of parasite eggs recovered from faecal samples of all host
species. A. P. elegans, B. Hymenolepis sp., C. cestode sp. #2, D. small spirurid, E. large spirurid, F.
“strongylid”; scale bar = 25 µm
58
Results
Fig. 4.2 Light microscope pictures of two nematode larvae recovered from faecal samples of all
host species. A. posterior, pointed end, B. anterior end (oesophagus); scale bar = 50 µm
Fig. 4.3 SEM picture of adult P. elegans recovered from necropsy of a titi monkey. Anterior end with
collar of festoons and proboscis armed with spiral rows of five to seven hooks; scale bar = 100 µm.
Parasite identification
Phylum/Class
Order/Family
Species or genus
Infected
study host
species
Acanthocephala/
Archiacanthocephalea
Oligacanthorhynchida/
Oligacanthorhynchidae
Prosthenorchis elegans
Sf, Sm, Cc
2. Hymenolepis sp.
Platyhelmintha/Cestodea
Cyclophyllida/Hymenolepididae
Hymenolepis cebidarum
Sf, Sm
3. Cestode sp. #2
Platyhelmintha/Cestodea
Cyclophyllida/Anoplocephalidae1
Paratriotaenia sp.
Sf, Sm
4. Small spirurida
Nematoda/Chromadorea
Spirurida/unknown
unknown
Sf, Sm, Cc
5. Large spirurida
Nematoda/Chromadorea
1. Spirurida/Gongylonematidae
a) Gongylonema sp.
Sf, Sm
2. Spirurida/Rhabdochonidae1
b) Trichospirura leptostoma
1. Tylenchida/Strongyloididae
a) Strongyloides cebus
2. Rhabditida/Trichostrongylidae
b) Molineus sp.
1. Tylenchida/Strongyloididae
a) Strongyloides sp.
2. Rhabditida/Metastrongylidae
b) Filaroides sp.
3. Rhabditida/Metastrongylidae
c) Angiostrongylus costaricensis
Parasite morphospecies
1. Prosthenorchis
elegans
6. “Strongylids”
7. Nematode larvae
Nematoda/Chromadorea
Nematoda/Chromadorea
Results
Table 4.1 Parasite identification and the infected study host species
Sf, Sm, Cc
Sf, Sm, Cc
Sf: S. fuscicollis, Sm: S. mystax, Cc: C. cupreus. Letters a)-c) give the probable parasite identification. Taxonomy follows SCHNIEDER and
TENTER (2006) if not noted otherwise. 1 TOFT and EBERHARD (1998)
59
Results
60
Table 4.2 Descriptive statistics of length and width for eggs of six parasite morpho-species.
N gives the number of parasite stages measured. Median, minimum, maximum and IQR (interquartile
ranges) are presented for each parasite taxon and host species in µm.
Parameter
S. fuscicollis
S. mystax
C. cupreus
length
width
length
width
length
width
12
12
6
6
-
-
Median
69.4
39.0
70.2
41.9
Minimum
63.2
37.4
66.3
34.3
Maximum
74.5
43.3
74.1
44.5
IQR
6.5
3.8
6.3
6.1
56
56
4
4
-
-
Median
29.6
23.4
30.1
24.2
Minimum
21.8
16.1
28.1
21.1
Maximum
43.7
30.0
31.2
25.7
IQR
2.3
3.0
2.9
3.9
2
2
12
12
-
-
Median
65.2
58.9
66.1
54.6
Minimum
62.1
57.7
56.6
39.0
Maximum
68.3
60.0
74.1
64.0
IQR
6.2
2.3
9.1
9.8
77
77
77
77
71
71
Median
26.5
11.7
26.9
11.7
25.0
11.7
Minimum
21.8
10.1
15.6
9.6
21.1
9.8
Maximum
33.9
17.6
34.3
19.5
35.9
14.0
IQR
2.7
1.1
4.1
1.2
3.1
1.2
Prosthenorchis
elegans
N
Hymenolepis sp.
(oncosphere)
N
Cestode sp. #2
N
Small spirurids
N
Results
61
Parameter
Large spirurids
S. fuscicollis
S. mystax
C. cupreus
length
width
length
width
length
width
8
8
8
8
-
-
Median
57.7
23.4
57.5
32.8
Minimum
42.9
21.8
54.6
31.2
Maximum
64.4
33.5
59.3
33.9
IQR
8.3
10.1
1.5
0.4
88
88
47
47
27
27
Median
51.5
33.5
52.3
33.2
54.6
36.6
Minimum
46.8
28.9
46.8
23.4
49.9
33.2
Maximum
75.7
50.7
60.5
35.9
72.5
46.8
IQR
3.4
3.1
4.7
1.6
2.3
2.3
N
"Strongylids"
N
4.1.2
Protozoa
In a total of 84 samples for a subset of 28 individuals no protozoan oocysts/cysts or
trophozoites were found over all seasons.
4.2
Parasite ecology
Ecological data for the parasite taxa recovered from the three study host species is
compiled from the literature. In order to explore determinants of parasite diversity it is
essential to gather information on life cycle, potential intermediate hosts,
transmission modes, host specificity and potential primate host species (Table 4.3).
The references for the recovered parasite taxa can be found under the specific
parasite in Appendix A.
Table 4.3 Ecology of detected parasite taxa including life cycle, intermediate hosts and transmission modes, host specificity and potential
primate host species (the latter is written in brackets). * denotes potential intermediate hosts from closely related parasite species. Letters a) and b)
give the probable parasite identification.
Life
cycle
Potential intermediate hosts
Transmission mode
Host specificity (potential
primate host species)
indirect
Blattodea: Blatella sp.; Anobiidae:
Lasioderma sp., Stegobium sp.; other
Coleoptera
ingestion of intermediate
host
polyxenous (Alouatta, Aotus, Ateles,
Callicebus, Callithrix, Cebuella, Cebus,
Lagothrix, Leontopithecus, Saguinus,
Saimiri)
Hymenolepis sp.
indirect
* Coleoptera: Tenebrio sp.;
Siphonaptera: Xenopsylla sp.,
Ctenocephalides sp.; Lepidoptera:
Pyralis sp.; other arthropods
ingestion of intermediate
host
Cestode sp. #2
Paratriotaenia sp.
indirect
insects
ingestion of intermediate
host
polyxenous (Callimico, Callithrix,
Saguinus)
Small spirurid
indirect?
?
probably ingestion of
intermediate host
?
Blattodea, Coleoptera
ingestion of intermediate
host
polyxenous (Aotus, Ateles, Callicebus,
Callimico, Callithrix, Cebuella, Cebus,
Saguinus, Saimiri)
none
skin penetration or
ingestion of larva
polyxenous (Alouatta, Ateles,
Cebuella, Cebus, Lagothrix, Saguinus,
Saimiri, other Callitrichidae)
molluscs (slugs:Vaginulus sp.; snails)
ingestion of intermediate
host or mucus
contaminated food items
polyxenous (Alouatta, Ateles,
Cebuella, Cebus, Saimiri, Callithrix,
Lagothrix, Saguinus, other Callitrichidae
and Cebidae)
skin penetration or
ingestion of larva
polyxenous (Alouatta, Aotus, Ateles,
Cebuella, Cebus, Lagothrix, Saguinus,
Saimiri, other Callitrichidae and
Cebidae)
Parasite
P. elegans
Large spirurids
a) Gongylonema sp.
b) Trichospirura sp.
Nematode larvae
a) Strongyloides sp.
b) Filaroides sp./
Angiostrongylus sp.
“Strongylids”
a) Strongyloides sp.
b) Molineus sp.
indirect
direct
indirect
direct
none
polyxenous (Callicebus, Callithrix,
Saguinus, Saimiri)
Results
4.3
63
Variation in parasite species richness (PSR) and prevalence
The results of the ANOVA including all host species revealed a significant effect of
host species on PSR. The main effect of season, home range and the interactive
effects were not significant (Table 4.4). Excluding Callicebus from the analyses the
results confirmed that PSR is significantly influenced by host species (Table 4.5). For
this subset, again PSR was not significantly influenced by season, home range and
any interaction between the independent variables. Variation in PSR and prevalence
related to host-intrinsic and -extrinsic traits and the results of the respective groupwise comparison are described in the following chapters.
Table 4.4 F-, p-values and degrees of freedom (df) for the three host species generated by
ANOVA
Effect
df
F
p
Species
1
9.74
0.006
Season
1
0.98
0.323
Home range
2
1.23
0.312
Species * season
1
0.79
0.374
Species * home range
2
0.44
0.633
Season * home range
2
0.27
0.746
Species * home range * season
2
1.17
0.307
Results
64
Table 4.5 F-, p-values and degrees of freedom (df) for both Saguinus spp. generated by ANOVA
Effect
df
F
p
Species
1
9.99
0.005
Season
1
3.78
0.052
Home range
2
1.24
0.306
Species * season
1
0.85
0.355
Species * home range
2
0.42
0.644
Season * home range
2
0.18
0.815
Species * home range * season
2
1.21
0.297
4.3.1
Host-intrinsic factors
4.3.1.1 Host species
The maximum number of intestinal parasite taxa per individual was six in S. mystax
and seven in S. fuscicollis (Table 4.6). From C. cupreus a maximum of three parasite
taxa was recovered by faecal sampling. All 45 individuals had multiple parasite
infections with at least two (C. cupreus) or three (Saguinus) parasite taxa over the
study period. The frequency distribution of PSR is displayed in Fig. 4.4.
Table 4.6 Total Parasite species richness (PSR) per host species
Host
species
N of host
individuals
Median
IQR
Minimum
Maximum
S. fuscicollis
17
5
2
3
7
S. mystax
21
4
2
3
6
C. cupreus
7
3
1
2
3
Results
65
12
No. of host individuals
10
S. fuscicollis
S. mystax
C. cupreus
8
6
4
2
0
0
1
2
3
4
5
6
7
Total PSR
Fig 4.4 Distribution of PSR frequencies per host species. Bars denote the number of host
individuals with a specific PSR.
Total and seasonal PSR varied significantly over the three host species (PSR total
ANOVA F1,37=11.34, p=0.002; PSR seasonal ANOVA F1,36=9.74, p=0.006, Table
4.4). Both seasonal and total PSR were significantly higher in S. fuscicollis than in
S. mystax and also than in C. cupreus (Fig. 4.5; PSR total: ranked t-test: tSf vs. Sm=3.1,
df=34.6, p=0.004; tCC vs. SF=-8.97, df=22, p<0.001; tCC vs. SM=-5.69, df=25.5, p<0.001;
PSR seasonal: ranked t-test: tSf vs. Sm=3.24, df=66.8, p=0.002; tSf vs. Cc=8.51, df=24.4,
p<0.001; tSm vs. Cc=5.37, df=23.4, p<0.001).
Results
66
9
***
8
*
7
***
Total PSR
6
5
4
3
2
1
S. fuscicollis
S. mystax
Host species
C. cupreus
Fig. 4.5 Total parasite species richness (PSR) per host species. The boxes show the interquartile
ranges, bold horizontal bars show the median. The ends of the whiskers represent the minimum and
maximum values that are not outliers. Asterisks indicate statistical differences between groups: ranked
t-test: *p≤ 0.05; ***p≤ 0.001.
Prevalences of P. elegans, Hymenolepis sp., large spirurids and nematode larvae
were higher in S. fuscicollis than in S. mystax (Fig. 4.6). S. mystax exhibited a higher
prevalence of cestode sp. #2 than S. fuscicollis. Of the shared parasite taxa between
tamarins and Callicebus, Callicebus had the same prevalence in small spirurids and
nematode larvae but a lower prevalence of strongylids than both tamarin species
(Fig. 4.6). Differences of parasite prevalences were significant in the case of
Hymenolepis sp. (Fisher’s Exact test: p<0.001) and “strongylids” (χ²=11.362, df=2,
p=0.003).
Results
67
Prevalences of all host species
***
100
**
Prevalence in %
80
60
S. fuscicollis
S. mystax
C. cupreus
40
20
0
Pro
Hym
Cestode
sm Spir
lg Spir
Nemlarv
Strongy
Parasite taxa
Fig. 4.6 Prevalences of all parasite taxa per host species (Pro=Prosthenorchis elegans,
Hym=Hymenolepis sp., Cestode=cestode sp. #2, smSpir=small spirurid, lgSpir=large spirurid,
Nemlarva=Nematode larvae, Strongy=“strongylids”). S. fuscicollis N=17, S. mystax N=21, C. cupreus
N=7. Bars denote prevalence per parasite species for all host species. Asterisks indicate statistical
differences between groups. Fisher’s Exact test: ***p≤ 0.001, χ² **p≤ 0.01.
4.3.1.2 Host sex
Total PSR did not show significant sex-specific variability in S. fuscicollis and
C. cupreus (Fig. 4.7; MWU: S. fuscicollis U=35.0, Nfemale=7, Nmale=10, p=1.0). In
S. mystax males exhibited a lower PSR than females (MWU: U=12.5, Nfemale=5,
Nmale=16, p=0.015).
Results
68
8
*
7
Host sex
female
male
Total PSR
6
5
4
3
2
1
S. fuscicollis
S. mystax
Host species
C. cupreus
Fig. 4.7 Total parasite species richness (PSR) per sex and host species. The boxes show the
interquartile ranges, bold horizontal bars show the median. The ends of the whiskers represent the
minimum and maximum values that are not outliers. The circles represent outliers. Asterisks indicate
statistical differences between sexes: MWU: *p≤ 0.05.
The prevalences of nematode larvae, large spirurids and P. elegans were higher in
females than in males for both tamarin species (Fig. 4.8). Cestode sp. #2 showed a
higher prevalence in females of S. mystax and in males of S. fuscicollis. The pattern
of Hymenolepis sp. prevalence was inversed (Fig. 4.8). For strongylids and small
spirurids the proportion of infected male tamarins was equal to the proportion of
infected females. Callicebus did not exhibit a sex bias in small spirurids and
nematode larvae prevalence, but a male bias in “strongylid” infection (Fig. 4.8). Sex
differences in parasite prevalence were significant for P. elegans when combining the
data for both tamarin species: five out of 12 females were infected with the
acanthocephalan parasite while only two out of 26 males were infected (Fisher’s
exact p=0.022). The mean parasite prevalence over all seven parasite taxa was
Results
69
female biased in both tamarin species and male biased in C. cupreus (Fig. 4.9;
mean: S. fuscicollis -0.10, S. mystax -0.13; C. cupreus 0.03). The sex bias was not
significantly different from zero (t-test: S. fuscicollis T=-1.08, df=6, p=0.32, S. mystax
T=-1.52, df=6, p=0.18).
“Strongylids“
0
0
0
Nematode larvae
Parasite taxa
Large Spirurids
0
0
0
Small Spirurids
Cestode sp. #2
Hymenolepis sp.
P. elegans
-0.60
-0.40
-0.20
0
Sex bias in parasite prevalences
0.20
0.40
C. cupreus
S. mystax
S. fuscicollis
Fig. 4.8 Sex bias in parasite prevalences over all host species. Negative values represent a female
bias in parasite prevalence (male prevalence minus female prevalence), positive values a male bias.
Results
70
C. cupreus
S. mystax
Host species
S. fuscicollis
95% confidence
interval
mean
-0.40
-0.20
0
0.20
Mean sex bias in parasite prevalences
Fig. 4.9 Mean sex bias in parasite prevalences over all helminth taxa. Negative values represent a
female bias in mean parasite prevalence (male prevalence minus female prevalence), positive values
a male bias.
4.3.1.3 Strata use
In their forest strata use S. mystax and C. cupreus showed a similar distribution
pattern: both frequently used elevated heights in a uniform pattern and spent
approximately one third of their time in heights between 12 and 18 m (37% in
S. mystax, 35% in C. cupreus, Fig. 4.10). In contrast, S. fuscicollis spent almost two
thirds of their time (62%) in strata between 0 and 6 m. S. mystax and C. cupreus
spent little time on the ground (0.5% in S. mystax, 0.2% in C. cupreus), S. fuscicollis
spent 1.6% of the time on the ground.
Results
71
40
S. fuscicollis
S. mystax
C. cupreus
35
Frequency in %
30
25
20
15
10
5
0
ground
> 0-3
> 3-6
> 6-9
> 9-12
> 12-15
> 15-18
> 18
Height in m
Fig 4.10 Strata use for all host species. Bars show the frequency at which individuals were found at
the given height category.
There was a significant positive association between PSR and the time hosts stayed
on the ground (Spearman rank correlation: rs=0.626; N=42, p<0.001, excluding
Callicebus: rs=0.557; N=38, p=0.001). To give a visual picture of the relationship
between the two variables, in Fig. 4.11 median group PSR is plotted against the
proportion of time the hosts stayed on the ground. For parasite prevalence, a positive
and highly significant relationship was found for Hymenolepis sp. (rs=0.509; N=42,
p=0.001), cestode sp. #2 (rs=0.360; N=42, p=0.019), large spirurids (rs=0.572; N=42,
p<0.001). When omitting Callicebus, the correlation of cestode sp. #2 with time spent
on the ground was not significant (p=0.165). Results of all correlations are provided
in Appendix E.
Results
72
6
Median group PSR
5
4
3
Host species
S. fuscicollis
S. mystax
C. cupreus
2
0,0
0,5
1,0
1,5
2,0
2,5
3,0
% time on the ground
Fig. 4.11 Relationship between median group PSR and percent time on the ground. Data is
presented for all groups of the three host species.
4.3.1.4 Diet composition
Callicebus cupreus spent twice as much time (17%) than S. mystax (9%) and
S. fuscicollis (8%) on feeding activities (for complete activity budget see Appendix F).
The main food components of all study host species were fruit and animal prey. Yet,
they diverged in the proportion of the consumed food categories (Fig. 4.12 (A-C)): in
S. fuscicollis fruit formed almost half of the diet (49%), in S. mystax almost two thirds
(64%) and in C. cupreus 74% of the total diet. Across all primate species the second
highest proportion in diet was animal prey: it varied between 12% in C. cupreus, 19%
in S. mystax and 25% in S. fuscicollis. Both Saguinus species consumed a fairly high
amount of exudates or tree gums (S. mystax 13%, S. fuscicollis 23%) which was not
observed in C. cupreus. C. cupreus supplemented its diet with leaves (8%) and
flowers (1%) instead.
Results
73
(A) S. fuscicollis
(B) S. mystax
4%
3%
19%
25%
64%
13%
49%
23%
Diet components
Animal prey
Exudate
Fruit
UFO
(C) C. cupreus
5%
8%
12%
1%
Diet components
Animal prey
Flowers
Fruit
Leaves
UFO
74%
Fig. 4.12 (A-C) Diet composition of all study species. The sectors of the pie chart represent the diet
components fruit, animal prey, flowers, exudates, leaves and unknown feeding objects (UFO).
Results
74
The three primate species did not only diverge in their total proportion of animal prey
but also in the composition of animal matter (Table 4.7). By far the most abundant
component of animal prey in the two tamarin species was formed by orthopteran
insects (S. fuscicollis 59%, S. mystax 49%). In Callicebus animal matter was based
mainly on Hymenoptera and Isoptera, especially ants, represented in 56% of the
animal feeding events. This food category played a subordinate role in the diet of the
tamarins (S. fuscicollis 2% and S. mystax 5%) and included mostly termites. The
second main component of animal diet for Saguinus were other arthropods (including
Phasmatidea, Mantodea and unidentified arthropods): S. fuscicollis ingested 26%
and S. mystax 34% of this category. For Callicebus Orthoptera and other arthropods
represented the second and third most important animal prey items. They consumed
them in almost equal amounts (Orthoptera 13% and other arthropods 10%).
Amphibians were eaten by C. cupreus and S. fuscicollis in equally low proportion
(both 2%). S. mystax consumed a higher amount of amphibians (8%, especially
frogs). S. fuscicollis supplemented their diet with insects of the order Dictyoptera,
(1%, mainly cockroaches), Arachnida (4%) and reptilians (4%, mostly lizards), which
were not consumed by the other primate species. Both tamarin species ingested
Lepidoptera in low amounts (S. fuscicollis 1.6% and S. mystax 2.3%).
Table 4.7 Percentage of animal prey consumed by the three primate species categorized by prey
taxa
Animal prey taxon
S. fuscicollis
S. mystax
C. cupreus
Orthoptera
58.9
48.9
12.8
Hymenoptera, Isoptera
1.6
4.5
56.4
Lepidoptera
1.6
2.3
0
Dictyoptera
0.8
0
0
Arachnida
3.9
0
0
Other arthropods
25.6
34.1
10.3
Reptilia
3.9
0
0
Amphibia
2.3
8.0
2.6
Unidentified animal prey
1.4
2.2
17.9
Results
75
PSR is positively and significantly correlated with proportion of animal prey in the
host’s diet (Spearman rank correlation: rs=0.480; N=42, p=0.001, excluding
Callicebus: rs=0.325; N=38, p=0.047). The scatter plot (Fig. 4.13) displays the
association between group PSR and proportion of animal prey in diet. The
prevalence of cestode sp. #2 and large spirurids was also significantly and directly
related with the prey proportion consumed by the hosts, also after excluding
Callicebus from the analyses (all host species: cestode sp. #2: rs=0.51, N=42,
p=0.01; large spirurid: rs=0.441, N=42, p=0.003, all results see Appendix E). Other
parasite prevalences are not correlated with the proportion of animal prey in the
host’s diet.
6
Median group PSR
5
4
3
Host species
S. fuscicollis
S. mystax
C. cupreus
2
10
15
20
25
30
35
% animal prey in diet
Fig. 4.13 Relationship between median group PSR and proportion of animal prey in the hosts’
diet. Data is presented for all groups of the three host species.
Results
76
4.3.1.5 Home-range size
The home-range size of mixed-species troop West was 29.25 ha, of which 25.46 ha
were occupied by S. mystax and 28.47 ha by S. fuscicollis. Troop North was ranging
in an area of 30.75 ha (S. mystax 30.04; S. fuscicollis 26.29). The largest area was
held by troop East with totally 45.75 ha (S. mystax 39.58; S. fuscicollis 42.05). The
Callicebus group Casa had the smallest home range of 6.46 ha, located within the
home range of troop West (Fig.3.1). PSR was positively correlated with the homerange size of all host groups (Spearman rank correlation: rs=0.37; N=42, p=0.016,
excluding Callicebus: rs=0.176; N=38, p=0.291). Fig. 4.14 depicts the relationship
between group PSR and home-range size. The prevalence of large spirurids and the
cestode sp. showed a positive relation with the home-range size (large spirurids:
rs=0.31; N=42, p=0.046; cestode sp. #2: rs=0.388; N=42, p=0.011). When restricting
the analyses to tamarins, no correlation remained significant (see Appendix G).
6
Median group PSR
5
4
3
Host species
S. fuscicollis
S. mystax
C. cupreus
2
10
20
30
40
Home-range size (ha)
Fig. 4.14 Relationship between median group PSR and home-range size. Data is presented for all
groups of the three host species.
Results
77
4.3.1.6 Group size
In S. mystax mean group size varied between 3.5 individuals in group West, 5.8 in
group North and 6.7 in group East. Group size for S. fuscicollis did not vary that
much (group North 4.9, group East 5.3, group West 5.4 individuals). Group size of
the C. cupreus Casa with 3.8 individuals was comparable with S. mystax West.
PSR was not correlated with the mean host group size (Spearman rank correlation:
rs=0.139; N=42, p=0.38, excluding Callicebus: rs=-0.085; N=38, p=0.612). The scatter
plot shows the relationship between median PSR and mean size of the study host
groups (Fig. 4.15). A positive correlation was found for cestode sp. #2 prevalence
(rs=0.480; N=42, p=0.001), which also remained significant when Callicebus was
excluded (rs=0.381; N=38, p=0.018). When titi monkeys were removed from the
analysis, group size scaled negatively with prevalence of Hymenolepis sp. (rs=-0.378;
N=38, p=0.019). Other correlations were not significant (Appendix G).
6
Median group PSR
5
4
3
Host species
S. fuscicollis
S. mystax
C. cupreus
2
3
4
5
6
7
Mean group size
Fig. 4.15 Relationship between median group PSR and mean group size. Data is presented for all
groups of the three host species.
Results
78
4.3.1.7 Host density
The host density of S. fuscicollis varied between 0.13 (East) and 0.19 individuals per
ha (West, North). S. mystax had a similar density pattern: 0.14 (West), 0.17 (East)
and 0.19 individuals per ha (North). The Callicebus group showed a higher density:
0.59 individuals were present per ha. Host density was not correlated with either PSR
(Spearman rank correlation: rs=-0.167; N=42, p=0.291, excluding Callicebus:
rs=0.073; N=38, p=0.662) or with parasite prevalences (Appendix G). In Fig. 4.16 the
group PSR is plotted against host density in all study groups.
6
Host species
S. fuscicollis
S. mystax
C. cupreus
Median group PSR
5
4
3
2
0,1
0,2
0,3
0,4
0,5
0,6
Host density
Fig. 4.16 Relationship between median group PSR and host density. Data is presented for all
groups of the three host species.
Results
4.3.2
79
Host-extrinsic or habitat factors
4.3.2.1 Home ranges
PSR varied between the host groups across the different home ranges (West, East,
North, Casa, Puerto) but the differences were not significant in the overall model
(ANOVA all host species: F2,36=1.23, p=0.312, Saguinus: F2,32=1.24; p=0.306; Table
4.4 and 4.5). Nonetheless, in home range West both tamarin groups had a lower
median PSR than in the North (Fig. 4.17). The median PSR in home range East for
S. fuscicollis was the highest of all groups, but the median of S. mystax East was in
between home range North and West. For C. cupreus there was also a difference in
PSR over the two home ranges. The individuals from group Casa had a higher PSR
than group Puerto.
8
Host species
S. fuscicollis
S. mystax
C. cupreus
7
Total PSR
6
5
4
3
2
1
West
East
North
Home range
Casa
Puerto
Fig. 4.17 Total parasite species richness (PSR) per home range sorted by host species. The
boxes show the interquartile ranges, bold horizontal bars show the median. The ends of the whiskers
represent the largest and smallest values that are not outliers. The asterisks denote extreme values.
Results
80
The parasite prevalences showed home-range specific patterns. When considering
the prevalences separately per host species, the prevalences of cestode sp. #2 and
large spirurids varied significantly between the tamarin groups of the three home
ranges (Fig. 4.18; extension of Fisher’s Exact test: large spirurids: S. fuscicollis
p<0.048; S. mystax p=0.03; cestode sp. #2: S. fuscicollis p<0.035, S. mystax
p=0.003). C. cupreus showed similar parasite prevalences over both home ranges
(Fig.4.18). Combining the data of individuals of the mixed-species troops within the
three home ranges West, East and North significant differences were detected for
P. elegans, cestode sp. #2 and large spirurids (Fig. 4.19). In the mixed-species troop
North P. elegans was not prevalent, whereas all other troops were infected with this
parasite (Extension of Fisher’s Exact test: p=0.048). Cestode sp. #2 prevalence was
lower in troop West than in the other troops (Extension of Fisher’s Exact test:
p<0.001): in troop West two individuals out of a total of 12 individuals were infected,
whereas in troop East 11 out of 15 individuals and North all 11 individuals were
infected. Furthermore, differences in prevalence of large spirurids were significant
(Extension of Fisher’s Exact test: p=0.027). In troop West none of the individuals
harboured large spirurids, in troop East four out of 15 and in North 5 out of 11 hosts.
(A) Saguinus fuscicollis
100
*
SF West
*
SF East
Prevalence in %
80
SF North
60
40
20
0
Pro
Hym
Cestode
sm Spir
Parasite taxa
lg Spir
Nemlarv
Strongy
Results
81
(B) Saguinus mystax
100
**
SM West
*
SM East
Prevlence in %
80
SM North
60
40
20
0
Pro
Hym
Cestode
sm Spir
lg Spir
Nemlarv
Strongy
Parasite taxa
(C) Callicebus cupreus
100
CC Casa
CC West
Prevalence in %
80
60
40
20
0
Pro
Hym
Cestode
sm Spir
lg Spir
Nemlarv
Strongy
Parasite taxa
Fig. 4.18 (A-C) Group prevalences for all parasite taxa per host species (Pro=Prosthenorchis
elegans, Hym=Hymenolepis sp., Cestode=cestode sp. #2, smSpir=small spirurid, lgSpir=large
spirurid, Nemlarva=Nematode larvae, Strongy=“strongylids”). Bars denote prevalence per parasite
species for all groups per host species. Asterisks indicate statistical differences between groups.
Extension of Fisher’s Exact test: *p≤ 0.05; **p≤ 0.01.
Results
82
Parasite prevalences for Saguinus mixed-species troops
100
*
**
**
Prevalence in %
80
60
40
20
West
East
North
0
Pro
Hym
Cestode
sm Spir
lg Spir
Nemlarv
Strongy
Parasite taxa
Fig. 4.19 Parasite prevalences for Saguinus mixed species troops (Pro=Prosthenorchis elegans,
Hym=Hymenolepis sp., Cestode=cestode sp. #2, smSpir=small spirurid, lgSpir=large spirurid,
Nemlarva=Nematode larvae, Strongy=“strongylids”). Bars denote prevalence per parasite species for
individuals of mixed-species troops West, East and North. Asterisks indicate statistical differences
between home ranges: Extension of Fisher’s Exact test: *p≤ 0.05; **p≤ 0.01, ***p≤ 0.001.
4.3.2.2 Habitat use
The host’s use of the specific habitat characteristics is based on the habitat
descriptions that were gathered at 426 sampling points equally distributed over all
home ranges (West, East, North and Casa; for an overview see Appendix H). Data
on habitat use of all primate groups considering the specific habitat characteristics
are depicted in Fig 4.20 (A-G). Results of the correlations between PSR, prevalences
and the specific habitat use are given in each section separately; statistical
parameters are summarized in Table 4.8 and 4.9 at the end of this chapter. All
analyses were repeated after excluding Callicebus in order to minimize the risk that
the general pattern can be obscured by a non-representative data set of one host
species. Small spirurids and “strongylids” did not show any variability and thus were
excluded from these analyses.
Results
83
4.3.2.2.1 Drainage
All groups ranged the vast majority of their time in areas with good drainage (Fig.
4.20 (A)). Areas characterized by poor drainage were used in around 20% of the time
in case of groups West (S. mystax 24%, S. fuscicollis 21%) and Casa (19%);
whereas groups East and North were found only in less than 8% of the cases in
zones with poor drainage (East: S. mystax 6%, S. fuscicollis 5%; North: S. mystax
8%, S. fuscicollis 7%). There was no relationship between PSR and the use of poorly
drained areas. The more time hosts spent in areas of poor drainage the less
prevalent was the infection with cestode sp. #2 and large spirurids (Table 4.8). These
relationships remained significant when removing Callicebus from the analyses
(Table 4.9).
(A) Drainage
100
poor
intermediate
good
90
80
% of time
70
60
50
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20A Habitat use: drainage. Bars show percentage of time hosts spent in areas of specific
drainage.
Results
84
4.3.2.2.2 Soil type
Groups West and Casa ranged on clay soil in the majority of their time (Casa 66%,
groups West around 52%); while groups North and East used sandy soil areas more
often: groups East in more than 75%, and groups North in more than 68% of the
cases (Fig. 4.20 (B)). PSR and cestode sp. #2 and large spirurids prevalence scaled
negatively with the time hosts spent on clay soil (Table 4.8). When Callicebus was
excluded the correlation with PSR was not significant, the other correlations
remained significant (Table 4.9).
(B) Soil type
90
clay
mixed
sand
swampy
80
70
% of time
60
50
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20B Habitat use: soil type. Bars show percentage of time hosts spent in areas of specific soil
type.
Results
85
4.3.2.2.3 Ground inclination
More than two thirds of their time all groups were found in areas that exhibited a flat
ground profile (0-5%). Steep terrain of a slope of over 20% was used in less than 9%
of their time (Fig. 4.20 (C)). PSR and the prevalences of cestode sp. #2 and large
spirurids were positively associated with the use of flat terrain (Table 4.8). For
P. elegans the trend was reversed when considering the tamarins only (Table 4.9).
(C) Ground inclination
100
flat
intermediate
steep
90
80
% of time
70
60
50
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20C Habitat use: ground inclination. Bars show percentage of time hosts spent in areas of
specific ground inclination.
Results
86
4.3.2.2.4 Leaf litter height
Groups West and Casa ranged around half of their time in areas dominated by
scarce leaf litter (layer <5 cm): group Casa spent 56%, groups West around 47% of
their time in such areas (Fig. 4.20 (D)). Groups East and North, in contrast, used
mainly areas of high leaf litter (>10 cm): groups East in 53%, North S. mystax in 58%,
S. fuscicollis in 61% of their time. PSR and prevalence of cestode sp. #2 and large
spirurids showed a positive relationship with the time hosts stayed in areas with very
abundant leaf litter (>10 cm). There was a negative correlation with P. elegans when
Callicebus was removed from the analyses (see Table 4.8 and 4.9).
(D) Leaf litter height
60
0-5 cm
5-10 cm
10-15 cm
>15 cm
50
% of time
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20D Habitat use: leaf litter height. Bars show percentage of time hosts spent in areas of
specific leaf litter height.
Results
87
4.3.2.2.5 Deadwood abundance
All groups ranged primarily in areas that were characterized by low abundance of
deadwood (Fig. 4.20 (E)). Areas with higher deadwood abundance (≥1 deadwood
unit) were visited in around 5% (groups East), 9% (groups North), 16% (groups East)
and 34% (Casa) of the cases. PSR and the use of these areas were not correlated,
but the prevalence of cestode sp. #2 scaled negatively with high deadwood
abundance (Table 4.8). P. elegans manifested a trend for a positive correlation with
the time the hosts spent in areas with high deadwood abundance when the analyses
were restricted to tamarins (Table 4.9).
(E) Deadwood abundance
80
0 tree units
1 tree unit
>1 tree unit
70
60
% of time
50
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20E Habitat use: deadwood abundance. Bars show percentage of time hosts spent in areas
of specific deadwood abundance.
Results
88
4.3.2.2.6 Vegetation density
The major part of the time was spent in areas with intermediate vegetation density
characterized by an average of 400 to 800 trees (>10 cm DBH) per ha (Fig. 4.20 (F)).
In all groups the least amount of time was spent in areas with tree density over 2000
trees/ha (1% in groups East, around 3% in group Casa, groups East, S. mystax
North, and 8% in S. fuscicollis North). The time animals stayed in areas with dense
vegetation (>1200 trees/ha) scaled significantly positively with PSR and prevalence
of cestode sp. #2 and large spirurids (Table 4.8 and 4.9). The correlation with PSR
was not significant anymore when excluding Callicebus. There was a trend for a
weak negative correlation with prevalence of P. elegans.
(F) Vegetation density
60
0-400 trees/ha
400-800
800-1200
1200-2000
>2000
50
% of time
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20F Habitat use: vegetation density. Bars show percentage of time hosts spent in areas of
specific vegetation density.
Results
89
4.3.2.2.7 Understorey density
The proportion of time spent in areas with high understorey density varied between
17% (S. mystax West) and 28% (S. fuscicollis North) as depicted in Fig. 4.20 (G).
Tamarin groups West and the Callicebus group spent more time in areas with lower
understorey density (S. mystax 41%, S. fuscicollis 35%, C. cupreus 43%) compared
to groups North and East (groups North 6%, East 16%). The use of areas with high
understorey density did neither correlate with PSR nor with any parasite prevalence
(Table 4.8). When Callicebus was excluded PSR and cestode sp. #2 prevalence had
a trend for a weak positive correlation with time ranging in dense understorey (Table
4.9).
(G) Understorey density
70
low
intermediate
high
60
% of time
50
40
30
20
10
0
Cc Casa
Sm West
Sf West
Sm East
Sf East
Sm North
Sf North
Fig. 4.20G Habitat use: understorey density. Bars show percentage of time hosts spent in areas of
specific understorey density.
90
Results
In summary, a positive correlation existed between prevalences of cestode sp. #2
and large spirurids and the host’s time spent on flat terrain, in areas of high
vegetation density and high leaf litter abundance (Table 4.9). The relationship
between cestode sp. #2 and large spirurids prevalence and time ranged on clay soil
and in areas of poor drainage was negative (Table 4.9). The prevalence of
P. elegans showed an opposite pattern: prevalence was higher when the hosts spent
less time on flat terrain, in areas of high abundance of leaf litter and high vegetation
density, while prevalence was higher when spending more time in areas of high
deadwood abundance and clay soil. Prevalence of Hymenolepis sp. and nematode
larvae did not correlate with any of the measured habitat parameters. Following the
pattern of cestodes and large spirurids, the correlation between PSR and host’s time
spent on plain terrain and in areas of a high leaf litter layer was positive.
Table 4.8 Spearman's Rank Correlation Coefficient (rs) for total PSR and prevalence for five parasite species and proportion of time that
hosts spent in areas of specific habitat morphology; (*) p≤0.1, *p≤0.05; **p≤0.01, ***p≤0.001
All host species (N=42)
Time spent in specific
habitat morphology/
Parasite infection
poor
drainage
clay soil
flat terrain
leaf litter
height ≥10
cm
≥1 tree
units
deadwood
high
dense
vegetation underdensity
storey
PSR
-0.331
-0.420**
0.519***
0.519***
-0.257
0.379*
0.237
P. elegans
0.232
0.189
-0.275(*)
-0.275(*)
0.195
-0.157
-0.072
Hymenolepis sp.
-0.138
-0.114
0.170
0.170
0.070
0.178
0.134
Cestode sp. #2
-0.456**
-0.512***
0.665***
0.665***
-0.544***
0.488**
0.231
Large spirurid
-0.354*
-0.499***
0.504***
0.504***
-0.213
0.354*
0.048
Nematode larvae
-0.070
-0.033
0.079
0.079
0.061
-0.023
0.210
Table 4.9 Spearman's Rank Correlation Coefficient (rs) for total PSR and prevalence for five parasite species and proportion of time that
hosts spent in areas of specific habitat morphology; (*) p≤0.1, *p≤0.05; **p≤0.01, ***p≤0.001
Saguinus spp. (N=38)
Time spent in specific
habitat morphology/
Parasite infection
poor
drainage
flat terrain
leaf litter
height ≥10
cm
≥1 tree
units
deadwood
high
dense
vegetation underdensity
storey
clay soil
PSR
-0.266
-0.241
0.371*
0.371*
-0.035
0.191
0.284(*)
P. elegans
0.236
0.311(*)
-0.412*
-0.412*
0.318(*)
-0.274(*)
-0.072
Hymenolepis sp.
-0.119
0.046
0.022
0.022
0.271
0.032
0.154
Cestode sp. #2
-0.371*
-0.402*
0.594***
0.594***
-0.442**
0.371*
0.291(*)
Large spirurid
-0.315(*)
-0.487**
0.493**
0.493**
-0.149
0.315(*)
0.046
Nematode larvae
-0.082
-0.082
0.136
0.136
0.027
0.016
0.202
Results
4.3.3
93
Seasonality
4.3.3.1 PSR and prevalences
PSR did not differ significantly in dry and rainy season over all host species (Table
4.4 and 4.5). PSR did not follow a general pattern (Fig. 4.21): in S. fuscicollis PSR
stayed the same over the seasons; in S. mystax it was higher, whereas in C. cupreus
PSR was lower in the wet season. Prevalences of the seven parasite taxa showed no
seasonal differences (McNemar: N=35 for all parasites; P. elegans: p=1.0,
Hymenolepis sp. p=0.18, cestode sp. #2: p=1.0, small spirurids: p=1.0, large
spirurids: p=0.219, nematode larvae: p=0.687, “Strongylids”: p=0.625).
7
6
5
PSR
4
3
2
1
0
species
S. fuscicollis
S. mystax
C. cupreus
dry
wet
Season
Fig. 4.21 Parasite species richness (PSR) per season. The boxes show the interquartile ranges,
bold horizontal bars show the median. The ends of the whiskers represent the largest and smallest
values that are not outliers.
Results
94
4.3.3.2 Climate
During the study period mean rainfall ranged from 118 to 495 mm per month with
peaks in precipitation in November 2002 and Mai 2003 (Fig. 4.22). The total annual
precipitation was around 3460 mm (July 2002 to June 2003). The period between
July and October 2002 (mean monthly rain fall 198 mm) and between July and
September 2003 (mean 196 mm) was considered as core dry season. The core rainy
season lasted from March to June 2003 (mean 376 mm). Mean minimum monthly
temperature varied between 22.0 and 23.6°C and mean maximum temperature
between 25.4 and 28.3°C (Fig. 4.22).
Tmin
Tmax
600
28
500
26
400
24
300
22
200
20
100
18
Monthly Rainfall in mm
Temperature in °C
rainfall
30
0
Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr Mai Jun Jul Aug Sep
02 02 02 02 02 02 02 03 03 03 03 03 03 03 03 03
Months
Fig. 4.22 Climate profile. Lines indicate mean minimal and maximal temperature per month (Tmin,
Tmax), bars show mean monthly rainfall.
4.3.3.3 Phenology
The abundance of ripe fruit and young leaves peaked at the end of the dry season
and beginning of the rainy season (Fig. 4.23): 38% of the trees bore ripe fruits and
32% had formed new leaves at the study site. Until the end of rainy season fruit and
leaf abundance dropped and reached the minimum level in the middle of the dry
season (2% of trees with young leaves and 8% with ripe fruits). The variability in the
abundance of flowers was not as high as in leaves and fruits. The abundance pattern
Results
95
of flowers showed an opposite pattern: it had its trough at the beginning of the rainy
season (2%) and its maximum at the beginning of the dry season (15%). Food
abundance of ripe fruits was higher in the rainy season than in the dry season (Fig.
4.24; t-test for dependent samples: t=7.19, df=3, p= 0.019).
rainfall
young leaves
flowers
0,30
ripe fruits
700
600
200
0,05
100
0,00
0
Se
p
Au
g
Ju
ly
M
Fe
b
Ja
n
02
ec
D
ov
N
03
0,10
03
300
03
0,15
Ap
r0
3
M
ay
03
Ju
n
03
400
ar
03
0,20
03
500
03
0,25
02
Food Abundance Index
0,35
800
Rainfall in mm
0,40
Fig. 4.23 Phenology profile: food abundance index and rainfall. Lines indicate variation in food
abundance for young leaves, flowers and ripe fruits; bars show mean monthly rainfall.
Results
96
Relative abundance of ripe fruit
0,5
*
0,4
0,3
0,2
0,1
0,0
rainy season
dry season
Fig. 4.24 Comparison of relative abundance of ripe fruit in rainy and dry season. The boxes give
interquartile ranges, bold horizontal bars give median. The ends of the whiskers represent the largest
and smallest values that are not outliers. Asterisks indicate statistical differences between the
seasons. T-test for dependent samples: *p≤ 0.05
4.3.3.4 Diet
The proportion of animal prey in the host’s diet was slightly higher in the rainy than in
the dry season in all groups except group West. Yet, differences were not significant
(Wilcoxon’s test for matched pairs: Z=-1.521, N=7, p=0.128). The proportion of fruit
was generally higher in wet than in dry season, except for the mixed-species troop in
home range East. The results were not significant (Wilcoxon’s test for matched pairs:
Z=-1.352, N=7, p=0.176).
4.4
Variation in egg and larvae output
In general, the number of parasite stages emitted in faeces was low regarding all
host individuals over all seasons (Table 4.10). The highest parasite output was
measured for small spirurids (mean egg output was 47.8 eggs per 100 µl), but for the
other parasite taxa mean output was between 1.9 and 9.1 propagules per 100 µl.
Results
97
Table 4.10 Faecal egg and larvae output (refers to number of parasite stages per 100 µl faecal
sediment). N gives the number of faecal samples that were positive for a specific parasite, SD the
standard deviation, mean and maximum number of parasite stages per sample.
Parasite taxa
Mean
SD
Maximum
N
P. elegans
5.0
5.2
25
22
Hymenolepis sp.
9.1
14.1
59
49
Cestode sp. #2
4.6
6.7
28
41
Small spirurid
47.8
184.7
1860
215
Large spirurid
1.9
1.9
8
14
Nematode larvae
6.1
9.5
77
155
“Strongylids”
7.3
7.9
46
212
The results of the General Linear Mixed Model (GLMM) revealed that the effect of
species and season and of the interaction between these two variables varied
between the different parasite taxa (Table 4.11). For large spirurids, season had a
significant effect on egg output. In the case of nematode larvae and “strongylid” egg
output, the effect of the host species which shed the propagules was highly
significant while season had no effect. For P. elegans and small spirurids, the
interaction of species and season had a significant effect. For every parasite taxon
the seasonal pattern in egg or larvae output is shown in Fig 4.25 (A-G). The results of
the GLMM are displayed in Appendix I.
Results
98
Table 4.11 F values for main effects and interactions generated by GLMM for mean egg/larvae
output; *p≤ 0.05; **p≤ 0.01, ***p≤0.001
Parasite taxa
Host species
Season
Host species
* season
P. elegans
0.08
0.53
34.48**
Hymenolepis sp.
0.04
2.11
1.05
Cestode sp. #2
0.90
1.45
1.67
Small spirurid
1.59
1.81
4.95 **
Large spirurid
0.42
5.10 *
1.46
Nematode larvae
10.07 ***
2.63
0.55
“Strongylids”
12.78 ***
2.35
0.27
S. fuscicollis excreted more P. elegans eggs in the rainy season than in the dry
seasons (Fig. 4.25 (A)). For S. mystax the pattern was opposite. For S. fuscicollis
only the difference from the first dry season to the rainy season was significant (t-test
for dependent samples: tdry1
vs. rainy=-5.977,
df=2, p=0.027, trainy
vs. dry 2=9.639,
df=1,
p=0.066). For small spirurids the sample size for C. cupreus was very limited (N=1 for
dry and rainy season, N=4 for rainy season), thus for further tests this host species
was excluded. For Saguinus spp. no significant effect of host species and season
was detected (Fig. 4.22 (B); species: F1,30.8=0.125, p=0.726; season: F2,52=2.029,
p=0.142; season*species: F2,52=0.075, p=0.928). The egg output of large spirurids
showed a peak in the rainy season (Fig. 4.25 (C)). But after removing S. mystax from
the analyses (S. mystax had only two individuals that were present for dry and rainy
season) the results for S. fuscicollis failed to be significant (t-test for dependent
samples: tdry1
vs. rainy=-1.674,
df=3, p=0.193, trainy
vs. dry2=0.968,
df=4, p=0.388). The
nematode larvae output followed a host-specific pattern (Fig. 4.25 (D)): larvae output
was significantly higher in S. fuscicollis than in S. mystax (t-test for independent
samples: tSF
vs SM=4.037,
df=65, p≤0.001) and than in C. cupreus (tSF
vs CC=4.008,
df=38, p≤0.001). S. mystax excreted also more larvae than C. cupreus over all
seasons but the results failed to be significant (tCC vs SM=1.832, df=35, p=0.075). The
Results
99
same pattern was found for the “strongylid” egg output: S. fuscicollis shed more eggs
than S. mystax and C. cupreus, and C. cupreus had the lowest egg output of all host
species over all seasons (Fig. 4.25 (E); t-test for independent samples: tSF
SM=3.297,
df=67, p=0.002, tSF
vs CC=3.369,
df=37, p=0.002, tCC
vs SM=1.553,
vs
df=36,
p=0.129). For both cestode species the results from the GLMM showed no evidence
for seasonal or host-specific effects on egg output (Table 4.11, Fig. 4.25 (F, G)).
(A) P. elegans
1,50
Host species
S. fuscicollis
S. mystax
log egg output P. elegans
1,25
1,00
0,75
0,50
0,25
0,00
dry season 1
rainy season
dry season 2
Results
100
(B) Small spirurids
Host species
S. fuscicollis
S. mystax
C. cupreus
log egg output small spirurids
3
2
1
0
dry season 1
rainy season
dry season 2
(C) Large spirurids
1,00
Host species
S. fuscicollis
S. mystax
log egg output large spirurids
0,80
0,60
0,40
0,20
0,00
dry season 1
rainy season
dry season 2
Results
101
(D) Nematode larvae
Host species
S. fuscicollis
S. mystax
C. cupreus
log output nematode larvae
1,5
1,0
0,5
0,0
dry season 1
rainy season
dry season 2
(E) “Strongylids”
Host species
S. fuscicollis
S. mystax
C. cupreus
log egg output "strongylids"
1,5
1,0
0,5
0,0
dry season 1
rainy season
dry season 2
Results
102
(F) Hymenolepis sp.
2,5
Host species
S. fuscicollis
S. mystax
log egg output Hymenolepis sp.
2,0
1,5
1,0
0,5
0,0
dry season 1
rainy season
dry season 2
(G) Cestode sp. #2
1,50
Host species
S. fuscicollis
S. mystax
log egg output cestode sp. #2
1,25
1,00
0,75
0,50
0,25
0,00
dry season 1
rainy season
dry season 2
Fig. 4.25 (A-G) Mean egg/larvae output per season and host species. The boxes show
interquartile ranges, the bold horizontal bars give the median. The end of the ‘whiskers’ represent the
largest and smallest values that are not outliers or extreme values. The circles represent outliers.
Results
4.5
103
Post-mortem analyses
An adult female titi monkey of group Puerto was found in agony below the sleeping
tree of its group. The day before, the individual showed an apathetic behaviour, an
increased food uptake and a mild lameness. The female stayed distant to the other
group members. In general it was less shy than on the other days of observation.
The individual displayed convulsions and opisthotonus (i.e. spasm in which the back
arches and the head bends back) shortly before the female died. Death occurred
approximately two hours after retrieval. It weighed 720 g. Body condition of the
animal was poor: it was skinny, dehydrated and its pelage was dirty. The animal was
dissected immediately after death. Gross necropsy findings included severe
multifocal subacute to chronic ulcerative enteritis and severe chronic granulomatous
hepatitis. In detail the following observations were made.
4.5.1
Small and large intestine
Two parasites with a length of 17 and 30 mm were firmly attached to the intestinal
wall of the ileum by embedding their hooked proboscis into the mucosa and
submucosa (Fig. 4.26). The parasites’ bodies were protruding into the intestinal
lumen. The adult parasites were not pseudo-segmented and possessed a spheroid,
spinous proboscis (Fig. 4.3). The anterior end had a collar of festoons. The proboscis
was armed with six spiral rows each consisting of five to seven hooks. These
morphological characteristics determined the species as P. elegans. At the site of
attachment of the parasites a sharply delineated mucosal ulcer was present. The
ulcers extended into the lamina submucosa and tunica serosa and were surrounded
by connective tissue. Microscopically, the infection with P. elegans was associated
with diffuse chronic enteritis. The ulcers were surrounded by necrotic debris,
fibroblastic tissue and mixed inflammatory cell infiltration composed by neutrophils,
eosinophils, lymphocytes and macrophages (Fig. 4.26). In rare sites scar tissue
formation was represented by dense connective tissue extended to the serosal
surface. Macroscopically, in the large intestine, several ulcers were visible, ranging
from 1 to 4 mm in diameter. No parasites were found attached to those lesions.
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104
Histologically, severe multifocal chronic-active enteritis was evident; several
subacute ulcers were demonstrable.
Fig. 4.26 Light microscope picture of an adult P. elegans in the small intestine of a female titi
monkey. Cross section of the anterior end and proboscis of P. elegans which intrudes deeply into the
intestinal wall provoking mixed inflammatory cell infiltration. H.&E. stain; scale bar = 1000 µm
4.5.2
Liver
Macroscopically, disseminated red pintip-sized lesions were present on the
diaphragmatic and visceral surface of the liver. Histology of the liver specimens
revealed a severe chronic-active multifocal granulomatous hepatitis, characterized by
multiple microgranulomas consisting of necrotic hepatocytes and inflammatory cells,
especially lymphocytes, neutrophils and activated Kupffer cells. Multifocal fibrosis
with focal calcification was evident in the centrolobular area. Further findings included
focal gallstone formation and a mild chronic fibroblastic pericholangitis.
Results
4.5.3
105
Abdominal cavity
A cyst of approximately 5 mm in diameter with a white, slender parasite was found
retroperitoneally in the paramedian area of the abdominal cavity. Based on
morphological features like ventral mouth with four hooks, striated muscles, and the
structure of the body (Fig. 4.27) the parasite was identified as an arthropod or
pentastomid nymph (phylum Pentastomida, order Porocephalida). Sections of
arthropods usually show some chitin structures that could not be detected here.
Likewise pentastomid nymphs of the family Linguatulidae possess cuticular spines
which were not demonstrable. Since the cyst was located at the inner side of the
abdominal wall and spiny cuticles on the parasite’s body were missing, the diagnosis
of arthropods and Linguatulidae seemed less likely. Combining the morphological
features with findings in the literature, the parasite belongs probably to the
pentastomid family Porocephalidae.
Fig. 4.27 Light microscope picture of an abdominal cyst of a female titi monkey. Cross section of
a pentastomid nymph located in the centre of the abdominal cyst. Masson’s Trichrome stain;
scale bar = 500 µm
Results
106
4.5.4
Further pathological findings
There was moderate lymphoid depletion of the spleen with absence of follicular
structures. The lung showed mild peripheral alveolar emphysema and mild alveolar
histiocytosis. Mild focal lymphocytic infiltration was observed within the adrenal
medulla. The sections of intestine, liver and spleen for bacteria and fungi gave
negative results.
Discussion
107
5 DISCUSSION
Numerous parasitological studies have been carried out on intestinal parasites of wild
primate species, especially on Old World primates (e.g. MCGREW et al. 1989a;
APPLETON and BRAIN 1995; LANDSOUD-SOUKATE et al. 1995; MÜLLER-GRAF
et al. 1996; HUFFMAN et al. 1997; MUNENE et al. 1998; KARERE and MUNENE
2002; CHAPMAN et al. 2005; GILLESPIE et al. 2005; MUEHLENBEIN 2005;
PETRZELKOVA et al. 2006) but few studies have focused on wild New World
monkeys (e.g. APPLETON and BOINSKI 1991; GILBERT 1994; STONER 1996;
STUART et al. 1998; PACHECO et al. 2003; PHILLIPS et al. 2004).
To our knowledge, this is the first study on wild populations of sympatric primate
species to shed light on a diverse array of ecological determinants of parasite
species richness and prevalence. This study gathered baseline data on the intestinal
helminth spectrum of Saguinus fuscicollis, Saguinus mystax and Callicebus cupreus,
and examined various proposed host traits and environmental factors that can affect
parasite diversity. In addition, the results are based on a consistent, year-round
sampling regime and on standardized parasitological methods aimed at minimizing
bias.
5.1
Methodological considerations
Parasitological studies based on non-invasive methods have some limitations but
they are often the only feasible and responsible method for endangered or other wild
host species (STUART and STRIER 1995). In the following, the emerging
methodological problems of non-invasive faecal sampling in terms of the fixation
employed, concentration technique and parasite identification will be discussed.
There is also an evaluation of the reliability of the used disease metrics and the
emerging bias.
5.1.1 Faecal sampling, fixation and concentration technique
The faecal sampling regime is of great importance for measuring parasite species
richness and prevalence (HUFFMAN et al. 1997; HUDSON et al. 2002). A systematic
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Discussion
regime for the faecal sample collection was employed. This regime was based on
three important aspects: firstly, all group members were sampled equally. Secondly,
each host was sampled individually. Thirdly, samples of all hosts were collected on
non-consecutive days for three times in each season. This multiple sampling method
was validated by a study by MUEHLENBEIN (2005) and seems to reflect reliably the
PSR and prevalences (see also 5.1.4.1.).
Both fixation (preservation agent and period) and concentration techniques have a
major impact on recovery and identification of parasite stages in faeces (FOREYT
1986; ASH and ORIHEL 1987; DUSZYNSKI et al. 1999; MES 2003). In many field
studies, including the present one, fixation of the faecal material prior to examination
is inevitable. 10% neutral buffered formalin fixative was chosen because it provides
several advantages over other fixatives:
(a) it adequately preserves helminth eggs/larvae and protozoan (oo-)cysts (ASH and
ORIHEL 1987);
(b) it is a good long-term fixative even over a few years (ASH and ORIHEL 1987);
(c) for the performed formalin-ethyl acetate-sedimentation method, formalin fixation
results in higher recovery rates than fixation with polyvinyl alcohol, for example
(CARROLL et al. 1983).
(d) Less distortion of the stages is reported which accounts for a higher diagnostic
efficiency (CARROLL et al. 1983).
Despite the reported general advantages of formalin fixation, there are more suitable
fixatives for the conservation of specific parasites that can result in higher recovery
rates or better parasite identification (e.g. 2-2.5% potassium dichromate solution for
coccidian oocysts (DUSZYNSKI et al. 1999)).
Although formalin is suitable for long-term fixation, the parasite recovery rates
decrease as a function of the preservation period: for nematode eggs the evaluated
recovery rate dropped from 100 to 50% after 200 days of formalin fixation compared
to fresh samples (FOREYT 1986). The long storage time of the faecal samples in this
study (in some cases more than 24 months) could have caused a declining recovery
Discussion
109
of parasite stages. This in turn could have affected the sensitivity of the following
concentration method (KRAEMER 2005). The long preservation period and the
unspecific fixative might account for the failure to detect protozoa in the faecal
samples of the studied hosts. However, many studies revealed a good recovery rate
for protozoa for the same fixative and concentration method used in this study
(YOUNG et al. 1979; GARCIA and SHIMIZU 1981; PRICE 1981; TRUANT et al.
1981) including New World primate hosts (HENDRICKS 1974; STUART et al. 1990;
APPLETON et al. 1991). Yet, most studies did not report fixation periods prior to
examination. Information on the length of preservation time would be desirable to
improve comparisons between studies (especially on egg output) and to determine
the influence of fixation period.
In order to detect even small numbers of parasitic stages in the faecal samples, it is
indispensable to use a concentration procedure (ASH and ORIHEL 1987). The
performed formalin-ethyl acetate-sedimentation technique in combination with
formalin-fixed faecal samples is quoted as an excellent method for recovering
protozoa and helminths (ASH and ORIHEL 1987). Ethyl acetate seems to facilitate
the detection of some eggs (Hymenolepis and Taenia species), cysts (Giardia sp.,
Entamoeba sp.) and larvae (Strongyloides sp.), because they do not get trapped in
the debris as much as if centrifuged with ether (YOUNG et al. 1979; ASH and
ORIHEL 1987). The procedure of the formalin-ethyl acetate-sedimentation technique
was followed consistently for all faecal samples. Diverging from the original method
(ASH and ORIHEL 1987; ASH et al. 1994) two minor modifications were made to
achieve a greater sensitivity and accuracy: firstly, in order to reduce the variance
introduced by plant fibres or seeds in the faeces remnants, a polyamide sieve with
standardized mesh size was used instead of two layers of wet gauze (see also
chapter 5.3.3). The aim was also to raise the number of recovered parasites after the
straining procedure thanks to the non-adhesive property of polyamide. Secondly, the
centrifugation time was increased to 10 min because 5 min did not yield a sufficient
concentration of the parasite stages in the sediment of the C. cupreus faeces.
It was not possible to determine the efficiency of the preservation method and
concentration technique within the study because the faecal samples were too small
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Discussion
to be split up into various sub-samples to compare the results of alternative methods.
The precision of the microscopic examination was determined by an intra-observer
reliability test (see chapter 3.4.4). The results concord very largely in the different
examination processes of the parasitic stages. Evaluating the consistency of several
observations of subsets of the same sample also validated the method: the
concordance in the number of parasite stages counted over the different subsets
showed that the amount of sediment examined and the homogenization of the
samples was sufficient.
Evaluating the precision of this study compared to other studies presents several
problems even when they are carried out on the same host-parasite system. In this
case, data on prevalences or egg/larvae output on S. fuscicollis, S. mystax and
C. cupreus based on faecal samples is very limited, the number of examined hosts is
often small, the parasitological methods used diverge (fixation and concentration
techniques, necropsy) and often rely on single sampling. Additionally, the data often
combines results from animals of different groups or locations. Concerning the three
host species studied, there is only one record of S. fuscicollis based on faecal
sampling of four wild individuals in Peru (PHILLIPS et al. 2004). Two of them
harboured strongylids, Trichuris sp. and one of them was infected with two protozoan
taxa (Iodamoeba and Entamoeba). In the present study Trichuris and protozoan
species were not detected, but strongylids had a higher prevalence (100%, all 17
individuals were infected). Other reports were based on necropsies of newly imported
animals (DUNN 1963; COSGROVE et al. 1968; PORTER 1972; MICHAUD et al.
2003) which should render more exact results given the noticeable size of the adult
parasites. The recovery rate of strongylid eggs in this study was consistently higher
compared to other studies, even those that were based on large sample sizes and on
necropsies: 9-78% in 455 S. fuscicollis (COSGROVE et al. 1968), 12-17% in 78
S. fuscicollis and 0% in 19 S. mystax (PORTER 1972), whereas this study found
100% strongylid prevalence for S. fuscicollis and S. mystax. The detection of these
parasite eggs was very efficient although the size and the number of the excreted
eggs were relatively small (median size 51-54 µm, mean number of six eggs per
100 µl sediment; see chapter 4.1.1, Table 4.2 and 4.10). Even very small eggs from
Discussion
111
small spirurids (median size 25-27 µm, see chapter 4.1.1, Table 4.2 and 4.10), which
are probably one of the smallest intestinal helminth stages of New World primates,
were recovered from 100% of the individuals of all host species. Thus, the methods
employed in this study seem to yield very good results concerning the recovery rate
particularly in comparison with other studies based on faecal sampling or necropsies.
In conclusion, in terms of faecal sampling, parasite fixation and concentration method
the parasitological methods used yielded highly satisfying results for the helminths,
including compared to other parasitological studies. It can be pointed out that the
absence of intestinal protozoa is unlikely to be a consequence of methodological
deficiencies. Only if the number of protozoan stages in the faeces at the time of
defecation had been extremely low (and lower than in other studies) could the long
storage time have lead to an undetectably low number of protozoan stages at the
time of microscopic examination.
5.1.2 Helminth identification
Exact helminth identification that is exclusively based on coprological examinations
and the determination to the species level is limited without adult worms (STUART et
al. 1998; GILLESPIE et al. 2004; 2005) or coproculture for nematode larvae (ASH
and ORIHEL 1987; ASHFORD et al. 2000). Especially “strongylid” species represent
a large group of parasites that generally cannot be differentiated by faecal
examination (WARNICK 1992). The stage of development of parasite eggs or larvae
at the time of conservation can vary with temperature and intestinal passage time
which can further complicate parasite identification (ASH and ORIHEL 1987).
Although belonging to the same parasite species, both the excreted eggs in the
faeces and the adult worms may vary in size depending on the host species (FAUST
1967). An additional source of identification problems is the unanimity of parasite and
host taxonomy. Typographical errors, ambiguous names and synonymy for parasite
and host species, and wrong or incomplete host reports hamper parasite
classification (DUNN 1968; FREELAND 1983; BRACK 1987; STUART et al. 1998).
In many reports the origin of the host individuals remains obscure. Often little or no
information is available on the origin of the host individuals (zoo or laboratory animal,
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Discussion
wild captured or a pet), how much time or contact it had with humans prior to the
parasitological examination or where the sample was taken. Parasitological reports
often lack descriptions of sizes, life stages, characteristic morphological features and
photographical documentation. Thus, the accurate identification especially for rare
parasites in wild hosts is a challenging task. DUSZYNSKI and WILBER (1997)
proposed guidelines for protozoa, the application of which would be desirable for
reports on helminths as well.
The problems of helminth identification described in this study were tackled by exact
measuring of a representative number of parasite stages and statistical analyses of
their sizes, and by a detailed literature review. Yet, for future studies it would be
desirable to apply molecular techniques to confirm morphological parasite
identification.
5.1.3 Metrics of disease risk
There are many different metrics used in epidemiological studies for measuring
disease risk. Which metrics are the most relevant is a controversial issue and
depends strongly on the aims and type of study, and on the respective host-parasite
system. While some of the employed metrics (prevalence, PSR) rely on the presence
or absence of the parasites in the hosts, others (egg/larvae output) rely on the exact
number of parasite stages in the faecal samples (MARGOLIS et al. 1982; BUSH et
al. 1997). This leads to a varying sensitivity of the metrics of disease risk.
Primarily, prevalence and PSR were chosen in this study because they are relatively
robust metrics. Based on presence/absence data and multiple sampling of
individually recognized hosts they represent valuable measures of disease risk.
However, extrapolating the hosts’ disease risk from their PSR (also from
prevalences) is difficult, as it bears the risk of underestimating the actual number of
parasite species and neglecting their pathogenic potential. Particularly in noninvasive studies on wild host populations, if the determination of parasite species is
based on morphological features, the number of encountered parasite morphospecies might not reflect the true number of parasite species (or what at that time is
considered a “species”). Yet, PSR (e.g. KENNEDY et al. 1986; GUEGAN and
Discussion
113
KENNEDY 1993; FELIU et al. 1997; MORAND and HARVEY 2000; NUNN et al.
2003; VITONE et al. 2004; EZENWA et al. 2006) and prevalence (e.g. CÔTÉ and
POULIN 1995; MÜLLER-GRAF et al. 1996; CHAPMAN et al. 2005; GILLESPIE et al.
2005; MUEHLENBEIN 2005) has been used in many meta- and field studies and
these metrics often represent the only feasible measure of quantifying the disease
risk to which the hosts are exposed.
Secondarily, egg or larvae output was taken as a surrogate measure for propagule
excretion which represents a parameter of parasite transmission (FESTA-BIANCHET
1989; KAPEL et al. 2006). In many studies on primates, egg output is applied as a
measure for parasite intensity (MÜLLER-GRAF et al. 1996; STONER 1996;
CHAPMAN et al. 2005). However, there is little evidence that the number of parasite
stages shed in the faeces is linearly correlated with the intensity of infection
(ANDERSON and SCHAD 1985; WARNICK 1992; CABARET et al. 1998; BUSH et
al. 2001). Egg output is considered a poor estimator of parasite intensity because the
individual and temporal variability in parasite stage output can be very high. This is
mainly due to several aspects of the parasite ecology: propagule shedding depends
on the density of adult female worms at the same location within the host individual;
some parasite species release eggs or larvae intermittently, and prepatent adults,
larvae or adult males do not excrete propagules at all (ANDERSON and SCHAD
1985; WARNICK 1992; CABARET et al. 1998). Another source of high variability in
egg output is the fixation and concentration technique (see 5.1.1) (FOREYT 1986;
WARNICK 1992; MES 2003). The variation can be particularly high when the number
of parasite stages in the faecal samples is low (KRAEMER 2005).
The present study was aimed at reducing the confounding effects on egg and larvae
output resulting from fluctuations of undigested food components. The total number
of specific parasite stages was referred to faecal sediment after the removal of
feeding residuals instead of “original” faecal mass. The contribution of feeding
residuals like seeds, plant fibres or other undigested food items to the original faecal
mass is very variable in the study species, particularly since the hosts often swallow
whole seeds (KNOGGE and HEYMANN 2003, TIRADO HERRERA, unpublished
data). Since the amount of feeding residuals can vary seasonally, inter-specifically
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Discussion
and individually it is necessary to control for this confounding effect. In order to cope
with short-term fluctuation and variation resulting from some aspects of parasite
ecology (e.g. intermittent egg release, prepatent periods) the mean number of
helminth stages was derived from exactly three samples per individual per season.
In conclusion, for the purposes of this study PSR and prevalence are considered
robust metrics to assess the disease risk. Egg or larvae output is seen as a variable
for probability of parasite transmission but not as an indirect measure of parasite
intensity. The detection of seasonal and host-specific patterns of parasite stage
output seems reliable due to the improvements of the respective methods
undertaken.
5.1.4 Avoiding bias
In order to reduce selection, information and confounding bias, additional
methodological improvements described in the following chapters were undertaken.
5.1.4.1 Selection bias
In order to minimize the selection bias a systematic sampling method was employed:
all group members were sampled individually on non-consecutive days three times in
each season (see also 5.1.1). MUEHLENBEIN (2005) validated this serial sampling
method and showed that it adequately determined the parasite species richness and
prevalence. The sampling of individually identified hosts in this study ensures that
prevalences are assessed accurately: prevalence refers in fact to the number of
infected host individuals divided by the number of host individuals examined (sensu
BUSH et al. 1997). HUFFMAN and colleagues (1997) underlined the risk of
underestimating the infection rates when prevalence refers to the number of affected
samples per number of all examined faecal samples as frequently calculated in
studies on wild populations. It is also necessary to consider an equal number of
faecal samples per host because the detection of parasites increases with the
number of faecal samples examined (MUEHLENBEIN 2005).
Since one group of C. cupreus left the study area very soon after the onset of this
study the obtained data for parasitological and ecological analyses for C. cupreus
Discussion
115
was based on a very small sample size. This might have lead to an underestimation
of the parasite diversity and prevalence in C. cupreus based on the observation of
just one group. Data on strata use, diet composition, home-range size and
demographic parameters refer again to just one group. In order to circumvent
possible misleading results due to a possibly unrepresentative sample size of
C. cupreus all analyses were first performed including all host species and then
excluding Callicebus. If the results were consistent over both analyses the detected
pattern was considered to be more reliable.
5.1.4.2 Information bias
The information bias that can arise during processing and measuring the samples
was reduced by several means. First, standardised methods were used, and equal
analysis conditions for all samples were achieved (same observer and technical
equipment, especially the compound microscope and ocular micrometer). Second, all
microscopic examinations were done in a blind test. Third, an intra-observer reliability
test was performed in order to determine the degree of repeatability and precision of
the microscopic examination. Finally, examination time and amount of sediment were
limited for all samples in order to balance the sampling effort.
5.1.4.3 Confounding bias
Since there are various confounding factors in complex host-parasite interaction in
the tropics, the simultaneous examination of sympatric hosts represents a good
approach to control for potential confounders such as climatic factors, predation
pressure and food distribution. Particularly, both tamarin species occur in all three
home ranges simultaneously, which allows us to draw conclusions about the
influence of the host species independently from the influence of the home ranges.
A study based on three host species of which two are very closely related has to
consider the confounding effect of phylogenetic relationship. Similarity in parasite
diversity may be a consequence of similar ecological traits, but it can also be a
product of a shared evolutionary history and shared traits inherited from a common
ancestor. Several authors have pointed out the difficulties of studies on parasite
diversity and their ecological determinants if the phylogenetic context is not
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116
considered (e.g. POULIN 1995a; GREGORY et al. 1996; MORAND and HARVEY
2000; NUNN et al. 2003; VITONE et al. 2004). However, the discussion on how far
ecological or phylogenetic factors determine parasite diversity is not yet concluded
(BUSH et al. 1990; BUSH et al. 2001; NUNN and ALTIZER 2006). Some authors
underscore the dominant role of ecological factors including geographical association
over phylogenetic traits (BUSH et al. 1990; LILE 1998; ROY 2001). Especially in less
host-specific parasites, such as the intestinal helminths detected in this study, host
ecology rather than phylogenetic background seems to shape parasite diversity (LILE
1998). Aware of the possible phylogenetic confounders, the associations between
ecological traits and PSR/prevalence were examined separately: firstly including all
host species and secondly only for the two closely related tamarin species. Future
research extending on several groups of various species that are less closely related
could provide deeper insights into the role of ecological and phylogenetic
determinants.
5.2
Parasite diversity and host-intrinsic correlates
The present study was able to determine the intestinal helminth spectrum of
S. fuscicollis, S. mystax and C. cupreus in the wild. Saguinus fuscicollis and
S. mystax harboured the same seven intestinal helminth taxa, whereas C. cupreus
harboured only three of them (four including the acanthocephalan parasite which was
recovered in the necropsy).
No intestinal protozoa (oo-)cysts were detected in 84 samples of a representative
subset of 28 host individuals. Besides the methodological concerns outlined above
(chapter 5.1.1), the absence of intestinal protozoa infection can be a consequence of
a low exposure risk of the host population in this study. Protozoan infection of
Neotropical primates seems to be closely associated with infection in humans
(KUNTZ and MYERS 1972; VITAZKOVA and WADE 2006). There is a big
discrepancy between reports of intestinal protozoa in New World primates in captivity
and in the wild. Reviews on possible protozoan species in captive primates are quite
extensive (e.g. DUNN 1968; KUNTZ and MYERS 1972; KING 1976; GOZALO and
TANTALEÁN 1996), while reports on wild New World primate hosts are rare - also in
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117
comparison to helminth parasites (e.g. HENDRICKS 1974; STUART et al. 1990;
APPLETON and BOINSKI 1991; TOFT and EBERHARD 1998; DUSZYNSKI et al.
1999; PHILLIPS et al. 2004; CARMONA et al. 2005; VITAZKOVA and WADE 2006).
To date, records of natural infection with intestinal protozoa in wild Callicebus and
Saguinus include Chilomastix, Iodamoeba, Isospora and Entamoeba (HENDRICKS
1974; PHILLIPS et al. 2004). However, records cannot exclude anthropogenic
influence because the primates were either purchased from local animal vendors
(HENDRICKS 1974) or sampled at a National Reserve where human contact was
fairly frequent (approximately 50 people per day visited the area (PHILLIPS et al.
2004)). The primates studied at EBQB are subject to minimal human disturbance: the
primates have very limited contact with humans (research staff only, no direct
contact) or human waste or faeces.
Knowledge of parasites’ life cycle is fundamental in order to examine the ecology of
host-parasite interactions. Transmission modes and obligatory intermediate hosts
especially are key factors for understanding parasite diversity. In this study at least
five out of seven parasites have an indirect life cycle relying on arthropods or
molluscs as intermediate hosts. Probably no recovered parasite taxon is transmitted
by physical contact from one primate host to the other. Even the recovered, so-called
directly transmitted parasites that do not rely on intermediate hosts are closely linked
to environmental factors (nematode larvae and “strongylids”). These are soiltransmitted parasites that involve a free-living stage and develop into the infectious
larvae in the soil over several days or weeks before they infect the next definitive
host (FLYNN 1973; ASH and ORIHEL 1987; TOFT and EBERHARD 1998).
Interestingly, all parasite taxa that are transmitted directly do not show a high
variability in prevalence: nematode larvae and “strongylid” infection affects almost all
members of all host species (nematode larvae: 90% S. mystax, 100% S. fuscicollis
and C. cupreus, “strongylids”: 71% C. cupreus, which means five out of seven, 100%
S. fuscicollis and S. mystax).
The parasite infection of S. mystax, S. fuscicollis and C. cupreus can pose an
important risk to human health because these species are commonly kept as pet
animals or used for food in rural areas of Peru and their parasites are potentially
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Discussion
zoonotic (ORIHEL 1970; FLYNN 1973; MICHAUD et al. 2003). In combination with
poor sanitation, deprived economic background and crowded housing with domestic
animals, intestinal parasitism can present a serious public health problem (MICHAUD
et al. 2003). The reported low host-specificity of the recovered parasite taxa and the
close contact between the host species and the rural population can promote the
transmission from primates to humans. Infection and the manifestation of clinical
symptoms in humans are possible for all the parasites recovered, especially the
directly transmitted parasites. It is recorded explicitly in the literature on the following
recovered parasite taxa: Acanthocephala, various Hymenolepis sp., Gongylonema
sp., Strongyloides sp. and Angiostrongylus costaricensis (ORIHEL 1970; FLYNN
1973; BRACK 1987; NEAFIE and MARTY 1993; MICHAUD et al. 2003).
5.2.1 Host species
Although S. fuscicollis and S. mystax harboured the same parasite species, the
manifested individual parasite species richness (PSR) and prevalences were
different. On average, S. fuscicollis individuals were infected with one parasite
species more than S. mystax. Prevalences of Prosthenorchis elegans, Hymenolepis
sp. and large spirurids were consistently higher in S. fuscicollis than in S. mystax
whereas the prevalence of cestode sp. #2 was higher in S. mystax. C. cupreus did
not harbour these four parasite species. The other parasite species that all host
species shared (small spirurids, strongylids, and nematode larvae) did not show
variation: they infected almost all individuals in the respective groups. In terms of egg
or larvae output, S. fuscicollis had consistently higher strongylid egg and nematode
larvae output over all seasons than S. mystax and C. cupreus.
Since taxonomically related hosts are generally more prone to infections by the same
parasite species spectrum (THOMAS et al. 1995; GREGORY et al. 1996; BUSH et
al. 2001), it is not surprising that S. fuscicollis and S. mystax harboured the same
seven parasite species. However, it is remarkable that two host species, which are
phylogenetically as close as S. mystax and S. fuscicollis differ in all metrics of
disease risk, namely individual PSR, prevalence and egg and larvae output of some
parasites. Host specificity of the recovered parasite taxa is low, thus there was no
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119
reason to expect a different parasite pattern in the three host species. However,
closely related host species are not necessarily infected with the same prevalence
and intensity or show the same pathology when infected by the same parasite
species (FREELAND 1983; THOMAS et al. 1995; LILE 1998; KAPEL et al. 2006).
There is a variety of factors that may mediate the compatibility of hosts and parasites
including ecology, physiology, immunity and genetics which can vary even between
closely related species (FREELAND 1983; KENNEDY et al. 1986; LILE 1998;
WHITTINGTON et al. 2000). THOMAS et al. (1995) showed that two closely related
and sympatrically occurring host species (amphipods) experience a strongly
contrasted parasite-induced mortality. Additionally, one parasite species infecting
related hosts can vary in its reproductive capacity as measured by egg output
(KAPEL et al. 2006). KAPEL et al. (2006) infected four natural host species of the
same family (Canidae: wolves, dogs and relatives) with the same dose of
Echinococcus multilocularis protoscolices. Subsequently, the parasite showed
differences in life-history parameters between the hosts: life expectancy, daily
fecundity, onset of reproduction and total reproductive capacity differed significantly.
Although in the present study it cannot be determined whether the differences in egg
output are due to a higher helminth reproduction (biotic potential) or a higher intensity
per host individual, the results have epidemiological consequences. Given that
sympatric host species can differ in their susceptibility to parasites, the host species
that adds more infective stages of a given parasite to the shared pool of infective
stages than the others increases the disease risk for the others. Thus, interspecific
competition can operate indirectly by parasitism when the contribution to the disease
risk is asymmetrical (HUDSON et al. 2006). The higher contribution of parasite
stages by S. fuscicollis might also represent a cost of species coexistence for
S. mystax and C. cupreus (FREELAND 1979; 1983; LOEHLE 1995).
In summary, the intestinal helminth spectrum differs between tamarins and titi
monkeys. Both tamarin species share many morphological, behavioural and
ecological traits which might cause their similarity in parasitism. Despite their
phylogenetic relationship both tamarin species differ significantly in individual PSR,
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Discussion
prevalence and egg output. This comparative study aims to detect ecological factors
of the three host species that can cause the differences in patterns of parasitism.
5.2.2 Host sex
In general, it is reported that parasite prevalence and intensity in mammals is higher
in males than in females (POULIN 1996; ZUK and MCKEAN 1996; SCHALK and
FORBES 1997; KLEIN 2000; HUDSON et al. 2002; MOORE and WILSON 2002).
The hypothesis on male bias in parasite diversity and prevalence was not supported
by the results of this study. In titi monkeys, the PSR and prevalence was similar for
both sexes. In tamarins the females exhibited a higher degree of parasitism than
males. In S. mystax, PSR was higher in females than in males and, on average, the
females of both tamarin species had a higher prevalence of most parasite species.
The female bias was most pronounced in the prevalence of P. elegans.
The majority of primatological studies failed to find evidence for sex-specific patterns
(STUART et al. 1990; STONER 1993; GILBERT 1994; STONER 1996; STUART et
al. 1998; SLEEMAN et al. 2000; ECKERT et al. 2006). Some studies found support
for a male-biased parasitism for certain intestinal parasite taxa (PETTIFER 1984;
MÜLLER-GRAF et al. 1997; GILLESPIE et al. 2005). Female-biased parasitism was
only found in four primatological studies: female baboons had a higher egg output of
a spirurid parasites (Streptopharagus sp.) than males (MÜLLER-GRAF et al. 1996).
A study on De Brazza’s monkeys (Cercopithecus neglectus) revealed a higher
prevalence of Balantidium coli and Strongyloides sp. in females (KARERE and
MUNENE 2002). Female redtail guenons (Cercopithecus ascanius) harboured some
parasite species (Strongyloides sp., Oesophagostomum sp.) that males did not
harbour (GILLESPIE et al. 2004).
There are two possible principal reasons for the female bias in intestinal parasite
infection in Saguinus: either female tamarins are more exposed or susceptible to
parasites compared to male tamarins in this study population or the exposure risk or
susceptibility of male tamarins is decreased compared to the majority of male
mammals. In the case of the titi monkeys, the males and females might be equally
exposed or susceptible to pathogens or males might experience a lower disease risk
Discussion
121
than other male mammals. The fact that P. elegans and other female biased parasite
taxa are indirectly transmitted parasites puts more emphasis on the sex-specific
differences related to food uptake or encounter with intermediate hosts (PETTIFER
1984; MÜLLER-GRAF et al. 1997). The elevated protein demands during the
pregnancy and lactation might increase insect uptake and consequently the disease
risk (GILLESPIE et al. 2004; 2005; NUNN and ALTIZER 2006). In fact, higher insect
consumption during lactation was observed in a female titi monkey (TIRADO
HERRERA and HEYMANN 2003). Differences in the endocrine-immune system or
other circumstances that result in higher social or energetic stress for females
compared to males could render females more susceptible to parasites (FESTABIANCHET 1989; ZUK and MCKEAN 1996; KLEIN and NELSON 1999; KLEIN
2000). Susceptibility of the females might be increased by an impaired immune
function due to female’s progesterone and other pregnancy related hormones. The
energetic demands and stress level might be further increased in tamarins because
they give birth to heavy and rapidly developing twins (LÖTTKER et al. 2004b).
Tamarins exhibit a polyandrous mating system characterized by a high investment in
infant care by males (GARBER and LEIGH 1997; TARDIF et al. 1997). Cooperative
infant care in callitrichids and also in titi monkeys means that males transport the
young and that in the case of the callitrichids males also share food with them
(BICCA-MARQUES et al. 2002; HUCK et al. 2004). These traits are unlikely to be
compatible with selection on high, immune-compromising testosterone levels in
males (ZUK 1990; FOLSTAD and KARTER 1992). The mating system of the
tamarins is also characterized by a high reproductive skew in that only one female
per group can reproduce. The female-female competition for the breeding position
and competition for helpers in infant care might lead to higher stress levels in female
tamarins compared to females in polygynous mating systems. Male mammals mostly
live in polygynous mating systems and seem to suffer a higher exposure risk
because of a larger body size associated with higher metabolic rate as compared to
females (POULIN 1996; ZUK and MCKEAN 1996; HUDSON et al. 2002).
Additionally, males usually exhibit costly ornaments or weapons mediated by high
testosterone levels which could compromise the immune system (FOLSTAD and
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Discussion
KARTER 1992). By contrast, male titi monkeys do not exhibit a larger body mass
than females, and in tamarins sexual dimorphism is reversed: females are larger than
males and develop larger, probably costlier scent glands and show higher
frequencies of scent marking (HEYMANN 2000; BICCA-MARQUES et al. 2002;
HEYMANN 2003b). Behavioural patterns which can increase the stress level or
exposure risk either affect both sexes equally (e.g. territorial defence) or are rare
(e.g. aggression within the group) (ROBINSON et al. 1987; GOLDIZEN 1989;
HEYMANN 1996; GARBER 1997). Stress and parasite exposure due to dispersal
after sexual maturation will also affect both sexes equally in tamarins and titi
monkeys, where both males and females leave their natal group (BICCA-MARQUES
et al. 2002; LÖTTKER et al. 2004a).
The female bias in parasite prevalences in tamarins might be related to specific
characteristics of their mating system. Several aspects, including the larger body
size, more pronounced scent glands and scent marking behaviour, higher femalefemale competition might account for the higher susceptibility or exposure of female
tamarins compared to male tamarins or females in polygynous mating systems.
These results allows us to assume that the male bias in parasitism known from
polygynous mating systems is reversed in both polyandrous primate species (ZUK
1990; MOORE and WILSON 2002).
5.2.3 Strata use
The strata use hypothesis, which states that with increasing time on the ground the
hosts should have a higher PSR and prevalence, seemed to be supported by the
data. PSR and prevalence of large spirurids, cestode sp. #2 and Hymenolepis sp.
was higher in hosts that spent more time on the ground. NUNN et al. (2003) could
not detect any effects of the host’s strata use on parasite diversity when comparing
the data set of 101 primate species. In contrast, DUNN et al. (1968) found that in
mammals of a Malayan rain forest including primates (Macaca, Nycticebus,
Presbytis, Hylobates), the ground-living mammals had the highest prevalence of
cestodes and very high prevalence of nematode parasites compared to mammals
mainly using the canopy or intermediate strata. However, these authors argued that
Discussion
123
higher prevalences were associated rather with food preferences than with ground
use. They pointed out that prevalence depends largely on the transmission mode of
the parasites. The prediction of the present study was based on the assumption that
ground contact would enhance the transmission of directly transmitted parasites that
accumulate on the ground. This has to be interpreted cautiously because all directly,
soil-transmitted parasites (strongylids, nematode larvae) had a prevalence of almost
100% across all host species (see chapter 4.3.1.1). This low variation in soiltransmitted parasites gives us to assume that these parasites colonize the three
studied host species very efficiently. On the one hand, short periods of ground
contact might be sufficient to infect the hosts: the infective larvae are highly motile
and exhibit specific behaviours to locate appropriate hosts (HAWDON and HOTEZ
1996). On the other hand, the so-called soil-transmitted parasites might be less
dependent on the actual soil for their development into the infective larvae: the
microbes on which they feed might exist not only in the soil but also in detritus
material of other forest strata that the primates have more frequent contact with
(HAWDON and HOTEZ 1996).
All helminths of higher prevalences in the hosts that spent more time on the ground
were indirectly transmitted. This gives us to assume that the stratification of
intermediate hosts might be of greater importance rather than the actual contact of
hosts with the ground.
5.2.4 Diet
The data lends support to the diet hypothesis predicting that parasite richness and
prevalences increase with higher proportion of animal prey. In this study PSR and
prevalences of two indirectly transmitted parasite taxa (large spirurids and cestode
sp. #2) scaled positively with the proportion of animal prey in the host’s diet.
S. fuscicollis consumed the largest amount of animal prey over all seasons, followed
by S. mystax and C. cupreus which was reflected in their PSR.
A meta-study on primate species showed that diet composition is an important
predictor for PSR although the study focused on the proportion of leaves in the
primates’ diet (VITONE et al. 2004). The amount of leaves in diet positively
124
Discussion
correlated with PSR which was explained by a larger body mass, higher food uptake
per se and a higher probability of consumption of contaminated food. NUNN et al.
(2003) did not find support for this hypothesis in anthropoid primates. They attributed
these results to a high proportion of directly transmitted parasites in their data set
which are decoupled from trophic transmission. A study of twelve mammal species in
India did not find empirical support for the effect of diet on either parasite prevalence
or propagule output (WATVE and SUKUMAR 1995).
The life cycle of many parasites is as yet poorly understood (STUART and STRIER
1995). Knowledge of intermediate host species of intestinal parasites is extremely
scarce and often based on experimental infection. However, the spectrum of
intermediate hosts available under natural conditions might be potentially
underestimated in experimental studies. Indirectly transmitted parasite species which
were recovered in this study require insects of the orders Lepidoptera, Coleoptera,
Siphonaptera, or Dictyoptera to complete their life cycles. One parasite (nematode
larvae) possibly needs molluscs (e.g. FLYNN 1973; SHADDUCK and PAKES 1978;
BRACK 1987; POTKAY 1992; TOFT and EBERHARD 1998; ECKERT et al. 2005).
The studied host species were observed to prey on the majority of reported
intermediate host taxa that are known for the detected parasites: the observed prey
spectrum of the three host species included amphibians, arachnids (S. fuscicollis),
Lepidoptera (only Saguinus), Dictyoptera (only by S. fuscicollis), Orthoptera,
Hymenoptera (ants only S. mystax and Callicebus). These observations were in line
with those of other research carried out at EBQB (NICKLE and HEYMANN 1996;
HEYMANN et al. 2000; SMITH 2000). However, the same study groups were
reported to feed on lepidopteran insects (Callicebus), dictyopterans (tamarins) and
coleopterans (all three species) (NADJAFZADEH 2005). The most common prey
items ingested by tamarins were insects of the order Orthoptera, mainly katydids,
whereas C. cupreus consumed mainly insects of the order Hymenoptera represented
by ants. Concerning prey diversity, the tamarins’ diversity on the level as regards
species was highest in Orthoptera (NADJAFZADEH 2005). Of the two tamarin
species, S. fuscicollis had a higher diversity of insect prey than S. mystax (NICKLE
and HEYMANN 1996). C. cupreus showed a higher prey species diversity within the
Discussion
125
order Hymenoptera, Lepidoptera and Coleoptera (NADJAFZADEH 2005). While the
number of harboured parasite species is considerably higher in both tamarin species
(maximum PSR is seven in S. fuscicollis and six in S. mystax, see chapter 4.3.1.1)
than in C. cupreus (maximum PSR is three), the proportion of animal prey does not
differ so strongly (S. fuscicollis 25%, S. mystax 19%, C. cupreus 12%). Differences in
the prey spectrum within the tamarin species might also account for the observed
heterogeneity in parasite prevalences: whereas S. fuscicollis exhibits generally
higher prevalences in indirectly transmitted parasites, S. mystax has a higher
proportion of individuals infected with cestode sp. #2. Thus, for parasite diversity, the
amount of animal prey, as well as the type and diversity of animal prey seem to play
a fundamental role.
The observed prey taxa cover all orders of potential intermediate hosts of the
recovered parasites except molluscs and fleas (Siphonaptera). This incongruity
between observed prey taxa and known required intermediate hosts can be due to
methodological problems: firstly, behavioural observations can be limited when
feeding objects are small, feeding activity is rapid or the foraging occurs in relatively
high forest strata. Some of the possible intermediate host taxa are minute and
therefore ingestion is difficult to assess (e.g. more than half of the species of land
snails are smaller than 5 mm (TATTERSFIELD 1996; TATTERSFIELD et al. 2001) or
coleopterans harbouring P. elegans are around 3 mm (STUNKARD 1965b)).
Similarly, the ingestion of tiny fleas, responsible for cestode transmission, is
concealed to the observer’s view. These fleas could be ingested while grooming.
Secondly, any research on diet spectrum based on coprological examinations or
remains of insects dropped by the consumer is limited when prey items are wingless
or highly digestible. The incongruity of the observed animal prey spectrum and
intermediate host spectrum might be also associated with aspects of multi-host
systems, for example by introduction of paratenic hosts. These hosts harbour
infective stages, but parasites undergo neither development nor reproduction in
these hosts. They are not obligatory for the completion of the life cycle, but may close
ecological or trophic gaps (BUSH et al. 2001). If certain parasite species can resort to
paratenic hosts the infection can be successful although the hosts do not ingest the
126
Discussion
known intermediate hosts for this specific parasite. In many host-parasite systems
little is known about which species might serve as paratenic hosts and to which
extent they are involved. Furthermore, since in the case of the mollusc-transmitted
Angiostrongylus costaricensis the infection can also be elicited by ingestion of mucus
contaminated plants, the primates need not eat the snails (SLY et al. 1982; BRACK
1987).
The differences in foraging strategy and foraging height which might expose them to
different parasites or intermediate hosts might also account for the observed
heterogeneities in PSR and prevalence between the three host species. S. mystax
and C. cupreus scan their environment visually for prey and mostly capture exposed
prey. S. fuscicollis manipulates substrates, enters hollow tree trunks and investigates
leaf litter, capturing mainly concealed prey (NICKLE and HEYMANN 1996;
HEYMANN and BUCHANAN-SMITH 2000; NADJAFZADEH 2005). S. mystax and
C. cupreus forage mostly in lower and middle canopy strata, whereas S. fuscicollis
forages in the understorey and on the ground (NICKLE and HEYMANN 1996;
HEYMANN and BUCHANAN-SMITH 2000; NADJAFZADEH 2005). S. mystax and
C. cupreus show great similarities in their foraging strategies, but they diverge
essentially in their parasite diversity indicating that foraging strategies might account
less for variation in parasite patterns than diet composition.
In summary, the general assumption that the amount of animal prey in the host’s diet
correlates positively with parasite diversity and prevalence for indirect parasites can
be supported. Nevertheless, given the scarcity of knowledge of potential intermediate
and paratenic host species and possibly incomplete observations of the host’s animal
prey consumption, conclusions as to the influence of host diet can only remain
preliminary.
5.2.5 Home-range size
Home-range size should be a strong predictor for PSR especially when focusing on
indirect parasites. A larger home-range size was expected to translate into a higher
PSR because of a larger sampled area and a higher encounter probability with a
greater variety of intermediate hosts. In contrast, prevalence should increase in
Discussion
127
smaller areas because of constant infection and re-infection as a consequence of a
higher accumulation of parasites and a repeated use of a confined area. The results
of this study did not provide support for either of the predictions. PSR and the
prevalence of large spirurids and cestode sp. #2 only scaled significantly and
positively with home-range sizes when including all host species. The detected
relationships between helminth diversity and home-range size do not appear very
stable because they are based on analyses where one host species (Callicebus) is
represented by a single group in the smallest home range of all study groups.
Some studies on fish (GUEGAN and KENNEDY 1993) and mammals (WATVE and
SUKUMAR 1995) did not detect an influence of home-range size on PSR and
prevalences, whereas NUNN et al. (2003) found a negative correlation between
home-range size and helminth parasite richness in 101 anthropoid primate species.
VITONE et al. (2004) found support for the positive association between helminth
PSR and home-range size of 69 primate species when restricting the analyses to
indirect parasites. Primatological field studies revealed a positive correlation between
PSR and prevalence and home-range size for muriquis (Brachyteles arachnoides) in
Brazil (STUART et al. 1993), but negative association between home-range size and
parasite prevalence in red howling monkeys (Alouatta seniculus) (GILBERT 1994).
An important aspect which cannot be neglected when examining home-range size is
host group size or density which can confound the results. Home-range size in this
study is positively correlated with group size. Thus, the sampled area for the whole
group increases, but since the group includes more members the probability of
encountering infected intermediate hosts remains the same per capita. PSR or
infection rates do not necessarily increase with larger home-range sizes if available
host individuals increase in number or density. In a study on sympatric bovids the
intestinal parasite richness and prevalence was positively associated with the degree
of habitat overlap between the species (EZENWA 2003). The larger the home-range
size the higher the probability of sharing the area with diverse other host species that
can contribute to higher parasite diversity (LILE 1998). In this study the effect of
actual overlap with hetero-specifics and conspecifics was not further determined
because the adjacent Callicebus and Saguinus groups were not under routine
128
Discussion
observation. But it would be of great interest to investigate the correlation between
home-range overlap with other primate species and additional host species
transmitting generalist parasites, e.g. birds, rodents or other mammals.
In conclusion, the data does not lend support for the hypothesis that large homerange size is correlated with a high PSR and low parasite prevalences. Before
drawing conclusions on the general effects of home-range size on parasite diversity
studies need to be extended to a larger number of host groups and to host species
with a larger variability in home-range sizes. It also appears essential to evaluate the
importance of home-range size combined with aspects of host density, host group
size and the degree of overlap with other species harbouring generalist parasites.
5.2.6 Group size and host density
PSR and prevalence were expected to correlate positively with group size and host
density. Since the contact rate between individual hosts is higher in larger groups
with higher densities, the parasite transmission should increase. In this study the
results did not support this hypothesis: PSR did not correlate with group size. When
considering tamarin groups only, group size was positively associated with the
prevalence of cestode sp. #2 but negatively with Hymenolepis sp.. Neither PSR nor
prevalence was associated with host density.
Many cross-species analyses found a positive association between PSR and host
density in mammals in general (MORAND and POULIN 1998; ARNEBERG 2002;
POULIN and MOUILLOT 2004) and in primates (NUNN et al. 2003). However,
another study on primates that examined the influence of host density on indirectly
transmitted parasite diversity failed to find support for the group-size hypothesis
(VITONE et al. 2004). Host group size was found to correlate positively with
prevalence in birds, primates and insects (CÔTÉ and POULIN 1995) and with
ectoparasites species richness in fish (BAGGE et al. 2004). In contrast, in sympatric
bovids the influence of group size on species richness and prevalence of directly
(soil) transmitted strongylids was not confirmed (EZENWA 2004a). Reports of these
demographical effects on parasite diversity in primatological field studies diverge.
Two sympatric colobine species (Piliocolobus tephrosceles and Colobus guereza)
Discussion
129
manifested the expected massive increment of Trichuris sp. prevalence after an
increase in population size and density (CHAPMAN et al. 2005). But they showed the
opposite pattern in the following study period: in one host species, prevalence
decreased subsequently with increasing host density and group size; and the other
species showed increasing prevalence although host density and group size
declined. A study on muriquis (Brachyteles arachnoides) in Brazil revealed the
highest PSR and prevalences in the largest population with the lowest population
density (STUART et al. 1993). STONER (1993; 1996) found a higher prevalence in
howler monkeys (Alouatta palliata) at a lower density compared to other howler
populations (STUART et al. 1990). GILBERT (1994) found positive correlations with
parasite prevalence and host density but no correlation with group size in Alouatta
seniculus at a field site in the central Amazonian basin in Brazil.
In many cases, the studies that found evidence for the group-size and host-density
hypothesis referred mainly to parasites transmitted by physical contact (CÔTÉ and
POULIN 1995; ARNEBERG 2002) or were not analysed separately with regard to
differences in the parasites’ life cycles (STUART et al. 1993; GILBERT 1994;
STONER 1996; MORAND and POULIN 1998; NUNN et al. 2003; POULIN and
MOUILLOT 2004). Studies that examined indirectly and soil-transmitted parasites did
not provide support for these hypotheses (EZENWA 2004a; VITONE et al. 2004).
Additionally, the results are often based on estimates of population density or size
(STUART et al. 1993) or prevalence (STUART et al. 1993; GILBERT 1994;
CHAPMAN et al. 2005) which can distort the actual correlation between prevalence
and demographic parameters. In general it is difficult to control for confounding
effects when comparing different field studies which employed diverging sampling
and parasitological methods at different sites and in different seasons (see chapter
5.1.1.1).
As mentioned above, all recovered helminth taxa in this study are either indirectly or
soil (directly) transmitted parasites which are expected to be less related to host traits
than parasites transmitted by close physical contact between definitive hosts
(ARNEBERG 2002; VITONE et al. 2004). Host group size and density does not seem
to play an important role in this study because in general the contact frequency
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Discussion
among the hosts does not influence the probability of infection with indirect parasites.
One exception might be Hymenolepis sp. which can be transmitted by fleas during
grooming activities. Yet, host density might even have an opposite effect on other
indirectly transmitted parasites compared with directly transmitted ones. In groups
with a high density, the per capita probability of ingesting infected prey would
decrease faster than the proportion of infected prey of all available prey increases.
Infection patterns of indirectly transmitted parasites may thus follow the encounterdilution theory that was put forward for arthropod-borne or mobile parasites (DAVIES
et al. 1991; CÔTÉ and POULIN 1995; NUNN and HEYMANN 2005). If the parasites
are not host-specific, the transmission dynamics get even more complicated because
the encounter then depends on the abundance of additional host or reservoir species
(rodents, primates or other mammals) which can either reduce the disease risk
(encounter reduction) or increase it (encounter augmentation) (EZENWA 2004a;
KEESING et al. 2006). This aspect is important for S. mystax and S. fuscicollis
because they live in very close association which is likely to influence the
transmission patterns for shared parasite species.
Even for directly transmitted parasites the social organisation of the hosts might be
more important than their actual number per area. BAGGE et al. (2004) argued that
in highly aggregated species, dividing the number of host individuals by the area (in
that study fish per pond) ignores the possibility that habitat use might be
synchronized within the group members. The studied primate species live in stable
and cohesive groups with very intense contact between all group members especially
during social grooming (LÖTTKER et al. 2004a; LÖTTKER et al. 2007). Thus, the
introduction of novel pathogens by immigrated, new group members is reduced and
the spread of direct parasites should be even between the highly social hosts (CÔTÉ
and POULIN 1995; EZENWA 2004a; NUNN and ALTIZER 2006).
In conclusion, for the host-parasite interaction studied here, demographic factors
such as host group size or host density that can modulate contact frequencies play a
subordinate role. The predominant helminth taxa (indirect and soil-transmitted
parasites) seem to be less related to these definitive host characters.
Discussion
5.3
131
Parasite diversity and host-extrinsic correlates
The habitat influence is of paramount importance considering the fact that almost all
intestinal parasites release their propagules into the environment (ECKERT 2000;
BUSH et al. 2001). Especially indirectly transmitted parasites depend heavily on
favourable conditions for intermediate hosts to complete their life cycle (LILE 1998;
ARNEBERG 2002). All recovered helminth species in this study rely on
environmental factors: they are either indirectly transmitted parasites which depend
on the availability of intermediate hosts, or they are soil-transmitted parasites
requiring appropriate environmental conditions for the successful completion of an
often prolonged phase of external development (FLYNN 1973; ASH and ORIHEL
1987; TOFT and EBERHARD 1998). In this study, particularly the prevalences of
P. elegans, cestode sp. #2 and large spirurids mirror the importance of host-extrinsic
factors. Although the overall model did not detect a significant influence of home
ranges (see chapter 4.3.2.1), PSR and prevalences varied between the different
home ranges, independently from the host species occupying these areas. The
lowest PSR was detected in hosts of home range West, while PSR of hosts in home
range North and East was higher. The proportion of hosts infected with P. elegans
was higher in home range West than in East and missing in North; whereas large
spirurids were missing in West and in S. mystax of home range East. Cestode sp. #2
prevalences were low in West, higher in East and the highest in North.
Various studies on intestinal parasites of wild primates have emphasized the
importance of environmental factors for parasite diversity, especially humidity and
temperature (PETTIFER 1984; MCGREW et al. 1989b; STUART et al. 1990;
STONER 1993; STUART et al. 1993; APPLETON and BRAIN 1995; MÜLLER-GRAF
et al. 1996; STONER 1996; MÜLLER-GRAF et al. 1997). However, many studies
detected a difference in parasitism over the studied groups as a by-product of the
actual study and hypothesized that environmental factors might have caused this
difference. To date, the present study is the first parasitological study on primates
that focuses systematically on a diverse array of potential habitat factors proposed to
shape parasite diversity in wild host populations.
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Discussion
Concerning the methodology of habitat characterization, it has to be taken into
account that some of the measured variables are not constant over the seasons, e.g.
leaf litter height, ground humidity, understorey density. Leaf litter is especially subject
to seasonal variation: it accumulates in the dry season (BOINSKI and FOWLER
1989). In this study, characterization was carried out in one season for all home
ranges in order to control for seasonal confounders. Hence, the comparability of the
habitat characteristics between the different home ranges should be robust although
the habitat variables may change seasonally. The number and density of sampling
points (426 points on 100 ha) was relatively high. The sample size of 40 to 60
needed to achieve good precision for all plot-less estimators is by far exceeded
(KREBS 1999). Thus, the representation of the habitat characteristics should be
relatively accurate. In order to obtain precise and comparable measurements the
instructions were followed consistently throughout the whole study area. The
methods were chosen with regard to the efficacy, practicability and time investment
under field conditions. Although the method yields only estimates with regards to
some habitat characteristics, the results can shed light on the relationship between
parasitism and habitat use.
The frequency of use of the some habitat characteristics is highly correlated and
therefore it is difficult to disentangle the respective influence on parasite diversity.
The multicollinearity of the predictor variables is almost unavoidable in this
observational study because the variables cannot be manipulated independently.
The grouping of habitat characteristics into categories might also create higher
correlations between the independent variables. Due to constraints imposed by the
necessarily limited duration of the study and the number of habituated groups, it was
not possible to collect data over a broader range or over various conditions in order
to break up the multicollinearity. Since this is an exploratory study it is of great
interest to examine the effects of a broad spectrum of habitat variables; simply
eliminating collinear variables would not represent an adequate solution of the
problem. Interpreting the detected correlations cautiously and considering important
intercorrelations this approach will aid to identify factors that need to be incorporated
in future studies.
Discussion
133
5.3.1 Ground humidity
Parasite diversity and prevalence was predicted to increase with higher ground
humidity. In this study, ground humidity, estimated by categorical measures of
ground drainage, had a weak negative influence on parasite prevalence (cestode sp.
#2). Therefore, the ground-humidity hypothesis was not supported by the data.
In general, low environmental humidity has a negative impact on the survival of
parasite stages even on supposedly resistant parasite eggs such as those of Ascaris
sp. (WHARTON 1979; ARENE 1986). When relative humidity was reduced to 75% all
eggs collapsed after 8 days compared to less than 2% eggs that collapsed at 96%
humidity (WHARTON 1979). Similarly, a number of primatological studies found
higher prevalences and intensities of intestinal parasites in areas of higher humidity
(MCGREW et al. 1989b; STUART et al. 1990; STUART et al. 1993; STONER 1996;
LILLY et al. 2001). Sympatric gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan
troglodytes troglodytes) had higher prevalences of strongylids and ascarids in
habitats characterized by large swampy areas and dense vegetation (LILLY et al.
2001). There were higher strongylid prevalences in howling monkeys (Alouatta fusca)
from riverine groups than in those from dry forest groups (STUART et al. 1990).
Similarly, a riverine troop of Alouatta palliata exhibited higher intensities than a forest
troop (STONER 1996). Consistent with this pattern, muriquis (Brachyteles
arachnoides) revealed higher prevalences in more humid areas (STUART et al.
1993). Baboons (Papio anubis and Papio papio) and chimpanzees (Pan troglodytes
schweinfurthii) had a higher nematode prevalence at Gombe than at Mt. Assirik, the
former region showing higher humidity, moister soils and milder temperatures than
the latter (MCGREW et al. 1989b).
The conditions at the field site EBQB are described as very humid after the Holdridge
system (GARBER 1988). The minimum rainfall per month over the whole study
period was 118 mm and the total annual precipitation was over 3400 mm (see
chapter 4.3.3.2). Even in the driest month (June 2002), there were no more than five
consecutive days without rainfall. The humidity varies generally between 80 and
100%. The generally very moist conditions on the forest ground, further improved by
shading vegetation, leaf litter and deadwood, therefore probably offered sufficiently
134
Discussion
favourable conditions for parasite development and survival. In regions where
considerably dry and/or hot periods restrict the zones of parasite survival, areas that
maintain constant humidity might be of greater importance (MCGREW et al. 1989b).
In this study, the “poor drainage” category was characterized by a very moist
environment including areas with stagnant water or muddy soil in at least three out of
four sections. This very high moisture might exceed the optimum for most parasites.
Other important resources for intermediate hosts like leaf litter might be limited.
HAUSFATER and MEADE (1982) observed that on moist soils, a substantial part of
the deposited parasite eggs were destroyed by fungi and other soil micro-organisms.
Another important aspect of the present study is that in areas with very high ground
humidity, the hosts do not come to the ground for foraging purposes which would be
correlated with lower animal prey consumption as described above.
In summary, it is difficult to draw a final conclusion here as to the role of ground
humidity on parasite diversity because the constant, very humid climatic conditions in
the study area may already provide advantageous conditions for parasite
development. In turn, extreme moisture might even bring about negative effects for
external parasite stages.
5.3.2 Soil type
The time that hosts spend on clay soil was expected to have a positive influence on
parasite diversity and prevalence. The results of this study were contrary to the
predictions: PSR and the prevalences of cestode sp. #2 and large spirurids were
lower if hosts spent more time on clay soils.
Various studies of human parasites highlighting the importance of soil type for
parasite prevalences revealed diverse and opposing results (AUGUSTINE and
SMILLIE 1926; SORIANO et al. 2001; MABASO et al. 2003; PIERANGELI et al.
2003; SÁNCHEZ THEVENET et al. 2004; SAATHOFF et al. 2005a; SAATHOFF et
al. 2005b). On sandy soils AUGUSTINE and SMILLIE (1926) detected a higher
hookworm prevalence in children in Alabama. SAATHOFF et al. (2005a; 2005b)
found a strong negative influence of clay soil on prevalence of hookworms, but a
positive on Ascaris sp. prevalence in school children in South Africa. However, to our
Discussion
135
knowledge, the influence of soil type on primate parasites had not been studied
previously.
The results of the studies mentioned above seem to indicate a different influence of
soil type depending on the mobility of the parasite stages. It appears that clay soil
provides
advantageous
conditions
for
immobile
parasites
(eggs)
but
disadvantageous conditions for mobile parasites (larvae). The compact structure of
clay soils impedes the escape of mobile parasites from adverse environmental
conditions, whereas immobile parasites are not washed out and survive better in clay
soils (VINAYAK et al. 1979; MIZGAJASKA 1993; SAATHOFF et al. 2005a;
SAATHOFF et al. 2005b). But in this study the parasite prevalences of mobile (larvae
of strongylid and other nematodes) and immobile (all excreted eggs) parasites did
not seem to depend on the clay soil conditions mentioned. The prevalences of
parasites with mobile stages are not likely to depend on soil characteristics because
they show high values over all primate groups no matter how frequent their use of
clay or sand soil is (mean prevalence of strongylids is 94% and of nematode larvae
93%; see chapter 4.3.1.1). The negative influence of time on clay soil on prevalence
of some helminths with immobile stages (large spirurids and cestode sp. #2) might be
due to a different aspect. For the study groups the areas of clay soil coincided with
steep slopes which in combination probably promotes horizontal washout of the
parasite stages. Heavy, tropical rainfall can rinse them out to the creeks where they
become unavailable for infection. The frequency of use of clay soils correlated
negatively with the use of areas of a high abundance of leaf litter which can serve as
important resources for intermediate hosts. This intercorrelation could account for the
low parasite prevalences of large spirurids and cestodes in the study groups. The
relatively impermeable texture of clay might also inhibit the passive access of
parasite stages into deeper layers of the soil which would be essential for protection
against adverse environmental conditions and parasite predators, e.g. dung beetles
(FINCHER 1973; STOREY and PHILLIPS 1985; STROMBERG 1997; LARSEN and
ROEPSTORFF 1999). Experimental studies observed the highest survival rates in
Taenia eggs which were buried in the soil deeper than 10 cm (STOREY and
PHILLIPS 1985). Especially, the impact of dung beetles on unprotected parasite
136
Discussion
stages is massive: they can destroy up to 35% of the eggs compared to areas
without beetles (FINCHER 1973; HAUSFATER and MEADE 1982). At EBQB around
30% of the tamarin faeces were buried and probably preyed on by dung beetles
(L. Culot, pers. comm.). Another adverse effect on parasite survival could be the
limited aeration in clay soils (MABASO et al. 2003). For example LARSEN and
ROEPSTORFF (1999) pointed out that a lack of oxygen reduces the viability of
Ascaris eggs. Other important soil characteristics such as acidity, salinity, mineral
and nutrient content was not considered in the present study. Laboratory
experiments under defined soil conditions analysing a set of abiotic factors
separately would enable us to determine their role for parasite diversity. To better
understand the effects of soil type, it would be helpful to differentiate between mobile
and immobile parasites in future studies. Finally, for indirectly transmitted parasites
the soil type might play a subordinate role compared to the factors influencing
intermediate host abundance.
5.3.3 Habitat morphology
Habitat morphology was expected to influence parasite diversity by shaping the
possibility of parasite stage accumulation in the host’s habitat. On even grounds the
horizontal washout of parasite stages should be lower than on steep terrains so that
parasites can accumulate and develop into infective stages. In agreement with the
prediction, PSR and prevalence of cestode sp. #2 and large spirurid were higher in
groups that used flat terrain more frequently. However, the use of flat terrain was also
highly associated with the use of areas of high leaf litter layers and high deadwood
abundance which complicates the interpretation of the data.
5.3.4 Resources for intermediate hosts
The high abundance of resources for intermediate hosts, especially leaf litter and
deadwood abundance, should translate into a higher PSR and prevalence of
indirectly transmitted parasites. The present study found some evidence for the
expected favourable effect of leaf litter: the use of zones with high leaf litter
contributed to high PSR and high prevalence of two indirectly transmitted parasites
Discussion
137
(cestode sp. #2 and large spirurids). Yet, the prevalence of P. elegans showed an
opposite pattern: it was negatively related to leaf litter height. The expected positive
effect of deadwood was not confirmed: only cestode sp. #2 prevalence was
significantly associated with the time spent in areas with high deadwood abundance,
but the correlation was negative.
Leaf litter can have several positive effects on the abundance of parasites and
intermediate hosts: it provides nutrients and shelter for a great variety of arthropods,
and it can regulate microclimatic conditions (PFEIFFER 1996; DALY et al. 1998;
SAYER 2006). Some studies revealed a positive correlation of leaf litter height and
litter arthropod abundance (BULTMAN and UETZ 1984; FRITH and FRITH 1990).
LASSAU et al. (2005) showed that diversity and abundance of beetles, the largest
order of insects and important intermediate hosts, correlated positively with the
amount of leaf litter. The higher abundance of intermediate hosts in areas with higher
leaf litter layer could have led to higher prevalences in hosts that frequent these
areas.
The prevalence of P. elegans did not seem to be influenced positively by deadwood
abundance although most of the identified intermediate hosts (generally cockroaches
and beetles) live on detritus material. Basic knowledge of the intermediate host
spectrum of P. elegans is derived from experimental studies or studies on laboratory
animals (STUNKARD 1965b; SCHMIDT 1972; KING 1993; GOZALO 2003).
However, experimental studies cannot examine the wide array of potential
intermediate host species that may be relevant in the wild. The studies focus on
potential intermediate hosts that play a role in primate husbandry but might not even
exist in a natural setting. Thus, probably many intermediate host species and their
diverse ecological requirements are yet unknown. This complicates the identification
of ecological factors in the host’s environment that drive transmission patterns for
specific parasites.
Deadwood abundance, counter to expectations, did not influence parasite diversity.
This might be due to the relatively rough method of estimating the abundance of
deadwood which did not include its quality for potential intermediate hosts. First of all,
138
Discussion
an appropriate surrogate measurement for quantitative deadwood availability is
considered the basal area of deadwood (GROVE 2002b). In the same study this
parameter correlated strongly with beetle species richness and abundance (GROVE
2002b). Second, the method used in the present study did not include the following
aspects of deadwood quality that are potentially relevant for intermediate host
abundance: the degree of deadwood decomposition, the tree species, elevation of
logs from the ground, the presence of bark and volume of coarse woody debris are
also expected to have an influence on the arthropod composition (GROVE 2002a; b;
KELLY and SAMWAYS 2003). In tropical areas young logs, elevated from the
ground, with 80% of the bark remaining harboured the most species-rich arthropod
community (KELLY and SAMWAYS 2003). The role of deadwood abundance on
parasite diversity merits further exploration by means of more detailed descriptions of
deadwood abundance and quality for intermediate hosts.
In summary, the present results indicate that the general pattern of intestinal helminth
diversity can be linked to the abundance of resources for intermediate hosts.
However, due to limited knowledge of the life cycles of most parasites and the
requirements of their intermediate hosts it is difficult to predict infection patterns on a
smaller scale. In order to examine the role of resources for parasite diversity on a
larger scale, future studies need to focus on a larger number of host species
harbouring various parasites that rely on identified intermediate hosts.
5.3.5 Vegetation density
Denser vegetation was expected to offer more favourable conditions for excreted
parasite stages and some taxa of intermediate hosts. Thus, hosts ranging more time
in dense vegetation should harbour a greater variety of parasites with higher
prevalences. In this study, high density of trees more than 10 cm DBH had a positive
influence on helminth diversity and on the prevalences of two indirectly transmitted
parasites, but correlated negatively with P. elegans prevalence. Understorey density,
in contrast, was found to correlate weakly with PSR and prevalence of cestode sp.
#2.
Discussion
139
Dense vegetation constitutes more favourable and stable microclimatic conditions for
parasite stages in terms of humidity, temperature and protection from sunlight. A
study on hookworm and Ascaris infection in South Africa revealed a strong positive
association of prevalence and vegetation density (SAATHOFF et al. 2005a;
SAATHOFF et al. 2005b). Several experiments have shown the detrimental effect of
temperature increases, humidity loss and ultraviolet light on the fitness of parasite
stages (WHARTON 1979; ARENE 1986; UDONSI and ATATA 1987). Relatively
small changes in temperature or humidity due to forest gaps or lighted spots can
reduce viability and infectivity of eggs and larvae. Even supposedly extremely
resistant, thick-shelled parasite eggs are vulnerable to such changes (WHARTON
1979; ARENE 1986). Higher temperatures speed up development of the eggs but
they have adverse effects on the parasites’ fitness: lower hatching rate, reduced
survival, desiccation tolerance and penetration activity of the larvae (ARENE 1986).
In the case of Ascaris eggs, temperatures of about 30°C decrease the survival rate
by around 30% and the penetration ability by around 60% compared to eggs
embryonated at 26°C (ARENE 1986). Reduced humidity significantly decreases the
survival of parasite eggs (see chapter 5.3.1). A deleterious effect of ultraviolet light on
parasite stages has been proposed by many authors (VINAYAK et al. 1979;
STOREY and PHILLIPS 1985; LARSEN and ROEPSTORFF 1999; SAATHOFF et al.
2005a). UDONSI (1987) showed that after two days at a constant temperature
(30°C), the survival rate of Necator americanus larvae in the shade was 40% higher
than in the sunlight. Additionally, high vegetation density seems to foster the
abundance of some intermediate host taxa: SHELLY (1988) found a higher
abundance of Coleoptera, Formicidae and Psocoptera in dense, shaded vegetation
than in gaps in lowland rainforest.
Surprisingly, the density of trees of more than 10 cm DBH had a significant effect on
prevalence of cestode sp. #2 and large spirurids whereas density of the understorey
(vegetation height less than three meters) did not. Two aspects of the method might
have influenced this outcome. Firstly, the specific composition or characteristics of
the vegetation were not determined in this study. This aspect might have a
considerable impact on the abundance of some intermediate host taxa that are
Discussion
140
closely linked to certain qualities of the vegetation, e.g. leaf-eating insects (PATZ et
al. 2000). Secondly, the method did not assess density quantitatively but by
categories of visibility. The category “dense understorey” is characterized by very
limited visibility which might be influential on the behaviour of the hosts. In areas with
very poor visibility the studied primates rarely come to the ground. This is probably
due to an increased risk of predation in habitats where the prey’s visual field is
obscured and detection of approaching or hidden, terrestrial predators is more
difficult (LAZARUS and SYMONDS 1992; COWLISHAW et al. 2004). In turn, if PSR
and parasite prevalences are influenced by the time hosts spend on the ground,
ground use might affect the underlying pattern more than the favourable conditions
for parasites in dense understoreys.
Taken together, although not reflected in the overall model in this study, habitat
characteristics seem to contribute to shaping assemblages of parasite communities
particularly of indirectly transmitted parasites like large spirurids and cestode sp. #2.
However, some parasite taxa (directly transmitted parasites and the small spirurids)
did not seem to depend on the measured environmental factors. The prevalence of
P. elegans, large spirurids and cestode sp. #2 showed a correlation with the use of
specific areas. The higher the frequency of use of areas of high leaf litter abundance
and dense vegetation the higher the prevalences. The use of clay soil and areas with
poor drainage and high deadwood abundance were negatively correlated with
helminth prevalences. It is unlikely that single habitat characteristics shape parasite
diversity, and intercorrelations between various factors make it difficult to disentangle
the effect of single habitat factors. Corresponding to the exploratory character of this
study it has to be underlined that the results should be seen as preliminary. Studies
on a broader array of parasite taxa, host species and habitat variables need to be
conducted before a more generalized statement can be made about the impact of
habitat characteristics on parasite diversity.
5.4
Seasonal variation in parasite diversity
Seasonally varying factors may operate on host-intrinsic and -extrinsic factors as well
as on parasites themselves. Environmental factors like temperature and humidity are
Discussion
141
intimately linked with host-intrinsic factors that can modify the host’s susceptibility.
However, environmental factors can also directly affect the viability of parasite stages
outside their hosts and the abundance of intermediate hosts, thus increasing the
infection risk of the hosts. This study focused on two aspects of seasonality: firstly,
the increased exposure risk due to environmental factors that enhance parasite
fitness (environment hypothesis); and secondly the increased host susceptibility due
to a poorer nutritional status (nutritional-status hypothesis). Both hypotheses lead to
diverging predictions: The environment hypothesis leads to the prediction that PSR
and prevalence should increase in the rainy season due to increased survival of
parasite stages. The nutritional status hypothesis predicts that PSR and prevalence
should decrease in the rainy season due to higher food availability.
The results here indicate that PSR did not show a consistent seasonal pattern over
all host species. The median PSR was lower in the rainy season for C. cupreus, but
did not differ between the seasons in S. mystax and S. fuscicollis. The prevalence of
all parasites was similar in the rainy and dry season. The egg output of large
spirurids was significantly higher in the rainy season in both host species and the
same was true for P. elegans, but only in S. fuscicollis. The observed seasonality in
PSR of C. cupreus might be associated with a small sample size of C. cupreus due
to the absence of group Puerto in the wet season. Only five individuals were sampled
for both seasons. The seasonal variation in egg output of two parasite species was
significant but relatively low: the mean egg output raised by two eggs per sample for
large spirurids and P. elegans in the rainy compared to the dry season (see chapter
4.4). Comparable studies detected seasonal variations in egg output of two intestinal
parasite species of chimpanzees, where mean egg production showed increases
from under 50 propagules per 1 g faeces to over 200 (maximum 1000) after the
onset of the rainy season (HUFFMAN et al. 1997). The variation in egg output
observed in this study is so low that it is difficult to see a significant seasonal effect.
Hence, the data provided very limited support for a seasonal pattern in PSR,
prevalence and in propagule release.
Some primatological studies lend support for the hypothesis of seasonal variation in
parasitism. ECKERT et al. (2006) detected a higher prevalence of nematode larvae
142
Discussion
in Alouatta pigra during the rainy season. Seasonal variability in egg output and
prevalences was also evident in chimpanzees (Pan troglodytes schweinfurthii):
prevalences of nematode larvae, Oesophagostomum sp. and egg output of Trichuris
sp. and Oesophagostomum sp. was higher in the rainy than in the dry season
(HUFFMAN et al. 1997). Baboons (Papio ursinus) exhibited higher intensities of a
cestode (Bertiella studeri) and a nematode (Oesophagostomum bifurcum), but lower
intensities of Trichostrongylus sp. during the rainy season (PETTIFER 1984). Many
studies on intestinal parasites in primates did not find seasonal differences either in
PSR, parasite prevalences or in egg output (MCGREW et al. 1989b; GILBERT 1994;
MÜLLER-GRAF et al. 1997; GILLESPIE et al. 2004; 2005; VITAZKOVA and WADE
2006). The cited studies give a diverse picture of seasonal patterns in parasitism.
Clear seasonal changes in prevalences, intensities or egg output were often limited
to very few parasite species. Additionally, changes were observed at sites of very
pronounced seasonality in terms of temperature and/or rainfall (PETTIFER 1984;
HUFFMAN et al. 1997). The majority of the studies did not detect a consistent
seasonal pattern.
5.4.1 Host susceptibility related to the nutritional status
The nutritional status of wild primates can vary as a function of food availability and
quality (GOLDIZEN et al. 1988; KOENIG et al. 1997). When ripe fruit was scarce
free-ranging S. fuscicollis suffered a mean weight loss of 5.8% (range 0.5-13.5%)
(GOLDIZEN et al. 1988). The phenological method employed in this study is most
likely to reflect the seasonal changes of food abundance as a surrogate measure for
the nutritional status of the hosts (CHAPMAN 1992; HEIDUCK 1997; STEVENSON
et al. 1998). The results demonstrate that at the study site fruit availability is
significantly higher in the rainy than in the dry season. Especially frugivorous
primates like the three study species rely on the availability of ripe fruit to cover their
energetic needs because they provide a rich source of simple sugar (RICHARD
1985; PERES 1994). However, insect consumption is also of importance because
primates can supply their demand of proteins, fat, and essential minerals (RICHARD
1985). Animal prey abundance, namely arthropods and amphibians, was not
Discussion
143
determined in this study but is also expected to be higher in the rainy season
(TANAKA and TANAKA 1982; PEARSON and DERR 1986; SHELLY 1988; FRITH
and FRITH 1990; WATLING and DONNELLY 2002). The observed frequency of
feeding on fruit or animal matter did not differ over the seasons across all primate
groups although fruit and insect availability is supposed to be higher in the rainy
season. Yet, primates do not have to invest as much energy in searching for food as
in periods of food scarcity and they can select the best quality items.
Taken together, the overall nutritional status of the studied hosts should be better in
the rainy season because of higher food availability. This should translate into better
immune responses (BUNDY and GOLDEN 1987; HOLMES 1993; BEISEL 1996;
COOP and HOLMES 1996; KOSKI and SCOTT 2001) and a lower PSR and lower
parasite prevalences of the hosts.
The inferred better nutritional status in the rainy season does not coincide with lower
PSR, prevalence or egg/larvae output. The lack of seasonality in PSR and
prevalence in the study species might be due to a less pronounced immunosupression in the dry season. The degree of malnutrition might be lower than
expected because the primates can circumvent bottlenecks of fruit scarcity by shifting
their diet to other food plants or components to fulfil their energy demands (PERES
1994). For example, tamarins can switch to Parkia sp. exudates or nectar of
Symphonia sp. (PERES 1994; 2000) and titi monkeys to higher seed or leaf
consumption (WRIGHT 1989; HEIDUCK 1997). Additionally, the phenological
method can mirror a general pattern but single fruiting trees with an irregular fruiting
pattern, e.g. Parkia sp., might represent significant resources to alleviate fruit scarcity
(PERES 2000). And finally, the overall immune status might be less affected because
energetically costly periods like gestation, lactation and infant-carrying fell into the
period of maximum fruit availability (SOINI and SOINI 1990; LÖTTKER et al. 2004a).
5.4.2 Host exposure
The viability of parasite stages is higher in moist and warm conditions (e.g.
WHARTON 1979; UDONSI and ATATA 1987; BETHONY et al. 2006). Similarly, the
abundance of arthropods and amphibians, important groups of intermediate hosts, is
144
Discussion
generally higher in warmer and more humid seasons (e.g. TANAKA and TANAKA
1982; PEARSON and DERR 1986; WATLING and DONNELLY 2002). Thus, the
exposure risk for the hosts should be higher in the rainy season which in turn, should
lead to a higher PSR and parasite prevalence of the hosts.
The climatic conditions at the field site are very humid as outlined above (see chapter
4.3.3.2 and 5.3.1). In addition the minimal temperature did not drop below 17°C (at
night time during the few "cold" days of the year). These constantly warm and humid
conditions seem not to significantly hinder parasite survival and development so that
parasite exposure is similarly high over the seasons. Studies that detect seasonal
patterns of infection dynamics were carried out at places where the climate shows
pronounced hot and/or dry phases (PETTIFER 1984; HUFFMAN et al. 1997;
ROEPSTORFF and MURRELL 1997; PIERANGELI et al. 2003). The expected
beneficial influence of increased humidity in the rainy seasons might have had even
opposite effects on the viability of excreted parasites stages. For example, parasite
stages in the environment can equally be cleared away by heavy precipitations
(NUNN and ALTIZER 2006) and the activity of egg destroying organisms is
enhanced in humid and warm seasons (HAUSFATER and MEADE 1982; LARSEN
and ROEPSTORFF 1999).
The postulated fluctuation of intermediate host abundance might also be a
consequence of more marked seasonality (JANZEN and SCHOENER 1968). The dry
season during the study period might not have led to such a negative impact on the
arthropod abundance that parasites experienced a bottleneck of intermediate hosts.
Seasonal arthropod abundance can diverge considerably from the general pattern
because the arthropod taxa differ in their main food sources (BUSKIRK and
BUSKIRK 1976; BOINSKI and FOWLER 1989; PINHEIRO et al. 2002). Herbivorous
arthropod abundance is tied to young leaf occurrence, whereas detritivorous
arthropods like collembolans, isopods and cockroaches peak when dead leaves are
abundant (BUSKIRK and BUSKIRK 1976; BOINSKI and FOWLER 1989). Thus, a
general abundance pattern of arthropod orders may be less relevant for the
transmission of a specific parasite species which requires certain intermediate hosts
to complete its life cycle. By contrast, high intermediate host abundance might also
Discussion
145
have a negative influence on PSR and prevalence. The abundance of arthropods can
increase markedly in wet seasons, in terra firme forests up to 2.3 times (PEARSON
and DERR 1986). Since parasite egg/larvae output and arthropod uptake by hosts do
not increase considerably, but arthropod abundances increase in the wet season, the
per capita probability of encountering infected intermediate hosts decreases in the
wet season (encounter reduction) (KEESING et al. 2006). Thus, higher arthropod
abundance might translate into a lower individual disease risk.
There are two aspects of parasite ecology that make it difficult to study seasonal
effects on parasite exposure: Firstly, even if parasites suffered from deficient
transmission pathways in the dry season they could bridge the temporary bottleneck
of intermediate hosts by using paratenic hosts (BUSH et al. 2001). Secondly,
parasite diversity would not reflect seasonal changes in exposure risk when the life
span of the parasites is long enough to outlive the adverse effects of the seasons.
Many human intestinal parasites that can also infect primates are known to have a
life span or a persistence of infection of over one year up to 25 years, e.g.
hookworms, Strongyloides stercoralis, Trichostrongylus spp., Hymenolepis nana
(ASH and ORIHEL 1987; BETHONY et al. 2006). Once the infection is established
and the host’s defences or self-medication do not expel the parasites, the effects of
seasonally varying exposure risk might be less measurable in terms of PSR and
prevalence.
In conclusion, the results indicate that in the studied populations the seasonal
variation of parasite diversity is not pronounced. The examined aspects of
seasonality, namely nutritional status and climatic conditions, might not affect host
susceptibility and/or exposure, or parasite viability, in the way that seasonal variation
in PSR, prevalences or egg/larvae output was detectable. The possibility cannot be
excluded that both aspects have opposite effects which can outweigh each other.
5.5
Parasites and their impact on the host’s survival
It is difficult to measure the actual impact of parasites on the survival of wild hosts.
Different metrics, namely parasite species richness (PSR) and prevalence in this
146
Discussion
study, aimed at evaluating the disease risk for host individuals or populations. While
prevalence is related to the probability of infection for the host individuals, the
number of different parasite species (PSR) is more strongly associated with the
outcome of infection, the probability of morbidity or mortality (MORALES-MONTOR et
al. 2004; CHAPMAN et al. 2005). However, the quantitative measurement of the
number of parasite species does not necessarily reflect the actual pathogenic
potential of the parasite assemblage. The potential pathogenicity of each single
parasite species and their interactive effects should be taken into account when
assessing the outcome of the infection and the impact on the host’s fitness. Infection
with one highly virulent parasite species may have a more detrimental effect on the
host than the infection with several other, less virulent parasite species. Evaluating
parasite pathogenicity is particularly difficult because the manifestation of disease
symptoms depends on the interaction of many host- and parasite-intrinsic factors
(BUSH et al. 2001). Most insights into pathological impacts are obtained by
laboratory studies in which hosts on the one hand might show more severe
pathologies because of additional stress, crowding and lack of appropriate nutrition.
On the other hand, hosts in captivity might present less severe pathologies because
inter- and intraspecific competition for food resources is less than in the wild. Hence,
the same parasite species might be almost non-virulent or can cause severe
pathologies, depending on the conditions influencing host and parasite (BRACK
1987; TOFT and EBERHARD 1998). This can result in an enormous variation of the
impact on host fitness and the regulation of host populations. In the following section
the pathological alterations in the female titi monkey are discussed with regard to the
impact of the detected parasites.
The adult female titi monkey did not show conspicuous behavioural alterations until
one day before it died. On the last day it showed an apathetic behaviour and did not
stay close to the other two group members as normally. Its nutritional status was
poor; with 720 g the body weight was markedly below the range of mean adult body
weight (adult C. cupreus female: 750-1000 g (SMITH and JUNGERS 1997; BICCAMARQUES et al. 2002)). Parasites belonging to two different species were detected:
Discussion
147
adult acanthocephalan worms of the species Prosthenorchis elegans were recovered
from the small intestine and a pentastomid nymph from the abdominal wall.
The major findings of the necropsy concerned alterations in the digestive system,
liver, spleen and abdominal cavity. Severe multifocal subacute to chronic enteritis of
the small and large intestine was diagnosed. Multiple ulcers affected severely all
layers of the intestinal wall. Severest chronic lesions were associated with the
presence of P. elegans, others resulted probably from former parasite attachments
(KING 1993). Multifocal hepatitis with evidence of granuloma and necrosis accounts
for an infectious aetiology. Agents capable of causing such hepatitis include viruses,
bacteria, fungi and helminths (KELLY 1992; HERMANNS 1999). In the present case
the test for bacteria, viruses and fungi gave negative results. In contrast, the
centrolobular liver cell necrosis is usually characteristic for toxic degeneration
(KELLY 1992; DAHME and WEISS 1999). Two explanations for the hepatitis seem
possible: the hepatitis may have developed as a response to pathogen infection or as
a consequence of toxins which stem from the digestive tract. Given that the gut
barrier manifested functional disorders due to the parasitic ulcerative enteritis, enteric
bacteria, their metabolites and toxins can pass the mucosal barrier and reach extraintestinal sites, especially the liver via the portal stream (DAHME and WEISS 1999).
Lymphoid depletion was observed in the spleen. Secondary follicles, representing
activated lymphatic tissue, were not present. The spleen is an important organ for
primary and secondary immune responses: the white pulp providing lymphocytes and
plasma cells for cellular and humoral specific immune defence (DAHME and WEISS
1999). Lack of secondary follicles may account for reduced immune activity and
hence an increased risk of infection.
The parasite recovered from the abdominal wall was probably a pentastomid nymph
of the family Porocephalidae. Except for one genus, pentastomids are usually
parasites of serpents including arboreal snakes such as boas (SELF and
COSGROVE 1972; TOFT and EBERHARD 1998) and use mammals as intermediate
hosts (NELSON et al. 1966; SELF and COSGROVE 1972). The two pentastomid
genera Porocephalus (South America, Africa) and Linguatula (cosmopolitan) infect a
wide range of New World primate species (Callicebus caligatus, Cebus apella,
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Discussion
Saimiri sciureus, Callimico goeldii, Saguinus fuscicollis and Saguinus nigricollis)
(DUNN 1968; COSGROVE et al. 1970b; SELF and COSGROVE 1972; TOFT and
EBERHARD 1998). Primates function as intermediate hosts and get infected orally
through water and food contaminated with serpent faeces, nasal secretion or exuvia
(SELF and COSGROVE 1968; COSGROVE et al. 1970b; SELF and COSGROVE
1972; TOFT and EBERHARD 1998). Eggs hatch in the gut, and the liberated larvae
migrate to various tissues where they moult into nymphs. Snakes ingest pentastomid
nymphs when they prey on primates or other infected mammals (SELF and
COSGROVE 1972). The usual location of pentastome nymphs are lungs, liver,
serosa and other tissues including the leptomeninx (NELSON et al. 1966; SELF and
COSGROVE 1968). Inflammatory responses elicited by dead nymphs are of major
pathological importance compared to the lesions induced by living nymphs (NELSON
et al. 1966). In rare cases, fatal peritonitis is reported (SELF and COSGROVE 1972).
In the present case, no signs of inflammation were observed.
In conclusion, the results of the necropsy and histopathological examinations suggest
that the acute and chronic infection with P. elegans had a strong detrimental effect on
the female titi monkey. The occurrence of ulcers, scar tissue and diffuse chronic
enteritis associated with P. elegans reduced the digestive function of the intestine
and affected the barrier function against intruding pathogens and toxins. Thus, in the
present case infection with P. elegans had a massive and long-term impact on the
host’s resource utilisation and the defence mechanisms in the digestive tract. The
chronic parasitic infection with P. elegans could have even caused the death of its
host due to severe hepatitis. The lymphoid depletion of the spleen may have
impaired the immune status additionally. Parasite infection with pentastomids seems
not to have caused any local inflammatory reactions or further impairment of health.
Since insights into the pathological impacts of parasites on wild hosts are very
difficult to obtain, even single cases like the one reported in this study can provide
valuable information on how the parasites can damage the host’s tissues and organs.
Furthermore, the detection of adult intestinal parasites enabled exact parasite
identification and a positive match with the excreted eggs in faecal samples of other
studied hosts.
Discussion
5.6
149
Conclusions
This study investigated the role of host-intrinsic traits and environmental factors for
parasite species richness (PSR) and parasite prevalences of intestinal helminths of
three sympatric New World primate species.
The host species represented an important predictor for PSR. Both tamarin species
(Saguinus mystax and Saguinus fuscicollis) had a completely overlapping spectrum
of intestinal parasites: they harboured all of the seven detected helminth taxa.
Callicebus cupreus harboured only four taxa out of the seven recovered from the
tamarins. Despite the overlapping spectrum of intestinal parasites in both tamarin
species that are closely related, on average, individuals of S. fuscicollis were infected
with a larger number of different parasite species (PSR), exhibited a larger proportion
of individuals infected (prevalence) with Prosthenorchis elegans, Hymenolepis sp.
and large spirurids, and excreted more eggs of “strongylids” and nematode larvae
compared with individuals of S. mystax. Due to higher infection rates and higher
egg/larvae output, S. fuscicollis added more infective stages to the shared pool of
infective stages than S. mystax and therefore S. fuscicollis potentially increased the
disease risk for the other sympatric species. This might also represent a cost of
species coexistence.
The results suggest that the male-biased parasitism predominating in polygynous
mating systems is reversed in the polyandrous tamarin species. The female bias in
intestinal helminth prevalences in tamarins may be associated with specific
characteristics related to the hosts’ mating system. Several aspects, including the
larger body size and higher female-female competition might account for the higher
susceptibility or exposure of female tamarins. Directions for future research need to
include specific immunological and endocrine parameters in order to identify possible
mechanisms for the observed female bias.
The results reinforce the idea that the spectrum and amount of animal prey play an
important role for helminth diversity and prevalence for indirectly transmitted
parasites. Nevertheless, given the scarcity of knowledge of potential intermediate
and paratenic host species, conclusions on the influence of host diet can only be
150
Discussion
tentative. The effect of group size and host density did not seem to account for the
heterogeneity in parasite infection patterns. Since most of the recovered parasite
taxa were transmitted by intermediate hosts and therefore do not depend on the
physical contact between the primates, these results are not surprising. Future
studies need to incorporate information of the parasitic life cycles which should allow
a more detailed view of the underlying transmission patterns.
PSR and parasite prevalences of three of the seven parasite taxa varied
considerably over the three home ranges of the Saguinus species although the
overall statistical model revealed no significant influence of the host’s home range.
The prevalences of P. elegans, large spirurids and cestode sp. #2 were associated
with the use of specific areas within the home ranges of the groups. The higher the
frequency of use of areas with very abundant leaf litter and dense vegetation the
higher the prevalences of large spirurids and cestode sp. #2. The time ranging on
clay soil was negatively correlated with large spirurids and cestode sp. #2, and the
use of areas of high deadwood abundance was negatively correlated with
prevalences of the latter. P. elegans showed an opposite trend with respect to the
use of the same habitat characteristics. Multiple habitat characteristics are likely to
interact to affect parasite diversity. Multicollinearity between the frequencies with
which various habitat factors were used made it difficult to disentangle the effects of
single habitat variables. Corresponding to the exploratory character of this study it
has to be underlined that the results can only be tentative.
No seasonal pattern was detected either in PSR, parasite prevalences or in egg and
larvae output. The examined aspects of seasonality, namely the nutritional status and
the climatic conditions, might not have affected the host’s susceptibility, exposure or
parasite viability in the way that seasonal variation in PSR, prevalences or egg output
was detectable. Additionally, the possibility cannot be excluded that both aspects
have opposite effects outweighing each other: the expected favourable climatic
conditions for parasite viability coincided with the positive effects of high food
abundance that can booster the host’s immune system.
Discussion
151
The findings of the necropsy of the female titi monkey provided deeper insights into
the parasites’ impact on the survival of wild hosts. The occurrence of ulcers, scar
tissue in the small intestine and the diffuse chronic enteritis associated with
P. elegans may have reduced the digestive function of the intestine and affected the
barrier function against intruding pathogens and toxins. Thus, these results suggest
that the infection with P. elegans had a massive and long-term impact on the host’s
resource utilisation and the defence mechanisms in the digestive tract.
The standardized and improved parasitological methods (faecal sampling regime,
concentration technique and microscopic examination) revealed highly satisfying
results, also compared to other studies on wild hosts. Based on consistent methods
and the critical use of metrics of disease risk the results are likely to precisely reflect
patterns of parasitism of the three host species. In order to cope with problems
arising in non-invasive surveys based on faecal sampling, parasite identification was
based on exact measurement of a representative number of eggs and statistic
analyses of parasite sizes combined with a comprehensive and detailed literature
review of possible parasite species. The identification of the acanthocephalan
species was possible due to the recovery of adult worms from a necropsied host.
Yet, for future studies it would be desirable to apply molecular techniques for parasite
identification to the species level.
The results of this study contributed to the understanding of host-parasite
interactions.
The
study
encompassed
a
wide
array
of
host-intrinsic
and
environmental factors that are assumed to shape the assemblage of parasite
communities. Since it focused on intestinal helminths of only few groups sympatric
primate species the conclusions have to be drawn cautiously. However, it sheds light
on the possible factors of parasite diversity and aids to put forward novel hypotheses.
152
Summary
6 SUMMARY
Britta Müller (2007)
Determinants of the diversity of intestinal parasite communities in sympatric
New World primates (Saguinus mystax, Saguinus fuscicollis, Callicebus
cupreus)
Parasites can exert an important impact on host population regulation in terms of
reducing fecundity and/or survival of the host individuals. They can even provoke
rapid declines of host populations or extinctions of host species. Thus, it is of basic
and applied importance to accurately assess the patterns of parasitism in wild hosts.
Using a comprehensive comparative approach, this is the first study that has
systematically explored the role of a diverse array of host-intrinsic traits and
environmental factors potentially affecting parasite diversity in sympatric wild
primates. Furthermore, this non-invasive, year-round study provided baseline data on
the intestinal parasite spectrum of three New World primate species (Saguinus
mystax, Saguinus fuscicollis and Callicebus cupreus).
Multiple faecal samples on non-consecutive days were collected over a 15-month
period from 45 individually recognized hosts of eight primate study groups at the
Estación Biológica Quebrada Blanco (EBQB) field site in Peru. More than 430 faecal
samples were processed by the formalin ethyl-acetate sedimentation technique and
examined microscopically for propagules of helminths and protozoa. Parasite species
richness (PSR), prevalence (proportion of infected hosts with a specific parasite) and
egg or larva output were determined as metrics of disease risk. Data on activity
patterns, ranging and group composition of the hosts was collected to explore the
importance of the following host-intrinsic factors on parasitism: host sex, strata use,
diet composition, nutritional status, home-range size, host density and group size. In
order to elucidate host-extrinsic environmental factors that may shape parasite
diversity, different habitat variables were measured, such as ground humidity, soil
type, habitat morphology, resource distribution for intermediate hosts and vegetation
Summary
153
density. Seasonal fruit availability was assessed as a surrogate measure for the
nutritional status, as this is assumed to influence the host’s defences against
pathogens.
The parasitological methods (faecal sampling regime, adapted concentration
technique and microscopic examination) revealed highly satisfying results,
particularly in comparison to other parasitological studies on wild hosts. Seven
different helminth taxa but no protozoa were detected. One acanthocephalan species
(Prosthenorchis elegans), two cestode species (probably Hymenolepis cebidarum
and unidentified cestode sp. #2), two Spirurida species (large spirurid: Gongylonema
sp. or Trichospirura leptostoma, and a small unidentified spirurid), “strongylids”
(Strongyloides sp. or Molineus sp.) and nematode larvae (Strongyloides, Filaroides
or Angiostrongylus sp.) were recovered from the three host species. All parasite taxa
of this study have a broad host spectrum and at least five out of seven parasites are
transmitted by intermediate hosts which are mainly insects. Two parasite taxa were
probably soil-transmitted parasites.
Both Saguinus species harboured all seven helminth taxa and had a completely
overlapping spectrum of intestinal helminths. C. cupreus harboured only three taxa
out of the seven taxa recovered from Saguinus (small spirurids, “strongylids” and
nematode larvae). All host species were infected with at least three (Saguinus) or two
parasite species (Callicebus). All three host species differed significantly in the
number of different parasite species (PSR), with S. fuscicollis showing the highest,
S. mystax intermediate and C. cupreus the lowest parasite diversity. This difference
was also reflected at the level of prevalences of specific parasites (P. elegans,
Hymenolepis sp. and large spirurids). Saguinus fuscicollis individuals also excreted
more propagules of “strongylids” and nematode larvae. Females of both Saguinus
species showed higher prevalences in most parasite taxa than males. This sex bias
was not observed in C. cupreus. Host-intrinsic factors, such as the proportion of
animal prey in diet or time spent on the ground were positively associated with PSR
and prevalence of two parasite taxa. Other host-intrinsic factors such as group size,
host density and home-range size did not seem to account for the heterogeneity in
parasite infection patterns.
154
Summary
Over the three home ranges of both Saguinus species, PSR and prevalences of most
indirectly transmitted parasite taxa varied considerably although the overall statistical
model revealed no significant influence of the host’s home range on PSR and
prevalences. The prevalences of P. elegans, large spirurids and cestode sp. #2 were
associated with the use of specific areas within the home ranges of the groups. The
higher the frequency of use of areas with very abundant leaf litter and dense
vegetation the higher the prevalences of large spirurids and cestode sp. #2. The time
animals ranged on clay soil was negatively correlated with large spirurids and
cestode sp. #2, and the use of areas of high deadwood abundance was negatively
correlated with prevalences of the latter. P. elegans showed an opposite trend with
respect to the use of the same habitat characteristics.
No seasonal pattern was detected either in PSR, parasite prevalences or in egg and
larvae output. Thus, in the present study the examined aspects of seasonality,
namely the nutritional status and the climatic conditions, did not seem to have a
measurable impact on the host’s susceptibility and/or parasite viability.
By means of standardized and improved methods, the critical use of metrics of
disease risk and meticulous parasite identification, the results of this study are likely
to accurately reflect patterns of parasitism. In order to characterize the role of hostintrinsic and host-extrinsic factors it is of major importance to take parasite ecology
and in particular parasitic life cycle into account. The results of this study on three
sympatric New World primate species suggest that host-intrinsic traits like sex, diet
and strata use, as well as environmental factors (e.g. vegetation density, soil type,
leaf litter and deadwood abundance) can shape the composition of intestinal parasite
communities.
Zusammenfassung
155
7 ZUSAMMENFASSUNG (GERMAN SUMMARY)
Britta Müller (2007)
Determinanten der Diversität intestinaler Parasitengemeinschaften sympatrischer
Neuweltaffenspezies
(Saguinus
mystax,
Saguinus
fuscicollis,
Callicebus cupreus).
Parasiten stellen wichtige ökologische und evolutionäre Faktoren dar. Sie können regulierend in die Entwicklung der Populationsdichte ihrer Wirte eingreifen, indem sie
die Reproduktions- und/oder die Überlebensrate reduzieren. Sie können sogar zu
dramatischen Einbrüchen der Wirtspopulation oder zum Aussterben einer Wirtsspezies führen. Daraus ergibt sich die ebenso zentrale wie grundlegende Bedeutung,
die auftretenden Parasitenbefallsmuster und Wirt-Parasit-Interaktionen in Wildtierpopulationen genauer zu untersuchen. Der hier angewandte vergleichende Ansatz ist
der erste dieser Art, der systematisch und umfassend sowohl potenzielle
wirtsspezifische Aspekte als auch Umweltfaktoren bei Primaten untersucht, welche
bei der Zusammensetzung von intestinalen Parasitengemeinschaften eine Rolle
spielen können. Darüber hinaus lieferte diese nicht-invasive ganzjährige Studie
grundlegende
Informationen
zum
intestinalen
Parasitenspektrum
der
drei
untersuchten wild lebenden Neuweltaffenspezies (Saguinus mystax, Saguinus
fuscicollis und Callicebus cupreus).
Von insgesamt 45 Wirtstieren aus acht Gruppen wurden mehrmals Kotproben an
nicht aufeinander folgenden Tagen an der Feldstation „Estación Biológica Quebrada
Blanco“ (EBQB) in Peru gesammelt. Die Kotproben konnten den jeweiligen
Wirtstieren eindeutig individuell zugeordnet werden. Über 430 Kotproben wurden mit
dem Formalin-Ethylacetat-Sedimentations-Verfahren bearbeitet und mikroskopisch
auf Parasitenstadien von Helminthen und Protozoen untersucht. Als Messgrößen für
das Erkrankungsrisiko (disease risk) wurden Parasitenspeziesreichtum (Anzahl der
unterschiedlichen Parasitenarten pro Wirt, PSR), Prävalenz (Anteil der infizierten
Tiere
an
der
Gesamtzahl
der
untersuchten
Tiere,
bedeutet
hier
aller
Zusammenfassung
156
Gruppenmitglieder)
und
Parasiteneier-
beziehungsweise
-larvenausscheidung
herangezogen. Daten zum Verhalten der Wirtstiere, ihrer Gruppenzusammensetzung
(Gruppengröße,
Geschlechter-
und
Altersklassen-Verhältnis)
und
ihrer
Habitatnutzung wurden aufgenommen, um den Einfluss folgender wirtsspezifischer
Faktoren
zu
klären:
Geschlecht,
Aufenthaltshöhe
im
Wald,
Ernährungs-
zusammensetzung, Ernährungszustand, Streifgebietsgröße, Wirtsdichte sowie Gruppengröße. Um die Bedeutung von Umweltfaktoren auf Parasitenbefall eingehender
zu untersuchen, wurden verschiedene Habitatcharakteristika in den Streifgebieten
der drei Primatenarten erfasst. Untersucht wurden die Bodenfeuchte, der Bodentyp,
die Habitatmorphologie (Bodenneigung), die Verteilung der Ressourcen für mögliche
Zwischenwirte (insbesondere Laubspreudichte und Totholzabundanz) und die
Vegetationsdichte.
Da
im
Rahmen
dieser
nicht-invasiven
Studie
der
Ernährungszustand der Wirtstiere nicht direkt festgestellt werden konnte, wurde die
saisonale Fruchtverfügbarkeit durch phänologische Untersuchung der spezifischen
Fruchtbäume der drei Primatenarten ermittelt und als indirektes Maß für den
Ernährungszustand der Wirte herangezogen.
Die parasitologischen Methoden (systematische Kotprobensammlung, modifizierte
Konzentrationsmethode und mikroskopische Untersuchung) erwiesen sich als sehr
effizient, besonders im Vergleich zu anderen parasitologischen Studien an Wildtieren. Es wurden sieben verschiedene Helminthentaxa (eine AcanthocephalaSpezies, zwei Cestoda- und vier Nematoda-Taxa), und keine Protozoen gefunden.
Die Taxa wurden wie folgt identifiziert: Prosthenorchis elegans (Acanthocephala),
Hymenolepis sp. (wahrscheinlich Hymenolepis cebidarum) und eine nicht näher
bestimmbare Zestoden sp. (eventuell Paratriotaenia sp., im Folgenden Zestoden sp.
#2 genannt), zwei Spiruridentaxa („großer Spirurida“: Gongylonema sp. oder
Trichospirura
leptostoma;
„kleiner
Spirurida“
[nicht
weiter
bestimmbar]),
“Strongyliden” (Strongyloides sp. oder Molineus sp.) und Nematodenlarven
(Strongyloides, Filaroides oder Angiostrongylus sp.). Alle Parasitentaxa zeichnen
sich durch ein breites Wirtsspektrum (polyxen) aus, wenigstens fünf von sieben
Parasiten besitzen einen indirekten Entwicklungszyklus mit mindestens einem
Wirtswechsel (heteroxen), wobei meist Insekten als Zwischenwirte dienen. Zwei
Zusammenfassung
157
Parasitentaxa sind so genannte „soil-transmitted parasites“, die sich zwar direkt
entwickeln, aber auf eine verlängerte Phase in der Außenwelt (üblicherweise auf
dem Boden) angewiesen sind.
Beide Saguinus-Spezies waren von sieben Parasitentaxa infiziert und überlappten
vollkommen in ihrem Parasitenspektrum. Callicebus cupreus war mit drei Parasitenarten infiziert, die mit denen der Saguinus-Arten identisch waren („kleine Spirurida“,
“Strongyliden” und Nematodenlarven). Alle Wirtstiere waren mindestens mit zwei (bei
C. cupreus) beziehungsweise drei Helminthenarten (bei Saguinus) befallen. Der PSR
unterschied sich signifikant zwischen den drei Wirtsarten: S. fuscicollis wies den
höchsten PSR auf, S. mystax einen mittleren und C. cupreus den geringsten PSR.
Diese Rangfolge ergab sich besonders aus den erhöhten Prävalenzen für
P. elegans, Hymenolepis sp. und „große Spirurida“ bei S. fuscicollis.
Die in zahlreichen Studien postulierte Hypothese der höheren Parasitenprävalenz bei
männlichen Säugetieren wurde in dieser Studie nicht bestätigt. Die polyandrisch
lebenden Saguinus-Weibchen zeigten im Durchschnitt eine höhere Prävalenz bei
Magen-Darm-Parasiten als ihre männlichen Artgenossen. Die erwartete Tendenz für
höhere Prävalenzen bei den Männchen wurde auch bei den monogamen C. cupreus
nicht bestätigt. Da das vorherrschende Paarungssystem bei Säugetieren die
Polygynie ist und sich daraus bestimmte Eigenschaften für die darin lebenden
Männchen ergeben, ist es plausibel, dass die generellen Muster nicht unkritisch auf
Säuger in monogamen oder polyandrischen Systemen übertragen werden dürfen.
Besonders
der
fehlende
(C. cupreus)
beziehungsweise
inverse
(Saguinus)
Geschlechtsdimorphismus und die geringere intrasexuelle Konkurrenz der Männchen
könnten die fehlende männchenspezifische Tendenz in der Parasitenprävalenz
erklären.
Als weitere wirtsspezifische Faktoren, die maßgeblich die Parasitendiversität
beeinflussen können, stellten sich die Nahrungszusammensetzung (Anteil an
tierischer Beute an der Gesamternährung) und die Aufenthaltshöhe im Wald
(Bodenaufenthaltszeit) heraus. PSR und Prävalenz der Zestoden sp. #2 und „großen
Spirurida“ korrelierten positiv mit dem Anteil an tierischer Beute und der
Zusammenfassung
158
Bodenaufenthaltszeit der Wirte. Mit zunehmendem Anteil tierischer Beute kann die
Aufnahme von potenziellen Zwischenwirten in der Nahrung und daraus resultierend
das Infektionsrisiko ansteigen. Gleiches gilt für verlängerte Bodenaufenthaltszeit,
während derer Kontakt zu den dort häufiger akkumulierten Parasitenstadien möglich
ist. Hierbei darf aber nicht unbeachtet bleiben, dass dieser grundlegende
Erklärungsansatz für indirekt übertragene Parasiten weniger plausibel ist, da hier die
Aufnahme von Zwischenwirten zur Infektion führt. Andere wirtsspezifische Faktoren,
wie Streifgebietsgröße, Gruppengröße und Wirtsdichte zeigten keinen signifikanten
Zusammenhang mit PSR und Parasitenprävalenz. Dies dürfte gleichfalls mit dem
hohen Anteil an indirekt übertragenen Parasitenspezies zusammenhängen, die
unabhängiger von Kontaktraten der Wirtstiere innerhalb einer Gruppe sind.
PSR und Parasitenprävalenz variierten erheblich zwischen den drei Streifgebieten
(West, Ost, Nord) der Saguinus-Arten, obwohl sich diese Divergenzen nicht in den
Ergebnissen des statistischen Modells widerspiegelten. Insbesondere die Prävalenzen von „großen Spirurida“ und Zestoden sp. #2 korrelierten signifikant positiv
mit der Nutzung von Streifgebietsanteilen, wo hohe Laubspreudichte (über 10 cm)
und erhöhte Vegetationsdichte (dichtes Unterholz und Baumdichte über 1200 Bäume
pro ha) vorherrschte. Diese Ergebnisse entsprechen den Vorhersagen der
Hypothesen,
da
für
höhere
Vegetationsdichte
günstigere
Bedingungen
für
Parasitenstadien und für höhere Laubspreu mehr Ressourcen für potenzielle
Zwischenwirte erwartet wurden. Die Prävalenzen von „großen Spirurida“ und
Zestoden sp. #2 korrelierten signifikant negativ mit der Zeit, die sich die Wirte auf
Tonböden aufhielten. Dieser Zusammenhang wurde auch in anderen Studien
gefunden. Besondere Aspekte der Parasitenökologie, wie zum Beispiel die Mobilität
der
Parasitenstadien
in
verschiedenen
Substraten
sowie
biochemische
Eigenschaften des Bodens dürften hierbei eine Rolle spielen. Die Prävalenz der
Zestoden sp. #2 korreliert negativ mit der Zeit, welche die Wirte in Arealen mit hoher
Totholzabundanz verbrachten. Dieses unerwartete Ergebnis könnte auf andere, in
dieser Studie nicht erfasster Variablen – wie zum Beispiel Degradierungszustand
oder Rindenanteil des Totholzes - zurückzuführen sein. Die Prävalenz von
P. elegans zeigte ein entgegengesetztes Muster in Bezug auf die oben genannten
Zusammenfassung
159
Habitatcharakteristika. Dies verdeutlicht, dass Erkenntnisse, die durch experimentelle
Studien über Zwischenwirte gewonnen wurden, nicht ohne weiteres auf komplexe
Ökosysteme übertragen werden können. Da die Nutzungsfrequenz der einzelnen
Habitatcharakteristika stark korreliert, ist die Aussage zum Einfluss einzelner
Variablen schwierig. Daher kann diese explorative Studie vor allem Hypothesen
generierend wirken und Faktoren identifizieren, die in zukünftigen ökologischparasitologischen Studien Berücksichtigung finden sollten.
Ein saisonales Muster des PSR, der Prävalenzen und Parasitenstadienausscheidung, wie es sich aus günstigeren Überlebensbedingungen für Parasitenstadien in
der Regenzeit ergeben könnte, wurde nicht beobachtet. Ebenso wenig scheint sich
der verschlechterte Ernährungszustand der Wirte in der Trockenzeit und die damit
eventuell
verbundene
reduzierte
Parasitenabwehr
auf
den
Parasitenbefall
auszuwirken. Vermutlich haben die saisonalen Einflüsse von Ernährungsstatus und
klimatischen Bedingungen eine geringe Wirkung auf die Wirtsempfänglichkeit beziehungsweise auf das Expositionsrisiko in dem untersuchten Wirts-Parasiten-System,
sodass sich Veränderungen kaum an den gewählten Variablen messen ließen. Es ist
außerdem denkbar, dass sich die entgegengesetzten Effekte aufheben (besserer
Abwehrstatus zu Zeiten der größeren Überlebenschancen der Parasiten).
Durch die konsequente Anwendung standardisierter und für diese Studie adaptierter
parasitologischer Methoden und aufgrund des kritischen Gebrauchs der epidemiologischen Maßzahlen und Messgrößen des „disease risk“, konnte diese Studie einen
Beitrag dazu leisten, auftretende Muster von Parasitismus bei drei sympatrischen
Neuweltprimatenarten zu identifizieren. Generell dürfen Aspekte der Parasitenökologie, insbesondere der Entwicklungszyklus und die möglichen Zwischenwirte,
nicht unberücksichtigt bleiben, wenn die Bedeutung der wirts- und umweltspezifischen Faktoren auf Parasitendiversität ermittelt werden soll. Die Ergebnisse dieser
vergleichenden parasitologischen Studie liefern Hinweise darauf, dass gleichermaßen wirtsspezifische (Wirtsgeschlecht, Nahrungszusammensetzung, Aufenthaltshöhe), wie auch habitatspezifische Faktoren (Laubspreu-, Vegetationsdichte, Bodentyp, Totholzabundanz) Einfluss auf die Zusammensetzung von intestinalen Helminthengemeinschaften nehmen können.
160
Resumen
8 RESUMEN (SPANISH SUMMARY)
Britta Müller (2007)
Determinantes de la diversidad de comunidades de parásitos intestinales en
primates simpátricos neotropicales (Saguinus mystax, Saguinus fuscicollis,
Callicebus cupreus).
Los parásitos pueden tener un importante impacto sobre las poblaciones de
huéspedes en libertad al reducir la fecundidad y/o la supervivencia de éstos. Los
parásitos pueden incluso provocar la extinción completa de las especies afectadas.
Es por lo tanto esencial, a nivel teórico y aplicado, examinar con precisión los
patrones de parasitismo en huéspedes en libertad. Éste es el primer estudio que
evalúa sistemáticamente el papel de una serie de factores intrínsicos de los
huéspedes y ambientales que pueden afectar la diversidad de parásitos en primates
silvestres a través de un enfoque comprensivo y comparativo. Este estudio no
invasivo, efectuado durante un ciclo de un año, proporciona además informaciones
básicas sobre el espectro de parásitos intestinales de tres especies de primates
neotropicales (Saguinus mystax, Saguinus fuscicollis y Callicebus cupreus).
Se recogieron múltiples muestras fecales de 45 individuos en días no consecutivos
durante 15 meses en la Estación Biológica Quebrada Blanco (EBQB) en Perú. Se
analizaron más de 430 muestras por el método de sedimentación con formol y
acetato de etilo y luego se examinaron microscópicamente para identificar los
distintos estadios de helmintos y protozoos. Se tomaron medidas como la riqueza de
especies de parásitos (PSR), la prevalencia (número de animales infectados por un
cierto parásito comparado con el número total de animales examinados) y la
eliminación de huevos y larvas para evaluar el riesgo de enfermedad (disease risk).
Se recogieron datos de actividad, movimiento y composición de los grupos para
estudiar la influencia de los siguientes factores intrínsicos de los huéspedes: sexo de
los huéspedes, uso de estratos del bosque, composición de la dieta, estado
nutricional, tamaño del área domiciliar (home range), densidad de huéspedes y
Resumen
161
tamaño del grupo. Para explorar factores extrínsecos o ambientales que pueden
modificar la diversidad de parásitos, se midieron las siguientes variables del hábitat:
humedad y tipo de suelo, morfología del hábitat (inclinación del terreno), distribución
de los recursos para huéspedes intermedios (abundancia de hojarasca y de madera
muerta). La estado nutricional puede afectar a las defensas contra los patógenos, y
se midió indirectamente a través de la disponibilidad de frutas.
Los métodos parasitológicos (recogida sistemática de muestras fecales, técnica
modificada de sedimentación, examen microscópico) brindaron resultados muy
satisfactorios, especialmente en comparación con otros estudios parasitológicos de
fauna silvestre. Se identificaron siete taxones de helmintos: una especie de
acantocéfalo (Prosthenorchis elegans), dos especies de céstodos (una especie
indeterminada: Cestoda sp. y otra, probablemente Hymenolepis cebidarum), dos
especies de Spirurida (Gongylonema sp. o Trichospirura leptostoma; y una especie
indeterminada), “strongylids” (Strongyloides sp. o Molineus sp.) y larvas de
nematodos (Strongyloides, Filaroides o Angiostrongylus sp.). Todos los parásitos
encontrados tenían un espectro de huéspedes muy amplio y por lo menos cinco de
los siete son transmitidos por huéspedes intermedios, sobre todo insectos. Dos
taxones se transmiten a través del suelo (soil-transmitted).
Ambas especies de Saguinus hospedaron siete taxones de parásitos intestinales.
C. cupreus hospedó únicamente tres de las siete especies halladas en Saguinus.
Todas las especies huéspedes presentan distintas PSR. S. fuscicollis mostró la más
alta PSR, seguido por S. mystax y C. cupreus. Esta diferencia se mostró igualmente
en la prevalencia de P. elegans, Hymenolepis sp. y Cestoda sp..
Las hembras de Saguinus presentaron una prevalencia de parásitos en promedio
más alta que los machos conespecíficos. Factores como la proporción de presa
animal en la dieta y el tiempo pasado en el suelo correlacionan positivamente con la
PSR y la prevalencia de dos de los parásitos. En cuanto a los factores ambientales,
la frecuencia de uso de áreas con abundante hojarasca y vegetación densa influyó
positivamente la prevalencia de dos parásitos. Sin embargo, el uso de un hábitat de
suelo arcilloso y madera muerta abundante disminuyó la prevalencia de esos
162
Resumen
mismos parásitos. No se pudo detectar variabilidad estacional ni en la PSR, ni en la
prevalencia ni en la excreción de huevos o larvas. Por lo tanto, ni el cambio de la
disponibilidad de los frutos (que altera el estado físico y las defensas), ni el cambio
de las condiciones climáticas (que probablemente modifica la viabilidad de los
parásitos) parecen influir en las variables medidas de disease risk en este estudio.
Mediante el empleo de métodos mejorados y estandardizados, el uso de las
medidas del disease risk de forma crítica y la meticulosa identificación morfológica
de los parásitos, el presente estudio ayuda a elucidar los patrones de parasitismo en
los tres primates neotropicales estudiados. Para caracterizar el papel de los factores
ambientales e intrínsicos de los huéspedes es de gran importancia tener en cuenta
la ecología de los parásitos, en particular su ciclo de vida. Los resultados de este
estudio sobre los parásitos intestinales de tres especies de primates sugieren que
factores intrínsicos de los huéspedes como sexo, dieta y uso de los estratos del
bosque, junto con factores ambientales tales como la densidad de vegetación, tipo
de suelo, abundancia de hojarasca y madera muerta, pueden influir la composición
de las comunidades de parásitos.
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190
10 APPENDICES
APPENDIX A: List of intestinal helminths found in Saguinus and Callicebus species, including morphological
features of eggs and larvae, potential hosts, origin of hosts, pathological alterations
1. TREMATODA
Parasite
species
A. Diplostomidae
Neodiplostomum
tamarini
Neodiplostomum
sp.
Size in
µm
Morpho Host species
-logy
Host
Intermediate
origin hosts
S. nigricollis,
S. fuscicollis,
Saguinus sp.
Saguinus sp.
not known, molluscs,
insects, amphibians,
reptiles or fish
Pathogenicity
Comments
unknown
References
9; 21; 35; 54
7; 38; 54
B. Echinostomatidae
Echinostoma
aphylactum
37; 64; 65
S. geoffroyi,
Saguinus sp.
C. Dicrocoeliidae
Athesmia foxi
not known, molluscs,
insects, amphibians,
reptiles or fish
nonpathogenic/
obstruction
and inflammation of
bile ducts
syn. A.
heterolecithodes, A.
heterolecithoides
7; 9; 18; 20;
21; 26; 37;
47; 53; 54;
59; 63-65;
68
Appendix
c, w
17-21x27- ovoid,
C. albifrons,
34
thick shell, C. apella,
operculum C. capucinus,
S. oedipus,
S. sciureus,
S. fuscicollis,
S. nigricollis,
S. geoffroyi,
Cebus sp., Saimiri
sp., Saguinus sp.,
Callicebus sp.
Athesmia
heterolecithodes
Athesmia sp.
Platynosomum
amazonensis
Platynosomum
marmoseti
Platynosomum
sp.
Zoonorchis
goliath
Size in
µm
Morpho Host species
-logy
17-21x27- ovoid,
A. trivirgatus,
34
thick shell, C. capucinus,
operculum S. geoffroyi,
S. mystax,
S. labiatusf
C. caligatus,
C. apella,
Saguinus sp.,
Callicebus sp.
20-35x34- ovoid,
C. goeldii,
thick shell, S. nigricollis,
50 (for
P. concin- operculum S. mystax,
num)
S. fuscicollis,
C. jaccus,
Saguinus sp.
20-35x34- ovoid,
S. fuscicollis,
thick shell, S. nigricollis,
50 (for
P. concin- operculum Saguinus sp.
num)
Saguinus sp.
22-26x34- operculu41
lated
A. trivirgatus,
S. geoffroyi, Aotus
sp., Saguinus sp.
40
A. trivirgatus,
S. fuscicollis,
S. mystax, Aotus
sp., Saimiri sp.,
Cebus sp.,
Saguinus sp.
S. fuscicollis,
Saguinus sp.
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
c
nonpathogenic
syn. A.
heterolecithoides, A. foxi
20; 21; 26;
37; 44; 54;
59; 63-65
not known, molluscs,
insects, amphibians,
reptiles or fish
Appendix
Parasite
species
7; 18; 37; 38
w, i
not known, molluscs,
insects, amphibians,
reptiles or fish
unknown
syn.
Conspicuum
conspicuum
7; 9; 21; 26;
35-37; 53;
54; 59; 63;
65
i
not known, molluscs,
insects, amphibians,
reptiles or fish
unknown
syn.
Conspicuum
conspicuum
9; 21; 26;
35-37; 59
7; 18; 54
26; 35; 37;
64; 65
D. Lecitodendriidae
Phaneropsolus
orbicularis
Phaneropsolus
sp.
w
not known, molluscs,
insects, amphibians,
reptiles or fish
I
not known, molluscs,
insects, amphibians,
reptiles or fish
unknown
7; 9; 18; 21;
26; 37; 53;
54; 59; 64;
65
9; 18; 38; 54
191
23-29x
12-15 (for
P. bonnei)
operculated
192
2. CESTODA
Parasite
species
Size in
µm
Morpho Host species
-logy
Host
Intermediate
origin hosts
Pathogenicity
22-25
oval
C. cupreus
c
spindle
shape,
packed in
capsules,
each of 4
eggs (for
R. demerariensis)
C. cupreus,
Alouatta sp.,
Callithrix sp.,
Callicebus sp.,
Saimiri sp.
i
S. nigricollis,
C personatus nigrifrons,
S. sciureus,
Callithrix sp.,
Saguinus sp.,
Callicebus sp.,
Cebus sp.,
Alouatta sp.,
Ateles sp.
C. moloch, Cebus
sp., Alouatta sp.,
Callicebus sp.
w, c
insects, coleoptera
enteritis
w
oribatid mites,
experimentally:
Scholoribates
laevigatus, Galumma
spp. (B. studeri)
unknown
Comments
References
A. Davaineidae
Railletina
trinitatae
Raillietina sp.
4; 16
unknown, beetles,
flies, ants, snails
(Raillietina sp.)
not known, beetles,
flies, ants, snails
(Raillietina sp.)
Raillietina
demerariensis in
A. caraya,
A. seniculus,
A. pigra
4; 13; 17;
21; 25; 35;
38; 47-49;
54; 64; 65
syn. Artiotaenia
megastoma,
Matheovataenia,
Oochoristica
11; 17; 18;
21; 26; 27;
35; 38; 48;
52; 65
B. Anoplocephalidae
Atriotaenia
megastoma
egg:
46x50,
oncosphere
18-20 (for
B. studeri)
thin shell,
irregular
ovoid
contour,
inner shell
with bicornuate
protrusion
4; 17; 21;
35; 38; 48;
54; 59; 65;
70
Appendix
Bertiella
mucronata
egg: 2541x33-45,
oncosphere:
24-33x3041
Size in
µm
Morpho Host species
-logy
egg: 2541x33-45,
oncoMathevotaenia
sphere:
sp.
24-33x3041
46-56,
with
mucus 8696, oncosphere
Paratriotaenia sp.
37-43,
hooks 18
(for
P. oedipomidatis)
Host
Intermediate
origin hosts
Pathogenicity
References
syn.
11; 22; 35;
Matheovataenia 38; 47; 48;
52; 65
coleoptera,
lepidoptera, Tribolium
sp.
Saguinus sp.,
Saimiri sp.,
Callicebus sp.
Comments
4; 9; 21; 35;
38; 48; 53;
62; 65
S. fuscicollis,
S. fuscicollis
illigeri,
S. leucopus,
S. oedipus,
C. goeldii,
Saguinus sp.,
Callithrix sp.
w, i, l
insects
unknown
S. nigricollis,
C. nigrifrons,
Callicebus sp.,
Saguinus sp.,
Callithrix sp.
S. mystax, NWP
c
unknown
unknown
2; 11; 17;
18; 21; 35;
38; 52; 65
c
beetles (Tenebrio
molitor, T. obscurus),
fleas (Xenopsylla
cheopsis, Nosopsyllus
fasciatus,
Ctenocephalides
canis), mealmoth
(Pyralis farinalis),
arthropods
rarely
enteritis and
abscessation of
lymph
nodes
4; 21; 26;
38; 44; 48;
59
P. oedipomidatus in
Callithrix sp.
Appendix
Parasite
species
C. Hymenolepididiae
Hymenolepis
cebidarum
Hymenolepis
diminuta
193
egg 68,
oncosphere
30x27,
hooks 16
52-81x62- sphaerical
88
thick
membrane,
straw
coloured,
three
pairs of
hooks in
the oncosphere
Size in
µm
Morpho Host species
-logy
Hymenolepis
nana
30-35x44- greyish,
Saimiri sp., NWP
62
oval, 2
membraneous
shells, the
inner one
with 2
poles, 3
pairs of
hooks
Host
Intermediate
origin hosts
flour beetles, fleas or
no intermediate host
Pathogenicity
Comments
References
194
Parasite
species
4; 17; 21;
35; 38; 48;
59; 65
rarely
enteritis and
abscessation of
lymph
nodes
3. NEMATODA
A. Capillariidae
Size in
µm
Morpho Host species
-logy
Capillaria
hepatica
29-37x48- barrel
62
shaped, 2
polar
"plugs",
striated
shell
Cebus sp., Saimiri
sp., Ateles sp.,
Cebidae
22x54
Saimiri sp.,
Alouatta sp.,
Lagothrix sp.,
Cebidae
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
no intermediate host
hepatitis,
nodules in
liver,
cirrhosis
syn. Hepaticola 5; 21; 26;
51; 59; 65;
hepatica,
68
spurious
passage of eggs
if animals ingest
infected prey
no intermediate host
typhlitis,
colitis,
secondary
infections
Trichuris
trichuria for
humans and
some NWP sp.
B Trichuridae
Trichuris sp.
21; 35; 51;
65; 68
C. Gnathostomatidae
Gnathostoma sp.
Saguinus sp.
54
Leontopithecus
sp., Saguinus sp.
18; 54
Appendix
Gnathostoma
weinberg
Size in
µm
Morpho Host species
-logy
Enterobius
vermicularis
Trypanoxyuris
callicebi
Trypanoxyuris
callithricis
Trypanoxyuris
croizati
Trypanoxyuris
minutus
21-24x45- thin52
shelled,
symmetrical
45x90
thinshelled,
symmetrical
21x36-42 symmetrical
21x40
relatively
thickshelled,
symmetrical
75x35
Trypanoxyuris
tamarini
Trypanoxyuris
spp.
20-32x4660
thinshelled,
symmetrical
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
Callithrix sp.,
Callitrichidae
l
no intermediate host
anal
pruritus,
irritation
syn. BuckleyEnterobius
21; 65
C. moloch,
w
no intermediate host
S. geoffroyi,
C jacchus
w, l, c
no intermediate host
C. torquatus
w
no intermediate host
S. oedipus,
A. pigra,
A. seniculus,
Cebus sp., Ateles
sp., Alouatta sp.,
Callithrix sp.
S. nigricollis,
Saguinus sp.
w
no intermediate host
unknown
syn.
Trypanoxyuris
oedipi,
Enterobius
minutus
14; 21; 29;
32; 43; 51;
64; 65; 71
w, i
no intermediate host
unknown
syn.
Paraoxyuronema tamarini
9; 13; 21;
28; 32; 33;
51; 54; 65
w
no intermediate host
C. moloch
Appendix
D. Oxyuridae
30; 31
syn.
Hapaloxyuris
callithricis
28; 33; 64;
65
31
18; 26; 28;
29; 32; 33;
54; 55; 70
195
Morpho Host species
-logy
30-40x40- oval eggs
60
with
smooth
thick shell,
embryoPhysaloptera spp.
nated
(P.caucasi
ca)
Host
Intermediate
origin hosts
Comments
References
insects, beetles,
gastritis,
katydids, cockroaches oesopha(Blatella sp.)
gitis,
ulcerative
enteritis
syn. Abbreviata
sp.,
Physaloptera
dilatata in NWP
4; 18; 21;
35; 38; 64;
65; 68
l, z
cockroaches,
arthropods
enteritis
syn. Rictularia
21; 65; 71
z
cockroaches
enteritis
syn. Rictularia
nycticebi
26; 42; 45;
65; 68
S. geoffroyi,
Cebus sp.,
Lagothrix sp.,
Callithrix sp.,
Callicebus sp.,
Saguinus sp.,
Alouatta sp.,
Pithecia sp.,
Callitrichidae,
Cebidae, NWP
Pathogenicity
196
E. Physalopte- Size in
ridae
µm
F. Rictulariidae
Pterygodermatites alphi
Pterygodermatites nycticebi
26-36x39- thick45
shelled,
embryonated
Cebus sp.,
Saguinus sp.,
Callithrix sp.
L. rosalia,
Saguinus sp.,
Callitrichidae
Callicebus sp.
Rictularia sp.
38; 65
G. Rhabdochonidae
Trichospirura
leptostoma
23-30x50- thick55
shelled,
containing
embryo
with tooth
C. moloch,
S. fuscicollis,
S. oedipus,
C. jacchus,
Callimico,
Saguinus sp.,
Aotus sp., Saimiri
sp., Callitrichidae,
Cebidae
i, w
roaches
pancreatitis,
cholangitis,
fibrosis,
occasionally
obstructive
jaundice
9; 10; 21;
26; 35; 38;
50-52; 61;
65; 68
Appendix
Size in
µm
Morpho Host species
-logy
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
nonpathogenic
Gongylonema
capucini in
C. capucinus,
Gongylonema
saimirisi in
Saimiri sp.,
Cebus sp.,
Callicebus sp.,
Gongylonema
pulchrum in
C. capucinus,
Ateles sp.
4; 21; 23;
26; 35; 40;
41; 51; 65
23-26x40- ovoid,
50
thick,
transparent shell,
larvated
C. capucinus,
Saimiri sp. Cebus
sp, Ateles sp.,
Callicebus sp.
l, z
cockroaches, beetles
40x55
C. jacchus,
S. fuscicollis,
C. capucinus
S. mystax
c, l
cockroach
non(Leucophaea madera) pathogenic
Gongylonema
spp.
Appendix
H. Gongylonematidae
I. Spiruridae
Protospirura
muricola
larvated
Spirura delicata
58x33
Spirura
guianensis
Spirura tamarini
Spirura sp.
w
w, c, l
S. nigricollis,
S. fuscicollis,
S. geoffroyi,
Saimiri sp.,
Saguinus sp.
c, i, l
S. nigricollis,
S. mystax, Saimiri
sp.
66
arthropods, locusts
(experimentally
Locusta migratoria)
oesophagitis, death
syn. Spirura
tamarini,
Protospirura
guianensis
3; 9; 21; 49;
51; 53; 54;
56; 57; 64;
65
syn. Spirura
guianensis,
Protospirura
guianensis
3; 8; 49; 64;
65
9; 54
197
30-40x54- subglobu60
lar egg
with thick,
hyalin,
smooth
shell,
embryonated
30-40x54- thickshelled
60 (for
egg with
Spirura
larva
tamarini)
6; 53; 54;
64; 65
Ascaris sp.
Size in
µm
Morpho Host species
-logy
35-45x45rounded,
70
thick shell,
brown
mammillated layer
S. geoffroyi ,
A trivirgatus,
C. capucinus,
A. fusciceps
53
C. jacchus,
C. pygmaea,
S. mystax,
S. leucopus,
S. oedipus,
S. geoffroyi,
C. aurita,
C. nigrifrons,
Saguinus sp.,
Callithrix sp.,
Callicebus sp.
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
no intermediate host
nonpathogenic,
in large
numbers
occlusion of
bowl
4; 21; 51;
unfertilized
eggs: elongated 54; 59; 64;
and larger than 65; 68
fertilized eggs,
shell is thinner
cockroaches
unknown
syn. Subulura
jacchi
no intermediate host
enterocolitis, dermatitis, pulmonary haemorrhages,
bronchopneumonia
198
J. Ascarididae
K. Subuluridae
Primasubulura
jacchi
w, c
9; 11; 12;
18; 21; 26;
27; 38; 44;
52-54; 6365
L. Strongyloididae
Strongyloides
cebus
eggs: 2035x40-70,
larva1:
150-190
ovoid,
thinshelled,
embryonated or
with larva
S. fuscicollis,
Cebus sp.,
Lagothrix sp.,
Ateles sp., Saimiri
sp., Saguinus sp.,
Callitrichidae
51; 59; 68
M. Ancylostomatidae
L. lagothricha,
Saimiri sp.,
Saguinus sp.
c, p
no intermediate host
enteritis with
haemorrhages
4; 38; 54;
63-65
Appendix
Ancylostoma sp.
4; 8; 18; 21;
35; 38; 47;
51; 53; 54;
59; 65; 68
Size in
µm
Morpho Host species
-logy
Host
Intermediate
origin hosts
no intermediate host
Ateles sp.,
C. capucinus,
Cebidae
Necator
americanus
C. calvus,
C. capucinus
Necator sp.
c, p
no intermediate host
Pathogenicity
Comments
4; 21; 51;
59; 64; 65;
68
enteritis with
haemorrhages,
anaemia
enteritis with
haemorrhages,
anaemia
63-65
1; 59
N. Metastrongylidae
Angiostrongylus
costaricensis
Filariopsis arator
Filariopsis asper
Filariopsis
cebuellae
Filaroides
barretoi
References
Appendix
Parasite
species
larva1: 14- larva1:
15x260notch
290
close to
the tip,
slender
esophagus, nerve
ring
long,
larva1:
tapered
10x340tail
350
(80µm)
S. mystax,
Callitrichidae
c, i
C. apella,
C. capucinus,
C. albifrons,
Alouatta sp.,
Cebus sp.
A. seniculus,
Alouatta sp.,
Cebus sp.
C. pygmaea
S. mystax,
S. labiatus,
Callithrix sp,
Saimiri sp.,
Saguinus sp.
slugs (Vaginulus
plebius), fresh water
snails, molluscs
granulomatous appendicitis, intestinal ulcera,
peritonitis,
arteritis,
thrombosis
unknown
unknown
4; 46; 54;
60; 65; 68
syn. Filaroides
arator,
Filaroides cebi
unknown
w
unknown
18; 21; 35;
39; 65; 67
18; 35; 65;
67
67
18; 21; 26;
35; 44; 65;
67
199
nonpathogenic/
atelectasis,
pulmonary
haemorrhages
syn. Filaroides
cebuellae
syn.
Oslerus/Filariopsis barretoi
Size in
µm
Filaroides cebi
larva1: 911x250260
Morpho Host species
-logy
Filaroides
gordius
Host
Intermediate
origin hosts
unknown
C. apella,
C. macrocephalus, C. capucinus,
C. albifrons,
Cebus sp.
S. fuscicollis,
S. nigricollis,
S. sciureus,
Saimiri sp.
Comments
References
syn.
23; 65; 67
Filaroides/Filariopsis cebi
unknown
syn.
nonpathogenic/ Oslerus/Filariatelectasis, opsis gordius
pulmonary
haemorrhag
es
unknown
no intermediate host
unknown
unknown
S. fuscicollis,
Saimiri sp.,
Lagothrix sp.,
Callithrix sp.,
Alouatta sp.,
Cebus sp.,
Saguinus sp.,
Callitrichidae,
Cebidae
Filaroides sp.
Pathogenicity
200
Parasite
species
18; 21; 35;
65; 67
9; 21; 34;
38; 49; 54;
65; 68
O. Trichostrongylidae
31-41x6279
Longistriata
dubia
Longistriata sp.
w, c
w
S. mystax,
S. sciureus,
Cebus sp., Saimiri
sp.
no intermediate host
no intermediate host
syn.
Boreostrongylus
romerolagi n.
sp.
9; 18; 21;
24; 35; 51;
53; 54; 59;
65; 70
38; 54
nonpathogenic
18; 21; 26;
27; 35; 54;
59
Appendix
Molineus elegans
30-37x59- ellypsoid,
63
thin shell
slightly
tapered at
one end
S. sciureus,
S. nigricollis,
S. fuscicollis,
C. moloch,
Saguinus sp.,
Alouatta sp.,
Saimiri sp.
Saguinus sp.
Molineus midas
Molineus
torulosus
Molineus
vexillarius
Size in
µm
Morpho Host species
-logy
Host
Intermediate
origin hosts
30x50
morula
stage
c
S. midas
Cebus sp., Saimiri w,c
sp., Aotus sp.,
Saimiri sp.,
Cebidae, NWP
w, c
S. fuscicollis,
S. leucopus,
S. oedipus,
Saguinus sp.
20-29x4052
20-29x4052
Pathogenicity
Comments
References
19
no intermediate host
no intermediate host
Appendix
Parasite
species
18; 21; 26;
35; 51; 54;
59; 65; 68
ulcerative or
haemorrhagic
enteritis
nonpathogenic
9; 15; 18;
21; 35; 53;
54
4. ACANTHOCEPHALA
Parasite
Size in
species
µm
A. Oligacanthorhynchidae
Prosthenorchis
elegans
Morpho Host species
-logy
41-43x60- thick65
walled
eggs, fine
reticular
sculpturing in
outer
shell,
raphe of
middle
shell
Host
Intermediate
origin hosts
cockroaches (Blattella
germanica, Blabera
fusca, Rhyparobia
madera), beetles
(Lasioderma
serricorne, Stegobium
paniceum), insects
granulomatous,
ulcerative
enteritis,
occasionally
mechanical
blockage of
the intestine
or perforation,
peritonitis
Comments
References
9; 16; 17;
21; 26; 27;
35; 38; 44;
47; 49; 53;
54; 58; 59;
63-65; 6870
201
w, c
S. nigricollis,
S. oedipus,
S. fuscicollis,
S. mystax,
S. geoffroyi,
C. pygmaea,
S. boliviensis,
S. sciureus,
C. cupreus,
Cebuella sp.,
Ateles sp., Saimiri
sp, Alouatta sp.,
Aotus sp.,
Lagothrix sp.,
Callitrichidae
Pathogenicity
Size in
µm
Prosthenorchis
spirula
49-53x78- Outer
81
shell
lightly
sculptured, no
raphe
Prosthenorchis
sp.
Morpho Host species
-logy
Host
Intermediate
origin hosts
Pathogenicity
Comments
References
S. oedipus,
C. jacchus
cockroaches
syn
Prosthenorchis
sigmoides
9; 18; 21;
53; 54; 58;
64; 65
S. fuscicollis,
S. mystax,
S. oedipus,
C. jacchus
S. geoffroyi
cockroaches
P. lenti
53; 54; 64
202
Parasite
species
Legend:
A.-O.=families of the cited parasite species, taxonomy follows SCHNIEDER and TENTER (2006) if not otherwise noted in the references.
grey shaded cells= parasite taxa recovered in this study
Host species:
Alouatta: A. carata, A. pigra, A. seniculus
Aotus: A. trivirgatus
Ateles: A. fusciceps
Cacajao: C. calvus
Callicebus: C. cupreus, C. moloch, C personatus nigrifrons, C. caligatus, C. nigrifrons, C. torquatus
Callimico: C. goeldii
Callithrix: C. jacchus, C. aurita
Cebuella: C. pygmaea
Cebus: C. albifrons, C. apella, C. capucinus, C. macrocephalus
Lagothrix: L. lagothricha
Leontopithecus: L. rosalia
Saguinus: S. nigricollis, S. fuscicollis, S. mystax, S. oedipus, S. geoffroyi, S. labiatus, S. fuscicollis illigeri, S. leucopus, S. midas
Saimiri: S. sciureus, S. boliviensis
NWP: New World primates
Appendix
Host origin: w=wild, c=captured wild animals, i=imported, l=laboratory, p=pet, z=zoo animal
Appendix
203
REFERENCES (LIST OF HELMINTH PARASITES OF STUDY SPECIES)
1. ANDERSON (2000); 2. BAER (1927); 3. BLANCHARD and EBERHARD (1986);
4. BRACK (1987); 5. BRACK et al. (1994); 6. CAMPOS and VARGAS-VARGAS
(1978); 7. COSGROVE (1966); 8. COSGROVE et al. (1963); 9. COSGROVE et al.
(1968); 10. COSGROVE et al. (1970a); 11. DE MELO et al. (1997); 12. DE
RESENDE et al. (1994); 13. DEINHARDT et al. (1967); 14. DIAZ-UNGRIA (1964);
15. DUNN (1961); 16. DUNN (1962); 17. DUNN (1963); 18. DUNN (1968);
19. DURETTE-DESSET and CORVIONE (1998); 20. FAUST (1967); 21. FLYNN
(1973); 22. GALLATI (1959); 23. GEBAUER (1933); 24. GIBBONS and KUMAR
(1980); 25. GILBERT (1994); 26. GOZALO (2003); 27. HORNA and TANTALEÁN
(1990); 28. HUGOT (1984); 29. HUGOT (1985); 30. HUGOT and VAUCHER (1985);
31. HUGOT et al. (1994); 32. INGLIS and DUNN (1964); 33. INGLIS and
COSGROVE (1965); 34. KIM and WOLF (1980); 35. KING (1976); 36. KINGSTON
and COSGROVE (1967); 37. KUNTZ (1972); 38. KUNTZ and MYERS (1972);
39. LEE et al. (1996); 40. LUCKER (1933a); 41. LUCKER (1933b); 42. MATERN and
FIEGE (1989); 43. MENSCHEL and STROH (1963); 44. MICHAUD et al. (2003);
45. MONTALI et al. (1983); 46. MORERA (1973), 47. MOVTSCHAN (1974);
48. MYERS (1972); 49. NELSON et al. (1966); 50. ORIHEL and SEIBOLD (1971);
51. ORIHEL and SEIBOLD (1972); 52. PACHECO et al. (2003); 53. PORTER (1972);
54. POTKAY (1992); 55. PRIETO et al. (2002); 56. QUENTIN (1973); 57. RIBEIRO
AMATO et al. (1976); 58. SCHMIDT (1972); 59. SHADDUCK and PAKES (1978);
60. SLY et al. (1982); 61. SMITH and CHITWOOD (1967); 62. STUNKARD (1965);
63. TANTALEÁN et al. (1990); 64. THATCHER and PORTER (1968); 65. TOFT and
EBERHARD (1998); 66. VINCENTE et al. (1992); 67. WEBSTER (1978); 68. WOLFF
(1990); 69. WORMS (1967); 70. YAGI et al. (1988); 71. YAMASHITA (1963)
Appendix
204
APPENDIX B: Group composition over the study period
1. Group composition of S. fuscicollis
Individuals
per group
sex
2002
age*
2003
6
7
8
9
10
11
12
1
2
3
4
5
6
7
8
5
5
5
5
5
5
5
5
5
6
6
6
6
6
6
4
4
4
4
4
6
6
6
6
6
6
6
6
6
6
4
4
5
5
5
5
5
5
5
5
5
5
5
5
5
West:
Carlos
m
ad
Bryan
m
ad
Vidal
m
inf
Racna
f
ad
Arsénica
f
ad
Emilia
f
juv
total
East:
P. pela.
m
ad
Abrán
m
ad
Asrael
m
juv
Cuerno
m
inf
Gordita
f
ad
Brittita
f
inf
total
North:
Codito
m
ad
Tito
m
ad
Shaolín
m
inf
Kali
f
ad
Tablita
f
ad
total
Appendix
205
2. Group composition of S. mystax
Individuals
per group
sex
age*
2003
2002
6
7
8
9
10
11
12
1
2
3
4
5
6
7
8
3
3
3
3
3
3
1
1
1
1
4
4
4
4
4
8
8
8
8
6
6
7
7
6
6
6
6
6
6
6
5
5
5
5
6
6
6
6
6
6
6
6
7
6
6
West:
Quinto
m
ad
Victor
m
ad
Piwi
m
ad
Beto
m
ad
Diablo
m
juv
Petronila
f
ad
total
East:
Blanco
m
ad
Moli
m
ad
Adán
m
ad
Pit
m
ad
Prado
m
ad
Chavo
m
sub
Isma.
m
sub
Gaston
m
inf
Punta
f
ad
total
North:
Muno
m
ad
Joel
m
ad
Virilo
m
inf
Sipuca
f
ad
Mauricia
f
ad
Pitufina
f
juv
Jenni
f
inf
total
Appendix
206
3. Group composition of C. cupreus
Individuals
per group
sex
age*
2003
2002
6
7
8
9
10
11
12
1
2
3
4
5
6
7
8
3
3
4
4
4
4
4
4
4
4
4
3
3
3
3
3
Casa:
Pluto
m
ad
Cocoliso
m
juv
Cría
f
inf
Olivia
f
ad
total
Puerto:
Mocho
m
ad
Roki
m
juv
H. repro.
f
ad
Gloria
f
ad
total
3
Legend:
sex: f= female, m=male
*Age classes: ad = adult, sub = subadult, juv = juvenile, inf = infant; refers to the age when the
individual was first observed, for both Saguinus species defined by SOINI and SOINI (1990), for
Callicebus cupreus by MAYEAUX et al. (2002) and KINZEY (1981)
grey field: animal was present, hatched field: presence of adult was uncertain or infant was carried by
group members
APPENDIX C: Parasite morphology: comparison of length and width of parasite
stages
Results of Kruskal-Wallis test, Mann-Whitney U-test, respectively
Parasite taxa
Length
H
Prosthenorchis elegans
Hymenolepis sp.
Width
U
p
30
105.5
H
U
p
0.616
24
0.291
0.853
102.5
0.786
Cestode sp. #2
Small spirurida
13.391
Large spirurida
“Strongylids”
0.001
32.0
21.241
6
1.0
<0.001
0.042
10.5
30.279
0.021
<0.001
Appendix
207
Results of post hoc tests (Mann-Whitney U-test)
1. Small spirurids
Host species
Sf
Sf (N=77)
U=2639.0
p=0.714
Cc (N=71)
U=2039.5
p=0.021
Cc
U=2752.5
p=1.0
U=2318.0
p=0.321
U=2080.5
p=0.033
width
Sm (N=77)
Sm
U=1844.0
p=0.003
length
2. “Strongylids”
Host species
Sf
Sm (N=47)
U=1873.5
p=1.0
Cc (N=27)
U=589.5
p≤0.001
Cc
U=1786.5
p=0.57
U=182.5
p≤0.001
U=59.0
p≤0.001
U=389.5
p=0.015
length
width
Sf (N=88)
Sm
208
APPENDIX D: Correlations between independent variables
Spearman Rank Correlation, N=42
variable
HRS
HRS
GS
HD
AP
GT
clay
flat
drain
US
VD
LL
DW
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.19
0.00
0.01
0.71
0.43
0.12
0.21
0.00
0.16
0.00
0.20
0.00
0.16
0.97
0.00
0.54
0.00
0.32
0.01
0.00
0.00
0.32
0.67
0.00
0.00
0.00
0.00
0.39
0.00
0.00
0.01
0.00
0.00
0.00
0.01
0.00
0.00
0.29
0.00
0.00
0.09
0.00
0.00
0.02
0.00
0.14
0.00
.
0.00
0.58
0.00
0.00
0.97
0.05
0.14
0.37
0.00
0.10
0.70
.
HD
-0.47
0.13
AP
0.71
0.24
-0.62
GT
0.57
0.20
-0.10
0.68
clay
-0.84
-0.45
0.45
-0.81
-0.63
0.42
0.22
-0.16
0.79
0.71
-0.74
drain
-0.83
-0.51
0.38
-0.85
-0.61
0.76
-0.54
US
-0.21
0.20
0.73
-0.14
0.39
0.26
0.23
0.09
VD
0.85
0.43
-0.67
0.95
0.54
-0.86
0.64
-0.90
-0.31
LL
0.42
0.22
-0.16
0.79
0.71
-0.74
1.00
-0.54
0.23
0.64
DW
0.06
0.01
0.07
-0.40
-0.17
0.35
-0.78
0.01
-0.14
-0.26
-0.78
HRS
GS
HD
AP
GT
clay
flat
drain
US
VD
LL
p
flat
rs
GS
0.00
DW
Legend:
bold printed cells if rs <-0.7 or >0.7 and if p<0.05
Appendix
HRS=Home-range size, GS=mean group size, HD=host density, AP=% animal prey. GT=% ground time, clay=clay soil, flat=flat terrain, drain=poor
drainage, US=dense understorey, VD=high vegetation density, LL=leaf litter >10 cm, DW=high deadwood abundance
Appendix
209
APPENDIX E: PSR/prevalences and correlations with proportion of animal prey
and time spent on the ground
Spearman Rank Correlation, N=42, all host species
Parasite
% animal prey
% ground time
rs
p
rs
p
PSR
0.48
0.001
0.63
0.000
P. elegans
-0.18
0.243
-0.11
0.470
Hymenolepis sp.
0.30
0.052
0.51
0.001
Cestode sp. #2
0.51
0.001
0.36
0.019
Large spirurid
0.44
0.003
0.57
0.000
Nematode larvae
0.02
0.883
0.23
0.145
Spearman Rank Correlation, N=38, excluding Callicebus
Parasite
% animal prey
% ground time
rs
p
rs
p
PSR
0.32
0.047
0.56
0.000
P. elegans
-0.30
0.063
-0.17
0.299
Hymenolepis sp.
0.18
0.272
0.48
0.003
Cestode sp. #2
0.40
0.014
0.23
0.165
Large spirurid
0.42
0.009
0.57
0.000
Nematode larvae
0.07
0.672
0.27
0.105
Appendix
210
APPENDIX F: Activity budgets of all study species
1. S. fuscicollis
2. S. mystax
6%
7%
3%
4%
8%
36%
29%
9%
47%
51%
3. C. cupreus
8%
1%
38%
17%
36%
Activity
Foraging
Grooming
Ingestion
Locomotion
Resting
Appendix
211
APPENDIX G: PSR/prevalences and correlation with home-range size, mean
group size and host density
Spearman Rank Correlation, N=42, all host species
Parasite
Home-range size
Mean group size
Host density
rs
p
rs
p
rs
p
PSR
0.37
0.016
0.14
0.380
-0.17
0.291
P. elegans
-0.05
0.776
-0.07
0.650
-0.12
0.449
Hymenolepis sp.
0.18
0.260
-0.19
0.229
-0.29
0.063
Cestode sp. #2
0.39
0.011
0.48
0.001
0.01
0.950
Large spirurid
0.31
0.046
-0.01
0.951
-0.12
0.445
Nematode larvae
0.03
0.837
0.01
0.930
0.15
0.330
Spearman Rank Correlation, N=38, excluding Callicebus
Parasite
Home-range size
Mean group size
Host density
rs
p
rs
p
rs
p
PSR
0.18
0.291
-0.08
0.612
0.07
0.662
P. elegans
-0.14
0.397
-0.12
0.463
-0.05
0.750
Hymenolepis sp.
0.03
0.850
-0.38
0.019
-0.17
0.313
Cestode sp. #2
0.25
0.138
0.38
0.018
0.26
0.122
Large spirurid
0.26
0.110
-0.11
0.493
-0.04
0.811
Nematode larvae
0.08
0.625
0.02
0.922
0.14
0.414
Appendix
212
APPENDIX H: Habitat characteristics of the home ranges
Habitat
characteristic
Home range
categories
Casa
West
East
North
0-400
24.2
17.9
12.0
14.6
400-800
42.4
45.3
49.2
50.4
800-1200
24.2
23.9
20.8
22.0
1200-2000
6.1
10.3
16.9
8.9
>2000
3.0
2.6
1.1
4.1
low
42.4
30.6
16.0
13.5
intermediate
39.4
47.7
63.3
51.9
high
18.2
21.6
20.7
34.6
0-5
48.5
39.3
10.9
15.4
leaf litter height
5-10
33.3
39.3
34.4
36.6
(cm)
10-15
15.2
15.4
36.1
34.1
>15
3.0
6.0
16.9
11.4
clay
66.7
53.4
10.4
6.5
mixed
6.1
11.2
13.7
19.5
sand
18.2
29.3
71.4
67.5
swampy
9.1
6.0
4.4
6.5
poor
15.2
14.5
6.6
10.6
intermediate
3.0
3.4
3.8
4.9
good
81.8
82.1
89.6
84.6
flat
69.7
75.2
86.9
92.7
intermediate
21.2
12.8
8.7
5.7
steep
9.1
12.0
4.4
1.6
0
51.5
66.7
67.2
67.5
1
30.3
23.9
27.3
26.0
>1
18.2
9.4
5.5
6.5
vegetation density
(trees/ha)
understorey
density
soil type
drainage
ground inclination
deadwood
abundance
(tree units)
Appendix
213
APPENDIX I: Variation in egg and larvae output including all host species
Degrees of freedom (df), F-, p-values generated by GLMM
Effect per parasite
df
F
p
species
1
0.08
0.799
season
2
0.53
0.632
species * season
2
34.48
0.007
species
1
0.04
0.847
season
2
2.11
0.142
species * season
2
1.05
0.363
species
1
0.90
0.351
season
2
1.45
0.245
species * season
2
1.67
0.201
species
2
1.59
0.217
season
2
1.81
0.173
species * season
3
4.95
0.004
species
1
0.42
0.529
season
2
5.10
0.025
species * season
2
1.46
0.270
species
2
10.07
0.000
season
2
2.63
0.080
species * season
3
0.55
0.649
species
2
12.78
0.000
season
2
2.35
0.104
species * season
3
0.27
0.850
P. elegans
Hymenolepis sp.
Cestoda sp
small Spirurids
Large Spirurids
Nematode larvae
“Strongylids”
Danksagung
214
11 DANKSAGUNG/AGRADECIMIENTOS/ACKNOWLEDGEMENTS
Dass diese Arbeit soweit gediehen ist, verdanke ich der Unterstützung einer Vielzahl
von Menschen, denen ich an dieser Stelle ganz herzlich danken möchte.
Zunächst möchte ich mich bei Herrn Univ. Prof. Dr. F.-J. Kaup für seine freundliche
Betreuung und die gute Zusammenarbeit bedanken. Ein großes Dankeschön gebührt
Herrn PD Dr. Eckhard W. Heymann für die Grundsteinlegung dieser Arbeit, die
unermüdliche und uneingeschränkte Unterstützung während der Feldarbeit, die
konstruktiven Diskussionen und die allzeit mögliche Rücksprache bei der Auswertung und Zusammenstellung dieser Arbeit. Ich möchte ihm an dieser Stelle auch
danken, dass er mir diese großartige Möglichkeit gegeben hat, das für mich neue
Feld der Verhaltensökologie zu betreten, und mir dabei so viel Vertrauen entgegen
gebracht hat. Herrn Dr. Christian Epe möchte ich für seine tatkräftigen und auch
„postwendenden“ Anregungen bei der parasitologischen Methodenerarbeitung, sowie
bei Durchsicht der Manuskripte danken. Frau Dr. Kerstin Mätz-Rensing sei gedankt
für
ihre
Unterstützung
besonders
während
der
Laborphase,
wo
sie
den
reibungslosen Ablauf ermöglichte, für ihre pathologisch-histologischen Anregungen
und die sorgfältige Überarbeitung der vorläufigen Versionen. Mein Dank gilt ebenso
Frau Dr. Martina Zöller für die Korrekturen des pathologischen Teils. Sehr, sehr
herzlich möchte ich Herrn Prof. D. W. Büttner danken. Von seiner engagierten und
detaillierten Einweisung in einige Grundsätze der parasitologischen Methodologie
und der Helminthologie, der kritischen Auseinandersetzung mit meinem Thema und
seiner unbestechlichen Durchsicht des Manuskripts hat meine Arbeit an vielen
entscheidenden Stellen profitiert. Bei Herrn Prof. Dr. E. Tannich bedanke ich mich für
die Einladung ans Bernhard-Nocht-Institut, seine konstruktiven Anregungen und das
Interesse an meiner Arbeit.
Gracias a todos los que hicieron posible la realización de mi “gran obra” en el Perú.
En primer lugar quiero decirles gracias a los asistentes de campo Camilo Flores
Amasifuén, Ney y Jeisen Shahuano Tello y Jenni Pérez Yamacita. ¡Sin su gran
Danksagung
215
apoyo este trabajo no hubiera sido el mismo! Ebenso wäre diese Arbeit um einiges
ärmer, wenn die zahlreichen PraktikantInnen nicht so engagiert mitgewirkt hätten.
Deswegen ein besonderer Dank an Wolf-Christian Saul, Jenny „Pen“ Kröger,
Barbara Kremeyer und die anderen StudentInnen aus der bunten internationalen
Mischung. Quisiera darle un especial agradecimiento al director de la Estación
Experimental del Instituto Veterinario de Investigaciones Tropicales y de Altura
(IVITA) Dr. Enrique Montoya por su hospitalidad y su colaboración mientras
desarrollaba el trabajo en Perú. Muchisimas gracias también a los médicos
veterinarios de la estación, Dra. Nofre Sánchez Perrea y Dr. Hugo Gálvez Carillo, y
al biológo Dr. Carlos Ique por apoyarme en el trabajo de campo y de laboratorio. De
igual manera quiero agradecerles su ayuda a Arnulfo, Lester, Zoilita y los demás del
equipo IVITA que siempre me han dado un gran apoyo. Gracias muy especiales a
Nelly Tanchiva Flores y su familia por resolver cualquier problemita del trabajo y por
compartir muchos momentos de la vida “pishcota” que nunca voy a olvidar. A mi
familia limeña le agradezco de todo corazón por siempre estar presente.
In
der
methodologischen
Selbstfindungsphase
erfuhr
ich
besonders
viel
Unterstützung von den technischen AssistentInnen der Sektion Parasitologie des
Bernhard-Nocht-Institutes,
von
Frau
Scholz
vom
Institut
für
Medizinische
Mikrobiologie der Universitätskliniken Göttingen und Frau Rudloff aus der
Parasitologischen Abteilung des Tierparks Berlin Friedrichsfelde. Besonders gedankt
sei auch Frau Hafiza Zuri, Elke Lischka und Herrn Wolfgang Henkel der Abteilung
Infektionspathologie des Deutschen Primatenzentrums, die mir bei allen möglichen
und fast unmöglichen Dingen im Labor geholfen haben. Herausstellen möchte ich
auch die großartige, Theorie- und Praxis-bezogene Hilfe von Frau Dr. Christina
Schlumbohm.
Den Mitgliedern der Abteilung Verhaltensökologie & Soziobiologie des DPZ
(Ehemalige und Assoziierte eingeschlossen) sei ebenfalls ausdrücklich gedankt! Die
zahlreichen Seminare mit kritischen Diskussionen und stimulierenden Denkanstößen
haben mein wissenschaftliches Vorankommen entscheidend geprägt. Namentlich
möchte ich mich bei Prof. Dr. Peter M. Kappeler für die feinsinnigen Kommentare, die
kritische Auseinandersetzung mit meinem Projekt und die wissenschaftliche
Danksagung
216
Förderung in Form von Kongress- und Kurs- Teilnahmen bedanken. Ein herzliches
Dankeschön gilt besonders Dagmar Lorch und Markus Port für die „akkurate“ und
überaus produktive Überarbeitung meiner Entwürfe und den Beistand in allen Hoch-,
Tief-, Schräg- und Querlagen, aber auch Dr. Manfred Eberle, Dr. Antje Engelhardt,
Dr. Dietmar P. Zinner, Dr. Daniel Stahl, Dr. Yann Clough für diverse, unverzichtbare
Hilfestellungen. Ein Riesendankeschön geht an Dr. Maren Huck und Dr. Petra
Löttker, die im wahrsten Sinne des Wortes vom Mehrzellstadium bis zur Geburt mit
logistischer, fachlicher und persönlicher Unterstützung Patinnen standen und so
manches Mal die „shalupa“ aus dem Schlamm gezogen haben...
Die Parasitendiversität lebte durch die Diversität der an ihrer Identifikation beteiligten
Personen. Bei der Literaturrecherche und Parasitenbestimmung waren mir Dr. M.
Brack, Dr. A. Gozalo, Prof. Dr. A. L. De Melo, Dr. M. Tantaleán Vidaurre und Dr. W.
Tscherner eine unersetzliche Hilfe. Thanks to Dr. Sonia Altizer and Dr. Amy
Pederson for teaching inspiring classes in disease ecology at Mountain Lake
Biological Station. I benefited greatly from the fruitful discussions and helpful
comments on my project. Thanks to all y’all! Frage fünf StatistikerInnen und …letzten
Endes verdanke ich Frau Dr. Karin Neubert von der Abteilung Medizinische Statistik
des
Universitätsklinikums
Göttingen
den
Abschluss
meiner
statistischen
Erkundungszüge, wunderbare Erste-Hilfe-Pakete inklusive! Dass dieses Werk
sprachlich noch abgerundet und poliert wurde, verdanke ich Frau Ingrid Rossbach,
Katie Gascoigne, Petra Schnüll und Don Yvan Lledo Ferrer.
The study was conducted under a letter of understanding between the Universidad
Nacional de la Amazonía Peruana (UNAP), Iquitos (Peru), and the German Primate
Center (DPZ) in Göttingen. I especially thank the German Academic Exchange
Service (DAAD) and the German Research Foundation (DFG) for financial support;
and the Boehringer Ingelheim Fonds (B.I.F) and Sanofi-Aventis (i-lab Award) for the
travel allowances. Ein besonderer Dank gebührt Frau Maria-Luise Nünning für Ihre
tolle Betreuung während des DAAD finanzierten Aufenthaltes in Peru. Frau
C. Schmetz vom Bernhard-Nocht-Institut möchte ich sehr danken für die Präparation
und REM-Aufnahme des Acanthocephalen; und Julia Diegmann und Mirjam
Nadjafzadeh für das freundliche Überlassen der „Wirtsfotos“.
Danksagung
217
Eine Danksagung ist wohl nie vollständig, aber irgendwann muss sie zu Ende
gehen...To all these people, my sincere thanks! ¡MuchisSIsimas gracias!
Zum Schluss möchte ich meinen Freundinnen und Freunden danken, die zum Teil
fachlich, zum Teil auch erfrischend unfachlich zum Gedeihen dieses Werkes
beigetragen haben. Der alles umfassende, abschließende Dank gehört meinen
Eltern. Weit über die biologische Ermöglichung dieser für mich wichtigen Arbeit
hinausgehend, bedanke ich mich auch von ganzem Herzen bei ihnen für die
uneingeschränkte Unterstützung, die unzählbaren Aufmunterungen und das immer
spürbare An-mich-Glauben!
ISBN 978-3-939902-34-8
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