REVIEW/ ARTÍCULO DE REVISIÓN
Key words: biodiversity – helminths – latitude – study effort – taxonomic resolution – tropics.
Abstract
Although the latitudinal gradient in species richness is one of the clearest global patterns of biodiversity, evidence
to date suggests that it either does not apply to parasites, or that if it does then the relationship is weak. In this short
review, I use a large database including information from 950 surveys of helminth parasite diversity in vertebrate
host populations to show that there is no latitudinal gradient in parasite species richness among bird or mammal
hosts, and a weak one among fish hosts going against the general trend: fish from temperate latitudes tend to
harbour more helminth species than those from the tropics. However, analyses of that database also show that
several disparities between temperate and tropical parasite surveys can underlie the above finding. First, surveys of
parasite diversity are accumulating at a much higher rate in temperate areas than in the tropics. Second, the overall
level of parasitological knowledge per host species is generally higher for temperate vertebrates than for tropical
ones. Third, the taxonomic resolution achieved per survey is also generally higher for temperate vertebrates than
for tropical ones. Data from temperate and tropical regions are therefore not truly comparable at present, and it may
be premature to attempt any large-scale test of the latitudinal diversity gradient hypothesis, or to accept the
conclusions of previous studies attempting such a test.
Palabras clave: biodiversidad - esfuerzo del estudio - helmintos - latitud - resolución taxonómica - trópicos.
Resumen
Aunque el gradiente latitudinal de riqueza específica es uno de los patrones globales de biodiversidad más
evidentes, sin embargo, hasta la fecha, o bien no se ajusta para el caso de los parásitos, o si ocurre, la relación es
débil. En esta breve revisión, utilizo una amplia base de datos con información sobre 950 estudios de diversidad de
parásitos helmintos en poblaciones de vertebrados (aves, mamíferos y peces) para demostrar que no existe un
gradiente latitudinal de la riqueza específica de parásitos entre aves o mamíferos; y que sí existe una débil relación
en el caso de los peces, siendo ésta contraria la tendencia general. Es decir, los peces de latitudes templadas tienden
a albergar más especies de helmintos que los de los trópicos. Sin embargo, estos análisis también muestran ciertas
discrepancias entre los estudios parasitológicos de zonas templadas y tropicales que subyacen a los resultados
obtenidos. En primer lugar, la tasa de elaboración de estudios sobre diversidad parasitaria en áreas templadas es
mucho mayor que en áreas tropicales. En segundo lugar, el conocimiento global parasitológico a nivel del
hospedador es generalmente mayor para los vertebrados de zonas templadas. Y en tercer lugar, la resolución
taxonómica alcanzada en cada estudio, también es generalmente mayor en hospedadores de las zonas templadas
que de las tropicales. Por lo tanto, los estudios de las regiones templadas y tropicales no son del todo comparables
por el momento, es por ello que quizás sea prematuro, intentar comprobar a gran escala la hipótesis del gradiente
latitudinal de diversidad, así como, el aceptar las conclusiones de estudios previos que han intentado comprobarla.
Neotrop. Helminthol., 4(2), 2010
2010 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
LATITUDINAL GRADIENTS IN PARASITE DIVERSITY:
BRIDGING THE GAP BETWEEN TEMPERATE AND TROPICAL AREAS
GRADIENTE LATITUDINAL DE DIVERSIDAD PARASITARIA:
LLENANDO EL VACÍO ENTRE LAS ÁREAS TEMPLADAS Y TROPICALES
1
Robert Poulin
Suggested citation: Poulin, R. Latitudinal gradients in parasite diversity: bridging the gap between temperate and tropical areas.
Neotropical Helminthology, vol. 4, nº 2, pp. 169-177.
1 Department of Zoology, University of Otago, Dunedin, New Zealand.
169
INTRODUCTION
Perhaps the most striking global pattern of
biodiversity is the latitudinal gradient in species
richness: as a general rule, there are more species in
the tropics than at higher latitudes (Gaston, 2000;
Willig et al., 2003; Hillebrand, 2004). Several non-
mutually exclusive processes are believed to have
generated this pattern, ranging from the greater
input of solar energy at lower latitudes to a greater
amount of effective evolutionary time because of
fewer geological disruptions (Rosenzweig, 1995).
These are all universal processes that should affect
all taxa, thus explaining why the latitudinal
gradient of diversity applies to the majority of plant
and animal groups that have been investigated.
Parasites should be no exception; in principle, both
the number of parasite species per host species, as
well as the total number of parasite species per unit
area should also increase toward the equator.
However, the various studies focused on parasites
have not revealed strong or universal latitudinal
gradients in parasite diversity (see reviews in
Poulin & Morand, 2000, 2004).
There are several possible explanations for this
discrepancy between results on free-living
organisms and those on parasites. For instance,
perhaps the number of parasite species that can
exploit a host is limited by the resources available
in this host, so that regardless of local
biogeographical conditions, the average or
maximum number of parasite species per host
species is constrained by host properties. Another
explanation might be that there has been a
disproportionately low study effort aimed at
finding and identifying parasites in animals from
tropical areas. Surveys of parasite biodiversity
require both taxonomic expertise and a greater
investment of time than surveys of free-living
organisms, because of the additional effort needed
for dissection, finding parasites within the host's
body, and preparing them for microscopy. These
surveys have a long tradition in North America and
Europe, but have only been initiated more recently
in tropical areas, which may explain why parasite
faunas in tropical areas do not always seem more
diverse than those in temperate areas. Discovery
and proper identification of parasites is crucial for
conservation biology as well as for mitigating the
risks of emerging diseases associated with
biological invasions and other environmental
perturbations (Brooks & Hoberg, 2000, 2001). It is
therefore important to obtain some quantitative
information on the gap, if any, between the levels
of effort invested in parasite diversity surveys
between tropical areas and higher latitudes.
This short paper examines trends in parasite
diversity and in the scientific effort invested
toward discovering parasites as a function of
latitude. Here, the focus is on contrasting tropical
areas with higher latitudes on a global scale;
therefore, the analysis includes not only the
Neotropics, but all tropical areas delimited by the
Tropic of Cancer (23.4°N) and the Tropic of
Capricorn (23.4°S). To provide a quantitative basis
for discussion, I use simple analyses on data from a
large database compiled by Poulin & Leung
(2010). This database consists of data on 950
surveys of helminth communities from 650
different species of fish, bird and mammal hosts
studied between the years 1936 and 2009; the full
data set, including the list of the original 545
published sources, is available with the online
version of Poulin & Leung's (2010) article. Each
entry in this dataset corresponds to one parasite
survey providing a clear list of all species of
tr ematodes, cestodes , nematodes and
acanthocephalans found in one sample of hosts
from the same species from one locality, i.e. one
local parasite community; some host species have
been the subject of a few separate studies, and thus
for those host species there are two or more entries
in the dataset. The dataset was assembled from
studies found with a search of the Web of Science
that were available to the authors in electronic or
printed form (see Poulin & Leung, 2010, for
details). It is therefore likely that it excludes many
relevant studies from tropical areas published in
local journals. However, this is part of the problem:
if data on tropical parasites are unavailable to the
international scientific community, it will be
difficult for anyone to attempt large-scale tests of
latitudinal biodiversity gradients or other patterns.
Nevertheless, the dataset does provide a basis for
comparisons and discussion.
I will tackle four questions in this article. First, is
there some support for a latitudinal gradient of
parasite species richness among the studies in the
dataset? Second, is there a difference in the
cumulative number of parasite surveys over time
between the tropics and areas at higher latitudes?
Third, is there a difference between the tropics and
Latitudinal gradients in parasite diversity Poulin
170
areas at higher latitudes with respect to the average
study effort invested per host species? Four, is the
taxonomic resolution achieved during parasite
identification as part of diversity surveys the same
in the tropics as in areas at higher latitudes? Each of
these will be addressed with simple analyses using
the database described above, and discussed in
relation to the literature to provide a brief overview
of the challenges ahead.
LATITUDINAL GRADIENT IN PARASITE
DIVERSITY
The available empirical evidence for an
association between latitude and parasite species
richness is equivocal at best (see Poulin & Morand,
2004). For instance, among mammal species,
Poulin (1995) found no relationship between
helminth species richness and latitude. In contrast,
Nunn et al. (2005) found that the number of
parasite species, including both metazoans and
microparasites, infecting primates increased
toward the equator, while Lindenfors et al. (2007)
found exactly the opposite trend, i.e. greater
richness at higher latitudes, for parasites in
carnivores. Studies of pathogen richness among
human populations tend to show that parasite
diversity is greatest in tropical countries, although
the challenges of disentangling the respective
effects of climatic, ecological, socio-economic and
political factors make it difficult to assign causality
to any particular factor (Guernier et al., 2004;
Dunn et al., 2010).
The overall picture emerging from studies of fish
parasites is equally muddled. Among marine fish
species, there seems to exist a latitudinal gradient
in ectoparasite species richness. As a rule, the
diversity of ectoparasites, in particular
monogeneans, is higher in tropical or warm water
areas than in temperate regions (Poulin & Rohde,
1997; Rohde & Heap, 1998). This pattern is
independent of any differences in host body sizes
or of potential phylogenetic influences (Poulin &
Rohde, 1997). In contrast, there is no measurable
difference in the species richness of endoparasite
species between tropical and temperate areas
(Rohde & Heap, 1998). Among freshwater fish
species, comparative studies have revealed that
temperate fish species are hosts to richer
assemblages of helminth parasites than tropical
fish species (Choudhury & Dick, 2000). This
surprising trend persists once we eliminate the
potentially confounding effects of differences in
sampling effort, host body size, and host
phylogenetic affinities (Poulin, 2001). Therefore,
there is no consistency among the results obtained
for fish hosts: parasite species richness peaks in
temperate regions for helminths of freshwater
fishes, it peaks in the tropics for ectoparasites of
marine fishes, and it shows no latitudinal variation
for endoparasites of marine fishes.
Here, I provide an additional empirical test of the
latitudinal gradient in parasite diversity, using the
database described above. In this database, most
available surveys (828 out of 950) came from the
Northern Hemisphere. I treated latitude regardless
of whether it was north or south, since preliminary
analyses indicated that it made no difference
whether or not the two hemispheres were
differentiated. Endohelminth species richness is
defined as the total number of endohelminth
species found in a particular survey. Correlations
between endohelminth species richness (log-
transformed) and latitude of the survey were not
statistically significant for bird hosts (r = -0.11, P =
0.13) and mammal hosts (r = -0.01, P = 0.80), but
there was a significant positive correlation in fish
hosts (r = 0.14, P = 0.002) (Fig. 1). In other words,
fish at higher latitudes tend to harbour more
species of helminths than those at lower latitudes,
i.e. those in the tropics. This is a relatively weak
pattern, however, since latitude explained only
<3% of the variance in parasite species richness.
Thus, there are many fish populations from high
latitudes harbouring relatively poor parasite
communities (see Fig. 1).
These new results echo those of Choudhury &
Dick (2000) and Poulin (2001) by suggesting that
fish at higher latitudes might harbour richer
parasite assemblages, but the pattern is weak. For
bird and mammal hosts, no latitudinal gradient is
apparent across the many surveys in the database.
These results do not bring us closer to determining
whether or not there is a latitudinal gradient in
parasite diversity; instead, they just add to the
growing list of inconsistent patterns reported to
date. The lack of congruence among these past
results suggests at least two possibilities. First,
maybe there is no latitudinal gradient in species
diversity applying to parasites. Solar energy
ultimately controls the productivity and diversity
of ecosystems, but for parasites the direct
determinant of resource availability is the host, and
171
Neotrop. Helminthol., 4(2), 2010
maybe host properties such as body size, metabolic
rate or lifespan, are much more important for
parasite diversification than the latitude at which
the host lives. There may be a few exceptions, such
as ectoparasites of marine fish hosts; Rohde (1992)
has proposed that higher water temperature in
tropical seas should promote higher mutation rates
and shorter generation times in monogeneans,
possibly leading to higher rates of diversification.
For other parasites in general, however, tropical
areas may not necessarily be hotspots of diversity.
Latitudinal gradients of species richness indeed
tend to be weak for small-bodied taxa (Hillebrand
& Azovsky, 2001), and parasites do tend to be
small. Second, perhaps there really is a latitudinal
gradient in parasite species diversity but we cannot
detect it because currently available data are
inadequate. It is not farfetched to believe that more
data are available from temperate regions of North
America and Europe than for tropical regions of
the world, simply because (i) North American and
European countries have a longer history of
scientific research, and (ii) governments of these
countries invest a proportionally greater amount of
money into science, including basic biological
research, than governments of most tropical
countries. Therefore, the lack of data may mask a
true underlying latitudinal gradient in parasite
diversity. The next three sections of this review
explore this possibility by examining the evidence
that tropical parasite data are not really comparable
to temperate parasite data.
CUMULATIVE NUMBER OF SURVEYS
The more we study something, the better we know
it. Existing knowledge of parasite diversity is
increasing at different rates for different parts of
the world, and these differences make it difficult to
compare parasite diversity between different
geographical areas. For instance, in a comparison
between parasite diversity in New Zealand and
Canadian fishes, differences in past study effort
between the two countries appeared to account for
most of the variation found, and suggested that
parasite diversity in New Zealand has been
severely underestimated (Poulin, 2004). It is
therefore important to assess whether surveys of
parasite diversity in temperate and tropical areas
have been performed at comparable rates.
A look at the cumulative number of parasite
surveys in vertebrate hosts published over time
reveals some clear patterns (Fig. 2). Firstly, the
number of surveys of parasites in tropical
vertebrates only started to rise in the 1980s,
whereas by that time surveys of parasites in
temperate vertebrates were accumulating at a
steady rate. Secondly, in the past decade, the rate of
increase in the number of published surveys is
Figure 1. Species richness of endohelminth parasites
plotted as a function of the latitude at which a host
sample has been collected, for 419 surveys of fish hosts,
161 surveys of bird hosts, and 370 survey of mammal
hosts. The best-fit line is shown for the only significant
relationship, i.e. that observed in fish hosts.
172
Latitudinal gradients in parasite diversity Poulin
much higher for temperate hosts than for tropical
hosts (Fig. 2). These findings suggest that the study
effort devoted to tropical parasite assemblages is
still lagging behind that devoted to temperate
parasites. Of course, these results are derived from
a database assembled from studies that were both
(i) included in the Web of Science, and (ii)
available either electronically or in print via the
University of Otago's excellent library. Many
parasite surveys published in local journals were
no doubt missed, and these may include a
disproportionate number of surveys from tropical
regions. However, any attempt to test the existence
of a latitudinal gradient in parasite diversity will
have to be based on internationally available data,
and presently, on this international level, research
on tropical parasite assemblages is clearly far
behind that on their temperate counterparts.
Another difference between surveys in temperate
areas and those in tropical areas concerns the
frequency at which the same host species is studied
more than once. As stated earlier, some host species
have been the subject of a few separate studies, and
for those host species there are two or more entries
in the database. In temperate areas, the database
included 807 surveys on 527 host species, among
which 146 species, or 27.7%, were the subject of
more than one survey. In tropical areas, there were
143 surveys on 123 host species, among which 8
species, or 6.5%, were the subject of more than one
survey. Thus temperate host species are about 4
times more likely to be surveyed more than once,
generally in different localities, than tropical host
species. Since both the composition of parasite
communities and the abundance of specific
parasite species can vary substantially among
localities (Poulin & Morand, 1999; Poulin, 2006;
Krasnov et al., 2005, 2008), the data currently
available for temperate species is more
representative simply because for many host
species it covers a broader portion of the
geographic range.
The available number of surveys of parasite
diversity in tropical vertebrates is growing rapidly,
but still trailing that for temperate hosts. This is
probably only a temporary problem, however,
since a large group of very active researchers in
Latin America is rapidly closing that gap (see
Salgado-Maldonado et al., 2000). Indeed, a few
very active individuals can speed up parasite
discovery in an entire geographical region over a
few years of intense work, as illustrated by the
history of research on cestodes from Australia
(Beveridge & Jones, 2002). Thus, we are fast
approaching a time when the discrepancy in
available parasite surveys between temperate
regions and the tropics will vanish, allowing more
robust tests of the latitudinal gradient in parasite
diversity.
STUDY EFFORT PER HOST SPECIES
The number of available parasite surveys for a
region is not the only measure of how much
research effort has been invested in the study of
parasitism in that region. There are also many
studies on the taxonomy, pathology, life cycles,
etc. of parasite species. The combined research
effort put into all these aspects of host-parasite
relationships must also be comparable between
geographical regions if we want to use them in the
same analysis, for instance by comparing parasite
diversity between temperate and tropical regions.
In the database used here, the relative study effort
devoted to parasites in the host species was
estimated as the total number of records obtained
from a search of the Web of Science using the
keywords: Latin binomial name of host species
AND (parasit* OR helminth* OR tremat* OR
digenea* OR nemat* OR cestod* or
acanthoceph*). Although this measure does not
Figure 2. Cumulative number of parasite surveys as a
function of year of publication for vertebrate hosts
sampled in the tropics (between 23.4°N and 23.4°S) and
outside the tropics.
173
Neotrop. Helminthol., 4(2), 2010
perfectly capture all previous work on the
taxonomy, pathology, life cycles, etc., of parasites
found in the host species, it reflects the extent to
which researchers have studied the parasites of that
host. This is also a much more relevant measure of
study effort than host sample size, since existing
knowledge of the biology of parasites in a given
host species depends on the extent of previous
work rather than on how many individual hosts are
examined in a particular survey. Based on this
measure, the study effort devoted to parasites of
both fish and mammal hosts in the tropics was
significantly lower than that devoted to host
species outside the tropics (one-way ANOVAs on
log-transformed study effort; fish: F = 36.44, P
1,417
< 0.0001; mammals, F = 26.07, P < 0.0001). The
1,368
difference is substantial: on average, the study
effort toward parasites of non-tropical species of
fish and mammals is about three times higher than
for tropical species (Fig. 3). The difference was not
significant for bird hosts, however (F = 2.47, P =
1,159
0.11), most likely because the sample size for
tropical bird hosts is very small, i.e. only 6
available surveys of parasites for tropical birds
(Fig. 3).
These results indicate clearly that for the two host
taxa for which sufficient data are available, i.e. fish
and mammals, much more parasitological research
is carried out per host species in temperate areas
than in the tropics. This is likely to seriously impact
our attempts to search for latitudinal gradients in
parasite species diversity. For instance, this would
mean that there are, on average, more taxonomic
studies performed on temperate parasites than on
tropical parasites. Taxonomy allows us to
distinguish between closely related species, and
with better taxonomic knowledge, we can achieve
more accurate estimates of parasite species
diversity. The next section illustrates how the
lower study effort devoted to parasitism in the
tropics has seemingly impacted our ability to
discriminate among related species.
T A X O N O M I C R E S O L U T I O N O F
PARASITES
It is becoming increasingly clear that nature is full
of cryptic species that cannot be distinguished
from each other based on morphology, even by
expert taxonomists. In recent years, a large number
of studies have used molecular tools to discover
new species, with the result that what was
previously thought to represent a single species is
in fact a complex of two or more closely related
species (Poulin & Morand, 2004; Pérez-Ponce de
León & Nadler, 2010). This revolution in our
understanding of biodiversity is happening at a
time when changing funding priorities are
threatening the maintenance of taxonomic
expertise in museums and universities. The
worldwide loss of taxonomic expertise is seen as
one of the greatest challenges to current research in
parasite biodiversity and ecology (Brooks &
Hoberg, 2000, 2001; Cribb, 2004).
There may already be measurable effects of this
loss in taxonomic expertise. Among the surveys in
the database used here, parasite taxa are often not
identified all the way down to species level, but
only to genus or family level. A classical example
is provided by the nematode Anisakis, which is
almost always listed only by genus name in
numerous surveys of parasites of marine fishes.
Recently, Poulin & Leung (2010) have showed that
the level of taxonomic resolution achieved per
survey has decreased significantly in the past ten
years compared to the previous decades. The
gradual loss of taxonomic experts mentioned
above is one possible explanation. In the context of
latitudinal gradients in diversity, it is now
Figure 3. Mean (±SE) study effort devoted to parasites
of host species sampled in the tropics (between 23.4°N
and 23.4°S) and outside the tropics, shown separately
for fish, bird and mammal hosts. Study effort is
measured as the total number of relevant records
obtained from a search of the Web of Science. Numbers
on the bars indicate sample sizes.
Latitudinal gradients in parasite diversity Poulin
174
important to compare the level of species
identification achieved in parasite surveys from
temperate and tropical regions.
Here, taxonomic resolution was calculated for each
of the 950 surveys in the database as the proportion
of endohelminth taxa, out of the total recovered in a
survey, that were identified to species level, i.e.
given a full binomial Latin name. Thus, for
example, a taxonomic resolution value of 1.0 in a
given survey means that all species were identified
to species level, and a value of 0.5 means that only
half of the parasites were identified to species
level. Taxonomic resolution for both fish and
mammal hosts in the tropics was significantly
lower than that for hosts outside the tropics (one-
way ANOVAs on arcsine-transformed taxonomic
resolution; fish: F = 7.19, P = 0.007; mammals,
1,417
F = 5.23, P = 0.022). The difference is modest,
1,368
with the resolution achieved in non-tropical
species of fish and mammals being not quite 10%
higher than for tropical species (Fig. 4). However,
the difference was not statistically significant for
bird hosts (F = 1.82, P = 0.17), possibly because
1,159
the sample size for tropical bird hosts is very small,
i.e. only 6 available surveys of parasites for tropical
birds (Fig. 4).
These results suggest that estimates of parasite
species richness cannot be compared between the
tropics and temperate areas, because at the moment
the lower taxonomic resolution achieved in
tropical parasite surveys probably leads to small
but systematic errors in richness values. Assuming
that some of the taxa identified only to genus or
family level often consist of two of more cryptic
species, parasite species diversity in the tropics is
more likely to be underestimated than in temperate
regions.
Based on a large database compiled from 950
surveys of parasite diversity in vertebrate hosts, the
present study has found no consistent or
convincing evidence for a latitudinal gradient in
parasite species richness. However, analyses of
this database also indicate that (i) surveys of
parasite diversity are accumulating at a much
higher rate in temperate areas than in the tropics,
(ii) the overall level of parasitological knowledge
per host species is generally higher for temperate
vertebrates than for tropical ones, and (iii) the
taxonomic resolution achieved per survey is also
generally higher for temperate vertebrates than for
tropical ones. It is therefore premature to attempt
any rigorous large-scale test of the latitudinal
diversity gradient hypothesis, because temperate
and tropical data are not yet comparable in a
quantitative manner. The current rate at which new
parasitological knowledge is accumulating in the
tropical region, especially in the Neotropics,
suggests that such a test will be realistic within just
a few years. At present, it would be safer not to
consider parasites as exceptions to the almost
universal pattern of increasing diversity toward the
equator (Gaston, 2000), since the final verdict is
still awaiting the data.
I thank Tommy Leung for his invaluable assistance
in compiling the database used for the analyses in
the present article, and Isabel Blasco-Costa for
translating the title and abstract into Spanish.
Figure 4. Mean (±SE) taxonomic resolution of parasites
in host surveys from the tropics (between 23.4°N and
23.4°S) and outside the tropics, shown separately for
fish, bird and mammal hosts. Taxonomic resolution is
the proportion of helminth taxa in each survey identified
to species level. Numbers on the bars indicate sample
sizes.
CONCLUSIONS
ACKNOWLEDGMENTS
Neotrop. Helminthol., 4(2), 2010
175
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* Correspondence to author/Autor para
correspondencia:
Robert Poulin
Department of Zoology, University of Otago,
Dunedin, New Zealand
Correspondence:
Tel.: +64 3 479-7983
Fax.: +64 3 479-7584
E-mail/correo electrónico:
robert.poulin@stonebow.otago.ac.nz
Received July 1, 2010.
Accepted October 27, 2010.
177
Neotrop. Helminthol., 4(2), 2010
