Abstract
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
Resumen
BIODIVERSITY OF FISH PARASITES FROM GUANDU RIVER, SOUTHEASTERN
BRAZIL: AN ECOLOGICAL APPROACH
BIODIVERSIDAD DE LOS PARÁSITOS DE PECES DE RÍO GUANDU, SURESTE DE
BRASIL: UNA APROXIMACIÓN ECOLÓGICA
1 1 2*
Rodney K. de Azevedo ; Vanessa D. Abdallah & José L. Luque
1 Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro, Seropédica, Brasil.
2 Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Caixa Postal: 74.508, Seropédica,
Brazil, CEP: 23851-970. E-mail: jlluque@ufrrj.br
*Correspondence to author/ Autor para correspondencia: José L. Luque
Suggested citation: Azevedo, R.K., Abdallah, V.D. & Luque, J.L. 2011. Biodiversity of fish parasites from Guandu river,
Southeastern Brazil: an ecological approach. Neotropical Helminthology, vol 5, nº 2, pp.185-199.
Key words: Biodiversity- Brazil- ecology parasite- fishes- Guandu River- parasites.
En el presente trabajo, se realiza un análisis comparativo de las comunidades de parásitos de 21
especies de peces en el río Guandu, Brasil y se evaluó el efecto de algunas de las características del
huésped (tamaño corporal, comportamiento social, hábitat de los peces, categoría trófica y capacidad
de migrar) en la diversidad de sus comunidades de parásitos metazoarios. Como una medida de
diversidad, hemos utilizado la riqueza de especies de parásitos y la diversidad taxonómica. La riqueza
de especies de parásitos y la diversidad taxonómica no se vieron afectados por el número de los
espécimenes examinados por especie. El tamaño del cuerpo de los peces mostró una correlación
significativa con la riqueza de especies de parásitos, aunque no hay correlación con la diversidad
taxonómica de los parásitos. Las principales características asociadas a la diversidad taxonómica de los
parásitos son la formación de cardúmenes y la categoría trófica omnívora. Las comunidades de
parásitos de peces en el río Guandu presentaron comunidades parasitarias aisladas.
Palabras clave: Biodiversidad- Brasil- ecología parasitaria- parásitos- peces - río Guandu.
Neotrop. Helminthol., 5(2), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043
185
Here, we performed a quantitative analysis of the parasite communities in 21 species of fish from
Guandu River, Brazil; we evaluated the effects of some host traits (body size, social behavior, fish's
habitat, trophic category and ability to migration) on the diversity of their communities of metazoan
parasites. To measure quantitative diversity, we used parasite species richness, as well as the average
taxonomic distinctness of the assemblage and its variance. The parasite species richness, the taxonomic
distinctness and the variance were unaffected by the number of host individuals examined per species.
Fish body length proved to be the main predictor of parasite species richness, although it did not
correlate with parasite taxonomic distinctiveness. The mains host features associated with the
taxonomic diversity of parasites were schooling behavior and omnivores trophic category. Parasite
communities found in fish from Guandu River isolationist communities.
INTRODUCTION
Parasite communities are playing an increasingly
important role as models for the study of
biodiversity and biogeography (Poulin & Morand,
2000). Given the integral roles played by parasites
in natural ecosystems, identifying hotspots of high
parasite diversity, as well as areas of relatively low
parasite diversity, is crucial for a complete
understanding of the functioning of the biosphere.
Currently, the biodiversity of marine and
freshwater ecosystems of Latin America is
threatened, mainly by environmental problems
resulting from the destruction and degradation of
the ecosystems. In this context, parasite
biodiversity can be very important because
parasitism plays key roles in ecosystems,
regulating the abundance or density of host
populations, stabilize food webs and structuring
animal communities (Luque & Poulin, 2007).
Takemoto et al. (2005) performed the first study
relating the different features of host species and
the parasite species richness in freshwater fishes
from Neotropical Region. In fish, for instance,
some previous studies have found that host body
size is a good predictor of parasite species richness
whereas others have found no effect of host size.
The same is true for a range of other host features. It
is therefore difficult to assess the relative
importance of different host traits for the evolution
of parasite diversity in general (Luque et al., 2004;
Luque & Poulin, 2008).
In the present study, we examine the relationship
between different features of host species and the
diversity of metazoan parasite communities across
species of fish hosts from Guandu River (Fig. 1) in
function of the strategic importance of this river,
which is the main source of potable water in Rio de
Janeiro, Brazil. The Guandu River supply water to
90% of population of City of Rio de Janeiro and
although be a very impacted environment (Bizerril
& Primo, 2001), it maintains an important level of
biodiversity of fishes, and consequently, fish
parasites (Azevedo et al., 2010). In addition, data
about population and community and quantitative
descriptors from the fish hosts are given herein.
Between April 2003 to September 2009 were
analyzed 786 specimens of fish, belonging to 21
species (Table 1) from the Guandu river, near the
dam of water treatment station (WTS) (22°48'32"S,
43°37'35"W). The taxonomy of the fishes follows
that of Reis et al. (2003). Parasites were collected
from the body surface, gills, and body cavities, and
viscera after examination under a stereoscopic
microscope. Washings from gills and gut lumen
were strained using a sieve (53 and 75 μm mesh
size) to retain even the smallest parasites.
Following Bush et al. (1997), prevalence, intensity
and abundance mean were calculated for parasites
of all fish species.
Pearson's correlation coefficient r was used to
analyze the possible correlation between the host's
total body length and the abundance of parasites,
with previous logarithmic transformation Log
(x+1) (Zar, 1999). The analysis included only
parasite species with prevalence greater than 10%
(Bush et al., 1990).
The following descriptors were calculated at the
parasites infracommunity level: total prevalence,
total intensity, total abundance, total species
richness, endoparasite and ectoparasite species
richness, Margalef's richness index (d), Brillouin's
diversity index (H) (log 10 based), Pielou's
evenness index (J`) and Berger-Parker dominance
index. In addition the Bray-Curtis similarity index
was calculated among infracommunities within
host fish species (Magurran, 2004). These
descriptors were used for all parasites with
exception of myxozoans. Statistical significance
level was established at P<0.05. All results were
presented in tabular form (Tables 2 and 3). The
relative abundance of metazoan parasites was
calculated at the level of infracommunities for all
species of fish that had more than three species of
parasites. The results were presented in graphical
form (Figs. 2 and 3).
For each fish species, the average taxonomic
distinctness (Δ+) and variance in taxonomic
distinctness (Λ+) of the parasite component
community were computed, following the
procedures and taxonomies used by Luque &
Poulin (2008). The effect of host length on
taxonomic distinctness, on variance and on total
richness were evaluated using the Pearson
correlation coefficient on logarithmic transformed
data. The Student`s t test or ANOVA test,
depending of the number of variables with previous
transformation, was used to verify the influence of
MATERIAL AND METHODS
186
Biodiversity of fish parasites from Guandu river
Azevedoet al.
the followings variables in the taxonomic
distinctness and variance in taxonomic
distinctness: (1) whether the fish species forms
schools or not, with species adopting schooling
only in some parts of the year (e.g. during the
reproductive period) classified as schooling; (2)
whether the fish's habitat is benthic, benthopelagic
or demersal; (3) the trophic category, where the fish
species were distributed into four categories:
detritivores, herbivores, omnivores or carnivores
and (4) whether species accomplish or not
migration, being classificated as potamodromous
or diadromous. Data were obtained from Fishbase
(Froese & Pauly, 2010). Table 4 showed the entire
data set of host species included in the analyses.
The present study follows the classification and
systematic arrangements used by Azevedo et al.
(2010). Parasite species names follow those
provided in the most recent taxonomic literature.
Species of fishes are arranged in alphabetical
sequence and valid names are adopted from Froese
& Pauly (2010).
Figure 1. Map of the Guandu River and the area of collection
(circle) near to the dam of water treatment station (WTS)
(22°48'32” S, 43°37'35” W).
Figure 2. Species richness of fish parasites according to
zoological group reported in the Guandu River, State of Rio de
Janeiro, between 2003 to 2009.
Figure 3. Distribution of parasite genera in fish's species
collected from Guandu River, State of Rio de Janeiro, between
2003 to 2009.
RESULTS
A total of 786 specimens of fish was analyzed and
were found 15.630 specimens of parasite
belonging to 81 species. Nine groups of metazoan
parasites were found: Acanthocephala, Cestoda,
Crustacea, Digenea, Hirudinea, Mollusca,
Monogenea Myxozoa and Nematoda. In these fish,
187
Neotrop. Helminthol., 5(2), 2011
Table 1. Prevalence, mean abundance, mean intensity, site of infection / infestation of metazoan parasites from fish collected in the Guandu river, State of Rio de
Janeiro, Brazil. (s = standard deviation, * parasites that had a positive correlation between abundance and its host's total length through Pearson's correlation
coefficient r).
188
Biodiversity of fish parasites from Guandu river
Azevedoet al.
Site of infection
(metacerraride)
(Table 1)
outer surface of
the bladder Eyes
189
Neotrop. Helminthol., 5(2), 2011
Site of infection
Digenea
(Table 1)
190
Biodiversity of fish parasites from Guandu river
Azevedoet al.
Digenea
Site of infection
(Table 1)
191
Neotrop. Helminthol., 5(2), 2011
Site of infection
(Table 1)
192
Biodiversity of fish parasites from Guandu river
Azevedoet al.
Site of infection
(Table 1)
193
Neotrop. Helminthol., 5(2), 2011
Site of infection
Nematoda
(Table 1)
194
Biodiversity of fish parasites from Guandu river
Azevedoet al.
Site of infection
a total of 69% were parasitized by at least one
species of metazoan parasite. The percentage of
parasitism was 55% for endoparasite and 45% for
ectoparasites.
The monogeneans had higher species richness at
component community level. Of all the parasites
found, the digenean had lower specificity, since the
metacercaria Austrodiplostomum compactum
(Lutz, 1928) was found parasitizing nine different
species of fish. Of all the species of parasites
collected only four showed positive correlation
between the hosts' total length and abundance: in
Geophagus brasiliensis (Quoy and Gaimard,
1824) the digenean Posthodiplostomum
macrocotyle Dubois, 1937 (r=-0,289; p=0,041), in
Hypostomus affinis (Steindachner, 1877) the
monogenean Hyperopletes malmbergi Boeger,
Kritsky and Belmont- Jégu, 1994 (r=0,394;
p=0,028), in Mylossoma aureum (Spix and
Agassiz, 1829) the monogenean Anacanthorus
paraspathulatus Kritsky, Boeger and van Every,
1992 (r=0,484; p=0,049) and in Pimelodus
maculatus Lacépède, 1803 the nematoda
Cucullanus (Cucullanus) pinnai pinnai Travassos,
Artigas and Pereira, 1928 (r=0,513; p=0,001).
Centropomus undecimalis (Bloch, 1792) showed
the highest mean parasite diversity (H)=0.57±0.42
and Margalef's richness index (d)=0.64±0.48. The
values found for the index of interactivity CC in
50
parasite communities in fishes from Gaundu river
were high, indicative of isolationist communities.
The host's total length was positively correlated
with richness (r=0.999, p=0.00), but not with either
Δ+ (r=-0.169; p=0.563) or Λ+ (r=0.03, p=0.917).
The richness was not significantly correlated with
Δ+ (r=-0.017, p =0.558) nor with Λ+ (r=0.032,
p=0.912), showing that species with high parasite
richness does not necessarily have high taxonomic
distinctness and variance. The number of fish
examined was not correlated with richness
(r=0.223, p =0.602), with taxonomic distinctness
(r=-0.119, p =0.454), or with the variance
(r=0.031, p =0.908), showing that these indexes are
independent of the sampling effort.
Of the categorical variables considered, only two
significant results were obtained: Δ+ varied
significantly between schooling and non-schooling
fish species (t=2.527, p=0.026) and among fish
species with different trophic category (detritivores
and omnivores) (t=2.905, p=0.033). Omnivores
and schooling fish species had higher values of Δ+
than other groups.
DISCUSSION
The results of this study indicate that the parasite
communities of fish in the Guandu River were
characterized by low parasite species richness and
evenness, by isolationist communities and by
greater values of taxonomic diversity in omnivores
and schooling fish species.
According to Kennedy (2009) all parasite species
have a niche selection to a greater or lesser degree,
but isolationist communities have species poor and
the species are independent of each other. By
contrast, interactive communities have highest
species richness. Communities could be located
anywhere along this continuum, and those of
freshwater fish tend to be found towards the
isolationist end.
(Table 1)
195
Neotrop. Helminthol., 5(2), 2011
Our results suggesting that host feeding habits and
the formation of schools may influence the
taxonomic diversity, since omnivores and
schooling fish species had higher parasite diversity
than other groups. According Luque et al. (2004)
many researches have found that schooling fish
species are used by more species of parasites than
solitary species, for both external parasites and all
parasites combined. The fact of omnivores fish
species present greater diversity can also be
explained, because the greater the variety of food,
the greater the intake of various intermediate hosts
and easier to contamination by parasites is acquired
via the food web.
A study by Takemoto et al. (2005) in the floodplain
of the upper Paraná River found that parasite
species richness in freshwater fish species was not
associated with several host characteristics, with
the exception of host population density. However,
in the study by Luque et al. (2004), the fish size
proved to be the main predictor of total parasite
species richness in marine fish. This result was also
found in this study. According to Luque et al.
(2004) following from island biogeographical
theory larger-bodied hosts should be able to
accommodate more parasite species than small
ones; they may also incur higher exposure to
internal parasites because of the quantities of food
they ingest, and to external parasites because their
larger surface area facilitates contact with infective
stages.
Considering both the approach and the results, the
present study includes both key improvements on
earlier studies of this kind and novel findings,
making its contribution particularly relevant. The
majority of earlier studies on the richness of
freshwater fish parasites have used data from fish
species that do not occur in the same geographical
areas, with exception to work of Takemoto et al.
(2005). The present study focused on a set of fish
species from the same general area (Guandu river),
thus minimizing any differences in parasite
availability. In addition, this study was the first to
incorporate the average taxonomic distinctness of
the assemblage and its variance as a measure of
taxonomic diversity in freshwater fish. For data, all
study in freshwater fish has used species richness
Rodney K. de Azevedo was supported by a student
fellowship from FAPERJ (Fundação Carlos
Chagas Filho de Amparo à Pesquisa do Estado do
Rio de Janeiro); Vanessa D. Abdallah was
supported by a student fellowship from CNPq
( C o n s e l h o N a c i o n a l d e P e s q u i s a e
Desenvolvimento Tecnológico, Brazil). José L.
Luque was supported by a Research fellowship
from CNPq and a grant from FAPERJ.
ACKNOWLEDGMENTS
study in freshwater fish has used species richness
as their sole measure of the diversity of parasite
assemblages. According to Luque et al. (2004) the
richness is a convenient measure, but it does not
capture all facets of diversity. It ignores the
evolutionary relationships among species
coexisting in an assemblage. Applied to parasite
assemblages, measures of diversity that
incorporate information on the relationships
among parasite species can shed light on how the
assemblage has been structured.
196
Biodiversity of fish parasites from Guandu river
Azevedoet al.
Hosts (N) P(%) MA MI ML
(cm)
MR Parasite
richness §
D
Astronotus ocellatus
35 74.00 13.71±0.38 18.46±0.51 20.44 1.77±1.23 2 (5) 0.43±0.41
Astyanax bimaculatus
40 30.00 0.95±0.05 3.16±0.15 9.92 0.37±0.58 2 (2) 0.03±0.12
Astyanax parahybae
40 35.00 0.65±0.03 1.86±0.08 10.39 0.35±0.48 2 (2) 0
Centropomus undecimalis
31 90.00 18.73±0.57 20.81±0.27 28.75 2.76±1.63 7 (5) 0.64±0.48
Cichla ocellaris
26 100.00 32.50±2.10 32.50±2.10 26.36 2.30±1.31 3 (4) 0.51±0.46
Cyphocharax gilbert 60 58.00 5.50±0.002 9.42±0.004 16.32 0.86±0.89 6 (1) 0.17±0.37
Geophagus brasiliensis
50 90.00 11.68±0.25 12.97±0.28 15.49 1.26±0.69 7 (3) 0.19±0.30
Gymnotus carapo
30 67.00 2.33±0.10 3.50±0.15 36.46 1.00±0.83 9 (1) 0.33±0.55
Hoplosternum littorale
10 60.00 2.91±0.05 4.85±0.08 19.65 1.03±1.13 5 (2) 0.25±0.52
Hypostomus affinis
31 87.00 26.35±1.09 30.25±1.26 27.75 2.09±1.30 2 (5) 0.46±0.38
Leporinus conirostris
18 61.00 27.33±3.80 44.72±6.23 36.60 0.72±0.57 1 (1) __
Leporinus copelandii 30 27.00 1.86±0.25 7.00±0.96 34.75 0.70±0.75 2 (3) 0.01±0.05
Loricariichthys castaneus 32 75.00 21.06±0.76 28.08±1.01 27.90 1.25±0.95 2 (3) 0.21±0.34
Mugil liza 34 79.00 12.50±0.83 15.74±1.04 34.05 1.82±1.78 6 (7) 0.48±0.66
Mylossoma aureum
17 100.00 223.70±12.96 223.70±12.96 15.66 1.64±0.49 1 (1) 0.18±0.22
Oligosarcus hepsetus
40 25.00 0.57±0.04 2.30±0.17 16.61 0.25±0.44 2 (1) 0
Pimelodus maculatus
40 100.00 59.42±1.50 59.42±1.50 22.92 2.57±1.22 5 (5) 0.42±0.28
Rhamdia quelen
32 80.00 40.16±1.99 50.20±2.49 32.68 1.46±1.00 5 (3) 0.21±0.25
Tilapia rendalii 30 84.00 2.8±0.09 3.36±0.10 22.14 0.83±0.38 0 (1) __
Trachelyopterus striatulus
60 95.00 40.83±0.64 42.98±0.67 19.20 1.46±0.74 8 (3) 0.16±0.22
Table 2. Number of hosts examined (N), total prevalence P(%), mean total abundance (MA), mean total intensity
(MI), mean length of hosts (ML), mean total species richness (MR), parasites richness and Margalef's richness index
(d) of metazoan parasites from Guandu River, State of Rio de Janeiro, Brazil.
(§) Endoparasites and ectoparasites (in parentheses).
Hosts ( H) J’ Dominant
taxon
Bray-Curtis Berger-
Parker
Δ+
Λ+
Astronotus ocellatus
0.45±0.34 0.62±0.43 Monogenea 41.70 (33.90-48.40) 0.45±0.30 95.60 311.30
Astyanax bimaculatus
0.02±0.09 0.04±0.19 Digenea 8.10 (6.10-9.50) 0.31±0.46 __ __
Astyanax parahybae
0 0 Digenea 6.30 ( 4.40-7.70) 0.35±0.48 __ __
Centropomus undecimalis
0.57±0.42 0.60±0.39 Monogenea 33.04 (26.90-38.40) 0.57±0.29 87.50 176.30
Cichla ocellaris
0.31±0.32 0.45±0.41 Cestoda 43.10 (38.60-48.06) 0.80±0.20 83.80 589.60
Cyphocharax gilbert 0.08±0.16 0.16±0.32 Digenea 13.60 (11.70-15.80) 0.51±0.46 91.60 68.89
Geophagus brasiliensis
0.11±0.18 0.20±0.32 Digenea 52.10 (48.80-55.30) 0.85±0.28 92.60 341.70
Gymnotus carapo
0.13±0.19 0.31±0.46 Nematoda 9.00 (5.90-13.00) 0.52±0.42 94.90 115.70
Hoplosternum littorale
0.13±0.25 0.19±0.37 Digenea 20.40 (17.80-22.60) 0.50±0.45 90.10 355.50
Hypostomus affinis
0.31±0.26 0.43±0.34 Monogenea 42.90 (36.40-48.50) 0.72±0.30 90.90 278.30
Leporinus conirostris
__ __ Digene 27.70 ( 22.70-27.70) __ __ __
Leporinus copelandii 0 0.005±0.03 Myxozoa 2.20( 1.40-2.90) 0.26±0.45 89.60 176.30
Loricariichthys castaneus 0.13±0.20 0.23±0.33 Monogenea 32.90 (28.70-37.40) 0.67±0.41 97.94 24.80
Mugil liza 0.26±0.40 0.32±0.42 Monogenea 9.40 (7.06-12.20) 0.62±0.39 80.60 642.10
Mylossoma aureum
0.14±0.18 0.25±0.32 Nematoda 59.50 (49.60-66.90) 0.92±0.13 __ __
Oligosarcus hepsetus
0 0 Digenea 4.70 ( 3.10-5.40) 0.25±0.44 __ __
Pimelodus maculatus
0.46±0.31 0.51±0.34 Monogenea 43.70 (37.90-490) 0.78±0.17 87.50 556.60
Rhamdia quelen 0.12±0.20 0.19±0.27 Monogenea 9.60 (6.60-13.20) 0.73±0.39 96.10 104.70
Tilapia rendalii __ __ Crustacea 55.10 ( 55.10-55.10) __ __ __
Trachelyopterus striatulus 0.07±0.13 0.11±0.19 Monogenea 60.90 (58.10-63.50) 0.92±0.22 92.60 35.80
Table 3. Brillouin's diversity index (H), Pielou's evenness index (J'), dominant taxon, Bray-Curtis similarity index,
+ +
Berger-Parker dominance index, average taxonomic distinctness (Δ) and variance in taxonomic distinctness (Λ) of
metazoan parasites from Guandu river, State of Rio de Janeiro, Brazil.
197
Neotrop. Helminthol., 5(2), 2011
Hosts Family Mean
length of
hosts (cm)
Formation
of
schools *
Environment§ Trophic
category
Potamodromous Diadromous
Astronotus ocellatus
Cichlidae 45.70 1 2 4 2 2
Astyanax bimaculatus
Characidae 17.50 1 2 4 1 2
Astyanax parahybae
Characidae 5.60 1 2 4 2 2
Centropomus
undecimalis
Centropomidae 140.00 1 3 4 2 1
Cichla ocellaris
Cichlidae 74.00 1 2 4 2 2
Cyphocharax gilbert Curimatidae 12.60 1 2 3 1 2
Geophagus brasiliensis
Cichlidae 28.00 1 2 2 1 2
Gymnotus carapo
Gymnotidae 60.00 2 2 4 1 2
Hoplosternum littorale
Callichthyidae 24.00 1 1 4 2 2
Hypostomus affinis
Loricariidae 39.70 2 3 3 2 2
Leporinus conirostris
Anostomidae 24.50 1 2 3 1 2
Leporinus copelandii Anostomidae 23.00 1 2 3 1 2
Loricariichthys
castaneus
Loricariidae 25.00 2 1 3 2 2
Mugil liza Mugilidae 80.00 1 1 1 2 1
Mylossoma aureum
Characidae 20.00 1 2 3 1 2
Oligosarcus hepsetus
Characidae 23.80 1 2 4 2 2
Pimelodus maculatus
Pimelodidae 36.00 1 2 3 1 2
Rhamdia quelen
Heptapteridae 35.00 2 2 4 1 2
Tilapia rendalii Cichlidae 45.00 1 2 3 2 1
Trachelyopterus
striatulus
Auchenipteridae 20.00 2 1 3 2 1
Table 4. Summary of the data (obtained from Fishbase) on the 20 fish species included in the analyses.
*(1) schooling, (2) non-schooling
§ (1) benthic, (2) benthopelagic, (3) demersal
ƥ (1) detritivores, (2) herbivores, (3) omnivores, (4) carnivores
(1) potamodromous, (2) non-potamodromous
(1) diadromous, (2) non-diadromous
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Received July 14, 2011.
Accepted October 31, 2011.
Correspondence to author/Autor para correspondencia:
José L. Luque
Curso de Pós-Graduação em Ciências Veterinárias,
Universidade Federal Rural do Rio de Janeiro,
Seropédica, Brasil.
Departamento de Parasitologia Animal, Universidade
Federal Rural do Rio de Janeiro, Caixa Postal: 74.508,
Seropédica, Brazil, CEP: 23851-970.
E-mail/correo electrónico:
E-mail: jlluque@ufrrj.br
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