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Seasonal Influence on the Parasite Fauna of a Wild Population of Astronotus
ocellatus (Perciformes: Cichlidae) from the Brazilian Amazon
Author(s): Lígia R. Neves , Felipe B. Pereira , M. Tavares-Dias , and José L. Luque
Source: Journal of Parasitology, 99(4):718-721. 2013.
Published By: American Society of Parasitologists
DOI:
http://dx.doi.org/10.1645/12-84.1
URL:
http://www.bioone.org/doi/full/10.1645/12-84.1
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Seasonal Influence on the Parasite Fauna of a Wild Population of
Astronotus ocellatus
(Perciformes: Cichlidae) from the Brazilian Amazon
L´ıgia R. Neves, Felipe B. Pereira*, M. Tavares-Dias, and Jos ´e L. Luque†,Laborato´rio de Aquicultura e Pesca, Embrapa Amapa´, Caixa Postal 10, CEP 68903-419, Macapa´, AP, Brazil; *Curso de Po´s-Gradua¸ca˜o em Ciˆencias Veterina´rias, Universidade Federal Rural do Rio de Janeiro, CEP 23890-000, Serop´edica, RJ, Brazil; †Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Caixa Postal 74508, CEP 23851-970, Serop´edica, RJ, Brazil. Correspondence should be sent to:luqueufrrj@gmail.com
ABSTRACT: Parasite infracommunities were studied in 202 specimens of
Astronotus ocellatus collected from a freshwater lake in the State of Amapa´, northern Brazil. Relationships between some host attributes (i.e., ontogeny, sex, and body size) and parasite infections were analyzed, but the primary focus was the seasonal variation in the parasite fauna. In total, 6,308,912 parasites belonging to 11 different taxa were found. Protozoa were the most abundant and dominant taxa, but monogeneans, trematode metacercariae, and nematode larvae were also prevalent and abundant. Fish ontogeny had a weak influence on parasite infection rates; juveniles were more parasitized byDolops nanaandPosthodiplostomumsp. The abundances of all parasite species were weakly correlated with host body size (low r2 values), except D. nana, Contracaecum sp., and
Posthodiplostomum sp., which exhibited no correlation between abundance and host body size. Prevalence and abundance were different between flood and drainage seasons for all parasite species, except forD. nanaand the 2 metacercarial species.Astronotus ocellatusmay represent a link in food-web transmissions for parasites because it is used both as definitive and intermediate host. The parasite fauna ofA. ocellatuswas composed primarily of ectoparasites, and this could be considered typical of fishes that inhabit lentic waters. Seasonality was a strong determinant in the parasite community structure.
The Amazon rain forest biome is composed of a series of environments, several of which exhibit marked seasonal variations based on flood and drainage periods (Moraes et al., 2005; Cunha et al., 2010). This seasonal pattern is annual and, together with fish attributes such as sex, age, body size, behavior, and feeding habits, may clearly affect a parasite community structure (Wootten, 1973; Leong and Holmes, 1981; Price and Clancy, 1983; Kennedy and Bush, 1994).
The ‘‘Oscar’’ Astronotus ocellatus (Agassiz, 1831) (Perciformes: Cichlidae) is native to rivers and lakes of the Amazon Basin (Pavanelli, 2000), but it is also found in drainage basins in northeastern, southeastern, and southern Brazil as an introduced species, due to its great economic value (Azevedo et al., 2007) and trophic plasticity (Firouzbakhsh et al., 2011). In nature,A. ocellatusindividuals are commonly found in shaded lentic areas of calm and clear waters, where they can seek shelter under submerged branches (Azevedo et al., 2007; Soares et al., 2008). This species has the capacity to ambush and capture prey, which are mainly small fishes, crustaceans, gastropods, and larvae of aquatic insects (Santos et al., 2006; Azevedo et al., 2007; Soares et al., 2008).
Studies addressing ecological aspects of the parasite fauna from A. ocellatusin Brazilian waters are still scarce, with only 1 survey from a natural habitat of the Amazon (Malta, 1984), and 1 of introduced fishes from the Guandu River in the State of Rio de Janeiro (Azevedo et al., 2007). As a result, the present investigation was conducted to evaluate the seasonal influence on the parasite community structure of a wild population ofA. ocellatuscollected in a lake from the Brazilian Amazon, as well its relationship with some of the host attributes.
Fishes were collected monthly with gillnets in the northern portion of Pracu ´uba Lake (0184304700N, 5084704500W), located in the municipality of Pracu ´uba, State of Amapa´, northern Brazil, and kept in thermal boxes filled with ice prior to examination. The local climate is typical of the tropical rain forest, with maximum rainfall rates in summer and spring (December to May) and minimum rainfall rates in winter and autumn (June to November) (Souza and Cunha, 2010), consisting of 2 seasonal periods (i.e., flooding and drainage). In total, 202 (115 females, 73 males, and 14 juveniles) fishes were sampled over 12 mo (May 2010 to April 2011), 93 during flooding and 109 in the drainage season. Fishes were measured for total length (LT), weighed, sexed, and then examined first for ectoparasites (skin, mucus, eyes, gills, and mouth cavity) and afterward for endoparasites (all visceral organs, blood vessels, and body cavity). The methods described by Eiras et al. (2006) were used to detect and quantify protistan parasites. To quantify metazoan parasites, each organ was dissected separately and washed in running water. All material retained on a 154-lm mesh was examined under a stereomicroscope. Parasites were fixed, preserved, and stained using standard techniques (Amato et al., 1991; Eiras et al., 2006). Voucher specimens were deposited at Instituto de Pesquisas Cient ´ıficas e Tecnolo´gicas do Estado do Amapa´ (IEPA)/ Curadoria das Cole ¸c ˜oes Cient ´ıficas, Fauna do Amapa´ (CCFA) (accession numbers: IEPA 001-P to IEPA 008-P).
The parasitological terminology used throughout follows that described by Bush et al. (1997). Prevalence, abundance, and mean abundance were calculated and used for the analysis of the parasite community. Statistical analyses were performed only for those parasite species with a greater than 10% prevalence rate. The variance-to-mean ratio of parasite abundance (dispersion index) and discrepancy index (Poulin, 1993) were computed using the Quantitative Parasitology 3.0 software program and employed to detect distribution patterns of the parasite infracommunities (Ro´zsa et al., 2000). The following community descriptors were calculated on the parasite infracommunity level: number of parasite individuals (total abundance), species richness, and frequency of dominance (percentage of infracommunities in which a parasite species was numerically dominant) (Magurran, 1988; Rohde et al., 1995).
Linear regression analysis was performed to evaluate the association between fish weight and LT. One-way ANOVA, followed by a post hoc Tukey test, was used to compare the LTvalues among male, female, and juveniles ofA. ocellatus(Zar, 1999). Possible differences in prevalence, abundance, and species richness among juvenile, male, and female fishes were evaluated with ANOVA, followed by a post hoc Tukey test (Zar, 1999). Abundance and species richness were log-transformed (log10[xþ 1]), and prevalence was arcsine-transformed (Zar, 1999). Seasonal variations in prevalence were evaluated by a logistic regression (Dohoo et al., 2003); the same variations in abundance and species richness were evaluated by a Poisson regression model (Dohoo et al., 2003). A linear regression analysis was employed to evaluate the relationship between parasite abundance (log-transformed) and fish LT, as well species richness (log-transformed) and fish LT (Zar, 1999). All means are followed by standard deviation (6SD) values. Statistical tests were performed using the SYSTATt and R program with the Vegan package included (Wilkinson, 1990; Oksanen et al., 2007). The significance level was set to 5% (P,0.05).
DOI: 10.1645/12-84.1
Fish weight was positively associated with LT(r 2
¼0.8,P,0.001). Females (LT¼2,402 6278 mm, 1,600 to 2,900 mm) were larger than males (LT¼2,2866287 mm, 1,700 to 2,900 mm) (P¼0.02) and juveniles (LT¼2,1726404 mm, 1,500 to 2,920 mm) (P¼0.01); males and juveniles did not differ in body size (P¼0.36).
In total, 6,308,912 parasites were collected. The specimens belonged to 11 different taxa: 3 Protozoa, 3 Monogenea, 2 Digenea metacercariae, 1 larval Nematoda, 1 Branchiura, and 1 Hirudinea (Table I). Among the entire fish sample, 92.0% were parasitized by at least 1 species. The protist
Ichthyophthirius multifiliis (Fouquet, 1866) (Ciliophora: Ichthyophthir-iidae) was the most prevalent, abundant, and dominant species. Hirudinea species had the lowest prevalence rate and was the only parasite taxon excluded from the statistical analysis. The least abundant species was
Dolops nanaLemos de Castro, 1950 (Branchiura: Argulidae). All parasite species exhibited an aggregated distribution pattern (Table I), with mean richness of 5.562.1 (0 to 9) per fish.
Species richness did not differ among juveniles (P¼0.60), male (P¼
0.94), and female (P¼0.98) fishes, nor between seasons (P¼0.18).Dolops nana was more prevalent in juveniles than in adults (P ¼ 0.02);
Posthodiplostomumsp. was more prevalent (P¼0.02) and abundant (P
¼ 0.002) in juveniles than in adults. All protists and the nematode
Contracaecumsp. were more abundant and prevalent during the flood season (Table II); all monogenean species were more abundant and prevalent during the drainage season (Table II); the infection rates of the 2 digenean metacercariaeHerpetodiplostomumsp. andPosthodiplostomum
sp., and of the crustaceanD. nanawere not seasonally different (Table II). Fish LTwas weakly and positively correlated with the abundance for all parasite species, except forContracaecumsp.,D. nana, and Posthodiplos-tomumsp. (Table II), and LTwas positively correlated (weak correlation) with species richness (r2
¼0.028,P¼0.017).
This is the first ecological survey reporting the complete parasite fauna ofA. ocellatusfrom a natural habitat in Brazil, and its seasonal variations. Moreover, this is the first record ofIchthyophthirius multifiliis, Pscinoo-dinium pillulare (Schaperclaus, 1954) (Dinoflagellida), Dolops nana, metacercariae from Posthodiplostomum and Herpetodiplostomum, and the protist genus Trichodina parasitizing A. ocellatus in Brazil. The component community of parasites in the present work exhibited an
aggregated pattern of distribution, which is very common among parasite component communities (Crofton, 1971; Poulin, 1993), mitigating harm to host populations and reducing interspecific competition among parasites (Ewald, 1995; Zuben, 1997).
It is clear that protists, especiallyI. multifiliisandP. pillulare, exhibited a much higher parasite burden than the other species, perhaps due to the small size, low specificity, and high reproductive and infection rates among such parasites (Pavanelli et al., 2008; Tavares-Dias et al., 2001). Furthermore, aquatic environments favor the dispersion and survival of those ectoparasites with free-swimming stages during some phase of the life cycle (Dogiel, 1961; Malta, 1984). That is why adult monogenean and digenean metacercariae were also prevalent. Malta (1984) analyzed the crustacean parasites of a wild population ofA. ocellatusin the Amazon; he found 3Dolopsspp. and 1Argulussp., with low prevalence values similar to that found forD. nanain the present study. In contrast, Azevedo et al. (2007) reported the monogeneanGusseivasp. as the most prevalent and dominant species fromA. ocellatusintroduced in a river in Rio de Janeiro, whereas immature forms such as nematode larvae ofContracaecumsp. and the cystacanth ofPolymorphussp. were much less prevalent; protists were not studied. If we exclude the protists from the present work, the monogeneanGussevia asotaKritsky, Tatcher and Boeger, 1989 becomes the most prevalent and dominant species, followed by the 2 metacercariae species, and then byContracaecumsp. larvae. Monogeneans of the genus
Gusseviaare well adapted to this host (Azevedo et al., 2007; Abdallah et al., 2008). In addition, the lentic habitat preferred byA. ocellatusfavors the colonization by ectoparasites, and also the encounter between their free-swimming larvae and the host (Dogiel, 1961). Hirudinean and crustaceans seem to be the least abundant species in the parasite community structure of A. ocellatus, as reported here, and also by Azevedo et al. (2007).
Sex differences did not appear to influence the parasite community structure, probably because male and female fishes share the same type of habitat and have similar feeding habits and behavior (Braga, 1962). However,D. nana was more prevalent in juvenile fishes, and Posthodi-plostomumsp. was more prevalent and also more abundant in juvenile fishes. Young individuals of A. ocellatus are more vagile than adults TABLEI. Site of infection (SI), prevalence (Prev.), mean6SD abundance (MA), variance-to-mean ratio (ID), index of discrepancy (D), and frequency of dominance (FD) of the parasites collected fromAstronotus ocellatusin State of Amapa´, northern Brazil.
Parasite species SI Prev. (%) MA ID D FD (%)
Protozoa
Ichthyophthirius multifiliis Gills 88.6 28,824627,536 7,073.5 * 87.2
Piscinoodinium pillulare Gills 54.5 2,31065,290 9,458.0 * 2.1
Trichodinasp. Gills 10.4 26.36109 458.0 0.93 0
Monogenea
Gussevia asota Gills 41.6 4.4614.4 47.0 0.84 0
Gussevia astronoti Gills 68.3 4.566.9 10.5 0.66 0
Gussevia rogersi Gills 87.6 21.7625.6 10.5 0.66 1.6
Digenea
Herpetodiplostomumsp. metacercariae Gills 70.3 5.5610.3 19.2 0.69 0
Posthodiplostomumsp. metacercariae Gills 59.4 2.263.8 6.5 0.69 0
Nematoda
Contracaecumsp. larvae Mesenteries 53.0 32.3684.4 220.5 0.86 1.1
Branchiura
Dolops nana Gills 15.3 0.561.5 4.3 0.89 0
Hirudinea
Glossiphoniidae gen. sp. Gills 1.0 21.7625.6 1.6 0.98 0
* Sample size too large, precluding calculation.
(Braga, 1962), which may increase the probability of encounter between these individuals andD. nanaandPosthodiplostomumsp. in that case.
Parasite abundance and species richness increased with the increase of host body size for most of the species, which agrees with some authors that consider hosts as islands for parasite colonization (Kellog, 1913; Janzen, 1968, 1973), using the analogy from island biogeography theory (MacArthur and Wilson, 2001). However, these correlations were very weak, as evidenced by extremely low values ofr2(body size explained less than 10% of variance on parasite abundance and species richness). Thus, this indicates that factors other than host body size are more important determinants of variations of abundance and species richness among the host population. This also explains the lack of relationship between abundance ofContracaecumsp.,D. nana, andPosthodiplostomumsp. and host body size. Diet composition may be important forContracaecumsp. infection, since it is a heteroxenous nematode with hosts related to food-web links; in the case ofD. nanaandPosthodiplostomumsp., which exhibit direct life cycles, environmental conditions could influence infection patterns.
Pracu ´uba Lake is located in the domain of an Amazon tropical rain forest, which is characterized by 2 distinct seasons during a year, i.e., 1 flood period when the lakes are expanded and 1 drainage period when they remain much more reduced (Souza and Cunha, 2010). Our data show an accentuated seasonal influence in the parasite community structure, but this seasonality affects each parasite group in different ways. First, species richness was statistically similar between seasons, perhaps indicating that these parasites can, at least, infect the host independent of seasonal variations; parasite prevalence and abundance were seasonally different. Second, all protozoan species andContracaecumsp. were more abundant and prevalent during flood season; in the case of protists, it is probable that chemical and physical variables of water (i.e., temperature, dissolved oxygen, pH, and turbulence) act on their demographic patterns (Pavanelli et al., 1997), since the intense variation in water levels at the lake may affect its physicochemical properties. Seasonal variation in the infection patterns of Contracaecum sp. may be related to the abundance of intermediate hosts for this parasite (i.e., small crustaceans), which are eaten by the fish. Furthermore, a decrease in water volume is known to cause nutritional imbalances, reducing the production of food in general (Madanire-Moyo et al., 2011). Lastly, the infection rates of monogenean species were higher during the drainage period; parasite infection is favored by reduced water levels, concentrating parasites and hosts, and increasing the probability of infection, since they have a simple direct life cycle (Madanire-Moyo et al., 2011). The 2 larval digeneans exhibited similar prevalence and abundance between seasons, probably because they have a complex life cycle, with low specificity of intermediate hosts and asexual reproduction, where a single miracidium results in a large number
of free-swimming cercariae. This complexity of life cycle may overshadow seasonal variations in that case.
This ecological survey is the first pass to understand patterns and processes of parasite infections in wild populations of A. ocellatus. Considering the complexity and diversity of the Amazonian ecosystems that are occupied by this fish, similar investigations need to be conducted in the future for a better understanding of the factors that determine these patterns and processes.
Felipe B. Pereira was supported by a graduate fellowship from the CAPES (Coordena ¸ca˜o de Aperfei ¸coamento de Pessoal de N ´ıvel Superior). Jos ´e L. Luque was supported by a fellowship from the CNPq (Conselho Nacional de Desenvolvimento Cient ´ıfico e Tecnolo´gico, Brazil).
LITERATURE CITED
ABDALLAH, V. D., R. K. AZEVEDO,ANDJ. L. LUQUE. 2008. Notes on the
morphology of two species ofGusseviaKohn & Paperna (Monoge-nea: Dactylogyridae) parasitic on Astronotus ocellatus (Agassiz) (Perciformes: Cichlidae) from Brazil. Pan-American Journal of Aquatic Sciences3:101–104.
AMATO, J. F. R., A. B. WALTER,ANDS. B. AMATO. 1991. Protocolo para
laborato´rio. Coleta e Processamento de Parasitas do Pescado, 1st ed. Imprensa Universita´ria Universidade Federal Rural do Rio de Janeiro, Serop ´edica, Rio de Janeiro, Brazil, 81 p.
AZEVEDO, R. K., V. D ABDALLAH,AND J. L. LUQUE. 2007. Ecologia da
comunidade de metazoa´rios parasitos do apaiariAstronotus ocellatus
(Cope,1872) (Perciformes: Cichlidae) do Rio Guandu, Estado do Rio de Janeiro, Brasil. Revista Brasileira Parasitologia Veterina´ria16:15– 20.
BRAGA, R. A. 1962. Apaiari ou acara´-a ¸cu,Astronotus ocellatus ocellatus
Spix. Departamento Nacional de Obras Contra a Seca, Fortaleza, Ceara´, Brazil, 2 p.
BUSH, A. O., K. D. LAFFERTY, J. M. LOTZ,ANDA. W. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology83:575–583.
CROFTON, H. D. 1971. A quantitative approach to parasitism. Parasitology
62:179–193.
CUNHA, A. C., E. B. SOUZA,ANDH. F. A. CUNHA. 2010. Tempo clima e recursos h ´ıdricos: Resultados do projeto REMETAP no estado do Amapa´, 1st ed. Instituto de Estudos e Pesquisas do Amapa´, Macapa´, Amapa´, Brazil, 216 p.
DOGIEL, V. A. 1961. Ecology of the parasites of freshwater fishes. In
Parasitology of fishes, V. A. Dogiel, G. K. Petrushevsky, and Y. I. Polyanski (eds.). University Press, Leningrad, Russian Soviet Federative Socialist Republic, p. 1–47.
DOHOO, I., W. MARTIN,ANDH. STRYHN. 2003. Veterinary epidemiologic
research, 1st ed. AVC Inc., Charlottetown, Prince Edward Island, Canada, 865 p.
TABLEII. Regression analysis between fish LT(mm) and parasite abundance (log transformed), differences in prevalence (Prev.), and mean abundance6 SD (MA) during the flood and drainage seasons, evaluated by logistic and Poisson models, respectively, for the parasites collected fromAstronotus ocellatusin State of Amapa´, northern Brazil.
Parasite species
Fish LT3abundance Drainage season Flood season
Logistic Poisson r2* P* Prev. (%) MA Prev. (%) MA P P Ichthyophthirius multifiliis 0.073 0.047 82 11,311621,500 97 41,394628,771 0.003 ,0.001 Piscinoodinium pillulare 0.044 0.049 53 1,42763,085 72 3,04866,515 0.043 ,0.001 Trichodinasp. 0.015 0.044 2 156121 21 546108 ,0.001 ,0.001 Gussevia asota 0.097 0.048 57 7618 23 163 ,0.001 ,0.001 Gussevia astronoti 0.061 0.032 66 1266 44 466 0.032 ,0.001 Gussevia rogersi 0.052 0.001 95 25630 82 13618 ,0.001 ,0.001 Herpetodiplostomumsp. 0.047 0.050 73 5611 67 568 0.409 0.269 Posthodiplostomumsp. 0.001 0.055 60 262 59 365 0.859 0.346 Contracaecumsp. 0.003 0.970 38 13659 71 546102 ,0.001 0.001 Dolops nana 0.037 0.600 14 161 17 161 0.462 0.499
EIRAS, J. C., R. M. TAKEMOTO,ANDG. C. PAVANELLI. 2006. M ´etodos de
estudo e t ´ecnicas laboratoriais em parasitologia de peixes, 2nd ed. Editora da Universidade Estadual de Maranga´, Maringa´, Parana´, Brazil, 199 p.
EWALD, P. W. 1995. The evolution of virulence: A unifying link between
parasitology and ecology. Journal of Parasitology81:659–669. FIROUZBAKHSH, F., F. NOORI, M. K. KHALESI,ANDK. JANI-KHALIL. 2011.
Effects of a probiotic, protexin, on the growth performance and hematological parameters in the Oscar (Astronotus ocellatus) finger-lings. Fish Physiology and Biochemistry37:833–842.
JANZEN, D. H. 1968. Host plants as islands in evolutionary and contemporary time. American Naturalist102:592–595.
———. 1973. Host plants as islands. II. Competition in evolutionary and contemporary time. American Naturalist107:786–790.
KELLOG, V. L. 1913. Distribution and species forming of ecto-parasites. American Naturalist47:129–158.
KENNEDY, C. R.,ANDA. O. BUSH. 1994. The relationship between pattern and scale in parasite communities: A stranger in a strange land. Parasitology109:187–196.
LEONG, T. S.,ANDJ. C. HOLMES. 1981. Communities of metazoan parasites
in open water fishes of Cold Lake, Alberta. Journal of Fish Biology
18:693–713.
MACARTHUR, R. M., AND E. O. WILSON. 2001. The theory of island
biogeography, 30th ed. Princeton University Press, Princeton, New Jersey, 224 p.
MADANIRE-MOYO, G. N., M. M. MATLA, P. A. S. OLIVIER,ANDW. J. LUUS -POWELL. 2011. Population dynamics and spatial distribution of
monogeneans on the gills of Oreocrhomis mossambicus (Peters, 1852) from two lakes of the Limpopo River system, South Africa. Journal of Helminthology85:146–152.
MAGURRAN, A. E. 1988. Ecological diversity and its measurement, 1st ed. Princeton University Press, Princeton, New Jersey, 179 p.
MALTA, J. C. O. 1984. Os peixes de um lago de va´rzea da Amaz ˆonia Central (Lago Janauaca´, Rio Solim ˜oes) e suas rela ¸c ˜oes com os crusta´ceos ectoparasitas (Branchiura: Argulidae). Acta Amaz ˆonica
14:355–372.
MORAES, B. C., J. M. N. COSTA, A. L. COSTA,ANDM. H. COSTA. 2005. Spatial and temporal variation in the precipitation in the State of Parana´. Acta Amazonica35:207–214.
OKSANEN, J., R. KINDT, P. LEGENDRE, R. B. O’HARA, AND M. H. H. STEVENS. 2007. Vegan: Community ecology package. R package
version 1.8-8. Available at: http://r-forge.r-project.org/projects/ vegan/. Accessed 5 June 2012.
PAVANELLI, G. C. 2000. Sanidade de peixes, ra˜s, crusta´ceos e moluscos.In
Aquicultura no Brasil: Bases para um desenvolvimento sustenta´vel, W. C. Velenti, C. R. Poli, J. A. Pereira, and J. R. Borghetti (eds.). CNPq, Bras ´ılia, Distrito Federal, Brazil, p. 197–246.
———, J. C. EIRAS, AND R. M. TAKEMOTO. 2008. Doen ¸cas de peixes:
Profilaxia, diagno´stico e tratamento, 3rd ed. Editora da Universidade Estadual de Maringa´, Maringa´, Parana´, Brazil, 317 p.
———, M. H. MACHADO,ANDR. M. TAKEMOTO. 1997. Fauna helm ´ıntica de peixes do rio Parana´, regia˜o de Porto Rico, Parana´.InA plan ´ıcie de inunda ¸ca˜o do alto rio Parana´: Aspectos f ´ısicos, biolo´gicos e socioeconomicos, E. A. M. Vazzoler, A. A. Agostinho, and N. S. Hahn (eds.). Editora da Universidade Estadual de Maringa´, Maringa´, Parana´, Brazil, p. 307–329.
POULIN, R. 1993. The disparity between observed and uniform
distribu-tions: A new look at parasite aggregation. International Journal for Parasitology23:937–944.
PRICE, P. W.,ANDK. M. CLANCY. 1983. Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology69:449– 454.
ROHDE, K., C. HAYWARD,ANDM. HEAP. 1995. Aspects of the ecology of
metazoan ectoparasites of marine fishes. International Journal for Parasitology25:945–970.
RO´ZSA, L., J. REICZIGEL,ANDG. MARJOROS. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology86:228–232.
SANTOS, G. M., E. J. G. FERREIRA,ANDJ. A. S. ZUANON. 2006. Peixes
comerciais de Manaus, 1st ed. IBAMA ProVa´rzia, Manauas, Amazonas, Brazil, 144 p.
SOARES, M. G. M., E. L. COSTA, F. K. SIQUEIRA-SOUZA, H. D. B. ANJOS, K. C. YAMAMOTO,ANDC. E. C. FREITAS. 2008. Peixes de lagos do m ´edio
Rio Solim ˜oes, 1st ed. Editora da Universidade do Amazonas, Manaus, Amazonas, Brazil, 175 p.
SOUZA, E. B.,ANDA. C. CUNHA. 2010. Climatologia de precipita ¸ca˜o no estado do Amapa´ e mecanismos clima´ticos de grande escala. In
Tempo, clima e recursos h ´ıdricos: Resultados do Projeto REMETAP no estado do Amapa´, A. C. Cunha, E. B. Souza, and H. F. A. Cunha (eds.). Instituto de Estudos e Pesquisas do Amapa´, Macapa´, Amapa´, Brazil, p. 177–195.
TAVARES-DIAS, M., F. R. MORAES, M. L. MARTINS,ANDS. N. KRONKA.
2001. Fauna parasita´ria de peixes oriundos de ‘‘pesque-pagues’’ do munic ´ıpio de Franca, Sa˜o Paulo, Brasil. II. Metazoa´rios. Revista Brasileira de Zoologia18:81–95.
WILKINSON, L. 1990. SYSTAT: The system for statistics, 1st ed. Systat
Inc., Evanston, Illinois, 822 p.
WOOTTEN, R. 1973. The metazoan parasite-fauna of fish from Hannigfield Reservoir, Essex, in relation to features of the habitat and host populations. Journal of Zoology171:323–331.
ZAR, J. H. 1999. Biostatistical analysis, 4th ed. Prentice Hall, Upper
Saddle River, New Jersey, 960 p.
ZUBEN, C. J. V. 1997. Impica ¸c ˜oes da agrega ¸ca˜o espacial de parasitas para a
din ˆamica populacional nna intera ¸ca˜o hospedeiro-parasita. Revista de Sa ´ude P ´ublica31:523–530.
