Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil

Diversidade dos parasitos de peixes da planície de inundação do Alto Rio Paraná, Brasil

Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil

Diversidade dos parasitos de peixes da planície de inundação do Alto Rio Paraná, Brasil

Takemoto, RM.^*; Pavanelli, GC.; Lizama, MAP.; Lacerda, ACF.; Yamada, FH.; Moreira, LHA.; Ceschini, TL.; Bellay, S.

Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais - PEA, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura - Nupélia, Laboratório de Ictioparasitologia, Universidade Estadual de Maringá - UEM, Av. Colombo, 5790, CEP 87020-900, Maringá, PR, Brazil

ABSTRACT

The aim of the present study was to provide a current survey of the species of parasites found in the Upper Paraná River floodplain, as well as to investigate which strategies and mechanisms used by parasites, are favored and which environmental factors influence the parasite community in the studied environments. During a seven-year period from February 2000 to September 2007, 3,768 fish belonging to 72 species were collected and analyzed for the purpose of studying the parasite fauna. A total of 337 species of parasites were reported, including 12 new descriptions: one myxosporid, Henneguya paranaensis Eiras, Pavanelli and Takemoto, 2004; eight monogeneans, Kritskyia annakohnae Boeger, Tanaka and Pavanelli, 2001; Kritskyia boegeri Takemoto, Lizama and Pavanelli, 2002; Kritskyia eirasi Guidelli, Takemoto and Pavanelli, 2003; Demidospermus labrosi França, Isaac, Pavanelli and Takemoto, 2003; Demidospermus mandi França, Isaac, Pavanelli and Takemoto, 2003; Pseudovancleaveus paranaensis França, Isaac, Pavanelli and Takemoto, 2003; Tereancistrum curimba Lizama, Takemoto and Pavanelli, 2004 and Tereancistrum toksonum Lizama, Takemoto and Pavanelli, 2004; two digeneans, Sanguinicola platyrhynchi Guidelli, Isaac and Pavanelli, 2002 and Dadayius pacupeva Lacerda, Takemoto and Pavanelli, 2003 and one cestode, Nomimoscolex pertierrae Chambrier, Takemoto and Pavanelli, 2005. In addition, several other species were reported for the first time in new hosts or in the floodplain. Monogeneans presented the highest number of species, followed by digeneans. The infection site with the highest species richness was the intestine, with 127 species.

Keywords: ichthyoparasites, biodiversity, helminthes, crustaceans, parasite ecology.

RESUMO

O objetivo do presente trabalho foi realizar um novo levantamento das espécies de parasitos encontradas na planície de inundação do Alto Rio Paraná, bem como investigar quais estratégias e mecanismos utilizados pelos parasitos são mais favorecidos e quais fatores ambientais estão influenciando a comunidade parasitária nos ambientes estudados. Durante o período de fevereiro de 2000 a setembro de 2007, 3.768 espécimes de peixes pertencentes a 72 espécies foram coletados e analisados, visando o estudo da fauna parasitária. Até o momento foram registradas, 337 espécies de parasitos, sendo 12 novas espécies: uma de mixosporídeo, Henneguya paranaensis Eiras, Pavanelli e Takemoto, 2004; oito de monogenéticos, Kritskyia annakohnae Boeger, Tanaka e Pavanelli, 2001; Kritskyia boegeri Takemoto, Lizama e Pavanelli, 2002; Kritskyia eirasi Guidelli, Takemoto e Pavanelli, 2003; Demidospermus labrosi França, Isaac, Pavanelli e Takemoto, 2003; Demidospermus mandi França, Isaac, Pavanelli e Takemoto, 2003; Pseudovancleaveus paranaensis França, Isaac, Pavanelli e Takemoto, 2003; Tereancistrum curimba Lizama, Takemoto e Pavanelli, 2004 e Tereancistrum toksonum Lizama, Takemoto e Pavanelli, 2004; duas de digenéticos, Sanguinicola platyrhynchi Guidelli, Isaac e Pavanelli, 2002 e Dadayius pacupeva Lacerda, Takemoto e Pavanelli, 2003 e uma de cestóide, Nomimoscolex pertierrae Chambrier, Takemoto e Pavanelli, 2005. Além dessas novas espécies, várias outras foram registradas pela primeira vez em novos hospedeiros ou na planície. O grupo dos monogenéticos foi o que apresentou maior número de espécies encontradas, seguido pelos digenéticos. O intestino foi o sítio de infecção que apresentou a maior riqueza, com 127 espécies.

Palavras-chave: ictioparasitos, biodiversidade, helmintos, crustáceos, ecologia de parasitos.

1. Introduction

Floodplains are ecosystems that experience recurrent floods, favoring certain adaptations of the organisms inhabiting them and resulting in the presence of communities with characteristic structures and functions (Junk, et al. 1989). Floods can alter the population dynamics of the ichthyofauna, as well as their physiological and biological conditions, thereby influencing the structure and composition of the parasite fauna. In addition, chemical and physical variables of the water such as dissolved oxygen, temperature and turbulence can contribute to the emergence and increases in the demography of some parasite species (Pavanelli et al., 1997).

Luque and Poulin (2008) reported that differences in the taxonomic diversification of the parasite assemblages of different fish species were mainly related to the environment (higher values in benthic-demersal species), trophic level (positive correlation) and temperature (positive correlation for all groups of parasites in freshwater fishes). Therefore, the Upper Paraná River floodplain, characterized by a wide variety of habitats and species, favors the occurrence of a great diversity of fish parasites.

Lizama et al. (2006a) and Yamada et al. (2007) found higher parasitism indexes of monogeneans and digeneans in open lagoons in the Upper Paraná River floodplain. The authors explain that the presence of morphological adaptations, such as eggs with adhesive appendices that allow for attachment to a substrate, could explain the higher number of monogeneans. Meanwhile, digeneans could be more prevalent in these environments due to the great quantity of intermediate hosts in open lagoons. Studying Pseudoplatystoma corruscans (Spix and Agassiz, 1829) and Schizodon borelli (Boulenger, 1900), Machado et al. (1995) observed that fish were more parasitized by cestodes in semi-lentic environments and by nematodes in lentic environments, probably because of the great variety of prey and availability of shelter.

The parasite fauna of fish from the Upper Paraná River floodplain was previously detailed by Pavanelli et al. (1997, 2004). The present study investigates which reproductive strategies and dispersion mechanisms are favored, and which environmental factors (internal and external) influence the parasite community. In addition, this paper complements previous studies presenting an updated list of species of parasites and hosts.

2. Materials and Methods

All fish were collected in the floodplain of the Upper Paraná River, Brazil, from February 2000 to September 2007. Fishes were captured using gill nets, and parasites were collected with the aid of a stereoscopic microscope. The eyes, skin, fins, gills, nostrils and mouth cavity of the selected individuals were studied for ectoparasites. The body cavity was opened to examine the liver, stomach, pyloric caeca, intestine and gonads microscopically for endoparasites (see Eiras et al., 2006). The literature used to identify the parasites included original descriptions. Quantitative information on the prevalence and intensity of infection by different parasites and on parasite community descriptors have been published previously for the following fish species: Prochilodus lineatus (Valenciennes, 1837) (Takemoto et al., 2002; Eiras et al., 2004; Lizama et al., 2004; 2005; 2006a, b); Acestrorhynchus lacustris (Lütken, 1875) (Carvalho et al., 2003); Iheringichthys labrosus (Lütken, 1874) (França et al., 2003); Hemisorubim platyrhynchos (Valenciennes, 1840) (Guidelli et al., 2003a); Leporinus spp. (Guidelli et al., 2003b; 2006); Metynnis maculatus (Kner, 1858) (= M. lippincottianus) (Lacerda et al., 2003); A. lacustris, S. borellii, P. lineatus, Serrasalmus marginatus Valenciennes, 1837 and S. maculatus Kner, 1858 (Lacerda et al., 2007); Potamotrygon spp. (Lacerda et al., 2008; 2009); Hoplias aff. malabaricus (Bloch, 1794), Satanoperca pappaterra (Heckel, 1840), Plagioscion squamosissimus (Heckel, 1840), Crenicichla britskii Kullander, 1982, Cichla monoculus Spix and Agassiz, 1831 (= C. kelberi) and Cichlasoma paranaense Kullander, 1983 (Aoyama et al., 2005); P. squamosissimus (Tavernari et al., 2005); P. corruscans (Chambrier et al., 2006); Loricariichthys platymetopon Isbrücker and Nijssen, 1979 (Ferrari et al., 2007); S. papaterra (Yamada et al., 2007) and Cichla spp. (Yamada et al., 2008).

3. Results

We collected and analyzed 3,768 fish belonging to 72 species. A total of 337 species of parasites were reported (^{Appendix 1}), including the description of 12 new species: one myxosporid, Henneguya paranaensis Eiras, Pavanelli and Takemoto, 2004; eight monogeneans, Kritskyia annakohnae Boeger, Tanaka and Pavanelli, 2001; K. boegeri Takemoto, Lizama and Pavanelli, 2002; K. eirasi Guidelli, Takemoto and Pavanelli, 2003; Demidospermus labrosi França, Isaac, Pavanelli and Takemoto, 2003; D. mandi França, Isaac, Pavanelli and Takemoto, 2003; Pseudovancleaveus paranaensisFrança, Isaac, Pavanelli and Takemoto, 2003; Tereancistrum curimba Lizama, Takemoto and Pavanelli, 2004 e T. toksonum Lizama, Takemoto and Pavanelli, 2004; two digeneans, Sanguinicola platyrhynchi Guidelli, Isaac and Pavanelli, 2002 and Dadayius pacupeva Lacerda, Takemoto and Pavanelli, 2003 and one cestode, Nomimoscolex pertierrae Chambrier, Takemoto and Pavanelli, 2006.

In total, 12 groups of parasites were collected, mainly Platyhelminthes (Monogenea, Digenea and Cestoda) and Nematoda. Among the groups of parasites found, monogeneans presented the greatest number of species with 82 (Figure 1), including species that parasitized gills, nasal fossae and urinary bladder. Among digeneans and nematodes, which also presented high numbers of species, adults and larval forms were observed. Sixty-nine species of digeneans were recorded, with 28 reported as larvae. Nine out of 66 species of nematodes were larvae, and Contracaecum sp. (Anisakidae) was the most common.

The main infection site was the intestine, which was parasitized by 127 different species of parasites, including digeneans, cestodes, nematodes and acanthocephalans. These species were always found as adults (Figure 2). The gills presented the second highest number of species (91), mainly monogeneans and copepods. In the mesentery, the helminthes were mainly larval forms.

The parasitic protozoa are usually classified according to their motility mechanisms. These include amoeboid, flagellated, and ciliated forms. Among the protozoa, three species of Phylum Sarcomastigophora were reported: Trypanosoma guairaensis Eiras, Rego and Pavanelli, 1989, T. scrofae Eiras and Pavanelli, 1989 and T. nupelianus Eiras, Rego and Pavanelli, 1990, parasitizing Megalancistrus parananus (Peters, 1881), P. lineatus and Rhineleps aspera Spix and Agassiz, 1829, respectively.

The myxozoans, which until recently were considered protozoans, are now considered metazoans. The genus Henneguya was reported in the floodplain, with the description of a new species, H. paranaensis Eiras, Pavanelli and Takemoto, 2004.

During this period, the class Monogenea had the largest number of new species.

Digeneans presented the second highest number of species and low host specificity. Some species that parasitize fish in the larval stage, such as Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) (probably introduced), were reported in nine different species of hosts: H. aff. malabaricus, S. pappaterra, P. squamosissimus, C. britskii, Cichla kelberi Kullander and Ferreira, 2006 (= Cichla monoculus), C. paranaense, Hypostomus regani (Ihering, 1905), S. borellii, and Auchenipterus osteomystax (Miranda Ribeiro, 1918).

Nematodes also generally have low host specificity, such as the nematode Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas and Pereira, 1928, which was reported in nine different species of hosts (S. marginatus, S. maculatus, S. borelli, H. aff. malabaricus, M. lippincottianus, Leporinus elongatus Valenciennes, 1850, L. obtusidens (Valenciennes, 1837), L. lacustris Amaral Campos, 1945 and P. corruscans) in the current study. However, Moravec (1998) had already registered this species in more than 40 species of fish from the Neotropical region. Another species of nematode that presented low specificity was the larvae of Contracaecum sp., which was already reported in 17 different species of hosts. This species deserves special attention because it parasitizes fish as larvae, using it as an intermediate host and then presenting zoonotic potential.

During this period only one species of cestode was described, Nomimoscolex pertierrae Chambrier, Takemoto and Pavanelli, 2006. In previous studies, the occurrence of this group was observed mainly in Siluriform fishes and with high host specificity. Considering only the fish "pintado", P. corruscans and "jaú", Zungaro zungaro (Humboldt, 1821) (= Paulicea luetkeni), six species of proteocephalideans were reported in each species, all adults. Larval stages of Cyclophyllidea were also reported, including Valipora campylancristrota (Wedl, 1855) in P. lineatus, Pimelodus maculatus Lacépède, 1803 and Hoplosternum littorale (Hancock, 1828), all parasitizing the gall bladder. In the stingrays Potamotrygon motoro (Müller and Henle, 1841) and P. falkneri Castex and Maciel, 1963, cestodes of orders Tetraphyllidea, Acanthobothrium regoi Mayes, Brooks and Thorson, 1981, Rhinebothrium paratrygoni Rego and Dias, 1976, Potamotrygonocestus travassosi Rego, 1979 and Trypanorhyncha, Paroncomegas araya (Woodland, 1934) were reported.

Among the acanthocephalans, Quadrigyrus machadoi Fabio, 1983 presented low specificity, occurring in seven different species of hosts (P. motoro, P. falkneri, H. aff. malabaricus, Gymnotus carapo Linnaeus, 1758, P. maculatus, H. platyrhynchos and C. kelberi). Acanthocephalans of the genus Quadrigyrus occurred as adults and larvae.

The main families of Copepoda reported in the floodplain were Ergasilidae and Vaigamidae, parasitizing the branchial arcs and the nostrils, respectively. In addition, copepods of family Therodamasidae were observed parasitizing the branchial arcs of P. maculatus. This family is characterized by an anterior structure that penetrates into the tissues of the branchial arcs of the host, causing considerable lesions. This is the first record of this family in the Upper Paraná River floodplain.

Branchiura, Isopoda, Hirudinea, Pentastomida and Acarina presented low species diversity.

4. Discussion

In previous studies, Takemoto et al. (2004) reported 184 species of fish parasites in the Upper Paraná River floodplain. Currently, 337 species are known. This augmentation of species richness is due to the increase in the quantity of studies conducted in recent years, which have included different species of fish.

In addition to the previously described species, several other species were reported for the first time in the floodplain. In P. maculatus, for example, we reported the first copepods of the family Therodamasidae, and this is also the first record for the Upper Paraná River basin.

Myxozoa is a group of parasitic organisms for which the basic knowledge regarding phylogenetic affinities and life cycles has changed dramatically in the last two decades. The myxozoans were included as unicellular protozoans. However, according to Smothers et al. (1994) and Siddall et al. (1995), recent evidence clearly indicates that myxozoans are true metazoans. In the Upper Paraná River floodplain, only the genus Henneguya was observed.

Monogenea is the group that has presented the greatest number of species so far. Monogeneans are a diverse group of parasites that exhibit a relatively high degree of host specificity when compared to other groups of parasites. Because monogeneans do not represent a zoonotic problem for humans, and because most of them are not pathogenic, very little is known about the biology of most species (Bush et al., 2001).

The number of species recorded in this class tends to increase in the floodplain, since previous studies have already shown its high species richness in every species of host.

Among the groups of parasites found, digeneans presented the second highest number of species (69), including adults and larval stages. Some species of digeneans presented low specificity and were mainly present in larval forms. As an example we can cite D. (A.) compactum, a digenean that, in the metacercaria stage, parasitizes the eyes of fish. This parasite was probably introduced to the floodplain with P. squamosissimus. Despite being almost an obligatory parasite of this species, we noticed that in recent years, the number of species of parasitized hosts has increased considerably. We recorded this digenean in nine species of fish, showing low specificity and rapid adaptation to the new environment.

The conservation of the native fauna depends on research to increase knowledge regarding which parasites spread globally (Font, 2003). The goal of ecologists is not only to document the distribution of parasites, but also to determine methods by which parasites can disperse to new areas. Through the determination of the groups of parasites that can establish themselves in a new environment, it is possible to determine which strategies of reproduction are favored. Improved understanding of these mechanisms of dispersion can increase the chances of limiting the dispersion of certain parasites (Font, 2003).

Digeneans represent the highest number of species because fish can act as intermediate hosts, harboring larval stages, and also as definitive hosts, harboring adult forms. Moreover, the majorities of the fish examined here occupy intermediate levels in the food chain and can be parasitized by both forms.

Another larvae that showed low specificity was the nematode Contracaecum sp. This species belongs to the family Anisakidae and is of great importance in public health because of its high zoonotic potential. Anisakids are important to humans on a number of counts: economically, politically and mainly pathologically. Paratenic hosts are often fish that are important for human consumption. The worms do not mature in humans and the pathology is mostly associated with penetration of the small intestine and stomach by the larvae. The degree of discomfort is likely a consequence of the number of larvae penetrating. In rare cases, humans have died from anisakiasis due to severe peritonitis (Bush et al., 2001). However, there are no records of this zoonosis in the region and this is probably due to the fact that all of the larvae of this species were encysted in the mesentery, which is not used for human consumption.

The occurrence of a few species of some groups may be due to the absence or low number of certain hosts required for a particular stage of the developmental cycle. This is probably the case for the pentastomids that parasitize fish as larvae and alligators as adults. Although there are alligators in the floodplain, their numbers are relatively small when compared to other regions. The pentastomids are a small group of parasites that includes about 100 species. Studies on the phylogenetic relationships of the Pentastomida, a group traditionally treated as a separate phylum, suggest that they are truly arthropods with possible affinities for the crustacean (Bush et al., 2001).

The diversity of endohelminths can vary according to the environment or the species of host, and can be related to the size, longevity and particularly the food of the host. The intermediate host is necessarily part of the diet of the definitive host (Luque and Poulin, 2008). Furthermore, fish with a longer lifespan present more time of exposure to parasites, favoring cumulative processes in the host.

In the Upper Paraná River floodplain, Takemoto et al. (2005) studied the effects of several host traits (body size, social behavior, reproductive behavior, spawning type, trophic category, feeding habits, relative position in the food web, preference for certain habitats and whether the fish species are native or exotic) on metazoan endoparasite species richness. The CPUE (number of individuals of a given fish species captured per 1,000 m² of net during 24 hours) was the sole significant predictor of parasite species richness, regardless of control for the confounding influences of host phylogeny and sampling effort. The results suggest that in the Upper Paraná River floodplain (with homogeneous physical characteristics and occurrence of many flood pulses), population density of different host species might be the major determinant of the parasite species richness. This result is in concordance with epidemiological theory predicting that hosts with larger or denser populations will more readily sustain several parasite populations. Because parasites in this study use fish as either intermediate or definitive hosts, depending on species, this situation might reflect a combination of large intermediate and definitive host populations facilitating parasite transmission and reproduction, respectively. However, it is important to mention that the cited study was developed utilizing data obtained from 1986 to 2003, and current floods pulses do not occur periodically as they used to because of the construction of several hydroelectric power plants upstream from the studied area.

To date, 182 species of fish have been registered in the Upper Paraná River floodplain (Graça and Pavanelli, 2007). If we assume that each species of host can harbor an average of ten species of parasites (Takemoto et al., 2004), there should be about 1,820 species of parasites in the floodplain. However, in the present study we recorded less than 350 species of parasites, with many more to be studied. This number, however, may be much higher, considering that in some hosts such as P. lineatus, 33 species of parasites were reported.

To understand the role of the community of parasites in an ecosystem, previous knowledge of the species that compose it is required. Continuation of studies using taxonomic and systematic approaches is the key to understanding how biotic and abiotic factors affect species, since there is no way to understand the effects on a population without knowing the species.

Acknowledgements - We would like to express our gratitude to several people who helped us to obtain the data presented in this work: Gislaine M Guidelli, Patrícia M Machado Aoyama, Andréia Isaac, Solange de Carvalho, Ana Paula Ferrari, Jakeline G França, Fernando de C Tavernari, Kennya F Ito, Sara T Moreira, Eliane da S Fernandes, Luciana MS Hino, Letícia C Karling, Filipe MS Alvarenga, Paula G Milani and Ana Cláudia Munhoz RM Takemoto and GC Pavanelli were supported by a Research Fellowship from CNPq (Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico, Brazil). ACF Lacerda, FH Yamada and S Bellay were supported by Masters Scholarships from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). LHA Moreira was also supported by CNPq (Master Scholarship).

Received November 27, 2008

Accepted March 13, 2009

Distributed June 30, 2009 (With 2 figures)

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Appendix 1

Publication Dates

• Publication in this collection
  01 Sept 2009
• Date of issue
  June 2009

History

• Received
  27 Nov 2008
• Accepted
  13 Mar 2009