Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain/Fauna endoparasitaria de Serrasalmus spp. (Characidae: Serrasalminae) de uma planicie de inundacao neotropical.
Floodplains are the most dynamic systems, because of a large and complex biodiversity existence and maintenance (Powers, Sun, Parker, Dietrich, & Wootton, 1995). Besides, floodplains form a wide aquatic habitats variety (as rivers, lagoons and canals) associated to the transition between aquatic and terrestrial environments (Junk, 1980). These complexity occurs because of flood pulses, which are considered the main force to regulates the community and ecosystem structure and activity (Junk, Bayley, & Sparks, 1989).
However, fish communities are adapted to the hydrological and geomorphological environment (Agostinho, Gomes, & Zalewski, 2001). So, structure changes in ecosystems can cause species introductions (Lockwood, Hoopes, & Marchetti, 2007). Agostinho, Julio Junior, and Petrere Junior (1994) reported, in the upper Parana river floodplain, at least 17 exclusive species of the lower Parana river that colonized the upper Parana river because of the Itaipu reservoir, that was constructed 150 km downstream of the Sete Quedas falls, a geographical barrier for many fish species.
This introduction process happens to S. marginatus Valenciennes, 1837 and S. maculatus Kner, 1858 (1) since the Itaipu reservoir construction, which caused the two population fauna mixing. Because of this process, S. marginatus achieved large population growing in the new habitat, demonstrated by the increasing number of specimens collected (Agostinho, 2003).
Regarding to the evolutionary time in the earth, fishes are the most parasitized vertebrates. Thus, they are exposure and adapted to parasitic organisms in a longer time and, besides, fishes live in aquatic environments which facilitate parasites transmission and spread (Malta, 1984). This transmission can happen in the food chain, where the hosts are infected by trophic transmission or by water (direct cycle)
Minchella and Scott (1991) assumed the parasites relevance to the ecosystem saying that they participate in the food chain, of the biomass of hosts (much of this is formed by the parasitic populations), of the imposition of energy demands to their hosts, increasing their mortality rate and of the outcome changes in interspecific competition. Furthermore, the parasites may help to increase host susceptibility to predation, influencing it in the choice of partner and still increasing the sex ratio of the host population. So, there is a several ways in which parasites act on the hosts population dynamics, influencing the abundance and diversity of species in the environment.
According to Bonsall and Hassell (1997) in a situation in which the parasite cause some damage to the native host, classical ecological theory predicts that simple interactions in which species share common natural enemies are unstable, leading to one species to be eliminated from the interaction. This effect arises through competitive interactions mediated by the natural enemies 'apparent competition'.
Therefore, it is fundamental to study the host-parasite-environment relationship and analyze how fish and parasites population influences each other. Since hosts are in introduction species context, endoparasites ecological research allows to learn better these communities in order to determine parasites distribution in native and non-native host species as a way to analyze the influence of parasites in their inter and intraspecific competition (apparent competition).
Material and methods
Fishes were collected in the upper Parana river floodplain (22[degrees]45'S and 53[degrees]16'W) in Mato Grosso do Sul State next to Porto Rico city--PR (Figure 1). Samples were made in many environments: canals, rivers, open and closed lagoons, performed by Ilter-CNPq project (International Long Term Ecological Research)--Site 6.
[FIGURE 1 OMITTED]
Fishes were caught using different mesh sizes gill nets, from March 2013 until September 2014. This act was authorized by the Ethics Committee of the State University of Maringa (CEAE--Opinion 123/2010) and Ibama (22442-1). After identification, for each specimen captured, the following data were recorded: date, season and sampling point, total length (cm) and standard length (cm), total weight (g), sex, gonadal maturity stage and gonadal weight (g). Body condition was estimated by the relative condition factor (Kn), which is the relation between observed weight and weight provided by a regression of weight/length considering all fish sample (Le Cren, 1951).
Hosts autopsy and endoparasites collecting, fixing and preservation were made according to Eiras, Takemoto, and Pavanelli (2006); ectoparasites were not considered. Parasitological variables analyzed were: infracommunity richness (parasite species number per host individual), prevalence (number of hosts infected per number of hosts examined given as percentage), abundance (number of individuals of a particular parasite in/on a single host regardless of whether or not the hosts is infected) and intensity (number of individuals of a particular parasite species in a single infected host (Bush, Lafferty, Lotz, & Shostak, 1997).
Only parasite species that presented over 10% prevalence were considered in ecological analyses (Bush, Aho, & Kennedy, 1990). To determine a possible correlation between the abundance/host size and abundance/relative condition factor (Kn), Spearman's rank correlation coefficient "rs" was used, obtained according to Zar (2010). Pearson correlation coefficient "r" was applied to detect correlations between parasite prevalence and host size. For this test, prevalence data was previously transformed angularly (arc sine) and samples of hosts were separated into standard length classes (Zar, 2010).
Nonparametric Mann-Whitney test (U) with normal approximation Z was used to determine differences between Kn of infected and non-infected individuals and to determine hosts sex influence in the infection abundance of each parasite species (Zar, 2010). The G loglikelihood test, using a 2 x 2 contingency table, was used to verify the host sex influence in endoparasites infection prevalence (Zar, 2010).
Subsequent analysis contemplated each specimen infracommunity to two fish species. Each infracommunity diversity was calculated using Brillouin diversity index (H) (Zar, 2010). Dominance was estimated by Berger-Parker index (Magurran, 2004), d = Nmax./Nt; Nmax. refers to number of individuals in most abundant parasite species and Nt refers to total number of individuals in the sample.
Spearman's rank correlation coefficient "rs" was used to evaluate correlations between host standard length and species diversity (Brillouin index) and between relative condition factor and diversity (Zar, 2010). In order to verify differences between hosts males and females due to parasitic infracommunities diversity, Mann-Whitney U test was used (Zar, 2010).
Statistical analyzes were made using BioEstat 5.0 (Ayres, Ayres, Ayres, & Santos, 2007) and Past (Hammer, Harper, & Yan, 2001) programs.
In total, 58 fish were collected, 27 S. marginatus (standard length: 10.5 to 21.5) and 31 S. maculatus (standard length: 9.0 to 23.0). Endoparasites found in these two fish species totaled 897 individuals, with ten different species; five of those species present simultaneously in two hosts species (Table. 1). In total, eight endoparasite species were found in S. marginatus and seven species in S. maculatus.
Kritskyia annakohnae, Echinorhynchus sp. Contracaecum sp. Contracaecum sp. type 1 showed over 10% prevalence in S. marginatus and S. maculatus. Thus, following statistics analyzes contemplated such this species.
Spearman's rank correlation coefficient "rs" showed positive and significant correlation between S. marginatus standard length and Echinorhynchus sp. abundance (Figure 2 and Table 2). Pearson correlation coefficient "r" showed a significant negative correlation only between S. marginatus standard length and K. annakohnae prevalence (Figure. 3 and Table. 2).
Fish relative condition factor (Kn) ranged from 0.89 to 1.42 for S. marginatus and 0.36 to 1.35 for S. maculatus. According to Spearman's rank correlation coefficient "rs", S. marginatus relative condition factor was correlated negatively and significantly with Kritskyia annakohnae abundance (Figure 4 and Table 3).
According to Mann-Whitney U tests, S. marginatus Kn differ between infected and non-infected fish to K. annakohnae, taking into account that the Kn of the infected fish was lower if compared to the Kn of non-infected fish. (Table 3).
Considering a total of 27 S. marginatus specimens, 15 were female and 12 were males. Those, 13 females (86.66%) and 11 male (91.66%) were infected by at least one endoparasite species. On the other hand, S. maculatus presented a total of 31 specimens, which 16 female and 15 male. Those, 15 (93.75%) females and 12 (80%) males were infected by at least one endoparasite species. Mann-Whitney U tests, and G loglikelihood showed that species abundance and parasites prevalence did not differ between males and females (Table. 4).
Spearman's rank correlation coefficient "rs" did not show significant correlation between infracommunities diversity (Brillouin Index) and hosts standard length for both: S. marginatus (rs = 0.302, p = 0.1613) and S. maculates (rs = 0.016, p = 0.937). Similarly, there was no significant correlation between relative condition factor and parasites mean diversity for S. marginatus (rs = -0.2273, p = 0.2969) or S. maculatus (rs = -0.0438; p = 0.8282).
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
Berger-Parker dominance index presented mean around on 1 [+ or -] 0.36 for S. marginatus and 1 [+ or -] 0.40 for S. maculatus, being K. annakohnae the predominant species to S. maculatus with 429 specimens collected (76. 88%) and Echinorhynchus sp. predominant specie to S. marginatus with 181 specimens collected (53.07%).
[FIGURE 4 OMITTED]
In the total, the average diversity of endoparasites hasn't shown meaning ful difference when compared to the host sex of both species: S. marginatus (Z = 0.0615, p = 0.9509) and S. maculatus (Z = 0.2196, p = 0.8262); that is, parasite diversity has presented independency regarding to the host sex.
Serrasalmus marginatus and S. maculatus were more parasitized by Monogenea. It can be related to monoxenic life cycle of these parasites, since they do not need an intermediate host to be transmitted from one host to another.
Considering the K. annakohnae monoxenic cycle, transmission occurs directly from one host to another, which can be explained by the behavior of S. maculatus and S. marginatus to form shoals (Sazima & Machado, 1990). Both species promote this parasite occurrence. On the other hand, the presence of this parasite in both fish species can also be explained by phylogenetic closely, since a parasite may have hierarchical preference for hosts, which occurs when the cost for the parasite access the same resource is explored between the host species (Sazima, Janz, & Nylin, 1998).
Monogeneans are mainly fish ectoparasites located in gills (Eiras, 1994) and records are rare in internal organs. Fischthal and Allison (1941), Kohn (1990) and Bilong Bilong, Birgi, & Euzet (1994) recorded these parasites in urinary bladder. Kearn (1987), in a study about stingrays internal monogeneans, proposed that swimmers parasite larvae can have direct access to sewer and, from there, they can go for their sites of infection such as rectal glands. So, it is possible that this happens with K. annakohnae, as urinary duct open up in fish cloaca, thus enabling infective forms access to the urinary bladder.
Because S. marginatus and S. maculatus eat mainly pieces of fins and other lower fish parts, it does not explain parasites transmission by trophic via, since a stomach contents analysis showed that crustaceans are also food content forthose fish species. Crustaceans are, in general, intermediate hosts for some Echinorhynchus (Acanthocephala) species and, because of this, crustaceans can carry larval forms of these parasites (Schmidt, 1985). As S. marginatus presents territoriality and aggression in its behavior (Agostinho, 2003), this allows a better foraging for this species and consequently a large amount of acanthocephalans. So, S. marginatus ingests a greater number of infected intermediate hosts than S. maculatus and consequently a large amount of acanthocephalans larvae.
Regarding to Nematoda, the results of the research indicate that the highest prevalences occurred to Contracaecum sp. and Contracaecum sp. type 1 in both hosts species, what suggest that two fishes species can be intermediate hosts for these nematodes, as these parasites uses those fishes as intermediate hosts (Eiras, 1994; Moravec, 1998).
In fish populations, intensity of infection by metazoan parasites increases with age or host size (Dogiel, 1970). Echinorhynchus sp. abundance was correlated positively with S. marginatus standard length, since older fishes are bigger to accumulate parasites than younger. So, when fishes grows up, they can offer more internal spaces for parasites establishment (Poulin, 2000).
Significant negative correlation between K. annakohnae prevalence and S. marginatus standard length demonstrated that there is a higher number of infected fish in smaller size classes. It is possible considering direct cycle influence in parasitology variables as abundance (Zelmer & Arai, 1998) and morphological and physiological factors that are involved in selection of microhabitats by parasites, especially the selection of smaller places as a facilitator for mating meetings (Rohde, 2005). Urinary bladder is this parasite site of infection and this organ is smaller in small fish, what suggested actually that the reduction of space facilitates mating and then a higher prevalence in smaller size classes fishes.
Kritskyia annakohnae abundance influenced in S. marginatus condition factor, which is explained by Yamada, Takemoto, and Pavanelli (2008): parasitized and non-parasitized fishes may show a difference in your composition, being Kn of infected fish lower if compared with the not infected fish. So parasites can change the hosts condition by direct action. Echinorhynchus sp. presented a high relatively abundance value, but this had not influenced the hosts relative condition factor. This is possible because of time adjustment in host-parasite relationship, that includes, in this case, a potential loss of parasites pathogenicity.
Parasites prevalence and abundance in congeneric host species did not show any differences between the sex of the hosts. According to Agostinho (2003), in a study about those species condition factor variation pattern in the Parana river floodplain, it indicated that the most important is food availability and not reproductive events, since in food shortages periods have shown reduced condition factor, especially in immature individuals. Besides, it can be assumed that males and females have similar diets, what did not influence these fishes parasitism. Similar results were found by Machado, Pavanelli, and Takemoto (1994); Machado Almeida, Pavanelli, and Takemoto (2000) for different host species.
Richness and diversity communities are often related parasites to hosts body length. Different length class fishes differ in their life way and, as a consequence, differs in their exposure to parasites degree (Guegan & Hugueny, 1994). Besides that, some parasites species may occur in some hosts length classes and be absent in others, because of diet habits, behavior and fish microhabitats.
Relationship between host variables (body size, relative condition factor and host sex) and parasite diversity was not found. Although parasitic composition may be a indicator of habitat and hosts migration routes, these pattern may be related to fish immune system, or influenced by food habits (smaller fishes can use features that are not accessible to adults). Another explanation consists in environments, with higher intermediate hosts concentration, frequented by young fish (Monteiro, Santos, Zuchi, & Brasil-Sato, 2009), that allows the parasite transmission via trophic in this case.
Kritskyia annakohnae predominance in S. marginatus urinary bladder can be related to the idea of apparent competition. In this case, when two hosts species share infective stages, tolerant to infection species can act as a parasite reservoir to less tolerant. So, more tolerant host species acts as a competitive top, and this competition is mediated by mechanism of sharing parasites (Greenman & Hudson, 2000). In this context, it was suggested that K. annakohnae reservoir could be S. marginatus and less tolerant species could be S. maculatus.
Knowledge of parasitological variables in the context of species introduction opens way for new research that explain occurrence of each parasite species in hosts, native or introduced. If the parasite is the inductor subject of host population changes (apparent competition), it is necessary to carry out experiments that verify this mechanism.
Agostinho, A. A., Gomes, L. C, & Zalewski, M. (2001). The importance of floodplains for the dynamics of fish communities of the upper river Parana. Ecohydrology and Hydrobiology, 1(2), 209-217.
Agostinho, A. A., Julio Junior, H. F., & Petrere Junior, M. (1994). Itaipu reservoir (Brazil): impacts of the impoundment on the fish fauna and fisheries. In I. G. Cowx, (Ed.), Rehabilitation of freshwater fisheries (p. 171-184). Oxford, UK: Blackwell
Agostinho, C. S. (2003). Reproductive aspects of piranhas Serrasalmus spilopleura and Serrasalmus marginatus into the upper Parana river, Brazil. Brazilian Jounal of Biology, 63(1), 1-6.
Ayres, M., Ayres, J. R. M., Ayres, D. L., & Santos, A. S. (2007). Bioestat 5.0: aplicacoes estatisticas na area de ciencias biologicas e medicas. Belem: Sociedade Civil Mamiraua. Brasilia, DF: CNPq.
Bilong Bilong, C. F., Birgi, E., & Euzet, L. (1994). Urogyrus cichlidarum gen. nov., sp. nov., Urogyridae fam. nov., monogene parasite de lavessie urinaire de poissons cichlide sau Cameroun. Canadian Journal of Zoology, 72(3), 561-566.
Bonsall, M. B., & Hassell, M. P. (1997). Apparent competition structures ecological assemblages. Nature, 388(6640), 371-373.
Bush, A. O., Aho, J. M., & Kennedy, C. R. (1990). Ecological versus phylogenetics determinants of helminth parasite community richness. Evolutionary Ecology, 4(1), 1-20.
Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. (Rev. Ed.). Journal of Parasitology, 83(4), 575-583.
Dogiel, V. A. (1970). Ecology of the parasites of freshwater fishes. In V. A. Dogiel, G. K. Petrushevski, & Y. I. Polyanski (Eds.), Parasitology of fishes (p. 1-47). London, UK: Oliver & Boyd.
Eiras, J. C. (1994). Elementos de ictioparasitologia. Porto, PT: Fundacao Eng. Antonio de Almeida.
Eiras, J. C., Takemoto, R. M., & Pavanelli, G. C. (2006). Metodos de estudo e tecnicas laboratoriais em parasitologia de peixes. Maringa, PR: Eduem.
Fischthal, J. H., & Allison, L. N. (1941). Acolpenteron ureteroecetes a monogenetic trematode from the ureters of the black basses, with a revision of the family Calceostomatidae (Gyrodactyloidea). Journal of Parasitology, 27(6), 517-524.
Greenman, J. V., & Hudson, P. J. (2000). Parasite mediated and direct competition in a two-host shared macroparasite system. Theoretical Population Biology, 37(1), 13-34.
Guegan, J. F., & Hugueny, B. (1994). A nested parasites species subset pattern in tropical fish-host as major determinant of parasite infracommunity structure. Oecologia, 100(1-2), 184-189.
Hammer, O., Harper, D. A. T., & Yan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1-9.
Jegu, M., & Santos, G. M. (2001). Mise au point propos de Serrasalmus spilopleura Kner, 1858 etre habilitation de S. maculatus Kner, 1858 (Characidae: Serrasalminae). Cybium, 23(2), 119-143.
Junk, W. J. (1980). Areas inundaveis: um desafio para limnologia. Acta Amazonica, 10(4), 775-795.
Junk, W. J., Bayley, P. B., & Sparks, R. E. (1989). The flood pulse concept in river-floodplains systems. In D. P. Dogde (Ed.), Proceedings of the International Large River Symposium (LARS) (p. 110-127). Ottawa, CA: Canadian Special Publication of Fisheries and Aquatic Sciences 106.
Kearn, G. C. (1987).The site of development of the monogenean Calicotyle kroyeri, a parasite of rays. Marine Biological Associationof the United Kingdom, 67(1), 77-87.
Kohn, A. (1990). Kritskya moraveci n. g., n. sp. (Monogenea, Dactylogyridae) from the urinary bladder and ureters of Rhamdia quelen (Quoy & Gaimard, 1824) (Pisces: Pimelodidae) in Brazil. Systematic Parasitology, 17(2), 81-85.
Le Cren, E. D. (1951). The length-weight relationship and seasonal cycle in gonad weight and conditions in the perch (Perca fluviatilis). Journal of Animal Ecology, 20(2), 201-211.
Lockwood, J. L., Hoopes, M. F., & Marchetti, M. P. (2007). Invasion Ecology. Oxford, UK: Blackwell Publishing.
Machado, M. H., Pavanelli, G. C., & Takemoto, R. M. (1994). Influence of host's sex and size on endoparasitic infrapopulations of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Parana river, Brazil. Revista Brasileira de Parasitologia Veterinaria, 3(2), 143-148.
Machado, P. M., Almeida, S. C., Pavanelli, G. C., & Takemoto, R. M. (2000). Ecological aspects of Endohelminths Parasitizing Cichla monoculus Spix, 1831 (Perciformes, Cichlidae) in the Parana river near Porto Rico, State of Parana, Brazil. Journal Helminthological Society of Washington, 67(2), 210-217.
Magurran, A. E. (2004). Measuring biological diversity. Oxford, UK: Blackwell.
Malta, J. C. O. (1984). Os peixes de um lago de varzea da Amazonia central (Lago Janauaca, Rio Solimoes) e suas relacoes com os crustaceos ectoparasitas (Branchiura: Argulidae). Acta Amazonica, 14(3-4), 355-372.
Minchella, D. J., & Scott, M. E. (1991). Parasitism: A Cryptic Determinant of Animal Community Structure. Trends in Ecology and Evolution, 6(8), 250-254.
Monteiro, C. M., Santos, D. M., Zuchi, N. A., & Brasil-Sato, M. C. (2009). Ecological parameters of the endohelminths in relation to size and sex of Prochilodus argenteus (Actinopterygii: Prochilodontidae) from the upper Sao Francisco river, Minas Gerais, Brazil. Zoologia, 26(4), 753-757.
Moravec, F. (1998). Nematodes of freshwater fishes of the Neotropical Region. Praha, CZ: Academy of Sciences of the Czech Republic.
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical. Journal of Fish Biology, 36(1), 126-137.
Powers, M. E., Sun, A., Parker, M., Dietrich, W. E., & Wootton, J. T. (1995). Hydraulic Food-chain Models: an approach to the study of food web dynamics in large rivers. BioScience, 43(2), 159-167.
Rohde, K. (2005). Marine parasitology. Wallingford, UK: Cabi Publishing.
Sazima, I., Janz, N., & Nylin, S. (1998). Butterflies and plants: a phylogenetic study. Evolution, 32(2), 486-502.
Sazima, I., & Machado, F. A. (1990). Underwater observations of piranhas in western Brazil. Environment Biology of Fishes, 28(1-4), 17-31.
Schmidt, G. D. (1985). Biology of the Acanthocephala. In D. W. T. Crompton, & B. B. Nickol (Eds.), Development and life cycles (p. 273-305). Cambridge, UK: Cambridge University Press.
Yamada, F. H., Takemoto, R. M., & Pavanelli, G. C. (2008). Relacao entre fator de condicao relativo (Kn) e abundancia de ectoparasitos de branquias, em duas especies de ciclideos da bacia do rio Parana, Brasil. Acta Scientiarum. Biological Sciences, 30(2), 213-217.
Zar, J. H. (2010). Biostatistical Analysis. New Jersey, US: Prentice-Hall.
Zelmer, D. A., & Arai, H. P. (1998). The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca Jlavescens, from Garner lake, Alberta, Canada. The Journal of Parasitology, 84(1), 24-28.
Received on July 20, 2015.
Accepted on February 17, 2016.
Guilherme Pomaro Casali  * and Ricardo Massato Takemoto [1,2]
 Programa de Pos-graduacao em Biologia Comparada, Universidade Estadual de Maringa, Av. Colombo, 5790, 87020-900, Maringa, Parana, Brazil.  Nucleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringa, Maringa, Parana, Brazil. *Author for correspondence. E-mail: email@example.com
(1) S. maculatus Kner, 1858 earlier identified as S. spilopleura Kner, 1860 (Jegu & Santos, 2001).
Table 1. Endorasites of Serrasalmus marginatus and S. maculatus from upper Parana river Floodplain, collected from March 2013 to September 2014. P = prevalence; MA = mean abundance; MI = mean intensity. Host species Taxonomic Parasite Infection group species site S. marginatus Monogenea K. annakohnae Urinary Boeger, Tanaka bladder & Pavanelli, 2001 Acanthocephala Echinorhynchus Intestine and sp. Pyloric cecum Nematoda Procamallanus Intestine (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 Contracaecum Mesentery sp. (larva) Railliet & Henry, 1912 Contracaecum Mesentery sp. type 1 of Moravec, Kohn & Fernandes, 1993 Spiroxys sp. Mesentery Hysterothylacium Mesentery sp. (larva) Ward &Magath, 1917 Goezia sp. Mesentery (larva) Zeder, 1800 S. maculatus Monogenea K. annakohnae Urinary (Boeger, Tanaka bladder & Pavanelli, 2001) Acanthocephala Echinorhynchus Intestine sp. and Estomach Nematoda Procamallanus Pyloric (Spirocamauanus) cecum inopinatus Travassos, Artigas & Pereira, 1928 Procamallanus Intestine (Spirocamauanus) neocabauemi (Caballero- Deloya, 1977) Contracaecum Mesentery sp. (larva) Railliet & Henry, 1912 Contracaecum Mesentery sp. type 1 of Moravec, Kohn & Fernandes, 1993 Contracaecum Mesentery sp. type 2 of Moravec, Kohn & Fernandes, 1993 Host species Taxonomic Parasite P (%) group species S. marginatus Monogenea K. annakohnae 71.42 Boeger, Tanaka & Pavanelli, 2001 Acanthocephala Echinorhynchus 60.71 sp. Nematoda Procamallanus 3.57 (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 Contracaecum 17.85 sp. (larva) Railliet & Henry, 1912 Contracaecum 28.57 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Spiroxys sp. 3.57 Hysterothylacium 3,57 sp. (larva) Ward & Magath, 1917 Goezia sp. 3.57 (larva) Zeder, 1800 S. maculatus Monogenea K. annakohnae 65.62 (Boeger, Tanaka & Pavanelli, 2001) Acanthocephala Echinorhynchus 50 sp. Nematoda Procamallanus 3.57 (Spirocamauanus) inopinatus Travassos, Artigas & Pereira, 1928 Procamallanus 3.57 (Spirocamauanus) neocabauemi (Caballero- Deloya, 1977) Contracaecum 34.37 sp. (larva) Railliet & Henry, 1912 Contracaecum 28.57 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Contracaecum 9.37 sp. type 2 of Moravec, Kohn & Fernandes, 1993 Host species Taxonomic Parasite MA group species S. marginatus Monogenea K. annakohnae 4.53 Boeger, Tanaka & Pavanelli, 2001 Acanthocephala Echinorhynchus 6.28 sp. Nematoda Procamallanus 0.035 (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 Contracaecum 0.32 sp. (larva) Railliet & Henry, 1912 Contracaecum 0.71 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Spiroxys sp. 0.035 Hysterothylacium 0.035 sp. (larva) Ward & Magath, 1917 Goezia sp. 0.035 (larva) Zeder, 1800 S. maculatus Monogenea K. annakohnae 13.65 (Boeger, Tanaka & Pavanelli, 2001) Acanthocephala Echinorhynchus 2.65 sp. Nematoda Procamallanus 0.035 (Spirocamauanus) inopinatus Travassos, Artigas & Pereira, 1928 Procamallanus 0.035 (Spirocamauanus) neocabauemi (Caballero- Deloya, 1977) Contracaecum 0.84 sp. (larva) Railliet & Henry, 1912 Contracaecum 0.9 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Contracaecum 0.09 sp. type 2 of Moravec, Kohn & Fernandes, 1993 Host species Taxonomic Parasite MI group species S. marginatus Monogenea K. annakohnae 6.35 Boeger, Tanaka & Pavanelli, 2001 Acanthocephala Echinorhynchus 10.35 sp. Nematoda Procamallanus 1 (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 Contracaecum 1.80 sp. (larva) Railliet & Henry, 1912 Contracaecum 2.25 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Spiroxys sp. 1 Hysterothylacium 1 sp. (larva) Ward & Magath, 1917 Goezia sp. 1 (larva) Zeder, 1800 S. maculatus Monogenea K. annakohnae 20.80 (Boeger, Tanaka & Pavanelli, 2001) Acanthocephala Echinorhynchus 5.31 sp. Nematoda Procamallanus 1 (Spirocamauanus) inopinatus Travassos, Artigas & Pereira, 1928 Procamallanus 1 (Spirocamauanus) neocabauemi (Caballero- Deloya, 1977) Contracaecum 2.45 sp. (larva) Railliet & Henry, 1912 Contracaecum 2.07 sp. type 1 of Moravec, Kohn & Fernandes, 1993 Contracaecum 1 sp. type 2 of Moravec, Kohn & Fernandes, 1993 Table 2. Correlations between hosts standard length and parasites abundance and prevalence values, obtained by Spearman's rank (rs) and Pearson correlation (r). Serrasalmus margintaus and S. maculatus collected in the upper Parana river floodplain between March 2013 and September 2014 (p = significance level). Host species Parasite species rs p Serrasalmus K. annakohnae -0.2219 0.2658 marginatus Echinoihynckus sp. 0.4674 0.0090 * Contracaecum sp. 0.2984 0.1304 Contracaecum sp. type 1 0.3039 0.1233 Serrasalmus K. annakohnae 0.3074 0.0769 maculatus Echinorhynchus sp. -0.0877 0.5577 Contracaecum sp. 0.0706 0.7058 Contracaecum sp. type 1 0.0418 0.8235 Host species Parasite species r p Serrasalmus K. annakohnae -0.8533 0,0307 * marginatus Echinoihynckus sp. 0.155 0.7693 Contracaecum sp. 0.3513 0.4947 Contracaecum sp. type 1 0.0831 0.8756 Serrasalmus K. annakohnae 0.3561 0.3865 maculatus Echinorhynchus sp. 0.3691 0.3682 Contracaecum sp. 0.0404 0.9243 Contracaecum sp. type 1 -0.2789 0.5035 * Significant "p" values. Table 3. Correlation values between relative condition factor (Kn) and parasite abundance, obtained by Spearman's rank correlation coefficient (rs) and Mann-Whitney test. Values with normal approximation "Z" differentiating Kn of parasitized and non-parasitized fishes. Serrasalmus marginatus and S. maculatus data collected in the upper Parana river floodplain between March 2013 and September 2014 (p = significance level). Host species Parasite species rs p S. marginatus Kritskyia annakohnae -0.4744 0.0124 * Echinorhynchus sp. -0.1972 0.1838 Contracaecum sp. 0.0581 0.7736 Contracaecum sp. type 1 0.1765 0.3786 S. maculatus Kritskyia annakohnae -0.0136 0.9420 Echinorhynchus sp. 0.0201 0.9143 Contracaecum sp. 0.2828 0.1231 Contracaecum sp. type 1 0.1569 0.3993 Host species Parasite species Z p S. marginatus Kritskyia annakohnae 2.6004 0.0093 * Echinorhynchus sp. 0.7029 0.4821 Contracaecum sp. 0.3433 0.7314 Contracaecum sp. type 1 0.2196 0.8262 S. maculatus Kritskyia annakohnae 0.3096 0.7568 Echinorhynchus sp. 0.1581 0.8744 Contracaecum sp. 1.3418 0.1797 Contracaecum sp. type 1 0.9924 0.3210 * Significant "p" values. Table 4. Mann-Whitney U test values with normal approximation "Z", and G loglikelihood between hosts sex with infection prevalence and abundance, to Serrasaimus marginatus and S. maculatus collected in floodplain Parana river, from March 2013 to September 2014. (p = significance level). Hosts species Parasites species Z p S. marginatus K. annakohnae 0.0244 0.9805 Echinorhynchus sp. 0.2196 0.8262 Contracaecum sp. 0.0976 0.9223 Contracaecum sp. type 1 0.2196 0.8262 S. maculatus K. annakohnae 1.4033 0.1605 Echinorhynchus sp. 0.1779 0.8588 Contracaecum sp. 0.6522 0.5143 Contracaecum sp. type 1 0.8499 0.3954 Hosts species Parasites species G p S. marginatus K. annakohnae 0.9943 0.3187 Echinorhynchus sp. 0.1275 0.7210 Contracaecum sp. 0.0494 0.8241 Contracaecum sp. type 1 * * S. maculatus K. annakohnae 1.6018 0.2056 Echinorhynchus sp. 0.0345 0.8527 Contracaecum sp. 0.9967 0.3181 Contracaecum sp. type 1 0.3133 0.5757 * Data for which the analysis were not done.
|Printer friendly Cite/link Email Feedback|
|Author:||Casali, Guilherme Pomaro; Takemoto, Ricardo Massato|
|Publication:||Acta Scientiarum. Biological Sciences (UEM)|
|Date:||Jan 1, 2016|
|Previous Article:||Mild-acid hydrolysis of a native polysulfated fraction from Acanthophora muscoides generates sulfated oligosaccharides displaying in vitro thrombin...|
|Next Article:||Composition and structure of the gallery forest in the Taquarucu Grande Sub-basin, Municipality of Palmas, Tocantins State/Composicao floristica e...|