Community ecology of the metazoan parasites of Brazilian sardinella, Sardinella brasiliensis (Steindachner, 1879) (Actinopterygii: Clupeidae) from the coastal zone of the State of Rio de Janeiro, Brazil/Ecologia da comunidade dos metazoarios parasitos da sardinha Sardinella brasiliensis (Steindachner, 1879) (Actinopterygii: Clupeidae) do litoral do Estado do Rio de Janeiro, Brasil.
The Brazilian sardinella, Sardinella brasiliensis (Steindachner) is a marine finfish that inhabits coastal waters from Rio de Janeiro to south Brazil, always forming large schools. This species feeds mainly of the planktonic organisms filtered by gill rakers (Figueiredo and Menezes, 1978). It's the most important marine fishery resource of Brazil, in volume production, with landings concentrated in the States of Rio de Janeiro, Sao Paulo e Santa Catarina, contributing to world food resources in two ways: directly, through actual consumption (fresh, frozen or processed) and indirectly, by providing products used for animal feeds and fertilizers or by serving as bait to catch other fishes. (Paiva, 1997; Whitehead, 1985).
In Brazil, the parasitic fauna of clupeid fishes is poorly known, with most studies of taxonomy origin, performed by Vaz and Pereira (1930), Kohn and Buhrnheim (1964), Travassos et al. (1967), Feijo et al. (1979), Wallet and Kohn (1987), Fabio (1988), Fernandes and Goulart (1989), with descriptions and records of digenetic trematodes; Kohn and Santos (1988) and Santos and Kohn (1992) for monogeneans; Palm (1997) and Rodrigues et al. (1990) for cestodes; Vicente et al. (1985) and Feijo et al. (1979) for nematodes; Month (1980) and Amado and Falavigna (1996) for copepods. Studies regarding to ecological aspects were performed by Luque et al. (2000) and Tavares et al. (2004), on the parasitic fauna of Harengula clupeola (Cuvier) and S. brasiliensis, and Brevoortia aurea (Spix and Agassiz), respectively.
In this report, we analyze the composition and structure of the metazoan parasite communities of S. brasiliensis from the coastal zone of the State of Rio de Janeiro, Brazil.
2. Material and Methods
Between March 2010 and August 2011, 100 specimens of S. brasiliensis were necropsied, from the coast of Cabo Frio, Rio de Janeiro, Brazil (22[degrees]51>S, 43[degrees]56>O), to study their community of metazoan parasites. Fishes were identified according to Figueiredo and Menezes (1978). The analysis included only parasite species with prevalence higher than 10% (Bush et al., 1990).
The variance-to-mean ratio of parasite abundance (index of dispersion) and the discrepancy index, computed using the program Quantitative Parasitology 3.0 (Rozsa et al., 2000), were used to detect distribution patterns of the infrapopulations (Poulin, 1993). The dominance frequency and the relative dominance (number of specimens of one species/total number of specimens of all species in the infracommunity) of each parasite species were calculated according to Rohde et al. (1995). The parasite species diversity was calculated using the Brillouin index (H), because each fish analyzed corresponded to a fully censused community (Zar, 1996). The Spearman's rank correlation coefficient rs was calculated to determine possible correlations between the total length of hosts and parasite abundance. Pearson's correlation coefficient r was used to indicate the relationship between the host's total length and parasite prevalence, with previous arcsine transformation of the prevalence data (Zar, 1996). The effect of host sex on abundance and prevalence of parasites was tested using the Zc (normal) approximation to the Mann-Whitney test and the Fisher exact test, respectively. Parasite species diversity was calculated using the Brillouin's index (H) (Zar, 1996). The probable variation of diversity in relation to host sex (Mann-Whitney test) and to host total length (Spearman's rank correlation coefficient) was tested. Possible interspecific association between concurrent species was determined using the chi-square test. Possible covariation among the abundance of concurrent species was analyzed using the Spearman's rank correlation coefficient. The ecological terminology used follows Bush et al. (1997). Statistical significance level was evaluated at p [less than or equal to] 0.05. Voucher specimens of helminths were deposited in the Helminthological Collection of Institute Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil; copepods were deposited in the Carcinological Collection of National Museum of Rio de Janeiro (MNRJ), Brazil.
The average total length of the fish was 12.7-24.8 (20.4 [+ or -] 1.91) cm, and the weight was 25-120 (77.6 [+ or -] 19.8) g. The average total length of male (20.6 [+ or -] 1.2, n = 79) and female (20 [+ or -] 2.8, n = 21) fishes in the studied sample were significantly different (t = -2.890, P = 0.005).
3.1. Component community
Eleven species of metazoan parasites were collected (Table 1). Sardinella brasiliensis is a new host record for most of these species with exceptions made for the digeneans Myosaccium ecaude Montgomery and Parahemiurus merus Price (Luque et al., 2000), and for the copepod Clavellisa ilishae Pillai (Moreira et al., 2013). The digenetic trematode M. ecaude was the most abundant, prevalent, and dominant species, representing 72.7% of metazoan parasites collected with greatest values of mean relative dominance and frequency of dominance (Table 2).
Adult endoparasites represented 98.98% of all parasites collected, larval endoparasites amounted to 0.64%, and ectoparasites made up 0.38%. All parasites of S. brasiliensis had the typical aggregated pattern of distribution, except the cestode Callitetrarhynchus gracilis Rudolphi that showed dispersion index lower than 1, indicating a uniform pattern of distribution (Table 3). Only M. ecaude showed positively correlation between host's total length and parasite abundance (rs = 0.197, p = 0.049). The host's total length was not correlated with the prevalence of any species. The sex of hosts did not influence prevalence and abundance of any parasite species.
All specimens of S. brasiliensis were parasitized by at least one parasite species. A total of 6,866 individual parasites were collected, with mean of 68.7 [+ or -] 71.2 parasites/ fish. Positive correlations were detected between parasite abundance and host's total length (rs = 0.222, p = 0.026), but the host's total length was not correlated with parasite species richness (rs = 0.193, p = 0.055). Six hosts (6%) showed infection with one parasite species, and 48 (48%), 36 (36%), 7 (7%) e 3 (3%) had multiple infections with 2, 3, 4, 5 parasite species, respectively (Figure 1). Mean parasite species diversity (H = 0.545 [+ or -] 0.228) was not correlated with host's total length (rs = 0.168, p = 0.094) and no significant differences in parasite diversity were observed between male (H = 0.529 [+ or -] 0.239) and female (H = 0.605 [+ or -] 0.175) fishes ([Z.sub.c] = -1.292, p = 0.196).
The endoparasites were separated into two groups helminth larval stages (cestodes and nematodes) and adult endoparasites (digeneans)--and were used to determine possible interspecific associations. Ectoparasites (copepods and monogeneans) were not included in this analysis because none of the species of this group showed prevalence higher than 10%. The helminth larval stages pair, C. gracilis--Hysterothylacium sp., did not share significant association and covariation ([chi square] = 0.63, p = 0.429; [r.sub.s] = -0.083, p = 0.412). The three pairs of endoparasites speciesM. ecaude--P. merus, M. ecaude--Prodistomum gracile, P. merus--P. gracile, showed positive covariation (Table 4).
The parasite community of S. brasiliensis showed digenetic trematodes dominance, which was previously reported by Luque et al. (2000) in a quantitative study of clupeid fishes from the coastal zone of the state of Rio de Janeiro. The dominance of digenean endoparasites has been described for several parasite communities of marine fishes from the coastal zone of southeastern Brazil (Luque et al., 1996; Takemoto et al., 1996; Knoff et al., 1997; Luque and Chaves, 1999; Silva et al., 2000; Luque and Alves, 2001; Tavares and Luque, 2004). The feeding of S. brasiliensis, which is predominantly composed by zooplanktonic copepods (Schneider and Schwingel, 1999), may favor the transmission of these parasites, since many of them act as intermediate hosts for digeneans.
Regarding to the study previously performed by Luque et al. (2000), the parasite species richness has increased and another important change was the presence of larval stages of helminths that were absent in the previous study, the nematodes Hysterothylacium sp., Pseudoterranova sp. and Raphidascaris sp., and the cestodes C. gracilis and Nybelinia sp. These differences may be related to the number of specimens necropsied, changes in coastal ecological features, seasonality, and the lack of studies on the parasites of clupeid fishes in the region. This low infection of larval stages of helminths was also observed in other clupeid fishes by Perez-Ponce de Leon et al. (2000), in Mexico. And according to some authors, the presence of larval stages of helminths can be considered as a reflection of the intermediate trophic level of the host (George-Nascimento, 1987; Luque and Poulin, 2004).
The schooling habits of herrings might facilitate the transmission of some ectoparasites with direct life cycle, such as copepods and monogeneans (Luque and Alves, 2001). However, in this study a low prevalence in both taxa was observed, which may have been influenced by host biology, parasite specificity, hydrological conditions or environmental and ecological conditions of the region (Cone and Burt, 1982; Ibagy and Sinque, 1985). The monogenean Cribomazocraes travassosi Kohn and Santos was originally described parasitizing Harengula clupeola, and this paper reports the first occurrence of this species in S. brasiliensis, but with a low prevalence as previously mentioned, which may be an indication of the host specificity demonstrated by many monogeneans.
The parasite community of S. brasiliensis had the typically aggregated pattern of distribution, with exception made for Callitetrarhynchus gracilis who had an index of dispersion less than 1, thus indicating a uniform pattern of distribution, which is not a common occurrence in helminths. According to Von Zuben (1997) there are three factors that can lead to a uniform pattern of distribution: (1) mortality of parasites; (2) density dependent processes; and (3) the mortality of the host induced by the parasite (mortality rate positively correlated with parasite charge).
Unlike the pattern previously observed, the parasite abundance was positively correlated with host's total length. According to Polyansky (1961) quantitative and qualitative changes in parasitism are expected with fish growth. Diet, body mass and school formation are factors considered by Polyansky and Bychowsky (1963) as responsible for the number of parasite species harbored by a host. But according to Luque and Alves (2001), generalizations about the influence of host size on the quantitative and qualitative composition of parasitic infracommunities should be avoided.
The absence of correlations between host gender and the prevalence and abundance of the parasite community of S. brasiliensis has been reported before by Luque et al. (2000). However, different patterns have already been observed for other clupeid fishes from the coastal zone of the State of Rio de Janeiro (Luque et al., 2000; Tavares et al., 2004), which suggests a heterogeneous pattern, but additional studies are needed to evaluate the community structure of clupeid fishes in the Neotropical region.
Sardinella brasiliensis showed a lack of parasite species associated pairs, but according to Rohde et al. (1995) this is a common pattern in the majority of studied marine fish. Positive and negative associations between helminth species can provide strong evidence that species interactions exist and act on community structure (Poulin, 2001). But according to Rohde et al. (1995) and Poulin (2001), interspecific relationships can only be considered valid when tested under experimental conditions.
AMADO, MAP. and FALAVIGNA, CER., 1996. New species of parasitic copepods of the genus Acusicola (Poecilostomatoida: Ergasilidae) from gill filaments of coastal and freshwater Brazilian fishes, and proposition of Acusicola rogeri n. sp. for A. tenax sensu Cressey & Collette (1970). Hydrobiologia, vol. 324, no. 3, p. 183-193. http://dx.doi.org/10.1007/BF00016390.
BUSH, AO., AHO, J. and KENNEDY, CR., 1990. Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology, vol. 4, no. 1, p. 1-20. http://dx.doi.org/10.1007/BF02270711.
BUSH, AO., LAFFERTY, KD., LOTZ, JM. and SHOSTAK, AW., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, vol. 83, no. 4, p. 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
CONE, DK. and BURT, MDB., 1982. The host specificity of Urocleidus adspectus Mueller, 1936 (Monogenea: Ancyrocephalinae). The Journal of Parasitology, vol. 68, no. 6, p. 1168-1170. http://dx.doi.org/10.2307/3281117.
FABIO, SP., 1988. Sobre tres Hemiuridae parasitos de peixes do litoral do Estado do Rio de Janeiro. Arquivos da Universidade Federal Rural do Rio de Janeiro, vol. 7, p. 157-160.
FEIJO, LMF., RODRIGUES, HO. and RODRIGUES, SS., 1979. Contribuicao ao estudo da fauna helmintologica de sardinhas (Sardinella sp.) do litoral do Estado do rio de Janeiro. Atas da Sociedade de Biologia do Rio de Janeiro, vol. 20, p. 23-27.
FERNANDES, BM. and GOULART, MB., 1989. Dinosoma clupeola sp. n.(Hemiuridae) and Pseudoacanthostomumfloridensis Nahhas & Short, 1965 (Acanthostomidae), digenetic trematodes in Brazilian marine fishes. Memorias do Instituto Oswaldo Cruz, vol. 84, no. 1, p. 103-106. http://dx.doi.org/10.1590/S007402761989000100018.
FIGUEIREDO, JL. and MENEZES, NA., 1978. Manual de Peixes marinhos do sudeste do Brasil II Teleostei. Sao Paulo: Museu de Zoologia. 110 p.
GEORGE-NASCIMENTO, MA., 1987. Ecological helminthology of wildlife animal hosts from South America: a literature review and a search for patterns in marine food webs. Revista Chilena de Historia Natural, vol. 60, p. 181-202.
IBAGY, AS. and SINQUE, C., 1985. Distribuicao de ovos e larvas de Sciaenidae (Teleostei, Perciformes) na regiao costeira do Rio Grande do Sul, Brasil. Arquivos de Biologia e Tecnologia, vol. 38, no. 1, p. 249-270.
KNOFF, M., LUQUE, JL. and AMATO JF., 1997. Community ecology of the metazoan parasites of grey mullets, Mugil platanus (Osteichthyes: Mugilidae) from the littoral of the state of Rio de Janeiro, Brazil. Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 57, no. 3, p. 441-454. PMid:9430918.
KOHN, A. and BUHRNHEIM, PF., 1964. Um novo hospedeiro e nova distribuicao geografica paraMyosaccium ecaude Montgomery, 1957 (Trematoda, Hemiuridae). Atas da Sociedade de Biologia do Rio de Janeiro, vol. 8, no. 5, p. 50-52.
KOHN, A. and SANTOS, CP., 1988. First report of Mazocroeoides georgei Price, 1936 and Mazocraeoides opisthonema Hargis, 1955 in Brazil with new synonysms (Monogenea, Mazocraeidae). Memorias do Instituto Oswaldo Cruz, vol. 83, no. 4, p. 437-440. http://dx.doi.org/10.1590/S0074-02761988000400007.
LUQUE, JL. and ALVES, DR., 2001. Ecologia das comunidades de metazoarios parasitos, do xareu, Caranx hippos (Linnaeus) e do xerelete, Caranx latus Agassiz (Osteichthyes, Carangidae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoologia, vol. 18, no. 2, p. 399-410. http://dx.doi.org/10.1590/S0101-81752001000200011.
LUQUE, JL. and CHAVES, ND., 1999. Ecologia da comunidade de metazoarios parasitos da anchova Pomatomus saltator (Linnaeus) (Osteichthyes, Pomatomidae) do litoral do Estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoologia, vol. 16, no. 3, p. 711-723. http://dx.doi.org/10.1590/S0101-81751999000300010.
LUQUE, JL. and POULIN, R., 2004. Use of fish as intermediate hosts by helminth parasites: a comparative analysis. Acta Parasitologica, vol. 49, no. 4, p. 353-361.
LUQUE, JL., AMATO, JFR. and TAKEMOTO, RM., 1996. Comparative analysis of the communities of metazoan parasites of Orthopristis ruber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the southeastern Brazilian littoral: I. structure and influence of the size and sex of hosts. Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 56, p. 279-292.
LUQUE, JL., VINAS, RA., PARAGUASSU, AR. and ALVES, DR., 2000. Metazoarios Parasitos das sardinhas Sardinella brasiliensis e Harengula clupeola (Osteichthyes, Clupeidae) do litoral do Estado do Rio de Janeiro, Brasil. Revista Universidade Rural--Serie Ciencias da Vida, vol. 22, supplement, p. 71-76.
MONTU, M., 1980. Parasite copepods of southern Brazilian fishes. I. Ergasilus euripedesi n.sp. (Copepoda: Cyclopoidea). Iheringia Serie Zoologia, vol. 56, p. 53-62.
MOREIRA, J., PASCHOAL, F., CEZAR, AD. and LUQUE, JL., 2013. Occurrence of Clavellisa ilishae (Copepoda: Lernaeopodidae) parasitizing herrings (Actinopterygii: Clupeidae) in Brazil. Revista Brasileira de Parasitologia Veterinaria, vol. 22, no. 4, p. 616-618. http://dx.doi.org/10.1590/S1984-29612013000400028. PMid:24473893.
PAIVA, MP., 1997. Recursos pesqueiros estuarinos e marinhos do Brasil. Fortaleza: UFC Edicoes. 286 p.
PALM, HW., 1997. Trypanorhynch Cestodes of commercial fishes from Northeast Brazilian coastal waters. Memorias do Instituto Oswaldo Cruz, vol. 92, no. 1, p. 69-79. http://dx.doi.org/10.1590/S0074-02761997000100014.
PEREZ-PONCE DE LEON, G., GARCIA PRIETO, L. and ROSAS VILLA C., 2000. Helmintofauna de Opisthonema libertate y Harengula thrissina (Osteichthyes: Clupeidae) de la bahia de Chamela, Jalisco, Mexico. Revista de Biologia Tropical, vol. 48, no. 4, p. 759-763. PMid:11487924.
POLYANSKY, YI.,1961. Ecology of parasites of marine fishes. In DOGIEL, AV., PETRUSHEVSKI, GK. and POLYANSKI, YI. (Eds.). Parasitology of fishes, Edinburgh: Oliver and Boyd. p. 1-47.
POLYANSKY, YI. and BYCHOWSKY, BE., 1963. Parasite fauna of sea fish. Results and perspectives of investigations by Soviet parasitologists on fish parasites in seas of the USSR. Jerusalem: Israel Program for Scientific Translations. p. 187-193.
POULIN, R., 2001. Interactions between species and the structure of helminth communities. Parasitology, vol. 122, supplement, p. S3-S11. http://dx.doi.org/10.1017/S0031182000016991. PMid:11442194.
POULIN, R., 1993. The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology, vol. 23, no. 7, p. 937-944. http://dx.doi.org/10.1016/0020-7519(93)90060-C. PMid:8106186.
RODRIGUES, HO., RODRIGUES, SS. and FARIA, Z., 1990. Contribution to the knowledge of the helminthological fauna of vertebrates of Marica, Rio de Janeiro State, Brazil. Memorias do Instituto Oswaldo Cruz, vol. 85, no. 1, p. 115-116. http://dx.doi.org/10.1590/S0074-02761990000100020.
ROHDE, K., HAYWARD, C. and HEAP, M., 1995. Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology, vol. 25, no. 8, p. 945-970. http://dx.doi.org/10.1016/0020-7519(95)00015-T PMid:8550295.
ROZSA, L., REICZIGEL, J. and MAJOROS, G., 2000. Quantifying parasites in samples of hosts. The Journal of Parasitology, vol. 86, no. 2, p. 228-232. http://dx.doi.org/10.1645/00223395(2000)086[0228:QPISOH]2.0.CO;2. PMid:10780537.
SANTOS, CP. and KOHN, A., 1992. Description of Cribomazocraes travassosi n. sp. (Monogenea: Mazocraeidae), a fish parasite from the Atlantic Ocean. Memorias do Instituto Oswaldo Cruz, vol. 87, p. 247-250. http://dx.doi.org/10.1590/S0074-02761992000500046.
SCHNEIDER, F. and SCHWINGEL, PR., 1999. Estudo preliminar da ecologia trofica da Sardinella brasiliensis na costa sudeste do Brasil. Brazilian Journal of Aquatic Science and Technology., vol. 3, no. 1, p. 67-72. http://dx.doi.org/10.14210/bjast.v3n1.p67-72.
SILVA, LO., LUQUE, JL., ALVES, DR. and PARAGUASSU, AR., 2000. Ecologia da comunidade de metazoarios parasitos do peixe-espada Trichiurus lepturus Linnaeus (Osteichthyes, Trichiuridae) do litoral do Estado do Rio de Janeiro, Brasil. Rev. Bras. Zooc., vol. 2, no. 2, p. 115-133.
TAKEMOTO, RM., AMATO, JFR. and LUQUE, JL., 1996. Comparative analysis of the metazoan parasite communities of leatherjackets, Oligoplites palometa, O. saurus, and O. saliens (Osteichthyes:Carangidae) from Sepetiba Bay, Rio de Janeiro, Brazil. Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 56, no. 4, p. 639-650. PMid:9253203.
TAVARES, LER. and LUQUE, JL., 2004. Community ecology of metazoan parasites of the later juvenile common snook Centropomus undecimalis (Osteichthyes: Centropomidae) from the coastal zone of the State of RIo de Janeiro, Brazil. Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 64, no. 3A, p. 523-529. http://dx.doi.org/10.1590/S1519-69842004000300015. PMid:15622849.
TAVARES, LE., LUQUE, JL. and BICUDO, AJ. , 2004. Metazoan parasites of Brazilian menhaden Brevoortia aurea (Spix & Agassiz, 1829) (Osteichthyes: Clupeidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Revista Brasileira de Biologia = Brazilian Journal of Biology, vol. 64, no. 3A, p. 553-554. http://dx.doi.org/10.1590/S1519-69842004000300019. PMid:15622853.
TRAVASSOS, L., FREITAS, JFT and BUHRNHEIM, PF., 1967. Relatorio da excursao do Instituto Oswaldo Cruz ao Estado do Espirito Santo em Novembro de 1964. Boletim do Museu de BiologiaMello Leitao, vol. 31, p. 1-54.
VAZ, Z. and PEREIRA, C., 1930. Um novo hemiurideo parasito de Sardinella aurita. Revista de Biologia e Hygiene, vol. 2, p. 150.
VICENTE, JJ., RODRIGUES, HO. and GOMES, DC. 1985. Nematoides do Brasil. 1a parte: nematoides de peixes. Atas da Sociedade de Biologia do Rio de Janeiro, vol. 25, p. 1-79.
VON ZUBEN, CJ., 1997. Implicacoes da agregacao espacial de parasitas para a dinamica populacional na interacao hospedeiroparasita. Revista de Saude Publica, vol. 31, no. 5, p. 523-530. http://dx.doi.org/10.1590/S0034-89101997000600014. PMid:9629733.
WALLET, M. and KOHN, A., 1987. Trematodes parasites de poisson marins du littoral de Rio de Janeiro, Bresil. Memorias do Instituto Oswaldo Cruz, vol. 82, no. 1, p. 21-27. http://dx.doi.org/10.1590/S0074-02761987000100004.
WHITEHEAD, PJP, 1985. An Annotated and IIlustrated Catalogue of the Herrings, Sardines, Pilchards, Sprats, Shads, Anchovies and Wolf-herrings. Part. 1--Chirocentridae, Clupeidae and Pristigasteridae. Rome: FAO. 303 p. FAO Fisheries Synopsis, no. 125, vol. 7.
ZAR, JH., 1996. Biostatistical Analysis. 3rd ed. New Jersey: Prentice-Hall. 662 p.
Moreira, J. (a), Paschoal, F. (b), Cezar, AD. (c) and Luque, JL. (d) *
(a) Curso de Pos-Graduacao em Ciencias Veterinarias, Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro--UFRRJ, BR 465, Km 7, CEP 23890-000, Seropedica, RJ, Brazil
(b) Programa de Pos-Graduacao em Biologia Animal, Universidade Federal Rural do Rio de Janeiro--UFRRJ, BR 465, Km 7, CEP 23890-000, Seropedica, RJ, Brazil
(c) Centro de Estudos e Pesquisas Biologicas--CEPBio, Universidade Castelo Branco--UCB, Avenida Santa Cruz, 1631, Realengo, CEP 21710-250, Rio de Janeiro, RJ, Brazil
(d) Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro--UFRRJ, CP 74540, CEP 23851-970, Seropedica, RJ, Brazil
* e-mail: firstname.lastname@example.org
Received: January 17, 2014--Accepted: March 15, 2014--Distributed: August 31, 2015
(With 1 figure)
Table 1. Prevalence, mean intensity, mean abundance, and site of infection of metazoan parasites of Sardinella brasiliensis from the coastal zone of the State of Rio de Janeiro. Parasites Prevalence (%) Mean intensity Digenea Parahemiurus merus CHIOC 94 18.9 [+ or -] 15.7 No. 37932 Myosaccium ecaude CHIOC 98 50.9 [+ or -] 61.6 No. 37933 Prodistomum gracile CHIOC 13 2.2 [+ or -] 2.0 No. 37935 Monogenea Cribomazocraes travassosi 3 1.3 [+ or -] 0.6 CHIOC No. 37938 Cestoda Callitetrarhynchus gracilis 15 1.1 [+ or -] 0.3 (plerocercoid) CHIOC No. 37936/37937 Nybelinia sp. (plerocercoid) 1 1 CHIOC No. 37939 Nematoda Hysterothylacium sp. (larval) 13 1.8 [+ or -] 1.5 CHIOC No. 35924 Pseudoterranova sp. (larval) 1 1 CHIOC No. 35925 Raphidascaris sp. (larval) 2 1 CHIOC No. 35926/35927 Copepoda Clavellisa ilishae MNRJ 4 2.8 [+ or -] 2.9 No. 23421 Nothobolochus cresseyi MNRJ 10 1.1 [+ or -] 0.3 No. 24144 Site of infection/ Parasites Mean abundance infestation Digenea Parahemiurus merus CHIOC 17.8 [+ or -] 15.9 Stomach No. 37932 Myosaccium ecaude CHIOC 49.9 [+ or -] 61.4 Stomach No. 37933 Prodistomum gracile CHIOC 0.3 [+ or -] 1.0 Intestine No. 37935 Monogenea Cribomazocraes travassosi 0.04 [+ or -] 0.2 Gills CHIOC No. 37938 Cestoda Callitetrarhynchus gracilis 0.2 [+ or -] 0.4 Body cavity (plerocercoid) CHIOC No. 37936/37937 Nybelinia sp. (plerocercoid) 0.01 [+ or -] 0.1 Body cavity CHIOC No. 37939 Nematoda Hysterothylacium sp. (larval) 0.2 [+ or -] 0.8 Mesenteries CHIOC No. 35924 Pseudoterranova sp. (larval) 0.01 [+ or -] 0.1 Mesenteries CHIOC No. 35925 Raphidascaris sp. (larval) 0.02 [+ or -] 0.1 Mesenteries CHIOC No. 35926/35927 Copepoda Clavellisa ilishae MNRJ 0.1 [+ or -] 0.7 Gills No. 23421 Nothobolochus cresseyi MNRJ 0.1 [+ or -] 0.3 Gills No. 24144 Table 2. Frequency of dominance and mean relative dominance of metazoan parasites of Sardinella brasiliensis from the coastal zone of the State of Rio de Janeiro. Frequency of Frequency of dominance Parasites dominance shared with one or more species Parahemiurus merus 15 3 Myosaccium ecaude 82 3 Parasites Mean relative dominance Parahemiurus merus 0.313 [+ or -] 0.213 Myosaccium ecaude 0.662 [+ or -] 0.222 Table 3. Values of variance to mean ratio of parasite abundance (ID) and index of Discrepancy (D) of metazoan parasites of Sardinella brasiliensis from the coastal zone of the State of Rio de Janeiro. Parasites ID D Parahemiurus merus 14.213 0.454 Myosaccium ecaude 75.513 0.538 Prodistomum gracile 3.613 0.912 Callitetrarhynchus gracilis 0.975 * 0.850 Hysterothylacium sp. 2.704 0.906 * significant values. Table 4. Concurrent species pairs of endoparasites in Sardinella brasiliensis from the coastal zone of the State of Rio de Janeiro. Parasites [chi square] P Parahemiurus merus--Myosaccium ecaude 0.13 0.718 P. merus--Prodistomum gracile 0.95 0.329 M. ecaude--P.gracile 0.31 0.581 Parasites [r.sub.s] P Parahemiurus merus--Myosaccium ecaude 0.558 * <0.0001 P. merus--Prodistomum gracile 0.231 * 0.021 M. ecaude--P.gracile 0.222 * 0.026 ([chi square]) Chi-square test; (r) values of Spearman's rank correlation coefficient. (p) significant level. * significant values. Figure 1. Distribution of species richness in the parasite infracommunities of Sardinella brasiliensis from the coastal zone of the State of Rio de Janeiro. Parasite species richness Host infected (%) 1 6 2 48 3 36 4 7 5 3 Note: Table made from bar graph.
|Printer friendly Cite/link Email Feedback|
|Author:||Moreira, J.; Paschoal, F.; Cezar, A.D.; Luque, J.L.|
|Publication:||Brazilian Journal of Biology|
|Date:||Aug 1, 2015|
|Previous Article:||Feather mites (Acari, Astigmata) associated with birds in an Atlantic Forest fragment in Northeastern Brazil/ Acaros de pena (Acari: Astigmata)...|
|Next Article:||Bird assemblage mist-netted in an Atlantic Forest area: a comparison between vertically-mobile and ground-level nets/Assembleia de aves capturadas em...|