Metazoan parasites of Geophagus brasiliensis (Perciformes: Cichlidae) in Patos lagoon, extreme south of Brazil

Metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) da Lagoa dos Patos, extremo sul do Brasil

Gabriela Lopes Rassier Tatiana Cheuiche Pesenti Joaber Pereira Júnior Diego Silva da Silva Emília Welter Wendt Cassandra de Moraes Monteiro Maria Elizabeth Aires Berne About the authors

Abstract

This study has evaluated the parasitic fauna of 79 pearl cichlids (Geophagus brasiliensis) from the estuary of Patos Lagoon (31° 57' S and 52° 06' W), Rio Grande do Sul, Brazil, during the months of May and June in 2011 and 2012. All the hosts analyzed were infected with at least one species of parasite. A total of eleven metazoa were identified in 459 specimens collected. The trematode Austrodiplostomum compactum (34.2%) and ergasilids Ergasilus lizae (32.9%) and Gauchergasilus lizae (32.9%) were the most prevalent species. The trematodes Thometrema overstreeti and Posthodiplostomum sp. had significantly higher prevalence in fish longer than 20 cm. The sex of the host had no effect on parasite prevalence and abundance. Pearl cichlids are registered as a new host for the trematodes Lobatostoma sp., Homalometron pseudopallidum and Thometrema overstreeti, for the ergasilids Ergasilus lizae and Gauchergasilus euripedesi and for the argulid Argulus spinolosus. The crustacean E. lizae is recorded in Rio Grande do Sul for the first time.

Keywords:
Helminths; Crustacea; Hirudinea; Cichlidae; parasitological indices

Resumo

Este estudo avaliou a fauna parasitária de 79 Geophagus brasiliensis (acarás) proveniente do Estuário da Lagoa dos Patos (31°57’S e 52°06’W), Rio Grande do Sul, no período de Maio e Junho de 2011 a 2012. Todos os hospedeiros analisados estavam infectados com pelo menos uma espécie de parasito. Um total de onze metazoários foi identificado em 459 espécimes coletados. O trematoda Austrodiplostomum compactum (34,2%) e os ergasilídeos Ergasilus lizae (32,9%) e Gauchergasilus lizae (32,9%) foram às espécies mais prevalentes. Os trematodeos Thometrema overstreeti e Posthodiplostomum sp. apresentaram uma prevalência significativamente maior nos peixes acima de 20 cm. O gênero sexual dos hospedeiros não apresentou influência sobre a prevalência e a abundância parasitária. Geophagus brasiliensis é registrado como um novo hospedeiro para os trematódeos Lobatostoma sp., Homalometron pseudopallidum e Thometrema overstreeti, para os ergasilídeos Ergasilus lizae e Gauchergasilus euripedesi e para o argulídeo Argulus spinolosus. O crustáceo E. lizae é registrado pela primeira vez no Rio Grande do Sul.

Palavras-chave:
Helmintos; Crustacea; Hirudinea; Cichlidae; índices parasitológicos

Introduction

The Patos Lagoon, located in the southernmost area of Brazil, is 265 km long and has 10.000 km2 of surface area. It is thus one of the largest coastal lagoons in the world. The estuary of the Patos Lagoon encompasses over 900 km2 in the southernmost area of the lagoon (BONILHA & ASMUS, 1994Bonilha LE, Asmus ML. Modelo ecológico do fitoplâncton e zooplâncton do estuário da Lagoa dos Patos, RS. Publ Acad Ciências Est 1994; 87(1): 347-362.).

Although there is great diversity of fish in the estuary of the Patos Lagoon, there are few studies on the parasitic fauna of these fish. In the area of the estuary, parasitological studies have been conducted on Micropogonias furnieri (Desmarest, 1823) (VELLOSO & PEREIRA, 2010Velloso AL, Pereira J Jr. Influence of ectoparasitism on the welfare of Micropogonias furnieri.Aquaculture 2010; 310(1-2): 43-46. http://dx.doi.org/10.1016/j.aquaculture.2010.10.030.
http://dx.doi.org/10.1016/j.aquaculture....
), Paralichthys orbignyanus (Valenciennes, 1839) (VELLOSO et al., 2005Velloso AL, Pereira J Jr, Cousin JCB. Therodamas fluviatilis (Copepoda: Ergasilidae), parasito de (Teleostei: Paralichthyidae) do estuário da Lagoa dos Patos e costa adjacente, RS, Brasil. Paralichthys orbignyanusBol Inst Pesca 2005; 31: 65-71.) and Mugil platanus (Günther, 1880) (EIRAS et al., 2007Eiras JC, Abreu PC, Robaldo R, Pereira J Jr. Myxobolus platanus n. sp. (Myxosporea: Myxobolidae), a parasite of Günther, 1880 (Osteichthyes: Mugilidae) from Lagoa dos Patos, RS, Brazil. Mugil platanusArq Bras Med Vet Zootec 2007; 59(4): 895-898. http://dx.doi.org/10.1590/S0102-09352007000400012.
http://dx.doi.org/10.1590/S0102-09352007...
).

Parasite diversity in host fish depends directly on the degree of diversity of the habitat (D’AMELIO & GERASI 1997D’Amelio S, Gerasi L. Evaluation of environmental deterioration by analysing fish parasite biodiversity and community structure. Parassitologia 1997; 39(3): 237-241. PMid:9802073.; GELNAR et al., 1997Gelnar M, Sebelová S, Dusek L, Koubková B, Jurajda P, Zahrádková S. Biodiversity of parasites in freshwater environment in relation to pollution. Parassitologia 1997; 39(3): 189-199. PMid:9802067.). Thus, many studies have been conducted regarding the use of fish parasites as environmental bioindicators (SURES, 2003Sures B. Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 2003; 126(7 Suppl): S53-S60. http://dx.doi.org/10.1017/S003118200300372X. PMid:14667172.
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, 2004Sures B. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol 2004; 20(4): 170-177. http://dx.doi.org/10.1016/j.pt.2004.01.014. PMid:15099556.
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; MARCOGLIESE, 2005Marcogliese DJ. Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 2005; 35(7): 705-716. http://dx.doi.org/10.1016/j.ijpara.2005.01.015. PMid:15925594.
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; NACHEV et al., 2010Nachev M, Zimmermann S, Rigaud T, Sures B. Is metal accumulation in dependent on parasite sex or infrapopulation size? Pomphorhynchus laevisParasitology 2010; 137(8): 1239-1248. http://dx.doi.org/10.1017/S0031182010000065. PMid:20380766.
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; VIDAL-MARTÍNEZ et al., 2010Vidal-Martínez VM, Pech D, Sures B, Purucker T, Poulin R. Can parasites really reveal environmental impact? Trends Parasitol 2010; 26(1): 44-51. http://dx.doi.org/10.1016/j.pt.2009.11.001. PMid:19945346.
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; KHAN, 2011Khan RA. Chronic exposure and decontamination of a marine sculpin (Myoxocephalus scorpius) to Polychlorinated Biphenyls using selected body indices, blood values, histopathology, and parasites as bioindicators. Arch Environ Contam Toxicol 2011; 60(3): 479-485. http://dx.doi.org/10.1007/s00244-010-9547-9. PMid:20559629.
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).

In aquaculture, situations that lead to the rupture of the host-parasite-environment balance can trigger disease outbreaks. In addition to the consequences of parasitism itself, parasitized fish are more susceptible to secondary infections by bacteria and fungi. Thus, their zootechnical and reproductive performances are compromised and they transmit pathogenic agents to the farming environment, thereby leading to great economic losses (MARTINS, 1998Martins ML. Doenças infecciosas e parasitárias de peixes. Jaboticabal: FUNEP; 1998. Boletim Técnico do centro de Aquicultura da UNESP, vol. 3.; LIMA & LEITE, 2006Lima LC, Leite RC. Boas coletas garantem bons diagnósticos. Panorama da Aquicultura 2006; 16(96): 24-29.).

In relation to public health, parasitic zoonoses transmitted through fish consumption have increasingly drawn the attention of researchers and sanitation authorities worldwide, due to consumption of raw or insufficiently cooked fish (BOUREE et al., 1995Bouree P, Paugam A, Petithory JC. Anisakidosis: report of 25 cases and review of the literature. Comp Immunol Microbiol Infect Dis 1995; 18(2): 75-84. http://dx.doi.org/10.1016/0147-9571(95)98848-C. PMid:7621671.
http://dx.doi.org/10.1016/0147-9571(95)9...
; LUQUE, 2004Luque JL. Biologia, epidemiologia e controle de parasitos de peixes. Rev Bras Parasitol Vet 2004; 13(S1): 161-165.).

Geophagus brasiliensis (Quoy & Gaimard 1824), known as the acará, caraúna, acará-ferreira or pearl cichlid, occurs in rivers, streams and ponds in South and Central America. This species is used in recreational fishing in fee-fishing ponds because they can easily reproduce and also in the aquarium trade due to their attractive coloration (BIZERRIL & PRIMO, 2001Bizerril CRSF, Primo PBS. Peixes de águas interiores do estado do Rio de Janeiro. Rio de Janeiro: Fundação de Estudos do Mar; 2001.). Studies conducted with the aim of using G. brasiliensis in aquaculture in southern Brazil have shown that it presents good development in cold waters, thus highlighting the importance of using a native fish species as an alternative for diversifying species in a farming system (AMARAL et al., 2011Amaral H Jr, Argento JR No, Garcia S, Mello GL. Pesquisa de comparação entre a taxa de crescimento do Acará e a Tilápia . Geophagus brasiliensisOreochromis niloticus em condições de monocultivo intensivo utilizando ração e alimento vivoRev Electrón Vet 2011; 12(9): 1-22.).

During the initial development stages of G. brasiliensis, these fish are plankton-eaters (LAZZARO, 1991Lazzaro X. Feeding convergence in South American and African zooplanktivorous cichlids and Geophagus brasiliensisTilapia rendalli.Environ Biol Fishes 1991; 31(3): 283-293. http://dx.doi.org/10.1007/BF00000693.
http://dx.doi.org/10.1007/BF00000693...
). Later on, they become omnivorous bottom-dwellers and present territorial behavior (BEATTY et al., 2013Beatty SJ, Morgan DL, Keleher J, Allen MG, Sarre GA. The tropical South American cichlid, in Mediterranean climatic south-western Australia. Geophagus brasiliensisAquatic Invasions 2013; 8(1): 21-36. http://dx.doi.org/10.3391/ai.2013.8.1.03.
http://dx.doi.org/10.3391/ai.2013.8.1.03...
). However, this characteristic, as well as marked differences in behavior and size (length and weight) between males and females, is reflected in the composition and mean value of their food consumption. In addition, for G. brasiliensis in the Patos/Mirim lagoon system, gastropods are the most important component of their diet (40.64% among adult males and 35.55% among adult females), with important variations in diet relating to the stage of maturity of this host (BASTOS et al., 2011Bastos RF, Condini MV, Varela AS Jr, Garcia AM. Diet and food consumption of the pearl cichlid Geophagus brasiliensis (Teleostei: Cichlidae): relationships with gender and sexual maturity. Neotrop Ichthyol 2011; 9(4): 825-830. http://dx.doi.org/10.1590/S1679-62252011005000049.
http://dx.doi.org/10.1590/S1679-62252011...
). In Brazil, studies on helminths parasitizing G. brasiliensis have been reported in the Rio de Janeiro (PARAGUASSU et al., 2005Paraguassú AR, Alves DR, Luque JL. Metazoários parasitos do acará Geophagus brasiliensis (Quoy; Gaimard, 1824) (Osteichthyes: Cichlidae) do reservatório de Lajes, estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 2005; 14(1): 35-39. PMid:16153342.; AZEVEDO et al., 2006Azevedo RK, Abdallah VD, Luque JL. Ecologia da comunidade de metazoários parasitos do acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2006; 28(4): 403-411.; CARVALHO et al., 2010Carvalho AR, Tavares LER, Luque JL. Variação sazonal dos metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) no rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2010; 32(2): 159-167.) Parana (BELLAY et al., 2012Bellay S, Ueda BH, Takemoto RM, Lizama MAP, Pavanelli GC. Fauna parasitária de (Perciformes: Cichlidae) em reservatórios do estado do Paraná, Brasil. Geophagus brasiliensisR Bras Bioci Porto Alegre 2012; 10(1): 74-78.). Because of the importance of parasitic diseases in fish with regard to public health and, and as environmental bioindicators. The present study was proposed with the objective of identifying the parasitic fauna and its infection levels in G. brasiliensis from the southernmost area of Brazil.

Material and Methods

A total of 79 specimens of G. brasiliensis (30 females, 43 males and six unidentified), were collected from the estuary of the Patos Lagoon by local fishermen using nets and casting nets, in the months of May and June in 2011 and 2012. After the fish had been caught, they were placed in a polystyrene box with ice and were transported to the Parasitology Laboratory of the Federal University of Pelotas. Firstly, the fish were measured (total length [TL] and standard length [SL]) and weighed, and a thorough external evaluation was performed in order to collect ectoparasites. Next, the fish were necropsied. Their organs were removed and placed individually in Petri dishes for helminth inspection.

Collection, fixation and quantification of parasites were performed in accordance with Eiras et al. (2006)Eiras JC, Takemoto RM, Ricardo M, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: Eduem; 2006.. Prevalence, mean intensity and mean abundance values were calculated in accordance with Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
. The influence of the sex of the host on the abundance and prevalence of parasitic infections was analyzed through the Bootstrap-t test and chi-square test respectively, and p ≤ 0.05 was taken to be significant. Pearson’s correlation coefficient was used to determine possible correlations between the total length of the host and the prevalence of parasitic infection. The samples from the hosts were separated into nine class intervals of amplitude 2 cm, with previous angular transformation of the prevalence data (ZAR, 1999Zar JH. Biostatistical analysis. 4th ed. New Jersey: Prentice Hall; 1999.). Spearman's rank correlation coefficient (“rs”) was used for determining the correlation between the standard length and abundance of parasite species (ZAR, 1999Zar JH. Biostatistical analysis. 4th ed. New Jersey: Prentice Hall; 1999.).

Results

The biometric parameters of Geophagus brasiliensis evaluated are described in Table 1.

Table 1
Biometric parameters of 30 females and 43 males of Geophagus brasiliensis during May and June 2011 and 2012, in Patos Lagoon, Rio Grande do Sul, Brazil.

All the hosts were infected by at least one species of metazoan parasite. A total of 459 specimens of metazoan parasites were found, and eleven genera and eight species were identified (Table 2). Digeneans were the most diverse group, represented by six species. Metacercariae of Austrodiplostomum compactum (Lutz, 1928) were found in the eyes of the hosts (Figure 1a, b) and were the most prevalent trematode (34.2%), followed by Lobatostoma sp. (28.76%), which was found in the intestines. Among the ectoparasites, the ergasilids Ergasilus lizae (Kroyer, 1863), Gauchergasilus euripedesi (Montú, 1980) (32.9%) and Glossiphinidae gen. sp (24.05%) predominated, parasitizing the gills.

Table 2
Parasitological indexes of metazoans from Geophagus brasiliensis (n = 79) from Patos Lagoon, Rio Grande do Sul, Brazil.
Figure 1
(a) The eye of the Geophagus brasiliensis infected by metacercariae of Austrodiplostomum compactum. (b) Detail showing the metacercariae of A. compactum in the eye of the G. brasiliensis.

Thometrema overstreeti (Brooks et al., 1979) (adults in the intestines) and Posthodiplostomum sp. (metacercariae in the eyes and on the surface of the swim bladder) presented significantly higher prevalence in fish longer than 20 cm. The sex of the host did not present any influence on the prevalence or abundance of the metazoan parasites found in G. brasiliensis.

Discussion

Eleven parasite taxa were identified, with greatest representation of trematodes, as also observed in studies conducted in Rio de Janeiro on this same host (AZEVEDO et al., 2006Azevedo RK, Abdallah VD, Luque JL. Ecologia da comunidade de metazoários parasitos do acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2006; 28(4): 403-411.; CARVALHO et al., 2010Carvalho AR, Tavares LER, Luque JL. Variação sazonal dos metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) no rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2010; 32(2): 159-167.). This is probably due to the omnivorous-opportunistic habits of these fish and because they cohabit with a wide diversity of intermediate hosts, since many of these trematodes use two or more hosts to complete their biological cycle (EIRAS, 1994Eiras JC. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida; 1994.). In addition, G. brasiliensis is a benthic species, and this habit favors contact with mollusks, which act as intermediate hosts for trematodes (MARCOGLIESE, 2002Marcogliese DJ. Food webs and the transmission of parasites to marine fish. Parasitology 2002; 124(7 Suppl): S83-S99. http://dx.doi.org/10.1017/S003118200200149X. PMid:12396218.
http://dx.doi.org/10.1017/S0031182002001...
).

Metacercariae of A. compactum presented the highest prevalence (34.2%) among the parasites reported. Santos et al. (2012)Santos RS, Marchiori N, Santarém VA, Takahashi HK, Mouriño JLP, Martins ML. Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in the eyes of fishes from Paraná River, Brazil. Acta Sci Biol Sci 2012; 34(2): 225-231. http://dx.doi.org/10.4025/actascibiolsci.v34i2.9337.
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analyzed Geophagus surinamensis (Bloch, 1791) and observed higher prevalence (46.1%), which was associated with water temperatures that ranged from 21.4 to 29°C. Previous studies also suggested that the biology of this parasite depends on high temperatures (MARTINS et al., 2002Martins ML, Mello A, Paiva FC, Fujimoto RY, Schalch SHC, Colombano NC. Prevalência, sazonalidade e intensidade de infecção por Lutz, 1928 (Digenea, Diplostomidae), em peixes do reservatório de Volta Grande, Estado de Minas Gerais, Brasil. Diplostomum (Austrodiplostomum) compactumActa Sci Biol Sci 2002; 24(2): 469-474.; HAKALAHTI et al., 2006Hakalahti T, Karvonen A, Valtonen ET. Climate warming and disease risks in temperate regions– Argulus coregoni and Diplostomum spathaceum as case studies. J Helminthol 2006; 80(2): 93-98. http://dx.doi.org/10.1079/JOH2006351. PMid:16768854.
http://dx.doi.org/10.1079/JOH2006351...
). In the present study, although the prevalence of this trematode was 34.2%, all the sampling was performed between May and June, when the mean environmental temperatures are lower. Cercariae are probably released from gastropods during periods of higher temperatures, thus resulting in accumulation of the parasites in colonization processes that occur during these higher-temperature periods. The fact that gastropod mollusks comprise the main component of the diet of G. brasiliensis in the Patos/Mirim lagoon system may have contributed to these values (BASTOS et al., 2011Bastos RF, Condini MV, Varela AS Jr, Garcia AM. Diet and food consumption of the pearl cichlid Geophagus brasiliensis (Teleostei: Cichlidae): relationships with gender and sexual maturity. Neotrop Ichthyol 2011; 9(4): 825-830. http://dx.doi.org/10.1590/S1679-62252011005000049.
http://dx.doi.org/10.1590/S1679-62252011...
). Moreover, the same authors showed that significant variation in the diet occurs, according to the host’s maturity stage. Other facts may have favored transmission, such as strategies of releasing cercariae close to the intermediate host and the lentic condition of the environment (SANTOS et al., 2012Santos RS, Marchiori N, Santarém VA, Takahashi HK, Mouriño JLP, Martins ML. Austrodiplostomum compactum (Lutz, 1928) (Digenea, Diplostomidae) in the eyes of fishes from Paraná River, Brazil. Acta Sci Biol Sci 2012; 34(2): 225-231. http://dx.doi.org/10.4025/actascibiolsci.v34i2.9337.
http://dx.doi.org/10.4025/actascibiolsci...
). Regarding the infection site of A. compactum in the host, this has been recorded on the surface of the swim bladder (CARVALHO et al., 2012Carvalho AR, Azevedo RK, Abdallah VD, Luque JLF. Metacercárias livres de Diplostomidae (Digenea: Diplostomidea) em (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Geophagus brasiliensisActa Sci Biol Sci 2012; 34(2): 233-239. http://dx.doi.org/10.4025/actascibiolsci.v34i2.5957.
http://dx.doi.org/10.4025/actascibiolsci...
). However in the present study, in which total necropsies were performed, metacercariae of A. compactum were only reported in the eyes of G. brasiliensis, which makes it possible to accept the hypothesis postulated by Eiras (1994)Eiras JC. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida; 1994., i.e. that different species of Displostomidae can present specificity for infection sites in the host.

In the present study, Lobatostoma sp. is reported for the first time in G. brasiliensis. Lobatostoma jungwirthi was described in Geophagus brachyurus (Cope, 1894) in the Sinos River, São Leopoldo, RS, Brazil, by Kritscher (1974)Kritscher E. Lobatostoma jungwirthi nov. spec. (Aspidocotylea, Aspidogastridae) aus Cope, 1894 (Pisc., Cichlidae). Geophagus brachyurusAnn Naturhistor Mus Wien 1974; 78: 381-384.. This same species was recorded in the freshwater mollusk Heleobia castellanosae (Gaillard, 1974) in Buenos Aires, and this is the only species that parasites freshwater fish. Thus, it can be suggested that the Lobatostoma sp. reported here may be the same species described by Zylber & Nunez (1999)Zylber MI, Núñez MO. Some aspects of the development of Kritscher, 1974 (Aspidogastrea) in snails and cichlid fishes from Buenos Aires, Argentina. Lobatostoma jungwirthiMem Inst Oswaldo Cruz 1999; 94(1): 31-35. http://dx.doi.org/10.1590/S0074-02761999000100010.
http://dx.doi.org/10.1590/S0074-02761999...
. According to these authors, the lifecycle of L. jungwirthi is heteroxenous and very similar to what was described by Rohde & Sandland (1973)Rohde K, Sandland R. Host parasite relations in Rohde (Trematoda: Aspidogastrea). Lobatostoma manteriZ Parasitenkd 1973; 42(2): 115-136. http://dx.doi.org/10.1007/BF00329789. PMid:4764658.
http://dx.doi.org/10.1007/BF00329789...
, Rohde (1994)Rohde K. The minor groups of parasitic platyhelminthes. Adv Parasitol 1994; 33: 145-234. http://dx.doi.org/10.1016/S0065-308X(08)60413-3. PMid:8122566.
http://dx.doi.org/10.1016/S0065-308X(08)...
for Lobatostoma manteri, because both species need a vertebrate host to complete their lifecycles. Rohde & Sandland (1973)Rohde K, Sandland R. Host parasite relations in Rohde (Trematoda: Aspidogastrea). Lobatostoma manteriZ Parasitenkd 1973; 42(2): 115-136. http://dx.doi.org/10.1007/BF00329789. PMid:4764658.
http://dx.doi.org/10.1007/BF00329789...
observed that in mollusks, the larvae hatch in the stomach and, depending on the species, remain in this organ or migrate to the digestive glands, where they grow until the pre-adult stage, presenting all the adult characteristics, including one testicle and ovary. However, they do not eliminate eggs, and fish are infected through ingestion of these mollusks. Thus, the transmission of this trematode must be associated with ingestion of gastropod mollusks, which are one of the main components of the diet of G. brasiliensis in the Patos/Mirim lagoon system (BASTOS et al., 2011Bastos RF, Condini MV, Varela AS Jr, Garcia AM. Diet and food consumption of the pearl cichlid Geophagus brasiliensis (Teleostei: Cichlidae): relationships with gender and sexual maturity. Neotrop Ichthyol 2011; 9(4): 825-830. http://dx.doi.org/10.1590/S1679-62252011005000049.
http://dx.doi.org/10.1590/S1679-62252011...
).

Black spot disease, which occurs frequently in many species of fish, is caused by a variety of parasite species but predominantly by metacercariae of Posthodiplostomum sp. In the present study, metacercariae of Posthodiplostomum sp. were found in the eyes and on the surface of the swim bladder. Azevedo et al. (2006)Azevedo RK, Abdallah VD, Luque JL. Ecologia da comunidade de metazoários parasitos do acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2006; 28(4): 403-411. reported P. macrocotyle (Dubois, 1937) in G. brasiliensis, in their eyes, mouth cavity, stomach and gonads.

The presence of metacercariae of Clinostomum sp. on the external surface of the fish causes black spot or yellow spot disease, which can lead to economic losses because it hampers commercialization of the fish, can cause death among young hosts and also makes them more susceptible to attack by predators. Metacercariae of Clinostomum marginatum (Rudolphi, 1819) were found in the fins of G. brasiliensis. There are previous records of this parasite in other species of cichlids such as Cichla ocellaris (Bloch & Schneider, 1801) and Crenicichla sp., in their gills, skin and fins (THATCHER, 1981Thatcher VE. Patologia de peixes da Amazônia Brasileira, 1. Aspectos gerais. Acta Amazon 1981; 11(1): 125-140.). Clinostomum sp. was also reported by Paraguassú et al. (2005)Paraguassú AR, Alves DR, Luque JL. Metazoários parasitos do acará Geophagus brasiliensis (Quoy; Gaimard, 1824) (Osteichthyes: Cichlidae) do reservatório de Lajes, estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 2005; 14(1): 35-39. PMid:16153342. in the fins of G. brasiliensis with lower prevalence (3%).

This was the first report of Thometrema overstreeti in G. brasiliensis. It has already been reported in Pimelodus maculatus (Lacépéde, 1803) in southern Brazil (KOHN et al., 1990Kohn A, Fernandes BMM, Gibson DI, Fróes OM. On the Brazilian species of Halipegine genera (Trematoda: Derogenidae) from fishes, with new morphological data, hosts and synonyms. Syst Parasitol 1990; 16(3): 201-211. http://dx.doi.org/10.1007/BF00009148.
http://dx.doi.org/10.1007/BF00009148...
). The latter is also an opportunistic omnivorous bottom-dwelling fish, which allows completion of the parasite’s cycle.

Another trematode found in G. brasiliensis in this study was Homalometron pseudopallidum (Martorelli, 1986), which has been reported in over 20 species of fish, especially marine fish, but with few records in freshwater fish. Thus, this was the first report of H. pseudopallidum in G. brasiliensis. This species was reported in Gymnogeophagus australis (Eigenmann, 1907) in Argentina (KOHN et al., 2007Kohn A, Fernandes BMM, Cohen SC. South Americam trematodes parasites of fishes. Rio de Janeiro: Fiocruz; 2007.). Both of these hosts belong to the same family; they share the same feeding habit and co-occur in rivers and ponds in southern Brazil (REIS & MALABARBA, 1987Reis RE, Malabarba LR. Revision of the Neotropical cichlid genus Ribeiro, 1918, with descriptions of two new species (Pisces, Perciformes). GymnogeophagusRev Bras Zool 1987; 4(4): 259-305. http://dx.doi.org/10.1590/S0101-81751987000400002.
http://dx.doi.org/10.1590/S0101-81751987...
).

The only nematode detected was Contracaecum sp. (Anisakidae), which was found in the larval stage. Species of Contracaecum sp. are of public health importance because they are responsible for emerging diseases such as anisakiasis, which affects humans after consuming raw or poorly cooked fish dishes, such as sushi, sashimi and ceviche (MINETA et al., 2006Mineta S, Shimanuki A, Sugiura Y, Tsuchiya M, Kaneko Y, Sugiyama K, et al. Chronic anisakiasis of the ascending colon associated with carcinoma. J Nippon Med Sch 2006; 73(3): 169-174. http://dx.doi.org/10.1272/jnms.73.169. PMid:16790986.
http://dx.doi.org/10.1272/jnms.73.169...
; FELIZARDO et al., 2009Felizardo NN, Knoff M, Pinto RM, Gomes DC. Larval anisakid nematodes of the flounder Jordan, 1890 (Piscei: Teleostei) from Brazil. Paralichthys isoscelesNeotrop Helminthol 2009; 3(2): 57-64.). No cases of this have been reported in humans in Brazil, although there have been reports of occurrences of larvae of anisakids in various fish (BARROS et al., 2006Barros LA, Moraes J Fo, Oliveira RL. Nematóides com potencial zoonótico em peixes com importância econômica provenientes do rio Cuiabá. Rev Bras Ci Vet 2006; 13(1): 55-57., 2007Barros LA, Moraes J Fo, Oliveira RL. Larvas de nematóides de importância zoonótica encontradas em traíras (Hoplias malabaricus bloch, 1794) no município de Santo Antonio do Leverger, MT. Arq Bras Med Vet Zootec 2007; 59(2): 533-535. http://dx.doi.org/10.1590/S0102-09352007000200042.
http://dx.doi.org/10.1590/S0102-09352007...
; SAAD & LUQUE, 2009Saad CDR, Luque JL. Larvas de Anisakidae na musculatura do pargo, , no Estado do Rio de Janeiro, Brasil. Pagrus pagrusRev Bras Parasitol Vet 2009; 18(Suppl S1): 71-73. http://dx.doi.org/10.4322/rbpv.018e1014. PMid:20040196.
http://dx.doi.org/10.4322/rbpv.018e1014...
; KNOFF et al., 2013Knoff M, São Clemente CS, Fonseca MCG, Felizardo NN, Lima FC, Pinto RM, et al. Anisakidae nematodes in the blackfin goosefish, Miranda-Ribeiro, 1915 purchased in the State of Rio de Janeiro, Brazil. Lophius gastrophysusActa Sci Biol Sci 2013; 35(1): 129-133. http://dx.doi.org/10.4025/actascibiolsci.v35i1.12185.
http://dx.doi.org/10.4025/actascibiolsci...
; MATTOS et al., 2014Mattos DPBG, Lopes LMS, Verícimo MA, Alvares TS, São Clemente SC. Anisakidae larvae infection in five commercially important fish species from the State of Rio de Janeiro, Brazil. Rev Bras Med Vet 2014; 36(4): 375-379.). Reports of larvae of Contracaecum sp. sampled in G. brasiliensis in Brazil have presented higher rates, as reported by Paraguassú et al. (2005)Paraguassú AR, Alves DR, Luque JL. Metazoários parasitos do acará Geophagus brasiliensis (Quoy; Gaimard, 1824) (Osteichthyes: Cichlidae) do reservatório de Lajes, estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 2005; 14(1): 35-39. PMid:16153342. (14%) and Bellay et al. (2012)Bellay S, Ueda BH, Takemoto RM, Lizama MAP, Pavanelli GC. Fauna parasitária de (Perciformes: Cichlidae) em reservatórios do estado do Paraná, Brasil. Geophagus brasiliensisR Bras Bioci Porto Alegre 2012; 10(1): 74-78. (40.62%) in reservoirs in the states of Rio de Janeiro and Paraná, respectively. In turn, in studies conducted in the Guandu River in the state of Rio de Janeiro, Azevedo et al. (2006)Azevedo RK, Abdallah VD, Luque JL. Ecologia da comunidade de metazoários parasitos do acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2006; 28(4): 403-411. and Carvalho et al. (2010)Carvalho AR, Tavares LER, Luque JL. Variação sazonal dos metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) no rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2010; 32(2): 159-167. both observed a prevalence of 6%, i.e. close to what was found in the present study. These differences may be associated with the time at which sampling was performed, as well as with the availability of hosts used by G. brasiliensis in its food chain. Although larvae of Contracaecum sp. were only found in the intestinal lumen of G. brasiliensis at low parasitological levels, the zoonotic risk is not eliminated, given that there is a possibility of migration of these larvae to the muscle tissue of the host, both in the living fish and after capture, especially because of the length of time for which the fish remain in the boat and/or in the fish warehouse, without being eviscerated, as well as through the use of viscera in typical dishes (BOUREE et al., 1995Bouree P, Paugam A, Petithory JC. Anisakidosis: report of 25 cases and review of the literature. Comp Immunol Microbiol Infect Dis 1995; 18(2): 75-84. http://dx.doi.org/10.1016/0147-9571(95)98848-C. PMid:7621671.
http://dx.doi.org/10.1016/0147-9571(95)9...
; LYMBERY & CHEACH, 2007Lymbery AJ, Cheah FY. Anisakid nematodes and anisakiasis. In: Murrell KD, Fried B, editors. Food-borne parasitic zoonoses. New York: Springer; 2007. p. 185-207. World Class Parasites, vol. 11. http://dx.doi.org/10.1007/978-0-387-71358-8_5.
http://dx.doi.org/10.1007/978-0-387-7135...
).

Regarding ectoparasites, the argulid Argulus spinulosus (Silva, 1980), ergasilids E. lizae and G. euripedesi and leeches Glossiiphonidae gen. sp. (Hirudinea) were identified.

Argulus spinolosus has already been reported in another cichlid, Oreochromis niloticus (Linnaeus, 1758), in traditional fish-farming tanks in Santa Catarina, with prevalence of 33% (GHIRALDELLI et al., 2006Ghiraldelli L, Martins ML, Jerônimo GT, Yamashita MM, Adamante WB. Ectoparasites communities from cultivated in the State of Santa Catarina, Brazil. Oreochromis niloticusJ Fish Aquatic Sci 2006; 1(2): 181-190. http://dx.doi.org/10.3923/jfas.2006.181.190.
http://dx.doi.org/10.3923/jfas.2006.181....
), i.e. greater than what was found in G. brasiliensis in the present study (7.59%). During the reproduction period of argulids, females abandon the host and search for solid substrates to lay their eggs. Infecting larvae are able to swim and infect new fish, thus continuing the lifecycle (EIRAS, 1994Eiras JC. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida; 1994.). Thus, the confined fish-farming environment can facilitate the lifecycle of argulids (GOMES & MALTA, 2002Gomes AL, Malta JCO. Postura, desenvolvimento e eclosão dos ovos de Lemos de Castro (Crustacea, Brachiura) em laboratório, parasita de peixes da Amazônia Central. Dolops carvalhoiRev Bras Zool 2002; 19: 141-149. http://dx.doi.org/10.1590/S0101-81752002000600013.
http://dx.doi.org/10.1590/S0101-81752002...
).

The ergasilid G. euripedesi is widely distributed in estuarine waters, from the state of Rio Grande do Sul to Sergipe (MONTÚ & BOXSHALL, 2002Montú MA, Boxshall GA. , a new genus for Montú, 1980, an abundant parasitic copepod from the Patos Lagoon in southern Brazil. GauchergasilusErgasilus euripedesiSyst Parasitol 2002; 51(1): 21-28. http://dx.doi.org/10.1023/A:1012985717903. PMid:11721192.
http://dx.doi.org/10.1023/A:101298571790...
). This ergasilid has already been reported in the gills of M. furnieri, which were also sampled in the same estuary of Patos Lagoon (VELLOSO & PEREIRA, 2010Velloso AL, Pereira J Jr. Influence of ectoparasitism on the welfare of Micropogonias furnieri.Aquaculture 2010; 310(1-2): 43-46. http://dx.doi.org/10.1016/j.aquaculture.2010.10.030.
http://dx.doi.org/10.1016/j.aquaculture....
).

Ergasilus lizae has already been reported parasitizing the gill filaments of Mugil curema (Valenciennes, 1836) (CAVALCANTI et al., 2011Cavalcanti ETS, Takemoto RM, Alves LC, Chellappa S, Pavanelli G. Ectoparasitic crustaceans on mullet, (Osteichthyes: Mugilidae) in the coastal waters of Rio Grande do Norte State, Brazil. Mugil curemaActa Sci Biol Sci 2011; 33(3): 357-362.) and Mugil planatus (Günther, 1880) (LUQUE & TAVARES, 2007Luque JL, Tavares LER. Checklist of Copepoda associated with fishes from Brazil. Zootaxa 2007; 1579: 1-39.) in the state of Rio Grande do Norte. For the state of Rio Grande do Sul, this is a new record of occurrence. When fixed in the gills, they cause partial or total occlusion of the blood vessels of the lamellae, as well as hyperplasia and increased mucus, thus causing reduction of the respiratory ability of the host and facilitating occurrences of secondary infections (EIRAS, 1994Eiras JC. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida; 1994.).

Glossiphoniidae is composed of species that occur in freshwater environments on all continents except Antarctica. In the gills of G. brasiliensis, in the present study, the prevalence of parasitism due to leeches Glossiphoniidae gen. sp. (13.7%) was similar (10%) to what was observed in Guandu River in Rio de Janeiro (AZEVEDO et al., 2006Azevedo RK, Abdallah VD, Luque JL. Ecologia da comunidade de metazoários parasitos do acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Perciformes: Cichlidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Sci Biol Sci 2006; 28(4): 403-411.). However, this was lower that the values observed in the Lajes reservoir in the same state (74%) (PARAGUASSÚ et al., 2005Paraguassú AR, Alves DR, Luque JL. Metazoários parasitos do acará Geophagus brasiliensis (Quoy; Gaimard, 1824) (Osteichthyes: Cichlidae) do reservatório de Lajes, estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 2005; 14(1): 35-39. PMid:16153342.). According to Eiras (1994)Eiras JC. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida; 1994., the most important consequence of this parasitic disease is that leeches have the ability to transmit protozoa and other pathogens such as Trypanosoma spp. and haemogregarines, to fish.

The helminths T. overstreeti and Posthodiplostomum sp. presented a correlation between body length and prevalence, thus indicating that larger fish present higher chances of becoming infected by parasites. This corroborates the affirmation of Takemoto & Pavanelli (2000)Takemoto RM, Pavanelli GC. Aspects of the ecology of proteocephalid cestodes parasites of (Pimelodidae) of the upper Paraná river, Brazil. I. Structure and influence of host’s size and sex. Sorubim limaBraz J Biol 2000; 60(4): 577-584. http://dx.doi.org/10.1590/S0034-71082000000400006. PMid:11241955.
http://dx.doi.org/10.1590/S0034-71082000...
that the greater surface area and viability of space in large fish and the larger amount of food that they ingest can favor higher levels of parasitism.

Conclusions

Geophagus brasiliensis is a new host for the trematodes Lobatostoma sp., Homalometron pseudopallidum and Thometrema overstreeti, as well as for the ergasilids Ergasilus lizae and Gauchergasilus euripedesi and for the argulid Argulus spinolosus. Ergalisus lizae is reported for the first time in Rio Grande do Sul. The sex of the host does not represent a determining factor for parasitism. The trematodes Thometrema overstreeti and Posthodiplostomum sp. presented significantly higher prevalence in fish longer than 20 cm.

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Publication Dates

  • Publication in this collection
    04 Dec 2015
  • Date of issue
    Oct-Dec 2015

History

  • Received
    02 Sept 2015
  • Accepted
    09 Oct 2015
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