First report of Livoneca guianensis (Isopoda: Cymothoidae) in Leporinus fasciatus (Pisces: Anostomidae) in Brazil

Primeiro registro de Livoneca guianensis (Isopoda: Cymothoidae) em Leporinus fasciatus (Pisces: Anostomidae) no Brasil

Marcos Sidney Brito Oliveira Marcos Tavares-Dias About the authors

Abstract

This study aimed to report the first record of the occurrence of the parasite Livoneca guianensis in Leporinus fasciatus in Brazil. In September 2019, during surveys of the parasites in 12 specimens of L. fasciatus from the lower Jari River basin, in Amapá State, Brazil, one specimen of L. guianensis was found in the tongue of one host. The prevalence of L. guianensis was 8.3%, and it was observed that this parasite has a geographic distribution restricted to South America, parasitizing fish species from Guyana and Brazil. This study contributed to the first report on the occurrence of L. guianensis for L. fasciatus in Brazil. In addition, increased the knowledge on the geographic distribution of this parasite with morphometric data, which are scarce for this Cymothoidae.

Keywords:
Isopoda; ectoparasite; gill; freshwater fish; Jari River

Resumo

Este estudo objetivou registrar a primeira ocorrência de Livoneca guianensis em Leporinus fasciatus no Brasil. Em setembro de 2019, durante uma pesquisa sobre parasitos em 12 espécimes de L. fasciatus do baixo Rio Jari, Estado do Amapá, norte do Brasil, um espécime de L. guianensis foi encontrado na língua de um hospedeiro. A prevalência de L. guianensis foi de 8,3% e foi observado que esse parasito tem distribuição geográfica restrita à América do Sul, parasitando espécies de peixes da Guiana e do Brasil. Este estudo contribuiu com o primeiro relato da ocorrência de L. guianensis para L. fasciatus no Brasil. Além disso, aumentou o conhecimento sobre a distribuição geográfica desse parasito, contribuindo com dados morfométricos que são escassos para esse Cymothoidae.

Palavras-chave:
Isopoda; ectoparasitos; brânquia; peixe de água doce; Rio Jari

Isopoda of the family Cymothoidae Leach, 1818 are obligatory ectoparasites with direct life cycle and they parasitize both marine and freshwater fish (Smit et al., 2014Smit NJ, Bruce NL, Hadfield KA. Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Int J Parasitol Parasites Wildl 2014; 3(2): 188-197. http://dx.doi.org/10.1016/j.ijppaw.2014.03.004. PMid:25180163.
http://dx.doi.org/10.1016/j.ijppaw.2014....
; Tavares-Dias et al., 2015Tavares-Dias M, Dias-Júnior MBF, Florentino AC, Silva ALM, Cunha AC. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev Bras Parasitol Vet 2015; 24(2): 136-147. http://dx.doi.org/10.1590/S1984-29612015036. PMid:26154954.
http://dx.doi.org/10.1590/S1984-29612015...
; Oliveira et al., 2017Oliveira MSB, Corrêa LL, Ferreira DO, Neves LR, Tavares-Dias M. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Parasit Dis 2017; 41(2): 565-570. http://dx.doi.org/10.1007/s12639-016-0852-8. PMid:28615880.
http://dx.doi.org/10.1007/s12639-016-085...
). The genus Livoneca Leach, 1818 is consisted of 18 species of ectoparasites: Livoneca bowmani Brusca, 1981; Livoneca ovalis Say, 1818; Livoneca redmanii Leach, 1818; Livoneca desterroensis Thatcher, Souza-Conceição & Jost de 2003; Livoneca enigmatica Fryer, 1968; Livoneca galinae Kononenko, 1989; Livoneca guianensis Van Name, 1925; Livoneca intermedia Nierstrasz, 1931; Livoneca lazzari Pearse, 1921; Livoneca orinoco Bowman & Diaz-Ungria, 1957; Livoneca papernea Trilles, Colorni & Golani, 1999; Livoneca parasilura Shen, 1933; Livoneca pomatoi Gaillat Airoldi, 1940; Livoneca reniformis Menzies & Frankenberg, 1966; Livoneca ricinoides Risso, 1816; Livoneca soudanensis Richardson, 1911; Livoneca tenuistylis Richardson, 1912 and Livoneca texana Pearse, 1952 (Boyko et al., 2008Boyko CB, Bruce NL, Hadfield KA, Merrin KL, Ota Y, Poore GCB, et al. Cymothoidae Leach, 1818 [online]. World Register of Marine Species; 2008 [cited 2020 Jul 3]. Available from: http://marinespecies.org/aphia.php?p=taxdetails&id=118274
http://marinespecies.org/aphia.php?p=tax...
). Livoneca guianensis was described only from the oral cavity of the fish Leporinus fasciatus Bloch, 1794 (Anostomidae) and Pimelodus clarias (Pimelodidae) from Guyana (Van Name, 1925Van Name BWG. The isopods of Kartabo, Bartica district, British Guiana. Zoologica 1925; 6(5): 461-503.). Thus, the present study contributes with the first report of L. guianensis for L. fasciatus in Brazil, in addition to providing morphometric data for this parasite, which are scarce.

In September 2019, 12 specimens of L. fasciatus were collected in the lower Jari River system [1°9'6.23”S 51°59'25.94”W], near the Jarilândia District, municipality of Vitória do Jari, Amapá State, Northern Brazil (Figure 1). Fish were collected using gillnets (15 m long, 1.5 deep, 20, 25 and 30 mm between knots) and were measured for total length (cm) and weight (g). All fish were examined for crustacean ectoparasites, which were maintained in ethanol solution (70%) for 24 h, and then preserved in alcohol (70%) with glycerin (10%) for further morphological analyses. Measurements recorded for the L. guianensis were the length and width of the body; length of the pereons, dactyls and pleonites; as well as length and width of the telson. The host and parasite were identified at the higher taxonomic level according to specialized literature (Van Name, 1925Van Name BWG. The isopods of Kartabo, Bartica district, British Guiana. Zoologica 1925; 6(5): 461-503.; Queiroz et al., 2013Queiroz LJ, Torrente-Vilara G, Ohara WM, Pires THS, Zuano J, Doria CR. Peixes do Rio Madeira. 1. ed. São Paulo: Dialeto Latin American Documentary; 2013. (vol. 1).).

Figure 1
Collection site of Leporinus fasciatus in the Jari River basin, in eastern Amazon (Brazil).

Specimens of L. fasciatus (Figure 2A, B) showed an average media length of 18.1 (10.8-26.2) cm and average weight of 83.6 (11.8-183.8) g. Only one specimen (8.3%) of L. fasciatus measuring 22.2 cm in length and weighing 111.2 g was parasitized by L. guianensis ♀ (Figure 2CF) that was found in the tongue of this host (Figure 2B). Small lesions were observed on the host tongue due to the fixation of the parasite claws. The measurements of L. guianensis are shown in Table 1.

Figure 2
Female of Livoneca guianensis fixed on the tongue of Leporinus fasciatus from the Jari River basin, in eastern Amazon, Brazil (A, B). Views of the Livoneca guianensis dorsal (C) ventral (D), frontal (E) and back (F).
Table 1
Measurement of Livoneca guianensis female collected in Leporinus fasciatus gills from the Jari River, in eastern Amazon (Brazil).

In general, parasitic cymothoids occur with little infestation in gills of host fish because these ectoparasites may cause considerable damage to fish when feeding from mucous and epithelial cells, perforating the fish skin (Tavares-Dias et al., 2014Tavares-Dias M, Araújo CS, Barros MS, Viana GM. New hosts and distribution records of Braga patagonica, a parasite Cymothoidae of fishes from the Amazon. Braz J Aquat Sci Tech 2014; 18(1): 91-97. http://dx.doi.org/10.14210/bjast.v18n1.p91-97.
http://dx.doi.org/10.14210/bjast.v18n1.p...
, 2015Tavares-Dias M, Dias-Júnior MBF, Florentino AC, Silva ALM, Cunha AC. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev Bras Parasitol Vet 2015; 24(2): 136-147. http://dx.doi.org/10.1590/S1984-29612015036. PMid:26154954.
http://dx.doi.org/10.1590/S1984-29612015...
). This is related to competition for resource, because possibly the size of the infestation site (i. e. tongue) is a limiting factor for cohabiting two or more specimens of L. guianensis or other isopod species of large size. The registration of L. guianensis in larger L. fasciatus corroborates the hypothesis that larger fish with a larger available area are more prone to infestation by this isopod species (Arneberg et al., 1998Arneberg P, Skorping A, Read AF. Parasite abundance, body size, life histories, and the energetic equivalence rule. Am Nat 1998; 151(6): 497-513. http://dx.doi.org/10.1086/286136. PMid:18811372.
http://dx.doi.org/10.1086/286136...
; Poulin, 1999Poulin R. Body size vs abundance among parasite species: positive relationships? Ecography 1999; 22(3): 246-250. http://dx.doi.org/10.1111/j.1600-0587.1999.tb00499.x.
http://dx.doi.org/10.1111/j.1600-0587.19...
). The low prevalence of this cymothoids may be due to its low fertility rate, infestation, survival, environmental conditions, predation or even host behavior. These parasites infest the ventral part of the opercular cavity or the mouth of their hosts (Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Moscow: Pensoft Publishers Sofia; 2006. (vol. 1).; Tavares-Dias et al., 2014Tavares-Dias M, Araújo CS, Barros MS, Viana GM. New hosts and distribution records of Braga patagonica, a parasite Cymothoidae of fishes from the Amazon. Braz J Aquat Sci Tech 2014; 18(1): 91-97. http://dx.doi.org/10.14210/bjast.v18n1.p91-97.
http://dx.doi.org/10.14210/bjast.v18n1.p...
; Oliveira et al., 2017Oliveira MSB, Corrêa LL, Ferreira DO, Neves LR, Tavares-Dias M. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Parasit Dis 2017; 41(2): 565-570. http://dx.doi.org/10.1007/s12639-016-0852-8. PMid:28615880.
http://dx.doi.org/10.1007/s12639-016-085...
). In general, the cymothoid species are protandrous hermaphrodites, and mainly females are found parasitizing fish, however, males are occasionally found together with females. The presence of L. guianensis female without a male partner is a strong indication that the males may have been swept from the oral cavity or swallowed by the host fish (Bakenhaster et al., 2006Bakenhaster MD, McBride RS, Price WW. Life history of Glossobius hemiramphi (Isopoda: Cymothoidae): development, reproduction, and symbiosis with its host Hemiramphus brasiliensis (Pisces: Hemiramphidae). J Crustac Biol 2006; 26(3): 283-294. http://dx.doi.org/10.1651/C-2573.1.
http://dx.doi.org/10.1651/C-2573.1...
), but is also possible that the male spontaneously leaves the host, either due to biological necessity or perception of fish stress at the time of host collection. In the present study, L. guianensis was found in the tongue of L. fasciatus, in which small lesions caused by the attachment of the parasite claws were observed. Similar lesions were also attributed to the isopod Braga patagonica Schioedte & Meinert, 1884 in Colossoma macropomum Cuvier, 1816 tegument (Tavares-Dias et al., 2014Tavares-Dias M, Araújo CS, Barros MS, Viana GM. New hosts and distribution records of Braga patagonica, a parasite Cymothoidae of fishes from the Amazon. Braz J Aquat Sci Tech 2014; 18(1): 91-97. http://dx.doi.org/10.14210/bjast.v18n1.p91-97.
http://dx.doi.org/10.14210/bjast.v18n1.p...
).

Species of the genus Livoneca have a wide geographical distribution, with records in Asia, Africa, North America, Central America, South America, and Europe (Bruce, 1990Bruce N. The genera Catoessa, Elthusa, Enispa, Ichthyoxenus, Idusa, Livoneca and Norileca n. gen. (Isopoda, Cymothoidae), crustacean parasites of marine fishes, with descriptions of Eastern Australian species. Rec Aust Mus 1990; 42(3): 247-300. http://dx.doi.org/10.3853/j.0067-1975.42.1990.118.
http://dx.doi.org/10.3853/j.0067-1975.42...
). However, the taxonomic status of most Livoneca species, including L. guianensis, is considered uncertain (Bruce, 1990Bruce N. The genera Catoessa, Elthusa, Enispa, Ichthyoxenus, Idusa, Livoneca and Norileca n. gen. (Isopoda, Cymothoidae), crustacean parasites of marine fishes, with descriptions of Eastern Australian species. Rec Aust Mus 1990; 42(3): 247-300. http://dx.doi.org/10.3853/j.0067-1975.42.1990.118.
http://dx.doi.org/10.3853/j.0067-1975.42...
). Therefore, new taxonomic revisions of these species are necessary, of which can change the biogeographical status currently established for these isopods. After description of L. guianensis collected in L. fasciatus and P. clarias in Guyana (Van Name, 1925Van Name BWG. The isopods of Kartabo, Bartica district, British Guiana. Zoologica 1925; 6(5): 461-503.), this parasite was found in Brazil in the oral cavity of Leporinus friderici Bloch, 1794 in the Jari River, a tributary of the Amazon River basin in Northern Brazil (Oliveira et al., 2017Oliveira MSB, Corrêa LL, Ferreira DO, Neves LR, Tavares-Dias M. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Parasit Dis 2017; 41(2): 565-570. http://dx.doi.org/10.1007/s12639-016-0852-8. PMid:28615880.
http://dx.doi.org/10.1007/s12639-016-085...
). Therefore, L. guianensis has a distribution exclusive to South America and may be widely distributed in this Neotropical region. In conclusion, this study contributed the first report of the occurrence of L. guianensis in L. fasciatus in Brazil, thus increasing our knowledge about the geographic distribution of this parasite. Furthermore, the present study contributed morphometric data, which are scarce for this cymothoid.

Acknowledgements

We would like to thank Mr. João Pena de Oliveira for his assistance in collecting fish, to the National Council for Scientific and Technological Development/CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the research grant provided to Tavares-Dias, M (Grant 303013/2015-0), to the Post-graduate Program of studies in Tropical Biodiversity (PPGBio - Programa de Pós-graduação em Biodiversidade Tropical) and Coordination for the Improvement of Higher Education Personnel (CAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for granting a doctoral fellowship to Oliveira, MSB.

  • How to cite: Oliveira MSB, Tavares-Dias M. First report of Livoneca guianensis (Isopoda: Cymothoidae) in Leporinus fasciatus (Pisces: Anostomidae) in Brazil. Braz J Vet Parasitol 2020; 29(4): e020420. https://doi.org/10.1590/S1984-29612020106

References

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    » http://dx.doi.org/10.1086/286136
  • Bakenhaster MD, McBride RS, Price WW. Life history of Glossobius hemiramphi (Isopoda: Cymothoidae): development, reproduction, and symbiosis with its host Hemiramphus brasiliensis (Pisces: Hemiramphidae). J Crustac Biol 2006; 26(3): 283-294. http://dx.doi.org/10.1651/C-2573.1
    » http://dx.doi.org/10.1651/C-2573.1
  • Boyko CB, Bruce NL, Hadfield KA, Merrin KL, Ota Y, Poore GCB, et al. Cymothoidae Leach, 1818 [online]. World Register of Marine Species; 2008 [cited 2020 Jul 3]. Available from: http://marinespecies.org/aphia.php?p=taxdetails&id=118274
    » http://marinespecies.org/aphia.php?p=taxdetails&id=118274
  • Bruce N. The genera Catoessa, Elthusa, Enispa, Ichthyoxenus, Idusa, Livoneca and Norileca n. gen. (Isopoda, Cymothoidae), crustacean parasites of marine fishes, with descriptions of Eastern Australian species. Rec Aust Mus 1990; 42(3): 247-300. http://dx.doi.org/10.3853/j.0067-1975.42.1990.118
    » http://dx.doi.org/10.3853/j.0067-1975.42.1990.118
  • Oliveira MSB, Corrêa LL, Ferreira DO, Neves LR, Tavares-Dias M. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Parasit Dis 2017; 41(2): 565-570. http://dx.doi.org/10.1007/s12639-016-0852-8 PMid:28615880.
    » http://dx.doi.org/10.1007/s12639-016-0852-8
  • Poulin R. Body size vs abundance among parasite species: positive relationships? Ecography 1999; 22(3): 246-250. http://dx.doi.org/10.1111/j.1600-0587.1999.tb00499.x
    » http://dx.doi.org/10.1111/j.1600-0587.1999.tb00499.x
  • Queiroz LJ, Torrente-Vilara G, Ohara WM, Pires THS, Zuano J, Doria CR. Peixes do Rio Madeira 1. ed. São Paulo: Dialeto Latin American Documentary; 2013. (vol. 1).
  • Smit NJ, Bruce NL, Hadfield KA. Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Int J Parasitol Parasites Wildl 2014; 3(2): 188-197. http://dx.doi.org/10.1016/j.ijppaw.2014.03.004 PMid:25180163.
    » http://dx.doi.org/10.1016/j.ijppaw.2014.03.004
  • Tavares-Dias M, Araújo CS, Barros MS, Viana GM. New hosts and distribution records of Braga patagonica, a parasite Cymothoidae of fishes from the Amazon. Braz J Aquat Sci Tech 2014; 18(1): 91-97. http://dx.doi.org/10.14210/bjast.v18n1.p91-97
    » http://dx.doi.org/10.14210/bjast.v18n1.p91-97
  • Tavares-Dias M, Dias-Júnior MBF, Florentino AC, Silva ALM, Cunha AC. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev Bras Parasitol Vet 2015; 24(2): 136-147. http://dx.doi.org/10.1590/S1984-29612015036 PMid:26154954.
    » http://dx.doi.org/10.1590/S1984-29612015036
  • Thatcher VE. Amazon fish parasites 2nd ed. Moscow: Pensoft Publishers Sofia; 2006. (vol. 1).
  • Van Name BWG. The isopods of Kartabo, Bartica district, British Guiana. Zoologica 1925; 6(5): 461-503.

Publication Dates

  • Publication in this collection
    04 Dec 2020
  • Date of issue
    2020

History

  • Received
    27 Aug 2020
  • Accepted
    08 Oct 2020
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