First record of two Copepoda species parasitizing Colomesus tocantinensis (Tetraodontiformes: Tetraodontidae) in the Tocantins-Araguaia basin, Brazil

Primeiro registro de duas espécies de Copepoda parasitando Colomesus tocantinensis (Tetraodontiformes: Tetraodontidae) na bacia do Tocantins-Araguaia, Brasil

Abstract

Considering the lack of studies on freshwater fishes of the genus Colomesus, we conducted a survey the parasite fauna of Colomesus tocantinensis collected from the Tocantins River, Brazil. We first recorded the presence of the ectoparasites Ergasilus colomesus and Lernaea sp. where 96.77% of the fish were parasitized.

Keywords:
Pufferfish; Lernaeidae; Ergasilidae; Legal Amazon; fish parasites

Resumo

Considerando a ausência de estudos com os peixes de água doce do gênero Colomesus, foi realizado um levantamento da parasitofauna de Colomesus tocantinensis coletados no rio Tocantins. Foi registrada pela primeira vez a presença dos ectoparasitas Ergasilus colomesus e Lernaea sp. onde 96,77% dos peixes estavam parasitados.

Palavras-chave:
Baiacu; Lernaeidae; Ergasilidae; Amazônia Legal; parasitas de peixe

The Tocantins River is composed of the Tocantins-Araguaia basin and is located in the Legal Amazon. It originates in the state of Goiás and runs northward for 2500 km, passing through the states of Tocantins, Maranhão, and Pará (Santos et al., 2004). The Tocantins-Araguaia basin is known to drain part of the extreme south of the Brazilian Shield to the extreme north of the Amazon basin, making the ichthyofauna of both basins closely related and presenting a high degree of endemism and diversity (Goulding et al., 2003; Lucinda et al., 2007; Bertaco & Carvalho, 2010; Amaral et al., 2013).

The family Tetraodontidae is composed of 192 fish species, distributed in 28 genus that occur in the seas, estuaries, and rivers of tropical and temperate regions (Fricke et al., 2023). The genus Colomesus comprises only three fish species, two of which are freshwater: Colomesus asellus (Müller & Troschel, 1849) and C. tocantinensis Amaral et al., 2013, both endemic to South America and distributed throughout the Amazon and Tocantins-Araguaia basins, respectively (Amaral et al., 2013).

These animals, known as “pufferfish,” can inflate their bodies in stressful situations and are coveted by the ornamental fish industry. The two species have similar morphological characteristics; however, their feeding habits have only been recorded in studies conducted with C. asellus (Bartolette et al., 2018). The same is observed for the parasitic fauna of these hosts; thus far, only the ectoparasite E. colomesus Thatcher and Boeger, 1983 has been found in the gills of C. asellus (Thatcher & Boeger, 1983; Virgilio et al., 2021), whereas for C. tocantinensis there are no parasitological records. Considering the absence of biological and ecological studies of C. tocantinensis, we present the first parasitological survey of this species.

Thirty-one individuals of C. tocantinensis were collected with nets of different mesh sizes from the Tocantins River, city of Porto Nacional (10°42'25.9 “S, 48°25'14.0 “W) in 2018. The procedures for necropsy of the hosts and collection, preservation, and preparation of parasites were performed according to the methods reported by Eiras et al. (2006). Parasitological indices were calculated according to Bush et al. (1997). Representative host specimens were deposited in the Ichthyological Collection of Universidade Federal de Tocantins (UNT 20349).

Thirty of the analyzed hosts were parasitized by at least one parasite. We recorded, for the first time, the interaction of Lernaea sp. (Figure 1) and E. colomesus (Figure 2) with C. tocantinensis. One Lernaea sp. specimen was found in only one individual, and the parasite with the highest frequency of occurrence, abundance, and mean intensity was E. colomesus, which was the central parasite for the host and had a high prevalence (Table 1). In a study describing the interaction of this parasite with C. asellus, prevalence was also high as the parasite was present in 76% of the hosts collected (Thatcher & Boeger, 1983). However, in a study conducted by Virgilio et al. (2021), the prevalence of E. colomesus in individuals of C. asellus was low and varied between the dry and flood periods, with values of 37.5% and 23.8%, respectively.

Figure 1
(A) Lernaea sp. parasite of Colomesus tocantinensis; (B) Anchor (arrows I, II, III and IV: holdfast); (C) Apical view of anchor attachment.

Figure 2
(A) Ergasilus colomesus parasite of Colomesus tocantinenses (dorsal view); (B) First antenna; (C) Modified second antenna (Arrow I: Spine; Arrow II: Laterally inflated anther basal segment; (D) Legs; (E) Uropod (Arrow I: Long, sparsely hairy bristle).

Table 1
Prevalence (%), Mean Intensity and Mean Abundance of ectoparasites of Colomesus tocantinensis from the Tocantins-Araguaia basin collected in the Tocantins River.

Parasites	Prevalence (%)	Mean Intensity (±SE)	Mean Abundance (±SE)
Copepoda
Ergasilus colomesus	96.77	8.56±1.90	8.29±1.86
Lernaea sp.	3.22	1±1	0.03±1

• SE: Standard error.

The family Ergasilidae, in general, does not exhibit high specificity; however, through evaluation of the species of the genus Ergasilus in isolation, several records of parasites restricted to a single host can be varified (Luque et al., 2013). We found that although the two Colomesus species inhabit different basins, the E. colomesus parasite maintained specificity at the host genus level. In general, ectoparasites do not require intermediate hosts to complete their life cycle. In the case of copepods, the initial stages (nauplii and copepodites) are freeborn, and after actively infecting the host, they undergo metamorphosis until they reach the adult stage and reproduce (Ohtsuka et al., 2018). These characteristics (specificity and reproduction) may explain the presence of copepods in C. tocantinensis.

The absence of endoparasites recorded in this study can be explained by the biology of the “pufferfish,” as these fish have three defense mechanisms: being venomous, inflation (with water or air), and aposematism (dorsal transverse black bars as warning coloration) (Krebs & Davis, 1993), which can prevent predation. Thus, from an endoparasitic perspective, non-host species that consume infected intermediate hosts are a ‘dead end’ and cannot act as competent final hosts to complete their life cycle (Mouritsen & Poulin, 2003; Song & Proctor, 2020). Considering that endoparasites primarily use the trophic pathway to access their hosts (Lafferty et al., 2008), and that there is no influence of ontogeny or hydrometric period on the feeding of C. tocantinensis individuals (Bartolette et al., 2018), it is unlikely that the absence of endoparasites is due to collection bias or sampling number, as these variables would not inhibit infection.

Our study provides new insights on the parasitic fauna of C. tocantinensis, analyzing for the first time the record of two species of ectoparasites (Lernaea sp. and E. colomesus) for this host. We emphasize the need for further study, as existing studies on the biology and ecology of this species are limited.

Acknowledgements

We are grateful to all who assisted us in the field and laboratory during the collection of the fish, especially Dra. Eliane da Silva Fernandes and the team at the Federal University of Tocantins: Dra. Elineide Eugênio Marques, Dr. Thiago Nilton Alves Pereira, and MsC. Alice Ferreira Araujo. Funding This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq with two scholarships for a doctorate (processes authors ALL and WTH: 88882.344478/2019-01 and 140855/2021-1, respectively) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES with three scholarships for a doctorate (processes authors GM, LDC and JOSS: 88887.713849/2022-00, 88887.495295/2020-00 and 88882.344446/2011-01, respectively).

• How to cite: Michelan G, Hasuike WT, Cavalcanti LD, Lehun AL, Silva JOS, Takemoto RM. First record of two Copepoda species parasitizing Colomesus tocantinensis (Tetraodontiformes: Tetraodontidae) in the Tocantins-Araguaia basin, Brazil. Braz J Vet Parasitol 2023; 32(3): e006523. https://doi.org/10.1590/S1984-29612023030

References

• Amaral CRL, Brito PM, Silva DA, Carvalho EF. A new cryptic species of South American freshwater pufferfish of the genus Colomesus (Tetraodontidae), based on both morphology and DNA data. PLoS One 2013; 8(9): e74397. http://dx.doi.org/10.1371/journal.pone.0074397 PMid:24040239.
  » http://dx.doi.org/10.1371/journal.pone.0074397
• Bartolette R, Rosa DCO, Soares BE, Beserra DA, Albrecht MP, Brito MFG. Seasonal and ontogenetic diet patterns of the freshwater pufferfish Colomesus asellus (Müller & Troschel, 1849) in the upper-middle Tocantins River. Acta Sci Biol Sci 2018; 40(1): e35282. http://dx.doi.org/10.4025/actascibiolsci.v40i1.35282
  » http://dx.doi.org/10.4025/actascibiolsci.v40i1.35282
• Bertaco VA, Carvalho FR. New species of Hasemania (Characiformes: Characidae) from Central Brazil, with comments on the endemism of upper rio Tocantins basin, Goiás State. Neotrop Ichthyol 2010; 8(1): 27-32. http://dx.doi.org/10.1590/S1679-62252010000100004
  » http://dx.doi.org/10.1590/S1679-62252010000100004
• 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
• Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes 2. ed. Maringá: Eduem; 2006.
• Fricke R, Eschmeyer WN, Van der Laan R. Eschmeyer’s catalog of fishes: genera, species, references [online]. 2023 [cited 2023 Jan 23]. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
  » http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
• Goulding M, Barthem R, Ferreira EJG, Duenas R. The Smithsonian atlas of the Amazon Washington: Smithsonian Books; 2003.
• Krebs JR, Davis NB. An introduction to behavioural ecology 3nd ed. Oxford: Blackwell Scientific Publications; 1993.
• Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, et al. Parasites in food webs: the ultimate missing links. Ecol Lett 2008; 11(6): 533-546. http://dx.doi.org/10.1111/j.1461-0248.2008.01174.x PMid:18462196.
  » http://dx.doi.org/10.1111/j.1461-0248.2008.01174.x
• Lucinda PHF, Freitas IS, Soares AB, Marques EE, Agostinho CS, Oliveira RJ. Fish, Lajeado reservoir, rio Tocantins drainage, state of Tocantins, Brazil. Check List 2007; 3(2): 70-83. http://dx.doi.org/10.15560/3.2.70
  » http://dx.doi.org/10.15560/3.2.70
• Luque JL, Vieira FM, Takemoto RM, Pavanelli GC, Eiras JC. Checklist of Crustacea parasitizing fishes from Brazil. Check List 2013; 9(6): 1449-1470. http://dx.doi.org/10.15560/9.6.1449
  » http://dx.doi.org/10.15560/9.6.1449
• Mouritsen KN, Poulin R. Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator’s nightmare. Int J Parasitol 2003; 33(10): 1043-1050. http://dx.doi.org/10.1016/S0020-7519(03)00178-4 PMid:13129526.
  » http://dx.doi.org/10.1016/S0020-7519(03)00178-4
• Ohtsuka S, Madinabeitia I, Yamashita H, Maran BAV, Suárez-Morales E, Ho JS. Planktonic phases in symbiotic copepods: a review. Bull South Calif Acad Sci 2018; 117(2): 104-119. http://dx.doi.org/10.3160/3616.1
  » http://dx.doi.org/10.3160/3616.1
• Santos GM, Juras AA, Mérona BD, Jégue M. Peixes do baixo rio Tocantins: 20 anos depois da Usina Hidrelétrica Tucuruí Brasília: Eletronorte; 2004.
• Song Z, Proctor H. Parasite prevalence in intermediate hosts increases with waterbody age and abundance of final hosts. Oecologia 2020; 192(2): 311-321. http://dx.doi.org/10.1007/s00442-020-04600-4 PMid:32006182.
  » http://dx.doi.org/10.1007/s00442-020-04600-4
• Thatcher VE, Boeger WA. The parasitic crustaceans of fishes from the Brazilian Amazon. 4. Ergasilus colomesus n. sp. (Copepoda: Cyclopoida) from an ornamental fish, Colomesus asellus (Tetraodontidae) and aspects of Its pathogenicity. Trans Am Microsc Soc 1983; 102(4): 371-379. http://dx.doi.org/10.2307/3225850
  » http://dx.doi.org/10.2307/3225850
• Virgilio LR, Machado EO, Freire NA, Takemoto RM, Camargo LMA, Meneguetti DUO. Ergasilus colomesus (Copepoda: Ergasilidae) parasitizing gills of Colomesus asellus (Tetraodontiformes: Tetraodontidae) in the western Brazilian Amazon. Ann Parasitol 2021; 67(1): 123-127. PMid:34022783.

Publication Dates

• Publication in this collection
  29 May 2023
• Date of issue
  2023

History

• Received
  05 Apr 2023
• Accepted
  03 May 2023