Abstract:
Leucism is an anomaly recorded in fish species as well as in many other groups of animals in natural environments. An individual with leucism is characterized by the loss of brown or black pigmentation over most of the body. Here, we recorded this condition for an individual of marbled swamp eel Synbranchus marmoratus (Synbranchiformes: Synbranchidae) captured in the Furnas megareservoir, Grande River basin, in Minas Gerais state, southeastern Brazil. The individual had a general color of the body with shades ranging from pale to intense yellowish, but the eyes were black. We also present a discussion on the influence of leucism on the survival of the individual in this study.
Keywords:
Color anomaly; fish; Furnas megareservoir; Grande River basin; pigmentation
Resumo:
Leucismo é uma anomalia registrada em espécies de peixes assim como em muitos outros grupos de animais em ambientes naturais. Um indivíduo com leucismo é caracterizado pela perda de pigmentação marrom ou preta na maior parte do corpo. Neste trabalho, nós registramos essa condição para um indivíduo de muçum Synbranchus marmoratus (Synbranchiformes: Synbranchidae) capturado no megareservatório de Furnas, bacia do Rio Grande, no estado de Minas Gerais, sudeste brasileiro. O indivíduo apresentava coloração geral do corpo com tonalidades que variavam do amarelado pálido ao intenso, mas os olhos eram pretos. Nós também apresentamos uma discussão sobre a influência do leucismo na sobrevivência do indivíduo deste estudo.
Palavras-chave:
Anomalia na coloração; bacia do Rio Grande; megareservatório de Furnas; peixe; pigmentação
Introduction
Neotropical freshwater fishes have been increasingly studied for anomalies. Most existing studies focus on the abnormal color pattern (e.g., Nobile et al. 2016NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534.; Azevedo-Santos et al. 2020aAZEVEDO-SANTOS, V.M., PELICICE, F.M., SAZIMA, I. & HENRY, R. 2020a. A case of complete albinism in the catfish Cambeva guareiensis (Siluriformes: Trichomycteridae). Biota Neotrop. 20(4): e20201066.; Romano & Pedrosa 2020ROMANO, L.A. & PEDROSA, V.F. 2020. Leucism in South American Lungfishes Lepidosiren paradoxa Fitzinger, 1837 (Osteichthyes, Dipnoi, Lepidosirenidae) from Argentina. Braz. J. Vet. Pathol. 13(1): 51–52.; Ferraz et al. 2023FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189.), but other conditions (e.g., tumors and pughead) have also been documented (e.g., Catelani et al. 2017CATELANI, P.A., BAUER, A.B., DI DARIO, F., PELICICE, F.M. & PETRY, A.C. 2017. First record of pughead deformity in Cichla kelberi (Teleostei: Cichlidae), an invasive species in an estuarine system in south-eastern Brazil. J. Fish Biol. 90(6): 2496–2503.; Correia-Silva et al. 2024CORREIA-SILVA, G., CORAZZA, L.Q., OTTONI, F.P., SILVA, C.V., NUNES, A.V.P., KATZ, A.M. & AZEVEDO-SANTOS, V.M. 2024. Anomalous specimens of Rhamdia quelen (Siluriformes: Heptapteridae) and Gymnotus cf. sylvius (Gymnotiformes: Gymnotidae). Cybium 48:177–180.).
There are different color-related anomalies in freshwater fishes. Generally, these conditions attract the attention of the scientific community (e.g., Nobile et al. 2016NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534.; Ferraz et al. 2023FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189.) and fishermen (e.g., Table S1). Leucism is an anomaly in which there is a total or partial loss of color (hence the chromatophores) on the body of a fish or other animal (McCardle 2013MCCARDLE, H. 2013. Albinism in Wild Vertebrates. London: LAMBERT Academic Publishing, 88 pp.; Henle et al. 2017HENLE, K., DUBOIS, A. & VERSHININ, V. 2017. Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Mertensiella 25: 9–48.). However, in leucism, unlike complete albinism (cf. Carvalho & de Pinna 1986CARVALHO, A.M. & DE PINNA, M.C.C. 1986. Estudo de uma população hipógea de Trichomycterus (Ostariophysi, Siluroidei, Trichomycteridae) da gruta Olhos d’Água, MG. Espeleo-Tema 15: 53–64.; Sazima & Pombal-Jr. 1986SAZIMA, I. & POMBAL-JR, J.P. 1986. Um albino de Rhamdella minuta, com notas sobre comportamento (Osteichthyes, Pimelodidae). Rev. Bras. Biol. 46(2): 377–381.; Azevedo-Santos et al. 2020aAZEVEDO-SANTOS, V.M., PELICICE, F.M., SAZIMA, I. & HENRY, R. 2020a. A case of complete albinism in the catfish Cambeva guareiensis (Siluriformes: Trichomycteridae). Biota Neotrop. 20(4): e20201066.), the eyes still have pigmentation; and can often be of the same tone as that of non-anomalous animals of the same species (e.g., Nobile et al. 2016NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534.; Ferraz et al. 2023FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189.). Cases of leucism are documented sparsely in Neotropical freshwater fishes (e.g., Nobile et al. 2016NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534.; Anaguano-Yancha 2018; Romano & Pedrosa 2020ROMANO, L.A. & PEDROSA, V.F. 2020. Leucism in South American Lungfishes Lepidosiren paradoxa Fitzinger, 1837 (Osteichthyes, Dipnoi, Lepidosirenidae) from Argentina. Braz. J. Vet. Pathol. 13(1): 51–52.; Ferraz et al. 2023FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189.).
Synbranchus marmoratus Bloch, 1795, a species popularly known as “muçum” in Brazil, or marbled swamp eel, is one of the thousands of Neotropical freshwater fishes (~6,200 species sensuAlbert et al. 2020ALBERT, J.S., TAGLIACOLLO, V.A. & DAGOSTA, F. 2020. Diversification of Neotropical freshwater fishes. Annu. Rev. Ecol. Evol. Syst. 51: 27–53.). Among the synbranchids, it is the species possessing the widest geographic distribution, occurring from Mexico to the northern Argentina, in numerous types of environments, from streams (including headwaters) to artificial lakes (Kullander 2003KULLANDER, S.O. 2003. Family Synbranchidae (Swamp-eels). In R.E. Reis, S.O. Kullander & C.J. Ferraris (Eds.), Check list of the freshwater fishes of South America (pp. 594–595). Edipucrs.). In general, the color of the species varies from brown to dark gray, with spots (generally small) distributed throughout its body (Torres et al. 2005TORRES, R.A., ROPER, J.J., FORESTI, F. & OLIVEIRA, C. 2005. Surprising genomic diversity in the Neotropical fish Synbranchus marmoratus (Teleostei: Synbranchidae): how many species? Neotrop. Ichthyol. 3(2): 277–284.; Ota et al. 2018OTA, R.R., DEPRÁ, G.D.C., GRAÇA, W.J.D. & PAVANELLI, C.S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop. Ichthyol. 16: e170094.). Recently, we obtained a specimen of S. marmoratus with the absence of dark coloration along the body, but with pigmented eyes. So, here, we record and illustrate this case of leucism.
Material and Methods
1.Study area
The Furnas megareservoir, located in Minas Gerais state, southeastern Brazil, was built to generate and supply electrical energy. However, the aquatic environments of the megareservoir are widely used for several activities such as tourism, aquaculture (e.g., tilapia farming), leisure, and fishing (Azevedo-Santos et al. 2011AZEVEDO-SANTOS, V.M., RIGOLIN-SÁ, O., PELICICE, F.M. 2011. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of non-native fish in Furnas Reservoir, Minas Gerais, Brazil. Neotrop. Ichthyol. 9: 915–919.; Chaves et al. 2023CHAVES, A.J.P., ZARA, F.J. & PASCHOAL, L.R.P. 2023. Long-term monitoring of the nonnative giant river prawn Macrobrachium rosenbergii (De Man, 1879) in the Furnas mega reservoir (southeastern Brazil). Nauplius 31: e2023025.).
The specimen was captured in a small channel connected to the initial portion of the impoundment of the left arm of the Sapucaí River in the Furnas megareservoir (coordinates 21°30’27.7”S, 46°00’09.4”W), Grande River basin, in the municipality of Alfenas (Figure 1). This area shows signs of anthropogenic activities since the region close to the channel is used for tilapia farming. The sediment in the aquatic environment has a clayey-silty nature, and the maximum depth of the channel can reach 10 meters in certain months of the year.
Station of the capture of the leucistic Synbranchus marmoratus Bloch, 1795, Alfenas, Minas Gerais state, southeastern Brazil.
Sampling and specimen analysis
The specimen was captured on 16 October 2023, using a gill net (40 mm mesh). We measured the total length (TL in cm) of the specimen with an ichthyometer with an accuracy of 1 millimeter. Subsequently, the animal was weighed on a digital scale (accuracy: 0.001 g) and euthanized, fixed, and preserved according to Azevedo-Santos et al. (2020b)AZEVEDO-SANTOS, V.M., PELICICE, F.M. & HENRY, R. 2020b. Knowing biodiversity: Fishes from the Guareí River basin, a tributary of the Jurumirim reservoir, Paranapanema River, Brazil. Biota Neotrop. 20(3): e20201031.. Identification of the individual was performed by analyzing external morphology, according to Ota et al. (2018)OTA, R.R., DEPRÁ, G.D.C., GRAÇA, W.J.D. & PAVANELLI, C.S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop. Ichthyol. 16: e170094..
The skin color tones of the captured specimen were analyzed and checked using the Pantone® color reference guide (Formula guide Solid Coated – GP1401). We adopted this methodology to standardize the descriptions of the animal’s color both in aquatic and external environments – since, in the latter, it was possible to observe a large release of mucus and, consequently, a change in the individual’s colorimetric pattern (LRP Paschoal, personal observation). Therefore, the interval between the codes for the lightest and darkest shades of the colors observed on the skin of the animal was used. After all analyses, the specimen was deposited in the scientific collection of the Department of Zoology and Botany of São Paulo State University in São José do Rio Preto (DZSJRP), São Paulo state, southeastern Brazil.
Results
The leucistic individual of Synbranchus marmoratus (DZSJRP 24795) has 105.34 cm of TL and weighs 2.360 kg. The specimen showed scars on its dorsal region due to entanglement in the gill net (Figures 2 A–B and 3A).
Coloration in life (within the water) of Synbranchus marmoratus Bloch, 1795 (DZSJRP 24795): (a) right side and (b) dorsal view. Note the scars in the medial region of the fish’s body.
Coloration in life (outside the water) of Synbranchus marmoratus Bloch, 1795 (DZSJRP 24795): (a) dorsal view and (b) cephalic view.
The color of the individual in the aquatic environment was pale yellow (134C, 7506C-7508C), both in lateral and dorsal views; without major changes in colorimetric variation along its length or in its ventral region (Figure 2). When removed from the aquatic environment, the animal showed an intense yellow color (1375C) in its lighter areas, mainly in the dorsal region (Figure 3A); while in darker areas, such as the gill chamber (Figure 3B), the tone was orange (7410C e 7576C). The eyes showed pigmentation in the iris in life (Figures 2 and 3) and after fixation (data not shown here).
Discussion
The individuals of Synbranchus marmoratus, including those that occur in the upper Paraná River basin, exhibit dark brown coloration with several light brown and black spots, a typical pattern for the species (e.g., Fig. 2B in Favorito et al. 2005FAVORITO, S.E., ZANATA, A.M., & ASSUMPÇÃO, M.I. 2005. A new Synbranchus (Teleostei: Synbranchiformes: Synbranchidae) from ilha de Marajó, Pará, Brazil, with notes on its reproductive biology and larval development. Neotrop. Ichthyol. 3: 319–328.; Fig. 3M in Lima et al. 2014LIMA, S.M.Q., DE PAIVA, R., RAMOS, T. & MENDES, L. 2014. Fish fauna of Pratagi River coastal microbasin, extreme north Atlantic Forest, Rio Grande do Norte state, northeastern Brazil. Check List 10(5), 968–975.; Fig. 32A in Ota et al. 2018OTA, R.R., DEPRÁ, G.D.C., GRAÇA, W.J.D. & PAVANELLI, C.S. 2018. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop. Ichthyol. 16: e170094.; Fig. 6E in Azevedo-Santos et al. 2020bAZEVEDO-SANTOS, V.M., PELICICE, F.M. & HENRY, R. 2020b. Knowing biodiversity: Fishes from the Guareí River basin, a tributary of the Jurumirim reservoir, Paranapanema River, Brazil. Biota Neotrop. 20(3): e20201031.). It is important to emphasize that the individual recorded lacked dark pigments (i.e., brown or black); however, its small eyes were pigmented. These characteristics fall within the definition of leucism (sensuHenle et al. 2017HENLE, K., DUBOIS, A. & VERSHININ, V. 2017. Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Mertensiella 25: 9–48.). This condition is known for Neotropical freshwater fishes (e.g., Anaguano-Yancha 2018ANAGUANO-YANCHA, F. 2018. Nuevos casos de leucismo en peces andinos del género Astroblepus (Siluriformes: Astroblepidae) Leucismo en peces andinos. Av. Cienc. Ing. 10(16): 64–73.), but we did not find records for S. marmoratus or any other synbranchid species in the wild.
It can be seen that the specimen of S. marmoratus was a large adult, with a significant length when considering the maximum known size for the species (150 cm; see Kullander 2003KULLANDER, S.O. 2003. Family Synbranchidae (Swamp-eels). In R.E. Reis, S.O. Kullander & C.J. Ferraris (Eds.), Check list of the freshwater fishes of South America (pp. 594–595). Edipucrs.). Its length suggests that leucism was not considered a deleterious or unfavorable character for the animal to survive in the aquatic environment of the Furnas megareservoir. Recently, Ferraz et al. (2023)FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189. demonstrated that for Heptapterus mustelinus (Valenciennes, 1835), leucism did not exert or negatively influence the presence of individuals with this condition in the population. In turn, Nobile et al. (2016)NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534. also recorded a large individual of Rhinelepis aspera Spix & Agassiz, 1829, with an anomaly determined as “partial albinism” (= leucism herein). Therefore, for these species, survival seems to be better related to other traits than the presence of a normal color pattern. Synbranchus marmoratus is a species that usually inhabits cavities (Kullander 2003KULLANDER, S.O. 2003. Family Synbranchidae (Swamp-eels). In R.E. Reis, S.O. Kullander & C.J. Ferraris (Eds.), Check list of the freshwater fishes of South America (pp. 594–595). Edipucrs.), which can hardly be overcome by other Neotropical predators with non-cylindrical bodies [e.g., Cichla spp., Galeocharax gulo (Cope, 1870), Hoplias spp., Salminus spp.]. Possibly, the habit of living in galleries contributed to the survival of the leucistic individual until the adult phase.
Supplementary Material
The following online material is available for this article:
Table S1–Videos posted by fishermen presenting anomalous specimens (sensuHenle et al. 2017HENLE, K., DUBOIS, A. & VERSHININ, V. 2017. Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Mertensiella 25: 9–48.) from Brazilian freshwater environments.
Acknowledgments
We are grateful to the fish farmer Bruno Ribeiro who kindly provided the specimen for this report, and Dr. Francisco Langeani (DZSJRP) for the curatorial assistance. LRPP was supported by the São Paulo Research Foundation (FAPESP) postdoctoral fellowship 2022/09727-0. FJZ thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) program [Ciências do Mar II (CIMAR II #1989/2014 proc. 23038.004309/2014-5)], FAPESP program [JP 2005#04707-5 and Biota Intercrusta #2018/13685-5], and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [PQ2# 309298/2020-2 and PQ1D #308324/2023-4] for financial support.
Data Availability
Supporting data are available at https://repositorio.unesp.br/items/3cd1bcd1-9cdb-41b6-8713-7405dbf0fc30.
References
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- ANAGUANO-YANCHA, F. 2018. Nuevos casos de leucismo en peces andinos del género Astroblepus (Siluriformes: Astroblepidae) Leucismo en peces andinos. Av. Cienc. Ing. 10(16): 64–73.
- AZEVEDO-SANTOS, V.M., PELICICE, F.M., SAZIMA, I. & HENRY, R. 2020a. A case of complete albinism in the catfish Cambeva guareiensis (Siluriformes: Trichomycteridae). Biota Neotrop. 20(4): e20201066.
- AZEVEDO-SANTOS, V.M., PELICICE, F.M. & HENRY, R. 2020b. Knowing biodiversity: Fishes from the Guareí River basin, a tributary of the Jurumirim reservoir, Paranapanema River, Brazil. Biota Neotrop. 20(3): e20201031.
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- CORREIA-SILVA, G., CORAZZA, L.Q., OTTONI, F.P., SILVA, C.V., NUNES, A.V.P., KATZ, A.M. & AZEVEDO-SANTOS, V.M. 2024. Anomalous specimens of Rhamdia quelen (Siluriformes: Heptapteridae) and Gymnotus cf. sylvius (Gymnotiformes: Gymnotidae). Cybium 48:177–180.
- FAVORITO, S.E., ZANATA, A.M., & ASSUMPÇÃO, M.I. 2005. A new Synbranchus (Teleostei: Synbranchiformes: Synbranchidae) from ilha de Marajó, Pará, Brazil, with notes on its reproductive biology and larval development. Neotrop. Ichthyol. 3: 319–328.
- FERRAZ, M., SCHULZ, U.H., LUCENA, C.A.S. & LEHMANN, P. 2023. A case of leucosis in Heptapterus mustelinus (Siluriformes, Heptapteridae) among populations of streams in southern Brazil. Has leucosis in Heptapterus mustelinus an adaptive value in shaded streams? Neotrop. Biol. Conserv. 18(3): 177–189.
- MCCARDLE, H. 2013. Albinism in Wild Vertebrates. London: LAMBERT Academic Publishing, 88 pp.
- HENLE, K., DUBOIS, A. & VERSHININ, V. 2017. Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Mertensiella 25: 9–48.
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- LIMA, S.M.Q., DE PAIVA, R., RAMOS, T. & MENDES, L. 2014. Fish fauna of Pratagi River coastal microbasin, extreme north Atlantic Forest, Rio Grande do Norte state, northeastern Brazil. Check List 10(5), 968–975.
- NOBILE, A.B., FREITAS-SOUZA, D., LIMA, F.P., ACOSTA, A.A. & SILVA, R.J. 2016. Partial albinism in Rhinelepis aspera from the Upper Paraná Basin, Brazil, with a review of albinism in South American freshwater fishes. Rev. Mex. Biodivers. 87(2): 531–534.
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- ROMANO, L.A. & PEDROSA, V.F. 2020. Leucism in South American Lungfishes Lepidosiren paradoxa Fitzinger, 1837 (Osteichthyes, Dipnoi, Lepidosirenidae) from Argentina. Braz. J. Vet. Pathol. 13(1): 51–52.
- SAZIMA, I. & POMBAL-JR, J.P. 1986. Um albino de Rhamdella minuta, com notas sobre comportamento (Osteichthyes, Pimelodidae). Rev. Bras. Biol. 46(2): 377–381.
- TORRES, R.A., ROPER, J.J., FORESTI, F. & OLIVEIRA, C. 2005. Surprising genomic diversity in the Neotropical fish Synbranchus marmoratus (Teleostei: Synbranchidae): how many species? Neotrop. Ichthyol. 3(2): 277–284.
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Publication Dates
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Publication in this collection
20 Sept 2024 -
Date of issue
2024
History
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Received
20 Nov 2023 -
Accepted
15 Aug 2024