Ichthyological notes – Notes ichtyologiques

Albinism in the smooth Gymnura micrura (, Gymnuridae): first record and morphometric

© SFI © comparisons Received: 29 Aug. 2011 Accepted: 23 Mar. 2012 Editor: R. Causse by

Marcelo Reis*, Henrique Grande, Morgana Maria Macedo & Vandick da Silva Batista (1) Résumé. - Un cas d’albinisme chez la raie-papillon glabre Gym- 1992). The colour pattern for normal specimens is a grey, brown, nura micrura (Elasmobranchii, Gymnuridae). light green or purple dorsal surface with round spots, and a white ventral surface (Bigelow and Schroeder, 1953). Ecologically, this L’albinisme est une anomalie héréditaire caractérisée par l’ab- species prefers the neritic waters of the continental shelf and is usu- sence d’un pigment, la mélanine. Des cas d’albinisme ont été rap- portés fréquemment chez les téléostéens, mais moins souvent chez ally found on soft bottoms. The species can also be found on brack- les requins et les raies. Cette note présente un cas d’albinisme chez ish estuaries or hyper-saline lagoons (Cervigón et al., 1992). une raie-papillon glabre Gymnura micrura (Bloch & Schneider, Here, we report the first record of albinism in the smooth but- 1801), femelle capturée par des pêcheurs artisanaux sur le plateau terfly ray, and present detailed morphometric comparisons of the continental du nord-est du Brésil. Aucune différence significative albino exemplar with normal specimens caught in the same area. n’a été observée entre les données morphométriques de ce spéci- We test, with such comparisons the hypothesis that the albinism has men, qui présentait un albinisme total, et des individus normale- no negative influence above morphometrics relations and charac- ment pigmentés du même sexe capturés dans la même zone. Les teristics. régressions de la largeur du disque et la longueur totale contre les largeurs du disque et le poids de 28 individus femelles (en plus The albino specimen of G. micrura was caught on 8 August de l’albinos) ont démontré que l’albinos était dans la fourchette 2010 by artisanal fishermen on the continental shelf of Alagoas normale des valeurs de l’échantillon. Par ailleurs, une analyse en State (9º40’S, 35º40’W) at 22 m depth, in a fishing site known as composantes principales (PCA), utilisant les données morphomé- São Miguel mud. As the name suggests, this site has a soft bottom triques, a placé l’albinos dans les mêmes limites que les individus of silt and is located in the delta of São Miguel River, 8.4 km from normalement pigmentés et a démontré que l’albinos était semblable the coast. morphométriquement aux échantillons normaux. Comme cela a été The specimen was caught using shrimp trawling nets (40 mm observé dans des études antérieures, nous concluons que l’albinis- me chez Gymnura micrura a une influence mineure sur sa crois- mesh in the body and 20 mm mesh in the bag). In the laboratory, sance et son histoire de vie. the specimen was identified, photographed, measured, and fixed in 10% formalin. The morphometric data were acquired according to Key words. - Elasmobranchii - Rajiformes - Gymnuridae - Gymnu- the guidelines of Compagno (1984). After processing, the specimen ra micrura - Northeastern Brazil - Pigment abnormality - Rays. was deposited under registration MUFAL-1448 in the Museum of Natural History of the Federal University of Alagoas, Northeastern Brazil. Albinism is a hereditary lack of pigmentation caused by an In order to eliminate the effects of sexual dimorphism and enzyme deficiency involving the metabolism of melanin. The type regional phenotypic variation, morphometric comparisons were of albinism can be characterized in terms of whether the lack of made between the albino and apparently ‘normal’ specimens of the pigmentation is restricted to part of the body or the entire body same sex caught in the same area. We used the data from 28 normal (Boncinelli, 1998). The proximate cause of albinism is generally female plus the albino. Regression and variance analyses (one-way attributed to lack of activity of the enzyme tyrosinase, a key com- ANOVA) were used to comparison between the albino and normal ponent of the pathway leading to the formation of melanin (Bech- specimens. Principal component analysis (PCA) was applied using tel, 1991). Total or partial albinism has been previously reported for several species of sharks and rays (Clark, 2002; Bottaro et al., 2005; Sandoval-Castillo et al., 2006). The smooth butterfly rayGymnura micrura (Bloch & Schneider, 1801) is a Rajiformes that is physically character- ized by a broad, rhomboid-shaped body with a short tail lacking a dorsal spine. The snout is obtuse and angular, with front edges of the disk concave. The tail has low dorsal and ventral finfolds and 3-4 dark crossbars (Cervigón et al., Figure 1. - Albino (left) and normal (right) specimens of Gymnura micrura.

(1) LAEPP/LABMAR/UFAL, Rua Aristeu de Andrade 452 Farol, Maceió, Alagoas, Brasil CEP. 57021-090. [[email protected]] [[email protected]] [[email protected]] * Corresponding author [[email protected]]

Cybium 2013, 37(3): 217-219. Albinism in Gymnura micrura Re i s e t a l .

Figure 2. - Regressions of log of disc width vs. log of weight (A) and log of total length vs. log of weight (B) using the albino speci- men and data from 28 female individuals of G. micrura. The albino specimen is repre- sented by the white dot.

Figure 3. - Principal component analy- sis (PCA) of morphometric data. The ellipse highlights the group formed by the albino and normally pigmented speci- mens of the same size class. The albino is represented by the white square. Squares (N3 = 20-30 cm size-class); inverse triangles (N4 = 30-40 cm), circles (N5 = 40-50 cm), lozenges (N6 = 50-60 cm), and triangles (N7 = 60-70 cm). following variables: disc width, total length, pre-oral length and of Rhinopteridae, Myliobatidae, Mobulidae, Torpedinidae, Narcini- mouth width, with the objective to verify if the albino fell within dae (Sandoval-Castillo et al., 2006) and Rhinobatidae (Ben Souissi the typical morphometric boundaries of the species. In this analy- et al., 2007). The number of albinism reports in elasmobranchs is sis the specimens were grouped into six size classes according to lower than in . One possible reason for the lower frequen- disc width (10-20 cm; 21-30 cm; 31-40 cm, 41-50 cm, 51-60 cm; cy of observations of this unusual phenotype in elasmobranchs is 61-70 cm). The albino specimen was a juvenile female measuring a lower relative abundance of cartilaginous in nature (Bonfil, 252 mm in disc width, 175 mm in total length, and 120.32 g total 1994) and a lower relative frequency of cartilaginous fish captured weight. It lacked pigmentation in the entire integument and retina in commercial catch as compared to teleosts. compared with normal specimens (Fig. 1). Such a combination Although the precise age of the specimen was not determined indicates that the specimen may be considered a case of complete by growth marks in the calcified structures, the size-weight rela- albinism. tionship did not reveal morphometric differences between the albi- Regression analyses of disc width and total length against no and normal specimens. Moreover, the literature already shows weight of 28 individuals (plus the albino) demonstrated a highly that albino elasmobranchs of considerable size have been captured significant relationship (p < 0.001). These results demonstrated that (Clark, 2002). This fact may suggest that albino individuals may eat the albino was within the normal range of sample values (Fig. 2). and grow just like normal individuals. It is possible that albinism Univariate analysis made using the disc width, total length and may be disadvantageous by making these phenotypically distinct weight, also indicated that there are no significant morphometric individuals more conspicuous to predators. By contrast, it seems differences (p0.05 = 0.71) between the albino and the normally pig- that albinism may have low influence in feeding, growth and anoth- mented specimens. er aspects of life, such reproduction (Joseph, 1961). Our results, in The PCA model explained 99.91% of the data variability. Fac- agreement with previous studies (Sandoval-Castillo et al., 2006) tor 1 explained 99.77% of explained variation and mainly repre- allows us to make the assumption that, despite being an albino phe- sents disc width, total length and weight. When the PCA data is notype that makes an individual more visible to predators, it can plotted, it reveals the existence of morphometric groups that relate exert little influence on aspects of growth and performance of these to individuals within the same size class. The albino was within the specimens. group formed by the individuals of the same size-class (21-30 cm), demonstrating that it possessed the same morphometric character- Acknowledgements. - The authors would like to thank CAPES, CNPQ and istics as normally pigmented individuals (Fig. 3). the Fundação de Amparo à Pesquisa de Alagoas – FAPEAL for financial To our knowledge, the literature contains no record of albinism support, our team in the Laboratório de Ecologia, Peixes e Pesca for the for Gymnuridae. There are, however, cases of albinism recorded in help with the field and laboratory work, Dr. Richard Ladle and Dr. Ana Mal- four species of Rajidae, two species of Dasyatidae, and one species hado for the revisions, and Dr. Nídia Fabré for constant guidance.

218 Cybium 2013, 37(3) Re i s e t a l . Albinism in Gymnura micrura

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