ANNALES · Ser. hist. nat. · 30 · 2020 · 2 193 received: 2020-09-09 DOI 10.19233/ASHN.2020.23 LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF SENEGAL (EASTERN TROPICAL ATLANTIC) Christian CAPAPÉ Laboratoire d’Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France e-mail: capape@univ-montp2.fr Youssouph DIATTA & Almamy DIABY Laboratoire de Biologie marine, Institut fondamental d’Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP 206, Dakar, Senegal Sihem RAFRAFI-NOUIRA Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d’Aquaculture de Bizerte, BP 15, 7080 Menzel Jemil, Tunisia Christian REYNAUD Laboratoire Interdisciplinaire en Didactique, Education et Formation, Université de Montpellier, 2 place Marcel Godechot, B.P. 4152, 34092 Montpellier cedex 5, France ABSTRACT In the present paper, a case of leucism/piebaldism is reported in a striped panray Zanobatus schoenleinii (Müller & Henle, 1841) captured at a low depth off the coast of Senegal (eastern tropical Atlantic). This is the second case recorded to date for this species. The specimen was sub-adult male with developed but flexible claspers, which measured 495 mm total length and 279 mm disc width, and weighed 751 g. Comments on albinism in fishes are provided in this paper, especially those reported in batoid species. Key words: morphology, colour, pigmentation, morphometric measurements, batoid species ESEMPLARE LEUCISTICO DI ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE) AL LARGO DELLA COSTA DEL SENEGAL (ATLANTICO TROPICALE ORIENTALE) SINTESI L’articolo riporta un caso di leucismo/piebaldismo in un esemplare di Zanobatus schoenleinii (Müller & Henle, 1841), catturato in acque poco profonde al largo della costa del Senegal (Atlantico tropicale orientale). Si tratta del secondo caso di questo tipo registrato fino ad oggi per tale specie. L’esemplare era un maschio sub-adulto, con pterigopodi sviluppati ma flessibili, di lunghezza totale pari a 495 mm, larghezza del disco di 279 mm e 751 g di peso. Gli autori discutono i casi di albinismo nei pesci, in particolare quelli riportati per le specie batoidi. Parole chiave: morfologia, colore, pigmentazione, misure morfometriche, specie batoidi ANNALES · Ser. hist. nat. · 30 · 2020 · 2 194 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 INTRODUCTION The striped panray, Zanobatus schoenleiniii (Mül- ler & Henle, 1841), is an endemic species known from the eastern tropical Atlantic, where it only oc- curs in the area between southern Morocco (Lloris & Rucabado 1998), Mauritania (Maurin & Bonnet, 1970), Senegal (Diatta et al., 2013), Guinea-Bissau (Sanches, 1991), and the Gulf of Guinea (Blache et al., 1970). Zanobatus schoenleinii is both commonly and abundantly captured in handicraft fishery through- out the coast of Senegal (Cadenat,1951; Séret & Opic, 1990; Capapé et al., 1995). The species inhabits shallow coastal waters not exceeding 50 m of depth (Capapé et al., 1995). In the wake of a Fig. 1: Map of the Senegalese coast indicating the capture site of the leucistic specimen of Zanobatus schoenleinii (black star). Sl. 1: Zemljevid senegalske obale z označeno lokaliteto, kjer je bil ujet belični primerek vrste Zanobatus schoenleinii (črna zvezdica). ANNALES · Ser. hist. nat. · 30 · 2020 · 2 195 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 collaboration with experienced fishermen, several Z. schoenleinii were collected in shallow coastal waters surrounding the touristic area of Dakar. All collected specimens were delivered to the laboratory for thorough examination, including the abnormal specimens described and commented in the present paper. MATERIAL AND METHODS A total of 105 specimens were captured on 25 May 2019 using trammel nets at a depth between 5 and 10 m on soft bottom, off Ouakam, a handicraft fishery site located 5 km north Dakar, in Cape Verde Peninsula, Senegal, at 14° 43’ 26’’ N and 17° 29’ 21’’ W (Fig. 1). Of these specimens, 104 were normal and one specimen abnormal, displaying non-pigmented areas on the dorsal sur- face. All specimens were measured to the nearest millimetre and weighed to the nearest gram. The normal specimens ranged between 253 mm and 580 mm in total length (TL), 154 and 340 mm in disc width (DW), and weighed between 104 and 1433 g in total body weight (TBW). However, a sub-sample includ- ing 51 normal specimens and the single abnormal specimen was used in order to obtain a more visible view, allowing to clearly distinguish this abnormal speci- men from the normal specimens. The subgroup ranged between 250 and 300 mm DW and weighed between 561 and 1346 g TBW. Morphometric measurements recorded on one of the normal specimens and the abnormal specimens are presented in Ta- ble 1, following Diatta et al. (2013). Both specimens were fixed in 10% buffered for- maldehyde, preserved in 75 % ethanol and deposited in the Ichthyological Collection of the Institut Supérieur d’Aquaculture et de Pêche of Bizerte (Tunisia), receiving catalogue numbers, ISPAB-Zan-sch-01 for the normal specimen and ISPAB-Zan- sch-02 for the abnormal specimen. The relation between DW and TBW was used as a complement following Fro- ese et al. (2011), including all specimens, normal and abnormal, to show if this latter would have been able to develop in the wild like normal specimens. This relation, TBW = aDWb, was converted into its linear regression, expressed in decimal logarithmic coordinates, and correlations were assessed by least-squares regres- sion as: log TBW = log a + b logDW. Significance of constant b differences was assessed according to the hypothesis of isometric growth if b = 3, positive allometry if b > 3, negative isometry if b < 3 (Pauly, 1983). These two latter tests were performed by us- ing logistic model STAT VIEW 5.0. RESULTS AND DISCUSSION All normal specimens were identified as Zanoba- tus schoenleinii following the combination of main Fig. 2: Normal specimen of Zanobatus schoenleinii (Ref. ISPAB- Zan-sch-01), from the coast of Senegal. Dorsal surface, scale bar = 100 mm. Sl. 2: Normalni primerek vrste Zanobatus schoenleinii (Ref. ISPAB- Zan-sch-01) iz senegalske obale. Hrbtna stran, merilo = 100 mm. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 196 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 morphological characters: disc sub-circular, wider than long; snout blunt, angle nearly 120° in front; nostrils narrow, anterior valves connected across the internarial space; mouth straight; teeth small; spiracles large without folds; dorsal and caudal fins small and rounded; covered by a rigid skin, unlike and minute scales, a medial row of thorns in disk and tail, and three rows arranged in an arc of circle on each shoulder; back brown with dark cross bands with white spots in between near the pectoral edges (Tab. 1; Fig. 2). Such description is in total agree- ment with Garman (1913), Cadenat (1951), Blache et al. (1970), and Séret & Opic (1990). The abnormal specimen was a sub-adult male of Zanobatus schoenleinii, with developed but flexible claspers, measuring 495 mm TL, 279 mm DW and 751 g TBW (Tab. 1; Fig. 3). The central part of the disc was brown with dark spots externally larger and abundant on the central part of the disc, conversely, dark cross bands were totally lacking. An area sur- rounding eyes and spiracles was clear and whitish. The edges of both pectorals were largely clear, both dorsal fins and caudal fin whitish, belly entirely beige. The eye colour was black, which confirmed that the specimen was simultaneously leucistic and piebald and not a true albino (sensu Quigley et al. (2019). It is the second case reported for Z. schoen- leinii, a similar specimen was previously collected from the coast of Senegal (Diatta et al., 2013). Quigley et al. (2019) noted that albinism is a disor- der controlled by different genes in which the pigment melanin is absent or non-functional. Additionally, leucism is a partial lack of pigmentation of the skin controlled by a single recessive allele (Jones et al., 2016). The term partial albinism or pseudo-albinism was previously used, but is now considered obsolete (Van Grouw, 2006). Lipej et al. (2011) showed that large albino specimens of marbled torpedo Torpedo marmorata Risso, 1810 could also be captured in the wild and that, consequently, total or partial albinism does not compromise life and development. Similar patterns were also reported for the striped panray (Diatta et al., 2013). The relationship log DW versus log TBW is log TBW = -6.97 + 4.07 * log DW; r = 0.94, n = 52. It appears a positive allometry but the leucistic piebald specimen which clearly displays a TBW lower than this of the other specimens (Fig. 4). Following the opinion of Quigley et al. (2019), such pattern suggests that this abnormal specimen did not develop like other normal specimens in the wild due to being Fig. 3: Leucistic piebald specimen of Zanobatus schoenleinii (Ref. ISPAB- Zan-sch-01) from the coast of Sene- gal. A. Dorsal surface, scale bar = 80 mm. B. Ventral surface, scale bar = 100 mm. Sl. 3: Belični piebaldistični primerek vrste Zanobatus schoenleinii (Ref. ISPAB- Zan-sch-01) iz senegalske obale. A. Hrbtna stran, merilo = 80 mm. B. Trebušna stran, merilo = 100 mm. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 197 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 Tab. 1: The morphometric measurements (in mm and as % DW) and total body weight recorded in the leucistic piebald specimen of Zanobatus schoenleinii (ISPAB-Zan-sch-02) and compared to a normal specimen (ISPAB-Zan-sch-01), both from the coast of Senegal. Tab. 1: Morfometrične meritve (v mm in kot % DW) in celotna telesna masa pri beličnemu piebaldističnemu primerku vrste Zanobatus schoenleinii (ISPAB-Zan-sch-02) v primerjavi z normalnim primerkom (ISPAB-Zan-sch-01). Oba sta bila ujeta ob senegalski obali. References ISPAB-Zan-sch-01 ISPAB-Zan-sch-02 Measurements MM % DW MM % DW Total length 559 194.8 495 177.4 Disc length 313 94.8 255 91.4 Disc width 330 100.0 279 100.0 Disc depth 44 13.3 34 12.2 Eyeball length 17 5.2 18 6.5 Pre-orbital length 70 21.2 59 21.2 Inter-orbital length 26 7.9 28 10.0 Spiracle diameter 23 6.7 19 6.8 Interspiracular width 33 10.0 30 10.8 Space between eye and spiracle 13 3.9 11 3.9 Pre-oral length 72 21.2 60 21.5 Mouth width 43 13.0 43 15,4 First gill-slit 8 2.5 9 3.2 Fifth gill-slit 7 2.4 7 2.5 Width between first gill-slit 82 24.8 69 24.7 Width between fifth gill-slit 51 15.5 43 15.4 Snout tip to eye 81 24.3 68 24.4 Snout tip to mouth 81 24.3 68 24.4 Snout tip to first gill-slit 106 32.1 102 36.6 Snout tip to fifth gill-slit 150 45.5 132 47.3 Snout tip to vent 270 81.8 225 80.7 Pectoral fin anterior margin 205 71.4 185 66.3 Pectoral fin posterior margin 184 62.1 143 51.3 Pelvic fin anterior margin 50 15.2 48 17.2 Pelvic fin posterior margin 77 23.3 55 19.7 Second dorsal inneredge 10 3.0 11 3.9 Interdorsal distance 30 9.1 32 11.5 Second dorsal to caudal birth 28 8.6 35 12.5 Total body weight 1507 751 ANNALES · Ser. hist. nat. · 30 · 2020 · 2 198 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 maladapted. But it could also explain why of the 633 batoid species known to date worldwide, only 22 cases of albinism, leucism and piebaldsim had been reported (Quigley et al., 2018), 23 including the present specimen. Talent (1973) noted that lack of pigmentation could be considered as disadvantage for sharks and rays, calling the attention of possible predators to their presence in the wild. Generally, abnormal specimens are considered of lower value than normal specimens among fishermen and are sometimes discarded at sea; this could also explain their scarcity in fish landings. Unfavourable envi- ronmental conditions, such as large exposure to pollutants, could also play a role in the lack of pigmenta- tion, especially in species living a benthic zones, such as Zanobatus schoenleinii. Such phenomenon was particularly observed in batoids, which generally inhabit sandy-muddy bottoms (Ribeiro-Prado et al., 2008; Diatta et al., 2013). The fact that albi- nos, leucistic and piebald specimens are more sensitive to pollutants than normal specimens remains a valid hypothesis, which should, however, be validated by further studies. Since Diop et al. (2012) and Bonnin et al. (2016) report that the coast of Senegal, especially around the touristic area of Dakar, has been, for decades, increasingly exposed to pollutants in the wild and their impact on the local biodiversity cannot be totally ruled out, the presently studied case could be a good instance of that. Fig. 4: Total body mass (TBM) versus disc width (DW) relationship expressed in logarithmic co-ordinates for normal and leucistic piebald specimens of Zanobatus schoenleinii collected from the coast of Senegal. Sl. 4: Odnos med celotno telesno maso (TBM) in širino diska (DW), iz- ražen v logaritmični skali pri normalnih in leucističnih piebaldističnih primerkih vrste Zanobatus schoenleinii, ujetih ob senegalski obali. ANNALES · Ser. hist. nat. · 30 · 2020 · 2 199 Christian CAPAPÉ et al.: LEUCISTIC PIEBALD STRIPED PANRAY, ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE), FROM THE COAST OF ..., 193–200 BELIČNI PRIMEREK VRSTE ZANOBATUS SCHOENLEINII (CHONDRICHTHYES: ZANOBATIDAE) IZ SENEGALSKE OBALE (VZHODNI TROPSKI ATLANTIK) Christian CAPAPÉ Laboratoire d’Ichtyologie, Université de Montpellier, case 104, 34095 Montpellier cedex 5, France e-mail: capape@univ-montp2.fr Youssouph DIATTA & Almamy DIABY Laboratoire de Biologie marine, Institut fondamental d’Afrique noire, (IFAN Ch. A. Diop), Université Cheikh Anta Diop de Dakar, BP 206, Dakar, Senegal Sihem RAFRAFI-NOUIRA Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d’Aquaculture de Bizerte, BP 15, 7080 Menzel Jemil, Tunisia Christian REYNAUD Laboratoire Interdisciplinaire en Didactique, Education et Formation, Université de Montpellier, 2 place Marcel Godechot, B.P. 4152, 34092 Montpellier cedex 5, France ABSTRACT V pričujočem prispevku avtorji poročajo o primeru beličnosti/piebaldizma pri vrsti skata Zanobatus schoenleinii (Mül- ler & Henle, 1841), ujetega v plitvini ob obali Senegala (tropski vzhodni Atlantik). Gre za drugi primer pojava te anomalije pri tej vrsti. Primerek je bil subadultni samec, ki je meril 495 mm v dolžino, 279 mm v premeru diska in tehtal 751 g, ter imel razvita, a še vedno prožna klasperja. Avtorji nadalje razpravljajo o primerih albinizma, še posebej tistih pri skatih. 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