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The present study aims to understand how ecological and biological factors affect the Hg levels in stingrays occurring in the Northeastern Brazilian coast. Total mercury (Hg), methylmercury (MeHg) and stable isotope (δ13C and δ15N) analyses were performed in five species. Hypanus americanus and Gymnura micrura showed the highest total Hg concentrations (300 and 176 ng.g−1, respectively). Hypanus guttatus exhibited a significant correlation between total Hg and size. Both species of the genus Hypanus presented the highest percentage of MeHg, around 100%, whereas the other species showed median percentages below 50%. The δ13C and δ15N signatures suggest that all studied species present the same foraging habitat but different trophic positions. Trophic position and animal size were the main factors influencing total Hg and MeHg concentrations in batoid species. The genus Hypanus, present in the Brazilian fish markets, showed concentrations above the accepted limits for human consumption.

Gymnurahemecus bulbosus gen. et sp. nov. infects the heart of smooth butterfly rays, Gymnura micrura in the Gulf of Mexico. Gymnurahemecus differs from all other accepted aporocotylid genera by having one column of C-shaped lateral tegumental spines, a medial oesophageal bulb anterior to a diverticulate region of the oesophagus, inverse U-shaped intestinal caeca, a non-looped testis, an oviducal ampulla, a Laurer's canal, and a post-caecal common genital pore. The new species, the shark blood flukes (Selachohemecus spp. and Hyperandrotrema spp.), and the chimaera blood fluke Chimaerohemecus trondheimensis are unique by having C-shaped lateral tegumental spines. Selachohemecus spp. and the new species have a single column of lateral tegumental spines, whereas Hyperandrotrema spp. and C. trondheimensis have 2-7 columns of lateral tegumental spines. The new species differs from Selachohemecus spp. most notably by having an inverse U-shaped intestine. The other ray blood flukes (Orchispirium heterovitellatum, Myliobaticola richardheardi, and Ogawaia glaucostegi) differ from the new species by lacking lateral tegumental spines, a medial oesophageal bulb, and a Laurer's canal and by having a looped testis. Phylogenetic analysis using large subunit ribosomal DNA (28S) indicated that the new species is sister to the clade that includes the other sequenced adult blood fluke (O. glaucostegi), which infects a ray in Australia. These results agree with and extend previous morphology- and nucleotide-based phylogenetic assertions that the blood flukes of early-branching jawed craniates (Chondrichthyes) are monophyletic and phylogenetically separated from the blood flukes of later-branching ray-finned fishes (Actinopterygii: Euteleostei).

A new species of Empruthotrema Johnston & Tiegs, 1922 is described based on specimens collected from the olfactory sacs of smooth butterfly rays Gymnura micrura (Bloch & Schneider) captured in Mobile Bay (northcentral Gulf of Mexico), Alabama, USA. Empruthotrema longipenis n. sp. is most similar to the type-species Empruthotrema raiae (MacCallum, 1916) Johnston & Tiegs, 1922 by having 12 marginal and two interhamular loculi with members of haptoral hook pair 1 located midway along the periphery of each interhamular loculus and those of hook pair 2 located at the marginal termini of the bilateral septa flanking the interhamular loculi. Empruthotrema longipenis n. sp. differs from E. raiae by having a much longer male copulatory organ and from its remaining congeners by the sinistral and extracecal ejaculatory bulb flanking the pharynx, the number of interhamular and marginal septa, and the distribution of hook pairs 1 and 2 along the haptoral margin. This is the first report of a monocotylid from the smooth butterfly ray and from Mobile Bay. The diversity of haptoral morphotypes among the currently accepted species of Empruthotrema is detailed and discussed in the context of monophyly of the genus.

Globalmente a explotacao dos peixes cartilaginosos marinhos e cada vez mais crescente principalmente em areas costeiras. Entretanto, existem areas no Atlântico Sul Ocidental que ainda sao pouco conhecidas quanto a sua biodiversidade de elasmobrânquios. Portanto, o objetivo deste trabalho e de conhecer a comunidade de elasmobrânquios marinho-estuarinos e suas respectivas areas de uso em uma unidade de conservacao de uso sustentavel (APA do Delta do Parnaiba), no nordeste do Brasil, a partir do monitoramento dos desembarques da pesca artesanal na regiao. A partir do monitoramento de 1184 desembarques realizados entre janeiro de 2016 e janeiro de 2017, foi possivel identificar nove especies de tubaroes ( Carcharhinus leucas, C. porosus, C. acronotus, C. limbatus, Galeocerdo cuvier, Sphyrna mokarran, S. lewini, Rhizoprionodon porosus e Ginglymostoma cirratum ) e sete especies de raias ( Hypanus guttatus, H. americanus, H. marianae, Fontitrygon geijskesi, Gymnura micrura, Aetobatus narinari e Rhinoptera bonasus ) que fazem uso de tres areas batimetricamente distintas. As especies com as maiores frequencias de ocorrencia foram R. porosus (36%) e H. gutattus (61%). Os resultados demonstram que a area e utilizada por distintas especies, dentre elas especies consideradas em risco de extincao, como o S. mokarran . USE OF AN ENVIRONMENTAL PROTECTION AREA BY A COMMUNITY OF ELASMOBRANCHS IN THE TROPICAL SOUTHWESTERN ATLANTIC ABSTRACT Worldwide the exploitation of marine cartilaginous fi sh is increasing, mainly in coastal regions. However, there are areas in the Southwestern Atlantic that are still little known about their elasmobranch biodiversity. Therefore, this work aims to know the community of marine estuarine elasmobranchs and their respective areas of use in a sustainable use conservation unit (APA of the Parnaiba Delta), in the northeast of Brazil, from the monitoring of the landings of the fi shing in the region. From the monitoring of 1184 landings between January 2016 and January 2017, it was possible to identify nine species of sharks (Carcharhinus leucas, C. porosus, C. acronotus, C. limbatus, Galeocerdo cuvier, Sphyrna mokarran, S. lewini, Rhizoprionodon porosus and Ginglymostoma cirratum) and seven species of stingrays (Hypanus guttatus, H. americanus, H. marianae, Fontitrygon geijskesi, Gymnura micrura, Aetobatus narinari and Rhinoptera bonasus) which make use of three diff erent depth ranges. The most frequent species were R. porosus (36%) and H. gutattus (61%). The results demonstrate that the area is used by diff erent species, among them species considered endangered, such as S. mokarran. Keywords: Selachians; Batoids; Conservation biology.

An extensive taxonomic revision of Gymnura micrura based on external and internal morphology, and considering specimens from its entire geographical distribution in the Atlantic Ocean, is presented. Gymnura micrura is redescribed and a neotype is designated; its distributional range is limited to the Southwestern Atlantic. Two new species of butterfly rays are described: Gymnura lessae , sp. nov., occurring in the North and Central Western Atlantic, and Gymnura sereti , sp. nov., found in the Eastern Central Atlantic. The three species are morphologically very similar (with G. micrura most similar to G. lessae , sp. nov.) and cannot be distinguished based on the primary diagnostic characters typically utilized for butterfly rays. The dorsal color, smaller size and eventual presence of a dorsal fin in some males may be helpful to distinguish G. micrura , whereas the size and morphology of the clasper are the main external characters separating G. sereti , sp. nov., from the other two species, although the shape of disc (especially among adult males) and contour of the lower lip are also helpful. Despite the skeleton being conservative among the species, we found consistent variations that support the validity of the new species described. Due to similarity in external morphology these internal characters were fundamental to discriminate the new species. The scapulocoracoid was an important diagnostic skeletal structure, exhibiting a series of variations that separated the three species. Variations in the synarcual, outline of the dorsal cranial fontanelle, number and shape of mesopterygia, and small differences in the mandibular arches and pelvic girdle were useful to diagnose G. sereti, sp. nov. The contour of the hyomandibula was an important diagnostic character distinguishing G. lessae , sp. nov., from the other two species. Meristic data were also useful, with G. sereti, sp. nov., presenting a lower number of radials in the second element of the mesopterygium and a higher number of diplospondylous vertebrae. In contrast, G. lessae , sp. nov., presented a higher number of pectoral-fin radials. Subtle, but consistent differences, were also found in the design of the ventral lateral-line system. A Canonical Discriminant Analysis provides strong statistical support for the validity of the new species, significantly distinguishing the three species groupings ( p < 0.00001). External morphology, ventral lateral-line system and skeleton are described and illustrated for all three valid species.

Gymnura micrura (Bloch & Schneider 1801) Smooth (or Lesser) Butterfly Ray (Figs. 1–10, 34a, 35, 36a – 38a, 39–41, 42a – 44a, 45, 46a – 48a; Tabs. 1–2) Raja micrura Bloch & Schneider, 1801: 360 (original description, type locality: Suriname) ? Trygon micrura: Müller, 1837: 40 (not seen: Rio de Janeiro, according to Bigelow & Schroeder [1953] identification probable because said to agree with description of Raja micrura of Bloch & Schneider 1801). Pteroplatea maclura: Puyo, 1936: 79, 250 (French Guiana; not seen). Pteroplatea maclura (in part): Müller & Henle, 1841: 169 (description, specimens from Suriname and Brazil only); Duméril, 1865: 614 (description, specimens from Brazil only, size probably erroneous as the New York specimen [= G. lessae, sp. nov.] recorded with a width of 2 meters is the same specimen analyzed by Müller & Henle, 1841, who had earlier characterized it as small); Günther, 1870: 487 (description, specimen from Brazil only). Pteroplatea micrura: Metzelaar, 1919: 8, 199 (listed, Trinidad, perhaps Curaçao). Pteroplatea micrura (in part): Meek & Hildebrand, 1923: 87 (not present in Panamá, color description matching G. lessae, sp. nov.). Gymnura micrura: Nishida, 1990: 65, 66, 83, 84, fig. 59B (skeletal morphology, clasper;?Suriname); Lovejoy, 1996: 214, 215, 223, 224, 227, 228, 230, 236, 242, 256, fig 7E (lateral line canals, skeletal morphology; Guianas and Suriname); Mazzoleni & Schwingel, 1999: 144, 116 (listed, Southern Brazil); Menni & Stehmann, 2000: 92 (distribution, South America); Furtado Jr. et al. 2003: 8, 9 (fisheries, North Brazil); Carvalho et al., 2004: 10, 33, 38, 39, 74, 79, 82, 86, 87, figs. 15, 31, 35B, 36C-B, 38C, 39A-B (skeletal morphology, Suriname); Meneses et al. 2005: 80, 82 (listed; Sergipe, Brazil); Nunes et al. 2005: 51, 52, 53 (inventory; Maranhão, Brazil); Yokota & Lessa, 2006: 349 –360 (nursery area, Northeastern Brazil); Yokota & Lessa, 2007: 249 –257 (reproductive biology, Northeastern Brazil); Basílio et al. 2008: 67 – 69 (checklist; Curu River estuary, Ceará, Brazil); Lessa et al. 2008 (fisheries, Northeastern Brazil); Basilio et al. 2009: 41 (listed; Ceará, Brazil); Bornatowski et al. 2009: 3 (listed; Southern Brazil); Nunes & Piorski, 2009: 479 –482 (presence dorsal fin; Maranhão, Brazil); Reis et al. 2012: 217 –219 (albinism; Alagoas, Brazil); Yokota et al., 2012: 1315 –1326 (reproductive biology, Northeastern Brazil); Ragno, 2013: 57, 58, 130, 177, fig. 46 (lateral line; Rio Grande do Norte, Brazil); Yokota et al., 2013: 1325 –1329 (diet, Northeastern Brazil); Fontenelle & Carvalho, 2015: 7 –9, figs. 8, 9E, 10E (brain morphology; Rio Grande do Norte, Brazil); Garcia Jr. et al., 2015: 4 (checklist; Rio Grande do Norte, Brazil); Willems et al., 2016: 36, 38, 40, 41 (fisheries, Suriname). Gymnura micrura (in part): Rosenberger, 2001: 615, 616, 618, 620, 621, 623–627 (systematics, specimen FMNH 89993 only [Suriname],?FMNH 89992); McEachran & Carvalho, 2002: 577 (identification guide, Western Central Atlantic; illustration is of G. lessae, sp. nov.). Not Raja maclura: Lesueur, 1817: 41, pl. not numbered (original description, Newport, Rhode Island, junior synonym of G. altavela). Not Pteroplatea micrura: Müller & Henle, 1841: 169 (Java, India, Red Sea; = Gymnura poecilura [Shaw, 1804]); Cantor, 1849: 1409 (= G. poecilura [Shaw, 1804]); Blyth, 1860: 29 (= G. poecilura [Shaw, 1804]); Day, 1865: 278 (= G. poecilura [Shaw, 1804]); Duméril, 1865: 613 (description, mouth of Ganges, = G. poecilura, [Shaw, 1804]); Günther, 1870: 487 (= G. poecilura [Shaw, 1804]); Day, 1878: pl. CXCIV, fig. 2 (= G. poecilura [Shaw, 1804]); Day, 1889: 56, fig. 23 (= G. poecilura [Shaw, 1804]); Wood-Mason & Alcock, 1891: 359 –367, pl. 7–8 (embryonic development, = G. poecilura [Shaw, 1804]); Alcock, 1892: 1 –8, pl. 4 (embryonic development, = G. poecilura [Shaw, 1804]); Annandale, 1909: 39 (= G. poecilura [Shaw, 1804]); Pillay, 1929: 353 (= G. poecilura [Shaw, 1804]). ?Not Gymnura sp. cf. micrura: Compagno & Last, 1999: 1507, 1509 (identification guide, Western Central Pacific); Randall & Lim, 2000: 583 (checklist, South China Sea); Jacobsen & Bennett, 2009: 1, 21, 22, 24, 25 (taxonomic revision, Indo-West Pacific). Not Gymnura micrura: Fowler, 1941: 455 (description based on a G. australis [Ramsay & Ogilby] specimen [USNM 39978]); Talwar & Kacker, 1984: 181 (= Gymnura poecilura [Shaw, 1804]); Raje, 2003: 89, 91–95 (probably equals Gymnura poecilura [Shaw, 1804]); Raje et al. 2007 (= Gymnura poecilura [Shaw, 1804]). Neotype. USNM 156714 (289 mm DW, adult male), Suriname, 6o20’45”N, 54o56’30”W, 0 to 26m, Vessel Coquette, station 145, trawl, 30.v.1957, accession num. 215120, USNM 440341 recatalogued from USNM 156714 (Fig. 1). Designated herein. Diagnosis. A small to medium size butterfly ray occurring in the Western South Atlantic distinguished from congeners (except the two new species described in this study) by the combination of the following characters: absence of spiracular tentacle and caudal stings; dorsal fin usually absent (a small dorsal fin may be present in some males); tail relatively short (mean post-cloacal length 22% DW) and prominently banded, presenting 3 to 5 black bands that may be less distinct in large adults. Gymnura micrura is distinguished from G. lessae, sp. nov. and G. sereti, sp. nov. by its usually uniformly brown or gray dorsal disc, without any vermiculate pattern (vs. dorsal side brownish, usually with a vermiculate pattern in both new species). Gymnura micrura may be further distinguished from G. sereti, sp. nov. by the following characters: clasper of mature males more slender and longer, Lclasper 9.3–11% DW (vs. clasper stouter and shorter, Lclasper 6.8–9.2% DW); cranial fontanelle U-shaped (vs. keyhole-shaped fontanelle); mesopterygium divided into one anterior solid element and 5–7 smaller fragments (vs. mesopterygium divided into two solid elements); distance between anteroventral (AVF) and posteroventral (PVF) fenestrae of scapulocoracoid representing 30–35% of scapulocoracoid length (vs. distance between AVF and PVF representing about 20% of scapulocoracoid length); lateral projection of the base of synarcual starting at its anterior third (vs. lateral projection of the base of synarcual starting synarcual half-length); thicker proximal portion of Meckel’s cartilage representing 28–40% of Meckel’s cartilage width (vs. 10–24%); lower number of diplospondylous vertebrae (mean 98 vs. 110, respectively), and higher number of radials associated to the mesopterygial fragments compared to the second mesopterygial element of G. sereti (range 15–17 vs. 10–15, respectively). Gymnura micrura is most similar to G. lessae, sp. nov., but may be further differentiated from it by the following characters: dorsal contour of hyomandibula with two conspicuous humps (vs. dorsal contour of the hyomandibula with a conspicuous proximal protuberance followed by an inconspicuous distal protuberance); projection of the anteroventral fenestra of coracoid bar in the form of a funnel with a large opening and closing (vs. projection of the anteroventral fenestra with a relatively narrower opening and end) and lower number of pectoral radials (range 112–119 vs. 118–127, respectively). Other diagnostic differences are described below. Description. Measurements are presented in Table 1; meristic data in Table 2. The following description is based on all specimens examined. Throughout the text the proportions are presented as: minimum value–maximum value (mean). See Figs. 1–4, 5a–h, 6a and 7–9 for external morphology and color, Fig. 34a for ventral lateral-line pattern, Figs. 5i, 6b, 35, 36a – 38a, 39–41, 42a – 44a, 45 and 46a – 48a for skeletal morphology and Fig. 10 for geographical distribution. External morphology. Disc lozenge shaped, 1.54–1.92 (1.75) times broader than long [1.54–1.72 (1.64) for adult males; 1.75–1.92 (1.81) for adult females]. Trunk strongly flattened, slightly raised above scapular region and posterior head. Snout relatively short and obtuse with a subtle lobe at snout tip. Sexual dimorphism evident in disc shape, mainly between adults, with adult males presenting proportionally longer snouts with smaller angles, which confers a triangular shape to the anterior half of the disc (Fig. 2). Preoral snout length 8.6–14 (11)% DW [8–11 (9)% DW in adult females; 12–14 (13)% DW in adult males], preorbital snout length 6.1–13 (9.4)% DW [7–10 (8)% DW in adult females; 10–13 (11)% DW in adult males], preorbital snout width 31–40 (37)% DW, postspiracle snout width 42–54 (49)% DW. Anterior margins of disc with a slight medial concavity and becoming weakly convex towards extremities (in adult males these curves may be less noticeable, with the anterior margins almost straight in some males) (Fig. 2); pectoral-fin apices acutely angular (sometimes moderately angular in adult males); posterior margins weakly convex; free rear tip broadly rounded; axis of greatest width positioned posteriorly to one-half disc length. Pelvic fin single lobed, rectangular, their corners rounded (Fig. 3). Skin entirely smooth, without denticles on dorsal and ventral surface of the disc. Interorbital space broad, interorbital width 7.9–9.8 (8.7)% DW. Eyes dorsolateral, small, oval and protruding slightly; eye diameter 1.2–2.2 (1.7)% DW, representing 13–25 (19)% of interorbital width; orbit diameter 1.9–3.5 (2.5)% DW, representing 59–108 (86)% of spiracle length. Eyes more protruded and relatively larger in embryos. Spiracles immediately following the eyes, relatively large, lozenge-shaped, contour of the inner spiracular margin concave (Fig. 4a); spiracle length 2.1–4 (2.9)% DW, 1.1–2.7 (1.8) times eye diameter; its inner posterior margin without tentacles. Ventral head length 20–27 (23)% DW. Nostrils narrowly oval, diagonally directed, only the circular distal margin not covered by nasal curtain, posterior lateral margin with lobe (Fig. 4c); nostril length 1.8–4.3 (3.2)% DW [2.5–3.4 (2.9)% DW in adult females; 3.1–4.3 (3.7)% DW in adult males], 1.0–3.0 (1.8) times internasal width; internasal width 1.1–2.7 (1.8)% DW. Anterior nasal flaps medially expanded and fused into a broad, skirt-shaped, posteriorly expanded nasal curtain that covers the internasal space and reaches mouth (Fig. 4b). Nasal curtain skirtshaped, weakly to moderately bilobed, wide, its width 1.9–4.3 (3.0) times length; lateral margin concave; posterolateral apices rounded; posterior margin straight to weakly concave, a small gap may be present medially. Mouth relatively wide, its width 7.5–10 (8.5)% DW, 32–45 (38)% head length, 0.9–1.8 (1.2) times nasal curtain width; without papillae on floor or labial folds, although some striations may originate radially from mouth corners; lower lip arched rearward toward corners, uniformly convex or weakly to moderately concave along medial region, without any lump or knob (Fig. 4b); a strip of corrugated skin forms a half-circle below mouth; strips ends at the mouth corners. Small, numerous and closely crowded teeth in bands; teeth with one medial, pointed cusp directed towards inside of mouth; tooth base somewhat swollen, entirely twisted to the opposite direction; in labial face, tooth resembling a three-armed boomerang (Fig. 4d); teeth similar between jaws and sexes; their number increasing with growth. Gill slits moderately S-shaped, first four gill slits markedly larger than fifth (Fig. 4b). Distance between gill slits decreasing posteriorly; distance between inner ends of fifth pair 60–74 (67)% distance between inner ends of first pair; distance between inner ends of first pair 15–18 (16)% DW, 58–82 (72)% ventral head length, 6.3–14.0 (9.3) times internasal width; distance between inner ends of fifth pair 10–12 (11)% DW, 40–56 (48)% ventral head length, 4.1–9.3 (6.3) times internasal width. Tail slender and short, whip-like, cross-banded (see section on color), tapering toward tip, without caudal stings at any age (Fig. 9); postcloacal tail 17–30 (22)% DW, 30–47 (38)% DL, 30–56 (45)% precloacal length; tail usually lacking dorsal fin, however some males (about 25% of males) may present a small plesodic dorsal fin at tail base with varying degrees of development (Figs. 5a–h); when present the dorsal fin is situated at the level of free rear tips of pelvic fin, distance from snout tip to anterior base of the dorsal fin representing 76–80 (78)% of total length; low longitudinal skin folds present on dorsal and ventral surfaces of tail, skin folds not reaching the tail tip. Clasper of mature males cylindrical, somewhat depressed, relatively slender and longer (compared to G. sereti, sp. nov.) (Fig. 6); distance from posterior margin of cloaca to clasper tip 9.3–11.0 (9.9)% DW; clasper tapering slightly distally; clasper tip conical, bluntly pointed to pointed, not calcified; portion not calcified relatively shorter than in G. lessae, sp. nov. and G. sereti, sp. nov.; apopyle (on the anterior dorsal surface) connected to hypopyle by a long, dorsomedial, posteriorly curved clasper groove; spermatic duct almost reaching clasper tip; rhipidion and pseudorhipidion (“small flap” of Nishida 1990) absent; a long ventral pseudosiphon (“SAC 1” of Nishida 1990) laterodistally situated to hypopyle; a well-developed dorsal pseudosiphon (“SAC 2” of Nishida 1990) on inner margin of clasper; dorsal pseudosiphon more posteriorly located when compared to G. sereti, sp. nov.; ventral surface of clasper entirely smooth. Coloration. Dorsal side usually uniformly light to dark brown, grayish, sometimes slightly roseate, not vermiculated (Figs. 7a, 8); irregular dark patches or irregular dark round spots may be present, especially in freshly caught specimens (Figs. 7b, c). Living specimens may be variable in color according to the environment (Figs. 7d, e), but they tend to become uniformly brown or gray when preserved. Ventral surface whitish to brownish, creamy, slightly roseate, yellowish or copper, generally darkening toward edges. Tail prominently cross-banded, with 3–5 black bands (Fig. 9a); bands diffuse or less distinct in large specimens (Fig. 9b). Size, reproduction, diet and habitat. Size at birth ranging from 135 to 185 mm DW; size at 50% maturity was estimated at 269 (265–273) mm and 405 (401–409) mm for males and females, respectively (Yokota et al. 2012). The largest male analyzed was 360 mm DW (MZUSP 9926, from Espírito Santo, Brazil), and males of this species shall reach a maximum of 450 mm DW. The largest female analyzed was 629 mm DW (sampled in Rio Grande do Norte, Brazil, by the first author) and the females reach around 800 mm DW. This species is matrotrophic viviparous (lipid histotrophy) and appears to be reproductively active throughout the year, producing 1–6 young per litter (Yokota et al. 2012). Diet consists mainly of bony fishes with evidence of feeding specialization, ingesting intermittently proportionally larger fishes (Yokota et al. 2013). This is a demersal species living along the coast on sandy and muddy bottoms, but also occurs in estuaries. Geographical distribution. According to material examined, G. micrura is distributed in the Atlantic coast of South America from Venezuela (including Trinidad & Tobago) to Rio de Janeiro State, Brazil (Fig. 10). The species is also registered in São Paulo and Paraná States, Brazil (Gonzalez 1995, P. Charvet, pers. comm.). The species is relatively common in the north of South America and northern and northeastern regions of Brazil, with its abundance declining towards the south, where its occurrence may be related to seasonal warmer water. There are no confirmed records of this species in Colombia and Panama (Meek & Hildebrand 1923, Mejía-Falla et al. 2007), and it is not known if the species occurs in the Caribbean Sea, beyond the Venezuelan coast. Remarks. The original description of Gymnura micrura (as Raja micrura Bloch & Schneider 1801) is brief, nondiagnostic, presenting characters that are commonly shared by all species in the genus, and is not illustrated; however, the type locality is clearly stated as Suriname (“Habitat in Surinamo”, p. 360). This fixed the name micrura to the butterfly ray without caudal stings and spiracular tentacles commonly found in the region, in contrast to G. altavela (Linnaeus 1758), which possesses spiracular tentacles and caudal stings and does not occur in the area. Bloch & Schneider mention that type material would probably be housed in the “Museo Vaillanti Parisiis”. After an exhaustive search in the Muséum national d'Histoire naturelle in Paris and other collections, we are not able to locate any type material for G. micrura. At the same time, this type material was never mentioned in any study subsequent to the original description (e.g. Séret & McEachran 1986) and is considered to be unknown in Eschmeyer et al. (2017); the type material was probably lost or destroyed. As this species is central to a complex taxonomic problem, in which three distinct species were being identified under the name G. micrura (two of these are described as new here), the designation of a neotype for this species is expressly required to define the nominal taxon objectively and clarify its taxonomic status. The designed neotype matches the available information from the original type locality. Fowler (1941) characterized the type locality of Bloch & Schneider as “likely erroneous” but without further comment. This author probably made this comment because the species he named G. micrura is not that of Bloch & Schneider, but a misidentification of Gymnura from the Indian Ocean and Indo-Pacific region. His description of G. micrura, for example, is based on a specimen of G. australis (Ramsey & Ogilby 1886) (USNM 39978). Hence, a type locality in South America for a species from the Indo-Pacific region is erroneous. Müller & Henle (1841) mistakenly applied the specific name micrura to G. poecilura of Shaw (1804), and were followed by many others authors (e.g. Cantor 1849, Blyth 1860, Day 1865, Duméril 1864, Günther 1870, Day 1878, 1889, Wood-Mason & Alcoc, Published as part of Carvalho, Marcelo Rodrigues De, 2017, Taxonomic and morphological revision of butterfly rays of the Gymnura micrura (Bloch & Schneider 1801) species complex, with the description of two new species (Myliobatiformes: Gymnuridae), pp. 1-74 in Zootaxa 4332 (1) on pages 6-19, DOI: 10.11646/zootaxa.4332.1.1, http://zenodo.org/record/1052041, {"references":["Bloch, M. E. & Schneider, J. G. (1801) M. E. Blochii, Systema Ichthyologiae Iconibus cx Ilustratum. Post obitum auctoris opus inchoatum absolvit, correxit, interpolavit Jo. Gottlob Schneider, Saxo. Sumtibus Auctoris Impressum et Bibliopolio Sanderiano Commissum, Berolini, 584 pp. [in Latin]","Bigelow, H. B. & Schroeder, W. C. (1953) The Fishes of the Western North Atlantic, Part II. Sawfishes, skates, rays and chimaeroids. Memoirs of the Sears Foundation for Marine Research, 2, 1 - 588.","Puyo, J. (1936) Contribution a l'etude ichthyologique de la Guyane francaise. Peches et pecheries. Bulletin de la Societe d'Histoire Naturelle de Toulouse, 70, 5 - 258.","Muller, J. & Henle, F. G. J. (1841) Systematische Beschreibung der Plagiostomen. Veit und Comp., Berlin, 200 pp.","Dumeril, A. H. A. (1865) Histoire naturelle des poissons ou ichthyologie generale. Tome Premier. I. Elasmobranches. Plagiostomes et Holocephales ou Chimeres, 1, 1 - 720 + pp. 1 - 8 (Atlas).","Gunther, A. (1870) Catalogue of the fishes in the British Museum. Volume Eight. Trustees of the British Museum, London, 549 pp.","Metzelaar, J. (1919) Report on the fishes, collected by Dr. J. Boeke in the Dutch West Indies 1904 - 1905, with comparative notes on marine fishes of tropical West Africa. F. J. Belanfante, ' s-Gravenhage, 314 pp.","Meek, S. E. & Hildebrand, S. F. (1923) The marine fishes of Panama. Part I. Field Museum of Natural History Publication Zoological Series, 15, 1 - 330.","Nishida, K. (1990) Phylogeny of the suborder Myliobatidoidei. Memoirs of the Faculty of Fisheries Hokkaido University, 37 (1 / 2), 1 - 108.","Lovejoy, N. R. (1996) Systematics of myliobatoid elasmobranchs: with emphasis on the phylogeny and historical biogeography of neotropical freshwater stingrays (Potamotrygonidae: Rajiformes). Zoological Journal of the Linnaen Society, 117, 207 - 257. https: // doi. org / 10.1006 / zjls. 1996.0038","Mazzoleni, R. C. & Schwingel, P. R. (1999) Elasmobranch species landed in Itajai harbor, southern Brazil. Notas Tecnicas Facimar, 3, 111 - 118.","Menni, R. C. & Stehmann, F. W. (2000) Distribution, environment and biology of Batoids fishes off Argentina, Uruguay and Brazil. A review. Revista del Museo Argentino de Ciencias Naturales, 2 (1), 69 - 109. https: // doi. org / 10.22179 / revmacn. 2.126","Furtado Jr., I., Tavares, M. C. da S. & Brito, C. S. F. de (2003) Avaliacao do potencial de producao de peixes, com rede-de-arrasto de parelha, na plataforma continental da regiao norte do Brasil (area de pesca do camarao-rosa). Boletim Tecnico- Cientifico do CEPNOR, 3 (1), 135 - 146.","Carvalho, M. R. de, Maisey, J. G. & Grande, L. (2004) Freshwater stingrays of the Green River Formation of Wyoming (Early Eocene), with the description of a new genus and species and an analysis of its phylogenetic relationships (Chondrichthyes: Myliobatiformes). Bulletin of the American Museum of Natural History, 284, 1 - 136. https: // doi. org / 10.1206 / 0003 - 0090 (2004) 284 2.0. CO; 2","Meneses, T. S., Santos, F. N. & Pereira, C. W. (2005) Fauna de elasmobranquios do litoral do estado de Sergipe, Brasil. Arquivos de Ciencias do Mar, 38, 79 - 93.","Nunes, J. L. S., Almeida, Z. S. de & Piorski, N. M. (2005) Rays captured by the artisanal fisheries in shallow waters of Maranhao State, Brazil. Arquivos de Ciencias do Mar, 38, 49 - 54.","Yokota, L. & Lessa, R. P. (2006) A nursery area for sharks and rays in Northeastern Brazil. Environmental Biology of Fishes, 75 (3), 349 - 360. https: // doi. org / 10.1007 / s 10641 - 006 - 0038 - 9","Yokota, L. & Lessa, R. P. (2007) Reproductive biology of three ray species: Gymnura micrura (Bloch & Schneider, 1801), Dasyatis guttata (Bloch & Schneider, 1801) and Dasyatis marianae Gomes, Rosa & Gadig, 2000, caught by artisanal fisheries in Northeastern Brazil. Cahiers de Biologie Marine, 48, 249 - 257.","Basilio, T. H., Faria, V. V. & Furtado-Neto, M. A. A. (2008) Elasmobranch fauna of the Curu river estuary, Ceara State, Brazil. Arquivos de Ciencias do Mar, 41 (2), 65 - 72.","Lessa, R. P., Barreto, R. R., Quaggio, A. L. C., Valenca, L. R., Santana, F., Yokota, L. & Gianeti, M. D. (2008) Survey of elasmobranch species caught by fishing gears that operate on the nursery ground of Caicara do Norte, Rio Grande do Norte State. Arquivos de Ciencias do Mar, 41 (2), 58 - 64.","Basilio, T. H., Godinho, W. O., Araujo, M. E. de, Furtado-Neto, M. A. de A. & Faria, V. V. (2009) Ichthyofauna of the Curu River estuary, Ceara State, Brazil. Arquivos de Ciencias do Mar, 42 (2), 81 - 88.","Bornatowski, H., Abilhoa, V. & Charvet-Almeida, P. (2009) Elasmobranchs of the Parana Coast, southern Brazil, south-western Atlantic. Marine Biodiversity Records, 2, 1 - 6. https: // doi. org / 10.1017 / s 1755267209990868","Nunes, J. L. S. & Piorski, N. M. (2009) A dorsal fold in Gymnura micrura (Bloch and Schneider, 1801) (Chondrichthyes: Gymnuridae). Brazilian Archives of Biology and Technology, 52 (2), 479 - 482. https: // doi. org / 10.1590 / S 1516 - 89132009000200027","Reis, M., Grande, H., Macedo, M. M. & Batista, V. da S. (2012) Albinism in the smooth butterfly ray Gymnura micrura (Elasmobranchii, Gymnuridae): first record and morphometric comparisons. Cybium, 37 (3), 217 - 219.","Yokota, L., Goitein, R., Gianeti, M. D. & Lessa, R. T. P. (2012) Reproductive biology of the Smooth Butterfly Ray Gymnura micrura. Journal of Fish Biology, 81 (4), 1315 - 1326. https: // doi. org / 10.1111 / j. 1095 - 8649.2012.03413. x","Ragno, M. P. (2013) Distribuicao e morfologia dos canais da linha lateral em raias e sua relevancia sistematica (Chondrichthyes: Elasmobranchii). Master's Thesis. Universidade de Sao Paulo, Sao Paulo, 184 pp. https: // doi. org / 10.11606 / D. 41.2013. tde- 31032014 - 114920","Yokota, L., Goitein, R., Gianeti, M. D. & Lessa, R. T. P. (2013) Diet and feeding strategy of the Smooth Butterfly Ray Gymnura micrura in Northeastern Brazil. Journal of Applied Ichthyology, 29 (6), 1 - 5. https: // doi. org / doi: 10.1111 / jai. 12213","Fontenelle, J. P. & Carvalho, M. R. de (2015) Systematic implications of brain morphology in potamotrygonidae (Chondrichthyes: Myliobatiformes). Journal of Morphology, 277 (2), 252 - 263. https: // doi. org / 10.1002 / jmor. 20493","Garcia Jr. J., Nobrega, M. F. & Oliveira, J. E. L. (2015) Coastal fishes of Rio Grande do Norte, northeastern Brazil, with new records. Check List, 11 (3), 1 - 24. https: // dx. doi. org / 10.15560 / 11.3.1659","Willems, T., Depestele, J., Backer, A. de & Hostens, K. (2016) Ray bycatch in a tropical shrimp fishery: Do Bycatch Reduction Devices and Turtle Excluder Devices effectively exclude rays? Fisheries Research, 175, 35 - 42. https: // doi. org / 10.1016 / j. fishres. 2015.11.009","McEachran, J. D. & Carvalho, M. R. de (2002) Gymnuridae: Butterfly Rays. In: Carpenter, K. E. (Ed.), The Living Marine Resources of the Western Central Atlantic. Volume 1: Introduction, Mollusks, Crustaceans, Hagfishes, Sharks, Batoid fishes and Chimaeras. FAO, Rome, pp. 575 - 577.","Lesueur, C. A. (1817) Description of three new species of the genus Raja. Journal of the Academy of Natural Sciences, 1 (3), 41 - 45.","Shaw, G. (1804) General zoology or systematic natural history. Vol. 5. Part 2. G. Kearsley, London, vi + 213 pp. [pp. vi + 251 - 463]","Cantor, T. E. (1849) Catalogue of Malayan fishes. Journal of the Asiatic Society of Bengal, 18 (2), 983 - 1443.","Blyth, E. (1860) The cartilaginous fishes of lower Bengal. Journal of the Asiatic Society of Bengal, 29 (1), 35 - 45.","Day, F. (1865) The fishes of Malabar. Bernard Quaritch, London, 293 pp.","Day, F. (1878) The fishes of India; being a natural history of the fishes known to inhabit the seas and fresh waters of India, Burma, and Ceylon. Part 4. B. Quaritch, London, 227 pp. [pp. 553 - 779] https: // doi. org / 10.5962 / bhl. title. 55567","Day, F. (1889) Fishes. In: Blanford, W. T. (Ed.), The fauna of British India including Ceylon and Burma. Vol. 1. Taylor & Francis, London, pp. 1 - 548.","Wood-Mason, J. & Alcock, A. (1891) On the uterine villiform papillae of Pteroplatea micrura and their relation to their embryo. Proceedings of the Royal Society of London, 49, 359 - 367. https: // doi. org / 10.1098 / rspl. 1890.0103","Alcock, A. (1892) Some observations on the embryonic history of Pteroplatea micrura. The Annals and Magazine of Natural History, 55 (6), 1 - 8.","Annandale, N. (1909) Report on the fishes taken by the Bengal fisheries steamer \" Golden Crown. \" Part I, Batoidei. Memoirs of the Indian Museum, 2 (1), 1 - 58. https: // doi. org / 10.5962 / bhl. part. 29058","Pillay, R. S. N. (1929) A list of fishes taken in Travancore from 1901 - 1915. The Journal of the Bombay Natural History Society, 33, 347 - 379.","Randall, J. E. & Lim, K. K. P. (2000) A checklist of the fishes of the South China Sea. Raffles Bulletin of Zoology, 8 (Supplement), 569 - 667.","Jacobsen, I. P. & Bennett, M. B. (2009) A Taxonomic Review of the Australian Butterfly Ray Gymnura australis (Ramsay & Ogilby, 1886) and Other Members of the family Gymnuridae (Order Rajiformes) from the Indo-West Pacific. Zootaxa, 2228, 1 - 28.","Fowler, H. W. (1941) Contributions to the biology of the Philippine archipelago and adjacent regions. The fishes of the groups Elasmobranchii, Holocephali, Isospondyli, and Ostariophysi obtained by the United States Bureau of fisheries steamer \" Albatross \" in 1907 to 1910, chiefly in the Philippine Islands and adjacent seas. Bulletin of the United States National Museum, 13 (100), 1 - 879.","Talwar, P. K. & Kacker, R. K. (1984) Commercial sea fishes of India. Zoological Survey of India, Calcutta, 997 pp.","Raje, S. G. (2003) Some aspects of biology of four species of rays off Mumbai water. Indian Journal of Fisheries, 50 (1), 89 - 96.","Raje, S. G., Sivakami, S., Mohan, R. G., Kumar, P. P. M., Raju, A. A. & Joshi, K. K. (2007) An Atlas on the Elasmobranch fishery resources of India. CMFRI Special Publication. No 95. Central Marine Fisheries Research Institute, Kochi, 253 pp.","Mejia-Falla, P. A., Navia, A. F., Mejia-Ladino, L. M., Acero, A. P. & Rubio, E. A. (2007) Tiburones y rayas de Colombia (Pisces, Elasmobranchii): lista actualizada, revisada y comentada. Boletin de Investigaciones Marinas y Costeras, 36, 111 - 149.","Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordinus, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Impensis Direct. Laurentii Salvii, Holmiae, 824 pp.","Seret, B. & McEachran, J. D. (1986) Catalogue critique des types de poissons du Museum national d'Histoire naturelle. (Suite) Poissons batoides (Chondrichthyes, Elasmobranchii, Batoidea). Bulletin du Museum National d'Histoire Naturelle, 8 (4), 3 - 50.","Eschmeyer, W. N., Fricke, R. & Lann, R. van der (2017) Catalog of Fishes: Genera, Species, References. Available from: http: / / researcharchive. calacademy. org / research / ichthyology / catalog / fishcatmain. asp (accessed 16 May 2017)"]}

Summary The purpose of the present study was to analyze the diet of the smooth butterfly ray Gymnura micrura using qualitative and quantitative approaches to describe the feeding spectrum as well as ecological aspects related to feeding and niche width. The rays were obtained through monthly sampling as by-catch from bottom trawl fisheries in northeastern Brazil from August 2007 to July 2008. A total of 286 stomachs were sampled, of which 176 contained food items. G. micrura is a predator in the region that feeds intermittently on large whole prey items, followed by a long period of digestion with simply little or no feeding activity. A low diversity of food items was found in the G. micrura diet, with an absolute predominance of teleosts, especially the roughneck grunt Pomadasys corvinaeformis. It is suggested that the species has a narrow feeding niche and a high degree of specialization. This presumed high degree of feeding specialization is discussed and the findings are compared in light of similar studies for closely related species, allowing to propose the family as primarily constituting piscivorous rays.

This study provides the first detailed information on the reproductive biology of the smooth butterfly ray Gymnura micrura. A total of 905 individuals were sampled, 377 of which were used for the reproductive study. Juveniles accounted for 75% of the sample, but all life cycle stages were present in the study area. The disc width at which 50% were mature (W(D50))was estimated at 269 and 405 mm for males and females, respectively. The W(D50V) (based on the onset of vitellogenesis) was estimated at 359 mm. Uterine fecundity (mean ±s.d. = 3·8 ± 1·3; range: 1-6) was positively correlated with female size. A 3564% gain in mean wet mass was observed from egg to full-term embryo in utero. Size at birth ranged from 135 to 175 mm W(D) (19·5 to 55·0 g), with a mean of 165·1 mm W(D) (43·3 g). The embryo sex ratio was not significantly different from 1:1. The ovaries of pregnant females were undergoing vitellogenesis during gestation, with females ready to ovulate soon after parturition. Gymnura micrura may have an asynchronous reproductive cycle, with females reproducing continuously throughout the year.

In order to know the morphological organization of the digestive system of the smooth butterfly ray Gymnura micrura, specimens were collected with a trawl net in coastal lagoons and littoral of the Gulf of Mexico. Samples were fixed in formaldehyde and preserved in ethylic alcohol. In the laboratory, the anatomic analysis of the digestive tract components and its glands, together with the comparison with representative species of the Rhinobatidae, Rajidae, Urotrygonidae, and Dasyatidae families, allowed for the recognition that the general organization of the digestive system of G. micrura fits to the general morphological pattern of Batoidea. However, some significant differences were recognized between this species and the remaining rays, such as the slender nature of its jaws, the reduced volume of the mandible musculature, and the welldefined development of two anterior hepatic lobes separated from each other. It is outstanding the number of two posterior hepatic lobes as a shared morphological character with other Myliobatoidei. This species shows sexual dental dimorphism, consisting in a greater size of the dental cuspid in each tooth of males

This study explores the dichotomy between undulatory (passing multiple waves down the fin or body) and oscillatory (flapping) locomotion by comparing the kinematics of pectoral fin locomotion in eight species of batoids (Dasyatis americana, D. sabina, D. say, D. violacea, Gymnura micrura, Raja eglanteria, Rhinobatos lentiginosus and Rhinoptera bonasus) that differ in their swimming behavior, phylogenetic position and lifestyle. The goals of this study are to describe and compare the pectoral fin locomotor behavior of the eight batoid species, to clarify how fin movements change with swimming speed for each species and to analyze critically the undulation/oscillation continuum proposed by Breder using batoids as an example. Kinematic data were recorded for each species over a range of swimming velocities (1–3 disc lengths s(−1)). The eight species in this study vary greatly in their swimming modes. Rhinobatos lentiginosus uses a combination of axial-based and pectoral-fin-based undulation to move forward through the water, with primary thrust generated by the tail. The pectoral fins are activated in short undulatory bursts for increasing swimming speed and for maneuvering. Raja eglanteria uses a combination of pectoral and pelvic locomotion, although only pectoral locomotion is analyzed here. The other six species use pectoral locomotion exclusively to propel themselves through the water. Dasyatis sabina and D. say have the most undulatory fins with an average of 1.3 waves per fin length, whereas Rhinoptera bonasus has the most oscillatory fin behavior with 0.4 waves per fin length. The remaining species range between these two extremes in the degree of undulation present on their fins. There is an apparent trade-off between fin-beat frequency and amplitude. Rhinoptera bonasus has the lowest frequency and the highest fin amplitude, whereas Rhinobatos lentiginosus has the highest frequency and the lowest amplitude among the eight species examined. The kinematic variables that batoids modify to change swimming velocity vary among different species. Rhinobatos lentiginosus increases its tail-beat frequency to increase swimming speed. In contrast, the four Dasyatis species increase swimming speed by increasing frequency and wavespeed, although D. americana also changes wave number. Raja eglanteria modifies its swimming velocity by changing wavespeed and wave number. Rhinoptera bonasus increases wavespeed, Gymnura micrura decreases wave number, and both Rhinoptera bonasus and Gymnura micrura increase fin-tip velocity to increase swimming velocity. Batoid species fall onto a continuum between undulation and oscillation on the basis of the number of waves present on the fins.

To clarify the taxonomic status of Gymnura crebripunctata and Gymnura marmorata, the extent of morphological and nucleotide variation between these nominal species was examined using multivariate morphological and mitochondrial DNA comparisons of the same characters with congeneric species. Discriminant analysis of 21 morphometric variables from four species (G. crebripunctata, G. marmorata, Gymnura micrura and Gymnura poecilura) successfully distinguished species groupings. Classification success of eastern Pacific species improved further when specimens were grouped by species and sex. Discriminant analysis of size-corrected data generated species assignments that were consistently accurate in separating the two species (100% jackknifed assignment success). Nasal curtain length was identified as the character which contributed the most to discrimination of the two species. Sexual dimorphism was evident in several characters that have previously been relied upon to distinguish G. crebripunctata from G. marmorata. A previously unreported feature, the absence of a tail spine in G. crebripunctata, provides an improved method of field identification between these species. Phylogenetic and genetic distance analyses based on 698 base pairs of the mitochondrial cytochrome b gene indicate that G. crebripunctata and G. marmorata form highly divergent lineages, supporting their validity as distinct species. The closely related batoid Aetoplatea zonura clustered within the Gymnura clade, indicating that it may not represent a valid genus. Strong population structuring (overall Phi(ST) = 0.81, P < 0.01) was evident between G. marmorata from the Pacific coast of the Baja California peninsula and the Gulf of California, supporting the designation of distinct management units in these regions.

This paper reports a dorsal fold which is a membranous structure located on the tail of two juvenile butterfly rays, Gymnura micrura (Bloch & Scheneider, 1801), caught through artisanal fishery in the shallow waters of Maranhão State (Brazil).Neste manuscrito registra-se uma nadadeira dorsal em dois espécimes juvenis de Gymnura micrura (Bloch and Scheneider, 1801) capturadas pela pesca artesanal em águas rasas do estado do Maranhão (Brasil).

Sampling two Onslow Bay sites bi-weekly from 1975–2010 using semi-balloon otter trawls 950 times collected two species of butterfly rays Gymnura altevala and Gymnura micrura: 37 were G. altevala and 244 were G. micrura. All but one male G. altevala were collected at the inshore site. Most specimens of both species were less than 1,000 mm disc width (DW). Most specimens were collected in April and October. Both species remain infrequent visitors of North Carolinian waters.