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Journal of The Malacological Society of London Molluscan Studies Journal of Molluscan Studies (2017) 83: 384–398. doi:10.1093/mollus/eyx029 Advance Access publication date: 17 July 2017 Featured Article One for each ocean: revision of the Bursa granularis (Röding, 1798) species complex (Gastropoda: Tonnoidea: Bursidae) Downloaded from https://academic.oup.com/mollus/article-abstract/83/4/384/3977763 by IFREMER user on 25 January 2019 Malcolm T. Sanders1,2, Didier Merle1, Philippe Bouchet2, Magalie Castelin2, Alan G. Beu3, Sarah Samadi2 and Nicolas Puillandre2 1Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements CR2P – UMR7207 – CNRS, MNHN, UPMC, Muséum national d’Histoire naturelle, Sorbonne Universités, 8 rue Buffon, CP 38, 75005 Paris, France; 2Institut de Systématique, Évolution, Biodiversité ISYEB – UMR 7205 – CNRS, MNHN, UPMC, EPHE, Muséum national d’Histoire naturelle, Sorbonne Universités, 57 rue Cuvier, CP26, F-75005 Paris, France; and 3GNS Science, PO Box 30-368, Lower Hutt 5040, New Zealand Correspondence: N. Puillandre; e-mail: [email protected] (Received 20 March 2017; editorial decision 12 June 2017) ABSTRACT Bursa granularis (Röding, 1798) is a tonnoidean gastropod that is regarded as broadly distributed throughout the Indo-Pacific and tropical western Atlantic. Because of its variable shell it has received no less than thir- teen names, now all synonymized under the name B. granularis. We sequenced a fragment of the cox1 gene for 82 specimens covering a large part of its distribution and most type localities. Two delimitation meth- ods were applied, one based on genetic distance (ABGD) and one based on phylogenetic trees (GMYC). All analyses suggest that specimens identified as B. granularis comprise four distinct species: one limited to the tropical western Atlantic, another to southwestern Western Australia and two in the Indo-Pacific (from the Red Sea to the open Pacific) that are partly sympatric—but not syntopic—in Japan, the Philippines, Vanuatu and New Caledonia. Based on comparison of shell characters, we applied the following available names to the four species, respectively: B. cubaniana (d’Orbigny, 1841), B. elisabettae Nappo, Pellegrini & Bonomolo, 2014, B. granularis s. s. and B. affinis Broderip, 1833. We provide new standardized concho- logical descriptions for each of them. Our results demonstrate that a long planktotrophic larval stage, com- mon among Tonnoidea, does not necessarily ensure a circumtropical species distribution. INTRODUCTION Scheltema & Eyster, 1984), resulting in a cosmopolitan distribu- Tonnoideans are a rather small superfamily of Caenogastropoda tion. Scheltema (1971) also kept larvae that had been collected in (about 357 species, WoRMS, 2017) related to the neogastropods, the plankton alive in an aquarium, and found that some taxa lived either as its sister group (Zou, Li & Kong, 2011) or belonging as planktonic veliger larvae for several months or more (e.g. within Neogastropoda (Hayashi, 2005; Colgan et al., 2007; Cunha, Monoplex nicobaricus lived for 390 d in captivity). Grande & Zardoya, 2009; Williams, Foster & Littlewood, 2014; As in most other marine gastropods, tonnoidean species were Osca, Templado & Zardoya, 2015). Notwithstanding the non- first described based on features of the teleoconch, using a limited planktotrophic development of a few Australian species, one of the number of specimens and characters. The available material of characteristic features of tonnoidean gastropods is their long to many species of Bursidae described before 1960 rarely exceeded extremely long planktonic larval stages, termed teleplanic larvae three specimens. Because of this limited evaluation of the intraspe- (derived from the Greek tele, distant and planos, wandering; cific variability, numerous new species were described for every Scheltema, 1971). The record has been observed for a larva of newly recognized morphological form. When additional material Fusitriton oregonensis (Ranellidae), which lived in an aquarium for became available, malacologists realized that they might have 4.5 years without metamorphosing (Strathmann & Strathmann, greatly underestimated the intraspecific shell variability, since sup- 2007). An indirect estimation of the duration of larval life was also posedly geographically restricted species were actually morpho- proposed by Scheltema (1972) who, based on the extent of the dis- logically highly similar to other nominal species from other tribution area and the speed of ocean currents, inferred the time it localities, to the extent that they shared identical protoconchs. would take for the larvae to cross ocean basins—generally several This was the first step towards an important synonymization trend months. Conversely, and in quite circular reasoning, the duration in tonnoidean systematics. Also, taking into account the expected of this larval time led to the hypothesis that some species may great dispersal abilities, modern authors (e.g. Beu, 1998; Nappo, have trans-oceanic dispersal capabilities (e.g. Scheltema, 1966, Pellegrini & Bonomolo, 2014) followed the lead of Scheltema to 1968, 1971, 1972, 1986a, b, 1988; Laursen, 1981; Pechenik, the point where some very well-defined morphs were ranked as no © The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: [email protected] BURSA GRANULARIS COMPLEX more than subspecies. They thus recognized a smaller number of of the B. granularis complex. Our goal was to clarify species delimi- species, but with trans-oceanic distributions. tation within the B. granularis complex and to test the hypothesis Among the Tonnoidea, the family Bursidae includes 54 Recent that this supposed species has a world-wide geographical species (WoRMS, 2017), among which several are potentially spe- distribution. cies complexes, i.e. species for which alternative hypotheses of The specimens were first separated tentatively into morphospe- delimitation have been proposed in the literature. In particular, cies based on shell characters. In a second step, all the specimens the Bursa granularis complex, already identified as such by Castelin were sequenced (cytochrome c oxidase subunit I gene) to test et al. (2012), is typically recognized as a single species by modern whether the recognized morphogroups corresponded to distinct authors (Beu, 1998, 2005, 2010), although sometimes with subspe- molecular clusters. Finally, we assigned available names to the dif- cies (Nappo et al., 2014). According to both the literature and the ferent genetic and morphological groups identified within the GBIF (2016) database (Fig. 1), B. granularis has a subtropical and complex and considered the implication in terms of their geo- fi tropical distribution throughout the Indo-West Paci c, the eastern graphical distributions. Downloaded from https://academic.oup.com/mollus/article-abstract/83/4/384/3977763 by IFREMER user on 25 January 2019 Pacific and the tropical western Atlantic. [In the eastern Atlantic, it has only been recorded from the Cape Verde Islands (Garcia- Talavera, 1983, cited by Beu, 1998), but this record was not con- firmed by Rolán (2005).] This distribution would make it one of MATERIAL AND METHODS the most widespread species among the Tonnoidea. However, this apparently cosmopolitan species has received no fewer than ten Sampling names (Beu, 1998). WoRMS (2017) lists 13 synonyms of Tritonium The material for this study was collected from various localities granulare Röding, 1798: Tritonium jabick Roding, 1798, Biplex rubicola during a series of shallow-water and deep-sea expeditions to Saudi Perry, 1811, Ranella granifera Lamarck, 1816, Ranella affinis Arabia (University of Florida UF 2013), Vietnam (NT 2014), Broderip, 1833, Ranella cubaniana d’Orbigny, 1841, Ranella livida Vanuatu (UF 2005, Santo Marine biodiversity survey 2006), Reeve, 1844, Bursa cumingiana Dunker, 1862, Bursa alfredensis Mozambique (MAINBAZA 2009, INHACA 2011), Madagascar Turton, 1932, Bursa kowiensis Turton, 1932, Bursa cubaniana inter- (UF 2008), the Philippines (PANGLAO 2004, UF 2015), Mariana media Nowell-Usticke, 1959, Bursa corrugata lineata Nowell-Usticke, Islands (UF 2008), Micronesia (UF 2008), Okinawa, Japan (UF 1959 and Bursa granularis elisabettae Nappo et al. 2014. The numer- 2010), Guam (UF 2010), Marquesas Islands (Pakaihi I Te Moana ous alternative species hypotheses led to various usages of these 2012), Papua New Guinea (PAPUA NIUGINI 2012), Marshall names in the literature; whereas 19th century authors (e.g. Reeve, Islands (UF 2008), New Caledonia (TERRASSES 2008, UF 1844b) recognized up to four different species, the latest revision 2013), Taiwan (UF 2005), Florida, USA (UF 2010), Guadeloupe proposed to group them all under the name B. granularis (Röding, (KARUBENTHOS 2012) and Western Australia (UF 2009, 1798)(Beu, 1998). Two of these names, however have been accepted WESTERN AUSTRALIA 2011). MNHN specimens collected by Nappo et al. (2014) at the rank of subspecies—B. granularis cubaniana before 2012 were anaesthetized with an isotonic solution of — and B. granularis elisabettae in addition to the nominotypical subspecies MgCl2 and fixed in 96% ethanol. Specimens collected after 2012 B. granularis granularis. were processed with a microwave oven (Galindo et al., 2014); the Using several molecular markers, Castelin et al. (2012) identified living molluscs in small volumes of sea water were exposed to two morphologically distinct