The Bubble Snails (Gastropoda, Heterobranchia) of Mozambique: an Overlooked Biodiversity Hotspot
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Mar Biodiv DOI 10.1007/s12526-016-0500-7 ORIGINAL PAPER The bubble snails (Gastropoda, Heterobranchia) of Mozambique: an overlooked biodiversity hotspot Yara Tibiriçá1,2 & Manuel António E. Malaquias3 Received: 9 October 2015 /Revised: 14 March 2016 /Accepted: 17 April 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract This first account, dedicated to the shallow water Keywords Mollusca . Acteonoidea . Cephalaspidea . Sea marine heterobranch gastropods of Mozambique is presented slugs . Taxonomy . Biodiversity . Africa . Western Indian with a focus on the clades Acteonoidea and Cephalaspidea. Ocean Specimens were obtained as a result of sporadic sampling and two dedicated field campaigns between the years of 2012 and 2015, conducted along the northern and southern coasts of Introduction Mozambique. Specimens were collected by hand in the inter- tidal and subtidal reefs by snorkelling or SCUBA diving down The shallow water marine heterobranch gastropods (sea slugs to a depth of 33 m. Thirty-two species were found, of which and alikes) of the Western Indian Ocean (WIO), an area con- 22 are new records to Mozambique and five are new for the fined between the East African coast and the Saya de Malha, Western Indian Ocean. This account raises the total number of Nazareth, and Cargados Carajos banks of the Mascarene shallow water Acteonoidea and Cephalaspidea known in Plateau (Obura 2012), have received little attention when Mozambique to 39 species, which represents approximately compared to other parts of the Indo-West Pacific, and most 50 % of the Indian Ocean diversity and 83 % of the diversity accounts are relatively old with few recent contributions (e.g. of these molluscs found in the Red Sea. A gap in sampling von Martens 1879;Bergh1900;Eliot1904, 1905, 1906; was identified in the central swamp/mangrove bio-region of Barnard 1927; MacNae and Kalk 1958, 1962;Rudman Mozambique, and therefore, we suggest that future research 1972b; Gosliner 1987; Yonow and Hayward 1991; Branch efforts concentrate on or at least consider this region. et al. 2008;Goslineretal.2008, 2015; Malaquias and Reid 2008; Price et al. 2011; Yonow 2012; Carmona et al. 2014a; King and Fraser 2014). Mozambique has the third largest coastline among eastern African countries, stretching over 2,400 km across subtropical Communicated by V. Urgorri and tropical latitudes. Few works have reported the occur- rence of marine heterobranch gastropod species in the country * Manuel António E. Malaquias and no dedicated account is available. The latter are either [email protected] generalistic faunistic reports (Bergh 1900; MacNae and Kalk 1958, 1962), field guides covering broader geographical re- 1 A.C.C.M. Zavora Marine Lab, Zavora, Inharrime, Inhambane gions (Branch et al. 2008;Goslineretal.2008, 2015;King Province 1113, Mozambique and Fraser 2014), or systematic revisions of certain genera 2 Department of Biology, Faculty of Marine and Environmental (Malaquias and Reid 2008; Price et al. 2011; Carmona et al. Sciences, University of Cádiz, Poligono del Rio San Pedro s/n, Apdo. 40, 11510 Puerto Real, Cadiz, Spain 2014a). Gosliner et al. (2008), in their book about the shallow- 3 Phylogenetic Systematics and Evolution Research Group, Section of Taxonomy and Evolution, Department of Natural History, University water sea slugs (Heterobranchia in part) of the tropical and Museum of Bergen, University of Bergen, Bergen PB 7800, 5020, adjacent temperate areas of the Indo-West Pacific region Norway (IWP), have cited the occurrence of 1397 species, but of those Mar Biodiv only 16 were specifically reported to occur in Mozambique, This paper provides the first dedicated account on the ma- representing little more than 1 % of the known diversity of the rine heterobranchs clades Acteonoidea and Cephalaspidea of entire IWP. This low number of species is in sharp contrast to Mozambique, based on a review of the literature and newly the richness of marine life in IWP countries and the diversity collected material. These two groups are commonly designat- of ecosystems in Mozambique where three major bio-regions ed as bubble snails because of the presence of a rounded shell are recognized: (1) the subtropical submerged rocky reefs on with an involute or short spire in many genera; they occur the south between Ponta do Ouro on the border with South mostly in shallow coastal areas in soft substrates of mud, sand, Africa (26°51′S) and the Bazaruto archipelago (22°05′S), (2) and seagrass, but there are exceptions with some genera (e.g. the central mangrove/swamp region between Bazaruto and Philine, Scaphander) extending their bathymetric distribution Pebane (17°05′S), and (3) the tropical coral reefs in the north into the deep sea, as well as a single genus that is specialized in between Pebane and the Rovuma River on the border with intertidal and shallow subtidal rocky-shores (Smaragdinella) Tanzania (10°28′S) (Ministry for the Coordination of (Gosliner et al. 2008;Oskarsetal.2015). Environmental Affairs 1997; Pereira et al. 2014). Moreover, the Mozambique Channel is an extremely productive area due to a complex upwelling pattern and converging eddy dipoles Material and methods (Pereira et al. 2014; Ternon et al. 2014). This diversity of biota and high oceanic productivity contributes to an explanation of Specimens were collected as a result of sporadic sampling the recognized high marine biodiversity of the country report- along the coast of Mozambique (Fig. 1) during 4 years be- ed for some taxonomic groups; for example, Mozambique is tween 2012 and 2015 and during two dedicated field cam- known to have the second highest diversity of corals in the paigns: 23 Jan–03 Feb 2014 in Inhambane Province, southern entire Indo-Pacific (Obura 2012). Mozambique and 12–28 May 2015 around Pemba and Vamizi The marine heterobranch gastropods contain some of the Island, northern Mozambique. Specimens were collected by most spectacular and colourful gastropods of our seas, of snorkelling and SCUBA diving between the tidal zone and up which the nudibranchs are a prime example (Gosliner et al. to a depth of 33 m. Several subtropical and tropical habitats 2008, 2015). The aesthetic value of these animals makes them were surveyed including tidal and subtidal reefs, fringing coral one of the most appealing groups for recreational divers and reefs, submerged rocky reefs, seagrass, sand flats, and estuar- has triggered the development of a dedicated industry of sa- ies (Table 1). All specimens were collected by hand, measured faris and cruises (e.g. Nudibranch cruises in Indonesia [http:// (total length BTL^), and photographed. Specimens were fro- www.thearenui.com/VanessaKnutson2016Komodo.html]and zen in seawater overnight, defrosted, and transferred to 96 % the Nudibranch Safari in Norway at Gulen [http://www. ethanol. scubapixel.com/blog/20715-nudibranch-safari-2016]). The classification and nomenclature adopted in this work The systematics of heterobranch gastropods went through mostly follows the World Register of Marine Species dramatic rearrangements in recent years. The traditional clade (WoRMS Editorial Board 2015), but for higher ranks we Opisthobranchia, previously regarded as one of the three sub- adopted Schrödl (2014). Voucher specimens were deposited classes of Gastropoda (Kay et al. 1998; Burn and Thompson at the Department of Natural History of the University 1998), is now considered polyphyletic, and the relationships Museum of Bergen, Norway (ZMBN), and at the Zavora and composition of several of its previous lineages have suf- Marine Laboratory, A.C.C.M., Mozambique (YT). fered striking reorganisations (Jörger et al. 2010; Schrödl Duplicates of these collections are deposited at the Natural 2014;Oskarsetal.2015). The formal use of the name History Museum of Maputo, Mozambique (MHN). Opisthobranchia has been abandoned in recent works (e. g. Schrödl 2014;Caballeretal.2015); for example, the order Cephalaspidea (bubble snails), which previously included Results the acteonids (Acteon, Pupa), ringiculids (Ringicula), aplustrids (Hydatina, Micromelo), runcinids (Runcina), plus In total, 32 species were recorded during our surveys; four all other traditional cephalaspids (e.g. aglajids, bullids, species of Acteonoidea and 28 species of Cephalaspidea. diaphanids, haminoeids, etc.) (see Burn and Thompson Eight families were sampled, with Aglajidae being the most 1998), has been split into three independent lineages of equal diverse with 13 species, followed by Haminoeidae (seven rank, namely the Acteonoidea (now part of the so called species), Philinidae and Aplustridae (three species each), BLower Heterobranchs^), the Runcinacea, and the Bullidae and Gastropteridae (two species each), and Cephalaspidea (Mikkelsen 1996; Vonnemann et al. 2005; Acteonidae and Colpodaspididae (one each). Malaquias et al. 2009). The latter two clades are included in Twenty-two species are new records to Mozambique and a larger group termed Euopisthobranchia (Jörger et al. 2010; five of them are first cited in the Western Indian Ocean Schrödl 2014). (WIO). Mar Biodiv Fig. 1 Main collecting areas; for details of sampling sites, see Table 1 Taxonomic list Distribution: Occurs throughout the IWP; Papua New Class GASTROPODA Cuvier, 1797 Guinea (Gosliner et al. 2008), Australia (Rudman 1971; Subclass HETEROBRANCHIA Burmeister, 1837 Gosliner et al. 2008), and the Philippines (Gosliner et al. Clade ACTEONACEA d’Orbigny 1835 2008). WIO: Tanzania (Adams 1855), Mozambique