Stramonita Brasiliensis (Gastropoda: Muricidae) Living As Inquiline on the Shell of Pugilina Tupiniquim (Gastropoda: Melongenidae)
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Bull Mar Sci. 92(3):371–376. 2016 note http://dx.doi.org/10.5343/bms.2016.1003 Stramonita brasiliensis (Gastropoda: Muricidae) living as inquiline on the shell of Pugilina tupiniquim (Gastropoda: Melongenidae) 1 Laboratório de Bentos Costeiro, Silvio Felipe B Lima 1 * Departamento de Biologia, 2 Centro de Ciências Biológicas e Vinícius Queiroz da Saúde, Universidade Federal Geraldo Semer P Oliveira 3 de Sergipe, São Cristóvão 49100- 4 000, Sergipe, Brazil. Martin Lindsey Christoffersen Carmen Regina P Guimarães 1 2 Departamento de Fisiologia Geral, Instituto de Biociências, Universidade de São Paulo, São Paulo 05508-900, Brazil. ABSTRACT.—We report the first documented association 3 AGF Largo da Lapinha, of the gastropods Stramonita brasiliensis Claremont and D. Liberdade, Salvador 40375-973, G. Reid, 2011 and Pugilina tupiniquim Abbate and Simone, Bahia, Brazil. 2015 based on specimens found in the intertidal zone off 4 Laboratório de Filogenia the state of Maranhão, northeastern Brazil. In total, 206 de Metazoa, Departamento specimens of P. tupiniquim were observed and 91 had S. de Sistemática e Ecologia, brasiliensis species on the dorsal surface of the shell. Three Universidade Federal da Paraíba, to six specimens were often found on the shell, which Castelo Branco, João Pessoa serves as a hard substrate for the occupation of the muricid. 58051-900, Paraíba, Brazil. An association was inferred due to the high frequency of * Corresponding author email: associated pairs, including the presence of S. brasiliensis <[email protected]>. spawns. It is also likely that P. tupiniquim plays a role in transporting S. brasiliensis from sandy plains to areas with favorable substrates and/or food sources. None of the shells exhibited perforations or injuries caused by S. brasiliensis. Pugilina tupiniquim was observed feeding on dead fish, while no feeding behavior of S. brasiliensis was observed in the region. Based on the evidence presented herein, the Date Submitted: 13 January, 2016. relationship between these gastropods is considered as a case Date Accepted: 1 June, 2016. of commensalism, more specifically inquilinism. Available Online: 17 June, 2016. Ecological interactions among mollusks occur under a number of harmonic and disharmonic interspecific relationships (Rios 2009). For example, fissurellids, nerit- ids, and littorinids are gastropods that usually live aggregated on or under rocks, mangrove roots, corals, and/or calcareous algae from the intertidal zone to shal- low waters (Rios 2009). The gastropods, Diodora patagonica (d’Orbigny, 1839), Fissurellidea megatrema (d’Orbigny, 1841), and Lottia abrolhosensis (Petuch, 1979), may be associated with bivalves and other gastropods from the intertidal zone to sub- tidal regions (Rios 2009). Members of the families Hipponicidae and Calyptraeidae, are among the marine gastropods found on shells of other mollusks: i.e., Hipponix grayanus Menke, 1853 and Crucibulum auricula (Gmelin, 1791) often live as epizoic species on Lobatus gallus (Linnaeus, 1758) and Tonna pennata (Mörch, 1853), re- spectively (Rios 2009). Bulletin of Marine Science 371 © 2016 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 372 Bulletin of Marine Science. Vol 92, No 3. 2016 Despite the high number of other cases of ecological interactions among marine mollusks, mainly involving predation or parasitic relationships (see Beesley et al. 1998, Mills et al. 2007, Redfern 2013), there is little information on the extent of these associations and their specific type (e.g., commensalism, inquilinism and pho- resis). Commensalism, as defined by Paracer and Ahmadjian (2000), is an association in which one organism benefits, where the other is neither harmed nor benefited. This concept also includes cases of phoresis and inquilinism, defined as relation- ships where the benefit is transport and shelter, respectively (Paracer and Ahmadjian 2000). Cases of inquilinism involving marine mollusks and other invertebrates are common in the literature. However, such cases are reported mostly from fossil re- cords, for which shells have been identified as “hosts” in the associations, presumably providing shelter to the inquilines (Fraaye and Jäger 1995a,b, Fraaije and Pennings 2006, Landman et al. 2014). Currently, there are no records of recent mollusks acting as inquilines in intrinsic relationships. The aim of the present study was to make the first report of Stramonita brasiliensis Claremont and D. G. Reid, 2011 (Fig. 1B) living as a possible inquiline on Pugilina tupiniquim Abbate and Simone, 2015 (Fig. 1A) off northeastern Brazil, and to com- ment on the probable implications of this ecological interaction. Material and Methods Associated pairs of S. brasiliensis and P. tupiniquim were found on 17 May, 2015, during low tide in the intertidal zone between Arraial Bay and Panaquatira Beach in the city of São Luís, state of Maranhão, northeastern Brazil. The following ecological descriptors common in studies addressing associations between invertebrates were calculated: prevalence of inquilinism (Pi = percentage of S. brasiliensis on P. tupin- iquim) and prevalence of spawns (Ps = percentage of S. brasiliensis spawn on P. tu- piniquim). A portion collected specimens are in the Coleção de Invertebrados Paulo Young, Universidade Federal da Paraíba, Brazil (UFPB MOLL 3622, 3623); Museu Nacional, Universidade do Rio de Janeiro, Brazil (MNRJ 34.778, 34.779); and Museu de Zoologia, Universidade de São Paulo, Brazil (MZSP 122216, 122217). Results The associated gastropods were found in the intertidal zone on predominantly muddy, sand bottoms. In all cases, specimens of S. brasiliensis were found on the dorsal surface of the shell of P. tupiniquim. In total, 206 P. tupiniquim individuals were found in a stretch of approximately 10 km between Arraial Bay and Panaquatira Beach. Among this total, 91 specimens of P. tupiniquim were found with S. brasilien- sis on the dorsal surface of the shell (Pi = 44.2%) and 22 had spawns of this muricid (Ps = 10.7%) (Fig. 1C). A total of 40 associated pairs of S. brasiliensis occurring on P. tupi- niquim [two with the presence of spawns of the muricid (Ps = 5%)] were haphazardly sampled. Pi on this date was 100%. Up to nine specimens of the muricid were associ- ated on the melongenid (Mean Burden ranged 0–9). However, three to six specimens of S. brasiliensis were usually found on each P. tupiniquim shell. Specimens of P. tupiniquim were observed feeding on dead fish within wooden corrals, which is a regional method of capturing fish. No feeding behavior was ob- served for S. brasiliensis. This species was also found on wood used for the construc- tion of the corrals and rocky aggregations in the region. Lima et al.: Stramonita associated with Pugilina 373 Figure 1. (A) Pugilina tupiniquim, length 153 mm; (B) Stramonita brasiliensis, length 29 mm. (C–D) Interaction between marine gastropods showing muricid S. brasiliensis (length: C = 32 mm; D = 29 mm) on dorsal side of shell of P. tupiniquim (length: C = 120 mm; D = 132 mm). Discussion Although both S. brasiliensis and P. tupiniquim are active predators of a variety of invertebrates (D’Asaro 1966, Matthews-Cascon et al. 1990), it is possible to catego- rize this relationship as a case of inquilinism. This assumption is based on: (1) the lack of injuries on the shells of P. tupiniquim; and (2) the preference for a hard substrate by the muricid. Muricids are among the main carnivorous gastropods that can to perforate the shells of other mollusks for feeding (Ponder 1998, Herbert et al. 2007). Thus, P. tupiniquim may be susceptible to the predation by the muricid. However, no predation activity or hole marks from S. brasiliensis were found on shells of the melongenid. This may be because certain muricids have rather specific eating habits, as in the case of Urosalpinx cinerea (Say, 1822), Vitularia salebrosa (King, 1832), and, likely, S. brasiliensis, which prefer to prey on oysters (D’Asaro 1966, Ponder 1998, Herbert et al. 2007, Rios 2009, Rossato et al. 2014). The muricid is often found on rocky substrates (Santos and Boehs 2011, Rossato et al. 2014), while the melongenid usually inhabits muddy, sand bottoms (Matthews- Cascon et al. 1990, 2003, Rios 2009, Abbate and Simone 2015). It seems likely in the study area that shells of living P. tupiniquim serve as a convenient hard substrate and provide a unique opportunity for the occupation of S. brasiliensis, directly benefit- ing the muricid for serving as a shelter and a site for spawns (Fig. 1C–D), possibly 374 Bulletin of Marine Science. Vol 92, No 3. 2016 increasing the chance of hatchling survival due to the movements of the melongenid. This was inferred based on the high frequency of associated pairs in the region. No direct observations were made to demonstrate transportation of the muricid on the melongenid to possibly favorable adjacent areas. However, it is likely that P. tu- piniquim plays such a role, suggesting a possible case of phoresis, in which specimens of S. brasiliensis are transported from sandy plains to areas with favorable hard sub- strates and/or food sources. Although some muricids live on soft bottoms (Radwin and D’Attilio 1976, Ponder 1998), the preference for hard substrates on other species is so strong that such species avoid crossing soft bottoms, even to find prey (Carriker 1955). Reports of commensalism (lato sensu) involving marine mollusks are relatively com- mon in the literature on both fossil and recent species. Among the records