Contributions to Zoology, 86 (2) – 2017Gerrit Potkamp; Mark J.A. Vermeij; Bert W. Hoeksema: Genetic and morphological variation in corallivorous snails (Coralliophila spp.) living on different host corals at Curaçao, southern Caribbean

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Shallow tropical coral reefs are known as the world’s most diverse marine ecosystems, with estimates of global species numbers ranging to over one million, constituting a large portion of marine species (Reaka-Kudla, 1997; Plaisance et al., 2011; Appeltans et al., 2012; Fisher et al., 2015). Many coral-associated species depend on their host for food, shelter or recruitment (Scott, 1987; Stella et al., 2010, 2011; Hoeksema et al., 2012, 2017). Currently, 51 invertebrates are known that feed on live scleractinian corals, of which 17 are obligate corallivores (Rotjan and Lewis 2008), while many other species prey on coral species other than scleractinians (Schiaparelli et al., 2005; Reijnen et al., 2010; Wolf et al., 2014; Sánchez et al., 2016). New cases of corallivory, involving new records of predator-prey combinations, are still being reported regularly (e.g., Berumen and Rotjan, 2010; Vermeij, 2010).

Snails belonging to the subfamily Coralliophilinae (Gastropoda: Muricidae), with 200-250 species described worldwide, are corallivores that feed on anthozoan host species (Oliverio and Mariottini, 2001a; Oliverio, 2008; Oliverio et al., 2009). Within this subfamily, species of the genus Coralliophila Adam and Adams, 1853 are common corallivores found on reefs in the Caribbean and Brazil, with C. galea (Dillwyn, 1823) and C. caribaea Abbott, 1958 as the most abundant species. These species associate with a wide range of anthozoan host species belonging to the hexacoral orders Scleractinia, Zoantharia or Coralliomorpharia, and/or the octocoral order Alcyonacea (Robertson, 1970; Miller, 1981; Dias and Gondim, 2016). Overlap in host species has been reported for C. galea and C. caribaea, involving hosts belonging to the Scleractinia, Zoantharia and Coralliomorpharia, but host partitioning has also been observed whereby C. caribaea only preyed on alcyonaceans (Robertson, 1970; Miller, 1981), whereas C. galea preferred scleractinians (Miller, 1981).

In the ecological literature, the most common Coralliophila species in the Caribbean, C. galea, has often been misidentified as C. abbreviata (Lamarck, 1816) (see Bouchet, 2015; Netchy et al., 2016). Coralliophila abbreviata is a junior synonym of C. erosa (Röding, 1798), a species exclusively known from the Indo-Pacific (Oliverio, 2008). Predation by Coralliophila galea can negatively impact coral communities (Baums et al., 2003a). Bruckner et al. (1997), for example, measured a mean tissue consumption per snail of 1.9 cm2 day-1, with a maximum of 6.5 cm2 day-1 on Acropora palmata (Lamarck, 1816). C. galea predation also prevented the recovery of Acropora cervicornis (Lamarck, 1816) populations from damage caused by a hurricane (Knowlton et al. 1988, 1990).

Host-specific differences in morphological and ecological traits may arise in both Coralliophila species, like host-related size structuring (Hayes, 1990a; Bruckner et al., 1997; Baums et al., 2003a; Johnston and Miller, 2006, Johnston et al., 2012) and timing of sex change in C. galea (Baums et al., 2003a; Johnston and Miller, 2006). Host-associated cryptic species also occur among coral-associated gastropods in the Indo-Pacific. Gittenberger and Gittenberger (2011) reported on an adaptive, host-associated radiation among endolithic snails of the genus Leptoconchus Rüppell, 1834 (Coralliophilinae), consisting of 14 cryptic species living inside the skeletons of 24 species of mushroom coral hosts (Scleractinia: Fungiidae). A similar adaptive radiation was found among 22 snails of the family Epitoniidae divided over 34 host coral species (Gittenberger and Gittenberger, 2005; Gittenberger and Hoeksema, 2013). In C. galea, only a weak genetic divergence existed between snails associated with the scleractinians Acropora palmata and Orbicella spp. (Johnston et al., 2012).

In the present study, host-specific differences in size, shell shape and allometric patterns as well as genetic differences in both C. galea and C. caribaea were found in response to living of different scleractinian and alcyonacean host species. To study shell morphology independent of shell size, landmark-based geometric morphometrics were used to model shell shape (see e.g., Stone, 1998; Carvajal-Rodríguez et al., 2005; Queiroga et al., 2011; Mariani et al., 2012; Burridge et al., 2015; Liew and Schilthuizen, 2016). Host-related size structuring has been observed for C. galea, and was consequently also expected for C. caribaea in addition to host-associated differences in shell shape and allometry.

Two mitochondrial markers (12S rRNA and cytochrome c oxidase subunit I) were used to assess intraspecific host-associated genetic divergence in C. galea and C. caribaea across the whole range of their host species at Curaçao, extending the results of Johnston et al. (2012). Based on Johnston et al. (2012), who found high gene flow across the Caribbean and weak host-associated divergence within C. galea, we expect genetic divergence among host species to be low or absent for both C. galea and C. caribaea. By combining morphological and genetic methods, additional information has been obtained regarding the evolutionary and ecological relations between corallivorous snails and their hosts. Lastly, a new species, C. curacaoensis Potkamp and Hoeksema sp. nov., was found and described (see Appendix).