To refer to this article use this url: http://contributionstozoology.nl/vol85/nr03/a03


Contributions to Zoology, 85 (3) – 2016

Prey selection of corallivorous muricids at Koh Tao (Gulf of Thailand) four years after a major coral bleaching event

Michelangelo S. Moerland1, Chad M. Scott2, Bert W. Hoeksema3

1.  Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands. E-mail: angelo.moerland@gmail.nl

2.  New Heaven Reef Conservation Program, 48 Moo 2, Koh Tao, Suratthani 84360, Thailand

3.  Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands

Keywords: corallivory,Drupella,Morula,Muricidae,resource selection.

Abstract


Corallivorous Drupella (Muricidae) snails at Koh Tao are reported to have extended their range of prey species following a major coral bleaching event in 2010. Populations of their preferred Acropora prey had locally diminished in both size and abundance, and the snails had introduced free-living mushroom corals in their diet. Although the coral community largely recovered, the Drupella population grew and reached outbreak proportions. For this study, corallivorous muricids at Koh Tao were studied more intensively to examine their identities, distribution and prey choice four years after the bleaching event. Drupella rugosa was identified as the major outbreak species and occurred at densities > 3 m-2 in depth ranges of 2-5 and 5-8 m. The density of D. rugosa was related to the live coral cover, Acropora colony density, and depth. Resource selection ratios revealed that species of Acropora, Psammocora and Pavona corals were attacked more frequently than would be expected based on their availability. Strikingly, fungiid corals were now avoided as prey in the recovered coral community, despite them being part of the preferred diet directly after the bleaching. Although D. rugosa showed a clear prey preference, it appears to be plastic by changing with prey availability. The muricids Drupella margariticola and Morula spinosa occurred in much lower densities and were less often associated with corals. Snails of the opportunistic corallivore D. margariticola usually co-occurred in D. rugosa aggregations, although they also formed feeding aggregations by themselves. Whether M. spinosa generally associates with corals as a corallivore or a scavenger has yet to be determined. Molecular analyses did not reveal cryptic speciation among snails sampled from different coral hosts and also no geographic variation. The present study also showed that corallivory is more common among D. margariticola and M. spinosa than previously known.

Introduction


Coral reefs host a wide array of life forms. Next to providing substrate and shelter to invertebrates (Patton, 1994; Stella et al., 2011; Hoeksema et al., 2012a) and fish (Bos and Hoeksema, 2015, references herein), corals also serve as a food source for diverse opportunistic and obligate corallivores (Robertson, 1970; Glynn, 1990; Gittenberger and Hoeksema, 2013). Scleractinian coral-feeding lineages have evolved multiple times among the gastropod families Architectonicidae, Epitoniidae and Muricidae (Robertson, 1970; Glynn, 1990; Barco et al., 2010). The large family Muricidae Costa, 1776 encompasses the entirely corallivorous subfamily Coralliophilinae Chenu, 1858 (Oliverio and Mariottini 2001; Barco et al., 2010), the possibly opportunistic coral-feeding Morula spinosa (Adams and Adams, 1853) (Yokochi, 2004) and Ergalatax junionae Houart, 2008 (Saledhoust et al., 2011), and the genus Drupella Thiele, 1925, which also holds a number of corallivorous species (Claremont et al., 2011a). Although the genus Drupella represents only a fraction of all corallivorous species, they have a reputation for their ability to degrade coral reefs on a large scale (Turner, 1994).

On account of molecular analyses, at least four obligate corallivorous Drupella species are distinguished, i.e., D. cornus (Röding, 1798), D. eburnea (Küster, 1862), D. fragum (Blainville, 1832) and D. rugosa (Born, 1778), and one species complex that exhibits opportunistic corallivory, i.e., D. margariticola (Broderip, 1833) (Taylor, 1980; Johnson and Cumming, 1995; Claremont et al., 2011a). While most related muricids are scavengers and predators of other molluscs, the radula of obligate corallivorous Drupella is altered for feeding effectively on coral tissue (Fujioka, 1982). The opportunistic feeding by D. margariticola on the other hand, is suggested to happen after co-occurring D. rugosa snails have initiated feeding on a coral prey since their own feeding apparatus is less suited for that purpose (Morton and Blackmore, 2009; Claremont et al. 2011a).

Drupella snails predominantly occur in small aggregations that prey on the same coral colony at night, but retreat to the underside or between branches of the colony during the day (Boucher, 1986; Hoeksema et al., 2013). Such aggregations seem to occur because individual snails are attracted to conspecifics (Morton et al., 2002; Schoepf et al., 2010), and to compounds that are secreted by stressed or damaged corals (Morton et al., 2002, Kita et al., 2005). Furthermore, aggregations of different species combinations have also been reported (Cumming, 1999; Morton and Blackmore, 2009), although those species may show different reef habitat preferences based on wave exposure and depth (Turner, 1994; Cumming, 1999). Other than common feeding aggregations, some large accumulations of Drupella are thought to be closely related offspring resulting from massive reproduction events (Baird, 1999; Cumming, 1999, 2009). Recruits of the same cohorts usually form large feeding aggregations, in which individuals show a common history of settlement and growth (Johnson et al., 1993).

Destructive outbreaks of Drupella have been witnessed throughout the Indo-Pacific since the 1980s. These outbreaks (usually > 3 individuals m-2) can be compared to the extensively studied corallivorous sea star Acanthaster plancii (Linnaeus, 1758), which can cause severe damage when occurring in high densities (Glynn, 1990; Cumming, 2009; Scott et al., 2015). Such outbreaks occur frequently and cause secondary mortality by succeeding earlier stressful events on reefs (Antonius and Riegl, 1998). These events are either natural or human-induced and can be related to coral bleaching (Baird, 1999; Hoeksema et al., 2013), destructive fishing (McClanahan, 1994), deteriorating water quality (Plass-Johnson et al., 2015), diving tourism (Guzner et al., 2010), nutrient enrichment (Al-moghrabi, 1997), siltation (Moyer et al., 1982), and storm damage (Boucher, 1986; Ayling and Ayling, 1992). The Drupella species that have been reported to occur in elevated densities are D. fragum (Moyer et al., 1982; Fujioka and Yamazato, 1983), D. cornus (Ayling and Ayling, 1987; Antonius and Riegl, 1998; Turner, 1994) and D. rugosa (Moyer et al., 1982; Cumming, 1999). In his review, Cumming (1999) concluded that only populations of D. fragum and D. cornus have attained persistent, considerable densities in outbreak situations. Densities were found of up to 5.1 individuals m-2 for D. fragum in Japan (Fujioka and Yamazato, 1983) and 18.5 individuals m-2 in for D. cornus in West Australia (Ayling and Ayling, 1987).

Prey choices of Drupella spp. have been documented in numerous normal and outbreak populations. Prey selection is complex and affected by relative abundance of coral taxa (Morton and Blackmore, 2009), although strong preferences for certain prey taxa and coral growth forms have been observed (Schoepf et al., 2010; Al-Horani et al., 2011). Most of the assumptions on this subject do not take relative availability of coral taxa into account, with exception of some papers on D. cornus (Turner, 1994; Schoepf et al., 2010). Results from most studies revealed a strong preference for acroporids (Acropora spp., followed by Montipora spp.) and some pocilloporid and poritid genera (Moyer et al., 1982; Fujioka and Yamazato, 1983; Turner, 1994; Al-Moghrabi, 1997; McClanahan, 1997; Cumming, 2002; Morton and Blackmore, 2009; Schoepf et al., 2010; Al-Horani et al., 2011). Many other taxa are mostly witnessed to be less commonly attacked or wholly avoided. Preferences are thought to depend on coral protein content and morphological complexity, both of which are high in Acropora (Keesing, 1990). Prey selection was also seen to differ within D. cornus age groups, with juveniles preferring structurally complex prey species that provide shelter (Forde, 1992; McClanahan, 1997; Schoepf et al., 2010). In some areas, Drupella prey preference is reported to differ from the above cited reports, due to a different coral assemblage composition or a lack of Acropora prey. Drupella cornus has been reported to favour corals of other genera at the periphery of its distribution range, such as Porites in Kenya (McClanahan 1997), and Pocillopora and Porites in Hawaii (Robertson 1970). A study by Morton et al. (2002) found that D. rugosa snails still preferred Acropora spp. despite their low abundance in the reefs of Hong Kong, which are primarily dominated by massive corals. So although their diet varies according to the coral fauna composition, Drupella snails still maintain a dominant preference for Acropora. Prey shifts have also been documented after the preferred prey becomes less available. For instance following coral death by bleaching (Zuschin and Oliver, 2003; Hoeksema et al., 2013) or even as direct consequence of predation by Drupella itself (Forde, 1992; Shafir and Gur, 2008).

One of such prey shifts to less preferred stony corals was documented for Koh Tao (Gulf of Thailand) following a mass coral bleaching event in 2010, related to elevated sea surface temperatures (Hoeksema et al., 2013). The bleaching caused coral mortality throughout the Gulf of Thailand and adjacent areas, thereby locally decreasing diversity and abundance of various coral species (Yeemin et al., 2012). However, some coral species were more susceptible to bleaching than others (Hoeksema and Matthews, 2011; Guest et al., 2012), and some reefs at Koh Tao showed relatively fast recovery (Hoeksema et al., 2012b), whereas local bleaching could still be noticed (or perhaps again) in some corals in February 2011 (Hoeksema and Matthews, 2015). Furthermore, the reefs around Koh Tao are increasingly subjected to sediment run-off from deforestation and development, pollution from the growing settlement on the island, as well as pressure from fishing and tourism-related activities (Weterings, 2011). Acropora colonies were specifically affected by bleaching and were further degraded by feeding Drupella (Hoeksema et al., 2013), of which the po­pulation density doubled between 2009 and 2014 (unpublished data). Subsequently, Drupella aggregations started to form on less preferred prey, after the preferred prey species diminished. Peculiarly, many feeding aggregations moved to mushroom species (Fungiidae) co-occurring in large assemblages, which are usually avoided (Hoeksema et al., 2013). Fungiids were still being preyed upon by Drupella in 2013 (Kim, 2013).

The present study looks into the Drupella population at Koh Tao four years after the 2010 bleaching event. The population size and its distribution over sites and depths were measured for the muricids D. rugosa and D. margariticola, as well for the poorly studied Morula spinosa. Coral prey choice and microhabitat use were assessed to show ontogenetic and interspecific differences. Furthermore, molecular analyses were performed to investigate genetic differences of snails based on prey choice and geography. Seen in the light of the previous events that changed Koh Tao’s reef community, along with the role of Drupella therein, the Drupella prey choice and its plasticity and potential ecological impact are discussed.

Material and methods


Molecular species identifications

Drupella and Morula snails were sampled to verify their identification at (sub)species level in order to examine if there is any geographic or prey-related cryptic speciation. Care was taken to include diverse within-species morphologies, which were stored on a > 70% alcohol solution. All specimens were obtained from Chalok Baan Kao, except for some D. rugosa from Sairee Beach found on Fungia fungites (Linnaeus, 1758). Sequences of muricid species and outgroups based on analyses by Barco et al. (2010), Claremont et al. (2011a), for Drupella, and Claremont et al. (2013) for Morula were downloaded from the NCBI GenBank sequence database (http://www.ncbi.nlm.nih.gov/Genbank; Appendix I).

The extraction of DNA was performed with, and according to the manufacturer’s protocol of, the DNEasy Blood and Tissue Kit (QIAGEN, Venlo, The Netherlands). The mitochondrial genes cytochrome c oxidase subunit I (COI) and 12S rRNA (12S) were amplified through the use of primers previously designed to work on muricids (Table 1). The most rewarding reaction mix consisted of 1 µL 10-100× diluted DNA, 0.2 µM (1µL) of both the F and R primer, 2.5 µL dNTPs, 2.5 µL 10× NH4 reaction buffer (Bioline), 2 and 1.6 µM (1 and 0.8 µL) MgCl2 for COI and 12S respectively, 0.2 µL Q-solution (QIAGEN) and 1 unit (0.2 µL) Taq polymerase. To reach a total reaction mixture volume of 25 µL the appropriate amount of MQ H2 O was added. The optimal PCR procedure for COI consisted of 5 min of initial denaturation at 95°C and 65 cycles of 40 s at 94°C, 40 s at 54°C for annealing and 60 s at 72°C for primer extension, followed by a final extension of 5 min at 72°C. The 65 cycles for 12S consisted of 60 s 60°C and 50 s at 72°C. The PCRs ran on a MyCyclerTM Thermal Cycler (Bio-Rad). Sanger sequencing was performed by BaseClear (Leiden, The Netherlands).

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Table 1. Primers used for amplification of markers 12S and COI of all muricid snail species.

Sequences were assembled and edited with Geneious version 6.1.6 (Drummond et al., 2013). When indistinct peaks occurred in the forward and reverse sequences nucleotides were labelled as N. Sequences were aligned with the Geneious alignment function. The model of molecular evolution was selected for the dataset of both markers under Akaike’s Information Criterion with jModelTest version 0.1.1 (Posada, 2008). When substitution models were not available in the phylogenetic software package, one that was and had the lowest AIC was selected. Bayesian inference (BI) analyses were performed with MrBayes version 3.2.2 (Ronquist et al., 2012). Branches that showed less than 50% posterior probability (PP) in the consensus tree were collapsed. The calculated MrBayes PP support values were obtained after 5,000,000 generations were sampled every 1,000 generations and a burn-in proportion of 25% was discarded.

Field survey

The study area encompassed nine sites around Koh Tao (Fig. 1), including some sites previously surveyed by Hoeksema et al. (2013), which consisted mostly of reef flats and gradually declining slopes. Fieldwork was conducted April - June 2014 during daytime. A sufficient number of replicate measurements were required to study Drupella densities because of their possible clumped distributions (Cumming, 1999). A total of 31 belt quadrats of 1×10 m2 were laid out, covering an area of 310 m2. One to four quadrats were measured per depth range per site. A distinction was made between shallow (2-5 m depth, 18 total) and slightly deeper (5-8 m depth, 13 total) quadrats that were laid out haphazardly within areas with high hard coral abundance. Use of belt quadrats is recommended when densities of corals and coral-associated fauna are measured at different depths (e.g. Dai and Yang, 1995; Oigman-Pszczol and Creed, 2006; Gittenberger and Hoeksema, 2013).

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Fig. 1. Map of Koh Tao with transect sites at reef flats and slopes (numbers) and inspected outcrops and pinnacles (letters): 1) Had Sai Nuan, 2) Chalok Baan Kao, 3) Taa Chaa, 4) Aow Leuk, 5) Tanote, 6) Hin Wong Bay, 7) Mango Bay, 8) Twins, 9) Sairee, a) Shark Island, b) Hin Wong Pinnacle, c) White Rock, d) Chumphon Pinnacle, e) Southwest Pinnacle and f) Sail Rock. After Chansang et al. (1999) and Hoeksema et al. (2012).

The substrate composition within quadrats was estimated (m-2), and consisted of the categories sand, rubble (including dead coral), rock, anthropogenic trash, sponge, algae, soft coral, healthy hard coral, recently killed coral and bleached coral. Coral colonies were included if at least half of the colony cover fitted inside the quadrat. All scleractinian corals were considered potential prey for corallivores and were thus included. Since Cumming (1999) observed that Drupella snails tend to avoid small coral colonies (Ø < 10 cm), these were not taken into account except when preyed upon. For all corals the following data was recorded: identity at genus level, size as maximum diameter measured (cm) and growth form (B, branching/arborescent; Bu, bushy/caespitose; C, corymbose; D, digitate; E, encrusting; F, foliose; L, laminar; M, massive; R, solitary/ mushroom; S, submassive; T, tabular). For the names of coral genera identified during the present study, recent relevant taxonomic studies were used that were based on phylogenetic analyses (Wallace et al., 2007; Stefani et al., 2008; Gittenberger et al., 2011; Arrigoni et al., 2014; Huang et al., 2014).

For each muricid species, individuals were counted within each quadrat, depending on whether their prey coral was also mostly situated inside the quadrat (> 50%). Snail specimens could be identified in the field through characteristics described by Fujioka (1982) and supporting illustrations (e.g. Johnson and Cumming 1995). Inspection of the shell aperture was needed when shells were overgrown by crustose coralline algae. Snail size, based on shell length, was determined per size class as defined for D. cornus by Turner (1994) and Schoepf et al. (2010): juveniles (< 10 mm (recruits), 10-19 mm), adults (20-29 mm, > 29 mm). The size was measured for snails that could be sampled without causing damage to the coral and it was estimated for individuals that could not be caught.

Statistics

The density of muricids and its variation over depth was analysed through both Mann-Whitney-Wilcoxon tests and linear regression. The distribution of age groups over depth and substrates were compared through Chi-squared tests. Distribution over reefs in general for D. rugosa was investigated with linear regressions and generalized linear models. Median snail group sizes on coral colonies and among age groups were compared through Kruskall-Wallis tests and investigated further through Mann-Whitney-Wilcoxon tests. Statistical analyses were performed in RStudio (R Development Core Team 2010).

Prey preferences were assessed for D. rugosa through resource selection functions (Manly et al., 1993). This was done by estimating the selection ratio (ωi) for all potential prey genera and growth forms and the associated Bonferroni corrected 95 and 99% confidence interval with the formulas:

Formule.jpg

where o i is the proportion of occupied colonies of coral genus i among all occupied colonies of all genera, a i is the proportion of available colonies of coral genus i among all available colonies of all genera, Z a/2k is the critical value of a standard normal distribution upper tail area of ∝/2k, k is the total number of coral genera in the analysis and u + is the total number of coral colonies of all genera that are occupied. The confidence interval suggested that a prey was attacked less than expected from its relative availability when below 1 and more than expected from its relative availability when above 1. When the confidence interval encompassed 1, the prey species was not considered attacked significantly less or more than could be expected from its relative abundance. In addition to the resource selection of all D. rugosa, selection of juveniles and adults was calculated as well. The functions were applied according to Schoepf et al. (2002), although coral genera were taken into account, not species. All present scleractinian genera were included, as they were all considered potential prey species. This approach widens the resulting confidence intervals, making it less likely to find significant deviations from expected colony occupations. When availability of a coral genus was considered too low to be representative (< 7 colonies), such a genus was omitted from the analysis. Colonies of < 10 cm in diameter were also omitted from the analysis.

Since the analysis does not take D. rugosa group size into account, the mean group size per coral genus was compared with the results afterwards. Furthermore, when noting presence/absence (use/non-use) it can be difficult to demonstrate if the host coral is also used as prey (Boyce et al., 2002). This seems less problematic for Drupella snails, which feed and rest on the same colony, directly linking presence to use and justifying the use of this method.

Results


Species identifications

After optimizing PCR conditions, both primer pairs worked on all muricids. The product size was approximately 720 for COI and 540 for 12S, and ultimate sequence sizes used for analysis were respectively 701 and 569 resulting in a concatenated analysis of 1270 characters based on 69 taxa. The models that were chosen were HKY+I+G for COI and GTR+I+G for 12S. The individual trees showed clear grouping of species in both Drupella and Morula (PP > 95%), although COI was more useful in resolving relationships within Drupella and 12S was more useful in resolving relationships in Morula.

The analysis produced well-defined groups with the two markers (Fig. 2). All species from this study fell within clear groups with their conspecifics (PP = 100%). Morula appeared polyphyletic as is currently being addressed (Claremont et al., 2013), while the genus Drupella was well-defined. The D. margariticola samples were part of the ‘Continental’ clade of the species complex and, just as the coral eating specimens from Hong Kong, could not be distinguished from regions from which their coral feeding behaviour has not been documented. Furthermore, no distinction could be observed between D. rugosa specimens taken from Acropora and Fungia corals.

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Fig. 2. Phylogeny of Muricidae with Coralliophila as muricid outgroup based on a Bayesian inference (BI) analysis of a two-locus molecular dataset (mitochondrial COI and 12S), with emphasis on on Drupella and Morula diversity. Values above branches are MrBayes posterior probabilities as percentages. Specimens from Koh Tao are labelled R3, R7, R8 (D. rugosa), M2, M3, M4 (D. margariticola), S2 and S3 (M. spinosa). The coral prey from which a specimen was obtained is mentioned if applicable. The scale bar indicates the number of substitutions per site.

Distribution of muricids

The total of muricid individuals found within the 31 quadrats was 1249, consisting of 1145 Drupella rugosa, 60 D. margariticola and 40 Morula spinosa snails. Two quadrats were excluded from prey choice analyses due to minor uncertainties in the data and three large recruitment aggregations were left out of the mean site density calculation to prevent over-estimation. D. rugosa snails were found in every 10-m2 belt quadrat in which their number varied from one to 168 (Table 2). The average density (±SE) for D. rugosa calculated from all site densities was 3.17±0.69 indiv. m-2 in shallow areas and 3.45±1.54 indiv. m-2 in slightly deeper areas. D. margariticola occurred in relatively small numbers (shallow: 0.21±0.07 indiv. m-2, deep: 0.06±0.03 indiv. m-2) and M. spinosa occurred in even lower densities (shallow: 0.17±0.06 indiv. m-2; deep: 0.12±0.05 indiv. m-2) and generally did not seem as restricted to coral reef habitat as Drupella. All species were rare at pinnacles, with 0-2 individuals observed per dive. Related corallivores, e.g. other species of Drupella and Coralliophilinae, were not recorded at Koh Tao within and outside this study.

Although numbers of all three muricid species generally decreased with depth and were hardly seen below 8 m depth, no significant differences were found between medians of the shallow and slightly deeper quadrats (D. rugosa: W = 11, p = 0.147; D. margariticola: W = 20, p = 0.147; M. spinosa: W = 16.5, p = 0.460). Linear regressions based on the average depth of quadrats also showed slight negative trends that were insignificant (D. rugosa: p = 0.358; D. margariticola: p = 0.148; M. spinosa: p = 0.161). However, the distribution of juveniles and adults varied significantly over depth for D. rugosa (X2 = 2610.57, p < 0.0001, Fig. 3) and M. spinosa (X2 = 2.96, p < 0.0001), but not for D. margariticola (X2 = 49.50, p = 0.085). Juveniles were more abundant in shallow quadrats whereas adults were more abundant in the deeper quadrats.

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Table 2. Density (indiv. m-2) of Drupella rugosa, D. margariticola and Morula spinosa in transects at nine sites (Fig. 1) and two depth ranges: dark = 2-5 m, white = 5-8 m. Densities are the mean of 1-4 transects. Large aggregations of recruits have been omitted.

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Fig. 3. Mean density (+SE) of Drupella rugosa per size class in shallow (3-5m) and deep (5-8m) transects.

All species and their age groups were most abundant on stony coral than on any other substrate (Fig. 4). The total number of individuals on living coral was highest for D rugosa (95%) and D. margariticola (82%), which otherwise occurred on coral rubble. Relatively fewer M. spinosa snails were found on live coral substrate (65%), and they were also encountered on rock, rubble and sand. Substrate occupation differed between juveniles and adults only in D. rugosa, for which juveniles were found proportionally more on live coral (D. rugosa: X2 = Inf., p < 0.0001; D. margariticola: X2 = 1.28, p = 0.258; M. spinosa: X2 = 0.04, p = 0.842). D. rugosa were predominantly found on larger coral heads (> 10 cm diameter) (Fig. 5).

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Fig. 4. Total numbers of snail individuals per size class found on stony coral (HC) and other kinds of substrate for A) Drupella rugosa, B) D. margariticola and C) Morula spinosa.

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Fig. 5. Total number of coral colonies occupied by Drupella rugosa per colony size class based on maximum diameter (cm). Only one of the 235 occupied colonies fell within the 1-10 cm colony size range.

A significant positive correlation was found for Drupella density and healthy stony coral cover (r = 0.118, Adj. R2 = 0.199, p < 0.01). When the numerical transect variables were analysed in a generalized linear model to explain D. rugosa distribution, the simplest significant model under a quasi-poisson link function consisted of Acropora density (p < 0.01), depth (p < 0.01), and rubble (p < 0.05). The proportion of the variance that could be explained with this model is 0.56, which is quite low.

Some D. rugosa aggregations consisted of high numbers of recruits or juveniles and sometimes a few adults on the coral colony margin. These were all found on digitate, tabular and bushy Acropora colonies. All were found on different sites between 2 and 4 m depth and contained up to ~100 individuals. Three large aggregations of recruits (55, 56 and 96 individuals in size) were found within quadrats, which is three aggregations per 310 m2, or roughly one per 100 m2.

Prey choice

A total of 2714 coral colonies belonging to 33 genera were observed within the belt quadrats. The total number of coral colonies occupied by muricid snails was 235 for Drupella rugosa, 17 for D. margariticola and 25 for Morula spinosa (Table 3). Specimens of the opportunistic corallivore D. margariticola were found commonly, but not exclusively, together with those of D. rugosa (eight out of 17 colonies). Some M. spinosa snails were also found within a D. rugosa aggregation (four out of 25 colonies). The mean number of individuals per colony was 4.2±0.6 for D. rugosa, 2.8±0.8 for D. margariticola and 1.1±0.1 for M. spinosa. Group size did not differ between D. rugosa juveniles and adults in general (W = 5186, p = 0.337), although the aggregation size on different coral groups did vary: juveniles W = 7.74, p = 0.038; adults W = 14.29, p = 0.001 (Fig. 6).

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Fig. 6. Mean (+SE) group size of A) juvenile and B) adult Drupella rugosa on corals belonging to various genera and their growth forms: Acropora (B = branching/ arborescent, Bu = bushy/ caespitose, CDT = corymbose/ digitate/ tabular), Goniopora, Montipora, Pavona, Platygyra, Pocillopora, Porites (B = branching S = submassive), Psammocora.

The resource selection ratios revealed differences in prey selection between D. rugosa juveniles (including recruits) and adults (Table 4). Corals of only a few genera were preyed upon by juvenile snails. Acropora corals were favoured by both juvenile and adult snails, although adult D. rugosa were absent on corymbose, digitate or tabular colonies. All Acropora growth forms had high occupation rates and mean abundances of snails per occupied colony. Psammocora corals had the highest occupation rate and also strikingly higher mean group size of occupants than those of the other genera, with the exception of Acropora. Psammocora was significantly selected for by snails of all size classes. Colonies of Goniopora, Montipora (S), Platygyra and Porites (B and S) were attacked by adult snails as expected from their abundance. Pocillopora corals were ignored by juveniles and used less than expected by adults. The abundant Pavona colonies were occupied more than expected by adult muricids and less than expected by juveniles. Strikingly, the 612 fungiid corals were devoid of snails and were only very rarely noted to be preyed upon outside the quadrats.

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Table 3. Coral taxa and number of colonies > 10 cm found within the belt quadrats.

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Table 4. Overview of prey choice by Dru­pella rugosa through resource selection ratios of all, juvenile and adults occupied coral colonies. The occupation is in percentage of all colonies of that genus (and growth forms). The resource selection ratios with Bonferroni corrected 95 and 99% CI’s are calculated to show in which proportion groups are used as would be expected from their availability. They were preferred at p < 0.05 (*) or p < 0.01 (**), avoided at p < 0.01 (--), not used significantly more or less than expected (NS) or remained unused. Coral growth forms: B = branching/ arborescent, Bu = bushy/ caespitose, CDT = corymbose/ digitate/ tabular, S = submassive, EFL = encrusting/ foliose/ laminar.

Prey preference by D. margariticola snails followed that of co-occurring D. rugosa. When separate from their congeners, D. margariticola individuals were still observed to feed on corals of the same genera, although it is not known whether they initiated feeding on the coral while it was healthy or when it was already damaged or diseased. The coral genera selected by D. margariticola snails and the percentage of attacked colonies were Acropora (1.8%, B: 0.8%, Bu: 4.1%), Montipora (1.1%, S: 1.8%) and Pavona (0.7%). Only one or two M. spinosa individuals were found together on the same coral colony, and prey choice generally followed that of D. rugosa, although they were found relatively less commonly on Acropora. The coral genera selected by M. spinosa individuals and the percentage of colonies occupied by them were Acropora (0.4%, Bu 1.4%), Goniastrea (10%), Goniopora (4.1%), Montipora (3.3%, S: 5.5%), Pavona (1.3%), Porites (1.7%, S: 1.2%) and Psammocora (12%).

Discussion


Corallivorous muricids have been studied before in relation to changes in prey choice and their distribution at Koh Tao (Hoeksema et al., 2013). The present study allows a comparison of the muricid species composition with other situations in which muricids co-occurred in different geographic and ecological settings. The co-occurrence of coral feeding Drupella rugosa and D. margariticola has been extensively described for Hong Kong (e.g. Taylor, 1980; Morton and Blackmore, 2009). D. rugosa has been reported to reach high densities in co-occurrence with other Drupella species with high ecological impact on the Great Barrier Reef (Cumming, 1999). It is also known to co-exist with the muricid corallivorous snail Coralliophilla violacea (Kiener, 1836) (= C. nerotoidea (Gmelin, 1891)) (Fujioka and Yamazato 1983; Schuhmacher, 1992; McClanahan, 1994; Al-Moghrabi, 1997). The latter species has been reported to occur as individuals and in aggregations (Oren et al., 1998; Chen et al., 2004) but was not observed at Koh Tao. The extent of the diet of Morula spinosa has not consisively been defined despite its wide Indo-Pacific distribution (Taylor, 1978; Yokochi, 2004; Titlyanov and Titlyanova, 2009).

Implications for muricid (sub)species

Molecular characterization of the corallivorous muricids of Koh Tao shows that all species fall neatly within the expected existing groups of widely sampled muricid species. The two marker dataset produced a satisfactory tree with strong branch support. For Drupella rugosa, variation in shell morphology was noted. Nevertheless, no molecular basis was found to distinguish the variation, as was also found when Johnson and Cumming (1995) tested for D. fragum and D. rugosa hybrids. Moreover, no prey-related cryptic speciation seems to occur in D. rugosa, although data on this subject is preliminary and specimens from different prey should be more thoroughly sampled. Host-associated differentiation is already known from a selection of Caribbean and Indo-Pacific coralliophillines (Johnston et al., 2012; Simmonds et al., 2012), although this may not be the case and otherwise harder to prove for Drupella, owing to their cryptic and adaptive prey choice.

The sampled D. margariticola were part of the ‘Continental’ clade in which corallivory was already known to occur (Claremont et al., 2011a). The theory that all snails belonging to this clade could potentially feed on coral tissue is supported by this study and possibly far more widespread than currently documented. Coral consumption by Morula spinosa has formerly been documented for Japan (Yokochi, 2004) and now for Thailand. The coral feeding individuals do not differ genetically from conspecifics and thus the same applies, implying that this widespread species may feed on corals in other locations. Moreover, more muricid taxa could be able to opportunistically feed on corals than is currently known, as it has only recently been discovered for M. spinosa (Yokochi, 2004) and Ergalatax junionae (Saledhoust et al., 2011).

Distribution and habitat

Among Drupella species, D. rugosa was the first to catch attention because of its potential to cause damage to coral reefs (Moyer et al., 1982). Afterwards, D. cornus and D. fragum outbreaks were observed with mean densities higher than 3 indiv. m-2 (reviewed in Cumming, 2009). The density of > 3 D. rugosa m-2 at Koh Tao for both shallow and deep quadrats during an ongoing outbreak is in line with the documented outbreaks of their congeners. A number of indicators for problematic Drupella populations are also in line with an outbreak (Cumming, 2009), since 9% of all coral colonies were preyed on and large aggregations of juveniles (50-100 indiv.) were frequently encountered. For D. margariticola local mean densities of approximately 5 indiv. m-2 were found in Hong Kong (Morton and Blackmore, 2009), which was up to 1.3 indiv. m-2 at Koh Tao. Regarding the distribution of M. spinosa the highest mean local density in the present study measured was 0.5 indiv. m-2. Earlier reports on the occurrence and distribution of this species did not give quantitative data (Taylor, 1978; Yokochi, 2004). Concerning the density of populations of both D. margariticola and M. spinosa it is not known whether these have grown over previous years and it is not established in what density they occur under normal circumstances.

Since the 2010 mass bleaching event in the Gulf of Thailand, stony coral cover had declined and coral reef communities had changed (Chavanich et al., 2012; Yeemin et al., 2012). The reefs of Koh Tao were also affected by bleaching and other detrimental effects (Hoeksema and Matthews, 2011; Weterings, 2011; Hoeksema et al., 2013), and as such Drupella snails were able to thrive and more than double their relative abundance between 2009 and 2014 (unpublished data). Although some variation over sites occurs, a very high difference in occupation was noted among different habitats around Koh Tao. This was also described for Lizard Island (Great Barrier Reef), where D. rugosa occurs mostly on sheltered slopes, and D. cornus and D. fragum mostly occupy exposed reef crests (Cumming, 1999). Most reefs around Koh Tao are built on gentle slopes with moderate wave action, which appears ideal for D. rugosa. The pinnacles and rocky outcrops around Koh Tao (see Fig. 1) are exposed to stronger wave action and currents. Their steep slopes show low coral cover and therefore Drupella snails were rare.

The present results show a preference for high Acropora densities (see also Cumming, 2009), large colony sizes (see also Cumming, 2009; Schoepf et al., 2010) and a high cover of rubble and dead coral on which individuals dwell when not on a living colony. A high healthy stony coral cover was also preferred, although indications of correlations with unhealthy reef sites have been found before in Hong Kong (Morton et al., 2002) and Koh Tao (unpublished data). No single variable was able to appropriately explain Drupella distribution and the generalized model could only explain part of the variation in the data. A negative correlation of Drupella density with depth was found in earlier years for D. rugosa at Koh Tao (unpublished data), but this correlation was not significant in the present study. This is presumably due to the wide 3-m intervals (2-5 and 5-8 m) within which quadrats were laid out and the high densities found below 5 m depth at Taa Chaa. The drivers for the distribution of Drupella species remain unclear, although various aspects have also been discussed in previous studies, such as depth (Schoepf et al., 2010), habitat (Cumming, 1999), substrate cover and coral communities (e.g. Cumming, 1999; Morton and Blackmore, 2009; Schoepf et al., 2010), reef status, and anthropogenic reef use (e.g. McClanahan, 1994; Morton et al., 2002).

The distribution of D. margariticola and M. spinosa seemed less dependent on coral cover owing to their relatively high occupation of other substrata and their ability to feed on other prey. M. spinosa was more commonly found on sandy substrates and isolated outcrops than Drupella spp. Juveniles of D. rugosa were found more in shallow areas and juveniles of all species were more abundant on stony coral, although this was not significant for D. margariticola. In general there appeared to be different habitat and prey requirements for juvenile snails as compared to the adults.

Scleractinian prey preferences

A high prey preference for Acropora spp. was found for D. rugosa, although there were differences in occupation rate and aggregation size for juveniles and adults on different species (and growth forms), which was also revealed through resource selection functions for D. cornus (Schoepf et al., 2010). The present study also points out that Montipora is occupied less than can be expected from its availability and only by fairly small aggregations. This is even more so for Pocillopora species, which were generally observed to be one of the main prey species at Koh Tao in earlier years. In contrast, other studies point out that Drupella species, and D. rugosa in particular, often prey on Montipora and Pocillopora corals (e.g. Boucher, 1986; Baird, 1999), although there are many observations that do not take their relative abundance into account. The newly discovered preference for the relatively rare Psammocora contigua (Esper, 1794) is remarkable, whereas the preference of adult D. rugosa for Pavona spp. may be related to their abundance at Koh Tao. Compared to the coral community seen in Hong Kong (Morton and Blackmore, 2009), massive and encrusting corals do not dominate Koh Tao reefs and where local Acropora abundance is low, other genera with branching (Porites), foliose (Pavona) or submassive/ foliose (Psammocora) growth forms are selected as second-choice prey of D. rugosa. Furthermore, the coral genera preyed on by Drupella snails within quadrats only represented a portion of the available prey. Predation on other taxa was observed in the same and previous years (Hoeksema et al., 2013), although most of those occurrences are rare. Coral genera that D. rugosa has been observed to feed upon on Koh Tao reefs were Acropora, Alveopora, Ctenactis, Diploastrea, Euphyllia, Favites, Fungia, Galaxea, Goniastrea, Goniopora, Hydnophora, Leptoria, Lithophyllon, Lobophyllia, Merulina, Montipora, Pavona, Platygyra, Pleuractis, Psammocora, Pocillopora, Porites, Sandalolitha (examples in Fig. 7).

FIG2

Fig. 7. Drupella rugosa aggregations feeding on coral colonies from a variety of families. A: Psammocora contigua (Psammocoridae), B: Pavona sp. (Agariciidae), C: Diploastrea heliopora (Diploastreidae), D: Goniastrea sp. (Merulinidae), also with a single Drupella margariticola individual, E: Euphyllia ancora (Euphyllidae) F: Porites digitata (Poritidae).

The present study shows that fungiids, which were abundant in transects, were avoided by Drupella. After the 2010 bleaching event, Drupella at Koh Tao were witnessed to feed on fungiid corals in large aggregations after nearby Acropora colonies had died (Hoeksema et al., 2013). This was the first ever description of Drupella feeding on fungiids in high numbers. Although this was unusual, it was not entirely unexpected as Drupella diet is plastic and these corals also host various groups of parasitic molluscs (Gittenberger and Gittenberger, 2011; Hoeksema et al., 2012b; Gittenberger and Hoeksema, 2013). Kim (2013) reported that Fungia fungites at Koh Tao was still being preyed upon by large aggregations of adults in 2013. This was remarkable since fungiids quickly recovered from bleaching (Hoeksema et al., 2012a, 2013), and were not likely to be more vulnerable to predation. In the Java Sea, where massive coral bleaching was observed in 1983, neither mushroom corals nor other corals were reported as being under attack by Drupella (Brown and Suharsono, 1990; Hoeksema, 1991), although it was already known that secondary disturbances by predators after bleaching may occur (Glynn, 1988). Similarly, muricid predators of octocorals in Brazil also became more noticeable four years after the latter suffered from bleaching in 2010 (Dias and Gondim, 2016). The delayed shift of Drupella back to the preferred Acropora could be on account of a delayed recovery of the Acropora assemblages at Koh Tao and a co-occurring colony size and density refuge.

Drupella margariticola occurred in fairly low densities around Koh Tao. They were able to form small coral feeding aggregations separate from D. rugosa, although they occasionally co-occurred. This suggests that D. margariticola was able to initiate feeding by itself, although it is currently unknown whether it only occurs on already damaged colonies. They attacked corals of the common genera Acropora, Montipora and Pavona. Considering its low density around the island and relatively small size, D. margariticola is not expected to pose significant problems for coral reef communities as its large and numerous relatives. Nevertheless, its ability to initiate attacks on coral colonies and the proportion of corals in its diet might have been underestimated before. The first record of D. margariticola as opportunistic coral predator came from Hong Kong, where it co-occurred with D. rugosa (Morton et al., 2002; Morton and Blackmore, 2009). The present observation at Koh Tao is its second record as a corallivore, even though the species is known to have a widespread Indo-Pacific distribution. Its dietary preferences may previously have remained unnoticed because of its usually low population densities.

It is still unclear how Morula spinosa is able to feed on scleractinians, and they may be better described as coral scavengers than corallivores. Individuals have been found on damaged colonies of coral genera similar to those occupied by D. rugosa, whereas they have also been found on non-coral substrate and in non-reef habitats. Only one or two individuals occurred together and rarely in co-existence with Drupella aggregations. This indicates that they are able to feed on coral tissue, but not as intensively as Drupella snails. Coral damage by M. spinosa has been reported before, although this does not seem to be substantial (Yokochi, 2004), and mainly opportunistically on damaged or stressed corals (Titlyanov and Titlyanova, 2009). Their presence on a coral also does not always coincide with clear feeding scars and as such their presence could also mean that they associate with their host for other reasons. The main portion of its diet may consist of other molluscs, polychaetes, cadavers and other food sources many related predatory muricid species are known to feed on (see Taylor, 1978; Barco et al., 2010).

Local and widespread ecological implications

The outbreak densities of the Drupella rugosa population at Koh Tao were restricted to certain depths at reef flats and gentle slopes which occur much around the coastline. The population has grown despite removal efforts (unpublished data), and can have harmful effects on the already stressed reefs (Weterings, 2011; Lamb et al., 2014). Effects on reef health and the coral community by D. margariticola and Morula spinosa are expected to be negligible according to their low numbers and non-obligate feeding on corals. This is mostly in line with earlier descriptions of coral predation by these muricids (Morton and Blackmore, 2009; Yokochi, 2004). Although coral prey selection based on their relative abundance was not calculated for Hong Kong, occupation instances have been witnessed to differ between D. rugosa at Koh Tao and Hong Kong on account of differences in coral communities. Both examples of D. rugosa populations are unique regarding their prey choice in different coral communities (this study, Morton et al., 2002; Morton and Blackmore, 2009; Hoeksema et al., 2013) and climatic regimes (Morton and Blackmore, 2009; Tsang and Ang, 2015).

Juveniles of D. rugosa were found to prefer Acropora species with caespitose/digitate/tabular growth forms (Fig. 8), on which they form large feeding aggregations through which the colony ultimately perishes. This is in line with earlier notes on juveniles preferring Acropora both as a food source and as a sheltered habitat (Forde, 1992; McClanahan, 1997; Schoepf et al., 2010). Branching Psammocora contigua corals showed more aggregations of adult D. rugo­sa than expected and also a single juvenile aggregation. P. contigua and caespitose/digitate/tabular Acropora spp. were found to be relatively rare within transects. Their branches were in general brittle and commonly mechanically damaged and affected by some bleaching. Their fragile state within the local coral community along with continued high predation pressure by Drupella snails could have detrimental effects for these specific groups. Nevertheless, there are indications that coral species are able to escape feeding Drupella through small (< 10 cm) colony size refuge (Cumming, 2009), depth refuge (> 8 m), and a low relative availability. They may also benefit from the possible ability of Drupella to adapt to community changes and from its dietary shifts involving less preferred prey species that are in high abundance for elongated periods of time (Hoeksema et al., 2013). Drupella populations were observed to diminish living reef cover in many different habitats and coral communities (Moyer et al., 1982; Ayling and Ayling, 1992; McClanahan, 1994; Al-moghrabi, 1997; Antonius and Riegl, 1998), and change the coral community structure (Forde, 1992; Shafir and Gur, 2008; Hoeksema et al., 2013). Long-term monitoring should indicate whether Drupella outbreaks may be able to change the coral community so that certain coral species become locally endangered or extinct.

FIG2

Fig. 8. Typical feeding pattern of Drupella rugosa recruits on acroporid corals. Many 0-2 cm snails are grouped together in a cryptic manner between Acropora sp. branches and a clear zonation is revealed of dead, recently killed and living coral.

Acknowledgements


The authors thank the interns Maria Fredriksson, Florian Lang, Spencer Arnold and Melody Lim of the New Heaven Reef Conservation Program who helped obtain data in the field. In addition, Bastian Reijnen assisted with useful advice during lab work. The first author was financially supported by the A.M. Buitendijkfonds (Naturalis), J.J. ter Pelkwijkfonds (Naturalis) and LUSTRA and Outbound study grants (Leiden University). We also thank Marco Oliverio and two anonymous reviewers for their constructive comments on the manuscript.

Received: 1 August 2015

Revised and accepted: 8 January 2016

Published online: 26 August 2016

Editor: D. Huang

References


Al-Horani FA, Hamdi M, Al-Rousan SA. 2011. Prey selection and feeding rates of Drupella cornus (Gastropoda: Muricidae) on corals from the Jordanian coast of the Gulf of Aqaba, Red Sea. Jordan Journal of Biological Sciences 4: 191-198.

Al-Moghrabi SM. 1997. Bathymetric distribution of Drupella cornus and Coralliophila neritoidea in the Gulf of Aqaba (Jordan). Proceedings of the 8 th International Coral Reef Symposium, Panama 2: 1345-1350.

Antonius A, Riegl B. 1998. Coral disease and Drupella cornus invasions in the Red Sea. Coral Reefs 17: 48.

Arrigoni R, Terraneo TI, Galli P, Benzoni F. 2014. Lobophyl­liidae (Cnidaria, Scleractinia) reshuffled: Pervasive non-monophyly at genus level. Molecular Phylogenetics and Evolution 73: 60-64.

Ayling AM & Ayling AL. 1987. Ningaloo Marine Park: preliminary fish density assessment and habitat survey, with information on coral damage due to Drupella grazing. Report to the Department of Conservation and Land Management, Western Australia.

Ayling AM, Ayling AL. 1992. Preliminary information on the effects of Drupella spp. Grazing on the Great Barrier Reef, in Drupella cornus: a symposium, ed. S. Turner, Western Australia: Department of Conservation and Land Management, CALM Occasional Paper 3/92.

Baird A. 1999. A large aggregation of Drupella rugosa following the mass bleaching of coral on the Great Barrier Reef. Reef Research 9: 6-7.

Barco A, Claremont M, Reid DG, Houart R, Bouchet P, Williams ST, Cruaud C, Couloux A, Oliveiro M. 2010. A molecular phylogenetic framework for the Muricidae, a diverse family of carnivorous gastropods. Molecular Phylogenetics and Evolution 56: 1025-1039.

Bos AR, Hoeksema BW. 2015. Cryptobenthic fishes and co-inhabiting shrimps associated with the mushroom coral Helio­fungia actiniformis (Fungiidae) in the Davao Gulf, Philippines. Environmental Biology of Fishes 98: 1479-1489.

Boucher LM. 1986. Coral predation by muricid gastropods of the genus Drupella at Enewetak, Marshall Islands. Bulletin of Marine Science 38: 9-11.

Boyce MS, Vernier PR, Nielsen SE, Schmiegelow FKA. 2002. Evaluating resource selection functions. Ecological Modelling 157: 281-300.

Brown BE, Suharsono. 1990. Damage and recovery of coral reefs affected by El Nino related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8: 163-170.

Chansang H, Satapoomin U, Boonyanate P. 1999. Maps of coral reefs in Thai waters. Vol. 1, Gulf of Thailand. Coral Reef Management Project, Department of Fisheries, Phuket: 284.

Chavanich S, Viyakarn V, Adams P, Klammer J, Cook N. 2012. Reef communities after the 2010 mass coral bleaching at Racha Yai Island in the Andaman Sea and Koh Tao in the Gulf of Thailand. Phuket Marine Biological Center Research Bulletin 71: 103-110.

Chen MH, Soong K, Tsai ML. 2004. Host effect on size structure and timing of sex change in the coral-inhabiting snail Coralliophila violacea. Marine Biology 144: 287-293.

Claremont M, Reid DG, Williams ST. 2008. A molecular phylogeny of the Rapaninae and Ergalataxinae (Neogastropoda: Muricidae). Journal of Molluscan Studies 74: 215-221.

Claremont M, Reid DG, Williams ST. 2011a. Evolution of corallivory in the gastropod genus Drupella. Coral Reefs 30: 977-990.

Claremont M, Williams ST, Barraclough TG, Reid DG. 2011b. The geographic scale of speciation in a marine snail with high dispersal potential. Journal of Biogeography 38: 1016-1032.

Claremont M, Houart R, Williams ST, Reid DG. 2013. A molecular phylogenetic framework for the Ergalataxinae (Neogastropoda: Muricidae). Journal of Molluscan Studies 79: 19-29.

Cumming RL. 1999. Predation on reef-building corals: multiscale variation in the density of three corallivorous gastropods, Drupella spp. Coral Reefs 18: 147-157.

Cumming RL. 2002. Tissue injury predicts colony decline in reef-building corals. Marine Ecology Progress Series 242: 131-141.

Cumming RL. 2009. Population outbreaks and large aggregations of Drupella on the Great Barrier Reef. Great Barrier Reef Marine Park Authority, Research Publication 96: 1-26.

Dai CF, Yang HP. 1995. Distribution of Spirobranchus giganteus corniculatus (Hove) on the coral reefs of southern Taiwan. Zoological Studies 34: 117-125.

Dias TLP, Gondim AI. 2016. Bleaching in scleractinians, hydrocorals, and octocorals during thermal stress in a northeastern Brazilian reef. Marine Biodiversity 46: 303-307.

Drummond AJ, Ashton B, Buxton S, et al. 2013. Geneious v6.1.6. Available from http://www.geneious.com.

Forde MJ. 1992. Populations, behavior and effects of Drupella cornus on the Ningaloo Reef, Western Australia. Pp. 45-50 in: Turner S, ed., Drupella cornus: a synopsis. Proceedings of a Workshop held at the Department of Conservation and Land Management, Como, Western Australia, 21-22 Nov. 1991. Calm Occasional Paper: 3/92.

Fujioka Y. 1982. On the secondary sexual characters found in the dimorphic radula of Drupella (Gastropoda: Muricidae) with reference to its taxonomic revision. Venus 40: 203-223.

Fujioka Y, Yamazato K. 1983. Host selection of some Okinawan coral associated gastropods belonging to the genera Drupella, Coralliophila and Quoyula. Galaxea 2: 59-73.

Gittenberger A, Gittenberger E. 2011. Cryptic, adaptive radiation of endoparasitic snails: sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Organisms, Diversity and Evolution 11: 21-41.

Gittenberger A, Hoeksema BW. 2013. Habitat preferences of coral-associated wentletrap snails (Gastropoda: Epitoniidae). Contributions to Zoology 82: 1-25.

Glynn P. 1988 El Niño-Southern Oscillation 1982-1983: nearshore population, community, and ecosystem responses. Annual Review of Ecology and Systematics 19: 309-345.

Glynn P. 1990. Feeding ecology of selected coral-reef macroconsumers: patterns and effects on coral community structure. Pp. 365-400 in: Dubinsky Z., ed., Ecosystems of the world, 25, Elsevier Science, Amsterdam, The Netherlands.

Guest JR, Baird AH, Maynard JA, Muttagin E, Edwards AJ, Campbell SJ, Yewdall SJ, Affendi YA, Chou LM. 2012. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7: e33353.

Guzner B, Novplanzky A, Shalit O, Shadwick NE. 2010. Indirect impacts of recreational scuba diving: patterns of growth and predation in branching stony corals. Bulletin of Marine Science 86: 727-742.

Hoeksema BW. 1991. Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Marine Ecology Progress Series 74: 225-237.

Hoeksema BW, Matthews JL. 2011. Contrasting bleaching patterns in mushroom coral assemblages at Koh Tao, Gulf of Thailand. Coral Reefs 30: 95.

Hoeksema BW, Matthews JL. 2015. Partial bleaching in an assemblage of small apozooxanthellate corals of the genera Heteropsammia and Heterocyathus. Coral Reefs 34: 1227.

Hoeksema BW, Matthews JL, Yeemin T. 2012a. The 2010 coral bleaching event and its impact on the mushroom coral fauna of Koh Tao, Western Gulf of Thailand. Phuket Marine Biological Center Research Bulletin 71: 71-81.

Hoeksema BW, Van der Meij SET, Fransen CHJM. 2012b. The mushroom coral as a habitat. Journal of the Marine Biological Association of the United kingdom 92: 647-663.

Hoeksema BW, Scott C, True JD. 2013. Dietary shift in corallivorous Drupella snails following a major bleaching event at Koh Tao, Gulf of Thailand. Coral Reefs 32: 423-428.

Huang D, Benzoni F, Fukami H, Knowlton N, Smith ND, Budd AF. 2014. Taxonomic classification of the reef coral families Merulinidae, Montastraeidae, and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society 171: 277-355.

Johnston L, Miller MW, Baums IB. 2012. Assessment of host-associated genetic differentiation among phenotypically divergent populations of a coral-eating gastropod across the Caribbean. PLoS ONE 7(7): e47630. http://dx.doi.org/10.1371/journal.pone.0047630

Johnson MS, Cumming RL. 1995. Genetic distinctness of three widespread and morphologically variable species of Drupella (Gastropoda, Muricidae). Coral Reefs 14: 71-78.

Johnson MS, Holborn K, Black R. 1993. Fine-scale patchiness and genetic heterogeneity of recruits of the corallivorous gastropod Drupella cornus. Marine Biology 117: 91-96.

Keesing JK. 1990. Feeding biology of the crown-of-thorns starfish, Acanthaster planci (Linnaeus). PhD thesis, James Cook University of North Queensland, Townsville: 197.

Kim T. 2013. Determining the abundance, density, population structure, and feeding preference of Drupella snails on Koh Tao, Thailand. Bachelor thesis, Mahidol University, Bangkok.

Kita M, Kitamura M, Koyama T, Teruya T, Matsumoto H, Nakano Y, Uemura D. 2005. Feeding attractants for the muricid gastropod Drupella cornus, a coral predator. Tetrahedon Letters 46: 8583-8585.

Lamb JB, True JD, Piromvaragorn S, Willis BL. 2014. Scuba diving damage and intensity of tourist activities increases coral disease prevalence. Biological Conservation 178: 88-96.

Manly BFJ, McDonald LL, Thomas DL. 1993. Resource selection by animals: statistical design and analysis for field studies. Chapman and Hall, London.

McClanahan TR. 1994. Coral-eating snail Drupella cornus population increases in Kenyan coral reef lagoons. Marine Ecology Progress Series 115: 131-137.

McClanahan TR. 1997. Dynamics of Drupella cornus populations on Kenyan coral reefs. Proceedings of the 8 th International Coral Reef Symposium, Panama 1: 633-638.

Morton B, Blackmore G, Kwok CT. 2002. Corallivory and prey choice by Drupella rugosa (Gastropoda: Muricidae) in Hong Kong. Journal of Molluscan Studies 68: 217-223.

Morton B, Blackmore G. 2009. Seasonal variations in the density of and corallivory by Drupella rugosa and Cronia margariticola (Caenogastropoda: Muricidae) from the coastal waters from Hong Kong: ‘plagues’ or ‘aggregations’? Journal of the Marine Biological Association of the United Kingdom 89: 147-159.

Moyer JT, Emerson WK, Ross M. 1982. Massive destruction of scleractinian corals by the muricid gastropod, Drupella, in Japan and the Philippines. The Nautilus 96: 69-82.

Oigman-Pszczol SS, Creed JC. 2006. Distribution and abundance of fauna on living tissues of two Brazilian hermatypic corals (Mussismilia hispida (Verril, 1902) and Siderastrea stellata Verril, 1868). Hydrobiologia 563: 143-154.

Oliverio M, Mariottini P. 2001. A molecular framework for the phylogeny of Coralliophila and related muricoids. Journal of Molluscan Studies 67: 215-224.

Oliverio M, Modica MV. 2010. Relationships of the haematophagous snail Colubraria (Rachiglossa: Colubrariidae), within the neogastropod phylogenetic framework. Zoological Journal of the Linnean Society 158: 779-800.

Oren U, Brickner I, Loya Y. 1998. Prudent sessile feeding by the corallivore Coralliophila violacea on coral energy sinks. Proceedings of the Royal Society London Series B 265: 2043-2050.

Patton WK. 1994. Distribution and ecology of animals associated with branching corals (Acropora spp.) from the Great Barrier Reef. Bulletin of Marine Science 55: 193-211.

Plass-Johnson JG, Schwieder H, Heiden J, Weiand L, Wild C, Jompa J, Ferse SCA, Teichberg M. 2015. A recent outbreak of crown-of-thorns starfish (Acanthaster planci) in the Spermonde Archipelago, Indonesia. Regional Environmental Change 15: 1157-1162.

R Depelopment Core Team. 2010. R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing. http://www.rstudio.com.

Robertson R. 1970. Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pacific Science 24: 43-54.

Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Hohna B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542.

Saledhoust A, Negarestan H, Jami MJ, Morton B. 2011. Corallivorous snails: first record of corallivory by Ergalatax junionae (Gastropoda: Muricidae) in the Persian Gulf. Marine Biodiversity Records 4: e99.

Schoepf V, Herler J, Zuschin M. 2010. Microhabitat use and prey selection of the coral-feeding snail Drupella cornus in the Northern Red Sea. Hydrobiologia 641: 45-57.

Schuhmacher H. 1992. Impact of some corallivorous snails on stony corals in the Red Sea. Proceedings of the 7 th International Coral reef Symposium, Guam 2: 840-846.

Scott CM, Mehrotra R, Urgell P. 2015. Spawning observation of Acanthaster planci in the Gulf of Thailand. Marine Biodiversity 45: 621-622.

Shafir S, Gur O. 2008. A Drupella cornus outbreak in the Northern Gulf of Eilat and changes in coral prey. Coral Reefs 27: 379.

Simmonds SE, Rachmawati R, Cheng SC, Barber PH. 2012. Host-specificity and ecological speciation in Indo-Pacific corallivorous gastropods. Contributed talk. Western Society of Naturalists. Monterey, California.

Stefani F, Benzoni F, Pichon M, Cancelliere C, Galli P. 2008. A multidisciplinary approach to the definition of species boundaries in branching species of the coral genus Psammocora (Cnidaria, Scleractinia). Zoologica Scripta 37: 71-91.

Stella JS, Pratchett MS, Hutchins PA, Jones GP. 2011. Coral-associated invertebrates: diversity, ecology importance and vulnerability to disturbance. Oceanography and Marine Biology: An Annual Review 49: 43-104.

Taylor JD. 1978. Habitats and diet of predatory gastropods at Addu Atoll, Maldives. Journal of Experimental Marine Biology and Ecology 31: 83-103.

Taylor JD. 1980. Diets and habitats of shallow water predatory gastropods around Tolo Channel, Hong Kong. In: Morton B. (ed.) Proceedings of the first international workshop on the malacofauna of Hong Kong and Southern China, Hong Kong, 1977. Hong Kong University Press: 163-165.

Titlyanov EA, Titlyanova TV. 2009. The dynamics of the restoration of mechanical damage to colonies of the scleractinian coral Porites lutea under conditions of competition with algal settlers for substratum. Russian Journal of Marine Biology 35: 230-325.

Tsang RHL, Ang P. 2015. Cold temperature stress and predation effects on corals: their possible roles in structuring a nonreefal coral community. Coral Reefs 34: 97-108.

Turner SJ. 1994. Spatial variability in the abundance of the corallivorous gastropod Drupella cornus. Coral Reefs 13: 41-48.

Wallace CC, Chen CA, Fukami H, Muir PR. 2007. Recognition of separate genera within Acropora based on new morphological, reproductive and genetic evidence from Acropora togianensis, and elevation of the subgenus Isopora Studer, 1878 to genus (Scleractinia: Astrocoeniidae; Acroporidae). Coral Reefs 26: 231-239.

Weterings R. 2011. A GIS-based assessment of threats to the natural environment on Koh Tao, Thailand. Kasetsart Journal: Natural Science 45: 743-755.

Yeemin T, Pengsakun S, Yucharoen M, Klinthong W, Sangmanee K, Sutthacheep M. 2012. Long-term decline in Acropora species at Kut Island, Thailand, in relation to coral bleaching events. Marine Biodiversity 43: 23-29.

Yokochi H. 2004. Predation damage to corals. Pp. 49-55 in: The Japanese Coral Reef Society and Ministry of the Environment, ed. Coral reefs of Japan. Ministry of the Environment, Tokyo, Japan. 356 p.

Zou S, Li U, Kong L. 2011. Additional gene data and increased sampling give new insights into the phylogenetic relationships of Neogastropoda, within the caenogastropod phylogenetic framework. Molecular Phylogenetics and Evolution 61: 425-435.

Zuschin M, Oliver PG. 2003. Bivalves and bivalve habitats in the northern Red Sea. The northern Bay of Safaga (Red Sea, Egypt): an actuopalaeontological approach. VI, Bivalvia Naturhistorisches Museum, Wien: 304.

Appendix


GenBank accession numbers for 12S and COI sequences. Accession numbers beginning with EU were first published by Claremont et al. (2008), FM by Oliverio and Modica (2010), FN by Barco et al. (2010), FR by Claremont et al. (2011), GU by Zou et al. (2011), HE by Claremont et al. (2013), and HQ by Zou et al. (2011). Field collection numbers and Naturalis Biodiversity Center collection numbers (RMNH) are listed for new sequences with GenBank accession numbers KT343581 through KT343595.

FIG2

Appendix