Next Article in Journal
Transformations of Vascular Flora of a Medieval Settlement Site: A Case Study of a Fortified Settlement in Giecz (Wielkopolska Region, Western Poland)
Next Article in Special Issue
Density and Bleaching of Corals and Their Relationship to the Coral Symbiotic Community
Previous Article in Journal
The Influence of Volcanism, Soils, and Climate in the Endemicity Levels of Asteraceae in the Arequipa Region (Southern Peru)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 15
Issue 1
10.3390/d15010034
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Resource Partitioning by Corallivorous Snails on Bonaire (Southern Caribbean)

by
Lukas Verboom
1,2 and
Bert W. Hoeksema
1,2,*
1
Taxonomy, Systematics and Geodiversity Group, Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands
2
Groningen Institute for Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(1), 34; https://doi.org/10.3390/d15010034
Submission received: 8 November 2022 / Revised: 20 December 2022 / Accepted: 23 December 2022 / Published: 28 December 2022
(This article belongs to the Special Issue Symbiotic Invertebrates in Coral Reef Communities)
Browse Figures
Versions Notes

Abstract

:
A biodiversity survey on three corallivorous snails (Mollusca: Gastropoda) was performed at 28 sites around the island of Bonaire to assess their distribution patterns and associated host corals. The snails and their hosts were identified and counted in three depth zones: 5–10, 10–20, and 20–30 m. The snails were Coralliophila galea and C. salebrosa (Muricidae: Coralliophilinae), and Cyphoma gibbosum (Ovulidae: Simniinae). All three species were widespread around the island without apparent interspecific geographical variation. Coralliophila galea was found exclusively on scleractinian corals, Coralliophila salebrosa almost exclusively on octocorals, and Cyphoma gibbosum only on octocorals. Coralliophila salebrosa showed more dietary overlap with Cyphoma gibbosum than with Coralliophila galea. Coralliophila galea was the most commonly encountered species with the largest number of host species. Owing to its hosts distribution, this species also showed a greater maximum depth and a wider bathymetrical range than the other two snails. The other two snails were shallower and their depth ranges did not differ significantly. Host-coral size did not seem to have influence on the number of snails per host. Coral damage caused by the snails was visible but appeared to be low, causing no mortality in Bonaire, which suggests that the relation with their hosts is more parasitic than predatory. Because these three corallivores have occasionally been reported to occur as outbreaks in other Caribbean localities and may act as vectors in the dispersal of coral diseases, it is recommended that future studies should focus on their population dynamics.

1. Introduction

Coral reefs in the Atlantic, including those in the Caribbean Sea and the Gulf of Mexico, are relatively poor in species compared to those in the Indo-West Pacific [1,2]. This is also evident for corals. For example, the number of ca. 75 Atlantic scleractinian reef coral species is only 10% of the much larger number of ca. 750 Indo-Pacific species [3]. For various other groups of reef-dwelling corals, such as octocorals, similar comparisons are more difficult to make because of insufficient taxonomic knowledge and lack of biogeographic review studies.
Reef corals are host to many other groups of invertebrates, among which various species of gastropod molluscs [4,5]. Most of these snails are host-specific to a certain degree, either as corallivorous parasites or as predators [6]. In daylight, they can be observed roaming on the coral surface [7,8,9], hiding underneath their host corals [10,11], inside coral crevices [12,13], in between coral branches [14,15], or on the outer surface of branches by use of camouflage [16,17]. They belong to a number of families, such as Epitoniidae [18], Muricidae [19,20,21], Pediculariidae [22,23,24], Ovulidae [23,25,26], and Trinchesiidae [27,28,29,30]. Some other coral-associated gastropods live entirely or partly embedded in the coral skeleton, such as the Leptoconchus species of the family Muricidae [31,32]) and worm snails of the family Vermetidae [33,34].
Corallivorous snails have a reputation for causing damage to coral reefs [35,36,37] and have the potential to form aggregations that can manifest themselves as outbreaks [38,39,40,41,42,43,44]. The snails are also known to spread infectious coral diseases [45,46,47,48,49]. Therefore, monitoring of their abundance could be relevant during surveys of coral reef health, especially in tropical marine protected areas (MPAs).
A well-known example of such an MPA is Bonaire National Marine Park in the southern Caribbean (12°9′ N, 68°16′ W), which was established in 1979 and is important for the local diving industry [50]. Although Bonaire is known to harbor one of the best preserved coral reef ecosystems in the Caribbean Sea [51], the island itself is undergoing much urban development and its reefs are therefore under much anthropogenic stress [52,53,54,55].
Relatively few studies on Bonaire have a focus on its marine biodiversity and the role of coral-associated fauna therein. Therefore, an expedition was organized in 2019 to survey its coral reef biota [56]. Special attention was given to the role of interspecific relationships in benthic communities, mostly involving cnidarians that live in association with other invertebrates. This resulted in the discovery of various novel associations [34,57,58,59,60,61,62,63,64], two of which appeared to be harmful to corals. One these two was about symbiotic worm snails and the other one about sabellid worms that lived partly embedded in the coral skeletons [34,60]. Here, we report on the abundance and co-occurrences of corallivorous snails because of the possible damage they may cause to their coral prey.
The most common corallivorous snails in the Caribbean are species of the genera Coralliophila (Muricidae) and Cyphoma (Ovulidae) [65]. These snails usually stay on the same coral that they eat and can be found on the outer surface of coral branches, underneath coral margins, and inside crevasses of massive corals [12,36,66,67]. There are a few records of Coralliophila aggregations that consume large portions of the host-coral’s soft tissue [36,68]. In total, eight valid Coralliophila species are known to occur in the Caribbean [68], of which C. galea (previously also recorded as C. abbreviata) and C. salebrosa (previously recorded as C. caribea) [12,68], are most commonly recorded. Coralliophila species show weak genetic diversity between hosts, and there are some clear differences in shell morphology for specimens living on different hosts [12,69,70,71]. Coralliophila species feed with the help of a proboscis, which is inserted into the oral opening of coral polyps [72,73]. Many Coralliophila species are sessile for long periods of time, feeding off nearby corals without destroying the host-coral tissue [73,74].
Currently, 15 Cyphoma species are recognised in the Caribbean, of which Cyphoma gibbosum is by far the most common [23,75]. They are vividly coloured molluscs with different patterns on their mantle, which is key to their identification [26,75,76]. It is typically coloured light brown, with black ring-shaped markings. The number and size of these marks are variable, and occasionally different marks develop. The species is active during the day and snails are often seen foraging by SCUBA divers. Cyphoma gibbosum has been found to consume octocoral species of the families Gorgoniidae, Plexauridae, Briareidae, and, occasionally, Anthothelidae [7,26,77,78,79].
Since most Coralliophila and Cyphoma species are considered host generalists, the present study aims to study (1) which corallivorous snails are present on Bonaire, (2) how they differ in geographical and bathymetrical distributions, (3) and what are their host ranges and overlaps therein. Eventually, the results may show which coral taxa are potentially most in danger in the event of outbreaks.

2. Materials and Methods

Data collection. The field survey on Bonaire was performed between the 23rd of October and the 8th of November, 2019. Distribution data on Coralliophila and Cyphoma was collected during SCUBA diving in daytime at 28 different locations (one dive each) around the island (ESM Figure S1, Table S1). Most localities were at the leeward site of the island, where wave action is less strong than at the windward side. The roving diving (timed-swim) technique was employed based on fixed periods of observations [80]. One extra night dive was performed to study the foraging behaviour of the snails, which was not part of the regular survey. During each dive, 20 min were spent per depth zone (5–10, 10–20, and 20–30 m) to record coral-snail associations by visual inspection. Whenever snails were found on a hard coral (Scleractinia), the number of individuals was counted visually and also determined by manually touching the host along and below its edges. Octocorals were only visually scanned for snails. Notes were made of the number of snail individuals, their identity, depth, host-coral identity, host-coral size, and presence/absence of apparent host-coral damage (visible as grazing wounds). The coral length was measured using a measuring tape. Notes were written on a home-made PVC slate and entered in the database after each dive. Pictures were taken of the snails and their hosts for the conformation of their identity. The camera was an Olympus tough TG5, with an underwater housing.
Specimen identification. Coralliophila species were identified based on the work by Potkamp et al. [12], who found three reef-dwelling species at the adjacent island of Curaçao. Coralliophila galea and C. salebrosa can be distinguished based on the colouration of their shell aperture and operculum. Coralliophila galea has an orange-white shell aperture and orange operculum and C. salebrosa has a purple-white shell aperture and a red-brown operculum (Figure 1a,b). Coralliophila curacaoensis is smaller and its shell is more angular than the other species; the colour of its operculum is intermediate between that of C. galea and C. salebrosa [12]. For the identification of Cyphoma snails (Figure 1c), the work by Lorenz [76] was used, which differentiated between various colour morphs despite the apparent genetic heterogeneity, because in previous studies, different Cyphoma colour morphs showed variation in coral associations [76,81]. The coral identifications were carried out with the help of two publications: a printed field guide [82] and an online source that was published as electronic supplementary material [83]. Octocoral identification is often tedious and requires microscopic examination of skeletal sclerites [84]. Because the aim of this research was to find as many gastropod-coral associations as possible, we recorded octocoral hosts at species level when they could be easily identified in the field and otherwise at genus level.
Analysis. The results were analysed in R version 3.6.2 and 4.2.1 [85]. Differences in bathymetrical distributions were examined using ANOVA. A linear model was used to correlate coral sizes with the number of snail individuals found on a coral.
Bipartite network. For the snail–coral interactions, a bipartite network was composed using the R-package bipartite [86,87]. This network allows for comparisons between interacting species and is often used for interactions between predators and prey species [88,89]. The H2’-factor was calculated with the function H2fun [90]. This value is an index of entropy, where 0 means that there is no specialization and interactions are completely random and 1 means that all species in a system are specialized. Non-randomness was tested with the function wine, which estimates the weighted interaction nestedness of a dataset.
Principle component analyses. Principle component analyses were performed using the numerical data collected with each observation: locality coordinates, depth, number of snails, and coral size. The analysis was done once to interspecifically compare the snail species, and again for every recorded snail species to compare associated coral species. A generalised mixed model (GLM) was then used to assess the significance of individual predictors in the dataset; the GLM used was a negative binomial GLM to avoid over-dispersion. This analysis was performed using the glm.nb function from the package “MASS” in R. The data were log-transposed.
GIS. The maps in this report were generated using ArcMap 10.5.1. For the distribution maps displaying snail abundance per site, a light grey map provided by Esri was used as a base layer. Total abundance of each species was displayed for each dive site. For the map displaying the dive sites, a world topographical map, also provided by Esri, was used (ESM Figure S1).

3. Results

Coralliophila snails were generally immobile on dead patches of coral along the edges of the host-coral colonies. During the day, only a few were found on top of living coral but these were not foraging. Foraging behaviour was only observed once, during a night dive that was not part of the regular survey. Cyphoma gibbosum was seen to be actively foraging in day light.
In total, 689 corallivorous gastropods were recorded, representing two Coralliophila species, C. galea and C. salebrosa (Figure 1a,b). A single Coralliophila specimen could not be identified. Only one Cyphoma species was represented, i.e., Cyphoma gibbosum (Figure 1c).
No Coralliophila grazing scars were found. Patches of dead coral were present in the crevices where the snails were settled but these were not new. Cyphoma gibbosum snails were usually found on wounds of a few centimetres long on octocoral branches where soft tissue was damaged or had disappeared. There are no quantitative data for this.
There was no indication of dissimilarity among the three species with regard to geographical distribution (Figure 2a–c). The southernmost locality, Red Slave (Bon.27), was the only site without Coralliophila records, but the nearest dive sites, Bon.07 and Bon.17, yielded 19 and 56 snails, respectively, with all three species represented (Figure 2a–c).
Coralliophila galea was the most commonly species observed species, represented by 575 individuals on 101 scleractinian host corals at 26 out of 28 localities. Up to 36 snails were encountered on a single coral. Coralliophila salebrosa was rarer with 34 snails on 16 host corals (predominantly octocorals) at 10 localities. The highest number of snails on a single host was four. Cyphoma gibbosum was found exclusively on octocorals—79 individuals on 40 host corals at 20 localities. The highest number of individuals on a single coral was eight. As host corals, 10 scleractinian species, five octocoral species, and three octocoral genera were recorded (Table 1).
A bipartite network visualised interactions between snails and their host corals with possible overlapping (Figure 3). The H2’-value is the measurement of entropy, where a value of 0 implies no specialization and 1 implies extreme specialization [90]. With all coral and snail species, H2’ = 0.833, and for only the octocorals H2’ = 0.123. The model shows statistically dissimilar food utilisations on the analysed coral selection (p < 0.01).
Coralliophila galea was found in association with nine scleractinian coral species. It was most common on Orbicella annularis, represented by 85% records. Madracis auretenra, Orbicella franksi, and Agaricia agaricites were the only other host species with more than 10 C. galea records (Table 1). Coralliophila salebrosa was almost exclusively found on octocorals. Only one individual was found on a scleractinian coral, Madracis auretenra. The recorded host species for Cyphoma gibbosum are all in the octocoral families Gorgoniidae and Plexauridae (Table 1). The diversity of octocoral hosts was higher than that of Coralliophila salebrosa. It seemed to be absent at localities near Kralendijk, the only town on Bonaire. Antillogorgia bipinnata, which was common on Bonaire, was commonly found to host Cyphoma gibbosum, but not Coralliophila salebrosa.
A principal component analysis (PCA) tested the significance of numerical variables on the observations. The data concerned depth, coral size, number of snails, and locality coordinates (Figure 4). The analysis was done for all snail species together (Figure 4a) and for each separate one (Figure 4b–d). The longitudinal and latitudinal coordinates have opposite correlations, because most localities are on a Northwest/Southeast line (Figure 2). The interspecific comparison does not show obvious ecological differences (Figure 4a). The generalised mixed model shows that depth is the only significant predictor for the number of snails per observed association (p < 0.001; z = −3.5).
For Coralliophila salebrosa and Cyphoma gibbosum, the number of data points is too low to show reliable correlations in the PCA. For Coralliophila galea, there seems to be a correlation between the number of snails and the size of the coral, which are negatively correlated with the depth of the observation. The number of snails per coral also seems to be negatively correlated with depth. Agaricia agaricites stands out as host with no more than two snail individuals per coral colony. Overall, this host was utilised at greater depths than all hosts together, with an average depth of 15 m.
There was a slight correlation between coral size and the number of snails (Figure 5), but this was not significant (C. galea: R = 0.02, F = 2.14, p = 0.14; C. salebrosa: R = 0.08, F = 2.27, p = 0.15; C. gibbosum: R = 0.01, F = 0.50, p = 0.48). The five observations with the highest number of snail individuals all concern Coralliophila galea on Orbicella annularis colonies between 60 and 80 cm in width. On average, there were slightly more individuals of Coralliophila galea on Orbicella annularis compared to the other coral species, but this difference was not significant. Hence, there is no evidence of a relationship between coral size and the number of corallivorous snails.
There was variation in bathymetrical distribution among the snail species (Figure 6; ANOVA: F = 5.27; p < 0.05). Coralliophila galea was on average deeper than the other two species and it was much more common at depths over 20 m; among 25 recorded corallivorous snails, 22 were Coralliophila galea, two were C. salebrosa, and one, Coralliophila sp., was unidentified. Differences in bathymetrical distributions between any two species were not significant. No coral damage was observed around C. salebrosa snails. They were always found on the base of the host but within reach of some polyps.
Coralliophila galea was the only species found abundantly below a depth of 10 m. The host utilization varies among the three depth ranges (Figure 7). In the shallowest zone (0–10 m), the most utilised coral species was Orbicella annularis with 90% of the encountered snails. No apparent feeding scars were seen on O. annularis. Orbicella franksi was not noted as a host at that depth. At 10–20 m depth, almost all snails were found on O. annularis, whereas O. franksi was the second-most common host. No O. annularis was observed at deeper than 20 m. Three observations of Coralliophila galea concerned O. franksi, with densities of one, two and five snails per coral, all at a depth of 21 m.

4. Discussion

Our survey of the distribution and diet of corallivorous gastropods on Bonaire indicated interspecific overlaps in resource use. There were no signs of coral mortality because of predation. It appears that there is no shortage of food for the snails, which eventually might cause interspecific competition among them. There are reports from other Caribbean areas that mention severe coral mortality because of corallivorous snails [36,91]. The lack of mortality can be linked to the low densities of the three snail species.
Coralliophila galea was the most common species and found at the widest depth range, from 2 to 29 m, which approached the maximum survey depth. Since Bonaire’s coral reefs extend beyond 50 m depth [51,92] and many of the same host coral species may occur there as those at 30 m [93], it is likely that C. galea occurs at a greater depth than the presently recorded maximum depth. All encountered host associations for C. galea were also found in Curaçao [12]. Orbicella annularis was by far the most common host of Coralliophila galea, which also agrees with results found on Curaçao [94]. Studies in other Caribbean localities also reported this association as common [95,96]. Orbicella annularis can be distinguished from other Orbicella species by its tendency to form columns with wide space in between them, allowing for settlement of Coralliophila clusters [82]. Coral colonies of this species have many depressions in their surface without live tissue, which provide an optimal resting place for parasitic snails. At 20–30 m depth, no C. galea were recorded on O. annularis, which was found to be relatively rare in this depth range at nearby Curaçao [97]. The depth distribution and differences in host occupation across depths can therefore be explained by host availability, even though this was not recorded in the present study.
In the present study, no apparent recent feeding scars were seen on Orbicella annularis. Coralliophila galea may appear to be immobile for days or there may be some movement in time spans of several weeks without any increase in size of the scars presumably because they predominantly feed by probing polyps without killing them [12,75]. However, they may become lethal to their hosts when they reach high densities [35,36,68]. A single Coralliophila galea individual was observed on top of a living Acropora palmata causing much damage, suggesting that this coral may be susceptible to attacks by the snail, which is consistent with observations in other Caribbean areas [98,99,100].
Coralliophila salebrosa was almost exclusively found in association with octocorals, whereas on Curaçao, this species was also found on 12 different scleractinian corals [12] and an additional scleractinian host species was recently recorded from Brazil [101]. Our results are in line with previous studies on host preference of this species [102,103]. The search effort by Potkamp et al. [12] on Curaçao was not specified, but their study took place in less than two months and was comparable to the effort of the present study.
No damage to the corals was observed around the snails of Coralliophila salebrosa. Its feeding mechanism has not been studied as much as that of C. galea, but it is similar to that and of other congenerics, causing minimal damage [6,12,75,101,104,105]. Therefore, the effects are less visible as no scar of removed tissue can be observed, although severe damage may occur when the snails occur in large aggregations [36,68]. Since our observations were done during the day, it is possible that the location where Coralliophila snails were observed was not exactly the same as where they graze, but studies suggest that they generally do not move much for long periods of time [74,75].
Coralliophila curacaoensis, originally described from Curaçao, was not found during the present survey. This species is only known from two host species, Madracis auretenra and M. decactis, and two localities, Curaçao in the southern Caribbean and Martinique in the eastern Caribbean [12,68]. It is impossible to prove that C. curacaoensis is absent on Bonaire, but we can assume that it is at best very rare. Although Bonaire and Curaçao are only 40 km apart, their marine faunas are not entirely the same as observed in comparisons of anthozoan faunas [64,106].
We encountered 79 individuals of Cyphoma gibbosum, which is the most common reported ovulid species throughout the Caribbean. All encountered individuals were normally coloured, with round black ring-shaped markings (Figure 1c). It was most abundant around 10 m deep, which is also the depth where most gorgonian prey species are present. The predation marks on the corals were clearly visible but since snail densities were fairly low (Figure 2c). The current numbers of snails are therefore not expected to have an effect on the coral populations.
The absence of other Ovulidae observations during the survey can be related to their rarity. Earlier, two other species have been recorded as Bonaire, namely Cyphoma signatum and C. cassidyae [76]. Both of these species/morphs are rarely encountered [76,107]. Cyphoma signatum is usually found on Plexaurella spp., whereas C. cassidyae is probably polyphagous [76,81]. Other authors consider the three species to be synonymous [26,72].
The prey preference of Cyphoma gibbosum varies across different areas in the Caribbean. For example, whereas Pseudoplexaura corals were commonly predated by the snail in Puerto Rico [7], they were rarely predated in Florida [78]. Some species are never eaten by Cyphoma species; the reason for this is unclear but could be related to anti-predatory toxins. Octocorals have developed allelochemicals to protect against predation, and C. gibbosum has developed detoxifying enzymes to neutralise these chemical toxins [108]. Some have suggested that octocorals avoided by C. gibbosum may have other secondary metabolites that the snails cannot break down [78]. Local outbreaks are known to cause considerable damage to octocoral populations [41,109].
The three corallivores of the present study were encountered on a range of food sources, which differed strongly between the species (Figure 5 and Figure 6). The difference in utilisation of coral species was found to be statistically significant, also when only comparing the two predators on octocorals. This shows that in an area where multiple related food taxa are available to a generalist predator, food preferences arise, which may prevent competition between species. The process by which natural selection drives competing species into different patterns of resource use or different niches is called niche partitioning [110]. These differences may perhaps be caused by differences in secondary metabolites produced by the prey species, their sclerite size, or nutritional value [26].
The size of the coral was not a significant predictor in the number of snails found on a coral. Potkamp et al. [94] found that larger colonies were more likely to contain Coralliophila snails, and that the snails were generally absent on small coral colonies. This was most obvious at 5 m depth, where small colonies with a diameter of <35 cm did not contain snails. The smallest diameter of Orbicella annularis on which we recorded Coralliophila snails was 20 cm, so this is likely to be similar in Bonaire.
The aim of this survey was to obtain quantitative data on corallivorous snails. Due to the limited time, corals without snails were not identified and measured, so that we could spend more time looking for snails and get more data on host preference. A downside to this approach is that we cannot quantify snail densities and their effects, and because we have not recorded coral densities, we cannot relate snail numbers per host to the density of that host. For example, octocorals were more common on reef flats than on reef slopes, and consequently, corallivorous species associating with gorgonians are also expected to be more common in shallower waters. Nonetheless, the present study provides a baseline on knowledge of corallivorous molluscs on Bonaire, which may assist in future management strategies [111].

5. Conclusions

This study on corallivorous snails contributes to the knowledge on marine diversity of Bonaire’s coral reefs. Even though the three snail species of this study showed much overlap in their spatial distributions, there was modest similarity in their diets and there were no signs of much damage or even mortality among the corals. The snails did not show outbreaks and the reefs of Bonaire appeared not to be threatened by their presence. An earlier study on the adjacent island of Curacao showed much more overlap in dietary overlap. The lack of Cyphoma gibbosum records around the capital Kralendijk suggests that this species could be negatively affected by the anthropogenic disturbances here [112]. Subsequent research needs to investigate whether species richness near Kralendijk is also less for other taxa. It seems that coral reefs of Bonaire are currently not under much stress from corallivorous molluscs. Because these species have occasionally been reported to occur as outbreaks in other Caribbean localities and may act as vectors in the dispersal of coral diseases, it is recommended that future studies should focus on their population dynamics.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d15010034/s1, Figure S1 Location of the 28 study sites. Table S1 Locality names and coordinates. Tables S2–S4 Raw data.

Author Contributions

Conceptualization, L.V. and B.W.H.; methodology, L.V. and B.W.H.; investigation, L.V.; resources, L.V. and B.W.H.; data curation, L.V.; writing—original draft preparation, L.V. and B.W.H.; writing—review and editing, L.V. and B.W.H.; visualization, L.V. and B.W.H.; supervision, B.W.H.; project administration, B.W.H.; funding acquisition, B.W.H. All authors have read and agreed to the published version of the manuscript.

Funding

Fieldwork on Bonaire was supported by a biodiversity research grant from the World Wildlife Fund Netherlands (WNF), the Treub Maatschappij (Society for the Advancement of Research in the Tropics), and the Jan Joost ter Pelkwijk Fund.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data supporting the findings of this study are available as Electronic Supplementary Data of this article.

Acknowledgments

We are grateful to the funding agencies mentioned above. We thank the staff of Stichting Nationale Parken Bonaire (STINAPA), and the Bonaire and Dutch Caribbean Nature Alliance (DCNA) for assistance in the application of the research permit. Dive Friends (Bonaire) and Budget Car Rental provided logistic support. The authors would like to thank the other expedition members of the Bonaire Marine Biodiversity Expedition (2019) for their companionship and help. We thank Dive Friends (Bonaire) and Budget Car Rental for logistic support. We thank four reviewers for their constructive comments, which helped us to improve the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Reaka-Kudla, M.L. Biodiversity of Caribbean coral reefs. In Caribbean Marine Biodiversity: The Known and the Unknown; Miloslavich, P., Klein, E., Eds.; DEStech Publishers: Lancaster, PA, USA, 2005; pp. 259–276. [Google Scholar]
  2. Miloslavich, P.; Díaz, J.M.; Klein, E.; Alvarado, J.J.; Díaz, C.; Gobin, J.; Escobar-Briones, E.; Cruz-Motta, J.J.; Weil, E.; Cortés, J.; et al. Marine biodiversity in the Caribbean: Regional estimates and distribution patterns. PLoS ONE 2010, 5, e11916. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. DeVantier, L.; Turak, E.; Szava-Kovats, R. Species richness and abundance of reef-building corals in the Indo-West Pacific: The local–regional relation revisited. Front. Mar. Sci. 2020, 7, 487. [Google Scholar] [CrossRef]
  4. Stella, J.S.; Pratchett, M.S.; Hutchings, P.A.; Jones, G.P. Coral-associated invertebrates: Diversity, ecological importance and vulnerability to disturbance. Oceanogr. Mar. Biol. Annu. Rev. 2011, 49, 43–104. [Google Scholar]
  5. Hoeksema, B.W.; van der Meij, S.E.T.; Fransen, C.H.J.M. The mushroom coral as a habitat. J. Mar. Biol. Assoc. U. K. 2012, 92, 647–663. [Google Scholar] [CrossRef] [Green Version]
  6. Nützel, A. Gastropods as parasites and carnivorous grazers: A major guild in marine ecosystems. In The Evolution and Fossil Record of Parasitism; De Baets, K., Huntley, J.W., Eds.; Springer: Cham, Switzerland, 2021; pp. 209–229. [Google Scholar] [CrossRef]
  7. Lucas, M.Q.; Rodríguez, L.R.; Sanabria, D.J.; Weil, E. Natural prey preferences and spatial variability of predation pressure by Cyphoma gibbosum (Mollusca: Gastropoda) on octocoral communities off La Parguera, Puerto Rico. Int. Sch. Res. Notices 2014, 2014, 742387. [Google Scholar] [CrossRef] [Green Version]
  8. Pinto, T.K.; Benevides, L.J.; Sampaio, C.L.S. Cyphoma macumba Petuch 1979 (Gastropoda: Ovulidae): A versatile predator of the Brazilian Octocorallia. Mar. Biodivers. 2017, 47, 165–166. [Google Scholar] [CrossRef]
  9. Shaver, E.C.; Renzi, J.J.; Bucher, M.G.; Silliman, B.R. Relationships between a common Caribbean corallivorous snail and protected area status, coral cover, and predator abundance. Sci. Rep. 2020, 10, 16463. [Google Scholar] [CrossRef]
  10. Gittenberger, A.; Hoeksema, B.W. Habitat preferences of coral-associated wentletrap snails (Gastropoda: Epitoniidae). Contrib. Zool. 2013, 82, 1–25. [Google Scholar] [CrossRef] [Green Version]
  11. Hoeksema, B.W.; Scott, C.; True, J.D. Dietary shift in corallivorous Drupella snails following a major bleaching event at Koh Tao, Gulf of Thailand. Coral Reefs 2013, 32, 423–428. [Google Scholar] [CrossRef]
  12. Potkamp, G.; Vermeij, M.J.A.; Hoeksema, B.W. Genetic and morphological variation in corallivorous snails (Coralliophila spp.) living on different host corals at Curaçao, southern Caribbean. Contrib. Zool. 2017, 86, 111–144. [Google Scholar] [CrossRef]
  13. Kaullysing, D.; Taleb-Hossenkhan, N.; Kulkarni, B.; Bhagooli, R. Variations in the density of two ectoparasitic gastropods (Coralliophila spp.) on scleractinian corals on a coast-reef scale. Symbiosis 2019, 78, 65–71. [Google Scholar] [CrossRef]
  14. Moerland, M.S.; Scott, C.M.; Hoeksema, B.W. Prey selection of corallivorous muricids at Koh Tao (Gulf of Thailand) four years after a major coral bleaching event. Contrib. Zool. 2016, 85, 291–309. [Google Scholar] [CrossRef] [Green Version]
  15. Saponari, L.; Dehnert, I.; Galli, P.; Montano, S. Assessing population collapse of Drupella spp. (Mollusca: Gastropoda) 2 years after a coral bleaching event in the Republic of Maldives. Hydrobiologia 2021, 848, 2653–2666. [Google Scholar] [CrossRef]
  16. Sánchez, J.A. Remarkable specialization in Eastern Pacific sea fan ectoparasites (Neosimnia). Coral Reefs 2013, 32, 891. [Google Scholar] [CrossRef] [Green Version]
  17. Sánchez, J.A.; Fuentes-Pardo, A.P.; Almhain, Í.N.; Ardila-Espitia, N.E.; Cantera-Kintz, J.; Forero-Shelton, M. The masquerade game: Marine mimicry adaptation between egg-cowries and octocorals. PeerJ 2016, 4, e2051. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Gittenberger, A.; Gittenberger, E. A hitherto unnoticed adaptive radiation: Epitoniid species (Gastropoda: Epitoniidae) associated with corals (Scleractinia). Contrib. Zool. 2005, 74, 125–203. [Google Scholar] [CrossRef] [Green Version]
  19. Oliverio, M. Coralliophilinae (Neogastropoda: Muricidae) from the southwest Pacific. Mem. Mus. Natl. Hist. Nat. 2008, 196, 481–585. [Google Scholar]
  20. Taviani, M.; Angeletti, L.; Dimech, M.; Mifsud, C.; Freiwald, A.; Harasewych, M.G.; Oliverio, M. Coralliophilinae (Gastropoda: Muricidae) associated with deep-water coral banks in the Mediterranean. Nautilus 2009, 123, 106–112. [Google Scholar]
  21. Claremont, M.; Houart, R.; Williams, S.T.; Reid, D.G. A molecular phylogenetic framework for the Ergalataxinae (Neogastropoda: Muricidae). J. Mollusc. Stud. 2013, 79, 19–29. [Google Scholar] [CrossRef] [Green Version]
  22. Goud, J.; Hoeksema, B.W. Pedicularia vanderlandi spec. nov., a symbiotic snail (Caenogastropoda: Ovulidae) on the hydrocoral Distichopora vervoorti Cairns and Hoeksema, 1998 (Hydrozoa: Stylasteridae), from Bali, Indonesia. Zool. Verh. 2001, 334, 77–97. [Google Scholar]
  23. Lorenz, F.; Fehse, D. The Living Ovulidae. A Manual of the Families of Allied Cowries: Ovulidae, Pediculariidae and Eocypraeidae; Conchbooks: Hackenheim, Germany, 2009. [Google Scholar]
  24. Braga-Henriques, A.; Carreiro-Silva, M.; Porteiro, F.M.; de Matos, V.; Sampaio, Í.; Ocaña, O.; Avila, S.P. The association between a deep-sea gastropod Pedicularia sicula (Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa: Stylasteridae) in the Azores. ICES J. Mar. Sci. 2011, 68, 399–407. [Google Scholar] [CrossRef] [Green Version]
  25. Schiaparelli, S.; Barucca, M.; Olmo, E.; Boyer, M.; Canapa, A. Phylogenetic relationships within Ovulidae (Gastropoda: Cypraeoidea) based on molecular data from the 16S rRNA gene. Mar. Biol. 2005, 147, 411–420. [Google Scholar] [CrossRef]
  26. Reijnen, B.T.; Hoeksema, B.W.; Gittenberger, E. Host specificity and phylogenetic relationships among Atlantic Ovulidae (Mollusca: Gastropoda). Contrib. Zool. 2010, 79, 69–78. [Google Scholar] [CrossRef]
  27. Fritts-Penniman, A.L.; Gosliner, T.M.; Mahardika, G.N.; Barber, P.H. Cryptic ecological and geographic diversification in coral-associated nudibranchs. Mol. Phylogenet. Evol. 2020, 144, 106698. [Google Scholar] [CrossRef]
  28. Mehrotra, R.; Arnold, S.; Wang, A.; Chavanich, S.; Hoeksema, B.W.; Caballer, M. A new species of coral-feeding nudibranch (Mollusca: Gastropoda) from the Gulf of Thailand. Mar. Biodivers. 2020, 50, 36. [Google Scholar] [CrossRef]
  29. Wang, A.; Conti-Jerpe, I.E.; Richards, J.L.; Baker, D.M. Phestilla subodiosus sp. nov. (Nudibranchia, Trinchesiidae), a corallivorous pest species in the aquarium trade. ZooKeys 2020, 909, 35278. [Google Scholar] [CrossRef]
  30. Yiu, S.K.F.; Chung, S.S.W.; Qiu, J.W. New observations on the corallivorous nudibranch Phestilla melanobrachia: Morphology, dietary spectrum and early development. J. Mollusc. Stud. 2021, 87, eyab034. [Google Scholar] [CrossRef]
  31. Hoeksema, B.W.; Gittenberger, A. Records of some marine parasitic molluscs from Nha Trang, Vietnam. Basteria 2008, 72, 129–133. [Google Scholar]
  32. Gittenberger, A.; Gittenberger, E. Cryptic, adaptive radiation of endoparasitic snails: Sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Org. Divers. Evol. 2011, 11, 21–41. [Google Scholar] [CrossRef] [Green Version]
  33. Bieler, R.; Petit, R.E. Catalogue of Recent and fossil “worm-snail” taxa of the families Vermetidae, Siliquariidae, and Turritellidae (Mollusca: Caenogastropoda). Zootaxa 2011, 2948, 1–103. [Google Scholar] [CrossRef] [Green Version]
  34. Hoeksema, B.W.; Harper, C.E.; Langdon-Down, S.J.; van der Schoot, R.J.; Smith-Moorhouse, A.; Spaargaren, R.; Timmerman, R.F. Host range of the coral-associated worm snail Petaloconchus sp. (Gastropoda: Vermetidae), a newly discovered cryptogenic pest species in the southern Caribbean. Diversity 2022, 14, 196. [Google Scholar] [CrossRef]
  35. Knowlton, N.; Lang, J.C.; Keller, B.D. Case study of natural population collapse: Post-hurricane predation on Jamaican staghorn corals. Smithson. Contrib. Mar. Sci. 1990, 31, 1–25. [Google Scholar] [CrossRef]
  36. Bruckner, A.W.; Bruckner, R.J. Mechanical lesions and corallivory. In Diseases of Coral; Woodley, C.M., Downs, C.A., Bruckner, A.W., Porter, J.W., Galloway, S.B., Eds.; John Wiley & Sons: Hoboken, NJ, USA, 2016; pp. 242–265. [Google Scholar] [CrossRef]
  37. Scott, C.M.; Mehrotra, R.; Hein, M.Y.; Moerland, M.S.; Hoeksema, B.W. Population dynamics of corallivores (Drupella and Acanthaster) on coral reefs of Koh Tao, a diving destination in the Gulf of Thailand. Raffles Bull. Zool. 2017, 65, 68–79. [Google Scholar]
  38. Boucher, L.M. Coral predation by muricid gastropods of the genus Drupella at Enewetak, Marshall Islands. Bull. Mar. Sci. 1986, 38, 9–11. [Google Scholar]
  39. Cumming, R.; McCorry, D. Corallivorous gastropods in Hong Kong. Coral Reefs 1998, 17, 178. [Google Scholar] [CrossRef]
  40. Cumming, R.L. Predation on reef-building corals: Multiscale variation in the density of three corallivorous gastropods, Drupella spp. Coral Reefs 1999, 18, 147–157. [Google Scholar] [CrossRef]
  41. Schärer, M.T.; Nemeth, M.I. Mass mortality of gorgonians due to a Cyphoma gibbosum (Linnaeus) population outbreak at Mona Island, Puerto Rico. Coral Reefs 2010, 29, 533. [Google Scholar] [CrossRef] [Green Version]
  42. Bessey, C.; Babcock, R.C.; Thomson, D.P.; Haywood, M.D.E. Outbreak densities of the coral predator Drupella in relation to in situ Acropora growth rates on Ningaloo Reef, Western Australia. Coral Reefs 2018, 37, 985–993. [Google Scholar] [CrossRef]
  43. Bruckner, A.W.; Coward, G.; Bimson, K.; Rattanawongwan, T. Predation by feeding aggregations of Drupella spp. inhibits the recovery of reefs damaged by a mass bleaching event. Coral Reefs 2017, 36, 1181–1187. [Google Scholar] [CrossRef]
  44. Hamman, E.A. Aggregation patterns of two corallivorous snails and consequences for coral dynamics. Coral Reefs 2018, 37, 851–860. [Google Scholar] [CrossRef]
  45. Dalton, S.J.; Godwin, S. Progressive coral tissue mortality following predation by a corallivorous nudibranch (Phestilla sp.). Coral Reefs 2006, 25, 529. [Google Scholar] [CrossRef]
  46. Gignoux-Wolfsohn, S.; Marks, C.; Vollmer, S. White Band Disease transmission in the threatened coral, Acropora cervicornis. Sci. Rep. 2012, 2, 804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Raymundo, L.J.; Work, T.M.; Miller, R.L.; Lozada-Misa, P.L. Effects of Coralliophila violacea on tissue loss in the scleractinian corals Porites spp. depend on host response. Dis. Aquat. Organ. 2016, 119, 75–83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Nicolet, K.J.; Chong-Seng, K.M.; Pratchett, M.S.; Willis, B.L.; Hoogenboom, M.O. Predation scars may influence host susceptibility to pathogens: Evaluating the role of corallivores as vectors of coral disease. Sci. Rep. 2018, 8, 5258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Montano, S.; Aeby, G.; Galli, P.; Hoeksema, B.W. Feeding behavior of Coralliophila sp. on corals affected by Caribbean ciliate infection (CCI): A new possible vector? Diversity 2022, 14, 363. [Google Scholar] [CrossRef]
  50. Thur, S.M. User fees as sustainable financing mechanisms for marine protected areas: An application to the Bonaire National Marine Park. Mar. Policy 2010, 34, 63–69. [Google Scholar] [CrossRef]
  51. Trembanis, A.C.; Forrest, A.L.; Keller, B.M.; Patterson, M.R. Mesophotic coral ecosystems: A geoacoustically derived proxy for habitat and relative diversity for the leeward shelf of Bonaire, Dutch Caribbean. Front. Mar. Sci. 2017, 4, 51. [Google Scholar] [CrossRef] [Green Version]
  52. Bak, R.P.M.; Nieuwland, G.; Meesters, E.H. Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curaçao and Bonaire. Coral Reefs 2005, 24, 475–479. [Google Scholar] [CrossRef]
  53. Stokes, M.D.; Leichter, J.J.; Genovese, S.J. Long-term declines in coral cover at Bonaire, Netherlands Antilles. Atoll Res. Bull. 2010, 582, 1–21. [Google Scholar] [CrossRef]
  54. de Bakker, D.M.; Meesters, E.H.; Bak, R.P.M.; Nieuwland, G.; van Duyl, F.C. Long-term shifts in coral communities on shallow to deep reef slopes of Curaçao and Bonaire: Are there any winners? Front. Mar. Sci. 2016, 3, 247. [Google Scholar] [CrossRef] [Green Version]
  55. de Bakker, D.M.; van Duyl, F.C.; Bak, R.P.M.; Nugues, M.M.; Nieuwland, G.; Meesters, E.H. 40 years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: The rise of slimy cyanobacterial mats. Coral Reefs 2017, 36, 355–367. [Google Scholar] [CrossRef] [Green Version]
  56. Hoeksema, B.W. (Ed.) Marine Biodiversity of Bonaire: A Baseline Survey, 2nd ed.; Naturalis Biodiversity Center: Leiden, The Netherlands; ANEMOON Foundation: Bennebroek, The Netherlands, 2022. [Google Scholar]
  57. García-Hernández, J.E.; de Gier, W.; van Moorsel, G.W.N.M.; Hoeksema, B.W. The scleractinian Agaricia undata as a new host for the Caribbean coral gall crab Opecarcinus hypostegus at Bonaire, southern Caribbean. Symbiosis 2020, 81, 303–311. [Google Scholar] [CrossRef]
  58. Hoeksema, B.W.; García-Hernández, J.E. Host-related morphological variation of dwellings inhabited by the crab Domecia acanthophora in the corals Acropora palmata and Millepora complanata (Southern Caribbean). Diversity 2020, 12, 143. [Google Scholar] [CrossRef] [Green Version]
  59. Hoeksema, B.W.; García-Hernández, J.E.; van Moorsel, G.W.N.M.; Olthof, G.; ten Hove, H.A. Extension of the recorded host range of Caribbean Christmas tree worms (Spirobranchus spp.) with two scleractinians, a zoantharian, and an ascidian. Diversity 2020, 12, 115. [Google Scholar] [CrossRef] [Green Version]
  60. Hoeksema, B.W.; Timmerman, R.F.; Spaargaren, R.; Smith-Moorhouse, A.; van der Schoot, R.J.; Langdon-Down, S.J.; Harper, C.E. Morphological modifications and injuries of corals caused by symbiotic feather duster worms (Sabellidae) in the Caribbean. Diversity 2022, 14, 332. [Google Scholar] [CrossRef]
  61. Korzhavina, O.A.; Hoeksema, B.W.; Ivanenko, V.N. A review of Caribbean Copepoda associated with reef-dwelling cnidarians, echinoderms and sponges. Contrib. Zool. 2019, 88, 297–349. [Google Scholar] [CrossRef] [Green Version]
  62. Montano, S.; Reimer, J.D.; Ivanenko, V.N.; García-Hernández, J.E.; van Moorsel, G.W.N.M.; Galli, P.; Hoeksema, B.W. Widespread occurrence of a rarely known association between the hydrocorals Stylaster roseus and Millepora alcicornis at Bonaire, southern Caribbean. Diversity 2020, 12, 218. [Google Scholar] [CrossRef]
  63. Montenegro, J.; Hoeksema, B.W.; Santos, M.E.A.; Kise, H.; Reimer, J.D. Zoantharia (Cnidaria: Hexacorallia) of the Dutch Caribbean with historical distribution records from the Atlantic and one new species of Parazoanthus. Diversity 2020, 12, 190. [Google Scholar] [CrossRef]
  64. Reimer, J.D.; Wee, H.B.; García-Hernández, J.E.; Hoeksema, B.W. Same but different? Zoantharian assemblages (Anthozoa: Hexacorallia: Zoantharia) in Bonaire and Curaçao, southern Caribbean. Coral Reefs 2022, 41, 383–396. [Google Scholar] [CrossRef]
  65. Rotjan, R.D.; Lewis, S.M. Impact of coral predators on tropical reefs. Mar. Ecol. Prog. Ser. 2008, 367, 73–91. [Google Scholar] [CrossRef]
  66. Miller, M. Corallivorous snail removal: Evaluation of impact on Acropora palmata. Coral Reefs 2001, 19, 293–295. [Google Scholar] [CrossRef]
  67. Precht, W.; Bruckner, A.; Aronson, R.; Bruckner, R. Endangered acroporid corals of the Caribbean. Coral Reefs 2002, 21, 41–42. [Google Scholar] [CrossRef]
  68. Garrigues, B.; Lamy, D.; Zuccon, D. The Coralliophilinae from the Antilles and French Guiana with the description of six new species. Xenophora Taxon. 2022, 37, 4–53. [Google Scholar]
  69. Johnston, L.; Miller, M.W. Variation in life-history traits of the corallivorous gastropod Coralliophila abbreviata on three coral hosts. Mar. Biol. 2007, 150, 1215–1225. [Google Scholar] [CrossRef]
  70. Johnston, L.; Miller, M.W.; Baums, I.B. Assessment of host-associated genetic differentiation among phenotypically divergent populations of a coral-eating gastropod across the Caribbean. PLoS ONE 2012, 7, e47630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  71. Simmonds, S.E.; Chou, V.; Cheng, S.H.; Rachmawati, R.; Calumpong, H.P.; Ngurah Mahardika, G.; Barber, P.H. Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle. Coral Reefs 2018, 37, 355–371. [Google Scholar] [CrossRef]
  72. Miller, A.C. Observations on the associations and feeding of six species of prosobranch gastropods on anthozoans. Atoll Res. Bull. 1972, 152, 4–5. [Google Scholar]
  73. Martin, D.; Gil, J.; Abgarian, C.; Evans, E.; Turner, E.M.; Nygren, A. Coralliophila from Grand Cayman: Specialized coral predator or parasite? Coral Reefs 2014, 33, 1017. [Google Scholar] [CrossRef] [Green Version]
  74. Ott, B.; Lewis, J.B. The importance of the gastropod Coralliophila abbreviata (Lamarck) and the polychaete Hermodice carunculata (Pallas) as coral reef predators. Can. J. Zool. 1972, 50, 1651–1656. [Google Scholar] [CrossRef]
  75. Reijnen, B.T.; van der Meij, S.E.T. Coat of many colours-DNA reveals polymorphism of mantle patterns and colouration in Caribbean Cyphoma Röding, 1798 (Gastropoda, Ovulidae). PeerJ 2017, 5, e3018. [Google Scholar] [CrossRef] [Green Version]
  76. Lorenz, F. The “Black Morph Cyphoma” from the Netherlands Antilles (Gastropoda: Ovulidae). Acta Conchyl. 2020, 19, 69–75. [Google Scholar]
  77. Nowlis, J.P. Mate-and oviposition-influenced host preferences in the coral-feeding snail Cyphoma gibbosum. Ecology 1993, 74, 1959–1969. [Google Scholar] [CrossRef]
  78. Chiappone, M.; Dienes, H.; Swanson, D.W.; Miller, S.L. Density and Gorgonian host-occupation patterns by Flamingo Tongue snails (Cyphoma gibbosum) in the Florida keys. Caribb. J. Sci. 2003, 39, 116–127. [Google Scholar]
  79. Lasker, H.R.; Coffroth, M.A.; Fitzgerald, L.M. Foraging patterns of Cyphoma gibbosum on octocorals: The roles of host choice and feeding preference. Biol. Bull. 1988, 174, 254–266. [Google Scholar] [CrossRef]
  80. Hoeksema, B.W.; Koh, E.G.L. Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s–2006) in changing reef conditions. Raffles Bull. Zool. Suppl. 2009, 22, 91–101. [Google Scholar]
  81. Ruesink, J.L.; Harvell, C.D. Specialist predation on the Caribbean gorgonian Plexaurella spp. by Cyphoma signatum (Gastropoda). Mar. Ecol. Prog. Ser. 1990, 65, 265–272. [Google Scholar] [CrossRef]
  82. Humann, P.; Deloach, N. Reef Coral Identification: Florida, the Caribbean and the Bahamas, 3rd ed.; New World Publications Inc.: Jacksonville, FL, USA, 2013. [Google Scholar]
  83. Hoeksema, B.W.; van der Loos, L.M.; van Moorsel, G.W.N.M. Coral diversity matches marine park zonation but not economic value of coral reef sites at St. Eustatius, eastern Caribbean. J. Environ. Manag. 2022, 320, 115829. [Google Scholar] [CrossRef]
  84. Bayer, F.M. The shallow-water Octocorallia of the West Indian region. Stud. Fauna Curaçao Caribb. Isl. 1961, 12, 506065. [Google Scholar]
  85. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2022; Available online: https://www.r-project.org/ (accessed on 11 September 2022).
  86. Dormann, C.F.; Gruber, B.; Fründ, J. Introducing the bipartite Package: Analysing Ecological Networks. R News 2008, 8, 8–11. [Google Scholar]
  87. Dormann, C.F.; Fruend, J.; Gruber, B.; Beckett, S.; Devoto, M.; Felix, G.M.F.; Iriondo, J.M.; Opsahl, T.; Pinheiro, R.B.P.; Strauss, R.; et al. Visualising Bipartite Networks and Calculating Some (Ecological) Indices. 2022. Available online: https://github.com/biometry/bipartite (accessed on 11 September 2022).
  88. Pavlopoulos, G.A.; Kontou, P.I.; Pavlopoulou, A.; Bouyioukos, C.; Markou, E.; Bagos, P.G. Bipartite graphs in systems biology and medicine: A survey of methods and applications. GigaScience 2018, 7, giy014. [Google Scholar] [CrossRef]
  89. Coker, D.J.; DiBattista, J.D.; Stat, M.; Arrigoni, R.; Reimer, J.; Terraneo, T.I.; Villabos, R.; Nowicki, J.P.; Bunce, M.; Berumen, M.L. DNA metabarcoding confirms primary targets and breadth of diet for coral reef butterflyfishes. Coral Reefs 2022, in press. [Google Scholar] [CrossRef]
  90. Blüthgen, N.; Menzel, F.; Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol. 2006, 6, 9. [Google Scholar] [CrossRef]
  91. Brawley, S.H.; Adey, W.H. Coralliophila abbreviata: A significant corallivore! Bull. Mar. Sci. 1982, 32, 595–599. [Google Scholar]
  92. Frade, P.R.; Bongaerts, P.; Baldwin, C.C.; Trembanis, A.C.; Bak, R.P.M.; Vermeij, M.J.A. Bonaire and Curaçao. In Mesophotic Coral Ecosystems. Coral Reefs of the World; Loya, Y., Puglise, K., Bridge, T., Eds.; Springer: Cham, Switzerland, 2019; Volume 12, pp. 149–162. [Google Scholar] [CrossRef]
  93. Bongaerts, P.; Ridgway, T.; Sampayo, E.M.; Hoegh-Guldberg, O. Assessing the ‘deep reef refugia’ hypothesis: Focus on Caribbean reefs. Coral Reefs 2010, 29, 309–327. [Google Scholar] [CrossRef]
  94. Potkamp, G.; Vermeij, M.J.A.; Hoeksema, B.W. Host-dependent variation in density of corallivorous snails (Coralliophila spp.) at Curaçao, southern Caribbean. Mar. Biodivers. 2017, 47, 91–99. [Google Scholar] [CrossRef] [Green Version]
  95. Hayes, J.A. Distribution, movement and impact of the corallivorous gastropod Coralliophila abbreviata (Lamarck) on a Panamánian patch reef. J. Exp. Mar. Biol. Ecol. 1990, 142, 25–42. [Google Scholar] [CrossRef]
  96. Baums, I.B.; Miller, M.W.; Szmant, A.M. Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two seleractinian hosts. II. Feeding, respiration and growth. Mar. Biol. 2003, 142, 1093–1101. [Google Scholar] [CrossRef]
  97. Van der Schoot, R.J.; Hoeksema, B.W. Abundance of coral-associated fauna in relation to depth and eutrophication along the leeward side of Curaçao, southern Caribbean. Mar. Environ. Res. 2022, 181, 105738. [Google Scholar] [CrossRef]
  98. Bruckner, A.; Bruckner, R. Condition of restored Acropora palmata fragments off Mona Island, Puerto Rico, 2 years after the Fortuna Reefer ship grounding. Coral Reefs 2001, 20, 235–243. [Google Scholar] [CrossRef]
  99. Williams, D.E.; Miller, M.W. Attributing mortality among drivers of population decline in Acropora palmata in the Florida Keys (USA). Coral Reefs 2012, 31, 369–382. [Google Scholar] [CrossRef]
  100. Bright, A.J.; Rogers, C.S.; Brandt, M.E.; Muller, E.; Smith, T.B. Disease prevalence and snail predation associated with swell-generated damage on the threatened coral, Acropora palmata (Lamarck). Front. Mar. Sci. 2016, 3, 77. [Google Scholar] [CrossRef] [Green Version]
  101. Queiroz, V.; Sales, L.; Neves, E.; Johnsson, R. Siderastrea stellata Verrill, 1868 as a new host for the corallivore snail Coralliophila caribaea Abbott, 1958 and some biological aspects of their association. Spixiana 2021, 44, 17–18. [Google Scholar]
  102. Del Mónaco, C.; Villamiza, E.; Narciso, S. Selectividad de presas de Coralliophila abbreviata y C. caribaea en arrecifes coralinos del Parque Nacional Morrocoy, Venezuela: Una aproximación experimental. Lat. Am. J. Aquat. Res. 2010, 38, 57–70. [Google Scholar] [CrossRef]
  103. Miller, A.C. Cnidarian prey of the snails Coralliophila abbreviata and C. caribaea (Gastropoda: Muricidae) in Discovery Bay, Jamaica. Bull. Mar. Sci. 1981, 31, 932–934. [Google Scholar]
  104. Oren, U.; Brickner, I.; Loya, Y. Prudent sessile feeding by the corallivore snail, Coralliophila violacea on coral energy sinks. Proc. R. Soc. B 1998, 265, 2043–2050. [Google Scholar] [CrossRef] [Green Version]
  105. Clements, C.S.; Hay, M.E. Overlooked coral predators suppress foundation species as reefs degrade. Ecol. Appl. 2018, 28, 1673–1682. [Google Scholar] [CrossRef]
  106. Hoeksema, B.W.; García-Hernández, J.E. Diversity and distribution of stony corals. In Marine Biodiversity of Bonaire: A Baseline Study, 2nd ed.; Hoeksema, B.W., Ed.; Naturalis Biodiversity Center: Leiden, The Netherlands, 2022; pp. 17–19. [Google Scholar]
  107. De Jong, K.M.; Coomans, H.E. Marine gastropods from Curaçao, Aruba and Bonaire. Stud. Fauna Curaçao Caribb. Isl. 1988, 69, 1–261. Available online: https://repository.naturalis.nl/pub/506113 (accessed on 11 September 2022).
  108. Whalen, K.E.; Starczak, V.R.; Nelson, D.R.; Goldstone, J.V.; Hahn, M.E. Cytochrome P450 diversity and induction by gorgonian allelochemicals in the marine gastropod Cyphoma gibbosum. BMC Ecol. 2010, 10, 24. [Google Scholar] [CrossRef] [Green Version]
  109. Williams, E.H.; Bunkley-Williams, L. Marine major ecological disturbances of the Caribbean. Infect. Dis. Rev. 2000, 2, 110–127. [Google Scholar]
  110. Hector, A.; Hooper, R. Ecology: Darwin and the first ecological experiment. Science 2002, 295, 639–640. [Google Scholar] [CrossRef]
  111. Shaver, E.C.; Burkepile, D.E.; Silliman, B.R. Local management actions can increase coral resilience to thermally-induced bleaching. Nat. Ecol. Evol. 2018, 2, 1075–1079. [Google Scholar] [CrossRef] [PubMed]
  112. De Bakker, D.M.; van Duyl, F.C.; Perry, C.T.; Meesters, E.H. Extreme spatial heterogeneity in carbonate accretion potential on a Caribbean fringing reef linked to local human disturbance gradients. Glob. Change Biol. 2019, 25, 4092–4104. [Google Scholar] [CrossRef] [PubMed]
Diversity 15 00034 g001 550
Figure 1. The three corallivorous snails encountered on Bonaire: (a) Coralliophila galea; (b) Coralliophila salebrosa; (c) Cyphoma gibbosum.
Figure 1. The three corallivorous snails encountered on Bonaire: (a) Coralliophila galea; (b) Coralliophila salebrosa; (c) Cyphoma gibbosum.
Diversity 15 00034 g001
Diversity 15 00034 g002 550
Figure 2. Distribution of three corallivorous snail species at 28 localities around Bonaire.
Figure 2. Distribution of three corallivorous snail species at 28 localities around Bonaire.
Diversity 15 00034 g002
Diversity 15 00034 g003 550
Figure 3. Bipartite network showing the associations between predator species (left side) and the host-coral species (right side: red = scleractinians; yellow = octocorals). The width of the grey lines represents the number of snails found per association. Coralliophila sp. is an unidentified snail.
Figure 3. Bipartite network showing the associations between predator species (left side) and the host-coral species (right side: red = scleractinians; yellow = octocorals). The width of the grey lines represents the number of snails found per association. Coralliophila sp. is an unidentified snail.
Diversity 15 00034 g003
Diversity 15 00034 g004 550
Figure 4. Interspecific relations of corallivorous snails and their host species by PCA. Each data point is an observation. Components: depth, coral size, number of snails, locality coordinates. (a) Snails species and environmental variables; (b–d) Snail species with their host corals.
Figure 4. Interspecific relations of corallivorous snails and their host species by PCA. Each data point is an observation. Components: depth, coral size, number of snails, locality coordinates. (a) Snails species and environmental variables; (b–d) Snail species with their host corals.
Diversity 15 00034 g004
Diversity 15 00034 g005 550
Figure 5. Linear regression of snail numbers and coral size for three snails species. Each dot represents an observation of a snail colony on a coral. For Coralliophila galea, the red points indicate observations on the coral species Orbicella annularis. The correlations are not significant.
Figure 5. Linear regression of snail numbers and coral size for three snails species. Each dot represents an observation of a snail colony on a coral. For Coralliophila galea, the red points indicate observations on the coral species Orbicella annularis. The correlations are not significant.
Diversity 15 00034 g005
Diversity 15 00034 g006 550
Figure 6. Box plot comparing the depth distributions for the different snail species. Interspecific variation is significant (ANOVA: F = 5.27; p < 0.05) but differences between any two species are not.
Figure 6. Box plot comparing the depth distributions for the different snail species. Interspecific variation is significant (ANOVA: F = 5.27; p < 0.05) but differences between any two species are not.
Diversity 15 00034 g006
Diversity 15 00034 g007 550
Figure 7. Host utilization by Coralliophila galea in three depth ranges.
Figure 7. Host utilization by Coralliophila galea in three depth ranges.
Diversity 15 00034 g007
Table
Table 1. Host corals of corallivorous gastropods on Bonaire. The total number of associated snails is shown with the number of host corals in brackets. Coralliophila sp. is an unidentified snail.
Table 1. Host corals of corallivorous gastropods on Bonaire. The total number of associated snails is shown with the number of host corals in brackets. Coralliophila sp. is an unidentified snail.
Snail Species
Host Coral TaxaCoralliophila galeaCoralliophila salebrosaCoralliophila sp.Cyphoma gibbossum
Scleractinia
Acroporidae
Acropora palmata6 (1)
Agariciidae
Agaricia agaricites14 (10)
Agaricia humilis1 (1)
Agaricia lamarcki2 (2)
Meandrinidae
Eusmilia fastigiata 1 (1)
Merulinidae
Orbicella annularis500 (70)
Orbicella franksi18 (7)
Montastraeidae
Montastraea cavernosa1 (1)
Mussidae
Pseudodiploria strigosa9 (1)
Pocilloporidae
Madracis auretenra24 (8)1 (1)
Octocorallia
Gorgoniidae
Antillogorgia bipinnata 12 (7)
Antillogorgia sp. 3 (1) 6 (4)
Gorgonia ventalina 3 (2) 3 (2)
Plexauridae
Eunicea flexuosa 5 (3)
Eunicea fusca 2 (1)
Eunicea sp. 4 (3) 13 (6)
Plexaura homomalla 6 (2) 14 (4)
Pseudoplexaura sp. 17 (7) 24 (13)
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Verboom, L.; Hoeksema, B.W. Resource Partitioning by Corallivorous Snails on Bonaire (Southern Caribbean). Diversity 2023, 15, 34. https://doi.org/10.3390/d15010034

AMA Style

Verboom L, Hoeksema BW. Resource Partitioning by Corallivorous Snails on Bonaire (Southern Caribbean). Diversity. 2023; 15(1):34. https://doi.org/10.3390/d15010034

Chicago/Turabian Style

Verboom, Lukas, and Bert W. Hoeksema. 2023. "Resource Partitioning by Corallivorous Snails on Bonaire (Southern Caribbean)" Diversity 15, no. 1: 34. https://doi.org/10.3390/d15010034

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop