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Growth and Survival Reduces Coral Dendropoma Maximum The Downloaded from rsbl.royalsocietypublishing.org on May 19, 2010 The vermetid gastropod Dendropoma maximum reduces coral growth and survival Jeffrey S. Shima, Craig W. Osenberg and Adrian C. Stier Biol. Lett. published online 19 May 2010 doi: 10.1098/rsbl.2010.0291 Supplementary data "Data Supplement" http://rsbl.royalsocietypublishing.org/content/suppl/2010/05/19/rsbl.2010.0291.DC1.ht ml References This article cites 23 articles, 4 of which can be accessed free http://rsbl.royalsocietypublishing.org/content/early/2010/05/18/rsbl.2010.0291.full.html #ref-list-1 P<P Published online 19 May 2010 in advance of the print journal. Subject collections Articles on similar topics can be found in the following collections ecology (1444 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here Advance online articles have been peer reviewed and accepted for publication but have not yet appeared in the paper journal (edited, typeset versions may be posted when available prior to final publication). Advance online articles are citable and establish publication priority; they are indexed by PubMed from initial publication. Citations to Advance online articles must include the digital object identifier (DOIs) and date of initial publication. To subscribe to Biol. Lett. go to: http://rsbl.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on May 19, 2010 Biol. Lett. fishes, Cole et al. 2008) and mutualists (Pratchett doi:10.1098/rsbl.2010.0291 et al. 2000). Other studies have identified anthropo- Published online genic activities (e.g. nutrient enrichment, Bruno et al. Marine biology 2003; sedimentation, McCulloch et al. 2003; and dis- ease, Harvell et al. 2002; Bruno et al. 2003)as drivers of coral declines. These factors undoubtedly The vermetid gastropod contribute to coral dynamics in many locations and times, but given the diversity of species and biological Dendropoma maximum interactions that comprise coral reef ecosystems (and the relatively limited breadth of scientific study), it is reduces coral growth and likely that coral dynamics might be influenced by survival species interactions still unrecognized by scientists. Although coral reefs are largely known for their more Jeffrey S. Shima1,*,†, Craig W. Osenberg2,† charismatic inhabitants, many small, relatively cryptic and Adrian C. Stier2 species (e.g. small invertebrates) are potentially impor- 1School of Biological Sciences, Victoria University of Wellington, tant players but easily overlooked. For example, Wellington, New Zealand vermetid gastropods are sessile and feed via extruded 2Department of Biology, University of Florida, Gainesville, FL, USA mucus nets that often contact neighbouring substrates, *Author for correspondence ( [email protected]). including corals (Morton 1965; Hughes & Lewis †These authors contributed equally to this work. 1974). The largest vermetid, Dendropoma maximum Coral reefs are one of the most diverse systems on (see electronic supplementary material, appendix A), the planet; yet, only a small fraction of coral reef is common and widespread throughout the Indo-Pacific species have attracted scientific study. Here, we (Hadfield et al.1972; Hughes & Lewis 1974; Zvuloni document strong deleterious effects of an often et al.2008), and aspects of its feeding ecology have overlooked species—the vermetid gastropod, been examined by a number of workers (e.g. Smalley Dendropoma maximum—on growth and survi- val of reef-building corals. Our surveys of 1984; Kappner et al.2000; Ribak et al.2005; Gagern vermetids on Moorea (French Polynesia) et al.2008). In the Gulf of Aqaba (Red Sea), the pres- revealed a negative correlation between the den- ence of D. maximum was correlated with morphological sity of vermetids and the per cent cover of live anomalies and reduced size in a branching coral coral. Furthermore, the incidence of flattened (Zvuloni et al.2008). Here, we explore vermetid– coral growth forms was associated with the pres- coral interactions in more detail using a series of field ence of vermetids. We transplanted and followed observations combined with experiments designed to the fates of focal colonies of four species of quantify the degree to which vermetids cause reductions corals on natural reefs where we also manipu- in growth and survival of four coral species. lated presence/absence of vermetids. Vermetids reduced skeletal growth of focal corals by up to 81 per cent and survival by up to 52 per cent. Susceptibility to vermetids varied among coral 2. MATERIAL AND METHODS species, suggesting that vermetids could shift (a) Field surveys coral community composition. Our work high- We surveyed 90 interspersed patch reefs in a shallow (2–3 m) lagoon of Moorea, French Polynesia (17.488S and 149.818W). Each reef lights the potential importance of a poorly was comprised entirely of a single massive Porities lobata coral studied gastropod to coral dynamics. colony (see electronic supplementary material, appendix B for dis- cussion of coral taxonomy). We recorded reef morphology (binary Keywords: coral growth; coral survival; Dendropoma response variable: either ‘flattened’ or ‘rugose’, see electronic sup- maximum; vermetid gastropod plementary material, appendix A, figure A1c) from a distance of approximately 5 m (where reef morphology was apparent but the presence of vermetids was not). We then surveyed each reef under closer inspection and recorded the presence or absence of vermetids. 1. INTRODUCTION We evaluated the relationship between coral morphology and Coral reefs are biologically diverse habitats that provide vermetid presence–absence using a x2 test. important ecosystem services including coastal fish- We quantified covariation between vermetid densities and the proportion of the reef substrate that was dead (i.e. hard substrate eries, and protection against storms, tsunamis and other than live coral) in 103, 22.36 Â 22.36 cm quadrats hap- rising sea levels (Pratchett et al. 2008). Corals also hazardly placed on monotypic patches of four focal species play an important ecological function, providing bio- (electronic supplementary material, appendix B) of common reef- genic structures for many species of fishes and other building coral: Porites lobata (n ¼ 37), Pocillopora (n ¼ 26), Porites rus (n ¼ 20) and Montipora (n ¼ 20). We visually estimated the pro- invertebrates (Jones et al. 2004). However, consider- portion of coral substrate that was dead, and counted the number of able evidence suggests that the abundance and vermetids that were greater than or equal to 5 mm in aperture diam- physiological performance of reef building corals is eter (i.e. readily identifiable as D. maximum). We evaluated variation in vermetid densities among substrate types using ANOVA, and declining in many areas (Gardner et al. 2003; Bellwood relationships between the proportion of dead substrate and vermetid et al. 2006), potentially jeopardizing many of their density using least-squares linear regression. ecosystem services. Recent studies of coral dynamics have focused on a (b) Field experiments limited set of factors, including hurricanes (Woodley We conducted six field experiments to quantify the effects of verme- et al. 1981), competitors (e.g. algae: Carpenter & tid gastropods on skeletal growth and survival of four focal coral species: Porites lobata, P. r u s , Pocillopora, Montipora at a site in Mahar- Edmunds 2006; Box & Mumby 2007), conspicuous epa lagoon, and on two of these species (P. lobata and Pocillopora)at predators (e.g. crown-of-thorns sea star, Done 1992; another site (West Temae lagoon). Focal corals (juvenile P. lobata; fragments from larger colonies for other species) were attached to Electronic supplementary material is available at http://dx.doi.org/ plastic bases (approx. 10 Â 10 cm) using epoxy and weighed 10.1098/rsbl.2010.0291 or via http://rsbl.royalsocietypublishing.org. (Davies 1989). Received 25 March 2010 Accepted 28 April 2010 This journal is q 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on May 19, 2010 2 J. S. Shima et al. Vermetid–coral interactions (a)(1.0 b) 0.8 0.6 0.4 proportion dead 0.2 0 5101520012345 (c) 1.0 (d) 0.8 0.6 0.4 proportion dead 0.2 0 24680 5 10 15 vermetid density (no. per 500 cm2) vermetid density (no. per 500 cm2) Figure 1. Relationships between the local density of Dendropoma maximum (number of snails 5 mm aperture diameter in a 500 cm2 quadrat) and the proportion of that quadrat consisting of dead coral for monospecific sites consisting of (a) Porites lobata (r ¼ 0.59, p , 0.0001, n ¼ 37). (b) Pocillopora (r ¼ 0.48, p ¼ 0.01, n ¼ 26). (c) Porites rus (r ¼ 0.73, p ¼ 0.0002, n ¼ 20). (d) Montipora (r ¼ 20.01, p ¼ 0.95, n ¼ 20). 2 Our experiments were conducted on small (less than 5 m ), Table 1. Surveys of 90 interspersed colonies of the coral shallow (approx. 2 m depth) patch reefs that (initially) had local Porites lobata reveal an association between the presence or populations of the vermetid gastropod, D. maximum. We randomly selected half of the 12 study reefs within each experiment (n ¼ 6) absence of D. maximum and coral morphology. Presence of and removed vermetids. The remaining reefs comprised a control vermetid is associated with stunted and flattened coral group (n ¼ 6) (vermetids were present at ambient densities). Focal growth forms and extensive dead patches on reefs (x2 ¼ corals were weighed in the laboratory, transplanted in triplicate to 65.0, d.f. ¼ 1, p , 0.0001). See also electronic each reef and secured to galvanized staples (previously affixed to supplementary material, appendix A. the reef) using plastic cable ties. All experiments were initiated between 2 June and 10 June 2006. Our observations after transplant- ing corals showed that most corals were directly contacted by mucus reef morphology with vermetids without vermetids nets in the treatments, where vermetids were not removed, in a manner similar to what we have observed with naturally occurring corals.
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