Abstract
Coral reefs in the Florida Keys have degraded in recent decades, prompting efforts to re-establish populations of staghorn coral, Acropora cervicornis, to restore structure and ecological function. However, predation on these corals by the corallivorous gastropod, Coralliophila galea, has been a substantial and chronic impediment to restoration efforts. Therefore, we conducted a series of manipulative laboratory experiments and a 2-week, in situ proof-of-concept trial to determine whether Thais deltoidea, a carnivorous gastropod that co-occurs with C. galea, can control C. galea corallivory and thus improve A. cervicornis survival. Our laboratory results showed that T. deltoidea preys upon C. galea, although it is not a preferred prey choice. Nevertheless, treatments with T. deltoidea had significantly higher percentages of live coral tissue than when T. deltoidea was absent. This occurred not only because T. deltoidea consumed C. galea, but also because the presence of T. deltoidea elicited an escape response in C. galea, significantly reducing the amount of time C. galea spent feeding on A. cervicornis colonies. This trophic relationship was also seen in our in situ proof-of-concept trial. We observed significantly fewer C. galea on A. cervicornis when T. deltoidea was present which led to a higher, if not statistically significant, percentage of live tissue on our A. cervicornis outplants. Ecological processes need to be incorporated into coral reef ecosystem restoration to achieve positive outcomes. Integrating T. deltoidea into coral restoration efforts may improve success by mitigating C. galea corallivory through the non-consumptive, risk-adverse, escape response that T. deltoidea provokes, initiating a trophic cascade that improves the long-term survival of outplanted corals. Further research is needed to determine the long-term efficacy of this approach, but the addition of gastropod trophodynamics to coral reef ecosystem restoration may prove useful.
Similar content being viewed by others
References
Baums IB, Miller MW, Szmant AM (2003a) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. I: population structure of snails and corals. Mar Biol 142:1083–1091
Baums IB, Miller MW, Szmant AM (2003b) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. II: feeding, respiration, and growth. Mar Biol 142:1093–1101
Bayne RC, Newell BL (1983) Physiological energetics of marine molluscs. In: Saleuddin ASM, Wilbur KM (eds) The mollusca: physiology, part 1, vol 4. Academic Press, New York, pp 407–511
Booth HS, Pusack TJ, White JW, Stallings CD, Kimbro DL (2018) Intraspecific predator inhibition, not a prey size refuge, enables oyster population persistence during predator outbreaks. Mar Ecol Prog Ser 602:155–167
Brawley SH, Adey WH (1982) Coralliophila abbreviata: a significant corallivore. Bull Mar Sci 32:595–599
Bright AJ, Cameron CM, Miller MW (2015) Enhanced susceptibility to predation in corals of compromised condition. PeerJ 3:e1239. https://doi.org/10.7717/peerj.1239
Bruno JF, Selig ER, Casey KS (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:1220–1227
Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 64:1297–1304
Clench WJ (1947) The genera Purpura and Thais in the western Atlantic. Johnsonia 2:61–91
Croll RP (1983) Gastropod chemoreception. Biol Rev 58:293–319
Delgado GA, Glazer RA, Stewart NJ (2002) Predator-induced behavioral and morphological plasticity in the tropical marine gastropod Strombus gigas. Biol Bull 203:112–120
Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100
Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060
Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soule ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–306
Ferrier GA, Zimmer CA, Zimmer RK (2016) Chemical ecology of wave-swept shores: the primacy of contact cues in predation by whelks. Biol Bull 231:207–215
Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movments: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Giacoletti A, Rinaldi A, Mercurio M, Mirto S, Sara G (2016) Local consumers are the first line to control biological invasions: a case study with the whelk Stramonita haemastoma (Gastropoda: Muricidae). Hydrobiologia 772:117–129
Gosselin LA, Chia F (1996) Prey selection by inexperienced predators: do early juvenile snails maximize net energy gains on their first attack? J Exp Mar Biol Ecol 199:45–58
Hall MR, Motti CA, Kroon F (2017) The potential role of the giant triton snail, Charonia tritonis (Gastropoda: Ranellidae) in mitigating population outbreaks of the crown-of-thorns starfish. Integrated Pest Management of Crown-of-Thorns Starfish. Report to the National Environmental Science Programme. Reef and Rainforest Research Centre Limited, Cairns
Hayes JA (1989) The biology and ecology of Coralliophila abbreviata Lamarck (Gastropoda, Coralliophilidae): The importance of corallivores in the ecology of coral reefs. Ph.D. dissertation, University of Texas at Austin, Texas, USA
Hein MY, Willis BL, Beeden R, Birtles A (2017) The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs. Rest Ecol 25:873–883
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. TREE 23:202–210
Hughes TP, Kerry J, Alvarez-Noriega M, Álvarez-Romero J, Anderson K, Baird A, Babcock R, Beger M, Bellwood DR, Berkelmans R, Bridge TC (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Humphries AT, La Peyre MK, Decossas GA (2011) The effect of structural complexity, prey density, and “predator-free space” on prey survivorship at created oyster reef mesocosms. PLoS ONE 6(12):e28339. https://doi.org/10.1371/journal.pone.0028339
Jackson JBC (2008) Ecological extinction and evolution in the brave new ocean. PNAS 105:11458–11465
Jackson JBC, Donovan MK, Cramer KL, Lam VV (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network, IUCN, Gland
Johnston L, Miller MW (2014) Negative indirect effects of neighbors on imperiled scleractinian corals. Coral Reefs 33:1047–1056
Knowlton N (1992) Thresholds and multiple stable states in coral reef community dynamics. Amer Zool 32:674–682
Ladd MC, Miller MW, Hunt JH, Sharp WC, Burkepile DE (2018) Harnessing ecological processes to facilitate coral restoration. Front Ecol Environ 16:239–247
Lieury N, Ruette S, Devillard S, Albaret M, Drouyer F, Baudoux B, Millon A (2015) Compensatory immigration challenges predator control: an experimental evidence-based approach improves management. J Wildl Manage 79:425–434
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lirman D, Thyberg T, Herlan J, Hill C, Young-Lahiff C, Schopmeyer S, Huntington B, Santos R, Drury C (2010) Propagation of the threatened staghorn coral Acropora cervicornis: methods to minimize the impacts of fragment collection and maximize production. Coral Reefs 29:729–735
Maldonado MA, Martin PR (2019) Dealing with a hyper-successful neighbor: effects of the invasive apple snail Pomacea canaliculata on exotic and native snails in South America. Curr Zool 65:225–235
Miller MW (2001) Corallivorous snail removal: evaluation of impact on Acropora palmata. Coral Reefs 19:293–295
Miller SL, Chiappone M, Rutten LM (2011) Abundance, distribution, and condition of Acropora corals, other benthic coral reef organisms, and marine debris in the upper Florida Keys National Marine Sanctuary: 2011 Quick Look Report and Data Summary. Center for Marine Science/University of North Carolina Wilmington, Key Largo, p 262
National Marine Fisheries Service (2015) Recovery plan for elkhorn (Acropora palmata) and staghorn (A. cervicornis) corals. National Marine Fisheries Service, Silver Spring
Palmer AR (1984) Prey selection by thaidid gastropods: some observational and experimental field tests of foraging models. Oecologia 62:162–172
Pennings SC (1990) Predator-prey interactions in opisthobranch gastropods: effects of prey body size and habitat complexity. Mar Ecol Prog Ser 62:95–101
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509
Pusack TJ, White JW, Tillotson HG, Kimbro DL, Stallings CD (2018) Size-dependent predation and intraspecific inhibition of an estuarine snail feeding on oysters. J Exp Mar Biol Ecol 501:74–82
Rice MM, Ezzat L, Burkepile DE (2019) Corallivory in the Anthropocene: interactive effects of anthropogenic stressors and corallivory on coral reefs. Front Mar Sci 5:525
Rinkevich B (1995) Restoration strategies for coral reefs damaged by recreational activities: the use of sexual and asexual recruits. Rest Ecol 3:241–251
Rinkevich B (2014) Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Curr Opin Environ Sustain 7:28–36
Ripple WJ, Beschta RL (2004) Wolves, elk, willows, and trophic cascades in the upper Gallatin Range of Southwestern Montana, USA. Forest Ecol Manage 200:161–181
Ripple WJ, Beschta RL (2006) Linking wolves to willows via risk-sensitive foraging by ungulates in the northern Yellowstone ecosystem. Forest Ecol Manage 230:96–106
Ripple WJ, Beschta RL (2007) Restoring Yellowstone’s aspen with wolves. Biol Conserv 138:514–519
Ripple WJ, Larsen EJ, Renkin RA, Smith DW (2001) Trophic cascades among wolves, elk and aspen on Yellowstone National Park’s northern range. Biol Conserv 102:227–234
Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91
Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS ONE 3(2):e1548. https://doi.org/10.1371/journal.pone.0001548
Schopmeyer SA, Lirman D, Bartels E, Gilliam DS, Goergen EA, Griffin SP, Johnson ME, Lustic C, Maxwell K, Walter CS (2017) Regional restoration benchmarks for Acropora cervicornis. Coral Reefs 36:1047–1057
Sharp WC, Delgado GA (2015) Predator-prey interactions between the corallivorous snail Coralliophila abbreviata and the carnivorous deltoid rock snail Thais deltoidea. Biol Bull 229:129–133
Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY (2016) Fear of large carnivores causes a trophic cascade. Nat commun 7:10698
Williams DE, Miller MW (2005) Coral disease outbreak: pattern, prevalence, and transmission in Acropora cervicornis. Mar Ecol Prog Ser 301:119–128
Williams DE, Miller MW, Bright AJ, Cameron CM (2014) Removal of corallivorous snails as a proactive tool for the conservation of acroporid corals. PeerJ 2:680. https://doi.org/10.7717/peerj.680
Wirsing AJ, Heithaus MR (2009) Olive-headed sea snakes Disteria major shift seagrass microhabitats to avoid shark predation. Mar Ecol Prog Ser 387:287–293
Wirsing AJ, Ripple WJ (2011) A comparison of shark and wolf research reveals similar behavioral responses by prey. Front Ecol Environ 9:335–341
Young CN, Schopmeyer SA, Lirman D (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bull Mar Sci 88:1075–1098
Acknowledgements
This project was funded by the Florida Fish and Wildlife Conservation Commission’s Florida’s Wildlife Legacy Initiative and the US Fish and Wildlife Service’s State Wildlife Grants program (Grant #9750-295-1252). Additional funding was provided by the Wildlife Foundation of Florida’s Charles Stroh Fund for the restoration of Davis Reef as well as the Florida Fish and Wildlife Conservation Commission’s Fish and Wildlife Research Institute. Work was conducted under Florida Keys National Marine Sanctuary permit numbers FKNMS-2011-150-A1, FKNMS-2011-159-A4, and FKNMS-2016-060. The authors would like to thank Einat Sandbank for her contributions in the laboratory and in the field. Casey Butler, Jennifer Granneman, Colin Howe, Stephanie Schopmeyer, and two anonymous reviewers made valuable suggestions that greatly improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Topic Editor Mark Vermeij
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Delgado, G.A., Sharp, W.C. Capitalizing on an ecological process to aid coral reef ecosystem restoration: Can gastropod trophodynamics enhance coral survival?. Coral Reefs 39, 319–330 (2020). https://doi.org/10.1007/s00338-020-01893-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-020-01893-y