Skip to main content
Log in

Protection of host anemones by snapping shrimps: a case for symbiotic mutualism?

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

The sea anemone Bartholomea annulata is an ecologically important member of Caribbean coral reefs which host a variety of symbiotic crustacean associates. Crustacean exosymbionts typically gain protection from predation by dwelling with anemones. Concurrently, some symbionts may provide protection to their host by defending against anemone predators such as the predatory fireworm, Hermodice carunculata, which can severely damage or completely devour prey anemones. Herein we show through both field and laboratory studies that anemones hosting the symbiotic alpheid shrimp Alpheus armatus are significantly less likely to sustain damage by H. carunculata than anemones without this shrimp. Our results suggest that the association between A. armatus and B. annulata, although complex because of the numerous symbionts involved, may be closer to mutualism on the symbiotic continuum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baeza J, Thiel M (2003) Predicting territorial behavior in symbiotic crabs using host characteristics: a comparative study and proposal of a model. Mar Biol 142:93–100

  • Barroso R, Paiva PC (2007) Amphinomidae (Annelida: Polychaeta) from Rocas Atoll, Northeastern Brazil. Arq Museu Nac 65:357–362

    Google Scholar 

  • Becker JH, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515–520

    Google Scholar 

  • Becker JHA, Curtis LM, Grutter AS (2005) Cleaner shrimp use a rocking dance to advertise cleaning service to clients. Curr Biol 15:760–764

    Article  PubMed  CAS  Google Scholar 

  • Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347

    Article  Google Scholar 

  • Brooks WR, Gwaltney CL (1993) Protection of symbiotic cnidarians by their hermit crab hosts: evidence for mutualism. Symbiosis 15:1–13

    Google Scholar 

  • Brooks WR, Mariscal RN (1984) The acclimation of anemone fishes to sea anemones: protection by changes in the fish’s mucous coat. J Exp Mar Biol Ecol 80:277–285

    Article  Google Scholar 

  • Budd AF, Fukami H, Smith ND, Knowlton N (2012) Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linnean Soc 166:465–529

    Article  Google Scholar 

  • Bunkley-Williams L, Williams EH (1998) Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana 71:862–869

    Article  Google Scholar 

  • Calado R, Dionísio G, Dinis MT (2007) Decapod crustaceans associated with the snakelock anemone Anemonia sulcata: living there or just passing by? Sci Mar 71:287–292

    Article  Google Scholar 

  • Camp DK, Lyons WG, Perkins TH (1998) Checklist of selected shallow-water marine invertebrates of Florida

  • Chapuis L, Bshary R (2010) Signalling by the cleaner shrimp Periclimenes longicarpus. Anim Behav 79:645–647

    Article  Google Scholar 

  • Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol 38:311–355

    Google Scholar 

  • Crawford JA (1992) Acclimation of the shrimp, Periclimenes anthophilus, to the giant sea anemone, Condylactis gigantea. Bull Mar Sci 50:331–341

    Google Scholar 

  • Criales MM (1984) Shrimps associated with coelenterates, echinoderms, and molluscs in the Santa Marta region, Colombia. J Crustac Biol 4:307–317

    Article  Google Scholar 

  • Dickman CR (1992) Commensal and mutualistic interactions among terrestrial vertebrates. Trends Ecol Evol 7:194–197

    Article  PubMed  CAS  Google Scholar 

  • Fauchald K (1973) Polychaetes from Central American sandy beaches. Bull South Calif Acad Sci 72:19–31

    Google Scholar 

  • Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar Ecol Prog Ser 234:119–125

    Article  Google Scholar 

  • Floeter SR, Vaquez DP, Grutter AS (2007) The macroecology of marine cleaning mutualisms. J Anim Ecol 76:105–111

    Article  PubMed  Google Scholar 

  • Genovese SJ, Witman JD (2004) Wind-mediated diel variation in flow speed in a Jamaican back reef environment: effects on ecological processes. Bull Mar Sci 75:281–293

    Google Scholar 

  • Glynn PW (1980) Defense by symbiotic crustacea of host corals elicited by chemical cues from predator. Oecologia 47:287–290

    Article  Google Scholar 

  • Guo CC, Hwang JS, Fautin DG (1996) Host selection by shrimps symbiotic with sea anemones: a field survey and experimental laboratory analysis. J Exp Mar Biol Ecol 202:165–176

    Article  Google Scholar 

  • Gwaltney CL, Brooks WR (1994) Host specificity of the anemone shrimp Periclimenes pedersoni and P. yucatanicus in the Florida Keys. Symbiosis 16:83–93

    Google Scholar 

  • Haine ER (2008) Symbiont-mediated protection. Proc R Soc B Biol Sci 275:353–361

    Article  Google Scholar 

  • Hattori A (2002) Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. J Anim Ecol 71:824–831

    Article  Google Scholar 

  • Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453

    Article  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Herrnkind W, Stanton G, Conklin E (1976) Initial characterization of the commensal complex associated with the anemone, Lebrunia danae, at Grand Bahama. Bull Mar Sci 26:65–71

    Google Scholar 

  • Huebner LK, Chadwick NE (2012a) Patterns of cleaning behaviour on coral reef fish by the anemoneshrimp Ancylomenes pedersoni. J Mar Biol Assoc U K 92:1557–1562

    Article  Google Scholar 

  • Huebner LK, Chadwick NE (2012b) Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp. J Exp Mar Biol Ecol 416–417:237–242

    Article  Google Scholar 

  • Hughes M (1996) The function of concurrent signals: visual and chemical communication in snapping shrimp. Anim Behav 52:247–257

    Article  Google Scholar 

  • Humann P, Deloach N (2002) Reef fish, creature, coral identification. Florida Caribbean Bahamas New World Publications Inc

  • Humann P, Deloach N (2003) Symbiosis. Reef fish behavior, Florida, Caribbean, Bahamas

  • Jonasson MW (1987) Cleaning behavior comparison of two shrimp species (Stenopus hispidus and Lysmata grabhami). J Zool 213:117–131

    Article  Google Scholar 

  • Knowlton N, Keller BD (1982) Symmetric fights as a measure of escalation potential in a symbiotic, territorial snapping shrimp. Behav Ecol Sociobiol 10:289–292

    Article  Google Scholar 

  • Knowlton N, Keller BD (1985) Two more sibling species of alpheid shrimps associated with the Caribbean sea anemones Bartholomea annulata and Heteractis lucida. Bull Mar Sci 37:893–904

    Google Scholar 

  • Knowlton N, Keller BD (1986) Larvae which fall far short of their potential: highly localized recruitment in an alpheid shrimp with extended larval development. Bull Mar Sci 39:213–223

    Google Scholar 

  • Knowlton RE, Moulton JM (1963) Sound production in the snapping shrimps Alpheus (Crangon) and Synalpheus. Biol Bull 125:311–331

    Article  Google Scholar 

  • Limbaugh C (1961) Cleaning symbiosis. Sci Am 205:42–49

    Article  Google Scholar 

  • Lizama J, Blanquet RS (1975) Predation on sea anemones by the amphinomid polychaete Hermodice carunculata. Bull Mar Sci 25:442–443

    Google Scholar 

  • Losey GS (1972) The ecological importance of cleaning symbiosis. Copeia 4:820–833

    Article  Google Scholar 

  • McCammon A (2010) Snapping shrimp protect host anemones from predators. Biology, Boca Raton

    Google Scholar 

  • McCammon A, Sikkel P, Nemeth D (2010) Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment. Coral Reefs 29:419–426

    Article  Google Scholar 

  • McKeon CS, Stier AC, McIlroy SE, Bolker BM (2012) Multiple defender effects: synergistic coral defense by mutualist crustaceans. Oecologia 169:1095–1103

    Article  PubMed  Google Scholar 

  • Meinkoth NA (2007) National Audubon Society field guide to North American seashore creatures. Alfred A. Knopf, Inc., New York

    Google Scholar 

  • Mercier A, Hamel J-F (1994) Deleterious effects of a pycnogonid on the sea anemone Bartholomea annulata. Can J Zool 72:1362–1364

    Article  Google Scholar 

  • Mihalik MB, Brooks WR (1995) Protection of the symbiotic shrimps Periclimenes pedersoni, P. yucatanicus, and Thor spec. from fish predators by their host sea anemones. Proceedings of the 6th International Conference on Coelenterate Biology 1995: 337–343

  • Nelsen M (2008) Modeling of population dynamics in the corkscrew anemone Bartholomea annulata on Caribbean coral reefs. Master’s. Biology, Auburn

    Google Scholar 

  • Nizinski MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, and atypical symbiotic cleaner shrimp. Bull Mar Sci 45:174–188

    Google Scholar 

  • Okuno J, Bruce AJ (2010) Designation of Ancylomenes gen. nov., for the ‘Periclimenes aesopius species group’ (Crustacea: Decapoda: Palaemonidae), with the description of a new species and a checklist of congeneric species. Zootaxa 2372:85–105

    Google Scholar 

  • Östlund-Nilsson S, Becker JHA, Nilsson GE (2005) Shrimps remove ectoparasites from fishes in temperate waters. Biol Lett 1:454–456

    Article  PubMed  PubMed Central  Google Scholar 

  • Porat D, Chadwick-Furman NE (2005) Effects of anemonefish on giant sea anemones: ammonium uptake, zooxanthella content and tissue regeneration. Mar Freshw Behav Physiol 38:43–51

    Article  CAS  Google Scholar 

  • Poulin R, Grutter AS (1996) Cleaning symbioses: proximate and adaptive explanations. Bioscience 46:512–517

    Article  Google Scholar 

  • Poulin R, Vickery WL (1995) Cleaning symbiosis as an evolutionary game: to cheat or not to cheat? J Theor Biol 175:63–70

    Article  PubMed  Google Scholar 

  • Roopin M, Henry R, Chadwick N (2008) Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar Biol 154:547–556

    Article  CAS  Google Scholar 

  • Roughgarden J (1975) Evolution of marine symbiosis—a simple cost-benefit model. Ecology 56:1201–1208

    Article  Google Scholar 

  • Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247

    Article  Google Scholar 

  • Silbiger NJ, Childress MJ (2008) Interspecific variation in anemone shrimp distribution and host selection in the Florida Keys (USA): implications for marine conservation. Bull Mar Sci 83:329–345

    Google Scholar 

  • Smith WL (1977) Beneficial behavior of a symbiotic shrimp to its host anemone. Bull Mar Sci 27:343–346

    Google Scholar 

  • Souza J, Rodrigues H, Neves B, Perez C (2007) First report of bristleworm predator of the reef octocoral Carijoa riisei. Coral Reefs 26:1033

    Article  Google Scholar 

  • Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198:27–36

    Article  Google Scholar 

  • Spotte S (1997) Sexual and regional variation in the morphology of the spotted anemone shrimp Periclimenes yucatanicus (Decapoda: Caridea: Palaemonidae). J Crustac Biol 17:389–397

    Article  Google Scholar 

  • Stanton A (2003) Bristleworms nano-reef. Nano-Reef.com

  • Stier AC, Gil MA, McKeon CS, Lemer S, Leray M, Mills SC, Osenberg CW (2012) Housekeeping mutualisms: do more symbionts facilitate host performance? PLoS ONE 7:e32079

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Van Tassell JL, Brito A, Bortone SA (1994) Cleaning behavior among marine fishes and invertebrates in the Canary Islands. Cybium 18:117–127

    Google Scholar 

  • Vreeland HV, Lasker HR (1989) Selective feeding of the polychaete Hermodice carunculata Pallas on Caribbean gorgonians. J Exp Mar Biol Ecol 129:265–277

    Article  Google Scholar 

  • Walker MJA, Masuda VL (1990) Toxins from marine invertebrates marine toxins. American Chemical Society, Washington, DC, pp 312–332

    Google Scholar 

  • Wirtz P, de Melo G, de Grave S (2009) Symbioses of decapod crustaceans along the coast of Espírito Santo, Brazil. Marine Biodiversity Records 2

  • Witman J (1988) Effects of predation by the fireworm Hermodice carunculata on milleporid hydrocorals. Bull Mar Sci 42:446–458

    Google Scholar 

  • Yáñez-Rivera B, Suárez-Morales E (2008) Pseudanthessius tortuosus Stock, 1967 (Copepoda: Cyclopoida) from the amphinomid polychaete Hermodice carunculata (Pallas) in the western Caribbean. Syst Parasitol 69:211–220

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to the staff at the Virgin Islands Environmental Resource Station (VIERS), the McLean Marine Science Center and the Center for Marine and Environmental Studies (CMES) of the University of the Virgin Islands, and Gumbo Limbo Environmental Complex of Boca Raton, Florida, for logistic support and use of their facilities. Many thanks to A.W. Parr, S.W. Parr, R.L. Welicky, G. Rivera, W. Sears, T.J. Smith, B. Tuttle, B. Weldon, and volunteers from the 2008 and 2009 Virgin Islands Earthwatch teams for assisting with the development of protocol and collection of data and to anonymous reviewers for constructive comments on the manuscript. We acknowledge the YouTube, LLC website for hosting video of this work at: http://www.youtube.com/watch?v=bYxluzkeUc0.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to W. Randy Brooks.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Video of interaction between Hermodice carunculata fireworm and Alpheus armatus snapping shrimp (MPG 4000 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McCammon, A.M., Brooks, W.R. Protection of host anemones by snapping shrimps: a case for symbiotic mutualism?. Symbiosis 63, 71–78 (2014). https://doi.org/10.1007/s13199-014-0289-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-014-0289-8

Keywords

Navigation