BBSR
Marine Invertebrates of Bermuda

Symbiotic Cleaner Shrimp (Periclimenes anthophilus)

Ayla Doubleday
and
James B. Wood (Ed)


Taxonomy  Habitat  Ecology  Recent Research  Commercial Importance  Bermuda Laws  Personal Interest  References  Links 


Symbiotic Cleaner Shrimp Periclimenes anthophilus
Abstract


Periclimenes anthophilus is a cleaner shrimp in symbiotic association with the Giant Sea Anemone Condylactis gigantea. They are found only around the waters of Bermuda ranging from 1-15m (Sargent and Wagenbach 1975). They are not space limited because not all anemones are colonized, and they are randomly distributed with respect to available host habitat (Nizinski 1989). Their predator avoidance is mainly due to their transparent coloring and ability to hide within their host. Acclimation to their host is completed by chemically camouflaging themselves with the nematocysts of the anemone (Crawford 1992). The species was previously thought to be Periclimenes pederonsi until 1964, when Holthius and Eibl-Ebesfeldt discovered otherwise. Their diet is probably related to P. pederonsi which consists mostly of ectoparasites digested while cleaning fish (Becker and Grutter 2004). P. anthophilus has been described as a cleaning shrimp displaying a symbiosis with ten different fish species. This is mainly due to the research by Sargent and Wagenbach (1975). They described each shrimp as having its own cleaning station.

Taxononmy

Phylum: Arthropoda
  Class: Malacostraca
    Order: Decapoda
      Family: Palaemonidae

Identification of Periclimenes anthophilus can be difficult. P. anthophilus has been distinguished from Periclimenes pedersoni Chade due to a slight variation in the carpus of the major second periopod, and because it associates with a different host anemone Bartholomea annulata (Chace 1972). P. anthophilus is a species with a longitudinal suture (brachiostegal groove) present, at least anteriorly. They have walking legs with dactyl which terminate in two unequal teeth. There is no spine on the ventral surface between their anterior pair of legs. Their coloration is very transparent, with distinctive white, pale purple and reddish brown markings (Sterrer 1986).

Habitat


Shrimp of the Periclimenes Genus are found largely distributed throughout the Caribbean (Nizinski 1989). The species Periclimenes anthophilus has been found only in the waters around Bermuda, identified in 1964 by Holthuis and Eibl-Eibesfeldt. They can be easily misidentified with Periclimenes pedersoni because of their similar coloration and morhpology. P. anthophilus exists in depths of 1-15m on or near the anemone Condylactis gigantea (Sargent and Wagenbach 1975). They are found among the different reef zones of Bermuda ranging from inshore patch reefs to the rim reefs. They are not space limited because not all anemones are colonized, and they are randomly distributed with respect to available host habitat (Nizinski 1989).



Ecology


The social structure of Periclimenes anthophilus is mainly dependent upon their close symbiotic relationship with the giant sea anemone Condylactis gigantea. The shrimps are protected from predators by hiding among the anemones tentacles (Nizinski 1989). Within the anemones they can be found in populations ranging from 1-11 individuals, surprisingly social interactions are rare (Nizinski 1989). Population size is limited to recruitment success and predation levels, and is not regulated by social hierarchies or territoriality as is commonly found in other anemone shrimp (Nizinski 1989). Laboratory experiments suggest no strong social structure, no evidence of a dominance hierarchy, territoriality, or individual recognition (Nizinkski 1989). Cleaning symbioses can be one-sided and not mutualistic (Poulin and Grutter 1996). Some people believe that this is the case between the two organisms. Others have researched that the symbiotic shrimp provides the anemone with regenerated nitrogen (Spotte 1995).

Periclimenes anthophilus is very small being easy prey for many invertivores. However, their cryptic coloring and disguise patterns help them hide, camoflauged within their host anemone Condylactis gigantea. P. anthophilus displays a high host specificity to this cnidarian. But, it is difficult to reside within tentacles of an actinarian. P. anthophilus has evolved mechanisms to counter these stinging nematocysts. The exoskeletons of shrimps do not appear to protect them from the anemone nematocysts and protection occurs after a time of acclimation (Crawford 1992). It has been suggested that anemone shrimp acclimate to their hosts in the same way as anemone fishes. This is by chemically camouflaging themselves in the anemone mucus which contains thousands of nematocysts secreted by the anemone (Crawford 1992). P. anthophilus have been seen to cut off pieces of mucus using the chelae of its chelipeds and coating its body (Crawford 1992). Once shrimps are fully acclimated to their host the anemones will not respond to them differently and completely dismiss their presence (Levine and Blanchard 1980).

Periclimenes anthophilus has been described as a cleaning shrimp displaying a symbiosis with ten different fish species. This is mainly due to the research by Sargent and Wagenbach (1975). They described each shrimp as having its own cleaning station. The shrimp would rock laterally on their last three periopods in motion with the anemone. When a fish approached they would extend one or both of their antennae towards the host fish which had approached. They would then stroke the host with the antennae and board it walking over its body removing and ingesting ectoparasites. There has also been studies stating that no cleaning behavior was observed (Nizinski 1989).

Upon gut inspection of wild shrimps it has been found that the diet of the cleaner shrimp Periclimenes holthuisi consists of crustacean ectoparasites from the Family Gnathiidae and the Class Copepoda (Becker and Grutter 2004). This shrimp is closely related to Periclimenes anthophilus and probably has a similar diet. In some laboratory conditions it has been shown that P. holthuisi eat parasitic monogenean flatworms (Becker and Grutter 2004). P. holthuisi significantly reduced the mongenean flatworms existing on captive surgeonfish by 74.5% within 48 hours (Becker and Grutter 2004). However there is no evidence of monogeneans existing within wild shrimp guts (Rhode 2002). The closely related cleaner shrimp Periclimenes pedersoni from the Caribbean removed one species of ectoparasitic juvenile cymothoid isopod, Anilocra haemuli (Bunkley-Williams and Williams 1998).

Little has been studied with regards to specific behavior of Periclimenes anthophilus while reproducing, there is some statistical studies of the related shrimp Periclimenes brevicarpalis rate of larval release. They are separate sex individuals unlike the shrimp Lysmata wurdemanni which are simultaneous hermaphrodites (Lin and Zhang 2004). Ovarian maturation and spawning occur when the diet is supplemented with an Annelid which is full of lipids containing cholesterol and polyunsaturated fatty acids (Middleditch et al.). Larval release also occurs in association with their host. It has been shown that female shrimp of Periclimenes brevicarpalis, when kept with their anemone, released larvae 10 times during a 30 day period (Daphne et al. 1995). The female shrimp that were kept isolated from the anemone released larvae only 8 times within a 30 day period (Daphne et al. 1995).


Recent Research


Crawford (1992) researched the acclimation of Periclimenes anthophilus to the giant sea anemone Condylactis gigantea. Upon introduction into an aquarium with C. gigantea, the unacclimated shrimp swam directly towards the anemone contacting the anemone tentacles with its antennae, periopods, or both. Usually the shrimp was stung and jerked backwards upon the first few contacts. Occasionally an appendage of the shrimp would adhere to a tentacle and the shrimp would pull itself free. In the end it was discovered that the acclimated shrimp was not stung and the unacclimated shrimp was stung by the anemone regardless of the state of the anemone. This is important information to know, regarding the outcome of what would happen if a shrimp were separated from its anemone, due to a storm or disease.


Research was done by Becker and Grutter (2005) using Cephalopholis cyanostigma and Urocaridella sp. in hopes to describe the behavior of cleaner shrimps in general. Doing field-based research they described that when a potential client swam near a cleaning station, one to several cleaner shrimp performed a side-to-side movement or rocking dance while approaching the potential client in the water. This dance was followed by a cleaning interaction. They discovered a mean of 27.7 fish cleaned per hour. They noted this was very similar to the cleaning dance of Periclimenes sp. describing Periclimenes as performing vigorous whipping of their antennae and lateral body swaying while standing in a conspicuous location when a client fish is nearby.

Commercial Importance


Marine ornamental species trade is a multi-million dollar industry (Calado et al. 2003). Marine tropical decapod crustaceans are also among the most popular invertebrate species in the aquarium trade industry (Calado et al. 2003) Cleaner shrimp in particular are often used in aquariums because of their aesthetic appeal. Luckily, Periclimenes anthophilus has avoided this commercial value.

Bermuda Laws


In 1966 the Coral Reef Preserves Act was passed and revised in 1989. This prohibits the removal of marine fauna or flora on the North Shore Coral Reef Preserve. This also covers the South Shore Coral Reef Preserve. Specific boundaries of the preserves can be found under Laws of Bermuda Title 20, Item 12.

Personal Interest


I was first interested in these shrimp because of their ability to hide within anemones. I became infatuated with the idea of looking for them and counting how many I could find, it especially interested me because there was so little research done regarding them. These shrimp also amaze me because they have so many symbiotic relationships. They can acclimate to an anemone, and are allowed to board fish in order to clean them. It shows the dependence of all the organisms in an ecosystem. The anemone must rely on its symbiotic zooxanthellae, the shrimp on the anemone and the fish rely on the shrimp.

References

  • Becker J., and Grutter A. (2004). Cleaner shrimp do clean. Coral Reefs.Vol 23: pp 515-520.

  • Becker Justine, Curtis Lynda, and Grutter Alexander. Cleaner shrimp use a rocking dance to advertise cleaning service to clients (2005). Current Biology. Vol 15: pp 760-764.

  • Bunkley-Williams L, and Williams E. (1998). Ability of pedersoni cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana. Vol 71: pp 862-869.

  • Calado R., Narciso L., Morais S., Rhyne A., and Lin J. (2003). A rearing system for the culture of ornamental decapod crustacean larvae. Aquaculture. Vol 218: pp 329-339.

  • Chace F. (1972). The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow water species (Crustacea: Decapoda: Natantia). Smithsonian Contribution to Zoology. Vol 98: pp 29-39.

  • Crawford James (1992). Acclimation of the shrimp Periclimenes anthophilus to the giant sea anemone Condylactis gigantea. Bulletin of Marine Science. Vol 50: pp 331-341.

  • Daphne Fautin, Chau-Chih Guo and Jiang-Shiou Hwang (1995). Costs and benefits of the symbiosis between the anemoneshrimp Periclimenes brevicarpalis and its host Entacmaea quadricolor. Marine Ecology Progress Series. Vol 129: pp 77-84.

  • Levine Daniel and Blanchard Orland (1980). Acclimation of two shrimps of the genus Periclimenes to sea anemones. Bulletin of Marine Science. Vol 30: pp 460-466.

  • Lin J. And Zhang D. (2004). Reproduction in a simultaneous hermaphroditic shrimp, Lysmata wurdemanni: any two will do? Marine Biology. Vol 139: pp 1155-1158.

  • Middleditch B., Missler S., Hines H., McVey J, Brown A, Ward D, and Lawrence A. (1980).Metabolic profiles of penaied shrimp: dietary lipids and ovarian maturation. Journal of Chromatography. Vol195: pp 359-368.

  • Nizinski Martha (1989). Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, and atypical symbiotic cleaner shrimp. Bulletin of Marine Science. Vol 45: pp 174-188.

  • Poulin Robert and Grutter Alexander (1996). Cleaning symbioses: proximate and adaptiveexplanations. BioScience. Vol 46: pp 512-517.

  • Rhode K. (2002). Ecology and biogeography of marine parasites. Advance Marine Biology. Vol:43 pp 2-86.

  • Sargent Craig and Wagenbach Gary (1975). Cleaning Behavior of the shrimp, Periclimenes anthophilus Holthuis and Eibl-Eibesfeldt (Crustacea: Decapoda: Natantia). Bulletin of Marine Science. Vol 25: pp 466-472.

  • Spotte Stephen (1995). Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. Journal of Experimental Marine Biology and Ecology. Vol 198: pp 27-36.

  • Sterrer Wolfgang (1986). Marine Fauna and Flora of Bermuda. John Wiley & Sons: NY: pp545-548.


  • Links

    Condylactis gigantea
    Shrimp structure
    Periclimenes pedersoni