Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T08:39:44.980Z Has data issue: false hasContentIssue false

Comparative cleaning behaviour of Pederson's cleaner shrimp (Ancylomenes pedersoni) between geographically close yet ecologically dissimilar coral reef habitats

Published online by Cambridge University Press:  03 November 2020

Joseph J. Romain
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, ColchesterCO4 3SQ, UK Operation Wallacea, Wallace House, Old Bolingbroke, SpilsbyPE23 4EX, UK
Dan A. Exton
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, SpilsbyPE23 4EX, UK
David J. Smith
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, ColchesterCO4 3SQ, UK
Amelia Rose
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, SpilsbyPE23 4EX, UK Department of Zoology, The Tinbergen Building, University of Oxford, South Parks Road, OxfordOX1 3PS, UK
Clayton Vondriska
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, SpilsbyPE23 4EX, UK Department of Environmental Sciences, Arkansas State University, 2105 Aggie Rd, State University, AR 72467, USA Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, 1315 Kinnear Road, Columbus, Ohio 43210, USA
Benjamin M. Titus*
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, 1315 Kinnear Road, Columbus, Ohio 43210, USA Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th St, New York, NY, 10024, USA
*
Author for correspondence: Benjamin M. Titus, E-mail: [email protected]

Abstract

Cleaning mutualisms are important interactions on coral reefs. Intraspecific variation in cleaning rate and behaviour occurs geographically and is often attributed to local processes. However, our understanding of fine-scale variation is limited, but would allow us to control for geography and region-specific behavioural patterns. Here, we compare the cleaning activity of Pederson's cleaner shrimp (Ancylomenes pedersoni) on two neighbouring, yet ecologically dissimilar, reef systems in Honduras: Banco Capiro, an offshore bank close to significant land runoff with high coral cover but a depleted fish population, and an oligotrophic fringing reef around the island of Utila, with lower coral cover but high fish abundance and diversity. The proportion of realized to potential fish clientele was <60% at both sites, and the composition of clientele was neither reflective of the demographics of the resident assemblages at each site nor similar between sites. Parrotfishes represented 13–15% of total fish abundance at both sites yet accounted for >50% (Banco Capiro) and 10% (Utila) of all cleans. Conversely, the schoolmaster snapper (Lutjanus apodus) represented ~1% of total fish abundance at both sites yet accounted for 40% (Utila) and 1% (Banco Capiro) of all cleans. After standardizing our cleaning rate data by clientele abundance, we find that clientele at Banco Capiro engage in over four times as many cleaning encounters per hour with A. pedersoni than at Utila. Our study highlights the variable nature of coral reef cleaning interactions and the need to better understand the ecological and environmental drivers of this biogeographic variation.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andradi-Brown, DA, Macaya-Solis, C, Exton, DA, Gress, E, Wright, G and Rogers, AD (2016 a) Assessing Caribbean shallow and mesophotic reef fish communities using Baited-Remote Underwater Video (BRUV) and diver-operated video (DOV) survey techniques. PLoS ONE 11, 123.CrossRefGoogle ScholarPubMed
Andradi-Brown, DA, Gress, E, Wright, G, Exton, DA and Rogers, AD (2016 b) Reef fish community biomass and trophic structure changes across shallow to upper-mesophotic reefs in the Mesoamerican Barrier Reef, Caribbean. PLoS ONE 11(6), e0156641.CrossRefGoogle ScholarPubMed
Andradi-Brown, DA, Vermeij, MJA, Slattery, M, Lesser, M, Bejarano, I, Appeldoorn, R, Goodbody-Gringley, G, Chequer, AD, Pitt, JM, Eddy, C, Smith, SR, Brokovich, E, Pinheiro, HT, Jessup, ME, Shepherd, B, Rocha, LA, Curtis-Quick, J, Eyal, G, Noyes, TJ, Rogers, AD and Exton, DA (2017) Large-scale invasion of western Atlantic mesophotic reefs by lionfish potentially undermines culling-based management. Biological Invasions 19, 939954.CrossRefGoogle Scholar
Andradi-Brown, DA, Gress, E, Laverick, JH, Monfared, MA, Rogers, AD and Exton, DA (2018) Wariness of reef fish to passive diver presence with varying dive gear type across a coral reef depth gradient. Journal of the Marine Biological Association of the United Kingdom 98, 17331743.CrossRefGoogle Scholar
Arnal, C and Côté, IM (1998) Interactions between cleaning gobies and territorial damselfish on coral reefs. Animal Behaviour 55, 14291442.CrossRefGoogle ScholarPubMed
Arnal, C, Côté, I, Sasal, P and Morand, S (2000) Cleaner-client interactions on a Caribbean reef: influence of correlates of parasitism. Behavioral Ecology and Sociobiology 47, 353358.CrossRefGoogle Scholar
Arnal, C, Côté, I and Morand, S (2001) Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behavioral Ecology and Sociobiology 51, 17.Google Scholar
Artim, J and Sikkel, P (2013) Live coral repels a common reef fish ectoparasite. Coral Reefs 32, 487494.CrossRefGoogle Scholar
Bansemer, C, Grutter, AS and Poulin, R (2002) Geographic variation in the behaviour of the cleaner fish Labroides dimidiatus (Labridae). Ethology 108, 353366.CrossRefGoogle Scholar
Berry, W, Rubinstein, N, Melzian, B and Hill, B (2003) The Biological Effects of Suspended and Bedded Sediment (SABS) in Aquatic Systems: A Review. Duluth, MN: United States Environmental Protection Agency.Google Scholar
Bodmer, MD, Rogers, AD, Speight, MR, Lubbock, N and Exton, DA (2015) Using an isolated population boom to explore barriers to recovery in the keystone Caribbean coral reef herbivore Diadema antillarum. Coral Reefs 34, 10111021.CrossRefGoogle Scholar
Briones-Fourzán, P, Pérez-Ortiz, M, Negrete-Soto, F, Barradas-Ortiz, C and Lozano-Álvarez, E (2012) Ecological traits of Caribbean sea anemones and symbiotic crustaceans. Marine Ecology Progress Series 470, 5568.CrossRefGoogle Scholar
Bshary, R (2003) The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. Journal of Animal Ecology 72, 169176.CrossRefGoogle Scholar
Bshary, R and Schäffer, D (2002) Choosy reef fish select cleaner fish that provide high-quality service. Animal Behaviour 63, 557564.CrossRefGoogle Scholar
Bshary, R, Grutter, AS, Willener, AS and Leimar, O (2008) Pairs of cooperating cleaner fish provide better service quality than singletons. Nature 455, 964966.CrossRefGoogle ScholarPubMed
Bunkley-Williams, L and Williams, EH (1998) Ability of Pederson cleaner shrimp to remove juveniles of the parasitic cymothoid isopod, Anilocra haemuli, from the host. Crustaceana 71, 862869.CrossRefGoogle Scholar
Caves, EM, Green, PA and Johnsen, S (2018) Mutual visual signalling between the cleaner shrimp Ancylomenes pedersoni and its client fish. Proceedings of the Royal Society B: Biological Sciences 285, 20180800.CrossRefGoogle ScholarPubMed
Chapman, MR and Kramer, DL (2000) Movements of fishes within and among fringing coral reefs in Barbados. Environmental Biology of Fishes 57, 1124.CrossRefGoogle Scholar
Chapuis, L and Bshary, R (2009) Strategic adjustment of service quality to client identity in the cleaner shrimp, Periclimenes longicarpus. Animal Behaviour 78, 455459.CrossRefGoogle Scholar
Cheney, KL and Côté, IM (2003) Do ectoparasites determine cleaner fish abundance? Evidence on two spatial scales. Marine Ecology Progress Series 263, 189196.CrossRefGoogle Scholar
Clague, GE, Cheney, KL, Goldizen, AW, McCormick, MI, Waldie, PA and Grutter, AS (2011) Long-term cleaner fish presence affects growth of a coral reef fish. Biology Letters 7, 863865.CrossRefGoogle ScholarPubMed
Côté, IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanography and Marine Biology 38, 311355.Google Scholar
Dromard, CR, Bouchon-Navaro, Y, Cordonnier, S, Harmelin-Vivien, M and Bouchon, C (2018) Microhabitat characteristics of Stegastes planifrons and S. adustus territories. Environmental Biology of Fishes 101, 441448.CrossRefGoogle Scholar
Dubin, RE (1981) Pair spawning in the princess parrotfish, Scarus taeniopterus. Copeia 2, 475477.CrossRefGoogle Scholar
Dunkley, K, Ellison, AR, Mohammed, RS, van Oosterhout, C, Whittey, KE, Perkins, SE and Cable, J (2019) Long-term cleaning patterns of the sharknose goby (Elacatinus evelynae). Coral Reefs 38, 321330.CrossRefGoogle Scholar
Exton, DA, Ahmadia, GN, Cullen-Unsworth, LC, Jompa, J, May, D, Rice, J, Simonin, PW, Unsworth, RKF and Smith, DJ (2019) Artisanal fish fences pose broad and unexpected threats to the tropical coastal seascape. Nature Communications 10, 19.CrossRefGoogle ScholarPubMed
Floeter, SR, Vázquez, DP and Grutter, AS (2007) The macroecology of marine cleaning mutualisms. Journal of Animal Ecology 76, 105111.CrossRefGoogle ScholarPubMed
Froese, R. and Pauly, D (eds) (2000) Fishbase 2000: Concepts, Designs and Data Sources. Los Baños, Laguna: ICLARM.Google Scholar
Grutter, AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Marine Ecology Progress Series 115, 2130.CrossRefGoogle Scholar
Grutter, AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proceedings of the Royal Society of London B: Biological Sciences 268, 13611365.CrossRefGoogle ScholarPubMed
Grutter, AS and Poulin, R (1998) Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Marine Ecology Progress Series 164, 263271.CrossRefGoogle Scholar
Grutter, AS, Murphy, JM and Choat, JH (2003) Cleaner fish drives local fish diversity on coral reefs. Current Biology 13, 6467.CrossRefGoogle ScholarPubMed
Huebner, LK and Chadwick, NE (2012 a) Patterns of cleaning behaviour on coral reef fish by the anemone shrimp Ancylomenes pedersoni. Journal of the Marine Biological Association of the United Kingdom 92, 15571562.CrossRefGoogle Scholar
Huebner, LK and Chadwick, NE (2012 b) Reef fishes use sea anemones as visual cues for cleaning interactions with shrimp. Journal of Experimental Marine Biology and Ecology 416, 237242.CrossRefGoogle Scholar
Huebner, LK, Shea, CP, Schueller, PM, Terrell, AD, Ratchford, SG and Chadwick, NE (2019) Crustacean symbiosis with Caribbean sea anemones Bartholomea annulata: occupancy modeling, habitat partitioning, and persistence. Marine Ecology Progress Series 631, 99116.CrossRefGoogle Scholar
Hughes, TP, Anderson, KD, Connolly, SR, Heron, SF, Kerry, JT, Lough, JM, Baird, AH, Baum, JK, Berumen, ML, Bridge, TC, Claar, DC, Eakin, CM, Gilmour, JP, Graham, NAJ, Harrison, H, Hobbs, JPA, Hoey, AS, Hoogenboom, M, Lowe, RJ, McCulloch, MT, Pandolfi, JM, Pratchett, M, Schoepf, V, Torda, G and Wilson, SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science (New York, N.Y.) 359, 8083.CrossRefGoogle ScholarPubMed
Hunt, CL, Kelly, GR, Windmill, H, Curtis-Quick, J, Conlon, H, Bodmer, MDV, Rogers, AD and Exton, DA (2019) Aggregating behaviour in invasive Caribbean lionfish is driven by habitat complexity. Scientific Reports 9, 19.CrossRefGoogle ScholarPubMed
Kopp, D, Bouchon-Navaro, Y, Louis, M, Legendre, P and Bouchon, C (2010) Spatial and temporal variation in a Caribbean herbivorous fish assemblage. Journal of Coastal Research 28, 6372.Google Scholar
Kulbicki, M and Arnal, C (1999) Cleaning of fish ectoparasites by a Palaemonidae shrimp on soft bottoms in New Caledonia. Cybium 23, 101104.Google Scholar
Limbaugh, C, Pederson, H and Chace, FA (1961) Shrimps that clean fishes. Bulletin of Marine Science 11, 237257.Google Scholar
Mahnken, C (1972) Observations on cleaner shrimps of the genus Periclimenes. Bulletin of the Natural History Museum of Los Angeles County 14, 7183.Google Scholar
Marcogliese, D (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124, 8399.CrossRefGoogle ScholarPubMed
Martínez, M, Luis, M, Gutiérrez-Estrada, JC, Mazenet-González, J and Soriguer, MC (2010) Seasonal patterns of three fish species in a Caribbean coastal gill-net fishery: biologically induced or climate-related aggregations? Fisheries Research 106, 358367.CrossRefGoogle Scholar
Mascaró, M, Rodríguez-Pestaña, L, Chiappa-Carrara, X and Simões, N (2012) Host selection by the cleaner shrimp Ancylomenes pedersoni: do anemone host species, prior experience or the presence of conspecific shrimp matter? Journal of Experimental Marine Biology and Ecology 413, 8793.CrossRefGoogle Scholar
McCammon, A, Sikkel, P and Nemeth, D (2010) Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment. Coral Reefs 29, 419426.CrossRefGoogle Scholar
Mumby, PJ and Wabnitz, CCC (2002) Spatial patterns of aggression, territory size, and harem size in five sympatric Caribbean parrotfish species. Environmental Biology of Fishes 63, 265279.CrossRefGoogle Scholar
Nizinski, MS (1989) Ecological distribution, demography and behavioral observations on Periclimenes anthophilus, an atypical symbiotic cleaner shrimp. Bulletin of Marine Science 45, 174188.Google Scholar
O'Reilly, E, Titus, BM, Nelsen, MW, Ratchford, MW and Chadwick, NE (2018) Giant ephemeral anemones? Rapid growth and high mortality in the corkscrew sea anemone Bartholomea annulata under variable conditions. Journal of Experimental Marine Biology and Ecology 509, 4453.CrossRefGoogle Scholar
Potts, GW (1973) The ethology of Labroides dimidiatus (cuv. & val.) (Labridae. Pisces) on Aldabra. Animal Behaviour 21, 250291.CrossRefGoogle Scholar
R CoreTeam (2013) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Robertson, DR, Schober, UM and Brawn, JD (1993) Comparative variation in spawning output and juvenile recruitment of some Caribbean reef fishes. Marine Ecology Progress Series 94, 105113.CrossRefGoogle Scholar
Rosa, R, Lopes, AR, Pimentel, M, Faleiro, F, Baptista, M, Trübenbach, K, Narcisco, L, Dionísio, G, Pegado, MR, Repolho, T, Calado, R and Diniz, M (2014) Ocean cleaning stations under a changing climate: biological responses of tropical and temperate fish-cleaner shrimp to global warming. Global Change Biology 20, 30683079.CrossRefGoogle Scholar
Sasal, P, Mouillot, D, Fichez, R, Chifflet, S and Kulbicki, M (2007) The use of fish parasites as biological indicators of anthropogenic influences in coral-reef lagoons: a case study of Apogonidae parasites in New-Caledonia. Marine Pollution Bulletin 54, 16971706.CrossRefGoogle ScholarPubMed
Sazima, I, Sazima, C, Francini-Filho, RB and Moura, RL (2000) Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeast Brazil. Environmental Biology of Fishes 59, 6977.CrossRefGoogle Scholar
Sazima, C, Guimarães, PR Jr, Dos Reis, SF and Sazima, I (2010) What makes a species central in a cleaning mutualism network? Oikos 119, 13191325.CrossRefGoogle Scholar
Sikkel, PC (2000) Habitat/sex differences in time at cleaning stations and ectoparasite loads in a Caribbean reef fish. Marine Ecology Progress Series 193, 191199.CrossRefGoogle Scholar
Sikkel, PC, Cheney, KL and Côté, IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Animal Behaviour 68, 241247.CrossRefGoogle Scholar
Silvano, RAM, Tibbetts, I and Grutter, A (2012) Potential effects of fishing on cleaning interactions in a tropical reef. Coral Reefs 31, 11931198.CrossRefGoogle Scholar
Simpson, EH (1949) Measurement of diversity. Nature 163, 688.CrossRefGoogle Scholar
Smit, NJ, Bruce, NL and Hadfield, KA (2014) Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. International Journal for Parasitology: Parasites and Wildlife 3, 188197.Google ScholarPubMed
Sullivan, KM and Sluka, R (1996) The ecology of shallow-water groupers (Pisces: Serranidae) in the upper Florida Keys, USA. In Biology, Fisheries and Culture of Tropical Groupers and Snappers. ICLARM Conference Proceedings 48, 7484.Google Scholar
Sun, D, Cheney, KL, Werminghausen, J, Meekan, MG, McCormick, MI, Cribb, TH and Grutter, AS (2015) Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs. Biology Letters 11, 20150456.CrossRefGoogle ScholarPubMed
Titus, BM and Daly, M (2015) Fine-scale phylogeography reveals cryptic biodiversity in Pederson's cleaner shrimp, Ancylomenes pedersoni (Crustacea: Caridea: Palaemonidae), along the Florida Reef Tract. Marine Ecology 36, 13791390.CrossRefGoogle Scholar
Titus, BM and Daly, M (2017) Specialist and generalist symbionts show counterintuitive levels of genetic diversity and discordant demographic histories along the Florida Reef Tract. Coral Reefs 36, 339354.CrossRefGoogle Scholar
Titus, BM, Daly, M and Exton, DA (2015 a) Do reef fish habituate to diver presence? Evidence from two reef sites with contrasting historical levels of SCUBA intensity in the Bay Islands, Honduras. PLoS ONE 10, e0119645.CrossRefGoogle ScholarPubMed
Titus, BM, Daly, M and Exton, DA (2015 b) Temporal patterns of Pederson shrimp (Ancylomenes pedersoni Chace 1958) cleaning interactions on Caribbean coral reefs. Marine Biology 162, 16511664.CrossRefGoogle Scholar
Titus, BM, Palombit, S and Daly, M (2017 a) Endemic diversification in an isolated archipelago with few endemics: an example from a cleaner shrimp species complex in the Tropical Western Atlantic. Biological Journal of the Linnean Society 122, 98112.CrossRefGoogle Scholar
Titus, BM, Vondriska, C and Daly, M (2017 b) Comparative behavioural observations demonstrate the ‘cleaner’ shrimp Periclimenes yucatanicus engages in true symbiotic cleaning interactions. Open Science 4, 170078.Google ScholarPubMed
Titus, BM, Daly, M, Vondriska, C, Hamilton, I and Exton, DA (2019) Lack of strategic service provisioning by Pederson's cleaner shrimp (Ancylomenes pedersoni) highlights independent evolution of cleaning behaviors between ocean basins. Scientific Reports 9, 629.CrossRefGoogle ScholarPubMed
Vaughan, DB, Grutter, AS, Costello, MJ and Hutson, KS (2017) Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses. Fish and Fisheries 18, 698716.CrossRefGoogle Scholar
Watson, DL and Harvey, ES (2007) Behaviour of temperate and sub-tropical reef fishes towards a stationary SCUBA diver. Marine and Freshwater Behaviour and Physiology 40, 85103.CrossRefGoogle Scholar
White, JW, Grigsby, C and Warner, R (2007) Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish. Coral Reefs 26, 8794.CrossRefGoogle Scholar