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Decreased movement related to parasite infection in a diel migratory coral reef fish

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Abstract

Risk of infection by parasites may be an important contributing cause or consequence of animal movement patterns. The diel movement patterns of French grunt, a common Caribbean coral reef fish, are well documented and known to connect reef and seagrass habitat. In the northeastern Caribbean, French grunts are known to be infected by Anilocra haemuli, one of the largest and most conspicuous ectoparasitic isopods. Studies on Anilocra infection have demonstrated that infection reduces host swimming performance and condition and may alter host behavior. We tested predictions of the hypothesis that A. haemuli infection influences the movement patterns of host French grunt, specifically whether short-distance daytime movements and/or reef–seagrass migration at dusk was associated with infection. We conducted focal observations on infected and uninfected fish during both daytime resting and dusk migration periods. We also conducted daytime and nocturnal surveys in reef habitat, documenting changes in the proportion of infected individuals. We found that infected fish move significantly less than uninfected conspecifics during the day and observed 100 % of uninfected focal fish and 37.5 % of infected focal fish departing the reef during dusk. In reef habitat, the proportion of fish infected with Anilocra was also significantly greater at night compared to daytime. We suggest that A. haemuli infection alters host movement patterns and that parasitism may therefore indirectly influence trophic connectivity between reef and seagrass ecosystems.

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References

  • Adamo SA (2003) Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav Evol 60:370–377

    Article  Google Scholar 

  • Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302

    Article  CAS  PubMed  Google Scholar 

  • Appeldoorn RS, Aguilar–Perera A, Bouwmeester BLK, Dennis GD, Hill RL, Mertern W, Recksiek CW, Williams SJ (2009) Movement of fishes (Grunts: Haemulidae) across the coral reef seascape: a review of scales, patterns and processes. Caribb J Sci 45:304–316

    Google Scholar 

  • Arias-González JE, Morand S (2006) Trophic functioning with parasites: a new insight for ecosystem analysis. Mar Ecol Prog Ser 320:43–53

    Article  Google Scholar 

  • Arnal C, Côté IM, Morand S (2001) Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behav Ecol Sociobiol 51:1–7

    Article  Google Scholar 

  • Baker RR (1978) The evolutionary ecology of animal migration. Hodder and Staughton, London

    Google Scholar 

  • Bakker TCM, Mazzi D, Zala S (1997) Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78:1098–1104

    Article  Google Scholar 

  • Bartel RA, Oberhauser KS, De Roode JC, Altizer SM (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92:342–351

    Article  PubMed  Google Scholar 

  • Binning SA, Roche DG, Layton C (2013) Ectoparasites increase swimming costs in coral reef fish. Biol Lett 9: 20120927

  • Binning SA, Barnes JI, Davies JN, Backwell PR, Keogh JS, Roche DG (2014) Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Anim Behav 93:1–7

    Article  Google Scholar 

  • Bloomfield AL, Gillanders BM (2005) Fish and invertebrate assemblages in seagrass, mangrove, saltmarsh, and nonvegetated habitats. Coast Estuar Res Fed 28:63–77

    Article  Google Scholar 

  • Boisclair D, Tang M (1993) Empirical analysis of the influence of swimming pattern on the net energetic cost of swimming in fishes. J Fish Biol 42:169–183

    Article  Google Scholar 

  • Börger L, Dalziel BD, Fryxell JM (2008) Are there general mechanisms of animal home range behaviour? A review and prospects for future research. Ecol Lett 11:637–650

    Article  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Bunkley–Williams L, Williams EH (1981) Nine new species of Anilocra (Crustacea: Isopoda: Cymothoidae) external parasites of West Indian coral reef fishes. P Biol Soc Wash 94:1005–1047

  • Bunkley–Williams L, Williams EH (1998) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–896

    Article  PubMed  Google Scholar 

  • Byers JE (2009) Including parasites in food webs. Trends Parasitol 25:55–57

    Article  PubMed  Google Scholar 

  • Cheney KL, Côté IM (2001) Are Caribbean cleaning symbioses mutualistic? Costs and benefits of visiting cleaning stations to longfin damselfish. Anim Behav 62:927–933

    Article  Google Scholar 

  • Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165

    Article  PubMed Central  PubMed  Google Scholar 

  • Clark RD, Pittman S, Caldow C, Christensen J, Roque B, Appeldoorn RS, Monaco ME (2009) Nocturnal fish movement and trophic flow across habitat boundaries in a coral reef ecosystem (SW Puerto Rico). Caribb J Sci 45:282–303

    Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) (2001) Dispersal. Oxford Univ Press, Oxford

    Google Scholar 

  • Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896

    Article  CAS  PubMed  Google Scholar 

  • Coile AM, Welicky RL, Sikkel PC (2014) Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol Res 113:3875–80

    Article  CAS  PubMed  Google Scholar 

  • Danilowicz BS, Sale PF (1999) Relative intensity of predation on the French grunt, Haemulon flavolineatum, during diurnal, dusk, and nocturnal periods on a coral reef. Mar Biol 133:337–343

    Article  Google Scholar 

  • Dowgiallo MJ (1979) Variation of metazoan parasites of the French grunt Haemulon flavolineatum (Demarest) (Osteichthyes: Pomadasyidae), by habitat type and season with an analysis of competition among parasites. Masters Thesis, Univ Puerto Rico–Mayagüez

  • Dumont HJ, Hinnekint BON (1973) Mass migration in dragonflies, especially in Libellula quadrimaculata L.: a review, a new ecological approach and a new hypothesis. Odonatologica 2:1–20

    Google Scholar 

  • Dyer WG, Williams EH, Bunkley–Williams L (1992) Homalometron dowgialloi sp. n. (Homalometridae) from Haemulon flavolineatum and additional records of digenetic trematodes of marine fishes in the West Indies. J Helminthol Soc Wash 59:182–189

    Google Scholar 

  • Ezenwa VO (2004) Host social behavior and parasitic infection: a multifactorial approach. Behav Ecol 15:446–454

    Article  Google Scholar 

  • Firth D (1993) Bias reduction of maximum likelihood estimates. Biometrika 80:27–38

    Article  Google Scholar 

  • Fish FE (2010) Swimming strategies for energy economy. In: Domenici P, Kapoor BD (eds) Fish locomotion: an eco-ethological perspective. Science Publishers, Springer, US, pp 90–122

    Chapter  Google Scholar 

  • Fogelman RM, Grutter AS (2008) Mancae of the parasitic cymothoid isopod, Anilocra apogonae: early life history, host-specificity, and effect on growth and survival of preferred young cardinal fishes. Coral Reefs 27:685–693

    Article  Google Scholar 

  • Fogelman RM, Kuris AM, Grutter AS (2009) Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus. Int J Parasitol 39:577–83

    Article  PubMed  Google Scholar 

  • Folstad I, Nilssen AC, Halvorsen O, Andersen J (1991) Parasite avoidance: the cause of post-calving migrations in Rangifer? Can J Zool 69:2423–2429

    Article  Google Scholar 

  • Fulton CJ (2010) The role of swimming in reef fish ecology. In: Domenici P, Kapoor BD (eds) Fish locomotion: an eco-ethological perspective. Science Publishers, Springer, US, pp 333–373

    Google Scholar 

  • Grant JWA (1997) Territoriality. In: Godin J-GJ (ed) Behavioural ecology of teleost fishes. Oxford University Press, Oxford, pp 81–103

  • Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58

    Article  Google Scholar 

  • Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673

    Article  CAS  Google Scholar 

  • Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. P Roy Soc Lond B 268:1361–1365

    Article  CAS  Google Scholar 

  • Hadfield KA, Sikkel PC, Smit NJ (2014) New records of fish parasitic isopods of the gill-attaching genus Mothocya Costa, in Hope, 1851 from the Virgin Islands, Caribbean, with description of a new species. Zookeys 439:109–125

    Article  PubMed  Google Scholar 

  • Hatcher MJ, Dick JT, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194

    Article  Google Scholar 

  • Helfman GS (1986) Fish behaviour by day, night and twilight. In: Pitcher TJ (ed) The behaviour of teleost fishes. Croom Helm, London, pp 366–387

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

    Article  Google Scholar 

  • Kaldonski N, Perrot-Minnot MJ, Cézilly F (2007) Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim Behav 74:1311–1317

    Article  Google Scholar 

  • Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129:159–164

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD (1999) The evolution of trophic transmission. Parasitol Today 15:111–115

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Morris AK (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397

    Article  Google Scholar 

  • Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Landeau L, Terborgh J (1986) Oddity and the ‘confusion effect’ in predation. Anim Behav 34:1372–1380

    Article  Google Scholar 

  • Lima SL, Zollner PA (1996) Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol 11:131–135

    Article  CAS  PubMed  Google Scholar 

  • Marcogliese DJ, Cone DK (1997) Food webs: a plea for parasites. Trends Ecol Evol 12:320–325

    Article  CAS  PubMed  Google Scholar 

  • McFarland W (1980) Observations on recruitment in haemulid fishes. P Gulf Caribb Fish Inst 32:132–138

    Google Scholar 

  • McFarland WN (1991) The visual world of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic, San Diego, pp 289–297

    Google Scholar 

  • McFarland WN, Wahl CM (1996) Visual constraints on migration behavior of juvenile French grunts. Environ Biol Fish 46:109–122

    Article  Google Scholar 

  • McFlarland W, Ogden J, Lythgoe J (1979) The influence of light on the twilight migrations of grunts. Environ Biol Fish 4:9–22

    Article  Google Scholar 

  • Meadows DW, Meadows CM (2003) Behavioral and ecological correlates of foureye butterflyfish, Chaetodon capistratus, (Perciformes: Chaetodontidae) infected with Anilocra chaetodontis (Isopoda: Cymothoidae). Rev Biol Trop 51(Suppl 4):77–81

    PubMed  Google Scholar 

  • Mikheev VN, Pasternak AF (2006) Defense behavior of fish against predators and parasites. J Ichthyol 46:S173–S179

    Article  Google Scholar 

  • Miller AA, Poulin R (2001) Parasitism, movement, and distribution of the snail Diloma subrostrata (Trochidae) in a soft-sediment intertidal zone. Can J Zool 79:2029–2035

    Article  Google Scholar 

  • Milner–Gulland EJ, Fryxell JM, Sinclair ARE (2011) Animal migration: a synthesis. Oxford Univ Press, Oxford

    Book  Google Scholar 

  • Møller AP, Szép T (2011) The role of parasites in ecology and evolution of migration and migratory connectivity. J Ornithol 152:141–150

    Article  Google Scholar 

  • Møller AP, de Lope F, Saino N (2004) Parasitism, immunity, and arrival date in a migratory bird, the barn swallow. Ecology 85:206–219

    Article  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford Univ Press, Oxford

    Google Scholar 

  • Mooring MS, Hart BL (1992) Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123:173–193

    Article  Google Scholar 

  • Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA, Merrill EH, Haydon DT (2010) Building the bridge between animal movement and population dynamics. Philos T Roy Soc B 365:2289–301

    Article  Google Scholar 

  • Morand S, Arias–González JE (1997) Is parasitism a missing ingredient in model ecosystems? Ecol Model 95:61–74

    Article  Google Scholar 

  • Mumby P, Edwards A, Arias–González JE et al (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536

    Article  CAS  PubMed  Google Scholar 

  • Nagelkerken I, van der Velde G (2004) Relative importance of interlinked mangroves and seagrass beds as feeding habitats for juvenile reef fish on a Caribbean island. Mar Ecol Prog Ser 274:153–159

    Article  Google Scholar 

  • Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Moriniére E, van der Velde G (2000a) Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog Ser 194:55–64

    Article  Google Scholar 

  • Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Moriniére E, van der Velde G (2000b) Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Mar Ecol Prog Ser 202:175–192

    Article  Google Scholar 

  • Nagelkerken I, Kleijnen S, Klop T, van den Brand RACJ, Cocheret de la Moriniére E, van der Velde G (2001) Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves/seagrass beds. Mar Ecol Prog Ser 214:225–235

    Article  Google Scholar 

  • Nagelkerken I, Roberts CM, van der Velde G, Dorenbosch M, van Riehl MC, Cocheret de la Moriniére E, Nienhuis PH (2002) How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Mar Ecol Prog Ser 244:299–305

    Article  Google Scholar 

  • Nakamura Y, Sano M (2005) Comparison of invertebrate abundance in a seagrass bed and adjacent coral and sand areas at Amitori Bay, Iriomote Island, Japan. Fish Sci 71:543–550

    Article  CAS  Google Scholar 

  • Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105:19052–19059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogden JC, Zieman JC (1977) Ecological aspects of coral reef–seagrass bed contacts in the Caribbean. Third Int Coral Reef Symp, Miami, pp 377–382

    Google Scholar 

  • Ostlund–Nilsson S, Curtis L, Nilsson GE, Grutter AS (2005) Parasitic isopod Anilocra apogonae, a drag for the cardinal fish Cheilodipterus quinquelineatus. Mar Ecol Prog Ser 287:209–216

    Article  Google Scholar 

  • Owen–Smith N, Fryxell JM, Merrill EH (2010) Foraging theory upscaled: the behavioural ecology of herbivore movement. Philos T Roy Soc B 365:2267–2278

    Article  Google Scholar 

  • Parrish JK, Viscido SV, Grünbaum D (2002) Self-organized fish schools: an examination of emergent properties. Biol Bull 202:296–305

    Article  PubMed  Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study Behav 41:151–186

    Article  Google Scholar 

  • Poulin R, FitzGerald GJ (1989a) Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.). Behav Ecol Sociobiol 24:251–255

    Article  Google Scholar 

  • Poulin R, FitzGerald GJ (1989b) Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can J Zool 67:14–18

    Article  Google Scholar 

  • Poulin R, Grutter AS (1996) Proximate symbioses: cleaning and adaptive explanation. Bioscience 46:512–517

    Article  Google Scholar 

  • Poulin R, Closs GP, Lill AW, Hicks AS, Herrmann KK, Kelly DW (2012) Migration as an escape from parasitism in New Zealand galaxiid fishes. Oecologia 169:955–963

    Article  PubMed  Google Scholar 

  • Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5:297–307

    Article  PubMed  Google Scholar 

  • Rodgers GM, Kelley JL, Morrell LJ (2010) Colour change and assortment in the western rainbowfish. Anim Behav 79:1025–1030

    Article  Google Scholar 

  • Schreck CB, Olla BL, Davis MW (1997) Behavioural response to stress. In: Iwama G, Pickering A, Sumpter J, Schreck C (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 145–170

    Google Scholar 

  • Seppälä O, Karvonen A, Tellervo Valtonen E (2005) Impaired crypsis of fish infected with a trophically transmitted parasite. Anim Behav 70:895–900

    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 

  • Sikkel PC, Herzlieb S, Kramer D (2005) Compensatory cleaner-seeking behavior following spawning in female yellowtail damselfish. Mar Ecol Prog Ser 296:1–11

    Article  Google Scholar 

  • Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689

    Article  Google Scholar 

  • Sikkel PC, Ziemba RE, Sears WT, Wheeler JC (2009) Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28:489–495

    Article  Google Scholar 

  • Verweij MC, Nagelkerken I, Wartenbergh SLJ, Pen IR, van der Velde G (2006) Caribbean mangroves and seagrass beds as daytime feeding habitats for juvenile French grunts, Haemulon flavolineatum. Mar Biol 149:1291–1299

    Article  Google Scholar 

  • Welicky RL, Sikkel PC (2014) Variation in occurrence of the fish–parasitic cymothoid isopod, Anilocra haemuli, infecting French grunt (Haemulon flavolineatum) in the North-eastern Caribbean. Mar Freshw Res 65:1018–1026

    Article  CAS  Google Scholar 

  • Wendelaar Bonga S (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  • Wikelski M, Hau M (1995) Is there an endogenous tidal foraging rhythm in marine iguanas? J Biol Rhythm 10:335–350

    Article  CAS  Google Scholar 

  • Williams EH, Bunkley–Williams L, Dowgiallo MJ, Dyer WG (2014) Influence of collection methods on the occurrence of alimentary canal helminth parasites in fish. J Parasitol 77:1019–1022

    Article  Google Scholar 

  • Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH (2007) Parasites alter community structure. Proc Natl Acad Sci USA 104:9335–9339

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank J. Artim, E. Brill, A. McCammon, J. Sellers, L. Renoux, W. Jenkins, and the staff of the Virgin Islands Environmental Resource Station for logistic support. We also thank S. Binning and an anonymous reviewer for their invaluable feedback on the manuscript. A portion of the fieldwork reported herein was also supported by the U.S. National Science Foundation (OCE OCE-121615, PC Sikkel, PI). This is contribution number 135 from the University of the Virgin Islands Center for Marine and Environmental Studies.

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All activities reported herein are in compliance with the laws of the US Virgin Islands and US National Park System.

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  1. Department of Biological Sciences and Environmental Sciences Program, Arkansas State University, PO Box 599, State University, AR, 72647, USA

    R. L. Welicky & P. C. Sikkel

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Correspondence to P. C. Sikkel.

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Welicky, R.L., Sikkel, P.C. Decreased movement related to parasite infection in a diel migratory coral reef fish. Behav Ecol Sociobiol 69, 1437–1446 (2015). https://doi.org/10.1007/s00265-015-1956-3

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