Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-19T13:16:26.043Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite-mediated host behavioural modifications: Gyrodactylus turnbulli infected Trinidadian guppies increase contact rates with uninfected conspecifics

Published online by Cambridge University Press:  08 November 2017

Michael Reynolds Open the ORCID record for Michael Reynolds [Opens in a new window] ,
Elisavet A. Arapi  and
Jo Cable
Michael Reynolds*
Affiliation:
School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK
Elisavet A. Arapi
Affiliation:
School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK
Jo Cable
Affiliation:
School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK
*
Author for correspondence: Michael Reynolds, E-mail: reynoldsm4@cardiff.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

While group formation provides antipredatory defences, increases foraging efficiency and mating opportunities, it can be counterintuitive by promoting disease transmission amongst social hosts. Upon introduction of a pathogen, uninfected individuals often modify their social preferences to reduce infection risk. Infected hosts also exhibit behavioural changes, for example, removing themselves from a group to prevent an epidemic. Conversely, here we show how Trinidadian guppies infected with a directly transmitted ectoparasite, Gyrodactylus turnbulli, significantly increase their contact rates with uninfected conspecifics. As uninfected fish never perform this behaviour, this is suggestive of a parasite-mediated behavioural response of infected hosts, presumably to offload their parasites. In the early stages of infection, however, such behavioural modifications are ineffective in alleviating parasite burdens. Additionally, we show that fish exposed to G. turnbulli infections for a second time, spent less time associating than those exposed to parasites for the first time. We speculate that individuals build and retain an infection cue repertoire, enabling them to rapidly recognize and avoid infectious conspecifics. This study highlights the importance of considering host behavioural modifications when investigating disease transmission dynamics.

Keywords

GyrodactylusPoecilia reticulatasocialityinfectious diseasetransmission dynamicsbehavioural modification
Type
Research Article
Information
Parasitology , Volume 145 , Issue 7 , June 2018 , pp. 920 - 926
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Adamo, SA and Webster, JP (2013) Neural parasitology: how parasites manipulate host behaviour. Journal of Experimental Biology 216, 1–2.CrossRefGoogle ScholarPubMed
Alexander, RD (1974) The evolution of social behaviour. Annual Review of Ecology, Evolution and Systematics 5, 325–383.Google Scholar
Bakke, TA, Cable, J and Harris, PD (2007) The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Advances in Parasitology 64, 161–378.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-6. http://CRAN.R-project.org/package=lme4.Google Scholar
Bell, DC, Atkinson, JS and Carlson, W (1999) Centrality measures for disease transmission networks. Social Networks 21, 1–21.CrossRefGoogle Scholar
Boeger, WA, Kritsky, DC, Pie, MR and Engers, KB (2005) Mode of transmission, host switching, and escape from the Red Queen by viviparous gyrodactylids (Monogenoidea). Journal of Parasitology 91, 1000–1007.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, J-SS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127–135.Google Scholar
Buchmann, K (1998) Binding and lethal effect of complement from Oncorhynchus mykiss on Gyrodactylus derjavini (Platyhelminthes: Monogenea). Diseases of Aquatic Organisms 32, 195–200.CrossRefGoogle ScholarPubMed
Buchmann, K and Bresciani, J (1998) Microenvironment of Gyrodactylus derjavini: association between mucous cell density and microhabitat selection. Parasitology Research 84, 17–24.Google Scholar
Cable, J and van Oosterhout, C (2007) The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biological Journal of the Linnean Society 90, 647–655.Google Scholar
Cable, J, Scott, ECG, Tinsley, RC and Harris, PD (2002) Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. Journal of Parasitology 88, 183–184.CrossRefGoogle ScholarPubMed
Côté, IM (2000) Evolution and ecology of cleaning symbiosis in the sea. Oceangeographic Marine Biology 38, 311–355.Google Scholar
Côté, IM and Poulin, R (1995) Parasitism and group size in social animals: a meta-analysis. Behavioural Ecology 6, 159–165.Google Scholar
Craft, ME (2015) Infectious disease transmission and contact networks in wildlife and livestock. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20140107.Google Scholar
Croft, DP, Krause, J and James, R (2004) Social networks in the guppy (Poecilia reticulata). Proceedings of the Royal Society of London B: Biological Sciences 271, 516–519.Google Scholar
Croft, DP, Edenbrown, M, Darden, SK, Ramnarine, IW, van Oosterhout, C and Cable, J (2011) Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies Poecilia reticulata. Behavioural Ecology and Sociobiology 65, 2219–2227.Google Scholar
Curtis, VA (2014) Infection-avoidance behaviour in humans and other animals. Trends in Immunology 35, 457–464.Google Scholar
Danon, L, Ford, AP, House, T, Jewell, CP, Keeling, MJ, Roberts, GO, Ross, JV and Vernon, MC (2011) Networks and the epidemiology of infectious disease. Interdisciplinary Perspectives on Infectious Diseases 2011, 284909.Google Scholar
Duncan, P and Vigne, N (1979) Effect of group-size in horses on the rate of attacks by blood-sucking flies. Animal Behaviour 27, 623–625.Google Scholar
Faria, PJ, van Oosterhout, C and Cable, J (2010) Optimal release strategies for captive-bred animals in reintroduction programs: experimental infections using the guppy as a model organism. Biological Conservation 143, 35–41.CrossRefGoogle Scholar
Glaser, R and Kiecolt-Glaser, JK (2005) Stress-induced immune dysfunction: implications for health. Nature Reviews Immunology 5, 243–251.Google Scholar
Griffiths, SW and Magurran, AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Animal Behaviour 56, 689–693.CrossRefGoogle ScholarPubMed
Grutter, A (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Inter-Research Marine Ecology Progress Series 130, 61–70.Google Scholar
Hart, BL (2011) Behavioural defences in animals against pathogens and parasite: parallels with the pillars of medicine in humans. Philosophical Transactions of the Royal Society B: Biological Sciences 366, 3406–3417.Google Scholar
Heinze, J and Walter, B (2010) Moribund ants leave their nests to die in social isolation. Current Biology 20, 249–252.Google Scholar
Johnson, MB, Lafferty, KD, van Oosterhout, C and Cable, J (2011) Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE 6, e22634.CrossRefGoogle ScholarPubMed
Kiesecker, JM, Skelly, DK, Beard, KH and Preisser, E (1999) Behavioural reduction of infection risk. Proceedings of the National Academy of Sciences USA 96, 9165–9168.Google Scholar
Kolluru, GT, Grether, GF, Dunlop, E and South, SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behavioural Ecology 20, 131–137.Google Scholar
Koprivnikar, J and Penalva, L (2015) Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLoS ONE 10, e0116569.Google Scholar
Krause, J and Ruxton, GD (2002) Living in Groups. Oxford, UK: Oxford University Press.Google Scholar
Lloyd-Smith, JO, Schreiber, SJ, Kopp, PE and Getz, WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.CrossRefGoogle ScholarPubMed
Mateo, JM (2004) Recognition systems and biological organization: the perception component of social recognition. Annales Zoologici Fennici 41, 729–745.Google Scholar
Mohammed, RS, Reynolds, M, James, J, Williams, C, Mohammed, A, Ramsubhag, A, van Oosterhout, C and Cable, J (2016) Getting into hot water: sick guppies frequent warmer thermal conditions. Oecologia 181, 911–917.Google Scholar
Moore, MM, Kaattari, SL and Olson, RE (1994) Biologically active factors against the monogenetic trematodes Gyrodactylus stellatus in the serum and mucus of infected juvenile English soles. Journal of Aquatic Animal Health 6, 93–100.Google Scholar
Mooring, MS and Hart, BL (1992) Animal grouping for protection from parasites: selfish herd and ecounter-dilution effects. Behaviour 123, 173–193.Google Scholar
Mooring, MS, McKenzie, AA and Hart, BL (1996) Grooming in impala: role of oral grooming in removal of ticks and effects of ticks in increasing grooming rate. Physiology and Behaviour 59, 965–971.Google Scholar
Patterson, JE and Ruckstuhl, KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology.CrossRefGoogle Scholar
Paxton, CG (1996) Isolation and the development of shoaling in two populations of the guppy. Journal of Fish Biology 49, 514–520.Google Scholar
Pie, MR, Engers, KB and Boeger, WA (2006) Density-dependent topographical specialization in Gyrodactylus anisophyarynx (Monogenoidea, Gyrodactylidae): boosting transmission or evading competition? Journal of Parasitology 92, 459–463.Google Scholar
Pinheiro, JC and Bates, DM (2000) Linear mixed-effects models: basic concepts and examples. In Chambers J, Eddy W, Härdle W, Sheather S and Tierney L (eds). Mixed-Effects Models in S and S-PLUS. Statistics and Computing. New York, NY: Springer, pp. 3–56. doi: 10.1007/0-387-22747-4_1.Google Scholar
Pitcher, TJ (1983) Heuristic definitions of shoaling behaviour. Animal Behaviour 31, 611–163.Google Scholar
Pitcher, TJ, Magurran, AE and Allan, JR (1983) Shifts of behaviour with shoal size in cyprinids. Proceedings of the British Freshwater Fisheries Conference 3, 220–228.Google Scholar
Poirotte, C, Massol, F, Herbert, A, Willaume, E, Bomo, PM, Kappeler, PM and Charpentier, MJE (2017) Madrills use olfaction to socially avoid parasitized conspecifics. Science Advances 3, e1601721.Google Scholar
Proudfoot, K and Habing, G (2015) Social stress as a cause of diseases in farm animals: current knowledge and future direction. The Veterinary Journal 206, 15–21.Google Scholar
Rätti, O, Ojanen, U and Helle, P (2006) Increasing group size dilutes black fly attack rate in Black Grouse. Ornis Fennica 83, 86–90.Google Scholar
R Development Core Team (2009) R: A Language and Environment for Statistical Computing: The R Foundation for Statistical Computing. Vienna, Austria.Google Scholar
Reynolds, WW, Casterlin, ME and Covert, JB (1976) Behavioural fever in teleost fish. Nature 259, 41–42.CrossRefGoogle Scholar
Richards, GR and Chubb, J (1996) Host response to initial and challenge infections, following treatment, of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on the guppy (Poecilia reticulata). Parasitology Research 82, 242–247.Google Scholar
Rodgers, GM, Ward, JR, Askwith, B and Morrell, LJ (2011) Balancing the dilution and oddity effects. Decisions depend on body size. PLoS ONE 6, e14819.Google Scholar
Rueppell, O, Hayworth, MK and Ross, NP (2010) Altruistic self-removal of health-compromised honey bee workers from their hive. Journal of Evolutionary Biology 23, 1538–1546.Google Scholar
Sansom, A, Lind, J and Cresswell, W (2009) Individual behaviour and survival: the roles of predator avoidance, foraging success, and vigilance. Behavioural Ecology 20, 1168–1174.CrossRefGoogle Scholar
Schelkle, B, Snellgrove, D and Cable, J (2013) In vitro and in vivo efficacy of garlic compounds against Gyrodactylus turnbulli infecting the guppy (Poecilia reticulata). Veterinary Parasitology 198, 96–101.Google Scholar
Schneider, SA, Scharffetter, C, Wagner, AE, Boesch, C, Bruchhaus, I, Rimbach, G and Roeder, T (2016) Social stress increases the susceptibility to infection in the ant Harpegnathos saltator. Scientific Reports 6, 25800.CrossRefGoogle ScholarPubMed
Scott, ME (1985) Dynamics of challenge infection of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). Journal of Fish Biology 8, 495–503.Google Scholar
Scott, ME and Robinson, MA (1984) Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies, Poecilia reticulata (Peters), following treatment. Journal of Fish Biology 24, 581–586.Google Scholar
Sherman, PW, Lacey, EE, Reeve, HK and Keller, L (1995) The eusociality continuum. Behavioural Ecology 6, 102–108.Google Scholar
Soto, CG, Zhang, JS and Shi, YH (1994) Intraspecific cleaning behaviour in Cyprinus carpio in aquaria. Journal of Fish Biology 44, 172–174.Google Scholar
Stephenson, JF and Reynolds, M (2016) Imprinting can cause a maladaptive preference for infectious conspecifics. Biology Letters 12, 20160020.Google Scholar
Stephenson, JF, Young, KA, Fox, J, Jokela, J, Cable, J and Perkins, SE (2017) Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160093.Google Scholar
Stoltze, K and Buchmann, K (2001) Effect of Gyrodactylus derjavini infections on cortisol production in rainbow trout fry. Journal of Helminthology 75, 291–294.Google Scholar
Titus, BM, Vondriska, C and Daly, M (2017) Comparative behavioural observations demonstrate the ‘cleaner’ shrimp Periclimenes yucatanicus engages in true symbiotic cleaning interactions. Royal Society Open Science 4, 170078.Google Scholar
Urawa, S (1992) Trichodina truttae Mueller 1937 (Ciliophora, Peritrichida) on juvenile chum salmon (Oncorhynchus keta): pathogenicity and host–parasite interactions. Fish Pathology 27, 29–37.Google Scholar
Ward, AJW, Duff, AJ, Krause, J and Barber, I (2005) Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environmental Biology of Fishes 72, 155–160.CrossRefGoogle Scholar
Wey, T, Blumstein, DT, Shen, W and Jordán, F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Animal Behaviour 75, 333–344.Google Scholar
Whitehead, H (1997) Analysing animal social structure. Animal Behaviour 53, 1053–1067.Google Scholar
Whiteman, EA and Côté, IM (2002) Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons. Journal of Fish Biology 60, 1443–1458.Google Scholar