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Modification of host social networks by manipulative parasites
In: BehaviourAbstract
Social network models provide a powerful tool to estimate infection risk for individual hosts and track parasite transmission through host populations. Here, bringing together concepts from social network theory, animal personality, and parasite manipulation of host behaviour, I argue that not only are social networks shaping parasite transmission, but parasites in turn shape social networks through their effects on the behaviour of infected individuals. Firstly, I review five general categories of behaviour (mating behaviour, aggressiveness, activity levels, spatial distribution, and group formation) that are closely tied to social networks, and provide evidence that parasites can affect all of them. Secondly, I describe scenarios in which behaviour-altering parasites can modify either the role or position of individual hosts within their social network, or various structural properties (e.g., connectance, modularity) of the entire network. Experimental approaches allowing comparisons of social networks pre- versus post-infection are a promising avenue to explore the feedback loop between social networks and parasite infections.
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-
Barber, I. & Dingemanse, N.J. (2010). Parasitism and the evolutionary ecology of animal personality. — Phil. Trans. Roy. Soc. Lond. B 365: 4077-4088.
-
Barber, I., Huntingford, F.A. & Crompton, D.W.T. (1995). The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. — J. Fish Biol. 47: 524-536.
-
Berdoy, M., Webster, J.P. & Macdonald, D.W. (2000). Fatal attraction in rats infected with Toxoplasma gondii. — Proc. Roy. Soc. Lond. B: Biol. Sci. 267: 1591-1594.
-
Bethel, W.M. & Holmes, J.C. (1973). Altered evasive behavior and responses to light in amphipods harbouring acanthocephalan cystacanths. — J. Parasitol. 59: 945-956.
-
Carney, W.P. (1969). Behavioral and morphological changes in carpenter ants harboring dicrocoelid metacercariae. — Am. Midl. Nat. 82: 605-611.
-
Cheeseman, C.L. & Mallinson, P.J. (1981). Behaviour of badgers (Meles meles) infected with bovine tuberculosis. — J. Zool. 194: 284-287.
-
Croft, D.P., Edenbrow, M., Darden, S.K., Ramnarine, I.W., van Oosterhout, C. & Cable, J. (2011). Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies Poecilia reticulata. — Behav. Ecol. Sociobiol. 65: 2219-2227.
-
Curtis, L.A. (1987). Vertical distribution of an estuarine snail altered by a parasite. — Science 235: 1509-1511.
-
Drewe, J.A. (2010). Who infects whom? Social networks and tuberculosis transmission in wild meerkats. — Proc. Roy. Soc. Lond. B: Biol. Sci. 277: 633-642.
-
Duncan, P. & Vigne, N. (1979). The effect of group size in horses on the rate of attacks by blood-sucking flies. — Anim. Behav. 27: 623-625.
-
Fenner, A.L., Godfrey, S.S. & Bull, C.M. (2011). Using social networks to deduce whether residents or dispersers spread parasites in a lizard population. — J. Anim. Ecol. 80: 835-843.
-
Forbes, M.R.L. (1991). Ectoparasites and mating success of male Enallagma ebrium damselflies (Odonata, Coenagrionidae). — Oikos 60: 336-342.
-
Fox, A. & Hudson, P.J. (2001). Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus). — Ecol. Lett. 4: 139-143.
-
Freeland, W.J. (1977). Blood-sucking flies and primate polyspecific associations. — Nature 269: 801-802.
-
Godfrey, S.S. (2013). Networks and the ecology of parasite transmission: a framework for wildlife parasitology. — Int. J. Parasitol. Parasites Wildl. 2: 235-245.
-
Godfrey, S.S., Moore, J.A., Nelson, N.J. & Bull, C.M. (2010). Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). — Int. J. Parasitol. 40: 1575-1585.
-
Gourbal, B.E.F., Lacroix, A. & Gabrion, C. (2002). Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. — Parasitol. Res. 88: 912-917.
-
Grear, D.A., Luong, L.T. & Hudson, P.J. (2013). Network transmission inference: host behavior and parasite life cycle make social networks meaningful in disease ecology. — Ecol. Appl. 23: 1906-1914.
-
Hamilton, W.D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? — Science 218: 384-386.
-
Hammond-Tooke, C.A., Nakagawa, S. & Poulin, R. (2012). Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. — Behaviour 149: 601-622.
-
Heins, D.C., Ulinski, B., Johnson, J. & Baker, J.A. (2004). Effect of the cestode macroparasite Schistocephalus pungitii on the reproductive success of ninespine stickleback, Pungitius pungitius. — Can. J. Zool. 82: 1731-1737.
-
Helluy, S. (1983). Relations hôtes-parasites du trematode Microphallus papillorobustus (Rankin, 1940). II. Modifications du comportement des Gammarus hôtes intermédiaires et localisation des métacercaires. — Ann. Parasitol. Hum. Comp. 58: 1-17.
-
Kekalainen, J., Lai, Y.T., Vainikka, A., Sirkka, I. & Kortet, R. (2014). Do brain parasites alter host personality? Experimental study in minnows. — Behav. Ecol. Sociobiol. 68: 197-204.
-
Klein, S.L. (2003). Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. — Physiol. Behav. 79: 441-449.
-
Krause, J. & Godin, J.G.J. (1994). Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanous. — Can. J. Zool. 72: 1775-1779.
-
Lester, R.J.G. (1971). The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. — Can. J. Zool. 49: 361-366.
-
Loot, G., Brosse, S., Lek, S. & Guégan, J.F. (2001). Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. — Freshwat. Biol. 46: 1219-1227.
-
MacIntosh, A.J.J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M.A. & Hernandez, A.D. (2012). Monkeys in the middle: parasite transmission through the social network of a wild primate. — PLoS ONE 7: e51144.
-
Maksimowich, D.S. & Mathis, A. (2000). Parasitized salamanders are inferior competitors for territories and food resources. — Ethology 106: 319-329.
-
Mikheev, V.N., Pasternak, A.F., Taskinen, J. & Valtonen, E.T. (2010). Parasite-induced aggression and impaired contest ability in a fish host. — Parasites Vect. 3: 17.
-
Moore, J. (2002). Parasites and the behavior of animals. — Oxford University Press, Oxford.
-
Newman, M., Barabási, A.L. & Watts, D.J. (2006). The structure and dynamics of networks. — Princeton University Press, Princeton, NJ.
-
Pan, T., Gladen, K., Duncan, E.C., Cotner, S., Cotner, J.B., McEwen, D.C. & Wisenden, B.D. (2016). Bold, sedentary fathead minnows have more parasites. — Zebrafish 13: 248-255.
-
Pedersen, A.B. & Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. — Trends Ecol. Evol. 22: 133-139.
-
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. — Adv. Stud. Behav. 41: 151-186.
-
Poulin, R. (2013). Parasite manipulation of host personality and behavioural syndromes. — J. Exp. Biol. 216: 18-26.
-
Poulin, R. & FitzGerald, G.J. (1989). Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.). — Behav. Ecol. Sociobiol. 24: 251-255.
-
Poulin, R. & Maure, F. (2015). Host manipulation by parasites: a look back before moving forward. — Trends Parasitol. 31: 563-570.
-
Quinn, S.C., Brooks, R.J. & Cawthorn, R.J. (1987). Effects of the protozoan parasite Sarcocystis rauschorum on open-field behaviour of its intermediate vertebrate host, Dicrostonyx richardsoni. — J. Parasitol. 73: 265-271.
-
Rau, M.E. (1984). Loss of behavioural dominance in male mice infected with Trichinella spiralis. — Parasitology 88: 371-373.
-
Réale, D., Dingemanse, N.J., Kazem, A.J.N. & Wright, J. (2010). Evolutionary and ecological approaches to the study of personality. — Phil. Trans. Roy. Soc. Lond. B 365: 3937-3946.
-
Réale, D., Reader, S.M., Sol, D., McDougall, P.T. & Dingemanse, N.J. (2007). Integrating animal temperament within ecology and evolution. — Biol. Rev. 82: 291-318.
-
Rode, N.O., Lievens, E.J.P., Flaven, E., Segard, A., Jabbour-Zahab, R., Sanchez, M.I. & Lenormand, T. (2013). Why join groups? Lessons from parasite-manipulated Artemia. — Ecol. Lett. 16: 493-501.
-
Sah, P., Leu, S.T., Cross, P.C., Hudson, P.J. & Bansal, S. (2017). Unraveling the disease consequences and mechanisms of modular structure in animal social networks. — Proc. Natl. Acad. Sci. USA 114: 4165-4170.
-
Schall, J.J. (1982). Lizards infected with malaria: physiological and behavioral consequences. — Science 217: 1057-1059.
-
Schall, J.J. (1983). Lizard malaria: cost to vertebrate host’s reproductive success. — Parasitology 87: 1-6.
-
Schall, J.J. & Dearing, M.D. (1987). Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. — Oecologia 73: 389-392.
-
Schmid-Hempel, R. & Müller, C.B. (1991). Do parasitized bumblebees forage for their colony? — Anim. Behav. 41: 910-912.
-
Scott, J. (2013). Social network analysis, 3rd edn. — Sage Publications, London.
-
Shaner, P.-J.L., Yu, A.-Y., Ke, L. & Li, S.-H. (2017). Spacing behaviors and spatial recruitment of a wild rodent in response to parasitism. — Ecosphere 8: e01780.
-
Sih, A., Hanser, S.F. & McHugh, K.A. (2009). Social network theory: new insights and issues for behavioral ecologists. — Behav. Ecol. Sociobiol. 63: 975-988.
-
Sprengel, G. & Lüchtenberg, H. (1991). Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. — Dis. Aquat. Org. 11: 31-35.
-
Springer, A., Kappeler, P.M. & Nunn, C.L. (2017). Dynamic vs. static social networks in models of parasite transmission: predicting Cryptosporidium spread in wild lemurs. — J. Anim. Ecol. 86: 419-433.
-
Stamps, J. & Groothuis, T.G.G. (2010). The development of animal personality: relevance, concepts and perspectives. — Biol. Rev. 85: 301-325.
-
Stumbo, A.D., James, C.T., Goater, C.P. & Wisenden, B.D. (2012). Shoaling as an antiparasite defence in minnows (Pimephales promelas) exposed to trematode cercariae. — J. Anim. Ecol. 81: 1319-1326.
-
Thomas, F., Adamo, S. & Moore, J. (2005). Parasitic manipulation: where are we and where should we go? — Behav. Proc. 68: 185-199.
-
Thomas, F., Oget, E., Gente, P., Desmots, D. & Renaud, F. (1999). Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae). — J. Evol. Biol. 12: 385-390.
-
Thomas, F., Renaud, F. & Cézilly, F. (1996). Assortative pairing by parasitic prevalence in Gammarus insensibilis (Amphipoda): patterns and processes. — Anim. Behav. 52: 683-690.
-
Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P. & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? — J. Evol. Biol. 15: 356-361.
-
Wang, X., Brown, C.M., Smole, S., Werner, B.G., Han, L., Farris, M. & DeMaria, A. (2010). Aggression and rabid coyotes, Massachusetts, USA. — Emerg. Infect. Dis. 16: 357-359.
-
Webster, J.P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. — Parasitology 109: 583-589.
-
Wey, T., Blumstein, D.T., Shen, W. & Jordán, F. (2008). Social network analysis of animal behaviour: a promising tool for the study of sociality. — Anim. Behav. 75: 333-344.
-
White, L.A., Forester, J.D. & Craft, M.E. (2017). Using contact networks to explore mechanisms of parasite transmission in wildlife. — Biol. Rev. 92: 389-409.
-
Yanoviak, S.P., Kaspari, M., Dudley, R. & Poinar, G. (2008). Parasite-induced fruit mimicry in a tropical canopy ant. — Am. Nat. 171: 536-544.
-
Zohar, S. & Holmes, J.C. (1998). Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study. — Behav. Ecol. 9: 206-211.
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Modification of host social networks by manipulative parasites
In: BehaviourAbstract
Social network models provide a powerful tool to estimate infection risk for individual hosts and track parasite transmission through host populations. Here, bringing together concepts from social network theory, animal personality, and parasite manipulation of host behaviour, I argue that not only are social networks shaping parasite transmission, but parasites in turn shape social networks through their effects on the behaviour of infected individuals. Firstly, I review five general categories of behaviour (mating behaviour, aggressiveness, activity levels, spatial distribution, and group formation) that are closely tied to social networks, and provide evidence that parasites can affect all of them. Secondly, I describe scenarios in which behaviour-altering parasites can modify either the role or position of individual hosts within their social network, or various structural properties (e.g., connectance, modularity) of the entire network. Experimental approaches allowing comparisons of social networks pre- versus post-infection are a promising avenue to explore the feedback loop between social networks and parasite infections.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 907 | 223 | 47 |
| Full Text Views | 306 | 26 | 0 |
| PDF Views & Downloads | 136 | 37 | 0 |