Experimental demonstration of a behavioural modification in a cyprinid fish, Rutilus rutilus (L.), induced by a parasite, Ligula intestinalis (L.)

Behavioural changes in parasitized hosts have been experimentally investigated by comparing the swimming behaviour of roach, Rutilus rutilus, infected by the tapeworm Ligula intestinalis with that of uninfected roach when they were exposed to the same overhead heron stimulus. Before the stimulus was presented, infected fish swam close to the surface and uninfected fish were preferentially found near the bottom of the tank. The stimulus clearly induced a change in the vertical distribution of infected fish only. On the other hand, infected roach were less active than uninfected fish before, during, and after the stimulus was presented. Proximate mechanisms of these behavioural changes are discussed. These behavioural differences, i.e., roach surfacing, swimming, and response to stimulus, probably favour the predation of infected roach by avian predators. Résumé : Les modifications du comportement chez des organismes parasités ont été étudiées expérimentalement par comparaison du comportement de nage chez des gardons Rutilus rutilus infectés par le cestode Ligula intestinalis et chez des gardons sains, particulièrement quand ils étaient exposés au même stimulus, un héron en surplomb. Avant l’introduction du héron, les poissons infectés nageaient près de la surface et les poissons sains semblaient préférer le fond de l’aquarium. Le stimulus a déclenché un changement dans la répartition verticale, mais seulement chez les poissons infectés. Par ailleurs, les poissons infectés étaient moins actifs que les poissons sains avant, pendant et après l’introduction du prédateur. Les mécanismes immédiats qui régissent les changements de comportement sont examinés. Ces différences de comportement, retour en surface, nage et réponse au stimulus, favorisent probablement la prédation des gardons infectés par des oiseaux prédateurs. [Traduit par la Rédaction] 744 Loot et al. Introduction Phenotypic changes in parasitized animals have been reported in a large range of host–parasite systems (Moore 1984; Barnard and Behnke 1990; Combes 1991, 1995; Adamo 1997; Poulin 1998; Poulin and Thomas 1999; Arnott et al. 2000). Although the adaptive value of these changes is sometimes difficult to assess (e.g., Poulin 1995), many have been considered adaptations for parasite transmission (e.g., Holmes and Bethel 1972; Curtis 1987; Combes 1991; Moore 1993; Maitland 1994; Poulin 1994; Vance 1996; Kuris 1997). Behavioural changes making intermediate hosts more susceptible to predation by the parasite’s next host have been documented in some trophically transmitted parasites (see Poulin 1994; Lafferty 1999), but in most cases the ecological results of behavioural changes have not been examined. For instance, parasitized intermediate hosts may experience a higher risk of predation by final hosts because of impaired motor performance (e.g., Hay and Aitken 1984), increased or decreased activity levels (e.g., Gotelli and Moore 1992; Poulin et al. 1992), or direct movement toward the microhabitats of foraging predators (e.g., Helluy 1984; Lafferty and Morris 1996; Thomas and Poulin 1998; Berdoy et al. 2000). The tapeworm Ligula intestinalis has a three-host lifecycle (Rosen 1920). The coracidium larva penetrates the gut wall of a copepod microcrustacean and develops into the procercoid form in the haemocoel. The infected copepod is ingested by a planktivorous cyprinid fish and the procercoid then develops into a plerocercoid larva located in the host’s abdominal cavity. The cycle of the parasite is completed when the fish is preyed upon by a piscivorous bird, and the plerocercoid then matures in the host’s intestine. Several studies have shown that plerocercoids have severe effects on fish viability and behaviour (Moisan 1956; Arme and Owen 1968, 1970; Sweeting 1975, 1976; Taylor and Hoole 1989; Wyatt and Kennedy 1989). Field observations suggest that Can. J. Zool. 80: 738–744 (2002) DOI: 10.1139/Z02-043 © 2002 NRC Canada 738 Received 25 May 2001. Accepted 15 February 2002. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 2 May 2002. G. Loot1 and S. Lek. Centre d’Études des Systèmes Aquatiques Continentaux, Unité Mixte de Recherche (UMR)—Centre National de la Recherche Scientifique (CNRS) 5576, Bâtiment IVR3, Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse CEDEX 4, France. S. Aulagnier. Institut de Recherche sur les Grands Mammifères, Institut National de la Recherche Agronomique, B.P. 27, 31326 Castanet-Tolosan CEDEX 4, France. F. Thomas and J.-F. Guégan. Centre d’Etudes sur le Polymorphisme des Micro-organismes, Centre Institut de Recherche pour le Développement de Montpellier, UMR CNRS–IRD 9926, 911 avenue du Val de Montferrand, F-34394 Montpellier CEDEX 5, France. 1Corresponding author (e-mail: [email protected]). J:\cjz\cjz80\cjz-04\Z02-043.vp Monday, April 29, 2002 10:12:03 AM Color profile: Disabled Composite Default screen