735 J. Parasitol., 93(4), 2007, pp. 735–741  American Society of Parasitologists 2007 EFFECTS OF ACANTHOCEPHALUS LUCII (ACANTHOCEPHALA) ON INTERMEDIATE HOST SURVIVAL AND GROWTH: IMPLICATIONS FOR EXPLOITATION STRATEGIES Daniel P. Beneshand E. Tellervo Valtonen Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyva ¨ skyla ¨ , Finland. e-mail: dabenesh@cc.jyu.fi ABSTRACT: Intermediate host exploitation by parasites is presumably constrained by the need to maintain host viability until transmission occurs. The relationship between parasitism and host survival, though, likely varies as the energetic requirements of parasites change during ontogeny. An experimental infection of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) was conducted to investigate host survival and growth throughout the course of parasite development. Individual isopods were infected by exposure to fish feces containing parasite eggs. Isopods exposed to A. lucii had reduced survival, but only early in the infection. Mean infection intensity was high relative to natural levels, but host mortality was not intensity dependent. Similarly, a group of naturally infected isopods harboring multiple cystacanths did not have lower survival than singly infected isopods. Isopods that were not exposed to the parasite exhibited sexual differences in survival and molting, but these patterns were reversed or absent in exposed isopods, possibly as a consequence of castration. Further, exposed isopods seemed to have accelerated molting relative to unexposed controls. Infection had no apparent effect on isopod growth. The effects of A. lucii on isopod survival and growth undermine common assumptions concerning parasite- induced host mortality and the resource constraints experienced by developing parasites. For parasites with complex life cycles, intermediate hosts serve a variety of functions, 2 of the most important being that (1) they are an energy resource for parasites, allowing growth and in some cases asexual reproduction, and (2) they are vessels for transmitting parasites to the next host in the life cycle, com- monly through predation (Parker, Chubb, Ball, and Roberts, 2003). These 2 roles of intermediate hosts presumably impose conflicting selective pressures on parasites. Parasite growth and maturation requires consumption of host resources, and heavy exploitation of intermediate hosts may benefit parasites by in- creasing growth rates, production of infective stages, and/or adult success. However, damage done is likely constrained by the need to keep the intermediate host alive long enough to mature and be successfully transmitted to the next host. There- fore, the optimal level of host exploitation (virulence by some definitions) is expected to reflect a tradeoff between the benefits of resource consumption and the costs of reduced host viability (Ebert and Herre, 1996; Poulin, 1998). There are examples of parasite-induced reductions in inter- mediate host viability within all major helminth groups, e.g., nematodes (Ashworth et al., 1996), trematodes (Sorensen and Minchella, 2001), cestodes (Rosen and Dick, 1983), and acan- thocephalans (Hynes and Nicholas, 1958). On the other hand, there are also systems in which neither parasitism nor infection intensity affects host survival (e.g., Uznanski and Nickol, 1980; Wedekind, 1997; Hurd et al., 2001). Thus, the host exploitation strategies employed by larval helminths seem to vary widely. Recognizing which factors mediate the relationship between parasitism and intermediate host survival in different systems is a necessary step toward explaining this variability. For in- stance, host sex (Shostak et al., 1985), host condition (Krist et al., 2004), and infection intensity (Fredensborg et al., 2004) may all exacerbate or buffer parasite-induced mortality. More- over, the probability of host death can vary with parasite de- velopment (Shostak et al., 1985; Schjetlein and Skorping, 1995; Sorensen and Minchella, 1998; Duclos et al., 2006). The aim of this study was to examine intermediate host ex- ploitation, as well as some potential factors influencing it, by an acanthocephalan. The host-parasite system examined was Received 6 October 2006; revised 14 January 2007; accepted 15 Jan- uary 2007. Acanthocephalus lucii and its isopod intermediate host, Asellus aquaticus. Acanthocephalus lucii exhibits a typical acantho- cephalan life cycle (Schmidt, 1985); the definitive host is a vertebrate, commonly European perch (Perca fluviatalis), and an arthropod, in this case an isopod (A. aquaticus), serves as intermediate host. Adult worms mate in the intestine of fish, and females release eggs into the environment with the feces. Isopods become infected by ingesting eggs. The parasite de- velops in the isopod to the infective cystacanth stage, and the life cycle is completed when an infected isopod is eaten by an appropriate definitive host. Brattey (1986) found that isopods exposed to A. lucii eggs experienced higher mortality than un- exposed isopods. Conversely, Hasu et al. (2006) observed that infected isopods actually survive better than controls. Given this contradictory evidence, additional investigation into the consequences of A. lucii infection on intermediate host survival seems warranted. The specific goals of this study were (1) to assess how A. lucii infection affects isopod survival throughout parasite de- velopment and (2) to evaluate whether A. lucii affects host growth, or molting behavior, or both. MATERIALS AND METHODS Animal collection and maintenance Isopods were collected at the end of August 2005 with a dip net from Niemija ¨rvi, a small pond in central Finland (62°12'N, 25°45'E) in which the only fish species present is Carassius carassius, the crucian carp. Thus, all isopods were uninfected because the definitive host of the parasite is not present in the pond. In the laboratory, isopods were fed on a diet of leaves, primarily of alder (Alnus glutinosa). Leaves were conditioned in aerated lake water for at least 2 wk to allow microbial colonization prior to being offered to isopods. Animals were maintained at approximately 18 C under constant illumination. Experimental infection To collect A. lucii eggs, perch were isolated in a large tank during August 2005. Water flow through the tank was set at a very low level to allow feces accumulation. Perch feces were collected and stored in refrigerated lake water. Owing to mortality and the subsequent addition of new individuals, the number of fish in the tank fluctuated with time, but there were usually more than 50 fish. Some of these perch were dissected (n = 93, mean length = 12.99 cm, standard deviation [SD]  2.4), and A. lucii prevalence was 75% with a mean infection intensity of 4.8 (SD  4.8). Some of the collected feces were examined with a light microscope to confirm the presence of mature eggs.