Seasonal Changes in Host Phenotype Manipulation by an Acanthocephalan: Time to Be Transmitted?
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219 Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted? D. P. BENESH1*, T. HASU2,O.SEPPA¨ LA¨ 3 and E. T. VALTONEN2 1 Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plo¨n, Germany 2 Department of Biological and Environmental Science, POB 35, FI-40014 University of Jyva¨skyla¨, Finland 3 EAWAG, Swiss Federal Institute of Aquatic Science and Technology, and ETH-Zu¨rich, Institute of Integrative Biology (IBZ), U¨ berlandstrasse 133, PO Box 611, CH-8600, Du¨bendorf, Switzerland (Received 23 July 2008; revised 25 September and 7 October 2008; accepted 7 October 2008; first published online 18 December 2008) SUMMARY Many complex life cycle parasites exhibit seasonal transmission between hosts. Expression of parasite traits related to transmission, such as the manipulation of host phenotype, may peak in seasons when transmission is optimal. The acanthocephalan Acanthocephalus lucii is primarily transmitted to its fish definitive host in spring. We assessed whether the parasitic alteration of 2 traits (hiding behaviour and coloration) in the isopod intermediate host was more pronounced at this time of year. Refuge use by infected isopods was lower, relative to uninfected isopods, in spring than in summer or fall. Infected isopods had darker abdomens than uninfected isopods, but this difference did not vary between seasons. The level of host alteration was unaffected by exposing isopods to different light and temperature regimes. In a group of infected isopods kept at 4 xC, refuge use decreased from November to May, indicating that reduced hiding in spring develops during winter. Keeping isopods at 16 xC instead of 4 xC resulted in higher mortality but not accelerated changes in host behaviour. Our results suggest that changes in host and/or parasite age, not environmental conditions, underlie the seasonal alteration of host behaviour, but further work is necessary to determine if this is an adaptive parasite strategy to be transmitted in a particular season. Key words: Acanthocephala, Asellus aquaticus, host manipulation, host-parasite interaction, host pigmentation, inter- mediate host, plastic/flexible behaviour, seasonality, trophic transmission. INTRODUCTION by Moore, 2002; Thomas et al. 2005). Both field observations (e.g. Brown et al. 2001; Perrot-Minnot For parasites with complex life cycles, transmission et al. 2007; Lagrue et al. 2007) and laboratory ex- between hosts often exhibits a seasonal rhythm. periments (e.g. Bethel and Holmes, 1977; Moore, Many studies have focused on how seasonal changes 1983; Bakker et al. 1997) indicate that some ma- in host availability and feeding behaviour affect nipulative parasites render their intermediate hosts parasite transmission rates (e.g. Chubb, 1982). For more susceptible to predation. Thus, in many cases, example, Amundsen et al. (2003) found that the host manipulation clearly seems to be an adaptive abundance of cestodes Cyathocephalus truncatus in parasite strategy to increase the likelihood of reach- arctic charr intestines increased in autumn as the ing the next host. Despite its link with transmission, parasite’s amphipod intermediate host became a host manipulation has never been considered as a more common item in the fishes’ diet. Parasite trans- factor influencing seasonal variation in parasite oc- mission rates, however, are not solely determined by currence. host ecology. Parasites have evolved a number of Organisms with complex life cycles often move strategies to increase their likelihood of transmission from the larval to the adult habitat in particular (Poulin, 2007), perhaps the most striking of which seasons, because the quality and longevity of these is host phenotype manipulation. Hosts infected two habitats changes over time (Rowe and Ludwig, with trophically-transmitted parasites often exhibit 1991; Abrams et al. 1996; Gotthard, 2001). For in- altered behaviours and/or appearance that seem to stance, the larval habitat could deteriorate and/or make them more conspicuous to predators (reviewed disappear in some seasons (e.g. summer pond dry- ing), which would restrict the time available for the habitat switch. When confronted with such seasonal * Corresponding author: Department of Evolutionary time constraints, free-living organisms with complex Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plo¨n, Germany. life cycles are often able to increase their growth rate Tel: +49 4522763258. Fax: +49 4522763310. E-mail: and/or decrease their transitional size so as to switch [email protected] habitats before conditions deteriorate (e.g. Leimar, Parasitology (2009), 136, 219–230. f 2008 Cambridge University Press doi:10.1017/S0031182008005271 Printed in the United Kingdom Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 30 May 2017 at 15:07:33, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182008005271 D. P. Benesh and others 220 1996; Johansson and Rowe, 1999; Margraf et al. mortality (Experiment 3) could induce changes in the 2003). Seasonal time constraints are also common parasitic alteration of these traits. in parasite life cycles. For example, in the arctic charr-C. truncatus system, the fishes’ seasonal pref- erence for amphipods restricts parasite transmission MATERIALS AND METHODS mainly to autumn (Amundsen et al. 2003). Like Study animals free-living organisms, parasites are expected to ad- just their transmission strategies when faced with All experimental isopods were collected from Lake seasonal constraints. Particularly, host phenotype Jyva¨sja¨rvi, Central Finland (62x14kN25x44kE). manipulation may become more beneficial, or more Isopods infected with A. lucii cystacanths were necessary, as the time available for transmission initially identified by their darkened respiratory shrinks. opercula (Brattey, 1983). Because we used naturally We studied seasonal variation in host manipulation infected isopods, infection was not a randomly as- by an acanthocephalan (Acanthocephalus lucii). signed treatment. Thus, there may be pre-existing Freshwater fish serve as the definitive host of A. lucii, differences between uninfected and infected isopods, particularly European perch (Perca fluviatilis). Adult and we acknowledge the possibility that such differ- worms mate and produce eggs in the intestine of their ences might impact the measured phenotypic traits. fish hosts, and the eggs are released into the en- To describe seasonal changes in host manipulation, vironment via the host’s faeces. There, they are though, we preferred to use naturally-infected iso- ingested by the intermediate host, isopods of the pods, because they have been exposed to the myriad species Asellus aquaticus. Parasites develop in iso- of factors that may lead to seasonality. With exper- pods over the course of several weeks to the infective imental infections, potential factors affecting ma- cystacanth stage (Andryuk, 1979). As parasites reach nipulation could be explored, but it is not possible the cystacanth stage, the respiratory opercula of their to infer a seasonal pattern of host manipulation from hosts (appendages used to circulate water for res- such designs. Moreover, experimental infections piration) become conspicuously darker (Brattey, often produce high infection intensities (i.e. higher 1983) and the entire host abdomen (pleon) takes on a than the typical natural infection level of 1 parasite darker appearance (Benesh et al. 2008). Infected per host; Brattey, 1986; Hasu et al. 2007; Benesh and isopods also spend less time hiding than uninfected Valtonen, 2007a), which may lead to unnatural isopods (Benesh et al. 2008), but their response to changes in host phenotype. Also, in some relevant light or a disturbance is unaltered (Lyndon, 1996). seasons, such as early spring, experimental infections Finally, infected isopods are more susceptible to are impossible, because there are very few gravid predation by perch, suggesting that some aspect of female worms in fish at this time (Benesh, unpub- the infection increases the probability of parasite lished observation). transmission (Brattey, 1983; Seppa¨la¨ et al. 2008). Across Europe, the life cycle of A. lucii has a fairly Experiment 1 – host manipulation in different seasons clear seasonal structure. In general, parasites mature and reproduce in fish in the spring and summer, In this experiment, isopods were collected at differ- isopods become infected in the summer and fall, and ent times of the year, but observed under the same transmission to fish occurs in the spring (Brattey, laboratory conditions. Isopods were collected during 1988; see also Chubb, 1982 and references therein). 3 different seasons in 2006: (1) spring, shortly after This is the commonest seasonal cycle reported for the ice thaw, 11–17 May, (2) late summer, 11–21 acanthocephalans (Nickol, 1985). Parasite abun- August, and (3) towards the end of fall, 9–12 dance in isopods is low throughout the year, par- October. Immediately after collection, isopods were ticularly in summer when isopod populations brought to the laboratory and individually isolated in experience considerable turnover (Brattey, 1986). plastic containers (10r15r5 cm) with 300–400 ml The spring peak in transmission to fish appears to be of lake water. Each container was supplied with at least partially caused by an increasing proportion conditioned