977 An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators V. MEDOC and J.-N. BEISEL* Université Paul Verlaine-Metz, Laboratoire des Interactions Ecotoxicologie, Biodiversité, Ecosystèmes (LIEBE), CNRS UMR 7146, Campus Bridoux, rue du général Delestraint, F-57070 Metz, France (Received 28 September 2007; revised 26 December 2007 and 7 March 2008; accepted 7 March 2008; first published online 14 May 2008) SUMMARY Among the potential effects of parasitism on host condition, the ‘ increased host abilities ’ hypothesis is a counterintuitive pattern which might be predicted in complex-life-cycle parasites. In the case of trophic transmission, a parasite increasing its intermediate host’s performance facing non-host predators improves its probability of transmission to an adequate, definitive host. In the present study, we investigated the cost of infection with the acanthocephalan Polymorphus minutus on the locomotor/escape performance of its intermediate host, the crustacean Gammarus roeseli. This parasite alters the behaviour of its intermediate host making it more vulnerable to predation by avian definitive hosts. We assessed the swimming speeds of gammarids using a stressful treatment and their escape abilities under predation pressure. Despite the encystment of P. minutus in the abdomen of its intermediate host, infected amphipods had significantly higher swimming speeds than uninfected ones (increases of up to 35%). Furthermore, when interacting with the non-host crustacean predator Dikerogammarus villosus, the highest escape speeds and greatest distances covered by invertebrates were observed for parasitized animals. The altered behaviour observed among the manipulated invertebrates supported the ‘ increased host abilities ’ hypothesis, which has until now remained untested experimentally. The tactic of increasing the ability of infected intermediate hosts to evade potential predation attempts by non-host species is discussed. Key words: escape response, Gammarus roeseli, locomotor performance, non-host predators, parasite-induced behaviour, Polymorphus minutus. INTRODUCTION Parasites with complex life-cycles have received a growing amount of interest because of the subtle interactions they develop with their intermediate hosts. Indeed, natural selection is thought to favour any parasite-induced alteration of host phenotype that results in increased trophic transmission to final hosts (the ‘ manipulation hypothesis ’, see Moore and Gotelli, 1990). This is a well-developed characteristic in acanthocephalans which use invertebrates to reach their final, vertebrate hosts via the trophic pathway (Bethel and Holmes, 1977 ; Moore, 1984 ; Kennedy, 2006). Parasite-induced behavioural alterations are varied and include reaction to light (Bauer et al. 2000 ; Cézilly et al. 2000 ; PerrotMinnot, 2004), vertical distribution (Cézilly et al. 2000 ; Bauer et al. 2005 ; Médoc et al. 2006), drift behaviour (McCahon et al. 1991 ; Maynard et al. 1998), activity level (Dezfuli et al. 2003) and antipredator behaviour (Baldauf et al. 2007 ; PerrotMinnot et al. 2007 ; Kaldonski et al. 2007). Even though the resulting trophic transmission has rarely been verified in the field, manipulation tends to make infected intermediate hosts more likely to be preyed * Corresponding author : Tel: +(0)3 87 37 84 29. Fax : +(0)3 87 37 84 23. E-mail : beisel@univ-metz.fr upon by the parasite’s definitive host (Lagrue et al. 2007 ; Perrot-Minnot et al. 2007). Basically, we considered 3 hypotheses about the potential effects of parasitism on host condition (Fig. 1). Firstly, the ‘ no effect ’ hypothesis (Fig. 1A) is very poorly documented because it has not generated wide support in the scientific community (Poulin, 2000), considering that it is difficult to imagine an infection without any negative consequences on host condition. Secondly, contrary to the previous hypothesis, the ‘ handicapped host ’ hypothesis, in which parasitism-induced effects handicap the infested animals (Fig. 1B), is frequently cited. Effects can include direct, pathological ones, for example when the parasite Pomphorhynchus laevis reduces growth rate and oxygen consumption in its Gammarus pulex host (Rumpus and Kennedy, 1974). Alternatively, the effect could be more indirect as observed by Mouritsen and Poulin (2003) when infection by the trematode Curtuteria australis decreased the ability of its intermediate host, the New Zealand Austrovenus stutchburyi cockle, to burrow. As a result, this ‘handicapped’ mollusc becomes more conspicuous to both definitive avian hosts and non-host fishes. Finally, according to the ‘ increased host abilities ’ hypothesis (Fig. 1C), both the parasite and its intermediate host benefit from parasiteinduced behavioural alterations. For parasites with Parasitology (2008), 135, 977–984. f 2008 Cambridge University Press doi:10.1017/S0031182008004447 Printed in the United Kingdom 978 V. Medoc and J.-N. Beisel A B C Fig. 1. Potential effects of parasitism on host condition as predicted by the ‘no effect ’ (A), the ‘handicapped host ’ (B) and the ‘ increased host abilities ’ (C) hypotheses. complex life-cycles, this apparently paradoxical pattern could be favoured by natural selection if the increased abilities of the manipulated intermediate hosts prevent parasites from dying in unsuitable predators. A potential mechanism underlying the ‘ increased host abilities ’ hypothesis could be tradeoffs in energy allocation within host-parasite systems. Thus, infected hosts might avoid unsuitable predatory hosts more effectively than uninfected ones if, for example, they allocate energy to locomotory instead of reproductive or foraging functions. An increased ability of infected intermediate hosts to evade predation attempts by non-host species does not prevent the parasite from manipulating its intermediate host in ways that increase encounter rates with appropriate final hosts, in particular when the non-host species is an arthropod and the final host is a waterbird. Gammarus roeseli is a freshwater amphipod of Balkan-European origin (Karaman and Pinkster, 1997 ; Pöckl et al. 2003) that was recorded for the first time in France (vicinity of Paris) in 1835 (Jazdzewski, 1980). Now considered as naturalized in France, G. roeseli is the intermediate host for the acanthocephalan Polymorphus minutus. Following a physical stimulus, infected G. roeseli exhibit vertical displacement towards the water’s surface which could enhance their chances of it being consumed by a bird, the parasite’s definitive host (Bauer et al. 2005). Within a biological invasion context, this reverse geotactism renders parasitized specimens less vulnerable than uninfected G. roeseli to the new, benthic predator Dikerogammarus villosus (Médoc et al. 2006). D. villosus is a crustacean gammarid of Ponto-Caspian origin whose aggressive, predatory behaviour is well documented (Dick and Platvoet, 2000 ; Dick et al. 2002 ; Bollache et al. 2004). This amphipod has never been observed as an intermediate or a paratenic host of P. minutus (personal observations). The Gammarus/Polymorphus host-parasite association allows us to investigate a counter-intuitive tactic that consists of increasing the ability of infected intermediate hosts to evade predation attempts by non-host species. This hypothesis has received little attention until now and has remained untested experimentally. Thanks to the development of a method to measure accurately the swimming speed of invertebrates, we studied a predator prey interaction regarding the escape speeds of preys. In this study, we investigated in detail the escape efficiency of G. roeseli in predator evasion faced with the benthic amphipod D. villosus. To test the ‘ increased host abilities ’ hypothesis, the locomotor performance of P. minutus-infected G. roeseli was assessed experimentally, under stressful conditions, by recording several parameters including time spent without displacement, average and maximum speeds. Next, to assess the infected host’s reaction under predation pressure, we measured the escape speed, the distance covered by G. roeseli and the distance between the prey and the potential predator. MATERIALS AND METHODS Biological material In spring and summer 2006, we used a pond net (500 mm mesh) to collect G. roeseli in the Nied River (Laquenexy, North-eastern France, 49x05k N and 6x19k E) and D. villosus in the Moselle River (Metz, North-eastern France, 49x07k N and 6x10k E). The yellow-orange cystacanth (the infective stage of P. minutus inside its intermediate host), visible through the host’s translucent cuticle, distinguished infected G. roeseli from uninfected ones. All experiments were performed with males. G. roeseli males were identified during the precopula mate-guarding phase to avoid any confusion while D. villosus males (from 13 to 18 mm in length) were sexed using sexual dimorphism, with males exhibiting massive gnathopods (Devin et al. 2004). To avoid effects of size or parasitic-load, we only selected G. roeseli males measuring 9¡1 mm in length and harbouring 1 cystacanth. Animals were maintained separately in the laboratory in aerated, temperature-stabilized (12¡1 xC) water from the Nied River for 5 days before the experiments began. Alder-leaf discs (˘=20 mm) were provided to satiation as the sole food resource. Video recording device The horizontal plan was filmed using a hermetic box (28 cm longr28 cm wider37 cm high) with a source of diffuse light and a webcam (Philips ToUcam Pro II Pcvc840). This device is assumed to protect the organisms from any external disturbance during experiments. Tests were performed in a 979 Escape behaviour and host manipulation Fig. 2. Pattern of escape speed of Gammarus roeseli during the first 3 sec after an aggressive encounter with the benthic predator Dikerogammarus villosus. Following the recording method, each dot represents a frame (20 frames/s). The swimming speeds (median and interquartile range) were obtained for each frame (see text for details) with uninfected (A) and Polymorphus minutus-infected (B) gammarids (Nuninfected=Ninfected=36). cylindrical glass receptacle lacking any places of refuge (˘: 140 mm, height : 74 mm), placed inside the box, and filled with 250 ml of aerated, temperature-stabilized (12¡1 xC) Nied river water. The low water level (B 35 mm) encouraged amphipod displacement horizontally. Filming began once the amphipod (G. roeseli in the first experiment and D. villosus in the second) was carefully introduced into the glass receptacle, using a spoon. Each video capture was recorded for 3 min at a rate of 20 frames/ s. After each experiment the G. roeseli were dissected to verify infection by P. minutus. The video shots were analysed using unpublished software developed in our laboratory. This software locates the moving subject in a given area and computes its XY coordinates into displacement metrics. Experiment 1 : Locomotor performance A G. roeseli (uninfected or P. minutus-infected) was introduced into the device and a first 3-min video capture (control) was began immediately. Locomotor performance was assessed by exposing the invertebrate under test to high water velocity. Thus, at the end of the first video, we generated a circular water-flow (B 14.66 cm.sx1 at the periphery of the receptacle) inside the receptacle using a magnetic stirrer (Hanna Instruments 190 M). The rotation speed was too low to injure invertebrates (B300 rot.minx1), but the resulting flow kept the amphipod moving. Three successive agitation periods (lasting 3, 6 and then 9 min) were each followed by a 3-min video capture. The magnetic agitator was removed during filming. This experiment was replicated 20 times with both uninfected and P. minutusinfected G. roeseli. The 3 and 6-min agitation periods only slightly affected the swimming performance of gammarids (results not shown), so in the Results section, we focused on the first (Control) and last (called ‘ After Treatment ’ hereafter) video shots. The entire sequences (3600 frames for 3 min) were analysed with our software. The time spent without locomotor activity and the average and maximum escape speeds in infected G. roeseli were compared to those of uninfected individuals, before and after the treatment. Experiment 2 : Escape behaviour A single G. roeseli was placed into the glass receptacle using a spoon and acclimatized for 5 min. Then a D. villosus male was added and a 3-min video capture started. Twelve replicates were performed for both uninfected and P. minutus-infected gammarids. All D. villosus were used only once and we changed the water before each new video shot. The shorttime experiments (3 min) prevented the prey from being consumed by D. villosus, but its aggressiveness caused an escape response in G. roeseli (pre-experimental inquiry). Predator encounters were numerous in each video shot and many of them were not aggressive. We therefore examined the 3 strongest escapes following an aggressive contact with D. villosus using our software and considered V. Medoc and J.-N. Beisel 980 these data as independent. The strongest escapes were considered as the most representative of the host potentialities. Initially, we studied the escape pattern of G. roeseli regarding its swimming speed following an encounter with D. villosus. For both uninfected and P. minutus-infected individuals, the escape speed peaked during the first second after a contact, and then decreased with time (see Fig. 2). Consequently, during the video shot analyses, we focused on the first second following a physical contact with the benthic predator to highlight differences in the escape performance between the two prey types. The escape response of G. roeseli within the first second following a predator encounter was divided into 4 time-intervals (0–0.25 s, 0.30–0.50 s, 0.55–0.75 s and 0.80–1 s). The average escape speed was calculated for each time-interval while the distance covered by G. roeseli and its distance from D. villosus were calculated after 0.25, 0.5, 0.75 and 1 s (representing the end of the 4 timeintervals). Statistical analysis Speeds were calculated for each frame (20 frames/s), based on the distance covered by G. roeseli between 2 consecutive frames. The maximum speed was defined as the 95-percentile speed to reduce the variability induced by extreme values. For Exp. 1, as data did not meet normality and homogeneity assumptions (following Shapiro-Wilk W-tests), we performed non-parametric statistics. The swimming activity of each individual being recorded before and after the agitation periods (paired samples), the treatment effect was assessed using Wilcoxon paired-sample tests. Then, MannWhitney U-tests were performed to evaluate differences between uninfected and P. minutus-infected gammarids (independent samples). For Exp. 2, data that met normality and homogeneity assumptions (following Shapiro-Wilk W-tests) were tested for significance with parametric statistics (Student t-tests), or otherwise, with nonparametric statistics (Mann Whitney U-tests). We performed all tests with a 5 % type I error risk, using STATISTICA Software 6.0 (StatSoft, France). Experiment 1 : Parasitism and locomotor activity Fig. 3. Locomotor performance of Gammarus roeseli infected by Polymorphus minutus. The time spent without displacement (A), maximum (B) and average (C) speeds (median and interquartile range) were obtained for uninfected (white bars) and infected (black bars) amphipods before (Control) and after an experimental treatment including 3 disturbance sequences (Nuninfected=Ninfected=20, see text for details). The asterisks indicate significant differences between uninfected and parasitized animals (Mann-Whitney U-test, Pf0.05), whereas lower-case letters indicate significant differences in the measurements before and after treatment (Wilcoxon paired-sample test, Pf0.05). No significant differences were found in the stationary times between uninfected and infected amphipods (Mann Whitney U-test, control : U=170, N1=N2=20, P=0.43 ; after treatment : U=195, N1=N2=20, and P=0.90, Fig. 3A) and the treatment had no effect on this parameter (Wilcoxon paired-sample test, uninfected : T=79, N=20, P= 0.332 ; infected : T=90, N=20, P=0.575). While the maximum speeds decreased significantly during experiments (uninfected : T=41, N=20, P=0.017 ; infected : T=39, N=20, P=0.014), values were 34.5 % higher for infected compared to uninfected gammarids in controls (Mann Whitney U-test, U=93, N1=N2=20, P=0.003, Fig. 3B) and RESULTS 981 Escape behaviour and host manipulation Table 1. Swimming speed (median and interquartile range) of uninfected and Polymorphus minutus-infected Gammarus roeseli following contact with the benthic predator, Dikerogammarus villosus (Significant statistical effects (Pf0.05, Nuninfected=Ninfected=36) are shown in bold.) Swimming speed (mm.sx1) Mann Whitney U-Test Time interval (s) Uninfected P. minutus-infected U 0–0.25 0.30–0.50 0.55–0.75 0.80–1 81.0 (70.0–93.5) 70.3 (39.6–98.5) 59.1 (30.4–89.7) 56.1 (28.1–80.5) 98.4 (87.5–121.9) 74.5 (39.4–109.9) 51.6 (27.7–85.0) 44.1 (28.2–77.1) 316 590 596 591 P <0.001 0.519 0.564 0.526 remained 35 % higher after treatment (U=108, N1=N2=20, P=0.012). The average speeds also decreased significantly with treatment (Wilcoxon paired-sample test, uninfected : T=38, N=20, P= 0.012 ; infected : T=6, N=20, P<0.001). Infected G. roeseli were slightly faster than uninfected ones in controls (Mann Whitney U-test, U=135, N1= N2=20, P=0.081, Fig. 3C) and this difference became significant (by 19.4 %) after treatment (U=119, N1=N2=20, P=0.028). Experiment 2 : The escape speeds of intermediate hosts During the first quarter of a second, the median swimming speeds of infected animals were 21.5 % higher (Mann Whitney U-test, U=316, N1= N2=36, P<0.001, Table 1), but after this short period no differences in speed were found between uninfected and infected amphipods. The highest speeds were reached at the beginning (0–0.25 s) of the escape response, with infected individuals reaching a maximal escape speed of 150 mm.sx1, a value 26 % higher (Fig. 4) than that of uninfected individuals (U=357, N1=N2=36, P<0.001). G. roeseli covered a distance at least 21.2 % longer when infected with P. minutus only at the beginning of the escape response (at t=0.25 s : U=316, N1= N2=36, P<0.001 ; at t=1 s : U=583, N1=N2=36, P=0.469, Table 2A). Hence, at the beginning of the escape movement, the distance between the potential predator and infected G. roeseli was significantly greater than with uninfected individuals (at t=0.25 s : 24.2 %, Table 2B). DISCUSSION This study assessed the effects of P. minutus infection on the locomotor/escape performance of its intermediate host, according to 3 hypotheses designated ‘ no effect ’, ‘ handicapped host ’ and ‘ increased host abilities ’. Acanthocephalan parasites encysted in the abdomen of their intermediate hosts have been found to compress the internal organs, which is usually considered as a handicap (Dezfuli and Giari, 1999). To support this idea, Pascoe et al. (1995) found, in Fig. 4. Escape speed of Gammarus roeseli interacting with a predatory species. The escape speeds (means¡S.D.) were observed for uninfected and Polymorphus minutus-infected G. roeseli in the first second following contact with Dikerogammarus villosus. Nuninfected= Ninfected=36 and the asterisk indicates a significant difference between uninfected and infected gammarids (Student t-test, Pf0.05). The dotted lines refer to the maximum swimming speeds (mean values) of uninfected (A, N=20) and P. minutus-infected amphipods (B, N=20) measured without D. villosus, during the first experiment (control, see text for details). the study of another host-parasite association, that the feeding performance of Gammarus pulex was altered by its infection with the acanthocephalan parasite Pomphorhynchus laevis. In the presence of brine shrimp eggs, infected amphipods had significantly longer median-feeding times than uninfected ones, which was attributed to the potential physical obstruction caused by developing cystacanth inside the host (Pascoe et al. 1995). For the first time, we measured the escape speed of a crustacean amphipod and the cost of infection by an acanthocephalan parasite on its swimming performance. Despite most previous findings pointing to behavioural or physiological alterations induced by parasites (reviewed by Kennedy, 2006), our results appeared counter-intuitive by supporting the ‘ increased host abilities ’ hypothesis. While the time spent without displacement remained unchanged during tests, the average and maximum swimming speeds of G. roeseli in the absence of the 982 V. Medoc and J.-N. Beisel Table 2. Cumulative distance covered by uninfected and Polymorphus minutus-infected Gammarus roeseli following a contact with Dikerogammarus villosus (A), and distance between G. roeseli and this potential predator (B) (median and interquartile range) (Significant statistical effects (Pf0.05, Nuninfected=Ninfected=36) are shown in bold.) (A) distance covered by G. roeseli (mm) Mann Whitney U-Test Time (s) Uninfected P. minutus-infected U 0.25 0.5 0.75 1 20.3 (17.5–23.4) 37.0 (29.5–44.9) 50.4 (37.3–66.6) 67.1 (49.1–91.3) 24.6 (21.9–30.5) 44.0 (34.1–56.3) 56.5 (41.3–74.0) 69.4 (50.0–97.7) 316 470 537 583 P <0.001 0.045 0.211 0.469 (B) distance between G. roeseli and D. villosus (mm) Mann Whitney U-Test Time (s) Uninfected P. minutus-infected U P 0.25 0.5 0.75 1 33.1 (29.9–40.3) 39.3 (33.4–55.3) 50.0 (34.1–66.0) 54.7 (33.4–73.4) 41.1 (33.3–46.4) 48.6 (38.9–61.9) 50.2 (38.2–78.7) 52.9 (32.3–78.7) 393 495 576 646 0.004 0.086 0.423 0.987 predator were significantly higher when infected by P. minutus (at least 20 %), both before and after the treatments. Furthermore, following an encounter with the benthic predator D. villosus, the highest escape speeds were observed in infected animals. As the difference between escape and capture in a predator-prey encounter can be decided in a splitsecond interaction (Wisenden et al. 1999), parasitized amphipods exhibiting a prompt escape might have much more time to seek shelter from attack than healthy individuals. To support this idea, we found that the distance covered by infected gammarids, at the beginning of an escape (0–0.5 s), significantly exceeded those of uninfected individuals. Consequently, the distance between D. villosus and G. roeseli was greater when the latter was infected by P. minutus. Thus, under natural conditions, this ability might increase the probability for infected prey to be out of reach of a potential predator. From the parasite’s perspective, the increased escape response of infected G. roeseli interacting with D. villosus does not directly enhance parasite transmission to the definitive host, but might prevent cystacanths from dying in an inappropriate, non-host predator. Combined with a negative geotaxis (Bauer et al. 2005 ; Médoc et al. 2006) the escape response induced by P. minutus makes the infected intermediate hosts available for surface predators. However, the transmission of P. minutus to water birds remains to be verified experimentally (but see Bethel and Holmes, 1977 with Gammarus lacustris infected by Polymorphus paradoxus). The deleterious effects of P. minutus infection on the fitness of its crustacean hosts are welldocumented, especially in Gammarus pulex. Alibert et al. (2002) suggested a positive association between acanthocephalan infection and developmental instability in G. pulex. Ward (1986) reported total castration of infected females and an accompanying decrease in their pairing probability (Bollache et al. 2002). Finally, acanthocephalans do not interfere with spermatogenesis according to CharniauxCotton and Payen (1985) (reported in G. lacustris infected by Polymorphus parodoxus and P. marilis, see Zohar and Holmes, 1998). However, the pairing success of G. pulex males infected with P. minutus is considerably reduced (Bollache et al. 2001). G. roeseli used in this study is considered to be a recent host species compared to the more intensively studied G. pulex. Although both amphipod species show a negative geotaxis when parasitized with P. minutus, the effect is greater in the native host G. pulex than in G. roeseli (see Bauer et al. 2005). Without further investigation and considering only the deleterious effects of infection on a host’s condition, such differences in the manipulation efficiency could be wrongfully interpreted as a less well-adapted strategy to newly-colonizing host species. In contrast, our results contribute additional elements to the P. minutus-induced effects underlying a potential adaptation which might favour parasite fitness with regard to non-host predator avoidance. The selective role of non-host predators on the parasite’s transmission strategy was demonstrated in a mollusc/ trematode host-parasite association (Levri, 1998). Escape behaviour and host manipulation The author found that infection with the trematode Microphallus sp. altered the daily foraging behaviour of the snail Potamopyrgus antipodarum in a timespecific manner, which minimizes its exposure to an inappropriate predator, the New Zealand fish (Gobiomorphus cotidianus). In support of the ‘ increased host abilities ’ hypothesis, a recent study performed on the same G. roeseli population investigated the salinity tolerance of this host-parasite system (Piscart et al. 2007). Infected amphipods were found to be much more resistant than uninfected individuals, and this pattern was not related to ATPase activity, the principal ion-exchange mechanism in aquatic crustaceans. Beyond the implication for animal dispersion, this pattern might increase parasite fitness by keeping the transmission effective under stressful conditions. In conclusion, short time-scale measurements of G. roeseli swimming speed indicated that the first second following an encounter with a benthic predator was crucial in determining the outcome of the interaction. Infection with P. minutus significantly increased G. roeseli swimming activity over this critical time-frame, thus reducing the chance of parasite death in an unsuitable host species. However, although this would leave the infected gammarid available for predation by a suitable water bird definitive host, the impact of this increase in swimming ability on interactions with water bird predators remains to be investigated. We wish to thank Philippe Rousselle (Université Paul Verlaine – Metz) warmly for the computer software used in the behavioural study of gammarids and Anna MathenyCartier for her linguistic corrections of an earlier version of the manuscript. We gratefully thank Dennis Webb (University of Rennes) for its suggestions on a revised manuscript. We are grateful to the two anonymous reviewers for their helpful comments and suggestions. This study was funded by the French Ministry of Ecology and Sustainable Development as part of the 2003–2005 Biological Invasions Program, and by a grant from the ‘ Conseil Régional de la Région Lorraine ’ to V.M. REFERENCES Alibert, P., Bollache, L., Corberant, D., Guesdon, V. and Cézilly, F. (2002). Parasitic infection and developmental stability : fluctuating asymmetry in Gammarus pulex infected with two acanthocephalan species. The Journal of Parasitology 88, 47–54. Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104. Baldauf, S. A., Thünken, T., Frommen, J. G., Bakker, T. C. M., Heupel, O. and Kullmann, H. (2007). Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours. International Journal for Parasitology 37, 61–65. 983 Bauer, A., Haine, E. R., Perrot-Minnot, M.-J. and Rigaud, T. (2005). The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts : the native Gammarus pulex and the invasive Gammarus roeseli. Journal of the Zoological Society of London 267, 39–43. Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. and Cézilly, F. (2000). Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native invader gammarid species. International Journal for Parasitology 30, 1453–1457. Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 65, 667–669. Bollache, L., Devin, S., Wattier, R., Chovet, M., Beisel, J.-N., Moreteau, J.-C. and Rigaud, T. (2004). Rapid extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France : potential consequences. Archiv für Hydrobiologie 160, 57–66. Bollache, L., Gambade, G. and Cézilly, F. (2001). The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea : Amphipoda). Behavioral Ecology and Sociobiology 49, 296–303. Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea : Amphipoda). Journal of Invertebrate Pathology 79, 102–110. Cézilly, F., Grégoire, A. and Bertin, A. (2000). Conflict between co-occuring manipulative parasites ? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex. Parasitology 120, 625–630. Charniaux-Cotton, H. and Payen, G. (1985). Sexual differentiation. In The Biology of the Crustacea, vol.9. Integument, Pigments, and Hormonal Processes (ed. Bliss, D. E. and Manter, L. H.), pp. 217–300. Academic Press, New York. Devin, S., Piscart, C., Beisel, J.-N. and Moreteau, J.-C. (2004). Life history traits of the invader Dikerogammarus villosus (Crustacea : Amphipoda) in the Moselle River, France. International Review of Hydrobiology 89, 21–34. Dezfuli, B. S. & Giari, L. (1999). Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host-parasite interface. Folia Parasitologica 46, 117–122. Dezfuli, B. S., Maynard, B. J. and Wellnitz, T. A. (2003). Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitologica 50, 129–134. Dick, J. T. A. and Platvoet, D. (2000). Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proceedings of the Royal Society of London 267, 977–983. Dick, J. T. A., Platvoet, D. and Kelly, D. W. (2002). Predatory impact of the freshwater invader V. Medoc and J.-N. Beisel Dikerogammarus villosus (Crustacea : Amphipoda). Canadian Journal of Fisheries and Aquatic Sciences 59, 1078–1084. Jazdzewski, K. (1980). Range extensions of some gammaridean species in European inland waters caused by human activity. Crustaceana 6, 84–107. Kaldonski, N., Perrot-Minnot, M.-J. and Cézilly, F. (2007). Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Animal Behaviour 74, 1311–1317. Karaman, G. S. and Pinkster, S. (1977). Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda) Part II. Gammarus roeseli-group and related species. Bijdragen tot de Dierkunde 47, 165–196. Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge. Lagrue, C., Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. and Bollache, L. (2007). Modification of host’s behavior by a parasite : field evidence for adaptive manipulation. Ecology 88, 2839–2847. Levri, E. P. (1998). The influence of non-host predators on parasite-induced behavioural changes in a freshwater snail. Oikos 81, 531–537. Maynard, B. J., Wellnitz, T. A., Zanini, N., Wright, W. G. and Dezfuli, B. S. (1998). Parasite-altered behavior in a crustacean intermediate host : field and laboratory studies. Journal of Parasitology 84, 1102–1106. McCahon, C. P., Maund, S. J. and Poulton, M. J. (1991). The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex). Freshwater Biology 25, 507–513. Médoc, V., Bollache, L. and Beisel, J.-N. (2006). Host manipulation of a freshwater crustacean (Gammarus roeseli) by an acanthocephalan parasite (Polymorphus minutus) in a biological invasion context. International Journal for Parasitology 36, 1351–1358. Moore, J. K. (1984). Altered behavioural responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist 123, 572–577. Moore, J. K. and Gotelli, N. J. (1990). Phylogenetic perspective on the evolution of altered host behaviours : a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. and Behnke, J. M.), pp. 193–229. Taylor & Francis, London. Mouritsen, K. M. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator : a manipulator’s nightmare. International Journal for Parasitology 33, 1043–1050. 984 Pascoe, D., Kedwards, T. J., Blockwell, S. J. and Taylor, E. J. (1995). Gammarus pulex (L.) feeding bioassay – effects of parasitism. Bulletin of Environmental Contamination and Toxicology 55, 629–632. Perrot-Minnot, M. J. (2004). Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis. International Journal for Parasitology 34, 45–54. Perrot-Minnot, M. J., Kaldonski, N. and Cézilly, F. (2007). Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalaninfected amphipod. International Journal for Parasitology 37, 645–651. Piscart, C., Webb, D. and Beisel, J. N. (2007). An acanthocephalan parasite increases the salinity tolerance of the freshwater amphipod Gammarus roeseli (Crustacea : Gammaridae). Naturwissenschaften 94, 741–747. Pöckl, M., Webb, B. W. and Sutcliffe, D. W. (2003). Life history and reproduction capacity of Gammarus fossarum and G. roeseli (Crustacea : Amphipoda) under naturally fluctuating water temperatures : a simulation study. Freshwater Biology 48, 53–66. Poulin, R. (1995). ‘‘ Adaptive ’’ changes in the behaviour of parasited animals : a critical review. International Journal for Parasitology 25, 1371–1383. Poulin, R. (2000). Manipulation of host behaviour by parasites : a weakening paradigm ? Proceedings of the Royal Society of London 267, 787–792. Rumpus, A. E. and Kennedy, C. R. (1974). The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host Gammarus pulex. Parasitology 68, 271–284. Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation : where are we and where should we go ? Behavioural Processes 68, 185–199. Ward, P. (1986). A comparative field study of the breeding behaviour of a stream and pond population of Gammarus pulex (Amphipoda). Oikos 46, 29–36. Wisenden, B. D., Cline, A. and Sparkes, S. T. C. (1999). Survival benefit to antipredator behavior in the amphipod Gammarus minus (crustacea: Amphipoda) in response to injury-released chemical cues from conspecifics and heterospecifics. Ethology 105, 407–414. Zohar, S. and Holmes, J. C. (1998). Pairing success of male Gammarus lacustris infected by two acanthocephalans : a comparative study. Behavioral Ecology 9, 206–211.