Spines and Behaviour As Defences Against Fish Predators in an Invasive

ANIMAL BEHAVIOUR, 2006, 72, 627e633 doi:10.1016/j.anbehav.2005.11.020

Spines and behaviour as defences against ﬁsh predators in an invasive freshwater amphipod

LOI¨C BOLLACHE, NICOLAS KALDONSKI, JEAN-PHILIPPE TROUSSARD, CLE´ MENT LAGRUE & THIERRY RIGAUD Equipe Ecologie Evolutive, UMR CNRS 5561 Bioge´osciences, Universite´ de Bourgogne

(Received 18 August 2005; initial acceptance 25 October 2005; ﬁnal acceptance 12 November 2005; published online 12 July 2006; MS. number: 8663)

Selective predation may be an important proximate cause of the success or failure of invader species. Gam- marus roeseli is an invasive amphipod, for which the causes of establishment in rivers where the native species, Gammarus pulex, predominates remain unstudied. Freshwater amphipods are important prey for numerous fish predators, but empirical evidence of lower predation rates on exotic prey is scarce. In laboratory experiments, we compared the susceptibility of G. pulex and G. roeseli to fish predation, determined the mechanisms influencing prey selection, and studied the interaction between behavioural and morphological defences. Fish predators (brown trout, Salmo trutta fario) preyed selectively on G. pulex, but not be- cause of differences in attack or capture probability. The presence of spines in G. roeseli appeared to contribute to its underpredation. Differential prey selection in this case might therefore have resulted from the trout’s reaction to an adverse stimulus. We found no significant difference in antipredator behaviour between G. pulex and G. roeseli. General behavioural differences were nevertheless found between species, with G. roeseli spending more time under shelters than G. pulex. However, microcosm experiments suggested that this difference was not important for differential predation. Antipredator behaviour may nevertheless be important for G. roeseli against other predators less sensitive to spines. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Predation risk is recognized as a major selective force in competition (Chaneton & Bonsall 2000), or when preda- the evolution of numerous traits developed by many tors reduce the abundance of their prey, allowing potential organisms to reduce their susceptibility to predation competitors to coexist (Shurin 2001; Ç elik et al. 2002). (Sih 1987; Abrams 2001). These traits include antipredator Understanding the mechanisms that influence prey sus- behaviours such as reduced activity and increased use of ceptibility within new predatoreprey interactions emerg- shelters to decrease detection, or chemical and morpholog- ing after a recent colonization may be important for ical defences to diminish the probability of a successful understanding the success of the invasion. capture (Kerfoot & Sih 1987; Laurila et al. 1997; Tollrian In Burgundy, eastern France, the invasive freshwater & Harvell 1999). Susceptibility to predation of exotic prey amphipod Gammarus roeseli is commonly found living in species introduced to novel areas is regarded as a potentially sympatry with the native species Gammarus pulex. Native important proximate factor in their ability to become es- to the Balkan area (Karaman & Pinkster 1977), G. roeseli tablished (Lodge 1993), as natural predators contribute to has colonized several Western European countries over biotic resistance by killing and eating exotic species (Robin- the past century, largely helped by human activities (Jazd- son & Wellborn 1988; Reusch 1998). If natural enemies zewski 1980; Jazdzewski & Roux 1988). Freshwater amphi- such as predators and parasites are rare or have little impact pods have a central position in the food web as prey of against new species, invaders may have an important ad- numerous invertebrates, fish and waterfowl (MacNeil vantage, which could be essential to their success (Sakai et al. 1999a), and are known to have a large number of be- et al. 2001; Shea & Chesson 2002). Natural enemies may havioural and morphological defences. For example, im- also drive community invasibility by altering competitive mobility, decreased activity and use of shelters between interactions between native and exotic prey species. This stones of bottom sediments, as well as morphological could be either through enemy-mediated apparent structures such as spines or carbonate deposits, have been reported in several species to offer protection against Correspondence: L. Bollache, Equipe Ecologie Evolutive, UMR CNRS predation (Andersson et al. 1986; Holomuzki & Hoyle 5561 Biogeósciences, Universite´ de Bourgogne, 6 Blvd Gabriel, 21000 1990; Friberg et al. 1994; Wellborn 1995; Starry et al. Dijon, France (email: [email protected]). 1998; Ruff & Maier 2000). Gammarus roeseli individuals 627 0003e3472/06/$30.00/0 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 628 ANIMAL BEHAVIOUR, 72,3

differ morphologically from G. pulex in having a mid-dor- of the same size would acquire the same amount of food, sal carina on each of the metasomes, similar to three ro- we compared the relation between size and dry weight in bust spines (Karaman & Pinkster 1977; Fig. 1). Spines are the two gammarid species. The relation was highly signif- known to be morphological antipredatory adaptations in icant in both G. pulex (N ¼ 30; Y ¼9.44 þ 1.42X, many organisms such as fish (Hoogland et al. 1956), gas- r2 ¼ 0.69, P < 0.0001) and G. roeseli (N ¼ 30; Y ¼10.13 þ tropods (West & Cohen 1996) and crustaceans (Morgan 1.45X, r2 ¼ 0.74, P < 0.0001). An analysis of covariance 1989; Tollrian 1995). Variation among Gammarus species revealed no significant difference between the slopes in the presence of dorsal spines might cause differential (F1, 56 ¼ 0.009, P ¼ 0.92), and dry weight was the same vulnerability to predation, but this remains to be demon- in G. pulex and G. roeseli for the same size (comparison strated. A priori morphological defences such as spines of intercepts: F1, 56 ¼ 1.26, P ¼ 0.27). may explain the establishment and persistence of G. roeseli in communities already saturated by G. pulex (Jazdzewski & Roux 1988). However, while antipredator defences Microcosm Experiment have been documented in several gammarids, little is We used brown trout, Salmo trutta fario, purchased from known about the relation between these different traits Corgoloin fish farm, Burgundy, eastern France, for the lab- within a single species and the variability of such traits be- oratory experiment. These fish had never experienced tween species. Our objectives in this study were (1) to test Gammarus as food before. They were less than 1 year whether the native G. pulex and the exotic species G. roeseli old, with a mean fork length of 135 mm (range are differentially susceptible to fish predation, (2) to exam- 120e152 mm). Before the experiment, trout were accli- ine the role of G. roeseli dorsal spines against fish predation, mated to laboratory conditions for at least 3 weeks in (3) to compare the antipredator behaviour of G. pulex and 500-litre aerated tanks filled with tap water, with a maxi- G. roeseli and (4) to analyse the outcome of interactions mum density of 25 fish per tank, and fed during this between morphological and behavioural traits against period with frozen chironomid larvae. fish predation in the two species. We carried out the microcosm experiment (N ¼ 10 replicates) in aquaria (40 21 cm and 25 cm deep) containing 50% trout tank water and 50% tap water, with METHODS washed river sand substrate on the bottom. A trout was placed into an aquarium 24 h before the experiment General Methods (MacNeil et al. 1999b). At the start of the experiment, 20 individuals of each of the two prey species, G. pulex and We collected sympatric G. pulex and G. roeseli between G. roeseli, were simultaneously offered to the trout. A February 2002 and March 2003 from the River Ouche, at plastic sheet separated the tank into a large compartment Parc de la Colombie`re, Dijon, eastern France, using the (30 cm) containing the substrate and the 40 gammarids kick-sampling method (Hynes 1954). Individuals were im- and a smaller compartment (10 cm) containing the trout. mediately transferred to the laboratory, in well-aerated After a prey acclimatization period (30 min), we carefully holding tanks (50 40 cm and 15 cm deep) filled with removed the partition to minimize the disturbance to dechlorinated tap water, with leaf material provided for both trout and prey. One hour later, the trout and all food. Each species was maintained separately. The room the surviving gammarids were removed and counted. To temperature was kept constant at 15 C and the light:dark analyse differential predation between the two prey types, cycle was 12:12 h. Aquaria were lit with a solar spectrum we used a two-tailed Wilcoxon signed-ranks test (Siegel & fluorescent light with a 9000 K colour temperature. Castellan 1988). To avoid a confounding effect of prey size in predation experiments, we used only G. pulex and G. roeseli males of similar size (mean total length SE of G. pulex individuals: Responses to Predator Chemical Cues 14.58 0.17 mm; G. roeseli: 14.63 0.22 mm, as measured according to Bollache et al. 2000; t318 ¼ 0.96, We tested the behavioural responses of G. pulex and P ¼ 0.34). To see whether a fish eating G. pulex or G. roeseli G. roeseli to predator (brown trout) chemical stimuli in

(a) (b)

Figure 1. (a) Gammarus roeseli and (b) Gammarus pulex. Arrows highlight the ‘spines’ on the back of G. roeseli. BOLLACHE ET AL.: AMPHIPOD ANTIPREDATOR DEFENCES 629 the laboratory in two experiments. We obtained the pred- G. roeseli. Trout feeding behaviour was videorecorded from ator stimuli by maintaining one trout for 24 h in a tank behind the curtain, with a Panasonic RX 600 VHS-C cam- filled with dechlorinated tap water (scented water: 0.01 g era recorder, and analysed frame by frame if necessary of fish/ml of water, following Mathis & Hoback 1997). with a Toshiba V-362F VHS videotape recorder and Dechlorinated tap water was used as a control. In the first a Sony Trinitron KV A2520B colour TV set. One prey was experiment, the locomotor (i.e. swimming) activity of am- introduced to the tank every 2 min during 10 min. The re- phipods was investigated in Pyrex crystallizing dishes cording began when the first gammarid was introduced (11 cm diameter, 9 cm deep) filled with 100 ml of tap wa- into the tank. In accordance with Gill & Hart (1994) and ter, with a cylinder (5 cm diameter) placed in the middle MacNeil et al. (1999b), we analysed five behaviours: (1) to prevent gammarids crossing the dish. Under this appa- encounter (E): fish turns body and displays characteristic ratus we drew eight equidistant diameter lines. We esti- orientation movement towards the prey (sudden twitch mated swimming activity by the number of lines crossed of the head towards a particular prey item, see Metcalfe per unit of time. One gammarid was used per trial. Prelim- et al. 1987); (2) attack (A): fish suddenly lunges at prey inary control experiments revealed no significant effect of and opens mouth to strike (Scott 1987); (3) capture (C): gammarid size on locomotor activity (Pearson correlation: fish grasps prey in jaws; (4) mastication (M): prey is G. pulex: r23 ¼ 0.23, P ¼ 0.15; G. roeseli: r23 ¼ 0.44, chewed inside the jaws before being swallowed and fish P ¼ 0.92), nor any effect of individual fatigue during shows buccal movements that could be counted; and (5) a time compatible with the experimental procedure (three ingestion (I): mastication ceases and prey does not reap- measures of 5 min each, made over 30 min, repeated mea- pear from mouth. If no encounter was detected 5 min af- sures ANOVA: G. pulex: F2, 25 ¼ 0.02, P ¼ 0.98; G. roeseli: ter the introduction of the last prey, we excluded the fish F2, 25 ¼ 0.35, P ¼ 0.70). During experimental series, indi- from the analysis. viduals were allowed to acclimate in the dish for 5 min, We calculated attack probability (proportion of encoun- and we recorded activity for 5 min. Then, 6 ml of control ters resulting in attack ¼ A/E), capture success (proportion or scented water was added and homogenized with of attacks resulting in capture ¼ C/A), attack efficiency a spoon. We recorded activity after treatment for 5 min. (proportion of attacks resulting in ingestion ¼ I/A) and This allowed us to compare activity before and after the capture efficiency (proportion of captures resulting in in- treatment within a species and between the two species. gestion ¼ I/C). We also measured handling time (the We made 51 and 48 replicates with G. pulex and G. roeseli, time from the first physical contact with the prey until respectively, with both control and scented water. the fish rejected the prey or the prey had been swallowed, In a second experiment, we investigated refuge usage in Gill & Hart 1994), time spent by prey in the fish’s mouth similar dishes, where the central cylinder was replaced by before ingestion and the number of chews by the trout for a black plastic cube (Duplo, Lego, Berkshire, U.K.; each gammarid ingested. Data were analysed with two- 3 3 2.5 cm) providing a refuge for the amphipods. tailed ManneWhitney U tests (Siegel & Castellan 1988). The dish was filled with 100 ml of control or scented water. Again, one individual was tested per trial. After its introduction, we recorded the time spent under the refuge during Dorsal Spines and Predation Probability 5 min. Data that did not meet normality (after a Shapiroe Despite numerous attempts, we were unable to add Wilk test) were analysed by Wilcoxon signed-ranks tests for artificial spines to G. pulex. We therefore tested the effect intraspecific comparisons and ManneWhitney U tests for of spines on the probability of being predated by remov- interspecific comparisons (Siegel & Castellan 1988). ing spines from G. roeseli individuals (spineless individ- Statistical tests were two tailed. Otherwise, parametric tests uals). Spines were cut with fine scissors. We obtained were used. We made 53 and 54 replicates for each species, a control group by manipulating individuals for 1 min, with control and scented water, respectively. the same time as for spineless G. roeseli, and cutting the cuticle at the base of each spine with a scalpel three times. During both spine removal and cutting, no haemolymph Trout Feeding Behaviour escaped from individuals. The effect of treatment on predation rate was tested with the same protocol as the one Feeding behaviour was observed in aerated tanks described above for G. pulex versus G. roeseli. We provided (40 21 cm and 25 cm deep) filled 24 h before each ex- 20 individuals of control G. roeseli (i.e. not manipulated) perimental replicate with 50% trout tank water and 50% to a single trout predator along with 20 individuals of tap water. To acclimatize the fish in the observation tanks spineless G. roeseli (Gr ) or 20 individuals of wounded and to standardize their feeding motivation, we placed all sp G. roeseli (Gr ). We counted surviving gammarids after trout in the tank and deprived them of food for 48 h be- w 1 h. Ten replicates were made for each treatment. fore the experiment (following MacNeil et al. 1999b). To avoid disturbance, we hid experimental tanks behind a curtain so that fish and observer were never in visual Refuge Usage and Predation Probability contact during the experiment. All tanks were also covered on three sides with black plastic, leaving one side The effect of refuge usage on predation was tested with clear for recording. The top of the tank was covered with the same microcosm protocol as the one used for testing a net, with a hole to introduce the prey. The experiment differential predation, but we placed a piece of air brick was carried out with a single prey type, G. pulex or (21.5 5 5 cm) into the sand, where gammarids could 630 ANIMAL BEHAVIOUR, 72,3

ﬁnd refuge. We used 20 G. roeseli and 20 G. pulex per trial, 150 and we counted the surviving gammarids after 1 h. Ten (a) replicates were made.

RESULTS 125 Microcosm Experiment

Trout ate G. pulex signiﬁcantly more than G. roeseli (Wilcoxon signed-ranks test: Z ¼ 2.54, N ¼ 20, P ¼ 0.01; 100 Fig. 2). Locomotor activity index

Responses to Predator Chemical Cues 51 51 48 48 75 Before After Before After Treatment with control water had no significant effect on locomotor activity (Wilcoxon signed-ranks test: G. G. pulex G. roeseli pulex: T ¼120.5, N ¼ 51, P ¼ 0.30; G. roeseli: T ¼ 136, N ¼ 48, P ¼ 0.11), whereas locomotor activity decreased af- 250 (b) ter the introduction of scented water (G. pulex: T ¼ 256.5, N ¼ 51, P ¼ 0.01; G. roeseli: T ¼ 185, N ¼ 48, P ¼ 0.05; Fig. 3a). The decrease in activity (the activity before minus 200 the activity after the introduction of the predatory signal) did not differ significantly between species (ManneWhit- 150 ney U test: U ¼ 1354, N1 ¼ 51, N2 ¼ 48, P ¼ 0.36). No significant difference in the time spent in the refuge was detected between control and scented water (Manne 100 Whitney U test: G. pulex: U ¼ 1347, N1 ¼ 53, N2 ¼ 54, P ¼ 0.61; G. roeseli: U ¼ 1398, N1 ¼ 53, N2 ¼ 54, P ¼ 0.85), showing no effect of predator signal on this behaviour in 50 the two species. However, the interspecific comparison showed that G. roeseli spent more time in the refuge than Time spent under refuge (s) 107 G. pulex did (U ¼ 4605, N ¼ N ¼ 107, P ¼ 0.01; Fig. 3b). 107 1 2 0 G. pulex G. roeseli Trout Feeding Behaviour Figure 3. (a) Locomotor activity (the number of lines crossed by an individual during 5 min, see text) before and after the introduction There was no significant difference between prey species of fish chemical stimuli, and (b) time spent under a refuge during in attack probability and capture success (Table 1). a 5-min period in G. pulex and G. roeseli. Means are given þ SEM. Numbers in the bars are sample sizes.

20 However, there was a significant effect of prey species on 18 attack efficiency and capture efficiency. Significantly 16 more G. pulex were successfully ingested when attacked compared to G. roeseli, and there was a significantly higher 14 proportion of captures resulting in ingestion for G. pulex 12 than for G. roeseli. Gammarus roeseli were more often re- 10 jected by the trout after their capture than G. pulex (Table 1). Among the prey that were ingested, we found no sig- 8 nificant interspecific difference in mean time between 6 the first contact and ingestion, nor in mean time spent 4 in the mouth of the predator (Table 1). However, a signifi-

Number of gammarids eaten cant species effect was found in the number of mastica- 2 tions before ingestion, G. roeseli being chewed for longer 0 than G. pulex (Table 1). G. pulex G. roeseli G. pulex G. roeseli Without refuge With refuge Figure 2. Number of Gammarus eaten in the microcosm experiment Dorsal Spines and Predation Probability without a refuge and with a refuge provided for the gammarids. N ¼ 10 replicates (10 different trout) with 20 prey of each species Control G. roeseli (i.e. individuals with spines and not provided per trout (see text). Means are given SEM. Lines connect manipulated) were eaten signiﬁcantly less than spineless values for each replicate. G. roeseli (Wilcoxon signed-ranks test: Z ¼3.01, N ¼ 10, BOLLACHE ET AL.: AMPHIPOD ANTIPREDATOR DEFENCES 631

Table 1. Brown trout feeding behaviour according to prey species, when ﬁve prey were serially presented during 10 min (see text) G. pulex G. roeseli P*

Attack probability 0.810.02 (80) 0.770.02 (80) NS Capture success 0.750.03 (74) 0.740.02 (77) NS Attack efficiency 0.540.04 (74) 0.420.04 (77) 0.05 Capture efficiency 0.540.04 (70) 0.390.04 (76) 0.01 Time between first contact and ingestion (s) 18.482.55 (65) 21.732.70 (52) NS Time spent in mouth (s) 14.351.76 (65) 18.002.27 (52) NS Number of mastications 11.831.24 (65) 16.831.67 (52) 0.02

Means are shown SEM. Sample sizes are given in parentheses. *ManneWhitney U test.

P ¼ 0.002; Fig. 4). However, we found no difference in pre- similar proportions in the microcosm experiment, G. pulex dation between the control and wounded G. roeseli (Z ¼ 0, were eaten more often. The behaviour of the trout indi- N ¼ 10, P ¼ 1.00; Fig. 4), showing that the stress of manip- cates that this selective predation was not due to differ- ulation and cutting was not the cause of the overpredation ences in attack or capture probability. The higher on spineless prey. number of G. pulex ingested seems directly related to a higher efficiency in capture, G. roeseli being more often rejected by the predator after their capture than G. pulex. Refuge Usage and Predation Probability Prey handling time by fish predators varies with the morphological type of the prey, other things being equal As in experiments without refuges, G. pulex were eaten (Hoyle & Keast 1987), such that a predator should con- significantly more than G. roeseli (Wilcoxon signed-ranks sume prey of a morphological type that maximizes energy test: Z ¼2.48, N ¼ 10, P ¼ 0.01; Fig. 2). Despite the lower gain per foraging time (Pyke 1979). The two types of prey number of individuals eaten in the two species in experi- offered in our predation experiments differed mainly in ments with refuges (Fig. 2), there was no significant differ- the presence or absence of spines, and provided similar ence in predation according to refuge presence energetic rewards. Therefore, the observed differential pre- e (Mann Whitney U test: U ¼ 65.5, N1 ¼ 10, N2 ¼ 10, dation could be based on a proximal reaction of the trout P ¼ 0.24; Fig. 2). to an adverse stimulus. Experimental tests on the effects of the dorsal spines of G. roeseli on predation probability in- dicated that spineless individuals were more often in- DISCUSSION gested than individuals with spines. Spines are known to The results of the laboratory microcosm experiment in- protect against predators by reducing capture success dicated selective predation by trout on the two Gammarus (e.g. Tollrian 1995), and, in our study, the presence of species. Although the two prey species were represented in spines explains why G. roeseli was more frequently rejected by the trout than G. pulex. In addition, G. roeseli was chewed for longer before ingestion than G. pulex. Sneddon et al. (2003) found receptors in the head of rain- bow trout, Oncorhynchus mykiss, capable of detecting nox- 5 ious stimuli to which fish respond with profound behavioural and physiological changes. Thus, the differences in attack and capture efficiency between G. roeseli and G. pulex that we observed could have resulted from the fish reacting to spine-induced adverse stimuli. Prey behavioural traits could also be implicated in the observed differential predation. A decrease in locomotor activity in the presence of a fish signal is an antipredator behaviour commonly reported in gammarid species (Wil- Differential predation 0 liams & Moore 1985; Andersson et al. 1986). In our experiments, the two Gammarus species were both less active in the presence of a fish predator signal. However, G. roeseli always spent more time under a refuge than G. pulex. Grsp – Gr Grw – Gr The trait compensation hypothesis predicts that a spe- Prey types cies with an efficient morphological defence will show Figure 4. Differential predation (number of prey 1 eaten number weak antipredator behaviour, whereas the cospecialization of prey 2 eaten) of gammarids (Gr: nonmanipulated Gammarus roe- hypothesis predicts that a species with strong morpho- seli;Grsp: spineless G. roeseli;Grw: wounded G. roeseli). N ¼ 10 rep- logical defence will show marked antipredator behaviour licates (10 different trout), with 20 prey of each type provided per (DeWitt et al. 1999; Mikolajewski & Johansson 2004). trout (see text). Means are given SEM. Gammarus pulex and G. roeseli showed a similar decrease 632 ANIMAL BEHAVIOUR, 72,3

in their activity in reaction to the fish signal. This suggests Bollache, L., Gambade, G. & Ce´zilly, F. 2000. The influence of no link (positive or negative) between the behavioural and micro-habitat segregation on size-assortative pairing in Gammarus morphological antipredator defences in G. roeseli. On the pulex (L.) (Crustacea, Amphipoda). Archiv fu¨r Hydrobiologie, 147, e other hand, G. roeseli spent more time under refuges 547 558. than G. pulex both in the presence and in the absence of Byers, J. E. 2002. Physical habitat attribute mediates biotic resistance e the fish signal, which could be interpreted as a strong in- to non-indigenous species invasion. Oecologia, 130, 146 156. trinsic antipredator behaviour. This finding supports the Ç elik, K., Schindler, J. E., Foris, W. J. & Knight, J. C. 2002. Predator- mediated coexistence of exotic and native crustaceans in a fresh- cospecialization hypothesis. However, the presence of ref- water lake. Biological Invasions, 4, 451e454. uges in the microcosm experiment did not increase the Chaneton, E. J. & Bonsall, M. B. 2000. Enemy-mediated apparent differential predation rate between G. roeseli and G. pulex competition: empirical patterns and the evidence. Oikos, 88, compared to trials without refuges. This result suggests 380e394. that longer shelter usage in G. roeseli does not increase Crawley, M. J. 1987. What makes a community invasible? In: Colo- the efficiency of spines against fish predation. Possibly, nization, Succession and Stability (Ed. by A. J. Gray, M. J. we had too few replicates, or the experiment was too Crawley & P. J. Edwards), pp. 429e453. Oxford: Blackwell. short, for us to find evidence of a benefit of spending DeWitt, T. J., Sih, A. & Hucko, J. A. 1999. Trait compensation and more time under a refuge. However, since gammarids are cospecialization in a freshwater snail: size, shape and antipredator prey for a wide range of vertebrate and invertebrate pred- behaviour. Animal Behaviour, 58, 397e407. ators (from fish and salamanders to dragonflies and cray- Friberg, N., Andersen, T. H., Hansen, H. O., Iversen, T. M., Jacob- fish, MacNeil et al. 1999a), behavioural defences could sen, D., Krøjgaard, L. & Larsen, S. E. 1994. The effect of brown be efficient against predators other than fish, which are in- trout (Salmo trutta L.) on stream invertebrate drift, with special ref- e sensitive to spines (Wudkevich et al. 1997). erence to Gammarus pulex L. Hydrobiologia, 294, 105 110. Our results may be important for understanding the Gill, A. B. & Hart, P. J. B. 1994. Feeding behaviour and prey choice of the threespine stickleback: the interacting effects of prey size, success of the invasive species G. roeseli. While many stud- fish size and stomach fullness. Animal Behaviour, 47, 921e932. ies have emphasized the importance of an ability to escape Hazlett, B. A., Burba, A., Gherardi, F. & Acquistapace, P. 2003. natural enemies in the successful establishment of exotic Invasive species of crayfish use a broader range of predation-risk species (Crawley 1987; Shea & Chesson 2002), empirical cues than native species. Biological Invasions, 5, 223e228. evidence of lower predation rates on exotic prey as a com- Holomuzki, J. R. & Hoyle, J. D. 1990. Effect of predatory fish on hab- ponent of invasion success is less clear (Byers 2002; Hazlett itat use and diel movement of the stream amphipod, Gammarus et al. 2003). Some studies have provided examples where minus. Freshwater Biology, 24, 509e517. community structures change when species differ in their Hoogland, R., Morris, D. & Tinbergen, N. 1956. The spines of sensitivity to a common enemy (e.g. Wanink & Witte sticklebacks (Gasterosteus and Pygosteus) as a means of defence 2000; Lingle 2002). In our case, direct evidence for the ef- against predators (Perca and Esox). Behaviour, 10, 205e236. fect of differential predation on G. roeseli’s invasive success Hoyle, J. A. & Keast, A. 1987. The effect of prey morphology and would require long-term experiments in seminatural habi- size on handling time in a piscivore, the largemouth bass tats, or direct comparisons between rivers with different (Micropterus salmoides). Canadian Journal of Zoology, 65, e predator abundance, but we can tentatively propose that 1972 1977. lower predation favours the installation of this species in Hynes, H. B. N. 1954. The ecology of Gammarus duebeni Lilljeborg and its occurrence in fresh water in western Britain. Journal of communities saturated with competitors such as G. pulex. Animal Ecology, 23,38e84. Jazdzewski, K. 1980. Range extensions of some gammaridean spe- Acknowledgments cies in European inland waters caused by human activity. Crusta- ceana, Supplement, 6,84e107. This study was funded by the programme ‘Invasions Jazdzewski, K. & Roux, A. L. 1988. Biogeógraphie de Gammarus Biologiques’ of the French Ministe`re de l’Ecologie et du roeseli Gervais en Europe, en particulier re´partition en France et De´veloppement Durable (grant no. 01121), and by a grant en Pologne. Crustaceana, Supplement, 13, 272e277. from the Conseil Re´gional de Bourgogne. We thank Karaman, G. S. & Pinkster, S. 1977. Freshwater Gammarus species Eleanor Haine and Frank Ce´zilly for critical reading and from Europe, North Africa and adjacent regions of Asia (Crustacea- comments, Bernard Rousseau, Philippe Baran, Pascal Amphipoda) Part II. Gammarus roeseli-group and related species. e Compagnat (Conseil Supe´rieur de la Peˆche) for help with Bijdragen tot de Dierkunde, 47, 165 196. electric fishing, and Laurent Dutal for help during field Kerfoot, W. C. & Sih, A. 1987. Predation: Direct and Indirect Impacts on Aquatic Communities. Hanover, New Hampshire: University work. 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