Freshwater Biology (2003) 48, 2085–2093

An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea) CALUM MACNEIL*, NINA J. FIELDING*, JAIMIE T. A. DICK*, MARK BRIFFA*, JOHN PRENTER* MELANIE J. HATCHER† AND ALISON M. DUNN‡ *School of Biology and Biochemistry, Queen’s University Belfast, Medical Biology Centre, Belfast, North Ireland, U.K. †School of Biological Sciences, University of Bristol, Bristol, England, U.K. ‡Centre for Biodiversity and Conservation, School of Biology, University of Leeds, England, U.K.

SUMMARY 1. The balance of predation between closely related invasive and native species can be an important determinant of the success or failure of biological invasions. In Irish freshwaters, the introduced amphipod Gammarus pulex has replaced the native G. duebeni celticus, possibly through differential mutual intraguild predation (IGP). Theoretically, parasitism could mediate such predation and hence the invasion outcome. However, this idea remains poorly studied. 2. In a field survey, we show that the acanthocephalan parasite Echinorynchus truttae is present in more G. pulex populations than G. d. celticus populations. In addition, within parasitised populations, E. truttae is more prevalent in the invader than in the native. 3. We show for the first time that an acanthocephalan parasite mediates predation between its intermediate macroinvertebrate hosts. In a field experiment, E. truttae parasitism of the invader lowered IGP upon the unparasitised native. In laboratory experiments, parasitism of G. pulex significantly reduced their predatory impact on recently moulted female G. d. celticus. Parasitism also appeared to cause reduction in predatory behaviour, such as attacks per contact on precopula guarded female natives. 4. We conclude that higher parasite prevalence in invaders as compared with natives, by mediation of interspecific interactions, could promote species coexistence, or at least slow species replacements, in this particular biological invasion. Keywords: acanthocephalan, biological invasion, Echinorynchus truttae, Gammarus, intraguild predation

Introduction During biological invasions, species replacements may result from predation among invaders and natives (Zaret & Paine, 1973; Dick, Montgomery & Elwood, 1993, 1999; Schoener & Spiller, 1996; Fritts & Rodda, 1998; Dick & Platvoet, 2000; Dick, Platvoet & Kelly, 2002). Such predatory interactions may, Correspondence: Calum MacNeil, School of Biology and Biochemistry, Queen’s University Belfast, Medical Biology Centre, 97 Lisburn Rd, Belfast BT9 7BL, N. Ireland, U.K. E-mail: [email protected]
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however, be mediated by factors which differentially affect invaders and natives. For example, each species may have different tolerances to pollutants, which will have a differential effect on their predatory abilities (MacNeil et al., 2001, 2003a). Parasitic infection is a biotic factor that could mediate species interactions (Settle & Wilson, 1990; Dunn & Dick, 1998; Rushton et al., 2000). Closely related host species are commonly susceptible to infection by the same parasite (Park, 1948; Thomas et al., 1995; Yan, Stevens & Goodnight, 1998), but often at different prevalence (Freeland, 1983; Schall, 1992; Dunn & Dick, 1998) and virulence (Park, 1948; Thomas et al., 1995), so that 2085

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putative competitors are differentially affected (Price, 1980; Schall, 1992; Hanley, Vollmer & Case, 1995; Thomas et al., 1995; Yan et al., 1998; Tompkins, Greenman & Hudson, 2001). Indeed, parasitemediated competition and apparent competition have been implicated in species invasions (Settle & Wilson, 1990; Rushton et al., 2000), whereas the role of parasite-mediated predation during invasions remains unknown. This is surprising, given the potential of predation among invaders and natives to change community structure (Zaret & Paine, 1973; Schoener & Spiller, 1996; Dick & Platvoet, 2000). Amphipod crustaceans provide an ideal model to test if and how parasites mediate predation during invasions. Amphipods feature in many invasions, because of coincidental transport with humans and deliberate introductions for fish farming, angling and even ecological experiments (Pinkster et al., 1992; Dick, Nelson & Bishop, 1997; MacNeil, Dick & Elwood, 1999a). In addition, intraguild predation (IGP), that is predation between species using the same resources in a similar way (Polis, Myers & Holt, 1989), is a driving force in exclusions and replacements involving amphipods (e.g. Dick, 1992, 1995, 1996; Dick & Platvoet, 1996, 2000; MacNeil, Elwood & Dick, 1999b; MacNeil & Prenter, 2000; MacNeil et al., 2003a). Further, amphipods are host to a wide variety of parasites that affect, for example, their behaviour (Crompton, 1970; Maynard et al., 1998; Cezilly, Gregoire & Bertin, 2000; Thomas, Fauchier & Lafferty, 2002). In Ireland, Gammarus pulex (L.) transplanted from England have invaded populations of the native G. duebeni celticus Stock & Pinkster (Strange & Glass, 1979). Males of each species frequently kill and eat moulting female congenerics (Dick, 1992), although precopula guarding reduces the frequency of such predation (Dick et al., 1993). Male G. pulex are more predatory than male G. d. celticus in attacking both guarding male and guarded female congenerics (Dick, Elwood & Montgomery, 1995). This differential IGP has resulted in the widespread replacement of the native (Dick, 1996; Dick et al., 1999; MacNeil et al., 2001). However, in many Irish rivers, parasites are found in both G. pulex and G. d. celticus (Dunn & Dick, 1998). For example, in the River Lagan, both amphipods are intermediate hosts for the brown trout acanthocephalan parasite Echinorhynchus truttae Schr. Despite numerous studies documenting how fish and bird acanthocephalan parasites alter the behaviour

and physiology of Gammarus hosts to facilitate trophic transmission (e.g. Kennedy, Broughton & Hine, 1978; Poulin, 1995; Lafferty, 1999; Cezilly et al., 2000; MacNeil et al., 2003b), no study has examined the potential impacts of acanthocephalan parasitism on IGP interactions between Gammarus species. Poulin (1995) recommended that, when studying behavioural changes in parasitised animals, one should adopt field experiments, as the consequences of a behavioural change induced by a parasite may vary according to conditions in which they are measured. The aims of the present study were thus to determine: (i) by field survey, whether patterns of parasitism in G. pulex differed from those in G. d. celticus; (ii) by field experiment, whether parasitism of G. pulex influences predation on G. d. celticus and (iii) by laboratory experiment, if parasitism of male G. pulex affects the predatory impact and behaviour of G. pulex towards moulted G. d. celticus females.

Methods Field survey E. truttae prevalences in G. pulex and G. d. celticus populations were determined by sampling 25 sites throughout the R. Lagan system (Fig. 1 and see Dick et al., 1993 for site details). During September 2000, each site was kick sampled (0.9 mm mesh net) to obtain at least 100 adult amphipods which were preserved on site in 70% ethanol. In the laboratory, adults were identified to species level and the presence/absence of E. truttae confirmed by dissection. Juvenile amphipods (<6 mm body length) were excluded, as parasitism is negligible in this size class (MacNeil et al., 2003b).

Field experiment This was conducted during August 2001 in the Minnowburn (U.K. grid ref. J333695), a tributary of the R. Lagan where G. pulex has replaced G. d. celticus in the lower stretches (see Fig. 1) and where E. truttae is present, with all parasites at the same cystacanth developmental stage in amphipod hosts at this time of year (MacNeil et al., 2003b). G. pulex were collected from a well defined riffle-pool sequence in which dissolved oxygen was 9.1 mg L)1, temperature 8.1 C (DO2 meter 9071, Jenway, U.K.), conductivity
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Parasite mediated intraguild predation 2087

Fig. 1 River Lagan survey sites, showing distributions and relative abundance of invader G. pulex and native G. duebeni celticus and prevalences of Echinorynchus truttae. Location of bioassay tube site is also indicated (see Fig. 2).

300 lS cm)1, pH 7.2 (Water-Test meter, Hanna, U.S.A.) and average score per taxon (ASPT) biotic index 4.5 (see Armitage et al., 1983). Adult G. d. celticus were collected from 4 km upstream, where dissolved oxygen was 9.1 mg L)1, temperature 8 C, conductivity 310 lS cm)1, pH 7.2 and ASPT 4.43. Unparasitised G. pulex, E. truttae parasitised G. pulex and unparasitised G. d. celticus were sorted by eye and housed separately overnight in plastic trays (30 · 60 · 10 cm, width · length · height), with aerated source water, substrate and leaf material from collection sites. Bioassay tubes (see MacNeil, Dick & Elwood, 2000a) were lengths of polyvinyl chloride (PVC) pipe (length 20 cm, diameter 5 cm) covered at both ends with nylon mesh (1 mm pore size). This retained amphipods and allowed free flow of water but prevented clogging with silt (MacNeil et al., 2000a). Tubes were secured to a slate base by a drain pipe clip and orientated 45  to the water flow on the river-bed to allow free flow through the tube while preventing amphipods being forced to one end. Each tube contained water-conditioned oak (Quercus robur) and alder (Alnus glutinosa) leaves, and five cat-fish food pellets providing for the omnivorous diet of
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amphipods (see MacNeil, Dick & Elwood, 1997). Two 5 cm strands of the pondweed Elodea canadensis and five hollow stone tubes (1 · 1 cm, length · diameter, 0.8 cm diameter hole) provided a standardised substrate within each tube. There were five experimental groups, each with n ¼ 8: (i) 10 unparasitised G. pulex, (ii) 10 parasitised G. pulex, (iii) 10 unparasitised G. d. celticus, (iv) five unparasitised G. pulex plus five unparasitised G. d. celticus and (v) five parasitised G. pulex plus five unparasitised G. d. celticus. Adult animals in each group were added at random (unsexed), with parasitised and unparasitised G. pulex matched in terms of body length by eye (to minimise stress). Eight sets of five tubes (one of each treatment) were placed throughout the site (sets at least 5 m apart), so that replicates were exposed to similar microhabitats and hydrological regimes. Individual tubes were thus treated as the replicate sample unit (see Gibbins, Soulsby & Merrix, 1994; MacNeil et al., 2000a). Tubes were examined weekly for 3 weeks, dead amphipods removed, additional food supplied and tubes placed back on the river-bed. The proportion of initial numbers that survived were arcsine transformed before statistical analysis (Sokal & Rohlf, 1995), but Fig. 2 shows untransformed percentages. Survival of unparasitised G. pulex, parasitised G. pulex and unparasitised G. d. celticus in single species tubes was compared in a two-factor A N O V A (‘Super A N O V A ’, Abacus Concepts, 1989), the factors being ‘amphipod group’ (as above) and ‘time’ (a repeated measure). Survival in mixed species tubes was analysed in a separate three-factor A N O V A , the factors being ‘species’ (repeated measure), ‘parasite status of G. pulex – unparasitised or parasitised’ and ‘time’ (repeated measure).

Laboratory experiment 1 In September 2001, G. pulex and G. d. celticus were collected, maintained as above, in a light : dark cycle appropriate for the time of year (12 : 12 h) and allowed to acclimatise for 2 weeks prior to experiments, which were conducted in a 1 : 1 mixture of water from the two sites. Moulted females are vulnerable to predation by congeneric males (Dick et al., 1995, 1999), thus we tested the effect of parasitism of G. pulex on the frequency of predation of G. d. celticus females. We

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Fig. 2 Mean (+SE) % survival of: (a) unparasitised and parasitised invader G. pulex and unparasitised native G. duebeni celticus in single species tubes; (b) unparasitised and parasitised invaders with the native in mixed species tubes and natives with unparasitised and parasitised invaders in mixed species tubes.

monitored 60 precopula pairs of G. d. celticus that had been placed individually in 330 mL containers. When a female moulted and was released by the guarding male, she was immediately presented to either an unparasitised or parasitised male G. pulex held in separate 330 mL containers n ¼ 30 both groups) and the outcome recorded after 12 h (constant light). Unparasitised and parasitised G. pulex were matched for size by eye and, at the end of the experiment, all G. pulex were killed and body lengths measured.

Laboratory experiment 2 Animals were collected and maintained as above. Precopula pairs of G. d. celticus were separated on tissue paper and individuals allowed to recover for 30 min. Then, using males and females not previously paired with one another, precopula pairs were allowed to establish for 30 min and then placed in a 330 mL plastic container with either unparasitised or parasitised male G. pulex (n ¼ 30 both groups), again matched for size by eye. We recorded behaviour using
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Parasite mediated intraguild predation 2089 Table 1 Behaviour recorded during predatory interactions (frequency as percentage of total observation period) (1) Gammarus pulex male swimming towards and contacting G. duebeni celticus pair with antennae (2) G. pulex grabbing at G. d. celticus female with gnathopods (3) G. pulex tugging at G. d. celticus female when female grabbed (4) G. pulex grabbing/attacking guarding G. d. celticus male (5) G. pulex other, non-contact behaviour (6) Defensive kicks at G. pulex male by guarding male G. d. celticus (7) G. d. celticus male other, non-contact behaviour (8) Defensive kicks at G. pulex male by G. d. celticus female (9) Kicks/attacks at G. pulex male (10) G. d. celticus female other, non-contact behaviour

‘The Observer’ (Noldus Information Technology, 1995) for 20 min per replicate (see Table 1 for details of activities recorded). At the end of the experiment, all G. pulex were killed and body lengths recorded. Behavioural frequency data were analysed by t-tests.

Results Field survey Of the 25 sites, 13 contained only G. pulex, eight only G. d. celticus and four were mixed (mean ± SE ¼ 274 ± 69 individuals collected per site; Fig. 1). Gammarus pulex was more frequently parasitised than G. d. celticus (94% compared with 42% of sites; v2 ¼ 9, d.f. ¼ 1, P < 0.01). In sites with the parasite present, E. truttae prevalence was significantly higher in G. pulex than in G. d. celticus, ranging from 1 to 8% in the former and 1% or less in the latter (Z ¼ 3.92, P < 0.0001, Mann–Whitney U-test).

Field experiment In single species tubes, there was no significant difference in survival among unparasitised invaders, parasitised invaders or natives [F2,21 ¼ 0.5, not significant (NS); Fig. 2a]. While survival of amphipods decreased significantly over time (F2,42 ¼ 78.8, P < 0.0001; Fig. 2a), this remained above 85% for all groups. There was no ‘group · time’ interaction (F44,42 ¼ 2.3, NS). In mixed species tubes, survival of G. pulex was significantly higher than that of G. d. celticus F1,14 ¼ 41.4, P < 0.0001; Fig. 2b), with G. pulex survival never <85% and unaffected by parasitism (Fig. 2b). There was a significant ‘species · parasite status of
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G. pulex ’ interaction (F1,14 ¼ 15.3, P < 0.01; Fig. 2b) and an overall ‘species · parasite status of G. pulex · time’ interaction (F2,28 ¼ 8.9, P < 0.01; Fig. 2b), which reflects the greater survival of G. d. celticus in the presence of parasitised as compared with unparasitised G. pulex, which is exaggerated over time. The presence of precopula pairs within each species in all single and mixed species tubes indicated that animals were not unduly stressed by tube conditions (MacNeil et al., 2000a). In mixed tubes we observed ‘clumps’ of several unparasitised invaders killing natives on three occasions and numerous G. d. celticus body parts were found in all mixed species tubes.

Laboratory experiment 1 Twelve (40%) moulted female natives were predated by unparasitised invaders compared with only two (7%) by parasitised invaders (P < 0.01, Fisher exact probability test). Body lengths of unparasitised and parasitised male G. pulex were not significantly different (means ± SE; 16.6 ± 0.8 mm and 16.9 ± 1.2 mm; t28 ¼ 1.4, NS).

Laboratory experiment 2 Parasitised G. pulex significantly more often contacted the G. d. celticus pair than did unparasitised G. pulex (t58 ¼ 6.9, P < 0.001). Despite this, grabbing and tugging at the pair was almost identical for both G. pulex groups, as was the defensive kicking of male and female G. d. celticus towards the two types of attackers. Consequently, parasitised G. pulex attacked pairs significantly less often per contact than did unparasitised G. pulex (t58 ¼ 2.7, P < 0.01; Fig. 3a), leading to significantly less defensive kicking from the pairs of male and female G. d. celticus (t58 ¼ 2.1, P < 0.05; Fig. 3b). Two unparasitised male G. pulex successfully took female G. d. celticus from their precopula pairs and ate them, whereas no parasitised male G. pulex did so. Mean body lengths of parasitised and unparasitised male G. pulex did not differ (means ± SE; 16.7 ± 0.7 mm and 16.5 ± 0.9 mm; t28 ¼ 1.2, NS).

Discussion Our field survey showed that first, significantly more G. pulex than G. d. celticus populations had E. truttae

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(a)

(b)

Fig. 3 Mean (+SE) numbers of: (a) predatory attacks per antennal contact by male G. pulex with Gammarus duebeni celticus pair (b) defensive kicks by G. d. celticus pair per attack by male G. pulex.

and, secondly, the invader, G. pulex, had a higher prevalence of E. truttae than did the native. Although at the ‘site level’ E. truttae prevalence never exceeded 8% for G. pulex, there can be strong ‘patch level’ aggregation of parasitised G. pulex. For instance, MacNeil et al. (2003a) found an overall E. truttae prevalence of 4.1% at the ‘site level’ (n ¼ 1100 adult G. pulex), but in patches of this site as delineated by a 0.25 · 0.25 m Surber sampler, up to 70% of individuals were parasitised. Thus, any effect of E. truttae parasitism on individual G. pulex may manifest itself in patch level interactions between G. pulex and co-occurring amphipods and non-amphipods (Kelly et al., 2003). In particular, as laboratory studies indicate that differential mutual IGP between G. pulex and G. d. celticus leads to the invader eliminating the native (Dick et al., 1993, 1995, 1999), parasitism has the potential to mediate this interaction, within invaded systems. In the field experiment, after 3 weeks, G. pulex was little affected by G. d. celticus. On the other hand, G. d. celticus survivorship declined dramatically in the

presence of both parasitised and unparasitised G. pulex, but parasitism clearly reduced the impact of G. pulex on G. d. celticus. Our data and observations indicate that unparasitised invaders were more predatory than those that were parasitised. Although this field experiment had the advantage of assessing the outcomes of IGP against a realistic habitat template, further evidence for parasitism reducing the predatory threat of the invader was provided in two laboratory experiments. First, there was lower predation of moulted female natives by parasitised than unparasitised invaders. Secondly, there were behavioural differences linked to parasitism that explain underlying IGP outcomes between the invader and native. Although E. truttae parasitised invaders had more contacts with paired natives than those unparasitised, contacts between a parasitised male invader and precopula pairs of G. d. celticus were less likely to lead to a predatory attack. The higher activity level of parasitised G. pulex is an important ‘trigger mechanism’ in stimulating brown trout to attack G. pulex (MacNeil, Elwood & Dick, 1999c), and thus facilitate trophic transmission. In the interaction between G. pulex and G. d. celticus, however, the parasite seems to reduce predatory capabilities, although the precise mechanism is uncertain and requires further study. Factors such as habitat preference and differential physico-chemical tolerance can promote coexistence between several amphipod species where, under other environmental regimes, one or more would be eliminated by IGP (Dick, 1996; MacNeil et al., 1999b,c, 2000a, 2001). Our study shows that parasitism may also influence the outcomes of IGP and therefore, species replacement or coexistence (MacNeil et al., 1997). If parasitism reduced the predatory tendencies of the native in a similar fashion to that of the invader, then higher prevalence in the native could promote its replacement. Of course, the effects of parasitism on IGP must be balanced against direct effects of the parasite on its host, which include increased vulnerability to predators that may be shared by both amphipod species (MacNeil et al., 1999a; MacNeil, Elwood & Dick, 2000b). Parasite-mediated competition between closely related species has received renewed interest as an important determinant of community structure (e.g. Schall, 1992; Thomas et al., 1995; Hudson & Greenman, 1998; Tompkins et al., 1999; Tompkins et al., 2001). However, our study shows that parasite
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Parasite mediated intraguild predation 2091 mediated predation between closely related host species could be an important community structuring mechanism in Irish freshwaters, particularly in river systems where parasite prevalence levels differ significantly between host species. In addition, G. pulex is a major predator of many other macroinvertebrate species (MacNeil et al., 1997, 2002; Kelly et al., 2002, 2003) and it is possible that the reduced predatory tendency witnessed in interactions with G. d. celticus could manifest itself in G. pulex interactions with these other prey species. There is increasing evidence that the invader has eliminated many non-amphipods in Irish rivers (MacNeil et al., 2000b; Kelly et al., 2002, 2003) and indeed, Savage (1996) regarded another invasive amphipod, G. tigrinus Sexton, as a ‘keystone species’ in an English lake, as it influenced the population dynamics of non-amphipod taxa. Thus, parasitism of such invaders could maintain or increase biodiversity and further research on the community influences of parasite mediated interspecific interactions is clearly required.

Acknowledgements Thanks to Gillian Riddell, Jason Pickford and Dr Zoe Ruiz, who were helpful in a variety of ways in the production of this manuscript. Funded by NERC grant GR3/12871.

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