Intraguild predation may reinforce a species–environment gradient

Acta Oecologica 41 (2012) 90e94

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Original article

Intraguild predation may reinforce a specieseenvironment gradient Calum MacNeil a, Jaimie T.A. Dick b, * a b

Dept of Environment, Food and Agriculture, Thie Slieau Whallian, Foxdale Road, St. Johns IM4 3AS, Isle of Man School of Biological Sciences, Queen’s University Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 February 2012 Accepted 26 April 2012 Available online 23 May 2012

Specieseenvironment gradients are ubiquitous in nature, with studies often partially explaining the replacement of species along such gradients by autecological factors such as differential physiological tolerances. However, lacking direct evidence, the majority of studies only infer some form of interspecific interaction, often competition, as reinforcing these gradients. There is usually the further implication that environmental factors mediate asymmetries in the interaction. Recognising the lack of explicit experimental considerations of how key inter-specific interactions are modified by the environment, we chose a study system where we were able to bring the species in question into the laboratory and conduct experiments to test hypotheses about gradient-induced asymmetries in an interspecific interaction. To this end, we tested the hypothesis that a speciesesalinity gradient may be reinforced by changes in the asymmetry of intraguild predation between two species of amphipod crustaceans with wide salinity tolerances. River and estuary surveys showed that Gammarus duebeni and Gammarus zaddachi have overlapping distributions, with both surviving and reproducing in salinities ranging from freshwater to fully marine. However, the former species is relatively more abundant in low salinities and the latter in higher salinities. In the laboratory, survival of both species was high in all salinities and cannibalism occurred at low frequencies. However, intraguild predation by males on moulted females was asymmetric in favour of G. duebeni at low salinities, this asymmetry completely reversing to favour G. zaddachi at higher salinities. Thus, we provide evidence that this species eenvironment gradient occurs due to overlapping physiological tolerances and salinity-driven shifts in the asymmetry of a key inter-specific interaction, intraguild predation. Ó 2012 Elsevier Masson SAS. All rights reserved.

Keywords: Species replacements Environmental gradients Intraguild predation Salinity tolerance Amphipod

1. Introduction Species replacements along environmental gradients are well documented, with many studies proposing that inter-specific interactions, primarily competition, might act to reinforce such specieseenvironment gradients (Terborgh, 1971; Bull, 1991; Werner and McPeek, 1994; Engels and Jensen, 2010). However, there are few empirical studies identifying and quantifying such inter-specific interactions (Taniguchi and Nakano, 2000; McCauley, 2007; Engels and Jensen, 2010), with demonstrations of shifts in interaction asymmetry due to environmental change remaining especially elusive. Further, competition is often cited as a reinforcing mechanism, but with little or no direct evidence other than the species distributional patterns themselves, a somewhat tautological argument (Dick, 2008). These loose references to competition may be particularly misleading where other inter-specific

* Corresponding author. Tel.: þ44 2890972286; fax: þ44 2890975877. E-mail address: [email protected] (J.T.A. Dick). 1146-609X/$ e see front matter Ó 2012 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2012.04.012

interactions have been ignored or not recognised. For example, decades of research on amphipod crustacean interactions assumed that inter-specific competition drove species distributions and abundances, with little empirical evidence (Dick, 1992, 2008). Intraguild predation (IGP), or predation among actual or potential competitors, has been shown to be widespread throughout the animal kingdom, ranging from aphids (Lucas, 2005) to fish (Szeinfeld, 1991) to big cats (Laurensen, 1994) and crucial to the trophic structuring of many animal communities (Arim and Marquet, 2004). It is now recognised that such IGP is ubiquitous among amphipods (Dick, 2008) and that small IGP asymmetries override even major differences in competitive abilities and reproductive rates between species (Dick et al., 1993; Dick and Platvoet, 1996; Otto, 1998; Hatcher et al., 2008). Here, we examine IGP as a potential mechanism in the reinforcement of a well-known speciesesalinity gradient in amphipods, focussing on quantifying shifts in the asymmetry of IGP along the environmental gradient. In Spooner’s classic study on amphipod crustaceans (Spooner, 1947), the relative distributions of an estuarine Gammarus

C. MacNeil, J.T.A. Dick / Acta Oecologica 41 (2012) 90e94

species, a salt-tolerant species and a freshwater species were ascribed to differences in salinity tolerance, this being an oftquoted example in text books (e.g. Begon et al., 1986). Similarly, the overlapping distributions of five Gammarus species have been ascribed to changing salinity and possibly competition (Fenchel and Kolding, 1979), although all the above authors recognised the lack of direct evidence for resource competition and indeed this might not be expected where resources are super-abundant and thus not limiting (see Dick, 2008). On the other hand, IGP among Gammarus species, and the mediation of this interaction by salinity conditions, might better explain gradients of co-existence and exclusion. Therefore, in the present study, we tested the hypothesis that changes across salinities in the asymmetry of IGP between the essentially salt-tolerant estuarine species Gammarus zaddachi Sexton, and the euryhaline species Gammarus duebeni Liljeborg, may reinforce the salinity gradient and account for field distribution patterns. 2. Materials and methods 2.1. Field surveys From FebruaryeMarch 2006, we kick-sampled G. duebeni and G. zaddachi from four rivers and their estuaries on The Isle of Man, British Isles (Fig. 1; Sulby River SC443951, River Douglas SC368756, SC375752, SC378752; Glashen Stream SC287683, SC287681, SC287677, Silverburn River SC267682, SC266676; grid references are U.K. ordnance survey), to assess the distributions and relative abundances of the two species with respect to salinity. Sample sites on each river/estuary were chosen on the basis of accessibility and safety, thus not all had the same number of sample sites (Fig. 1). At each sampling site, we collected between 130 and 520 individuals and used a Y.S.I. 556 MultiProbe to measure salinity and temperature over one tidal cycle (low to high tide, 7 h, one measurement per hour; see Fig. 1; Table 1). 2.2. Laboratory experiments To examine the influence of salinity on intraguild predation frequencies between the two species, we focussed on low (0&), moderate (6&) and high (33&) salinities as representative of field conditions (see Fig. 1; Table 1). All animals in experiments were collected from the River Douglas, since they were in greatest abundance there, G. duebeni were taken from the uppermost site (0&) and G. zaddachi from the lowermost site (33&; see Fig. 1), these sites offering large areas where we could collect large numbers of animals to provide sufficient replication in our control and experimental groups (see below). Experimental arenas were plastic aquaria (6 cm diameter) with 50 ml of the source water (0, 6 or 33&), with sand substrate and hiding places in the form of a ceramic tube 1 cm long, 0.6 cm diameter and a glass pebble 1.5 cm diameter and fed catfish food pellets (which both species readily consume) in excess. Temperature was maintained at 9  C, water aerated daily and salinities maintained by addition of distilled water. Animals used in laboratory experiments were adult males and females in, or separated from, pre-copulatory mate-guarding pairs (these were gently teased apart on tissue paper followed by a recovery period of 24 h). We used body size ranges of adults of the two species that were representative of field populations, that is, male and female G. duebeni of 35e46 mg and 17e25 mg respectively and G. zaddachi of 10e17 mg and 4e7 mg respectively. Control groups were single animals of each sex/species/salinity combination (n ¼ 72 each). Single males placed with either a single or a guarded female conspecific (n ¼ 72 all cases, each salinity) tested for frequencies of cannibalism. Concurrently, at each salinity,

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single males were placed with either a single or a guarded female congeneric and examined for intraguild predation (n ¼ 72 all cases). Aquaria were inspected daily until females moulted and either survived, were cannibalised or preyed upon (time to moult for both species ranged from 1 to 11 days). Statistical comparisons of raw frequency data were made with the Chi-square test, specifically, 2  2 contingency analysis. 3. Results 3.1. Field surveys In all rivers/estuaries sampled, G. duebeni dominated in low salinities, whereas G. zaddachi dominated in high salinities, with their relative abundances more evenly balanced at moderate salinities (Figs. 1and 2 and Table 1). Precopula pairs and juveniles of both species were present at all sites. We did not find any infections by microsporidian or acanthocephalan parasites, both of which are easily detected by eye (former turn the abdomen opaque, latter are coloured cysts visible through cuticle; see MacNeil et al., 2003a,b). No animals used in experiments had visible parasites. 3.2. Laboratory experiments In the laboratory experiments, mortality of single control animals at all of the sex/species/salinity combinations was negligible (3% or less) and cannibalism occurred at 0e8% per experimental group. At low and moderate salinities, there was significantly differential intraguild predation (IGP) in favour of G. duebeni (Table 2a and b; Fig. 2), however, this reversed at the high salinity, with G. zaddachi the superior intraguild predator (Table 2c, Fig. 2). Further, overall intraguild predation of G. zaddachi by G. duebeni decreased significantly as salinity increased (c2 ¼ 12.3, 11.7 and 23.8 for single females, guarded females and overall, respectively, all d.f. ¼ 2, P < 0.003 for both female groups and P < 0.0001 overall), whereas the reverse was true for G. zaddachi predation of G. duebeni (c2 ¼ 17.2, 13.7 and 30.7 respectively, all d.f. ¼ 2, P < 0.001 for both female groups and P < 0.0001 overall; see Table 2 and Fig. 2). At all salinities and for both species, mate-guarding did not significantly reduce intraguild predation of females (c2 ¼ 0.79, 0.48 and 0.46 for guarded versus single G. zaddachi females at 0, 6 and 33& respectively and c2 ¼ 0.65, 0 and 0.37 for guarded versus single G. duebeni females at 0, 6 and 33& respectively, all d.f. ¼ 2, all NS). Mean (s.e.) time to death at moult did not differ between the two species, this being 8.44 (0.96) days for G. zaddachi and 7.11 (0.84) days for G. duebeni (t ¼ 0.88, d.f. ¼ 160, NS). 4. Discussion Specieseenvironment gradients have traditionally been explained by autecological factors, such as physiological tolerance, however, the role of environmentally driven asymmetries in interspecific interactions in reinforcing such patterns has usually only been inferred (Bull, 1991; Taniguchi and Nakano, 2000). Although there has been more recent progress in disentangling the effects of abiotic and biotic drivers of community change along gradients (e.g. Lessard et al., 2011), explicit experimental considerations of how key inter-specific interactions are modified by the environment are still lacking. Here, we chose a study system where we were able to bring the animals in question into the laboratory and conduct wellreplicated experiments to test hypotheses about gradient-induced asymmetries in an inter-specific interaction. We thus provide a rare worked example of a reversal in the asymmetry of an interspecific interaction across an environmental gradient.

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Fig. 1. Relative abundance of Gammarus duebeni and G. zaddachi in Isle of Man river/estuary systems; þ denotes sample site location and corresponding salinity level (ppt) is shown beneath each site pie chart. The three sample site locations indicated for the River Douglas were also the collection sites for animals used in the laboratory study.

Physiological adaptation has allowed amphipods to inhabit marine, brackish and freshwater environments (Sutcliffe, 1968), with some species capable of survival and reproduction in an extremely wide range of salinities. G. zaddachi is primarily estuarine, but is capable of colonising freshwater (Spooner, 1947; Gaston and Spicer, 2001) and, in the present study, precopula breeding pairs and juveniles were found in freshwater. G. duebeni has even wider tolerances, being found in rivers and lakes, throughout estuaries and in hyper-saline rock pools (Gaston and Spicer, 2001;

Rock et al., 2007). In one study, G. duebeni was found in an Irish freshwater stream all the way down to the high water mark and in the surrounding rock pools with salinities up to 27& (McCartan and Slinn, 1953). Thus, in the absence of each other, either of these species could colonise virtually the entire salinity range of a river/estuary. This suggests that field patterns are also shaped by some form of inter-specific interaction. Since intraguild predation has now been recognised as a powerful force in determining invaderenative amphipod species displacements (Dick, 2008;

C. MacNeil, J.T.A. Dick / Acta Oecologica 41 (2012) 90e94 Table 1 Median (and range) salinity levels and water temperatures from designated low, moderate and high salinity sites on four sampled rivers/streams. Measurements taken over one tidal cycle for 7 h with one measurement per hour. Sites correspond to those detailed in Fig. 1. River/Stream

Site salinity level designation

Salinity level (&)

Water temperature ( C)

Sulby River River Douglas

High Low Moderate High Low Moderate High Low High

31 0 6 33 0 4 36 0 30

5.0 4.5 4.6 4.4 4.9 4.7 4.7 4.1 4.0

Glashen Stream

Silverburn River

(30e32) (0) (4e8) (32e34) (0) (3e5) (34e36) (0) (29e30)

(4.9e5.0) (4.4e4.6) (4.5e4.7) (4.3e4.5) (4.8e5.0) (4.6e4.8) (4.6e4.8) (4.0e4.3) (3.9e4.14)

Kestrup and Ricciardi, 2009; Piscart et al., 2009), we tested the hypothesis that salinity-driven shifts in the asymmetry of intraguild predation between G. duebeni and G. zaddachi may reinforce patterns of changing relative abundances in their overlapping distributions. We found from both the field and laboratory that both species survive and reproduce at all field salinities, the latter evidenced by pre-copulation and the presence of juveniles in brood pouches and samples. There was some cannibalism as expected (see Dick, 2008), but at low frequencies compared to IGP. The asymmetry in IGP was in favour of G. duebeni at low salinities, reversing at high salinity in favour of G. zaddachi. That salinity drove such a dramatic shift in intraguild predation is all the more remarkable since the male/ female body size ratio was much greater for G. duebeni males:G. zaddachi females than in the reciprocal interaction. However, in amphipods, moulting females are especially

100

80

%

60

40

O

O X

20

0

X 0

X 6 Salinity ppt

O 33

Fig. 2. Bars are percentage of river/estuary samples at each salinity comprised of Gammarus duebeni (clear) and G. zaddachi (stipled); from our laboratory experiments, X ¼ overall percentage of intraguild predation of female G. duebeni and O ¼ same of female G. zaddachi. Sketch shows a typical predatory attack by a male gammarid on a recently moulted female congeneric.

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Table 2 Frequencies of intraguild predation by Gammarus duebeni (Gd) on G. zaddachi (Gz) and vice versa under different salinities. Comparisons of raw data are with the c2 test (n ¼ 72 in all cases, except for ‘overall’ where n ¼ 144). Salinity/interaction (a) 0 ppt/Males þ Single females Guarded females Overall (b) 6 ppt/Males þ Single females Guarded females Overall (c) 33 ppt/Males þ Single females Guarded females Overall

Gd on Gz, %

Gz on Gd, %

c2

P

36 29 33

4 3 4

22.8 18.7 41.4

<0.0001 <0.0001 <0.0001

38 32 35

6 6 6

21.8 16.5 38.1

<0.0001 <0.0001 <0.0001

14 10 12

24 19 22

2.2 2.7 4.9

0.14 0.10 <0.03

vulnerable to predation by male congenerics and even females that are similar in size or indeed larger than congeneric males can be readily overpowered and consumed (Dick et al., 1993; Dick, 2008). We also found here that precopula mate-guarding did not protect females from IGP, as has been found in some other interacting species (Dick et al., 1993). The physiological process of moulting is heavily influenced by ionic conditions and such water chemistry is further associated with levels of IGP (e.g. Dick and Platvoet, 1996; Kestrup and Ricciardi, 2009). Thus, we speculate that moulting in females of the two species in the current study is differentially affected by salinity, such that females are then differentially susceptible to IGP. Whatever the mechanism, it is clear that IGP can rapidly remove reproductive females and thus reduce population recruitment, leading to very rapid species replacements, evidenced both empirically and theoretically (Dick et al., 1993; Hatcher et al., 2008). Empirical and theoretical studies of intraguild predation in combination with inter-specific competition agree that asymmetries in the former are much more important in driving species displacements than the latter (Dick et al., 1993; Hatcher et al., 2008). Also, the absolute levels of IGP are less important than relative levels (Dick and Platvoet, 1996). Further, even if salinity drives changes in the reproductive rates of the two species, we have previously shown that even very small differences in the asymmetry of IGP between species overrides even large species differences in reproductive rates (Dick and Platvoet, 1996). As asynchronies in IGP were very large in the present study, any influence of differences in reproductive rate are at best only likely to slightly refine the zones of co-existence (see Dick and Platvoet, 1996). In the present context, the changing asymmetries in IGP along the salinity gradient would thus be predicted to lead to near complete species exclusions, as indeed appears to occur at the lower and higher salinities, although both species are physiologically able to survive and reproduce at both extremes. The zones of co-existence appear to occur where intraguild predation becomes more balanced, and indeed, Dick and Platvoet (1996) showed theoretically that small shifts in the asymmetry of IGP could lead to ‘switches’ in species dominance, the time-lags giving the impression of co-existence. It is also likely, however, that upstream and downstream movements of the two species contribute to their mixing. Further, the present study highlights that simply invoking inter-specific competition as the likely interaction reinforcing a specieseenvironment gradient can be misleading, as more direct and powerful forces such as IGP might play the major role (Dick, 2008). Finally, we encourage others to engage in experimental elucidation of environmentally driven shifts in the strength of inter-specific interactions and the role this may play in reinforcing the ubiquitous phenomenon of specieseenvironment gradients.

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