MARINE ECOLOGY PROGRESS SERIES Vol. 291: 151–158, 2005 Published April 28 Mar Ecol Prog Ser Predatory nature of the littoral amphipod Echinogammarus marinus: gut content analysis and effects of alternative food and substrate heterogeneity Jaimie T. A. Dick*, Mark P. Johnson, Susan McCambridge, Jamie Johnson, Victoria E. E. Carson, David W. Kelly, Calum MacNeil School of Biology & Biochemistry, Medical Biology Centre, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK ABSTRACT: Interspecific interactions are major structuring forces in marine littoral communities; however, it is unclear which of these interactions are exhibited by many key-component species. Gut content analysis showed that the ubiquitous rocky/cobble shore amphipod Echinogammarus mari- nus, often ascribed as a mesograzer, consumes both algae and macroinvertebrates. Further, labora- tory experiments showed that E. marinus is an active predator of such macroinvertebrates, killing and consuming the isopod Jaera nordmanni and the oligochaete Tubificoides benedii. Predatory impacts of E. marinus were not alleviated by the presence of alternative food in the form of alga discs. However, in the presence of prey, consumption of alga by E. marinus was significantly reduced. Fur- ther, survival of prey was significantly higher when substrate was provided, but predation remained significant and did not decline with further increases in substrate heterogeneity. We conclude that such amphipods can have pervasive predatory impacts on a range of species, with implications for community structure, diversity and functioning. KEY WORDS: Littoral communities · Predation · Gut content · Amphipods · Heterogeneity · Echinogammarus marinus Resale or republication not permitted without written consent of the publisher INTRODUCTION Duffy & Harvilicz 2001). However, the emphasis on a ‘mesograzer’ lifestyle of widespread species such as Marine littoral communities are structured by a com- Gammarus locusta and Echinogammarus marinus has bination of physical factors and biotic interactions (Lit- led to neglect of the potential predatory impact of such tle & Kitching 1996). Classically, it is recognised that gammarids in aquatic communities (Kelly et al. 2002a). organisms on rocky/cobble shores such as algae, bar- Indeed, freshwater community ecology offers many nacles and mussels compete for space, with further lessons in this respect, with the presumed herbivo- structuring influences of predators such as crabs, dog- rous/detritivorous ‘functional’ role of freshwater Gam- whelks and starfish (e.g. see Paine 1980, Bertness marus species challenged by both field and laboratory 1999). However, the roles of many other key compo- studies (reviewed by MacNeil et al. 1997, see also nent species in structuring such communities remain Kelly et al. 2002a). In particular, freshwater Gammarus unclear, particularly where there is uncertainty spp. are now viewed as predators of a range of regarding the types of interspecific and trophic inter- macroinvertebrates (Kelly et al. 2002a,b), with major actions in which they engage. Amphipods are ubiqui- community structuring influences (Kelly et al. 2003). tous in the marine littoral zone and many species are Recognition of the potential predatory role of marine clearly able to utilise plant material in their diet (e.g. littoral amphipods is important if the range of lethal, Pavia et al. 1999, Duffy & Hay 2000, Karez et al. 2000, non-lethal, direct and indirect consequences of preda- *Email: [email protected] © Inter-Research 2005 · www.int-res.com 152 Mar Ecol Prog Ser 291: 151–158, 2005 tion (e.g. see Lima 1998) is to be appreciated in such County Down, Northern Ireland, from September to communities. It is thus now timely to explore predatory March of 2002 to 2003 and 2003 to 2004; laboratory interactions among marine littoral amphipods and work was conducted within the facility. We found 3 potential prey species. abundant algae growing on the cobbles: Ulva lactuca A number of techniques can be employed to exam- (green), Palmaria palmata (red) and Fucus vesiculosus ine the predatory nature of a particular species. Gut (brown). Of the variety of macroinvertebrates ob- content analyses can provide evidence of consumption served when turning over cobbles, Echinogammarus of animal material, and can indicate a ‘carnivorous’ marinus was very abundant, together with 3 other spe- diet (e.g. see Yu et al. 2003). Whilst such analyses can- cies which were judged as potential prey of E. marinus, not discriminate between active predation and scav- since they were smaller than and in close proximity to enging of cadavers, they can provide support for or the amphipod. These were the isopod Jaera nord- against active predation. Clearly, if no animal material manni, the tubificid oligochaete Tubificoides benedii is ever found in the gut of a particular species, then and the collembolan insect Anurida maritima. predation can be discounted; however, presence of Gut content analyses. In order to quantify the diets of animal material in the gut can stimulate further re- Echinogammarus marinus in the field, we examined search into potential predatory behaviour. Stable iso- gut content of freshly collected specimens and related tope ratios offer an alternative, with one study showing these to the gut content of individuals fed known diets that a freshwater amphipod, Dikerogammarus villosus, in the laboratory. is on the same trophic level as some predatory fish spe- First, 40 Echinogammarus marinus (20 male + 20 fe- cies (Marguillier 1998). However, this technique may male adults, 10 to 16 mm body length) were starved suffer inaccuracies in elucidating trophic pathways individually in plastic containers (5 cm diameter) with (Hart & Lovvorn 2002) and is less useful in identifying 8 cm depth seawater (8 to 12°C) and a continuous flow which species of prey are actually consumed and how of filtered seawater, gauze near the bottom allowed such predation may impact by structuring the wider faeces to sink out of reach of the amphipods and gauze community. Laboratory experiments offer close control over the top prevented escape. Each day, 4 individuals of confounding variables and confidence in ascribing were killed in warm water and their guts dissected, cause-and-effect relationships, but may be criticised until all specimens killed on 2 consecutive days had on the grounds of lack of realism (see Huston 1999, empty guts. From this, we determined that 7 d was the Kelly et al. 2002a). However, micro- and mesocosm optimal period to ensure that individual E. marinus had studies are increasingly recognised as being of high fully evacuated their guts. fidelity in extrapolation to field patterns and processes Second, 120 (60 male + 60 female) Echinogammarus (e.g. Bergstrom & Englund 2002, Dick et al. 2002). marinus starved for 7 d were individually isolated (as Herein, we examine the predatory nature of a ubiq- above) and randomly allocated to 6 groups represent- uitous marine littoral amphipod, Echinogammarus ing the 3 algae and 3 invertebrates (see preceeding marinus. This species is found along NE Atlantic coasts subsection). Algae was presented as 1 cm2 sections and from Norway and Iceland to the north coast of Portugal (live) prey body lengths were 3 to 5 mm (Jaera nord- (Lincoln 1979). It inhabits the intertidal zone among manni), 5 to 10 mm (Tubificoides benedii) and 3 to 4 mm stones, shingle and algae and is often highly abundant (Anurida maritima). Once each E. marinus had partially (Maranhao et al. 2001, Martins et al. 2002). First, we or wholly consumed its allocated food item, it was killed conducted gut content analysis of freshly caught indi- in warm water and its gut immediately dissected and viduals. Second, we used a laboratory microcosm ex- examined to provide ‘signatures’ for each food type. periment to elucidate the relative balance of predatory Third, 116 Echinogammarus marinus (sizes as above) and herbivorous feeding behaviour by offering alter- were collected in small batches of 10 to 20 individu- native foodstuffs. Third, we mimicked levels of physi- als d–1 following tidal exposure, their guts were dis- cal heterogeneity encountered in the rocky littoral sected, and individuals were sexed (presence/absence zone and examined predatory impacts that may rea- of penile papillae and brood pouches). Gut material sonably be extrapolated to the field. was compared to reference ‘signature’ samples (see preceeding paragraph). Percentage contribution (vol- ume) to the entire gut content was estimated for each MATERIALS AND METHODS food type (including ‘unidentified’). Means (raw data arcsine-transformed; Sokal & Rohlf 1995) were com- General. All algae and animal collections took place pared with respect to food type by a 1-factor repeated- by searching over and under cobbles on ‘Walter’s measures ANOVA, with Fisher’s protected least signif- Shore’ (54° 22.95’ N, 5° 33.3’ W) in front of the Marine icant difference (FPLSD) post-hoc tests (in Fig. 1 means Laboratory of Queen’s University Belfast at Portaferry, of raw percentages are shown for clarity). Chi-square Dick et al.: Predation by a littoral amphipod 153 analyses were conducted on the raw count data to test alga consumption by prey species, while Group 5 for sex differences in gut contents. assessed any natural alga decay in the presence of, but Microcosm experiments. For the laboratory experi- isolated from, the prey species. ments, we chose 2 representative potential prey species, Percentage prey survival (arcsine-transformed; see the hard-bodied isopod Jaera nordmanni and the soft- Sokal & Rohlf 1995) was examined by a 2-factor bodied worm Tubificoides benedii, and the most ANOVA with respect to ‘group’ (1, 2 and 3) and ‘prey abundant alga, Fucus vesiculosus, all of which appeared species’. The percentage remaining alga area (arcsine- in Echinogammarus marinus guts. In the laboratory, for transformed) was examined in a 2-factor ANOVA with 24 h prior to experiments, individuals of each species respect to ‘group’ (1, 2, 4 and 5) and ‘prey species’ (in were housed separately in pots (15 cm diam. × 10 cm Figs.