Key words: Fish, freshwater, functional feeding group, Gammarus spp., ...... Whale-lice (Amphipoda, Cyamidae) on Lagenorhynchus albirostris in Dutch waters.
Biol. Rev. (), , pp. – Printed in the United Kingdom
THE TROPHIC ECOLOGY OF FRESHWATER GAMMARUS SPP. (CRUSTACEA : AMPHIPODA) : PROBLEMS AND PERSPECTIVES CONCERNING THE FUNCTIONAL FEEDING GROUP CONCEPT B CALUM MACNEIL, JAIMIE T. A. DICK ROBERT W. ELWOOD School of Biology and Biochemistry, The Queen’s University of Belfast, Medical Biology Centre, Lisburn Road, Belfast BT BL, N. Ireland (Received June ; revised November ; accepted November ) ABSTRACT
Gammarus spp. are widespread throughout a diverse range of freshwater habitats and can be the dominant part of many benthic macroinvertebrate assemblages, in terms of both numbers and}or biomass. Although the vast majority of studies have emphasized the herbivorous nature of Gammarus spp. and their ‘ shredder ’ functional feeding group (FFG) classification, we show that a far wider food base is exploited than has been previously acknowledged. This ‘ plasticity ’ as herbivore}predator is linked to the success of Gammarus spp. in persisting in and colonizing}invading disturbance-prone ecosystems. Intraguild predation and cannibalism are more common than previously realized. This behaviour appears to be a causal mechanism in many amphipod species replacements. Additionally, Gammarus spp. are major predators of other members of the macroinvertebrate community. Furthermore, while many studies have emphasized fish predation on Gammarus spp., we illustrate how this fish : amphipod, predator : prey interaction may be a two-way process, with Gammarus spp. themselves preying upon juvenile and wounded}trapped fish. We urge that a new realism be adopted towards the trophic ecology of Gammarus spp. and their role as predators and prey and that previously established FFG assumptions of both the food and the feeder be questioned critically. Key words : Fish, freshwater, functional feeding group, Gammarus spp., macroinvertebrate, predation, shredder, trophic.
I. II. III. IV. V. VI. VII.
CONTENTS Introduction . . . . . . . . The feeding ecology of Gammarus . . . . Cannibalism and intraguild predation . . . Gammarus as predators of other taxa . . . Conclusions . . . . . . . . Acknowledgements . . . . . . References . . . . . . . .
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I. INTRODUCTION
‘ Every species has its niche, its place in the grand scheme of things.’ (Paul Colinvaux, Why Big Fierce Animals Are Rare)
During the past two decades, a ‘ trophic ’ or ‘ functional ’ approach to studies of freshwater macroinvertebrate community structure has been increasingly emphasized, whereby taxa are assigned to a trophic or functional feeding group (FFG) based on their
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perceived dominant feeding mode. ‘ Scrapers ’ graze organic biofilms or ‘ aufwuchs ’ covering stones and plants, ‘ shredders ’ harvest allochthonous detritus and coarse particulate organic matter (CPOM, " mm), sediment}deposit-feeding ‘ collectorgatherers ’ utilize fine and very fine particulate organic matter (FPOM, µm– mm ; VPOM, ±– µm), ‘ filterers ’ feed on suspended organic matter, ‘ herbivore shredders and piercers ’ feed on living macrophytes and, finally, ‘ predators ’ kill and eat members of other feeding groups (Cummins, , ; Cummins & Klug, ; Merritt & Cummins, ). FFGs represent attempts to ‘ make the diversity of nature tractable to ecological analysis ’ (Duffy & Hay, ) and this trophic approach has been widely adopted by freshwater ecologists, allowing as it does some insight into energy flow and material cycling within ecosystems (Vannote et al., ). However, despite the fact that individual freshwater Gammarus species have been well studied as regards energy budgets (Mathews, ; Nilsson, ) and herbivorous diets (e.g. Barlo$ cher & Kendrick, a, b ; Moore, ; Willoughby & Sutcliffe, ; Marchant & Hynes, ; Chamier, Sutcliffe & Lishman, ), many investigations of the functional organization of benthic faunal assemblages have not advanced beyond a rigid reliance on a simple FFG designation of Gammarus spp. as shredders. This review examines this assumption critically in the light of accumulated ecological and behavioural evidence. We consider the role of Gammarus spp. as herbivores and carnivores, as well as predators and prey, operating in a diverse array of habitats. We attempt to form a rounded, coherent synthesis of the trophic ecology of this supposed ‘ shredder ’ to assess ‘ its [true] place in the grand scheme of things ’ (Colinvaux, ). The crustacean sub-order Gammaridea comprises over species, that is, approximately % of the order Amphipoda (Bousfield, ). In contrast to the three other amphipod sub-orders (the Hyperiidea, Ingolfiellidea and Caprellidea), which are highly specialized and ecologically restricted, the Gammaridea are widespread throughout a range of marine, freshwater and terrestrial habitats (Bousfield, ; Lincoln, ; Lincoln & Boxshall, ). The amphipod genus with the highest number of epigean freshwater species is Gammarus, which comprises over freshwater species distributed widely throughout the northern hemisphere (Karaman & Pinkster, ). In freshwater ecosystems, abiotic factors such as temperature, salinity, oxygen, acidity and pollution influence the distribution of Gammarus species (Jeffries & Mills, ; Whitehurst & Lindsey, ). Gammarus spp. are often found in great abundance in or under any substratum that provides both shelter from predators and a supply of organic detritus and other foodstuffs, that is, under rocks, in gravel or coarse substrates and amongst living and dead vegetation (Fitter & Manuel, ). In many riverine communities, amphipod species such as Gammarus pulex (Linnaeus) can represent the dominant macroinvertebrate in terms of biomass, as in the Millstone Burn, Scotland, where Shaw () and C. MacNeil (personal observation) found that G. pulex represented over % and %, respectively, of the total macroinvertebrate biomass. II. THE FEEDING ECOLOGY OF GAMMARUS
In gammarids (¯ gammaridean amphipods), the third thoracic appendages, the gnathopods, are highly versatile limbs used for feeding, grooming, burrowing, agonistic encounters between males (Borowsky, ) and grasping females during amplexus} precopulatory pairing. In the laboratory, Gammarus tigrinus Sexton has been observed
Trophic ecology of Gammarus spp.
to use the gnathopods to carry strips of fish and to hold these strips up to the mandibles while feeding (C. MacNeil, personal observations). The mandibles are located lateral to the mouth and, in conjunction with the upper and lower lips, surround the mouth opening. The typical mandible consists of a strong chitinized incisor, a small accessory plate (the lacinia mobilis), a large medial molar and, in addition, a spine row between the molar and the lacinia. In the genus Gammarus, the molar is tough and ridged for crushing and grinding (Lincoln, ). Thus, the feeding apparatus of Gammarus spp. is clearly capable of coping with a wide variety of foodstuffs. Evidence for a herbivorous lifestyle in freshwater Gammarus spp. comes from a variety of sources. Gammarus pulex is reported to sustain itself on decaying allochthonous leaf litter and its encumbent microbial community (Embody, ; Mottram, ; Hargrave, ; Barlo$ cher and Kendrick, a, b ; Cummins et al., ; Moore, ; Marchant & Hynes, ; Barlo$ cher, ; Chamier et al., ). Morphological studies of G. pulex gut structure indicate that plant material is digested in the foregut and fungi are digested in the hindgut (Agrawal, ), using enzymes identified as cellulases (Monk, ; Chamier & Willoughby, ; Chamier, ). In addition, the frequently observed congregations of G. pulex in leaf packs}accumulations of autumn shed leaves (Gee, ) and the apparent subjection of G. pulex populations to food limitation upon dissipation of the initial autumnal pulse of leaf litter (Gee, ), have been cited as evidence of a primarily herbivorous existence. Cummins (, ) and Cummins & Klug () adopted an FFG (functional feeding group) approach to the perceived dominant feeding modes of freshwater macroinvertebrates, which encompasses assessment of morpho-behavioural adaptations, feeding methods, food particle size and food quality (see also Vannote et al., ). This approach designates amphipods as shredders or facultative shreddercollectors (Cummins & Klug, ). In this FFG role, Gammarus spp. are regarded as major riverine processors or shredders of large amounts of coarse particulate organic matter such as leaf litter (Willoughby & Sutcliffe, ; Jenio, ; Herbst, ; Rosset, Barlo$ cher & Oertli, ; Griffith, Perry & Perry, ). Gammarus pulex and Gammarus pseudolimnaeus Bousfield reportedly processed up to % and % respectively of total litter input into low order (i.e. headstreams and tributaries) British and Canadian river systems (Mathews, ; Marchant & Hynes, ). Not all leaves, however, are used easily as a food source. Cameron & LaPoint () found that tannins in Chinese tallow (Sapium sebiferum : Euphorbiaceae) leaves greatly inhibited feeding in Crangonyx shoemakeri (Hubricht & Mackin), which is a member of the Crangonyctidae family closely related to the Gammaridae. Furthermore, C. MacNeil (personal observation) found that Gammarus pulex had a very low shredding capacity (only ±¬−%³¬−& grams of leaf per large G. pulex per day ; mean³s.e., N ¯ ) for oak Quercus robur (Linnaeus) litter that has both high lignin and tannin levels. Indeed, there is a ‘ processing continuum ’ or a hierarchy of leaf palatability for gammarids, in which leaves with high lignin and tannin levels, such as oak and beech, rank lower than softer, low tannin-level elm and maple leaves (Kaushik & Hynes, ; Petesen & Cummins, ; Malicky, ). In addition, Barlo$ cher & Kendrick ( a, b) found that fungi influenced leaf palatability and were crucial modifiers of leaf material for G. pulex (Graca, Maltby & Calow, , ). In feeding tests, the youngest stream-conditioned leaves with the highest viable fungal and
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bacterial densities invariably were preferred to older, more sterile specimens (Kostalos & Seymour, ; Barlo$ cher, ; Sridhar & Barlo$ cher, ). The FFG shredder designation, however, is problematic, with the dilemma of whether it is the food or the feeder being categorized, resulting in macroinvertebrates such as amphipods being ‘ reluctantly forced ’ into FFGs (King et al., ). As well as amphipods, difficulties have been experienced in assigning realistic FFGs to Plecoptera, Ephemeroptera and Trichoptera, with considerations of changing life-history strategies, the physical mechanisms of feeding and differing proportions of resources available all ‘ blurring ’ final FFG assignments (Wallace, Woodall & Sherberger, ; Short, Canton & Ward, ; Hawkins, Murphy & Anderson, ; Bunn, Edward & Loneragan, ; Chessman, ; King et al., ; C. MacNeil, personal observations). For example, the physical feeding action on leaf material is highly age}body-size dependent (Feminella & Stewart, ). This is evident in Baetidae mayflies, commonly regarded as ‘ typical ’ collector-gatherers}scrapers (Cummins, ; Cummins & Klug, ) and also in Leuctridae stoneflies, which, like Gammarus spp., are also regarded as ‘ typical ’ shredders, with species such as Leuctra hippopus (Kempny) feeding as shredders when adult but as collector-gatherers when juvenile (Hildrew, Townsend & Henderson, ; Dobson & Hildrew, ; A. G. Hildrew, personal communication). Mouthpart specialization does not always mean obligate resource utilization (Minshall, ; Mihuc & Minshall, ) and, in reality, the mouthparts of such ephemeropteran and plecopteran families can cater for a wide range of food categories, ranging from CPOM such as leaf litter to aufwuchs and FPOM (Hawkins et al., ; Chessman, ). The actual feeding methods reflect such ambiguities in that many Plecoptera do not ‘ shred ’ leaves but rather scrape away soft epidermal tissue (Wallace et al., ; Short et al., ). CPOM may ultimately be degraded by these methods, such that these macroinvertebrates are still termed shredders or rather ‘ micro-shredders ’ or ‘ skeletonizers ’ (King et al., ). However, by such criteria, many ephemeropteran scrapers can also legitimately be termed shredders as they utilize CPOM in similar ways (Anderson & Sedell, ). Cummins () also recognized that the study of aquatic macroinvertebrate feeding ‘ has been characterized by preoccupation with mature representatives ’. To compensate for such difficulties, some studies (Hildrew et al., ; Dobson & Hildrew, ) have arbitrarily divided Leuctra spp. and Gammarus pulex samples into ‘ large ’ (i.e. shredders) and ‘ small ’ (i.e. collectors) individuals when considering FFG designations. Such divisions may hamper legitimate distinctions being drawn between riverine assemblages of shredders and other groups based on the FFG concept. Friberg & Jacobsen () argue that the ‘ feeding plasticity of detritivore-shredders is much greater than traditionally supposed ’, in that Gammarus spp. can eat fresh aquatic plant material as well as leaf litter. Marine trophic research (Duffy & Hay, ) also finds that designation of amphipods into FFGs based on feeding apparatus is too restrictive, when in reality there exist ‘ diverse feeding habits among herbivorous amphipods ’ (Duffy & Hay, ). Such herbivorous plasticity has been reflected in the apparent resource partitioning observed by Zimmerman, Gibson & Harrington (), who found four Florida lagoon gammarids, Gammarus mucronatus Say, Cymadusa compta (Smith), Melita nitida Smith and Grandidierella bonnieroides Stephenson, capable of using macro- and microphagous feeding modes to consume marine plant material
Trophic ecology of Gammarus spp.
ranging in size from large seagrass fragments to fine particle detritus. Many other studies have cited Gammarus spp. as capable of feeding on algae (Barlo$ cher & Kendrick, b, ; Nilsson, ; Moore, ; Van Dolah, ; Anderson & Sedell, ; Willoughby, ; Moss, ; Aliyev, ; Steele & Whittick, ). Even in the FFG mode, algae and aufwuchs may both be just as legitimately ‘ shreddable ’ as leaf litter (Hawkins et al., ; Barlo$ cher & Murdoch, ). Hynes () reports Gammarus lacustris Sars even destroying gill-nets and the bottoms of wooden fishing boats. Indeed, apart from cellulases, Gammarus spp. contain large amounts of amylases capable of digesting substantial quantities of a wide variety of detritus (Barlo$ cher & Howatt, ; Borowsky & Guarna, ). It has been hypothesized that released digestive amylases may play a role external to the amphipod, either in the predigestion of food or as an aid in locating food (Guarna & Borowsky, ). In addition, as Allan & Malmqvist () found using traps baited with cheese, Gammarus spp. are not just attracted by plant material. Friberg & Jacobsen () suggest three reasons for Gammarus spp. feeding plasticity. First, being highly mobile, individuals can move from unattractive to attractive food easily. Second, they speculate that G. pulex mouthparts are not adapted to handling some hard food items (citing Willer, ). Third, Gammarus spp. possess high respiration rates (Nilsson, ) such that, energetically speaking, individuals cannot afford to eat either difficult-to-handle material or food with low calorific value. A number of authors have recently questioned the supposed herbivorous diets of gammarids. Schwartz () complains that research on amphipod nutrition ‘ continues to be conducted with the assumption that amphipods feed only on decaying allochthonous material and fungi growing on such material ’. Gee () cited the apparent linkage between Gammarus pulex population dynamics and litter input} dissipation as good evidence of Gammarus herbivory. However, this cause-and-effect interpretation may be spurious if, for example, this reduction in allochthonous material is associated with reductions in populations of other macroinvertebrate species upon which Gammarus spp. prey (Dick, ). Indeed, one of the very few studies on Gammarus spp. gut contents found a high prevalence of animal material in both Gammarus duebeni Liljeborg and G. pulex from a variety of habitats in the Isle of Man (Hynes, ). Minshall () noted that the indigenous population of Gammarus minus Say of Morgan’s Creek, Kentucky, USA ‘ probably eats anything that is available ’ and, in reality, distinctions between FFGs remain arbitrary because the majority of macroinvertebrates are ‘ opportunistic generalists ’ or ‘ selective omnivores ’, feeding in direct proportion to the amount and quality of food available locally (Slack, ; Jones, ; Barnes, ; Gee, ). Within the order Amphipoda, herbivory is merely one of a diverse array of feeding modes ranging from ectoparasitism (Stock, ), filter-feeding (Holsinger & Langley, ; Blinn & Johnson, ), carnivory (Kozhov, ) and even coprophagy (Minckley, ). Keith () found that skeleton shrimps (Caprellidae) had a diverse diet ranging from diatoms and carrion to live prey. These traits may also be found in Gammarus spp. Many authors cite Gammarus species as carrion feeders (Embody, ; Hynes, ; Kinne, ; Kozhov, ; Willoughby & Sutcliffe, ; Brown & Diamond, ) and Schwartz () argues that other freshwater gammarids such as Crangonyx shoemakeri are ‘ at least facultatively predacious ’. LeRoux () used
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chopped earthworm to rear laboratory populations of gammarids, Oseid & Smith () used dead fish as well as leaves to rear Gammarus pseudolimnaeus and Vassallo & Steele () found that flesh supplements to an algal diet accelerated growth and maturation in Gammarus lawrencianus Bousfield. Delong, Summer & Thorp () found that Gammarus fasciatus Say supplemented its leaf diet with dead chironomids. These latter authors argued that a diverse potential food base benefits riverine populations by allowing exploitation of seasonal changes in abundance of specific foods. In disturbance-prone ecosystems such as rivers, with their inherent ‘ feast and famine ’ resource conditions, invertebrates invariably switch between foods as they become available (Koslucher & Minshall, ; Kostalos & Seymour, ; Short, ). Ultimately, the ability to assimilate a ‘ diverse suite ’ of foods must contribute to the ability of the gammarids to persist in and colonize new and variable habitats (Schwartz, ). Indeed, Conlan () provides numerous examples of how amphipods are themselves major creators of environmental disturbance by their exploitation of a variety of disparate food resources, arguing that large-scale destruction}alteration of food}physical resources by amphipods can affect the whole aquatic community. III. CANNIBALISM AND INTRAGUILD PREDATION
Hunte & Myers () note that cannibalism (i.e. the capturing, killing and devouring of an animal by a conspecific) has been reported in over animal species but ‘ has been viewed as an aberrant and occasional phenomenon ’ in orders such as the Amphipoda. Culver & Fong (), in their study of cave-dwelling amphipods, warn that ‘ a diversity of interactions may be lurking in apparently monotonous detritivore communities ’ and gammaridean cannibalism has been reported in many laboratory studies (Sexton, , ; Clemens, ; Jones, ; Schmitz, ; Kostalos & Seymour, ; Jenio, ; Dick, ). Indeed, Jenio () noted with surprise that when cannibalism commenced in Gammarus minus pinicollis Cole ‘ … elm leaves (their preferred culture food source) were ignored ’. Meijering () found male predation on females in mixed species precopula pairs of Gammarus pulex and Gammarus fossarum Koch. Minshall () found cannibalism in Gammarus minus in Morgan’s Creek, Kentucky, USA and Jenio (, ) observed that G. minus pinicollis was both the most voracious of three sympatric Gammarus species in Elm Spring, Illinois, USA and the most abundant by over a factor of two compared to Gammarus pseudolimnaeus and Gammarus troglophilus Hubricht and Mackin. Both cannibalism and interspecific predation on injured, diseased and dead Elm Spring Gammarus spp. were observed, with Jenio () concluding that cannibalism ‘ might turn out to be widespread with freshwater gammarids as more data become available ’. Cannibalism of juveniles by adults is common in amphipods (e.g. Steele & Steele, ; Dennert, ; Kostalos & Seymour, ; Pinkster, Smit & Brandse-De Jong, ; Skadsheim, ; Dick, Montgomery & Elwood, ; Dick, ). Hunte & Myers () even suggest that ‘ cannibalism may be an important agent of selection in the evolution of life histories ’, showing that changes in the phototactic behaviour of juveniles of three estuarine gammarid species, Gammarus lawrencianus, Gammarus tigrinus and Gammarus mucronatus coincided with juveniles becoming less vulnerable to cannibalism by adults (Hunte & Myers, ). Within crustacean populations, the largest individuals are often the most dominant,
Trophic ecology of Gammarus spp.
aggressive and superior competitors (Bovbjerg, ; Lee & Fielder, ). Ward (), for example, found that large male Gammarus duebeni gain advantage over smaller males in aggressive interactions during the breeding season. This advantage in size often predisposes the cannibalism of smaller by larger individuals (e.g. Dick, ). Such cannibalism may, in turn, predispose individuals of one species towards the killing and eating of individuals of other species, particularly congenerics and}or members of the same ecological guild (see Polis, Myers & Holt, and below). Goedmakers & Roux (), for example, examining mixed species pairs of Gammarus fossarum Koch, Gammarus wautieri Roux and Gammarus gauthieri Karaman, found that females of some larger species consumed males of smaller species. The devouring of the gammarid Crangonyx pseudogracilis Bousfield (juvenile and adult forms) by the much larger Gammarus pulex, Gammarus duebeni celticus Stock and Pinkster and Gammarus tigrinus has also been identified and investigated (Dick, ). In addition, the vulnerability of individual Gammarus spp. at moult may allow predation on equally sized or even larger species, for example, predation by G. tigrinus on the larger G. pulex and G. duebeni celticus (Dick, ; Dick & Platvoet, ). Coupled with this, any one species may be inherently more aggressive than another, leading to smaller individuals killing heterotrospecifics (Dick, Elwood & Montgomery, ). Predation such as that described above has been termed ‘ intraguild predation ’ or ‘ IGP ’ (Polis et al., ), defined as predation occurring between potentially competing species that exploit the same class of environmental resources, regardless of different foraging strategies, and thus belonging to the same ecological ‘ guild ’ (Root, ; Colinvaux, ; Lincoln & Boxshall, ; Dick, ). Such IGP, together with cannibalism and interspecific competition, has been quantified and compared, producing evidence that this behaviour has wide-ranging community consequences, particularly in respect to species exclusions and replacements (Dick, Elwood & Irvine, a ; Dick, Irvine & Elwood, b ; Dick, ; Dick et al., ). Crustaceans face increased risks of predation during and shortly after the vulnerable moulting period, since moulted individuals are very soft, relatively inactive and thus easily victimized (Embody, ; Willoughby & Sutcliffe, ; Jenio, , ; Ward, ; Dick et al., ; Dick, ). In addition, water conductivities, with their ionic influence on the physiology of crustacean moult, influence the predatory interactions between Gammarus species (Dick & Platvoet, ). The expulsion of the indigenous Gammarus duebeni celticus from its niche by the apparently ‘ competitively superior ’ Gammarus pulex has been well documented (Pinkster et al., ; Dennert, ; Strange & Glass, ). Dick () and Dick et al. (), investigating the interactions underpinning this replacement, found that newly moulted females of both species are preyed upon heavily by congeneric males, but that significantly more G. d. celticus females are devoured by G. pulex males than in the reciprocal interaction. Coupled with this, ‘ clumping ’ feeding frenzies on congenerics can result in higher frequencies of congeneric predation on G. d. celticus females than on G. pulex females. The superior ability of G. pulex both to resist predation and to prey on moulted G. d. celticus results in an asymmetry of impact on populations of the two species. This perhaps constitutes the ‘ driving force ’ behind the ousting of G. d. celticus from many of its Irish and other European rivers by incursions of G. pulex (Dick, , ; Dick et al., ). Also in Ireland, the apparent segregation of G. tigrinus to the centre
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of Lough Neagh, with G. d. celticus greatly dominant in near-shore areas, could be the result of similar interactions occurring within changing habitat templets (i.e. changing physiochemical regimes that may moderate competitive}predatory interactions). Dick et al. () put forward a model incorporating cannibalism, mutual predation and resource competition. This model indicates that, although cannibalism in the absence of predation may actually promote co-existence, cannibalism coinciding with predation of equal or greater magnitude results in rapid species eliminations and replacement. This may be a widespread phenomenon in amphipods and other taxa. Clearly, these reports of voracious cannibalism and intraguild predation do not fit well with the FFG image of Gammarus spp. as a somewhat passive shredder}detritivorous omnivore. Indeed, this FFG image is still stifling acceptance of research in the area of Gammarus spp. predation, because the fallacy of Gammarus spp. as almost totally reliant on allochthonous detritus and vegetation continues to be perpetuated in the literature. IV. GAMMARUS AS PREDATORS OF OTHER TAXA
Gammarids are also predators of other invertebrate groups (Clemens, ; Forsman, ; Hynes, ; Borovitskaya, ; Martin, ; Fries & Tesch, ; Lubyanov & Zubchenko, ; Anderson & Raasveldt, ; Bengtsson, ). In particular, Gammarus spp. predation on members of the Isopoda is well reported (e.g. Fries & Tesch, ; Minshall, ; Williams & Moore, ). Oseid & Smith () found exposure of Asellus communis to Gammarus pseudolimnaeus results in ‘ virtual elimination of the former by the latter ’. Exudates of Asellus aquaticus (Linnaeus) trigger aggregative ‘ clumping ’ feeding-frenzy behaviour in Gammarus pulex, even without the physical presence of the isopod (Bengtsson, ). The isopod normally actively avoids G. pulex via chemotaxic mechanisms. Similar predation on an isopod has been noted in the cave-dwelling Gammarus minus (Culver & Fong, ). There is considerable niche overlap between G. pulex and A. aquaticus (Graca et al., ) but Williams & Moore () showed that the isopod is more important to the gammarid as prey than as a serious competitor. However, Oseid & Smith () found that increasing cyanide pollution gradually shifts the competitive advantage from the aggressive G. pseudolimnaeus to the more passive A. communis, until, in extremely polluted areas, G. pseudolimnaeus is unable to compete with, let alone prey upon, the more resistant A. communis. This pollution-mediated amphipod : isopod predatory}competitive interaction has been exploited by Whitehurst () and Whitehurst & Lindsey (), who found that the Gammarus : Asellus ratio is highly sensitive to organic pollution levels and could be employed as a monitoring tool of water quality. The predatory repertoire of Gammarus spp. is often large, including chironomids (Jones, ; Minshall, ; Delong et al., ; C. MacNeil, personal observations), baetine mayflies and trichopterans (Minshall, ), plecopterans (Hynes, ), annelids (Dick, ) and cladocerans (Hutchinson, ). Kortelainen () found that Gammarus lacustris reduced the numbers of a cladoceran Sida sp. and a copepod Eudiaptomus sp. in a subarctic pond. Schwartz () found that Crangonyx shoemakeri consumed mosquito larvae and a constant quantity of Daphnia obtusa Kurz, even over a -fold range of detritus availability, emphasizing the consistent predation pressure amphipods exert in ponds and pools. These predatory amphipods, which are particularly common in shallow woodland pools lacking vertebrate predators, therefore
Trophic ecology of Gammarus spp.
have the potential to regulate the density of their prey. A similar potential for Gammarus spp. to regulate prey populations has been found by Anderson & Raasveldt () in certain North American lakes, where densities of zooplankton populations corresponded closely to variations in abundance of Gammarus lacustris lacustris Sars. Habitats lacking vertebrate predators may have amphipods as part of the plankton instead of their usual benthic habit (Hutchinson, ; Blinn & Johnson, ). Therefore, it is possible that macroinvertebrate prey experience a relatively constant predation pressure regardless of fluctuations in fish predation, because predatory gammarids exert a ‘ buffering ’ effect on prey community dynamics. Indeed, Roberts (), observing the predatory behaviour of Gammarus duebeni under laboratory conditions, found that they killed – mosquito larvae h−", ‘ often killing larvae when not hungry ’. He argues that predatory crustaceans could be successfully harnessed as effective biocontrols of salt-marsh mosquito larvae in preference to the use of toxic chemicals, and advocates enhancing their breeding and even release to control mosquito pests. As well as being noted scavengers of dead vertebrates, principally fish (Kozhov, ), amphipods may also be active predators of vertebrates in marine and freshwaters. Although the importance of gammarids as fish food has long been stressed (Mottram, ; Hynes, ; Degani et al., ; Ade, ; Andersen et al., ; Friberg et al., ), fish : amphipod predatory interactions are not exclusively one-way. Williamson (), for example, reports the hyperiid Themisto (¯ Parathemisto) gracilipes Norman eating part of the body wall of a live mm post-larval fish and Logachev & Mordinov () found gammarids feeding on round goby larvae Neogobius melanostomus. Similarly, Fries & Tesch () report Gammarus tigrinus attacking guppies, Lebistes reticulatus and tadpoles, although both vertebrates were too large and active to be either seriously wounded or devoured. Pinkster et al. () and Vader & Ramppainen () report Gammarus spp. attacking fish trapped in nets. G. tigrinus has been observed attacking netted fish in Lough Neagh, N. Ireland (H. B. N. Hynes, personal communication ; J. T. A. Dick & C. MacNeil, personal observations). In contrast to the difficulties that active prey present, fish eggs represent a rich static food source to amphipods. Brown & Diamond (), for example, found Gammarus pulex eating rainbow trout Salmo gairdneri Richardson eggs in the field. These wide-ranging reports of Gammarus spp. and other amphipods as active predators of other macroinvertebrate and indeed vertebrate groups contradict with assigned FFGs, which designate them trophic roles as herbivorous shredders or, at best, generalist omnivores. The full role of gammarids in influencing community structure will only be clarified when the fallacy of applying a single rigid FFG designation is revised in the light of such reports. V. CONCLUSIONS
() This review illustrates how Gammarus spp., typically viewed as archetypal shredders, utilize a much greater range of food resources than just allochthonous leaf material and its encumbent microbial community. These resources may be highly transitory in disturbance-prone aquatic ecosystems such as rivers, where stochastic and deterministic forces may be interacting constantly along very different spatial and temporal scales (Stanford & Ward, ; Hildrew & Townsend, ).
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() Although Gammarus spp. are widely acknowledged as important fish food (e.g. Mottram, ; Degani et al., ; Ade, ; Andersen et al., ), we have shown that such vertebrate : gammarid predatory interactions are not exclusively one-way. Cannibalism, intra- and interguild predation are also at work and these can lead to species replacements and thus large-scale community change. () Future work should not be ‘ strait-jacketed ’ into accepting only one established functional role for Gammarus spp. and, indeed, other macroinvertebrate genera in the community or assemblage being studied. Concepts such as the FFG are admittedly superficially attractive because ‘ stereotyping a species by classifying its feeding behaviour fits comfortably with a natural desire to name or label organisms ’ (Gerking, ). However, this invariably presents the dilemma of whether it is the assumed food or the feeder being assigned, with the result that some studies have reluctantly ‘ forced ’ taxa into FFGs (e.g. King et al., ). Thus, in many cases, ‘ functional feeding groups ’ may actually be ‘ fictional feeding groups ’ ! A compromise in accounting for all of these often contradictory considerations is the use of joint-assignments of FFGs to certain ‘ problem ’ taxa such as Gammarus ; however, this serves only to blunt the sensitivity in detecting any differences in functional or trophic organization of assemblages between habitats, which defeats the principal purpose of the FFG concept (King et al., ). Friberg & Jacobsen () argue that the FFG concept should not be applied ‘ too rigorously ’ and indeed, Mihuc & Minshall () note ‘ the prevalence of generalist trophic function among benthic macroinvertebrates ’ and that FFGs should not be used as ‘ trophic guilds ’. Consequently, they conclude that the concept ‘ should be used with caution to infer systems-level trophic dynamics in streams (e.g. system autotrophy or heterotrophy derived from scraper or shredder abundance or biomass) ’. Such strong reservations call into question the whole purpose of the FFG concept. Perhaps unsurprisingly, workers studying the feeding of other animals, such as fish, are reaching similar conclusions. Gerking () argues that ‘ what the fish should be eating should be cast aside and in its place researchers must accept gracefully what they are eating ’ and therefore ‘ the notion of broad trophic adaptability should be adopted ’. Trophic classifications such as the FFG concept, when applied to potentially omnivorous macroinvertebrates such as gammarids, should thus be treated with great caution, otherwise they mislead and oversimplify our understanding of riverine ecosystem processes. Indeed, unless precautions are taken, much otherwise valid and worthwhile freshwater research may be marred. Strict adherence to FFG designations, regardless of changing habitat templets, may establish erroneous linkages between macroinvertebrate assemblage composition and implied food resources. Therefore, we argue that designations of FFGs to potentially omnivorous groups such as amphipods must reflect both the versatility and transitory nature of dominant feeding modes. Thus, Gammarus spp. may be mainly shredders in one habitat in one season, collectorgatherers in the same habitat in a different season, mainly predators in a third ecosystem and probably generalist-detritivores under many more habitat templets. () To accompany trophic studies we recommend widespread adoption of gut dissection of Gammarus and other taxa at the locality being studied and at the time in question (e.g. Jones, ; Hynes, ; Barmuta, ; Dittrich, ; Dobson & Hildrew, ). If this is coupled with laboratory observations of macroinvertebrate feeding behaviour on possible food sources collected from the same locality, this may
Trophic ecology of Gammarus spp.
ascertain what is actually eaten and by what method by the amphipod or macroinvertebrate in question, and not what is assumed it should be eating. Only then, and regardless of established FFG designations, can one make a realistic attempt at assessing a species’ true dominant feeding mode and ‘ its place in the grand scheme of things ’ (Colinvaux, ). VI. ACKNOWLEDGEMENTS This study was undertaken during a Department of Education for Northern Ireland (D.E.N.I.) Research Studentship awarded to C. MacNeil. J. T. A. Dick acknowledges support under the Natural Environment Research Council (N.E.R.C.) Fellowship scheme. Thanks to the anonymous referee whose comments greatly improved this manuscript. Many thanks are due to Mike Jeffries, Chris Gibbons, David Turnbull, Sandy Milner, Jimmy Nail, Scott Mathieson, Peter Beardsley, Sam Felinus, Terry Clough and Alan Hildrew who have all, knowingly or unknowingly, shaped my (C. MacNeil) ideas on freshwater ecology over recent years. Thanks also to Andy Bridge, Johnny ‘ P ’ Prenter, Gillian Bell, Sarah Faloon and Ian Montgomery for creating an encouragingly nonchalant laboratory atmosphere in which to work. VII. REFERENCES A, R. (). The Trout and Salmon Handbook. A Guide to the Wild Fish. Blackwell, Oxford. A, V. P. (). Feeding appendages and the digestive system of Gammarus pulex. Acta Zoologica , –. A, R. I. (). Ecology and biology of Gammarus matienus (Crustacea, Amphipoda) in the waters of Azerbaijan. Hydrobiologia (), –. A, J. D. & M, B. (). Diel activity of Gammarus pulex (Crustacea) in a south Swedish stream : comparison of drift catches vs baited traps. Hydrobiologia (), –. A, T. H., F, N., H, H. O., I, T. M., J, D. & K, L. (). The effects of introduction of brown trout (Salmo trutta L.) on Gammarus pulex L. drift density in two fishless Danish streams. Archiv fuX r Hydrobiologie (), –. A, N. H. & S, J. R. (). Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology , –. A, R. S. & R, L. G. (). Gammarus and Chaborus predation. Canadian Wildlife Service Occasional Papers , –. B$ , F. (). The contribution of fungal enzymes to digestion of leaves by Gammarus fossarum Koch (Amphipoda). Oecologia , –. B$ , F. (). Factors that delay colonization of fresh alder leaves by aquatic hyphomycetes. Archiv fuX r Hydrobiologie (), –. B$ , F. & H, S. L. (). Digestion of carbohydrates and protein by Gammarus mucronatus Say (Amphipoda). Journal of Experimental Marine Biology and Ecology (–), –. B$ , F. & K, B. ( a). Fungi in the diet of Gammarus pseudolimnaeus. Oikos , –. B$ , F. & K, B. ( b). Fungi and food preferences of Gammarus pseudolimnaeus. Archiv fuX r Hydrobiologie , –. B$ , F. & K, B. (). Leaf conditioning by micro-organisms. Oecologia , –. B$ , F. & M, J. R. (). Hyporheic biofilms – a potential food source for interstitial animals. Hydrobiologia (–), –. B, L. A. (). Habitat patchiness and macrobenthic community structure in an upland stream in temperature Victoria, Australia. Freshwater Biology , –. B, R. D. (). Invertebrate Zoology. Holt – Saunders Japan Ltd., U.S.A. B, G. (). Energetic costs of amino acid exudation in the interaction between the predator Gammarus pulex L. and the prey Asellus aquaticus L. Journal of Chemical Ecology , –. B, D. W. & J, D. B. (). Filter feeding of Hyalella montezuma, an unusual behaviour for a freshwater amphipod. Freshwater Invertebrate Biology , –. B, M. P. (). Biology of G. pulex in water-bodies of the Leningrad district and its importance in fish-farming. TrudyX Leningradskogo obshchestva estestvoispyX tateleıW , –. (Freshwater Biological Association Translations (N.S.) No. ). B, B. (). The use of the males’ gnathopods during precopulation in some gammaridean amphipods. Crustaceana (), –. B, R. & G, M. M. (). Excess amylase in Gammarus palustris (Crustacea : Amphipoda) ; its release into and possible roles in environment. Marine Biology (), –.
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