Effects of environment and an introduced invertebrate species on the structure of benthic macroinvertebrate species at the catchment level

Biotic interactions such as predation and competition can influence aquatic communities at small spatial scales, but they are expected to be overridden by environmental factors at large scales. The continuing threat to freshwater biodiversity of biological invasions indicates that biotic factors do, however, have important structuring roles. In Irish rivers, the native amphipod Gammarus duebeni celticus has become locally extinct, ostensibly through differential predation by the more aggressive and introduced G. pulex. This mechanism explains impacts of G. pulex at within-river spatial scales on native macroinvertebrate community diversity, including declines in ephemeropterans, plecopterans, dipterans and oligochaetes. To determine if these patterns are predictable at larger spatial scales, we assessed patterns in native macroinvertebrate communities across river sites of the Erne catchment in 1998 and 1999, in conjunction with the distribution of G. pulex and G. d. celticus. In both years, G. pulex dominated invaded sites, whereas G. d. celticus occurred at low abundance in uninvaded sites. In both years, invaded sites had lower diversity and fewer pollution sensitive invertebrate species than un-invaded sites. Community ordination in 1998 showed that invaded sites had higher conductivity, smaller substrate particle size and comprised a lower proportion of pollution sensitive taxa including Ephemeroptera and Plecoptera. In contrast, in 1999, conductivity was the only variable explaining site ordination along axis 1, but was unable to separate sites with respect to invasion status. A second explanatory axis separated sites with respect to invasion status, with invaded sites having fewer taxa, including lower abundance of ephemeropterans, dipterans and plecopterans. Laboratory experiments examined the potential role of differential predation between the two Gammarus species in explaining these taxon specific patterns in the field. Survival of the ephemeropterans, Ephemerella ignita and Ecdyonurus venosus and the isopod, Asellus aquaticus, was lower when interacting with G. pulex than with G. d. celticus. This study indicates that G. putex may alter invertebrate community structure at scales beyond those detected within individual rivers. However, effects may be influenced by gradients in physico-chemistry, which may be temporal or depend on catchment characteristics. Invasions by amphipods have increased globally, thus comprehensive assessments of their impacts and of other aquatic invaders, may only be apparent when studies are conducted at a range of spatio-temporal scales.

Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus

The microsporidian parasite, Pleistophora mulleri, infects the abdominal muscle of the freshwater amphipod Gammarus duebeni celticus. We recently showed that P. mulleri infection was associated with G. d. celticus hosts being more vulnerable to predation by the invasive amphipod Gammarus pulex. Parasitized G. d. celticus also had a reduced ability to prey upon other co-occurring amphipods. We suggested the parasite may have pervasive influences on host ecology and behaviour. Here, we examine the association between P. mulleri parasitism and parameters influencing individual host fitness, behaviour and interspecific interactions. We also investigate the relationship between parasite prevalence and host population structure in the field. In our G. d. celticus study population, P. mulleri prevalence was strongly seasonal, ranging from 8.5% in summer to 44.9% in winter. The relative abundance of hosts with the heaviest parasite burden increased during summer, which coincided with high host mortality, suggesting that parasitism may regulate host abundance to some degree. Females were more likely to be parasitized than males and parasitized males were paired with smaller females than unparasitized males. Parasitism was associated with reduction in the host's activity level and reduced both its predation on the isopod Asellus aquaticus and aggression towards precopula pairs of the invasive G. pulex. We discuss the pervasive influence of this parasite on the ecology of its host.

Factors influencing the distribution of native and introduced Gammarus spp. in Irish river systems

Populations of Gammarus duebeni celticus, previously the only amphipod species resident in the rivers of the Lough Neagh catchment, N. Ireland, have been subjected to invasion by G. pulex from the British mainland. Numerous previous studies have investigated the potential behavioural mechanisms, principally differential mutual predation, underlying the replacement of G. d. celticus by G. pulex in Irish waters, and the mutually exclusive distributions of these species in Britain and mainland Europe. However, the relative degree of influence of abiotic versus biotic factors in structuring these amphipod communities remains unresolved. This study used principal component analysis (PCA) to distinguish physico-chemical parameters that have significant roles in determining the current distribution of G. pulex relative to G. d. celticus in L. Neagh rivers. We show that the original domination of rivers by the native G. d, celticus has changed radically, with many sites in several rivers containing either both species or only G. pulex. G. pulex was more abundant than the G. d. celticus in sites with low dissolved oxygen levels. This was reflected in the macroinvertebrate assemblages associated with G. pulex in these sites, which tended to be those tolerant of low biological water quality. The present study thus emphasizes the importance of the habitat template, particularly water quality, for Gammarus spp. interactions. If rivers become increasingly stressed by organic pollution, it is probable the range expansion of G. pulex will continue. Because these two species are not ecological equivalents, the outcomes of G. pulex incursions into G. d. celticus sites may ultimately depend on the prevailing physico-chemical regimes in each site.

Comparison of the functional responses of invasive and native amphipods

While we can usually understand the impacts of invasive species on recipient communities, invasion biology lacks methodologies that are potentially more predictive. Such tools should ideally be straightforward and widely applicable. Here, we explore an approach that compares the functional responses (FRs) of invader and native amphipod crustaceans. Dikerogammarus villosus is a Ponto-Caspian amphipod currently invading Europe and poised to invade North America. Compared with other amphipods that it actively replaces in fresh-waters, D. villosus exhibited significantly greater predation, consuming significantly more prey with a higher type II FR. This corroborates the known dramatic field impacts of D. villosus on invaded communities. In another species, FRs were nearly identical in invasive and native ranges. We thus propose that if FRs of other taxa and trophic groups follow such general patterns, this methodology has potential in predicting future invasive species impacts.

The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators, or both?

Gammarus spp. are traditionally viewed under the functional feeding group (FFG) concept as herbivorous 'shredders'. Although recent studies suggest that Gammarus should also be viewed as predators, this latter role remains contentious. Here, in a laboratory experiment, we objectively examine the balance between shredder and predator roles in a common freshwater species. Gammarus pulex preyed significantly on mayfly nymph, Baetis rhodani, in both the presence and absence of excess leaf material. There was no significant difference in predation where the alternative food, that is, leaf material, was present as compared to absent. Also, G. pulex shredded leaf material in the presence and absence of B. rhodani. However, shredding was significantly reduced where alternative food, that is, B. rhodani prey, was present as compared to absent. Further, G. pulex had a clear leaf species preference. Our results suggest that Gammarus function as both predators and shredders, with the balance of the two roles perhaps depending on food availability and quality. We discuss implications for the use of the FFG concept in assessing freshwater processes, and the role that Gammarus predation may play in structuring macroinvertebrate communities.

Variation in shell morphology of Calliostoma zizyphinum (Gastropoda : Trochidae)

Differences in shell morphology in the intertidal prosobranch mollusc Calliostoma zizyphinum were studied from a number of sites within four geographical reo ions of the British Isles with varying exposures to wave action and crab predation. Mean values of damage scarring were highest in shells sampled from Strangford Lough, Northern Ireland, and lowe;t in individuals from the Atlantic Coast. Shells collected front the Isle of Man were smaller than those from either the Atlantic coast of Ireland or Strangford Lough. Shells front Strangford Lough had taller shells (higher aspect ratio) than shells from the County Down and Atlantic Coast and shells from the County Down coast were more squat (lower aspect ratio) than those from all other areas. Shells from Strangford Lough were significantly thinner than shells from all other geographical areas. The relationships between shell damage scarring and shell size and tallness were not consistent among areas. Shells from Strangford Lough are notable in showing a steep, positive relationship between shell size and scarring and a steep, negative relationship between scarring and tallness. The unusual shell phenotypes observed in shells from Strangford 1,Lough may be explained by rapid shell growth, which would not only allow Calliostoma to attain a size refuge from crab predators but also to recover successfully from repeated crab attacks on the shell lip. Such a strategy would result in larger, thinner shells with a high number of damage scars.

Invader-invader interactions in relation to environmental heterogeneity leads to zonation of two invasive amphipods, Dikerogammarus villosus (Sowinsky) and Gammarus tigrinus Sexton: amphipod pilot species project (AMPIS) report 6

As biological invasions continue, interactions occur not only between invaders and natives, but increasingly new invaders come into contact with previous invaders. Whilst this can lead to species replacements, co-existence may occur, but we lack knowledge of processes driving such patterns. Since environmental heterogeneity can determine species richness and co-existence, the present study examines habitat use and its mediation of the predatory interaction between invasive aquatic amphipods, the Ponto-Caspian Dikerogammarus villosus and the N. American Gammarus tigrinus. In the Dutch Lake IJsselmeer, we found broad segregation of D. villosus and G. tigrinus by habitat type, the former predominating in the boulder zone and the latter in the soft sediment. However, the two species co-exist in the boulder zone, both on the short and longer terms. We used an experimental simulation of habitat heterogeneity and show that both species utilize crevices, different sized holes in a plastic grid, non-randomly. These amphipods appear to optimise the use of holes with respect to their 'C-shape' body size. When placed together, D. villosus adults preyed on G. tigrinus adults and juveniles, while G. tigrinus adults preyed on D. villosus juveniles. Juveniles were also predators and both species were cannibalistic. However, the impact on G. tigrinus of the superior intraguild predator, D. villosus, was significantly reduced where experimental grids were present as compared to absent. This mitigation of intraguild predation between the two species in complex habitats may explain the co-existence of these two invasive species.

FLEXIBLE OMNIVORY IN DIKEROGAMMARUS VILLOSUS (SOWINSKY, 1894) (AMPHIPODA) - AMPHIPOD PILOT SPECIES PROJECT (AMPIS) REPORT 5

Feeding in Dikerogammarus villosus (Sowinsky, 1894) males was observed in the field and recorded on video in the laboratory. The following feeding modes were recognized: detritus feeding, grazing, particle feeding, coprophagy, predation on benthic and free swimming invertebrates, predation on fish eggs and larvae, as well as feeding on byssus threads of the zebra mussel, Dreissena polymorpha (Pallas, 1771). The feeding methods are described and illustrated with screenshots of video recordings. The very flexible feeding modes of D. villosus, which make diet switches possible, form a trait that must be an important factor in the invasion success of this Ponto-Caspian gammaridean species, and may thus explain for a great deal its high ecosystem impact.

Role of behaviour in biological invasions and species distributions; lessons from interactions between the invasive Gammarus pulex and the native G-duebeni (Crustacea : Amphipoda)

In attempting to understand the distributions of both introduced species and the native species on which they impact, there is a growing trend to integrate studies of behaviour with more traditional life history/ecological approaches. The question of what mechanisms drive the displacement of the freshwater amphipod Gammarus duebeni by the often introduced G pulex is presented as a case study Patterns of displacement are well documented throughout Europe, but the speed and direction of displacement between these species can be varied. From early studies proposing interspecific competition as causal in these patterns, I review research progress to date. I show there has been no evidence for interspecific competition operating, other than the field patterns themselves, a somewhat tautological argument. Rather, the increased recognition of behavioural attributes with respect to the cannibalistic and predatory nature of these species gave rise to a series of studies unravelling the processes driving field patterns. Both species engage in 'intraguild predation' (IGP), with moulting females particularly vulnerable to predation by congeneric males. G pulex is more able both to engage in and avoid this interaction with G duebeni. However, several factors mediate the strength and asymmetry of this IGP, some biotic (e.g. parasitism) and others abiotic (e.g. water chemistry). Further, a number of alternative hypotheses that may account for the displacement (hybridization; parasite transmission) have been tested and rejected. While interspecific competition has been modelled mathematically and found to be a weak interaction relative to IGP, mechanisms of competition between these Gammarus species remain largely untested empirically. Since IGP may be finely balanced in some circumstances, I conclude that the challenge to detect interspecific competition remains and we require assessment of its role, if any, in the interaction between these species. Appreciation of behavioural attributes and their mediation should allow us to more fully understand, and perhaps predict, species introductions and resultant distributions.

Potential roles for differential body size and microhabitat complexity in mediating biotic interactions within invasive freshwater amphipod assemblages

Cannibalism and intraguild predation (IGP) are common amongst freshwater amphipod crustacean aswsemblages, particularly between individuals of different body size, with IGP of smaller by larger species. The decline of Gammarus tigrinus Populations in mainland Europe has been accompanied by the arrival of the Ponto-Caspian invader Dikerogammarus villosus and previous studies have implicated IGP of G. tigrinus by the larger D. villosus as the principal driving force in this replacement. We examined how factors such as microhabitat and body size may mediate both cannibalism within G. tigrinus populations and IGP by D. villosus and thus contribute to field patterns of coexistence and exclusion. A field Survey of an invaded Dutch fake indicated that G. tigrinus and D. villosus differed in distribution. with D. villosus being the numerically dominant amphipod (80-96 %) on the rocky boulder Substrate of the shoreline and G. tigrinus being the dominant amphipod (100 %) in the crushed shell/sand matrix immediately adjacent to this. Laboratory microcosm experiments indicated that G. tigrinus cannibalism, particularly of smaller by larger size classes, may be common. In addition, although D. villosus predation of all G. tigrinus size classes was extreme, the smallest size classes Suffered the highest predation. Indeed, when exposed to D. villosus, predation of larger G. tigrinus was lowest when smaller G. tigrinus were also present. Increasing microhabitat complexity from a simple bare substrate littered with Dreissena polymorpha zebra mussels to a Crushed shell/sand matrix significantly reduced both cannibalism and IGP. Our Study emphasizes the need to consider both life history stages and habitat template, when considering the impacts of biotic interactions and it also emphasizes that complex, interacting factors may be mediating the range expansion of D. villosus.

Differential drift and parasitism in invading and native Gammarus spp. (Crustacea : Amphipoda)

Invading and native species often interact directly, such as by predation, producing patterns of exclusion and coexistence. Less direct factors, such as interactions with the broader abiotic and biotic environment, may also contribute to such patterns, but these have received less recognition. In Northern Ireland, the North American Gammarus tigrinus has invaded freshwaters populated with the native Gammarus duebeni celticus, with intraguild predation between the two implicated in their relative success. However, these species also engage in day and night

Differential physico-chemical tolerances of amphipod species revealed by field transplantations

Physico-chemical regimes of river systems are major determinants of the distributions and relative abundances of macroinvertebrate taxa. Other factors, however, such as biotic interactions, may co-vary with changes in physico-chemistry and concomitant changes in community composition. Thus, direct cause and effect relationships may not always be established from field surveys. Equally, however, laboratory studies may suffer from lack of realism in extrapolation to the field. Here, we use balanced field transplantation experiments to elucidate the role of physico-chemical regime in determining the generally mutually exclusive distributions of two amphipod taxa, Gammarus (two species) and Crangonyx pseudogracilis. Within two river systems in Ireland, the former species dominate stretches of well oxygenated, high-quality water, whereas the latter dominates stretches of poorly oxygenated, low-quality water. G. pulex and G. duebeni celticus did not survive in bioassay tubes in areas dominated by C. pseudogracilis, which itself survived in tubes in such areas. However, both C. pseudogracilis and Gammarus spp. survived equally well in tubes in areas dominated by Gammarus spp. Physicochemical regime thus limits the movement of Gammarus spp. into C. pseudogracilis areas, but some other factor excludes C. pseudogracilis from Gammarus spp. areas. Since previous laboratory experiments showed high predation rates of Gammarus spp. on C. pseudogracilis, we propose that predation by the former causes exclusion of the latter. Hence, presumed effects of physico-chemical regime on macroinvertebrate presence/abundance may often require experimental field testing and appreciation of alternative explanations.

Invading predatory crustacean Dikerogammarus villosus eliminates bath native and exotic species

As the tempo of biological invasions increases, explanations and predictions of their impacts become more crucial. Particularly with regard to biodiversity, we require elucidation of interspecific behavioural interactions among invaders and natives. In freshwaters in The Netherlands, we show that the invasive Ponto-Caspian crustacean amphipod Dikerogammarus villosus is rapidly eliminating Gammarus duebeni, a native European amphipod, and Gammarus tigrinus, until now a spectacularly successful invader from North America. In the laboratory, survival of single (unguarded) female G. duebeni was significantly lower when male D. villosus were free to roam as compared with isolated within microcosms. In addition, survival of paired (guarded) female G. duebeni was significantly lower when male D. villosus as compared with male G. duebeni were present. D. villosus killed and consumed both recently moulted and, unusually, intermoult victims. Survival of G. tigrinus was significantly lower when D. villosus were free to roam as compared with isolated within microcosms and, again, both moulted and intermoult victims were preyed upon. Male D. villosus were significantly more predatory than were females, while female G. tigrinus were significantly more often preyed upon than were males. Predation by D. villosus on both species occurred over a range of water conductivities, an environmental feature previously shown to promote amphipod coexistence. This predatory invader is predicted to reduce further the amphipod diversity in a range of freshwater habitats in Europe and North America.

Predator-prey interactions between brown trout Salmo trutta and native and introduced amphipods; their implications for fish diets

An attempt to improve the food base for brown trout Salmo trutta in Northern Ireland was made in 1958.59 by deliberately introducing English Gammarus pulex into several Irish rivers. In addition. another amphipod Crangonyx pseudogracilis, was later accidently introduced into II ish waters. Our study represents the first attempt to examine the trophic interactions between a native fish predator (S. trutta) and an array of these native (Gammarus duebeni celticus) and introduced (G. pulex and C. pseudogracilis) amphipods. Feeding experiments, involving young brown trout predators and ampiphod prey, revealed that the fish actively selected C. pseudogracilis relative to two alternative Gammarus prey species. Although the trout encountered the Gammarus species more than C. pseudogracilis, they were eaten less than Crangonyx. Difficulties in handling and ingestion of Gammarus by trout may be a. key component of the preference fbr the smaller, more easily handled Crangonyx. The microdistribution of the species was altered by the fish, due to predation being greater in particular microhabitats, Our study showed that the introduction of the herbivorous C. pseudogracilis into Irish freshwaters may represent a useful addition to fish diets. particularly for small and/or juvenile fish. The reprecussions of the deliberate introduction of G. pulex are less clear. It may improve feeding for fish. but only if it can coexist with indigenous macroinvertebrates and thus ultimately improve the range and quantity of possible food items in predator diets. Alternatively, being highly predatory towards other macroinvertebrates including G. d. celticus and C. pseudogracilis. G. pulex may be deleterious to the diversity of the resident benthic community and hence reduce the diversity of prey available to fish predators.

Foraging ecology, fluctuating food availability and energetics of wintering brent geese

Changing energy requirements and dramatic shifts in food availability are major factors driving behaviour and distribution of herbivores. We investigate this in wintering East Canadian High Arctic light-bellied brent geese Branta bernicla hrota in Northern Ireland. They followed a sequential pattern of habitat use, feeding on intertidal Zostera spp. in autumn and early winter before moving to predominantly saltmarsh and farmland in late winter and early spring. Night-time feeding occurred throughout and made a considerable contribution to the birds' daily energy budget, at times accounting for > 50% of energy intake. Nocturnal feeding, however, is limited to the intertidal, possibly because of predation risk on terrestrial habitat, and increases with moonlight. The amount of Zostera spp., declined dramatically after the arrival of birds, predominantly, but not entirely, due to consumption by the birds. Birds gained fat reserves in the first 2 months but then this was dramatically lost as their major food source collapsed and their daily energy intake declined. Single birds consistently fared worse than paired birds and pairs with juveniles fared better than those without suggesting a benefit of having a family to compete for food. Many birds leave the Lough at this time of reduced Zostera spp. for other sea inlets in Ireland but some remain. Body condition of the latter gradually improved in early spring and reflected a heavy reliance on terrestrial habitats, particularly farmland, to meet the birds' daily energy requirements. However, even in the period immediately before migration to the breeding ground, the birds did not regain the amount of abdominal fatness observed in November. The dramatic changes in available food and requirements of the birds drive the major changes seen in foraging behaviour as the birds evade starvation in the wintering period.