Calum MacNeil

Widespread vertical transmission and associated host sex ratio distortion within the eukaryotic phylum Microspora

Vertical transmission (VT) and associated manipulation of host reproduction are widely reported among prokaryotic endosymbionts. Here, we present evidence for widespread use of VT and associated sex–ratio distortion in a eukaryotic phylum. The Microspora are an unusual and diverse group of eukaryotic parasites that infect all animal phyla. Following our initial description of a microsporidian that feminizes its crustacean host, we survey the diversity and distribution of VT within the Microspora. We find that vertically transmitted microsporidia are ubiquitous in the amphipod hosts sampled and that they are also diverse, with 11 species of microsporidia detected within 16 host species. We found that infections were more common in females than males, suggesting that host sex–ratio distortion occurs in five out of eight parasite species tested. Phylogenetic reconstruction demonstrates that VT occurs in all major lineages of the phylum Microspora and that sex–ratio distorters are found on multiple branches of the phylogenetic tree. We propose that VT is either an ancestral trait or evolves with peculiar frequency in this phylum. If the association observed here between VT and host sex–ratio distortion holds true across other host taxa, these eukaryotic parasites may join the bacterial endosymbionts in their importance as sex–ratio distorters.

The dynamics of predation on gammarus spp. (Crustacea: Amphipoda)

Gammarus spp. (Crustacea: Amphipoda) are widespread throughout a diverse range of marine, freshwater and estuarine/brackish habitats, often dominating benthic macroinvertebrate communities in terms of both numbers and/or biomass. Gammarus spp. are the dominant macroinvertebrate prey items of many fish, whether as a seasonal food source or a year‐round staple. Selective predation by fish on Gammarus spp. is often linked to parasitism and the body size of the prey. Gammarus spp. populations are under increasing threat from both pollution and replacement/displacement by introduced species. Loss of populations and species invasions/replacements could have significant impacts on native predator species if the predator(s) cannot successfully adapt their feeding patterns to cope with non‐indigenous Gammarus prey species. Despite this, many fish predation studies do not identify Gammarus prey to species level. This lack of precision could be important, as Gammarus spp. exhibit wide variations in physiochemical tolerances, habitat requirements, abilities to invade and susceptibility to replacement. Although rarely acknowledged, the impacts of nonpiscean predators (particularly macroinvertebrates) on Gammarus prey species may frequently be stronger than those exerted by fish. A major aim of this review is to ascertain the current importance of Gammarus as a prey species, such that the implications of changes in Gammarus spp. populations can be more accurately assessed by interested groups such as ecologists and fisheries managers. We also review the dynamics of Gammarus spp. as prey to a diverse array of mammals, birds, amphibians, insects, flatworms, other crustaceans such as crabs and crayfish and, perhaps most importantly, other Gammarus spp.

Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0–90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single–species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed–species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.

Sexual cannibalism and mate choice

Sexual cannibalism, where a female kills and consumes a courting male, represents an extreme form of sexual conflict and has been proposed as a mechanism of mate choice. We evaluate the evidence for mate choice through premating sexual cannibalism via mate rejection, other indirect mechanisms of mate ‘choice’ and choice in postmating sexual cannibalism. We highlight a paucity of investigations, particularly of field studies, and note gaps in our knowledge. There is empirical support for the size-dependent sexual cannibalism predicted by mate choice through premating sexual cannibalism. This may represent mate choice operating on absolute male size but it could be a by-product of female foraging behaviour and greater vulnerability of relatively smaller males. Thus, indirect mate choice is as plausible an explanation of size-dependent sexual cannibalism as is direct mate choice based on discrimination of male traits. Direct female choice, mediated through premating sexual cannibalism, has yet to be demonstrated. We suggest a framework for distinguishing direct and indirect choice and note an absence of information on which to test it. There is evidence for sequential mate choice in postmating sexual cannibalism, but the nature or basis of the females discriminatory behaviour remains unclear. Costs and long-term fitness benefits of the putative mate choice have been largely ignored. Reversed sexual cannibalism, in which the male eats the female, presumably occurs when the gain from food is high and potential gain from mating low and probably has little to do with mate choice.

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.

The validity of the Gammarus:Asellus ratio as an index of organic pollution: abiotic and biotic influences.

In freshwaters. Gammarus spp. are more sensitive to organic pollution than Asellus spp. and the relative abundance of the two taxa has been proposed as a pollution index. We tested the validity of this by examining the relationship between the Gammarus: Asellus (G : A) ratio and (1) a suite of physico-chemical variables. (2) established biotic (average score per taxon, ASPT) and richness (species richness (S) and Ephemeroptera, Plecoptera and Trichoptera families richness (EPT family richness)) indices generated from the macroinvertebrate community. In addition, we investigated a suspected biotic interaction, predation, between Gammarus and Asellus. Both univariate and multivariate analyses showed that the G: A ratio was sometimes responsive to changes in parameters linked to organic pollution, such as BOD5 and nitrate levels. However, the G : A ratio also appeared responsive to variables not directly linked to organic pollution, such as conductivity and distance from source. There were significant positive correlations among the G : A ratio and the ASPT, S and EPT, indicating that changes in the relative abundances of Gammarus and Asellus were reflected in changes in the pollution sensitivity and richness of the wider macroinvertebrate community. A laboratory experiment revealed significant predation of Asellus aquaticus juveniles by Gammarus duebeni celticus adults, but no reciprocal predation. We propose that the G: A ratio may be useful as a crude measure of organic pollution that could supplement more complex indices in a multimetric approach to pollution monitoring or be used for monitoring individual sites, where a simple technique is required for monitoring purposes over a period of time. Also, we urge recognition of the possible role of biotic interactions among taxa used in the generation of pollution indices.

Direct and indirect effects of species displacements; an invading freshwater amphipod can disrupt leaf litter processing and shredder efficiency

Abstract Invasive species may threaten the fundamental role played by native macroinvertebrate shredders in determining energy flow and the trophic dynamics of freshwater ecosystems. Functionally, amphipods have long been regarded as mainly shredders, but they are increasingly recognized as major predators of other macroinvertebrate taxa. Furthermore, intraguild predation (IGP) between native and invasive amphipods underlies many species displacements. We used laboratory mesocosms to investigate what might happen to shredders and leaf-litter processing in water bodies invaded by the highly predatory Ponto-Caspian amphipod Dikerogammarus villosus, which is spreading rapidly throughout Europe and may soon invade the North American Great Lakes. The leaf-shredding efficiency of D. villosus was significantly lower than that of 3 Gammarus species (2 native and 1 invasive) that D. villosus has either already displaced or may be currently displacing in The Netherlands. In addition, D. villosus was a major predator of all of these native and invasive amphipod shredders and of a common isopod shredder Asellus aquaticus. Leaf processing in Gammarus and Asellus mesocosms declined rapidly in the presence of D. villosus and ceased altogether within 4 d because by then, all potential shredders had been killed and consumed. Furthermore, the shredding efficiency of surviving amphipods and isopods declined significantly within 2 d of the release of D. villosus, a result indicating that predator-avoidance behavior may override leaf processing. We discuss the implications of these direct and indirect effects of D. villosus invasions and species displacements on community structure and litter processing in aquatic ecosystems.

The Replacement of a native freshwater amphipod by an invader : roles for environmental degradation and intraguild predation

We assessed the extent to which an invader, Gammarus pulex (Crustacea: Amphipoda), has replaced a native, Gammarus duebeni celticus, over a 13-year period in a European river system and some of the abiotic and biotic factors that could account for this. Between 1988 and 2001, 56% of mixed-species sites had become invader-only sites, whereas no mixed sites had become native only again. The native dominated areas of higher dissolved oxygen and water quality, with the reciprocal true for the invader. Field transplant experiments revealed that native survivorship was lower in areas where it had been replaced than in areas where the invader does not yet occur. In invader-only areas, native survivorship was lower than that of the invader when kept separately and lowest when both species were kept together. We also observed predation of the native by the invader. Laboratory oxygen manipulation experiments revealed that at 30% saturation, the natives survivorship was two thirds that of the invader. We conclude t...

Effects of the acanthocephalan parasite Echinorhynchus truttae on the feeding ecology of Gammarus pulex (Crustacea: Amphipoda)

The amphipod Gammarus pulex is an intermediate host to the acanthocephalan fish parasite Echinorhynchus truttae . Gammarus pulex has a wide trophic repertoire, feeding as a herbivore, detritivore and predator. In this study an examination was made of the effects of E. truttae parasitism on components of the G. pulex diet: stream-conditioned leaves, dead chironomids and live juvenile isopods Asellus aquaticus . Over 21 days, parasitism had no effect on daily feeding rates or wet weights of G. pulex fed on leaves or chironomids. Parasitism had a significant effect on the number of A. aquaticus killed by G. pulex , with parasitized individuals killing significantly fewer than their unparasitized counterparts. In addition, unparasitized amphipods killed all size classes of A. aquaticus indiscriminately, whereas parasitized animals tended to kill the smaller size classes. The impacts of the parasitism of G. pulex throughout the wider freshwater community are discussed.

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

Abstract 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. Physico-chemical 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.