Culturing freshwater pearl mussel Margaritifera margaritifera: a breakthrough in the conservation of an endangered species.

1. The freshwater pearl mussel Margaritifera margaritifera L. is globally endangered and is threatened by commercial exploitation, pollution and habitat loss throughout its range. Captive breeding would be a valuable tool in enhancing the status of M. margaritifera in the UK. 2. We have developed a semi-natural system for successfully infecting juvenile brown trout with glochidial M. margaritifera, and culturing juvenile mussels in experimental tanks where glochidial M. margaritifera can excyst from fish gills and settle into sediment. 3. Infected fish had less than 1% mortality. Levels of infection varied among fish. Two yearly cohorts of juvenile M. margaritifera were identified from samples of sediment taken from each experimental tank. Individuals range in size from 1.4 mm (2000 cohort) to >3 mm in length (1999 cohort). 4. The number of juvenile M. margaritifera present in the two experimental tanks are estimated to be between 3600 (tank A) and 0 (tank B) for the putative 1999 cohort and between 6000 (tank A) and 13 000 (tank B) for the putative 2000 cohort. 5. This pioneering method for large-scale cultivation of juvenile M. margaritifera is intermediate between the release of infected fish into rivers and the intensive cultivation systems developed in continental Europe and the USA for other species of unionid. This is the first time that large numbers of M. margaritifera have been cultured and represents a significant breakthrough in the conservation of this globally endangered Red Data List species. The method is straightforward and is most cost-effective when undertaken alongside established hatchery processes.

Diel variation in egg-laying by the freshwater fish louse Argulus foliaceus (Crustacea : Branchiura)

Removal of deposited eggs could be a useful control strategy for the damaging fish ectoparasite Argulus foliaceus, but focused control requires knowledge of egg-laying patterns. Here, we investigated diel changes in the egg-laying behaviour of a natural population of A. foliaceus. Data were collected from 17-28 May 2004. Days were divided into 3 time periods: 06:00-14:00, 14:00-22:00 and 22:00-06:00 h. Significantly more egg clutches were laid from 06:00-14:00 h than during the other 2 time periods, which were not significantly different from each other. Significantly more egg clutches per hour were laid during hours of daylight as compared to hours of darkness. Significantly more egg clutches were laid in the top 1 m of the water column than at the bottom, and this was consistent throughout all 3 time periods. It is suggested that the increase in egg-laying activity during daylight hours may be due to a higher motivation to search for hosts during the night and an increased ability to locate silhouetted egg-laying sites during the day. These data can provide information useful for egg removal and control strategies.

Invasion by the amphipod Gammarus pulex alters community composition of native freshwater macroinvertebrates

Assessing the effects of invading species on native community structure is often confounded by environmental factors and weakened by lack of replicated, long-term pre- and post-invasion monitoring. Here, we uncouple the community effects of a freshwater amphipod invader from environmental differences. In Irish rivers, the introduced Gammarus pulex replaces the native Gammarus duebeni celticus. However, the River Lissan in Northern Ireland is dissected by a weir that has slowed the upstream invasion by G. pulex. This allowed us in 2000 to sample three contiguous 150-m reaches that were (1) G. pulex dominated; (2) mixed Gammarus spp.; and (3) G. duebeni celticus only. In 2003, we resampled these reaches and one additional of mixed Gammarus species and one with only G. duebeni celticus further upstream. In temperature, conductivity, and pH, there were statistically significant but no biologically relevant differences among the five reaches of 2003, and between the three reaches surveyed in both years. Although there was evidence of recovery in macroinvertebrate diversity and richness in invaded reaches between years, continued upstream invasion was associated with sustained reductions in these community metrics as compared to un-invaded sites. Community ordination indicated (1) different associations of community composition attributed to the distribution, abundance, and biomass of the invader; and (2) increasing similarity of invaded communities over time. The impact mechanisms of G. pulex on macroinvertebrate community composition may include predation and competition. The consequences of the observed community changes for ecosystem functioning require further investigation.

Seasonal and vertical patterns of egg-laying by the freshwater fish louse Argulus foliaceus (Crustacea : Branchiura)

Argulus foliaceus is a damaging fish ectoparasite for which new control measures are being developed based on egg-removal, In an attempt to develop further understanding of seasonal and vertical egg-laying patterns in this parasite, egg-laying activity was monitored over the period 14 April to 17 November 2003 in 2 rainbow trout Oncorhynchus mykiss fisheries in Northern Ireland, UK. At Site 1, egg-laying was continuous from 21 April to 17 November, when water temperature was above 8 to 10 degrees C. At Site 2, egg-laying was continuous from 4 June to 29 October. In the early months of the season, egg-laying was recorded mainly within the top 1 m of the water column; however, a significant shift to deep water egg-laying was recorded between 7 July and 17 November at Site 1 and between 20 August and 29 October at Site 2. Egg clutches were preferentially laid at depths of up to 8.5 m during this time (Site 2), a feature of egg-laying hitherto unappreciated. Temperature and dissolved oxygen did not differ significantly among depths, but there was an increase in water clarity over time. However, the precise environmental triggers for deep water egg-laying are still unclear. These new insights into the reproductive behaviour of this species will be useful in developing control methods based on egg-removal.

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.

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.

Environmental mediation of intraguild predation between the freshwater invader Gammarus pulex and the native G. duebeni celticus

Invasive species and environmental change often occur simultaneously across a habitat and therefore our understanding of their relative roles in the decline of native species is often poor. Here, the environmental mediation of a critical interspecific interaction, intraguild predation (IGP), was examined between invasive (Gammarus pulex) and native (G. d. celticus) freshwater amphipods. In the laboratory, IGP asymmetries (males preying on congeneric females) were examined in river water sourced from zones where: (1) the invader has completely displaced the native; (2) the two species currently co-exist, and (3) the native currently persists uninvaded. The invader was always a more effective IG predator, but this asymmetry was significantly weaker moving from 'invader-only water' through 'co-existence water' to 'native-only water'. The constituent of the water that drives this mediation of IGP was not identified. However, balancing the rigour of laboratory experiments with field derived 'environment' has advanced understanding of known patterns in a native species decline, and its co-existence and persistence in the face of an invader.

A long-term study (1949-2005) of experimental introductions to an island; freshwater amphipods (Crustacea) in the Isle of Man (British Isles)

Using data from field introduction experiments with Gammarus spp. conducted in the rivers of a small island, commencing in 1949, with resampling in the 60s, 70s, 80s, 90s and finally in 2005, we aimed to examine the long-term interaction of the native freshwater amphipod Gammarus duebeni celticus with the introduced G. pulex. Using physico-chemical data from a 2005 island-wide survey, we also aimed to find what environmental factors could influence the distribution of the two species.

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.

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

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. © 2011 The North American Benthological Society.


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The pitfall with PIT tags: Marking freshwater bivalves for translocation induces short-term behavioural costs

Tagging animals is frequently employed in ecological studies to monitor individual behaviour, for example postrelease survival and dispersal of captive-bred animals used in conservation programmes. While the majority of studies focus on the efficacy of tags in facilitating the relocation and identification of individuals, few assess the direct effects of tagging in biasing animal behaviour. We used an experimental approach with a control to differentiate the effects of handling and tagging captive-bred juvenile freshwater pearl mussels, Margaritifera margaritifera, prior to release into the wild. Marking individuals with passive integrated transponder (PIT) tags significantly decreased their burrowing rate and, therefore, increased the time taken to burrow into the substrate. This effect was contributed to, in part, by the detrimental impacts of handling, which also significantly affected activity, burrowing ability and the time taken for each individual to emerge and start probing the substrate. Disturbance during handling and tagging may lead to indirect mortality after release by increasing the risk of predation or dislodgement during flooding, thereby potentially compromising any conservation strategy contingent on population supplementation or reintroduction. This is the first study to demonstrate that handling and PIT tagging has a detrimental impact on invertebrate behaviour. Moreover, our results provide useful information that will inform freshwater bivalve conservation strategies.

Towards a strategy for the conservation of the freshwater pearl mussel Margaritifera margaritifera in County Donegal, Ireland

This study attempts to identify the habitat requirements of the pearl mussel Margaritifea margaritifera in County Donegal, in north west Ireland, an area with little urban, industrial or intensive agricultural development. No mussels occur in rivers where calcium and conductivity levels are high or where the substratum is predominantly bedrock or fine sediment but it was not possible to distinguish clearly between mussel and non-mussel sites on the basis of ordination analysis. However, rivers which still support mussels and rivers with historical records of mussels are loosely grouped. Rivers which formerly supported mussels but lack living M. margaritifera appear to have suitable habitat for mussels; pearl fishing is the most likely reason for the extinction of these mussel populations. Where population densities are high, for example in locations on the rivers Eske, Clady and Owenea, conservation may necessitate the establishment of reserves. The prospect for the successful reintroduction of mussels into former mussel rivers such as the Finn and Eany Water, where suitable habitat exists and water quality is high, is very good.

Does the freshwater pearl mussel, Margaritifera margaritifera L., face extinction in Northern Ireland?

1. Until recently the status of Margaritifera margaritifera L. in Northern Ireland was not well documented. This paper presents the results of field surveys conducted in 1990/'91 and in 1996 at over 200 sites covering all major river systems in Northern Ireland. 2.Margaritifera populations in Northern Ireland were recorded at just 20 sites mainly located in the west of the province. Formerly many rivers supported vast numbers of mussels but anecdotal evidence points to periods of major declines in mussel populations since the turn of the century. 3. The absence of mussels smaller than 30 mm in length at most sites suggests very little or no recruitment during the past decade. During the surveys, deteriorating water quality, habitat disturbance and pearl fishing were recorded and are the major causes of the decline of the freshwater pearl mussel in Northern Ireland. 4. Unless the above problems are alleviated in the very near future, M.margaritifera will probably become extinct in Northern Ireland. © 1998 John Wiley & Sons, Ltd.