Nociception or pain in a decapod crustacean?

Nociception is the ability to perceive a noxious stimulus and react in a re flexive manner and occurs across a wide range of taxa. However, the ability to experience the associated aversive sensation and feeling, known as pain, is not widely accepted to occur in nonvertebrates. We examined the responses of a decapod crustacean, the prawn, Palaemon elegans, to different noxious stimuli applied to one antenna to assess reflex responses (nociception) and longer-term, specifically directed behavioural responses that might indicate pain. We also examined the effects of benzocaine, a local anaesthetic, on these responses. Noxious stimuli elicited an immediate reflex tail flick response, followed by two prolonged activities, grooming of the antenna and rubbing of the antenna against the side of the tank, with both activities directed specifically at the treated antenna. These responses were inhibited by benzocaine; however, benzocaine did not alter general swimming activity and thus the decline in grooming and rubbing is not due to general anaesthesia. Mechanical stimulation by pinching also resulted in prolonged rubbing, but this was not inhibited by benzocaine. These results indicate an awareness of the location of the noxious stimuli, and the prolonged complex responses indicate a central involvement in their organization. The inhibition by a local anaesthetic is similar to observations on vertebrates and is consistent with the idea that these crustaceans can experience pain.

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.

A spatio-temporal contrast of the predatory impact of an invasive freshwater crustacean

Aim: Impacts of invasive species may vary across invasion gradients, owing to trait-based sorting of individuals through dispersal: those aggregating at invasion fronts may be more aggressive and voracious. We examine, in the field and laboratory, variation in the predatory impacts of an invasive Ponto-Caspian crustacean Hemimysis anomala G.O. Sars, 1907 at two sites along a spatio-temporal gradient of invasion.

Location: Republic of Ireland.

Methods: We used reciprocal transplant field-deployed mesocosms to compare predation rates of invasion front and well-established H. anomala on natural zooplankton assemblages. In the laboratory, we measured the functional response (relationship between predation rate and prey supply) of H. anomala from both sites, for a per capita mechanistic comparison of predation efficiency. We also assessed prey selectivity of H. anomala in the mesocosm experiments to further compare feeding behaviour. Finally, we used a correlative approach to assess the community impact of H. anomala across sites, including a nearby uninvaded site, by comparing zooplankton diversities and densities.

Results: Invasion front H. anomala had higher predation rates than well-established H. anomala at high in situ zooplankton densities. Invasion front H. anomala also had higher functional responses - in particular showing higher 'attack rates' - indicating a heightened ability to locate and capture prey. Prey selectivity was consistent across the spatio-temporal contrast, with positive selection for cladocerans. Zooplankton diversity and density declined with time since H. anomala invasion, both being maximal at the uninvaded site.

Main conclusions: Our study, for the first time, (1) reveals differences in predatory per capita effects and associated behavioural traits between two sites along a spatio-temporal invasion gradient and (2) shows a negative community-level impact of the invasive H. anomala in natural water bodies. Further spatio-temporal comparisons of predatory per capita effects of invaders are needed to assess the generality of these results.

The less amorous Gammarus: predation risk affects mating decisions in Gammarus duebeni (Amphipoda)

We examined the trade-off between the behaviours associated with predator avoidance and mate acquisition in the mate-guarding amphipod crustacean Gammarus duebeni. We used laboratory experiments to investigate the impact of olfactory predator cues on activity, mate choice and mate-guarding behaviour of males and females. Pair formation declined under perceived risk of predation, reflecting reduced activity of both males and females and hence a reduced likelihood of encountering a mate. We also observed a reduction in the choosiness of both males and females. Under increased perceived predation risk, assessment of the female by the male was more likely to be followed by pair formation, and males showed a nonsignificant trend towards reduced discrimination in favour of large females and were less tenacious in their pair bond when they paired during exposure to predator cues. Females also showed less resistance behaviour, suggesting that both males and females trade off the costs of maximizing current reproductive success against the benefits of predator avoidance for survival and reproduction in the future. We discuss the implications of such context-dependent mating behaviours for ecological interactions between species and suggest that predators, via the effects of perceived predation risk on mate choice and mate guarding in the prey species, induce trait-mediated indirect effects with the potential to influence population dynamics and community structure. (C) 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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.

Predatory impact of the freshwater invader Dikerogammarus villosus (Crustacea : Amphipoda)

To assess the increasing threats to aquatic ecosystems from invasive species, we need to elucidate the mechanisms of impacts of current and predicted future invaders. Dikerogammarus villosus, a Ponto-Caspian amphipod crustacean, is invading throughout Europe and predicted to invade the North American Great Lakes. European field studies show that populations of macroinvertebrates decline after D. villosus invasion. The mechanism of such impacts has not been addressed empirically; however, D. villosus is known to prey upon and replace other amphipods. Therefore, in this study, we used microcosm and mesocosm laboratory experiments, with both single and mixed prey species scenarios, to assess any predatory impact of D. villosus on a range of macro invertebrate taxa, trophic groups, and body sizes. Dikerogammarus villosus predatory behaviour included shredding of prey and infliction of

High incidence of cryptic repeated elements in microsatellite flanking regions of galatheid genomes and its evolutionary implications

During the development of PCR primer sets for icrosatellite marker loci from enriched genomic libraries for three squat lobster species from Galatheidae (Decapoda: Anomura); Munida rugosa (Fabricius, 1775), M. sarsi (Huus, 1935), and Galathea strigosa (Linnaeus, 1761) (collectively known as squat lobsters), a number of unforeseen problems were encountered. These included PCR amplification failure, lack of amplification consistency, and the amplification of multiple fragments. Careful examination of microsatellite containing sequences revealed the existence of cryptic repeated elements on presumed unique flanking regions. BLAST analysis of these and other VNTR containing sequences (N 5 252) indicates that these cryptic elements can be grouped into families based upon sequence similarities. The unique features characterising these families suggest that different molecular mechanisms are involved. Of particular relevance is the association of microsatellites with mobile elements. This is the first reported observation of this phenomenon in crustaceans, and it also helps to explain why microsatellite primer development in galatheids has been relatively unsuccessful to date. We suggest a number of steps that can be used to identify similar problems in microsatellite marker development for other species, and also alternative approaches for both marker development and for the study of molecular evolution of species characterised by complex genome organisation. More specifically, we argue that new generation sequencing methodologies, which capitalise on parallel and multiplexed sequencing may pave the way forward for future crustacean research.

Marine reserve designation, trophic cascades and altered community dynamics

Marine ecosystems and their associated populations are increasingly at risk from the cumulative impacts of many anthropogenic threats that increase the likelihood of species extinction and altered community dynamics. In response, marine reserves can be used to protect exploited species and conserve biodiversity. The increased abundance of predatory species in marine reserves may cause indirect effects along chains of multi-trophic interactions. These trophic cascades can arise through direct predation, density-mediated indirect interactions (DMIIs), or indirect behavioural effects, termed trait-mediated indirect interactions (TMIIs). The extent of algal cover and the abundance of 4 primary consumers were determined in Lough Hyne, which was designated Europe's first marine nature reserve in 1981. The primary consumers were the sea urchin Paracentrotus lividus, the topshell Gibbula cineraria, the oyster Anomia ephippium, and the scallop Chlamys varia. The abundances of 3 starfish species (Marthasterias glacialis, Asterias rubens, and Asterina gibbosa) were also determined, as were 2 potential crustacean predators, Necora puber and Carcinus maenas. These data were compared with historical data from a 1962 (prey) and a 1963 (predator) survey to determine the nature of community interactions over adjacent trophic levels. The present study reveals a breakdown in population structure of the 4 surveyed prey species. Marine reserve designation has led to an increase in predatory crabs and M. glacialis, a subsequent decrease in primary consumers, especially the herbivore P. lividus, and an increase in macroalgal cover which is indicative of a trophic cascade. The study shows that establishing a Marine Reserve does not guarantee that conservation benefits will be distributed equally.

Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator

Emergent multiple predator effects (MPEs) might radically alter predictions of predatory impact that are based solely on the impact of individuals. In the context of biological invasions, determining if and how the individual-level impacts of invasive predators relates to their impacts in multiple-individual situations will inform understanding of how such impacts might propagate through recipient communities. Here, we use functional responses (the relationship between prey consumption rate and prey density) to compare the impacts of the invasive freshwater mysid crustacean Hemimysis anomala with a native counterpart Mysis salemaai when feeding on basal cladoceran prey (i) as individuals, (ii) in conspecific groups and (iii) in conspecific groups in the presence of a higher fish predator, Gasterosteus aculeatus. In the absence of the higher predator, the invader consumed significantly more basal prey than the native, and consumption was additive for both mysid species - that is, group consumption was predictable from individual-level consumption. Invaders and natives were themselves equally susceptible to predation when feeding with the higher fish predator, but an MPE occurred only between the natives and higher predator, where consumption of basal prey was significantly reduced. In contrast, consumption by the invaders and higher predator remained additive. The presence of a higher predator serves to exacerbate the existing difference in individual-level consumption between invasive and native mysids. We attribute the mechanism responsible for the MPE associated with the native to a trait-mediated indirect interaction, and further suggest that the relative indifference to predator threat on the part of the invader contributes to its success and impacts within invaded communities.

Effects of baited crab pots on cultivated mussel (Mytilus edulis) survival rates

The shore crab, Carcinus maenas, is recognized as a voracious predator of blue mussels, Mytilus edulis, having the potential to greatly reduce stocks in the benthic cultivation industry. As a consequence, baited crab pots are often deployed on and around cultivated benthic mussel beds to trap and remove crabs, in an attempt to reduce predatory pressure. Little is known about how C. maenas behaves around crab pots, but for many other crustacean fisheries, the trapping efficiency of pots is often low. Crabs may be attracted towards but not enter pots, instead feeding on cultivated mussels outside pots on the surrounding substratum. We tested whether the rate of loss of mussels attached to plates differed in areas next to baited pots compared with unbaited pots and to areas without any pots, at two sea loughs (60 km apart) in Northern Ireland. In Strangford Lough, more mussels were lost from plates next to baited pots than the other treatments. In Carlingford Lough, however, we found no difference in the number of mussels lost from plates in any treatment. This difference could be attributed to the different assemblages of mobile benthic predators at the two loughs. The presence of the starfish Asterias rubens, which was absent from experimental sites in Carlingford Lough, was thought to be responsible for increased predation rates near baited pots in Strangford. It is, therefore, important to consider local predator communities when deploying crab pots as a predator mitigation technique to ensure predation rates are in fact reduced and not enhanced. This study is of relevance not only to attempts to limit predation on commercial stocks of benthic cultivated mussels but also in situations where baited traps are deployed close to species vulnerable to mobile benthic predators.

Genetic assessment of parentage in the caridean rock shrimp Rhynchocinetes typus based on microsatellite markers

Over the past decade, the common rock shrimp, Rhynchocinetes typus H. Milne Edwards, 1837, has been the focus of extensive investigations on mating behaviour. The species is now perceived as a model system for the study of reproductive strategies and sexual conflict in crustaceans displaying external fertilization. Using molecular markers, the current study assesses whether social mating behaviour in common rock shrimp translates into true genetic parentage. In a large mesocosm tank with >200 individuals of both sexes, the analysis of 15 families (22 eggs per female) for three informative microsatellites unambiguously confirmed multiple paternity in 11 instances (73%) involving, in each case, two to four males. Where more than one male was identified siring a particular brood, reproductive skew was apparent towards a single individual. Results suggest that multiple paternity in this species results from subordinate male coercive behaviour, female solicitation of multiple male matings or a combination of both.

Interspecific comparison of estrogen and testosterone concentrations in three species of amphipods (Gammarus duebeni celticus, G. pseudolimnaeus, and G. pulex)

The presence and biological significance of vertebrate-related steroid sex hormones in aquatic invertebrates are poorly understood. We compared the concentrations of estrogen (17β-estradiol) and testosterone between amplexing male and female freshwater amphipods of three species from two continents: Gammarus duebeni celticusLiljeborg, 1852 and G. pulex(L., 1758) from Europe, and G. pseudolimnaeusBousfield, 1958 from North America. All three species were found to have measureable concentrations of both hormones in whole body lysate samples but the concentrations differed between species, with testosterone differing significantly between species only for male amphipods and estradiol differing significantly between species only for female amphipods. Concentrations of both testosterone and estrogen differed between males and females in two of the three species ( G. duebeni celticusand G. pseudolimnaeus). Females had the highest concentration of both hormones in G. duebeni celticusand the lowest concentration of both hormones in G. pseudolimnaeus. These results contribute to a growing body of evidence that these hormones are endogenously produced and biologically relevant in amphipods. Such evidence is particularly important in light of increasing prevalence of endocrine-disrupting compounds in the environment and the central role played by amphipods in aquatic ecosystems.

Trait-Mediated Effects of Parasites on Invader-Native Interactions.

Parasites have a variety of behavioural effects on their hosts, which can in turn affect species with which the host interacts. Here we review how these trait-mediated indirect effects of parasites can alter the outcomes of invader-native interactions, illustrating with examples from the literature and with particular regard to the invader-native crustacean systems studied in our laboratories. Parasites may potentially inhibit or exacerbate invasions via their effects on host behaviour, in addition to their direct virulence effects on hosts. In several crustacean systems, we have found that parasites influence both host predation rates on intra- and inter-guild prey and host vulnerability to being preyed upon. These trait effects can theoretically alter invasion impact and patterns of coexistence, as they indirectly affect interactions between predators and prey with the potential for further ramifications to other species in the food web. The fitness consequences of parasite-induced trait-mediated effects are rarely considered in traditional parasitological contexts, but demand attention in the context of ecological communities. We can regard these trait effects as a form of cryptic virulence that only becomes apparent when hosts are examined in the context of the other species with which they interact.

Two species of caridean shrimps (Decapoda:Hippolytidae and Nematocarcinidae) newly recorded from hydrothermally vents on the Manus Basin, Southwestern Pacific.

Two species of caridean shrimps are newly recorded from hydrothermal vents on the Manus Basin, southwestern Pacific, at depths of 1540-1577m. Lebbeus manus, new species, is related to L.curvirostris Zarenkov, 1976, L.elegans Komai, Hayashi & Kohtsuka, 2004, L.longipes (Kobjakova, 1936), L.vicinus vicinus (Rathbun, 1902) and L.vicinus motereyensis (Wicksten & Mendez, 1982) because of the lack of strap-like epipods on the second and third pereopods; but characters of the rostrum, carapace and abdomen immediately distinguish the new species from the these five taxa. Subadult and juvenile specimens of Nematocarcinus are referred to N.sp.aff.exilis, but their definite identification is postponed until additional specimens become available for study. There are a few minor differences between the present Manus specimens and European specimens representing N.exilis (Bate, 1888), suggesting that the Manus population may indeed represent a separate species.

Electric shock causes physiological stress responses in shore crabs, consistent with prediction of pain

Animal pain is defined by a series of expectations or criteria, one of which is that there should be a physiological stress response associated with noxious stimuli. While crustacean stress responses have been demonstrated they are typically preceded by escape behaviour and thus the physiological change might be attributed to the behaviour rather than a pain experience. We found higher levels of stress as measured by lactate in shore crabs exposed to brief electric shock than non-shocked controls. However, shocked crabs showed more vigorous behaviour than controls. We then matched crabs with the same level of behaviour and still found that shocked crabs had stronger stress response compared with controls. The finding of the stress response, coupled with previous findings of long-Term motivational change and avoidance learning, fulfils the criteria expected of a pain experience.