Parasites of the shore crab Carcinus maenas (L.): implications for reproductive potential and invasion success

The European shore crab, Carcinus maenas, is one of the most successful marine invasive species. Its success has been in part attributed to the loss of parasites, rekindling an interest in host-parasite interactions and impacts on host fitness in this crab. In the present study, we investigated C. maenas populations from Europe, South Africa and Australia for parasites, and assessed their impact on the fitness of male crabs. For the shore crab, testes weight along with success in mating competition is traded off against other life-history traits. We therefore used this parameter as an indicator both for reproductive fitness and a possible resource trade-off in response to parasite infestation. In the native range, crabs infested with Sacculina carcini showed significantly lower testes weight than uninfected crabs. However, helminth parasites did not generally cause reduced testes weights. Crab populations from South Africa and Australia were either parasitized at very low prevalences, or were completely parasite free. However, no population level effect of this parasite release was reflected in testes weight. These findings do not support a severe fitness impact of helminth parasites on C. maenas, which questions the role of parasites on its population dynamics, both in the native area and for invasive success.     

A membrane-bound hemoglobin from gills of the green shore crab Carcinus maenas

Most hemoglobins serve for the transport or storage of O(2). Although hemoglobins are widespread in "entomostracan" Crustacea, malacostracans harbor the copper-containing hemocyanin in their hemolymph. Usually, only one type of respiratory protein occurs within a single species. Here, we report the identification of a hemoglobin of the shore crab Carcinus maenas (Malacostraca, Brachyura). In contrast to the dodecameric hemocyanin of this species, C. maenas hemoglobin does not reside in the hemolymph but is restricted to the gills. Immunofluorescence studies and cell fractioning showed that C. maenas hemoglobin resides in the membrane of the chief cells of the gill. To the best of our knowledge, this is the first time that a membrane-bound hemoglobin has been identified in eukaryotes. Bioinformatic evaluation suggests that C. maenas hemoglobin is anchored in the membrane by N-myristoylation. Recombinant C. maenas hemoglobin has a hexacoordinate binding scheme at the Fe(2+) and an oxygen affinity of P(50) = 0.5 Torr. A rapid autoxidation rate precludes a function as oxygen carrier. We rather speculate that, analogous to prokaryotic membrane-globins, C. maenas hemoglobin carries out enzymatic functions to protect the lipids in cell membrane from reactive oxygen species. Sequence comparisons and phylogenetic studies suggested that the ancestral arthropod hemoglobin was most likely an N-myristoylated protein that did not have an O(2) supply function. True respiratory hemoglobins of arthropods, however, evolved independently in chironomid midges and branchiopod crustaceans.     

Inhibition between invasives: a newly introduced predator moderates the impacts of a previously established invasive predator

1. With continued globalization, species are being transported and introduced into novel habitats at an accelerating rate. Interactions between invasive species may provide important mechanisms that moderate their impacts on native species. 2. The European green crab Carcinus maenas is an aggressive predator that was introduced to the east coast of North America in the mid-1800 s and is capable of rapid consumption of bivalve prey. A newer invasive predator, the Asian shore crab Hemigrapsus sanguineus, was first discovered on the Atlantic coast in the 1980s, and now inhabits many of the same regions as C. maenas within the Gulf of Maine. Using a series of field and laboratory investigations, we examined the consequences of interactions between these predators. 3. Density patterns of these two species at different spatial scales are consistent with negative interactions. As a result of these interactions, C. maenas alters its diet to consume fewer mussels, its preferred prey, in the presence of H. sanguineus. Decreased mussel consumption in turn leads to lower growth rates for C. maenas, with potential detrimental effects on C. maenas populations. 4. Rather than an invasional meltdown, this study demonstrates that, within the Gulf of Maine, this new invasive predator can moderate the impacts of the older invasive predator.     

Cryptic invasions of the crab Carcinus detected by molecular phylogeography

Coastal marine ecosystems world-wide are threatened by invasions of nonindigenous species. The ubiquity of marine sibling species identifiable only by genetic analysis suggests that many invasions are cryptic and therefore undetected, causing an underestimation of the actual number and impacts of invading species. We test this hypothesis with European crabs in the genus Carcinus that have invaded five regions globally. Partial 16S ribosomal RNA gene sequences confirm sibling species status of morphologically similar Atlantic C. maenas and Mediterranean C. aestuarii . Based on 16S rRNA haplotypes, crabs from California, New England and Tasmania were all C. maenas . However, we report the cryptic multiple invasion of both species in Japan and South Africa, where only C. aestuarii and C. maenas , respectively, were previously recognized.     

Inhibition of carbonic anhydrase in the gills of two euryhaline crabs,Callinectes sapidus and Carcinus maenas,by heavy metals

Two subcellular fractions of gill tissue, cytoplasm and basolateral membranes, from two species of euryhaline decapod crustaceans, Callinectes sapidus and Carcinus maenas, acclimated to low salinity, were isolated via differential centrifugation. Carbonic anhydrase activity from both fractions was titrated against a variety of heavy metals in vitro. The metals Ag(+), Cd(2+), Cu(2+) and Zn(+) showed inhibitory action against the enzyme. Ki values for these metals against cytoplasmic CA from C. sapidus were in the range of 0.05-0.5 microM (for Ag(+), Cd(2+) and Cu(2+)) and 2-6 microM for Zn(+), some of the highest sensitivities reported for CA from an aquatic organism. The Ki values for these same metals were approximately 2-3 orders of magnitude higher for cytoplasmic CA from C. maenas, indicating that there are significant differences in heavy metal sensitivity in branchial CA from the two species, and that C. maenas possesses a metal-resistant CA isoform. It required concentrations of metals in the millimolar range, however, to inhibit CA activity from the membrane fraction of the gill of both species. There were no effects on either mortality or on hemolymph osmotic and ionic concentrations in C. maenas that were exposed to 10 microM Cd or Zn(+) at 32 per thousand salinity and subsequently transferred to 10 per thousand. The presence of a metal-resistant CA isoform in the gills of C. maenas suggests that this species would not be restricted from its normal estuarine environment by heavy metal pollution.     

Changes in abundance of native and introduced parasites (Hymenoptera: Braconidae), and of the target and non-target plant bug species (Hemiptera: Miridae), during two classical biological control programs in alfalfa.

High numbers of tarnished plant bugs [Lygus lineolaris (Palisot)], were once common in alfalfa, as was a low level of parasitism (9%) by the native Peristenus pallipes (Curtis). After the bivoltine European parasite Peristenus digoneutis Loan became well established, average parasitism of the first and second generations increased to 64%, and tarnished plant bug numbers dropped by 65%. This reduced host density eventually caused a decline in total parasitism by both parasite species to 22%. A few P. digoneutis also attacked the alfalfa plant bug, Adelphocoris lineolatus (Goeze), but did not reduce this pest or increase its parasitism rate. At another location, where P. digoneutis is not established, parasitism of first generation alfalfa plant bugs, an adventive (accidently introduced) pest, was increased to 21% by the introduced univoltine parasite, Peristenus conradi Marsh, and a slight reduction in the pest may have resulted. P. digoneutis did not parasitize the meadow plant bug, Leptopterna dolabrata (L.), an adventive pest of forage grasses, so did not affect this mirid or its parasite. Neither introduced parasite eliminated the native parasites of the tarnished or alfalfa plant bugs. The narrow host ranges of the braconid parasites of mirid nymphs are contrasted with the broad host range of the native tachinid parasite [Phasia robertsoni (Towns.)] of adult mirids. The major changes in mirid abundance and their mortality by parasites that slowly occurred during this 19-year study demonstrate the need for long-term field research, to adequately document and understand these complex interactions.     

Consumers that are not 'ideal' or 'free' can still approach the ideal free distribution using simple patch-leaving rules

1.  The ideal free distribution (IFD) has been widely used to determine whether consumers distribute themselves optimally. However, this theory is based on three assumptions that are clearly violated in many systems. The theory assumes that all individuals know the quality of each available site, are equally free to move between all sites, and have equal competitive abilities.
2.  I examine the utility of this theory to predict the distribution of the invasive European green crab Carcinus maenas , a species that likely violates all of these assumptions. I demonstrate three main findings.
3.  First, understanding how density-dependent interference and size alter individual foraging behaviour is important for understanding the density and biomass distribution of C. maenas in invaded habitats.
4.  Second, once behavioural mechanisms of crab foraging are accurately included in the model, the IFD does a good job of predicting the distribution of C. maenas , even though C. maenas violates the theory's fundamental assumptions.
5.  Third, C. maenas ' distribution can be obtained using simple decision rules and reasonable movement patterns.     

An experimental evaluation of host specificity: the role of encounter and compatibility filters for a rhizocephalan parasite of crabs

The encounter/compatibility paradigm of host specificity provides three qualitative pathways to the success or failure of a potential host-parasite interaction. It is usually impossible to distinguish between two of these (encounter and compatibility filters closed versus encounter filter open and compatibility filter closed) because unsuccessful infection attempts are difficult to observe in nature. We were able to open the encounter filter under experimental laboratory conditions. Our analytical system used the rhizocephalan barnacle, Sacculina carcini, a parasitic castrator of the European green crab, Carcinus maenas, and Pachygrapsus marmoratus, a native European crab that occurs with C. maenas but is not parasitized by S. carcini in nature. Penetration followed by unsuccessful infection of P. marmoratus crabs by parasitic barnacle larvae leaves a uniquely permanent record in the thoracic ganglion of the crabs. This provided us with a novel tool to quantify the encounter filter in a host-parasite system in nature. We demonstrated, in the laboratory, that the compatibility filter was closed and that, in nature, even where barnacle larvae were present, the encounter filter was also effectively closed. The closure of both filters in nature explains the failure of this potential host-parasite interaction, an outcome favored by selection in both host and parasite.     

The roles of Phlebotomus martini and P. celiae (Diptera: Phlebotominae) as vectors of visceral leishmaniasis in the Aba Roba focus, southern Ethiopia

Abstract. During field studies (December 1988 to April 1990) to determine the vectors of visceral leishmaniasis (kala-azar) in the Aba Roba (Segen Valley) focus of southern Ethiopia, a total of 40,770 sandflies (Diptera: Psychodidae: Phlebotominae) were collected and identified as six species of Phlebotomus and seventeen Sergentomyia spp. Nine of these species were anthropophilic (four Phlebotomus and five Sergentomyia spp.), the dominant being Phlebotomus (Synphlebotomus) martini, P.(S.)celiae and Sergentomyia (Sergentomyia) schwetzi. P. celiae adult populations increased during the rainy season. Of 2326 P. martini and 1044 P. celiae dissected, the parous rate was 29.9% and 24.4%, respectively. Leishmania promastigotes were detected in sixteen P. martini (eleven identified as L. donovani by isoenzyme analysis and/or a DNA probe) and in three P. celiae (two identified by DNA probe), giving overall infection rates of 0.7% (1.9% parous infection rate) and 0.3% (1.2% parous infection rate), respectively. Four isolates from P. martini were typed by their isoenzyme profile as L. donovani zymodeme MON-37 = LON-44, identical to one of the zymodemes isolated from patients in this focus. This is the first evidence that P. celiae is a vector and the first time that P. martini has been implicated in Ethiopia. Based on observations of abundance, seasonality and prevalence of infection of the two Synphlebotomus spp., it is concluded that P. martini is the major vector and P. celiae a secondary vector in the Aba Roba focus. The risk of infection with L. donovani is greatest during the wet season.     

The distribution and orientation of epizoic barnacles on crabs

The distribution and orientation of Balanus crenatus on Carcinus maenas is described. Elminius modestus was also found on C. maenas but it was not common. Both species of barnacle were also found on Cancer pagurus, although neither species of barnacle appeared to be as common on Cancer as on Carcinus. Possible reasons for this are discussed.
Treating the carapaces of similar sized C. maenas as sampling units it is clear that the distribution of B. crenatus over these sampling units is not random but is aggregated. This probably arises because of the gregarious nature of the cyprids when they settle out but other possibilities are considered. B. crenatus on the carapace of C. maenas is found exclusively in the grooves and depressions on the carapace and this is because the cyprids preferentially settle in concavities.
The orientation of B. crenatus also shows a consistent pattern, with the cirral nets facing predominantly backwards. This pattern could arise because the barnacle cyprids orientate to water currents, generated by the exhalant respiratory currents, flowing forwards over the carapace.     

Haemolymph parasite of the shore crab Carcinus maenas: pathology, ultrastructure and observations on crustacean haplosporidians

A protozoan parasite with some features of haplosporidians is described from the European shore crab Carcinus maenas. The parasite establishes a systemic infection through the haemal sinuses and connective tissues. Intracellular stages of the parasite were found within reserve inclusion, connective tissue, and muscle cells, while free forms were present in all haemal spaces. A uninucleate stage appeared to develop to a multinucleate plasmodial stage following multiple mitotic divisions of the nucleus. Histopathology also indicated that nuclear division may occur to form multinucleate plasmodia, in connective tissue, reserve inclusion and muscle cells, the multinucleate plasmodium being enclosed in the host-cell plasma membrane. It appears that the multinucleate plasmodium may then undergo internal cleavages which result in plasmodial fragmentation to form many uninucleate stages. Both stages, but particularly the uninucleate stage, contained cytoplasmic, large, ovoid, dense vesicles (DVs), some of which contained an internal membrane separating the medulla from the cortex, as in haplosporosomes. Golgi-like cisternae, closely associated with the nuclear membrane, formed DVs and haplosporosome-like bodies (HLBs), superficially resembling viruses. Infrequently, HLBs may condense to form haplosporosomes. The DVs, as in spores of some Haplosporidium spp. and paramyxeans, may give rise to, and are homologous with, haplosporosomes. Other features, such as the presence of an intranuclear mitotic spindle, lipid droplets, and attachment of DVs and haplosporosomes to the nuclear membrane, indicate that the C. maenas parasite is a haplosporidian. A similar organism reported from the haemolymph of spot prawns Pandalus spp., and haplosporidians reported from prawns Penaeus vannamei and crabs Callinectes sapidus may belong to this group. It is concluded that the well-characterised haplosporidians of molluscs and some other invertebrates may not be characteristic of the whole phylum, and that morphologically and developmentally similar organisms may also be haplosporidians, whether they have haplosporosomes or not.     

International cooperation on western corn rootworm ecology research: state-of-the-art and future research

1 Invasive pest species are challenging partly because the invasion process may be highly dynamic and because of the lack of knowledge of many researchers, professionals and farmers in the newly-invaded regions. The chrysomelid Diabrotica virgifera virgifera LeConte is such an invasive pest. It has been the main pest of continuous maize in the U.S.A. for more than 60 years and is currently spreading throughout Europe.
2 In the area with a long history of this pest (Central and North America), scientific knowledge concerning the ecology of this pest has accumulated over the last decades. This resource is of great importance to both America and Europe and has to be gathered, shared and adapted to new situations. We therefore examined, both qualitatively and quantitatively, the scientific literature relating to D.   virgifera virgifera ecology.
3 The quantitative analysis suggests that research on D.   virgifera virgifera ecology is still in its infancy in Europe and suffers from geographical barriers (between Europe and North America and between linguistic areas within Europe) and that scientific communication should be strengthened both between North America and Europe and within Europe.
4 As a first solution to this problem, we introduce three companion review articles that constitute a landmark for D.   virgifera virgifera research, enabling European and American scientists and decision-makers to orient themselves and discover new opportunities for research. We also stress that international research cooperation is the most important key to successfully manage invasive species.     

Ambient fauna impairs parasite transmission in a marine parasite-host system

To understand possible factors controlling transmission of trematode larvae between first and second intermediate hosts we examined the impact of ambient fauna on parasite transmission in a marine intertidal parasite-host association. Cockle hosts (Cerastoderma edule) kept together with selected co-occurring macrozoobenthic species in mesocosms acquired a lower parasite load compared to cockles kept alone, when targeted by cercariae of the trematode Himasthla elongata. The reduction of parasite load in the cockles differed between the 7 macrozoobenthic species tested and was between 35 and 91%. Three different types of reduction could be distinguished: (1) predators (Carcinus maenas, Crangon crangon) actively preying upon cercariae, (2) non-host filter feeders (Crepidula fornicata, Mya arenaria, Crassostrea gigas) filtering cercariae but not becoming infected and (3) alternative hosts (Mytilus edulis, Macoma balthica) becoming infected by the cercariae and thus distracting cercariae from the target hosts. In addition, interference competition may occur in the form of disturbance of cockles by ambient organisms resulting in lower filtration rates and subsequently lower parasite loads. Our results suggest that the species composition and relative abundance of the ambient fauna of parasite-host systems play an important role in controlling trematode transmission rates in benthic marine systems.     

Occurrence of Ditylenchus weischeri and Not D. dipsaci in Field Pea Harvest Samples and Cirsium arvense in the Canadian Prairies

The stem nematode, a parasite of the herbaceous perennial weed, Cirsium arvense (L.) Scop. and identified as Ditylenchus dipsaci (Kühn) Filipjev, was reported in the Canadian prairies in 1979. Recently, D. weischeri Chizhov parasitizing Cirsium arvense was described in Russia, and it has been shown that this species is not an agricultural pest. In this study, we examined Ditylenchus species found in field pea (Pisum sativum L.) grain harvest samples in 2009 and 2010 and from C. arvense shoots in pea fields in the Saskatchewan, Alberta, and Manitoba provinces. Samples from 538 fields (mainly yellow pea) were provided by 151 growers throughout the main pea-growing area of the Canadian prairies. Of the samples collected, 2% were positive for Ditylenchus. The population density of the nematode ranged between 4 and 1,500 nematodes kg^-1 pea harvest sample and related to presence of C. arvense seeds. Positive samples occurred in 2009 but not in 2010 and were from throughout the pea-growing area of the Canadian prairies and not related to cropping history. C. arvense collected from yellow pea fields in Saskatchewan and Manitoba, but not Alberta, were infested with Ditylenchus. Morphological and molecular (ITS-PCR-RFLP) traits indicated that this species belongs to D. weischeri. The results indicated the stem nematode found in yellow pea grain is D. weischeri which resided with C. arvense seeds and debris to pea samples. Unlike D. dipsaci, D. weischeri is not a nematode pest of economic importance; therefore, its presence in the pea harvest samples was not a concern.     

Interspecific hybridization and mitochondrial introgression in invasive carcinus shore crabs

Interspecific hybridization plays an important role in facilitating adaptive evolutionary change. More specifically, recent studies have demonstrated that hybridization may dramatically influence the establishment, spread, and impact of invasive populations. In Japan, previous genetic evidence for the presence of two non-native congeners, the European green crab Carcinus maenas and the Mediterranean green crab C. aestuarii, has raised questions regarding the possibility of hybridization between these sister species. Here I present analysis based on both nuclear microsatellites and the mitochondrial cytochrome C oxidase subunit I (COI) gene which unambiguously argues for a hybrid origin of Japanese Carcinus. Despite the presence of mitochondrial lineages derived from both C. maenas and C. aestuarii, the Japanese population is panmictic at nuclear loci and has achieved cytonuclear equilibrium throughout the sampled range in Japan. Furthermore, analysis of admixture at nuclear loci indicates dramatic introgression of the C. maenas mitochondrial genome into a predominantly C. aestuarii nuclear background. These patterns, along with inferences drawn from the observational record, argue for a hybridization event pre-dating the arrival of Carcinus in Japan. The clarification of both invasion history and evolutionary history afforded by genetic analysis provides information that may be critically important to future studies aimed at assessing risks posed by invasive Carcinus populations to Japan and the surrounding region.     

The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap

The genotypic structure of parasite populations is an important determinant of ecological and evolutionary dynamics of host-parasite interactions with consequences for pest management and disease control. Genotypic structure is especially interesting where multiple hosts co-exist and share parasites. We here analyze the natural genotypic distribution of Crithidia bombi, a trypanosomatid parasite of bumblebees (Bombus spp.), in two ecologically different habitats over a time period of three years. Using an algorithm to reconstruct genotypes in cases of multiple infections, and combining these with directly identified genotypes from single infections, we find a striking diversity of infection for both data sets, with almost all multi-locus genotypes being unique, and are inferring that around half of the total infections are resulting from multiple strains. Our analyses further suggest a mixture of clonality and sexuality in natural populations of this parasite species. Finally, we ask whether parasite genotypes are associated with host species (the phylogenetic hypothesis) or whether ecological factors (niche overlap in flower choice) shape the distribution of parasite genotypes (the ecological hypothesis). Redundancy analysis demonstrates that in the region with relatively high parasite prevalence, both host species identity and niche overlap are equally important factors shaping the distribution of parasite strains, whereas in the region with lower parasite prevalence, niche overlap more strongly contributes to the distribution observed. Overall, our study underlines the importance of ecological factors in shaping the natural dynamics of host-parasite systems.     

Developing the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and related species

The impacts of introduced marine pests are becoming increasingly apparent, prompting interest in the possibility of their biological control. We undertook laboratory and field experiments on host selection of one potential control agent (the endoparasitic barnacle, Sacculina carcini) against its natural host (the widely invasive European shore crab, Carcinus maenas) and several confamilial and more distantly related crustaceans. For comparison, we also tested host specificity in a related parasitic barnacle, Heterosaccus lunatus. The results confirm indistinct behavioral host selection in S. carcini, indicate very different mechanisms for host selection by S. carcini and H. lunatus (which could be related to differences between the two species in attachment points), and suggest host specificity in S. carcini depends on interactions between the parasite and the host's physiology. Development of convincing safety trials for marine parasites like S. carcini, in which the infective stage is a planktonic larva, will be more difficult than for many terrestrial parasites and will require detailed knowledge of the parasite's behavior and physiological interaction with its hosts.     

Response to soil biota by native, introduced non-pest, and pest grass species: is responsiveness a mechanism for invasion?

Soil biota have been credited with helping to maintain native plant diversity in multiple systems. Recent evidence suggests that introduced species may be less responsive to soil communities than most native species. If response to soil communities is correlated with invasive ability, we predict that introduced pest species should be less responsive to soil communities than introduced non-pest species or natives. In this study we test whether response to soil biota from two diverse grassland communities differs between four introduced pest, six introduced non-pest, and five native species in grasses in Yolo County, California. We found no variation in plant size or response to soil biota between introduced pest and introduced non-pest species, and these were combined in subsequent analyses. Overall, all introduced species grew significantly faster than native species. Native species showed greater variation in response to soil communities than both groups of introduced species, and native species’ response varied with soil community. Variation among native species’ response to soil nutrients and biota through processes like soil feedbacks may be key to maintaining diversity across landscapes in uninvaded environments. Introduced species appear less responsive to landscape variability in soil communities, which may allow them to establish and dominate plant communities in multiple habitats.     

Has the introduction of brown trout altered disease patterns in native New Zealand fish?

1. It is well recognised that non-indigenous species (NIS) can affect native communities via the 'spillover' of introduced parasites. However, two other potentially important processes, the 'spillback' of native parasites from a competent NIS host, where the latter acts as a reservoir leading to amplified infection in native hosts, and the 'dilution' of parasitism by a NIS host acting as a sink for native parasites, have either not been tested or largely overlooked.
2. We surveyed the helminth parasite fauna of native New Zealand fish in Otago streams that varied in the abundance of introduced brown trout Salmo trutta , to look for evidence of spillback and/or dilution. Spillover is not an issue in this system, with trout introduced as parasite-free eggs.
3. Seven native parasite species were present across 12 sites; significant inverse relationships with an index of trout abundance (i.e. dilution) were documented for three species infecting the native upland bully Gobiomorphus breviceps , and one species infecting the native roundhead galaxias Galaxias anomalus .
4. An inverse relationship between bully energy status and infection intensity of one parasite species suggests that parasite dilution could have positive effects on bully populations. Our failure to detect similar relationships for the other parasites does not preclude the possibility that dilution is beneficial to native fish, since parasites may have subtle or unmeasured impacts.
5. The parasite dilution patterns reported are compelling in that they occurred across several native host and parasite species; as such they have important implications for invasion ecology, providing an interesting contrast to the largely negative impacts reported for NIS. Mechanisms potentially responsible for the patterns observed are discussed.