Links community ecology and epidemiology to demonstrate how parasites affect species interactions and consequently ecosystem function, invasions and emerging ...
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We designed fluorescence in situ hybridization probes for two distinct microsporidian clades and demonstrated their application in detecting, respectively, Nosema/Vairimorpha and Dictyoceola species. We used them to study the vertical transmission of two microsporidia infecting the amphipod Gammarus duebeni.
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Feminizing parasites enhance their vertical transmission to the host offspring by converting genetic male hosts into phenotypic females. Crustacea are the only invertebrates where sexual differentiation is controlled by a specialised endocrine organ, the androgenic gland, rather than by the gonads. We showed that a feminizing microsporidian Microsporidium sp. inhibits androgenic gland differentiation. We investigated the effect of Microsporidium sp. and a second feminizing microsporidium, Nosema granulosis, on the masculinizing function of the androgenic gland in Gammarus duebeni. Androgenic gland implants had a masculinizing effect on the sexual characteristics and sexual behaviour of recipient female hosts, reflecting the masculinizing function of the androgenic gland. Individuals that had received androgenic glands showed changed morphology in comparison with controls; they were bigger overall, they lost their oostegite marginal setae, developed calceoli and acquired a male-like behaviour. This effect was observed in uninfected females, as well as in females infected with the Microsporidium sp. The masculinizing effect of androgenic gland implants was smaller in N. granulosis infected individuals. N. granulosis and Microsporidium sp. fall into distinct clades of the Microspora. It appears that these divergent parasites both act by inhibiting the development of the androgenic gland. However, they differ in their ability to inhibit the host's response to the hormone that controls male sexual differentiation.
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Branchiobdellidans or crayfish worms are clitellate annelids and ectosymbionts of freshwater crayfish. An investigation of branchiobdellidan infestation was undertaken in a population of endangered white-clawed crayfish (Austropotamobius pallipes) in the river Aire, UK. Thirty two percent of animals were infested either by the adult parasite or their cocoons (n=107). Parasite burden increased with host size, but did not differ with sex. Observations of crayfish gill tissue revealed a strong positive relationship between melanization of filaments and parasite prevalence and burden. Taxonomic identification revealed that 1 species of branchiobdellidan was present, Branchiobdella astaci. The first sequences were generated for this species and phylogenetically analysed alongside published sequences for 5 other branchiobdellidan species in Europe. The position of B. astaci within the genus Branchiobdella was confirmed, and it was found to cluster as a sister group to B. parasita.
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Background: Invasive predators may change the structure of invaded communities through predation and competition with native species. In Europe, the invasive signal crayfish Pacifastacus leniusculus is excluding the native white clawed crayfish Austropotamobius pallipes. Methodology and Principal Findings: This study compared the predatory functional responses and prey choice of native and invasive crayfish and measured impacts of parasitism on the predatory strength of the native species. Invasive crayfish showed a higher (>10%) prey (Gammarus pulex) intake rate than (size matched) natives, reflecting a shorter (16%) prey handling time. The native crayfish also showed greater selection for crustacean prey over molluscs and bloodworm, whereas the invasive species was a more generalist predator. A. pallipes parasitised by the microsporidian parasite Thelohania contejeani showed a 30% reduction in prey intake. We suggest that this results from parasite-induced muscle damage, and this is supported by a reduced (38%) attack rate and increased (30%) prey handling time. Conclusions and Significance: Our results indicate that the per capita (i.e., functional response) difference between the species may contribute to success of the invader and extinction of the native species, as well as decreased biodiversity and biomass in invaded rivers. In addition, the reduced predatory strength of parasitized natives may impair their competitive abilities, facilitating exclusion by the invader.© 2012 Haddaway et al.
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Relocation of threatened populations is a common method employed in conservation. However, environmental differences in the new habitat may reduce the survival of relocated populations, while phenotypic plasticity may enhance the likelihood of establishment of relocated populations in their novel environment. Conservation of the British white-clawed crayfish (Austropotamobius pallipes; IUCN Red Data List - Endangered) often involves relocation of threatened populations into isolated ponds (Ark Sites), where risk of competition with invasive crayfish is minimized. In this study, the morphology (using 12 morphometric variables) of A. pallipes in wild populations was investigated with respect to eco-geographic variables. A field cage experiment was carried out to compare the relative survival, growth, and change in morphology of crayfish from lotic (stream) and lentic (pond) donor habitats following relocation to a lentic recipient habitat. In the wild, lentic crayfish were broader than their lotic counterparts, which may reflect an increase in branchial (gill) volume in adaptation to an oxygen-poor benthic environment. In the relocation experiment there was no difference in the length, growth, or survival of animals from relocated lentic, lotic, or control populations. However, crayfish derived from a lotic population showed an increase in carapace width and areola width over the 4-month growing season following relocation. This evidence for phenotypic plasticity suggests that crayfish are resilient to relocation, and that they can adapt morphologically to novel environmental conditions. Relocation of threatened populations of A. pallipes may therefore prove a useful technique in the conservation of white-clawed crayfish populations within the UK.© 2012 John Wiley&Sons, Ltd.
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Community ecologists generally recognize the importance of species - such as pollinators - that have clear positive effects within ecosystems. However, parasites - usually regarded in terms of their detrimental effects on the individuals they infect - can also have positive impacts on other species in the community. We now recognize that parasites influence species coexistence and extirpation by altering competition, predation, and herbivory, and that these effects can, in turn, influence ecosystem properties. Parasites and pathogens act as ecosystem engineers, alter energy budgets and nutrient cycling, and influence biodiversity. Equally, because ecosystem properties - such as biodiversity - affect parasite populations, there is the potential for feedback between parasitism and ecosystem states. Using examples from animal and plant systems, we examine this potential bidirectional interdependence and challenge the conventional wisdom that parasites have only negative or inconsequential impacts on ecological communities.© The Ecological Society of America.
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Foraging, when senses are limited to olfaction, is composed of two distinct stages: the detection of prey and the location of prey. While specialist olfactory foragers are able to locate prey using olfactory cues alone, this may not be the case for foragers that rely primarily on vision. Visual predators in aquatic systems may be faced with poor visual conditions such as natural or human-induced turbidity. The ability of visual predators to compensate for poor visual conditions by using other senses is not well understood, although it is widely accepted that primarily visual fish, such as three-spined sticklebacks, Gasterosteus aculeatus, can detect and use olfactory cues for a range of purposes. We investigated the ability of sticklebacks to detect the presence of prey and to locate prey precisely, using olfaction, in clear and turbid (two levels) water. When provided with only a visual cue, or only an olfactory cue, sticklebacks showed a similar ability to detect prey, but a combination of these cues improved their performance. In open-arena foraging trials, a dispersed olfactory cue added to the water (masking cues from the prey) improved foraging success, contrary to our expectations, whereas activity levels and swimming speed did not change as a result of olfactory cue availability. We suggest that olfaction functions to allow visual predators to detect rather than locate prey and that olfactory cues have an appetitive effect, enhancing motivation to forage.© 2012 The Association for the Study of Animal Behaviour.
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The microsporidian parasite Thelohania contejeani causes porcelain disease and has been implicated in mass mortalities in populations of the endangered European crayfish Austropotamobius pallipes. However, the route of parasite transmission is not known. This paper investigates the horizontal transmission of T. contejeani between A. pallipes hosts as well as its transmissibility to the invasive signal crayfish (Pacifastacus leniusculus). Field collected juvenile A. pallipes and P. leniusculus were assigned to 1 of 3 experimental treatments; fed heavily infected A. pallipes tissue, exposed to water from tanks housing heavily parasitized A. pallipes, and a control group to provide an estimate of the baseline infection levels in the field. After 26 weeks, abdominal muscle samples were screened by PCR for T. contejeani. Infection was significantly higher in the treatment groups (83% in the cannibalism treatment, 42% in the water exposure treatment) than in the control group (4%), providing evidence for horizontal transmission of the parasite between A. pallipes hosts. Cannibalism and scavenging are common amongst crayfish, providing transmission opportunities in the field. The study also provides the first direct evidence for transmission of the parasite from an indigenous European crayfish species to the invasive signal crayfish, with 50% of P. leniusculus in each treatment, and 8% of control animals infected. We discuss the possibility that high density populations of the invasive signal crayfish may serve either as reservoirs or sinks for the parasite.
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Introduced species disrupt native communities and biodiversity worldwide. Parasitic infections (and at times, their absence) are thought to be a key component in the success and impact of biological invasions by plants and animals. They can facilitate or limit invasions, and positively or negatively impact native species. Parasites have not only direct effects on their hosts, but also indirect effects on the species with which their hosts interact. Indirect effects include density-mediated effects (resulting from parasite-induced reduction in host reproduction and survival) as well as trait-mediated indirect effects (resulting from parasite-induced changes in host phenotype, behaviour or life history). These effects are not mutually exclusive but often interact. The importance of these indirect interactions for invasion success, and the extent to which these effects ramify throughout communities and influence ecosystems undergoing biological invasion provide the focus of our review. Examples from the animal and plant literature illustrate the importance of parasites in mediating both competitive and consumer-resource interactions between native and invasive species. Parasites are involved in indirect interactions at all trophic levels. Furthermore, the indirect effects of parasitic infection are important at a range of biological scales from within a host to the whole ecosystem in determining invasion success and impact. To understand the importance of parasitic infection in invasion success and in the outcomes for invaded communities requires an interdisciplinary approach by ecologists and parasitologists, across animal and plant systems. Future research should develop a framework integrating community ecology, evolution and immunology to better understand and manage the spread of invasive species and their diseases.© 2012 The Authors. Functional Ecology © 2012 British Ecological Society.
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Emerging infectious diseases (EIDs) are recognized as having significant social, economic and ecological costs, threatening human health, food security, wildlife conservation and biodiversity. We review the processes underlying the emergence of infectious disease, focusing on the similarities and differences between conceptual models of disease emergence and biological invasions in general. Study of the IUCN's list of the world's worst invaders reveals that disease is cited as a driver behind the conservation, medical or economic impact of nearly a quarter of the species on the data base. The emergence of novel diseases in new host species are, in essence, examples of invasions by parasites. Many of the ecological and anthropogenic drivers of disease emergence and classical invasions are also shared, with environmental change and global transport providing opportunities for the introduction and spread of invaders and novel parasites. The phases of disease emergence and biological invasions have many parallels; particularly the early and late phases, where demographic and anthropogenic factors are key drivers. However, there are also differences in the intermediate phases, where host-parasite co-evolution plays a crucial role in determining parasite establishment in novel hosts. Similar opportunities and constraints on control and management occur at the different phases of invasions and disease emergence. However, exploitation of host immune responses offers additional control opportunities through contact control and vaccination against EIDs. We propose that cross-fertilization between the disciplines of disease emergence and invasion biology may provide further insights into their prediction, control and management.© 2012 British Ecological Society.
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Introduced species disrupt native communities and biodiversity worldwide. Parasitic infections (and at times, their absence) are thought to be a key component in the success and impact of biological invasions by plants and animals. They can facilitate or limit invasions, and positively or negatively impact native species. Parasites have not only direct effects on their hosts, but also indirect effects on the species with which their hosts interact. Indirect effects include density-mediated effects (resulting from parasite-induced reduction in host reproduction and survival) as well as trait-mediated indirect effects (resulting from parasite-induced changes in host phenotype, behaviour or life history). These effects are not mutually exclusive but often interact. The importance of these indirect interactions for invasion success, and the extent to which these effects ramify throughout communities and influence ecosystems undergoing biological invasion provide the focus of our review. Examples from the animal and plant literature illustrate the importance of parasites in mediating both competitive and consumer-resource interactions between native and invasive species. Parasites are involved in indirect interactions at all trophic levels. Furthermore, the indirect effects of parasitic infection are important at a range of biological scales from within a host to the whole ecosystem in determining invasion success and impact. To understand the importance of parasitic infection in invasion success and in the outcomes for invaded communities requires an interdisciplinary approach by ecologists and parasitologists, across animal and plant systems. Future research should develop a framework integrating community ecology, evolution and immunology to better understand and manage the spread of invasive species and their diseases.© 2012 British Ecological Society.
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Background: Sex-ratio distorting parasites are of interest due to their effects upon host population dynamics and their potential to influence the evolution of host sex determination systems. In theory, the ability to distort host sex-ratios allows a parasite with efficient vertical (hereditary) transmission to dispense completely with horizontal (infectious) transmission. However, recent empirical studies indicate that some sex-ratio distorting parasites have retained the capability for horizontal transmission. Results: Numerical simulations using biologically realistic parameters suggest that a feminising parasite is only likely to lose the capability for horizontal transmission if its host occurs at low density and/or has a male-biased primary sex ratio. It is also demonstrated that even a small amount of horizontal transmission can allow multiple feminising parasites to coexist within a single host population. Finally it is shown that, by boosting its host's rate of population growth, a feminising parasite can increase its own horizontal transmission and allow the invasion of other, more virulent parasites. Conclusions: The prediction that sex-ratio distorting parasites are likely to retain a degree of horizontal transmission has important implications for the epidemiology and host-parasite interactions of these organisms. It may also explain the frequent co-occurrence of several sex-ratio distorting parasite species in nature.© 2011 Ironside et al; licensee BioMed Central Ltd.
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Marking for recognition of individual animals is often required in population studies. Marking Crustacea requires that identifiers be readable throughout successive moults, making regular external tags unsuitable. A suite of marking methods have therefore been developed to cope with this. We review the efficacy, cost, and suitability of eight available marking methods for Crustacea, particularly for crayfish. Two methods are low cost and may have minimal impacts on growth and survival; visible implant elastomer (VIE) and electric cauterisation. Austropotamobius pallipes, the only native crayfish in Britain, is listed as Vulnerable by the IUCN and conservation efforts are currently underway to preserve the species. The success of relocation conservation may be assessed by analysing individual growth, survival and reproduction, requiring long-term identification of individuals in the wild. We experimentally assessed the impacts of VIE in juvenileA pallipes and electric cauterisation in adultA pallipes and Pacifastacus leniusculus. Our results indicate that electric cauterisation reduces growth in A pallipes but not P. leniusculus. We observed no impact of Visible Implant Elastomer on growth or survival in juvenile A pallipes, however tag migration was observed. The VIE method is suitable for marking large numbers of individuals, but caution must be used when individual recognition is required due to tag migration.© 2011 International Association of Astacology.
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Invasive signal crayfish are a major threat to the endangered native white-clawed crayfish in Britain. The River Wharfe in Yorkshire is the site of a signal crayfish invasion that has been progressing since the late 1980s. A recent discovery in this river was signal crayfish infected with Thelohania contejeani, a microsporidian parasite which normally infects white-clawed crayfish and causes porcelain disease. During 2007 and 2009 we delineated the ongoing invasion by trapping and hand sampling, and compared sex ratios and sizes seasonally and spatially. We screened crayfish of both species for T. contejeani using PCR to determine parasite prevalence. The invasion in the river has progressed at an overall downstream rate of 1.7 km yr and an overall upstream rate of 0.5 km yr. A reduction in native crayfish populations has occurred in the downstream reach of the river, even in locations not immediately threatened by signal crayfish. Sex ratios of captured signal crayfish varied seasonally and spatially throughout the invasion zone. Thelohania contejeani was found in both crayfish species at similar overall prevalence (12%, signal; 14%, white-clawed), and there is concern that signal crayfish may serve as reservoir hosts for the parasite where they co-occur with white-clawed crayfish.© 2011 International Association of Astacology.
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There is considerable current interest in the role that parasites can play in biological invasions. This review looks at the fate of parasites during a biological invasion and at their impact on native and invasive hosts, and asks whether parasites can mediate invasion success. An introduced species may lose its parasites as a result of the introduction and such release from its natural enemies may be an important factor determining invasion success. In addition, an introduced species may acquire parasites from its new environment or it may introduce novel parasites to hosts in the new range. As a result of local adaptation, parasites tend to have a differential effect on native versus invading hosts. The relative impact on the fitness of natives and invaders can be important for the outcome of an invasion and may, for example, reverse the pattern of competitive dominance seen in uninfected hosts. Parasites may mediate invasion success through their effect on host fitness and thus on host population growth and stability. Furthermore, by modifying host-host interactions (including competition and predation), parasites can be important factors that determine the success of an invasion and its impact on the recipient community.© 2009 Elsevier Ltd. All rights reserved.
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Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46 % of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45 % of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39 % of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24 %) and survival (44 %) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution. (c) 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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In the crustacean Gammarus duebeni, sex is determined by the interaction of a number of environmental, genetic and parasitic factors, which may, in turn, influence sex ratios and population dynamics. We produce novel evidence that environmental sex determination (ESD) in G. duebeni depends primarily on the interaction of two environmental cues: day length and temperature. Whereas previous work found that male-biased sex ratios were produced under long day conditions and female biases under short days, we show that, at the lower temperatures normally experienced by this species at northern latitudes, the reverse pattern can occur. We measured ESD in four U.K. populations and found among-population variation in the level of ESD and in the cues that determined sex. In the light of these findings, we conclude that patterns of ESD across the four populations may reflect selection based on differences in breeding season and discrete/overlapping generations.
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Recent reports have demonstrated a cost associated with intersexuality in Amphipoda, including reduced fecundity and fertility. In this study, the gross morphology of the gonads in normal and intersex Echinogammarus marinus (Amphipoda) were compared to determine whether resource allocation to gonadal tissue accounted for this reduced fitness. Evidence for the presence of the male sex-determining hormone, androgenic gland hormone (AGH), was compared between sexual phenotypes using MALDI mass spectrometry. Two distinct intersex phenotypes ('male' intersex and 'female' intersex) were found, with variation in gonadal structure corresponding with external phenotype. Examination of male intersexes revealed normal testicular development (testes, seminal vesicles and vas deferens), but also revealed the formation of an oviduct. Ovaries of intersex females showed normal ovarian development, but were reduced in length by approximately 20% due to the presence of vas deferens. The number of vas deferens in intersex females was equal to the number (one or two) of genital papillae. We hypothesise that the reduced ovarian length observed in intersex females is a likely cause of the reduced brood size previously reported in intersex females of this species. Variation in the sexual phenotype corresponded both to development of the androgenic gland and to expression of a peptide fragment corresponding to the A chain of androgenic gland hormone (AGH). Androgenic glands and a putative AGH peptide were present in males. However, in both normal and intersex females, the androgenic glands were only present in a rudiment form and the peptide was not detected. Intersex males were found to possess abnormal glands that appeared hypertrophied. However, AGH peptides were not detected, supporting the suggestion that the intersex phenotype is manifested via perturbations of AGH.
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Microsporidian parasites infect almost all invertebrate and vertebrate hosts and have significant effects on individual and population fitness. Phylogenetic analysis demonstrates that the phylum is highly divergent and that some lineages show strong associations with host taxa. We here examine the diversity and distribution of parasites in gastropod molluscs to test for host-parasite co-association. 16 populations representing 10 species of freshwater snails were screened using microsporidian specific small subunit rDNA primers. Four novel microsporidian parasite sequences were detected within populations of three host species from the genera Bulinus, Biomphalaria and Planorbis. Prevalence ranged from 5 to 84%. Phylogenetic analysis of these novel sequences reveals that they group together as a paraphyletic assemblage in the microsporidian tree basal to the two lineages containing the genera Encephalitozoon and Nosema. Preliminary observation of one microsporidian infection, show parasites distributed in all tissue systems of Bulinus globosus. However, infection is most prevalent in the digestive gland while also in the egg sacs, suggesting that the microsporidium is using a mixed strategy of horizontal and vertical transmission in this population.
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Parasites that are vertically transmitted (passed from mother to offspring via the gametes) have an unusual relationship with their hosts. Vertically transmitted parasites depend on successful host reproduction for transmission to the next generation of hosts. As a result, these parasites tend to have little effect on host growth, survival or reproduction. However, many vertically transmitted parasites including some viruses, bacteria and microsporidia, manipulate host reproduction and cause sex ratio distortion in the host population either through killing male hosts or by converting males into females. This review asks why parasites distort host sex ratios and considers the implications of sex ratio distorting parasites for host ecology and evolution.
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We investigated the effects of parasitism and temperature on the production of intersexes in the amphipod Gammarus duebeni from a field population at Cumbrae, Scotland. There was significant temporal variation in intersex frequency which ranged from 0.5 to 5.2% in monthly field collections. Prevalence of Nosema granulosis, a feminising microsporidian parasite, also varied temporally and there was a significant correlation between parasite prevalence and intersex frequency in the field. Intersexes ( 16.3 +/- 0.4 mg) were larger than true females ( 14.8 +/- 0.1 mg) but produced fewer eggs thus demonstrating a cost of intersexuality. Intersexes were less likely to be paired than true females. In a breeding experiment, only females infected by N. granulosis produced intersex offspring. Temperature had no effect on intersex frequency. Intersexes therefore appear to be the result of incomplete feminisation by N. granulosis in this population. These results contrast with previous studies of G. duebeni from different populations which found that intersexes were the result of abnormal development under environmental sex determination. We suggest that intersexuality may be induced by both environmental and parasitic factors in populations of G. duebeni.
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In lethal and sublethal ammonia toxicity tests, we examined differences in tolerance of three species of freshwater amphipods, one native and two invasive in Ireland. The native Gammarus duebeni celticus was slightly less tolerant to ammonia than the invasive G. pulex (96h LC50 = 1.155 and 1.544 mg l(-1), respectively), while another invader, Crangonyx pseudograeilis, had the lowest tolerance (LC50 = 0.36 mg l(-1)). Parasitism of G. pulex by the acanthocephalan Echinorhynchus truttae greatly reduced the tolerance of the invader to ammonia (LC50 = 0.381 mg l(-1)). Further, precopula pair disruption tests indicated that G. d. celticus was more sensitive to ammonia than G. pulex at sublethal levels. We discuss these results in the context of the ecological replacements of native by invader amphipods. (C) 2004 Elsevier Ltd. All rights reserved.
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With field, laboratory, and modeling approaches, we examined the interplay among habitat structure, intraguild predation (IGP), and parasitism in an ongoing species invasion. Native Gammarus duebeni celticus (Crustacea: Amphipoda) are often, but not always, replaced by the invader Gammarus pulex through differential IGP. The muscle-wasting microsporidian parasite Pleistophora mulleri infects the native but not the invader. We found a highly variable prevalence of P. mulleri in uninvaded rivers, with 0-91% of hosts parasitized per sample. In addition, unparasitized natives dominated fast-flowing riffle patches of river, whereas parasitized individuals dominated slower-flowing, pooled patches. We examined the survivorship of invader and native in single and mixed-species microcosms with high, intermediate, and zero parasite prevalence. G. pulex survivorship was high in all treatments, whereas G. duebeni subsp. celticus survivorship was significantly lower in the presence of the invader. Further, parasitized G. duebeni subsp. celticus experienced near-total elimination. Models of the species replacement process implied that parasite-enhanced IGP would make invasion by G. pulex more likely, regardless of habitat and parasite spatial structure. However, where heterogeneity in parasite prevalence creates a landscape of patches with different susceptibilities to invasion, G. pulex may succeed in cases where invasion would not be possible if patches were equivalent. The different responses of parasitized and unparasitized G. duebeni subsp. celticus to environmental heterogeneity potentially link landscape patterns to the success or failure of the invasion process.
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The amphipod Gammarus duebeni is host to the feminising microsporidian parasite Nosema granulosis that converts males into functional females. To test the hypothesis that the parasite acts through endocrine disruption we compared the morphology of the gonad and activity of the androgenic gland, which coordinates male sexual differentiation, in infected and uninfected animals. Male gonad consisted of testis, seminal vesicle and vas deferens that was anchored to the genital papilla on segment 7. The androgenic gland was associated with the distal end of the vas deferens. In female and intersex animals the bi-lobed ovary opened into the oviduct at segment 5, vestigial vas deferens and vestigial androgenic gland were retained. The majority of parasitised individuals (38/39) were either phenotypic females or intersexes with fully developed ovaries and an undifferentiated androgenic gland. Our data suggest that the parasite prevents differentiation of the androgenic gland. In further support of this hypothesis, mass spectrometry of a single androgenic gland from males revealed a dominant molecular ion with a mass/charge ratio of 4818.4 + H, corresponding to a peptide of androgenic gland hormone from Armadillidium vulgare. In contrast the vestigial androgenic gland from parasitised and unparasitised females showed only low intensity peaks. Our observations demonstrate that the parasite manipulates host sex by preventing androgenic gland differentiation, androgenic gland hormone production and consequently male differentiation. This is in agreement with observations of A. vulgare with inherited Wolbachia infection, suggesting that phylogenetically distant feminisers manipulate hosts through a common mechanism. The high frequency of infection in intersexes (89.3%) suggests that this phenotype results from incomplete feminisation by the parasite. (C) 2004 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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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.
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Biological invasions are global threats to biodiversity and parasites might play a role in determining invasion outcomes. Transmission of parasites from invading to native species can occur, aiding the invasion process, whilst the 'release' of invaders from parasites can also facilitate invasions. Parasites might also have indirect effects on the outcomes of invasions by mediating a range of competitive and predatory interactions among native and invading species. Although pathogen outbreaks can cause catastrophic species loss with knock-on effects for community structure, it is less clear what impact persistent, sub-lethal parasitism has on native-invader interactions and community structure. Here, we show that the influence of parasitism on the outcomes of animal invasions is more subtle and wide ranging than has been previously realized.
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Parasitism is known to be an important factor in determining the success of biological invasions. Here we examine Crangonyx pseudogracilis, a North American amphipod invasive in the United Kingdom and describe a novel microsporidium, Fibrillanosema crangonycis n.sp., n.g. The primary site of infection is the female gonad and the parasite is transovarially transmitted to the eggs. PCR screening reveals a female bias in the distribution of parasites (96.6% of females, N = 29; 22.2% of males, N = 27), which is indicative of host sex ratio distortion. The morphological and molecular characterisations of this new microsporidium place it outside all currently established genera. On the basis of these differences, we erect the new genus Fibrillanosema n.g. While F. crangonycis is morphologically identical to uncharacterised microsporidia from populations of North American amphipods, it is distinct from microsporidia found in European populations of amphipods. These data support the hypothesis that vertically transmitted parasites may be selectively retained during invasion events. Furthermore where vertical transmission is combined with host sex ratio distortion these parasites may directly enhance host invasion success through increased rates of population growth. (C) 2003 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
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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 native's survivorship was two thirds that of the invader. We conclude that decreasing water quality favours replacement of the native by the invader.
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The classification of a microsporidian parasite observed in the abdominal muscles of amphipod hosts has been repeatedly revised but still remains inconclusive. This parasite has variable spore numbers within a sporophorous vesicle and has been assigned to the genera Glugea, Pleistophora, Stempellia, and Thelohania. We used electron microscopy and molecular evidence to resolve the previous taxonomic confusion and confirm its identification as Pleistophora mulleri. The life cycle of P. mulleri is described from the freshwater amphipod host Gammarus duebeni celticus. Infection appeared as white tubular masses within the abdominal muscle of the host. Light and transmission electron microscope examination revealed the presence of an active microsporidian infection that was diffuse within the muscle block with no evidence of xenoma formation. Paucinucleate merogonial plasmodia were surrounded by an amorphous coat immediately external to the plasmalemma. The amorphous coat developed into a merontogenetic sporophorous vesicle that was present throughout sporulation. Sporogony was polysporous resulting in uninucleate spores, with a bipartite polaroplast, an anisofilar polar filament and a large posterior vacuole. SSU rDNA analysis supported the ultrastructural evidence clearly placing this parasite within the genus Pleistophora. This paper indicates that Pleistophora species are not restricted to vertebrate hosts.
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We investigated the effects of temperature on transovarial transmission and feminisation by Nosema granulosis, a microsporidian sex ratio distorter of the brackish water amphipod Gammarus duebeni. There was no difference in parasite transmission efficiency to the F-1 eggs of infected females maintained under two temperature conditions, 5 and 10degreesC (89 and 86%, respectively). When F-1 individuals were screened as adults, the proportion infected was also similar at both temperatures (74 and 75%, respectively). However, transmission to the eggs of the F-2 generation was significantly reduced at low temperatures (61% at 5degreesC and 91% at 10degreesC). In addition, feminisation efficiency was reduced substantially at low temperatures; at 10degreesC, a calculated 85% of infected males were feminised, but at 5degreesC only 49% were feminised. This is the first evidence for incomplete feminisation and temperature-dependent transmission and feminisation by this sex ratio distorter. We examine the consequences for parasite spread and maintenance in natural populations using a model to predict parasite prevalence in large populations. Reduced feminisation at low temperatures impedes the spread of the parasite so that it attains a substantially lower frequency, or may even be excluded, from host populations. (C) 2002 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved.
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Pollinating fig wasps are often used to study sex ratio evolution in structured mating populations. Theory predicts a female-biased sex ratio, becoming less female biased as female (foundress) density increases. We used Liporrhopalum tentacularis to test two mechanisms of sex-ratio control when foundresses oviposit simultaneously: (1) foundresses facultatively adjust the number,of males in clutches, and (2) they produce the same number of males regardless of clutch size, which, given limited numbers of oviposition sites, would lead to increases in sex ratio with increasing density. We then examined whether foundresses,can oviposit sequentially into figs. When oviposition was simultaneous, brood composition indicated facultative adjustment, although sex ratios were more female biased, than predicted. Instead, foundresses appeared to adjust their sex ratio in response to both others ovipositing and their own fecundity. We also found that foundresses are able to oviposit completely sequentially, with those arriving second adjusting their sex ratio in response to the previous oviposition. Hence, pollinating wasps may fail to fit, the predictions of classical sex ratio theory because the conditions under which foundresses oviposit, and their responses to changes in such conditions, are more complex than once assumed. (C) 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.
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We screened a population of the brackish water crustacean Gammarus duebeni from the Isle of Cumbrae for the presence of vertically transmitted microsporidia. We compared 2 screening techniques; light microscopy and PCR-based detection using generic 16S rDNA microsporidian primers. Fifty percent of females from this population tested positive for vertically transmitted microsporidia. The PCR screen was 100% efficient in comparison with existing LM based screening. In addition, the PCR screen produced bands of 2 sizes suggesting that more than I species of microsporidian was present. Sequencing revealed 2 distinct species of vertically transmitted microsporidia; 33% of females were infected with the feminizer Nosema granulosis and 17% were infected with a new species which we provisionally designate Microsporidium sp. On the basis of sequence information, we developed a discriminatory PCR-RFLP test based oil MspI and HaeIII digests. This screen allows rapid detection and discrimination of vertically transmitted microsporidia in natural field populations. We applied the PCR-RFLP screen to a second G. duebeni population from the Isle of Man. This population also hosted these 2 parasite species. In total 45% of females harboured N. granulosis and 10% harboured Microsporidium sp. No dual-infected individuals were found in either population. The occurrence of 2 vertically transmitted parasites within a population has implications for our understanding of parasite-host relationships in the field and we discuss factors affecting the dynamics of parasite-parasite competition and coexistence.
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The microsporidia are obligate intracellular parasites which have diverse life cycles involving both horizontal and vertical transmission and parasitise a wide range of vertebrate and invertebrate hosts. In this paper we consider the life cycles and diversity of the microsporidia. We focus in particular on the relationship between parasite transmission and virulence and its implications for host-parasite coevolution. The use of horizontal and vertical routes of transmission varies between species and there is a strong link between transmission and virulence. Horizontal transmission is characterised by a high parasite burden and associated pathogenicity. In contrast, vertical transmission is characterised by low virulence, which has led to under-reporting of this important transmission route. Vertically transmitted microsporidia may also cause male killing or feminisation of their host, with implications for host population sex ratio and stability. Phylogenetic analysis shows that vertical transmission occurs in diverse branches of the Microspora. We find that there is evidence for vertical transmission in both vertebrate and invertebrate hosts and conclude that it is a common or possibly even ubiquitous transmission route within this phylum. (C) 2001 Editions scientifiques et medicales Elsevier SAS.
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The microsporidia are an ancient and diverse group of protists which have many unusual characteristics. These include prokaryotic-like 70s ribosomes, enclosed nuclear division, a lack of mitochondria and complex life cycles which frequently involve vertical transmission. This use of vertical transmission is unparalleled by other protists and is seen only among bacterial endosymbionts and sex ratio distorters and in host cell organelles. Transovarially transmitted microsporidia can have unusual and profound effects on host population sex ratios. We here consider the mechanisms of transovarial transmission and its implications for parasite evolution. We review parasite/host relationships and the evolution of virulence under transovarial transmission and consider the implications of these parasites for host ecology and evolution.
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Parasitic sex ratio distorters were artificially transferred within and between crustacean host species in order to study the effects of parasitism on host fitness and sex determination and to investigate parasite-host specificity. Implantation of Nosema sp, to uninfected strains of its Gammarus duebeni host resulted in an active parasite infection in the gonad of recipient females and subsequent transovarial parasite transmission. The young of artificially infected females were feminized by the parasite, demonstrating that Nosema sp. is a cause of sex ratio distortion in its host. In contrast, eve were unable to cross-infect Annadillidium vulgare with the feminizing microsporidian from G. duebeni or to cross-infect G. duebeni with the feminizing bacterium Wolbachia sp. from A. vulgare.
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Gammarid crustacea exhibit precopula mate guarding in which a male will carry a potential mate beneath his ventral surface, guarding her for several days until she moults and lays her eggs. I investigated the role of the calceoli (bulb-like structures on the second antennae) in mate assessment and precopula pairing in two Gammarus species by comparing the behaviour of males with and without calceoli. Removal of the calceoli had no effect on the pattern of size-assortative mating, nor did it reduce the number of contacts made per unit time between potential mates. However, males without calceoli reduced their assessment of potential mates, were less likely to guard a suitable female and guarded for a shorter period. These data support the hypothesis that calceoli are used during contact assessment to determine a female's intermoult period and hence suitability for guarding. (C) 1998 The Association for the Study of Animal Behaviour.
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The amphipod Gammarus duebeni harbours several species of vertically transmitted, feminizing microsporidian parasites. G. duebeni were collected from 3 localities in the UK. Animals from Budle Bay, Northumberland, were infected with Octosporea effeminans, and those from Millport, Isle of Cumbrae and Fenham Flats, Northumberland were infected with microsporidia of the genus Nosema. We derived expected distributions of parasites per host embryonic cell by modelling parasite transmission as a multitype, Galton-Watson branching process. Parasite prevalence (proportion of females infected) was significantly heterogeneous among localities. Parasite burden in zygotes was much higher for females infected with Nosema than in animals infected with O. effeminans. There was no significant difference between localities in the number of Nosema in the zygotes. Comparison of models and data from 64-cell host embryos showed that the distributions of parasites per cell were consistent with the hypothesis that sorting of parasites into daughter cells is biased for at least 1 cell lineage. Host embryos infected with O. effeminans could expect to contain a growing number of parasites in each cell generation within such biased cell lineages; similar estimates for Nosema predict a decline in the number of parasites per cell within a biased lineage. We discuss the possibility that the 2 species of parasite may be employing different strategies in order to ensure transmission to the next host generation.
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The crustacean Gammarus duebeni exhibits precopula mate guarding and size-assortative pairing, in which larger males tend to pair with larger females. Size-assortative pairing may result from sexual selection or natural selection (mechanical or loading constraints limiting the size of female that can be carried by the male). If loading constraints are important, large females should have lower pairing success than females of intermediate size as they will be less likely to encounter sufficiently large males capable of carrying them in precopula. We tested this hypothesis in a laboratory study. Female pairing success was dependent on size; however, the relationship was curvilinear: pairing success increased with size up to a point, but larger females suffered decreased pairing success. This supports the hypothesis that loading constraints play a part in structuring size-assortative pairing in this species. We found no evidence for size-related female resistance in structuring the pattern of pairing. We considered size-related pairing success with regard to environmental sex determination and parasitic sex-ratio distortion in G. duebeni. (C) 1997 The Association for the Study of Animal Behaviour.
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Environmental sex determination (ESD) permits adaptive sex choice under patchy environmental conditions, where the environment affects sex-specific fitness and where offspring can predict their likely adult status by monitoring an appropriate environmental cue. For Gammarus duebeni, an amphipod with ESD, it has been proposed that this flexible sex determination system is adaptive because males gain more from large size. Under ESD, young which are born earlier in the season become mostly males and, experiencing longer to grow, are therefore larger at breeding than females which are born later in the season. In order to test the hypothesis that ESD is adaptive for this species we investigated the relationship between size and fitness for both males and females, in a population of G. duebeni known to have ESD. We measured size related pairing success and fecundity, and used these two measures to calculate the relative fitness gains achieved through an increase in size for either sex. The fitness of both males and females increased with size, but males gained more from an increase in size than did females, throughout the breeding season. The data support the adaptive explanation for the evolution and maintenance of ESD in this species.
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Vertically transmitted parasites are transmitted from generation to generation of hosts usually via the host's gametes. Owing to gamete size dimorphism, the major transmission route is transovarial and selection (on the parasite) favours strategies which increase the relative frequency of the transmitting (female) host sex. These strategies impose unusual selection pressures on the host, and coevolution between hosts and vertically transmitted parasites has been implicated in speciation, in the evolution of symbiosis, and in the evolution of novel systems of host reproduction and sex determination. We review the evolutionary implications of vertically transmitted parasites in arthropods before focusing on strategies of transmission of a parasitic sex ratio distorter in Gammarus duebeni. The efficiency of parasite transmission to new hosts is a key factor underlying the relationship between vertically transmitted parasites and their hosts. Vertically transmitted parasites must overcome 2 bottlenecks in order to ensure successful infection of future host generations: first, transmission from adult to gamete; and secondly, transmission to the germ-line of the infected host. We investigate these 2 processes with regard to transovarial transmission by a microsporidian parasite in Gammarus duebeni. Parasite transmission from adult to eggs is highly efficient, with 96% of eggs of infected mothers inheriting the infection, whereas transmission to germ-line within infected embryos is relatively inefficient (72%). We measure parasite distribution between cells of developing embryos, and use these distributions to infer possible mechanisms of parasite transmission to germ-line. Parasite distribution within the embryo is dependent on host cell lineage, and is not consistent with unbiased segregation between daughter cells. These results indicate that parasites segregate together at host cell division, and may reflect a strategy of differential segregation to the host germ-line. We consider alternative parasite strategies at the cell-level in terms of their evolutionary implications.
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