Nestedness in riverine mussel communities: patterns across sites and fish hosts

The pattern of nestedness, where species present in depauperate locations are subsets of species present in locations with higher species diversity, is often found in ecological communities. Mussel communities examined in four rivers in the upper Tennessee River basin appeared significantly nested. Mussel species distributions were mostly unrelated to differences in immigration and only weakly related to downstream direction, giving some indication of structuring by differences in extinction. Mussel species distributions were not related to the number of fish species used as hosts for mussel larvae. Mussel species were more likely to overlap on common fish hosts; however, the host‐use matrix was not nested – groups of mussel species used different sets of host fish species in a pattern that appeared phylogenetically related. Sites with high fish host abundance may support high mussel diversity by promoting the survival of mussel species that are less able to attract and infect hosts. Thus, nestedness in freshwater mussel communities may be driven by the array of host fish resources, combined with differences in species’ abilities to use fish hosts. An understanding of the nested pattern in this region can aid conservation of this imperiled fauna.     

Cross-resistance of largemouth bass to glochidia of unionid mussels

We tested whether host fish that acquired resistance to glochidia of one mussel species were cross-resistant to glochidia of other species. Largemouth bass (Micropterus salmoides) were primed with 4-5 successive infections of glochidia of Lampsilis reeveiana. The percentage of attached glochidia that survived and transformed to the juvenile stage (transformation success) was compared between primed fish and na?ve controls. Transformation success of L. reeveiana, Lampsilis abrupta, Villosa iris, and Utterbackia imbecillis was significantly lower on primed fish (37.8%, 43.5%, 67.0%, and 13.2%, respectively) than on control fish (89.0%, 89.7%, 90.0%, and 22.2% respectively). Immunoblotting was used to analyze the binding of serum antibodies from primed fish with glochidia proteins. Antibodies bound to glochidia proteins of similar molecular weight from L. reeveiana and L. abrupta. Bound proteins of V. iris differed in molecular weight from those of the Lampsilis species. There was no binding to specific glochidia proteins of U. imbecillis or Strophitus undulatus. Our results indicate that host-acquired resistance can extend across mussel genera and subfamilies and might involve both specific and nonspecific mechanisms. Understanding the specificity of acquired resistance of hosts to glochidia could enhance understanding of the evolutionary and ecological relationships between mussels and their host fishes.     

The role of local adaptation in shaping fish‐mussel coevolution

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Direct impact of invasive bivalve (<Emphasis Type="Italic">Sinanodonta woodiana</Emphasis>) parasitism on freshwater fish physiology: evidence and implications

Direct and potentially damaging effects of invasive alien species can remain unnoticed or insufficiently quantified, resulting in a lack of stakeholder awareness. We report for the first time that parasitic larvae (glochidia) of the invasive freshwater mussel Sinanodonta (Anodonta) woodiana (Unionidae, Bivalvia) cause an unexpected reduction in the condition factor of parasitized native fish species. The reduction in the body mass and condition factor of experimentally infested European chub (Squalius cephalus) was associated with changes in several physiological parameters measured in host fish plasma. Ion concentrations (potassium, chloride) and enzymes activities (aspartate aminotransferase, alanine aminotransferase, lactate dehydrogenase, alkaline phosphatase) were significantly affected; hence, the results reveal the complex effects of non-native glochidia on the homeostasis of the individually tested fish. Changes in host physiology and condition status were recorded also in environmentally relevant infestation intensities (mean of 3.02 ± 0.51 glochidia g^?1). Despite intensive concern regarding the negative biodiversity and ecosystem impacts of the adult stage of S. woodiana among conservationists and natural resource managers, potential effects of its larval stage have been neglected until now. Because fish hosts are an obligatory part of the reproductive cycle of the mussel and the main vector for spreading, documentation of this direct and easily quantifiable impact on fish has great potential to influence the key community of stakeholders in fisheries and aquaculture sectors and to serve as a strong motivating factor for invasive species control. We argue for more careful consideration of potential multiple life-stage effects of S. woodiana and of other invasive alien species as well, as different life stages can have highly specific impacts and corresponding relevance for key stakeholder groups.     

Parasite‐induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal

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紫黑翼蚌钩介幼虫寄主鱼的人工筛选及寄生包囊形成观察

选取16种鱼类, 对紫黑翼蚌(Potamilus alatus)钩介幼虫寄主鱼进行人工筛选试验, 结果表明: 仅在淡水石首鱼(Aplodinotus grunniens)上获得变态发育的稚蚌, 寄生变态率为(49.6±9.4)%, 但是过量寄生将导致淡水石首鱼的死亡。除眼斑拟石首鱼(Soiaenops ocellatus)外, 寄生在其他14种淡水鱼类均不可能实现钩介幼虫的变态。进一步扫描电镜观察显示: 钩介幼虫可在与淡水石首鱼同科的眼斑拟石首鱼鳃丝寄生并形成完整的包囊, 且在大规格鱼体形成包囊的速度明显快于幼鱼。但在寄生和淡水低渗双重胁迫下, 眼斑拟石首鱼出现极高的死亡率, 提示应进一步开展淡化驯养以提高眼斑拟石首鱼寄生后的成活率。其中黄颡鱼(Pelteobagrus fulvidraco)、小口黑鲈(Micropterus dolomieu) 、蓝鲶(Ictalurus furcatus)寄生后1—2d内脱落的幼虫几乎全部死亡, 推测3种鱼体中可能存在紫黑翼蚌幼虫的致死因子。综合研究表明: 紫黑翼蚌是目前发现对寄主鱼选择性最为专一的蚌类, 而眼斑拟石首鱼具有作为替代寄主鱼的潜能。     

Encapsulation of attached ectoparasitic glochidia larvae of freshwater mussels by epithelial tissue on fins of naive and resistant host fish

To metamorphose into juveniles and subsequently mature into adults, the glochidia larvae of freshwater mussels in the order Unionoida must temporarily parasitize the gills, fins, or other external structures of fish. Once attached to the fish, the glochidium is encapsulated by host fish epithelial tissue. The migration of epithelial cells of the bluegill sunfish Lepomis macrochirus over glochidia of Utterbackia imbecillis was examined by time-lapse video microscopy, and the morphology was examined by scanning electron microscopy. Initially, the leading edge epithelial cells migrating over the larvae became rounded and the cells moved as a sheet until the attached glochidium was completely covered. Cyst formation on host fish that had been repeatedly exposed to mussel larvae was significantly delayed and morphologically irregular compared to that on na?ve fish. Cyst formation on other species of fish that are less successful as hosts was examined. In general, it took longer for glochidia to become encapsulated on these less suitable potential hosts. The delay and irregularities in cyst formation on resistant fish and nonhost fish species may result in increased mortality and reduced success of metamorphosis of glochidia.     

THE BITTERLING–MUSSEL COEVOLUTIONARY RELATIONSHIP IN AREAS OF RECENT AND ANCIENT SYMPATRY

Host–parasite relationships are often characterized by the rapid evolution of parasite adaptations to exploit their host, and counteradaptations in the host to avoid the costs imposed by parasitism. Hence, the current coevolutionary state between a parasite and its hosts is predicted to vary according to the history of sympatry and local abundance of interacting species. We compared a unique reciprocal coevolutionary relationship of a fish, the European bitterling (Rhodeus amarus) and freshwater mussels (Unionidae) between areas of recent (Central Europe) and ancient (Turkey) sympatry. Bitterling parasitize freshwater mussels by laying their eggs in the gills of mussel and, in turn, mussel larvae (glochidia) parasitize the fish. We found that all bitterling from both regions avoided one mussel species. Preferences among other mussel species tended to be related to local mussel abundance rather than duration of sympatry. Individual fish were not consistent in their oviposition choices, precluding the evolution of host‐specific lineages. Mussels were demonstrated to have evolved strong defenses to bitterling parasitism in the area of ancient sympatry, but have no such defenses in the large areas of Europe where bitterling are currently invasive. Bitterling avoided glochidia infection irrespective of the duration of sympatry.     

Trophic relationships between the larvae of two freshwater mussels and their fish hosts

Freshwater mussels of the order Unionoida have life cycles that include larval attachment to and later metamorphosis on suitable host fishes. Information on the trophic relationship between unionoid larvae and their host fishes is scarce. We investigated the trophic interaction between fish hosts and encysted larvae of two species of freshwater mussels, Margaritifera margaritifera and Unio crassus, using stable isotope analyses of larvae and juvenile mussels as well as of host fish gill and muscle tissues before and after infestation. Due to different life histories and durations of host‐encystment, mass and size increase in M. margaritifera during the host‐dependent phase were greater than those of U. crassus. δ¹³C and δ¹⁵N signatures of juvenile mussels approached isotopic signatures of fish tissues, indicating a parasitic relationship between mussels and their hosts. Shifts were more pronounced for M. margaritifera, which had a five‐fold longer host‐dependent phase than U. crassus. The results of this study suggest that stable isotope analyses are a valuable tool for characterizing trophic relationships and life history strategies in host–parasite systems. In the case of unionoid mussels, stable isotopic shifts of the larvae are indicative of the nutritional versus phoretic importance of the host.     

Influence of cortisol on the attachment and metamorphosis of larval Utterbackia imbecillis on bluegill sunfish (Lepomis macrochirus)

The larvae of unionid freshwater mussels (i.e., glochidia) undergo a parasitic stage requiring their attachment to the external epithelia of fish hosts, where they metamorphose into free-living juveniles. We describe the physiological effects in bluegill sunfish (Lepomis macrochirus) of infection with glochidia from the paper pondshell (Utterbackia imbecillis). Glochidia accumulation on bluegill increased dramatically at concentrations of 2000 glochidia liter(-1) and above, reaching a maximum attachment density of about 30 glochidia g(-1) fish at 4000 glochidia liter(-1). Plasma cortisol was the most sensitive indicator of biological effect to glochidial exposure, increasing significantly in hosts exposed to 2000 glochidia liter(-1) or greater. Glochidia were 31% more likely to undergo successful juvenile metamorphosis when attached to bluegill with elevated plasma cortisol, largely due to the enhanced survivorship of these larvae during the first 48 h after infection. We tested the hypothesis that glochidial attachment and juvenile metamorphosis were stimulated directly by plasma cortisol in fish hosts. Bluegill were given an intraperitoneal injection of cortisol, then infected with 1000 glochidia liter(-1) at 48 h after hormone supplementation. Cortisol-injected fish had a 42% increase in the number of attached glochidia g(-1) fish and a 28% increase in larval metamorphosis compared to sham-injected and control fish. We provide evidence that cortisol enhances glochidial metamorphosis on hosts by improving the retention of attached glochidia. This study gives insights into the influence of host physiology on glochidial attachment and juvenile mussel transformation.     

Acquired resistance of bluegill sunfish Lepomis macrochirus to glochidia larvae of the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) after multiple infections

The effects of multiple infections on the host-parasite relationship between bluegill sunfish (Lepomis macrochirus) and parasitic glochidial larvae of the freshwater mussel Utterbackia imbecillis were examined. Na?ve, young-of-the-year bluegills were infected with glochidia and placed in individual observation chambers. Each day, water was drained from each chamber and the numbers of dead glochidia, live glochidia, partially metamorphosed glochidia, and fully metamorphosed juvenile mussels were counted. The same fishes were infected a total of 4 times. After 2 infections, the fish began to exhibit evidence of acquired resistance to glochidia. During the third and fourth infections, this resistance was clearly evidenced by the marked increase in the percentage of dead and live glochidia shed during the first 5 days of the infection and by the significant decrease in the success of metamorphosis. The total number of glochidia that successfully attached to the fish decreased significantly during the fourth infection relative to the first. The number of larvae attached to the host fish was positively correlated with the size of the fish during the first infection but was negatively correlated during all subsequent infections. Variance to mean ratios indicated that larvae were aggregated among host fishes during the infections. This study has important implications in propagation and conservation efforts of this endangered group of organisms.     

A review on the “in vitro” culture of freshwater mussels (Unionoida)

Many Unionoida are considered to be extinct, endangered, or of special concern. These bivalves have complex life cycle stages that limit successful culture. In nature, the larvae (glochidia) of these bivalves must successfully parasitize a host (mainly fish) in order to metamorphose into juveniles. The two artificial methods used to obtain juvenile freshwater mussels in laboratory are either by induced attachment to host fish or by in vitro culture of glochidia. This article is focused on the in vitro method that represents a novel and alternative process to fish infestation, offering the ability to obtain larger numbers of juveniles without the need for host fishes and reducing the overall costs of propagation. In vitro culture requires a medium which fulfills the nutritional needs of each glochidia species and avoids microbial contamination. Recently, this methodology has presented excellent results with survival and transformation rates up to 94% using host fish plasma. High efficiencies on growth, and survival rates (84%) of juvenile freshwater bivalve Hyriopsis myersiana (Lea, 1856) up to 120 days were obtained when reared in adequate recirculating aquacultural systems using a very specific diet. More research is still needed to demonstrate successful propagation, mainly concerning the media nutritional composition to increase glochidia transformation and juvenile quality.     

Mantle displays of freshwater mussels elicit attacks from fish

1. Gravid females of some North American freshwater mussel species (Bivalvia: Unionidae) display highly modified mantle margins and other reproductive structures which mimic small fish, terrestrial insects, or aquatic macro-invertebrates. We report the responses of fish to these lures, based on the results of laboratory encounters between the following pairs of displaying mussels and fishes: Lampsilis cardium and Micropterus coosae; L . perovalis and M . coosae; and Villosa nebulosa and Percina nigrofasciata . In all three encounters, the lures elicited attacks from fish.
2. Encounters between Lampsilis spp. and M. coosae resulted in gill infestations of the fish by larval mussels, which are obligate parasites on fish. An encounter between V . nebulosa and P . nigrofasciata did not result in infestation.
3. The use of these lures to attract fish may greatly increase the chances of parasite/host encounters and may also reduce the chances of infestation of unsuitable hosts.     

Do individual Activity Patterns of Brown Trout (Salmo trutta) alter the Exposure to Parasitic Freshwater Pearl Mussel (Margaritifera margaritifera) Larvae?

The hypothesis that interindividual differences in the activity of brown trout alter the exposure to parasitic freshwater pearl mussel glochidia was tested in a Swedish stream. Wild yearling brown trout (N = 103) were caught, individually tagged for identification and scored for open‐field activity during standardized laboratory tests in June. Fifty gravid freshwater pearl mussels were relocated to the stream, where after the trout were released back into the stream. The fish were recaptured in October (N = 35), checked for glochidia encystment (infested individuals: n = 6) and re‐scored for open‐field activity traits. Swimming velocity during the test was higher in fish infected with glochidia, suggesting that high activity could increase their exposure to glochidia. Potentially, as metabolism rate and ventilation rate typically increase with activity, elevated activity may lead to an increased likelihood of glochidia passing over the gills. This novel finding suggests that glochidia infestation is non‐random and that the behaviour of the host fish can influence the likelihood of glochidia infestation.     

Early life stages of exotic gobiids as new hosts for unionid glochidia

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A delayed effect of the aquatic parasite <Emphasis Type="Italic">Margaritifera laevis</Emphasis> on the growth of the salmonid host fish <Emphasis Type="Italic">Oncorhynchus masou masou</Emphasis>

Parasitic species often have detrimental effects on host growth and survival. The larvae of the genus Margaritifera (Bivalvia), called glochidia, are specialist parasites of salmonid fishes. Previous studies have reported negligible influences of the parasite on their salmonid hosts at natural infection levels. However, those studies focused mainly on their instantaneous effects (i.e., during the parasitic period). Given the time lag between physiological and somatic responses to pathogen infections, the effect of glochidial infection may become clearer during the post-parasitic period. Here, we examined whether the effect of glochidial infections of Margaritifera laevis on its salmonid host Oncorhynchus masou masou would emerge during the post-parasitic period. We performed a controlled aquarium experiment and monitored fish growth at two time intervals (i.e., parasitic and post-parasitic periods) to test this hypothesis. Consistent with previous observations, the effects of glochidial infection were unclear in the middle of the experiment (day 50; parasitic period). However, even with a natural glochidial load (48 glochidia per fish), we found a significant reduction in growth rates of infected fish in the extended period of the experiment (day 70; post-parasitic period). Our results suggest that examining only instantaneous effects may provide misleading conclusions about mussel–host relationships.     

Parasite transfer from crustacean to fish hosts in the Lübeck Bight,SW Baltic Sea

Four helminth parasites out of 19 species found in the Lübeck Bight, Baltic Sea, were chosen for investigations on the transfer from invertebrate to small-sized fish hosts: larvae of the tapewormsSchistocephalus sp. andBothriocephalus sp. (Cestoda) living in planktonic copepods as primary hosts;Podocotyle atomon (Digenea) andHysterothylacium sp. (Nematoda) were found in benthic crustaceans, especiallyGammarus spp. These hosts were the prey of 3 gobiid fishes,Gobiusculus flavescens (feeding mainly on plankton),Pomatoschistus minutus (preferring benthos), andP. pictus (feeding more on plankton than benthos). Because the fishes selected smaller sizes of crustaceans, they ingested all stages of the copepods but only the smaller-sized groups of gammarids which were often less infested by parasites. In order to evaluate the probability for a fish to be parasitized by a helminth, an infestation potential index (IP) was calculated.Podocotyle atomon andHysterothylacium sp. revealed an IP which was far lower in gobies than expected when the prevalences of the previous hosts were taken into consideration. The IP of tapeworm larvae was mainly influenced by the feeding pressure of the gobiid predators, which might change with developmental stage and season. It is concluded that parasite transfer to the next host decreases when sizes of prey and predator differ only moderately. This mechanism can reduce the numbers of parasites transferred to less suitable or wrong hosts.     

Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts,aggregation, prevalence,infestation intensity,and infracommunities

Streblidae and Nycteribiidae are families of bloodsucking flies that parasitize bats exclusively. We studied the community of these flies in a Cerrado area in the Central-West Brazil. We captured 708 bats over 17 nights from October 2012 to March 2013. Forty-five per cent of the hosts were parasitized by 836 specimens of bat flies of 22 species. The most abundant flies were Trichobius joblingi on Carollia perspicillata, followed by Megistopoda aranea on Artibeus planirostris, and Strebla guajiro on C. perspicillata. All bat flies showed a high level of specificity for their hosts. Trichobius joblingi was the bat fly with the highest prevalence (80%) and mean intensity of infestation (3.5) on hosts with a representative sample size (n > 20). This result is likely related to the type of roosting (cavity) used by C. perspicillata, primary host of this fly species. Anoura caudifer hosted the largest infracommunities (n = 7). However, most bats were parasitized by a single fly species, suggesting a pattern in infestations. The aggregation index was high, indicating an unequal occurrence in parasite infestations. The majority of hosts were infested by few or no flies and few hosts were highly infested, showing a negative binomial distribution.     

Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers

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Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts

The ectoparasitic mite, Varroa destructor, shifted host from the eastern honeybee, Apis cerana, to the western honeybee, Apis mellifera. Whereas the original host survives infestations by this parasite, they are lethal to colonies of its new host. Here, we investigated a population of A. cerana naturally infested by the V. destructor Korea haplotype that gave rise to the globally invasive mite lineage. Our aim was to better characterize traits that allow for the survival of the original host to infestations by this particular mite haplotype. A known major trait of resistance is the lack of mite reproduction on worker brood in A. cerana. We show that this trait is neither due to a lack of host attractiveness nor of reproduction initiation by the parasite. However, successful mite reproduction was prevented by abnormal host development. Adult A. cerana workers recognized this state and removed hosts and parasites, which greatly affected the fitness of the parasite. These results confirm and complete previous observations of brood susceptibility to infestation in other honeybee host populations, provide new insights into the coevolution between hosts and parasites in this system, and may contribute to mitigating the large‐scale colony losses of A. mellifera due to V. destructor.