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.     

Physiological and ecological hosts of Popenaias popeii (Bivalvia: Unionidae): laboratory studies identify more hosts than field studies

1. Freshwater mussels are critically endangered in North America, making it important to understand their environmental requirements at all life stages. As glochidia (larvae), they attach to fish hosts where they undergo substantial mortality, making this transition important in their life cycle. Larval host fish requirements have typically been described using data from laboratory infestations to determine suitable hosts. 2. Laboratory infestations circumvent many natural barriers that prevent infestation of physiologically compatible fishes by mussel larvae. While such methods are invaluable for identifying ‘physiological hosts,’ they cannot fully describe realised ‘ecological hosts’ in the field. 3. We studied Popenaias popeii in the Black River in New Mexico, because it is of conservation concern and it is the only mussel species present, facilitating identification of glochidial infestation. To explore the difference between physiological hosts and ecological hosts, we conducted a 3‐year field study of fishes infested by P. popeii glochidia. 4. Substantially fewer fish species were infested by P. popeii in the wild (10 of 20 observed) than had been identified as physiological hosts in laboratory trials (24 of 31). We combined data on fish abundance, proportion of fish hosts infested (prevalence) and the number of glochidia per fish (intensity) and identified three fish species that probably contributed substantially more to mussel recruitment by carrying more glochidia than other host species. 5. Similarities in behaviour among these fishes allowed us to hypothesise routes of infestation, such as benthos‐feeding by catostomids, that allow glochidia to infest these hosts at higher rates than other suitable hosts. Overall, this approach provides a method of quantifying the relative importance of different species of host fish in the mussel lifecycle.     

Evolution of active host-attraction strategies in the freshwater mussel tribe Lampsilini (Bivalvia: Unionidae)

Most freshwater mussels (Bivalvia: Unionoida) require a host, usually a fish, to complete their life cycle. Most species of mussels show adaptations that increase the chances of glochidia larvae contacting a host. We investigated the evolutionary relationships of the freshwater mussel tribe Lampsilini including 49 of the approximately 100 extant species including 21 of the 24 recognized genera. Mitochondrial DNA sequence data (COI, 16S, and ND1) were used to create a molecular phylogeny for these species. Parsimony and Bayesian likelihood topologies revealed that the use of an active lure arose early in the evolution of the Lampsiline mussels. The mantle flap lure appears to have been the first to evolve with other lure types being derived from this condition. Apparently, lures were lost independently in several clades. Hypotheses are discussed as to how some of these lure strategies may have evolved in response to host fish prey preferences.     

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.     

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.     

Dispersal limitation of unionid mussels and implications for their conservation

1. Freshwater unionid mussels are a highly imperilled group. Their dispersal abilities depend on the availability and the movement of host fish on which their parasitic mussel larvae develop. 2. We examined the relationship between the dispersal abilities of unionid mussels and their conservation status on a regional (SW Ontario) scale and their distribution and abundance on a catchment scale (Sydenham River, SW Ontario) by determining host specificity and estimating the dispersal abilities of mussels on fish from a review of the literature. 3. On the regional scale, we found that mussels with the most precarious conservation status relied on host fish with short movement distances, whereas vulnerable and more secure mussel species had host fish with 2–3 orders of magnitude larger movement distances. We were not able to detect a clear pattern on the catchment scale. 4. Our results suggest that limited dispersal by host fish affects the abundance and distribution of unionid mussels and ultimately their conservation status on a regional scale. Information on dispersal limitations because of differences in host fish communities should be included in conservation and management decisions to ensure connectivity and maintain functioning mussel metacommunities.     

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

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Life history traits and abundance can predict local colonisation and extinction rates of freshwater mussels

1. A critical need in conservation biology is to determine which species are most vulnerable to extinction. Freshwater mussels (Bivalvia: Unionacea) are one of the most imperilled faunal groups globally. Freshwater mussel larvae are ectoparasites on fish and depend on the movement of their hosts to maintain connectivity among local populations in a metapopulation. 2. I calculated local colonisation and extinction rates for 16 mussel species from 14 local populations in the Red River drainage of Oklahoma and Texas, U.S. I used general linear models and AIC comparisons to determine which mussel life history traits best predicted local colonisation and extinction rates. 3. Traits related to larval dispersal ability (host infection mode, whether a mussel species was a host generalist or specialist) were the best predictors of local colonisation. 4. Traits related to local population size (regional abundance, time spent brooding) were the best predictors of local extinction. The group of fish species used as hosts by mussels also predicted local extinction and was probably related to habitat fragmentation and host dispersal abilities. 5. Overall, local extinction rates exceeded local colonisation rates, indicating that local populations are becoming increasingly isolated and suffering an ‘extinction debt’. This study demonstrates that analysis of species traits can be used to predict local colonisation and extinction patterns and provide insight into the long‐term persistence of populations.     

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.     

An invasive species reverses the roles in a host-parasite relationship between bitterling fish and unionid mussels

The impact of multiple invading species can be magnified owing to mutual facilitation--termed 'invasional meltdown'--but invasive species can also be adversely affected by their interactions with other invaders. Using a unique reciprocal host-parasite relationship between a bitterling fish (Rhodeus amarus) and unionid mussels, we show that an invasive mussel reverses the roles in the relationship. Bitterling lay their eggs into mussel gills, and mussel larvae parasitize fish. Bitterling recently colonized Europe and parasitize all sympatric European mussels, but are unable to use a recently invasive mussel, Anodonta woodiana. The parasitic larvae of A. woodiana successfully develop on R. amarus, whereas larvae of European mussels are rejected by bitterling. This demonstrates that invading species may temporarily benefit from a coevolutionary lag by exploiting evolutionarily naive hosts, but the resulting relaxed selection may facilitate its exploitation by subsequent invading species, leading to unexpected consequences for established interspecific relationships.     

Effects of augmentative releases of the coccinellid, Adalia bipunctata, and of insecticide treatments in autumn on the spring population of aphids of the genus Dysaphis in apple orchards

The impact of augmentative releases of indigenous predators and insecticide applications to control the autumn aphid forms of the genus Dysaphis (Homoptera: Aphididae), major pest insects on apple trees, was assessed in one-year field experiments in Switzerland. Eggs and larvae of the two-spot ladybird beetle Adalia bipunctata (L.) (Coleoptera: Coccinellidae) were released on 4-year old apple trees in various numbers at five different dates in autumn 1998 when sexuales of the aphids were present. Additionally, Pyrethrum HP was sprayed at the same five dates to compare the effectiveness of these augmentative releases to a commonly applied insecticide. Augmentative releases of larvae before mid-October significantly prevented the deposition of overwintering eggs by aphids of the genus Dysaphis and consequently reduced the number of hatched fundatrices in spring, 1999. There was a significant negative functional response among the number of released coccinellid larvae in autumn 1998 and the number of observed fundatrices on apple trees in spring 1999. Applications of Pyrethrum HP before mid-October were more effective than augmentative releases of larvae of A. bipunctata. The release of coccinellid eggs had no impact on the number of fundatrices of the genus Dysaphis in the next spring because they did not hatch due to bad weather conditions. The weather conditions in autumn seemed to have an impact on the autumn migration of the winged aphids back to their primary host. The prevention of egg deposition of aphids in autumn is a promising control strategy and deserves further exploration for practical use.     

Past and present patterns of connectivity among populations of four cryptic species of freshwater mussels Velesunio spp. (Hyriidae) in central Australia

We examined genetic structure and levels of connectivity among subpopulations within each of four cryptic species belonging to the freshwater mussel genus Velesunio. We used allozymes and a fragment of the mitochondrial cytochrome c oxidase I gene to examine genetic variation in populations from isolated waterholes, belonging to four major inland drainages in eastern Australia. Based on evidence from other invertebrates in the region we predicted that, in each species, we would find evidence of historical connectivity among populations from different drainages. This was clearly not the case, as for the two species that occurred in more than one drainage there was evidence of both current and past restriction to gene flow. Moreover, given the potential for extensive dispersal of these mussels through the river systems during flood times via their fish hosts, we predicted low levels of genetic variation among populations from waterholes in the same drainage. Contrary to our expectations, all four species showed some evidence of restricted gene flow among waterholes within drainages. This suggests that either (a) mussel larvae are not produced during flood times, when their fish hosts would be free to move between waterholes, or (b) mussel larvae are attached to their hosts at these times, but the fish movement is limited between waterholes.     

Coextirpation of host–affiliate relationships in rivers: the role of climate change,water withdrawal,and host‐specificity

The role of climate‐related disturbances on complex host–affiliate relationships remains understudied, largely because affiliate species vary in host use and are often differentially susceptible to disturbance relative to their hosts. Here we report the first set of host–affiliate species–discharge relationships (SDR) in freshwater and examine how anticipated shifts in water availability (flow) will impact coextirpations. We used SDR for freshwater mussels and fish across 11 regions (over 350 rivers) in the continental United States that we coupled to future water availability (2070) to model mussel and fish coextirpations. We also used river‐specific host–affiliate matrices (presence–absence) to evaluate how host‐specificity (mean number of hosts used by an affiliate) and host‐overlap (extent to which affiliates share hosts) relate to extirpation vulnerability. We found that the strength and predictability of SDR models vary geographically and that mussels were more susceptible to flow alterations than fish. These patterns of extirpations were strongest in the southeast where: (1) flow reductions are expected to be greatest; (2) more species are lost per unit flow; (3) and more mussels are expected to be lost per unit of fish. We also found that overall mussel losses associated with reduction in habitat (water availability) were greater than those associated with loss of fish hosts which we assumed to be a function of host redundancy. These findings highlight the utility of SDR as a tool for conservation efforts but they also demonstrate the potential severity of reductions in mussel and fish richness as consequence of climate change and water use. Mussels provide key ecosystem services but face multiple pronged attacks from reductions in flow, habitat, and fish hosts. These losses in biodiversity and ecosystem functions can translate into major effects on food webs and nutrient recycling.     

Dispersal abilities of riverine freshwater mussels influence metacommunity structure

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The role of local adaptation in shaping fish‐mussel coevolution

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The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe

Several freshwater mussel species represent some of the most problematic invasive species and have considerably altered ecosystems worldwide. Their invasion potential has been partially attributed to their free-living larvae, which have a high dispersal capability. We investigated the invasion potential of Anodonta (Sinanodonta) woodiana, a species of East Asian unionid mussel established worldwide despite having an obligatory parasitic stage (glochidium), which must encyst on host fish. The invasion success of A. woodiana has been attributed to the success of worldwide introductions of its sympatric fish hosts. We experimentally found, however, that A. woodiana is a broad host generalist, which can complete its development on all eight fish species tested, both coinvasive and native. Subsequently, we used a data on the occurrence and relative abundance of potential hosts in river habitats in the Czech Republic to project scenarios of the effect of host availability on A. woodiana invasion. We found that host availability does not constitute a major limit for A. woodiana to colonise most aquatic habitats in Central Europe. In addition, we investigated seasonal dynamics of A. woodiana reproduction and did not detect any limitations of its reproduction by ambient water temperatures typical of a Central European lowland river. Consequently, we predict that A. woodiana may further increase the speed and range of its invasion and we discuss possible consequences to native habitats and communities, especially to the endangered species of unionid mussels.     

The impact of land use on the mussel Margaritifera margaritifera and its host fish Salmo trutta

Today, land use impacts a major proportion of all streams. Here, landscape features in corridors along streams and water chemical factors were analyzed in relation to recruitment of the threatened freshwater pearl mussel (Margaritifera margaritifera) and its host fish the brown trout (Salmo trutta). Mussel recruitment and trout density were negatively related to forest clear-cuts. Mussel recruitment was negatively related to water color and turbidity. Therefore, the threats to the mussel may be severe, as low mussel recruitment may be caused by direct effects on the juvenile mussels and indirect effects on the host fish. High proportions of lakes and ponds were found to be positive for recruitment and for trout, and deciduous forest was positively related to trout. The combination of investigations at different scales at the landscape level and at in-stream levels may be applicable to find threats to other threatened species. The results indicate that forestry activities may negatively affect recruitment of freshwater pearl mussels and its host fish. Reductions of forestry activities and the retaining of intact quantity and quality of the riparian zones next to streams, both for the mussel and its host fish may be important conservation measures to restore freshwater pearl mussel populations.     

Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators

Trematodes amplify asexually in their snail intermediate hosts, resulting in the potential release of hundreds to thousands of free-living cercariae per day for the life of the snail. The high number of cercariae released into the environment undoubtedly increases the probability of transmission. Although many individual cercariae successfully infect another host in their life cycle, most fail. Factors that prevent successful transmission of cercariae are poorly understood. Microcrustaceans and fish have been observed to eat cercariae of some species, although the possibility that predation represents a significant source of mortality for cercariae has been largely unexplored. We tested the cercariophagic activity of several freshwater invertebrates on Ribeiroia ondatrae, a trematode that causes limb deformities in amphibians. Individuals of potential predators were placed into wells of multiwell plates with 10-15 cercariae, and numbers of cercariae remaining over time were recorded and compared with numbers in control wells that contained no predators. Of the species tested, Hydra sp., damselfly (Odonata, Coenagrionidae) larvae, dragonfly (Odonata, Libellulidae), larvae, and copepods (Cyclopoida) consumed cercariae. In some cases, 80-90% of the cercariae offered to damselfly and dragonfly larvae were consumed within 10 min. In most cases, predators continued to consume cercariae at the same average rates when offered cercariae together with individuals of an alternate prey item. Hydra sp. ate fewer cercariae in these trials. Our findings suggest the need for field and laboratory studies to further explore the effects of predators on transmission of R. ondatrae to amphibian larvae. In addition, the results suggest that conservation of the biodiversity and numbers of aquatic predators may limit adverse impacts of trematode infections in vertebrate hosts.     

High levels of multiple paternity in a spermcast mating freshwater mussel

Multiple paternity is an important characteristic of the genetic mating system and common across a wide range of taxa. Multiple paternity can increase within‐population genotypic diversity, allowing selection to act on a wider spectre of genotypes, and potentially increasing effective population size. While the genetic mating system has been studied in many species with active mating behavior, little is known about multiple paternity in sessile species releasing gametes into the water. In freshwater mussels, males release sperm into the water, while eggs are retained and fertilized inside the female (spermcast mating). Mature parasitic glochidia are released into the water and attach to the gills of fish where they are encapsulated until settling in the bottom substrate. We used 15 microsatellite markers to detect multiple paternity in a wild population of the freshwater pearl mussel (Margaritifera margaritifera). We found multiple paternity in all clutches for which more than two offspring were genotyped, and numbers of sires were extremely high. Thirty‐two sires had contributed to the largest clutch (43 offspring sampled). This study provides the first evidence of multiple paternity in the freshwater pearl mussel, a species that has experienced dramatic declines across Europe. Previous studies on other species of freshwater mussels have detected much lower numbers of sires. Multiple paternity in freshwater pearl mussels may be central for maintaining genetic variability in small and fragmented populations and for their potential to recover after habitat restoration and may also be important in the evolutionary arms race with their fish host with a much shorter generation time.     

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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