The role of local adaptation in shaping fish‐mussel coevolution

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An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.     

Mechanisms and impact of differential fouling of the zebra mussel Dreissena polymorpha on different unionid bivalves

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Ecological correlates and phylogenetic signal of host use in North American unionid mussels

Mussels in the order Unionoida comprise ～75% of the world’s freshwater bivalve species and are free-living apart from a brief larval stage that parasitizes fish. We investigated the relationships among species of North American unionid mussels and their known host fishes from a macroevolutionary perspective to test whether and how ecological and evolutionary factors correlate with patterns of host use. A subset of 69 mussel species was chosen based on data availability regarding their fish host repertoires, phylogenetic relationships, and ecology. Despite the brevity of their parasitic life stages, the mussels conformed to the right-skewed distribution of host specificity typical of parasitic taxa, in which most species are specialists and a few are generalists. Phylogenetic least squares regression models identified affinity for low-gradient and riffle habitats, and colonization of post-glacial watersheds as the best predictors for the number of fish host species per mussel. However, the second-best model identified citation number as a predictor of the number of hosts, implying that many mussel–host interactions still remain to be identified. A Multiple Regression Mantel test was performed to identify factors associated with the proportion of hosts shared between pairs of mussel species. Range overlap, citations, genetic distance, and similarity in host infection strategy were significantly correlated with the proportion of hosts shared, yet total variation as explained by the best model was low (R²?=?0.14). There was evidence of a topological association between mussels and their hosts (P?=?0.001) and a significant phylogenetic signal of host specificity (λ?=?0.81, P?=?0.003), indicating closely related mussels that overlap in range are more likely to be competing for hosts. Our results provide an initial macroevolutionary framework for studying the evolution of host infection strategies in these mussels but also highlights gaps still remaining in our fundamental ecological knowledge of this endangered clade.     

Avoidance of host resistance in the oviposition-site preferences of rose bitterling

A contemporary outcome of dynamic host–parasite coevolution can be driven by the adaptation of a parasite to exploit its hosts at the population and species levels (parasite specialisation) or by local host adaptations leading to greater host resistance to sympatric parasite populations (host resistance). We tested the predominance of these two scenarios using cross-infection experiments with two geographically distant populations of the rose bitterling, Rhodeus ocellatus, a fish brood parasite of freshwater mussels, and four populations of their mussel hosts (two Anodonta woodiana and two Unio douglasiae populations) with varying degrees of geographic sympatry and local coexistence. Our data support predictions for host resistance at the species level but no effect of local coexistence between specific populations. Rhodeus ocellatus showed a preference for allopatric host populations, irrespective of host species. Host mussel response, in terms of ejection of R. ocellatus eggs, was stronger in the more widespread and abundant host species (A. woodiana) and this response tended to be higher in sympatric populations. These outcomes provide support for the importance of host resistance in bitterling oviposition-site decisions, demonstrating that host choice by R. ocellatus is adaptive by minimizing egg ejections. These findings imply that R. ocellatus, and potentially other bitterling species, may benefit from exploiting novel hosts, which may not possess appropriate adaptive responses to parasitism.     

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

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Population-specific responses to an invasive species

Predicting the impacts of non-native species remains a challenge. As populations of a species are genetically and phenotypically variable, the impact of non-native species on local taxa could crucially depend on population-specific traits and adaptations of both native and non-native species. Bitterling fishes are brood parasites of unionid mussels and unionid mussels produce larvae that parasitize fishes. We used common garden experiments to measure three key elements in the bitterling–mussel association among two populations of an invasive mussel (Anodonta woodiana) and four populations of European bitterling (Rhodeus amarus). The impact of the invasive mussel varied between geographically distinct R. amarus lineages and between local populations within lineages. The capacity of parasitic larvae of the invasive mussel to exploit R. amarus was higher in a Danubian than in a Baltic R. amarus lineage and in allopatric than in sympatric R. amarus populations. Maladaptive oviposition by R. amarus into A. woodiana varied among populations, with significant population-specific consequences for R. amarus recruitment. We suggest that variation in coevolutionary states may predispose different populations to divergent responses. Given that coevolutionary relationships are ubiquitous, population-specific attributes of invasive and native populations may play a critical role in the outcome of invasion. We argue for a shift from a species-centred to population-centred perspective of the impacts of invasions.     

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.     

No evidence for host specialization or host-race formation in the European bitterling (Rhodeus amarus), a fish that parasitizes freshwater mussels

Coevolutionary relationships between parasites and hosts can elevate the rate of evolutionary changes owing to reciprocal adaptations between coevolving partners. Such relationships can result in the evolution of host specificity. Recent methodological advances have permitted the recognition of cryptic lineages, with important consequences for our understanding of biological diversity. We used the European bitterling (Rhodeus amarus), a freshwater fish that parasitizes unionid mussels, to investigate host specialization across regions of recent and ancient sympatry between coevolving partners. We combined genetic data (12 microsatellite and 2 mitochondrial markers) from five populations with experimental data for possible mechanisms of host species recognition (imprinting and conditioning). We found no strong evidence for the existence of cryptic lineages in R. amarus, though a small proportion of variation among individuals in an area of recent bitterling–mussel association was statistically significant in explaining host specificity. No other measures supported the existence of host‐specific lineages. Behavioural data revealed a weak effect of conditioning that biased behavioural preferences towards specific host species. Host imprinting had no effect on oviposition behaviour. Overall, we established that populations of R. amarus show limited potential for specialization, manifested as weak effects of host conditioning and genetic within‐population structure. Rhodeus amarus is the only species of mussel‐parasitizing fish in Europe, which contrasts with the species‐rich communities of bitterling in eastern Asia where several host‐specific bitterling occur. We discuss costs and constraints on the evolution of host‐specific lineages in our study system and more generally.     

The zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) impacts European bitterling (<Emphasis Type="Italic">Rhodeus amarus</Emphasis>) load in a host freshwater mussel (<Emphasis Type="Italic">Unio pictorum</Emphasis>)

The European bitterling, Rhodeus amarus, is a non-indigenous fish species in British fresh waters. It lays its eggs in unionid mussels which themselves are vulnerable to fouling by the non-indigenous zebra mussel, Dreissena polymorpha. Observations from an unmanipulated natural system showed that only 27% of zebra mussel-fouled Unio pictorum hosted bitterling, while 47% of unfouled U. pictorum hosted bitterling. We conducted a field experiment in the River Great Ouse catchment, Cambridgeshire, England in May–June 2007 and 2008 to quantify the impact of zebra mussels on bitterling load in host mussels. Zebra mussel-fouled unionids were significantly less likely to host bitterling than unfouled unionids. The number of unionids hosting bitterling did not differ significantly whether the zebra mussels fouling the unionid were alive or dead. Bitterling appeared to discriminate against zebra mussel-fouled unionids less as the 2007 breeding season advanced, potentially because preferred unfouled unionids had a higher bitterling load, and were therefore relatively lower quality hosts than at the start of the breeding season.     

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.     

A multi‐basin approach determines variability in host fish suitability for unionids in tributaries of the Laurentian Great Lakes

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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.     

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.     

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.     

Dispersal abilities of riverine freshwater mussels influence metacommunity structure

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Population genetic structure of a rare unionid (<Emphasis Type="Italic">Lampsilis cariosa</Emphasis>) in a recently glaciated landscape

The yellow lampmussel (Lampsilis cariosa) is a rare unionid species in need of conservation, as it is declining throughout most of its Atlantic slope range in North America. Because freshwater mussels rely on a fish host for dispersal of their larvae, barriers to the movement of hosts, such as habitat fragmentation by dams, may indirectly affect population genetic structure. We used microsatellite loci to assess genetic variation for L. cariosa within and among three river drainages in the northern part of its range, which emerged from glaciation only ∼ ∼8–10 kya. Despite this relatively recent emergence, significant differences were observed among populations both within and among drainages, possibly because low effective population sizes meant that populations of these mussels achieved drift-migration equilibrium rapidly following glaciation. L. cariosa individuals could be assigned to their own drainages with 89.3% accuracy. Among-population differences were modest, however, in comparison to differences observed in another study of rare mussels south of the recently glaciated region. L. cariosa populations exhibited significant isolation by distance, but there was no additional variation explained by the number, size, or age of intervening dams. An understanding of mussel population genetic structure provides information, useful for conservation planning, on patterns of isolation and connectivity among populations.     

Reproductive Ecology and Host Utilization of Four Sympatric Bitterling (Acheilognathinae,Cyprinidae) in a Lowland Reach of the Harai River in Mie,Japan

Bitterling are fishes that use freshwater mussels for oviposition. The reproductive ecology and pattern of mussel utilization of four sympatric species of bitterling, Acheilognathus rhombeus, A. tabira tabira, Tanakia lanceolata, and T. limbata, were investigated in a lowland river with seven sympatric mussel species. Three bitterling species are spring spawners with overlapping spawning seasons. A. rhombeus is an autumn-spawning species and is temporally isolated in its reproduction from the other species. Ovipositor length during oviposition of T. limbata and T. lanceolata was short, while those of A. tabira tabira and A. rhombeus were long. Most T. limbata inhabited near-shore areas, whereas the two other spring-spawning species were distributed across the entire river. All bitterling species used Inversidens brandti, Obovalis omiensis and Inversiunio jokohamensis as spawning hosts, but not the other mussel species available. T. lanceolata, A. tabira tabira and A. rhombeus showed spawning preferences for O. omiensis and I. brandti. However, T. limbata did not show clear preferences for any of the mussel species they used. A. t. tabira showed a significant preference for large I. brandti in offshore areas, while the other spring-spawning bitterling showed a preference for mussels inshore. These results are discussed in the context of reproductive resource partitioning.     

Chasing a changing climate: Reproductive and dispersal traits predict how sessile species respond to global warming

Aim

Studies of species' range shifts have become increasingly relevant for understanding ecology and biogeography in the face of accelerated global change. The combination of limited mobility and imperilled status places some species at a potentially greater risk of range loss, extirpation or extinction due to climate change. To assess the ability of organisms with limited movement and dispersal capabilities to track shifts associated with climate change, we evaluated reproductive and dispersal traits of freshwater mussels (Unionida), sessile invertebrates that require species‐specific fish for larval dispersal.

Location

North American Atlantic Slope rivers.

Methods

To understand how unionid mussels may cope with and adapt to current and future warming trends, we identified mechanisms that facilitated their colonization of the northern Atlantic Slope river basins in North America after the Last Glacial Maximum. We compiled species occurrence and life history trait information for each of 55 species, and then selected life history traits for which ample data were available (larval brooding duration, host fish specificity, host infection strategy, and body size) and analysed whether the trait state for each was related to mussel distribution in Atlantic Slope rivers.

Results

Brooding duration (p < .01) and host fish specificity (p = .02) were significantly related to mussel species distribution. Long‐term brooders were more likely than short‐term brooders to colonize formerly glaciated rivers, as were host generalists compared to specialists. Body size and host infection strategy were not predictive of movement into formerly glaciated rivers (p > .10).

Main conclusions

Our results are potentially applicable to many species for which life history traits have not been well‐documented, because reproductive and dispersal traits in unionid mussels typically follow phylogenetic relationships. These findings may help resource managers prioritize species according to climate change vulnerability and predict which species might become further imperilled with climate warming. Finally, we suggest that similar trait‐based decision support frameworks may be applicable for other movement limited taxa.

     

Invasive zebra mussel (Dreissena polymorpha) threatens an exceptionally large population of the depressed river mussel (Pseudanodonta complanata) in a postglacial lake

1. Freshwater mussels are in decline worldwide, with the depressed river mussel Pseudanodonta complanata being one of the rarest and most endangered species in Europe. Invasive mussels are suspected to be an important factor of decline, but there is little information on their interaction with native species.
2. This study analyzed densities, depth distribution, and individual sizes and weights in one of the largest known populations of P. complanata in Europe in relation to the co‐occurring invasive zebra mussel Dreissena polymorpha and other mussel species, using a systematic transect analysis.
3. Pseudanodonta complanata was the dominant unionid species in Lake Siecino reaching densities of up to 26 ind/m², with half of the specimens found at a water depth of 2.0–4.0 m. Densities were highest on sandy substrates in areas of underwater currents. In contrast, 67% of native Unio tumidus were found at depths < 1 m, indicating different habitat preference.
4. In the study area, 91% of P. complanata, 92% of U. tumidus, and all Anodonta individuals were fouled by D. polymorpha. The dreissenid:unionid mass ratio (mean ± SD; maximum) was 0.43 ± 0.56; 4.22 and 0.86 ± 1.87; 8.76 in P. complanata and U. tumidus, respectively. Pseudanodonta complanata fouled with D. polymorpha were impaired in their anchoring capability and had shell deformations potentially affecting shell closing and filtration activity. Fouling intensity was negatively correlated with unionid density, potentially leading to accelerated population declines.
5. The observed adverse effects of invasive zebra mussels on the depressed river mussel and the difficulties in eradicating established populations of invasive mussels suggest that D. polymorpha should be considered a serious threat to P. complanata. Therefore, the further spread of zebra mussels into habitats with native unionids needs to be avoided by all means.