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.     

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.     

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

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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.     

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.     

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.     

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.     

Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis>) in northern Europe

Freshwater pearl mussels (Margaritifera margaritifera) are among the most critically threatened bivalve molluscs worldwide. An understanding of spatial patterns of genetic diversity is crucial for the development of integrative conservation strategies. We used microsatellites to study the genetic diversity and differentiation of 14 populations of M. margaritifera in central Sweden, an area which was described as a major secondary contact zone in postglacial colonisation for other species. Genetic diversity of Swedish pearl mussel populations was much greater than in central and southern Europe but similar to the genetic diversity observed in the northeastern portion of their European range. Genetic differentiation among populations was pronounced but to a large extent independent from present-day drainage systems. The complex patterns of genetic diversity and differentiation in pearl mussel seem to be strongly influenced by the species’ high degree of specialisation and extraordinary life history strategy which involves facultative hermaphrodism and an obligatory encystment stage on a host fish. Genetic drift effects and anthropogenic disturbances resulting in reduction of population size and loss of connectivity are less pronounced in northern pearl mussel populations compared to those in central and southern Europe.     

Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion

1. Freshwater mussels (Order Unionoida) are the most imperiled faunal group in North America; 60% of described species are considered endangered or threatened, and 12% are presumed extinct. Widespread habitat degradation (including pollution, siltation, river channelization and impoundment) has been the primary cause of extinction during this century, but a new stress was added in the last decade by the introduction of the Eurasian zebra mussel, Dreissena polymorpha , a biofouling organism that smothers the shells of other molluscs and competes with other suspension feeders for food. Since the early 1990s, it has been spreading throughout the Mississippi River basin, which contains the largest number of endemic freshwater mussels in the world. In this report, we use an exponential decay model based on data from other invaded habitats to predict the long-term impact of D. polymorpha on mussel species richness in the basin.
2. In North American lakes and rivers that support high densities (>3000 m⁻²) of D. polymorpha , native mussel populations are extirpated within 4–8 years following invasion. Significant local declines in native mussel populations in the Illinois and Ohio rivers, concomitant with the establishment of dense populations of D. polymorpha , suggest that induced mortality is occurring in the Mississippi River basin.
3. A comparison of species loss at various sites before and after invasion indicates that D. polymorpha has accelerated regional extinction rates of North American freshwater mussels by 10-fold. If this trend persists, the regional extinction rate for Mississippi basin species will be 12% per decade. Over 60 endemic mussels in the Mississippi River basin are threatened with global extinction by the combined impacts of the D. polymorpha invasion and environmental degradation.     

Divergence of ovipositor length and egg shape in a brood parasitic bitterling fish through the use of different mussel hosts

Bitterling fishes deposit their eggs on the gills of living mussels using a long ovipositor. We examined whether ovipositor length (OL) and egg shape correlated with differences in host mussel species in the family Unionidae among populations of the tabira bitterling (Acheilognathus tabira) in Japan. Bitterling populations that use mussels in the sub-family Anodontinae possessed longer ovipositors and more elongated eggs than those using mussels of Unioninae, as expected from the difference in host size between the sub-families (anodontine mussels are larger than unionine mussels). Based on a robust phylogeny of A. tabira populations, we demonstrated that the evolution of both OL and egg shape were correlated with host differences, but not with each other, suggesting that these traits have been selected for independently. Our study demonstrates how adaptive traits for brood parasitism may diverge with host shift due to different host availability and/or interspecific competition for hosts.     

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.     

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.

     

Overfishing in the Baltic Sea basin in Russia,its impact on the pearl mussel,and possibilities for the conservation of riverine ecosystems in conditions of high anthropogenic pressure

In recent studies nine populations of the freshwater pearl mussel have been described in the Baltic Sea basin in Russia. They are very scarce, although the condition of their habitats seems to be rather good. Overfishing of the host fish is a limiting factor for them. The number of salmon has decreased by at least 100 times over the past 200 years. Such a scale of decline tends to be hidden over time, and estimation of the normal conditions of the salmon–pearl mussel ecosystem becomes problematic. A significant increase in the number of salmon is necessary to prevent extinction of pearl mussels. Effective protected areas appear to be the only possibility for conservation of the pearl mussels and its host fish species.     

Remnant Populations and Plant Functional Traits in Abandoned Semi-Natural Grasslands

Although semi-natural grasslands in Europe are declining there is often a time delay in the local extinction of grassland species due to development of remnant populations, i.e., populations with an extended persistence despite a negative growth rate. The objectives of this study were to examine the occurrence of remnant populations after abandonment of semi-natural grasslands and to examine functional traits of plants associated with the development of remnant populations. We surveyed six managed semi-natural grasslands and 20 former semi-natural grasslands where management ceased 60–100 years ago, and assessed species response to abandonment, assuming a space-for-time substitution. The response of species was related to nine traits representing life cycle, clonality, leaf traits, seed dispersal and seed mass. Of the 67 species for which data allowed analysis, 44 species declined after grassland abandonment but still occurred at the sites, probably as remnant populations. Five traits were associated with the response to abandonment. The declining but still occurring species were characterized by high plant height, a perennial life form, possession of a perennial bud bank, high clonal ability, and lack of dispersal attributes promoting long-distance dispersal. Traits allowing plants to maintain populations by utilizing only a part of their life cycle, such as clonal propagation, are most important for the capacity to develop remnant populations and delay local extinction. A considerable fraction of the species inhabiting semi-natural grasslands maintain what is most likely remnant populations after more than 60 years of spontaneous succession from managed semi-natural grasslands to forest.     

Dispersal abilities of riverine freshwater mussels influence metacommunity structure

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Does mobility explain variation in colonisation and population recovery among stream fishes?

1. Colonisation and population recovery are crucial to species persistence in environmentally variable ecosystems, but are poorly understood processes. After documenting movement rates for several species of stream fish, we predicted that this variable would influence colonisation rates more strongly than local abundance, per cent occupancy, body size and taxonomic family. We also predicted that populations of species with higher movement rates would recover more rapidly than species with lower movement rates and that assemblage structure would change accordingly. 2. To test these predictions, we removed fishes from a headwater and a mainstem creek in southwest Virginia and monitored colonisation over a 2‐year period. Using an information–theoretic approach, we evaluated the relative plausibility of 15 alternative models containing different combinations of our predictor variables. Our best‐supported model contained movement rate and abundance and was 41 times more likely to account for observed patterns in colonisation rates than the next‐best model. Movement rate and abundance were both positively related to colonisation rates and explained 88% of the variation in colonisation rates among species. 3. Population recovery, measured as the per cent of initial abundance restored, was also positively associated with movement rate. One species recovered within 3 months, most recovered within 2 years, but two species still had not recovered after 2 years. Despite high variation in recovery, the removal had only a slight impact on assemblage structure because species that were abundant in pre‐removal samples were also abundant in post‐removal samples. 4. The significance of interspecific variation in colonisation and recovery rates has been underappreciated because of the widely documented recovery of stream fish assemblages following fish kills and small‐scale experimental defaunations. Our results indicate that recovery of the overall assemblage does not imply recovery of each component species. Populations of species that are rare and less mobile will recover more slowly and will be more vulnerable to extinction in systems where chemical spills, hydrological alteration, extreme droughts and other impacts are frequent.     

Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling

Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.     

Population genetics and phylogeography of freshwater mussels in North America, Elliptio dilatata and Actinonaias ligamentina (Bivalvia: Unionidae)

Extrinsic and intrinsic forces combined shape the population structure of every species differently. Freshwater mussels are obligate parasites to a host fish during a juvenile stage (glochidia). Elliptio dilatata (ED) and Actinonaias ligamentina (AL) are co-occurring freshwater mussel taxa with similar North American distribution and share some potential host fish. Using mitochondrial DNA, we determined the genotypes of 190 + individuals from collection sites in at least two tributaries in the Lake Erie and Ohio River watersheds, along with the Ouachita and Strawberry rivers in the southeast. Both species had followed a stepping-stone model of dispersal, with greater pairwise genetic structure among collection sites of ED. Also, phylogeographical analysis for ED found significant geographical structuring of haplotype diversity. Overall, within-population variation increased significantly from north to south, with low genetic diversity in the Strawberry River. We calculated significant among-population structure for both species (ED: Phi(ST) = 0.62, P < 0.001; AL: Phi(ST) = 0.16, P < 0.001). Genetic analysis identified the Ouachita River as an area of significant reproductive isolation for both species. Results for AL indicated dispersal into northern areas from two genetically distinct glacial refugia, where results for ED indicated dispersal followed by low gene flow in northern areas. The conservation strategies for mussels that co-occur in the same 'bed' could be species specific. Species such as ED have management units on the population scale, where AL has a more homogeneous genetic structure across its range.     

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.     

Which plant traits predict species loss in calcareous grasslands with extinction debt?

Aim Habitat loss and degradation pose a major threat to biodiversity, which can result in the extinction of habitat characteristic species. However, many species exhibit a delayed response to environmental changes because of the slow intrinsic dynamics of populations, resulting in extinction debt. We assess directly the changes in habitat characteristic species composition by comparing historical (1923) and current inventories in highly fragmented grasslands. We aim to characterize the species that constitute extinction debt in European calcareous grasslands. Location Europe, Estonia, 59–60° N, 24–25° E. Methods We related eleven life‐history traits and selected habitat preferences to local extinctions of populations in grasslands where extinction debt has been largely paid. Traits were chosen to describe species dispersal and persistence abilities and were quantified from databases. Results The studied grasslands have lost 90% of their area and 30% of their characteristic plant populations in 90 years. Species more prone to local population extinction were characterized by shorter life span, self‐pollination, a lack of clonal growth, fewer seeds per shoot, lower average height, lower soil nitrogen preference and higher requirements for light, indicating a limited ability to tolerate the range of changes in biotic and abiotic conditions of the sites. Locally extinct populations were also characterized by wind‐dispersed seeds, lower seed weight and lower terminal velocity of seeds, suggesting that species strategies for long‐distance dispersal are not favoured in highly fragmented landscapes. Thus, both increased habitat isolation and decreased habitat quality are important in determining local population extinction. Main conclusions Populations more prone to local extinction were characterized by a number of life‐history traits, demonstrating a greater extinction risk for species with poorer abilities for local persistence and competition. Our results can be applied to less degraded grasslands where the extinction debt is not yet paid to determine those species most susceptible to future extinction.