Predator‐induced morphological defences in two invasive dreissenid mussels: implications for species replacement

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Fouling of European freshwater bivalves (Unionidae) by the invasive zebra mussel (Dreissena polymorpha)

1. The zebra mussel (Dreissena polymorpha) is well known for its invasive success and its ecological and economic impacts. Of particular concern has been the regional extinction of North American freshwater mussels (Order Unionoida) on whose exposed shells the zebra mussels settle. Surprisingly, relatively little attention has been given to the fouling of European unionoids. 2. We investigated interspecific patterns in fouling at six United Kingdom localities between 1998 and 2008. To quantify the effect on two pan‐European unionoids (Anodonta anatina and Unio pictorum), we used two measures of physiological status: tissue mass : shell mass and tissue glycogen content. 3. The proportion of fouled mussels increased between 1998 and 2008, reflecting the recent, rapid increase in zebra mussels in the U.K. Anodonta anatina was consistently more heavily fouled than U. pictorum and had a greater surface area of shell exposed in the water column. 4. Fouled mussels had a lower physiological condition than unfouled mussels. Unlike tissue mass : shell mass ratio, tissue glycogen content was independent of mussel size, making it a particularly useful measure of condition. Unio pictorum showed a stronger decline in glycogen with increasing zebra mussel load, but had a broadly higher condition than A. anatina at the time of study (July). 5. Given the high conservation status and important ecological roles of unionoids, the increased spatial distribution and fouling rates by D. polymorpha in Europe should receive more attention.     

Factors affecting trematode infection rates in freshwater mussels

Mussels are intermediate hosts of digenean trematodes, but determinants of these infections remain unknown. To address this problem, we collected duck mussels Anodonta anatina in eighteen lakes from northeastern Poland and examined how mussel age, sex, and the encrustation with zebra mussels Dreissena polymorpha and environmental conditions in lakes influenced infection rates. We also assessed parasitic preferences to host gonads and hepatopancreas and the impact of parasites on female fertility. Mussels were infected with Rhipidocotyle campanula and Phyllodistomum sp. Infection rates were higher in older and female mussels but were unrelated to the biomass of encrusting D. polymorpha and the trophy, thermal conditions, and Ca²⁺ availability. Parasites occupied gonads more often than hepatopancreas. Infected females were less likely to carry glochidia and incubated fewer glochidia. We suggest that the risk of infection by digenean trematodes increases with the amount of water processed by filter-feeding hosts and/or that parasites actively seek hosts which can provide them with abundant resources. This mechanism explains why parasites more often occupied older and female mussels and targeted their gonads. Future research on trematode-mussel interactions should integrate knowledge on different elements of the complex trematode life cycles, including effects of higher-order hosts such as fish.     

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

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Temperature but not ocean acidification affects energy metabolism and enzyme activities in the blue mussel,Mytilus edulis

1. In mosaic marine habitats, such as intertidal zones, ocean acidification (OA) is exacerbated by high variability of pH, temperature, and biological CO₂ production. The nonlinear interactions among these drivers can be context‐specific and their effect on organisms in these habitats remains largely unknown, warranting further investigation.
2. We were particularly interested in Mytilus edulis (the blue mussel) from intertidal zones of the Gulf of Maine (GOM), USA, for this study. GOM is a hot spot of global climate change (average sea surface temperature (SST) increasing by >0.2°C/year) with >60% decline in mussel population over the past 40 years.
3. Here, we utilize bioenergetic underpinnings to identify limits of stress tolerance in M. edulis from GOM exposed to warming and OA. We have measured whole‐organism oxygen consumption rates and metabolic biomarkers in mussels exposed to control and elevated temperatures (10 vs. 15°C, respectively) and current and moderately elevated P _CO2 levels (~400 vs. 800 µatm, respectively).
4. Our study demonstrates that adult M. edulis from GOM are metabolically resilient to the moderate OA scenario but responsive to warming as seen in changes in metabolic rate, energy reserves (total lipids), metabolite profiles (glucose and osmolyte dimethyl amine), and enzyme activities (carbonic anhydrase and calcium ATPase).
5. Our results are in agreement with recent literature that OA scenarios for the next 100–300 years do not affect this species, possibly as a consequence of maintaining its in vivo acid‐base balance.

     

Does lake eutrophication support biological invasions in rivers? A study on Dreissena polymorpha (Bivalvia) in lake–river ecotones

The zebra mussel (Dreissena polymorpha) has all traits required to effectively colonize the aquatic environment and consequently reduce the diversity of native bivalves. We hypothesized that the zebra mussel chooses lake outlets characterized by medium current velocity and good food conditions. Here, we analyzed differences between bivalve abundances in lake outlets with varying environmental conditions such as the Carlson Index (trophy status), depth, width, current velocity, bed vegetation coverage, and type of bottom substrate. The results showed that the zebra mussel inhabits outlets that provide food (high trophy outlets) and have a mineral bed and a medium current velocity (ca. 0.2–0.3 m/s). The following main factors seem to be favorable for colonizing such outlets: (1) easy access to high amounts of food due to the increased density of the suspension drifting from the lake and (2) easy transport of the zebra mussel larvae from the lake to the downstream. The zebra mussel larvae drifting with the current may colonize the downstream. An increase in lake trophy may indirectly cause an increase in biological invasions in rivers.     

Population dynamics of little brown bats (Myotis lucifugus) at summer roosts: Apparent survival,fidelity, abundance,and the influence of winter conditions

1. White‐nose syndrome (WNS) has caused the death of millions of bats, but the impacts have been more difficult to identify in western North America. Understanding how WNS, or other threats, impacts western bats may require monitoring other roosts, such as maternity roosts and night roosts, where bats aggregate in large numbers.
2. Little brown bats (Myotis lucifugus) are experiencing some of the greatest declines from WNS. Estimating survival and understanding population dynamics can provide valuable data for assessing population declines and informing conservation efforts.
3. We conducted a 5‐year mark–recapture study of two M. lucifugus roosts in Colorado. We used the robust design model to estimate apparent survival, fidelity, and abundance to understand population dynamics, and environmental covariates to understand how summer and winter weather conditions impact adult female survival. We compared the fidelity and capture probability of M. lucifugus between colonies to understand how bats use such roosts.
4. Overwinter survival increased with the number of days with temperatures below freezing (β > 0.100, SE = 0.003) and decreased with the number of days with snow cover (β < −0.40, SE < 0.13). Adult female fidelity was higher at one maternity roost than the other. Overwinter and oversummer adult female survival was high (>0.90), and based on survival estimates and fungal‐swabbing results, we believe these populations have yet to experience WNS.
5. Recapture of M. lucifugus using antennas that continuously read passive integrated transponder tags allows rigorous estimation of bat population parameters that can elucidate trends in abundance and changes in survival. Monitoring populations at summer roosts can provide unique population ecology data that monitoring hibernacula alone may not. Because few adult males are captured at maternity colonies, and juvenile males have low fidelity, additional effort should focus on understanding male M. lucifugus population dynamics.

     

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.

     

Sexual,habitat‐constrained and parasite‐induced dimorphism in the shell of a freshwater mussel (Anodonta anatina,Unionidae)

Intraspecific trends in freshwater mussel (unionoid) shells that are consistently associated with differences in the mussels' sex and/or parasitic infestation can potentially be used to reconstruct sex ratios or parasitic levels of modern and ancient unionoid populations. In contrast to morphological patterns within mammal species, such dimorphic trends within unionoid species are, however, poorly understood. This study investigates, for the first time, to what extent sex, trematode infection and indirect habitat effects determine shell morphology in the freshwater mussel Anodonta anatina. Three of the five study populations displayed significant sexual shell width dimorphism. Here, shells of females were significantly wider than males, probably as a result of altered shell growth to accommodate marsupial gills. In two of these populations, female shells were additionally significantly thinner than those of males, which could be a result of resource depletion by offspring production. Two other A. anatina populations showed no significant dimorphic patterns, and our results indicate that this interpopulational difference in the degree of sexual dimorphism may reflect the overarching effect of habitat on morphology. Thus, populations in the most favourable habitats exhibit faster growth rates, attain larger maximum sizes and produce more offspring, which results in more swollen gills and consequently more inflated shells of gravid females compared to less fecund populations. None of the populations showed any evidence for sexual dimorphism in overall size, growth rate, sagittal shape and density of shells. In addition to sexual dimorphisms, infestation by bucephalid trematode parasites (Rhipidocotyle sp.) significantly altered sagittal and lateral shell shape of A. anatina in one of the populations, with infected specimens growing wider and more elongated. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Why do Argos satellite tags stop relaying data?

1. Satellite tracking of animals is very widespread across a range of marine, freshwater, and terrestrial taxa. Despite the high cost of tags and the advantages of long deployments, the reasons why tracking data from tags stop being received are rarely considered, but possibilities include shedding of the tag, damage to the tag (e.g., the aerial), biofouling, battery exhaustion, or animal mortality.
2. We show how information relayed via satellite tags can be used to assess why tracking data stop being received. As a case study to illustrate general approaches that are broadly applicable across taxa, we examined data from Fastloc‐GPS Argos tags deployed between 2012 and 2019 on 78 sea turtles of two species, the green turtle (Chelonia mydas) and the hawksbill turtle (Eretmochelys imbricata).
3. Tags transmitted for a mean of 267 days (SD = 113 days, range: 26–687 days, median = 251 days). In 68 of 78 (87%) cases, battery failure was implicated as the reason why tracking data stopped being received. Some biofouling of the saltwater switches, which synchronize transmissions with surfacing, was evident in a few tags but never appeared to be the reason that data reception ceased.
4. Objectively assessing why tags fail will direct improvements to tag design, setup, and deployment regardless of the study taxa. Assessing why satellite tags stop transmitting will also inform on the fate of tagged animals, for example, whether they are alive or dead at the end of the study, which may allow improved estimates of survival rates.

     

Seasonal effects of zebra mussels on littoral nitrogen transformation rates in Gull Lake, Michigan, U.S.A.

• 1 Zebra mussels (Dreissena polymorpha) are successful colonisers of lake littoral habitats and they interact strongly with littoral benthos. Previous research suggests that localised areas colonised by zebra mussels may be hotspots of nitrogen (N) cycling.
• 2 The effects of zebra mussels on nitrification and denitrification rates were examined approximately every other month for 1 year in Gull Lake, Michigan, U.S.A. Littoral sediment was collected from an area free of zebra mussels and distributed into shallow trays; rocks colonised with zebra mussels were placed in half of the trays, while uncolonised rocks were placed in the remaining trays. After an incubation period of 6–8 weeks in the lake, sediment and zebra mussels were collected from the trays, replaced with new sediment and zebra mussels, and placed in the lake for the next interval. In the laboratory, sediment nitrification and denitrification rates were measured for each tray.
• 3 Sediment nitrification rates did not increase in the presence of zebra mussels; instead nitrification rates were sensitive to changes in water temperature and increased with increasing exchangeable sediment ammonium. In contrast, denitrification rates increased in sediment trays with zebra mussels in the winter when nitrate (NO₃⁻) availability was high and when Chara did not grow in the trays.
• 4 Sediment denitrification was NO₃⁻‐limited in all seasons, regardless of zebra mussel treatment. However, sediment in the presence of zebra mussels responded less to NO₃⁻ addition, suggesting that NO₃⁻ limitation of denitrification can be reduced by zebra mussel activity. Zebra mussels have a seasonally variable impact on sediment denitrification rates, and this may translate into altered seasonal patterns of N cycling in localised areas of lakes where they are particularly abundant.

     

The growth of juvenile native mussels (Elliptio complanata) in lakes varies with sediment characteristics and site exposure

1. Unionid mussels are among the largest and longest-lived freshwater invertebrates and can play an important role in these ecosystems. They are also one of the most endangered groups of organisms. The juvenile stage is a particularly vulnerable part of mussel life history and is one of the most poorly known.
2. I compared the growth of young Elliptio complanata at 17 nearshore sites, in shallow (polymictic) and stratified lake basins, along gradients of sediment characteristics and site exposure (effective fetch). At each site, the growth of six to 14 small (20–68 mm) mussels collected on the sediment surface was measured, using internal growth lines. The growth of very young endobenthic mussels (22–40 mm) was also measured on four to six mussels at each of two sites.
3. Juveniles spend several years in the sediments, and I found that during this period growth is not constant but declines rapidly with age. Shifts in δ¹⁵N signatures suggest that juveniles change their habitat use towards a more planktonic baseline around the time of maturation, when they reach a length of 30–50 mm. Identical δ¹³C signatures in juveniles and adults suggest that both rely on food of planktonic origin, whether deposited or suspended.
4. The growth of juvenile mussels varies in a complex but predictable manner with sediment characteristics and wind-driven physical forces. Growth was highest in fine sediments with low organic content, in highly organic but coarse sediments, and in protected nearshore areas with low effective fetch. Interestingly, I also found high growth rates at exposed nearshore areas with fine sediments, suggesting that areas where bottom topography creates a refuge from currents and waves may provide particularly good conditions for the early growth of juvenile mussels.
5. Some parts of the shoreline may be more important than others for native mussel populations, and if we can identify those, they may warrant additional protection.

     

The influence of pre‐settlement and early post‐settlement processes on the adult distribution and relative dominance of two invasive mussel species

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The effects of flow and stream characteristics on the variation in freshwater mussel growth in a Southeast US river basin

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Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha

Freshwater fouling invertebrate zebra mussels (Dreissena polymorpha) harbor a diverse population of microorganisms in the Great Lakes of North America. Among the indigenous microorganisms, selective species are opportunistic pathogens to zebra mussels. Pathogenicity to zebra mussels by opportunistic bacteria isolated from the mussels was investigated in this study. Among the more than 30 bacteria isolated from temperature-stressed mussels, Aeromonas media, A. veronii, A. salmonicida subsp. salmonicida, and Shewanella putrefaciens are virulent pathogens to juvenile zebra mussels. Inoculation of a bacterial concentration of A. media, A. salmonicida subsp. salmonicida and S. putrefaciens at 10⁷ cells per zebra mussel resulted in 100% mortality within 5 days, and only 64.9% for A. veronii. In contrast, mortality was less than 12.3% following inoculation of a sterile phosphate buffer solution as a control. In addition, mortality was dependent on the size of the pathogen population used in inoculation and the incubation temperature, indicating the close relationship between the bacterial population and subsequent death. On the mussel tissue, a dense microbial population was evident from the moribund mussels viewed with Scanning Electron Microscope (SEM). Opportunistic bacteria invaded and destroyed the D. polymorpha tissue after 7 days of incubation when the bacterial inoculation was larger than 10⁵ per zebra mussel. Our results suggest that mussels are reservoirs of opportunistic pathogenic microorganisms to aquatic organisms and humans and a better understanding of the microbial ecology of the mussels will provide insights to the possible health hazards from these microorganisms.     

Predation by the invasive American signal crayfish, Pacifastacus leniusculus Dana, on the invasive zebra mussel, Dreissena polymorpha Pallas: the potential for control and facilitation

Non-indigenous crayfish often have major ecological impacts on invaded water bodies, and have contributed to the decline of native crayfish species throughout Europe. The American signal crayfish, Pacifastacus leniusculus, is the most widespread invasive crayfish in Great Britain, where the zebra mussel, Dreissena polymorpha, is similarly an invasive pest species. The potential for the American signal crayfish to regulate zebra mussel populations was investigated through a series of laboratory experiments. Crayfish were found to be highly size selective, consuming significantly more of the smallest size class of zebra mussels offered (7–12 mm), over medium (16–21 mm) and large (25–30 mm). Crayfish feeding rate on zebra mussels was not altered when mussels were presented clumped together in natural druses compared with mussels in a disassembled druse. Crayfish spent significantly more time foraging when mussels were unattached, and a greater proportion of attacks were on medium and large than on small mussels (83% of attacks were on medium and large mussels when unattached as opposed to 47% when on druses). Individual crayfish feeding rate decreased significantly at densities of > ~5 crayfish m⁻². Signal crayfish are, therefore, unlikely to be able to significantly impact established populations of zebra mussels in the wild, although zebra mussels have the potential to provide crayfish with a substantial food source.     

Thermal ecology and baseline energetic requirements of a large‐bodied ectotherm suggest resilience to climate change

1. Most studies on how rising temperatures will impact terrestrial ectotherms have focused on single populations or multiple sympatric species. Addressing the thermal and energetic implications of climatic variation on multiple allopatric populations of a species will help us better understand how a species may be impacted by altered climates.
2. We used eight years of thermal and behavioral data collected from four populations of Pacific rattlesnakes (Crotalus oreganus) living in climatically distinct habitat types (inland and coastal) to determine the field‐active and laboratory‐preferred body temperatures, thermoregulatory metrics, and maintenance energetic requirements of snakes from each population.
3. Physical models showed that thermal quality was best at coastal sites, but inland snakes thermoregulated more accurately despite being in more thermally constrained environments. Projected increases of 1 and 2°C in ambient temperature result in an increase in overall thermal quality at both coastal and inland sites.
4. Population differences in modeled standard metabolic rate estimates were driven by body size and not field‐active body temperature, with inland snakes requiring 1.6× more food annually than coastal snakes.
5. All snakes thermoregulated with high accuracy, suggesting that small increases in ambient temperature are unlikely to impact the maintenance energetic requirements of individual snakes and that some species of large‐bodied reptiles may be robust to modest thermal perturbations under conservative climate change predictions.

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Scaling the extinction vortex: Body size as a predictor of population dynamics close to extinction events

1. Mutual reinforcement between abiotic and biotic factors can drive small populations into a catastrophic downward spiral to extinction—a process known as the “extinction vortex.” However, empirical studies investigating extinction dynamics in relation to species'' traits have been lacking.
2. We assembled a database of 35 vertebrate populations monitored to extirpation over a period of at least ten years, represented by 32 different species, including 25 birds, five mammals, and two reptiles. We supplemented these population time series with species‐specific mean adult body size to investigate whether this key intrinsic trait affects the dynamics of populations declining toward extinction.
3. We performed three analyses to quantify the effects of adult body size on three characteristics of population dynamics: time to extinction, population growth rate, and residual variability in population growth rate.
4. Our results provide support for the existence of extinction vortex dynamics in extirpated populations. We show that populations typically decline nonlinearly to extinction, while both the rate of population decline and variability in population growth rate increase as extinction is approached. Our results also suggest that smaller‐bodied species are particularly prone to the extinction vortex, with larger increases in rates of population decline and population growth rate variability when compared to larger‐bodied species.
5. Our results reaffirm and extend our understanding of extinction dynamics in real‐life extirpated populations. In particular, we suggest that smaller‐bodied species may be at greater risk of rapid collapse to extinction than larger‐bodied species, and thus, management of smaller‐bodied species should focus on maintaining higher population abundances as a priority.

     

Targeted and passive environmental DNA approaches outperform established methods for detection of quagga mussels,Dreissena rostriformis bugensis in flowing water

1. The early detection of invasive non‐native species (INNS) is important for informing management actions. Established monitoring methods require the collection or observation of specimens, which is unlikely at the beginning of an invasion when densities are likely to be low. Environmental DNA (eDNA) analysis is a highly promising technique for the detection of INNS—particularly during the early stages of an invasion.
2. Here, we compared the use of traditional kick‐net sampling with two eDNA approaches (targeted detection using both conventional and quantitative PCR and passive detection via metabarcoding with conserved primers) for detection of quagga mussel, Dreissena rostriformis bugensis, a high priority INNS, along a density gradient on the River Wraysbury, UK.
3. All three molecular tools outperformed traditional sampling in terms of detection. Conventional PCR and qPCR both had 100% detection rate in all samples and outperformed metabarcoding when the target species was at low densities. Additionally, quagga mussel DNA copy number (qPCR) and relative read count (metabarcoding) were significantly influenced by both mussel density and distance from source population, with distance being the most significant predictor.
4. Synthesis and application. All three molecular approaches were more sensitive than traditional kick‐net sampling for the detection of the quagga mussel in flowing water, and both qPCR and metabarcoding enabled estimates of relative abundance. Targeted approaches were more sensitive than metabarcoding, but metabarcoding has the advantage of providing information on the wider community and consequently the impacts of INNS.

     

Growth characteristics of freshwater pearl mussels,Margaritifera margaritifera (L.)

• 1 Shell growth in the freshwater pearl mussel, Margaritifera margaritifera, was investigated. Three non‐linear growth models (i.e. power, logistic and von Bertalanffy) were fitted to Scottish length‐at‐age data sets and compared.
• 2 Overall, the von Bertalanffy model outperformed the other two approaches, generating the smallest residuals in eight out of 11 samples (the logistic model provided slightly better fits to the other three). It was concluded that individual M. margaritifera appear to grow in an approximately asymptotic fashion and that the von Bertalanffy equation is an appropriate growth model to fit to freshwater pearl mussel length‐at‐age data.
• 3 The ranges in von Bertalanffy parameter estimates observed (k = 0.023–0.075 year^‐1, L_∞ = 77–158 mm, t_o = ‐3.93–4.33 years) are typical of those reported in northern European populations.
• 4 Most of the populations investigated had relatively low k‐values and high maximum age (A_max) estimates. This feature, which suggests high long‐term productivity and less vulnerability to decline (i.e. larger, longer‐living mussels produce more offspring), may be a reason why these populations have survived until now. The population which appears to be the most vulnerable (i.e. which has the highest k and lowest A_max) is probably not recruiting adequately at present.
• 5 An index of absolute growth (mean shell length‐at‐age) was also used for comparing different populations. Observed between‐ and within‐river differences in mussel growth patterns may be associated with a number of environmental factors, particularly water temperature and productivity.
• 6 A significant positive relationship between river length and mean mussel length‐at‐age was observed. In general, mussels grow large in large, cold rivers and vice versa, although there are exceptions which suggest that additional factors may be involved.