Behaviour and physiology are linked in the responses of freshwater mussels to drought

1. Droughts have become prevalent in the south‐eastern U.S.A. and are predicted to become more common in the future. Drought conditions have particularly strong negative effects on sessile aquatic organisms with limited dispersal ability. This study explored the linkages between physiological tolerance, behavioural response and survival of three species of freshwater mussels subjected to drought. 2. To assess physiological tolerance, we measured survival under desiccation at 25, 35 and 45 °C in the laboratory. To assess behavioural responses, we tracked horizontal and vertical movement of mussels in a drying stream reach. 3. Uniomerus tetralasmus showed the greatest desiccation tolerance, Lampsilis straminea was intermediate, and Pyganodon grandis had the lowest tolerance at all temperatures. 4. In the drying stream reach, U. tetralasmus showed little horizontal movement and quickly became stranded. The other two species tracked the receding water. It was not until the pool had been reduced to c. 10% of its original size that ≥50% of P. grandis and L. straminea became stranded. 5. Uniomerus tetralasmus and L. straminea burrowed in response to becoming stranded; however, both species burrowed only shallowly (3–4 cm), presumably because burrowing to greater depths did not convey increasing thermal refuge. Pyganodon grandis rarely burrowed. No P. grandis survived the 15‐week drought, while 45% of L. straminea and 77% of U. tetralasmus survived. 6. Three strategies emerged for freshwater mussels to cope with drought conditions: tracking (intolerant), track then burrow (semi‐tolerant) and burrowing (tolerant). Results suggest that drought poses the greatest threat to intolerant trackers, while tolerant burrowers are the most resistant to drought conditions.     

Winter in water: differential responses and the maintenance of biodiversity

The ecological consequences of winter in freshwater systems are an understudied but rapidly emerging research area. Here, we argue that winter periods of reduced temperature and light (and potentially oxygen and resources) could play an underappreciated role in mediating the coexistence of species. This may be especially true for temperate and subarctic lakes, where seasonal changes in the thermal environment might fundamentally structure species interactions. With climate change already shortening ice‐covered periods on temperate and polar lakes, consideration of how winter conditions shape biotic interactions is urgently needed. Using freshwater fishes in northern temperate lakes as a case study, we demonstrate how physiological trait differences (e.g. thermal preference, light sensitivity) drive differential behavioural responses to winter among competing species. Specifically, some species have a higher capacity for winter activity than others. Existing and new theory is presented to argue that such differential responses to winter can promote species coexistence. Importantly, if winter is a driver of niche differences that weaken competition between, relative to within species, then shrinking winter periods could threaten coexistence by tipping the scales in favour of certain sets of species over others.     

Temperature-related differences in mitochondrial function among clones of the cladoceran Daphnia pulex

This study assessed the thermal sensitivity of mitochondrial respiration in the small crustacean Daphnia pulex. More specifically, we wanted to determine if clones that inhabit different latitudes and habitats showed differences in the thermal sensitivity of their mitochondrial function. The experimental design included two clones from temperate environments (Fence from Ontario and Hawrelak from Alberta) and two clones from subarctic environments (A24 from Manitoba and K154 from Quebec). The integrated mitochondrial function was measured with high-resolution respirometry following whole-animal permeabilization. Mitochondrial respiration was performed under six different temperatures (10, 15, 20, 25, 30, and 35 °C) in the clone Hawrelak and at two temperatures (10 and 20 °C) in the three other clones. In the clone Hawrelak, complexes I and II respiration showed higher sensitivity to temperature variation compared to complex IV respiration. Interestingly, the threshold plot showed no excess capacity of complex IV at 20 °C in this clone. The clones showed significant divergence in the ability to oxidize the complex I and complex IV substrates relative to the maximal oxidative phoshorylation capacity of mitochondria. More importantly, some of the clonal divergences were only detected under low assay temperatures, pointing toward the importance of this parameter in comparative studies. Future and more complex studies on clones from wider environmental gradients will help to resolve the link between mitochondrial function and adaptations of organisms to particular conditions, principally temperature.     

Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

Background  

Doubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).     

Phylogeography of the Coastal Mosquito Aedes togoi across Climatic Zones: Testing an Anthropogenic Dispersal Hypothesis

The coastal mosquito Aedes togoi occurs more or less continuously from subarctic to subtropic zones along the coasts of the Japanese islands and the East Asian mainland. It occurs also in tropical Southeast Asia and the North American Pacific coast, and the populations there are thought to have been introduced from Japan by ship. To test this hypothesis, the genetic divergence among geographic populations of A. togoi was studied using one mitochondrial and three nuclear gene sequences. We detected 71 mitochondrial haplotypes forming four lineages, with high nucleotide diversity around temperate Japan and declining towards peripheral ranges. The major lineage (L1) comprised 57 haplotypes from temperate and subarctic zones in Japan and Southeast Asia including southern China and Taiwan. Two other lineages were found from subtropical islands (L3) and a subarctic area (L4) of Japan. The Canadian population showed one unique haplotype (L2) diverged from the other lineages. In the combined nuclear gene tree, individuals with mitochondrial L4 haplotypes diverged from those with the other mitochondrial haplotypes L1—L3; although individuals with L1—L3 haplotypes showed shallow divergences in the nuclear gene sequences, individuals from Southeast Asia and Canada each formed a monophyletic group. Overall, the genetic composition of the Southeast Asian populations was closely related to that of temperate Japanese populations, suggesting recent gene flow between these regions. The Canadian population might have originated from anthropogenic introduction from somewhere in Asia, but the possibility that it could have spread across the Beringian land bridge cannot be ruled out.     

Evidence of Large Change in Unionid Mussel Abundance from Selective Muskrat Predation,as Inferred by Shell Remains Left on Shore

Three species of unionid mussels (Pyganodon grandis, Lampsilis siliquoidea, and Toxolasma parvus) were preyed on by muskrats (Ondatra zibethicus) that left shell remains at feeding sites (middens) along the shore of Lake LaSalle (West) in western New York State, USA. Mussels became established within five years of the construction of this small artificial lake, and individuals of all three species have grown rapidly to large size. The abundance of prey in middens in 1988–1990 and a marked decline in subsequently deposited shells indicate how dramatically muskrats had exploited this food source. They consumed > 2700 individuals of P. grandis (by far the most common prey item) through 1990, yet only 20 newly deposited shells were found in 1993. At a midden where prey depletion was directly catalogued during 1988, larger specimens of P. grandis were consumed first, suggesting size selection. L. siliquoidea has been least affected by predation, and was the mussel most often found alive in the littoral zone. No live T. parvus were ever collected, and this species is known only from middens. Complete collections of shell remains from the shoreline through 1999 suggest that the mussel population may be recovering slowly. Muskrat predation may be more important in influencing mussel population structure than previously realized, and the effects can be dramatic spatially and temporally.     

Edaphic factors do not govern the ectomycorrhizal specificity of Pisonia grandis (Nyctaginaceae)

Pisonia grandis (Nyctaginaceae), a widespread tree of Pacific coral atolls and islands, displays one of the more restrictive ranges of ectomycorrhizal (ECM) fungus associates among autotrophic plants. Only five ECM fungi are currently known associates; our study adds one. In many habitats, P. grandis is restricted to large seabird colonies where nitrogen and phosphorus inputs in the form of guano are substantial. It has been suggested that the ECM specificity displayed by P. grandis is the result of the unusual nutrient-rich habitat in which P. grandis grows. On Rota, Commonwealth of the Northern Mariana Islands, P. grandis grows in habitats heavily influenced by guano additions and also in upland forests where seabirds do not roost or nest. To test the hypothesis that the ECM specificity displayed by P. grandis is the result of nutrient-related or toxicity-related factors associated with guano inputs, we sampled P. grandis growing in both guano-rich and guano-poor habitats on Rota, Commonwealth of the Northern Mariana Islands. We identified ECM symbionts of P. grandis from both habitats as well as two symbionts of Intsia bijuga (Fabaceae) from nutrient-rich habitats. We identified three ECM symbionts of P. grandis from Rota; all three were found in both guano-rich and guano-poor habitats. No differences in community diversity were detected between guano-rich and guano-poor habitats. We also detected two ECM fungal species associating with I. bijuga but not associating with P. grandis inside guano-rich habitats. From these results, we infer that edaphic factors are not responsible for limiting the ECM community associating with P. grandis to its observed level of specificity.     

Parasitic mite and trematode abundance are associated with reduced reproductive output and physiological condition of freshwater mussels

Although historically understudied, parasites may play an important role in freshwater invertebrate population ecology and evolution. We quantified abundance of parasitic mites and trematodes in the freshwater mussel Pyganodon grandis, in a southeastern Alabama stream (USA), to assess parasite impact on adult mussel physiological condition and reproductive output. We used stepwise multiple regression analyses to assess the effects of mussel size and parasites on reproduction and condition. Multiple regression analysis found no multivariate models that predicted reproductive output or physiological condition. However, univariate models revealed that increased parasite densities predict reduced mussel reproductive output and physiological condition. These findings suggest that parasites may have important negative consequences for freshwater mussels. We hypothesize that elevated parasite loads may reduce mussel fitness in impounded or nutrient-enriched streams with high densities of intermediate hosts (chironomid midges).     

Vulnerability to climate warming and acclimation capacity of tropical and temperate coastal organisms

Ecological forecasting on the likely impacts of climate warming is crucial at a time when several ecosystems seem to be responding to this environmental threat. Among the most important questions are: which are the most vulnerable organisms to climate warming and where are they? Recently, there has been debate on whether the tropics or temperate zones are more vulnerable to warming. Vulnerability toward higher temperatures will depend on the organisms’ thermal limits and also on their acclimation capacity, which remains largely unknown for most species. The aim of the present work was to estimate (1) the upper thermal limits (Critical Thermal Maximum (CTMax)), (2) the warming tolerance (CTMax – Maximum Habitat Temperature) and (3) the acclimation capacity of tropical and temperate rocky shore organisms. Differences in biological groups (decapod crustaceans vs fish) were investigated and the effect of region (tropical vs temperate) and habitat (intertidal vs subtidal) was tested. Overall, 35 species were tested. For the assessment of the acclimation capacity, tropical-temperate pairs of closely related species of shrimp, crab and fish were selected. Warming tolerance was higher for temperate species than for tropical species and higher for subtidal species than for intertidal species, confirming that species with the highest thermal limits have the lowest warming tolerance. All species tested presented some acclimation capacity (CTMax_Trial − CTMax_Control), with the exception of gobiid fish, which was not observed to acclimate. The tropical species tested showed a lower acclimation capacity than their temperate counterparts. Given that tropical rocky shore organisms are already living very close to their thermal limits and that their acclimation capacity is limited, it is likely that the impacts of global warming will be evident sooner in the tropics than in the temperate zone.     

Population level differences in thermal sensitivity of energy assimilation in terrestrial salamanders

Thermal adaptation predicts that thermal sensitivity of physiological traits should be optimized to thermal conditions most frequently experienced. Furthermore, thermodynamic constraints predict that species with higher thermal optima should have higher performance maxima and narrower performance breadths. We tested these predictions by examining the thermal sensitivity of energy assimilation between populations within two species of terrestrial-lungless salamanders, Plethodon albagula and P. montanus. Within P. albagula, we examined populations that were latitudinally separated by >450 km. Within P. montanus, we examined populations that were elevationally separated by >900 m. Thermal sensitivity of energy assimilation varied substantially between populations of P. albagula separated latitudinally, but did not vary between populations of P. montanus separated elevationally. Specifically, in P. albagula, the lower latitude population had a higher thermal optimum, higher maximal performance, and narrower performance breadth compared to the higher latitude population. Furthermore, across all individuals as thermal optima increased, performance maxima also increased, providing support for the theory that “hotter is better”.     

Comparison of oxygen consumption in freshwater mussels (Unionidae) from different habitats during declining dissolved oxygen concentration

The rate of oxygen consumption (OC) of 9 species of freshwater mussels was measured under declining dissolved oxygen (DO) concentrations. The effects of temperature for some species also was investigated. The pattern of the OC vs. DO curve for each species was used in a hyperbolic model to compare abilities to regulate OC under low oxygen conditions. At 24.5 °C, Pyganodon grandis (from lakes), Amblema plicata and Quadrula pustulosa (from mud or sand in large rivers), Elliptio complanata (from pool areas in rivers), and Elliptio fisheriana and Elliptio lanceolata (from bank margins of rivers) were better able to maintain OC under low DO than were Villosa iris and Villosa constricta (which inhabit riffles) and Pleurobema cordatum (found in rivers with moderate flow). Villosa iris was especially sensitive to low oxygen conditions. The ability to maintain normal OC at low DO was improved considerably at 16.5 °C for V. iris, P. grandis and E. complanata. It is concluded that oxygen regulation ability appears to be related to the degree of hypoxia a species normally experiences in its habitat type, and it is enhanced at low temperature. The measurement of OC vs. DO may be a useful technique for estimating DO water quality criteria for endangered species because it is noninvasive.     

Revalidation and redescription of Potamon elbursi Pretzmann, 1976 (Brachyura, Potamidae) from Iran, based on morphology and genetics

In the current study, we redescribe and revalidate a freshwater crab species of the genus Potamon Savigny, 1816, from northern Iran. Potamon elbursi Pretzmann, 1962, differs from the species it has been synonymised with, Potamon persicum Pretzmann, 1962, mainly by the shape of the first gonopods in males. Consistent and marked genetic divergence was also recognised in the mitochondrial 16S rRNA and cytochrome oxidase subunit I genes. This study elevates P. elbursi to species rank and therefore increases the number of valid species of the genus Potamon to a total of twenty-two.     

Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species

Climate is an important factor limiting tree distributions and adaptation to different thermal environments may influence how tree populations respond to climate warming. Given the current rate of warming, it has been hypothesized that tree populations in warmer, more thermally stable climates may have limited capacity to respond physiologically to warming compared to populations from cooler, more seasonal climates. We determined in a controlled environment how several provenances of widely distributed Eucalyptus tereticornis and E. grandis adjusted their photosynthetic capacity to +3.5°C warming along their native distribution range (~16–38°S) and whether climate of seed origin of the provenances influenced their response to different growth temperatures. We also tested how temperature optima (T_opt) of photosynthesis and J_max responded to higher growth temperatures. Our results showed increased photosynthesis rates at a standardized temperature with warming in temperate provenances, while rates in tropical provenances were reduced by about 40% compared to their temperate counterparts. Temperature optima of photosynthesis increased as provenances were exposed to warmer growth temperatures. Both species had ~30% reduced photosynthetic capacity in tropical and subtropical provenances related to reduced leaf nitrogen and leaf Rubisco content compared to temperate provenances. Tropical provenances operated closer to their thermal optimum and came within 3% of the T_opt of J_max during the daily temperature maxima. Hence, further warming may negatively affect C uptake and tree growth in warmer climates, whereas eucalypts in cooler climates may benefit from moderate warming.     

Response of dominant grassland species in the temperate steppe of Inner Mongolia to different land uses at leaf and ecosystem levels

In order to study the responses of dominant species to different land uses in the semiarid temperate grassland of Inner Mongolia, we tested the physiological responses of Stipa grandis, Leymus chinensis, and Artemisia frigida to mowing, grazing exclusion, and grazing land uses at the leaf and ecosystem levels. The grazing-exclusion and mowing sites released CO₂, but the grazing site was a net carbon sink. L. chinensis and S. grandis contributed more to the ecosystem CO₂ exchange than A. frigida. At the grazing-exclusion and mowing sites, Leymus chinensis and Stipa grandis both exhibited a higher light-saturation point and higher maximum photosynthetic rate than that at the grazing site, which increased photosynthesis and growth compared to those at the grazing site. In contrast, A. frigida possessed a higher nitrogen content than the other species, and more of the light energy used for photosynthesis, particularly at the grazing site.     

Variation in setal micromechanics and performance of two gecko species

Biomechanical models of the gecko adhesive system typically focus on setal mechanics from a single gecko species, Gekko gecko. In this study, we compared the predictions from three mathematical models with experimental observations considering an additional gecko species Phelsuma grandis, to quantify interspecific variation in setal micromechanics. We also considered the accuracy of our three focal models: the frictional adhesion model, work of detachment model, and the effective modulus model. Lastly, we report a novel approach to quantify the angle of toe detachment using the Weibull distribution. Our results suggested the coupling of frictional and adhesive forces in isolated setal arrays, first observed in G. gecko is also present in P. grandis although P. grandis displayed a higher toe detachment angle, suggesting they produce more adhesion relative to friction than G. gecko. We also found the angle of toe detachment accurately predicts a species’ maximum performance limit when fit to a Weibull distribution. When considering the energy stored during setal attachment, we observed less work to remove P. grandis arrays when compared with G. gecko, suggesting P. grandis arrays may store less energy during attachment, a conclusion supported by our model estimates of stored elastic energy. Our predictions of the effective elastic modulus model suggested P. grandis arrays to have a lower modulus, E _eff, but our experimental assays did not show differences in moduli between the species. The considered mathematical models successfully estimated most of our experimentally measured performance values, validating our three focal models as template models of gecko adhesion (see Full and Koditschek in J Exp Biol 202(23):3325–3332, 1999), and suggesting common setal mechanics for our focal species and possibly for all fibular adhesives. Future anchored models, built upon the above templates, may more accurately predict performance by incorporating additional parameters, such as variation in setal length and diameter. Variation in adhesive performance may affect gecko locomotion and as a result, future ecological observations will help to determine how species with different performance capabilities use their habitat.     

Functional conservatism in mitochondrial evolution: insight from hybridization of arctic and brook charrs

To assess the potential adaptive value of mtDNA, we evaluated functional properties and thermal sensitivity of key mitochondrial enzymes in two species that have originally evolved in different thermal environments (arctic charr, Salvelinus alpinus, and brook charr, S. fontinalis), as well as in their hybrids. We measured the activity of two enzymes of the electron transport system (cytochrome c oxidase and NADH-ubiquinone oxidoreductase), one enzyme of the mitochondrial matrix (citrate synthase), and one enzyme of the anaerobic glycolysis (lactate dehydrogenase) in the red muscle at three temperatures (6 degrees C, 12 degrees C and 18 degrees C). Surprisingly, the species presented no significant differences in enzyme activity, thermal sensitivity or thermostability of key metabolic enzymes even though they evolved in different thermal environments and present important differences in amino acid sequences. It seems that amino acid substitutions between those species have minor impact on the functional properties of mitochondrial enzymes studied. The thermal sensitivity results (Q(10)) obtained for inner-membrane mitochondrial enzymes differed somewhat from those of mitochondrial matrix or cytosolic enzymes. This result indicates the modulation of thermal sensitivity of all mitochondrial inner-membrane processes by a common parameter, which could be the structural and functional properties of membrane phospholipids.     

MULTIPLE ORIGINS OF GENDER-ASSOCIATED MITOCHONDRIAL DNA LINEAGES IN BIVALVES (MOLLUSCA: BIVALVIA)

Previous studies have shown that marine mussels (genus Mytilus) and a freshwater mussel (Pyganodon grandis) contain two distinct gender-associated mitotypes, which is a characteristic feature of the phenomenon of doubly uniparental inheritance (DUI) of mitochondrial DNA (mtDNA). Here we present evidence for the presence of distinct male (M) and female (F) mitotypes in three other bivalve species, the mytilid Geukensia demissa, and the unionid species P. fragilis and Fusconaia flava. Nucleotide sequences of a segment of the COI gene from the M and F mitotypes from each of the three mytilid species (M. edulis, M. trossulus, G. demissa) and three unionid species (P. grandis, P. fragilis, F. flava) were used for phylogenetic analysis. The analysis suggests three independent origins of M and F mitotypes for the six species examined; one for the three unionid species, one for the two Mytilus species, and one for Geukensia. The first of these F/M divergence events, while of uncertain age, predates the divergence of the two unionid genera and is likely older than either of the two F/M divergence events in the mytilid taxa. The most parsimonious explanation of multiple F/M divergence events is that they represent independent origins of DUI. Another possibility is that, in a given taxon, an F or M mitotype assumes the role of the opposite mitotype (by virtue of a mechanism that remains to be clarified) and subsequently was fixed within its new gender. The fixation of a mtDNA lineage derived from a mitotype of switched function would reset the divergence of the gender-associated lineages to zero, thereby mimicking a de novo split of F and M lineages from a preexisting mtDNA genome that was not gender specific. Further broad-scale taxonomic studies of the occurrence of distinct M and F mitotypes may allow for the evaluation of the latter hypothesis.     

Pyganodon (Bivalvia: Unionoida: Unionidae) phylogenetics: a male- and female-transmitted mitochondrial DNA perspective

Species boundaries, evolutionary relationships and geographic distributions of many unionoid bivalve species, like those in the genus Pyganodon, remain unresolved in Eastern North America. Because unionoid bivalves are one of the most imperiled groups of animals in the world, understanding the genetic variation within and among populations as well as among species is crucial for effective conservation planning. Conservation of unionoid species is indispensable from a freshwater habitat perspective but also because they possess a unique mitochondrial inheritance system where distinct gender-associated mitochondrial DNA lineages coexist: a female-transmitted (F) mt genome and a male-transmitted (M) mt genome that are involved in the maintenance of separate sexes (=dioecy). In this study, 42 populations of Pyganodon sp. were sampled across a large geographical range and fragments of two mitochondrial genes (cox1 and cox2) were sequenced from both the M- and F-transmitted mtDNA genomes. Our results support the recency of the divergence between P. cataracta and P. fragilis. We also found two relatively divergent F and M lineages within P. grandis. Surprisingly, the relationships among the P. grandis specimens in the F and M sequence trees are not congruent. We found that a single haplotype in P. lacustris has recently swept throughout the M genotype space leading to an unexpectedly low diversity in the M lineage in that species. Our survey put forward some challenging results that force us to rethink hybridization and species boundaries in the genus Pyganodon. As the M and F genomes do not always display the same phylogeographic story in each species, we also discuss the importance of being careful in the interpretation of molecular data based solely on maternal transmitted mtDNA genomes. The involvement of F and M genomes in unionoid bivalve sex determination likely played a role in the genesis of the unorthodox phylogeographic patterns reported herein.     

Ecological Effects of the Invasive Giant Madagascar Day Gecko on Endemic Mauritian Geckos: Applications of Binomial-Mixture and Species Distribution Models

The invasion of the giant Madagascar day gecko Phelsuma grandis has increased the threats to the four endemic Mauritian day geckos (Phelsuma spp.) that have survived on mainland Mauritius. We had two main aims: (i) to predict the spatial distribution and overlap of P. grandis and the endemic geckos at a landscape level; and (ii) to investigate the effects of P. grandis on the abundance and risks of extinction of the endemic geckos at a local scale. An ensemble forecasting approach was used to predict the spatial distribution and overlap of P. grandis and the endemic geckos. We used hierarchical binomial mixture models and repeated visual estimate surveys to calculate the abundance of the endemic geckos in sites with and without P. grandis. The predicted range of each species varied from 85 km² to 376 km². Sixty percent of the predicted range of P. grandis overlapped with the combined predicted ranges of the four endemic geckos; 15% of the combined predicted ranges of the four endemic geckos overlapped with P. grandis. Levin''s niche breadth varied from 0.140 to 0.652 between P. grandis and the four endemic geckos. The abundance of endemic geckos was 89% lower in sites with P. grandis compared to sites without P. grandis, and the endemic geckos had been extirpated at four of ten sites we surveyed with P. grandis. Species Distribution Modelling, together with the breadth metrics, predicted that P. grandis can partly share the equivalent niche with endemic species and survive in a range of environmental conditions. We provide strong evidence that smaller endemic geckos are unlikely to survive in sympatry with P. grandis. This is a cause of concern in both Mauritius and other countries with endemic species of Phelsuma.