The effects of elevated water temperature on native juvenile ... - BioOne

Freshwater Science, 2013, 32(4):1168–1177 ’ 2013 by The Society for Freshwater Science DOI: 10.1899/12-132.1 Published online: 24 September 2013

The effects of elevated water temperature on native juvenile mussels: implications for climate change Alissa M. Ganser1,3, Teresa J. Newton2,4,

AND

Roger J. Haro1,5

1

2

University of Wisconsin–La Crosse, River Studies Center, La Crosse, Wisconsin 54601 USA US Geological Survey, Upper Midwest Environmental Sciences Center, La Crosse, Wisconsin 54603 USA

Abstract. Native freshwater mussels are a diverse but imperiled fauna and may be especially sensitive to increasing water temperatures because many species already may be living near their upper thermal limits. We tested the hypothesis that elevated water temperatures (20, 25, 30, and 35uC) adversely affected the survival and physiology of 2-mo-old juvenile mussels (Lampsilis abrupta, Lampsilis siliquoidea, and Megalonaias nervosa) in 28-d laboratory experiments. The 28-d LT50s (lethal temperature affecting 50% of the population) ranged from 25.3 to 30.3uC across species, and were lowest for L. abrupta and L. siliquoidea. Heart rate of L. siliquoidea was not affected by temperature, but heart rate declined at higher temperatures in L. abrupta and M. nervosa. However, for both of these species, heart rate also declined steadily during the experiment and a strong temperature 3 time interaction was detected. Juvenile growth was low for all species in all treatments and did not respond directly to temperature, but growth of some species responded to a temperature 3 time interaction. Responses to thermal stress differed among species, but potential laboratory artifacts may limit applicability of these results to real-world situations. Environmentally relevant estimates of upper thermal tolerances in native mussels are urgently needed to assess the extent of assemblage changes that can be expected in response to global climate change. Key words:

freshwater mussel, climate change, physiology, temperature, survival, heart rate, growth.

The effects of global climate change have been observed in an array of biological contexts ranging from osmotic challenges accompanying sea-level rise subsequent to glacial melting, poleward shifts of butterfly species, and coral bleaching (Hoegh-Guldberg 1999, Parmesan et al. 1999, Bahr et al. 2009). Freshwater ecosystems may be particularly sensitive to climate change because they are increasingly stressed by a wide variety of anthropogenic factors (Burton and Likens 1973, Webb and Walling 1988, Wright et al. 1999, Kaushal et al. 2008). Adverse effects of rising water temperatures on fish and aquatic invertebrates already have been documented (Sweeney and Vannote 1978, Winder and Schindler 2004, Dembski et al. 2006, Galbraith et al. 2010). Native freshwater mussels are relatively sedentary, often long-lived, benthic macroinvertebrates that have a complex life cycle involving a parasitic larval stage. These bivalves provide numerous ecological services

to aquatic systems including linking pelagic and benthic food webs, increasing habitat complexity, and providing structural refugia for other aquatic invertebrates (Strayer et al. 1994, Vaughn et al. 2004, Spooner and Vaughn 2006, Zimmerman and de Szalay 2007). North America has the most diverse freshwater mussel fauna in the world. However, ,70% of these species are considered of special concern, threatened, endangered, or extinct (Bogan 1993). Invasive species, habitat loss, and pollutants are all thought to contribute to mussel declines (Strayer et al. 2004), and global climate change and associated higher water temperatures may further affect these organisms (Hastie et al. 2003, Spooner and Vaughn 2008). Freshwater mussels may be particularly susceptible to climate change because of their patchy distribution, limited mobility, larval dependence on host fishes, and fragmentation of their ranges by habitat destruction. Climate change probably affects mussels via altered temperatures that decrease survival, growth, and reproductive success and altered precipitation patterns that affect the relationship between recruitment and stream flow (Hastie et al. 2003). Populations

3

Present address: University of Louisville, Louisville, Kentucky 40202 USA. E-mail: [email protected] 4 E-mail addresses: [email protected] 5 [email protected]

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of several mussel species already appear to be near their upper thermal limits (Pandolfo et al. 2010), and in some streams, species composition has shifted to more thermally tolerant mussel species (Spooner and Vaughn 2008, Galbraith et al. 2010). Specific effects of elevated temperatures on mussels include increased clearance rates, increased O2 consumption rates, decreased viability of glochidia, and decreased survival of juveniles (Zimmerman and Neves 2002, Spooner and Vaughn 2008, Pandolfo et al. 2010). Survival is the most common endpoint used in ecotoxicological studies of mussels (Newton and Cope 2007). However, environmental conditions can adversely affect an organism’s fitness before mortality occurs. Sublethal endpoints, such as heart rate, growth, and resource assimilation rates, can be useful indicators of stress in mussels (Polhill and Dimock 1996, Newton et al. 2003, Bringolf et al. 2007b, Spooner and Vaughn 2008, Pandolfo et al. 2009). Heart rate is a sensitive indicator of stress that generally increases with increasing water temperatures. It can be measured noninvasively, and it is used as a surrogate measure of metabolic rate in juvenile bivalves because of the difficulty of measuring O2 consumption in very small organisms (Lowe and Trueman 1972, Polhill and Dimock 1996, Pandolfo et al. 2009). Precise shell growth measurements made with computer imaging software can enable detection of small reductions in growth from effects, such as exposure to NH3 (Newton et al. 2003, Newton and Cope 2007). We evaluated the effects of increasing water temperature on survival, heart rate, and growth for juvenile mussels of 3 species. Methods Juvenile mussels were exposed to 1 of 4 watertemperature treatments (20, 25, 30, and 35uC), and each treatment was replicated 5 times in a completely randomized design. The 20uC treatment served as the baseline temperature. The experimental unit (test chamber) was a 39-L flow-through glass aquarium (900 mL/ min 6 10%). Water temperature in each test chamber was maintained by 4 mixing valves (Belimo Americas, Danbury, Connecticut) that delivered well water to each of 4 head boxes. Water from each head box was randomly distributed to the test chambers. Treatment temperatures and acclimation procedures followed Spooner and Vaughn (2008) and Pandolfo et al. (2010), and treatment temperatures encompassed the range experienced by mussel beds in the Upper Mississippi River during summer (TJN, unpublished data). Captively propagated juveniles of 3 species, Lampsilis abrupta, Lampsilis siliquoidea, and Megalonaias

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nervosa, were obtained from Missouri State University (see Barnhart 2006). These species are widely distributed in eastern North America, and they represent 2 of the 5 phylogenetic tribes within the family Unionidae in North America (Lampsilini: L. abrupta and L. siliquoidea; Quadrulini: M. nervosa). All mussels were ,2-mo old and were 1.5 to 3.0 mm long. On arrival at the laboratory, mussels were placed in 500-mm-mesh chambers in a flow-through water bath at the shipping temperature (22–24uC). Water temperature was decreased by ƒ 3uC/d (Galbraith et al. 2012) to 18uC. After a 4-d (L. abrupta and M. nervosa) or 7-d (L. siliquoidea) acclimation period at 18uC, 5 mussels from each species were randomly selected and allocated to each test chamber at 18uC. Equipment malfunction precluded similar acclimation periods among species. The temperature in each test chamber was increased incrementally (ƒ3uC/d) with the aid of a computer program until it reached the desired treatment temperature (20, 25, 30, or 35uC), and mussels were acclimated to each temperature for another 24 h before testing began. During the experiments, all 5 juveniles of each species in each test chamber were held in a single glass tube (2.8 or 3.8 cm diameter, 8.9– 10.2 cm long) covered on one end with 500- or 1000mm mesh and suspended in the test chamber. Experiments were run at each temperature for 28 d. Two separate experiments were conducted according to availability of juveniles. Experiment 1 was conducted with L. abrupta and M. nervosa, and experiment 2 was conducted with L. siliquoidea. A data logger (iButton, Alpha Mach, Inc., Mont StHilaire, Quebec, Canada) in the bottom of each test chamber measured temperature hourly, and daily temperature measurements were taken with a thermometer to provide real-time data. Temperature (YSI model 550A; Yellow Springs Instruments, Yellow Springs, Ohio), dissolved O2 (YSI model 550A), and pH (Accumet model AP72; Fisher Scientific, Pittsburgh, Pennsylvania) were measured daily in each test chamber according to standard methods (ASTM 2006). Alkalinity, hardness, and conductivity (Accumet model AP75A) were measured weekly using standard methods (APHA 1995). Water-quality data were within the ranges recommended by ASTM (2006) and were similar among temperature treatments and between experiments (Table 1). Water temperatures deviated ƒ3uC from target temperatures in experiment 1 and ƒ1uC in experiment 2. Water temperatures differed between daily and hourly measurements by 0.1–3.6% in experiment 1 and 0–5.3% in experiment 2. Mussels were fed daily with ,450 mL of a stock solution containing 6 mL of Nanno 3600 (,1–2 mm) and 12 mL of Shellfish diet

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TABLE 1. Mean (6 SD) water-quality characteristics of treatment water during 28-d exposures of juvenile mussels to elevated temperatures. Experiment 1 contained Lampsilis abrupta and Megalonaias nervosa; experiment 2 contained L. siliquoidea. Data were averaged across all test chambers. Variable Dissolved O2 (mg/L) Dissolved O2 (% saturation) pH Conductivity (mS/cm) Alkalinity (mg CaCO3/L) Hardness (mg CaCO3/L)

Experiment 1 Experiment 2 7.6 6 1.4 .90% 8.1 6 0.1 413 6 21 126 6 16 181 6 34

7.7 6 1.1 .84% 7.9 6 0.1 409 6 60 126 6 3 187 6 4

1800 (,5–20 mm) diluted in 11 L well water (Reed Mariculture, Campbell, California; Wang et al. 2007). Photoperiod was maintained at ,8 h light and 16 h dark, which corresponded to an 8-h work day. On days 0, 7, 14, 21, and 28, all mussels from each chamber were removed and transferred to a Petri dish containing treatment water. Individuals with widely gaped valves and no tissue were considered dead. Immediately after removal, heart rate of each live mussel was measured for 15 s by observing the heart through the transparent shell with the aid of a dissecting microscope (Pandolfo et al. 2009). Heartrate measurements were made consecutively by 2 observers, but these measurements differed by ƒ10% and were averaged prior to analysis. After measuring heart rate, a composite image of each mussel was taken using imaging software (Media Cybernetics, Bethesda, Maryland), and shell length, width, and area were measured from the images. All 3 growth metrics showed similar responses, and only shelllength data are presented. Marking individuals was not feasible, so the mean heart rate and mean shell length of individuals in each test chamber on each sampling day were used for statistical analysis. Growth achieved in each test chamber by each sampling day was expressed as mean observed shell length minus mean initial shell length. Statistical analysis Percent survival data were used to estimate the lethal temperature at which 5% (LT05) and 50% (LT50) of the population died on each sampling day. These measures were derived from logistic regression of mortality and temperature. Estimates of the LT05 and LT50 and their 95% confidence limits were calculated by probit analysis (ASTM 1989) and were considered significantly different among species or days when confidence intervals (CIs) did not overlap (APHA 1995). The effects of temperature, time, and

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their interaction on heart rate and length were evaluated with a repeated-measures analysis of variance (rmANOVA) (Maceina et al. 1994). Because of high mortality by day 7 at 35uC, heart rate and length data from this treatment were excluded from analysis. To meet the assumptions of rmANOVA, all measurements were treated independently and response variables were assessed for normality using the Shapiro-Wilk test (p § 0.05). All response variables were normally distributed, with the exception of L. siliquoidea growth. In this case, a quantile– quantile plot showed that the data followed a normal trend. Mauchly’s sphericity test was used to evaluate the assumption of homogeneity of variance. When this assumption was violated, degrees of freedom were adjusted with the Greenhouse–Geisser correction to reduce Type I error. Results Survival of juveniles in the baseline treatment (20uC) on day 28 averaged 88% for L. siliquoidea and 100% for L. abrupta and M. nervosa (Fig. 1A–C). All LT05s and LT50s declined with time and were lowest on day 28. Juvenile survival varied among species. On day 28, L. abrupta and L. siliquoidea had significantly lower LT50s than M. nervosa. A similar pattern was observed with LT05s on day 28, but this pattern was not statistically significant. On all other sampling days, LT05s and LT50s were higher for M. nervosa than Lampsilis spp., but CIs could not be computed for most values because of high survival. LT05 and LT50 values tended to be lower for L. siliquoidea than L. abrupta, but few of these differences were significant. The influence of temperature and time on heart rate varied among species (Fig. 2A–C, Table 2). Heart rate of L. siliquoidea was not affected by temperature or time and remained relatively constant throughout the experiment. Heart rate of L. abrupta and M. nervosa declined significantly with increasing temperature and over time. For example, mean heart rate of M. nervosa across sampling days was 31% lower at 30uC than at 20uC, and mean heart rate across temperatures was 36% lower on day 28 than on day 0. However, a strong temperature 3 time interaction affected heart rates of both species. Overall, L. siliquoidea had the lowest heart rate, averaging 4–8 beats/min less across temperature and time than the other species (Fig. 2B). Temperature did not directly affect growth of any species, but juveniles grew little during the experiment (Fig. 3A–C). Across species and temperatures, juvenile size on day 28 was only 8% greater than initial size, and juveniles grew an average of ,0.2 mm. Size of M. nervosa did not increase over time, but the

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FIG. 1. Mortality of 2-mo-old juvenile Lampsilis abrupta (A), Lampsilis siliquoidea (B), and Megalonaias nervosa (C) during a 28-d laboratory exposure to elevated water temperatures. Lethal temperatures (uC, 95% confidence limits in parentheses) that killed 5 (LT05) and 50% (LT50) of the population are reported. For day 28, LT05 or LT50 values with the same letter were not significantly different. Confidence intervals for LT05 and LT50 overlapped among species on all other days. An asterisk indicates that confidence limits could not be estimated because there was not a partial mortality in one treatment.

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FIG. 2. Grand mean (61 SE, n = 5) heart rate of 2-mo-old juvenile Lampsilis abrupta (A), Lampsilis siliquoidea (B), and Megalonaias nervosa (C) during a 28-d laboratory exposure to elevated water temperatures.

temperature 3 time interaction was marginally significant (Table 2). Both Lampsilis species grew over time, and the temperature 3 time interaction was significant. Discussion Elevated water temperatures directly (temperature effect) or indirectly (temperature 3 time effect) influenced the survival, heart rate, and growth of the juveniles of 3 species of mussels. Survival of L. siliquoidea was affected at temperatures as low as 19.6uC (28-d LT05) or 25.3uC (28-d LT50). In another study, 4-d LT05s of juveniles of 8 mussel species ranged from 26.4 to 32.5uC, and 4-d LT50s ranged

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from 33.1 to 35.1uC (Pandolfo et al. 2010). These values are considerably higher than the 28-d values in our study, but they are similar to 7-d values in our study. Two species were tested in both studies (L. siliquoidea and M. nervosa). Our 28-d LT50s were 7.2 and 9.1uC lower than our 7-d values or the 4-d LT50s reported by Pandolfo et al. (2010), respectively, and 28-d LT50s for M. nervosa were 5.3 and 3.7uC lower than values in the shorter exposures. This result suggests that the negative effect of exposure to high temperatures increases over time and further decreases juvenile survival. Mussels are thermoconformers whose physiological processes are constrained by water temperature (McMahon and Bogan 2001). Generally, heart rate increases with increasing temperature (e.g., Dietz and Tomkins 1980, Polhill and Dimock 1996, Pandolfo et al. 2009). However, a critical temperature threshold may exist beyond which heart rate reaches a plateau or decreases (Braby and Somero 2006). Heart rate of L. siliquoidea was unaffected by temperature even though this species was most sensitive (as measured by survival) to high temperature. Heart rates of L. abrupta and M. nervosa were consistently lower at higher temperatures. Juvenile heart rates may have decreased in an attempt to lower metabolic rate and conserve energy during thermal stress. However, heart rate of both species also decreased slightly, but consistently, throughout the experiment regardless of temperature, and the effect of temperature was confounded with the effect of time. Thus, handling stress may be partially responsible for these results. Juveniles were removed from the test chambers for only ,5 min when we measured heart rate, but this procedure may have stressed juveniles when repeated weekly. An alternative explanation is that the time effect reflected natural ontogenetic changes in physiology. Heart rate in mussels decreases steadily with age (Polhill and Dimock 1996). However, the 28-d duration of our study seems insufficient to observe a significant ontogenetic change in heart rate. Heart rate can be a sensitive sublethal indicator of thermal stress, but further research is needed to quantify the potential confounding factors in laboratory studies. Growth of juvenile mussels also is expected to increase with warmer temperatures, but it can be reduced by exposure to critical temperature thresholds or other sources of environmental stress (Bartsch et al. 2003, Bringolf et al. 2007b, Newton and Bartsch 2007). Temperature did not directly affect growth of any species, but our ability to detect such an effect was limited by the extremely low growth rates of all individuals. The growth rates we observed (ƒ8% by day 28, ,0.2 mm/mo) were similar to those for

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TABLE 2. Results of repeated-measures analysis of variance for the effects of time, temperature, and the temperature 3 time interaction on heart rate and growth (shell length) of 2-mo-old juvenile mussels exposed to 20, 25, or 30uC water for 28 d. Heart rate Species Lampsilis abrupta Lampsilis siliquoidea Megalonaias nervosa

a

Growth

Source

F

df

p

F

df

p

Temperature Time Temperature 3 time Temperature Time Temperature 3 time Temperature Time Temperature 3 time

14.20 33.31 7.13 0.72 1.42 0.65 28.32 51.83 6.83

2 4 8 2 4 8 2 4 8

0.002 ,0.001 ,0.001 0.514 0.250 0.728 ,0.001 ,0.001 ,0.001

1.32 36.79 11.10 0.25 6.00 4.67 1.28 3.03 3.29

2 1.9a 3.8a 2 2.1a 4.2a 2 1.3a 2.6a

0.311 ,0.001 ,0.001 0.787 0.009 0.008 0.313 0.094 0.054

Use of the conservative Greenhouse–Geisser decreased degrees of freedom

control mussels in other laboratory toxicity studies (e.g., ƒ7% by day 21, Bringolf et al. 2007a, c; see also Wang et al. 2007), and we followed a standard feeding regime (Wang et al. 2007). Nevertheless, consistently low growth in the laboratory is probably a consequence of insufficient diet or other suboptimal holding conditions. In the wild, juveniles of a wide range of species reach §10 to 30 mm by the end of their first year (,2–5 mm growth/mo over a 6-mo growing season), and propagated juveniles raised in outdoor ponds achieve similarly high growth in their first year (Haag and Warren 2010, P. Johnson [Alabama Aquatic Biodiversity Center], personal communication). Consequently, the 28-d duration of our experiments should have been sufficient to observe considerable growth under suitable holding conditions. Longer-duration experiments could provide better evaluation of growth effects, but maintaining juveniles in good condition could be difficult in longer experiments. Including sediment could enhance growth by allowing juveniles to feed more efficiently (Gatenby et al. 1996), but recovering juveniles from sediments can be difficult. Life histories of North American freshwater mussels vary widely from short-lived, fast-growing, and highly fecund species to long-lived, slow-growing species that devote less energy to reproduction (Haag 2012). These fundamental ecological differences probably will translate into predictable differences in thermal tolerance. However, at this time, drawing meaningful generalizations about patterns of thermal tolerance among species is difficult. For example, short-lived lampsiline mussels, such as L. cardium, are considered thermally sensitive, whereas the longlived quadruline M. nervosa is considered thermally tolerant (Waller et al. 1999, Spooner and Vaughn 2008). These characterizations are consistent with our finding of lower LT50s for Lampsilis spp. than M.

nervosa. However, some lampsilines, such as Obliquaria reflexa, are considered thermally tolerant, and other long-lived quadrulines (Quadrula pustulosa) are considered thermally sensitive (Spooner and Vaughn 2008). Similarly, the mean growth constant (K) for Lampsilis spp. (0.41) is nearly 63 higher than for M. nervosa (0.07; Haag and Rypel 2011), data suggesting that temperature may have strongly divergent effects on growth of these species. However, because of the low growth in our study and the absence of direct effects of temperature on growth, we are unable to draw conclusions about these potential relationships. Measurements of differences in thermal tolerance among species will be crucial in understanding effects of climate change on mussel assemblages, and data on thermal tolerance are needed for a wide array of species. As we move forward in studying the effects of climate change on native mussel assemblages, several issues inherent to laboratory studies of survival or sublethal stress must be resolved. Early life stages of freshwater mussels are often the most sensitive to environmental contaminants or stress (Cope et al. 2008), but most toxicological studies use artificially propagated juveniles because wild juveniles are difficult to collect in quantity. Captively produced juveniles have no environmentally relevant thermalacclimation history, so we should not expect them to be good at adjusting to temperature change. On the other hand, recent thermal history influenced thermal tolerance of adult mussels (Galbraith et al. 2012), but acclimation temperature did not affect thermal tolerance of glochidia or juvenile life stages (Pandolfo et al. 2010). Thus, thermal acclimation may not be well developed even in wild juveniles because of their limited thermal history, which may lessen concerns about the applicability of studies using captively produced individuals.

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FIG. 3. Grand mean (61 SE, n = 5) shell length of 2-moold juvenile Lampsilis abrupta (A), Lampsilis siliquoidea (B), and Megalonaias nervosa (C) during a 28-d laboratory exposure to elevated water temperatures. The y-axis scales are set to reflect the larger size of M. nervosa individuals at the time of experiment initiation.

A more serious issue is our ability to create holding conditions in the laboratory that are optimal for growth and physiological function. In our study, captively produced juvenile mussels were maintained for a long time in the laboratory on an artificial diet that may have resulted in a gradual decline in juvenile health over the course of the experiment, as suggested by the lack of growth and decreases in heart rate. Absolute water temperature might be less important than the rate of temperature change or the extent of daily temperature fluctuations. We followed existing protocols, but laboratory studies like ours typically involve relatively rapid temperature changes or static temperatures that do not reflect natural thermal regimes. However, more gradual changes in

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temperature in the laboratory result in further decreases in juvenile vigor. These issues make results of our study and those like it difficult to apply to realworld situations. Once these issues are better understood, more robust studies on the effects of climate change on native mussel assemblages can be implemented. Despite the limitations of laboratory studies, we observed increased mortality and sublethal indicators of stress at temperatures that are frequently encountered in nature, results that support suggestions that some mussel species may already be living close to their thermal limits (Pandolfo et al. 2010). Summer water temperatures in shallow waters of the Upper Mississippi River commonly reach 30–32uC (TJN, unpublished data) and can reach 35–40uC in southern USA streams (Spooner and Vaughn 2008). Consequently, either thermal stress is widespread in nature, or mussels have behavioral adaptations that reduce thermal stress during periods of high temperature. Burrowing in river sediments has been proposed as one adaptation by which mussels could alleviate thermal stress (Cope et al. 2008). In the Upper Mississippi River basin, sediment temperatures 15 cm deep in mussel beds can be as much as 3uC cooler than surface sediments (J. S. Sauer, US Geological Survey Upper Midwest Environmental Sciences Center, unpublished data). However, juvenile mussels in the laboratory rarely burrow .1 cm. In the wild, mussels are usually found within the top 10 cm of the sediment, and burrowing depths tend to be greatest in winter (Yeager et al. 1994, Balfour and Smock 1995, Schwalb and Pusch 2007). Nevertheless, burrowing behavior in mussels is poorly known, particularly with regard to differences among life stages and environmental conditions. Water temperatures in §20 major USA streams have already risen significantly above historical levels, and continued increases at current rates may lead to cascading effects on many biological processes, including a loss of aquatic biodiversity (Kaushal et al. 2010). Increasing water temperatures as a result of global climate change may adversely affect freshwater mussels if many species already are living near their upper thermal tolerances (Pandolfo et al. 2010). Warming water temperatures caused by altered climate patterns already have affected mussel assemblages by shifting species abundances toward greater representation of thermally tolerant species (Galbraith et al. 2010). Given their taxonomic and life-history diversity, mussels probably have an array of shortand long-term acclimation strategies and varying abilities to cope with thermal stress, and these differences will determine outcomes of climate

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change. For example, in rivers where a large proportion of the fauna is widely distributed (e.g., the Upper Mississippi River), individual species might have wide thermal tolerances or might show a high degree of genotypic or phenotypic plasticity. In contrast, species with narrow geographic ranges may be less able to adapt to changing water temperatures. Understanding the short- and long-term thermal acclimation strategies will be critical to understanding how global climate change will alter mussel assemblages. Acknowledgements We thank Patty Ries and Donica Spence for help with heart-rate and growth-rate assessments and Greg Sandland for advice on statistical analysis. Two anonymous referees provided input that greatly improved this manuscript. This research was funded by the US Geological Survey (USGS) National Climate Change and Wildlife Science Center, the USGS Upper Midwest Environmental Sciences Center, and the University of Wisconsin–La Crosse. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government. Literature Cited APHA (AMERICAN PUBLIC HEALTH ASSOCIATION). 1995. Standard methods for the examination of water and wastewater. 19th edition. American Public Health Association, American Water Works Association, and Water Environment Federation, Washington, DC. ASTM (AMERICAN SOCIETY FOR TESTING AND MATERIALS). 1989. Standard practice for conducting static acute toxicity tests with larvae of four species of bivalve molluscs. E724-89. Annual book of ASTM standards. Volume 11.04. American Society for Testing and Materials, West Conshohocken, Pennsylvania. ASTM (AMERICAN SOCIETY FOR TESTING AND MATERIALS). 2006. Standard guide for conducting laboratory toxicity tests with freshwater mussels. E2455-06. Annual Book of ASTM standards. Volume 11.06. American Society for Testing and Materials, West Conshohocken, Pennsylvania. BAHR, D. B., M. DYURGEROV, AND M. F. MEIER. 2009. Sea-level rise from glaciers and ice caps: a lower bound. Geophysical Research Letters 36:L03501. doi:10.1029/ 2008GL036309 BALFOUR, D. L., AND L. A. SMOCK. 1995. Distribution, age structure, and movements of the freshwater mussel Elliptio complanata (Mollusca: Unionidae) in a headwater stream. Journal of Freshwater Ecology 10:255–268. BARNHART, M. C. 2006. Buckets of muckets: a compact system for rearing juvenile freshwater mussels. Aquaculture 254:227–233.

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Received: 21 November 2012 Accepted: 27 July 2013