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Research in thermal biology: Burning questions for coldwater stream fishes

With the increasing appreciation of global warming impacts on ecological systems, in addition to the myriad of land management effects on water quality, the number of literature citations dealing with the effects of water temperature on freshwater fish has escalated in the past decade. Given the many biological scales at which water temperature effects have been studied, and the growing need to integrate knowledge from multiple disciplines of thermal biology to fully protect beneficial uses, we held that a survey of the most promising recent developments and an expression of some of the remaining unanswered questions with significant management implications would best be approached collectively by a diverse research community. We have identified five specific topic areas of renewed research where new techniques and critical thought could benefit coldwater stream fishes (particularly salmonids): molecular, organism, population/species, community and ecosystem, and policy issues in water quality. Our hope is that information gained through examination of recent research fronts linking knowledge at various scales will prove useful in managing water quality at a basin level to protect fish populations and whole ecosystems. Standards of the past were based largely on incipient lethal and optimum growth rate temperatures for fish species, while future standards should consider all integrated thermal impacts to the organism and ecosystem. ?? Taylor and Francis Group, LLC.

Reviews in Fisheries Science

Ecology of urban climates: The need for landscape biophysics in cities

In this chapter we will review and evaluate the climatic and ecological parallels between urbanization and climate change, with an emphasis on temperature and its effects on terrestrial ectotherms, a group of organisms thought to be particularly sensitive to climate change. We will summarize patterns of urban warming and how they relate to global climate change projections, then discuss the potential strengths and limitations of urban climates as a source of insight into biotic responses to climate change and highlight future research directions. Future work will benefit from explicit consideration of the mechanisms by which urbanization and urban warming drive ectotherms’ body temperatures and activity periods. Urban ecosystems may provide a valuable first approximation of the dramatic effects of warming on certain terrestrial systems, and continued advances in urban thermal biology will promote a mechanistic understanding of how organisms use, respond to, and adapt to the unique thermal landscapes of cities.

Book chapter

Cold-induced mortality of invasive Burmese pythons in south Florida

A recent record cold spell in southern Florida (2–11 January 2010) provided an opportunity to evaluate responses of an established population of Burmese pythons ( Python molurus bivittatus ) to a prolonged period of unusually cold weather. We observed behavior, characterized thermal biology, determined fate of radio-telemetered ( n = 10) and non-telemetered ( n = 104) Burmese pythons, and analyzed habitat and environmental conditions experienced by pythons during and after a historic cold spell. Telemetered pythons had been implanted with radio-transmitters and temperature-recording data loggers prior to the cold snap. Only one of 10 telemetered pythons survived the cold snap, whereas 59 of 99 (60%) non-telemetered pythons for which we determined fate survived. Body temperatures of eight dead telemetered pythons fluctuated regularly prior to 9 January 2010, then declined substantially during the cold period (9–11 January) and exhibited no further evidence of active thermoregulation indicating they were likely dead. Unusually cold temperatures in January 2010 were clearly associated with mortality of Burmese pythons in the Everglades. Some radio-telemetered pythons appeared to exhibit maladaptive behavior during the cold spell, including attempting to bask instead of retreating to sheltered refugia. We discuss implications of our findings for persistence and spread of introduced Burmese pythons in the United States and for maximizing their rate of removal.

Florida

Temperature impacts on dengue incidence are nonlinear and mediated by climatic and socioeconomic factors: A meta-analysis

Temperature can influence mosquito-borne diseases like dengue. These effects are expected to vary geographically and over time in both magnitude and direction and may interact with other environmental variables, making it difficult to anticipate changes in response to climate change. Here, we investigate global variation in temperature–dengue relationship by analyzing published correlations between temperature and dengue and matching them with remotely sensed climatic and socioeconomic data. We found that the correlation between temperature and dengue was most positive at intermediate (near 24°C) temperatures, as predicted from an independent mechanistic model. Positive temperature–dengue associations were strongest when temperature variation and population density were high and decreased with infection burden and rainfall mean and variation, suggesting alternative limiting factors on transmission. Our results show that while climate effects on diseases are context-dependent they are also predictable from the thermal biology of transmission and its environmental and social mediators.

PLOS Climate

Best practices for continuous monitoring of temperature and flow in wadeable streams

The United States Environmental Protection Agency (U.S. EPA) is working with its regional offices, states, tribes, river basin commissions and other entities to establish Regional Monitoring Networks (RMNs) for freshwater wadeable streams. To the extent possible, uninterrupted, biological, temperature and hydrologic data will be collected on an ongoing basis at RMN sites, which are primarily located on smaller, minimally disturbed forested streams. The primary purpose of this document is to provide guidance on how to collect accurate, year-round temperature and hydrologic data at ungaged wadeable stream sites. It addresses questions related to equipment needs, sensor configuration, sensor placement, installation techniques, data retrieval, and data processing. This guidance is intended to increase comparability of continuous temperature and hydrologic data collection at RMN sites and to ensure that the data are of sufficient quality to be used in future analyses. It also addresses challenges posed by year-round deployments. These data will be used for detecting temporal trends; providing information that will allow for a better understanding of relationships between biological, thermal, and hydrologic data; predicting and analyzing climate change impacts and quantifying natural variability.

Report

Importance of microscopy in durability studies of solidified and stabilized contaminated soils

Solidification/stabilization (S/S) is recognized by the U.S. EPA as a best demonstrated available technology for the containment of contaminated soils and other hazardous wastes that cannot be destroyed by chemical, thermal, or biological means. Despite the increased use of S/S technologies, little research has been conducted on the weathering and degradation of solidified and stabilized wastes once the treated materials have been buried. Published data to verify the performance and durability of landfilled treated wastes over time are rare. In this preliminary study, optical and electron microscopy (scanning electron microscopy [SEM], transmission electron microscopy [TEM] and electron probe microanalyses [EPMA]) were used to evaluate weathering features associated with metal-bearing contaminated soil that had been solidified and stabilized with Portland cement and subsequently buried on site, stored outdoors aboveground, or achieved in a laboratory warehouse for up to 6 yr. Physical and chemical alteration processes identified include: freeze-thaw cracking, cracking caused by the formation of expansive minerals such as ettringite, carbonation, and the movement of metals from waste aggregates into the cement micromass. Although the extent of degradation after 6 yr is considered slight to moderate, results of this study show that the same environmental concerns that affect the durability of concrete must be considered when evaluating the durability and permanence of the solidification and stabilization of contaminated soils with cement. In addition, such evaluations cannot be based on leaching and chemical analyses alone. The use of all levels of microscopic analyses must be incorporated into studies of the long-term performance of S/S technologies.Solidification/stabilization (S/S) is recognized by the U.S. EPA as a best demonstrated available technology for the containment of contaminated soils and other hazardous wastes that cannot be destroyed by chemical, thermal, or biological means. Despite the increased use of S/S technologies, little research has been conducted on the weathering and degradation of solidified and stabilized wastes once the treated materials have been buried. Published data to verify the performance and durability of landfilled treated wastes over time are rare. In this preliminary study, optical and electron microscopy (scanning electron microscopy [SEM], transmission electron microscopy [TEM] and electron probe microanalyses [EPMA]) were used to evaluate weathering features associated with metal-bearing contaminated soil that had been solidified and stabilized with Portland cement and subsequently buried on site, stored outdoors aboveground, or archived in a laboratory, warehouse for up to 6 yr. Physical and chemical alteration processes identified include: freeze-thaw cracking, cracking caused by the formation of expansive minerals such as ettringite, carbonation, and the movement of metals from waste aggregates into the cement micromass. Although the extent of degradation after 6 yr is considered slight to moderate, results of this study show that the same environmental concerns that affect the durability of concrete must be considered when evaluating the durability and permanence of the solidification and stabilization of contaminated soils with cement. In addition, such evaluations cannot be based on leaching and chemical analyses alone. The use of all levels of microscopic analyses must be incorporated into studies of the long-term performance of S/S technologies.

Soil Science Society of America Journal

Using the electron transport system as an indicator of organismal thermal tolerance and respiratory exploitation

Freshwater ecosystems are undergoing rapid thermal shifts, making it increasingly important to understand species-specific responses to these changes. Traditional techniques for determining a species’ thermal tolerance are often lethal and time consuming. Using the enzyme activity associated with the electron transport system (ETS; hereafter referred to as enzyme assay) may provide a non-lethal, rapid, and efficient alternative to traditional techniques for some species. We used largemouth bass Micropterus salmoides (Lacepede, 1802) to test the efficacy of using an enzyme assay to determine thermal tolerance and respiratory exploitation in response to variable acclimation temperatures. Three tissue types were dissected from fish acclimated to 20, 25, or 30 °C and used in ETS assays at temperatures ranging from 7.5 to 40 °C. While there were significant differences among tissue types and acclimation temperatures, maximal enzyme activity occurred from 25.23 to 31.91 °C. Fish lost equilibrium at 39–42 °C in traditional CT max trials, significantly higher than the upper optimum range determined via enzyme assays. The ratio of enzyme activity to measured whole organism respiration rate decreased with increasing water temperature, with the largest changes occurring at the upper optimum thermal range determined by enzyme assays. Our results indicate that ETS analysis may prove useful for obtaining biologically relevant thermal tolerances.

Canadian Journal of Zoology

Physically modeling operative temperatures and evaporation rates in amphibians

(1) We designed a physical model that simulates the thermal and evaporative properties of live Western toads ( Bufo boreas ). (2) In controlled tests, the model tracked the body temperature of live toads with an average error of 0.3±0.03 °C (test range=4–30 °C). (3) It estimated the evaporative water loss of live toads with an average error of 0.35–0.65 g/h, or about 14% (test range=0.7–9 g/h). (4) Data collected with this physical model should provide an effective way for biologists to better understand habitat selection in toads and other amphibians.

Journal of Thermal Biology

Sex, season, and time of day interact to affect body temperatures of the Giant Gartersnake

1.We examined multiple hypotheses regarding differences in body temperatures of the Giant Gartersnake using temperature-sensitive radio telemetry and an information-theoretic analytical approach.2.Giant Gartersnakes selected body temperatures near 30 ??C, and males and females had similar body temperatures most of the year, except during the midsummer gestation period.3.Seasonal differences in the body temperatures of males and females may relate to both the costs associated with thermoregulatory behavior, such as predation, and the benefits associated with maintaining optimal body temperatures, such as successful incubation.

Journal of Thermal Biology

Using motion-sensor camera technology to infer seasonal activity and thermal niche of the desert tortoise ( Gopherus agassizii )

Understanding the relationships between environmental variables and wildlife activity is an important part of effective management. The desert tortoise ( Gopherus agassizii ), an imperiled species of arid environments in the southwest US, may have increasingly restricted windows for activity due to current warming trends. In summer 2013, we deployed 48 motion sensor cameras at the entrances of tortoise burrows to investigate the effects of temperature, sex, and day of the year on the activity of desert tortoises. Using generalized estimating equations, we found that the relative probability of activity was associated with temperature (linear and quadratic), sex, and day of the year. Sex effects showed that male tortoises are generally more active than female tortoises. Temperature had a quadratic effect, indicating that tortoise activity was heightened at a range of temperatures. In addition, we found significant support for interactions between sex and day of the year, and sex and temperature as predictors of the probability of activity. Using our models, we were able to estimate air temperatures and times (days and hours) that were associated with maximum activity during the study. Because tortoise activity is constrained by environmental conditions such as temperature, it is increasingly vital to conduct studies on how tortoises vary their activity throughout the Sonoran Desert to better understand the effects of a changing climate.

California

Seasonal thermal ecology of adult walleye (Sander vitreus) in Lake Huron and Lake Erie

The purpose of this study was to characterize thermal patterns and generate occupancy models for adult walleye from lakes Erie and Huron with internally implanted biologgers coupled with a telemetry study to assess the effects of sex, fish size, diel periods, and lake. Sex, size, and diel periods had no effect on thermal occupancy of adult walleye in either lake. Thermal occupancy differed between lakes and seasons. Walleye from Lake Erie generally experienced higher temperatures throughout the spring and summer months than did walleye in Lake Huron, due to limnological differences between the lakes. Tagged walleye that remained in Saginaw Bay, Lake Huron (i.e., adjacent to the release location), as opposed to those migrating to the main basin of Lake Huron, experienced higher temperatures, and thus accumulated more thermal units (the amount of temperature units amassed over time) throughout the year. Walleye that migrated toward the southern end of Lake Huron occupied higher temperatures than those that moved toward the north. Consequently, walleye that emigrated from Saginaw Bay experienced thermal environments that were more favorable for growth as they spent more time within their thermal optimas than those that remained in Saginaw Bay. Results presented in this paper provide information on the thermal experience of wild fish in a large lake, and could be used to refine sex- and lake-specific bioenergetics models of walleye in the Great Lakes to enable the testing of ecological hypotheses.

Journal of Thermal Biology

The effects of fire on the thermal environment of sagebrush communities

Thermal heterogeneity provides options for organisms during extreme temperatures that can contribute to their fitness. Sagebrush ( Artemisia spp.) communities exhibit vegetation heterogeneity that creates thermal variation at fine spatial scales. However, fire can change vegetation and thereby variation within the thermal environment of sagebrush communities. To describe spatial and temporal thermal variation of sagebrush communities following wildfire, we measured black bulb temperature ( T bb ) at 144 random points dispersed within unburned and burned communities, for 24-h at each random point. We observed a wide thermal gradient in unburned (−7.3° to 63.3 °C) and burned (−4.6° to 64.8 °C) sagebrush communities. Moreover, unburned and burned sagebrush communities displayed high thermal heterogeneity relative to ambient temperature ( T air ). Notably, T bb varied by 47 °C in both unburned and burned communities when T air was 20 °C. However, fire greatly reduced the buffering capacity and thermal refuge of Wyoming big sagebrush ( A. tridentata wyomingensis ) communities during low and high T air . Furthermore, fire increased T bb in Wyoming big sagebrush and mountain big sagebrush ( A. t. vaseyana ) during the mid-day hours. These results demonstrate how fire changes the thermal environment of big sagebrush communities and the importance of shrub structure which can provide thermal refuge for organisms in burned communities during extreme low and high T air .

Journal of Thermal Biology

Shifts in hatching date of American crocodile (Crocodylus acutus) in southern Florida

Globally temperature of marine environments is on the rise and temperature plays an important role in the life-history of reptiles. In this study, we examined the relationship between sea surface temperature and average date of hatching for American crocodiles (Crocodylus acutus) over a 37-year period at two nesting sites, Everglades National Park and Florida Power and Light Turkey Point Power Plant site in southern Florida. Our results indicate that hatch dates are shifting 1.5 days earlier every two years and at half that rate for the Turkey Point site, and with every 1 °C degree increase in temperature, hatching occurs about 10 days earlier in the Everglades and 6 days earlier at Turkey Point. Our results on shifting hatch dates for American crocodiles provide further details about the impacts of temperature change on crocodile life history and suggest that increased temperature may affect their phenology.

Florida

How repeatable is CTmax within individual brook trout over short- and long-time intervals?

As stream temperatures increase due to factors such as heated runoff from impervious surfaces, deforestation, and climate change, fish species adapted to cold water streams are forced to move to more suitable habitat, acclimate or adapt to increased thermal regimes, or die. To estimate the potential for adaptation, a (within individual) repeatable metric of thermal tolerance is imperative. Critical thermal maximum (CTmax) is a dynamic test that is widely used to measure thermal tolerance across many taxa and has been used in fishes for decades, but its repeatability in most species is unknown. CTmax tests increase water temperature steadily over time until loss of equilibrium (LOE) is achieved. To determine if CTmax is a consistent metric within individual fish, we measured CTmax on the same lab-held individually-marked adult brook trout Salvelinus fontinalis at three different times (August & September 2016, September 2017). We found that CTmax is a repeatable trait (Repeatability ± S.E.: 0.48 ± 0.14). CTmax of individuals males was consistent over time, but the CTmax of females increased slightly over time. This result indicates that CTmax is a robust, repeatable estimate of thermal tolerance in a cold-water adapted fish.

Journal of Thermal Biology

Plasticity of Least Tern and Piping Plover nesting behaviors in response to sand temperature

Birds that nest on the ground in open areas, such as Piping Plovers ( Charadrius melodus ) and Interior Least Terns ( Sternula antillarum athalassos ), are exposed to high temperatures in thermally stressful environments. As a result, some ground-nesting avian species have adapted behavioral strategies to maintain thermal regulation of eggs and themselves. We assessed the impact of sand temperature on shorebird nesting behaviors by installing video cameras and thermocouples at 52 Least Tern and 55 Piping Plover nests on the Missouri River in North Dakota during the 2014–2015 breeding seasons. Daily duration and frequency of shading behaviors exhibited a nonlinear relationship with temperature; therefore, we used segmented regressions to determine at what threshold temperature (mean temperature = 25.7 ⸰ C for shading behavior daily frequency and mean temperature = 25.1 ⸰ C for shading behavior daily duration) shorebird adults exhibited a behavioral response to rising sand temperatures. Daily nest attendance of both species decreased with increasing sand temperatures in our system. Frequency and duration of daily shading behaviors were positively correlated with sand temperatures above the temperature threshold. Piping Plovers exhibited more and longer shading behaviors above and below the temperature thresholds (below: frequency = 10.30 ± 1.69 se, duration = 7.29 min ± 2.35 se; above: frequency = 59.27 ± 6.87 se) compared to Least Terns (below: frequency = −1.37 ± 1.98 se, duration = −0.73 min ± 1.51 se; above: frequency = 31.32 ± 7.29 se). The effects of sand temperature on avian ground-nesting behavior will be critical to understand in order to adapt or develop recovery plans in response to climate change.

North Dakota

Integrating thermal infrared stream temperature imagery and spatial stream network models to understand natural spatial thermal variability in streams

Under a warmer future climate, thermal refuges could facilitate the persistence of species relying on cold-water habitat. Often these refuges are small and easily missed or smoothed out by averaging in models. Thermal infrared (TIR) imagery can provide empirical water surface temperatures that capture these features at a high spatial resolution (<1 m) and over tens of kilometers. Our study examined how TIR data could be used along with spatial stream network (SSN) models to characterize thermal regimes spatially in the Middle Fork John Day (MFJD) River mainstem (Oregon, USA). We characterized thermal variation in seven TIR longitudinal temperature profiles along the MFJD mainstem and compared them with SSN model predictions of stream temperature (for the same time periods as the TIR profiles). TIR profiles identified reaches of the MFJD mainstem with consistently cooler temperatures across years that were not consistently captured by the SSN prediction models. SSN predictions along the mainstem identified ~80% of the 1-km reach scale temperature warming or cooling trends observed in the TIR profiles. We assessed whether landscape features (e.g., tributary junctions, valley confinement, geomorphic reach classifications) could explain the fine-scale thermal heterogeneity in the TIR profiles (after accounting for the reach-scale temperature variability predicted by the SSN model) by fitting SSN models using the TIR profile observation points. Only the distance to the nearest upstream tributary was identified as a statistically significant landscape feature for explaining some of the thermal variability in the TIR profile data. When combined, TIR data and SSN models provide a data-rich evaluation of stream temperature captured in TIR imagery and a spatially extensive prediction of the network thermal diversity from the outlet to the headwaters.

Oregon

Tolerance of northern Gulf of Mexico eastern oysters to chronic warming at extreme salinities

The eastern oyster, Crassostrea virginica , provides critical ecosystem services and supports valuable fishery and aquaculture industries in northern Gulf of Mexico (nGoM) subtropical estuaries where it is grown subtidally. Its upper critical thermal limit is not well defined, especially when combined with extreme salinities. The cumulative mortalities of the progenies of wild C. virginica from four nGoM estuaries differing in mean annual salinity, acclimated to low (4.0), moderate (20.0), and high (36.0) salinities at 28.9 °C (84 °F) and exposed to increasing target temperatures of 33.3 °C (92 °F), 35.6 °C (96 °F) or 37.8 °C (100 °F), were measured over a three-week period. Oysters of all stocks were the most sensitive to increasing temperatures at low salinity, dying quicker (i.e., lower median lethal time, LT 50 ) than at the moderate and high salinities and resulting in high cumulative mortalities at all target temperatures. Oysters of all stocks at moderate salinity died the slowest with high cumulative mortalities only at the two highest temperatures. The F1 oysters from the more southern and hypersaline Upper Laguna Madre estuary were generally more tolerant to prolonged higher temperatures (higher LT 50 ) than stocks originating from lower salinity estuaries, most notably at the highest salinity. Using the measured temperatures oysters were exposed to, 3-day median lethal Celsius degrees (LD 50 ) were estimated for each stock at each salinity. The lowest 3-day LD 50 (35.1–36.0 °C) for all stocks was calculated at a salinity of 4.0, while the highest 3-day LD 50 (40.1–44.0 °C) was calculated at a salinity of 20.0.

Louisiana, Texas

How quickly do brook trout lose long-term thermal acclimation?

Abundances of coldwater adapted stream fish populations are declining largely due to anthropogenic influences, including increased temperature. To persist in streams with unsuitable thermal habitat, fish must move to coldwater patches, acclimate, or adapt to water temperatures above thermal optima. Brook trout, a coldwater adapted salmonid, has previously displayed physiological plasticity and the ability for reversible thermal acclimation when reared at higher temperatures. However, because stream temperatures are not static, it is important to explore the rate at which thermal acclimation occurs to evaluate whether prior thermal experience will influence future thermal performance. To determine the temporal scale in loss of thermal acclimation as water temperatures cool, we acclimated brook trout to three thermal regimes: +0 °C (ambient; mimicking the daily average water temperature of a nearby long-term study site), as well as +2 °C and +4 °C above ambient. After 2 years of being reared under those conditions, fish from the warmer treatments were moved to a common, colder temperature (ambient). We then used critical thermal maximum to measure the loss in acclimation response of fish from each treatment over time. We found that regardless of initial acclimation temperature, thermal tolerance of warm acclimated fish decreased rapidly for 1 week, then gradually decreased, and was completely lost within 42 days. This gradual loss of acclimation may be valuable to persistence in warmer streams and will be important to include in models of the impact climate change has on brook trout and other aquatic ectotherms with significant thermal plasticity.

Massachusetts