Climate, Physiology, and Distributions: The Role of Thermal Physiology in Biological Invasions

Climate is a primary factor influencing species range dynamics, particularly for ectotherms whose body temperature is closely tied to the surrounding conditions. While range shifts of ectotherms are attributed to climate warming, the mechanism driving these shifts are not well understood. Studies in macrophysiology demonstrate that the interaction of climate with thermal physiology plays a key role in determining large-scale spatial and temporal patterns for many temperature-sensitive physiological traits. This work has revealed a clear relationship between thermal tolerance breadth and range size. However, more recent analyses of this relationship demonstrate that thermal tolerance breadth only provides a partial explanation for patterns in range size. Resting metabolism is a trait closely tied to energy balance, a key determinant of species distribution and abundance. At the whole-organism level, resting metabolism represents the energetic cost to fuel the maintenance of biological processes. Variation in this trait is related to climate and has a significant impact on how energy is allocated towards growth and reproduction. The aim of this dissertation was to understand the impact of climate on thermal physiology and species range dynamics using the Spongy moth (Lymantria dispar dispar) as a model system. The chapters of this dissertation addressed three primary questions: (Chapter 1) Do metabolic rate-temperature relationships (MR-T) vary across the invasive Spongy moth range and is that variation related to climate? (Chapter 2) How does MR-T vary with ontogeny? (Chapter 3) How does thermal performance at the cellular level compare to whole-organism performance? In the first chapter, we found that MR-T of third instar Spongy moth larvae showed significant variation among wild populations and this variation followed a latitudinal cline that was significantly related to climate variation. In the second chapter, larval MR-T showed significant variation across the first five instars of the larval stage. However, we found that the third instar was the most temperature-sensitive and showed the largest increase in metabolic rate after accounting for differences in body size among instars. In the third chapter, we found that whole-organism performance of metabolic rate and growth were mismatched at temperatures beyond the thermal optimum for growth and development of Spongy moth larvae. As temperature increased, metabolic rate continued to increase while growth rapidly declined. However, mitochondrial performance matched growth performance at these supraoptimal temperatures. Furthermore, this response of MR-T, growth, and mitochondrial performance was consistent across five Spongy moth populations. These results produced three primary conclusions. First, the latitudinal variation in whole-organism MR-T among Spongy moth populations was consistent with a pattern of thermal adaptation to divergent climates and suggests that Spongy moth populations have evolved in response to climate as they have spread and expanded their invasive range. Second, the thermal physiology of Spongy moth show significant variation during ontogeny. However, while MR-T does change with instar, our findings suggest it would not alter the conclusions of chapter 1 which is based on the third instar. Finally, the mismatch of MR-T with growth and mitochondrial performance follows the predictions made by the mitochondrial efficiency hypothesis which posits that changes in mitochondrial coupling efficiency is a key mechanism for reducing ectotherm performance. These provide strong evidence for a temperature-dependent link between mitochondria and whole-organism performance. The implications of these findings for the Spongy moth invasion, species range dynamics, and ectotherm performance are discussed further in each chapter

Energetic Consequences for a Northern, Range-Edge Lizard Population

Lizards at the northern, cool edge of their geographic range in the northern hemisphere should encounter environmental conditions that differ from those living near the core of their range. To better understand how modest climate differences affect lizard energetics, we compared daily feeding and metabolism rates of individual Sceloporus occidentalis in two populations during mid-summer. Chuckanut Beach (CB) was a cool, maritime climate in northern Washington State, and Sondino Ranch (SR) was a warmer, drier climate in southern, inland Washington. We found no difference between populations in daily energy expenditure (DEE), as calculated from doubly labeled water estimates. The CB population, however, had significantly higher prey availability and rate of daily energy intake (DEI) as estimated from fecal pellet masses. Consequently, CB lizards had higher size-adjusted body masses than lizards from SR. Within CB, during midsummer, DEE was similar to DEI. Within the SR population, DEE trended higher than DEI during midsummer, but was not significantly different. We found no population differences in lizard activity, active body temperature, or preferred body temperature. Hence, we infer the longer activity season for the SR population may compensate for the low food availability and high daily energy cost of midsummer. Moreover, for the CB population, we infer that cooler temperatures and higher food availability allow the lizards to compensate for the shorter activity. We also suggest the CB population may benefit from the predicted warmer temperatures associated with climate change given the similar activity-period body temperatures and DEE between these lizard populations assuming food availability is sufficient

How does spatial variation in climate cause spatiotemporal patterns in lizard energetics?

Sceloporus occidentalis occurs in two locales near the northern end of its geographic range that contrast markedly in climate. Both locales are in Washington state; one is cool, moist coastal temperate forest and the other is warm, dry pine-oak woodland in the state\u27s interior. The focus of this thesis was to investigate differences in lizard production and population structure between these locales by correlating daily and seasonal patterns of temperature, precipitation, and cloud cover with the measured and estimated patterns of lizard activity, energy expenditure, feeding rates and food availability. Based on air temperature records, the estimated activity season length for Sceloporus occidentalis was greater at the inland locale, at 207 days than at the coastal locale, at 191 days. Within the activity season there were more 138 warm, sunny days available for S. occidentalis activity at the inland locale, but only there were only 79 of these days available at the coastal locale. Daily activity on these sunny days was estimated to be about 9.5 hours at both locales. The combination of equal foraging time available at both locales on warm sunny days during mid-summer and higher arthropod abundances at the coastal locale in mid-summer were correlated with higher rates of daily fecal production by the coastal lizards (0.0252 g • g-1 • d-1) than by the inland lizards (0.0221 g • g-1 • d-1). Hence, calculated food intake rates of coastal lizards (0.0360 kJ • g-1 • d-1) were greater than food intake rates of inland lizards (0.0165 kJ • g-1 • d-1). Water influx rates, as measured by the doubly-labeled water technique corroborated the fecal production analysis. Moreover, the daily field metabolism of lizards at the two locales were similar during mid-summer, corroborating the similar activity period estimates based on weather data. Despite lower rates of lizard production during mid-summer for inland S. occidentalis, the greater number of days available for activity during the activity season for the inland lizards, and the larger body sizes reached by one-year old lizards inland provides correlative evidence from which to infer that inland lizards may become reproductive at an earlier age. Relative to the coastal S. occidentalis, the inland lizards (1) hatch 2 -- 3 weeks earlier, (2) have a longer activity season into the fall, (3) followed by an earlier beginning to the activity season in the spring, and (4) presumably have adequate food availability for growth when active. Both locales are in the northern portion of the geographic range of Sceloporus occidentalis. The expectations are that climate change will result in longer activity seasons for lizards at both locales, and that heat of summer may be severe for the inland population, perhaps necessitating migration of the inland population further upslope and further west toward cooler and more mesic conditions. But if one considers the many possible anthropogenic effects on the landscape as well as the potentially rapid rate of climate change, it is unclear whether there will be available habitat to be occupied upslope and further west, thus possibly imperiling inland populations of Sceloporus occidentalis

Unintended Facilitation Between Marine Consumers Generates Enhanced Mortality for Their Shared Prey

We manipulated predator densities and prey vulnerability to explore how interactions between two predators affect overall mortality of their shared prey. Our threemember study system included eastern oysters (Crassostrea virginica) and two of its major consumers: southern oyster drills (Stramonita haemastoma) and stone crabs (Menippe adina). Field experiments demonstrated that drills and crabs foraging together generated higher than expected oyster mortality based on each species operating independently, even though crabs also killed some drills. In subsequent laboratory trials, we experimentally mimicked the handling of oysters by foraging crabs and confirmed that crabs facilitated drills by breeching oyster valves, thereby granting easy access for drills to their prey. Facilitation between cooccurring predators is uncommon and typically occurs because the behavior or habitat selection of a prey species is altered by the presence of one predator, consequently making the prey more susceptible to another predator. Whereas oysters are sedentary regardless of the predator field, we observed an entirely different mechanism that resulted in predator facilitation. This involved direct attacks on the physical defenses of oysters by one predator that ultimately increased the overall consumption rate of foraging species. These dynamics significantly enhanced mortality risk for a foundation species within an estuarine ecosystem

Respiratory Evaporative Water Loss During Hovering and Forward Flight in Hummingbirds

Hummingbirds represent an end point for small body size and water flux in vertebrates. We explored the role evaporative water loss (EWL) plays in management of their large water pool and its use in dissipating metabolic heat. We measured respiratory evaporative water loss (REWL) in hovering hummingbirds in the field (6 species) and over a range of speeds in a wind tunnel (1 species) using an open-circuit mask respirometry system. Hovering REWL during the active period was positively correlated with operative temperature (Te) likely due to some combination of an increase in the vapor-pressure deficit, increase in lung ventilation rate, and reduced importance of dry heat transfer at higher Te. In rufous hummingbirds (Selasphorus rufus; 3.3 g) REWL during forward flight at 6 and 10 m/s was less than half the value for hovering. The proportion of total dissipated heat (TDH) accounted for by REWL during hovering at Te\u3e40 °C was b40% in most species. During forward flight in S. rufus the proportion of TDH accounted for by REWL was ~35% less than for hovering. REWL in hummingbirds is a relatively small component of the water budget compared with other bird species (b20%) so cutaneous evaporative water loss and dry heat transfer must contribute significantly to thermal balance in hummingbirds

Integrating Societal Perspectives and Values for Improved Stewardship of a Coastal Ecosystem Engineer

Oyster reefs provide coastal societies with a vast array of ecosystem services, but are also destructively harvested as an economically and culturally important fishery resource, exemplifying a complex social-ecological system (SES). Historically, societal demand for oysters has led to destructive and unsustainable levels of harvest, which coupled with multiple other stressors has placed oyster reefs among the most globally imperiled coastal habitats. However, more recent studies have demonstrated that large-scale restoration is possible and that healthy oyster populations can be sustained with effective governance and stewardship. However, both of these require significant societal support or financial investment. In our study, we explored relationships among how coastal societies (1) perceive and value oyster ecosystem services, (2) recognize and define problems associated with oyster decline, and (3) perceive or support stewardship initiatives. We specifically focused on the SES of eastern oysters (Crassostrea virginica) and coastal societies in the northern Gulf of Mexico, a region identified as offering among the last and best opportunities to sustainably balance conservation objectives with a wild fishery. We found that, in addition to harvest-related benefits, oysters were highly valued for providing habitat, mitigating shoreline erosion, and improving water quality or clarity. Our results also showed that although most respondents recognized that oyster populations have declined, many respondents characterized the problem differently than most scientific literature does. Among a variety of initiatives for enhancing sustainability, spawning sanctuaries and reef restoration were well supported in all states, but support for harvest reductions was less consistent. Our study suggests that public support for maintaining both harvest and ecosystem services exists at societal levels and that enhancing public awareness regarding the extent and causes of oyster decline could garner additional support for stewardship initiatives. Collectively, the societal, economic, and biophysical complexities of the northern Gulf of Mexico oyster SES illustrate the need and public support for developing more comprehensive management schemes for exploited ecosystem engineers

Red Snapper Distribution on Natural Habitats and Artificial Structures in the Northern Gulf of Mexico

In 2011, an intensive, multiple-gear, fishery-independent survey was carried out in the northern Gulf of Mexico (GOM) to collect comprehensive age and length information on Red Snapper Lutjanus campechanus. Based on this synoptic survey, we produced a spatial map of Red Snapper relative abundance that integrates both gear selectivity effects and ontogenetically varying habitat usage. Our methodology generated a spatial map of Red Snapper at a 10-km2 grid resolution that is consistent with existing knowledge of the species: Red Snapper occurred in relatively high abundances at depths of 50–90 m along the coasts of Texas and Louisiana and in smaller, patchy “hot spots” at a variety of depths along the Alabama coast and the west Florida shelf. Red Snapper biomass and fecundity estimates were higher for the northwestern GOM than for the northeastern GOM, as the latter area contained mostly smaller, younger individuals. The existence of similar surveys on petroleum platforms and artificial reefs also enabled us to calculate their relative contribution to Red Snapper distribution compared with that of natural habitats.We estimated that for the youngest ageclasses, catch rates were approximately 20 times higher on artificial structures than on natural reefs. Despite the high catch rates observed on artificial structures, they represent only a small fraction of the total area in the northern GOM; thus, we estimated that they held less than 14%of Red Snapper abundance. Because artificial structures—particularly petroleum platforms—attract mostly the youngest individuals, their contribution was even lower in terms of total population biomass (7.8%) or spawning potential (6.4%). Our estimates of Red Snapper relative abundance, biomass, and spawning potential can be used to design spatial management strategies or as inputs to spatial modeling techniques

Climate-Related Geographical Variation in Performance Traits across the Invasion Front of a Widespread Non-Native Insect

Aim Invasive species are ideal systems for testing geographical differences in performance traits and measuring evolutionary responses as a species spreads across divergent climates and habitats. The European gypsy moth, Lymantria dispar dispar L. (Lepidoptera: Erebidae), is a generalist forest defoliator introduced to Medford, Massachusetts, USA in 1869. The invasion front extends from Minnesota to North Carolina and the ability of this species to adapt to local climate may contribute to its continuing spread. We evaluated the performance of populations along the climatic gradient of the invasion front to test for a relationship between climate and ecologically important performance traits. Location Eastern United States of America Taxon Lymantria dispar dispar L. (Lepidoptera: Erebidae) Methods Insects from 14 populations across the US invasion front and interior of the invasive range were reared from hatch to adult emergence in six constant temperature treatments. The responses of survival, pupal mass and larval development time were analysed as a function of source climate (annual mean normal temperature), rearing temperature and their interaction using multiple polynomial regression. Results With the exception of female development time, there were no significant interactions between source climate and rearing temperature, indicating little divergence in the shape of thermal reaction norms among populations. Source population and rearing temperature were significant predictors of survival and pupal mass. Independent of rearing temperature, populations from warmer climates had lower survival than those from colder climates, but attained larger body size despite similar development times. Larval development time was dependent on rearing temperature, but there were not consistent relationships with source climate. Main Conclusions Thermal adaptation can be an important factor shaping the spread of invasive species, particularly in the context of climate change. Our results suggest that L. d. dispar is highly plastic, but has undergone climate-related adaptation in thermal performance and life-history traits as it spread across North America

Historical ecology with real numbers: past and present extent and biomass of an imperiled estuarine habitat

Historic baselines are important in developing our understanding of ecosystems in the face of rapid global change. While a number of studies have sought to determine changes in extent of exploited habitats over historic timescales, few have quantified such changes prior to late twentieth century baselines. Here, we present, to our knowledge, the first ever large-scale quantitative assessment of the extent and biomass of marine habitat-forming species over a 100-year time frame. We examined records of wild native oyster abundance in the United States from a historic, yet already exploited, baseline between 1878 and 1935 (predominantly 1885–1915), and a current baseline between 1968 and 2010 (predominantly 2000–2010). We quantified the extent of oyster grounds in 39 estuaries historically and 51 estuaries from recent times. Data from 24 estuaries allowed comparison of historic to present extent and biomass. We found evidence for a 64 per cent decline in the spatial extent of oyster habitat and an 88 per cent decline in oyster biomass over time. The difference between these two numbers illustrates that current areal extent measures may be masking significant loss of habitat through degradation

Coordinated Unmanned Aircraft System (UAS) and Ground-Based Weather Measurements to Predict Lagrangian Coherent Structures (LCSs)

Concentrations of airborne chemical and biological agents from a hazardous release are not spread uniformly. Instead, there are regions of higher concentration, in part due to local atmospheric flow conditions which can attract agents. We equipped a ground station and two rotary-wing unmanned aircraft systems (UASs) with ultrasonic anemometers. Flights reported here were conducted 10 to 15 m above ground level (AGL) at the Leach Airfield in the San Luis Valley, Colorado as part of the Lower Atmospheric Process Studies at Elevation—a Remotely-Piloted Aircraft Team Experiment (LAPSE-RATE) campaign in 2018. The ultrasonic anemometers were used to collect simultaneous measurements of wind speed, wind direction, and temperature in a fixed triangle pattern; each sensor was located at one apex of a triangle with ∼100 to 200 m on each side, depending on the experiment. A WRF-LES model was used to determine the wind field across the sampling domain. Data from the ground-based sensors and the two UASs were used to detect attracting regions (also known as Lagrangian Coherent Structures, or LCSs), which have the potential to transport high concentrations of agents. This unique framework for detection of high concentration regions is based on estimates of the horizontal wind gradient tensor. To our knowledge, our work represents the first direct measurement of an LCS indicator in the atmosphere using a team of sensors. Our ultimate goal is to use environmental data from swarms of sensors to drive transport models of hazardous agents that can lead to real-time proper decisions regarding rapid emergency responses. The integration of real-time data from unmanned assets, advanced mathematical techniques for transport analysis, and predictive models can help assist in emergency response decisions in the future