David L. Swanson: Research Interests

• Evolution of metabolic patterns in birds. A major research focus in my laboratory is the evolution of metabolic patterns in birds, principally focusing on the passerine birds or songbirds. Small birds that are resident in cold climates generally show marked winter increases in thermogenic capacity (overall capacity for heat production) that are accompanied by winter increases in cold hardiness. Thus, high thermogenic capacity appears to be a feature typical of birds wintering in cold climates. Our lab is interested in how selection for cold hardiness may have influenced whole-organism metabolic patterns in birds and how such past selection may affect present-day bird distributions. By investigating variation in thermogenic capacity and cold hardiness in birds with different lifestyles (e.g., migrants vs. residents) and among different avian taxa, and incorporating data on avian phylogeny and climatic evolution, we hope to elucidate fundamental relationships among cold, metabolic physiology and biogeography in birds.

          Current Projects:

• To address the question of whether thermogenic capacity varies with overwintering climate or phylogeny we are conducting comparative analyses of summit metabolic rates (M_sum, maximum cold-induced metabolic rates) in migrant and cold-climate resident birds from a diversity of avian taxa. We are also examining whether bird groups with high-enegy lifestyles (e.g., arctic-breeding shorebirds, aerial insectivores) achieve high maximal exercise and/or thermogenic metabolic rates as a by-product of their lifestyle. For example, we found that swallows, which are aerial insectivores that spend most of the day flying, had significantly higher BMR, but not Msum, compared to non-aerial insectivore birds (see Figure; data from Zhang et al. 2021. Ornithology 138: In press). Results from these studies should elucidate important factors in the evolution of thermogenic capacity in birds and this should, in turn, inform us of whether the evolution of high exercise or thermogenic capacities along with increases in cold tolerance in birds played an important role in the evolution of current biogeographic distributions.

• We are also currently examining the relationships among exercise maximum metabolic rates (MMR, using a hop-flutter wheel), summit metabolic rates (M_sum), and basal metabolic rates (BMR) in individual birds. Both sustained exercise and prolonged shivering are forms of endurance muscular activity, so physiological adjustments promoting endurance may enhance both exercise and shivering performance. If so, then MMR and M_sum should show correlated phenotypic variation among individual birds. In addition, if increases in exercise and shivering capacities incur support and maintenance costs, then BMR should also show correlated phenotypic variation with MMR and M_sum, as suggested by the aerobic capacity model for the evolution of endothermy.

My lab is also interested in the relationship between climatic variability and metabolic flexibility in birds. The climatic variability hypothesis (CVH) proposes that populations from more variable climates should show greater physiological flexibility. We have recently been studying extensions of the CVH to within-population metabolic variation between seasons in year-round resident birds. Because winter temperatures are more variable than summer temperatures, it might be expected that winter birds would show greater metabolic flexibility in response to temperature acclimation. Recent data from house sparrows do not support this hypothesis, as metabolic rates tended to be upregulated with cold acclimation in summer, but downregulated with both cold and warm acclimation in winter (see Swanson et al. 2020 Integrative Organismal Biology 2:obaa039), suggesting that the CVH does not apply to within-population responses to seasonal climatic variation. Our lab is also currently studying whether the CVH might apply to sympatric bird species occupying microclimates that differ in temperature variability. We quantified that open, exposed habitats, including grasslands and agricultural fields, show greater daily and seasonal temperature variability that wooded, sheltered habitats. Horned larks from open habitats showed greater seasonal variation in basal and summit (maximum cold-induced) metabolic rates than house sparrows from more sheltered habitats. These data suggest that the CVH may apply to sympatric bird species occupying microclimates that differ in temperature variability, but more research is needed on a wider variety of bird species from different microclimates to verify the generality of this result.

• Mechanisms of seasonal phenotypic flexibility of metabolism in small birds. Small birds wintering in cold climates generally show substantial improvements in cold hardiness in winter relative to summer and this improvement in cold hardiness is largely metabolic in nature. Another major focus of my laboratory is to examine the mechanistic basis of these seasonal improvements in cold hardiness. We take an integrative approach to addressing these mechanistic questions by looking at seasonal changes occurring over multiple levels of organization. Examples include thermogenic capacity and basal metabolic rate at the organismal level; mass changes in organs and tissues; and mobilization, transport and catabolic capacities for metabolic substrates in storage tissues, plasma and muscle cells, and transcriptomic and metabolomic profiles of pectoralis muscles to examine adjustments to major metabolic pathways. By studying winter acclimatization at these various hierarchical levels we hope to discern both fundamental and variable responses promoting cold adjustment in small birds.

          Current Projects:

• One of the typical seasonal changes associated with winter acclimatization in small birds is an increase in pectoralis muscle mass, which is associated with increased thermogenic capacity and cold tolerance. Winter increases in pectoralis mass generally range from about 10-30% in small birds, which rather closely parallels winter increases in M_sum, which generally range from about 10-40%. We have recently been investigating the factors which might regulate this muscle growth, focusing on myostatin, a potent autocrine/paracrine inhibitor of muscle growth in mammals and birds. We hypothesized that if myostatin plays a role in seasonal muscle mass regulation in birds, then myostatin gene expression and protein levels should be lower in winter and during migration (another period of muscle grwoth), which would free up the muscle to grow. Gene and protein expression data for myostatin and its metalloproteinase activators (TLL-1 and TLL-2) from a variety of bird species showing winter or migratory increases in muscle mass and M_sum, are generally consistent with our hypothesis, showing downregulation of the myostatin system in winter and migration relative to summer. We also used experimental approaches to this question and found that the myostatin system is also generally downregulated with flight- or cold-training in house sparrows, which is also consistent with the hypothesis that the myostatin system contributes to seasonal muscle mass regulation in birds (see Swanson and Vezina, 2015 J Ornithol 156(Suppl 1):S377-S388). We hope to continue this work comparing gene and protein expression of the myostatin system in birds inhabiting climates ranging from tropical to cold temperate to explore how climatic variability might be associated with seasonal phenotypic flexbility of the flight muscles and the myostatin system.

• A second general adjustment of small birds to changes in energy demands associated with cold exposure or migratory flights is an increased reliance on fats to fuel prolonged shivering or sustained flight. Because birds rely on fatty acids from adipose stores to fuel shivering and long-distance flight, adjustments in fat mobilization, transport and oxidation may be sites for seasonal adjustments. Fat oxidation capacities often are increased in winter and during migration in small birds and trans-membrane and intracellular transport capacities are also potentially limiting factors for fat metabolism. Our recent work has shown that fat transport and cellular catabolic capacities for a variety of energetically demaning activities in small birds result in upregulation of various steps in fat transport and catabolic pathways, with intracellular fatty acid binding protein in pectoralis muscle being a common target of upregulation.

• Modeling the Influence of Climate and Land Use Change on Grassland, Shrubland, and Riparian Bird Distribution and Abundance. My lab group is also interested in studying how climate and land use affect bird populations in the Northern Great Plains region and how climate and land use change might impact future bird distributions and abundance. We are currently using various ecological modeling approaches to investigate current climate and habitat associations in birds and to project future impacts of climate and land use change on bird populations in the Northern Great Plains region. Recent studies on grassland birds using a variety of potential future scenarios (see Baltensperger et al. 2020. Landscape Ecology 35:1757-1773) suggest that climate and land use trends might positively influence grassland bird abundance in the Northern Great Plains, although regions of high current abundance uniformly tend to be areas of future population declines (See the figure below for Grasshopper Sparrow for an example). We are also continuing work on developing models examining climate and land use impacts on grassland, shrubland and riparian birds in the region. Our objectives of these studies is to determine what climate and land use variables most impact current bird distributions and abundance so that we can better predict future bird responses to climate and land use/land cover trends.

• Physiology of freeze-tolerance and supercooling in overwintering anurans. Another aspect of my interest in cold tolerance physiology involves the overwintering strategies of terrestrial anurans. My laboratory has conducted studies of the physiological capacities underlying overwintering strategies in four species of terrestrially wintering anurans, the Plains Spadefoot (Spea bombifrons), Great Plains (Bufo cognatus) and Woodhouse's Toads (B. woodhousei) and the Chorus Frog (Pseudacris triseriata). The spadefoot and toads are freeze-intolerant burrowers, and the chorus frog is a freeze tolerant species that overwinters in shallow terrestrial hibernacula. Studies in my lab have shown that the chorus frog mobilizes glucose as a cryoprotectant upon freezing, but the burrowing anurans do not. This is associated with seasonal changes in enzymes involved in glycogen moblization and synthesis (regulating glucose mobilization) in chorus frogs and such changes are not present in the freeze-intolerant burrower. We have also documented that freezing survival and glucose mobilization is associated with body size and the size of the hepatic glycogen stores in chorus frogs.

          Current Projects:

• We are currently investigating, in collaboration with the lab of Dr. Jake Kerby (Department of Biology, USD) the interaction between emerging infectious amphibian diseases (ranavirus, chytrid), freezing tolerance, and overwintering success in chorus frogs. Because these emerging amphibian diseases are present in South Dakota, they could have serious population consequences for chorus frogs if they have negative effects on freezing tolerance and overwintering survival.

• We have also completed studies on Northern Cricket Frogs (Acris blanchardi), which reach the northwestern-most extent of their range in southeastern South Dakota. Blanchard's Cricket frogs have a unique overwintering strategy in that they use cracks or burrows in the mud of stream banks as hibernacula and largely avoid freezing in these thermally buffered hibernacula. Populations at the northern range extent in South Dakota show poor freezing tolerance similar to populations in more southern portions of their range. We monitored temperatures within these overwintering sites and found that some sites did not drop below the freezing point of the frog body fluids over the entire winter, some sites dropped below the freezing point for only a few hours on a few nights over the winter, and some sites dropped below the freezing point of the body fluids for long periods during the winter. Our data suggest that South Dakota cricket frogs may tolerate short (e.g., 6-hours) fairly well (80% survival), but not longer (24-hour, 0% survival)freezing bouts. Thus, the limited freezing tolerance in this species may be ecologically relevant in the species, allowing them to survive short bouts of temperatures below the freezing point of their body fluids, but it appears that behavioral selection of appropriate hibernaculum sites is critical for overwintering survival in Blanchard's cricket frogs and the cold winter temperatures may limit their range extent in South Dakota. We are currently conducting experiments to carefully document characteristics of hibernaculum sites used by Blanchard's cricket frogs in this area to determine what features are important to hibernacula site selection by this species.

• Use of woodland and wetland habitats by migrating and breeding birds in the northern prairie region. Another promienent research thrust in my laboratory is studying the use of woodland, wetland and grassland habitats for stopover biology and breeding in migrant birds. Much of our work to date has investigated the influence of woodland landscape patterns (i.e., large native riparian woodlands vs. small human-planted farmstead woodlots) on migration and breeding of passerine birds in South Dakota. Native riparian woodlands in the northern prairie region have been greatly reduced in extent over the past century by conversion to agriculture and flooding under reservoirs, but smaller woodland habitats surrounding farmsteads have appeared during this time. We are interested in determining if the farmstead woodlots can substitute for lost native woodland habitat for migrating and breeding woodland birds. Our data suggest that both woodland habitats serve as effective stopover habitat for migrating birds (see figure below on plasma metabolite levels of triglycerides, which increase with fattening, and beta-hydroxybutyrate, which increase when burning fat; from Liu and Swanson. 2014. Physiol Biochem Zool 87:183-195; spring on left, fall on right) and that both provide suitable breeding habitat for those birds nesting in both types of woodland. However, several breeding species occur only in native riparian habitats and do not occur, or occur at very low abundance, in woodlot habitats. Thus, farmstead woodlots appear to partially substitute for lost native woodland habitat, but preservation of native woodland habitats are necessary for maintaining overall bird diversity in the northern prairie region. We have also investigated shorebird migration stopover in natural wetland habitats compared to managed wetlands in the area (e.g., Big Stone National Wildlife Refuge). Similar to woodland results, natural and managed wetland habitats also appear to both serve as effective stopover locations, but, again, some differences in the biodiversity of shorebirds using the two categories of wetlands occur. Examples of specific aspects of our stopover biology studies include relative abundance and diversity of migrants at natural and artificial woodland and wetland habitats, stopover duration and mass gains of migrants, and orientation of nocturnal migratory flights through the region. Results of these studies should have significant importance for conservation of these birds, many of which are exhibiting regional or continental population declines, because the migration period is a very energetically demanding phase of the annual cycle.

          Current Projects:

• Stopover Biology of Grassland Birds: Most studies of stopover biology in birds have involved woodland and wetland habitats, but little is known of stopover ecology of grassland migrant birds, despite this group of birds showing the greatest population declines of any bird guild in North America. We are currently studying how grassland birds in the Northern Great Plains use restored native prairie and managed (e.g., Conservation Reserve Program) grassland habitats for migration stopover. These studies employ a combination of line transect surveys, mist-netting and plasma metabolite profiling to address questions relating to the stopover ecology of grassland birds in these habitats. Preliminary data suggest that grassland migrants are capable of adding fat in both grassland types during stopover, but some differences in the migrant community occur between the two grassland types.

• Bird Use of Early Successional Riparian Habitats for Breeding and Migration: Since the completion of the mainstem Missouri River dams in the 1950s-1960s, management for flood control has limited the creation of early successional riparian forest such that it is now the most imperiled habitat along the river, which is the most extensive riparian habitat in the Northern Great Plains. Additionally, ongoing management for federally listed species (Piping Plover: Charadrius melodus and Interior Least Tern: Sterna antillarum athalassos) includes removal of early successional vegetation. An understanding of the current status of early successional sandbar habitats, their trajectories of change, and the biological tradeoffs of current management strategies is necessary for a balanced ecosystem-based approach to riparian management along the Missouri River. We are currently studying the avian biodiversity of these early successional habitats during breeding and migration in combination with functional measures of habitat quality, which include monitoring nest success, radio-telemetry to document relative use of early and later successional riparian habitats by migrant, and plasma metabolite profiling to document fattening rates of migrants. Results from these studies can be used to help inform management decisions for conservation of a variety of woodland habitats, including early successional woodlands, to benefit the needs of both breeding and migrating birds.