Browsing by Subject "Zoology"

For primates, and other arboreal mammals, adopting suspensory locomotion represents one of the strategies an animal can use to prevent toppling off a thin support during arboreal movement and foraging. While numerous studies have reported the incidence of suspensory locomotion in a broad phylogenetic sample of mammals, little research has explored what mechanical transitions must occur in order for an animal to successfully adopt suspensory locomotion. Additionally, many primate species are capable of adopting a highly specialized form of suspensory locomotion referred to as arm-swinging, but few scenarios have been posited to explain how arm-swinging initially evolved. This study takes a comparative experimental approach to explore the mechanics of below branch quadrupedal locomotion in primates and other mammals to determine whether above and below branch quadrupedal locomotion represent neuromuscular mirrors of each other, and whether the patterns below branch quadrupedal locomotion are similar across taxa. Also, this study explores whether the nature of the flexible coupling between the forelimb and hindlimb observed in primates is a uniquely primate feature, and investigates the possibility that this mechanism could be responsible for the evolution of arm-swinging.

To address these research goals, kinetic, kinematic, and spatiotemporal gait variables were collected from five species of primate (Cebus capucinus, Daubentonia madagascariensis, Lemur catta, Propithecus coquereli, and Varecia variegata) walking quadrupedally above and below branches. Data from these primate species were compared to data collected from three species of non-primate mammals (Choloepus didactylus, Pteropus vampyrus, and Desmodus rotundus) and to three species of arm-swinging primate (Hylobates moloch, Ateles fusciceps, and Pygathrix nemaeus) to determine how varying forms of suspensory locomotion relate to each other and across taxa.

From the data collected in this study it is evident the specialized gait characteristics present during above branch quadrupedal locomotion in primates are not observed when walking below branches. Instead, gait mechanics closely replicate the characteristic walking patterns of non-primate mammals, with the exception that primates demonstrate an altered limb loading pattern during below branch quadrupedal locomotion, in which the forelimb becomes the primary propulsive and weight-bearing limb; a pattern similar to what is observed during arm-swinging. It is likely that below branch quadrupedal locomotion represents a “mechanical release” from the challenges of moving on top of thin arboreal supports. Additionally, it is possible, that arm-swinging could have evolved from an anatomically-generalized arboreal primate that began to forage and locomote below branches. During these suspensory bouts, weight would have been shifted away from the hindlimbs towards forelimbs, and as the frequency of these boats increased the reliance of the forelimb as the sole form of weight support would have also increased. This form of functional decoupling may have released the hindlimbs from their weight-bearing role during suspensory locomotion, and eventually arm-swinging would have replaced below branch quadrupedal locomotion as the primary mode of suspensory locomotion observed in some primate species. This study provides the first experimental evidence supporting the hypothetical link between below branch quadrupedal locomotion and arm-swinging in primates.

Zoonotic disease poses one of the greatest threats to both human and animal health in our world today. Recent pandemics such as Ebola, SARS-CoV2, and highly pathogenic Avian Influenza have shown the devastating consequences of infectious disease on both human and animal populations. Few studies have characterized the risk of interspecies pathogen transmission with one of our closest living relatives, Pan paniscus. This endangered species of great apes inhabits only rainforests of the Congo River Basin. Due to human encroachment, bushmeat trade, illegal pet trade, and deforestation, only 15,000-20,000 wild bonobos remain. The Lola Ya Bonobo Sanctuary (LYB) serves as the world’s only haven for orphaned and injured bonobos and presents a valuable opportunity to study the epidemiology of respiratory pathogens in a habituated population. This study aimed to characterize the risk factors for transmission of respiratory illness between bonobos and humans at LYB. Between 2014-2017 a cohort of 77 bonobos and 44 human staff were observed for signs of clinical illness and had their upper respiratory tract routinely sampled. We used a multiplex nucleic acid amplification assay to detect the presence of 18 viral and 3 bacterial respiratory pathogens. Of 282 total bonobo testing events, 93 (33%) returned positive results, primarily RSV-A (n = 41, 44.1%) and Rhinovirus/Enterovirus (n = 37, 39.8%). Although the point of entry into LYB could not be determined, RSV-A initially appeared in the infant and juvenile enclosures and spread serially through the older bonobo enclosures. Rhinovirus/Enterovirus appeared in diffuse clusters throughout the sanctuary. Although new bonobos are subject to a prolonged quarantine, current policy allows for relocation of bonobos between enclosures and frequent and sustained contact with human staff. Active surveillance for respiratory and other pathogens and additional infection control measures may benefit bonobo and human health.

An organism's ability to detect and interpret chemical signals from the surrounding environment is vital to its survival. In mammals, the vomeronasal organ provides an integral part of this requirement as it allows for the detection of inter-individual chemical signals. Located within the vomeronasal epithelium is a group of highly specialized receptors called vomeronasal type-1 receptors (V1Rs). These receptors bind pheromones and kairomones, which are chemical cues from conspecifics and heterospecifics, respectively. Recently, V1Rs have been recognized as highly variable across mammalian taxa. One extraordinary example is the mouse lemur, in which ~83% of the estimated 259 genes are expected to be intact. This relatively young and cryptically diverse prosimian group has a controversial history of species delimitation and it is possible that patterns in the rapidly evolving and highly diverse V1R gene family may provide insight into species boundaries. This study generated broad and deep coverage of the two most diverse V1R subfamilies across multiple Microcebus species. By utilizing Pacific Bioscience's single molecule real time sequencing technology, this study produced sequences at a fraction of the time and cost of the traditional method of Sanger-sequenced clones. The results advance our understanding of the high diversity-at least 5.6% and 9.9% sequence divergence intra- and inter-individually for V1RIX and V1Rstrep, respectively-and rapid evolution of V1Rs in mouse lemurs. Comparing these results with draft genome mined sequences demonstrates the limited utility of low coverage genomes for identifying variation in this gene family. The patterns uncovered here provide no clear evidence for the role of these two characterized subfamilies in maintaining or generating species boundaries, but may instead point to an alternative mechanism of species recognition that is more complex and intricate than previously envisioned.

Much of our knowledge of the mammalian immune system comes from laboratory studies of model organisms in highly controlled settings; however, in nature, organisms experience myriad biotic and abiotic pressures that can influence the immune response. Understanding how the immune system operates in natural systems therefore requires studies of animals living in socially and ecologically relevant environments. Here, I investigated the drivers of individual variation in immunocompetence in a wild population of meerkats (Suricata suricatta) living in the Kalahari Desert. The meerkat is characterised by aggressively mediated female social dominance, and although hormonal masculinization is present to varying degrees in all adult, female meerkats, the dominant female in each clan has greater concentrations of total androgens than does any other clan member. I therefore tested if the immunocompetence handicap hypothesis (ICHH), which posits that androgens in males mediate a trade off between reproductive success and immunocompetence, could apply to females and perhaps extend to their offspring. From 2012-2015, I followed and sampled approximately 300 meerkats living in 24 social clans. I related measures of immunocompetence (i.e., gastrointestinal parasite burdens and innate immune function) to environmental, demographic, social, and endocrine variables. I tested for transgenerational effects of maternally derived androgens on offspring immunocompetence by administering an antiandrogen to pregnant dominant dams. For adult meerkats, I found that there is a cost to dominance, in terms of reduced immunocompetence and that those with greater androgen concentrations (either inferred from fecal androgen metabolites or measured directly from blood as androstenedione, A4) had greater parasite burdens and weaker immune responses. Because, in female meerkats, A4 appears to exert the dual effects of promoting reproductive success and compromising immunity, I propose that the ICHH can apply to females. Moreover, the immunosuppressive consequences of female hormonal masculinization extend beyond the dams to their offspring, via prenatal exposure to raised androgens, and therefore may represent a transgenerational consequence of sexual selection operating in females. By studying immune function in natural systems, we can gain a broader perspective on immune function from an ecological and evolutionary context.

Seasonal polyphenism in insects is the phenomenon whereby multiple phenotypes can arise from a single genotype depending on environmental conditions during development. Many butterflies have multiple generations per year, and environmentally induced variation in wing color pattern phenotype allows them to develop adaptations to the specific season in which the adults live. Elements of butterfly color patterns are developmentally semi-autonomous allowing for detailed developmental and evolutionary changes in the overall color pattern. This developmental flexibility of the color pattern can result in extremely diverse seasonal phenotypes in a single species. In this study, we asked the following questions: a) How do wing phenotype elements such as shape and pattern vary between seasonal forms? b) Can this variation be explained phylogenetically? c) If so, what are the various pattern development strategies used to achieve crypsis in the dry season form? To answer these questions, we used high resolution images to analyze pattern element variation of 34 seasonally polyphenic butterfly species belonging to the tribe Junoniini (Lepidoptera: Nymphalidae). We show that forewing shape and eyespot size both vary seasonally, and that the methods by which phenotype elements change in the dry seasonal forms is different in different clades and may therefore have independent and diverse evolutionary origins.

Environmental factors are a crucial determinant of an animals fitness. The effects of environment on fitness are often mediated by behavioral mechanisms as well as mechanisms that are ‘under the skin,’ such as growth and physiology. In my dissertation work, I study how two environmental factors – dominance rank and early-life conditions – are associated with growth and physiology. My colleagues and I test these links in a population of wild baboons studied by the Amboseli Baboon Research Project. The Amboseli Baboons Research Project has been collecting behavioral and demographic data on the Amboseli baboons for over 50 years, fecal hormone data for over 20 years, and blood samples collected via brief anaesthetizations for nearly 10 years. We complemented these remarkable datasets with cross-sectional data of female baboon body size.

In Chapter 1, we address two gaps in our understand of female dominance rank: (1) do higher-ranking females experience fewer stressors than lower-ranking females, and (2) how should we best quantify female dominance rank? Using fecal glucocorticoid concentrations as a proxy for the intensity and/or frequency of stressors that a baboon experiences, we find that, indeed, higher-ranking females do experience fewer stressors than lower-ranking females. Surprisingly, we also find that the best way to understand this effect is by categorizing females into two groups: alpha females, who are the highest-ranking female in the group, and everyone else.

In Chapter 2, we then focus on differences in the competitive landscapes assumed by two common measures of dominance rank, ordinal and proportional ranks. We complement theoretical work with re-analysis of 20 prior Amboseli baboon studies to show that for males, ordinal rank (i.e., number of individual ranking above the focal animal) was always a better predictor of traits than proportional rank, whereas for females, some traits were better predicted by ordinal rank, and some were better predicted by proportional rank (i.e., proportion of the group that a focal animal dominates). Our results suggest that males compete for density-dependent resources, whereas females compete for a mix of density-dependent and density-independent resources. In addition, our study demonstrates a new way to learn about the nature of within-group competition.

In Chapter 3, we present two new methods to use with body size data collected via parallel-laser photogrammetry. One of these methods was developed by colleagues here at Duke University, and the other method was developed by colleagues at George Washington University. These methods automate part of the hand-measurement process – measuring the distance between the lasers – and effectively saves time while increasing accuracy and precision of the final body size measurement. Our two methods have different strengths and weaknesses, and we anticipate that researchers will gravitate toward one or the other depending on their dataset, with the ultimate goal of increasing the use, ease, and accuracy of parallel-laser photogrammetry in studies of behavioral ecology.

In Chapters 4, we use the method developed in Chapter 3 to test whether early-life adversity stunts body size in female baboons. While this effect has been found in humans and some nonhuman animals, data on inter-individual differences in body size are extremely rare in wild primates. Using a dataset of over 2,000 images of 127 female baboons, we present the first cross-sectional growth curve of wild female baboons from juvenescence throughout adulthood. We then test whether females exposed to three main sources of early-life adversity - drought, maternal loss, or a cumulative measure of adversity – are smaller for their age in juvenescence or adulthood. We find that early-life drought predicts smaller limb length but not smaller torso length; our other measures of early-life adversity do not predict differences in body size. Our results suggest that baboons grow plastically in response to energetic early-life stress, but that this plasticity seems limited to limb growth, not torso growth.

Finally, in Chapter 5, we test a component of the biological embedding hypothesis, which predicts that early-life adversity is associated with elevated baseline inflammation as well as heightened acute inflammation in adulthood. To our knowledge, these predictions have only been tested in humans. Using serum samples collected from 89 baboons via brief anaesthetization, we measured several biomarkers of baseline and acute inflammation: c-reactive protein, soluble urokinase plasminogen activator receptor, interleukin 6, interleukin 1-beta, and tumor necrosis factor alpha. We test two measures of early-life adversity: maternal loss and a cumulative measure that incorporates 5 different potential sources of adversity. In contrast to the predictions of the biological embedding hypothesis, we find that baboons who experienced early-life adversity have a mix of comparable or lower levels of baseline and acute inflammation compared to baboons who experience no adversity. Prior tests of the biological embedding hypothesis were performed in humans who generally had access to more calories, less active lifestyles, and lower pathogen burden than wild baboons. Our results highlight the varied effects that early-life adversity can have on an organism’s development depending on the broader environment in which that organism lives.

The composition and function of mammalian gut microbiomes are shaped by complex endogenous and exogenous factors that present on evolutionary and proximate timescales. In the Anthropocene era, host-associated microbiota are inevitably, yet differentially, influenced by natural and anthropogenic factors that vary across individuals and populations. In this dissertation, I used descriptive and experimental approaches, largely within a single species, the ring-tailed lemur (Lemur catta), to probe the roles of host physiology, environmental conditions, anthropogenic perturbation, and microbial environment in shaping primate microbiota across scales. First, I conducted a broad investigation of ring-tailed lemur gut microbiota and soil microbiota across 13 lemur populations (n = 209 individuals) spanning this species’ natural range in Madagascar, as well as multiple captivity settings in Madagascar and the U.S. By analyzing the lemur and soil microbiota, I showed that lemur gut microbiota vary widely within and between wild and captive populations, and that lemur and soil microbiota covary, suggesting a role for environmental acquisition in shaping interpopulation variation. Second, I analyzed vaginal, labial, and axillary microbiota of female ring-tailed lemurs and Coquerel’s sifakas (Propithecus coquereli) at the Duke Lemur Center (DLC) to demonstrate the influences of stable traits (e.g., species identity and mating system) and transient traits (e.g., ovarian hormones and forest access). We found that the effects of transient traits build on underlying differences mediated by stable traits. Third, and further focusing on DLC lemurs, but with a concentration on anthropogenic influence, I worked with a team of researchers to perform an experimental manipulation in ring-tailed lemurs to determine the influence of antibiotic treatment, with or without subsequent fecal transfaunation, on lemur gut microbiomes. I applied ecological frameworks to show that different facets of lemur microbial communities, such as bacterial diversity and composition, followed different recovery trajectories following antibiotic treatment. Fourth, I expanded my focus back to multiple ring-tailed lemur populations in natural and captivity settings to investigate the links between anthropogenic disturbance and antibiotic resistance genes (ARGs). I analyzed ARGs in wild and captive lemurs and soil from their habitats to show that lemur ARGs were correlated with anthropogenic disturbance and covaried with soil ARGs; lemur resistomes reflects multiple routes of ARG enrichment, including via antibiotic treatment or environmental acquisition. Integrating across these four data chapters, my results reveal that (a) the foundations of lemur-associated microbiomes are structured according to broad environmental conditions (e.g., wild vs. captive populations), but that between and within these broad categories, lemur microbiota are sensitive to more nuanced environmental variation, (b) lemur microbiota and resistomes co-vary with environmental microbiota, demonstrating the potential role of environmental acquisition in shaping host-associated communities across varying environments, and (c) integrating host microbial data across scales (e.g., at the individual and population level) with data on multiple facets of microbial communities (e.g., diversity, composition, membership, and resistomes), was key to providing a holistic perspective on host-associated and environmental microbe interactions across different microbial landscapes.

Primates span incredible behavioral and ecological diversity, and this diversity is reflected in the shape of the skull. This dissertation asks two questions surrounding the evolution of primate skull shape: 1) what are the macroevolutionary correlates of primate skull shape? And 2) what is the pattern of phenotypic integration in the primate skull at a macroevolutionary scale? To address these questions, I compiled a broad comparative dataset of anatomical landmarks identified from 3D scans of primate skulls and analyzed this data using statistical methods that combine geometric morphometrics and phylogenetic comparative methods. To investigate the macroevolutionary correlates of skull shape, I used multivariate phylogenetic generalized linear models to test for relationships between skull shape and several variables that are predicted to be correlated with skull shape: allometry, typical diet, tree gouging behavior, activity pattern, and sexual dimorphism. I found strong phylogenetic signal for primate skull shape, confirming the need for phylogenetic comparative methods. Allometry was a significant predictor of skull shape, with larger primates having relatively small, convergent orbits, and anteroposteriorly short skulls compared to small primates. Sexual dimorphism was associated with a dramatically lengthened rostrum, probably to facilitate a large gape in aggressive displays. Folivory was associated with deeper mandibles, which may improve mechanical advantage and strain resistance. To investigate patterns of phenotypic integration in the skull, I performed hierarchical clustering analyses on phylogenetically corrected inter-landmark covariance matrices. In contrast to previous research, I did not find evidence for distinct phenotypic modules in the primate skull, and I argue that this discrepancy is due to methodological shortcomings of past research that biased results towards identifying different anatomical regions as discrete modules. This dissertation represents one of the first investigations of primate skull shape at a macroevolutionary scale, and demonstrates that the combination of geometric morphometrics and phylogenetic comparative methods can yield novel insights into evolutionary morphology.

Studies of the social behavior of Cuvier’s beaked whales (Ziphius cavirostris) are challenging because of their pelagic habitat and the limited time they spend at the surface. The sociality of these deepest diving mammals is of great interest, however, including how social behavior might influence responses to anthropogenic disturbance as this species has a history of stranding in association with certain types of human-created noise. Beyond conservation concerns, the beaked whales (Family Ziphiidae) are a valuable group for the comparative study of the ecological influences on mammalian social evolution since they are an “out group within an out group”, including some of the most extreme diving mammals within the Cetacea which are themselves one of the few mammalian groups to become secondarily fully aquatic. The beaked whales are also the second most speciose family in the cetaceans and so can lend statistical power to formal comparative analyses. One unifying characteristic of most beaked whale species is sexually dimorphic dentition, where only adult males have erupted tusks which they appear to use as weapons in contests with each other as evidenced by the high level of scarring in adult males. Despite this, previous studies suggest a substantial amount of variation in beaked whale social structure and mating systems.

In this work, I investigated the social behavior of a relatively accessible, high density population of Cuvier’s beaked whales off the coast of Cape Hatteras, North Carolina, USA. I used data from photo identification surveys from a longitudinal study, as well as satellite-linked depth-recording telemetry tags to investigate within and between group behavior. In addition, I present a case study and assessment of how I optimized the programming of telemetry instruments to increase their value in behavioral studies.

I tested the stability of adult male-male interactions over the medium term using diving synchrony as a proxy for group membership and found that adult male-male pairs stayed remarkably synchronous for days to weeks, contrary to expectations that individuals would quickly competitively exclude each other. Using photo-identification records of whole groups, I did not find strong evidence for sexual segregation and instead found a high level of fission-fusion behavior between groups. In addition, I did not find strong evidence for long term stable group formations, although given the large population size and a relatively small sample size infrequent but important bonds among individuals may have been missed. Using a new programming regime to collect up to 14 days of time-series depth data on an individual, I was able to confirm that diel differences in dive depth were almost entirely explained by bouts of shallow diving which occur only a night. These shallow dives appear to be a separate mode of diving behavior not previously well described in the literature, and although this behavior may have multiple functions, it may be a useful behavioral modality to investigate further in relation to social behavior.

Finally, I argue that the application of similar methods used here combining photo-identification and telemetry tagging could lead to rapid discovery of social parameters in other hard to study pelagic Cetaceans including other Ziphiidae with a view toward building a comparative dataset.

Kinship plays a fundamental role in the evolution of social systems and is considered a key driver of group living. The quantity and quality of an individual’s social relationships can have significant fitness effects, and individuals often preferentially associate with close relatives, behavior which amplifies such benefits via inclusive fitness. Nevertheless, reproductive variation, dispersal, and mortality can alter kin availability. Here I investigate the repercussions of kin availability on social network structure in a fission-fusion population of Indo-Pacific bottlenose dolphins in Shark Bay, Western Australia. In my first chapter, I used data from next-generation sequencing to assign parentage and estimate genetic relatedness within the study population. I compared relatedness estimates to a multi-generational maternal pedigree and showed that these methods could classify up to third-degree kin with over 85% accuracy. Additionally, I conducted a series of social network analyses to measure how accuracy and precision of relatedness estimation influenced statistical power in these downstream analyses. In my second chapter, I assess different social association indices for their ability to predict interaction rates. Group membership is commonly used as a proxy for interaction, and this assumption can rarely be tested for cetaceans due to the difficulty of observing interactions which are often infrequent at the sea surface. To validate this assumption, I used two different data streams, group scan-sampling, used to generate group membership and association rates, and individual focal follows, used to calculate interaction rates. I input several association indices into a spatially explicit null model, and compared interaction rates between affiliates, i.e., pairs whose association rate significantly exceeds expectations, and non-affiliates. I show that an index incorporating group size performs the best across most examined scenarios, but the most commonly used indices, half-weight and simple ratio, perform similarly. In my third chapter, I investigate how the availability of kin shapes individual position within a social network. I measured females’ propensities to form relationships with both related and unrelated individuals, and showed that females have strong preferences for both close matrilineal kin and close non-matrilineal kin. Individuals also frequently affiliate with more distant kin, and only the availability of distant kin affects the total number of affiliative bonds that an individual forms. Individuals with fewer close matrilineal kin formed more bonds with unrelated individuals. These models suggest that while dolphins have strong kin preferences that shape some aspects of gregariousness, they are also socially plastic, and can compensate for the lack of preferred kin partners by forming affiliations with unrelated individuals. Together, my results provide guidelines for studying the effects of relatedness on social networks in wild populations. I demonstrate significant effects of kin availability on both direct and indirect connectivity within a social network, which have implications for understanding the structure and function of networks in animal societies.

Latch-mediated spring actuation (LaMSA) mechanisms allow a broad diversity of organisms to achieve ultrafast motion. Most research into biological LaMSA mechanisms focuses on a narrow size or age range of the organism when the LaMSA mechanism is fully developed. However, the emergence of LaMSA morphology and behavior during early life history offers novel insights into the scaling and ecology of ultrafast movement. In this thesis, I establish the emergence and kinematics of LaMSA morphology in two systems, the mantis shrimp Gonodactylaceus falcatus (Stomatopoda) and the snapping shrimp Alpheus heterochaelis (Alpheidae). I also examine the plasticity of LaMSA development in the snapping shrimp Alpheus heterochaelis. The mantis shrimp’s spring-actuated strike is one of the best-studied LaMSA mechanisms; however, we do not know when the LaMSA morphology or behavior emerges during development. In Chapter 2, I found that the mantis shrimp G. falcatus develop their LaMSA morphology in their fourth larval stage when they transition into the pelagic zone and begin feeding on plankton. Mathematical and physical models of LaMSA kinematics suggest that smaller mechanisms generate greater accelerations. Therefore, I hypothesized that larval mantis shrimp would accelerate their strikes faster than adult mantis shrimp. Larval kinematics showed that larvae achieve accelerations on par or lower than adult mantis shrimp species. However, the larval strikes are much faster than the swimming speeds of other small pelagic organisms. Snapping shrimp generate cavitation bubbles using a LaMSA mechanism in their major claw. However, we do not know when the snapping shrimp LaMSA morphology or behavior emerges during development, nor whether they can generate cavitation bubbles at that size. In Chapter 3, I establish that the snapping shrimp Alpheus heterochaelis develop LaMSA morphology and behavior between one- and two months after hatching, when their carapace is roughly four to five millimeters long. I again hypothesized that the juvenile snapping shrimp would generate accelerations much faster than adults. My data show that juvenile snapping shrimp can generate accelerations two orders of magnitude faster than adults when the juvenile is more than two orders of magnitude smaller in claw mass. Juvenile snapping shrimp struck so quickly that they generated and directed cavitation bubbles at the millimeter scale. Developmental stressors can affect how morphological traits grow across ontogeny. In some cases, resource allocation to specific body parts during development can mitigate the negative effects of stress. To our knowledge, the developmental plasticity of LaMSA morphology and kinematics has not been explored. In Chapter 4, I test whether the development of the snapping shrimp LaMSA morphology and kinematics is affected by changes in feeding frequency. Juvenile snapping shrimp fed less frequently during development grew more slowly than better-fed individuals. However, the snapping shrimp raised in the least frequently fed group developed slightly larger snapping claws relative to their body size than individuals in other food treatments. Feeding treatments did not appear to affect the scaling of LaMSA kinematics. This thesis shows that the emergence of LaMSA morphology and behavior inform ecological transitions across ontogeny. The findings from this work can provide novel insights into how size may constrain ultrafast motion. The methods and systems I developed offer new systems and approaches for learning about the scaling and plasticity of spring-actuated movement.

Rapid urbanization threatens the survival of native wildlife species worldwide. In order to fully grasp the implications of the ongoing growth of urban areas on biodiversity, conservationists need to be able to quantify the response patterns of a wide range of different species to the expansion of urban and suburban land use. In this study, we set up two road-based transects across gradients of urbanization and habitat loss in the diverse longleaf pine forests of the Sandhills region of North Carolina, USA. With funding provided by the NC Wildlife Resources Commission, we drove the transects repeatedly at night in the field seasons of 2006-2008, tallying all vertebrate animals encountered (live or dead). The first transect (driven in all three years; 75 km long) ran from the urban areas of Southern Pines and Pinehurst down to the remote and relatively pristine habitats associated with the state-owned Sandhills Gamelands. The second transect (driven in 2007 and partially in 2008; 69 km long) began at the terminus of the first transect in the Gamelands, and then stretched down to the urban zones of Hamlet and Rockingham.

A total of 4900 vertebrate animals representing 69 species were observed on or near the road routes after driving a total of 16,625 km. This total includes 592 nightjars (ground-nesting nocturnal birds; e.g. whip-poor-wills) that we heard while driving the transects. In addition, in 2007 we surveyed for the nightjars and for quail (a high-priority game species that also nests on the ground) using 75 point count locations evenly distributed along the northern road route.

Regression tree analysis (a robust, nonparametric technique with minimal assumptions) was used to model the animal observation rates for a given 1 km road segment or point count as a function of various habitat variables measured within corresponding buffer zones for each segment. We also modeled snake and bird encounter rates as a function of mesopredator mammal observations.

Our results reveal that amphibian, snake, and ground-nesting bird observation rates are negatively associated with increasing levels of traffic and impervious surface. Conversely, mesopredator mammals (and domestic cats in particular) responded slightly positively to increasing urbanization, and negatively to protected area coverage. Both ground-nesting birds and snakes showed signs of negative correlations with mesopredator encounter rates, although these trends were not always significant due to high variability in the mesopredator data.

In order to try and confirm the results of the regression tree analyses, we also used a multivariate ordination approach (non-metric multidimensional scaling) to visualize the integrated community structure of all of the major vertebrate groups we observed in the Sandhills. The ordinations revealed that while the snake, ground-nesting bird, and amphibian groups were similar to each other in terms of their avoidance of urban conditions, the cats and native mesopredator species actually seemed to define widely divergent axes of community variation. Cats in particular were separated from the other groups on 2 out of 3 axes of the species-space ordination. Still, as we noted above for the regression tree models, it is difficult to sort out with our correlative data set whether cats and other mesopredators truly played an independent role in structuring and/or depleting the other wildlife guilds along our route. More experimental approaches are recommended for trying to resolve whether overabundant predators or road mortality and inappropriate habitat are more to blame for the much reduced encounter rates we observed for the snakes, birds, and amphibians in urban areas. Future studies will also be needed to confirm the logical assumption that road encounter rates provide a reasonably accurate index of the relative abundance of the different animal groups along the survey routes.

The processes of locating and capturing food are critical components of a predator’s fitness, but can be difficult to observe, particularly in marine environments where foraging behavior is not often visible from the surface. Individuals and populations display a range of foraging adaptations, from stenophagous individuals who consume a single prey type to generalist populations that thrive with a variety of environments and prey taxa. Populations and individuals that show high levels of behavioral plasticity may be able to alter their foraging behavior when environmental conditions change, demonstrating new foraging strategies depending on the characteristics of the habitat and local prey fields. In this dissertation, I used high-resolution data from bio-logging tags deployed on three well-studied species of cetaceans (whales and dolphins) in novel environments, to analyze the role of environment in cetacean foraging strategies and kinematic behaviors. Bio-logging tags provide high-resolution information about predator foraging ecology, including foraging rates, kinematics of prey capture attempts, and even interactions between predators and prey. I first analyzed tag records from short-finned pilot whales (Globicephala macrorhynchus) foraging near the shelf-break off Cape Hatteras, North Carolina. In this analysis, I sought to determine if pilot whales forage near the seafloor when it is within reach, and whether such behavior affects their foraging rates and diel patterns. I tapped into the whale’s own sensory system, using the echoes of the animal’s echolocation clicks bouncing off the seafloor to demonstrate that many whales frequently foraged near the seafloor itself. I then used high-resolution kinematic data to investigate how benthic foraging affects the fine-scale details of prey capture attempts. Tagged whales were often upside-down while foraging benthically and appeared to pursue benthic prey as they attempted to escape by swimming away from the seafloor and into the water column. I used similar methods to study the foraging behavior of the offshore ecotype of common bottlenose dolphins (Tursiops truncatus) in pelagic waters near Bermuda. These offshore dolphins dive to considerable depths; I analyzed the effect of depth on the energetics and capture success rates of foraging attempts. I was able to eavesdrop on the echolocation clicks produced by dolphins during prey capture attempts to estimate the distance from the dolphin to its prey, and determine whether prey captures were successful. Dolphins foraging in deep dives encountered more prey and foraged with higher success rates than while foraging near the surface. Finally, I studied the fine-scale kinematics of humpback whales (Megaptera novaeangliae) foraging in winter feeding grounds near Virginia Beach, Virginia to determine how this extremely shallow water environment affected their foraging behavior. Humpback whales lunge-feeding in this area have limited maneuverability, likely due to the shallow nature of the environment, and exhibited simplified kinematics compared to studies in other areas. Nevertheless, these whales were still able to forage at high rates, with some evidence of higher foraging attempts made at dawn. The foraging ecology of these three species has been extensively studied elsewhere, but new environments present opportunities to discover novel foraging strategies. Overall, my dissertation illustrates the ways in which environmental features shape foraging behavior in these three species of behaviorally plastic cetaceans.

Sea urchins and brittle stars lack eyes, yet nonetheless are capable of vision, or the detection and resolution of spatial images and detail. Their vision, according to what is known today, is mediated through a light-sensing system that extends across the body and is processed via a decentralized nervous system. This is different from two-eyed and even most multi-eyed animals, where light is collected via discrete organs (eyes or eye cups) and processed in a brain or central ganglion. As benthic marine invertebrates, vision may be useful to sea urchins and brittle stars for navigating, finding shelter, or identifying predators. Although photoreceptor cells have been identified in brittle stars, much remains unknown about vision and light responses in both groups and the echinoderms as a whole (sea urchins, brittle stars, sea stars, sea cucumbers, and feather stars). My dissertation examines some of the gaps in this field of inquiry. I investigate (1) the potential ecological correlates of a sea urchin trait thought to mediate spatial vision, (2) how various regions of the urchin body differ in their sensitivity to light, and (3) if brittle stars are capable learning to associate a darkness cue with the presentation of food.

First, I performed a comparative study on the density of spines on sea urchins. As stated previously, sea urchins do not have eyes yet they are capable of resolving coarse images. One suggestion as to the mechanism of this capability is that the spines shade off-axis light from reaching the photosensitive test (skeleton). Following this hypothesis, the density of spines across the body determines the resolution (or sharpness) of vision by restricting the incidence of light on the photosensitive skin of the animal, creating receptive areas of different minimum resolvable angles. Previous studies have shown that predicted resolutions in several species closely match behaviorally-determined resolutions, ranging from 10° to 33°. Here we present a comparative morphological survey of spine density with species representatives from 22 of the 24 families of regular sea urchins (Class Echinoidea) in order to better understand the relative influences of phylogenetic history and three visually-relevant environmental variables on this trait. We estimated predicted resolutions by calculating spine densities from photographs of spineless sea urchin tests (skeletons). Analyses showed a strong phylogenetic signal in spine density differences between species. Phylogenetically-corrected Generalized Least Squares (PGLS) models incorporating all habitat parameters were the most supported, and no particular parameter was significantly correlated with spine density. Spine density is subject to multiple, overlapping selective pressures and therefore it is possible that either: 1) spine density does not mediate spatial vision in echinoids, or 2) visual resolution via spine density is a downstream consequence of sea urchin morphology rather than a driving force of adaptation in these animals.

Second, I examined the sensitivity to light on different parts of the body of the urchin species Lytechinus variegatus. The sensitivity of an eye is important to understand because it not only determines the light levels under which an eye can function but also indirectly affects how sharp the vision can be. It is unknown how sensitivity maps across the body in urchins, which may have implications for how various parts of the body are used in visual tasks. I tested the behavioral sensitivity response of L. variegatus to light on different regions of the body, using positive or negative phototaxis as response criteria. I tested the ambulacral region first, because this has been shown to be more sensitive to light than the interambulacral region in other urchin species. Individuals of L. variegatus were negatively phototactic to the brightest light (10,000 lux) and exhibited positive phototaxis to any dimmer light, responding to as little as 10 lux (or about the amount of ambient light in late civil twilight). Next, I tested the relative sensitivity response of the ambulacrum and interambulacrum, the two regions of the body, and confirmed that the ambulacrum is the more sensitive of the two in L. variegatus. Finally, I tested the relative sensitivity response of different angular heights (elevations) on the urchin body, along the oral-aboral axis, as these may be ecologically meaningful to the animal. There was a behavioral shift as elevation increased. Bright (10,000 lux) light at 0° (the equator of the animal) caused positive phototaxis; at 30° above the equator, roughly an equal number of urchins moved towards and away from the light; and at 60° above the equator the light caused a negative phototaxis response. The negative phototaxis observed with the light at a 60° elevation on the animal may have ecological consequences or indicate that this region is less sensitive to light. The data from this study can inform which regions and structures future studies may want to target for sensitivity and vision studies in L. variegatus.

Third, I tested whether individuals of the brittle star species Ophiocoma echinata were able to associate a period of darkness with the presentation of a food reward. Like other members of Phylum Echinodermata, the ophiuroid nervous system is decentralized, consisting of five radially arranged ganglia joined by a central nerve ring. While operant and classical conditioning have been observed in asteroids in a limited number of studies, members of the other echinoderm classes remain relatively untested. A group of individually housed Ophiocoma in an experimental group were trained by only presenting food during a period of darkness, while control group animals were fed under regular daytime room lights many hours after a period of darkness of the same duration. After the training period, the experimental group demonstrated they had learned to associate the two cues by regularly emerging during the dark period even when no food was presented. The untrained control animals, as well as pre-training experimental animals, did not emerge during the dark periods, as no food was presented. There was, however, significant variation within the experimental group in terms of the number of times individuals displayed the learned behavior and how quickly animals learned the association. This study shows that classical conditioning is possible in a class of animals without centralized nervous systems.

These results contribute to greater understandings of resolution, sensitivity, and light-guided tasks in the echinoderms which have implications for the visual ecology of these species as well as the study of sensing and processing in decentralized systems.