Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.

Eco-evolutionary trophic dynamics: loss of top predators drives trophic evolution and ecology of prey.

Ecosystems are being altered on a global scale by the extirpation of top predators. The ecological effects of predator removal have been investigated widely; however, predator removal can also change natural selection acting on prey, resulting in contemporary evolution. Here we tested the role of predator removal on the contemporary evolution of trophic traits in prey. We utilized a historical introduction experiment where Trinidadian guppies (Poecilia reticulata) were relocated from a site with predatory fishes to a site lacking predators. To assess the trophic consequences of predator release, we linked individual morphology (cranial, jaw, and body) to foraging performance. Our results show that predator release caused an increase in guppy density and a "sharpening" of guppy trophic traits, which enhanced food consumption rates. Predator release appears to have shifted natural selection away from predator escape ability and towards resource acquisition ability. Related diet and mesocosm studies suggest that this shift enhances the impact of guppies on lower trophic levels in a fashion nuanced by the omnivorous feeding ecology of the species. We conclude that extirpation of top predators may commonly select for enhanced feeding performance in prey, with important cascading consequences for communities and ecosystems.

Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play.

Interactions between natural selection and environmental change are well recognized and sit at the core of ecology and evolutionary biology. Reciprocal interactions between ecology and evolution, eco-evolutionary feedbacks, are less well studied, even though they may be critical for understanding the evolution of biological diversity, the structure of communities and the function of ecosystems. Eco-evolutionary feedbacks require that populations alter their environment (niche construction) and that those changes in the environment feed back to influence the subsequent evolution of the population. There is strong evidence that organisms influence their environment through predation, nutrient excretion and habitat modification, and that populations evolve in response to changes in their environment at time-scales congruent with ecological change (contemporary evolution). Here, we outline how the niche construction and contemporary evolution interact to alter the direction of evolution and the structure and function of communities and ecosystems. We then present five empirical systems that highlight important characteristics of eco-evolutionary feedbacks: rotifer-algae chemostats; alewife-zooplankton interactions in lakes; guppy life-history evolution and nutrient cycling in streams; avian seed predators and plants; and tree leaf chemistry and soil processes. The alewife-zooplankton system provides the most complete evidence for eco-evolutionary feedbacks, but other systems highlight the potential for eco-evolutionary feedbacks in a wide variety of natural systems.

Macrosystems ecology: Understanding ecological patterns and processes at continental scales

Macrosystems ecology is the study of diverse ecological phenomena at the scale of regions to continents and their interactions with phenomena at other scales. This emerging subdiscipline addresses ecological questions and environmental problems at these broad scales. Here, we describe this new field, show how it relates to modern ecological study, and highlight opportunities that stem from taking a macrosystems perspective. We present a hierarchical framework for investigating macrosystems at any level of ecological organization and in relation to broader and finer scales. Building on well-established theory and concepts from other subdisciplines of ecology, we identify feedbacks, linkages among distant regions, and interactions that cross scales of space and time as the most likely sources of unexpected and novel behaviors in macrosystems. We present three examples that highlight the importance of this multiscaled systems perspective for understanding the ecology of regions to continents. © The Ecological Society of America.

Soundscape Ecology of Hawaiian Spinner Dolphin Resting Bays

Sound is a key sensory modality for Hawaiian spinner dolphins. Like many other marine animals, these dolphins rely on sound and their acoustic environment for many aspects of their daily lives, making it is essential to understand soundscape in areas that are critical to their survival. Hawaiian spinner dolphins rest during the day in shallow coastal areas and forage offshore at night. In my dissertation I focus on the soundscape of the bays where Hawaiian spinner dolphins rest taking a soundscape ecology approach. I primarily relied on passive acoustic monitoring using four DSG-Ocean acoustic loggers in four Hawaiian spinner dolphin resting bays on the Kona Coast of Hawai‛i Island. 30-second recordings were made every four minutes in each of the bays for 20 to 27 months between January 8, 2011 and March 30, 2013. I also utilized concomitant vessel-based visual surveys in the four bays to provide context for these recordings. In my first chapter I used the contributions of the dolphins to the soundscape to monitor presence in the bays and found the degree of presence varied greatly from less than 40% to nearly 90% of days monitored with dolphins present. Having established these bays as important to the animals, in my second chapter I explored the many components of their resting bay soundscape and evaluated the influence of natural and human events on the soundscape. I characterized the overall soundscape in each of the four bays, used the tsunami event of March 2011 to approximate a natural soundscape and identified all loud daytime outliers. Overall, sound levels were consistently louder at night and quieter during the daytime due to the sounds from snapping shrimp. In fact, peak Hawaiian spinner dolphin resting time co-occurs with the quietest part of the day. However, I also found that humans drastically alter this daytime soundscape with sound from offshore aquaculture, vessel sound and military mid-frequency active sonar. During one recorded mid-frequency active sonar event in August 2011, sound pressure levels in the 3.15 kHz 1/3rd-octave band were as high as 45.8 dB above median ambient noise levels. Human activity both inside (vessels) and outside (sonar and aquaculture) the bays significantly altered the resting bay soundscape. Inside the bays there are high levels of human activity including vessel-based tourism directly targeting the dolphins. The interactions between humans and dolphins in their resting bays are of concern; therefore, my third chapter aimed to assess the acoustic response of the dolphins to human activity. Using days where acoustic recordings overlapped with visual surveys I found the greatest response in a bay with dolphin-centric activities, not in the bay with the most vessel activity, indicating that it is not the magnitude that elicits a response but the focus of the activity. In my fourth chapter I summarize the key results from my first three chapters to illustrate the power of multiple site design to prioritize action to protect Hawaiian spinner dolphins in their resting bays, a chapter I hope will be useful for managers should they take further action to protect the dolphins.

The Abundance and Behavioral Ecology of Cape Cod Gray Seals Under Predation Risk From White Sharks

The ultimate goal of wildlife recovery is abundance growth of a species, though it must also involve the reestablishment of the species’ ecological role within ecosystems frequently modified by humans. Reestablishment and subsequent recovery may depend on the species’ degree of adaptive behavior as well as the duration of their functional absence and the extent of ecosystem alteration. In cases of long extirpations or extensive alteration, successful reestablishment may entail adjusting foraging behavior, targeting new prey species, and encountering unfamiliar predatory or competitive regimes. Recovering species must also increasingly tolerate heightened anthropogenic presence, particularly within densely inhabited coastal zones. In recent decades, gray seals (Halichoerus grypus) recovered from exploitation, depletion, and partial extirpation in the Northwest Atlantic. On Cape Cod, MA, USA, gray seals have reestablished growing breeding colonies and seasonally interact with migratory white sharks (Carcarodon carcharias). Though well-studied in portions of their range due to concerns over piscivorous impacts on valuable groundfish, there are broad knowledge gaps regarding their ecological role to US marine ecosystems. Furthermore, there are few studies that explicitly analyze gray seal behavior under direct risk of documented shark predation.

In this dissertation, I apply a behavioral and movement ecology approach to telemetry data to understand gray seal abundance and activity patterns along the coast of Cape Cod. This coastal focus complements extensive research documenting and describing offshore movement and foraging behavior and allows me to address questions about movement decisions and risk allocation. Using beach counts of seals visible in satellite imagery, I estimate the total regional abundance of gray seals using correction factors from haul out behavior and demonstrate a sizeable prey base of gray seals locally. Analyzing intra-annual space use patterns, I document small, concentrated home ranges utilizing nearshore habitats that rapidly expand with shifting activity budgets to target disperse offshore habitats following seasonal declines in white sharks. During the season of dense shark presence, seals conducted abbreviated nocturnal foraging trips structured temporally around divergent use of crepuscular periods. The timing of coastal behavior with different levels of twilight indicate risk allocation patterns with diel cycles of empirical white shark activity. The emergence of risk allocation to explain unique behavioral and spatial patterns observed in these gray seals points to the importance of the restored predator-prey dynamic in gray seal behavior along Cape Cod.

Behavioral Ecology of the Western Atlantic Short-finned Pilot Whale (Globicephala macrorhynchus)

Social structure is a key determinant of population biology and is central to the way animals exploit their environment. The risk of predation is often invoked as an important factor influencing the evolution of social structure in cetaceans and other mammals, but little direct information is available about how cetaceans actually respond to predators or other perceived threats. The playback of sounds to an animal is a powerful tool for assessing behavioral responses to predators, but quantifying behavioral responses to playback experiments requires baseline knowledge of normal behavioral patterns and variation. The central goal of my dissertation is to describe baseline foraging behavior for the western Atlantic short-finnned pilot whales (Globicephala macrohynchus) and examine the role of social organization in their response to predators. To accomplish this I used multi-sensor digital acoustic tags (DTAGs), satellite-linked time-depth recorders (SLTDR), and playback experiments to study foraging behavior and behavioral response to predators in pilot whales. Fine scale foraging strategies and population level patterns were identified by estimating the body size and examining the location and movement around feeding events using data collected with DTAGs deployed on 40 pilot whales in summers of 2008-2014 off the coast of Cape Hatteras, North Carolina. Pilot whales were found to forage throughout the water column and performed feeding buzzes at depths ranging from 29-1176 meters. The results indicated potential habitat segregation in foraging depth in short-finned pilot whales with larger individuals foraging on average at deeper depths. Calculated aerobic dive limit for large adult males was approximately 6 minutes longer than that of females and likely facilitated the difference in foraging depth. Furthermore, the buzz frequency and speed around feeding attempts indicate this population pilot whales are likely targeting multiple small prey items. Using these results, I built decision trees to inform foraging dive classification in coarse, long-term dive data collected with SLTDRs deployed on 6 pilot whales in the summers of 2014 and 2015 in the same area off the coast of North Carolina. I used these long term foraging records to compare diurnal foraging rates and depths, as well as classify bouts with a maximum likelihood method, and evaluate behavioral aerobic dive limits (ADLB) through examination of dive durations and inter-dive intervals. Dive duration was the best predictor of foraging, with dives >400.6 seconds classified as foraging, and a 96% classification accuracy. There were no diurnal patterns in foraging depth or rates and average duration of bouts was 2.94 hours with maximum bout durations lasting up to 14 hours. The results indicated that pilot whales forage in relatively long bouts and the ADLB indicate that pilot whales rarely, if ever exceed their aerobic limits. To evaluate the response to predators I used controlled playback experiments to examine the behavioral responses of 10 of the tagged short-finned pilot whales off Cape Hatteras, North Carolina and 4 Risso’s dolphins (Grampus griseus) off Southern California to the calls of mammal-eating killer whales (MEK). Both species responded to a subset of MEK calls with increased movement, swim speed and increased cohesion of the focal groups, but the two species exhibited different directional movement and vocal responses. Pilot whales increased their call rate and approached the sound source, but Risso’s dolphins exhibited no change in their vocal behavior and moved in a rapid, directed manner away from the source. Thus, at least to a sub-set of mammal-eating killer whale calls, these two study species reacted in a manner that is consistent with their patterns of social organization. Pilot whales, which live in relatively permanent groups bound by strong social bonds, responded in a manner that built on their high levels of social cohesion. In contrast, Risso’s dolphins exhibited an exaggerated flight response and moved rapidly away from the sound source. The fact that both species responded strongly to a select number of MEK calls, suggests that structural features of signals play critical contextual roles in the probability of response to potential threats in odontocete cetaceans.