Using Stable Isotopes to Investigate Trophic Interactions of Bottlenose Dolphins (Tursiops truncatus) in the Coastal Everglades”

Top predators are best known for their ability to affect their communities through inflicting mortality on prey and inducing behavioral modifications (e.g. risk effects). Recent scientific evidence suggests that predators may have additional roles in bottom-up processes such as transporting materials within and across habitat boundaries. The Florida Coastal Everglades (FCE) is an “upside-down” oligotrophic estuary where productivity decreases from the mouth of the estuary to freshwater marshes. Research in the FCE suggest that predators can act as mobile links between disparate habitats and can potentially affect nutrient and biogeochemical dynamics through localized behaviors (e.g. American alligators and juvenile bull sharks). To date, little is known about bottlenose dolphins (Tursiops truncatus) in the FCE beyond broad-scale patterns of abundance. Because they are highly mobile mammals commonly found in coastal waters, bottlenose dolphins are an interesting case study for investigating the influence of ecology on the evolution of local adaptations. Within this influence lies the potential for investigation of the related roles those adaptations play in coastal ecosystems due to their high metabolic rates, movement capabilities, and tendency to display specialized foraging behaviors. Stable isotope analysis of biopsy samples were used to investigate habitat use, trophic interactions, and patterns of individual specialization in bottlenose dolphins to gain functional insights into ecosystem dynamics. δ13 C isotopic values are used to differentiate the relative importance of a food web to the diet of an organism, while δ15 N values are used to evaluate the relative trophic position of an organism. Dolphin δ13 C isotopic values seem to suggest that dolphins are foraging within single ecosystems and may not be moving nutrients across ecosystem boundaries while their δ15 N isotopic values appear to be of a top predator, at a similar level to bull sharks and alligators in FCE. Further research is necessary to provide vital insight into the large predators’ role in affecting the evolution of local adaptations. Conducting this research should also provide information for predicting how future changes occurring due to restoration dynamics (see CERP: evergladesplan.org) and climate change will affect the ecological roles of these animals.

Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae

Since the industrial revolution, [CO2]atm has increased from 280 µatm to levels now exceeding 380 µatm and is expected to rise to 730-1,020 µatm by the end of this century. The consequent changes in the ocean's chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (delta pH 0.5; 0.16 % CO2, ~1,600 µatm) significantly (p < 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO2 (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.

Seawater carbonate chemistry and biological processes during experiments with a Sea Star Crassaster papposus, 2010

Ocean acidification (OA) is believed to be a major threat for near-future marine ecosystems, and that the most sensitive organisms will be calcifying organisms and the free-living larval stages produced by most benthic marine species. In this respect, echinoderms are one of the taxa most at risk. Earlier research on the impact of near-future OA on echinoderm larval stages showed negative effects, such as a decreased growth rate, increased mortality, and developmental abnormalities. However, all the long-term studies were performed on planktotrophic larvae while alternative life-history strategies, such as nonfeeding lecithotrophy, were largely ignored. Here, we show that lecithotrophic echinoderm larvae and juveniles are positively impacted by ocean acidification. When cultured at low pH, larvae and juveniles of the sea star Crossaster papposus grow faster with no visible affects on survival or skeletogenesis. This suggests that in future oceans, lecithotrophic species may be better adapted to deal with the threat of OA compared with planktotrophic ones with potentially important consequences at the ecosystem level. For example, an increase in populations of the top predator C. papposus will likely have huge consequences for community structure. Our results also highlight the importance of taking varying life-history strategies into account when assessing the impacts of climate change, an approach that also provides insight into understanding the evolution of life-history strategies.

DNA from historical and trophy samples provides insights into white shark population origins and genetic diversity

Characterizing genetic variation by retrospective genotyping of trophy or historical artifacts from endangered species is an important conservation tool. Loss of genetic diversity in top predators such as the white shark Carcharodon carcharias remains an issue, exacerbated in this species by declining, sometimes isolated philopatric populations. We successfully sequenced mitochondrial DNA (mtDNA) D-loop from osteodentine of contemporary South African white shark teeth (from 3 jaws), and from 34 to 129 yr old dried cartilage and skin samples from 1 Pacific Ocean and 5 Mediterranean sharks. Osteodentine-derived sequences from South African fish matched those derived from an individual’s finclips, but were generally of poorer quality than those from skin and cartilage of historical samples. Three haplotypes were identified from historical Mediterranean samples (n = 5); 2 individuals had unique sequences and 3 shared the contemporary Mediterranean haplotype. Placement of previously undescribed mtDNA haplotypes from historical material within both the Mediterranean and Pacific clades fits with the accepted intra-specific phylogeny derived from contemporary material, verifying our approaches. The utility of our methodology is in its provision of additional genetic resources from osteodentine (for species lacking tooth pulp) and cartilage of rare and endangered species held in often uncurated, contemporary and historical dry collections. Such material can usefully supplement estimates of connectivity, population history, and stock viability. We confirm the depauperate haplotype diversity of historical Mediterranean sharks, consistent with founding by a small number of Pacific colonizers. The consequent lack of diversity suggests serious challenges for the maintenance of this top predator and the Mediterranean ecosystem.

DNA from historical and trophy samples provides insights into white shark population origins and genetic diversity

Characterizing genetic variation by retrospective genotyping of trophy or historical artifacts from endangered species is an important conservation tool. Loss of genetic diversity in top predators such as the white shark Carcharodon carcharias remains an issue, exacerbated in this species by declining, sometimes isolated philopatric populations. We successfully sequenced mitochondrial DNA (mtDNA) D-loop from osteodentine of contemporary South African white shark teeth (from 3 jaws), and from 34 to 129 yr old dried cartilage and skin samples from 1 Pacific Ocean and 5 Mediterranean sharks. Osteodentine-derived sequences from South African fish matched those derived from an individual’s finclips, but were generally of poorer quality than those from skin and cartilage of historical samples. Three haplotypes were identified from historical Mediterranean samples (n = 5); 2 individuals had unique sequences and 3 shared the contemporary Mediterranean haplotype. Placement of previously undescribed mtDNA haplotypes from historical material within both the Mediterranean and Pacific clades fits with the accepted intra-specific phylogeny derived from contemporary material, verifying our approaches. The utility of our methodology is in its provision of additional genetic resources from osteodentine (for species lacking tooth pulp) and cartilage of rare and endangered species held in often uncurated, contemporary and historical dry collections. Such material can usefully supplement estimates of connectivity, population history, and stock viability. We confirm the depauperate haplotype diversity of historical Mediterranean sharks, consistent with founding by a small number of Pacific colonizers. The consequent lack of diversity suggests serious challenges for the maintenance of this top predator and the Mediterranean ecosystem.

Análise biogeográfica da dieta de um predador de topo ao longo da região Paleártica

Existem vários estudos sobre a dieta de predadores de topo a uma escala local, mas o estudo da dieta de uma espécie ao longo de diferentes regiões geográficas poderá permitir a deteção de certos padrões e variações ecológicas. Para estudar a variação biogeográfica da dieta do bufo-real (Bubo bubo) ao longo do Paleártico criou-se uma base de dados baseada em 192 estudos. Pretendia-se analisar padrões em macro-escala de descritores da dieta e avaliar o efeito de diferentes condições ambientais, de descritores da paisagem e da disponibilidade de presas. Registaram-se 346813 presas de 698 espécies distintas. As principais presas são os lagomorfos e os roedores, enquanto que as aves constituem importantes presas alternativas. Temperaturas mais elevadas favorecem a diversidade trófica, mas esta diminui com a latitude e a longitude. Os resultados revelam a natureza oportunista do bufo-real e a sua elevada adaptabilidade trófica a diferentes habitats e condições ambientais; Biogeographic analysis of a top predator's diet across the Paleartic Region Summary: There are several studies about top predators' diet at a local scale, but studying a species diet across different geographic regions may allow the detection of certain patterns and variations which might influence its ecological features. We created a database of 192 papers to study the diet of the Eurasian Eagle Owl (Bubo bubo) across the Palearctic region. We analysed large scale biogeographical patterns of diet descriptors in relation to different environmental conditions, including climate, landscape and prey availability. We recorded 346816 preys from 698 different species. The main prey groups are lagomorphs and rodents, whereas birds represent important alternative prey. Higher temperatures favour a higher trophic diversity, which in turn decreases at lower latitudes and longitudes. The results reveal the opportunistic nature of the Eurasian Eagle Owl and its high trophic adaptability to different habitats and environments.

Habitat-specific foraging strategies in Australasian gannets

Knowledge of top predator foraging adaptability is imperative for predicting their biological response to environmental variability. While seabirds have developed highly specialised techniques to locate prey, little is known about intraspecific variation in foraging strategies with many studies deriving information from uniform oceanic environments. Australasian gannets (Morus serrator) typically forage in continental shelf regions on small schooling prey. The present study used GPS and video data loggers to compare habitat-specific foraging strategies at two sites of contrasting oceanographic regimes (deep water near the continental shelf edge, n=23; shallow inshore embayment, n=26), in south-eastern Australia. Individuals from the continental shelf site exhibited pelagic foraging behaviours typical of gannet species, using local enhancement to locate and feed on small schooling fish; in contrast only 50% of the individuals from the inshore site foraged offshore, displaying the typical pelagic foraging strategy. The remainder adopted a strategy of searching sand banks in shallow inshore waters in the absence of conspecifics and other predators for large, single prey items. Furthermore, of the individuals foraging inshore, 93% were male, indicating that the inshore strategy may be sex-specific. Large inter-colony differences in Australasian gannets suggest strong plasticity in foraging behaviours, essential for adapting to environmental change.

Factors Influencing Movements and Foraging Ecology of American Alligators (Alligator mississippiensis) in a Dynamic Subtropical Coastal Ecosystem

Top predators can have large effects on community and population dynamics but we still know relatively little about their roles in ecosystems and which biotic and abiotic factors potentially affect their behavioral patterns. Understanding the roles played by top predators is a pressing issue because many top predator populations around the world are declining rapidly yet we do not fully understand what the consequences of their potential extirpation could be for ecosystem structure and function. In addition, individual behavioral specialization is commonplace across many taxa, but studies of its prevalence, causes, and consequences in top predator populations are lacking. In this dissertation I investigated the movement, feeding patterns, and drivers and implications of individual specialization in an American alligator (Alligator mississippiensis) population inhabiting a dynamic subtropical estuary. I found that alligator movement and feeding behaviors in this population were largely regulated by a combination of biotic and abiotic factors that varied seasonally. I also found that the population consisted of individuals that displayed an extremely wide range of movement and feeding behaviors, indicating that individual specialization is potentially an important determinant of the varied roles of alligators in ecosystems. Ultimately, I found that assuming top predator populations consist of individuals that all behave in similar ways in terms of their feeding, movements, and potential roles in ecosystems is likely incorrect. As climate change and ecosystem restoration and conservation activities continue to affect top predator populations worldwide, individuals will likely respond in different and possibly unexpected ways.

Diet of the blue marlin, Makaira nigricans, off the south coast of Portugal

The blue marlin, Makaira nigricans (Istiophoridae), is a large, top predator with a worldwide distribution whose feeding ecology is still unknown in the northeast Atlantic. The stomach contents of 24 Atlantic blue marlin, caught by the Big Game fishing fleet (between 2007 and 2010) off the south coast of Portugal, were studied. All marlin fed exclusively on pelagic fish, with a total of 180 prey items recorded, belonging to 6 identified species. The most important family in the blue marlin diet was Scombridae, representing 70% of the total prey items. Among the Scombridae, the chub mackerel, Scomber colias, was the most important prey species (47.9% by weight, 51.1% by number, 58.3% by frequency of occurrence). The length of prey found in the stomachs ranged from 136 to 727 mm in length, and a significant positive correlation was found between prey and blue marlin size. Our results suggest that in this geographical area (NE Atlantic) marlin feed on a small spectrum of species, with a preference for foraging on seamounts.

Prey preference of lingcod (Ophiodon elongatus), a top marine predator: implications for ecosystem-based fisheries management

Many highly exploited ecosystems are managed on the basis of single-species demographic information. This management approach can exacerbate tensions among stakeholders with competing interests who in turn rely on data with notoriously high variance. In this case study, an application of diet and dive survey data was used to describe the prey preference of lingcod (Ophiodon elongatus) in a predictive framework on nearshore reefs off Oregon. The lingcod is a large, fast-growing generalist predator of invertebrates and fishes. In response to concerns that lingcod may significantly reduce diminished populations of rockfishes (Sebastes spp.), the diets of 375 lingcod on nearshore reefs along the Oregon Coast were compared with estimates of relative prey availability from dive surveys. In contrast to the transient pelagic fishes that comprised 46% of lingcod diet by number, rockfishes comprised at most 4.7% of prey items. Rockfishes were the most abundant potential prey observed in dive surveys, yet they were the least preferred. Ecosystem-based fisheries management (EBFM) requires information about primary trophic relationships, as well as relative abundance and distribution data for multiple species. This study shows that, at a minimum, predation relative to prey availability must be considered before predator effects can be understood in a management context.

Underestimated and severe : small mammal decline from the forests of south-eastern Australia since European settlement, as revealed by a top-order predator

In Australia, numerous small mammal species have suffered extinction or severe declines in distribution and abundance following European settlement. The extent of these declines from forested areas of south-eastern Australia, however, remains poorly understood. In this paper we use sub-fossil deposits of the sooty owl (Tyto tenebricosa tenebricosa) as a tool for understanding the diversity of the small mammal palaeocommunity. These results are compared to the contemporary sooty owl diet from the same geographical region to investigate the degree of small mammal decline following European settlement. Of 28 mammal species detected in sub-fossil deposits and considered prey items of the sooty owl at the time of European settlement, only 10 species were detected in the contemporary sooty owl diet. Numerous small mammal species have not only recently suffered severe declines in distribution and abundance but have also recently undergone niche contraction, as they occupied a greater diversity of regions and habitats at the time of European settlement. For some species our understanding of their true ecological niche and ecological potential is therefore limited. The species that underwent the greatest declines occupied open habitat types or were terrestrial. The severity of decline is also likely to have resulted in severe disruption of ecosystem functions, with wide scale ecosystem consequences. There is an urgent need to improve small mammal conservation, to maintain crucial ecosystem functions performed by small mammals. It is recommended that broad-scale exotic predator control programs are conducted which may also provide suitable conditions for the re-introduction of locally extinct species.

More than mere numbers: the impact of lethal control on the social stability of a top-order predator

Population control of socially complex species may have profound ecological implications that remain largely invisible if only their abundance is considered. Here we discuss the effects of control on a socially complex top-order predator, the dingo (Canis lupus dingo). Since European occupation of Australia, dingoes have been controlled over much of the continent. Our aim was to investigate the effects of control on their abundance and social stability. We hypothesized that dingo abundance and social stability are not linearly related, and proposed a theoretical model in which dingo populations may fluctuate between three main states: (A) below carrying capacity and socially fractured, (B) above carrying capacity and socially fractured, or (C) at carrying capacity and socially stable. We predicted that lethal control would drive dingoes into the unstable states A or B, and that relaxation of control would allow recovery towards C. We tested our predictions by surveying relative abundance (track density) and indicators of social stability (scent-marking and howling) at seven sites in the arid zone subject to differing degrees of control. We also monitored changes in dingo abundance and social stability following relaxation and intensification of control. Sites where dingoes had been controlled within the previous two years were characterized by low scent-marking activity, but abundance was similar at sites with and without control. Signs of social stability steadily increased the longer an area was allowed to recover from control, but change in abundance did not follow a consistent path. Comparison of abundance and stability among all sites and years demonstrated that control severely fractures social groups, but that the effect of control on abundance was neither consistent nor predictable. Management decisions involving large social predators must therefore consider social stability to ensure their conservation and ecological functioning.

The role of productivity in the ecological and evolutionary dynamics of predator-prey interaction

Productivity is predicted to drive the ecological and evolutionary dynamics of predator-prey interaction through changes in resource allocation between different traits. However, resources are seldom constantly available and thus temporal variation in productivity could have considerable effect on the species' potential to evolve. To study this, three long-term microbial laboratory experiments were established where Serratia marcescens prey bacteria was exposed to predation of protist Tetrahymena thermophila in different prey resource environments. The consequences of prey resource availability for the ecological properties of the predator-prey system, such as trophic dynamics, stability, and virulence, were determined. The evolutionary changes in species traits and prey genetic diversity were measured. The prey defence evolved stronger in high productivity environment. Increased allocation to defence incurred cost in terms of reduced prey resource use ability, which probably constrained prey evolution by increasing the effect of resource competition. However, the magnitude of this trade-off diminished when measured in high resource concentrations. Predation selected for white, non-pigmented, highly defensive prey clones that produced predation resistant biofilm. The biofilm defence was also potentially accompanied with cytotoxicity for predators and could have been traded off with high motility. Evidence for the evolution of predators was also found in one experiment suggesting that co-evolutionary dynamics could affect the evolution and ecology of predator-prey interaction. Temporal variation in resource availability increased variation in predator densities leading to temporally fluctuating selection for prey defences and resource use ability. Temporal variation in resource availability was also able to constrain prey evolution when the allocation to defence incurred high cost. However, when the magnitude of prey trade-off was small and the resource turnover was periodically high, temporal variation facilitated the formation of predator resistant biofilm. The evolution of prey defence constrained the transfer of energy from basal to higher trophic levels, decreasing the strength of top-down regulation on prey community. Predation and temporal variation in productivity decreased the stability of populations and prey traits in general. However, predation-induced destabilization was less pronounced in the high productivity environment where the evolution of prey defence was stronger. In addition, evolution of prey defence weakened the environmental variation induced destabilization of predator population dynamics. Moreover, protozoan predation decreased the S. marcescens virulence in the insect host moth (Parasemia plantaginis) suggesting that species interactions outside the context of host-pathogen relationship could be important indirect drivers for the evolution of pathogenesis. This thesis demonstrates that rapid evolution can affect various ecological properties of predator-prey interaction. The effect of evolution on the ecological dynamics depended on the productivity of the environment, being most evident in the constant environments with high productivity.

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.

Encounter success of free-ranging marine predator movements across a dynamic prey landscape

Movements of wide-ranging top predators can now be studied effectively using satellite and archival telemetry. However, the motivations underlying movements remain difficult to determine because trajectories are seldom related to key biological gradients, such as changing prey distributions. Here, we use a dynamic prey landscape of zooplankton biomass in the north-east Atlantic Ocean to examine active habitat selection in the plankton-feeding basking shark Cetorhinus maximus. The relative success of shark searches across this landscape was examined by comparing prey biomass encountered by sharks with encounters by random-walk simulations of ‘model’ sharks. Movements of transmitter-tagged sharks monitored for 964 days (16754km estimated minimum distance) were concentrated on the European continental shelf in areas characterized by high seasonal productivity and complex prey distributions. We show movements by adult and sub-adult sharks yielded consistently higher prey encounter rates than 90% of random-walk simulations. Behavioural patterns were consistent with basking sharks using search tactics structured across multiple scales to exploit the richest prey areas available in preferred habitats. Simple behavioural rules based on learned responses to previously encountered prey distributions may explain the high performances. This study highlights how dynamic prey landscapes enable active habitat selection in large predators to be investigated from a trophic perspective, an approach that may inform conservation by identifying critical habitat of vulnerable species.