Derek A. Burkholder

Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics

1. Risk effects of predators can profoundly affect community dynamics, but the nature of these effects is context dependent. 2. Although context dependence has hindered the development of a general framework for predicting the nature and extent of risk effects, recent studies suggest that such a framework is attainable if the factors that shape anti-predator behaviour, and its effectiveness, in natural communities are well understood. 3. One of these factors, the interaction of prey escape tactics and landscape features, has been largely overlooked. 4. We tested whether this interaction gives rise to interspecific variation in habitat-use patterns of sympatric large marine vertebrates at risk of tiger shark (Galeocerdo cuvier Peron and LeSueur, 1822) predation. Specifically, we tested the a priori hypothesis that pied cormorants (Phalacrocorax varius Gmelin, 1789) would modify their use of shallow seagrass habitats in a manner opposite to that of previously studied dolphins (Tursiops aduncus Ehrenberg, 1833), dugongs (Dugong dugon Müller, 1776), and green turtles (Chelonia mydas Linnaeus, 1758) because, unlike these species, the effectiveness of cormorant escape behaviour does not vary spatially. 5. As predicted, cormorants used interior and edge portions of banks proportional to the abundance of their potential prey when sharks were absent but shifted to interior portions of banks to minimize encounters with tiger sharks as predation risk increased. Other shark prey, however, shift to edge microhabitats when shark densities increase to take advantage of easier escape despite higher encounter rates with sharks. 6. The interaction of landscape features and escape ability likely is important in diverse communities. 7. When escape probabilities are high in habitats with high predator density, risk effects of predators can reverse the direction of commonly assumed indirect effects of top predators. 8. The interaction between landscape features and prey escape tactics can result in a single predator species having differential effects on their sympatric prey that could cascade through ecosystems and should be incorporated into a general framework for context dependence of risk effects.

Patterns of Top-Down Control in a Seagrass Ecosystem: Could a Roving Apex Predator Induce a Behaviour-Mediated Trophic Cascade?

1. The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in ecosystems around the world, but there remain important questions regarding the contexts in which such changes are most likely and the mechanisms through which they occur, particularly in marine ecosystems. 2. We used long-term exclusion cages to examine the effects of large grazers (sea cows, Dugong dugon; sea turtles Chelonia mydas) on seagrass community structure, biomass and nutrient dynamics. Experiments were conducted in habitats with high risk of predation (interior of shallow banks) and lower risk (edges of banks) to elucidate whether nonconsumptive (risk) effects of tiger sharks (Galeocerdo cuvier), a roving predator, structure herbivore impacts on seagrasses. 3. In lower-risk habitats, excluding large herbivores resulted in increased leaf length for Cymodocea angustata and Halodule uninervis. C. angustata shoot densities nearly tripled when released from herbivory, while H. uninervis nearly disappeared from exclusion cages over the course of the study. 4. We found no support for the hypothesis that grazing increases seagrass nutrient content. Instead, phosphorus content was higher in seagrasses within exclosures. This pattern is consistent with decreased light availability in the denser C. angustata canopies that formed in exclosures, and may indicate that competition for light led to the decrease in H. uninervis. 5. Impacts of large grazers were consistent with a behaviour-mediated trophic cascade (BMTC) initiated by tiger sharks and mediated by risk-sensitive foraging by large grazers. 6, Our results suggest that large-bodied grazers likely played important roles in seagrass ecosystem dynamics historically and that roving predators are capable of initiating a BMTC. Conservation efforts in coastal ecosystems must account for such interactions or risk unintended consequences.

Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem.

Extreme climatic events can trigger abrupt and often lasting change in ecosystems via the reduction or elimination of foundation (i.e., habitat-forming) species. However, while the frequency/intensity of extreme events is predicted to increase under climate change, the impact of these events on many foundation species and the ecosystems they support remains poorly understood. Here, we use the iconic seagrass meadows of Shark Bay, Western Australia--a relatively pristine subtropical embayment whose dominant, canopy-forming seagrass, Amphibolis antarctica, is a temperate species growing near its low-latitude range limit--as a model system to investigate the impacts of extreme temperatures on ecosystems supported by thermally sensitive foundation species in a changing climate. Following an unprecedented marine heat wave in late summer 2010/11, A. antarctica experienced catastrophic (>90%) dieback in several regions of Shark Bay. Animal-borne video footage taken from the perspective of resident, seagrass-associated megafauna (sea turtles) revealed severe habitat degradation after the event compared with a decade earlier. This reduction in habitat quality corresponded with a decline in the health status of largely herbivorous green turtles (Chelonia mydas) in the 2 years following the heat wave, providing evidence of long-term, community-level impacts of the event. Based on these findings, and similar examples from diverse ecosystems, we argue that a generalized framework for assessing the vulnerability of ecosystems to abrupt change associated with the loss of foundation species is needed to accurately predict ecosystem trajectories in a changing climate. This includes seagrass meadows, which have received relatively little attention in this context. Novel research and monitoring methods, such as the analysis of habitat and environmental data from animal-borne video and data-logging systems, can make an important contribution to this framework.

Seagrasses in the age of sea turtle conservation and shark overfishing

Efforts to conserve globally declining herbivorous green sea turtles have resulted in promising growth of some populations. These trends could significantly impact critical ecosystem services provided by seagrass meadows on which turtles feed. Expanding turtle populations could improve seagrass ecosystem health by removing seagrass biomass and preventing of the formation of sediment anoxia. However, overfishing of large sharks, the primary green turtle predators, could facilitate turtle populations growing beyond historical sizes and trigger detrimental ecosystem impacts mirroring those on land when top predators were extirpated. Experimental data from multiple ocean basins suggest that increasing turtle populations can negatively impact seagrasses, including triggering virtual ecosystem collapse. Impacts of large turtle populations on seagrasses are reduced in the presence of intact shark populations. Healthy populations of sharks and turtles, therefore, are likely vital to restoring or maintaining seagrass ecosystem structure, function, and their value in supporting fisheries and as a carbon sink.

Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem

Understanding forage choice of herbivores is important for predicting the potential impacts of changes in their abundance. Such studies, however, are rare in ecosystems with intact populations of both megagrazers (sirenians, sea turtles) and fish grazers. We used feeding assays and nutrient analyses of seagrasses to determine whether forage choice of grazers in Shark Bay, Australia, are influenced by the quality of seagrasses. We found significant interspecific variation in removal rates of seagrasses across three habitats (shallow seagrass bank interior, shallow seagrass bank edge, deep), but we did not detect variation in gazing intensity among habitats. In general, grazers were more likely to consume fast-growing species with lower carbon : nitrogen (C : N) and carbon : phosphorus (C : P) ratios, than the slower-growing species that are dominant in the bay. Grazer choices were not, however, correlated with nutrient content within the tropical seagrasses. Slow-growing temperate seagrasses that experienced lower herbivory provide greater habitat value as a refuge for fishes and may facilitate fish grazing on tropical species. Further studies are needed, however, to more fully resolve the factors influencing grazer foraging preferences and the possibility that grazers mediate indirect interactions among seagrass species.

Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter to consumers in a pristine seagrass ecosystem

The relative importance of the identity and abundance of primary producers in structuring trophic ecology, particularly in seagrass-dominated ecosystems, remains unclear. We assessed the contributions of seagrass, epiphytes, macroalgae, and other primary producers to the diets of resident animals in the nearly pristine seagrass-dominated environment of Shark Bay, Australia, by combining fatty acid composition with carbon, nitrogen, and sulfur stable isotopes of primary producers and consumers. Overall, mixed inputs of these primary producers fuel secondary production, with tropical detrital seagrass inputs supporting most fish species, likely through benthic intermediates. Epiphytic organic matter inputs were most closely associated with snails, whereas seagrass detritus, macroalgae, gelatinous zooplankton, and/or phytoplankton may all contribute to higher trophic levels including sea turtles and sharks. The fatty acid and isotope data suggest that diets of large-bodied consumers were highly variable – future food web studies need to incorporate large sample sizes to account for this variability.

Validation of a rapid visual-assessment technique for categorizing the body condition of Green Turtles (Chelonia mydas) in the field.

Abstract Many important questions in ecology and conservation biology require assessment of the body condition of animals, which is often achieved using mass and length data. However, fully quantitative condition indices can be difficult to obtain in the field for large taxa like marine turtles. Therefore, rapid visual-assessment techniques for categorizing condition can be useful for field studies. Here, we test whether a visual method of categorizing body condition in the Green Turtle (Chelonia mydas) based on the shape of a turtles plastron is comparable to two commonly used body condition indices derived from mass and length measurements. Condition scores for both mass–length indices varied in the expected manner with our visual condition categories, verifying that the rapid visual assessment technique accurately reflects differences in body condition. This technique should aid many field studies of turtles where body condition data are required but mass data cannot easily be obtained.

The trophic role of a large marine predator, the tiger shark Galeocerdo cuvier

Tiger sharks were sampled off the western (Ningaloo Reef, Shark Bay) and eastern (the Great Barrier Reef; GBR, Queensland and New South Wales; NSW) coastlines of Australia. Multiple tissues were collected from each shark to investigate the effects of location, size and sex of sharks on δ13C and δ15N stable isotopes among these locations. Isotopic composition of sharks sampled in reef and seagrass habitats (Shark Bay, GBR) reflected seagrass-based food-webs, whereas at Ningaloo Reef analysis revealed a dietary transition between pelagic and seagrass food-webs. In temperate habitats off southern Queensland and NSW coasts, shark diets relied on pelagic food-webs. Tiger sharks occupied roles at the top of food-webs at Shark Bay and on the GBR, but not at Ningaloo Reef or off the coast of NSW. Composition of δ13C in tissues was influenced by body size and sex of sharks, in addition to residency and diet stability. This variability in stable isotopic composition of tissues is likely to be a result of adaptive foraging strategies that allow these sharks to exploit multiple shelf and offshore habitats. The trophic role of tiger sharks is therefore both context- and habitat-dependent, consistent with a generalist, opportunistic diet at the population level.