Too hot to handle: Unprecedented seagrass death driven by marine heatwave in a World Heritage Area.

The increased occurrence of extreme climate events, such as marine heatwaves (MHWs), has resulted in substantial ecological impacts worldwide. To date, metrics of thermal stress within marine systems have focussed on coral communities, and less is known about measuring stress relevant to other primary producers, such as seagrasses. An extreme MHW occurred across the Western Australian coastline in the austral summer of 2010-2011, exposing marine communities to summer seawater temperatures 2-5°C warmer than average. Using a combination of satellite imagery and in situ assessments, we provide detailed maps of seagrass coverage across the entire Shark Bay World Heritage Area (ca. 13,000 km2 ) before (2002 and 2010) and after the MHW (2014 and 2016). Our temporal analysis of these maps documents the single largest loss in dense seagrass extent globally (1,310 km2 ) following an acute disturbance. Total change in seagrass extent was spatially heterogeneous, with the most extensive declines occurring in the Western Gulf, Wooramel Bank and Faure Sill. Spatial variation in seagrass loss was best explained by a model that included an interaction between two heat stress metrics, the most substantial loss occurring when degree heating weeks (DHWm) was ≥10 and the number of days exposed to extreme sea surface temperature during the MHW (DaysOver) was ≥94. Ground truthing at 622 points indicated that change in seagrass cover was predominantly due to loss of Amphibolis antarctica rather than Posidonia australis, the other prominent seagrass at Shark Bay. As seawater temperatures continue to rise and the incidence of MHWs increase globally, this work will provide a basis for identifying areas of meadow degradation, or stability and recovery, and potential areas of resilience.

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.

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.

Potential impacts of environmental bacteria on the microbiota of loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtle eggs and their hatching success.

Sea turtle hatching success can be affected by many variables, including pathogenic microbes, but it is unclear which microbes are most impactful and how they are transmitted into the eggs. This study characterized and compared the bacterial communities from the (i) cloaca of nesting sea turtles (ii) sand within and surrounding the nests; and (iii) hatched and unhatched eggshells from loggerhead (Caretta caretta) and green (Chelonia mydas) turtles. High throughput sequencing of bacterial 16S ribosomal RNA gene V4 region amplicons was performed on samples collected from 27 total nests in Fort Lauderdale and Hillsboro beaches in southeast Florida, United States. Significant differences were identified between hatched and unhatched egg microbiota with the differences caused predominately by Pseudomonas spp., found in higher abundances in unhatched eggs (19.29% relative abundance) than hatched eggs (1.10% relative abundance). Microbiota similarities indicate that the nest sand environment, particularly nest distance from dunes, played a larger role than the nesting mother's cloaca in influencing hatched and unhatched egg microbiota. Pathogenic bacteria potentially derive from mixed-mode transmission or additional sources not included in this study as suggested by the high proportion (24%-48%) of unhatched egg microbiota derived from unknown sources. Nonetheless, the results suggest Pseudomonas as a candidate pathogen or opportunistic colonizer associated with sea turtle egg-hatching failure.

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.

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.

State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem.

1. A predictive framework of community and ecosystem dynamics that applies across systems has remained elusive, in part because non-consumptive predator effects are often ignored. Further, it is unclear how much individual-level detail community models must include. 2. Previous studies of short-lived species suggest that state-dependent decisions add little to our understanding of community dynamics. Body condition-dependent decisions made by long-lived herbivores under risk of predation, however, might have greater community-level effects. This possibility remains largely unexplored, especially in marine environments. 3. In the relatively pristine seagrass community of Shark Bay, Australia, we found that herbivorous green sea turtles (Chelonia mydas Linnaeus, 1758) threatened by tiger sharks (Galeocerdo cuvier Peron and LeSueur, 1822) select microhabitats in a condition-dependent manner. Turtles in poor body condition selected profitable, high-risk microhabitats, while turtles in good body condition, which are more abundant, selected safer, less profitable microhabitats. When predation risk was low, however, turtles in good condition moved into more profitable microhabitats. 4. Condition-dependent use of space by turtles shows that tiger sharks modify the spatio-temporal pattern of turtle grazing and their impacts on ecosystem dynamics (a trait-mediated indirect interaction). Therefore, state-dependent decisions by individuals can have important implications for community dynamics in some situations. 5. Our study suggests that declines in large-bodied sharks may affect ecosystems more substantially than assumed when non-lethal effects of these top predators on mesoconsumers are not considered explicitly.