Fear of predators alters herbivore regulation of soil microbial community function.

Fear of predation can affect important ecosystem processes by altering the prey traits expression that, in turn, regulates the quantity and quality of nutritional inputs to soil. Here, we aimed to assist in bridging a knowledge gap in this cascading chain of events by exploring how risk of spider predation may affect grasshopper prey performances, and the activity of various microbial extracellular enzymes in the soil. Using a mesocosms field-experiment, we found that grasshoppers threatened by spider predation ate less, grew slower, and had a higher body carbon to nitrogen ratio. Herbivory increased activity of all microbial extracellular enzymes examined, likely due to higher availability of root exudates. Predation risk had no effect on C-acquiring enzymes but decreased activity of P-acquiring enzymes. We found contrasting results regarding the effect of predation on the activity of N-acetyl-glucosaminidase and leucine arylamidase N-acquiring enzymes, suggesting that predation risk may alter the composition of N-inputs to soil. Our work highlighted the importance of soil microbial enzymatic activity as a way to predict how changes in the aboveground food-web dynamics may alter key ecosystem processes like nutritional-cycling.

Top ten priorities for global saltmarsh restoration, conservation and ecosystem service research.

Coastal saltmarshes provide globally important ecosystem services including 'blue carbon' sequestration, flood protection, pollutant remediation, habitat provision and cultural value. Large portions of marshes have been lost or fragmented as a result of land reclamation, embankment construction, and pollution. Sea level rise threatens marsh survival by blocking landward migration where coastlines have been developed. Research-informed saltmarsh conservation and restoration efforts are helping to prevent further loss, yet significant knowledge gaps remain. Using a mixed methods approach, this paper identifies ten research priorities through an online questionnaire and a residential workshop attended by an international, multi-disciplinary network of 35 saltmarsh experts spanning natural, physical and social sciences across research, policy, and practitioner sectors. Priorities have been grouped under four thematic areas of research: Saltmarsh Area Extent, Change and Restoration Potential (including past, present, global variation), Spatio-social contexts of Ecosystem Service delivery (e.g. influences of environmental context, climate change, and stakeholder groups on service provisioning), Patterns and Processes in saltmarsh functioning (global drivers of saltmarsh ecosystem structure/function) and Management and Policy Needs (how management varies contextually; challenges/opportunities for management). Although not intended to be exhaustive, the challenges, opportunities, and strategies for addressing each research priority examined here, providing a blueprint of the work that needs to be done to protect saltmarshes for future generations.

Identifying conservation priorities for a widespread dugong population in the Red Sea: Megaherbivore grazing patterns inform management planning.

Extensive home ranges of marine megafauna present a challenge for systematic conservation planning because they exceed spatial scales of conventional management. For elusive species like dugongs, their management is additionally hampered by a paucity of basic distributional information across much of their range. The Red Sea is home to a wide-spread, globally important but data-poor population of dugongs. We surveyed the north-eastern Red Sea in the waters of NEOM, Kingdom of Saudi Arabia, to locate feeding sites and determine priority areas for dugong conservation. We conducted large-scale in-water surveys of dugong feeding trails across 27 seagrass meadows that span 0.7 degree of latitude and recorded nine seagrass species and 13 dugong feeding sites. Spread over ∼4'061 km2 of nearshore and offshore waters, many of these sites clustered around five main core feeding areas. Dugong feeding trails were mostly recorded at sites dominated by the fast-growing pioneer seagrasses Halodule uninervis, Halophila ovalis and/or H. stipulacea. Multispecific meadows with pioneer seagrasses tended to be sheltered and shallow, reflecting a similar spatial pattern to the identified dugong feeding sites. Often close to hotels and fishing harbours, these high-use dugong areas are subject to high boat traffic, fishing, and coastal development which places considerable pressures on this vulnerable mammal and its seagrass habitat. The rapidly accelerating coastal development in the northern Red Sea directly threatens the future of its dugong population. Although our sampling focuses on feeding signs in early successional seagrasses, the results are valuable to spatial conservation planning as they will trigger overdue conservation interventions for a globally threatened species in a data-poor area. Urgent dugong conservation management actions in the northern Red Sea should focus on shallow waters sheltered by coastal lagoons, bays and the lee of large islands.

The scent of fear makes sea urchins go ballistic.

BACKGROUND: Classic ecological formulations of predator-prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger some form of escape response to reduce the probability of capture. Here, we explore under laboratory-controlled conditions the long-term (minutes to hours) escaping response of the sea urchin Paracentrotus lividus, a key species in Mediterranean subtidal macrophyte communities. METHODS: Behavioural experiments involved exposing a random sample of P. lividus to either one of two treatments: (i) control water (filtered seawater) or (ii) predator-conditioned water (with cues from the main P. lividus benthic predator-the gastropod Hexaplex trunculus). We analysed individual sea urchin trajectories, computed their heading angles, speed, path straightness, diffusive properties, and directional entropy (as a measure of path unpredictability). To account for the full picture of escaping strategies, we followed not only the first instants post-predator exposure, but also the entire escape trajectory. We then used linear models to compare the observed results from control and predators treatments. RESULTS: The trajectories from sea urchins subjected to predator cues were, on average, straighter and faster than those coming from controls, which translated into differences in the diffusive properties and unpredictability of their movement patterns. Sea urchins in control trials showed complex diffusive properties in an information-limited environment, with highly variable trajectories, ranging from Brownian motion to superdiffusion, and even marginal ballistic motion. In predator cue treatments, variability reduced, and trajectories became more homogeneous and predictable at the edge of ballistic motion. CONCLUSIONS: Despite their old evolutionary origin, lack of cephalization, and homogenous external appearance, the trajectories that sea urchins displayed in information-limited environments were complex and ranged widely between individuals. Such variable behavioural repertoire appeared to be intrinsic to the species and emerged when the animals were left unconstrained. Our results highlight that fear from predators can be an important driver of sea urchin movement patterns. All in all, the observation of anomalous diffusion, highly variable trajectories and the behavioural shift induced by predator cues, further highlight that the functional forms currently used in classical predator-prey models are far from realistic.

Warming intensifies the interaction between the temperate seagrass Posidonia oceanica and its dominant fish herbivore Sarpa salpa.

Apart from directly influencing individual life histories of species, climate change is altering key biotic interactions as well, causing community processes to unravel. With rising temperatures, disruptions to producer-consumer relationships can have major knock-on effects, particularly when the producer is a habitat-forming species. We studied how sea surface temperature (SST) modifies multiple pathways influencing the interaction between the foundational seagrass species, Posidonia oceanica, and its main consumer, the fish Sarpa salpa in the Mediterranean Sea. We used a combination of a field-based temperature gradient approaches and experimental manipulations to assess the effect of temperature on seagrass performance (growth) and fish early life history (larval development) as well as on the interaction itself (seagrass palatability and fish foraging activity). Within the range of temperatures assessed, S. salpa larvae grew slightly faster at warmer conditions but maintained their settlement size, resulting in a relatively small reduction in pelagic larval duration (PLD) and potentially reducing dispersion. Under warmer conditions (>24 °C), P. oceanica reduced its growth rate considerably and seemed to display fewer deterring mechanisms as indicated by a disproportionate consumption in choice experiments. However, our field-based observations along the temperature gradient showed no change in fish foraging time, or in other aspects of feeding behaviour. As oceans warm, our results indicate that, while S. salpa may show little change in early life history, its preference towards P. oceanica might increase, which, together with reduced seagrass growth, could considerably intensify the strength of herbivory. It is unclear if P. oceanica meadows can sustain such an intensification, but it will clearly add to the raft of pressures this threatened ecosystem already faces from global and local environmental change.

The dominant seagrass herbivore Sarpa salpa shifts its shoaling and feeding strategies as they grow.

The relative benefits of group foraging change as animals grow. Metabolic requirements, competitive abilities and predation risk are often allometric and influenced by group size. How individuals optimise costs and benefits as they grow can strongly influence consumption patterns. The shoaling fish Sarpa salpa is the principal herbivore of temperate Posidonia oceanica seagrass meadows. We used in-situ observations to describe how ontogeny influenced S. salpa individual feeding behaviour, shoaling behaviour and group foraging strategies, and its potential consequences to seagrass meadows. Shoaling was strongly influenced by body length: shoals were highly length-assorted and there was a clear positive relationship between body length and shoal size. Foraging strategies changed dramatically with shoal size. Small shoals foraged simultaneously and scattered over large areas. In contrast, larger shoals (made of larger individuals) employed a potentially cooperative strategy where individuals fed rotationally and focused in smaller areas for longer times (spot feeding). Thus, as individuals grew, they increased their potential impact as well, not merely because they consumed more, but because they formed larger shoals capable of considerably concentrating their grazing within the landscape. Our results indicate that ontogenetic shifts in group foraging strategies can have large ecosystem-wide consequences when the species is an important ecosystem modifier.

Consumptive and non-consumptive effects of predators vary with the ontogeny of their prey.

Predators exert a strong influence on ecological communities by reducing the abundance of prey (consumptive effects) and shaping their foraging behavior (non-consumptive effects). Although the prevalence of trophic cascades triggered by non-consumptive effects is increasingly recognized in a wide range of ecosystems, how its relative strength changes as prey individuals grow in size along various life stages remains poorly resolved. We investigated how the effects of predators vary with the ontogeny of a key herbivorous sea urchin, which is responsible for transforming diverse macroalgal forests to a barren state dominated by bare rock and encrusting coralline algae. We conducted a series of field and laboratory experiments to determine how susceptibility to predation, prey behavioral responses, and grazing impact on algal cover vary with sea urchin size. The consumptive effects of predators were greater on smaller sea urchin size classes, which were more susceptible to predation. Unexpectedly however, predator non-consumptive effects acted only on larger sea urchins, significantly reducing their grazing activity in the presence of predator cues. Crucially, only these larger sea urchins were capable of overgrazing macroalgae in the field, with non-consumptive effects reducing sea urchin foraging activity and macroalgal grazing impact by 60%. The decoupling between risk and fear as prey grow indicates that the strength of consumptive and non-consumptive trophic cascades may act differently at different ontogenetic stages of prey. While the consumptive effects of predators directly influence population numbers, the consequences of non-consumptive effects may far outlive consumptive effects as prey grow, finding refuge in size, but not from fear.

The richness of small pockets: Decapod species peak in small seagrass patches where fish predators are absent.

Patchy landscapes behave differently from continuous ones. Patch size can influence species behaviour, movement, feeding and predation rates, with flow-on consequences for the diversity of species that inhabit these patches. To understand the importance of patchiness on regional species pools, we measured decapod richness and abundance in several seagrass patches with contrasting sizes. Additionally, we evaluated potential drivers of patch-specific species distribution including resource abundance, predator habitat use and the structural complexity of patches. Our results showed a non-random distribution of decapod species: small patches were clear hotspots of diversity and abundance, particularly of larger-bodied epifaunal decapods. Interestingly, these hotspots were characterized by lower nutrient resources, lower canopy height, but also lower predator use. Small fish invertivores such as Coris julis and several species of Symphodus were mostly restricted to large patches. These resident predators may be critical in clumping predation in large patches with consequences for how biodiversity of their prey is distributed across the seascape. Our results highlight the idea that a habitat mosaic with both large and small seagrass patches would potentially bolster biodiversity because preys and predators may seek refuge in patches of different sizes.

Contrasting effects of ocean warming on different components of plant-herbivore interactions.

There is increasing uncertainty of how marine ecosystems will respond to rising temperatures. While studies have focused on the impacts of warming on individual species, knowledge of how species interactions are likely to respond is scant. The strength of even simple two-species interactions is influenced by several interacting mechanisms, each potentially changing with temperature. We used controlled experiments to assess how plant-herbivore interactions respond to temperature for three structural dominant macrophytes in the Mediterranean and their principal sea urchin herbivore. Increasing temperature differentially influenced plant-specific growth, sea urchin growth and metabolism, consumption rates and herbivore preferences, but not movement behaviour. Evaluating these empirical observations against conceptual models of plant-herbivore performance, it appears likely that while the strength of herbivory may increase for the tested macroalga, for the two dominant seagrasses, the interaction strength may remain relatively unchanged or even weaken as temperatures rise. These results show a clear set of winners and losers in the warming Mediterranean as the complex factors driving species interactions change.

Immanent conditions determine imminent collapses: nutrient regimes define the resilience of macroalgal communities.

Predicting where state-changing thresholds lie can be inherently complex in ecosystems characterized by nonlinear dynamics. Unpacking the mechanisms underlying these transitions can help considerably reduce this unpredictability. We used empirical observations, field and laboratory experiments, and mathematical models to examine how differences in nutrient regimes mediate the capacity of macrophyte communities to sustain sea urchin grazing. In relatively nutrient-rich conditions, macrophyte systems were more resilient to grazing, shifting to barrens beyond 1 800 g m-2 (urchin biomass), more than twice the threshold of nutrient-poor conditions. The mechanisms driving these differences are linked to how nutrients mediate urchin foraging and algal growth: controlled experiments showed that low-nutrient regimes trigger compensatory feeding and reduce plant growth, mechanisms supported by our consumer-resource model. These mechanisms act together to halve macrophyte community resilience. Our study demonstrates that by mediating the underlying drivers, inherent conditions can strongly influence the buffer capacity of nonlinear systems.

The Mediterranean benthic herbivores show diverse responses to extreme storm disturbances.

Catastrophic storms have been observed to be one of the major elements in shaping the standing structure of marine benthic ecosystems. Yet, little is known about the effect of catastrophic storms on ecosystem processes. Specifically, herbivory is the main control mechanism of macrophyte communities in the Mediterranean, with two main key herbivores: the sea urchin Paracentrotus lividus and the fish Sarpa salpa. Consequently, the effects of extreme storm events on these two herbivores (at the population level and on their behaviour) may be critical for the functioning of the ecosystem. With the aim of filling this gap, we took advantage of two parallel studies that were conducted before, during and after an unexpected catastrophic storm event. Specifically, fish and sea urchin abundance were assessed before and after the storm in monitored fixed areas (one site for sea urchin assessment and 3 sites for fish visual transects). Additionally, we investigated the behavioural response to the disturbance of S. salpa fishes that had been tagged with acoustic transmitters. Given their low mobility, sea urchins were severely affected by the storm (ca. 50% losses) with higher losses in those patches with a higher density of sea urchins. This may be due to a limited availability of refuges within each patch. In contrast, fish abundance was not affected, as fish were able to move to protected areas (i.e. deeper) as a result of the high mobility of this species. Our results highlight that catastrophic storms differentially affect the two dominant macroherbivores of rocky macroalgal and seagrass systems due to differences in mobility and escaping strategies. This study emphasises that under catastrophic disturbances, the presence of different responses among the key herbivores of the system may be critical for the maintenance of the herbivory function.