Tolerance to aerial exposure influences distributional patterns in multi-species intertidal seagrass meadows.

Multi-specific seagrass meadow assemblages dominate most tropical intertidal regions but the relative role of environmental stress in determining distribution patterns is still uncertain. Here we combine observational and experimental approaches to examine aerial exposure as a factor driving species occurrence patterns in intertidal meadows of the Andaman archipelago, where up to 6 seagrass species co-occur. In the studied meadow, patterns of exposure did not map onto distance from the coast, instead creating a patchy matrix of exposure, based on fine-scale bathymetric differences. Distributional surveys showed that seagrass species were similarly patchy, often tracking the degree of aerial exposure during low tide. While some species (Halophila ovalis, Halophila minor, and Thalassia hemprichii) frequently occurred in submerged or subtidal areas and were rarely found in completely exposed areas, other species (Cymodocea rotundata, Halophila beccarii, and Halodule uninervis) also occupied areas that were subject to partial or complete aerial exposure during low tide. To confirm this pattern, we used field-based transplant experiments, employing a natural gradient of tidal exposure to subject six seagrass species to different desiccation exposure times. After a month, H. beccarii and H. uninervis transplants survived in areas that sustained more than 3 h of aerial tidal exposure without significant mortality, compared with other species (H. ovalis, H. minor, T. hemprichii, C. rotundata) that showed dramatic shoot mortality at the same exposure regimes. For all species, 4 h represented the upper limit of exposure, in both experimental and distributional studies. However, despite their wider tolerance of exposure to air, H. beccarii and H. uninervis did not dominate the entire meadow. This could be a result either of their poor tolerance to other environmental factors or their lower competitive abilities among other mechanisms. This suggests that in tropical multi-specific meadows, strong environmental filters could override clear intertidal zonation to create patchy matrices based on species tolerances.

Tropicalization shifts herbivore pressure from seagrass to rocky reef communities.

Climate-driven species redistributions are reshuffling the composition of marine ecosystems. How these changes alter ecosystem functions, however, remains poorly understood. Here we examine how impacts of herbivory change across a gradient of tropicalization in the Mediterranean Sea, which includes a steep climatic gradient and marked changes in plant nutritional quality and fish herbivore composition. We quantified individual feeding rates and behaviour of 755 fishes of the native Sarpa salpa, and non-native Siganus rivulatus and Siganus luridus. We measured herbivore and benthic assemblage composition across 20 sites along the gradient, spanning 30° of longitude and 8° of latitude. We coupled patterns in behaviour and composition with temperature measurements and nutrient concentrations to assess changes in herbivory under tropicalization. We found a transition in ecological impacts by fish herbivory across the Mediterranean from a predominance of seagrass herbivory in the west to a dominance of macroalgal herbivory in the east. Underlying this shift were changes in both individual feeding behaviour (i.e. food choice) and fish assemblage composition. The shift in feeding selectivity was consistent among temperate and warm-affiliated herbivores. Our findings suggest herbivory can contribute to the increased vulnerability of seaweed communities and reduced vulnerability of seagrass meadows in tropicalized ecosystems.

Learning takes time: Biotic resistance by native herbivores increases through the invasion process.

As invasive species spread, the ability of local communities to resist invasion depends on the strength of biotic interactions. Evolutionarily unused to the invader, native predators or herbivores may be initially wary of consuming newcomers, allowing them to proliferate. However, these relationships may be highly dynamic, and novel consumer-resource interactions could form as familiarity grows. Here, we explore the development of effective biotic resistance towards a highly invasive alga using multiple space-for-time approaches. We show that the principal native Mediterranean herbivore learns to consume the invader within less than a decade. At recently invaded sites, the herbivore actively avoided the alga, shifting to distinct preference and high consumptions at older sites. This rapid strengthening of the interaction contributed to the eventual collapse of the alga after an initial dominance. Therefore, our results stress the importance of conserving key native populations to allow communities to develop effective resistance mechanisms against invaders.

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.

Understanding the depth limit of the seagrass Cymodocea nodosa as a critical transition: Field and modeling evidence.

Changes in light and sediment conditions can sometimes trigger abrupt regime shifts in seagrass meadows resulting in dramatic and unexpected die-offs of seagrass. Light attenuates rapidly with depth, and in seagrass systems with non-linear behaviours, can serve as a sharp boundary beyond which the meadow transitions to bare sand. Determining system behaviour is therefore essential to ensuring resilience is maintained and to prevent stubborn critical ecosystem transitions caused by declines in water quality. Here we combined field and modelling studies to explore the transition from meadow to bare sand in the seagrass Cymodocea nodosa at the limit of its depth distribution in a shallow, light-limited bay. We first describe the relationship between light availability and seagrass density along a depth gradient in an extensive unfragmented meadow (Alfacs bay, NE Spain). We then develop a simple mechanistic model to characterise system behaviour. In the field, we identified sharp decline in shoot density beyond a threshold of ∼1.9 m depth, shifting from a vegetated state to bare sand. The dynamic population model we developed assumes light-dependent growth and an inverse density-dependent mortality due to facilitation between shoots (mortality rate decreases as shoot density increases). The model closely tracked our empirical observations, and both the model and the field data showed signs of bistability. This strongly suggests that the depth limit of C. nodosa is a critical transition driven by photosynthetic light requirements. While the mechanisms still need to be confirmed with experimental evidence, recognizing the non-linear behaviour of C. nodosa meadows is vital not only in improving our understanding of light effects on seagrass dynamics, but also in managing shallow-water meadows. Given the shallow threshold (<2m), light-limited systems may experience significant and recalcitrant meadow retractions with even small changes in sediment and light conditions. Understanding the processes underlying meadow resilience can inform the maintenance and restoration of meadows worldwide.

Exploring coexistence mechanisms in a three-species assemblage.

Interactions among species are essential in shaping ecological communities, although it is not always clear under what conditions they can persist when the number of species involved is higher than two. Here we describe a three-species assemblage involving the seagrass Cymodocea nodosa, the pen shell Pinna nobilis and the herbivore sea urchin Paracentrotus lividus, and we explore the mechanisms allowing its persistence through field observations and manipulative experiments. The abundance of pen shells was higher in seagrass beds than in bare sand, suggesting a recruitment facilitation. The presence of sea urchins, almost exclusively attached or around pen shells, indicated habitat facilitation for sea urchins, which overgrazed the meadow around the pen shells forming seagrass-free halos. Our results suggest that this system persists thanks to: (i) the behavioral reluctance of sea urchins to move far from pen shells, making their impact on seagrass strictly local, (ii) the sparse distribution of pen shells and (iii) the plant's resistance mechanisms to herbivory. Unpacking these mechanisms allows a better understanding of how ecological communities are assembled.

Temperature reduces fish dispersal as larvae grow faster to their settlement size.

As species struggle to cope with rising ocean temperatures, temperate marine assemblages are facing major reorganization. Many benthic species have a brief but critical period dispersing through the plankton, when they are particularly susceptible to variations in temperature. Impacts of rising temperatures can thus ripple through the population with community-wide consequences. However, responses are highly species-specific, making it difficult to discern assemblage-wide patterns in the life histories of different fish species. Here, we evaluate the responses to temperature in the early life histories of several fish species using otolith reconstructive techniques. We also assess the consequences of future warming scenarios to this assemblage. We sampled recent settlers of nine common species across a temperature gradient in the Mediterranean Sea and obtained environmental data for each individual. Using otolith microstructure, we measured early life traits including pelagic larval duration (PLD), growth rate, settlement size, hatching and settlement dates. We used a GLM framework to examine how environmental variables influenced early life-history parameters. We show that increasing temperature results in considerable reduction in the dispersal potential of temperate fish. We find a nearly universal, assemblage-wide decline in pelagic larval duration (PLD) of between 10% and 25%. This was because, with increasing temperature, larvae grew quicker to their settlement size. Settlement size itself was less affected by temperature and appears to be an ontogenetically fixed process. Given current estimates of ocean warming, there could be an assemblage-wide reduction in larval dispersal of up to 50 km across the Mediterranean, reducing connectivity and potentially isolating populations as waters warm.

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.

Wave exposure reduces herbivory in post-disturbed reefs by filtering species composition, abundance and behaviour of key fish herbivores.

Harsh environmental conditions limit how species use the landscape, strongly influencing the way assemblages are distributed. In the wake of repeated coral bleaching mortalities in Lakshadweep, we examined how wave exposure influences herbivory  in exposed and sheltered reefs. We used a combination of i. field observations of fish herbivore composition, abundance and activity across 6 exposed and 6 sheltered reefs; ii. experimental manipulations in a subset of these reefs (herbivore exclosures); and iii. opportunistic observations of fish recruitment, to determine how exposure influences herbivore biomass and herbivory. Species richness, biomass, abundance, total bite rates and species-specific per capita bite rates were lower in exposed compared to sheltered reefs, linked to strong environmental filtering of species composition, abundance and behaviour. For some critical species, this environmental filtering begins with differential recruitment and post-recruitment processes between exposures. Bite rates at sheltered sites were dominated by just a few species, most being laterally compressed surgeonfish that may find it difficult accessing or surviving in wave-battered shallow reefs. Exclosure experiments confirmed  that exposed reefs  were less controlled by herbivores than sheltered reefs. In post-disturbed reefs like Lakshadweep, environmental gradients appear to be key mediators of critical functions like herbivory by determining species composition, abundance and behaviour.

Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.

Without drastic efforts to reduce carbon emissions and mitigate globalized stressors, tropical coral reefs are in jeopardy. Strategic conservation and management requires identification of the environmental and socioeconomic factors driving the persistence of scleractinian coral assemblages-the foundation species of coral reef ecosystems. Here, we compiled coral abundance data from 2,584 Indo-Pacific reefs to evaluate the influence of 21 climate, social and environmental drivers on the ecology of reef coral assemblages. Higher abundances of framework-building corals were typically associated with: weaker thermal disturbances and longer intervals for potential recovery; slower human population growth; reduced access by human settlements and markets; and less nearby agriculture. We therefore propose a framework of three management strategies (protect, recover or transform) by considering: (1) if reefs were above or below a proposed threshold of >10% cover of the coral taxa important for structural complexity and carbonate production; and (2) reef exposure to severe thermal stress during the 2014-2017 global coral bleaching event. Our findings can guide urgent management efforts for coral reefs, by identifying key threats across multiple scales and strategic policy priorities that might sustain a network of functioning reefs in the Indo-Pacific to avoid ecosystem collapse.

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.

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.

Alternative reproductive tactics and inverse size-assortment in a high-density fish spawning aggregation.

BACKGROUND: At high densities, terrestrial and marine species often employ alternate reproductive tactics (ARTs) to maximize reproductive benefits. We describe ARTs in a high-density and unfished spawning aggregation of the squaretail grouper (Plectropomus areolatus) in Lakshadweep, India. RESULTS: As previously reported for this species, territorial males engage in pair-courtship, which is associated with a pair-spawning tactic. Here, we document a previously unreported school-courtship tactic; where territorial males court multiple females in mid-water schools, which appears to culminate in a unique 'school-spawning' tactic. Courtship tactics were conditional on body size, local mate density and habitat, likely associated with changing trade-offs between potential mating opportunities and intra-sexual competition. Counter-intuitively, the aggregation showed a habitat-specific inverse size-assortment: large males courted small females on the reef slope while small males courted equal-sized or larger females on the shelf. These patterns remained stable across two years of observation at high, unfished densities. CONCLUSIONS: These unique density-dependent behaviours may disappear from this aggregation as overall densities decline due to increasing commercial fishing pressure, with potentially large consequences for demographics and fitness.

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.

Seagrass Herbivory Levels Sustain Site-Fidelity in a Remnant Dugong Population.

Herds of dugong, a largely tropical marine megaherbivore, are known to undertake long-distance movements, sequentially overgrazing seagrass meadows in their path. Given their drastic declines in many regions, it is unclear whether at lower densities, their grazing is less intense, reducing their need to travel between meadows. We studied the effect of the feeding behaviour of a small dugong population in the Andaman and Nicobar archipelago, India to understand how small isolated populations graze seagrasses. In the seven years of our observation, all recorded dugongs travelled either solitarily or in pairs, and their use of seagrasses was limited to 8 meadows, some of which were persistently grazed. These meadows were relatively large, contiguous and dominated by short-lived seagrasses species. Dugongs consumed approximately 15% of meadow primary production, but there was a large variation (3-40% of total meadow production) in consumption patterns between meadows. The impact of herbivory was relatively high, with shoot densities c. 50% higher inside herbivore exclosures than in areas exposed to repeated grazing. Our results indicate that dugongs in the study area repeatedly graze the same meadows probably because the proportion of primary production consumed reduces shoot density to levels that are still above values that can trigger meadow abandonment. This ability of seagrasses to cope perhaps explains the long-term site fidelity shown by individual dugongs in these meadows. The fact that seagrass meadows in the archipelago are able to support dugong foraging requirements allows us to clearly identify locations where this remnant population persists, and where urgent management efforts can be directed.

Fish community reassembly after a coral mass mortality: higher trophic groups are subject to increased rates of extinction.

Since Gleason and Clements, our understanding of community dynamics has been influenced by theories emphasising either dispersal or niche assembly as central to community structuring. Determining the relative importance of these processes in structuring real-world communities remains a challenge. We tracked reef fish community reassembly after a catastrophic coral mortality in a relatively unfished archipelago. We revisited the stochastic model underlying MacArthur and Wilson's Island Biogeography Theory, with a simple extension to account for trophic identity. Colonisation and extinction rates calculated from decadal presence-absence data based on (1) species neutrality, (2) trophic identity and (3) site-specificity were used to model post-disturbance reassembly, and compared with empirical observations. Results indicate that species neutrality holds within trophic guilds, and trophic identity significantly increases overall model performance. Strikingly, extinction rates increased clearly with trophic position, indicating that fish communities may be inherently susceptible to trophic downgrading even without targeted fishing of top predators.

Positive interactions between irrawaddy dolphins and artisanal fishers in the Chilika Lagoon of eastern India are driven by ecology, socioeconomics, and culture.

In human-dominated landscapes, interactions and perceptions towards wildlife are influenced by multidimensional drivers. Understanding these drivers could prove useful for wildlife conservation. We surveyed the attitudes and perceptions of fishers towards threatened Irrawaddy dolphins (Orcaella brevirostris) at Chilika Lagoon India. To validate the drivers of fisher perceptions, we : (1) observed dolphin foraging behavior at stake nets, and (2) compared catch per unit effort (CPUE) and catch income of fishers from stake nets in the presence and absence of foraging dolphins. We found that fishers were mostly positive towards dolphins, believing that dolphins augmented their fish catch and using culture to express their perceptions. Foraging dolphins were observed spending half their time at stake nets and were associated with significantly higher catch income and CPUE of mullet (Liza sp.), a locally preferred food fish species. Wildlife conservation efforts should use the multidimensional drivers of human-wildlife interactions to involve local stakeholders in management.

Long-term occupancy trends in a data-poor dugong population in the Andaman and Nicobar archipelago.

Prioritizing efforts for conserving rare and threatened species with limited past data and lacking population estimates is predicated on robust assessments of their occupancy rates. This is particularly challenging for elusive, long-lived and wide-ranging marine mammals. In this paper we estimate trends in long-term (over 50 years) occupancy, persistence and extinction of a vulnerable and data-poor dugong (Dugong dugon) population across multiple seagrass meadows in the Andaman and Nicobar archipelago (India). For this we use hierarchical Bayesian dynamic occupancy models accounting for false negatives (detection probability<1), persistence and extinction, to two datasets: a) fragmentary long-term occurrence records from multiple sources (1959-2004, n = 40 locations), and b) systematic detection/non-detection data from current surveys (2010-2012, n = 57). Dugong occupancy across the archipelago declined by 60% (from 0.45 to 0.18) over the last 20 years and present distribution was largely restricted to sheltered bays and channels with seagrass meadows dominated by Halophila and Halodule sp. Dugongs were not found in patchy meadows with low seagrass cover. In general, seagrass habitat availability was not limiting for dugong occupancy, suggesting that anthropogenic factors such as entanglement in gillnets and direct hunting may have led to local extinction of dugongs from locations where extensive seagrass meadows still thrive. Effective management of these remnant dugong populations will require a multi-pronged approach, involving 1) protection of areas where dugongs still persist, 2) monitoring of seagrass habitats that dugongs could recolonize, 3) reducing gillnet use in areas used by dugongs, and 4) engaging with indigenous/settler communities to reduce impacts of hunting.