Impact of human disturbance on biogeochemical fluxes in tropical seascapes.

Tropical seascapes rely on the feedback relationships among mangrove forests, seagrass meadows, and coral reefs, as they mutually facilitate and enhance each other's functionality. Biogeochemical fluxes link tropical coastal habitats by exchanging material flows and energy through various natural processes that determine the conditions for life and ecosystem functioning. However, little is known about the seascape-scale implications of anthropogenic disruptions to these linkages. Despite the limited number of integrated empirical studies available (with only 11 out of 81 selected studies focusing on the integrated dynamics of mangroves, seagrass, and corals), this review emphasizes the importance of biogeochemical fluxes for ecosystem connectivity in tropical seascapes. It identifies four primary anthropogenic influences that can disturb these fluxes-nutrient enrichment, chemical pollution, microbial pollution, and solid waste accumulation-resulting in eutrophication, increased disease incidence, toxicity, and disruptions to water carbonate chemistry. This review also highlights significant knowledge gaps in our understanding of biogeochemical fluxes and ecosystem responses to perturbations in tropical seascapes. Addressing these knowledge gaps is crucial for developing practical strategies to conserve and manage connected seascapes effectively. Integrated research is needed to shed light on the complex interactions and feedback mechanisms within these ecosystems, providing valuable insights for conservation and management practices.

Addition of iron does not ameliorate sulfide toxicity by sargassum influx to mangroves but dampens methane and nitrous oxide emissions.

Sargassum spp. strandings in the tropical Atlantic harm local ecosystems due to toxic sulfide levels. We conducted a mesocosm experiment to test the efficacy of iron(III) (hydr)oxides in (a) mitigating sulfide toxicity in mangroves resulting from Sargassum and (b) reducing potentially enhanced greenhouse gas emissions. Our results show that iron addition failed to prevent mangrove mortality caused by highly toxic sulfide concentrations, which reached up to 15,000 µmol l-1 in 14 days; timely removal may potentially prevent mangrove death. Sargassum-impacted mesocosms significantly increased methane, nitrous oxide, and carbon dioxide emissions, producing approximately 1 g CO2-equivalents m-2 h-1 during daylight hours, thereby shifting mangroves from sinks to sources of greenhouse gasses. However, iron addition decreased methane emissions by 62 % and nitrous oxide emissions by 57 %. This research reveals that Sargassum strandings have multiple adverse effects related to chemical and ecological dynamics in mangrove ecosystems, including greenhouse gas emissions.

Herbivore effects increase with latitude across the extent of a foundational seagrass.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

High temperature and eutrophication alter biomass allocation of black mangrove (Avicennia germinans L.) seedlings.

Mangrove restoration is underway along tropical coastlines to combat their rapid worldwide decline. However, restoration success is limited due to local drivers such as eutrophication, and global drivers such as climate change, yet their interactions remain unclear. We conducted a mesocosm experiment to assess the impact of increased nutrients and temperature on the photosynthetic efficiency and development of black mangrove seedlings. Seedlings exposed to high temperature and eutrophication showed reduced root growth and disproportionally long stems, with lower net assimilation rates. This architectonical imbalance between root and stem growth may increase susceptibility to physical disturbances and dislodgement. Notably, none of the experimental seedlings displayed signs of photophysiological stress, and those exposed to increased nutrients and temperature exhibited robust photosynthetic performance. The disbalance in biomass allocation highlights the importance of considering local nutrient status and hydrodynamic conditions in restoration projects, ensuring the effective anchorage of mangrove seedlings and restoration success under a warming climate.

Habitat complexity drives food web structure along a dynamic mangrove coast.

Structurally complex habitats, such as mangrove forests, allow for rich assemblages of species that benefit from the provided space, volume and substrate. Changes in habitat complexity can affect species abundance, diversity and resilience. In this study, we explored the effects of habitat complexity on food web networks in four developmental stages of mangrove forests with differing structural complexities: climax > degrading > colonizing > bare, by analyzing food web structure, stable isotopes and habitat complexity. We found that food webs became gradually more biodiverse (species richness: +119 %), complex (link density: +39 %), and robust (connectance: -35 %) in climax versus bare stages with increasing complexity of the mangrove forest (i.e., number of trees, leaf cover, and pneumatophore densities). This study shows that habitat complexity drives food web network structure in dynamic mangrove forests. We recommend restoration practitioners to use this food web network approach to quantify habitat restoration successes complementary to traditional biodiversity metrics.

Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore.

Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.

Demographic changes in Pleistocene sea turtles were driven by past sea level fluctuations affecting feeding habitat availability.

Pleistocene environmental changes are generally assumed to have dramatically affected species' demography via changes in habitat availability, but this is challenging to investigate due to our limited knowledge of how Pleistocene ecosystems changed through time. Here, we tracked changes in shallow marine habitat availability resulting from Pleistocene sea level fluctuations throughout the last glacial cycle (120-14 thousand years ago; kya) and assessed correlations with past changes in genetic diversity inferred from genome-wide SNPs, obtained via ddRAD sequencing, in Caribbean hawksbill turtles, which feed in coral reefs commonly found in shallow tropical waters. We found sea level regression resulted in an average 75% reduction in shallow marine habitat availability during the last glacial cycle. Changes in shallow marine habitat availability correlated strongly with past changes in hawksbill turtle genetic diversity, which gradually declined to ~1/4th of present-day levels during the Last Glacial Maximum (LGM; 26-19 kya). Shallow marine habitat availability and genetic diversity rapidly increased after the LGM, signifying a population expansion in response to warming environmental conditions. Our results suggest a positive correlation between Pleistocene environmental changes, habitat availability and species' demography, and that demographic changes in hawksbill turtles were potentially driven by feeding habitat availability. However, we also identified challenges associated with disentangling the potential environmental drivers of past demographic changes, which highlights the need for integrative approaches. Our conclusions underline the role of habitat availability on species' demography and biodiversity, and that the consequences of ongoing habitat loss should not be underestimated.

The population genomic structure of green turtles (Chelonia mydas) suggests a warm-water corridor for tropical marine fauna between the Atlantic and Indian oceans during the last interglacial.

The occasional westward transport of warm water of the Agulhas Current, "Agulhas leakage", around southern Africa has been suggested to facilitate tropical marine connectivity between the Atlantic and Indian oceans, but the "Agulhas leakage" hypothesis does not explain the signatures of eastward gene flow observed in many tropical marine fauna. We investigated an alternative hypothesis: the establishment of a warm-water corridor during comparatively warm interglacial periods. The "warm-water corridor" hypothesis was investigated by studying the population genomic structure of Atlantic and Southwest Indian Ocean green turtles (N = 27) using 12,035 genome-wide single nucleotide polymorphisms (SNPs) obtained via ddRAD sequencing. Model-based and multivariate clustering suggested a hierarchical population structure with two main Atlantic and Southwest Indian Ocean clusters, and a Caribbean and East Atlantic sub-cluster nested within the Atlantic cluster. Coalescent-based model selection supported a model where Southwest Indian Ocean and Caribbean populations diverged from the East Atlantic population during the transition from the last interglacial period (130-115 thousand years ago; kya) to the last glacial period (115-90 kya). The onset of the last glaciation appeared to isolate Atlantic and Southwest Indian Ocean green turtles into three refugia, which subsequently came into secondary contact in the Caribbean and Southwest Indian Ocean when global temperatures increased after the Last Glacial Maximum. Our findings support the establishment of a warm-water corridor facilitating tropical marine connectivity between the Atlantic and Southwest Indian Ocean during warm interglacials.

Mimicry of emergent traits amplifies coastal restoration success.

Restoration is becoming a vital tool to counteract coastal ecosystem degradation. Modifying transplant designs of habitat-forming organisms from dispersed to clumped can amplify coastal restoration yields as it generates self-facilitation from emergent traits, i.e. traits not expressed by individuals or small clones, but that emerge in clumped individuals or large clones. Here, we advance restoration science by mimicking key emergent traits that locally suppress physical stress using biodegradable establishment structures. Experiments across (sub)tropical and temperate seagrass and salt marsh systems demonstrate greatly enhanced yields when individuals are transplanted within structures mimicking emergent traits that suppress waves or sediment mobility. Specifically, belowground mimics of dense root mats most facilitate seagrasses via sediment stabilization, while mimics of aboveground plant structures most facilitate marsh grasses by reducing stem movement. Mimicking key emergent traits may allow upscaling of restoration in many ecosystems that depend on self-facilitation for persistence, by constraining biological material requirements and implementation costs.

Population recovery changes population composition at a major southern Caribbean juvenile developmental habitat for the green turtle, Chelonia mydas.

Understanding the population composition and dynamics of migratory megafauna at key developmental habitats is critical for conservation and management. The present study investigated whether differential recovery of Caribbean green turtle (Chelonia mydas) rookeries influenced population composition at a major juvenile feeding ground in the southern Caribbean (Lac Bay, Bonaire, Caribbean Netherlands) using genetic and demographic analyses. Genetic divergence indicated a strong temporal shift in population composition between 2006-2007 and 2015-2016 (ϕST = 0.101, P < 0.001). Juvenile recruitment (<75.0 cm straight carapace length; SCL) from the north-western Caribbean increased from 12% to 38% while recruitment from the eastern Caribbean region decreased from 46% to 20% between 2006-2007 and 2015-2016. Furthermore, the product of the population growth rate and adult female abundance was a significant predictor for population composition in 2015-2016. Our results may reflect early warning signals of declining reproductive output at eastern Caribbean rookeries, potential displacement effects of smaller rookeries by larger rookeries, and advocate for genetic monitoring as a useful method for monitoring trends in juvenile megafauna. Furthermore, these findings underline the need for adequate conservation of juvenile developmental habitats and a deeper understanding of the interactions between megafaunal population dynamics in different habitats.

Optimism for mitigation of climate warming impacts for sea turtles through nest shading and relocation.

Increasing incubation temperatures may threaten the viability of sea turtle populations. We explored opportunities for decreasing incubation temperatures at a Caribbean rookery with extreme female-biased hatchling production. To investigate the effect of artificial shading, temperatures were measured under simple materials (white sheet, white sand, palm leaves). To test natural drivers of incubation temperature, temperatures were measured at average nest depths with shading on two beaches. Results from a pilot experiment suggest the most effective material was palm leaves. Shading decreased temperatures by a mean of 0.60 °C (SE = 0.10 °C, N = 20). Variation between beaches averaged 1.88 °C (SE = 0.13 °C, N = 20). We used long-term rookery data combined with experimental data to estimate the effect on sex ratio: relocation and shading could shift ratios from current ranges (97-100% female) to 60-90% female. A conservation mitigation matrix summarises our evidence that artificial shading and nest relocation are effective, low-cost, low-technology conservation strategies to mitigate impacts of climate warming for sea turtles.

Foundation species enhance food web complexity through non-trophic facilitation.

Food webs are an integral part of every ecosystem on the planet, yet understanding the mechanisms shaping these complex networks remains a major challenge. Recently, several studies suggested that non-trophic species interactions such as habitat modification and mutualisms can be important determinants of food web structure. However, it remains unclear whether these findings generalize across ecosystems, and whether non-trophic interactions affect food webs randomly, or affect specific trophic levels or functional groups. Here, we combine analyses of 58 food webs from seven terrestrial, freshwater and coastal systems to test (1) the general hypothesis that non-trophic facilitation by habitat-forming foundation species enhances food web complexity, and (2) whether these enhancements have either random or targeted effects on particular trophic levels, functional groups, and linkages throughout the food web. Our empirical results demonstrate that foundation species consistently enhance food web complexity in all seven ecosystems. Further analyses reveal that 15 out of 19 food web properties can be well-approximated by assuming that foundation species randomly facilitate species throughout the trophic network. However, basal species are less strongly, and carnivores are more strongly facilitated in foundation species' food webs than predicted based on random facilitation, resulting in a higher mean trophic level and a longer average chain length. Overall, we conclude that foundation species strongly enhance food web complexity through non-trophic facilitation of species across the entire trophic network. We therefore suggest that the structure and stability of food webs often depends critically on non-trophic facilitation by foundation species.

Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance.

Seagrass ecosystems are inherently dynamic, responding to environmental change across a range of scales. Habitat requirements of seagrass are well defined, but less is known about their ability to resist disturbance. Specific means of recovery after loss are particularly difficult to quantify. Here we assess the resistance and recovery capacity of 12 seagrass genera. We document four classic trajectories of degradation and recovery for seagrass ecosystems, illustrated with examples from around the world. Recovery can be rapid once conditions improve, but seagrass absence at landscape scales may persist for many decades, perpetuated by feedbacks and/or lack of seed or plant propagules to initiate recovery. It can be difficult to distinguish between slow recovery, recalcitrant degradation, and the need for a window of opportunity to trigger recovery. We propose a framework synthesizing how the spatial and temporal scales of both disturbance and seagrass response affect ecosystem trajectory and hence resilience.

Seagrass leaf element content: A global overview.

Knowledge on the role of seagrass leaf elements and in particular micronutrients and their ranges is limited. We present a global database, consisting of 1126 unique leaf values for ten elements, obtained from literature and unpublished data, spanning 25 different seagrass species from 28 countries. The overall order of average element values in seagrass leaves was Na>K>Ca>Mg>S>Fe>Al>Si>Mn>Zn. Although we observed differences in leaf element content between seagrass families, high intraspecific variation indicated that leaf element content was more strongly determined by environmental factors than by evolutionary history. Early successional species had high leaf Al and Fe content. In addition, seagrass leaf element content also showed correlations with macronutrients (N and P), indicating that productivity also depends on other elements. Expected genomes of additional seagrass species in combination with experiments manipulating (micro)nutrients and environmental drivers might enable us to unravel the importance of various elements to sustain productive and flourishing meadows.

How habitat-modifying organisms structure the food web of two coastal ecosystems.

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.

Drought, Mutualism Breakdown, and Landscape-Scale Degradation of Seagrass Beds.

In many marine ecosystems, biodiversity critically depends on foundation species such as corals and seagrasses that engage in mutualistic interactions [1-3]. Concerns grow that environmental disruption of marine mutualisms exacerbates ecosystem degradation, with breakdown of the obligate coral mutualism ("coral bleaching") being an iconic example [2, 4, 5]. However, as these mutualisms are mostly facultative rather than obligate, it remains unclear whether mutualism breakdown is a common risk in marine ecosystems, and thus a potential accelerator of ecosystem degradation. Here, we provide evidence that drought triggered landscape-scale seagrass degradation and show the consequent failure of a facultative mutualistic feedback between seagrass and sulfide-consuming lucinid bivalves that in turn appeared to exacerbate the observed collapse. Local climate and remote sensing analyses revealed seagrass collapse after a summer with intense low-tide drought stress. Potential analysis-a novel approach to detect feedback-mediated state shifts-revealed two attractors (healthy and degraded states) during the collapse, suggesting that the drought disrupted internal feedbacks to cause abrupt, patch-wise degradation. Field measurements comparing degraded patches that were healthy before the collapse with patches that remained healthy demonstrated that bivalves declined dramatically in degrading patches with associated high sediment sulfide concentrations, confirming the breakdown of the mutualistic seagrass-lucinid feedback. Our findings indicate that drought triggered mutualism breakdown, resulting in toxic sulfide concentrations that aggravated seagrass degradation. We conclude that external disturbances can cause sudden breakdown of facultative marine mutualistic feedbacks. As this may amplify ecosystem degradation, we suggest including mutualisms in marine conservation and restoration approaches.

Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas.

Marine protected areas (MPAs) are key tools for combatting the global overexploitation of endangered species. The prevailing paradigm is that MPAs are beneficial in helping to restore ecosystems to more 'natural' conditions. However, MPAs may have unintended negative effects when increasing densities of protected species exert destructive effects on their habitat. Here, we report on severe seagrass degradation in a decade-old MPA where hyper-abundant green turtles adopted a previously undescribed below-ground foraging strategy. By digging for and consuming rhizomes and roots, turtles create abundant bare gaps, thereby enhancing erosion and reducing seagrass regrowth. A fully parametrized model reveals that the ecosystem is approaching a tipping point, where consumption overwhelms regrowth, which could potentially lead to complete collapse of the seagrass habitat. Seagrass recovery will not ensue unless turtle density is reduced to nearly zero, eliminating the MPA's value as a turtle reserve. Our results reveal an unrecognized, yet imminent threat to MPAs, as sea turtle densities are increasing at major nesting sites and the decline of seagrass habitat forces turtles to concentrate on the remaining meadows inside reserves. This emphasizes the need for policy and management approaches that consider the interactions of protected species with their habitat.

Low-canopy seagrass beds still provide important coastal protection services.

One of the most frequently quoted ecosystem services of seagrass meadows is their value for coastal protection. Many studies emphasize the role of above-ground shoots in attenuating waves, enhancing sedimentation and preventing erosion. This raises the question if short-leaved, low density (grazed) seagrass meadows with most of their biomass in belowground tissues can also stabilize sediments. We examined this by combining manipulative field experiments and wave measurements along a typical tropical reef flat where green turtles intensively graze upon the seagrass canopy. We experimentally manipulated wave energy and grazing intensity along a transect perpendicular to the beach, and compared sediment bed level change between vegetated and experimentally created bare plots at three distances from the beach. Our experiments showed that i) even the short-leaved, low-biomass and heavily-grazed seagrass vegetation reduced wave-induced sediment erosion up to threefold, and ii) that erosion was a function of location along the vegetated reef flat. Where other studies stress the importance of the seagrass canopy for shoreline protection, our study on open, low-biomass and heavily grazed seagrass beds strongly suggests that belowground biomass also has a major effect on the immobilization of sediment. These results imply that, compared to shallow unvegetated nearshore reef flats, the presence of a short, low-biomass seagrass meadow maintains a higher bed level, attenuating waves before reaching the beach and hence lowering beach erosion rates. We propose that the sole use of aboveground biomass as a proxy for valuing coastal protection services should be reconsidered.