Integrating larval connectivity into the marine conservation decision-making process across spatial scales.

Larval dispersal connectivity is typically integrated into spatial conservation decisions at regional or national scales, but implementing agencies struggle with translating these methods to local scales. We used larval dispersal connectivity at regional (hundreds of kilometers) and local (tens of kilometers) scales to aid in design of networks of no-take reserves in Southeast Sulawesi, Indonesia. We used Marxan with Connectivity informed by biophysical larval dispersal models and remotely sensed coral reef habitat data to design marine reserve networks for 4 commercially important reef species across the region. We complemented regional spatial prioritization with decision trees that combined network-based connectivity metrics and habitat quality to design reserve boundaries locally. Decision trees were used in consensus-based workshops with stakeholders to qualitatively assess site desirability, and Marxan was used to identify areas for subsequent network expansion. Priority areas for protection and expected benefits differed among species, with little overlap in reserve network solutions. Because reef quality varied considerably across reefs, we suggest reef degradation must inform the interpretation of larval dispersal patterns and the conservation benefits achievable from protecting reefs. Our methods can be readily applied by conservation practitioners, in this region and elsewhere, to integrate connectivity data across multiple spatial scales.

Integración de la conectividad larval al proceso de toma de decisiones en la conservación marina en escalas espaciales Resumen Comúnmente se integra la conectividad de la dispersión larval a las decisiones de conservación espacial a escalas regionales o nacionales, pero las agencias de implementación luchan con la transferencia de estos métodos a las escalas locales. Usamos la conectividad de la dispersión larval a escalas regionales (cientos de kilómetros) y locales (decenas de kilómetros) para ayudar en el diseño de redes de reservas con protección total en Sulawesi Sudoriental, Indonesia. Usamos Marxan con la conectividad guiada por los modelos biofísicos de dispersión larval y detectamos a distancia los datos de hábitat de los arrecifes de coral para diseñar redes de reservas marinas para cuatro especies de importancia comercial en la región. Complementamos la priorización espacial regional con árboles de decisión que combinaron medidas de conectividad basadas en las redes y la calidad del hábitat para diseñar localmente los límites de la reserva. Usamos los árboles de decisión con los actores en talleres basados en el consenso para evaluar cualitativamente la conveniencia del sitio. También usamos Marxan para identificar áreas para la expansión subsecuente de la red. Las áreas prioritarias para la protección y los beneficios esperados difirieron entre especies, con un traslape reducido en las soluciones de la red de reservas. Ya que la calidad del arrecife varió considerablemente entre los arrecifes, sugerimos que la degradación de estos debe orientar la interpretación de los patrones de dispersión larval y los beneficios de conservación alcanzables con la protección de los arrecifes. Los practicantes de la conservación pueden aplicar nuestros métodos inmediatamente, en esta región o en cualquier otra, para integrar los datos de conectividad en varias escalas espaciales.

Comparing spatial conservation prioritization methods with site- versus spatial dependency-based connectivity.

Larval dispersal is an important component of marine reserve networks. Two conceptually different approaches to incorporate dispersal connectivity into spatial planning of these networks exist, and it is an open question as to when either is most appropriate. Candidate reserve sites can be selected individually based on local properties of connectivity or on a spatial dependency-based approach of selecting clusters of strongly connected habitat patches. The first acts on individual sites, whereas the second acts on linked pairs of sites. We used a combination of larval dispersal simulations representing different seascapes and case studies of biophysical larval dispersal models in the Coral Triangle region and the province of Southeast Sulawesi, Indonesia, to compare the performance of these 2 methods in the spatial planning software Marxan. We explored the reserve design performance implications of different dispersal distances and patterns based on the equilibrium settlement of larvae in protected and unprotected areas. We further assessed different assumptions about metapopulation contributions from unprotected areas, including the case of 100% depletion and more moderate scenarios. The spatial dependency method was suitable when dispersal was limited, a high proportion of the area of interest was substantially degraded, or the target amount of habitat protected was low. Conversely, when subpopulations were well connected, the 100% depletion was relaxed, or more habitat was protected, protecting individual sites with high scores in metrics of connectivity was a better strategy. Spatial dependency methods generally produced more spatially clustered solutions with more benefits inside than outside reserves compared with site-based methods. Therefore, spatial dependency methods potentially provide better results for ecological persistence objectives over enhancing fisheries objectives, and vice versa. Different spatial prioritization methods of using connectivity are appropriate for different contexts, depending on dispersal characteristics, unprotected area contributions, habitat protection targets, and specific management objectives. Comparación entre los métodos de priorización de la conservación espacial con sitio y la conectividad espacial basada en la dependencia.

La dispersión larval es un componente importante de las redes de reservas marinas. Existen dos estrategias conceptualmente distintas para incorporar la conectividad de la dispersión en la planeación espacial de estas redes y es una pregunta abierta cuándo alguna de las dos es la más apropiada. Los sitios candidatos a reserva pueden ser seleccionados individualmente con base en las propiedades locales de la conectividad o en la estrategia espacial basada en la dependencia que consiste en seleccionar grupos de fragmentos de hábitat con un vínculo fuerte. La primera estrategia actúa sobre sitios individuales, mientras que la segunda actúa sobre pares de sitios vinculados. Usamos una combinación de simulaciones de dispersión larval que representaban a diferentes paisajes marinos y estudios de caso de modelos biofísicos de dispersión larval en la región del Triángulo de Coral y en la provincia de Sulawesi Sudoriental, Indonesia, para comparar el desempeño de estos dos métodos en el software de planeación espacial Marxan. Exploramos las implicaciones del desempeño del diseño de la reserva de diferentes distancias y patrones de dispersión basados en el establecimiento del equilibrio de larvas en las áreas protegidas y sin protección. Además, analizamos las suposiciones sobre las contribuciones metapoblacionales de las áreas sin protección, incluyendo el caso de la reducción al 100% y escenarios más moderados. El método de la dependencia espacial fue adecuado cuando la dispersión estuvo limitada, una proporción elevada del área de interés estaba sustancialmente degradada o era baja la cantidad meta de hábitat protegido. Al contrario, cuando las subpoblaciones estaban bien conectadas, la reducción al 100% estuvo relajada, o si una mayor parte del hábitat estaba protegido, la protección de los sitios individuales con altos puntajes en las medidas de conectividad fue una mejor estrategia. Los métodos de dependencia espacial generalmente produjeron soluciones con una agrupación más espacial y con más beneficios dentro que fuera de las reservas en comparación con los métodos basados sitios. Por lo tanto, los métodos de dependencia espacial tienen el potencial de proporcionar mejores resultados para los objetivos de persistencia ecológica por encima de los objetivos de mejora de las pesquerías, y viceversa. Los diferentes métodos de priorización espacial que usan la conectividad son apropiados para contextos diferentes, dependiendo de las características de dispersión, las contribuciones del área sin protección, las metas de protección del hábitat y los objetivos específicos del manejo.

Scale dependence of coral reef oases and their environmental correlates.

Identifying relatively intact areas within ecosystems and determining the conditions favoring their existence is necessary for effective management in the context of widespread environmental degradation. In this study, we used 3766 surveys of randomly selected sites in the United States and U.S. Territories to identify the correlates of sites categorized as "oases" (defined as sites with relatively high total coral cover). We used occupancy models to evaluate the influence of 10 environmental predictors on the probability that an area (21.2-km2 cell) would harbor coral oases defined at four spatial extents: cross-basin, basin, region, and subregion. Across all four spatial extents, oases were more likely to occur in habitats with high light attenuation. The influence of the other environmental predictors on the probability of oasis occurrence were less consistent and varied with the scale of observation. Oases were most likely in areas of low human population density, but this effect was evident only at the cross-basin and subregional extents. At the regional and subregional extents oases were more likely where sea-surface temperature was more variable, whereas at the larger spatial extents the opposite was true. By identifying the correlates of oasis occurrence, the model can inform the prioritization of reef areas for management. Areas with biophysical conditions that confer corals with physiological resilience, as well as limited human impacts, likely support coral reef oases across spatial extents. Our approach is widely applicable to the development of conservation strategies to protect biodiversity and ecosystems in an era of magnified human disturbance.

Planning for resilience: Incorporating scenario and model uncertainty and trade-offs when prioritizing management of climate refugia.

Climate change has become the greatest threat to the world's ecosystems. Locating and managing areas that contribute to the survival of key species under climate change is critical for the persistence of ecosystems in the future. Here, we identify 'Climate Priority' sites as coral reefs exposed to relatively low levels of climate stress that will be more likely to persist in the future. We present the first analysis of uncertainty in climate change scenarios and models, along with multiple objectives, in a marine spatial planning exercise and offer a comprehensive approach to incorporating uncertainty and trade-offs in any ecosystem. We first described each site using environmental characteristics that are associated with a higher chance of persistence (larval connectivity, hurricane influence, and acute and chronic temperature conditions in the past and the future). Future temperature increases were assessed using downscaled data under four different climate scenarios (SSP1 2.6, SSP2 4.5, SSP3 7.0 and SSP5 8.5) and 57 model runs. We then prioritized sites for intervention (conservation, improved management or restoration) using robust decision-making approaches that select sites that will have a benign climate under most climate scenarios and models. The modelling work is novel because it solves two important issues. (1) It considers trade-offs between multiple planning objectives explicitly through Pareto analyses and (2) It makes use of all the uncertainty around future climate change. Priority intervention sites identified by the model were verified and refined through local stakeholder engagement including assessments of local threats, ecological conditions and government priorities. The workflow is presented for the Insular Caribbean and Florida, and at the national level for Cuba, Jamaica, Dominican Republic and Haiti. Our approach allows managers to consider uncertainty and multiple objectives for climate-smart spatial management in coral reefs or any ecosystem across the globe.

Classifying fishing behavioral diversity using high-frequency movement data.

Effective management of social-ecological systems (SESs) requires an understanding of human behavior. In many SESs, there are hundreds of agents or more interacting with governance and regulatory institutions, driving management outcomes through collective behavior. Agents in these systems often display consistent behavioral characteristics over time that can help reduce the dimensionality of SES data by enabling the assignment of types. Typologies of resource-user behavior both enrich our knowledge of user cultures and provide critical information for management. Here, we develop a data-driven framework to identify resource-user typologies in SESs with high-dimensional data. To demonstrate policy applications, we apply the framework to a tightly coupled SES, commercial fishing. We leverage large fisheries-dependent datasets that include mandatory vessel logbooks, observer datasets, and high-resolution geospatial vessel tracking technologies. We first quantify vessel and behavioral characteristics using data that encode fishers' spatial decisions and behaviors. We then use clustering to classify these characteristics into discrete fishing behavioral types (FBTs), determining that 3 types emerge in our case study. Finally, we investigate how a series of disturbances applied selection pressure on these FBTs, causing the disproportionate loss of one group. Our framework not only provides an efficient and unbiased method for identifying FBTs in near real time, but it can also improve management outcomes by enabling ex ante investigation of the consequences of disturbances such as policy actions.

Three decades of heat stress exposure in Caribbean coral reefs: a new regional delineation to enhance conservation.

Increasing heat stress due to global climate change is causing coral reef decline, and the Caribbean has been one of the most vulnerable regions. Here, we assessed three decades (1985-2017) of heat stress exposure in the wider Caribbean at ecoregional and local scales using remote sensing. We found a high spatial and temporal variability of heat stress, emphasizing an observed increase in heat exposure over time in most ecoregions, especially from 2003 identified as a temporal change point in heat stress. A spatiotemporal analysis classified the Caribbean into eight heat-stress regions offering a new regionalization scheme based on historical heat exposure patterns. The temporal analysis confirmed the years 1998, 2005, 2010-2011, 2015 and 2017 as severe and widespread Caribbean heat-stress events and recognized a change point in 2002-2004, after which heat exposure has been frequent in most subsequent years. Major heat-stress events may be associated with El Niño Southern Oscillation (ENSO), but we highlight the relevance of the long-term increase in heat exposure in most ecoregions and in all ENSO phases. This work produced a new baseline and regionalization of heat stress in the basin that will enhance conservation and planning efforts underway.

Correction: Widespread local chronic stressors in Caribbean coastal habitats.

[This corrects the article DOI: 10.1371/journal.pone.0188564.].

Widespread local chronic stressors in Caribbean coastal habitats.

Coastal ecosystems and the livelihoods they support are threatened by stressors acting at global and local scales. Here we used the data produced by the Caribbean Coastal Marine Productivity program (CARICOMP), the longest, largest monitoring program in the wider Caribbean, to evidence local-scale (decreases in water quality) and global-scale (increases in temperature) stressors across the basin. Trend analyses showed that visibility decreased at 42% of the stations, indicating that local-scale chronic stressors are widespread. On the other hand, only 18% of the stations showed increases in water temperature that would be expected from global warming, partially reflecting the limits in detecting trends due to inherent natural variability of temperature data. Decreases in visibility were associated with increased human density. However, this link can be decoupled by environmental factors, with conditions that increase the flush of water, dampening the effects of human influence. Besides documenting environmental stressors throughout the basin, our results can be used to inform future monitoring programs, if the desire is to identify stations that provide early warning signals of anthropogenic impacts. All CARICOMP environmental data are now available, providing an invaluable baseline that can be used to strengthen research, conservation, and management of coastal ecosystems in the Caribbean basin.

Symbiodinium biogeography tracks environmental patterns rather than host genetics in a key Caribbean reef-builder, Orbicella annularis.

The physiological performance of a reef-building coral is a combined outcome of both the coral host and its algal endosymbionts, Symbiodinium While Orbicella annularis-a dominant reef-building coral in the Wider Caribbean-is known to be a flexible host in terms of the diversity of Symbiodinium types it can associate with, it is uncertain how this diversity varies across the Caribbean, and whether spatial variability in the symbiont community is related to either O. annularis genotype or environment. Here, we target the Symbiodinium-ITS2 gene to characterize and map dominant Symbiodinium hosted by O. annularis at an unprecedented spatial scale. We reveal northwest-southeast partitioning across the Caribbean, both in terms of the dominant symbiont taxa hosted and in assemblage diversity. Multivariate regression analyses incorporating a suite of environmental and genetic factors reveal that observed spatial patterns are predominantly explained by chronic thermal stress (summer temperatures) and are unrelated to host genotype. Furthermore, we were able to associate the presence of specific Symbiodinium types with local environmental drivers (for example, Symbiodinium C7 with areas experiencing cooler summers, B1j with nutrient loading and B17 with turbidity), associations that have not previously been described.

Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation.

Disturbance releases space and allows the growth of opportunistic species, excluded by the old stands, with a potential to alter community dynamics. In coral reefs, abundances of fast-growing, and disturbance-tolerant sponges are expected to increase and dominate as space becomes available following acute coral mortality events. Yet, an increase in abundance of these opportunistic species has been reported in only a few studies, suggesting certain mechanisms may be acting to regulate sponge populations. To gain insights into mechanisms of population control, we simulated the dynamics of the common reef-excavating sponge Cliona tenuis in the Caribbean using an individual-based model. An orthogonal hypothesis testing approach was used, where four candidate mechanisms-algal competition, stock-recruitment limitation, whole and partial mortality-were incorporated sequentially into the model and the results were tested against independent field observations taken over a decade in Belize, Central America. We found that releasing space after coral mortality can promote C. tenuis outbreaks, but such outbreaks can be curtailed by macroalgal competition. The asymmetrical competitive superiority of macroalgae, given by their capacity to pre-empt space and outcompete with the sponge in a size-dependant fashion, supports their capacity to steal the opportunity from other opportunists. While multiple system stages can be expected in coral reefs following intense perturbation macroalgae may prevent the growth of other space-occupiers, such as bioeroding sponges, under low grazing pressure.

Quantifying the squeezing or stretching of fisheries as they adapt to displacement by marine reserves.

The designation of no-take marine reserves involves social and economic concerns due to the resulting displacement of fishing effort, when fishing rights are removed from those who traditionally fished within an area. Displacement can influence the functioning of the fishery and success of the reserve, yet levels of displacement are seldom quantified after reserve implementation and very rarely before that. We devised a simple analytical framework based on set theory to facilitate reserve placement. Implementation of the framework requires maps of fishing grounds, fishing effort, or catch per unit effort for at least 2 years. The framework quantifies the level of conflict that a reserve designation might cause in the fishing sector due to displacement and the opportunities to offset the conflict through fisher spatial mobility (i.e., ability of fishers to fish elsewhere). We also considered how the outputs of the framework can be used to identify targeted management interventions for each fishery. We applied the method in Honduras, where the largest marine protected area in Central America is being placed, for which spatial data on fishing effort were available for 6 fisheries over 3 years. The proposed closure had a greater negative impact on the shrimp and lobster scuba fisheries, which concentrated respectively 28% and 18% of their effort inside the reserve. These fisheries could not accommodate the displacement within existing fishing grounds. Both would be forced to stretch into new fishing grounds, which are available but are of unknown quality. These stakeholders will likely require compensation to offset costly exploratory fishing or to travel to fishing grounds farther away from port.

Delineating biophysical environments of the Sunda Banda Seascape, Indonesia.

The Sunda Banda Seascape (SBS), located in the center of the Coral Triangle, is a global center of marine biodiversity and a conservation priority. We proposed the first biophysical environmental delineation of the SBS using globally available satellite remote sensing and model-assimilated data to categorize this area into unique and meaningful biophysical classes. Specifically, the SBS was partitioned into eight biophysical classes characterized by similar sea surface temperature, chlorophyll a concentration, currents, and salinity patterns. Areas within each class were expected to have similar habitat types and ecosystem functions. Our work supplemented prevailing global marine management schemes by focusing in on a regional scale with finer spatial resolution. It also provided a baseline for academic research, ecological assessments and will facilitate marine spatial planning and conservation activities in the area. In addition, the framework and methods of delineating biophysical environments we presented can be expanded throughout the whole Coral Triangle to support research and conservation activities in this important region.

Anticipative management for coral reef ecosystem services in the 21st century.

Under projections of global climate change and other stressors, significant changes in the ecology, structure and function of coral reefs are predicted. Current management strategies tend to look to the past to set goals, focusing on halting declines and restoring baseline conditions. Here, we explore a complementary approach to decision making that is based on the anticipation of future changes in ecosystem state, function and services. Reviewing the existing literature and utilizing a scenario planning approach, we explore how the structure of coral reef communities might change in the future in response to global climate change and overfishing. We incorporate uncertainties in our predictions by considering heterogeneity in reef types in relation to structural complexity and primary productivity. We examine 14 ecosystem services provided by reefs, and rate their sensitivity to a range of future scenarios and management options. Our predictions suggest that the efficacy of management is highly dependent on biophysical characteristics and reef state. Reserves are currently widely used and are predicted to remain effective for reefs with high structural complexity. However, when complexity is lost, maximizing service provision requires a broader portfolio of management approaches, including the provision of artificial complexity, coral restoration, fish aggregation devices and herbivore management. Increased use of such management tools will require capacity building and technique refinement and we therefore conclude that diversification of our management toolbox should be considered urgently to prepare for the challenges of managing reefs into the 21st century.

Redefining thermal regimes to design reserves for coral reefs in the face of climate change.

Reef managers cannot fight global warming through mitigation at local scale, but they can use information on thermal patterns to plan for reserve networks that maximize the probability of persistence of their reef system. Here we assess previous methods for the design of reserves for climate change and present a new approach to prioritize areas for conservation that leverages the most desirable properties of previous approaches. The new method moves the science of reserve design for climate change a step forwards by: (1) recognizing the role of seasonal acclimation in increasing the limits of environmental tolerance of corals and ameliorating the bleaching response; (2) using the best proxy for acclimatization currently available; (3) including information from several bleaching events, which frequency is likely to increase in the future; (4) assessing relevant variability at country scales, where most management plans are carried out. We demonstrate the method in Honduras, where a reassessment of the marine spatial plan is in progress.

Hurricane-driven patterns of clonality in an ecosystem engineer: the Caribbean coral Montastraea annularis.

K-selected species with low rates of sexual recruitment may utilise storage effects where low adult mortality allows a number of individuals to persist through time until a favourable recruitment period occurs. Alternative methods of recruitment may become increasingly important for such species if the availability of favourable conditions for sexual recruitment decline under rising anthropogenic disturbance and climate change. Here, we test the hypotheses that asexual dispersal is an integral life history strategy not only in branching corals, as previously reported, but also in a columnar, 'K-selected' coral species, and that its prevalence is driven by the frequency of severe hurricane disturbance. Montastraea annularis is a long-lived major frame-work builder of Caribbean coral reefs but its survival is threatened by the consequences of climate induced disturbance, such as bleaching, ocean acidification and increased prevalence of disease. 700 M. annularis samples from 18 reefs within the Caribbean were genotyped using six polymorphic microsatellite loci. We demonstrate that asexual reproduction occurs at varying frequency across the species-range and significantly contributes to the local abundance of M. annularis, with its contribution increasing in areas with greater hurricane frequency. We tested several competing hypotheses that might explain the observed pattern of genotypic diversity. 64% of the variation in genotypic diversity among the sites was explained by hurricane incidence and reef slope, demonstrating that large-scale disturbances combine with local habitat characteristics to shape the balance between sexual and asexual reproduction in populations of M. annularis.

Seasonal and spatial heterogeneity of recent sea surface temperature trends in the Caribbean Sea and southeast Gulf of Mexico.

Recent changes in ocean temperature have impacted marine ecosystem function globally. Nevertheless, the responses have depended upon the rate of change of temperature and the season when the changes occur, which are spatially variable. A rigorous statistical analysis of sea surface temperature observations over 25 years was used to examine spatial variability in overall and seasonal temperature trends within the wider Caribbean. The basin has experienced high spatial variability in rates of change of temperature. Most of the warming has been due to increases in summer rather than winter temperatures. However, warming was faster in winter in the Loop Current area and the south-eastern Caribbean, where the annual temperature ranges have contracted. Waters off Florida, Cuba and the Bahamas had a tendency towards cooling in winter, increasing the amplitude of annual temperature ranges. These detailed patterns can be used to elucidate ecological responses to climatic change in the region.

Macrobentos de aguas profundas en la Costa Atlántica Venezolana / Macrobenthos from deep water in the Venezuelan Atlantic Coast

En Venezuela, los estudios del bentos marino se han concentrado en zonas costeras someras. La presente investigación ha permitido conocer y cuantificar, por vez primera, la macrofauna bentánica de aguas profundas, ubicadas en la zona noreste del Delta del Orinoco. Muestras de sedimento fueron tomadas con el empleo de una draga tipo box-core (0,25m² de área) en 81 estaciones comprendidas entre los 50 y 1500m de profundidad. Se colectaron 1673 organismos pertenecientes a 11 phyla, siendo los anélidos los más abundantes (63,56 por ciento) y de ellos los poliquetos representaron el 60,73 por ciento. Siguen en abundancia los crustáceos (15,42 por ciento), nemátodos (9,26 por ciento) y bivalvos (7,11 por ciento). El 70,47 por ciento de la fauna fue retenido en el tamiz de 0,5mm de apertura de malla. En general, esta comunidad bentónica se caracterizó por una elevada diversidad biológica, pero con una muy baja densidad de organismos (20,65 ±25,87ind/estación). Los mayores valores promedio (129 individuos) se obtuvieron en la zona somera de la plataforma, entre 0-200m, mientras que los valores más bajos se registraron a grandes profundidades (0-37 individuos).