The value of ecosystem services in global marine kelp forests.

While marine kelp forests have provided valuable ecosystem services for millennia, the global ecological and economic value of those services is largely unresolved. Kelp forests are diminishing in many regions worldwide, and efforts to manage these ecosystems are hindered without accurate estimates of the value of the services that kelp forests provide to human societies. Here, we present a global estimate of the ecological and economic potential of three key ecosystem services - fisheries production, nutrient cycling, and carbon removal provided by six major forest forming kelp genera (Ecklonia, Laminaria, Lessonia, Macrocystis, Nereocystis, and Saccharina). Each of these genera creates a potential value of between $64,400 and $147,100/hectare each year. Collectively, they generate between $465 and $562 billion/year worldwide, with an average of $500 billion. These values are primarily driven by fisheries production (mean $29,900, 904 Kg/Ha/year) and nitrogen removal ($73,800, 657 Kg N/Ha/year), though kelp forests are also estimated to sequester 4.91 megatons of carbon from the atmosphere/year highlighting their potential as blue carbon systems for climate change mitigation. These findings highlight the ecological and economic value of kelp forests to society and will facilitate better informed marine management and conservation decisions.

Coupling high-resolution coral bleaching modeling with management practices to identify areas for conservation in a warming climate: Keramashoto National Park (Okinawa Prefecture, Japan).

Increases in sea-surface temperature due to global warming are a major threat to tropical and subtropical corals as exposure to high water temperatures is the primary cause of coral bleaching. To continue receiving high ecosystem services from coral reef ecosystems in the future, it is important to predict the growth conditions of corals and take appropriate countermeasures to protect them at both global and local scales. The Kerama Islands (part of the Nansei Islands, Japan) were selected as the study area. The islands have been designated as a national park and attract substantial tourism, which utilizes the coral reef ecosystem. The selected study site is significant as it is known to act as a source of coral larvae for the surrounding area. In this study, coral bleaching and mortality rates under present and +1.5 °C/+2.0 °C water temperature conditions were estimated using a 1) three-dimensional hydrodynamic model with a spatial resolution of 100 m and 2) statistical model describing the relationship between various environmental parameters and coral bleaching and mortality rates. Applying a local hydrodynamic model enabled us to obtain high-resolution spatial and temporal variations in water temperature and current speed, and these data were used to obtain statistical model data. Coral conservation sites were prioritized based on 1) projections of the spatial distribution of bleaching and mortality rates under global warming conditions and 2) locations of the main diving and conservation points, with the intention of continuing the present use and management locations. The results of this study are expected to contribute to the management of coral reef ecosystems through conservation and adaptation strategies at local scales.

Maternal inheritance of F1 hybrid morphology and colony shape in the coral genus Acropora.

BACKGROUND: The coral genus Acropora contains more than 150 species with very high morphological diversity. This high diversity may have been caused by repeated hybridization via mass spawning. However, we have little information whether hybrids are formed in these corals. Identifying morphological differences between hybrids and their parental species would provide an opportunity to find wild hybrids in the field and to understand how colony shapes of Acropora have become highly diversified throughout evolutionary history. In the two morphologically distinctive coral species Acropora florida and A. intermedia in the Indo-Pacific, their gametes show high rates of bi-directional intercrossing in vitro, and thus these two species are ideal species to investigate the morphological traits of the hybrids. METHODS: We examined morphological characters of F1 hybrids from A. florida to A. intermedia, which were produced from in vitro crossing experiments. To compare morphological differences, we grew juveniles and mature colonies of reciprocal F1 hybrids (FLOint: A. florida eggs × A. intermedia sperm, and INTflo: A. intermedia eggs × A. florida sperm) and of the parental species (purebreds of A. intermedia and A. florida). We analyzed skeletal morphology such as colony size, branch length, and branching number, and compared them with those of a putative F1 hybrid between A. florida and A. intermedia found in the field. We also confirmed the molecular phylogenetic position of F1 hybrids, parental species, and a putative F1 hybrid using the mitochondrial non-coding region. RESULTS: Our morphological analysis revealed that branching number of the F1 hybrids was intermediate relative to the parental species. Moreover, the FLOint hybrids were morphologically more closely related to the maternal species A. florida, and the INTflo hybrids were to A. intermedia. Molecular data showed that A. florida and A. intermedia were clearly divided into two clades, and that F1 hybrids grouped in the clade based on their maternal parent. A very similar pattern to the INTflo hybrids was obtained for the putative F1 hybrid in nature. DISCUSSION: Our results revealed that F1 hybrids between two Indo-Pacific species A. florida and A. intermedia had intermediate morphology relative to their parent species but reflected the maternal parent more. Similarity to maternal species in hybrids is opposite to the Caribbean Acropora species that had more paternal morphological characters in hybrids. These results further suggest that some genetic factor in eggs is likely to affect determination of colony shape in the Indo-Pacific. At present, we have considered colonies with intermediate morphs between different species to be intra-specific morphological variation, but they may be real F1 hybrids. Indeed, a putative F1 hybrid represented similar morphological and molecular features to the F1 hybrids, and thus it is plausible to be attributed as a "real" F1 hybrid in nature.

Ocean currents and herbivory drive macroalgae-to-coral community shift under climate warming.

Coral and macroalgal communities are threatened by global stressors. However, recently reported community shifts from temperate macroalgae to tropical corals offer conservation potential for corals at the expense of macroalgae under climate warming. Although such community shifts are expanding geographically, our understanding of the driving processes is still limited. Here, we reconstruct long-term climate-driven range shifts in 45 species of macroalgae, corals, and herbivorous fishes from over 60 years of records (mainly 1950-2015), stretching across 3,000 km of the Japanese archipelago from tropical to subarctic zones. Based on a revised coastal version of climate velocity trajectories, we found that prediction models combining the effects of climate and ocean currents consistently explained observed community shifts significantly better than those relying on climate alone. Corals and herbivorous fishes performed better at exploiting opportunities offered by this interaction. The contrasting range dynamics for these taxa suggest that ocean warming is promoting macroalgal-to-coral shifts both directly by increased competition from the expansion of tropical corals into the contracting temperate macroalgae, and indirectly via deforestation by the expansion of tropical herbivorous fish. Beyond individual species' effects, our results provide evidence on the important role that the interaction between climate warming and external forces conditioning the dispersal of organisms, such as ocean currents, can have in shaping community-level responses, with concomitant changes to ecosystem structure and functioning. Furthermore, we found that community shifts from macroalgae to corals might accelerate with future climate warming, highlighting the complexity of managing these evolving communities under future climate change.

Author Correction: Declaration of local chemical eradication of the Argentine ant: Bayesian estimation with a multinomial-mixture model.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

High-resolution modeling of thermal thresholds and environmental influences on coral bleaching for local and regional reef management.

Coral reefs are one of the world's most threatened ecosystems, with global and local stressors contributing to their decline. Excessive sea-surface temperatures (SSTs) can cause coral bleaching, resulting in coral death and decreases in coral cover. A SST threshold of 1 °C over the climatological maximum is widely used to predict coral bleaching. In this study, we refined thermal indices predicting coral bleaching at high-spatial resolution (1 km) by statistically optimizing thermal thresholds, as well as considering other environmental influences on bleaching such as ultraviolet (UV) radiation, water turbidity, and cooling effects. We used a coral bleaching dataset derived from the web-based monitoring system Sango Map Project, at scales appropriate for the local and regional conservation of Japanese coral reefs. We recorded coral bleaching events in the years 2004-2016 in Japan. We revealed the influence of multiple factors on the ability to predict coral bleaching, including selection of thermal indices, statistical optimization of thermal thresholds, quantification of multiple environmental influences, and use of multiple modeling methods (generalized linear models and random forests). After optimization, differences in predictive ability among thermal indices were negligible. Thermal index, UV radiation, water turbidity, and cooling effects were important predictors of the occurrence of coral bleaching. Predictions based on the best model revealed that coral reefs in Japan have experienced recent and widespread bleaching. A practical method to reduce bleaching frequency by screening UV radiation was also demonstrated in this paper.

Intraspecific variations in responses to ocean acidification in two branching coral species.

Ocean acidification is widely recognised to have a negative impact on marine calcifying organisms by reducing calcifications, but controversy remains over whether such organisms could cope with ocean acidification within a range of phenotypic plasticity and/or adapt to future acidifying ocean. We performed a laboratory rearing experiment using clonal fragments of the common branching corals Montipora digitata and Porites cylindrica under control and acidified seawater (lower pH) conditions (approximately 400 and 900µatm pCO2, respectively) and evaluated the intraspecific variations in their responses to ocean acidification. Intra- and interspecific variations in calcification and photosynthetic efficiency were evident according to both pCO2 conditions and colony, indicating that responses to acidification may be individually variable at the colony level. Our results suggest that some corals may cope with ocean acidification within their present genotypic composition by adaptation through phenotypic plasticity, while others may be placed under selective pressures resulting in population alteration.

Declaration of local chemical eradication of the Argentine ant: Bayesian estimation with a multinomial-mixture model.

Determining the success of eradication of an invasive species requires a way to decide when its risk of reoccurrence has become acceptably low. In Japan, the area populated by the Argentine ant, Linepithema humile (Mayr), is expanding, and eradication via chemical treatment is ongoing at various locations. One such program in Tokyo was apparently successful, because the ant population decreased to undetectable levels within a short time. However, construction of a population model for management purposes was difficult because the probability of detecting ants decreases rapidly as the population collapses. To predict the time when the ant was eradicated, we developed a multinomial-mixture model for chemical eradication based on monthly trapping data and the history of pesticide applications. We decided when to declare that eradication had been successful by considering both 'eradication' times, which we associated with eradication probabilities of 95% and 99%, and an optimal stopping time based on a 'minimum expected economic cost' that considered the possibility that surveys were stopped too soon. By applying these criteria, we retroactively declared that Argentine ants had been eradicated 38-42 months after the start of treatments (16-17 months after the last sighting).

Improving the interpretability of climate landscape metrics: An ecological risk analysis of Japan's Marine Protected Areas.

Conservation efforts strive to protect significant swaths of terrestrial, freshwater and marine ecosystems from a range of threats. As climate change becomes an increasing concern, these efforts must take into account how resilient-protected spaces will be in the face of future drivers of change such as warming temperatures. Climate landscape metrics, which signal the spatial magnitude and direction of climate change, support a convenient initial assessment of potential threats to and opportunities within ecosystems to inform conservation and policy efforts where biological data are not available. However, inference of risk from purely physical climatic changes is difficult unless set in a meaningful ecological context. Here, we aim to establish this context using historical climatic variability, as a proxy for local adaptation by resident biota, to identify areas where current local climate conditions will remain extant and future regional climate analogues will emerge. This information is then related to the processes governing species' climate-driven range edge dynamics, differentiating changes in local climate conditions as promoters of species range contractions from those in neighbouring locations facilitating range expansions. We applied this approach to assess the future climatic stability and connectivity of Japanese waters and its network of marine protected areas (MPAs). We find 88% of Japanese waters transitioning to climates outside their historical variability bounds by 2035, resulting in large reductions in the amount of available climatic space potentially promoting widespread range contractions and expansions. Areas of high connectivity, where shifting climates converge, are present along sections of the coast facilitated by the strong latitudinal gradient of the Japanese archipelago and its ocean current system. While these areas overlap significantly with areas currently under significant anthropogenic pressures, they also include much of the MPA network that may provide stepping-stone protection for species that must shift their distribution because of climate change.

Projecting the impacts of rising seawater temperatures on the distribution of seaweeds around Japan under multiple climate change scenarios.

Seaweed beds play a key role in providing essential habitats and energy to coastal areas, with enhancements in productivity and biodiversity and benefits to human societies. However, the spatial extent of seaweed beds around Japan has decreased due to coastal reclamation, water quality changes, rising water temperatures, and heavy grazing by herbivores. Using monthly mean sea surface temperature (SST) data from 1960 to 2099 and SST-based indices, we quantitatively evaluated the effects of warming seawater on the spatial extent of suitable versus unsuitable habitats for temperate seaweed Ecklonia cava, which is predominantly found in southern Japanese waters. SST data were generated using the most recent multiple climate projection models and emission scenarios (the Representative Concentration Pathways or RCPs) used in the Coupled Model Intercomparison Project phase 5 (CMIP5). In addition, grazing by Siganus fuscescens, an herbivorous fish, was evaluated under the four RCP simulations. Our results suggest that continued warming may drive a poleward shift in the distribution of E. cava, with large differences depending on the climate scenario. For the lowest emission scenario (RCP2.6), most existing E. cava populations would not be impacted by seawater warming directly but would be adversely affected by intensified year-round grazing. For the highest emission scenario (RCP8.5), previously suitable habitats throughout coastal Japan would become untenable for E. cava by the 2090s, due to both high-temperature stress and intensified grazing. Our projections highlight the importance of not only mitigating regional warming due to climate change, but also protecting E. cava from herbivores to conserve suitable habitats on the Japanese coast.

Responses of calcification of massive and encrusting corals to past, present, and near-future ocean carbon dioxide concentrations.

In this study, we report the acidification impact mimicking the pre-industrial, the present, and near-future oceans on calcification of two coral species (Porites australiensis, Isopora palifera) by using precise pCO2 control system which can produce acidified seawater under stable pCO2 values with low variations. In the analyses, we performed Bayesian modeling approaches incorporating the variations of pCO2 and compared the results between our modeling approach and classical statistical one. The results showed highest calcification rates in pre-industrial pCO2 level and gradual decreases of calcification in the near-future ocean acidification level, which suggests that ongoing and near-future ocean acidification would negatively impact coral calcification. In addition, it was expected that the variations of parameters of carbon chemistry may affect the inference of the best model on calcification responses to these parameters between Bayesian modeling approach and classical statistical one even under stable pCO2 values with low variations.

Negative effects of ocean acidification on two crustose coralline species using genetically homogeneous samples.

We evaluated acidification effects on two crustose coralline algal species common to Pacific coral reefs, Lithophyllum kotschyanum and Hydrolithon samoense. We used genetically homogeneous samples of both species to eliminate misidentification of species. The growth rates and percent calcification of the walls of the epithallial cells (thallus surface cells) of both species decreased with increasing pCO2. However, elevated pCO2 more strongly inhibited the growth of L. kotschyanum versus H. samoense. The trend of decreasing percent calcification of the cell wall did not differ between these species, although intercellular calcification of the epithallial cells in L. kotschyanum was apparently reduced at elevated pCO2, a result that might indicate that there are differences in the solubility or density of the calcite skeletons of these two species. These results can provide knowledge fundamental to future studies of the physiological and genetic mechanisms that underlie the response of crustose coralline algae to environmental stresses.

Role of food source and predator avoidance in habitat specialization by an octocoral-associated amphipod.

Small marine invertebrates often use sessile organisms as microhabitats, which can provide food sources and/or serve as refugees from predators. Because of the availability of external food items such as epibionts and detritus in the marine environment, these invertebrates may not depend on the sessile organisms as sole food sources. In this study, I hypothesized that habitat specialization by a marine invertebrate is determined by factors other than food. Results of field surveys off the coast of the Izu Peninsula, on the eastern coast of Japan, showed that, with few exceptions, the distribution of the amphipod Incisocalliope symbioticus was restricted to the octocoral Melithaea flabellifera. When presented with several habitat options, I. symbioticus selected M. flabellifera most frequently, although some individuals chose the octocoral Acabaria japonica. The selection was proximately determined by water-borne cues from M. flabellifera that appear to be unrelated to the octocoral as a food source, since the amphipod preferred detritus to the octocoral. As a chemical refuge, M. flabellifera had an allelopathic effect that deterred fish predation on the exposed epifauna. With regard to octocoral habitat in the study area, I. symbioticus may be restricted to M. flabellifera because this was the only abundant octocoral consistently occurring in shallow water (< or =10 m), where predation is intensive. The relationship between I. symbioticus and M. flabellifera was commensal and was ultimately driven by the value of M. flabellifera as a chemical refuge from predation, rather than its food value. This study supports the idea that protection from predators, rather than food utilization, can promote ecological specialization.