Effects of climate warming on energetics and habitat of the world's largest marine ectotherm.

Responses of organisms to climate warming are variable and complex. Effects on species distributions are already evident and mean global surface ocean temperatures are likely to warm by up to 4.1 °C by 2100, substantially impacting the physiology and distributions of ectotherms. The largest marine ectotherm, the whale shark Rhincodon typus, broadly prefers sea surface temperatures (SST) ranging from 23 to 30 °C. Whole-species distribution models have projected a poleward range shift under future scenarios of climate change, but these models do not consider intraspecific variation or phenotypic plasticity in thermal limits when modelling species responses, and the impact of climate warming on the energetic requirements of whale sharks is unknown. Using a dataset of 111 whale shark movement tracks from aggregation sites in five countries across the Indian Ocean and the latest Earth-system modelling produced from Coupled Model Intercomparison Project Phase 6 for the Intergovernmental Panel on Climate Change, we examined how SST and total zooplankton biomass, their main food source, may change in the future, and what this means for the energetic balance and extent of suitable habitat for whale sharks. Earth System Models, under three Shared Socioeconomic Pathways (SSPs; SSP1-2.6, SSP3-7.0 and SSP5-8.5), project that by 2100 mean SST in four regions where whale shark aggregations are found will increase by up to 4.9 °C relative to the present, while zooplankton biomass will decrease. This reduction in zooplankton is projected to be accompanied by an increase in the energetic requirements of whale sharks because warmer water temperatures will increase their metabolic rate. We found marked differences in projected changes in the extent of suitable habitat when comparing a whole-species distribution model to one including regional variation. This suggests that the conventional approach of combining data from different regions within a species' distribution could underestimate the amount of local adaptation in populations, although parameterising local models could also suffer from having insufficient data and lead to model mis-specification or highly uncertain estimates. Our study highlights the need for further research into whale shark thermal tolerances and energetics, the complexities involved in projecting species responses to climate change, and the potential importance of considering intraspecific variation when building species distribution models.

Evaluating ecological benefits of oceanic protected areas.

Oceans beyond the continental shelf represent the largest yet least protected environments. The new agreement to increase protection targets to 30% by 2030 and the recent United Nations (UN) High Seas Treaty try to address this gap, and an increase in the declaration of oceanic Marine Protected Areas (oMPAs) in waters beyond 200 m in depth is likely. Here we find that there is contradictory evidence concerning the benefits of oMPAs in terms of protecting pelagic habitats, providing refuge for highly mobile species, and potential fisheries benefits. We discover a mismatch between oMPA management objectives focusing on protection of pelagic habitats and biodiversity, and scientific research focusing on fisheries benefits. We suggest that the solution is to harness emerging technologies to monitor inside and outside oMPAs.

Habitat traits and predation interact to drive abundance and body size patterns in associated fauna.

Habitat-forming organisms provide three-dimensional structure that supports abundant and diverse communities. Variation in the morphological traits of habitat formers will therefore likely influence how they facilitate associated communities, either via food and habitat provisioning, or by altering predator-prey interactions. These mechanisms, however, are typically studied in isolation, and thus, we know little of how they interact to affect associated communities. In response to this, we used naturally occurring morphological variability in the alga Sargassum vestitum to create habitat units of distinct morphotypes to test whether variation in the morphological traits (frond size and thallus size) of S. vestitum or the interaction between these traits affects their value as habitat for associated communities in the presence and absence of predation. We found morphological traits did not interact, instead having independent effects on epifauna that were negligible in the absence of predation. However, when predators were present, habitat units with large fronds were found to host significantly lower epifaunal abundances than other morphotypes, suggesting that large frond alga provided low-value refuge from predators. The presence of predators also influenced the size structure of epifaunal communities from habitat units of differing frond size, suggesting that the refuge value of S. vestitum was also related to epifauna body size. This suggests that habitat formers may chiefly structure associated communities by mediating size-selective predation, and not through habitat provisioning. Furthermore, these results also highlight that habitat traits cannot be considered in isolation, for their interaction with biotic processes can have significant implications for associated communities.

Improving the biological realism of predator-prey size relationships in food web models alters ecosystem dynamics.

Body-size relationships between predators and prey exhibit remarkable diversity. However, the assumption that predators typically consume proportionally smaller prey often underlies size-dependent predation in ecosystem models. In reality, some animals can consume larger prey or exhibit limited changes in prey size as they grow larger themselves. These distinct predator-prey size relationships challenge the conventional assumptions of traditional size-based models. Cephalopods, with their diverse feeding behaviours and life histories, offer an excellent case study to investigate the impact of greater biological realism in predator-prey size relationships on energy flow within a size-structured ecosystem model. By categorizing cephalopods into high and low-activity groups, in line with empirically derived, distinct predator-prey size relationships, we found that incorporating greater biological realism in size-based feeding reduced ecosystem biomass and production, while simultaneously increasing biomass stability and turnover. Our results have broad implications for ecosystem modelling, since distinct predator-prey size relationships extend beyond cephalopods, encompassing a wide array of major taxonomic groups from filter-feeding fishes to baleen whales. Incorporating a diversity of size-based feeding in food web models can enhance their ecological and predictive accuracy when studying ecosystem dynamics.

Priority areas to protect mangroves and maximise ecosystem services.

Anthropogenic activities threaten global biodiversity and ecosystem services. Yet, area-based conservation efforts typically target biodiversity protection whilst minimising conflict with economic activities, failing to consider ecosystem services. Here we identify priority areas that maximise both the protection of mangrove biodiversity and their ecosystem services. We reveal that despite 13.5% of the mangrove distribution being currently strictly protected, all mangrove species are not adequately represented and many areas that provide disproportionally large ecosystem services are missed. Optimising the placement of future conservation efforts to protect 30% of global mangroves potentially safeguards an additional 16.3 billion USD of coastal property value, 6.1 million people, 1173.1 Tg C, and 50.7 million fisher days yr-1. Our findings suggest that there is a pressing need for including ecosystem services in protected area design and that strategic prioritisation and coordination of mangrove conservation could provide substantial benefits to human wellbeing.

Trophic amplification: A model intercomparison of climate driven changes in marine food webs.

Marine animal biomass is expected to decrease in the 21st century due to climate driven changes in ocean environmental conditions. Previous studies suggest that the magnitude of the decline in primary production on apex predators could be amplified through the trophodynamics of marine food webs, leading to larger decreases in the biomass of predators relative to the decrease in primary production, a mechanism called trophic amplification. We compared relative changes in producer and consumer biomass or production in the global ocean to assess the extent of trophic amplification. We used simulations from nine marine ecosystem models (MEMs) from the Fisheries and Marine Ecosystem Models Intercomparison Project forced by two Earth System Models under the high greenhouse gas emissions Shared Socioeconomic Pathways (SSP5-8.5) and a scenario of no fishing. Globally, total consumer biomass is projected to decrease by 16.7 ± 9.5% more than net primary production (NPP) by 2090-2099 relative to 1995-2014, with substantial variations among MEMs and regions. Total consumer biomass is projected to decrease almost everywhere in the ocean (80% of the world's oceans) in the model ensemble. In 40% of the world's oceans, consumer biomass was projected to decrease more than NPP. Additionally, in another 36% of the world's oceans consumer biomass is expected to decrease even as projected NPP increases. By analysing the biomass response within food webs in available MEMs, we found that model parameters and structures contributed to more complex responses than a consistent amplification of climate impacts of higher trophic levels. Our study provides additional insights into the ecological mechanisms that will impact marine ecosystems, thereby informing model and scenario development.

Gelatinous larvacean zooplankton can enhance trophic transfer and carbon sequestration.

Larvaceans are gelatinous zooplankton abundant throughout the ocean. Larvaceans have been overlooked in research because they are difficult to collect and are perceived as being unimportant in biogeochemical cycles and food-webs. We synthesise evidence that their unique biology enables larvaceans to transfer more carbon to higher trophic levels and deeper into the ocean than is commonly appreciated. Larvaceans could become even more important in the Anthropocene because they eat small phytoplankton that are predicted to become more prevalent under climate change, thus moderating projected future declines in ocean productivity and fisheries. We identify critical knowledge gaps and argue that larvaceans should be incorporated into ecosystem assessments and biogeochemical models to improve predictions of the future ocean.

Demystifying global climate models for use in the life sciences.

For each assessment cycle of the Intergovernmental Panel on Climate Change (IPCC), researchers in the life sciences are called upon to provide evidence to policymakers planning for a changing future. This research increasingly relies on highly technical and complex outputs from climate models. The strengths and weaknesses of these data may not be fully appreciated beyond the climate modelling community; therefore, uninformed use of raw or preprocessed climate data could lead to overconfident or spurious conclusions. We provide an accessible introduction to climate model outputs that is intended to empower the life science community to robustly address questions about human and natural systems in a changing world.

A metric-based framework for climate-smart conservation planning.

Climate change is already having profound effects on biodiversity, but climate change adaptation has yet to be fully incorporated into area-based management tools used to conserve biodiversity, such as protected areas. One main obstacle is the lack of consensus regarding how impacts of climate change can be included in spatial conservation plans. We propose a climate-smart framework that prioritizes the protection of climate refugia-areas of low climate exposure and high biodiversity retention-using climate metrics. We explore four aspects of climate-smart conservation planning: (1) climate model ensembles; (2) multiple emission scenarios; (3) climate metrics; and (4) approaches to identifying climate refugia. We illustrate this framework in the Western Pacific Ocean, but it is equally applicable to terrestrial systems. We found that all aspects of climate-smart conservation planning considered affected the configuration of spatial plans. The choice of climate metrics and approaches to identifying refugia have large effects in the resulting climate-smart spatial plans, whereas the choice of climate models and emission scenarios have smaller effects. As the configuration of spatial plans depended on climate metrics used, a spatial plan based on a single measure of climate change (e.g., warming) will not necessarily be robust against other measures of climate change (e.g., ocean acidification). We therefore recommend using climate metrics most relevant for the biodiversity and region considered based on a single or multiple climate drivers. To include the uncertainty associated with different climate futures, we recommend using multiple climate models (i.e., an ensemble) and emission scenarios. Finally, we show that the approaches we used to identify climate refugia feature trade-offs between: (1) the degree to which they are climate-smart, and (2) their efficiency in meeting conservation targets. Hence, the choice of approach will depend on the relative value that stakeholders place on climate adaptation. By using this framework, protected areas can be designed with improved longevity and thus safeguard biodiversity against current and future climate change. We hope that the proposed climate-smart framework helps transition conservation planning toward climate-smart approaches.

Monitoring and modelling marine zooplankton in a changing climate.

Zooplankton are major consumers of phytoplankton primary production in marine ecosystems. As such, they represent a critical link for energy and matter transfer between phytoplankton and bacterioplankton to higher trophic levels and play an important role in global biogeochemical cycles. In this Review, we discuss key responses of zooplankton to ocean warming, including shifts in phenology, range, and body size, and assess the implications to the biological carbon pump and interactions with higher trophic levels. Our synthesis highlights key knowledge gaps and geographic gaps in monitoring coverage that need to be urgently addressed. We also discuss an integrated sampling approach that combines traditional and novel techniques to improve zooplankton observation for the benefit of monitoring zooplankton populations and modelling future scenarios under global changes.

Potential impacts of climate change on agriculture and fisheries production in 72 tropical coastal communities.

Climate change is expected to profoundly affect key food production sectors, including fisheries and agriculture. However, the potential impacts of climate change on these sectors are rarely considered jointly, especially below national scales, which can mask substantial variability in how communities will be affected. Here, we combine socioeconomic surveys of 3,008 households and intersectoral multi-model simulation outputs to conduct a sub-national analysis of the potential impacts of climate change on fisheries and agriculture in 72 coastal communities across five Indo-Pacific countries (Indonesia, Madagascar, Papua New Guinea, Philippines, and Tanzania). Our study reveals three key findings: First, overall potential losses to fisheries are higher than potential losses to agriculture. Second, while most locations (> 2/3) will experience potential losses to both fisheries and agriculture simultaneously, climate change mitigation could reduce the proportion of places facing that double burden. Third, potential impacts are more likely in communities with lower socioeconomic status.

A global, historical database of tuna, billfish, and saury larval distributions.

Knowing the distribution of fish larvae can inform fisheries science and resource management in several ways, by: 1) providing information on spawning areas; 2) identifying key areas to manage and conserve; and 3) helping to understand how fish populations are affected by anthropogenic pressures, such as overfishing and climate change. With the expansion of industrial fishing activity after 1945, there was increased sampling of fish larvae to help better understand variation in fish stocks. However, large-scale larval records are rare and often unavailable. Here we digitize data from Nishikawa et al. (1985), which were collected from 1956-1981 and are near-global (50°N-50°S), seasonal distribution maps of fish larvae of 18 mainly commercial pelagic taxa of the families Scombridae, Xiphiidae, Istiophoridae, Scombrolabracidae, and Scomberesocidae. Data were collected from the Pacific, Atlantic, and Indian Oceans. We present four seasonal 1° × 1° resolution maps per taxa representing larval abundance per grid cell and highlight some of the main patterns. Data are made available as delimited text, raster, and vector files.

Next-generation ensemble projections reveal higher climate risks for marine ecosystems.

Projections of climate change impacts on marine ecosystems have revealed long-term declines in global marine animal biomass and unevenly distributed impacts on fisheries. Here we apply an enhanced suite of global marine ecosystem models from the Fisheries and Marine Ecosystem Model Intercomparison Project (Fish-MIP), forced by new-generation Earth system model outputs from Phase 6 of the Coupled Model Intercomparison Project (CMIP6), to provide insights into how projected climate change will affect future ocean ecosystems. Compared with the previous generation CMIP5-forced Fish-MIP ensemble, the new ensemble ecosystem simulations show a greater decline in mean global ocean animal biomass under both strong-mitigation and high-emissions scenarios due to elevated warming, despite greater uncertainty in net primary production in the high-emissions scenario. Regional shifts in the direction of biomass changes highlight the continued and urgent need to reduce uncertainty in the projected responses of marine ecosystems to climate change to help support adaptation planning.

Movement ecology of black marlin Istiompax indica in the Western Indian Ocean.

The black marlin Istiompax indica is an apex marine predator and is susceptible to overfishing. The movement ecology of the species remains poorly known, particularly within the Indian Ocean, which has hampered assessment of their conservation status and fisheries management requirements. Here, we used pop-up archival satellite tags to track I. indica movement and examine their dispersal. Forty-nine tags were deployed off Kenya during both the north-east (November-April) and south-west (August-September) monsoon seasons, providing locations from every month of the year. Individual I. indica were highly mobile and track distance correlated with the duration of tag attachment. Mean track duration was 38 days and mean track distance was >1800 km. Individuals dispersed in several directions: north-east into Somalian waters and up to northern Oman, east towards the Seychelles, and south into the Mozambique Channel. Their core habitat shifted seasonally and overlapped with areas of high productivity off Kenya, Somalia and Oman during the first half of the year. A second annual aggregation off the Kenyan coast, during August and September, did not coincide with high chlorophyll-a (chl-a) concentrations or thermal fronts, and the drivers of the species' presence and movement from this second aggregation was unclear. We tested their habitat preferences by comparing environmental conditions at track locations to the conditions at locations along simulated tracks based on the empirical data. Observed I. indica preferred cooler water with higher chl-a concentrations and stayed closer to the coast than simulated tracks. The rapid and extensive dispersal of I. indica from Kenya suggests that there is likely a single stock in the Western Indian Ocean, with individuals swimming between areas of high commercial catches off northern Somalia and Oman, and artisanal and recreational fisheries catches throughout East Africa and Mozambique.

Mutualism promotes site selection in a large marine planktivore.

Mutualism is a form of symbiosis whereby both parties benefit from the relationship. An example is cleaning symbiosis, which has been observed in terrestrial and marine environments. The most recognized form of marine cleaning symbiosis is that of cleaner fishes and their clients.Cleaner species set up cleaning stations on the reef, and other species seek out their services. However, it is not well understood how the presence of cleaning stations influence movements of large highly mobile species. We examined the role of cleaning stations as a driver of movement and habitat use in a mobile client species.Here, we used a combination of passive acoustic telemetry and in-water surveys to investigate cleaning station attendance by the reef manta ray Mobula alfredi. We employed a novel approach in the form of a fine-scale acoustic receiver array set up around a known cleaning area and tagged 42 rays. Within the array, we mapped structural features, surveyed the distribution of cleaner wrasse, and observed the habitat use of the rays.We found manta ray space use was significantly associated with blue-streak cleaner wrasse Labroides dimidiatus distribution and hard coral substrate. Cleaning interactions dominated their habitat use at this site, taking precedence over other life history traits such as feeding and courtship.This study has demonstrated that cleaning symbiosis is a driver for highly mobile, and otherwise pelagic, species to visit inshore reef environments. We suggest that targeted and long-term use of specific cleaning stations reflects manta rays having a long-term memory and cognitive map of some shallow reef environments where quality cleaning is provided. We hypothesize that animals prefer cleaning sites in proximity to productive foraging regions.

Functional traits explain trophic allometries of cephalopods.

Individual body size strongly influences the trophic role of marine organisms and the structure and function of marine ecosystems. Quantifying trophic position-individual body size relationships (trophic allometries) underpins the development of size-structured ecosystem models to predict abundance and the transfer of energy through ecosystems. Trophic allometries are well studied for fishes but remain relatively unexplored for cephalopods. Cephalopods are important components of coastal, oceanic and deep-sea ecosystems, and they play a key role in the transfer of biomass from low trophic positions to higher predators. It is therefore important to resolve cephalopod trophic allometries to accurately represent them within size-structured ecosystem models. We assessed the trophic positions of cephalopods in an oceanic pelagic (0-500 m) community (sampled by trawling in a cold-core eddy in the western Tasman Sea), comprising 22 species from 12 families, using bulk tissue stable isotope analysis and amino acid compound-specific stable isotope analysis. We assessed whether ontogenetic trophic position shifts were evident at the species-level and tested for the best predictor of community-level trophic allometry among body size, taxonomy and functional grouping (informed by fin and mantle morphology). Individuals in this cephalopod community spanned two trophic positions and fell into three functional groups on an activity level gradient: low, medium and high. The relationship between trophic position and ontogeny varied among species, with the most marked differences evident between species from different functional groups. Activity-level-based functional group and individual body size are best explained by cephalopod trophic positions (marginal R2  = 0.43). Our results suggest that the morphological traits used to infer activity level, such as fin-to-mantle length ratio, fin musculature and mantle musculature are strong predictors of cephalopod trophic allometries. Contrary to established theory, not all cephalopods are voracious predators. Low activity level cephalopods have a distinct feeding mode, with low trophic positions and little-to-no ontogenetic increases. Given the important role of cephalopods in marine ecosystems, distinct feeding modes could have important consequences for energy pathways and ecosystem structure and function. These findings will facilitate trait-based and other model estimates of cephalopod abundance in the changing global ocean.

A database of zooplankton biomass in Australian marine waters.

Zooplankton biomass data have been collected in Australian waters since the 1930s, yet most datasets have been unavailable to the research community. We have searched archives, scanned the primary and grey literature, and contacted researchers, to collate 49187 records of marine zooplankton biomass from waters around Australia (0-60°S, 110-160°E). Many of these datasets are relatively small, but when combined, they provide >85 years of zooplankton biomass data for Australian waters from 1932 to the present. Data have been standardised and all available metadata included. We have lodged this dataset with the Australian Ocean Data Network, allowing full public access. The Australian Zooplankton Biomass Database will be valuable for global change studies, research assessing trophic linkages, and for initialising and assessing biogeochemical and ecosystem models of lower trophic levels.

Reduced exploitation is associated with an altered sex ratio and larger length at maturity in southwest Pacific (east Australian) Pomatomus saltatrix.

Pomatomus saltatrix is an important recreational fishing species with seven major populations worldwide. The reproductive biology of the southwest Pacific Ocean (east Australian) population is uncertain, with both an extended spawning and multiple spawning periods previously hypothesised. Here we demonstrate an altered sex ratio biased towards females and a larger length at 50% maturity (L50) compared to those recorded for the population 40 years ago, before comprehensive management strategies were implemented. We also report a second, previously undescribed, late-summer spawning event which was identified by analysing patterns in a gonadosomatic index across the whole population and an historical larval fish database. P. saltatrix are capable of spawning multiple times per season with estimates of batch fecundity ranging from 99,488 to 1,424,425 eggs per fish. When combined with the length frequency distribution of the population, the majority of eggs (64%) were shown to be produced by fish ≤40 cm fork length (FL). L50 was estimated at 30.2 and 31.5 cm FL for male and female P. saltatrix respectively, 4 cm larger than 40 years ago. The sex ratio of the population was found to have significantly shifted over the last 40 years from an equal sex ratio to a female dominated population (1.58 females:1 male). These dramatic alterations to the sex ratio and L50 highlights the value of monitoring the reproductive biology of exploited fish populations to ensure that management plans remain appropriate.

A database of marine larval fish assemblages in Australian temperate and subtropical waters.

Larval fishes are a useful metric of marine ecosystem state and change, as well as species-specific patterns in phenology. The high level of taxonomic expertise required to identify larval fishes to species level, and the considerable effort required to collect samples, make these data very valuable. Here we collate 3178 samples of larval fish assemblages, from 12 research projects from 1983-present, from temperate and subtropical Australian pelagic waters. This forms a benchmark for the larval fish assemblage for the region, and includes recent monitoring of larval fishes at coastal oceanographic reference stations. Comparing larval fishes among projects can be problematic due to differences in taxonomic resolution, and identifying all taxa to species is challenging, so this study reports a standard taxonomic resolution (of 218 taxa) for this region to help guide future research. This larval fish database serves as a data repository for surveys of larval fish assemblages in the region, and can contribute to analysis of climate-driven changes in the location and timing of the spawning of marine fishes.