Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

Changes in sea floor productivity are crucial to understanding the impact of climate change in temperate coastal ecosystems according to a new size-based model.

The multifaceted effects of climate change on physical and biogeochemical processes are rapidly altering marine ecosystems but often are considered in isolation, leaving our understanding of interactions between these drivers of ecosystem change relatively poor. This is particularly true for shallow coastal ecosystems, which are fuelled by a combination of distinct pelagic and benthic energy pathways that may respond to climate change in fundamentally distinct ways. The fish production supported by these systems is likely to be impacted by climate change differently to those of offshore and shelf ecosystems, which have relatively simpler food webs and mostly lack benthic primary production sources. We developed a novel, multispecies size spectrum model for shallow coastal reefs, specifically designed to simulate potential interactive outcomes of changing benthic and pelagic energy inputs and temperatures and calculate the relative importance of these variables for the fish community. Our model, calibrated using field data from an extensive temperate reef monitoring program, predicts that changes in resource levels will have much stronger impacts on fish biomass and yields than changes driven by physiological responses to temperature. Under increased plankton abundance, species in all fish trophic groups were predicted to increase in biomass, average size, and yields. By contrast, changes in benthic resources produced variable responses across fish trophic groups. Increased benthic resources led to increasing benthivorous and piscivorous fish biomasses, yields, and mean body sizes, but biomass decreases among herbivore and planktivore species. When resource changes were combined with warming seas, physiological responses generally decreased species' biomass and yields. Our results suggest that understanding changes in benthic production and its implications for coastal fisheries should be a priority research area. Our modified size spectrum model provides a framework for further study of benthic and pelagic energy pathways that can be easily adapted to other ecosystems.

Population parameters and conservation implications for one of the world's rarest marine fishes, the red handfish (Thymichthys politus).

Population estimates are required for effective conservation of many rare marine species, but can be difficult to obtain. The critically endangered red handfish (Thymichthys politus) is a coastal anglerfish known only from two fragmented populations in southeast Tasmania, Australia. It is at a high risk of extinction due to low numbers, loss of habitat, and the impacts of climate change. To aid conservation efforts, we provide the first empirical population size estimates of red handfish and investigate other important aspects of the species' life history, such as growth, habitat association, and movement. We surveyed both red handfish local populations via underwater visual census on scuba over 3 years and used photographic mark-recapture techniques to estimate biological parameters. In 2020, the local adult population size was estimated to be 94 (95% confidence interval [CI] 40-231) adults at one site, and 7 (95% CI 5-10) at the other site, suggesting an estimated global population of 101 adults. Movement of individuals was extremely limited at 48.5 m (± 77.7 S.D.) per year. We also found evidence of declining fish density, a declining proportion of juveniles, and increasing average fish size during the study. These results provide a serious warning that red handfish are likely sliding toward extinction, and highlight the urgent need to expand efforts for ex situ captive breeding to bolster numbers in the wild and maintain captive insurance populations, and to protect vital habitat to safeguard the species' ongoing survival in the wild.

Thermal biases and vulnerability to warming in the world's marine fauna.

A critical assumption underlying projections of biodiversity change associated with global warming is that ecological communities comprise balanced mixes of warm-affinity and cool-affinity species which, on average, approximate local environmental temperatures. Nevertheless, here we find that most shallow water marine species occupy broad thermal distributions that are aggregated in either temperate or tropical realms. These distributional trends result in ocean-scale spatial thermal biases, where communities are dominated by species with warmer or cooler affinity than local environmental temperatures. We use community-level thermal deviations from local temperatures as a form of sensitivity to warming, and combine these with projected ocean warming data to predict warming-related loss of species from present-day communities over the next century. Large changes in local species composition appear likely, and proximity to thermal limits, as inferred from present-day species' distributional ranges, outweighs spatial variation in warming rates in contributing to predicted rates of local species loss.

Global conservation outcomes depend on marine protected areas with five key features.

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km(2)), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.

Biological interactions both facilitate and resist climate-related functional change in temperate reef communities.

Shifts in the abundance and location of species are restructuring life on the Earth, presenting the need to build resilience into our natural systems. Here, we tested if protection from fishing promotes community resilience in temperate reef communities undergoing rapid warming in Tasmania. Regardless of protection status, we detected a signature of warming in the brown macroalgae, invertebrates and fishes, through increases in the local richness and abundance of warm-affinity species. Even so, responses in protected communities diverged from exploited communities. At the local scale, the number of cool-affinity fishes and canopy-forming algal species increased following protection, even though the observation window fell within a period of warming. At the same time, exploited communities gained turf algal and sessile invertebrate species. We further found that the recovery of predator populations following protection leads to marked declines in mobile invertebrates-this trend could be incorrectly attributed to warming without contextual data quantifying community change across trophic levels. By comparing long-term change in exploited and protected reefs, we empirically demonstrate the role of biological interactions in both facilitating and resisting climate-related biodiversity change. We further highlight the potential for trophic interactions to alter the progression of both range expansions and contractions.

Corrigendum: Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

[This corrects the article DOI: 10.1093/biosci/biw180.].

Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continental- and decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.

Do communities exist? Complex patterns of overlapping marine species distributions.

Understanding the way in which species are associated in communities is a fundamental question in ecology. Yet there remains a tension between communities as highly structured units or as coincidental collections of individualistic species. We explored these ideas using a new statistical approach that clusters species based on their environmental response: a species archetype, rather than clustering sites based on their species composition. We found groups of species that are consistently highly correlated, but that these groups are not unique to any set of locations and overlap spatially. The species present at a single site are a realization of species from the (multiple) archetype groups that are likely to be present at that location based on their response to the environment.

Congruence in demersal fish, macroinvertebrate, and macroalgal community turnover on shallow temperate reefs.

To support coastal planning through improved understanding of patterns of biotic and abiotic surrogacy at broad scales, we used gradient forest modeling (GFM) to analyze and predict spatial patterns of compositional turnover of demersal fishes, macroinvertebrates, and macroalgae on shallow, temperate Australian reefs. Predictive models were first developed using environmental surrogates with estimates of prediction uncertainty, and then the efficacy of the three assemblages as biosurrogates for each other was assessed. Data from underwater visual surveys of subtidal rocky reefs were collected from the southeastern coastline of continental Australia (including South Australia and Victoria) and the northern coastline of Tasmania. These data were combined with 0.01 degree-resolution gridded environmental variables to develop statistical models of compositional turnover (beta diversity) using GFM. GFM extends the machine learning, ensemble tree-based method of random forests (RF), to allow the simultaneous modeling of multiple taxa. The models were used to generate predictions of compositional turnover for each of the three assemblages within unsurveyed areas across the 6600 km of coastline in the region of interest. The most important predictor for all three assemblages was variability in sea surface temperature (measured as standard deviation from measures taken interannually). Spatial predictions of compositional turnover within unsurveyed areas across the region of interest were remarkably congruent across the three taxa. However, the greatest uncertainty in these predictions varied in location among the different assemblages. Pairwise congruency comparisons of observed and predicted turnover among the three assemblages showed that invertebrate and macroalgal biodiversity were most similar, followed by fishes and macroalgae, and lastly fishes and invertebrate biodiversity, suggesting that of the three assemblages, macroalgae would make the best biosurrogate for both invertebrate and fish compositional turnover.

Implications of macroalgal isolation by distance for networks of marine protected areas.

The global extent of macroalgal forests is declining, greatly affecting marine biodiversity at broad scales through the effects macroalgae have on ecosystem processes, habitat provision, and food web support. Networks of marine protected areas comprise one potential tool that may safeguard gene flow among macroalgal populations in the face of increasing population fragmentation caused by pollution, habitat modification, climate change, algal harvesting, trophic cascades, and other anthropogenic stressors. Optimal design of protected area networks requires knowledge of effective dispersal distances for a range of macroalgae. We conducted a global meta-analysis based on data in the published literature to determine the generality of relation between genetic differentiation and geographic distance among macroalgal populations. We also examined whether spatial genetic variation differed significantly with respect to higher taxon, life history, and habitat characteristics. We found clear evidence of population isolation by distance across a multitude of macroalgal species. Genetic and geographic distance were positively correlated across 49 studies; a modal distance of 50-100 km maintained F(ST) < 0.2. This relation was consistent for all algal divisions, life cycles, habitats, and molecular marker classes investigated. Incorporating knowledge of the spatial scales of gene flow into the design of marine protected area networks will help moderate anthropogenic increases in population isolation and inbreeding and contribute to the resilience of macroalgal forests.

Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Monitoring the resilience of a no-take marine reserve to a range extending species using benthic imagery.

Global climate change is driving the redistribution of marine species and thereby potentially restructuring endemic communities. Understanding how localised conservation measures such as protection from additional human pressures can confer resilience to ecosystems is therefore an important area of research. Here, we examine the resilience of a no-take marine reserve (NTR) to the establishment of urchin barrens habitat. The barrens habitat is created through overgrazing of kelp by an invading urchin species that is expanding its range within a hotspot of rapid climate change. In our study region, a multi-year monitoring program provides a unique time-series of benthic imagery collected by an Autonomous Underwater Vehicle (AUV) within an NTR and nearby reference areas. We use a Bayesian hierarchical spatio-temporal modelling approach to estimate whether the NTR is associated with reduced formation of urchin barrens, and thereby enhances local resilience. Our approach controls for the important environmental covariates of depth and habitat complexity (quantified as rugosity derived from multibeam sonar mapping), as well as spatial and temporal dependence. We find evidence for the NTR conferring resilience with a strong reserve effect that suggests improved resistance to the establishment of barrens. However, we find a concerning and consistent trajectory of increasing barrens cover in both the reference areas and the NTR, with the odds of barrens increasing by approximately 32% per year. Thus, whereas the reserve is demonstrating resilience to the initial establishment of barrens, there is currently no evidence of recovery once barrens are established. We also find that depth and rugosity covariates derived from multibeam mapping provide useful predictors for barrens occurrence. These results have important management implications as they demonstrate: (i) the importance of monitoring programs to inform adaptive management; (ii) that NTRs provide a potential local conservation management tool under climate change impacts, and (iii) that technologies such as AUVs and multibeam mapping can be harnessed to inform regional decision-making. Continuation of the current monitoring program is required to assess whether the NTR can provide long term protection from a phase shift that replaces kelp with urchin barrens.

Fish body sizes change with temperature but not all species shrink with warming.

Ectotherms generally shrink under experimental warming, but whether this pattern extends to wild populations is uncertain. We analysed ten million visual survey records, spanning the Australian continent and multiple decades and comprising the most common coastal reef fishes (335 species). We found that temperature indeed drives spatial and temporal changes in fish body size, but not consistently in the negative fashion expected. Around 55% of species were smaller in warmer waters (especially among small-bodied species), while 45% were bigger. The direction of a species' response to temperature through space was generally consistent with its response to temperature increase through time at any given location, suggesting that spatial trends could help forecast fish responses to long-term warming. However, temporal changes were about ten times faster than spatial trends (~4% versus ~40% body size change per 1 °C change through space and time, respectively). The rapid and variable responses of fish size to warming may herald unexpected impacts on ecosystem restructuring, with potentially greater consequences than if all species were shrinking.

Latitude and protection affect decadal trends in reef trophic structure over a continental scale.

The relative roles of top-down (consumer-driven) and bottom-up (resource-driven) forcing in exploited marine ecosystems have been much debated. Examples from a variety of marine systems of exploitation-induced, top-down trophic forcing have led to a general view that human-induced predator perturbations can disrupt entire marine food webs, yet other studies that have found no such evidence provide a counterpoint. Though evidence continues to emerge, an unresolved debate exists regarding both the relative roles of top-down versus bottom-up forcing and the capacity of human exploitation to instigate top-down, community-level effects. Using time-series data for 104 reef communities spanning tropical to temperate Australia from 1992 to 2013, we aimed to quantify relationships among long-term trophic group population density trends, latitude, and exploitation status over a continental-scale biogeographic range. Specifically, we amalgamated two long-term monitoring databases of marine community dynamics to test for significant positive or negative trends in density of each of three key trophic levels (predators, herbivores, and algae) across the entire time series at each of the 104 locations. We found that trophic control tended toward bottom-up driven in tropical systems and top-down driven in temperate systems. Further, alternating long-term population trends across multiple trophic levels (a method of identifying trophic cascades), presumably due to top-down trophic forcing, occurred in roughly fifteen percent of locations where the prerequisite significant predator trends occurred. Such alternating trophic trends were significantly more likely to occur at locations with increasing predator densities over time. Within these locations, we found a marked latitudinal gradient in the prevalence of long-term, alternating trophic group trends, from rare in the tropics (<5% of cases) to relatively common in temperate areas (~45%). Lastly, the strongest trends in predator and algal density occurred in older no-take marine reserves; however, exploitation status did not affect the likelihood of alternating long-term trophic group trends occurring. Our data suggest that the type and degree of trophic forcing in this system are likely related to one or more covariates of latitude, and that ecosystem resiliency to top-down control does not universally vary in this system based on exploitation level.

Exploited reefs protected from fishing transform over decades into conservation features otherwise absent from seascapes.

Tasmanian reef communities within "no-take" marine protected areas (MPAs) exhibited direct and indirect ecological changes that increasingly manifested over 16 years, eventually transforming into communities not otherwise present in the regional seascape. Data from 14 temperate and subtropical Australian MPAs further demonstrated that ecological changes continue to develop in MPAs over at least two decades, probably much longer. The continent-scale study additionally showed recently established MPAs to be consistently located at sites with low resource value relative to adjacent fished reference areas. This outcome was presumably generated by sociopolitical pressures and planning processes that aim to systematically avoid locations with valuable resources, potentially compromising biodiversity conservation goals. Locations that were formerly highly fished are needed within MPA networks if the networks are to achieve conservation aims associated with (1) safeguarding all regional habitat types, (2) protecting threatened habitats and species, and (3) providing appropriate reference benchmarks for assessing impacts of fishing. Because of long time lags, the ubiquity of fishing impacts, and the relatively recent establishment of MPAs, the full impact of fishing on coastal reefs has yet to be empirically assessed.

An evaluation of the error and uncertainty in epibenthos cover estimates from AUV images collected with an efficient, spatially-balanced design.

Efficient monitoring of organisms is at the foundation of protected area and biodiversity management. Such monitoring programs are based on a systematically selected set of survey locations that, while able to track trends at those locations through time, lack inference for the overall region being "monitored". Advances in spatially-balanced sampling approaches offer alternatives but remain largely untested in marine ecosystems. This study evaluated the merit of using a two-stage, spatially-balanced survey framework, in conjunction with generalized additive models, to estimate epifauna cover at a reef-wide scale for mesophotic reefs within a large, cross-shelf marine park. Imagery acquired by an autonomous underwater vehicle was classified using a hierarchical scheme developed under the Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI). At a realistic image subsampling intensity, the two-stage, spatially-balanced framework provided accurate and precise estimates of reef-wide cover for a select number of epifaunal classes at the coarsest CATAMI levels, in particular bryozoan and porifera classes. However, at finer hierarchical levels, accuracy and/or precision of cover estimates declined, primarily because of the natural rarity of even the most common of these classes/morphospecies. Ranked predictor importance suggested that bathymetry, backscatter and derivative terrain variables calculated at their smallest analysis window scales (i.e. 81 m2) were generally the most important variables in the modeling of reef-wide cover. This study makes an important step in identifying the constraints and limitations that can be identified through a robust statistical approach to design and analysis. The two-stage, spatially-balanced framework has great potential for effective quantification of epifaunal cover in cross-shelf mesophotic reefs. However, greater image subsampling intensity than traditionally applied is required to ensure adequate observations for finer-level CATAMI classes and associated morphospecies.

Gigapixel big data movies provide cost-effective seascape scale direct measurements of open-access coastal human use such as recreational fisheries.

Collecting data on unlicensed open-access coastal activities, such as some types of recreational fishing, has often relied on telephone interviews selected from landline directories. However, this approach is becoming obsolete due to changes in communication technology such as a switch to unlisted mobile phones. Other methods, such as boat ramp interviews, are often impractical due to high labor cost. We trialed an autonomous, ultra-high-resolution photosampling method as a cost effect solution for direct measurements of a recreational fishery. Our sequential photosampling was batched processed using a novel software application to produce "big data" time series movies from a spatial subset of the fishery, and we validated this with a regional bus-route survey and interviews with participants at access points. We also compared labor costs between these two methods. Most trailer boat users were recreational fishers targeting tuna spp. Our camera system closely matched trends in temporal variation from the larger scale regional survey, but as the camera data were at much higher frequency, we could additionally describe strong, daily variability in effort. Peaks were normally associated with weekends, but consecutive weekend tuna fishing competitions led to an anomaly of high effort across the normal weekday lulls. By reducing field time and batch processing imagery, Monthly labor costs for the camera sampling were a quarter of the bus-route survey; and individual camera samples cost 2.5% of bus route samples to obtain. Gigapixel panoramic camera observations of fishing were representative of the temporal variability of regional fishing effort and could be used to develop a cost-efficient index. High-frequency sampling had the added benefit of being more likely to detect abnormal patterns of use. Combinations of remote sensing and on-site interviews may provide a solution to describing highly variable effort in recreational fisheries while also validating activity and catch.

Local densities and habitat preference of the critically endangered spotted handfish (Brachionichthys hirsutus): Large scale field trial of GPS parameterised underwater visual census and diver attached camera.

The critically endangered spotted handfish (Brachionichthys hirsutus) is restricted to a limited number of locations in south-eastern Tasmania, Australia. As is often the case for rare species, conducting statistically adequate surveys for B. hirsutus can be costly and time consuming due to the low probability of encountering individuals. For the first time we used a highly efficient and rigorous Global Positioning System (GPS) parameterised underwater visual census (GUVC) to survey B. hirsutus abundance within all nine known local populations in the Derwent Estuary within one season. In addition, a benthic microhabitat assessment was conducted simultaneously using a GoPro® camera attached to diver to determine B. hirsutus microhabitat preferences. B. hirsutus local populations varied between sites, with densities ranging from 1.58 to 43.0 fishes per hectare. B. hirsutus demonstrates a strong preference for complex microhabitat features, such as depressions and ripple formations filled with biogenic substrates (e.g. shells) but avoids simple, low relief microhabitats (e.g. sand flats) and areas dominated by ephemeral, filamentous algae. Complex microhabitats may enable B. hirsutus to avoid predators, increase forage opportunities or provide higher quality spawning sites. This first wide-scale application of GUVC for B. hirsutus allowed us to survey a larger number of sites than previously possible to provide a robust reference point for future long-term monitoring.