The evolution of fast-growing coral reef fishes.

Individual growth is a fundamental life history trait1-4, yet its macroevolutionary trajectories have rarely been investigated for entire animal assemblages. Here we analyse the evolution of growth in a highly diverse vertebrate assemblage-coral reef fishes. We combine state-of-the-art extreme gradient boosted regression trees with phylogenetic comparative methods to detect the timing, number, location and magnitude of shifts in the adaptive regime of somatic growth. We also explored the evolution of the allometric relationship between body size and growth. Our results show that the evolution of fast growth trajectories in reef fishes has been considerably more common than the evolution of slow growth trajectories. Many reef fish lineages shifted towards faster growth and smaller body size evolutionary optima in the Eocene (56-33.9 million years ago), pointing to a major expansion of life history strategies in this Epoch. Of all lineages examined, the small-bodied, high-turnover cryptobenthic fishes shifted most towards extremely high growth optima, even after accounting for body size allometry. These results suggest that the high global temperatures of the Eocene5 and subsequent habitat reconfigurations6 might have been critical for the rise and retention of the highly productive, high-turnover fish faunas that characterize modern coral reef ecosystems.

Small predators dominate fish predation in coral reef communities.

Ecosystem processes are challenging to quantify at a community level, particularly within complex ecosystems (e.g., rainforests, coral reefs). Predation is one of the most important types of species interactions, determining several ecosystem processes. However, while it is widely recognised, it is rarely quantified, especially in aquatic systems. To address these issues, we model predation on fish by fish, in a hyperdiverse coral reef community. We show that body sizes previously examined in fish-fish predation studies (based on a metanalysis), only represent about 5% of likely predation events. The average fish predator on coral reefs is just 3.65 cm; the average fish prey just 1.5 cm. These results call for a shift in the way we view fish predation and its ability to shape the species or functional composition of coral reef fish communities. Considered from a functional group approach, we found general agreement in the distribution of simulated and observed predation events, among both predator and prey functional groups. Predation on coral reefs is a process driven by small fish, most of which are neither seen nor quantified.

Natural recovery of corals after severe disturbance.

Ecosystem recovery from human-induced disturbances, whether through natural processes or restoration, is occurring worldwide. Yet, recovery dynamics, and their implications for broader ecosystem management, remain unclear. We explored recovery dynamics using coral reefs as a case study. We tracked the fate of 809 individual coral recruits that settled after a severe bleaching event at Lizard Island, Great Barrier Reef. Recruited Acropora corals, first detected in 2020, grew to coral cover levels that were equivalent to global average coral cover within just 2 years. Furthermore, we found that just 11.5 Acropora recruits per square meter were sufficient to reach this cover within 2 years. However, wave exposure, growth form and colony density had a marked effect on recovery rates. Our results underscore the importance of considering natural recovery in management and restoration and highlight how lessons learnt from reef recovery can inform our understanding of recovery dynamics in high-diversity climate-disturbed ecosystems.

Spatial subsidies drive sweet spots of tropical marine biomass production.

Spatial subsidies increase local productivity and boost consumer abundance beyond the limits imposed by local resources. In marine ecosystems, deeper water and open ocean subsidies promote animal aggregations and enhance biomass that is critical for human harvesting. However, the scale of this phenomenon in tropical marine systems remains unknown. Here, we integrate a detailed assessment of biomass production in 3 key locations, spanning a major biodiversity and abundance gradient, with an ocean-scale dataset of fish counts to predict the extent and magnitude of plankton subsidies to fishes on coral reefs. We show that planktivorous fish-mediated spatial subsidies are widespread across the Indian and Pacific oceans and drive local spikes in biomass production that can lead to extreme productivity, up to 30 kg ha-1 day-1. Plankton subsidies form the basis of productivity "sweet spots" where planktivores provide more than 50% of the total fish production, more than all other trophic groups combined. These sweet spots operate at regional, site, and smaller local scales. By harvesting oceanic productivity, planktivores bypass spatial constraints imposed by local primary productivity, creating "oases" of tropical fish biomass that are accessible to humans.

Planktivores as trophic drivers of global coral reef fish diversity patterns.

One of the most prominent features of life on Earth is the uneven number of species across large spatial scales. Despite being inherently linked to energetic constraints, these gradients in species richness distribution have rarely been examined from a trophic perspective. Here we dissect the global diversity of over 3,600 coral reef fishes to reveal patterns across major trophic groups. By analyzing multiple nested spatial scales, we show that planktivores contribute disproportionally to the formation of the Indo-Australian Archipelago (IAA) marine biodiversity hotspot. Besides being "hotter" at the hotspot, planktivorous fishes display the steepest decline in species numbers with distance from the IAA when compared to other trophic groups. Surprisingly, we did not detect differences in diversification, transition, and dispersal rates in extant species phylogenies that would explain this remarkable gradient in planktivorous fish richness. Thus, we identify two potential complementary drivers for this pattern. First, exceptional levels of partitioning among planktivorous coral reef fishes were driven by temporally stable oceanographic conditions and abundant planktonic resources in the IAA. Second, extinctions of planktivores outside the IAA have been particularly pronounced during Quaternary climate fluctuations. Overall, our results highlight trophic ecology as an important component of global species richness gradients.

On the evolution of fish-coral interactions.

The biodiversity of tropical reefs is typified by the interaction between fishes and corals. Despite the importance of this ecological association, coevolutionary patterns between these two animal groups have yet to be critically evaluated. After compiling a large dataset on the prevalence of fish-coral interactions, we found that only a minority of fish species associate strongly with live corals (~5%). Furthermore, we reveal an evolutionary decoupling between fish and coral lineage trajectories. While fish lineages expanded in the Miocene, the bulk of coral diversification occurred in the Pliocene/Pleistocene. Most importantly, we found that coral association did not drive major differences in fish diversification. These results suggest that the Miocene fish diversification is more likely related to the development of novel, wave-resistant reef structures and their associated ecological opportunities. Macroevolutionary patterns in reef fishes are thus more strongly correlated with the expansion of reefs than with the corals themselves.

On the Challenges of Identifying Benthic Dominance on Anthropocene Coral Reefs.

The concept of dominance is frequently used to describe changes in rapidly reconfiguring ecosystems, but the definition of dominance can vary widely among studies. Using coral reefs as a model, we use extensive benthic composition data to explore how variability in applying dominance concepts can shape perceptions. We reveal that coral dominance is sensitive to the exclusion of key algal groups and the categorization of other benthic groups, with ramifications for detecting an ecosystem phase shift. For example, ignoring algal turf inflates the dominance of hard and soft corals in the benthic habitats underpinning reef ecosystems. We need a consensus on how dominance concepts are applied so that we can build a more comprehensive understanding of ecosystem shifts across a broad range of aquatic and terrestrial settings. For reefs, we highlight the benefits of comprehensive and inclusive surveys for evaluating and managing the altered ecosystem states that are emerging in the Anthropocene.

Broad-scale analysis of fish community data suggests critical need to support regional connectivity of coral reefs.

Connectivity is vital for the biodiversity and functioning of marine ecosystems. It is known to be important for coral reefs, but the scales at which connectivity effects matter-and, correspondingly, the scales at which management responses are needed-are poorly understood in marine systems. We used 23 years of fish monitoring data collected from ~50 different coral reefs by the Australian Institute of Marine Science, together with a range of geographic data layers (including the Allen Coral Atlas) and additional network analysis, to explore the balance of local and regional influence on fish communities. Variance partitioning indicated that 42% of the variance in fish community composition could be explained by regional effects or their interaction with coarse-grained local influences (habitat). The variance explained by regional influences was divided evenly between measures that capture location on environmental gradients (e.g., proximity to coastal shelf, latitude) and cross-scale centrality measures of reef location within a broader reef network. A total of 11% of variance could be directly or indirectly attributed to management. Our results provide clear evidence that management and restoration of reefs across the globe must consider both local and regional influences on reef-associated organisms and highlight the potential benefits of improving connectivity in human-dominated coastal seascapes.

Coral reefs in the Anthropocene.

Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.

Global warming and recurrent mass bleaching of corals.

During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Research priorities for the sustainability of coral-rich western Pacific seascapes.

Nearly a billion people depend on tropical seascapes. The need to ensure sustainable use of these vital areas is recognised, as one of 17 policy commitments made by world leaders, in Sustainable Development Goal (SDG) 14 ('Life below Water') of the United Nations. SDG 14 seeks to secure marine sustainability by 2030. In a time of increasing social-ecological unpredictability and risk, scientists and policymakers working towards SDG 14 in the Asia-Pacific region need to know: (1) How are seascapes changing? (2) What can global society do about these changes? and (3) How can science and society together achieve sustainable seascape futures? Through a horizon scan, we identified nine emerging research priorities that clarify potential research contributions to marine sustainability in locations with high coral reef abundance. They include research on seascape geological and biological evolution and adaptation; elucidating drivers and mechanisms of change; understanding how seascape functions and services are produced, and how people depend on them; costs, benefits, and trade-offs to people in changing seascapes; improving seascape technologies and practices; learning to govern and manage seascapes for all; sustainable use, justice, and human well-being; bridging communities and epistemologies for innovative, equitable, and scale-crossing solutions; and informing resilient seascape futures through modelling and synthesis. Researchers can contribute to the sustainability of tropical seascapes by co-developing transdisciplinary understandings of people and ecosystems, emphasising the importance of equity and justice, and improving knowledge of key cross-scale and cross-level processes, feedbacks, and thresholds.

Are fish communities on coral reefs becoming less colourful?

An organism's colouration is often linked to the environment in which it lives. The fishes that inhabit coral reefs are extremely diverse in colouration, but the specific environmental factors that support this extreme diversity remain unclear. Interestingly, much of the aesthetic and intrinsic value humans place on coral reefs (a core ecosystem service they provide) is based on this extreme diversity of colours. However, like many processes on coral reefs, the relationship between colouration and the environment is likely to be impacted by global environmental change. Using a novel community-level measure of fish colouration, as perceived by humans, we explore the potential links between fish community colouration and the environment. We then asked if this relationship is impacted by human-induced environmental disturbances, e.g. mass coral bleaching events, using a community-level dataset spanning 27 years on the Great Barrier Reef. We found that the diversity of colours found within a fish community is directly related to the composition of the local environment. Areas with a higher cover of structurally complex corals contained fish species with more diverse and brighter colourations. Most notably, fish community colouration contracted significantly in the years following the 1998 global coral bleaching event. Fishes with colouration directly appealing to human aesthetics are becoming increasingly rare, with the potential for marked declines in the perceived colour of reef fish communities in the near future. Future reefs may not be the colourful ecosystems we recognize today, representing the loss of a culturally significant ecosystem service.

Rising from the Ashes: The Biogeographic Origins of Modern Coral Reef Fishes.

During the excavation of Mayan tombs, little did the archaeologists know that the fossils they discovered in the tomb stones would fundamentally alter our understanding of the earliest origins of coral reef fishes. Located just 500 kilometers from the point where an asteroid impact reconfigured the world's biological systems 66 million years ago, we find the earliest origins of three typical reef fish groups. Their presence in Mexico just 3 million years after this impact finally reconciles the conflict between the fossil and phylogenetic evidence for the earliest origins of reef fishes. The incorporation of these fossils into a global reconstruction of fish evolutionary history reveals a new picture of the early biogeography of reef fishes, with strong Atlantic links. From locations associated with biological destruction and societal collapse, we see evidence of the origins of one of the world's most diverse and spectacular marine ecosystems: coral reefs.

Collapsing ecosystem functions on an inshore coral reef.

Ecosystem functions underpin productivity and key services to humans, such as food provision. However, as the severity of environmental stressors intensifies, it is becoming increasingly unclear if, and to what extent, critical functions and services can be sustained. This issue is epitomised on coral reefs, an ecosystem at the forefront of environmental transitions. We provide a functional profile of a coral reef ecosystem, linking time-series data to quantified processes. The data reveal a prolonged collapse of ecosystem functions in this previously resilient system. The results suggest that sediment accumulation in algal turfs has led to a decline in resource yields to herbivorous fishes and a decrease in fish-based ecosystem functions, including a collapse of both fish biomass and productivity. Unfortunately, at present, algal turf sediment accumulation is rarely monitored nor managed in coral reef systems. Our examination of functions through time highlights the value of directly assessing functions, their potential vulnerability, and the capacity of algal turf sediments to overwhelm productive high-diversity coral reef ecosystems.

Human exploitation shapes productivity-biomass relationships on coral reefs.

Coral reef fisheries support the livelihoods of millions of people in tropical countries, despite large-scale depletion of fish biomass. While human adaptability can help to explain the resistance of fisheries to biomass depletion, compensatory ecological mechanisms may also be involved. If this is the case, high productivity should coexist with low biomass under relatively high exploitation. Here we integrate large spatial scale empirical data analysis and a theory-driven modelling approach to unveil the effects of human exploitation on reef fish productivity-biomass relationships. We show that differences in how productivity and biomass respond to overexploitation can decouple their relationship. As size-selective exploitation depletes fish biomass, it triggers increased production per unit biomass, averting immediate productivity collapse in both the modelling and the empirical systems. This 'buffering productivity' exposes the danger of assuming resource production-biomass equivalence, but may help to explain why some biomass-depleted fish assemblages still provide ecosystem goods under continued global fishing exploitation.

Trophic separation in planktivorous reef fishes: a new role for mucus?

The feeding apparatus directly influences a species' trophic ecology. In fishes, our understanding of feeding modes is largely derived from studies of rigid structures (i.e. bones, teeth, gill rakers). A recently described lip innovation, however, highlighted the role of soft anatomy in enabling specialized feeding modes. In this study, we explore whether similar diversification may also occur in the soft anatomy of the buccal cavity. Using four key anatomical traits to classify 19 species (14 genera) of wrasses, we evaluated the relationship between anatomical specialization of the buccal cavity and diet. Our data revealed a previously undocumented anatomical adaptation in the mouths of fairy wrasses (Cirrhilabrus): the mucosa throughout the buccal cavity (i.e. anterior to the pharynx) is packed with goblet cells, enabling it to secrete large quantities of mucus in this region; a new trait that, until now, had not been documented in wrasses. This disparity reflects diet differences, with mucus secretion found only in planktivorous Cirrhilabrus that feed predominantly on amorphous organic material (potentially gelatinous organisms). This suggests a cryptic mucus-based resource partitioning in planktivorous wrasses.

Colour pattern divergence in reef fish species is rapid and driven by both range overlap and symmetry.

Signal divergence is an important process underpinning the diversification of lineages. Research has shown that signal divergence is greatest in species pairs that possess high geographic range overlap. However, the influence of range-size differences within pairs is less understood. We investigated how these factors have shaped signal divergence within brightly coloured coral reef butterflyfishes (genus: Chaetodon). Using a novel digital imaging methodology, we quantified both colouration and pattern using 250 000 sample points on each fish image. Surprisingly, evolutionary age did not affect colour pattern dissimilarity between species pairs, with average differences arising in just 300 000 years. However, the effect of range overlap and range symmetry was significant. Species-pair colour patterns become more different with increasing overlap, but only when ranges are similar in size. When ranges differ markedly in area, species-pair colour patterns become more similar with increasing overlap. This suggests that species with small ranges may maintain non-colour-based species boundaries.

The evolution of traits and functions in herbivorous coral reef fishes through space and time.

Herbivory by fishes has been identified as a key ecological process shaping coral reefs through time. Although taxonomically limited, herbivorous reef fishes display a wide range of traits, which results in varied ecosystem functions on reefs around the world. Yet, we understand little about how these trait combinations and functions in ecosystems changed through time and across biogeographic realms. Here, we used fossils and phylogenies in a functional ecological framework to reveal temporal changes in nominally herbivorous fish assemblages among oceanic basins in both trait space and lineage richness among functions. We show that the trait space occupied by extant herbivorous fishes in the Indo-Pacific resulted from an expansion of traits from the ancestral Tethyan assemblages. By contrast, trait space in the Atlantic is the result of lineage turnover, with relatively recent colonization by lineages that arose in the east Tethys/Indo-Pacific. From an ecosystem function perspective, the Atlantic supports a depauperate fauna, with few extant herbivorous reef fish lineages performing each function. Indo-Pacific fishes support both more functions and more lineages within each function, with a marked Miocene to Pleistocene expansion. These disparities highlight the importance of history in explaining global variation in fish functional composition on coral reefs.

Phylogenetics and geography of speciation in New World Halichoeres wrasses.

The New World Halichoeres comprises about 30 small to medium sized wrasse species that are prominent members of reef communities throughout the tropical Western Atlantic and Eastern Pacific. We conducted a phylogenetic analysis of this group and related lineages using new and previously published sequence data. We estimated divergence times, evaluated the monophyly of this group, their relationship to other labrids, as well as the time-course and geography of speciation. These analyses show that all members of New World Halichoeres form a monophyletic group that includes Oxyjulis and Sagittalarva. New World Halichoeres is one of numerous labrid groups that appear to have radiated rapidly about 32 Ma and form a large polytomy within the julidine wrasses. We reconstruct the tropical Western Atlantic to be the ancestral area of New World Halichoeres, with four invasions of the Eastern Pacific and one reversal from East Pacific to Western Atlantic. These five speciation events were spread across the history of the group, with none corresponding closely to the time of the closure of the Isthmus of Panama. Three speciation events within the Atlantic occurred across the Orinoco-Amazon outflow and within the Pacific, five involve splits between lineages that occupy coastal reef systems and offshore islands. Of eight sister species pairs, seven show complete allopatry and one is fully sympatric.

A unified model explains commonness and rarity on coral reefs.

Abundance patterns in ecological communities have important implications for biodiversity maintenance and ecosystem functioning. However, ecological theory has been largely unsuccessful at capturing multiple macroecological abundance patterns simultaneously. Here, we propose a parsimonious model that unifies widespread ecological relationships involving local aggregation, species-abundance distributions, and species associations, and we test this model against the metacommunity structure of reef-building corals and coral reef fishes across the western and central Pacific. For both corals and fishes, the unified model simultaneously captures extremely well local species-abundance distributions, interspecific variation in the strength of spatial aggregation, patterns of community similarity, species accumulation, and regional species richness, performing far better than alternative models also examined here and in previous work on coral reefs. Our approach contributes to the development of synthetic theory for large-scale patterns of community structure in nature, and to addressing ongoing challenges in biodiversity conservation at macroecological scales.