A Global Systematic Literature Review of Ecosystem Services in Reef Environments.

Ecosystem services (ES) embrace contributions of nature to human livelihood and well-being. Reef environments provide a range of ES with direct and indirect contributions to people. However, the health of reef environments is declining globally due to local and large-scale threats, affecting ES delivery in different ways. Mapping scientific knowledge and identifying research gaps on reefs' ES is critical to guide their management and conservation. We conducted a systematic assessment of peer-reviewed articles published between 2007 and 2022 to build an overview of ES research on reef environments. We analyzed the geographical distribution, reef types, approaches used to assess ES, and the potential drivers of change in ES delivery reported across these studies. Based on 115 articles, our results revealed that coral and oyster reefs are the most studied reef ecosystems. Cultural ES (e.g., subcategories recreation and tourism) was the most studied ES in high-income countries, while regulating and maintenance ES (e.g., subcategory life cycle maintenance) prevailed in low and middle-income countries. Research efforts on reef ES are biased toward the Global North, mainly North America and Oceania. Studies predominantly used observational approaches to assess ES, with a marked increase in the number of studies using statistical modeling during 2021 and 2022. The scale of studies was mostly local and regional, and the studies addressed mainly one or two subcategories of reefs' ES. Overexploitation, reef degradation, and pollution were the most commonly cited drivers affecting the delivery of provisioning, regulating and maintenance, and cultural ES. With increasing threats to reef environments, the growing demand for assessing the contributions to humans provided by reefs will benefit the projections on how these ES will be impacted by anthropogenic pressures. The incorporation of multiple and synergistic ecosystem mechanisms is paramount to providing a comprehensive ES assessment, and improving the understanding of functions, services, and benefits.

Bold-shy personality traits of globally invasive, native and hatchery-reared fish.

Bold behaviour of non-native species is hypothesized to facilitate invasion success, yet extreme boldness in wild and domesticated animals can be maladaptive. The purpose of this study was to compare individual behaviour among Australian native hatchery-reared (n = 33) and wild (n = 38) Murray cod (Maccullochella peelii) with invasive common carp (Cyprinus carpio; n = 30). Three laboratory tests measured individual behaviour: (1) emergence from a shelter, (2) exploration of a novel environment, and (3) approaching a predator. Wild invasive carp and hatchery-reared cod were generally faster and more likely to emerge and explore novel environments when compared with wild Murray cod. The 'bold-type' behaviours of hatchery-reared native cod were more like invasive carp than they were to 'shy-type' wild conspecifics, yet an important difference was that hatchery-reared cod spent substantially more time near a large predator while carp rapidly escaped. We suggest that these results are consistent with a bold-type invasion syndrome in invasive carp and learned boldness of hatchery-reared Murray cod. The propensity of invasive carp to rapidly explore and enter new environments, along with a fast predator escape response may have been important to their invasion success, while extreme risk-taking and predator naivety of hatchery-reared Murray cod may exacerbate post-release mortality rates in fisheries and conservation stocking programmes.

Sex and male breeding state predict intraspecific trait variation in mouth-brooding fishes.

Sex-specific reproductive roles contribute to sexual dimorphic morphological trait variations. In uniparental mouth-brooding fishes, the mouth performs a reproductive function in addition to its key roles in feeding and respiration, resulting in the potential for sex-specific functional performance trade-offs. Trait differences related to parental care may occur when the individual matures or be restricted to periods when the parent is mouth-brooding. This study explored sexual dimorphism and morphological trait adaptations related to feeding, breeding, respiration and locomotion performance in two paternal mouth-brooding freshwater fishes (Glossamia aprion and Neoarius graeffei). Eight morphological traits were evaluated for sexual dimorphism (non-brooder males vs. females) and male breeding state differences (brooders vs. non-brooders). Male breeding state was a significant predictor of trait variation in both species. Brooders differed in buccal volume and in several feeding and locomotory traits compared to non-brooder males. Non-brooder males had bigger buccal volumes and relative eye diameters (G. aprion) and larger relative gape sizes (N. graeffei) compared to females, a potential response to both mouth-brooding and feeding requirements. Although there were clear trait differences between brooder and non-brooder males, further research is required to confirm whether individuals return to their former morphology once mouth-brooding has ceased or if trait differences are maintained post-brooding. This study highlights the importance of considering the potential impacts of intraspecific trait variation on the performance of critical life functions, such as feeding, respiration and locomotion across the life history.

Diverse parentage relationships in paternal mouthbrooding fishes.

While mouthbrooding is not an uncommon parental care strategy in fishes, paternal mouthbrooding only occurs in eight fish families and is little studied. The high cost of paternal mouthbrooding to the male implies a low risk of investment in another male's offspring but genetic parentage patterns are poorly known for paternal mouthbrooders. Here, we used single-nucleotide polymorphism genetic data to investigate parentage relationships of broods of two mouthbrooders of northern Australian rivers, mouth almighty Glossamia aprion and blue catfish Neoarius graeffei. For N. graeffei, we found that the parentage pattern was largely monogamous with the brooder male as the sire. For G. aprion, the parentage pattern was more heterogeneous including observations of monogamous broods with the brooder male as the sire (73%), polygyny (13%), cuckoldry (6%) and a brood genetically unrelated to the brooder male (6%). Findings demonstrate the potential for complex interrelationships of male care, paternity confidence and mating behaviour in mouthbrooding fishes.

Biological trade-offs underpin coral reef ecosystem functioning.

Human impact increasingly alters global ecosystems, often reducing biodiversity and disrupting the provision of essential ecosystem services to humanity. Therefore, preserving ecosystem functioning is a critical challenge of the twenty-first century. Coral reefs are declining worldwide due to the pervasive effects of climate change and intensive fishing, and although research on coral reef ecosystem functioning has gained momentum, most studies rely on simplified proxies, such as fish biomass. This lack of quantitative assessments of multiple process-based ecosystem functions hinders local and regional conservation efforts. Here we combine global coral reef fish community surveys and bioenergetic models to quantify five key ecosystem functions mediated by coral reef fishes. We show that functions exhibit critical trade-offs driven by varying community structures, such that no community can maximize all functions. Furthermore, functions are locally dominated by few species, but the identity of dominant species substantially varies at the global scale. In fact, half of the 1,110 species in our dataset are functionally dominant in at least one location. Our results reinforce the need for a nuanced, locally tailored approach to coral reef conservation that considers multiple ecological functions beyond the effect of standing stock biomass.

Protecting connectivity promotes successful biodiversity and fisheries conservation.

The global decline of coral reefs has led to calls for strategies that reconcile biodiversity conservation and fisheries benefits. Still, considerable gaps in our understanding of the spatial ecology of ecosystem services remain. We combined spatial information on larval dispersal networks and estimates of human pressure to test the importance of connectivity for ecosystem service provision. We found that reefs receiving larvae from highly connected dispersal corridors were associated with high fish species richness. Generally, larval "sinks" contained twice as much fish biomass as "sources" and exhibited greater resilience to human pressure when protected. Despite their potential to support biodiversity persistence and sustainable fisheries, up to 70% of important dispersal corridors, sinks, and source reefs remain unprotected, emphasizing the need for increased protection of networks of well-connected reefs.

Fish biodiversity of Saint Peter and Saint Paul's Archipelago, Mid-Atlantic Ridge, Brazil: new records and a species database.

Saint Peter and Saint Paul's Archipelago (SPSPA), one of the smallest and most isolated island groups in the world, is situated on the Mid-Atlantic Ridge, between Brazil and the African continent. SPSPA has low species richness and high endemism; nonetheless, the diversity of fishes from deep habitats (>30 m depth) had not been previously studied in detail. Several expeditions conducted between 2009 and 2018 explored the shallow and deep reefs of SPSPA using scuba, closed-circuit rebreathers, manned submersibles, baited remote underwater stereo-videos (stereo-BRUV) and fishing between 0 and 1050 m depth. These expeditions yielded 41 new records of fishes for SPSPA: 9 in open waters, 9 in shallow waters (0-30 m), 8 in mesophotic ecosystems (30-150 m) and 15 in deeper reefs (>150 m). Combined with literature records of adult pelagic, shallow and deep-reef species, as well as larvae, the database of the fish biodiversity for SPSPA currently comprises 225 species (169 recorded as adult fishes and 79 as larvae, with 23 species found in both stages). Most of them (112) are pelagic, 86 are reef-associated species and 27 are deep-water specialists. Species accumulation curves show that the number of fish species has not yet reached an asymptote. Whereas the number of species recorded in SPSPA is similar to that in other oceanic islands in the Atlantic Ocean, the proportion of shorefishes is relatively lower, and the endemism level is the third highest in the Atlantic. Twenty-nine species are listed as threatened with extinction. Observations confirm the paucity of top predators on shallow rocky reefs of the island, despite the presence of several pelagic shark species around SPSPA. Because all of the endemic species are reef associated, it is argued that the new marine-protected areas created by the Brazilian government do not ensure the protection and recovery of SPSPA's biodiversity because they allow exploitation of the most vulnerable species around the archipelago itself. This study suggests a ban on reef fish exploitation inside an area delimited by the 1000 m isobath around the islands (where all known endemics are concentrated) as the main conservation strategy to be included in the SPSPA management plan being prepared by the Brazilian government.

Climate-driven shift in coral morphological structure predicts decline of juvenile reef fishes.

Rapid intensification of environmental disturbances has sparked widespread decline and compositional shifts in foundation species in ecosystems worldwide. Now, an emergent challenge is to understand the consequences of shifts and losses in such habitat-forming species for associated communities and ecosystem processes. Recently, consecutive coral bleaching events shifted the morphological makeup of habitat-forming coral assemblages on the Great Barrier Reef (GBR). Considering the disparity of coral morphological growth forms in shelter provision for reef fishes, we investigated how shifts in the morphological structure of coral assemblages affect the abundance of juvenile and adult reef fishes. We used a temporal dataset from shallow reefs in the northern GBR to estimate coral convexity (a fine-scale quantitative morphological trait) and two widely used coral habitat descriptors (coral cover and reef rugosity) for disentangling the effects of coral morphology on reef fish assemblages. Changes in coral convexity, rather than live coral cover or reef rugosity, disproportionately affected juvenile reef fishes when compared to adults, and explained more than 20% of juvenile decline. The magnitude of this effect varied by fish body size with juveniles of small-bodied species showing higher vulnerability to changes in coral morphology. Our findings suggest that continued large-scale shifts in the relative abundance of morphological groups within coral assemblages are likely to affect population replenishment and dynamics of future reef fish communities. The different responses of juvenile and adult fishes according to habitat descriptors indicate that focusing on coarse-scale metrics alone may mask fine-scale ecological responses that are key to understand ecosystem functioning and resilience. Nonetheless, quantifying coral morphological traits may contribute to forecasting the structure of reef fish communities on novel reef ecosystems shaped by climate change.

Ecological impacts and management strategies for recreational diving: A review.

Recreational diving is an expanding branch of ecotourism that when poorly managed, may cause considerable impacts to benthic organisms. Such impacts become a matter of concern in popular diving destinations. A systematic literature review was used to verify the characteristics of divers who cause damage to reefs, the effects on benthic organisms, and the range of management interventions available. We describe the knowledge gaps, addressed challenges and propose solutions hoping to reach successful management of diving tourism industry. We identified three main challenges on recreational diving management frameworks and discussed actions to overcome such challenges. The challenges are related to (1) the lack of baseline data and long-term monitoring; (2) integration of scientific research and management; and (3) adaptive management strategies and stakeholder involvement.

Does a bigger mouth make you fatter? Linking intraspecific gape variability to body condition of a tropical predatory fish.

In gape-limited predators, gape size restricts the maximum prey size a predator is capable to ingest. However, studies investigating the energetic consequences of this relationship remain scarce. In this study, we tested the hypothesis that gape-size variability influences individual body condition (a common proxy for fitness) in one of the largest freshwater teleost predators, the barramundi. We found that individual barramundi with larger gapes relative to body size had higher body condition values compared to conspecifics with smaller gapes. Body condition was highest soon after the wet season, a period of high feeding activity on productive inundated floodplains, and body condition decreased as the dry season progressed when fish were restricted to dry season remnant habitats. The increased condition obtained during the wet season apparently offsets weight loss through the dry season, as individuals with large gapes were still in better condition than fish with small gapes in the late-dry season. Elucidation of the links between intraspecific variability in traits and performance is a critical challenge in functional ecology. This study emphasizes that even small intraspecific variability in morphological trait values can potentially affect individual fitness within a species' distribution.

Marine reserves shape seascapes on scales visible from space.

Marine reserves can effectively restore harvested populations, and 'mega-reserves' increasingly protect large tracts of ocean. However, no method exists of monitoring ecological responses at this large scale. Herbivory is a key mechanism structuring ecosystems, and this consumer-resource interaction's strength on coral reefs can indicate ecosystem health. We screened 1372, and measured features of 214, reefs throughout Australia's Great Barrier Reef using high-resolution satellite imagery, combined with remote underwater videography and assays on a subset, to quantify the prevalence, size and potential causes of 'grazing halos'. Halos are known to be seascape-scale footprints of herbivory and other ecological interactions. Here we show that these halo-like footprints are more prevalent in reserves, particularly older ones (approx. 40 years old), resulting in predictable changes to reef habitat at scales visible from space. While the direct mechanisms for this pattern are relatively clear, the indirect mechanisms remain untested. By combining remote sensing and behavioural ecology, our findings demonstrate that reserves can shape large-scale habitat structure by altering herbivores' functional importance, suggesting that reserves may have greater value in restoring ecosystems than previously appreciated. Additionally, our results show that we can now detect macro-patterns in reef species interactions using freely available satellite imagery. Low-cost, ecosystem-level observation tools will be critical as reserves increase in number and scope; further investigation into whether halos may help seems warranted. Significance statement: Marine reserves are a widely used tool to mitigate fishing impacts on marine ecosystems. Predicting reserves' large-scale effects on habitat structure and ecosystem functioning is a major challenge, however, because these effects unfold over longer and larger scales than most ecological studies. We use a unique approach merging remote sensing and behavioural ecology to detect ecosystem change within reserves in Australia's vast Great Barrier Reef. We find evidence of changes in reefs' algal habitat structure occurring over large spatial (thousands of kilometres) and temporal (40+ years) scales, demonstrating that reserves can alter herbivory and habitat structure in predictable ways. This approach demonstrates that we can now detect aspects of reefs' ecological responses to protection even in remote and inaccessible reefs globally.

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot.

For tropical marine species, hotspots of endemism occur in peripheral areas furthest from the center of diversity, but the evolutionary processes that lead to their origin remain elusive. We test several hypotheses related to the evolution of peripheral endemics by sequencing ultraconserved element (UCE) loci to produce a genome-scale phylogeny of 47 butterflyfish species (family Chaetodontidae) that includes all shallow water butterflyfish from the coastal waters of the Arabian Peninsula (i.e., Red Sea to Arabian Gulf) and their close relatives. Bayesian tree building methods produced a well-resolved phylogeny that elucidated the origins of butterflyfishes in this hotspots of endemism. We show that UCEs, often used to resolve deep evolutionary relationships, represent an important tool to assess the mechanisms underlying recently diverged taxa. Our analyses indicate that unique environmental conditions in the coastal waters of the Arabian Peninsula probably contributed to the formation of endemic butterflyfishes. Older endemic species are also associated with narrow versus broad depth ranges, suggesting that adaptation to deeper coral reefs in this region occurred only recently (<1.75 Ma). Even though deep reef environments were drastically reduced during the extreme low sea level stands of glacial ages, shallow reefs persisted, and as such there was no evidence supporting mass extirpation of fauna in this region.

Intraspecific morphological and reproductive trait variation in mouth almighty Glossamia aprion (Apogonidae) across different flow environments.

Intraspecific variability, although comparably less studied than interspecific variation, is an important tool in understanding population responses to environmental gradients. This study investigated intraspecific trait variation across three contrasting aquatic flow habitat types (intermittent creek, billabong and river) in a common mouth-brooding freshwater fish in northern Australia, the mouth almighty Glossamia aprion. Samples of G. aprion were collected at various sites, within the Daly River catchment. It was predicted that a number of morphological and reproductive traits would vary among individuals across the contrasting habitats. Five out of the nine morphological and reproductive traits studied significantly varied across flow habitat types. Significant intraspecific variation in functional traits related to foraging and reproduction, such as relative eye size, eye vertical position and relative maxillary length in males suggest that the inherent characteristics of each flow habitat type could be exerting selective pressure on the morphology of G. aprion. Interestingly, traits related to swimming performance (body lateral shape) and manoeuvrability (pectoral fin ventral position) differed between flow habitat types but showed inconsistent responses to predictions. Whilst this study was temporally and spatially limited, it highlights that intraspecific variability in morphological traits can occur among flow habitat types over relatively small spatial scales.

Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs.

The rapid degradation of coral reefs is one of the most serious biodiversity problems facing our generation. Mesophotic coral reefs (at depths of 30 to 150 meters) have been widely hypothesized to provide refuge from natural and anthropogenic impacts, a promise for the survival of shallow reefs. The potential role of mesophotic reefs as universal refuges is often highlighted in reef conservation research. This hypothesis rests on two assumptions: (i) that there is considerable overlap in species composition and connectivity between shallow and deep populations and (ii) that deep reefs are less susceptible to anthropogenic and natural impacts than their shallower counterparts. Here we present evidence contradicting these assumptions and argue that mesophotic reefs are distinct, impacted, and in as much need of protection as shallow coral reefs.

Corrigendum: The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

This corrects the article DOI: 10.1038/sdata.2016.17.

The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism's function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.

Ecological and morphological traits predict depth-generalist fishes on coral reefs.

Ecological communities that occupy similar habitats may exhibit functional convergence despite significant geographical distances and taxonomic dissimilarity. On coral reefs, steep gradients in key environmental variables (e.g. light and wave energy) restrict some species to shallow depths. We show that depth-generalist reef fishes are correlated with two species-level traits: caudal fin aspect ratio and diet. Fishes with high aspect ratio (lunate) caudal fins produce weaker vortices in the water column while swimming, and we propose that 'silent swimming' reduces the likelihood of detection and provides an advantage on deeper reefs with lower light irradiance and water motion. Significant differences in depth preference among trophic guilds reflect variations in the availability of different food sources along a depth gradient. The significance of these two traits across three geographically and taxonomically distinct assemblages suggests that deep-water habitats exert a strong environmental filter on coral reef-fish assemblages.

Recreational Diver Behavior and Contacts with Benthic Organisms in the Abrolhos National Marine Park, Brazil.

In the last two decades, coral reefs have become popular among recreational divers, especially inside marine protected areas. However, the impact caused by divers on benthic organisms may be contributing to the degradation of coral reefs. We analyzed the behavior of 142 scuba divers in the Abrolhos National Marine Park, Brazil. We tested the effect of diver profile, reef type, use of additional equipment, timing, and group size on diver behavior and their contacts with benthic organisms. Eighty-eight percent of divers contacted benthic organism at least once, with an average of eight touches and one damage per dive. No significant differences in contacts were verified among gender, group size, or experience level. Artificial reef received a higher rate of contact than pinnacle and fringe reefs. Specialist photographers and sidemount users had the highest rates, while non-users of additional equipment and mini camera users had the lowest contact rates. The majority of contacts were incidental and the highest rates occurred in the beginning of a dive. Our findings highlight the need of management actions, such as the provision of pre-dive briefing including ecological aspects of corals and beginning dives over sand bottoms or places with low coral abundance. Gathering data on diver behavior provides managers with information that can be used for tourism management.