Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

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.

Morphological predictors of swimming speed performance in river and reservoir populations of Australian smelt Retropinna semoni.

Dam construction is a major driver of ecological change in freshwater ecosystems. Fish populations have been shown to diverge in response to different flow velocity habitats, yet adaptations of fish populations to river and reservoir habitats created by dams remains poorly understood. We aimed to evaluate divergence of morphological traits and prolonged swimming speed performance between lotic and lentic populations of Australian smelt Retropinna semoni and quantify the relationship between prolonged swimming speed performance and morphology. Prolonged swimming speed performance was assessed for 15 individuals from each of three river and two reservoir populations of R. semoni using the critical swimming speed test (Ucrit ). Body shape was characterized using geometric morphometrics, which was combined with fin aspect ratios and standard length to assess morphological divergence among the five populations. Best subsets model-selection was used to identify the morphological traits that best explain Ucrit variation among individuals. Our results indicate R. semoni from river populations had significantly higher prolonged swimming speed performance (Ucrit = 46.61 ± 0.98 cm s-1 ) than reservoir conspecifics (Ucrit = 35.57 ± 0.83 cm s-1 ; F1,74 = 58.624, Z = 35.938, P < 0.001). Similarly, R. semoni sampled from river populations had significantly higher fin aspect ratios (ARcaudal = 1.71 ± 0.04 and 1.29 ± 0.02 respectively; F(1,74) = 56.247, Z = 40.107, P < 0.001; ARpectoral = 1.85 ± 0.03 and 1.33 ± 0.02 respectively; F(1,74) = 7.156, Z = 4.055, P < 0.01). Best-subset analyses revealed Ucrit was most strongly correlated with pectoral and caudal fin aspect ratios (R2 adj = 0.973, AICc = 41.54). Body shape, however, was subject to a three-way interaction among population, habitat and sex effects (F3,74 = 1.038. Z = 1.982; P < 0.05). Thus sexual dimorphism formed a significant component of unique and complex variation in body shape among populations from different habitat types. This study revealed profound effects of human-altered flow environments on locomotor morphology and its functional link to changes in swimming performance of a common freshwater fish. While past studies have indicated body shape may be an important axis for divergence between lotic and lentic populations of several freshwater fishes, fin aspect ratios were the most important predictor of swimming speed in our study. Differences in body morphology here were inconsistent between river and reservoir populations, suggesting this aspect of phenotype may be more strongly influenced by other factors such as predation and sexual dimorphism.

Ecological Release from Aquatic Predation Is Associated with the Emergence of Marine Blenny Fishes onto Land.

An ecological release from competition or predation is a frequent adaptive explanation for the colonization of novel environments, but empirical data are limited. On the island of Rarotonga, several blenny fish species appear to be in the process of colonizing land. Anecdotal observations have implied that aquatic predation is an important factor in prompting such amphibious fish behavior. We provide evidence supporting this hypothesis by demonstrating that amphibious blennies shift their abundance up and down the shoreline to remain above predatory fishes that periodically move into intertidal areas during high tide. A predation experiment using blenny mimics confirmed a high risk of aquatic predation for blennies, significantly higher than predation experienced on land. These data suggest that predation has played an active role in promoting terrestrial activity in amphibious blennies and provide a rare example of how ecological release from predation could drive the colonization of a novel environment.

Influence of nursery microhabitats on the future abundance of a coral reef fish.

Species habitat associations are often complex, making it difficult to assess their influence on populations. Among coral reef fishes, habitat requirements vary among species and with ontogeny, but the relative importance of nursery and adult-preferred habitats on future abundances remain unclear. Moreover, adult populations may be influenced by recruitment of juveniles and assessments of habitat importance should consider relative effects of juvenile abundance. We conducted surveys across 16 sites and 200 km of reef to identify the microhabitat preferences of juveniles, sub-adults and adults of the damselfish Pomacentrus moluccensis Microhabitat preferences at different life-history stages were then combined with 6 years of juvenile abundance and microhabitat availability data to show that the availability of preferred juvenile microhabitat (corymbose corals) at the time of settlement was a strong predictor of future sub-adult and adult abundance. However, the influence of nursery microhabitats on future population size differed spatially and at some locations abundance of juveniles and adult microhabitat (branching corals) were better predictors of local populations. Our results demonstrate that while juvenile microhabitats are important nurseries, the abundance of coral-dependent fishes is not solely dependent on these microhabitats, especially when microhabitats are readily available or following large influxes of juveniles.

Localised intraspecific variation in the swimming phenotype of a coral reef fish across different wave exposures.

Wave-driven water flow is a major force structuring marine communities. Species distributions are partly determined by the ability to cope with variation in water flow, such as differences in the assemblage of fish species found in a given water flow environment being linked to swimming ability (based on fin shape and mode of locomotion). It remains unclear, however, whether similar assembly rules apply within a species. Here we show phenotypic variation among sites in traits functionally linked to swimming ability in the damselfish Acanthochromis polyacanthus. These sites differ in wave energy and the observed patterns of phenotypic differences within A. polyacanthus closely mirrored those seen at the interspecific level. Fish from high-exposure sites had more tapered fins and higher maximum metabolic rates than conspecifics from sheltered sites. This translates to a 36% larger aerobic scope and 33% faster critical swimming speed for fish from exposed sites. Our results suggest that functional relationships among swimming phenotypes and water flow not only structure species assemblages, but can also shape patterns of phenotypic divergence within species. Close links between locomotor phenotype and local water flow conditions appear to be important for species distributions as well as phenotypic divergence across environmental gradients.

Can juvenile supply predict future abundance of large-bodied reef fishes?

The extent to which juvenile abundance can predict future populations of lethrinids at Ningaloo Reef was assessed using size frequency data collected over 13 consecutive years. Annual abundance of juvenile lethrinids (<5 cm TL) was highest in northern Ningaloo during La Niña years, when seawater is warmer and oceanic currents stronger. Juvenile lethrinid abundance explained 35% of the variance in 1-2 year-old Lethrinus nebulosus abundance the following year, a steeper relationship in the north suggesting greater survival of juveniles. Juvenile lethrinid abundance was also positively correlated to abundance of 1-2 year-old L. atkinsoni in the southern region of Ningaloo. Abundance of juvenile lethrinids were however poor predictors of L. nebulosus and L. atkinsoni older than 2 years of age. Post settlement processes likely weaken the link between juvenile supply and abundance of lethrinids >2 years old making it difficult to accurately quantify the overall size of future lethrinid populations.

Combining stereo-video monitoring and physiological trials to estimate reef fish metabolic demands in the wild.

Organismal metabolic rates (MRs) are the basis of energy and nutrient fluxes through ecosystems. In the marine realm, fishes are some of the most prominent consumers. However, their metabolic demand in the wild (field MR [FMR]) is poorly documented, because it is challenging to measure directly. Here, we introduce a novel approach to estimating the component of FMR associated with voluntary activity (i.e., the field active MR [ AM R field ] ). Our approach combines laboratory-based respirometry, swimming speeds, and field-based stereo-video systems to estimate the activity of individuals. We exemplify our approach by focusing on six coral reef fish species, for which we quantified standard MR and maximum MR (SMR and MMR, respectively) in the laboratory, and body sizes and swimming speeds in the field. Based on the relationships between MR, body size, and swimming speeds, we estimate that the activity scope (i.e., the ratio between AM R field and SMR) varies from 1.2 to 3.2 across species and body sizes. Furthermore, we illustrate that the scaling exponent for AM R field varies across species and can substantially exceed the widely assumed value of 0.75 for SMR. Finally, by scaling organismal AM R field estimates to the assemblage level, we show the potential effect of this variability on community metabolic demand. Our approach may improve our ability to estimate elemental fluxes mediated by a critically important group of aquatic animals through a non-destructive, widely applicable technique.

The role of the reef flat in coral reef trophodynamics: Past, present, and future.

The reef flat is one of the largest and most distinctive habitats on coral reefs, yet its role in reef trophodynamics is poorly understood. Evolutionary evidence suggests that reef flat colonization by grazing fishes was a major innovation that permitted the exploitation of new space and trophic resources. However, the reef flat is hydrodynamically challenging, subject to high predation risks and covered with sediments that inhibit feeding by grazers. To explore these opposing influences, we examine the Great Barrier Reef (GBR) as a model system. We focus on grazing herbivores that directly access algal primary productivity in the epilithic algal matrix (EAM). By assessing abundance, biomass, and potential fish productivity, we explore the potential of the reef flat to support key ecosystem processes and its ability to maintain fisheries yields. On the GBR, the reef flat is, by far, the most important habitat for turf-grazing fishes, supporting an estimated 79% of individuals and 58% of the total biomass of grazing surgeonfishes, parrotfishes, and rabbitfishes. Approximately 59% of all (reef-wide) turf algal productivity is removed by reef flat grazers. The flat also supports approximately 75% of all grazer biomass growth. Our results highlight the evolutionary and ecological benefits of occupying shallow-water habitats (permitting a ninefold population increase). The acquisition of key locomotor and feeding traits has enabled fishes to access the trophic benefits of the reef flat, outweighing the costs imposed by water movement, predation, and sediments. Benthic assemblages on reefs in the future may increasingly resemble those seen on reef flats today, with low coral cover, limited topographic complexity, and extensive EAM. Reef flat grazing fishes may therefore play an increasingly important role in key ecosystem processes and in sustaining future fisheries yields.

Climatic forcing and larval dispersal capabilities shape the replenishment of fishes and their habitat-forming biota on a tropical coral reef.

Fluctuations in marine populations often relate to the supply of recruits by oceanic currents. Variation in these currents is typically driven by large-scale changes in climate, in particular ENSO (El Nino Southern Oscillation). The dependence on large-scale climatic changes may, however, be modified by early life history traits of marine taxa. Based on eight years of annual surveys, along 150 km of coastline, we examined how ENSO influenced abundance of juvenile fish, coral spat, and canopy-forming macroalgae. We then investigated what traits make populations of some fish families more reliant on the ENSO relationship than others. Abundance of juvenile fish and coral recruits was generally positively correlated with the Southern Oscillation Index (SOI), higher densities recorded during La Niña years, when the ENSO-influenced Leeuwin Current is stronger and sea surface temperature higher. The relationship is typically positive and stronger among fish families with shorter pelagic larval durations and stronger swimming abilities. The relationship is also stronger at sites on the coral back reef, although the strongest of all relationships were among the lethrinids (r = .9), siganids (r = .9), and mullids (r = .8), which recruit to macroalgal meadows in the lagoon. ENSO effects on habitat seem to moderate SOI-juvenile abundance relationship. Macroalgal canopies are higher during La Niña years, providing more favorable habitat for juvenile fish and strengthening the SOI effect on juvenile abundance. Conversely, loss of coral following a La Niña-related heat wave may have compromised postsettlement survival of coral dependent species, weakening the influence of SOI on their abundance. This assessment of ENSO effects on tropical fish and habitat-forming biota and how it is mediated by functional ecology improves our ability to predict and manage changes in the replenishment of marine populations.

Global ecological success of Thalassoma fishes in extreme coral reef habitats.

Phenotypic adaptations can allow organisms to relax abiotic selection and facilitate their ecological success in challenging habitats, yet we have relatively little data for the prevalence of this phenomenon at macroecological scales. Using data on the relative abundance of coral reef wrasses and parrotfishes (f. Labridae) spread across three ocean basins and the Red Sea, we reveal the consistent global dominance of extreme wave-swept habitats by fishes in the genus Thalassoma, with abundances up to 15 times higher than any other labrid. A key locomotor modification-a winged pectoral fin that facilitates efficient underwater flight in high-flow environments-is likely to have underpinned this global success, as numerical dominance by Thalassoma was contingent upon the presence of high-intensity wave energy. The ecological success of the most abundant species also varied with species richness and the presence of congeneric competitors. While several fish taxa have independently evolved winged pectoral fins, Thalassoma appears to have combined efficient high-speed swimming (to relax abiotic selection) with trophic versatility (to maximize exploitation of rich resources) to exploit and dominate extreme coral reef habitats around the world.

All in the ears: unlocking the early life history biology and spatial ecology of fishes.

Obtaining biological and spatial information of the early life history (ELH) phases of fishes has been problematic, such that larval and juvenile phases are often referred to as the 'black box' of fish population biology and ecology. However, a potent source of life-history data has been mined from the earstones (otoliths) of bony fishes. We systematically reviewed 476 empirical papers published between 2005 and 2012 (inclusive) that used otoliths to examine fish ELH phases, which has been an area of increasing attention over this period. We found that otolith-based research during this period could be split into two broad themes according to whether studies examined: (i) biological objectives related to intrinsic processes such as larval and juvenile age, growth and mortality, and/or (ii) spatial objectives, such as habitat use, dispersal and migration. Surprisingly, just 24 studies (5%) explored a combined biological-spatial objective by simultaneously exploiting biological and spatial information from otoliths, suggesting much more scope for such integrated research objectives to be answered via the use of multiple otolith-based techniques in a single study. Mapping otolith analytical techniques across these two approaches revealed that otolith structural analysis was mainly used to investigate biological processes, while otolith chemical analyses were most often applied to spatial questions. Heavy skew in research effort was apparent across biomes, with most (62%) publications specific to marine species, despite comparable levels of species richness and the importance of freshwater taxa (just 15% of papers). Indeed, around 1% (380 species) of a possible 31400+ extant species were examined in our surveyed papers, with a strong emphasis on temperate marine species of commercial value. Potential model species for otolith-based ELH ecology research are arising, with the eel genus Anguilla (24 studies) and the European anchovy Engraulis encrasicolis (14 studies) attracting more research effort than most other taxa. While there is a preponderance of common techniques (e.g. daily otolith increment counts, increment widths), novel techniques such as transgenerational marking and computed X-ray tomography, are increasingly being applied in published studies. The application of an integrative approach based on a combination of emerging techniques and traditional methods holds promise for major advances in our understanding of ELH fish ecology and to shine light into the 'black box' of fish ecology.

Climate-driven regime shift of a temperate marine ecosystem.

Ecosystem reconfigurations arising from climate-driven changes in species distributions are expected to have profound ecological, social, and economic implications. Here we reveal a rapid climate-driven regime shift of Australian temperate reef communities, which lost their defining kelp forests and became dominated by persistent seaweed turfs. After decades of ocean warming, extreme marine heat waves forced a 100-kilometer range contraction of extensive kelp forests and saw temperate species replaced by seaweeds, invertebrates, corals, and fishes characteristic of subtropical and tropical waters. This community-wide tropicalization fundamentally altered key ecological processes, suppressing the recovery of kelp forests.

Abundance, diversity, and feeding behavior of coral reef butterflyfishes at Lord Howe Island.

Endemic species are assumed to have a high risk of extinction because their restricted geographic range is often associated with low abundance and high ecological specialization. This study examines the abundance of Chaetodon butterflyfishes at Lord Howe Island in the south-west Pacific, and compares interspecific differences in local abundance to the feeding behavior and geographic range of these species. Contrary to expected correlations between abundance and geographic range, the single most abundant species of butterflyfish was Chaetodon tricinctus, which is endemic to Lord Howe Island and adjacent reefs; densities of C. tricinctus (14.1 ± 2.1 SE fish per 200m(2)) were >3 times higher than the next most abundant butterflyfish (Chaetodon melannotus), and even more abundant than many other geographically widespread species. Dietary breadth for the five dominant butterflyfishes at Lord Howe Island was weakly and generally negative correlated with abundance. The endemic C. tricinctus was a distinct outlier in this relationship, though our extensive feeding observations suggest some issues with the measurements of dietary breadth for this species. Field observations revealed that all bites taken on benthic substrates by C. tricinctus were from scleractinian corals, but adults rarely, if ever, took bites from the benthos, suggesting that they may be feeding nocturnally and/or using mid-water prey, such as plankton. Alternatively, the energetic demands of C. tricinctus may be fundamentally different to other coral-feeding butterflyfishes. Neither dietary specialization nor geographic range accounts for interspecific variation in abundance of coral reef butterflyfishes at Lord Howe Island, while much more work on the foraging behavior and population dynamics of C. tricinctus will be required to understand its' abundance at this location.

Energetic extremes in aquatic locomotion by coral reef fishes.

Underwater locomotion is challenging due to the high friction and resistance imposed on a body moving through water and energy lost in the wake during undulatory propulsion. While aquatic organisms have evolved streamlined shapes to overcome such resistance, underwater locomotion has long been considered a costly exercise. Recent evidence for a range of swimming vertebrates, however, has suggested that flapping paired appendages around a rigid body may be an extremely efficient means of aquatic locomotion. Using intermittent flow-through respirometry, we found exceptional energetic performance in the Bluelined wrasse Stethojulis bandanensis, which maintains tuna-like optimum cruising speeds (up to 1 metre s(-1)) while using 40% less energy than expected for their body size. Displaying an exceptional aerobic scope (22-fold above resting), streamlined rigid-body posture, and wing-like fins that generate lift-based thrust, S. bandanensis literally flies underwater to efficiently maintain high optimum swimming speeds. Extreme energetic performance may be key to the colonization of highly variable environments, such as the wave-swept habitats where S. bandanensis and other wing-finned species tend to occur. Challenging preconceived notions of how best to power aquatic locomotion, biomimicry of such lift-based fin movements could yield dramatic reductions in the power needed to propel underwater vehicles at high speed.

Body fineness ratio as a predictor of maximum prolonged-swimming speed in coral reef fishes.

The ability to sustain high swimming speeds is believed to be an important factor affecting resource acquisition in fishes. While we have gained insights into how fin morphology and motion influences swimming performance in coral reef fishes, the role of other traits, such as body shape, remains poorly understood. We explore the ability of two mechanistic models of the causal relationship between body fineness ratio and endurance swimming-performance to predict maximum prolonged-swimming speed (Umax ) among 84 fish species from the Great Barrier Reef, Australia. A drag model, based on semi-empirical data on the drag of rigid, submerged bodies of revolution, was applied to species that employ pectoral-fin propulsion with a rigid body at U max. An alternative model, based on the results of computer simulations of optimal shape in self-propelled undulating bodies, was applied to the species that swim by body-caudal-fin propulsion at Umax . For pectoral-fin swimmers, Umax increased with fineness, and the rate of increase decreased with fineness, as predicted by the drag model. While the mechanistic and statistical models of the relationship between fineness and Umax were very similar, the mechanistic (and statistical) model explained only a small fraction of the variance in Umax . For body-caudal-fin swimmers, we found a non-linear relationship between fineness and Umax , which was largely negative over most of the range of fineness. This pattern fails to support either predictions from the computational models or standard functional interpretations of body shape variation in fishes. Our results suggest that the widespread hypothesis that a more optimal fineness increases endurance-swimming performance via reduced drag should be limited to fishes that swim with rigid bodies.

Community change within a Caribbean coral reef Marine Protected Area following two decades of local management.

Structural change in both the habitat and reef-associated fish assemblages within spatially managed coral reefs can provide key insights into the benefits and limitations of Marine Protected Areas (MPAs). While MPA zoning effects on particular target species are well reported, we are yet to fully resolve the various affects of spatial management on the structure of coral reef communities over decadal time scales. Here, we document mixed affects of MPA zoning on fish density, biomass and species richness over the 21 years since establishment of the Saba Marine Park (SMP). Although we found significantly greater biomass and species richness of reef-associated fishes within shallow habitats (5 meters depth) closed to fishing, this did not hold for deeper (15 m) habitats, and there was a widespread decline (38% decrease) in live hard coral cover and a 68% loss of carnivorous reef fishes across all zones of the SMP from the 1990s to 2008. Given the importance of live coral for the maintenance and replenishment of reef fishes, and the likely role of chronic disturbance in driving coral decline across the region, we explore how local spatial management can help protect coral reef ecosystems within the context of large-scale environmental pressures and disturbances outside the purview of local MPA management.

Life history patterns shape energy allocation among fishes on coral reefs.

Although critically important, the link between animal life histories and ecosystem energetics is seldom explored. In the pursuit of ecological simplification, ecosystem properties are typically described by models based on static counts, where organisms are aggregated into trophic- or size-based groups. Consequently, output is often based on an assumption that larger group biomass equals greater energetic contribution. Here, we modelled the individual growth of over 58,000 fishes from 74 genera within a coral reef ecosystem to investigate the role and importance of taxon-specific life histories to the division, spatial distribution and relative contribution of biomass production within 14 coral reef fish families. Rank changes among families in standing biomass to biomass production indicated that small cryptic families (e.g. Gobiidae and Blenniidae) exhibit collective growth potentials equal to or exceeding those of many other common families composed of individuals with body-sizes 1-3 orders of magnitude larger. Remaining at high risk of predation throughout their lives as a consequence of their small size, these cryptic fishes also provide a constant food resource and supply of reproductive energy to coral reefs throughout the year. Enhanced further by the strength and diversity of their trophic relationships within food webs, the highly productive nature of these small cryptic fishes suggests they make a substantial contribution to the flow of energy in coral reef ecosystems via predatory pathways. It appears that life histories leave a strong imprint on ecosystem energy fluxes and illustrate the importance of incorporating taxon-specific features when assigning values to key ecosystem processes.