Physical, biological and anthropogenic drivers of spatial patterns of coral reef fish assemblages at regional and local scales.

Species abundance, diversity and community assemblage structure are determined by multiple physical, habitat and management drivers that operate across multiple spatial scales. Here we used a multi-scale coral reef monitoring dataset to examine regional and local differences in the abundance, species richness and composition of fish assemblages in no-take marine reserve (NTMR) and fished zones at four island groups in the Great Barrier Reef Marine Park, Australia. We applied boosted regression trees to quantify the influence of 20 potential drivers on the coral reef fish assemblages. Reefs in two locations, Magnetic Island and the Keppel Islands, had distinctive fish assemblages and low species richness, while the Palm and Whitsunday Islands had similar species composition and higher species richness. Overall, our analyses identified several important physical (temperature, wave exposure) and biological (coral, turf, macroalgal and unconsolidated substratum cover) drivers of inshore reef fish communities, some of which are being altered by human activities. Of these, sea surface temperature (SST) was more influential at large scales, while wave exposure was important both within and between island groups. Species richness declined with increasing macroalgal cover and exposure to cyclones, and increased with SST. Species composition was most strongly influenced by mean SST and percent cover of macroalgae. There was substantial regional variation in the local drivers of spatial patterns. Although NTMR zoning influenced total fish density in some regions, it had negligible effects on fish species richness, composition and trophic structure because of the relatively small number of species targeted by the fishery. These findings show that inshore reef fishes are directly influenced by disturbances typical of the nearshore Great Barrier Reef, highlighting the need to complement global action on climate change with more targeted localised efforts to maintain or improve the condition of coral reef habitats.

Contrasting hydrodynamic regimes of submerged pinnacle and emergent coral reefs.

Hydrodynamics on coral reefs vary with depth, reef morphology and seascape position. Differences in hydrodynamic regimes strongly influence the structure and function of coral reef ecosystems. Submerged coral reefs on steep-sided, conical bathymetric features like seamounts experience enhanced water circulation as a result of interactions between currents and the abrupt physical structure. There may also be similar interactions between smaller pinnacles and regional water currents in offshore locations (crests > 10 m), while shallow reefs (crests <10 m) may be more subject to surface currents driven by wind, waves and tide. Here we tested whether coral pinnacles experienced stronger and more variable currents compared to emergent reefs at the same depth in both nearshore and offshore positions. Current speeds and temperature were monitored for 12 months at 11 reefs, representing the three different reef categories: submerged offshore pinnacles, emergent offshore reefs and emergent nearshore reefs. We found different patterns in current speeds and temperature among reef types throughout the year and between seasons. Submerged pinnacles exhibited stronger, more variable current speeds compared to both near and offshore emergent reefs. We found seasonal changes in current speeds for pinnacle and nearshore reefs but no variation in current strength on offshore reefs. Whilst instantaneous current directions did reflect the seascape position of individual sites, there was no difference in the directional variability of current speeds between reef types. Annual daily average temperatures at all reef types were not strongly seasonal, changing by less than 2 °C throughout the year. Daily temperature ranges at specific sites however, exhibited considerable variability (annual range of up to 6.5 °C), particularly amongst offshore emergent reefs which experienced the highest temperatures despite greater exposure to regional-scale circulation patterns. Additionally, we found a consistent mismatch between satellite sea surface temperatures and in-situ temperature data, which was on average 2 °C cooler throughout the annual study period. Our results suggest that distinct hydrodynamic processes occur on smaller submerged structures that are physically analogous to seamounts. Our findings highlight important nuances in environmental processes that occur on morphologically distinct coral reef habitats and these are likely to be important drivers for the community dynamics of organisms that inhabit these reefs.

Life-history constraints, short adult life span and reproductive strategies in coral reef gobies of the genus Trimma.

Body size influences many life-history traits, with small-bodied animals tending to have short life spans, high mortality and greater reproductive effort early in life. In this study, the authors investigated the life-history traits and reproductive strategies of three small-bodied coral reef gobies of the genus Trimma: Trimma benjamini, Trimma capostriatum and Trimma yanoi. The authors found all Trimma species studied attained a small body size of <25 mm, had a short life span of <140 days and experienced high estimated daily mortality of 3.0%-6.7%. Furthermore, the pelagic larval phase accounted for 25.3%-28.5% of the maximum life span, and maturation occurred between 74.1 and 82.1 days at 15.2-15.8 mm, leaving only 35%-43% of the total life span as a reproductively viable adult. All mature individuals had gonad structures consistent with bidirectional sex change, with bisexual gonads including both ovarian and testicular portions separated by a thin wall of connective tissue. In the female and male phases, only ovaries or testes were mature, whereas gonadal tissue of the non-active sex remained. One T. benjamini individual and one T. yanoi individual had ovarian and testicular tissue active simultaneously. The results of this study highlight the life-history challenges small CRFs face on their path to reproduction and reproductive strategies that could be beneficial in fishes with high and unpredictable mortality and short reproductive life spans.

Minimum size limits and the reproductive value of numerous, young, mature female fish.

Fisheries management relies on various catch and effort controls to preserve spawning stock biomass and maximize sustainable yields while limiting fishery impacts on marine ecosystems. These include species-specific minimum or maximum size limits to protect either small non-reproductive subadults, a portion of reproductively mature adults, or large highly fecund individuals. Protecting size classes of mature fish is expected to yield a viable source of larvae for replenishing populations and reduce the risk of recruitment overfishing, yet size-specific recruitment contributions have rarely been assessed empirically. Here, we apply genetic parentage analysis to measure the reproductive success of a size-structured population of a commercially important species of coral grouper (Plectropomus maculatus-Serranidae) in no-take marine reserves (NTMRs) in the Great Barrier Reef Marine Park, Australia. Although the per capita reproductive success of individual fish increases rapidly with body length, the numerous young mature female fish, below the minimum size limit (MSL) (38 cm total length), were responsible for generating disproportionately large contributions (36%) towards larval replenishment of both fished and reserve reefs. Our findings indicate that MSLs are an effective harvest control measure to safeguard a portion of the spawning stock biomass for coral grouper and supplement recruitment subsidies assured from NTMRs.

Species integrity, introgression, and genetic variation across a coral reef fish hybrid zone.

Hybridization and introgression are evolutionarily significant phenomena breaking down species boundaries. "Hybrid zones" (regions of species overlap and hybridization) enable quantification of hybridization frequency and examination of mechanisms driving and maintaining gene flow. The hybrid anemonefish Amphiprion leucokranos is found where parent species (A. chrysopterus; A. sandaracinos) distributions overlap. Here, we examine geographic variation in hybridization and introgression, and potential impacts on parent species integrity through assessing relative abundance, social group composition, and genetic structure (mtDNA cytochrome b, 21 microsatellite loci) of taxa at three hybrid zone locations: Kimbe Bay (KB) and Kavieng (KA), Papua New Guinea; the Solomon Islands (SO). Relative abundances of and size disparities between parent species apparently drive hybridization frequency, introgression patterns, and genetic composition of taxa. Conspecific groups are most common in KB (65%) where parent species are similarly abundant. Conversely, mixed species groups dominate SO (82%), where A. chrysopterus is more abundant. Hybrids most commonly cohabit with A. sandaracinos in KB (17%), but with A. chrysopterus in KA (22%) and SO (50%). Genetic differentiation (nDNA) analyses indicate that parent species remain distinct, despite ongoing hybridization and hybrids are genetically similar to A. sandaracinos-resulting from persistent backcrossing with this smallest species. This study shows that hybridization outcomes may depend on the social and ecological context in which taxa hybridize, where relative abundance and disparate size of parent species explain the frequency and patterns of hybridization and introgression in the A. leucokranos hybrid zone, reflecting size-based dominance behaviors of anemonefish social groups.

Ecological and social constraints combine to promote evolution of non-breeding strategies in clownfish.

Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies. Cooperative breeding theory provides a solution to the paradox: non-breeders benefit by helping relatives and/or inheriting breeding positions; non-breeders do not disperse to breed elsewhere because of ecological constraints. However, the question of why non-breeders do not contest to breed within their group has rarely been addressed. Here, we use a wild population of clownfish (Amphiprion percula), where non-breeders wait peacefully for years to inherit breeding positions, to show non-breeders will disperse when ecological constraints (risk of mortality during dispersal) are experimentally weakened. In addition, we show non-breeders will contest when social constraints (risk of eviction during contest) are experimentally relaxed. Our results show it is the combination of ecological and social constraints that promote the evolution of non-breeding strategies. The findings highlight parallels between, and potential for fruitful exchange between, cooperative breeding theory and economic bargaining theory: individuals will forgo their own reproduction and wait peacefully to inherit breeding positions (engage in cooperative options) when there are harsh ecological constraints (poor outside options) and harsh social constraints (poor inside options).

Sexual dimorphism in the horn size of a pair-forming coral reef butterflyfish.

Sexual dimorphism is a common in the animal kingdom and is often linked to mate choice or competition for mates in polygynous mating systems. However, sexual dimorphism is less common in species that form heterosexual pairs and has not been recorded in pair-forming coral-reef fish. Here we demonstrate a pronounced morphological difference between males and females in the humphead bannerfish (Heniochus varius)-a pair-forming coral reef butterflyfish. Males of paired individuals collected in Kimbe Bay, Papua New Guinea had substantially larger hump and horn protrusions on their heads than females. Fish were also sexed, sized and aged to determine the reproductive and demographic basis of the pairing behaviour. H. varius pairs were exclusively heterosexual and were assorted strongly by total length and slightly less so by age. Females in pairs were generally the same size as male partners, but were frequently older by a year and sometimes more. Hump and horn lengths increased proportionally to body-size in both sexes, with horns growing at a greater rate among males. These findings suggest that H. varius form pairs primarily for reproductive purposes, with selection via a size-assortative process that likely also extends to selection for larger hump and horn protrusions among males. The larger humps and horns in males appear to be the first recorded example of a secondary sexual morphological characteristic in a pair-forming coral reef fish species.

A connectivity portfolio effect stabilizes marine reserve performance.

Well-managed and enforced no-take marine reserves generate important larval subsidies to neighboring habitats and thereby contribute to the long-term sustainability of fisheries. However, larval dispersal patterns are variable, which leads to temporal fluctuations in the contribution of a single reserve to the replenishment of local populations. Identifying management strategies that mitigate the uncertainty in larval supply will help ensure the stability of recruitment dynamics and minimize the volatility in fishery catches. Here, we use genetic parentage analysis to show extreme variability in both the dispersal patterns and recruitment contribution of four individual marine reserves across six discrete recruitment cohorts for coral grouper (Plectropomus maculatus) on the Great Barrier Reef. Together, however, the asynchronous contributions from multiple reserves create temporal stability in recruitment via a connectivity portfolio effect. This dampening effect reduces the variability in larval supply from individual reserves by a factor of 1.8, which effectively halves the uncertainty in the recruitment contribution of individual reserves. Thus, not only does the network of four marine reserves generate valuable larval subsidies to neighboring habitats, the aggregate effect of individual reserves mitigates temporal fluctuations in dispersal patterns and the replenishment of local populations. Our results indicate that small networks of marine reserves yield previously unrecognized stabilizing benefits that ensure a consistent larval supply to replenish exploited fish stocks.

Natal philopatry increases relatedness within groups of coral reef cardinalfish.

A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.

Strong habitat and weak genetic effects shape the lifetime reproductive success in a wild clownfish population.

The relative contributions of environmental, maternal and additive genetic factors to the Lifetime reproductive success (LRS) determine whether species can adapt to rapid environmental change. Yet to date, studies quantifying LRS across multiple generations in marine species in the wild are non-existent. Here we used 10-year pedigrees resolved for a wild orange clownfish population from Kimbe Island (PNG) and a quantitative genetic linear mixed model approach to quantify the additive genetic, maternal and environmental contributions to variation in LRS for the self-recruiting portion of the population. We found that the habitat of the breeder, including the anemone species and geographic location, made the greatest contribution to LRS. There were low to negligible contributions of genetic and maternal factors equating with low heritability and evolvability. Our findings imply that our population will be susceptible to short-term, small-scale changes in habitat structure and may have limited capacity to adapt to these changes.

Successful validation of a larval dispersal model using genetic parentage data.

Larval dispersal is a critically important yet enigmatic process in marine ecology, evolution, and conservation. Determining the distance and direction that tiny larvae travel in the open ocean continues to be a challenge. Our current understanding of larval dispersal patterns at management-relevant scales is principally and separately informed by genetic parentage data and biological-oceanographic (biophysical) models. Parentage datasets provide clear evidence of individual larval dispersal events, but their findings are spatially and temporally limited. Biophysical models offer a more complete picture of dispersal patterns at regional scales but are of uncertain accuracy. Here, we develop statistical techniques that integrate these two important sources of information on larval dispersal. We then apply these methods to an extensive genetic parentage dataset to successfully validate a high-resolution biophysical model for the economically important reef fish species Plectropomus maculatus in the southern Great Barrier Reef. Our results demonstrate that biophysical models can provide accurate descriptions of larval dispersal at spatial and temporal scales that are relevant to management. They also show that genetic parentage datasets provide enough statistical power to exclude poor biophysical models. Biophysical models that included species-specific larval behaviour provided markedly better fits to the parentage data than assuming passive behaviour, but incorrect behavioural assumptions led to worse predictions than ignoring behaviour altogether. Our approach capitalises on the complementary strengths of genetic parentage datasets and high-resolution biophysical models to produce an accurate picture of larval dispersal patterns at regional scales. The results provide essential empirical support for the use of accurately parameterised biophysical larval dispersal models in marine spatial planning and management.

Marine reserves stabilize fish populations and fisheries yields in disturbed coral reef systems.

Marine reserve networks are increasingly implemented to conserve biodiversity and enhance the persistence and resilience of exploited species and ecosystems. However, the efficacy of marine reserve networks in frequently disturbed systems, such as coral reefs, has rarely been evaluated. Here we analyze a well-mixed larval pool model and a spatially explicit model based on a well-documented coral trout (Plectropomus spp.) metapopulation in the Great Barrier Reef Marine Park, Australia, to determine the effects of marine reserve coverage and placement (in relation to larval connectivity and disturbance heterogeneity) on the temporal stability of fisheries yields and population biomass in environmentally disturbed systems. We show that marine reserves can contribute to stabilizing fishery yield while increasing metapopulation persistence, irrespective of whether reserves enhance or diminish average fishery yields. However, reserve placement and the level of larval connectivity among subpopulations were important factors affecting the stability and sustainability of fisheries and fish metapopulations. Protecting a mix of disturbed and non-disturbed reefs, rather than focusing on the least-disturbed habitats, was the most consistently beneficial approach across a range of dispersal and reserve coverage scenarios. Placing reserves only in non-disturbed areas was the most beneficial for biomass enhancement, but had variable results for fisheries and could potentially destabilize yields in systems with well-mixed larval or those that are moderately fished. We also found that focusing protection on highly disturbed areas could actually increase variability in yields and biomass, especially when degraded reef reserves were distant and poorly connected to the meta-population. Our findings have implications for the design and implementation of reserve networks in the presence of stochastic, patchy environmental disturbances.

Extra-pair mating in a socially monogamous and paternal mouth-brooding cardinalfish.

Many vertebrates form monogamous pairs to mate and care for their offspring. However, genetic tools have increasingly shown that offspring often arise from matings outside of the monogamous pair bond. Social monogamy is relatively common in coral reef fishes, but there have been few studies that have confirmed monogamy or extra-pair reproduction, either for males or for females. Here, long-term observations and genetic tools were applied to examine the parentage of embryos in a paternally mouth-brooding cardinalfish, Sphaeramia nematoptera. Paternal care in fishes, such as mouth-brooding, is thought to be associated with a high degree of confidence in paternity. Two years of observations confirmed that S. nematoptera form long-term pair bonds within larger groups. However, genetic parentage revealed extra-pair mating by both sexes. Of 105 broods analysed from 64 males, 30.1% were mothered by a female that was not the partner and 11.5% of broods included eggs from two females. Despite the high paternal investment associated with mouth-brooding, 7.6% of broods were fertilized by two males. Extra-pair matings appeared to be opportunistic encounters with individuals from outside the immediate group. We argue that while pair formation contributes to group cohesion, both males and females can maximize lifetime reproductive success by taking advantage of extra-pair mating opportunities.

Assessing the performance of artificial reefs as substitute habitat for temperate reef fishes: Implications for reef design and placement.

Artificial reefs (ARs) have been advocated and implemented as management tools for recreational fisheries, species conservation and habitat replacement. For ARs to function as substitute habitat for degraded natural reefs, they should perform as close as possible to local natural reefs, however this is seldom investigated. Here we evaluated the performance of new custom-designed reef structures (CDARs) as fish habitat. As a benchmark for their success, we compared fish abundance, diversity and community composition on CDARs to another commonly used AR type (Reef Balls (RBs)) and nearby natural reefs. Fish were monitored on all reef types over two recruitment seasons at three locations in Port Phillip Bay, Australia. Overall, there were no consistent differences in fish density among reef types, although densities on both AR designs were markedly lower than natural reefs at some locations. However, fish species richness on the CDARs was, on average, 2× higher than natural or RB reefs. There were large dissimilarities in fish community composition among reef types across all locations and years. These dissimilarities declined over time with the CDARs becoming more similar to natural communities than to RB reefs. Our results suggest that CDARs can play a role in reef fish conservation where natural reefs are under threat, supporting natural community structure and enhancing local biodiversity. Overall, our findings suggest that location of deployment, rather than design, has a more significant influence on fish abundances on ARs, whereas reef design is an important determinant of species diversity and community structure irrespective of location. ARs represent an important management tool for enhancing fisheries productivity and conservation in areas where reef habitat has been degraded or lost. However, failure to incorporate consideration of reef location and design into future AR deployments may lead to poor performance and failure to achieve restoration or conservation goals.

Marginal sinks or potential refuges? Costs and benefits for coral-obligate reef fishes at deep range margins.

Escalating climate-related disturbances and asymmetric habitat losses will increasingly result in species living in more marginal habitats. Marginal habitats may represent important refuges if individuals can acquire adequate resources to survive and reproduce. However, resources at range margins are often distributed more sparsely; therefore, increased effort to acquire resources can result in suboptimal performance and lead to marginal populations becoming non-self-sustaining sink-populations. Shifting resource availability is likely to be particularly problematic for dietary specialists. Here, we use extensive in situ behavioural observations and physiological condition measurements to examine the costs and benefits of resource-acquisition along a depth gradient in two obligate corallivore reef fishes with contrasting levels of dietary specialization. As expected, the space used to secure coral resources increased towards the lower depth margin. However, increased territory sizes resulted in equal or greater availability of resources within deeper territories. In addition, we observed decreased competition and no differences in foraging distance, pairing behaviour, body condition or fecundity at greater depths. Contrary to expectation, our results demonstrate that coral-obligate fishes can select high-quality coral patches on the deeper-reef to access equal or greater resources than their shallow-water counterparts, with no extra costs. This suggests depth offers a viable potential refuge for some at-risk coral-specialist fishes.

Host anemone size as a determinant of social group size and structure in the orange clownfish (Amphiprion percula).

The size and structure of social groups of animals can be governed by a range of ecological factors and behavioral interactions. In small, highly site-attached coral reef fishes, group size is often constrained by the size of the habitat patch they are restricted to. However, group size may also be influenced by changes in abundance along important environmental gradients, such as depth or distance offshore. In addition, the body size and sex structure within social groups can be determined by the size of the habitat patch and the dominance relationships among group members. Here we examined the roles of ecological factors and behavioral interactions in governing group size and structure in the orange clownfish, Amphiprion percula, on inshore reefs in Kimbe Bay, Papua New Guinea. We quantified relationships between ecological variables (anemone size, depth, and distance from shore) and social group variables (group size, and total body length of the three largest individuals (ranks 1, 2, and 3)). Anemone size explained the greatest amount of variation in group variables, with strong, positive relationships between anemone surface area and group size, and total length of individuals ranked 1, 2, and 3. Group structure was also weakly correlated with increasing depth and distance from shore, most likely through the indirect effects of these environmental gradients on anemone size. Variation in group size and the lengths of ranks 2 and 3 were all closely related to the length of rank 1. Path analysis indicated that anemone size has a strong direct effect on the length of rank 1. In turn, the length of rank 1 directly affects the size of the subordinate individuals and indirectly affects the group size through its influence on subordinates. Hence, anemone size directly and indirectly controls social group size and structure in this space-limited fish species. It is also likely that anemonefish have feedback effects on anemone size, although this could not be differentiated in the path analysis.

Strong effects of coral species on the diversity and structure of reef fish communities: A multi-scale analysis.

While there is increasing evidence for habitat specialization in coral reef fishes, the extent to which different corals support different fish communities is not well understood. Here we quantitatively assess the relative importance of different coral species in structuring fish communities and evaluate whether sampling scale and coral colony size affect the perceived strength of fish-habitat relationships. Fish communities present on colonies of eight coral species (Porites cylindrica, Echinopora horrida, Hydnophora rigida, Stylophora pistillata, Seriatopora hystrix, Acropora formosa, A. tenuis and A. millepora) were examined in the Lizard Island lagoon, Great Barrier Reef, Australia. Additionally, the differences in fish communities supported by three coral species (P. cylindrica, E. horrida, H. rigida) were investigated at three spatial scales of sampling (2x2 m, 1x1 m, 0.5x0.5 m). Substantial differences in fish communities were observed across the different coral species, with E. horrida and H. rigida supporting the most fish species and individuals. Coral species explained more of the variability in fish species richness (20.9-53.6%), than in fish abundance (0-15%). Most coral species supported distinctive fish communities, with dissimilarities ranging from 50 to 90%. For three focal coral species, a greater amount of total variation in fish species richness and fish abundance was evident at a larger scale of sampling. Together, these results indicate that the structure of reef fish communities is finely tuned to coral species. Loss of preferred coral species could have profound effects on reef fish biodiversity, potentially more so than would be predicted on the basis of declining coral cover alone.

Loss of live coral compromises predator-avoidance behaviour in coral reef damselfish.

Tropical reefs have experienced an unprecedented loss of live coral in the past few decades and the biodiversity of coral-dependent species is under threat. Many reef fish species decline in abundance as coral cover is lost, yet the mechanisms responsible for these losses are largely unknown. A commonly hypothesised cause of fish decline is the loss of shelter space between branches as dead corals become overgrown by algae. Here we tested this hypothesis by quantifying changes in predator-avoidance behaviour of a common damselfish, Pomacentrus moluccensis, before and after the death of their coral colony. Groups of P. moluccensis were placed on either healthy or degraded coral colonies, startled using a visual stimulus and their sheltering responses compared over a 7-week period. P. moluccensis stopped sheltering amongst the coral branches immediately following the death of the coral, despite the presence of ample shelter space. Instead, most individuals swam away from the dead coral, potentially increasing their exposure to predators. It appears that the presence of live coral rather than shelter per se is the necessary cue that elicits the appropriate behavioural response to potential predators. The disruption of this link poses an immediate threat to coral-associated fishes on degrading reefs.