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.

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.

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.

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.

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.

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.

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.

First genealogy for a wild marine fish population reveals multigenerational philopatry.

Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.

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.

Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish.

Colonial animals often form stable pair bonds, returning to the same site to breed with the same partner every year. Familiarity with both partner and breeding site has the potential to enhance an individual's reproductive success. However, it is often unknown whether the mating system arises because of site fidelity, mate fidelity or both. Here, observational and experimental studies are used to identify causal links between site fidelity and pair formation in a group-living coral reef cardinalfish, Sphaeramia nematoptera. A long-term field tagging study was undertaken to quantify site and mate attachment. This was followed by both mate removal and mate transplant experiments to test whether the prolonged association with home sites was primarily because of mate or site fidelity. Adult S. nematoptera exhibited a prolonged association with home sites and partners, with some pairs lasting more than 4 months at the same site. A Bayesian mixed effect model showed that individuals in pairs were more likely to remain site attached, regardless of sex and maturity. Following mate removal, 78% of S. nematoptera found a new partner within 2 weeks on the same site, supporting the hypothesis that individuals primarily exhibit site fidelity. This was confirmed by the partner translocation experiment, with only 1 of 24 fish following their translocated partner to a new site. In these cardinalfish, strong site attachment facilitates long-lasting pair bonds, as well as new pair formation when necessary, suggesting that site rather than mate fidelity is the major driver of the reproductive system.

Influence of sampling frequency and load calculation methods on quantification of annual river nutrient and suspended solids loads.

Better management of water quality in streams, rivers and lakes requires precise and accurate estimates of different contaminant loads. We assessed four sampling frequencies (2 days, weekly, fortnightly and monthly) and five load calculation methods (global mean (GM), rating curve (RC), ratio estimator (RE), flow-stratified (FS) and flow-weighted (FW)) to quantify loads of nitrate-nitrogen (NO3--N), soluble inorganic nitrogen (SIN), total nitrogen (TN), dissolved reactive phosphorus (DRP), total phosphorus (TP) and total suspended solids (TSS), in the Manawatu River, New Zealand. The estimated annual river loads were compared to the reference 'true' loads, calculated using daily measurements of flow and water quality from May 2010 to April 2011, to quantify bias (i.e. accuracy) and root mean square error 'RMSE' (i.e. accuracy and precision). The GM method resulted into relatively higher RMSE values and a consistent negative bias (i.e. underestimation) in estimates of annual river loads across all sampling frequencies. The RC method resulted in the lowest RMSE for TN, TP and TSS at monthly sampling frequency. Yet, RC highly overestimated the loads for parameters that showed dilution effect such as NO3--N and SIN. The FW and RE methods gave similar results, and there was no essential improvement in using RE over FW. In general, FW and RE performed better than FS in terms of bias, but FS performed slightly better than FW and RE in terms of RMSE for most of the water quality parameters (DRP, TP, TN and TSS) using a monthly sampling frequency. We found no significant decrease in RMSE values for estimates of NO3-N, SIN, TN and DRP loads when the sampling frequency was increased from monthly to fortnightly. The bias and RMSE values in estimates of TP and TSS loads (estimated by FW, RE and FS), however, showed a significant decrease in the case of weekly or 2-day sampling. This suggests potential for a higher sampling frequency during flow peaks for more precise and accurate estimates of annual river loads for TP and TSS, in the study river and other similar conditions.

Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish.

Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long-standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar-cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first- and later-generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid-shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome-wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.

Incorporating larval dispersal into MPA design for both conservation and fisheries.

Larval dispersal by ocean currents is a critical component of systematic marine protected area (MPA) design. However, there is a lack of quantitative methods to incorporate larval dispersal in support of increasingly diverse management objectives, including local population persistence under multiple types of threats (primarily focused on larval retention within and dispersal between protected locations) and benefits to unprotected populations and fisheries (primarily focused on larval export from protected locations to fishing grounds). Here, we present a flexible MPA design approach that can reconcile multiple such potentially conflicting management objectives by balancing various associated treatments of larval dispersal information. We demonstrate our approach based on alternative dispersal patterns, combinations of threats to populations, management objectives, and two different optimization strategies (site vs. network-based). Our outcomes highlight a consistently high effectiveness in selecting priority locations that are self-replenishing, inter-connected, and/or important larval sources. We find that the opportunity to balance these three dispersal attributes flexibly can help not only to prevent meta-population collapse, but also to ensure effective fisheries recovery, with average increases in the number of recruits at fishing grounds at least two times higher than achieved by standard habitat-based or ad-hoc MPA designs. Future applications of our MPA design approach should therefore be encouraged, specifically where management tools other than MPAs are not feasible.

The role of marine reserves in the replenishment of a locally impacted population of anemonefish on the Great Barrier Reef.

The development of parentage analysis to track the dispersal of juvenile offspring has given us unprecedented insight into the population dynamics of coral reef fishes. These tools now have the potential to inform fisheries management and species conservation, particularly for small fragmented populations under threat from exploitation and disturbance. In this study, we resolve patterns of larval dispersal for a population of the anemonefish Amphiprion melanopus in the Keppel Islands (southern Great Barrier Reef). Habitat loss and fishing appear to have impacted this population and a network of no-take marine reserves currently protects 75% of the potential breeders. Using parentage analysis, we estimate that 21% of recruitment in the island group was generated locally and that breeding adults living in reserves were responsible for 79% (31 of 39) of these of locally produced juveniles. Overall, the network of reserves was fully connected via larval dispersal; however, one reserve was identified as a critical source of larvae for the island group. The population in the Keppel Islands also appears to be well-connected to other source populations at least 60 km away, given that 79% (145 of 184) of the juveniles sampled remained unassigned in the parentage analysis. We estimated the effective size of the A. melanopus metapopulation to be 745 (582-993 95% CI) and recommend continued monitoring of its genetic status. Maintaining connectivity with populations beyond the Keppel Islands and recovery of local recruitment habitat, potentially through active restoration of host anemone populations, will be important for its long-term persistence.

Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park.

Larval dispersal is the key process by which populations of most marine fishes and invertebrates are connected and replenished. Advances in larval tagging and genetics have enhanced our capacity to track larval dispersal, assess scales of population connectivity, and quantify larval exchange among no-take marine reserves and fished areas. Recent studies have found that reserves can be a significant source of recruits for populations up to 40 km away, but the scale and direction of larval connectivity across larger seascapes remain unknown. Here, we apply genetic parentage analysis to investigate larval dispersal patterns for two exploited coral reef groupers (Plectropomus maculatus and Plectropomus leopardus) within and among three clusters of reefs separated by 60-220 km within the Great Barrier Reef Marine Park, Australia. A total of 69 juvenile P. maculatus and 17 juvenile P. leopardus (representing 6% and 9% of the total juveniles sampled, respectively) were genetically assigned to parent individuals on reefs within the study area. We identified both short-distance larval dispersal within regions (200 m to 50 km) and long-distance, multidirectional dispersal of up to ~250 km among regions. Dispersal strength declined significantly with distance, with best-fit dispersal kernels estimating median dispersal distances of ~110 km for P. maculatus and ~190 km for P. leopardus. Larval exchange among reefs demonstrates that established reserves form a highly connected network and contribute larvae for the replenishment of fished reefs at multiple spatial scales. Our findings highlight the potential for long-distance dispersal in an important group of reef fishes, and provide further evidence that effectively protected reserves can yield recruitment and sustainability benefits for exploited fish populations.

Bayesian methods of confidence interval construction for the population attributable risk from cross-sectional studies.

Population attributable risk measures the public health impact of the removal of a risk factor. To apply this concept to epidemiological data, the calculation of a confidence interval to quantify the uncertainty in the estimate is desirable. However, because perhaps of the confusion surrounding the attributable risk measures, there is no standard confidence interval or variance formula given in the literature. In this paper, we implement a fully Bayesian approach to confidence interval construction of the population attributable risk for cross-sectional studies. We show that, in comparison with a number of standard Frequentist methods for constructing confidence intervals (i.e. delta, jackknife and bootstrap methods), the Bayesian approach is superior in terms of percent coverage in all except a few cases. This paper also explores the effect of the chosen prior on the coverage and provides alternatives for particular situations. Copyright © 2016 John Wiley & Sons, Ltd.