Geographic variability in the gonadal development and sexual ontogeny of Hemigymnus, Cheilinus and Oxycheilinus wrasses among Indo-Pacific coral reefs.

Patterns of reproductive ontogeny in four species of coral reef wrasses (F: Labridae) Hemigymnus melapterus, Hemigymnus fasciatus, Cheilinus fasciatus and Oxycheilinus digramma were investigated. Populations of each species were sampled from two island groups of the central Great Barrier Reef (GBR), Australia, and from coral reefs in the central Philippines. These three sampling locations span 30° of latitude. The GBR and Philippine reefs experience biologically significant differences in water temperature, geography and human activity. The studied wrasses are effectively unfished in Australia but heavily fished in the Philippines. Gonad weights, histology and demographic data were obtained across the entire size and age range of H. melapterus, C. fasciatus and O. digramma from all locations. Analysis identified three processes of male recruitment: functional gonochorism and both forms of protogynous hermaphroditism, monandry and diandry. The expression of these distinct sexual ontogenies was locality dependent. Populations of H. melapterus, H. fasciatus, C. fasciatus and O. digramma on the GBR showed consistently uniform patterns of sexual ontogeny, with all species being exclusively monandric. H. melapterus, C. fasciatus and O. digramma in the Philippines displayed complex sexual ontogenies, with all species showing histological evidence of both diandry and functional gonochorism. Reproductive investment in gonadal tissue, and population sex structure, also differed between GBR and Philippine coral reefs. Philippine populations had substantially lower gonado-somatic indices than populations on the GBR. Nonetheless, Philippine populations matured more rapidly and displayed a protracted timing of sex change over a large size and age range. Thus, mature females appeared earlier and persisted later into ontogeny in the Philippines than on GBR reefs. Protracted timing of sex change on Philippine reefs is likely linked to the presence of primary males in the population, which is known to reduce the strength of selection for mature females to undergo sex change and become male. Hypotheses based on social structure of fish populations, environmental factors and evolutionary history were developed to account for the different patterns of sexual ontogeny in the focal wrasses.

Development of reproductive potential in protogynous coral reef fishes within Philippine no-take marine reserves.

Empirical evidence for increases in the reproductive potential (egg output per unit area) of coral reef fish in no-take marine reserves (NTMRs) is sparse. Here, we inferred the development of reproductive potential in two species of protogynous reef fishes, Chlorurus bleekeri (Labridae: Scarinae) and Cephalopholis argus (Epinephelidae), inside and outside of Philippine NTMRs. We estimated key reproductive parameters and applied these to species-specific density and length data from 17 NTMRs (durations of protection 0-11 years) and paired fished sites (controls) in a space-for-time substitution approach. For C. argus, we also used density and length data collected almost annually over 29 years from a NTMR and an adjacent control at Apo Island. The results suggest that C. bleekeri can develop 6.0 times greater reproductive potential in NTMRs than controls after 11 years of protection, equivalent to approximately 582,000 more eggs produced 500 m-2 inside NTMRs. Enhancement of reproductive potential in C. argus was not evident after 11 years in the space-for-time substitution. At Apo Island NTMR, reproductive potential of C. argus increased approximately 6-fold over 29 years but NTMR/control ratios in reproductive potential decreased through time (from 3.2 to 2.4), probably due to spillover of C. argus from the NTMR to the control. C. argus was estimated to produce approximately 113,000 more eggs 500 m-2 inside Apo Island NTMR at the 29th year of protection. Ratios of reproductive potential between NTMR and controls in C. bleekeri and C. argus were often greater than corresponding ratios in density or biomass. The study underscores the importance of species-specific reproductive life history traits that drive variation in the development of larval fish subsidies that originate from NTMRs.

Relative influence of environmental factors and fishing on coral reef fish assemblages.

Understanding whether assemblages of species respond more strongly to bottom-up (availability of trophic resources or habitats) or top-down (predation pressure) processes is important for effective management of resources and ecosystems. We determined the relative influence of environmental factors and predation by humans in shaping the density, biomass, and species richness of 4 medium-bodied (10-40 cm total length [TL]) coral reef fish groups targeted by fishers (mesopredators, planktivores, grazer and detritivores, and scrapers) and the density of 2 groups not targeted by fishers (invertivores, small fish ≤10 cm TL) in the central Philippines. Boosted regression trees were used to model the response of each fish group to 21 predictor variables: 13 habitat variables, 5 island variables, and 3 fishing variables (no-take marine reserve [NTMR] presence or absence, NTMR size, and NTMR age). Targeted and nontargeted fish groups responded most strongly to habitat variables, then island variables. Fishing (NTMR) variables generally had less influence on fish groups. Of the habitat variables, live hard coral cover, structural complexity or habitat complexity index, and depth had the greatest effects on density, biomass, and species richness of targeted fish groups and on the density of nontargeted fishes. Of the island variables, proximity to the nearest river and island elevation had the most influence on fish groups. The NTMRs affected only fishes targeted by fishers; NTMR size positively correlated with density, biomass, and species richness of targeted fishes, particularly mesopredatory, and grazing and detritivorous fishes. Importantly, NTMRs as small as 15 ha positively affected medium-bodied fishes. This finding provides reassurance for regions that have invested in small-scale community-managed NTMRs. However, management strategies that integrate sound coastal land-use practices to conserve adjacent reef fish habitat, strategic NTMR placement, and establishment of larger NTMRs will be crucial for maintaining biodiversity and fisheries.

Influencia Relativa de los Factores Ambientales y la Pesca sobre el Ensamblaje de Peces en los Arrecifes de Coral Resumen Es importante entender si el ensamblaje de especies responde con mayor fuerza al proceso de abajo-arriba (disponibilidad de recursos tróficos o hábitats) o al de arriba-abajo (presión de depredadores) para el manejo efectivo de los recursos y los ecosistemas. Determinamos la influencia relativa de los factores ambientales y la depredación humana en la configuración de la densidad, la biomasa y la riqueza de especies de cuatro peces de arrecife de coral con un tamaño corporal mediano (10-40 cm de longitud total [LT]) que son preferidos por los pescadores (mesodepredadores, planctívoros, forrajeros y detritívoros, y raspadores) y también determinamos la densidad de dos grupos que no son blanco de los pescadores (invertívoros y peces de talla pequeña ≤10 cm LT) en la región central de las Filipinas. Usamos árboles de regresión amplificados para modelar la respuesta de cada grupo de peces a 21 variables de predicción: trece variables de hábitat, cinco variables de isla y tres variables de pesca (ausencia o presencia de una reserva marina vedada [RMV], tamaño y antigüedad de la NTMR). Los grupos de peces preferidos y no preferidos por los pescadores respondieron con mayor fuerza a las variables de hábitat que a las variables de isla. Las variables de pesca (RMV) en general tuvieron una menor influencia sobre los grupos de peces. De las variables de hábitat, la cobertura de coral duro vivo, la complejidad estructural o el índice de complejidad del hábitat y la profundidad tuvieron el mayor efecto sobre la densidad, la biomasa y la riqueza de especies de los peces preferidos por los pescadores y sobre la densidad de los peces no preferidos por los pescadores. De las variables de isla, la proximidad al río más cercano y la elevación de la isla tuvieron la mayor influencia sobre los grupos de peces. Las RMVs afectaron sólo a los peces preferidos por los pescadores; el tamaño de la NTMR tuvo una correlación positiva con la densidad, la biomasa y la riqueza de especies de los peces preferidos por los pescadores, particularmente los peces mesodepredadores, forrajeros y detritívoros. De manera importante, las RMVs con un tamaño mínimo de 15 ha afectaron positivamente a los peces de talla mediana. Este hallazgo proporciona seguridad para las regiones que han invertido en RMVs de pequeña escala y manejadas por la comunidad. Sin embargo, las estrategias de manejo que integran prácticas firmes de uso de suelo costero para conservar el hábitat adyacente de peces, la ubicación estratégica de RMV y el establecimiento de RMVs más grandes serán cruciales para el mantenimiento de la biodiversidad y las pesquerías.

Coral cover a stronger driver of reef fish trophic biomass than fishing.

An influential paradigm in coral reef ecology is that fishing causes trophic cascades through reef fish assemblages, resulting in reduced herbivory and thus benthic phase shifts from coral to algal dominance. Few long-term field tests exist of how fishing affects the trophic structure of coral reef fish assemblages, and how such changes affect the benthos. Alternatively, benthic change itself may drive the trophic structure of reef fish assemblages. Reef fish trophic structure and benthic cover were quantified almost annually from 1983 to 2014 at two small Philippine islands (Apo, Sumilon). At each island a No-Take Marine Reserve (NTMR) site and a site open to subsistence reef fishing were monitored. Thirteen trophic groups were identified. Large planktivores often accounted for >50% of assemblage biomass. Significant NTMR effects were detected at each island for total fish biomass, but for only 2 of 13 trophic components: generalist large predators and large planktivores. Fishing-induced changes in biomass of these components had no effect on live hard coral (HC) cover. In contrast, HC cover affected biomass of 11 of 13 trophic components significantly. Positive associations with HC cover were detected for total fish biomass, generalist large predators, piscivores, obligate coral feeders, large planktivores, and small planktivores. Negative associations with HC cover were detected for large benthic foragers, detritivores, excavators, scrapers, and sand feeders. These associations of fish biomass to HC cover were most clear when environmental disturbances (e.g., coral bleaching, typhoons) reduced HC cover, often quickly (1-2 yr), and when HC recovered, often slowly (5-10 yr). As HC cover changed, the biomass of 11 trophic components of the fish assemblage changed. Benthic and fish assemblages were distinct at all sites from the outset, remaining so for 31 yr, despite differences in fishing pressure and disturbance history. HC cover alone explained ~30% of the variability in reef fish trophic structure, whereas fishing alone explained 24%. Furthermore, HC cover affected more trophic groups more strongly than fishing. Management of coral reefs must include measures to maintain coral reef habitats, not just measures to reduce fishing by NTMRs.

Non-reef habitats in a tropical seascape affect density and biomass of fishes on coral reefs.

Nonreef habitats such as mangroves, seagrass, and macroalgal beds are important for foraging, spawning, and as nursery habitat for some coral reef fishes. The spatial configuration of nonreef habitats adjacent to coral reefs can therefore have a substantial influence on the distribution and composition of reef fish. We investigate how different habitats in a tropical seascape in the Philippines influence the presence, density, and biomass of coral reef fishes to understand the relative importance of different habitats across various spatial scales. A detailed seascape map generated from satellite imagery was combined with field surveys of fish and benthic habitat on coral reefs. We then compared the relative importance of local reef (within coral reef) and adjacent habitat (habitats in the surrounding seascape) variables for coral reef fishes. Overall, adjacent habitat variables were as important as local reef variables in explaining reef fish density and biomass, despite being fewer in number in final models. For adult and juvenile wrasses (Labridae), and juveniles of some parrotfish taxa (Chlorurus), adjacent habitat was more important in explaining fish density and biomass. Notably, wrasses were positively influenced by the amount of sand and macroalgae in the adjacent seascape. Adjacent habitat metrics with the highest relative importance were sand (positive), macroalgae (positive), and mangrove habitats (negative), and fish responses to these metrics were consistent across fish groups evaluated. The 500-m spatial scale was selected most often in models for seascape variables. Local coral reef variables with the greatest importance were percent cover of live coral (positive), sand (negative), and macroalgae (mixed). Incorporating spatial metrics that describe the surrounding seascape will capture more holistic patterns of fish-habitat relationships on reefs. This is important in regions where protection of reef fish habitat is an integral part of fisheries management but where protection of nonreef habitats is often overlooked.

Fishing pressure impacts the abundance gradient of European lobsters across the borders of a newly established marine protected area.

Marine protected areas (MPAs) are considered viable fisheries management tools due to their potential benefits of adult spillover and recruitment subsidy to nearby fisheries. However, before-after control-impact studies that explore the biological and fishery effects of MPAs to surrounding fisheries are scarce. We present results from a fine-scale spatial gradient study conducted before and after the implementation of a 5 km2 lobster MPA in southern Norway. A significant nonlinear response in lobster abundance, estimated as catch-per-unit-effort (CPUE) from experimental fishing, was detected within 2 years of protection. After 4 years, CPUE values inside the MPA had increased by a magnitude of 2.6 compared to before-protection values. CPUE showed a significant nonlinear decline from the centre of the MPA, with a depression immediately outside the border and a plateau in fished areas. Overall fishing pressure almost doubled over the course of the study. The highest increase in fishing pressure (by a magnitude of 3) was recorded within 1 km of the MPA border, providing a plausible cause for the depression in CPUE. Taken together, these results demonstrate the need to regulate fishing pressure in surrounding areas when MPAs are implemented as fishery management tools.

Strategies in scheduling marine protected area establishment in a network system.

Instantaneous implementation of systematic conservation plans at regional scales is rare. More typically, planned actions are applied incrementally over periods of years or decades. During protracted implementation, the character of the connected ecological system will change as a function of external anthropogenic pressures, local metapopulation processes, and environmental fluctuations. For heavily exploited systems, habitat quality will deteriorate as the plan is implemented, potentially influencing the schedule of protected area implementation necessary to achieve conservation objectives. Understanding the best strategy to adopt for applying management within a connected environment is desirable, especially given limited conservation resources. Here, we model the sequential application of no-take marine protected areas (MPAs) in the central Philippines within a metapopulation framework, using a range of network-based decision rules. The model was based on selecting 33 sites for protection from 101 possible sites over a 35-yr period. The graph-theoretic network criteria to select sites for protection included PageRank, maximum degree, closeness centrality, betweenness centrality, minimum degree, random, and historical events. We also included a dynamic strategy called colonization-extinction rate that was updated every year based on the changing capacity of each site to produce and absorb larvae. Each rule was evaluated in the context of achieving the maximum metapopulation mean lifetime at the conclusion of the implementation phase. MPAs were designated through the alteration of the extinction risk parameter. The highest ranked criteria were PageRank while the actual implementation from historical records ranked lowest. Our results indicate that protecting the sites ranked highest with regard to larval supply is likely to yield the highest benefit for fish abundance and fish metapopulation persistence. Model results highlighted the benefits of including network processes in conservation planning.

Decadal-scale response of detritivorous surgeonfishes (family Acanthuridae) to no-take marine reserve protection and changes in benthic habitat.

No-take marine reserves (NTMR) are increasingly being implemented to mitigate the effects of fishing on coral reefs, yet determining the efficacy of NTMRs depends largely on partitioning the effects of fishing from the effect of benthic habitat. Species of coral-reef fishes typically decline in density when subjected to fishing or benthic disturbances, but this is not always the case. This study documents the long-term (8-31 years) response of six species of detritivorous surgeonfishes (family Acanthuridae) to NTMR protection and benthic habitat change at four islands (Apo, Sumilon, Mantigue, Selinog) in the central Philippines, each island with a NTMR and a monitored fished site. Despite being subject to moderate fishing pressure, these species did not increase in density with NTMR protection. However, density of these surgeonfishes had a strong negative relationship with cover of live hard coral and a strong positive relationship with cover of dead substratum (sand, rubble, hard dead substratum). These surgeonfishes typically feed over dead substrata and thus probably increase in density following large environmental disturbances that substantially reduce live hard coral cover. Here, we describe effects of environmental disturbance events (e.g., use of explosives, typhoons) that reduced live hard-coral cover and subsequent large increases (up to 25 fold) in surgeonfish densities, which then slowly (over 5-15 years) decreased in density as live hard coral recovered. Density of these functionally important surgeonfish species was influenced more by changes to benthic cover than by NTMR protection. Thus, we highlight the greater importance of bottom-up controls (i.e., benthic changes to food availability) than top-down control (i.e., fishing) on a functionally important group of coral-reef fishes.

Node self-connections and metapopulation persistence: reply to Saura (2018).

Saura () claims that studies using the Probability of Connectivity metric (PC) had already demonstrated the importance of including node self-connections in network metrics. As originally defined and used, PC cannot test the importance of self-connections. However, with key terms redefined, PC could be a useful tool in future work.

Network theory and metapopulation persistence: incorporating node self-connections.

Network analysis is gaining increasing importance in conservation planning. However, which network metrics are the best predictors of metapopulation persistence is still unresolved. Here, we identify a critical limitation of graph theory-derived network metrics that have been proposed for this purpose: their omission of node self-connections. We resolve this by presenting modifications of existing network metrics, and developing entirely new metrics, that account for node self-connections. Then, we illustrate the performance of these new and modified metrics with an age-structured metapopulation model for a real-world marine reserve network case study, and we evaluate the robustness of our findings by systematically varying particular features of that network. Our new and modified metrics predict metapopulation persistence much better than existing metrics do, even when self-connections are weak. Existing metrics become good predictors of persistence only when self-connections are entirely absent, an unrealistic scenario in the overwhelming majority of metapopulation applications. Our study provides a set of novel tools that can substantially enhance the extent to which network metrics can be employed to understand, and manage for, metapopulation persistence.

Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design.

Well-designed and effectively managed networks of marine reserves can be effective tools for both fisheries management and biodiversity conservation. Connectivity, the demographic linking of local populations through the dispersal of individuals as larvae, juveniles or adults, is a key ecological factor to consider in marine reserve design, since it has important implications for the persistence of metapopulations and their recovery from disturbance. For marine reserves to protect biodiversity and enhance populations of species in fished areas, they must be able to sustain focal species (particularly fishery species) within their boundaries, and be spaced such that they can function as mutually replenishing networks whilst providing recruitment subsidies to fished areas. Thus the configuration (size, spacing and location) of individual reserves within a network should be informed by larval dispersal and movement patterns of the species for which protection is required. In the past, empirical data regarding larval dispersal and movement patterns of adults and juveniles of many tropical marine species have been unavailable or inaccessible to practitioners responsible for marine reserve design. Recent empirical studies using new technologies have also provided fresh insights into movement patterns of many species and redefined our understanding of connectivity among populations through larval dispersal. Our review of movement patterns of 34 families (210 species) of coral reef fishes demonstrates that movement patterns (home ranges, ontogenetic shifts and spawning migrations) vary among and within species, and are influenced by a range of factors (e.g. size, sex, behaviour, density, habitat characteristics, season, tide and time of day). Some species move <0.1-0.5 km (e.g. damselfishes, butterflyfishes and angelfishes), <0.5-3 km (e.g. most parrotfishes, goatfishes and surgeonfishes) or 3-10 km (e.g. large parrotfishes and wrasses), while others move tens to hundreds (e.g. some groupers, emperors, snappers and jacks) or thousands of kilometres (e.g. some sharks and tuna). Larval dispersal distances tend to be <5-15 km, and self-recruitment is common. Synthesising this information allows us, for the first time, to provide species, specific advice on the size, spacing and location of marine reserves in tropical marine ecosystems to maximise benefits for conservation and fisheries management for a range of taxa. We recommend that: (i) marine reserves should be more than twice the size of the home range of focal species (in all directions), thus marine reserves of various sizes will be required depending on which species require protection, how far they move, and if other effective protection is in place outside reserves; (ii) reserve spacing should be <15 km, with smaller reserves spaced more closely; and (iii) marine reserves should include habitats that are critical to the life history of focal species (e.g. home ranges, nursery grounds, migration corridors and spawning aggregations), and be located to accommodate movement patterns among these. We also provide practical advice for practitioners on how to use this information to design, evaluate and monitor the effectiveness of marine reserve networks within broader ecological, socioeconomic and management contexts.

Ten things to get right for marine conservation planning in the Coral Triangle.

Systematic conservation planning increasingly underpins the conservation and management of marine and coastal ecosystems worldwide. Amongst other benefits, conservation planning provides transparency in decision-making, efficiency in the use of limited resources, the ability to minimise conflict between diverse objectives, and to guide strategic expansion of local actions to maximise their cumulative impact. The Coral Triangle has long been recognised as a global marine conservation priority, and has been the subject of huge investment in conservation during the last five years through the Coral Triangle Initiative on Coral Reefs, Fisheries and Food Security. Yet conservation planning has had relatively little influence in this region. To explore why this is the case, we identify and discuss 10 challenges that must be resolved if conservation planning is to effectively inform management actions in the Coral Triangle. These are: making conservation planning accessible; integrating with other planning processes; building local capacity for conservation planning; institutionalising conservation planning within governments; integrating plans across governance levels; planning across governance boundaries; planning for multiple tools and objectives; understanding limitations of data; developing better measures of progress and effectiveness; and making a long term commitment. Most important is a conceptual shift from conservation planning undertaken as a project, to planning undertaken as a process, with dedicated financial and human resources committed to long-term engagement.