Geoffrey P. Jones

Ocean acidification impairs olfactory discrimination and homing ability of a marine fish

The persistence of most coastal marine species depends on larvae finding suitable adult habitat at the end of an offshore dispersive stage that can last weeks or months. We tested the effects that ocean acidification from elevated levels of atmospheric carbon dioxide (CO2) could have on the ability of larvae to detect olfactory cues from adult habitats. Larval clownfish reared in control seawater (pH 8.15) discriminated between a range of cues that could help them locate reef habitat and suitable settlement sites. This discriminatory ability was disrupted when larvae were reared in conditions simulating CO2-induced ocean acidification. Larvae became strongly attracted to olfactory stimuli they normally avoided when reared at levels of ocean pH that could occur ca. 2100 (pH 7.8) and they no longer responded to any olfactory cues when reared at pH levels (pH 7.6) that might be attained later next century on a business-as-usual carbon-dioxide emissions trajectory. If acidification continues unabated, the impairment of sensory ability will reduce population sustainability of many marine species, with potentially profound consequences for marine diversity.

Coral Reef Fish Larvae Settle Close to Home

Population connectivity through larval dispersal is an essential parameter in models of marine population dynamics and the optimal size and spacing of marine reserves. However, there are remarkably few direct estimates of larval dispersal for marine organisms, and the actual birth sites of successful recruits have never been located. Here, we solve the mystery of the natal origin of clownfish (Amphiprion polymnus) juveniles by mass-marking via tetracycline immersion all larvae produced in a population. In addition, we established parentage by DNA genotyping all potential adults and all new recruits arriving in the population. Although no individuals settled into the same anemone as their parents, many settled remarkably close to home. Even though this species has a 9-12 day larval duration, one-third of settled juveniles had returned to a 2 hectare natal area, with many settling <100 m from their birth site. This represents the smallest scale of dispersal known for any marine fish species with a pelagic larval phase. The degree of local retention indicates that marine reserves can provide recruitment benefits not only beyond but also within their boundaries.

Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues

While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO2) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO2 exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations.

Habitat complexity modifies the impact of piscivores on a coral reef fish population

Abstract Patterns in juvenile mortality rates can have a profound affect on the distribution and abundance of adult individuals, and may be the result of a number of interacting factors. Field observations at Lizard Island (Great Barrier Reef, Australia) showed that for a coral reef damselfish, Pomacentrus moluccensis, juvenile mortality (over 1 year) varied between 20 and almost 100% among sites. Correlative data showed that juvenile mortality increased as a function of initial densities (recruitment), predator densities and the availability of preferred coral substrata. A multiple regression showed that these three variables together did not explain significantly more variation in mortality than the single factor showing the strongest relationship. This appeared to be because recruitment, predator densities and preferred coral substrata were all highly correlated, suggesting that one, two or all of these factors may be influencing juvenile mortality rates. One hypothesis was that density-dependent mortality in juveniles was the result of an interaction between predators (which appear to aggregate at high-recruitment sites) and the availability of preferred substrata (predator refuges). We tested this hypothesis by using both laboratory and field experiments to see whether fish predation could significantly alter survivorship of this damselfish, and whether this impact was dependent upon the coral substratum. The laboratory experiment was designed to test the effects of three common predators (Pseudochromis fuscus, Cephalopholis boenak and Thalassoma lunare) and three different coral substrata that varied in their complexity (Pocillopora damicornis, Acropora nasuta and A. nobilis) on the survival of juvenile Pomacentrus moluccensis. There was a significant interaction between predator species and microhabitat in determining survival. Pseudochromis fuscus and C. boenak were both significantly better at capturing juvenile damselfish than T. lunare. Juvenile survivorship was significantly better when they were given the more complex corals, Pocillopora damicornis and A. nasuta, compared with those given the open-structured species A. nobilis. This pattern reflects habitat selection in the field. Predators differed in their strike rates and the proportion of strikes that were successful, but all exhibited greater success at prey capture where A. nobilis was provided as shelter. The interaction between the effect of predator species and microhabitat structure on damselfish survival was tested in the field for a cohort of juvenile Pomacentrus moluccensis. We examined juvenile survival in the presence and absence of two predators that co-occur on natural patch reefs (C. boenak and Pseudochromis fuscus). The experimental patch reefs we used for this purpose were constructed from both high complexity (Pocillopora damicornis) and low complexity (A. nobilis) coral substrata. Both juveniles and predators were translocated to reefs at natural densities. The effects of predation were clearly dependent upon the microhabitat. Reefs of the high-complexity coral with predators supported the same high numbers of Pomacentrus moluccensis as the reefs with no resident predators. However, damselfish abundance was significantly lower on low-complexity reefs with resident predators, relative to the other treatments. Background rates of loss were high, even on preferred coral in the absence of the manipulated predator, suggesting that transient predators may be even more important than the residents. We suggest that adult abundances in this species were strongly influenced by the densities of different predators and the availability of preferred refuges.

Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges

The extent of larval dispersal on coral reefs has important implications for the persistence of coral reef metapopulations, their resilience and recovery from an increasing array of threats, and the success of protective measures. This article highlights a recent dramatic increase in research effort and a growing diversity of approaches to the study of larval retention within (self-recruitment) and dispersal among (connectivity) isolated coral reef populations. Historically, researchers were motivated by alternative hypotheses concerning the processes limiting populations and structuring coral reef assemblages, whereas the recent impetus has come largely from the need to incorporate dispersal information into the design of no-take marine protected area (MPA) networks. Although the majority of studies continue to rely on population genetic approaches to make inferences about dispersal, a wide range of techniques are now being employed, from small-scale larval tagging and paternity analyses, to large-scale biophysical circulation models. Multiple approaches are increasingly being applied to cross-validate and provide more realistic estimates of larval dispersal. The vast majority of empirical studies have focused on corals and fishes, where evidence for both extremely local scale patterns of self-recruitment and ecologically significant connectivity among reefs at scales of tens of kilometers (and in some cases hundreds of kilometers) is accumulating. Levels of larval retention and the spatial extent of connectivity in both corals and fishes appear to be largely independent of larval duration or reef size, but may be strongly influenced by geographic setting. It is argued that high levels of both self-recruitment and larval import can contribute to the resilience of reef populations and MPA networks, but these benefits will erode in degrading reef environments.

Larval dispersal connects fish populations in a network of marine protected areas

Networks of no-take marine protected areas (MPAs) have been widely advocated for the conservation of marine biodiversity. But for MPA networks to be successful in protecting marine populations, individual MPAs must be self-sustaining or adequately connected to other MPAs via dispersal. For marine species with a dispersive larval stage, populations within MPAs require either the return of settlement-stage larvae to their natal reserve or connectivity among reserves at the spatial scales at which MPA networks are implemented. To date, larvae have not been tracked when dispersing from one MPA to another, and the relative magnitude of local retention and connectivity among MPAs remains unknown. Here we use DNA parentage analysis to provide the first direct estimates of connectivity of a marine fish, the orange clownfish (Amphiprion percula), in a proposed network of marine reserves in Kimbe Bay, Papua New Guinea. Approximately 40% of A. percula larvae settling into anemones in an island MPA at 2 different times were derived from parents resident in the reserve. We also located juveniles spawned by Kimbe Island residents that had dispersed as far as 35 km to other proposed MPAs, the longest distance that marine larvae have been directly tracked. These dispersers accounted for up to 10% of the recruitment in the adjacent MPAs. Our findings suggest that MPA networks can function to sustain resident populations both by local replenishment and through larval dispersal from other reserves. More generally, DNA parentage analysis provides a direct method for measuring larval dispersal for other marine organisms.

Adaptive management of the Great Barrier Reef: A globally significant demonstration of the benefits of networks of marine reserves

The Great Barrier Reef (GBR) provides a globally significant demonstration of the effectiveness of large-scale networks of marine reserves in contributing to integrated, adaptive management. Comprehensive review of available evidence shows major, rapid benefits of no-take areas for targeted fish and sharks, in both reef and nonreef habitats, with potential benefits for fisheries as well as biodiversity conservation. Large, mobile species like sharks benefit less than smaller, site-attached fish. Critically, reserves also appear to benefit overall ecosystem health and resilience: outbreaks of coral-eating, crown-of-thorns starfish appear less frequent on no-take reefs, which consequently have higher abundance of coral, the very foundation of reef ecosystems. Effective marine reserves require regular review of compliance: fish abundances in no-entry zones suggest that even no-take zones may be significantly depleted due to poaching. Spatial analyses comparing zoning with seabed biodiversity or dugong distributions illustrate significant benefits from application of best-practice conservation principles in data-poor situations. Increases in the marine reserve network in 2004 affected fishers, but preliminary economic analysis suggests considerable net benefits, in terms of protecting environmental and tourism values. Relative to the revenue generated by reef tourism, current expenditure on protection is minor. Recent implementation of an Outlook Report provides regular, formal review of environmental condition and management and links to policy responses, key aspects of adaptive management. Given the major threat posed by climate change, the expanded network of marine reserves provides a critical and cost-effective contribution to enhancing the resilience of the Great Barrier Reef.

Larval export from marine reserves and the recruitment benefit for fish and fisheries

Marine reserves, areas closed to all forms of fishing, continue to be advocated and implemented to supplement fisheries and conserve populations. However, although the reproductive potential of important fishery species can dramatically increase inside reserves, the extent to which larval offspring are exported and the relative contribution of reserves to recruitment in fished and protected populations are unknown. Using genetic parentage analyses, we resolve patterns of larval dispersal for two species of exploited coral reef fish within a network of marine reserves on the Great Barrier Reef. In a 1,000 km(2) study area, populations resident in three reserves exported 83% (coral trout, Plectropomus maculatus) and 55% (stripey snapper, Lutjanus carponotatus) of assigned offspring to fished reefs, with the remainder having recruited to natal reserves or other reserves in the region. We estimate that reserves, which account for just 28% of the local reef area, produced approximately half of all juvenile recruitment to both reserve and fished reefs within 30 km. Our results provide compelling evidence that adequately protected reserve networks can make a significant contribution to the replenishment of populations on both reserve and fished reefs at a scale that benefits local stakeholders.

Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs

Networks of no-take reserves are important for protecting coral reef biodiversity from climate change and other human impacts. Ensuring that reserve populations are connected to each other and non-reserve populations by larval dispersal allows for recovery from disturbance and is a key aspect of resilience. In general, connectivity between reserves should increase as the distance between them decreases. However, enhancing connectivity may often tradeoff against a network’s ability to representatively sample the system’s natural variability. This “representation” objective is typically measured in terms of species richness or diversity of habitats, but has other important elements (e.g., minimizing the risk that multiple reserves will be impacted by catastrophic events). Such representation objectives tend to be better achieved as reserves become more widely spaced. Thus, optimizing the location, size and spacing of reserves requires both an understanding of larval dispersal and explicit consideration of how well the network represents the broader system; indeed the lack of an integrated theory for optimizing tradeoffs between connectivity and representation objectives has inhibited the incorporation of connectivity into reserve selection algorithms. This article addresses these issues by (1) updating general recommendations for the location, size and spacing of reserves based on emerging data on larval dispersal in corals and reef fishes, and on considerations for maintaining genetic diversity; (2) using a spatial analysis of the Great Barrier Reef Marine Park to examine potential tradeoffs between connectivity and representation of biodiversity and (3) describing a framework for incorporating environmental fluctuations into the conceptualization of the tradeoff between connectivity and representation, and that expresses both in a common, demographically meaningful currency, thus making optimization possible.

DISTURBANCE, HABITAT STRUCTURE, AND THE DYNAMICS OF A CORAL-REEF FISH COMMUNITY

Coral reef fishes occupy habitats that are patchy and subject to frequent natural disturbances. Although different types of disturbance are likely to generate different community responses, the relationship between different disturbance agents and their effects on reef fish communities has not been examined experimentally. We studied a set of natural patch reefs, dominated by a diverse array of soft and hard coral cover, at Lizard Island on the Great Barrier Reef (northeastern Australia). The fish assemblages on the reefs were sampled over 4 mo to establish baseline values and then experimentally disturbed. Two types of disturbance were carried out in a factorial combination: pulsed mortality by removing all fish from reefs and pulsed habitat disturbance. Habitat disturbance was applied at two levels: Level 1 consisted only of damaging all live hard corals with a hammer; Level 2 consisted of damaging all live hard corals, and in addition, using a hammer to reduce the height and complexity of the reef matrix. We then monitored the experiment for a further 19 mo, including two recruitment seasons. Unmanipulated control assemblages persisted through time, and despite large changes in total abundance, species composition remained consistent relative to disturbed treatments. Assemblages disturbed by fish removal were resilient, with recolonization from both immigration and larval settlement effectively removing differences between removal treatments and controls 3 mo after manipulation. Habitat disturbance alone generated differences between experimental and control assemblages, which persisted for the duration of the experiment. The more extreme level of habitat disturbance generated more extreme changes in fish assemblages when no pulsed mortality occurred. Habitat disturbance in combination with pulsed mortality generated similar community responses as the habitat disturbance treatment alone. However, fish removal had the effect of eliminating the difference between fish assemblages on reefs subjected to different levels of habitat disturbance. Community response to habitat disturbance was driven by species-specific patterns of reduced abundance of species associated with live coral in combination with increased numbers of those associated with rubble. Declines in the abundance of coral associates on damaged reefs were abrupt, with no recovery observed for the duration of the experiment. In contrast, increases in the abundance of rubble associates were more ephemeral, in that initial high levels of recruitment and immigration were followed by a high rate of loss. Habitat disturbance also generated reefs that typically supported lower fish abundance, fewer species, and increased evenness relative to controls. Our results support a model of patch-reef fish assemblages organized by a combination of deterministic factors (such as habitat structure) and stochastic processes (such as recruitment). These disparate mechanisms operate in concert to generate reasonably consistent patterns of community structure. Habitat structure appears to mediate much of the apparent determinism and is likely to operate both as a reflection of species-specific habitat preferences and by modifying interactions among fish species. Consequently, disturbance plays a substantial role in structuring communities of coral-reef fishes by modifying both spatial and temporal heterogeneity.