Mary C. Bonin

Contrasting effects of habitat loss and fragmentation on coral‐associated reef fishes

Disturbance can result in the fragmentation and/or loss of suitable habitat, both of which can have important consequences for survival, species interactions, and resulting patterns of local diversity. However, effects of habitat loss and fragmentation are typically confounded during disturbance events, and previous attempts to determine their relative significance have proved ineffective. Here we experimentally manipulated live coral habitats to examine the potential independent and interactive effects of habitat loss and fragmentation on survival, abundance, and species richness of recruitment-stage, coral-associated reef fishes. Loss of 75% of live coral from experimental reefs resulted in low survival of a coral-associated damselfish and low abundance and richness of other recruits 16 weeks after habitat manipulations. In contrast, fragmentation had positive effects on damselfish survival and resulted in greater abundance and species richness of other recruits. We hypothesize that spacing of habitat through fragmentation weakens competition within and among species. Comparison of effect sizes over the course of the study period revealed that, in the first six weeks following habitat manipulations, the positive effects of fragmentation were at least four times stronger than the effects of habitat loss. This initial positive effect of fragmentation attenuated considerably after 16 weeks, whereas the negative effects of habitat loss increased in strength over time. There was little indication that the amount of habitat influenced the magnitude of the habitat fragmentation effect. Numerous studies have reported dramatic declines in coral reef fish abundance and diversity in response to disturbances that cause the loss and fragmentation of coral habitats. Our results suggest that these declines occur as a result of habitat loss, not habitat fragmentation. Positive fragmentation effects may actually buffer against the negative effects of habitat loss and contribute to the resistance of reef fish populations to declines in coral cover.

Specializing on vulnerable habitat: Acropora selectivity among damselfish recruits and the risk of bleaching-induced habitat loss

Coral reef habitats are increasingly being degraded and destroyed by a range of disturbances, most notably climate-induced coral bleaching. Habitat specialists, particularly those associated with susceptible coral species, are clearly among the most vulnerable to population decline or extinction. However, the degree of specialization on coral microhabitats is still unclear for one of the most ubiquitous, abundant and well studied of coral reef fish families—the damselfishes (Pomacentridae). Using high taxonomic resolution surveys of microhabitat use and availability, this study provides the first species-level description of patterns of Acropora selectivity among recruits of 10 damselfish species in order to determine their vulnerability to habitat degradation. In addition, surveys of the bleaching susceptibility of 16 branching coral species revealed which preferred recruitment microhabitats are at highest risk of decline as a result of chronic coral bleaching. Four species (i.e., Chrysiptera parasema, Pomacentrus moluccensis, Dascyllus melanurus and Chromis retrofasciata) were identified as highly vulnerable because they used only branching hard corals as recruitment habitat and primarily associated with only 2–4 coral species. The bleaching surveys revealed that five species of Acropora were highly susceptible to bleaching, with more than 50% of colonies either severely bleached or already dead. These highly susceptible corals included two of the preferred microhabitats of the specialist C. parasema and represented a significant proportion of its total recruitment microhabitat. In contrast, highly susceptible corals were rarely used by another specialist, P. moluccensis, suggesting that this species faces a lower risk of bleaching-induced habitat loss compared to C. parasema. As degradation to coral reef habitats continues, specialists will increasingly be forced to use alternative recruitment microhabitats, and this is likely to reduce population replenishment. Future research should focus on examining the fitness costs of using these alternative microhabitats.

Habitat degradation modifies the strength of interspecific competition in coral dwelling damselfishes

Habitat degradation is predicted to exacerbate competition for critical resources; however, the relationship between habitat quality and competition is poorly understood. In this study, we used a manipulative experiment to test the effects of habitat degradation on competition between two planktivorous, coral-dwelling damselfishes, Chrysiptera parasema and Dascyllus melanurus. Experimental reefs were constructed with either healthy (100% live) or degraded (10% live) Acropora longicyathus coral, stocked with varying densities of these two fish species, and monitored for two months. On healthy habitat, the mortality of C. parasema was density dependent, and increased substantially in the presence of the dominant interspecific competitor D. melanurus. In contrast, on reefs where habitat was degraded, C. parasema mortality was highly variable, density independent, and was no longer influenced by the presence of dominant competitor D. melanurus. Behavioral observations revealed that agonistic interactions for both species increased with density on degraded habitat, but not on healthy habitat. In addition, on degraded reefs, both species displayed a reduced association with reef habitat and ventured further away from shelter with increasing densities of the dominant competitor D. melanurus. These results suggest that reduced habitat quality can have such a profound effect on reef fishes, that it eliminates density-dependent mortality and competitive dominance hierarchies, thereby substantially altering the mechanisms that structure reef fish communities.

Larval fish dispersal in a coral-reef seascape

Larval dispersal is a critical yet enigmatic process in the persistence and productivity of marine metapopulations. Empirical data on larval dispersal remain scarce, hindering the use of spatial management tools in efforts to sustain ocean biodiversity and fisheries. Here we document dispersal among subpopulations of clownfish (Amphiprion percula) and butterflyfish (Chaetodon vagabundus) from eight sites across a large seascape (10,000 km2) in Papua New Guinea across 2 years. Dispersal of clownfish was consistent between years, with mean observed dispersal distances of 15 km and 10 km in 2009 and 2011, respectively. A Laplacian statistical distribution (the dispersal kernel) predicted a mean dispersal distance of 13–19 km, with 90% of settlement occurring within 31–43 km. Mean dispersal distances were considerably greater (43–64 km) for butterflyfish, with kernels declining only gradually from spawning locations. We demonstrate that dispersal can be measured on spatial scales sufficient to inform the design of and test the performance of marine reserve networks.

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.

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.

Characterization and cross-amplification of microsatellite markers in four species of anemonefish (Pomacentridae, Amphiprion spp .)

Anemonefish are iconic symbols of coral reefs and have become model systems for research on larval dispersal and population connectivity in coral reef fishes. Here we present 24 novel microsatellite markers across four species of anemonefish and also test 35 previously published markers for cross-amplification on two anemonefish species in order to facilitate further research on their population genetics and phylogenetics. Novel loci were isolated from sequences derived from microsatellite-enriched or 454 GS-FLX shotgun sequence libraries developed using congeneric DNA. Primer testing successfully identified 15 new microsatellite loci for A. percula, 4 for A. melanopus, 3 for A. akindynos, and 2 for A. omanensis. These novel microsatellite loci were polymorphic with a mean of 10 ± 1.6 SE (standard error) alleles per locus and an average observed heterozygosity of 0.647 ± 0.032 SE. Reliable cross-amplification of 12 and 26 of the 35 previously published Amphiprion markers was achieved for A. melanopus and A. akindynos, respectively, suggesting that the use of markers developed from the DNA of congeners can provide a quick and cost-effective alternative to the isolation of new loci. Together, the markers presented here provide an important resource for ecological, evolutionary, and conservation genetic research on anemonefishes that will inform broader conservation and management actions for coral reef fishes.

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.

CORAL‐ASSOCIATED REEF FISHES

Many organisms are in decline due to the degradation of their natural habitat. Although it is often assumed that habitat loss and fragmentation are the cause of these declines, the independent effects of these two processes are rarely known. Using an array of experimental patch reefs, we measured and compared the effects of habitat loss and fragmentation on coral-associated damselfishes. We discovered that although 75% habitat loss resulted in low recruitment and survival compared to control reefs, habitat fragmentation actually improved damselfish recruitment and survival. These results suggest that habitat loss, not fragmentation, is the primary threat following habitat disturbance.