Partitioning no-take marine reserve (NTMR) and benthic habitat effects on density of small and large-bodied tropical wrasses

No-take marine reserves (NTMRs) are increasingly implemented for fisheries management and biodiversity conservation. Yet, assessing NTMR effectiveness depends on partitioning the effects of NTMR protection and benthic habitat on protected species. Such partitioning is often difficult, since most studies lack well-designed sampling programs (i.e. Before-After-Control-Impact-Pair designs) spanning long-term time scales. Spanning 31 years, this study quantifies the effects of NTMR protection and changes to benthic habitat on the density of tropical wrasses (F. Labridae) at Sumilon and Apo Islands, Philippines. Five species of wrasse were studied: two species of large-bodied (40-50 cm TL) Hemigymnus that were vulnerable to fishing, and three species of small-bodied (10-25 cm TL) Thalassoma and Cirrhilabrus that were not targeted by fishing. NTMR protection had no measurable effect on wrasse density, irrespective of species or body size, over 20 (Sumilon) and 31 (Apo) years of protection. However, the density of wrasses was often affected strongly by benthic cover. Hemigymnus spp. had a positive association with hard coral cover, while Thalassoma spp. and Cirrhilabrus spp. had strong positive associations with cover of rubble and dead substratum. These associations were most apparent after environmental disturbances (typhoons, coral bleaching, crown of thorns starfish (COTS) outbreaks, use of explosives and drive nets) reduced live hard coral cover and increased cover of rubble, dead substratum and sand. Disturbances that reduced hard coral cover often reduced the density of Hemigymnus spp. and increased the density of Thalassoma spp. and Cirrhilabrus spp. rapidly (1-2 years). As hard coral recovered, density of Hemigymnus spp. often increased while density of Thalassoma spp. and Cirrhilabrus spp. often decreased, often on scales of 5-10 years. This study demonstrates that wrasse population density was influenced more by changes to benthic cover than by protection from fishing

Trophic impact of large predators on coral reefs and management implications

Apex predators such as lions, wolves and orcas occupy the top of food chains and are known to exert strong top-down control of prey abundance, community structure and ecosystem productivity. Despite the importance of apex predators in both terrestrial and oceanic habitats, there is a paucity of information on this guild for coral reef ecosystems. Sharks are among the largest predators on coral reefs and may function as apex predators, but our understanding of the ecological role and importance of these organisms is poor. Recent declines in shark populations are also leading to concerns that these potentially important species may be effectively lost from reef systems before we realise their role in ecosystem dynamics. Thus, the overall focus of this thesis was to examine the status, trophic role and importance of large predators, namely reef sharks, on coral reefs, thereby providing management with improved tools for understanding how the removal of predators via fishing influences ecosystem properties. The high mobility and generally low abundances of reef sharks has led to considerable debate regarding the optimal method/s for assessing their population status. Due to controversy surrounding previous stock assessments, the focus of Chapter 2 was to evaluate potential biases in five survey methods (timed-swim, towed-diver, baited-remote-underwater- video, stationary-point-count, and audible-stationary-count) for assessing reef shark populations, and whether these biases (if any) vary among reefs that are subject to different levels of human interaction due to conservation zoning. For timed-swim, towed-diver, and baited-remote-underwater-video (BRUV) surveys, shark encounter rates were constant over time, suggesting minimal bias caused by, for example, shark attraction to divers. For audible-stationary-count (ASC) surveys, encounter rates were elevated initially, then decreased rapidly, but the extent of upward bias did not differ between management zones. Timed-swim, BRUV, and ASC surveys produced comparable estimates of shark density, however, towed-diver-surveys produced significantly lower estimates of shark density. These findings provide no evidence for biases in diver-surveys: encounter rates with sharks were not elevated when divers first entered the water; behavioural responses of sharks were consistent across management zones; and diver-surveys yielded abundance estimates comparable to stationary non-diver surveys. These results indicate that estimates of abundance generated by diver-surveys such as underwater visual transects are reliable, minimally biased, and suitable for assessing shark populations in the field. Quantifying the distribution and habitat use of sharks is critical for estimating their population sizes, understanding their ecological role, and for establishing appropriate conservation and management regimes. The goal of Chapter 3 was to survey shark populations across outer-shelf reefs of the Great Barrier Reef (GBR) in order to determine the diversity, abundance, and distribution of reef sharks across three major coral reef habitats: (1) the reef slope, (2) the back reef and (3) the reef flat. Results revealed that, of the variables that were examined, habitat was the best predictor of shark distribution and abundance. Specifically, overall shark abundance and diversity were significantly higher on the reef slope (and to a lesser degree, the back reef) than the reef flat. These results confirm that shark populations are not homogeneously distributed across coral reefs and also highlight the potential importance of the reef slope, with high levels of live coral cover, structural complexity, and diversity of potential prey species for sustaining reef shark populations. The goal of Chapter 4 was to examine the top-down influence of reef sharks and mesopredators (predatory teleost fishes) on herbivores across a large spatial gradient. The abundance, size structure, and biomass of apex predators, mesopredators, and herbivores across fished, no-take, and no-entry management zones of the GBR were estimated. Shark abundance and mesopredator size and biomass were higher in no-entry zones than in fished and no-take zones, which indicates the viability of strictly enforced human exclusion areas as tools for the conservation of predator communities. However, changes in predator populations due to protection in no-entry zones did not have a discernible influence on the density, size, or biomass of different functional groups of herbivorous fishes. The lack of a relationship between predators and herbivores suggests that top-down forces may be much weaker than previously thought and that food web models developed for terrestrial systems may not be appropriate for describing reef communities across large spatial scales. Using life-like models of a reef shark and another large predatory fish (coral-grouper), Chapter 5 examined the indirect effects of large predators on herbivore foraging behaviour and algal consumption. This study found that the presence of a model blacktip reef shark (1.7m length) or large coral-grouper (76 cm length) led to a substantial reduction in bite rate and species richness of herbivorous fishes feeding on a macroalgal thallus in the vicinity of the predator. The perceived risk of predation led to a near absolute localized cessation of macroagal removal. A smaller-sized model coral-grouper (48 cm length) also reduced herbivore diversity and activity but to a lesser degree than the larger model predators. These results highlight that the indirect effects of large predators on the foraging behaviour of herbivores may have flow-on effects on the biomass and distribution of macroalgae on a localized scale. Combined with the results of Chapter 4, this highlights that the ecological interactions and processes that contribute to ecosystem resilience may be more complex than previously assumed. Due to their large size and conspicuous predatory behaviour, reef sharks are typically assumed to be apex predators on coral reefs, but this title is tenuous because little is known about their trophic ecology and functional role. In Chapter 6 stomach contents and stable isotope ratios (δ13Carbon and δ15Nitrogen) were used to estimate diet, trophic level and sources of primary production of three reef sharks (Triaenodon obesus, Carcharhinus melanopterus and Carcharhinus amblyrhynchos) from the GBR. Their assumed functional roles as apex predators were evaluated by qualitative and quantitative comparisons with other sharks and large predatory fishes. It was found that reef sharks do not occupy the apex of coral reef food chains, but instead appear to have functional roles similar to those of large predatory fishes, which are typically regarded as high-level mesopredators. These findings suggest that a high degree of functional redundancy may exist within this guild of large predators, potentially explaining why shark-induced trophic cascades are rare or subtle in coral reef ecosystems. Furthermore, these results indicate that reef sharks should be reassigned to an alternative trophic group such as mesopredators. This change will increase the accuracy of ecosystem models, providing resource managers with improved tools for understanding how reef communities function and how removal of predators might affect ecosystem properties. The current body of work has advanced our understanding of reef sharks, particularly in terms of their response to protection from fishing, spatial distribution, behaviour towards divers and their functional roles on coral reefs. This thesis demonstrates that reef sharks respond positively to protection from fishing but that the flow-on effects to lower trophic levels are variable and inconsistent with theory surrounding trophic cascades. These advances will be important for improving ecosystem-based management strategies that aim to conserve not only individual species, but also their functions and interactions. Such an approach is paramount given that coral reefs around the globe face ever-intensifying human-induced threats such as overfishing and climate change

Supply risk of bait in Australia\u27s Southern Rock Lobster Fishery

Bait is an often-overlooked component in studies addressing operational and ecological risks in commercial fishing. One of the most valued fisheries in Australia, the Southern Rock Lobster Fishery, lacked analysis of bait use, which is relevant to both assessing ecological interactions of the fishery and also concerns around future supply. We conducted a survey to determine what species are predominantly being used as bait, assessed these species' sustainability status, and explored any risks around future supply. We found that fishers preferred a limited number of bait species and that some were being sourced from fisheries with an ‘unknown’ sustainability status, and many fishers were concerned about future bait supply. Insecurity of existing supply means that other bait options need to be explored. Furthermore, ongoing monitoring of species being used for bait would assist any future third party sustainability accreditation

Parks for sharks: human exclusion areas outperform no‐take marine reserves

We collected reef shark population data from a large network of no-take and no-entry reserves (ie human exclusion areas), as well as from fished reefs, in one of the world's most intensively managed marine parks - the Great Barrier Reef of Australia. The sampled reserves have been protected for varying lengths of time, making it possible to use space-for-time chronosequences to infer recovery trajectories of reef shark populations after extractive use is banned, and to compare the effectiveness of shark population recovery in no-take and no-entry reserves. After 20-40 years of protection, density and biomass of sharks in no-entry reserves approached asymptotes (ie plateaus) that were more than double and triple, respectively, those in no-take reserves. These results not only indicate that restoration of near-natural shark populations requires multidecadal time frames, but also clearly demonstrate the superior performance of no-entry reserves in terms of rebuilding shark populations. Ongoing poaching in no-take reserves, which are more difficult for law enforcement to police than no-entry reserves, is the probable cause of the disparity. Given the ubiquitous use of no-take reserves as ecological baselines and the potentially pervasive trophic effects of removing large predators, we argue that current perceptions of the structure and function of natural reef ecosystems may be skewed, which has broad implications for science and management of marine ecosystems

Indirect predator effects influence behaviour but not morphology of juvenile coral reef Ambon damselfish Pomacentrus amboinensis

A 6-week laboratory experiment exposed juvenile Ambon damselfish Pomacentrus amboinensis to visual and chemical cues of either a predator, a herbivore or a null control (sea water) and found no effect of predator cues on prey morphology (proportion of ocellus to eye diameter, body depth, standard length and fin area). Nonetheless, behaviour was significantly affected by predator presence, with prey less active and taking half as many feeding strikes when exposed to predators compared to fish from the null control. The presence of a herbivore also affected prey behaviour similar to that of the predator, suggesting that the presence of a non-predator may have important effects on development

How robust are estimates of coral reef shark depletion?

On coral reefs, diver-surveys of shark abundance indicate that populations are severely depleted, even in no-take zones with low-levels of illegal fishing, but are protected by strictly enforced no-entry zones. These findings have been questioned, on the grounds that diver-surveys overestimate shark abundance. We evaluated whether divers encounter sharks at higher rates when they first enter the water, and whether these effects vary among reefs that are subject to different levels of human interaction due to management zoning. We also examined the consistency of abundance estimates derived from multiple survey methods. For timed-swim, towed-diver, and baited-remote-underwater-video (BRUV) surveys, encounter rates were constant over time. For audible-stationary-count (ASC) surveys, encounter rates were elevated initially, then decreased rapidly, but the extent of upward bias did not differ between management zones. Timed-swim, BRUV, and ASC surveys produced comparable estimates of shark density, however, towed-diver-surveys produced significantly lower estimates of shark density. Our findings provide no evidence for biases in diver-surveys: encounter rates with sharks were not elevated when divers first entered the water; behavioural responses of sharks were consistent across management zones; and diver-surveys yielded abundance estimates comparable to other stationary methods. Previous studies using underwater counts have concluded that sharks are vulnerable to low levels of illegal fishing in no-take management zones, and that additional measures are needed to protect species, which, like sharks, have demographic characteristics that make them vulnerable to low levels of exploitation. Our results support the robustness of the abundance estimates on which those conclusions have been based

Diversity, abundance, and distribution of reef sharks on outer-shelf reefs of the Great Barrier Reef, Australia

Quantifying the distribution and habitat use of sharks is critical for understanding their ecological role and for establishing appropriate conservation and management regimes. On coral reefs, particularly the Great Barrier Reef (GBR), little is known regarding the distribution of sharks across major reef habitat types. In this study, we surveyed shark populations across outer-shelf reefs of the GBR in order to determine the diversity, abundance, and distribution of reef sharks across three major coral reef habitats: (1) the reef slope, (2) the back reef and (3) the reef flat. Model selection revealed that habitat was the principal factor influencing shark distribution and abundance. Specifically, overall shark abundance and diversity were significantly higher on the reef slope (and to a lesser degree, the back reef) than the reef flat. This confirms that shark populations are not homogeneously distributed across coral reefs. Thus, the results presented herein have important implications for shark population assessments. In addition, our results highlight the potential importance of the reef slope, with high levels of live coral cover and structural complexity, for sustaining reef shark populations. As this habitat is highly susceptible to disturbance events, this study provides a useful context for predicting and understanding how environmental degradation may influence reef shark populations in the future

Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs

Apex predators are declining at alarming rates due to exploitation by humans, but we have yet to fully discern the impacts of apex predator loss on ecosystem function. In a management context, it is critically important to clarify the role apex predators play in structuring populations of lower trophic levels. Thus, we examined the top-down influence of reef sharks (an apex predator on coral reefs) and mesopredators on large-bodied herbivores. We measured the abundance, size structure, and biomass of apex predators, mesopredators, and herbivores across fished, no-take, and no-entry management zones in the Great Barrier Reef Marine Park, Australia. Shark abundance and mesopredator size and biomass were higher in no-entry zones than in fished and no-take zones, which indicates the viability of strictly enforced human exclusion areas as tools for the conservation of predator communities. Changes in predator populations due to protection in no-entry zones did not have a discernible influence on the density, size, or biomass of different functional groups of herbivorous fishes. The lack of a relationship between predators and herbivores suggests that top-down forces may not play a strong role in regulating large-bodied herbivorous coral reef fish populations. Given this inconsistency with traditional ecological theories of trophic cascades, trophic structures on coral reefs may need to be reassessed to enable the establishment of appropriate and effective management regimes

Long-term no-take marine reserve and benthic habitat effects on coral reef fishes

No-take marine reserves (NTMRs) are advocated as tools to enhance or maintain density and assemblage structure of coral reef fishes. These reef fish population and assemblage attributes may be affected by both NTMR protection and benthic habitat change. Before-after-control-impact-pair (BACIP) sampling designs and long-term (8-30 yr) monitoring at 4 Philippine NTMRs were used to examine the relative effects of NTMR protection and benthic habitat change on densities and assemblage structures of fishery-targeted (Lethrinidae and Lutjanidae) and non-targeted (Pomacentridae) reef fishes. Targeted fish density increased significantly in NTMRs relative to fished control sites at all reserves over time. Non-targeted fish density and hard coral cover displayed a variety of patterns of change over time (unrelated to NTMR protection), but closely mirrored each other. Targeted fish were considered potential predators of non-targeted fish. Availability of potential prey for predators had a larger influence than the effect of potential predators on prey, with both processes much weaker than effects of habitat change. Multivariate analyses of long-term temporal data indicated that 65.8% of the variance in assemblage structure of non-targeted pomacentrids was explained by benthic habitat variables (structural complexity, cover of dead substrate) whereas NTMR protection alone explained only 9.7%. In contrast, 36.2% of assemblage structure of targeted lethrinids/lutjanids was explained by duration of NTMR protection (42.2% excluding effects of typhoons at one reserve), with habitat variables alone explaining 24.7%. These results help clarify the relative effects of NTMR protection, benthic habitat change, and potential trophic interactions on reef fishes targeted and non-targeted by fishing

Decadal-scale effects of benthic habitat and marine reserve protection on Philippine goatfish (F: Mullidae)

Reef fish populations can be affected by both fishing and changes in benthic habitat. Yet, partitioning these effects is often difficult, usually requiring an appropriate sampling design and long-term monitoring. Here we quantify, over a 30-yr period, the effects of benthic habitat change and no-take marine reserve (NTMR) protection on the density and species richness of a lightly harvested benthic-feeding reef fish family, the Mullidae (goatfish), at four Philippine islands. Boosted regression trees demonstrated that goatfish density and species richness had strong negative associations with hard coral cover and strong positive associations with cover of dead substratum. No-take marine reserve protection had no effect on the density or species richness of goatfish over 19 and 30 yr at Sumilon and Apo islands, respectively. However, environmental disturbances (e.g., typhoons, coral bleaching) that reduced hard coral cover subsequently led to increases in goatfish numbers for periods ranging from 2 to 8 yr. After initial increases due to benthic disturbance, goatfish populations decreased during coral recovery, occurring on timescales of 10-20 yr. This long-term, "natural experiment" demonstrated that changes to benthic habitat (bottom-up control) had a far greater effect on Philippine goatfish populations than protection from fishing (a top-down effect) in NTMRs. Given the strong positive response of goatfish populations to loss of live hard coral cover, this group of fishes may be a valuable indicator species for habitat degradation on coral reefs