Integrating complementary methods to improve diet analysis in fishery-targeted species.

Developing efficient, reliable, cost-effective ways to identify diet is required to understand trophic ecology in complex ecosystems and improve food web models. A combination of techniques, each varying in their ability to provide robust, spatially and temporally explicit information can be applied to clarify diet data for ecological research. This study applied an integrative analysis of a fishery-targeted species group-Plectropomus spp. in the central Great Barrier Reef, Australia, by comparing three diet-identification approaches. Visual stomach content analysis provided poor identification with ~14% of stomachs sampled resulting in identification to family or lower. A molecular approach was successful with prey from ~80% of stomachs identified to genus or species, often with several unique prey in a stomach. Stable isotope mixing models utilizing experimentally derived assimilation data, identified similar prey as the molecular technique but at broader temporal scales, particularly when prior diet information was incorporated. Overall, Caesionidae and Pomacentridae were the most abundant prey families (>50% prey contribution) for all Plectropomus spp., highlighting the importance of planktivorous prey. Less abundant prey categories differed among species/color phases indicating possible niche segregation. This study is one of the first to demonstrate the extent of taxonomic resolution provided by molecular techniques, and, like other studies, illustrates that temporal investigations of dietary patterns are more accessible in combination with stable isotopes. The consumption of mainly planktivorous prey within this species group has important implications within coral reef food webs and provides cautionary information regarding the effects that changing resources could have in reef ecosystems.

Rising temperatures may drive fishing-induced selection of low-performance phenotypes.

Climate warming is likely to interact with other stressors to challenge the physiological capacities and survival of phenotypes within populations. This may be especially true for the billions of fishes per year that undergo vigorous exercise prior to escaping or being intentionally released from fishing gear. Using adult coral grouper (Plectropomus leopardus), an important fisheries species throughout the Indo-Pacific, we show that population-level survival following vigorous exercise is increasingly compromised as temperatures increase from current-day levels (100-67% survival at 24-30 °C) to those projected for the end of the century (42% survival at 33 °C). Intriguingly, we demonstrate that high-performance individuals take longer to recover to a resting metabolic state and subsequently have lower survival in warm water compared with conspecifics that exercise less vigorously. Moreover, we show that post-exercise mortality of high-performance phenotypes manifests after 3-13 d at the current summer maximum (30 °C), while mortality at 33 °C occurs within 1.8-14.9 h. We propose that wild populations in a warming climate may become skewed towards low-performance phenotypes with ramifications for predator-prey interactions and community dynamics. Our findings highlight the susceptibility of phenotypic diversity to fishing activities and demonstrate a mechanism that may contribute to fishing-induced evolution in the face of ongoing climate change.

Global warming may disproportionately affect larger adults in a predatory coral reef fish.

Global warming is expected to reduce body sizes of ectothermic animals. Although the underlying mechanisms of size reductions remain poorly understood, effects appear stronger at latitudinal extremes (poles and tropics) and in aquatic rather than terrestrial systems. To shed light on this phenomenon, we examined the size dependence of critical thermal maxima (CTmax) and aerobic metabolism in a commercially important tropical reef fish, the leopard coral grouper (Plectropomus leopardus) following acclimation to current-day (28.5 °C) vs. projected end-of-century (33 °C) summer temperatures for the northern Great Barrier Reef (GBR). CTmax declined from 38.3 to 37.5 °C with increasing body mass in adult fish (0.45-2.82 kg), indicating that larger individuals are more thermally sensitive than smaller conspecifics. This may be explained by a restricted capacity for large fish to increase mass-specific maximum metabolic rate (MMR) at 33 °C compared with 28.5 °C. Indeed, temperature influenced the relationship between metabolism and body mass (0.02-2.38 kg), whereby the scaling exponent for MMR increased from 0.74 ± 0.02 at 28.5 °C to 0.79 ± 0.01 at 33 °C, and the corresponding exponents for standard metabolic rate (SMR) were 0.75 ± 0.04 and 0.80 ± 0.03. The increase in metabolic scaling exponents at higher temperatures suggests that energy budgets may be disproportionately impacted in larger fish and contribute to reduced maximum adult size. Such climate-induced reductions in body size would have important ramifications for fisheries productivity, but are also likely to have knock-on effects for trophodynamics and functioning of ecosystems.

Effects of Including Misidentified Sharks in Life History Analyses: A Case Study on the Grey Reef Shark Carcharhinus amblyrhynchos from Papua New Guinea.

Fisheries observer programs are used around the world to collect crucial information and samples that inform fisheries management. However, observer error may misidentify similar-looking shark species. This raises questions about the level of error that species misidentifications could introduce to estimates of species' life history parameters. This study addressed these questions using the Grey Reef Shark Carcharhinus amblyrhynchos as a case study. Observer misidentification rates were quantified by validating species identifications using diagnostic photographs taken on board supplemented with DNA barcoding. Length-at-age and maturity ogive analyses were then estimated and compared with and without the misidentified individuals. Vertebrae were retained from a total of 155 sharks identified by observers as C. amblyrhynchos. However, 22 (14%) of these were sharks were misidentified by the observers and were subsequently re-identified based on photographs and/or DNA barcoding. Of the 22 individuals misidentified as C. amblyrhynchos, 16 (73%) were detected using photographs and a further 6 via genetic validation. If misidentified individuals had been included, substantial error would have been introduced to both the length-at-age and the maturity estimates. Thus validating the species identification, increased the accuracy of estimated life history parameters for C. amblyrhynchos. From the corrected sample a multi-model inference approach was used to estimate growth for C. amblyrhynchos using three candidate models. The model averaged length-at-age parameters for C. amblyrhynchos with the sexes combined were L∞ = 159 cm TL and L0 = 72 cm TL. Females mature at a greater length (l50 = 136 cm TL) and older age (A50 = 9.1 years) than males (l50 = 123 cm TL; A50 = 5.9 years). The inclusion of techniques to reduce misidentification in observer programs will improve the results of life history studies and ultimately improve management through the use of more accurate data for assessments.

Evidence of Partial Migration in a Large Coastal Predator: Opportunistic Foraging and Reproduction as Key Drivers?

Understanding animal movement decisions that involve migration is critical for evaluating population connectivity, and thus persistence. Recent work on sharks has shown that often only a portion of the adult population will undertake migrations, while the rest may be resident in an area for long periods. Defining the extent to which adult sharks use specific habitats and their migratory behaviour is essential for assessing their risk of exposure to threats such as fishing and habitat degradation. The present study used acoustic telemetry to examine residency patterns and migratory behaviour of adult bull sharks (Carcharhinus leucas) along the East coast of Australia. Fifty-six VR2W acoustic receivers were used to monitor the movements of 33 bull sharks in the central Great Barrier Reef (GBR). Both males and females were detected year-round, but their abundance and residency peaked between September and December across years (2012-2014). High individual variability in reef use patterns was apparent, with some individuals leaving the array for long periods, whereas others (36%) exhibited medium (0.20-0.40) or high residency (> 0.50). A large portion of the population (51%) undertook migrations of up to 1,400 km to other coral reefs and/or inshore coastal habitats in Queensland and New South Wales. Most of these individuals (76%) were mature females, and the timing of migrations coincided with the austral summer (Dec-Feb). All migrating individuals (except one) returned to the central GBR, highlighting its importance as a potential foraging ground. Our findings suggest that adult bull sharks appear to be highly dependent on coral reef resources and provide evidence of partial migration, where only a portion of the female population undertook seasonal migrations potentially to give birth. Given that estuarine habitats face constant anthropogenic pressures, understanding partial migration and habitat connectivity of large coastal predators should be a priority for their management.

Dynamic habitat suitability modelling reveals rapid poleward distribution shift in a mobile apex predator.

Many taxa are undergoing distribution shifts in response to anthropogenic climate change. However, detecting a climate signal in mobile species is difficult due to their wide-ranging, patchy distributions, often driven by natural climate variability. For example, difficulties associated with assessing pelagic fish distributions have rendered fisheries management ill-equipped to adapt to the challenges posed by climate change, leaving pelagic species and ecosystems vulnerable. Here, we demonstrate the value of citizen science data for modelling the dynamic habitat suitability of a mobile pelagic predator (black marlin, Istiompax indica) within the south-west Pacific Ocean. The extensive spatial and temporal coverage of our occurrence data set (n = 18 717), collected at high resolution (~1.85 km(2) ), enabled identification of suitable habitat at monthly time steps over a 16-year period (1998-2013). We identified considerable monthly, seasonal and interannual variability in the extent and distribution of suitable habitat, predominately driven by chlorophyll a and sea surface height. Interannual variability correlated with El Nino Southern Oscillation (ENSO) events, with suitable habitat extending up to ~300 km further south during La Nina events. Despite the strong influence of ENSO, our model revealed a rapid poleward shift in the geometric mean of black marlin habitat, occurring at 88.2 km decade(-1) . By incorporating multiple environmental factors at monthly time steps, we were able to demonstrate a rapid distribution shift in a mobile pelagic species. Our findings suggest that the rapid velocity of climate change in the south-west Pacific Ocean is likely affecting mobile pelagic species, indicating that they may be more vulnerable to climate change than previously thought.

Ecological drivers of shark distributions along a tropical coastline.

As coastal species experience increasing anthropogenic pressures there is a growing need to characterise the ecological drivers of their abundance and habitat use, and understand how they may respond to changes in their environment. Accordingly, fishery-independent surveys were undertaken to investigate shark abundance along approximately 400 km of the tropical east coast of Australia. Generalised linear models were used to identify ecological drivers of the abundance of immature blacktip Carcharhinus tilstoni/Carcharhinus limbatus, pigeye Carcharhinus amboinensis, and scalloped hammerhead Sphyrna lewini sharks. Results indicated general and species-specific patterns in abundance that were characterised by a range of abiotic and biotic variables. Relationships with turbidity and salinity were similar across multiple species, highlighting the importance of these variables in the functioning of communal shark nurseries. In particular, turbid environments were especially important for all species at typical oceanic salinities. Mangrove proximity, depth, and water temperature were also important; however, their influence varied between species. Ecological drivers may promote spatial diversity in habitat use along environmentally heterogeneous coastlines and may therefore have important implications for population resilience.

Contrasting movements and connectivity of reef-associated sharks using acoustic telemetry: implications for management.

Understanding the efficacy of marine protected areas (MPAs) for wide-ranging predators is essential to designing effective management and conservation approaches. The use of acoustic monitoring and network analysis can improve our understanding of the spatial ecology and functional connectivity of reef-associated species, providing a useful approach for reef-based conservation planning. This study compared and contrasted the movement and connectivity of sharks with different degrees of reef association. We examined the residency, dispersal, degree of reef connectivity, and MPA use of grey reef (Carcharhinus amblyrhynchos), silvertip (C. albimarginatus), and bull (C. leucas) sharks monitored in the central Great Barrier Reef (GBR). An array of 56 acoustic receivers was used to monitor shark movements on 17 semi-isolated reefs. Carcharhinus amblyrhynchos and C. albimarginatus were detected most days at or near their tagging reef. However, while C. amblyrhynchos spent 80% of monitoring days in the array, C. albimarginatus was only detected 50% of the time. Despite both species moving similar distances (< 50 km), a large portion of the population of C. albimarginatus (71%) was detected on multiple reefs and moved more frequently between reefs and management zones than C. amblyrhynchos. Carcharhinus leucas was detected less than 20% of the time within the tagging array, and 42% of the population undertook long-range migrations to other arrays in the GBR. Networks derived for C. leucas were larger and more complex than those for C. amblyrhynchos and C. albimarginatus. Our findings suggest that protecting specific reefs based on prior knowledge (e.g., healthier reefs with high fish biomass) and increasing the level of protection to include nearby, closely spaced reef habitats (< 20 km) may perform better for species like C. albimarginatus than having either a single or a network of isolated MPAs. This design would also provide protection for larger male C. amblyrhynchos, which tend to disperse more and use larger areas than females. For wide-ranging sharks like C. leucas, a combination of spatial planning and other alternative measures is critical. Our findings demonstrate that acoustic monitoring can serve as a useful platform for designing more effective MPA networks for reef predators displaying a range of movement patterns.

Quantifying shark distribution patterns and species-habitat associations: implications of marine park zoning.

Quantifying shark distribution patterns and species-specific habitat associations in response to geographic and environmental drivers is critical to assessing risk of exposure to fishing, habitat degradation, and the effects of climate change. The present study examined shark distribution patterns, species-habitat associations, and marine reserve use with baited remote underwater video stations (BRUVS) along the entire Great Barrier Reef Marine Park (GBRMP) over a ten year period. Overall, 21 species of sharks from five families and two orders were recorded. Grey reef Carcharhinus amblyrhynchos, silvertip C. albimarginatus, tiger Galeocerdo cuvier, and sliteye Loxodon macrorhinus sharks were the most abundant species (>64% of shark abundances). Multivariate regression trees showed that hard coral cover produced the primary split separating shark assemblages. Four indicator species had consistently higher abundances and contributed to explaining most of the differences in shark assemblages: C. amblyrhynchos, C. albimarginatus, G. cuvier, and whitetip reef Triaenodon obesus sharks. Relative distance along the GBRMP had the greatest influence on shark occurrence and species richness, which increased at both ends of the sampling range (southern and northern sites) relative to intermediate latitudes. Hard coral cover and distance across the shelf were also important predictors of shark distribution. The relative abundance of sharks was significantly higher in non-fished sites, highlighting the conservation value and benefits of the GBRMP zoning. However, our results also showed that hard coral cover had a large effect on the abundance of reef-associated shark species, indicating that coral reef health may be important for the success of marine protected areas. Therefore, understanding shark distribution patterns, species-habitat associations, and the drivers responsible for those patterns is essential for developing sound management and conservation approaches.

Refuge-seeking impairments mirror metabolic recovery following fisheries-related stressors in the Spanish flag snapper (Lutjanus carponotatus) on the Great Barrier Reef.

Fisheries and marine park management strategies for large predatory reef fish can mean that a large proportion of captured fish are released. Despite being released, these fish may experience high mortality while they traverse the water column to locate suitable refuge to avoid predators, all the while recovering from the stress of capture. The predatory reef fish Spanish flag snapper (Lutjanus carponotatus) is frequently released because of a minimum-size or bag limit or by fishers targeting more desirable species. Using L. carponotatus as a model, we tested whether simulated fishing stress (exercise and air exposure) resulted in impairments in reflexes (e.g., response to stimuli) and the ability to identify and use refuge in a laboratory arena and whether any impairments were associated with blood physiology or metabolic recovery. Control fish were consistently responsive to reflex tests and rapidly located and entered refugia in the arena within seconds. Conversely, treatment fish (exhausted and air exposed) were unresponsive to stimuli, took longer to search for refugia, and were more apprehensive to enter the refuge once it was located. Consequently, treatment fish took more than 70 times longer than control fish to enter the coral refuge (26.12 vs. 0.36 min, respectively). The finding that fish exposed to stress were hesitant to use refugia suggests that there was likely cognitive, visual, and/or physiological impairment. Blood lactate, glucose, and hematocrit measures were perturbed at 15 and 30 min after the stressor, relative to controls. However, measurements of oxygen consumption rate revealed that about 50% of metabolic recovery occurred within 30 min after the stressor, coinciding with apparent cognitive/visual/physiological recovery. Recovering the treatment fish in aerated, flow-through chambers for 30 min before introduction to the behavioral arena restored reflexes, and "recovered" fish behaved more similarly to controls. Therefore, we suggest that temporarily holding coral reef fish that have undergone an exhaustive fishing interaction and an air exposure episode should enable significant recovery of cognitive and metabolic attributes that would enable fish to more rapidly locate and utilize refugia to avoid postrelease predation. However, after nonexhaustive fishing interactions (i.e., minimal reflex impairment), it is likely that immediate release would be most beneficial.