Intraguild processes drive space-use patterns in a large-bodied marine predator community.

Interspecific interactions, including predator-prey, intraguild predation (IGP) and competition, may drive distribution and habitat use of predator communities. However, elucidating the relative importance of these interactions in shaping predator distributions is challenging, especially in marine communities comprising highly mobile species. We used individual-based models (IBMs) to predict the habitat distributions of apex predators, intraguild (IG) prey and prey. We then used passive acoustic telemetry to test these predictions in a subtropical marine predator community consisting of eight elasmobranch (i.e. shark and ray) species in Bimini, The Bahamas. IBMs predicted that prey and IG prey will preferentially select habitats based on safety over resources (food), with stronger selection for safe habitat by smaller prey. Elasmobranch space-use patterns matched these predictions. Species with predator-prey and asymmetrical IGP (between apex and small mesopredators) interactions showed the clearest spatial separation, followed by asymmetrical IGP among apex and large mesopredators. Competitors showed greater spatial overlap although with finer-scale differences in microhabitat use. Our study suggests space-use patterns in elasmobranchs are at least partially driven by interspecific interactions, with stronger spatial separation occurring where interactions include predator-prey relationships or IGP.

Elucidating the role of competition in driving spatial and trophic niche patterns in sympatric juvenile sharks.

The coexistence of ecologically and morphologically similar species is often facilitated by the partitioning of ecological niches. While subordinate species can reduce competition with dominant competitors through spatial and/or trophic segregation, empirical support from wild settings, particularly those involving large-bodied taxa in marine ecosystems, are rare. Shark nursery areas provide an opportunity to investigate the mechanisms of coexistence. We used experimental and field studies of sympatric juvenile sharks (blacktip reef shark, Carcharhinus melanopterus; sicklefin lemon shark, Negaprion acutidens) to investigate how competitive ability influenced realized niches at St. Joseph Atoll, Seychelles. Captive trials revealed that sicklefin lemon sharks were dominant over blacktip reef sharks, consistently taking food rewards. In the field, blacktip reef sharks were captured over a broader area than sicklefin lemon sharks, but daily space use of actively tracked sharks showed a high degree of overlap across microhabitats. While stomach contents analysis revealed that blacktip reef shark diets included a broader range of prey items, stable isotope analysis demonstrated significantly higher mean δ13C values for sicklefin lemon sharks, suggesting diverging dietary preferences. Overall, our results matched theoretical predictions of subordinate competitors using a greater range of habitats and displaying broader feeding niches than competitively dominant species. While separating the realized and fundamental niche of marine predators is complicated, we provide evidence that resource partitioning is at least partially driven by interspecific competition.

Incorporating thermodynamics in predator-prey games predicts the diel foraging patterns of poikilothermic predators.

Models of foraging behaviour typically assume that prey do not adapt to temporal variation in predation risk, such as by avoiding foraging at certain times of the day. When this behavioural plasticity is considered-such as in predator-prey games-the role of abiotic factors is usually ignored. An abiotic factor that exerts strong influence on the physiology and behaviour of many animals is ambient temperature, although it is often ignored from game models as it is implicitly assumed that both predators and prey are homothermic. However, poikilotherms' performance may be reduced in cold conditions due to reduced muscle function, limiting the prey-capture ability of predators and the predator-avoidance and foraging abilities of prey. Here, we use a game-theoretic predator-prey model in which diel temperature changes influence foraging gains and costs to predict the evolutionarily stable diel activity of predators. Our model predicts the range of patterns observed in nature, including nocturnal, diurnal, crepuscular and a previously unexplained post-sunset crepuscular pattern observed in some sharks. In general, smaller predators are predicted to be more diurnal than larger ones. The safety of prey when not foraging is critical, explaining why predators in coral reef systems (with safe refuges) may often have different foraging patterns to pelagic predators. We make a range of testable predictions that will enable the further evaluation of this theoretical framework for understanding diel foraging patterns in poikilotherms.

Social dynamics and individual hunting tactics of white sharks revealed by biologging.

Social foraging, where animals forage in groups, takes many forms but is less studied in marine predators as measuring social associations in the wild is challenging. We used biologging (activity, cameras and telemetry receivers) sensors to measure social associations and simultaneous behaviour, in white sharks (Carcharodon carcharias) off Guadalupe Island, Mexico. Animal-borne telemetry receivers revealed that sharks varied in the number of associations they formed and occurred most often when sharks were swimming in straight paths or when they were turning frequently. While many associations were likely random, there was evidence of some stronger associations. Sharks varied in the depths they used and their activity, with some individuals more active in shallow water while others were more active 200-300 m deep. We propose that white sharks associate with other individuals so they can inadvertently share information on the location or remains of large prey. However, there may be a wide range of individual variability in both behaviour and sociality. Biologging now enables social associations of animals to be measured, concurrent with measures of their behaviour, so that social foraging of large marine predators can be quantified in the wild.

Sharks surf the slope: Current updrafts reduce energy expenditure for aggregating marine predators.

An animal's energy landscape considers the power requirements associated with residing in or moving through habitats. Within marine environments, these landscapes can be dynamic as water currents will influence animal power requirements and can change rapidly over diel and tidal cycles. In channels and along slopes with strong currents, updraft zones may reduce energy expenditure of negatively buoyant fishes that are also obligate swimmers. Despite marine predators often residing within high-current area, no study has investigated the potential role of the energetic landscape in driving such habitat selectivity. Over 500 grey reef sharks Carcharhinus amblyrhynchos reside in the southern channel of Fakarava Atoll, French Polynesia. We used diver observations, acoustic telemetry and biologging to show that sharks use regions of predicted updrafts and switch their core area of space use based on tidal state (incoming versus outgoing). During incoming tides, sharks form tight groups and display shuttling behaviour (moving to the front of the group and letting the current move them to the back) to maintain themselves in these potential updraft zones. During outgoing tides, group dispersion increases, swimming depths decrease and shuttling behaviours cease. These changes are likely due to shifts in the nature and location of the updraft zones, as well as turbulence during outgoing tides. Using a biomechanical model, we estimate that routine metabolic rates for sharks may be reduced by 10%-15% when in updraft zones. Grey reef sharks save energy using predicted updraft zones in channels and 'surfing the slope'. Analogous to birds using wind-driven updraft zones, negatively buoyant marine animals may use current-induced updraft zones to reduce energy expenditure. Updrafts should be incorporated into dynamic energy landscapes and may partially explain the distribution, behaviour and potentially abundance of marine predators.

Multiyear social stability and social information use in reef sharks with diel fission-fusion dynamics.

Animals across vertebrate taxa form social communities and often exist as fission-fusion groups. Central place foragers (CPF) may form groups from which they will predictably disperse to forage, either individually or in smaller groups, before returning to fuse with the larger group. However, the function and stability of social associations in predatory fish acting as CPFs is unknown, as individuals do not need to return to a shelter yet show fidelity to core areas. Using dynamic social networks generated from acoustic tracking data, we document spatially structured sociality in CPF grey reef sharks at a Pacific Ocean atoll. We show that sharks form stable social groups over multiyear periods, with some dyadic associations consistent for up to 4 years. Groups primarily formed during the day, increasing in size throughout the morning before sharks dispersed from the reef at night. Our simulations suggest that multiple individuals sharing a central place and using social information while foraging (i.e. local enhancement) will outperform non-CPF social foragers. We show multiyear social stability in sharks and suggest that social foraging with information transfer could provide a generalizable mechanism for the emergence of sociality with group central place foraging.

Habitat-specific inter and intraspecific behavioral interactions among reef sharks.

Behavioral interactions such as dominance are critical components of animal social lives, competitive abilities, and resulting distribution patterns with coexisting species. Strong interference competition can drive habitat separation, but less is known of the role of interference if agonistic interactions are weak. While most theoretical models assume interference abilities to be constant in an environment, few consider that the extent of interference can vary by habitat and change model predictions. Using baited underwater cameras, we show a consistent dominance status between two sympatric reef sharks at an uninhabited Pacific atoll. Blacktip reef shark (Carcharhinus melanopterus) and gray reef shark (Carcharhinus amblyrhyncos) relative abundance showed an inverse relationship to each other but the strength of this relationship varied by habitat. Reef shark relative abundance declined more rapidly in the presence of heterospecifics on forereef habitats as opposed to backreefs. In all habitats, gray reef sharks were more likely to bite bait cages than blacktips when both species were present, and appeared to be the dominant species. Intraspecific interactions were also apparent, with individual willingness to bite bait decreasing as the number of conspecifics increased. Gray reef sharks may exert differential control over blacktip foraging success in different habitats. Habitat-specific behavioral interactions may partially explain patterns of spatial separation between competing species where interference is weak.

An encounter between a pelagic shark and giant cephalopod.

An oceanic whitetip shark (Carcharhinus longimanus) was observed off the coast of Kona, Hawaii, with scars caused by the tentacles of a large cephalopod. While the exact species could not be confirmed, candidate species include the giant squid (Architeuthis dux) or species from the genera Thysanoteuthis (flying squids) and Megalocranchia (glass squids). Telemetry shows C. longimanus will dive within the mesopelagic zone and may interact with or even forage for large cephalopods.

Distribution, body size and biology of the megamouth shark Megachasma pelagios.

We compiled historical reports of megamouth sharks Megachasma pelagios (mostly fishery by-catch and strandings) from 1976 to 2018 (n = 117) and found that they are distributed globally (highest latitude, 36°) with three hotspots: Japan, Taiwan and the Philippines. Despite possible biases due to variability in fishing effort, more individuals were reported at higher latitudes in the summer, suggesting seasonal, latitudinal migrations. Sex ratios were female-biased in Japan, but more even in Taiwan and the Philippines, suggesting some sexual segregation. Females (total length, LT = 3.41-7.10 m) were larger than males (LT = 1.77-5.39 m) and matured at a larger LT (5.17 m) than males (4.26 m). Also, we reviewed the systematics, feeding ecology and swimming behaviour of Megachasma pelagios based on the literature. Our review shows that, compared with their morphology, anatomy and genetics, behavioural ecology of this species remains largely unknown and electronic tagging studies are warranted.

Size frequency, dispersal distances and variable growth rates of young sharks in a multi-species aggregation.

During a mark-recapture survey from November 2014 until April 2017, 333 neonatal and juvenile blacktip reef sharks Carcharhinus melanopterus and 302 neonatal and juvenile sicklefin lemon sharks Negaprion acutidens were tagged and measured at the uninhabited and isolated St. Joseph Atoll (Republic of Seychelles). Both species demonstrated seasonal reproductive synchronicity and relatively large sizes at birth. Despite the extended times at liberty > 2.5 years, the majority of recaptures were found in close proximity to the initial tagging location (< 500 m). Annual growth rates of C. melanopterus (n = 24) and N. acutidens (n = 62) ranged from 6.6 to 31.7 cm year-1 (mean ± SE; 16.2 ± 1.2 cm year-1 ) and 0.2 to 32.2 cm year-1 (11.8 ± 1 cm year-1 ), respectively and are to date the most variable ever recorded in wild juvenile sharks. High abundances of both species coupled with long-term and repeated recaptures are indicative of a habitat where juveniles can reside for their first years of life. However, large variability in annual growth rates in both species may suggest high intra and interspecific competition induced by a possibly resource limited, isolated habitat.

Seagrass digestion by a notorious 'carnivore'.

What an animal consumes and what an animal digests and assimilates for energetic demands are not always synonymous. Sharks, uniformly accepted as carnivores, have guts that are presumed to be well suited for a high-protein diet. However, the bonnethead shark (Sphyrna tiburo), which is abundant in critical seagrass habitats, has been previously shown to consume copious amounts of seagrass (up to 62.1% of gut content mass), although it is unknown if they can digest and assimilate seagrass nutrients. To determine if bonnetheads digest seagrass nutrients, captive sharks were fed a 13C-labelled seagrass diet. Digestibility analyses, digestive enzyme assays and stable isotope analyses were used to determine the bonnethead shark's capacity for digesting and assimilating seagrass material. Compound-specific stable isotope analysis showed that sharks assimilated seagrass carbon (13.6 ± 6.77‰ δ13C mean ± s.d. for all sharks and all amino acid types analysed) with 50 ± 2% digestibility of seagrass organic matter. Additionally, cellulose-component-degrading enzyme activities were detected in shark hindguts. We show that a coastal shark is digesting seagrass with at least moderate efficiency, which has ecological implications due to the stabilizing role of omnivory and nutrient transport within fragile seagrass ecosystems.

Mobile marine predators: an understudied source of nutrients to coral reefs in an unfished atoll.

Animal movements can facilitate important ecological processes, and wide-ranging marine predators, such as sharks, potentially contribute significantly towards nutrient transfer between habitats. We applied network theory to 4 years of acoustic telemetry data for grey reef sharks (Carcharhinus amblyrhynchos) at Palmyra, an unfished atoll, to assess their potential role in nutrient dynamics throughout this remote ecosystem. We evaluated the dynamics of habitat connectivity and used network metrics to quantify shark-mediated nutrient distribution. Predator movements were consistent within year, but differed between years and by sex. Females used higher numbers of routes throughout the system, distributing nutrients over a larger proportion of the atoll. Extrapolations of tagged sharks to the population level suggest that prey consumption and subsequent egestion leads to the heterogeneous deposition of 94.5 kg d-1 of nitrogen around the atoll, with approximately 86% of this probably derived from pelagic resources. These results suggest that sharks may contribute substantially to nutrient transfer from offshore waters to near-shore reefs, subsidies that are important for coral reef health.

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator.

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes.

Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources.

Digestive enzyme activities in the guts of bonnethead sharks (Sphyrna tiburo) provide insight into their digestive strategy and evidence for microbial digestion in their hindguts.

Few investigations have studied digestive enzyme activities in the alimentary tracts of sharks to gain insight into how these organisms digest their meals. In this study, we examined the activity levels of proteases, carbohydrases, and lipase in the pancreas, and along the anterior intestine, spiral intestine, and colon of the bonnethead shark, Sphyrna tiburo. We then interpreted our data in the context of a rate-yield continuum to discern this shark's digestive strategy. Our data show anticipated decreasing patterns in the activities of pancreatic enzymes moving posteriorly along the gut, but also show mid spiral intestine peaks in aminopeptidase and lipase activities, which support the spiral intestine as the main site of absorption in bonnetheads. Interestingly, we observed spikes in the activity levels of N-acetyl-ß-D-glucosaminidase and ß-glucosidase in the bonnethead colon, and these chitin- and cellulose-degrading enzymes, respectively, are likely of microbial origin in this distal gut region. Taken in the context of intake and relatively long transit times of food through the gut, the colonic spikes in N-acetyl-ß-D-glucosaminidase and ß-glucosidase activities suggest that bonnetheads take a yield-maximizing strategy to the digestive process, with some reliance on microbial digestion in their hindguts. This is one of the first studies to examine digestive enzyme activities along the gut of any shark, and importantly, the data match with previous observations that sharks take an extended time to digest their meals (consistent with a yield-maximizing digestive strategy) and that the spiral intestine is the primary site of absorption in sharks.

Age is not just a number: How incorrect ageing impacts close-kin mark-recapture estimates of population size.

Population size is a key parameter for the conservation of animal species. Close-kin mark-recapture (CKMR) relies on the observed frequency and type of kinship among individuals sampled from the population to estimate population size. Knowledge of the age of the individuals, or a surrogate thereof, is essential for inference with acceptable precision. One common approach, particularly in fish studies, is to measure animal length and infer age using an assumed age-length relationship (a 'growth curve'). We used simulation to test the effect of misspecifying the length measurement error and the growth curve on population size estimation. Simulated populations represented two fictional shark species, one with a relatively simple life history and the other with a more complex life history based on the grey reef shark (Carcharhinus amblyrhynchos). We estimated sex-specific adult abundance, which we assumed to be constant in time. We observed small median biases in these estimates ranging from 1.35% to 2.79% when specifying the correct measurement error standard deviation and growth curve. CI coverage was adequate whenever the growth curve was correctly specified. Introducing error via misspecified growth curves resulted in changes in the magnitude of the estimated adult population, where underestimating age negatively biased the abundance estimates. Over- and underestimating the standard deviation of length measurement error did not introduce a bias and had negligible effect on the variance in the estimates. Our findings show that assuming an incorrect standard deviation of length measurement error has little effect on estimation, but having an accurate growth curve is crucial for CKMR whenever ageing is based on length measurements. If ageing could be biased, researchers should be cautious when interpreting CKMR results and consider the potential biases arising from inaccurate age inference.

Habitat-specific impacts of climate change on the trophic demand of a marine predator.

Metabolic ecology predicts that ectotherm metabolic rates, and thus consumption rates, will increase with body size and temperature. Predicted climatic increases in temperature are likely to increase the consumption rates of ectothermic predators; however, the ecological impact of these increases will partly depend on whether prey productivity changes with temperature at a similar rate. Furthermore, total predator consumption and prey productivity will depend on species abundances that vary across habitat types. Here we combine energetics and biotelemetry to measure consumption rates in a critically endangered coral reef predator, the Nassau grouper (Epinephelus striatus), in The Bahamas. We estimate that, at present, the Nassau grouper needs to consume 2.2% ± 1.0% body weight day-1 , but this could increase up to 24% with a predicted 3.1°C increase in ocean temperature by the end of the century. We then used surveys of prey communities in two major reef habitat types (Orbicella reef and Gorgonian plain), to predict the proportion of prey productivity consumed by grouper and how this varied by habitat with changing climates. We found that at present, the predicted proportion of prey productivity consumed by Nassau grouper decreased with increasing prey productivity and averaged 1.2% across all habitats, with a greater proportion of prey productivity consumed (maximum of 5%) in Gorgonian plain habitats. However, because temperature increases consumption rates faster than prey productivity, the proportion of prey productivity consumed in a Gorgonian plain habitat could increase up to 24% under future climate change scenarios. Our results suggest that increasing ocean temperatures will lead to significant energetic challenges for the Nassau grouper because of differential impacts within reef food webs, but the magnitude of these impacts will probably vary across prey productivity gradients.

Spatial memory and animal movement.

Memory is critical to understanding animal movement but has proven challenging to study. Advances in animal tracking technology, theoretical movement models and cognitive sciences have facilitated research in each of these fields, but also created a need for synthetic examination of the linkages between memory and animal movement. Here, we draw together research from several disciplines to understand the relationship between animal memory and movement processes. First, we frame the problem in terms of the characteristics, costs and benefits of memory as outlined in psychology and neuroscience. Next, we provide an overview of the theories and conceptual frameworks that have emerged from behavioural ecology and animal cognition. Third, we turn to movement ecology and summarise recent, rapid developments in the types and quantities of available movement data, and in the statistical measures applicable to such data. Fourth, we discuss the advantages and interrelationships of diverse modelling approaches that have been used to explore the memory-movement interface. Finally, we outline key research challenges for the memory and movement communities, focusing on data needs and mathematical and computational challenges. We conclude with a roadmap for future work in this area, outlining axes along which focused research should yield rapid progress.

Telemetry and random-walk models reveal complex patterns of partial migration in a large marine predator.

Animals are often faced with complex movement decisions, particularly those that involve long-distance dispersal. Partial migrations, ubiquitous among all groups of vertebrates, are a form of long-distance movement that occurs when only some of the animals in a population migrate. The decision to migrate or to be a resident can be dependent on many factors, but these factors are rarely quantified in fishes, particularly top predators, even though partial migrations may have important implications for ecosystem dynamics and conservation. We utilized passive acoustic telemetry, with a Brownian bridge movement model and generalized additive mixed models, to explore the factors regulating partial migration in a large marine predator, the tiger shark, throughout the Hawaiian Islands. Although sharks tended to utilize a particular "core" island, they also demonstrated inter-island movements, particularly mature females that would swim from the northwestern Hawaiian Islands to the main Hawaiian Islands (MHI). Immigration to another island was a function of season, sea surface temperature (SST), and chlorophyll a concentration. Our results predict that 25% of mature females moved from remote French Frigate Shoals atoll to the MHI during late summer/early fall, potentially to give birth. Females with core home ranges within the MHI showed limited movements to the NWHI, and immigration to an island was better explained by SST and chlorophyll a concentration, suggesting a foraging function. Dispersal patterns in tiger sharks are complex but can be considered a mix of skipped-breeding partial migration by mature females and individual-based inter-island movements potentially linked to foraging. Therefore, sharks appear to use a conditional strategy based on fixed intrinsic and flexible extrinsic states. The application of Brownian bridge movement models to electronic presence/absence data provides a new technique for assessing the influence of habitat and environmental conditions on patterns of movement for fish populations.