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.

Energetic connectivity of diverse elasmobranch populations - implications for ecological resilience.

Understanding the factors shaping patterns of ecological resilience is critical for mitigating the loss of global biodiversity. Throughout aquatic environments, highly mobile predators are thought to serve as important vectors of energy between ecosystems thereby promoting stability and resilience. However, the role these predators play in connecting food webs and promoting energy flow remains poorly understood in most contexts. Using carbon and nitrogen isotopes, we quantified the use of several prey resource pools (small oceanic forage, large oceanics, coral reef, and seagrass) by 17 species of elasmobranch fishes (n = 351 individuals) in The Bahamas to determine their functional diversity and roles as ecosystem links. We observed remarkable functional diversity across species and identified four major groups responsible for connecting discrete regions of the seascape. Elasmobranchs were responsible for promoting energetic connectivity between neritic, oceanic and deep-sea ecosystems. Our findings illustrate how mobile predators promote ecosystem connectivity, underscoring their functional significance and role in supporting ecological resilience. More broadly, strong predator conservation efforts in developing island nations, such as The Bahamas, are likely to yield ecological benefits that enhance the resilience of marine ecosystems to combat imminent threats such as habitat degradation and climate change.

Observations of fin injury closure in Great Hammerheads and implications for the use of fin-mounted geolocators.

OBJECTIVE: Sharks face a high risk of injuries throughout all life stages and are therefore expected to show a good wound closure capacity. METHODS: Here, the wound closure of one major injury and one minor injury to the first dorsal fins of two free-ranging, mature female Great Hammerheads Sphyrna mokarran is described macroscopically. RESULT: The sharks showed complete wound closure of single, clean-cut lacerations measuring 24.2 and 11.6 cm in length after an estimated 323 and 138 days. These estimates were based on the observed closure rate and visual confirmation of a complete wound closure upon multiple resightings of the same individuals. Additionally, the posterior lateral displacement of fin-mounted geolocators within the fin and outside of the fin without causing external damage was documented in three additional Great Hammerheads. CONCLUSION: These observations supplement findings about wound closure capabilities in elasmobranchs. The documented geolocator displacement furthers the discussion about the safe use of these geolocators to track shark movements but also has implications for future tagging studies.

Predator-prey landscapes of large sharks and game fishes in the Florida Keys.

Interspecific interactions can play an essential role in shaping wildlife populations and communities. To date, assessments of interspecific interactions, and more specifically predator-prey dynamics, in aquatic systems over broad spatial and temporal scales (i.e., hundreds of kilometers and multiple years) are rare due to constraints on our abilities to measure effectively at those scales. We applied new methods to identify space-use overlap and potential predation risk to Atlantic tarpon (Megalops atlanticus) and permit (Trachinotus falcatus) from two known predators, great hammerhead (Sphyrna mokarran) and bull (Carcharhinus leucas) sharks, over a 3-year period using acoustic telemetry in the coastal region of the Florida Keys (USA). By examining spatiotemporal overlap, as well as the timing and order of arrival at specific locations compared to random chance, we show that potential predation risk from great hammerhead and bull sharks to Atlantic tarpon and permit are heterogeneous across the Florida Keys. Additionally, we find that predator encounter rates with these game fishes are elevated at specific locations and times, including a prespawning aggregation site in the case of Atlantic tarpon. Further, using machine learning algorithms, we identify environmental variability in overlap between predators and their potential prey, including location, habitat, time of year, lunar cycle, depth, and water temperature. These predator-prey landscapes provide insights into fundamental ecosystem function and biological conservation, especially in the context of emerging fishery-related depredation issues in coastal marine ecosystems.

Preliminary observations on the movement ecology of a crested horn shark (Heterodontus galeatus).

The residency and movements of a single acoustically tagged female crested horn shark (Heterodontus galeatus) were monitored in Jervis Bay, Australia. The individual was intermittently detected by receivers throughout the 8-year study period and showed preference for particular rocky reefs in terms of its residency indices and duration of residency events. This individual exhibited lower residency and dissimilar movement patterns to that of the well-studied and sympatric Port Jackson shark (Heterodontus portusjacksoni), highlighting the need for research into the basic life history and movement ecology of H. galeatus.

Thirty-five years of tiger shark Galeocerdo cuvier relative abundance near Bimini, The Bahamas, and the Southeastern United States with a comparison across jurisdictional bounds.

Abundances of large sharks are reported to have declined worldwide, and in response various levels of fisheries management and conservation efforts have been established. For example, marine-protected areas have been suggested as a means to protect large expanses of ocean from fishing and other industrial activities (e.g., habitat destruction), and in 2011 The Commonwealth of The Bahamas established The Bahamas Shark Sanctuary. Nonetheless, assessing the effectiveness of conservation efforts is challenging because consistent long-term data sets of shark abundances are often lacking, especially throughout the Caribbean and The Bahamas. In this study, the authors investigated the catch rates and demographics of tiger sharks Galeocerdo cuvier caught in a fishery-independent survey near Bimini, The Bahamas, from 1984 to 2019 to assess relative abundance trends following the banning of longline fishing in 1993 and the subsequent establishment of the shark sanctuary. To contextualize the relative abundance trends near Bimini, the authors compared this to the relative abundance of tiger sharks in a fishery-dependent survey from the Southeastern USA (SE USA), conducted from 1994 to 2019. The data of this study suggest that local abundance of tiger sharks has been stable near Bimini since the 1980s, including after the ban of longline fishing and the implementation of the shark sanctuary. In comparison, the abundance near the SE USA has slowly increased in the past decade, following potential declines in the decade preceding the USA Shark Management Plan. The results of this study provide some optimism that current conservation efforts in The Bahamas have been effective to maintain local tiger shark abundance within the protected area. In addition, current fisheries management in the SE USA is allowing this species to recover within those waters.

Vertical space use and thermal range of the great hammerhead (Sphyrna mokarran), (Rüppell, 1837) in the western North Atlantic.

The great hammerhead (Sphyrna mokarran) is a highly mobile, large-bodied shark primarily found in coastal-pelagic and semi-oceanic waters across a circumtropical range. It is a target or by-catch species in multiple fisheries, and as a result, rapid population declines have occurred in many regions. These declines have contributed to the species being assessed as globally critically endangered on the IUCN Red List. Although conservation and management measures have yielded promising results in some regions, such as the United States, high levels of at-vessel and post-release mortality remain a major concern to the species population recovery. This examined the vertical space use and thermal range of pop-off archival satellite-tagged S. mokarran in the western North Atlantic Ocean, expanding the understanding of the ecological niche of this species and providing insight into by-catch mitigation strategies for fisheries managers. The results showed that S. mokarran predominantly used shallow depths (75% of records <30 m) and had a narrow temperature range (89% of records between 23 and 28°C). Individual differences in depth use were apparent, and a strong diel cycle was observed, with sharks occupying significantly deeper depths during the daytime. Furthermore, two individuals were confirmed pregnant with one migrating from the Bahamas to South Carolina, U.S.A., providing further evidence of regional connectivity and parturition off the U.S. East Coast. The findings suggest that S. mokarran may be vulnerable to incidental capture in the western North Atlantic commercial longline fisheries due to substantial vertical overlap between the species and the gear. The results can be incorporated into conservation and management efforts to develop and/or refine mitigation measures focused on reducing the by-catch and associated mortality of this species, which can ultimately aide S. mokarran population recovery in areas with poor conservation status.

Personality-driven life history trade-offs differ in two subpopulations of free-ranging predators.

Consistent individual differences in behaviour (i.e. personality) can be explained in an evolutionary context if they are favoured by life history trade-offs as conceptualized in the pace-of-life syndrome (POLS) hypothesis. Theory predicts that faster-growing individuals suffer higher mortality and that this trade-off is mediated through exploration/risk-taking personality, but empirical support for this remains limited and ambiguous. Equivocal support to the POLS hypothesis suggests that the link between life history and personality may only emerge under certain circumstances. Understanding personality-driven trade-offs would be facilitated by long-term studies in wild populations experiencing different ecological conditions. Here, we tested whether personality measured in semi-captivity was associated with a growth-mortality trade-off via risk-taking in the wild in two subpopulations of juvenile lemon sharks Negaprion brevirostris known to differ in their predator abundance. We expected stronger personality-driven trade-offs in the predator-rich environment as compared to the predator-poor environment. Sharks were captured yearly from 1995 onwards allowing us to obtain long-term data on growth and apparent survival in each subpopulation. We then used a novel open-field assay to test sharks for exploration personality yearly from 2012 to 2017. A subset of the tested sharks was monitored in the field using telemetry to document risk-taking behaviours. We tested (a) if fast explorers in captivity took more risks and grew faster in the wild and (b) if natural selection acted against more explorative, faster-growing sharks. In the subpopulation with fewer predators, more explorative sharks in captivity took more risks in the wild and grew faster. In turn, larger, fast-growing sharks had lower apparent survival. In the predator-rich subpopulation, despite finding selection on fast growth, we found no link between exploration personality and the growth-mortality trade-off. Our study demonstrates that the association between personality and life history is favoured in some ecological contexts but not in others. We identify predator and resource abundance as two main potential drivers of the personality-mediated trade-off and emphasize that future work on the POLS hypothesis would benefit from an approach integrating behaviour and life history across ecological conditions.

Anatomy of the mechanosensory lateral line canal system and electrosensory ampullae of Lorenzini in two species of sawshark (fam. Pristiophoridae).

It has long been assumed that the elongated rostra (the saws) of sawsharks (family: Pristiophoridae) and sawfish (family: Pristidae) serve a similar function. Recent behavioural and anatomical studies have shed light on the dual function of the pristid rostrum in mechanosensory and electrosensory prey detection and prey manipulation. Here, the authors examine the distributions of the mechanosensory lateral line canals and electrosensory ampullae of Lorenzini in the southern sawshark, Pristiophorus nudipinnis and the longnose sawshark, Pristiophorus cirratus. In both species, the receptive fields of the mechano- and electrosensory systems extend the full length of the rostrum indicating that the sawshark rostrum serves a sensory function. Interestingly, despite recent findings suggesting they feed at different trophic levels, minimal interspecific variation between the two species was recorded. Nonetheless, compared to pristids, the pristiophorid rostrum possesses a reduced mechanosensory sampling field but higher electrosensory resolution, which suggests that pristiophorids may not use their rostrums to disable large prey like pristids do.

Residency and movement patterns of adult Port Jackson sharks (Heterodontus portusjacksoni) at a breeding aggregation site.

Examining the movement ecology of mesopredators is fundamental to developing an understanding of their biology, ecology and behaviour, as well as the communities and ecosystems they influence. The limited research on the residency and movements of benthic marine mesopredators has primarily used visual tags, which do not allow for the efficient and accurate monitoring of individual space use. In this study, the authors investigated the residency and movement patterns of Port Jackson sharks Heterodontus portusjacksoni (Meyer 1793) at a breeding aggregation site in Jervis Bay, south-eastern Australia, using passive acoustic telemetry to further our understanding of the movement ecology of these important mesopredators. Between 2012 and 2014, individuals were tagged with acoustic transmitters, and their residency and movements within the bay were monitored for up to 4 years. H. portusjacksoni showed strong preferences for particular reefs within and between breeding seasons. Males had significantly higher residency indices at their favoured sites relative to females, suggesting that males may be engaging in territorial behaviour. Conversely, female H. portusjacksoni exhibited higher roaming indices relative to males indicating that females may move between sites to assess males. Finally, H. portusjacksoni showed temporal variation in movements between reefs with individuals typically visiting more reefs at night relative to the day, dusk and dawn corresponding with their nocturnal habits.

Linking local movement and molecular analysis to explore philopatry and population connectivity of the southern stingray Hypanus americanus.

Limited data pertaining to life history and population connectivity of the data-deficient southern stingray (Hypanus americanus) are available. To determine potential vulnerabilities of their populations, this study aimed to analyse their movement patterns and genetic variability. A population of southern stingrays encompassing nine sites around Cape Eleuthera, the Bahamas, has been monitored using mark-recapture, spanning a 2.5 year period. Out of 200 individual stingrays, more than a third were encountered again. The home range of the females appears to be restricted, which supports the notion of high site residency. As resident populations of stingrays could suffer from a lack of population connectivity and be predestined for genetic isolation and local extirpation, this study further investigated the genetic connectivity of four sample sites in the central and western Bahamas. A haplotype analysis from the mitochondrial D-loop region showed that no distinct population structure strictly correlated with the sample site. These findings were complemented by five microsatellite loci that revealed high degrees in genotypic variability and little population differentiation. The results suggest gene flow mediated by both males and females.

Thermal performance responses in free-ranging elasmobranchs depend on habitat use and body size.

Temperature is one of the most influential drivers of physiological performance and behaviour in ectotherms, determining how these animals relate to their ecosystems and their ability to succeed in particular habitats. Here, we analysed the largest set of acceleration data compiled to date for elasmobranchs to examine the relationship between volitional activity and temperature in 252 individuals from 8 species. We calculated activation energies for the thermal performance response in each species and estimated optimum temperatures using an Arrhenius breakpoint analysis, subsequently fitting thermal performance curves to the activity data. Juveniles living in confined nursery habitats not only spent substantially more time above their optimum temperature and at the upper limits of their performance breadths compared to larger, less site-restricted animals, but also showed lower activation energies and broader performance curves. Species or life stages occupying confined habitats featured more generalist behavioural responses to temperature change, whereas wider ranging elasmobranchs were characterised by more specialist behavioural responses. The relationships between the estimated performance regimes and environmental temperature limits suggest that animals in confined habitats, including many juvenile elasmobranchs within nursery habitats, are likely to experience a reduction of performance under a warming climate, although their flatter thermal response will likely dampen this impact. The effect of warming on less site-restricted species is difficult to forecast since three of four species studied here did not reach their optimum temperature in the wild, although their specialist performance characteristics may indicate a more rapid decline should optimum temperatures be exceeded.

No apparent negative tagging effects after 13 years at liberty for lemon shark, Negaprion brevirostris implanted with acoustic transmitter.

An intact and uncompromised internal acoustic transmitter was non-lethally recovered from a lemon shark Negaprion brevirostris, after 13 years at liberty. The shark, first tagged at an estimated age of 2 years old near South Bimini, Bahamas in 2004, was recaptured in 2017 with a total length of 264 cm. The tagged shark displayed typical growth rate, pregnancy, natal homing and pupping behaviour of other individuals in this population. This observation provides important evidence regarding the effects from long-term retention of implanted acoustic transmitters in a carcharhinid shark.

Evaluation of Comprehensive Coelomic Fluid Analysis through Coelomic Pore Sampling as a Novel Diagnostic Tool in Elasmobranchs.

The objectives of this study were to describe a minimally invasive coelomic fluid sampling technique in elasmobranchs, to characterize the coelomic fluid composition in clinically normal and abnormal animals, and to compare findings from wild and managed populations. Fluid was collected via the coelomic pore in 89 individuals from 16 species spanning clinically normal and abnormal patients within a managed population (n = 54), a semi-managed open-lagoon population (n = 18), and a wild population (n = 17). Biochemical and cytological fluid analyses were performed on all samples, and bacterial and fungal culture, protein electrophoresis, and cholesterol electrophoresis were performed on a subset of samples. The presence of a variable volume of colorless to white and clear to slightly turbid coelomic fluid was consistent with a normal finding; however, the cytological and chemical makeup of coelomic fluid was found to provide additional clinically relevant information. The coelomic fluid from some of the abnormal samples (n = 37) contained white blood cells (n = 15) and concurrent bacteria (n = 7), the latter suggestive of bacterial coelomitis. Yolk was identified in both clinically normal and abnormal females. Of the biochemical parameters tested, calcium, chloride, cholesterol, osmolality, phosphorus, salinity, sodium, specific gravity, total protein, and urea nitrogen have clinical utility. Abnormal samples were mostly associated with reproductive disease, but to a lesser extent with coelomitis and hemocoelom. The wild and semi-managed groups had biochemical differences presumably reflective of the higher salinity of ocean water compared with that in the managed habitat. Aerobic bacteria were identified in normal (n = 7) and abnormal (n = 11) animals. Positive bacterial culture without inflammation may be normal. This study contributes to a further understanding of elasmobranch coelomic fluid analysis and its use as a diagnostic modality for the evaluation of elasmobranch health.

Risky business for a juvenile marine predator? Testing the influence of foraging strategies on size and growth rate under natural conditions.

Mechanisms driving selection of body size and growth rate in wild marine vertebrates are poorly understood, thus limiting knowledge of their fitness costs at ecological, physiological and genetic scales. Here, we indirectly tested whether selection for size-related traits of juvenile sharks that inhabit a nursery hosting two dichotomous habitats, protected mangroves (low predation risk) and exposed seagrass beds (high predation risk), is influenced by their foraging behaviour. Juvenile sharks displayed a continuum of foraging strategies between mangrove and seagrass areas, with some individuals preferentially feeding in one habitat over another. Foraging habitat was correlated with growth rate, whereby slower growing, smaller individuals fed predominantly in sheltered mangroves, whereas larger, faster growing animals fed over exposed seagrass. Concomitantly, tracked juveniles undertook variable movement behaviours across both the low and high predation risk habitat. These data provide supporting evidence for the hypothesis that directional selection favouring smaller size and slower growth rate, both heritable traits in this shark population, may be driven by variability in foraging behaviour and predation risk. Such evolutionary pathways may be critical to adaptation within predator-driven marine ecosystems.

Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni.

Basic understanding of the fundamental principles and mechanisms involved in learning is lacking for elasmobranch fishes. Our aim in this study was to experimentally investigate the learning and memory capacity of juvenile Port Jackson sharks, Heterodontus portusjacksoni. Sharks (N = 30) were conditioned over a 19-day period to associate an underwater LED light or stream of air-bubbles [conditioned stimulus (CS)] with a food reward [unconditioned stimulus (US)], using three procedures (delay, trace and control). During experiments, the CS signalled at a random time between 180 and 300 s for 30 s (six times per day). For the delay the US overlapped in time with the CS, for the trace the US delivered 10 s after the CS and for our control the US was delivered at random time between 180 and 300 s after the CS. H. portusjacksoni sharks trained in all procedures improved consistently in their time to obtain food, indicative of Pavlovian learning. Importantly, the number of sharks in the feeding area 5 s prior to CS onset did not change over time for any procedures. However, significantly more sharks were present 5 s after CS onset for delay for both air-bubble and light CS. Sharks trained in the delay and trace procedures using air-bubbles as the CS also displayed significantly more anticipatory behaviours, such as turning towards the CS and biting. Sharks trained with the light CS did not exhibit such behaviours; however, trace procedural sharks did show a significant improvement in moving towards the CS at its onset. At 20 and 40 days after the end of the conditioning experiments, some sharks were presented the CS without reward. Two sharks trained in the delay procedure using air-bubbles as the CS exhibited biting behaviours: one at 20 and the other at 40 days. This study demonstrates that H. portusjacksoni have the capacity to learn a classical conditioning procedure relatively quickly (30 trials during 5 days) and associate two time-separated events and retention of learnt associations for at least 24 h and possibly up to 40 days.

Social learning in juvenile lemon sharks, Negaprion brevirostris.

Social learning is taxonomically widespread and can provide distinct behavioural advantages, such as in finding food or avoiding predators more efficiently. Although extensively studied in bony fishes, no such empirical evidence exists for cartilaginous fishes. Our aim in this study was to experimentally investigate the social learning capabilities of juvenile lemon sharks, Negaprion brevirostris. We designed a novel food task, where sharks were required to enter a start zone and subsequently make physical contact with a target in order to receive a food reward. Naive sharks were then able to interact with and observe (a) pre-trained sharks, that is, 'demonstrators', or (b) sharks with no previous experience, that is, 'sham demonstrators'. On completion, observer sharks were then isolated and tested individually in a similar task. During the exposure phase observers paired with 'demonstrator' sharks performed a greater number of task-related behaviours and made significantly more transitions from the start zone to the target, than observers paired with 'sham demonstrators'. When tested in isolation, observers previously paired with 'demonstrator' sharks completed a greater number of trials and made contact with the target significantly more often than observers previously paired with 'sham demonstrators'. Such experience also tended to result in faster overall task performance. These results indicate that juvenile lemon sharks, like numerous other animals, are capable of using socially derived information to learn about novel features in their environment. The results likely have important implications for behavioural processes, ecotourism and fisheries.

Ultrasonographic and hormonal characterization of reproductive health and disease in wild, semiwild, and aquarium-housed southern stingrays (Hypanus americanus).

OBJECTIVE: To characterize physical examination, plasma biochemical, and ultrasonographic findings in aquarium-housed, managed semiwild, and wild southern stingrays (Hypanus americanus) with and without reproductive disease. ANIMALS: Southern stingrays from aquarium (n = 48), lagoon (managed semiwild; 34), and wild (12) habitats. PROCEDURES: Limited, opportunistic prosections were performed of presumed anatomically normal wild southern stingrays and compared with findings for aquarium-housed stingrays with reproductive disease. Ultrasonographic video data from both groups were used to assign a score (1 to 5) indicating increasing severity of ovarian and uterine reproductive disease. Plasma total 17ß-estradiol, estrone, progesterone, and testosterone concentrations were measured with enzyme immunoassays validated for use in southern stingrays. RESULTS: Ultrasonographic ovarian scores were significantly correlated with uterine scores. No reproductive disease was detected in semiwild or wild stingrays, but 65% (31/48) of aquarium-housed stingrays had developing or advanced reproductive disease (ie, ultrasonographic ovarian or uterine score of 4 or 5). Significant correlations were identified between ovarian and uterine disease status and plasma concentrations of all steroid hormones except testosterone. CONCLUSIONS AND CLINICAL RELEVANCE: Findings suggested that ultrasonography and plasma hormone concentrations may be useful in the identification of reproductive disease and determination of disease severity in southern stingrays.

Biodiversity assessment of tropical shelf eukaryotic communities via pelagic eDNA metabarcoding.

Our understanding of marine communities and their functions in an ecosystem relies on the ability to detect and monitor species distributions and abundances. Currently, the use of environmental DNA (eDNA) metabarcoding is increasingly being applied for the rapid assessment and monitoring of aquatic species. Most eDNA metabarcoding studies have either focussed on the simultaneous identification of a few specific taxa/groups or have been limited in geographical scope. Here, we employed eDNA metabarcoding to compare beta diversity patterns of complex pelagic marine communities in tropical coastal shelf habitats spanning the whole Caribbean Sea. We screened 68 water samples using a universal eukaryotic COI barcode region and detected highly diverse communities, which varied significantly among locations, and proved good descriptors of habitat type and environmental conditions. Less than 15% of eukaryotic taxa were assigned to metazoans, most DNA sequences belonged to a variety of planktonic "protists," with over 50% of taxa unassigned at the phylum level, suggesting that the sampled communities host an astonishing amount of micro-eukaryotic diversity yet undescribed or absent from COI reference databases. Although such a predominance of micro-eukaryotes severely reduces the efficiency of universal COI markers to investigate vertebrate and other metazoans from aqueous eDNA, the study contributes to the advancement of rapid biomonitoring methods and brings us closer to a full inventory of extant marine biodiversity.