Diving into the vertical dimension of elasmobranch movement ecology.

Knowledge of the three-dimensional movement patterns of elasmobranchs is vital to understand their ecological roles and exposure to anthropogenic pressures. To date, comparative studies among species at global scales have mostly focused on horizontal movements. Our study addresses the knowledge gap of vertical movements by compiling the first global synthesis of vertical habitat use by elasmobranchs from data obtained by deployment of 989 biotelemetry tags on 38 elasmobranch species. Elasmobranchs displayed high intra- and interspecific variability in vertical movement patterns. Substantial vertical overlap was observed for many epipelagic elasmobranchs, indicating an increased likelihood to display spatial overlap, biologically interact, and share similar risk to anthropogenic threats that vary on a vertical gradient. We highlight the critical next steps toward incorporating vertical movement into global management and monitoring strategies for elasmobranchs, emphasizing the need to address geographic and taxonomic biases in deployments and to concurrently consider both horizontal and vertical movements.

Analysing detection gaps in acoustic telemetry data to infer differential movement patterns in fish.

A wide array of technologies are available for gaining insight into the movement of wild aquatic animals. Although acoustic telemetry can lack the fine-scale spatial resolution of some satellite tracking technologies, the substantially longer battery life can yield important long-term data on individual behavior and movement for low per-unit cost. Typically, however, receiver arrays are designed to maximize spatial coverage at the cost of positional accuracy leading to potentially longer detection gaps as individuals move out of range between monitored locations. This is particularly true when these technologies are deployed to monitor species in hard-to-access locations.Here, we develop a novel approach to analyzing acoustic telemetry data, using the timing and duration of gaps between animal detections to infer different behaviors. Using the durations between detections at the same and different receiver locations (i.e., detection gaps), we classify behaviors into "restricted" or potential wider "out-of-range" movements synonymous with longer distance dispersal. We apply this method to investigate spatial and temporal segregation of inferred movement patterns in two sympatric species of reef shark within a large, remote, marine protected area (MPA). Response variables were generated using network analysis, and drivers of these movements were identified using generalized linear mixed models and multimodel inference.Species, diel period, and season were significant predictors of "out-of-range" movements. Silvertip sharks were overall more likely to undertake "out-of-range" movements, compared with gray reef sharks, indicating spatial segregation, and corroborating previous stable isotope work between these two species. High individual variability in "out-of-range" movements in both species was also identified.We present a novel gap analysis of telemetry data to help infer differential movement and space use patterns where acoustic coverage is imperfect and other tracking methods are impractical at scale. In remote locations, inference may be the best available tool and this approach shows that acoustic telemetry gap analysis can be used for comparative studies in fish ecology, or combined with other research techniques to better understand functional mechanisms driving behavior.

Depth-dependent dive kinematics suggest cost-efficient foraging strategies by tiger sharks.

Tiger sharks, Galeocerdo cuvier, are a keystone, top-order predator that are assumed to engage in cost-efficient movement and foraging patterns. To investigate the extent to which oscillatory diving by tiger sharks conform to these patterns, we used a biologging approach to model their cost of transport. High-resolution biologging tags with tri-axial sensors were deployed on 21 tiger sharks at Ningaloo Reef for durations of 5-48 h. Using overall dynamic body acceleration as a proxy for energy expenditure, we modelled the cost of transport of oscillatory movements of varying geometries in both horizontal and vertical planes for tiger sharks. The cost of horizontal transport was minimized by descending at the smallest possible angle and ascending at an angle of 5-14°, meaning that vertical oscillations conserved energy compared to swimming at a level depth. The reduction of vertical travel costs occurred at steeper angles. The absolute dive angles of tiger sharks increased between inshore and offshore zones, presumably to reduce the cost of transport while continuously hunting for prey in both benthic and surface habitats. Oscillatory movements of tiger sharks conform to strategies of cost-efficient foraging, and shallow inshore habitats appear to be an important habitat for both hunting prey and conserving energy while travelling.

Complete mitochondrial genome of the gray reef shark, Carcharhinus amblyrhynchos (Carcharhiniformes: Carcharhinidae).

We report the first mitochondrial genome sequences for the gray reef shark, Carcharhinus amblyrhynchos. Two specimens from the British Indian Ocean Territory were sequenced independently using two different next generation sequencing methods, namely short read sequencing on the Illumina HiSeq and long read sequencing on the Oxford Nanopore Technologies' MinION sequencer. The two sequences are 99.9% identical and are 16,705 base pairs (bp) and 16,706 bp in length. The mitogenome contains 22 tRNA genes, two rRNA genes, 13 protein-coding genes and two non-coding regions; the control region and the origin of light-strand replication (OL).

Mitochondrial genome of the Silvertip shark, Carcharhinus albimarginatus, from the British Indian Ocean Territory.

The Chagos archipelago in the British Indian Ocean Territory (BIOT) has been lacking in detailed genetic studies of its chondrichthyan populations. Chondrichthyes in Chagos continue to be endangered through illegal fishing operations, necessitating species distribution and abundance studies to facilitate urgent monitoring and conservation of the species. Here, we present a complete mitochondrial genome of the Silvertip Shark, Carcharhinus albimarginatus sampled in the Chagos archipelago. The mitochondrial genome of C. albimarginatus was 16,706 bp in length and consisted of 13 protein-coding genes, 22 tRNA genes, two rRNA genes, a replication origin and a D-loop region. GC content was at 38.7% and the control region was 1,065 bp in length. We expect that mitogenomes presented here will aid development of molecular assays for species distribution studies. Overall these studies will promote effective conservation of marine ecosystemes in the BIOT.

Complete mitochondrial genome of the whitetip reef shark Triaenodon obesus from the British Indian Ocean Territory Marine Protected Area.

We present the first mitochondrial genome of Trianenodon obesus from the Chagos Archipelago in the British Indian Ocean Territory (BIOT) Marine Protected Area. The mitogenome was 16,702 bp in length and consisted of 13 protein-coding genes (PCGs), 22 tRNA genes, 2 rRNA genes, and a non-coding control region (D-loop). GC content was at 38.9%. The control region was 1064 bp in length. This mitogenome for the BIOT MPA T. obesus differed from the previously published T. obesus genome by 15 bp and the differences include a 2 bp insertion and 13 single nucleotide polymorphisms distributed across the mitogenome in the BIOT MPA sequence. Whole mitogenome sequence of T. obesus from the Chagos archipelago presented here fills existing gaps in genetic information on marine species from the BIOT MPA and provides additional tools for species specific assessments as to the effectiveness of MPA management. In addition, methods presented here lay the framework for genetic studies in remote locations with limited infrastructure.

Mitochondrial genome of the silky shark Carcharhinus falciformis from the British Indian Ocean Territory Marine Protected Area.

We present the first mitochondrial genome of Carcharhinus falciformis from the Chagos Archipelago in the British Indian Ocean Territory (BIOT) Marine Protected Area (MPA). The mitochondrial genome of C. falciformis is 16,701 bp in length and consists of 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and a non-coding control region (D-loop). GC content was at 40.1%. The control region was 1063 bp in length. The complete mitogenome sequence of C. falciformis from the BIOT MPA will enable improved conservation measures of the CITES listed species through studies of species distribution, population abundance, fishing pressure and wildlife trade.

Global spatial risk assessment of sharks under the footprint of fisheries.

Effective ocean management and the conservation of highly migratory species depend on resolving the overlap between animal movements and distributions, and fishing effort. However, this information is lacking at a global scale. Here we show, using a big-data approach that combines satellite-tracked movements of pelagic sharks and global fishing fleets, that 24% of the mean monthly space used by sharks falls under the footprint of pelagic longline fisheries. Space-use hotspots of commercially valuable sharks and of internationally protected species had the highest overlap with longlines (up to 76% and 64%, respectively), and were also associated with significant increases in fishing effort. We conclude that pelagic sharks have limited spatial refuge from current levels of fishing effort in marine areas beyond national jurisdictions (the high seas). Our results demonstrate an urgent need for conservation and management measures at high-seas hotspots of shark space use, and highlight the potential of simultaneous satellite surveillance of megafauna and fishers as a tool for near-real-time, dynamic management.

Cryptic habitat use of white sharks in kelp forest revealed by animal-borne video.

Traditional forms of marine wildlife research are often restricted to coarse telemetry or surface-based observations, limiting information on fine-scale behaviours such as predator-prey events and interactions with habitat features. We use contemporary animal-attached cameras with motion sensing dataloggers, to reveal novel behaviours by white sharks, Carcharodon carcharias, within areas of kelp forest in South Africa. All white sharks tagged in this study spent time adjacent to kelp forests, with several moving throughout densely kelp-covered areas, navigating through channels and pushing directly through stipes and fronds. We found that activity and turning rates significantly increased within kelp forest. Over 28 h of video data revealed that white shark encounters with Cape fur seals, Arctocephalus pusillus pusillus, occurred exclusively within kelp forests, with seals displaying predator evasion behaviour during those encounters. Uniquely, we reveal the use of kelp forest habitat by white sharks, previously assumed inaccessible to these large predators.

A comparison of linear demographic models and fraction of lifetime egg production for assessing sustainability in sharks.

Conventional methods for management of data-rich fisheries maintain sustainable populations by assuring that lifetime reproduction is adequate for individuals to replace themselves and accounting for density-dependent recruitment. Fishing is not allowed to reduce relative lifetime reproduction, the fraction of current egg production relative to unfished egg production (FLEP), below a sustainable level. Because most shark fisheries are data poor, other representations of persistence status have been used, including linear demographic models, which incorporate life-history characteristics in age-structured models with no density dependence. We tested how well measures of sustainability from 3 linear demographic methods (rebound potential, stochastic growth rate, and potential population increase) reflect actual population persistence by comparing values of these measures with FLEP for 26 shark species. We also calculated the value of fishing mortality (F) that would allow all 26 species to maintain an accepted precautionary threshold for sharks of FLEP = 60%, expressing F as a fraction of natural mortality (M). Values of stochastic growth rate and potential population growth did not covary in rank order with FLEP (p = 0.057 and p = 0.077, respectively) and neither was significantly correlated with FLEP. Ordinal ranking of rebound potential positively covaried with FLEP (p = 0.00013), but the relative rankings of some species were substantially out of order. Adopting a sustainable limit of F = 0.16M would maintain all 26 species above the precautionary minimum value of FLEP (60%). We concluded that shark-fishery and conservation policies should rely on calculation of replacement (i.e., FLEP), and that sharks should be fished at a precautionary level that would protect all stocks (i.e., F< 0.16M).

Eating or meeting? Cluster analysis reveals intricacies of white shark (Carcharodon carcharias) migration and offshore behavior.

Elucidating how mobile ocean predators utilize the pelagic environment is vital to understanding the dynamics of oceanic species and ecosystems. Pop-up archival transmitting (PAT) tags have emerged as an important tool to describe animal migrations in oceanic environments where direct observation is not feasible. Available PAT tag data, however, are for the most part limited to geographic position, swimming depth and environmental temperature, making effective behavioral observation challenging. However, novel analysis approaches have the potential to extend the interpretive power of these limited observations. Here we developed an approach based on clustering analysis of PAT daily time-at-depth histogram records to distinguish behavioral modes in white sharks (Carcharodon carcharias). We found four dominant and distinctive behavioral clusters matching previously described behavioral patterns, including two distinctive offshore diving modes. Once validated, we mapped behavior mode occurrence in space and time. Our results demonstrate spatial, temporal and sex-based structure in the diving behavior of white sharks in the northeastern Pacific previously unrecognized including behavioral and migratory patterns resembling those of species with lek mating systems. We discuss our findings, in combination with available life history and environmental data, and propose specific testable hypotheses to distinguish between mating and foraging in northeastern Pacific white sharks that can provide a framework for future work. Our methodology can be applied to similar datasets from other species to further define behaviors during unobservable phases.

Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias).

The white shark (Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (δ(13)C) and nitrogen (δ(15)N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle δ(13)C and δ(15)N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.

A first estimate of white shark, Carcharodon carcharias, abundance off Central California.

The decline of sharks in the global oceans underscores the need for careful assessment and monitoring of remaining populations. The northeastern Pacific is the home range for a genetically distinct clade of white sharks (Carcharodon carcharias). Little is known about the conservation status of this demographically isolated population, concentrated seasonally at two discrete aggregation sites: Central California (CCA) and Guadalupe Island, Mexico. We used photo-identification of dorsal fins in a sequential Bayesian mark-recapture algorithm to estimate white shark abundance off CCA. We collected 321 photographs identifying 130 unique individuals, and estimated the abundance off CCA to be 219 mature and sub-adult individuals ((130, 275) 95% credible intervals), substantially smaller than populations of other large marine predators. Our methods can be readily expanded to estimate shark population abundance at other locations, and over time, to monitor the status, population trends and protection needs of these globally distributed predators.

Long-term individual identification and site fidelity of white sharks, Carcharodon carcharias, off California using dorsal fins.

Mark-recapture techniques can be used to estimate white shark (Carcharodon carcharias) population abundance. These frameworks are based on assumptions that marks are conserved and animals are present at the sampling location over the entire duration of the study. Though these assumptions have been validated across short-time scales for white sharks, long-term studies of population trends are dependent on these assumptions being valid across longer periods. We use 22 years of photographic data from aggregation sites in central California to support the use of dorsal fin morphology as long-term individual identifiers. We identified five individuals over 16-22 years, which support the use of dorsal fins as long-time individual identifiers, illustrate strong yearly site fidelity to coastal aggregation sites across extended time periods (decades), and provide the first empirical validation of white shark longevity >22 years. These findings support the use of fin morphology in mark-recapture frameworks for white sharks.

Philopatry and migration of Pacific white sharks.

Advances in electronic tagging and genetic research are making it possible to discern population structure for pelagic marine predators once thought to be panmictic. However, reconciling migration patterns and gene flow to define the resolution of discrete population management units remains a major challenge, and a vital conservation priority for threatened species such as oceanic sharks. Many such species have been flagged for international protection, yet effective population assessments and management actions are hindered by lack of knowledge about the geographical extent and size of distinct populations. Combining satellite tagging, passive acoustic monitoring and genetics, we reveal how eastern Pacific white sharks (Carcharodon carcharias) adhere to a highly predictable migratory cycle. Individuals persistently return to the same network of coastal hotspots following distant oceanic migrations and comprise a population genetically distinct from previously identified phylogenetic clades. We hypothesize that this strong homing behaviour has maintained the separation of a northeastern Pacific population following a historical introduction from Australia/New Zealand migrants during the Late Pleistocene. Concordance between contemporary movement and genetic divergence based on mitochondrial DNA demonstrates a demographically independent management unit not previously recognized. This population's fidelity to discrete and predictable locations offers clear population assessment, monitoring and management options.