Camrin D. Braun

Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea.

Knowledge of the habitat use and migration patterns of large sharks is important for assessing the effectiveness of large predator Marine Protected Areas (MPAs), vulnerability to fisheries and environmental influences, and management of shark–human interactions. Here we compare movement, reef-fidelity, and ocean migration for tiger sharks, Galeocerdo cuvier, across the Coral Sea, with an emphasis on New Caledonia. Thirty-three tiger sharks (1.54 to 3.9 m total length) were tagged with passive acoustic transmitters and their localised movements monitored on receiver arrays in New Caledonia, the Chesterfield and Lord Howe Islands in the Coral Sea, and the east coast of Queensland, Australia. Satellite tags were also used to determine habitat use and movements among habitats across the Coral Sea. Sub-adults and one male adult tiger shark displayed year-round residency in the Chesterfields with two females tagged in the Chesterfields and detected on the Great Barrier Reef, Australia, after 591 and 842 days respectively. In coastal barrier reefs, tiger sharks were transient at acoustic arrays and each individual demonstrated a unique pattern of occurrence. From 2009 to 2013, fourteen sharks with satellite and acoustic tags undertook wide-ranging movements up to 1114 km across the Coral Sea with eight detected back on acoustic arrays up to 405 days after being tagged. Tiger sharks dove 1136 m and utilised three-dimensional activity spaces averaged at 2360 km3. The Chesterfield Islands appear to be important habitat for sub-adults and adult male tiger sharks. Management strategies need to consider the wide-ranging movements of large (sub-adult and adult) male and female tiger sharks at the individual level, whereas fidelity to specific coastal reefs may be consistent across groups of individuals. Coastal barrier reef MPAs, however, only afford brief protection for large tiger sharks, therefore determining the importance of other oceanic Coral Sea reefs should be a priority for future research.

Extreme diving behaviour in devil rays links surface waters and the deep ocean

Ecological connections between surface waters and the deep ocean remain poorly studied despite the high biomass of fishes and squids residing at depths beyond the euphotic zone. These animals likely support pelagic food webs containing a suite of predators that include commercially important fishes and marine mammals. Here we deploy pop-up satellite archival transmitting tags on 15 Chilean devil rays (Mobula tarapacana) in the central North Atlantic Ocean, which provide movement patterns of individuals for up to 9 months. Devil rays were considered surface dwellers but our data reveal individuals descending at speeds up to 6.0 m s−1 to depths of almost 2,000 m and water temperatures <4 °C. The shape of the dive profiles suggests that the rays are foraging at these depths in deep scattering layers. Our results provide evidence of an important link between predators in the surface ocean and forage species occupying pelagic habitats below the euphotic zone in ocean ecosystems.

Diving Behavior of the Reef Manta Ray Links Coral Reefs with Adjacent Deep Pelagic Habitats

Recent successful efforts to increase protection for manta rays has highlighted the lack of basic ecological information, including vertical and horizontal movement patterns, available for these species. We deployed pop-up satellite archival transmitting tags on nine reef manta rays, Manta alfredi, to determine diving behaviors and vertical habitat use. Transmitted and archived data were obtained from seven tagged mantas over deployment periods of 102–188 days, including three recovered tags containing 2.6 million depth, temperature, and light level data points collected every 10 or 15 seconds. Mantas frequented the upper 10 m during daylight hours and tended to occupy deeper water throughout the night. Six of the seven individuals performed a cumulative 76 deep dives (>150 m) with one individual reaching 432 m, extending the known depth range of this coastal, reef-oriented species and confirming its role as an ecological link between epipelagic and mesopelagic habitats. Mean vertical velocities calculated from high-resolution dive data (62 dives >150 m) from three individuals suggested that mantas may use gliding behavior during travel and that this behavior may prove more efficient than continuous horizontal swimming. The behaviors in this study indicate manta rays provide a previously unknown link between the epi- and mesopelagic layers of an extremely oligotrophic marine environment and provide evidence of a third marine species that utilizes gliding to maximize movement efficiency.

Movement Patterns of Juvenile Whale Sharks Tagged at an Aggregation Site in the Red Sea

Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009–2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5–7 m total length with a sex ratio of approximately 1∶1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.

First record of living Manta alfredi × Manta birostris hybrid

Following a recent taxonomic revision, two manta species (Manta alfredi and Manta birostris ) have been advocated based on meristic and morphological characteristics (Marshall et al. 2009). Subsequent genetic analyses of the two species using mitochondrial and nuclear markers confirmed two distinguishable genetic groups (Kashiwagi et al. 2012). Using the above taxonomic and genetic criteria, we provide evidence for the first record of a living Manta alfredi ×Manta birostris hybrid. The Manta individual (Fig. 1a, b) was non-lethally sampled from a known manta aggregation site in Dunganab Bay, Sudan, Red Sea, in October 2012. The individual was identified in the field as Manta alfredi based on distinguishing morphological criteria: dorsoventral colouration/spot patterns, mouth and pectoral fin colouration, and absence of remnant spine (Fig. 1b; Marshall et al. 2009). DNA was recovered from a fin clip using standard molecular genetic protocols. The mitochondrial gene ND5 (1,154 bp) and nuclear gene RAG1 (646 bp) were amplified following Kashiwagi et al. (2012), and sequenced. Recovered sequences (GenBank accession nos. KF574269-KF574270) were aligned with those previously reported (Kashiwagi et al. 2012) and a haplotype network was constructed in TCS 1.21 (Clement et al. 2000). TheManta specimen was confirmed to carry a newManta alfredi mtDNA haplotype (red in Fig. 1). However, the RAG1 sequence indicates that this individual is an interspecific hybrid. The twoManta species are reciprocally monophyletic at the RAG1 locus, which contains two species-specific single nucleotide polymorphisms (SNPs): at position 73 (M . alfredi : G; M . birostris : A) and position 507 (M . alfredi : A; M . birostris : C) following Kashiwagi et al. (2012). The hybrid individual is heterozygous at both SNPs (see inset chromatograms). Heterozygosity was confirmed by sequencing this individual in triplicate in both forward and reverse directions at RAG1 . Our finding indicates that reproductive isolation among M . alfredi and M . birostris may be less complete than previously thought, or alternatively, that species-specific taxonomic and genetic differentiation is not as unambiguous as currently suggested. Given the designation of the two discrete species as vulnerable on the IUCN Red List and their recent listing on CITES appendix II following concern over increasing global R. P. Walter (*) : S. T. Kessel :A. T. Fisk :D. D. Heath : N. E. Hussey University of Windsor – GLIER, Windsor, Canada e-mail: rwalter@uwindsor.ca

Population structure of a whale shark Rhincodon typus aggregation in the Red Sea.

The presence of whale sharks Rhincodon typus were recorded around Shib Habil, a small, coastal reef off the Red Sea coast of Saudi Arabia, from 2010 to 2015. A total of 267 suitable photographs resulting in the identification of 136 individuals, were documented from 305 encounters. Sharks were divided evenly between the sexes with no evidence of temporal or spatial segregation. All individuals were immature based on size estimates and, for males, juvenile clasper morphology. Scars were reported for 57% of R. typus with 15% showing evidence of propeller trauma. Estimates of population size and patterns of residency were calculated by modelling the lagged identification rate. Multiple models were run simultaneously and compared using the Akaike information criterion. An open population model was found to best represent the data and estimates a daily abundance between 15 and 34 R. typus during the aggregation season, with local residence times ranging from 4 to 44 days. Residence times away from Shib Habil range from 15 to 156 days with a permanent emigration-death rate between 0·07 and 0·58 individuals year(-1) . These results are broadly similar to those from other aggregations of R. typus, although the observed sexual parity and integration found at this site is unique for the species and needs further study.

HMMoce: An R package for improved geolocation of archival‐tagged fishes using a hidden Markov method

Electronic tagging of marine fishes is commonly achieved with archival tags that rely on light levels and sea surface temperatures to retrospectively estimate movements. However, methodological issues associated with light-level geolocation have constrained meaningful inference to species where it is possible to accurately estimate time of sunrise and sunset. Most studies have largely ignored the oceanographic profiles collected by the tag as a potential way to refine light-level geolocation estimates. Open-source oceanographic measurements and outputs from high-resolution models are increasingly available and accessible. Temperature and depth profiles recorded by electronic tags can be integrated with these empirical data and model outputs to construct likelihoods and improve geolocation estimates. The R package HMMoce leverages available tag and oceanographic data to improve position estimates derived from electronic tags using a hidden Markov approach. We illustrate the use of the model and test its performance using example blue and mako shark archival tag data. Model results were validated using independent, known tracks and compared to results from other geolocation approaches. HMMoce exhibited as much as six-fold improvement in pointwise error as compared to traditional light-level geolocation approaches. The results demonstrated the general applicability of HMMoce to marine animals, particularly those that do not frequent surface waters during crepuscular periods.

Isolation and characterization of 29 microsatellite markers for the bumphead parrotfish, Bolbometopon muricatum, and cross amplification in 12 related species

We isolated and characterized 29 microsatellite loci for the bumphead parrotfish, Bolbometopon muricatum, a wide-ranging parrotfish listed as vulnerable by the International Union for Conservation of Nature (IUCN). The 29 loci were tested on 95 individuals sampled from the Solomon Islands. The number of alleles ranged from two to ten. Evidence of linkage disequilibrium was found for only one pair of loci (Bm54 and Bm112). Two loci (Bm20 and Bm119) showed significant departure from Hardy-Weinberg equilibrium. We also tested each locus for amplification and polymorphism on 11 other scarine labrid species and one labrid species. Amplification success ranged from zero to ten loci per species. These microsatellite loci are the first specific set for B. muricatum and will be a useful tool for assessing genetic population structure, genetic diversity, and parentage in future studies.

Convergence of marine megafauna movement patterns in coastal and open oceans

Significance Understanding the key drivers of animal movement is crucial to assist in mitigating adverse impacts of anthropogenic activities on marine megafauna. We found that movement patterns of marine megafauna are mostly independent of their evolutionary histories, differing significantly from patterns for terrestrial animals. We detected a remarkable convergence in the distribution of speed and turning angles across organisms ranging from whales to turtles (epitome for the slowest animals on land but not at sea). Marine megafauna show a prevalence of movement patterns dominated by search behavior in coastal habitats compared with more directed, ballistic movement patterns when the animals move across the open ocean. The habitats through which they move will therefore need to be considered for effective conservation. The extent of increasing anthropogenic impacts on large marine vertebrates partly depends on the animals’ movement patterns. Effective conservation requires identification of the key drivers of movement including intrinsic properties and extrinsic constraints associated with the dynamic nature of the environments the animals inhabit. However, the relative importance of intrinsic versus extrinsic factors remains elusive. We analyze a global dataset of ∼2.8 million locations from >2,600 tracked individuals across 50 marine vertebrates evolutionarily separated by millions of years and using different locomotion modes (fly, swim, walk/paddle). Strikingly, movement patterns show a remarkable convergence, being strongly conserved across species and independent of body length and mass, despite these traits ranging over 10 orders of magnitude among the species studied. This represents a fundamental difference between marine and terrestrial vertebrates not previously identified, likely linked to the reduced costs of locomotion in water. Movement patterns were primarily explained by the interaction between species-specific traits and the habitat(s) they move through, resulting in complex movement patterns when moving close to coasts compared with more predictable patterns when moving in open oceans. This distinct difference may be associated with greater complexity within coastal microhabitats, highlighting a critical role of preferred habitat in shaping marine vertebrate global movements. Efforts to develop understanding of the characteristics of vertebrate movement should consider the habitat(s) through which they move to identify how movement patterns will alter with forecasted severe ocean changes, such as reduced Arctic sea ice cover, sea level rise, and declining oxygen content.

Integrating Archival Tag Data and a High-Resolution Oceanographic Model to Estimate Basking Shark (Cetorhinus maximus) Movements in the Western Atlantic

Basking shark (Cetorhinus maximus) populations are considered ‘vulnerable’ globally and ‘endangered’ in the northeast Atlantic by the International Union for the Conservation of Nature. Much of our knowledge of this species comes from surface observations in coastal waters, yet recent evidence suggests the majority of their lives may be spent in the deep ocean. Depth preferences of basking sharks have significantly limited movement studies that used pop-up satellite archival transmitting (PSAT) tags as conventional light-based geolocation is impossible for tagged animals that spend significant time below the photic zone. We tagged 57 basking sharks with PSAT tags in the NW Atlantic from 2004-2011. Many individuals spent several months at meso- and bathy-pelagic depths where accurate light-level geolocation was impossible during fall, winter and spring. We applied a newly-developed geolocation approach for the PSAT data by comparing three-dimensional depth-temperature profile data recorded by the tags to modeled in-situ oceanographic data from the high-resolution HYbrid Coordinate Ocean Model (HYCOM). Observation-based likelihoods were leveraged within a state-space hidden Markov model (HMM). The combined tracks revealed that basking sharks moved from waters around Cape Cod, MA to as far as the SE coast of Brazil (20°S), a total distance of over 17,000km. Moreover, 59% of tagged individuals with sufficient deployment durations (> 250 days) demonstrated seasonal fidelity to Cape Cod and the Gulf of Maine, with one individual returning to within 60 km of its tagging location one year later. Tagged sharks spent most of their time at epipelagic depths during summer months around Cape Cod and in the Gulf of Maine. During winter months, sharks spent extended periods at depths of at least 600 m while moving south to the Sargasso Sea, the Caribbean Sea, or the western tropical Atlantic. Our work demonstrates the utility of applying advances in oceanographic modeling to understanding habitat use of highly migratory, often meso- and bathy-pelagic, ocean megafauna. The large-scale movement patterns of tagged sharks highlight the need for international cooperation when designing and implementing conservation strategies to ensure that the species recovers from the historical effects of over-fishing throughout the North Atlantic Ocean.