Demian D. Chapman

Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions.

Stable-isotope analysis (SIA) can act as a powerful ecological tracer with which to examine diet, trophic position and movement, as well as more complex questions pertaining to community dynamics and feeding strategies or behaviour among aquatic organisms. With major advances in the understanding of the methodological approaches and assumptions of SIA through dedicated experimental work in the broader literature coupled with the inherent difficulty of studying typically large, highly mobile marine predators, SIA is increasingly being used to investigate the ecology of elasmobranchs (sharks, skates and rays). Here, the current state of SIA in elasmobranchs is reviewed, focusing on available tissues for analysis, methodological issues relating to the effects of lipid extraction and urea, the experimental dynamics of isotopic incorporation, diet-tissue discrimination factors, estimating trophic position, diet and mixing models and individual specialization and niche-width analyses. These areas are discussed in terms of assumptions made when applying SIA to the study of elasmobranch ecology and the requirement that investigators standardize analytical approaches. Recommendations are made for future SIA experimental work that would improve understanding of stable-isotope dynamics and advance their application in the study of sharks, skates and rays.

Marine reserve design and evaluation using automated acoustic telemetry: A case-study involving coral reef-associated sharks in the mesoamerican Caribbean

A non-overlapping acoustic receiver array was used to track the movements of two common shark species, nurse Ginglymostoma cirratum (n=25) and Caribbean reef Carcharhinus perezi (n=5), in and around Glover’s Reef Marine Reserve (GRMR), off the coast of Belize, between May and October, 2004. Although both species exhibited partial site fidelity in that they were most likely to be detected near the area of original capture, both species also moved widely throughout the 10 by 30 km atoll. One Caribbean reef shark was detected by a monitor at Lighthouse Reef, 30 km from Glover’s Reef across deep (>400m) open water. The mean minimum linear dispersal (MLD) was 10.5 km for Caribbean reef sharks and 7.7 km for nurse sharks, with many individuals traveling more than the 10 km width of the no-take “conservation zone” of the marine reserve. Although most sharks were tagged within the conservation zone, individuals were detected outside this part of GRMR on average 48 days out of the 150 days of observations. However, of 7 nurse sharks tagged near the center of the conservation zone, 4 were never detected outside of this part of the reserve. In general, this study suggests that effective conservation of these large roving predators requires an ecosystem-based management approach including a zoned management plan, similar to that used at GRMR, in which a fairly large no-take reserve, incorporating diverse habitats and the connections between them, is surrounded by a larger area in which fishing is regulated. S I N T R O D U C T I O N harks are increasingly threatened by overexploitation and habitat degradation around the world, and marine reserves are now being considered as a potential component of conservation strategies for these top-predators (Camhi, 1998; FAO, 2000; Watts, 2001; Baum et al., 2003; Simpfendorfer & Heupel, 2004). However, because sharks can range widely (Kohler et al., 1998; Holland et al., 1999; Boustany et al., 2002) and no-take marine reserves will

Reef sharks exhibit site-fidelity and higher relative abundance in marine reserves on the Mesoamerican Barrier Reef.

Carcharhinid sharks can make up a large fraction of the top predators inhabiting tropical marine ecosystems and have declined in many regions due to intense fishing pressure. There is some support for the hypothesis that carcharhinid species that complete their life-cycle within coral reef ecosystems, hereafter referred to as “reef sharks”, are more abundant inside no-take marine reserves due to a reduction in fishing pressure (i.e., they benefit from marine reserves). Key predictions of this hypothesis are that (a) individual reef sharks exhibit high site-fidelity to these protected areas and (b) their relative abundance will generally be higher in these areas compared to fished reefs. To test this hypothesis for the first time in Caribbean coral reef ecosystems we combined acoustic monitoring and baited remote underwater video (BRUV) surveys to measure reef shark site-fidelity and relative abundance, respectively. We focused on the Caribbean reef shark (Carcharhinus perezi), the most common reef shark in the Western Atlantic, at Glovers Reef Marine Reserve (GRMR), Belize. Acoustically tagged sharks (N = 34) were detected throughout the year at this location and exhibited strong site-fidelity. Shark presence or absence on 200 BRUVs deployed at GRMR and three other sites (another reserve site and two fished reefs) showed that the factor “marine reserve” had a significant positive effect on reef shark presence. We rejected environmental factors or site-environment interactions as predominant drivers of this pattern. These results are consistent with the hypothesis that marine reserves can benefit reef shark populations and we suggest new hypotheses to determine the underlying mechanism(s) involved: reduced fishing mortality or enhanced prey availability.

A streamlined, bi-organelle, multiplex PCR approach to species identification: Application to global conservation and trade monitoring of the great white shark, Carcharodon carcharias

The great white shark, Carcharodoncarcharias, is the most widely protectedelasmobranch in the world, and is classified asVulnerable by the IUCN and listed on AppendixIII of CITES. Monitoring of trade in whiteshark products and enforcement of harvest andtrade prohibitions is problematic, however, inlarge part due to difficulties in identifyingmarketed shark parts (e.g., dried fins, meatand processed carcasses) to species level. Toaddress these conservation and managementproblems, we have developed a rapid, moleculardiagnostic assay based on species-specific PCRprimer design for accurate identification ofwhite shark body parts, including dried fins. The assay is novel in several respects: Itemploys a multiplex PCR assay utilizing bothnuclear (ribosomal internal transcribed spacer2) and mitochondrial (cytochrome b) locisimultaneously to achieve a highly robustmeasure of diagnostic accuracy; it is verysensitive, detecting the presence of whiteshark DNA in a mixture of genomic DNAs from upto ten different commercially fished sharkspecies pooled together in a single PCR tube;and it successfully identifies white shark DNAfrom globally distributed animals. Inaddition to its utility for white shark trademonitoring and conservation applications, thishighly streamlined, bi-organelle, multiplex PCRassay may prove useful as a general model forthe design of genetic assays aimed at detectingbody parts from other protected and threatenedspecies.

Virgin birth in a hammerhead shark.

Parthenogenesis has been documented in all major jawed vertebrate lineages except mammals and cartilaginous fishes (class Chondrichthyes: sharks, batoids and chimeras). Reports of captive female sharks giving birth despite being held in the extended absence of males have generally been ascribed to prior matings coupled with long-term sperm storage by the females. Here, we provide the first genetic evidence for chondrichthyan parthenogenesis, involving a hammerhead shark (Sphyrna tiburo). This finding also broadens the known occurrence of a specific type of asexual development (automictic parthenogenesis) among vertebrates, extending recently raised concerns about the potential negative effect of this type of facultative parthenogenesis on the genetic diversity of threatened vertebrate species.

There and Back Again: A Review of Residency and Return Migrations in Sharks, with Implications for Population Structure and Management

The overexploitation of sharks has become a global environmental issue in need of a comprehensive and multifaceted management response. Tracking studies are beginning to elucidate how shark movements shape the internal dynamics and structure of populations, which determine the most appropriate scale of these management efforts. Tracked sharks frequently either remain in a restricted geographic area for an extended period of time (residency) or return to a previously resided-in area after making long-distance movements (site fidelity). Genetic studies have shown that some individuals of certain species preferentially return to their exact birthplaces (natal philopatry) or birth regions (regional philopatry) for either parturition or mating, even though they make long-distance movements that would allow them to breed elsewhere. More than 80 peer-reviewed articles, constituting the majority of published shark tracking and population genetic studies, provide evidence of at least one of these behaviors in a combined 31 shark species from six of the eight extant orders. Residency, site fidelity, and philopatry can alone or in combination structure many coastal shark populations on finer geographic scales than expected based on their potential for dispersal. This information should therefore be used to scale and inform assessment, management, and conservation activities intended to restore depleted shark populations.

Two decades of genetic profiling yields first evidence of natal philopatry and long‐term fidelity to parturition sites in sharks

Sharks are a globally threatened group of marine fishes that often breed in their natal region of origin. There has even been speculation that female sharks return to their exact birthplace to breed (‘natal philopatry’), which would have important conservation implications. Genetic profiling of lemon sharks (Negaprion brevirostris) from 20 consecutive cohorts (1993–2012) at Bimini, Bahamas, showed that certain females faithfully gave birth at this site for nearly two decades. At least six females born in the 1993–1997 cohorts returned to give birth 14–17 years later, providing the first direct evidence of natal philopatry in the chondrichthyans. Long‐term fidelity to specific nursery sites coupled with natal philopatry highlights the merits of emerging spatial and local conservation efforts for these threatened predators.

Predominance of genetic monogamy by females in a hammerhead shark, Sphyrna tiburo: implications for shark conservation

There is growing interest in the mating systems of sharks and their relatives (Class Chondrichthyes) because these ancient fishes occupy a key position in vertebrate phylogeny and are increasingly in need of conservation due to widespread overexploitation. Based on precious few genetic and field observational studies, current speculation is that polyandrous mating strategies and multiple paternity may be common in sharks as they are in most other vertebrates. Here, we test this hypothesis by examining the genetic mating system of the bonnethead shark, Sphyrna tiburo, using microsatellite DNA profiling of 22 litters (22 mothers, 188 embryos genotyped at four polymorphic loci) obtained from multiple locations along the west coast of Florida. Contrary to expectations based on the ability of female S. tiburo to store sperm, the social nature of this species and the 100% multiple paternity observed in two other coastal shark species, over 81% of sampled bonnethead females produced litters sired by a single male (i.e. genetic monogamy). When multiple paternity occurred in S. tiburo, there was an indication of increased incidence in larger mothers with bigger litters. Our data suggest that sharks may exhibit complex genetic mating systems with a high degree of interspecific variability, and as a result some species may be more susceptible to loss of genetic variation in the face of escalating fishing pressure. Based on these findings, we suggest that knowledge of elasmobranch mating systems should be an important component of conservation and management programmes for these heavily exploited species.

Genetic profiling reveals illegal international trade in fins of the great white shark, Carcharodon carcharias

Great white sharks are protected by national legislation in several countries, making this species the most widely protected elasmobranch in the world. Although the market demand for shark fins in general has continued to grow, the value and extent of utilization of white shark fins in trade has been controversial. We combine law enforcement with genetic profiling to demonstrate that illegal trade in fins of this species is occurring in the contemporary international market. Furthermore, we document the presence of fins from very young white sharks in the trade, suggesting a multiple-use market (food to trophies) exists for fins of this species. The presence of small fins in the trade contradicts the view that white shark fins have market value only as large display trophies, and not as food. Our findings indicate that effective conservation of protected shark species will require international management regimes that include monitoring of the shark fishery and trade on a species-specific basis.

Complex Movements, Philopatry and Expanded Depth Range of a Severely Threatened Pelagic Shark, the Oceanic Whitetip (Carcharhinus longimanus) in the Western North Atlantic

Oceanic whitetip sharks (Carcharhinus longimanus) have recently been targeted for conservation in the western North Atlantic following severe declines in abundance. Pop-up satellite archival tags were applied to 11 mature oceanic whitetips (10 females, 1 male) near Cat Island in the central Bahamas 1–8 May 2011 to provide information about the horizontal and vertical movements of this species. Another large female was opportunistically tagged in the U.S. Exclusive Economic Zone (EEZ). Data from 1,563 total tracking days and 1,142,598 combined depth and temperature readings were obtained. Sharks tagged at Cat Island stayed within 500 km of the tagging site for ∼30 days before dispersing across 16,422 km2 of the western North Atlantic. Maximum individual displacement from the tagging site ranged from 290–1940 km after times at liberty from 30–245 days, with individuals moving to several different destinations (the northern Lesser Antilles, the northern Bahamas, and north of the Windward Passage). Many sharks returned to The Bahamas after ∼150 days. Estimated residency times within The Bahamas EEZ, where longlining and commercial trade of sharks is illegal, were generally high (mean = 68.2% of time). Sharks spent 99.7% of their time shallower than 200 m and did not exhibit differences in day and night mean depths. There was a positive correlation between daily sea surface temperature and mean depth occupied, suggesting possible behavioral thermoregulation. All individuals made short duration (mean = 13.06 minutes) dives into the mesopelagic zone (down to 1082 m and 7.75°C), which occurred significantly more often at night. Ascent rates during these dives were significantly slower than descent rates, suggesting that these dives are for foraging. The sharks tracked appear to be most vulnerable to pelagic fishing gear deployed from 0–125 m depths, which they may encounter from June to October after leaving the protected waters of The Bahamas EEZ.