Debra L. Abercrombie

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.

Global-scale genetic identification of hammerhead sharks: Application to assessment of the international fin trade and law enforcement

The future status of sharks is an issue of widespread conservation concern due to declines in many species in the face of high levels of exploitation to satisfy market demands for products, especially fins. Substantial declines in the large-bodied hammerhead sharks, Sphyrna lewini, S. mokarran and S. zygaena, even in regions where some management occurs, indicate that informed conservation measures are warranted for these circumglobally distributed species. Despite the importance of assessing shark catch and trade on a species-specific basis to detect potential overexploitation of individual species, achieving this goal for hammerheads has proven elusive due to difficulties in identification of their products. Here, we present the development and application of a diagnostic, streamlined, five-primer multiplex polymerase chain reaction assay utilizing species-specific primers based on nuclear ribosomal ITS2 for the three hammerhead species throughout their global distribution. Application of this assay to investigations of the fin market confirmed the presence of hammerhead fins in the international trade. A study of the world’s largest fin market in Hong Kong revealed a high concordance between specific Chinese-name trade categories and fins from these three species (“Bai Chun” with S. lewini, “Gui Chun” with S. zygaena and “Gu Pian” with S.␣mokarran), and clear species preferences. This concordance information allows the use of market records for monitoring species-specific trends in trade and exploitation rates. The assay is also proving useful for identification of shark body parts in U.S. fisheries law-enforcement activities. Screening of morphologically identified “ S. lewini” from globally distributed areas using this assay with subsequent whole ITS2 sequencing suggests a cryptic species closely related to S. lewini occurs off the SE USA coast.

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.

A Novel Mini-DNA Barcoding Assay to Identify Processed Fins from Internationally Protected Shark Species

There is a growing need to identify shark products in trade, in part due to the recent listing of five commercially important species on the Appendices of the Convention on International Trade in Endangered Species (CITES; porbeagle, Lamna nasus, oceanic whitetip, Carcharhinus longimanus scalloped hammerhead, Sphyrna lewini, smooth hammerhead, S. zygaena and great hammerhead S. mokarran) in addition to three species listed in the early part of this century (whale, Rhincodon typus, basking, Cetorhinus maximus, and white, Carcharodon carcharias). Shark fins are traded internationally to supply the Asian dried seafood market, in which they are used to make the luxury dish shark fin soup. Shark fins usually enter international trade with their skin still intact and can be identified using morphological characters or standard DNA-barcoding approaches. Once they reach Asia and are traded in this region the skin is removed and they are treated with chemicals that eliminate many key diagnostic characters and degrade their DNA (“processed fins”). Here, we present a validated mini-barcode assay based on partial sequences of the cytochrome oxidase I gene that can reliably identify the processed fins of seven of the eight CITES listed shark species. We also demonstrate that the assay can even frequently identify the species or genus of origin of shark fin soup (31 out of 50 samples).

The behavioural and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal

Sand tiger sharks (Carcharias taurus) have an unusual mode of reproduction, whereby the first embryos in each of the paired uteri to reach a certain size (‘hatchlings’) consume all of their smaller siblings during gestation (‘embryonic cannibalism’ or EC). If females commonly mate with multiple males (‘behavioural polyandry’) then litters could initially have multiple sires. It is possible, however, that EC could exclude of all but one of these sires from producing offspring thus influencing the species genetic mating system (‘genetic monogamy’). Here, we use microsatellite DNA profiling of mothers and their litters (n = 15, from two to nine embryos per litter) to quantify the frequency of behavioural and genetic polyandry in this system. We conservatively estimate that nine of the females we examined (60%) were behaviourally polyandrous. The genetic mating system was characterized by assessing sibling relationships between hatchlings and revealed only 40 per cent genetic polyandry (i.e. hatchlings were full siblings in 60% of litters). The discrepancy stemmed from three females that were initially fertilized by multiple males but only produced hatchlings with one of them. This reveals that males can be excluded even after fertilizing ova and that some instances of genetic monogamy in this population arise from the reduction in litter size by EC. More research is needed on how cryptic post-copulatory and post-zygotic processes contribute to determining paternity and bridging the behavioural and genetic mating systems of viviparous species.

Methylmercury in dried shark fins and shark fin soup from American restaurants.

Consumption of meat from large predatory sharks exposes human consumers to high levels of toxic monomethylmercury (MMHg). There also have been claims that shark fins, and hence the Asian delicacy shark fin soup, contain harmful levels of neurotoxic chemicals in combination with MMHg, although concentrations of MMHg in shark fins are unknown. We measured MMHg in dried, unprocessed fins (n=50) of 13 shark species that occur in the international trade of dried shark fins as well as 50 samples of shark fin soup prepared by restaurants from around the United States. Concentrations of MMHg in fins ranged from 9 to 1720 ng/g dry wt. MMHg in shark fin soup ranged from <0.01 to 34 ng/mL, with MMHg averaging 62 ± 7% of total Hg. The highest concentrations of MMHg and total Hg were observed in both fins and soup from large, high trophic level sharks such as hammerheads (Sphyrna spp.). Consumption of a 240 mL bowl of shark fin soup containing the average concentration of MMHg (4.6 ng/mL) would result in a dose of 1.1 μg MMHg, which is 16% of the U.S. EPAs reference dose (0.1 μg MMHg per 1 kg per day in adults) of 7.4 μg per day for a 74 kg person. If consumed, the soup containing the highest measured MMHg concentration would exceed the reference dose by 17%. While shark fin soup represents a potentially important source of MMHg to human consumers, other seafood products, particularly the flesh of apex marine predators, contain much higher MMHg concentrations and can result in substantially greater exposures of this contaminant for people.

Into the deep: the functionality of mesopelagic excursions by an oceanic apex predator

Abstract Comprehension of ecological processes in marine animals requires information regarding dynamic vertical habitat use. While many pelagic predators primarily associate with epipelagic waters, some species routinely dive beyond the deep scattering layer. Actuation for exploiting these aphotic habitats remains largely unknown. Recent telemetry data from oceanic whitetip sharks (Carcharhinus longimanus) in the Atlantic show a strong association with warm waters (>20°C) less than 200 m. Yet, individuals regularly exhibit excursions into the meso‐ and bathypelagic zone. In order to examine deep‐diving behavior in oceanic whitetip sharks, we physically recovered 16 pop‐up satellite archival tags and analyzed the high‐resolution depth and temperature data. Diving behavior was evaluated in the context of plausible functional behavior hypotheses including interactive behaviors, energy conservation, thermoregulation, navigation, and foraging. Mesopelagic excursions (n = 610) occurred throughout the entire migratory circuit in all individuals, with no indication of site specificity. Six depth‐versus‐time descent and ascent profiles were identified. Descent profile shapes showed little association with examined environmental variables. Contrastingly, ascent profile shapes were related to environmental factors and appear to represent unique behavioral responses to abiotic conditions present at the dive apex. However, environmental conditions may not be the sole factors influencing ascents, as ascent mode may be linked to intentional behaviors. While dive functionality remains unconfirmed, our study suggests that mesopelagic excursions relate to active foraging behavior or navigation. Dive timing, prey constituents, and dive shape support foraging as the most viable hypothesis for mesopelagic excursions, indicating that the oceanic whitetip shark may regularly survey extreme environments (deep depths, low temperatures) as a foraging strategy. At the apex of these deep‐water excursions, sharks exhibit a variable behavioral response, perhaps, indicating the presence or absence of prey.

Species composition of the international shark fin trade assessed through a retail-market survey in Hong Kong

The shark fin trade is a major driver of shark exploitation in fisheries all over the world, most of which are not managed on a species-specific basis. Species-specific trade information highlights taxa of particular concern and can be used to assess the efficacy of management measures and anticipate emerging threats. The species composition of the Hong Kong Special Administrative Region of China, one of the worlds largest fin trading hubs, was partially assessed in 1999-2001. We randomly selected and genetically identified fin trimmings (n = 4800), produced during fin processing, from the retail market of Hong Kong in 2014-2015 to assess contemporary species composition of the fin trade. We used nonparametric species estimators to determine that at least 76 species of sharks, batoids, and chimaeras supplied the fin trade and a Bayesian model to determine their relative proportion in the market. The diversity of traded species suggests species substitution could mask depletion of vulnerable species; one-third of identified species are threatened with extinction. The Bayesian model suggested that 8 species each comprised >1% of the fin trimmings (34.1-64.2% for blue [Prionace glauca], 0.2-1.2% for bull [Carcharhinus leucas] and shortfin mako [Isurus oxyrinchus]); thus, trade was skewed to a few globally distributed species. Several other coastal sharks, batoids, and chimaeras are in the trade but poorly managed. Fewer than 10 of the species we modeled have sustainably managed fisheries anywhere in their range, and the most common species in trade, the blue shark, was not among them. Our study and approach serve as a baseline to track changes in composition of species in the fin trade over time to better understand patterns of exploitation and assess the effects of emerging management actions for these animals.

A multiplex PCR mini-barcode assay to identify processed shark products in the global trade

Protecting sharks from overexploitation has become global priority after widespread population declines have occurred. Tracking catches and trade on a species-specific basis has proven challenging, in part due to difficulties in identifying processed shark products such as fins, meat, and liver oil. This has hindered efforts to implement regulations aimed at promoting sustainable use of commercially important species and protection of imperiled species. Genetic approaches to identify shark products exist but are typically based on sequencing or amplifying large DNA regions and may fail to work on heavily processed products in which DNA is degraded. Here, we describe a novel multiplex PCR mini-barcode assay based on two short fragments of the cytochrome oxidase I (COI) gene. This assay can identify to species all sharks currently listed on the Convention of International Trade of Endangered Species (CITES) and most shark species present in the international trade. It achieves species diagnosis based on a single PCR and one to two downstream DNA sequencing reactions. The assay is capable of identifying highly processed shark products including fins, cooked shark fin soup, and skin-care products containing liver oil. This is a straightforward and reliable identification method for data collection and enforcement of regulations implemented for certain species at all governance levels.