A truer measure of the market: the molecular ecology of fisheries and wildlife trade

Wildlife and fisheries markets are end-points in the supply chain of both legitimate and illegitimate or unregulated trade in species and natural products. Molecular ecology provides powerful tools for surveillance and estimation of this trade. Here, I review the application of these tools to market surveys and species in trade, including species identification and molecular taxonomy, population assignment and 'mixed-stock' analysis, genetic tracking and capture-recapture by individual identification. I consider the analogy of markets to natural populations and also the unique features that require novel analytical approaches and sampling design. In the most developed of these applications, the molecular ecology of market surveys and confiscated trade shipments has provided independent estimates of illegal, unregulated or unreported exploitation for sharks, elephants and whales. Although each study has taken advantage of information from trade records or official government reports concerning the ostensible levels of exploitation, it is telling that the truer measure of exploitation seems to arise from the market end-point of the supply chain.     

Incomplete reporting of whale, dolphin and porpoise 'bycatch' revealed by molecular monitoring of Korean markets

We report the results of molecular monitoring of 'whalemeat' markets in the Republic of (South) Korea based on nine systematic surveys from February 2003 to February 2005. As Korea has no programme of commercial or scientific whaling and there is a closure on the hunting of dolphins and porpoises, the only legal source of these products was assumed to be incidental fisheries mortalities ('bycatch') as reported by the government to the International Whaling Commission. Species identification of 357 products using mitochondrial DNA control region or cytochrome b sequences and the web-based programme DNA-surveillance revealed three species of baleen whales (North Pacific minke, common form Bryde's and humpback), three species of beaked whales (Cuvier's, Stejneger's and Blainville's), seven species of dolphins (short-finned pilot, false killer and killer whales; Risso's, bottlenose, common and Pacific white-sided dolphins) and two species of porpoises (harbour and finless). Comparison of market products with official records revealed a number of discrepancies. Of the eight species identified on the markets in 2003, three were not reported in official records for that year. Of the 11 species identified in 2004, five were not reported as bycatch, although one species, a humpback whale, was reported as 'stranded'. We also found significant inconsistencies in the expected frequencies of products from most species, including a large over-representation of finless porpoises and false killer whales. We suggest ways in which market surveys could be improved to provide better information on the magnitude of fisheries bycatch and other illegal, unregulated and unreported (IUU) exploitation of wildlife.     

Bushmeat and bycatch: the sum of the parts

In many developing countries, the killing of wild animals for commercial purposes (the bushmeat trade) is a significant factor in the reduction of biodiversity, and probably represents a major threat to the survival of many more populations than we know. This includes marine species such as cetaceans, sea turtles and sirenians ("marine bushmeat"), which are often neglected in the discussion of this issue. Estimating the impact of the bushmeat trade anywhere is problematic because even the most thorough visual surveys of meat markets cannot easily translate an observed quantity of butchered products into the number of animals killed. In this issue of Molecular Ecology, Baker et al. provide a powerful new tool for such assessments: molecular identification of commercially available products from a depleted population of minke whales in South Korea is combined with genotyping and novel capture-recapture methods to estimate not only the number of individuals taken, but also the persistence of the resulting products in the marketplace.     

Predicted decline of protected whales based on molecular genetic monitoring of Japanese and Korean markets

We present a two-tiered analysis of molecular genetic variation in order to determine the origins of whale' products purchased from retail markets in Japan and the Republic of (South) Korea during 1993-1999. This approach combined phylogenetic analysis of mitochondrial DNA sequences for identification of protected species with a statistical comparison of intraspecific haplotype frequencies for distinguishing regional subpopulations or 'stocks' hunted for scientific research by the Japanese and killed incidentally in coastal fisheries by the Koreans. The phylogenetic identification of 655 products included eight species or subspecies of baleen whales, sperm whales, a pygmy sperm whale, two species of beaked whales, porpoises, killer whales and numerous species of dolphins as well as domestic sheep and horses. Six of the baleen whale species (the fin, sei, common-form and small-form Bryde's, blue or blue/fin hybrid, and humpback) and the sperm whale are protected by international agreements dating back to at least 1989 for all species and 1966 for some species. We compared the haplotype frequencies from the Japanese market sample to those reported from scientific hunting in the western North Pacific stock for products derived from the exploited North Pacific minke whale. The market sample differed significantly from the scientific catch (p < 0.001), showing a greater than expected frequency of haplotypes characteristic of the protected Sea of Japan stock. We used a 'mixed-stock' analysis and maximum-likelihood methods to estimate that 31% (95% confidence interval 19-43%) of the market for this species originated from the Sea of Japan stock. The source of these products was assumed to be undocumented 'incidental takes' from fisheries' by-catch, although we cannot exclude the possibility of illegal hunting or smuggling. The demographic impact of this undocumented exploitation was evaluated using the model of population dynamics adopted by the Scientific Committee of the International Whaling Commission. For the range of exploitation consistent with the market sample, this protected stock was predicted to decline towards extinction over the next few decades. These results confirmed the power of molecular methods in monitoring retail markets and pointed to the inadequacy of the current moratorium for ensuring the recovery of protected species. More importantly, the integration of genetic evidence with a model of population dynamics identified an urgent need for actions to limit undocumented exploitation of a 'protected' stock of whales.     

CAPTURE-RECAPTURE ESTIMATES OF HECTOR'S DOLPHIN ABUNDANCE AT BANKS PENINSULA, NEW ZEALAND

Capture-recapture techniques have been extensively used to estimate survival rates of Hector's dolphins at Banks Peninsula, but not abundance. We analyzed nine seasons of photo-identification data using a model-fitting approach in the computer program MARK, and then used MARK's estimates of capture probabilities to calculate the abundance of distinctive individuals. We extrapolated these estimates to include unmarked individuals using five seasons of data on the proportion of identifiable individuals in this population, obtained from "random photography." This capture-recapture approach suggests a 1996 population of about 1,100 (CV = 0.21). This is very similar to the 1997 line-transect estimate of about 900 (CV = 0.28), especially considering that the two techniques do not necessarily measure the same thing. An important advantage of the capture-recapture approach stems from the inherent versatility of photo-ID data. If the sampling design is appropriate, an unbiased abundance estimate can be achieved as a spin-off from work directed at other questions. However, in our view, line-transect estimates are easier to interpret because the sampling design is explicit.     

Forensic genetic identification of sturgeon caviars traveling in world trade

Caviar is among the world’s most valuable wildlife products. Exploitation of sturgeon and paddlefish for the caviar trade has severely reduced abundance, and harvest of most species is regulated under CITES. International trade requires that importing nations verify the species source of caviars they receive; the US domestic trade has no such requirement. We report the results of forensic species identifications of US caviar imports from 1998 to 2008 and of US domestic market caviars from 1997 to 1998. Twelve species were identified overall and species origins were mislabeled three times as often among US domestic market caviars (14.7 %) as among imports (4.9 %). Industry practices associated with the re-packaging of caviars for domestic markets and re-export from intermediate countries have created opportunities for the co-mingling of legitimate caviars with those from illegal, unreported and unregulated sources.     

The catch and trade of seahorses in Vietnam

Catch monitoring and surveys were used to assess the seahorse trade in Vietnam. Despite low daily catch rates, potentially 6.5 t of dried seahorses (~2.2 million seahorses) were taken annually as bycatch by trawlers operating out of five coastal provinces of Vietnam. Individual seahorse catches were collated by a few local buyers, who supplied wholesalers in three major markets: Ho Chi Minh City, Hai Phong City and Da Nang. Domestic consumption was small and most seahorses were exported, generally through unofficial and unregulated channels across the northern border into Guangxi province of China. Overall, the seahorse trade was of low economic value to Vietnam, but may constitute an important source of income to upper level buyers and exporters. Most fishers and buyers surveyed reported that seahorse catch had declined over time. This paper should help in meeting the new CITES requirements – through implementation of an Appendix II listing in 2004 – that all international trade in seahorses must be monitored and managed for sustainability.     

ABUNDANCE OF BLUE AND HUMPBACK WHALES IN THE EASTERN NORTH PACIFIC ESTIMATED BY CAPTURE-RECAPTURE AND LINE-TRANSECT METHODS

We estimated humpback and blue whale abundance from 1991 to 1997 off the west coast of the U. S. and Mexico comparing capture-recapture models based on photographically identified animals and line-transect methods from ship-based surveys. During photo-identification research we obtained 4,212 identifications of 824 humpback whales and 2,403 identifications of 908 blue whales primarily through non-systematic small-boat surveys along the coast of California, Oregon, and Washington. Line-transect surveys from NOAA ships in 1991, 1993, and 1996 covered approximately 39,000 km along the coast of Baja California, California, Oregon, and Washington out to 555 km from shore. The nearshore and clumped distribution of humpback whales allowed photographic identification from small boats to cost-effectively sample a substantial portion of the population, but made it difficult to obtain effective samples in the line-transect surveys covering broad areas. The humpback capture-recapture estimates indicated humpback whale abundance increased over the six years (from 569 to 837). The broader more offshore distribution of blue whales made it harder to obtain a representative sample of identification photographs, but was well suited to the line-transect estimates. The line-transect estimates, after correction for missed animals, indicated approximately 3,000 blue whales (CV = 0.14). Capture-recapture estimates of blue whales were lower than this: approximately 2,000 when using photographs obtained from the line-transect surveys as one of the samples. Comparison of the results from the two methods provides validation, as well as insight into potential biases associated with each method.     

Trends in bowhead whales in West Greenland: Aerial surveys vs. genetic capture‐recapture analyses

We contrast two methods for estimating the trends of bowhead whales (Balaena mysticetus) in West Greenland: (1) double platform visual aerial survey, corrected for missed sightings and the time the whales are available at the surface; and (2) a genetic capture‐recapture approach based on a 14‐yr‐long biopsy sampling program in Disko Bay. The aerial survey covered 39,000 km² and resulted in 58 sightings, yielding an abundance estimate of 744 whales (CV = 0.34, 95% CI: 357–1,461). The genetic method relied on determining sex, mitochondrial haplotypes and genotypes of nine microsatellite markers. Based on samples from a total of 427 individuals, with 11 recaptures from previous years in 2013, this resulted in an estimate of 1,538 whales (CV = 0.24, 95% CI: 827–2,249). While the aerial survey is considered a snapshot of the local spring aggregation in Disko Bay, the genetic approach estimates the abundance of the source of this aggregation. As the whales in Disko Bay primarily are adult females that do not visit the bay annually, the genetic method would presumably yield higher estimates. The studies indicate that an increase in abundance observed between 1998 and 2006 has leveled off.     

Multi‐methods approach to characterizing the magnitude,impact, and spatial risk of Irrawaddy dolphin (Orcaella brevirostris) bycatch in small‐scale fisheries in Malampaya Sound,Philippines

Addressing the urgent conservation threat of marine mammal bycatch in small‐scale fisheries requires information on bycatch magnitude, gear types, population impacts, and risk. However, data on these proximate attributes are widely lacking in developing countries. This study used a multi‐methods approach integrating boat surveys and interviews with fishermen (n = 526) to assess proximate attributes of bycatch for the Critically Endangered subpopulation of Irrawaddy dolphins (Orcaella brevirostris) in Malampaya Sound, Philippines. Given an updated population estimate of 35 individuals (CV = 22.9%), the estimated rate of bycatch fatalities exceeds the potential biological removal rate. Spatial overlap scores were calculated to characterize overlap between dolphins and fisheries as a proxy of bycatch risk. These scores identified particularly high risk areas that could be prioritized for gear bans. However, completely reducing bycatch risk would require more widespread bans beyond these high risk areas. Implementing gear restrictions will be immensely challenging, given serious obstacles to fisheries management at this site. The multi‐methods approach describes the urgency of the bycatch problem and the changes required for mitigation, setting the stage for identifying and evaluating potential solutions. It can be readily applied to developing country sites to guide more efficient and complete data collection and conservation efforts.     

Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models

Over‐exploitation of top predators and fish stocks has altered ecosystems towards less productive systems with fewer trophic levels. In the Celtic Sea (CS), discards and bycatch levels have prompted concern about some fisheries, while fin and humpback whales are recovering from centuries of over‐exploitation. A lack of empirical evidence on the preferred diet of some predators such as whales in the CS has hindered the implementation of effective conservation measures using an ecosystem‐based approach to fisheries management. Using a Bayesian framework (SIAR), stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope mixing models were used to assign proportionate diet solutions to fin and humpback whales (skin biopsies) and putative prey items: herring (Clupea harengus), sprat (Sprattus sprattus), and krill (Meganyctiphanes norvegica and Nyctiphanes couchii) in the CS. Krill was the single most important prey item in the diet of fin whales, but one of the least important for humpback whales (albeit based on a small sample of humpback whale samples). Age 0 sprat and herring comprised a large proportion of the diet of both species, followed by older sprat (age 1–2) and older herring (age 2–4). An ecosystem based approach to fisheries management will be required in the CS if we seek effective conservation of both fin and humpback whales, and sustainable fisheries.     

Estimation of minke whale abundance from an acoustic line transect survey of the Mariana Islands

The minke whale is one of the most abundant species of baleen whales worldwide, yet is rarely sighted in subtropical waters. In the North Pacific, they produce a distinctive sound known as the “boing,” which can be used to acoustically localize individuals. A vessel‐based survey using both visual and passive acoustic monitoring was conducted during the spring of 2007 in a large (616,000 km²) study area encompassing the Mariana Islands. We applied line transect methods to data collected from a towed hydrophone array to estimate the abundance of calling minke whales in our study area. No minke whales were sighted, but there were hundreds of acoustic detections of boings. Computer algorithms were developed to localize calling minke whales from acoustic recordings, resulting in over 30 independent localizations, a six‐fold increase over those estimated during the survey. The two best estimates of abundance of calling minke whales were determined to be 80 and 91 animals (0.13 and 0.15 animals per 1,000 km2, respectively; CV = 34%). These are the first density and abundance estimates for calling minke whales using towed hydrophone array surveys, and the first estimates for this species in the Mariana Islands region. These are considered minimum estimates of the true number of minke whales in the study area.     

Molecular genetic identification of whale and dolphin products from commercial markets in Korea and Japan

We report the methods and results of molecular genetic identification of the species and, in some cases, geographical origins of whale and dolphin products purchased from retail markets and restaurants in Japan and South Korea. As reported previously (Baker & Palumbi 1994), we used the polymerase chain reaction (PCR) and a portable laboratory to amplify, purify and later sequence a portion of the mitochondrial DNA control region from 16 commercial products purchased in Japan. This ‘spot check’ revealed a surprising variety of species for sale, including minke, fin and humpback whales and one or two species of dolphins sold as ‘kujira’ or whale. In the Korean survey, DNA amplifications were conducted by two of us (C.S.B. and F.C.) working with independent equipment and reagents. The two sets of DNA amplifications were returned to our respective laboratories and sequenced independently for cross-validation. Among the total of 17 species-specific sequences we found a dolphin, a beaked whale, 13 Northern Hemisphere minke whales (representing at least seven distinct individuals) and two whales which are closely related to the recognized sei and Bryde's whales but could not be identified as either using available type sequences. We suggest that these two specimens represent a currently unrecognized species or subspecies of Bryde's whale, possibly the so-called ‘small-form’ reported from the tropical waters of the Indo-Pacific. We conclude that molecular systematic analyses of DNA sequences have tremendous utility for the identification of whale and dolphin products. However, there are certain constraints on the application of these techniques for monitoring whaling or trade in whale products. First, PCR and DNA sequencing can generate misleading artefacts. These can generally be recognized or eliminated through experimental controls. Second, phylogenetic reconstructions of DNA sequences can be misinterpreted if the database of type sequences is inadequate or the taxonomy of the group is incomplete. This constraint is, at present, a more serious obstacle to molecular monitoring of whaling. Our results highlight uncertainties about the taxonomic status of oceanic populations and morphological forms of two species (or species complexes) targeted by legal and illegal hunting, the minke and Bryde's whales. Despite these uncertainties, it is difficult to reconcile some of the species available in Japanese and Korean commercial markets with recent catch records made available to the International Whaling Commission. It is particularly disturbing that two specimens of an unrecognized species or subspecies of baleen whale were for sale in a restaurant in South Korea in October, 1994, 8 years after the acceptance of an international moratorium on commercial whaling.     

PHOTOGRAPHIC IDENTIFICATION OF NORTHERN BOTTLENOSE WHALES (HYPEROODON AMPULLATUS): SOURCES OF HETEROGENEITY FROM NATURAL MARKS

The use of natural marks in capture-recapture studies can lead to unequal capture probabilities. This paper examined a catalog of northern bottlenose whale ( Hyperoodon ampullatus ) photographs from the Gully, Nova Scotia, to identify potential sources of heterogeneity. This information can be used to select appropriate individuals and photographs to include in analyses. Individual northern bottlenose whales were sufficiently marked to uniquely identify individuals (= 14.5 marks/individual; range 1-67), but not all mark types persisted over time. Reliable marks were defined as mark types that were not lost over the nine-yeat study period (notches, back indentation, and mottled patches). Individuals were considered reliably marked if they possessed at least one back indentation or mottled patch (located within one dorsal fin width, at the base of the dorsal fin) or a notch on the dorsal fin. Sixty-six percent (SE = 5%) of the population were reliably marked. Longterm analyses (months to years) should use only reliably marked individuals, and the results scaled to account for the rest of the population. Our results also showed that photographic quality affected an observer's ability to identify individuals. For this catalog, quantitative analysis indicated only photographs of Q ≥ 4 (on a 6-point scale with 6 representing the highest quality) should be included in mark-recapture analyses sensitive to heterogeneity.     

Elasmobranchs in southern Indonesian fisheries: the fisheries, the status of the stocks and management options

The biology of elasmobranchs makes them very vulnerable to fishing pressure and there is increasing international concern over their exploitation. In northern Australia the stocks of some species may be shared with those in southern Indonesia. Indonesia has the highest landings of elasmobranchs worldwide (>100,000 t p.a.) and millions of Indonesian artisanal fishers rely heavily on elasmobranchs taken in target fisheries. They are also taken by industrial trawlers and as bycatch in pelagic tuna fisheries. This paper, resulting from a collaborative project between Australia and Indonesia, summarises the elasmobranch fisheries; the characteristics of the fisheries are outlined, the status of the stocks are assessed, and management options described and discussed. The project focussed on representative markets and fish landing sites in southern Indonesia from 2001 to 2005. Data were from market surveys, the records of the Indonesian Directorate General of Capture Fisheries, and from research cruises. Data from the ongoing tuna monitoring programme showed that shark bycatch from the tuna fleets forms about 11% of shark landings in Indonesia. Yield per recruit and related analyses were used to integrate biological information to indicate the productivity of each species to allow for management policy options and constraints. Research cruise data show that catch rates of elasmobranchs in the Java Sea declined by at least one order of magnitude between 1976 and 1997. The results indicate strongly that many of the shark and ray species in Indonesia are overfished and that the most effective management strategy may need to involve capacity control, such as licencing, gear restrictions and catch limits, together with controls on the fin trade.     

Passive acoustic density estimation of sperm whales in the Tongue of the Ocean,Bahamas

Long‐term passive acoustic monitoring of marine mammals on navy ranges provides the opportunity to better understand the potential impact of sonar on populations. The navy range in Tongue of the Ocean (TOTO), Bahamas contains extensive hydrophone arrays, potentially allowing estimation of the density of deep diving, vocally active species such as the sperm whale (Physeter macrocephalus). Previous visual surveys in TOTO have been of limited spatio–temporal coverage and resulted in only sporadic sightings of sperm whales, whereas passive acoustic observations suggest the species is present year round. However, until now the means of acoustically determining the specific number of individuals in each cluster has been limited. We used recently developed algorithms to identify the number of echolocating whales present during a 42 d study period. We screened a 297 h acoustic data set to determine the proportion of time animals were present; fifty 10 min samples during presence were analyzed to estimate the number of individuals vocalizing during each sample. These counts were combined with an independent estimate of the proportion of 10 min periods when tagged animals vocalize. The estimated average density was 0.16 whales/1,000 km² (CV 27%; 95% CI 0.095–0.264). The method is potentially applicable to other areas containing dense hydrophone arrays.     

A preliminary survey of whale shark Rhincodon typus catch and trade in China: an emerging crisis

This study gives an account of spatial and temporal distribution of whale shark Rhincodon typus catch events in China on the basis of historical records and information obtained from interviews with fishing industry stakeholders. A total of 186 R. typus were recorded with key harvest areas identified as in Hainan and Zhejiang, and the peak catching seasons were May to June and September to October. Aspects of the R. typus trade are discussed, including products, markets and the process. The results suggest that R. typus is increasingly becoming a targeted resource in China as a consequence of fierce competition for large shark fins and an emerging local market for consumption of all body parts. Current obstacles and potential measures for sustainable exploitation and trade of R. typus are discussed.     

ESTIMATION OF AGE-SPECIFIC PROBABILITIES OF FIRST RETURN AND ANNUAL SURVIVAL RATES FOR THE MALE GRAY SEAL (HALICHOERUS GRYPUS) ON SABLE ISLAND FROM CAPTURE-RECAPTURE DATA

We used a longitudinal capture-recapture study to estimate the age-specific probabilities of first return to the breeding colony and annual survival rates for male gray seals ( Halichoerus grypus ), based on resightings of seals branded as young on Sable Island. We estimated that the average age of first returns for seals born in 1969–1970 to be 9.1 (SE 0.4) yr; for seals born in 1973–1974 it is estimated to be 9.8 (SE 0.2) yr. The estimated annual survival rate of these males was estimated to be 0.976 (SE 0.003).     

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.