Estimating the number of whales entering trade using DNA profiling and capture-recapture analysis of market products

Surveys of commercial markets combined with molecular taxonomy (i.e. molecular monitoring) provide a means to detect products from illegal, unregulated and/or unreported (IUU) exploitation, including the sale of fisheries bycatch and wild meat (bushmeat). Capture-recapture analyses of market products using DNA profiling have the potential to estimate the total number of individuals entering the market. However, these analyses are not directly analogous to those of living individuals because a ‘market individual’ does not die suddenly but, instead, remains available for a time in decreasing quantities, rather like the exponential decay of a radioactive isotope. Here we use mitochondrial DNA (mtDNA) sequences and microsatellite genotypes to individually identify products from North Pacific minke whales (Balaenoptera acutorostrata ssp.) purchased in 12 surveys of markets in the Republic of (South) Korea from 1999 to 2003. By applying a novel capture-recapture model with a decay rate parameter to the 205 unique DNA profiles found among 289 products, we estimated that the total number of whales entering trade across the five-year survey period was 827 (SE, 164; CV, 0.20) and that the average ‘half-life’ of products from an individual whale on the market was 1.82 months (SE, 0.24; CV, 0.13). Our estimate of whales in trade (reflecting the true numbers killed) was significantly greater than the officially reported bycatch of 458 whales for this period. This unregulated exploitation has serious implications for the survival of this genetically distinct coastal population. Although our capture-recapture model was developed for specific application to the Korean whale-meat markets, the exponential decay function could be modified to improve the estimates of trade in other wildmeat or fisheries markets or abundance of living populations by noninvasive genotyping.

(Table 2) Concentrations of polychlorinated naphthalene congeners in blubber samples from whales, seals and porpoises between 1986-2009

A selection of PCN congeners was analyzed in pooled blubber samples of pilot whale (Globicephala melas), ringed seal (Phoca hispida), minke whale (Balaenoptera acutorostrata), fin whale (Balaenoptera physalus), harbour porpoise (Phocoena phocoena), hooded seal (Cystophora cristata) and Atlantic whitesided dolphin (Lagenorhynchus acutus), covering a time period of more than 20 years (1986-2009). A large geographical area of the North Atlantic and Arctic areas was covered. PCN congeners 48, 52, 53, 66 and 69 were found in the blubber samples between 0.03 and 5.9 ng/g lw. Also PCBs were analyzed in minke whales and fin whales from Iceland and the total PCN content accounted for 0.2% or less of the total non-planar PCB content. No statistically significant trend in contaminant levels could be established for the studied areas. However, in all species except minke whales caught off Norway the lowest Sum PCN concentrations were found in samples from the latest sampling period.

Estimates of Marine Mammal, Sea Turtle, and Seabird Mortality in the California Drift Gillnet Fishery for Swordfish and Thresher Shark, 1996–2002

Estimates of incidental marine mammal, sea turtle, and seabird mortality in the California drift gillnet fishery for broadbill swordfish, Xiphias gladius, and common thresher shark, Alopias vulpinus, are summarized for the 7-year period, 1996 to 2002. Fishery observer coverage was 19% over the period (3,369 days observed/17,649 days fished). An experiment to test the effectiveness of acoustic pingers on reducing marine mammal entanglements in this fishery began in 1996 and resulted in statistically significant reductions in marine mammal bycatch. The most commonly entangled marine mammal species were the short-beaked common dolphin, Delphinus delphis; California sea lion, Zalophus californianus; and northern right whale dolphin, Lissodelphis borealis. Estimated mortality by species (CV and observed mortality in parentheses) from 1996 to 2002 is 861 (0.11, 133) short-beaked common dolphins; 553 (0.16, 103) California sea lions; 151 (0.25, 31) northern right whale dolphins; 150 (0.21, 27) northern elephant seals, Mirounga angustirostris; 54 (0.41, 10) long-beaked common dolphins, Delphinus capensis; 44 (0.53, 6) Dall’s porpoise, Phocoenoides dalli; 19 (0.60, 5) Risso’s dolphins, Grampus griseus; 11 (0.71, 2) gray whales, Eschrichtius robustus; 7 (0.83, 2) sperm whales, Physeter macrocephalus; 7 (0.96, 1) short-finned pilot whales, Globicephala macrorhychus; 12 (1.06, 1) minke whales, Balaenoptera acutorostrata; 5 (1.05, 1) fin whales, Balaenoptera physalus; 11 (0.68, 2) unidentified pinnipeds; 33 (0.52, 4) leatherback turtles, Dermochelys coriacea; 18 (0.57, 3) loggerhead turtles, Caretta caretta; 13 (0.73, 3) northern fulmars, Fulmarus glacialis; and 6 (0.86, 2) unidentified birds.

Whale distribution in relation to prey abundance and oceanographic processes in the shelf waters of the Western Antarctic Peninsula

The Western Antarctic Peninsula (WAP) is a biologically rich area supporting large standing stocks of krill and top predators (including whales, seals and seabirds). Physical forcing greatly affects productivity, recruitment, survival and distribution of krill in this area. In turn, such interactions are likely to affect the distribution of baleen whales. The Southern Ocean GLOBEC research program aims to explore the relationships and interactions between the environment, krill and predators around Marguerite Bay (WAP) in autumn 2001 and 2002. Bathymetric and environmental variables including acoustic backscattering as an indicator of prey abundance were used to model whale distribution patterns. We used an iterative approach employing (1) classification and regression tree (CART) models to identify oceanographic and ecological variables contributing to variability in humpback Megaptera novaeangliae and minke Balaenoptera acutorstrata whale distribution, and (2) generalized additive models (GAMs) to elucidate functional ecological relationships between these variables and whale distribution. The CART models indicated that the cetacean distribution was tightly coupled with zooplankton acoustic volume backscatter in the upper (25 to 100 m), and middle (100 to 300 m) portions of the water column. Whale distribution was also related to distance from the ice edge and bathymetric slope. The GAMs indicated a persistent, strong, positive relationship between increasing zooplankton volume and whale relative abundance. Furthermore, there was a lower limit for averaged acoustic volume backscatter of zooplankton below which the relationship between whales and prey was not significant. The GAMs also supported an annual relationship between whale distribution, distance from the ice edge and bathymetric slope, suggesting that these are important features for aggregating prey. Our results demonstrate that during the 2 yr study, whales were consistently and predictably associated with the distribution of zooplankton. Thus, humpback and minke whales may be able to locate physical features and oceanographic processes that enhance prey aggregation.

Inferring activity budgets in wild animals to estimate the consequences of disturbances

Activity budgets can provide a direct link to an animal's bioenergetic budget and is thus a valuable unit of measure when assessing human-induced nonlethal effects on wildlife conservation status. However, activity budget inference can be challenging for species that are difficult to observe and require multiple observational variables. Here, we assessed whether whalewatching boat interactions could affect the activity budgets of minke whales (Balaenoptera acutorostrata). We used a stepwise modeling approach to quantitatively record, identify, and assign activity states to continuous behavioral time series data, to estimate activity budgets. First, we used multiple behavioral variables, recorded from continuous visual observations of individual animals, to quantitatively identify and define behavioral types. Activity states were then assigned to each sampling unit, using a combination of hidden and observed states. Three activity states were identified: nonfeeding, foraging, and surface feeding (SF). From the resulting time series of activity states, transition probability matrices were estimated using first-order Markov chains. We then simulated time series of activity states, using Monte Carlo methods based on the transition probability matrices, to obtain activity budgets, accounting for heterogeneity in state duration. Whalewatching interactions reduced the time whales spend foraging and SF, potentially resulting in an overall decrease in energy intake of 42%. This modeling approach thus provides a means to link short-term behavioral changes resulting from human disturbance to potential long-term bioenergetic consequences in animals. It also provides an analytical framework applicable to other species when direct observations of activity states are not possible.

Estimating cumulative exposure of wildlife to non-lethal disturbance using spatially explicit capture-recapture models

Impact assessments often focus on short-term behavioral responses of animals to human disturbance. However, the cumulative effects caused by repeated behavioral disruptions are of management concern because these effects have the potential to influence individuals' survival and reproduction. We need to estimate individual exposure rates to disturbance to determine cumulative effects. We present a new approach to estimate the spatial exposure of minke whales to whalewatching boats in Faxaflõi Bay, Iceland. We used recent advances in spatially explicit capture-recapture modeling to estimate the probability that whales would encounter a disturbance (i.e., whalewatching boat). We obtained spatially explicit individual encounter histories of individually identifiable animals using photo-identification. We divided the study area into 1-km2 grid cells and considered each cell a spatially distinct sampling unit. We used capture history of individuals to model and estimate spatial encounter probabilities of individual minke whales across the study area, accounting for heterogeneity in sampling effort. We inferred the exposure of individual minke whales to whalewatching vessels throughout the feeding season by estimating individual whale encounters with vessels using the whale encounter probabilities and spatially explicit whalewatching intensity in the same area, obtained from recorded whalewatching vessel tracks. We then estimated the cumulative time whales spent with whalewatching boats to assess the biological significance of whalewatching disturbances. The estimated exposure levels to boats varied considerably between individuals because of both temporal and spatial variations in the activity centers of whales and the whalewatching intensity in the area. However, although some whales were repeatedly exposed to whalewatching boats throughout the feeding season, the estimated cumulative time they spent with boats was very low. Although whalewatching boat interactions caused feeding disruptions for the whales, the estimated low cumulative exposure indicated that the whalewatching industry in its current state likely is not having any long-term negative effects on vital rates.

Japan’s whaling plan under scrutiny

Eighteen years after initiating scientific whaling in Antarctic waters, Japan presented a new and more ambitious program to the International Whaling Commission (IWC); the proposal was made in early June during the IWC’s annual meeting in Ulsan, Korea. Japan now wishes to more than double its annual catch of Antarctic minke whales (from about 440 to 935), and to expand lethal sampling to include an additional yearly take of 50 humpback and 50 fin whales. Unlike catches for commercial whaling, scientific catches are unregulated. Since 1987, Japan has taken some 6,800 minke whales from Antarctic waters, despite ongoing criticism of the relevance and direction of Japan’s research. The IWC was set up to regulate commercial whaling and to conserve whale populations, under the authority of the 1946 International Convention for the Regulation of Whaling. Following a well-documented failure of management that led to the collapse of most global whale populations, the IWC set a zero quota for commercial whaling (the moratorium). This was made effective from 1986. Norway, the former Soviet Union and Japan initially objected to the moratorium, but Japan withdrew its objection and ceased commercial whaling in 1988.

Species abundance and water and sediment characteristics for three ANDEEP stations on Maud Rise and the Weddell Sea

The benthic fauna was investigated during the expedition ANT-XXIV/2 (2007/08) in relation to oceanographic features, biogeochemical properties and sediment characteristics, as well as the benthic, pelagic and air-breathing fauna. The results document that Maud Rise (MR) differs distinctly from surrounding deep-sea basins investigated during previous Southern Ocean expeditions (ANDEEP 2002, 2005). Considering all taxa, the overall similarity between MR and adjacent stations was low (~20% Bray-Curtis-Similarity), and analyses of single taxa show obvious differences in species composition, abundances and densities. The composition and diversity of bivalves of MR are characterised by extremely high abundances of three species, especially the small sized Vesicomya spp. Exceptionally high gastropod abundance at MR is due to the single species Onoba subantarctica wilkesiana, a small brooder that may prey upon abundant benthic foraminiferas. The abundance and diversity of isopods also show that one family, Haplomunnidae, occurs with a surprisingly high number of individuals at MR while this family was not found at any of the 40 bathyal and abyssal ANDEEP stations. Similarly, polychaetes, especially the tube-dwelling, suspension-feeder fraction, are represented by species not found at the comparison stations. Sponges comprise almost exclusively small specimens in relatively high numbers, especially a few species of Polymastiidae. Water-column sampling from the surface to the seafloor, including observations of top predators, indicate the existence of a prospering pelagic food web. Local concentrations of top predators and zooplankton are associated with a rich ice-edge bloom located over the northern slope of MR. There the sea ice melts, which is probably accelerated by the advection of warm water at intermediate depth. Over the southern slope, high concentrations of Antarctic krill (Euphausia superba) occur under dense sea ice and attract Antarctic Minke Whales (Balaenoptera bonaerensis) and several seabird species. These findings suggest that biological prosperity over MR is related to both oceanographic and sea-ice processes. Downward transport of the organic matter produced in the pelagic realm may be more constant than elsewhere due to low lateral drift over MR.

Physical oceanography, sea-bed photographs and videos of benthos from the Weddell Sea taken with remote operated vehicle CHEROKEE during POLARSTERN cruise ANT-XXIII/8

The marine ecosystem on the eastern shelf of the Antarctic Peninsula was surveyed 5 and 12 years after the climate-induced collapse of the Larsen A and B ice shelves. An impoverished benthic fauna was discovered, that included deep-sea species presumed to be remnants from ice-covered conditions. The current structure of various ecosystem components appears to result from extremely different response rates to the change from an oligotrophic sub-ice-shelf ecosystem to a productive shelf ecosystem. Meiobenthic communities remained impoverished only inside the embayments. On local scales, macro- and mega-epibenthic diversity was generally low, with pioneer species and typical Antarctic megabenthic shelf species interspersed. Antarctic Minke whales and seals utilised the Larsen A/B area to feed on presumably newly established krill and pelagic fish biomass. Ecosystem impacts also extended well beyond the zone of ice-shelf collapse, with areas of high benthic disturbance resulting from scour by icebergs discharged from the Larsen embayments.

Report on Marine Mammal Unusual Mortality Event UMESE0501Sp: Multispecies Mass Stranding of Pilot Whales (Globicephala macrorhynchus), Minke Whale (Balaenoptera acutorostrata), and Dwarf Sperm Whales (Kogia sima) in North Carolina on 15-16 January 2005

On 15-16 January 2005, three offshore species of cetaceans (33 short-finned pilot whales, Globicephala macrorhynchus, one minke whale, Balaenoptera acutorostrata, and two dwarf sperm whales, Kogia sima) stranded alive on the beaches of North Carolina. The pilot whales stranded near Oregon Inlet, the minke whale in northern North Carolina, and the dwarf sperm whales near Cape Hatteras. Live strandings of three species in one weekend was unique in North Carolina and qualified as an Unusual Mortality Event. Gross necropsies were conducted on 16-17 January 2005 on 27 pilot whales, two dwarf sperm whales, and the minke whale. Samples were collected for clinical pathology, parasitology, gross pathology, histopathology, microbiology and serology. There was variation in the number of animals sampled for each collection type, however, due to carcasses washing off the beach or degradation in carcass condition during the course of the response. Comprehensive histologic examination was conducted on 16 pilot whales, both dwarf sperm whales, and the minke whale. Limited organ or only head tissue suites were obtained from nine pilot whales. Histologic examination of tissues began in February 2005 and concluded in December 2005 when final sampling was concluded. Neither the pilot whales nor dwarf sperm whales were emaciated although none had recently ingested prey in their stomachs. The minke whale was emaciated; it was likely a dependent calf that became separated from the female. Most serum biochemistry abnormalities appear to have resulted from the stranding and indicated deteriorating condition from being on land for an extended period. Three pilot whales had clinical evidence of pre-existing systemic inflammation, which was supported by histopathologic findings. Although gross and histologic lesions involving all organ systems were noted, consistent lesions were not observed across species. Verminous pterygoid sinusitis and healed fishery interactions were seen in pilot whales but neither of these changes were causes of debilitation or death. In three pilot whales and one dwarf sperm whale there was evidence of clinically significant disease in postcranial tissues which led to chronic debilitation. Cardiovascular disease was present in one pilot whale and one dwarf sperm whale; musculoskeletal disease and intra-abdominal granulomas were present in two pilot whales. These lesions were possible, but not definitive, causal factors in the stranding. Remaining lesions were incidental or post-stranding. The minke whale and three of five tested pilot whales had positive morbillivirus titers (≥1:8 with one at >1:256), but there was no histologic evidence of active viral infection. Parasites (nematodes, cestodes, and trematodes) were collected from 26 pilot whales and two dwarf sperm whales. Sites of collection included stomach, nasal/pterygoid, peribullar sinuses, blubber, and abdominal cavity. Parasite species, locations and loads were within normal limits for free-ranging cetaceans and were not considered causative for the stranding event. Gas emboli lesions which were considered consistent with or diagnostic of sonarassociated strandings of beaked whales or small cetaceans were not found in the whales stranded as part of UMESE0501Sp. Twenty-five heads were examined with nine specific anatomic locations of interest: extramandibular fat, intramandibular fat, auditory meatus, peribullar acoustic fat, peribullar soft tissue, peribullar sinus, pterygoid sinus, melon, and brain. The common finding in all examined heads was verminous pterygoid sinusitis. Intramandibular adipose tissue reddening, typically adjacent to the vascular plexus, was observed in some individuals and could represent localized hemorrhage resulting from vascular rete rupture, hypostatic congestion, or erythrocyte rupture during the freeze/thaw cycle. One cetacean had peracute to acute subdural hemorrhage that likely occurred from thrashing on the beach post-stranding, although its occurrence prior to stranding cannot be excluded. Information provided to NMFS by the U.S. Navy indicated routine tactical mid-frequency sonar operations from individual surface vessels over relatively short durations and small spatial scales within the area and time period investigated. No marine mammals were detected by marine mammal observers on operational vessels; standard operating procedure for surface naval vessels operating mid-frequency sonar is the use of trained visual lookouts using high-powered binoculars. Sound propagation modeling using information provided to NMFS indicated that acoustic conditions in the vicinity likely depended heavily on position of the receivers (e.g., range, bearing, depth) relative to that of the sources. Absent explicit information on the location of animals meant that it was not possible to estimate received acoustic exposures from active sonar transmissions. Nonetheless, the event was associated in time and space with naval activity using mid-frequency active sonar. It also had a number of features in common (e.g., the “atypical” distribution of strandings involving multiple offshore species, all stranding alive, and without evidence of common infectious or other disease process) with other sonar-related cetacean mass stranding events. Given that this event was the only stranding of offshore species to occur within a 2-3 day period in the region on record (i.e., a very rare event), and given the occurrence of the event simultaneously in time and space with a naval exercise using active sonar, the association between the naval sonar activity and the location and timing of the event could be a causal rather than a coincidental relationship. However, evidence supporting a definitive association is lacking, and, in particular, there are differences in operational/environmental characteristics between this event and previous events where sonar has apparently played a role in marine mammal strandings. This does not preclude behavorial avoidance of noise exposure. No harmful algal blooms were present along the Atlantic coast south of the Chesapeake Bay during the months prior to the event. Environmental conditions, including strong winds, changes in upwelling- to downwelling-favorable conditions, and gently sloping bathymetry, were consistent with conditions which have been correlated with other mass strandings. In summary, we did not find commonality in gross and histologic lesions that would indicate a single cause for this stranding event. Three pilot whales and one dwarf sperm whale had debilitating conditions identified that could have contributed to stranding, one pilot whale had a debilitating condition (subdural hemorrhage) that could have been present prior to or resulting from stranding. While the pilot and dwarf sperm whale strandings may have had a common cause, the minke whale stranding was probably just coincidental. On the basis of examination of physical evidence in the affected whales, however, we cannot definitively conclude that there was or was not a causal link between anthropogenic sonar activity or environmental conditions (or a combination of these factors) and the strandings. Overall, the cause of UMESE0501Sp in North Carolina is not and likely will not be definitively known. (PDF contains 240 pages)

Forty Years of Winter: Cetaceans Observed During the Southbound Migration of Gray Whales, Eschrichtius robustus, Near Granite Canyon, Central California

From December to February in most years from 1967 to 2007, observers counted gray whales, Eschrichtius robustus, from shore sites south of Carmel in central California. In addition to gray whales, other cetacean species were also recorded. These observations were summarized and compared among survey platforms and to ocean conditions. Eleven cetacean species were identified including eight odontocete species (killer whale, Orcinus orca; Pacific white-sided dolphin, Lagenorhynchus obliquidens; common dolphin, Delphinus spp.; bottlenose dolphin, Tursiops truncatus, northern right whale dolphin, Lissodelphis borealis; Risso’s dolphin, Grampus griseus; Dall’s porpoise, Phocoenoides dalli; and harbor porpoise, Phocoena phocoena) and three mysticete species (humpback whale, Megaptera novaeangliae; minke whale, Balaenoptera acutorostrata; and blue whale, Balaenoptera musculus). As expected, the detection of certain species among survey platforms (shore-based census watches, 25-power “Big Eye” binocular watches, and aerial surveys) was limited by species surfacing behavior and/or bathymetric preference. Comparisons among the shore-based census efforts showed a significant difference in sightings rates from 1967–84 (n = 14, mean = 0.11, SD = 0.11) to 1985–2007 (n = 11, mean = 1.48, SD = 0.47; t-Test: p < 0.001, df = 23). The warm period observed during the 1990’s may partially explain the increase in sighting rates and diversity of species observed at the census site compared to the much cooler temperatures of the 1970’s.

(Table 3) Concentrations of polybrominated diphenyl ether and congeners in blubber samples from whales, seals and porpoises between 1986-2009

A selection of PBDE congeners was analyzed in pooled blubber samples of pilot whale (Globicephala melas), ringed seal (Phoca hispida), minke whale (Balaenoptera acutorostrata), fin whale (Balaenoptera physalus), harbor porpoise (Phocoena phocoena), hooded seal (Cystophora cristata) and Atlantic white-sided dolphin (Lagenorhynchus acutus), covering a time period of more than 20 years (1986-2009). The analytes were extracted and cleaned-up using open column extraction and multi-layer silica gel column chromatography, and the analysis was performed on a GC-MS system operating in the NCI mode. The highest PBDE levels were found in the toothed whale species pilot whale and white-sided dolphin, and the lowest levels in fin whales and ringed seals. One-sided analyses of variance (ANOVA) followed by Tukey comparisons of means were applied to test for differences between years and sampling areas. Due to inter-year sampling variability, only general comparisons of PBDE concentrations between different sampling areas could be made. Differences in PBDE concentrations between three sampling periods, from 1986 to 2007, were evaluated in samples of pilot whales, ringed seals, white-sided dolphins and hooded seals. The highest PBDE levels were found in samples from the late 1990s or beginning of 2000, possibly reflecting the increase in the global production of technical PBDE mixtures in the 1990s. The levels of BDE #153 and #154 increased relative to the total PBDE concentration in some of the species in recent years, which may indicate an increased relative exposure to higher brominated congeners. In order to assess the effect of measures taken in legally binding international agreements, it is important to continuously monitor POPs such as PBDEs in sub-Arctic and Arctic environments.

(Table 2) Polybrominated diphenyl ether concentration in blubber samples from whales, seals and porpoises between 1986-2009

A selection of MeO-BDE and BDE congeners were analyzed in pooled blubber samples of pilot whale (Globicephala melas), ringed seal (Phoca hispida), minke whale (Balaenoptera acutorostrata), fin whale (Balaenoptera physalus), harbor porpoise (Phocoena phocoena), hooded seal (Cystophora cristata), and Atlantic white-sided dolphin (Lagenorhynchus acutus), covering a time period of more than 20 years (1986-2009). The analytes were extracted and cleaned-up using open column extraction and multi-layer silica gel column chromatography. The analysis was performed using both low resolution and high resolution GC-MS. MeO-PBDE concentrations relative to total PBDE concentrations varied greatly between sampling periods and species. The highest MeO-PBDE levels were found in the toothed whale species pilot whale and white-sided dolphin, often exceeding the concentration of the most abundant PBDE, BDE-47. The lowest MeO-PBDE levels were found in fin whales and ringed seals. The main MeO-BDE congeners were 6-MeO-BDE47 and 2'-MeO-BDE68. A weak correlation only between BDE47 and its methoxylated analog 6-MeO-BDE47 was found and is indicative of a natural source for MeO-PBDEs.

Cytochrome p450 isozyme protein verified in the skin of southern hemisphere humpback whales (megaptera novaeangliae) : implications for biochemical biomarker assessment

Large mysticete whales represent a unique challenge for chemical risk assessment. Few epidemiological investigations are possible due to the low incidence of adult stranding events. Similarly their often extreme life-history adaptations of prolonged migration and fasting challenge exposure assumptions. Molecular biomarkers offer the potential to complement information yielded through tissue chemical analysis, as well as providing evidence of a molecular response to chemical exposure. In this study we confirm the presence of cytochrome P450 reductase (CPR) and cytochrome P450 isoenzyme 1A1 (CYP1A1) in epidermal tissue of southern hemisphere humpback whales (Megaptera novaeangliae). The detection of CYP1A1 in the integument of the humpback whale affords the opportunity for further quantitative non-destructive investigations of enzyme activity as a function of chemical stress.