Interspecific Introgression in Cetaceans: DNA Markers Reveal Post-F1 Status of a Pilot Whale

Visual species identification of cetacean strandings is difficult, especially when dead specimens are degraded and/or species are morphologically similar. The two recognised pilot whale species (Globicephala melas and Globicephala macrorhynchus) are sympatric in the North Atlantic Ocean. These species are very similar in external appearance and their morphometric characteristics partially overlap; thus visual identification is not always reliable. Genetic species identification ensures correct identification of specimens. Here we have employed one mitochondrial (D-Loop region) and eight nuclear loci (microsatellites) as genetic markers to identify six stranded pilot whales found in Galicia (Northwest Spain), one of them of ambiguous phenotype. DNA analyses yielded positive amplification of all loci and enabled species identification. Nuclear microsatellite DNA genotypes revealed mixed ancestry for one individual, identified as a post-F1 interspecific hybrid employing two different Bayesian methods. From the mitochondrial sequence the maternal species was Globicephala melas. This is the first hybrid documented between Globicephala melas and G. macrorhynchus, and the first post-F1 hybrid genetically identified between cetaceans, revealing interspecific genetic introgression in marine mammals. We propose to add nuclear loci to genetic databases for cetacean species identification in order to detect hybrid individuals.     

A simple photograph‐based approach for discriminating between free‐ranging long‐finned (Globicephala melas) and short‐finned (G. macrorhynchus) pilot whales off the east coast of the United States

Line transect based abundance estimation is complicated for long‐finned (LFPW, Globicephala melas) and short‐finned (SFPW, G. macrorhynchus) pilot whales because of their similarity in appearance and their overlapping summertime range in some areas. We developed a photograph‐based approach to distinguish between species of free‐ranging pilot whales in the northwest Atlantic. We collected skin samples and photographs during the summers of 2004–2007 and used skin samples to distinguish species based on mitochondrial DNA. Relative morphometric measurements from photographs were examined using mixed‐effect models and logistic regression. The best model among 94 candidate models had an overall classification error rate of 2.5%. We tested the presence/absence of pigmentation in four regions of the dorsal body (melon, eye, cape, and saddle) for differences. Pigmentation was present in all four regions in 100% of the SFPWs sampled. Melon patch, blaze, and saddle patch pigmentation were present in 6%, 68%, and 50%, respectively, of the LFPWs, but the cape was completely absent. Both types of analyses provided positive species discrimination of free‐ranging animals. We created a cost‐effective, simple tool which could ultimately assist in providing appropriate management, mitigation, and conservation strategies for both northwest Atlantic species of pilot whales.     

Stomach contents of mass-stranded short-finned pilot whales (Globicephala macrorhynchus) from North Carolina

We examined the stomach contents of 27 short‐finned pilot whales (Globicephala macrorhynchus) that mass stranded on the North Carolina coast on 15 January 2005. Eleven whales had prey parts in their forestomachs. We used frequency of occurrence and numerical abundance to assess the relative importance of prey. Brachioteuthis riisei (numerical abundance 28%), an oceanic species, was the most important cephalopod prey, but Taonius pavo (12%) and Histioteuthis reversa (9%) also represented a substantial part of the diet. A large number of otoliths belonging to the fish Scopelogadus beanii were present (25%). These results differ from reports of the stomach contents of short‐finned pilot whales from the Pacific coast in which neritic species dominate the diet. Our findings also suggest that there is a considerable difference between the diet of short‐ and long‐finned pilot whales (Globicephala melas) in the western North Atlantic. The latter feed predominantly on the long‐finned squid (Loligo pealei) whereas the former feed on deep‐water species. Our results indicate the whales fed primarily off the continental shelf prior to stranding.     

Morbillivirus ecology in polar bears (Ursus maritimus)

Polar bear (Ursus maritimus) morbillivirus infection was initially reported by Follmann and co-workers in 1996, based upon serologic results using canine distemper virus (CDV). The impetus for the evaluation of polar bear populations for morbillivirus infections was prompted by epidemics of canine distemper-like disease in seal populations in the north Atlantic regions of Greenland, Europe, and Russia. Since marine morbilliviruses have been further characterized into three major species, phocine distemper virus (PDV), dolphin morbillivirus (DMV) and porpoise morbillivirus (PMV), it was of value to determine the origin of the polar bear infection. One hundred serum samples were selected from a group of sera collected from regions of Alaska and Russia and tested by differential serum neutralization assay against the three major marine morbilliviruses and CDV, to determine the predominant virus infecting the polar bear. Polar bears had higher serum antibody titers to CDV than they did to PDV, DMV, and PMV. These data suggest that polar bears are being infected with a morbillivirus of terrestrial origin. Furthermore, based on the high serum antibody prevalence in the population, the virus may be indigenous to the polar bear and not necessarily the result of interspecies transmission from other arctic mammals susceptible to CDV and/or marine morbilliviruses. Accepted: 20 December 1999     

Patterns and trends in the diet of long‐finned pilot whales (Globicephala melas) in the northeast Atlantic

There is little previous information on feeding habits of long‐finned pilot whales (Globicephala melas) in the northeast Atlantic. The present study analyzed stomach contents of pilot whales stranded in Portugal (n = 6), Galicia (northwest Spain) (n = 32), and Scotland (United Kingdom) (n = 10), from 1990 to 2011. These animals ranged from 213 to 555 cm in length (24 females, 19 males and 5 of unknown sex). The main prey identified were cephalopods of the families Octopodidae and Ommastrephidae, the former being numerically more important in Iberia (Portugal and Galicia) and the latter more important in Scotland, with Iberian whales also showing a more diverse diet. Multivariate analysis revealed evidence of geographical and seasonal variation in diet. Generalized Additive Modeling results indicated that more octopus (Eledone cirrhosa) were eaten in Iberia than in Scotland, more in the first half of the year, and more in larger whales. Numbers of ommastrephid squids in the stomach decreased over the study period and varied with season and whale length. This study confirms cephalopods as the main prey of pilot whales, as previously reported, although our results also suggest that, in the northeast Atlantic, ommastrephid squid are largely replaced as the main prey by octopods at lower latitudes.     

MORBILLIVIRUS INFECTION IN BOTTLENOSE DOLPHINS: EVIDENCE FOR RECURRENT EPIZOOTICS IN THE WESTERN ATLANTIC AND GULF OF MEXICO

Morbillivirus infection is widespread among odontocetes of the western Atlantic and Gulf of Mexico. Serologic evidence of infection in bottlenose dolphins, Tursiops truncatus , was first detected during an epizootic along the mid-Atlantic coast in 1987. Here, we report recurrent epizootics in the coastal dolphin population since at least the early 1980s based on serological surveys and regional stranding frequencies. The first observed epizootic of this series occurred in the Indian and Banana Rivers in 1982 and was followed by others on the mid-Atlantic coast in 1987–1988 and in the Gulf of Mexico between 1992 and 1994. This temporal pattern of infection is likely facilitated by the population size and its fragmentation into relatively discrete coastal communities. Introduction of morbillivirus into a community with a sufficient number of naive hosts may precipitate an epizootic, depending on the potential for transmission within the group. Propagation of an epizootic along the coast is probably determined by frequency of contact between adjacent communities and seasonal migrations.
Morbillivirus antibodies were also detected in serum from offshore bottlenose dolphins. The sero-prevalence in the latter may be higher than in coastal dolphins because of their close association with enzootically infected pilot whales ( Globicephala spp.). Occasional contact between offshore and coastal dolphins may provide an epizootiologic link between pilot whales and coastal dolphin communities.     

Notes on New Zealand mammals 6. Second report on the stomach contents of long‐finned pilot whales,Globicephala melas

Abstract

We report data on the stomach contents of the long‐finned pilot whale, Globicephala melas, recovered from a group of whales stranded on Ruakaka Beach, northeastern New Zealand, in November 2006. In nine whales for which identifiable stomach contents were recovered (three that stranded on 10 November and six that stranded on 11 November) prey remains comprised exclusively cephalopod beaks attributed to five squid species. The stomachs of a further two whales contained unidentifiable upper beaks only, while the stomachs of five whales were completely empty. No whale appeared to have been satiated immediately before stranding, given that the maximum biomass of prey recently consumed by any one whale was calculated to be <5 kg. All squids ingested represented oceanic species, found from 50 to 1000 m but more common towards the deeper end of this range. These data both complement and contrast with the only other dietary information available for this species in New Zealand waters, reported from stomach contents of whales stranded on Farewell Spit, South Island in December 2005.     

Delphinid whistle production and call matching during playback of simulated military sonar

In 2007 and 2008, controlled exposure experiments were performed in the Bahamas to study behavioral responses to simulated mid‐frequency active sonar (MFA) by three groups of odontocetes: false killer whales, Pseudorca crassidens; short‐finned pilot whales, Globicephala macrorhynchus; and melon‐headed whales, Peponocephala electra. An individual in each group was tagged with a Dtag to record acoustic and movement data. During exposures, some individuals produced whistles that seemed similar to the experimental MFA stimulus. Statistical tests were thus applied to investigate whistle‐MFA similarity and the relationship between whistle production rate and MFA reception time. For the false killer whale group, overall whistle rate and production rate of the most MFA‐like whistles decreased with time since last MFA reception. Despite quite low whistle rates overall by the melon‐headed whales, statistical results indicated minor transient silencing after each signal reception. There were no apparent relationships between pilot whale whistle rates and MFA sounds within the exposure period. This variability of responses suggests that changes in whistle production in response to acoustic stimuli depend not only on species and sound source, but also on the social, behavioral, or environmental contexts of exposure.     

PHYSICAL HABITAT OF CETACEANS ALONG THE CONTINENTAL SLOPE IN THE NORTHCENTRAL AND WESTERN GULF OF MEXICO

The physical habitat of cetaceans found along the continental slope in the north-central and western Gulf of Mexico was characterized from shipboard sighting data, simultaneous hydrographic measurements, and satellite remote sensing. The study area was encompassed by the longitude of the Florida-Alabama border (87.5°W), the southernmost latitude of the Texas-Mexico border (26.0°N), and the 100-m and 2,000-m isobaths. Shipboard surveys were conducted seasonally for two years from April 1992 to May 1994. A total of 21,350 km of transect was visually sampled in an area of 154,621 km². Sighting localities of species in the study area were differentiated most clearly with bottom depth. Atlantic spotted dolphins (Stenella frontalis) were consistently found in the shallowest water on the continental shelf and along the shelf break. In addition, the bottom depth gradient (sea floor slope) was less for Atlantic spotted dolphins than for any other species. Bottlenose dolphins (Tursiops truncatus) were found most commonly along the upper slope in water significantly deeper than that for Atlantic spotted dolphins. All the other species and species categories were found over deeper bottom depths; these were Risso's dolphins (Grampus griseus), short-finned pilot whales (Glob-icephala macrorhynchus), pygmy/dwarf sperm whales (Kogia spp.), roughtoothed dolphins (Steno bredanensis), spinner dolphins (Stenella longirostris), sperm whales (Physeter macrocephalus), striped dolphins (Stenella coeruleoalba), Mesoplodon spp., pantropical spotted dolphins (Stenella attenuata), Clymene dolphins (Stenella clymene) and unidentified beaked whales (Ziphiidae). Risso's dolphins and short-finned pilot whales occurred along the upper slope and, as a subgroup, were significantly different from striped dolphins, Mesoplodon spp., pantropical spotted dolphins, Clymene dolphins, and unidentified beaked whales, which occurred in the deepest water. Pygmy/dwarf sperm whales, rough-toothed dolphins, spinner dolphins, and sperm whales occurred at intermediate depths between these two subgroups and overlapped them.     

First report on the stomach contents of long‐finned pilot whales,Globicephala melas,stranded in New Zealand

Abstract

Stomach contents of the long‐finned pilot whale, Globicephala melas, are reported for the first time from New Zealand waters. Analyses based on two male and three female whales (2.5–5.3 m in length) that stranded on Farewell Spit, Golden Bay, South Island in December 2005 revealed a diet comprised exclusively of cephalopods (2-33 lower cephalopod beaks per stomach). Two genera of cephalopod from two orders; arrow squid, Nototodarus spp. (Teuthoidea: Ommastrephidae), and common octopus, Pinnoctopus cordiformis (Octopoda: Octopodidae) were represented. A further five pilot whale stomachs were examined and found to be empty.     

Evidence of susceptibility to morbillivirus infection in cetaceans from the United States

Cetacean morbilliviruses (CeMV) are viruses that can cause mass mortalities among various odontocete species. In this study levels of “herd” immunity in cetaceans from the U.S. coast are described from the distribution and prevalence of antibodies against morbilliviruses. Neutralizing antibody titers against dolphin morbillivirus (DMV), porpoise morbillivirus (PMV), phocine distemper (PDV), and canine distemper viruses (CDV) were measured. Positive samples had higher titers against the CeMV than against the other morbilliviruses tested, indicating that although PDV or CDV can be used to investigate exposure their use may result in a higher false negative rate. The results suggest that morbillivirus did not persist in coastal populations of bottlenose dolphins (Tursiops truncatus) after the major outbreaks that occurred in the 1980s and 1990s. Bottlenose dolphins from Beaufort, North Carolina; St. Joseph Bay, Florida; and Cape May, New Jersey had anti‐DMV seroprevalences ranging from between 15% and 33% but those from Charleston, South Carolina and Sarasota Bay, Florida, sampled in recent years were largely negative. These latter groups are therefore now vulnerable to infection and could experience high mortality if exposed to CeMV. Sero‐surveys of this kind are therefore vital for assessing the risk of new and recurring viral outbreaks in coastal cetaceans.     

Clinicoimmunopathologic findings in Atlantic bottlenose dolphins Tursiops truncatus with positive cetacean morbillivirus antibody titers

Sera from free-ranging Atlantic bottlenose dolphins Tursiops truncatus inhabiting the Indian River Lagoon (IRL), Florida were tested for antibodies to cetacean morbilliviruses from 2003 to 2007 as part of a multidisciplinary study of individual and population health. A suite of clinicoimmunopathologic variables were evaluated in morbillivirus-seropositive dolphins (n = 14) and seronegative healthy dolphins (n = 49). Several important differences were found. Serum alkaline phosphatase, creatine phosphokinase, chloride, albumin and albumin/globulin ratios were significantly lower in seropositive dolphins. Innate immunity appeared to be upregulated with significant increases in lysozyme concentration and marginally significant increases in monocytic phagocytosis. Adaptive immunity was also impacted in dolphins with positive morbillivirus antibody titers. Mitogen-induced T lymphocyte proliferation responses were significantly reduced in dolphins with positive morbillivirus antibody titers, and marginally significant decreases were found for absolute numbers of CD4+ lymphocytes. The findings suggest impairment of cell-mediated adaptive immunity, similar to the immunologic pattern reported with acute morbillivirus infection in other species. In contrast, dolphins with positive morbillivirus antibody titers appeared to have at least a partially upregulated humoral immune response with significantly higher levels of gamma globulins than healthy dolphins, which may represent an antibody response to morbillivirus infection or other pathogens. These data suggest that subclinical dolphin morbillivirus infection in IRL dolphins may produce clinicoimmunopathologic perturbations that impact overall health.     

Short‐finned pilot whales (Globicephala macrorhynchus) of the Mariana Archipelago: Individual affiliations,movements, and spatial use

Little is known about short‐finned pilot whales (Globicephala macrorhynchus) in the western North Pacific outside of Japanese coastal waters. To expand understanding of short‐finned pilot whale ecology in the region, we conducted small‐boat surveys in 2010?2016 within the Mariana Archipelago to investigate individual associations, movements, spatial use, and dive behavior of short‐finned pilot whales. We collected genetic, photo‐identification, and satellite‐tag data and identified 191 distinctive individuals. A preliminary social network diagram of photo‐cataloged individuals revealed a main cluster that comprised 82% of individuals, representing all five mitochondrial DNA haplotypes identified within the population. Kernel density estimates for tagged short‐finned pilot whales (n = 11) during summer were used to identify areas with the highest probability of use (10% probability density contour), core area (50%) and home range (95%). The area with highest probability of use by short‐finned pilot whales was off the northwest side of Guam. Satellite tag data also suggest that some individuals are island‐associated year‐round. Data from five location‐dive tags demonstrated that the short‐finned pilot whales dove more often to intermediate depths at twilight and night, suggesting they may target prey that forage on the deep scattering layer as it migrates to and from the surface.     

Diphyllobothriids (Cestoda: Pseudophyllidea) from the long-finned pilot whale Globicephala melas (Traill, 1809) off the Faroe Islands,with comments on the taxonomy of Diphyllobothrium Cobbold, 1858 species from cetaceans

The taxonomy of marine species of the genus Diphyllobothrium, particularly those parasitic in cetaceans, is rather confused. During parasitological investigations of long-finned pilot whales Globicephala melas from waters off the Faroe Islands, five diphyllobothriid species were detected: Diphyllobothrium sp. (possibly D. polyrugosum), D. stemmacephalum, Diphyllobothrium sp. A, Diphyllobothrium sp. B and Diphyllobothriidae sp. D. stemmacephalum is reported for the first time from G. melas. The stituation regarding the taxonomy of Diphylobothrium species from cetaceans is briefly reviewed. It is concluded that the recent development of genetic techniques may be of great value in relation to clarifying the taxonomy of this group.     

Differences in acoustic signals from Delphinids in the western North Atlantic and northern Gulf of Mexico

Whistle characteristics were quantitatively compared between both geographically separated and neighboring populations of Atlantic spotted dolphins (Stenella frontalis), bottlenose dolphins (Tursiops truncatus), and pilot whales (Globicephala spp.) in U.S. waters to evaluate if intraspecific acoustic differences exist between groups. We compared nine whistle characteristics between continental shelf and offshore Atlantic spotted dolphins in the western North Atlantic and between northern Gulf of Mexico and western North Atlantic bottlenose dolphins and pilot whales using discriminant analysis. Offshore Atlantic spotted dolphin whistles were significantly different (Hotelling's T², P= 0.0003) from continental shelf whistles in high frequency, bandwidth, duration, number of steps, and number of inflection points. Atlantic bottlenose dolphin whistles were significantly different (Hotelling's T², P < 0.0001) from those in the Gulf of Mexico in duration, number of steps, and number of inflection points. There was no significant difference between pilot whale whistles in the two basins. The whistle differences indicate acoustic divergence between groups in different areas that may arise from geographic isolation or habitat separation between neighboring but genetically distinct populations of dolphins. This study supports the premise that acoustic differences can be a tool to evaluate the ecological separation between marine mammal groups in field studies.     

Stomach contents of long‐finned pilot whales,Globicephala melas,mass‐stranded on Farewell Spit,Golden Bay in 2005 and 2008

Abstract

New data are reported on the diet of the long‐finned pilot whale, Globicephala melas, based on stomach contents recovered from whales involved in a mass stranding on Farewell Spit, Golden Bay, South Island, on 23 January 2008. The stomachs of 11 whales were examined, from which identifiable prey remains were recovered from six, four females and two males (3.1–5.4 m in length). Prey remains comprised exclusively cephalopod beaks (1–46 beaks per whale), attributed to two genera in two orders: arrow squid, Nototodarus spp. (Teuthoidea: Ommastrephidae), and common octopus, Pinnoctopus cordiformis (Octopoda: Octopodidae). The stomachs of eight whales were infested with parasitic nematodes, with two ulcerated; the stomachs of five whales did not contain any prey remains. These data complement and are comparable to the only other information available for this species from this region, reported from whales mass‐stranded at this same location in December 2005. Lower beak rostral length versus mantle length and biomass regression equations for Nototodarus spp. are reviewed, highlighting the importance of the use of species‐specific regression equations for reconstructing both cephalopod mantle length and biomass from lower beak remains in dietary studies.     

Worldwide mitochondrial DNA diversity and phylogeography of pilot whales (Globicephala spp.)

Pilot whales (Globicephala spp.) provide an interesting example of recently diverged oceanic species with a complex evolutionary history. The two species have wide but largely non‐overlapping ranges. Globicephala melas (long‐finned pilot whale; LFPW) has an antitropical distribution and is found in the cold‐temperate waters of the North Atlantic and Southern Hemisphere, whereas Globicephala macrorhynchus (short‐finned pilot whale; SFPW) has a circumglobal distribution and is found mainly in the tropics and subtropics. To investigate pilot whale evolution and biogeography, we analysed worldwide population structure using mitochondrial DNA (mtDNA) control region sequences (up to 620 bp) from a variety of sources (LFPW = 643; SFPW = 150), including strandings in New Zealand and Tasmania, and whale‐meat products purchased on the markets of Japan and Korea. Phylogenetic reconstructions failed to support a reciprocal monophyly of the two species, despite six diagnostic substitutions, possibly because of incomplete lineage sorting or inadequate phylogenetic information. Both species had low haplotype and nucleotide diversity compared to other abundant widespread cetaceans (LFPW, π = 0.35%; SFPW, π = 0.87%) but showed strong mtDNA differentiation between oceanic basins. Strong levels of structuring were also found at the regional level. In LFPW, phylogeographic patterns were suggestive either of a recent demographic expansion or selective sweep acting on the mtDNA. For SFPW, the waters around Japan appear to represent a centre of diversity, with two genetically‐distinct forms, as well as a third population of unknown origin. The presence of multiple unique haplotypes among SFPW from South Japan, together with previously documented morphological and ecological differences, suggests that the southern form represents a distinct subspecies and/or evolutionary significant unit. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 729–744.     

Detection of specific antibodies to morbilliviruses, Toxoplasma, and Brucella species in eared seals in North-West of Pacific Ocean

Presence of antibodies to morbilliviruses, Toxoplasma, and Brucella species in eared seals in North-West of Pacific Ocean was studied. Sera from 189 cubs of eared seals from different rookeries and regions. It has been shown that 10-22% of cubs living on Russian coast have antibodies to such dangerous diseases as morbillivirus infection, brucellosis, and toxoplasmosis. Antibodies to the two pathogens were detected in several animals, and brucellosis was more frequently detected associated infection. These results confirm hypothesis that all 3 pathogens are enzootic in eared seals population.     

Fatal Asphyxiation in Two Long-Finned Pilot Whales (Globicephala melas) Caused by Common Soles (Solea solea)

Long-finned pilot whales (Globicephala melas) are rare visitors to the southern North Sea, but recently two individual strandings occurred on the Dutch coast. Both animals shared the same, unusual cause of death: asphyxiation from a common sole (Solea solea) stuck in their nasal cavity. This is a rare cause of death in cetaceans. Whilst asphyxiation has been reported in smaller odontocetes, there are no recent records of this occurring in Globicephala species. Here we report the stranding, necropsy and diet study results as well as discuss the unusual nature of this phenomenon. Flatfish are not a primary prey species for pilot whales and are rarely eaten by other cetaceans, such as harbour porpoises (Phocoena phocoena), in which there are several reports of asphyxiation due to airway obstruction by soles. This risk may be due to the fish’s flexible bodies which can enter small cavities either actively in an attempt to escape or passively due to the whale ‘coughing’ or ‘sneezing’ to rid itself of the blockage of the trachea. It is also possible that the fish enter the airways whilst the whale is re-articulating the larynx after trying to ingest large, oddly shaped prey. It is unlikely that the soles entered the airways after the death of the whales and we believe therefore that they are responsible for the death of these animals.     

Stomach contents of long-finned pilot whales (Globicephala melas) from southern Chile

The widely distributed long-finned pilot whale (Globicephala melas) has been reported off the Chilean coast, from Iquique (20°12′S) south to Navarino Island (55°15′S; 67°30′W), but little is known about its biology or ecology in the region. Here, we report on the prey of this species, identified by stomach content analyses from animals stranded on Holget Islets, Beagle Channel, southern Chile in August 2006. The stomachs of seven individuals (six females and one male) contained cephalopod remains. The prey composition found in these southern Chilean pilot whales was similar to that described in other parts of the world and the Southern Ocean. This is the first report on the feeding habits of this species from Chile.