Decompression sickness ('the bends') in sea turtles.

Decompression sickness (DCS), as clinically diagnosed by reversal of symptoms with recompression, has never been reported in aquatic breath-hold diving vertebrates despite the occurrence of tissue gas tensions sufficient for bubble formation and injury in terrestrial animals. Similarly to diving mammals, sea turtles manage gas exchange and decompression through anatomical, physiological, and behavioral adaptations. In the former group, DCS-like lesions have been observed on necropsies following behavioral disturbance such as high-powered acoustic sources (e.g. active sonar) and in bycaught animals. In sea turtles, in spite of abundant literature on diving physiology and bycatch interference, this is the first report of DCS-like symptoms and lesions. We diagnosed a clinico-pathological condition consistent with DCS in 29 gas-embolized loggerhead sea turtles Caretta caretta from a sample of 67. Fifty-nine were recovered alive and 8 had recently died following bycatch in trawls and gillnets of local fisheries from the east coast of Spain. Gas embolization and distribution in vital organs were evaluated through conventional radiography, computed tomography, and ultrasound. Additionally, positive response following repressurization was clinically observed in 2 live affected turtles. Gas embolism was also observed postmortem in carcasses and tissues as described in cetaceans and human divers. Compositional gas analysis of intravascular bubbles was consistent with DCS. Definitive diagnosis of DCS in sea turtles opens a new era for research in sea turtle diving physiology, conservation, and bycatch impact mitigation, as well as for comparative studies in other air-breathing marine vertebrates and human divers.

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals.

Decompression sickness (DCS; 'the bends') is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N(2)) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N(2) tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N(2) loading to management of the N(2) load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Phenotypic and genetic divergence among harbour porpoise populations associated with habitat regions in the North Sea and adjacent seas.

Determining the mechanisms that generate population structure is essential to the understanding of speciation and the evolution of biodiversity. Here, we investigate a geographical range that transects two habitat gradients, the North Sea to North Atlantic transition, and the temperate to subpolar regions. We studied the harbour porpoise (Phocoena phocoena), a small odontocete inhabiting both subpolar and temperate waters. To assess differentiation among putative populations, we measured morphological variation at cranial traits (N = 462 individuals) and variation at eight microsatellite loci for 338 of the same individuals from Norwegian, British and Danish waters. Significant morphological differentiation reflected the size of the buccal cavity. Porpoises forage in relatively shallow waters preying mainly on benthic species in British and Danish waters, and on mesopelagic and pelagic fish off the coast of Norway. We suggest that the observed differentiation may be explained by resource specialization and either adaptation or developmental responses to different local habitats.

Postmortem evidence of interactions of bottlenose dolphins (Tursiops truncatus) with other dolphin species in south-west England.

Reports of violent interactions between bottlenose dolphins (Tursiops truncatus) and harbour porpoises (Phocoena phocoena) in the coastal waters of the UK are well documented. Examination of stranded cetaceans by the Cornwall Wildlife Trust Marine Strandings Network and the UK Cetacean Strandings Investigation Programme has indicated that seven animals, of four other species, found stranded in south-west England, had pathology consistent with bottlenose dolphin interaction, including two juvenile and two adult common dolphins (Delphinus delphis), one juvenile pilot whale (Globicephala melas), one juvenile Risso's dolphin (Grampus griseus) and one adult striped dolphin (Stenella coeruleoalba). Although recorded traumatic lesions were often not as severe as those found in harbour porpoises, it is probable that the interactions did contribute to stranding and/or death in all four of the juvenile animals examined. Furthermore, analysis of photographs taken before establishment of the Marine Strandings Network revealed rake (teeth) marks consistent with bottlenose dolphin interaction on one stranded common dolphin in 1992. A number of causes have been suggested for these interactions in harbour porpoises stranded in the UK and it is possible that any combination of these factors may also be implicated in the cases described in this report.

Mass-dependent predation risk and lethal dolphin-porpoise interactions.

In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin 'predation' occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation-predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.

An insight into the epidemiology of dolphin morbillivirus worldwide.

Serum samples from 288 cetaceans representing 25 species and originating from 11 different countries were collected between 1995 and 1999 and examined for the presence of dolphin morbillivirus (DMV)-specific antibodies by an indirect ELISA (iELISA) (N = 267) or a plaque reduction assay (N = 21). A total of 35 odontocetes were seropositive: three harbour porpoises (Phocoena phocoena) and a common dolphin (Delphinus delphis) from the Northeastern (NE) Atlantic, a bottlenose dolphin (Tursiops truncatus) from Kent (England), three striped dolphins (Stenella coeruleoalba), two Risso's dolphins (Grampus griseus) and a bottlenose dolphin from the Mediterranean Sea, one common dolphin from the Southwest (SW) Indian Ocean, three Fraser's dolphins (Lagenodelphis hosei) from the SW Atlantic, 18 long-finned pilot whales (Globicephala melas) and a bottlenose dolphin from the SW Pacific as well as a captive bottlenose dolphin (Tursiops aduncus) originally from Taiwan. The presence of morbillivirus antibodies in 17 of these animals was further examined in other iELISAs and virus neutralization tests. Our results indicate that DMV infects cetaceans worldwide. This is the first report of DMV-seropositive animals from the SW Indian, SW Atlantic and West Pacific Oceans. Prevalence of DMV-seropositives was 85.7% in 21 pilot whales from the SW Pacific and both sexually mature and immature individuals were infected. This indicates that DMV is endemic in these animals. The same situation may occur among Fraser's dolphins from the SW Atlantic. The prevalence of DMV-seropositives was 5.26% and 5.36% in 19 common dolphins and 56 harbour porpoise from the NE Atlantic, respectively, and 18.75% in 16 striped dolphins from the Mediterranean. Prevalence varied significantly with sexual maturity in harbour porpoises and striped dolphins; all DMV-seropositives being mature animals. The prevalence of seropositive harbour porpoise and striped dolphins appeared to have decreased since previous studies. These data suggest that DMV is not endemic within these populations, that they are losing their humoral immunity against the virus and that they may be vulnerable to new epidemics.

Exposure to heavy metals and infectious disease mortality in harbour porpoises from England and Wales.

We investigate whether long-term exposure to heavy metals, including immunosuppressive metals like mercury (Hg), is associated with infectious disease in a wild cetacean. Post-mortem investigations on 86 harbour porpoises, Phocoena phocoena, found dead along the coasts of England and Wales revealed that 49 of the porpoises were healthy when they died as a consequence of physical trauma (most frequently entrapment in fishing gear). In contrast, 37 porpoises died of infectious diseases caused by parasitic, bacterial, fungal and viral pathogens (most frequently pneumonia caused by lungworm and bacterial infections). We found that mean liver concentrations of Hg, selenium (Se), the Hg:Se molar ratio, and zinc (Zn) were significantly higher in the propoises that died of infectious disease compared to healthy porpoises that died from physical trauma. Liver concentrations of lead (Pb), cadmium (Cd), copper (Cu) and chromium (Cr) did not differ between the two groups. Hg, Se, and the Hg:Se molar ratio were also positively correlated with age. The association between Zn concentration and disease status may result from Zn redistribution in response to infection. Further work is required to evaluate whether chronic exposure to Hg may have presented a toxic challenge to the porpoises that succumbed to infectious disease.

Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales.

Bioaccumulation of immunosuppressive organochlorines like polychlorinated biphenyls (PCBs) may pose a threat to the health and viability of cetacean populations. To investigate possible associations between chronic exposure to PCBs and infectious disease mortality in harbour porpoises Phocoena phocoena in UK waters, blubber concentrations of 25 individual chlorobiphenyl (CB) congeners in 34 healthy harbour porpoises that died due to physical trauma (mainly by-catch) were compared with CB concentrations in 33 animals that died due to infectious disease. The infectious disease group had significantly greater total 25 CBs (sigma 25CBs) concentrations than the physical trauma group (P < 0.001). The mean sigma 25CBs concentration in animals that died due to physical trauma was 13.6 mg kg-1 extractable lipid whereas the mean concentration in the infectious disease group was 31.1 mg kg-1 extractable lipid. The relationship between higher sigma 25CBs and the infectious disease group was not confounded by age, sex, nutritional status, season, location or year of stranding. In addition, adult females had significantly lower sigma 25CBs levels than adult males (P < 0.05) due to maternal transfer of CBs to offspring. These findings are consistent with the hypothesis that chronic PCB exposure predisposes harbour porpoises in UK waters to infectious disease mortality, although further research is required to test these associations more robustly.

Causes of mortality and non-fatal conditions among grey seals (Halichoerus grypus) found dead on the coasts of England, Wales and the Isle of Man.

A survey of the diseases detectable in 141 grey seals stranded on the coasts of England and Wales away from breeding colonies was carried out between mid-1989 and early 1997. The most common fatal conditions in pups less than three weeks of age were trauma (24 per cent of deaths) and dystocia (12 per cent); in pups more than three weeks of age thy were starvation (22 per cent) and pneumonia (22 per cent); in juveniles they were drowning in fishing gear (30 per cent) and starvation (19 per cent), and in adults a variety of respiratory diseases were the most common causes of death (45 per cent). Many other diseases, both fatal and non-fatal, were recorded.

Pulmonary pathology of harbour porpoises (Phocoena phocoena) stranded in England and Wales between 1990 and 1996.

The pathological changes observed in the lungs of 197 freshly dead to moderately decomposed harbour porpoises (Phocoenaphocoena) stranded in England and Wales between October 1990 and December 1996 were reviewed. In 135 (69 per cent of the cases) macroscopic nematode infections of the bronchial tract with Pseudalius inflexus and Torynurus convolutus, either singly or in combination, were recorded, and 106 (54 per cent) also had P inflexus within the pulmonary blood vessels. All the macroscopically parasitised porpoises were adults or juveniles although two neonates had histological evidence of nematode infection. There were 62 cases of mild to severe, subacute to chronic bronchitis and bronchiolitis, 113 cases of mild to severe chronic granulomatous interstitial pneumonia, and 34 cases of mild to severe vasculitis or thrombovasculitis of pulmonary blood vessels attributable to these nematode infections. In 35 cases necropurulent or purulent (broncho)pneumonias were attributed either to secondary bacterial infections of the lungs or to septicaemias associated in seven cases with Streptococcus canis, in two cases with group B Salmonella species, in one case with Escherichia coli and in one case with Streptococcus lactis. The pulmonary lesions in 67 animals known or diagnosed to have been entrapped in fishing gear were non-specific and included persistent foam in the airways in 45 cases, diffuse congestion in 53, oedema in 50, and multifocal intra-alveolar haemorrhage in 33 cases. Seven cases of acute fibrinous or chronic fibrous pleuritis, seven cases of chronic necropurulent pneumonia associated with mycotic infections, four porpoises with traumatic lesions of the thorax and other parts of the body consistent with fatal attack from bottlenose dolphins (Tursiops truncatus), and one case of diffuse bronchointerstitial pneumonia associated with generalised morbillivirus infection were also recorded.

Entanglement in fishing gear and other causes of death in cetaceans stranded on the coasts of England and Wales.

Between August 1990 and September 1995 the carcases of 422 cetaceans of 12 species that had died around the coasts of England and Wales were examined. There were 234 harbour porpoises (Phocoena phocoena), 138 common dolphins (Delphinus delphis), and 50 individuals of 10 other species of dolphins and whales. The cause of death was diagnosed in the harbour porpoises and common dolphins was entanglement in fishing gear (bycatch). Of the cases in which the cause of death was established, 66 (38 per cent) of 176 harbour porpoises, 86 (80 percent) of 108 common dolphins, and six (19 per cent) of 31 individuals of other species had been bycaught. Neonatal starvation, pneumonia and generalised infections accounted for a further 31 per cent of the diagnosed causes of death in harbour porpoises. The proportion of stranded common dolphins that had been bycaught was consistently high except during 1995, but the proportion of stranded harbour porpoises which had been bycaught increased in each successive year.

Antibodies to Brucella in marine mammals around the coast of England and Wales.

Following the isolation of previously unrecognised species of Brucella from stranded seals and cetaceans in Scotland and northern England, a serological survey was carried out to investigate the range of marine mammal species which may have been exposed to Brucella species around the coasts of England and Wales, the prevalence of infection and the temporal and geographical distribution of seropositive animals. Serum collected from 153 stranded marine mammals from the coasts of England and Wales between 1989 and 1995 were tested by competitive and indirect ELISA. Positive titres were recorded for six of 62 (10 per cent) grey seals (Halichoerus grypus), one of 12 (8 per cent) common seals (Phoca vitulina), 11 of 35 (31 per cent) harbour porpoises (Phocoena phocoena) and nine of 29 (31 per cent) common dolphins (Delphinus delphis) tested. Positive titres were also found in a striped dolphin (Stenella coeruleoalba), a bottlenose dolphin (Tursiops truncatus), a killer whale (Orcinus orca) and a pilot whale (Globicephala melas). The seropositive animals were from all around the coasts of England and Wales and the first seropositive sample was from a common dolphin in 1990.

True hermaphroditism: first evidence of an ovotestis in a cetacean species.

An immature unilateral hermaphrodite common dolphin (Delphinus delphis) was found stranded on the southwest coast of the UK. The external phenotype was that of a female, but internally there was one ovotestis, containing both ovarian follicles and testicular tubular elements, and a contralateral ovary. Ovarian portions of the ovotestis appeared normal and demonstrated follicular development, whereas the testicular tissue exhibited hypoplasia and degeneration. This is the first reported case of an ovotestis in a cetacean species.

Infection with Brucella ceti and high levels of polychlorinated biphenyls in bottlenose dolphins (Tursiops truncatus) stranded in south-west England.

Eight bottlenose dolphins (Tursiops truncatus) that stranded in Cornwall, south-west England, between June 2004 and December 2007 were examined using standardised postmortem examination and bacteriological methods. Evidence of Brucella species infection was found in four of these dolphins on culture. In addition, of the eight dolphins, four were positive and two were weakly positive for antibodies to Brucella species on serological analyses of pericardial and other fluids using a competitive ELISA and two indirect ELISAs. High or very high levels of the sum of 25 individual chlorobiphenyl congeners (∑25CBs) were also determined in blubber samples from two of the dolphins (45.5 and 446.6 mg/kg lipid weight).

Prevalence of a host-adapted group B Salmonella enterica in harbour porpoises (Phocoena phocoena) from the south-west coast of England.

A monophasic group B Salmonella enterica 4,12:a:- was first isolated in harbour porpoises (Phocoena phocoena) in Scotland in 1991. This paper reports the isolation of the same group B S enterica from harbour porpoise carcases found stranded along the Cornwall and Devon coastlines. Between 1991 and 2002, 80 harbour porpoises were submitted for postmortem examination and subjected to bacteriological examination under the UK Cetacean Strandings Investigation Programme. A total of 28 Salmonella isolates were recovered and subjected to several tests, including biochemical, molecular and serological analysis.