Ailsa J. Hall

Is Marine Mammal Health Deteriorating? Trends in the Global Reporting of Marine Mammal Disease

A recent rise in the reporting of diseases in marine organisms has raised concerns that ocean health is deteriorating. The goal of this study was to determine whether or not there has been a recent deterioration in marine mammal health by investigating the trends in disease reports over the past 40 years (categorized by the method of study, the species affected, and the etiology of the disease) and by exploring the changes in frequency of mass mortality events among marine mammals reported in the United States since 1978. The number of papers on marine mammal disease published each year has increased since 1966, although the annual publication rate appears to have stabilized since ∼1992. Those published in the 1960s and 1970s were largely about helminth and bacterial disease, those investigating viruses emerged in the late 1970s and increased in the 1980s and 1990s, whereas protozoal diseases and harmful algal toxins were largely not reported until the 1990s. The annual number of mass mortality events in the U.S. approximately doubled between 1980 and 1990 but since 2000 has been between seven and eight events per year. Causes of mass mortality events have included biotoxins, viruses, bacteria, parasites, human interactions, oil spills, and changes in oceanographic conditions. Events due to biotoxins appear to be increasing, but the change in the frequency of mass mortality events from other causes over the past 40 years cannot be determined from the available published literature due to changes in marine mammal abundance, inconsistencies in effort and extent of resources for pathological investigation, and advances in technology that have allowed improved detection of pathogens and toxins in more recent years. To ensure future information on the true incidence of marine diseases and their underlying causes is more reliable, specific and directed marine health monitoring programs, well-equipped stranding networks, and dedicated diagnostic laboratories are needed.

The Risk of Infection from Polychlorinated Biphenyl Exposure in the Harbor Porpoise (Phocoena phocoena): A Case–Control Approach

The objective of this study was to determine whether the risk of mortality from infectious disease in harbor porpoise in U.K. waters increased with high exposure to polychlorinated biphenyls (PCBs), using a case–control study design. This is the first time that data from a long-term marine mammal strandings scheme have been used to estimate any increase in risk. The exposure odds ratio (OR) from a logistic regression model with infectious disease deaths as cases and physical trauma deaths as controls, after controlling for the effect of confounding factors, was 1.048 [95% confidence interval (CI), 1.02–1.07]. To further adjust for the difference in energetic status between cases and controls and account for the negative relationship between PCBs (sum of 25 chlorobiphenyl congeners) and blubber mass, we also “standardized” the blubber PCBs to an optimal blubber mass. This lowered the OR to 1.02 (95% CI, 1.00–1.03). Thus, for each 1 mg/kg increase in blubber PCBs, the average increase in risk of infectious disease mortality was 2%. A doubling of risk occurred at approximately 45 mg/kg lipid. In this study, we have endeavored to avoid selection bias by using controls that died of physical trauma as representative of the exposure prevalence in the population that gave rise to the cases. In addition, we controlled for the effect of variation in energetic status among the cases and controls. However, as with case–control studies in human and veterinary epidemiology, unforeseen misclassification errors may result in biased risk estimates in either direction.

Overcoming the challenges of studying conservation physiology in large whales: a review of available methods

A description and comparison of the four major methods available for studying conservation physiology of large whales, namely analysis of faecal, respiratory vapour, and skin/blubber biopsy samples, and photographs.

Individual-Based Model Framework to Assess Population Consequences of Polychlorinated Biphenyl Exposure in Bottlenose Dolphins

Marine mammals are susceptible to the effects of anthropogenic contaminants. Here we examine the effect of different polychlorinated biphenyl (PCB) accumulation scenarios on potential population growth rates using, as an example, data obtained for the population of bottlenose dolphins from Sarasota Bay, Florida. To achieve this goal, we developed an individual-based model framework that simulates the accumulation of PCBs in the population and modifies first-year calf survival based on maternal blubber PCB levels. In our example the current estimated annual PCB accumulation rate for the Sarasota Bay dolphin population might be depressing the potential population growth rate. However, our predictions are limited both by model naivety and parameter uncertainty. We emphasize the need for more data collection on the relationship between maternal blubber PCB levels and calf survivorship, the annual accumulation of PCBs in the blubber of females, and the transfer of PCBs to the calf through the placenta and during lactation. Such data require continued efforts directed toward long-term studies of known individuals in wild and semi-wild populations.

Cetacean Morbillivirus: Current Knowledge and Future Directions

We review the molecular and epidemiological characteristics of cetacean morbillivirus (CeMV) and the diagnosis and pathogenesis of associated disease, with six different strains detected in cetaceans worldwide. CeMV has caused epidemics with high mortality in odontocetes in Europe, the USA and Australia. It represents a distinct species within the Morbillivirus genus. Although most CeMV strains are phylogenetically closely related, recent data indicate that morbilliviruses recovered from Indo-Pacific bottlenose dolphins (Tursiops aduncus), from Western Australia, and a Guiana dolphin (Sotalia guianensis), from Brazil, are divergent. The signaling lymphocyte activation molecule (SLAM) cell receptor for CeMV has been characterized in cetaceans. It shares higher amino acid identity with the ruminant SLAM than with the receptors of carnivores or humans, reflecting the evolutionary history of these mammalian taxa. In Delphinidae, three amino acid substitutions may result in a higher affinity for the virus. Infection is diagnosed by histology, immunohistochemistry, virus isolation, RT-PCR, and serology. Classical CeMV-associated lesions include bronchointerstitial pneumonia, encephalitis, syncytia, and lymphoid depletion associated with immunosuppression. Cetaceans that survive the acute disease may develop fatal secondary infections and chronic encephalitis. Endemically infected, gregarious odontocetes probably serve as reservoirs and vectors. Transmission likely occurs through the inhalation of aerosolized virus but mother to fetus transmission was also reported.

Transplacental transfer of organochlorines in california sea lions (Zalophus californianus)

The transplacental transfer of organochlorines (OCs) in California sea lions (Zalophus californianus) was investigated by analyzing blubber samples from 20 female sea lions and their fetuses during the last trimester of pregnancy. A rapid, high-performance liquid chromatographic, photodiode-array method was used to measure blubber concentrations of polychlorinated biphenyls (PCBs), including dioxin-like congeners, as well as DDTs and hexachlorobenzene. Summed values of PCBs (sigmaPCBs), of DDTs (sigmaDDTs), and of PCB toxic equivalents (sigmaPCB TEQs) were calculated from these data. The ratios of mean blubber concentrations of fetal sigmaPCBs to maternal blubber concentrations of sigmaPCBs were 0.45 by wet weight and 0.97 by lipid weight, but these ratios varied widely among mother-fetus pairs. Mean ratios of fetal sigmaDDTs to maternal sigmaDDTs were 0.53 by wet weight and 1.12 by lipid weight. Fetuses were classified into two age groups, based on date of recovery, to examine differences in OC transfer because of gestational age. Fetal to maternal ratios for individual PCB congeners, DDT compounds, and sigmaPCBs, sigmaDDTs, and sigmaPCB TEQs were lower among premature compared with late-term fetuses. These ratios increased for both groups as the logarithmic n-octanol/water partition coefficient (log Kow) for each compound decreased. Linear predictions for sigmaPCB and sigmaDDT concentrations in fetal blubber could be obtained using the sigmaPCB and sigmaDDT concentrations in maternal blubber, maternal and fetal blubber lipid content, maternal mass, and maternal age. Fetal TEQ was explained by maternal TEQ and maternal age. The ability to predict contaminant concentrations in fetal blubber from maternal parameters is important for developing risk assessment models for marine mammals.

Morbilliviruses in aquatic mammals: report on round table discussion

A workshop was organised to ascertain the current situation with regard to morbillivirus infections in aquatic animals. The great interest generated by the discovery of these new virus infections in 1988 has to some extent abated but much high quality research has continued in this field as the workshop showed. There is some serological evidence that the viruses have continued to circulate in most areas since the initial epizootics. As to their origin, it appears that the most likely source of the European seal morbillivirus (PDV-1) is the North Atlantic and Artic seal populations. As to the origin of the Mediterranean dolphin morbillivirus and the morbilliviruses isolated from porpoises, there is serological evidence that the viruses are widespread in many cetacean species in the Atlantic and 93% of long-finned pilot whales (Globicephala melas) which mass stranded between 1982 and 1993 were morbillivirus seropositive. The epizootic in freshwater seals in Lake Baikal was unrelated to events in the European marine mammal populations. The virus which infected these animals (PDV-2) is indistinguishable from canine distemper field strains. Serological and molecular biological studies provided evidence for the presence of the virus in the seals, at least as late as the Summer of 1992 when the animals were last sampled.

Polychlorinated biphenyls, DDT, polybrominated diphenyl ethers, and organic pesticides in United Kingdom harbor seals (Phoca vitulina)—mixed exposures and thyroid homeostasis

Polychlorinated biphenyls, DDT and its metabolites, polybrominated diphenyl ethers, and selected organochlorine pesticide concentrations were measured in blubber samples from 60 free-living harbor seals in 2003 from five sites around the United Kingdom coast. Significant regional differences among contaminant levels were found, with seals on Islay and Jura (southwest Scotland) having the highest levels of polychlorinated biphenyls and seals in the Wash (eastern England) having the highest polybrominated diphenyl ether levels. Animals from the north and northeast of Scotland (Orkney and the Moray Firth) had the lowest levels of all the contaminant groups studied. Congener-specific profiles of polychlorinated biphenyls and polybrominated diphenyl ethers showed relatively higher levels of the lower chlorinated and brominated compounds at the more northerly sites, with the lowest total levels of both chemical groups. Significant positive relationships between blubber contaminants and total triiodothyronine (TT3) concentrations were found after controlling for the potential effects of confounding because of sex, mass, and season. Increased serum TT3 levels were significantly related to higher blubber contaminant concentrations in the following order: sum of all contaminants > polybrominated diphenyl ethers > polychlorinated biphenyls > DDT. Serum TT3 levels in the harbor seals with the highest exposures might be indicative of a T3 thyrotoxicosis, but without information on free T3 and circulating thyroid-stimulating hormone levels, it is difficult to determine the importance of this observation for the health of the individuals or populations. However, the mixture of contaminants to which United Kingdom harbor seals are exposed has changed over the last few decades, and the toxicological and epidemiological importance of adding the brominated compounds to the classical organochlorine and heavy metal mixture is not known.

Thyroid hormones as biomarkers in grey seals

Changes in grey seal (Halichoerus grypus) serum thyroid hormones with age, sex and during lactation were investigated. Concentrations were related to polychlorinated biphenyl (PCB) uptake and exposure in pups and females. There was no effect of sex or stage of lactation on either free or total thyroxine (T4) and triiodothyronine (T3), but significant age-related variability was seen. Pups had significantly higher concentrations of total T4 than adults (p <0.0001) and serum levels declined with age. In general, there was no significant relationship between PCB exposure to pups through female milk or between PCB blubber concentrations and thyroid hormone levels, when the effect of age was controlled for. However, the ratio T3:T4 was significantly correlated with the concentration of one congener, CB169 (p = 0.048), when stage of lactation was used as a covariate. In conclusion, serum thyroid hormone levels may be less useful biomarkers of contaminant exposure in seals than other biochemical measures. Although concentrations vary predictably with age, other factors, such as condition and nutritional status, may compromise their usefulness in assessing contaminant-induced hormone disruption in pinnipeds.

HEMATOLOGY AND SERUM CHEMISTRY IN STRANDED AND WILD-CAUGHT HARBOR SEALS IN CENTRAL CALIFORNIA: REFERENCE INTERVALS, PREDICTORS OF SURVIVAL, AND PARAMETERS AFFECTING BLOOD VARIABLES

Blood was collected from stranded harbor seal (Phoca vitulina) pups at admission (n=64) and release (n=45) from rehabilitation in 2007 and 2008 and from wild-caught harbor seal pups, subadults, and adults (n=110) in 2004, 2007, and 2008. Blood values measured at the time of admission were not predictive of survival during rehabilitation. Mass was associated with survival until release, and all pups that died weighed less than 10 kg at the time of admission. Do ¨hle bodies were observed in leukocytes from 15% to 22% of the pups in rehabilitation, but not in the wild pups. Thresholds (95% confidence intervals) among wild pups were less than those in the released pups for leukocytes, neutrophils, total cholesterol, alanine aminotransferase (ALT), glucose, phosphorus, sodium, potassium, total protein, albumin, and globulin; thresholds were greater in wild pups than in released pups for hemoglobin (HGB), hematocrit (HCT), and glucose. Thresholds among released pups were less than those in wild pups for HGB, HCT, mean cell volume, chloride, and creatine kinase; thresholds among released pups were greater than those in wild pups for neutrophils, platelets, total cholesterol, triglycerides, ALT, aspartate aminotrans-ferase, sorbitol dehydrogenase, bilirubin, phosphorus, potassium, total protein, and albumin. Age, girth, and geographic location affected the blood variables from wild-caught pups; age class, geographic location, sex, and body condition affected the blood variables of wild-caught, subadult and adult harbor seals.