The term “mass die-off’ has been used rather imprecisely in the scientific literature. In general, it is an event that involves the death of many hundreds of individuals in a relatively short interval (usually 1-2 months). Mass die-offs of rare species may involve smaller numbers of individuals, but the use of this term can be justified if a large proportion of the population is involved in the die-off. Strandings of groups of social cetaceans, such as pilot whales (Globicephala macro-rhynchus and G. melas) and false killer whales (Feresa attenu-ata), should probably not be regarded as mass die-offs. However, large numbers of dead bodies may wash up along a short section of coast during a mass die-off, and this may, initially, resemble a stranding event. Marine mammals spend most of their lives at sea and only a fraction of the number of individuals that die during a mass die-off are likely to be observed. As a result, die true magnitude and effect of a mass die-off cannot be assessed from a simple body count. The scale of the die-off is usually best estimated by comparing abundance estimates made before and after the event.
I. Diagnosis
The fact that marine mammals spend most of their lives at sea makes it not only difficult to determine how many individuals have died during a mass die-off, but also difficult to diagnose the cause. Many days may elapse between the death of an individual and the recovery of its carcass. To make matters worse, many die-offs occur along remote stretches of coastline where access is difficult, further increasing the time between death and examination. The problem is further complicated because many of the agents that can cause mass die-offs also reduce resistance to diseases. Exposure to these agents may then allow other pathogens, which would otherwise by relatively harmless, to contribute toward an individual’s death.
Despite these problems, it has proved possible to identify with some confidence the causes of several of the mass die-offs that were observed in the last 20 years of the 20th century. Three factors appear to be particularly important: infectious diseases, naturally occurring toxins, and environmental events. Several of these factors may act together, and the effects of any one of them can be amplified by anthropogenic factors (such as previous exposure to potentially toxic chemicals).
II. Disease
Disease of one kind or another is a frequent cause of mortality in marine mammal populations, but highly infectious disease organisms (particularly viruses) can cause the death of large numbers of animals in a very short period. An influenza virus probably caused die death of at least 450 harbor seals (Phoca vitulina) along die New England coast of the United States in 1979-1980. The family of viruses that is most often associated widi disease-induced die-offs, however, is the morbilliviruses. Measles is the most familiar virus in this family. Canine distemper virus (probably contracted from domestic dogs or farmed mink) caused the death of several thousand Baikal seals (Pusa sibirica) in the Russian Federation in 1987-1988. The closely related phocine distemper virus caused the death of 18,000 harbor seals in the North Sea during 1988, and a dolphin morbillivirus caused the death of several thousand striped dolphins (Stenella coendeoalba) in the Mediterranean Sea between 1990 and 1992. The death of more than 740 bottlenose dolphins (Tursiops tnmcatus) along the Atlantic coast of die United States in 1987 was initially attributed to poisoning by algal toxins (see later), but more recent evidence suggests that this was also caused by dolphin morbillivirus. Morbilliviruses tend to suppress dieir host’s immune system, thus increasing the risk of secondary infection by a wide range of disease agents. These secondary infections are often the final cause of death for an individual infected with a morbillivirus, which can make it difficult to diagnose the real cause of a die-off.
III. Toxins
Some species of single-celled algae (notably diatoms and di-noflagellates) produce poisonous compounds (known as phyco-toxins), which can accumulate in any fish or invertebrates animals that eat them. When environmental conditions are particularly suitable, these organisms multiple rapidly, creating “blooms.” The resulting high concentrations of phycotoxins can cause mass mortalities of fish and fish predators. The best documented event of this kind involving marine mammals was the death of over 400 California sea lions (Zalophus californianus) along the central California coast during May and June 1998. This coincided with a bloom of an algal diatom, which is known to produce domoic acid, a dangerous neurotoxin, in the same area. Domoic acid was detected in northern anchovies, which are plankton feeders and a well-known prey of sea lions, and in the body fluid of sick sea lions. These sea lions also showed many of the neurological symptoms commonly associated with domoic acid poisoning.
Toxins produced by dinoflagellate protozoa have been implicated in the deaths of Hawaiian monk seals (Monachus schauinslandi) in 1978, in the death of 14 humpback whales (Megaptera novaeangliae) in Cape Cod Bay in 1987, and in the death of large numbers of manatees (Trichechus manatus) in Florida in 1982 and 1996.
In May and June 1997 the bodies of over 100 Mediterranean monk seals (Monachus monachus) were found along a short stretch of the West African coast near the border between Mauritania and the former Western Sahara. Initial investigations revealed that at least some of these individuals had been infected with a morbillivirus, which most closely resembled dolphin morbillivirus, and the mass die-off was originally attributed to this agent. However, most of the seals died quickly with few, if any, overt signs of disease. This was very different from what had been observed in other morbillivirus-induced events. Subsequent analysis provided evidence of the presence of several phy-cotoxins in dead seals and high concentrations of a dinoflagellate known to produce at least one of these phycotoxins in local coastal waters. It is possible that both agents were involved in the die-off. On the basis of the evidence currently available, it is not possible to say with any confidence that either was responsible.
IV. Environmental Effects
Unusual environmental conditions can cause high levels of mortality, particularly among young animals. For example, severe storms coupled with unusually high tides during the winter of 1982-1983 resulted in the death of up to 80% of all northern elephant seal (Mirounga angustirostris) pups born at some California colonies.
Even more dramatic effects can be caused by changes in oceanographic conditions. For example, El Nino southern oscillation events can dramatically alter the availability of prey species around marine mammal colonies. The severe 1982-1983 El Nino event bad wide-ranging effects on fur seal and sea lion colonies throughout the eastern Pacific. Its effects were even evident in populations of seals in the Antarctic.
An intrusion of low oxygen content water into the coastal waters of Namibia in early 1994 resulted in a massive reduction in the availability of fish. Colonies of Cape fur seals (Arc-tocephalus pusillus pusillus) in Namibia suffered the highest levels of pup mortality ever observed: approximately 120,000 pups had died by the end of May 1994. There was also very high mortality among those subadult males that remained on the breeding grounds.
V. Anthropogenic Effects
Deliberate killing by humans can cause mass die-offs of marine mammals, but the effects of such activities are dealt with elsewhere. However, human activities can also result in mass die-offs through indirect effects. The most obvious of diese is the exposure of marine mammals to harmful chemicals that are spilled or discharged into the marine environment. Although marine mammals are probably less vulnerable to the effects of oil spills than seabirds, species such as the sea otter (Enhydra lutris), which rely on dieir dense fur for insulation, can be seriously affected. Indeed, it is estimated that 3500 to 5500 sea otters died in 1989 after die tanker Exxon Valdez spilled 42 million liters of oil in Prince William Sound, Alaska. Odier chemicals may have a more insidious effect. A wide range of man-made halogenated organic compounds are preferentially soluble in fat and can accumulate at high concentrations in the blubber of predatory marine mammals. These compounds can lower resistance to disease, and individuals with high tissue levels may be particularly vulnerable during mass die-offs caused by disease agents. High organochlorine levels may well have been a contributory factor to mortality during die morbillivirus epidemics in die North Sea and Mediterranean.
A combination of environmental factors and fishing activity may also result in die-offs. For example, large numbers of harp seals (Pagophilus groenlandicus) appeared off the north coast of Norway between 1985 and 1988, probably as a result of the collapse of the stocks of capelin, an important prey species, in the Barents and Norwegians Seas. Many of these seals became entangled in fishing nets and subsequently drowned. The Norwegian government compensated fishermen for the damage this caused, and these compensation statistics provide an estimate of the minimum number of seals that drowned. Compensation for 79,000 seals was paid in 1987 and 1988.
VI. Effects on Populations
Determining the effect of mass die-offs on the marine mammal population is often difficult because baseline data on the size and status of the affected population are lacking. However, their impact can be substantial. For example, the morbillivirus-induced die-off in the North Sea killed approximately 40% of the harbor seal population, and local mortality rates were as high as 60%. The mass die-off of Mediterranean monk seals in 1997 killed 70% of the local population and about one-third of the world population of this species.
Some marine mammal populations have shown a remarkable ability to recover from the effects of die-offs. The North Sea harbor population returned to its pre-epidemic level within 10 years of the seal die-off, although some local populations (e.g., those along the eastern seaboard of England) are still depleted. However, species whose populations are already small (such as the Mediterranean monk seal, whose world population was less than 1000 individuals at the time of the die-off) may be reduced to such low levels that they are more susceptible to other problems associated with low population size (such as increased levels of inbreeding and the loss of genetic diversity through genetic drift). As a result, their risk of extinction may be increased substantially.
VII. Future Trends
There are a number of grounds for predicting that the frequency of mass die-offs will increase during this century. Certainly marine mammals populations, like many other species, will be exposed ever more frequently to novel pathogens as a result of the increased movement of humans and their domestic animals who can act as vectors for these agents. Global warming is also likely to lead to new movement patterns, which will increase the exchange rate of these pathogens.
Exposure to toxins, particularly those produced by dinofla-gellate algae, is also likely to increase. Levels of nutrients and minerals, which are normally in short supply, are periodically increased in coastal waters by large-scale run-off of rainwater from agriculture land. This occurs more frequently now because of modern drainage techniques and can create conditions that are favorable to algal blooms. In addition, dinoflagellates are particularly well adapted to transportation in the ballast water of large ships because, when conditions are unfavorable, they become encased in a protective cyst. As a result, many species that historically had a very restricted distribution now have a global one. For example, Gymnodinium catenatum (one of the species implicated in the mass die-off of Mediterranean monk seals) was, until recently, confined to the east coast of the United States, but since 1970 it has been recorded in Japan and Australia, as well as off the west coast of Africa.
