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THE MOST COMMON DEFINITION OF DISEASE is “any departurefrom normality” (Rothman 1986). This description may seem simple enough,and it may indeed be straightforward to diagnose disease among individual an-

imals in close contact with humans. Yet establishing its occurrence, frequency, andparticularly its impact on wildlife populations presents a challenge that has been con-fronted only in recent years.

For a disease to have an effect on a population, it must first affect an individual. Itsconsequent effect at the population level then depends on what is happening to thepopulation’s demography (i.e., its fecundity, survival, and dispersal). Little is knownabout the ecological significance of disease in marine mammal populations becausework to date has focused mostly on individual animal health. For the most part, ef-fort has been directed toward infectious disease, the category that we emphasizehere. However, it should be remembered that many other diseases could concur-rently have a negative impact on a particular species or population. As they are diffi-cult to diagnose and are perhaps relatively rare in marine mammals, they may be eas-ily overlooked. Such diseases are likely to belong to the other major categories:malignant, congenital, degenerative, deficiency, functional, toxic, and metabolic.

Theoretical studies suggest that infectious diseases regulate host abundance by ex-erting density-dependent effects on reproduction or survival (Anderson 1979). How-ever, there have been few empirical studies on free-living animals to determinewhether the effects of disease on populations are indeed density dependent. This ispartially because: (a) density-dependent effects are hard to detect when populations

F R A N C E S M . D. G U L L A N D A N D A I L S A J . H A L L

The Role of InfectiousDisease in InfluencingStatus and Trends

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are at equilibrium, and (b) most disease investigations inwildlife have focused on determining the proximate ratherthan predisposing causes of large die-offs.

A few studies of terrestrial wildlife have shown that in-teractions between disease and factors such as host nutri-tion, behavior, genetics, and climate can influence life his-tory parameters and population dynamics (reviewed inHudson et al. 2002). Such investigations depend upon con-current monitoring of both infectious disease and host pop-ulation dynamics, which has rarely happened in marinemammal disease research. To date, most research has fo-cused on the causes of morbidity and mortality in strandedand captive animals and on the health of hunted animals.These studies have shown that there are a number of dis-eases in free-living marine mammal populations that cancause mortality or decrease growth and reproduction bothas primary or secondary factors, interacting with other fac-tors discussed later in the chapter.

Epidemiology (the study of the occurrence of disease) isa relatively new discipline with a number of specifically de-fined terms that can be confused with each other, butwhich, in fact, mean quite different things. In order to avoidsuch misunderstanding, some definitions of common epi-demiological terms are given in Table 4.1.

THE INFLUENCE OF DISEASE ONSTATUS AND TRENDS OF MARINEMAMMAL POPULATIONS

Disease and Marine Mammal Mortality

EPIDEMIC DISEASES. Epidemic diseases (sometimesreferred to as epizootics when dealing with animals ratherthan humans) are those that occur at a time or in a placewhere they are not usually found or with a greater fre-quency than expected in a certain period. The most dra-matic effect of disease on marine mammal populations isthe increase in mortality during an epidemic. Severe epi-demics might reduce host population density to such an ex-tent that stochastic events or previously unimportant eco-logical factors may further reduce the host population size(Harwood and Hall 1990). For example, canine distemperdramatically reduced black-footed ferret (Mustela nigripes)populations in Wyoming, bringing them to extinction in thewild (Thorne and Williams 1988), and avian malaria re-duced native Hawaiian honeycreeper (Hemignathus parvus)populations to such small numbers that many were finallyeliminated by predation or habitat loss (Warner 1968). Theimportance of infectious disease epidemics in causing de-clines in marine mammal populations as a result of in-creased mortality is unclear, as few marine mammal die-offshave been sufficiently investigated to determine their causeand because it is often difficult to determine pre-epidemichost population size accurately.

Recent epidemics among marine mammals have causeddramatic mortality, but the effects on host population size

have varied. For example, approximately 18,000 harbor seals(Phoca vitulina) (70% of the population) died in the phocinedistemper virus (PDV) epidemic in Europe in 1988, and ageand sex distributions were skewed for several years after theepidemic (Heide-Jørgensen et al. 1992a). Ten years later,however, the population in most of Europe had recoveredto pre-epidemic numbers (Reijnders et al. 1997). The originof this morbillivirus epidemic is unclear, but it may havebeen introduced to harbor seals by the southward dispersalof harp seals (Phoca groenlandica) from the Barents andGreenland seas, where the virus is believed to be endemic

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Table 4.1 Definitions of terms commonly used in epidemiological studies

Term Definition

Prevalence This is a static measure; the proportion of a defined group having a condition at one point in time, often expressed as a percentage. A period preva-lence is the proportion having a condition at any time within a stated period.P = number with disease/total number sampled

Incidence This is a kinetic measure; the proportion of a defined group developing a condition within a stated period. The term is often used in reference to a disease frequency but epidemiologically it is a proportion, that is, a number of cases related to a defined population and a stated period of time.I = number of new cases/total number individualsx time sampled

Intensity This is usually used in reference to parasites either: (i) the mean number of parasites within infected members of the host population, or (ii) the mean parasite burden of the entire population. It is important to distinguish between these two, as unless the prevalence is 100%, the population parasite burden will be less than the mean number within the infected members of the host population.

Rate Rates constitute the underlying principal concept in epidemiology as the basis for comparison betweenpopulation groups and most rates take the form:Frequency of observed state or event/Total number in whom this state or event might occur

Microparasite Parasites that undergo direct multiplication within their definitive hosts (e.g., viruses, rickettsia, bacteria, fungi, and protozoa)

Macroparasite Parasites that in general do not multiply within their definitive hosts, but instead produce transmission stages (eggs and larvae) that pass into the external environment or to vectors.

Endemic A disease whose prevalence or occurrence does not exhibit wide fluctuations through time in a defined location or population.

Epidemic A sudden, rapid spread or increase in the prevalence or intensity of a parasite or disease. An epidemic is often the result of a change in circumstances that favors pathogen transmission.

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(Stuen et al. 1994). This introduction of a virus into a naïvepopulation with large numbers of susceptible animals with-out antibodies allowed rapid transmission above a thresholdlevel, resulting in an epidemic.

A mathematical model developed in 1992 to investigatethe infection dynamics of this disease predicted that rein-troduction of the virus resulting in large-scale mortalitywould not occur again for at least 10 years, after which timethe number of susceptible (nonimmune) harbor sealswould again be sufficient to maintain an epidemic (Gren-fell et al. 1992). A new outbreak of PDV occurred in theNorth Sea in 2002 ( Jensen et al. 2002), killing more than20,000 harbor seals (cwss.www.de/news/publications/Wsnl/Wsnl02-2/articles/1-seal-epidemic.pdf; and www.waddensea-secretariat.org/news/news/Seals/01-seal-news.html). Inter-estingly, no influx of harp seals was reported prior to thisoutbreak. The questions about triggers and disease vectorsof the 2002 epidemic still have to be answered.

The impacts of morbillivirus epidemics on other marinemammal populations are less well documented. Outbreaksof canine distemper (CDV) killed 5,000–10,000 Baikal seals(Pusa sibirica) in 1987–1988 (Grachev et al. 1989) and 10,000Caspian seals (P. caspica) in 2000 (Kennedy et al. 2000), andmay also have been responsible for the deaths of 2,500crabeater seals (Lobodon carcinophagus) in the Antarctic in1955 (Laws and Taylor 1957, Bengtson et al. 1991). A mor-billivirus was isolated from Mediterranean monk seals(Monachus monachus) that died during an epidemic, but itsimportance relative to biotoxins in causing mortality re-mains controversial (Hernandez et al. 1998). Dolphin mor-billivirus (DMV) caused the deaths of several thousandstriped dolphins (Stenella coeruleoalba) in the MediterraneanSea in 1990–1992 (Domingo et al. 1990) and then spread toshort-beaked common dolphins (Delphinus delphis) in theBlack Sea in 1994 (Birkun et al. 1999). It was also found intissues of bottlenose dolphins (Tursiops truncatus) from adie-off of approximately 750 animals along the easternUnited States in 1987–1988 (Lipscomb et al. 1994). As pop-ulation estimates and stock structure for this latter speciesare unclear, the percentage of the dolphin population af-fected is unknown but may have been as much as 50% ofone stock (National Oceanic and Atmospheric Administra-tion 2000). A fourth morbillivirus, porpoise morbillivirus(PMV), was detected in dead bottlenose dolphins in 1993 inthe northern Gulf of Mexico and in a die-off of harbor por-poises (Phocoena phocoena) in the Irish Sea in 1994 (Kennedyet al. 1988, Taubenberger et al. 1996). The PMV and DMVviruses are antigenically similar and may represent differentstrains of a “cetacean” morbillivirus referred to as CMV(Blixenkrone-Møller et al. 1996). Although CMV infectionhas been documented to have caused die-offs of cetaceans,the numerical effect on cetacean populations is still uncer-tain, mostly because of a lack of knowledge regarding mor-tality at times other than during epidemics and changes inpopulation size and structure over time.

A smaller epidemic in harbor seals occurred along theNew England coast of the United States in 1979–1980 and

was associated with influenza A infection (Geraci et al.1982). Unusually warm conditions, crowding, and a con-current respiratory infection with mycoplasma may havetriggered this epidemic, which killed at least 450 seals (3–5%of the local population) (Payne and Schneider 1984).

Bacteria can also cause epidemic mortality in marinemammals. Leptospira pomona was first isolated from Cali-fornia sea lions (Zalophus californianus) in 1970 and has sincecaused periodic die-offs of sea lions along the northern Cal-ifornia coast about every 4 years (Vedros et al. 1971, Gullandet al. 1996). Despite hundreds of animals dying in each out-break, the impact of the mortality has not prevented thegrowth of the California sea lion population, currently esti-mated at about 10% a year (Forney et al. 2000). Similarly, agram-negative pleiomorphic bacterium that was believedresponsible for an epidemic in the endangered Hooker’s sealion (Phocarctos hookeri) population in New Zealand in 1998caused mortality of 60% of that year’s pup production(Baker 1999), followed by a 5% decrease in pup productionthe following year. No long-term impact on the populationdynamics of these sea lions has been detected (I. Wilkinson,pers. comm.).

ENDEMIC DISEASES. Endemic diseases (or enzooticdiseases in animals) are those that occur in a population ata regular, predictable rate. Endemic diseases, which can alsocause widespread mortality, do not exhibit wide spatial ortemporal fluctuations in occurrence although suddenchanges in host susceptibility or pathogen transmission cancause an endemic disease to become epidemic. A number ofmicroparasites that cause endemic mortality have beenidentified in stranded marine mammals. These include atleast ten families of viruses (reviewed by Visser et al. 1991,VanBressem et al. 1999), thirty genera of bacteria (reviewed byDunn et al. 2001), and several fungi (reviewed by Reidarsonet al. 2001) that have been associated with disease in indi-vidual marine mammals. Their effects on populations arecurrently unknown as their dynamics are not understood.

Macroparasites (helminths and arthropods) are rarely as-sociated with epidemics because their transmission dynam-ics are different than those of the microparasites (virusesand bacteria). They do not reproduce in the host, do notelicit long-lasting immunity, and have an aggregated distri-bution within the host population (Shaw and Dobson 1995).This aggregation has important implications for effects onthe host; as a rule, the stability of the host-parasite interac-tion is enhanced by parasite aggregation. The interactionamong aggregation, parasite virulence, transmission effi-ciency, and the host’s population growth rate in the absenceof parasites determines whether the host-parasite interac-tion is stable or exhibits cyclic or chaotic dynamics (Wilsonet al. 2002). As macroparasites tend to have dose-dependenteffects on host morbidity and mortality, effects are morelikely in individuals at the “tail” of the distribution. Smallsample sizes are thus likely to miss affected hosts.

The effects of macroparasite-induced mortality on ma-rine mammal host populations are thus difficult to docu-

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ment, and few studies have attempted to assess them. An ex-ception is a study of cranial lesions caused by the nematodeCrassicauda sp. in spotted dolphins (Stenella attenuata) killedaccidentally in the eastern tropical Pacific tuna fishery (Per-rin and Powers 1980). Changes in the prevalence of irre-versible lesions with age suggested that Crassicauda hadcaused 11–14% of the natural mortality, although biasessuch as dolphins with lesions being caught preferentially inthe fishery could have affected the study results. Lambert-son (1986) similarly examined the prevalence of Crassicaudaboopis in North Atlantic fin whales (Balaenoptera physalus)and estimated parasite-associated mortality to be 4.4–4.9%of the total. He also suggested that infection of blue whales(Balaenoptera musculus) with Crassicauda boopis could limitrecruitment in this species as mortality attributed to infec-tion occurred at about the same age (1 year) as the inferredpeak in natural mortality estimated from population mod-els of this species (Lambertson 1992).

Disease and Marine Mammal Reproduction

Infectious diseases alter reproductive rates in terrestrialmammals and birds by decreasing fertility and causing abor-tion, premature parturition, and neonatal mortality (Scott1988, Feore et al. 1997). These effects may be destabilizingand can regulate host population dynamics in some cases—for example, the nematode Trichostrongylus tenuis causes cy-cles in red grouse (Lagopus lagopus) populations by decreas-ing reproduction (Hudson 1986). Many infectious agentsthat could have similar effects in marine systems have onlyrecently been isolated from marine mammals, and theirprevalence and impact on free-ranging marine mammalpopulations are unknown (Dailey 2001, Dunn et al. 2001).

Caliciviruses and Leptospira interrogans var. pomona havebeen isolated from cases of abortion and premature pup-ping in California sea lions with high levels of organochlo-rines (Gilmartin et al. 1976); herpesviruses have been de-tected in aborted harbor seal fetuses and dead pups(Osterhaus et al. 1985, Gulland et al.1997); Coxiella burnettiwas detected in a case of placentitis in a harbor seal (La-Pointe et al. 1999); Toxoplasma gondii was detected in a fetusof a dead Risso’s dolphin (Grampus griseus; Resendes et al.2002); and a Brucella sp. has been isolated from an abortedbottlenose dolphin (Miller et al. 1999). Papillomaviruseshave been detected in cases of genital warts in Burmeister’sporpoises (Phocoena spinipinnis) in Peru, where the lesionsmay be sufficiently severe to impede copulation (VanBressem et al. 1999).

Although such pathogens have rarely been isolated frommarine mammals and to date have only been detected in afew individuals, serological surveys suggest that exposure tothese diseases is widespread. Antibodies to Brucella spp. havebeen detected in a wide range of cetacean and pinnipedspecies around the United Kingdom, Canada, and theUnited States; antibodies to Chlamydia spp. are common inSteller sea lions (Eumetopias jubatus) and Hawaiian monkseals (Monachus schauinslandi); antibodies to caliciviruses

and herpesviruses are present in most pinniped speciestested; and antibodies to Toxoplasma gondii are prevalent inmost coastal cetaceans and pinnipeds (Braun pers. comm.,Barlough et al. 1987, Stenvers et al. 1992, Nielsen et al. 1996,Jepson et al. 1997, Zarnke et al. 1997, Forbes et al., 2000,Mikaelian et al. 2000, Burek et al. 2001). Thus infectiousagents shown to cause reproductive failure in individual ma-rine mammals and terrestrial mammal populations existand are probably widespread, but their direct and indirecteffects on the distribution and abundance of marine mam-mals still need to be determined.

Disease and Marine Mammal Condition and Growth

Experimental studies in birds have shown that parasites maydirectly limit the growth of individuals (Booth et al. 1993),potentially reducing future survival and delaying the onsetof sexual maturity. Macroparasites such as nematodes,trematodes, and cestodes are common in marine mammals,but whether or not the parasites limit growth in these hostshas not been established because research concerning thisrelationship has been so limited. In two separate surveys ofringed seals (Pusa hispida) infected with the lungworm Oto-strongylus circumlitus, no correlation between intensity of in-fection and body condition could be detected, althoughthere was a slight reduction in respiratory parenchyma in in-fected seals (Onderka 1989, Bergeron et al. 1997). The de-crease in the prevalence of infection after the first winter,however, suggests that O. circumlitus may play a role in de-creasing overwinter juvenile survival. We are unaware offurther studies directly investigating impacts of disease onthe growth of marine mammals.

In a mark-recapture study of gray seals (Halichoerus gry-pus) Hall et al. (2002) found that postweaned pups with hightotal immunoglobulin G, particularly males in poor condi-tion, had a lower first-year survival probability. It is notknown whether this was because the pups were exposed todisease (although all appeared clinically healthy) or becauseindividuals with naturally high IgG had to make a trade-offbetween resources needed for growth and developmentagainst those needed to maintain relatively higher circulat-ing antibody levels. Such studies, which investigate the in-terplay between growth and exposure/response to infec-tious disease, may help us understand more about therelative importance of such interactions during vulnerableperiods in the animals’ life history.

Disease and Host Defenses

The form and function of marine mammal immune sys-tems have been the focus of attention and research only inthe last few years, and then largely because many persistentocean contaminants have been shown to be immunotoxicto laboratory animals and other species (De Swart et al.1994, De Guise et al. 1998). How immunity is affected bytoxic contaminants has thus been the driving force behind

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much of the research in this field, often with the underlyingassumption that the immune systems of marine and terres-trial species must be similar (see also O’Hara and O’Sheathis volume). However, immunity to disease is clearly af-fected by many factors, including age, sex, species, and sea-son (Nelson et al. 2002). Relatively little is known about theimmune systems of marine mammals, particularlycetaceans (De Guise 2002) and how they have evolved com-pared to the systems of terrestrial species. The integrity andmaintenance of immunity are central to the prevention ofdisease in individuals and populations. The system’s mainpurpose is to control infection by pathogens. If we are to un-derstand more about the impact of disease on marine mam-mal populations, then host defense mechanisms should beconsidered in their widest context, from the viewpoints ofboth comparative and functional immunology.

INTERACTIONS OF DISEASE WITHOTHER FACTORS THAT AFFECTMARINE MAMMAL POPULATIONS

Changes in disease prevalence and, in turn, increased hostmorbidity or mortality may result from increases in hostsusceptibility, pathogenicity of the disease agent, or trans-mission of pathogens to hosts. A number of discrete or in-teracting factors can influence each of these processes, asdiscussed later in the chapter.

Nutrition

Food limitation may alter the prevalence and incidence ofdisease by decreasing the host’s immune response to infec-tion (Seth and Boetra 1986) or by altering host behavior(Scott 1988). Interactions between food limitation and par-asitism can determine which individuals die during popula-tion crashes of ungulates (Gulland 1992). Food limitation,nutritional deficiencies, and infectious diseases all occur inmarine mammals, but the interactions among them havenot been examined. It was suggested that poor nutritionamong seals in some areas of the North Sea resulted inhigher mortality from PDV during the 1988 epidemic, al-though evidence for nutritional immunosuppression in thiscase was lacking because of the immunosuppressive effectof the virus itself (Heide-Jorgensen et al. 1992b). StrandedCalifornia sea lions that are suffering from food deprivationor are feeding on unusual prey species during El Niño yearshave heavier burdens of the gastric nematode Contracaecumcorderoi than do stranded animals in other years, and the for-mer are more likely to die from peritonitis caused by perfo-rated parasitic ulcers (Fletcher et al. 1998). Mortality fromperitonitis following migration of parasites from the intes-tine also occurs in California sea otters (Enhydra lutris nereis),in this case following infection with the acanthocephalansProfilicollis altmani, P. kenti, and P. major. Young male ottersare more frequently affected by these parasites than areother otters (Mayer et al. 2003). The acanthocephalans are

acquired by the consumption of crabs (Emerita spp. and Ble-pharipoda spp.) that are intermediate hosts of these parasitesbut are not the preferred food of most otters. Mayer et al.(2003) hypothesize that young males are more susceptibleto infection by acanthocephalans because their lack of feed-ing experience and low social status lead them to forage onless desirable prey species.

Population Density

Population density can have dramatic effects on disease dy-namics, as it can affect the transmission of diseases directlyas well as indirectly via effects on host nutrition and preda-tion (Hudson et al. 2002). The spread of PDV during the1988 epidemic among North Sea harbor seals was limited insome areas by low host density (Thompson and Hall 1993).Recent changes in the mortality of pinnipeds associatedwith hookworm infestation suggest that this macroparasiteaffects host mortality in density-dependent ways. The hook-worm Uncinaria lucasi was an important cause of northernfur seal (Callorhinus ursinus) pup mortality on the PribilofIslands in the 1960s (Olsen and Lyons 1965). Since then, pupnumbers and parasite-associated mortality have decreased(Fowler 1990), suggesting that lower pup densities are re-ducing parasite transmission. Interestingly, initial work sug-gests that, as California sea lion pup numbers increase onSan Miguel Island off California, mortality associated withhookworm infection is increasing (Lyons et al. 1997).

Host Movement and Distribution

Movement of a pathogen-infected host into a previously un-exposed host population can result in severe epidemics andcan contribute to the competitive success of the invadinghost (Daszak et al. 2001). Anthropogenic movement of aninfected host is called “pathogen pollution” (Daszak et al.2000). Movements of uninfected hosts into areas with en-demic pathogens can also result in disease outbreaks in thenew range of the host (Daszak et al. 2001). Movements ofmarine mammals prompted by environmental changes,such as El Niño events and global warming, can lead tomovement of pathogens into susceptible host populations.For example, as noted earlier, the 1988 PDV epidemic in theNorth Sea harbor seal population was likely triggered by thesouthward movement of harp seals from the Barents andGreenland seas, carrying the virus from where it was en-demic into an area with a naïve population (Heide-Jorgensen et al. 1992a). A dramatic reduction in the fishstocks in the Barents Sea in 1987 probably caused the harpseals to forage farther south in search of prey. The commonlungworm of Arctic seals, Otostrongylus circumlitus, has onlyrecently been reported in the increasing northern elephantseal (Mirounga angustirostris) population in California,where it kills the host before the parasite reproduces (Gul-land et al. 1997). This is probably a new host-parasite asso-ciation, judging by the high pathogenicity and lack of trans-mission of the parasite before the death of the host. It may

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be the result of expansion of the elephant seal populationleading to increased range overlap with Arctic phocids.

Parasites can affect the coexistence of closely related hostspecies if the parasites have a differential impact on the de-mographic rates of the hosts (Holt and Pickering 1985).Hookworm (Uncinaria spp.) infections of South Americansea lions (Otaria byronia) and fur seals (Arctocephalus aus-tralis) along the coasts of Chile and Uruguay may be exam-ples of such parasite-mediated competition, as intensity ofinfections was greater, while prevalence of lesions waslower, in fur seal pups compared to sea lion pups (George-Nascimento et al. 1992). The demographic effects of theparasite on the two host species are still unclear, and mo-lecular techniques are needed to clarify whether or not theUncinaria sp. in the two hosts is indeed the same species.

Population density may also influence haul-out behaviorof harbor seals, which, in turn, influences their degree of ag-gregation and thus the transmission rates of contagious dis-eases such as PDV. Outbreaks of PDV in Europe occurredwhen the population density of seals was high relative tohistorical levels.

Host Genetics

Species differences in susceptibility to different diseases pre-sumably reflect genetic differences among hosts. For exam-ple, gray seals (Halichoerus grypus) are more resistant to PDVthan sympatric harbor seals (Thompson and Hall 1993).Within the few mammalian species studied to date (miceand sheep), parasite resistance and reproductive success co-vary with parental similarity (Smith et al. 1999). Polymor-phisms at certain alleles controlling immune responses cor-relate with parasite resistance, and polymorphism at themajor histocompatibility complex (MHC) is associated withimproved immune response (Slate et al. 2000, Coltman et al.2001, Messaudi et al. 2002). No studies have yet investigatedthe correlation between MHC variability and disease resist-ance in marine mammals. In a recent study of stranded Cal-ifornia sea lions, parental relatedness as measured by poly-morphism at eleven microsatellites was greater in animalsstranding with infectious diseases than in those stranding asa result of trauma (Acevedo-Whitehouse et al. 2003).Among the sea lions with infectious diseases, animals withhelminth infections were more inbred than animals withbacterial infections, and there was a significant positive re-gression of parasite diversity on inbreeding. These resultsdemonstrate the importance of host genetics in modulatingthe host-parasite interaction, but do not identify mecha-nisms by which such effects occur.

Predation and Fisheries Bycatch

In terrestrial systems it has been shown that the interactionbetween parasitism and predation can magnify apparentlysmall effects of parasites on host morbidity. For example,free-ranging snowshoe hares (Lepus americanus) that hadtheir worm burdens reduced by anthelmintics were signifi-

cantly less likely to be caught by predators than a similargroup of controls (Murray et al. 1997). Predation rates werereduced still further in hares that received food supplemen-tation, suggesting an interaction between parasite-inducedsusceptibility to predation and the host’s plane of nutrition.As a result of logistic difficulties in conducting such studies,little is known about interactions between predation andparasitism in marine mammals. It is likely that infectiousdiseases predispose marine mammals to both predation andfisheries bycatch. For example, beach-cast sea otters in Cal-ifornia have been observed to suffer from both protozoal en-cephalitis and great white shark wounds, suggesting thatneurological disease associated with protozoal infection in-creased their vulnerability to predation (Thomas and Cole1996). Disease studies using bycaught, stranded, and har-vested animals could address these issues further.

Increased Urbanization of the Coast

As human populations increase along coastlines, so doescontact between marine mammals and humans, their petsand livestock, and their associated pathogens. Molecularanalyses of morbillivirus isolates from tissues of Baikal andCaspian seals collected during two successive epidemics inthese populations revealed wild-type CDV (Mamaev et al.1995, Kennedy et al. 2000). Transmission of CDV probablyoccurs via aerosols from domestic or feral dogs althoughaerosol transmission of CDV from adjacent susceptible ter-restrial wildlife species such as foxes is also possible (Lyonset al. 1993).

Influenza B (B/Seal/Netherlands/1/99) was isolated in1999 from a juvenile harbor seal with respiratory signs (thefirst time that influenza B had been isolated from a non-human; Osterhaus et al. 2000). Sequence analysis of the iso-late showed it to be closely related to strains present in thehuman population in 1995. Moreover, retrospective sero-surveys showed no antibodies to influenza B in the seal pop-ulation around The Netherlands prior to 1995. Seals pre-sumably were infected by a virus transmitted from humansin 1995 and may now serve as reservoirs for influenza Bviruses that had previously circulated only among humans.

Contact between humans and marine mammals is alsoincreased by the practice of rehabilitating sick or injuredmarine mammals in urban areas. This also increases the ex-posure of the animals to pathogens of terrestrial mammalsas they are often housed in rehabilitation facilities accessibleto wildlife such as small rodents. Kidney failure and mortal-ity associated with Leptospira interrogans var. gryppotyphosahave been observed in harbor seals infected during rehabil-itation, probably as a result of exposure to terrestrial ro-dents or skunks (Stamper et al. 1998).

Sewage containing pathogens may also influence diseasefrequency in marine mammals. Toxoplasma gondii, an obli-gate parasite of felids that is shed as infective oocysts in catfeces, appears to be common in southern sea otters, causingvarying degrees of meningoencephalitis (Cole et al. 2000).Sea otters may be infected through ingestion of the oocyst

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stage, either directly from the water or by consuming filter-feeding invertebrates that concentrate the oocysts. Envi-ronmental contamination by feral and domestic cat popula-tions, either directly or from the human disposal of cat fecesin sewage, might play a significant role in epidemiology ofsea otter toxoplasmosis (Cole et al. 2000). Salmonella bovismorbificans, a bacterial serotype associated with cattle, hasbeen isolated from harbor seals around the United King-dom. This may indicate contamination of seal habitat withagricultural runoff (Baker et al. 1995).

Pathogen antimicrobial resistance has been recognized inmarine mammals admitted to rehabilitation facilities ( John-son et al. 1998). Frequent use of antibiotics for the treatmentof humans, domestic pets, and livestock, combined with thecontamination of the environment with resistant bacteriathrough raw sewage spills, municipal water dumping, andagricultural and storm/flood runoff, has resulted in antibi-otic-resistant bacteria in the environment. The distributionof these bacteria in marine mammal populations is un-known, but it is likely influenced by urbanization and isprobably an important indicator of pathogen movement be-tween terrestrial and marine mammals.

Runoff from urban and agricultural areas may also influ-ence the prevalence of infectious diseases by altering the fre-quency of harmful algal blooms, which appears to be in-creasing (Harvell et al. 1999, Van Dolah this volume). Sometoxins produced by harmful algal blooms, such as breve-toxin, may alter the immune system of mammalian hosts,increasing their susceptibility to infectious diseases (Bossartet al. 1998). As brevetoxin-producing blooms are common inareas where die-offs of bottlenose dolphins associated withDMV have occurred, it is possible that brevetoxin modulatedthe immune response of the dolphins to the virus, therebyincreasing the severity of the die-off (Geraci et al. 1999).

Pathogens may also be transported around the marineenvironment by the global movement of ballast water inships (Ruiz et al. 2000). A recent study showed that Vibriocholerae can often be delivered to estuaries with commercialports and that some bacteria in ballast tanks are viable uponarrival.

Contaminants

Experimental studies on captive harbor seals fed fish withvarying levels of organochlorine contaminants and oncetacean cells in vitro have shown that organochlorines haveimmunotoxic properties, decreasing natural killer cell ac-tivity as well as a series of mitogen- and antigen-induced T-cell responses (De Swart et al. 1994, De Guise et al. 1998).The effect of this alteration of the immune response on re-sistance to infectious disease in the wild is unclear, as mostfield studies have a number of confounding variables otherthan contaminants and disease status. Field studies investi-gating relationships between organochlorine exposure andeffects on the immune system or deaths from disease havenot shown consistent patterns, probably because of thesevariables and small sample sizes.

Blubber organochlorine levels in about 100 harbor por-poises that died around the United Kingdom in 1989–1992were not significantly different in animals that died from in-fectious disease and those that died from trauma (primarilyin fisheries) (Kuiken et al. 1994). However, animals that diedof trauma were not necessarily free of infectious disease. Incontrast, a second study of this same population based onsamples from fresh carcasses collected from 1990 to 1996showed significantly higher concentrations of total PCBs,and of sixteen out of twenty-five PCB congeners, in harborporpoises that died from infectious disease ( Jepson et al.1999). Organochlorine concentrations in blubber of harborseals that died in the 1988 phocine distemper virus (PDV)outbreak in the United Kingdom had higher levels thanthose that survived, but the relationship was confounded bythe weight loss in sick animals, which may have concen-trated lipid soluble compounds in blubber (Hall et al. 1992).Concentrations of PCBs in blubber of striped dolphins fromthe Mediterranean Sea that died during a morbillivirus epi-demic in the early 1990s were extremely high compared toother marine mammals and to striped dolphins sampled bybiopsy in the area before and after the epidemic, suggestingthat PCBs may have influenced susceptibility to morbil-livirus (Aguilar and Borrell 1994). Other studies have foundno statistical associations between organochlorine concen-trations in juvenile harbor seals collected before and duringa PDV outbreak, and the addition of PCBs to the diet of cap-tive harbor seals did not affect susceptibility to morbilliviruschallenge (Blomkvist et al. 1992, Harder et al. 1992).

Exposure to organochlorines has also confounded inves-tigations into the cause of premature parturition in Califor-nia sea lions on San Miguel Island. Sea lions that gave birthto pups prematurely had higher levels of organochlorines intheir blubber than did females carrying pups to term, butthe former also had antibodies (indicating exposure) to Lep-tospira interrogans and caliciviruses (Gilmartin et al. 1976).These pathogens are capable of causing abortion, and dif-ferences in blubber organochlorine levels may be the con-sequence rather than the cause of differences in puppingdate. Thus, from the available data, organochlorines couldhave: (a) modified immune responses to the pathogens thatcaused the early births, (b) caused the premature parturi-tion, or (c) had no effect on parturition date. The etiologyof premature parturition in this species remains unclear,and the interactions among infectious disease, immunity,and exposure to contaminants remain elusive, mostly be-cause of the large number of confounding variables in fieldstudies and the lack of experimental studies determining effects of exposure to contaminants on marine mammals(O’Shea and Brownell 1998).

Further discussion of contaminants can be found in thechapter by O’Hara and O’Shea in this volume.

Stress

Marine mammals encounter stressors daily; predators, intra-and interspecific aggressors, and adverse oceanic or weather

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conditions can challenge homeostatic processes. Anthro-pogenic factors such as vessel traffic, fishing, and under-water noise may increase the homeostatic response to alevel that elicits an adverse stress response, which can mod-ulate resistance to infectious diseases. The subtle physio-logical changes involved in the stress response of marinemammals are still poorly understood but are likely to de-crease the immune response through a number of endo-crine changes and direct effects on the lymphoid system (re-viewed by St. Aubin and Dierauf 2001).

Few studies have investigated the effects of stress on dis-ease epidemiology in marine mammals. Wilson et al. (1999)found that epidermal lesions in bottlenose dolphins weremore common in animals potentially stressed by low watertemperatures and salinity. Outbreaks of phocine herpesvirus 1 in harbor seals occur in rehabilitation centers, wherestress is likely a precipitating factor (Visser et al. 1991).

Multiple Pathogens

Interactions among pathogens, particularly between micro-and macroparasites or among different macroparasitespecies, are often reported in wildlife disease studies (Kre-cek et al. 1987). These co-occurrences and associations haveimplications for the impact of the primary disease on thehost population as the behavior and infectivity of each de-termines its distribution and transmission characteristics.Modeling and predicting the effects of these complexities onhost population dynamics may cause other problems(Gupta et al. 1994). Some examples of associations havebeen reported in marine mammals. Geraci et al. (1981) re-ported that the seal louse (Echinophthirius horridus) is an im-portant intermediate host for three developmental stages ofthe heartworm (Dipetalonema spirocauda) in the harbor seal.Brucella infection has been found in Parafilaroides sp. lung-worms in harbor seals (Garner et al. 1997), and phocine herpesvirus 1 is often secondarily associated with PDV inharbor seals (Osterhaus et al. 1985).

REVIEW OF SCIENTIFICAPPROACHES

Trends in Prevalence of Marine Mammal Diseases

Reports of emerging and resurging marine mammal dis-eases are increasing in frequency and severity (Harvell et al.1999). This increase may be due, in part, to improved ob-servation and record-keeping following opportunistic ex-aminations, increased numbers of necropsies performed bypathologists rather than biologists, and multidisciplinary in-vestigations of recent epizootics. Stranded animals, fish-eries bycatch, subsistence-harvested animals, and animalscaught for research purposes are being more closely exam-ined by veterinarians and pathologists. Additionally, variousnovel technologies have enhanced our ability to identify andmeasure pathogens and toxins so that agents previously un-detected or unidentified can now be assayed even in smallor decomposing tissue samples.

It is difficult to determine whether there has been a realincrease in the occurrence of marine mammal disease or,rather, whether increased reporting reflects increased inter-est in marine mammals generally and, perhaps, marinemammal disease in particular. To investigate and assesstrends in marine mammal disease over the past 50 years, wereviewed 500 papers published in peer-reviewed journalssince 1966. As with other scientific literature, the number ofpapers on marine mammal disease published each year hasincreased (Fig. 4.1). In this sample, the number of papers in-creased fourfold over a period of around 40 years, withpeaks occurring during and after the European distemperoutbreaks. A list of the papers reviewed (with their ab-stracts) can be found at www.smru.st-and.ac.uk.

To assess trends in the occurrence of marine mammaldisease, we categorized the published studies by the diseaseagents investigated (viral, bacterial, parasitic, fungal, proto-zoal, and harmful algal toxins). Trends in the different dis-

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Fig. 4.1. Number of papers published on marinemammal disease, 1966–2002.

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ease agents (as proportions of the total number of papersreviewed, by 3-year blocks) are shown in Figure 4.2a,b.

The papers published in the 1960s and 1970s concernedprimarily parasitic and bacterial disease. Investigations ofviruses emerged in the late 1970s and increased in the 1980sand 1990s. Fungal disease, especially lobomycosis in dol-phins, seems to have been studied particularly in the late1970s and early 1980s, whereas protozoal diseases and theeffects of harmful algal toxins on marine mammals wererarely reported until the 1990s. Although biased in someways (e.g., by delays in completing and publishing analyses),the broad trends seem essentially accurate. They appear toreflect our increasing ability to investigate the effects of thepathogens that are harder to isolate, such as small bacteria,protozoa, and algal toxins.

A number of mass mortalities of marine mammals havebeen reported in the literature, and this phenomenon maydate back at least as far as the 1800s (reviewed in Harwoodand Hall 1990). Such high-profile events have been observedand described by naturalists in the past back to Aristotle, butit appears that unusual mortality events have become more

frequent worldwide, particularly in the late twentieth andearly twenty-first centuries. Certainly, interest in the popu-lation and genetic effects of disease on particular marinemammal species has increased since the large die-offs of har-bor seals and bottlenose dolphins in the late 1980s. This canbe seen in Figure 4.3a, where the papers on mass mortality,compared with studies on individually stranded animals,peak in the early 1990s. Many studies of die-offs that haveoccurred since the late 1990s have not yet been published,so the recent decrease indicated in the figure may not signala declining trend in the longer term.

Disease Sampling Strategies

Using the same literature database, we reviewed the differ-ent scientific approaches that have been used. Most studieshave focused on individuals, and 15% of the publications inthe database were case studies reporting disease in a singleanimal. Few studies have included sufficient numbers of in-dividuals to support inferences at the population level ex-cept in the case of mass mortalities.

Role of Infectious Disease 55

Fig. 4.2. Proportion of disease-related paperspublished each year, classified by pathogen.

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56

Fig. 4.3. Proportion of disease-related paperspublished each year, classified by samplesource.

Host populations can be sampled by examining stranded,harvested, bycaught, captive, or live-captured-and-releasedanimals. Figure 4.3a,b show the trends in each of these sam-pling methods. Studies using harvested and captive animalshave declined steadily. Interestingly, the number of studieson wild or live-captured-and-released animals has declinedslightly. Studies dependent entirely on animals bycaught infishing nets did not begin to appear until the late 1990s. Thisconclusion, however, is biased, as studies of “stranded” an-imals sometimes include bycaught animals as well as thosefound washed ashore from natural causes.

Increased concern for animal welfare throughout muchof the world has led to many live-stranded animals beingtaken into captivity for rehabilitation. This in turn has led tothe development of centers specifically designed to treatand release animals back into the wild. Such rehabilitationefforts have had important implications for the study of ma-rine mammal disease. Figure 4.4 shows how studies using

these animals have been reported in the literature, with nopapers before 1985. Although rehabilitated individuals are abiased sample of their populations and only include morbidanimals that were salvaged for rehabilitation, they clearlyprovide a significant sampling route for the study of marinemammal disease.

Each sampling method has advantages and limitationsand these are reviewed later in the chapter.

STRANDED ANIMALS AND MASS MORTALITIES.Stranded animals are a useful source of information on dis-eases in marine mammals. As can be seen in Figure 4.3, theyprovided the basis for the largest proportion, 53%, of the papers reviewed. A number of infectious agents in marinemammals were first identified in stranded animals, afterwhich their presence in the free-ranging population was con-firmed. These include PDV, which caused the deaths of morethan 18,000 harbor seals in Europe in 1988 and more than

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20,000 in 2002 (Osterhaus and Vedder 1988, Jensen et al.2002), phocine herpes virus (PhHV1) isolated from strandedharbor seals in 1985 (Osterhaus et al. 1985), and Brucellamaritimus in a variety of species (Garner et al. 1997).

Stranded animals can also be sampled to quantify contam-inant levels in tissues, and they can alert us to diseases that arepresent in the more inaccessible wild animals but would bedifficult to detect by random sampling. For example, 17% ofthe sexually mature California sea lions that stranded anddied along the northern coast of California showed neoplasiawhen examined postmortem (Gulland et al. 1996). In com-parison, only one case of neoplasia has been observed in Cal-ifornia sea lions at rookeries on San Miguel Island, wherethere are more than 100,000 of these animals (T. Spraker pers.comm.). Neoplasia pathogenesis is thus more readily studiedwith stranded sea lions than with those at rookeries, andstranded animals essentially serve as sentinels for their wildcounterparts. Stranded animals do not constitute an idealsentinel system, however, as they do not represent the entirepopulation (Aguilar and Borrell 1994). Also, samples consist-ing of stranded animals usually have skewed age and sexstructures, and biological data such as individual life histories,feeding habits, reproductive success, or disease progressionare not typically available. Finally, contaminant levels in tis-sues collected from animals found dead may be significantlyaffected by decomposition (Borrell and Aguilar 1990).

It is expected that epidemics, when they occur, cause mor-tality in animals of all ages and leave survivors that generatean immune response to the agent concerned (Heesterbeekand Roberts 1995). Often a proportion of the carcasses washashore, but this may not always be the case; in areas of lowhuman population densities and convoluted coastlines,those that do come ashore may not always be found and re-ported. Alternative methods for retrospective detection ofthe infectious agent that caused an epidemic are to test sur-vivors for antibodies or to examine animals susceptible to thesame diseases that share habitat with the species in question.For example, distemper antibodies were found in domesticdogs in areas surrounding African wild dog (Lycaon pictus)

habitat in Kenya. These wild dog packs disappeared, leadingto the conclusion that the wild dogs died from distemper al-though no carcasses were found (Alexander and Appel 1994).

Stranded animals, whether alive or dead, can be used todetect disease, but their usefulness is limited when the ob-jective is to assess the prevalence of a disease and its impacton a host population. As noted earlier, stranded-animal sam-ples are skewed toward those carcasses that are likely towash ashore. Decomposition is a problem for obtaining ac-curate diagnoses and good histology from dead strandedanimals, while human concern and intervention can inter-fere with research on live stranded animals.

HARVESTED ANIMALS. Disease occurrence in har-vested animals has been considered in the past but thissource of material has contributed to only a small propor-tion of the studies reviewed (9%). The sample taken is oftenskewed and not representative of the population (oftenpups or juveniles are overrepresented and, in the case ofcommercial whaling, adults may be overrepresented; e.g.,Lambertson 1986, 1992). The number and geographical dis-tribution of species that can be studied in this way are alsolimited. However, studies of harvested animals can be verygood for indicating the prevalence of infection using sero-logical, molecular, and histological methods.

CAPTIVE ANIMALS. Up to the mid-1980s, disease amongcaptive animals was well reported. However, with the de-cline in the number of display facilities maintaining live ma-rine mammals, there has been a decline in information fromthis source. There are also major limitations when studyingdisease in captive animals and making inferences aboutthose in the wild. Studies generally report single cases whereintervention and treatment make it difficult to interpret thenatural course of any disease. Many captive animals arekept in unnatural environments together with other speciesthat they would not normally encounter and are also fed un-natural diets, so the stress in such situations might exacer-bate any disease states.

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Fig. 4.4. Proportion of disease-related paperspublished each year on live-stranded animals.

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LIVE-CAPTURED-AND-RELEASED ANIMALS. Carry-ing out studies on free-living individuals that are captured,sampled, and released within a short time frame has its ownlimitations. Apart from being expensive, it is often stressfulfor the animals, particularly if chase/capture scenarios areinvolved, which can confound the results obtained. Suchstudies are often logistically difficult to execute, yield rela-tively small sample sizes, and are limited in the species thatare amenable to being sampled (pinnipeds and some smallcetaceans). Again, the sample obtained may be skewed andlimited in season. However, some unique long-term, longi-tudinal studies (such as on the Sarasota Bay bottlenose dol-phins; Wells et al. 1987) are akin to cohort studies in humanepidemiology, which is currently the most powerful studydesign in which to investigate the prevalence and impact ofdisease on a population (Rothman 1986).

BYCAUGHT ANIMALS. Disease studies using only by-caught animals are rare, other than studies on dolphinstaken in the eastern tropical Pacific tuna industry. Many in-dividuals accidentally caught in fishing nets are removedand discarded; they may later wash ashore and be reportedas strandings. The main limitations of bycaught samples arethat the number of species that can be sampled is limited,only small numbers are usually obtained, and samples areoften not representative of the population. Because entan-glement is generally fatal, the types of studies that can becarried out are limited to those that involve dead animals.Nevertheless, bycatch provides opportunities for some use-ful research regarding disease prevalence, and it can providecontrols for other disease studies.

LICENSED EXPERIMENTAL RESEARCH FACILITIES.Relatively few research facilities throughout the world arelicensed within their country to keep marine mammals incaptivity for short periods of time for research purposes.Whereas most studies carried out in such facilities addressquestions of basic physiology, some disease studies havealso been conducted (Harder et al. 1992, De Swart et al.1994). Research into health status and immune function us-ing these semiexperimental systems could help fill some ofthe gaps in knowledge, although it would be limited inscope (e.g., age, gender, species) and applicability.

Each of the sampling sources described previously hasadvantages and disadvantages, so that the choice of methodmay depend on the questions being addressed as much ason the logistical difficulties involved in sampling animals us-ing the different methods. For example, if the objective of astudy is to detect a particular disease within a population,then stranded animals might be the best sources. However,if the aim is to determine the point or period prevalence ofa disease, live-captured or bycaught animals would probablybe more suitable. The latter are also likely to be the most ap-propriate sources when a random sample of controls is re-quired from a population. Most work on diseases of marinemammals to date has been opportunistic, taking advantageof animals available from a variety of sources. To develop

clean hypothesis testing and clarify some of the importantinteractions between infectious agents and other factors, in-creased use of experimental facilities with clearly designedstudies is needed.

Review of the Disease Literature

Table 4.2 identifies the different types of studies that havebeen reported in the literature surveyed. These have beencategorized into broad classes that reflect the main methodused in the paper to detect, diagnose, investigate, or modelthe disease agent or process being studied. Because many ofthe studies used multiple methods, they are given in thetable as the total number of papers using each method type,by 3-year classes.

As can be seen, most publications include informationabout the pathology and clinical signs of the disease, withsome histology and virology reported, particularly in the1990s. Very few papers have included epidemiology ormathematical modeling, and recent advances in moleculartechniques only begin to appear in the late 1990s and early2000s. Interestingly, there are still few published studies ofhost genetics and immune function and even fewer that em-ploy or describe new diagnostic methods.

Table 4.3 shows the number of papers by species. Thevast majority of studies have been carried out on the harborseal, with the bottlenose dolphin the most commonly stud-ied cetacean. This probably reflects the relative abundanceand nearshore distribution of these two species and the factthat bottlenose dolphins have often been kept in captive dis-play facilities where case studies have been carried out. Har-bor seals can also be studied in captivity and have been sub-ject to mass mortalities in recent years; harbor porpoises,which also are high on the list, are often subject to strand-ing or bycatch. Interestingly, the distribution is about equalbetween seals and cetaceans, but it is clear that almost noth-ing has been reported about diseases in some species.

KEY ISSUES AND RECOMMENDEDFUTURE RESEARCH

There is a lack of essential information needed to predictand prevent diseases that negatively impact marine mam-mal populations. Our understanding of diseases in marinemammals is poor compared to our knowledge of suchprocesses in terrestrial animals. This is due to a lack of re-sources to routinely analyze and interpret disease in ma-rine mammals, as well as to logistic difficulties that havehampered opportunistic investigations to date. As a result,we still do not know which diseases are normal compo-nents of a healthy marine ecosystem and which are noveland a consequence of anthropogenic factors. We also donot know if there is a real increase in diseases in marinemammals, nor do we know how to control or prevent thesediseases. To overcome these hurdles, we have to invest inan infrastructure that will change how we study diseases in

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marine mammals. The designation of a specialized marinemammal disease laboratory as a centralized resourcewould allow for diagnosis and pathogenesis research (aschematic diagram of how such a system would addressvarious questions in this field is shown in Figure 4.5). Sam-ples could be screened against a standard panel of diseases,and collaborations would be encouraged to investigateemerging and previously unstudied pathogens. Data andsamples could be made available for collaborative research.Such an approach requires a long-term commitment,transgenerational studies, longitudinal studies, and base-line monitoring, all necessary elements to determine thetrue impact of disease on marine mammal population.

Key Issues

1. Multidisciplinary approaches are currently rare.2. There are few laboratories with expertise and resources

to analyze samples specifically from marine mammals.3. There are few statisticians with appropriate expertise

and there is a severe lack of good experimental design.

4. Measuring disease or changes in disease in free-ranginganimals in a marine system is logistically difficult.

Future Research Areas

1. Standardize data collection and integrate disease datacollection with other marine mammal population datato develop baseline information. This is needed to givea solid baseline with high-quality accessible data on theidentity of endemic diseases and their effects in marinemammals.• Develop a centralized marine mammal diagnostic

laboratory: (a) Develop reagents that function acrossspecies (e.g., biomarkers, monoclonal and polyclonalantibodies, primers); (b) develop culture techniquesfor infectious agents, including viruses, bacteria andrickettsia; (c) standardize serology tests for diseases inmarine mammals; (d) improve field methods (e.g.,RNA preservation media such as “RNA Later”) thatallow the use of molecular techniques (e.g., for RT-PCR and viral DNA/RNA detection).

Role of Infectious Disease 59

Table 4.2 Number of Papers Categorized by Type of Study (Discipline) and Year

Pathology/Year clinicalGroup Serology Bacteriology Immunology Virology Histology signs

1966 1 1 0 0 0 41969 1 1 0 0 2 61972 2 3 1 1 1 91975 1 5 1 3 4 71978 2 3 0 10 6 181981 0 3 0 9 0 61984 1 3 1 7 3 91987 8 6 2 6 4 201990 12 11 3 27 19 321993 8 11 4 24 17 231996 10 18 2 15 12 281999 12 22 9 15 21 452002 7 2 1 3 7 10

Epidemiology/ NewYear Hematology/ Vaccine mathematical diagnostic HostGroup Molecular biochemistry development modeling methods genetics

1966 0 0 0 0 1 01969 0 0 1 0 0 01972 0 0 0 0 0 01975 0 0 0 0 1 01978 0 1 0 0 0 11981 0 1 0 0 0 01984 0 0 0 0 0 01987 0 2 2 2 0 01990 8 1 2 8 3 11993 13 0 0 1 8 01996 19 2 0 4 1 01999 26 1 2 2 9 02002 6 1 0 0 0 0

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Table 4.3 Study Species Reported in Papers Reviewed

Species 1–5 6–10 11–30 31–50 >50

Antarctic phocids xArctocephalus australis gracilis South American fur seal xArctocephalus forsteri New Zealand fur seal xArctocephalus pusillus doriferus Australian fur seal xArctocephalus pusillus pusillus South African fur seal xArctocephalus townsendi Guadalupe fur seal xArctocephalus tropicalis Antarctic fur seal xBalaena mysticetus Bowhead whale xBalaenoptera acutorostrata Minke whale xBalaenoptera borealis Sei whale xBalaenoptera musculus Blue whale xBalaenoptera physalus Fin whale xCallorhinus ursinus Northern fur seal xCystophora cristata Hooded seal xDelphinapterus leucas Beluga xDelphinus delphis Common dolphin xEnhydra lutris Sea otter xErignathus barbatus barbatus Bearded seal xEschrichtius robustus Gray whale xEumetopias jubatus Steller sea lion xGlobicephala melaena Long-finned pilot whale xGrampus griseus Risso’s dolphin xHalichoerus grypus Gray seal xHydrurga leptonyx Leopard seal xInia geoffrensis Boto xKogia breviceps Pygmy sperm whale xLagenorhynchus acutus White-sided dolphin xLagenorhynchus albirostris White-beaked dolphin xLagenorhynchus obliquidens Pacific white-sided dolphin xLissodelphis borealis Northern right whale xLobodon carcinophagus Crabeater seal xMegaptera novaengliae Humpback whale xMirounga angustirostris Northern elephant seal xMirounga leonina Southern elephant seal xMonachus schauinslandi Monk seal xNeophoca cinerea Australian sea lion xNeophocaena phocaenoides Finless porpoise xObobenus rosmarus divergens Pacific walrus xObobenus rosmarus rosmarus Atlantic walrus xOrcinus orca Killer whale xOtaria byronia Southern sea lion xPhoca caspica Caspian seal xPhoca groenlandica Harp seal xPhoca hispida hispida Ringed seal xPhoca sibirica Baikal seal xPhoca vitulina Harbor seal xPhocarctos hookeri Hooker’s sea lion xPhocoena phocoena Harbor porpoise xPhoecoena spinipinnis Burmeister’s porpoise xPhyster macrocephalus Sperm whale xPlatanista gangetica Ganges river dolphin xSousa chinensis Indo-Pacific humpback dolphin xStenella attenuata Pantropical spotted dolphin xStenella coeruleoalba Striped dolphin xTrichechus manatus latirostris Florida manatee xTursiops truncatus Common bottlenose dolphin xZalophus californianus California sea lion x

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• Standardize and centralize collection of additional ma-rine mammal disease and population data (e.g., serol-ogy data, bacterial culture data, parasite identification).

• Provide routine training to relevant sites regardingstandardized data collection, reporting, and epidemi-ological analysis.

• Thoroughly analyze and report the National Oceanicand Atmospheric Administration’s (NOAA) MarineMammal Health and Stranding Program Level A ret-rospective data.

2. Identify unusual disease outbreaks. This is needed toidentify epidemic and novel diseases that can reducesurvival of marine mammals.• Enable rapid reporting of NOAA’s Level A data to the

centralized database; ensure that current data areroutinely reported to target audiences.

• Develop a rapid-response team with skills to diagnosedisease and conduct epidemiological investigation.

• Develop multidisciplinary teams to identify factorsleading to disease outbreaks.

3. Identify risk factors and evaluate interventions. This isneeded to be able to control diseases and factors precip-itating them in marine mammals.• Support for multidisciplinary teams that can priori-

tize case-control and cohort studies related to abnor-mal disease processes and interventions.

• Establish the nature of the interactions among disease, immunity, and nutrition by experimental and field studies using robust epidemiological studydesigns.

• Develop a standardized, centralized marine mammalpopulation database that is linkable to outside envi-ronmental databases (e.g., water temperature, salin-ity, harmful algal blooms).

4. Determine associations between health effects and pop-ulation parameters, especially in regard to nonfatal dis-eases currently largely ignored. This is needed to deter-mine the impact of diseases on populations of marinemammals, and thus the significance of disease in con-servation and management of marine systems.

Role of Infectious Disease 61

MATHEMATICAL MODELS FORPREDICTION AND RISK ASSESSMENT

STRESS, CONTAMINANTEXPOSURE, NUTRITION

INDIVIDUALPOPULATION

Treatment

Prevention: Vaccinationand deworming inendangered /smallpopulations

IMMUNE SYSTEM (ecologicalimmunology—comparative immunology,seasonal patterns in immunity,immunogenetics, etc.)

Nonfatal diseasesFatal diseases

Routine samplesfrom dead animals

Routine samplesfrom live animals

Cycles ofdisease

MOLECULAR STUDIES(e.g., RNA for genomicapproaches)

EPIDEMIOLOGICAL STUDIES (factors/causes ofdisease—primary and secondary pathogens,macroparasites, contaminants, sex, age, season,transmission probabilities, density, movements, etc.)

META-ANALYSIS (combinations of data from manydifferent studies and populations—increase power)

GENETICS—markers for“fitness” anddiseasesusceptibility

New reagents and methodsfor disease detection

Research Service

Diagnostic Service

Fig. 4.5. Schematic diagram suggesting how a specialized marine mammal disease laboratory could be used to address questions involving marinemammal disease.

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