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Human Influences on Wildlife Disease Scott D. Fitzgerald, DVM, PhD, Diplomate ACVP, ACPV Department of Pathobiology & Diagnostic Investigation, and the Diagnostic Center for Population & Animal Health, Michigan State University, East Lansing, MI Human influences on the progression of wildlife disease are unfortunately overwhelmingly on the negative side, leading to increased disease, geographic spread, introduction of diseases to new host species, decreasing the general wildlife population’s health and vigor, and promoting new emerging disease conditions. Disease at the Interface: The interface refers to the interaction, close association of wildlife species, domestic species, and the human species. Unfortunately, the interface area is always expanding due to human encroachment, poor biosecurity, habitat destruction, deforestation, urbanization, habitat fragmentation, animal relocation, etc. Diseases at the interface tend to be zoonotic, emerging, spreading, and frequently epizootic. Basic Principals of Human Influence on Wildlife Disease: Noninfectious agents -Release of man-made biocides & toxins: insecticides, herbicides, pesticides, PFOS, AA -Move, concentrate, & release of natural toxicants: heavy metals, halides, petroleum -Alteration of bodies of water increasing growth of natural toxins: cyanobacteria, domoic acid, botulism, Avian Vacuolar Myelinopathy -Mycotoxin growth on agricultural crops: secondary poisoning of wildlife -Acidification of water/rain: altered mineral availability Infectious agents: -Intentional translocation of agents: Myxomatosis, Rabbit Hemorrhagic Disease -Accidental translocation of agents: Fascioloides, Elaphostrongylus, rabies, WNV, CWD, Monkey Pox -Accidental discharge of agents into environment: E. coli, Vibrio, cryptosporidia -Introduce new disease vectors: Mosquitoes, ticks -Introduce new intermediate hosts: voles, brushtail possum -Artificial wildlife concentration: tuberculosis, brucellosis, finch conjunctivitis Diseases of high density in captive populations: Johne’s disease -Translocation susceptible hosts into endemic area: Whooping cranes, meningeal worm -Habitat change: forcing contact between domestic & wildlife, altering balance species: Canine Distemper in lions, Nipah virus, Hendra virus -Humans as disease reservoir for wildlife: Human tuberculosis to elephants and mongooses, measles to primates, Staphylococcus to eagles Toward an Improved Definition of Emerging Disease Approximately 80% of emerging diseases are zoonotic, transmissible between humans and animals. The Centers for Disease Control (CDC) provide a definition of emerging disease for use in human medicine, however, as veterinarians/comparative pathologists/wildlife biologists we would like to develop a more broad definition for our use. Category Host species CDC- Human Use Humans only Disease agent Infectious agents Time span Evidence of emergence 2 plus decades Significant increase in disease prevalence Health effect Significant morbidty +/mortality Veterinary Use All vertebrate & invertebrate animals Infectious, toxic & environmental diseases 2 plus years Increase in prevalence, spread to new host species, spread to new geographic region Significant morbidity +/mortality Specific Disease Examples Man-made Biocides & Toxins: 1) DDT in wild birds: This insecticide, Dichloro-diphenyl-trichlorotethane, is familiar to everyone, from its initial implication in massive bird population declines in Rachel Carson’s book Silent Spring in 1961. Originally developed in the ‘40s, used extensively in the ‘50s and ‘60s in the war against malaria, credited with saving over 500 million human lives in 2 decades. It was subsequently implicated in the population declines of the bald eagle, peregrine falcon, and brown pelican, due to decrease egg-shell thickness, decreased hatch rates, and possible carcinogenesis, and banned by the EPA in 1972. However, most research studies have failed to show any correlation with egg-shell thickness and DDT levels, the population declines have been questioned, and in general DDT is now generally thought to be a minor cause of bird population declines. 2) PFOS in fish, birds, & mammals: This supposedly inert agent, perfluorooctane sulfonate, has been widely used in Scothgard fabric protection, foam fire retardants, pesticides, and even microwave popcorn. Its manufacture has been largely decreased since 2002, but it has proven to have long term environmental persistence, bioaccumulation, and toxicity. It has been detected worldwide, in Artic polar bears, pelagic albatross, dolphins, seals, fish, etc. Its toxicity has been studied primarily in fish and fish-eating birds and mammals, and appears to have estrogenic-like activity and relate to decreased reproductive function. 3) PTFE in birds: This agent commonly used in cooking pans and utensils is formed when Teflon coatings are overheated, resulting in the gaseous release of polytetrafluoroethylene. Pet birds are extremely sensitive and die of respiratory distress and pulmonary edema. Unfortunately, regular release occurs in the vicinity of manufacturing plants, resulting in die-offs of various wild passerines. Concentration & Release of Natural Toxicants: 4) Mining, excavation, and petroleum drilling and transportation: Harvesting of natural mineral resources frequently results in toxic exposure of wildlife. Leeching of water with heavy metals such as lead from active or inactive mines, the use of mercury in gold sluicing resulting in ground or water contamination, mining for toxic halides such as fluoride, and the drilling of, distillation, and transport of petroleum products including oil through pipelines or tankers may all result in spills and wildlife exposures. Certainly everyone is well familiar with major oil spills from sea-faring tankers and its results on waterfowl, sea otters, and aquatic organisms. The oil destroys the natural buoyancy and water-repellant nature of feathers, its ingestion during preening leads to gastro-intestinal upsets and inappetance, hypothermia, etc. 5) Release of natural toxic materials: The widespread use of lead shot in hunting, and lead sinkers in fishing has resulted in massive contamination of marshes, ponds, lakes, etc. throughout North America. Secondary ingestion by waterfowl such as dabbling ducks leads to chronic emaciation, gizzard erosions, bile stasis, anemia, weakness, paralysis and death. The use of lead shot has been banned in USA since 1991, decreasing lead poisoning in waterfowl by an estimated 78%, but massive contamination persists in many areas. Eutrophication of water causing increased natural toxins 6) Stagnant warm water increases Clostridium botulinum toxicity: As shallow water pools stagnant and heat up in warm weather, with streams diverted, and run-off of rain water disrupted by agricultural and suburban practices, waterfowl are concentrated in higher density by marsh drainage, and dead carcasses increase by disease and hunting, an environment favorable to Cl. botulinum spore development. More carcasses, greater numbers of infectious spores, maggots on carcasses concentrate the spores, and attract live birds to feed on these maggots, resulting in increased numbers of birds poisoned by Cl. botulinum. Classically, botulism results in flaccid paralysis of the legs, wings, eventually neck and head, leading to drowning, or inability to escape predation or ingest food. 7) Man-made artificial lakes leading to the AVM: Avian Vacuolar Myelinopathy is a toxic disorder associated with both seasonality (fall/winter), man-made bodies of water, an unknown toxin present in hydrilla water plant, and high mortality in waterfowl such as coots. In addition, the toxin remains in the ingested bird, so secondary intoxication of eagles and other raptors also occurs. The affected birds become uncoordinated, swim in circles, and cannot fly. There are no gross lesions, but microscopically there is edema of the white matter myelin within the cerebellum and optic areas, due to splitting and edema of the myelin sheaths ultrastructurally. Acidification of water & rain Infectious Agents Intentional Translocation of Infectious Agents 8) Myxomatosis in Australia: Rabbits were introduced to Australia in 1859 for hunting; subsequently over ran the continent due to lack of predator control, destroying crops and damaging the environment. Rabbit Myxomatosis was intentionally released in 1950 to control the rabbit population explosion. The disease wiped out 99% of an estimated 600 million rabbits in 2 years time, allowing for improved crop yields, and increased wool and meat production. Within 10 years, widespread resistance was developing in the remaining rabbit population, which has subsequently increased, but never to the pre-Myxomatosis levels. 9) Rabbit Hemorrhagic Disease in New Zealand: Similar massive populations of introduced rabbits occurred in New Zealand. The farmers and public demanded a biologic control be utilized as in Australia, and RHD was investigated, but the Ministry of Agriculture decided not to allow importation and release of the calicivirus. Within a month persons unknown had illegally imported and released RHD and started a massive rabbit die-off in NZ. While the government tried to stop the RHD disease spread, farmers mixed viscera from dead rabbits in kitchen blenders and spread the disease in their vegetable patches to further disseminate the disease. Deaths occur quickly with bleeding from the nose and mouth, and disseminated hepatic necrosis. Since 1997 rabbits have developed some immunity, population numbers are increasing, but sequential waves of mortality still spread throughout the wild rabbit populations. Accidental Translocation of Infectious Agents 10) Elaphostrongylus rangiferi into Newfoundland: This extra-pulmonary lungworm has long been endemic in reindeer in northern Sweden, Finland, Norway, and Russia. It was accidentally translocated to Newfoundland, Canada, in infested reindeer from Norway in 1908. These captive reindeer escaped into the wild, and co-habitation with native reindeer led to its spread. This disease may result in pneumonia in severe infestations, as well as the brain and spinal cord resulting weakness, head tilt, incoordination, ataxia and paralysis. Snails and slugs are important intermediate hosts. 11) Rabies Epidemic in Eastern USA Raccoons: Various strains of rabies have been endemic in specific wildlife species in various geographic regions of North America for many decades. Heavy vaccination of the domestic dog & cat populations have served as a buffer to rabid wildlife and so rabies cases have steadily dropped in prevalence over the last 50 years. However, beginning in 1978 a number of rabid wild raccoons were translocated for hunting purposes from Florida and Georgia to Virginia, setting off a major raccoon epidemic which has raged over the Eastern half of the US for the last 30 years. Now the entire Eastern coast, and inland states such as Pennsylvania, Tennesee, Eastern Ohio, Alabama, Vermont and West Virginia suffer from endemic raccoon rabies. Only development of an effective oral vaccine broadcast in bait prevents further spread of the disease. 12) West Nile Virus introduction to North America: West Nile virus entered New York City in 1998 by way of unknown transcontinental traveler. It may have been a swarm of infected mosquitoes in the wheel bay of an airplane from Asia, or a handful of infected stow-away birds in the hold of a transport ship from Europe or Africa, we will never know. However, in 7 short years the virus has traversed the North American continent to become an endemic disease which has killed millions of corvids, thousands of horses, hundreds of humans, and found dozens of new mosquito hosts and been reported in 138 bird species, and dozens of mammalian and reptilian wildlife species. Accidental Discharge of agents into the Environment 13) Waste Effluent into the Oceans- Treated human and animal sewage is discharged by the tons daily into rivers, lakes, and directly into the ocean. While treated to varying degrees, this effluent is certainly not sterile. Surveys have found marked elevations of E. coli, various Vibrio species including V. cholera and V. parahemolytica, and Cryptosporidium in fish, shrimp, bi-valves, and in our rapidly declining coral reefs. Introduction of New Disease Vectors 14) Introduction of Mosquitoes to Hawaii: The threatened, endangered, and extinct Hawaiian Forest Birds are an excellent example of so many different human influences. These include massive deforestation of the Hawaiian Islands, introduction of all manner of pest species including dogs, cats, rats, snakes, goats, as well as many exotic bird species able to out-compete the endemic species. However, accidental introduction of mosquitoes carrying avian malaria, and avian pox viruses, are two recent pressures with interesting effects. The pressure exerted by malaria parasites and pox viruses cause high morbidity and mortality in Forest birds at low elevations, with mosquitoes serving as the vector for both disease agents. As mosquito species are more numerous around water at lower elevations, the healthier and better reproductive populations of endemic Forest birds have been forced into higher elevations (above 1200 m) on the volcanic mountains, but of course still within the forested regions. Introduction of New Intermediate Hosts 15) Introduction of the Brushtail Possum to New Zealand: It seemed like a good idea at the time. Brushtail possums were intentionally introduced to New Zealand from Australia in the 1850’s to serve as the basis for a fur industry. With no natural predators and an ideal environment their population exploded to between 60-70 million animals, covering 95 percent of the the islands, at densities up to 20 times that found in their native Australian forests. These aggressive invaders have had devastating effects on native bird life, particularly the endangered kiwis, massive damage to the native vegetation, and they are the number one wildlife reservoir for bovine tuberculosis, which is now widespread in cattle and deer populations. For the last 20 years tens of millions of dollars have been spent annually on poisoning and trapping possums to help control tuberculosis. And virtually nobody uses them for fur anymore. Artificial Wildlife Concentration 16) Bovine Tuberculosis in MI Deer: Starting 1917 the USDA began a nationwide effort to eradicate bovine tuberculosis in the USA. Unfortunately, bovine tuberculosis has a wide host range, including humans and white-tailed deer. The disease spilled from domestic cattle into the wild deer populations during the first half of the 20th century, and was discovered at an endemic prevalence rate of 45% in the northeastern corner of the lower peninsula of Michigan. For the last dozen years, many millions of dollars have been spent annually on wild deer surveillance, as well as domestic cattle surveillance and culling towards eradication. The common habit of supplemental feeding and baiting of wild deer, to grow bigger sport bucks and increase hunting efficiency have contributed significantly to the continuance of tuberculosis in wild deer populations. 17) Mycoplasma Conjunctivitis in Wild Finches: Mycoplasma gallisepticum is a respiratory pathogen of domestic fowl. In the Washington D.C-VirginiaMaryland area in late 1994 bird enthusiasts reported seeing growing numbers of finches (purple, house, gold) with periorbital swelling, and ocular discharge. Thirteen years later the disease has spread all the way to the West Coast, helped in large measure by the close aggregation of birds present at feeding stations. Salmonella in wild birds is similarly aided by this un-natural high density feeding congregations. Translocation of Susceptible Hosts into an Endemic Disease Area 18) Whooping Cranes introduced into EEE endemic area: Patuxent Wildlife Research Center has long served as an alternate breeding site to try and aid the survival of the endangered Whooping Crane. This goal is reached by foster rearing the endangered chicks with the common Sandhill Crane, and establish an alternate flock and migration path in case of natural disaster wiping out the small remaining flock at Port Aransas, Texas. The problem is that Eastern Equine Encephalitis is endemic in Maryland, and young Whooping Cranes are relatively susceptible to the disease which is generally subclinical in Sandhill Cranes. Sudden death without premonitory signs, to lethargy, ataxia and widespread necrosis and visceral gout accompanied infections by EEE. In 1984 nearly 20 percent mortality was associated with EEE infection. Since then, the use of equine vaccines against EEE has helped hold the disease in check. Habitat Change leading to contact between Domestic & Wildlife Species 19) Hendra Virus in Australia: As humans continue to spread their farms, ranches, suburbs, etc. into ever more remote areas, we are stimulating more interactions between wildlife, domestic animals and humans (that interface again). This interaction led to severe disease and death of a prominent horse trainer and 14 of his horses in Queensland, Australia in 1994. Scientists found a previously unknown paramyxovirus, first called equine morbillivirus but now named Hendra virus. This virus remains subclinical in various Australian fruit bats and flying foxes, but when horses, humans, or cats are exposed to urine, or reproductive fluids from these bats, high mortality may result. 20) Canine Distemper in Serengeti Lion Population: Another interface issue. Humans have segregated the wildlife into a National Park, and built houses right up to the park borders. Many households have domestic dogs, which run free, and are unvaccinated for Canine Distemper. These dogs interact with the jackals and African wild dogs, which associate around the lion kills, and spread domestic distemper to the lions. Paramyxoviridae (canine distemper, phocine distemper, Hendra virus) and Orthomyxoviridae (human influenza, swine influenza, equine influenza, avian influenza) seem particularly able to jump into new host species and create new emerging disease conditions. In 1994 and subsequent years a major epidemic, killing 30-40% of the lion population, and characterized by pneumonia, seizures, myotonia, etc. Since that time, pharmaceutical companies have donated large numbers of free vaccines to prevent the distemper in domestic dogs and reduce the spill-over into the wildlife. Humans as Disease Reservoirs for Wildlife Species These are just a few examples to illustrate the many varied ways that human actions can influence and contribute to disease problems in wildlife populations. General References 1) Samuel WM, Pybus MJ, Kocan AA. Parasitic Diseases of Wild Mammals, 2nd ed. Ames, IA: Iowa State University Press, pp. 1-559, 2001. 2) Williams ES, Barker IK. Infectious Diseases of Wild Mammals, 3rd ed. Ames, IA: Iowa State University Press, pp. 1-558, 2001. 3) Wobeser, GA. Essentials of Disease in Wild Animals. Ames, Iowa: Blackwell Publishing, pp. 1-243, 2006.