YS 24-1 Infectious Diseases of Wolves in Yellowstone

Infectious Diseases of Wolves in Yellowstone

by Emily S. Almberg, Paul C. Cross, Peter J. Hudson, Andrew P. Dobson, Douglas W. Smith, & Daniel R. Stahler

The summer of 2005 began with such promise for wolves in Yellowstone. The population had been at an all-time high the last few years, and the wolves appeared to be in good condition. Several packs had been particularly busy during the breeding season, and early summer pup counts suggested another healthy crop of new wolves rising through the ranks.

And then something changed.

While monitoring dens to count pups, we noticed huge declines in pup numbers. The Slough Creek pack started out with 18 pups among three litters; by August, these numbers had declined to three lethargic pups. Similar things were happening across the northern portion of the park. We were soon looking at the worst pup survival rates since wolf reintroduction; by the end 2005, total wolf population numbers in the park had dropped by over 30%. That was the summer we came to understand the importance of infectious diseases for wolves in Yellowstone.

Parasites and pathogens are often overlooked in studies of wild populations. This is due, in part, to the logistical issues of studying disease impacts; often there are few outward signs of illness, bodies are seldom recovered soon enough for disease tests, and the proximate cause of death (e.g., injuries from other wolves) are often more obvious than a predisposing illness. As a result, viruses, bacteria, worms, and mites were historically perceived as factors that only impacted weak individuals or randomly caused outbreaks in overly-dense populations. This perception may have been reinforced by the history of over-hunting that reduced wildlife populations to low densities with reduced rates of disease transmission, leading us to forget or underestimate the ability of disease to cause significant amounts of mortality.

Following the summer of 2005, the Yellowstone Wolf Project expanded its monitoring efforts to include parasites and pathogens to better understand the cause of poor pup survival in 2006 and the overall health of wolves. That winter, the Wolf Project collected blood serum, as they always do, during their annual capture and radio-collaring efforts. Blood serum contains a record of many of the pathogens the animal has been exposed to over the course of its life. When we analyzed the serum, the results were clear: wolves in Yellowstone had just experienced a massive outbreak of canine distemper virus (CDV; Almberg et al. 2009). CDV is a close relative of measles, and is one of the most significant diseases of domestic dogs and wild carnivores worldwide.

We now know wolves in Yellowstone have experienced three major outbreaks of CDV in 1999, 2005, and 2008 (figure 1); and during these outbreaks many other carnivores, including coyotes, foxes, cougars, black and grizzly bears, and likely badgers, were also infected ("canine" distemper is a misnomer—the virus actually infects a wide range of carnivore species; Almberg et al. 2010). Outbreaks of CDV are particularly lethal for young animals. Wolf pup survival in the northern region of the park during outbreak years was only 23%, as compared to 77% in non-outbreak years. Adults appeared less affected; but among those exposed to CDV for the first time, survival is roughly half of what it is normally. Once an individual survives a CDV infection, it is thought to be immune for life. As a result, it may take several years before an area has enough susceptible individuals to support another outbreak.

We don't know where CDV is circulating during non-outbreak years, but we are fairly certain it is absent from large carnivores in Yellowstone during that time. Previous research suggests it is unlikely that domestic dogs are playing any significant role in the ecology of the virus in the Greater Yellowstone Ecosystem and that it is circulating at a fairly large spatial scale among a variety of other carnivore species (e.g., raccoons, skunks, and coyotes) throughout the region (Almberg et al. 2010). It remains to be seen whether some of the more recent lower densities of wolves will help reduce the frequency and extent of any future outbreaks within the park.

In addition to CDV, there is another parasite that has had measurable impacts on wolves in Yellowstone: the microscopic mite, Sarcoptes scabiei. Introduced as part of predator-eradication efforts in the early 1900s, sarcoptic mange presumably persisted among other furbearing species until reappearing within Yellowstone packs in 2007. The mite burrows into its host's skin, where it causes the infected individual to scratch itself to the point of hair loss (figure 2). These hairless lesions can result in an estimated doubling of energy expenditure to keep warm during winter months (figure 3), decreased body condition, and an increased risk of mortality.

In the first few years after mange was detected among wolves in Yellowstone, the mite successfully spread to nearly all packs in the northern region of the park, and caused fairly prevalent and severe infections (Almberg et al. 2012). Monthly monitoring, in part supported through citizen science efforts (www.yellowstonewolf. org), has shown individuals can recover from infections; but they have no long-term immunity. Individual infections can last anywhere from months to years, and infection waxes and wanes within the population over time and seasons. Furthermore, we now know the impacts of the mite on an individual wolf depend on the context. An infected wolf living in a large, healthy pack survives just as well as an uninfected wolf; however, as pack size decreases or the proportion of infected pack mates increases, infected individuals are much more likely to die (Almberg et al. 2015). We suspect that larger packs with many healthy pack mates are able to offset the effects of the mite by providing food and helping to defend the territory of those that are sick.

Wolves, like all the large mammals in Yellowstone, are infected with a diverse array of pathogens. We know that nearly all wolves in Yellowstone become infected with canine parvovirus, canine adenovirus-1, and canine herpesvirus at some point in their lives. We have also detected canine coronavirus-1, canine adenovirus-2, and Bordetella bronteseptica; but currently we have no estimate of how common these infections are or their impacts (although they can cause severe illness in domestic dogs). Some of the wolves carry Neospora caninium and Echinococcus granulosus, a protozoan parasite and a tapeworm, respectively, that use both wolves (and other canids, including domestic dogs and coyotes) and ungulates to carry out their life cycles.

E. granulosus has been the subject of much controversy and misinformation. There are two "biotypes" of E. granulosus circulating within North America. The northern biotype (strains G8/G10) that circulates among wolves, coyotes, domestic dogs, and wild ungulates is capable of causing an extremely rare and relatively benign, treatable infection in humans through the ingestion of infected canid fecal material (Foreyt et al. 2009). The domestic biotype, which circulates among dogs and domestic ungulates, particularly sheep, occurs throughout the sheep-herding regions of the world and is capable of causing more severe infections in humans (Thompson 2008). All reintroduced wolves were treated to remove parasites including E. granulosus prior to release; and although we lack definitive evidence, E. granulosus was likely present within the Greater Yellowstone Ecosystem prior to wolf reintroduction. The odds of people contracting E. granulosus are extremely low. In fact, to-date, not one wolf biologist ever tested has contracted E. granulosus, despite decades of potential exposures (Mech 2010).

All disease monitoring efforts to-date point to one obvious conclusion: parasites are everywhere! We have only looked for a small fraction of the parasites that are likely circulating, and yet we have ample evidence that wolves in Yellowstone routinely experience many different infections and have steadily acquired a characteristic community of pathogens since their reintroduction. While we have begun to understand the effects of sarcoptic mange, the impacts of other parasites remain unknown. For example, we now know we are more likely to detect viral parasites on dead wolves, regardless of the cause of death, than we are on live wolves sampled during capture. Of course, this information does not tell us whether parasites are just helping to finish off an individual that was already likely to die for other reasons ("compensatory mortality") or whether these parasites are causing extra mortality that we currently fail to measure at the population level. It does point to the distinct possibility that we have consistently underestimated the role of parasites within the ecosystem.

We now recognize infectious diseases, along with prey abundance and social competition, as one of the key factors affecting wolf population dynamics. In addition to continuing to study the impacts of parasites on wolf numbers, we have begun to think about how parasitism of a top predator may have cascading effects through the food chain. For example, in the years of CDV outbreaks, we see higher rates of elk calf recruitment, presumably mediated through lower rates of predation. We have also begun to think about how wolves may be shaping the parasite populations of their prey. Theoretical and empirical work have demonstrated how predators may target infected prey, if the infection makes prey easier to catch. This may have the larger effect of helping to keep prey populations healthy—something to keep in mind as other diseases, such as brucellosis and chronic wasting disease, continue to expand their range within the region.

 
Figure 1
Figure 1. Minimum number of wolves (black) and those infected with sarcoptic mange (blue) in Yellowstone National Park, 1995-2014. Years of canine distemper virus (CDV) outbreaks are marked in red.
 
Figure 2
Figure 2. A wolf pup infected with sarcoptic mange in Yellowstone. The hairless lesions are characteristic of this infection. NPS photo.
 
Figure 3
Figure 3. Thermal cameras have been used to estimate the heat loss associated with mange infections in wolves. This is a thermal image of a wolf in Yellowstone suffering from severe mange, with areas of hair loss illustrated in red. An uninfected wolf would look almost entirely blue. The color bar on the right shows the temperature in degrees Celsius. Photo credit: USGS.
 
Literature Cited

Almberg, E.S., P.C. Cross, A.P. Dobson, D.W. Smith, and P.J. Hudson. 2012. Parasite invasion following host reintroduction: a case study of Yellowstone's wolves. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 367:2840-2851.

Almberg, E.S., P.C. Cross, A.P. Dobson, D.W. Smith, M.C. Metz, D.R. Stahler, and P.J. Hudson. 2015. Social living mitigates the costs of a chronic illness in a cooperative carnivore. Ecology Letters 18:660-667.

Almberg, E.S., P.C. Cross, and D.W. Smith. 2010. Persistence of canine distemper virus in the Greater Yellowstone Ecosystem's carnivore community. Ecological Applications 20:2058-2074.

Almberg, E.S., L.D. Mech, D.W. Smith, J.W. Sheldon, and R.L. Crabtree. 2009. A serological survey of infectious disease in Yellowstone National Park's canid community. PLoS One 4:e7042.

Foreyt, W.J., M.L. Drew, M. Atkinson, and D. McCauley. 2009. Echinococcus granulosus in gray wolves and ungulates in Idaho and Montana, USA. Journal of Wildlife Diseases 45:1208-1212.

Mech, L.D. 2010. Reality check: western wolves and parasites. International Wolf Center. http://howlcolorado.org/2010/03/15/ reality-check-western-wolves-and-parasites/ Thompson, R.C.A. 2008. The taxonomy, phylogeny, and transmission of Echinococcus. Experimental Parasitology 119:439- 446.


Emily Almberg recently completed her PhD at Penn State University studying the dynamics of sarcoptic mange in the wolves of Yellowstone. Currently, Emily is a disease ecologist with Montana Fish, Wildlife and Parks and is working on a range of wildlife health projects statewide.

Last updated: July 6, 2016

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