Disease: A Critical Issue for Urban Wildlife

For a variety of reasons, urban development can lead to increased disease susceptibility for wildlife living near urban centers.  Disease is a central issue in carnivore conservation, and so understanding those factors that increase our local carnivore disease vulnerability is especially important to promoting their conservation.  Locally, biologists are studying disease using a variety of methods, and we are addressing how each of the three factors listed above may interact to increase disease prevalence in local bobcats and mountain lions.  One example of how disease may be the result of interacting consequences of urban development is notoedric mange that we are observing with increased prevalence in bobcats across California.  

Notoedric Mange: A Sentinel for a Big Problem in our Local Ecosystems?

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Notoedric mange is an ectoparasitic disease- a parasite that lives in the skin and/or hair of an animal. The responsible agent for notoedric mange is a microscopic mite (mites are close relatives of spiders and ticks), Notoedres cati.  This tiny insect-like organism is closely related to the mites responsible for dog or human scabies.  Mange causes intense itching and can lead to hair loss and an allergic-like reaction by the skin.  The mites burrow into the skin, creating tunnels where they remain, feeding and reproducing.  They likely consume skin cells, lymph fluids, and perhaps blood, but the exact diet of the mites remains unknown.  It is thought that when an animal has a healthy immune system, the animal infected by notoedric should be able to 'control' the infection, keeping it at subclinical levels where no obvious symptoms of mange are present.  However, if an infected animal is somehow immune compromised (ie., has an immune system weakened due to another disease, stressed by malnutrition, etc.), then the mites will continue to reproduce an invade nearly the entire body of the infected animal.  In this case, hair loss will be extensive across the body of the affected animal, the skin becomes thickened and can even crack and become infected with bacteria.  If the skin has wounds due to the severity of infection, bacteria can enter the bloodstream of the animal and lead to a systemic bacterial infection which weakens the animal further and may even kill the animal. During the course of increasing severity of infection, the affected animal also becomes emaciated and dehydrated.

A photo of B250 on August 27, 2010 when he was humanely captured as part of the bobcat disease susceptibility project through UCLA. He was released on site after samples were collected.

B250 one year after his capture in August 2011. Here he is seen with severe notoedric mange and looks vastly different than the photo taken one year earlier. Despite efforts to capture and treat him, biologists were unable to and he most likely died short after this photo was taken.

How has notoedric mange affected local wildlife?  Notoedric mange is an increasing problem for bobcat populations in California.  Since 2002, a mange epizootic (the animal equivalent of epidemic) has had a significant impact on bobcat populations in the Santa Monica Mountains National Recreation Area (SMMNRA) where National Park Service biologists are conducting a long-term bobcat study.  More than 50% of radio-collared bobcats in the Thousand Oaks area died between 2002 and 2006 because of notoedric mange.  The survival rate for radio-collared bobcats in this region fell from a high of 85% in 1997 when the study began, to a low of 28% in 20033, due to the prevalence and seriousness of notoedric mange for bobcats in this population.  Although it has been a few years since we observed notoedric mange to be a source of mortality for bobcats in the Thousand Oaks population, the population has not rebounded, and there remain fewer bobcats in the area than before 2002.

Notoedric mange is now observed to affect bobcats in other parts of SMMNRA, including around Moorpark, Bel Air, Beverly Hills, Hollywood Hills, Topanga, and a case from Malibu was recently documented.  So, although the Thousand Oaks population seems no longer threatened with this disease, other populations in SMMNRA are threatened.  Further, notoedric mange is now known to affect bobcats in other counties including San Diego, Santa Barabara, Orange County, and even in 4 northern California counties near Cupertino, CA.  

This outbreak of disease is significant and alarming for several reasons.  Until 2002, notoedric mange was never documented to reach epizootic proportions or cause population declines in any species of wild cat worldwide.  In fact, until 2002, notoedric mange was reported only in incidental (ie., one individual) cases for several wild cat species4-9 and so was considered a typically benign disease for wild cats.  Thus, for a disease considered rare and typically benign for wild cats, the question of why and how it is causing population declines in bobcats across at least 7 counties in the State is raised.  We are addressing this important question with our research, and have learned that perhaps there are other underlining factors predisposing bobcats to severe, terminal notoedric mange.  

Mange and Poisons Linked? A Sentinal for a Larger Problem?  In our efforts to understand why bobcats are dying of notoedric mange, we have diligently performed necropsies (the animal equivalent of autopsy) on many bobcats that died of mange.  What we have observed is that a common thread between all the bobcats that die of mange is that they are exposed to anticoagulant rat poisons (see 'Poisons' for more info).  However, the bobcats show no outward signs of anticoagulant rat poison exposure symptoms.  We know they are exposed because we collect liver samples (the poisons accumulate in the liver) and test them for the actual anticoagulant compounds.  What we have noticed is that the bobcats that have died with mange all have concentrations of anticoagulant compounds in their liver, and the level of exposure typically exceeds 0.05 parts per million (ppm) in the liver tissue3,10.  Further, all of these individuals are exposed to more than one of the seven commercially available anticoagulant rat poison compounds available on the market, suggesting that they are chronically exposed to the poisons.  The bottom line is that using our data we have collected since 2002, bobcats are 7 times likely to die of notoedric mange if they are exposed to greater than 0.05ppm of anticoagulant rat poisons.  Further, we have never found a bobcat that died of mange that was not exposed to anticoagulant rat poisons.  We therefore hypothesize that chronic exposure to the anticoagulant poisons decreases the immune competence of the bobcats, making them more susceptible to severe cases of mange.  However, it is important to remember that we have observed no causative link by which this can occur!!!!  In other words, we don't know how anticoagulant exposure could affect the immune system of bobcats such that they are more susceptible to terminal mange.  Further, the poisons do not cause mange!  Rather, the mites cause mange, though perhaps the poisons increase the susceptibility of the bobcats to severe, fatal mange.  This potential link is a core focus of the 'Bobcat Disease Susceptibility' project that Laurel Serieys is working on for her dissertation research.  

Is mange treatable?  This is a common question we biologists studying this issue receive, and the answer is yes!  This is also one of the tragedies to observing animals sick with the disease.  It is highly treatable, particularly before the animal reaches the terminal state.  The progression from first showing symptoms to having severe terminal mange seems to vary for individuals in the length of time it takes to get from one stage to the other.  Further, we have observed some animals to die with what appears to be only mild-moderate mange, while others are able to survive for weeks in what appears a "on death's doorstep" stage.  This variation may be a result of the individual's strength, age, season, or other factors that could affect the progression of the disease in each individual.  However, if we catch the animal in an early enough stage, we can treat with doses of RevolutionTM.  The active ingredient in RevolutionTM is salimectin, and this is perhaps a drug that you have given to your own cat or dog at home for treatment of ticks or fleas.  It is a topical drug that is placed on the skin of the animal between the shoulders.  We have treated several bobcats with this drug, and thanks to a generous donation from Pfizer, we have started giving a prophylactic dose of RevolutionTM to all of our bobcats that we capture during our field research. 

Some have asked why we do not do more to try to capture every bobcat that we learn of that has mange.  There are several reasons why we simply cannot do this.  One is that it is exceedingly difficult to capture affected animals, particularly if the only information we have about them is one person's report of a sighting.  We have learned through extensive experience that when the bobcats are in the severely sick stage, they are nearly impossible to capture in a cage, and thus we must try to capture them using catchpoles- ie., walk up to the animal and use a pole with a wire noose on it to capture the individual.  Imagine if you were tasked with that job!  Where would you start to even look for the animal, let alone, try to get close enough to do that?!  There are rare opportunities for this to occur, and generally the opportunities arise only when a resident or hiker in a park reports the sick individual to us in a timely manner.  However, when it is possible to walk up to the sick bobcat and capture it, 100% of the time, the bobcat is too sick to recover from the mange and dies within 48 hours.  Additionally, if the problem leading to the animal's death is related to anticoagulant exposure, treating and releasing every animal we can does not resolve the precipitating issue.  As researchers and conservation biologists, we are working toward learning about the factors increasing bobcat susceptibility to notoedric mange and hopefully mitigating the circumstances leading to these mass mortalities in bobcats.  Finally, the sad truth is that even if we treat a bobcat for mange, by law, we must release the animal within 3 miles of the capture location.  If anticoagulant exposure is related to increased susceptibility to severe mange, we are simply putting the bobcats back into the area that lead to their sickness to begin with.  We have experienced that one bobcat that had mange that we successfully rehabilitated (and was radio-collared so we could learn its fate after release from the rehabilitation center) died later from mange and was exposed to anticoagulant rat poisons.  Thus, the treatment of every animal with mange is not going to solve the greater problem of mange in bobcats if it is related to anticoagulant rat poisons.   

Is the mange observed in coyotes the same mange affecting bobcats? Notoedric mange is a disease more typically associated with cats, while the closely related, sarcoptic mange mites are more typically associated with dogs.  There are other mange mite species as well, and we have even observed other mite species in our study area.  We have not tested coyotes locally to determine which mange mites they are carrying.  However, we do not believe that coyotes are carrying the notoedric mange mites, nor do we believe that the anticoagulants are related to an apparent rash in recent coyote mange cases observed in various parts of California.  Why not?  Well, as it turns out, coyotes are far more sensitive to the effects of anticoagulants than cats, and are 100 times more vulnerable to the toxic effects of some anticoagulant compounds compared to cats.  This observation seems to extend into wild cat and wild dog species as well.  In fact, during the 1996-2004 coyote study conducted by the National Park Service in the Santa Monica Mountains, anticoagulant rat poison exposure was the number 2 source of mortality for coyotes (being hit by cars was the number 1 source of mortality).

For bobcats, on the other hand, we have only had a couple cases deaths due to anticoagulant poisoning.  Our hypothesis in the case of bobcats is that the sublethal, chronic exposure to anticoagulant poisons is, over time, somehow decreasing their resistance to notoedric mange.  Anticoagulant poison exposure may be increasing their risk to death due to other, unrelated causes.  Since coyotes do not seem able to tolerate the sublethal, chronic exposure to the poisons and instead are more likely to die directly from the poison exposure. 

Other Questions That Remain...Among the questions of how anticoagulant exposure could affect bobcat immunity and whether there is an causative link between anticoagulants and mange, other important questions remain.  Little is known about the biology of this particular mite species, so we have many unanswered questions about how these mites have come to impact our bobcats so significantly. For instance, we are thus far unsure of where our bobcats are contracting the mange mites. We suspect that the bobcats are getting the mites from one of several potential sources including their small mammal prey, domestic cats, or from one another.  Notoedric mange is more  We are currently collaborating  with Janet Foley at UC Davis to identify potential sources of the mange mite. Lynx affected by notoedric mange in Switzerland were thought to have contracted the ectoparasite from domestic cats.

What else are we doing to study disease in our local carnivores?

Presently, we are involved in a collaborative, inter-disciplinary and inter-agency study of disease in bobcats and mountain lions in the Santa Monica Mountains.  The collaborating groups include UCLA, the National Park Service, UC Davis and Colorado State University.  There are a variety of ways to study disease in wildlife, and these include:

1.  Measuring diseases that animals are exposed to using blood samples.  This involves measuring the antibodies specific to certain diseases that can be found in our bloodstreams after exposure to a disease.  Alternatively, some for some pathogens, the DNA of the diseases themselves (such as viruses and some blood-infecting pathogens) can be detected directly within blood samples collected from individuals.  We are utilizing both methods to study diseases that bobcats and mountain lions are exposed to in the Santa Monica Mountains.  The study contributes to a larger, southwestern U.S. National Science Foundation study of diseases found in these two species of wild cats, as well as feral domestic cats in the same region, that is being performed by our collaborators Drs.Kevin Crooks and Sue VandeWoude at Colorado State University.    

2.  Identification and quantification of fecal parasites.  There are many different types of diseases that can be detected in fecal material.  Of interest to us, and contributing to the larger bobcat disease susceptibility project in progress by Laurel Serieys are internal parasites, such as tapeworms and roundworms that can potentially infect the gastrointestinal tract or even other organs like the heart and lungs.  To gather information about the internal parasites affecting bobcats locally (and mountain lions when the rare opportunity arises), we collect fecal material from bobcats at the time of capture, as well as fresh fecal samples that we find on trails when we are out doing our field work.  Then Laurel, along with UCLA undergraduate students, perform fecal floats to isolate the eggs shed by internal parasites found in various organs in the bobcats. For those samples that are collected during routine field work, Laurel and UCLA undergaduate students also perform genetic analysis on each fecal sample collected to ensure that it is bobcat, and identify if it is a bobcat we have captured in the past, or have collected other fecal samples from before. In quantifying the number of parasites detected in the fecal samples, we hope to examine whether there are differences in the parasite load (ie., the total number of parasites detected) for bobcats that live in urban areas vs. more protected, less urban-influenced regions.  

3.  Collect and identify ectoparasites.  Our last method we are employing to study disease in bobcats and mountain lions is to collect the parasites that live on their skin and hair and identify them.  A disease of particular concern to us is notoedric mange, and so we are especially diligent to perform the protocols required to sample for notoedric mange on all of the animals we capture.  We are collaborating with the Janet Foley lab at UC Davis to help identify some parasites we collect.

References

1.  Bradley, C.A. and Altizer, S. 2007. Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution, 22: 95-102.

2.  Funk, S.M., Fiorello, C.V., Cleaveland, S., and Gompper, M.E. 2001. The role of disease in carnivore ecology and conservation.  In: Carnivore Conservation (Gittleman, J.L., Funk, S.m. Macdonald, D. and Wayne, R.K., eds.) pp. 443-466. (Cambridge University Press)

3.  Riley, S.P.D., Bromley, C., Poppenga, R.H., Whited, L. and Sauvajot, R.M. 2007.  Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban Southern California. Journal of Wildlife Management, 71(6): 1874-1884. 

4.  Maehr, D.S. et. al. 1995. Notoedric mange in the Florida panther (Felis concolor coryi). Journal of Wildlife Diseases, 31: 251-254.

5.  Pence, D. B., F. D. Matthews, and L. A. Windberg. 1982. Notoedric mange in the bobcat, Felis rufus, from south Texas. Journal of Wildlife Diseases, 18:47-50.

6.  Pence, D.B., Tewes, M.E., Shindle, D.B., Dunn, D.M. 1995. Notoedric mange in an ocelot (Felis pardalis) from southern Texas. Journal of Wildlife Diseases, 31: 558-561. 

7.  Pence, D.B., and Ueckermann, E. 2002. Sarcoptic mange in wildlife. Revue Scientifique et Technique, 21: 285–398.

8.  Penner, L.R. and Parke, W.N. 1953. Notoedric mange in the bobcat, Lynx rufus. Journal of Mammalogy, 35: 458. 

9.  Ryser-Degiorgis, M.P., Ryser, A., Bacciarini, L.N., Angst, C., Gottstein, B., Janovsky, M., Breitenmoser, U. 2002. Notoedric and Sarcoptic mange in free-ranging lynx from Switzerland. Journal of Wildlife Diseases, 38: 228-232. 

10.  Riley, S.P.D., Boydston, E.E., Crooks, K.R., Lyren, L.M. 2010. Bobcats (Lynx rufus). In: Urban Carnivores (Gehrt, S.D., Riley, S.P.D., Cypher, B.L., eds.) pp. 121-138 (John Hopkins University Press)