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Conditioned Taste Aversion

Condition Taste Aversion as a non-lethal method of reducing predator-wildlife and predator-livestock conflicts
Ron Thompson, Primero Conservation,
The recent headlines in southern California read: Kill mountain lion P-45? Malibu rancher’s hunting permit incites uproar
Having dealt with similar incidents concerning mountain lions or pumas (Puma concolor) while working for Arizona Game and Fish Department, often in the city limits of Phoenix, I could relate to what California’s wildlife agency did next. They went to their predator conflict toolbox and pulled out a depredation permit, and then a public relations fire storm followed. I discuss here an alternative tool that has a valid physiological basis, yet still needs the rigorous tests of the scientific method: Condition Taste Aversion (CTA).
CTA has been successfully demonstrated on a wide variety of both captive and free-ranging predators using mostly domestic prey or invasive species such as cane toads. In these studies, animals that consumed bait laced with an undetectable dose of an aversion agent, such as Thiabenzadol (TBZ), later avoided both baits and live prey with the same taste and scent associations as the baits.
CTA affects vertebrates through their long-term memory as affected by the vagus nerve. If any animal, liquid, or vegetable matter makes a vertebrate sick, aversion to the offending food remains in that vertebrate’s memory and induces nausea. The purpose of this note is to briefly summarize the process of CTA, provide specific outcomes that have resulted with captive animals, and suggest that similar outcomes would be observed in wild free-roaming predators.  To understand the process only requires reflection upon occasions when you consumed some food and then became severely ill.  Once recovered from illness, a visceral feeling of “disgust” occurs upon tasting or smelling the particular food that preceded the illness.  It does not matter where the food was consumed; it does not matter where next the food might be encountered.  It is not necessary for more than a single full-dose taste-illness event in order for the aversive effect to take place. It does not even matter what actually caused the illness.  Although most illnesses are induced by food-borne toxins, motion sickness, nausea due to influenza, illness induced by expo- Perspectives sure to environmental toxins, and even chemotherapy or radiation treatments may induce food aversions that can be life-long.  All vertebrates share neural anatomy, largely in the brain stem and largely reflexive, which is responsible for lasting change in food preferences induced by illness. Nonetheless, we must add rigor to CTA testing and carefully observe how predators regard the taste and scent of foods that have made them sick in the past.
Lowell K. Nicolaus, Northern Illinois University, challenged biologists that had contacted him through his website to condition captive pumas against eating desert bighorn sheep (Ovis canadensis) meat. Currently pumas in 4 states (Arizona, New Mexico, California and Texas) are being killed by private, state and federal wildlife agencies in attempts to increase desert bighorn numbers. Desert bighorn hunting permits can fetch funds as high as $400,000 for a single auction permit for state agency coffers, or $70,000/permit for private landowners. Removal of pumas is conducted under contract protocols that are often less restrictive than trapping regulations for licensed fur trappers. Two puma trappers in Texas alone reportedly remove between 150-200 pumas annually from various private properties in the Trans-Pecos region. Traps in Texas are often checked less than once every two weeks (personal observation from GPS collared animals). Puma in New Mexico can now be trapped year long with no restrictions on numbers on private land. These circumstances should encourage biologists to apply science to seek alternative non-lethal methods to effectively reduce puma predation on vulnerable populations of wild prey species as well as depredation on domestic stock.
As a result of Dr. Nicolaus' challenge, we averted a captive male and female puma against desert bighorn sheep using a dosage of 250 mg of TBZ/kg of puma weight. Ground desert sheep meat was placed in 2-kg meat packages wrapped in fresh desert sheep hide, avoiding human scent contamination throughout the process. Aversion against the meat was achieved with a single treatment on the first feeding; complete aversion was exhibited during two subsequent contiguous day feedings and again at two months post-treatment. Treated pumas continued to reject bighorn sheep meat wrapped, like a burrito, in a desert sheep hide. Instead of a proclamation of success, Dr. Nicolaus simply stated:
“How long CTA lasts is a big question everybody is asking. One of the only ways one might reduce an aversion is to food-deprive captive animals, set the target food in front of them with nothing else to eat, let it sit there for hours.  Now, what goes on in the mind of a very hungry predator is the possibility that the food was previously only toxic seasonally (some naturally-occurring poisons are only toxic some times in the year), or only toxic in one part but not all of it.”
So, what biologists might see during simple experiments are exaggerated neophobia in which the test subject (e.g., puma) smells the food, then leaves and returns repeatedly. It may then lick the bait, and possibly chew on it a little, even swallow some. If the food no longer has toxin in it, then no illness follows and so the predator may lose its fear and eventually consume the food each time it is subsequently offered.  For this to happen, the predator must be confined with the food for long periods over multiple occasions, so the predator can learn that the food is no longer toxic.  It has not learned that the food is safe--it has learned that sometimes the food is dangerous and sometimes it is not; hence it might never return to full confidence in this particular food.
If an average predator requires 10 such post-treatment toxinfree tests, given at one-week intervals, before it begins to eat the food, you might conclude that the aversion lasted 10 weeks.  If you conduct the post toxin tests each month, then you might conclude that the aversion lasted 10 months.  If you do it every year, then you might conclude that the aversion lasted a decade.  Every bit of this is a function of the experimental design--arbitrary decisions made by the biologist.  Attempts to study behavior under such conditions have the same external validity as confessions taken under torture and for just the same reasons. 
Now, consider a top predator in the wild that must expend a lot of time and effort to obtain food.  For this animal, a real risk exists that they might sprain an ankle, break a tooth, snap a bone-- all potentially lethal injuries.  Consider also that in this process any predator that discloses intent and presence in pursuing prey will alert nearby prey, thereby reducing potential for success in the immediate area for a while. Predators that for whatever the reason, miss too many meals are in a real fix. 
Consider finally, that such a predator must move great distances tracking prey by distal sensory cues such as scent. Will a predator risk pursuing a prey whose scent it had previously found disgusting and which it may not be able to eat?  What are the odds that such a predator will ever go through the process described above for reducing the aversion?  None of this can be legitimately tested in captivity.  So, though it is informative to initially experiment with captive animals, it tells only a small amount of what we, as “conflict predator managers”, really need to know.
I doubt if we shall have any better opportunities than what just occurred with the most famous puma in North America, P-45.  Nonetheless, it may be unlikely for the NGOs protesting California’s handling of P-45 to support CTA experiments – the “chemical poisoning” of an animal, or that wildlife agencies will invest in such research. In Texas and New Mexico, state agency personnel and associated wild sheep sport-hunting organizations went to great lengths to take CTA off the selection of tools in the conflict resolution tool box.
Recently our group, Primero Conservation, under the guidance of Rodrigo Nuñez, PhD and Ivonne Cassaigne, DVM, PhD, successfully averted 5 jaguars held in captivity from eating domestic sheep. The Mexican government financially supported the experiment and the results will be published shortly.
For additional information on CTA established to honor the memory of Dr. Nicolaus.
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