Nuisance Ecology: Do Scavenging Condors Exact Foraging Costs on Pumas in Patagonia?

1. What they did

Prey animals often give up food early when they feel at risk of being caught, and researchers measure this as “landscapes of fear”. The authors asked whether a top predator can face something similar from scavengers. In Chilean Patagonia, Andean condors gather in numbers at puma kills. The authors asked three questions: (1) Do condors cost pumas food? (2) If so, do pumas behave as if they know it? (3) Do pumas forage like prey animals in a risky landscape?

• Following pumas. They caught pumas in 2008 and 2009, and fitted nine with Global Positioning System (GPS) collars that took a location every 2 hours and sent the data by satellite (Argos). They monitored them for an average of about 9 months.
• Finding kills. Places where a puma made two or more locations within 150 m (GPS clusters) were visited by CyberTracker-certified observers, who identified prey, decided whether the puma had killed or scavenged it, noted whether it was cached, measured canopy cover, and recorded whether condors had been there.
• Measuring feeding. From the collar data they worked out handling time (hours a puma stayed with a kill), search time (hours until the next kill), distances moved between kills, and kill rates.
• Mapping risk. They gave each habitat a score for how easily condors could see a carcass, from forest (lowest) to open valley steppe (highest), and mapped where condors had found kills. Combining the two gave risk classes from 2 to 8.
• Giving-up time. For kills where a puma left more than 10% of the edible meat, they used the time spent at the carcass as a “giving-up time” (GUT): the shorter the time, the greater the risk the puma seemed to feel. They tested whether condor risk or prey density better explained GUTs.

2. What they found

Kills and condors

• They investigated 694 GPS clusters and found 433 kill sites and 6 cases of puma scavenging. Prey were 350 ungulates (302 guanacos, 41 domestic sheep, 7 huemul) and 83 small to medium-sized animals.
• Condors were recorded at 43% of 296 ungulate kills where their presence could be determined with certainty.
• Pumas left an estimated 29 kg of meat (range 0 to 75 kg) at each ungulate kill.
• Of 266 ungulate kills with known handling time, pumas left 133 (50%) after a single night with more than 10% of the edible meat remaining, and another 56 (21%) after two nights. The authors report that pumas never returned to check those carcasses.

Handling time, search time and kill rates

• Handling time went up with prey weight and when the kill was cached, and went down when condors were present. Together these explained 63% of the variation.
• Shorter handling times were followed by shorter search times before the next kill. Prey weight did not affect search time.
• Mean search time was about 70 hours, and pumas moved on average about 20 km between kills (about 33 km with a correction for the real winding path).
• Ungulate kill rates averaged 12.49 kg per day, 50% higher than the 8.28 kg per day reported for pumas in North America. Kill rates did not differ between males and females. Pumas spent on average about 29% of their time at kill sites.

Risk and giving-up time

• GUTs were shortest in the riskiest areas (about 21 to 26 hours in risk classes 6 to 8) and longest in forest (about 94 hours in class 2).
• Risk of condor harassment explained GUTs; prey density did not.
• Pumas made disproportionately many kills in the riskiest areas: 4 to 5 times more often than expected in the two highest risk classes.
• The authors saw condors challenge a puma for a carcass only once. That puma could not hold off attacks from several sides and finally left the kill to the condors. Condors fed in groups of up to 28.

3. What they concluded

• Scavengers can impose foraging costs on top predators, and pumas appear aware of the risk of their kills being found by condors in open country.
• Condors shortened the time pumas spent at their kills, and the authors suggest pumas made up for these losses by killing more often.
• Pumas behaved like prey animals in a landscape of fear: they left food sooner where risk was higher, yet hunted most in the high-risk, high-reward open areas where prey was plentiful.
• Caching delayed, but did not stop, condors finding kills in open habitats.
• The authors leave open why pumas abandon kills in the first place: condor harassment, or fear of people, since pumas in open steppe were heavily persecuted by hunters and ranchers. Either way, they argue, condors take the remaining meat, so condors exact the cost.
• Simple single predator, single prey models may not predict real predator and prey dynamics. By raising puma kill rates, scavengers may indirectly affect prey populations and communities.

4. How tracking was or was not used

• Finding pumas for capture: the team rode on horseback until they found fresh puma tracks, often in snow, then used hounds to bring the puma to a tree or rock outcrop.
• Kittens: the number of kittens with collared females was found through captures, direct observation, tracks in snow and cameras at kills.
• Kill site investigations: observers identified prey from hair, skin, rumen and bone fragments, and used bite marks and which body parts were eaten to tell a kill from scavenging. They recorded whether carcasses were cached (covered with debris).
• Condor presence: recorded from sightings, cameras, and signs at the kill, including feathers, droppings and footprints. The authors did not try to judge condor presence at kills visited more than two weeks after the puma left, because signs were harder to interpret.
• Walking puma trails: a correction factor for distances travelled came from walking a sample of 2-hour segments of puma trails (described in an earlier paper).

5. Tracker or observer certification

Certified trackers. The kill site investigations were done by CyberTracker-certified observers; the paper cites Evans et al. (2009) and Elbroch et al. (2011) for the certification. The level of certification is not given. Neal Wight, Cristián Rivera, Casey McFarland and René Millacúra are thanked for help with kill site investigations.

6. Other technologies, skills or innovations

• Argos-GPS collars (SirTrack, Televilt, Lotek, Telonics) and very high frequency (VHF) radio collars, with satellite uplinks every 2 to 5 days.
• Handheld GPS units (Garmin eTrex and Summit) to guide observers to clusters.
• A convex spherical crown densiometer to measure canopy cover over each kill.
• Remote cameras at kills.
• A new measure, giving-up time (GUT), adapted from giving-up density experiments so that wild kills of different sizes could be compared without feeding stations.
• Ages of guanaco and huemul from tooth eruption, and weights from growth estimates, to estimate kilograms killed.

7. Implications for conservation (from the paper)

• Scavengers usually seen as harmless opportunists may indirectly shape communities by increasing predators’ pressure on their prey.
• Higher puma kill rates mean more encounters with prey, which could be a problem for rare prey. In this area it may partly explain the unsustainable puma predation on endangered huemul.
• The Andean condor is listed as near threatened by the International Union for Conservation of Nature (IUCN).
• Future research should ask whether people or condors drive pumas to abandon kills, and how much condors affect puma survival and breeding.