Context is King: Squirrels’ bodies react differently to warnings about different predators

One if by land, and two if by sea/And I on the opposite shore will be/Ready to ride and spread the alarm/Through every Middlesex village and farm/For the country folk to be up and to arm.

On April 18, 1775, Paul Revere told three Boston patriots to hang two lanterns in the steeple of the city’s Old North Church. A militia waiting across the Charles River in Charlestown kept an eye out for these signal lanterns and were prepared act appropriately as soon as they saw one or both of the lights stab out at the darkness. The meaning of the two lanterns has been memorized by countless American schoolchildren in the century and a half since Longfellow published “Paul Revere’s Ride.” One lantern told the militia that the British Army would march over Boston Neck and the Great Bridge, and two meant that that the Redcoats would take boats across the river to land near Phips farm.

Many, if not most, birds and mammals that live in groups have their own signals and alarms that alert members of the group to predators and other dangers. An alarm call can mean the difference between life and death for animals who didn’t detect the threat on their own and younger animals who are especially vulnerable to predation. Belding’s ground squirrels take a cue from Revere and use two different alarm calls to warn of two types of danger. Whistle alarm calls signal aerial predators and trill alarm calls signal terrestrial ones. A squirrel needs to react differently to each type of call and to each type of predator. Listeners respond to whistles by entering a burrow or another hiding spot, and adopt a “posting” stance on their hind legs in response to trills.

When young Belding’s squirrels first emerge from their burrows when they’re a month old, they don’t respond appropriately to the two different calls and if they respond at all, they typically just freeze. They pick up on the appropriate behavioral responses very quickly, though, often within five days of coming above ground. Watching the responses of mom, dad and the other squirrels could teach a youngster what they need to know pretty quickly, but Jill Mateo, from the Department of Comparative Human Development at the University of Chicago, wondered if there was also a physiological factor. For many species, the sight, sound or even odor of a predator spurs physiological changes that make individuals better prepared to track predators and the responses of other animals, hide and be still, defend themselves or run/fly/swim like hell. Maybe a squirrel’s body reacts differently to a whistle than it does to a trill – to two lanterns than it does to one, if you will – and helps prime the squirrel for one response or another.

For the first five days after they come aboveground, juvenile ground squirrels show a higher level of cortisol (a steroid hormone released in response to stress) than during the days before emergence or the weeks after. To see if the hormone had some role in ground squirrels learning appropriate anti-predator behavior, Mateo tested how the levels of the hormone changed in response to different alarm and non-alarm calls. She caught pregnant female squirrels at a few sites near the Sierra Nevada Aquatic Research Laboratory (SNARL) at Mammoth Lakes, CA and brought them back to the lab so they could give birth and rear their young. Around the time the babies would normally leave the burrow, Mateo placed them, in pairs, in a large, dark wooden box once per day and played either a recording of ground squirrel whistle alarms, trill alarms, squeals young squirrels use during play or a silent control.

Every time a squirrel heard a recording, Mateo took a blood sample from it. These tests continued until she had one blood sample for each of the four recordings from a squirrel or until the squirrel turned 35 days old (in some cases, she was not able to get complete samples from a squirrel before it reached the age limit or did not have a large enough sample to analyze). After two rounds of tests in 2006 and 2008, Mateo had partial samples from 32 squirrels and complete samples from 17 of those.

Mateo analyzed the samples and, using a squirrel’s cortisol concentration following the silent stimulus as its baseline, looked at the hormone’s percent change in response to the alarm calls and play noises. Because multiple squirrels from several different litters were tested, Mateo averaged the cortisol responses to each recording for each litter.

For all litters, cortisol concentrations were higher following playback of trill alarm calls than after the other recordings. The change in cortisol levels compared to the baseline was only significant in response to the playback of the trill alarm calls. The whistle alarms did not increase cortisol concentrations, but earlier research by Mateo showed that they do elicit bradycardia, a slower than normal heart rate.

So the squirrels do have different physiological responses to the two alarm calls. What relationship do these changes inside the body have with behavior, though, and what do they have to do with air versus ground attacks? Mateo hypothesizes that cortisol might not increase in response to whistles because attacks by avian predators often only last a few seconds and most birds don’t make repeated attacks if their first one is unsuccessful; the attack would be over before circulating cortisol increased. Bradycardia, however, is associated in young squirrels with decreased motor activity and enhanced information processing. If the heart slows in response to whistles, the squirrels can stay still and pay attention in case it needs to make a break for a hiding spot.

On the other hand, the terrestrial predators that squirrels respond to with trills usually spend a significant amount of time either moving around squirrel burrows or waiting near one to attempt an ambush. Increased cortisol makes glucose available as fuel to the squirrels’ bodies for sustained vigilance in posting stances and, if needed, multiple escape attempts.

Both of these physiological reactions increase arousal and attention in a variety of species, so both might also just aid young squirrels in noticing and paying attention to the responses that nearby adults have to the alarm calls, making for a faster association between the alarms and their appropriate responses.

References: Mateo JM (2010). Alarm calls elicit predator-specific physiological responses. Biology letters, 6 (5), 623-5 PMID: 20236965

Mateo JM (1996). Early auditory experience and the ontogeny of alarm-call discrimination in Belding’s ground squirrels (Spermophilus beldingi). Journal of comparative psychology (Washington, D.C. : 1983), 110 (2), 115-24 PMID: 8681525

Image: “Belding’s Ground Squirrel in the Sierra Nevada Mountains, California, USA” by Justin.Johnsen via Wikimedia Commons. Used under a Creative Commons Attribution 3.0 license.


Deathstalker v. Nightstalker: Bats take down highly venomous prey without a care in the world

There are some 1,400 described species of scorpion in the world, and while only 25 of those have proven they can take down a human being with their venom, many more of them can easily injure and kill smaller creatures. Given that, you’d expect scorpions to be important predators in desert food webs, but you might not expect them to be equally important as prey.

Otonycteris hemprichii

Yes, despite the pincers and the stinger and the venom, plenty of animals – among them, centipedes, tarantulas, lizards, owls,shrews and bats – regularly chow down on scorpions. Hemprich’s long-eared bat (Otonycteris hemprichii, at right), found in deserts in northern Africa, the Middle East and south-central Asia, considers scorpions a major food group, along with beetles, centipedes and spiders. In Israel’s Negev Desert, the proportions of these groups in the bat’s diet changes throughout the year, with scorpion fragments found in only 10% of bat droppings in the early spring and in a whopping 70% in the late summer.

That’s a whole lot of scorpions they’re eating, and while some of those are certainly weakly toxic Large-clawed Scorpions, the bats also prey on the Palestine yellow scorpion (Leiurus quinquestriatus, below). Everything you need to know about L. quinquestriatus can be summed up in its nickname, the deathstalker. These scorpions are considered some of the most dangerous in the world and possess a highly toxic venom that contains a grab bag of neurotoxins. Their sting can cause extreme pain, fever, convulsions, paralysis and death (via heart or respiratory failure), even in humans. These scorpions are also “sit-and-wait predators” that hunt by remaining quiet and still and lashing out at unsuspecting prey that wanders too close.

They certainly sound appetizing, but how do the bats deal with prey that present such a challenge to both detecting and disabling them? Carmi Korine, of Ben-Gurion University of the Negev in Midreshet Ben-Gurion, Israel, and colleagues found that Hemprich’s long-eared bat is what’s known as a gleaner, which means it takes prey from surfaces and not right out of the air, as many bats do. Korine and his team hypothesized that, like gleaning Pallid bats that prey on scorpions in North America, Hemprich’s bat might rely on passive gleaning to find its meals, simply listening for the prey to make noise instead of actively using echolocation to detect it based on its echo signature. The researchers figured that, if that was the way the bats hunted, then they would select prey based on 1) body size (bigger scorpions being easier to detect), and 2) toxicity (less venomous scorpions posing less risk of injury).

The team captured eight O. hemprichii individuals, set them up in a room with a scorpion buffet that included both living and dead Large-clawed Scorpions (Scorpio maurus palmatus), Israeli common scorpions (Buthus occitanus israelis) and, of course, deathstalkers.

When the bats took off to search for food, they spent a few minutes circling the room and dropped down directly onto a scorpion once they noticed it. They only went after the live scorpions, ignoring the dead ones and even walking right over motionless live ones if they missed on their initial divebomb, confirming that they glean passively and rely on prey noises.

Once they landed on a scorpion, the bats immediately started biting the scorpions’ heads. The scorpions did not take this lying down and fought back, stinging the bats on the head and face and, in one case, under the eyelid. The bats made no observable attempts to either avoid or disable the stingers and once they had killed the scorpions they often ate the whole thing, including the stinger and poison gland.

This is how the bats hunted all the scorpions. Contrary to the researchers’ predictions, the bats showed no preference among scorpion species based on either on size or toxicity, diving on their prey immediately after detection without any further inspection and going only on limited acoustic information. In 49% of the test sessions the bats actually went after the more poisonous of the available species (and in 24 direct comparisons, the deathstalker was chosen 50% of the time).

The researchers did not have an explanation for the bats’ indifference to the danger their meals pose, but speculated that either scorpions aren’t able to pierce the bat’s skin, or that the bats have at least a partial tolerance to the venom. Given that the bats regularly ate the stingers and venom glands, it seems more likely that their just tough enough to handle what the deathstalkers can dish out.

For other takes on this study, see Michael Marshall’s post at Zoologger and Zen Faulke’s post at Neuro Dojo .

Reference: Holderied M, Korine C, & Moritz T (2010). Hemprich’s long-eared bat (Otonycteris hemprichii) as a predator of scorpions: whispering echolocation, passive gleaning and prey selection. Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology PMID: 21086132

Images: “Otonycteris hemprichii” by Wikimedia Commons user Charlotte Roemer, used under a Creative Commons license.

“Deathstalker near Tzehelim, Israel” by Wikimedia Commons user Yair Goldstof, used under a Creative Commons license