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.