Behavioural Processes 100 (2013) 197–199
Contents lists available at ScienceDirect
Behavioural Processes
jou rn al h om epa ge: www.elsevier.com/locate/behavproc
Short report
Barbados green monkeys (Chlorocebus sabaeus) recognize ancestral
alarm calls after 350 years of isolation
Melissa Burns-Cusato
a,*
, Brian Cusato
a
, Amanda C. Glueck
b
a
Centre College, Danville, KY, United States
b
Texas Christian University, Fort Worth, United States
a r t i c l e i n f o
Article history:
Received 1 May 2013
Received in revised form 1 August 2013
Accepted 25 September 2013
Keywords:
Chlorocebus
Vervet
Green monkeys
Anti-predator behavior
Predator isolation
Alarm call
a b s t r a c t
Vervet monkeys (Chlorocebus pygerythrus) produce alarm calls and anti-predator behaviors that are spe-
cific to a threatening predator’s mode of attack. Upon hearing a leopard alarm, the monkeys will run up
trees where they are relatively safe. In contrast, eagle alarms prompt the monkeys to run under bushes
and snake alarms stimulate bipedal standing. Early researchers proposed that the meaning of each alarm
call is conveyed by observational learning. If this true then absence of the predator that elicits the alarm
call may lead to alteration or decay of the alarm’s meaning since there is no longer opportunity for obser-
vational learning to occur. The present study tested this hypothesis by presenting alarm calls to a closely
related species of monkeys (Chlorocebus sabaeus) that have been isolated from their ancestral predators
for more than 350 years. The monkeys ran up trees in response to a leopard alarm, but not when the
same alarm was played backwards and not in response to a snake alarm. Snake alarms failed to reliably
elicit bipedal standing. These results suggest that the leopard alarm call conveys the same information to
Barbados green monkeys as West African green monkeys despite generations of isolation from leopards.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Many species that live in groups produce alarm calls in response
to potential threats (Hollen and Radford, 2009). In some of these
species, the ability to recognize predators, produce accurate alarms,
and respond to the alarm calls of conspecifics is mediated by genetic
mechanism (e.g., Reichert and Hedrick, 1990). In others species
comparable anti-predator behaviors are learned though experi-
ence (Jamieson and Ludwig, 2012). Further still, evidence suggests
that for a third set of species alarm call behaviors are mediated by
both genetic and experiential mechanisms (Curio, 1993; Hollen and
Radford, 2009).
Vervet monkeys (Chloroecbus pygerythrus) have evolved a com-
plex alarm call system with corresponding anti-predator behaviors
that are specific to the predator’s mode of attack (Seyfarth et al.,
1980). Vervet predators fall into three general categories: avian,
terrestrial, and snake-like and each category evokes an acoustically
distinct alarm call. For instance, the monkeys emit a loud bark at the
sight of a leopard, a double-syllable cough when a crowned eagle
is spotted, and a soft chutter when a snake is detected (Struhsaker,
1967; Cheney and Seyfarth, 1990). The response to the alarm calls
*
Corresponding author at: Centre College, 600 West Walnut Street, Danville, KY
40422, United States. Tel.: +1 859 238 5384.
E-mail address: m.cusato@centre.edu (M. Burns-Cusato).
is also predator-specific so monkeys that hear an alarm for a partic-
ular predator category will respond with an anti-predator behavior
that warrants the best chance of escape. Predators in the terrestrial
category, such as leopards, tend to attack monkeys on the ground
so vervets respond to a leopard alarm by running high into a tree
(Seyfarth et al., 1980). In contrast, because avian predators attack
monkeys from the air, the monkeys are most likely to escape an
avian attack by hiding under a bush. Consistent with this, Cheney
and Seyfarth (1990) observed that vervets are more likely to run
under a bush than up a tree after hearing an avian alarm call.
Monkeys can often drive snakes out of the area by mobbing them.
Thus, when a monkey sees a snake and utters the snake alarm,
other monkeys in the area will rise to a bipedal stance, look down
to locate the snake, then approach the snake to mob it with fel-
low troop-members. Thus, evidence suggests that each alarm call
is referentially functional, conveying a distinctly different message
about a potential predator (i.e., the presence of a predator and the
best means of escape).
Recent research indicates that the alarm calls and correspond-
ing anti-predator behavior of green monkeys is very similar to
that of vervet monkeys (Price and Fischer, 2013). Once considered
a subspecies of vervets, the green monkey (Chlorocebus sabaeus)
is now widely considered to be a separate species altogether
(Groves, 2001). Nevertheless, the two species share many predators
and anti-predator vocalizations and behaviors. For example, both
species are preyed upon by leopards and snakes in their African
0376-6357/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.beproc.2013.09.012