Our results indicate that marine iguanas are able to differentiate between the alarm call and song of Galápagos mockingbirds and increase anti-predator vigilance behaviours in response to alarm calls. This is the first demonstration that a species that lacks vocal communication can associate the auditory alarm signals of another species with the threat of predation.
The relative response of iguanas to alarm call versus song was consistent across sites, but sites differed in overall responsiveness to playbacks. This could result from variation in the ambient noise affecting receiver volume and/or sound quality. The distance from the playback speaker to the iguanas was not a significant factor in predicting response, but ambient noise might have varied between sites due to differences in wind speed and distance from the ocean. Alternatively, there may be a true difference in the responsiveness of animals between sites, which could be due to a variety of factors including variations in predation pressure, topography or the frequency of mockingbird vocalizations. The flight trajectory of hunting hawks is highly predictable on Santa Fe—hawks appear first at the northern end of each site and then proceed along the island's coastline in a clockwise direction until prey is captured (). It is possible that this consistent flight pattern results in higher predation rates at site 3, where individuals exhibited the highest level of responsiveness to both types of playbacks.
Iguanas displayed greater responsiveness to playbacks earlier in the day. It is conceivable, but was not tested here, that marine iguanas with lower body temperatures are more responsive to alarm calls because they are less agile and thus escape more slowly than individuals with high body temperatures during the midday or afternoon periods (Wikelski & Trillmich 1994
The behaviour of iguanas during playbacks may have been influenced by conspecifics; however, the higher proportion of alert behaviour exhibited during alarm calls indicates that at least some individuals are capable of discriminating between these acoustic stimuli. Because we wanted to standardize our sound playback, both of the mockingbird recordings we used for playbacks came from the same individual. However, the downside of this experimental paradigm was that we were not able to correct for possible variations in individual vocalizations (Kroodsma 1989
). Nevertheless, we suggest that our use of mockingbird song as a control may ameliorate potential bias introduced by using just one alarming individual.
The adoption of anti-predator defences can impose significant costs in prey species (Blumstein 2002
). Marine iguanas adopt thermoregulatory postures that involve orienting either directly towards the Sun or at 90° angles to it. This behavioural thermoregulation is vital; individuals unable to adjust their body position quickly overheat and succumb (Bartholomew 1969
). Even though hunting hawks predictably approach the site from the north, marine iguanas are unable to maintain vigilance in this direction, as doing so would probably impair their thermoregulatory capabilities. The ability to capitalize on the auditory alarm system of another species, particularly an endotherm less constrained by thermoregulatory needs, could provide a significant benefit to marine iguanas. Auditory communication is rapid and can travel over long distances without a direct line of sight, making it an ideal way to transmit information about impending predation in locations with varied topography.
The energetic cost of escape behaviours can also be substantial (Ydenberg & Dill 1986
; Cooper & Frederick 2007
). Juvenile and female-sized marine iguanas often walk or run towards a position of safety during hawk hunting flights; these short bursts of locomotion greatly increase the heart rate and energetic expenditure of iguanas (Vitousek et al. in preparation
). Female marine iguanas face high energetic constraints, particularly during the breeding season (Vitousek et al. 2007
). The ability to gain additional information about the presence of a predator might enable a more effective and/or less costly anti-predator response. Energetics may also explain the low rate of escape behaviour in response to playbacks. Confirming predator location prior to flight provides the most energetically efficient means of capitalizing on heterospecific signals.
This is the first finding that a species lacking vocal communication eavesdrops on and discriminates between heterospecific vocalizations. Heterospecific call recognition in marine iguanas cannot result from generalizing conspecific alarm calls and may instead involve associative learning of complex auditory signals. It is unclear whether this ability is indeed learned or whether naive iguanas are able to recognize and respond appropriately to the alarm calls of mockingbirds. Further research will address this question and investigate whether this ability is localized to the Santa Fe population or is a more general phenomenon.