9Have you ever played the game Marco Polo? In this game, the chosen player who is “It” shouts “Marco” and the other players have to respond by shouting “Polo”, which “It” uses to acoustically locate them. Just as the players are required to use the skills of sound localization and vocal trickery to win the game, we see the same skills being used in the natural world by parasites to exploit host risk perception. Because reproductive costs for many species can be substantial, they employ a variety of tricks to minimize and pass these costs to others.
Brood parasitic birds such as common cuckoos (Cuculus canorus) lay their eggs in the nests of another host species, so that the parents rear the foreign young at the expense of their own offspring. If parasites want to lay eggs into their hosts’ nest, it would seem reasonable to expect that the parasites will come and go in a quiet manner. However, the female cuckoos often give a conspicuous ‘chuckle’ call after parasitizing a host’s clutch. Why do they give this striking call?
In a study by York and Davies, the scientists hypothesize that the female common cuckoos (Cuculus canorus) use a predatory hawk-like call to manipulate their reed warbler (Acrpcephalus scirpaceus) host behavior and thus increase the success of parasitism. It is widely known that adult birds distinguish threats to themselves from those to their offspring. Parents would attack nest predators that present no direct threat to them, but they may readily flee from the nest if threatened by a hawk. By exploiting this fundamental trade-off in the hosts, the cuckoos may use deceptive signals to parasitize their hosts’ nests.
Previous studies have shown that the hosts defend against parasitic cuckoos by mobbing adult cuckoos and by rejecting eggs that appear different than their own. As a result, cuckoos manipulate hosts using sensory cues, such as visual or vocal imitation. The female cuckoo chuckle call ‘kwik-kwik-kwik…’ is similar in frequency and rate to the ‘kiii-kiii-kiii…’ call of Accipiter hawks. In addition, the parasitic cuckoos have a hawk-like plumage that may serve as an advantage to fool their hosts (Fig. 1).
York and Davies performed field experiments in which they tested whether female cuckoo calls provoke vigilance in reed warblers. The four treatments of their experiment: a ‘kwik-kwik-kwik…’ call of a female cuckoo (threat to clutch), a ‘kiii-kiii-kiii…’ call of a Eurasian sparrowhawk Accipiter nisus (a threat to the adults), a ‘cuck-oo’ call of a male cuckoo (no threat to either but serves as a potential cue to parasitism risk), and a ‘coo-cooo-coo’ call of a collared dove Streptopelia decaoto (a harmless control). Reed warblers were more likely to be vigilant during hawk and female cuckoo calls (Fig. 2).
Vigilant responses were noted by how the hosts would continuously scan the surroundings for danger upon hearing the call. The increase in vigilance to both of those calls indicate that reed warblers perceive female cuckoo calls as a threat possibly due to acoustic similarity.
The scientists also performed playback experiments to tits (Paridae) which are prey of sparrowhawks, but not targets of cuckoos. Therefore, they should not respond to female cuckoo calls as a threat unless they mistake them for hawk calls. Similar to the results of the reed warbler vigilance, tits were more likely to become vigilant during hawk calls and female cuckoo calls. Although cuckoos are not a threat to tits, their vigilant response to both is likely due to their perceived acoustic similarity.
To further test the acoustic similarity of the female cuckoo and hawk calls, York and Davies performed an experiment to test how reed warblers’ exposure to the four calls influenced their nest defences (egg rejection and mobbing). Results show that reed warblers that had been exposed to hawk or female cuckoo calls were more likely to accept the foreign egg. They were still more than twice as likely to keep a foreign egg in their clutch following female cuckoo calls compared with male cuckoo calls. However, the call type did not affect mobbing responses. Since mobbing is a common generalized defence, they may not respond specifically to cuckoos.
Because male cuckoo calls had similar effect on host responses like the harmless dove control, it is likely that they call conspicuously to attract females; their calls are likely to be a poor predictor of local parasitism risk. In contrast, the presence and call of a female cuckoo is a strong predictor of parasitism risk. This would reduce the potential for hosts to learn to discriminate female cuckoo chuckles from hawk calls.
By using this fundamental trade-off in warblers’ defences between clutch- and self-protection, female cuckoos may distract the warblers’ attention and misdirect their defences to reduce egg rejection and increase the success of parasitism.
York and Davies show that research involving deception in nature can be studied by better understanding the coevolutionary arms race between cuckoos and their hosts. Their results suggest that the use of female vocal calls are associated with a brood-parasitic lifestyle, including secretive behavior to avoid alerting hosts and visual similarity of the plumage to throw off host recognition. As the scientists phrased, the cunning female cuckoos may have the “last laugh” in this battle of host defences versus parasite trickery.
York, J. E. & Davies, N. B. (2017). Female cuckoo calls misdirect host defences towards the wrong enemy. Nature Ecology & Evolution, 1-6. https://doi.org/10.1038/s41559-017-0279-3