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Vocal Mimicry of Alarmassociated Sounds by a Drongo Elicits Flee

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Vocal Mimicry of Alarmassociated Sounds by a Drongo Elicits Flee ethologyinternational journal of behavioural biology Ethology Vocal Mimicry of Alarm-Associated Sounds by a Drongo Elicits Flee and Mobbing Responses from Other Species that Participate in Mixed-Species Bird Flocks Eben Goodale*, Chaminda P. Ratnayake† & Sarath W. Kotagama† * Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China † Field Ornithology Group of Sri Lanka, Department of Zoology, University of Colombo, Colombo, Sri Lanka Correspondence Abstract Eben Goodale, Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical A growing number of studies have shown that vocal mimicry appears to Botanical Garden, Chinese Academy of be adaptive for some bird species, although the exact function of this Sciences, Menglun, Mengla, Yunnan Province behaviour varies among species. Previous work has looked at the function 666303, China. of the vocal mimicry of non-alarm sounds by the Greater Racket-tailed E-mail: [email protected] Drongo (Dicurus paradiseus). But drongos also imitate sounds associated with danger, such as predators’ vocalisations or the mobbing-specific Received: August 17, 2013 vocalisations of other prey species, raising the question of whether the Initial acceptance: September 20, 2013 function of mimicry can vary even within a species. In a playback experi- Final acceptance: December 6, 2013 ment, we compared the effect on other species of different drongo vocali- (V. Janik) sations including: (1) predator mimicry, (2) mobbing mimicry, (3) drongo doi: 10.1111/eth.12202 species-specific alarms, (4) drongo species-specific non-alarms and (5) a control (barbet) sound. Both mobbing mimicry and drongo species-spe- Keywords: alarm calls, bird song, cific alarms elicited flee responses from the most numerous species in the Dicruridae, interspecific communication, flocks, the Orange-billed Babbler (Turdoides rufescens). Mobbing mimicry mixed-species flocks also elicited mobbing responses from the Orange-billed Babbler and from another gregarious babbler, the Ashy-headed Laughingthrush (Garrulax cinereifrons); when responses from both species were considered together, they were elicited at a significantly higher level by mobbing mimicry than by the barbet control, and a level that tended to be higher (0.07 < p < 0.10) than the response to drongo-specific alarms. Predator mimicry elicited flee and mobbing responses at an intermediary level. Our results support the hypotheses that mobbing mimicry is a specific category of mimicry that helps attract the aid of heterospecifics during mobbing and that alarm mimicry can in some cases be beneficial to the caller. (Baylis 1982). Two recent reviews found that there Introduction was ‘little evidence for vocal mimicry having evolved Bird song learning has become a model of vocal learn- to serve important functions in most birds’ (Gar- ing, illustrating the interaction between innate ten- amszegi et al. 2007), and ‘there is no compelling evi- dencies and environmental influences, as it has been dence to support any of the functional hypotheses’ shown that while birds can learn many different (Kelley et al. 2008), although both these reviews vocalisations, they tend to learn some vocalisations, emphasised that their conclusions were based on a specifically conspecific ones, better than others, such small number of studies. as heterospecific vocalisations (Marler & Peters 1987). One potential problem in assigning a single function Interestingly, however, the strength of this filter var- to vocal mimicry is that it has been shown to have dif- ies: while some species almost never sing heterospeci- ferent functions in different species. In some brood fic songs, others do quite frequently (Vernon 1973). parasitic species, for example, male birds imitate the The benefits of such vocal mimicry are controversial songs of their host species, which allows females to 266 Ethology 120 (2014) 266–274 © 2014 Blackwell Verlag GmbH E. Goodale, C. P. Ratnayake & S. W. Kotagama Heterospecific Responses to Alarm-Associated Mimicry identify and mate with the correct species (Payne participate with drongos in mixed-species flocks. In a et al. 2000). Mimicry might help birds attract mates in playback experiment, we compared five different other species, if females prefer males that use imita- treatments that included different drongo vocalisa- tions to increase the size of their repertoires (Howard tions: (1) predator mimicry, (2) mobbing mimicry, (3) 1974), and/or judge the quality of males based on the species-specific alarms, (4) species-specific non-alarms accuracy of their imitation (Coleman et al. 2007; and a (5) control sound. We looked at both immediate Zann & Dunstan 2008). These functions of mimicry flee responses to playback and more delayed mobbing have conspecific audiences, but other putative func- responses, when birds grouped together and tions of mimicry have heterospecific audiences. For approached the speaker. For the immediate responses, example, some birds could repel heterospecific com- we chose as subjects Orange-billed Babblers (Turdoides petitors from their territory (Rechten 1978), although rufescens), the most numerous species in mixed-species this hypothesis has yet to be supported by field data. flocks (Kotagama & Goodale 2004), which respond to A recent study did, however, demonstrate that birds heterospecific alarms immediately by jumping or fly- in mixed-species groups can use the mimicry of alarm ing into vegetation (Goodale & Kotagama 2008). We calls to scare other species away from food (Flower noted any delayed mobbing response from any flock 2011). Mimicry can also be used to decrease the risk participant. of predation, either by increasing the mobbing activity We specifically hypothesised that (1) drongo mim- of other species of birds (Chu 2001) or by confusing or icry of predators may be used by drongos to startle startling the predator itself, especially if the mimicry other species away from food resources (similar to the suggests the presence of another predator that might result of Flower 2011). This hypothesis predicts that prey on the predator the calling bird is interacting babblers would immediately flee into vegetation upon with (Igic & Magrath 2013). the playback of predator mimicry. Further, we Previous research on the Greater Racket-tailed hypothesised that (2) drongo mimicry of other Drongo (Dicrurus paradiseus lophorhinus) has shown species’ mobbing vocalisations may be used to dilute that this species uses mimicry in a variety of contexts the risk of mobbing to drongos by increasing the and in a context-specific manner (Goodale & Kota- mobbing of other species (Chu 2001). This hypothesis gama 2006a), raising the question of whether vocal predicts that other species would make a mobbing mimicry can serve different functions even within a response specifically to the playback of mobbing species. The imitation of non-alarm vocalisations of mimicry. Both hypotheses predict that response to other species, which drongos incorporate into their mimicry should be higher than response to the own species-typical non-alarm vocalisations, is attrac- drongo species-specific alarm notes, because other- tive to other species and may help drongos reform wise drongos might be better served using their own mixed-species flocks (Goodale & Kotagama 2006b), species-specific vocalisations instead of mimicry. from which drongos benefit (Satischandra et al. 2007). Drongos also incorporate sounds associated Methods with danger (hereafter referred to as ‘danger mim- icry’) into their own species-typical alarm vocalisa- Study Site tions. Danger mimicry includes the imitation of the vocalisations (usually advertisement or contact calls) This study was conducted in the Sinharaja World Her- of predators and nest predators (‘predator mimicry’), itage Reserve (6°26′N80°21′E, 450–600 m), the most and the imitation of other (non-predator) species’ extensive remaining lowland rainforest in Sri Lanka. mobbing vocalisations (‘mobbing mimicry’) and alarm Mixed-species bird flocks in Sinharaja average 11 spe- calls in response to aerial predators (‘aerial alarm cies and nearly 41 individuals (in an average of mimicry’, Goodale & Kotagama 2005). Given that ani- 45 minutes of observation, Kotagama & Goodale mals have been shown to respond to different kinds of 2004). These flocks are led by the highly gregarious alarm calls in different ways (i.e. the idea of ‘referen- Orange-billed Babbler, but Greater Racket-tailed tial alarm calls’, Seyfarth et al. 1980) and that they Drongos are also found in a high percentage of them may respond to predator vocalisations differently than (89%) and occasionally lead the flocks. the alarm calls of prey species (Barrera et al. 2011), it is possible that these various forms of danger mimicry Construction of Playback Exemplars could have separate functions. Here, we test the hypothesis that danger mimicry The majority of the audiorecordings used for mak- functions to affect the behaviour of other species that ing the playback exemplars were made during a Ethology 120 (2014) 266–274 © 2014 Blackwell Verlag GmbH 267 Heterospecific Responses to Alarm-Associated Mimicry E. Goodale, C. P. Ratnayake & S. W. Kotagama simultaneous study that concentrated on mimicry by included. These consisted of 2-min recordings taken drongos at the nest (during the nesting season, Janu- randomly throughout the day and some opportunistic ary – April, 2008 and 2009, Goodale et al. 2014), and recordings of adult drongos vocalising when young
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