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Gestural communication in a new world parrot
Behavioural Processes 105 (2014) 46–48
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Gestural communication in a new world parrot Leiliany N. Moura a,∗ , Maria L. Silva a , Marilice M.F. Garotti b , Angélica L.F. Rodrigues a , Adrine C. Santos b , Ivete F. Ribeiro b a b
Laboratório de Ornitologia e Bioacústica, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Brazil Laboratório de Ecologia e Desenvolvimento, Núcleo de Teoria e Pesquisa do Comportamento, Universidade Federal do Pará, Belém, Brazil
a r t i c l e
i n f o
Article history: Received 9 October 2013 Received in revised form 25 February 2014 Accepted 1 March 2014 Keywords: Amazon parrots Biparental care Breeding behavior Communication Gestures
a b s t r a c t Male birds can use visual signals to provide information about their sexual status, via bright coloration, sophisticated sexual displays and elaborate tail and head crests. The majority of forest bird species use vocal communication as their main strategy to show their physiological status during breeding season. It is also used to keep contact between individuals in the same group, in agonistic contexts, and by chicks begging for food. We registered, for the very first time, gestural communication acting in the context of biparental care for the Orange-winged Amazon, Amazona amazonica. This parrot presents at least nine different sounds uttered in contexts of alarm, agonistic, foraging, contact flight and others. This finding suggests that despite being a vocal species, this parrot can perform gestural communication related to parental care. The gestures exhibited by this species represent a strategy for survival, a clever way to protect the nest, reducing the risk of attracting the attention of predators. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Acoustic and visual communication systems related to mating selection, parental care, and agonistic conflicts can be observed among birds (Catchpole and Slater, 2008; Matyjasiak, 2004; Moura et al., 2011). Parrots use acoustic signals as a primary source of communication, and the vocal repertoire of some species has been described elsewhere (Fernandez-Juricic et al., 1998a,b; Toyne et al., 1995; Wirminghaus et al., 2000). The Orange-winged Amazon, Amazona amazonica, utters nine vocalizations in different behavioral contexts, such as to maintain pair and group contact, in dangerous (three types of alarm call) and agonistic situations (Moura et al., 2011). Gestural communication is a visual signal that acts over short distances and is quickly attenuated or hidden by objects in the environment. It must be transmitted in places with a minimum amount of light intensity (Bradbury, 1998; Langbauer, 2000). Gestures can be defined as non-verbal communication in which a visible corporal action communicates a particular message (Liebal and Call,
∗ Corresponding author at: Laboratório de Ornitologia e Bioacústica, Instituto de Ciências Biológicas, Universidade Federal do Pará, Augusto Corrêa, 01, Guamá, 66075110 Belém, Pará, Brazil. Tel.: +55 9132018230. E-mail addresses: [email protected], [email protected] (L.N. Moura), [email protected] (M.L. Silva), [email protected] (M.M.F. Garotti), [email protected] (A.L.F. Rodrigues), drica [email protected] (A.C. Santos), [email protected] (I.F. Ribeiro). http://dx.doi.org/10.1016/j.beproc.2014.03.003 0376-6357/© 2014 Elsevier B.V. All rights reserved.
2012). It requires participation of a receiver to attend to a particular proposal. In this case the sender waits for an answer from the receiver and/or looks at the receiver and keeps displaying the gesture when an appropriate answer is not given. Unlike vocal communication, which can be highly conspicuous, gestural signals are highly directional, and animals that use them to communicate can avoid predators (Bradbury, 1998). Orange-winged Amazons are sexually monomorphic and monogamous for life (Sick, 1997). They nest in tree cavities and the courtship behavior is characterized by male feeding female. This species presents a long incubation period (about 30 days), nestlings are altricial, hatch asynchronously in small broods, and have a low survival rate. These characteristics may lead to pair-bond formation and cooperation in parental care (Moura et al., 2011). The aim of this study is to describe gestural communication in Orange-winged Amazons: a complex sequence of postural movements used by pairs as breeding behavior. This behavior was not described before in captivity or in nature. We have found the unexpected gestures in biparental context during observations of reproductive behavior. 2. Methods The study was conducted in nest sites of Orange-winged Amazons that are associated with open areas on plantations and on the forest edge, spanning 278 km2 , in a privately owned land in Santa Bárbara do Pará, North Brazil (01◦ 12 17 S; 48◦ 18 05 W).
L.N. Moura et al. / Behavioural Processes 105 (2014) 46–48
47
3.1. Gestural communication I: inducing the female to approach and enter the nest
Fig. 1. (A) Gestures performed by male to encourage female to enter the nest. (B) Gestures performed by male to encourage the female to enter and/or to leave the nest.
Of the 15 episodes observed, the presumed male used this type of gestural communication in 14 observations. For this the male perched near the nest-tree and, apparently, after checking for predators, signaled to the presumed female, which was in a nearby tree, that she could approach the nest. The gestural communication I was done by the male raising himself up momentarily and quickly bending his head back by about 45◦ , at a speed of 0.12 ± 0.04 m/s (Fig. 1A), until the female approached and looked toward him. After the female looked at the male, he performed a downward head movement, at a speed of 0.05 ± 0.03 m/s, signaling to encourage her to enter the nest (Fig. 1B). When she did not enter the nest, he moved his head down again and waited for the answer, or moved himself out to a more visible perch where she could see him and repeated the head-down movement, until she entered the nest. In one observation the male perched in the nesttree, and after signaling to the female, which was perched in a tree about 2 m away, he performed a head-down movement and 3 s later she entered the nest cavity. The whole gestural sequence was performed without vocalization and the female entered the nest on average 6.5 ± 6.8 min after the male start signaling.
By Leiliany Moura and Madlene Cardoso.
3.2. Gestural communication II: signaling to the female to leave the nest Field visits were made to 16 active nest sites, from 2005 to 2011, totaling 111 observations (continuous recording technique), each from 5h40 to 11h00 and from 15h30 to 19h00, throughout six breeding seasons, once a week. This study covered the whole breeding season, which in the Amazon region begins in late August and extends into January. Some visual displays were recorded using digital cameras (Canon Powershot S2Is and Panasonic Lumix DMC-FZ18) for posterior analysis. Data were expressed as means ± standard deviation.
This behavior was observed in seven episodes and resulted in the exit of females from the nest. For this purpose, the male perched in the nest-tree and signaled moving his head down (Fig. 1B) until the female left the cavity. This took on average 7.4 ± 7.9 min after signaling is initiated. In most of the observations (93%) of females leaving the nest, however, the male did not perform gestural signs. Instead, he perched near the nest-tree and emitted a specific vocalization until she put her head outside the nest (see Moura et al., 2011). Thus, the use of gestures to encourage the female to leave the nest occurred secondarily.
3. Results 4. Discussion The breeding season of parrots was observed over six breeding seasons, with the initial objective of studying the reproductive and vocal behavior of pairs. It was not expected to find gestural communication during the study. According to our observations, a pair waits four months between the egg-laying and the flight of young. However, as the onset of the reproductive effort is asynchronous among pairs, the breeding season extents for about six months. During the incubation period (about four weeks) and early nestling period (about eight weeks) the female of Orange-winged Amazon leaves the nest cavity twice a day to be fed by the male. Later, when the chicks are feathered and do not need to be brooded by the parents, the female does not spend the night in the nest cavity anymore, but the pair keep feeding the chicks twice a day (for about four weeks). We observed the females entering the nest 101 times, in which it was registered 15 episodes (15%) of gestural communication emitted by the presumed male (there is no sexual dimorphism). This signaling resulted in the female approaching and entering the nest cavity following gestural communication I (Fig. 1A and B), five times in the morning and 10 times in the afternoon. We also observed the females leaving the nest 98 times, and seven times (7%) that behavior happened after the male performed a gestural sign following gestural communication II (Fig. 1B). The gestural communication was observed only for a period of about two months of reproductive season: in the early nestling period, soon after hatching until the chicks are fully feathered.
Our long-term investigation of the breeding behavior of A. amazonica permitted the above description of two gestural communication patterns in a biparental care context in the wild. These results show a special non-vocal communication around the nest of this parrot species, which uses vocal communication most of the time, probably as an adaptation to avoid attention from predators. The signal to make the female exit the nest was mostly performed with male vocalizations. It is plausible to think that in this case it was necessary to use an alternative signaling method in a situation where vision is not entirely possible, given that the female is inside the nest cavity at that moment. The observations shown herein provide important information regarding the complex social communication strategies among these birds through a different modality – visual. Animal species with a social complex structure show complex communication systems (Cheney et al., 1986; Rendall and Owren, 2002; Snowdon, 2004). Group life and parental care demand highenergy rates and a specific communication system to allow the proper expression of physiological status for mating, social hierarchy, and actions against threats to survival (Kumar, 2003; Lasswell, 2007; McGregor and Peake, 2000). Various factors can affect the size of the communication repertoire, including the flexibility of social structure. In non-human primates, societies in which the hierarchical system is not as rigid and shows egalitarian tendencies, communication repertoires
48
L.N. Moura et al. / Behavioural Processes 105 (2014) 46–48
tend to be wider because these species need to negotiate more (Maestripieri, 1999). When predictions based on ecological, social, and cognitive criteria were considered, Liebal et al. (2004) concluded that Siamangs, Symphalangus syndactylus, used a wider repertoire of non-vocal communicative signals than expected. Indeed, these authors have registered 31 non-vocal signals within gestures, tactile signals, and facial expressions in these primates. The monogamous mating system lacks a dominance hierarchy and is characterized by a strong bonding between the adult male and female (Kleiman, 1977). Siamangs and Psittacidae present longterm monogamy. Despite being distant in the phylogenetic tree, the high energy cost of their mating system leads to the maintenance of a strong bond between males and females. Thus, these animals may develop sophisticated communication systems that will insure their survival, that of their offspring, and consequently that of their species (Wachtmeister, 2001). As mentioned in the introduction, Orange-winged Amazons have a sophisticated acoustic communication system and a priori can convey information in various behavioral contexts. Indeed, for alerting imminent danger they have three different alarm calls, besides having contact call, food call, agonistic call, and other distress calls (Moura et al., 2011). Our data reveal that these parrots have an even more complex communication repertoire because males present two specific gestural sequences. This observation is intriguing because in this context, the use of gestural communication toward the receptor is independent of individual sender self-necessities and occurred without the presence of a real immediate danger. It is possible that these gestural sequences are used to warn of possible threats toward the offspring and are performed in silence as a strategy to avoid calling the attention of potential predators in the area surrounding the nest. Nevertheless, further studies will be necessary to confirm this supposition. Considering the entire reproductive season, only in two of four months it was observed gestural communication: in the early nestling period. This is a period in which the nestlings are completely dependent on parental care and are more vulnerable to intruders or predators. It is probably for this reason that pairs of Orange-winged Amazon use gestures instead of vocal communication in this situation. In addition to being subject to predators, parrots are frequently exposed to poachers that harvest them to sell as pet in illegal wildlife trade (Prestes et al., 1997; Wright et al., 2001). During the breeding seasons studied here, 11 out of 16 nests observed were either predated (n = 4) or harvested by poachers (n = 7). Thus, there is a need to increase the protection of nest sites. An environment with many dead trees, where animal species select some tree hole cavities to build nests instead of others, is not easy to be sure in which one the nest was built. Therefore, the movement to enter or to leave the nest is the best way to discover a parrot nest, and it is possible that these moments are crucial for their reproductive success. The results reported here show for the first time evidence of gestural communication in the context of biparental care in Orangewinged Amazons. Most gestural communication data published elsewhere refer to physiological and hierarchical status of the individual sender specifically connected to the necessities of the self. Indeed, authors have reviewed the literature on such gestural repertoires among birds, mammals, and some reptiles but connection with necessities of the self were always very clear
in those studies (e.g. Kleiman, 1977; Langbauer, 2000; Pika and Bugnyar, 2011; Woo and Rieucau, 2012). An important question to be addressed in future studies is whether the gestural communication repertoire described here is an isolated phenomenon or something more ordinary that has somehow been overlooked so far. We intend to study more Amazon bird species to begin to elucidate this question. Acknowledgments We thank D. Aleixo, D.O. Ferraz, E.R. Oliveira, J.L. Magalhães, P.C.R. Costa, R. Emin-Lima, and R.S. Oliveira for fieldwork assistance; M. Cardoso for drawing assistance; M. Gahr, S. Wright, and W. Wright for the English revision of an earlier draft. References Bradbury, J.W., 1998. Principles of Animal Communication. Sinauer Associates Inc., Sunderland. Catchpole, C.K., Slater, P.J.B., 2008. Bird Song: Biological Themes and Variations. Cambridge University Press, Great Britain. Cheney, D.L., Seyfarth, R.M., Smuts, B.B., 1986. Social relationships and social cognition in nonhuman primates. Science 234, 1361–1366. Fernandez-Juricic, E., Martella, M.B., Alvarez, E.V., 1998a. Vocalizations of the bluefronted amazon (Amazona aestiva) in the Chancaní Reserve, Córdoba, Argentina. Wilson Bull. 110, 352–361. Fernandez-Juricic, E., Alvarez, E.V., Martella, M.B., 1998b. Vocalizations of bluecrowned conures (Aratinga acuticaudata) in the Chancaní Reserve, Córdoba, Argentina. Ornitol. Neotrop. 9, 31–40. Kleiman, D.G., 1977. Monogamy in mammals. Q. Rev. Biol. 52, 39–69. Kumar, A., 2003. Acoustic communication in birds: differences in songs and calls, their production and biological significance. Resonance 8, 44–55. Langbauer Jr., W.R., 2000. Elephant communication. Zoo Biol. 19, 425–445. Lasswell, H.D., 2007. The structure and function of communication in society. I˙ letis¸im kuram ve aras¸tırma dergisi 24, 215–228. Liebal, K., Pika, S., Tomasello, M., 2004. Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45, 41–57. Liebal, K., Call, J., 2012. The origins of non-human primates’ manual gestures. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 118–128. Maestripieri, D., 1999. The biology of human parenting: insights from nonhuman primates. Neurosci. Biobehav. Rev. 23, 411–422. Matyjasiak, P., 2004. Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male blackcaps. Behav. Ecol. 16, 467–471. McGregor, P.K., Peake, T.M., 2000. Communication networks: social environments for receiving and signalling behaviour. Acta Ethol. 2, 71–81. Moura, L.N., Silva, M.L., Vielliard, J.M.E., 2011. Vocal repertoire of wild breeding Orange-winged Parrot Amazona amazonica in Amazonia. Bioacoustics 20, 331–340. Pika, S., Bugnyar, T., 2011. The use of referential gestures in ravens (Corvus corax) in the wild. Nat. Commun. 2, 560. Prestes, N.P., Martinez, J., Meyers, P.A., Hansen, L.H., Xavier, M.N., 1997. Nest characteristics of the red-spectacled Amazon Amazona pretrei Temminck, 1830 (Psittacidae). Ararajuba 5, 151–158. Rendall, D., Owren, M.J., 2002. Animal vocal communication: say what? In: Bekoff, M., Allen, C., Burghardt, G. (Eds.), The Cognitive Animal. MIT Press, Cambridge, pp. 307–314. Sick, H., 1997. Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro. Snowdon, C.T., 2004. Social processes in the evolution of complex cognition and communication. In: Oller, D.K., Griebel, U. (Eds.), Evolution of Communication Systems – A Comparative Approach. MIT Press, Cambridge, pp. 131–150. Toyne, E.P., Flanagan, J.N.M., Jeffcote, M.T., 1995. Vocalizations of the endangered red-faced parrot Hapalopsittaca pyrrhops in southern Ecuador. Ornitol. Neotrop. 6, 125–128. Wachtmeister, C.A., 2001. Display in monogamous pairs: a review of empirical data and evolutionary explanations. Anim. Behav. 61, 861–868. Wirminghaus, J.O., Downs, C.T., Symes, C.T., Dempster, E., Perrin, M.R., 2000. Vocalisations and behaviours of the Cape Parrot Poicephalus robustus (Psittaciformes Psittacidae). Durban Mus. Novit. 25, 12–17. Woo, K.L., Rieucau, G., 2012. Aggressive signal design in the Jacky Dragon (Amphibolurus muricatus): display duration affects efficiency. Ethology 118, 157–168. Wright, T.F., Toft, C.A., Enkerlin-Hoeflich, E., Gonzalez-Elizondo, J., Albornoz, M., Rodríguez-Ferraro, A., et al., 2001. Nest poaching in neotropical parrots. Conserv. Biol. 15, 710–720.
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Gestural communication in a new world parrot Leiliany N. Moura a,∗ , Maria L. Silva a , Marilice M.F. Garotti b , Angélica L.F. Rodrigues a , Adrine C. Santos b , Ivete F. Ribeiro b a b
Laboratório de Ornitologia e Bioacústica, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Brazil Laboratório de Ecologia e Desenvolvimento, Núcleo de Teoria e Pesquisa do Comportamento, Universidade Federal do Pará, Belém, Brazil
a r t i c l e
i n f o
Article history: Received 9 October 2013 Received in revised form 25 February 2014 Accepted 1 March 2014 Keywords: Amazon parrots Biparental care Breeding behavior Communication Gestures
a b s t r a c t Male birds can use visual signals to provide information about their sexual status, via bright coloration, sophisticated sexual displays and elaborate tail and head crests. The majority of forest bird species use vocal communication as their main strategy to show their physiological status during breeding season. It is also used to keep contact between individuals in the same group, in agonistic contexts, and by chicks begging for food. We registered, for the very first time, gestural communication acting in the context of biparental care for the Orange-winged Amazon, Amazona amazonica. This parrot presents at least nine different sounds uttered in contexts of alarm, agonistic, foraging, contact flight and others. This finding suggests that despite being a vocal species, this parrot can perform gestural communication related to parental care. The gestures exhibited by this species represent a strategy for survival, a clever way to protect the nest, reducing the risk of attracting the attention of predators. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Acoustic and visual communication systems related to mating selection, parental care, and agonistic conflicts can be observed among birds (Catchpole and Slater, 2008; Matyjasiak, 2004; Moura et al., 2011). Parrots use acoustic signals as a primary source of communication, and the vocal repertoire of some species has been described elsewhere (Fernandez-Juricic et al., 1998a,b; Toyne et al., 1995; Wirminghaus et al., 2000). The Orange-winged Amazon, Amazona amazonica, utters nine vocalizations in different behavioral contexts, such as to maintain pair and group contact, in dangerous (three types of alarm call) and agonistic situations (Moura et al., 2011). Gestural communication is a visual signal that acts over short distances and is quickly attenuated or hidden by objects in the environment. It must be transmitted in places with a minimum amount of light intensity (Bradbury, 1998; Langbauer, 2000). Gestures can be defined as non-verbal communication in which a visible corporal action communicates a particular message (Liebal and Call,
∗ Corresponding author at: Laboratório de Ornitologia e Bioacústica, Instituto de Ciências Biológicas, Universidade Federal do Pará, Augusto Corrêa, 01, Guamá, 66075110 Belém, Pará, Brazil. Tel.: +55 9132018230. E-mail addresses: [email protected], [email protected] (L.N. Moura), [email protected] (M.L. Silva), [email protected] (M.M.F. Garotti), [email protected] (A.L.F. Rodrigues), drica [email protected] (A.C. Santos), [email protected] (I.F. Ribeiro). http://dx.doi.org/10.1016/j.beproc.2014.03.003 0376-6357/© 2014 Elsevier B.V. All rights reserved.
2012). It requires participation of a receiver to attend to a particular proposal. In this case the sender waits for an answer from the receiver and/or looks at the receiver and keeps displaying the gesture when an appropriate answer is not given. Unlike vocal communication, which can be highly conspicuous, gestural signals are highly directional, and animals that use them to communicate can avoid predators (Bradbury, 1998). Orange-winged Amazons are sexually monomorphic and monogamous for life (Sick, 1997). They nest in tree cavities and the courtship behavior is characterized by male feeding female. This species presents a long incubation period (about 30 days), nestlings are altricial, hatch asynchronously in small broods, and have a low survival rate. These characteristics may lead to pair-bond formation and cooperation in parental care (Moura et al., 2011). The aim of this study is to describe gestural communication in Orange-winged Amazons: a complex sequence of postural movements used by pairs as breeding behavior. This behavior was not described before in captivity or in nature. We have found the unexpected gestures in biparental context during observations of reproductive behavior. 2. Methods The study was conducted in nest sites of Orange-winged Amazons that are associated with open areas on plantations and on the forest edge, spanning 278 km2 , in a privately owned land in Santa Bárbara do Pará, North Brazil (01◦ 12 17 S; 48◦ 18 05 W).
L.N. Moura et al. / Behavioural Processes 105 (2014) 46–48
47
3.1. Gestural communication I: inducing the female to approach and enter the nest
Fig. 1. (A) Gestures performed by male to encourage female to enter the nest. (B) Gestures performed by male to encourage the female to enter and/or to leave the nest.
Of the 15 episodes observed, the presumed male used this type of gestural communication in 14 observations. For this the male perched near the nest-tree and, apparently, after checking for predators, signaled to the presumed female, which was in a nearby tree, that she could approach the nest. The gestural communication I was done by the male raising himself up momentarily and quickly bending his head back by about 45◦ , at a speed of 0.12 ± 0.04 m/s (Fig. 1A), until the female approached and looked toward him. After the female looked at the male, he performed a downward head movement, at a speed of 0.05 ± 0.03 m/s, signaling to encourage her to enter the nest (Fig. 1B). When she did not enter the nest, he moved his head down again and waited for the answer, or moved himself out to a more visible perch where she could see him and repeated the head-down movement, until she entered the nest. In one observation the male perched in the nesttree, and after signaling to the female, which was perched in a tree about 2 m away, he performed a head-down movement and 3 s later she entered the nest cavity. The whole gestural sequence was performed without vocalization and the female entered the nest on average 6.5 ± 6.8 min after the male start signaling.
By Leiliany Moura and Madlene Cardoso.
3.2. Gestural communication II: signaling to the female to leave the nest Field visits were made to 16 active nest sites, from 2005 to 2011, totaling 111 observations (continuous recording technique), each from 5h40 to 11h00 and from 15h30 to 19h00, throughout six breeding seasons, once a week. This study covered the whole breeding season, which in the Amazon region begins in late August and extends into January. Some visual displays were recorded using digital cameras (Canon Powershot S2Is and Panasonic Lumix DMC-FZ18) for posterior analysis. Data were expressed as means ± standard deviation.
This behavior was observed in seven episodes and resulted in the exit of females from the nest. For this purpose, the male perched in the nest-tree and signaled moving his head down (Fig. 1B) until the female left the cavity. This took on average 7.4 ± 7.9 min after signaling is initiated. In most of the observations (93%) of females leaving the nest, however, the male did not perform gestural signs. Instead, he perched near the nest-tree and emitted a specific vocalization until she put her head outside the nest (see Moura et al., 2011). Thus, the use of gestures to encourage the female to leave the nest occurred secondarily.
3. Results 4. Discussion The breeding season of parrots was observed over six breeding seasons, with the initial objective of studying the reproductive and vocal behavior of pairs. It was not expected to find gestural communication during the study. According to our observations, a pair waits four months between the egg-laying and the flight of young. However, as the onset of the reproductive effort is asynchronous among pairs, the breeding season extents for about six months. During the incubation period (about four weeks) and early nestling period (about eight weeks) the female of Orange-winged Amazon leaves the nest cavity twice a day to be fed by the male. Later, when the chicks are feathered and do not need to be brooded by the parents, the female does not spend the night in the nest cavity anymore, but the pair keep feeding the chicks twice a day (for about four weeks). We observed the females entering the nest 101 times, in which it was registered 15 episodes (15%) of gestural communication emitted by the presumed male (there is no sexual dimorphism). This signaling resulted in the female approaching and entering the nest cavity following gestural communication I (Fig. 1A and B), five times in the morning and 10 times in the afternoon. We also observed the females leaving the nest 98 times, and seven times (7%) that behavior happened after the male performed a gestural sign following gestural communication II (Fig. 1B). The gestural communication was observed only for a period of about two months of reproductive season: in the early nestling period, soon after hatching until the chicks are fully feathered.
Our long-term investigation of the breeding behavior of A. amazonica permitted the above description of two gestural communication patterns in a biparental care context in the wild. These results show a special non-vocal communication around the nest of this parrot species, which uses vocal communication most of the time, probably as an adaptation to avoid attention from predators. The signal to make the female exit the nest was mostly performed with male vocalizations. It is plausible to think that in this case it was necessary to use an alternative signaling method in a situation where vision is not entirely possible, given that the female is inside the nest cavity at that moment. The observations shown herein provide important information regarding the complex social communication strategies among these birds through a different modality – visual. Animal species with a social complex structure show complex communication systems (Cheney et al., 1986; Rendall and Owren, 2002; Snowdon, 2004). Group life and parental care demand highenergy rates and a specific communication system to allow the proper expression of physiological status for mating, social hierarchy, and actions against threats to survival (Kumar, 2003; Lasswell, 2007; McGregor and Peake, 2000). Various factors can affect the size of the communication repertoire, including the flexibility of social structure. In non-human primates, societies in which the hierarchical system is not as rigid and shows egalitarian tendencies, communication repertoires
48
L.N. Moura et al. / Behavioural Processes 105 (2014) 46–48
tend to be wider because these species need to negotiate more (Maestripieri, 1999). When predictions based on ecological, social, and cognitive criteria were considered, Liebal et al. (2004) concluded that Siamangs, Symphalangus syndactylus, used a wider repertoire of non-vocal communicative signals than expected. Indeed, these authors have registered 31 non-vocal signals within gestures, tactile signals, and facial expressions in these primates. The monogamous mating system lacks a dominance hierarchy and is characterized by a strong bonding between the adult male and female (Kleiman, 1977). Siamangs and Psittacidae present longterm monogamy. Despite being distant in the phylogenetic tree, the high energy cost of their mating system leads to the maintenance of a strong bond between males and females. Thus, these animals may develop sophisticated communication systems that will insure their survival, that of their offspring, and consequently that of their species (Wachtmeister, 2001). As mentioned in the introduction, Orange-winged Amazons have a sophisticated acoustic communication system and a priori can convey information in various behavioral contexts. Indeed, for alerting imminent danger they have three different alarm calls, besides having contact call, food call, agonistic call, and other distress calls (Moura et al., 2011). Our data reveal that these parrots have an even more complex communication repertoire because males present two specific gestural sequences. This observation is intriguing because in this context, the use of gestural communication toward the receptor is independent of individual sender self-necessities and occurred without the presence of a real immediate danger. It is possible that these gestural sequences are used to warn of possible threats toward the offspring and are performed in silence as a strategy to avoid calling the attention of potential predators in the area surrounding the nest. Nevertheless, further studies will be necessary to confirm this supposition. Considering the entire reproductive season, only in two of four months it was observed gestural communication: in the early nestling period. This is a period in which the nestlings are completely dependent on parental care and are more vulnerable to intruders or predators. It is probably for this reason that pairs of Orange-winged Amazon use gestures instead of vocal communication in this situation. In addition to being subject to predators, parrots are frequently exposed to poachers that harvest them to sell as pet in illegal wildlife trade (Prestes et al., 1997; Wright et al., 2001). During the breeding seasons studied here, 11 out of 16 nests observed were either predated (n = 4) or harvested by poachers (n = 7). Thus, there is a need to increase the protection of nest sites. An environment with many dead trees, where animal species select some tree hole cavities to build nests instead of others, is not easy to be sure in which one the nest was built. Therefore, the movement to enter or to leave the nest is the best way to discover a parrot nest, and it is possible that these moments are crucial for their reproductive success. The results reported here show for the first time evidence of gestural communication in the context of biparental care in Orangewinged Amazons. Most gestural communication data published elsewhere refer to physiological and hierarchical status of the individual sender specifically connected to the necessities of the self. Indeed, authors have reviewed the literature on such gestural repertoires among birds, mammals, and some reptiles but connection with necessities of the self were always very clear
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