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Vocal repertoire and group-specific signature in the Smooth-billed Ani, Crotophaga ani Linnaeus, 1758 (Cuculiformes, Aves)

Abstract

Vocal plasticity reflects the ability of animals to vary vocalizations according to context (vocal repertoire) as well as to develop vocal convergence (vocal group signature) in the interaction of members in social groups. This feature has been largely reported for oscine, psittacine and trochilid birds, but little has been investigated in birds that present innate vocalization. The smooth-billed ani (Crotophaga ani) is a social bird that lives in groups between two and twenty individuals, and which presents innate vocalization. Here we analyzed the vocal repertoire of this species during group activities, and further investigated the existence of a vocal group signature. The study was conducted in the Southeast of Brazil between May 2017 and April 2018. Two groups of smooth-billed anis were followed, Guararema and Charqueada groups, and their vocalizations were recorded and contextualized as to the performed behavior. The vocal repertoire was analyzed for its composition, context and acoustic variables. The acoustic parameters maximum peak frequency, maximum fundamental frequency, minimum frequency, maximum frequency and duration were analyzed. To verify the vocal signature of the group, we tested whether there was variation in the acoustic parameters between the monitored groups. We recorded ten vocalizations that constituted the vocal repertoire of the Smooth-billed Ani, five of which (“Ahnee”, “Whine”, “Pre-flight”, “Flight” and “Vigil”) were issued by the two groups and five exclusive to the Charqueada group. There were significant differences in the acoustic parameters for “Flight” and “Vigil” vocalizations between the groups, suggesting vocal group signature for these sounds. We established that the Smooth-billed Ani has a diverse vocal repertoire, with variations also occurring between groups of the same population. Moreover, we found evidence of vocal group signature in vocalizations used in the context of cohesion, defense and territory maintenance.

Keywords.
Vocal communication; Behavior; Vocal plasticity; Vocal group signature

INTRODUCTION

Acoustic communication is generally used for recognition among individuals (Beecher, 1988Beecher, M.D. 1988. Kin recognation in birds. Behavior Genetics, 18(4): 465-482.; Berg et al., 2011Berg, K.S.; Delgado, S.; Okawa, R.; Beissinger, S.R. & Bradbury, J.W. 2011. Contact calls are used for individuals mate recognition in free-ranging Green-rumped Parrotlets, Forpus passerines. Animal Behaviour, 81: 241-248.; Elie & Theunissen, 2018Elie, J.E. & Theunissen, F.E. 2018. Zebra finches identify individuals using vocal signatures unique to each call type. Nature Communications, 9: 4026. http://doi.org/10.1038/s41467-018-06394-9
http://doi.org/10.1038/s41467-018-06394-...
; Benti et al., 2019Benti, B.; Curé, C. & Dufour, V. 2019. Individual signature in the most common and context-independent call of the Rook (Corvus frugilegus). The Wilson Journal of Ornithology, 131(2): 373-381.); acquisition of information about populations (Salinas-Melgoza & Wright, 2012Salinas-Melgoza, A. & Wright, T.F. 2012. Evidence for vocal learning and limited dispersal as dual mechanisms for dialect maintenance in a parrot. PLoS ONE, 7: e48667.); and vocal labeling, especially among social birds (Wanker et al., 2005Wanker, R.; Sugama, Y. & Prinage, S. 2005. Vocal labelling of family members in Spectacled Parrotlets, Forpus conspicillatus. Animal Behaviour, 70(1): 111-118.). The use of a vocalization associated with a specific context is related to the bird’s experience in using the respective signal (Janik & Slater, 2000Janik, V.M. & Slater, P.J.B. 2000. The different roles of social learning in vocal communication. Animal Behaviour, 60: 1-11.). Thus, the study of vocal repertoire provides information on how an animal interacts with other species (e.g.,Hurd, 1996Hurd, C.R. 1996. Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus). Behavioral Ecology and Sociobiology, 38(4): 287-292.; Kort & Cate, 2001Kort, S.R. & Cate, C.T. 2001. Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Animal Behaviour, 61: 239-247.; Goodale & Kotagama, 2006Goodale, E. & Kotagama, S.W. 2006. Context-dependent vocal mimicry in a passerine Bird. Proceedings of the Royal Society B, 273(1588): 875-880. http://doi.org/10.1098/rspb.2005.3392
http://doi.org/10.1098/rspb.2005.3392...
), with members of its own species, and with the environment.

The vocal plasticity of some bird species allows acoustic variations that can better adjust a vocalization to a specific environment noise profiles (Brumm et al., 2009Brumm, H.; Schmidt, R. & Schrader, L. 2009. Noise-dependent vocal plasticity in domestic fowl. Animal Behaviour, 78(3): 741-746.; Hardman et al., 2017Hardman, S.I.; Zollinger, S.A.; Koselj, K.; Leitner, S.; Marshall, R.C. & Brumm, H. 2017. Lombard effect onset times reveal the speed of vocal plasticity in a songbird. Journal of Experimental Biology, 220(6): 1065-1071. http://doi.org/10.1242/jeb.148734
http://doi.org/10.1242/jeb.148734...
; Lazerte et al., 2017Lazerte, S.E.; Otter, K.A. & Slabbekoorn, H. 2017. Mountain Chickadees adjust songs, calls and chorus composition with increasing ambient and experimental anthropogenic noise. Urban Ecosystems, 20(5): 989-1000.), change some vocal characteristic of adult animals based on experience and context learned throughout life (James & Sakata, 2019James, L.S. & Sakata, J.T. 2019. Developmental modulation and predictability of age-dependent vocal plasticity in adult Zebra Finches. Brain Research, 1721: 146336. http://doi.org/10.1016/j.brainres.2019.146336
http://doi.org/10.1016/j.brainres.2019.1...
), or to interact within a social system, resulting in vocal convergence or a vocal group signature (Mammen & Nowicki, 1981Mammen, D.L. & Nowicki, S. 1981. Individual differences and within-flock convergence in Chickadee calls. Behavioral Ecology and Sociobiology, 9(3): 179-186.; Tyack, 2008Tyack, P.L. 2008. Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. Journal of Comparative Psychology, 122(3): 319-331.; Martins et al., 2018Martins, B.A.; Rodrigues, G.S.R. & Araújo, C.B. 2018. Vocal dialects and their implications for reintroductions. Perspectives in Ecology and Conservation, 16: 83-80.; Elie & Theunissen, 2018Elie, J.E. & Theunissen, F.E. 2018. Zebra finches identify individuals using vocal signatures unique to each call type. Nature Communications, 9: 4026. http://doi.org/10.1038/s41467-018-06394-9
http://doi.org/10.1038/s41467-018-06394-...
; Benti et al., 2019Benti, B.; Curé, C. & Dufour, V. 2019. Individual signature in the most common and context-independent call of the Rook (Corvus frugilegus). The Wilson Journal of Ornithology, 131(2): 373-381.).

Vocal group signatures are found in animal species that build stable social groups (Boughman, 1998Boughman, J.W. 1998. Vocal learning by greater spear-nosed bats. Proceedings of the Royal Society of London , Series B: Biological Sciences, 265(1392): 227-233.; Sharp et al., 2005Sharp, S.P.; Mcgowan, A.; Wood, M.J. & Hatchwell, B.J. 2005. Learned kin recognition cues in a social bird. Nature, 434(7037): 1127-1129.; Benti et al., 2019Benti, B.; Curé, C. & Dufour, V. 2019. Individual signature in the most common and context-independent call of the Rook (Corvus frugilegus). The Wilson Journal of Ornithology, 131(2): 373-381.). Such signatures can have multiple implications, including group cohesion during flight or foraging (Ford, 1991Ford, J.K.B. 1991. Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Canadian Journal of Zoology, 69(6): 1454-1483.; Boughman, 1998Boughman, J.W. 1998. Vocal learning by greater spear-nosed bats. Proceedings of the Royal Society of London , Series B: Biological Sciences, 265(1392): 227-233.; Hile & Striedter, 2000Hile, A.G. & Striedter, G.F. 2000. Call convergence within groups of female Budgerigars (Melopsittacus undulatus). Ethology, 106(12): 1105-1114.), interactions with social partners (Vehrencamp et al., 2003Vehrencamp, S.L.; Ritter, A.R.; Keever, M. & Bradbury, J.W. 2003. Responses to playback of local versus distant contact calls in the Orange-fronted Conure, Aratinga canicularis. Ethology, 109: 37-54.; Radford, 2005Radford, A.N. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behaviour, 70(5): 1227-1234.), and even allows the inclusion or exclusion of non-group members (Tyack, 2008Tyack, P.L. 2008. Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. Journal of Comparative Psychology, 122(3): 319-331.; Salinas-Melgoza & Wright, 2012Salinas-Melgoza, A. & Wright, T.F. 2012. Evidence for vocal learning and limited dispersal as dual mechanisms for dialect maintenance in a parrot. PLoS ONE, 7: e48667.). In the case of exclusion of non-group members, a vocal group signature acts as a password (Tyack, 2008Tyack, P.L. 2008. Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. Journal of Comparative Psychology, 122(3): 319-331.) that allows, for instance, access to shared resources among group members. As a result, animals living in stable social groups may benefit from improved access to food resources, either through foraging or group defense (Krebs et al., 1972Krebs, J.R.; Macroberts, M.H. & Cullen, J.M. 1972. Flocking and feeding in the Great Tit Parus major: an experimental study. Ibis, 114(4): 507-530.; Rabenold, 1987Rabenold, P.P. 1987. Recruitment to food in black vultures: evidence for following from communal roosts. Animal Behaviour, 35(6): 1775-1785.; Brown, 1988Brown, C.R. 1988. Social foraging in Cliff Swallows: local enhancement, risk sensitivity, competition and the avoidance of predators. Animal Behaviour, 36(3): 780-792.; Wilkinson, 1992Wilkinson, G.S. 1992. Information transfer at evening bat colonies. Animal Behaviour, 44(3): 501-518.; Brown & Brown, 1996Brown, C.R. & Brown, M.B. 1996. Coloniality in the Cliff Swallow. Chicago, The University of Chicago Press.; Elie & Theunissen, 2018Elie, J.E. & Theunissen, F.E. 2018. Zebra finches identify individuals using vocal signatures unique to each call type. Nature Communications, 9: 4026. http://doi.org/10.1038/s41467-018-06394-9
http://doi.org/10.1038/s41467-018-06394-...
).

However, vocal convergence or development of a vocal group signature depends on vocal learning (Bradbury & Vehrencamp, 1998Bradbury, J.W. & Vehrencamp, S.L. 1998. Principles of animal communication. Massachusets, Sinauer Press.). Therefore, vocal signatures have been associated to birds that learn vocalizations, such as Songbirds (Nowicki, 1983Nowicki, S. 1983. Flock-specific recognation of chickadee calls. Behavioral Ecology and Sociobiology, 12(4): 317-320., 1989Nowicki, S. 1989. Vocal plasticity in captive Black-capped Chickadees: the acoustic basis and rate of call convergence. Animal Behaviour, 37: 64-73.; Camacho-Schlenker et al., 2011Camacho-Schlenker, S.; Courvoisier, H. & Aubin, T. 2011. Song sharing and singing strategies in the Winter Wren Troglodytes troglodytes. Behavioural Processes, 87(3): 260-267.), Psittaciformes (Hile & Striedter, 2000Hile, A.G. & Striedter, G.F. 2000. Call convergence within groups of female Budgerigars (Melopsittacus undulatus). Ethology, 106(12): 1105-1114.; Berg et al., 2011Berg, K.S.; Delgado, S.; Okawa, R.; Beissinger, S.R. & Bradbury, J.W. 2011. Contact calls are used for individuals mate recognition in free-ranging Green-rumped Parrotlets, Forpus passerines. Animal Behaviour, 81: 241-248.; Martins et al., 2018Martins, B.A.; Rodrigues, G.S.R. & Araújo, C.B. 2018. Vocal dialects and their implications for reintroductions. Perspectives in Ecology and Conservation, 16: 83-80.) and Trochilidae (Araya-Salas et al., 2019Araya-Salas, M.; Smith-Vidaurre, G.; Mennill, D.J.; Gonzáles-Gomes, P.L.; Cahill, J. & Wright, T.F. 2019. Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning. Proceedings of Royal Society B, 286(1903): 20190666.. These birds have regions of the telencephalon that are responsible for vocal learning and that have morphological similarity between these groups (Jarvis et al., 2000Jarvis, E.D.; Ribeiro, S.; da Silva, M.L.; Ventura, D.; Vielliard, J. & Mello, C.V. 2000. Behaviour ally driven gene expression reveals song nuclei in hummingbird brain. Nature, 406(6796): 628-632. http://doi.org/10.1038/35020570
http://doi.org/10.1038/35020570...
).

On the other hand, vocal group signature studies with bird groups of innate vocalization are scarce (Baker, 2004Baker, M.C. 2004. The chorus song of cooperatively breeding Laughing Kookaburras (Coraciiformes, Halcyonidae: Dacelo novaeguineae): characterization and comparison among groups. Ethology, 110: 21-35.; Radford, 2005Radford, A.N. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behaviour, 70(5): 1227-1234.). Among these innate vocalizations birds, the Smooth-billed Ani (Crotophaga ani Linnaeus, 1758) can be highlighted.

The Smooth-billed Ani is a social bird, living in groups of two to more than twenty members, with an average of seven individuals. They use communal nests and cooperate to maximize the survival of the group (Davis, 1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.), and are widely seen in cultivated regions and in open landscapes with shrubs. These animals present uniform black color, a high beak, and length of about 36 cm. They are poor fliers, with little wind resistance (Sick, 2001Sick, H. 2001. Ornitologia brasileira. Rio de Janeiro, Editora Nova Fronteira.). This species occurs in the American continent, from Florida to Argentina and throughout Brazil and is mainly insectivorous, feeding largely on arthropods such as spiders, bedbugs and locusts (Sick, 2001Sick, H. 2001. Ornitologia brasileira. Rio de Janeiro, Editora Nova Fronteira.).

The vocal repertoire of the Smooth-billed Ani has been studied in Cuba (Davis, 1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and Puerto Rico (Grieves, 2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.) by analysis of the bird’s acoustic parameters, and associated with the bird’s behavior. However, no study has been conducted in other localities of the American continent in order to identify how this repertoire occurs in different populations. Furthermore, the existence of vocal signature in this group has not yet been investigated.

Considering the limited number of studies on the vocal communication of the Smooth-billed Ani (Davis, 1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.; Grieves, 2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.; Grieves et al., 2015Grieves, L.A.; Logue, D.M. & Quinn, J.S. 2015. Vocal repertoire of cooperatively breeding Smooth-billed Anis. Journal of Field Ornithololy, 86(2): 130-143.), the present work had the following aims: (1) To describe the vocal repertoire of the species in the Southeast of Brazil and the context of its vocalizations; (2) to verify whether there are differences in its vocal repertoire with geographical variation; and (3) to assess the occurrence of a vocal group signature in this species.

MATERIAL AND METHODS

Study area

The data was collected in the municipality of Alegre, state of Espírito Santo, in the Southeast of Brazil. The predominant biome in this area is the Atlantic Forest, with tropical and humid Cwa climate characterized by hot and rainy summer and cool and dry winter. The mean annual temperature is 23.1ºC, varying between 16.9 ºC and 29.0 ºC, and the total annual precipitation amounts to 1,341 mm (Lima et al., 2008Lima, J.S.S.; Silva, S.A.; Oliveira, R.B.; Cecílio, R.A. & Xavier, A.C. 2008. Variabilidade temporal da precipitação mensal em Alegre, ES. Revista Ciência Agronômica, 39(2): 327-332.).

Two groups were sampled in different areas (one in Guararema and the other in Charqueada) (Fig. 1), apart by a distance of 3.5 km. These areas are characterized by the cultivation of eucalyptus, coffee, fruits and bamboo, with few farmhouses, dirt roads, and little traffic.

Figure 1
Location of the studied groups of Smooth-billed Ani in the municipality of Alegre, ES, Brazil.

Acoustic data

Sampling was carried out between May 2017 and April 2018. Observations and data collection occurred twice a month for each Smooth-billed Ani group, being performed from 06.00 until 10.00 a.m. and from 04.00 p.m. until the return to the roost in the late afternoon. We recorded vocalizations from the two distinct groups, a group identified as Charqueada formed by 7 individuals, and the other group called Guararema with 10 individuals. Because Smooth-billed Anis are very territorial, occupying the same territory and roost tree for a long period, the groups in this study were accompanied when leaving as well as returning to the same roost, which allowed distinguishing the flocks. During data collection, the displacement areas of the groups were different, further suggesting that the two groups were distinct and did not meet during the field work.

For the collection of behavioral data, we adopted the ad libitum (Altmann, 1974Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49(3-4): 227-266.) methodology, in which the observer freely records the behaviors of the individuals in a non-systematic way, from the moment of encountering them until the loss of visual contact, without time restrictions. A Celestron 8 × 21 binocular was used for the observations. If the birds vocalized, the vocalization was recorded and associated with the observed behavior. There were two observers, one for recording bird vocalizations and the other for observing and recording behaviors. Behavior collection was always performed by the same observer so as to avoid divergences in the behavior identification.

The recordings were always made from a distance of 10-15 meters so as not to interfere with the behavior of the observed population. Recordings were made with a Sony Icd-px240 digital voice recorder and a Sennheiser MKE600 (40-20,000 Hz) directional microphone. The vocalizations were recorded in MP3 and transformed to WAVE using the software Audacity version 2.4.0. After the transformation, the voices were analyzed in the WAVE format with 44.1-KHz, 16-bit sampling frequency. Considering that each flock comprised several individuals, and the recordings were made on different days and months, it is expected that the recordings of several individuals in the flock contribute to the group sampling as a whole, as well as to the identification of a vocal group signature.

Data analysis

To analyze Smooth-billed Ani’s vocal repertoire, the vocalizations were categorized according to their structure and context. To define the context, the behavior was associated to the bird’s vocalization. The nomenclature for vocalization was based on the context and followed the denominations proposed by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), who worked with this species in Puerto Rico. If no literature was available to designate the voicing, it was named according to the related behavior observed.

The vocalizations that are part of the vocal repertoire were also characterized in terms of the number of syllables, number of notes and the presence and absence of harmonics (Fig. 2). The recorded vocalizations with different structures, but same context were considered as the same voice, since the context was the same.

Figure 2
Song structure of the Smooth-billed Ani showing the notes, sillable and harmonic.

To compare the vocal repertoire we used the acoustic parameters “maximum peak frequency” (MPF), “maximum fundamental frequency” (MFF), “minimum frequency” (or low frequency) (MIF), “maximum frequency” (or high frequency) (MAF) and “duration” (DUR), obtained with the aid of the Avisoft-SASLab Lite software, version 5.1.22 (FFT lenght = 64; Frame = 100%; Window = Hamming; Bandwidth = 896 Hz; Resolution = 689 Hz). In Avisoft-SASLab software, after generating the spectogram, we use the option “activate rectangular cursor” to select the voice and in the tools tab, we click on “automatic parameter measurements setup” to select the acoustic parameters.

The acoustic parameters used to compare the geographical variation between the data obtained in our work with those from Puerto Rico (Grieves, 2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.) were MPF, MIF, MAF and Dur. To verify vocal group signature, we checked if there was a statistical difference between the parameters MPF, MFF, MIF, MAF and Dur of the voices of the groups Charqueada and Guararema. These acoustic variables were tested for normality using the Shapiro-Wilk test. We used the Mann-Whitney test for non-parametric data and analysis of variance (ANOVA) for parametric data. The analyses were performed in the R Studio software (RStudio Team, 2016RStudio Team. 2016. RStudio: Integrated development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com.
http://www.rstudio.com...
).

RESULTS

A total of 207 vocalizations were obtained, of which 135 vocalizations were from the Charqueada group and 72 from the Guararema group. We identified ten vocal behaviors, constituting the vocal repertoire of the Smooth-billed Ani. Each vocalization was characterized in the context in which it was produced, and according to its structure (Table 1). Two vocalizations, “INR” and “Vigil”, were only verified in the present population, of which “INR” was less frequent (n = 8) in the recordings and only for the Charqueada group. The “Vigil” vocalization was more frequent and in both Smooth-billed Ani groups (15 recordings for Guararema group and 29 for Charqueada group).

Table 1
Vocal repertoire of the Smooth-billed Ani. Char = Charqueada group, Guar = Guararema group.

The vocalizations “Whine”, “Flight” and “INR” presented different structures in the same context. The “Whine” vocalization had six different structures (Figs. 2B, C, D, E, F and G), varying between 2 and 3 notes and in the presence or absence of harmonics. The sounds “Flight” and “INR” showed variation in the number of notes, with 2 or 3 notes each (Table 1, Fig. 3).

Figure 3
Spectrograms of the ten types of vocalizations of the Smooth-billed Ani: “Ahnee” (A), “Whine” (B, C, D, E, F and G), “Pre-flight” (H), “Shout” (I), “Flight” (J and K), “Hoot” (L), “Grunt” (M), “Ee-oo-ee” (N), “Vigil” (O), “INR” (P and Q).

“Ahnee”, “Whine”, “Pre-flight”, “Flight”, “Grunt”, “Shout”, “Hoot” and “Ee-oo-ee” were also recorded in the vocal repertoire of Smooth-billed Ani by other authors (Davis, 1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.). When comparing our data with those available by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), it we observed that the mean values for the parameter “maximum mean frequency” were higher for the present population in all similar vocalizations, while for the parameters “minimum frequency” and “maximum peak frequency” the means were higher for the population studied by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), except for “Hoot” sounds. The parameter “duration” had higher values in our study for the sounds “Ahnee”, “Pre-flight”, “Shout”, “Hoot” and “Ee-oo-ee”, while the other vocalizations had shorter duration by comparison (Table 2).

Table 2
Mean values (± SD) for the acoustic parameters of similar vocalizations between the data by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.) and those obtained in this work.

We also observed a variation in the vocal repertoire between the Guararema and Charqueada groups. Although the field sampling effort was similar between Smooth-billed Ani groups (Charqueada = 1,271 minutes and Guararema = 1,129 minutes), the number of vocal records was different, with 135 vocalizations recorded for the Charqueada group and 72 for the Guararema group. The Charqueada group also had a greater number of vocal behaviors (n = 10) than the Guararema group (n = 5) (Table 1). “Whine” (n = 31), “Flight” (n = 29) and “Vigil” (n = 27) were the most recorded vocalizations in the Charqueada group, while in the Guararema group “Flight” was the most frequent (n = 37).

The vocalizations “Ahnee”, “Whine”, “Pre-flight”, “Flight” and “Vigil” were recorded for both groups (Charqueada and Guararema) (Fig. 4), while “INR”, “Ee-oo-ee”, “Hoot”, “Grunt” and “Shout” were only verified for the Charqueada group. There were no vocalizations exclusive to the Guararema group (Table 1).

The vocal group signature were verified to “Flight” and “Vigil” vocalizations, in which there were statistical differences between the groups (Tables 3 and 4). For “Flight”, the variation occurred in the parameter MIF (Wilcox-test = 657.5, degrees of freedom [df] = 1, p = 0.0292), whereas for “Vigil”, variation was detected in MAF (Wilcox-test = 117, df = 1, p = 0.0489) and MPF (Wilcox-test = 110.5, df = 1, p = 0.0281), suggesting a vocal group signature for these vocalizations.

Figure 4
Boxplots (median and quartiles) of acoustic parameters of the similar vocalizations of Charqueada and Guararema groups of Smooth-billed Ani. Vocalizations: “Ahnee”, “Whine”, “Pre-flight”, “Flight” and “Vigil”. Acoustic parameters: DUR = duration; MPF = maximum peak frequency; MFF = maximum fundamental frequency; MIF = minimum frequency; MAF = maximum frequency.

Table 3
Mean values (± SD) for the acoustic parameters of similar vocalizations between the Smooth-billed Ani groups, Guararema (Guar) and Charqueada (Char). DUR = Duration; MAF = Maximum frequency; MIF = Minimum frequency; MFF = Maximum fundamental frequency; MPF = Maximum peak frequency. * Statistical difference between areas.

Table 4
T test and Mann-Whitney values comparing similar vocalizations between the Smooth-billed Ani groups, Charqueada and Guararema. df = Degrees of freedom; DUR = Duration; MAF = Maximum frequency; MIF = Minimum frequency; MFF = Maximum fundamental frequency; MPF = Maximum peak frequency. * Statistical difference.

DISCUSSION

Here ten vocalizations were recorded in the observed Smooth-billed Ani population, compared to 13 vocalizations reported by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.) in Puerto Rico and 11 by Davis (1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) in Cuba.

Such difference in the vocal repertoire of these birds may be related to the period of data sampling. The vocalizations that were recorded only by Davis (1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), were associated to defense and protection of the nests. They recorded voices associated with defense of the nests and danger behavior, as “Alarm call”, “Quack”, “Whew” (Davis, 1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and “Ahnee alarm”, “Chlurps”, “Chucks” (Grieves, 2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), and related to the presence of birds in the nests, as “Complaint”, “Objecting”, “Chuckle” in Davis (1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and “Growls” and “Whistle” in Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.).

The recording of these vocalizations by these authors but not by us could be because the sampling effort of the work of these authors was all during the breeding season, which may have increased the chances of recording these types of vocal behaviors. On the other hand, we distribute our sampling effort in the two phases of the animal’s life, reproductive and non-reproductive period, which may have decreased our chances of recording vocalizations associated with reproductive behavior, but favored the possibility of recording the vocalization of “Vigil”, associated with the vigilance behavior during group foraging.

The vocalizations recorded only in this study were “Vigil” and “INR”. The first voice was frequent in our study, while the second one (“INR”) was less frequent, and only in one of the groups. The “INR” sound was considered as a different vocalization from “Whine” because, despite having the same context of the bird within the roost, it does not precede the bird’s departure from the roost, but rather its remaining in it. This different voices recorded in this study and by others authors demonstrating a variation in the vocal repertoire of the Smooth-billed Ani populations.

The vocal repertoire of the species is composed by at least ten different types of vocalizations, eight (“Ahnee”, “Pre-flight”, “Flight”, “Grunt”, “Shout”, “Hooot”, “Ee-oo-ee” and “Whine”) were also mentioned by Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), and five (“Ahnee”, “Grunt”, “Hoot”, “Shout” and “Whine”) by Davis (1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.). Despite this variation in vocal repertoire in relation to the observations of Davis (1940Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.) and Grieves (2014Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani. Hamilton, Ontario (Master Dissertation). McMaster University.), it can be said that Smooth-billed Anis have a well-defined repertoire, characterized by vocalizations like “Ahnee”, “Whine”, “Pre-flight”, “Flight”, “Grunt”, “Shout”, “Hoot” and “Eo-e-ee”, as they occur in more than one population. Moreover, the fact that one or more vocalizations have not been detected in all studies does not necessarily mean that they do not integrate the repertoire, but rather that they may just not have been recorded in a specific sampling period.

Vocal repertoire variations have been studied in other birds with less or more elaborate repertoires. For instance, the great curassow (Crax rubra) has been reported to exhibit only five vocalization types, of which two are sex-specific (Baldo & Mennill, 2011Baldo, S. & Mennill, D.J. 2011. Vocal behavior of Great Curassows, a vulnerable Neotropical Bird. Journal of Field Ornithology, 82(3): 249-258. http://doi.org/10.1111/j.1557-9263.2011.00328.x
http://doi.org/10.1111/j.1557-9263.2011....
), whereas the Niceforo’s wren (Thryophilus nicefori) displays 21 sound types, with sexual variation in the vocal repertoire, ranging from 12 to 21 sound types in males and 7 to 9 in females (Valderrama et al., 2008Valderrama, S.; Parra, J.; Dávila, N. & Mennill, D.J. 2008. Vocal BehaVior of the critically endangered Niceforo’s Wren (Thryothorus nicefori). The Auk, 125(2): 395-401.). Compared with variation of these extremes, Smooth-billed Anis have a well-diversified repertoire.

Another important aspect in the bioacoustics of the Smooth-billed Ani is its ability to modify the vocalization structure for the same context. For instance, it uses the vocalizations “Whine”, “Flight” and “INR”, which differ in number of notes and the presence or not of harmonics, all in the same context, as shown in Table 1 and Fig. 3.

In the case of the two groups of Smooth-billed Ani that we followed, we found that there were differences between the groups for some similar voices, specifically for “Flight” and “Vigil” voices. This difference was interpreted as a vocal group signature, detected by significant differences in some acoustic parameters of these vocalizations. This is consistent with the circumstances of these vocalizations, since “Flight” is used in the context of group cohesion during flight, as also observed in budgerigars (Hile & Striedter, 2000Hile, A.G. & Striedter, G.F. 2000. Call convergence within groups of female Budgerigars (Melopsittacus undulatus). Ethology, 106(12): 1105-1114.), whereas “Vigil” is used in territory surveillance and monitoring, alerting the other members of the group about any imminent danger. This type of vocal signature is related to various mammal groups, such as bats (Boughman, 1998Boughman, J.W. 1998. Vocal learning by greater spear-nosed bats. Proceedings of the Royal Society of London , Series B: Biological Sciences, 265(1392): 227-233.; Wenrickboughman & Swilkinson, 1998Wenrickboughman, J. & Swilkinson, G. 1998. Greater spear-nosed bats discriminate group mates by vocalizations. Animal Behaviour, 55(6): 1717-1732.; Gillam & Chaverri, 2012Gillam, E.H. & Chaverri, G. 2012. Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Animal Behaviour, 83(1): 269-276.; Knörnschild et al., 2012Knörnschild, M.; Nagy, M; Metz, M.; Mayer, F. & Helversen, O.V. 2012. Learned vocal group signatures in the polygynous bat Saccopteryx bilineata. Animal Behaviour, 84(4): 761-769.), wolves (Zaccaroni et al., 2012Zaccaroni, M.; Passilongo, D.; Buccianti, A.; Dessì-Fulgheri, F.; Facchini, C.; Gazzola, A.; Maggini, I. & Apollonio, M. 2012. Group specific vocal signature in free-ranging Wolf packs. Ethology Ecology & Evolution, 24(4): 322-331.), gazelles (Volodin et al., 2014Volodin, I.A.; Volodina, E.V.; Lapshina, E.N.; Efremova, K.O. & Soldatova, N.V. 2014. Vocal group signatures in the goitred gazelle Gazella subgutturosa. Animal Cognition, 17(2): 349-357.), meerkats (Townsend et al., 2010Townsend, S.W.; Hollén, L.I. & Manser, M.B. 2010. Meerkat close calls encode group-specic signatures, but receivers fail to discriminate. Animal Behaviour, 80(1): 133-138.), whales (Vester et al., 2016Vester, H.; Hammerschmidt, K.; Timme, M. & Hallerberg, S. 2016. Quantifying group specificity of animal vocalizations without specific sender information. Physical Review E, 93(2): 022138. http://doi.org/10.1103/PhysRevE.93.022138
http://doi.org/10.1103/PhysRevE.93.02213...
), as well as for birds that exhibit vocalization learning (Mammen & Nowicki, 1981Mammen, D.L. & Nowicki, S. 1981. Individual differences and within-flock convergence in Chickadee calls. Behavioral Ecology and Sociobiology, 9(3): 179-186.; Nowicki, 1983Nowicki, S. 1983. Flock-specific recognation of chickadee calls. Behavioral Ecology and Sociobiology, 12(4): 317-320., 1989Nowicki, S. 1989. Vocal plasticity in captive Black-capped Chickadees: the acoustic basis and rate of call convergence. Animal Behaviour, 37: 64-73.; Baker, 2004Baker, M.C. 2004. The chorus song of cooperatively breeding Laughing Kookaburras (Coraciiformes, Halcyonidae: Dacelo novaeguineae): characterization and comparison among groups. Ethology, 110: 21-35.; Elie & Theunissen, 2018Elie, J.E. & Theunissen, F.E. 2018. Zebra finches identify individuals using vocal signatures unique to each call type. Nature Communications, 9: 4026. http://doi.org/10.1038/s41467-018-06394-9
http://doi.org/10.1038/s41467-018-06394-...
; Martins et al., 2018Martins, B.A.; Rodrigues, G.S.R. & Araújo, C.B. 2018. Vocal dialects and their implications for reintroductions. Perspectives in Ecology and Conservation, 16: 83-80.; Araya-Salas et al., 2019Araya-Salas, M.; Smith-Vidaurre, G.; Mennill, D.J.; Gonzáles-Gomes, P.L.; Cahill, J. & Wright, T.F. 2019. Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning. Proceedings of Royal Society B, 286(1903): 20190666.; Benti et al., 2019Benti, B.; Curé, C. & Dufour, V. 2019. Individual signature in the most common and context-independent call of the Rook (Corvus frugilegus). The Wilson Journal of Ornithology, 131(2): 373-381.). However, as previously mentioned, studies in birds with innate vocalization are scarce (Baker, 2004Baker, M.C. 2004. The chorus song of cooperatively breeding Laughing Kookaburras (Coraciiformes, Halcyonidae: Dacelo novaeguineae): characterization and comparison among groups. Ethology, 110: 21-35.; Radford, 2005Radford, A.N. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behaviour, 70(5): 1227-1234.).

Considering all the above, the present study represents a relevant contribution of acoustic information for the Smooth-billed Anis, a group of birds with innate vocalization and elaborate vocal repertoire, including interpopulation variation. In addition, it provides evidence of vocal group signature in the species, serving as basis for further research to increase the knowledge about this bird group.

CONCLUSION

The Smooth-billed Ani has an elaborate vocal repertoire, presenting voicings that are common across populations (e.g., “Ahnee”, “Pre-flight”, “Flight”, “Shout”, “Hoot”, “Grunt”, “Whine”, “Ee-oo-ee”). Variations were observed in the vocal repertoire and in the acoustic parameters of vocalizations between different populations, or even between groups of the same population, but further studies in other populations should be performed to better clarify these variations. In addition, we found an evidence of a vocal group signature in vocalizations used in the context of cohesion, defense and territory maintenance, in which there is a need to identify the group itself and not the individuals.

ACKNOWLEDGMENTS

We would like to thank Ricardo Brioschi Lyra for reviewing and commenting the article, and Guilherme Ferreira Ramos, Lais Gonçalves Pires de Souza and Patrick de Oliveira Guimarães for their support in the field activities. We also thank the Federal University of Espírito Santo and the Pro-Rectory of Research and Post-Graduation for the registration and approval of the project.

REFERENCES

  • Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49(3-4): 227-266.
  • Araya-Salas, M.; Smith-Vidaurre, G.; Mennill, D.J.; Gonzáles-Gomes, P.L.; Cahill, J. & Wright, T.F. 2019. Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning. Proceedings of Royal Society B, 286(1903): 20190666.
  • Baker, M.C. 2004. The chorus song of cooperatively breeding Laughing Kookaburras (Coraciiformes, Halcyonidae: Dacelo novaeguineae): characterization and comparison among groups. Ethology, 110: 21-35.
  • Baldo, S. & Mennill, D.J. 2011. Vocal behavior of Great Curassows, a vulnerable Neotropical Bird. Journal of Field Ornithology, 82(3): 249-258. http://doi.org/10.1111/j.1557-9263.2011.00328.x
    » http://doi.org/10.1111/j.1557-9263.2011.00328.x
  • Beecher, M.D. 1988. Kin recognation in birds. Behavior Genetics, 18(4): 465-482.
  • Benti, B.; Curé, C. & Dufour, V. 2019. Individual signature in the most common and context-independent call of the Rook (Corvus frugilegus). The Wilson Journal of Ornithology, 131(2): 373-381.
  • Berg, K.S.; Delgado, S.; Okawa, R.; Beissinger, S.R. & Bradbury, J.W. 2011. Contact calls are used for individuals mate recognition in free-ranging Green-rumped Parrotlets, Forpus passerines Animal Behaviour, 81: 241-248.
  • Boughman, J.W. 1998. Vocal learning by greater spear-nosed bats. Proceedings of the Royal Society of London , Series B: Biological Sciences, 265(1392): 227-233.
  • Bradbury, J.W. & Vehrencamp, S.L. 1998. Principles of animal communication Massachusets, Sinauer Press.
  • Brown, C.R. 1988. Social foraging in Cliff Swallows: local enhancement, risk sensitivity, competition and the avoidance of predators. Animal Behaviour, 36(3): 780-792.
  • Brown, C.R. & Brown, M.B. 1996. Coloniality in the Cliff Swallow Chicago, The University of Chicago Press.
  • Brumm, H.; Schmidt, R. & Schrader, L. 2009. Noise-dependent vocal plasticity in domestic fowl. Animal Behaviour, 78(3): 741-746.
  • Camacho-Schlenker, S.; Courvoisier, H. & Aubin, T. 2011. Song sharing and singing strategies in the Winter Wren Troglodytes troglodytes Behavioural Processes, 87(3): 260-267.
  • Davis, D.E. 1940. Social nesting habits of the Smooth-billed Ani. The Auk, 57: 179-218.
  • Elie, J.E. & Theunissen, F.E. 2018. Zebra finches identify individuals using vocal signatures unique to each call type. Nature Communications, 9: 4026. http://doi.org/10.1038/s41467-018-06394-9
    » http://doi.org/10.1038/s41467-018-06394-9
  • Ford, J.K.B. 1991. Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Canadian Journal of Zoology, 69(6): 1454-1483.
  • Gillam, E.H. & Chaverri, G. 2012. Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Animal Behaviour, 83(1): 269-276.
  • Goodale, E. & Kotagama, S.W. 2006. Context-dependent vocal mimicry in a passerine Bird. Proceedings of the Royal Society B, 273(1588): 875-880. http://doi.org/10.1098/rspb.2005.3392
    » http://doi.org/10.1098/rspb.2005.3392
  • Grieves, L.A. 2014. Acoustic communication in the joint-nesting Smooth-billed Ani, Crotophaga ani Hamilton, Ontario (Master Dissertation). McMaster University.
  • Grieves, L.A.; Logue, D.M. & Quinn, J.S. 2015. Vocal repertoire of cooperatively breeding Smooth-billed Anis. Journal of Field Ornithololy, 86(2): 130-143.
  • Hardman, S.I.; Zollinger, S.A.; Koselj, K.; Leitner, S.; Marshall, R.C. & Brumm, H. 2017. Lombard effect onset times reveal the speed of vocal plasticity in a songbird. Journal of Experimental Biology, 220(6): 1065-1071. http://doi.org/10.1242/jeb.148734
    » http://doi.org/10.1242/jeb.148734
  • Hile, A.G. & Striedter, G.F. 2000. Call convergence within groups of female Budgerigars (Melopsittacus undulatus). Ethology, 106(12): 1105-1114.
  • Hurd, C.R. 1996. Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus). Behavioral Ecology and Sociobiology, 38(4): 287-292.
  • James, L.S. & Sakata, J.T. 2019. Developmental modulation and predictability of age-dependent vocal plasticity in adult Zebra Finches. Brain Research, 1721: 146336. http://doi.org/10.1016/j.brainres.2019.146336
    » http://doi.org/10.1016/j.brainres.2019.146336
  • Janik, V.M. & Slater, P.J.B. 2000. The different roles of social learning in vocal communication. Animal Behaviour, 60: 1-11.
  • Jarvis, E.D.; Ribeiro, S.; da Silva, M.L.; Ventura, D.; Vielliard, J. & Mello, C.V. 2000. Behaviour ally driven gene expression reveals song nuclei in hummingbird brain. Nature, 406(6796): 628-632. http://doi.org/10.1038/35020570
    » http://doi.org/10.1038/35020570
  • Knörnschild, M.; Nagy, M; Metz, M.; Mayer, F. & Helversen, O.V. 2012. Learned vocal group signatures in the polygynous bat Saccopteryx bilineata Animal Behaviour, 84(4): 761-769.
  • Kort, S.R. & Cate, C.T. 2001. Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Animal Behaviour, 61: 239-247.
  • Krebs, J.R.; Macroberts, M.H. & Cullen, J.M. 1972. Flocking and feeding in the Great Tit Parus major: an experimental study. Ibis, 114(4): 507-530.
  • Lazerte, S.E.; Otter, K.A. & Slabbekoorn, H. 2017. Mountain Chickadees adjust songs, calls and chorus composition with increasing ambient and experimental anthropogenic noise. Urban Ecosystems, 20(5): 989-1000.
  • Lima, J.S.S.; Silva, S.A.; Oliveira, R.B.; Cecílio, R.A. & Xavier, A.C. 2008. Variabilidade temporal da precipitação mensal em Alegre, ES. Revista Ciência Agronômica, 39(2): 327-332.
  • Mammen, D.L. & Nowicki, S. 1981. Individual differences and within-flock convergence in Chickadee calls. Behavioral Ecology and Sociobiology, 9(3): 179-186.
  • Martins, B.A.; Rodrigues, G.S.R. & Araújo, C.B. 2018. Vocal dialects and their implications for reintroductions. Perspectives in Ecology and Conservation, 16: 83-80.
  • Nowicki, S. 1983. Flock-specific recognation of chickadee calls. Behavioral Ecology and Sociobiology, 12(4): 317-320.
  • Nowicki, S. 1989. Vocal plasticity in captive Black-capped Chickadees: the acoustic basis and rate of call convergence. Animal Behaviour, 37: 64-73.
  • Rabenold, P.P. 1987. Recruitment to food in black vultures: evidence for following from communal roosts. Animal Behaviour, 35(6): 1775-1785.
  • Radford, A.N. 2005. Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green woodhoopoe. Animal Behaviour, 70(5): 1227-1234.
  • RStudio Team. 2016. RStudio: Integrated development for R RStudio, Inc., Boston, MA. http://www.rstudio.com
    » http://www.rstudio.com
  • Salinas-Melgoza, A. & Wright, T.F. 2012. Evidence for vocal learning and limited dispersal as dual mechanisms for dialect maintenance in a parrot. PLoS ONE, 7: e48667.
  • Sharp, S.P.; Mcgowan, A.; Wood, M.J. & Hatchwell, B.J. 2005. Learned kin recognition cues in a social bird. Nature, 434(7037): 1127-1129.
  • Sick, H. 2001. Ornitologia brasileira Rio de Janeiro, Editora Nova Fronteira.
  • Townsend, S.W.; Hollén, L.I. & Manser, M.B. 2010. Meerkat close calls encode group-specic signatures, but receivers fail to discriminate. Animal Behaviour, 80(1): 133-138.
  • Tyack, P.L. 2008. Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. Journal of Comparative Psychology, 122(3): 319-331.
  • Valderrama, S.; Parra, J.; Dávila, N. & Mennill, D.J. 2008. Vocal BehaVior of the critically endangered Niceforo’s Wren (Thryothorus nicefori). The Auk, 125(2): 395-401.
  • Vehrencamp, S.L.; Ritter, A.R.; Keever, M. & Bradbury, J.W. 2003. Responses to playback of local versus distant contact calls in the Orange-fronted Conure, Aratinga canicularis Ethology, 109: 37-54.
  • Vester, H.; Hammerschmidt, K.; Timme, M. & Hallerberg, S. 2016. Quantifying group specificity of animal vocalizations without specific sender information. Physical Review E, 93(2): 022138. http://doi.org/10.1103/PhysRevE.93.022138
    » http://doi.org/10.1103/PhysRevE.93.022138
  • Volodin, I.A.; Volodina, E.V.; Lapshina, E.N.; Efremova, K.O. & Soldatova, N.V. 2014. Vocal group signatures in the goitred gazelle Gazella subgutturosa Animal Cognition, 17(2): 349-357.
  • Wanker, R.; Sugama, Y. & Prinage, S. 2005. Vocal labelling of family members in Spectacled Parrotlets, Forpus conspicillatus Animal Behaviour, 70(1): 111-118.
  • Wenrickboughman, J. & Swilkinson, G. 1998. Greater spear-nosed bats discriminate group mates by vocalizations. Animal Behaviour, 55(6): 1717-1732.
  • Wilkinson, G.S. 1992. Information transfer at evening bat colonies. Animal Behaviour, 44(3): 501-518.
  • Zaccaroni, M.; Passilongo, D.; Buccianti, A.; Dessì-Fulgheri, F.; Facchini, C.; Gazzola, A.; Maggini, I. & Apollonio, M. 2012. Group specific vocal signature in free-ranging Wolf packs. Ethology Ecology & Evolution, 24(4): 322-331.

FUNDING INFORMATION

  • The authors declare that the research was developed with their own funding.

Edited by

Luís Fábio Silveira

Publication Dates

  • Publication in this collection
    17 Sept 2021
  • Date of issue
    2021

History

  • Received
    21 July 2020
  • Accepted
    17 June 2021
  • Published
    30 July 2021
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