Call Recognition in Brown Jays Cyanocorax morio Lisa Michl Department of Zoology and Psychology, University o f Wisconsin Madison Abstract Call recognition in birds is important so energy and time are not wasted. Many studies have used heterospecific calls that were evolutionarily distant from the species being tested to show that recognition was possible. Thi s study looked at species recognition of both an evolutionary distant species common potoo, Nyctibius griseus : Nyctibiidae and of a species in the same family magpie jay, Calocitta formosa : Corvidae in brown jays Cyanocorax morio : Corvidae. Three di fferent calls brown jay, magpie jay, and common potoo were played in ten different territories of brown jays in the Monteverde area during the dry season. Results suggested that brown jays could distinguish their call from the other two species p = 0.0 19. Brown jays also responded more strongly to the magpie jay call than to the common potoo call, suggesting that evolutionary similar species have similar structure to their calls as opposed to evolutionarily distant species. Resumen El reconocimien to de llamadas en aves es importante para que estos organismos no desperdicien energÃa y tiempo. Muchos estudios han u tilizado el uso de llamadas heteroespecÃficas evolutivamente distantes del de la especie examinada para determinar si el reconocimiento de dichas vocalizaciones es posible. Se es t udiÃ³ el reconocimiento de especies en piapias Cyanocorax morio : Corvidae entre una especie de ave evolutivamente distante El pÃ¡jaro palo, Nyctibius griseus : Nyctibiidae y una especie en la misma familia La ur raca azul, Cyanocorax morio : Corvidae. Se probaron tres llamadas diferentes piapia, urraca azul y pÃ¡jaro palo en diez territorios de piapias en el Ã¡rea de Monteverde durante la estaciÃ³n seca. Los resultados sugirieron que las piapias pueden distinguir su llamada de las de las otras dos especies p = 0.019. Las piapias tambiÃ©n respondieron mÃ¡s a la llamada de la urraca azul que a la llamada del pÃ¡jaro palo, sugiriendo que las especies relacionadas poseen estructuras similares en sus llamadas y diferentes d e las estructuras de las llamadas de especies evolutivamente distantes. Introduction Vocalization allows birds to communicate with conspecifics in order to establish social links and recognize each other Martens 1996; Charrier & Sturdy 2005. Social links are usually associated with group living and allow group members to maintain a cohesive bond. Distinguishing individuals or group members is especially important in cooperatively breeding birds to establish who is a competitor and who is a friend Radford 2003. Group recognition has been found in both green woodhoopoes Phoeniculus purpureus Radford 2005 and Mexican jays Aphelocoma ultramarina : Corvidae Hopp et al. 2001. This is the result of both species living in large groups. Large gro up living has been suggested to lead to higher cognitive abilities because of the demands of a social lifestyle Bond et al. 2003.
The capacity to distinguish between group members and non members is important, but being able to distinguish a conspecific from a heterospecific is vital. Reacting to a heterospecific vocalization wastes energy and time with no reward Amezquita et al. 2005. Therefore, species of birds have developed mechanisms to distinguish their species call from another species. Charr ier and Sturdy 2005 conducted a study with black capped chickadees Poecile atricapillus to further research on species recognition. They used both the species call black capped chickadee and a heterospecific call gray crowned rosy finch, Leucostict e tephrocotis of a non predatory and non competing species that had a call acoustically distinct from the black capped chickadee. They found a higher response to the black capped chickadee call compared to the gray crowned rosy finch call. These results s uggested that black capped chickadees are able to discriminate between conspecific calls and heterospecific calls. Studies with red winged blackbird Agelaius phoeniceus have also shown they can distinguish between a call from their own species and anoth er species Beletshk et al. 1980. Although many vocalization studies have been conducted with songbirds, few studies have been done with larger species of cooperatively breeding birds. The brown jay Cyanocorax morio : Corvidae is a cooperatively breed ing species of birds found from Mexico to northern Panama Lawton 1983. During the breeding season January May they are territorial and stay in groups of three to 17 individuals Williams et al. 1994. Territories consist of a collection of pasture an d forest ranging from three to five hectares Lawton 1983. Mexican jays A. ultramarina live in similar groups and have territories like brown jays C. morio . They have been shown to respond stronger to calls from their group than to calls from members outside their group Hopp et al. 2001, suggesting that this species can recognize calls between groups because of defining characteristics. Species in the same family have similar characteristics or cognitive abilities, so brown jays are likely to posses s similar mechanisms for distinguishing calls. Bond et al. 2003 found that birds living in large groups also have higher cognitive abilities then birds living in pairs. Therefore, brown jays should be able to distinguish between calls from their own spe cies and calls of another species. Few studies have directly tested whether a species can recognize its own species call from another species call in the same family. Species interbreed with individuals that are similar because calls are distinct for eac h species Ridley 1993. Therefore, species should be able to recognize the difference between their own species call and a call of another species in the same family. This study was conducted to determine if C. morio brown jays could distinguish their s pecies call from a different species common potoo, Nyctibius griseus : Nyctibiidae and from a species in the same family magpie jay, Calocitta formosa : Corvidae. Methods This study was conducted in and around the Monteverde area from April 13 May 7, 2006. Brown jay breeding season occurs during the dry season between January and May. They defend their territory during this time Lawton 1983. A total of ten brown jay territories Fig. 1 were found by going out in the field and spotting brown jays . A previously recorded call of a brown jay from Voices of the Neo tropical Rainforest was played when a brown jay was found in the field to make sure that the area was within a territory. A site was chosen in each territory to conduct the trials; the s ite consisted of an
open area of at least ten meters. Five out of the ten sites were pasture, with the rest being in open areas of grass or in an opening in the forest. Trials were run between the hours of 07:00 and 12:00 for the first three weeks of the study. The trials were carried out between 06:00 and 11:00 after three weeks because of lack of response to any call at the time due to possible habituation. Tests consisted of playing a call and observing the behaviors. Three calls were used to determin e if brown jays could distinguish conspecifics from heterospecifics: brown jay, white throated magpie jay C. formosa , and common potoo N. griseus . Magpie jays are not found in the Monteverde area, so brown jays had no previous experience with their ca lls. The common potoo call was used because it is a species of bird that is active at night; being nocturnal implies that the brown jays had never heard or interacted with the common potoo as a competitor or predator and would therefore not respond to that call as suggested by Charrier and Sturdy 2005. The magpie jay and the common potoo calls were taken from Voices of the Neo tropical Rainforest. Ten seconds of the previously recorded call were used and each call was assumed to be a primary call that can elicit a territorial response in brown jays Hopp et al. 2001. The play back consisted of one minute of silence, followed by ten seconds of the call, and then five seconds of silence. This sequence was repeated four times to allow the brown jays to hear and respond to the call. All calls were played from an iPod connected to JBL on tour speakers 6V; the iPod and speakers were placed in a bag and then duct taped onto a tree 0.5 1 m off the ground at each site to simulate a place from where a bi rd would call. The minute of silence before each call allowed time to set up and establish a hiding spot for that site to make sure that the birds were responding to the call and not to the presence of the researcher. Behaviors were recorded onto a previ ously made behavior sheet Appendix 1. The behaviors that were considered were: vocalization, coming near, watching, staying within the area, head bobbing, and posturing Table 1. The five behaviors were recorded for ten minutes following the first call . An event was recorded anytime it was observed for all brown jays in the area; so that the birds would not become habituated to the calls, each territory only received one call per day. The orders of the territories were also randomized that day, along with the order of the calls. Each call was played three times in all ten territories. A total of 90 trials were conducted resulting in 90 minutes of observation time.
TABLE 1. List and definitions of the behaviors used in evaluating the frequen cy of response from brown jays to three different calls brown jay, magpie jay, and common potoo. Monteverde, Costa Rica. April May 2006. Behavior Name Description Vocalization Any call coming from a bird Coming Near Coming within 2 meters of the spea kers in any direction Watching Looking in the direction of the speakers for five or more seconds. New behavior is accounted for after the bird looks away for five or more seconds Staying within the area When the bird is within ten meters radius of the speakers, staying for five seconds. New behavior if it leaves the area and comes back Head Bobbing Quickly lowering and raising its head Hale et al, 2003 Posturing Vertical body position with the bill held high and tail low, or in a horizontal crouch Hale et al., 2003
FIGURE 1. Location of the ten brown jay Cyanocorax morio sites used to determine if brown jays could recognize heterospecifc calls from conspecific calls. Each territory consists of at least ten meters of open space and is locate d in and around Monteverde, Costa Rica. RESULTS The number of birds for each territory was between two and seven mean = 4.6, with a total of 46 birds. Pseudoreplication must be taken into account in this study because the sample size of the birds was so small. The probability of the same bird responding more than once was very high. To lessen the effects of pseudoreplication, the average response per bird was found for each trial. A Kruskal Wallis test was conducted comparing the call type to the re sponse per bird. A significant difference p = 0.019 between the calls and amount of response was found. To determine where the significant differences were located among all three calls, a Post Hoc Tukey type multiple comparison test was conducted. The Post Hoc test revealed that there was a significant difference between all three comparisons of the calls. The strongest response was for the brown jay call mean =
53.48, followed by the magpie jay mean = 47.98, and then the common potoo mean = 35.03 Fig. 2. FIGURE 2. Average response per brown jay for each trial N = 90 compared to all three calls used brown jay, magpie jay, and common potoo. The brown jay had the most responses per bird, followed by the magpie jay, and then the common poto o determined by a Kruskal Wallis Test and a Post Hoc Tukey type multiple comparison test. Monteverde, Costa Rica. April May 2006. The number of birds that came during each trial varied, along with the total number of birds for each site Table 2. A K ruskal Wallis test was done to determine whether the average number of birds per site that responded was significantly different for each call. A significant difference p = 0.036 was found. A Post Hoc Tukey type multiple comparison test was done to det ermine where the significant differences occurred. More birds came to the brown jay call mean = 20.15 than to the common potoo call mean = 10.10. There was not a significant difference between the brown jay call and the magpie jay call mean = 16.25 , or between the magpie jay call and the common potoo call Fig 3. TABLE 2. The total number of observed brown jays C. morio occurring in each of the 10 sites in Monteverde, Costa Rica. April May 2006. Site 1 2 3 4 5 6 7 8 9 10 # of Birds 6 6 2 1 6 5 7 3 6 4 0 0.5 1 1.5 2 2.5 3 1 Call Average Response per bird Brown Jay Magpie Magpie Jay Common Potoo
FIGURE 3. The average number of birds that responded per total number of birds for that site compared to each call. More birds came to the brown jay call BJ, then the magpie jay call MJ, and then the common potoo call CP. A two way contingency table was used to determine which behaviors were used more frequently in response to all calls. The birds responded to each call mostly with a vocalization 47.4%, followed by watching 21.2% and head bobbing 20.8% Table 3. TABLE 3. Total number of responses and percentages for all six behaviors vocalization, coming near, watching, head bobbing, staying near, and posturing of brown jays in Monteverde, Costa Rica. April May 2006. Behavior Vocalization Coming N ear Watching Head Bobbing Staying Near Posturing Total 139 16 62 61 8 7 Percent 47.4 5.5 21.2 20.8 2.7 2.4 A Kruskal Wallis test was used to determine if there was any significant difference among the ten different sites in the average number of birds that responded, the average response per bird, the average number of vocalizations per bird, the average number of head bobbing per bird, the average number of watching per bird, and the average number of several infrequent behaviors coming near, staying near, and posturing per bird. No significant differences were found p > 0.05 among the groups. 0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 0.4 BJ MJ CP Average Number of Birds Call
DISCUSSION Brown jays responded more strongly to their own call compared to a call from another species. This was the case for both the magpie jay call and the common potoo call. These results agreed with previous studies on heterospecific calls Beletshk et al. 1980; Charrier and Sturdy 2001. It is now known that another species of Passeriformes can recognize conspecific calls over heterospecific calls C harrier and Sturdy 2001, Beletshk et al. 1980. Knowing heterospecific calls from conspecific calls allows brown jays to save energy and time responding to a territorial intrusion from another species that will not compete for breeding rights. This is e specially important in brown jays because they are cooperative breeders Stiles and Skutch 1989. The breeding season is a stressful time and most of their energy is spent building a nest and in other breeding behaviors Lawton 1983. Spending time respon ding to heterospecific calls within their territories would lessen the amount of energy directed toward breeding thus decreasing their fitness. Another reason for not responding to heterospecific calls could be because of evolutionarily divergent species. Martens 1996 suggest that differences in vocalizations are important isolation mechanism in species, indicating that different species are likely to have vocal differences. The brown jays also responded more strongly to the magpie jay call than to the common potoo call. One possible explanation for this is that species that are in the same Family Corvidae share some similar characteristics, because they have not evolved separately for as long as species in different families. Therefore, brown jays are more likely to recognize some aspects of the magpie jay call as their own rather than the common potoo call Family Nyctibiidae. The number of birds coming to the site when the brown jay call was played was greater than the number of birds coming to the magpie jay call or the common potoo call. This further strengthens the belief that brown jays can detect difference between their own call and that of another species. Most of the birds responded by coming to the speakers when the brown jay call was played, suggesting that they all knew how to react to their own species call. The brown jays also responded to each call more frequently with certain behaviors. The most commonly used behavior was vocalization. Vocalization allows birds to communicate without being seen and can convey many messages like age, sex, or fitness Kroodsma and Miller 1996. Communicating their fitness without actually fighting requires less energy, so vocalizations are likely to be used over other behaviors. Head bobbing an d watching were the next two most common behaviors that the brown jays used in response to the calls. Both of these behaviors require visual contact, which is usually harder and less likely to occur. Reacting to each call is an act of territorial defense , which requires energy and maybe fighting. A shortened lifespan could result from using energy to respond to the call and fight with the intruder Alcock 2005. Watching allows the birds to evaluate the situation before taking action, which could save e nergy in the long run. Head bobbing is an aggressive behavior that only uses displays, so the possibility of getting hurt from an interaction is not possible. Coming near was not observed that often. This could be due to the fact that coming within two meters of the bird would result in a fight or otherwise more aggressive interaction where the birds might be hurt. Posturing was also not observed that often, probably because posturing
was usually followed by chases at least in the Hale et al. 2005 stu dy. Posturing then would result in a more interactive response than the one that birds were willing to put in. This study also showed that among all ten groups there was no significant difference in the average number of birds that arrived or showed up. There were no significant difference among the groups and all the behaviors. These data suggest that brown jays responded with similar actions at each of the ten sites. There was nothing about each site that could have altered the results or caused one site to have a completely different reaction in the birds. This suggests that environmental factors and the number of birds in each territory did not affect cognitive abilities or vocal recognition. Further studies should look at what specific parts of th e call convey species information, as has been done for both red winged black birds A. phoeniceus Beletsky et al. 1980 and black capped chickadees P. atricapillus Charrier and Sturdy 2001. Understanding what part of the call allows brown jays to respond stronger to magpie jay calls than to common potoo calls would show what aspects of the call have derived more recently. These studies could also look at whether the brown jay can distinguish group members from non members as has been shown in the Mexican jays A. ultramarina Hopp et al. 2001. This would show that more species of cooperatively breeding birds have the ability to distinguish group members from non members. Another aspect to consider would be the age of the birds that responded to each call to determine if there is a difference in age of birds that respond to heterospecific or conspecific calls. Determining the age of the bird could suggest whether knowing the difference between heterospecific calls and conspecific calls is innate or learned. ACKNOWLEDGMENTS I would like to thank Javier MÃ© ndez for advising me, Maria Jost , and Oliver Hyman for all their help in my statistical analysis, Karen Masters for helping with the statistics of my project, Alan Masters for his support, Kev in Loope for helping me cut all three calls, the Brenes family for supporting my research, and the owners of the land that I used for my ten study sites, especially La Colina Lodge. LITERATURE CITED Alcock, J. 2005. Animal Behavior, Eigth edidition. Sina uer Associates, Inc., Sunderland, Massachusetts, p.264 265. Amezquita, A., Castellanos, L., and Hodl, W. 2005. Auditory matching of male Epipedobates femoralis Anura: Dendrobatidae under field conditions. Behaviour, 70:1377 1386. Beletsky, L. D., Chao, S., and Smith, D. G. 1980. An investigation of song based species recognition in the red winged blackbird Agelaius phoeniceus. Behavior , 73:189 203. Bond, A. B., Kamil, A. C., and Balda, R. P. 2003. Social complexity and transitive inference in corvid s. Animal Behavior , 65:479 487. Charrier, I. and C. B. Sturdy. 2005. Call based species recognition in black capped chickadees. Behavioral Processes 70:271 281. Hale, A. M., D. A. Williams, and K. N. Rabenold. 2003. Territoriality and neighbor assessm ent in Brown jays Cyanocorax morio in Costa Rica. The Auk, 1202: 446 456. Hopp, S. L., P. Jablonskit, and J. L. Brown. 2001. Recognition of group membership by voice in Mexican jays, Aphelocoma ultramarina . Animal Behavior 62: 297 303. Lawton, M. F. 1983 Cyanocorax morio In D. H. Janzen. Costa Rican Natural History, p. 573 574. University of Chicago Press, Chicago.
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APPENDIX 1 TABLE 1. Frequency table used to take data of each of the six behaviors of brown jays in response to three different calls. All data was conducted between 06:00 and 12:00 in Monteverde, Costa Rica from April May 2006. Behavioral Observatio ns Date: Group: Time: Number of Birds: Weather: Call: Age of Bird: Behavior Frequency Vocalization Coming Near Watching Staying within the area Head Bobbing Posturing