- Email: [email protected]
Temporal coordination signals coalition quality
Current Biology Vol 17 No 11 R406
is suitable for representing objects with sparse codes that support a stable conscious perception in the face of dynamic inputs [14], and also for reconciling a temporal mismatch between features that are processed at different timings across cortical areas [4,5]. The above freezing display can be further used as a tool to investigate the neural basis for the dynamics of visual awareness. Acknowledgments The author thanks Shin Shimojo, Takeo Watanabe, Shin’ya Nishida, and David Whitney for comments and discussions. Supplemental data Supplemental data, including experimental procedures and several movies are available at http://www.current-biology. com/cgi/content/full/17/11/R404/DC1 References 1. Nijhawan, R. (1994). Motion extrapolation in catching. Nature 370, 256–257. 2. Sheth, B.R., Nijhawan, R., and Shimojo, S. (2000). Changing objects lead briefly flashed ones. Nat. Neurosci. 3, 489–495. 3. Eagleman, D.M., and Sejnowski, T.J. (2000). Motion integration and postdiction in visual awareness. Science 287, 2036–2038. 4. Moutoussis, K., and Zeki, S. (1997). A direct demonstration of perceptual asynchrony in vision. Proc. R. Soc. Lond. B 264, 393–399. 5. Nishida, S., and Johnston, A. (2002). Marker correspondence, not processing latency, determines temporal binding of visual attributes. Curr. Biol. 12, 359–368. 6. Breitmeyer, B.G. (1984). Visual Masking: An Integrative Approach. Oxford U. Pr., New York. 7. Paradiso, M.A., and Nakayama, K. (1991). Brightness perception and filling-in. Vision Res. 31, 1221–1236. 8. Nakayama, K., Shimojo, S., and Ramachandran, V.S. (1990). Transparency: relation to depth, subjective contours, luminance, and neon color spreading. Perception 19, 497–513. 9. Zhou, H., Friedman, H.S., and von der Heydt, R. (2000). Coding of border ownership in monkey visual cortex. J. Neurosci. 20, 6594–6611. 10. Di Lollo, V., Enns, J.T., and Rensink, R.A. (2000). Competition for consciousness among visual events: the psychophysics of reentrant visual processes. J. Exp. Psychol. Gen. 129, 481–507. 11. Pessoa, L., and DeWeerd, P. (2003). Fillingin: From Perceptual Completion to Cortical Reorganization. Oxford U Pr., New York. 12. Pinna, B., Werner, J.S., and Spillmann, L. (2003). The watercolor effect: a new principle of grouping and figure-ground organization. Vision Res. 43, 43–52. 13. Kamitani, Y., and Shimojo, S. (1999). Manifestation of scotomas created by transcranial magnetic stimulation of human visual cortex. Nat. Neurosci. 2, 767–771. 14. Yarrow, K., Haggard, P., Heal, R., Brown, P., and Rothwell, J.C. (2001). Illusory perceptions of space and time preserve cross-saccadic perceptual continuity. Nature 414, 302–305.
NTT Communication Science Laboratories, Japan. E-mail: [email protected].
Temporal coordination signals coalition quality Michelle L. Hall and Robert D. Magrath Coordinated displays are widely used to defend shared resources, and may signal coalition strength so that groups can assess the relative competitive ability of rivals and avoid unnecessary fights. Joint vocal displays are known to facilitate numerical assessment of relative group size in some animals, but it is not known whether features of coordinated vocal displays can signal coalition strength independent of coalition size. We show experimentally that precise coordination between partners in avian duets increases the perceived threat of these joint territorial displays, and provide the first evidence that established pairs produce more highly coordinated duets than new pairs. Duet precision thus serves as an honest signal of coalition strength. This is the first reported evidence of cooperative benefits for precise temporal coordination of signals. In animals from social shrimp (Synalpheus) to lion (Panthera leo), groups use coordinated displays to defend resources [1,2]. In some birds, singing in chorus allows numerical assessment by rival groups [3], but it is not known whether joint vocal displays signal aspects of coalition strength other than group size. Temporal coordination between partners in some duetting birds is strikingly precise, and might signal pair stability to territorial rivals [4]. But there is no empirical evidence that temporal precision of duets improves with pair duration [5] or influences the effectiveness of the territorial display, and the function of such remarkable coordination within duets is unknown. Paired Australian magpie- larks (Grallina cyanoleuca) sing notes in rapid alternation to produce antiphonal duets for territorial defence (Figure 1A). Experiments show duets are more threatening
territorial displays than solo songs [6]. Within duets, individuals initiate each note a mean of 0.5 seconds after the start of their partner’s note (their ‘reaction time’), with mean standard deviations of 0.04 seconds (8% of mean reaction times) [7]. Levels of coordination vary, but highly coordinated partners create a series of closely spaced alternating notes that, to an uneducated ear, sound like the song of a single bird (audio and Figure S1 in the Supplemental data available on-line with this issue). Magpie-larks are ideal for testing whether temporal precision signals coalition strength independently of coalition size: they defend territories in pairs; alternating notes in duets do not increase signal amplitude; and variability in reaction times provides a simple measure of duet coordination that can be quantified and manipulated. Paired birds sometimes constitute a territorial threat: in the mosaic of territories that are defended year-round, established pairs may expand their territory at the expense of neighbours, and around 20% of new pairs involve two new birds occupying an area [8]. We simulated territorial intrusion by a pair, testing the function of duet precision with a playback experiment broadcasting ‘coordinated’ and ‘uncoordinated’ duets on twelve magpie-lark territories (see Supplemental Experimental Procedures). Playback stimuli contained identical notes repeated equally often, but differed in the timing of male and female contributions, so that precision was at the extremes of the natural range [7]. We used male song rate as a measure of response because earlier experiments showed it to be the most sensitive to differences in threat to the territory [6]. Male magpie-larks responded more aggressively to playback of precisely coordinated duets than uncoordinated duets (Figure 1B), showing that a high level of coordination created a more threatening territorial display. Precise duets are therefore likely to be more effective for territorial defence because they signal coalition quality to rivals.
Magazine R407
Acknowledgements We thank N.E. Langmore, M.D. Jen nions, R. Heinsohn, T.H. Clutton- Brock and A. Cockburn for comments. The research was partially supported by an Australian Postgraduate Award to M.L.H.
Male songs/5 min
8 6 4 2 0
Coordinated
Uncoordinated
Duet stimuli C
100
11(5.3)
11(3.7)
12(4.1)
17(7.7)
Day 1 -7
Day 8 -28
Year 1
Year 2+
80
60
40
20
0
Stage of partnership
Current Biology
Figure 1. Coordination in magpie-lark duets. (A) Pair duetting with synchronised wing display. (B) Male song rate is higher in response to simulated intruders producing highly coordinated than uncoordinated duets (repeated measures GLM: F1,11 = 7.3, P = 0.02). Song rate is the sum of solo songs and initiated duets in the 5-min playback period [6]. (C) Males (black bars) and females (white bars) that have been paired longer are more likely to produce highly coordinated duets, defined here as those with a S.D. of reaction time < 0.05 seconds (logistic regression, males: Wald chi-square = 10.9, P = 0.01; females: Wald chi-square = 10.3, P = 0.02). Bars show mean ± s.e.m.; N = 12 in (B) and is shown above bars in (C) as the number of pairs and mean number of duets measured per pair.
References 1. Toth, E., and Duffy, J.E. (2005). Coordinated group response to nest intruders in social shrimp. Biol. Lett. 1, 49–52. 2. McComb, K., Packer, C., and Pusey, A. (1994). Roaring and numerical assessment in contests between groups
12 10
Supplemental data Supplemental data, including experimental procedures and audio files are available at http://www.current-biology.com/cgi/ content/full/17/11/R406/DC1
B
A
Highly coordinated duets (%)
Coalition quality depends on ongoing motivation and ability to act collectively [9]. Partners that had been together longer were more likely to produce well- coordinated duets (Figure 1C; Supplemental Experimental Procedures). Coordination of duets thus signals ongoing motivation to act collectively (coalition stability). Furthermore, duet precision is a complex coordination task that might be an index of ability to act collectively [9]: duet ‘tempo’ is slower when partners are far apart, suggesting that precision requires partners to make note-by-note adjustments, with delays caused by the slow speed of sound [7]. Our results provide experimental evidence from the territorial displays of duetting birds that precise temporal coordination between partners signals coalition quality. Previous work has shown benefits of signal coordination in the context of mate attraction. Competition results in precise temporal coordination of signals as male katydids (Neoconocephalus spiza) and fiddler crabs (Uca annulipes) strive to produce the leading calls preferred by females [10,11], while cooperating males in the lekking long-tailed manakin (Chiroxiphia linearis) attract more females if their songs have closely matched frequencies [12]. Our results extend these, showing that selection also favours the evolution of precise temporal coordination of signals between group members cooperating to defend a resource.
of female lions, Panthera leo. Anim. Behav. 47, 379–387. 3. Seddon, N., and Tobias. J.A. (2003). Communal singing in the cooperatively breeding subdesert mesite Monias benschi: evidence of numerical assessment? J. Avian Biol. 34, 72–80. 4. Wiley, R.H., and Wiley, M.S. (1977). Recognition of neighbours’ duets by stripe-backed wrens Campylorhynchus nuchalis. Behaviour 62, 10–34. 5. Marshall-Ball, L., Mann, N., and Slater, P.J.B. (2006). Multiple functions to duet singing: hidden conflicts and apparent cooperation. Anim. Behav. 71, 823–831. 6. Hall, M.L. (2000). The function of duetting in magpie-larks: conflict, cooperation, or commitment? Anim. Behav. 60, 667–677. 7. Hall, M.L. (2006). Convergent vocal strategies of males and females are consistent with a cooperative function of duetting in Australian magpie-larks. Behaviour 143, 425–449. 8. Hall, M.L. (1999). The importance of pair duration and biparental care to
reproductive success in the monogamous Australian magpie-lark. Aust. J. Zool. 47, 439–454. 9. Hagen, E.H., and Bryant, G.A. (2003). Music and dance as a coalition signaling system. Hum. Nature-Int Bios. 14, 21–51. 10. Greenfield, M..D, and Roizen, I. (1993). Katydid synchronous chorusing is an evolutionarily stable outcome of female choice. Nature 364, 618–620. 11. Backwell, P., Jennions, M., Passmore, N., and Christy, J. (1998). Synchronized courtship in fiddler crabs. Nature 391, 31–32. 12. Trainer, J.M., and McDonald, D.B. (1995). Singing performance, frequency matching and courtship success of longtailed manakins (Chiroxiphia linearis). Behav. Ecol. Sociobiol. 37, 249–254.
School of Botany and Zoology, Australian National University, Canberra, A.C.T., 0200, Australia. E-mail: [email protected]
is suitable for representing objects with sparse codes that support a stable conscious perception in the face of dynamic inputs [14], and also for reconciling a temporal mismatch between features that are processed at different timings across cortical areas [4,5]. The above freezing display can be further used as a tool to investigate the neural basis for the dynamics of visual awareness. Acknowledgments The author thanks Shin Shimojo, Takeo Watanabe, Shin’ya Nishida, and David Whitney for comments and discussions. Supplemental data Supplemental data, including experimental procedures and several movies are available at http://www.current-biology. com/cgi/content/full/17/11/R404/DC1 References 1. Nijhawan, R. (1994). Motion extrapolation in catching. Nature 370, 256–257. 2. Sheth, B.R., Nijhawan, R., and Shimojo, S. (2000). Changing objects lead briefly flashed ones. Nat. Neurosci. 3, 489–495. 3. Eagleman, D.M., and Sejnowski, T.J. (2000). Motion integration and postdiction in visual awareness. Science 287, 2036–2038. 4. Moutoussis, K., and Zeki, S. (1997). A direct demonstration of perceptual asynchrony in vision. Proc. R. Soc. Lond. B 264, 393–399. 5. Nishida, S., and Johnston, A. (2002). Marker correspondence, not processing latency, determines temporal binding of visual attributes. Curr. Biol. 12, 359–368. 6. Breitmeyer, B.G. (1984). Visual Masking: An Integrative Approach. Oxford U. Pr., New York. 7. Paradiso, M.A., and Nakayama, K. (1991). Brightness perception and filling-in. Vision Res. 31, 1221–1236. 8. Nakayama, K., Shimojo, S., and Ramachandran, V.S. (1990). Transparency: relation to depth, subjective contours, luminance, and neon color spreading. Perception 19, 497–513. 9. Zhou, H., Friedman, H.S., and von der Heydt, R. (2000). Coding of border ownership in monkey visual cortex. J. Neurosci. 20, 6594–6611. 10. Di Lollo, V., Enns, J.T., and Rensink, R.A. (2000). Competition for consciousness among visual events: the psychophysics of reentrant visual processes. J. Exp. Psychol. Gen. 129, 481–507. 11. Pessoa, L., and DeWeerd, P. (2003). Fillingin: From Perceptual Completion to Cortical Reorganization. Oxford U Pr., New York. 12. Pinna, B., Werner, J.S., and Spillmann, L. (2003). The watercolor effect: a new principle of grouping and figure-ground organization. Vision Res. 43, 43–52. 13. Kamitani, Y., and Shimojo, S. (1999). Manifestation of scotomas created by transcranial magnetic stimulation of human visual cortex. Nat. Neurosci. 2, 767–771. 14. Yarrow, K., Haggard, P., Heal, R., Brown, P., and Rothwell, J.C. (2001). Illusory perceptions of space and time preserve cross-saccadic perceptual continuity. Nature 414, 302–305.
NTT Communication Science Laboratories, Japan. E-mail: [email protected].
Temporal coordination signals coalition quality Michelle L. Hall and Robert D. Magrath Coordinated displays are widely used to defend shared resources, and may signal coalition strength so that groups can assess the relative competitive ability of rivals and avoid unnecessary fights. Joint vocal displays are known to facilitate numerical assessment of relative group size in some animals, but it is not known whether features of coordinated vocal displays can signal coalition strength independent of coalition size. We show experimentally that precise coordination between partners in avian duets increases the perceived threat of these joint territorial displays, and provide the first evidence that established pairs produce more highly coordinated duets than new pairs. Duet precision thus serves as an honest signal of coalition strength. This is the first reported evidence of cooperative benefits for precise temporal coordination of signals. In animals from social shrimp (Synalpheus) to lion (Panthera leo), groups use coordinated displays to defend resources [1,2]. In some birds, singing in chorus allows numerical assessment by rival groups [3], but it is not known whether joint vocal displays signal aspects of coalition strength other than group size. Temporal coordination between partners in some duetting birds is strikingly precise, and might signal pair stability to territorial rivals [4]. But there is no empirical evidence that temporal precision of duets improves with pair duration [5] or influences the effectiveness of the territorial display, and the function of such remarkable coordination within duets is unknown. Paired Australian magpie- larks (Grallina cyanoleuca) sing notes in rapid alternation to produce antiphonal duets for territorial defence (Figure 1A). Experiments show duets are more threatening
territorial displays than solo songs [6]. Within duets, individuals initiate each note a mean of 0.5 seconds after the start of their partner’s note (their ‘reaction time’), with mean standard deviations of 0.04 seconds (8% of mean reaction times) [7]. Levels of coordination vary, but highly coordinated partners create a series of closely spaced alternating notes that, to an uneducated ear, sound like the song of a single bird (audio and Figure S1 in the Supplemental data available on-line with this issue). Magpie-larks are ideal for testing whether temporal precision signals coalition strength independently of coalition size: they defend territories in pairs; alternating notes in duets do not increase signal amplitude; and variability in reaction times provides a simple measure of duet coordination that can be quantified and manipulated. Paired birds sometimes constitute a territorial threat: in the mosaic of territories that are defended year-round, established pairs may expand their territory at the expense of neighbours, and around 20% of new pairs involve two new birds occupying an area [8]. We simulated territorial intrusion by a pair, testing the function of duet precision with a playback experiment broadcasting ‘coordinated’ and ‘uncoordinated’ duets on twelve magpie-lark territories (see Supplemental Experimental Procedures). Playback stimuli contained identical notes repeated equally often, but differed in the timing of male and female contributions, so that precision was at the extremes of the natural range [7]. We used male song rate as a measure of response because earlier experiments showed it to be the most sensitive to differences in threat to the territory [6]. Male magpie-larks responded more aggressively to playback of precisely coordinated duets than uncoordinated duets (Figure 1B), showing that a high level of coordination created a more threatening territorial display. Precise duets are therefore likely to be more effective for territorial defence because they signal coalition quality to rivals.
Magazine R407
Acknowledgements We thank N.E. Langmore, M.D. Jen nions, R. Heinsohn, T.H. Clutton- Brock and A. Cockburn for comments. The research was partially supported by an Australian Postgraduate Award to M.L.H.
Male songs/5 min
8 6 4 2 0
Coordinated
Uncoordinated
Duet stimuli C
100
11(5.3)
11(3.7)
12(4.1)
17(7.7)
Day 1 -7
Day 8 -28
Year 1
Year 2+
80
60
40
20
0
Stage of partnership
Current Biology
Figure 1. Coordination in magpie-lark duets. (A) Pair duetting with synchronised wing display. (B) Male song rate is higher in response to simulated intruders producing highly coordinated than uncoordinated duets (repeated measures GLM: F1,11 = 7.3, P = 0.02). Song rate is the sum of solo songs and initiated duets in the 5-min playback period [6]. (C) Males (black bars) and females (white bars) that have been paired longer are more likely to produce highly coordinated duets, defined here as those with a S.D. of reaction time < 0.05 seconds (logistic regression, males: Wald chi-square = 10.9, P = 0.01; females: Wald chi-square = 10.3, P = 0.02). Bars show mean ± s.e.m.; N = 12 in (B) and is shown above bars in (C) as the number of pairs and mean number of duets measured per pair.
References 1. Toth, E., and Duffy, J.E. (2005). Coordinated group response to nest intruders in social shrimp. Biol. Lett. 1, 49–52. 2. McComb, K., Packer, C., and Pusey, A. (1994). Roaring and numerical assessment in contests between groups
12 10
Supplemental data Supplemental data, including experimental procedures and audio files are available at http://www.current-biology.com/cgi/ content/full/17/11/R406/DC1
B
A
Highly coordinated duets (%)
Coalition quality depends on ongoing motivation and ability to act collectively [9]. Partners that had been together longer were more likely to produce well- coordinated duets (Figure 1C; Supplemental Experimental Procedures). Coordination of duets thus signals ongoing motivation to act collectively (coalition stability). Furthermore, duet precision is a complex coordination task that might be an index of ability to act collectively [9]: duet ‘tempo’ is slower when partners are far apart, suggesting that precision requires partners to make note-by-note adjustments, with delays caused by the slow speed of sound [7]. Our results provide experimental evidence from the territorial displays of duetting birds that precise temporal coordination between partners signals coalition quality. Previous work has shown benefits of signal coordination in the context of mate attraction. Competition results in precise temporal coordination of signals as male katydids (Neoconocephalus spiza) and fiddler crabs (Uca annulipes) strive to produce the leading calls preferred by females [10,11], while cooperating males in the lekking long-tailed manakin (Chiroxiphia linearis) attract more females if their songs have closely matched frequencies [12]. Our results extend these, showing that selection also favours the evolution of precise temporal coordination of signals between group members cooperating to defend a resource.
of female lions, Panthera leo. Anim. Behav. 47, 379–387. 3. Seddon, N., and Tobias. J.A. (2003). Communal singing in the cooperatively breeding subdesert mesite Monias benschi: evidence of numerical assessment? J. Avian Biol. 34, 72–80. 4. Wiley, R.H., and Wiley, M.S. (1977). Recognition of neighbours’ duets by stripe-backed wrens Campylorhynchus nuchalis. Behaviour 62, 10–34. 5. Marshall-Ball, L., Mann, N., and Slater, P.J.B. (2006). Multiple functions to duet singing: hidden conflicts and apparent cooperation. Anim. Behav. 71, 823–831. 6. Hall, M.L. (2000). The function of duetting in magpie-larks: conflict, cooperation, or commitment? Anim. Behav. 60, 667–677. 7. Hall, M.L. (2006). Convergent vocal strategies of males and females are consistent with a cooperative function of duetting in Australian magpie-larks. Behaviour 143, 425–449. 8. Hall, M.L. (1999). The importance of pair duration and biparental care to
reproductive success in the monogamous Australian magpie-lark. Aust. J. Zool. 47, 439–454. 9. Hagen, E.H., and Bryant, G.A. (2003). Music and dance as a coalition signaling system. Hum. Nature-Int Bios. 14, 21–51. 10. Greenfield, M..D, and Roizen, I. (1993). Katydid synchronous chorusing is an evolutionarily stable outcome of female choice. Nature 364, 618–620. 11. Backwell, P., Jennions, M., Passmore, N., and Christy, J. (1998). Synchronized courtship in fiddler crabs. Nature 391, 31–32. 12. Trainer, J.M., and McDonald, D.B. (1995). Singing performance, frequency matching and courtship success of longtailed manakins (Chiroxiphia linearis). Behav. Ecol. Sociobiol. 37, 249–254.
School of Botany and Zoology, Australian National University, Canberra, A.C.T., 0200, Australia. E-mail: [email protected]