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DOI: 10.1126/science.1108841 , 1934 (2005);308 Science
, et al.Christopher N. Templeton Information About Predator Size Allometry of Alarm Calls: Black-Capped Chickadees Encode
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the stimulus duration-response relation in Fig.
4B would not have remained linear). Thus,
phosphorylation and arrestin binding are un-
likely to constitute the standard termination of
olfactory responses. Possibly, phosphorylation
is important for desensitization in situations
of prolonged and intense stimulation.
A short-lived receptor-odorant complex
does not preclude an overall high olfactory
sensitivity. Repeated bindings of odorant
molecules to the same receptor allow signal
integration, especially if receptor phosphoryl-
ation does not occur (unlike in vision, where
a photon acts only once and a photobleached
pigment molecule is nonfunctional). The total
rate of odorant-binding events is also ampli-
fied by orders of magnitude by the total num-
ber of receptor molecules on an ORN. The
supralinear interactions occurring when uni-
tary transduction domains overlap can further
enhance sensitivity at intermediate odorant
concentrations and durations. Finally, a high
convergence of sensory input at the glomer-
ulus (23) may boost sensitivity. The glomer-
ulus is the synaptic plexus in the olfactory
bulb that integrates signals from all ORNs
expressing the same odorant receptor species.
In principle, this convergence can increase
indefinitely by simply expanding the surface
area of the olfactory epithelium and therefore
the number of ORNs expressing a given odor-
ant receptor. This increase in convergence may
explain why the olfactory sensitivity in many
animals is much higher than it is in humans.
Unlike the retinotopic map in vision, which
imposes a functional limit on the degree of
convergence from photoreceptors, no corre-
sponding limitation exists in olfaction.
References and Notes 1. L. B. Buck, Cell 100, 611 (2000). 2. D. Schild, D. Restrepo, Physiol. Rev. 78, 429 (1998).
3. H. R. Matthews, J. Reisert, Curr. Opin. Neurobiol. 13, 469 (2003).
4. A. Menini, C. Picco, S. Firestein, Nature 373, 435 (1995).
5. G. Lowe, G. H. Gold, Proc. Natl. Acad. Sci. U.S.A. 92, 7864 (1995).
6. G. H. Gold, G. Lowe, Nature 376, 27 (1995). 7. S. Firestein, C. Picco, A. Menini, J. Physiol. 468, 1 (1993). 8. D. A. Baylor, T. D. Lamb, K.-W. Yau, J. Physiol. 288,
613 (1979). 9. T. D. Lamb, P. A. McNaughton, K.-W. Yau, J. Physiol.
319, 463 (1981). 10. G. Lowe, G. H. Gold, J. Physiol. 442, 147 (1991). 11. J. Reisert, H. R. Matthews, J. Gen. Physiol. 112, 529
(1998). 12. Materials and methods as well as additional notes are
available as supporting material on Science Online. 13. S. J. Kleene, Neuroscience 66, 1001 (1995). 14. J. del Castillo, B. Katz, J. Physiol. 124, 560 (1954). 15. S. Serizawa et al., Science 302, 2088 (2003). 16. J. W. Lewcock, R. R. Reed, Proc. Natl. Acad. Sci.
U.S.A. 101, 1069 (2004). 17. J. J. Tesmer, R. K. Sunahara, A. G. Gilman, S. R. Sprang,
Science 278, 1907 (1997). 18. Leskov et al., Neuron 27, 525 (2000). 19. K.-W. Yau, Invest. Ophthalmol. Vis. Sci. 35, 9 (1994). 20. T. M. Dawson et al., Science 259, 825 (1993). 21. S. Schleicher, I. Boekhoff, J. Arriza, R. J. Lefkowitz, H.
Breer, Proc. Natl. Acad. Sci. U.S.A. 90, 1420 (1993). 22. K. Peppel et al., J. Biol. Chem. 272, 25425 (1997). 23. P. Mombaerts et al., Cell 87, 675 (1996). 24. K. Nakatani, K.-W. Yau, Nature 334, 69 (1988). 25. K. Nakatani, K.-W. Yau, J. Physiol. 395, 695 (1988). 26. We thank D. A. Baylor, P. A. Fuchs, J. S. Kauer, T. D.
Lamb, J. Nathans, R. R. Reed, F. Rieke, D. T. Yue, and members of the Yau laboratory, especially J. Bradley and C.-Y. Su, for critique and discussions, V. Kefalov for help in initial experiments, and D. Chaudhuri for help in computations using MatLab. V.B. also thanks D. McClellen for instruction in scientific writing. This work was supported by Howard Hughes Medical Institute and grants from NIH (DC06904) and the Human Frontier Science Program.
Supporting Online Material www.sciencemag.org/cgi/content/full/308/5730/1931/ DC1 Materials and Methods Figs. S1 to S4 References and Notes
18 January 2005; accepted 3 May 2005 10.1126/science.1109886
Allometry of Alarm Calls: Black-Capped Chickadees Encode Information About Predator Size
Christopher N. Templeton,1*. Erick Greene,1 Kate Davis2
Many animals produce alarm signals when they detect a potential predator, but we still know little about the information contained in these signals. Using presentations of 15 species of live predators, we show that acoustic features of the mobbing calls of black-capped chickadees (Poecile atricapilla) vary with the size of the predator. Companion playback experiments revealed that chickadees detect this information and that the intensity of mobbing behavior is related to the size and threat of the potential predator. This study demonstrates an unsuspected level of complexity and sophistication in avian alarm calls.
Predation is a major cause of mortality for
most species of animals, and many produce
alarm signals when they perceive a potential
predator (1). Alarm calls often differ in
acoustic structure, depending on the situation
in which they are produced (2–5). If a
species is preyed upon by different predators
that use different hunting strategies or vary
in the degree of danger they present, selec-
tion can favor variation in alarm signals
Fig. 4. (A) Unitary re- sponses for two odorants with different potencies on the same cell are very similar. (Top) Re- lation between re- sponse amplitude and odorant concentration for acetophenone and cineole odorants. Each point represents the av- erage of four to eight stimulus trials. Although the duration of aceto- phenone stimulation was twice as long as that for cineole, the response with all recep- tors bound by aceto- phenone was a factor of 7 less than the re- sponse to cineole. (Bot- tom) Variance/mean analysis of the unitary response to the two odorants. The quantal responses to the two odorants were similar (0.48 pA for cineole and 0.56 pA for acetophenone). Thirty trials each of 100 mM cineole at 25-ms duration and 2 mM acetophenone at 50-ms duration. The two stimuli were chosen to produce responses of comparable amplitudes. The slight difference in response kinetics for the two odorants was due to a change in cell condition during the experiment; this was not observed in other experiments. We chose this cell because of the large difference in efficacy between the two odorants. (B) Estimation of cineole dwell-time on the receptor. (Top) Relation between response amplitude and cineole concentration at two durations. Even when all receptors were bound (Q1 mM cineole), the response amplitude increased linearly with the odorant pulse duration. Each point represents the average of 3 to 20 stimulus trials. (Bottom) Complete data from the same experiment at a saturating cineole concentration of 2 mM and applied for four different durations. (Inset) Linear increase of the response with odorant duration. The time inter- cept of the linear-regression fit is near zero.
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R E P O R T S
24 JUNE 2005 VOL 308 SCIENCE www.sciencemag.org1934
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that encode this information (6). Such var-
iation in alarm signals can be used to trans-
fer information about the type of predator
Ereferential alarm call systems (7)^, the degree of threat that a predator represents Erisk-based systems (8)^, or both (9, 10).
In addition to discriminating among
broad types of predators (e.g., raptor versus
snake), discriminating among morphologi-
cally similar predators within a single type
(e.g., different species of raptors) could also
be adaptive if the predators vary in the
degree of threat they pose. One species that
is faced with numerous, morphologically
similar predators is the black-capped chick-
adee (Poecile atricapilla). Chickadees are
small, common songbirds that are wide-
spread throughout North America. In the non-
breeding season, chickadees form flocks of six
to eight birds (11). They use an elaborate
system of vocalizations to mediate social
interactions in these flocks (12, 13) and to
warn conspecifics about predators (14, 15).
Chickadees produce two very different
alarm signals in response to predators: When
flying raptors are detected, chickadees pro-
duce a high-frequency, low-amplitude Bseet[ alarm call; in response to a perched or sta-
tionary predator, they produce a loud, broad-
band Bchick-a-dee[ alarm call that is composed of several types of syllables (16) (Fig. 1A).
Whereas the Bseet[ alarm call functions to warn of flying predators, the Bchick-a-dee[ mobbing alarm call recruits other chickadees
Eand often many other species (17)^ that harass, or mob, a perched predator. This
Bchick-a-dee[ call is a complex vocalization that is also produced in many other situations
and encodes information about food and
identity (both individual and flock) in addi-
tion to information about predators (11).
We examined variation in the mobbing
vocalizations and behavior of black-capped
chickadees by conducting predator presenta-
tions and playback experiments with chick-
adees living under semi-natural conditions in
large, outdoor experimental aviaries (18).
We presented flocks of color-marked chick-
adees with 13 species of live, perched raptors
and two species of live mammalian preda-
tors. The predators varied considerably in
body size (e.g., factor of 20 difference in
body mass between northern pygmy-owl and
great horned owl), activity patterns, hunting
strategies, and diet (Table 1). The raptors
ranged from small, maneuverable predators
whose diets include many small birds, to
large, less maneuverable predators that eat
few small birds. We also used two types of
controls: a procedural control with a live
bobwhite quail (Colinus virginianus); and no
presentation, with observers present as they
would be during predator presentations. Dur-
ing each predator presentation, two observers
recorded chickadee vocalizations, noting the
color band combination of each calling in-
dividual. By conducting controlled presenta-
tions of live predators to birds living under
semi-natural conditions, we could isolate
vocal responses to specific species of pred-
ators from other features such as the loca-
tion, behavior, or movement pattern of the
predator.
Spectrographic analyses of the more than
5000 Bchick-a-dee[ mobbing alarm calls we
recorded (Fig. 1) revealed previously un-
suspected levels of acoustic variation. The
number of mobbing calls produced in response
to each predator was highly variable [analy-
sis of variance (ANOVA): F 16, 34
0 5.17, P G 0.0001^, with the smaller, higher risk, preda- tors eliciting significantly more calls than the
larger predators or controls (Tukey_s post hoc tests: P G 0.05). The total number of syllables per alarm call differed among predator treat-
ments (F 0 3.05, P G 0.0001). In particular, the average number of D syllables, or notes,
per call differed significantly across predator
treatments (F 0 7.771, P G 0.0001). There was a strong inverse relationship between the
number of D notes per alarm call and the
wingspan of the raptors, with the smallest
predators eliciting calls with the most D notes
(Fig. 2A; r2 0 0.512, P G 0.0001). There was also a strong inverse relationship between the
number of D notes and predator body length
when both the mammals and raptors were
1Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA. 2Raptors of the Rockies, Post Office Box 250, Florence, MT 59833, USA.
*Present address: Department of Biology, Box 351800, University of Washington, Seattle, WA 98195, USA. .To whom correspondence should be addressed. E-mail: [email protected]
Fig. 1. Features of the ‘‘chick-a-dee’’ mobbing vocalization. (A) The call usually contains both ‘‘chick’’ sections (A, B, and C syllable types) and ‘‘dee’’ sec- tions (D syllable types) (11). (B) Acoustic varia- bles measured from power spectrum analy-
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evit al
e R
) B
d( e
d util
p m
A A
A B C C D D D
B F1
F2
L U
P
M
"chick" "dee"
Time (s) ses from the center of a D note. The amplitude has been scaled relative to the highest energy overtone (dB 0 0). Acoustic variables were the peak frequency (P), the lower and upper frequencies above –10 dB (L and U, respectively), the frequency of the first and second peaks above –30 dB (F1 and F2, respectively), and the maximum frequency peak above –30 dB (M). The bandwidth at –10 dB was calculated by subtracting L from U; the bandwidth at –30 dB was calculated by subtracting F1 from M. The interval between overtones was deter- mined by subtracting F1 from F2.
saw-whet pygmy-owl
Cooper's
peregrine red tail
great horned gyrfalcon
great gray
kestrel
short-eared
prairie
rough-leg
bobwhite
merlin cat
ferret
1.5
3.5
2.0
2.5
3.0
4.0
1.0
4.5
ll ac r
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et o
n D f
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b m
u N
20 4030 605010 Predator body length (cm)
1.5
3.5
2.0
2.5
3.0
4.0
1.0
4.5
20 40 10060 12080 140
saw-whet pygmy-owl
Cooper's
peregrine
red tail great horned
gyrfalcon great gray
kestrel
short-eared
prairie
rough-leg
bobwhite
merlin
ll ac r
e p s
et o
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b m
u N
Predator wingspan (cm)
B
A
Fig. 2. Chickadees vary their mobbing calls in response to variation in predator body size. (A) Mean number of D syllables per call as a function of wingspan for raptors ( y 0 4.4 – 0.02x; r2 0 0.512, P G 0.0001). (B) Mean number of D syllables per call as a function of body length for raptors and mammals ( y 0 4.4 – 0.4x; r2 0 0.361, P G 0.0001). Each taxonomic group of raptors is represented by a different symbol (&, owl; r, falcon; h, hawk; �, mammal). A bobwhite quail (>) was used as the procedural control. The dashed line displays the mean number of D notes per control trial without any stimulus.
R E P O R T S
www.sciencemag.org SCIENCE VOL 308 24 JUNE 2005 1935
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included in the analysis (Fig. 2B; r2 0 0.361, P G 0.0001).
Many other acoustic features of these
mobbing calls (Fig. 1) also varied in relation
to the predator treatment. For example, in
comparisons of mobbing calls given in re-
sponse to a northern pygmy-owl and a great
horned owl (small and large predators, re-
spectively), the duration of the Bdee[ section (all D notes) was significantly longer (ANOVA:
F 1,14
0 9.984, P 0 0.003), the interval between the Bchick[ and Bdee[ sections was signifi- cantly shorter (F 0 11.364, P 0 0.001), the first D note of each call was shorter (F 0 9.984, P 0 0.003), and the interval between the first and second D notes was also shorter
in small predator alarm call variants (F 0 9.043, P 0 0.004). Calls that chickadees produced during the large predator presen-
tations tended to have D notes that con-
tained more high-energy peaks above –10
dB (F 0 2.855, P 0 0.097) spanning a wider bandwidth (F 0 2.719, P 0 0.105) than those produced during encounters with small pred-
ators. D notes elicited by large predators also
tended to have more widely spaced overtones
(F 0 3.385, P 0 0.071). No differences were observed in any of the other measured features
(P 9 0.2 for all). Do these acoustic differences in mobbing
calls transmit information about the potential
predator to other chickadees? We conducted
playback experiments (18) to test how
chickadees reacted to the mobbing calls that
they produced in response to different pred-
ators by broadcasting variations of the
Bchick-a-dee[ alarm vocalization associated with different predators. We played mobbing
calls that flock mates produced in response
to a great horned owl (large predator), a north-
ern pygmy-owl (small predator), and control
calls of a pine siskin (Carduelis pinus).
Chickadees exhibited longer and more intense
mobbing behavior when they heard alarm
calls recorded in response to a pygmy-owl
than when they heard alarm calls recorded in
response to a great horned owl or control vo-
calizations (Fig. 3). They produced signifi-
cantly more Bchick-a-dee[ calls in response to playback of mobbing alarm calls elicited by a
small predator than they did when presented
with playbacks of mobbing calls elicited by a
large predator or control vocalizations (Fig.
3A; Kruskal-Wallis K 0 11.50, P 0 0.003). Chickadees approached the hidden speaker
more closely in response to the small predator
mobbing call treatment than in response to the
large predator mobbing call or control treat-
ments (K 0 14.69, P 0 0.001); more individ- uals approached within 3 m (Fig. 3B; K 0 14.40, P 0 0.001) and within 1 m (K 0 11.34, P 0 0.003) of the speaker in response to the small predator alarm calls than in response to
the large predator alarm calls or control
vocalizations. After playback of small preda-
tor alarm calls, chickadees also mobbed for
longer periods than they did after playback of
large predator alarm calls and control sounds
(K 0 12.69, P 0 0.002). Previous studies have shown that animals
produce different antipredator vocalizations
for aerial and terrestrial predators. Most of
these studies, however, have presented these
two types of predators in different ways
(19–21), potentially confounding the inter-
pretation that prey distinguish between types
of predators and not their location or
Table 1. Species presented to chickadee flocks. Length and wingspan were measured from animals used in experiments; mass (26) and diet information (27–29) were summarized from published accounts. The sex of each raptor used in the experiments is indicated in brackets.
Predator species Mass (g)
Length (cm)
Wingspan (cm)
Time active
Primary diet
Hawks Cooper’s hawk
(Accipiter cooperii) [F] 450 44 81 Day Small birds
Red-tailed hawk (Buteo jamaicensis) [F]
1,080 53 120 Day Small mammals, few birds
Rough-legged hawk (B. lagopus) [M]
990 49 138 Day Small mammals
Falcons American kestrel
(Falco sparverius) [M] 117 25 58 Day Inverts, small mammals,
small birds Merlin (F. columbarius) [F] 190 28 61 Day Small birds Peregrine falcon
(F. mexicanus) [F] 720 47 120 Day Medium-sized birds
Prairie falcon (F. peregrinus) [F]
720 45 100 Day Small mammals, some birds
Gyrfalcon (F. rusticolus) [M] 1,400 52 115 Day Medium-sized mammals and birds
Owls Northern pygmy-owl
(Glaucidium gnoma) [M] 70 15 31 Day Small birds, small mammals
Saw-whet owl (Aegolius acadicus) [M]
80 17 39 Night Small mammals, some small birds
Short-eared owl (Asio flammeus) [M]
350 34 89 Both Small mammals
Great horned owl (Bubo virginianus) [M]
1,400 48 121 Night Small to medium-sized mammals
Great gray owl (Strix nebulosa) [M]
1,080 58 132 Both Small mammals
Mammals Domestic cat
(Felis domesticus) 15,000 45 — Both Birds, small mammals, insects
Ferret (Mustela putorius) 1,000 32 — Day Small mammals, eggs, some small birds
Control Bobwhite quail
(Colinus virginianus) 170 22 42 Day Seeds, insects
0
20
10
30
0
2
4
3
5
1
Control Large Predator
Small Predator
sll ac "
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B 6
40 A
B
Alarm Call Treatment
Fig. 3. Chickadees respond to predator-specific acoustic variations in their mobbing alarm calls. Two behavioral variables were used to quantify chickadees’ responses to the three playback stimuli: control sounds (pine siskin calls), ‘‘chick- a-dee’’ calls produced in response to a large predator (great horned owl), and ‘‘chick-a-dee’’ calls produced in response to a small predator (northern pygmy-owl). (A) Boxplots (showing median, interquartile range (IQR), range, and outliers) of the number of ‘‘chick-a-dee’’ calls produced during the first 90 s after the start of each playback treatment. (B) Boxplots of the number of birds approaching within 3 m of the speaker after each treatment. All pairwise comparisons were significantly different (Mann- Whitney U, P G 0.05).
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behavior. Our results show that chickadees do
not vocally discriminate between raptors and
mammals when they are presented in similar
ways, and thus the Bchick-a-dee[ call does not refer specifically to the type of predator.
Instead, these vocal signals likely con-
tain information about the degree of threat
that a predator represents. Maneuverability
(e.g., as measured by turning radius, or
radial acceleration) is extremely important
in determining the outcome of predator-prey
interactions and is inversely related to wing-
span and body size in birds (22, 23). Body
size may be a good predictor of risk for
chickadees: Small raptors tend to be much
more maneuverable than larger raptors and
likely pose a greater threat to chickadees.
In addition to being one of the most sub-
tle and sophisticated signaling systems yet
discovered, this system is unusual in that it
combines aspects of both referential and
risk-based antipredator vocalization systems
(10, 24, 25). To denote the presence of a rap-
idly moving predator (e.g., raptor in flight),
chickadees produce a Bseet[ alarm call. When they encounter a stationary predator (e.g.,
perched raptor), they use the Bchick-a-dee[ mobbing call. These two vocalizations appear
to be functionally referential to the type of
predator encounter (i.e., each denotes a spe-
cific type of encounter). In addition, we have
shown that subtle variation in the Bchick-a- dee[ mobbing call reflects the size of a specific predator, a characteristic of a risk-
based system. Thus, chickadees convey infor-
mation about predators at two different levels:
A coarse level of encoding (Bseet[ or Bchick- a-dee[) signifies the type of predator encoun- ter, and a fine level of encoding (variants of
Bchick-a-dee[) signifies the degree of danger presented by that specific predator encounter.
The Bchick-a-dee[ vocalization is remark- ably versatile; it is used in many different
contexts and apparently conveys many differ-
ent types of information. The fact that so
much information can be transmitted by subtle
variations in one type of vocalization raises
some fascinating questions about how finely
chickadees can discriminate between similar
stimuli, and how they categorize different as-
pects of their environment.
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29. K. R. Foresman, The Wild Mammals of Montana (Allen, Lawrence, KS, 2001).
30. We thank K. Dial for discussions about scaling; J. Graham for statistical advice; C. Eldermire, N. Schwab, and C. Putnam for help with data collection; and D. Emlen, B. Walker, and M. Parker for helpful comments on the manuscript. Supported by donations from Marchie’s Nursery, Caras Nursery, Swift Instruments, and the Birdwatcher’s Country Store.
Supporting Online Material www.sciencemag.org/cgi/content/full/308/5730/1934/ DC1 Materials and Methods
17 December 2004; accepted 4 May 2005 10.1126/science.1108841
R E P O R T S
www.sciencemag.org SCIENCE VOL 308 24 JUNE 2005 1937
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