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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.
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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, 1Kate Davis 2 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 )Unitaryre- sponses for two odorants with different potencies onthesamecellare 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. 2 0 01- 5- 0 2 1 0 0 03 06 2 1 0 0 51 03 1 0 03 - 51 - 0 0552 0 0 5 1 0 3 A Mean (pA) )s( t 0 5 σ2(pA 2) ) s m 52( elo eni c )sm 0 5( enonehp otec a pA Conc. (mM) Conc. (mM) B eloe ni c M m 2 sm 05 sm 52 pA pA ) s( t pA T (ms) REPORTS 24 JUNE 2005 VOL 308 SCIENCE www.sciencemag.org 1934 on February 27, 2012 www.sciencemag.org Downloaded from that encode this information (6). Such var- iation in alarm signals can be used to trans- fer information about the type of predator E referential alarm call systems ( 7)^ ,thedegree of threat that a predator represents Erisk-based systems ( 8)^ ,orboth( 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)andto 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 chick adeesE and often many other species ( 17)^ that harass, or mob, a perched predator. This B chick-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 05.17, PG 0.0001 ^, with the smaller, higher risk, preda- tors eliciting significantly more calls than the larger predators or controls (Tukey _s post hoc tests: PG0.05). The total number of syllables per alarm call differed among predator treat- ments ( F03.05, PG0.0001). In particular, the average number of D syllables, or notes, per call differed significantly across predator treatments ( F07.771, PG0.0001). 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; r 200.512, PG0.0001). 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- 0 3 6 9 1.0 0.5 0 )zHk( ycneuqerF -50 -30 -20 -10 0 -40 654321 Frequency (kHz) ev i tale R) Bd( ed util pmA A AB C C D D D B F1F2 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 00). 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'speregrinered 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 l l ac rep s e ton D fo rebm uN 20 40306050 10 Predator body length (cm) 1.5 3.5 2.0 2.5 3.0 4.0 1.0 4.5 20 40 100 60 12080 140 saw-whet pygmy-owl Cooper'speregrine red tailgreat horned gyrfalcon great gray kestrel short-eared prairie rough-leg bobwhite merlin llac rep s eton D fo rebmuN 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 ( y0 4.4 – 0.02 x; r 20 0.512, PG 0.0001). ( B)MeannumberofD syllables per call as a function of body length for raptors and mammals ( y0 4.4 – 0.4 x; r 20 0.361, P G 0.0001). Each taxonomic group of raptors is represented by a different symbol ( &,owl; r, falcon; h,hawk; ,mammal).Abobwhitequail ( > ) was used as the procedural control. The dashed line displays the mean number of D notes per control trial without any stimulus. REPORTS www.sciencemag.org SCIENCE VOL 308 24 JUNE 2005 1935 on February 27, 2012 www.sciencemag.org Downloaded from included in the analysis (Fig. 2B;r 200.361, P G0.0001).
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, P00.003), the interval between the Bchick [and Bdee [sections was signifi- cantly shorter ( F011.364, P00.001), the first D note of each call was shorter ( F0 9.984, P00.003), and the interval between the first and second D notes was also shorter in small predator alarm call variants (F 0 9.043, P00.004). 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 ( F02.855, P00.097) spanning a wider bandwidth ( F02.719, P00.105) than those produced during encounters with small pred- ators. D notes elicited by large predators also tended to have more widely spaced overtones ( F 03.385, P00.071). No differences were observed in any of the other measured features ( P 90.2 for all).
Do these acoustic differences in mobbing calls transmit information about the potential predator to other chickadees? We conducted playback experiments ( 18)totesthow chickadees reacted to the mobbing calls that they produced in response to different pred- ators by broadcasting variations of the B chick-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 K011.50, P00.003).
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 ( K014.69, P00.001); more individ- uals approached within 3 m (Fig. 3B; K0 14.40, P00.001) and within 1 m ( K011.34, P 00.003) 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 012.69, P00.002).
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 sl l ac "eed - a-kcihc" #rekaeps g nihca o rppa sd r iB 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). REPORTS 24 JUNE 2005 VOL 308 SCIENCE www.sciencemag.org 1936 on February 27, 2012 www.sciencemag.org Downloaded from behavior. Our results show that chickadees do not vocally discriminate between raptors and mammals when they are presented in similar ways, and thus theBchick-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- spanandbodysizeinbirds( 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 B chick-a-dee [) signifies the degree of danger presented by that specific predator encounter.
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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 REPORTS www.sciencemag.org SCIENCE VOL 308 24 JUNE 2005 1937 on February 27, 2012 www.sciencemag.org Downloaded from
