Acoustic communication in the gray treefrog,Hyla versicolor: evolutionary and neurobiological implications
Acoustic communication in the gray treefrog,H. versicolor, was studied by analyzing the vocalizations of males and observing the phonotactic behavior of gravid females in response to pairs of synthetic stimuli, which usually simulated choices between calls of conspecific males at different temperatures or choices between calls of conspecific males and those of a sibling species,H. chrysoscelis. Calls ofH. chrysoscelis were also analyzed acoustically.
Pulse duty cycle (pulse duration divided by pulse period) averaged about 0.50 in the calls of both species over a wide range of temperature (Table 1). Pulse rise-time (as a percentage of pulse duration), which was also temperature-independent, was significantly longer inH. versicolor than inH. chrysoscelis (Table 1). The species difference in pulse shape was evident at a distance of 10 m from calling frogs (Fig. 1).
Females strongly preferred a linear approximation to the pulse shape (rise-time) typical of conspecific calls to an approximation of the pulse shape typical ofH. chrysoscelis (Figs. 1, 2A). Females did not show a preference between linear and exponential approximations of the conspecific pulse shape (Figs. 1, 2B).
When offered choices between synthetic calls that differed in pulse rate (pulses per s=p/s), females were usually very selective, choosing a stimulus with a pulse rate typical of a conspecific male at the test temperature over alternatives that differed by as little as 25% (Figs. 4–6). When both the call rate and pulse rate of synthetic calls were changed (Fig. 3), females showed temperature-dependent reversals in preference between 16 and 24°C (16 p/s vs 25 p/s) and between 16 and 20°C (15 p/s vs 20 p/s), but not between 20 and 24°C (20 p/s vs 25 p/s) (Table 2A–C).
When the call rates of alternative stimuli were the same, the pulse rate selectivity of females at 20°C was biased toward stimuli with low pulse rates (Table 2F). Females tested at 16°C rejected strongly alternatives with a high pulse rate, but females tested at 24°C did not reject strongly alternatives with a low pulse rate (Table 2E). Females tested at 24°C were also less selective than females tested at 20°C in rejecting alternatives with a high pulse rate, in the range ofH. chrysoscelis (Table 2D). Females tested at 24°C did, however, strongly reject an alternative with both a pulse rate and pulse shape typical ofH. chrysoscelis (Fig. 6).
Call duration and call rate were also relevant properties; changes in these variables modified preferences based on differences in pulse rate, provided that the pulse rates of both alternatives were within the range of variation produced by conspecific males over the normal range of breeding temperatures (Figs. 4–6).
Females showed a weak preference for synthetic calls with a bimodal spectral structure typical of conspecific males (1.1 kHz [−6 dB]+2.2 kHz) to a synthetic call with a single spectral component of 2.2 kHz. In tests of single-component stimuli of 1.9 or 2.2 kHz against alternatives of lower and higher frequencies, female preferences indicated a pattern of relative frequency sensitivity (Fig. 7) that was similar to that of an audiogram based on evoked potentials in the midbrain over the same range of frequency.
About 50% of the females tested responded phonotactically to a recorded call ofH. chrysoscelis when they had no other choice (Table 3). Thus, heterospecific signals were not only audible, but also behaviorally effective in the context of courtship.
Pattern of female preferences with respect to pulse shape and pulse rate suggest that the potential for mismating with males ofH. chrysoscelis has been an important selective force in the evolution of acoustic pattern discrimination inH. versicolor.
Results of this study are compared with those of other anurans and acoustic insects. Temperature-dependent shifts in temporal pattern preference, similar but less pronounced than those reported here for both fine temporal and gross temporal properties, were found in some species but not in others.
The pulse rate of the male's call increases linearly over a wide range of temperature (9–34°C; Gayou 1984), but female selectivity for pulse rate differs within the range of 16–24°C and is biased toward low pulse rates (Table 2). Thus, it is unlikely that both the temporal patterning of the male's call and temporal pattern recognition by the female are controlled rigidly and linearly by the same neural circuitry.
We discuss neurophysiological studies of temporal pattern selectivity in acoustic insects and anurans. There are several neural correlates of behavioral selectivity in gray treefrogs, but no published data concerning a neural correlate of the asymmetry in the strength of pulse rate preferences in gray treefrogs.
KeywordsPulse Rate Pulse Shape Female Preference Acoustic Communication Conspecific Male
pulses per second
Unable to display preview. Download preview PDF.
- Bogart JP (1980) Evolutionary implications of polyploidy in amphibians and reptiles. In: Lewis W (ed) Polyploidy: biological relevance. Plenum, New York, pp 341–378Google Scholar
- Brenowitz EA, Rose G, Capranica RR (1985) Neural correlates of temperature coupling in the vocal communication system of the gray treefrog (Hyla versicolor). Brain Res 359:364–367Google Scholar
- Doherty JA (1985a) Temperature coupling and ‘trade-off’ phenomena in the acoustic communication system of the cricket,Gryllus bimaculatus De Geer (Gryllidae). J Exp Biol 114:17–35Google Scholar
- Doherty JA (1985b) Trade-off phenomena in calling song recognition and phonotaxis in the cricket,Gryllus bimaculatus (Orthoptera, Gryllidae). J Comp Physiol A 156:787–801Google Scholar
- Doherty JA (1985c) Phonotaxis in the cricket,Gryllus bimaculatus De Geer: comparisons of choice and no-choice paradigms. J Comp Physiol A 157:279–289Google Scholar
- Doherty JA, Gerhardt HC (1984) Acoustic communication in hybrid treefrogs: sound production by males and selective phonotaxis of females. J Comp Physiol A 154:319–330Google Scholar
- Doherty JA, Hoy RR (1985) Communication in insects III. The auditory behavior of crickets: some views of genetic coupling, song recognition, and predator detection. Q Rev Biol 60:457–472Google Scholar
- Eggermont JJ, Epping WJM (1986) Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. III. Stimulation with natural and synthetic mating calls. Hearing Res 24:255–268Google Scholar
- Epping WJM, Eggermont JJ (1986) Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. II. Stimulation with amplitude modulated sound. Hearing Res 24:55–72Google Scholar
- Gayou DC (1984) Effects of temperature on the mating call ofHyla versicolor. Copeia 1984:733–738Google Scholar
- Gerhardt HC (1974) The significance of some spectral features in mating call recognition in the green treefrog (Hyla cinerea). J Exp Biol 61:229–241Google Scholar
- Gerhardt HC (1975) Sound pressure levels and radiation patterns of the vocalizations of some North American frogs and toads. J Comp Physiol 102:1–12Google Scholar
- Gerhardt HC (1978) Temperature coupling in the vocal communication system of the gray treefrogHyla versicolor. Science 199:992–994Google Scholar
- Gerhardt HC (1981a) Mating call recognition in the green treefrog (Hyla cinerea): importance of two frequency bands as a function of sound pressure level. J Comp Physiol 144:9–16Google Scholar
- Gerhardt HC (1981b) Mating call recognition in the barking treefrog (Hyla gratiosa): responses to synthetic calls and comparisons with the green treefrogs (Hyla cinerea). J Comp Physiol 144:17–25Google Scholar
- Gerhardt HC (1982) Sound pattern recognition in some North American treefrogs (Anura: Hylidae): implications for mate choice. Am Zool 22:581–595Google Scholar
- Gerhardt HC (1983) Acoustic communication in treefrogs. Verh Dtsch Zool Ges 1983:25–35Google Scholar
- Gerhardt HC (in press) Acoustic properties used in call recognition by frogs and toads. In: Fritzsch B, Hetherington T, Ryan M, Wilczynski W, Walkowiak W (eds) The evolution of the amphibian auditory system. John Wiley, New YorkGoogle Scholar
- Hall J, Feng AS (1986) Neural analysis of temporally patterned sounds in the frog's thalamus: processing of pulse duration and pulse repetition rate. Neurosci Letters 63:215–220Google Scholar
- Hedwig B (1986) On the role in stridulation of plurisegmental interneurons of the acridid grasshopperOmocestus viridulus L. II. Anatomy and physiology of ascending and T-shaped interneurons. J Comp Physiol A 158:429–444Google Scholar
- Helversen O von (1979) Angeborenes Erkennen akustischer Schlüsselreize. Verh Dtsch Zool Ges 1979:42–59Google Scholar
- Helversen O von, Helversen D von (1981) Korrespondenz zwischen Gesang und auslösenden Schema bei Feldheuschrekken. Nova Acta Leopoldina 54:449–462Google Scholar
- Hillery CM (1984) Detection of amplitude-modulation tones by frogs: implications for temporal processing mechanisms. Hearing Res 14:129–143Google Scholar
- Hoy RR, Paul RC (1973) Genetic control of song specificity in crickets. Science 195:82–83Google Scholar
- Huber F, Thorson J (1985) Cricket auditory communication. Sci Am 253:60–68Google Scholar
- Klump GM, Gerhardt HC (1987) Use of non-arbitrary acoustic criteria in mate choice by female gray treefrogs. Nature (London) 326:286–288Google Scholar
- Littlejohn MJ, Loftus-Hills JJ (1968) An experimental evaluation of premating isolation in theHyla ewingi complex (Anura: Hylidae). Evolution 22:659–663Google Scholar
- Littlejohn MJ, Fouquette MJ, Johnson C (1960) Call discrimination by female frogs of theHyla versicolor complex. Copeia 1960:47–49Google Scholar
- Lombard RE, Straughan IR (1974) Functional aspects of anuran middle ear structures. J Exp Biol 61:57–71Google Scholar
- Ralin DB, Selander RK (1979) Evolutionary genetics of diploidtetraploid species of treefrogs of the genusHyla. Evolution 33:595–608Google Scholar
- Ralin DB, Romano MA, Kilpatrick CW (1983) The tetraploid treefrogHyla versicolor: evidence for a single origin from the diploid H.chrysoscelis. Herpetologica 39:212–225Google Scholar
- Rose GJ, Capranica RR (1984) Processing amplitudemodulated sounds by the auditory midbrain of two species of toads: matched temporal filters. J Comp Physiol A 154:211–219Google Scholar
- Rose GJ, Capranica RR (1985) Sensitivity to amplitude modulated sounds in the anuran auditory system. J Neurophysiol 53:446–465Google Scholar
- Rose GJ, Brenowitz EA, Capranica RR (1985) Species specificity and temperature dependency of temporal processing by the auditory midbrain in two species of treefrogs. J Comp Physiol A 157:763–769Google Scholar
- Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185Google Scholar
- Schneider H (1982) Phonotaxis bei Weibchen des Kanarischen Laubfrosches,Hyla meridionalis. Zool Anz (Jena) 208:161–174Google Scholar
- Schwartz JJ (1987) The function of call alternation in anuran amphibians: a test of three hypotheses. Evolution 41:461–471Google Scholar
- Taigen TL. Wells KD (1985) Energetics of vocalization by an anuran amphibian (Hyla versicolor) J Comp Physiol B 155:163–170Google Scholar
- Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378Google Scholar
- Walkowiak W (1984) Neuronal correlates of the recognition of pulsed sound signals in the grass frog. J Comp Physiol A 155:57–66Google Scholar
- Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9–18Google Scholar