Vocally Mediated Social Recognition in Frogs

Territorial animals often respond less aggressively toward established neighbors, compared to unfamiliar individuals, based on the perception of individual differences in vocalizations (Bee 2005). This behavior, which is often termed "individual voice recognition", "neighbor recognition", "neighbor-stranger discrimination", or the "dear enemy effect", is common among songbirds and is believed to be an adaptation for avoiding repeated interactions with territorial neighbors. Davis (1987, Behav Ecol Sociobiol 21: 185-190) showed that, like male songbirds, territorial males of the North American bullfrog (Rana catesbeiana) can discriminate between their territorial neighbors and unfamiliar conspecifics based on a combination of vocal and spatial cues. A major goal of our research has been to better understand the nature of this adaptation by investigating the mechanisms and evolution of neighbor recognition in territorial frogs.

North American Bullfrogs (Rana catesbeiana) and Green Frogs (Rana clamitans ) - We have conducted extensive acoustic and statistical analyses to determine what aspects of the bullfrog and greenfrog advertisement call are individually distinctive in order to determine how individual identity is conveyed in advertisement calls (Bee et al. 2001, Bee & Gerhardt 2001b, Bee 2004). In our analyses, fundamental frequency exhibited the lowest within-individual variation, the highest ratio of among-individual to within-individual variation, and the highest repeatability between recordings made on different days. In a multivariate discriminant function analysis, calls were assigned to the correct individual more often than expected by chance, and fundamental frequency was significantly correlated with the first discriminant function, which explained most of the variation among individuals. The reason that fundamental frequency varies so little within individuals is because this call property is determined largely by body size. Hence, the size-related variation in fundamental frequency among male in the population could function as a reliable voice recognition cue in many cases. Based on these acoustical and statistical analyses, we hypothesized that neighbor-stranger discrimination in bullfrogs could be partially mediated by individual differences in the spectral or fine-temporal properties related to the perceived pitch of advertisement calls.

We have conducted field playback experiments with bullfrogs based on the habituation-discrimination paradigm to investigate the perceptual basis of neighbor-stranger discrimination in this species (Bee and Gerhardt 2001b, 2001c, 2002). Playabacks initially evoked intense aggressive responses. With repeated playbacks during an the habituation phase, the magnitude of aggressive responses decreased. In the subsequent discrimination phase, changes in the fundamental frequency, the sound source location, or both the frequency and location of the acoustic stimulus elicited significant recovery of habituated aggressive responses. In some tests, individuals discriminated differences in fundamental frequency as small as 5-10%, which fall within the range of among-individual differences in this call property. Changes in the harmonic fine-structure of the stimulus, or changes in gross temporal properties of the amplitude envelope, generally failed to elicit renewed aggression in the discrimination phase. These results are the first to show that frogs possess the ability to learn to recognize a conspecific by an individually distinctive voice property. Neighbor-stranger discrimination based on the pitch of acoustic signals is also known from two songbirds. Thus, my results demonstrate evolutionary convergence in the vocally mediated social recognition systems of territorial frogs and songbirds.

Strawberry Dart-poison Frogs (Dendrobates pumilio) - In an effort to better understand the evolution of neighbor recognition in territorial frogs, we have conducted a comparative neighbor-stranger playback study with the territorial strawberry dart-poison frog (Dendrobates pumilio) in Panama (Bee 2003a). This is a species that defends long-term breeding or multi-purpose territories and has individually distinctive calls (Prohl, 2003, Ethology 109:273–290; Prohl & Berke 200, Oecologia 129:534–542). We presented territorial males with the calls of their nearyby neighbors and those of unfamiliar strangers. Based on the hypothesis that the defense of long-term breeding territories selects for the evolution of "dear enemy" relationships between territorial neighbors (Temeles, 1994, Anim Behav 47:339–350), we predicted that males would respond more aggressively toward strangers than toward the calls of their neighbors. Surprisingly, we found absolutely no differences in how males responded to neighbors and strangers. Our results call into question Temeles' (1994) hypothesis and suggest that certain perceptual constraints might limit the evolution of dear enemy recognition in some species.

Ongoing Work - We are currently investigating vocally mediated neighbor recognition in two additional frog species that also appear to defend long-term breeding or multi-purpose territories. Beth Pettitt, a Ph.D. student in the lab, is currently working in Guyana to study the territorial and vocal behavior of the golden rocket frog (Anomaloglussus beebei). We are also working in collaboration with Chuan Ming-Feng and Kam Yeong-Choy from the Tunghai University in Taiwan to investigate vocally mediated neighbor recognition in another territorial ranid frog (Rana adenopleura) that is only distantly related to North American bullfrogs and gree frogs.

Related Publications:

• Bee MA (2005) Individual recognition in animal species. In: The Encyclopedia of Language and Linguistics: Volume 2. (section editor, Naguib M), Elsevier Science: London, pp. 617-626. PDF

• Bee MA (2003a) A test of the "dear enemy effect" in the strawberry dart-poison frog (Dendrobates pumilio). Behavioral Ecology and Sociobiology, in press. PDF

• Bee MA (2003b) Experience-based plasticity of acoustically evoked aggressive behavior in a territorial frog. Journal of Comparative Physiology A, 189: 485-496. PDF

• Bee MA and Gerhardt HC (2002) Individual voice recognition in a territorial frog (Rana catesbeiana). Proceedings of the Royal Society of London Series B, 269, 1443-1448. PDF

• Bee MA (2001) Habituation and sensitization of aggression in bullfrogs (Rana catesbeiana): Testing the dual-process theory of habituation. Journal of Comparative Psychology, 115, 307-316. PDF

• Bee MA and Gerhardt HC (2001a) Habituation as a mechanism of reduced aggression between adjacently territorial male bullfrogs (Rana catesbeiana). Journal of Comparative Psychology, 115, 68-82. PDF

• Bee MA and Gerhardt HC (2001b) Neighbour-stranger discrimination by territorial male bullfrogs (Rana catesbeiana): I. Acoustic basis. Animal Behaviour, 62, 1129-1140. PDF

• Bee MA and Gerhardt HC (2001c) Neighbour-stranger discrimination by territorial malebullfrogs (Rana catesbeiana): II. Perceptual basis. Animal Behaviour, 62, 1141-1150. PDF

• Bee MA, Kozich CE, Blackwell KJ, and Gerhardt HC (2001) Individually distinct advertisement calls of territorial male green frogs, Rana clamitans: Implications for individual discrimination. Ethology, 107, 65-84. PDF