Socially Mediated Plasticity of Aggressive Signaling

In frogs, signaling males usually compete for calling sites or territories from which they advertise to attract females. The benefits of possessing and defending a calling site or territory include having a restricted area that provides access to either a signaling space free from competing signalers, a breeding resource required by females, or both. Defense of a calling site or territory is costly in terms of energy expenditure, increased predation risk, and decreased mate attraction effort. Hence, we might expect mechanisms to evolve that would allow males to modify their level of aggression in competitive interactions in ways that balance the costs of aggressive signaling with the benefits of maintaining a calling site or territory. Recent studies in frogs demonstrate that repeated exposure to a new calling neighbor leads to adaptive modifications in aggression that can serve to ammeliorate these costs. Our lab is interested in understanding the nature of this adaptation in terms of the processes that mediate the decresed levels of aggression between adjacent neighbors, the operation of these processes in the animal's natural enviroment, and the selective advantages associated with plasticity in aggressive signaling. We are examining plasticity of aggressive signaling in two anuran species with very different mating systems in order to understand the similarities and differences in plasticity that may be due to differences in breeding ecology.

Bullfrogs (Rana catesbeiana):

The bullfrog mating system is resource defense polygyny. Males can defend a territory for extended periods (e.g. 2-4 weeks), and often share a common boundary with the same neighbor during this time. The potential costs associated with defending a long-term territory have likely selected for neighbor-stranger discrimination in this species. Previous work on vocally mediated social recognition among territorial male bullfrogs demonstrates that repeated exposure to a neighbor's calls results in decrements in aggression that are long-term and specific to both the signal and its location of origin (Bee and Gerhardt 2001a). These response decrements exhibit many characteristics of a simple form of learning called habituation. Our previous research has examined the operation of these learning processes in the bullfrog's natural habitat. Biotic and abiotic factors related to a subject's body size, physiological condition, and calling activity, the acoustically simulated size and fighting ability of the simulated neighbor, the density of other calling males in the chorus, the overall calling activity in the chorus, the spatial distances between adjacent neighbors, the time of night, and the time of season appear to have little influence on changes in a male's aggressive calling behavior in comparison with factors related to the rate and intensity with which the simulated neighbor calls (Bee 2001). These results strongly suggest that plasticity of the aggressive response is perhaps mediated solely by the interaction itself and is not influenced strongly by other biotic and abiotic factors. At a proximate level, there are a number of explanations that could account for the decreased aggression exhibited during extended playbacks. The patterns of response decrement and stimulus-specific response recovery in response to a potent novel acosutic stimulus in playback tests are inconsistent with explanations such as sensory adaptation, effector fatigue, non-specific changes in motivation, and auditory habituation (Bee 2003b). These results, then, indicate that a centrally-mediated form of long-term learning underlies plasticity of aggressive signaling in bullfrogs. In the future, we will be investigating these processes at the behavioral and physiological levels.

Spring Peepers (Pseudacris crucifer):

In contrast to bullfrogs, spring peepers may be considered a "lek" breeding species, meaning that males congregate at a breeding site and defend exclusive calling sites, but do not defend particular resources needed by females for the purpose of breeding. Moreover, in contrast to bullfrogs, there is little evidence to suggest that male spring peepers are faithful to a particular calling site for many consecutive days. One striking feature of a spring peeper chorus is the temporal and spatial variability in the local density of signaling males, which varies greatly both seasonally and within nights as males join and leave the chorus. Collaborative work with Vince Marshall (University of Illinois) and Sarah Humfeld (University of Missouri) has shown that a short-term form of behavioral plasticity allows male spring peepers to modify their aggressive behavior in an adaptive way that effectively tracks changes in the local density of signaling males in this highly variable social environment (Marshall, Humfeld, & Bee 2003). As density increases, the distance between nearby neighbors decreases, and the perceived amplitude of a neighbor's calls consequently increases. Aggressive signaling is evoked when the perceived amplitude of a neighbor's calls exceeds a male's threshold for switching from advertisement to aggressive calls. We found that a male's "aggressive threshold" is positively correlated with the amplitude of the nearest neighbor's calls at the subject's calling site. Playbacks at intensities above a male's aggressive threshold led to temporary increases in the male's aggressive threshold. These thresholds returned to baseline levels after a 20-minute recovery period during which no calls were broadcast. In these playback tests, a male's aggressive response quickly habituated with repeated playbacks simulating a persistently calling neighbor. In contrast to bullfrogs, in which responses usually habituate over the course of several hours, aggressive responses by male spring peepers habituated in less than a minute. In follow-up tests, we have shown that the habituated aggressive response can be reinstated by broadcasting a different call type as the stimulus (Bee et al. 2002). Together, these results are consistent with the operation of a short-term form of stimulus specific habituation that allows a male's aggressive threshold to track the density of nearby callers. We are interested in continuing this work to test a number of hypotheses about behavioral plasticity and sound pattern recognition.

In several frogs, aggressive calls evoke fewer phonotactic responses from gravid females than do advertisement calls in two-choice phonotaxis tests. Moreover, it is well-established that females frogs, including female spring peepers, prefer males that produce advertisement calls at high rates. Hence, one ultimate-level hypothesis for why the aggressive response of male spring peepers quickly habituates is that males pay a high cost in terms of lost mating opportunities during episodes of aggressive signaling. In two-choice phonotaxis tests in the laboratory, females did prefer advertisement calls to aggressive calls, but this preference was weak and could be abolished by reducing the amplitude of the prefered advertisement calls by just 6 dB, which acoustically simulates a doubling of the distance to the male producing advertisement calls (Marshall, Humfeld, & Bee 2003). Thus female preferences for advertisement calls probably plays some role in selecting for males that avoid prolonged aggressive encounters. We believe, however, that it is an interaction between female mating preferences and energetic constraints associated with aggressive signaling that plays an important functional role in mediating aggression in this species. In the playback tests with males, we found that, over the first minute of stimulation, during which the bulk of aggressive responses occurred, there was no trade-off in the production of advertisement calls and aggressive calls. Thus, we believe that female choice for males that persistently call at high rates imposes a cost on males, because males could lose mating opportunities if advertisement calls were traded off with aggressive calls. Males avoid making this trade-off by increasing their total calling effort by the addition of aggressive calls to advertisement calls during periods of aggressive signaling. This, in turn, imposes high energetic costs. (Acoustic signaling in frogs is one of the most energetically demanding activites known among vertebrates!) Hence, female mate choice and energetic constraints, together, probably function as selective pressures favoring plasticity of aggressive signaling in spring peepers. This hypothesis requires direct testing in the future by measuring the metabolic costs of aggressive signaling.

Related Publications:

• Humfeld SC, Marshall VT, Bee MA (2009) Context-dependent plasticity of aggressive signalling in a dynamic social environment. Animal Behaviour, 78, 915-924. PDF

• Marshall VT, Humfeld SC, and Bee MA (2003) Plasticity of aggressive signalling and its evolution in male spring peepers (Pseudacris crucifer). Animal Behaviour, 65, 1223-1234. 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, Marshall VT, Humfeld SC, and Gerhardt HC (2002) The role of learning in the formation of frog choruses. Integrative and Comparative Biology, 42, 1193.

• 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.

• 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 Schachtman TR (2000) Is habituation a mechanism of neighbor recognition in green frogs? Behavioral Ecology and Sociobiology, 48, 165-168. PDF