7.3 Neighbor Recognition and the Dear Enemy Effect in Anurans
7.3.1 Bullfrogs (Ranidae)
7.3.1.1 Bullfrogs: Natural History
It was not long after the publications of Wilson’s (1975)Sociobiology: The New Synthesis, marking the dawn of behavioral ecology, and Wells’ (1977) seminal paper on anuran social and reproductive behaviors that North American bullfrogs (Rana catesbeiana) claimed center stage in studies describing anuran mating and territorial behaviors and quantifying factors that influence reproductive success (Emlen1976; Howard1978a,b,1979,1981,1983,1984; Ryan1980). These studies reported on key features of bullfrog behavior that would lay a solid foundation for future studies of neighbor recognition in this species. The species’mating system is characterized as resource defense polygyny, though as predicted by Wells (1977), there is some variation in the mating system, with males apparently engaging in lek polygyny prior to sorting out stable territorial boundaries with their neighbors.
Males establish and defend territories on the surface of the water or along the bank of ponds, lakes, and streams. Females oviposit in these territories, in which the structure of submerged vegetation turns out to be an important breeding resource.
Not all territories are created equally, and these early studies revealed that larger males win more fights over territories and they possess better territories, as mea- sured, for example, in terms of embryo survival. Individual males can occupy the same territory for more than 4 weeks, and adjacent neighbors can share a common territorial boundary for more than 2 weeks (Haas1977; Bee2001b). While floating in its territory, a male bullfrog produces advertisement calls consisting of one or more (usually about six or seven) long notes or “croaks,” each lasting about 700 ms and separated from the next by about 500 ms (Fig. 7.3a). Studies investigating patterns of individual distinctiveness in bullfrog advertisement calls are reviewed in Sect. 7.4.1. When approached by an intruder who calls in close proximity, a territorial male will use acoustically distinctive aggressive calls (Wiewandt1969) and approach the intruder in a splashy display. If the intruder persists, territorial contests can escalate to all-out physical combat (Fig.7.4). Larger males typically win more contests, and the most escalated contests occur between males of similar size. Of greatest relevance to considering vocally mediated social recognition in bullfrogs are the facts that males are territorial and aggressive and exhibit reason- ably long-term defense of a breeding resource.
Fig. 7.3 (continued) (a) Five-note call from a North American bullfrog (Rana catesbeiana). (b) Three-note call from a golden rocket frog (Anomaloglossus beebei). (c) Pulsatile call of an agile frog (Rana dalmatina); recording courtesy of Vanessa Sarasola, Rafael Marquez, and www.
Fonozoo.com. (d) Call group of a strawberry poison frog (Oophaga pumilio) depicted at two different timescales (d1andd2); thehighlighted boxind1shows the portion of the call group depicted ind2. (e) Two examples (e1ande2) of a “long call” produced by two different males of the concave-eared torrent frog (Odorrana tormota); recordings courtesy of Albert Feng, Peter Narins, and Junxian Shen. (f) Four-note call from an olive frog (Babina adenopleura)
7.3.1.2 Bullfrogs: Neighbor Recognition
Davis (1987) investigated whether territorial male bullfrogs could discriminate between their neighbors and strangers based on individual differences in advertise- ment calls. In the first of two experiments, he used a within-subjects design to present territorial males with the prerecorded calls of an adjacent territorial neigh- bor or an unfamiliar stranger. After removing the neighbor, sounds were presented from a speaker floating on a Styrofoam platform positioned in the neighbor’s territory. Playbacks of the two stimulus types were separated by brief time-outs of 15–20 min, and stimulus order was counterbalanced across subjects. Davis (1987) counted the numbers of advertisement calls and aggressive calls elicited by each stimulus, and he measured the number of meters subjects approached toward the playback speaker. Ten of the 11 subjects responded more strongly to playbacks of the calls of a stranger compared with those of their neighbor (Fig. 7.5a). No males exhibited more escalated responses to the calls of their neighbor compared with those of a stranger. These results, which were consistent Fig. 7.4 Two male bullfrogs (Rana catesbeiana) fighting over a territory. Shown here is a series of photographs (a–d) of a fight sequence. (a) Two males initially face off while directing advertisement calls and distinctive aggressive calls toward their opponent. (b) The encounter eventually escalates to physical combat in which the two males wrestle and grapple with each other. (c,d) One male (the eventual loser) is flipped onto its back and submerged below the surface of the water. These sorts of fights are common, especially early during the breeding season, as neighboring males sort out stable territory boundaries. Photos copyright Robert McCaw (www.
robertmccaw.com), used with permission
with numerous previous studies of neighbor recognition in territorial songbirds, were the first data (and for nearly 15 years, the only data) indicating that territorial frogs can perceptually and behaviorally discriminate between the calls of neighbors and strangers in ways consistent with the dear enemy effect.
But Davis (1987) went one step further in a second experiment, in which he presented the advertisement calls of each subject’s neighbor from both the neigh- bor’s usual territorial position and from the opposite side of the subject’s territory.
Similar designs had been used in previous studies of songbirds to show that residents associate the songs of neighbors with particular locations. The typical outcome of such experiments in songbirds was that subjects responded more aggressively toward the familiar songs of neighbors presented from an incorrect or novel location. And this is what Davis (1987) found too. All nine of his subjects responded more aggressively toward a neighbor’s call coming from an unfamiliar location compared to when it came from the neighbor’s normal location (Fig.7.5b).
Fig. 7.5 Results from a playback study of the dear enemy effect in bullfrogs (Rana catesbeiana). Results shown are redrawn from Davis (1987) and depict the mean numbers of advertisement calls and aggressive calls produced and the distances moved toward the playback speaker in response to (a) the calls of a neighbor or stranger broadcast from the direction of the neighbor’s usual territory and (b) the calls of a neighbor broadcast from the direction of the neighbor’s usual territory or from a new, unfamiliar location on the opposite side of the subject’s territory
The standard interpretation of such results is that territory holders can do more than merely discriminate between familiar and unfamiliar sounds (Beer 1970; Falls 1982). Rather, they can also learn to associate familiar sounds with a particular location.
That Davis’s (1987) results with bullfrogs exhibited such remarkable similarity to those reported previously in many songbirds suggested some anurans might possess perceptual and cognitive abilities beyond those historically attributed to this group, for which learning in the context of communication is often dismissed.
More to the point, Davis’s (1987) results were important because they showed evolutionary convergence in thebehaviorsof territorial anurans and songbirds in the context of social recognition. To what extent there has been convergence in the perceptual and cognitive mechanisms underlying these behavioral similarities is a largely open question.
A number of methodological issues deserve discussion because they potentially qualify Davis’s (1987) interpretation of his results. Two issues relate to the number of strangers used as stimulus donors and what they sounded like. First, though he typically describes his first experiment using the plural form “strangers,” Davis’s (1987) text is not entirely clear on whether his playbacks used a single stranger stimulus, a small subset of stranger stimuli, or a unique stranger stimulus for each neighbor. This uncertainty goes to the generalizability of his results, and some would say to the issue of pseudoreplication, though to be fair to Davis (1987), these contentious issues of playback design would not erupt in the literature for 2 more years (Catchpole1989; Kroodsma 1989a,b,1990; Searcy1989; McGregor et al.
1992; Kroodsma et al.2001). Second, Davis (1987) provided no description of the acoustic properties of his neighbor and stranger stimuli. Is there some chance that his stranger stimuli were (or stimulus was) perceived as somehow more threatening than neighbors, for example, by virtue of having acoustic properties that conveyed information about larger size, superior fighting ability, or higher motivation to fight? This seems unlikely given the results of later work showing that territorial bullfrogs did not behaviorally discriminate between stimuli having different fun- damental frequencies, an acoustic property strongly predictive of body size, which in turn predicts fighting ability in this species (Bee 2002). Nevertheless, this uncertainty underscores a persistent need to carefully characterize the acoustic properties of sounds used as neighbor and stranger stimuli. A third issue concerns the presence of neighbors in the unfamiliar locations used in Experiment 2. Davis (1987) only reports that “If a second neighbor occupied a territory opposite the subject male..., then it was also removed prior to the playback session.” This issue is relevant because it remains ambiguous as to whether subjects respondedonlyto a change in a familiar neighbor’s position or whether they responded to replacing a neighbor on one side of their territory with a neighbor from the opposite side. The latter scenario has been interpreted as evidence of recognition of multiple individ- uals in some songbird studies. Whether frogs can recognize multiple familiar neighbors thus remains an open and important question.