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Acoustic Interference and Recognition Space Within a Complex Assemblage of Dendrobatid Frogs

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Acoustic Interference and Recognition Space Within a Complex Assemblage of Dendrobatid Frogs Acoustic interference and recognition space within a complex assemblage of dendrobatid frogs Adolfo Amézquitaa,1, Sandra Victoria Flechasa, Albertina Pimentel Limab, Herbert Gasserc, and Walter Hödlc aDepartment of Biological Sciences, Universidad de los Andes, Bogotá, AA 4976, Colombia; bInstituto Nacional de Pesquisas da Amazônia, CEP 69060-001, Manaus, Brazil; and cDepartment of Evolutionary Biology, Institute of Zoology, University of Vienna, A-1090 Vienna, Austria Edited by Michael J. Ryan, University of Texas at Austin, Austin, TX, and accepted by the Editorial Board September 1, 2011 (received for review March 24, 2011) In species-rich assemblages of acoustically communicating animals, insects (22), and frogs (23, 24). Because heterospecific sounds may heterospecific sounds may constrain not only the evolution of sig- represent noise that interferes with signal detection (25, 26), the nal traits but also the much less-studied signal-processing mecha- communication systems should reveal adaptations that reduce its nisms that define the recognition space of a signal. To test the effects. To date, most research to validate this idea has been hypothesis that the recognition space is optimally designed, i.e., conducted on the characteristics of the signals or on the pattern of that it is narrower toward the species that represent the higher signaling activity (27, 28), but compelling evidence suggests that potential for acoustic interference, we studied an acoustic assem- recognition systems can evolve without concomitant variation in blage of 10 diurnally active frog species. We characterized their the signals (20, 29). We present here a manipulative study on a calls, estimated pairwise correlations in calling activity, and, to species-rich assemblage of diurnal frogs to test the general model the recognition spaces of five species, conducted playback hypothesis that the recognition space is shaped in a way that experiments with 577 synthetic signals on 531 males. Acoustic co- minimizes the overlapping of signal space with those of co- occurrence was not related to multivariate distance in call param- occurring species. eters, suggesting a minor role for spectral or temporal segregation The importance of acoustic communication for anuran re- among species uttering similar calls. In most cases, the recognition production is well established (30, 31). Typically, male breeding space overlapped but was greater than the signal space, indicating success depends on producing advertisement calls that attract that signal-processing traits do not act as strictly matched filters females. In a fairly less-studied scenario, male breeding success against sounds other than homospecific calls. Indeed, the range of depends on the successful and prolonged defense (against other the recognition space was strongly predicted by the acoustic dis- males) of a territory containing resources essential for re- tance to neighboring species in the signal space. Thus, our data production (32). Males of the latter species announce territory provide compelling evidence of a role of heterospecific calls in ownership by producing redundant series of advertisement calls evolutionarily shaping the frogs’ recognition space within a com- throughout the breeding season; they also react toward conspe- plex acoustic assemblage without obvious concomitant effects on cific calling intruders by increasing signaling rate or intensity and the signal. by attacking them (33). Because both levels of reaction increase energy expenditure and conspicuousness to potential predators, Amazonia | animal communication | bioacoustics | perception natural selection on signal-detection and signal-recognition mech- anisms should be evident in the male–male communication sys- ate-recognition signals mediate successful breeding and, tems of territorial species (20). Mtherefore, are often affected by strong selective forces that Our null hypothesis states that the recognition space of each may lead to adaptation and reproductive isolation (1, 2). Although species occupies the available signal space of the whole frog the causes (3, 4) and consequences (5, 6) of signal evolutionary assemblage; males of each species should then indiscriminately ’ divergence are relatively well studied, much less is known about react to every species signal. We anticipated at least three sce- the evolution of physiological mechanisms underlying the sensory narios that falsify the null hypothesis (Fig. 1). In our matched- processing of signals (7, 8). At the most basic level, signal detection spaces hypothesis, the recognition space is perfectly matched to and signal recognition are prerequisites for the appropriate re- the signal space, indicating pleiotropic relationships between action of receivers, rendering signal-processing traits at least as signal-producing and signal-recognition traits or strong natural selection against detecting sounds other than the signals. Our important as signal traits in potentially affecting the evolutionary matched-spaces hypothesis differs from the original matched- fate of a lineage (9–11). filter hypothesis (34) in including the whole signal space rather Signals must encode a minimum amount of information allow- than only the spectral parameters and in emphasizing the signal ing for species recognition because of the high costs of reacting parameters’ range instead of the average values. In the spectral- toward heterospecific signals as if they were homospecific(“false ” partitioning hypothesis, the recognition space is partitioned in the alarms ) (12, 13). Signal recognition occurs when receivers com- spectral but not in the temporal domain of call parameters, pare detected signals to preexisting templates, often in the central suggesting an effect of masking interference in shaping the rec- nervous system. It is usually tested with playback experiments and ognition space. The filled-gaps hypothesis adds to the spectral- is assumed when tested receivers exhibit overt behavioral respon- partitioning hypothesis by including the temporal domain of the ses (14, 15), i.e., when they “treat as valid” the stimulus signal (16). The recognition space of a given signal is thus estimated as the range of signal values that elicit effective (meeting some minimum Author contributions: A.A., A.P.L., and W.H. designed research; A.A., S.V.F., A.P.L., H.G., criterion) behavioral responses in the receivers (13). and W.H. performed research; A.A. and S.V.F. analyzed data; and A.A. wrote the paper. The recognition space may be larger than necessary for the The authors declare no conflict of interest. fi recognition of conspeci c signals (17, 18), presumably because This article is a PNAS Direct Submission. M.J.R. is a guest editor invited by the Editorial sensory systems trade off their communicative function with other Board. ecological functions such as predator or prey detection (19). The Freely available online through the PNAS open access option. role of heterospecific signals in shaping the recognition space has 1To whom correspondence should be addressed. E-mail: [email protected]. received less attention (20). One example would be the effect of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. masking interference on acoustic communication in birds (21), 1073/pnas.1104773108/-/DCSupplemental. 17058–17063 | PNAS | October 11, 2011 | vol. 108 | no. 41 www.pnas.org/cgi/doi/10.1073/pnas.1104773108 Downloaded by guest on October 2, 2021 EVOLUTION Fig. 1. Four hypotheses on the shape of the recognition space (dotted lines) and its relationship with the signal space defined by individual signals (filled circles) of three hypothetically co-occurring species (colored circles). signal. The recognition space should then extend beyond the limits of the species-specific signals, depending on the multi- variate distance to the neighboring species in the signal space; this result would indicate that recognition spaces are constrained fi by the probability of heterospeci c interference. Because the Fig. 2. Oscillogram (lower, blue) and sonogram (upper, gray) of the ad- last two hypotheses imply a role for heterospecific signals, we vertisement calls of 10 acoustically co-occurring frog species at Panguana, quantified the actual magnitude of this influence by estimating Peru. A1, Allobates sp. 1; A2, Allobates sp. 2; A3, Allobates sp. 3; Af, Allo- species acoustic co-occurrence from recordings of the acoustic bates femoralis; Ah, Ameerega hahneli; Ape, Ameerega petersi; Api, environment. Ameerega picta;At,Ameerega trivittata;La,Leptodactylus andreae;RI, Our aims were thus (i) to estimate the degree of signaling co- Ranitomeya lamasi. occurrence between every pair of species in an assemblage of diurnal frogs, (ii) to characterize the parameters of their ad- calls and arranged in three species as multinote calls. Call vertisement calls, (iii) to estimate the potential of call parameters fi fi parameters were successfully combined in two discriminant axes to allow discrimination between homospeci c and heterospeci c that explained 92.0% of variance and classified very well (98.7% fi signals, (iv) to estimate the recognition space of ve species by of correct classifications) each species’ call (Fig. 3). The variables fi conducting playback experiments, and, nally, (vi) to test the that most contributed to discriminate calls were low frequency four hypotheses (Fig. 1) by mapping the recognition spaces onto (discrimination coefficient = 0.63) in the first discriminant func- the
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