Why do Chinese alligators (Alligator sinensis) form bellowing choruses: A playback approach

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1 Why do Chinese alligators (Alligator sinensis) form bellowing choruses: A playback approach Xianyan Wang Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan , People s Republic of China and Graduate School of the Chinese Academy of Sciences, Beijing , People s Republic of China Ding Wang a Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan , People s Republic of China Song Zhang, Chaolin Wang, and Renping Wang Anhui Research Center for the Chinese Alligator Reproduction, Xuancheng , People s Republic of China Xiaobing Wu College of Life Sciences, Anhui Normal University, Wuhu , People s Republic of China Received 17 September 2008; revised 8 February 2009; accepted 13 July 2009 Crocodilians are quite vocal relative to other reptile groups, and the alligators are among the most vocal of the crocodilians. The Chinese alligator, Alligator sinensis, is usually solitary but engages in bellowing choruses in certain waters during the mating season. This paper reports the organization of Chinese alligator s bellowing choruses based upon field observations and playback experiments. Alligators of both genders engaged in the choruses, remaining immobile throughout and inclining toward bellowing synchronously i.e., starting and finishing at about the same time. The choruses lasted about 10 min with abrupt onset and offset. Moreover, playback experiments revealed that both male and female alligators responded equally to bellowing stimuli from the same and opposite sexes and that none of the tested alligators approached the loudspeaker in spite of playback of male or female stimuli. These suggest that Chinese alligators may not bellow to compete for or attract mates during the choruses. Instead, when their ecological behaviors, namely, dispersed inhabitation, multi-copulation, restricted mating season, etc., are considered, we hypothesize that they may synchronize bellows to enhance group detectability for assembling individuals into certain waters for subsequent copulations Acoustical Society of America. DOI: / PACS number s : Ka MCH Pages: I. INTRODUCTION a Author to whom correspondence should be addressed. Electronic mail: wangd@ihb.ac.cn An efficient system of signals and responses is important for successful reproduction Patterson, The role of acoustic signals in reproduction has been well investigated in insects Minckley et al., 1995; Snedden, 1996; Snedden and Greenfield, 1998, amphibians Wells, 1988; Schwartz, 1993, 2001; Cocroft and Ryan, 1995; Kime et al., 2004, birds Morse, 1989; Lind et al., 1996; Liu et al., 1998, and mammals Southall et al., 2003; Notman and Rendall, 2005; Deecke et al., Diverse vocal behaviors and acoustic tactics are employed in different species reproduction patterns. Many studies of anurans, for example, have shown that overlapping calls are less attractive to females than nonoverlapping calls Schwartz and Wells, 1983, 1984; Wells and Schwartz, 1984, especially if the overlap obscures fine temporal properties of the call Schwartz, Males may respond to the calls of their neighbors in ways that help them maintain or increase their relative attractiveness. For instance, they may elevate the rate, complexity, duration, and intensity of their call, and may also shift the timing of their advertisement calls or call elements to reduce the potential for acoustic interference or to increase the likelihood that their signals will lead rather than follow those of their neighbors reviewed in Schwartz and Buchanan, Reptiles, in general, are relatively nonvocal, and consequently their acoustic signals and vocal behaviors have received relatively little attention Marcellini, 1977; Vliet, 1989; Young, Some reptile groups, especially the crocodilian species, produce striking vocalizations during the mating season Zhu, 1957; Campbell, 1973; Gans and Maderson, 1973; Herzog and Burghardt, 1977; Chen et al., 1985, 2003; Vliet, 1989; Wang et al., 2006, 2007, but there are very few reports that address the precise roles of these acoustic signals in successful reproduction. The Chinese alligator, Alligator sinensis, is one of the most endangered of the 23 crocodilian species in the world Thorbjarnarson, Wild individuals currently number less than 150 and are restricted to a small area in southern Anhui Province and perhaps in adjacent Zhejiang and Jiangsu Provinces of China Ding et al., 2001; Chen et al., 2082 J. Acoust. Soc. Am , October /2009/126 4 /2082/6/$ Acoustical Society of America

2 TABLE I. Characteristic parameters of 26 Chinese alligators 13 males and 13 females used in playback experiments. Mean Std. deviation Minimum Maximum Male BL cm Snout-vent length cm Weight kg Female BL cm Snout-vent length cm Weight kg Chinese alligators are usually solitary and territorial but move into specific ponds, lakes, swamps, and marshes for copulation during mating season from late May through middle June Chen et al., 1985, 2003; Wang et al., 2006, Previous investigations have shown that vocal communication plays a vital role in social interactions and reproduction of Chinese alligators Zhu, 1957; Chen et al., 1985, 2003; Wu and Wang, 2004; Wang et al., Though both male and female alligators bellow throughout the active season, these vocalizations are greatly heightened during the mating season Wu and Wang 2004; Wang et al., During the mating period, the bellows of one alligator stimulate neighboring others to bellow, eventually forming a chorus Wang et al., The choruses are believed to be highly related to mating, but the mechanisms are still unknown. Because both male and female Chinese alligators participate in these bellowing choruses and it is difficult to differentiate males from females by appearance alone, or by different vocal behaviors as American alligator Alligator mississippiensis has, clear observations seem rarely possible. The present report describes the first experiments to address this issue by playing back male and female bellowing stimuli to both male and female alligators individually to determine the mechanism involved in the bellowing chorus. II. METHODS A. Study site and subjects Experiments were carried out during the mating season of Chinese alligator in 2006 and 2008 within Anhui Research Center for Chinese Alligator Reproduction ARCCAR, located in Xuancheng City in Southern Anhui Province, China. The study site is a reproductive enclosure N, E that primarily consists of four permanent ponds. Most individuals of the reproductive cohort are wild-caught, although a few are first- and second-generation offsprings from artificial reproduction see Zhang et al and Wang et al for more details. The focal field observation pond was approximately 2000 m 2 with a 400 m 2 island densely covered by shrub situated in the center. During the study, a total of 26 Chinese alligators 13 males and 13 females were harmlessly captured and transported to a m 3 outdoor arena individually. All captured alligators were sexually mature snout-head rubbing, mounting behaviors, and bellowing activities had been observed before capture. The gender of each alligator was confirmed by touching the cloaca. Immediately after capture, the body length BL and snout-vent length of each alligator were measured, and the weight was calculated based on the following formula: weight= BL BL BL 3, provided by Chen et al Table I. B. Field observations To avoid disturbing the animals, field observations were performed behind a brick boundary wall 1.5 m high using the naked eye and/or Fujinon 7 50 binoculars at distances ranging from 2 to 30 m. We collected information on behavioral context, number of bellows in each bellowing sequence i.e., a succession of bellows produced in a regularly repeated unit Garrick et al., 1978, total number of sequences, and responses from neighboring animals to focal bellowers using the target objective observation method Zhang et al., 2005 during choruses. We also noted individuals activities after choruses. C. Playback experiments The signals used for playback experiments were recorded from 19 male and 23 female alligators in captivity within ARCCAR using an omnidirectional Fidek KSM-81 microphone frequency response: Hz, +5.5/ 11.4 db, Japan connected to a Sony TCD-D100 digital audio tape recorder sampling frequency: 48 khz, Japan and Sony digital audio tape. All vocalizations were recorded at a distance of approximately 3 m. The recordings were replayed from the recorder and were then transformed into, and saved as, sound files in wav format on a computer by PC-based signal processing software, COOL EDIT PRO 2.0, with a 22 khz sampling frequency and 16-bit. The software was also used to edit and playback sound files during playback experiments. We chose signals with high signal-to-noise ratio and representative of the population mean as playback stimuli. After each alligator was transported to the arena, it was given more than 48 h to adapt to its new surroundings before testing began. Some fish were provided according to the feeding arrangement of ARCCAR during the playback period. The tested alligator was released at the same place where it was captured when tests were completed, and another alligator was brought into the arena. Because Chinese alligator has two pairs of musk glands that are believed to release substances that influence social interaction Chen et al., 1985, 2003, the arena was always washed before a new alligator was introduced to it. As bellowing activities mostly occurred in shallow water Wang et al., 2006, water depth in the arena during playback experiments was controlled and ranged from 11.6 to 19.0 cm according to the BL J. Acoust. Soc. Am., Vol. 126, No. 4, October 2009 Wang et al.: Bellowing chorus of Chinese alligators 2083

3 FIG. 1. Color online Wave form and spectrogram of bellows of a male Chinese alligator. a Wave form of a sequence of four bellows used in playback experiments. Panels b and c show the wave form and spectrogram, respectively, of the second bellow of the sequence. of each alligator, which may facilitate the head oblique and tail arched bellowing posture see Wang et al., Both air and water temperatures were measured during the playback period air temperature: C; water temperature: C. Playback experiments were conducted between 0600 and 0700 h, a period corresponding to the time of natural bellowing activity of Chinese alligators Wang et al., 2006 during clam and dry weather conditions to avoid sound propagation problems due to wind. Stimuli were broadcast from an IBM computer using the COOL EDIT PRO 2.0 software over a Shock wave SC-2105 amplified speaker effective range Hz, which was mounted on the arena wall, 1 m above the floor. Peak sound pressure levels SPLs, in db of playback stimuli were verified at 90 db re 20 Pa, measured 5 m from the loudspeaker using a hand-held Realistic sound level meter type DT-805, re 20 Pa, C-weighting, fast response. This level corresponded to that of natural bellows at that distance Wang et al., After the equipment were installed and verified, more than 30 min was spent on acclimation before playback tests commence at about 0600 every morning. Four male or female bellows were broadcast with a silent interval of 2.5 s i.e., a bellowing sequence, Fig. 1 a and 2 a, a rhythm that corresponds to that of natural bellows emission. Then, after at least a 5-min period of silence, another bellowing sequence was broadcast. Each alligator was presented with three male sequences and three female sequences. The order of sequence presentation was randomized to avoid habituation. Totally, 78 male and 78 female bellowing sequences were edited and played back, each broadcast only once. D. Criteria of responses and data analysis On the basis of natural observations, responses of alligators to bellows of neighboring individuals were ranked as follows: 0 none, no reaction to the stimulus tagged as no reaction ;1 weak, presented a head oblique and tail arched posture but did not bellow tagged as HOTA ; and 2 strong, responded to the stimulus by bellowing with a FIG. 2. Color online Wave form and spectrogram of bellows of a female Chinese alligator. a Wave form of a sequence of four bellows used in playback experiments. Panels b and c show the wave form and spectrogram, respectively, of the second bellow of the sequence. HOTA posture tagged as bellowing. If the emitted stimuli induced no change in the behavior of the focal animal within 5 min of being presented, we scored it as a no reaction. We monitored each alligator s response and timed response latency i.e., time between stimulus onset and the alligator s response in every playback trial behind the arena wall. Statistical analysis was done using the mean response per subject as the sample points; thus, the sample size is the number of subjects. The two-tailed Wilcoxon paired-sample signed rank test was used to compare the response intensities of male and female alligators to the same- and opposite-sex stimuli and the differences in the latency of responses to male and female stimuli. Statistical significance was set at P All statistical calculations were carried out using SPSSs III. RESULTS A. General description of bellowing choruses Choruses were usually initiated by vocalizations from one alligator other times by meteorological thunders and then intensified as neighboring individuals joined in. Alligators tended to bellow synchronously i.e., starting and finishing at about the same time, and choruses were characterized by abrupt onsets and offsets. Choruses lasted for a period of min means SD; N=103. During the mating season, the inter-chorus silence was h means SD; N=123. Alligators remained immobile during choruses, but vigorous swimming, snout-head rubbing, and mounting behaviors were frequently observed afterwards. B. Both male and female alligators responded equally to the same- and opposite-sex stimuli Playback tests showed that male alligators responded equally to the same- and opposite-sex stimuli Z= 0.597, N=13, and P=0.551 Fig. 3 a. Male stimuli evoked 79.5% bellowing, 12.8% HOTA, and 7.7% no reaction. Female stimuli evoked 76.9% bellowing, 12.8% HOTA, and 10.3% no reaction. Response latencies to male and female stimuli 2084 J. Acoust. Soc. Am., Vol. 126, No. 4, October 2009 Wang et al.: Bellowing chorus of Chinese alligators

4 10.3% HOTA, and 2.5% no reaction to female stimuli. Response latencies to male and female stimuli were also not significantly different Z= 1.58, N=13, and P=0.114 Fig. 4 b. None of the tested alligators approached the loudspeaker during any trial in spite of playback of male or female stimuli. IV. DISCUSSION FIG. 3. Response intensities of tested alligators to male and female bellowing stimuli. a Male and b female alligators responded equally well to the same- and opposite-sex bellowing stimuli. Bars show means+sd and N =13. were not significantly different Z= 0.490, N=13, and P =0.624 Fig. 4 a. Female alligators also responded equally well to male and female stimuli Z= 1.51, N=13, and P =0.131 Fig. 3 b, with 76.9% bellowing, 15.4% HOTA, and 7.7% no reaction to male stimuli and 87.2% bellowing, FIG. 4. Response latencies of tested alligators to male and female bellowing stimuli. There is no significant difference in the response latencies of a male and b female alligators to the same- and opposite-sex bellowing stimuli. Bars show means+sd and N=13. In numerous densely congregative insects and anuran species, competitive interactions between males are the best explanation for the emergence of synchronized vocalizations Greenfield and Roizen, 1993; Greenfield, 1994; Greenfield et al., During choruses, males advertise vocally to attract females for mating Minckley et al., 1995; Schwartz and Buchanan, Females, on the other hand, are in general voiceless and move among the males to choose appropriate mates on the basis of their advertisement calls Morris, 1991; Howard and Young, 1998; Wollerman and Wiley, 2002; Smith and Roberts, Unlike many insect and anuran species, however, the following reasons indicate that Chinese alligators may not bellow to compete for or attract mates during choruses: i both male and female Chinese alligators engage in bellowing choruses and bellow synchronously; ii attending alligators remain stationary throughout; and iii the choruses last only about 10 min with abrupt onset and offset, with an average of bellows per alligator during each chorus Wang et al., Male and female alligators bellow synchronously and remain stationary throughout the chorus, suggesting that male bellows may not be attractive to neighboring females; otherwise, females would approach bellowing males and vice versa. In addition, unlike those of insects and anurans, which last several hours or even throughout an entire night Brenowitz and Rose, 1999; Grafe, 1999, a 10- min alligator chorus might not be sufficient for every individual to find an appropriate mate. No alligator bellowed alone after the end of the choruses. Our deduction is further supported by studies by Chen et al. 1985, 2003 and Wang et al. 2006, in which they found that bellowing activities mostly occur during and h, which is more than 12 h ahead of the peak time of copulation around midnight. Bellowing activity involves a significant energy cost Chen et al., 1985, The bellows have an average SPL of 90.8 db re 20 Pa at 5 m distance. Chinese alligators may not have enough energy to bellow as long as insects and anurans do, so the chorus lasts just 10 min and the total number of bellows per alligator is during a chorus Wang et al., This might explain why the Chinese alligator does not bellow to compete for or attract mates. The deduction is also strengthened by results from the playback experiments that both male and female alligators respond equally to same- and opposite-sex bellowing stimuli without ambiguity and that none of the tested alligators approach the loudspeaker in spite of playback of male or female stimuli, which indicate that bellowing choruses may have other biological functions rather than as signal to compete for or attract mates. Besides, for attracting mates, the J. Acoust. Soc. Am., Vol. 126, No. 4, October 2009 Wang et al.: Bellowing chorus of Chinese alligators 2085

5 following hypotheses have also been proposed to explain why certain animals synchronous chorusing might be adaptive, none but the last one of which seems reasonable for Chinese alligators: Species synchronize calling i to establish dominance hierarchy, ii to confuse predators, and iii to enhance group detectability i.e., by maximizing the peak amplitude of group signaling reviewed in Grafe, Studies of the American alligator show that bellowing activity provides information about the body size and social status of the active bellower Garrick and Lang, 1977; Garrick et al., Hierarchy is obvious in some crocodilian species, such as Nile crocodile Crocodylus niloticus, Indian gavial Gaviails gangeticus, and Estuarine crocodile Crocodylus porosus reviewed in Chen et al., Thus, one might suggest the possibility that Chinese alligators bellow to increase their dominance status, with large, aggressive individuals controlling access to mates and resources. In reality, however, Chinese alligators live in separate territories throughout most time of the year, and dominance hierarchies do not seem to exist Chen et al., 1985, Hence, this hypothesized function for Chinese alligator bellowing seems implausible. Study on neotropical tree frog Smilisca sila shows that overlapping calls attract fewer predatory bats than alternating calls Tuttle and Ryan, Yet, Chinese alligator is at the top of the local food chain no predator is known to attack adult Chinese alligator Chen et al., 1985, So, it is hard to say that Chinese alligators synchronize bellowing to reduce predation. Chinese alligator lives in temperate climates, which force mating to occur within a restricted time frame Chen et al., 1985, Male alligator mates with more than one female and female alligator can produce clutches fathered by more than one male Chen et al., 1985, 2003; Davis et al., This means that the females can carry offspring of various genetic compositions, which help the alligators tolerate and thrive in new environments and habitats Davis et al., Consequently, with widely distributed individuals congregating into a small number of waters, it becomes quite cost-efficient for alligators to copulate with more mates in a limited time frame. Meanwhile, an efficient communication signal is required for them to locate certain aggregative waters in the dense vegetative habitat. Compared to visual and olfactory signals, auditory signal is an effective way for Chinese alligators to locate certain aggregative waters. Dense vegetation restricts visual communication, and efficacy of olfactory signaling is low Chen et al., 2003; Wang et al., The bellow, characterized by low dominant frequency and high SPL, which facilitate propagation in the high densely vegetated environment Wang et al., 2007, can serve as an efficient beacon that allows widely dispersed alligators of both genders to locate a certain breeding aggregation. The synchronous bellows of many alligators help to enhance group detectability over a further spatial range and also provide information about the number of attending alligators, which would contribute to a larger number of copulations. These may explain why both male and female alligators respond equally to the same- and opposite-sex bellowing stimuli to form bellowing choruses and why there is a 12-h interval between peak times of bellowing and copulations. The field observation of Wang et al finds that bellowing chorus does have congregative effect during the mating season. As the current wild alligators are mainly scattered in the h m 2 national reserve, it results in a lack of communication between individuals and, in turn, a lack of reproductive success Ding et al., Although the tested alligators are living in semi-natural condition though once wildcaught, their higher density may lead to a population with reproductive behaviors that more closely reflect the wild alligators prior to reaching the endangered situation of the present. This study would be useful in the reintroduction of artificially reproduced alligators back to the wild. But further works, such as those on Chinese alligator s hearing capability, active space of the bellows, and alligator s responses at different distances from the source to single and chorused bellows, are required to directly test the hypothesis about enhancing group detectability. ACKNOWLEDGMENTS The authors are extremely grateful to Hongxing Zhu, Tongsheng Xia, Jialong Zhu, Xuesong Zhang, Jiangjiang Zhou, Yongkang Zhou, and Yijiang Ou of ARCCAR, Songhai Li and Kexiong Wang of Research Group on Conservation Biology of Aquatic Animals of the Institute of Hydrobiology, Chinese Academy of Sciences, and Baoshan Xia of College of Life Sciences, Anhui Normal University for providing helpful suggestions in conducting playback experiments. The authors would also like to express appreciation to the two reviewers for their valuable comments on this manuscript. Financial support was provided by National Basic Research Program of China Grant No. 2007CB and National Natural Science Foundation of China Grant No Brenowitz, E. A., and Rose, G. J Female choice and plasticity of male calling behaviour in the Pacific treefrog, Anim. Behav. 57, Campbell, H. H Observations on the acoustic behavior of crocodilians, Zoologica N.Y. 58, Chen, B. H., Hua, T. M., Wu, X. B., and Wang, C. 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