How, When, and Where to Perform Visual Displays: the Case of the Amazonian Frog Hyla Parviceps

Herpetologica, 60(4), 2004, 420–429 Ó 2004 by The Herpetologists’ League, Inc.

HOW, WHEN, AND WHERE TO PERFORM VISUAL DISPLAYS: THE CASE OF THE AMAZONIAN FROG HYLA PARVICEPS

1,3 2 ADOLFO AME´ ZQUITA AND WALTER HO¨ DL 1Depto. de Ciencias Biolo´gicas, Universidad de los Andes, A.A. 4976, Bogota´, Colombia 2Institute of Zoology, University of Vienna, Althanstraße 14, A-1090, Vienna, Austria

ABSTRACT: We performed intrusion experiments and observed the course of 13 male-male agonistic interactions to gather information on the communicative role of visual signaling in the Amazonian tree frog Hyla parviceps. To obtain information on the ecological context potentially associated with visual signaling, we performed nightly censuses of calling activity and tested whether males differentially used microhabitats in relation to properties that affect both acoustic and visual communication. Among seven behaviors performed by males, two were visual displays. Foot-flagging displays and advertisement calls were used at a similar rate and at similar distances between interactants. Arm-waving displays were less common and used at a closer range than foot-flagging displays. The analysis of a dyadic transition matrix revealed that foot flagging significantly elicited foot-flagging displays by the opponent frog. Furthermore, resident males produced more arm wavings and calls than intruders, although the latter difference was not significant. We conclude that male H. parviceps respond to intruders by combining advertisement calls and visual displays, and that visual signals may serve functionally as a spacing mechanism. Comparing the properties of perches used by calling males with a random sample of available perches indicates that males prefer perches surrounded by denser and higher vegetation. Furthermore, calling activity occurred during or shortly after heavy rains and coincided with calling activity of several co-occurring species of hylid frogs, which probably decreases the locatability of calling males. We suggest that, under these conditions, the simultaneous production of auditory and visual signals may momentarily increase a sender’s locatability when a conspecific receiver is detected. Key words: Agonistic interactions; Anura; Communication; Habitat selection; Visual signaling

ALTHOUGH anurans are well known to use context and the environmental conditions un- auditory signals as the primary mode of intra- der which it occurs. speciﬁc communication (Gerhardt, 1994; Several environmental conditions may have Rand, 1988; Wells, 1977), individuals of some favored the evolution of visual displays in species perform remarkable visual displays in anurans (Ho¨dl and Ame´zquita, 2001). Breed- variable social contexts (Davison, 1984; Had- ing in noisy environments, such as near fast dad and Giaretta, 1999; Harding, 1982; Lind- streams or waterfalls, may require that acous- quist and Hetherington, 1996; Richards and tic signals be emphasized by visual displays James, 1992). Reviews on the use of visual (Haddad and Giaretta, 1999; Ho¨dl et al., 1997; displays by anuran amphibians (Ho¨dl and Lindquist and Hetherington, 1996). In arbo- Ame´zquita, 2001), reveal that all species real hylids, calling from elevated perches in performing visual displays perform acoustic dense vegetation may reduce an emitter’s displays as well, which makes it difﬁcult to locatability (Passmore et al., 1984) or attrac- separate the functional role of each mode of tiveness (Penna and Solı´s, 1998) and, thus, communication. Moreover, most reports on favor the use of complementary visual displays. visual displays in anurans remain anecdotal, The consequences of habitat use for acoustic and controlled experiments have been per- communication in a single anuran species have formed only recently in an attempt to elucidate been discussed to some extent (Etges, 1987; their communicative role (Lindquist and Wells and Schwartz, 1982). Visual signals, Hetherington, 1996). Visual signaling can be however, differ from auditory signals in both hypothesized as either an alternative or com- propagation distance and sender’s locatability plementary communication mode in anurans, (Bradbury and Vehrencamp, 1998). Thus, the prevalence of which depends on the social species that perform both acoustic and visual displays may differ in the ecological correlates of communication. An understanding of the evolution of visual displays in anurans requires 3 CORRESPONDENCE: e-mail, [email protected] accurate descriptions of the behaviors and

420 December 2004] HERPETOLOGICA 421 the social context in which these acts are males, as well as amplectant pairs, of H. performed. parviceps were found in the vegetation above The Amazonian tree frog Hyla parviceps is or beside the ponds. Eggs are laid on the water considered an opportunistic breeder because surface, and larvae probably complete their its calling activity, mainly nocturnal, seems to development in a short time interval under tem- be associated with occasional heavy rains poral restrictions that are imposed by pond (Crump, 1974; Weygoldt, 1986). We inciden- flooding. We conducted our study with frogs tally observed males of this species extending displaying from two ponds that measured 18 3 both arms and legs during one breeding night, 630.3 m (length3width3depth) and 12353 when the density of conspecific and hetero- 0.2 m. Both ponds were completely sur- specific calling males was very high. The prob- rounded by forest. Other anuran species calling ability of auditory interference suggested that at the site during this study included Allo- H. parviceps might have aggressive or court- phryne ruthveni, Osteocephalus taurinus, Sci- ship visual signals redundant with acoustic nax sp., Hyla granosa,andLeptodactylus signals. The observation that males call mainly knudseni. at night and from dense vegetation suggested On 37 consecutive days at the onset of the that visual signals might be correlated with rainy season, we performed daily censuses environmental conditions that favor signal of the number of calling males at the study propagation. Therefore, our aims in this study ponds. During this time period, water levels in are (1) to describe the visual displays of H. the ponds rose from ,2 cm to the level at parviceps as well as some ecological conditions which they became completely flooded by the under which they are performed, (2) to per- Surumoni river. We visited ponds between form intrusion experiments to obtain infor- 2000 h and 0100 h, walking slowly to spot all mation about the social context associated with calling males. When no calls were heard, visual signaling, and (3) to test whether males we waited at least 1 h at each pond before differentially use microhabitats for signaling declaring no calling activity. To test for activity. association between rainfall and calling activity, we used data on daily rainfall above the forest canopy from a weather station at less MATERIALS AND METHODS than 200 m from the furthest pond (Szarzyn- Study Site, Study Species, and ski, J; Surumoni-Project: Climate Monitoring, Breeding Activity 1997; Forest-Atmosphere Interaction Re- From 8 April–5 May of 1997, we studied search; Department of Geography, University a population of H. parviceps occurring at about of Mannheim). 150 m elevation at the Surumoni River (Venezuela) within the Orinoco drainage (38 Behavioral Observations and 109 N, 658 409 W). The rainy season there Intrusion Experiments extends from April–November, with a rainfall We observed 17 male-male interactions to peak during the months of May–July (about 400 describe visual signaling behavior and the asso- mm/mo). Annual precipitation is near 3000 mm ciated social context. Because most of the but year-to-year fluctuations of about 500 mm spontaneous visual signals occurred during the are common. Mean annual temperature is few hours when the density of calling individ- 25.5–26.5 C, and average diurnal temperature uals was highest, only 4 observations were range (5–10 C) exceeds among-years variation made of spontaneous interactions and 13 ob- (,4 C). The vegetation at the study site consists servations were of intrusion experiments. The primarily of a relatively old, secondary growth procedure consisted of displacing a calling forest with a canopy at about 30 m. male from its perch to a new perch located at At the study site, H. parviceps was found at least 50 cm from a calling male. The displaced streamside ponds that were formed during male was never one of the closest neighbors of water-level rise of Surumoni river at the begin- the resident (i.e., calling) male. We then ning of the rainy season. Ponds formed in this waited until one of the males either started way existed for only a few weeks before to call or made visual contact. Afterwards, one becoming fully connected to the river. Calling of us dictated sequentially all observed behav- 422 HERPETOLOGICA [Vol. 60, No. 4 ioral patterns into a tape recorder (Fagen and Young, 1978; Lehner, 1979). We also noted inter-individual distances (initially expressed in body-length units) at which behaviors were performed. An interaction was considered ter- minated when one of the individuals jumped away from the other so that visual contact was interrupted. In the course of inter-individual interactions, we observed two kinds of behaviors that can be classified as visual displays. We name them foot flagging and arm waving, following Ho¨dl and Ame´zquita (2001). During a foot-flagging display, a male raised one or both hind legs by extending it/them into an arc above the sub- FIG. 1.—Foot-flagging male of Hyla parviceps (Hylidae) strate level. The leg was then returned to the during call interval. Photograph taken by W. Ho¨dl at body side. At maximum extension, toes were Surumoni river near La Esmeralda, Amazonas, Venezuela. outstretched, spread, and sometimes vibrated (Fig. 1). At maximum extension, hind legs re- The perch properties measured were chosen vealed contrasting orange spots, visible only from the literature (Arak and Eiriksson, 1992; from behind the frog. Hind legs were either si- Etges, 1987) according to the potential value multaneously or alternatively extended. Foot for increasing the propagation of the signals flagging was by far the most frequently and for reducing locatability of senders to observed display during both intrusion experi- potential predators. Measured properties in- ments and occasional observations. In H. parvi- cluded perch height, height of calling site ceps, arm waving consisted of lifting an arm and above water level; perch size, leaf area (esti- waving it up and down in an arc above the head. mated as an ellipse based on the length of the A maximum of five waving movements were leaf’s orthogonal axes) or branch thickness performed consecutively without contacting (horizontal diameter of trunk at the place the substrate. The movements were not per- where the frog was located); vegetation den- formed in any recognizable temporal pattern. sity, measured as the number of leaves that Other behaviors observed during agonistic intersect a vertical cylinder (5 cm width 3 70 interactions include approaching, jumping cm height) centered at the frog’s location; away, turning, and uttering advertisement upper cover, as the approximate distance from calls. Approaching and jumping away are the frog to the top of the bush or tree where it defined according to the position of the in- was perched; and distance to the pond edge, teracting individual, i.e., approaching means expressed as positive if perches were directly walking so that the inter-individual distance is above water and as negative if they were reduced and jumping away means jumping outside the pond. All perch variables were (rarely walking) so that the interacting in- measured the following day to avoid disturbing dividual is left behind. Turning describes the animals excessively. When water level rose a group of behaviors in which the observed throughout the night, perch height and dis- individual reorients the body without displac- tance to pond edge were estimated, based on ing. Turning is characterized by sequential marks left during the previous night. lifting of every foot. To estimate perch availability, we measured the same properties on all potential perches Perch Use and Perch Availability (leaves as well as branches) intersecting vertical To sample the characteristics of perches planes of two transect lines per pond. The used by displaying frogs, the exact place was azimuth direction of the first transect plane at marked where each calling male was located each pond was randomly chosen; the second during the census. In most cases, males that plane was orthogonal to it (in order to reduce had been momentarily displaced resumed the potential effect of environmental gra- calling within a few minutes at a nearby perch. dients). Transect planes extended up to 2 m December 2004] HERPETOLOGICA 423

To test whether visual displays were signiﬁ- cantly preceded by any other behavior, we performed binomial tests between observed and expected behavioral transitions (Baker and Gillingham, 1983; Bels and Crama, 1994). To test whether perches are selected according to the properties we measured, we compared each property between used and available perches with a Kolmogorov-Smirnov test. Since the null hypothesis is that no selection of perches occurs, we used a Bonfer- roni procedure to adjust signiﬁcance levels for the number of variables tested (Scheiner, 1993).

RESULTS Calling and breeding activities are opportu-

FIG. 2.—Observed (open circles) occurrence of calling nistic in H. parviceps. Most breeding activity activity by males of Hyla parviceps in a given night as occurred between 0–2 d of a heavy rainfall. We a function of daily rainfall. Data were collected during 37 used daily rainfall and daily temperature consecutive days at the beginning of the rainy season at (minimum, average, maximum) as predictor Surumoni river near La Esmeralda, Amazonas, Venezuela. Filled circles denote the corresponding expected proba- variables of presence (1) or absence (0) of bilities according to a logistic regression model. nightly calling activity in a logistic regression model. Only daily rainfall was a significant predictor of calling activity (Log likelihood if term outside the pond edge, which represents the removed 5 À19.13, P 5 0.001, n 5 31 d; P . maximum distance at which a calling frog was 0.354 for other variables), and calling activity detected. most probably occurred when rainfall exceeded 30 mm/d (Fig. 2). Statistical analyses In the course of 13 male–male behavioral interactions, we observed 309 behaviors per- To compare the prevalence of behaviors, formed by 27 different males. Sixty-seven of the inter-individual distance at which they these acts (21.7%) were foot-flagging displays, were performed, and their frequency in re- and 18 (5.8%) were arm-waving displays. Foot lation to the status of the individual at the flagging was performed in 9 and arm waving in beginning (resident versus intruder) and at the 8 of 13 male-male interactions. Within a single end (winner versus loser) of the interaction, we interaction, foot-flagging displays were as com- used the experimentally induced behavioral mon as acoustic signals (Fig. 3), whereas arm- interactions as the statistical units of analysis waving displays were less common than (i.e., we calculated one value of each variable acoustic signals. for each behavioral interaction). Nonparamet- ric analyses were used because of nonnormal distribution of data. When Are Visual Displays Performed? To analyze behavioral transitions within the To know whether visual displays are pref- same subset of data, behavioral sequences erentially performed when males approach were displayed in the form of a first-order each other beyond a threshold distance, we contingency table. Rows represent preceding compared the inter-individual distance at behaviors and columns represent succeeding which behaviors were performed. For each behaviors that were performed by another single interaction, we calculated the minimum, individual (Fagen and Young, 1978). Given the median, and maximum distance at which each prevalence of low frequency values within the category of behavior was performed. Foot- cells, a randomization test was used to evaluate flagging distance (average minimum À average the independence between rows and columns. maximum; 8–21 cm) was slightly shorter than 424 HERPETOLOGICA [Vol. 60, No. 4

FIG. 4.—Minimum (left extreme), median (ﬁlled circle), and maximum (right extreme) distance between opponents at which visual displays (arm waving and foot ﬂagging) and other behaviors are performed in the course of agonistic interactions between males of Hyla parviceps (n 5 13 behavioral interactions).

FIG. 3.—Number of occurrences of visual displays (arm waving and foot flagging) compared to other behaviors performed by males of Hyla parviceps (Hylidae) in the havior was associated with the preceding act course of agonistic interactions. Bars indicate median performed by another individual (Monte Carlo values, upper and lower end of the boxes denote upper and 3 lower quartiles; open circles represent outliers and points Test on a 7 7 contingency table: number of represent extremes from each distribution (n 5 13 trials 5 100,000, P 5 0.0013 6 0.0001, n 5 behavioral interactions). 161 transitions). To know the potential role of any behavior in eliciting a visual display, we performed binomial tests between those be- calling distance (15–26 cm). Arm waving was havioral transitions that presented the largest performed at shorter distances (11–13 cm) differences between observed and expected than calling (Fig. 4). frequencies according to the dyadic matrix Resident males performed more arm-wav- (Baker and Gillingham, 1983; Bels and Crama, ing displays (Fig. 5a; Wilcoxon signed ranks 1994). We corrected the significance levels for test; Z 5 À2.23, P 5 0.026; n 5 13 the tests performed using a sequential Bon- interactions) and tended to produce more calls ferroni adjustment (Scheiner, 1993). Foot- (Z 5 À1.75, P 5 0.081; n 5 13 interactions) flagging displays were significantly preceded than intruders. There was no difference in the by foot flagging of the interacting individual number of arm-waving displays between males (Binomial randomization test; one-tailed P 5 that remained at the calling perches at the end 0.0001, critical P-value 5 0.0500) and turning of the interactions (winning males) and fleeing movements were significantly preceded by (losing) males (Fig. 5a; Wilcoxon signed ranks turning movements of the interacting individ- test; Z 5 À0.21, P 5 0.832; n 5 13 ual (Binomial randomization test; one-tailed interactions). Likewise, the number of foot P 5 0.0046, critical P-value 5 0.0250). flagging displays did not differ between Otherwise, calling tended to follow approach- resident and intruder (Fig. 5a; Wilcoxon ing (Binomial randomization test; one-tailed signed ranks test; Z 5 À0.85, P 5 0.397; n 5 test P 5 0.0302, critical P-value 5 0.0125); and 13 interactions), and between winner and loser approaching tended to follow moving away (Fig. 5a; Wilcoxon signed ranks test; Z 5 (Binomial randomization test; one-tailed test À1.19, P 5 0.236; n 5 13 interactions) males. P 5 0.0201, critical P-value 5 0.0063). Arm The first-order sequential analysis on a dy- waving was not significantly preceded by any adic matrix (Table 1) revealed that the behavior (one-tailed test P . 0.1769 in all probability of one individual performing a be- cases). December 2004] HERPETOLOGICA 425

Where Are Visual Displays Performed? Male H. parviceps differentially used perches in relation to vegetation density and cover height (Fig. 6). More males were found at perches that were surrounded by dense vegetation (Kolmogorov-Smirnov test; Z 5 3.30, P , 0.001) and that were part of high trees (Z 5 2.75, P , 0.001). Males, however, did not differentially use perches in relation to their height (Z 5 1.15, P 5 0.141), their distance to pond edge (Z 5 0.73, P 5 0.670), their area (for leaf perches; Z 5 1.31, P 5 0.066), or their thickness (for branch perches; Z 5 1.00, P 5 0.273).

DISCUSSION In the course of male-male agonistic interactions in H. parviceps, visual signals are at least as frequently used as acoustic signals. Both types of signals were observed in most interactions and were produced at similar rates during a single interaction. The extensive use of visual signals suggests that they are functional components of the communication system and poses interesting questions about their communicative role and the evolutionary scenario under which they evolved. Below we discuss our results from two perspectives: (1) the probable communicative role of the visual signals and (2) the possible ecological correlates of the visual signaling in H. parviceps.

The Communicative Role of Visual Signals Social interactions have favored the evolution of 2–3 across-species categories of signals in anurans (Bogert, 1960; Duellman and Trueb, 1986; Kluge, 1981; Rand, 1988): advertisement calls, aggressive/territorial calls, and, in some species, courtship calls. Spontaneous (i.e., in FIG. 5.—Number of occurrences of visual displays (arm the absence of other individuals) performance waving and foot ﬂagging) and other behaviors performed of visual signals has been reported for some by males of Hyla parviceps in the course of agonistic anuran species that evolved visual communica- interactions. Occurrences are separated according to the tion (Ho¨dl et al., 1997; Pavan et al., 2001), status of the individual at the beginning (A; white: resident, oblique lines: intruder) and at the end (B; white: winner, suggesting a communicative role comparable to oblique lines: loser) of each trial. Bars indicate median the role of advertisement calls: to indicate values; upper and lower end of the boxes denote upper and a male’s reproductive disposition to potential lower quartiles; open circles represent outliers and points receivers of either sex (Grafe, 1995; Harrison represent extreme values from each distribution. See text for details of the statistical analyses (n 5 13 behavioral and Littlejohn, 1985; Ryan and Rand, 1998; interactions). Schwartz and Wells, 1985). We believe, however, that visual signaling in H. parviceps does not serve advertisement purposes, because we 426 HERPETOLOGICA [Vol. 60, No. 4

TABLE 1.—Dyadic matrix summing up behavioral transitions during male-male agonistic interactions in the Amazonian tree frog Hyla parviceps. Asterisks denote behavioral transitions that occurred at frequencies higher than expected according to binomial tests. See text for details of analyses.

Successive behavioral unit

Approach Arm waving Assault Call Foot ﬂagging Move away Turn Total Approach Count 5.0 1.0 1.0 9.0 2.0 3.0 4.0 25.0 Expected count 3.6 1.1 0.9 4.7 4.8 4.0 5.9 25.0 Arm waving Count 1.0 0.0 0.0 0.0 0.0 1.0 1.0 3.0 Expected count 0.4 0.1 0.1 0.6 0.6 0.5 0.7 3.0 Assault Count 0.0 0.0 0.0 3.0 3.0 4.0 0.0 10.0 Expected count 1.4 0.4 0.4 1.9 1.9 1.6 2.4 10.0 Call Count 7.0 0.0 3.0 7.0 8.0 4.0 9.0 38.0 Expected count 5.4 1.7 1.4 7.1 7.3 6.1 9.0 38.0 Foot ﬂagging Count 0.0 1.0 1.0 5.0 **12.0** 3.0 3.0 25.0 Expected count 3.1 1.1 0.9 4.7 4.8 4.0 5.9 25.0 Move away Count 7.0 2.0 1.0 1.0 3.0 3.0 5.0 22.0 Expected count 3.1 1.0 0.8 4.1 4.2 3.6 5.2 22.0 Turn Count 3.0 3.0 0.0 5.0 3.0 8.0 **16.0** 38.0 Expected count 5.4 1.7 1.4 7.1 7.3 6.1 9.0 38.0 Total Count 23.0 7.0 6.0 33.0 31.0 26.0 38.0 161.0 Expected count 23.0 7.0 6.0 33.0 31.0 26.0 38.0 161.0

never observed visual displays performed by Most visual displays occurred at inter- individuals that were not approached by individual distances below 30 cm, which may a second male. There is still a good possibility be partly attributed to an experimental artifact, that visual displays play a role as courtship i.e., experimental observations were initiated signals that allow, for example, sex recognition by placing a male within 50 cm of a focal male. between males and females (Rand, 1988; Wells, However, during both registered and non- 1977; Zimmermann and Zimmermann, 1988). registered spontaneous interactions that in- In addition to the male-male interactions volved visual displays, we always estimated described in this paper, we observed two inter-individual distances shorter than 50 cm. male-female encounters that involved 21 In other anuran species (Grafe, 1995; behaviors, six of them consisting of arm-waving Schwartz and Wells, 1985; Wells and displays that were performed by a single male in Schwartz, 1984), focal males produced more, one of the interactions. This interaction did not more complex, or longer aggressive calls when lead to amplexus and oviposition. experimental stimuli simulated one individual From our data, the functional role of visual excessively approaching the calling male. In signals in H. parviceps can be compared to the this study, resident males tended to perform role of aggressive calls. Because males in more arm waving (significant differences) and almost all intrusion experiments performed to call more (nonsignificant differences) than some kind of visual displays, we interpret arm intruders (Fig. 5). In our opinion, the sum of waving and foot flagging as behaviors that our results strongly suggests that visual signals signal aggressive motivational states. Further- play a role in the evolution of agonistic more, foot flagging significantly elicited foot interactions. flagging by interacting males. Advertisement calls were also produced after the intrusion of a second male, but we did not find any evidence Ecological Correlates of Visual Signaling of a distinctive aggressive call in H. parviceps. In another study, we have explored several Instead, most males responded to intruders by hypotheses about ecological correlates for the combining advertisement calls and visual dis- evolution of visual communication: diurnality, plays, suggesting that visual signals may func- aposematism, signaling from acoustically com- tion as aggressive calls (mediating spacing) in plex environments, and signaling from noisy other species. environments (Ho¨dl and Ame´zquita, 2001). December 2004] HERPETOLOGICA 427

Calling males were disproportionally found at perches with high vegetation density. From the acoustic point of view, this result is unexpected since sound propagation may be diminished under these conditions (Ellinger and Ho¨dl, 2003; Penna and Solı´s, 1998; Richards and Wiley, 1980). One can speculate that perches within dense vegetation reduce locatability of senders to aerial predators such as bats. Calling male Physalaemus pustulosus (Ryan, 1985; Tuttle and Ryan, 1981) and Smilisca sila (Da Silva Nunes, 1988) change their behavior in the presence of bats. Indeed, during the course of this study, we observed bats preying upon frogs such as Osteocephalus taurinus that were calling from elevated perches. In spite of the potential benefits as antipredator strategy, calling from relatively hidden perches reduces the locatability of males to potential conspecific receivers, which could in turn reduce mating opportunities or increase the costs (time, energy, predation risk) of repelling other males. Under this scenario, the simultaneous production of auditory and visual signals may momentarily increase a sender’s locatability when a conspecific receiver is detected. Moreover, calling activity of males of H. parviceps is strongly FIG. 6.—Features of perches used by males of Hyla associated with heavy rains (this study; Crump, parviceps to call and perform visual displays (oblique lines) 1974; Weygoldt, 1986), when the cacophony as compared with features of available (white) perches (see produced by other breeding species may text for sampling procedure). Asterisks denote perch features in which used perches differed from available negatively affect acoustic communication perches at P , 0.008 (after Bonferroni’s correction). Bars (Narins and Zelick, 1988; Schwartz and Wells, indicate median values, upper and lower end of the boxes 1983). Visual signaling may thus favor species denote upper and lower quartiles, and open circles recognition in species breeding within large represent outliers from each distribution. assemblages, when acoustic and visual environments become too complex. These hypoth- The repertoire of visual signals is relatively low eses deserve further testing by comparing, for in H. parviceps, which agrees with previous example, phylogenetically close species that predictions on the relative importance of vary in signal stereotipicity, signal repertoire, diurnality in the evolution of anuran visual and microhabitat used for displaying. communication. Whereas the frog species Acknowledgments.—This research was funded by the exhibiting the largest repertoires of visual Austrian Science Foundation (FWF) grant to W. Ho¨dl (P displays are diurnal, H. parviceps is primarily 11565-Bio). We thank I. Strausz for invaluable field assis- nocturnal and only occasionally extends its tance and personal support; B. Rojas, V. Flechas, and L. breeding activity to the first hours of the Castellanos for help in data organization; and J. Szarzynski and N. Ellinger for providing data on the local weather. daytime. Furthermore, the coloration pattern of H. parviceps in the resting position does not seem to contrast against natural backgrounds. LITERATURE CITED We, therefore, discuss below the possible ARAK, A., AND T. EIRIKSSON. 1992. Choice of singing sites importance of visual signaling for communica- by male bushcrickets (Tettigonia viridissima) in relation tion in environments where the locatability of to signal propagation. Behavioral Ecology and Sociobi- sender is reduced. ology 30:365–372. 428 HERPETOLOGICA [Vol. 60, No. 4

BAKER, R. E., AND J. C. GILLINGHAM. 1983. An analysis of gladiator frog. Miscellaneous Publications of the Mu- courtship behavior in Blanding’s turtle, Emydoidea seum of Zoology, University of Michigan 160:1–170. blandingi. Herpetologica 39:166–173. LEHNER, P. N. 1979. Handbook of Ethological Methods. BELS, V. L., AND Y. J. M. CRAMA. 1994. Quantitative Garland STPM Press, New York, New York, U.S.A. analysis of the courtship and mating behavior in the LINDQUIST, E. D., AND T. E. HETHERINGTON. 1996. Field loggerhead musk turtle Sternotherus minor (Reptilia: studies on visual and acoustic signaling in the earless Kinosternidae) with comments on courtship behavior in Panamanian golden frog, Atelopus zeteki. Journal of turtles. Copeia 1994:676–684. Herpetology 30:347–374. BOGERT, C. M. 1960. The influence of sound on the NARINS, P. M., AND R. ZELICK. 1988. The effects of noise on behavior of amphibians and reptiles. Pp. 137–320. In W. auditory processing and behavior in amphibians. Pp. E. Lanyon and W. N. Tavolga (Eds.), Animal Sounds 511–536. In B. Fritzsch, M. J. Ryan, W. Wilczynski, T. and Communication. American Institute of Biological E. Hetherington, and W. Walkowiak (Eds.), The Science Publication No. 7, Washington, D.C., U.S.A. Evolution of the Amphibian Auditory System. John BRADBURY, J. W., AND S. L. VEHRENCAMP. 1998. Principles Wiley and Sons, New York, New York, U.S.A. of Animal Communication. Sinauer Associates, Sunder- PASSMORE, N. I., R. R. CAPRANICA,S.R.TELFORD, AND P. J. land, Massachusetts, U.S.A. BISHOP. 1984. Phonotaxis in the painted reed frog CRUMP, M. L. 1974. Reproductive strategies in a tropical (Hyperolius marmoratus): the localization of elevated anuran community. The University of Kansas Museum sound sources. Journal of Comparative Physiology A of Natural History Miscellaneous Publication 61:1–65. 154:189–197. DA SILVA NUNES, V. 1988. Vocalizations of treefrogs PAVAN, D., P. NARVAES, AND M. T. RODRIGUES. 2001. A new (Smilisca sila) in response to bat predation. Herpeto- species of leptodactylid frog from the Atlantic forest of logica 44:8–10. southeastern Brazil with notes on the status and on the DAVISON, G. W. H. 1984. Foot-flagging display in Bornean speciation of the Hylodes species groups. Papeís Avulsos frogs. The Sarawak Museum Journal 33:177–178. de Zoologia 41:405–423. DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of PENNA, M., AND R. SOLI´S. 1998. Frog call intensities and Amphibians. McGraw-Hill, New York, New York, U.S.A. sound propagation in the South American temperate ELLINGER, N., AND W. HO¨ DL. 2003. Habitat acoustics of forest region. Behavioral Ecology and Sociobiology a neotropical lowland forest. Bioacoustics 13:297–321. 42:371–381. ETGES, W. J. 1987. Call site choice in male anurans. Copeia RAND, A. S. 1988. An overview of anuran acoustic com- 1987:910–923. munication. Pp. 415–431. In B. Fritzsch, M. J. Ryan, W. FAGEN, R. M., AND D. Y. YOUNG. 1978. Temporal patterns Wilczynski, T. E. Hetherington, and W. Walkowiak of behaviors: durations, intervals, latencies, and se- (Eds.), The Evolution of the Amphibian Auditory Sys- quences. Pp. 79–114. In P. W. Colgan (Ed.), Quantita- tem. John Wiley and Sons, New York, New York, U.S.A. tive Ethology. John Wiley and Sons, New York, New RICHARDS, S. J., AND C. JAMES. 1992. Foot-flagging displays York, U.S.A. of some Australian frogs. Memoirs of the Queensland GERHARDT, H. C. 1994. The evolution of vocalization in Museum 32:302. frogs and toads. Annual Review of Ecology and RICHARDS, D. G., AND R. H. WILEY. 1980. Reverberations Systematics 25:293–324. and amplitude fluctuations in the propagation of sound GRAFE, T. U. 1995. Graded aggressive calls in the African in a forest: implications for animal communication. painted reed frog Hyperolius marmoratus (Hyper- American Naturalist 115:381–399. oliidae). Ethology 101:67–81. RYAN, M. J. 1985. The Tu´ ngara Frog. A Study in Sexual HADDAD, C. F. B., AND A. GIARETTA. 1999. Visual and Selection and Communication. University of Chicago acoustic communication in the Brazilian torrent frog, Press, Chicago, Illinois U.S.A. Hylodes asper (Anura: Leptodactylidae). Herpetologica RYAN, M. J., AND A. S. RAND. 1998. Evoked response in 55:324–333. male tu´ ngara frogs: pre-existing biases in male re- HARDING, K. A. 1982. Courtship display in a Bornean frog. sponses? Animal Behaviour 56:1509–1516. Proceedings of the Biological Society of Washington SCHEINER, S. M. 1993. Introduction: theories, hypotheses, 95:621–624. and statistics. Pp. 1–13. In S. M. Scheiner and J. HARRISON, P. A., AND M. J. LITTLEJOHN. 1985. Diphasy in Gurevitch (Eds.), Design and Analysis of Ecological the advertisement calls of Geocrinia laevis (Anura: Experiments. Chapman and Hall, New York, New York, Leptodactylidae): vocal responses of males during field U.S.A. playback experiments. Behavioral Ecology and Sociobi- SCHWARTZ, J. J., AND K. D. WELLS. 1983. The influence of ology 18:67–73. background noise on the behavior of a neotropical HO¨ DL, W., AND A. AME´ ZQUITA. 2001. Visual signaling in treefrog, Hyla ebraccata. Herpetologica 39:121–129. anuran amphibians. Pp. 121–141. In M. J. Ryan (Ed.), SCHWARTZ, J. J., AND K. D. WELLS. 1985. Intra-and Anuran Communication. Smithsonian Institution Press, interspecific vocal behavior of the neotropical treefrog Washington, DC, U.S.A. Hyla microcephala. Copeia 1985:27–38. HO¨ DL, W., M. T. RODRIGUES,G.M.ACCACIO,P.H.LARA, TUTTLE, M. D., AND M. J. RYAN. 1981. Bat predation and D. PAVAN,L.SCHIESARI, AND G. SKUK. 1997. Foot- the evolution of frog vocalizations in the neotropics. flagging display in the Brazilian stream-breeding frog Science 214:677–678. Hylodes asper (Leptodactylidae). Scientific film, Ctf WELLS, K. D. 1977. The courtship of frogs. Pp. 233–262. In 2703 O¨ WF, Vienna, Austria. D. H. Taylor and S. I. Guttman (Eds.), The Re- KLUGE, A. G. 1981. The life history, social organization, and productive Biology of Amphibians. Plenum Press, New parental behavior of Hyla rosenbergi, a nest-building York, New York, U.S.A. December 2004] HERPETOLOGICA 429

WELLS, K. D., AND J. J. SCHWARTZ. 1982. The effect of tematik, O¨ kologie und Geographie der Tiere 113:429– vegetation on the propagation of calls in the neotropical 454. frog Centrolenella ﬂeischmanni. Herpetologica 38: ZIMMERMANN, H., AND E. ZIMMERMANN. 1988. Etho- 449–455. Taxonomie und zoogeographische Artengruppenbil- WELLS, K. D., AND J. J. SCHWARTZ. 1984. Vocal com- dung bei Pfeilgiftfro¨schen (Anura: Dendrobatidae). munication in a neotropical treefrog, Hyla ebraccata: Salamandra 24:125–160. advertisement calls. Animal Behaviour 32:405–420. WEYGOLDT, P. 1986. Beobachtungen zur O¨ kologie und Biologie von Fro¨schen an einem neotropischen Accepted: 3 June 2004 Bergbach. Zoologische Jahrbu¨ cher, Abteilung fu¨ r Sys- Associate Editor: Edmond Brodie

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A REPATRIATION STUDY OF THE EASTERN MASSASAUGA (SISTRURUS CATENATUS CATENATUS) IN WISCONSIN

1,4 2 3 RICHARD KING ,CRAIG BERG , AND BOB HAY 1Necedah National Wildlife Refuge, Necedah, WI 54646, USA 2Milwaukee County Zoo, Milwaukee, WI 53226, USA 3Wisconsin Department of Natural Resources, Madison, WI 53703, USA

The use of relocations, repatriations, and translocations as amphibian and reptile conservation strategies has received much debate. In the case of endangered species, their use may outweigh the potential negative consequences. We performed an experimental repatriation of the eastern massasauga (Sistrurus catenatus catenatus), which has experienced range-wide population declines and extirpations. The experiment included measures to minimize negative conspeciﬁc effects to the donor populations as well as inter-species effects on the release and donor sites. Snakes released during late July had lower mortality rates, larger home ranges, and gained more mass than snakes released in early September. The July release cohort also successfully reproduced, while no breeding activity was observed with September release snakes. Results of this study suggest that repatriation may be a viable method of restoring eastern massasauga populations. We hope the methods and conservation measures used in this experiment will serve as a template for future repatriations. Key words: ecology; recovery; repatriation; Sistrurus; snakes

ALTHOUGH herpetologists undoubtedly have The purpose of this study was development been conducting transplants for decades, only of an ethical repatriation method for a species recently has the efficacy of transplanting or that clearly warrants it, the eastern massasauga repatriating individuals received rigorous de- (Sistrurus catenatus catenatus), in the hope bate (Burke, 1991; Dodd and Seigel, 1991; that it will serve as a template for future re- Grifith et al., 1989; Plummer and Mills, 2000; patriations. We chose a study design that mini- Reinert, 1991; Sealy, 1997). Ultimately, the mizes impacts on the founder and resident need for repatriation (Dodd and Seigel, 1991) snake populations. To achieve this, the study involves balancing two opposing issues: (1) the sites had to meet the following criteria: (1) sites need to recover a species, which often includes had to be void of eastern massasaugas, which expanding populations into formerly occupied by definition eliminated any impacts on habitats and (2) the obligation to do no harm resident massasaugas; (2) the sites had to have to the individuals being released as well as harbored eastern massasaugas in the past, resident animals. which demonstrates the sites’ ability to harbor massasaugas if habitat conditions are right; and (3) the cause of extirpation, in this case habitat degradation, must have been reversed prior to 4 CORRESPONDENCE: e-mail, [email protected] the study (Dodd and Seigel, 1991).