Behavioral Ecology Advance Access originally published online on September 29, 2004
Behavioral Ecology 2005 16(1):301-308; doi:10.1093/beheco/arh165
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Female preference for fast-rate, high-pitched calls in Hermann's tortoises Testudo hermanni
Laboratorio di Eco-Etologia, Dipartimento di Biologia Animale, Università di Pavia, P.zza Botta 9, 27100 Pavia, Italy
Address correspondence to P. Galeotti. E-mail: galeozot{at}unipv.it.
Received 23 December 2003; revised 23 July 2004; accepted 17 August 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The courtship and mounting behavior of promiscuous tortoises is based on a multiple signaling system that includes visual, olfactory, tactile, and acoustic signals. Vocalizations related to mounting seem to be particularly intriguing because tortoises vocalize mainly at this time. Vocalizations and courtship behavior might be costly for males, and if these costs increase differentially for different males, then the potential exists for vocalizations and displays to reveal male individual quality on which females could base their mate choice. In the present study, by using individuals breeding in seminatural enclosures, we experimentally investigated whether the mounting call of male Hermann's tortoises (Testudo hermanni) represents a relevant stimulus to both males and females. We also looked for potential preference toward different acoustic stimuli in order to determine which call features, if any, played a role in attracting potential partners or deterring rivals. Females were sensitive to call playback, whereas males apparently paid little attention to playback. In addition, females showed a significant preference toward high-pitched calls emitted at high rate. Also, females exhibited a strong tendency toward short-duration calls. Because call rate is related to hematocrit in Hermann's tortoise males, by responding to fast-rate calls females are also choosing high-quality partners as sires of their offspring. This is the first study in which an attractive function of tortoise vocalizations has been documented.
Key words: call features, calling rate, mate choice, playback experiments, tortoise, Testudo hermanni.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The "good-genes" models of sexual selection (Halliday, 1978
; Trivers, 1972; Zahavi, 1975, 1977) assume that female mate-choice is based on signals that reliably indicate male quality, for example, the relative ability to sire fit offspring, dominance (Borgia, 1979), or disease resistance (Hamilton and Zuk, 1982). In assessment contexts, the need for signal reliability justifies extra high investment that takes the form of extravagant secondary sexual characters (Grafen, 1990; Zahavi, 1991).
Song and other acoustic signals used during the breeding season are the male traits most often shown to be sexually selected (for a review, see Andersson, 1994). Evidence for sexual selection of acoustic signals comes from pattern of song use, effects on recipient of the signal, and correlation with the mating system (for a review, see Searcy and Yasukawa, 1996). As Darwin (1871) first suggested, song, similar to other male secondary sexual characters, may have probably evolved via intra- and intersexual selection and therefore has assumed the dual function of mate attraction/stimulation and repulsion of rivals competing for limited resources (Catchpole, 1982; Catchpole and Slater, 1995; Searcy and Andersson, 1986). There is a debate about the relative importance of the two components of sexual selection in shaping the structure of acoustic signals used in sociosexual contexts. Intrasexual selection appears to be more common and should promote signal structure adapted mainly for territorial defense; intersexual selection may be less common (or more difficult to detect) and should produce acoustic structure adapted primarily for the direct attraction of females (Catchpole, 1982). However, male-male competition and female mate choice do not necessarily impose antagonistic selective pressure on song because acquiring crucial resources through song is merely an initial and essential stage in attracting a female for breeding, and there is good evidence that most species retained considerable duality of function in a unique signal (Catchpole, 1982; Catchpole and Slater, 1995).
Elaborate acoustic signals during courtship occur in many animal taxa, the most studied of which are insects (orthopteran), anurans, and songbirds (Searcy and Nowicki, 2000). In all these groups, male vocalizations can have several different effects on females: attracting them from a distance, priming them into physiological condition for breeding, and stimulating them for copulation (see Kroodsma and Byers, 1992). Complex vocalizations with clear sexual function are also found in some mammals (see Clutton-Brock and Albon, 1979; Mitani 1985, 1988) and fishes (see Myrberg et al., 1986). In chelonian, courtship vocalizations occur in 35 species belonging to families Testudinidae, Tryonichidae, Emydidae, and Bataguridae (Galeotti et al., 2004), but little is known about their possible function in sexual selection processes (Sacchi et al., 2003). Moreover, it is not clear yet whether sexual selection does ever exist in this peculiar reptile group (Berry and Shine, 1980; Olsson and Madsen, 1998; Swingland and Stubbs, 1985; Willemsen and Hailey, 2003) and whether both components, intra- and intersexual selection, are at work simultaneously. To date, many investigators have emphasized the role of intermale combats in determining a hierarchy among males, with high-ranking individuals achieving more copulations and therefore high paternity (Kaufmann, 1992; Niblick et al., 1994; Weaver, 1970). In this scenario, females should only be the prize for the winner. However, in many species of Testudinidae, intermale aggressions (fighting) are limited to contests over thermoregulatory and foraging sites and never precede courtship and mounting of females (e.g. Geochelone elephantopus: Desola, 1930; Gopherus agassizi: Householder, 1950; Niblick et al., 1994; Gopherus polyphemus: Auffenberg, 1966; Gopherus berlandieri: Weaver, 1970; Testudo hermanni: Swingland and Stubbs, 1985; T. marginata: Sacchi et al., 2003). In addition, males are smaller than are females in most Testudinidae, particularly among European tortoises (Willemsen and Hailey, 2003). This sexual dimorphism is not owing to natural selection for fecundity (greater volume for eggs in females, Willemsen and Hailey, 2003), and it is not consistent with an intrasexual selection model, that should favor larger males with higher competitive abilities (Berry and Shine, 1980). On the other hand, females are not prone to indiscriminate mounting and copulations by males, but they often try to avoid sexual intercourses by running away rapidly; a male is therefore forced to pursue the female, while biting her legs and roaming her carapaces until she "accepts" to cooperate. This courtship behavior is energetically expensive and may represent a cue females use to assess partner endurance. Therefore, though not excluding the presence of intrasexual selection in tortoise mating system, it seems likely that females are the choosy sex.
Tortoises mate promiscuously, and their courtship behavior is based on a multiple signaling system that includes olfactory, visual, tactile, and acoustic signals. Of particular interest are the vocalizations associated with mounting, as this is the predominant, or for most species the only, behavior during which tortoises vocalize (Ernst and Barbour, 1989; Galeotti et al., 2004). Despite this, chelonian vocalizations have been studied only occasionally (Campbell and Evans, 1967, 1972; Mrosovsky, 1972; for a review, see Gans and Maderson, 1973), and investigators considered tortoise vocalizations as simple "noises" involuntarily produced by copulatory movements (see Mrosovsky, 1972; Weaver, 1970;). Many studies (Campbell and Evans, 1967; Gulick and Zwick, 1966; Patterson, 1966; Ridgway et al., 1969; Wever and Vernon, 1956) ascertained that a number of tortoise species have a considerable auditory sensitivity to sounds below 1000 Hz, and this no doubt enables the animal to perceive many acoustic signals both on land and in water. Moreover, in a recent study on the terrestrial Testudo marginata (Sacchi et al., 2003), we showed that three features of male mounting calls (call rate, frequency, and duration) strongly correlated with male body condition and his mounting success (number of mounts achieved and number of females mounted). If the cost imposed by acoustic signals increases differently for different males, then the potential exists for these behavioral traits to reveal the ability of male to withstand such costs. Therefore, vocalizations may convey information about male features which may influence, directly or indirectly, sound production, and courting intensity and, hence, male quality. Mounting calls of male tortoises might indeed affect mate choice, enabling females to assess the quality of potential partners.
The aim of the present study was to investigate whether acoustic signals exhibited by male Hermann's tortoises (Testudo hermanni) during courtship may have any effect on male and female behavior. The function of these unique vocalizations is mostly unknown. Recently, we found that different call features of male Hermann's tortoises (i.e., calling rate, frequency modulation, call duration) were significantly related to various aspects of male quality (relative mass and length size, and general health condition, Pellitteri Rosa, 2003; Sacchi, 2004), suggesting that calling is a costly condition-dependent display that enables males to succeed in sexual competition. By analogy with bird song, mounting calls might accomplish the dual function of addressing pre- and postcopulatory female mate choice (intersexual function) and deterring potential rivals from sexual interference (intrasexual function).
Assuming that vocalizations are directed to the mounted female, male tortoises might call during mounting and copulation (1) to induce female to cooperate, thus obtaining an effective copulation or multiple copulations and thereby increasing the male probability to sire a greater proportion of young in resulting clutches; or (2) to avoid their own sperms to be ejected or otherwise not used by females for egg fertilization. In both cases, females tortoises might select mate or stored sperm on the basis of reliable information on individual quality conveyed by calls, if these calls reliably reflects aspects of male heritable qualities, such as general health condition and ability in courtship, that are relevant to female inclusive fitness.
On the other hand, assuming that vocalizations may be directed to different receivers, male tortoises may vocalize during mounting and copulation as a simple mate-guarding strategy in order to prevent sexual interferences from other males, or also to recruit other females and to obtain subsequent additional copulations (Bradbury and Vehrencamp, 1998).
To investigate call functions in this species, we used an experimental approach based on discrimination tests, in which a pair of acoustic stimuli was presented simultaneously to either male or female Hermann's tortoises. Our general prediction was that mounting call was a relevant signal for both sexes if it accomplished the dual function of attracting females and deterring other males. Our specific predictions regarding effects of call features were that both sexes should be more responsive to high call rates and to short, high pitched, and highly frequency-modulated calls. These predictions come from the general finding that in many animals high-intensity signals are far more effective in both courtship and fighting contexts (see Catchpole and Slater, 1995; Gibson and Bradbury, 1985; Lopez and Narins, 1991; McComb, 1991; Møller et al., 1998), and from a companion study on 49 Hermann's tortoise breeding males that was performed during free interactions in seminatural enclosure (Pellitteri Rosa, 2003; Sacchi, 2004).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We performed this study during spring and summer 2002–2003, at the "CARAPAX" European Centre for Tortoise Conservation, located at Massa Marittima (Tuscany, central Italy), where 8000 individuals of several tortoise species reproduce in enclosures, in seminatural conditions, and at high density.
Study species
The Hermann's tortoise, one of the three Testudinidae species autochthonous to Europe, maintains nonexclusive home ranges and exhibits a promiscuous mating system with multiple copulations. As in other Testudinidae, the male pursues the female during courtship, bites at her legs, and occasionally rams her shell, while forcing the female from refuges (Hailey and Willemsen, 2000; Galeotti P, Sacchi R, personal observations). The apparent aim of all these behaviors is to stop and immobilize female in order to achieve a successful mount. Mounting may occur also while the female is moving, which hardly allows a successful copulation (only 0.36% actual matings on 1115 courtship attempts; Willemsen and Hailey, 2003). Courtship in T. hermanni is thus of the mounted pattern rather than premounted, as defined by Bels and Crama (1994), and females might assess male quality by this endurance race. Vocalizations occur mainly during the stationary mounting, in which the male makes repeated thrusts around the base of the female's tail by using the large spur on the tip of his tail (Hailey, 1990; Sacchi R, personal observations). Mounting males emit regular series of peepings, which sound like whimpers or wailings and are highly stereotyped within an individual. They are modulated in frequency and show a harmonic structure: up to five harmonics are evident from sonagrams (Figure 1). Call duration in our sample of recorded individuals averaged 144 ± SE 5.8 ms (range = 87–259 ms, N = 40), and the interval between calls 2.4 ± 0.1 s (range = 1.4–5.9 s). The mean fundamental frequency ranged from 418.6–883.3 Hz, averaging 602.1 ± 17.1 Hz. The natural rate of call delivering was 1.4 calls per 5 s, that is, about one call every each 3 s (N = 49).
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General design and playback procedure
Experiments were conducted from 10 May–25 June 2002 and from 3–14 May 2003, from 0800–1900 h in an outdoor square arena (80 x 80 cm) within a great enclosure (650 m2) in which Hermann's tortoises reproduced freely. A green-colored plastic fence, 20 cm high, bounded the experimental arena. Two small loudspeakers (Philips-speaker system) connected to a compact disc (CD) player (Sony Discman D-171) were centered on two opposite sides of the experimental arena, 25 cm from the ground (Figure 2).
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For each experiment (see below) we used 20 different males and 20 different females, for a total of 160 individuals, all coming from a captive Tuscanian population. Tested animals were all sexually mature, and experiments were conducted only while tortoises were courting in the great enclosure, on calm dry days and with ambient temperature ranging from 24°C–30°C.
Before the start of each trial, the individuals to be tested were placed in a smaller circular enclosure in the middle of the square arena for 2 min, in order to allow them to stabilize their behavior. They were then released in the arena and trial started. Each trial lasted 10 min, during which an individual, either male or female, was presented simultaneously with two different acoustic stimuli, depending on the experiment type (see below). Two observers recorded behavior at a distance of 1 m from focal tortoises. Potential preference for one of the two stimuli was determined by the number of tested individuals spending more time in the half arena facing the speaker that emitted a given stimulus. Each individual received 5 min of stimulation in sessions of 1 min each (20 calls per min), regularly alternated to 1 min of silence as control (i.e., Playback, Silence, PSPSPSPS). In this way, we could check if call playback had any effect on tortoises, by comparing the behaviors of tested individuals in the two periods (playback/silence). The time of stimulation was reliable because reaction times of individuals were generally short: on average 21.3 s ± 4.1 s for males versus 19.1 s ± 3.8 s for females. To avoid stimuli overlapping, the start of one stimulus was out of phase by 1.5 s relative to the other. The side of the arena from which a stimulus was emitted changed from trial to trial; for example, if in the former trial speaker A had emitted stimulus A, in the next trial speaker A emitted stimulus B, and vice versa.
The stimuli we presented were derived from high-quality recordings (maximum intensity and minimal background noise) obtained in previous years from Hermann's male tortoises of the same Tuscanian population, at the CARAPAX. For each stimulus, we prepared a track by using a mounting call of a different male and replicating it 20 times with regular 3-s intervals between calls (which corresponds closely to the natural call delivering in our tortoise population, see Study Species) by using the options provided by the COOL. Edit PRO software; to control for sound intensity, all tracks were normalized (80%). Tracks of the two stimuli presented to animals in each experiment were mastered on an audio CD in a stereophonic track, one stimulus on the right and the other on the left channel, respectively, in order to be broadcasted by the same audio-CD player at the same volume in all experiments. To avoid pseudoreplication, in each trial we used pairs of stimuli obtained from different males, so that for each experiment we used the calls of 40 different males. Experiments on males preceded experiments on females.
Experiment 1: long call versus short call
In this experiment we checked the effect of call duration on tested individuals, while controlling for call frequency and modulation. Stimuli differed significantly in their duration (Table 1): mean duration (±SE) of long calls was 248 ± 11 ms (range = 210–360 ms) and of short calls was 147 ± 4 ms (range = 120–190 ms); mean difference in duration between long and short calls was 100 ± 8 ms (range = 65–200 ms). Mean frequency was 607 ± 9 Hz (range = 550–643 Hz) and 612 ± 4 Hz (range = 580–660 Hz) for short and long calls, respectively.
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Experiment 2: high-pitched versus low-pitched call
We investigated the effect of call fundamental frequency on tested individuals, while controlling for call duration and frequency modulation. Mean frequency of high pitched calls was 751 ± 20 Hz (range = 565–939 Hz) and of low-pitched calls was 505 ± 18 Hz (range = 406–659 Hz); mean difference in frequency between high- and low-pitched calls was 246 ± 15 Hz (range = 143–348 Hz), a significant difference (Table 1). Mean durations were 202 ± 4 ms (range = 190–280 ms) and 196 ± 3 ms (range = 170–258 ms) for high- and low-pitched calls, respectively.
Experiment 3: highly modulated call versus smoothly modulated call
We studied the effect of the amplitude of frequency modulation (
F) by submitting both sexes to two differently modulated calls, while keeping their duration and frequency constant. Stimuli were significantly different in their frequency modulation (Table 1): mean F of highly modulated calls was 808 ± 32 Hz (range = 650–1190 Hz), that of smoothly modulated calls was 507 ± 24 Hz (range = 280–630 Hz). Mean difference between F of the two stimuli was 301 ± 20 Hz (range = 370–560 Hz). Duration and fundamental frequency were set constant for all calls to 144 ms and 602 Hz, respectively, which correspond to the mean duration and frequency of the calls in the present study population.
Experiment 4: fast call rate versus slow call rate
In this experiment we checked the effect of calling rate on tested individuals, while controlling for call frequency and duration. To each subject, we presented the same call of a male, while varying only its delivering rate: one call per 5 s and three calls per 5 s for slow and fast call rates, respectively. Mean call duration was 173 ± 12 ms (range = 92–292 ms), and mean frequency was 643 ± 31 Hz (range = 410–878 Hz).
Statistical analysis
To check whether tortoises paid attention to the acoustic stimulus, that is, were attracted by call playback, we compared the number of times the experimental individuals displayed the behavior "observe" (tortoise stops to move, extends neck and raise the head while looking at the speaker) during playback periods versus silence periods, in all four experiments performed, by using the Wilcoxon's test for matched-pairs. The "observe" display, widespread in Testudinidae, is used by both sexes in different contexts, including courtship, and denotes attentiveness toward objects, movements, noises, and sounds around the focal individual (Carpenter and Ferguson, 1977, Sacchi R, Galeotti P, personal observations). No other relevant behavior was observed during experiments, apart from walking and stopping.
To determine a potential preference toward a certain stimulus, we used simple chi-squared goodness-of-fit tests to compare the observed distribution of experimental tortoises near each stimulus in each experiment, based on time spent near each stimulus, with the expected distribution under the null hypothesis of no association between stimuli and individuals. We also performed one sample t test to check whether the difference in times spent by tested individuals in each half arena deviated significantly from zero.
All tests were two-tailed and were performed using the SPSS 10.0 statistical package. Unless otherwise stated, values reported are mean ± SE.
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RESULTS |
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Playback effect
In all the experiments but one, females observed significantly more often when calls were played back than during silence periods (duration: Z = 2.315, p = .021; frequency: Z = 2.14, p = .033; frequency modulation: Z = 1.51, p = .13; call rate: Z = 2.64, p = .008; N = 20 for each experiment, Wilcoxon test) (Figure 3a). Conversely, males did not display observe differently during playback and silence periods in all experiments, although in the call duration experiment they undoubtedly paid attention to playback (duration: Z = 1.81, p = .07; frequency: Z = 1.51, p = .13; frequency modulation: Z = 0.14, p = .88; call rate: Z = 0.37, p = .71; N = 20 for each experiment, Wilcoxon test) (Figure 3b). The condition of tested individuals did not affect their responsive behavior because no correlations were found between male size and response to the stimuli as measured by the number of displays observe exhibited by animals during playback or silence periods (all p values > .4, Spearman rank test).
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Experiment 1
More females spent their time in the half arena facing the loudspeaker broadcasting the short-duration call than those in the half arena facing the loudspeaker emitting the long-duration call, although the difference was not significant
(Figure 4a). On average, females stayed 351 s ± 22.3 s in the short-duration call arena versus 243 s ± 22.7 s in the long-duration call arena (t19 = 1.6, p = .12). Males were apparently indifferent to the stimuli 
and they spent 321 s ± 25.7 s in the short-duration call arena versus 278 s ± 25.8 s in the long-duration call arena (t19 = 0.87, p = .39).
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Experiment 2
Significantly more females preferred to stay in the half arena facing the loudspeaker broadcasting high-pitched calls than in the half arena facing low-pitched calls
(Figure 4b). Female stay in the high-pitched call arena averaged 368.2 s ± 18.5 s versus 216 s ± 16.3 s in the low-pitched call arena (t19 = 3.45, p = 0.003). Males did not show any tendency 
and they spent nearly the same time (306 s ± 22.9 s versus 289 s ± 22.6 s) in the two half arenas (t19 = 0.39, p = .70).
Experiment 3
Neither males nor females showed any preference toward highly modulated versus smoothly modulated calls (both p > .35) (Figure 4c). Females spent 283.7 s ± 22.1 s and 309.8 s ± 21.8 s in the highly and smoothly modulated call arenas, respectively (t19 = 0.59, p = .56); males, 320.4 s ± 13.1 s versus 277.2 s ± 13.6 s (t19 = 1.6, p = .12).
Experiment 4
Females were significantly attracted by the loudspeaker broadcasting fast-rate calls rather than the one broadcasting slow-rate calls 
(Figure 4d). On average, females spent 381.2 s ± 18.7 s in the fast-rate arena versus 211.3 s ± 17.6 s in the slow-rate arena (t19 = 3.4, p = .003). Males did not show any tendency 
and spent 312.4 s ± 13.1 s in the fast-rate arena versus 282.4 ± 12.8 s in the slow-rate arena (t19 = 1.2, p = .26).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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This experimental study showed for the first time in chelonians that female Hermann's tortoises pay attention to the quantity and quality of male mounting call, favoring fast-rate, high-pitched calls. On the other hand, males appear to detect conspecific calls, but they do not react to them in a consistent way, showing mixed responses to playback, with some individuals approaching and some retreating from the call of other males. Taken together, these findings weaken the hypothesis that male mounting calls may serve an intrasexual function (i.e., avoiding rival interferences during mounting) and rather suggest that they are mainly directed to females, accomplishing an intersexual function toward the mounted female and possibly toward other females nearby.
Mounting calls vary significantly among the European tortoise species (Galeotti et al., 2004); therefore, they might simply represent species-specific signals, enabling females to reject erroneous partners of sympatric species, especially because male tortoises are notoriously indiscriminate breeders, trying to copulate with any tortoise-like object (Ballasina, 1995). However, females may easily discriminate partner species by odors and courtship displays that differ greatly among European tortoises (Willemsen and Hailey, 2003). Therefore, mounting call may represent an additional cue able to convey further information about the quality of emitter to the receiver. Consistent with this hypothesis, females appeared to prefer high-pitched calls than low-pitched calls, thus exhibiting sensitivity to changes in call acoustic structure and the ability to discriminate between calls at different frequencies (and therefore among different individuals). This preference for high-pitched calls might be simply owing to a female auditory system biased toward high frequencies because of a genetic predisposition to respond to high-frequency sounds in female tortoises. Sensory system is shaped by natural selection for tasks unrelated to mate choice, thus introducing a bias (Ryan and Rand, 1990) that may be simply exploited by males emitting high-pitched calls in order to stimulate females. However, high-pitched calls are typical of small-sized males, because a negative relationship between call frequency and head size exists in this species (Pellitteri Rosa, 2003; Sacchi, 2004). In addition, the strong tendency toward short calls exhibited by female Hermann's tortoises, as also occurs in T. marginata and in T. graeca (Sacchi, 2004; Sacchi et al., 2003), further indicates a possible preference for small males, because call duration is directly related to male shell size (Pellitteri Rosa, 2003; Sacchi, 2004).
If this selection pressure in favor of small males exists on part of Hermann's tortoise females, we could expect a strong inverse sexual dimorphism in this species, and a lowered age of sexual maturity in males. This is just what occurs: males are significantly smaller than are females (441 ± 14.4 g versus 789 ± 23.1 g, personal observations on 134 males and 165 females; Willemsen and Hailey, 1999, 2003), and they attain sexual maturity at 8–10 years, whereas females at 12–18 years (Ballasina, 1995; Willemsen and Hailey, 1999). In fact, fighting is so rare (Willemsen and Ryan, 1999; Sacchi R, Galeotti P, personal observations) and density of natural populations so low in this tortoise species (less than three individuals per hectare in Greece; Swingland and Stubbs, 1985; one to five individuals per hectare in Tuscany; Ballasina D, personal communication), that male breeding success depends primarily on male ability to find dispersed females and to court them effectively, not on his size or aggressiveness. Small males became active earlier in the morning owing to their high area/volume ratio and are more mobile and energetically cheaper than are large males (Lebboroni and Chelazzi, 2000); thus, they may encounter more females and sustain courtship costs more easily than do large males, presumably achieving higher breeding success. Females choosing small males are therefore likely to obtain genes that may confer such qualities to their sons. The lower relative mass in male Hermann's tortoises could therefore be the result from the combination of female preference and the advantage of increased mobility (Bonnet et al., 2001).
Female attraction toward the fast call rates we found in Hermann's tortoises confirms the well-documented directional female preference for courtship signals produced at higher rates (see Ryan and Keddy-Hector, 1992), which suggests a generalized female choice for costly signals because of supposed links between metabolism and call rate. Indeed, we found a strong direct relationship between call rate and hematocrit value in male Hermann' tortoises (Pellitteri Rosa, 2003; Sacchi, 2004), which indicated that only males with high aerobic capacity were able to produce high call rates (because high hematocrit values are also related to high aerobic capacity; see Chappel et al., 1997). Aerobic respiration is the metabolic foundation of sustainable power production, and hence, aerobic capacity presumably influences Darwinian fitness through effects on locomotory performance and courtship endurance. Thus, females may actually assess general health condition and vigor of prospecting partners by using their call rates while mounting as honest, condition-dependent signals. Mating success is often correlated with the intensity of courtship displays in many animals (Catchpole and Slater, 1995; Gibson and Bradbury, 1985; Hoglund and Robertson, 1990; McComb, 1991; Møller et al., 1998; Passmore et al., 1992). Male Hermann's tortoises signaling at faster rate apparently win sexual competition; actually, stronger signalers obtained a higher mounting success in terms of total mounts effected, mount frequency per interaction, and number of females mounted during the breeding season (Pellitteri Rosa, 2003; Sacchi, 2004; Sacchi et al., 2003), which may undoubtedly confer them a fitness advantage over less active males. Females in turn, by choosing such stronger signalers, may benefit from having viable and competitive sons able to sustain intense and prolonged courtships.
How may the potential for female choice, shown by the present study, be applicable under natural ecological and demographic conditions? The mounting call of male tortoises may be heard from 30–40 m in grassland and scrubland habitats, thus enabling females to address their attention toward the sound source from a distance. Although female Hermann's tortoises rarely experience the chance for hearing and simultaneously comparing two or more males in nature, this may nevertheless occur when tortoises congregate at particular sites (e.g., under fruiting trees) and several males gather around single females (Moskovits, 1988). In any case, females may exert mate choice without comparing two or more males at a time, providing they posses an adaptive threshold of partner acceptance, based on courtship signals, below which mounting males are not allowed to achieve any actual coition. Therefore, females might simply assess whether the male's courtship performances, including vocalizations, are below or above this threshold, without the need to compare several partners at the same time or to remember call features of sequential partners.
We acknowledge that the two-way choice design of our experiments was unable to clearly separate preference for a stimulus from avoidance of the opposite stimulus. However, the stimuli we used were all natural calls recorded in the field, and their acoustic features fell in the natural range of variation for tortoise vocalizations. Therefore, it was unlikely that these stimuli were so disturbing as to repel individuals and to mask their preference. Moreover, females in the field did not avoid males with a slow call rate or with low frequency calls, but they cooperated effectively only with males with fast call rates or high frequency calls (Pellitteri Rosa, 2003; Sacchi, 2004), thus allowing copulation only to these individuals, which undoubtedly suggests a real preference by females for such strong signalers.
In conclusion, the present study showed that female Hermann's tortoises favor fast-rate, high-pitched calls, which are typical of good-condition and small-sized individuals. Indeed, mounting calls appears to be a key character in intersexual selection process of tortoises, enabling females to assess the endurance ability of potential partners and their mobility.
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ACKNOWLEDGEMENTS |
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We are very grateful to Dr. D. Rubolini and Dr. M. Elgar for providing helpful comments and suggestions on an earlier version of this manuscript, and to three anonymous referees for their valuable suggestions and criticisms. Thanks are also due to Dr. D. Ballasina, for his warm hospitality at the CARAPAX. The present study was financially supported by a MURST grant (COFIN 2000) to P.G., and was carried out in conformity with the Italian current laws on tortoise detention.
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