Receiver sex differences in visual response to dynamic motion signals in Sceloporus lizards

Visual signal properties often vary greatly between and within individuals in a variety of social contexts. While it is widely known that visual displays emitted by senders can exhibit great variation in efficacy and content, far less is understood whether and how receivers vary in the ability to respond to variability in signal properties, such as motion. Here, we tested for receiver sex differences in visual response latency to motion signals in Sceloporus undulatus lizards. We used a moving robotic lizard model as a visual stimulus to assay response latency in male and female lizards. We measured visual reaction times to slow and fast, up-and-down motions, characteristic of territorial and courtship male motion displays, respectively. We found sex differences in response latency to the two different displays. Specifically, male lizards were faster than females at responding to slow motion produced by the robotic lizard, while female lizards were faster than males at responding to fast motion. These results demonstrate that dynamic visual signals that vary temporally under different social contexts can differ in eliciting a visual response from each sex. Our study highlights that physical differences in dynamic and complex visual signals exhibited during different social contexts (i.e., territorial and courtship contexts) can closely match sex differences in visual responses.     

Does cadence of Iguana iguana displays facilitate individual recognition?

Iguanid lizards communicate threat, courtship and territorial advertisement through stereotyped headbob displays. It has been hypothesized that slight interindividual differences in these displays might enhance individual recognition and maintain dominance relationships within populations, but the precise display elements responsible have not been determined. The purpose of this study was to examine if experimentally induced differences in displays would decrease recognition of individual conspecifics. Specifically, social interactions between adult male green iguanas (Iguana iguana) were examined at normothermic and hypothermic body temperatures. Whereas the cadence (rate of muscle contraction) of stereotypic displays of individual lizards was slowed at hypothermic body temperature (Q ₁₀ 1.6), the amplitude (maximal muscle contraction) of hypothermic displays remained constant relative to normothermic displays. Normothermic lizards viewing a display from a hypothermic lizard responded to that display as if it were performed at a normothermic cadence. During paired encounters between lizards (one hypothermic, one normothermic), dominant/subordinate dyads within the group were unusually maintained regardless of which individual was hypothermic. The exception occurred when dominant individuals at the lowest experimental body temperatures retreated from subordinate individuals. The results suggest that individual lizards recognized their relative social status even when cadence of displays was radically altered, indicating that cadence alone probably does not function in individual recognition. Other morphological, display elements, or scent cues may provide information useful in individual recognition.Communicated by G.M. Klump     

Persistence of individually distinctive display patterns in fatigued side-blotched lizards ( Uta stansburiana)

Iguanian lizards perform conspicuous species-typical push-up displays, which are used in territory advertisement, threat, and courtship contexts. Subtle individually distinctive differences in push-up characteristics have been suggested to play a role in the recognition of social partners. However, if the structure of push-ups is responsive to changing physiological states then their capacity to promote recognition may be limited. The current study evaluated whether the push-ups performed while in an experimentally imposed state of fatigue by male side-blotched lizards (Uta stansburiana), retain the individually distinctive characteristics apparent in rested lizards. We found repeatable among-individual differences in the duration and the relative height of push-up components. Repeatability values did not change consistently between the rested and fatigued conditions, nor when both conditions were pooled, indicating that these push-up characteristics do not change with fatigue. Similarly, discriminant functions that were generated using push-ups from one state assigned push-ups performed in an alternate state to the correct individuals. Furthermore, when analyzed independently of individual identity, the values of display parameters examined in the current study did not change significantly between states, and discriminant function analysis could not reliably classify push-ups to the correct state. Taken together the results show that individually distinctive push-up characteristics are robust to effects of fatigue, consistent with their suggested role in social recognition. In the future, video playback experiments can test whether lizards utilize the signature-like characteristics of push-ups to discriminate among individuals.Communicated by T. Czeschlik     

Signal use by collared lizards, Crotaphytus collaris: the effects of familiarity and threat

Many lizard species use lateral compressions of the body during agonistic encounters. I investigated the signal value of the frequency at which these displays are presented and how that rate is affected by familiarity and threat. The response of resident collared lizards (Crotaphytus collaris) to tethered strangers, neighbors on the correct boundary, and neighbors displaced to the opposite boundary, was recorded by counting the number of lateral displays directed at the intruder and the number of subsequent acts of escalated aggression. There was no relationship between size asymmetry of the opponent and the rate of lateral display or aggression, nor was there a relationship between body size and the rate of lateral display or aggression. However, there was a high positive correlation between lateral display rate and aggression, suggesting that the rate of lateral displays is a conventional signal of motivation to attack. The highest rates of display and aggression were directed toward displaced neighbors, somewhat less toward strangers, and the least toward neighbors at the correct boundary. The ratio of aggressive acts to lateral displays followed the same pattern, presumably because the perceived threat to the resident decreases in the same order. Taken together these data suggest that collared lizards are able to assess the threat of an opponent and signal motivation to respond aggressively towards that opponent.Communicated by S. Downes     

Egg incubation temperature affects male reproductive success but not display behaviors in lizards

The complex ritualized displays of males in many territorial species suggest that selection has shaped male behaviors in ways that affect fitness. In this study, we evaluated the link between display behavior during male–male interactions and reproductive success in the Australian jacky dragon (Amphibolurus muricatus), a lizard species that uses a complex series of movement patterns for communication. We quantified variation in male display behaviors by using video playback experiments in the laboratory, and subsequently assessed variation in male reproductive success by paternity analyses of offspring. Because the lizards used in this study came from eggs incubated under three thermal environments, we also could evaluate the impact of developmental temperature on adult behavior and reproductive success. Incubation temperature had a strong effect on male reproductive success; males produced under intermediate temperatures sired more offspring than those produced under extreme developmental temperatures. However, incubation temperature did not affect male display behavior, nor was male behavior associated with reproductive success. Our findings do not support the common assumption that display behaviors used during male–male interactions affect reproductive success.     

Information content is more important than sensory system or physical distance in guiding the long-term evolutionary relationships between signaling modalities in Sceloporus lizards

Long-term signal evolution is shaped by a variety of selective pressures including the need to convey additional information or to improve message transfer to specific receivers or through multiple environments. Here, we test the relative importance of information and sensory modality in shaping the long-term evolution of multimodal signals in Sceloporus lizards. To broadcast identity at territorial boundaries, male Sceloporus use both visual motion (headbob) and chemical signals, whereas they use color (blue belly patches) to signal aggression. Using modern phylogenetic comparative methods, we found a negative correlation between evolutionary changes in visual motion (headbobs) and chemical (femoral pore) signals, but only indirect ties between the evolution of color and motion signals (both of which are perceived visually) through viviparity, and no evidence of an evolutionary link between color and chemical signals. We also find a negative correlation between arboreality and chemical signals. Thus, information content (in this case, broadcasting individual identity versus signaling aggression) appears to play a more important role than sensory modality or physical distance in guiding long-term signal evolution. Additional insights into the underlying evolutionary processes are described, illustrating the utility of a phylogenetic approach.     

Male response to an aggressive visual signal, the wing wave display, in swamp sparrows

Signaling often involves complex suites of behaviors that incorporate different sensory modalities. Whatever modality is used to establish that a signal functions in communication researchers must demonstrate that receivers respond to it. The territory defense response of male swamp sparrows involves a variety of behaviors that includes both vocal and visual displays. One of these, the “wing wave” display, is a distinctive movement that predicts physical attack. Here, we use robotic taxidermic mounts paired with song to test the hypothesis that wing waving is a signal and, specifically, that male receivers respond to wing waving as a signal of aggressive intent. As predicted, subjects responded more aggressively to the mount during wing waving trials than during stationary trials. A second experiment demonstrated that this effect cannot be attributed simply to increased attention to movement. Less expectedly, subjects did not alter their own display behavior in response to wing waving as compared to a static mount. We conclude that the wing wave display in the context of singing is a signal that functions in male–male aggressive communication. Questions remain, including whether wing waving functions as a signal in the absence of singing and whether wing waving and song are redundant signals or communicate different information.     

Soft song is a reliable signal of aggressive intent in song sparrows

Animals frequently use signals to modulate aggressive interactions. Establishing that a signal is aggressive or threatening requires demonstrating that it is more commonly used in agonistic contexts, that it predicts subsequent aggressive behaviors by the sender, and that receivers respond differently to this signal. Like many birds, song sparrows (Melospiza melodia) produce a low-amplitude “soft song” vocalization that has been hypothesized to be an aggressive signal. Soft song meets the first two criteria, but previous research has failed to demonstrate that soft song provokes aggression or that receivers even perceive soft song differently from normal loud song. We used a playback experiment with taxidermic mount presentation to test whether territorial male song sparrows respond differently to loud and soft song playbacks. Subjects reacted more strongly to the soft song playback by approaching the mount more closely, increasing wing wave displays, and increasing the proportion of their own songs that were soft songs, with further trends toward increasing the number of flights and attacks. These results confirm that soft song is a conventional signal of aggression in song sparrows and that increased receiver retaliation maintains its reliability.     

Strike-induced chemosensory searching by a teiid lizard,the golden tegu (Tupinambis nigropunctatus)

Summary Strike-induced chemosensory searching (SICS) is experimentally demonstrated in a teiid lizard,Tupinambis nigropunctatus. SICS consists of a concurrent post-strike elevation in tongue-flick rate (PETF) and searching movements after voluntary release or escape of bitten prey or removal of prey from the predator's mouth. The results are consistent with previous data showing that PETF and/or SICS occur in all families of scleroglossan lizards and snakes and all families of actively foraging lizards yet studied. The relatively short duration of SICS (2 min) in a lizard having lingual and vomeronasal structure highly specialized for chemosensory sampling and analysis suggests that phylogenetic and ecological factors may be more important than morphology in determining the duration. The greatest known durations occur only in the presumably monophyletic clade containing varanoid lizards and snakes, all of which have highly developed chemical sampling and chemoreceptor apparatus, but in addition feed on prey that has a high probability of being relocated by prolonged scent-trailing. Because only active foragers move through the habitat while tongue-flicking and exhibit lingually mediated prey chemical discrimination, only active foragers may be expected to use SICS. SICS would appear to be useless to an ambush forager and might disrupt its defensive crypticity, rendering it more detectable to predators and prey. Therefore, it may be predicted that SICS is adaptively adjusted to foraging mode.     

Defensive secretion of a flightless grasshopper: Failure to prevent lizard attack

Summary We tested the role of a grasshopper defensive secretion in deterring lizard predation. Adults, but not young larvae, of the chemically defended lubber grasshopperRomalea guttata (=microptera) froth a volatile secretion when attacked by predators. The lizardAnolis carolinensis failed to strike juvenile lubbers (which lack secretion) in laboratory trials. Survivorship of palatable crickets loaded with secretion offered toA. carolinensis was not significantly different from survivorship of control crickets. In experiments designed to investigate if lizards learn an aversion to the secretion, striking times forSceloporus undulatus fed wax worms coated with secretion were not significantly different over three days of trials. Three primary conclusions are drawn from these data. First, the secretion may not be necessary for lubber protection from lizards. Second, lubber secretion does not appear to deter lizards from attacking or eating prey items. Third, lizards do not appear to develop an aversion to the secretion.     

Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola

Female preference for dominant males is widespread and it is generally assumed that success in male-male competition reflects high quality. However, male dominance is not always attractive to females. Alternatively, relatively symmetric individuals may experience fitness advantages, but it remains to be determined whether males with more symmetrical secondary sexual traits experience advantages in both intra- and intersexual selection. We analysed the factors that determine dominance status in males of the lizard Lacerta monticola, and their relationship to female mate preference, estimated by the attractiveness of males' scents to females. Sexually dimorphic traits of this lizard (head size and femoral pores) appear to be advanced by different selection pressures. Males with relatively higher heads, which give them advantage in intrasexual contests, were more dominant. However, head size was unimportant to females, which preferred to be in areas marked by relatively heavier males, but also by males more symmetric in their counts of left and right femoral pores. Chemicals arising from the femoral pores and other glands might honestly indicate quality (i.e. related to the symmetry levels) of a male to females and may result from intersexual selection. Females may use this information because the only benefit of mate choice to female lizards may be genetic quality. Chemical signals may be more reliable and have a greater importance in sexual selection processes of lizards than has previously been considered.     

Prey chemical discrimination in ambush foragers: absence in representatives of two additional iguanian lizard families and probable olfactory mediation in a gekkonine gecko

Summary. Lingually mediated prey chemical discrimination in lizards has evolved in active foragers, been lost in taxa that have reverted to ambush foraging, and has not evolved in taxa that have retained the ancestral ambushing. Previous studies have shown that all families of insectivorous ambushers lack prey chemical discrimination, including most families of iguanian lizards and two gekkonid species. I conducted experimental studies of prey chemical discrimination in representatives of two additional iguanian families and a third gekkonid lizard. An oplurid species, Oplurus cuvieri and a corytophanid, Corytophanes cristatus, did not discriminate among prey chemicals and control substances. Prey chemical discrimination is now known to be absent in insectivorous ambush foragers in all but one of the families in Iguania, one of the two major lizard radiations. Hoplocercidae remains unstudied. Like other ambushing gekkonid lizards, Pachydactylus turneri did not exhibit elevated tongue-flick rates in response to prey chemicals. However, after tongue-flicking or being touched on the labial scales by cotton swabs, these lizards bit swabs bearing prey chemicals more frequently than control stimuli. They also exhibited buccal pulsing more frequently in response to prey chemicals than deionized water, suggesting olfactory sampling. The unusually highly developed olfactory organs of gekkonid lizards and their nocturnal habits suggest that olfaction may be more important to foraging than in other lizards. Further studies are needed to determine relative roles of olfaction and vomerolfaction in selective response to prey chemicals and to ascertain whether and to what extent the tongue may be used to locate and identify prey. Received 30 March 1999; accepted 26 July 1999     

Homing behaviour in the sleepy lizard (Tiliqua rugosa): the role of visual cues and the parietal eye

To investigate how visual cues are integrated into a navigational strategy for homing in the Australian sleepy lizard (Tiliqua rugosa), lizards were displaced beyond their home range, either with full access to visual cues or with no access to visual cues during the displacement. Homeward orientation was significantly worse when lizards were denied visual cues during the displacement than when they were not. However when lizards were displaced with their field of view restricted to the sky, their homeward orientation was equally as good as that of lizards displaced with no visual restriction. These experiments suggest that sleepy lizards use celestial cues to determine the compass bearing of the outward journey, and reverse this bearing to orient in the homeward direction (course reversal). In a subsequent experiment, lizards oriented randomly with respect to home when the parietal eye was entirely covered with a patch during the displacement and return, while control lizards fitted with a sham parietal eye patch were well oriented towards home. In both groups, the lateral eyes were unobstructed and had complete access to visual cues including celestial cues and landmarks. These results suggest that the parietal eye plays a highly significant role in sleepy lizard homing, perhaps mediating a sky polarization compass sense.     

Advertisement-call modification,male competition,and female preference in the bird-voiced treefrog <Emphasis Type="Italic">Hyla avivoca</Emphasis>

Senders and receivers influence dynamic characteristics of the signals used for mate attraction over different time scales. On a moment-to-moment basis, interactions among senders competing for a mate influence dynamic characteristics, whereas the preferences of receivers of the opposite gender exert an influence over evolutionary time. We observed and recorded the calling patterns of the bird-voiced treefrog Hyla avivoca to assess how the dynamic characters of calls vary during interactions among groups of males in a chorus. This question was also addressed using playback experiments with males. Playback experiments with females showed how changes in dynamic call properties are likely to affect male mating success. Frogs calling in pairs, groups, or in response to playbacks produced longer calls than did isolated males. During call overlap, males often increased the duration of the silent interval (gaps) between the pulses of their calls so that the pulses of the calls of two neighbors interdigitated. This change resulted in increased variability of pulse rate, a traditionally static acoustic property; however, males also produced high proportions of non-overlapped calls in which variability in pulse rate was low and had species-typical values. Females preferred long calls to short- and average-duration calls, and non-overlapped calls to overlapped calls. Given a choice between pairs of overlapped calls, females preferred pairs in which the proportion of overlap was low and pairs in which the pulses of such calls interdigitated completely. The observed patterns of vocal competition thus reflect the preferences of conspecific females, which have influenced the evolution of the calling behavior of H. avivoca. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Field playback of male display attracts females in lek breeding sage grouse

Summary Recent correlational studies of lekking sage grouse suggest that male vocal display attracts females. To test this hypothesis further, the natural displays of a territorial male were supplemented with the tape-recorded display of another, reproductively-successful, individual. Significantly, more females approached the speaker's location on days when the recording was played, and also on non-playback days immediately following a playback, than on other non-playback days (Fig. 1). Analysis of male displays indicated that females were responding to the playback itself rather than to changes in male behavior. The after-response following a playback suggests that some females present during a playback remembered its location and approached on a subsequent lek visit. The results provide necessary support for the epigamic function of vocal display, and suggest ways in which female responses to male display may influence lek structure.     

The response of female Mountain White-crowned Sparrows to songs from their natal dialect and an alien dialect

Summary Female Mountain White-crowned Sparrows from Colorado were tested in a laboratory playback experiment to determine their response to male songs from their own natal dialect and to those from an alien dialect of the same subspecies, Zonotrichia leucophrys oriantha (Fig. 1). Observations were made on locomotor activity and copulation postures produced during each experimental test session.The subjects gave copulation displays almost exclusively when hearing their natal dialect and new or no displays when hearing the alien dialect (Fig. 2). The birds also exhibited significantly greater locomotor activity when hearing the natal dialect than they did when hearing the alien dialect (Fig. 3).We conclude that females are sensitized by their early song learning experience to be responsive to songs from their natal dialect and virtually sexually unresponsive to songs from an alien dialect. We speculate that the copulation posture given in the experiment implies that females in natural populations would preferably only mate assortatively with males from their natal dialect region.     

The effects of early experience on subsequent feeding responses in the Tegu,Tupinambis teguixin (Squamata : Teiidae)

The purpose of this study was to assess the effects of early feeding experiences on subsequent responses to prey in the tegu, Tupinambis teguixin. Five-day old lizards were exposed to the odors of various prey and control substances on cotton-tipped applicators with the tongue-flick attack score (TFAS) chosen as the dependent variable. Each lizard was exposed to four stimuli: two controls (deionised water and cologne), and extracts from a mouse Mus musculus, and a lizard Ameiva ameiva, in a repeated measures, randomized block design, receiving one stimulus training session / day over a 40-day period. Tongue-flicks directed toward the applicator were counted over a 1 min period as well as the amount of time that elapsed from the first tongue flick to any bite that may have occurred. Live neonatal mice (but not A. ameiva), offered on a weekly basis, were used as a food source for tegus over a 10-month period. After 10 months, tegus were exposed to applicators containing control odors as well as those containing extracts from mice and lizards (A. ameiva). Mouse extracts elicited significantly higher TFAS as compared to those elicited by A. ameiva or control odors, suggesting that prey odors encountered in the environment shortly after hatching can influence prey preferences by these lizards later in life. These results also indicate that tegu lizards can learn to use specific odor cues associated with naturally occurring prey as releasers for subsequent hunting behaviors.     

Shifted balance of risk and cost after autotomy affects use of cover,escape, activity,and foraging in the keeled earless lizard (<Emphasis Type="Italic">Holbrookia propinqua</Emphasis>)

Autotomy of expendable body parts is often a successful last-chance antipredatory defense for a variety of invertebrates and vertebrates, especially lizards. However, loss of a body part imposes costs and risks, some of which may be reduced by modifying subsequent behavior. I studied effects of experimentally induced autotomy of the tail in the keeled earless lizard (Holbrookia propinqua) on use of cover, escape behavior, activity, and feeding. Autotomized lizards stayed closer to plant cover than sham-autotomized lizards (having intact tails) when approached by an investigator simulating a predator. Autotomized males, but not females, fled further than sham-autotomized lizards. Autotomy did not affect the distance from an approaching predator when the lizards began to flee. After autotomy, the number of days on which lizards were active differed between sexes and lizards made fewer attempts to catch prey per unit time than lizards with intact tails. Tail loss did not affect the percentage of time spent moving. Staying closer to refuge, fleeing further after autotomy, and decreasing surface activity may compensate for decreased maximum escape speed or agility, and may reflect use of a greater margin of safety when the tail is unavailable for autotomy. Decrease in surface activity may be comparable to use of safer microhabitats reported for other lizards and damselflies subsequent to autotomy. Several possible reasons for the lower rate of feeding attempts by autotomized lizards are discussed.     

Experimental support for the cost–benefit model of lizard thermoregulation

According to Huey and Slatkin’s [Q Rev Biol 51:363–384, 1976] cost–benefit model of behavioural thermoregulation, lizards should adjust their thermoregulatory strategy between active thermoregulation and thermoconformity (no thermoregulation) according to the costs (time and energy spent thermoregulating, exposure to predators), benefits (optimised physiological performance) and thermal quality of environment associated with a given situation. However, Gilchrist’s [Am Nat 146:252–270, 1995] model of thermal specialisation suggests that apparently costly mechanisms of behavioural thermoregulation can greatly increase fitness if the optimal body temperature is achieved. Field studies of ectotherm thermoregulatory strategies under extreme cold conditions and experiments testing the effects of cool environments on thermoregulatory behaviour are surprisingly scarce. We conducted laboratory experiments to test if common lizards Zootoca vivipara (an active thermoregulator in the field) are able to switch between active thermoregulation and thermoconformity in response to different thermal environments. We found that lizards in treatments with an opportunity to reach their preferred body temperature thermoregulated accurately, maintained their level of daily activity and improved their body condition considerably. In contrast, lizards in the treatment where the preferred body temperature could not be reached became thermoconformers, decreased their daily activity (except for gravid females) and did not increase their body condition. Our results show that lizards can indeed change their thermoregulatory strategy but stress that maintaining the preferred body temperature and, thus, optimising the physiological performance have high priority in lizard behaviour.     

Scent marking pheromones in lizards: cholesterol and long chain alcohols elicit avoidance and aggression in male Acanthodactylus boskianus (Squamata: Lacertidae)

Femoral gland secretions are believed to play an important role in chemical communication and social organization of lizards. In spite of this, few studies have investigated the chemical composition and the behavioural roles of these secretions. The lacertid lizard Acanthodactylus boskianus is a good example, having these well-developed glands in both sexes. We used GC–MS chemical analysis of gland secretions and y-maze choice test bioassays to investigate the ability of the lizards to detect and respond to different synthetic blends made from compounds identified in the gland secretions. Based upon the GC–MS quantification data, we selected representatives of the main chemical groups (steroids, alcohols, acids, alkanes) detected in the lizard secretions and used these in a behavioural bioassay against controls. Males showed significant avoidance behaviour for cholesterol and alcohol blends, combined with agonistic behaviour towards these stimuli. Females did not show any significant selection to particular odour combinations. The data support the hypotheses that lizards can potentially use femoral gland secretions in chemical odour trails and utilize scent to mark territories and potentially also to establish dominance hierarchies. Cholesterol and long chain alcohols are suggested as potential candidates functioning as scent marking pheromones in A. boskianus.