Refuge sharing network predicts ectoparasite load in a lizard

Living in social groups facilitates cross-infection by parasites. However, empirical studies on indirect transmission within wildlife populations are scarce. We investigated whether asynchronous overnight refuge sharing among neighboring sleepy lizards, Tiliqua rugosa, facilitates indirect transmission of its ectoparasitic tick, Amblyomma limbatum. We fitted 18 neighboring lizards with GPS recorders, observed their overnight refuge use each night over 3 months, and counted their ticks every fortnight. We constructed a transmission network to estimate the cross-infection risk based on asynchronous refuge sharing frequencies among all lizards and the life history traits of the tick. Although self-infection was possible, the network provided a powerful predictor of measured tick loads. Highly connected lizards that frequently used their neighbors’ refuges were characterized by higher tick loads. Thus, indirect contact had a major influence on transmission pathways and parasite loads. Furthermore, lizards that used many different refuges had lower cross- and self-infection risks and lower tick loads than individuals that used relatively fewer refuges. Increasing the number of refuges used by a lizard may be an important defense mechanism against ectoparasite transmission in this species. Our study provides important empirical data to further understand how indirectly transmitted parasites move through host populations and influence individual parasite loads.     

Network structure and parasite transmission in a group living lizard,the gidgee skink, <Emphasis Type="Italic">Egernia stokesii</Emphasis>

Gidgee skinks (Egernia stokesii) form large social aggregations in rocky outcrops across the Flinders Ranges in South Australia. Group members share refuges (rock crevices), which may promote parasite transmission. We measured connectivity of individuals in networks constructed from patterns of common crevice use and observed patterns of parasitism by three blood parasites (Hemolivia, Schellackia and Plasmodium) and an ectoparasitic tick (Amblyomma vikirri). Data came from a 1-year mark-recapture study of four populations. Transmission networks were constructed to represent possible transmission pathways among lizards. Two lizards that used the same refuge within an estimated transmission period were considered connected in the transmission network. An edge was placed between them, directed towards the individual that occupied the crevice last. Social networks, a sub-set of same-day only associations, were small and highly fragmented compared with transmission networks, suggesting that non-synchronous crevice use leads to more transmission opportunities than direct social association. In transmission networks, lizards infested by ticks were connected to more other tick-infested lizards than uninfected lizards. Lizards infected by ticks and carrying multiple blood parasite infections were in more connected positions in the network than lizards without ticks or with one or no blood parasites. Our findings suggest higher levels of network connectivity may increase the risk of becoming infected or that parasites influence lizard behaviour and consequently their position in the network. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau and R. James).     

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.     

Variation in homeward orientation performance in the sleepy lizard (Tiliqua rugosa): effects of sex and reproductive period

Sleepy lizards are monogamous skinks which show high pair fidelity. This study reveals inter- and intrasexual differences in homeward orientation performance in this lizard. Male and female lizards were displaced during three phases of the spring activity period, the pre-pairing, pairing/mating, and post-pairing periods. All groups (with the exception of post-pairing males) were significantly oriented homewards, but males were significantly better oriented towards home than females during the pairing period. Furthermore, males were significantly better homeward oriented during the pre-pairing and pairing periods than in the post-pairing period. Similar results were observed for rate of movement away from the release site. In sleepy lizards, sex-based differences in homing behaviour are unlikely to be attributable to differences in the area of familiarity, or availability of orientation mechanisms. However differences in homing motivation may explain these differences. Males may miss mating if absent from the home range during the pre-pairing and pairing periods, while females may still be able to obtain a mating even when absent. Females however may be more motivated than males to return to the familiar home range during the post-pairing period to ensure efficient feeding during internal embryo development. Received: 16 February 1998 / Accepted after revision: 28 March 1998     

Relatedness and avoidance of inbreeding in the lizard, Tiliqua rugosa

Two potential mechanisms for reducing the level of inbreeding, sex-biased dispersal and kin avoidance, were examined in the Australian sleepy lizard, Tiliqua rugosa. The home range centres, and the genotypes at four polymorphic microsatellite DNA loci were determined for adult lizards in a 70-ha study area near Mount Mary, South Australia. From estimates of genetic relatedness, females were as closely related to other females as they were to males, both within the whole study area, and within home ranges. Similarly, males were as closely related to other males as they were to females. This suggests that dispersal in the population is not sex-biased. Sleepy lizards form monogamous pairs during the spring. Partners were less closely related to each other than to other potential partners in the home range area. This suggests active choice of unrelated partners. The mechanism for recognising related from unrelated individuals is unknown, but the behaviour could reduce inbreeding. Received: 7 November 1998 / Accepted: 30 May 1999     

Sex- and performance-based escape behaviour in an Asian agamid lizard,Phrynocephalus vlangalii

In lizards, males are predicted to sprint faster and run for longer than females by virtue of higher testosterone levels and differences in morphology. Consequently, escape behaviour is also predicted to be associated with sex and locomotor performance, yet these links have rarely been explored. Here, we tested whether escape behaviour is associated with locomotor performance in the toad-headed agama, Phrynocephalus vlangalii, and whether it is sex-dependent. This species is also characterized by elaborate tail displays, which we examined as a potential pursuit-deterrent signal. Tail waves were performed by a very small proportion (2/58, 3 %) of individuals during predatory trials, suggesting that tail signalling functions exclusively in a social context. To understand the relationships between sex, escape behaviour and performance, we first measured escape behaviour (flight initiation distance, flight distance—measured differently compared to previous studies of lizard escape behaviour, and refuge use) in the field before measuring maximal sprint speed and endurance on the same individuals in the laboratory. Flight initiation distance did not differ between the sexes and was unrelated to performance capacity (maximal endurance and sprint speed) but was positively related to body size with larger individuals fleeing earlier. Males fled farther than females, but flight distance was also unrelated to either endurance or sprint speed. Interestingly, faster females were less likely to enter a refuge than slower females, whereas sprint speed and the probability of taking refuge were unrelated for males. Our results suggest that when males and females are not obviously sexually dimorphic, they are more likely to overlap in escape tactics.     

Home range overlap of mothers and their offspring in the sleepy lizard, Tiliqua rugosa

This paper reports a field investigation of interactions between juveniles and their mothers in the Australian sleepy lizard, Tiliqua rugosa. In their first spring season, juvenile lizards maintain home ranges largely within the home range of their mother. Juvenile home ranges are significantly smaller than those of adult males and females, and juveniles move significantly less often and significantly shorter distances than adults. While siblings were never found together in the spring, they showed a significant tendency to be closer to each other than if they were randomly located in their home ranges. Juveniles and mothers were never found together, nor was there any evidence for any positive (or negative) spatial association. Nevertheless, the extended tolerance of home range overlap represents a greater degree of mother-offspring association than has been previously reported for other lizards. Despite this, the level of parental care can only be described as minimal. Received: 20 June 1997 / Accepted after revision: 29 December 1997     

Mate fidelity in an Australian lizard Trachydosaurus rugosus

Summary The Australian sleepy lizard Trachydosaurus rugosus is a large mainly herbivorous skink, which occupies overlapping home ranges. In the Mt. Mary study area, South Australia, 6567 captures were made of 2412 different individuals between February 1982 and December 1986. The mating season when male and female lizards formed pairs was in the spring months of October and November. Some lizards were captured in pairs more than once in the same mating season. Amongst this group over 90% of females and over 70% of males were found with the same partner. These monogamous pair-bonds lasting up to eight weeks, had been predicted by Stamps (1983) for large lizards with overlapping home ranges. In addition 79% of females and 68% of males recaptured in pairs in subsequent years were found with the same partner. This mate fidelity is too high to be accounted for by chance encounters. The selective advantages of actively choosing the same partner each year are discussed.     

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.     

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.     

Social monogamy and extra-pair fertilization in an Australian lizard, Tiliqua rugosa

This study investigates social monogamy in the Australian sleepy lizard, Tiliqua rugosa. At a 70-ha site near Mount Mary, South Australia, we radio tracked 55 adult female and 39 adult male lizards during their spring activity periods. Each lizard was observed in 1–5 years. Females were observed with a single male partner on an average of 10.8 days per year, although in 17.3% of cases, females were observed on 2 or fewer days with a male. The most intense pairing period each year was 15 September–15 November when females were with male partners on an average of 36% of observation days. Partnerships lasted an average of 43.3 days each year. After mating in early November, the pairs separated. Observations of females pairing with other males were rare. Most males (82%) were also consistently monogamous, although 7 were observed pairing with 2 females within one season. To investigate paternity, we allowed 21 gravid females to give birth to 42 offspring in the laboratory. We determined genotypes at five polymorphic microsatellite DNA loci for the females, their male partners and their offspring. Four litters (19%) and 6 of the offspring from those litters (14.3%) showed evidence of extra-pair fertilization (EPF). Although the sample sizes are small, females of polygynous males were more likely to experience EPF. Received: 22 February 1998 / Accepted after revision: 23 May 1998     

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.     

Do mountain log skinks (<Emphasis Type="Italic">Pseudemoia entrecasteauxii</Emphasis>) modify their behaviour in the presence of two predators?

Prey often adopt antipredator strategies to reduce the likelihood of predation. In the presence of predators, prey may use antipredator strategies that are effective against a single predator (specific) or that are effective against several predators (nonspecific). Most studies have been confined to single predator environments although prey are often faced with multiple predators. When more than one predator is present, specific antipredator behaviours can conflict and avoidance of one predator may increase vulnerability to another. To test how prey cope with this dilemma, I recorded the behaviours of lizards responding to the nonlethal cues of a bird and snake presented singly and simultaneously. Lizards use specific and conflicting antipredator tactics when confronted with each predator, as evidenced by refuge use. However, when both predators were present, lizards refuge use was the same as in the predator-free environment, indicating that they abandoned refuge use as a primary mechanism for predator avoidance. In the presence of both predators, they reduced their overall movement and time spent thermoregulating. This shift in behaviour may represent a compromise to minimize overall risk, following a change in predator exposure. This provides evidence of plasticity in lizard antipredator behaviour and shows that prey responses to two predators cannot be accurately predicted from what is observed when only one predator is present.Communicated by W. Cooper     

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.     

SOCPROG programs: analysing animal social structures

SOCPROG is a set of programs which analyses data on animal associations. Data usually come from observations of the social behaviour of individually identifiable animals. Associations among animals, sampling periods, restrictions on the data and association indices can be defined very flexibly. SOCPROG can analyse data sets including 1,000 or more individuals. Association matrices are displayed using sociograms, principal coordinates analysis, multidimensional scaling and cluster analyses. Permutation tests, Mantel and related tests and matrix correlation methods examine hypotheses about preferred associations among individuals and classes of individual. Weighted network statistics are calculated and can be tested against null hypotheses. Temporal analyses include displays of lagged association rates (rates of reassociation following an association). Models can be fitted to lagged association rates. Multiple association measures, including measures produced by other programs such as genetic or range use data, may be analysed using Mantel tests and principal components analysis. SOCPROG also performs mark-recapture population analyses and movement analyses. SOCPROG is written in the programming language MATLAB and may be downloaded free from the World Wide Web.     

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.     

Size-based predation by kookaburras (Dacelo novaeguineae) on lizards (Eulamprus tympanum: Scincidae): what determines prey vulnerability?

Lizards and birds are both popular ”model organisms” in behavioural ecology, but the interactions between them have attracted little study. Given the putative importance of birds as predators of diurnal lizards, it is of considerable interest to know which traits (of lizards as well as birds) influence the outcome of a predatory attempt. We studied predation by giant terrestrial kingfishers (kookaburras, Dacelo novaeguineae: Alcedinidae) on heliothermic diurnal lizards (highland water skinks, Eulamprus tympanum: Scincidae), with particular reference to the role of prey (lizard) size. Our approach was twofold: to gather direct evidence (sizes of lizards consumed in the field, compared to those available) and indirect evidence (size-related shifts in lizard behaviour). We quantified the size structure of a natural population of skinks (determined by an extensive mark-recapture program), and compared it to the sizes of wild lizards taken by kookaburras (determined by analysis of prey remains left at the birds’ nests). Kookaburras showed size-based predation: they preyed mainly on small and medium-sized rather than large lizards in the field. However, the mechanism producing this bias remains elusive. It is not due to any distinctive behavioural attributes (locomotor ability, activity level, habitat usage) of the lizards of the size class disproportionately taken by the kookaburras. The greater vulnerability of subadult lizards may reflect subtle ontogenetic shifts in ecological and behavioural traits, but our data suggest that great caution is needed in inferring patterns of vulnerability to predation from indirect measures based on either the prey or the predator alone. Instead, we need direct observations on the interaction between the two. Received: 30 May 2000 / Revised: 29 July 2000 / Accepted: 26 August 2000     

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