Survival estimation in a long-lived monitor lizard: radio-tracking of Varanus mertensi

The population dynamics of varanids (large monitor lizards) is poorly understood. We report on the most detailed study to date of a population of one of Australia’s largest semi-aquatic varanids, Varanus mertensi. Survival of V. mertensi was derived from known-fate modelling of radio-tracked individuals over two and a half years. We demonstrate empirically what intuition suggests; that apparent survival probability in long-lived lizards is high over short sampling periods, with body size and gender influencing these estimates. Survival estimation in long-lived species such as varanids clearly requires long-term studies.     

The evolution of bipedal postures in varanoid lizards

The bipedal posture (BP) and gait of humans are unique evolutionary hallmarks, but similar stances and forms of locomotion have had enormous influences on a range of phylogenetically diverse tetrapods, particularly dinosaurs and birds, and a range of mammalian lineages, including non-human apes. The complex movements involved in bipedalism appear to have modest evolutionary origins, and it is presumed that a stable and erect posture is a prerequisite for erect strides and other bipedal movements. Facultative bipedalism in several lineages of lizards is achieved by running, but some varanid lizards (genus Varanus) exhibit BPs without running. In these cases, BPs (BP_standing) are not used as a form of locomotion; rather, BP_standing is associated with defensive displays, and such postures also probably permit better inspection of the environment. Yet, in other varanids, BPs have been observed only during combat episodes (BP_combat), where both contestants rise together and embrace in the so-called clinch phase. Numerous other species, however, show neither type of BP. Past researchers have commented that only large-bodied varanids exhibit BP, a behaviour that appears to show phylogenetic trends. We termed this idea the King–Green–Pianka (KGP) bipedal hypothesis. In this article, we address two main questions derived from the KGP hypothesis. First, what is the phylogenetic distribution of BP in Varanus and close relatives (varanoids)? Second, is BP positively correlated with the phylogenetic distribution of large body size (e.g. snout–vent length, SVL)? In addition, we asked a related question: do the lengths of the femur and tail show body size-independent adaptive trends in association with BP? Because varanid species that show BP_standing also use these postures during combat (BP_combat), both types of BP were analysed collectively and simply termed BP. Using comparative phylogenetic analyses, the reconstruction of BP required three steps, involving a single gain and two losses. Specifically, BP was widespread in the monophyletic Varanus, and the single gain occurred at the most recent common ancestor of the African clade. The two losses of BP occurred in different clades (Indo-Asian B clade and Indo-Australian Odatria clade). BPs are absent in the sister group to Varanus (Lanthanotus borneensis) and the other outgroup species (Heloderma spp.). Our phylogenetic reconstruction supports the KGP prediction that BP is restricted to large-bodied taxa. Using the Hansen model of adaptive evolution on a limited, but highly relevant morphological dataset (i.e. SVL; femur length, FL; tail length, TL), we demonstrated that these characters were not equivalent in their contribution to the evolution of BP in Varanus. SVL was significantly correlated with BP when modelled in a phylogenetic context, but the model identified random processes as dominant over adaptive evolution, suggesting that a body size threshold might be involved in the evolution of BP. A Brownian motion (BM) model outperformed the selection model in our analysis of relative TL, suggesting that TL and BP evolved independently. The selection model for relative FL outperformed the BM model, indicating that FL and BP share an adaptive history. Our non-phylogenetic analyses involving regression residuals of FL and TL vs. SVL showed no significant correlation between these characters and BP. We suggest that BP in Varanus provides a convergent or analogue model from which to investigate various forms of bipedalism in tetrapod vertebrates, especially other reptiles, such as theropod dinosaurs. Because BP_standing in varanids is possibly an incipient stage to some form of upright locomotion, its inclusion as a general model in evolutionary analyses of bipedalism of vertebrates will probably provide novel and important insights. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97 , 652–663.     

Head shape evolution in monitor lizards (Varanus): interactions between extreme size disparity,phylogeny and ecology

Characterizing patterns of observed current variation, and testing hypotheses concerning the potential drivers of this variation, is fundamental to understanding how morphology evolves. Phylogenetic history, size and ecology are all central components driving the evolution of morphological variation, but only recently have methods become available to tease these aspects apart for particular body structures. Extant monitor lizards (Varanus) have radiated into an incredible range of habitats and display the largest body size range of any terrestrial vertebrate genus. Although their body morphology remains remarkably conservative, they have obvious head shape variation. We use two‐dimensional geometric morphometric techniques to characterize the patterns of dorsal head shape variation in 36 species (375 specimens) of varanid, and test how this variation relates to size, phylogenetic history and ecology as represented by habitat. Interspecific head shape disparity is strongly allometric. Once size effects are removed, principal component analysis shows that most shape variation relates to changes in the snout and head width. Size‐corrected head shape variation has strong phylogenetic signal at a broad level, but habitat use is predictive of shape disparity within phylogenetic lineages. Size often explains shape disparity among organisms; however, the ability to separate size and shape variation using geometric morphometrics has enabled the identification of phylogenetic history and habitat as additional key factors contributing to the evolution of head shape disparity among varanid lizards.     

Earliest example of a giant monitor lizard (varanus, varanidae, squamata)

Background

Varanidae is a clade of tiny (<20 mm pre-caudal length [PCL]) to giant (>600 mm PCL) lizards first appearing in the Cretaceous. True monitor lizards (Varanus) are known from diagnostic remains beginning in the early Miocene (Varanus rusingensis), although extremely fragmentary remains have been suggested as indicating earlier Varanus. The paleobiogeographic history of Varanus and timing for origin of its gigantism remain uncertain.

Methodology/Principal Findings

A new Varanus from the Mytilini Formation (Turolian, Miocene) of Samos, Greece is described. The holotype consists of a partial skull roof, right side of a braincase, partial posterior mandible, fragment of clavicle, and parts of six vertebrae. A cladistic analysis including 83 taxa coded for 5733 molecular and 489 morphological characters (71 previously unincluded) demonstrates that the new fossil is a nested member of an otherwise exclusively East Asian Varanus clade. The new species is the earliest-known giant (>600 mm PCL) terrestrial lizard. Importantly, this species co-existed with a diverse continental mammalian fauna.

Conclusions/Significance

The new monitor is larger (longer) than 99% of known fossil and living lizards. Varanus includes, by far, the largest limbed squamates today. The only extant non-snake squamates that approach monitors in maximum size are the glass-snake Pseudopus and the worm-lizard Amphisbaena. Mosasauroids were larger, but exclusively marine, and occurred only during the Late Cretaceous. Large, extant, non-Varanus, lizards are limbless and/or largely isolated from mammalian competitors. By contrast, our new Varanus achieved gigantism in a continental environment populated by diverse eutherian mammal competitors.     

Comparing macroecological patterns across continents: evolution of climatic niche breadth in varanid lizards

Macroecological analyses often test hypotheses at the global scale, or among more closely related species in a single region (e.g. continent). Here, we test several hypotheses about climatic niche widths among relatively closely related species that occur across multiple continents, and compare patterns within and across continents to see if they differ. We focus on the lizard genus Varanus (monitor lizards), which occurs in diverse environments in Africa, Asia, and Australia. We address three main questions. 1) How do climatic niche breadths of species on a given niche axis change based on the position of species along that niche axis? (E.g. are species that occur in more extreme environments more narrowly specialized for those conditions?) 2) Are there trade‐offs in niche breadths on temperature and precipitation axes among species, or are niche widths on different axes positively related? 3) Is variation in niche breadths among species explained primarily by within‐locality seasonal variation, or by differences in climatic conditions among localities across the species range? We generate a new time‐calibrated phylogeny for Varanus and test these hypotheses within and between continents using climatic data and phylogenetic methods. Our results show that patterns on each continent often parallel each other and global patterns. However, in many other cases, the strength of relationships can change dramatically among closely related species on different continents. Overall, we found that: 1) species in warmer environments have narrower temperature niche breadths, but there is no relationship between precipitation niche breadth and niche position; 2) temperature and precipitation niche breadths tend to be positively related among species, rather than showing trade‐offs; and 3) within‐locality seasonal variation explains most variation in climatic niche breadths. Some of these results are concordant with previous studies (in amphibians and North American lizards), and might represent general macroecological patterns.     

Size-related activity patterns in an herbivorous lizard

A study of the pre-breeding season behavior of a colony (N=16) of Ctenosaura hemilopha revealed significant differences among the four size classes with respect to time of activity. Comparisons of lizard size classes showed that the smaller lizards emerged earlier, had earlier activity periods, and usually fed earlier than the larger lizards (all P<0.01). The two smaller sizes were also aggressive earlier in the day than the two larger classes (P<001). Members of all size classes ate the same food items, but food competition was absent. Thus, the differences in activity patterns among the size classes are not due to avoidance of food competition, an explanation which has been invoked for insectivorous lizards. These patterns probably result from the fact that thermal inertia increases with body size. Differences in activity patterns of insectivorous species can also originate from thermoregulatory constraints, and could provide the variation upon which selection for reduced competition may have acted to increase separation along the time axis of niche space.     

Monitor lizards: a pan-African check-list of their zoogeography (Sauria: Varanidae: Polydaedalus)

Aim This goal of this paper is to present an up‐to‐date, accurate check‐list and distribution of the monitor lizards on the African continent. No such list of their distribution has been attempted since Robert F. Mertens' (1942) treatise (Abhandlungen Senckenbergischen Naturforschenden Gesellschaft, 462 , 465 , 466 ). Location The localities included herein are all countries on the African continent, and adjacent islands, with a list of Varanus known to Yemen and Saudi Arabian Republics included for clarity. One fossil Varanus rusingensis is included, as it is the first, and only described, fossil African Varanus known. Methods Locality records were reviewed from literature sources, museum voucher specimens, personal comments, field observations and photographic records. Results A summation of 3,268 locality records are included herein from the methods listed, with maps depicting these records. Main conclusions From the locality records listed herein, it is evident that the Nile monitor (V. niloticus) has the widest distribution, and that the Yemen monitor (V. yemenensis) has the most restricted distribution; paradoxically, both features may be indicative of their relic habitation on the African continent.     

Metabolic rate and endurance capacity in Australian varanid lizards (Squamata: Varanidae: Varanus)

In ecomorphological and ecophysiological studies, locomotor performance is often considered to be an intermediate step between the form of an organism and its environment. We examined this premise by measuring morphology, physiology and circular track endurance in the closely related group of Australian varanid lizards. Body size, body mass and relative body proportions were poor indicators of endurance. Body mass was not correlated with endurance and size-free lower forelimb length had only a weak relationship with endurance. Instead, maximal metabolic rate was positively correlated with endurance capacity in varanids. A comparison of varanids with other groups of lizards supported this result as varanids showed both elevated maximal metabolic rate and elevated endurance scores when compared with similar sized non-varanid lizards. There was support for a strong association between endurance with foraging mode and climate. Varanid species with higher endurance tended to be widely foraging and from xeric climates, while sit-and-wait and mesic species showed reduced endurance.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 664–676.     

Island/mainland body size differences in Australian varanid lizards

Island varanids seem to be an exception to the rule that territorial vertebrate taxa often become gigantic relative to mainland relatives when on islands, whereas non-territorial species become dwarfed (Case 1978). However, no systematic island/mainland studies have examined the empirical size trends in this group of carnivorous lizards. We perform such an analysis for the Australian region and critically evaluate various selective agents that might be responsible for size changes in several island populations. Insular gigantism occurs at least four times among the island populations examined. The magnitude of size change is positively correlated to prey abundance on the islands (as indirectly measured through a condition index of the lizards, essentially a measure of how fat they arc) and the size of prey: islands with large prey have large varanids and vice versa. Since the island population with the largest size change, the Reevesby Varanus rosenbergi, was introduced less than 100 years ago, these size changes can be quite rapid. This might indicate that selective coefficients are strong; however, we can not exclude the possibility that these size differences have no genetic component and simply reflect environmental differences in growth rate and shifts in age structure between island and mainland locations.     

Hemiclitoris discovered: a fully differentiated erectile structure in female monitor lizards (Varanus spp.) (Reptilia: Varanidae)

In female monitor lizards (Varanus spp.), the ubiquitous presence of paired evertible and erectile structures in the ventral portion of the tail root, which are miniaturized mirror images of the hemipenes of the males, was discovered. These organs contain all the structural elements (including a forked retractor muscle, supporting ossifications, epidermal flounces etc.) that are also characteristic for the hemipenes of the respective conspecific males. Consequently, it is proposed that the term hemiclitoris be used for this organ. A preliminary survey showed this organ to be present in several other squamate families, suggesting that it is ubiquitous in all female Squamata.     

Temporal activity and dietary selection in two coexisting desert snakes,the Saharan sand viper (Cerastes vipera) and the crowned leafnose (Lytorhynchus diadema)

The Saharan sand viper (Cerastes vipera) and the crowned leafnose (Lytorhynchus diadema) are two snake species well adapted to desert sand dunes and, in Israel, coexist in the western Negev Desert. C. vipera is a sit-and-wait ambusher while L. diadema is an active hunter. We studied the seasonal and diel activity patterns and dietary selection of these two species while free-living in the field. Both species were active from early spring until late fall but displayed (i) different seasonal activity patterns – C. vipera was bimodal with peaks in spring and autumn whereas L. diadema was basically unimodal with a peak in summer; (ii) different nocturnal above-ground activity patterns – C. vipera was active mainly during the first three hours of darkness while L. diadema was constantly active during the first seven hours of darkness; and (iii) different patterns of nocturnal behavior – C. vipera moved up to 50 m while L. diadema moved several hundred meters each night. Dietary selection differed between these snake species although lizards, mainly Nidua fringe-fingered lizards (Acanthodactylus scutellatus), were the main dietary item for both. We concluded that temporal partitioning in above-ground activity, different foraging strategies and differences in dietary selection may contribute towards the coexistence of the two snake species.     

A spectacular new Philippine monitor lizard reveals a hidden biogeographic boundary and a novel flagship species for conservation

As humans continue to explore the last uncharted regions of the planet, discoveries of previously unknown species of large vertebrates have become infrequent. Here, we report on the discovery of a spectacular new species of giant, secretive, frugivorous, forest monitor lizard (Genus: Varanus) from the forests of the northern Philippines. Using data from morphology and mitochondrial and nuclear DNA sequences, we demonstrate the taxonomic distinctiveness of this new 2 m long species and provide insight into its historical biogeography and systematic affinities. Our molecular phylogenetic analyses indicate that the new species is closely related to Varanus olivaceus (from southern Luzon and nearby islands), but it differs from this and other varanids with respect to characteristics of scalation, colour pattern, body size, anatomy of the reproductive organs and genetic divergence. The new species appears to be restricted to forests of the central and northern Sierra Madre mountain range; it is separated from the range of V. olivaceus by a more than 150 km stretch that includes at least three low-elevation river valley barriers to dispersal. This discovery identifies a seldom-perceived biogeographic boundary and emphasizes the need for continued biodiversity research in the megadiverse conservation hotspot of the Philippines. It is anticipated that the new species will serve as an important flagship species for conservation efforts aimed at preserving the remaining forests of northern Luzon.     

Neurocranial osteology and systematic relationships of Varanus (Megalania) prisca Owen, 1859 (Squamata: Varanidae)

The neurocranial osteology of the giant monitor lizard Varanus (Megalania) prisca Owen, 1859 is described in detail for the first time. Optimization of neurocranial characters onto phylogenetic topologies for varanoids, including Lanthanotus, Heloderma, and Varanus species nests V. prisca within an Indo‐Australian clade of Varanus on the basis of characters of the otic capsule. A sister‐taxon relationship between V. prisca and Varanus komodoensis Ouwens, 1912 is proposed based on apomorphies of the crista prootica, fenestra vestibuli, occipital recess, and supraoccipital. These results support a monophyletic clade of giant monitors among Indo‐Australian species, and unambiguously synonymize Megalania with Varanus at both generic and subgeneric levels. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 445–457.     

Physiological ecology of the mangrove-dwelling varanid Varanus indicus

Some species of terrestrial lizards in wet-dry tropical climates reduce their body temperatures (T(b)'s) and activity and lower their metabolic rates during the dry season when food and water resources are scarce. However, semiaquatic lizards have access to water and presumably food throughout the year, so it is possible that they will not have the seasonal response seen in terrestrial species. We studied the thermal biology, energetics, and water flux of Varanus indicus, a semiaquatic, mangrove-dwelling varanid in tropical northern Australia. Although V. indicus remained active all year, they reduced their activity in the dry season, but not to the extent of terrestrial varanids. Varanus indicus field metabolic rates decreased by 38% in the dry season mostly as a result of the reduction in activity. Although food and water depletion are the driving forces behind decreases in dry season T(b) selection and energetics for many varanids, V. indicus appears not to be subject to these pressures to the same extent. Thermoregulatory indices indicate that V. indicus actively thermoregulate in the wet and dry seasons, but they do not fully exploit the available thermal resources. These lizards are unusual among varanid lizards in that their midday T(b)'s are relatively low (about 31 degrees C) despite the availability of thermal resources that would allow them to attain substantially higher T(b)'s.     

WHY ARE CLUTCH SIZES MORE VARIABLE IN SOME SPECIES THAN IN OTHERS?

Animal species differ in the variability of their clutch sizes, as well as in mean clutch sizes. This phenomenon is particularly obvious in lizards, where virtually invariant clutch sizes have evolved independently in at least 23 lineages in seven families. Reduced variance in clutch size may arise either as an adaptation (because females with less variable clutch sizes have higher fitness) or as an indirect by-product of selection on other life-history characteristics. Comparative data on Australian scincid lizards indicate that variance in clutch sizes is lowest among species with low mean clutch sizes, small body sizes and a low variance in body sizes of adult females. Phylogenetic analysis shows that evolutionary decreases in the variance of clutch size have accompanied decreases in mean clutch sizes and decreases in the variance of adult female body sizes. Tropical lizards may also exhibit lower variance in clutch size. Most of these characteristics are correlated in occurrence, and may be allometrically tied to small body size. Hence, low variance in clutch size may be a consequence of allometric effects on a correlated suite of life-history characteristics. Exceptions to the general patterns noted above—especially, lizard species with invariant clutch sizes but large body sizes—may be due to loss of genetic variance for clutch sizes in lineages that have passed through a “bottleneck” of small body sizes and hence, low variance in clutch sizes.     

Is the Evolution of Viviparity Accompanied by a Relative Increase in Maternal Abdomen Size in Lizards?

Female reptiles with viviparous reproduction should leave space for their eggs that reach the maximum mass and volume in the oviducts. Is the evolution of viviparity accompanied by a relative increase in maternal abdomen size, thus allowing viviparous females to increase the amount of space for eggs? To answer this question, we compared morphology and reproductive output between oviparous and viviparous species using three pairs of lizards, which included two Eremias, two Eutropis and two Phrynocephalus species with different reproductive modes. The two lizards in each pair differed morphologically, but were similar in the patterns of sexual dimorphism in abdomen and head sizes and the rates at which reproductive output increased with maternal body and abdomen sizes. Postpartum females were heavier in viviparous species, suggesting that the strategy adopted by females to allocate energy towards competing demands differs between oviparous and viviparous species. Reproductive output was increased in one viviparous species, but decreased in the other two, as compared with congeneric oviparous species. The space requirement for eggs did not differ between oviparous and viviparous females in one species pair, but was greater in viviparous females in the other two pairs greater in relative clutch mass and relative litter mass. In the two Phrynocephalus species, viviparous females produced heavier clutches than did oviparous females not by increasing the relative size of the abdomen, but by being more full of eggs. In none of the three species pairs was the maternal abdomen size greater in the viviparous species after accounting for body size. Our data show that the evolution of viviparity is not accompanied by a relative increase in maternal abdomen size in lizards. Future work could usefully investigate other lineages of lizards to determine whether our results are generalisable to all lizards.     

Body proportions,microhabitat selection,and adaptive radiation of Liolaemus lizards in central Chile

Summary A biometric analysis of body proportions with presumably functional meaning for microhabitat selection was made on 12 species of Liolaemus lizards in central Chile. Characters studied were forelimb length, hindlimb length, tail length (all standardized by the corresponding snout-vent length), and the ratio forelimb/hindlimb length. It is shown that irrespective of terrestrial, saxicolous, or arboreal habits, Liolaemus species are remarkably similar in body proportions. The only exceptions are: L. lemniscatus, an open ground-dweller which exhibits significantly shorter limbs; and L. chiliensis and L. schroederi, both shrub-climbers which exhibit significantly longer tail. It is concluded that the adaptive radiation of Liolaemus lizards in central Chile has been accomplished mainly by diversification of activity time, food size, and microhabitat type. Morphological divergence in body proportions seems to have played an unimportant role.     

Ecological aspects of thermoregulation at high altitudes: the case of andean Liolaemus lizards in northern Chile

Summary We document activity field temperatures, daily activity patterns, and extent of thermoregulation in four species of Liolaemus lizards inhabiting at high altitude (above 3500 m) in the Andes of northern Chile. These four species have similar activity field temperature (Tb near 29°C) despite their being distributed at different altitudinal belts. However, conspicuous differences exist between higher-altitude (L. alticolor and L. jamesi) and lower-altitude (L. islugensis and L. ornatus) lizards regarding extent of thermoregulation and activity period. Some differences in morphology, behavior, and patterns of microhabitat occupancy are also apparent among these four species and are seemingly related to the thermal environment to which they are subjected. In comparison to eight low-altitude Liolaemus species in central Chile (Tb near 35°C) the four high-altitude species in northern Chile have lower activity field temperature. The latter is apparently due to the constraints imposed by the harsh Andean thermal environment, a hypothesis supported by the fact that high-altitude Liolaemus lizards under laboratory conditions demonstrate body temperatures that exceed by 5°C or more, those recorded in the field.     

Overdispersion of body size in Australian desert lizard communities at local scales only: no evidence for the Narcissus effect

Both local and regional processes may contribute to community diversity and structure at local scales. Although many studies have investigated patterns of local or regional community structure, few have addressed the extent to which local community structure influences patterns within regional species pools. Here we investigate the role of body size in community assembly at local and regional scales in Ctenotus lizards from arid Australia. Ctenotus has long been noted for its exceptional species diversity in the Australian arid-zone, and previous studies have attempted to elucidate the processes underlying species coexistence within communities of these lizards. However, no consensus has emerged on the role of interspecific competition in the assembly and maintenance of Ctenotus communities. We studied Ctenotus communities at several hundred sites in the arid interior of Australia to test the hypothesis that body sizes within local and regional Ctenotus assemblages should be overdispersed relative to null models of community assembly, and we explored the relationship between body size dispersion at local and regional scales. Results indicate a striking pattern of community-wide overdispersion of body size at local scales, as measured by the variance in size ratios among co-occurring species. However, we find no evidence for body size overdispersion within regional species pools, suggesting a lack of correspondence between processes influencing the distribution of species phenotypes at local and regional scales. We suggest that size ratio constancy in Ctenotus communities may have resulted from contemporary ecological interactions among species or ecological character displacement, and we discuss alternative explanations for the observed patterns. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Niche segregation among sympatric Amazonian teiid lizards

We examined standard niche axes (time, place, and food) for three sympatric teiid lizards in the Amazon rain forest. Activity times during the day were similar among species. Ameiva ameiva were in more open microhabitats and had higher body temperatures compared with the two species of Kentropyx. Microhabitat overlaps were low and not significantly different from simulations based on Monte Carlo analysis. Grasshoppers, crickets, and spiders were important in the diets of all three species and many relatively abundant prey were infrequently eaten (e.g., ants). Dietary overlaps were most similar between the two species of Kentropyx even though microhabitat overlaps were relatively low. A Monte Carlo analysis on prey types revealed that dietary overlaps were higher at all ranks than simulated overlaps indicating that use of prey is not random. Although prey size was correlated with lizard body size, there were no species differences in adjusted prey size. A. ameiva ate more prey items at a given body size than either species of Kentropyx. Body size varies among species, with A. ameiva being the largest and K. altamazonica the smallest. The two species of Kentropyx are most distant morphologically, with A. ameiva intermediate. The most distant species morphologically are the most similar in terms of prey types. A morphological analysis including 15 species from four genera revealed patterns of covariation that reflected phylogenetic affinities (i.e., taxonomic patterns are evident). A cluster analysis revealed that A. ameiva, K. pelviceps, and K. altamazonica were in the same morphological group and that within that group, A. ameiva differed from the rest of the species. In addition, K. pelviceps and K. altamazonica were distinguishable from other species of Kentropyx based on morphology. Received: 26 December 1998 / Accepted: 15 September 1999