Rock-dwelling lizards exhibit less sensitivity of sprint speed to increases in substrate rugosity

Effectively moving across variable substrates is important to all terrestrial animals. The effects of substrates on lizard performance have ecological ramifications including the partitioning of habitat according to sprinting ability on different surfaces. This phenomenon is known as sprint sensitivity, or the decrease in sprint speed due to change in substrate. However, sprint sensitivity has been characterized only in arboreal Anolis lizards. Our study measured sensitivity to substrate rugosity among six lizard species that occupy rocky, sandy, and/or arboreal habitats. Lizards that use rocky habitats are less sensitive to changes in substrate rugosity, followed by arboreal lizards, and then by lizards that use sandy habitats. We infer from comparative phylogenetic analysis that forelimb, chest, and tail dimensions are important external morphological features related to sensitivity to changes in substrate rugosity.     

Adhesion and allometry from metamorphosis to maturation in hylid tree frogs: a sticky problem

Many species of climbing frog possess large disc-like digital pads, which facilitate adhesion. The consensus of earlier studies is that frogs depend on a wet adhesive mechanism, chiefly influenced by pad area and surface tension properties of the mediating adhesive fluid. The relationship between morphology, size and adhesion is of particular interest for tree frogs, because evolution of adhesive ability has facilitated niche expansion into arboreal habitats. If frogs are geometrically similar, and growth occurs isometrically, then mass will increase at a higher rate than toe-pad area, and an adhesive system directly dependent on area may be adversely affected. We investigated scaling of adhesive ability with ontogeny in seven species of hylid tree frog to test whether the responses to the challenges of maintaining adhesion with growth were sufficient to allow adult frogs to stick as effectively on smooth substrates as juvenile frogs. In all species, mass increased at a lower rate than expected with isometric growth. This was less pronounced in larger species, perhaps owing to the demands of locomotory modes such as jumping. In smaller hylids, this non-isometric increase in mass was sufficient to enable adult frogs to adhere as effectively as juveniles. In larger species, however, the ability of adult frogs to adhere was significantly lower than that of juveniles, despite evidence of increased toe-pad efficiency. Within all species adhesive forces increased at a greater rate than toe-pad area, suggestive of changes in the relative influence of the contributory components of the wet adhesive mechanism with growth.     

Convergent evolution across the Australian continent: ecotype diversification drives morphological convergence in two distantly related clades of Australian frogs

Animals from different clades but subject to similar environments often evolve similar body shapes and physiological adaptations due to convergent evolution, but this has been rarely tested at the transcontinental level and across entire classes of animal. Australia's biome diversity, isolation and aridification history provide excellent opportunities for comparative analyses on broad‐scale macroevolutionary patterns. We collected morphological and environmental data on eighty‐four (98%) Australian hylid frog species and categorized them into ecotypes. Using a phylogenetic framework, we tested the hypothesis that frogs from the same ecotype display similar body shape patterns: (i) across all the Australian hylids, and (ii) through comparison with a similar previous study on 127 (97%) Australian myobatrachid species. Body size and shape variation did not follow a strong phylogenetic pattern and was not tightly correlated with environment, but there was a stronger association between morphotype and ecotype. Both arboreal and aquatic frogs had long limbs, whereas limbs of fossorial species were shorter. Other terrestrial species were convergent on the more typical frog body shape. We quantified the strength of morphological convergence at two levels: (i) between fossorial myobatrachid and hylid frogs, and (ii) in each ecomorph within the hylids. We found strong convergence within ecotypes, especially in fossorial species. Ecotypes were also reflected in physiological adaptations: both arboreal and cocooned fossorial frogs tend to have higher rates of evaporative water loss. Our results illustrate how adaptation to different ecological niches plays a crucial role in morphological evolution, boosting phenotypic diversity within a clade. Despite phylogenetic conservatism, morphological adaptation to repeatedly emerging new environments can erase the signature of ancestral morphotypes, resulting in phenotypic diversification and convergence both within and between diverse clades.     

Preferred temperature correlates with evaporative water loss in hylid frogs from northern Australia

We measured temperature preferences of 12 species of hylid frogs (Litoria and Cyclorana) from northern Australia in a laboratory thermal gradient. These species represented a range of ecological habitat use (aquatic, terrestrial, arboreal), adult body size (0.5-60 g), and cutaneous resistance to water loss (Rc=0.6-63.1 s cm-1). We found significant differences among species in selected skin temperature and gradient temperature but not in the variances of these measures (an index of precision of temperature selection). The species' differences correlated significantly with cutaneous resistance to water loss, with more-resistant frogs selecting higher skin and substrate temperatures in the thermal gradient, even after phylogenetic relationships are taken into account. Because cutaneous resistance to water loss also correlates with ecological habit (arboreal>terrestrial>aquatic), we suggest that their higher resistance to water loss allows arboreal and terrestrial species better ability to tolerate high temperatures, where growth or locomotory speed may be higher, without the associated risk of desiccation.     

Getting a grip on the evolution of grasping in musteloid carnivorans: a three‐dimensional analysis of forelimb shape

The ability to grasp and manipulate is often considered a hallmark of hominins and associated with the evolution of their bipedal locomotion and tool use. Yet, many other mammals use their forelimbs to grasp and manipulate objects. Previous investigations have suggested that grasping may be derived from digging behaviour, arboreal locomotion or hunting behaviour. Here, we test the arboreal origin of grasping and investigate whether an arboreal lifestyle could confer a greater grasping ability in musteloid carnivorans. Moreover, we investigate the morphological adaptations related to grasping and the differences between arboreal species with different grasping abilities. We predict that if grasping is derived from an arboreal lifestyle, then the anatomical specializations of the forelimb for arboreality must be similar to those involved in grasping. We further predict that arboreal species with a well‐developed manipulation ability will have articulations that facilitate radio‐ulnar rotation. We use ancestral character state reconstructions of lifestyle and grasping ability to understand the evolution of both traits. Finally, we use a surface sliding semi‐landmark approach capable of quantifying the articulations in their full complexity. Our results largely confirm our predictions, demonstrating that musteloids with greater grasping skills differ markedly from others in the shape of their forelimb bones. These analyses further suggest that the evolution of an arboreal lifestyle likely preceded the development of enhanced grasping ability.     

The specialisation of the third metacarpal and hand in arboreal frogs: Adaptation for arboreal habitat?

Skeletal morphology is directly associated with habitat characteristics. To investigate the arboreal adaptation, we studied the osteological morphology of the forelimbs and the third metacarpals of arboreal frogs (Rhacophoridae and Hylidae) and non‐arboreal frogs (Bombinatoridae, Bufonidae, Megophryidae, Ranidae, and Microhylidae) using transparent specimens or X‐rays of skeletons. Our results revealed that the bony knob on the third metacarpal, which formed by a dilated and elongated lateral articular cartilage (AL) through endochondral ossification, occurred only in species of Rhacophorinae. The results of the phylogenetic comparative methods and correlation analysis strongly supported the conclusion that the bony knob is a phylogenetic independent evolution trait and had a significant correlation with the arboreal habitat. Furthermore, anatomical observation showed that a muscle adhered to the bony knob. Therefore, we speculated that the bony knob might act as an enlarged attachment point for larger or more musculatures to help with grasping. In addition, the relative length of the hand showed a significant difference between arboreal and non‐arboreal species (p = .007), suggesting that longer hands might be an arboreal adaptive trait. Overall, this study leads to a deeper understanding of the arboreal adaptation.     

Comparative analysis of cutaneous evaporative water loss in frogs demonstrates correlation with ecological habits

Most frog species show little resistance to evaporative water loss (EWL), but some arboreal species are known to have very high resistances. We measured EWL and cutaneous resistance to evaporation (Rc) in 25 species of frogs from northern Australia, including 17 species in the family Hylidae, six species in the Myobatrachidae, and one each in the Bufonidae and the Microhylidae. These species display a variety of ecological habits, including aquatic, terrestrial, and arboreal specialisations, with the complete range of habits displayed within just the one hylid genus, Litoria. The 25 species measured in this study have resistances that range from Rc=0 to 63.1. These include low values indistinguishable from a free water surface to high values typical of "waterproof" anuran species. There was a strong correlation between ecological habit and Rc, even taking phylogenetic relationships into account; arboreal species had the highest resistance, aquatic species tended to have little or no resistance, and terrestrial species tended to have resistance between those of arboreal and aquatic frogs. For one species, Litoria rubella, we found no significant changes in EWL along a 1,500-km aridity gradient. This study represents the strongest evidence to date of a link between ecological habits and cutaneous resistance to water loss among species of frogs.     

Recurrent ecological adaptations revealed through a molecular analysis of the secretive cophyline frogs of Madagascar

The cophyline microhylid frogs of Madagascar show a wide range of habitat specialization, ranging from terrestrial/burrowing and semi-arboreal to entirely arboreal species. The classification of these frogs is thus far mainly based upon morphological, largely osteological, characters that might be homoplastic. Using 1173 bp of DNA sequences from the mitochondrial 12S and 16S rRNA genes, we here present a molecular phylogeny for 28 species of all known genera, except for the genus Madecassophryne. The resulting maximum likelihood tree contained four major clades: one represented by the genus Anodonthyla, the second by Cophyla and Platypelis, the third by several terrestrial and semi-arboreal species of the genus Plethodontohyla, and the fourth by species of the genera Stumpffia, Plethodontohyla, and Rhombophryne. The results confirm that several cophyline lineages adapted independently to similar habitats, with multiple shifts among terrestriality and arboreality. The direction of these shifts cannot be ascertained due to unclarified relationships among the most basal lineages, but for one terrestrial species (Anodonthyla montana), it is most parsimonious to assume that it evolved from arboreal ancestors. Our results suggest that the genus Plethodontohyla is probably paraphyletic, and that the classification of this and of the genus Rhombophryne needs to be re-assessed.     

Amphibian biology and husbandry

Extant amphibians comprise three lineages-- salamanders (Urodela or Caudata), frogs and toads (Anura), and caecilians (Gymnophiona, Apoda, or Caecilia)--which contain more than 6,000 species. Fewer than a dozen species of amphibians are commonly maintained in laboratory colonies, and the husbandry requirements for the vast majority of amphibians are poorly known. For these species, a review of basic characteristics of amphibian biology supplemented by inferences drawn from the morphological and physiological characteristics of the species in question provides a basis for decisions about housing and feeding. Amphibians are ectotherms, and their skin is permeable to water, ions, and respiratory gases. Most species are secretive and, in many cases, nocturnal. The essential characteristics of their environment include appropriate levels of humidity, temperature, and lighting as well as retreat sites. Terrestrial and arboreal species require moist substrates, water dishes, and high relative humidity. Because temperature requirements for most species are poorly known, it is advisable to use a temperature mosaic that will allow an animal to find an appropriate temperature within its cage. Photoperiod may affect physiology and behavior (especially reproduction and hibernation), and although the importance of ultraviolet light for calcium metabolism by amphibians is not yet known, ecological observations suggest that it might be important for some species of frogs. Some amphibians are territorial, and some use olfactory cues to mark their territory and to recognize other individuals of their species. All amphibians are carnivorous as adults, and the feeding response of many species is elicited by the movement of prey. Diets should include a mixture of prey species, and it may be advisable to load prey with vitamins and minerals.     

Wiping behavior, skin resistance, and the metabolic response to dehydration in the arboreal frog Phyllomedusa hypochondrialis

Several species of arboreal frogs secrete lipids from cutaneous glands and wipe these secretions over the body surfaces to reduce evaporative water losses. Following wiping, frogs become immobile in water-conserving postures, and some have suggested they are torpid. Here we report wiping behaviors and the physiological correlates of immobile postures in the arboreal monkey frog Phyllomedusa hypochondrialis. Skin resistance to water loss was comparatively high, and rates of evaporation were as low as 4% of that from a free water surface. Standard rates of metabolism (SMR) varied from 89 microL O2 h(-1) at 18 degrees C to 316 microL O2 h(-1) at 34 degrees C and were sensitive to both temperature (T) and body mass (W; mL O2 h(-1) = 0.016W0.642 x 10(0.030T)). The mean SMR did not change significantly during four consecutive days of dehydration when animals lost 19%-34% of body mass. Therefore, it appears these frogs do not routinely depress metabolic rates following wiping. However, some individuals that lost higher percentages of body water exhibited trends of decreasing oxygen consumption, suggesting that suppression of metabolic rates might occur at greater levels of body water deficit or perhaps during a slower course of dehydration than imposed by our experiments (e.g., individuals that are secluded during periods of drought).     

Increasing arboreality with altitude: a novel biogeographic dimension

Biodiversity is spatially organized by climatic gradients across elevation and latitude. But do other gradients exist that might drive biogeographic patterns? Here, we show that rainforest''s vertical strata provide climatic gradients much steeper than those offered by elevation and latitude, and biodiversity of arboreal species is organized along this gradient. In Philippine and Singaporean rainforests, we demonstrate that rainforest frogs tend to shift up in the rainforest strata as altitude increases. Moreover, a Philippine-wide dataset of frog distributions shows that frog assemblages become increasingly arboreal at higher elevations. Thus, increased arboreality with elevation at broad biogeographic scales mirrors patterns we observed at local scales. Our proposed ‘arboreality hypothesis’ suggests that the ability to exploit arboreal habitats confers the potential for larger geographical distributions because species can shift their location in the rainforest strata to compensate for shifts in temperature associated with elevation and latitude. This novel finding may help explain patterns of species richness and abundance wherever vegetation produces a vertical microclimatic gradient. Our results further suggest that global warming will ‘flatten’ the biodiversity in rainforests by pushing arboreal species towards the cooler and wetter ground. This ‘flattening’ could potentially have serious impacts on forest functioning and species survival.     

Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

The ecomorphology of Bornean tree frogs (family Rhacophoridae)

Ecomorphological studies generally assume a causal relationship between morphology and ecology mediated by performance. That assumption was tested in a community of Bornean tree frogs of the family Rhacophoridae. Biomechanical models allow a priori predictions about expected intra- and interspecific correlations among toepad area, hind-limb length, body mass, sticking ability, jumping distance, microhabitat, vertical height and substrate. Both intra- and interspecifically, size and shape variables showed patterns of association with ecology predicted on the basis of maintaining relative as well as absolute levels of performance. Unexpectedly, the form-function relationship between toepad area and sticking ability differed intra- and interspecifically. These findings indicate the need for more empirical work examining morphology-performance relationships and their use in ecology.     

Small frogs get their worms first: the role of nonodonate arthropods in the recruitment of Haematoloechus coloradensis and Haematoloechus complexus in newly metamorphosed northern leopard frogs, Rana pipiens, and woodhouse's toads, Bufo woodhousii

Studies on the life cycles and epizootiology of North American frog lung flukes indicate that most species utilize odonates as second intermediate hosts; adult frogs become infected by ingesting odonate intermediate hosts. Newly metamorphosed frogs are rarely infected with these parasites, predominantly because they are gape-limited predators that cannot feed on large intermediate hosts such as dragonflies. We examined the role of the frog diet and potential intermediate hosts in the recruitment of the frog lung fluke, Haematoloechus coloradensis, to metamorphosed northern leopard frogs (Rana pipiens), Woodhouse's toads (Bufo woodhousii), and bullfrogs (Rana catesbeiana) from western Nebraska. Because of the uncertain validity of H. coloradensis as a distinct species from Haematoloechus complexus, morphological characters of both species were reevaluated and the life cycles of both species were completed in the laboratory. The morphological data on H. coloradensis and H. coimplexus indicate that they differ in their oral sucker to pharynx ratio, uterine loop distribution, and placement of vitelline follicles. However, in terms of their life cycles, both species are quite similar in their use of physid snails as first intermediate hosts, a wide range of nonodonate and odonate arthropods as second intermediate hosts, and leopard frogs and toads as definitive hosts. These results indicate that H. coloradensis and H. complexus are generalists at the second intermediate host level and might be able to infect newly metamorphosed leopard frogs and toads by using small nonodonate arthropods more commonly than other frog lung fluke species. Comparisons of population structure of adult flukes in newly metamorphosed leopard frogs indicate that the generalist nature of H. coloradensis metacercariae enables it to colonize young of the year leopard frogs more commonly than other Haematoloechus spp. that only use odonates as second intermediate hosts. In this respect, the generalist nature of H. coloradensis and H. complexus at the second intermediate host level is an avenue for the colonization of young of year frogs.     

Incipient morphological specializations associated with fossorial life in the skull of ground squirrels (Sciuridae,Rodentia)

Anatomical and biological specializations have been studied extensively in fossorial rodents, especially in subterranean species, such as mole-rats or pocket-gophers. Sciurids (i.e., squirrels) are mostly known for their diverse locomotory behaviors, and encompass many arboreal species. They also include less specialized fossorial species, such as ground squirrels that are mainly scratch diggers. The skull of ground squirrels remains poorly investigated in a fossorial context, while it may reflect incipient morphological specializations associated with fossorial life, especially due to the putative use of incisors for digging in some taxa. Here, we present the results of a comparative analysis of the skull of five fossorial sciurid species, and compare those to four arboreal sciurids, one arboreal/fossorial sciurid and one specialized fossorial aplodontiid. The quantification of both cranial and mandibular shapes, using three dimensional geometric morphometrics, reveals that fossorial species clearly depart from arboreal species. Fossorial species from the Marmotini tribe, and also Xerini to a lesser extent, show widened zygomatic arches and occipital plate on the cranium, and a wide mandible with reduced condyles. These shared characteristics, which are present in the aplodontiid species, likely represent fossorial specializations rather than relaxed selection on traits related to the ancestral arboreal condition of sciurids. Such cranial and mandibular configurations combined with proodont incisors might also be related to the frequent use of incisors for digging (added to forelimbs), especially in Marmotini evolving in soft to hard soil conditions. This study provides some clues to understand the evolutionary mechanisms shaping the skull of fossorial rodents, in relation to the time spent underground and to the nature of the soil.     

Whole animal measurements of shear and adhesive forces in adult tree frogs: insights into underlying mechanisms of adhesion obtained from studying the effects of size and scale

This allometric study of adhesion in 15 Trinidadian tree frog species investigates how relationships between length, area and mass limit the ability of adult frog species of different sizes to adhere to inclined and overhanging surfaces. Our experiments show that hylid frogs possess an area-based wet adhesive system in which larger species are lighter than expected from isometry and adhere better than expected from their toe pad area. However, in spite of these adaptations, larger species adhere less well than smaller species. In addition to these adhesive forces, tree frogs also generate significant shear forces that scale with mass, suggesting that they are frictional forces. Toe pads detach by peeling and frogs have strategies to prevent peeling from taking place while they are adhering to surfaces, including orienting themselves head-up on slopes. The scaling of tree frog adhesion is also used to distinguish between different models for adhesion, including classic formulae for capillarity and Stefan adhesion. These classic equations grossly overestimate the adhesive forces that tree frogs produce. More promising are peeling models, designed to predict the pull-off forces of adhesive tape. However, more work is required before we can qualitatively and quantitatively describe the adhesive mechanism of tree frogs.     

Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia

The frog genus Leptopelis is composed of ~50 species that occur across sub‐Saharan Africa. The majority of these frogs are typically arboreal; however, a few species have evolved a fossorial lifestyle. Most species inhabit lowland forests, but a few species have adapted to high elevations. Five species of Leptopelis occupy the Ethiopian highlands and provide a good opportunity to study the evolutionary transition from an arboreal to a fossorial lifestyle, as well as the diversification in this biodiversity hot spot. We sequenced 14 nuclear and three mitochondrial genes, and generated thousands of SNPs from ddRAD sequencing to study the evolutionary relationships of Ethiopian Leptopelis. The five species of highland Leptopelis form a monophyletic group, which diversified during the late Miocene and Pliocene. We found strong population structure in the fossorial species L. gramineus, with levels of genetic differentiation between populations similar to those found between arboreal species. This could indicate that L. gramineus is a complex of cryptic species. We propose that after the original colonization of the Ethiopian highlands by the ancestor of the L. gramineus group, episodes of vicariance fragmented the ancestral populations of this group. We also report the re‐evolution of arboreality in L. susanae, which evolved from a fossorial ancestor, a rare ecological switch in frogs that had previously been reported only once.     

Evolution of morphology and locomotor performance in anurans: relationships with microhabitat diversification

The relationships between morphology, performance, behavior and ecology provide evidence for multiple and complex phenotypic adaptations. The anuran body plan, for example, is evolutionarily conserved and shows clear specializations to jumping performance back at least to the early Jurassic. However, there are instances of more recent adaptation to habit diversity in the post‐cranial skeleton, including relative limb length. The present study tested adaptive models of morphological evolution in anurans associated with the diversity of microhabitat use (semi‐aquatic arboreal, fossorial, torrent, and terrestrial) in species of anuran amphibians from Brazil and Australia. We use phylogenetic comparative methods to determine which evolutionary models, including Brownian motion (BM) and Ornstein‐Uhlenbeck (OU) are consistent with morphological variation observed across anuran species. Furthermore, this study investigated the relationship of maximum distance jumped as a function of components of morphological variables and microhabitat use. We found there are multiple optima of limb lengths associated to different microhabitats with a trend of increasing hindlimbs in torrent, arboreal, semi‐aquatic whereas fossorial and terrestrial species evolve toward optima with shorter hindlimbs. Moreover, arboreal, semi‐aquatic and torrent anurans have higher jumping performance and longer hindlimbs, when compared to terrestrial and fossorial species. We corroborate the hypothesis that evolutionary modifications of overall limb morphology have been important in the diversification of locomotor performance along the anuran phylogeny. Such evolutionary changes converged in different phylogenetic groups adapted to similar microhabitat use in two different zoogeographical regions.     

Patterns of morphological variation and correlates of habitat use in Chameleons

The lizard family Chameleonidae is one of the most distinctive taxa of all vertebrates. Nonetheless, despite great intrafamilial diversity, little research has been conducted on morphological variation among chameleons. As a first step in this direction, we took morphological measurements on the head, limbs, spines, and tail of 56 species. Our goals were to investigate whether morphological variation correlates with differences in ecology and to examine whether correlations exist among different aspects of morphology. Based on existing information, species were classified either as arboreal or terrestrial, the latter referring to species that are known to use the ground on a regular basis. This study confirms that considerable intrafamilial variation exists among chameleons and that these traits appear to be evolutionarily quite labile. Once the effects of size are removed, functionally related traits tend to covary; however, few correlations are observed between non-functionally related traits. Many differences in the lengths of the limbs and head elements were detected between terrestrial and arboreal species, but the functional and selective significance of these differences is not clear. Further research on chameleon behaviour and ecology is required to understand the factors contributing to chameleon morphological diversity. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 91–103.