Evolution of diel activity patterns in skinks (Squamata: Scincidae), the world's second‐largest family of terrestrial vertebrates

Many animals have strict diel activity patterns, with unique adaptations for either diurnal or nocturnal activity. Diel activity is phylogenetically conserved, yet evolutionary shifts in diel activity occur and lead to important changes in an organism's morphology, physiology, and behavior. We use phylogenetic comparative methods to examine the evolutionary history of diel activity in skinks, one of the largest families of terrestrial vertebrates. We examine how diel patterns are associated with microhabitat, ambient temperatures, and morphology. We found support for a nondiurnal ancestral skink. Strict diurnality in crown group skinks only evolved during the Paleogene. Nocturnal habits are associated with fossorial activity, limb reduction and loss, and warm temperatures. Our results shed light on the evolution of diel activity patterns in a large radiation of terrestrial ectotherms and reveal how both intrinsic biotic and extrinsic abiotic factors can shape the evolution of animal activity patterns

A database of the morphology, ecology and literature of the world's limb‐reduced skinks

Aim Limb-reduced squamates are a convenient model system to investigate macroevolutionary trends in morphology. Here, we provide morphological, ecological and literature data on all known species of limb-reduced skinks (Scincidae) and their relatives, representing one of the most diverse and widely distributed groups of limb-reduced squamates. Location Global. Taxon Skinks (Reptilia, Squamata: Scincidae). Limb-reduced forms. Methods Morphological data were sourced from the primary literature, spanning a period of over 150 years. Linear body measurements were averaged across all values in the literature, preserving proportionality to body length. For digits and presacral vertebrae, we used maximum recorded counts. Ecological and biogeographical data were sourced from habitat assessments in the primary literature, online databases and field guides. Literature data were sorted according to type of study. To exemplify the applicability of the database, we used Markov-chain ordered models to estimate the evolutionary frequency of limb reduction and loss in skinks. Results We find evidence of limb reduction and loss in a total of 394 species worldwide, representing ~23% of all skink species, and ~30% of genera. The distribution of limb-reduced and limbless forms differs from that of fully limbed forms, as they are present in all biogeographic realms with the almost complete exclusion of the Americas. We estimate that limb reduction evolved more than 50 times in skinks, and that loss of at least one limb pair evolved at least 24 times. Main conclusions The dataset captures a broad spectrum of morphological and ecological variation in a large, globally distributed taxonomic group. It establishes a widely applicable definition of limb reduction based on limb proportions as a reference for future studies. Such an extensive collection of morphological and ecological data can pave the way for investigations of dramatic morphological transitions and their ecological drivers at a global and local scale

Macroecological and biogeographical patterns of limb reduction in the world's skinks

First published: 08 December 2022Aim: Limb reduction is a dramatic evolutionary transition, yet whether it is achieved in similar trajectories across clades, and its environmental drivers, remain unclear. We investigate the macroevolutionary and biogeographical patterns of limb reduction in skinks, where limb reduction occurred more often than in any other tetrapod clade, and test their associations with substrate categories using a global database. We test for habitat associations of body shapes in a group of Australian skinks using quantitative habitat data. Location: Global (Scincidae), Australia (Sphenomorphinae). Taxon: Skinks, Australian Sphenomorphinae. Materials and Methods: We use morphological data to explore the patterns of limb reduction in the world's skinks, investigating how body proportions differ across skink clades and subfamilies. We examine the relationships between body shape and substrate (coarsely classified). Further, we investigate the relationships between body shape and high-resolution soil and climate properties extracted from each species' distribution for Australian sphenomorphines. Results: Relationships between limb lengths and trunk elongation show idiosyncratic patterns across skink clades. Presacral vertebrae numbers positively correlate with trunk elongation in all taxa, except Glaphyromorphus. Skinks from sandy habitats show greater disparity between forelimb and hindlimb lengths than all other substrate categories. In sphenomorphines, shorter limbs and elongated trunks correlate with colder, more humid microhabitats and richer soils; high limb disparity correlates with hot, arid microhabitats and sandy, poor substrates. Main Conclusions: The evolutionary trajectories of limb reduction in skinks are cladespecific and sometimes unique. Selection for specific limb proportions and body sizes in limb-reduced forms changes across substrates. On poor, sandy substrates of arid environments, body shapes with longer hindlimbs may be more efficient for locomotion in a granular fluid (i.e. sand) and exploit the air–substrate interface than complete limblessness. On richer, more humid substrates, such morphology is rare, indicating that navigating cluttered substrates selects for more equal and shorter limb lengths.Marco Camaiti, Alistair R. Evans, Christy A. Hipsley, Mark N. Hutchinson, Shai Meiri, Rodolfo de Oliveira Anderson, Alex Slavenko, David G. Chappl

Reptiles as food: Predation of Australian reptiles by introduced red foxes compounds and complements predation by cats

Context: Invasive species are a major cause of biodiversity loss across much of the world, and a key threat to Australia’s diverse reptile fauna. There has been no previous comprehensive analysis of the potential impact of the introduced European red fox, Vulpes vulpes, on Australian reptiles. Aims: We seek to provide an inventory of all Australian reptile species known to be consumed by the fox, and identify characteristics of squamate species associated with such predation. We also compare these tallies and characteristics with reptile species known to be consumed by the domestic cat, Felis catus, to examine whether predation by these two introduced species is compounded (i.e. affecting much the same set of species) or complementary (affecting different groups of species). Methods: We collated records of Australian reptiles consumed by foxes in Australia, with most records deriving from fox dietary studies (tallying >35 000 samples). We modelled presence or absence of fox predation records against a set of biological and other traits, and population trends, for squamate species. Key results: In total, 108 reptile species (~11% of Australia’s terrestrial reptile fauna) have been recorded as consumed by foxes, fewer than that reported for cats (263 species). Eighty-six species have been reported to be eaten by both predators. More Australian turtle species have been reported as consumed by foxes than by cats, including many that suffer high levels of predation on egg clutches. Twenty threatened reptile species have been reported as consumed by foxes, and 15 by cats. Squamate species consumed by foxes are more likely to be undergoing population decline than those not known to be consumed by foxes. The likelihood of predation by foxes increased with squamate species’ adult body mass, in contrast to the relationship for predation by cats, which peaked at ~217 g. Foxes, but not cats, were also less likely to consume venomous snakes. Conclusions: The two introduced, and now widespread, predators have both compounding and complementary impacts on the Australian reptile fauna. Implications: Enhanced and integrated management of the two introduced predators is likely to provide substantial conservation benefits to much of the Australian reptile fauna

Counting the bodies: Estimating the numbers and spatial variation of Australian reptiles, birds and mammals killed by two invasive mesopredators

Aim Introduced predators negatively impact biodiversity globally, with insular fauna often most severely affected. Here, we assess spatial variation in the number of terrestrial vertebrates (excluding amphibians) killed by two mammalian mesopredators introduced to Australia, the red fox (Vulpes vulpes) and feral cat (Felis catus). We aim to identify prey groups that suffer especially high rates of predation, and regions where losses to foxes and/or cats are most substantial. Location Australia. Methods We draw information on the spatial variation in tallies of reptiles, birds and mammals killed by cats in Australia from published studies. We derive tallies for fox predation by (i) modelling continental-scale spatial variation in fox density, (ii) modelling spatial variation in the frequency of occurrence of prey groups in fox diet, (iii) analysing the number of prey individuals within dietary samples and (iv) discounting animals taken as carrion. We derive point estimates of the numbers of individuals killed annually by foxes and by cats and map spatial variation in these tallies. Results Foxes kill more reptiles, birds and mammals (peaking at 1071 km−2 year−1) than cats (55 km−2 year−1) across most of the unmodified temperate and forested areas of mainland Australia, reflecting the generally higher density of foxes than cats in these environments. However, across most of the continent – mainly the arid central and tropical northern regions (and on most Australian islands) – cats kill more animals than foxes. We estimate that foxes and cats together kill 697 million reptiles annually in Australia, 510 million birds and 1435 million mammals. Main conclusions This continental-scale analysis demonstrates that predation by two introduced species takes a substantial and ongoing toll on Australian reptiles, birds and mammals. Continuing population declines and potential extinctions of some of these species threatens to further compound Australia's poor contemporary conservation record

A global reptile assessment highlights shared conservation needs of tetrapods

Comprehensive assessments of species’ extinction risks have documented the extinction crisis and underpinned strategies for reducing those risks. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened—confirming a previous extrapolation and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods—agriculture, logging, urban development and invasive species—although the threat posed by climate change remains uncertain. Reptiles inhabiting forests, where these threats are strongest, are more threatened than those in arid habitats, contrary to our prediction. Birds, mammals and amphibians are unexpectedly good surrogates for the conservation of reptiles, although threatened reptiles with the smallest ranges tend to be isolated from other threatened tetrapods. Although some reptiles—including most species of crocodiles and turtles—require urgent, targeted action to prevent extinctions, efforts to protect other tetrapods, such as habitat preservation and control of trade and invasive species, will probably also benefit many reptiles.Neil Cox, Bruce E. Young, Philip Bowles, Miguel Fernandez, Julie Marin, Giovanni Rapacciuolo, Monika Böhm, Thomas M. Brooks, S. Blair Hedges, Craig Hilton-Taylor, Michael Hoffmann, Richard K. B. Jenkins, Marcelo F. Tognelli, Graham J. Alexander, Allen Allison, Natalia B. Ananjeva, Mark Auliya, Luciano Javier Avila, David G. Chapple, Diego F. Cisneros-Heredia, Harold G. Cogger, Guarino R. Colli, Anslem de Silva, Carla C. Eisemberg, Johannes Els, Ansel Fong G., Tandora D. Grant, Rodney A. Hitchmough, Djoko T. Iskandar, Noriko Kidera, Marcio Martins, Shai Meiri, Nicola J. Mitchell, Sanjay Molur, Cristiano de C. Nogueira, Juan Carlos Ortiz, Johannes Penner, Anders G. J. Rhodin, Gilson A. Rivas, Mark-Oliver Rödel, Uri Roll, Kate L. Sanders, Georgina Santos-Barrera, Glenn M. Shea, Stephen Spawls, Bryan L. Stuart, Krystal A. Tolley, Jean-François Trape, Marcela A. Vidal, Philipp Wagner, Bryan P. Wallace, Yan Xi

Rock removal associated with agricultural intensification will exacerbate the loss of reptile diversity

Rocky environments host rich levels of biodiversity and provide vital habitat for specialised organisms, range-restricted species and a broad range of ectotherms adapted to saxicoline environments. In Australia, rock habitat is being destroyed during soil amelioration practices associated with agricultural intensification. Advances in rock crushing technology, developed to expand or increase crop yields and efficiency, pose an undocumented threat to global biodiversity, especially reptiles dependent on non-renewable rock habitat in agricultural landscapes. Rock removal is a legislated key threatening process in parts of Australia and will accelerate biodiversity loss if not mitigated. We estimated reptile species’ range overlap with dryland cropping and modified pastoral regions within the Australian wheat-sheep zone to assess the potential impacts of rock crushing practices. We examined species- and family-richness within the impact zone and across bioregions within the impact zone, to identify areas where rock removal has the greatest potential to impact terrestrial and fossorial squamates. Our analysis revealed that 159 potentially impacted reptile species occur within the study area, representing 16% of Australian terrestrial squamates. Fourteen of these species, including six threatened species, have more than 50% range overlap with areas of intensive agriculture, and include several endangered pygopodids, scincids and agamids. Bioregions rich in rock and burrow-dwelling reptiles include the Brigalow Belt South, Murray Darling Depression, Darling Riverine Plains, Eyre Yorke Block, Avon Wheatbelt, Nandewar, Flinders Lofty Block and New South Wales South Western Slopes. Synthesis and applications. The conservation of reptiles in agricultural landscapes requires appropriate management and retention of surface rocks. Potential yield increases from destroying rock habitat to intensify or expand cropland will not compensate for the net loss of reptile populations dependent on non-renewable resources. Financial incentives to prevent the expansion and transformation of non-arable landscapes to cropland are required to prevent the ongoing loss of biodiversity

Evolution and maintenance of colour pattern polymorphism in Liopholis (Squamata : Scincidae)

We examined the evolution and maintenance of colour pattern polymorphism in an Australian lineage of scincid lizards, the genus Liopholis. Liopholis comprises 11 species, with representatives in both the temperate zone and arid zone. Specimens from all major Australian museums were examined to characterise colour pattern polymorphism within Liopholis, and investigate geographic variation in the relative abundance of morphs within polymorphic species. We used a previously published phylogeny for Liopholis to investigate the evolution and maintenance of colour pattern polymorphism within the group. Five species were found to exhibit colour pattern polymorphism (L. margaretae margaretae Storr, L. m. personata Storr, L. montana Donnellan et al., L. multiscutata Mitchell & Behrndt, L. pulchra Werner, L. whitii Lacépède), with six species being monomorphic (L. guthega Donnellan et al., L. inornata Rosén, L. kintorei Stirling & Zietz, L. modesta Storr, L. slateri Storr, L. striata Sternfeld). Three colour morphs occur in L. whitii, with the relative abundance of each varying significantly among latitudes. The patterned morph is most common, while the incidence of the plain-back morph decreases at latitudes higher than 35°S. The L. whitii patternless morph occurs only within a narrow latitudinal band (34–38°S). In L. multiscutata, the relative abundance of the patterned (~89–93%) and patternless morph (~7–11%) is consistent across regions, except for the Nullarbor Plain region where the patternless morph is more common (~39%). Our analyses suggest a single origin of colour pattern polymorphism in Liopholis, followed by the subsequent loss of polymorphism on four occasions. The secondary loss of polymorphism might be associated with climate or habitat, possibly as the result of shifts into the arid zone or alpine regions of Australia. This study provides the necessary framework for future studies of colour pattern polymorphism in Liopholis.David G. Chapple, Mark N. Hutchinson, Brad Maryan, Mike Plivelich, Jennifer A. Moore and J. Scott Keog

Specialist versus Generalist at the Intraspecific Level: Functional Morphology and Substrate Preference of Mediodactylus kotschyi Geckos

Populations of the same species occupying different microhabitats can either exhibit generalized traits across them or display intraspecific variability, adapting to each microhabitat in order to maximize performance. Intraspecific variability contributes to the generation of diversity, following selection and adaptation, and understanding such variability is important for comprehending how individuals choose their microhabitats. Compared with interspecific variability, however, intraspecific variability in functional morphology and its relationship with microhabitat preference and use have been relatively little studied. Here we examined whether populations of the gecko Mediodactylus kotschyi that differ in the substrates they occupy display habitat-specific behaviors and differing morphologies associated with functional adaptation to their microhabitats. We collected 207 geckos from under or on rocks or on trees from seven populations in Greece. On large islands individuals occupy both substrates; whereas small islets are devoid of trees and the geckos are restricted to rocks, while on the mainland they are only found on trees. We determined gecko substrate preferences in the laboratory, together with their clinging abilities to the different substrates. We measured their limbs, digits, and claws and assessed how these measurements relate to clinging ability. Geckos from all populations preferred the tree made available to them, but this preference was not statistically significant. Geckos from both large and small islands clung better to the tree than to the rock in the laboratory, while those from the mainland clung similarly to both substrates. Geckos collected from trees had longer manual digits and hind limbs. Geckos collected from large and small islands had taller (longer on the dorso-ventral axis; henceforth deeper ) claws. Longer digits and deeper but shorter claws were associated with a better ability to cling to rocks. Our findings suggest that while M. kotschyi is potentially preferentially arboreal, due to the great variation and plasticity it possesses, it can successfully also exploit the habitats available on the smallest, treeless islets in the Aegean Sea. Our study suggests that the dichotomous use of generalist versus specialist in describing species habitat use is oversimplified, and we suggest the use of a generalist specialist gradient instead. © 2021 Oxford University Press. All rights reserved