Burrowing with a kinetic snout in a snake (Elapidae: Aspidelaps scutatus)

Of the few elongate, fossorial vertebrates that have been examined for their burrowing mechanics, all were found to use an akinetic, reinforced skull to push into the soil, powered mostly by trunk muscles. Reinforced skulls were considered essential for head‐first burrowing. In contrast, I found that the skull of the fossorial shield‐nosed cobra (Aspidelaps scutatus ) is not reinforced and retains the kinetic potential typical of many non‐fossorial snakes. Aspidelaps scutatus burrows using a greatly enlarged rostral scale that is attached to a kinetic snout that is independently mobile with respect to the rest of the skull. Two mechanisms of burrowing are used: (1) anteriorly directed head thrusts from a loosely bent body that is anchored against the walls of the tunnel by friction, and (2) side‐to‐side shovelling using the head and rostral scale. The premaxilla, to which the rostral scale is attached, lacks any direct muscle attachments. Rostral scale movements are powered by, first, retractions of the palato‐pterygoid bar, mediated by a ligament that connects the anterior end of the palatine to the transverse process of the premaxilla and, second, by contraction of a previously undescribed muscle slip of the m. retractor pterygoidei that inserts on the skin at the edge of the rostral scale. In derived snakes, palatomaxillary movements are highly conserved and power prey capture and transport behaviors. Aspidelaps scutatus has co‐opted those mechanisms for the unrelated function of burrowing without compromising the original feeding functions, showing the potential for evolution of functional innovations in highly conserved systems.     

A multilocus phylogeny of Malagasy scincid lizards elucidates the relationships of the fossorial genera Androngo and Cryptoscincus

A phylogeny for 29 species of scincine lizards from Madagascar, based on 3693 bp of six mitochondrial and five nuclear genes, revealed multiple parallel evolution of adaptations for a burrowing life, and unexpected relationships of the monotypic genera Androngo and Cryptoscincus. Androngo trivittatus was sister to Pygomeles braconnieri, and Cryptoscincus minimus was deeply nested within the genus Paracontias, all of these being fossorial taxa of elongated bodies and partly or fully reduced limbs. To account for these results, we place Cryptoscincus as a junior synonym of Paracontias, and discuss possible taxonomic consequences that may affect the status of Androngo, once additional data become available.     

A new species of the genus Mekongina Fowler, 1937 (Cypriniformes: Cyprinidae) from South China

A new species of cyprinid fish, Mekongina lancangensis, is described from the upper Mekong River drainage in Southern Yunnan, China. The new species is distinguished from the other species of Mekongina occurring in the lower Mekong River drainage by possessing the following combination of characters: one pair of rostral barbels; two rows of tubercles irregularly scattered on the snout and cheeks, with two enlarged tubercles present at each side of anterior of the snout; 19–27 rostral marginal lappets; lateral line with 38–41 scales; 5·5 or 6·5 scales in transverse series from dorsal‐fin origin to lateral line; 18–20 circumpeduncular scales; snout length 31·9–36·9% head length; tip of depressed anal‐fin rays extending to the caudal‐fin base.     

Ontogenetic allometry constrains cranial shape of the head‐first burrowing worm lizard Cynisca leucura (Squamata: Amphisbaenidae)

Amphisbaenians are fossorial, predominantly limbless squamate reptiles with distinct cranial shapes corresponding to specific burrowing behaviors. Due to their cryptic lifestyles and the scarcity of museum specimens, little is known of their intraspecific variation, particularly regarding cranial osteology. This represents a critical lack of information, because the majority of morphological investigations of squamate relationships are based on cranial characters. We investigated cranial variation in the West African Coast Worm Lizard Cynisca leucura, a round‐headed member of the Amphisbaenidae. Using geometric morphometric analyses of three‐dimensional computed tomographic scans, we found that cranial osteology of C. leucura is highly conserved, with the majority of shape changes occurring during growth as the cranium becomes more slender and elongate, accompanied by increasing interdigitation among the dermal roofing bones. Elements of the ventral portion of the cranium remain loosely connected in adults, possibly as a protective mechanism against repeated compression and torsion during burrow excavation. Intraspecific variation was strongly correlated with size change from juveniles to adults, indicating a dominant role of ontogenetic allometry in determining cranial shape. We found no evidence of sexual dimorphism, either during growth or among adults. Given the fossorial habits of C. leucura, we hypothesize that cranial allometry is under strong stabilizing selection to maintain adequate proportions for head‐first digging, thereby constraining the ability of individuals to respond to differing selection pressures, including sexual selection and variation in diet or microhabitat. For species in which digging imposes less mechanical stress (e.g., in softer sand), allometric associations during growth may be weakened, allowing changes to the ontogenetic trajectory and subsequent morphological traits. Such developmental dissociation between size and shape, known as heterochrony, may also be implicit in the evolution of the other amphisbaenian cranial shapes (shovel, spade, and keel), which may themselves be functionally adapted for their respective burrowing techniques. J. Morphol. 277:1159–1167, 2016. © 2016 Wiley Periodicals, Inc.     

Skeletal development in the fossorial gymnophthalmids Calyptommatus sinebrachiatus and Nothobachia ablephara

The development of the cartilaginous and bony elements that form the skull and axial and appendicular skeleton is described in detail for the post-ovipositional embryonic development of the fossorial gymnophthalmid species Calyptommatus sinebrachiatus and Nothobachia ablephara. Both species have a snake-like morphology, showing an elongated body and reduced or absent limbs, as well as modifications in skull bones for burrowing, such as complex articulation surfaces and development of bony extensions that enclose and protect the brain. Similar morphological changes have originated independently in several squamate groups, including the one that led to the snake radiation. This study characterizes the patterns of chondrogenesis and osteogenesis, with special emphasis on the features associated with the burrowing habit, and may be used for future comparative analyses of the developmental patterns involved in the origin of the convergent serpentiform morphologies.     

Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships

The affinities of three problematic groups of elongate, burrowing reptiles (amphisbaenians, dibamids and snakes) are reassessed through a phylogenetic analysis of all the major groups of squamates, including the important fossil taxa Sineoamphisbaena, mosasauroids and Pachyrhachis; 230 phylogenetically informative osteological characters were evaluated in 22 taxa. Snakes (including Pachyrhachis) are anguimorphs, being related firstly to large marine mosasauroids, and secondly to monitor lizards (varanids). Scincids and cordylids are not related to lacertiforms as previously thought, but to anguimorphs. Amphisbaenians and dibamids are closely related, and Sineoamphisbaena is the sister group to this clade. The amphisbaenian-dibamid-Sineoamphisbaena clade, in turn, is related to gekkotans and xantusiids. When the fossil taxa are ignored, snakes, amphisbaenians and dibamids form an apparently well-corroborated clade nested within anguimorphs. However, nearly all of the characters supporting this arrangement are correlated with head-first burrowing (miniaturization, cranial consolidation, body elongation, limb reduction), and invariably co-occur in other tetrapods with similar habits. These characters are potentially very misleading because of their sheer number and because they largely represent reductions or losses. It takes very drastic downweighting of these linked characters to alter tree topology: if fossils are excluded from the analysis, a (probably spurious) clade consisting of elongate, fossorial taxa almost always results. These results underscore the importance of including all relevant taxa in phylogenetic analyses. Inferring squamate phylogeny depends critically on the inclusion of certain (fossil) taxa with combinations of character states that demonstrate convergent evolution of the elongate, fossorial ecomorph in amphisbaenians and dibamids, and in snakes. In the all-taxon analysis, the position of snakes within anguimorphs is more strongly-corroborated than the association of amphisbaenians and dibamids with gekkotans. When the critical fossil taxa are deleted, snakes ‘attract’ the amphisbaenian-dibamid clade on the basis of a suite of correlated characters. While snakes remain anchored in anguimorphs, the amphisbaenian-dibamid clade moves away from gekkotans to join them. Regardless of the varying positions of the three elongate burrowing taxa, the interrelationships between the remaining limbed squamates (‘lizards’) are constant; thus, the heterodox affinities of scincids, cordylids, and xantusiids identified in this analysis appear to be robust. Finally, the position of Pachyrhachis as a basal snake rather than (as recently suggested) a derived snake is supported on both phylogenetic and evolutionary grounds.     

The molecular evolutionary tree of lizards,snakes, and amphisbaenians

Squamate reptiles (lizards, snakes, amphisbaenians) number approximately 8200 living species and are a major component of the world's terrestrial vertebrate diversity. Recent molecular phylogenies based on protein-coding nuclear genes have challenged the classical, morphology-based concept of squamate relationships, requiring new classifications, and drawing new evolutionary and biogeographic hypotheses. Even the key and long-held concept of a dichotomy between iguanians (～1470 sp.) and scleroglossans (all other squamates) has been refuted because molecular trees place iguanians in a highly nested position. Together with snakes and anguimorphs, iguanians form a clade – Toxicofera – characterized by the presence of toxin secreting oral glands and demonstrating a single early origin of venom in squamates. Consequently, neither the varanid lizards nor burrowing lineages such as amphisbaenians or dibamid lizards are the closest relative of snakes. The squamate timetree shows that most major groups diversified in the Jurassic and Cretaceous, 200–66 million years (Myr) ago. In contrast, five of the six families of amphisbaenians arose during the early Cenozoic, ～60–40 Myr ago, and oceanic dispersal on floating islands apparently played a significant role in their distribution on both sides of the Atlantic Ocean. Among snakes, molecular data support the basic division between the small fossorial scolecophidians (～370 sp.) and the alethinophidians (all other snakes, ～2700 sp.). They show that the alethinophidians were primitively macrostomatan and that this condition was secondarily lost by burrowing lineages. The diversification of alethinophidians resulted from a mid-Cretaceous vicariant event, the separation of South America from Africa, giving rise to Amerophidia (aniliids and tropidophiids) and Afrophidia (all other alethinophidians). Finally, molecular phylogenies have made it possible to draw a detailed evolutionary history of venom among advanced snakes (Caenophidia), a key functional innovation underlying their radiation (～2500 sp.). To cite this article: N. Vidal, S.B. Hedges, C. R. Biologies 332 (2009).     

Fine‐ and Broad‐Scale Approaches to Understanding the Evolution of Aggression in Crickets

Male field crickets frequently engage in agonistic contests to establish dominance in social interactions and gain access to mate attraction territories. Crickets (Orthoptera: Gryllidae) are often used as a model taxon to study aggression, but limited documentation of aggression in some cricket species hinders our understanding of its evolutionary costs and benefits. Our study investigated cricket aggression at two scales: the within‐species scale for two cricket species, Gryllus assimilis and G. veletis, whose aggression had not been adequately documented and the among‐species scale to detect evolutionary patterns in species’ levels of aggression. In both G. veletis and G. assimilis, winners spent more time being aggressive than losers, but they were not larger or heavier. Collectively, our results reveal that G. veletis males are more aggressive than G. assimilis. Male G. veletis had higher aggression scores that male G. assimilis. The majority of G. veletis contests escalated to grappling (a highly aggressive behavior), while less than one quarter of G. assimilis contests escalated to grappling. Further, G. veletis males transitioned between two of the most aggressive behaviors most often while G. assimilis transitioned between two of the least aggressive behaviors most often. We integrate this new information on aggression for G. assimilis and G. veletis with previously documented aggression data for many cricket species to investigate aggression in a broader evolutionary context than previously possible. Within a phylogenetic context, we test the hypothesis that species whose males use burrows from which to call and attract females are more aggressive than species with non‐burrowing males. We found evidence consistent with this hypothesis; species with burrowing males tended to be more aggressive than species with non‐burrowing males. Together, our study provides fine‐scale understanding of aggression in two cricket species and broad‐scale evolutionary context for aggression across cricket species.     

Burrow structure and foraging costs in the fossorial rodent,Thomomys bottae

Summary A model for calculating the energy cost of burrowing by fossorial rodents is presented and used to examine the energetics of foraging by burrowing. The pocket gopher Thomomys bottae (Rodentia: Geomyidae) digs burrows for access to food. Feeding tunnels of Thomomys are broken into segments by laterals to the surface that are used to dispose of excavated soil. Energy cost of burrowing depends on both soil type and on burrow structure, defined by the length of burrow segments, angle of ascent of laterals, depth of feeding tunnels, and burrow diameter. In a desert scrub habitat, Thomomys adjust burrow segment length to minimize cost of burrowing. Observed segment lengths (mean=1.33 m) closely approximate the minimum-cost segment length of 1.22 m. Minimizing energy expended per meter of tunnel constructed maximizes efficiency of foraging by burrowing in the desert scrub. Burrow diameter and cost of burrowing increase with body size, while benefits do not, so foraging by burrowing becomes less enconomical as body size increases. Maximum possible body size of fossorial mammals depends on habitat productivity and energy cost of burrowing in local soils.     

Extraordinary fossorial adaptations in the oligocene palaeanodonts Epoicotherium and Xenocranium (Mammalia)

New fossils of the rare Oligocene mammals Xenocranium and Epoicotherium add information on their skulls and provide the first information on their postcranial skeletons. These epoicotheres, the latest surviving palaeanodonts, have numerous fossorial adaptations and must have been predominantly subterranean. Their skeletal specializations are similar to, and equal or surpass in degree of development, those of most living fossorial mammals. Principal modifications of the skull are the expanded, domed occiput with broad lambdoid crests, hypertrophy of the malleus-incus and related changes in other ear components, reduced eyes, and (in Xenocranium) a flaring, upturned, spatulate snout. The neck was strengthened by synostosis of the 2nd through 5th cervical vertebrae. The forelimb elements have exaggerated crests, processes, and fossae for muscles used in digging or in stabilizing certain joints. The scapula has a high, stout spine with bifid acromion, a “secondary spine,” and an expanded postscapular fossa for attachment of the teres major muscle. The humerus has an elongate pectoral crest, large lesser tuberosity, long entepicondyle, and large hooklike supinator crest. The enormous incurved olecranon process of the ulna provided insertion for the massive triceps and origin for the carpal and digital flexors, and the latter gained mechanical advantage by incorporating in its tendon a large carpal sesamoid. In the greatly shortened hand, digit three is largest, with its metacarpal and proximal phalanx fused and its claw-bearing ungual-phalanx very large. These traits indicate that Xenocranium and Epoicotherium were among the most specialized “rapid-scratch” diggers ever to evolve. Their remarkable convergence to chrysochlorids reflects a similar mode of digging, with extensive use of the snout for loosening and lifting soil when making shallow foraging burrows. For deeper burrowing, the forelimbs probably loosened the soil while the rear limbs moved it behind. Like many extant subterranean mammals, Xenocranium and Epoicotherium were essentially sightless, but they were specialized for low frequency sound reception. Their extinction may have been due to a combination of environmental change and competition with other fossorial animals, such as proscalopine insectivores and rhineurid amphisbaenians.     

Landscape ecology of the burrowing bettong: Warren distribution and patch dynamics in semiarid eastern Australia

Abstract In arid and semiarid Australia fossorial vertebrates have been a major component of the soil biota mediating many fundamental landscape processes. However, many species such as the burrowing bettong (Bettongia lesueur) have become seriously depleted following European pastoral settlement. As ‘landscape engineers’, they were responsible for creating and maintaining a high degree of surface heterogeneity that promoted a diverse and productive herbaceous understorey, particularly in ‘hard‐red’ communities dominated by mulga (Acacia aneura). While their regional extinction has had major impacts by contributing to desertification and loss of biodiversity, relict warrens ‘engineered’ by B. lesueur still remain in certain ecosystems and despite continual weathering, contribute significantly to herbage productivity and species diversity. This paper details the results obtained from a number of field studies aimed at determining the distribution of relict warrens at contrasting scales and their influence on landscape patch dynamics resulting from their impacts on soil nutrients, herbage composition and herbivory. Finally, the conservation implications following the continental extinction of this species and the resulting loss of fundamental ecosystem services, as well as cultural values, are discussed in the context of future re‐introduction efforts.     

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.     

Moringua edwardsi (Moringuidae: Anguilliformes): Cranial specialization for head‐first burrowing?

The order Anguilliformes forms a natural group of eel-like species. Moringua edwardsi (Moringuidae) is of special interest because of its peculiar fossorial lifestyle: this species burrows head-first. Externally pronounced morphological specializations for a fossorial lifestyle include: reduced eyes, lack of color, low or absent paired vertical fins, elongated, cylindrical body, reduced head pores of the lateral line system, etc. Many fossorial amphibians, reptiles, and even mammals have evolved similar external specializations related to burrowing. The present study focuses on osteological and myological features of M. edwardsi in order to evaluate the structural modifications that may have evolved as adaptations to burrowing. Convergent evolutionary structures and possible relations with head-first burrowing, miniaturization, feeding habits, etc., were investigated. Body elongation, reduction of the eyes, modified cranial lateral line system, and modified skull shape (pointed though firm) can be considered specializations for head-first burrowing. Hyperossification can probably be regarded more as a specialization to both head-first burrowing and feeding, even though an impact of miniaturization cannot be excluded. Hypertrophied adductor mandibulae muscles and the enlarged coronoid process can be associated with both feeding requirements (it enhances bite forces necessary for their predatory behavior) and with a burrowing lifestyle, as well as miniaturization.     

Strange bedfellows: Mammal burrow disturbances may provide thermoregulatory microsites for fossorial reptiles in densely vegetated dunes

Burrow excavation by mammals generates heterogeneity within landscapes. Globally, these disturbances are known to provide significant ecosystem benefits. Most investigations of native Australian burrowing mammal disturbances has focused on the role of burrows in landscape function and interspecific thermal refugia. Herein, we present a novel observation of the fossorial skink Lerista bougainvillii utilizing burrow mounds of the common wombat (Vombatus ursinus) for possible thermoregulatory gains. In the early morning, when thermoregulatory opportunities were limited, L. bougainvillii were detected in mounds that appeared hotter than adjoining vegetation. These observations suggest that in densely vegetated habitats thermal heterogeneity caused by mammal burrows may offer important thermoregulatory opportunities for fossorial species with limited climbing capacity.     

Systematics of limbless scincid lizards from northern Madagascar: morphology,phylogenetic relationships and implications for classification (Squamata: Scincidae)

We report on the rediscovery of two limbless scincid species, Paracontias rothschildi Mocquard, 1905 and Paracontias minimus (Mocquard, 1906), after more than a century. The two species were found in syntopy in sandy soils of Forêt d’Orangea, Antsiranana Province, northern Madagascar, which probably constitutes the respective type locality and confirms the species’ Malagasy origin. Both taxa are redescribed based on newly collected material, and compared to other Malagasy species. In addition, Paracontias fasika n. sp. is described from the same locality and habitat. We discuss the taxonomy and origin of all three species and provide preliminary data on their natural history. Molecular relationships among seven Paracontias species are compared to external morphological characters formerly used in skink systematics. Our results indicate that morphology in fossorial skinks is well suited to distinguish species, but is of rather limited value to elucidate phylogenetic relationships. Similarities between these skinks in external characters apparently are the result of convergent evolution due to parallel selective pressures.     

Balitora eddsi,a new species of hillstream loach (Ostariophysi: Balitoridae) from Nepal

A new species of hillstream loach Balitora eddsi is described from the Karnali River drainage in south‐western Nepal. The new species is distinguished from all its congeners by possessing the following combination of characters: six to seven unbranched pectoral‐fin rays, pelvic‐fin length 12–14% standard length (L_S), dorsal surface without circular or irregular shaped dark blotches, snout pointed, median lobe between anterior rostral barbels pointed posteriorly, dorsal‐fin origin posterior to pelvic‐fin origin, lateral line scales 66–67, caudal peduncle length 22–23·2% L_S, caudal peduncle depth 4·1–4·2 times its length.