Osteology of the Asian narrow‐mouth toad Kaloula borealis (Amphibia, Anura, Microhylidae) with comments on its osteological adaptation to fossorial life

Abstract

Osteology of vertebrates plays an indispensable role in taxonomy, form‐function evolution and ecological adaptations. The Asian narrow‐mouth toad genus Kaloula is an interesting group that is known for many species having a fossorial life. However, to date, there has been no comprehensive osteological account of Kaloula. Herein, we present the osteology of K. borealis with the help of micro‐CT scanning and double‐staining technologies, which is the first detailed osteological description of the genus. Osteological comparisons with other members of Microhylinae indicate that K. borealis is characterized by the following traits: skull obviously wider than long; suture between frontoparietals narrow; parasphenoid posterior to vomer; premaxilla, maxilla and vomer edentate; clavicles absent; procoracoids small; omosternum and sternum cartilaginous; crista femoris present and large; femur longer than tibiofibula; prehallux including one element. Remarkably, the species possesses a series of osteological specializations that probably are adaptations for the hindlimbs‐first burrowing and a fossorial life, including stout hindlimb, robust crista femoris, tibiofibula shorter than femur, enlarged prehallux, long anterior ramus of the pterygoid and branched bronchial processes of the cricoid. These findings will contribute to the systematics of microhylids and evolutionary interpretations of the osteological adaptation to fossorial life.

Impact of the Miocene orogenesis on Kaloula spp. radiation and implication of local refugia on genetic diversification

“…For instance, the digging strategy displayed by K. borealis as a specialization to temperate climate (Boring & Liu 1937) resulted in changes to its osteological structure such as wider skull and longer femur, in comparison to Microhylinae from lower latitude (Zhang et al . 2020).…”

“…In addition, K. borealis individuals that dispersed to northern latitudes are likely to have become locally adapted, and diverged from their tropical biogeographical origin (Dutta et al 2004). For instance, the digging strategy displayed by K. borealis as a specialization to temperate climate (Boring & Liu 1937) resulted in changes to its osteological structure such as wider skull and longer femur, in comparison to Microhylinae from lower latitude (Zhang et al 2020).…”

Consequences of parallel miniaturisation in Microhylinae (Anura, Microhylidae), with the description of a new genus of diminutive South East Asian frogs

“…Terminologies used to describe the shape of terminal phalanges (simple, knobbed, T-shaped, and Y-shaped) followed Parker (1927) and . Comparative morphological and osteological data for other genera were taken from a number of revisions of Microhylinae (Parker 1934;Boring and Liu 1937;Duellman and Trueb 1986;Dubois 1987;Fei et al 2009;McPartlin 2010;Chandramouli and Dutta 2015;Poyarkov et al 2018b;Zhang et al 2020;Suwannapoom et al 2020). External morphology was described following Poyarkov et al (2014Poyarkov et al ( , 2019; mensural data were taken with a Mitutoyo dial caliper (Mitutoyo Corporation, Kawasaki, Japan) to the nearest 0.1 mm.…”

“…In his review of Asian microhylid taxa, Parker only focused on the most variable parts of the skeleton (such as the palatine region and pectoral girdle), but description of generalized osteology generally was not included (Parker 1934). In recent years skeletal morphology of only a few species in Microhylinae has been described in substantial detail, including the genus Uperodon (Chandramouli and Dutta 2015;Garg et al 2018), Kaloula borealis (Boring and Liu 1937;Zhang et al 2020), and Glyphoglossus guttulatus (McPartlin 2010).…”

Digital dissection of the head of the frogs Calyptocephalella gayi and Leptodactylus pentadactylus with emphasis on the feeding apparatus

“…Some exemplary studies include cranial anatomy of tadpoles (Haas et al 2014 ), tongue musculature and surface structure (Kleinteich & Gorb, 2015a , 2015b ), comparison of appendicular skeleton in recent and fossil frogs (Matthews & du Plessis, 2016 ) and myoanatomical reconstructions of Xenopus laevis (Porro & Richards, 2017 ). Recent studies focused on the osteology of a fossorial frog (Zhang et al 2019 ), humerus of burrowing frogs (Keeffe & Blackburn, 2020 ) and the description of the pelvic and hind limb skeleton in relation to frog locomotion (Buttimer et al, 2020 ). These fragmentary datasets call for a more holistic digital dissection that includes mineralized (bone) and unmineralized (cartilage) skeletal elements, musculature and associated structures.…”