Armored with skin and bone: A combined histological and μCT‐study of the exceptional integument of the Antsingy leaf chameleon Brookesia perarmata (Angel, 1933)

Pia J Schucht,Benedikt Geier,Frank Glaw,Markus Lambertz,Peter T Rühr

doi:10.1002/jmor.21135

Abstract

Madagascar's endemic ground-dwelling leaf chameleons (Brookesiinae: Brookesia Gray, 1865 + Palleon Glaw, et al., Salamandra, 2013, 49, pp. 237-238) form the sister taxon to all other chameleons (i.e., the Chamaeleoninae). They possess a limited ability of color change, a rather dull coloration, and a nonprehensile tail assisting locomotion in the leaf litter on the forest floor. Most Brookesia species can readily be recognized by peculiar spiky dorsolateral projections ("Rückensäge"), which are caused by an aberrant vertebral structure and might function as body armor to prevent predation. In addition to a pronounced Rückensäge, the Antsingy leaf chameleon Brookesia perarmata (Angel, 1933) exhibits conspicuous, acuminate tubercle scales on the lateral flanks and extremities, thereby considerably enhancing the overall armored appearance. Such structures are exceptional within the Chamaeleonidae and despite an appreciable interest in the integument of chameleons in general, the morphology of these integumentary elements remains shrouded in mystery. Using various conventional and petrographic histological approaches combined with μCT-imaging, we reveal that the tubercle scales consist of osseous, multicusped cores that are embedded within the dermis. Based on this, they consequently can be interpreted as osteoderms, which to the best of our knowledge is the first record of such for the entire Chamaeleonidae and only the second one for the entire clade Iguania. The combination of certain aspects of tissue composition (especially the presence of large, interconnected, and marrow-filled cavities) together with the precise location within the dermis (being completely enveloped by the stratum superficiale), however, discriminate the osteoderms of B. perarmata from those known for all other lepidosaurs.

Highlights

Chameleons as a whole (Squamata: Iguania: Chamaeleonidae) are captivating animals and their exceptional integument in general is morphologically well studied, especially with regard to color change (e.g., Best, 1968; Ligon & McGraw, 2013; Stuart-Fox & Moussalli, 2008; Teyssier, Saenko, Van Der Marel, & Milinkovitch, 2015; van der Hoeven, 1831) and microstructure (e.g., Canham, 1999; Riedel, Böhme, Bleckmann, & Spinner, 2015; Schleich & Kästle, 1985; Spinner, Westhoff, & Gorb, 2013). One of their more unusual clades is represented by the so-called leaf chameleons of the genus Brookesia Gray, 1865, which is endemic to Madagascar (Glaw, 2015) and which together with Palleon Glaw, Hawlitschek, & Ruthensteiner, 2013 forms the Brookesiinae, which in turn comprises the sister taxon to all remaining chameleons (Tolley, Townsend, & Vences, 2013; Townsend & Larson, 2002; Townsend, Vieites, Glaw, & Vences, 2009)
A striking morphological feature of this group concerns a more-orless developed row of spiky projections running along their back. This Brookesia-specific “Rückensäge” (“spinal saw”; Boettger, 1878, 1893) and its underlying peculiar vertebral structure has been subject to several osteological studies, in Brookesia superciliaris (Kuhl, 1820) (Parker & Taylor, 1942; Siebenrock, 1893)
The macroscopic external appearance of the conspicuous putative body armor of Brookesia perarmata has been known since the original description of this species by Angel (1933)

Summary

Introduction

Chameleons as a whole (Squamata: Iguania: Chamaeleonidae) are captivating animals and their exceptional integument in general is morphologically well studied, especially with regard to color change (e.g., Best, 1968; Ligon & McGraw, 2013; Stuart-Fox & Moussalli, 2008; Teyssier, Saenko, Van Der Marel, & Milinkovitch, 2015; van der Hoeven, 1831) and microstructure (e.g., Canham, 1999; Riedel, Böhme, Bleckmann, & Spinner, 2015; Schleich & Kästle, 1985; Spinner, Westhoff, & Gorb, 2013) One of their more unusual clades is represented by the so-called leaf chameleons of the genus Brookesia Gray, 1865, which is endemic to Madagascar (Glaw, 2015) and which together with Palleon Glaw, Hawlitschek, & Ruthensteiner, 2013 forms the Brookesiinae, which in turn comprises the sister taxon to all remaining chameleons (Tolley, Townsend, & Vences, 2013; Townsend & Larson, 2002; Townsend, Vieites, Glaw, & Vences, 2009). The principle aim of the present study was to identify the histological structure and three-dimensional (3D) tissue composition of the different elements of the integumentary armor of this intriguing leaf chameleon

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Conclusion