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Descriptive Skeletal Anatomy of Blommersia Transmarina (Amphibia: Anura: Mantellidae) from the Comoro Islands

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Descriptive Skeletal Anatomy of Blommersia Transmarina (Amphibia: Anura: Mantellidae) from the Comoro Islands Contributions to Zoology 89 (2020) 14-73 CTOZ brill.com/ctoz Descriptive skeletal anatomy of Blommersia transmarina (Amphibia: Anura: Mantellidae) from the Comoro Islands Javier H. Santos-Santos Department of Biogeography and Global Change (BGC-MNCN-CSIC), Museo Nacional de Ciencias Naturales, C/José Gutiérrez Abascal 2, 28006, Madrid, Spain Department of Animal Biology, University of Barcelona, Avenida Diagonal 645, 08028, Barcelona, Spain [email protected] Mireia Guinovart-Castán Department of Biogeography and Global Change (BGC-MNCN-CSIC), Museo Nacional de Ciencias Naturales, C/José Gutiérrez Abascal 2, 28006, Madrid, Spain David R. Vieites Department of Biogeography and Global Change (BGC-MNCN-CSIC), Museo Nacional de Ciencias Naturales, C/José Gutiérrez Abascal 2, 28006, Madrid, Spain [email protected] Abstract Mantellid frogs present an extensive adaptive radiation endemic to Madagascar and Comoros, being the subfamily Mantellinae the most morphologically and ecologically diverse. The Mantellinae present key innovative evolutionary traits linked to their unique reproductive behavior, including the presence of femoral glands and a derived vomeronasal organ. In addition, previous studies pointed to size differ- entiation in playing an important role in species’ dispersal capacities and shaping of their geographic ranges. Despite the high phenotypic variation observed in this clade, to date an exhaustive morphologi- cal analysis of their anatomy has still not been performed, much less in relation to internal structures. Here, we present a comprehensive skeletal description of a mantellid species, Blommersia transmarina, from the island of Mayotte in the Indian Ocean, which has potentially undergone a process of moderate gigantism compared to other Blommersia species. We describe its intraspecific skeletal variation utilizing non-destructive volume renderings from μCT-scans, and characterize the presence of sexual dimorphism and size covariation in skeletal structures. Notably, we found numerous signs of hyperossification, a novel structure for mantellids: the clavicular process, and the presence of several appendicular sesamoids. Our findings suggest that skeletal phenotypic variation in this genus may be linked to biomechanical function for reproduction and locomotion. © SANTOS-SANTOS et al., 2020 | doi:10.1163/18759866-20191405 This is an open access article distributed under the terms of the cc-by 4.0 License. Downloaded from Brill.com10/04/2021 09:02:24AM via free access 204346 Descriptive skeletal anatomy of Blommersia transmarina 15 Keywords Anura: Mantellidae – computed tomography – hyperossifcation – intraspecific variation – osteology – size variation Introduction nauticus and Blommersia transmarina (Glaw et al., 2019). Mayotte consists of a main island, The Mantellidae represents the most species- Maore, and a small island, Pamanzi; with rich and ecologically diverse anuran fam- transmarine colonization having occurred ily endemic to the islands of Madagascar and exclusively on Maore. B. transmarina appears Mayotte (Glaw & Vences, 2007). It is divided to have likely having undergone a process of into three subfamilies: Mantellinae (Laurent, moderate gigantism (Glaw et al., 2019), a com- 1946), Laliostominae (Vences & Glaw, 2001), mon phenomenon in oceanic islands (Daugh- and Boophinae (Vences & Glaw, 2001). Exten- erty et al., 1993; Lomolino, 2005; Li et al., 2011). sive work (Guibé, 1978; Scott, 2005; Glaw & Several recent works studied anatomical Vences, 2006; Vieites et al., 2009) has been car- subsystems of various species within Man- ried out in view of resolving their systematics, tellidae, including external morphology (e.g., biogeography, and phylogenetic relationships Blommersia Vences et al., 2010; Pabijan et al., to elucidate their evolutionary history and 2011; Gephyromantis Scherz et al., 2017a; shed light on the nature of active speciation Guibemantis Vences et al., 2015; Mantidacty- processes. In this respect, variation in body lus Vences et al., 2002; Tysingymantis Glaw size has been found to influence species’ et al., 2006), femoral glands (Vences et al., range sizes and biogeographic setting, linking 2007; Altig, 2008), intercalary elements (Man- smaller body sizes to higher clade diversity zano et al., 2007), etc. However, there is cur- and geographically closer and more fragment- rently no study of skeletal data that makes ed ranges (Wollenberg et al., 2011; Pabijan reference to size differentiation, especially in et al., 2012). view that body size is known to influence dis- The Mantellidae is phylogenetically nested persal and evolutionary rates within the genus within Indian frogs and its most recent com- (Wollenberg et al., 2011; Pabijan et al., 2012). mon ancestor is estimated to have dispersed Since B. transmarina is the largest Blommersia from this landmass and colonized the island species identified to date (Glaw et al., 2019), it of Madagascar in the Early Cretaceous be- constitutes the perfect starting point to set a tween 87–76 Mya (Million years ago) (Crottini base to study the processes of miniaturization et al., 2012; Samonds et al., 2013). In addition, in the internal anatomy of mantellids on the there have been two more recent colonization grounds that miniaturization can lead to re- events by oceanic dispersal that are estimated duced ossification of post-metamorphic skel- to have occurred between 8–6 Mya (Vences et etal elements, hyperossification, and presents al., 2003; Crottini et al., 2012) from mainland more structural trade-offs than enlargement Madagascar to the neighboring island of May- (Hanken, 1993; Yeh, 2002; Hall, 2005; Pérez- otte in the Comoros, 300 km off the northwest Ben et al., 2018). coast of Madagascar, involving Boophinae and Here, we present the first comprehensive Mantellinae members of this family, which skeletal description of a species within the have recently been described as Boophis Mantellidae (but see Guibé, 1978; Scott, 2005), Downloaded from Brill.com10/04/2021 09:02:24AM via free access 204346 16 Santos-Santos et al. elaborating precise anatomical descriptions fixed with cotton and submerged in 70% etha- of all skeletal elements, and define the level of nol within 50 mL polypropylene falcon tubes intraspecific phenotypic variation (n = 10) of before CT-scanning in a Nikon XT H-160 sys- highly variable elements. Anatomical descrip- tem [reconstructed voxel size (μm) = 29.5–42 tions are based on high-resolution rendered (isometric); X-ray (kV) = 53–56; X-ray (μA) = skeletons obtained from μCT (i.e., computed 172–188; Projections = 1800; voxels = 1008] at tomography) volume scans of individuals the internal Service of Non-destructive Tech- recently captured in Mayotte, Comoros. Ap- niques of the MNCN-CSIC. The CT-scans proximations of non-calcified structures were were reconstructed with CT Pro 3D software. inferred from additional CT-scans of stained Individual skeletons were volume rendered specimens (see Santos-Santos, 2019). Descrip- and visualized in Avizo® version 9.2 software tions are made with elements referenced in a with volrenWhite and physics colormaps to primary anterior (rostral) to posterior (cau- observe bone densities. Images were taken dal) axis and a secondary proximal (medial) in perspective mode in Avizo® to capture the to distal (lateral) axis. With this anatomical largest amount of skeletal features in each study we aim to create a reference for future view. Additional CT-scans of priorly soft- comparative studies with other mantellids tissue-stained specimens were performed to species, as well as explore their phenotypic corroborate the position of non-calcified ana- evolutionary processes, including miniatur- tomical elements; these were performed with a ization / size variation in the family. custom setup [reconstructed voxel size (μm) = 30–35 (isometric); X-ray (kV) = 80; X-ray (μA) = 375; Projections = 1801; voxels = 1166] at the Material and methods Center for X-ray Tomography (UGCT) in col- laboration with the Evolutionary Morphol- A total of 10 (five male and five female) adult ogy of Vertebrates Lab of Ghent University, Blommersia transmarina individuals were re- Belgium (see Santos-Santos, 2019). The speci- trieved from the collections at the National men MNCN50446 was used as a reference Museum of Natural History (MNCN-CSIC) for the generalized anatomical description. in Madrid, Spain (table 1). Individuals were The .stl file of its skeletal segmentation is Table 1 Data and external snout–vent length (SVLext) in mm of the Blommersia transmarina individuals used for the current study. Collection n° Field n° Sex SVLext Locality MNCN50430 DRV6835 F 29.28 Mont Choungui MNCN50431 DRV6848 F 26.5 Mont Combani MNCN50432 DRV6805 F 29.13 Mont Combani MNCN50433 DRV6813 F 30.38 Mont Tsapere MNCN50435 DRV6832 M 25.5 Mont Bénara MNCN50436 DRV6833 M 27.5 Mont Bénara MNCN50437 DRV6841 M 24.64 Mont Bénara MNCN50439 DRV6836 M 27 Mont Bénara MNCN50446 DRV6807 M 29 Mont Tsapere N/A DRV6851 F 24.5 Mont Combani Downloaded from Brill.com10/04/2021 09:02:24AM via free access 204346 Descriptive skeletal anatomy of Blommersia transmarina 17 available on the Spanish National Research Results Council (CSIC) repository (https://digital.csic .es/handle/10261/190938). Skull In addition, a total of 123 linear distances There are two types of bone in the cranium: (see Appendix 1) were measured on the ren- endochondral (i.e., develops from osteoblasts dered skeletons of all individuals to obtain within cartilage) and dermal or membranous
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