Whether the forelimb-digging apparatus of tooth-digging subterranean mammals has similar levels of specialization as compared to scratch-diggers is still unknown. We assessed the scapular morphology and forelimb musculature of all four solitary African mole rats (Bathyergidae): two scratch-diggers, Bathyergus suillus and Bathyergus janetta, and two chisel-tooth diggers, Heliophobius argenteocinereus and Georychus capensis. Remarkable differences were detected: Bathyergus have more robust neck, shoulder, and forearm muscles as compared to the other genera. Some muscles in Bathyergus were also fused and often showing wider attachment areas to bones, which correlate well with its more robust and larger scapula, and its wider and medially oriented olecranon. This suggests that shoulder, elbow, and wrist work in synergy in Bathyergus for generating greater out-forces and that the scapula and proximal ulna play fundamental roles as pivots to maximize and accommodate specialized muscles for better (i) glenohumeral and scapular stabilization, (ii) powerful shoulder flexion, (iii) extension of the elbow and (iv) flexion of the manus and digits. Moreover, although all bathyergids showed a similar set of muscles, Heliophobius lacked the m. tensor fasciae antebrachii (aiding with elbow extension and humeral retraction), and Heliophobius and Georychus lacked the m. articularis humeri (aiding with humeral adduction), indicating deeper morphogenetic differences among digging groups and suggesting a relatively less specialized scratch-digging ability. Nevertheless, Heliophobius and Bathyergus shared some similar adaptations allowing scratch-digging. Our results provide new information about the morphological divergence within this family associated with the specialization to distinct functions and digging behaviors, thus contributing to understand the mosaic of adaptations emerging in phylogenetically and ecologically closer subterranean taxa. This and previous anatomical studies on the Bathyergidae will provide researchers with a substantial basis on the form and function of the musculoskeletal system for future kinematic investigations of digging behavior, as well as to define potential indicators of scratch-digging ability.

Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic

Mammal Research Institute Department of Zoology and Entomology University of Pretoria Pretoria South Africa

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Acuña, F. , Sidorkewicj, N.S. , Popp, A.I. & Casanave, E.B. (2017) A geometric morphometric study of sex differences in the scapula, humerus and ulna of Chaetophractus villosus (Xenarthra, Dasypodidae). Iheringia Série Zoologia, 107, e2017010.

Adobe Inc . (2015) Adobe Photoshop. Available from: https://www.adobe.com/products/photoshop.html

Böhmer, C. , Theil, J.‐C. , Fabre, A.‐C. & Herrel, A. (2021) Atlas of terrestrial mammal limbs, 1st edition. Boca Raton, FL: CRC Press.

Bennett, N.C. & Faulkes, C.G. (2000) African mole rats: ecology and eusociality. Cambridge, UK: Cambridge University Press.

Bennett, N.C. , Faulkes, C.G. , Hart, L. & Jarvis, J. (2009) Bathyergus suillus (Rodentia: Bathyergidae). Mammalian Species, 828, 1–7.

Bryja, J. , Konvičková, H. , Bryjová, A. , Mikula, O. , Makundi, R. , Chitaukali, W.N. et al. (2018) Differentiation underground: range‐wide multilocus genetic structure of the silvery mole‐rat does not support current taxonomy based on mitochondrial sequences. Mammalian Biology, 93, 82–92.

Cain, B.W. , Reynolds, T. & Sarko, D.K. (2019) Superficial, suprahyoid, and infrahyoid neck musculature in naked mole‐rats (Heterocephalus glaber): relative size and potential contributions to independent movement of the lower incisors. Journal of Morphology, 280, 1185–1196. PubMed

Cox, P.G. & Faulkes, C.G. (2014) Digital dissection of the masticatory muscles of the naked mole‐rat, Heterocephalus glaber (Mammalia, Rodentia). PeerJ, 2, e448. PubMed PMC

Cox, P.G. , Faulkes, C.G. & Bennett, N.C. (2020) Masticatory musculature of the African mole‐rats (Rodentia: Bathyergidae). PeerJ, 8, e8847. Available from: 10.7717/peerj.8847 PubMed DOI PMC

Cuthbert, K. (1975) Burrowing and the associated modifications in the mole‐rats Bathyergus suillus and Georychus capensis ‐ a comparative study. Cape Town, South Africa: Zoology Honours Project, University of Cape Town.

Doubell, N.S. , Sahd, L. & Kotzé, S.H. (2020) Comparative forelimb morphology of scratch‐digging and chisel‐tooth digging African mole‐rat species. Journal of Morphology, 281, 1029–1046. PubMed

Ercoli, M.D. , Álvarez, A. , Stefanini, M.I. , Busker, F. & Morales, M.M. (2015) Muscular anatomy of the forelimbs of the lesser grison (Galictis cuja), and a functional and phylogenetic overview of Mustelidae and other Caniformia. Journal of Mammalian Evolution, 22, 557–591.

Fernández, M.E. , Vassallo, A.I. & Zárate, M. (2000) Functional morphology and palaeobiology of the Pliocene rodent Actenomys (Caviomorpha: Octodontidae): the evolution to a subterranean mode of life. Biological Journal of the Linnean Society of London, 71, 71–90.

Fischer, M.S. , Schilling, N. , Schmidt, M. , Haarhaus, D. & Witte, H. (2002) Basic limb kinematics of small therian mammals. Journal of Experimental Biology, 205, 1315–1338. PubMed

Fournier, M. , Hautier, L. & Gomes Rodrigues, H. (2021) Evolution towards Fossoriality and morphological convergence in the skull of Spalacidae and Bathyergidae (Rodentia). Journal of Mammalian Evolution, 28, 979–993.

Gambaryan, P.P. & Gasc, J.‐P. (1993) Adaptive properties of the musculoskeletal system in the mole‐rat Myospalax myospalax (Marnmalia, Rodentia), cinefluorographical, anatomical and biomechanical analyses of the burrowing. Zoologische Jahrbuch, Anatomie, 123, 363–401.

Gambaryan, P.P. , Zherebtsova, O.V. & Perepelova, A.A. (2013) Comparative analysis of forelimb musculature in Laonastes aenigmamus (Rodentia: Diatomyidae). Proceedings of the Zoological Institute RAS, 317(3), 226–245.

García‐Esponda, C.M. , Calanoce, A.R. & Candela, A.M. (2021) Brachiocephalic muscular arrangements in cavioid rodents (Caviomorpha): a Functional, anatomical, and evolutionary study. Journal of Mammalian Evolution, 28, 529–541.

Gasse, H. , Van Den Broeck, W. , Egerbacher, M. , Staszyk, C. , Budras, K.‐D. , Constantinescu, G.M. et al. (2017) Nomina Anatomica Veterinaria, 6th edition. Hanover: International Committee on Veterinary Gross Anatomical Nomenclature.

Genelly, R.E. (1965) Ecology of the common mole‐rat (Cryptomys hottentotus) in Rhodesia. Journal of Mammalogy, 46, 647–665.

Gomes Rodrigues, H. , Šumbera, R. & Hautier, L. (2016) Life in burrows channelled the morphological evolution of the skull in rodents: the case of African mole‐rats (Bathyergidae, Rodentia). Journal of Mammalian Evolution, 23, 175–189. Available from: 10.1007/s10914-015-9305-x DOI

Gomes Rodrigues, H. , Šumbera, R. , Hautier, L. & Herrel, A. (2023) Digging up convergence in fossorial rodents: insights into burrowing activity and Morpho‐functional specializations of the masticatory apparatus. In: Bels, V.L. & Russell, A.P. (Eds.) Convergent Evolution. Springer, Cham: Fascinating Life Sciences.

Greene, E.C. (1935) The anatomy of the rat. Transactions of the American Philosophical Society, 27, 1–370.

Hamilton, W.J., Jr. (1928) Heterocephalus, the remarkable African burrowing rodent. The Museum of the Brooklyn Institute of Arts and Sciences, 3(5), 173–191.

Herbst, M. & Bennett, N.C. (2006) The burrow architecture and burrowing dynamics of the endangered Namaqua dune mole‐rat, Bathyergus janetta (Rodentia: Bathyergidae). Journal of Zoology, 270, 420–428.

Hildebrand, M. (1985) Digging of quadrupeds. In: Hildebrand, M., Bramble, D., Liem, K. & Wake, D.B. (Eds.) Functional vertebrate morphology. Massachusetts and London: The Belknap Press of Harvard University Press, pp. 89–109.

Hill, J.E. (1937) Morphology of the pocket gopher mammalian genus Thomomys, Vol. 42. Berkeley: University of California Publications in Zoology, pp. 81–171.

Hite, N.J. , Germain, C. , Cain, B.W. , Sheldon, M. , Perala, S.S.N. & Sarko, D.K. (2019) The better to eat you with: bite force in the naked mole‐rat (Heterocephalus glaber) is stronger than predicted based on body size. Frontiers in Integrative Neuroscience, 13, 70. PubMed PMC

Holliger, C.D. (1916) Anatomical adaptations in the thoracic limb of the California pocket gopher and other rodents. Zoology, University of California Publications, 13, 447–494.

Howell, B. (1965) Speed in mammals, their specialization for running and leaping. New York and London: Hafner Publishing Company.

Jarvis, J. & Sale, J. (1971) Burrowing and burrow patterns of east African mole‐rats Tachyoryctes, Heliophobius and Heterocephalus . Journal of Zoology, 163, 451–479.

Jenkins, P.A. & Weijs, W.A. (1979) The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). Journal of Zoology, 188, 379–410.

Klingener, D. (1964) The comparative myology of four dipodoid rodents (Genera Zapus, Napaeozapus, Sicista, and Jaculus). Miscellaneous Publications, Museum of Zoology, University of Michigan, 124, 1–100.

Klingener, D. (1970) Superficial Facial Musculature of Aplodontia. Journal of Mammalogy, 51(1), 35–41.

Kraus, A. , Lövy, M. , Mikula, O. , Okrouhlík, J. , Bennett, N.C. , Herrel, A. et al. (2022) Bite force in the strictly subterranean rodent family of African mole‐rats (Bathyergidae): the role of digging mode, social organization and ecology. Functional Ecology, 36, 2344–2355.

Lövy, M. , Šklíba, J. , Burda, H. , Chitaukali, W.N. & Šumbera, R. (2012) Mole‐rat habitat characteristics. Journal of Zoology, 286, 145–153.

Lehmann, W.H. (1963) The forelimb architecture of some fossorial rodents. Journal of Morphology, 113, 59–76. PubMed

Lessa, E.P. & Stein, B.R. (1992) Morphological constraints in the digging apparatus of pocket gophers (Mammalia, Geomyidae). Biological Journal of the Linnean Society, 47(4), 439–453.

Marcy, A.E. , Hadly, E.A. , Sherratt, E. , Garland, K. & Weisbecker, V. (2016) Getting a head in hard soils: convergent skull evolution and divergent allometric patterns explain shape variation in a highly diverse genus of pocket gophers (Thomomys). BMC Evolutionary Biology, 16, 207. PubMed PMC

Marshall, S.K. , Superina, M. , Spainhower, K.B. & Butcher, M.T. (2021) Forelimb myology of armadillos (Xenarthra: Cingulata, Chlamyphoridae): anatomical correlates with fossorial ability. Journal of Anatomy, 238, 551–575. PubMed PMC

McIntosh, A.F. & Cox, P.G. (2016a) Functional implications of craniomandibular morphology in African mole ‐rats (Rodentia: Bathyergidae). Biological Journal of the Linnean Society, 117, 447–462.

McIntosh, A.F. & Cox, P.G. (2016b) The impact of gape on the performance of the skull in chisel‐tooth digging and scratch digging mole‐rats (Rodentia: Bathyergidae). Royal Society Open Science, 3, 160568. PubMed PMC

Miles, S.Τ. (1941) The shoulder anatomy of the armadillo. Journal of Mammalogy, 22, 157–169.

Milne‐Edwards, H. , Huet, L. , Mesnel, A. , Milne‐Edwards, A. & Severeyns, G. (1868) Recherches pour servir à l’histoire naturelle des mammifères : comprenant des considérations sur la classification de ces animaux. Available from: 10.5962/bhl.title.59889 DOI

Montoya‐Sanhueza, G. , Bennett, N.C. , Chinsamy, A. & Šumbera, R. (2022) Functional anatomy and disparity of the postcranial skeleton of African mole‐rats (Bathyergidae). Frontiers in Ecology and Evolution, 10, 857474. Available from: 10.3389/fevo.2022.857474 DOI

Montoya‐Sanhueza, G. , Šaffa, G. , Šumbera, R. , Chinsamy, A. , Jarvis, J.U.M. & Bennett, N.C. (2022) Fossorial adaptations in African mole‐rats (Bathyergidae) and the unique appendicular phenotype of naked mole‐rats. Communications Biology, 5, 526. PubMed PMC

Montoya‐Sanhueza, G. , Šumbera, R. , Bennett, N.C. & Chinsamy, A. (2022) Developmental plasticity in the ossification of the proximal femur of Heterocephalus glaber (Bathyergidae, Rodentia). Journal of Mammalian Evolution, 29, 663–675.

Montoya‐Sanhueza, G. , Wilson, L.A.B. & Chinsamy, A. (2019) Postnatal development of the largest subterranean mammal (Bathyergus suillus): Morphology, osteogenesis, and modularity of the appendicular skeleton. Developmental Dynamics, 248, 1101–1128. PubMed

Moore, A.L. , Budny, J.E. , Russell, A.P. & Butcher, M.T. (2013) Architectural specialization of the intrinsic thoracic limb musculature of the American badger (Taxidea taxus). Journal of Morphology, 274(1), 35–48. PubMed

Morgan, C.C. (2009) Geometric morphometrics of the scapula of South American caviomorph rodents (Rodentia: Hystricognathi): form, function and phylogeny. Mammalian Biology, 74, 497–506.

Morgan, C.C. (2015) The postcranial skeleton of caviomorphs: morphological diversity, adaptations and patterns. Ch 5. SAREM Series A ‐ Mammalogical Research, 1, 167–198.

Mpagike, F.H. & Makungu, M. (2023) Osteology and radiographic anatomy of the thoracic limb of the greater cane rat (Thryonomys swinderianus). Anatomia, Histologia, Embryologia, 52(3), 393–402. PubMed

Nakai, D. & Fujiwara, S. (2023) Fossorial mammals emphasise the forelimb muscle moment arms used for digging: new indices for reconstruction of the digging ability and behaviours in extinct taxa. Journal of Anatomy, 242, 846–861. PubMed PMC

Nevo, E. (1979) Adaptive convergence and divergence of subterranean mammals. Annual Review of Ecology and Systematics, 10, 269–308.

Nevo, E. (1999) Mosaic evolution of subterranean mammals: regression, progression and global convergence. Oxford: Oxford University Press.

Olson, R.A. , Womble, M.D. , Thomas, D.R. , Glenn, Z.D. & Butcher, M.T. (2016) Functional morphology of the forelimb of the nine‐banded armadillo (Dasypus novemcinctus): comparative perspectives on the myology of Dasypodidae. Journal of Mammalian Evolution, 23, 49–69.

Onwuama, K.T. , Adeniyi, O.S. , Olajide, H.J. , Tavershima, D. & Sulaiman, S.O. (2015) Macro–anatomical and morphometric studies of the Grasscutter (Thryonomys winderianus) forelimb skeleton. International Journal of Veterinary Sciences and Animal Husbandry, 2(1), 6–12.

Orcutt, Ε.E. (1940) Studies on the muscles of the head, neck, and pectoral appendages of Geomys bursarius . Journal of Mammalogy, 21, 37–52.

Parsons, F.G. (1894) On the myology of the sciuromorphine and hystricomorphine rodents. Proceedings Zoological Society of London, 18, 251–297.

Parsons, F.G. (1896) Myology of rodents –part II. An account of the myology of the Myomorpha, together with a comparison of the muscles of the various suborders of rodents. Journal of Zoology, 64, 159–192.

Sahd, L. , Bennett, N.C. & Kotzé, S.H. (2019) Hind foot drumming: morphological adaptations of the muscles and bones of the hind limb in three African mole‐rat species. Journal of Anatomy, 235, 811–824. PubMed PMC

Sahd, L. , Bennett, N.C. & Kotzé, S.H. (2020) Hind foot drumming: Morphofunctional analysis of the hind limb osteology in three species of African mole‐rats (Bathyergidae). Journal of Morphology, 281, 438–449. PubMed

Sahd, L. , Doubell, N. , Bennett, N.C. & Kotzé, S.H. (2023) Muscle architecture and muscle fibre type composition in the forelimb of two African mole‐rat species, Bathyergus suillus and Heterocephalus glaber. Journal of Morphology, 284, e21557. PubMed

Salton, J.A. & Sargis, E.J. (2008) Evolutionary morphology of the Tenrecoidea (Mammalia) forelimb skeleton. In: Sargis, E. & Dagosto, M. (Eds.) Mammalian evolutionary morphology, a tribute to Frederick S. Szalay. Dordrecht: Springer Netherlands, pp. 51–72.

Seckel, L. & Janis, C. (2008) Convergences in scapula morphology among small cursorial mammals: an osteological correlate for Locomotory specialization. Journal of Mammalian Evolution, 15, 261–279.

Stein, B. (2000) Morphology of subterranean rodents. In: Lacey, E.A., Patton, J. & Cameron, G.N. (Eds.) Life underground: the biology of subterranean rodents. Chicago: The University of Chicago Press, pp. 19–61.

Šumbera, R. , Chitaukali, W.N. & Burda, H. (2007) Biology of the silvery mole‐rat (Heliophobius argenteocinereus). Why study a neglected subterranean rodent species? In: Subterranean rodents: news from underground. Berlin Heidelberg New York: Springer‐Verlag, pp. 220–236.

Šumbera, R. , Mazoch, V. , Patzenhauerová, H. , Lövy, M. , Šklíba, J. , Bryja, J. et al. (2012) Burrow architecture, family composition and habitat characteristics of the largest social African mole‐rat: the giant mole‐rat constructs really giant burrow systems. Acta Theriologica, 57(2), 121–130.

Thewissen, J.G.M. & Badoux, D.M. (1986) The descriptive and functional myology of the fore‐limb of the aardvark (Orycteropus afer, Pallas 1766). Anatomischer Anzeiger, 162, 109–123. PubMed

Thorington, R.W. , Darrow, K. & Betts, A.D.K. (1997) Comparative myology of the forelimb of squirrels. Journal of Morphology, 234, 155–182. PubMed

Uhrová, M. , Mikula, O. , Bennett, N.C. , van Daele, P. , Piálek, L. , Bryja, J. et al. (2022) Species limits and phylogeographic structure in two genera of solitary African mole‐rats Georychus and Heliophobius . Molecular Phylogenetics and Evolution, 167, 107337. PubMed

Van Daele, P.A. , Herrel, A. & Adriaens, D. (2009) Biting performance in teeth‐digging African mole‐rats (Fukomys, Bathyergidae, Rodentia). Physiological and Biochemical Zoology, 82(1), 40–50. Available from: 10.1086/594379 PubMed DOI

Van Wassenbergh, S. , Heindryckx, S. & Adriaens, D. (2017) Kinematics of chisel‐tooth digging by African mole‐rats. Journal of Experimental Biology, 220(23), 4479–4485. PubMed

Vassallo, A.I. (1998) Functional morphology, comparative behaviour, and adaptation in two sympatric subterranean rodents genus Ctenomys (Caviomorpha: Octodontidae). Journal of Zoology, 244, 415–427.

Visser, J.H. , Bennett, N.C. & Jansen van Vuuren, B. (2017) Distributional range, ecology, and mating system of the cape mole‐rat (Georychus capensis) family Bathyergidae. Canadian Journal of Zoology, 95(10), 713–726.

Warburton, N.M. , Lea, G. , Sandra, J. & Camille, F. (2014) Adaptations for digging in the forelimb muscle anatomy of the southern brown bandicoot (Isoodon obesulus) and bilby (Macrotis lagotis). Australian Journal of Zoology, 61, 402–419.

Woods, C.A. (1972) Comparative myology of jaw, hyoid and pectoral appendicular regions of new and Old World Hystricomorph rodents. Bulletin of the American Museum of Natural History, 147, 115–198.

Zelová, J. , Šumbera, R. , Okrouhlík, J. & Burda, H. (2010) Cost of digging is determined by intrinsic factors rather than by substrate quality in two subterranean rodent species. Physiology and Behavior, 99(1), 54–58. PubMed