Analysis of the Form-Function Relationship: Digging Behavior as a Case Study

Abstract

Studies of functional morphology focus on species showing evident specializations, or at least some degree of divergence from the so-called “generalized phenotype.” This may have led to the proposal of the form-function correlation paradigm, which assumes that there is a close relationship between anatomical traits and their biological use. A question that arises in relation to digging is what minimum structural and functional requirements would be needed to carry it out properly regarding a particular biological role? Here, we review the main approaches and results achieved in the study of morphological traits related to the highly mechanically demanding function of digging, especially in the South American subterranean rodents Ctenomys and related caviomorph rodents within the mammalian context. It is seen that whatever the biological role that soil digging will play for a particular group of organisms, they must have the ability to disaggregate a relatively resistant material and, therefore, the magnitude of the produced force is a critical point. Muscles of diggers should not only be able to produce large forces but also to sustain them for long periods of time, for which the muscle architecture is another important issue. Digging tools (e.g., limb bones, claws, incisors, skull) must have the capacity to withstand the concomitant reaction forces without structural failure. In this regard cranial sutures, jaw and skull geometry could play an important role in force dissipation. Examples of species that do not diverge from the generalized surface-dweller phenotype, but are nonetheless capable of constructing complex burrows, are examined regarding some evolutionary scenarios where fulfilling minimum functional requirements would have allowed organisms to adequately perform new biological roles.

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References

  1. Ade M, Ziekur I (1999) The forepaws of the rodents Cryptomys hottentotus (Bathyergidae) and Nannospalax ehrenbergi (Muridae, Spalacinae): phylogenetic and functional aspects. Mitt Mus Naturkd Berl in Zool Reihe 75:11–17

    Google Scholar 

  2. Álvarez GI, Díaz AO, Vassallo AI, Longo MV, Becerra, F (2012) Histochemical and morphometric analysis of the musculature of the forelimb of the subterranean rodent Anat Histol Embryol 41:317–325

    PubMed  Google Scholar 

  3. Álvarez A, Vieytes EC, Becerra F, Olivares AI, Echeverría AI, Verzi DH, Vassallo AI (2015) Diversity of craniomandibular morphology in caviomorph rodents: an overview of macroevolutionary and functional patterns. In: Vassallo AI, Antenuchi CD (eds) Biology of Caviomorph Rodents: Diversity and Evolution. SAREM Sociedad Argentina para el Estudio de los Mamíferos, Buenos Aires, pp 199–228

    Google Scholar 

  4. Becerra F (2011) Aparato masticatorio en roedores caviomorfos (Rodentia, Hystricognathi): análisis morfo-funcional con énfasis en el género Ctenomys (Ctenomyidae). PhD dissertation, University of Mar del Plata

  5. Becerra F, Casinos A, Vassallo AI (2013) Biting performance and skull biomechanics of a chisel tooth digging rodent (Ctenomys tuconax; Caviomorpha; Octodontoidea). J Exp Zool 319A:74–85

    Google Scholar 

  6. Becerra F, Echeverría AI, Casinos A, Vassallo AI (2014) Another one bites the dust: bite force and ecology in three caviomorph rodents (Rodentia, Hystricognathi). J Exp Zool 321A:220–232

    Google Scholar 

  7. Becerra F, Echeverría AI, Vassallo AI, Casinos A (2011) Bite force and jaw biomechanics in the subterranean rodent Talas tuco-tuco (Ctenomys talarum) (Caviomorpha: Octodontoidea). Can J Zool 89:334–342

    Google Scholar 

  8. Biknevicius A (1993) Biomechanical scaling of limb bones and differential limb use in caviomorph rodents. J Mammal 74:95–10

    Google Scholar 

  9. Blits KC (1999) Aristotle: form, function, and comparative anatomy. Anat Rec 257:58–63

    CAS  PubMed  Google Scholar 

  10. Borges LR, Maestri R, Kubiak BB, Galiano D, Fornel R, Freitas TRO (2016) The role of soil features in shaping the bite force and related skull and mandible morphology in the subterranean rodents of genus Ctenomys (Hystricognathi: Ctenomyidae). J Zool 117:447–462

    Google Scholar 

  11. Buezas GN, Becerra F, Echeverría AI, Cisilino A, Vassallo AI (2019) Mandible strength and geometry in relation to bite force: a study in three caviomorph rodents. J Anat 234:564–575

    PubMed  Google Scholar 

  12. Buezas GN, Becerra F, Vassallo AI (2017) Cranial sutural morphology in caviomorph rodents (Rodentia; Ctenohystrica). J Morphol 278:1125–1136

    PubMed  Google Scholar 

  13. Campos CM, Tognelli MF, Ojeda RA (2001) Dolichotis patagonum. Mammal Species 625:1–5

    Google Scholar 

  14. Carrizo LV, Tulli MJ, Abdala V (2014) An ecomorphological analysis of forelimb musculotendinous system in sigmodontine rodents (Rodentia, Cricetidae, Sigmodontinae). J Mammal 95:843–854

    Google Scholar 

  15. Cohen M, Longo MV, Vassallo AI, Díaz AO (2017) Estudio histoquímico preliminar de los músculos tríceps longus y bíceps brachii del roedor epígeo Cavia aperea. XXX Jornadas Argentinas de Mastozoología. Bahía Blanca, 14-17 de Noviembre

  16. Costa FR, Clerici GP, Rosa PS, Ribeiro LL, Rocha-Barbosa O (2017) Kinematic description of the vertical climbing of Dasypus novemcinctus (Xenarthra,Dasypodidae): the first report of this ability in armadillos. Mastozool Neotrop 24:451–456

    Google Scholar 

  17. Cox PG, Faulkes CG (2014) Digital dissection of the masticatory muscles of the naked mole-rat, Heterocephalus glaber (Mammalia, Rodentia). PeerJ 2:e448

  18. Cox PG, Hautier L (eds) (2015) Evolution of the Rodents: Advances in Phylogeny, Functional Morphology and Development. Cambridge University Press, Cambridge

  19. Cubo J, Ventura J, Casinos A (2006) A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae). Biol J Linn Soc 87:381–391

    Google Scholar 

  20. Currey JD (2002) Bone: Structure and Mechanics. Princeton University Press, Princeton

    Google Scholar 

  21. Echeverría AI (2011) Ontogenia del comportamiento en el roedor subterráneo Ctenomys talarum (Rodentia: Ctenomyidae). PhD dissertation, University of Mar del Plata

  22. Echeverría AI, Abdala V, Longo MV, Vassallo AI (2019) Functional morphology and identity of the thenar pad in the subterranean genus Ctenomys (Rodentia, Caviomorpha). J Anat 235:940–952

    PubMed  Google Scholar 

  23. Echeverría AI, Becerra F, Vassallo AI (2014) Postnatal ontogeny of limb proportions and functional indices in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae). J Morphol 275:902–913

    PubMed  Google Scholar 

  24. Echeverría AI, Biondi LM, Becerra F, Vassallo AI (2016) Postnatal development of subterranean habits in tuco-tucos Ctenomys talarum (Rodentia, Caviomorpha, Ctenomyidae) J Ethol 34:107-118

    Google Scholar 

  25. Elissamburu A (2004) Análisis morfométrico y morfofuncional del esqueleto apendicular de Paedotherium (Mammalia, Notoungulata). Ameghiniana 41:363–380

    Google Scholar 

  26. Elissamburu A, Vizcaíno SF (2004) Limb proportions and adaptations in caviomorph rodents (Rodentia: Caviomorpha). J Zool 262:145–159

    Google Scholar 

  27. Ercoli MD, Álvarez A, Stefanini MI, Busker F, Morales MM (2015) Muscular anatomy of the forelimbs of the lesser grison (Galictis cuja), and a functional and phylogenetic overview of Mustelidae and other Caniformia. J Mammal Evol 22:57–91

    Google Scholar 

  28. Eyal S, Rubin S, Krief S, Levin L, Zelzer E (2019) Common cellular origin and diverging developmental programs for different sesamoid bones. Development 146. doi:https://doi.org/10.1242/dev.167452

  29. Fernández ME, Vassallo AI, Zárate M (2000) Functional morphology and paleobiology of the Pliocene rodent Actenomys (Caviomorpha: Octodontidae): the evolution to a subterranean mode of life. Biol J Linn Soc 71:71–90

    Google Scholar 

  30. Gambaryan PP, Gasc JP, Renous S (2002) Cinefluorographical study of the burrowing movements in the common mole, Talpa europaea (Lipotyphla, Talpidae). Russ J Theriol 1:91–109

    Google Scholar 

  31. Gomes Rodrigues H, Sumbera R, Hautier L (2016) Life in burrows channelled the morphological evolution of the skull in rodents: the case of African mole-rats (Bathyergidae, Rodentia). J Mammal Evol 23:175–189

    Google Scholar 

  32. Haffner M (1998) A comparison of the gross morphology and micro-anatomy of the foot pads in two fossorial and two climbing rodents (Mammalia). J Zool 244:287–294

    Google Scholar 

  33. Hautier L, Lebrun R, Saksiri S, Michaux J, Vianey-Liaud M, Marivaux L (2011) Hystricognathy vs sciurognathy in the rodent jaw: a new morphometric assessment of hystricognathy applied to the living fossil Laonastes (Diatomyidae). PLoS One 6:e18698.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Herring SW (2010) Muscle-bone interactions and the development of skeletal phenotype. In: Hallgrimsson B, Hall BK (eds) Epigenetics. University of California Press, Berkeley, pp 221–237

    Google Scholar 

  35. Herring SW, Teng S (2000) Strain in the braincase and its sutures during function. Am J Phys Antropol 112:575–593

    CAS  Google Scholar 

  36. Hickman GC (1985) Surface-mound formation by the tuco-tuco, Ctenomys fulvus (Rodentia: Ctenomyidae), with comments on earth-pushing in other fossorial mammals. J Zool 205:385–390

    Google Scholar 

  37. Hildebrand M (1985) Digging in quadrupeds. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional Vertebrate Morphology. Belknap Press, Cambridge, pp 89–109

    Google Scholar 

  38. Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) (1985) Functional Vertebrate Morphology. Belknap Press, Cambridge

  39. Jaslow CR (1990) Mechanical properties of cranial sutures. J Biomech 23:313–321

    CAS  PubMed  Google Scholar 

  40. Kley NJ, Kearney M (2007) Adaptations for digging and burrowing. In: Hall BK (ed) Fins into Limbs: Evolution, Development, and Transformation. University of Chicago Press, Chicago, pp 284–309

    Google Scholar 

  41. Laland KN, Odling-Smee J, Gilbert SF (2008) EvoDevo and niche construction: building bridges. J Exp Zool B Mol Dev Evol 310:549–566

    PubMed  Google Scholar 

  42. Lehman WH (1963) The forelimb architecture of some fossorial rodents. J Morphol 113:59–75

    Google Scholar 

  43. Lessa EP, Stein BR (1992) Morphological constraints in the digging apparatus of pocket gophers (Mammalia, Geomyidae). Biol J Linn Soc 47:439–453

    Google Scholar 

  44. Lessa EP, Vassallo AI, Verzi DH, Mora MS (2008) Evolution of morphological adaptations for digging in living and extinct ctenomyid and octodontid rodents. Biol J Linn Soc 95:267–283

    Google Scholar 

  45. Longo MV, Díaz AO (2013) The claw closer muscle of two estuarine crab species, Cyrtograpsus angulatus and Neohelice granulata (Grapsoidea, Varunidae): histochemical fibre type composition. Acta Zool 94:233–239

    Google Scholar 

  46. Longo MV, Díaz AO, Goldemberg AL (2011) The claw closer muscle of Neohelice granulata (Grapsoidea, Varunidae): a morphological and histochemical study. Acta Zool 92:126–133

    Google Scholar 

  47. Longo MV, Díaz AO, Vassallo AI (2017) Morfología funcional de la musculatura masetérica del roedor subterráneo Ctenomys talarum: histoquímica de tipos de fibras. XXX Jornadas Argentinas de Mastozoología. Bahía Blanca, 14-17 de Noviembre

  48. Marroig G, Cheverud JM (2001) A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55:2576–2600

    CAS  PubMed  Google Scholar 

  49. Mayr E (1963) Animal Species and Evolution. Harvard University Press, Cambridge

    Google Scholar 

  50. McIntosh AF, Cox PG (2016) The impact of gape on the performance of the skull in chisel-tooth digging and scratch digging mole-rats (Rodentia: Bathyergidae). R Soc Open Sci 3(10): 160568

    PubMed  PubMed Central  Google Scholar 

  51. Menegaz RA, Sublett SV, Figueroa SD, Hoffman TJ, Ravosa MJ, Aldridge K (2010) Evidence for the influence of diet on cranial form and robusticity. Anat Rec 293:630–641

    Google Scholar 

  52. Mora MS, Becerra F, Vassallo AI (2018) An allometric analysis of sexual dimorphism in Ctenomys australis: integrating classic morphometry and functional performance in vivo. Zoology 127:27–39

    PubMed  Google Scholar 

  53. Morgan CC, Verzi DH (2006) Morphological diversity of the humerus of the South American subterranean rodent Ctenomys (Rodentia, Ctenomyidae). J Mammal 87:1252–1260

    Google Scholar 

  54. Napier JR (1980) Hands. Princeton University Press, Princeton

    Google Scholar 

  55. Ojeda AA, Tarquino-Carbonell A, Veléz LM, Ojeda RA (2018) Tympanoctomys: 75 años de historia. Estado actual del género y perspectivas futuras. Rev Mus Argentino Cienc Nat 20:109–122

    Google Scholar 

  56. Ozkaya N, Nordin M (1999) Fundamentals of Biomechanics. Springer Verlag, Berlin

    Google Scholar 

  57. Pardiñas UFJ, Galliari CA (2001) Reithrodon auritus. Mammal Species 664:1–8

    Google Scholar 

  58. Pedersen SC (2000) Skull growth and the acoustical axis of the head in bats. In: Adams RA, Pedersen SC (eds) Ontogeny, Functional Ecology, and Evolution of Bats. Cambridge University Press, Cambridge, pp 174–213

    Google Scholar 

  59. Pérez EM (1992) Agouti paca. Mammal Spec 404:1–7

    Google Scholar 

  60. Pérez MJ, Barquez RM, Díaz MM (2017) Morphology of the limbs in the semi-fossorial desert rodent species of Tympanoctomys (Octodontidae, Rodentia). Zoo Keys 710:77–96

    Google Scholar 

  61. Radinsky LB (1984) Ontogeny and phylogeny in horse skull evolution. Evolution 38:1–15

    PubMed  Google Scholar 

  62. Radinsky LB (1985a) Approaches in evolutionary morphology: a search for patterns. Annu Rev Ecol Syst 16:1–14

    Google Scholar 

  63. Radinsky LB (1985b) Patterns in the evolution of unguate jaw shape. Am Zool 25:303–314

    Google Scholar 

  64. Rayfield E (2007) Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu Rev Earth Planet Sci 35:541–576

    CAS  Google Scholar 

  65. Redford KH, Eisenberg JF (1992) Mammals of the Neotropics. Vol. 2. The South Cone: Chile, Argentina, Uruguay, Paraguay. University of Chicago Press, Chicago

    Google Scholar 

  66. Reichman OJ, Smith SC (1990) Burrows and burrowing behavior by mammals. In: Genoways HH (ed) Current Mammalogy. Plenum Press, New York, pp 197–244

    Google Scholar 

  67. Segura V (2015) A three-dimensional skull ontogeny in the bobcat (Lynx rufus) (Carnivora: Felidae): a comparison with other carnivorans. Can J Zool 93:225–237

    Google Scholar 

  68. Smith KK (1993) The form of the feeding apparatus in terrestrial vertebrates: Studies of adaptation and constraint. In: Hanken J, Hall BK (eds) The Skull - Functional and Evolutionary Mechanisms, Vol 3. University of Chicago Press, Chicago, pp 150–196

    Google Scholar 

  69. Soons J, Herrel A, Genbrugge A, Aerts P, Podos J, Adriaens D, de Witte Y, Jacobs P, Dirckx J (2010) Mechanical stress, fracture risk and beak evolution in Darwin’s ground finches (Geospiza). Philos Trans R Soc B 365:1093–1098

    Google Scholar 

  70. Stein BR (2000) Morphology of subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life Underground: The Biology of Subterranean Rodents. University of Chicago Press, Chicago, pp 19–61

    Google Scholar 

  71. Tavares WC, Vozniak JH, Pessôa LM (2019) Evolution of appendicular specializations for fossoriality in euryzygomatomyine spiny rats across different Brazilian biomes (Echimyidae, Hystricognathi, Rodentia). J Mammal Evol https://doi.org/10.1007/s10914-019-09459-8

  72. Tognelli M, Campos C, Ojeda RA (2001) Microcavia australis. Mammal Species 648:1–4

    Google Scholar 

  73. Ubilla M (2008) Postcranial morphology of the extinct caviine rodent Microcavia criolloensis (late Pleistocene, South America). Zool J Linn Soc 154:795–806

    Google Scholar 

  74. Ubilla M, Altuna C (1990) Analyse de la morphologie de la main chez des espèces de Ctenomys de l’Uruguay (Rodentia, Octodontidae): adaptations au fouissage et implications évolutives. Mammalia 54:108–117

    Google Scholar 

  75. Van Daele PA, Herrel A, Adriaens D (2009) Biting performance in teeth-digging African mole-rats (Fukomys, Bathyergidae, Rodentia). Physiol Biochem Zool 82:40–50

    PubMed  Google Scholar 

  76. Van Wassenbergh S, Heindryckx S, Adriaens D (2017) Kinematics of chisel-tooth digging by African mole-rats. J Exp Biol 220:4479–4485

    PubMed  Google Scholar 

  77. Vassallo AI (1998) Functional morphology, comparative behavior, and adaptation in two sympatric subterranean rodent genus Ctenomys (Rodentia: Octodontidae). J Zool 244:415–427

    Google Scholar 

  78. Vassallo AI, Becerra F, Echeverría AI, Casinos A (2015) Ontogenetic integration between force production and force reception: a case study in Ctenomys (Rodentia: Caviomorpha). Acta Zool 97:232–240

    Google Scholar 

  79. Vassallo AI, Mora MS (2007) Interspecific scaling and ontogenetic growth patterns of the skull in living and fossil ctenomyid and octodontid rodents (Caviomorpha: Octodntoidea). In: Kelt DA, Lessa EP, Salazar-bravo J, Patton JL (eds) The Quintessential Naturalist: Honoring the Life and Legacy of Oliver P. Pearson. Univ Calif Publ Zool 134:945–968

    Google Scholar 

  80. Verzi DH, Álvarez A, Olivares AI, Morgan CC, Vassallo AI (2010) Ontogenetic trajectories of key morphofunctional cranial traits in South American subterranean ctenomyid rodents. J Mammal 91:1508–1516

    Google Scholar 

  81. Vieytes EC, Morgan CC, Verzi DH (2007) Adaptive diversity of incisor enamel microstructure in South American burrowing rodents (family Ctenomyidae, Caviomorpha). J Anat 211:296–302

    PubMed  PubMed Central  Google Scholar 

  82. Vizcaíno SF, Fariña RA, Mazzetta GV (1999) Ulnar dimensions and fossoriality in armadillos. Acta Theriol 44:309–320

    Google Scholar 

  83. Wake MH (1993) The skull as a locomotor organ. In: Hanken J, Hall BK (eds) The Skull: Functional and Evolutionary Mechanisms. University of Chicago Press, Chicago, pp 197–240

    Google Scholar 

  84. Weber JN, Peterson BK, Hoekstra HE (2013) Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493:402–406

    CAS  PubMed  Google Scholar 

  85. Weijs WA, Brugman P, Klok EM (1987) The growth of the skull and jaw muscles and its functional consequences in the New Zealand rabbit (Oryctolagus cuniculus). J Morphol 194:143–161

    CAS  PubMed  Google Scholar 

  86. Woods CA (1972) Comparative myology of jaw, hyoid and pectoral appendicular regions of new and Old World hystricomorph rodents. Bull Am Mus Nat Hist 147:119–198

    Google Scholar 

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Acknowledgements

We thank Drs. S. Vizcaíno, G. Cassini, and N. Toledo for the invitation to participate in the symposium “The paradigm of shape-function correlation in mastozoology: a tribute to Leonard Radinsky,” which was held in La Rioja during the XXXI Jornadas Argentinas de Mastozoología. We thank Joshua Asel who kindly provided the photo of the rata vizcacha colorada (Tympanoctomys barrerae). Financial support: CONICET PIP 2014-2016 N ° 11220130100375 and Grant EXA918 / 18 from University of Mar del Plata.

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Vassallo, A.I., Becerra, F., Echeverría, A.I. et al. Analysis of the Form-Function Relationship: Digging Behavior as a Case Study. J Mammal Evol 28, 59–74 (2021). https://doi.org/10.1007/s10914-019-09492-7

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Keywords

  • Functional morphology
  • Muscle force
  • Form and function correlation
  • Subterranean mammals
  • Ctenomys