Skip to main content
Log in

Ear morphology in two root-rat species (genus Tachyoryctes) differing in the degree of fossoriality

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

It is supposed that the subterranean lifestyle in mammals is reflected in ear morphology and tuning of hearing to low frequencies. We studied two root-rat species to see if their ear morphology reflects the difference in the amount of their surface activity. Whereas the more subterranean Tachyoryctes splendens possesses shorter pinnae as expected, it has smaller bullae compared to the more epigeic Tachyoryctes macrocephalus. The ratio between the eardrum and the stapedial footplate area and the ratio between the mallear and the incudal lever were lower in T. splendens (19.3 ± 0.3 and 1.9 ± 0.0, respectively) than in T. macrocephalus (21.8 ± 0.6 and 2.1 ± 0.1), probably reflecting the latter’s higher surface activity. The cochlea in both species has 3.5 coils, yet the basilar membrane is longer in the smaller T. splendens (13.0 ± 0.5 versus 11.4 ± 0.7 mm), which indicates its wider hearing range and/or higher sensitivity (to some frequencies). In both root-rat species, the highest density of outer hair cells (OHC) was in the apical part of the cochlea, while the highest density of inner hair cells (IHC) was in its middle part. This OHC density pattern corresponds with good low-frequency hearing, whereas the IHC pattern suggests sensitivity to higher frequencies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and material

The data that support the findings of this study are available within the article.

Code availability

Not applicable.

Abbreviations

BH:

Bullar height

BL:

Bullar length

BM:

Basilar membrane

BV:

Bullar volume

BW:

Bullar width

CBL:

Condylobasal length

IHC:

Inner hair cells

OC:

Organ of Corti

OCW:

Organ of Corti width

OHC:

Outer hair cells

TR:

Triad = three rows of OHC

References

  • Argyle AC, Mason MJ (2008) Middle ear structures of Octodon degus (Rodentia: Octodontidae) in comparison with those in subterranean caviomorphs. J Mammal 89:1447–1455

    Article  Google Scholar 

  • Begall S, Burda H (2006) Acoustic communication and burrow acoustics are reflected in the ear morphology of the coruro (Spalacopus cyanus, Octodontidae), a social fossorial rodent. J Morphol 267:382–390

    Article  PubMed  Google Scholar 

  • Begall S, Burda H, Schneider B (2004) Hearing in coruros (Spalacopus cyanus): special audiogram features of a subterranean rodent. J Comp Physiol A 190:963–969

    Google Scholar 

  • Begall S, Lange S, Schleich CE, Burda H (2007a) Acoustics, audition and auditory system. In: Begall S, Burda H, Schleich CE (eds) Subterranean rodents: news from underground. Springer, Berlin, pp 97–111

    Chapter  Google Scholar 

  • Begall S, Burda H, Schleich CE (2007b) Introduction. In: Begall S, Burda H, Schleich CE (eds) Subterranean rodents: news from underground. Springer, Berlin, pp 3–7

    Chapter  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Asociates Inc, Suderland

    Google Scholar 

  • Bruns V, Müller M, Hofer W, Heth G, Nevo E (1988) Inner ear structure electrophysiological audiograms of the subterranean mole rat, Spalax ehrenbergi. Hear Res 33:1–9

    Article  CAS  PubMed  Google Scholar 

  • Burda H (1985) Qualitative assessment of postnatal maturation of the organ of Corti in two rat strains. Hear Res 17:201–208

    Article  CAS  PubMed  Google Scholar 

  • Burda H (2006) Ear and eye in subterranean mole-rats, Fukomys anselli (Bathyergidae) and Spalax ehrenbergi (Spalacidae): progressive specialisation or regressive degeneration? Anim Biol 56:475–486

    Article  Google Scholar 

  • Burda H, Ballast L, Bruns V (1988) Cochlea in old world mice and rats (Muridae). J Morphol 198:269–285

    Article  CAS  PubMed  Google Scholar 

  • Burda H, Bruns V, Nevo E (1989) Middle ear and cochlear receptors in the subterranean mole-rat, Spalax ehrenbergi. Hear Res 39:225–230

    Article  CAS  PubMed  Google Scholar 

  • Burda H, Bruns V, Müller M (1990) Sensory adaptations in subterranean mammals. Evolution of subterranean mammals at the organismal and molecular levels. Progr Clin Biol Res 335:269–293

    CAS  Google Scholar 

  • Burda H, Bruns V, Hickman GC (1992) The ear in subterranean Insectivora and Rodentia in comparison with ground-dwelling representatives. I. Sound conducting system of the middle ear. J Morphol 214:49–61

    Article  CAS  PubMed  Google Scholar 

  • Coleman MN, Colbert MW (2010) Correlations between auditory structures and hearing sensitivity in non-human primates. J Morphol 271:511–532

    PubMed  Google Scholar 

  • Crumpton N, Kardjilov N, Asher RJ (2015) Convergence vs. specialization in the ear region of moles (Mammalia). J Morphol 276:900–914

    Article  PubMed  Google Scholar 

  • Echteler SM, Fay RR, Popper AN (1994) Structure of the mammalian cochlea. In: Fay RR, Popper AN (eds) Comparative hearing: mammals. Springer, New York, pp 134–171

    Chapter  Google Scholar 

  • Ekdale EG (2016) Form and function of the mammalian inner ear. J Anat 228(2):324–337

    Article  PubMed  Google Scholar 

  • Fleischer G (1978) Evolutionary principles of the mammalian middle ear. Adv Anat Embryol Cell Biol 55:1–70

    Google Scholar 

  • Francescoli G (2000) Sensory capabilities and communication in subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life underground: the biology of subterranean rodents. University of Chicago Press, Illinois, pp 111–144

    Google Scholar 

  • Gerhardt P, Henning Y, Begall S, Malkemper EP (2017) Audiograms of three subterranean rodent species (genus Fukomys) determined by auditory brainstem responses reveal extremely poor high-frequency cut-offs. J Exp Biol 220:4377–4382

    Article  PubMed  Google Scholar 

  • Heffner H (1980) Hearing in Glires: domestic rabbit, cotton rat, feral house mouse, and kangaroo rat. J Acoust Soc Am 68:1584–1599

    Article  Google Scholar 

  • Heffner RS, Heffner HE (1990) Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius). Hear Res 46:239–252

    Article  CAS  PubMed  Google Scholar 

  • Heffner RS, Heffner HE (1992) Hearing and sound localization in blind mole rats (Spalax ehrenbergi). Hear Res 62:206–216

    Article  CAS  PubMed  Google Scholar 

  • Heffner RS, Heffner HE (1993) Degenerate hearing and sound localization in naked mole rats (Heterocephalus glaber), with an overview of central auditory structures. J Comp Neurol 331:418–433

    Article  CAS  PubMed  Google Scholar 

  • Heffner RS, Heffner HE, Contos C, Kearns D (1994) Hearing in prairie dogs: transition between surface and subterranean rodents. Hear Res 73:185–189

    Article  CAS  PubMed  Google Scholar 

  • Heth G, Frankenberg E, Nevo E (1986) Adaptive optimal sound for vocal communication in tunnels of a subterranean mammal (Spalax ehrenbergi). Experientia 42:1287–1289

    Article  CAS  PubMed  Google Scholar 

  • Hrouzková E, Dvořáková V, Jedlička P, Šumbera R (2013) Seismic communication in demon African mole rat Tachyoryctes daemon from Tanzania. J Ethol 31:255–259

    Article  Google Scholar 

  • Hrouzková E, Šklíba J, Pleštilová L, Hua L, Meheretu Y, Sillero-Zubiri C, Šumbera R (2018) Seismic communication in spalacids: signals in the giant root-rat and Gansu zokor. Hystrix It J Mammal 29:243–245

    Google Scholar 

  • Jarvis JUM, Sale JB (1971) Burrowing and burrow patterns of East-African mole-rats Tachyoryctes, Heliophobius and Heterocephalus. J Zool 163:451–479

    Article  Google Scholar 

  • Katandukila JV, Bennett NC, Chimimba CT, Faulkes CG, Oosthuizen MK (2013) Locomotor activity patterns of captive East African root rats, Tachyoryctes splendens (Rodentia: Spalacidae), from Tanzania, East Africa. J Mammal 94:1393–1400

    Article  Google Scholar 

  • Katandukila JV, Chimimba CT, Bennett NC, Makundi RH, Le Comber SC, Faulkes CG (2014) Sweeping the house clean: burrow architecture and seasonal digging activity in the East African root rat from Tanzania. J Zool 293:271–280

    Article  Google Scholar 

  • Kokiso A, Bekele A (2008) Ecology of common mole-rat, Tachyoryctes splendens and its impacts on farmlands at Angecha, Central Ethiopia. Act Zool Sinica 54:30–35

    Google Scholar 

  • Lange S (2005) Sinnesökologie afrikanischer Sandgräber (Bathyergidae) am Beispiel von Hör- und Geruchssinn. Dissertation (PhD thesis), Universität Duisburg-Essen, p 177

  • Lange S, Stalleicken J, Burda H (2004) Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris. J Morphol 262:770–779

    Article  PubMed  Google Scholar 

  • Lange S, Burda H, Wegner RE, Dammann P, Begall S, Kawalika M (2007) Living in a “stethoscope”: burrow acoustics promote auditory specializations in subterranean rodents. Naturwissenschaften 94:134–138

    Article  CAS  PubMed  Google Scholar 

  • Lavocat R, Parent JP (1985) Phylogenetic analysis of middle ear features in fossil and living rodents. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Springer, Boston, pp 333–354

    Chapter  Google Scholar 

  • Manoussaki D, Chadwick RS, Ketten DR, Arruda J, Dimitriadis EK, O’Malley JT (2008) The influence of cochlear shape on low-frequency hearing. Proc Natl Acad Sci 105:6162–6166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mason MJ (2001) Middle ear structures in fossorial mammals: a comparison with non-fossorial species. J Zool 255:467–486

    Article  Google Scholar 

  • Mason MJ (2004) The middle ear apparatus of the tuco-tuco Ctenomys sociabilis (Rodentia, Ctenomyidae). J Mammal 85:797–805

    Article  Google Scholar 

  • Mason MJ (2013) Of mice, moles and guinea-pigs: functional morphology of the middle ear in living mammals. Hear Res 301:4–18

    Article  PubMed  Google Scholar 

  • Mason MJ (2016) Structure and function of the mammalian middle ear. II: inferring function from structure. J Anat 228:300–312

    Article  PubMed  Google Scholar 

  • Mason MJ, Lai FWS, Li JG, Nevo E (2010) Middle ear structure and bone conduction in Spalax, Eospalax, and Tachyoryctes mole-rats (Rodentia: Spalacidae). J Morphol 271:462–472

    PubMed  Google Scholar 

  • Nevo E (1979) Adaptive convergence and divergence of subterranean mammals. Annu Rev Ecol Syst 10:269–308

    Article  Google Scholar 

  • Nevo E (1999) Mosaic evolution of subterranean mammals (regression, progression and convergence). Oxford University Press, Oxford, p 413

    Google Scholar 

  • Norris RW (2017) Family Spalacidae (Muroid mole-rats). In: Wilson DE, Lacher TE Jr, Mittermeier RA (eds) Handbook of the mammals of the world—vol 7. Rodents II. Lynx Editions, p 1008

    Google Scholar 

  • Plassmann W, Kadel M (1991) Low-frequency sensitivity in a gerbilline rodent, Pachyuromys duprasi. Brain Behav Evol 38:115–126

    Article  CAS  PubMed  Google Scholar 

  • Pleštilová L, Hrouzková E, Burda H, Šumbera R (2016) Does the morphology of the ear of the Chinese bamboo rat (Rhizomys sinensis) show “subterranean” characteristics? J Morphol 277:575–584

    Article  PubMed  Google Scholar 

  • Pleštilová L, Hrouzková E, Burda H, Hua L, Šumbera R (2019) Additional row of outer hair cells—the unique pattern of the Corti organ in a subterranean rodent, the Gansu zokor (Eospalax cansus). Mamm Biol 94:11–17

    Article  Google Scholar 

  • Rado R, Himelfarb M, Arensburg B, Terkel J, Wollberg Z (1989) Are seismic communication signals transmitted by bone conduction in the blind mole rat? Hear Res 41:23–30

    Article  CAS  PubMed  Google Scholar 

  • Rosowski JJ (1994) Outer and middle ears. In: Fay RR, Popper AN (eds) Comparative hearing: mammals. Springer, New York, pp 172–247

    Chapter  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Tinevez JY (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  CAS  PubMed  Google Scholar 

  • Schleich CE, Vassallo AI (2003) Bullar volume in subterranean and surface-dwelling caviomorph rodents. J Mammal 84:185–189

    Article  Google Scholar 

  • Schleich CE, Begall S, Burda H (2006) Morpho-functional parameters of the inner ear in Ctenomys talarum; Rodentia, Ctenomyidae. Folia Zool 55:264–272

    Google Scholar 

  • Slepecky NB (1996) Structure of the mammalian cochlea. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 44–129

    Chapter  Google Scholar 

  • Smith AT, Xie Y (2008) A guide to the mammals of China. Princeton University Press, Princeton, p 576

    Google Scholar 

  • Šumbera R, Krásová J, Lavrenchenko LA, Mengistu S, Bekele A, Mikula O, Bryja J (2018) Ethiopian highlands as a cradle of the African fossorial root-rats (genus Tachyoryctes), the genetic evidence. Mol Phylogenet Evol 126:105–115

    Article  PubMed  Google Scholar 

  • Vlasatá T, Šklíba J, Lövy M, Meheretu Y, Sillero-Zubiri C, Šumbera R (2017) Daily activity patterns in the giant root rat (Tachyoryctes macrocephalus), a fossorial rodent from the Afro-alpine zone of the Bale Mountains, Ethiopia. J Zool 302:157–163

    Article  Google Scholar 

  • Wannaprasert T (2016) Functional morphology of the ear of the lesser bamboo rat (Cannomys badius). Mammal Study 41:107–117

    Article  Google Scholar 

  • West CD (1985) The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. J Acoust Soc Am 77:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Yalden DW (1985) Tachyoryctes macrocephalus. Mamm Species 237:1–3

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Ethiopian Wildlife Conservation Authority (EWCA) for permission to conduct field research in Ethiopia. We thank the Bale Mountains National Park for kind cooperation. We thank Matěj Lövy, Tereza Vlasatá, and Jan Šklíba for assistance and collecting specimens of Tachyoryctes macrocephalus in the field and to Christopher Mark Steer for English proofreading.

Funding

This work was supported by the Czech Science Foundation (GAČR) projects P506/11/1512 and 20-10222S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucie Pleštilová.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Ethics approval

All procedures involving wild-caught animals were performed and approved by the Institutional Animal Care and Use Committee at the University of South Bohemia and the Ministry of Education, Youth and Sports (n. 7942/2010-30).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pleštilová, L., Hrouzková, E., Burda, H. et al. Ear morphology in two root-rat species (genus Tachyoryctes) differing in the degree of fossoriality. J Comp Physiol A 207, 469–478 (2021). https://doi.org/10.1007/s00359-021-01489-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-021-01489-z

Keywords

Navigation