Skip to main content
Log in

Who nose the borzoi? Turbinal skeleton in a dolichocephalic dog breed (Canis lupus familiaris)

  • Original investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

The domestic dog (Canis lupus familiaris) shows a high intraspecific morphological diversity in its facial shape with a less well-known effect of different snout length types on the intranasal structures, i.e. the turbinal skeleton. Sighthounds are supposed to have a less developed sense of smell in favor of their visual abilities. It has been proposed that within the small space of a sighthound’s slender snout the turbinals are less in number and reduced. In a recent ethological study the English greyhound failed at an odor-discrimination task. To test this hypothesis we performed a morphological and morphometric analysis of the turbinal skeleton in the borzoi as a member of the sighthound group based on high resolution computed tomography. For comparison we included saluki, German shepherd and Eurasian wolf in our study; borzoi and German shepherd are represented by different ontogenetic stages. Histological serial sections of a prenatal whippet were investigated to confirm identification of single turbinals. In order to elucidate the proportions and complexity of the turbinal skeleton we applied a new morphometric approach. Our results clearly show no significant difference in the number of turbinals in all investigated specimens but an unexpected high number of interturbinals in the sighthounds in comparison to the German shepherd and the wolf, a large surface area and a high surface density and turbinal complexity. Consequently, the turbinal morphology of the borzoi and most probably the sighthound group in general clearly shows no skeletal evidence for a reduced olfactory sense. Thus, our study demonstrates that the bony turbinals alone cannot provide a proxy for olfactory abilities in dogs. The epithelium, the olfactory receptors with their corresponding genes, the brain, and the ethology need to be considered as well when analyzing a species’ olfactory performance.

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.

Similar content being viewed by others

Abbreviations

AE:

exterior surface area

ALB:

area of length and breadth of snout

AT:

turbinal surface area

BOR:

borzoi

BZB:

bizygomatic breadth

C:

upper canine

DOL:

dolichocephalic

dP2-4:

deciduous upper premolar 2-4

ep:

epiturbinal of eth-moturbinal I

et:

ethmoturbinal

etr:

ethmoturbinal recess

EW:

Eurasian wolf

f:

frontal

ft:

frontoturbinal

ftr:

frontoturbinal recess

GLS:

greatest length of skull

GSD:

German shepherd

IAE:

index exterior surface area

IAT:

index turbinal surface area

IBL:

index breadth to length of skull

IFB:

index facial length to length of braincase

IOB:

interorbital breadth

it:

interturbinal

it:

prominent interturbinal homologous between all individuals

j:

jugal

lac:

lacrimal

LBC:

length of braincase

lh:

lamina horizontalis

LPII:

length of palate II

ls:

lamina semicircularis

lt:

lamina terminalis

ltp:

lamina transversalis posterior

lv:

lamina verticalis

M1-2:

upper molar 1-2

MES:

mesaticephalic

[MfN]:

alternative labelling of mammal collection at Museum für Naturkunde Berlin, Germany

MNHN:

Muséum national d’Histoire naturelle, Paris, France

mt:

maxilloturbinal

mx:

maxillary

mxr:

maxillary recess

mxs:

maxillary sinus

n:

nasal

NMBE:

Naturhistorisches Museum der Burgergemeinde Bern, Switzerland

nd:

nasopharyngeal duct

NLII:

nasal length II

ns:

nasal septum

nt:

nasoturbinal

P2-4:

upper premolar 2-4

pa:

pars anterior(etI)

pl:

palate

pmx:

praemaxillary

pn:

paries nasi

pp:

pars posterior(etI)

upr:

uncinate process

SDEN:

surface density

SMF:

Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Germany

TC:

turbinal complexity

tn:

tectum nasi

WH:

whippet

ZMBMAM:

mammal collection of Museum für Naturkunde Berlin, Germany

References

  • Ash, E.C., 1927. Dogs: Their History and Development, vol I. Ernest Benn Limited, London.

    Google Scholar 

  • Baron, G., Frahm, H.D., Bhatnagar, K.P., Stephan, H., 1983. Comparison of brain structure volumes in Insectivora and Primates. III. Main olfactory bulb (MOB). J. Hirnforsch. 24, 551–568.

    CAS  PubMed  Google Scholar 

  • Beckmann, L., 1894. Geschichte und Beschreibung der Rassen des Hundes. Bd. I. Druck und Verlag von Friedrich Bieweg und Sohn, Braunschweig.

    Google Scholar 

  • Brehm, A.E., 1876. Brehms Thierleben. Allgemeine Kunde des Thierreichs. Bibliographisches Institut, Leipzig.

    Google Scholar 

  • Burk, R.L., 1992a. Computed tomographic anatomy of the canine nasal passages. Vet. Radiol. Ultrasoun. 33, 170–176.

    Google Scholar 

  • Burk, R.L., 1992b. Computed tomographic imaging of nasal disease in 100 dogs. Vet. Radiol. Ultrasoun. 33, 177–180.

    Google Scholar 

  • Craven, B.A., Neuberger, T., Paterson, E.G., Webb, A.G., Josephson, E.M., Morrison, E.E., Settles, G.S., 2007. Reconstruction and morphometric analysis of the nasal airway of the dog (Canis familiaris) and implications regarding olfactory airflow. Anat. Rec. 290, 1325–1340.

    Google Scholar 

  • Craven, B.A., Paterson, E.G., Settles, G.S., 2010. The fluid dynamics of canine olfaction: unique nasal airflow patterns as an explanation of macrosmia. J. Roy. Soc. Interface 7, 933–943.

    Google Scholar 

  • Ellenberger, W., Baum, H., 1891. Systematische und topographische Anatomie des Hundes. Paul Parey, Berlin, Hamburg.

    Google Scholar 

  • Finck, M., Ponce, F., Guilbaud, L., Chervier, C., Floch, F., Cadore, J.L., Chuzel, T., Hugonnard, M., 2015. Computed tomography or rhinoscopy as the first-line procedure for suspected nasal tumor: a pilot study. Can. Vet. J. 56, 185–192.

    PubMed  PubMed Central  Google Scholar 

  • Green, P.A., Van Valkenburgh, B., Pang, B., Bird, D., Rowe, T., Curtis, A., 2012. Respiratory and olfactory turbinal size incanid and arctoid carnivorans. J. Anat. 221, 609–621.

    PubMed  PubMed Central  Google Scholar 

  • Guagnin, M., Perri, A.R., Petraglia, M.D., 2018. Pre-Neolithic evidence for dog-assisted hunting strategies in Arabia. J. Anthropol. Archaeol. 49, 225–236.

    Google Scholar 

  • Hall, N.J., Glenn, K., Smith, D.W., Wynne, C.D., 2015. Performance of Pugs, German Shepherds, and Greyhounds (Canis lupus familiaris) on an odor-discrimination task. J. Comp. Psychol. 129, 237–246.

    PubMed  Google Scholar 

  • Hillenius, W.J., 1992. The evolution of nasal turbinates and mammalian endothermy. Paleobiology 18, 17–29.

    Google Scholar 

  • Hillenius, W.J., 1994. Turbinates intherapsids — evidence for late permian origins of mammalian endothermy. Evolution 48, 207–229.

    PubMed  Google Scholar 

  • Hofer, H., 1952. Der Gestaltwandel des Schädels der Säugetiere und Vögel, mit besonderer Berücksichtigung der Knickungstypen und der Schädelbasis. Verh. Anat. Ges. 50, 102–113.

    Google Scholar 

  • Issel-Tarver, L., Rine, J., 1996. Organization and expression of canine olfactory receptor genes. Proc. Natl. Acad. Sci. U. S. A. 93, 10897–10902.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn, H.J., 1971. Die Entwicklung und Morphologie des Schädels von Tachyglossus aculeatus. Abh. senckenb. naturforsch. Ges. 528, 1–224.

    Google Scholar 

  • Lesniak, A., Walczak, M., Jezierski, T., Sacharczuk, M., Gawkowski, M., Jaszczak, K., 2008. Canine olfactory receptor gene polymorphism and its relation to odor detection performance by sniffer dogs. J. Hered. 99, 518–527.

    CAS  PubMed  Google Scholar 

  • Macrini, T.E., 2012. Comparative morphology of the internal nasal skeleton of adult marsupials based on X-ray computed tomography. B. Am. Mus. Nat. Hist. 365, 1–91.

    Google Scholar 

  • Maier, W., Ruf, I., 2014. Morphology of the nasal capsule of primates — with special reference to Daubentonia and Homo. Anat. Rec. 297, 1985–2006.

    Google Scholar 

  • Mazák, J.H., 2010. Geographical variation and phylogenetics of modern lions based on craniometric data. J. Zool. 281, 194–209.

    Google Scholar 

  • McGreevy, P., Grassi, T.D., Harman, A.M., 2004. A strong correlation exists between the distribution of retinal ganglion cells and nose length in the dog. Brain Behav. Evol. 63, 13–22.

    PubMed  Google Scholar 

  • Mech, L.D., 1974. Canis lupus. Mamm. Species 37, 1–6.

    Google Scholar 

  • Oechtering, G.U., Pohl, S., Schlueter, C., Lippert, J.P., Alef, M., Kiefer, I., Ludewig, E., Schuenemann, R., 2016. A novel approach to brachycephalic syndrome. 1. Evaluation of anatomical intranasal airway obstruction. Vet. Surg. 45, 165–172.

    PubMed  Google Scholar 

  • Pang, B., Yee, K.K., Lischka, F.W., Rawson, N.E., Haskins, M.E., Wysocki, C.J., Craven, B.A., Van Valkenburgh, B., 2016. The influence of nasal airflow on respiratory and olfactory epithelial distribution in felids. J. Exp. Biol. 219, 1866–1874.

    PubMed  PubMed Central  Google Scholar 

  • Paulli, S., 1900a. Über die Pneumaticität des Schädels bei den Säugetieren. Eine morphologische Studie. I. Über den Bau des Siebbeins. Über die Morphologie des Siebbeins und die Pneumaticität bei den Monotremen und den Marsupialiern. Morphol. Jb. 28, 147–178.

    Google Scholar 

  • Paulli, S., 1900b. Über die Pneumaticität des Schädels bei den Säugetieren. Eine morphologische Studie. II. Über die Morphologie des Siebbeins und der Pneumaticität bei den Ungulaten und Probosciden. Morphol. Jb. 28, 179–251.

    Google Scholar 

  • Paulli, S., 1900c. Über die Pneumaticität des Schädels bei den Säugetieren. Eine morphologische Studie. III. Über die Morphologie des Siebbeins und die Pneumaticität bei den Insectivoren, Hyracoideen, Chiropteren, Carnivoren, Pinnipeden, Edentaten, Rodentiern, Prosimiern und Primaten, nebst einer zusammenfassenden Übersicht über die Morphologie des Siebbeins und die der Pneumaticität des Schädels bei den Säugetieren. Morphol.Jb. 28, 483–564.

    Google Scholar 

  • Quignon, P., Rimbault, M., Robin, S., Galibert, F., 2012. Genetics of canine olfaction and receptor diversity. Mamm. Genome 23, 132–143.

    PubMed  Google Scholar 

  • R Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Reinbach, W., 1952a. Zur Entwicklung des Primordialcraniums von Dasypus novemcinctus LINNÉ (Tatusia novemcincta LESSON) I. Z. Morphol. Anthropol. 44, 375–444.

    Google Scholar 

  • Reinbach, W., 1952b. Zur Entwicklung des Primordialcraniums von Dasypus novemcinctus LINNÉ (Tatusia novemcincta LESSON) II. Z. Morphol. Anthropol. 45, 1–72.

    Google Scholar 

  • Robin, S., Tacher, S., Rimbault, M., Vaysse, A., Dréano, S., André, C., Hitte, C., Galibert, F., 2009. Genetic diversity of canine olfactory receptors. BMC Genomics 10, 21.

    PubMed  PubMed Central  Google Scholar 

  • Rowe, T.B., Eiting, T.P., Macrini, T.E., Ketcham, R.A., 2005. Organization of the olfactory and respiratory skeleton in the nose of the gray short-tailed Opossum Monodelphis domestica. J. Mamm. Evol. 12, 303–336.

    Google Scholar 

  • Ruf, I., 2004. Vergleichend-ontogenetische Untersuchungen an der Ethmoidalregion der Muroidea (Rodentia, Mammalia). Ein Beitrag zur Morphologie und Systematik der Nagetiere. Dissertation. Eberhard-Karls-Universität Tübingen, pp. 1–301 https://doi.org/nbn-resolving.de/urn:nbn:de:bsz:21-opus-13618.

    Google Scholar 

  • Ruf, I., 2014. Comparative anatomy and systematic implications of the turbinal skeleton in Lagomorpha (Mammalia). Anat. Rec. 297, 2031–2046.

    Google Scholar 

  • Ruf, I., Janßen, S., Zeller, U., 2015. The ethmoidal region of the skull ofPtilocerus lowii (Ptiloceridae, Scandentia, Mammalia) — a contribution to the reconstruction ofthe cranial morphotype of primates. Primate Biol. 2, 89–110.

    Google Scholar 

  • Schliemann, H., 1966. Zur Morphologie und Entwicklung des Craniums von Canis lupus f. familiaris L. Morphol.Jb. 109, 501–603.

    CAS  Google Scholar 

  • Schreider, J.P., Raabe, O.G., 1981. Anatomy ofthe nasal-pharyngeal airway of experimental animals. Anat. Rec. 200, 195–205.

    CAS  PubMed  Google Scholar 

  • Smith, T.D., Rossie, J.B., 2008. Nasal fossa of mouse and dwarf lemurs (Primates, Cheirogaleidae). Anat. Rec. 291, 895–915.

    Google Scholar 

  • Smith, T.D., Bhatnagar, K.P., Tuladhar, P., Burrows, A.M., 2004. Distribution of olfactory epithelium in the primate nasal cavity: are microsmia and macrosmia valid morphological concepts? Anat. Rec. 281, 1173–1181.

    Google Scholar 

  • Smith, T.D., Bhatnagar, K.P., Rossie, J.B., Docherty, B.A., Burrows, A.M., Cooper, G.M., Mooney, M.P., Siegel, M.I., 2007. Scaling ofthe first ethmoturbinal in nocturnal strepsirrhines: olfactory and respiratory surfaces. Anat. Rec. 290, 215–237.

    Google Scholar 

  • Tacher, S., Quignon, P., Rimbault, M., Dreano, S., Andre, C., Galibert, F., 2005. Olfactory receptor sequence polymorphism within and between breeds of dogs. J. Hered. 96, 812–816.

    CAS  PubMed  Google Scholar 

  • Van Valkenburgh, B., Theodor, J., Friscia, A., Pollack, A., Rowe, T., 2004. Respiratory turbinates of canids and felids: a quantitative comparison. J. Zool. 264, 281–293.

    Google Scholar 

  • Van Valkenburgh, B., Pang, B., Bird, D., Curtis, A., Yee, K., Wysocki, C., Craven, B.A., 2014. Respiratory and olfactory turbinals in feliform and caniform carnivorans: the influence of snout length. Anat. Rec. 297, 2065–2079.

    Google Scholar 

  • Voit, M., 1909. Das Primordialcranium des Kaninchens unter Berücksichtigung der Deckknochen. Ein Beitrag zur Morphologie des Säugetierschädels. Anat. Hefte 38, 425–616.

    Google Scholar 

  • vom Hagen, A., 1935. Die Hunderassen. Ein Handbuch für Hundeliebhaber und Züchter. Akademische Verlagsgesellschaft Athenaion M.B.H., Potsdam.

    Google Scholar 

  • Yang, M., Geng, G.J., Zhang, W., Cui, L., Zhang, H.X., Zheng, J.L., 2016. SNP genotypes of olfactory receptor genes associated with olfactory ability in German Shepherd dogs. Anim. Genet. 47, 240–244.

    CAS  PubMed  Google Scholar 

  • Young, A., Bannasch, D., 2006. Morphological variation in the dog. In: Ostrander, E., Giger, U., Lindblad-Toh, K. (Eds.), The Dog and its Genome. Cold Springer Harbor Laboratory Press, New York, pp. 47–65.

    Google Scholar 

  • Zeller, U., 1983. Zur Ontogenese und Morphologie des Craniums von Tupaia belangeri (Tupaiidae, Scandentia, Mammalia). Dissertation. Georg-August-Universitaet zu Goettingen, pp. 1–308.

    Google Scholar 

  • Zeller, U., 1989. Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Protheria: Monotremata). Abh. Senckenberg. Naturforsch. Ges. 545, 1–188.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Franziska Wagner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wagner, F., Ruf, I. Who nose the borzoi? Turbinal skeleton in a dolichocephalic dog breed (Canis lupus familiaris). Mamm Biol 94, 106–119 (2019). https://doi.org/10.1016/j.mambio.2018.06.005

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2018.06.005

Keywords

Navigation