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Australian Mammalogy Australian Mammalogy Society
Journal of the Australian Mammal Society
RESEARCH ARTICLE

Comparative tongue anatomy of the rakali (Hydromys chrysogaster) and greater stick-nest rat (Leporillus conditor) (Rodentia; Muridae)

Alexia Humphries A , Bernadette Seow A , Shriya Danee A , Bastian Ness A and Natalie Marina Warburton https://orcid.org/0000-0002-8498-3053 B *
+ Author Affiliations
- Author Affiliations

A School of Veterinary Medicine, Murdoch University, Murdoch, WA 6150, Australia.

B Centre for Terrestrial Ecosystems Science and Sustainability, Harry Butler Institute, Murdoch University, Building 250, 90 South Street Murdoch, WA 6150, Australia.

* Correspondence to: N.Warburton@murdoch.edu.adu.au

Handling Editor: Stewart Nicol

Australian Mammalogy 45(2) 210-219 https://doi.org/10.1071/AM22029
Submitted: 26 September 2022  Accepted: 16 December 2022   Published: 23 January 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Mammal Society.

Abstract

For many mammals, the tongue provides an important functional interface with the environment through roles including manipulating, ingesting, and mechanically processing food items. As such, the adaptations of the tongue reflect different physical properties of an animal’s diet. We sought to investigate whether adaptations of the tongue are apparent in two native Australian rodents that have divergent dietary niches: the semiaquatic and mixed feeding rakali (Hydromys chrysogaster) and the arid dwelling, herbivorous stick-nest rat (Leporillus conditor). Both species retained many lingual features typical of rodents. A notable difference was a large, annular pad surrounding the single circumvallate papilla in H. chrysogaster, suggesting an enhanced gustatory function, which would be consistent with adaptation to a semiaquatic, mixed diet. In contrast, L. conditor appeared to have reduced gustatory sensitivity and mechanical dexterity, consistent with crushing their preferred succulent plant forage and manipulating sticks for nest building. The descriptions provide a novel view of the evolution of soft tissues within Australian endemic rodents.

Keywords: circumvallate papilla, Conilurini, histology, Hydromyini, lingual papillae, Muridae, Rodentia, serous gustatory glands, taste buds.


References

Abayomi, T. A., Ofusori, D. A., Ayoka, O. A., Odukoya, S. A., Omotoso, E. O., Amegor, F. O., et al. (2009). A comparative histological study of the tongue of rat (Rattus norvegicus), bat (Eidolon helvum) and pangolin (Manis tricuspis). International Journal of Morphology 27, 1111–1119.
A comparative histological study of the tongue of rat (Rattus norvegicus), bat (Eidolon helvum) and pangolin (Manis tricuspis).Crossref | GoogleScholarGoogle Scholar |

Atkinson, C. A., Lund, M. A., and Morris, K. D. (2008). BiblioRakali: the Australian water rat, Hydromys chrysogaster Geoffroy, 1804 (Muridae: Hydromyinae), a subject-specific bibliography. Conservation Science Western Australia 7, 65–71.

Barclay, S. D., Costello, B., and Sherwin, W. B. (2006). Limited cross-species microsatellite amplification and the isolation and characterization of new microsatellite markers for the greater stick-nest rat (Leporillus conditor). Molecular Ecology Notes 6, 882–885.
Limited cross-species microsatellite amplification and the isolation and characterization of new microsatellite markers for the greater stick-nest rat (Leporillus conditor).Crossref | GoogleScholarGoogle Scholar |

Breed, A., and Eden, P. (2008). Rodents. In ‘Medicine of Australian Mammals’. (Eds L. Vogelnest, and R. Woods.) pp. 503–526. (CSIRO Publishing.)

Brignot, H., and Feron, G. (2019). Oral lipolysis and its association with diet and the perception and digestion of lipids: A systematic literature review. Archives of Oral Biology 108, 104550.
Oral lipolysis and its association with diet and the perception and digestion of lipids: A systematic literature review.Crossref | GoogleScholarGoogle Scholar |

Cizek, P., Hamouzova, P., Goździewska-Harłajczuk, K., Klećkowska-Nawrot, J., and Kvapil, P. (2022). Ultrastructure of the tongue in the African pygmy hedgehog (Atelerix albiventris), comparison within the family Erinaceidae. Acta Zoologica 103, 442–452.
Ultrastructure of the tongue in the African pygmy hedgehog (Atelerix albiventris), comparison within the family Erinaceidae.Crossref | GoogleScholarGoogle Scholar |

Copley, P. (1999). Natural histories of Australia’s stick-nest rats, genus Leporillus (Rodentia: Muridae). Wildlife Research 26, 513–539.
Natural histories of Australia’s stick-nest rats, genus Leporillus (Rodentia: Muridae).Crossref | GoogleScholarGoogle Scholar |

Dellmann, H. D., and Brown, E. M. (1983). Digestive system. In ‘Textbook of Veterinary Histology’, 3rd edn. pp. 212–216. (Lea and Febiger: Philadelphia, USA.)

Dyce, K. M., Sack, W. O., and Wensing, C. J. G. (2010). The digestive apparatus. In ‘Textbook of Veterinary Anatomy’, 4th edn. pp. 102–105. (Saunders: St. Louis, MO.)

El Bakary, N. E. R., and Abumandour, M. M. A. (2017). Morphological studies of the tongue of the Egyptian water buffalo (Bubalus bubalis) and their lingual papillae adaptation for its feeding habits. Anatomia, Histologia, Embryologia 46, 474–486.
Morphological studies of the tongue of the Egyptian water buffalo (Bubalus bubalis) and their lingual papillae adaptation for its feeding habits.Crossref | GoogleScholarGoogle Scholar |

El Bakary, N. E. R., and Emura, S. (2016). Morphology of the lingual papillae in the least weasel (Mustela nivalis). International Journal of Morphology 34, 305–309.
Morphology of the lingual papillae in the least weasel (Mustela nivalis).Crossref | GoogleScholarGoogle Scholar |

Emura, S., and Sugiyama, K. (2016). Morphology of the lingual papillae of the Asian short-clawed otter. Okajimas Folia Anatomica Japonica 93, 105–110.
Morphology of the lingual papillae of the Asian short-clawed otter.Crossref | GoogleScholarGoogle Scholar |

Erdoğan, S., Villar Arias, S., and Pérez, W. (2015). Morphology of the lingual surface of South American fur seal (Arctocephalus australis) and sea lion (Otaria flavescens). Microscopy Research and Technique 78, 140–147.
Morphology of the lingual surface of South American fur seal (Arctocephalus australis) and sea lion (Otaria flavescens).Crossref | GoogleScholarGoogle Scholar |

Fish, F. E., and Baudinette, R. V. (1999). Energetics of locomotion by the Australian water rat (Hydromys chrysogaster): a comparison of swimming and running in a semi-aquatic mammal. Journal of Experimental Biology 202, 353–363.
Energetics of locomotion by the Australian water rat (Hydromys chrysogaster): a comparison of swimming and running in a semi-aquatic mammal.Crossref | GoogleScholarGoogle Scholar |

Fleming, P. A., and Bateman, P. W. (2016). The good, the bad, and the ugly: which Australian terrestrial mammal species attract most research? Mammal Review 46, 241–254.
The good, the bad, and the ugly: which Australian terrestrial mammal species attract most research?Crossref | GoogleScholarGoogle Scholar |

Ford, F. (2006). A splitting headache: relationships and generic boundaries among Australian murids. Biological Journal of the Linnean Society 89, 117–138.
A splitting headache: relationships and generic boundaries among Australian murids.Crossref | GoogleScholarGoogle Scholar |

Ghoshal, N. G., and Bal, H. S. (1989). Comparative morphology of the stomach of some laboratory mammals. Laboratory Animals 23, 21–29.
Comparative morphology of the stomach of some laboratory mammals.Crossref | GoogleScholarGoogle Scholar |

Goździewska-Harłajczuk, K., Klećkowska-Nawrot, J., Barszcz, K., Marycz, K., Nawara, T., Modlińska, K., and Stryjek, R. (2018). Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study. Anatomical Science International 93, 514–532.
Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study.Crossref | GoogleScholarGoogle Scholar |

Halpern, B. P. (1977). Functional anatomy of the tongue and mouth of mammals. In ‘Drinking Behavior ’. (Eds A. W. M. Weijnen, and J. Mendelson.) pp. 1–92. (Springer: Boston.)

Iwasaki, S-i. (2002). Evolution of the structure and function of the vertebrate tongue. Journal of Anatomy 201, 1–13.
Evolution of the structure and function of the vertebrate tongue.Crossref | GoogleScholarGoogle Scholar |

Jackowiak, H., and Godynicki, S. (2005). The distribution and structure of the lingual papillae on the tongue of the bank vole Clethrionomys glareolus. Folia Morphologica 64, 326–333.

Karan, M., Yilmaz, S., and Aydin, A. (2011). Morphology of the filiform lingual papillae in porcupine (Hystrix cristata). Anatomia, Histologia, Embryologia 40, 100–103.
Morphology of the filiform lingual papillae in porcupine (Hystrix cristata).Crossref | GoogleScholarGoogle Scholar |

Kawai, T., and Fushiki, T. (2003). Importance of lipolysis in oral cavity for orosensory detection of fat. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 285, R447–R454.
Importance of lipolysis in oral cavity for orosensory detection of fat.Crossref | GoogleScholarGoogle Scholar |

Kemper, C. M., and Watts, C. H. (1989). Muridae. In ‘Fauna of Australia. Vol 1. Mammalia. Vol. 1’. (Eds D. W. Walton, and B. J. Richardson.) pp. 939–956. (AGPS Canberra)

Lawes, M. J., Fisher, D. O., Johnson, C. N., Blomberg, S. P., Frank, A. S. K., Fritz, S. A., et al. (2015). Correlates of Recent Declines of Rodents in Northern and Southern Australia: Habitat Structure Is Critical. PLoS One 10, e0130626.
Correlates of Recent Declines of Rodents in Northern and Southern Australia: Habitat Structure Is Critical.Crossref | GoogleScholarGoogle Scholar |

Massoud, D., and Abumandour, M. M. A. (2019). Descriptive studies on the tongue of two micro‐mammals inhabiting the Egyptian fauna; the Nile grass rat (Arvicanthis niloticus) and the Egyptian long‐eared hedgehog (Hemiechinus auritus). Microscopy Research and Technique 82, 1584–1592.
Descriptive studies on the tongue of two micro‐mammals inhabiting the Egyptian fauna; the Nile grass rat (Arvicanthis niloticus) and the Egyptian long‐eared hedgehog (Hemiechinus auritus).Crossref | GoogleScholarGoogle Scholar |

McCarthy, L., and Head, L. (2001). Holocene variability in semi-arid vegetation: new evidence from Leporillus middens from the Flinders Ranges, South Australia. The Holocene 11, 681–689.
Holocene variability in semi-arid vegetation: new evidence from Leporillus middens from the Flinders Ranges, South Australia.Crossref | GoogleScholarGoogle Scholar |

McCarthy, L., Head, L., and Quade, J. (1996). Holocene palaeoecology of the northern Flinders Ranges, South Australia, based on stick-nest rat (Leporillus spp.) middens: a preliminary overview. Palaeogeography, Palaeoclimatology, Palaeoecology 123, 205–218.
Holocene palaeoecology of the northern Flinders Ranges, South Australia, based on stick-nest rat (Leporillus spp.) middens: a preliminary overview.Crossref | GoogleScholarGoogle Scholar |

McClung, J. R., and Goldberg, S. J. (2000). Functional anatomy of the hypoglossal innervated muscles of the rat tongue: a model for elongation and protrusion of the mammalian tongue. The Anatomical Record 260, 378–386.
Functional anatomy of the hypoglossal innervated muscles of the rat tongue: a model for elongation and protrusion of the mammalian tongue.Crossref | GoogleScholarGoogle Scholar |

McNally, J. (1960). The biology of the Water Rat Hydromys chrysogaster Geoffroy (Muridae: Hudromyinae) in Victoria. Australian Journal of Zoology 8, 170–180.
The biology of the Water Rat Hydromys chrysogaster Geoffroy (Muridae: Hudromyinae) in Victoria.Crossref | GoogleScholarGoogle Scholar |

Miller, J. L., Watkin, K. L., and Chen, M. F. (2002). Muscle, adipose, and connective tissue variations in intrinsic musculature of the adult human tongue. Journal of Speech, Language, and Hearing Research 45, 51–65.
Muscle, adipose, and connective tissue variations in intrinsic musculature of the adult human tongue.Crossref | GoogleScholarGoogle Scholar |

Murray, B. R., Dickman, C. R., Watts, C. H. S., and Morton, S. R. (1999). The dietary ecology of Australian desert rodents. Wildlife Research 26, 421–437.
The dietary ecology of Australian desert rodents.Crossref | GoogleScholarGoogle Scholar |

Nonaka, K., Zheng, J. H., and Kobayashi, K. (2008). Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits. Okajimas Folia Anatomica Japonica 85, 57–66.
Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits.Crossref | GoogleScholarGoogle Scholar |

Olsen, P. D. (1995). Water-rat Hydromys chrysogaster. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 628–629. (Reed Books: Chatswood, NSW.)

Ryan, S. A., Moseby, K. E., and Paton, D. C. (2003). Comparative foraging preferences of the greater stick-nest rat Leporillus conditor and the European rabbit Oryctolagus cuniculus: implications for regeneration of arid lands. Australian Mammalogy 25, 135–146.
Comparative foraging preferences of the greater stick-nest rat Leporillus conditor and the European rabbit Oryctolagus cuniculus: implications for regeneration of arid lands.Crossref | GoogleScholarGoogle Scholar |

Sadeghinezhad, J., Tootian, Z., and Javadi, F. (2018). Anatomical and histological structure of the tongue and histochemical characteristics of the lingual salivary glands in the Persian squirrel (Sciurus anomalus). Anatomical Science International 93, 58–68.
Anatomical and histological structure of the tongue and histochemical characteristics of the lingual salivary glands in the Persian squirrel (Sciurus anomalus).Crossref | GoogleScholarGoogle Scholar |

Samuelson, D. A. (2007). Digestive system l: oral cavity and alimentary canal. In ‘Textbook of Veterinary Histology’, 1st edn. pp. 315–320. (Saunders: St. Louis, MO.)

Sclafani, A., and Ackroff, K. (2018). Role of lipolysis in postoral and oral fat preferences in mice. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 315, R434–R441.
Role of lipolysis in postoral and oral fat preferences in mice.Crossref | GoogleScholarGoogle Scholar |

Shindo, J., Yoshimura, K., and Kobayashi, K. (2006). Comparative morphological study on the stereo-structure of the lingual papillae and their connective tissue cores of the American beaver (Castor canadensis). Okajimas Folia Anatomica Japonica 82, 127–138.
Comparative morphological study on the stereo-structure of the lingual papillae and their connective tissue cores of the American beaver (Castor canadensis).Crossref | GoogleScholarGoogle Scholar |

Short, J., Copley, P., Ruykys, L., Morris, K., Read, J., and Moseby, K. (2019). Review of translocations of the greater stick-nest rat (Leporillus conditor): lessons learnt to facilitate ongoing recovery. Wildlife Research 46, 455–475.
Review of translocations of the greater stick-nest rat (Leporillus conditor): lessons learnt to facilitate ongoing recovery.Crossref | GoogleScholarGoogle Scholar |

Smith, A. P., and Quin, D. G. (1996). Patterns and causes of extinction and decline in Australian conilurine rodents. Biological Conservation 77, 243–267.
Patterns and causes of extinction and decline in Australian conilurine rodents.Crossref | GoogleScholarGoogle Scholar |

Sonntag, C. F. (1924). The comparative anatomy of the tongues of the Mammalia.—X. Rodentia. Proceedings of the Zoological Society of London 94, 725–741.
The comparative anatomy of the tongues of the Mammalia.—X. Rodentia.Crossref | GoogleScholarGoogle Scholar |

Stangl Jr, F. B., and Pfau, R. S. (1994). Gross morphology and distribution patterns of lingual papillae in some geomyid and heteromyid rodents. Paper presented at the Proceedings of the Oklahoma Academy of Science.

Wannaprasert, T., Phanthuma‐opas, P., and Jindatip, D. (2020). Morphology and microstructure of the tongue of the lesser bamboo rat (Cannomys badius). Acta Zoologica 101, 282–291.
Morphology and microstructure of the tongue of the lesser bamboo rat (Cannomys badius).Crossref | GoogleScholarGoogle Scholar |

Watts, C. H. S., and Aslin, H. J. (1981). Systematic treatment of stick-nest rats. In ‘The rodents of Australia’. pp. 144–151. (Angus & Robertson: Australia.)

Woollard, P., Vestjens, W. J. M., and MacLean, L. (1978). The Ecology of the Eastern Water Rat Hydromys chrysogaster at Griffith, N.S.W.: Food and Feeding Habits. Wildlife Research 5, 59–73.
The Ecology of the Eastern Water Rat Hydromys chrysogaster at Griffith, N.S.W.: Food and Feeding Habits.Crossref | GoogleScholarGoogle Scholar |

Yoshimura, K., Shindoh, J., and Kobayashi, K. (2002). Scanning electron microscopy study of the tongue and lingual papillae of the California sea lion (Zalophus californianus californianus). The Anatomical Record 267, 146–153.
Scanning electron microscopy study of the tongue and lingual papillae of the California sea lion (Zalophus californianus californianus).Crossref | GoogleScholarGoogle Scholar |

Yoshimura, K., Shindo, J., Miyawaki, Y., Kobayashi, K., and Kageyama, I. (2007). Scanning electron microscopic study on the tongue and lingual papillae of the adult spotted seal, Phoca largha. Okajimas Folia Anatomica Japonica 84, 83–98.
Scanning electron microscopic study on the tongue and lingual papillae of the adult spotted seal, Phoca largha.Crossref | GoogleScholarGoogle Scholar |

Yoshimura, K., Shindo, J., and Kageyama, I. (2018). Comparative morphology of the lingual papillae and their connective tissue cores in the tongue of Pallas’s squirrel (Callosciurus erythraeus thai, Kloss, 1917). Zoological Science 35, 353–359.
Comparative morphology of the lingual papillae and their connective tissue cores in the tongue of Pallas’s squirrel (Callosciurus erythraeus thai, Kloss, 1917).Crossref | GoogleScholarGoogle Scholar |