Growth and wear of incisor and cheek teeth in domestic rabbits (Oryctolagus cuniculus) fed diets of different abrasiveness

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 321, Issue 5, 2014, Pages 283-298

  Müller, Jacqueline ^a   Clauss, Marcus ^a   Codron, Daryl ^a,b   Schulz, Ellen ^c   Hummel, Jürgen ^d   Fortelius, Mikael ^e   Kircher, Patrick ^a   Hatt, Jean Michel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b NATIONAL MUSEUM   (South Africa)

^c UNIVERSITY OF HAMBURG   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ORYCTOLAGUS CUNICULUS;

ANIMAL; ANIMAL FOOD; DIET; GROWTH, DEVELOPMENT AND AGING; MASTICATION; PATHOLOGY; RABBIT; TOOTH; TOOTH DISEASE; VETERINARY;

ANIMAL FEED; ANIMALS; DIET; MASTICATION; RABBITS; TOOTH; TOOTH WEAR;

EID: 84899898486     PISSN: 19325223     EISSN: 19325231     Source Type: Journal    
DOI: 10.1002/jez.1864     Document Type: Article

References (98)

1. Boehmer E, Koestlin RG. 1988. Zahnerkrankungen bzw.-anomalien bei Hasenartigen und Nagern. Prakt Tierarzt 11:37-50.
2. Butler PM. 1972. Some functional aspects of molar evolution. Evolution 26:474-483.
3. Capello V. 2008. Diagnosis and treatment of dental disease in pet rodents. J Exotic Pet Med 17:114-123.
4. Capello V, Cauduro A. 2008. Clinical technique: application of computed tomography for diagnosis of dental disease in the rabbit, guinea pig, and chinchilla. J Exotic Pet Med 17:93-101.
5. Clauss M. 2012. Clinical technique: feeding hay to rabbits and rodents. J Exotic Pet Med 21:80-86.
6. Clauss M, Franz-Odendaal TA, Brasch J, Castell JC, Kaiser TM. 2007. Tooth wear in captive giraffes (Giraffa camelopardalis): mesowear analysis classifies free-ranging specimens as browsers but captive ones as grazers. J Zoo Wildl Med 38:433-445.
7. Clauss M, Hofmann RR, Streich WJ, Fickel J, Hummel J. 2008. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157:377-385.
8. Crossley DA. 1995. Clinical aspects of lagomorph dental anatomy: the rabbit (Oryctolagus cuniculus). J Vet Dent 12:137-140.
9. Crossley DA. 2000. Rodent and rabbit radiology. In: DeForge DH, Colmery BH, editors. An atlas of veterinary dental radiology. Ames, IA: Iowa State University Press, p. 247-259.
10. Crossley DA. 2003. Oral biology and disorders of lagomorphs. Vet Clin North Am Exotic Anim Pract 6:629-659.
11. Damuth J, Janis CM. 2011. On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biol Rev 86:733-758.
12. Damuth J, Janis CM. 2014. A comparison of observed molar wear rates in extant herbivorous mammals. Ann Zool Fenn 51:188-200.
13. Erickson KL. 2014. Prairie grass phytolith hardness and the evolution of ungulate hypsodonty. Hist Biol (in press) doi 10.1080/08912963.2013.841155.
14. Fortelius M. 1985. Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zool Fenn 180:1-76.
15. Fortelius M, Solounias N. 2000. Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets. Am Mus Nov 3301:1-36.
16. Franz-Odendaal TA, Kaiser TM. 2003. Differential mesowear in the maxillary and mandibular cheek dentition of some ruminants (Artiodactyla). Ann Zool Fenn 40:395-410.
17. Fritz J, Hummel J, Kienzle E, et al. 2009. Comparative chewing efficiency in mammalian herbivores. Oikos 118:1623-1632.
18. Fritz J, Streich WJ, Schwarm A, Clauss M. 2012. Condensing results of wet sieving analyses into a single data: a comparison of methods for particle size description. J Anim Physiol Anim Nutr 96:783-797.
19. Harcourt-Brown FM. 1995. A review of clinical conditions in pet rabbits associated with their teeth. Vet Rec 137:341-346.
20. Harcourt-Brown FM. 1996. Calcium deficiency, diet and dental disease in pet rabbits. Vet Rec 139:567-571.
21. Harcourt-Brown F. 2009. Dental disease in pet rabbits 1. Normal dentition, pathogenesis and aetiology. In Pract 31:370-379.
22. Harkness JE, Turner PV, VandeWoude S, Wheler CL. 2010. Harkness and Wagner's biology and medicine of rabbits and rodents. Ames, IA: Blackwell Publishing.
23. Healy WB, Ludwig TG. 1965. Wear of sheep's teeth: I. The role of ingested soil. N Z J Agric Res 8:737-752.
24. Healy WB, Cutress TW, Michie C. 1967. Wear of sheep's teeth: IV. Reduction of soil ingestion and tooth wear by supplementary feeding. N Z J Agric Res 10:201-209.
25. Hummel J, Findeisen E, Südekum K-H, et al. 2011. Another one bites the dust: faecal silica levels in large herbivores correlate with high-crowned teeth. Proc R Soc B 278:1742-1747.
26. Jekl V, Redrobe S. 2013. Rabbit dental disease and calcium metabolism - the science behind divided opinions. J Small Anim Pract 54:481-490.
27. Jekl V, Hauptman K, Knotek Z. 2008. Quantitative and qualitative assessments of intraoral lesions in 180 small herbivorous mammals. Vet Rec 162:442-449.
28. Jekl V, Gumpenberger M, Jeklova E, et al. 2011a. Impact of pelleted diets with different mineral compositions on the crown size of mandibular cheek teeth and mandibular relative density in degus (Octodon degus). Vet Rec 168:641.
29. Jekl V, Krejcirova L, Buchtova M, Knotek Z. 2011b. Effect of high phosphorus diet on tooth microstructure of rodent incisors. Bone 49:479-484.
30. Kaiser TM, Fortelius M. 2003. Differential mesowear in occluding upper and lower molars: opening mesowear analysis for lower molars and premolars in hypsodont horses. J Morphol 258:67-83.
31. Kaiser TM, Brasch J, Castell JC, Schulz E, Clauss M. 2009. Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics. Mamm Biol 74:425-437.
32. Kaiser TM, Fickel J, Streich WJ, Hummel J, Clauss M. 2010. Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. J Zool 281:12-25.
33. Kaiser TM, Müller DWH, Fortelius M, et al. 2013. Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Rev 43:34-46.
34. Kojola I, Helle T, Huhta E, Niva A. 1998. Foraging conditions, tooth wear and herbivore body reserves: a study of female reindeer. Oecologia 117:26-30.
35. Langenecker M, Clauss M, Hässig M, Hatt J-M. 2009. Vergleichende Untersuchung zur Krankheitsverteilung bei Kaninchen, Meerschweinchen, Ratten und Frettchen. Tierärztl Praxis 37:326-333.
36. Lennox AM. 2008. Diagnosis and treatment of dental disease in pet rabbits. J Exotic Pet Med 17:107-113.
37. Lobprise HB, Wiggs RB. 1991. Dental and oral disease in lagomorphs. J Vet Dent 8:11-17.
38. Loe LE, Bonenfant C, Langvatn R, et al. 2006. Increased effect of harsh climate in red deer with a poor set of teeth. Oecologia 147:24-30.
39. Lord B. 2011. Dental disease in the rabbit Part 1: normal dentition and diet. Companion Anim 16:53-55.
40. Lucas PW. 1979. The dental-dietary adaptations of mammals. Neues Jahrb Geol Palaeontol Monatsh 8:486-516.
41. Lucas PW, Omar R, Al-Fadhalah K, et al. 2013. Mechanisms and causes of wear in tooth enamel: implications for hominin diets. J Roy Soc Int 10:20120923.
42. Ludwig TG, Healy WB, Cutress TW. 1966. Wear of sheep's teeth: III. Seasonal variation in wear and ingested soil. N Z J Agric Res 9:157-164.
43. Mainland IL. 2000. A dental microwear study of seaweed eating and grazing sheep from Orkney. Int J Osteoarchaeol 10:93-107.
44. Mainland IL. 2003a. Dental microwear in grazing and browsing Gotland sheep (Ovis aries) and its implications for dietary reconstruction. J Archaeol Sci 30:1513-1527.
45. Mainland IL. 2003b. Dental microwear in modern Greek ovicaprids: identifying microwear signatures associated with a diet of leafy-hay. Br School Athens Stud 9:45-50.
46. Mainland IL. 2006. Pastures lost? A dental microwear study of ovicaprine diet and management in Norse Greenland. J Archaeol Sci 33:238-252.
47. Martin Jurado O, Clauss M, Hatt J-M. 2008. Irregular tooth wear and longevity in captive wild ruminants: a pilot survey of necropsy reports. J Zoo Wildl Med 39:69-75.
48. Merceron G, Escarguel G, Angibault JM, Verheyden-Tixier H. 2010. Can dental microwear textures record inter-individual dietary variations? PLoS ONE 5:e9542.
49. Meredith A. 2007. Rabbit dentistry. Eur J Companion Anim Pract 17:55-62.
50. Mosallanejad B, Moarrabi A, Avizeh R, Ghadiri A. 2010. Prevalence of dental malocclusion and root elongation in pet rabbits at Ahvaz, Iran. Iran J Vet Sci Technol 2:109-116.
51. Mullan SM, Main DCJ. 2006. Survey of the husbandry, health and welfare of 102 pet rabbits. Vet Rec 159:103-109.
52. Ness AR. 1956. The response of the rabbit mandibular incisor to experimental shortening and to the prevention of its eruption. Proc R Soc B 146:129-154.
53. Prebble JL, Meredith AL. 2014. Food and water intake and selective feeding in rabbits on four feeding regimes. J Anim Physiol Anim Nutr. Available online ahead of print: doi: 10.1111/jpn.12163.
54. Rabenold D, Pearson OM. 2011. Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei. PLoS ONE 6:e28379.
55. Rabenold D, Pearson OM. 2014. Scratching the surface: A critique of Lucas et al. (2013)'s conclusion that phytoliths do not abrade enamel. J Hum Evol (in press) doi 10.1016/j.jhevol.2014.02.001.
56. Rensberger JM. 1975. Function in the cheek tooth evolution of some hypsodont geomyid rodents. J Paleontol 49:10-22.
57. Rensberger J. 1986. Early chewing mechanisms in mammalian herbivores. Palaeobiol 12:474-494.
58. Rinaldi C, Cole TM. 2004. Environmental seasonality and incremental growth rates of beaver (Castor canadensis) incisors: impications for palaeobiology. Palaeogeogr Palaeoclimatol Palaeoecol 206:289-301.
59. Rodrigues HG, Merceron G, Viriot L. 2009. Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): ecological implications. Naturwiss 96:537-542.
60. Sanson GD, Kerr SA, Gross KA. 2007. Do silica phytoliths really wear mammalian teeth? J Archaeol Sci 34:526-531.
61. Sarnat BG, Hook WE. 1942. Effects of hibernation on tooth developement. Anat Rec 38:471-493.
62. Schmidt-Kittler N. 2002. Feeding specializations in rodents. Senck Leth 82:141-152.
63. Schour I, Medak H. 1951. Experimental increase in rate of eruption and growth of rat incisors by eliminating attrition. J Dent Res 30:521.
64. Schulz E, Calandra I, Kaiser TM. 2010. Applying tribology to teeth of hoofed mammals. Scanning 32:162-182.
65. Schulz E, Piotrowski V, Clauss M, et al. 2013. Dietary abrasiveness Is associated with variability of microwear and dental surface texture in rabbits. PLoS ONE 8:e56167.
66. Schumacher M. 2011. Measurement of clinical crown length of incisor and premolar teeth in clinically healthy rabbits. J Vet Dent 28:90-95.
67. Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M. 2009. More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comp Biochem Physiol A 152:504-512.
68. Scott JR. 2012. Dental microwear texture analysis of extant African Bovidae. Mammalia 6:157-174.
69. Scott RS, Teaford MF, Ungar PS. 2012. Dental microwear texture and anthropoid diets. Am J Phys Anthropol 147:551-579.
70. Shadle AR. 1936. The attrition and extrusive growth of the four major incisor teeth of domestic rabbits. J Mammal 17:15-21.
71. Skogland T. 1988. Tooth wear by food limitation and its life history consequences in wild reindeer. Oikos 51:238-242.
72. Solounias N, Tariq M, Hou S, Danowitz M, Harrison M. 2014. A new method of tooth mesowear and a test of it on domestic goats. Ann Zool Fenn 51:111-118.
73. Spannbrucker D, Schmidtke D, Schmidtke HO. 1977. Anomalien der Backenzähne bei Zwergkaninchen und Meerschweinchen. Kleintierpraxis 22:331-334.
74. Statsoft_Inc. 2007. STATISTICA V8.0 (data analysis software system).
75. Strömberg CAE. 2004. Using phytolith assemblages to reconstruct the origin and spread of grass-dominated habitats in the great plains of North America during the late Eocene to early Miocene. Palaeogeogr Palaeoclimatol Palaeoecol 207:239-275.
76. Taylor LA, Kaiser TM, Schwitzer C, et al. 2013. Detecting inter-cusp and inter-tooth wear patterns in Rhinocerotids. PLoS ONE 8:e80921.
77. Taylor LA, Müller DHW, Schwitzer C, et al. 2014. Tooth wear in captive rhinos differs from that of free-ranging conspecifics. Contrib Zool 83:107-117.
78. Thenius E. 1989. Zähne und Gebiss der Säugetiere. Berlin/New York: De Gruyter.
79. Ungar PS. 2010. Mammal teeth: origin, evolution and diversity. Baltimore, MD: John Hopkins University Press.
80. Ungar PS, Brown CA, Bergstrom TS, Walker A. 2003. Quantification of dental microwear by tandem confocal microscopy and scalesensitive fractal analyses. Scanning 25:185-193.
81. Van Caelenberg A, De Rycke L, Hermans K, et al. 2008. Diagnosis of dental problems in pet rabbits (Oryctolagus cuniculus). Vlaams Diergeneesk Tijdschr 77:386-394.
82. Van Caelenberg AI, De Rycke LM, Hermans K, et al. 2010. Computed tomography and cross-sectional anatomy of the head in healthy rabbits. Am J Vet Res 71:293-303.
83. Van Caelenberg AI, De Rycke LM, Hermans K, et al. 2011. Comparison of radiography and CT to identify changes in the skull of four rabbits with dental disease. J Vet Dent 28:172-181.
84. Van Soest PJ, Robertson JB, Lewis BA. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583-3597.
85. VDLUFA. 2007. Verband Deutscher Landwirtschaftlicher Untersuchungs- und Forschungsanstalten. Handbuch der Landwirtschaftlichen Versuchs- und Untersuchungsmethodik (VDLUFA-Methodenbuch), Bd. III. Die Chemische Untersuchung von Futtermitteln. Darmstadt, Germany: VDLUFA-Verlag.
86. Veiberg V, Mysterud A, Gaillard JM, et al. 2007. Bigger teeth for longer life? Longevity and molar height in two roe deer populations. Biol Lett 3:268-270.
87. von Koenigswald WV. 1996. Die Zahl der Schmelzschichten in den Inzisiven bei den Lagomorpha und ihre systematische Bedeutung. Bonner Zool Beitr 46:33-57.
88. von Koenigswald W, Golenishev FN. 1979. A method for determining growth rates in continuously growing molars. J Mammal 60:397-400.
89. von Koenigswald W, Anders U, Engels S, Schultz JA, Ruf I. 2010. Tooth morphology in fossil and extant Lagomorpha (Mammalia) reflects different mastication patterns. J Mamm Evol 17:275-299.
90. Walker A, Hoeck HN, Perez L. 1978. Microwear of mammalian teeth as an indicator of diet. Science 201:908-910.
91. Ward J, Mainland IL. 1999. Microwear in modern rooting and stall-fed pigs: the potential of dental microwear analysis for exploring pig diet and management in the past. Environ Archaeol 4:25-32.
92. Weijs WA, Dantuma R. 1981. Functional anatomy of the masticatory apparatus in the rabbit (Oryctolagus cuniculi). Neth J Zool 31:99-147.
93. Weijs WA, Brugman P, Grimbergen CA. 1989. Jaw movements and muscle activity during mastication in growing rabbits. Anat Rec 224:407-416.
94. Williams SH, Kay RF. 2001. A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. J Mamm Evol 8:207-229.
95. Wöhlbier W. 1983. Handelsfuttermittel. Band 2. Teil A Futtermittel pflanzlicher Herkunft. Stuttgart, Germany: Eugen Ulmer.
96. Wolf P, Kamphues J. 1995. Probleme der art- und bedarfsgerechten Ernährung kleiner Nager als Heimtiere. Prakt Tierarzt 88:1088-1092.
97. Wolf P, Kamphues J. 1996. Untersuchungen zu Fütterungseinflüssen auf die Entwicklung der Incisivi bei Kaninchen, Chinchilla und Ratte. Kleintierpraxis 10:723-732.
98. Wolf P, Bucher L, Kamphues J. 1999. Die Futter-, Energie- und Wasseraufnahme von Zwergkaninchen unter praxisüblichen Fütterungsbedingungen. Kleintierpraxis 44:235-312.