Ontogenetic allometry of the Beagle

BMC Veterinary Research

Nadja Schilling²  Ingo Nolte¹  Patrick Wefstaedt¹  Daniela Helmsmüller¹ 

[1] Small Animal Clinic, University of Veterinary Medicine Hannover, Foundation, Bünteweg 9, 30559 Hannover, Germany;Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-University, Erbertstr. 1, 07743 Jena, Germany

关键词: Body mass;    Serial homology;    Bone growth;    Body proportions;    Limb proportions;    Scaling;   

Others  :  1119435
DOI  :  10.1186/1746-6148-9-203

 received in 2012-09-14, accepted in 2013-10-07,  发布年份 2013

【 摘 要 】

Background

Mammalian juveniles undergo dramatic changes in body conformation during development. As one of the most common companion animals, the time line and trajectory of a dog’s development and its body’s re-proportioning is of particular scientific interest. Several ontogenetic studies have investigated the skeletal development in dogs, but none has paid heed to the scapula as a critical part of the mammalian forelimb. Its functional integration into the forelimb changed the correspondence between fore- and hindlimb segments and previous ontogenetic studies observed more similar growth patterns for functionally than serially homologous elements. In this study, the ontogenetic development of six Beagle siblings was monitored between 9 and 51 weeks of age to investigate their skeletal allometry and compare this with data from other lines, breeds and species.

Results

Body mass increased exponentially with time; log linear increase was observed up to the age of 15 weeks. Compared with body mass, withers and pelvic height as well as the lengths of the trunk, scapula, brachium and antebrachium, femur and crus exhibited positive allometry. Trunk circumference and pes showed negative allometry in all, pelvis and manus in most dogs. Thus, the typical mammalian intralimb re-proportioning with the proximal limb elements exhibiting positive allometry and the very distal ones showing negative allometry was observed. Relative lengths of the antebrachium, femur and crus increased, while those of the distal elements decreased.

Conclusions

Beagles are fully-grown regarding body height but not body mass at about one year of age. Particular attention should be paid to feeding and physical exertion during the first 15 weeks when they grow more intensively. Compared with its siblings, a puppy’s size at 9 weeks is a good indicator for its final size. Among siblings, growth duration may vary substantially and appears not to be related to the adult size. Within breeds, a longer time to physically mature is hypothesized for larger-bodied breeding lines. Similar to other mammals, the Beagle displayed nearly optimal intralimb proportions throughout development. Neither the forelimbs nor the hindlimbs conformed with the previously observed proximo-distal order of the limb segment’s growth gradients. Potential factors responsible for variations in the ontogenetic allometry of mammals need further evaluation.

【 授权许可】

   
2013 Helmsmüller et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]McMahon TA: Size and shape in biology. Science 1973, 179:1201-1204.
• [2]Peters SE: Postnatal development of gait behavior and functional allometry in domestic cat (Felis catus). J Zool (Lond) 1983, 199:461-486.
• [3]Carrier DR: Ontogenetic limits on locomotor performance. Physiol Zool 1996, 69:467-488.
• [4]Shapiro LJ, Young JW: Kinematics of quadrupedal locomotion in sugar gliders (Petaurus breviceps): effects of age and substrate size. J Exp Biol 2012, 215:480-496.
• [5]Lumer H: Evolutionary allometry in the skeleton of the domesticated dog. Am Nat 1940, 74:439-467.
• [6]Casinos A, Bou J, Castiella MJ, Viladiu C: On the allometry of long bones in dogs (Canis familiaris). J Morph 1986, 190:73-79.
• [7]Chase K, Carrier DR, Adler FR, Jarvik T, Ostrander EA, Lorentzen TD, Lark KG: Genetic basis for systems of skeletal quantitative traits: Principal component analysis of the canid skeleton. PNAS 2002, 99:9930-9935.
• [8]McLain RF, Yerby SA, Moseley TA: Comparative morphometry of L4 vertebrae: comparison of large animal models for the human lumbar spine. Spine 2002, 27:200-206.
• [9]Carrier DR, Chase K, Lark KG: Genetics of canid skeletal variation: size and shape of the pelvis. Genome Res 2005, 15:1825-1830.
• [10]Ocal MK, Ortance OC, Parin U: A quantitative study on the sacrum of the dog. Ann Anat 2006, 188:477-482.
• [11]Drake AG, Klingenberg CP: The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc Royal Soc Biol Sci Ser B 2008, 275:71-76.
• [12]Quignon P, Schoenebeck JJ, Chase K, Parker HG, Mosher DS, Johnson GS, Lark KG, Ostrander EA: Fine mapping a locus controlling leg morphology in the domestic dog. Cold Spring Harb Symp Quant Biol 2009, 74:327-333.
• [13]Delaquerriere-Richardson L, Anderson C, Jorch UM, Cook M: Radiographic studies on bone in Beagles subjected to low levels of dietary lead since birth. Vet Hum Toxicol 1982, 24:401-405.
• [14]Kealy RD, Lawler DF, Ballam JM, Lust G, Smith GK, Biery DN, Olsson SE: Five-year longitudinal study on limited food consumption and development of osteoarthritis in coxofemoral joints of dogs. J Am Vet Med Assoc 1997, 210:222-225.
• [15]Henschel E: Zur Anatomie und Klinik der wachsenden Unterarmknochen. Arch Exp Vet Med 1972, 26:741-787.
• [16]Olson NC, Carrig CB, Brinker WO: Asynchronous growth of the canine radius and ulna: effects of retardation of longitudinal growth of the radius. Am J Vet Res 1979, 40:351-355.
• [17]Vanden Berg-Foels WS, Todhunter RJ, Schwager SJ, Reeves AP: Effect of early postnatal body weight on femoral head ossification onset and hip osteoarthritis in a canine model of developmental dysplasia of the hip. Pediat Res 2006, 60:549-554.
• [18]Weise G: Über das Wachstum verschiedener Hunderassen. Z Säugetierk 1964, 257-282.
• [19]Yonamine H, Ogi N, Ishikawa T, Ichiki H: Radiographic studies on skeletal growth of the pectoral limb of the Beagle. Jpn J Vet Sci 1980, 42:417-425.
• [20]Conzemius MG, Smith GK, Brighton CT, Marion MJ, Gregor TP: Analysis of physeal growth in dogs, using biplanar radiography. Am J Vet Res 1994, 55:22-27.
• [21]Salomon F-V, Schulze A, Böhme U, Arnold U, Gericke A, Gille U: Das postnatale Wachstum des Skeletts und der Körpermasse beim Beagle. Anat Histol Embryol 1999, 28:221-228.
• [22]Schulze A, Kaiser M, Gille U, Salomon F-V: Vergleichende Untersuchung zum postnatalen Wachstum der Vordergliedmaße verschiedener Hunderassen. Tierärztl Prax Kleint 2003, 4:219-224.
• [23]Schulze A, Gille U, Vom Stein S, Salomon F-V: Vergleichende Untersuchungen zum postnatalen Wachstum der Hintergliedmaßen verschiedener Hunderassen. Tierärztl Prax Kleint 2007, 3:200-205.
• [24]Hawthorne AJ, Booles D, Nugent PA, Gettinby G, Wilkinson J: Body-weight changes during growth in puppies of different breeds. J Nutr 2004, 134:S2027-S2030.
• [25]Schmidt M, Fischer MS: Morphological integration in mammalian limb proportions: Dissociation between function and development. Evolution 2009, 63:749-766.
• [26]Fischer MS: Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea). J Hum Evol 1994, 26:501-524.
• [27]Fischer MS, Schilling N, Schmidt M, Haarhaus D, Witte HF: Basic limb kinematics of small therian mammals. J Exp Biol 2002, 205:1315-1338.
• [28]Lilje KE, Tardieu C, Fischer MS: Scaling of long bones of ruminants with respect to the scapula. J Zool Syst Evol Res 2003, 41:118-126.
• [29]Richmond RJ, Berg RT: Bone growth and distribution in swine as influenced by live weight, breed, sex, and ration. Can J Anim Sci 1972, 52:47-56.
• [30]Carrier DR: Postnatal ontogeny of the musculo-skeletal system in the Black-tailed jack rabbit (Lepus californicus). J Zool (Lond) 1983, 201:27-55.
• [31]Roth VL: How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species. J Vert Paleontol 1984, 4:126-145.
• [32]Schilling N, Petrovitch A: Postnatal allometry of the skeleton of Tupaia glis (Scandentia: Tupaiidae) and Galea musteloides (Rodentia: Caviidae) - a test of the three-segment limb hypothesis. Zoology 2006, 109:148-163.
• [33]Lammers AR, German RZ: Ontogenetic allometry in the locomotor skeleton of specialized half-bounding mammals. J Zool (Lond) 2002, 258:485-495.
• [34]Seyfarth A, Günther M, Blickhan R: Stable operation of an elastic three-segment leg. Biol Cybern 2001, 84:365-382.
• [35]Prittie J: Canine parvoviral enteritis: a review of diagnosis, management, and prevention. J Vet Emerg Crit Care 2004, 14:167-176.
• [36]Helmink SK, Shanks RD, Leighton EA: Breed and sex differences in growth curves for two breeds of dog guides. J Anim Sci 2000, 78:27-32.
• [37]Sokal RR, Rohlf FJ: Biometry: The principles and practices of statistics in biological research. 2nd edition. New York: WH Freemann; 1981:1-859.
• [38]Zar JH: Calculation and miscalculation of the allometric equation as a model in biological data. BioScience 1968, 18:1118-1120.
• [39]Schulze A, Gille U, Salomon F-V: Untersuchungen zum postnatalen Skelett- und Körpermassewachstum von Hunden der Rasse Deutsche Dogge. Tierärztl Prax Kleint 2001, 29:358-365.
• [40]Skoglund S: On the postnatal development of postural mechanisms as revealed by electromyography and myography in decerebrate kittens. Acta Physiol Scand 1960, 49:299-371.
• [41]Altman J, Sudarshan K: Postnatal development of locomotion in the laboratory rat. Anim Behav 1975, 23:896-920.
• [42]Geisler HC, Westerga J, Gramsbergen A: Development of posture in the rat. Acta Neurobiol Exp 1993, 53:517-523.
• [43]Cazalet JR, Menard I, Cremieux J, Clarac F: Variability as a characteristic of immature motor system: an electromyographic study of swimming in the newborn rat. Behav Brain Res 1990, 40:215-225.
• [44]Schulze A, Salomon F-V: Das postnatale Wachstum der Gliedmaßenknochen bei Hunden der Rasse Deutsche Dogge. Kleintierpraxis 2001, 46:475-486.
• [45]Taylor AB: Relative growth, ontogeny, and sexual dimorphism in Gorilla (Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological considerations. Am J Primatol 1997, 43:1-31.
• [46]Lumer H, Schultz AH: Relative growth of the limb segments and tail in Ateles geoffroyi and Cebus capucinus. Hum Biol 1947, 19:53-67.
• [47]Jungers WL, Fleagle JG: Postnatal growth allometry of the extremities in Cebus albifrons and Cebus apella: a longitudinal and comparative study. Am J Phys Anthrop 1980, 53:471-478.
• [48]Maunz M, German RZ: Ontogeny and limb bone scaling in two New World marsupials, Monodelphis domestica and Didelphis virginiana. J Morph 1997, 231:117-130.
• [49]Turnquist JE, Wells JP: Ontogeny of locomotion in rhesus macaques (Macaca mulatta): I. Early postnatal ontogeny of the muskuloskeletal system. J Hum Evol 1994, 26:487-499.
• [50]Watkins MA, German RZ: Ontogenetic allometry of ossified fetal limb bones. Growth Dev Aging 1992, 56:259-267.
• [51]Glassman DM: The relation of long bone diaphyseal length to chronological age in immature saddle-back tamarius, Saguinus fuscicollis. Primates 1984, 25:352-361.
• [52]Günther M, Keppler V, Seyfarth A, Blickhan R: Human leg design: optimal axial alignment under constraints. J Math Biol 2004, 48:623-646.
• [53]Fischer MS, Witte H: The functional morphology of the three-segmented limb of mammals and its specialities in small and medium-sized mammals. Proc Eur Mechanics Coll Euromech, Biol and Technol Walking 1998, 375:10-17.
• [54]Fischer MS, Lilje KE: Hunde in Bewegung. Kosmos Verlag 2011, 1-207.