Why do heavy littermates grow better than lighter ones? A study in wild and domestic European rabbits

Physiology and Behavior

Volumn 95, Issue 3, 2008, Pages 441-448

  Rödel, Heiko G ^a   Bautista, Amando ^b   García Torres, Esmeralda ^b   Martínez Gómez, Margarita ^b,c   Hudson, Robyn ^c  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b CENTRO TLAXCALA DE BIOLOGÍA DE LA CONDUCTA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Body mass; Early development; Individual differences; Oryctolagus cuniculus; Sibling competition; Thermoregulation

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL HOUSING; ARTICLE; BEHAVIOR; BIRTH WEIGHT; BODY MASS; BODY TEMPERATURE; CONTROLLED STUDY; CORRELATION ANALYSIS; DOMESTIC ANIMAL; ENVIRONMENTAL FACTOR; FEMALE; FOOD INTAKE; GROWTH RATE; MALE; MILK; NEWBORN; NONHUMAN; ORYCTOLAGUS CUNICULUS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RABBIT; WILD ANIMAL;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BODY MASS INDEX; BODY TEMPERATURE; BODY WEIGHT; EATING; ENVIRONMENT; LITTER SIZE; MILK; RABBITS; TIME FACTORS;

EID: 52949083603     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2008.07.011     Document Type: Article

References (65)

1. Arendt J.D. Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72 (1997) 149-177
2. Argente M.J., Santacreu M.A., Climent A., and Blasco A. Relationship between uterine and fetal traits in rabbits selected on uterine capacity. J Anim Sci 81 (2003) 1265-1273
3. Bates D. Fitting linear mixed models in R. R News 5 (2005) 27-39
4. Bautista A., Drummond H., Martínez-Gómez M., and Hudson R. Thermal benefit of sibling presence in the newborn rabbit. Dev Psychobiol 43 (2003) 208-215
5. Bautista A., Mendoza-Degante M., Coureaud G., Martínez-Gómez M., and Hudson R. Scramble competition in newborn domestic rabbits for an unusually restricted milk supply. Anim Behav 70 (2005) 1011-1021
6. Bautista A., García-Torres E., Martínez-Gómez M., and Hudson R. Do newborn domestic rabbits Oryctolagus cuniculus compete for thermally advantageous positions in the litter huddle?. Behav Ecol Sociobiol 62 (2008) 331-339
7. Bernard E., and Hull D. The effects of the environmental temperature on the growth of new-born rabbits reared in incubators. Biol Neonate 7 (1964) 172-178
8. Blumberg M.S., and Sokoloff G. Thermoregulatory competence and behavioral expression in the young of altricial species - revisited. Dev Psychobiol 33 (1998) 107-123
9. Case T.J. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 53 (1978) 243-282
10. Coureaud G., Schaal B., Coudert P., Hudson R., Rideaud P., and Orgeur P. Mimicking natural nursing conditions promotes early pup survival in domestic rabbits. Ethology 106 (2000) 207-225
11. Coureaud G., Schaal B., Coudert P., Rideaud P., Fortun-Lamothe L., Hudson R., et al. Immediate postnatal suckling in the rabbit: its influence on pup survival and growth. Reprod Nutr Dev 40 (2000) 19-32
12. Coureaud G., Fortun-Lamothe L., Langlois D., and Schaal B. The reactivity of neonatal rabbits to the mammary pheromone as a probe for viability. Animal 1 (2007) 1026-1032
13. Corbet G.B. Taxonomy and origins. In: Thompson H.V., and King C.M. (Eds). The European rabbit. The history and biology of a successful colonizer (1994), Oxford University Press, Oxford 1-7
14. Dobson S.F., Risch T.S., and Murie J.O. Increasing returns in the life history of Columbian ground squirrels. J Anim Ecol 68 (1999) 73-86
15. Drake A., Fraser D., and Weary D.M. Parent-offspring resource allocation in domestic pigs. Behav Ecol Sociobiol 62 (2008) 309-319
16. Drummond H., Vázquez E., Sánchez-Colón S., Martínez-Gómez M., and Hudson R. Competition for milk in the domestic rabbit: survivors benefit from littermate deaths. Ethology 106 (2000) 511-526
17. Engqvist L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70 (2005) 967-971
18. Faraway J. Extending the linear model with R (2006), Chapman & Hall/CRC, New York
19. Faraway J. Changes to the mixed effects models. Chapter in ELM (2007). http://www.maths.bath.ac.uk/~jjf23/ELM/
20. Festa-Bianchet M., Jorgenson J.T., and Réale D. Early development, adult body mass, and reproductive success in bighorn sheep. Behav Ecol 11 (2000) 633-639
21. Fey K., and Trillmich F. Sibling competition in guinea pigs (Cavia aperea f. porcellus): scrambling for mother's teats is stressful. Behav Ecol Sociobiol 62 (2008) 321-329
22. Foxcroft G.R., Dixon W.T., Nowak S., Putman C.T., Town S.C., and Vinsky M.D.A. The biological basis for prenatal programming of postnatal performance in pigs. J Anim Sci 84 (2006) E105-E112
23. Fraser D., and Thompson B.K. Armed sibling rivalry among piglets. Behav Ecol Sociobiol 29 (1990) 9-15
24. Gilbert C., Blanc S., Giroud S., Trabalon M., Le Maho Y., Perret M., et al. Role of huddling on the energetics of growth in a newborn altricial mammal. Am J Physiol Regul Integr Comp Physiol 293 (2007) R867-R876
25. Hackländer K., Arnold W., and Ruf T. Postnatal development and thermoregulation in the precocial European hare (Lepus europaeus). J Comp Physiol B 172 (2002) 183-190
26. Haywood S., and Perrins C.M. Is clutch size affected by environmental conditions during growth?. Proc R Soc Lond B 249 (1992) 195-197
27. Hofer H., and East M.L. Siblicide in Serengeti spotted hyenas: a long-term study of maternal input and cub survival. Behav Ecol Sociobiol 62 (2008) 341-351
28. Hudson R., and Distel H. The pattern of behaviour of rabbit pups in the nest. Behaviour 79 (1982) 255-272
29. Hudson R., and Distel H. Nipple location by newborn rabbits: behavioural evidence for pheromonal guidance. Behaviour 85 (1983) 260-275
30. Hudson R., and Distel H. Sensitivity of female rabbits to changes in photoperiod as measured by pheromone emission. J Comp Physiol 167 (1990) 225-230
31. Hudson R., Bilkó Á., and Altbäcker V. Nursing, weaning and the development of independent feeding in the rabbit. Z Säugetierk (now Mamm Biol) 61 (1996) 39-48
32. Hudson R., Cruz Y., Lucio R.A., Ninomiya J., and Martínez-Goméz M. Temporal and behavioral patterning of parturition in rabbits and rats. Physiol Behav 66 (1999) 599-604
33. Hudson R., and Trillmich F. Sibling competition and cooperation in mammals: challenges, developments and prospects. Behav Ecol Sociobiol 62 (2008) 299-307
34. Hull D. Oxygen consumption and body temperature of newborn rabbits and kittens exposed to cold. J Physiol 177 (1965) 192-202
35. Jilge B., and Hudson R. Diversity and development of circadian rhythms in the European rabbit. Chronobiol Int 18 (2001) 1-26
36. Kraft R. Vergleichende Verhaltensstudien an Wild- und Hauskaninchen. I. Das Verhaltensinventar von Wild- und Hauskaninchen. Z Tierzücht Züchtungsbiol 95 (1979) 140-162
37. Kraus C., Trillmich F., and Künkele J. Reproduction and growth in a precocial small mammal, Cavia magna. J Mamm 86 (2005) 763-772
38. Laurien-Kehnen C., and Trillmich F. Maternal food restriction delays weaning in the guinea pig, Cavia porcellus. Anim Behav 27 (2003) 1202-1209
39. Lenihan C., and Van Vuren D. Growth and survival of juvenile yellow-bellied marmots (Marmota flaviventris). Can J Zool 74 (1996) 297-302
40. Marboutin E., and Hansen K. Survival rates in a non-harvested brown hare population. J Wildl Manage 62 (1998) 772-779
41. Martínez-Gómez M., Juárez M., Distel H., and Hudson R. Overlapping litters and reproductive performance in the domestic rabbit. Physiol Behav 82 (2004) 629-636
42. Mendl M. The effect of litter size variation on mother-offspring relationships and behavioural and physical development in several mammalian species (principally rodents). Anim Behav 215 (1998) 15-34
43. Mock D.W., and Parker G.A. The evolution of sibling rivalry (1997), Oxford University Press, Oxford
44. Murie J.O., and Boag D.A. The relationship of body weight to overwinter survival in Colombian ground squirrels. J Mammal 65 (1984) 688-690
45. Mykytowycz R., and Dudzinszki M.L. Aggressive and protective behaviour of adult rabbits, Oryctolagus cuniculus, towards juveniles. Behaviour 43 (1972) 97-120
46. Nagelkerke N.J.D. A note on a general definition of the coefficient of determination. Biometrika 78 (1991) 691-692
47. Pacheco-Cobos L., Rosetti M., Distel H., and Hudson R. To stay or not to stay: the contribution of tactile and thermal cues to coming to rest in newborn rabbits. J Comp Physiol A 189 (2003) 383-389
48. Patton N.M. Colony husbandry. In: Manning P.J., Ringler D.H., and Newcomer C.E. (Eds). The biology of the laboratory rabbit (1994), Academic Press, New York 27-45
49. Development Core Team R. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing (2007). 3-900051-07-0. http://wwwR-projectorg http://wwwR-projectorg
50. Rödel H.G., Bora A., Kaetzke P., Khaschei M., Hutzelmeyer H., and von Holst D. Over-winter survival in subadult European rabbits: weather effects, density-dependence, and the impact of individual characteristics. Oecologia 140 (2004) 566-576
51. Rödel H.G., Wibbelt G., Starkloff A., and von Holst D. Post-natal remains of the foetal membranes affect growth and survival of wild European rabbit pups. Mamm Biol 72 (2007) 313-319
52. Rödel H.G., Hudson R., and von Holst D. Optimal litter size for individual growth of European rabbit pups depends on their thermal environment. Oecologia 155 (2008) 677-689
53. Rödel H.G., Prager G., Stefanski V., von Holst D., and Hudson R. Separating maternal and litter size effects on early postnatal growth in two species of altricial mammals. Physiol Behav 93 (2008) 826-834
54. Rödel H.G., Starkloff A., Prager G., Seltmann M.W., and von Holst D. Causes and predictors of nest mortality in a European rabbit population. Mamm Biol (2008) 10.1016/j.mambio.2008.04.003
55. Roshan P.D., and Greene H.S.N. The influence of intrauterine factors on the fetal weight of rabbits. J Exp Med 63 (1936) 901-921
56. Russelt A.F., Clutton-Brock T.H., Brotherton P.N.M., Sharpe L.L., McIlrath G.M., Dalerum F.D., et al. Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta. J Anim Ecol 71 (2002) 700-709
57. Sandell M., and Smith H.G. Dominance, prior occupancy, and winter residence in the great tit (Parus major). Behav Ecol Sociobiol 29 (1991) 147-152
58. Scantlebury M., Bennett N.C., Speakman J.R., Pillay N., and Schradin C. Huddling in groups leads to daily energy savings in free-living African four-striped grass mice, Rhabdomys pumilio. Funct Ecol 20 (2006) 166-173
59. Schradin C., and Pillay N. The influence of the father on offspring development in the striped mouse. Behav Ecol 16 (2005) 450-455
60. Sokal M., and Sinclair J. Effects of temperature on growth of newborn rabbits. Biol Neonate 28 (1976) 1-11
61. Stearns S.C. The evolution of life histories (1992), Oxford University Press, Oxford
62. von Holst D., Hutzelmeyer H., Kaetzke P., Khaschei M., Rödel H.G., and Schrutka H. Social rank, fecundity and lifetime reproductive success in wild European rabbits Oryctolagus cuniculus. Behav Ecol Sociobiol 51 (2002) 245-254
63. Wauters L., Bijnens L., and Dhondt A.A. Body mass at weaning and juvenile recruitment in the red squirrel. J Anim Ecol 62 (1993) 280-286
64. White P.A. Maternal response to neonatal sibling conflict in the spotted hyena, Crocuta crocuta. Behav Ecol Sociobiol 62 (2008) 353-361
65. Zarrow M.X., Denenberg V.H., and Anderson C.O. Rabbit: frequency of suckling in the pup. Science 150 (1965) 1835-1836