Ecological conditions experienced by offspring during pregnancy and early post-natal life determine mandible size in roe deer

English version

Autoři: Anna Maria De Marinis ^aff001; Roberta Chirichella ^aff002; Elisa Bottero ^aff002; Marco Apollonio ^aff002
Působiště autorů: Italian Institute for Environmental Protection and Research (ISPRA), Ozzano dell'Emilia (BO), Italy ^aff001; Department of Veterinary Medicine, University of Sassari, Sassari, Italy ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222150

Souhrn

Population dynamics studies and harvesting strategies often take advantage of body size measurements. Selected elements of the skeletal system such as mandibles, are often used as retrospective indices to describe body size. The variation in mandibular measurements reflects the variation in the ecological context and hence the variation in animal performance. We investigated the length of the anterior and posterior sections of the mandible in relation to the conditions experienced by juveniles of 8–10 months of age during prenatal and early postnatal life and we evaluated these parameters as ecological indicators of juvenile condition as well as female reproductive condition in a roe deer population living in the southern part of the species range. We analyzed a sample of over 24,000 mandibles of roe deer shot in 22 hunting districts in the Arezzo province (Tuscany, Central Italy) from 2005 to 2015 per age class. Mandible total length in juveniles is equal to 90% of total length in adults. In this stage of life the growing of the mandible’s anterior section is already completed while that of the posterior section is still ongoing. Environmental conditions conveyed by forest productivity, agricultural land use, local population density and climate strongly affected the growth of the anterior and posterior sections of the mandibles. Conditions experienced both by pregnant females and offspring played an important role in shaping the length of the anterior section, while the size of the posterior section was found to be related to the conditions experienced by offspring. Temporal changes of the length of the anterior section are a particularly suitable index of growth constraints. Anterior section length in fact differs according to more or less advantageous conditions recorded not only in the year of birth, but also in the previous year. Similarly, the sexual size dimorphism of the anterior section of the roe deer mandible can be used to describe the quality of females above two years of age, as well as habitat value. Hence the anterior section length of the mandible and its sexual size dimorphism are indexes that can provide cues of population performance, because they capture the system’s complexities, while remain simple enough to be easily and routinely used in the majority of European countries where roe deer hunting period extends from early autumn to late spring.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Population biology – Anatomy – Medicine and health sciences – Digestive system – Physiology – Vertebrates – Amniotes – Mammals – Physiological parameters – Population metrics – Body weight – Earth sciences – Seasons – Ruminants – Spring – Mouth – Mandible – Deer – Population density – Autumn – Winter – Summer

Zdroje

1. Toïgo C, Gaillard JM. Causes of sex-biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? Oikos. 2003;101:376–384.

2. Clutton-Brock TH, Price OF, Albon SD, Jewell PA. Early development and population fluctuations in Soay sheep. J Anim Ecol. 1992;61: 381–396.

3. Gaillard JM, Delorme D, Boutin JM, van Laere G, Boisaubert B, Pradel R. Roe deer survival patterns: a comparative analysis of contrasting populations. J Anim Ecol. 1993;62:778–791.

4. Gaillard JM, Delorme D, Van Laere G, Duncan P, Lebreton JD. Early survival in roe deer: causes and consequences of cohort variation in two contrasted populations. Oecologia. 1997;112:502–513. doi: 10.1007/s004420050338 28307627

5. Loison A, Langvatn R, Solberg EJ. Body mass and winter mortality in red deer calves: Disentangling sex and climate effects. Ecography. 1999;22 (1):20–30.

6. Côté SD, Festa-Bianchet M. Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia. 2001;127(2):230–8. doi: 10.1007/s004420000584 24577654

7. Festa-Bianchet M, Jorgenson JT, Bérubé CH, Portier C, Wishart WD. Body mass and survival of bighorn sheep. Can J Zool. 1997;75(9):1372–1379.

8. McElligott AG, Gammell MP, Harty HC, Paini DR, Murphy DT, Walsh JT, Hayden TJ. Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success?. Behavioral Ecology and Sociobiology. 2001;49(4):266–72.

9. Douhard M, Gaillard JM, Delorme D, Capron G, Duncan P, Klein F, Bonenfant C. Variation in adult body mass of roe deer: early environmental conditions influence early and late body growth of females. Ecology. 2013;94(8):1805–1814. doi: 10.1890/13-0034.1 24015524

10. Flajšman K, Klemen J, Pokorny B. Age-related effects of body mass on fertility and litter size in roe deer. PLoS ONE. 2017;12(4):e0175579. doi: 10.1371/journal.pone.0175579 28403161

11. Albon SD, Mitchell B, Huby BJ, Brown D. Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. J Zool. 1986;209:447–460.

12. Bertouille S, De Crombrugghe SA. Fertility of red deer in relation to area, age, body mass, and mandible length. Z Jagdwiss. 2002;48:87–98.

13. Albon SD, Clutton-Brock TH, Langvatn R. Cohort variation in reproduction and survival: implications for population demography. In: Brown RD, editor. The biology of deer. Springer; 1992. pp. 15–21.

14. Sauer J, Slade R. Size-based demography of vertebrates. Annu Rev Ecol Evol Syst. 1987;18:71–90.

15. Gamelon M, Gaillard JM, Servanty S, Gimenez O, Toïgo C, Baubet E, Klein F, Lebreton JD. Making use of harvest information to examine alternative management scenarios: A body weight-structured model for wild boar. J Appl Ecol. 2012;9:833–841.

16. Forchhammer MC, Clutton-Brock TH, Lindström J, Albon S. Climate and population density induce long-term cohort variation in a northern ungulate. J. Anim. Ecol. 2001;70:721–729.

17. Weladji RB, Holand O. Global climate change and reindeer: effects of winter wheather on the autumn weight and growth of calves. Oecologia. 2003;136:317–323. doi: 10.1007/s00442-003-1257-9 12707839

18. Clutton-Brock TH. The evolution of parental care. Princeton University Press, Princeton, NJ; 1991.

19. Jönsson KI. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos. 1997;78:57–66.

20. Stephens PA, Boyd IL, McNamara JM, Houston AI. Capital breeding and income breeding: their meaning, measurement, and worth. Ecology. 2009;90:2057–2067. doi: 10.1890/08-1369.1 19739368

21. Andersen R, Gaillard JM, Linnell JDC, Duncan P. Factors affecting maternal care in an income breeder, the European roe deer. J Anim Ecol. 2000;69 (4):672–682.

22. Apollonio M, Andersen R, Putman RJ. European ungulates and their management in the 21st century. Cambridge: Cambridge University Press; 2010.

23. Chirichella R, Pokorny B, Bottero E, Flajšman K, Mattioli L, Apollonio M. Factors affecting implantation failure in roe deer. J Wildl Manage. 2018; Forthcoming.

24. Benton TG, Stewart J, Plaistow J, Coulson TN. Complex population dynamics and complex causation: devils, details and demography. Proc Biol Sci. 2006;273(1591):1173–1181. doi: 10.1098/rspb.2006.3495 16720388

25. Charmantier A, Garant D. Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B Biol Sci. 2005;272:1415–25.

26. Zanneśe A, Morellet N, Targhetta C, Coulon A, Fuser S, Hewison AJM, Ramanzin M. Spatial structure of roe deer populations: towards defining management units at a landscape scale. J Appl Ecol 2006;43:1087–1097.

27. Hewison AJ, Vincent JP, Bideau E, Angibault JM, Putman RJ. Variation in cohort mandible size as an index of roe deer (Capreolus capreolus) densities and population trends. J. Zool. 1996;239(3):573–81.

28. Høye TT, Forchhammer MC. Early developed section of the jaw as an index of prenatal growth conditions in adult roe deer Capreolus capreolus. Wildl Biol. 2006;12(1):71–76.

29. Dvořák J, Kamler J, Šarman J. Vyhodnocení vybraných parametrů spodních čelistí srnce obecného (Capreolus capreolus L.) z oblasti Hodonínska. Folia Venatoria 2002;32: 35–40. [in Slovak]

30. Wustinger J, Galli J, Rozpędek W. An osteometric study on recent roe deer (Capreolus capreolus L., 1758). Folia Morphol. 2005; 64 (2):97–100.

31. Labus ND, Babovic-Jaksic T, Vasic PS. Sexual and age differences in craniometrics characteristics of roe deer (Capreolus capreolus L.) from area of Mountain Prokletije. Natura Montenegrina. 2010;9(3):583–592.

32. Avdić R, Hadžiomerović N, Tandir F, Bejdić P, Ćutahija V. Analysis of morphometric parameters of the Roe deer mandible (Capreolus capreolus) and mandible of the sheep (Ovis aries). Veterinaria. 2013;62(1–2):1–9.

33. Hanzal V, Janiszewski P, Tajchman K, Košinová K. The correlation between mandibular length versus body mass and age in the European roe deer (Capreolus capreolus L.). Appl Ecol Env Res. 2017;15(4):1623–1632.

34. Stubbe C, Passarge H. Rehwild. VEB Deutscher Landwirtschafts-verlag. Berlin, Germany; 1979.

35. Zedja J, Koubek P. On the geographical variability of roe bucks (Capreolus capreolus). Folia Zool. 1988;37:219–229.

36. Fandos P, Reig S. Craniometric variability in two populations of roe deer (Capreolus capreolus) from Spain. J Zool. 1993;231:39–49.

37. Aragon S, Braza F, San Jose C, Fandos P. Variation in skull morphology of roe deer (Capreolus capreolus) in western and central Europe. J Mamm. 1998;79(1):131–140.

38. Sheremetyeva IN, Sheremetyev IS. Skull variation in the Siberian roe deer Capreolus pygargus from the Far East: a revision of the distribution of the subspecies. Eur J Wildl Res. 2008;54:557–569.

39. Hanzal V, Ježek M, Janiszewski P, Kusta T. Development of craniometric traits of wild boar (Sus scrofa). Sylwan. 2012;156 (11):855–862.

40. Mendoza M, Janis CM, Palmqvist P. Characterizing complex craniodental patterns related to feeding behaviour in ungulates: a multivariate approach. J Zool. 2002;258: 223–246.

41. De Marinis AM, Chirichella R, Bottero E, Apollonio M. Ecological factors affecting eruption timing of mandibular teeth in roe deer. Eur J Wildl Res. 2018;64:50.

42. Milošević-Zlatanović S, Tomašević Kolarov N, Vukov T, tamenković S. Correlation patterns in roe deer cranium: sexual dimorphism across different habitats. J. Zool. 2016;300:291–304.

43. Hewison AJM, Gaillard JM, Delorme D, Van Laere HG, Amblard T, Klein F. Reproductive constraints, not environmental conditions, shape the ontogeny of sex‐specific mass–size allometry in roe deer. Oikos. 2011;120 (8):1217–1226.

44. Post E, Stenseth NC, Langvatn R, Fromentin JM. Global climate change and phenotypic variation among red deer cohorts. Proc R Soc Lond B Biol Sci. 1997;264:1317–1324.

45. Andersen J. Analysis of a danish roe-deer population (Capreolus capreolus L.), based upon the extermination of the total stock. Dan Rev Game Biol. 1953;2:127–155.

46. Klein DR, Strandgaard H. Factors affecting growth and body size of roe deer. J Wildl Manag. 1972;36:64–79.

47. Garel M, Gaillard JM, Delorme D, Van Laere G. Eruption patterns of permanent front teeth as an indicator of performance in roe deer. Ecol. Indic. 2014;45:300–307.

48. Apollonio M, Mattioli L. Il lupo in provincia di Arezzo. Montepulciano, Italy. Editrice Le Balze. 2006. [in Italian]

49. Bassi E, Willis SG, Passilongo D, Mattioli L, Apollonio M. Predicting the spatial distribution of wolf (Canis lupus) breeding areas in a mountainous region of Central Italy. PLoS ONE. 2015;10(6):e0124698. doi: 10.1371/journal.pone.0124698 26035174

50. Ratcliffe PR, Mayle B. Roe deer biology and management. Forestry Commission Bulletin 105, London, United Kingdom; 1992.

51. Desiato F, Fioravanti G, Fraschetti P, Perconti W, Piervitali E, Pavan V. Gli indicatori del clima in Italia nel 2015. Sistema Nazionale per la Protezione dell’Ambiente. Stato dell’Ambiente. 2016; 65. [in Italian]

52. Melis C, Jedrzejewska B, Apollonio M, Barton KA, Jedrzejewski W, Linell JDC, Kojola I, Kusak J, Adamic M, Ciuti S, Delehan I, Dykyy I, Krapinec K, Mattioli L, Sagaydak A, Samchuk N, Schmidt K, Shkvyrya M, Sidorovich VE, Zawadzka B, Zhyla S. Predation has a greater impact in less productive environments: variation in roe deer, Capreolus capreolus, population density across Europe. Glob. Ecol. Biogeogr. 2009;18:724–734.

53. Linnell JDC, Andersen R. Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. J Zool. 1998;244:497–504.

54. Mattioli L, Capitani C, Avanzinelli E, Bertelli I, Gazzola A, Apollonio M. Predation by wolves (Canis lupus) on roe deer (Capreolus capreolus) in north-eastern Apennine, Italy. J Zool. 2004;264:249–258.

55. Davis ML, Stephens PA, Willis SG, Bassi E, Marcon A, Donaggio E, Capitani C, Apollonio M. Prey selection by an apex predator: the importance of sampling uncertainty. PLoS ONE. 2012;7(10):e47894. doi: 10.1371/journal.pone.0047894 23110122

56. Cutini A, Chianucci F, Chirichella R, Donaggio E, Mattioli L, Apollonio M. Mast seeding in deciduous forests of the northern Apennines (Italy) and its influence on wild boar population dynamics. Ann Forest Sci. 2013;70: 493–502.

57. Chianucci F, Mattioli L, Amorini E, Giannini T, Marcon A, Chirichella R, Apollonio M, Cutini A. Early and long-term impacts of browsing by roe deer in oak coppiced woods along a gradient of population density. Annals of Silvicultural Research. 2014;38(2): 10–14.

58. Borkowski J, Palmer SCF, Borowski Z. Drive counts as a method of estimating ungulate density in forests: mission impossible? Acta Theriol. 2011;56:239–253. doi: 10.1007/s13364-010-0023-8 21765532

59. Li J, Heap AD. A review of spatial interpolation methods for environmental scientists. Geoscience Australia, Canberra, Australia; 2008.

60. Suttie JM, Mitchell B. Jaw length and hind foot length as measures of skeletal development of red deer (Cervus elaphus). Journal of Zoology 1983;200:431–434).

61. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2018. Available from: https://www.R-project.org/

62. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 2013;36:27–46.

63. Burnham KP, Anderson DR. Model selection and multimodal inference: a practical information-theoretic approach. Springer-Verlag, New York; 2002.

64. Symonds MRE, Mousalli A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol. 2011;65:13–21.

65. Hofmann RR. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia. 1989;78:443–457. doi: 10.1007/BF00378733 28312172

66. Duncan P, Tixier H, Hofmann RR, Lechner-Doll M. Feeding strategies and the physiology of digestion in roe deer. In: Andersen R, Duncan P, Linnell JDC, editors. The European roe deer: The biology of success. Oslo: Scandinavian University Press; 1998. pp. 91–116.

67. Freschi P, Fascetti S, Riga F, Cosentino C, Rizzardini G, Musto M. Diet composition of the Italian roe deer (Capreolus capreolus italicus) (Mammalia:Cervidae) from two protected areas. Eur. Zool. J. 2007;84(1):34–42.

68. Mauget C, Mauget R, Sempéré A. Energy expenditure in European roe deer fawns during the suckling period and its relationship with maternal reproductive cost. Can J Zool. 1999;77(3):389–396.

69. McLoughlin PD, Gaillard JM, Boyce MS, Bonenfant C, Messier F, Duncan P, et al. Lifetime reproductive success and composition of the home range in a large herbivore. Ecology. 2007;88(12):3192–3201. doi: 10.1890/06-1974.1 18229853

70. Pettorelli N, Gaillard JM, Van Laere G, Duncan P, Kjellander P, Liberg O, et al. Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality. Proc R Soc Lond B Biol Sci. 2002;269:747–53.

71. Bisi F, Chirichella R, Chianucci F, von Hardenberg J, Cutini A, Martinoli A, Apollonio M. Climate, tree masting and spatial behaviour in wild boar (Sus scrofa L.): insight from a long-term study. Ann Forest Sci. 2018;75:46.

72. Hewison AJM, Vincent JP, Joachim J, Angibault JM, Cargnelutti B, Cibien C. The effects of woodland fragmentation and human activity on roe deer distribution in agricultural landscapes. Can. J. Zool. 2001;79:679–689.

73. Azorit C, Analla M, Muñoz-Cobo J. Variation of mandible size in red deer Cervus elaphus hispanicus from southern Spain. Acta Theriol. 2003;48(2):221–228.

74. Couturier S, Otto RD, Côté SD, Luther G, Mahoney SP. Body size variations in caribou ecotypes and relationships with demography. J Wildl Manage. 2010;74(3):395–404.

75. Plard F, Gaillard JM, Coulson T, Hewison AJM, Delorme D, Warnant C, et al. Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biol. 2014;12(4):e1001828. doi: 10.1371/journal.pbio.1001828 24690936

76. Gaillard JM, Festa-Bianchet M, Yoccoz NG. Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol. 1998;13:58–63. 21238201

77. Wauters LA, de Crombrugghe SA, Nour N, Matthysen E. Do female roe deer in good condition produce more sons than daughter. Behav Ecol Sociobiol. 1995;37(3):189–193.

78. Morellet N, Gaillard JM, Hewison AJM, Ballon P, Boscardin Y, Duncan P, et al. Indicators of ecological change: new tools for managing populations of large herbivores. J. Appl. Ecol. 2007;44:634–643.

79. Post E, Stenseth NC, Langvatn R, Fromentin JM. Global climate change and phenotypic variation among red deer cohorts. Proc R Soc Lond B Biol Sci. 1997;264:1317–1324

80. LeBlanc M, Festa-Bianchet M, Jorgenson JT. Sexual size dimorphism in bighorn sheep (Ovis canadensis): effect of population density. Can J Zool. 2001;79:1661–1670.

Ecological conditions experienced by offspring during pregnancy and early post-natal life determine mandible size in roe deer

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