Early end of embryonic diapause and overall reproductive activity in roe deer populations from Bavaria

C. Ehrmantraut; T. Wild; S.-A. Dahl; N. Wagner; A. König

doi:10.1071/AN23040

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 63(16)

Early end of embryonic diapause and overall reproductive activity in roe deer populations from Bavaria

C. Ehrmantraut

^A ^* , T. Wild

^A , S.-A. Dahl

^A , N. Wagner

^B and A. König

^A

+ Author Affiliations

- Author Affiliations

^A Technical University of Munich, Wildlife Biology and Management Unit, Hans-Carl-von-Carlowitz-Platz 2, Freising D-85354, Germany.

^B Zweckverband Natura Ill-Theel, In der Meulwies 1, Marpingen-Berschweiler D-66646, Germany.

^* Correspondence to: christian.ehrmantraut@tum.de

Handling Editor: Gordon Dryden

Animal Production Science 63(16) 1623-1632 https://doi.org/10.1071/AN23040
Submitted: 25 January 2023 Accepted: 4 September 2023 Published: 2 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

According to the established, older literature, the embryonic diapause (ED) in roe deer ends in late December. In many other species groups, phenological phases are shifting as a result of climatic changes. Whether this is the case in roe deer for the period of ED has not yet been explicitly investigated.

Aim

The aim of this study was to obtain an up-to-date overview of the reproduction of roe deer in Bavaria, particularly with regard to climate change.

Methods

For this purpose, uterus samples were taken from roe deer aged at least 1 year between September and January and examined macroscopically. The samples were collected during regular hunting activities in Bavaria in the years 2017–2020.

Key results

A large proportion of the female roe deer examined was found to have been already engaged in reproduction. In 98% of the animals, Corpora lutea (CL) were present in the ovaries. Adult does had significantly more CL than did subadult does just reaching sexual maturity. In 75 roe deer does, 128 embryos, in total, were detected. On average, 1.67 embryos were found per doe with visible embryos. Of these does, 30% carried a single embryo, 67% were bearing twins and 3% were bearing triplets. The animals with visible embryos ranged in age from 1 to 12 years. In a few cases, ED was already completed in November or early December. By the end of the hunting season, a correspondingly wide variety of developmental stages of embryos was visible. Our study suggests potential indications that older animals or those with a higher body mass end ED earlier.

Conclusions

Overall, the results indicated vigorous reproductive activity in the study area. The results showed that some individuals already end the ED in November or early December, so they may adapt to an earlier onset of the vegetation period. In contrast, we found a few individuals that ended the ED during January, which illustrates the temporal range of the ED.

Implications

Whether the early end of diapause in these roe deer is a reaction to climatic changes or whether there are other underlying causes is something that requires further investigation.

Keywords: Bavaria, Capreolus capreolus, Corpora lutea, embryo, embryonic diapause, Germany, reproduction, roe deer, uterus.

References

Acevedo P, Delibes-Mateos M, Escudero MA, Vicente J, Marco J, Gortazar C (2005) Environmental constraints in the colonization sequence of roe deer (Capreolus capreolus Linnaeus, 1758) across the Iberian Mountains, Spain. Journal of Biogeography 32, 1671-1680.
| Crossref | Google Scholar |

Aitken RJ (1974) Delayed implantation in roe deer (Capreolus capreolus). Journal of Reproduction and Fertility 39, 225-233.
| Crossref | Google Scholar | PubMed |

Aitken RJ (1977) Embryonic diapause. In ‘Development in mammals, Vol. 1’. (Ed. MH Johnson) pp. 307–359. (Elsevier: Amsterdam, Netherlands)

Aitken RJ (1981) Aspects of delayed implantation in the roe deer (Capreolus capreolus). Journal of Reproduction and Fertility 29, 83-95.
| Google Scholar | PubMed |

Andersen J (1953) Analysis of a Danish roe-deer population. Danish Review of Game Biology 2, 131-155.
| Google Scholar |

Andersen R, Duncan P, Linnell JDC (Eds) (1998) ‘The European roe deer: the biology of success.’ (Scandinavian University Press: Oslo, Norway)

Andersen R, Gaillard J-M, Linnell JDC, Duncan P (2000) Factors affecting maternal care in an income breeder, the European roe deer. Journal of Animal Ecology 69, 672-682.
| Crossref | Google Scholar |

Arlt D, Pärt T (2017) Marked reduction in demographic rates and reduced fitness advantage for early breeding is not linked to reduced thermal matching of breeding time. Ecology and Evolution 7, 10782-10796.
| Crossref | Google Scholar | PubMed |

Bayerisches Landesamt für Umwelt (2022) Klima in Bayern. Available at https://www.lfu.bayern.de/klima/klimawandel/klimafaktenblaetter/index.html. [Verified 9 January 2023]

Bayerische Staatsforsten AöR (2019) Standorte. Available at https://www.baysf.de/de/ueber-uns/standorte.html [Verified 9 January 2023]

Bischoff TLW (1854) ‘Entwicklungsgeschichte des Rehes.’ (J. Ricker’sche Buchhandlung: Giessen, Germany)

Bonnet T, Morrissey MB, Morris A, Morris S, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2019) The role of selection and evolution in changing parturition date in a red deer population. PLoS Biology 17, e3000493.
| Crossref | Google Scholar | PubMed |

Borg K (1971) On mortality and reproduction of roe deer in Sweden during the period 1948-1969. Viltrevy 7, 121-149.
| Google Scholar |

Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3331-3340.
| Crossref | Google Scholar |

Bubenik AB (1984) ‘Ernährung, Verhalten und Umwelt des Schalenwildes.’ (BLV Verlagsgesellschaft: München, Wien, Zürich)

Chirichella R, Pokorny B, Bottero E, Flajšman K, Mattioli L, Apollonio M (2019) Factors affecting implantation failure in roe deer. The Journal of Wildlife Management 83, 599-609.
| Crossref | Google Scholar |

Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends in Ecology & Evolution 22, 357-365.
| Crossref | Google Scholar | PubMed |

Clements MN, Clutton-Brock TH, Albon SD, Pemberton JM, Kruuk LEB (2011) Gestation length variation in a wild ungulate. Functional Ecology 25, 691-703.
| Crossref | Google Scholar |

Danilkin AA (1996) ‘Behavioural ecology of Siberian and European roe deer.’ (Chapman & Hall: London, UK)

Ellenberg H (1978) Zur Populationsökologie des Rehes (Capreolus capreolus L., Cervidae) in Mitteleuropa. Spixiana, Zeitschrift für Zoologie Supplement 2, 1-211.
| Google Scholar |

Enders RK (1952) Reproduction in the mink (Mustela visori). Proceedings of the American Philosophical Society 96, 691-755.
| Google Scholar |

Flajšman K, Jerina K, Pokorny B (2017) Age-related effects of body mass on fertility and litter size in roe deer. PLoS ONE 12(4), e0175579.
| Crossref | Google Scholar | PubMed |

Gaillard J-M, Mark Hewison AJ, Klein F, Plard F, Douhard M, Davison R, Bonenfant C (2013) How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer. Ecology Letters 16, 48-57.
| Crossref | Google Scholar | PubMed |

Garel M, Gaillard J-M, Jullien J-M, Dubray D, Maillard D, Loison A (2011) Population abundance and early spring conditions determine variation in body mass of juvenile chamois. Journal of Mammalogy 92, 1112-1117.
| Crossref | Google Scholar |

Grøtan V, Sæther B-E, Lillegård M, Solberg EJ, Engen S (2009) Geographical variation in the influence of density dependence and climate on the recruitment of Norwegian moose. Oecologia 161, 685-695.
| Crossref | Google Scholar | PubMed |

Hagen R, Ortmann S, Elliger A, Arnold J (2021) Advanced roe deer (Capreolus capreolus) parturition date in response to climate change. Ecosphere 12, e03819.
| Crossref | Google Scholar |

Helle T, Kojola I (2008) Demographics in an alpine reindeer herd: effects of density and winter weather. Ecography 31, 221-230.
| Crossref | Google Scholar |

Hewison AJM, Gaillard JM (2001) Phenotypic quality and senescence affect different components of reproductive output in roe deer. Journal of Animal Ecology 70(4), 600-608.
| Crossref | Google Scholar |

Hoffmann B, Barth D, Karg H (1978) Progesterone and estrogen levels in peripheral plasma of the pregnant and nonpregnant roe deer (Capreolus capreolus). Biology of Reproduction 19, 931-935.
| Crossref | Google Scholar | PubMed |

Horak A (1989) Histologische und histomorphometrische Untersuchungen am Ovarium des Rehes (Capreolus capreolus, L.) und er zyklischen Veränderungen seiner Funktionsstrukturen. PhD thesis, Justus-Liebig-University, Gießen, Germany.

Kałuziński J (1982) Dynamics and structure of a field roe deer population. Acta Theriologica 27, 385-408.
| Crossref | Google Scholar |

Keibel F (1899) Zur Entwicklungsgeschichte des Rehes. Anatomischer Anzeiger 16, 64-65.
| Google Scholar |

Kerby J, Post E (2013) Capital and income breeding traits differentiate trophic match–mismatch dynamics in large herbivores. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 20120484.
| Crossref | Google Scholar |

König A, Hudler M, Dahl S-A, Bolduan C, Brugger D, Windisch W (2020) Response of roe deer (Capreolus capreolus) to seasonal and local changes in dietary energy content and quality. Animal Production Science 60(10), 1315-1325.
| Crossref | Google Scholar |

Kourkgy C, Garel M, Appolinaire J, Loison A, Toïgo C (2016) Onset of autumn shapes the timing of birth in Pyrenean chamois more than onset of spring. Journal of Animal Ecology 85(2), 581-590.
| Crossref | Google Scholar | PubMed |

Kurt F (2002) ‘Das Reh in der Kulturlandschaft: Ökologie, Sozialverhalten, Jagd und Hege.’ (Franckh-Kosmos)

Lambert RT, Ashworth CJ, Beattie L, Gebbie FE, Hutchinson JS, Kyle DJ, Racey PA (2001) Temporal changes in reproductive hormones and conceptus–endometrial interactions during embryonic diapause and reactivation of the blastocyst in European roe deer (Capreolus capreolus). Reproduction 121(6), 863-871.
| Crossref | Google Scholar |

Lengwinat T, Meyer HHD (1996) Investigations of BrdU incorporation in roe deer blastocysts in vitro. Animal Reproduction Science 45, 103-107.
| Crossref | Google Scholar |

Lindenmayer DB, Lavery T, Scheele BC (2022) Why we need to invest in large-scale, long-term monitoring programs in landscape ecology and conservation biology. Current Landscape Ecology Reports 7, 137-146.
| Crossref | Google Scholar |

Linnell JDC, Wahlström K, Gaillard JM (1998) From birth to independence: birth, growth, neonatal mortality, hiding behaviour and dispersal. In ‘The European roe deer: the biology of success’. (Eds R Andersen, P Duncan, JDC Linnell) pp. 257–285. (Scandinavian University Press: Oslo, Norway)

Lopes FL, Desmarais JA, Murphy BD (2004) Embryonic diapause and its regulation. Reproduction 128, 669-678.
| Crossref | Google Scholar | PubMed |

Mall FP (1907) On measuring human embryos. The Anatomical Record 1, 129-140.
| Crossref | Google Scholar |

Marrot P, Charmantier A, Blondel J, Garant D (2018) Current spring warming as a driver of selection on reproductive timing in a wild passerine. Journal of Animal Ecology 87, 754-764.
| Crossref | Google Scholar | PubMed |

Mauget C, Mauget R, Sempéré A (1997) Metabolic rate in female European roe deer (Capreolus capreolus): incidence of reproduction. Canadian Journal of Zoology 75, 731-739.
| Crossref | Google Scholar |

Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397, 659.
| Crossref | Google Scholar |

Merkle JA, Monteith KL, Aikens EO, Hayes MM, Hersey KR, Middleton AD, Oates BA, Sawyer H, Scurlock BM, Kauffman MJ (2016) Large herbivores surf waves of green-up during spring. Proceedings of the Royal Society B: Biological Sciences 283, 20160456.
| Crossref | Google Scholar |

Mitchell B (1967) Growth layers in dental cement for determining the age of red deer (Cervus elaphus L.). Journal of Animal Ecology 36(2), 279-293.
| Crossref | Google Scholar |

Moyes K, Nussey DH, Clements MN, Guiness FE, Morris A, Morris S, Pemberton JM, Kruuk LEB, Clutton-Brock TH (2011) Advancing breeding phenology in response to environmental change in a wild red deer population. Global Change Biology 17, 2455-2469.
| Crossref | Google Scholar |

Murray DL, Hussey KF, Finnegan LA, et al. (2012) Assessment of the status and viability of a population of moose (Alces alces) at its southern range limit in Ontario. Canadian Journal of Zoology 90, 422-434.
| Crossref | Google Scholar |

Mysterud A, Røed KH, Holand Ø, Yoccoz NG, Nieminen M (2009) Age-related gestation length adjustment in a large iteroparous mammal at northern latitude. Journal of Animal Ecology 78, 1002-1006.
| Crossref | Google Scholar | PubMed |

Neumann W, Singh NJ, Stenbacka F, Malmsten J, Wallin K, Ball JP, Ericsson G (2020) Divergence in parturition timing and vegetation onset in a large herbivore-differences along a latitudinal gradient. Biology Letters 16, 20200044.
| Crossref | Google Scholar | PubMed |

Paoli A, Weladji RB, Holand Ø, Kumpula J (2018) Winter and spring climatic conditions influence timing and synchrony of calving in reindeer. PLoS ONE 13(4), e0195603.
| Crossref | Google Scholar |

Peláez M, San Miguel A, Rodríguez-Vigal C, Perea R (2017) Climate, female traits and population features as drivers of breeding timing in Mediterranean red deer populations. Integrative Zoology 12(5), 396-408.
| Crossref | Google Scholar | PubMed |

Pettorelli N, Mysterud A, Yoccoz NG, Langvatn R, Stenseth NC (2005) Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes. Proceedings of the Royal Society B: Biological Sciences 272, 2357-2364.
| Crossref | Google Scholar |

Pettorelli N, Pelletier F, Hardenberg Av, Festa-Bianchet M, Côté SD (2007) Early onset of vegetation growth vs. rapid green-up: impacts on juvenile mountain ungulates. Ecology 88, 381-390.
| Crossref | Google Scholar | PubMed |

Plard F, Gaillard J-M, Bonenfant C, Hewison AJM, Delorme D, Cargnelutti B, Kjellander P, Nilsen EB, Coulson T (2013) Parturition date for a given female is highly repeatable within five roe deer populations. Biology Letters 9, 20120841.
| Crossref | Google Scholar | PubMed |

Plard F, Gaillard J-M, Coulson T, Hewison AJM, Delorme D, Warnant C, Bonenfant C (2014a) Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biology 12, e1001828.
| Crossref | Google Scholar | PubMed |

Plard F, Gaillard J-M, Coulson T, Hewison AJM, Delorme D, Warnant C, Nilsen EB, Bonenfant C (2014b) Long-lived and heavier females give birth earlier in roe deer. Ecography 37, 241-249.
| Crossref | Google Scholar |

Pockels Dr (1836) Ueber die Brunftzeit der Rehe. In ‘Archiv fuer Anatomie, Physiologie und wissenschaftliche Medicin’. (Ed. J Müller) pp. 193–204. (G. Eichler: Berlin)

Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 2367-2373.
| Crossref | Google Scholar |

Prell H (1938) Die Tragzeit des Rehes. Züchtungskunde 13, 325-345.
| Google Scholar |

Ptak GE, Tacconi E, Czernik M, Toschi P, Modlinski JA, Loi P (2012) Embryonic diapause is conserved across mammals. PLoS ONE 7(3), e33027.
| Crossref | Google Scholar |

Raesfeld F (1956) ‘Das Rehwild.’ (Paul Parey: Hamburg & Berlin, Germany)

Rehnus M, Peláez M, Bollmann K (2020) Advancing plant phenology causes an increasing trophic mismatch in an income breeder across a wide elevational range. Ecosphere 11, e03144.
| Crossref | Google Scholar |

Rieck W (1955) Die Setzzeit bei Reh-, Rot-, und Damwild in Mitteleuropa. Zeitschrift für Jagdwissenschaft 1(2), 69-75.
| Crossref | Google Scholar |

Ross MV, Alisauskas RT, Douglas DC, Kellett DK (2017) Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology 98, 1869-1883.
| Crossref | Google Scholar | PubMed |

Sakurai T (1906) Normentafel zur Entwicklungsgeschichte des Rehes (Cervus capreolus). In ‘Normentafeln zur Entwicklungsgeschichte der Wirbelthiere’. (Ed. F Keibel) pp. 1–100. (Gustaf Fischer Verlag: Jena)

Sempéré A, Blanvillain C, Mauget R, Chemineau P (1993) The role of the photoperiod in the sexual cycle in female roe deer (Capreolus capreolus). In ‘Deer in China: biology and management’. (Eds N Ohtaishi, HI Sheng) pp. 364–371. (Elsevier: Amsterdam, Netherlands)

Short RV, Hay MF (1966) Delayed implantation in the roe deer (Capreolus capreolus). In ‘Comparative biology of reproduction in mammals’. (Ed. IW Rowlands) pp. 173–194. (Academic Press: New York, NY, USA)

Short RV, Mann T (1966) The sexual cycle of a seasonally breeding mammal, the roe buck (Capreolus capreolus). Journal of Reproduction and Fertility 12, 337-351.
| Crossref | Google Scholar |

Smith-Jones C (2022) ‘A guide to the deer of the world.’ (Stackpole Books)

Stieve H (1950) Anatomisch-biologische Untersuchungen über die Fortpflanzungstätigkeit des europäischen Rehes (Capreolus capreolus). Zeitschrift für Mikroskopisch-Anatomische Forschung 55, 427-530.
| Google Scholar |

Strandgaard H (1972) An investigation of Corpora lutea, embryonic development, and time of birth of roe deer (Capreolus capreolus) in Denmark. Danish Review of Game Biology 6(7), 1-22.
| Google Scholar |

Stubbe C, Stubbe M, Stubbe I (1981) Zur Reproduktion der Rehwildpopulation – Capreolus c. capreolus (L., 1758) – des Wildforschungsgebietes Hakel. Hercynia N. F 19(1), 97-109.
| Crossref | Google Scholar |

van Der Weijden VA, Bick JT, Bauersachs S, Rüegg AB, Hildebrandt TB, Goeritz F, Jewgenow K, Giesbertz P, Daniel H, Derisoud E, Chavatte-Palmer P, Bruckmaier RM, Drews B, Ulbrich SE (2021) Amino acids activate mTORC1 to release roe deer embryos from decelerated proliferation during diapause. Proceedings of the National Academy of Sciences 118, e2100500118.
| Crossref | Google Scholar |

Visser ME, Noordwijk AJv, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society of London. Series B: Biological Sciences 265, 1867-1870.
| Crossref | Google Scholar |

Wade-Smith J, Richmond ME, Mead RA, Taylor H (1980) Hormonal and gestational evidence for delayed implantation in the striped skunk, Mephitis mephitis. General and Comparative Endocrinology 42, 509-515.
| Crossref | Google Scholar | PubMed |

Wandeler AI (1975) Die Fortpflanzungsleistung des Rehes (Capreolus capreolus L.) im Berner Mittelland. Jahrbuch des Naturhistorischen Museums Bern 5, 245-296.
| Google Scholar |

Williams CT, Klaassen M, Barnes BM, Buck CL, Arnold W, Giroud S, Vetter SG, Ruf T (2017) Seasonal reproductive tactics: annual timing and the capital-to-income breeder continuum. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160250.
| Crossref | Google Scholar |

Ziegler L (1843) ‘Beobachtungen über die Brunst und den Embryo der Rehe.’ (Hellweg’sche Hofbuchhandlung: Hannover, Germany)