The ecology and evolution of reproductive timing and synchrony have been a topic of great interest in evolutionary ecology for decades. Originally motivated by questions related to behavioral and reproductive adaptation to environmental conditions, the topic has acquired new relevance in the face of climate change. However, there has been relatively little research on reproductive phenology in mammalian carnivores. The Eurasian lynx (Lynx lynx) occurs across the Eurasian continent, covering three of the four main climate regions of the world. Thus, their distribution includes a large variation in climatic conditions, making it an ideal species to explore reproductive phenology. Here, we used data on multiple reproductive events from 169 lynx females across Europe. Mean birth date was May 28 (April 23 to July 1), but was ~10 days later in northern Europe than in central and southern Europe. Birth dates were relatively synchronized across Europe, but more so in the north than in the south. Timing of birth was delayed by colder May temperatures. Severe and cold weather may affect neonatal survival via hypothermia and avoiding inclement weather early in the season may select against early births, especially at northern latitudes. Overall, only about half of the kittens born survived until onset of winter but whether kittens were born relatively late or early did not affect kitten survival. Lynx are strict seasonal breeders but still show a degree of flexibility to adapt the timing of birth to surrounding environmental conditions. We argue that lynx give birth later when exposed to colder spring temperatures and have more synchronized births when the window of favorable conditions for raising kittens is shorter. This suggests that lynx are well adapted to different environmental conditions, from dry and warm climates to alpine, boreal, and arctic climates. This variation in reproductive timing will be favorable in times of climate change, as organisms with high plasticity are more likely to adjust to new environmental conditions.

Centro de Ecología Instituto Venezolano de Investigaciones Científicas Caracas Venezuela

Chair of Wildlife Ecology and Management Faculty of Environment and Natural Resources University of Freiburg Freiburg Germany

Department of Forestry and Renewable Forest Resources Biotechnical Faculty University of Ljubljana Ljubljana Slovenia

Department of Forestry and Wildlife Management Inland Norway University of Applied Sciences Koppang Norway

Department of Research and Nature Protection Šumava National Park Administration Kašperské Hory Czech Republic

Department of Visitor Management and National Park Monitoring Bavarian Forest National Park Grafenau Germany

Department of Zoology Institute of Ecology and Earth Sciences University of Tartu Tartu Estonia

Ekoakademi Ekolojik Danışmanlık Aydın Turkey

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Foundation KORA Ittigen Switzerland

Geonatura Zagreb Croatia

Grimsö Wildlife Research Station Department of Ecology Swedish University of Agricultural Sciences Sweden

Harz National Park Wernigerode Germany

Institute of Nature Conservation Polish Academy of Sciences Kraków Poland

Latvian State Forest Research Institute Silava Salaspils Latvia

Macedonian Ecological Society Skopje Macedonia

Mammal Research Institute Polish Academy of Sciences Białowieża Poland

Norwegian Institute for Nature Research Oslo Norway

Norwegian Institute for Nature Research Trondheim Norway

NP OÖ Kalkalpen GesmbH Molln Austria

Progetto Lince Italia Tarvisio Italy

Wildlife Sciences Georg August University Goettingen Germany

Zobrazit více v PubMed

Andrews, C. J. , Thomas, D. G. , Yapura, J. , & Potter, M. A. (2019). Reproductive biology of the 38 extant felid species: A review. Mammal Review, 49, 16–30.

Balme, G. A. , Batchelor, A. , Britz, N. D. , Seymour, G. , Grover, M. , Hes, L. , Macdonald, D. W. , & Hunter, L. T. B. (2013). Reproductive success of female leopards Panthera pardus: The importance of top‐down processes. Mammal Review, 43, 221–237.

Bates, B. , Maechler, M. , Bolker, B. , & Walker, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67, 1–48.

Belotti, E. , Weder, N. , Bufka, L. , Kaldhusdal, A. , Küchenhoff, H. , Seibold, H. , Woelfing, B. , & Heurich, M. (2015). Patterns of Lynx predation at the interface between protected areas and multi‐use landscapes in Central Europe. PLoS One, 10, e0138139. PubMed PMC

Bivand, R. , Pebesma, E. , & Gomez‐Rubio, V. (2013). Applied spatial data analysis with R (2nd ed.). Springer.

Boutros, D. , Breitenmoser‐Würsten, C. , Zimmermann, F. , Ryser, A. , Molinari‐Jobin, A. , Capt, S. , Guntert, M. , & Breitenmoser, U. (2007). Characterisation of Eurasian lynx Lynx lynx den sites and kitten survival. Wildlife Biology, 13, 417–429.

Boutin, S. , & Lane, J. E. (2014). Climate change and mammals: evolutionary versus plastic responses. Evolutionary Applications, 7, 29–41. PubMed PMC

Bowyer, R. T. , Van Ballenberghe, V. , & Kie, J. G. (1998). Timing and synchrony of parturition in Alaskan moose: Long‐term versus proximal effects of climate. Journal of Mammalogy, 79, 1332–1344.

Boyce, M. S. (1979). Seasonality and patterns of natural selection for life histories. American Naturalist, 114, 569–583.

Breitenmoser, U. , Kavczensky, P. , Dötterer, M. , Breitenmoser‐Würsten, C. , Capt, S. , Bernhart, F. , & Liberek, M. (1993). Spatial‐organization and recruitment of Lynx (Lynx‐Lynx) in a reintroduced population in the Swiss Jura Mountains. Journal of Zoology, 231, 449–464.

Chmura, H. E. , Kharouba, H. M. , Ashander, J. , Ehlman, S. M. , Rivest, E. B. , & Yang, L. H. (2019). The mechanisms of phenology: The patterns and processes of phenological shifts. Ecological Monographs, 89(1), e01337.

Clutton‐Brock, T. H. , Major, M. , Albon, S. D. , & Guinness, F. E. (1987). Early development and population‐dynamics in Red Deer 1. Density‐dependent effects on juvenile survival. Journal of Animal Ecology, 56, 53–67.

English, A. K. , Chauvenet, A. L. M. , Safi, K. , & Pettorelli, N. (2012). Reassessing the determinants of breeding synchrony in ungulates. PLoS One, 7, e41444. PubMed PMC

Fick, S. E. , & Hijmans, R. J. (2017). WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315.

Gaillard, J. M. , Boutin, J. M. , Delorme, D. , VanLaere, G. , Duncan, P. , & Lebreton, J. D. (1997). Early survival in roe deer: Causes and consequences of cohort variation in two contrasted populations. Oecologia, 112, 502–513. PubMed

Gaillard, J. M. , Nilsen, E. B. , Odden, J. , Andrén, H. , & Linnell, J. D. C. (2014). One size fits all: Eurasian lynx females share a common optimal litter size. Journal of Animal Ecology, 83, 107–115. PubMed

Garcia‐Rodriguez, A. , Rigg, R. , Elguero‐Claramunt, I. , Bojarska, K. , Krofel, M. , Parchizadeh, J. , Pataky, T. , Seryodkin, I. , Skuban, M. , Wabakken, P. , Zieba, F. , Zwijacz‐Kozica, T. , & Selva, N. (2020). Phenology of brown bear breeding season and related geographical cues. European Zoological Journal, 87, 552–558.

Gervasi, V. , Nilsen, E. B. , Odden, J. , Bouyer, Y. , & Linnell, J. D. C. (2014). The spatio‐temporal distribution of wild and domestic ungulates modulates lynx kill rates in a multi‐use landscape. Journal of Zoology, 292, 175–183.

Gittleman, J. L. , & Thompson, S. D. (1988). Energy allocation in mammalian reproduction. American Zoologist, 28, 863–875.

Grøtan, V. , Sæther, B. E. , Engen, S. , Solberg, E. J. , Linnell, J. D. C. , Andersen, R. , Brøseth, H. , & Lund, E. (2005). Climate causes large‐scale spatial synchrony in population fluctuations of a temperate herbivore. Ecology, 86, 1472–1482.

Heurich, M. , Premier, J. , Oeser, J. , Streif, S. , Bastianelli, M. , Morelle, K. , Focardi, S. , De Groeve, J. , Urbano, F. , & Cagnacci, F. (2021). EUROLYNX: Collaborative science for studying Eurasian lynx movement ecology at the range of its distribution. Cat News Special Issue, 14, 60–63.

Hijmans, R. J. (2022). raster: Geographic data analysis and modeling . R package version 3.5‐15.

Hodge, S. J. , Bell, M. B. V. , & Cant, M. A. (2011). Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal. Biology Letters, 7, 54–56. PubMed PMC

Ims, R. A. (1990). The ecology and evolution of reproductive synchrony. Trends in Ecology & Evolution, 5, 135–140. PubMed

Jansen, B. D. , & Jenks, J. A. (2012). Birth timing for Mountain Lions (Puma concolor); testing the prey availability hypothesis. PLoS One, 7, e44625. PubMed PMC

Jewgenow, K. , Painer, J. , Amelkina, O. , Dehnhard, M. , & Goeritz, F. (2014). Lynx reproduction – long‐lasting life cycle of corpora lutea in a feline species. Reproductive Biology, 14, 83–88. PubMed

Jönsson, K. I. (1997). Capital and income breeding as alternative tactics of resource use in reproduction. Oikos, 78, 57–66.

Kourkgy, C. , Garel, M. , Appolinaire, J. , Loison, A. , & Toigo, C. (2016). Onset of autumn shapes the timing of birth in Pyrenean chamois more than onset of spring. Journal of Animal Ecology, 85, 581–590. PubMed

Krishnamoorthy, K. , & Lee, M. (2014). Improved tests for the equality of normal coefficients of variation. Computational Statistics, 29, 215–232.

Krofel, M. , Fležar, U. , Hočevar, L. , Sindičić, M. , Gomerčić, T. , Konec, M. , Slijepčević, M. , Bartol, M. , Črtalič, J. , Jelenčič, M. , Kljun, M. , Molinari‐Jobin, A. , Pičulin, A. , Potočnik, H. , Rot, A. , Skrbinšek, T. , Topličanec, I. , & Černe, R. (2021). Surveillance of the reinforcement process of the Dinaric – SE Alpine lynx population in the lynx‐monitoring year 2019–2020 .

Krofel, M. , Huber, D. , & Kos, I. (2011). Diet of Eurasian lynx Lynx lynx in the northern Dinaric Mountains (Slovenia and Croatia) importance of edible dormouse Glis glis as alternative prey. Acta Theriologica, 56, 315–322.

Krofel, M. , Skrbinsek, T. , & Kos, I. (2013). Use of GPS location clusters analysis to study predation, feeding, and maternal behavior of the Eurasian lynx. Ecological Research, 28, 103–116.

Laundré, J. W. , & Hernandez, L. (2007). Do female pumas (Puma concolor) exhibit a birth pulse? Journal of Mammalogy, 88, 1300–1304.

Lenth, R. V. (2022). emmeans: Estimated marginal means, aka least‐squares means . R package version 1.7.4‐1.

Linnell, J. D. C. , Aanes, R. , & Andersen, R. (1995). Who killed Bambi? The role of predation in the neonatal mortality of temperate ungulates. Wildlife Biology, 1, 209–223.

Linnell, J. D. C. , Breitenmoser, U. , Breitenmoser‐Würsten, C. , Odden, J. , & von Arx, M. (2009). The recovery of Eurasian lynx in Europe: What part has reintroduction played? In Hayward M. W. & Somers M. J. (Eds.), Reintroduction of top‐order predators (pp. 72–91). Wiley‐Blackwell.

Loarie, S. R. , Duffy, P. B. , Hamilton, H. , Asner, G. P. , Field, C. B. , & Ackerly, D. D. (2009). The velocity of climate change. Nature, 462, 1052–1111. PubMed

Lüdecke, D. , Ben‐Shachar, M. S. , Patil, I. , Waggoner, P. , & Makowski, D. (2021). Performance: An R package for assessment, comparison and testing of statistical models. Journal of Open Source Software, 6, 3139.

Mahoney, P. J. , Joly, K. , Borg, B. L. , Sorum, M. S. , Rinaldi, T. A. , Saalfeld, D. , Golden, H. , Latham, A. D. M. , Kelly, A. P. , Mangipane, B. , Koizumi, C. L. , Neufeld, L. , Hebblewhite, M. , Boelman, N. T. , & Prugh, L. R. (2020). Denning phenology and reproductive success of wolves in response to climate signals. Environmental Research Letters, 15, 125001.

Marwick, B. , & Krishnamoorthy, K . (2019). cvequality: Tests for the equality of coefficients of variation from multiple groups .

Mattisson, J. , Arntsen, G. B. , Nilsen, E. B. , Loe, L. E. , Linnell, J. D. C. , Odden, J. , Persson, J. , & Andren, H. (2014). Lynx predation on semi‐domestic reindeer: Do age and sex matter? Journal of Zoology, 292, 56–63.

Mattisson, J. , Odden, J. , Linnell, J. D. , Painer, J. , Persson, J. , & Andrén, H. (2020). Parturition dates in wild Eurasian lynx: Evidence of a second oestrus? Mammalian Biology, 100, 549–552.

Mattisson, J. , Odden, J. , Nilsen, E. B. , Linnell, J. D. C. , Persson, J. , & Andren, H. (2011). Factors affecting Eurasian lynx kill rates on semi‐domestic reindeer in northern Scandinavia: Can ecological research contribute to the development of a fair compensation system? Biological Conservation, 144, 3009–3017.

Mengüllüoğlu, D. , Ambarli, H. , Berger, A. , & Hofer, H. (2018). Foraging ecology of Eurasian lynx populations in Southwest Asia: Conservation implications for a diet specialist. Ecology and Evolution, 8, 9451–9463. PubMed PMC

Michel, E. S. , Strickland, B. K. , Demarais, S. , Belant, J. L. , Kautz, T. M. , Duquette, J. F. , Beyer, D. E. , Chamberlain, M. J. , Miller, K. V. , Shuman, R. M. , Kilgo, J. C. , Diefenbach, D. R. , Wallingford, B. D. , Vreeland, J. K. , Ditchkoff, S. S. , DePerno, C. S. , Moorman, C. E. , Chitwood, M. C. , & Lashley, M. A. (2020). Relative reproductive phenology and synchrony affect neonate survival in a nonprecocial ungulate. Functional Ecology, 34, 2536–2547.

Molinari‐Jobin, A. , Molinari, P. , Loison, A. , Gaillard, J. M. , & Breitenmoser, U. (2004). Life cycle period and activity of prey influence their susceptibility to predators. Ecography, 27, 323–329.

Molinari‐Jobin, A. , Zimmermann, F. , Ryser, A. , Molinari, P. , Haller, H. , Breitenmoser‐Würsten, C. , Capt, S. , Eyholzer, R. , & Breitenmoser, U. (2007). Variation in diet, prey selectivity and home‐range size of Eurasian lynx Lynx lynx in Switzerland. Wildlife Biology, 13, 393–405.

Mueller, S. A. , Prost, S. , Anders, O. , Breitenmoser‐Würsten, C. , Kleven, O. , Klinga, P. , Konec, M. , Kopatz, A. , Krojerová‐Prokešová, J. , Middelhoff, T. L. , Obexer‐Ruff, G. , Reiners, T. E. , Schmidt, K. , Sindičič, M. , Skrbinšek, T. , Tám, B. , Saveljev, A. P. , Naranbaatar, G. , & Nowak, C. (2022). Genome‐wide diversity loss in reintroduced Eurasian lynx populations urges immediate conservation management. Biological Conservation, 266, 109442.

Odden, J. , Linnell, J. D. C. , & Andersen, R. (2006). Diet of Eurasian lynx, Lynx lynx, in the boreal forest of southeastern Norway: The relative importance of livestock and hares at low roe deer density. European Journal of Wildlife Research, 52, 237–244.

Painer, J. , Goeritz, F. , Dehnhard, M. , Hildebrandt, T. B. , Naidenko, S. V. , Sanchez, I. , Munoz, M. A. Q. , & Jewgenow, K. (2014). Hormone‐induced luteolysis on physiologically persisting corpora lutea in Eurasian and Iberian lynx (Lynx lynx and Lynx pardinus). Theriogenology, 82, 557–562. PubMed

Painer, J. , Jewgenow, K. , Dehnhard, M. , Arnemo, J. M. , Linnell, J. D. C. , Odden, J. , Hildebrandt, T. B. , & Goeritz, F. (2014). Physiologically persistent Corpora lutea in Eurasian Lynx (Lynx lynx) – Longitudinal ultrasound and endocrine examinations intra‐vitam. PLoS One, 9, e90469. PubMed PMC

Panzacchi, M. , Linnell, J. D. C. , Odden, J. , Odden, M. , & Andersen, R. (2008). When a generalist becomes a specialist: Patterns of red fox predation on roe deer fawns under contrasting conditions. Canadian Journal of Zoology, 86, 116–126.

Pelaez, M. , Gaillard, J. M. , Bollmann, K. , Heurich, M. , & Rehnus, M. (2020). Large‐scale variation in birth timing and synchrony of a large herbivore along the latitudinal and altitudinal gradients. Journal of Animal Ecology, 89, 1906–1917. PubMed

R Core Team . (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.

Riehl, C. (2018). Reproductive synchrony. In Vonk J. & Shackelford T. K. (Eds.), Encyclopedia of animal cognition and behavior. Springer International Publishing AG.

Rode, K. D. , Olson, J. , Eggett, D. , Douglas, D. C. , Durner, G. M. , Atwood, T. C. , Regehr, E. V. , Wilson, R. R. , Smith, T. , & St Martin, M. (2018). Den phenology and reproductive success of polar bears in a changing climate. Journal of Mammalogy, 99, 16–26.

Rutberg, A. T. (1987). Adaptive hypotheses of birth synchrony in ruminants ‐ an interspecific test. American Naturalist, 130, 692–710.

Samelius, G. , Andrén, H. , Liberg, O. , Linnell, J. D. C. , Odden, J. , Ahlqvist, P. , Segerström, P. , & Sköld, K. (2012). Spatial and temporal variation in natal dispersal by Eurasian lynx in Scandinavia. Journal of Zoology, 286, 120–130.

Schmidt, K. (1998). Maternal behaviour and juvenile dispersal in the Eurasian lynx. Acta Theriologica, 43, 391–408.

Schmidt, K. (2008). Behavioural and spatial adaptation of the Eurasian lynx to a decline in prey availability. Acta Theriologica, 53, 1–16.

Thackeray, S. J. , Henrys, P. A. , Hemming, D. , Bell, J. R. , Botham, M. S. , Burthe, S. , Helaouet, P. , Johns, D. G. , Jones, I. D. , Leech, D. I. , Mackay, E. B. , Massimino, D. , Atkinson, S. , Bacon, P. J. , Brereton, T. M. , Carvalho, L. , Clutton‐Brock, T. H. , Duck, C. , Edwards, M. , … Wanless, S. (2016). Phenological sensitivity to climate across taxa and trophic levels. Nature, 535, 241–U294. PubMed

Thackeray, S. J. , Sparks, T. H. , Frederiksen, M. , Burthe, S. , Bacon, P. J. , Bell, J. R. , Botham, M. S. , Brereton, T. M. , Bright, P. W. , Carvalho, L. , Clutton‐Brock, T. , Dawson, A. , Edwards, M. , Elliott, J. M. , Harrington, R. , Johns, D. , Jones, I. D. , Jones, J. T. , Leech, D. I. , … Wanless, S. (2010). Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Global Change Biology, 16(12), 3304–3313.

Valdmann, H. , Andersone‐Lilley, Z. , Koppa, O. , Ozolins, J. , & Bagrade, G. (2005). Winter diets of wolf Canis lupus and lynx Lynx lynx in Estonia and Latvia. Acta Theriologica, 50, 521–527.

Vogt, K. , Vimercati, E. , Ryser, A. , Hofer, E. , Signer, S. , Signer, C. , & Breitenmoser, U. (2018). Suitability of GPS telemetry for studying the predation of Eurasian lynx on small‐ and medium‐sized prey animals in the Northwestern Swiss Alps. European Journal of Wildlife Research, 64, 73.

Vucetich, J. A. , Smith, D. W. , & Stahler, D. R. (2005). Influence of harvest, climate and wolf predation on Yellowstone elk, 1961‐2004. Oikos, 111, 259–270.

Walton, Z. , Mattisson, J. , Linnell, J. D. , Stien, A. , & Odden, J. (2017). The cost of migratory prey: seasonal changes in semi‐domestic reindeer distribution influences breeding success of Eurasian lynx in northern Norway. Oikos, 126(5), 642–650.

White, S. , Briers, R. A. , Bouyer, Y. , Odden, J. , & Linnell, J. D. C. (2015). Eurasian lynx natal den site and maternal home‐range selection in multi‐use landscapes of Norway. Journal of Zoology, 297, 87–98.

Wickham, H. (2011). The Split‐apply‐combine strategy for data analysis. Journal of Statistical Software, 40, 1–29.

Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer‐Verlag.

Wickham, H. , Averick, M. , Bryan, J. , Chang, W. , D'Agostino, L. , François, R. , Grolemund, G. , Hayes, A. , Henry, L. , Hester, J. , Kuhn, M. , Lin Pedersen, T. , Miller, E. , Milton Bache, S. , Müller, K. , Ooms, J. , Robinson, D. , Paige Seidel, D. , Spinu, V. , … Yutani, H. (2019). Welcome to the tidyverse. Journal of Open Source Software, 4, 1686.

Zettlemoyer, M. A. , & Peterson, M. L. (2021). Does phenological plasticity help or hinder range shifts under climate change? Frontiers in Ecology and Evolution, 9, 689192.

Zimmermann, F. , Breitenmoser‐Würsten, C. , & Breitenmoser, U. (2005). Natal dispersal of Eurasian lynx (Lynx lynx) in Switzerland. Journal of Zoology, 267, 381–395.

Žunna, A. , Ozoliņš, J. , Stepanova, A. , Ornicāns, A. , & Bagrade, G. (2011). Food habits of the lynx (Lynx lynx) in Latvia based on hunting data. In Stubbe M. (Ed.), Beiträge zur Jagd‐ und Wildforschung (pp. 309–317). Gesellschaft für Wildtier‐ und Jagdforschung e.V.

Survival of Eurasian lynx in the human-dominated landscape of Europe

Rehabilitation and release of orphaned Eurasian lynx (Lynx lynx) in Europe: Implications for management and conservation

Zobrazit více v PubMed

Dryad
10.5061/dryad.xksn02vjk