There are several mechanisms that allow plants to temporarily escape from top-down control. One of them is trophic cascades triggered by top predators or pathogens. Another is satiation of consumers by mast seeding. These two mechanisms have traditionally been studied in separation. However, their combined action may have a greater effect on plant release than either process alone. In 2015, an outbreak of a disease (African swine fever, ASF) caused a crash in wild boar (Sus scrofa) abundance in Białowieża Primeval Forest. Wild boar are important consumers of acorns and are difficult to satiate relative to less mobile granivores. We hypothesized that the joint action of the ASF outbreak and masting would enhance regeneration of oaks (Quercus robur). Data from ungulate exclosures demonstrated that ASF led to reduction in acorn predation. Tree seedling data indicated that oak recruitment increased twofold relative to pre-epidemic period. Our results showed that perturbations caused by wildlife disease travel through food webs and influence forest dynamics. The outbreak of ASF acted synergistically with masting and removed herbivore top-down control of oaks by mobile consumers. This illustrates that the ASF epidemic that currently occurs across Europe can have broad effects on forest dynamics.

Department of Forest Biodiversity Faculty of Forestry University of Agriculture al 29 Listopada 46 31 425 Kraków Poland

Department of Forest Management Planning Dendrometry and Forest Economics Institute of Forests Sciences Warsaw University of Life Sciences Nowoursynowska Str 159 Warszawa 02 776 Poland

Department of Forest Resources Management Forest Research Institute Sękocin Stary ul Braci Leśnej 3 05 090 Raszyn Poland

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Kamýcká 129 165 00 Prague Czech Republic

Department of Systematic Zoology Faculty of Biology Adam Mickiewicz University in Poznań Ulica Uniwersytetu Poznańskiego 6 Poznań 61 614 Poland

INRAE LESSEM University Grenoble Alpes 2 rue de la Papeterie BP 76 Saint Martin d'Hères 38400 France

Mammal Research Institute Polish Academy of Sciences Ul Stoczek 1 17 230 Białowieża Poland

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Kelly D, Sork VL. 2002. Mast seeding in perennial plants: why, how, where? Annu. Rev. Ecol. Syst. 33, 427-447. (10.1146/annurev.ecolsys.33.020602.095433) DOI

Dale EE, Foest JJ, Hacket-Pain A, Bogdziewicz M, Tanentzap AJ. 2021. Macroevolutionary consequences of mast seeding. Phil. Trans. R. Soc. B 376, 20200372. (10.1098/rstb.2020.0372) PubMed DOI PMC

Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM. 2010. The functional response of a hoarding seed predator to mast seeding. Ecology 91, 2673-2683. (10.1890/09-1816.1) PubMed DOI

Koenig WD, Kelly D, Sork VL, Duncan RP, Elkinton JS, Peltonen MS, Westfall RD. 2003. Dissecting components of population-level variation in seed production and the evolution of masting behavior. Oikos 102, 581-591. (10.1034/j.1600-0706.2003.12272.x) DOI

Kelly D. 2021. Mast seeding: the devil (and the delight) is in the detail. New Phytol. 229, 1829-1831. (10.1111/nph.16990) PubMed DOI

Curran LM, Webb CO. 2000. Experimental tests of the spatiotemporal scale of seed predation in mast-fruiting Dipterocarpaceae. Ecol. Monogr. 70, 129-148. (10.1890/0012-9615(2000)070[0129:ETOTSS]2.0.CO;2) DOI

Bogdziewicz M, Szymkowiak J, Tanentzap AJ, Calama R, Marino S, Steele MA, Seget B, Piechnik Ł, Żywiec M. 2021. Seed predation selects for reproductive variability and synchrony in perennial plants. New Phytol. 229, 2357-2364. (10.1111/nph.16835) PubMed DOI PMC

Zwolak R, Celebias P, Bogdziewicz M. In press. Global patterns in the predator satiation effect of masting—a meta-analysis. Proc. Natl Acad. Sci. USA. PubMed PMC

Ripple WJ, et al. 2014. Status and ecological effects of the world's largest carnivores. Science 343, 1241484. (10.1126/science.1241484) PubMed DOI

Bubnicki JW, Churski M, Schmidt K, Diserens TA, Kuijper DP. 2019. Linking spatial patterns of terrestrial herbivore community structure to trophic interactions. eLife 8, e44937. (10.7554/eLife.44937) PubMed DOI PMC

Hebblewhite M, White CA, Nietvelt CG, McKenzie JA, Hurd TE, Fryxell JM, Bayley SE, Paquet PC. 2005. Human activity mediates a trophic cascade caused by wolves. Ecology 86, 2135-2144. (10.1890/04-1269) DOI

Prins HHT, van der Jeugd HP. 1993. Herbivore population crashes and woodland structure in East Africa. J. Ecol. 81, 305-314. (10.2307/2261500) DOI

Buck JC, Ripple WJ. 2017. Infectious agents trigger trophic cascades. Trends Ecol. Evol. 32, 681-694. (10.1016/j.tree.2017.06.009) PubMed DOI

Gallardo MC, Reoyo AdlT, Fernández-Pinero J, Iglesias I, Muñoz MJ, Arias ML. 2015. African swine fever: a global view of the current challenge. Porc. Health Manag. 1, 21. (10.1186/s40813-015-0013-y) PubMed DOI PMC

Morelle K, Bubnicki J, Churski M, Gryz J, Podgórski T, Kuijper DPJ. 2020. Disease-induced mortality outweighs hunting in causing wild boar population crash after African Swine fever outbreak. Front. Vet. Sci. 7, 378. (10.3389/fvets.2020.00378) PubMed DOI PMC

Sánchez-Cordón PJ, Montoya M, Reis AL, Dixon LK. 2018. African swine fever: a re-emerging viral disease threatening the global pig industry. Vet. J. 233, 41-48. (10.1016/j.tvjl.2017.12.025) PubMed DOI PMC

Gómez JM, Hódar JA. 2008. Wild boars (Sus scrofa) affect the recruitment rate and spatial distribution of holm oak (Quercus ilex). Forest Ecol. Manag. 256, 1384-1389. (10.1016/j.foreco.2008.06.045) DOI

Burrascano S, Copiz R, Vico ED, Fagiani S, Giarrizzo E, Mei M, Mortelliti A, Sabatini FM, Blasi C. 2015. Wild boar rooting intensity determines shifts in understorey composition and functional traits. Community Ecol. 16, 244-253. (10.1556/168.2015.16.2.12) DOI

Cocquelet A, Mårell A, Bonthoux S, Baltzinger C, Archaux F. 2019. Direct and indirect effects of ungulates on forest birds' nesting failure? An experimental test with artificial nests. Forest Ecol. Manag. 437, 148-155. (10.1016/j.foreco.2019.01.025) DOI

van Ginkel HAL, Kuijper DPJ, Churski M, Zub K, Szafrańska P, Smit C. 2013. Safe for saplings not safe for seeds: Quercus robur recruitment in relation to coarse woody debris in Białowieża Primeval Forest, Poland. Forest Ecol. Manag. 304, 73-79. (10.1016/j.foreco.2013.04.037) DOI

Bogdziewicz M, Zwolak R, Crone EE. 2016. How do vertebrates respond to mast seeding? Oikos 125, 300-307. (10.1111/oik.03012) DOI

Gamelon M, Focardi S, Baubet E, Brandt S, Franzetti B, Ronchi F, Venner S, Sæther BE, Gaillard JM. 2017. Reproductive allocation in pulsed-resource environments: a comparative study in two populations of wild boar. Oecologia 183, 1065-1076. (10.1007/s00442-017-3821-8) PubMed DOI

Touzot L, Schermer É, Venner S, Delzon S, Rousset C, Baubet É, Gaillard J-M, Gamelon M. 2020. How does increasing mast seeding frequency affect population dynamics of seed consumers? Wild boar as a case study. Ecol. Appl. 30, e02134. (10.1002/eap.2134) PubMed DOI

Podgórski T, Baś G, Jędrzejewska B, Sönnichsen L, Śnieżko S, Jędrzejewski W, Okarma H. 2013. Spatiotemporal behavioral plasticity of wild boar (Sus scrofa) under contrasting conditions of human pressure: primeval forest and metropolitan area. J. Mammal. 94, 109-119. (10.1644/12-MAMM-A-038.1) DOI

Bisi F, Chirichella R, Chianucci F, Von Hardenberg J, Cutini A, Martinoli A, Apollonio M. 2018. Climate, tree masting and spatial behaviour in wild boar (Sus scrofa L.): insight from a long-term study. Ann. Forest Sci. 75, 46. (10.1007/s13595-018-0726-6) DOI

Bogdziewicz M, Marino S, Bonal R, Zwolak R, Steele MA. 2018. Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation. Ecology 99, 2575-2582. (10.1002/ecy.2510) PubMed DOI

Jaroszewicz B, Cholewińska O, Gutowski JM, Samojlik T, Zimny M, Latałowa M. 2019. Białowieża forest—a relic of the high naturalness of European forests. Forests 10, 849. (10.3390/f10100849) DOI

Bogdziewicz M, et al. 2017. Masting in wind-pollinated trees: system-specific roles of weather and pollination dynamics in driving seed production. Ecology 98, 2615-2625. (10.1002/ecy.1951) PubMed DOI

Schermer É, et al. 2019. Pollen limitation as a main driver of fruiting dynamics in oak populations. Ecol. Lett. 22, 98-107. (10.1111/ele.13171) PubMed DOI

Crawley MJ, Long CR. 1995. Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. J. Ecol. 83, 683-696. (10.2307/2261636) DOI

Bosch J, Iglesias I, Muñoz MJ, de la Torre A. 2017. A cartographic tool for managing African swine fever in Eurasia: mapping wild boar distribution based on the quality of available habitats. Transboundary Emerging Dis. 64, 1720-1733. (10.1111/tbed.12559) PubMed DOI

Schley L, Roper TJ. 2003. Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops. Mamm. Rev. 33, 43-56. (10.1046/j.1365-2907.2003.00010.x) DOI

Groot Bruinderink GWTA, Hazebroek E, Van Der Voot H. 1994. Diet and condition of wild boar, Sus scrofu scrofu, without supplementary feeding. J. Zool. 233, 631-648. (10.1111/j.1469-7998.1994.tb05370.x) DOI

Herrero J, Irizar I, Laskurain NA, García-Serrano A, García-González R. 2005. Fruits and roots: wild boar foods during the cold season in the Southwestern Pyrenees. Italian J. Zool. 72, 49-52. (10.1080/11250000509356652) DOI

Jedrzejewska B, Jedrzejewski W, Bunevich AN, Milkowski L, Krasinski ZA. 1997. Factors shaping population densities and increase rates of ungulates in Bialowieza Primeval Forest (Poland and Belarus) in the 19th and 20th centuries. Acta Theriologica 42, 399-451.

Keuling O, Stier N, Roth M. 2008. Annual and seasonal space use of different age classes of female wild boar Sus scrofa L. Eur. J. Wildl. Res. 54, 403-412. (10.1007/s10344-007-0157-4) DOI

Kuijper DPJ, Cromsigt JPGM, Jędrzejewska B, Miścicki S, Churski M, Jędrzejewski W, Kweczlich I. 2010. Bottom-up versus top-down control of tree regeneration in the Białowieża Primeval Forest, Poland. J. Ecol. 98, 888-899. (10.1111/j.1365-2745.2010.01656.x) DOI

Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM. 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378-400.

Hartig F. 2020. DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. See https://cran.rproject.org/web/packages/DHARMa/vignettes/DHARMa.html.

Curran LM, Leighton M. 2000. Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecol. Monogr. 70, 101-128. (10.1890/0012-9615(2000)070[0101:VRTSVI]2.0.CO;2) DOI

Dobson A, Crawley M. 1994. Pathogens and the structure of plant communities. Trends Ecol. Evol. 9, 393-398. (10.1016/0169-5347(94)90062-0) PubMed DOI

Vesterdal L, Clarke N, Sigurdsson BD, Gundersen P. 2013. Do tree species influence soil carbon stocks in temperate and boreal forests? Forest Ecol. Manag. 309, 4-18. (10.1016/j.foreco.2013.01.017) DOI

Courbaud B, et al. 2021. Factors influencing the rate of formation of tree-related microhabitats and implications for biodiversity conservation and forest management. J. Appl. Ecol. 59, 492-503. (10.1111/1365-2664.14068) DOI

Scheffer M, van Nes EH, Holmgren M, Hughes T. 2008. Pulse-driven loss of top-down control: the critical-rate hypothesis. Ecosystems 11, 226-237. (10.1007/s10021-007-9118-8) DOI

Churski M, Bubnicki JW, Jędrzejewska B, Kuijper DPJ, Cromsigt JPGM. 2017. Brown world forests: increased ungulate browsing keeps temperate trees in recruitment bottlenecks in resource hotspots. New Phytol. 214, 158-168. (10.1111/nph.14345) PubMed DOI

Kuijper DPJ, Jędrzejewska B, Brzeziecki B, Churski M, Jędrzejewski W, Żybura H. 2010. Fluctuating ungulate density shapes tree recruitment in natural stands of the Białowieża Primeval Forest, Poland. J. Veget. Sci. 21, 1082-1098. (10.1111/j.1654-1103.2010.01217.x) DOI

Pucek Z, Jędrzejewski W, Jędrzejewska B, Pucek M. 1993. Rodent population dynamics in a primeval deciduous forest (Białowieża National Park) in relation to weather, seed crop, and predation. Acta Theriologica 38, 199-232. (10.4098/AT.ARCH.93-18) DOI

Pesendorfer MB, Bogdziewicz M, Szymkowiak J, Borowski Z, Kantorowicz W, Espelta JM, Fernández-Martínez M. 2020. Investigating the relationship between climate, stand age, and temporal trends in masting behavior of European forest trees. Glob. Change Biol. 26, 1654-1667. (10.1111/gcb.14945) PubMed DOI PMC

Smit C, Kuijper DPJ, Prentice D, Wassen MJ, Cromsigt JPGM. 2012. Coarse woody debris facilitates oak recruitment in Białowieża Primeval Forest, Poland. Forest Ecol. Manag. 284, 133-141. (10.1016/j.foreco.2012.07.052) DOI

Kuijper DPJ, de Kleine C, Churski M, van Hooft P, Bubnicki J, Jędrzejewska B. 2013. Landscape of fear in Europe: wolves affect spatial patterns of ungulate browsing in Białowieża Primeval Forest, Poland. Ecography 36, 1263-1275. (10.1111/j.1600-0587.2013.00266.x) DOI

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