Protecting structural features, such as tree-related microhabitats (TreMs), is a cost-effective tool crucial for biodiversity conservation applicable to large forested landscapes. Although the development of TreMs is influenced by tree diameter, species, and vitality, the relationships between tree age and TreM profile remain poorly understood. Using a tree-ring-based approach and a large data set of 8038 trees, we modeled the effects of tree age, diameter, and site characteristics on TreM richness and occurrence across some of the most intact primary temperate forests in Europe, including mixed beech and spruce forests. We observed an overall increase in TreM richness on old and large trees in both forest types. The occurrence of specific TreM groups was variably related to tree age and diameter, but some TreM groups (e.g., epiphytes) had a stronger positive relationship with tree species and elevation. Although many TreM groups were positively associated with tree age and diameter, only two TreM groups in spruce stands reacted exclusively to tree age (insect galleries and exposed sapwood) without responding to diameter. Thus, the retention of trees for conservation purposes based on tree diameter appears to be a generally feasible approach with a rather low risk of underrepresentation of TreMs. Because greater tree age and diameter positively affected TreM development, placing a greater emphasis on conserving large trees and allowing them to reach older ages, for example, through the establishment of conservation reserves, would better maintain the continuity of TreM resource and associated biodiversity. However, this approach may be difficult due to the widespread intensification of forest management and global climate change.

Importancia de conservar los árboles viejos y grandes para la continuidad de los microhábitats relacionados Resumen La protección de las características estructurales, como los microhábitats relacionados a los árboles (MhAr), es una herramienta económica importante para la conservación de la biodiversidad que puede aplicarse en los paisajes boscosos extensos. Aunque el diámetro, especie y vitalidad del árbol influyen sobre el desarrollo de los MhAr, todavía se sabe poco sobre las relaciones entre la edad del árbol y el perfil. Modelamos los efectos de la edad y diámetro del árbol y las características del sitio sobre la riqueza y presencia de los MhAr en algunos de los bosques primarios más preservados de Europa, incluyendo los bosques mixtos de hayas y abetos, con una estrategia basada en los anillos de crecimiento y un conjunto con datos de 8038 árboles. Observamos un incremento generalizado en la riqueza de MhAr en los árboles viejos y grandes en ambos tipos de bosques. La presencia de grupos específicos de MhAr tuvo una relación variada con el diámetro y la edad del árbol, aunque algunos grupos de MhAr (p. ej.: epífitas) tuvieron una relación positiva más fuerte con la elevación y la especie del árbol. Mientras que muchos grupos de MhAr estuvieron asociados positivamente con la edad y diámetro del árbol, sólo dos grupos de MhAr en los abetos reaccionaron exclusivamente a la edad del árbol (galerías de insectos y savia expuesta) sin responder al diámetro. Por lo tanto, la retención de los árboles con fines de conservación basada en los diámetros parece ser una estrategia plausible con un riesgo bajo de subrepresentación de los MhAr. Ya que a mayor edad y diámetro del árbol hubo efectos positivos en el desarrollo de los MhAr, poner un mayor énfasis sobre la conservación de los árboles grandes y permitirles alcanzar una edad mayor, por ejemplo, a través del establecimiento de reservas de conservación, mantendría de mejor manera la continuidad del MhAr y de la biodiversidad asociada. Sin embargo, esta estrategia puede ser complicada debido a la intensificación generalizada de la gestión forestal y el cambio climático mundial.

Bern University of Applied Sciences School of Agricultural Forest and Food Sciences HAFL Zollikofen and Swiss Federal Institute for Forest Snow and Landscape Research WSL Birmensdorf Switzerland

Department of Biology and General Ecology Faculty of Ecology and Environmental Sciences Technical University in Zvolen Zvolen Slovakia

Department of Forest Ecology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Prague Czech Republic

Forest Biometrics Laboratory Faculty of Forestry 'Stefan cel Mare' University of Suceava Suceava Romania

Univ Grenoble Alpes INRAE UR Lessem Lessem France

Université de Toulouse INRAE UMR DYNAFOR Castanet Tolosan France and CNPF CRPF Occitanie Tarbes France

University of Vermont Rubenstein School of Environment and Natural Resources Burlington Vermont USA

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Asbeck, T., Pyttel, P., Frey, J., & Bauhus, J. (2019). Predicting abundance and diversity of tree-related microhabitats in Central European montane forests from common forest attributes. Forest Ecology and Management, 432, 400-408.

Asbeck, T., Großmann, J., Paillet, Y., Winiger, N., & Bauhus, J. (2021a). The use of tree-related microhabitats as forest biodiversity indicators and to guide integrated forest management. Current Forestry Reports, 7, 59-68.

Asbeck, T., Kozák, D., Spînu, A. P., Mikoláš, M., Zemlerová, V., & Svoboda, M. (2021b). Tree-related microhabitats follow similar patterns but are more diverse in primary compared to managed temperate mountain forests. Ecosystems, 25, 712-726.

Basile, M., Asbeck, T., Jonker, M., Knuff, A. K., Bauhus, J., Braunisch, V., Mikusiński, G., & Storch, I. (2020a). What do tree-related microhabitats tell us about the abundance of forest-dwelling bats, birds, and insects? Journal of Environmental Management, 264, 110401.

Basile, M., Asbeck, T., Pacioni, C., Mikusiński, G., & Storch, I. (2020b). Woodpecker cavity establishment in managed forests: Relative rather than absolute tree size matters. Wildlife Biology, 1, 1-9.

Barredo, J. I., Brailescu, C., Teller, A., Sabatini, F. M., Mauri, A., & Janouskova, K. (2021). Mapping and assessment of primary and old-growth forests in Europe. Publications Office of the European Union.

Blicharska, M., & Mikusiński, G. (2014). Incorporating social and cultural significance of large old trees in conservation policy. Conservation Biology, 28(6), 1558-1567.

Brooks, M. E., Kristensen, K., Van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal, 9, 378-400.

Burrascano, S., De Andrade, R. B., Paillet, Y., Ódor, P., Antonini, G., Bouget, C., Campagnaro, T., Gosselin, F., Janssen, P., Persiani, A. M., Nascimbene, J., Sabatini, F. M., Stizia, T., & Blasi, C. (2018). Congruence across taxa and spatial scales: Are we asking too much of species data? Global Ecology and Biogeography, 27(8), 980-990.

Buse, J., Schröder, B., & Assmann, T. (2007). Modelling habitat and spatial distribution of an endangered longhorn beetle-A case study for saproxylic insect conservation. Biological Conservation, 137(3), 372-381.

Bütler, R., Lachat, T., Krumm, F., Kraus, D., & Larrieu, L. (2020). Field guide to tree-related microhabitats. Descriptions and size limits for their inventory. Swiss Federal Institute for Forest, Snow and Landscape Research WSL.

Courbaud, B., Pupin, C., Letort, A., Cabanettes, A., & Larrieu, L. (2017). Modelling the probability of microhabitat formation on trees using cross-sectional data. Methods in Ecology and Evolution, 8(10), 1347-1359.

Courbaud, B., Larrieu, L., Kozak, D., Kraus, D., Lachat, T., Ladet, S., Müller, J., Sagheb-Talebi, K., Schuck, A., Stillhard, J., Svoboda, M., & Zudin, S. (2022). Factors influencing the rate of formation of tree-related microhabitats and implications for biodiversity conservation and forest management. Journal of Applied Ecology, 59(2), 492-503.

Di Filippo, A., Biondi, F., Maugeri, M., Schirone, B., & Piovesan, G. (2012). Bioclimate and growth history affect beech lifespan in the Italian Alps and Apennines. Global Change Biology, 18, 960-972.

Duncan, R. P. (1989). An evaluation of errors in tree age estimates based on increment cores in kahikatea (Dacrycarpus dacrydioides). New Zealand Natural Sciences, 16, 31-37.

Fox, J., & Weisberg, S. (2019). An R companion to applied regression (3rd ed.).

Fritz, Ö., & Heilmann-Clausen, J. (2010). Rot holes create key microhabitats for epiphytic lichens and bryophytes on beech (Fagus sylvatica). Biological Conservation, 143(4), 1008-1016.

Gao, T., Nielsen, A. B., & Hedblom, M. (2015). Reviewing the strength of evidence of biodiversity indicators for forest ecosystems in Europe. Ecological Indicators, 57, 420-434.

Gouix, N., Sebek, P., Valladares, L., Brustel, H., & Brin, A. (2015). Habitat requirements of the violet click beetle (Limoniscus violaceus), an endangered umbrella species of basal hollow trees. Insect Conservation and Diversity, 8(5), 418-427.

Hagge, J., Bässler, C., Gruppe, A., Hoppe, B., Kellner, H., Krah, F. S., Müller, J., Siebold, S., Stengel, E., & Thorn, S. (2019). Bark coverage shifts assembly processes of microbial decomposer communities in dead wood. Proceedings of the Royal Society B, 286(1912), 20191744.

Handegard, E., Gjerde, I., Bollandsås, O. M., & Storaunet, K. O. (2021). Identifying old Norway spruce and Scots pine trees by morphological traits and site characteristics. Scandinavian Journal of Forest Research, 36(7-8), 550-562.

Hartig, F. (2022). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.5.

Holmes, R. L. (1983). Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bulletin, 43, 69-75.

Hubau, W., De Mil, T., Van den Bulcke, J., Phillips, O. L., Angoboy Ilondea, B., Van Acker, J., Sullivan, M. J. P., Nsenga, L., Toriambe, B., Couralet, C., Banin, L. F., Begne, S. K., Baker, T. R., Bourland, T., Chezeaux, E., Clark, C. J., Collins, M., Comiskey, J. A., Cuni-Sanchez, A., & Beeckman, H. (2019). The persistence of carbon in the African forest understory. Nature Plants, 5(2), 133-140.

Issartel, J., & Coiffard, C. (2011). Extreme longevity in trees: Live slow, die old? Oecologia, 165(1), 1-5.

IUCN. (2018). Raising the profile of primary and intact forests. International Union for the Conservation of Nature.

Jahed, R. R., Kavousi, M. R., Farashiani, M. E., Sagheb-Talebi, K., Babanezhad, M., Courbaud, B., Wirtz, R., Müller, J., & Larrieu, L. (2020). A comparison of the formation rates and composition of tree-related microhabitats in beech-dominated primeval Carpathian and Hyrcanian forests. Forests, 11(2), 144.

Janda, P., Tepley, A. J., Schurman, J. S., Brabec, M., Nagel, T. A., Bače, R., Begovič, K., Chaskovskyy, O., Čada, V., Dušátko, M., Frankovič, M., Kameniar, O., Kozák, D., Lábusová, J., Langbehn, T., Málek, J., Mikoláš, M., Nováková, M. H., Svobodová, K., & Svoboda, M. (2019). Drivers of basal area variation across primary late-successional Picea abies forests of the Carpathian Mountains. Forest Ecology and Management, 435, 196-204.

Janda, P., Trotsiuk, V., Mikoláš, M., Bače, R., Nagel, T. A., Seidl, R., Seedre, M., Morrissey, R. C., Kucbel, S., Jaloviar, P., Jasík, M., Vysoký, J., Šamonil, P., Čada, V., Mrhalová, H., Lábusová, J., Nováková, M. H., Rydval, M., Matějů, L., & Svoboda, M. (2017). The historical disturbance regime of mountain Norway spruce forests in the Western Carpathians and its influence on current forest structure and composition. Forest Ecology and Management, 388, 67-78.

Kraus, D., Bütler, R., Krumm, F., Lachat, T., Larrieu, L., Mergner, U., Paillet, Y., Schuck, A., & Winter, S. (2016). Catalogue of tree microhabitats: Reference field list. http://iplus.efi.int/uploads/Tree%20Microhabitat%20Catalogues/Catalogue_TreeMicrohabitats_EN.pdf

Krumm, F., Schuck, A., & Rigling, A. (2020). How to balance forestry and biodiversity conservation - A view across Europe. European Forest Institute (EFI); Swiss Federal Institute for Forest, Snow and Landscape Research (WSL).

Kozák, D., Mikoláš, M., Svitok, M., Bače, R., Paillet, Y., Larrieu, L., Nagel, T. A., Begovič, K., Čada, V., Diku, A., Frankovič, M., Janda, P., Kameniar, O., Keren, S., Kjučukov, P., Lábusová, J., Langbehn, T., Málek, J., Mikac, S., & Svoboda, M. (2018). Profile of tree-related microhabitats in European primary beech-dominated forests. Forest Ecology and Management, 429, 363-374.

Kõrkjas, M., Remm, L., & Lõhmus, A. (2021a). Development rates and persistence of the microhabitats initiated by disease and injuries in live trees: A review. Forest Ecology and Management, 482, 118833.

Kõrkjas, M., Remm, L., & Lõhmus, A. (2021b). Tree-related microhabitats on live Populus tremula and Picea abies in relation to tree age, diameter, and stand factors in Estonia. European Journal of Forest Research, 140(5), 1227-1241.

Kuhn, M., & Johnson, K. (2013). Applied predictive modeling. Springer.

Larrieu, L., & Cabanettes, A. (2012). Species, live status, and diameter are important tree features for diversity and abundance of tree microhabitats in subnatural montane beech-fir forests. Canadian Journal of Forest Research, 42, 1433-1445.

Larrieu, L., Cabanettes, A., Lachat, T., Paillet, Y., Winter, S., Gonin, P., Bouget, C., & Deconchat, M. (2014). Deadwood and tree-microhabitat dynamics in unmanaged temperate mountain mixed forests: A life-cycle approach for biodiversity monitoring. Forest Ecology and Management, 334, 163-173.

Larrieu, L., Paillet, Y., Winter, S., Bütler, R., Kraus, D., Krumm, F., Lachat, T., Michel, A. K., Regnery, B., & Vandekerkhove, K. (2018). Tree related microhabitats in temperate and Mediterranean European forests: A hierarchical typology for inventory standardization. Ecological Indicators, 84, 194-207.

Larrieu, L., Gosselin, F., Archaux, F., Chevalier, R., Corriol, G., Dauffy-Richard, E., Deconchat, M., Gosselin, M., Ladet, S., Savoie, J. M., Tillon, L., & Bouget, C. (2019). Assessing the potential of routine structural and dendrometric variables as potential habitat surrogates from multi-taxon data in European temperate forests. Ecological Indicators, 104, 116-126.

Larrieu, L., Cabanettes, A., Courbaud, B., Goulard, M., Heintz, W., Kozák, D., Kraus, D., Lachat, T., Ladet, S., Müller, J., Paillet, Y., Schuck, A., Stillhard, J., & Svoboda, M. (2021). Co-occurrence patterns of tree-related microhabitats: A method to simplify routine monitoring. Ecological Indicators, 127, 107757.

Larsson, L. A. (2003). CDendro: Cybis Dendro dating program. Cybis Elektronik & Data AB.

Lindenmayer, D. B., Laurance, W. F., & Franklin, J. F. (2012). Global decline in large old trees. Science, 338(6112), 1305-1306.

Lindenmayer, D. B., Laurance, W. F., Franklin, J. F., Likens, G. E., Banks, S. C., Blanchard, W., Gibbons, P., Ikin, K., Blair, D., McBurney, L., Manning, A. D., & Stein, J. A. R. (2014). New policies for old trees: Averting a global crisis in a keystone ecological structure. Conservation Letters, 7(1), 61-69.

Liu, J., Xia, S., Zeng, D., Liu, C., Li, Y., Yang, W., Yang, B., Zhang, J., Silk, F., & Lindenmayer, D. B. (2022). Age and spatial distribution of the world's oldest trees. Conservation Biology, 36, e13907.

Lutz, J. A., Furniss, T. J., Johnson, D. J., Davies, S. J., Allen, D., Alonso, A., Anderson-Texeira, K. J., Andrade, A., Baltzer, A., Becker, K. M. L., Blomdahl, E. M., Bourg, N. A., Bunyavejchewin, S., Burslem, D. F. R. P., Cansler, C. A., Cao, K., Cao, M., Cárdenas, D., Chang, L., … Zimmerman, J. K. (2018). Global importance of large-diameter trees. Global Ecology and Biogeography, 27(7), 849-864.

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(60), 3139.

Michel, A. K., Winter, S., & Linde, A. (2011). The effect of tree dimension on the diversity of bark microhabitat structures and bark use in Douglas-fir (Pseudotsuga menziesii var. menziesii). Canadian Journal of Forest Research, 41(2), 300-308.

Mikoláš, M., Ujházy, K., Jasík, M., Wiezik, M., Gallay, I., Polák, P., Vysoký, J., Čiliak, M., Meigs, G. W., Svoboda, M., Trotsiuk, V., & Keeton, W. S. (2019). Primary forest distribution and representation in a Central European landscape: Results of a large-scale field-based census. Forest Ecology and Management, 449, 117466.

Mitchell, R. J., Hewison, R. L., Beaton, J., & Douglass, J. R. (2021). Identifying substitute host tree species for epiphytes: The relative importance of tree size and species, bark and site characteristics. Applied Vegetation Science, 24(2), e12569.

Muys, B., Angelstam, P., Bauhus, J., Bouriaud, L., Jactel, H., Kraigher, H., Müller, J., Pettorelli, N., Pötzelsberger, E., Primmer, E., Svoboda, M., Thorsen, J. B., & Van Meerbeek, K. (2022). Forest biodiversity in Europe. From Science to Policy 13. European Forest Institute.

Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4(2), 133-142.

Paillet, Y., Archaux, F., Du Puy, S., Bouget, C., Boulanger, V., Debaive, N., Gilg, O., Gosselin, F., & Guilbert, E. (2018). The indicator side of tree microhabitats: A multi-taxon approach based on bats, birds and saproxylic beetles. Journal of Applied Ecology, 55(5), 2147-2159.

Paillet, Y., Debaive, N., Archaux, F., Cateau, E., Gilg, O., & Guilbert, E. (2019). Nothing else matters? Tree diameter and living status have more effects than biogeoclimatic context on microhabitat number and occurrence: An analysis in French forest reserves. PLoS One, 14(5), 1-18.

Pantic, D., Medarevic, M., Dees, M., Borota, D., Tubic, B., Obradovic, S., Šljukic, B., Čukovic, D., & Marinkovic, M. (2015). Analysis of the growth characteristics of a 450-year-old silver fir tree. Archives of Biological Sciences, 67(1), 155-160.

Pavlin, J., Nagel, T. A., Svitok, M., Pettit, J. L., Begović, K., Mikac, S., Dikku, A., Toromani, E., Panayotov, M., Zlatanov, T., Haruta, O., Dorog, S., Chaskovskyy, O., Mikoláš, M., Janda, P., Frankovič, M., Rodrigo, R., Vostarek, O., Synek, M., & Svoboda, M. (2021). Disturbance history is a key driver of tree life span in temperate primary forests. Journal of Vegetation Science, 32(5), e13069.

Pettit, J. L., Pettit, J. M., Janda, P., Rydval, M., Čada, V., Schurman, J. S., Nagel, T. A., Bače, R., Saulnier, M., Hofmeister, J., Matula, R., Kozák, D., Frankovič, M., Turcu, D. O., Mikoláš, M., & Svoboda, M. (2021). Both cyclone-induced and convective storms drive disturbance patterns in European primary beech forests. Journal of Geophysical Research: Atmospheres, 126(7), e2020JD033929.

Puverel, C., Abourachid, A., Böhmer, C., Leban, J. M., Svoboda, M., & Paillet, Y. (2019). This is my spot: What are the characteristics of the trees excavated by the Black Woodpecker? A case study in two managed French forests. Forest Ecology and Management, 453, 117621.

Quinn, G., & Keough, M. (2002). Experimental design and data analysis for biologists. Cambridge University Press.

Ranius, T., Svensson, G. P., Berg, N., Niklasson, M., & Larsson, M. C. (2009). The successional change of hollow oaks affects their suitability for an inhabiting beetle, Osmoderma eremita. Annales Zoologici Fennici, 46(3), 205-216.

Ray-Mukherjee, J., Nimon, K., Mukherjee, S., Morris, D. W., Slotow, R., & Hamer, M. (2014). Using commonality analysis in multiple regressions: A tool to decompose regression effects in the face of multicollinearity. Methods in Ecology and Evolution, 5, 320-328.

R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing.

Regnery, B., Couvet, D., Kubarek, L., Julien, J. F., & Kerbiriou, C. (2013). Tree microhabitats as indicators of bird and bat communities in Mediterranean forests. Ecological Indicators, 34, 221-230.

Remm, J., & Lõhmus, A. (2011). Tree cavities in forests-The broad distribution pattern of a keystone structure for biodiversity. Forest Ecology and Management, 262(4), 579-585.

Sabatini, F. M., Burrascano, S., Keeton, W. S., Levers, C., Lindner, M., Pötzschner, F., Verkerk, J. P., Bauhus, J., Buchwald, E., Chaskovskyy, O., Debaive, N., Horváth, F., Garbarino, M., Grigoriadis, N., Lombardi, F., Duarte, I. M., Meyer, P., Midteng, R., Mikac, S., & Kuemmerle, T. (2018). Where are Europe's last primary forests? Diversity and Distributions, 24(10), 1426-1439.

Sabatini, F. M., Bluhm, H., Kun, Z., Aksenov, D., Atauri, J. A., Buchwald, E., Burrascano, S., Cateau, E., Diku, A., Duarte, I. M., López, A. B. F., Garbarino, M., Grigoriadis, N., Horváth, F., Keren, S., Kitenberga, M., Kiš, A., Kraut, A., Ibisch, P. L., … Kuemmerle, T. (2021). European primary forest database v2. 0. Scientific Data, 8(1), 1-14.

Seidl, R., & Turner, M. G. (2022). Post-disturbance reorganization of forest ecosystems in a changing world. Proceedings of the National Academy of Sciences, 119(28), e2202190119.

Senf, C., & Seidl, R. (2021). Mapping the forest disturbance regimes of Europe. Nature Sustainability, 4(1), 63-70.

Shmueli, G., Minka, T. P., Kadane, J. B., Borle, S., & Boatwright, P. (2005). A useful distribution for fitting discrete data: Revival of the Conway-Maxwell-Poisson distribution. Journal of the Royal Statistical Society: Series C (Applied Statistics), 54, 127-142.

Stokes, M. A., & Smiley, T. L. (1968). Tree-ring dating. University of Chicago Press.

Ulyshen, M. D., Ulyshen, M. D., & Koerner. (2018). Saproxylic insects. Springer.

van Pelt, R. (2007). Identifying mature and old forests in Western Washington. Washington State Department of Natural Resources.

Vasaitis, R. (2013). 10 Heart rots, sap rots and canker rots. Infectious forest diseases.

Veen, P., Fanta, J., Raev, I., Biriş, I. A., de Smidt, J., & Maes, B. (2010). Virgin forests in Romania and Bulgaria: Results of two national inventory projects and their implications for protection. Biodiversity and Conservation, 19(6), 1805-1819.

Vuidot, A., Paillet, Y., Archaux, F., & Gosselin, F. (2011). Influence of tree characteristics and forest management on tree microhabitats. Biological Conservation, 144, 441-450.

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

Winter, S., & Möller, G. C. (2008). Microhabitats in lowland beech forests as monitoring tool for nature conservation. Forest Ecology and Management, 255(3-4), 1251-1261.

Yamaguchi, D. K. (1991). A simple method for cross-dating increment cores from living trees. Canadian Journal of Forest Research, 21, 414-416.

Zheng, Z., Zhang, S., Baskin, C., Baskin, J., Schaefer, D., Yang, X., & Yang, L. (2016). Hollows in living trees develop slowly but considerably influence the estimate of forest biomass. Functional Ecology, 30, 830-838.