Latitudinal gradients of biodiversity and ecosystem services in protected and non-protected oak forest areas can inform climate smart conservation^✩

Abstract

Adaptive governance of areas set aside for future protection of biodiversity, sustainable production, and recreation requires knowledge about whether and how effects of area protection are modulated by climate change and redistribution of species. To investigate this, we compare biodiversity of plants (assessed using vegetation plots) and arthropods (collected with Malaise traps, analyzed using metabarcoding) and productivity (tree growth, determined using dendrochronology) in protected and non-protected oak (Quercus spp.) forests along a latitudinal gradient (55.6 °N – 60.8 °N) in Sweden. We also compare historical, recent and projected future climate in the region. In contrast to established global latitudinal diversity gradients, species richness of plants and arthropods increased northwards, possibly reflecting recent climate-induced community redistributions, but neither was higher in protected than in non-protected areas, nor associated with contemporary ground temperature. Species composition of arthropods also did not differ between protected and non-protected areas. Arthropod biomass increased with latitude, suggesting that the magnitude of cascading effects mediated via their roles as pollinators, herbivores, and prey for other trophic levels, varies geographically and will change with a moving climate. Annual growth rate of oaks (an ecosystem service in the form of biomass increase and carbon sequestration) was independent of latitude and did not differ between protected and non-protected areas. Our findings question the efficacy of contemporary designation and management of protected oak forests, and emphasize that development and implementation of modified climate smart conservation strategies is needed to safeguard ecosystem functioning, biodiversity, and recreational values of protected forest areas against future challenges.

Keywords

Biological diversity / Conservation biology / Decision making / Forest ecosystems / Global warming / Species-richness gradients

Declaration of competing interests

The authors declare that there are no known competing financial interests or personal relationships that influenced the work reported in this paper.

Credit authorship contribution statement

Anders Forsman: Conceptualization, Data curation, Methodology, Formal analysis, Writing – original draft, Writing – review & editing. Johanna Sunde: Conceptualization, Methodology, Writing – review & editing. Romana Salis: Conceptualization, Methodology, Formal analysis, Writing – review & editing. Markus Franzén: Conceptualization, Data curation, Methodology, Formal analysis - climate data, Writing – review & editing.

Acknowledgements

We express our profound gratitude to Jonas Lundqvist, Marcus Hall, Sara Forsman, and Nikolaj Gubonin for their invaluable contributions to the fieldwork and data collection, and to Johannes Edvardsson for his expert dendrochronological assessments of the oak stands. We are grateful to two anonymous reviewers for comments on the manuscript. This research was financially supported by The Swedish National Research Programme on Climate and Formas, under grant numbers Dnr. 2018-02846 and Dnr. 2021-02142, to M.F., A.F., and J.S., and by Linnaeus University, to A.F. and M.F. The funders had no role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.

References

[1] Abbott, R. E., Doak, D. F., DeMarche, M. L., 2017. Portfolio effects, climate change, and the persistence of small populations: analyses on the rare plant Saussurea weberi. Ecology 98(4), 1071-1081.

[2] Aerts, R, Honnay, O., 2011. Forest restoration, biodiversity and ecosystem functioning. BMC Ecol., 11(1), 29.

[3] Aerts, R, Honnay, O, Van Nieuwenhuyse, A., 2018. Biodiversity and human health: mechanisms and evidence of the positive health effects of diversity in nature and green spaces. Brit. Med. Bull., 127(1), 5-22.

[4] Anderson-Teixeira, K. J., Herrmann, V, Rollinson, C. R., Gonzalez, B, Gonzalez-Akre, E. B., Pederson, N, Alexander, M. R., Allen, C. D., Alfaro-Sánchez, R, Awada, T, Baltzer, J. L., Baker, P. J., Birch, J. D., Bunyavejchewin, S, Cherubini, P, Davies, S. J., Dow, C, Helcoski, R, Kašpar, J, Lutz, J. A., Margolis, E. Q., Maxwell, J. T., McMahon, S. M., Piponiot, C, Russo, S. E., Sniderhan, A. E., Tepley, A. J., Vašíčková, I, Vlam, M, Zuidema, P. A., 2022. Joint effects of climate, tree size, and year on annual tree growth derived from tree-ring records of ten globally distributed forests. Glob. Change Biol., 28(1), 245-266.

[5] Auffret, A. G, Svenning, J-.C., 2022. Climate warming has compounded plant responses to habitat conversion in northern Europe. Nat. Commun., 13(1), 7818.

[6] Bacon, S, Smith, A. F., Döringer, S, Bečka, P, Hußlein, M, Porst, F, Stemberg, J, Heurich, M., 2023. Visitors to national parks show positive attitudes towards recolonising wolves in the Bohemian Forest Ecosystem. Biol. Conserv., 288, 110349.

[7] Balmford, A., 2021. Concentrating vs. spreading our footprint: how to meet humanity's needs at least cost to nature. J. Zool., 315(2), 79-109.

[8] Baston, D., 2023. Package ‘exactextractr’. R Foundation for statistical computing.

[9] Belinchón, R, Martínez, I, Escudero, A, Aragón, G, Valladares, F., 2007. Edge effects on epiphytic communities in a Mediterranean Quercus pyrenaica forest. J. Veget. Sci., 18 (1), pp. 81-90

[10] Betzholtz, P-E, Forsman, A, Franzén, M., 2023. Increased abundance coincidences with range expansions and phenology shifts: a long-term case study of two Noctuid moths in Sweden. Diversity 15, 1177.

[11] Bitterlich, W., 1984. The relascope idea: relative measurements in forestry. Commonwealth Agricultural Bureaux, Farnham Royal

[12] Bräker, O. U., 2002. Measuring and data processing in tree-ring research – a methodological introduction. Dendrochr 20(1), 203-216.

[13] Brienen, R. J. W., Caldwell, L, Duchesne, L, Voelker, S, Barichivich, J, Baliva, M, Ceccantini, G, Di Filippo, A, Helama, S, Locosselli, G. M., Lopez, L, Piovesan, G, Schöngart, J, Villalba, R, Gloor, E., 2020. Forest carbon sink neutralized by pervasive growth-lifespan trade-offs. Nat. Commun., 11(1), 4241.

[14] Brown, M. B., Morrison, J. C., Schulz, T. T., Cross, M. S., Püschel-Hoeneisen, N, Suresh, V, Eguren, A., 2022. Using the conservation standards framework to address the effects of climate change on biodiversity and ecosystem services. Climate 10(2), 13.

[15] Buchner, D, T-Macher, H, Leese, F., 2022. APSCALE: advanced pipeline for simple yet comprehensive analyses of DNA metabarcoding data. Bioinformatics 38(20), 4817-4819.

[16] Butt, N, Chauvenet, A. L. M., Adams, V. M., Beger, M, Gallagher, R. V., Shanahan, D. F., Ward, M, Watson, J. E. M., Possingham, H. P., 2021. Importance of species translocations under rapid climate change. Conserv. Biol., 35(3), 775-783.

[17] Cannon, P. G., Gilroy, J. J., Tobias, J. A., Anderson, A, Haugaasen, T, Edwards, D. P., 2019. Land-sparing agriculture sustains higher levels of avian functional diversity than land sharing. Glob. Change Biol., 25(5), 1576-1590.

[18] Cook, E. R., Holmes, R. L., 1984. Program ARSTAN User Manual. Laboratory of Tree Ring Research. University of Arizona

[19] Creer, S, Deiner, K, Frey, S, Porazinska, D, Taberlet, P, Thomas, W. K., Potter, C, Bik, H. M., 2016. The ecologist's field guide to sequence-based identification of biodiversity. Methods Ecol. Evol., 7(9), 1008-1018.

[20] Cristescu, M. E., 2014. From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends Ecol. Evol., 29(10), 566-571.

[21] Dey, D. C., 2014. Sustaining oak forests in Eastern North America: regeneration and recruitment, the pillars of sustainability. For. Sci., 60(5), 926-942.

[22] Elbrecht, V, Braukmann, T, Ivanova, N, Prosser, S, Hajibabaei, M, Wright, M, Zakharov, E, Hebert, P, Steinke, D., 2019. Validation of COI metabarcoding primers for terrestrial arthropods. PeerJ 7, e7745.

[23] Forsman, A, Betzholtz, P. E., Franzén, M., 2016. Faster poleward range shifts in moths with more variable colour patterns. Sci. Rep., 6, 36265.

[24] Forster, E. J., Healey, J. R., Dymond, C, Styles, D., 2021. Commercial afforestation can deliver effective climate change mitigation under multiple decarbonisation pathways. Nat. Commun., 12(1), 3831.

[25] Fritts, H. C., 1976. Tree Rings and Climate. Academic Press, London

[26] Frøslev, T. G., Kjøller, R, Bruun, H. H., Ejrnæs, R, Brunbjerg, A. K., Pietroni, C, Hansen, A. J., 2017. Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nat. Commun., 8(1), 1188.

[27] Gamache, I, Payette, S., 2004. Height growth response of tree line black spruce to recent climate warming across the forest-tundra of eastern Canada. J. Ecol., 92(5), 835-845.

[28] GBIF.org, 2023. Global Biodiversity Information Facility (GBIF) Home Page (accessed 19 Decmber 2023).

[29] Giesecke, T., 2005. Holocene dynamics of the southern boreal forest in Sweden. Holocene 15(6), 858-872.

[30] Götmark, F., 2013. Habitat management alternatives for conservation forests in the temperate zone: review, synthesis, and implications. For. Ecol. Manage., 306, 292-307.

[31] Guo, F, Lenoir, J, Bonebrake, T. C., 2018. Land-use change interacts with climate to determine elevational species redistribution. Nat. Commun., 9(1), 1315.

[32] Hansen, L, Hoffman, J, Drews, C, Mielbrecht, E., 2010. Designing climate-smart conservation: guidance and case studies. Conserv. Biol., 24(1), 63-69.

[33] Hebert, P. D., Cywinska, A, Ball, S. L., DeWaard, J. R., 2003. Biological identifications through DNA barcodes. P. R. Soc. B: Biol. Sci., 270(1512), 313-321.

[34] Hijmans, R. J., Bivand, R, Pebesma, E, Sumner, M. D., 2023. Spatial Data Analysis R Package 'terra' version 1.7-55.

[35] Hillebrand, H., 2004. On the generality of the latitudinal diversity gradient. Am. Nat., 163(2), 192-211.

[36] Hoffmann, S, Irl, S. D. H., Beierkuhnlein, C., 2019. Predicted climate shifts within terrestrial protected areas worldwide. Nat. Commun., 10(1), 4787.

[37] Holmes, R. L., 1983. Computer-assisted quality control in tree-ring dating and measurement. Tree-ring Bull., 43, 69-78.

[38] Horváth, Z, Ptacnik, R, Vad, C. F., Chase, J. M., 2019. Habitat loss over six decades accelerates regional and local biodiversity loss via changing landscape connectance. Ecol. Lett., 22(6), 1019-1027.

[39] Hulshof, C. M., Swenson, N. G., Weiser, M. D., 2015. Tree height-diameter allometry across the United States. Ecol. Evol., 5(6), 1193-1204.

[40] IPCC, 2023. Summary for policymakers. In: Team, C.W., Lee, H., Romero, J. (Eds.), Climate Change 2023: Synthesis Report. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland, pp. 1–34.

[41] Janz, N, Nylin, S, Wahlberg, N., 2006. Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evol. Biol., 6, 4.

[42] Jetz, W, Fine, P. V. A., 2012. Global gradients in vertebrate diversity predicted by historical area-productivity dynamics and contemporary environment. PLoS Biol., 10(3), e1001292.

[43] Johnson, P. S., Shifley, S. R., Fogers, R, Dey, D. C., Kabrick, J. M., 2019. The Ecology and Silviculture of Oaks, 3rd ed. CAB International, Wallingford, Oxforshire, UK

[44] Johnson, S. E., Abrams, M. D., 2009. Age class, longevity and growth rate relationships: protracted growth increases in old trees in the eastern United States. Tree Physiol., 29(11), 1317-1328.

[45] Jonason, D, Franzén, M, Ranius, T., 2014. Surveying moths using light traps: effects of weather and time of year. PLoS One 9(3), e92453.

[46] Kindvall, O, Franzén, M, Askling, J, Forsman, A, Johansson, V., 2022. Subsidized common agricultural policy grazing jeopardizes the protection of biodiversity and Natura 2000 targeted species. Anim. Conserv., 25(5), 597-607.

[47] Kozák, D, Svitok, M, Zemlerová, V, Mikoláš, M, Lachat, T, Larrieu, L, Paillet, Y, Buechling, A, Bače, R, Keeton, W. S., Vítková, L, Begovič, K, Dušátko, M, Ferenčík, M, Frankovič, M, Gloor, R, Hofmeister, J, Janda, P, Kameniar, O, Kníř, T, Majdanová, L, Mejstřík, M, Pavlin, J, Ralhan, D, Rodrigo, R, C-Roibu, C, Synek, M, Vostarek, O, Svoboda, M., 2023. Importance of conserving large and old trees to continuity of tree-related microhabitats. Conserv. Biol., 37(3), e14066.

[48] Krsnik, G, Reynolds, K. M., Murphy, P, Paplanus, S, Garcia-Gonzalo, J, González Olabarria, J. R., 2023. Forest use suitability: towards decision-making-oriented sustainable management of forest ecosystem services. Geogr. Sustain., 4(4), 414-427.

[49] Lawrence, E. R., Fraser, D. J., 2020. Latitudinal biodiversity gradients at three levels: linking species richness, population richness and genetic diversity. Glob. Ecol. Biogeogr., 29(5), 770-788.

[50] Le Saout, S, Hoffmann, M, Shi, Y, Hughes, A, Bernard, C, Brooks, T. M., Bertzky, B, Butchart, S. H. M., Stuart, S. N., Badman, T, Rodrigues, A. S. L., 2013. Protected areas and effective biodiversity conservation. Science 342(6160), 803-805.

[51] Leray, M, Knowlton, N, Machida, R. J., 2022. MIDORI2: a collection of quality controlled, preformatted, and regularly updated reference databases for taxonomic assignment of eukaryotic mitochondrial sequences. Environ. DNA 4(4), 894-907.

[52] Lindbladh, M, Foster, D. R., 2010. Dynamics of long-lived foundation species: the history of Quercus in southern Scandinavia. J. Ecol., 98(6), 1330-1345.

[53] Löf, M, Brunet, J, Filyushkina, A, Lindbladh, M, Skovsgaard, J. P., Felton, A., 2016. Management of oak forests: striking a balance between timber production, biodiversity and cultural services. Int. J. Biodivers. Sci. Ecosyst. Serv. Manag., 12(1-2), 59-73.

[54] Luedtke, J. A., Chanson, J, Neam, K, Hobin, L, Maciel, A. O., Catenazzi, A, Borzée, A, Hamidy, A, Aowphol, A, Jean, A, Sosa-Bartuano, Á, Fong, G. A., de Silva, A, Fouquet, A, Angulo, A, Kidov, A. A., Muñoz Saravia, A, Diesmos, A. C., Tominaga, A, Shrestha, B, Gratwicke, B, Tjaturadi, B, Martínez Rivera, C. C., Vásquez Almazán, C. R., Señaris, C, Chandramouli, S. R., Strüssmann, C, Cortez Fernández, C. F., Azat, C, Hoskin, C. J., Hilton-Taylor, C, Whyte, D. L., Gower, D. J., Olson, D. H., Cisneros-Heredia, D. F., Santana, D. J., Nagombi, E, Najafi-Majd, E, Quah, E. S. H., Bolaños, F, Xie, F, Brusquetti, F, Andreone, F, Glaw, F, Castañeda, F. E., Kraus, F, Parra-Olea, G, Chaves, G, Medina-Rangel, G. F., González-Durán, G, Ortega-Andrade, H. M., Machado, I. F., Das, I, Dias, I. R., Urbina-Cardona, J. N., Crnobrnja-Isailović, J, J-Yang, H, Jiang, J. P., Wangyal, J. T., Rowley, J. J. L., Measey, J, Vasudevan, K, Chan, K. O., Gururaja, K. V., Ovaska, K, Warr, L. C., Canseco-Márquez, L, Toledo, L. F., Díaz, L. M., Khan, M. M. H., Meegaskumbura, M, Acevedo, M. E., Napoli, M. F., Ponce, M. A., Vaira, M, Lampo, M, Yánez-Muñoz, M. H., Scherz, M. D, Rödel, M-.O, Matsui, M, Fildor, M, Kusrini, M. D., Ahmed, M. F., Rais, M, Kouamé, N. G. G., García, N, Gonwouo, N. L., Burrowes, P. A., Imbun, P. Y., Wagner, P, Kok, P. J. R., Joglar, R. L., Auguste, R. J., Brandão, R. A., Ibáñez, R, von May, R, Hedges, S. B., Biju, S. D., Ganesh, S. R., Wren, S, Das, S, Flechas, S. V., Ashpole, S. L., Robleto-Hernández, S. J., Loader, S. P., Incháustegui, S. J., Garg, S, Phimmachak, S, Richards, S. J., Slimani, T, Osborne-Naikatini, T, Abreu-Jardim, T. P. F., Condez, T. H., De Carvalho, T. R., Cutajar, T. P., Pierson, T. W., Nguyen, T. Q., Kaya, U, Yuan, Z, Long, B, Langhammer, P, Stuart, S. N., 2023. Ongoing declines for the world's amphibians in the face of emerging threats. Nature 622(7982), 308-314.

[55] Mahmud, M, Maxwell, T. L., Cueff, S, Schroeder, R, Bazot, S, Delpierre, N, Marmagne, A, Vincent, G, Barthes, L., 2022. Recently absorbed nitrogen incorporates into new and old tissues: evidence from a ¹⁵N-labelling experiment in deciduous oaks. Plant Soil 480(1), 407-421.

[56] Mannion, P. D., Upchurch, P, Benson, R. B. J., Goswami, A., 2014. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol., 29(1), 42-50.

[57] Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J., 17, 10-12.

[58] Masson-Delmotte, V. P., Zhai, P, Pirani, S. L., Connors, C, Péan, S, Berger, N, Caud, Y, Chen, L, Goldfarb, M. I., Scheel Monteiro, P. M., 2021. Scheel Monteiro. IPCC, 2021:summary for policymakers. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change

[59] Maxwell, S. L., Fuller, R. A., Brooks, T. M., Watson, J. E. M., 2016. Biodiversity: the ravages of guns, nets and bulldozers. Nature 536(7615), 143-145.

[60] Meinshausen, M, Nicholls, Z. R. J., Lewis, J, Gidden, M. J., Vogel, E, Freund, M, Beyerle, U, Gessner, C, Nauels, A, Bauer, N, Canadell, J. G., Daniel, J. S., John, A, Krummel, P. B., Luderer, G, Meinshausen, N, Montzka, S. A., Rayner, P. J., Reimann, S, Smith, S. J., van den Berg, M, Velders, G. J. M., Vollmer, M. K., Wang, R. H. J., 2020. The shared socio-economic pathway (SSP) greenhouse gas concentrations and their extensions to 2500. Geosci. Model Dev., 13(8), 3571-3605.

[61] Methorst, J, Rehdanz, K, Mueller, T, Hansjürgens, B, Bonn, A, Böhning-Gaese, K., 2021. The importance of species diversity for human well-being in Europe. Ecol. Econ., 181, 106917.

[62] Morelli, T. L., Barrows, C. W., Ramirez, A. R., Cartwright, J. M., Ackerly, D. D., Eaves, T. D., Ebersole, J. L., Krawchuk, M. A., Letcher, B. H., Mahalovich, M. F., Meigs, G. W., Michalak, J. L., Millar, C. I., Quiñones, R. M., Stralberg, D, Thorne, J. H., 2020. Climate-change refugia: biodiversity in the slow lane. Front Ecol. Evol., 18(5), 228-234.

[63] MSB, 2023. Swedish Civil Contingencies Agency. Beredskap för värmebölja.

[64] Norman, J, Ellingson, L, Boman, M, Mattsson, L., 2010. The value of forests for outdoor recreation in southern Sweden: are broadleaved trees important. Ecol. Bull., 53, 21-32.

[65] O'Neill, B. C., Carter, T. R., Ebi, K, Harrison, P. A., Kemp-Benedict, E, Kok, K, Kriegler, E, Preston, B. L., Riahi, K, Sillmann, J, van Ruijven, B. J., van Vuuren, D, Carlisle, D, Conde, C, Fuglestvedt, J, Green, C, Hasegawa, T, Leininger, J, Monteith, S, Pichs-Madruga, R., 2020. Achievements and needs for the climate change scenario framework. Nat. Clim. Chang., 10(12), 1074-1084.

[66] Oksanen, J, Simpson, G. L., Blanchet, F. G., Kindt, R, Legendre, P, Minchin, P. R., O'Hara, R. B., Solymos, P, Stevens, M. H. H., Szoecs, E, Wagner, H, Barbour, M, Bedward, M, Bolker, B, Borcard, D, Carvalho, G, Chirico, M, Caceres, M. D., Durand, S, Weedon, J., 2022. vegan: Community Ecology Package (2.6-4)[Computer software].

[67] Pascual, U., 2022. Climate-smart conservation: an opportunity for transformative change in the mainstream conservation movement. One Earth 5(6), 609-611.

[68] Pecl, G. T., Araujo, M. B., Bell, J. D., Blanchard, J, Bonebrake, T. C., Chen, I. C., Clark, T. D., Colwell, R. K., Danielsen, F, Evengard, B, Falconi, L, Ferrier, S, Frusher, S, Garcia, R. A., Griffis, R. B., Hobday, A. J., Janion-Scheepers, C, Jarzyna, M. A., Jennings, S, Lenoir, J, Linnetved, H. I., Martin, V. Y., McCormack, P. C., McDonald, J, Mitchell, N. J., Mustonen, T, Pandolfi, J. M., Pettorelli, N, Popova, E, Robinson, S. A., Scheffers, B. R., Shaw, J. D., Sorte, C. J. B., Strugnell, J. M., Sunday, J. M., Tuanmu, M. N., Verges, A, Villanueva, C, Wernberg, T, Wapstra, E, Williams, S. E., 2017. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355(6332), eaai9214.

[69] Peng, L, Searchinger, T. D., Zionts, J, Waite, R., 2023. The carbon costs of global wood harvests. Nature 620(7972), 110-115.

[70] Phalan, B, Onial, M, Balmford, A, Green, R. E., 2011. Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333(6047), 1289-1291.

[71] Piovesan, G, Cannon, C. H., Liu, J, Munné-Bosch, S., 2022. Ancient trees: irreplaceable conservation resource for ecosystem restoration. Trends Ecol. Evol., 37(12), 1025-1028.

[72] Porfirio, L. L., Harris, R. M. B., Lefroy, E. C., Hugh, S, Gould, S. F., Lee, G, Bindoff, N. L., Mackey, B., 2014. Improving the use of species distribution models in conservation planning and management under climate change. PLoS One 9(11), e113749.

[73] Prentice, I. C., Sykes, M. T., Cramer, W., 1991. The possible dynamic response of northern forests to global warming. Glob. Ecol. Biogeogr. Lett., 1(5), 129-135.

[74] Radchuk, V, Reed, T, Teplitsky, C, van de Pol, M, Charmantier, A, Hassall, C, Adamík, P, Adriaensen, F, Ahola, M. P., Arcese, P, Miguel Avilés, J, Balbontin, J, Berg, K. S., Borras, A, Burthe, S, Clobert, J, Dehnhard, N, de Lope, F, Dhondt, A. A., Dingemanse, N. J., Doi, H, Eeva, T, Fickel, J, Filella, I, Fossøy, F, Goodenough, A. E., Hall, S. J. G., Hansson, B, Harris, M, Hasselquist, D, Hickler, T, Joshi, J, Kharouba, H, Martínez, J. G, Mihoub, J-.B, Mills, J. A., Molina-Morales, M, Moksnes, A, Ozgul, A, Parejo, D, Pilard, P, Poisbleau, M, Rousset, F, M-Rödel, O, Scott, D, Senar, J. C., Stefanescu, C, Stokke, B. G., Kusano, T, Tarka, M, Tarwater, C. E., Thonicke, K, Thorley, J, Wilting, A, Tryjanowski, P, Merilä, J, Sheldon, B. C., Pape Møller, A, Matthysen, E, Janzen, F, Dobson, F. S., Visser, M. E., Beissinger, S. R., Courtiol, A, Kramer-Schadt, S., 2019. Adaptive responses of animals to climate change are most likely insufficient. Nat. Commun., 10(1), 3109.

[75] Ranius, T, Jansson, N., 2000. The influence of forest regrowth, original canopy cover and tree size on saproxylic beetles associated with old oaks. Biol. Conserv., 95(1), 85-94.

[76] Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., Hirota, M. M., 2009. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv., 142(6), 1141-1153.

[77] Ribes, A, Qasmi, S, Gillett, N. P., 2021. Making climate projections conditional on historical observations. Sci. Adv., 7(4), eabc0671.

[78] Rinn, F., 2003. TSAP-Win^TM, software for tree-ring measurement, analysis and presentation. Rinntech, Heidelberg

[79] Roebroek, C. T. J., Duveiller, G, Seneviratne, S. I., Davin, E. L., Cescatti, A., 2023. Releasing global forests from human management: how much more carbon could be stored?. Science 380(6646), 749-753.

[80] Rushing, C. S., Royle, J. A., Ziolkowski, D. J., Pardieck, K. L., 2020. Migratory behavior and winter geography drive differential range shifts of eastern birds in response to recent climate change. Proc. Natl. Acad. Sci. U.S.A., 117(23), 12897-12903.

[81] Salis, R, Sunde, J, Gubonin, N, Franzén, M, Forsman, A., 2024. Performance of DNA barcoding, standard barcoding and morphological approaches in the identification of insect biodiversity. Mol. Ecol. Resour., 24, p. e14018.. doi: 10.1111/1755-0998.14018.

[82] Santangeli, A, Weigel, B, Antão, L. H., Kaarlejärvi, E, Hällfors, M, Lehikoinen, A, Lindén, A, Salemaa, M, Tonteri, T, Merilä, P, Vuorio, K, Ovaskainen, O, Vanhatalo, J, Roslin, T, Saastamoinen, M., 2023. Mixed effects of a national protected area network on terrestrial and freshwater biodiversity. Nat. Commun., 14(1), 5426.

[83] SCB, 2017. Statistics Sweden, Protected Nature 2016-12-31 MI 41 SM 1701 MI41 - Protected nature.

[84] SCB, 2023. Statistics Sweden, Protected Nature 2022-12-31 MI 41 2022A01, MI41 - Protected nature.

[85] Scheffers, B. R., De Meester, L, Bridge, T. C. L., Hoffmann, A. A., Pandolfi, J. M., Corlett, R. T., Butchart, S. H. M., Pearce-Kelly, P, Kovacs, K. M., Dudgeon, D, Pacifici, M, Rondinini, C, Foden, W. B., Martin, T. G., Mora, C, Bickford, D, Watson, J. E. M., 2016. The broad footprint of climate change from genes to biomes to people. Science 354(6313), aaf7671.

[86] Scheffers, B. R., Pecl, G., 2019. Persecuting, protecting or ignoring biodiversity under climate change. Nat. Clim. Chang., 9(8), 581-586.

[87] Schindler, D. E., Hilborn, R, Chasco, B, Boatright, C. P., Quinn, T. P., Rogers, L. A., Webster, M. S., 2010. Population diversity and the portfolio effect in an exploited species. Nature 465(7298), 609-612.

[88] Stein, B. A., Glick, P, Edelson, N, Staudt, A., 2014. Climate-smart conservation: putting adaption principles into practice. U.S. Climate Resilience Toolkit, National Wildlife Federation, Washington, D.C, p. 272

[89] Stephenson, N. L., Das, A. J., Condit, R, Russo, S. E., Baker, P. J., Beckman, N. G., Coomes, D. A., Lines, E. R., Morris, W. K., Rüger, N, Blundo, C, Bunyavejchewin, S, Chuyong, G, Davies, S. J, Duque, Á, Ewango, C. N., Flores, O, Franklin, J. F., Grau, H. R., Hao, Z, Harmon, M. E., Hubbell, S. P., Kenfack, D, Lin, Y, Makana, J. R., Malizia, A, Malizia, L. R., Pabst, R. J., Pongpattananurak, N, Su, S. H., Sun, I. F., Tan, S, Thomas, D, van Mantgem, P. J., Wang, X, Wiser, S. K., Zavala, M. A., 2014. Rate of tree carbon accumulation increases continuously with tree size. Nature 507(7490), 90-93.

[90] Suggitt, A. J., Wheatley, C. J., Aucott, P, Beale, C. M., Fox, R, Hill, J. K., Isaac, N. J. B., Martay, B, Southall, H, Thomas, C. D., Walker, K. J., Auffret, A. G., 2023. Linking climate warming and land conversion to species’ range changes across Great Britain. Nat. Commun., 14(1), 6759.

[91] Sunde, J, Franzén, M, P-Betzholtz, E, Francioli, Y, Pettersson, L. B., Pöyry, J, Ryrholm, N, Forsman, A., 2023. Century-long butterfly range expansions in northern Europe depend on climate, land use and species traits. Commun. Biol., 6, 601.

[92] Suzuki-Ohno, Y, Yokoyama, J, Nakashizuka, T, Kawata, M., 2020. Estimating possible bumblebee range shifts in response to climate and land cover changes. Sci. Rep., 10(1), 19622.

[93] SverigesRiksdag, 2022. The Swedish Code of Statutes, Land Code (SFS 1970:994).

[94] Taberlet, P, Coissac, E, Pompanon, F, Brochmann, C, Willerslev, E., 2012. Towards next-generation biodiversity assessment using DNA metabarcoding. Mol. Ecol., 21(8), 2045-2050.

[95] Tallamy, D. W., Shropshire, K. J., 2009. Ranking lepidopteran use of native versus introduced plants. Conserv. Biol., 23(4), 941-947.

[96] Tälle, M, Öckinger, E, Löfroth, T, Pettersson, L. B., Smith, H. G., Stjernman, M, Ranius, T., 2023. Land sharing complements land sparing in the conservation of disturbance-dependent species. Ambio 52(3), 571-584.

[97] Tebaldi, C, Debeire, K, Eyring, V, Fischer, E, Fyfe, J, Friedlingstein, P, Knutti, R, Lowe, J, O'Neill, B, Sanderson, B, van Vuuren, D, Riahi, K, Meinshausen, M, Nicholls, Z, Tokarska, K. B., Hurtt, G, Kriegler, E, Lamarque, J. F., Meehl, G, Moss, R, Bauer, S. E., Boucher, O, Brovkin, V, Byun, Y. H., Dix, M, Gualdi, S, Guo, H, John, J. G., Kharin, S, Kim, Y, Koshiro, T, Ma, L, Olivié, D, Panickal, S, Qiao, F, Rong, X, Rosenbloom, N, Schupfner, M, Séférian, R, Sellar, A, Semmler, T, Shi, X, Song, Z, Steger, C, Stouffer, R, Swart, N, Tachiiri, K, Tang, Q, Tatebe, H, Voldoire, A, Volodin, E, Wyser, K, Xin, X, Yang, S, Yu, Y, Ziehn, T., 2021. Climate model projections from the Scenario Model Intercomparison Project (ScenarioMIP) of CMIP6. Earth Syst. Dyn., 12(1), 253-293.

[98] Thomas, C. D., Cameron, A, Green, R. E., Bakkenes, M, Beaumont, L. J., Collingham, Y. C., Erasmus, B. F. N., de Siqueira, M. F., Grainger, A, Hannah, L, Hughes, L, Huntley, B, van Jaarsveld, A. S., Midgley, G. F., Miles, L, Ortega-Huerta, M. A., Townsend Peterson, A, Phillips, O. L., Williams, S. E., 2004. Extinction risk from climate change. Nature 427(6970), 145-148.

[99] Thomas, C. D., Gillingham, P. K., 2015. The performance of protected areas for biodiversity under climate change. Biol. J. Linn. Soc., 115(3), 718-730.

[100] Tompkins, E. L., Adger, W. N., 2004. Does adaptive management of natural resources enhance resilience to climate change?. Ecol. Soc., 9(2), 10.

[101] Twardek, W. M., Taylor, J. J., Rytwinski, T, Aitken, S. N., MacDonald, A. L., Van Bogaert, R, Cooke, S. J., 2023. The application of assisted migration as a climate change adaptation tactic: an evidence map and synthesis. Biol. Conserv., 280, 109932.

[102] UN_DESA, 2023. The Sustainable Development Goals Report 2023: Special Edition. UN DESA, New York.

[103] Vieira, S, Trumbore, S, Camargo, P. B., Selhorst, D, Chambers, J. Q., Higuchi, N, Martinelli, L. A., 2005. Slow growth rates of Amazonian trees: consequences for carbon cycling. Proc. Natl. Acad. Sci. U.S.A., 102(51), 18502-18507.

[104] Way, D. A., Oren, R., 2010. Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol., 30(6), 669-688.

[105] Whittaker, R. H., 1975. Communities and Ecosystems, 2nd ed. MacMillan, New York

[106] Williams, M. I., Dumroese, R. K., 2013. Preparing for climate change: forestry and assisted migration. J. For., 111(4), 287-297.

[107] Willig, M. R., Kaufman, D. M., Stevens, R. D., 2003. Latitudinal gradients of biodiversity: pattern, process, scale and synthesis. Annu. Rev. Ecol. Syst., 34, 273-309.

[108] Willig, M. R., Presely, S. J. 2018. Latitudinal gradients of biodiversity: theory and empirical patterns. DellaSala D.A., Goldstein M.I. (Eds.), The Encyclopedia of the Anthropocene, Elsevier, Oxford, pp.13-19.

[109] WorldData, 2023. The climate in Sweden.

[110] Zelinka, M. D., Myers, T. A., McCoy, D. T., Po-Chedley, S, Caldwell, P. M., Ceppi, P, Klein, S. A., Taylor, K. E., 2020. Causes of higher climate sensitivity in CMIP6 models. Geophys. Res. Lett., 47(1), e2019GL085782.