Land Use Change Consistently Reduces α- But Not β- and γ-Diversity of Bees

Land use change threatens global biodiversity and compromises ecosystem functions, including pollination and food production. Reduced taxonomic α-diversity is often reported under land use change, yet the impacts could be different at larger spatial scales (i.e., γ-diversity), either due to reduced β-diversity amplifying diversity loss or increased β-diversity dampening diversity loss. Additionally, studies often focus on taxonomic diversity, while other important biodiversity components, including phylogenetic diversity, can exhibit differential responses. Here, we evaluated how agricultural and urban land use alters the taxonomic and phylogenetic α-, β-, and γ-diversity of an important pollinator taxon-bees. Using a multicontinental dataset of 3117 bee assemblages from 157 studies, we found that taxonomic α-diversity was reduced by 16%-18% in both agricultural and urban habitats relative to natural habitats. Phylogenetic α-diversity was decreased by 11%-12% in agricultural and urban habitats. Compared with natural habitats, taxonomic and phylogenetic β-diversity increased by 11% and 6% in urban habitats, respectively, but exhibited no systematic change in agricultural habitats. We detected a 22% decline in taxonomic γ-diversity and a 17% decline in phylogenetic γ-diversity in agricultural habitats, but γ-diversity of urban habitats was not significantly different from natural habitats. These findings highlight the threat of agricultural expansions to large-scale bee diversity due to systematic γ-diversity decline. In addition, while both urbanization and agriculture lead to consistent declines in α-diversity, their impacts on β- or γ-diversity vary, highlighting the need to study the effects of land use change at multiple scales.

Toby P.N. Tsang was supported by the Hong Kong General Research Fund (17115119) and the University of Toronto Scarborough Postdoctoral Fellowship Program. The Hong Kong General Research Fund was awarded to Lauren C. Ponisio and Timothy C. Bonebrake. Lauren C. Ponisio was also funded by the NSF (Award ID: 2009075). A. A. Amado De Santis was partly supported by the National Research Council of Argentina (CONICET), SIGMA Xi Foundation, a PIUNT project from the National University of Tucumán, Argentina (UNT), and PUE 023 project from the National Research Council of Argentina (CONICET). Adrian González-Chaves was funded by a grant from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; Interface Project, No. 2013/23457-6). Alexandra-Maria Klein was supported by the German Science Foundation (DFG), Grant Number KL 1849/4-1, and the Alexander-von-Humboldt Foundation. Alyssa B. Stewart was partly supported by funding from Mahidol University (Strategic Research Fund) and the Thailand Research Fund (Grant MRG6080124). András Báldi was partly funded by the European Union's Horizon 2020 project “Safeguard” (Grant Agreement ID: 101003476). Andrea Holzschuh was supported by the European Union's Horizon 2020 project “Safeguard” (Grant Agreement No. 101003476) and the Federal Ministry of Food and Agriculture (BMEL) via the Federal Office for Agriculture and Food (BLE) (Grant No. 2821ABS002). Anson Main was supported by the Missouri Department of Conservation. Antonio Diego de Melo Bezerra was supported by CAPES (Coordination of Superior Level Staff Improvement). Annika Hass, Catrin Westphal, and Svenja Bänsch were supported by the LEGATO project that was funded by the BMBF (German Federal Ministry of Education and Research) Framework Programme Research for Sustainable Development (FONA, FKZ: 01LL0917A, 01LL0917D). Drissa Coulibaly and Katharina Stein were funded by the German Federal Ministry of Education and Research (BMBF) within the project WASCAL (West African Science Service Centre on Climate Change and Adapted Land Use). Svenja Bänsch was also supported by the DAAD (Germany Academic Exchange Service) scholarship. Benoît Geslin and Isabelle Dajoz were funded by the Region Ile-de-France through the DIM Astréa and the R2DS program. Blandina Felipe Viana and Juliana Hipólito were supported by the Brazilian National Council for Scientific and Technological Development (CNPq) through the following projects: codes INCT IN-TREE (465767/2014-1) and PVE—Science Without Borders (407152/2013-0); Juliana Hipólito was supported by CAPES scholarships; and Blandina Felipe Viana was supported by CNPq for the grant (PQ code: 305470/2013-2). Breno M. Freitas was funded by CNPq through the project code Universal 14/2011 (#473454/2011-4) and Breno M. Freitas was supported by a CNPq Research Grant (#302934/2010-3). Bruno Ferreira Marques was supported by CNPq for a Research Productivity Fellowship (#308358/2019-8). Luísa G. Carvalheiro was funded by CNPq (#307625/2021-4). Mariana Beal-Neves was supported by CAPES (Coordination of Superior Level Staff Improvement). Ana Carolina Pereira Machado was supported by CNPq (#141736/2020-8) and CAPES (#COOPBRASS: 88887.947041/2024-00). André Rodrigo Rech was supported by FAPEMIG (#APQ-00932-21, #APQ-03100-21, #APQ-01152-22, #APQ-01151-23, #APQ-03262-23, and #RED-00039-23), CNPq (#311665/2022-5 and #423939/2021-1), and CAPES (#88887.837988/2023-00 and #88887.368784/2019-00). Catalina Gutiérrez-Chacón was supported by the Colombian Department of Science, Technology and Innovation—Colciencias (call 529). Caleb Wilson and Mary A. Jamieson were supported by the Foundation for Food and Agricultural Research New Innovator Award (FFAR Award No. 430876) (https://foundationfar.org/) and the Oakland University Provost Graduate Student Research Award (Oakland.edu). David Kleijn and Jeroen Scheper were supported by the European Community's Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No 244090, STEP Project (Status and Trends of European Pollinators, www.step-project.net). Jeroen Scheper and David Kleijn were also supported by the Dutch Ministry of Economic Affairs (BO-11-011.01-011 and KB-14-003-006). Eileen F. Power and Jane C. Stout were supported by the Irish Department of Agriculture, Fisheries and Food Research Stimulus Fund (RSF), funded under the National Development Plan (2007–2013). Elsa Youngsteadt was supported by the USDA National Institute of Food and Agriculture Award Number 2020-67013-31916 and USDA National Institute of Food and Agriculture Hatch Project 1018689. Eunice Enríquez was supported by Organization for Women in Science for the Developing World (OWSD), and the Secretaria nacional de Ciencia y Tecnology del gobierno de Guatemala (SENACYT). Frédéric McCune and Valérie Fournier were funded by the Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grant Program and the Fonds de Recherche Nature et Technologies Québec (FRQNT). Gideon Pisanty and Yael Mandelik were partially funded by the Israel Ministry of Agriculture Research Grant No. 824-0112-08 and the Israel Science Foundation Research Grant No. 919/09. Jose L. Gonzalez-Andujar, Jordi Izquierdo, and Jane Morrison were supported by FEDER (European Regional Development Funds) and the Spanish Ministry of Economy and Competitiveness grants (Project Numbers AGL2012-33736 and AGL2015-64130-R). The Natural Sciences and Engineering Research Council of Canada (NSERC) provided Jane Morrison with a doctoral scholarship. Katherine J. Turo was supported by USDA-NIFA Postdoctoral Fellowship 2021-67012-35153 and the National Science Foundation, Grant/Award Numbers: CAREER 1253197 and DGE-1343012. Keng-Lou James Hung was supported by UC San Diego Academic Senate Bridge Fund Grant BIO088B, NSF Doctoral Dissertation Improvement Grant DEB-1501566, National Geographic Society Young Explorer Grant 9014-11, a Mildred E. Mathias Graduate Student Research Grant from the University of California Natural Reserve System, the Jeanne Marie Messier Memorial Endowed Fund, Sigma Xi Grant in Aid of Research G20111015158245, and NSF Biological Research Collection Grant DBI-0956388. Montserrat Plascencia, Robyn D. Quistberg, and Stacy Philpott were funded by the USDA National Institute of Food and Agriculture, Grant/Award Number: 2016-67019-25185, and USDA National Institute of Food and Agriculture, Grant/Award Number: 2016-67032-24987. Kristoffer Hylander and Ulrika Samnegård were supported by the Swedish research councils: The Swedish International Development Coordination Agency (SIDA) (SWE-2009-134, awarded to Kristoffer Hylander) and Formas (229-2009-991, awarded to Kristoffer Hylander). K. Ballare was supported in part by the Graduate Program in Ecology, Evolution and Behavior at The University of Texas at Austin, Texas Department of Parks and Wildlife, and the USDA Forest Service. Laura A. Burkle was supported by Washington University in St. Louis, Tyson Research Center, Montana State University, National Science Foundation (DEB 0934376, 20133168225, and 1256788), and Western Sustainable Agriculture Research and Education (SW13-043). Natalia Escobedo-Kenefic and Patricia Landaverde-González were supported by Dirección General de Investigación de la Universidad de San Carlos de Guatemala (Digi-USAC) through the research grant 4.8.63.2.272012. Natapot Warrit and Pakorn Nalinrachatakan were supported by BIFA: Biodiversity Fund for Asia (BIFA5_005 and BIFA6_009) via GBIF and the National Science and Technology Development Agency (NSTDA), Thailand. Pornpimon Tangtorwongsakul was funded by The National Science and Technology Development Agency (NSTDA) under the project “Effect of urbanisation on species richness and abundance of indicator species inhabiting Thailand's most important wetland.” Yunhui Liu was supported by the National Natural Science Foundation of China (No. 41871186). Yves Basset was funded by the Czech Science Foundation (GAČR 20-31295S). The Missouri Cooperative Fish and Wildlife Research Unit is jointly sponsored by the Missouri Department of Conservation, the University of Missouri, the US Fish and Wildlife Service, the US Geological Survey, and the Wildlife Management Institute. Use of trade, product, or firm names is for descriptive purposes only and does not imply US Government endorsement.

Peer reviewed