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    Data sharing practices and data availability upon request differ across scientific disciplines

    Our study uniquely points to differences among scientific disciplines in data availability as published along with the article and upon request from the authors. We demonstrate that in several disciplines such as forestry, materials for energy and catalysis and psychology, critical data are still unavailable for re-analysis or meta-analysis for more than half of the papers published in Nature and Science in the last decade. These overall figures roughly match those reported for other journals in various research fields8,11,13,22, but exceed the lowest reported values of around 10% available data13,23,24. Fortunately, data availability tends to improve, albeit slowly, in nearly all disciplines (Figs. 3, 7), which confirms recent implications from psychological and ecological journals13,31. Furthermore, the reverse trend we observed in microbiology corroborates the declining metagenomics sequence data availability22. Typically, such large DNA sequence data sets are used to publish tens of articles over many years by the teams producing these data; hence releasing both raw data and datasets may jeopardise their expectations of priority publishing. The weak discipline-specific differences among Nature and Science (Fig. 2) may be related to how certain subject editors implemented and enforced stringent data sharing policies.After rigorous attempts to contact the authors, data availability increased by one third on average across disciplines, with full and at least partial availability reaching 70% and 83%, respectively. These figures are in the top end of studies conducted thus far8,22 and indicate the relatively superior overall data availability in Science and Nature compared with other journals. However, the relative rates of data retrieval upon request, decline sharing data and ignoring the requests were on par with studies covering other journals and specific research fields10,12,25,26,28. Across 20 years, we identified the overall loss of data at an estimated rate of 3.5% and 5.9% for initially available data and data effectively available upon request, respectively. This rate of data decay is much less than 17% year−1 previously reported in plant and animal sciences based on a comparable approach24.While the majority of data are eventually available, it is alarming that less than a half of the data clearly stated to be available upon request could be effectively obtained from the authors. Although there may be objective reasons such as force majeure, these results suggest that many authors declaring data availability upon contacting may have abused the publishers’ or funders’ policy that allows statements of data availability upon request as the only means of data sharing. We find that this infringes research ethics and disables fair competition among research groups. Researchers hiding their own data may be in a power position compared with fair players in situations of big data analysis, when they can access all data (including their own), while others have more limited opportunities. Data sharing is also important for securing a possibility to re-analyse and re-interpret unexpected results9,32 and detect scientific misconduct25,33. More rigorous control of data release would prevent manuscripts with serious issues in sampling design or analytical procedures from being prepared, reviewed and eventually accepted for publication.Our study uniquely recorded the authors’ concerns and specific requests when negotiating data sharing. Concerns and hesitations about data sharing are understandable because of potential drawbacks and misunderstandings related to data interpretation and priority of publishing17,34 that may outweigh the benefits of recognition and passive participation in broader meta-studies. Nearly one quarter of researchers expressed various concerns or had specific requests depending on the discipline, especially about the specific objectives of our study. Previous studies with questionnaires about hypothetical data sharing unrelated to actual data sharing reveal that financial interests, priority of additional publishing and fear of challenging the interpretations after data re-analysis constitute the authors’ major concerns12,35,36. Another study indicated that two thirds of researchers sharing biomedical data expected to be invited as co-authors upon use of their data37 although this does not fulfil the authorship criteria6,38. At least partly related to these issues, the reasons for declining data sharing differed among disciplines: while social scientists usually referred to the loss of data, psychologists most commonly pointed out ethical/legal issues. Recently published data were, however, more commonly declined due to ethical/legal issues, which indicates rising concerns about data protection and potential misuse. Although we offered a possibility to share anonymised data sets, such trimmed data sets were never obtained from the authors, suggesting that ethical issues were not the only reason for data decline. Because research fields strongly differed in the frequency of no response to data requests, most unanswered requests can be considered declines that avoid official replies, which may harm the authors’ reputation.Because we did not sample randomly across journals, our interpretations are limited to the journals Nature and Science. Our study across disciplines did not account for the particular academic editor, which may have partly contributed to the differences among research fields and journals. Not all combinations of disciplines, journals and time periods received the intended 25 replicate articles because of the poor representation of certain research fields in the 2000–2009 period. This may have reduced our ability to detect statistically significant differences among the disciplines. We also obtained estimates for the final data availability for seven out of nine disciplines. Although we excluded the remaining two disciplines from comparisons of initial and final data availability, it may have slightly altered the overall estimates. The process of screening the potentially relevant articles chronologically backwards resulted in overrepresentation of more recent articles in certain relatively popular disciplines, which may have biased comparisons across disciplines. However, the paucity of residual year effect and year x discipline interaction in overall models and residual time effect in separate analyses within research fields indicate a minimal bias (Figure S1).We recorded the concerns and requests of authors that had issues with initial data sharing. Therefore, these responses may be relatively more sceptic than the opinions of the majority of the scientific community publishing in these journals. It is likely that the authors who did not respond may have concerns and reasons for declining similar to those who refused data sharing.Our experience shows that receiving data typically required long email exchanges with the authors, contacting other referred authors or sending a reminder. Obtaining data took on average 15 days, representing a substantial effort to both parties39. This could have been easily avoided by releasing data upon article acceptance. On the other hand, we received tips for analysis, caution against potential pitfalls and the authors’ informed consent upon contacting. According to our experience, more than two thirds of the authors need to be contacted for retrieving important metadata, variance estimates or specifying methods for meta-analyses40. Thus, contacting the authors may be commonly required to fill gaps in the data, but such extra specifications are easier to provide compared with searching and converting old datasets into a universally understandable format.Due to various concerns and tedious data re-formatting and uploading, the authors should be better motivated for data sharing41. Data formatting and releasing certainly benefits from clear instructions and support from funders, institutions and publishers. In certain cases, public recognition such as badges of open data for articles following the best data sharing practices and increasing numbers of citations may promote data release by an order of magnitude42. Citable data papers are certainly another way forward43,44, because these provide access to a well-organised dataset and add to the authors’ publication record. Encouraging enlisting published data sets with download and citation metrics in grant and job applications alongside with other bibliometric indicators should promote data sharing. Relating released data in publicly available research accounts such as ORCID, ResearcherID and Google Scholar would benefit both authors, other researchers and evaluators. To account for many authors’ fear of data theft17 and to prioritise the publishing options of data owners, setting a reasonable embargo period for third-party publishing may be needed in specific cases such as immediate data release following data generation45 and dissertations.All funders, research institutions, researchers, editors and publishers should collectively contribute to turn data sharing into a win-win situation for all parties and the scientific endeavour in general. Funding agencies may have a key role here due to the lack of conflicting interests and a possibility of exclusive allocation to depositing and publishing huge data files46. Funders have efficient enforcing mechanisms during reports periods, with an option to refuse extensions or approving forthcoming grant applications. We advocate that funders should include published data sets, if relevant, as an evaluation criterion besides other bibliometric information. Research institutions may follow the same principles when issuing institutional grants and employing research staff. Institutions should also insist their employees on following open data policies45.Academic publishers also have a major role in shaping data sharing policies. Although deposition and maintenance of data incur extra costs to commercial publishers, they should promote data deposition in their servers or public repositories. An option is to hire specific data editors for evaluating data availability in supplementary materials or online repositories and refusing final publishing before the data are fully available in a relevant format47. For efficient handling, clear instructions and a machine-readable data availability statement option (with a QR code or link to the data) should be provided. In non-open access journals, the data should be accessible free of charge or at reduced price to unsubscribed users. Creating specific data journals or ‘data paper’ formats may promote publishing and sharing data that would otherwise pile up in the drawer because of disappointing results or the lack of time for preparing a regular article. The leading scientometrics platforms Clarivate Analytics, Google Scholar and Scopus should index data journals equally with regular journals to motivate researchers publishing their data. There should be a possibility of article withdrawal by the publisher, if the data availability statements are incorrect or the data have been removed post-acceptance30. Much of the workload should stay on the editors who are paid by the supporting association, institution or publisher in most cases. The editors should grant the referees access to these data during the reviewing process48, requesting them a second opinion about data availability and reasons for declining to do so. Similar stringent data sharing policies are increasingly implemented by various journals26,30,47.In conclusion, data availability in top scientific journals differs strongly by discipline, but it is improving in most research fields. As our study exemplifies, the ‘data availability upon request’ model is insufficient to ensure access to datasets and other critical materials. Considering the overall data availability patterns, authors’ concerns and reasons for declining data sharing, we advocate that (a) data releasing costs ought to be covered by funders; (b) shared data and the associated bibliometric records should be included in the evaluation of job and grant applications; and (c) data sharing enforcement should be led by both funding agencies and academic publishers. More

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    Invasion dynamics of the European bumblebee Bombus terrestris in the southern part of South America

    1.Clavero, M. & Garcia-Berthou, E. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20, 110–110. https://doi.org/10.1016/j.tree.2005.01.003 (2005).Article 
    PubMed 

    Google Scholar 
    2.Grinnell, J. The niche-relationships of the California thrasher. Auk 34, 427–433 (1917).Article 

    Google Scholar 
    3.Elton, C. S. Animal Ecology and Evolution (Clarendon Press, 1930).
    Google Scholar 
    4.Arim, M., Abades, S. R., Neill, P. E., Lima, M. & Marquet, P. A. Spread dynamics of invasive species. Proc. Natl. Acad. Sci. U.S.A. 103, 374–378. https://doi.org/10.1073/pnas.0504272102 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    5.Kopf, R. K. et al. Confronting the risks of large-scale invasive species control. Nat. Ecol. Evol. 1, 0172. https://doi.org/10.1038/s41559-017-0172 (2017).Article 

    Google Scholar 
    6.Lonsdale, W. M. Global patterns of plant invasions and the concept of invasibility. Ecology 80, 1522–1536. https://doi.org/10.2307/176544 (1999).Article 

    Google Scholar 
    7.Pyšek, P. et al. MAcroecological framework for invasive aliens (MAFIA): Disentangling large-scale context dependence in biological invasions. Neobiota https://doi.org/10.3897/neobiota.62.52787 (2020).Article 

    Google Scholar 
    8.Donaldson, J. E. et al. Invasion trajectory of alien trees: the role of introduction pathway and planting history. Glob. Change Biol. 20, 1527–1537. https://doi.org/10.1111/gcb.12486 (2014).ADS 
    Article 

    Google Scholar 
    9.Sax, D. F. & Brown, J. H. The paradox of invasion. Glob. Ecol. Biogeogr. 9, 363–371. https://doi.org/10.1046/j.1365-2699.2000.00217.x (2000).Article 

    Google Scholar 
    10.Valido, A., Rodriguez-Rodriguez, M. C. & Jordano, P. Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci. Rep. 9, a4711. https://doi.org/10.1038/s41598-019-41271-5 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    11.Morales, C. L. & Aizen, M. A. Invasive mutualisms and the structure of plant–pollinator interactions in the temperate forests of north-west Patagonia, Argentina. J. Ecol. 94, 171–180. https://doi.org/10.1111/j.1365-2745.2005.01069.x (2006).Article 

    Google Scholar 
    12.Richardson, D. M., Allsopp, N., D’Antonio, C. M., Milton, S. J. & Rejmanek, M. Plant invasions—The role of mutualisms. Biol. Rev. 75, 65–93. https://doi.org/10.1017/S0006323199005435 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Simberloff, D. & Von Holle, B. Positive interactions of nonindigenous species: Invasional meltdown?. Biol. Invasions 1, 21–32. https://doi.org/10.1023/A:1010086329619 (1999).Article 

    Google Scholar 
    14.Vazquez, D. P. & Aizen, M. A. Asymmetric specialization: A pervasive feature of plant-pollinator interactions. Ecology 85, 1251–1257. https://doi.org/10.1890/03-3112 (2004).Article 

    Google Scholar 
    15.Shigesada, N. & Kawasaki, K. Biological Invasions: Theory and Practice (Oxford University Press, 1997).
    Google Scholar 
    16.Liebhold, A. M., Keitt, T. H., Goel, N. & Bertelsmeier, C. Scale invariance in the spatial-dynamics of biological invasions. Neobiota https://doi.org/10.3897/neobiota.62.53213 (2020).Article 

    Google Scholar 
    17.Mainali, K. P. et al. Projecting future expansion of invasive species: Comparing and improving methodologies for species distribution modeling. Glob. Change Biol. 21, 4464–4480. https://doi.org/10.1111/gcb.13038 (2015).ADS 
    Article 

    Google Scholar 
    18.Barbet-Massin, M., Rome, Q., Villemant, C. & Courchamp, F. Can species distribution models really predict the expansion of invasive species?. PLoS ONE 13, e0193085. https://doi.org/10.1371/journal.pone.0193085 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Dafni, A., Kevan, P., Gross, C. L. & Goka, K. Bombus terrestris, pollinator, invasive and pest: An assessment of problems associated with its widespread introductions for commercial purposes. Appl. Entomol. Zool. 45, 101–113. https://doi.org/10.1303/aez.2010.101 (2010).Article 

    Google Scholar 
    20.Velthuis, H. H. W. & van Doorn, A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37, 421–451. https://doi.org/10.1051/apido:2006019 (2006).Article 

    Google Scholar 
    21.Medel, R., González-Browne, C., Salazar, D. A., Ferrer, P. & Ehrenfeld, M. The most effective pollinator principle applies to new invasive pollinators. Biol. Lett. https://doi.org/10.1098/rsbl.2018.0132 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Smith-Ramirez, C. et al. The reasons why Chile should stop importing commercial bumblebee Bombus terrestris (Linnaeus) and to start controlling it. Gayana 82, 118–127. https://doi.org/10.4067/S0717-65382018000200118 (2018).Article 

    Google Scholar 
    23.Aizen, M. A. et al. Coordinated species importation policies are needed to reduce serious invasions globally: The case of alien bumblebees in South America. J. Appl. Ecol. 56, 100–106. https://doi.org/10.1111/1365-2664.13121 (2019).Article 

    Google Scholar 
    24.Acosta, A. L., Giannini, T. C., Imperatriz-Fonseca, V. L. & Saraiva, A. M. Worldwide alien invasion: A methodological approach to forecast the potential spread of a highly invasive pollinator. PLoS ONE 11, e0148295. https://doi.org/10.1371/journal.pone.0148295 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Geslin, B. & Morales, C. L. New records reveal rapid geographic expansion of Bombus terrestris Linnaeus, 1758 (Hymenoptera: Apidae), an invasive species in Argentina. CheckList 11, a1620. https://doi.org/10.15560/11.3.1620 (2015).Article 

    Google Scholar 
    26.Montalva, J., Sepulveda, V., Vivallo, F. & Silva, D. P. New records of an invasive bumble bee in northern Chile: Expansion of its range or new introduction events?. J. Insect Conserv. 21, 657–666. https://doi.org/10.1007/s10841-017-0008-x (2017).Article 

    Google Scholar 
    27.González-Varo, J. P. et al. Combined effects of global change pressures on animal-mediated pollination. Trends Ecol. Evol. 28, 524–530. https://doi.org/10.1016/j.tree.2013.05.008 (2013).Article 
    PubMed 

    Google Scholar 
    28.Knapp, J. L., Becher, M. A., Rankin, C. C., Twiston-Davies, G. & Osborne, J. L. Bombus terrestris in a mass-flowering pollinator-dependent crop: A mutualistic relationship?. Ecol. Evol. 9, 609–618. https://doi.org/10.1002/ece3.4784 (2019).Article 
    PubMed 

    Google Scholar 
    29.Nilsen, E. B., Pedersen, S. & Linnell, J. D. C. Can minimum convex polygon home ranges be used to draw biologically meaningful conclusions?. Ecol. Res. 23, 635–639. https://doi.org/10.1007/s11284-007-0421-9 (2008).Article 

    Google Scholar 
    30.Kadoya, T. & Washitani, I. Predicting the rate of range expansion of an invasive alien bumblebee (Bombus terrestris) using a stochastic spatio-temporal model. Biol. Conserv. 143, 1228–1235. https://doi.org/10.1016/j.biocon.2010.02.030 (2010).Article 

    Google Scholar 
    31.Kadoya, T., Ishii, H. S., Kikuchi, R., Suda, S. & Washitani, I. Using monitoring data gathered by volunteers to predict the potential distribution of the invasive alien bumblebee Bombus terrestris. Biol. Conserv. 142, 1011–1017. https://doi.org/10.1016/j.biocon.2009.01.012 (2009).Article 

    Google Scholar 
    32.Murúa, M., Espindola, A., González, A. & Medel, R. Pollinators and crossability as reproductive isolation barriers in two sympatric oil-rewarding Calceolaria (Calceolariaceae) species. Evol. Ecol. 31, 421–434. https://doi.org/10.1007/s10682-017-9894-3 (2017).Article 

    Google Scholar 
    33.Valdivia, C. E., Carroza, J. P. & Orellana, J. I. Geographic distribution and trait-mediated causes of nectar robbing by the European bumblebee Bombus terrestris on the Patagonian shrub Fuchsia magellanica. Flora 225, 30–36. https://doi.org/10.1016/j.flora.2016.09.010 (2016).Article 

    Google Scholar 
    34.Herbertsson, L. et al. Long-term data shows increasing dominance of Bombus terrestris with climate warming. Basic Appl. Ecol. 53, 116–123. https://doi.org/10.1016/j.baae.2021.03.008 (2021).Article 

    Google Scholar 
    35.Aizen, M. A. et al. When mutualism goes bad: Density-dependent impacts of introduced bees on plant reproduction. New Phytol. 204, 322–328. https://doi.org/10.1111/nph.12924 (2014).Article 

    Google Scholar 
    36.Esterio, G. et al. Assessing the impact of the invasive buff-tailed bumblebee (Bombus terrestris) on the pollination of the native Chilean herb Mimulus luteus. Arthropod-Plant Interact. 7, 467–474. https://doi.org/10.1007/s11829-013-9264-1 (2013).Article 

    Google Scholar 
    37.Morales, C. L., Arbetman, M. P., Cameron, S. A. & Aizen, M. A. Rapid ecological replacement of a native bumble bee by invasive species. Front. Ecol. Environ. 11, 529–534. https://doi.org/10.1890/120321 (2013).Article 

    Google Scholar 
    38.Plischuk, S., Antunez, K., Haramboure, M., Minardi, G. M. & Lange, C. E. Long-term prevalence of the protists Crithidia bombi and Apicystis bombi and detection of the microsporidium Nosema bombi in invasive bumble bees. Environ. Microbiol. Rep. 9, 169–173. https://doi.org/10.1111/1758-2229.12520 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Plischuk, S. & Lange, C. E. Invasive Bombus terrestris (Hymenoptera: Apidae) parasitized by a flagellate (Euglenozoa: Kinetoplastea) and a neogregarine (Apicomplexa: Neogregarinorida). J. Invertebr. Pathol. 102, 261–263. https://doi.org/10.1016/j.jip.2009.08.005 (2009).Article 

    Google Scholar 
    40.Plischuk, S., Meeus, I., Smagghe, G. & Lange, C. E. Apicystis bombi (Apicomplexa: Neogregarinorida) parasitizing Apis mellifera and Bombus terrestris (Hymenoptera: Apidae) in Argentina. Environ. Microbiol. Rep. 3, 565–568. https://doi.org/10.1111/j.1758-2229.2011.00261.x (2011).Article 
    PubMed 

    Google Scholar 
    41.Ruz, L. & Herrera, R. Preliminary observations on foraging activities of Bombus dahlbomii and Bombus terrestris (Hymenoptera: Apidae) on native and non-native vegetation in Chile. Acta Hortic. 561, 165–169. https://doi.org/10.17660/ActaHortic.2001.561.24 (2000).Article 

    Google Scholar 
    42.Sáez, A., Morales, C. L., Garibaldi, L. A. & Aizen, M. A. Invasive bumble bees reduce nectar availability for honey bees by robbing raspberry flower buds. Basic Appl. Ecol. 19, 26–35. https://doi.org/10.1016/j.baae.2017.01.001 (2017).Article 

    Google Scholar 
    43.Sáez, A., Morales, J. M., Morales, C. L., Harder, L. D. & Aizen, M. A. The costs and benefits of pollinator dependence: Empirically based simulations predict raspberry fruit quality. Ecol. Appl. 28, 1215–1222. https://doi.org/10.1002/eap.1720 (2018).Article 
    PubMed 

    Google Scholar 
    44.Schmid-Hempel, R. et al. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83, 823–837. https://doi.org/10.1111/1365-2656.12185 (2014).Article 
    PubMed 

    Google Scholar 
    45.Torretta, J. P., Medan, D. & Arahamovich, A. H. First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina. Trans. Am. Entomol. Soc. 132, 285–289 (2006).Article 

    Google Scholar 
    46.Arismendi, N., Bruna, A., Zapata, N. & Vargas, M. Molecular detection of the tracheal mite Locustacarus buchneri in native and non-native bumble bees in Chile. Insect Soc 63, 629–633. https://doi.org/10.1007/s00040-016-0502-2 (2016).Article 

    Google Scholar 
    47.Polidori, C. & Nieves-Aldrey, J. Comparative flight morphology in queens of invasive and native Patagonian bumblebees (Hymenoptera: Bombus). Crit. Biol. 338, 126–133. https://doi.org/10.1016/j.crvi.2014.11.001 (2015).Article 

    Google Scholar 
    48.Vieli, L., Davis, F. W., Kendall, B. E. & Altieri, M. Landscape effects on wild Bombus terrestris (Hymenoptera: Apidae) queens visiting highbush blueberry fields in south-central Chile. Apidologie 47, 711–716. https://doi.org/10.1007/s13592-015-0422-6 (2016).Article 

    Google Scholar 
    49.Sáez, A., Morales, C. L., Ramos, L. Y. & Aizen, M. A. Extremely frequent bee visits increase pollen deposition but reduce drupelet set in raspberry. J. Appl. Ecol. 51, 1603–1612. https://doi.org/10.1111/1365-2664.12325 (2014).Article 

    Google Scholar 
    50.Montalva, J., Dudley, L., Arroyo, M. K., Retamales, H. & Abrahamovich, A. H. Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.) in Chile. J. Apicult Res. 50, 11–21. https://doi.org/10.3896/Ibra.1.50.1.02 (2011).Article 

    Google Scholar 
    51.GBIF.org. GBIF Occurrence Download (April 15, 2020). https://doi.org/10.15468/dl.f15467jezh.52.R: A Language and Environment for Statistical Computing, Version 3.6.3 (Foundation for Statistical Computing, 2020). More

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    Geodiversity impacts plant community structure in a semi-arid region

    1.Gray, M., Gordon, J. & Brown, E. Geodiversity and the ecosystem approach: The contribution of geoscience in delivering integrated environmental management. Proc. Geol. Assoc. 124, 659–673 (2013).Article 

    Google Scholar 
    2.Gray, M. Valuing geodiversity in an ‘ecosystem services’ context. Scott. Geogr. J. 128, 177–194 (2012).Article 

    Google Scholar 
    3.Warren, A. & French, J. R. Habitat Conservation: Managing the Physical Environment (Wiley, Hoboken, 2001).
    Google Scholar 
    4.Gordon, J. E., Barron, H. F., Hansom, J. D. & Thomas, M. F. Engaging with geodiversity—Why it matters. Proc. Geol. Assoc. 123, 1–6 (2012).Article 

    Google Scholar 
    5.Hjort, J., Gordon, J. E., Gray, M. & Hunter, M. L. Why geodiversity matters in valuing nature’s stage. Conserv. Biol. 29, 630–639 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Gray, M. Geodiversity: Valuing and Conserving Abiotic Nature 448 (Wiley, 2004).
    Google Scholar 
    7.Serrano, E. & Ruiz-Flano, P. Geodiversity. A theoretical and applied concept. Geogr. Helv. Jg 62, 140–147 (2007).Article 

    Google Scholar 
    8.Comer, P. J. et al. Incorporating geodiversity into conservation decisions. Conserv. Biol. 29, 692–701 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Pătru-Stupariu, I. et al. Integrating geo-biodiversity features in the analysis of landscape patterns. Ecol. Indic. 80, 363–375 (2017).Article 

    Google Scholar 
    10.Chakraborty, A. & Gray, M. A call for mainstreaming geodiversity in nature conservation research and praxis. J. Nat. Conserv. 56, 125862 (2020).Article 

    Google Scholar 
    11.Poesen, J., Torri, D. & Bunte, K. Effects of rock fragments on soil erosion by water at different spatial scales: A review. CATENA 23, 141–166 (1994).Article 

    Google Scholar 
    12.Zhang, Y., Zhang, M., Niu, J., Li, H. & Xiao, R. Rock fragments and soil hydrological processes: Significance and progress. CATENA 147, 153–166 (2016).Article 

    Google Scholar 
    13.Xia, L. et al. Effects of rock fragment cover on hydrological processes under rainfall simulation in a semi-arid region of China. Hydrol. Process. 32, 792–804 (2018).ADS 
    Article 

    Google Scholar 
    14.Lavee, H. & Poesen, J. W. A. Overland flow generation and continuity on stone-covered soil surfaces. Hydrol. Process. 5, 345–360 (1991).ADS 
    Article 

    Google Scholar 
    15.Agassi, M. & Levy, G. Stone cover and rain intensity—Effects on infiltration, erosion and water splash. Soil Res. 29, 565–575 (1991).Article 

    Google Scholar 
    16.Mandal, U. K. et al. Soil infiltration, runoff and sediment yield from a shallow soil with varied stone cover and intensity of rain. Eur. J. Soil Sci. 56, 435–443 (2005).Article 

    Google Scholar 
    17.Cerdà, A. Effects of rock fragment cover on soil infiltration, interrill runoff and erosion. Eur. J. Soil Sci. 52, 59–68 (2001).Article 

    Google Scholar 
    18.Jury, W. A. & Bellantuoni, B. Heat and water movement under surface rocks in a field soil: I. Thermal effects. Soil Sci. Soc. Am. J. 40, 505–509 (1976).ADS 
    Article 

    Google Scholar 
    19.Yuan, C., Lei, T., Mao, L., Liu, H. & Wu, Y. Catena soil surface evaporation processes under mulches of different sized gravel. CATENA 78, 117–121 (2009).CAS 
    Article 

    Google Scholar 
    20.Poesen, J. & Lavee, H. Rock fragments in top soils: Significance and processes. CATENA 23, 1–28 (1994).Article 

    Google Scholar 
    21.Yizhaq, H., Stavi, I., Shachak, M. & Bel, G. Geodiversity increases ecosystem durability to prolonged droughts. Ecol. Complex. 31, 96–103 (2017).Article 

    Google Scholar 
    22.Stavi, I., Rachmilevitch, S. & Yizhaq, H. Geodiversity effects on soil quality and geo-ecosystem functioning in drylands. CATENA 176, 372–380 (2019).CAS 
    Article 

    Google Scholar 
    23.Preisler, Y. et al. Mortality versus survival in drought-affected Aleppo pine forest depends on the extent of rock cover and soil stoniness. Funct. Ecol. 33, 901–912 (2019).Article 

    Google Scholar 
    24.Sauer, T. J. & Logsdon, S. D. Hydraulic and Physical Properties of Stony Soils in a Small Watershed. Soil Sci. Soc. Am. J. 66, 1947–1956 (2002).25.Arnau-Rosalén, E., Calvo-Cases, A., Boix-Fayos, C., Lavee, H. & Sarah, P. Analysis of soil surface component patterns affecting runoff generation. An example of methods applied to Mediterranean hillslopes in Alicante (Spain). Geomorphology 101, 595–606 (2008).ADS 
    Article 

    Google Scholar 
    26.Ceacero, C. J., Díaz-Hernández, J. L., de Campo, A. D. & Navarro-Cerrillo, R. M. Soil rock fragment is stronger driver of spatio-temporal soil water dynamics and efficiency of water use than cultural management in holm oak plantations. Soil Tillage Res. 197, 104495 (2020).Article 

    Google Scholar 
    27.Burnett, M. R., August, P. V., Brown, J. H. & Killingbeck, K. T. The influence of geomorphological heterogeneity on biodiversity I. A patch-scale perspective. Conserv. Biol. 12, 363–370 (2008).Article 

    Google Scholar 
    28.Engelbrecht, B. et al. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80–82 (2007).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Stavi, I., Rachmilevitch, S. & Yizhaq, H. Small-scale geodiversity regulates functioning, connectivity, and productivity of shrubby, semi-arid rangelands. L. Degrad. Dev. 29, 205–209 (2018).Article 

    Google Scholar 
    30.Dubinin, V., Stavi, I., Svoray, T., Dorman, M. & Yizhaq, H. Hillslope geodiversity improves the resistance of shrubs to prolonged droughts in semiarid ecosystems. J. Arid Environ. 188, 104462 (2021).ADS 
    Article 

    Google Scholar 
    31.Ochoa-Hueso, R. et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J. Ecol. 106, 242–253 (2018).CAS 
    Article 

    Google Scholar 
    32.Stavi, I., Rachmilevitch, S., Hjazin, A. & Yizhaq, H. Geodiversity decreases shrub mortality and increases ecosystem tolerance to droughts and climate change. Earth Surf. Process. Landforms 43, 2808–2817 (2018).ADS 
    Article 

    Google Scholar 
    33.Suggitt, A. J. et al. Extinction risk from climate change is reduced by microclimatic buffering. Nat. Clim. Change 8, 713–717 (2018).ADS 
    Article 

    Google Scholar 
    34.Bailey, J. J., Boyd, D. S. & Field, R. Models of upland species’ distributions are improved by accounting for geodiversity. Landscape Ecol. https://doi.org/10.1007/s10980-018-0723-z (2018).Article 

    Google Scholar 
    35.Lenoir, J. et al. Local temperatures inferred from plant communities suggest strong spatial buffering of climate warming across Northern Europe. Glob. Change Biol. 19, 1470–1481 (2013).ADS 
    Article 

    Google Scholar 
    36.Lawler, J. J. et al. The theory behind, and the challenges of, conserving nature’s stage in a time of rapid change. Conserv. Biol. 29, 618–629 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Nichols, W. F., Killingbeck, K. T. & August, P. V. The influence biodiversity of geomorphological heterogeneity: II. A landscape perspective. Soc. Conserv. Biol. 12, 371–397 (1998).Article 

    Google Scholar 
    38.Alahuhta, J., Toivanen, M. & Hjort, J. Geodiversity–biodiversity relationship needs more empirical evidence. Nat. Ecol. Evol. 4, 2–3 (2020).PubMed 
    Article 

    Google Scholar 
    39.Evenari, M., Shanan, L., Tadmor, N. & Shkolnik, A. The Negev: The Challenge of a Desert (Harvard University Press, 1982).Book 

    Google Scholar 
    40.Akttani, H., Trimborn, P. & Ziegler, H. Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst. Evol. 206, 187–221 (1997).Article 

    Google Scholar 
    41.Harley, J. The Biology of Mycorrhiza (Leonard Hill, 1969).
    Google Scholar 
    42.Mejsti, V. K. & Cudlin, P. Mycorrhiza in some plant desert species in Algeria. Plant Soil 71, 363–366 (1983).Article 

    Google Scholar 
    43.Segoli, M., Ungar, E. D. & Shachak, M. Shrubs enhance resilience of a semi-arid ecosystem by engineering and regrowth. Ecohydrology 1, 330–339 (2008).Article 

    Google Scholar 
    44.Gilad, E., Von Hardenberg, J., Provenzale, A., Shachak, M. & Meron, E. Ecosystem engineers: From pattern formation to habitat creation. Phys. Rev. Lett. 93, 098105 (2004).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Wright, J. P., Jones, C. G., Boeken, B. & Shachak, M. Predictability of ecosystem engineering effects on species richness across environmental variability and spatial scales. J. Ecol. 94, 815–824 (2006).Article 

    Google Scholar 
    46.Katra, I., Blumberg, D. G., Lavee, H. & Sarah, P. Spatial distribution dynamics of topsoil moisture in shrub microenvironment after rain events in arid and semi-arid areas by means of high-resolution maps. Geomorphology 86, 455–464 (2007).ADS 
    Article 

    Google Scholar 
    47.Hoffman, O., de Falco, N., Yizhaq, H. & Boeken, B. Annual plant diversity decreases across scales following widespread ecosystem engineer shrub mortality. J. Veg. Sci. 27, 578–586 (2016).Article 

    Google Scholar 
    48.Shachak, M. et al. Woody species as landscape modulators and their effect on biodiversity patterns. Bioscience 58, 209–221 (2008).Article 

    Google Scholar 
    49.Madrigal-González, J., García-Rodríguez, J. A. & Alarcos-Izquierdo, G. Testing general predictions of the stress gradient hypothesis under high inter- and intra-specific nurse shrub variability along a climatic gradient. J. Veg. Sci. 23, 52–61 (2012).Article 

    Google Scholar 
    50.Boeken, B. & Shachak, M. The dynamics of abundance and incidence of annual plant species during colonization in a desert. Ecography (Cop.) 21, 63–73 (1998).Article 

    Google Scholar 
    51.Golodets, C. & Boeken, B. Moderate sheep grazing in semiarid shrubland alters small-scale soil surface structure and patch properties. CATENA 65, 285–291 (2006).Article 

    Google Scholar 
    52.Boeken, B. & Shachak, M. Desert plant communities in human-made patches-implications for management. Ecol. Appl. 4, 702–716 (1994).Article 

    Google Scholar 
    53.Hoffman, O., Yizhaq, H. & Boeken, B. Small-scale effects of annual and woody vegetation on sediment displacement under field conditions. CATENA 109, 157–163 (2013).Article 

    Google Scholar 
    54.Zaady, E., Arbel, S., Barkai, D. & Sarig, S. Long-term impact of agricultural practices on biological soil crusts and their hydrological processes in a semiarid landscape. J. Arid Environ. 90, 5–11 (2013).ADS 
    Article 

    Google Scholar 
    55.Zaady, E., Stavi, I. & Yizhaq, H. Hillslope geodiversity effects on properties and composition of biological soil crusts in drylands. Eur. J. Soil Sci. https://doi.org/10.1111/ejss.13097 (2021).Article 

    Google Scholar 
    56.Feinbrun-Dothan, N. & Danin, A. Analytical Flora of Eretz-Israel (Cana Publishing Ltd, 1991).
    Google Scholar 
    57.Solovchenko, A., Merzlyak, M. N., Khozin-Goldberg, I., Cohen, Z. & Boussiba, S. Coordinated carotenoid and lipid syntheses induced in parietochloris incisa (chlorophyta, trebouxiophyceae) mutant deficient in δ5 desaturase by nitrogen starvation and high light. J. Phycol. 46, 763–772 (2010).CAS 
    Article 

    Google Scholar 
    58.Shannon, C. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    59.Simpson, E. Measurement of diversity. Nature 163, 688 (1949).ADS 
    MATH 
    Article 

    Google Scholar 
    60.R Core Team. R: A language and environment for statistical Computing. R Foundation for Statistical  Computing, Vienna, Austria (2020).61.Richerson, P. J. & Lum, K. Patterns of plant species diversity in California: Relation to weather and topography. Am. Nat. 116, 504–536 (1980).Article 

    Google Scholar 
    62.Kerr, J. T. & Packer, L. Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature 385, 252–254 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    63.Alahuhta, J. et al. The role of geodiversity in providing ecosystem services at broad scales. Ecol. Indic. 91, 47–56 (2018).Article 

    Google Scholar 
    64.Zarnetske, P. L. et al. Towards connecting biodiversity and geodiversity across scales with satellite remote sensing. Wiley Online Libr. 28, 548–556 (2019).
    Google Scholar 
    65.Schrodt, F. et al. To advance sustainable stewardship, we must document not only biodiversity but geodiversity. Proc. Natl. Acad. Sci. U. S. A. 116, 16155–161658 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Read, Q. D. et al. Beyond counts and averages: Relating geodiversity to dimensions of biodiversity. Wiley Online Libr. 29, 696–710 (2020).
    Google Scholar 
    67.Antonelli, A. et al. Geological and climatic influences on mountain biodiversity. Nat. Geosci. 11, 718–725 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    68.Knudson, C., Kay, K. & Fisher, S. Appraising geodiversity and cultural diversity approaches to building resilience through conservation. Nat. Clim. Change 8, 678–685 (2018).ADS 
    Article 

    Google Scholar 
    69.Beier, P., Hunter, M. L. & Anderson, M. Special section: Conserving nature’s stage. Conserv. Biol. 29, 613–617 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    70.Dubinin, V., Svoray, T., Stavi, I. & Yizhaq, H. Using LANDSAT 8 and VENµS data to study the effect of geodiversity on soil moisture dynamics in a semiarid shrubland. Remote Sens. 12, 3377 (2020).ADS 
    Article 

    Google Scholar 
    71.Renne, R. R. et al. Soil and stand structure explain shrub mortality patterns following global change–type drought and extreme precipitation. Ecology 100, e02889 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    72.Gutterman, Y., Golan, T. & Garsani, M. Porcupine diggings as a unique ecological system in a desert environment. Oecologia 85, 122–127 (1990).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Armas, C., Pugnaire, F. I. & Sala, O. E. Patch structure dynamics and mechanisms of cyclical succession in a Patagonian steppe (Argentina). J. Arid Environ. 72, 1552–1561 (2008).ADS 
    Article 

    Google Scholar 
    74.Pickett, S. & White, P. The Ecology of Natural Disturbance and Patch Dynamics (Academic Press, 1985). https://doi.org/10.1016/C2009-0-02952-3.Book 

    Google Scholar 
    75.Segoli, M., Ungar, E. D., Giladi, I., Arnon, A. & Shachak, M. Untangling the positive and negative effects of shrubs on herbaceous vegetation in drylands. Landsc. Ecol. 27, 899–910 (2012).Article 

    Google Scholar 
    76.Rodríguez, F., Mayor, Á. G., Rietkerk, M. & Bautista, S. A null model for assessing the cover-independent role of bare soil connectivity as indicator of dryland functioning and dynamics. Ecol. Indic. 94, 512–519 (2018).Article 

    Google Scholar 
    77.Zelnik, Y. R., Kinast, S., Yizhaq, H., Bel, G. & Meron, E. Regime shifts in models of dryland vegetation. Philos. Trans. R. Soc. A https://doi.org/10.1098/rsta.2012.0358 (2013).Article 
    MATH 

    Google Scholar 
    78.Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. PNAS 103, 1342–1346 (2006).79.Kardol, P. et al. Climate change effects on plant biomass alter dominance patterns and community evenness in an experimental old-field ecosystem. Glob. Change Biol. 16, 2676–2687 (2010).ADS 
    Article 

    Google Scholar 
    80.Hillebrand, H., Bennett, D. M. & Cadotte, M. W. Consequences of dominance: A review of evenness effects on local and regional ecosystem processes. Ecology 89, 1510–1520 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    81.Stavi, I., Yizhaq, H., Szitenberg, A. & Zaady, E. Patch-scale to hillslope-scale geodiversity alleviates susceptibility of dryland ecosystems to climate change: Insights from the Israeli Negev. Curr. Opin. Environ. Sustain. 50, 129–137 (2021).Article 

    Google Scholar 
    82.Loarie, S. R. et al. Climate change and the future of California’s endemic flora. PLoS ONE 3, 2502 (2008).ADS 
    Article 
    CAS 

    Google Scholar 
    83.Loarie, S. R. et al. The velocity of climate change. Nature 462, 1052–1055 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Ashcroft, M. B., Chisholm, L. A. & French, K. O. Climate change at the landscape scale: Predicting fine-grained spatial heterogeneity in warming and potential refugia for vegetation. Glob. Change Biol. 15, 656–667 (2009).ADS 
    Article 

    Google Scholar 
    85.Correa-Metrio, A., Meave, J. A., Lozano-García, S. & Bush, M. B. Environmental determinism and neutrality in vegetation at millennial time scales. J. Veg. Sci. 25, 627–635 (2014).Article 

    Google Scholar 
    86.Baumgartner, J., Esperon-Rodriguez, M. & Beaumont, L. Identifying in situ climate refugia for plant species. Ecography (Cop.) 41, 1850–1863 (2018).Article 

    Google Scholar 
    87.Alahuhta, J. et al. The Role of Geodiversity in Providing Ecosystem Services at Broad Scales (Elsevier, 2018).Book 

    Google Scholar 
    88.Parks, K. E. & Mulligan, M. On the relationship between a resource based measure of geodiversity and broad scale biodiversity patterns. Biodivers. Conserv. 19, 2751–2766 (2010).Article 

    Google Scholar 
    89.Keppel, G. et al. The capacity of refugia for conservation planning under climate change. Front. Ecol. Environ. 13, 106–112 (2015).Article 

    Google Scholar 
    90.Mokany, K. et al. Past, present and future refugia for Tasmania’s palaeoendemic flora. J. Biogeogr. 44, 1537–1546 (2017).Article 

    Google Scholar  More

  • in

    Plant mixture balances terrestrial ecosystem C:N:P stoichiometry

    Data collectionWe systematically searched all peer-reviewed publications that were published prior to May 2021, which investigated the effects of plant diversity on terrestrial C:N:P ratios (i.e., plants, soils, soil microbial biomass, and extracellular enzymes) using the Web of Science (Core Collection; http://www.webofknowledge.com), Google Scholar (http://scholar.google.com), and the China National Knowledge Infrastructure (CNKI; https://www.cnki.net) using the search term: “C:N or C:P or N:P or C:N:P AND plant OR soil OR microbial biomass OR extracellular enzyme OR exoenzyme AND plant diversity OR richness OR mixture OR pure OR polyculture OR monoculture OR overyielding”, and also searched for references within these papers. Our survey also included studies summarized in previously published diversity-ecosystem functioning meta-analyses15,17,20,33. The literature search was performed following the guidelines of PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) (Moher, Liberati44; Supplementary Fig. 5).We employed the following criteria to select the studies: (i) they were purposely designed to test the effects of plant diversity on C:N:P ratios, (ii) they had at least one species mixture treatment and corresponding monocultures, (iii) they had the same initial climatic and soil properties in the monoculture and mixture treatment plots. In thirteen publications, several experiments, each with independent controls, were conducted at different locations and were considered to be distinct studies. In total, 169 studies met these criteria (Supplementary Fig. 5 and Supplementary Table 3). When different publications included the same data, we recorded the data only once. When a study included plant species mixtures of different numbers of species, we considered them as distinct observations.For each site, we extracted the means, the number of replications, and standard deviations of the C:N, N:P, and C:P ratios of plants (including leaves, shoots, fine roots, total roots), soils, soil enzymes as well as soil microbial biomass C:N ratios, if reported. Similar to Zhou and Staver45, we collected nine types of soil enzymes and integrated individual soil enzymes into combined enzymes to represent proxies targeting specific resource acquisitions: C-acquisition (average of Invertase, α-Glucosidase, β-1,4-Glucosidase, Cellobiohydrolase, β-1,4-Xylosidase), N-acquisition (average of β-1,4-N-acetylglucosaminidase, Leucine-aminopeptidase, Urease), and P-acquisition (phosphatase). The ratios of each type of enzyme were subsequently calculated, referred to as soil enzyme C:N, C:P, and N:P. When an original study reported the results graphically, we used Plot Digitizer version 2.0 (Department of Physics at the University of South Alabama, Mobile, AL, USA) to extract data from the figures. This resulted in 52 studies for plant C:N ratios, 35 studies for plant N:P ratios, 17 studies for plant C:P ratios, 83 studies for soil C:N ratios, 42 studies for soil N:P ratios, 19 studies for soil C:P ratios, 33 studies for soil microbial biomass C:N ratios, 41 studies for soil enzyme C:N ratios, 40 studies for soil enzyme N:P ratios and 34 studies for soil enzyme C:P ratios (Supplementary Table 3).We also extracted species compositions in mixtures, latitude, longitude, stand age, ecosystem type (i.e, forest, grassland, cropland, pot), mean annual temperature (MAT, °C), management practice (fertilization or not), soil type (FAO classification) and sampled soil depth from original or cited papers, or cited data sources. The mean annual aridity index and solar radiation data were retrieved from the CGIAR-CSI Global Aridity Index data set46 and WorldClim Version 247 using location information. The annual aridity index was calculated as the ratio of the mean annual precipitation to mean annual potential evapotranspiration48. Stand age (SA) was recorded as the number of years since stand establishment following stand-replacing disturbances in forests, and the number of years between the initiation and measurements of the experiments in grasslands, croplands, and pots. Observations were averaged if multiple measurements were conducted during different seasons within a year. The species proportions in plant mixtures were based on the stem density in forests and pots, coverage in croplands, and sown seeds in grasslands. Soil depth was recorded as the midpoint of each soil depth interval49. We employed the weighted averages of soil C:N, C:P, and N:P ratios of monocultures in each study as proxies for the status of background nutrients. For studies that did not report soil C:N, C:P, and N:P ratios of monocultures, we used the initial soil C:N, C:P, and N:P ratios (before experiment establishment, if reported) as proxies for the status of background nutrients. When a study reported the soils, soil microbial biomass or soil enzyme C:N:P data from multiple soil depths, we used the soil C:N, C:P, and N:P ratios of the corresponding depths as background nutrient proxies. For plant C:N:P data, we used the uppermost soil layer C:N, C:P, and N:P ratios as background nutrient proxies, since it contains the majority of the available nutrients essential for plant growth50. We compared the estimates for the data sets with and without pot studies and found that both data sets yielded qualitatively similar results (Supplementary Tables 2 and 4). Thus, we reported results based on the whole data set.We employed two key functional traits to describe the functional composition: ‘leaf nitrogen content per leaf dry mass’ (Nmass, mg g−1), and “specific leaf area” (SLA, mm2 mg−1; i.e., leaf area per leaf dry mass), as they are expected to be related to plant growth rate, resource uptake and use efficiency27, and are available for large numbers of species. We obtained the mean trait values of Nmass and SLA data by using all available measurements for each plant species from the TRY Plant Trait Database51 except for two studies that included the data in their original publication52, or related publications in the same sites53. Functional diversity (FDis) was calculated as functional dispersion, which is the mean distance of each species to the centroid of all species in the functional trait space, based on the two traits together54. The calculation of FDis was conducted using the FD package54.Data analysisThe natural log-transformed response ratio (lnRR) was employed to quantify the effects of plant mixture following Hedges, Gurevitch55:$${{{{{{mathrm{ln}}}}}}}{RR}={{{{{{mathrm{ln}}}}}}}({bar{X}}_{{{{{{mathrm{t}}}}}}}/{bar{X}}_{{{{{{mathrm{c}}}}}}})={{{{{{{mathrm{ln}}}}}}}bar{X}}_{{{{{{mathrm{t}}}}}}}-{{{{{{{mathrm{ln}}}}}}}bar{X}}_{{{{{{mathrm{c}}}}}}}$$
    (1)
    where ({overline{X}}_{{{{{{rm{t}}}}}}}) and ({overline{X}}_{{{{{{rm{c}}}}}}}) are the observed values of a selected variable in the mixture and the expected value of the mixture in each study, respectively. If a study has multiple richness levels in mixtures (for example, 1, 4, 8, and 16), lnRR was calculated for the species richness levels 4, 8, and 16, respectively. We calculated ({overline{X}}_{{{{{{rm{c}}}}}}}) based on weighted values of the component species in monocultures following Loreau and Hector39:$$overline{{X}_{{{{{{mathrm{c}}}}}}}}=sum ({p}_{i}times {m}_{i})$$
    (2)
    where mi is the observed value of the selected variable of the monoculture of species i and pi is the proportion of species i density in the corresponding mixture. When a study reported multiple types of mixtures (species richness levels) and experimental years, ({overline{X}}_{{{{{{rm{t}}}}}}}) and ({overline{X}}_{{{{{{rm{c}}}}}}}) were calculated separately for each mixture type and experimental year.In our data set, sampling variances were not reported in 37 of the 169 studies, and no single control group mean estimate is present with standard deviation or the standard error reported. Like the previous studies6,56, we employed the number of replications for weighting:$${W}_{{{{{{mathrm{r}}}}}}}=({N}_{{{{{{mathrm{c}}}}}}}times {N}_{{{{{{mathrm{t}}}}}}})/({N}_{{{{{{mathrm{c}}}}}}}+{N}_{{{{{{mathrm{t}}}}}}})$$
    (3)
    where Wr is the weight associated with each lnRR observation, and Nc and Nt are the number of replications in monocultures and corresponding mixtures, respectively.The C:N, N:P, and C:P ratios of plants, soils, and soil enzymes, as well as soil microbial biomass C:N ratios were considered as response variables and analyzed separately. To validate the linearity assumption for the continuous predictors, we initially graphically plotted the lnRR vs. individual predictors, including FDis, SA, and background nutrient status (N, i.e., C:N, C:P, and N:P ratios of soil) and identified logarithmic functions as an alternative to linear functions. We also statistically compared the linear and logarithmic functions with the predictor of interest as the fixed effect, and “study” and measured plant parts (i.e., leaves, shoots, fine roots, total roots) or soil depth as the random effects, using Akaike information criterion (AIC). The random factors were used to account for the autocorrelation among observations within each “Study”, and potential influences of variation in measured plant parts and soil depth. We found that the linear FDis, SA, and N resulted in lower, or similar AIC values (∆AIC  More

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    Beneficial insects are associated with botanically rich margins with trees on small farms

    1.Scheper, J. et al. Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss—a meta-analysis. Ecol. Lett. 16, 912–920. https://doi.org/10.1111/ele.12128 (2013).Article 
    PubMed 

    Google Scholar 
    2.Holzschuh, A., Steffan-Dewenter, I. & Tscharntke, T. How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids?. J. Anim. Ecol. 79, 491–500 (2010).Article 

    Google Scholar 
    3.Mwangi, D. et al. Diversity and abundance of native bees foraging on hedgerow plants in the Kakamega farmlands, western Kenya. J. Apic. Res. 51, 298–305. https://doi.org/10.3896/ibra.1.51.4.02 (2012).Article 

    Google Scholar 
    4.Rollin, O. et al. Weed-insect pollinator networks as bio-indicators of ecological sustainability in agriculture. A review. Agronomy Sustain. Develop. 36, 8. https://doi.org/10.1007/s13593-015-0342-x (2016).Article 

    Google Scholar 
    5.Bianchi, F. J. J. A., Booij, C. J. H. & Tscharntke, T. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. Royal Soc. B Biol. Sci. 273, 1715–1727 (2006).CAS 
    Article 

    Google Scholar 
    6.Landis, D. A., Wratten, S. D. & Gurr, G. M. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45, 175–201. https://doi.org/10.1146/annurev.ento.45.1.175 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    7.Pollier, A., Tricault, Y., Plantegenest, M. & Bischoff, A. Sowing of margin strips rich in floral resources improves herbivore control in adjacent crop fields. Agric. For. Entomol. 21, 119–129. https://doi.org/10.1111/afe.12318 (2019).Article 

    Google Scholar 
    8.Marshall, E. J. P., West, T. M. & Kleijn, D. Impacts of an agri-environment field margin prescription on the flora and fauna of arable farmland in different landscapes. Agr. Ecosyst. Environ. 113, 36–44. https://doi.org/10.1016/j.agee.2005.08.036 (2006).Article 

    Google Scholar 
    9.Karp, D. S. et al. Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc. Natl. Acad. Sci. 115, E7863. https://doi.org/10.1073/pnas.1800042115 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Elisante, F. et al. Insect pollination is important in a smallholder bean farming system. PeerJ 8, e10102 (2020).Article 

    Google Scholar 
    11.Karanja, R., Njoroge, G., Gikungu, M. & Newton, L. Bee interactions with wild flora around organic and conventional coffee farms in Kiambu district, central Kenya. J. Pollination Ecol. 2, 7–12. https://doi.org/10.26786/1920-7603(2010)5 (2010).Article 

    Google Scholar 
    12.Koji, S., Khan, Z. R. & Midega, C. A. O. Field boundaries of Panicum maximum as a reservoir for predators and a sink for Chilo partellus. J. Appl. Entomol. 131, 186–196. https://doi.org/10.1111/j.1439-0418.2006.01131.x (2007).Article 

    Google Scholar 
    13.Nel, L. et al. Exotic plants growing in crop field margins provide little support to mango crop flower visitors. Agric. Ecosyst. Environ. 250, 72–80. https://doi.org/10.1016/j.agee.2017.09.002 (2017).Article 

    Google Scholar 
    14.Gaigher, R., Pryke, J. S. & Samways, M. J. High parasitoid diversity in remnant natural vegetation, but limited spillover into the agricultural matrix in South African vineyard agroecosystems. Biol. Cons. 186, 69–74. https://doi.org/10.1016/j.biocon.2015.03.003 (2015).Article 

    Google Scholar 
    15.Vogel, C., Chunga, T. L., Sun, X., Poveda, K. & Steffan-Dewenter, I. Higher bee abundance, but not pest abundance, in landscapes with more agriculture on a late-flowering legume crop in tropical smallholder farms. PeerJ 9, e10732. https://doi.org/10.7717/peerj.10732 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Tscharntke, T. et al. When natural habitat fails to enhance biological pest control—Five hypotheses. Biol. Cons. 204, 449–458. https://doi.org/10.1016/j.biocon.2016.10.001 (2016).Article 

    Google Scholar 
    17.Griffiths, G. J. K., Holland, J. M., Bailey, A. & Thomas, M. B. Efficacy and economics of shelter habitats for conservation biological control. Biol. Control 45, 200–209. https://doi.org/10.1016/j.biocontrol.2007.09.002 (2008).Article 

    Google Scholar 
    18.Albrecht, M., Duelli, P., Schmid, B. & Müller, C. B. Interaction diversity within quantified insect food webs in restored and adjacent intensively managed meadows. J. Anim. Ecol. 76, 1015–1025. https://doi.org/10.1111/j.1365-2656.2007.01264.x (2007).Article 
    PubMed 

    Google Scholar 
    19.Lemessa, D., Hambäck, P. A. & Hylander, K. Arthropod but not bird predation in Ethiopian homegardens is higher in tree-poor than in tree-rich landscapes. PLoS ONE 10, e0126639. https://doi.org/10.1371/journal.pone.0126639 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Urbanowicz, C., Muñiz, P. A. & McArt, S. H. Honey bees and wild pollinators differ in their preference for and use of introduced floral resources. Ecol. Evol. 10, 6741–6751 (2020).Article 

    Google Scholar 
    21.Seitz, N., van Engelsdorp, D. & Leonhardt, S. D. Are native and non-native pollinator friendly plants equally valuable for native wild bee communities?. Ecol. Evol. 10, 12838–12850. https://doi.org/10.1002/ece3.6826 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Vaudo, A. D., Tooker, J. F., Grozinger, C. M. & Patch, H. M. Bee nutrition and floral resource restoration. Current Opinion Insect Sci. 10, 133–141. https://doi.org/10.1016/j.cois.2015.05.008 (2015).Article 

    Google Scholar 
    23.Delaney, A. et al. Local-scale tree and shrub diversity improves pollination services to shea trees in tropical West African parklands. J. Appl. Ecol. https://doi.org/10.1111/1365-2664.13640 (2020).Article 

    Google Scholar 
    24.Miller, D., Muñoz-Mora, J. C. & Christiaensen, L. in Agriculture in Africa: Telling Myths from Facts (eds L. Christiaensen & L. Demery) Ch. 13, 115–121 (The World Bank Group, 2018).25.Meijer, S. S., Catacutan, D., Sileshi, G. W. & Nieuwenhuis, M. Tree planting by smallholder farmers in Malawi: Using the theory of planned behaviour to examine the relationship between attitudes and behaviour. J. Environ. Psychol. 43, 1–12. https://doi.org/10.1016/j.jenvp.2015.05.008 (2015).Article 

    Google Scholar 
    26.Otieno, M. et al. Enhancing legume crop pollination and natural pest regulation for improved food security in changing African landscapes. Glob. Food Sec. 26, 100394. https://doi.org/10.1016/j.gfs.2020.100394 (2020).Article 

    Google Scholar 
    27.Masiga, R. et al. Do French beans (Phaseolus vulgaris) grown in proximity to Mt Kenya forest in Kenya experience pollination deficit?. J. Pollination Ecol. 14, 255–260 (2014).Article 

    Google Scholar 
    28.Liaw, A. & Wiener, M. Classification and regression by random. Forest R news 2, 18–22 (2002).
    Google Scholar 
    29.R Core Team. R: A language and environment for statistical computing. https://www.R-project.org/. (2020).30.ggplot2: Elegant graphics for data analysis (Springer-Verlag New York, 2016).31.Hagen, M. & Kraemer, M. Agricultural surroundings support flower–visitor networks in an Afrotropical rain forest. Biol. Cons. 143, 1654–1663. https://doi.org/10.1016/j.biocon.2010.03.036 (2010).Article 

    Google Scholar 
    32.Rezende, M. Q., Venzon, M., Perez, A. L., Cardoso, I. M. & Janssen, A. Extrafloral nectaries of associated trees can enhance natural pest control. Agric. Ecosyst. Environ. 188, 198–203. https://doi.org/10.1016/j.agee.2014.02.024 (2014).Article 

    Google Scholar 
    33.Letourneau, D. K. et al. Does plant diversity benefit agroecosystems? A synthetic review. Ecol. Appl. 21, 9–21 (2011).Article 

    Google Scholar 
    34.Classen, A. et al. Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proc. Royal Soc. B Biol. Sci. 281, 20133148. https://doi.org/10.1098/rspb.2013.3148 (2014).Article 

    Google Scholar 
    35.Letourneau, D. K., Jedlicka, J. A., Bothwell, S. G. & Moreno, C. R. Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 40, 573–592. https://doi.org/10.1146/annurev.ecolsys.110308.120320 (2009).Article 

    Google Scholar 
    36.Paredes, D., Karp, D. S., Chaplin-Kramer, R., Benítez, E. & Campos, M. Natural habitat increases natural pest control in olive groves: economic implications. J. Pest. Sci. 92, 1111–1121 (2019).Article 

    Google Scholar 
    37.Gurr, G. M. et al. Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nat. Plants 2, 1–4 (2016).Article 

    Google Scholar 
    38.Frankie, G. et al. Native and non-native plants attract diverse bees to urban gardens in California. J. Pollination Ecol. 25, 16–23 (2019).39.Mkenda, P. et al. Extracts from field margin weeds provide economically viable and environmentally benign pest control compared to synthetic pesticides. PLoS ONE 10, e0143530. https://doi.org/10.1371/journal.pone.0143530 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    40.Rioba, N. B. & Stevenson, P. C. Ageratum conyzoides L. for the management of pests and diseases by small holder farmers. Ind. Crops Prod. 110, 22–29. https://doi.org/10.1016/j.indcrop.2017.06.068 (2017).Article 

    Google Scholar 
    41.Mwangi, D. M. & Wambugu, C. Adoption of forage legumes: the case of Desmodium intortum and Calliandra calothyrsus in central Kenya. Tropical Grasslands 37, 227–238 (2003).
    Google Scholar 
    42.Chaplin-Kramer, R. et al. Global malnutrition overlaps with pollinator-dependent micronutrient production. Proc. Royal Soc. B Biol. Sci. 281, 20141799. https://doi.org/10.1098/rspb.2014.1799 (2014).Article 

    Google Scholar 
    43.Mkindi, A. et al. Invasive weeds with pesticidal properties as potential new crops. Ind. Crops Prod. 110, 113–122. https://doi.org/10.1016/j.indcrop.2017.06.002 (2017).CAS 
    Article 

    Google Scholar 
    44.Njovu, H. K. et al. Leaf traits mediate changes in invertebrate herbivory along broad environmental gradients on Mt. Kilimanjaro. Tanzania. J. Animal Ecol. 88, 1777–1788. https://doi.org/10.1111/1365-2656.13058 (2019).Article 

    Google Scholar 
    45.Elisante, F. et al. Enhancing knowledge among smallholders on pollinators and supporting field margins for sustainable food security. J. Rural. Stud. 70, 75–86. https://doi.org/10.1016/j.jrurstud.2019.07.004 (2019).Article 

    Google Scholar 
    46.Ensslin, A. et al. Effects of elevation and land use on the biomass of trees, shrubs and herbs at Mount Kilimanjaro. Ecosphere 6, art45. https://doi.org/10.1890/ES14-00492.1 (2015).Article 

    Google Scholar 
    47.Mkenda, P. A. et al. Field margin vegetation in tropical African bean systems harbours diverse natural enemies for biological pest control in adjacent crops. Sustainability 11, 6399. https://doi.org/10.3390/su11226399 (2019).Article 

    Google Scholar 
    48.Matechou, E., Freeman, S. N. & Comont, R. Caste-specific demography and phenology in bumblebees: Modelling BeeWalk data. J. Agric. Biol. Environ. Stat. 23, 427–445. https://doi.org/10.1007/s13253-018-0332-y (2018).MathSciNet 
    Article 
    MATH 

    Google Scholar 
    49.Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).Article 

    Google Scholar 
    50.Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27(379–423), 623–656 (1948).MathSciNet 
    Article 

    Google Scholar 
    51.Ulrich, H. Predation by adult Dolichopodidae (Diptera): a review of literature with an annotated prey-predator list. Studia Dipterologica 11, 369–403 (2004).
    Google Scholar 
    52.Negro, M. et al. Effects of forest management on ground beetle diversity in alpine beech (Fagus sylvatica L.) stands. Forest Ecol. Manage. 328, 300–309. https://doi.org/10.1016/j.foreco.2014.05.049 (2014).Article 

    Google Scholar 
    53.Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. Royal Statistic. Soc. Ser. B Statistic. Methodol. 73, 3–36 (2011).MathSciNet 
    Article 

    Google Scholar 
    54.Dormann, C. F., Gruber, B. & Fruend, J. Introducing the bipartite package: analysing ecological networks. R news 8(2), 8–11 (2008).
    Google Scholar  More

  • in

    The isotopic niche of Atlantic, biting marine mammals and its relationship to skull morphology and body size

    1.Pauly, D., Trites, A. W., Capuli, E. & Christensen, V. Diet composition and trophic levels of marine mammals. ICES J. Mar. Sci. 55, 467–481 (1998).Article 

    Google Scholar 
    2.Wilson, D. E. & Mittermeier, R. A. Handbook of the mammals of the world. Sea mammals (Lynx Edicions 2014).3.Plagányi, E. E. & Butterworth, E. S. Competition with fisheries in Encyclopedia of Marine Mammals (eds W. F. Perrin, B. Würsing, & J. G. M. Thewsissen) 269–275 (Academic Press, 2009).4.Read, A. J. The looming crisis: interactions between marine mammals and fisheries. J. Mammal. 89, 541–548 (2008).Article 

    Google Scholar 
    5.Morissette, L., Christensen, V. & Pauly, D. Marine mammal impacts in exploited ecosystems: would large scale culling benefit fisheries? PLoS One 7, e43966 (2012).6.Gerber, L. R., Morissette, L., Kaschner, K. & Pauly, D. Should whales be culled to increase fishery yield?. Science 323, 880–881 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.DeMaster, D. P., Fowler, C. W., Perry, S. L. & Richlen, M. F. Predation and competition: the impact of fisheries on marine-mammals populations over the next one hundred years. J. Mammal. 82, 641–651 (2001).Article 

    Google Scholar 
    8.Smith, T. D. Interactions between marine mammals and fisheries: an unresolved problem for fisheries research in Whales, seals, fish and man (eds A.S. Blix, L. Walløe, & t Ø. Ultan) 527–536 (Elsevier Science, 1995).9.Hall, A. J., Watkins, J. & Hammond, P. S. Seasonal variation in the diet of harbour seals in the south-western North Sea. Mar. Ecol. Prog. Ser. 170, 269–281 (1998).ADS 
    Article 

    Google Scholar 
    10.Santos, M. B., Martin, V., Fernández, A. & Pierce, G. J. Insights into the diet of beaked whales from the atypical mass stranding in the Canary Islands in September 2002. J. Mar. Biol. Assoc. U. K. 87, 243–251 (2007).Article 

    Google Scholar 
    11.Gómez-Campos, E., Borrell, A., Cardona, L., Forcada, J. & Aguilar, A. Overfishing of small pelagic fishes increases trophic overlap between immature and mature striped dolphins in the Mediterranean sea. PLoS One 6, e24554 (2011).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    12.Adam, P. J. & Berta, A. Evolution of prey capture strategies and diet in the pinnipedimorpha (Mammalia, Carnivora). Oryctos 4, 83–107 (2002).
    Google Scholar 
    13.Kienle, S. S. & Berta, A. The better to eat you with: the comparative feeding morphology of phocid seals (Pinnipedia, Phocidae). J. Anat. 228, 396–413 (2016).PubMed 
    Article 

    Google Scholar 
    14.McCurry, M. R., Fitzgerald, E. M. G., Evans, A. R., Adams, J. W. & McHenry, C. R. Skull shape reflects prey size niche in toothed whales. Biol. J. Linn. Soc. 121, 936–946 (2017).Article 

    Google Scholar 
    15.McCurry, M. R. et al. The remarkable convergence of skull shape in crocodilians and toothed whales. Proc. R. Soc. B 284, 20162348 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    16.Davis, R. W. Marine Mammals: adaptations for an aquatic life (Springer, 2019).Book 

    Google Scholar 
    17.Marshall, C. D. & Pyenson, N. D. Feeding in aquatic mammals: an evolutionary and functional approach in Feeding in vertebrates: evolution, morphology, behaviour, biomechanics. Fascinating Life Sciences (eds V. Bels & I. Whishaw) 743–785 (Springer, Cham, 2019).18.Werth, A. J. Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J. Mammal. 87, 579–588 (2006).Article 

    Google Scholar 
    19.Kelley, N. P. & Motani, R. Trophic convergence drives morphological convergence in marine tetrapods. Biol. Lett. 11, 20140709 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Kienle, S. S., Law, C. J., Costa, D. P., Berta, A. & Mehta, R. S. Revisiting the behavioural framework of feeding in predatory aquatic mammals. Proc. R. Soc. B 284, 20171035 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Segura, A. M., Franco-Trecu, V., Franco-Fraguas, P. & Arim, M. Gape and energy limitation determining a humped relationship between trophic position and body size. Can. J. Fish. Aquat. Sci. 72, 198–205 (2015).CAS 
    Article 

    Google Scholar 
    22.Taylor, M. A. How tetrapods feed in water: a functional analysis by paradigm. Zool. J. Linn. Soc. 91, 171–195 (1987).Article 

    Google Scholar 
    23.Werth, A. Feeding in marine mammals in Feeding: form, function, and evolution in tetrapod vertebrates (ed K. Schwenk) 487–526 (Academic Press, 2010).24.Hocking, D. P., Salverson, M., Fitzgerald, E. M. G. & Evans, A. R. Australian fur seals (Arctocephalus pusillus doriferus) use raptorial biting and suction feeding when targeting prey in different foraging scenarios. PLoS One 9, e112521 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    25.Dalerum, F. & Angerbjörn, A. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144, 647–658 (2005).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Bearhop, S., Adams, C. E., Waldrons, S., Fuller, R. A. & Macleod, H. Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol. 73, 1007–1012 (2004).Article 

    Google Scholar 
    27.Layman, C. A., Arrington, D. A., Montanä, C. G. & Post, D. M. Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology 88, 42–48 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Michener, R. H. & Lajtha, K. Stable isotopes in ecology and environmental science. Second edn, (Blackwell publishing, 2007).30.Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718 (2002).Article 

    Google Scholar 
    31.Das, K. et al. Marine mammals from northeast Atlantic: relationship between their trophic status as determined by d13C and d15N measurements and their trace metal concentration. Mar. Environ. Res. 56, 349–365 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Das, K., Lepoint, G., Leroy, Y. & Bouquegneau, J. M. Marine mammals from the southern North Sea: feeding ecology data from d13C and d15N measurements. Mar. Ecol. Prog. Ser. 263, 287–298 (2003).ADS 
    Article 

    Google Scholar 
    33.Mèndez-Fernandez, P. et al. Foraging ecology of five toothed whale species in the Northwest Iberian Peninsula, inferred using carbon and nitrogen isotope ratios. J. Exp. Mar. Biol. Ecol. 413, 150–158 (2012).Article 
    CAS 

    Google Scholar 
    34.Pinela, A. M., Borrell, A., Cardona, L. & Aguilar, A. Stable isotope analysis reveals habitat partitioning among marine mammals off the NW African coast and unique trophic niches for two globally threatened species. Mar. Ecol. Prog. Ser. 416, 295–306 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    35.Costa, A. F., Botta, S., Siciliano, S. & Giarrizzo, T. Resource partitioning among stranded aquatic mammals from Amazon and northeastern coast of Brazil revealed through carbon and nitrogen stable isotopes. Sci. Rep. 10, 12897 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Bisi, T. L. et al. Trophic relationships and habitat preferences of delphinids from the southeastern Brazilian coast determined by carbon and nitrogen stable isotope composition. PLoS One 8, e82205 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Riccialdelli, L., Newsome, S. D., Fogel, M. L. & Goodall, R. N. Isotopic assessment of prey and habitat preferences of a cetacean community in the southwestern South Atlantic Ocean. Mar. Ecol. Prog. Ser. 418, 235–248 (2010).ADS 
    Article 

    Google Scholar 
    38.Saporiti, F. et al. Resource partitioning among air-breathing marine predators: are body size and mouth diameter the major determinants?. Mar. Ecol. 37, 957–969 (2016).ADS 
    Article 

    Google Scholar 
    39.Ford, J. K. B. Killer whale Orcinus orca in Encyclopedia of Marine Mammals (eds B. Würsig, J.G.M. Thewissen, & K.M. Kovacs) 531–537 (Academic Press, 2018).40.Durban, J. W. & Pitman, R. L. Antarctic killer whales make rapid, round-trip movements to subtropical waters: evidence for physiological maintenance migrations?. Biol. Lett. 8, 274–277 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Drago, M. et al. Mouth gape determines the response of marine top predators to long-term fishery-induced changes in food web structure. Sci. Rep. 8, 15759 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    42.Drago, M. et al. Isotopic niche partitioning between two apex predators over time. J. Anim. Ecol. 86, 766–780 (2017).PubMed 
    Article 

    Google Scholar 
    43.Bond, A. L. & Hobson, K. A. Reporting stable-isotope ratios in ecology: Recommended terminology, guidelines and best practices. Waterbirds 35, 324–331 (2012).Article 

    Google Scholar 
    44.Skrzypek, G. Normalization procedures and reference material selection in stable HCNOS isotope analyses: an overview. Anal. Bioanal. Chem. 405, 2815–2823 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Newsome, S. D., Clementz, M. T. & Koch, P. L. Using stable isotope biogeochemistry to study marine mammal ecology. Mar. Mamm. Sci. 26, 509–572 (2010).CAS 

    Google Scholar 
    46.Keeling, C. D. The Suess effect: 13Carbon-14Carbon interactions. Environ. Int. 2, 229–300 (1979).CAS 
    Article 

    Google Scholar 
    47.Verburg, P. The need to correct for the Suess effect in the application of δ13C in sediment of autotrophic Lake Tanganyika, as a productivity proxy in the Anthropocene. J. Paleolimnol. 37, 591–602 (2007).ADS 
    Article 

    Google Scholar 
    48.Gruber, N. et al. Spatiotemporal patterns of carbon-13 in the global surface oceans and the oceanic Suess effect. Global Biogeochem. Cycles 13, 307–335 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    49.Quay, P., Sonnerup, R., Westby, T., Stutsman, J. & McNichol, A. Changes in the 13C/12C of dissolved inorganic carbon in the ocean as a tracer of anthropogenic CO2 uptake. Global Biogeochem. Cycles 17, 1004 (2003).ADS 
    Article 
    CAS 

    Google Scholar 
    50.Borrell, A., Abad-Oliva, N., Gómez-Campos, E., Giménez, J. & Aguilar, A. Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans. Rapid Commun. Mass Spectrom. 26, 1596–1602 (2012).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.McMahon, K. W., Hamady, L. L. & Thorrold, S. R. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol. Oceanogr. 58, 697–714 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    52.R Core Team. R: A language and environment for statistical computing, http://www.R-project.org. (2018).53.Hobson, K. A. & Clark, R. G. Assessing avian diets using stable isotopes analysis. I: Turnover of 13C in tissues. The Condor 94, 181–188 (1992).Article 

    Google Scholar 
    54.Hobson, K. A. & Clark, R. G. Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. The Condor 94, 189–197 (1992).Article 

    Google Scholar 
    55.Casey, M. M. & Post, D. M. The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth Sci. Rev. 106, 131–148 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    56.Barnes, C., Seeting, C. J., Jennings, S., Barry, J. T. & Polunin, N. V. C. Effect of temperature and ration size on carbon and nitrogen isotope trophic fractionation. Funct. Ecol. 21, 356–362 (2007).Article 

    Google Scholar 
    57.Bloomfield, A. L., Elsdon, T. S., Walther, B. D. & Gier, E. J. Temperature and diet affect carbon and nitrogen isotopes of fish muscle: can amino acid nitrogen isotopes explain effects?. J. Exp. Mar. Biol. Ecol. 399, 48–59 (2011).CAS 
    Article 

    Google Scholar 
    58.Saporiti, F. et al. Latitudinal changes in the structure of marine food webs in the Southwestern Atlantic Ocean. Mar. Ecol. Prog. Ser. 538, 23–34 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    59.Wells, R. S. & Scott, M. D. Bottlenose dolphin, Tursiops truncatus, common bottlenose dolphin in Encyclopedia of Marine Mammals (eds B. Würsig, J.G.M. Thewissen, & K.M. Kovacs) 118–125 (Academic Press, 2018).60.Natoli, A., Peddemors, V. M. & Hoelzel, A. R. Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. J. Evol. Biol. 17, 363–375 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Costa, A. P. B., Rosel, P. E., Daura-Jorge, F. G. & Simões-Lopes, P. C. Offshore and coastal common bottlenose dolphins of the western South Atlantic face-to-face: what the skull and the spine can tell us. Mar. Mamm. Sci. 32, 1433–1457 (2016).Article 

    Google Scholar 
    62.Drago, M. et al. Stable oxygen isotopes reveal habitat use by marine mammals in the Río de la Plata estuary and adjoining Atlantic Ocean. Estuar. Coast. Shelf Sci. 238, 106708 (2020).63.Koen, A. M., Pedraza, S. N., Sciavini, A. C. M., Goodall, R. N. & Crespo, E. A. Stomach contents of false killer whales (Pseudorca crassidens) stranded on the coasts of the strait of Magellan, Tierra del Fuego. Mar. Mamm. Sci. 15, 712–724 (1999).64.Page, C. E. & Cooper, N. Morphological convergence in ‘river dolphin’ skulls. PeerJ 5, e4090 (2017).65.Cohen, J. E., Pimm, S. L., Yodzis, P. & Saldañas, J. Body sizes of animal predators and animal prey in food webs. J. Anim. Ecol. 62, 67–78 (1993).Article 

    Google Scholar 
    66.Cohen, J. E., Jonsson, T. & Carpenter, S. R. Ecological community description using the food web, species abundance, and body size. Proc. Natl. Acad. Sci. U.S.A. 100, 1781–1786 (2003).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Warren, P. H. & Lawton, J. H. Invertebrate predator-prey body size relationships: an explanation for upper triangular food webs and patterns in food web structure?. Oecologia 74, 231–235 (1987).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Kerr, S. R. & Dickie, L. M. The biomass spectrum: a predator-prey theory of aquatic production. (Columbia University Press, 2001).69.Leaper, R. & Huxham, M. Size constraints in a real food web: predator, parasite and prey body-size relationships. Oikos 99, 443–456 (2002).Article 

    Google Scholar 
    70.Memmott, J., Martinez, N. D. & J.E., C. Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. J. Anim. Ecol. 69, 1–15 (2000).71.Williams, R. J. & Martinez, N. D. Simple rules yield complex food webs. Nature 404, 180–183 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Jennings, S. Size-based analyses of aquatic food webs in Aquatic food webs: an ecosystem approach (eds A. Belgrano, U.M. Scharler, J. Dunne, & R.E. Ulanowicz) 86–97 (Oxford University Press, 2005).73.Layman, C. A., Winemiller, K. O., Arrington, D. A. & Jepsen, D. B. Body size and trophic position in a diverse tropical food web. Ecology 86, 2530–2535 (2005).Article 

    Google Scholar 
    74.Jeglinski, J., Goetz, K. T., Werner, C., Costa, D. P. & Trillmich, F. Same size – same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. J. Anim. Ecol. 82, 694–706 (2013).PubMed 
    Article 

    Google Scholar 
    75.Akin, S. & Winemiller, K. O. Body size and trophic position in a temperate estuarine food web. Acta Oecol. 33, 144–153 (2008).ADS 
    Article 

    Google Scholar 
    76.Romanuk, T. N., Hayward, A. & Hutchings, J. A. Trophic level scales positively with body size in fishes. Glob. Ecol. Biogeogr. 20, 231–240 (2011).Article 

    Google Scholar 
    77.Madigan, D. J. et al. Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem. Sci. Rep. 2, 654 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar  More

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    Biodiversity needs every tool in the box: use OECMs

    COMMENT
    26 July 2021

    Biodiversity needs every tool in the box: use OECMs

    To conserve global biodiversity, countries must forge equitable alliances that support sustainability in traditional pastoral lands, fisheries-management areas, Indigenous territories and more.

    Georgina G. Gurney

    0
    ,

    Emily S. Darling

    1
    ,

    Gabby N. Ahmadia

    2
    ,

    Vera N. Agostini

    3
    ,

    Natalie C. Ban

    4
    ,

    Jessica Blythe

    5
    ,

    Joachim Claudet

    6
    ,

    Graham Epstein

    7
    ,

    Estradivari

    8
    ,

    Amber Himes-Cornell

    9
    ,

    Harry D. Jonas

    10
    ,

    Derek Armitage

    11
    ,

    Stuart J. Campbell

    12
    ,

    Courtney Cox

    13
    ,

    Whitney. R. Friedman

    14
    ,

    David Gill

    15
    ,

    Peni Lestari

    16
    ,

    Sangeeta Mangubhai

    17
    ,

    Elizabeth McLeod

    18
    ,

    Nyawira A. Muthiga

    19
    ,

    Josheena Naggea

    20
    ,

    Ravaka Ranaivoson

    21
    ,

    Amelia Wenger

    22
    ,

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    Customary fishing-rights holders from Totoya Island, Fiji, marking a sacred reef area as a no-fishing zone.Credit: Keith Ellenbogen

    Global support is growing for the 30 × 30 movement — a goal to conserve 30% of the planet by 2030. In May, the G7 group of wealthy nations endorsed the commitment to this target that had been made by more than 50 countries in January. It is likely to be the headline goal when parties to the Convention on Biological Diversity (CBD) meet to discuss the latest global conservation agreement in May 2022 in Kunming, China.So where do the sacred forests of Estonia or shipwrecks in North America’s Great Lakes come in? What do these share with managed fishing grounds in Fiji and bighorn-sheep hunting areas in Mexico? All have the potential to be recognized using a conservation policy tool called other effective area-based conservation measures, or OECMs. Together with protected areas — from Malaysia’s Taman Negara National Park to the Cerbère-Banyuls Marine Reserve in southern France — OECMs could help to achieve the 30% target.Devised in 2010 and defined in 2018, the OECM tool is little known outside specialist circles. Less than 1% of the world’s land and freshwater environments and less than 0.1% of marine areas are currently covered under this designation. Meanwhile, biodiversity is in free fall and protected areas alone can’t stem the loss. Both designations are among the international policy instruments being negotiated ahead of the CBD conference.We call on the CBD parties and the conservation community of policymakers, scientists, practitioners and donors to study and use OECMs more, alongside protected areas. This policy tool can advance equitable and effective conservation if CBD parties stay true to the convention’s intent to sustain biodiversity rather than ‘achieve’ area-based targets. But more groundwork must be laid to realize its potential.Improvements are needed in research, policy and practice. Local managers and CBD parties need better ways to assess whether potential OECMs contribute to sustaining biodiversity, so that areas are properly designated. The conservation community needs to develop processes to ensure that OECM recognition strengthens, rather than displaces, existing local governance. And researchers need to articulate the value of OECMs to encourage policymakers to use them.Bigger toolkit Protected areas have expanded rapidly in the past 10 years, and now cover 15.7% of the world’s land and fresh water, and 7.7% of the marine realm. Defined by the CBD as areas designated or regulated and managed for biodiversity conservation, they are an essential conservation approach. But some have failed to be equitable or effective: aligning biodiversity goals with local values, needs and governance can be difficult in some contexts1,2. This conflict can lead to inequities, non-compliance and poor biodiversity outcomes.
    Indigenous rights vital to survival
    OECMs can have an important and complementary role3. The tool recognizes managed areas that sustain biodiversity, irrespective of their objective. OECM recognition can support Indigenous and local communities in managing their lands and seas — be it for hunting, fishing or other cultural practices — while conserving nature. It opens up new conservation opportunities in landscapes where there is relatively light human usage, such as pastoralism with a low density of livestock. These regions make up nearly 56% of the world’s lands, and contain more Key Biodiversity Areas — sites of global important to biodiversity — than do remaining large wild areas4. So, management approaches that accommodate the ways people use landscapes and seascapes are crucial.Some managed areas do not safeguard biodiversity5. But there is a wealth of evidence suggesting that many do. For example, a study of the Peruvian Amazon found that Indigenous peoples’ territories were, on average, more effective than state-governed protected areas at preventing deforestation6. A review of 61 areas managed under territorial-use rights in fisheries in Chile found positive effects on biodiversity; some had levels of fish biomass and biodiversity that were comparable to those in a protected area that restricts all fishing7. And abandonment of agricultural management systems involving low-intensity farming methods in Europe — such as traditional haymaking in Romania — has been linked repeatedly to biodiversity loss8.Perhaps many of these could be recognized as OECMs (see ‘Conservation potential’). Doing so depends on the consent of the relevant governing bodies, and whether the managed area meets the CBD’s definition and criteria for OECMs, including demonstrated or expected biodiversity outcomes.

    EquityOECMs can help to ensure that international conservation targets are legitimate to the many and diverse actors required to turn the tide on biodiversity loss.Too often, the costs of conservation are felt locally while many of the benefits are shared globally — from carbon sequestration to preserving genetic resources. For instance, rainforest conservation, including a protected area, in the Ankeniheny-Zahamena Corridor in Madagascar meant that local farmers of vanilla, cloves and rice bore opportunity costs representing 27–84% of their average annual household income. The protection scheme is intended to cut 10 million tonnes of carbon dioxide emissions over 10 years9.Such inequities can occur when protected areas do not prioritize local values and needs. Although protected areas can have multiple objectives, the widely followed guidance from the International Union for Conservation of Nature (IUCN) advises that nature conservation should retain priority over all other objectives. This can alienate people who manage areas for other reasons. Even in the instance of Indigenous Protected Areas in Australia, which have resulted in an array of social and biodiversity benefits, the IUCN definition can undermine Indigenous Australians’ conceptualization of humans as part of nature, which underpins their governance systems2. This stands in contrast to the Western world view of humans as distinct from nature — a concept that is embedded in the IUCN definition and conservation more generally2,3.
    A spatial overview of the global importance of Indigenous lands for conservation
    However, OECMs need not have conservation as an objective. This means that they can be used to recognize the contributions of a myriad of actors who manage areas that sustain nature, regardless of why they do so. Indigenous peoples, for instance, manage 37% of the world’s natural lands10 for many reasons, such as maintaining rights, harvesting and cultural identity2,10,11. Recognition of Indigenous territories as OECMs could help to overcome current challenges of insecure rights, insufficient funding and exclusion of these communities from decision-making12. For example, Indonesia has initiated revisions to its conservation laws to accommodate coastal OECMs, which could provide opportunities for Indigenous and local communities to gain legal recognition of their rights to use and manage fisheries.OECMs can thus ensure a more equitable approach to conservation decision-making. They enable the participation of those who govern areas that sustain biodiversity but who are currently not involved in decision-making. For example, fisheries-management organizations have rebuilt some fish stocks, contributing to biodiversity and wider ecosystem health, yet the fisheries and conservation sectors are often divided13. OECMs can foster cooperation between sectors, and encourage the participation of fisheries-management organizations in conservation decision-making.EffectivenessCollectively, alongside protected areas, OECMs can increase the effectiveness of the global conservation system in four key ways.First, they support management that is tailored to its context14, and aligned with local values, governance and traditional knowledge systems. This fosters the local leadership, support and compliance that are key to biodiversity benefits14. For example, in Mo’orea, French Polynesia, protected areas that restricted all fishing did not meet fishers’ needs, leading to non-compliance and relatively little change in the density and biomass of coral-reef fish15. Conversely, a management area in Labrador, Canada, implemented at the behest of crab fishers, maintained the fishery and increased the biomass of fish species such as Atlantic cod (Gadus morhua) and other, non-target species16. This area seems likely to meet the OECM criteria.

    Estonia’s sacred groves are protected for their spiritual significance.Credit: Toomas Tuul/FOCUS/Universal Images Group via Getty

    Second, OECMs, together with protected areas, can help to ensure a well-connected conservation network in which all elements of biodiversity are represented and in which ecological processes, such as species movements, are sustained. For instance, Kenya’s wildlife conservancies provide geographical bridges between protected areas for the movement of wildlife such as zebras, and have potential to be recognized as OECMs.Third, OECMs can increase the diversity of tools in the global conservation system. This bolsters the system’s resilience to social and biophysical shifts, including climate change14. Redundancy in governance arrangements can help to mitigate risks associated with the current reliance on government-led protected areas, which are vulnerable to shifts in national priorities. For example, in 2017, the Bears Ears National Monument, a protected area in Utah, was downsized by 85% to make way for oil and gas exploration under a former US presidential administration.Fourth, OECMs help to bring conservation outcomes into focus. A key criterion for official designation is demonstrated or expected biodiversity outcomes, such as the restoration of a crucial habitat. This is not the case for protected areas, where a focus on coverage has, in some cases, led to expansion with scant biodiversity gains4.Five steps Key concerns remain about the misuse of OECM recognition. CBD parties might use it to meet commitments without actually tackling biodiversity loss. For example, in 2017, Canada increased the marine area it planned to report almost sixfold, by reclassifying 51 fishery closures as OECMs17. This decision was criticized on the grounds of insufficient evidence that these areas sustain biodiversity. Another concern is that, despite the focus on equity, any attempts to influence local governance could be perceived as a ‘land grab’ or ‘sea grab’ by external actors such as national governments, foreigners or international organizations. For example, the establishment of some privately owned protected areas in southern Chile has been suggested to have involved coercion and intimidation of smallholder farmers.
    Area-based conservation in the twenty-first century
    The conservation community needs to take the following five steps to overcome these key challenges to using the OECM policy tool.Show that they work. The 2019 IUCN Guidelines for Recognizing and Reporting OECMs provide clear criteria for identifying managed areas that are suitable for a full assessment against the CBD’s definition. However, research is needed on how to meet the crucial criteria of demonstrated or expected in situ conservation of biodiversity. This is challenging and resource-intensive, especially because of the variety of actors involved. Ideas based in Western science might not align with the knowledge systems of all involved.Guidelines should build on existing approaches for evaluation, such as the IUCN Green List for Protected and Conserved Areas and the Indicators of Resilience in Socio-ecological Production Landscapes (SEPLs). They should include recent advances focused on outcomes18 and should be tailored to different types of managed area. To ensure that these are salient, credible and legitimate to those governing OECMs, they should be co-produced by groups such as rights holders, civil-society organizations, government and industry, as well as by academics from various disciplines. This transdisciplinary approach is growing rapidly, with examples ranging from management at the national level (such as New Zealand’s Sustainable Seas National Science Challenge) to the monitoring of coral reefs as social-ecological systems19.

    Pastoral lands in Africa are often governed to maintain sustainable grazing.Credit: Steve Pastor

    Strengthen existing local governance. Many rights holders have raised concerns that formal recognition of their managed areas for conservation might infringe their rights. For example, few communities in Fiji have had their fisheries-management areas recognized under national conservation laws, because that currently requires the communities to waive their customary rights20.Engaging with global conservation processes might also erode self-determination through the imposition of external world views2,3,12. Although OECMs open the door to recognizing diverse relations between humans and nature, it is crucial that the need for demonstrated or expected biodiversity outcomes does not diminish other priorities and values.OECM recognition must strengthen existing local governance, rather than displace or substantially alter it. This will require guidelines to be informed by principles of procedural equity and tailored to different types of managed area. Their development should draw on existing approaches such as the Australian Indigenous-led Healthy Country Planning and Our Knowledge, Our Way guidelines, which have underpinned engagement with the national carbon sequestration scheme11.Secure funding. Funding for recognizing and reporting OECMs should be made available to ensure costs are not a barrier or burden for under-resourced groups. A prominent role for OECMs in the next CBD agreement will help — this policy guides conservation investments from nations and donors.
    Sixty years of tracking conservation progress using the World Database on Protected Areas
    Importantly, the diversity of managed areas that OECMs encompass can provide funding opportunities beyond conventional conservation funders, whose resources for protected-area funding are already overstretched. Conservation practitioners should engage private sectors that manage areas that could be recognized as OECMs, and access funding earmarked for other priorities such as health and development. For example, the Watershed Interventions for Systems Health project in Fiji, which aims to reduce waterborne diseases using nature-based solutions, is supported by both conservation and public-health funding.Conservation donors and practitioners should co-design new funding strategies for OECMs with those governing these areas. This will help to ensure that local priorities are supported. For example, Coast Funds, a unique conservation trust fund, was developed by First Nations people in collaboration with conservation practitioners and the forestry industry to support stewardship of the Great Bear Rainforest and Haida Gwaii regions of British Columbia, Canada.Agree on metrics. The record of progress towards the CBD’s area-based target, the World Database on Protected Areas, assumes that all reported protected areas have biodiversity conservation as a main objective. But some CBD parties report areas that have other primary objectives, such as sustainable harvesting20. This leads to inaccurate accounting at the global level, and to misunderstanding of management actually occurring on the ground. Canada, among others, is developing legislation that demarcates protected areas and OECMs. But it is not clear whether all CBD parties will do the same.Policymakers need to agree on targets that are based on outcomes — not just coverage — for both OECMs and protected areas. These might include, for example, changes in the populations of multiple species relative to a reference point. In constructing these targets, the conservation community should be guided by the development and health sectors, which have long used outcome targets. For example, the United Nations Sustainable Development Goal 1.2 aims to reduce at least by half the proportion of people living in multidimensional, regionally-defined poverty by 2030. A common currency of outcomes could alleviate concerns that there is an uneven burden of proof for the OECM and protected-area tools. It could also prevent the misuse of either to meet targets based on area without actually sustaining biodiversity.Include OECMs in other environmental agreements. Addressing the interrelated global challenges of biodiversity loss, climate change and sustainability requires the coordination of policy across sectors. Right now, OECMs appear only in CBD policy. But they could contribute to the mandates of other intergovernmental initiatives. Policymakers should include OECMs alongside protected areas in international agreements such as the Sustainable Development Goals, new global climate agreements being negotiated under the UN convention on climate, and the emerging UN treaty on marine biodiversity in areas beyond national jurisdiction.New targets negotiated at the upcoming CBD meeting will set the global conservation agenda over the next decade. If the steps we outline here are implemented, OECMs could be central to the transformations needed for a sustainable future for the planet.

    Nature 595, 646-649 (2021)
    doi: https://doi.org/10.1038/d41586-021-02041-4

    References1.Oldekop, J. A., Holmes, G., Harris, W. E. & Evans, K. L. Conserv. Biol. 30, 133–141 (2016).PubMed 
    Article 

    Google Scholar 
    2.Lee, E. Antipode 48, 355–374 (2016).Article 

    Google Scholar 
    3.Jonas, H. D., Barbuto, V., Jonas, H. C., Kothari, A. & Nelson, F. PARKS 20, 111–128 (2014).Article 

    Google Scholar 
    4.Ellis, E. C. One Earth 1, 163–167 (2019).Article 

    Google Scholar 
    5.Donald, P. F. et al. Conserv. Lett. 12, e12659 (2019).Article 

    Google Scholar 
    6.Schleicher, J., Peres, C. A., Amano, T., Llactayo, W. & Leader-Williams, N. Sci. Rep. 7, 11318 (2017).PubMed 
    Article 

    Google Scholar 
    7.Gelcich, S., Martínez-Harms, M. J., Tapia-Lewin, S., Vasquez-Lavin, F. & Ruano-Chamorro, C. Conserv. Lett. 12, e12637 (2019).Article 

    Google Scholar 
    8.Lomba, A. et al. Front. Ecol. Environ. 18, 36–42 (2020).Article 

    Google Scholar 
    9.Poudyal, M. et al. PeerJ 6,e5106 (2018).PubMed 
    Article 

    Google Scholar 
    10.Garnett, S. T. et al. Nature Sustain. 1, 369–374 (2018).Article 

    Google Scholar 
    11.Ansell, J. et al. Int. J. Wildland Fire 29, 371–385 (2019).Article 

    Google Scholar 
    12.Corson, C. et al. Conserv. Soc. 12, 190–202 (2014).Article 

    Google Scholar 
    13.Hilborn, R. Nature 535, 224–226 (2016).PubMed 
    Article 

    Google Scholar 
    14.Carlisle, K. & Gruby, R. L. Policy Stud. J. 47, 927–952 (2019).Article 

    Google Scholar 
    15.Thiault, L. et al. Ecosphere 10, e02576 (2019).Article 

    Google Scholar 
    16.Kincaid, K. & Rose, G. Can. J. Fish. Aqua. Sci. 74, 1490–1502 (2017).Article 

    Google Scholar 
    17.Lemieux, C. J. & Gray, P. A. J. Environ. Stud. Sci. 10, 483–491 (2020).Article 

    Google Scholar 
    18.Geldmann, J. et al. Conserv. Lett. https://doi.org/10.1111/conl.12792 (2021).Article 

    Google Scholar 
    19.Gurney, G. G. et al. Biol. Conserv. 240, 108298 (2019).Article 

    Google Scholar 
    20.Govan, H. & Jupiter, S. PARKS 19, 73–80 (2013).Article 

    Google Scholar 
    Download references

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    Niche partitioning among dead wood-dependent beetles

    1.Polechová, J. & Storch, D. Ecological niche. Encycl. Ecol. 2, 1088–1097 (2008).
    Google Scholar 
    2.Vannette, R. L. & Fukami, T. Historical contingency in species interactions: Towards niche-based predictions. Ecol. Lett. 17, 115–124 (2014).PubMed 
    Article 

    Google Scholar 
    3.Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton University Press, 2011).Book 

    Google Scholar 
    4.Clark, J. S. The coherence problem with the unified neutral theory of biodiversity. Trends Ecol. Evol. 27, 198–202 (2012).PubMed 
    Article 

    Google Scholar 
    5.McGill, B. J. A test of the unified neutral theory of biodiversity. Nature 422, 881–885 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Bocci, A. et al. Sympatric snow leopards and Tibetan wolves: Coexistence of large carnivores with human-driven potential competition. Eur. J. Wildl. Res. 63, 92 (2017).Article 

    Google Scholar 
    7.Dueser, R. D. & Shuggart, H. H. Niche pattern in a forest-floor small-mammal fauna. Ecology 60, 108–118 (1979).Article 

    Google Scholar 
    8.Cloyed, C. S. & Eason, P. K. Niche partitioning and the role of intraspecific niche variation in structuring a guild of generalist anurans. R. Soc. Open Sci. 4, 170060 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Armstrong, R. A. & McGehee, R. Coexistence of species competing for shared resources. Theor. Popul. Biol. 9, 317–328 (1976).MathSciNet 
    CAS 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    10.Paillet, Y. et al. The indicator side of tree microhabitats: A multi-taxon approach based on bats, birds and saproxylic beetles. J. Appl. Ecol. 55, 2147–2159 (2018).Article 

    Google Scholar 
    11.Kadowaki, K. Species coexistence patterns in a mycophagous insect community inhabiting the wood-decaying bracket fungus Cryptoporus volvatus (Polyporaceae: Basidiomycota). Eur. J. Entomol. 107, 89 (2010).Article 

    Google Scholar 
    12.Peter, A.-K. Survival in adults of the water frog Rana lessonae and its hybridogenetic associate Rana esculenta. Can. J. Zool. 79, 652–661 (2001).Article 

    Google Scholar 
    13.Borkowski, A. & Skrzecz, I. Ecological segregation of bark beetle (Coleoptera, Curculionidae, Scolytinae) infested Scots pine. Ecol. Res. 31, 135–144 (2016).Article 

    Google Scholar 
    14.Bobiec, A., Gutowski, J. M. & Laudenslayer, W. F. The Afterlife of a Tree (WWF Poland, 2005).
    Google Scholar 
    15.Alexander, K. N. Tree biology and saproxylic Coleoptera: issues of definitions and conservation language. Rev. Ecol. 10, 9–13 (2008).
    Google Scholar 
    16.Véle, A. & Horák, J. The importance of host characteristics and canopy openness for pest management in urban forests. Urban For. Urban Green. 36, 84–89 (2018).Article 

    Google Scholar 
    17.Přikryl, Z. B., Turčáni, M. & Horák, J. Sharing the same space: Foraging behaviour of saproxylic beetles in relation to dietary components of morphologically similar larvae. Ecol. Entomol. 37, 117–123 (2012).Article 

    Google Scholar 
    18.Brin, A. & Bouget, C. Biotic interactions between saproxylic insect species. In Saproxylic insects: Diversity, ecology and conservation (ed. Ulyshen, M. D.) 471–514 (Springer, 2018).Chapter 

    Google Scholar 
    19.Stokland, J. N., Siitonen, J. & Jonsson, B. G. Biodiversity in Dead Wood (Cambridge University Press, 2012).Book 

    Google Scholar 
    20.Radchuk, V., Turlure, C. & Schtickzelle, N. Each life stage matters: The importance of assessing the response to climate change over the complete life cycle in butterflies. J. Anim. Ecol. 82, 275–285 (2013).PubMed 
    Article 

    Google Scholar 
    21.Biedermann, P. H. & Taborsky, M. Larval helpers and age polyethism in ambrosia beetles. Proc. Natl. Acad. Sci. U.S.A. 108, 17064–17069 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Hanks, L. M. Influence of the larval host plant on reproductive strategies of cerambycid beetles. Annu. Rev. Entomol. 44, 483–505 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Horak, J. What is happening after an abiotic disturbance? Response of saproxylic beetles in the Primorsky Region woodlands (Far Eastern Russia). J. Insect Conserv. 19, 97–103 (2015).Article 

    Google Scholar 
    24.Hůrka, K. Beetles of the Czech and Slovak Republics (Kabourek, 2005).
    Google Scholar 
    25.Horák, J. & Chobot, K. Phenology and notes on the behaviour of Cucujus cinnaberinus: Points for understanding the conservation of the saproxylic beetle. North-West. J. Zool. 7, 352–355 (2011).
    Google Scholar 
    26.Finke, D. L. & Snyder, W. E. Niche partitioning increases resource exploitation by diverse communities. Science 321, 1488–1490 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    27.Crowson, R. Observations on Dendrophagus crenatus (Paykull)(Cucujidae) and some comparisons with piestine Staphylinidae (Coleoptera). Entomol. Mon. Mag. 104, 161–169 (1969).
    Google Scholar 
    28.Tarno, H. et al. The behavioral role of males of platypus quercivorus murayama in their subsocial colonies. Agrivita 38, 47–54 (2016).
    Google Scholar 
    29.Della Rocca, F. & Milanesi, P. Combining climate, land use change and dispersal to predict the distribution of endangered species with limited vagility. J. Biogeogr. 47, 1427–1438 (2020).Article 

    Google Scholar 
    30.Buse, J. “Ghosts of the past”: flightless saproxylic weevils (Coleoptera: Curculionidae) are relict species in ancient woodlands. J. Insect Conserv. 16, 93–102 (2012).Article 

    Google Scholar 
    31.Røed, K. H. et al. Isolation and characterization of ten microsatellite loci for the wood-living and threatened beetle Cucujus cinnaberinus (Coleoptera: Cucujidae). Conserv. Genet. Resour. 6, 641–643 (2014).Article 

    Google Scholar 
    32.Konvicka, M., Hula, V. & Fric, Z. Habitat of pre-hibernating larvae of the endangered butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae): What can be learned from vegetation composition and architecture?. Eur. J. Entomol. 100, 313–322 (2003).Article 

    Google Scholar 
    33.Bonacci, T. et al. Artificial feeding and laboratory rearing of endangered saproxylic beetles as a tool for insect conservation. J. Insect Sci. 20, 20 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Mazzei, A. et al. Rediscovering the ‘umbrella species’ candidate Cucujus cinnaberinus (Scopoli, 1763) in Southern Italy (Coleoptera Cucujidae), and notes on bionomy. Ital. J. Zool. 78, 264–270 (2011).Article 

    Google Scholar 
    35.Horák, J., Chumanová, E. & Chobot, K. Habitat preferences influencing populations, distribution and conservation of the endangered saproxylic beetle Cucujus cinnaberinus (Coleoptera: Cucujidae) at the landscape level. Eur. J. Entomol. 107, 81–88 (2010).Article 

    Google Scholar 
    36.Hardin, G. The competitive exclusion principle. Science 131, 1292–1297 (1960).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Carmel, Y. et al. Using exclusion rate to unify niche and neutral perspectives on coexistence. Oikos 126, 1451–1458 (2017).Article 

    Google Scholar 
    38.Horák, J., Chumanová, E. & Hilszczański, J. Saproxylic beetle thrives on the openness in management: a case study on the ecological requirements of Cucujus cinnaberinus from Central Europe. Insect Conserv. Divers. 5, 403–413 (2012).Article 

    Google Scholar 
    39.Keddy, P. Competiton 2nd edn. (Springer, 2001).Book 

    Google Scholar 
    40.Bonacci, T. et al. Beetles “in red”: are the endangered flat bark beetles Cucujus cinnaberinus and C. haematodes chemically protected? (Coleoptera: Cucujidae). Eur. Zool. J. 85, 128–136 (2018).Article 
    CAS 

    Google Scholar 
    41.Chararas, C., Chipoulet, J. M. & Courtois, J. E. Purification partielle et caracterisation d’une beta-glucosidase des larves de Pyrochroa coccinea (Coleoptere, Pyrochroidae). C. R. Séances Soc. Biol. Fil. 1771, 22–27 (1983).
    Google Scholar 
    42.Dettner, K. Description of defensive glands from cardinal beetles (Coleoptera, Pyrochroidae)—their phylogenetic significance as compared with other heteromeran defensive glands. Entomol. Basil. 9, 204–215 (1984).
    Google Scholar 
    43.Nardi, G. & Bologna, M. Cantharidin attraction in Pyrochroa (Coleoptera: Pyrochroidae). Entomol. News 111, 74–75 (2000).
    Google Scholar 
    44.Hirzel, A. & Guisan, A. Which is the optimal sampling strategy for habitat suitability modelling. Ecol. Model. 157, 331–341 (2002).Article 

    Google Scholar 
    45.Jaworski, T. et al. Saproxylic moths reveal complex within-group and group-environment patterns. J. Insect Conserv. 20, 677–690 (2016).Article 

    Google Scholar 
    46.Gotelli, N. J., Hart, E. M. & Ellison, A. M. EcoSimR: Null Model Analysis for Ecologicaldata. R package version 0.1.0 (Zenodo, 2015).47.Heiberger, R. M. HH: Statistical Analysis and Data Display: Heiberger and Holland. https://CRAN.R-project.org/package=HH (2020).48.Walsh, C. & Mac Nally, R. M. Hier.Part: Hierarchical partitioning. https://cran.r-project.org/web/packages/hier.part/index.html (2020). More