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    Long-term application of fertilizer and manures affect P fractions in Mollisol

    Total P and available P
    Fertilizer application significantly (P  0.05). The highest increase in available P concentration in NPK + S treatment observed in the 60–100 cm soil depth, with the increase of 111% and 115% in 60–80 cm and 80–100 cm soil depths, respectively, over CK treatment.
    Figure 2

    Effect of long-term application of chemical fertilizer, organic manure, and straw on total phosphorus (P) and available P concentrations. * indicates significant difference at P  3.6%) was associated with OM treatment, especially at the 0–20 and 20–40 cm soil depths (Fig. 3). The PAC values under NPK, NPK + S and OM treatments increased by 7.6%, 4.5% and 11.5% in the 0–20 cm soil depth and 4.2%, 1.3%, and 5.8% in 20–40 cm soil depth, respectively as compared to the CK treatment. However, PAC value for soil depth below 40 cm showed the trend, NPK  More

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    A recipe to reverse the loss of nature

    NEWS AND VIEWS
    09 September 2020

    How can the decline in global biodiversity be reversed, given the need to supply food? Computer modelling provides a way to assess the effectiveness of combining various conservation and food-system interventions to tackle this issue.

    Brett A. Bryan &

    Brett A. Bryan is at the Centre for Integrative Ecology, Deakin University, Melbourne, Victoria 3125, Australia.
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    Carla L. Archibald

    Carla L. Archibald is at the Centre for Integrative Ecology, Deakin University, Melbourne, Victoria 3125, Australia.

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    Nature is in trouble, and its plight will probably become even more precarious unless we do something about it1. Writing in Nature, Leclère et al.2 quantify what might be needed to reverse this deeply worrying path while also feeding people’s increasingly voracious appetites. The authors’ answer is to team ambitious conservation measures with food-system transformation in the hope of reversing the trend of global terrestrial biodiversity loss.

    By nature, we mean the diversity of life that has evolved over billions of years to exist in dynamic balance with Earth’s biophysical environment and the ecosystems present. Nature contributes to human well-being in many ways, and the services it provides, such as carbon sequestration by plants or pollination by insects, could impose a vast cost if lost3. Although the slow and long-term decline of Earth’s biodiversity4 is often overshadowed by climate change, and more recently by the COVID-19 pandemic, the loss of biodiversity is no less of a risk than those posed by the other challenges. Many would argue that the effect of biodiversity losses could surpass the combined impacts of climate change and COVID-19.
    More and more, the realization is growing that, as a planet, we are what we eat. Human demand for food is accelerating with the ever-increasing global population (projected to approach 10 billion by 2050), and each successive generation is wealthier and consumes more resource-intensive diets than did the previous one5. Trying to balance this rapidly rising demand against the limited amount of land available for crops and pasture sets agriculture and nature (Fig. 1) on a collision course6. As Leclère and colleagues show, a bold and integrated strategy is required immediately to turn this around.

    Figure 1 | A bean field bordering a rainforest reserve near Sorriso, Brazil.Credit: Florian Plaucheur/AFP/Getty

    Taking a long view out to the year 2100, Leclère et al. present a global modelling study assessing the ability of ambitious conservation and food-system intervention scenarios to reverse the decline, or, as they call it, “bending the curve”, of biodiversity losses resulting from changes in agricultural land use and management. Projections of future land use and biodiversity are uncertain, and when these models are combined, this uncertainty is compounded. One of the great innovations of Leclère and colleagues’ work is in embracing this uncertainty by combining an ensemble of four global land-use models and eight global biodiversity models and measuring the performance of future land-use scenarios in terms of higher-level model-independent metrics such as the amount of biodiversity loss avoided.
    Importantly, the study also included a baseline (termed BASE) scenario — the world expected without interventions — and Leclère et al. used this to gauge the effectiveness of the intervention scenarios. Although it is not a focus of the paper, it’s worth pausing to ponder the sobering picture painted by this business-as-usual future largely bereft of birdsong and insect chirp.
    Choosing to act now can make a difference to nature’s plight. Most (61%) of the model combinations run by the authors indicated that implementing ambitious conservation actions led to a positive uptick in the biodiversity curve by 2050. Such conservation actions included: extending the global conservation network by establishing protected nature reserves; restoring degraded land; and basing future land-use decisions on comprehensive landscape-level conservation planning. This comprehensive conservation strategy avoids more than half (an average of 58%) of the biodiversity losses expected if nothing is done, but also leads to a hike in food prices.

    When conservation actions were teamed with a range of equally ambitious food-system interventions, the prognosis for global biodiversity in the model was improved further. Including both supply- and demand-side measures, these approaches included boosting agricultural yields, having an increasingly globalized food trade, reducing food waste by half, and the global adoption of healthy diets by halving meat consumption. These combined measures of conservation and food-systems actions avoided more than two-thirds of future biodiversity losses, with the integrated action portfolio (combining all actions) avoiding an average of 90% of future biodiversity losses. Almost all models predicted a biodiversity about-face by mid-century. These food-system measures also avoided adverse outcomes for food affordability.
    Leclère and colleagues’ work complements the current global climate-change scenario framework (tools for future planning by governments and others, including scenarios called shared socio-economic pathways, which integrate future socio-economic projections with greenhouse-gas emissions), and represents the most comprehensive incorporation of biodiversity into this scenario framing7 so far. However, a major limitation of the present study is that it does not consider the potential impact of climate change on biodiversity. This raises an internal inconsistency because, on the one hand, the baseline scenario considers land-use, social and economic changes under approximately 4 °C of global heating by 21008, yet, on the other hand, it does not consider the profound effect of warming on plant and animal populations and the ecosystems they comprise9. Also absent from the models were other threats to biodiversity, including harvesting, hunting and invasive species10. Although Leclère and colleagues recognized these limitations and assigned them a high priority for future research, unfortunately for us all, omitting these key threats probably means that the authors’ estimates of biodiversity’s plight and the effectiveness of integrated global conservation and food-system action are overly optimistic. To truly bend the curve, Leclère and colleagues’ integrated portfolio will need to be substantially expanded to address the full range of threats to biodiversity.
    Although the models say that a better future is possible, is the combination of the multiple ambitious conservation and food-system interventions considered by Leclère et al. a realistic possibility? Achieving each one of the conservation and food-system actions would require a monumental coordinated effort from all nations. And even if the global community were to get its act together in prioritizing conservation and food-system transformation, would such efforts come in time and be enough to save our planet’s natural legacy? We certainly hope so.

    doi: 10.1038/d41586-020-02502-2

    References

    1.
    Díaz, S. et al. Science 366, eaax3100 (2019).

    2.
    Leclère, D. et al. Nature https://doi.org/10.1038/s41586-020-2705-y (2020).

    3.
    Costanza, R. et al. Glob. Environ. Change Hum. Policy Dimens. 26, 152–158 (2014).

    4.
    Butchart, S. H. M. et al. Science 328, 1164–1168 (2010).

    5.
    Springmann, M. et al. Nature 562, 519–525 (2018).

    6.
    Montesino Pouzols, F. et al. Nature 516, 383–386 (2014).

    7.
    Kok, M. T. J. et al. Biol. Conserv. 221, 137–150 (2018).

    8.
    Leclère, D. et al. Towards Pathways Bending the Curve of Terrestrial Biodiversity Trends Within the 21st Century https://doi.org/10.22022/ESM/04-2018.15241 (Int. Inst. Appl. Syst. Analysis, 2018).

    9.
    Warren, R., Price, J., Graham, E., Forstenhaeusler, N. & VanDerWal, J. Science 360, 791–795 (2018).

    10.
    Driscoll, D. A. et al. Nature Ecol. Evol. 2, 775–781 (2018).

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    Canadian permafrost stores large pools of ammonium and optically distinct dissolved organic matter

    Properties of permafrost soils
    All sites contained syngenetic permafrost in which the active layer and the uppermost permafrost have experienced numerous freeze-thaw cycles since formation during the Holocene22. Permafrost organic matter radiocarbon ages ranged from 7850 ± 30 to 830 ± 20 y B.P. (Supplementary Data), with the western sites containing the oldest SOM and the northern Hudson Bay peatlands containing the youngest SOM.
    For organic layers, permafrost soil C:N atomic ratios (14.50 [12.61–19.67], median [25th–75th]) were lower and H:C atomic ratios (0.13 [0.13–0.14]) were greater relative to the active layer, 23.89 [19.33–29.50] and 0.14 [0.12–0.15], respectively (Supplementary Fig. 1). Similarly for mineral layers, permafrost C:N ratios were lower (12.0 [3.23–18.09]) and H:C ratios higher (0.24 [0.15–0.86]) compared to the active layer, 16.21 [13.67–18.87] and 0.17 [0.15–0.21], respectively. For both thermal layers, in organic layers C:N ratios were higher and H:C ratios were lower than in mineral layers.
    These stoichiometric properties are typical of boreal and tundra soils (Supplementary Fig. 1)23. The higher C:N and very low H:C ratios of the organic layers relative to mineral layers suggest higher contents of condensed aromatic structures originating from peat24. Permafrost layers displayed lower C:N properties suggesting different SOM composition (e.g., lignin, tannins, lipids, sugars or amino acids) and an enrichment in microbial biomass relative to the active layer24. The absence of a downward trend of C:N and H:C within the permafrost (Supplementary Fig. 1), except at Daring Lake, indicates that soil development and microbial processing were effectively halted soon after permafrost aggradation23.
    Active layer and permafrost yields of DOC and nitrogen
    DOC content correlated with soil C content in both active layer (r2 [log–log] = 0.748, P  More

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    Chemical pollution imposes limitations to the ecological status of European surface waters

    1.
    Hoekstra, A. Y. & Wiedmann, T. O. Humanity’s unsustainable environmental footprint. Science 344, 1114–1117. https://doi.org/10.1126/science.1248365 (2014).
    ADS  CAS  Article  PubMed  Google Scholar 
    2.
    Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 736–746. https://doi.org/10.1126/science.1259855 (2015).
    ADS  CAS  Article  Google Scholar 

    3.
    Wang, H. et al. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388, 1459–1544. https://doi.org/10.1016/S0140-6736(16)31012-1 (2016).
    Article  Google Scholar 

    4.
    Grizzetti, B. et al. Human pressures and ecological status of European rivers. Sci. Rep. 7, 205. https://doi.org/10.1038/s41598-017-00324-3 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    5.
    Hoekstra, A. Y. & Mekonnen, M. M. The water footprint of humanity. Proc. Natl. Acad. Sci. 109, 3232–3237. https://doi.org/10.1073/pnas.1109936109 (2012).
    ADS  Article  PubMed  Google Scholar 

    6.
    Vörösmarty, C. J. et al. Global threats to human water security and river biodiversity. Nature 467, 555–561. https://doi.org/10.1038/nature09440 (2010).
    ADS  CAS  Article  PubMed  Google Scholar 

    7.
    Millennium Ecosystem Assessment. Ecosystems and Human Well-being. A Framework for Assessment https://pdf.wri.org/ecosystems_human_wellbeing.pdf (2003).

    8.
    Carpenter, S. R., Stanley, E. H. & Vander Zanden, M. J. State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annu. Rev. Environ. Resour. 36, 75–99. https://doi.org/10.1146/annurev-environ-021810-094524 (2011).
    Article  Google Scholar 

    9.
    Richmond, E. K. et al. A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nat. Commun. 9, 4491. https://doi.org/10.1038/s41467-018-06822-w (2018).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    10.
    Maes, J. et al. An indicator framework for assessing ecosystem services in support of the EU Biodiversity Strategy to 2020. Ecosyst. Serv. 17, 14–23. https://doi.org/10.1016/j.ecoser.2015.10.023 (2016).
    Article  Google Scholar 

    11.
    Anzaldua, G. et al. Getting into the water with the ecosystem services approach: the DESSIN ESS evaluation framework. Ecosyst. Serv. 30, 318–326. https://doi.org/10.1016/j.ecoser.2017.12.004 (2018).
    Article  Google Scholar 

    12.
    Van Vliet, M. T. H., Florke, M. & Wada, Y. Quality matters for water scarcity. Nat. Geosci. 10, 800–802. https://doi.org/10.1038/NGEO3047 (2017).
    ADS  Article  Google Scholar 

    13.
    Bernhardt, E. S., Rosi, E. J. & Gessner, M. O. Synthetic chemicals as agents of global change. Front. Ecol. Environ. 15, 84–90. https://doi.org/10.1002/fee.1450 (2017).
    Article  Google Scholar 

    14.
    Global Chemicals Outlook II—from legacies to innovative solutions: implementing the 2030 agenda for sustainable development. Synthesis report https://wedocs.unep.org/bitstream/handle/20.500.11822/28113/GCOII.pdf?sequence=1&isAllowed=y (2019).

    15.
    Birk, S. et al. Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-020-1216-4 (2020).
    Article  PubMed  Google Scholar 

    16.
    A guide to SDG interactions. From sciene to implementation https://council.science/publications/a-guide-to-sdg-interactions-from-science-to-implementation/ (2017).

    17.
    EC. Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH). Off. J. Eur. Union L 396, 1–848 https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02006R01907-20140410&from=EN (2006).

    18.
    Geiser, K. Chemicals Without Harm. Policies for a Sustainable World (MIT Press, Cambridge, 2015).
    Google Scholar 

    19.
    Escher, B. I., Stapleton, H. M. & Schymanski, E. L. Tracking complex mixtures of chemicals in our changing environment. Science 367, 388–392. https://doi.org/10.1126/science.aay6636 (2020).
    ADS  CAS  Article  PubMed  Google Scholar 

    20.
    UNESCO. Solving the puzzle: the ecosystem approach and biosphere reserves https://unesdoc.unesco.org/ark:/48223/pf0000119790 (2000).

    21.
    Nõges, P., van de Bund, W., Cardoso, A. C., Solimini, A. G. & Heiskanen, A. S. Assessment of the ecological status of European surface waters: a work in progress. Hydrobiologia 633, 197–211. https://doi.org/10.1007/s10750-009-9883-9 (2009).
    CAS  Article  Google Scholar 

    22.
    Tsakiris, G. The status of the European waters in 2015: a review. Environ. Process. 2, 543–557. https://doi.org/10.1007/s40710-015-0079-1 (2015).
    Article  Google Scholar 

    23.
    Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Off. J. Eur. Commun. L 327, 1–72 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ:L:2000:2327:TOC (2000).

    24.
    Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674. https://doi.org/10.1038/s41586-019-1684-3 (2019).
    ADS  CAS  Article  PubMed  Google Scholar 

    25.
    Rockström, J. et al. A safe operating space for humanity. Nature 461, 472–475. https://doi.org/10.1038/461472a (2009).
    ADS  CAS  Article  PubMed  Google Scholar 

    26.
    Clean Water Rule: Definition of “Waters of the United States”. Federal Register 80, 37054–37127, Monday, June 29, 2015/Rules https://www.govinfo.gov/content/pkg/FR-2015-06-29/pdf/2015-13435.pdf (2015).

    27.
    C&L Inventory. Database containing classification and labelling information on notified and registered substances received from manufacturers and importers https://echa.europa.eu/information-on-chemicals/cl-inventory-database (accessed March 4, 2019) (2019).

    28.
    Posthuma, L., de Zwart, D. & Dyer, S. D. Chemical mixtures affect freshwater species assemblages: from problems to solutions. Curr. Opin. Environ. Sci. Health 11, 78–89. https://doi.org/10.1016/j.coesh.2019.09.002 (2019).
    Article  Google Scholar 

    29.
    The Water Framework Directive and the Floods Directive: Actions towards the ‘good status’ of EU water and to reduce flood risks. Communication from the Commission to the European Parliament and the Council, 9.3.2015. COM(2015) 120 final https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A52015DC0120 (2015).

    30.
    EC. Fitness check of the Water Framework Directive, Groundwater Directive, Environmental Quality Standards Directive and Floods Directive https://ec.europa.eu/environment/water/fitness_check_of_the_eu_water_legislation/documents/Water%20Fitness%20Check%20-%20SWD(2019)439%20-%20web.pdf. 1–176 (2019).

    31.
    Arle, J., Mohaupt, V. & Kirst, I. Monitoring of surface waters in Germany under the Water Framework Directive—a review of approaches, methods and results. Water 8, 217. https://doi.org/10.3390/w8060217 (2016).
    Article  Google Scholar 

    32.
    Drakvik, E. et al. Statement paper on advancing the assessment of chemical mixtures and their risks for human health and the environment. Environ. Int. 134, 105267. https://doi.org/10.1016/j.envint.2019.105267 (2020).
    CAS  Article  PubMed  Google Scholar 

    33.
    Brack, W. et al. High-resolution mass spectrometry to complement monitoring and track emerging chemicals and pollution trends in European water resources. Environ. Sci. Eur. 31, 62. https://doi.org/10.1186/s12302-019-0230-0 (2019).
    Article  Google Scholar 

    34.
    Van Gils, J. et al. The European Collaborative Project SOLUTIONS developed models to provide diagnostic and prognostic capacity and fill data gaps for chemicals of emerging concern. Environ. Sci. Eur. 31, 72. https://doi.org/10.1186/s12302-019-0248-3 (2019).
    Article  Google Scholar 

    35.
    van Gils, J. et al. Computational material flow analysis for thousands of chemicals of emerging concern in European waters. J. Hazard. Mater. https://doi.org/10.1016/j.jhazmat.2020.122655 (2020).
    Article  PubMed  Google Scholar 

    36.
    Pistocchi, A. et al. Assessment of the effectiveness of reported Water Framework Directive Programmes of Measures. Part III—JRC Pressure Indicators v.2.0: nutrients, urban runoff, flow regime and hydromorphological alteration https://doi.org/10.2760/325451 (2018).

    37.
    EC. Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Off. J. Eur. Union L 226, 1–17 https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:2226:0001:0017:EN:PDF (2013).

    38.
    EEA. European waters—assessment of status and pressures https://www.eea.europa.eu/publications/state-of-water (2018).

    39.
    Dulio, V. et al. Emerging pollutants in the EU: 10 years of NORMAN in support of environmental policies and regulations. Environ. Sci. Eur. 30, 5. https://doi.org/10.1186/s12302-018-0135-3 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    40.
    Guidelines for the health risk assessment of chemical mixtures Fed. Reg. 51 185, 34014–34025 https://www.epa.gov/sites/production/files/32014-34011/documents/chem_mix_31986.pdf (1986).

    41.
    Calamari, D. & Vighi, M. A proposal to define quality objectives for aquatic life for mixtures of chemical substances. Chemosphere 25, 531–542. https://doi.org/10.1016/0045-6535(92)90285-Y (1992).
    ADS  Article  Google Scholar 

    42.
    Technical guidance for deriving environmental quality standards. Common Implementation Strategy for the Water framework Directive (2000/60/EC)—Guidance Document No. 27 https://circabc.europa.eu/sd/a/ba6810cd-e611-4f72-9902-f0d8867a2a6b/Guidance%20No%2027%20-%20Deriving%20Environmental%20Quality%20Standards%20-%20version%202018.pdf (2011).

    43.
    Posthuma, L. & De Zwart, D. Encyclopedia of Toxicology 3rd edn, Vol. 4, 363–368 (Elsevier Inc., Academic Press, 2014).
    Google Scholar 

    44.
    Birk, S. et al. Three hundred ways to assess Europe’s surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol. Ind. 18, 31–41. https://doi.org/10.1016/j.ecolind.2011.10.009 (2012).
    Article  Google Scholar 

    45.
    De Zwart, D. & Posthuma, L. Complex mixture toxicity for single and multiple species: proposed methodologies. Environ. Toxicol. Chem. 24, 2665–2676. https://doi.org/10.1897/04-639r.1 (2005).
    Article  PubMed  Google Scholar 

    46.
    Lyche Solheim, A. et al. A new broad typology for rivers and lakes in Europe: Development and application for large-scale environmental assessments. Sci. Total Environ. 697, 134043. https://doi.org/10.1016/j.scitotenv.2019.134043 (2019).
    ADS  CAS  Article  Google Scholar 

    47.
    Cade, B. S. & Noon, B. R. A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1, 412–420 https://www.jstor.org/stable/3868138 (2003).

    48.
    Vermeulen, R., Schymanski, E. L., Barabási, A.-L. & Miller, G. W. The exposome and health: where chemistry meets biology. Science 367, 392–396. https://doi.org/10.1126/science.aay3164 (2020).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    49.
    Posthuma, L., van Gils, J., Zijp, M. C., van de Meent, D. & de Zwart, D. Species sensitivity distributions for use in environmental protection, assessment, and management of aquatic ecosystems for 12 386 chemicals. Environ. Toxicol. Chem. 38, 905–917. https://doi.org/10.1002/etc.4373 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    50.
    Hoondert, R. P. J., Oldenkamp, R., de Zwart, D., van de Meent, D. & Posthuma, L. QSAR-based estimation of Species Sensitivity Distribution parameters: an exploratory investigation. Environ. Toxicol. Chem. 38, 2764–2770. https://doi.org/10.1002/etc.4601 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    51.
    Williams, A. J. et al. The CompTox Chemistry Dashboard: a community data resource for environmental chemistry. J. Chem. Inform. 9, 61. https://doi.org/10.1186/s13321-017-0247-6 (2017).
    CAS  Article  Google Scholar 

    52.
    Blum, C. et al. The concept of sustainable chemistry: key drivers for the transition towards sustainable development. Sustain. Chem. Pharm. 5, 94–104. https://doi.org/10.1016/j.scp.2017.01.001 (2017).
    CAS  Article  Google Scholar 

    53.
    Kostal, J., Voutchkova-Kostal, A., Anastas, P. T. & Zimmerman, J. B. Identifying and designing chemicals with minimal acute aquatic toxicity. Proc. Natl. Acad. Sci. U.S.A. 112, 6289–6294. https://doi.org/10.1073/pnas.1314991111 (2015).
    ADS  CAS  Article  PubMed  Google Scholar 

    54.
    Saouter, E. et al. Environmental footprint: update of Life Cycle Impact Assessment methods—ecotoxicity freshwater, human toxicity cancer, and non-cancer https://doi.org/10.2760/178544 (2018).

    55.
    Rapport, D. & Friend, A. Towards a comprehensive framework for environmental statistics. A stress-response approach https://www.worldcat.org/title/towards-a-comprehensive-framework-for-environmental-statistics-a-stress-response-approach/oclc/21772350 (1979).

    56.
    Kaika, M. & Page, B. The EU Water Framework Directive: part 1. European policy-making and the changing topography of lobbying. Eur. Environ. 13, 314–327. https://doi.org/10.1002/eet.331 (2003).
    Article  Google Scholar 

    57.
    Page, B. & Kaika, M. The EU Water Framework Directive: part 2. Policy innovation and the shifting choreography of governance. Eur. Environ. 13, 328–343. https://doi.org/10.1002/eet.332 (2003).
    Article  Google Scholar 

    58.
    Elosegi, A., Gessner, M. O. & Young, R. G. River doctors: learning from medicine to improve ecosystem management. Sci. Total Environ. 595, 294–302. https://doi.org/10.1016/j.scitotenv.2017.03.188 (2017).
    ADS  CAS  Article  PubMed  Google Scholar 

    59.
    Kortenkamp, A. & Faust, M. Regulate to reduce chemical mixture risk. Science 361, 224–226. https://doi.org/10.1126/science.aat9219 (2018).
    ADS  CAS  Article  PubMed  Google Scholar 

    60.
    Voulvoulis, N., Arpon, K. D. & Giakoumis, T. The EU Water Framework Directive: from great expectations to problems with implementation. Sci. Total Environ. 575, 358–366. https://doi.org/10.1016/j.scitotenv.2016.09.228 (2017).
    ADS  CAS  Article  PubMed  Google Scholar 

    61.
    Giakoumis, T. & Voulvoulis, N. The transition of EU water policy towards the Water Framework Directive’s integrated river basin management paradigm. Environ. Manag. 62, 819–831. https://doi.org/10.1007/s00267-018-1080-z (2018).
    ADS  Article  Google Scholar 

    62.
    Suter, G. W., Traas, T. P. & Posthuma, L. In Species Sensitivity Distributions in Ecotoxicology, Ch 21 (eds Posthuma, L. et al.) 437–474 (CRC Press, Boca Raton, 2002).
    Google Scholar 

    63.
    Kortenkamp, A. et al. Common assessment framework for HRA and ERA higher tier assessments including fish and drinking water and multi-species ERA via SSD, population-level ERA via IBM and food web vulnerability ERA. SOLUTIONS Deliverable D18.1 https://www.solutions-project.eu/wp-content/uploads/2018/11/D18.1_SOLUTIONS-D18_1-after-peer-review-clean-V2_Kortenkamp_chm_with_annex.pdf (2018).

    64.
    Posthuma, L., De Zwart, D., Keijzers, R. & Postma, J. Water systems analysis with the ecological key factor ‘toxicity’. Part 2. Calibration. Toxic pressure and ecological effects on macrofauna in the Netherlands (in Dutch) https://www.stowa.nl/sites/default/files/assets/PUBLICATIES/Publicaties%202016/STOWA%202016-15/STOWA%202016-15B.pdf (STOWA, Amersfoort, the Netherlands, 2016).

    65.
    Posthuma, L. & De Zwart, D. Predicted effects of toxicant mixtures are confirmed by changes in fish species assemblages in Ohio, USA, rivers. Environ. Toxicol. Chem. 25, 1094–1105. https://doi.org/10.1897/05-305r.1 (2006).
    CAS  Article  PubMed  Google Scholar 

    66.
    Posthuma, L. & De Zwart, D. Predicted mixture toxic pressure relates to observed fraction of benthic macrofauna species impacted by contaminant mixtures. Environ. Toxicol. Chem. 31, 2175–2188. https://doi.org/10.1002/etc.1923 (2012).
    CAS  Article  PubMed  Google Scholar 

    67.
    Berger, E., Haase, P., Oetken, M. & Sundermann, A. Field data reveal low critical chemical concentrations for river benthic invertebrates. Sci. Total Environ. 544, 864–873. https://doi.org/10.1016/j.scitotenv.2015.12.006 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    68.
    Posthuma, L. et al. Mixtures of chemicals are important drivers of impacts on ecological status in European surface waters. Environ. Sci. Eur. 31, 71. https://doi.org/10.1186/s12302-019-0247-4 (2019).
    Article  Google Scholar 

    69.
    Zijp, M. C., Posthuma, L. & Van de Meent, D. Definition and applications of a versatile chemical pollution footprint methodology. Environ. Sci. Technol. 48, 10588–10597. https://doi.org/10.1021/es500629f (2014).
    ADS  CAS  Article  PubMed  Google Scholar 

    70.
    Bjørn, A., Diamond, M., Birkved, M. & Hauschild, M. Z. Chemical footprint method for improved communication of freshwater ecotoxicity impacts in the context of ecological limits. Environ. Sci. Technol. 48, 13253–13262. https://doi.org/10.1021/es503797d (2014).
    ADS  CAS  Article  PubMed  Google Scholar 

    71.
    Kapo, K. E. et al. iSTREEM®: an approach for broad-scale in-stream exposure assessment of “down-the-drain” chemicals. Integr. Environ. Assess. Manag. 12, 782–792. https://doi.org/10.1002/ieam.1793 (2016).
    Article  PubMed  Google Scholar 

    72.
    Donnelly, C., Arheimer, B., Capell, R., Dahne, J. & Stromqvist, J. Regional overview of nutrient load in Europe—challenges when using a large-scale model approach, E-HYPE. Understanding fresh-water quality problems in a changing world https://iahs.info/uploads/dms/15569.361%2049-58.pdf (2013).

    73.
    Posthuma, L., Suter, G. W. I. & Traas, T. P. Species Sensitivity Distributions in Ecotoxicology (CRC-Press, Boca Raton, 2002).
    Google Scholar 

    74.
    Drescher, K. & Bödeker, W. Assessment of the combined effects of substances—the relationship between concentration addition and independent action. Biometrics 51, 716–730. https://doi.org/10.2307/2532957 (1995).
    MathSciNet  Article  MATH  Google Scholar 

    75.
    EEA. WISE WFD database at https://www.eea.europa.eu/data-and-maps/data/wise-wfd-3 (2012).

    76.
    Globevnik, L., Koprivsek, M. & Snoj, L. Metadata to the MARS spatial database. Freshw. Metadata J. 21, 1–7. https://doi.org/10.15504/fmj.2017.21 (2017).
    Article  Google Scholar 

    77.
    Birk, S. et al. Intercalibrating classifications of ecological status: Europe’s quest for common management objectives for aquatic ecosystems. Sci. Total Environ. 454–455, 490–499. https://doi.org/10.1016/j.scitotenv.2013.03.037 (2013).
    ADS  CAS  Article  PubMed  Google Scholar 

    78.
    Zijp, M. C., Huijbregts, M. A. J., Schipper, A. M., Mulder, C. & Posthuma, L. Identification and ranking of environmental threats with ecosystem vulnerability distributions. Sci. Rep. 7, 9298. https://doi.org/10.1038/s41598-017-09573-8 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar  More

  • in

    Cropland expansion in the United States produces marginal yields at high costs to wildlife

    1.
    USDA. 2012 National Resources Inventory: Summary Report. http://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/nrcseprd396218.pdf (2015).
    2.
    U.S. EPA. Biofuels and the Environment: The Second Triennial Report to Congress. 159 (2018).

    3.
    Monfreda, C., Ramankutty, N. & Foley, J. A. Farming the planet: 2. Geographic distribution of crop areas, yields, physiological types, and net primary production in the year 2000. Glob. Biogeochem. Cycles 22, https://doi.org/10.1029/2007GB002947 (2008).

    4.
    Cassidy, E. S., West, P. C., Gerber, J. S. & Foley, J. A. Redefining agricultural yields: from tonnes to people nourished per hectare. Environ. Res. Lett. 8, 034015 (2013).
    ADS  Google Scholar 

    5.
    Spawn, S. A., Lark, T. J. & Gibbs, H. K. Carbon emissions from cropland expansion in the United States. Environ. Res. Lett. 14, 045009 (2019).
    ADS  CAS  Google Scholar 

    6.
    Yu, Z., Lu, C., Tian, H. & Canadell, J. G. Largely underestimated carbon emission from land use and land cover change in the conterminous US. Glob. Change Biol. 25, 3741–3752 (2019).

    7.
    West, P. C. et al. Trading carbon for food: Global comparison of carbon stocks vs. crop yields on agricultural land. Proc. Natl Acad. Sci. USA 107, 19645–19648 (2010).
    ADS  CAS  PubMed  Google Scholar 

    8.
    Johnson, J. A., Runge, C. F., Senauer, B., Foley, J. & Polasky, S. Global agriculture and carbon trade-offs. Proc. Natl Acad. Sci. USA 111, 12342–12347 (2014).
    ADS  CAS  PubMed  Google Scholar 

    9.
    Lark, T. J., Salmon, J. M. & Gibbs, H. K. Cropland expansion outpaces agricultural and biofuel policies in the United States. Environ. Res. Lett. 10, 044003 (2015).
    ADS  Google Scholar 

    10.
    Henwood, W. D. & TOWARD, A. Strategy for the conservation and protection of the world’s temperate grasslands. Gt. Plains Res. 20, 121–134 (2010).
    Google Scholar 

    11.
    Tollefson, J. One million species face extinction. Nature 569, 171 (2019).
    ADS  CAS  PubMed  Google Scholar 

    12.
    Díaz, S. et al. Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. https://www.ipbes.net/sites/default/files/downloads/spm_unedited_advance_for_posting_htn.pdf Advance Unedited Version (2019).

    13.
    Werling, B. P. et al. Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes. Proc. Natl Acad. Sci. USA 111, 1652–1657 (2014).
    ADS  CAS  PubMed  Google Scholar 

    14.
    Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).
    ADS  CAS  PubMed  Google Scholar 

    15.
    Meehan, T. D., Hurlbert, A. H. & Gratton, C. Bird communities in future bioenergy landscapes of the Upper Midwest. Proc. Natl Acad. Sci. USA 107, 18533–18538 (2010).
    ADS  CAS  PubMed  Google Scholar 

    16.
    Thogmartin, W. E. et al. Restoring monarch butterfly habitat in the Midwestern US: ‘all hands on deck’. Environ. Res. Lett. 12, 074005 (2017).
    ADS  Google Scholar 

    17.
    Smith, G. W. A Critical Review of the Aerial and Ground Surveys of Breeding Waterfowl in North America. https://apps.dtic.mil/docs/citations/ADA322667 (1995).

    18.
    Bakker, K. K. & Higgins, K. F. Planted grasslands and native sod prairie: equivalent habitat for grassland birds? West. North Am. Nat. 69, 235–242 (2009).
    Google Scholar 

    19.
    Dodds, W. K. et al. Comparing ecosystem goods and services provided by restored and native lands. BioScience 58, 837–845 (2008).
    Google Scholar 

    20.
    Lark, T. J., Larson, B., Schelly, I., Batish, S. & Gibbs, H. K. Accelerated conversion of native prairie to cropland in Minnesota. Environ. Conserv. 1–8 https://doi.org/10.1017/S0376892918000437 (2019).

    21.
    Wimberly, M. C. et al. Cropland expansion and grassland loss in the eastern Dakotas: New insights from a farm-level survey. Land Use Policy 63, 160–173 (2017).
    Google Scholar 

    22.
    Boryan, C., Yang, Z., Mueller, R. & Craig, M. Monitoring US agriculture: the US Department of Agriculture, National Agricultural Statistics Service, Cropland Data Layer Program. Geocarto Int. 26, 341–358 (2011).
    Google Scholar 

    23.
    Caro, T. Conservation by Proxy: Indicator, Umbrella, Keystone, Flagship, and Other Surrogate Species (Island Press, 2010).

    24.
    Yu, Z. & Lu, C. Historical cropland expansion and abandonment in the continental U.S. during 1850 to 2016. Glob. Ecol. Biogeogr. 27, 322–333 (2018).
    MathSciNet  Google Scholar 

    25.
    Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191 (2018).
    PubMed  PubMed Central  Google Scholar 

    26.
    Haan, N. L. & Landis, D. A. The importance of shifting disturbance regimes in monarch butterfly decline and recovery. Front. Ecol. Evol. 7, 191 (2019).

    27.
    Lukens, L. et al. Monarch habitat in conservation grasslands. Front. Ecol. Evol. 8, 13 (2020).

    28.
    Reynolds, R. E., Shaffer, T. L., Loesch, C. R. & Cox, R. R. The farm bill and duck production in the prairie pothole region: increasing the benefits. Wildl. Soc. Bull. 34, 963–974 (2006).
    Google Scholar 

    29.
    Walker, J. et al. An integrated strategy for grassland easement acquisition in the Prairie Pothole Region, USA. J. Fish. Wildl. Manag. 4, 267–279 (2013).
    Google Scholar 

    30.
    USDA, N. 2017 Census of Agriculture. https://www.nass.usda.gov/Publications/AgCensus/2017/index.php#full_report (2019).

    31.
    USDA. 2015 National Resources Inventory: Summary Report. http://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/nrcseprd396218.pdf (2018).

    32.
    Yang, L. et al. A new generation of the United States National Land Cover Database: Requirements, research priorities, design, and implementation strategies. ISPRS J. Photogramm. Remote Sens. 146, 108–123 (2018).
    ADS  Google Scholar 

    33.
    Estel, S. et al. Mapping farmland abandonment and recultivation across Europe using MODIS NDVI time series. Remote Sens. Environ. 163, 312–325 (2015).
    ADS  Google Scholar 

    34.
    Yin, H. et al. Mapping agricultural land abandonment from spatial and temporal segmentation of Landsat time series. Remote Sens. Environ. 210, 12–24 (2018).
    ADS  Google Scholar 

    35.
    Yin, H. et al. Monitoring cropland abandonment with Landsat time series. Remote Sens. Environ. 246, 111873 (2020).
    ADS  Google Scholar 

    36.
    Anderson, J. R. A Land Use and Land Cover Classification System for Use with Remote Sensor Data (U.S. Government Printing Office, 1976).

    37.
    Rogan, J. et al. Land-cover change monitoring with classification trees using landsat TM and ancillary data. Photogramm. Eng. Rem. Sensing 69, 793–804 (2003).

    38.
    Johnson, D. M. An assessment of pre- and within-season remotely sensed variables for forecasting corn and soybean yields in the United States. Remote Sens. Environ. 141, 116–128 (2014).
    ADS  Google Scholar 

    39.
    Kukal, M. S. & Irmak, S. U.S. agro-climate in 20th century: growing degree days, first and last frost, growing season length, and impacts on crop yields. Sci. Rep. 8, 1–14 (2018).
    ADS  Google Scholar 

    40.
    Ramankutty, N., Foley, J. A., Norman, J. & McSweeney, K. The global distribution of cultivable lands: current patterns and sensitivity to possible climate change. Glob. Ecol. Biogeogr. 11, 377–392 (2002).
    Google Scholar 

    41.
    Lubowski, R. N. et al. Environmental Effects of Agricultural Land-use Change: The Role of Economics and Policy https://doi.org/10.22004/ag.econ.33591 (2006).

    42.
    Hendricks, N. P. & Er, E. Changes in cropland area in the United States and the role of CRP. Food Policy 75, 15–23 (2018).
    Google Scholar 

    43.
    Alonso, W. Location and land use. Toward a general theory of land rent. Locat. Land Use Gen. Theory Land Rent 204 (1964).

    44.
    Wimberly, M. C., Narem, D. M., Bauman, P. J., Carlson, B. T. & Ahlering, M. A. Grassland connectivity in fragmented agricultural landscapes of the north-central United States. Biol. Conserv. 217, 121–130 (2018).
    Google Scholar 

    45.
    Bennett, A. F. Linkages in the Landscape: The Role of Corridors and Connectivity in Wildlife Conservation (Iucn, 1999).

    46.
    Helms, D. Readings in the History of the Soil Conservation Service, Washington, DC. Read. Hist. Soil Conserv. Serv. 60–73 https://www.nrcs.usda.gov/wps/portal/nrcs/detail/national/about/history/?cid=nrcs143_021436 (1992).

    47.
    Abubakar, M. S., Ahmad, D. & Akande, F. B. A review of farm tractor overturning accidents and safety. Pertanika J. Sci. Technol. 18, 377–385 (2010).
    Google Scholar 

    48.
    Xie, Y., Lark, T. J., Brown, J. F. & Gibbs, H. K. Mapping irrigated cropland extent across the conterminous United States at 30 m resolution using a semi-automatic training approach on Google Earth Engine. ISPRS J. Photogramm. Remote Sens. 155, 136–149 (2019).
    ADS  Google Scholar 

    49.
    Scanlon, B. R. et al. Groundwater depletion and sustainability of irrigation in the US High Plains and Central Valley. Proc. Natl Acad. Sci. USA 109, 9320–9325 (2012).
    ADS  CAS  PubMed  Google Scholar 

    50.
    Oberhauser, K. & Guiney, M. Insects as flagship conservation species. Terr. Arthropod. Rev. 1, 111–123 (2009).
    Google Scholar 

    51.
    Gustafsson, K. M., Agrawal, A. A., Lewenstein, B. V. & Wolf, S. A. The monarch butterfly through time and space: the social construction of an icon. BioScience 65, 612–622 (2015).
    Google Scholar 

    52.
    Pleasants, J. Milkweed restoration in the Midwest for monarch butterfly recovery: estimates of milkweeds lost, milkweeds remaining and milkweeds that must be added to increase the monarch population. Insect Conserv. Divers. https://doi.org/10.1111/icad.12198 (2016).

    53.
    Thogmartin, W. E. et al. Monarch butterfly population decline in North America: identifying the threatening processes. R. Soc. Open Sci. 4, 170760 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    54.
    Stenoien, C. et al. Monarchs in decline: a collateral landscape-level effect of modern agriculture. Insect Sci. 25, 528–541 (2018).
    PubMed  Google Scholar 

    55.
    Lipsey, M. K. et al. One step ahead of the plow: Using cropland conversion risk to guide Sprague’s Pipit conservation in the northern Great Plains. Biol. Conserv. 191, 739–749 (2015).
    Google Scholar 

    56.
    Runge, C. A. et al. Unintended habitat loss on private land from grazing restrictions on public rangelands. J. Appl. Ecol. 56, 52–62 (2019).

    57.
    Sylvester, K. M., Gutmann, M. P. & Brown, D. G. At the margins: agriculture, subsidies and the shifting fate of North America’s native grassland. Popul. Environ. 37, 362–390 (2016).
    CAS  PubMed  Google Scholar 

    58.
    Claassen, R., Wade, T., Breneman, V., Williams, R. & Loesch, C. Preserving native grassland: Can Sodsaver reduce cropland conversion? J. Soil Water Conserv. 73, 67A–73A (2018).
    Google Scholar 

    59.
    Lark, T. J. Protecting our prairies: Research and policy actions for conserving America’s grasslands. Land Use Policy 97, 104727 (2020).
    Google Scholar 

    60.
    Hudson, L. N. et al. The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project. Ecol. Evol. 7, 145–188 (2017).
    PubMed  Google Scholar 

    61.
    Yesson, C. et al. How global is the global biodiversity information facility? PLoS ONE 2, e1124 (2007).

    62.
    Hertel, T. W. The global supply and demand for agricultural land in 2050: a perfect storm in the making? Am. J. Agric. Econ. 93, 259–275 (2011).
    Google Scholar 

    63.
    Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global Food Demand and the Sustainable Intensification of Agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).
    ADS  CAS  PubMed  Google Scholar 

    64.
    Babcock, B. A. Extensive and intensive agricultural supply response. Annu Rev. Resour. Econ. 7, 333–348 (2015).
    Google Scholar 

    65.
    Zhao, X., Van Der Mensbrugghe, D. & Tyner, W. E., Modeling land physically in CGE models: new insights on intensive and extensive margins, 2017 Annual Meeting, July 30-August 1, Chicago, Illinois 258363, Agricultural and Applied Economics Association. https://doi.org/10.22004/ag.econ.258363 (2017).

    66.
    Barr, K. J., Babcock, B. A., Carriquiry, M. A., Nassar, A. M. & Harfuch, L. Agricultural Land Elasticities in the United States and Brazil. Appl. Econ. Perspect. Policy 33, 449–462 (2011).
    Google Scholar 

    67.
    Molotoks, A. et al. Global projections of future cropland expansion to 2050 and direct impacts on biodiversity and carbon storage. Glob. Change Biol. 24, 5895–5908 (2018).
    Google Scholar 

    68.
    Boysen, L. R., Lucht, W. & Gerten, D. Trade-offs for food production, nature conservation and climate limit the terrestrial carbon dioxide removal potential. Glob. Change Biol. 23, 4303–4317 (2017).
    ADS  Google Scholar 

    69.
    Zabel, F. et al. Global impacts of future cropland expansion and intensification on agricultural markets and biodiversity. Nat. Commun. 10, 1–10 (2019).
    ADS  CAS  Google Scholar 

    70.
    Campbell, B. M. et al. Agriculture production as a major driver of the Earth system exceeding planetary boundaries. Ecol. Soc. 22, 8 (2017).

    71.
    Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).
    PubMed  Google Scholar 

    72.
    Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).
    ADS  CAS  PubMed  Google Scholar 

    73.
    Godfray, H. C. J. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).
    ADS  CAS  Google Scholar 

    74.
    Mourad, M. Recycling, recovering and preventing “food waste”: competing solutions for food systems sustainability in the United States and France. J. Clean. Prod. 126, 461–477 (2016).
    Google Scholar 

    75.
    Parfitt, J., Barthel, M. & Macnaughton, S. Food waste within food supply chains: quantification and potential for change to 2050. Philos. Trans. R. Soc. B Biol. Sci. 365, 3065–3081 (2010).
    Google Scholar 

    76.
    Shepon, A., Eshel, G., Noor, E. & Milo, R. The opportunity cost of animal based diets exceeds all food losses. Proc. Natl Acad. Sci. USA 115, 3804–3809 (2018).
    CAS  PubMed  Google Scholar 

    77.
    Lobell, D. B., Cassman, K. G. & Field, C. B. Crop yield gaps: their importance, magnitudes, and causes. Annu. Rev. Environ. Resour. 34, 179 (2009).
    Google Scholar 

    78.
    Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254–257 (2012).
    ADS  CAS  PubMed  Google Scholar 

    79.
    Howell, T. A. Enhancing water use efficiency in irrigated agriculture. Agron. J. 93, 281–289 (2001).
    Google Scholar 

    80.
    Zhang, X. et al. Managing nitrogen for sustainable development. Nature 528, 51–59 (2015).
    ADS  CAS  PubMed  Google Scholar 

    81.
    Kladivko, E. J. et al. Cover crops in the upper midwestern United States: Potential adoption and reduction of nitrate leaching in the Mississippi River Basin. J. Soil Water Conserv. 69, 279–291 (2014).
    Google Scholar 

    82.
    Basche, A. D. & DeLonge, M. S. Comparing infiltration rates in soils managed with conventional and alternative farming methods: A meta-analysis. PLoS ONE 14, e0215702 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    83.
    Chandrasoma, J. M., Christianson, R. D. & Christianson, L. E. Saturated buffers: What is their potential impact across the US Midwest? Agric. Environ. Lett. 4, https://doi.org/10.2134/ael2018.11.0059 (2019).

    84.
    Schulte, L. A. et al. Prairie strips improve biodiversity and the delivery of multiple ecosystem services from corn–soybean croplands. Proc. Natl Acad. Sci. USA 114, 11247–11252 (2017).
    CAS  PubMed  Google Scholar 

    85.
    Renard, D. & Tilman, D. National food production stabilized by crop diversity. Nature 571, 257 (2019).
    CAS  PubMed  Google Scholar 

    86.
    Basso, B., Shuai, G., Zhang, J. & Robertson, G. P. Yield stability analysis reveals sources of large-scale nitrogen loss from the US Midwest. Sci. Rep. 9, 5774 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    87.
    Fargione, J. E. et al. Natural climate solutions for the United States. Sci. Adv. 4, eaat1869 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 

    88.
    LaCanne, C. E. & Lundgren, J. G. Regenerative agriculture: merging farming and natural resource conservation profitably. PeerJ 6, e4428 (2018).
    PubMed  PubMed Central  Google Scholar 

    89.
    Lark, T. J., Mueller, R. M., Johnson, D. M. & Gibbs, H. K. Measuring land-use and land-cover change using the U.S. department of agriculture’s cropland data layer: Cautions and recommendations. Int. J. Appl. Earth Obs. Geoinf. 62, 224–235 (2017).
    ADS  Google Scholar 

    90.
    Lark, T. J. America’s Food- and Fuel-Scapes: Quantifying Agricultural Land-Use Change Across the United States (The University of Wisconsin, Madison, 2017).

    91.
    Homer, C. et al. Completion of the 2011 National Land Cover Database for the conterminous United States–representing a decade of land cover change information. Photogramm. Eng. Remote Sens. 81, 345–354 (2015).
    Google Scholar 

    92.
    Kim, K. E. Adaptive majority filtering for contextual classification of remote sensing data. Int. J. Remote Sens. 17, 1083–1087 (1996).
    ADS  Google Scholar 

    93.
    Tobler, W. R. A computer movie simulating urban growth in the Detroit region. Econ. Geogr. 46, 234–240 (1970).
    Google Scholar 

    94.
    Miller, H. J. Tobler’s first law and spatial analysis. Ann. Assoc. Am. Geogr. 94, 284–289 (2004).
    Google Scholar 

    95.
    Breiman, L. Random forests. Mach. Learn 45, 5–32 (2001).
    MATH  Google Scholar 

    96.
    Jeong, J. H. et al. Random forests for global and regional crop yield predictions. PLoS ONE 11, e0156571 (2016).
    PubMed  PubMed Central  Google Scholar 

    97.
    USDA – National Agricultural Statistics Service. Guide to NASS Surveys http://www.nass.usda.gov/Surveys/Guide_to_NASS_Surveys/index.php. (2020).

    98.
    Soil Survey Staff, N. R. C. S., United States Department of Agriculture. Soil Survey Geographic (SSURGO) Database for the United States. (2018).

    99.
    Gesch, D. et al. The national elevation dataset. Photogramm. Eng. Remote Sens. 68, 5–32 (2002).
    Google Scholar 

    100.
    Gorelick, N. et al. Google Earth Engine: planetary-scale geospatial analysis for everyone. Remote Sens. Environ. 202, 18–27 (2017).
    ADS  Google Scholar 

    101.
    Team, R. C. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2017).

    102.
    Hydric Soils—Introduction | NRCS Soils. https://www.nrcs.usda.gov/wps/portal/nrcs/detail/soils/use/hydric/?cid=nrcs142p2_053961 (2020).

    103.
    Cowardin, L. M., Shaffer, T. L. & Arnold, P. M. Evaluations of Duck Habitat and Estimation of Duck Population Sizes with a Remote-Sensing-Based System. https://apps.dtic.mil/docs/citations/ADA322572 (1995).

    104.
    Jin, S. et al. Overall methodology design for the United States national land cover database 2016 products. Remote Sens. 11, 2971 (2019).
    ADS  Google Scholar  More

  • in

    Paddy fields located in water storage zones could take over the wetland plant community

    Study site
    The study was conducted in the Tone river basin, central Japan (Fig. 1). The Tone river is Japan’s second-longest river, running through the entire Kanto plain in central Japan. The Tone river basin is covered mainly by rice paddies and also contains arable fields other than rice, seminatural grasslands, coppice forests, farm villages, and urban areas29. The Tone river basin is located in the Kanto plain which is the largest plain field in Japan (approximately 170,000 km2), including large floodplains. Thus, this area have a variety of both terrain conditions and agricultural modernization works.
    Figure 1

    Location of the Tone river basin and monitoring sites.

    Full size image

    Plants community data
    The Institute for Agro-Environmental Sciences, NARO, Japan conducted the program for monitoring biodiversity, including birds29 and plants34, in each of the thirty-two 1-km2 grids in the Tone river basin in 2002. In this program, the Tone river basin was initially divided into one hundred 1-km square grids (hereafter, 1-km grid), and each square was classified into one of four major land use types in the region: (1) midstream paddy; (2) downstream lowland paddy; (3) plateau and valley-bottom paddy; and (4) urban fringe29. Then, eight grids were selected randomly as study sites from each land use type, making a total of 32 grids (Fig. 1). The grids were more than 5 km apart (Fig. 1), so they were spatially independent of each other. In this study we used the plant monitoring records from the program. In the plant monitoring program there were three terms—2002, 2007, and 2012—of vegetation survey based on the Braun–Blanquet approach in each 1 km grid 35. In each survey, approximately 20 quadrats measuring 1 m2 were placed randomly in each 1-km grid in each survey term and the coverage ratios of all plant species in four hierarchies—(1) tall tree, (2) semi-tall tree, (3) shrub, and (4) grasses—were recorded. In this study, we used only the grasses class without abundance and the presence or absence of species records in the grasses class. We pooled all the species records within each 1-km grid for analysis. All plant monitoring data are available as Open Data (CC BY 4.0) at github space own by Dr. N. Iwasaki who was the member of this monitoring program (https://github.com/wata909/RuLIS_monitoring, accessed at 25, May 2020).
    Dividing wetland plants and non-wetland plants
    To test our hypothesis, we needed to divide the plants that typically grow in wetlands (hereafter, wetland plants) and those that typically grown in non-wetlands (hereafter, non-wetland plants) to evaluate the habitat quality of paddy fields as wetland. To this end, we used a published checklist of wetland plants in Japan (Shutoh et al. 2019; https://wetlands.info/tools/plantsdb/wetlandplants-checklist/, accessed at 25, May 2020). This checklist defined 8,358 Japanese vascular plants as wetland and aquatic plants according to their habitat requirements and the “wetland” definition of the Ramsar Convention (Ramsar Convention Secretariat 2016, https://www.ramsar.org/sites/default/files/documents/library/manual6-2013-e.pdf, accessed at 25, May 2020). We used this checklist to identify the wetland plant species in the monitoring records.
    Land use, terrain condition, and human activity
    A digitized land use map for paddy fields in 2009 that relatively matched the plant monitoring terms (2002, 2007, and 2012) was prepared from the National Land Numerical Information (National Land Information Division, MLIT of Japan: https://nlftp.mlit.go.jp/ksj-e/index.html, accessed at 25, May 2020). These map data were developed using both topographic maps and satellite imaging data, with the land use labeled on the basis of nationwide land use classifications, including paddy fields, at approximately 100-m grid resolution (National Land Information Division, MLIT of Japan: https://nlftp.mlit.go.jp/ksj-e/index.html, accessed at 25, May 2020).
    A FAV, which was ascertained by accumulating the weights of all cells that flowed into each downslope cell, was used to define the concave areas (ESRI, https://pro.arcgis.com/en/pro-app/tool-reference/spatial-analyst/how-flow-accumulation-works.htm, accessed at 25, May 2020); lower elevations and valley areas had a higher FAV because they could potentially store more water, whereas higher ridge areas had low FAVs (Fig. 2). We used FAV to define the wetland potential, as this value could reflect the water accumulation from upper areas to lower areas, which strongly relates to the natural process of wetland formation36. We considered that terrain variable could reflect the geographical conditions of paddy field namely potentially wetland habitat for their intact ecosystem. We considered high FAV areas to have high potential of wetland habitat for their intact ecosystem. We calculated FAV value on a whole for mainland Japan; therefore, that range could cover the entire basin which overlapped with our target areas. The FAV was calculated using ArcGIS 10.5 with Spatial analyst (ESRI, Redlands, CA, USA) using a 50-m digital elevation model from the Japanese Map Centre (https://www.jmc.or.jp/, accessed at 25, May 2020). The FAV and paddy field maps were overlaid, and the total FAVs for paddy fields in each 1-km grid were calculated to determine the potentiality of the paddy fields in the 1-km grid being wetland. If a paddy field had an extremely high FAV within the basin which included the paddy field, that paddy field could have been a wetland because that area could store a large amount of water naturally.
    Figure 2

    Conceptual image of the flow accumulation value to indicate the potential of wetland.

    Full size image

    The proportional area of field consolidation as current human activity was calculated for each grid square using digital polygon data on the shape of farmland, as derived from aerial imagery collected in 2001 by the Ministry of Agriculture, Forestry, and Fisheries (MAFF), Japan. We obtained data on land leveling in agricultural areas from MAFF (https://www.maff.go.jp/j/tokei/porigon/, accessed at 25, May 2020) and used these data as an index of consolidated farmland because land leveling is one of the important components of agricultural consolidation in Japan4,23. Generally, agricultural consolidation in Japan involves land leveling, which integrates small, patchy farmland areas. Each polygon was assigned a status of “leveled” or “not leveled” according to its current status. Using ArcGIS, we calculated the ratio of consolidation for paddy fields in each 1-km grid that had survey sites.
    Statistical analysis
    We performed the two types of analysis used in this study with the statistical package R version 3.5.2 (R development core Team, https://www.r-project.org/, accessed at 17, Feb. 2020). First, we tested the species number in each 1-km grid using GLM with Poisson distributions (log link) and a Wald test37. The response variables were total species number, number of wetland plants, and number of non-wetland plants in each 1-km grid in each survey term. Explanatory variables were the log-transformed FAV values for the paddy fields and consolidation ratio of the paddy field within the 1-km grid. The aim of this analysis was to assess the effects on species diversity of both the original environmental condition of and current human activities in the paddy fields. Prior to the GLM analysis, all explanatory variables were tested for multicollinearity by calculating the variance inflation factors (VIFs)38; no significant multicollinearity was found (VIF  More

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    Environmental filtering and spillover explain multi-species edge responses across agricultural boundaries in a biosphere reserve

    1.
    Vandermeer, J. & Perfecto, I. Tropical conservation and grassroots social movements: ecological theory and social justice. Bull. Ecol. Soc. Am. 88, 171–175 (2007).
    Google Scholar 
    2.
    Singer, B. How useful is the landscape approach? In Proceedings of the 2nd world heritage forests meeting (9–11 March 2005) (2007).

    3.
    Wiens, J. A. (2002). Central concepts and issues of landscape ecology. In Gutzwiller, K. J. (Eds.), Applying landscape ecology in biological conservation (pp. 3–21). Springer.

    4.
    Schonewald-Cox, C. M. & Bayless, J. W. The boundary model: a geographical analysis of design and conservation of nature reserves. Biol. Conserv. 38, 305–322 (1986).
    Google Scholar 

    5.
    Ewers, R. M. & Didham, R. K. Confounding factors in the detection of species responses to habitat fragmentation. Biol. Rev. 81, 117–142 (2006).
    PubMed  Google Scholar 

    6.
    Driscoll, D. A., Banks, S. C., Barton, P. S., Lindenmayer, D. B. & Smith, A. L. Conceptual domain of the matrix in fragmented landscapes. Trends Ecol. Evol. 28, 605–613 (2013).
    PubMed  Google Scholar 

    7.
    Prevedello, J. A. & Vieira, M. V. Does the type of matrix matter? A quantitative review of the evidence. Biodivers. Conserv. 19, 1205–1223 (2010).
    Google Scholar 

    8.
    Campbell, R. E., Harding, J. S., Ewers, R. M., Thorpe, S. & Didham, R. K. Production land use alters edge response functions in remnant forest invertebrate communities. Ecol. Appl. 21, 3147–3161 (2011).
    Google Scholar 

    9.
    Tscharntke, T., Rand, T. A. & Bianchi, F. J. J. A. The landscape context of trophic interactions: insect spillover across the crop-noncrop interface. Ann. Zool. Fennici 42, 421–432 (2005).
    Google Scholar 

    10.
    Ng, K., Barton, P. S., Macfadyen, S., Lindenmayer, D. B. & Driscoll, D. A. Beetle’s responses to edges in fragmented landscapes are driven by adjacent farmland use, season and cross-habitat movement. Landsc. Ecol. 33, 109–125 (2018).
    Google Scholar 

    11.
    Ruffell, J. & Didham, R. K. Towards a better mechanistic understanding of edge effects. Landsc. Ecol. 31, 2205–2213 (2016).
    Google Scholar 

    12.
    Murcia, C. Edge effects in fragmented forests: implications for conservation. Trends Ecol. Evol. 10, 58–62 (1995).
    CAS  PubMed  Google Scholar 

    13.
    Ruffel, J. et al. Discriminating the drivers of edge effects on nest predation: forest edges reduce capture rates of ship rats (Rattus rattus), a globally invasive nest predator, by altering vegetation structure. PLoS ONE 9, e113098 (2014).
    ADS  Google Scholar 

    14.
    Mairota, P. et al. Very high resolution earth observation features for testing the direct and indirect effects of landscape structure on local habitat quality. Int. J. Appl. Earth Obs. Geoinf. 34, 96–102 (2015).
    ADS  Google Scholar 

    15.
    Laurance, W. F., Didham, R. K. & Power, M. E. Ecological boundaries: a search for synthesis. Trends Ecol. Evol. 16, 70–71 (2001).
    Google Scholar 

    16.
    Perfecto, I. & Vandermeer, J. Quality of agroecological matrix in a tropical montane landscape: ants in coffee plantations in southern mexico. Conserv. Biol. 16, 174–182 (2002).
    Google Scholar 

    17.
    Kupfer, J. A., Malanson, G. P. & Franklin, S. B. Not seeing the ocean for the islands: the mediating influence of matrix-based processes on forest fragmentation effects. Glob. Ecol. Biogeogr. 15, 8–20 (2006).
    Google Scholar 

    18.
    Leibold, M. A. et al. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7, 601–613 (2004).
    Google Scholar 

    19.
    Ries, L. & Debinski, D. M. Butterfly responses to habitat edges in the highly fragmented prairies of Central Iowa. J. Anim. Ecol. 70, 840–852 (2001).
    Google Scholar 

    20.
    de Lange, H. J., Lahr, J., Brouwer, J. H. D. & Faber, J. H. Review of available evidence regarding the vulnerability of off-crop non-target arthropod communities in comparison to in-crop non-target arthropod communities. Support. Publ. EN-348 (2012).

    21.
    Ppr, E. F. S. A. Scientific opinion addressing the rate of the science on risk assessment of plant protection products for non-target arthropods. EFSA J. 13, 3996 (2015).
    Google Scholar 

    22.
    Ries, L. & Sisk, T. D. Butterfly edge effects are predicted by a simple model in a complex landscape. Oecologia 156, 75–86 (2008).
    ADS  PubMed  Google Scholar 

    23.
    Ries, L., Murphy, S. M., Wimp, G. M. & Fletcher, R. J. Closing persistent gaps in knowledge about edge ecology. Curr. Landsc. Ecol. Rep. 2, 30–41 (2017).
    Google Scholar 

    24.
    Wilson, D. S. Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 73, 1984–2000 (1992).
    Google Scholar 

    25.
    Ries, L., Fletcher, R. J. J., Battin, J. & Sisk, T. D. Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu. Rev. Ecol. Evol. Syst. 35, 491–522 (2004).
    Google Scholar 

    26.
    Ries, L. & Sisk, T. D. What is an edge species? The implications of sensitivity to habitat edges. Oikos 119, 1636–1642 (2010).
    Google Scholar 

    27.
    Pandit, S. N., Kolasa, J., Cottenie, K., Andit, S. H. N. P. & Olasa, J. U. K. Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology 90, 2253–2262 (2009).
    PubMed  Google Scholar 

    28.
    van Schalkwyk, J., Pryke, J. S. & Samways, M. J. Contribution of common vs. rare species to species diversity patterns in conservation corridors. Ecol. Indic. 104, 279–288 (2019).
    Google Scholar 

    29.
    Kotze, D. J. & Samways, M. J. No general edge effects for invertebrates at Afromontane forest/grassland ecotones. Biodivers. Conserv. 10, 443–466 (2001).
    Google Scholar 

    30.
    Rand, T. A., Tylianakis, J. M. & Tscharntke, T. Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol. Lett. 9, 603–614 (2006).
    PubMed  Google Scholar 

    31.
    Winegardner, A. K., Jones, B. K., Ng, I. S. Y., Siqueira, T. & Cottenie, K. The terminology of metacommunity ecology. Trends Ecol. Evol. 27, 253–254 (2012).
    PubMed  Google Scholar 

    32.
    Lanta, V., Nordahl, K., Gilbert, S., Söderman, G. & Rinne, V. Biotic filtering and mass effects in small shrub patches: is arthropod community structure predictable based on the quality of the vegetation?. Ecol. Entomol. 43, 234–244 (2018).
    Google Scholar 

    33.
    Duelli, P. & Obrist, M. K. Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic Appl. Ecol. 4, 129–138 (2003).
    Google Scholar 

    34.
    Katayama, N., Bouam, I., Koshida, C. & Baba, Y. G. Biodiversity and yield under different land-use types in orchard/vineyard landscapes: a meta-analysis. Biol. Conserv. 229, 125–133 (2019).
    Google Scholar 

    35.
    Lucey, J. M. et al. Tropical forest fragments contribute to species richness in adjacent oil palm plantations. Biol. Conserv. 169, 268–276 (2014).
    Google Scholar 

    36.
    Vink, N. & Tregurtha, N. Agriculture and mariculture first paper: structure, performance and future prospects—an overview (Department of Agriculture, Forestry, and Fisheries, Cape Town, 2007).
    Google Scholar 

    37.
    Thorpe, P. T., Pryke, J. S. & Samways, M. J. Review of ecological and conservation perspectives on future options for arthropod management in Cape Floristic Region pome fruit orchards. Afr. Entomol. 24, 279–306 (2016).
    Google Scholar 

    38.
    van Schalkwyk, J., Pryke, J. S., Samways, M. J. & Gaigher, R. Complementary and protection value of a Biosphere Reserve buffer zone for increasing local representativeness of ground-living arthropods. Biol. Conserv. 239, 108292 (2019).
    Google Scholar 

    39.
    Chao, A. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783 (1987).
    MathSciNet  CAS  PubMed  MATH  Google Scholar 

    40.
    Oksanen, J. et al. vegan: community ecology package (2019).

    41.
    R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2019).

    42.
    De Cáceres, M. & Legendre, P. Associations between species and groups of sites: indices and statistical inference. Ecology 90, 3566–3574 (2009).
    Google Scholar 

    43.
    Tichý, L. & Chytrý, M. Statistical determination of diagnostic species for site groups of unequal sample size. J. Veg. Sci. 17, 809–818 (2006).
    Google Scholar 

    44.
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Google Scholar 

    45.
    Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280 (2001).
    ADS  PubMed  Google Scholar 

    46.
    Dray, S., Legendre, P. & Peres-Neto, P. R. Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol. Model. 196, 483–493 (2006).
    Google Scholar 

    47.
    Blanchet, G., Legendre, P. & Borcard, D. Forward selection of spatial explanatory variables. Ecology 89, 2623–2632 (2008).
    PubMed  Google Scholar 

    48.
    Bauman, D., Drouet, T., Fortin, M.-J. & Dray, S. Optimizing the choice of a spatial weighting matrix in eigenvector-based methods. Ecology 99, 2159–2166 (2018).
    PubMed  Google Scholar 

    49.
    Wagner, H. H. Direct multi-scale ordination with canonical correspondence analysis. Ecology 85, 342–351 (2004).
    Google Scholar 

    50.
    Dray, S. et al. adespatial: multivariate multiscale spatial analysis (2019).

    51.
    UNESCO. Biosphere reserves—learning sites for sustainable development (2017). https://www.unesco.org/new/en/natural-sciences/environment/ecological-sciences/biosphere-reserves/. Accessed 2 March 2020.

    52.
    Kammerer, M. A., Biddinger, D. J., Rajotte, E. G. & Mortensen, D. A. Local plant diversity across multiple habitats supports a diverse wild bee community in pennsylvania apple orchards. Environ. Entomol. 45, 32–38 (2016).
    PubMed  Google Scholar 

    53.
    Witt, A. B. R. & Samways, M. J. Influence of agricultural land transformation and pest management practices on the arthropod diversity of a biodiversity hotspot, the Cape Floristic Region, South Africa. Afr. Entomol. 12, 89–95 (2004).
    Google Scholar 

    54.
    Adu-Acheampong, S., Bazelet, C. S. & Samways, M. J. Extent to which an agricultural mosaic supports endemic species-rich grasshopper assemblages in the Cape Floristic Region biodiversity hotspot. Agric. Ecosyst. Environ. 227, 52–60 (2016).
    Google Scholar 

    55.
    Magura, T. Carabids and forest edge: spatial pattern and edge effect. For. Ecol. Manag. 157, 23–37 (2002).
    Google Scholar 

    56.
    Kautz, M., Schopf, R. & Ohser, J. The ‘sun-effect’: microclimatic alterations predispose forest edges to bark beetle infestations. Eur. J. For. Res. 132, 453–465 (2013).
    Google Scholar 

    57.
    Greenslade, P. Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). J. Anim. Ecol. 33, 301–310 (1964).
    Google Scholar 

    58.
    Gascon, C. et al. Matrix habitat and species richness in tropical forest remnants. Biol. Conserv. 91, 223–229 (1999).
    Google Scholar 

    59.
    Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2017).
    Google Scholar 

    60.
    Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science (80-) 344, 296–299 (2014).
    ADS  CAS  Google Scholar 

    61.
    Epstein, D. L., Zack, R. S., Brunner, J. F., Gut, L. & Brown, J. J. Effects of broad-spectrum insecticides on epigeal arthropod biodiversity in Pacific Northwest apple orchards. Environ. Entomol. 29, 340–348 (2000).
    CAS  Google Scholar 

    62.
    Markó, V. & Kádár, F. Effects of different insecticide disturbance levels and weed patterns on carabid beetle assemblages. Acta Phytopathol. Entomol. Hungarica 40, 111–143 (2005).
    Google Scholar 

    63.
    Ries, L. & Sisk, T. D. A predictive model of edge effects. Ecology 85, 2917–2926 (2004).
    Google Scholar 

    64.
    Gerlach, J., Samways, M. & Pryke, J. Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. J. Insect Conserv. 17, 831–850 (2013).
    Google Scholar 

    65.
    Nuyttens, D. et al. Drift from field crop sprayers using an integrated approach: results of a five-year study. Trans. ASABE 54, 403–408 (2011).
    Google Scholar 

    66.
    Zaady, E., Katra, I., Shuker, S., Knoll, Y. & Shlomo, S. Tree belts for decreasing aeolian dust-carried pesticides from cultivated areas. Geosciences 8, 286 (2018).
    ADS  Google Scholar 

    67.
    Blitzer, E. J. et al. Spillover of functionally important organisms between managed and natural habitats. Agric. Ecosyst. Environ. 146, 34–43 (2012).
    Google Scholar 

    68.
    Leibold, M. A., Chase, J. M. & Ernest, S. K. M. Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystems attributes. Ecology 98, 909–919 (2017).
    PubMed  Google Scholar 

    69.
    With, K. A. The landscape ecology of invasive spread. Conserv. Biol. 16, 1192–1203 (2002).
    Google Scholar 

    70.
    Hickey, M. B. C. & Doran, B. A review of the efficiency of buffer strips for the maintenance and enhancement of riparian ecosystems. Water Qual. Res. J. Canada 39, 311–317 (2004).
    Google Scholar 

    71.
    Vought, L. B. M. & Lacoursièr, J. O. Restoration of streams in the agricultural landscapes. In Restoration of Lakes, Streams, Floodplains, and Bogs in Europe Vol. 3 (ed. Eiseltová, M.) (Springer, Berlin, 2010).
    Google Scholar 

    72.
    Samways, M. J., Osborn, R. & Carliel, F. Effect of a highway on ant (Hymenoptera: Formicidae) species composition and abundance, with a recommendation for roadside verge width. Biodivers. Conserv. 6, 903–913 (1997).
    Google Scholar 

    73.
    Nyhus, P. J. & Adams, M. S. Biosphere Reserves of the World—Principles and Practice (University of Wisconsin, Madison, 1995).
    Google Scholar 

    74.
    UNESCO. Management Manual for UNESCO Biosphere Reserves in Africa. (2015).

    75.
    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton University Press, Princeton, 1967).
    Google Scholar 

    76.
    Mehring, M. & Stoll-Kleemann, S. How effective is the buffer zone? Linking institutional processes with satellite images from a case study in the Lore Lindu forest biosphere reserve, Indonesia. Ecol. Soc. 16, 3 (2011).
    Google Scholar 

    77.
    Badejo, M. A. & Ola-Adams, B. A. Abundance and diversity of soil mites of fragmented habitats in a biopshere reserve in southern Nigeria. Pesqui. Agropecuária Bras. 35, 2121–2128 (2000).
    Google Scholar 

    78.
    Dutta, P. et al. Mosquito biodiversity of Dibru-Saikhowa biosphere reserve in Assem, India. J. Environ. Biol. 31, 695–699 (2010).
    CAS  PubMed  Google Scholar 

    79.
    González-Moreno, A., Bordera, S., Leirana-Alcocer, J., Delfín-González, H. & Ballina-Gómez, H. S. Explaining variations in the diversity of parasitoid assemblages in a biosphere reserve of Mexico: evidence from vegetation, land management and seasonality. Bull. Entomol. Res. 108, 602–615 (2018).
    PubMed  Google Scholar 

    80.
    McIntyre, S. & Barrett, G. W. Habitat variegation, an alternative to fragmentation. Conserv. Biol. 6, 146–147 (1992).
    Google Scholar 

    81.
    Ingham, D. S. & Samways, M. J. Application of fragmentation and variegation models to epigaeic invertebrates in South Africa. Conserv. Biol. 10, 1353–1358 (1996).
    Google Scholar 

    82.
    Guevara, S. & Laborde, J. The landscape approach: designing new reserves for protection of biological and cultural diversity in Latin America. Environ. Ethics 30, 251–262 (2008).
    Google Scholar 

    83.
    Brunckhorst, D. Building capital through bioregional planning and biosphere reserves. Ethics Sci. Environ. Polit. 1, 19–32 (2001).
    Google Scholar  More