More stories

  • in

    The future of Viscum album L. in Europe will be shaped by temperature and host availability

    Walas, Ł, Ganatsas, P., Iszkuło, G., Thomas, P. A. & Dering, M. Spatial genetic structure and diversity of natural populations of Aesculus hippocastanum L. in Greece. PLoS ONE 14, e0226225 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Song, Y. G. et al. Past, present and future suitable areas for the relict tree Pterocarya fraxinifolia (Juglandaceae): Integrating fossil records, niche modeling, and phylogeography for conservation. Eur. J. For. Res. 140, 1323–1339 (2021).Article 

    Google Scholar 
    Dyderski, M. K., Paź, S., Frelich, L. E. & Jagodziński, A. M. How much does climate change threaten European forest tree species distributions?. Glob. Change Biol. 24, 1150–1163 (2018).ADS 
    Article 

    Google Scholar 
    Chakraborty, D., Móricz, N., Rasztovits, E., Dobor, L. & Schueler, S. Provisioning forest and conservation science with high-resolution maps of potential distribution of major European tree species under climate change. Ann. For. Sci. 78, 1–18 (2021).Article 

    Google Scholar 
    Williams, J. N. et al. Using species distribution models to predict new occurrences for rare plants. Divers. Distrib. 15, 565–576 (2009).Article 

    Google Scholar 
    Watling, J. I. et al. Performance metrics and variance partitioning reveal sources of uncertainty in species distribution models. Ecol. Modell. 309, 48–59 (2015).ADS 
    Article 

    Google Scholar 
    Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259 (2006).Article 

    Google Scholar 
    Phillips, S. J., Dudík, M. & Schapire, R. E. [Internet] Maxent software for modeling species niches and distributions. url: http://biodiversityinformatics.amnh.org/open_source/maxent/. Accessed 13 July 2022.Elith, J. et al. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57 (2011).Article 

    Google Scholar 
    Marcer, A., Sáez, L., Molowny-Horas, R., Pons, X. & Pino, J. Using species distribution modelling to disentangle realised versus potential distributions for rare species conservation. Biol. Conserv. 166, 221–230 (2013).Article 

    Google Scholar 
    Rigling, A., Eilmann, B., Koechli, R. & Dobbertin, M. Mistletoe-induced crown degradation in Scots pine in a xeric environment. Tree Physiol. 30, 845–852 (2010).PubMed 
    Article 

    Google Scholar 
    Sangüesa-Barreda, G., Linares, J. C. & Camarero, J. J. Mistletoe effects on Scots pine decline following drought events: Insights from within-tree spatial patterns, growth and carbohydrates. Tree Physiol. 32, 585–598 (2012).PubMed 
    Article 

    Google Scholar 
    Kollas, C., Gutsch, M., Hommel, R., Lasch-Born, P. & Suckow, F. Mistletoe-induced growth reductions at the forest stand scale. Tree Physiol. 38, 735–744 (2018).PubMed 
    Article 

    Google Scholar 
    Schulze, E. D. & Ehleringer, J. R. The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta 162, 268–275 (1984).PubMed 
    Article 

    Google Scholar 
    Escher, P. et al. Transpiration, CO2 assimilation, WUE, and stomatal aperture in leaves of Viscum album L: Effect of abscisic acid (ABA) in the xylem sap of its host (Populus x euamericana). Plant Physiol. Biochem. 46, 64–70 (2008).PubMed 
    Article 

    Google Scholar 
    Zweifel, R., Bangerter, S., Rigling, A. & Sterck, F. J. Pine and mistletoes: How to live with a leak in the water flow and storage system?. J. Exp. Bot. 63, 2565–2578 (2012).PubMed 
    Article 

    Google Scholar 
    Mutlu, S., Osma, E., Ilhan, V., Turkoglu, H. I. & Atici, O. Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap. Trees 30, 815–824 (2016).Article 

    Google Scholar 
    Tsopelas, P., Angelopoulos, A., Economou, A. & Soulioti, N. Mistletoe (Viscum album) in the fir forest of Mount Parnis Greece. For. Ecol. Manag. 202, 59–65 (2004).Article 

    Google Scholar 
    Dobbertin, M. & Rigling, A. Pine mistletoe (Viscum album ssp. austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. For. Pathol. 36, 309–322 (2006).Article 

    Google Scholar 
    Lech, P., Żółciak, A. & Hildebrand, R. Occurrence of European mistletoe (Viscum album L.) on forest trees in Poland and its dynamics of spread in the period 2008–2018. Forests 11, 83 (2020).Article 

    Google Scholar 
    Iszkuło, G. et al. Jemioła jako zagrożenie dla zdrowotności drzewostanów iglastych. Sylwan 164, 226–236 (2020) ([In Polish]).
    Google Scholar 
    Mellado, A., Morillas, L., Gallardo, A. & Zamora, R. Temporal dynamic of parasite-mediated linkages between the forest canopy and soil processes and the microbial community. New Phytol. 211, 1382–1392 (2016).PubMed 
    Article 

    Google Scholar 
    Mellado, A. & Zamora, R. Generalist birds govern the seed dispersal of a parasitic plant with strong recruitment constraints. Oecologia 176, 139–147 (2014).ADS 
    PubMed 
    Article 

    Google Scholar 
    Hódar, J. A., Lázaro-González, A. & Zamora, R. Beneath the mistletoe: parasitized trees host a more diverse herbaceous vegetation and are more visited by rabbits. Ann. For. Sci. 75, 1–8 (2018).Article 

    Google Scholar 
    Zuber, D. Biological flora of Central Europe: Viscum album L. Flora Morphol. Distrib Funct. Ecol. Plants 199, 181–203 (2004).Article 

    Google Scholar 
    Urech, K. & Baumgartner, S. Chemical constituents of Viscum album L.: Implications for the pharmaceutical preparation of mistletoe. In: Mistletoe: From mythology to evidence-based medicine. (eds. Zänker, K.S. & Kaveri, S. V.), 11–23. (S. Karger AG, Basel, Switzerland, 2015).Singh, B. N. et al. European Viscum album: a potent phytotherapeutic agent with multifarious phytochemicals, pharmacological properties and clinical evidence. RSC Adv. 6, 23837–23857 (2016).ADS 
    Article 

    Google Scholar 
    Jeffree, C. E. & Jeffree, E. P. Redistribution of the potential geographical ranges of mistletoe and colorado beetle in Europe in response to the temperature component of climate change. Funct. Ecol. 10, 562–577 (1996).Article 

    Google Scholar 
    Troels-Smith, J. Ivy, mistletoe and elm climate indicators-fodder plants. A contribution to the interpretation of the pollen zone border VII-VIII. Dan. Geol. Undersøg. IV Række 4, 1–32 (1960).
    Google Scholar 
    Dobbertin, M. et al. The upward shift in altitude of pine mistletoe (Viscum album ssp. austriacum) in Switzerland—the result of climate warming?. Int. J. Biometeorol. 50, 40–47 (2005).ADS 
    PubMed 
    Article 

    Google Scholar 
    Zamora, R. & Mellado, A. Identifying the abiotic and biotic drivers behind the elevational distribution shift of a parasitic plant. Plant Biol. 21, 307–317 (2019).PubMed 
    Article 

    Google Scholar 
    Barney, C. W., Hawksworth, F. G. & Geils, B. W. Hosts of Viscum album. Eur. J. Plant Pathol. 28, 187–208 (1998).
    Google Scholar 
    Böhling, N. et al. Notes on the Cretan mistletoe, Viscum album subsp. creticum subsp. nova (Loranthaceae/Viscaceae). Isr. J. Plant Sci. 50, 77–84 (2002).
    Google Scholar 
    Plants of the World Online [Internet] url: https://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:921668-1. Accessed 13 July 2022.Zuber, D. & Widmer, A. Phylogeography and host race differentiation in the European mistletoe (Viscum album L.). Mol. Ecol. 18, 1946–1962 (2009).PubMed 
    Article 

    Google Scholar 
    Schaller, G., Urech, K., Grazi, G. & Giannattasio, M. Viscotoxin composition of the three European subspecies of Viscum album. Planta Med 64, 677–678 (1998).PubMed 
    Article 

    Google Scholar 
    Kahle-Zuber, D. Biology and evolution of the European mistletoe (Viscum album). Doctoral Thesis. ETH Zurich. (2008).Zuber, D. & Widmer, A. Genetic evidence for host specificity in the hemi-parasitic Viscum album L. (Viscaceae). Mol. Ecol. 9, 1069–1073 (2000).PubMed 
    Article 

    Google Scholar 
    Mejnartowicz, L. Relationship and genetic diversity of mistletoe [Viscum album L.] subspecies. Acta Soc. Bot. Pol. Pol. 75, 39–49 (2006).Article 

    Google Scholar 
    Xie, W., Adolf, J. & Melzig, M. F. Identification of Viscum album L. miRNAs and prediction of their medicinal values. PLoS ONE 12, e0187776 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Valle, A. C. V., de Carvalho, A. C. & Andrade, R. V. Viscum album-literature review. Int. J. Sci. Res 10, 63–71 (2021).
    Google Scholar 
    Schröder, L. et al. The gene space of European mistletoe (Viscum album). Plant J. 109, 278–294 (2022).PubMed 
    Article 

    Google Scholar 
    Sangüesa-Barreda, G. et al. Delineating limits: Confronting predicted climatic suitability to field performance in mistletoe populations. J. Ecol. 106, 2218–2229 (2018).Article 

    Google Scholar 
    GBIF.org [Internet] GBIF Occurrence Download Doi: https://doi.org/10.15468/dl.zw6f5q. Accessed 27 July 2021.GBIF.org [Internet] GBIF Occurrence Download Doi: https://doi.org/10.15468/dl.6wmc9d. Accessed 6 August 2021.FloraWeb [Internet] url: https://www.floraweb.de. Accessed 10 December 2021.Pladias – Database of the Czech Flora and Vegetation. [Internet] url: www.pladias.cz. Accessed 14 July 2022.Zając, A., Zając, M., Tertil, R. & Harman, I. Atlas rozmieszczenia roślin naczyniowych w Polsce. 593 (Instytut Botaniki Uniwersytetu Jagiellońskiego, Kraków, 2001) [In Polish].Idžojtić, M., Kogelnik, M., Franjić, J. & Škvorc, Ž. Hosts and distribution of Viscum album L. ssp. album in Croatia and Slovenia. Plant Biosyst. 140, 50–55 (2006).Article 

    Google Scholar 
    Varga, I. et al. Changes in the Distribution of European Mistletoe (Viscum album) in Hungary During the Last Hundred Years. Folia Geobot 49, 559–577 (2014).Article 

    Google Scholar 
    Wild, J. et al. Plant distribution data for the Czech Republic integrated in the Pladias database. Preslia 91, 1–24 (2019).Article 

    Google Scholar 
    Krasylenko, Y. et al. The European mistletoe (Viscum album L.): Distribution, host range, biotic interactions, and management worldwide with special emphasis on Ukraine. Botany 98, 499–516 (2020).Article 

    Google Scholar 
    Karger, D. N. et al. Climatologies at high resolution for the Earth land surface areas. Sci. Data 4, 170122 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Karger D. N., et al. Data from: Climatologies at high resolution for the earth’s land surface areas. Dryad Digital Repository (2018).Gutjahr, O. et al. Max planck institute earth system model (MPI-ESM1. 2) for the high-resolution model intercomparison project (HighResMIP). Geosci. Model Dev. 12, 3241–3281 (2019).ADS 
    Article 

    Google Scholar 
    Hijmans, R. J., & van Etten, J. raster: Geographic analysis and modeling with raster data. R package version 2.0-12. (2012).R Core Team. The Comprehensive R Archive Network. [Internet] url: https://cran.r-project.org/ Accessed 14 July 2022.Chakraborty, D., Móricz, N., Rasztovits, E., Dobor, L. & Schueler, S. Provisioning forest and conservation science with European tree species distribution models under climate change (Version v1). Zenodo https://doi.org/10.5281/zenodo.3686918 (2020).Wang, Z., Chang, Y. I., Ying, Z., Zhu, L. & Yang, Y. A parsimonious threshold-independent protein feature selection method through the area under receiver operating characteristic curve. Bioinformatics 23, 2788–2794 (2007).PubMed 
    Article 

    Google Scholar 
    Lobo, J. M., Jiménez-Valverde, A. & Hortal, J. The uncertain nature of absences and their importance in species distribution modelling. Ecography 33, 103–114 (2010).Article 

    Google Scholar 
    QGIS Development Team. QGIS Geographic Information Sys-tem. Open Source Geospatial Foundation Project. [Internet]. url: https://www.qgis.org/en/site/. Accessed 14 July 2022.Fischer, J. T. Water relations of mistletoes and their hosts. In: The biology of mistletoes. (eds. Calder, M., & Bernhard, T.), 163–184 (Academic Press, Sydney, 1983).Skre, O. The regional distribution of vascular plants in Scandinavia with requirements for high summer temperatures. Norweg. J. Bot. 26, 295–318 (1979).
    Google Scholar 
    Wangerin, B. Loranthaceae. In: Lebensgeschichte der Blütenpflanzen Mitteleuropas (eds. Kirchner, O. V., Loew, E., & Schroeter, C.) 2, 953–1146 (E. Ulmer, Stuttgart, 1937).Rybalka, I. A. Relationship between density of the white mistletoe (Viscum album L.) and some landscape and environmental characteristics of urban areas in the case of Kharkiv. Ekologicheskiy Vestnik 1, 87–97 (2017).
    Google Scholar 
    Patykowski, J. & Kołodziejek, J. Comparative analysis of antioxidant activity in leaves of different hosts infected by mistletoe (Viscum album L. subsp. album). Arch. Biol. Sci. 65, 851–861 (2013).Article 

    Google Scholar 
    Skrypnik, L., Maslennikov, P., Feduraev, P., Pungin, A. & Belov, N. Ecological and landscape factors affecting the spread of European mistletoe (Viscum album L.) in urban areas (A Case Study of the Kaliningrad City, Russia). Plants 9, 394 (2020).PubMed Central 
    Article 

    Google Scholar 
    Kunick, W. Veränderungen von Flora und Vegetation einer Grosstadt dargestellt am Beispiel von Berlin (West). PhD Thesis, Technische Universität (1974). [In German].Kołodziejek, J., Patykowski, J. & Kołodziejek, R. Distribution, frequency and host patterns of European mistletoe (Viscum album subsp. album) in the major city of Lodz Poland. Biol. 68, 55–64 (2013).
    Google Scholar 
    Caudullo, G., Welk, E. & San-Miguel-Ayanz, J. Chorological maps for the main European woody species. Data Brief 12, 662–666 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    O’Donnell, M. S. & Ignizio, D. A. Bioclimatic predictors for supporting ecological applications in the conterminous United States. US Geol. Surv. Data Ser. 691, 4–9 (2012).
    Google Scholar 
    Luther, P., Becker, H. & Leroi, R. Die Mistel: Botanik, Lektine, medizinische Anwendung. Springer (1987).Gazol, A. et al. Distinct effects of climate warming on populations of silver fir (Abies alba) across Europe. J. Biogeogr. 42, 1150–1162 (2015).Article 

    Google Scholar 
    Tikkanen, O. P. et al. Freezing tolerance of seeds can explain differences in the distribution of two widespread mistletoe subspecies in Europe. For. Ecol. Manag. 482, 118806 (2021).Article 

    Google Scholar 
    Pilichowski, S. et al. Wpływ Viscum album ssp. austriacum (Wiesb.) Vollm. na przyrost radialny Pinus sylvestris L. Sylwan 162, 452–459 (2018) ([In Polish]).
    Google Scholar 
    Szmidla, H., Tkaczyk, M., Plewa, R., Tarwacki, G. & Sierota, Z. Impact of common mistletoe (Viscum album L.) on scots pine forests—A call for action. Forests 10, 847 (2019).Article 

    Google Scholar 
    Wójcik, R. & Kędziora, W. Abundance of Viscum in central Poland: Results from a large-scale mistletoe inventory. Environ. Sci. Proc. 3, 98 (2020).
    Google Scholar 
    Sangüesa-Barreda, G., Linares, J. C. & Camarero, J. J. Drought and mistletoe reduce growth and water-use efficiency of Scots pine. For. Ecol. Manag. 296, 64–73 (2013).Article 

    Google Scholar 
    Mathiasen, R. L., Nickrent, D. L., Shaw, D. C. & Watson, D. M. Mistletoes: Pathology, systematics, ecology, and management. Plant Dis. 92, 988–1006 (2008).PubMed 
    Article 

    Google Scholar 
    Catal, Y. & Carus, S. Effect of pine mistletoe on radial growth of crimean pine (Pinus nigra) in Turkey. J. Environ. Biol. 32, 263 (2011).PubMed 

    Google Scholar 
    Skre, O. High temperature demands for growth and development in Norway Spruce [Picea abies (L.) Karst.] in Scandinavia. Meld Nor Landbrukshøgsk 51, 1–29 (1971).
    Google Scholar 
    Utaaker, K. A temperature-growth index—the respiration equivalent—used in climatic studies on the meso-scale in Norway. Agric. Meteorol. 5, 351–359 (1968).Article 

    Google Scholar 
    Iversen, J. Viscum, Hedera and Ilex as climate indicators: A contribution to the study of the post-glacial temperature climate. Geol. fören. Stockh. förh. 66, 463–483 (1944).Article 

    Google Scholar 
    Briggs, J. Mistletoe, Viscum album (Santalaceae), in Britain and Ireland; a discussion and review of current status and trends. Brit. Ir. Bot. 3, 419–454 (2021).
    Google Scholar  More

  • in

    Early-season plant-to-plant spatial uniformity can affect soybean yields

    Sites description and field operationsA total of six field studies were conducted in two different regions over two seasons. Four studies (two dryland and two irrigated) were in Kansas, United States (dryland: 39°4′30″ N, − 96°44′43″ W, irrigated: 39°4′25″N, − 96°43′12″ W) during the 2019 and 2020 growing seasons (hereafter referred to as USDry19, USIrr19, USDry20, and USIrr20 studies). The remaining two studies (dryland) were in Entre Rios, Argentina (31°50′49″ S; 60°32′16″ W) during the 2018/2019 and 2019/2020 growing seasons (hereafter referred to as Arg19 and Arg20 studies). The soils were Fluventic Hapludolls [silt loam, 40% sand, 13% clay, 47% silt, organic matter (OM) 1.7%, 7.7 pH, 31.1 ppm P (Bray−1)] at the US dryland studies, and Pachic Argiudolls [silty clay loam, 10.1% sand, 30.6% clay and 59.3% silt, OM 3.2%, 6.8 pH, 34.7 ppm P (Bray−1)] at the US irrigated studies. At the Argentinian studies soil was a Vertic Argiudoll in 2019 [silty clay loam to clay loam, 3.9% sand, 27.6% clay, 67.9% silt, OM 2.65%, 7.2 pH, 12.5 ppm P (Bray−1)] and an Acuic Argiudoll in 2020 [silt loam to silty-clay-loam, 5.6% sand, 28.6% clay, 65.8% silt, OM 3.33%].The US dryland and irrigated studies were sown on June 4, 2019, and May 20, 2020. In 2019, the dryland study was replanted on June 29 due to poor emergence after the first sowing. The studies in Argentina were sown on December 5 in 2018 and November 20 in 2019. At all six studies, plots were kept free of weeds, pests, and diseases through recommended chemical control.The genotypes used in the US were P40A47X (MG 4.0) and P39A58X (MG 3.9) (Corteva Agriscience, Johnston, IA, USA) in 2019 and 2020, respectively. Both varieties are tolerant to glyphosate and dicamba herbicides (RR2X) and have low lodging probability. For the northeast region of Kansas, recommended sowing dates range from May 15 to June 15 along with MG 421. In addition, recommended seeding rates are between 270 and 355 thousand seeds ha−1 for low-yielding environments and 190 to 285 thousand seeds ha−1 for medium- and high-yielding environments13. In Argentina, the genotype AW5815IPRO (MG 5.8, Bayer, Leverkusen, Germany) was used both in 2020 and 2021, it is tolerant to glyphosate and sulfonylureas, and has low lodging probability. Recommended sowing dates for Entre Rios considering soybeans as a single crop range from October 20 to December 10, and MG usually range from 4 to 6; lastly, seeding rate recommendations are between 200 and 250 thousand seeds ha−1 in the region22.Study designThe studies carried out in the US were arranged as a split plot design with three replicates in both 2019 and 2020. In 2019, the main plot treatment factor was planter type with two levels [John Deere (Moline, Illinois, US) Max Emerge planter (ME, 12 rows), and John Deere Exact Emerge Planter (EE, 16 rows)], and the split-plot treatment factor was seeding rate with two levels (160 and 321 thousand seeds ha−1). In 2020 the main plot treatment factor was also planter type with two levels (ME and EE), and the split-plot treatment factor was seeding rate with four levels (160, 215, 270 and 321 thousand seeds ha−1). Planting speed was 7 km h−1 in both studies and years, plots were 24 and 32 rows wide when planted with ME and EE, respectively, with 0.76 m row spacing. Plot length was 80 m in the dryland studies and 160 m in the irrigated studies. The studies in Argentina were arranged as a single replicate of each seeding rate (100, 230, 360 and 550 thousand seeds ha−1) in both years. Planting speed was 5.5 km h−1 in both years, and plots were 10 rows wide with 0.52 m row spacing and 350 m in length.All treatment factors in US studies were evaluated with the overall goal of producing substantial variation in the variable of interest, plant-to-plant spatial uniformity, rather than to make an inference of their effect on yield. The Argentinian studies were only used for selection of stand uniformity variables due to the single replicate. Plant spatial uniformity variables were first fitted using the data from US studies (details below), and then the best explanatory metrics were selected to re-fit the relationships combining both data sets from US and Argentina. Finally, sowing dates, maturity groups, and seeding rates evaluated in this study at both locations (Arg and US) were aligned with those recommended for each region.Data collection and spacing uniformity variablesTwo segments of 2 m in length were established early in the season inside each plot. At the V5 (US studies) and R1 (Arg studies) soybean development stage23, the cumulative distance of the plants within each segment was measured and then used to calculate multiple derived variables. Plant spacing (cm) was calculated as the average distance between neighboring plants. In addition, the distance from a plant to each neighboring plant was classified as shorter or longer than the plant spacing (named nearest and farthest neighbor distance, respectively). Achieved versus Target Evenness Index (ATEI, dimensionless) was calculated as the ratio between the observed plant spacing and the theoretical plant spacing (TPS, cm), where TPS is the expected plant spacing derived from a specific seeding rate and row width (Eq. 1).$$ATEI = frac{Spacing;(cm) }{{TPS;(cm)}}$$
    (1)
    The ATEI index was designed to account for the proximity of the observed plant spacing to the TPS. Values closer to 1 indicate that the plant spacing is close to the TPS and values that are below or above 1 indicate that the plant spacing is lower or higher than the TPS, respectively; thereby departing from an ideal plant spacing. Hence, ATEI values greater than 1 depict both (i) non-uniform plant-to-plant spacing distribution and (ii) plant densities below the target (seeding rate). To further understand the meaning of ATEI, the relative density (rd) was calculated as the ratio between plant density (based on the number of plants in the 2 m segment) and seeding rate.To account for the unevenness of distance from a plant to both neighboring plants within the row, we used the Evenness Index (EI, dimensionless), calculated as the ratio between the distance to the nearest neighbor (cm) and the plant spacing (cm) of a given plant (Eq. 2). The Evenness Index values range from 0 to 1, a value closer to 1 indicates that a plant is equidistantly spaced to both of its neighboring plants within the row, if zero then those plants are occupying the same position (as doubles). It is important to note that EI does not provide information on the spacing (in distance, cm) or how close the spacing is compared to the TPS, but only describes the unevenness distance of a plant to its neighboring plants within a row.$$Evenness ;Index; (EI) = frac{nearest; neighbor ;(cm)}{{Spacing; (cm)}}$$
    (2)
    In addition, the distance from a plant to its preceding neighboring plant, and the TPS were used to classify the position of each plant into one of eight classes (Fig. 1). Plants were classified in classes ranging from “double” (preceding plant distance  Double-skip) as a function of seeding rate, planter type and their interaction (fixed effects), and block nested in site-year (random effect) (Tables 1 and 2). Independent models for each of the 4 US studies were built assessing the effects of planter type, seeding rate, and their interaction (fixed effects), and seeding rate nested in planter type, and in block (random effects) on the same variables previously mentioned (Supplementary Table 1). The models were run using the lmer function from lme4 package in R (R Core Team, 2021). In addition, the US and Arg studies were combined to evaluate the effect of site-year on yield, plant density, and all stand uniformity variables (Supplementary Fig. 1) using the lm function from package stats. Means separation were performed using Fisher’s LSD (Least Significance Difference) test (alpha = 0.05) with emmeans function from package emmeans.Table 1 Effect of planter type, seeding rate, and their interaction on variables from plant position classification for all US studies. References: percentage of perfectly spaced plants (Perfect), percentage of plants misplaced by 66% (Mis 66), percentage of plants misplaced by 33% (Mis 33), percentage of double plants (Double), percentage of short skips plants (Short-skip), percentage of long skip plants (Long-skip), percentage of double skips plants (Double-skip), and percentage of greater than double skip plants ( > Double-skip).Full size tableTable 2 Effect of planter type, seeding rate, and their interaction on yield and stand uniformity variables for all US studies. References: Spacing between plants standard deviation (Spacing sd), achieved versus targeted evenness index mean and standard deviation (ATEI and ATEI sd, respectively), and evenness index mean and standard deviation (EI and EI sd, respectively).Full size tableCommunity-scale data from the four US studies were combined and fitted to bivariate linear regression models with yield as the response variable and each of the stand spatial uniformity variables as the explanatory variable. Significant models (alpha = 0.05) were further evaluated by calculating the coefficient of determination (R2) and root mean squared error (RMSE) (Fig. 2). Models with the lower RMSE and higher R2 were selected as those that best captured the effect of non-uniform stands on soybean yield. After variables were selected, both US and Arg data sets were combined and the linear regressions between the selected variables and yield were re-fitted to assess the consistency of the relationships when an independent data set was included. Community-scale yield from US and Arg studies was modelled as a function of the selected stand uniformity variable, country (US and Arg), and their interaction (fixed effects) (Fig. 3). The spatial uniformity metric showing the most consistent relationship for both US and Arg studies (i.e., non-significant interaction between stand uniformity metric and country), was selected to continue the analysis. The bivariate linear regression models were run with function lm.Figure 2Relationship between stand uniformity variables and soybean yield for US studies. ATEI mean and sd achieved versus targeted evenness index mean and standard deviation, EI mean and sd evenness index mean and standard deviation, Perfect percentage of perfectly spaced plants, R2 coefficient of determination, RMSE root mean square error. All stand uniformity variables presented a significant slope at alpha = 0.05.Full size imageFigure 3Relationship of spacing standard deviation (Spacing sd, cm) and achieved versus targeted evenness index standard deviation (ATEI sd) to soybean yield. Different colors and line types denote different countries (Argentina, Arg—full line, red points; United States, US—dashed line, blue points). R2 coefficient of determination, RMSE root mean square error.Full size imageDifferent environmental conditions and seeding rate levels may modify the effect of plant spatial uniformity on yield. To explore this, each of the studies from Arg and US were separated into low- (USDry19 and ArgDry20, mean of 2.7 Mg ha−1), medium- (USIrr19, USDry20 and ArgDry19, mean of 3.0 Mg ha−1), and high- (USIrr20, mean of 4.3 Mg ha−1) yield environments based on the effect of site-year on yield (Supplementary Fig. 1). Additionally, the tested seeding rates were separated in low ( 300 thousand seeds ha−1) levels based on the current optimal seeding rate for medium yielding environments (235 thousand seeds ha−1, 4 Mg ha−1)13 and the extreme values proposed by Suhre et al.11 (148 and 445 thousand seeds ha−1). This classification was used to model yield as a function of (i) the selected stand uniformity metric, yield environment, and their interaction, and (ii) the selected stand uniformity metric, seeding rate levels, and their interaction. These models were tested to obtain a robust conclusion on the overall effect of yield environment and seeding rate levels, and their interactions (all treated as fixed effects) with plant-to-plant spatial uniformity relative to the response variable, soybean yield. The Akaike information criteria (AIC) was used to compare the full (with interactions) relative to the reduced models (single effects).Ethics declarationsExperimental research and field studies on plants including the collection of plant material, complied with relevant institutional, national, and international guidelines and legislation. More

  • in

    Independent origin of large labyrinth size in turtles

    Steinhausen, W. Über die Beobachtungen der Cupula in den Bogengangsampullen des Labyrinthes des Lebendes Hechts. Pflug. Arch. 232, 500–512 (1933).Article 

    Google Scholar 
    Wever, E. G. The reptile ear. (Princeton University Press, 1978).Wilson, V. J. & Melvill Jones, G. Mammalian vestibular physiology. (Plenum Press, 1979).Spoor, F. & Zonneveld, F. Comparative review of the human bony labyrinth. Yearb. Phys. Anthropol. 41, 211–251 (1998).Article 

    Google Scholar 
    Rabbitt, R. D., Damiano, E. R. & Grant, J. W. Biomechanics of the semicircular canals and otolith organs. In: Highstein, F. M., Ray, R. R., Popper, A. N. (eds) Springer Handbook Of Auditory Research, vol. 19, The Vestibular System, pp. 153–201 (Springer, New York, 2004).Georgi, J. A. & Sipla, J. S. Comparative and functional anatomy of balance in aquatic reptiles and birds. In: Thewissen, J. G. M., Nummela, S. (eds) Sensory Evolution On The Threshold, Adaptations In Secondarily Aquatic Vertebrates.pp. 233–256 (University of California Press, 2008).David, R. et al. Motion from the past. A new method to infer vestibular capacities of extinct species. C. R. Palevol. 9, 397–410 (2010).Article 

    Google Scholar 
    Oman, C. M., Marcus, E. N. & Curthoys, I. S. The influence of the semicircular canal morphology on endolymph flow dynamics. Acta Otolaryngol. 103, 1–13 (1987).CAS 
    PubMed 
    Article 

    Google Scholar 
    Georgi, J. A., Sipla, L. S. & Forster, C. A. Turning semicircular canal function on its head: dinosaurs and a novel vestibular analysis. PLoS One 8, e58517 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Spoor, F., Bajpai, S., Hussain, S. T., Kumar, K. & Thewissen, J. G. M. Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417, 163–166 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Spoor, F. et al. The primate semicircular canal system and locomotion. Proc. Nat. Acad. Sci. USA 104, 10808–10812 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cox, P. G. & Jeffery, N. Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids and modern humans. J. Anat. 213, 83–596 (2008).
    Google Scholar 
    Cox, P. G. & Jeffery, N. Semicircular canals and agility: the influence of size and shape measures. J. Anat. 216, 37–47 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Silcox, M. T. et al. Semicircular canal system in early primates. J. Hum. Evol. 56, 315–327 (2009).PubMed 
    Article 

    Google Scholar 
    Lebrun, R. et al. Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J. Anat. 216, 368–380 (2010).PubMed 
    Article 

    Google Scholar 
    Billet, G. et al. High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths. Proc. R. Soc. Lond. B. 279, 3932–3939 (2012).
    Google Scholar 
    Gunz, P., Ramsier, M., Kuhrig, M., Hublin, J.-J. & Spoor, F. The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. J. Anat. 220, 529–543 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Malinzak, M. D., Kaya, R. F. & Hullar, T. E. Locomotor head movements and semicircular canal morphology in primates. Proc. Natl Acad. Sci. USA 109, 914–919 (2012).Article 

    Google Scholar 
    Alloing-Séguier, L. et al. The bony labyrinth in diprotodontian marsupial mammals: diversity in extant and extinct forms and relationships with size and phylogeny. J. Mamm. Evol. 20, 191–198 (2013).Article 

    Google Scholar 
    Berlin, J. C., Kirk, E. C. & Rowe, T. B. Functional implications of ubiquitous semicircular canal non-orthogonality in mammals. PLoS One 8, e79585 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Davies, K. T. J., Bates, P. J. J., Maryanto, I., Cotton, J. A. & Rossiter, S. J. The evolution of bat vestibular systems in the face of potential antagonistic selection pressures for flight and echolocation. PLoS One 8, e61998 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Grohé, C. et al. Bony labyrinth shape variation in extant Carnivora: a case study of Musteloidea. J. Anat. 228, 366–383 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pfaff, C., Martin, T. & Ruf, I. Bony labyrinth morphometry indicates locomotor adaptations in the squirrel-related clade (Rodentia, Mammalia). Proc. R. Soc. B 282, 20150744 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Melville Jones, G. & Spells, K. E. A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc. R. Soc. Lond. B Biol. Sci. 157, 403–419 (1963).ADS 
    Article 

    Google Scholar 
    Kemp, A. D. & Kirk, E. C. Eye size and visual acuity influence vestibular anatomy in mammals. Anat. Rec. 297, 781–790 (2014).Article 

    Google Scholar 
    Ekdale, E. G. Form and function of the mammalian ear. J. Anat. 228, 324–337 (2016).PubMed 
    Article 

    Google Scholar 
    Goyens, J. High ellipticity reduces semicircular canal sensitivity in squamates compared to mammals. Sci. Rep. 9, 16428 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Witmer, L. M., Chatterjee, S., Franzosa, J. & Rowe, T. Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425, 950–953 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Lautenschlager, S., Rayfield, E. J., Altangerel, P., Zanno, L. E. & Witmer, L. M. The endocranial anatomy of Therizinosauria and its implications for sensory and cognitive function. PLoS ONE 7, e52289 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cuthbertson, R. S., Maddin, H. C., Holmes, R. B. & Anderson, J. S. The braincase and endosseous labyrinth of Plioplatecarpus peckensis (Mosasauridae, Plioplatecarpinae), with functional implications for locomotor behavior. Anat. Rec. 298, 1597–1611 (2015).Article 

    Google Scholar 
    Schade, M., Rauhut, O. W. M. & Evers, S. W. Neuroanatomy of the spinosaurid Irritator challengeri (Dinosauria: Theropoda) indicates potential adaptations for piscivory. Sci. Rep. 10, 9259 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Benson, R. B. J., Starmer-Jones, E., Close, R. A. & Walsh, S. A. Comparative analysis of vestibular ecomorphology in birds. J. Anat. 231, 990–1018 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dudgeon, T. W., Maddin, H. C., Evans, D. C. & Mallon, J. C. The internal cranial anatomy of Champsosaurus (Choristodera: Champsosauridae): implications for neurosensory function. Sci. Rep. 10, 7122 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bronzati, M. et al. Deep evolutionary diversification of semicircular canals in archosaurs. Curr. Biol. 31, 2520–2529 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hansen, M., Hoffman, E. A., Norell, M. A. & Bhullar, B.-A. S. The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization. Science 372, 601–609 (2021).ADS 
    Article 

    Google Scholar 
    Ernst, C. H. & Barbour, R. W. Turtles Of The World. (Smithsonian Institution Press, Washington, D.C., 1989).Evers, S. W. & Benson, R. B. J. A new phylogenetic hypothesis of turtles with implications for the timing and number of evolutionary transitions to marine lifestyles in the group. Palaeontology 62, 93–134 (2019).Article 

    Google Scholar 
    Joyce, W. G. A review of the fossil record of basal Mesozoic turtles. Bull. Peabody Mus. Nat. Hist. 58, 65–113 (2017).Article 

    Google Scholar 
    Lautenschlager, S., Ferreira, G. S. & Werneburg, I. Sensory evolution and ecology of early turtles revealed by digital endocranial reconstructions. Front. Ecol. Evol. 6, 1–7 (2018).Article 

    Google Scholar 
    Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 123, 1–15 (1985).Article 

    Google Scholar 
    Sugiura, N. Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun. Stat. Theory Methods 7, 13–26 (1978).MATH 
    Article 

    Google Scholar 
    Foth, C. et al. Comparative analysis of the shape and size of the middle ear cavity of turtles reveals no correlation with habitat ecology. J. Anat. 235, 1078–1097 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Neenan, J. M. et al. Evolution of the sauropterygian labyrinth with increasingly pelagic lifestyles. Curr. Biol. 27, 3852–3858 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Loza, C. M., Latimer, A. E., Sánchez-Villagra, M. R. & Carlini, A. A. Sensory anatomy of the most aquatic of carnivorans: the Antarctic Ross seal, and convergences with other mammals. Biol. Lett. 13, 20170489 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Werneburg, I. & Maier, W. Diverging development of akinetic skulls in cryptodire and pleurodire turtles: an ontogenetic and phylogenetic study. Vertebr. Zool. 69, 113–143 (2019).
    Google Scholar 
    Ferreira, G. S. & Werneburg, I. Evolution, diversity, and development of the craniocervical system in turtles with special reference to jaw musculature. In: Ziermann, J., Diaz, R. R. Jr, Diogo, R. (eds) Heads, Jaws and Muscles: Evolution, Development, Anatomical Diversity And Function (Springer, Cham, 2019).David, R. J. A. et al. Comment on “The early origin of a birdlike inner ear and the evolution of dinosaurian movement and vocalization”, Science (in press).Schwab, J. A. et al. Inner ear sensory system changes as extinct crocodylomorphs transitioned from land to water. Proc. Nat. Acad. Sci. USA 117, 10422–10428 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yang, L. M. & Ornitz, D. M. Sculpturing the skull through neurosensory epithelial-mesenchymal signaling. Dev. Dyn. 248, 88–97 (2019).PubMed 
    Article 

    Google Scholar 
    Kandel, B. M. & Hullar, T. E. The relationship of head movements to semicircular canal size in cetaceans. J. Exp. Biol. 213, 1175–1181 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Moll, D. Food and feeding behavior of the turtle, Dermatemys mawei, in Belize. J. Herpetol. 23, 445–447 (1989).Article 

    Google Scholar 
    Evers, S. W. et al. Neurovascular anatomy of the protostegid turtle Rhinochelys pulchriceps and comparisons of membranous and endosseous labyrinth shape in an extant turtle. Zool. J. Linn. Soci. 187, 800–828 (2019).
    Google Scholar 
    Ekdale, E. G. Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS One 8, e66624 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Joyce, W. G. Phylogenetic relationships of Mesozoic turtles. Bull. Peabody Mus. Nat. Hist. 48, 3–102 (2007).Article 

    Google Scholar 
    Sterli, J. & De La Fuente, M. S. Anatomy of Condorchelys antiqua Sterli, 2008, and the origin of the modern jaw closure mechanism in turtles. J. Vertebr. Paleontol. 30, 351–366 (2010).Article 

    Google Scholar 
    Ferreira, G. S. et al. Feeding biomechanics suggests progressive correlation of skull architecture and neck evolution in turtles. Sci. Rep. 10, 5505 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Aerts, P., Van Damme, J. & Herrel, A. Intrinsic mechanics and control of fast cranio-cervical movements in aquatic feeding turtles. Am. Zool. 41, 1299–1310 (2001).
    Google Scholar 
    Herrel, A., Van Damme, J. & Aerts, P. Cervical anatomy and function in turtles. In Biology Of Turtles. In: Wyneken, J., Godfrey, M. H., Bels, V. (eds) pp. 163–185 (CRC Press, Boca Raton, 2008).Narazaki, T., Sato, K., Abernathy, K. J., Marshall, G. J. & Miyazaki, N. Loggerhead turtles (Caretta caretta) use vision to forage on gelatinous prey in mid-water. PLoS One 8, e66043 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Guthrie, D. M. “Role of vision in fish behaviour”. In: T. J. Pitcher (eds) The Behaviour Of Teleost Fishes. pp. 75–113 (Springer, Boston, 1986).Sterli, J. & Joyce, W. G. The cranial anatomy of the Early Jurassic turtle Kayentachelys aprix. Acta Paleontol. Pol. 52, 675–694 (2007).
    Google Scholar 
    Werneburg, I. The tendinous framework in the temporal skull region of turtles and considerations about its morphological implications in amniotes: a review. Zool. Sci. 30, 141–153 (2013).Article 

    Google Scholar 
    Werneburg, I. Neck motion in turtles and its relation to the shape of the temporal skull region. C. R. Palevol. 14, 527–548 (2015).Article 

    Google Scholar 
    TTWG, Turtle Taxonomy Working Group, Rhodin, A. G. J. et al. Turtles of the world, 8th edition: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chelonian Res. Monogr. 7, 1–292 (2017).
    Google Scholar 
    Gower, J. C. Generalized Procrustes analysis. Psychometrika 40, 33–50 (1975).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Adams, D. C., Collyer, M. L., Kaliontzopoulou, A. Geomorph: Software for geometric morphometric analyses. R package version 3.1.0. https://cran.r-project.org/package=geomorph (2019).R Core Team, R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/ (2019).Rholf, E. J. & Corti, M. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753 (2000).Article 

    Google Scholar 
    Adams, D. C. & Felice, R. N. Assessing trait covariation and morphological integration on phylogenies using evolutionary covariance matrices. PLoS One 9, e94335 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kendall, D. G. The diffusion of shape. Adv. Appl. Probab. 9, 428–430 (1977).Article 

    Google Scholar 
    Bookstein, F. L. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1, 97–118 (1997).Article 

    Google Scholar 
    Gunz, P., Mitteroecker, P. & Bookstein, F. L. “Semilandmarks in three dimensions. In: Slice, D. E. (ed) Modern Morphometrics in Physical Anthropology, pp. 73–98 (Kluwer Academic, 2005).Webster, M. & Sheets, H. A practical introduction to land- mark-based geometric morphometrics. In: Alroy, J., Hunt, G. (eds) Quantitative Methods in Paleobiology. Paleontological Society Papers 16, pp. 163–188 (Paleontological Society, 2010).Gunz, P. & Mitteroecker, P. Semilandmarks: a method for quantifying curves and surfaces. Hystrix 24, 103–109 (2013).
    Google Scholar 
    Bookstein, F. L. Size and shape spaces for landmark data in two dimensions. Stat. Sci. 1, 181–242 (1986).MATH 

    Google Scholar 
    Pereira, A. G., Sterli, J., Moreira, F. R. R. & Schrago, C. G. Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Mol. Phylogenet. Evol. 113, 59–66 (2017).PubMed 
    Article 

    Google Scholar 
    Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).Article 

    Google Scholar 
    Lloyd, G. T. Estimating morphological diversity and tempo with discrete character-taxon matrices: implementation, challenges, progress, and future directions. Biol. J. Linn. Soc. 118, 131–151 (2016).Article 

    Google Scholar 
    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ferreira, G. S., Bronzati, M., Langer, M. C. & Sterli, J. Phylogeny, biogeography, and diversification patterns of side-necked turtles (Testudines: Pleurodira). R. Soc. Open Sci. 5, 171773 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bapst, D. W. A stochastic rate-calibrated method for time-scaling phylogenies of fossil taxa. Methods Ecol. Evol. 4, 724–733 (2013).Article 

    Google Scholar 
    Laurin, M. The evolution of body size, Cope’s Rule and the origin of amniotes. Syst. Biol. 53, 594–622 (2004).PubMed 
    Article 

    Google Scholar 
    Pace, C. M., Blob, R. W. & Westneat, M. W. Comparative kinematics of the forelimb during swimming in red-eared slider (Trachemys scripta) and spiny softshell (Apalone spinifera) turtles. J. Exp. Biol. 204, 3261–3271 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Claude, J., Paradis, E., Tong, H. & Auffray, J.-C. A geometric morphometric assessment of the effects of environment and cladogenesis on the evolution of the turtle shell. Biol. J. Linn. Soc. 79, 485–501 (2003).Article 

    Google Scholar 
    Angielczyk, K. D., Feldman, C. R. & Miller, G. R. Adaptive evolution of plastron shape in emydine turtles. Evolution 65, 377–394 (2011).PubMed 
    Article 

    Google Scholar 
    Angielczyk, K. D., Burroughs, R. W. & Feldman, C. R. Do turtles follow the rules? Latitudinal gradients in species richness, body size, and geographic range area of the World’s turtles. J. Exp. Zool. Mol. Dev. Evol. 324, 270–294 (2015).Article 

    Google Scholar 
    Pritchard, P. C. H. Oiscivory in turtles, and evolution of the long-necked Chelidae. Symp. Zool. Soc. Lond. 52, 87–110 (1984).
    Google Scholar 
    Joyce, W. G. et al. A new pelomedusoid turtle, Sahonachelys mailakavava, from the Late Cretaceous of Madagascar provides evidence for convergent evolution of specialized suction feeding among pleurodires. R. Soc. Open Sci. 8, 210098 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Adams, D. C. A method for assessing phylogenetic least squares models for shape and other high‐dimensional multivariate data. Evolution 68, 2675–2688 (2014).PubMed 
    Article 

    Google Scholar 
    Adams, D. C., Collyer, M. L. & Kaliontzopoulou, A. Multivariate phylogenetic comparative methods: evaluations, comparisons, and recommendations. Syst. Biol. 67, 14–31 (2018).PubMed 
    Article 

    Google Scholar 
    Collyer, M. L., Sekora, D. J. & Adams, D. C. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115, 357–365 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lowi-Merri, T. M., Benson, R. B. J., Claramunt, S. & Evans, D. C. The relationship between sternum variation and mode of locomotion in birds. BMC Biol. 19, 1–23 (2021).Article 

    Google Scholar 
    Adams, D. C. & Collyer, M. L. Phylogenetic ANOVA: group-clade aggregation, biological challanges, and a refined permutation procedure. Evolution 72, 1204–1215 (2018).PubMed 
    Article 

    Google Scholar 
    Friedman, S. T., Martinez, C. M., Price, S. A. & Wainwright, P. C. The influence of size on body shape diversification across Indo-Pacific shore fishes. Evolution 73, 1873–1884 (2019).PubMed 
    Article 

    Google Scholar 
    Foth, C., Rabi, M. & Joyce, W. G. Skull variation in extant and extinct Testudinata and its relation to habitat and feeding ecology. Acta Zool. 98, 310–325 (2017).Article 

    Google Scholar 
    Grafen, A. The phylogenetic regression. Philos. Trans. R. Soc. Lond. B Biol. Sci. 326, 119–157 (1989).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ritz, C. & Spiess, A.-N. qpcR: an R package for sigmoidal model selection in quantitative real-rime polymerase chain reaction analysis. Bioinformatics 24, 1549–1551 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Akaike, H. Information Theory As An extension Of The Maximum Likelihood Principle. In: Petrov, B. N., Csaki, F. (eds) Second International Symposium on Information Theory, pp. 267–281 (Akademiai Kiado, New York, 1973).Burnham, K. P., Anderson, D. Model selection and multi-model inference: a practical information-theoretic approach. (Springer, New York, 2002).Nagelkerke, N. J. D. A note on a general definition of the coefficient of determination. Biometrika 78, 691–692 (1991).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D., R. Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–141, URL: https://CRAN.R-project.org/package=nlme. (2019).Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Racicot, R. A. & Colbert, M. W. Morphology and variation in porpoise (Cetacea: Phocoenidae) cranial endocasts. Anat. Rec. 296, 979–992 (2013).Article 

    Google Scholar 
    Evers, S. W. Code and Data to “Independent origin of large labyrinth size in turtles”. Zenodo https://doi.org/10.5281/zenodo.7024572 (2022).Article 

    Google Scholar  More

  • in

    Towards an absolute light pollution indicator

    DefinitionWe present here a new statistical approach to measure and characterize light pollution. The objective is to define an indicator which is not limited to clear sky measurements and does not require a precise calibration of a photometer. The key attributes of the indicator are the following:

    It requires the automated acquisition of a large number of zenithal NSB measures when the Sun is below (-18^{circ }) and the Moon below (-5^{circ });

    The acquisitions must at least cover a period of 6 months in order to record a wide range of possible weather conditions from perfectly clear to totally overcast skies. The objective is to obtain a significant sample of every type of cloud conditions (e.g. cloud density and ceiling altitude) as well as a good characterization of the average clear sky ;

    It is based on the analysis of the zenithal NSB measure dispersion which is directly linked to the level of light pollution a site experiences.

    As presented above in Fig. 2, the NSB density histograms, which are assembled from a large number of NSB measures, display a higher density zone which denotes a characteristic clear sky level that we name nominal NSB in the scope of the indicator calculation. On both sides of the clear sky level (above and below), NSB measures are distributed in a way that reflect the zenithal night sky luminance in cloudy conditions: NSB measures above the clear sky level mean that the light pollution is amplified by clouds while those below the clear sky level indicate a darker environment where clouds mask light pollution from distant sources as well as natural light sources. The calculation of the indicator is based on the evaluation of the NSB measure dispersion on both sides of the nominal NSB (i.e. characteristic clear sky level). Since there can have strong variations of artificial light emitted into the environment at the beginning and end of the night (decrease then increase of human activity, extinction of public lighting, etc.), the range of NSB measures retained for calculating the indicator is restricted to a portion in the middle of the night, typically 2 h.Figure 8 shows a typical NSB density histogram for a site which is quite severely impacted by light pollution. It covers a 2 h time range between 23:00 UTC and 01:00 UTC and one can easily see that the zone above the nominal NSB is much higher and denser than the one below, i.e. cloud conditions create more often a brighter environment than a darker one and with a greater amplitude.Figure 8NSB density histogram where the nominal NSB that represents the most common clear sky conditions is identified. It delimits two areas, the NSB bright dispersion above the nominal NSB and the NSB dark dispersion below.Full size imageBased on the determination of the nominal NSB, a quantitative indicator, called NDR for NSB Dispersion Ratio, is calculated in the following way:$$begin{aligned} NDR = (N_b cdot MAD_b) / (N_d cdot MAD_d) end{aligned}$$where (N_b) is the number of measures above the nominal NSB (brighter sky), (N_d) is the number of measures below the nominal NSB (darker sky), (MAD_b) is the median absolute deviation of the measures in the bright dispersion zone (above the nominal NSB) and (MAD_d) is the median absolute deviation of the measures in the dark dispersion zone (below the nominal NSB). The median absolute deviation is a statistical tool used to measure the variability of a data set, which is exactly what we try to achieve with the two NSB extensions above and below the nominal NSB. It is formally defined as (MAD = median(|X_i – tilde{{mathbf {X}}}|)) where (X_i) in our case represents an NSB value and (tilde{{mathbf {X}}}) is (median(X_i)). The median absolute deviation is a better choice than the usual standard deviation to measure the spread of NSB measures since the data does not follow a normal distribution.In order to make the determination of the NSB Dispersion Ratio stronger from a statistical standpoint, we use a bootstrapping with replacement resampling method on the set of night portions used to compute the indicator. Assuming we have N night portions at our disposal, we randomly select a sample of N items in this set of night portions knowing that a given item can appear multiple times in the sample (hence the bootstrapping with replacement). The NDR value is then computed for the considered sample. This process is repeated 1000 times and the average NDR value if eventually computed. This average value represents the actual NDR indicator of the considered site.The NDR indicator takes into account both the number of NSB values on each side of the nominal NSB and the dispersion of these values. This is what makes it relevant as an indicator of light pollution which encompasses all kinds of meteorological conditions experienced at a particular site. On that aspect, it is therefore not an astronomical light pollution indicator since it is not focused on clear sky conditions. On the opposite, it requires to have a significant number of NSB measures in all sorts of cloudy conditions so that a valid NDR indicator can be derived.A key aspect of the NDR calculation methodology is to determine the level of the nominal NSB, i.e. the typical clear sky level, since it will be used to differentiate the NSB measures that go in each of the two sets to calculate the bright and dark dispersions. As we have seen earlier in the article, such a determination can be biased by natural light sources that raise or lower clear sky NSB at different times of the night. This can result into a “blurry” high density zone which makes the determination of the nominal NSB difficult or even impossible depending on the observation period. Based on the quantitative estimate of the different natural light sources presented above, the most important bias to address is the contribution of the Galactic plane. This contribution must be eliminated for all the NSB measures which are used to calculate the NDR indicator. In order to do that, Noxi, the Ninox processing software developed by DarkSkyLab, calculates for each NSB measure the corresponding Galactic plane and star fields contribution using the galactic coordinates of the zenith and integrating the combined flux of all stars in the field of view using the UCAC4 astrometry and photometry star catalogue. It is not possible to cancel the contribution of the airglow due to its unpredictable nature, but since it only appears in rare occasions, it is not seen as a problem and is ignored. Regarding the contribution of the zodiacal light, it is considered as minimal at the zenith and it is also ignored.As an example, Fig. 9 shows on the left an NSB density histogram where the Galactic plane bias has not been corrected in the data, and on the right the same data but with the Galactic plane bias corrected. It is easy to see that in the latter the nominal NSB is much easier to determine, providing a more accurate reference level to calculate the NDR indicator. Once the Galactic plane bias has been corrected, the nominal NSB is determined as the highest density zone of the NSB histogram. It must be noted that, as of today, all the NSB measures are corrected from the Galactic plane bias without regards to the presence of clouds or high levels of light pollution. This results into an additional source of inaccuracy that will be addressed in the future through the implementation of two heuristics within the Noxi software:

    1.

    A first heuristic will determine if a night portion is considered as having a clear sky or not so that the Galactic bias correction is applied only if the sky is clear. In order to do that, we have developed an indicator called the NSS (for Night Sky Stability). To determine the NSS for a full night of measures or just a night portion, we fit the NSB curve with a degree 10 polynomial and we then compute the difference between each NSB measure and it polynomial counterpart. As a result, we obtain a set of residuals. The variance of all the residuals defines the NSS for the considered NSB dataset. Below a given value, the sky is considered as clear knowing that the NSS indicator has been calibrated on several NSB data sets for which the corresponding weather conditions are known;

    2.

    A second heuristic will allow us to weight the Galactic bias correction to be applied to NSB measures according to their value. For non-polluted skies with high values of NSB, the full Galactic bias correction will be applied while below a certain NSB threshold (for instance 21 mag(_{mathrm{SQM}})/arcsec(^{2}) which corresponds roughly to the brightest parts of the Milky Way) no correction will be applied.

    Figure 9NSB density histograms of the same data set with no correction of the Galactic plane bias applied on the left and a full correction applied on the right.Full size imageThe NDR indicator is unitless since it is the ratio of two quantities with the same unit (mag(_{mathrm{SQM}})/arcsec(^{2})). For the data set presented in Fig. 9, the NDR value which is obtained is 25 (which is justified by the fact that the bright extension in the density histogram is much higher and denser than the dark extension). This denotes a quite high level of light pollution despite the fact that the nominal NSB is at a level of 21.6 mag(_{mathrm{SQM}})/arcsec(^{2}). This highlights the fact that there is not always a strict correlation between the typical clear sky NSB obtained for a given site and its NDR indicator, i.e. the presence of clouds decreases the NSB more than we could have expected just by knowing the clear sky NSB. On that respect, the NDR ratio brings more information that the clear sky NSB alone.In addition to provide an indicator which is representative of light pollution in all possible atmospheric conditions, the NDR provides a tool to compare locations in a more meaningful way than just using a set of standalone NSB evaluations. First it is not dependent of an inter-calibration between different systems and second its statistical nature makes it more robust when it comes to perform comparisons.NDR into practiceThe NDR indicator has been calculated for several different sites by DarkSkyLab during various projects in France that involved NSB measuring sessions in the field. To demonstrate some of the results that have been obtained, Fig. 10 provides the density histograms of 4 different sites which have quite different light pollution profiles.Figure 10NSB density histograms of 4 different sites used to compute the NDR indicator. The nominal NSB (which corresponds to the most common clear sky conditions) is noted with a white tick mark next to the vertical axis. Relative levels of the bright and dark dispersion terms (((N_b cdot MAD_b)) and ((N_d cdot MAD_d))) are noted respectively with an orange tick mark and a green tick mark. The computed values of the NDR indicator and nominal NSB are provided in the top-left corner of each figure.Full size imageTo build these diagrams, only the measures acquired during a few hours in the middle of the nights have been used to ensure the maximum stability of the NSB curves and avoid lighting extinctions that create large gaps in NSB profiles. The Galactic plane bias is corrected on all plots and the same NSB scale is used in order to perform comparisons between the 4 sites. One can notice that the number of measures and nights for the 4 sites are quite different. However, they are all sufficient to derive a meaningful value of the NDR indicator using the bootstrapping with replacement resampling method described above, but it is clear that the more NSB measures used, the more accurate the NDR indicator.Table 2 summarizes the NDR indicators as well as the nominal NSB for the 4 sites which are sorted in the order of decreasing NDR indicator values.Table 2 Summary of the nominal NSB and NDR indicators of the 4 different sites.Full size tableOne can see that the NDR indicator values are not strictly correlated to the nominal NSB values, e.g. despite the fact that the nominal NSB of site (a) is slightly better than the one of site (b), the NDR indicator value is much larger for site (a) than for site (b). This can be explained if we consider the specificities of each site:

    Cervières (a) is a small village in the Haut-Forez area, France, which is surrounded by large cities (Lyon, Saint-Etienne and Clermont-Ferrand at a distance between 50 to 80 km) and a closer mid-size city (Roanne at 30 km). At the top of that, the town of Noirétable and a large highway rest area are just 2 km away without any nocturnal extinction applied (as opposed to the village of Cervières itself for which public lighting is turned off from 23:00 to 05:00 local time). These conditions are favourable to the presence of a constant light pollution background which has a negative impact on the zenithal NSB measures in most cloudy conditions (distant large cities for high elevation clouds and Noirétable and the highway rest area for lower elevation clouds). Only rare cloud conditions actually protect the site from the effect of mid-distance light sources. In clear sky conditions, however, the fact that there is no close light sources provides reasonably good NSB levels;

    The Copernic Association Observatory (b) is located 6 km from the large town of Gap in the mountain area of Hautes-Alpes in the south of France. There is no significant short distant light sources but in many cloud conditions the contribution of Gap has a very negative impact on the zenithal luminance. However, due to the fact that the observatory is at a higher altitude on the hills surrounding the city of Gap, there are cloud conditions that make the site darker. In clear sky conditions, the proximity of Gap does not permit a quality better than that of a rural sky;

    The Astrièves Observatory (c) is located near the center of the small town of Gresse-en-Vercors in the Parc Naturel Régional du Vercors. There is a full nocturnal extinction of the village for a large part of the night resulting in a good sky quality in clear sky conditions. The large city of Grenoble is at a distance of 30 km in a valley at the north-east, and the two locations are separated by a few mountains which efficiently help masking the light pollution as soon as the cloud ceiling is below a certain altitude, resulting into a dark environment. On the opposite, high elevation clouds reflect the light from Grenoble and increase the zenithal luminance;

    Eourres (d) is a small and isolated village located 20 km west of Sisteron in the department of Hautes-Alpes, France, which is surrounded by mountains. There is no significant light sources closer than those of Sisteron and this results into a very good night sky quality with, most of the times, a very dark environment in cloudy conditions.

    Figure 11 provides a graphical representation of the NDR indicator values for the 4 sites. On the NDR scale, the value 1 indicates that the bright and dark dispersion terms (respectively ((N_b cdot MAD_b)) and ((N_d cdot MAD_d))) are equal, which means there is a balance between dark and bright conditions at the zenith on the considered site with reference to the most common clear sky level.Figure 11Summary of the NDR indicators obtained for the 4 sites. The diagram uses 1 as the pivotal value to delineate sites according to the two bright and dark dispersion terms ((N_b cdot MAD_b)) and ((N_d cdot MAD_d)).Full size imageThe NDR can theoretically vary between 0 (totally dark site) and several hundreds (extremely bright site) but in practice the best sites can reach NDR indicator values down to 0.3 in the best preserved locations and up to 200 for very large and polluted cities.Robustness of the NDR indicatorIt is important to evaluate how the NDR indicator is dependant on the number of measures used to compute it and to figure out what would be the minimum number of night sessions required to obtain a meaningful NDR indicator value at a given site. To achieve that, we have used the data from two of the four sites presented above (the two which have the largest number or recorded nights: Cervières with 424 nights and the Astrièves Observatory with 373 nights). The 1000-step bootstrapping procedure has been repeatedly executed on each data set with a regularly decreasing sample of nights: starting from the full number of nights, a decrement of 10 nights is applied at each step until only 20 nights are remaining. At every bootstrap step, each sample is composed of n nights randomly chosen among the N available ones knowing that any night can be selected several times.Figure 12 shows the NDR indicator values that have been obtained for each of the two sites as a function of the night sample considered. The 95% confidence interval is plotted against each NDR indicator value (it is preferred to the standard deviation since the NSB distribution in the data sets is not normal). In the right plot of Fig. 12, the last confidence interval for the 24 night sample is too wide to fit in the y-axis NDR range (the top value is 195).Figure 12Results of the NDR resampling on the two data sets of Cervières and Astrièves Observatory. The horizontal axis is the number of nights considered into the night sample and the vertical axis provides the NDR indicator obtained for each sampling set through a 1000-iteration bootstrapping with replacement calculation.Full size imageDiscussion on the required number of nightsWe can see in Fig. 12 that the NDR indicator and the confidence interval remain stable down to 200 nights. Below this threshold, the NDR starts to become unstable with growing confidence intervals. Based on this data, we can estimate that the minimum number of nights required to compute a robust NDR indicator is 200 (therefore between 7 and 8 months since there are periods around the full moons where there is no night portions recorded).However, depending on the measuring session objectives, the NDR indicator can be considered as accurate enough even when using a smaller number of nights. If the goal is simply to get a first estimate of the light pollution level at a given site, we can consider that 90 nights (a little more than 3 months of measures) are enough. On the opposite, if we want to perform a comparison between several sites for evaluating the impact of light pollution on a particular species, we might want to perform at least 200 nights of measurement to get a better accuracy for the NDR indicator. The experience from DarkSkyLab through many NSB measuring sessions is that 3 to 4 months of measures are required to get a meaningful density histogram, hence an accurate enough NDR indicator, so that a site can be sufficiently characterized from a light pollution perspective. Such a measuring period usually guarantees that the clear sky nominal NSB is well defined and that various cloud conditions have been observed. This estimate is sustained by the results obtained in Fig. 12.Value of the NDR indicator for ecological researchThe study of the impact of light pollution on biodiversity is currently in full expansion, amplifying a political and citizen demand for the reclamation of the night2,32,33.We identify three main contributions of the NDR indicator for ecological research. First, it overcomes the limits of an old problem of communication in terms of measurement units between disciplines and potentially limits the use of units without real meaning from a biodiversity point of view34,35. Secondly, the use of the NDR indicator limits the common biases linked to a characterization of the effects of anthropogenic light which is too limited in time and space35. Indeed, the life history traits of species are not only shaped by the intensity of light emitted into the nocturnal environment but also by its variation over time34,35,36. Currently, the characterization of light pollution is too often limited in time and space, which can lead to misinterpretation37. Thirdly, the NDR indicator provides ecological researchers with a unit of measurement that integrates a sufficiently long time step to study the impact of light pollution on the evolutionary processes at work in the life of species and particularly on population dynamics and animal behavior36,38,39.Limitations and future improvements of the NDR indicatorThe main limitation of the NDR indicator resides in the possible difficulty to identify a well defined value for the nominal NSB, i.e. the NSB value that represents the most common clear sky conditions of a given site. For the most part, this is due to the contribution of the Galactic plane to the zenithal sky brightness and, to a lower extent, to the contribution of other natural light sources (dense star fields, airglow and zodiacal light). The residual spread of NSB measures is due to changing atmospheric conditions at various time scales, but, for this particular contribution, we can expect a statistical compensation to eliminate a systematic associated bias.At the moment, the contribution of the Galactic plane and star fields is canceled into the NSB measures by calculating in the Noxi software the integrated flux of all the stars that belong to the field of view (using the UCAC4 star catalogue). However, this approach has proven some limitations, especially in the southern hemisphere where the Galactic center goes through the zenith and is particularly bright. A probable explanation for that lack of predictability is the fact that the Galactic plane contains diffuse sources such as nebulae which are not accounted for into the star catalogues and which actually cannot be ignored. To address this issue, DarkSkyLab has the project to create a brightness map of the Galactic plane with a square degree resolution or better so that the contribution of all sources can be correctly accounted for.In addition to better correcting the Galactic plane bias, an improvement must be made with regards to the NSB measures that need to be corrected. At the moment, all NSB measures are corrected from the Galactic plane bias without regards to the presence of clouds or high levels of light pollution. So a first heuristic must be implemented to only apply the bias correction to clear sky NSB measures. An other heuristic must also be developed to reduce the correction applied as a function of the NSB level.A third limitation of the NDR indicator is related to a possible lack of cloudy conditions at some sites (e.g. in the Atacama desert in Chile with more than 320 clear nights per year), the reason simply being that the NDR indicator requires the presence of clouds to differentiate the bright and dark extensions into the NSB density histograms. This means that the NDR indicator can hardly be used for such astronomy-oriented sites which experience rare cloudy conditions. More

  • in

    Fitness costs associated with a GABA receptor mutation conferring dieldrin resistance in Aedes albopictus

    Agnew P, Berticat C, Bedhomme S, Sidobre C, Michalakis Y (2004) Parasitism increases and decreases the costs of insecticide resistance in mosquitoes. Evolution 58:579–586CAS 
    PubMed 
    Article 

    Google Scholar 
    Ahmad NA, Endersby-Harshman NM, Mohd Mazni NR, Mohd Zabari NZA, Amran SNS, Ridhuan Ghazali MK et al. (2020) Characterization of sodium channel mutations in the Dengue vector mosquitoes Aedes aegypti and Aedes albopictus within the context of ongoing Wolbachia releases in Kuala Lumpur, Malaysia. Insects 11:529PubMed Central 
    Article 

    Google Scholar 
    Alout H, Ndam NT, Sandeu MM, Djégbe I, Chandre F, Dabiré RK et al. (2013) Insecticide resistance alleles affect vector competence of Anopheles gambiae s.s. for Plasmodium falciparum field isolates. PLoS ONE 8:e63849CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Andreasen MH, ffrench-Constant RH (2002) In situ hybridization to the Rdl locus on polytene chromosome 3L of Anopheles stephensi. Med Vet Entomol 16:452–455CAS 
    PubMed 
    Article 

    Google Scholar 
    Assogba BS, Djogbénou LS, Milesi P, Berthomieu A, Perez J, Ayala D et al. (2015) An ace-1 gene duplication resorbs the fitness cost associated with resistance in Anopheles gambiae, the main malaria mosquito. Sci Rep. 5:14529CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Assogba BS, Milesi P, Djogbénou LS, Berthomieu A, Makoundou P, Baba-Moussa LS et al. (2016) The ace-1 locus is amplified in all resistant Anopheles gambiae mosquitoes: fitness consequences of homogeneous and heterogeneous duplications. PloS Biol 14:e2000618PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Atyame CM, Alout H, Mousson L, Vazeille M, Diallo M, Weill M et al. (2019) Insecticide resistance genes affect Culex quinquefasciatus vector competence for West Nile virus. Proc Biol Sci 286:20182273CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Auteri M, La Russa F, Blanda V, Torina A (2018) Insecticide resistance associated with kdr mutations in Aedes albopictus: an update on worldwide evidences. Biomed Res Int 2018:e3098575Article 

    Google Scholar 
    Berticat C, Boquien G, Raymond M, Chevillon C (2002) Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet Res 79:41–47Berticat C, Duron O, Heyse D, Raymond M (2004) Insecticide resistance genes confer a predation cost on mosquitoes, Culex pipiens. Genet Res 83:189–196CAS 
    PubMed 
    Article 

    Google Scholar 
    Bhatia SC, Deobhankar RB (1963) Reversion of dieldrin-resistance in the field population of A. culicifacies in Maharashtra State (erstwhile Bombay State), India. Indian J Malariol 17:339–351CAS 
    PubMed 

    Google Scholar 
    Bonizzoni M, Gasperi G, Chen X, James AA (2013) The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol 29:460–468PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bourguet D, Guillemaud T, Chevillon C, Raymond M (2004) Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution 58:128–135PubMed 
    Article 

    Google Scholar 
    Brooke BD, Hunt RH, Coetzee M (2000) Resistance to dieldrin + fipronil assorts with chromosome inversion 2La in the malaria vector Anopheles gambiae. Med Vet Entomol 14:190–194CAS 
    PubMed 
    Article 

    Google Scholar 
    Buckingham SD, Biggin PC, Sattelle BM, Brown LA, Sattelle DB (2005) Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol Pharm 68:942–951CAS 
    Article 

    Google Scholar 
    Chen H, Li K, Wang X, Yang X, Lin Y, Cai F et al. (2016) First identification of kdr allele F1534S in VGSC gene and its association with resistance to pyrethroid insecticides in Aedes albopictus populations from Haikou City, Hainan Island, China. Infect Dis Poverty 5:31PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Davari B, Vatandoost H, Oshaghi MA, Ladonni H, Enayati AA, Shaeghi M et al. (2007) Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spectrum to pyrethroids and fipronil. Pestic Biochem Physiol 89:97–103CAS 
    Article 

    Google Scholar 
    Delatte H, Paupy C, Dehecq JS, Thiria J, Failloux AB, Fontenille D (2008) Aedes albopictus, vector of Chikungunya and Dengue viruses in Reunion Island: biology and control. Parasite 15:3–13CAS 
    PubMed 
    Article 

    Google Scholar 
    Deng J, Guo Y, Su X, Liu S, Yang W, Wu Y et al. (2021) Impact of deltamethrin-resistance in Aedes albopictus on its fitness cost and vector competence. PLoS Negl Trop Dis 15:e0009391CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Djogbénou L, Weill M, Hougard J-M, Raymond M, Akogbéto M, Chandre F (2007) Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol 44:805–810PubMed 

    Google Scholar 
    Du W, Awolola TS, Howell P, Koekemoer LL, Brooke BD, Benedict MQ et al. (2005) Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol Biol 14:179–183CAS 
    PubMed 
    Article 

    Google Scholar 
    Duron O, Labbé P, Berticat C, Rousset F, Guillot S, Raymond M et al. (2006) High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution 60:303–314CAS 
    PubMed 
    Article 

    Google Scholar 
    ffrench-Constant RH, Rocheleau TA, Steichen JC, Chalmers AE (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363:449–451CAS 
    PubMed 
    Article 

    Google Scholar 
    ffrench-Constant RH, Anthony N, Aronstein K, Rocheleau T, Stilwell G (2000) Cyclodiene insecticide resistance: from molecular to population genetics. Annu Rev Entomol 45:449–466CAS 
    PubMed 
    Article 

    Google Scholar 
    Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. SAGE, Thousand Oaks California, https://socialsciences.mcmaster.ca/jfox/Books/Companion/
    Google Scholar 
    Freeman JC, Smith LB, Silva JJ, Fan Y, Sun H, Scott JG (2021) Fitness studies of insecticide resistant strains: lessons learned and future directions. Pest Manag Sci 77:3847–3856CAS 
    PubMed 
    Article 

    Google Scholar 
    Gratz NG (2004) Critical review of the vector status of Aedes albopictus. Med Vet Entomol 18:215–227CAS 
    PubMed 
    Article 

    Google Scholar 
    Grau-Bové X, Tomlinson S, O’Reilly AO, Harding NJ, Miles A, Kwiatkowski D et al. (2020) Evolution of the insecticide target Rdl in African Anopheles is driven by interspecific and interkaryotypic introgression. Mol Biol Evol 37:2900–2917PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Grigoraki L, Lagnel J, Kioulos I, Kampouraki A, Morou E, Labbé P et al. (2015) Transcriptome profiling and genetic study reveal amplified carboxylesterase genes implicated in temephos resistance, in the Asian tiger mosquito Aedes albopictus. PLoS Negl Trop Dis 9:e0003771PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hamon J, Garret-Jones C (1962) Insecticide-resistance in major vectors of malaria, and its operational importance. Bull World Health Organ, Geneva
    Google Scholar 
    Hartley CJ, Newcomb RD, Russell RJ, Yong CG, Stevens JR, Yeates DK et al. (2006) Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proc Natl Acad Sci USA 103:8757–8762CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391CAS 
    PubMed 
    Article 

    Google Scholar 
    Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34:653–665CAS 
    PubMed 
    Article 

    Google Scholar 
    Hosie AM, Baylis HA, Buckingham SD, Sattelle DB (1995) Actions of the insecticide fipronil, on dieldrin-sensitive and -resistant GABA receptors of Drosophila melanogaster. Br J Pharm 115:909–912CAS 
    Article 

    Google Scholar 
    Ishak IH, Riveron JM, Ibrahim SS, Stott R, Longbottom J, Irving H et al. (2016) The Cytochrome P450 gene CYP6P12 confers pyrethroid resistance in kdr-free Malaysian populations of the Dengue vector Aedes albopictus. Sci Rep. 6:24707CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kasai S, Ng LC, Lam-Phua SG, Tang CS, Itokawa K, Komagata O et al. (2011) First detection of a putative knockdown resistance gene in major mosquito vector, Aedes albopictus. Jpn J Infect Dis 64:217–221CAS 
    PubMed 
    Article 

    Google Scholar 
    Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431–1437CAS 
    PubMed 
    Article 

    Google Scholar 
    Kolaczinski J, Curtis C (2001) Laboratory evaluation of fipronil, a phenylpyrazole insecticide, against adult Anopheles (Diptera: Culicidae) and investigation of its possible cross-resistance with dieldrin in Anopheles stephensi. Pest Manag Sci 57:41–45CAS 
    PubMed 
    Article 

    Google Scholar 
    Kraemer MU, Sinka ME, Duda KA, Mylne AQ, Shearer FM, Barker CM et al. (2015) The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife 4:e08347PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Labbé P, David J-P, Alout H, Milesi P, Djogbénou L, Pasteur N et al. (2017) 14 – Evolution of resistance to insecticide in disease vectors. In: Tibayrenc M (ed) Genetics and Evolution of Infectious Diseases, Second Edition. Elsevier, London, p 313–339Chapter 

    Google Scholar 
    Latreille AC, Milesi P, Magalon H, Mavingui P, Atyame CM (2019) High genetic diversity but no geographical structure of Aedes albopictus populations in Réunion Island. Parasit Vectors 12:597PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lebon C, Alout H, Zafihita S, Dehecq JS, Weill M, Tortosa P et al. (2022) Spatio-temporal dynamics of a dieldrin resistance gene in Aedes albopictus and Culex quinquefasciatus populations from Reunion Island. J Insect Sci 22:4PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lebon C, Soupapoule K, Wilkinson DA, Goff GL, Damiens D, Gouagna LC (2018) Laboratory evaluation of the effects of sterilizing doses of γ-rays from Caesium-137 source on the daily flight activity and flight performance of Aedes albopictus males. PLoS ONE 13:e0202236PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li Y, Xu J, Zhong D, Zhang H, Yang W, Zhou G et al. (2018) Evidence for multiple-insecticide resistance in urban Aedes albopictus populations in southern China. Parasit Vectors 11:4PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Low VL, Vinnie-Siow WY, Lim YAL, Tan TK, Leong CS, Chen CD et al. (2015) First molecular genotyping of A302S mutation in the gamma aminobutyric acid (GABA) receptor in Aedes albopictus from Malaysia. Trop Biomed 32:554–556CAS 
    PubMed 

    Google Scholar 
    McKenzie BA, Wilson AE, Zohdy S (2019) Aedes albopictus is a competent vector of Zika virus: a meta-analysis. PLoS ONE 14:e0216794CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milesi P, Pocquet N, Labbé P (2013) BioRssay: A R script for bioassay analyses. http://www.isem.univ-montp2.fr/recherche/equipes/genomique-de-ladaptation/personnel/labbepierrick/Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I et al. (2017) Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis 11:e0005625PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ozoe Y, Kita T, Ozoe F, Nakao T, Sato K, Hirase K (2013) Insecticidal 3-benzamido-N-phenylbenzamides specifically bind with high affinity to a novel allosteric site in housefly GABA receptors. Pestic Biochem Physiol 107:285–292CAS 
    PubMed 
    Article 

    Google Scholar 
    Paupy C, Ollomo B, Kamgang B, Moutailler S, Rousset D, Demanou M et al. (2009) Comparative role of Aedes albopictus and Aedes aegypti in the emergence of Dengue and Chikungunya in central Africa. Vector Borne Zoonotic Dis 10:259–266Article 

    Google Scholar 
    Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Platt N, Kwiatkowska RM, Irving H, Diabaté A, Dabire R, Wondji CS (2015) Target-site resistance mutations (kdr and RDL), but not metabolic resistance, negatively impact male mating competiveness in the malaria vector Anopheles gambiae. Heredity 115:243–252CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/
    Google Scholar 
    Ranson H, Burhani J, Lumjuan N, Black WCI (2010) Insecticide resistance in Dengue vectors. TropIKA.net [online] 1. http://journal.tropika.net/scielo.php?script=sci_arttext&pid=S2078-86062010000100003&lng=en&nrm=iso. Accessed 03 March 2022Raymond M, Berticat C, Weill M, Pasteur N, Chevillon C (2001) Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation? Genetica 112–113:287–296PubMed 
    Article 

    Google Scholar 
    Renault P, Solet J-L, Sissoko D, Balleydier E, Larrieu S, Filleul L et al. (2007) A major epidemic of Chikungunya virus infection on Réunion Island, France, 2005–2006. Am J Trop Med Hy 77:727–731Article 

    Google Scholar 
    Rowland M (1991a) Behaviour and fitness of γHCH/dieldrin resistant and susceptible female Anopheles gambiae and An. stephensi mosquitoes in the absence of insecticide. Med Vet Entomol 5:193–206CAS 
    PubMed 
    Article 

    Google Scholar 
    Rowland M (1991b) Activity and mating competitiveness of γHCH/dieldrin resistant and susceptible male and virgin female Anopheles gambiae and An. stephensi mosquitoes, with assessment of an insecticide-rotation strategy. Med Vet Entomol 5:207–222CAS 
    PubMed 
    Article 

    Google Scholar 
    Russell VL (2021) Emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.5.1. https://CRAN.R-project.org/package=emmeansSu X, Guo Y, Deng J, Xu J, Zhou G, Zhou T et al. (2019) Fast emerging insecticide resistance in Aedes albopictus in Guangzhou, China: alarm to the Dengue epidemic. PLoS Negl Trop Dis 13:e0007665CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tantely ML, Tortosa P, Alout H, Berticat C, Berthomieu A, Rutee A et al. (2010) Insecticide resistance in Culex pipiens quinquefasciatus and Aedes albopictus mosquitoes from La Réunion Island. Insect Biochem Mol Biol 40:317–324CAS 
    PubMed 
    Article 

    Google Scholar 
    Taskin BG, Dogaroglu T, Kilic S, Dogac E, Taskin V (2016) Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field populations of Culex pipiens. Pestic Biochem Physiol 129:14–27CAS 
    PubMed 
    Article 

    Google Scholar 
    Taylor‐Wells J, Brooke BD, Bermudez I, Jones AK (2015) The neonicotinoid imidacloprid, and the pyrethroid deltamethrin, are antagonists of the insect Rdl GABA receptor. J Neurochem 135:705–713PubMed 
    Article 

    Google Scholar 
    Therneau T (2015) A Package for Survival Analysis in S. R package version 2.38. https://CRAN.R-project.org/package=survivalThompson M, Shotkoski F, ffrench-Constant R (1993) Cloning and sequencing of the cylodienne insecticide resistance from the yellow fewer Aedes aegypti. FEBS Lett 325:187–190CAS 
    PubMed 
    Article 

    Google Scholar 
    Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S (2007) A single mutation in Chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3:e201PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A, Ranson H (2012) Insecticide resistance in the major Dengue vectors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol 104:126–131CAS 
    Article 

    Google Scholar 
    Wondji CS, Dabire RK, Tukur Z, Irving H, Djouaka R, Morgan JC (2011) Identification and distribution of a GABA receptor mutation conferring dieldrin resistance in the malaria vector Anopheles funestus in Africa. Insect Biochem Mol Biol 41:484–491CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xu J, Bonizzoni M, Zhong D, Zhou G, Cai S, Li Y et al. (2016) Multi-country survey revealed prevalent and novel F1534S mutation in voltage-gated sodium channel (VGSC) gene in Aedes albopictus. PLoS Negl Trop Dis 10:e0004696PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yang C, Huang Z, Li M, Feng X, Qiu X (2017) RDL mutations predict multiple insecticide resistance in Anopheles sinensis in Guangxi, China. Malar J 16:482PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhou X, Yang C, Liu N, Li M, Tong Y, Zeng X et al. (2019) Knockdown resistance (kdr) mutations within seventeen field populations of Aedes albopictus from Beijing China: first report of a novel V1016G mutation and evolutionary origins of kdr haplotypes. Parasit Vectors 12:180PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Pollinator biological traits and ecological interactions mediate the impacts of mosquito-targeting malathion application

    Garibaldi, L. A. et al. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 14(10), 1062–1072 (2011).PubMed 
    Article 

    Google Scholar 
    Kremen, C. et al. Pollination and other ecosystem services produced by mobile organisms: A conceptual framework for the effects of land-use change. Ecol. Lett. 10(4), 299–314 (2007).PubMed 
    Article 

    Google Scholar 
    Kluser, S. & Peduzzi, P. Global pollinator decline: A literature review. Preprint at http://archive-ouverte.unige.ch/unige 32258 (2007).Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 25(6), 345–353 (2010).PubMed 
    Article 

    Google Scholar 
    Rhodes, C. J. Pollinator decline—an ecological calamity in the making?. Sci. Prog. 101(2), 121–160 (2018).PubMed 
    Article 

    Google Scholar 
    Huang, H. & D’Odorico, P. Critical transitions in plant-pollinator systems induced by positive inbreeding-reward-pollinator feedbacks. Iscience 23(2), 100819 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Krishnan, N. et al. Assessing field-scale risks of foliar insecticide applications to monarch butterfly (Danaus plexippus) larvae. Environ. Toxicol. Chem. 39(4), 923–941 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bargar, T. A., Hladik, M. L. & Daniels, J. C. Uptake and toxicity of clothianidin to monarch butterflies from milkweed consumption. PeerJ 8, e8669 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Emmel, T. C. & Tucker, J. C. In Mosquito Control Pesticides: Ecological Impacts and Management Alternatives (eds Emmel, T. C. & Tucker, J. C.) 105 (Scientific Publishers, 1991).Johnson, R. M., Ellis, M. D., Mullin, C. A. & Frazier, M. Pesticides and honey bee toxicity–USA. Apidologie 41(3), 312–331 (2010).CAS 
    Article 

    Google Scholar 
    Olaya-Arenas, P., Scharf, M. E. & Kaplan, I. Do pollinators prefer pesticide-free plants? An experimental test with monarchs and milkweeds. J. Appl. Ecol. 57(10), 2019–2030 (2020).CAS 
    Article 

    Google Scholar 
    Berryman, A. A. What causes population cycles of forest Lepidoptera?. Trends Ecol. Evol. 11(1), 28–32 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    Elkinton, J. & Boettner, G. Benefits and harm caused by the introduced generalist tachinid, Compsilura concinnata North America. Biol. Control 57(2), 277–288 (2012).
    Google Scholar 
    Beschta, R. L. & Ripple, W. J. Riparian vegetation recovery in Yellowstone: The first two decades after wolf reintroduction. Biol. Conserv. 198, 93–103 (2016).Article 

    Google Scholar 
    Oberhauser, K. et al. Lacewings wasps and fliesoh my insect enemies take a bite out of monarchs. In Monarchs in a Changing World: Biology and Conservation of an iconic insect (eds Oberhauser, K. S. et al.) 71–82 (Cornell University Press, 2015).Chapter 

    Google Scholar 
    Zalucki, M. P., Clarke, A. R. & Malcolm, S. B. Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol. 47(1), 361–393 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hermann, S. L., Blackledge, C., Haan, N. L., Myers, A. T. & Landis, D. A. Predators of monarch butterfly eggs and neonate larvae are more diverse than previously recognised. Sci. Rep. 9(1), 1–9 (2019).CAS 
    Article 

    Google Scholar 
    McCoshum, S. M., Andreoli, S. L., Stenoien, C. M., Oberhauser, K. S. & Baum, K. A. Species distribution models for natural enemies of monarch butterfly (Danaus plexippus) larvae and pupae: Distribution patterns and implications for conservation. J. Insect Conserv. 20(2), 223–237 (2016).Article 

    Google Scholar 
    Geest, E. A., Wolfenbarger, L. L. & McCarty, J. P. Recruitment, survival and parasitism of monarch butterflies (Danaus plexippus) in milkweed gardens and conservation areas. J. Insect Conserv. 23(2), 211–224 (2019).Article 

    Google Scholar 
    Stenoien, C. et al. Monarchs in decline: A collateral landscape-level effect of modern agriculture. Insect Sci. 25(4), 528–541 (2018).PubMed 
    Article 

    Google Scholar 
    Crone, E. E., Pelton, E. M., Brown, L. M., Thomas, C. C. & Schultz, C. B. Why are monarch butterflies declining in the west? Understanding the importance of multiple correlated drivers. Ecol. Appl. 29(7), e01975 (2019).PubMed 
    Article 

    Google Scholar 
    Brower, L. P. et al. Effect of the 2010–2011 drought on the lipid content of monarchs migrating through Texas to overwintering sites in Mexico. In The Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly (eds Oberhauser, K. S. et al.) 117–129 (Cornell University Press, 2015).
    Google Scholar 
    Thogmartin, W. E. et al. Monarch butterfly population decline in North America: Identifying the threatening processes. R. Soc. Open Sci. 4(9), 170760 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Olaya-Arenas, P. & Kaplan, I. Quantifying pesticide exposure risk for monarch caterpillars on milkweeds bordering agricultural land. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00223 (2019).
    Article 

    Google Scholar 
    Olaya-Arenas, P., Hauri, K., Scharf, M. E. & Kaplan, I. Larval pesticide exposure impacts monarch butterfly performance. Sci. Rep. 10(1), 1–12 (2020).Article 

    Google Scholar 
    Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. PNAS 108(2), 662–667 (2011).ADS 
    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Epstein, L. Fifty years since silent spring. Annu. Rev. Phytopathol. 52, 377–402 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rayor, L. S. Effects of monarch larval host plant chemistry and body size on Polistes wasp predation. In The Monarch Butterfly Biology and Conservation (eds Oberhauser, K. S. & Solensky, M. J.) 39–46 (Cornell University Press, 2004).
    Google Scholar 
    Baker, A. M. & Potter, D. A. Invasive paper wasp turns urban pollinator gardens into ecological traps for monarch butterfly larvae. Sci. Rep. 10(1), 1–7 (2020).Article 

    Google Scholar 
    Castellanos, I. & Barbosa, P. Dropping from host plants in response to predators by a polyphagous caterpillar. J. Lepid. Soc. 65(4), 270–272 (2011).
    Google Scholar 
    Kessler, S. C. et al. Bees prefer foods containing neonicotinoid pesticides. Nature 521(7550), 74–76 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Liao, L.-H., Wu, W.-Y. & Berenbaum, M. R. Behavioral responses of honey bees (Apis mellifera) to natural and synthetic xenobiotics in food. Sci. Rep. 7(1), 1–8 (2017).Article 

    Google Scholar 
    Musser, R. O. et al. Caterpillar saliva beats plant defences. Nature 416(6881), 599–600 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Schmidt, J. & Smith, J. Host examination walk and oviposition site selection of Trichogramma minutum: Studies on spherical hosts. J. Insect Behav. 2(2), 143–171 (1989).Article 

    Google Scholar 
    Ramos, R. S. et al. Investigation of the lethal and behavioral effects of commercial insecticides on the parasitoid wasp Copidosoma truncatellum. Chemosphere 191, 770–778 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Chareonviriyaphap, T. et al. Pesticide avoidance behavior in Anopheles albimanus, a malaria vector in the Americas. J. Am. Mosq. Control Assoc. 13(2), 171–183 (1997).CAS 
    PubMed 

    Google Scholar 
    Nansen, C., Baissac, O., Nansen, M., Powis, K. & Baker, G. Behavioral avoidance-will physiological insecticide resistance level of insect strains affect their oviposition and movement responses?. PLoS ONE 11(3), e0149994 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martini, X., Kincy, N. & Nansen, C. Quantitative impact assessment of spray coverage and pest behavior on contact pesticide performance. Pest Manag. Sci. 68(11), 1471–1477 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bull, D. & Coleman, R. Effects of pesticides on Trichogramma spp. Southwest. Entomol. Suppl. 8, 156–168 (1985).CAS 

    Google Scholar 
    Thubru, D., Firake, D. & Behere, G. Assessing risks of pesticides targeting lepidopteran pests in cruciferous ecosystems to eggs parasitoid, Trichogramma brassicae (Bezdenko). Saudi J. Biol. Sci. 25(4), 680–688 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Selwood, K. & Zimmer, H. Refuges for biodiversity conservation: A review of the evidence. Biol. Conserv. 245, 108502 (2020).Article 

    Google Scholar 
    Chmiel, J. A., Daisley, B. A., Pitek, A. P., Thompson, G. J. & Reid, G. Understanding the effects of sublethal pesticide exposure on honey bees: A role for probiotics as mediators of environmental stress. Front. Ecol. Evol. 8, 22 (2020).Article 

    Google Scholar 
    Chittka, L., Williams, N., Rasmussen, H. & Thomson, J. Navigation without vision: Bumblebee orientation in complete darkness. Proc. R. Soc. B 266(1414), 45–50 (1999).PubMed Central 
    Article 

    Google Scholar 
    Young, M. W. & Kay, S. A. Time zones: A comparative genetics of circadian clocks. Nat. Rev. Genet. 2(9), 702–715 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mallet, J. Gregarious roosting and home range in Heliconius butterflies. Natl. Geogr. Res. 2(2), 198–215 (1986).
    Google Scholar 
    Chang, Y.-M. et al. Roosting site usage, gregarious roosting and behavioral interactions during roost-assembly of two Lycaenidae butterflies. Zool. Stud. 59, e10 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Vulinec, K. Collective security aggregation by insects as a defence. In Insect Defences. Adaptive Mechanisms of Prey and Predators (eds Evans, D. L. & Schmidt, J. O.) 251–288 (State University of New York, 1990).
    Google Scholar 
    Salcedo, C. Environmental elements involved in communal roosting in Heliconius butterflies (Lepidoptera: Nymphalidae). Environ. Entomol. 39(3), 907–911 (2010).PubMed 
    Article 

    Google Scholar 
    Giordano, B. V., McGregor, B. L., Runkel, A. E. IV. & Burkett-Cadena, N. D. Distance diminishes the effect of deltamethrin exposure on the monarch butterfly, Danaus plexippus. J. Am. Mosq. Control Assoc. 36(3), 181–188 (2020).PubMed 
    Article 

    Google Scholar 
    Matzrafi, M. Climate change exacerbates pest damage through reduced pesticide efficacy. Pest Manag. Sci. 75(1), 9–13 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hewitt, A. Spray drift: Impact of requirements to protect the environment. Crop Prot. 19(8–10), 623–627 (2000).Article 

    Google Scholar 
    Nail, K. R., Stenoien, C. & Oberhauser, K. S. Immature monarch survival: Effects of site characteristics, density and time. Ann. Entomol. Soc. 108(5), 680–690 (2015).Article 

    Google Scholar 
    Payne, C. C. & Mertens, P. P. Cytoplasmic polyhedrosis viruses. In The Reoviridae (ed. Joklik, K.) 425–504 (Springer, 1983).Chapter 

    Google Scholar 
    Zalucki, M. P. et al. It’s the first bites that count: Survival of first-instar monarchs on milkweeds. Austral. Ecol. 26(5), 547–555 (2001).Article 

    Google Scholar 
    Salvato, M. Influence of mosquito control chemicals on butterflies (Nymphalidae, Lycaenidae, Hesperiidae) of the lower Florida keys. J. Lepid. Soc. 55(1), 8–14 (2001).
    Google Scholar 
    Frey, D. F. & Leong, K. L. Can microhabitat selection or differences in ‘catchability’ explain male-biased sex ratios in overwintering populations of monarch butterflies?. Anim. Behav. 45(5), 1025 (1993).Article 

    Google Scholar 
    Macgregor, C. J. & Scott-Brown, A. S. Nocturnal pollination: An overlooked ecosystem service vulnerable to environmental change. Emerg. Top. Life Sci. 4(1), 19–32 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Biological invasions as a selective filter driving behavioral divergence

    Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, (2017).IPBES. Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. (IPBES secretariat, 2019). https://doi.org/10.5281/zenodo.3831673.Elton, C. S. The Ecology of Invasions by Animals and Plants. (University of Chicago Press, 1958).Lockwood, J. L., Hoopes, M. F. & Marchetti, M. P. Invasion Ecology. (Wiley-Blackwell, 2013).O’Dowd, D. J., Green, P. T. & Lake, P. S. Invasional “meltdown” on an oceanic island. Ecol. Lett. 6, 812–817 (2003).
    Google Scholar 
    Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G. & Dickman, C. R. Invasive predators and global biodiversity loss. Proc. Natl Acad. Sci. 113, 11261–11265 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Spatz, D. R. et al. Globally threatened vertebrates on islands with invasive species. Sci. Adv. 3, (2017).Pimentel, D. et al. Economic and environmental threats of alien plant, animal, and microbe invasions. Agriculture, Ecosyst. Environ. 84, 1–20 (2001).
    Google Scholar 
    Hoffmann, B. D. & Broadhurst, L. M. The economic cost of managing invasive species in Australia. NeoBiota 31, 1–18 (2016).
    Google Scholar 
    Kolar, C. S. & Lodge, D. M. Progress in invasion biology: predicting invaders. Trends Ecol. Evolution 16, 199–204 (2001).
    Google Scholar 
    Jeschke, J. M. & Strayer, D. L. Invasion success of vertebrates in Europe and North America. Proc. Natl Acad. Sci. 102, 7198–7202 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lovell, R. S. L., Blackburn, T. M., Dyer, E. E. & Pigot, A. L. Environmental resistance predicts the spread of alien species. Nat. Ecol. Evolution 5, 322–329 (2021).
    Google Scholar 
    Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evolution 26, 333–339 (2011).
    Google Scholar 
    Chapple, D. G., Simmonds, S. M. & Wong, B. B. M. Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol. Evolution 27, 57–64 (2012).
    Google Scholar 
    Chapple, D. G. & Wong, B. B. M. The role of behavioural variation across different stages of the introduction process. in Biological Invasions and Animal Behaviour (eds. Weis, Judith, S. & Sol, Daniel.) 7–25 (Cambridge University Press, 2016).Holway, D. & Suarez, A. Animal behavior: an essential component of invasion biology. Trends Ecol. Evolution 14, 328–330 (1999).CAS 

    Google Scholar 
    Felden, A. et al. Behavioural variation and plasticity along an invasive ant introduction pathway. J. Anim. Ecol. 87, 1653–1666 (2018).PubMed 

    Google Scholar 
    D’Amore, D. M., Popescu, V. D. & Morris, M. R. The influence of the invasive process on behaviours in an intentionally introduced hybrid, Xiphophorus helleri-maculatus. Anim. Behav. 156, 79–85 (2019).
    Google Scholar 
    Perkins, T. A., Boettiger, C. & Phillips, B. L. After the games are over: life‐history trade‐offs drive dispersal attenuation following range expansion. Ecol. Evolution 6, 6425–6434 (2016).
    Google Scholar 
    Phillips, B. L., Brown, G. P., Travis, J. M. J. & Shine, R. Reid’s Paradox revisited: the evolution of dispersal kernels during range expansion. Am. Naturalist 172, S34–S48 (2008).
    Google Scholar 
    Shine, R., Brown, G. P. & Phillips, B. L. An evolutionary process that assembles phenotypes through space rather than through time. Proc. Natl Acad. Sci. 108, 5708–5711 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lindström, T., Brown, G. P., Sisson, S. A., Phillips, B. L. & Shine, R. Rapid shifts in dispersal behavior on an expanding range edge. Proc. Natl Acad. Sci. 110, 13452–13456 (2013).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Heger, T. & Jeschke, J. M. The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123, 741–750 (2014).
    Google Scholar 
    Colautti, R. I., Ricciardi, A., Grigorovich, I. A. & MacIsaac, H. J. Is invasion success explained by the enemy release hypothesis? Ecol. Lett. 7, 721–733 (2004).
    Google Scholar 
    Wilson, J. R. U., Dormontt, E. E., Prentis, P. J., Lowe, A. J. & Richardson, D. M. Something in the way you move: dispersal pathways affect invasion success. Trends Ecol. Evolution 24, 136–144 (2009).
    Google Scholar 
    Wilson, S. & Swan, G. A complete guide to reptiles of Australia. (New Holland Publishers, 2021).Chapple, D. G., Miller, K. A., Kraus, F. & Thompson, M. B. Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Diversity Distrib. 19, 134–146 (2013).
    Google Scholar 
    Chapple, D., Knegtmans, J., Kikillus, H. & van Winkel, D. Biosecurity of exotic reptiles and amphibians in New Zealand: building upon Tony Whitaker’s legacy. J. R. Soc. N.Z. 46, 66–84 (2016).
    Google Scholar 
    Chapple, D. G., Whitaker, A. H., Chapple, S. N. J., Miller, K. A. & Thompson, M. B. Biosecurity interceptions of an invasive lizard: Origin of stowaways and human-assisted spread within New Zealand. Evolut. Appl. 6, 324–339 (2013).
    Google Scholar 
    Tingley, R., Thompson, M. B., Hartley, S. & Chapple, D. G. Patterns of niche filling and expansion across the invaded ranges of an Australian lizard. Ecography 39, 270–280 (2016).
    Google Scholar 
    Chapple, D. G. et al. Biology of the invasive delicate skink (Lampropholis delicata) on Lord Howe Island. Aust. J. Zool. 62, 498–506 (2014).
    Google Scholar 
    Moule, H. et al. A matter of time: temporal variation in the introduction history and population genetic structuring of an invasive lizard. Curr. Zool. 61, 456–464 (2015).CAS 

    Google Scholar 
    Chapple, D. G., Simmonds, S. M. & Wong, B. B. M. Know when to run, know when to hide: can behavioral differences explain the divergent invasion success of two sympatric lizards? Ecol. Evolution 1, 278–289 (2011).
    Google Scholar 
    Cromie, G. L. & Chapple, D. G. Impact of tail loss on the behaviour and locomotor performance of two sympatric Lampropholis skink species. PLoS ONE 7, e34732 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Brand, J. A. et al. Rapid shifts in behavioural traits during a recent fish invasion. Behav. Ecol. Sociobiol. 75, 134 (2021).
    Google Scholar 
    Myles-Gonzalez, E., Burness, G., Yavno, S., Rooke, A. & Fox, M. G. To boldly go where no goby has gone before: boldness, dispersal tendency, and metabolism at the invasion front. Behav. Ecol. 26, 1083–1090 (2015).
    Google Scholar 
    Pintor, L. M., Sih, A. & Bauer, M. L. Differences in aggression, activity and boldness between native and introduced populations of an invasive crayfish. Oikos 117, 1629–1636 (2008).
    Google Scholar 
    Mueller, J. C. et al. Selection on a behaviour-related gene during the first stages of the biological invasion pathway. Mol. Ecol. 26, 6110–6121 (2017).MathSciNet 
    CAS 
    PubMed 

    Google Scholar 
    Snell-Rood, E. C. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85, 1004–1011 (2013).
    Google Scholar 
    Niemelä, P. T., Niehoff, P. P., Gasparini, C., Dingemanse, N. J. & Tuni, C. Crickets become behaviourally more stable when raised under higher temperatures. Behav. Ecol. Sociobiol. 73, 81 (2019).
    Google Scholar 
    Polverino, G. et al. Psychoactive pollution suppresses individual differences in fish behaviour. Proc. R. Soc. B: Biol. Sci. 288, 20202294 (2021).
    Google Scholar 
    Royauté, R., Garrison, C., Dalos, J., Berdal, M. A. & Dochtermann, N. A. Current energy state interacts with the developmental environment to influence behavioural plasticity. Anim. Behav. 148, 39–51 (2019).
    Google Scholar 
    Michelangeli, M., Chapple, D. G., Goulet, C. T., Bertram, M. G. & Wong, B. B. M. Behavioral syndromes vary among geographically distinct populations in a reptile. Behav. Ecol. 30, 393–401 (2019).
    Google Scholar 
    Nicolaus, M., Tinbergen, J. M., Ubels, R., Both, C. & Dingemanse, N. J. Density fluctuations represent a key process maintaining personality variation in a wild passerine bird. Ecol. Lett. 19, 478–486 (2016).PubMed 

    Google Scholar 
    Lapiedra, O., Schoener, T. W., Leal, M., Losos, J. B. & Kolbe, J. J. Predator-driven natural selection on risk-taking behavior in anole lizards. Science 360, 1017–1020 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Gruber, J., Brown, G., Whiting, M. J. & Shine, R. Geographic divergence in dispersal-related behaviour in cane toads from range-front versus range-core populations in Australia. Behav. Ecol. Sociobiol. 71, 38 (2017).
    Google Scholar 
    Gruber, J., Brown, G., Whiting, M. J. & Shine, R. Is the behavioural divergence between range-core and range-edge populations of cane toads (Rhinella marina) due to evolutionary change or developmental plasticity? R. Soc. Open Sci. 4, 170789 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Morgan, D., Waas, J. R. & Innes, J. Do territorial and non-breeding Australian Magpies Gymnorhina tibicen influence the local movements of rural birds in New Zealand? Ibis 148, 330–342 (2006).
    Google Scholar 
    O’leary, R. A. & Jones, D. N. Foraging by suburban Australian magpies during dry conditions. Corella 26, 53–54 (2002).
    Google Scholar 
    Wright, T. F., Eberhard, J. R., Hobson, E. A., Avery, M. L. & Russello, M. A. Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol. Ecol. Evolution 22, 393–404 (2010).
    Google Scholar 
    Dingemanse, N. J. & Wolf, M. Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim. Behav. 85, 1031–1039 (2013).
    Google Scholar 
    Ducatez, S., Sol, D., Sayol, F. & Lefebvre, L. Behavioural plasticity is associated with reduced extinction risk in birds. Nat. Ecol. Evolution 4, 788–793 (2020).
    Google Scholar 
    Cole, E. F. & Quinn, J. L. Personality and problem-solving performance explain competitive ability in the wild. Proc. R. Soc. B: Biol. Sci. 279, 1168–1175 (2012).
    Google Scholar 
    Webster, M. M., Ward, A. J. W. & Hart, P. J. B. Individual boldness affects interspecific interactions in sticklebacks. Behav. Ecol. Sociobiol. 63, 511–520 (2009).
    Google Scholar 
    McGhee, K. E., Pintor, L. M. & Bell, A. M. Reciprocal behavioral plasticity and behavioral types during predator-prey interactions. Am. Naturalist 182, 704–717 (2013).
    Google Scholar 
    Ioannou, C. C., Payne, M. & Krause, J. Ecological consequences of the bold–shy continuum: the effect of predator boldness on prey risk. Oecologia 157, 177–182 (2008).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Moran, N. P., Wong, B. B. M. & Thompson, R. M. Weaving animal temperament into food webs: implications for biodiversity. Oikos 126, 917–930 (2017).
    Google Scholar 
    Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Moule, H., Michelangeli, M., Thompson, M. B. & Chapple, D. G. The influence of urbanization on the behaviour of an Australian lizard and the presence of an activity–exploratory behavioural syndrome. J. Zool. 298, 103–111 (2016).
    Google Scholar 
    Michelangeli, M., Wong, B. B. M. & Chapple, D. G. It’s a trap: sampling bias due to animal personality is not always inevitable. Behav. Ecol. 27, 62–67 (2016).
    Google Scholar 
    Michelangeli, M., Melki-Wegner, B., Laskowski, K., Wong, B. B. M. & Chapple, D. G. Impacts of caudal autotomy on personality. Anim. Behav. 162, 67–78 (2020).
    Google Scholar 
    Shine, R. Locomotor speeds of gravid lizards: Placing “costs of reproduction” within an ecological context. Funct. Ecol. 17, 526–533 (2003).
    Google Scholar 
    Naimo, A. C., Jones, C., Chapple, D. G. & Wong, B. B. M. Has an invasive lizard lost its antipredator behaviours following 40 generations of isolation from snake predators? Behav. Ecol. Sociobiol. 75, 131 (2021).
    Google Scholar 
    Brand, J. A. et al. Population differences in the effect of context on personality in an invasive lizard. Behav. Ecol. 32, 1363–1371 (2021).
    Google Scholar 
    Goulet, C. T., Thompson, M. B., Michelangeli, M., Wong, B. B. M. & Chapple, D. G. Thermal physiology: a new dimension of the pace‐of‐life syndrome. J. Anim. Ecol. 86, 1269–1280 (2017).PubMed 

    Google Scholar 
    Michelangeli, M., Goulet, C. T., Kang, H. S., Wong, B. B. M. & Chapple, D. G. Integrating thermal physiology within a syndrome: locomotion, personality and habitat selection in an ectotherm. Funct. Ecol. 32, 970–981 (2018).
    Google Scholar 
    Bell, A. M. Randomized or fixed order for studies of behavioral syndromes? Behav. Ecol. 24, 16–20 (2013).PubMed 

    Google Scholar 
    Friard, O. & Gamba, M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evolution 7, 1325–1330 (2016).
    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/. (2019).Bürkner, P. C. brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).
    Google Scholar 
    Munson, A. A., Michelangeli, M. & Sih, A. Stable social groups foster conformity and among-group differences. Anim. Behav. 174, 197–206 (2021).
    Google Scholar 
    Royauté, R. & Dochtermann, N. A. Comparing ecological and evolutionary variability within datasets. Behav. Ecol. Sociobiol. 75, 127 (2021).
    Google Scholar 
    Dalos, J., Royauté, R., Hedrick, A. V. & Dochtermann, N. A. Phylogenetic conservation of behavioural variation and behavioural syndromes. J. Evolut. Biol. 35, 311–321 (2022).
    Google Scholar 
    Miller, K. A., Duran, A., Melville, J., Thompson, M. B. & Chapple, D. G. Sex-specific shifts in morphology and colour pattern polymorphism during range expansion of an invasive lizard. J. Biogeogr. 44, 2778–2788 (2017).
    Google Scholar 
    Michelangeli, M., Chapple, D. G. & Wong, B. B. M. Are behavioural syndromes sex specific? Personality in a widespread lizard species. Behav. Ecol. Sociobiol. 70, 1911–1919 (2016).
    Google Scholar 
    Vehtari, A., Gelman, A. & Gabry, J. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Stat. Comput. 27, 1413–1432 (2017).MathSciNet 
    MATH 

    Google Scholar 
    Nakagawa, S. & Schielzeth, H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935–956 (2010).PubMed 

    Google Scholar 
    Chapple, D. G. et al. Data from Chapple et al. “Biological invasions as a selective filter driving behavioral divergence”. Monash University. Dataset. https://doi.org/10.26180/18851036.v2 (2022). More

  • in

    Warming reduces global agricultural production by decreasing cropping frequency and yields

    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).CAS 
    Article 

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

    Google Scholar 
    Hong, C. et al. Global and regional drivers of land-use emissions in 1961–2017. Nature 589, 554–561 (2021).CAS 
    Article 

    Google Scholar 
    Laurance, W. F., Sayer, J. & Cassman, K. G. Agricultural expansion and its impacts on tropical nature. Trends Ecol. Evol. 29, 107–116 (2014).Article 

    Google Scholar 
    Cassman, K. G. & Grassini, P. A global perspective on sustainable intensification research. Nat. Sustain. 3, 262–268 (2020).Article 

    Google Scholar 
    Hodge, I., Hauck, J. & Bonn, A. The alignment of agricultural and nature conservation policies in the European Union. Conserv. Biol. 29, 996–1005 (2015).Article 

    Google Scholar 
    Heilmayr, R., Rausch, L. L., Munger, J. & Gibbs, H. K. Brazil’s Amazon Soy Moratorium reduced deforestation. Nat. Food 1, 801–810 (2020).Article 

    Google Scholar 
    Diffenbaugh, N. S. et al. Quantifying the influence of global warming on unprecedented extreme climate events. Proc. Natl Acad. Sci. USA 114, 4881–4886 (2017).CAS 
    Article 

    Google Scholar 
    Iizumi, T. & Ramankutty, N. How do weather and climate influence cropping area and intensity? Glob. Food Security 4, 46–50 (2015).Article 

    Google Scholar 
    Davis, K. F., Downs, S. & Gephart, J. A. Towards food supply chain resilience to environmental shocks. Nat. Food 2, 54–65 (2020).Article 

    Google Scholar 
    Wang, X. et al. Emergent constraint on crop yield response to warmer temperature from field experiments. Nat. Sustain. 3, 908–916 (2020).Article 

    Google Scholar 
    Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616–620 (2011).CAS 
    Article 

    Google Scholar 
    Sloat, L. L. et al. Climate adaptation by crop migration. Nat. Commun. 11, 1243 (2020).CAS 
    Article 

    Google Scholar 
    Afifi, T., Liwenga, E. & Kwezi, L. Rainfall-induced crop failure, food insecurity and out-migration in Same-Kilimanjaro, Tanzania. Clim. Dev. 6, 53–60 (2014).Article 

    Google Scholar 
    Stigter, K. in Applied Agrometeorology (ed. Stigter, K.) 531–534 (Springer, 2010).Seifert, C. A. & Lobell, D. B. Response of double cropping suitability to climate change in the United States. Environ. Res. Lett. 10, 024002 (2015).Article 

    Google Scholar 
    Kawasaki, K. Two harvests are better than one: double cropping as a strategy for climate change adaptation. Am. J. Agr. Econ. 101, 172–192 (2019).Article 

    Google Scholar 
    Ceglar, A., Zampieri, M., Toreti, A. & Dentener, F. Observed northward migration of agro‐climate zones in Europe will further accelerate under climate change. Earths Future 7, 1088–1101 (2019).Article 

    Google Scholar 
    Cohn, A. S., VanWey, L. K., Spera, S. A. & Mustard, J. F. Cropping frequency and area response to climate variability can exceed yield response. Nat. Clim. Change 6, 601–604 (2016).Article 

    Google Scholar 
    Challinor, A. J., Simelton, E. S., Fraser, E. D. G., Hemming, D. & Collins, M. Increased crop failure due to climate change: assessing adaptation options using models and socio-economic data for wheat in China. Environ. Res. Lett. 5, 034012 (2010).Article 

    Google Scholar 
    Ray, D. K. & Foley, J. A. Increasing global crop harvest frequency: recent trends and future directions. Environ. Res. Lett. 8, 044041 (2013).Article 

    Google Scholar 
    Wu, W. et al. Global cropping intensity gaps: increasing food production without cropland expansion. Land Use Policy 76, 515–525 (2018).Article 

    Google Scholar 
    Pugh, T. A. M. et al. Climate analogues suggest limited potential for intensification of production on current croplands under climate change. Nat. Commun. 7, 12608 (2016).CAS 
    Article 

    Google Scholar 
    Scherer, L. A., Verburg, P. H. & Schulp, C. J. E. Opportunities for sustainable intensification in European agriculture. Glob. Environ. Change 48, 43–55 (2018).Article 

    Google Scholar 
    Qin, Y. et al. Agricultural risks from changing snowmelt. Nat. Clim. Change 10, 459–465 (2020).Article 

    Google Scholar 
    Waha, K. et al. Multiple cropping systems of the world and the potential for increasing cropping intensity. Glob. Environ. Change 64, 102131 (2020).Article 

    Google Scholar 
    Raderschall, C. A., Vico, G., Lundin, O., Taylor, A. R. & Bommarco, R. Water stress and insect herbivory interactively reduce crop yield while the insect pollination benefit is conserved. Glob. Chang. Biol. 27, 71–83 (2021).CAS 
    Article 

    Google Scholar 
    Ding, M. et al. Variation in cropping intensity in Northern China from 1982 to 2012 based on GIMMS-NDVI data. Sustainability 8, 1123 (2016).Article 

    Google Scholar 
    Yu, Q., Xiang, M., Sun, Z. & Wu, W. The complexity of measuring cropland use intensity: an empirical study. Agr. Syst. 192, 103180 (2021).Article 

    Google Scholar 
    Moore, F. C. & Lobell, D. B. Adaptation potential of European agriculture in response to climate change. Nat. Clim. Change 4, 610–614 (2014).Article 

    Google Scholar 
    Agnolucci, P. et al. Impacts of rising temperatures and farm management practices on global yields of 18 crops. Nat. Food 1, 562–571 (2020).Article 

    Google Scholar 
    Zhu, P. & Burney, J. Temperature‐driven harvest decisions amplify US winter wheat loss under climate warming. Glob. Change Biol. 27, 550–562 (2021).CAS 
    Article 

    Google Scholar 
    Ortiz-Bobea, A., Knippenberg, E. & Chambers, R. G. Growing climatic sensitivity of U.S. agriculture linked to technological change and regional specialization. Sci. Adv. 4, 4343 (2018).Article 

    Google Scholar 
    Duku, C., Zwart, S. J. & Hein, L. Impacts of climate change on cropping patterns in a tropical, sub-humid watershed. PLoS ONE 13, 0192642 (2018).Article 

    Google Scholar 
    Folberth, C. et al. The global cropland-sparing potential of high-yield farming. Nat. Sustain. 3, 281–289 (2020).Article 

    Google Scholar 
    Lobell, D. B. et al. The critical role of extreme heat for maize production in the United States. Nat. Clim. Change 3, 497–501 (2013).Article 

    Google Scholar 
    Yang, X. et al. Potential benefits of climate change for crop productivity in China. Agric. For. Meteorol. 208, 76–84 (2015).Article 

    Google Scholar 
    Burney, J., Woltering, L. & Burke, M. Solar-powered drip irrigation enhances food security in the Sudano–Sahel. Proc. Natl Acad. Sci. USA 107, 1848–1853 (2010).CAS 
    Article 

    Google Scholar 
    You, L. et al. What is the irrigation potential for Africa? A combined biophysical and socioeconomic approach. Food Policy 36, 770–782 (2011).Article 

    Google Scholar 
    Zheng, B., Chenu, K., Fernanda Dreccer, M. & Chapman, S. C. Breeding for the future: what are the potential impacts of future frost and heat events on sowing and flowering time requirements for Australian bread wheat (Triticum aestivium) varieties? Glob. Change Biol. 18, 2899–2914 (2012).Article 

    Google Scholar 
    Flach, R., Fader, M., Folberth, C., Skalský, R. & Jantke, K. The effects of cropping intensity and cropland expansion of Brazilian soybean production on green water flows. Environ. Res. Commun. 2, 071001 (2020).Article 

    Google Scholar 
    Wood, S. A., Jina, A. S., Jain, M., Kristjanson, P. & DeFries, R. S. Smallholder farmer cropping decisions related to climate variability across multiple regions. Glob. Environ. Change 25, 163–172 (2014).Article 

    Google Scholar 
    Paola, A. D. et al. The expansion of wheat thermal suitability of Russia in response to climate change. Land Use Policy 78, 70–77 (2018).Article 

    Google Scholar 
    Brunelle, T. & Makowski, D. Assessing whether the best land is cultivated first: a quantile analysis. PLoS ONE 15, e0242222 (2020).CAS 
    Article 

    Google Scholar 
    Lark, T. J., Spawn, S. A., Bougie, M. & Gibbs, H. K. Cropland expansion in the United States produces marginal yields at high costs to wildlife. Nat. Commun. 11, 4295 (2020).CAS 
    Article 

    Google Scholar 
    Zabel, F., Putzenlechner, B. & Mauser, W. Global agricultural land resources—a high resolution suitability evaluation and its perspectives until 2100 under climate change conditions. PLoS ONE 9, e107522 (2014).Article 

    Google Scholar 
    Petkeviciene, B. The effects of climate factors on sugar beet early sowing timing. Agron. Res. 7, 436–443 (2009).
    Google Scholar 
    Ainsworth, E. A. & Long, S. P. 30 years of free-air carbon dioxide enrichment (FACE): what have we learned about future crop productivity and its potential for adaptation? Glob. Change Biol. 27, 27–49 (2021).CAS 
    Article 

    Google Scholar 
    Collins, M. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) Ch. 11 (Cambridge Univ. Press, 2013).Pendergrass, A. G., Knutti, R., Lehner, F., Deser, C. & Sanderson, B. M. Precipitation variability increases in a warmer climate. Sci. Rep. 7, 17966 (2017).Article 

    Google Scholar 
    Asadieh, B. & Krakauer, N. Y. Global trends in extreme precipitation: climate models versus observations. Hydrol. Earth Syst. Sci. 19, 877–891 (2015).Article 

    Google Scholar 
    Zhang, Y., You, L., Lee, D. & Block, P. Integrating climate prediction and regionalization into an agro-economic model to guide agricultural planning. Clim. Change 158, 435–451 (2020).Article 

    Google Scholar 
    Turner, S. W. D., Hejazi, M., Yonkofski, C., Kim, S. H. & Kyle, P. Influence of groundwater extraction costs and resource depletion limits on simulated global nonrenewable water withdrawals over the twenty‐first century. Earths Future 7, 123–135 (2019).Article 

    Google Scholar 
    Zhu, W., Jia, S., Devineni, N., Lv, A. & Lall, U. Evaluating China’s water security for food production: the role of rainfall and irrigation. Geophys. Res. Lett. 46, 11155–11166 (2019).Article 

    Google Scholar 
    FAOSTAT (Food and Agriculture Organization of the United Nations, 1997).Egli, L., Schröter, M., Scherber, C., Tscharntke, T. & Seppelt, R. Crop asynchrony stabilizes food production. Nature 588, E7–E12 (2020).CAS 
    Article 

    Google Scholar 
    Hersbach, H. et al. ERA5 Hourly Data on Single Levels from 1979 to Present (Copernicus Climate Change Service (C3S) Climate Data Store (CDS), accessed 1 August 2020); https://doi.org/10.24381/cds.adbb2d47 (2018).Feng, P. et al. Impacts of rainfall extremes on wheat yield in semi-arid cropping systems in eastern Australia. Clim. Change 147, 555–569 (2018).Article 

    Google Scholar 
    Teluguntla, P. et al. in Land Resources Monitoring, Modeling, and Mapping with Remote Sensing (ed. Thenkabail, P. S.) 849 (CRC Press, 2015).Hawkins, E. et al. Increasing influence of heat stress on French maize yields from the 1960s to the 2030s. Glob. Change Biol. 19, 937–947 (2013).Article 

    Google Scholar 
    Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).Article 

    Google Scholar 
    Lobell, D. B., Bänziger, M., Magorokosho, C. & Vivek, B. Nonlinear heat effects on African maize as evidenced by historical yield trials. Nat. Clim. Change 1, 42–45 (2011).Article 

    Google Scholar 
    Deryng, D., Sacks, W. J., Barford, C. C. & Ramankutty, N. Simulating the effects of climate and agricultural management practices on global crop yield. Glob. Biogeochem. Cycles 25, GB2006 (2011).New, M., New, M., Lister, D., Hulme, M. & Makin, I. A high-resolution data set of surface climate over global land areas. Clim. Res. 21, 1–25 (2002).Article 

    Google Scholar 
    Willmott, C. J. Terrestrial Air Temperature and Precipitation: Monthly and Annual Time Series (1950–1996) (Center for Climatic Research, 2000); http://climate.geog.udel.edu/~climate/html_pages/README.ghcn_ts2.htmlVan Beveren, I. Total factor productivity estimation: a practical review. J. Econ. Surv. 26, 98–128 (2012).Article 

    Google Scholar 
    Xu, J. et al. Double cropping and cropland expansion boost grain production in Brazil. Nat. Food 2, 264–273 (2021).Article 

    Google Scholar 
    Friedl, M. & Gray, J. MCD12Q2 MODIS/Terra+ Aqua Land Cover Dynamics Yearly L3 Global 500 m SIN Grid V006 (NASA EOSDIS, 2019).Sulla-Menashe, D. & Friedl, M. A. User Guide to Collection 6 MODIS Land Cover (MCD12Q1 and MCD12C1) Product (USGS, 2018).Schwalm, C. R., Glendon, S. & Duffy, P. B. RCP8.5 tracks cumulative CO2 emissions. Proc. Natl Acad. Sci. USA 117, 19656–19657 (2020).CAS 
    Article 

    Google Scholar 
    Lange, S. Trend-preserving bias adjustment and statistical downscaling with ISIMIP3BASD (v1.0). Geosci. Model Dev. 12, 3055–3070 (2019).Article 

    Google Scholar 
    Peng Zhu. Climate effects on caloric yield and cropping frequency. Zenodo https://doi.org/10.5281/zenodo.7038556 (2022). More