More stories

  • in

    Global patterns and climatic controls of forest structural complexity

    1.
    Ali, A. et al. Impacts of climatic and edaphic factors on the diversity, structure and biomass of species-poor and structurally-complex forests. Sci. Total Environ. 706, 135719 (2020).
    ADS  CAS  PubMed  Article  Google Scholar 
    2.
    Gauthier, S., Bernier, P., Kuuluvainen, T., Shvidenko, A. Z. & Schepaschenko, D. G. Boreal forest health and global change. Science 349, 819–822 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    3.
    Seidl, R. et al. Forest disturbances under climate change. Nat. Clim. Change 7, 395–402 (2017).
    ADS  Article  Google Scholar 

    4.
    Penone, C. et al. Specialisation and diversity of multiple trophic groups are promoted by different forest features. Ecol. Lett. 22, 170–180 (2019).
    PubMed  Article  Google Scholar 

    5.
    Stein, A., Gerstner, K. & Kreft, H. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol. Lett. 17, 866–880 (2014).
    PubMed  Article  Google Scholar 

    6.
    Gough, C. M., Atkins, J. W., Fahey, R. T. & Hardiman, B. S. High rates of primary production in structurally complex forests. Ecology 100, e02864 (2019).
    PubMed  Article  Google Scholar 

    7.
    Stark, S. C. et al. Amazon forest carbon dynamics predicted by profiles of canopy leaf area and light environment. Ecol. Lett. 15, 1406–1414 (2012).
    PubMed  Article  Google Scholar 

    8.
    Ammer, C. et al. Key ecological research questions for Central European forests. Basic Appl. Ecol. 32, 3–25 (2018).
    Article  Google Scholar 

    9.
    Kreft, H. & Jetz, W. Global patterns and determinants of vascular plant diversity. Proc. Natl Acad. Sci. USA 104, 5925–5930 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 

    10.
    Harrison, S., Spasojevic, M. J. & Li, D. Climate and plant community diversity in space and time. Proc. Natl Acad. Sci. USA 117, 4464–4470 (2020).
    CAS  PubMed  Article  Google Scholar 

    11.
    Ehbrecht, M., Schall, P., Ammer, C. & Seidel, D. Quantifying stand structural complexity and its relationship with forest management, tree species diversity and microclimate. Agric. Meteorol. 242, 1–9 (2017).
    Article  Google Scholar 

    12.
    Seidel, D., Ehbrecht, M., Annighöfer, P. & Ammer, C. From tree to stand-level structural complexity—Which properties make a forest stand complex? Agric. Meteorol. 278, 107699 (2019).
    Article  Google Scholar 

    13.
    Davies, A. B. & Asner, G. P. Advances in animal ecology from 3D-LiDAR ecosystem mapping. Trends Ecol. Evol. 29, 681–691 (2014).
    PubMed  Article  Google Scholar 

    14.
    Gough, C. M., Atkins, J. W., Fahey, R. T., Hardiman, B. S. & LaRue, E. A. Community and structural constraints on the complexity of eastern North American forests. Glob. Ecol. Biogeogr. 29, 2107–2118 (2020).

    15.
    MacArthur, R. H. & MacArthur, J. W. On bird species diversity. Ecology 42, 594–598 (1961).
    Article  Google Scholar 

    16.
    Ishii, H. T., Tanabe, S. & Hiura, T. Exploring the relationships among canopy structure, stand productivity, and biodiversity of temperate forest ecosystems. Science 50, 342–355 (2004).
    Google Scholar 

    17.
    Pretzsch, H. Forest dynamics, growth, and yield. In Forest Dynamics, Growth and Yield: From Measurement to Model (ed. Pretzsch, H.) 1–39 (Springer, 2009).

    18.
    Dassot, M., Constant, T. & Fournier, M. The use of terrestrial LiDAR technology in forest science: application fields, benefits and challenges. Ann. Sci. 68, 959–974 (2011).
    Article  Google Scholar 

    19.
    Ehbrecht, M., Schall, P., Juchheim, J., Ammer, C. & Seidel, D. Effective number of layers: a new measure for quantifying three-dimensional stand structure based on sampling with terrestrial LiDAR. Ecol. Manag. 380, 212–223 (2016).
    Article  Google Scholar 

    20.
    Juchheim, J., Ammer, C., Schall, P. & Seidel, D. Canopy space filling rather than conventional measures of structural diversity explains productivity of beech stands. Ecol. Manag. 395, 19–26 (2017).
    Article  Google Scholar 

    21.
    Atkins, J. W., Fahey, R. T., Hardiman, B. S. & Gough, C. M. Forest canopy structural complexity and light absorption relationships at the subcontinental scale. J. Geophys. Res. Biogeosci. 123, 1387–1405 (2018).
    Article  Google Scholar 

    22.
    Sapijanskas, J., Paquette, A., Potvin, C., Kunert, N. & Loreau, M. Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences. Ecology 95, 2479–2492 (2014).
    Article  Google Scholar 

    23.
    Fotis, A. T. et al. Forest structure in space and time: Biotic and abiotic determinants of canopy complexity and their effects on net primary productivity. Agric. Meteorol. 250–251, 181–191 (2018).
    Article  Google Scholar 

    24.
    Juchheim, J., Ehbrecht, M., Schall, P., Ammer, C. & Seidel, D. Effect of tree species mixing on stand structural complexity. Int. J. Res. 93, 75–83 (2020).
    Google Scholar 

    25.
    Zemp, D. C. et al. Mixed-species tree plantings enhance structural complexity in oil palm plantations. Agric. Ecosyst. Environ. 283, 106564 (2019).
    Article  Google Scholar 

    26.
    Jucker, T., Bouriaud, O. & Coomes, D. A. Crown plasticity enables trees to optimize canopy packing in mixed-species forests. Funct. Ecol. 29, 1078–1086 (2015).
    Article  Google Scholar 

    27.
    Morin, X. Species richness promotes canopy packing: a promising step towards a better understanding of the mechanisms driving the diversity effects on forest functioning. Funct. Ecol. 29, 993–994 (2015).
    Article  Google Scholar 

    28.
    McDowell, N. et al. Drivers and mechanisms of tree mortality in moist tropical forests. New Phytol. 851–869 https://doi.org/10.1111/nph.15027@10.1111/(ISSN)1469-8137. (2018).

    29.
    Pretzsch, H. Size-structure dynamics in mixed versus monospecific stands. In Mixed-Species Forests: Ecology and Management (eds. Pretzsch, H., Forrester, D. I. & Bauhus, J.) 211–269 (Springer, 2017).

    30.
    Moncrieff, G. R., Bond, W. J. & Higgins, S. I. Revising the biome concept for understanding and predicting global change impacts. J. Biogeogr. 43, 863–873 (2016).
    Article  Google Scholar 

    31.
    Stegen, J. C. et al. Variation in above-ground forest biomass across broad climatic gradients. Glob. Ecol. Biogeogr. 20, 744–754 (2011).
    Article  Google Scholar 

    32.
    Dubayah, R. et al. The global ecosystem dynamics investigation: high-resolution laser ranging of the Earth’s forests and topography. Sci. Remote Sens. 1, 100002 (2020).
    Article  Google Scholar 

    33.
    Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Article  Google Scholar 

    34.
    Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).
    Article  Google Scholar 

    35.
    Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on earth a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933–938 (2001).
    Article  Google Scholar 

    36.
    Currie, D. J. et al. Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecol. Lett. 7, 1121–1134 (2004).
    Article  Google Scholar 

    37.
    Valladares, F. & Niinemets, Ü. Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst. 39, 237–257 (2008).
    Article  Google Scholar 

    38.
    Ryan, M. G., Phillips, N. & Bond, B. J. The hydraulic limitation hypothesis revisited. Plant Cell Environ. 29, 367–381 (2006).
    PubMed  Article  Google Scholar 

    39.
    Klein, T., Randin, C. & Körner, C. Water availability predicts forest canopy height at the global scale. Ecol. Lett. 18, 1311–1320 (2015).
    PubMed  Article  Google Scholar 

    40.
    Asner, G. P. et al. Airborne laser-guided imaging spectroscopy to map forest trait diversity and guide conservation. Science 355, 385–389 (2017).
    ADS  CAS  PubMed  Article  Google Scholar 

    41.
    Schneider, F. D. et al. Mapping functional diversity from remotely sensed morphological and physiological forest traits. Nat. Commun. 8, 1441 (2017).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    42.
    Thonicke, K. et al. Simulating functional diversity of European natural forests along climatic gradients. J. Biogeogr. 47, 1069–1085 (2020).
    Article  Google Scholar 

    43.
    Willim, K. et al. Assessing understory complexity in beech-dominated Forests (Fagus sylvatica L.) in Central Europe—from managed to primary forests. Sensors 19, 1684 (2019).
    Article  Google Scholar 

    44.
    Eggeling, W. J. Observations on the Ecology of the Budongo Rain Forest, Uganda. J. Ecol. 34, 20–87 (1947).
    Article  Google Scholar 

    45.
    Stephens, S. L. & Gill, S. J. Forest structure and mortality in an old-growth Jeffrey pine-mixed conifer forest in north-western Mexico. Ecol. Manag. 205, 15–28 (2005).
    Article  Google Scholar 

    46.
    Senf, C., Mori, A. S., Müller, J. & Seidl, R. The response of canopy height diversity to natural disturbances in two temperate forest landscapes. Landsc. Ecol. https://doi.org/10.1007/s10980-020-01085-7. (2020)

    47.
    Senf, C. & Seidl, R. Mapping the forest disturbance regimes of Europe. Nat. Sustain. 1–8 https://doi.org/10.1038/s41893-020-00609-y. (2020).

    48.
    Krug, J. H. A. Adaptation of Colophospermum mopane to extra-seasonal drought conditions: site-vegetation relations in dry-deciduous forests of Zambezi region (Namibia). Ecosystems 4, 25 (2017).
    Google Scholar 

    49.
    Stovall, A. E. L., Shugart, H. & Yang, X. Tree height explains mortality risk during an intense drought. Nat. Commun. 10, 4385 (2019).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    50.
    Zemp, D. C. et al. Self-amplified Amazon forest loss due to vegetation-atmosphere feedbacks. Nat. Commun. 8, 1–10 (2017).
    Article  CAS  Google Scholar 

    51.
    Schuldt, B. et al. How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? N. Phytol. 210, 443–458 (2016).
    Article  Google Scholar 

    52.
    Astrup, R., Bernier, P. Y., Genet, H., Lutz, D. A. & Bright, R. M. A sensible climate solution for the boreal forest. Nat. Clim. Change 8, 11–12 (2018).
    ADS  Article  Google Scholar 

    53.
    Trisos, C. H., Merow, C. & Pigot, A. L. The projected timing of abrupt ecological disruption from climate change. Nature 580, 496–501 (2020).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    54.
    Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    55.
    Klein, T. & Hartmann, H. Climate change drives tree mortality. Science 362, 758–758 (2018).
    ADS  CAS  PubMed  Google Scholar 

    56.
    Puettmann, K. J., Coates, K. D. & Messier, C. C. A Critique of Silviculture: Managing for Complexity. (Island Press, 2012).

    57.
    Camarretta, N. et al. Monitoring forest structure to guide adaptive management of forest restoration: a review of remote sensing approaches. New For. https://doi.org/10.1007/s11056-019-09754-5. (2019).

    58.
    Chiarucci, A. & Piovesan, G. Need for a global map of forest naturalness for a sustainable future. Conserv. Biol. 34, 368–372 (2020).
    PubMed  Article  Google Scholar 

    59.
    Potapov, P. et al. The last frontiers of wilderness: tracking loss of intact forest landscapes from 2000 to 2013. Sci. Adv. 3, e1600821 (2017).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    60.
    Bastin, J.-F. et al. The global tree restoration potential. Science 365, 76–79 (2019).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    61.
    Keane, R. E., Holsinger, L. M. & Loehman, R. Bioclimatic modeling of potential vegetation types as an alternative to species distribution models for projecting plant species shifts under changing climates. Ecol. Manag. 477, 118498 (2020).
    Article  Google Scholar 

    62.
    Kier, G. et al. Global patterns of plant diversity and floristic knowledge. J. Biogeogr. 32, 1107–1116 (2005).
    Article  Google Scholar 

    63.
    Schneider, F. D. et al. Towards mapping the diversity of canopy structure from space with GEDI. Environ. Res. Lett. https://doi.org/10.1088/1748-9326/ab9e99. (2020).

    64.
    Campbell, N. A. Biology. (Pearson Education, 1996).

    65.
    Buchwald, E. A hierarchical terminology for more or less natural forests in relation to sustainable management and biodiversity conservation. In Proc. Third Expert Meeting on Harmonizing Forest-related Definitions for Use by Various Stakeholders. Vol. 18 (Food and Agriculture Organization of the United Nations, 2005).

    66.
    Frey, J., Asbeck, T. & Bauhus, J. Predicting tree-related microhabitats by multisensor close-range remote sensing structural parameters for the selection of retention elements. Remote Sens. 12, 867 (2020).
    ADS  Article  Google Scholar 

    67.
    Ehbrecht, M., Schall, P., Ammer, C., Fischer, M. & Seidel, D. Effects of structural heterogeneity on the diurnal temperature range in temperate forest ecosystems. Ecol. Manag. 432, 860–867 (2019).
    Article  Google Scholar 

    68.
    Ehbrecht et al. ehbrechtetal/Stand-structural-complexity-index–SSCI: R-code to compute the stand structural complexity index (SSCI). https://doi.org/10.5281/zenodo.4295910. (2017).

    69.
    Trabucco, A. & Zomer, R. Global Aridity Index and Potential Evapotranspiration (ET0) Climate Database v2. https://doi.org/10.6084/m9.figshare.7504448.v3. (2019)

    70.
    Hengl, T. et al. SoilGrids250m: Global gridded soil information based on machine learning. PLoS ONE 12, e0169748 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    71.
    Wieder, W. R., Boehnert, J., Bonan, G. B. & Langseth, M. Regridded Harmonized World Soil Database v1.2. ORNL DAAC. https://doi.org/10.3334/ORNLDAAC/1247 (2014).

    72.
    Fehrmann, L. et al. A unified framework for land cover monitoring based on a discrete global sampling grid (GSG). Environ. Monit. Assess. 191, 46 (2019).
    PubMed  Article  Google Scholar  More

  • in

    Effects of a commercially formulated glyphosate solutions at recommended concentrations on honeybee (Apis mellifera L.) behaviours

    1.
    Gallai, N., Salles, J., Settele, J. & Vaissière, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).
    Article  Google Scholar 
    2.
    Carreck, N. L. & Ratnieks, F. L. W. The dose makes the poison: have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies?. J. Apicult. Res. 53, 607–614 (2014).
    Article  Google Scholar 

    3.
    Gross, M. New fears over bee declines. Curr. Biol. 21, 137–139 (2011).
    Article  CAS  Google Scholar 

    4.
    Lundin, O., Smith, H. G., Fries, I. & Bommarco, R. Neonicotinoid insecticides and their impacts on bees: A systematic review of research approaches and identification of knowledge gaps. PLoS ONE 10, 2 (2015).
    Google Scholar 

    5.
    Rucker, R. R., Thurman, W. N. & Burgett, M. Honey bee pollination markets and the internalization of reciprocal benefits. Am. J. Agr. Econ. 94, 956–977 (2012).
    Article  Google Scholar 

    6.
    Kremen, C., Williams, N. M. & Thorp, R. W. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. USA. 99, 16812–16816 (2002).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    7.
    Koh, I., Lonsdorf, E. V., Artz, D. R., Pitts-Singer, T. L. & Ricketts, T. H. Ecology and economics of using native managed bees for almond pollination. J. Econ. Entomol. 111, 16–25 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    8.
    Stein, K. et al. Bee pollination increases yield quantity and quality of cash crops in Burkina Faso, West Africa. Sci. Rep.-UK 7, 17610–17691 (2017).
    Article  CAS  Google Scholar 

    9.
    Claudianos, C. et al. A deficit of detoxification enzymes: Pesticide sensitivity and environmental response in the honeybee. Insect Mol. Biol. 15, 615–636 (2006).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    10.
    Abraham, J. et al. Commercially formulated glyphosate can kill non-target pollinator bees under laboratory conditions. Entomol. Exp. Appl. 166, 695–702 (2018).
    CAS  Article  Google Scholar 

    11.
    Polyzou, A., Froment, M., Masson, P. & Belzunces, L. P. Absence of a protective effect of the oxime 2-PAM toward paraoxon-poisoned honey bees: Acetylcholinesterase reactivation not at fault. Toxicol. Appl. Pharm. 152, 184–192 (1998).
    CAS  Article  Google Scholar 

    12.
    Stanley, J., Sah, K., Jain, S. K., Bhatt, J. C. & Sushil, S. N. Evaluation of pesticide toxicity at their field recommended doses to honeybees, Apis cerana and A. mellifera through laboratory, semi-field and field studies. Chemosphere 119, 668–674 (2015).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    13.
    Christen, V. & Fent, K. Exposure of honey bees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environ. Pollut. 226, 48–59 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    14.
    Friol, P. S., Catae, A. F., Tavares, D. A., Malaspina, O. & Roat, T. C. Can the exposure of Apis mellifera (Hymenoptera, Apiadae) larvae to a field concentration of thiamethoxam affect newly emerged bees?. Chemosphere 185, 56–66 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    Fulton, C. A. et al. An assessment of pesticide exposures and land use of honey bees in Virginia. Chemosphere 222, 489–493 (2019).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    16.
    Report, C. R. I. Glyphosate industry overview in China, 2011–2020 (CRI, Shanghai, 2018).
    Google Scholar 

    17.
    Herbert, L. T., Vazquez, D. E., Arenas, A. & Farina, W. M. Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J. Exp. Biol. 217, 3457–3464 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    18.
    Motta, E. V. S., Raymann, K. & Moran, N. A. Glyphosate perturbs the gut microbiota of honey bees. Proc. Natl. Acad. Sci. USA. 115, 10305–10310 (2018).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    19.
    Rahimian, Y. Effect of glyphosate on honey bee (Apis mellifera) performance. Arthropods. 7, 77–81 (2018).
    Google Scholar 

    20.
    Thompson, H. M. et al. Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr. Environ. Asses. 10, 463–470 (2014).
    ADS  CAS  Article  Google Scholar 

    21.
    FAO, China at a glance. http://www.fao.org/china/fao-in-china/china-at-a-glance/en/. (2019) Available.

    22.
    Hou, J. H. Path construction for the reform of the rural land property system. J. Huaiyin Inst. Technol. (2019).

    23.
    Zhang, C. et al. Health effect of agricultural pesticide use in China: Implications for the development of GM crops. Sci. Rep.-UK 6, 2 (2016).
    Article  CAS  Google Scholar 

    24.
    Michalková, V. & Pekár, S. How glyphosate altered the behaviour of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: Carabidae). Biol. Control. 51, 444–449 (2009).
    Article  CAS  Google Scholar 

    25.
    Janssens, L. & Stoks, R. Stronger effects of Roundup than its active ingredient glyphosate in damselfly larvae. Aquat. Toxicol. 193, 210–216 (2017).
    CAS  PubMed  Article  Google Scholar 

    26.
    García-Espiñeira, M., Tejeda-Benitez, L. & Olivero-Verbel, J. Toxicity of atrazine- and glyphosate-based formulations on Caenorhabditis elegans. Ecotox. Environ. Safe. 156, 216–222 (2018).
    Article  CAS  Google Scholar 

    27.
    Tierney, K. B., Singh, C. R., Ross, P. S. & Kennedy, C. J. Relating olfactory neurotoxicity to altered olfactory-mediated behaviors in rainbow trout exposed to three currently-used pesticides. Aquat. Toxicol. 81, 55–64 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    28.
    Tierney, K. B., Ross, P. S., Jarrard, H. E., Delaney, K. R. & Kennedy, C. J. Changes in juvenile coho salmon electro-olfactogram during and after short-term exposure to current-use pesticides. Environ. Toxicol. Chem. 25, 2809–2817 (2006).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    29.
    Cattani, D. et al. Developmental exposure to glyphosate-based herbicide and depressive-like behavior in adult offspring: implication of glutamate excitotoxicity and oxidative stress. Toxicology 387, 67–80 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    30.
    Zaluski, R., Kadri, S. M., Alonso, D. P., Martins Ribolla, P. E. & de Oliveira, O. R. Fipronil promotes motor and behavioral changes in honey bees (Apis mellifera) and affects the development of colonies exposed to sublethal doses. Environ. Toxicol. Chem. 34, 1062–1069 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    31.
    El Hassani, A. K. et al. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch. Environ. Con. Tox. 54, 653–661 (2008).
    Article  CAS  Google Scholar 

    32.
    Balbuena, M. S. et al. Effects of sublethal doses of glyphosate on honeybee navigation. J. Exp. Biol. 218, 2799–2805 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    33.
    Company, Monsanto. Material safety data sheet for Roundup Original Herbicide. https://www.fumigationzone.com/files/53/Roundup+Original+-+EPA. (2006).

    34.
    Decourtye, A., Lacassie, E. & Pham-Delègue, M. Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest. Manag. Sci. 59, 269–278 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Haydak, M. H. Honey bee nutrition. Annu. Rev. Entomol. 15, 143–156 (1970).
    Article  Google Scholar 

    36.
    Winston, M. L. The biology of the honey bee. Q. Rev. Biol. 27, 239–243 (1987).
    Google Scholar 

    37.
    Wang, N. et al. Influence of sediment on the fate and toxicity of a polyethoxylated tallowamine surfactant system (MON 0818) in aquatic microcosms. Chemosphere 59, 545–551 (2005).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    38.
    Brausch, J. M., Beall, B. & Smith, P. N. Acute and sub-lethal toxicity of three POEA surfactant formulations to Daphnia magna. Bull. Environ. Contam. Toxicol. 78, 510–514 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    39.
    Brausch, J. M., Brausch, J. M., Smith, P. N. & Smith, P. N. Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp Thamnocephalus platyurus. Arch. Environ. Con. Tox. 52, 217–221 (2007).
    CAS  Article  Google Scholar 

    40.
    Benachour, N. & Seralini, G. Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem. Res. Toxicol. 22, 97–105 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    41.
    Gasnier, C. et al. Dig1 protects against cell death provoked by glyphosate-based herbicides in human liver cell lines. J. Occup. Med. Toxicol. 5, 29 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    42.
    Tsui, M. T. K. & Chu, L. M. Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factors. Chemosphere 52, 1189–1197 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    43.
    Marc, J. et al. A glyphosate-based pesticide impinges on transcription. Toxicol. Appl. Pharm. 203, 1–8 (2005).
    CAS  Article  Google Scholar 

    44.
    Defarge, N. et al. Co-Formulants in glyphosate-based herbicides disrupt aromatase activity in human cells below toxic levels. Int. J. Env. Res. Pub. He. 13, 264 (2016).
    Article  CAS  Google Scholar 

    45.
    NPIC., Techincal fact sheet for glyphosate. http://npic.orst.edu/factsheets/archive/glyphotech.html (2011).

    46.
    Mengoni, G. C. & Farina, W. M. Impaired associative learning after chronic exposure to pesticides in young adult honey bees. J. Exp. Biol. 221, 2 (2018).
    Google Scholar 

    47.
    Balbuena, M. S., Arenas, A. & Farina, W. M. Floral scents learned inside the honeybee hive have a long-lasting effect on recruitment. Anim. Behav. 84, 77–83 (2012).
    Article  Google Scholar 

    48.
    Goyret, J. & Farina, W. M. Non-random nectar unloading interactions between foragers and their receivers in the honeybee hive. Sci. Nat.-Heidelberg. 92, 440–443 (2005).
    CAS  Article  Google Scholar 

    49.
    Faita, M. R., Oliveira, E. D. M., Alves, V. V., Orth, A. I. & Nodari, R. O. Changes in hypopharyngeal glands of nurse bees (Apis mellifera) induced by pollen-containing sublethal doses of the herbicide Roundup. Chemosphere 211, 566–572 (2018).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    50.
    Mesnage, R. et al. Glyphosate exposure in a farmer’s family. J. Environ. Prot. 03, 1001–1003 (2012).
    CAS  Article  Google Scholar 

    51.
    Samsel, A. & Seneff, S. Glyphosate’s suppression of cytochrome p450 enzymes and amino acid biosynthesis by the gut microbiome: pathways to modern diseases. Entropy-Switz. 15, 1416–1463 (2013).
    ADS  CAS  Article  Google Scholar 

    52.
    Ying, C. Brief analysis on the application technique of Roundup. Forest Investig. Des. 2, 39–40 (2007).
    MathSciNet  Google Scholar 

    53.
    Jing, X., Qi, J. & Yang, H. Pesticide residue level and dietary exposure risk assessment of Lycium barbarum in Golmud. Ecol. Environ. 28, 1007–1012 (2019).
    Google Scholar 

    54.
    Decourtye, A. et al. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch. Environ. Con. Tox. 48, 242–250 (2005).
    CAS  Article  Google Scholar  More

  • in

    Beneath the glacier

    The frigid environment under glaciers is inhospitable to all but the most intrepid of microscopic life. To eke out a living, these microbes must do without sunlight and the photosynthetically fixed carbon that fuels most other ecosystems on Earth. Instead, such ecosystems are likely supported by chemosynthetic primary production that capitalizes on energy from inorganic reactions to produce biomass, but the exact mechanisms enabling such chemosynthetic life under the ice are unknown.

    Eric Dunham, from Montana State University, USA, and colleagues collected sediments from a glacial system in Iceland that overlays a silicate mineral-rich basaltic catchment, conditions that are prevalent across glacial systems. High concentrations of the reductant hydrogen (H2) were detected, which likely formed when silicate minerals pulverized by the glacier reacted with water. In microcosms seeded with the sediments and amended with H2 and 14CO2, subglacial microbes could oxidize H2, using the resulting energy for chemosynthetic carbon fixation. Metagenomic sequencing from enrichment cultures revealed two prominent autotrophic hydrogenotroph populations, one likely restricted to H2-based chemoautotrophy and one with genomic potential for mixotrophy. The populations exhibited rates of H2 oxidation and carbon fixation approximately tenfold higher than those taken from a Canadian glacier overlying carbonate and shale, suggesting specialization to H2-rich conditions in basalt-glacier systems.

    Credit: Natthawat/Getty Images

    Interactions between glaciers and rock that can turn an otherwise inhospitable environment into a home for microbes could have implications beyond present-day Earth. Icy H2-dependent primary production could have sustained life during Snowball Earth episodes in our planet’s distant past, or could pave the way for life to evolve on Saturn’s frozen moon Enceladus. More

  • in

    Developmental stages of peach, plum, and apple fruit influence development and fecundity of Grapholita molesta (Lepidoptera: Tortricidae)

    Stage development and survival rates
    Egg duration of G. molesta was not affected by fruit species (F = 0.54, df = 2, 261, P = 0.581), by collection date (F = 0.06, df = 2, 261, P = 0.941), or by fruit species by collection date interaction (F = 0.24, df = 4, 261, P = 0.914) (Table 1). Durations of other life stages were all significantly affected by fruit species (larva F = 28.16, df = 2, 144, P  More

  • in

    Group-level cooperation in chimpanzees is shaped by strong social ties

    1.
    House, J. S., Landis, K. R. & Umberson, D. Social relationships and health. Science 241, 540–545 (1988).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 
    2.
    Holt-Lunstad, J., Smith, T. B. & Layton, J. B. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 7, e1000316 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    3.
    Silk, J. B., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance infant survival. Science 302, 1231–1234 (2003).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    4.
    Wittig, R. M. et al. Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations. Nat. Commun. 7, 13361 (2016).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    5.
    Schülke, O., Bhagavatula, J., Vigilant, L. & Ostner, J. Social bonds enhance reproductive success in male macaques. Curr. Biol. 20, 2207–2210 (2010).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    6.
    Cameron, E. Z., Setsaas, T. H. & Linklater, W. L. Social bonds between unrelated females increase reproductive success in feral horses. Proc. Natl Acad. Sci. USA 106, 13850–13853 (2009).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    7.
    Silk, J. B. et al. Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20, 1359–1361 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    8.
    Barocas, A., Ilany, A., Koren, L., Kam, M. & Geffen, E. Variance in centrality within rock Hyrax social networks predicts adult longevity. PLoS ONE 6, e22375 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Riehl, C. & Strong, M. J. Stable social relationships between unrelated females increase individual fitness in a cooperative bird. Proc. R. Soc. B 285, 20180130 (2018).
    PubMed  Article  Google Scholar 

    10.
    Cheney, D. L. Extent and limits of cooperation in animals. Proc. Natl. Acad. Sci. USA 201100291 (2011) https://doi.org/10.1073/pnas.1100291108.

    11.
    Boyd, R. & Richerson, P. J. The evolution of indirect reciprocity. Soc. Netw. 11, 213–236 (1989).
    MathSciNet  Article  Google Scholar 

    12.
    Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).
    Article  Google Scholar 

    13.
    Nowak, M. A., Tarnita, C. E. & Wilson, E. O. The evolution of eusociality. Nature 466, 1057–1062 (2010).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    14.
    Apicella, C. L., Marlowe, F. W., Fowler, J. H. & Christakis, N. A. Social networks and cooperation in hunter-gatherers. Nature 481, 497–501 (2012).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    15.
    Dyble, M. et al. Networks of food sharing reveal the functional significance of multilevel sociality in two hunter-gatherer groups. Curr. Biol. 26, 2017–2021 (2016).
    CAS  PubMed  Article  Google Scholar 

    16.
    Samuni, L. et al. Social bonds facilitate cooperative resource sharing in wild chimpanzees. Proc. R. Soc. B 285, 20181643 (2018).
    PubMed  Article  Google Scholar 

    17.
    Mitani, J. C. Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633–640 (2009).
    Article  Google Scholar 

    18.
    Langergraber, K. E., Mitani, J. C. & Vigilant, L. The limited impact of kinship on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. USA 104, 7786–7790 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 

    19.
    Kern, J. M. & Radford, A. N. Social-bond strength influences vocally mediated recruitment to mobbing. Biol. Lett. 12, (2016).

    20.
    Gero, S., Engelhaupt, D., Rendell, L. & Whitehead, H. Who cares? Between-group variation in alloparental caregiving in sperm whales. Behav. Ecol. 20, 838–843 (2009).
    Article  Google Scholar 

    21.
    Wilkinson, G. S., Carter, G. G., Bohn, K. M. & Adams, D. M. Non-kin cooperation in bats. Philos. Trans. R. Soc. B 371, 20150095 (2016).
    Article  Google Scholar 

    22.
    Langergraber, K. E., Watts, D. P., Vigilant, L. & Mitani, J. C. Group augmentation, collective action, and territorial boundary patrols by male chimpanzees. Proc. Natl Acad. Sci. USA 114, 7337–7342 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    23.
    Samuni, L., Mielke, A., Preis, A., Crockford, C. & Wittig, R. M. Intergroup competition enhances chimpanzee (Pan troglodytes verus) in-group cohesion. Int. J. Primatol. (2019).

    24.
    Majolo, B., deBortoli Vizioli, A., Martínez-Íñigo, L. & Lehmann, J. Effect of group size and individual characteristics on intergroup encounters in primates. Int. J. Primatol. (2020), https://doi.org/10.1007/s10764-019-00119-5.

    25.
    Mirville, M. O. et al. Factors influencing individual participation during intergroup interactions in mountain gorillas. Anim. Behav. 144, 75–86 (2018).
    Article  Google Scholar 

    26.
    Arseneau-Robar, T. J. M., Taucher, A. L., Schnider, A. B., van Schaik, C. P. & Willems, E. P. Intra- and interindividual differences in the costs and benefits of intergroup aggression in female vervet monkeys. Anim. Behav. 123, 129–137 (2017).
    Article  Google Scholar 

    27.
    Willems, E. P. & van Schaik, C. P. Collective action and the intensity of between-group competition in nonhuman primates. Behav. Ecol. 26, 625–631 (2015).
    Article  Google Scholar 

    28.
    Schel, A. M., Townsend, S. W., Machanda, Z., Zuberbühler, K. & Slocombe, K. E. Chimpanzee alarm call production meets key criteria for intentionality. PLoS ONE 8, e76674 (2013).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    29.
    Fuong, H., Maldonado-Chaparro, A. & Blumstein, D. T. Are social attributes associated with alarm calling propensity? Behav. Ecol. 26, 587–592 (2015).
    Article  Google Scholar 

    30.
    Crockford, C., Wittig, R. M., Mundry, R. & Zuberbühler, K. Wild chimpanzees inform ignorant group members of danger. Curr. Biol. 22, 142–146 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    31.
    Nam, K.-B., Simeoni, M., Sharp, S. P. & Hatchwell, B. J. Kinship affects investment by helpers in a cooperatively breeding bird. Proc. R. Soc. B 277, 3299–3306 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    32.
    Samuni, L., Wittig, R. & Crockford, C. Adoption in the Taï chimpanzees: costs, benefits and strong social relationships. In The Chimpanzees of the Taï Forest: 40 Years of Research (eds Boesch, C. & Wittig, R.) 141–158 (Cambridge University Press, 2019).

    33.
    Bowles, S. Did warfare among ancestral hunter-gatherers affect the evolution of human social behaviors? Science 324, 1293–1298 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    34.
    Puurtinen, M. & Mappes, T. Between-group competition and human cooperation. Proc. R. Soc. Lond. B 276, 355–360 (2009).
    Google Scholar 

    35.
    Mitani, J. C., Watts, D. P. & Amsler, S. J. Lethal intergroup aggression leads to territorial expansion in wild chimpanzees. Curr. Biol. 20, R507–R508 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    36.
    Lemoine, S. et al. Between-group competition impacts reproductive success in wild chimpanzees. Curr. Biol. (2020).

    37.
    Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414–417 (2014).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    38.
    Williams, J. M., Oehlert, G. W., Carlis, J. V. & Pusey, A. E. Why do male chimpanzees defend a group range? Anim. Behav. 68, 523–532 (2004).
    Article  Google Scholar 

    39.
    Wrangham, R.W. Evolution of coalitionary killing. Yrbk. Phys. Anthropol. 42, 1–30 (1999).
    Article  Google Scholar 

    40.
    Wilson, M. L., Hauser, M. D. & Wrangham, R. W. Does participation in intergroup conflict depend on numerical assessment, range location, or rank for wild chimpanzees? Anim. Behav. 61, 1203–1216 (2001).
    Article  Google Scholar 

    41.
    McComb, K., Packer, C. & Pusey, A. Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Anim. Behav. 47, 379–387 (1994).
    Article  Google Scholar 

    42.
    Langergraber, K. E., Mitani, J. & Vigilant, L. Kinship and social bonds in female chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 840–851 (2009).
    PubMed  Article  Google Scholar 

    43.
    Wittig, R. M., Crockford, C., Langergraber, K. & Zuberbühler, K. Triadic social interactions operate across time: a field experiment with wild chimpanzees. Proc. R. Soc. B 281, 20133155 (2014).
    PubMed  Article  Google Scholar 

    44.
    Watts, D. P. & Mitani, J. C. Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138, 299–327 (2001).
    Article  Google Scholar 

    45.
    Samuni, L. et al. Oxytocin reactivity during intergroup conflict in wild chimpanzees. Proc. Natl Acad. Sci. USA 114, 268–273 (2017).
    CAS  PubMed  Article  Google Scholar 

    46.
    De Dreu, C. K. W. et al. The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328, 1408–1411 (2010).
    ADS  PubMed  Article  CAS  Google Scholar 

    47.
    Wrangham, R. W. Why are male chimpanzees more gregarious than mothers? in Primate Males: Causes and Consequences of Variation in Group Composition (ed. Kappeler, P. M.) (Cambridge University Press, 2000).

    48.
    Boesch, C. et al. Intergroup conflicts among chimpanzees in Taï National Park: lethal violence and the female perspective. Am. J. Primatol. 70, 519–532 (2008).
    PubMed  Article  Google Scholar 

    49.
    Van Belle, S., Garber, P. A., Estrada, A. & Di Fiore, A. Social and genetic factors mediating male participation in collective group defence in black howler monkeys. Anim. Behav. 98, 7–17 (2014).
    Article  Google Scholar 

    50.
    Thompson, F. J., Marshall, H. H., Vitikainen, E. I. K. & Cant, M. A. Causes and consequences of intergroup conflict in cooperative banded mongooses. Anim. Behav. 126, 31–40 (2017).
    Article  Google Scholar 

    51.
    Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).
    ADS  MathSciNet  CAS  PubMed  MATH  Article  Google Scholar 

    52.
    Smith, D. et al. Camp stability predicts patterns of hunter-gatherer cooperation. R. Soc. Open Sci. 3, 160131 (2016).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    53.
    Samuni, L., Preis, A., Deschner, T., Wittig, R. M. & Crockford, C. Cortisol and oxytocin show independent activity during chimpanzee intergroup conflict. Psychoneuroendocrinology 104, 165–173 (2019).
    CAS  PubMed  Article  Google Scholar 

    54.
    Surbeck, M. et al. Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees. Curr. Biol. 29, R354–R355 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    55.
    Crockford, C., Samuni, L., Vigilant, L. & Wittig, R. M. Postweaning maternal care increases male chimpanzee reproductive success. Sci. Adv. 6, eaaz5746 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    56.
    McDonald, M. M., Navarrete, C. D. & Vugt, M. V. Evolution and the psychology of intergroup conflict: the male warrior hypothesis. Philos. Trans. R. Soc. B 367, 670–679 (2012).
    Article  Google Scholar 

    57.
    Bernhard, H., Fischbacher, U. & Fehr, E. Parochial altruism in humans. Nature 442, 912–915 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 

    58.
    Kaplan, H. S., Hill, K., Lancaster, J. & Hurtado, A. M. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. Issues News Rev. 9, 156–185 (2000).
    Article  Google Scholar 

    59.
    Boesch, C. Cooperative hunting in wild chimpanzees. Anim. Behav. 48, 653–667 (1994).
    Article  Google Scholar 

    60.
    Samuni, L., Preis, A., Deschner, T., Crockford, C. & Wittig, R. M. Reward of labor coordination and hunting success in wild chimpanzees. Commun. Biol. 1, 138 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    61.
    Boesch, C. & Boesch-Achermann, H. The Chimpanzees of the Taï Forest: Behavioural Ecology and Evolution (Oxford University Press, 2000).

    62.
    Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, 227–266 (1974).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Wittig, R. M. & Boesch, C. Observation protocol and long-term data collection in Taï. In The Taï Chimpanzees: 40 years of Research (Cambridge University Press, 2019).

    64.
    Goodall. The Chimpanzees of Gombe: Patterns of Behavior (Harvard University Press, 1986).

    65.
    Schubert, G. et al. Co-residence between males and their mothers and grandmothers is more frequent in bonobos than chimpanzees. PLoS ONE 8, e83870 (2013).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    66.
    Arandjelovic, M. et al. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol. Ecol. Resour. 9, 28–36 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    67.
    Neumann, C. et al. Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim. Behav. 82, 911–921 (2011).
    Article  Google Scholar 

    68.
    Foerster, S. et al. Chimpanzee females queue but males compete for social status. Sci. Rep. 6, 1–11 (2016).
    Article  CAS  Google Scholar 

    69.
    Mielke, A. et al. Bystanders intervene to impede grooming in Western chimpanzees and sooty mangabeys. R. Soc. Open Sci. 4, 171296 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    70.
    Kulik, L. Development and Consequences of Social Behavior in Rhesus Macaques (Macaca mulatta) (University of Leipzig, 2015).

    71.
    Tkaczynski, P. J. et al. Long-term repeatability in social behaviour suggests stable social phenotypes in wild chimpanzees. R. Soc. Open Sci. 7, 200454 (2020).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    72.
    Anderson, D. P., Nordheim, E. V., Boesch, C. & Moermond, C. Factors influencing fission-fusion grouping in chimpanzees in the Taï National Park, Côte D’Ivoire. In Behavioural Diversity in Chimpanzees and Bonobos (eds Boesch, C., Hohmann, G. & Marchant, L. F.) 90–101 (Cambridge University Press, 2002).

    73.
    Baayen, R. H. Analyzing Linguistic Data: A Practical Introduction to Statistics using R (Cambridge University Press, 2008).

    74.
    Goodall, J. Population dynamics during a 15 year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania. Z. Tierpsychol. 61, 1–60 (1983).
    Article  Google Scholar 

    75.
    Behringer, V., Deschner, T., Deimel, C., Stevens, J. M. G. & Hohmann, G. Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees. Horm. Behav. 66, 525–533 (2014).
    CAS  PubMed  Article  Google Scholar 

    76.
    Emery Thompson, M., Muller, M. N. & Wrangham, R. W. The energetics of lactation and the return to fecundity in wild chimpanzees. Behav. Ecol. 23, 1234–1241 (2012).
    Article  Google Scholar 

    77.
    Nissen, H. W. & Yerkes, R. M. Reproduction in the chimpanzee: report on forty-nine births. Anat. Rec. 86, 567–578 (1943).
    Article  Google Scholar 

    78.
    Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23–35 (2011).
    Article  Google Scholar 

    79.
    Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: keep it maximal. J. Mem. Lang. 68, 255–278 (2013).
    Article  Google Scholar 

    80.
    Schielzeth, H. & Forstmeier, W. Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416–420 (2009).
    PubMed  Article  Google Scholar 

    81.
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2016).

    82.
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Article  Google Scholar 

    83.
    Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).
    Article  Google Scholar 

    84.
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage Publications, 2011).

    85.
    Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge University Press, 2002).

    86.
    Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011).
    PubMed  Article  Google Scholar 

    87.
    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).
    Article  Google Scholar  More

  • in

    Life history, climate and biogeography interactively affect worldwide genetic diversity of plant and animal populations

    1.
    Ceballos, G. & Ehrlich, P. R. Mammal population losses and the extinction crisis. Science 296, 904–907 (2002).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 
    2.
    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    3.
    Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6, 8568 (2015).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    4.
    Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    5.
    Tilman, D. et al. Future threats to biodiversity and pathways to their prevention. Nature 546, 73–81 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Mittell, E. A., Nakagawa, S. & Hadfield, J. D. Are molecular markers useful predictors of adaptive potential? Ecol. Lett. 18, 772–778 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    7.
    Vilas, A., Pérez-Figueroa, A., Quesada, H. & Caballero, A. Allelic diversity for neutral markers retains a higher adaptive potential for quantitative traits than expected heterozygosity. Mol. Ecol. 24, 4419–4432 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    8.
    Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M. & Wayne, R. K. Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290–295 (2000).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    9.
    Paz-Vinas, I. et al. Systematic conservation planning for intraspecific genetic diversity. Proc. R. Soc. B Biol. Sci. 285, 20172746 (2018).
    Article  Google Scholar 

    10.
    Eckert, C. G., Samis, K. E. & Lougheed, S. C. Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol. Ecol. 17, 1170–1188 (2008).
    CAS  PubMed  Article  Google Scholar 

    11.
    Attard, C. R. M. et al. Low genetic diversity in pygmy blue whales is due to climate-induced diversification rather than anthropogenic impacts. Biol. Lett. 11, 20141037 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    12.
    Ma, G., Rudolf, V. H. W. & Ma, C. Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob. Chang. Biol. 21, 1794–1808 (2015).
    ADS  PubMed  Article  Google Scholar 

    13.
    Johnson, D. W., Freiwald, J. & Bernardi, G. Genetic diversity affects the strength of population regulation in a marine fish. Ecology 97, 627–639 (2016).
    CAS  PubMed  Google Scholar 

    14.
    Coates, D. J., Byrne, M. & Moritz, C. Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front. Ecol. Evol. 6, 165 (2018).
    Article  Google Scholar 

    15.
    Willoughby, J. R. et al. The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings. Biol. Conserv. 191, 495–503 (2015).
    Article  Google Scholar 

    16.
    Blanchet, S., Prunier, J. G. & De Kort, H. Time to go bigger: emerging patterns in macrogenetics. Trends Genet. 33, 579–580 (2017).
    CAS  PubMed  Article  Google Scholar 

    17.
    Bruford, M. W., Davies, N., Dulloo, M. E., Faith, D. P. & Walters, M. In The GEO Handbook on Biodiversity Observation Networks 107–128 (Springer International Publishing, 2017).

    18.
    Hamrick, J. L. & Godt, M. J. W. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. B Biol. Sci. 351, 1291–1298 (1996).
    ADS  Article  Google Scholar 

    19.
    Cahill, A. E. & Levinton, J. S. Genetic differentiation and reduced genetic diversity at the northern range edge of two species with different dispersal modes. Mol. Ecol. 25, 515–526 (2016).
    PubMed  Article  Google Scholar 

    20.
    Gelmi-Candusso, T. A., Heymann, E. W. & Heer, K. Effects of zoochory on the spatial genetic structure of plant populations. Mol. Ecol. 26, 5896–5910 (2017).
    PubMed  Article  Google Scholar 

    21.
    Vranckx, G., Jacquemyn, H., Muys, B. & Honnay, O. Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv. Biol. 26, 228–237 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    22.
    Eo, S. H., Doyle, J. M. & DeWoody, J. A. Genetic diversity in birds is associated with body mass and habitat type. J. Zool. 283, 220–226 (2011).
    Article  Google Scholar 

    23.
    Davey, C. M., Chamberlain, D. E., Newson, S. E., Noble, D. G. & Johnston, A. Rise of the generalists: evidence for climate driven homogenization in avian communities. Glob. Ecol. Biogeogr. 21, 568–578 (2012).
    Article  Google Scholar 

    24.
    Romiguier, J. et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261–263 (2014).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    25.
    Doyle, J. M., Hacking, C. C., Willoughby, J. R., Sundaram, M. & DeWoody, J. A. Mammalian genetic diversity as a function of habitat, body size, trophic class, and conservation status. J. Mammal. 96, 564–572 (2015).
    Article  Google Scholar 

    26.
    Miller, J. E. D., Damschen, E. I., Harrison, S. P. & Grace, J. B. Landscape structure affects specialists but not generalists in naturally fragmented grasslands. Ecology 96, 3323–3331 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    27.
    Dalongeville, A., Andrello, M., Mouillot, D., Albouy, C. & Manel, S. Ecological traits shape genetic diversity patterns across the Mediterranean Sea: a quantitative review on fishes. J. Biogeogr. 43, 845–857 (2016).
    Article  Google Scholar 

    28.
    Mitton, J. B. & Lewis, W. M. Relationships between genetic variability and life history features of bony fishes. Evolution 43, 1712–1723 (1989).
    PubMed  Article  PubMed Central  Google Scholar 

    29.
    Vachon, F., Whitehead, H. & Frasier, T. R. What factors shape genetic diversity in cetaceans? Ecol. Evol. 8, 1554–1572 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    30.
    Jackson, J. M. et al. Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude. Mol. Ecol. 27, 2926–2942 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    31.
    Yannic, G. et al. Genetic diversity in caribou linked to past and future climate change. Nat. Clim. Chang. 4, 132–137 (2014).
    ADS  Article  Google Scholar 

    32.
    Lira-Noriega, A. & Manthey, J. D. Relationship of genetic diversity and niche centrality: a survey and analysis. Evolution 68, 1082–1093 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    33.
    Duncan, S. I., Crespi, E. J., Mattheus, N. M. & Rissler, L. J. History matters more when explaining genetic diversity within the context of the core-periphery hypothesis. Mol. Ecol. 24, 4323–4336 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    34.
    Garner, T. W. J., Pearman, P. B. & Angelone, S. Genetic diversity across a vertebrate species’ range: a test of the central-peripheral hypothesis. Mol. Ecol. 13, 1047–1053 (2004).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Munwez, I. et al. The change in genetic diversity down the core-edge gradient in the eastern spadefoot toad (Pelobates syriacus). Mol. Ecol. 19, 2675–2689 (2010).
    Article  CAS  Google Scholar 

    36.
    Jones, M. E., Paetkau, D., Geffen, E. & Moritz, C. Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol. Ecol. 13, 2197–2209 (2004).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    37.
    White, T. A. & Searle, J. B. Genetic diversity and population size: island populations of the common shrew, Sorex araneus. Mol. Ecol. 16, 2005–2016 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    38.
    Conord, C., Gurevitch, J. & Fady, B. Large-scale longitudinal gradients of genetic diversity: a meta-analysis across six phyla in the Mediterranean basin. Ecol. Evol. 2, 2600–2614 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    39.
    Whitlock, R. Relationships between adaptive and neutral genetic diversity and ecological structure and functioning: a meta-analysis. J. Ecol. 102, 857–872 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    40.
    García-Verdugo, C. et al. Do island plant populations really have lower genetic variation than mainland populations? Effects of selection and distribution range on genetic diversity estimates. Mol. Ecol. 24, 726–741 (2015).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    41.
    Patiño, J. et al. A roadmap for island biology: 50 fundamental questions after 50 years of The Theory of Island Biogeography. J. Biogeogr. 44, 963–983 (2017).
    Article  Google Scholar 

    42.
    Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    43.
    Schluter, D. & Pennell, M. W. Speciation gradients and the distribution of biodiversity. Nature 546, 48–55 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    44.
    Miraldo, A. et al. An Anthropocene map of genetic diversity. Sci 353, 1532–1535 (2016).
    ADS  CAS  Article  Google Scholar 

    45.
    Hirao, A. S. et al. Genetic diversity within populations of an arctic-alpine species declines with decreasing latitude across the Northern Hemisphere. J. Biogeogr. 44, 2740–2751 (2017).
    Article  Google Scholar 

    46.
    Kim, M.-S., Richardson, B. A., McDonald, G. I. & Klopfenstein, N. B. Genetic diversity and structure of western white pine (Pinus monticola) in North America: a baseline study for conservation, restoration, and addressing impacts of climate change. Tree Genetics & Genomes, 7. PLoS Genet. 1, 11–21 (2011).
    Google Scholar 

    47.
    Adams, R. I. & Hadly, E. A. Genetic diversity within vertebrate species is greater at lower latitudes. Evol. Ecol. 27, 133–143 (2013).
    Article  Google Scholar 

    48.
    Gratton, P. et al. Which latitudinal gradients for genetic diversity? Trends Ecol. Evol. 32, 724–726 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    49.
    Lumibao, C. Y., Hoban, S. M. & McLachlan, J. Ice ages leave genetic diversity ‘hotspots’ in Europe but not in Eastern North America. Ecol. Lett. 20, 1459–1468 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    50.
    Schoville, S. D. et al. Adaptive genetic variation on the landscape: methods and cases. Annu. Rev. Ecol. Evol. Syst. 43, 23–43 (2012).
    Article  Google Scholar 

    51.
    Manel, S. et al. Global determinants of freshwater and marine fish genetic diversity. Nat. Commun. 11, 1–9 (2020).
    ADS  Article  CAS  Google Scholar 

    52.
    Socolar, J. B., Gilroy, J. J., Kunin, W. E. & Edwards, D. P. How should beta-diversity inform biodiversity conservation? Trends Ecol. Evol. 31, 67–80 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    53.
    Browne, L., Ottewell, K., Sork, V. L. & Karubian, J. The relative contributions of seed and pollen dispersal to gene flow and genetic diversity in seedlings of a tropical palm. Mol. Ecol. 27, 3159–3173 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    54.
    Laughlin, D. C. & Messier, J. Fitness of multidimensional phenotypes in dynamic adaptive landscapes. Trends Ecol. Evol. 30, 487–496 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    55.
    Raffard, A., Santoul, F., Cucherousset, J. & Blanchet, S. The community and ecosystem consequences of intraspecific diversity: a meta-analysis. Biol. Rev. 94, 648–661 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    56.
    Nybom, H. & Bartish, I. V. Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect. Plant Ecol. Evol. Syst. 3, 93–114 (2000).
    Article  Google Scholar 

    57.
    Honnay, O. & Jacquemyn, H. Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv. Biol. 21, 823–831 (2007).
    PubMed  Article  PubMed Central  Google Scholar 

    58.
    Jarne, P. & Auld, J. R. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60, 1816–1824 (2006).
    PubMed  Article  PubMed Central  Google Scholar 

    59.
    Suggitt, A. J. et al. Extinction risk from climate change is reduced by microclimatic buffering. Nat. Clim. Chang. 8, 713–717 (2018).
    ADS  Article  Google Scholar 

    60.
    Lawrence, E. R. & Fraser, D. J. Latitudinal biodiversity gradients at three levels: linking species richness, population richness and genetic diversity. Glob. Ecol. Biogeogr. 29, 770–788 (2020).
    Article  Google Scholar 

    61.
    Mariette, S., Le Corre, V., Austerlitz, F. & Kremer, A. Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol. Ecol. 11, 1145–1156 (2002).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    62.
    Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J. & Sheldon, B. C. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 18, 2746–2765 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    63.
    Brown, S. C., Wigley, T. M. L., Otto-Bliesner, B. L., Rahbek, C. & Fordham, D. A. Persistent Quaternary climate refugia are hospices for biodiversity in the Anthropocene. Nat. Clim. Chang. 10, 244–248 (2020).
    ADS  Article  Google Scholar 

    64.
    Storey, J., Bass, A., Dabney, A. & Robinson, D. qvalue: Q-value estimation for false discovery rate control. R package version 2.14.1. https://doi.org/10.1111/ele.12303 (2019).

    65.
    Nowakowski, A. J. et al. Thermal biology mediates responses of amphibians and reptiles to habitat modification. Ecol. Lett. 21, 345–355 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    66.
    Stevens, V. M. et al. A comparative analysis of dispersal syndromes in terrestrial and semi-terrestrial animals. Ecol. Lett. 17, 1039–1052 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    67.
    Bilton, D. T., Freeland, J. R. & Okamura, B. Dispersal in freshwater invertebrates. Annu. Rev. Ecol. Syst. 32, 159–181 (2001).
    Article  Google Scholar 

    68.
    Kappes, H. & Haase, P. Slow, But Steady: Dispersal of Freshwater Molluscs (Springer, 2012).

    69.
    Grace, J. B. et al. Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature 529, 390–393 (2016).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    70.
    Brun, P. et al. The productivity-biodiversity relationship varies across diversity dimensions. Nat. Commun. 10, 5691 (2019).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    71.
    McGlynn, T. P., Weiser, M. D. & Dunn, R. R. More individuals but fewer species: testing the ‘more individuals hypothesis’ in a diverse tropical fauna. Biol. Lett. 6, 490–493 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    72.
    Binks, R. M., Millar, M. A. & Byrne, M. Not all rare species are the same: contrasting patterns of genetic diversity and population structure in two narrow-range endemic sedges. Biol. J. Linn. Soc. 114, 873–886 (2015).
    Article  Google Scholar 

    73.
    Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y. & Lobo, J. Genetic consequences of habitat fragmentation in plant populations: Susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    74.
    Cardillo, M. et al. Evolution: multiple causes of high extinction risk in large mammal species. Science 309, 1239–1241 (2005).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    75.
    LaManna, J. A. et al. Plant diversity increases with the strength of negative density dependence at the global scale. Science 356, 1389–1392 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    76.
    Mittelbach, G. G. A matter of time for tropical diversity. Nature 550, 51–52 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    77.
    Usinowicz, J. et al. Temporal coexistence mechanisms contribute to the latitudinal gradient in forest diversity. Nature 550, 105–108 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    78.
    Eziz, A. et al. Drought effect on plant biomass allocation: a meta-analysis. Ecol. Evol. 7, 11002–11010 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    79.
    Siepielski, A. M. et al. Precipitation drives global variation in natural selection. Science 355, 959–962 (2017).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    80.
    Martin, T. E. Age-related mortality explains life history strategies of tropical and temperate songbirds. Science 349, 966–970 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    81.
    Winemiller, K. O., Fitzgerald, D. B., Bower, L. M. & Pianka, E. R. Functional traits, convergent evolution, and periodic tables of niches. Ecol. Lett. 18, 737–751 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    82.
    Kuussaari, M. et al. Extinction debt: a challenge for biodiversity conservation. Trends Ecol. Evol. 24, 564–571 (2009).
    PubMed  Article  Google Scholar 

    83.
    Talluto, M. V., Boulangeat, I., Vissault, S., Thuiller, W. & Gravel, D. Extinction debt and colonization credit delay range shifts of eastern North American trees. Nat. Ecol. Evol. 1, 1–6 (2017).
    Article  Google Scholar 

    84.
    Cronk, Q. Plant extinctions take time: many plant species may already be functionally extinct. Science 353, 446–447 (2016).
    ADS  CAS  PubMed  Article  Google Scholar 

    85.
    Aguilar, R. et al. Habitat fragmentation reduces plant progeny quality: a global synthesis. Ecol. Lett. 22, 1163–1173 (2019).
    PubMed  Article  Google Scholar 

    86.
    González, A. V., Gómez‐Silva, V., Ramírez, M. J. & Fontúrbel, F. E. Meta‐analysis of the differential effects of habitat fragmentation and degradation on plant genetic diversity. Conserv. Biol. 34, 711–720 (2019).
    PubMed  Article  Google Scholar 

    87.
    Wood, J. L. A., Yates, M. C. & Fraser, D. J. Are heritability and selection related to population size in nature? Meta-analysis and conservation implications. Evol. Appl. 9, 640–657 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    88.
    Yates, M. C., Bowles, E. & Fraser, D. J. Small population size and low genomic diversity have no effect on fitness in experimental translocations of a wild fish. Proc. R. Soc. B Biol. Sci. 286, 20191989 (2019).
    CAS  Article  Google Scholar 

    89.
    De Kort, H., Mergeay, J., Jacquemyn, H. & Honnay, O. Transatlantic invasion routes and adaptive potential in North American populations of the invasive glossy buckthorn, Frangula alnus. Ann. Bot. 118, 1089–1099 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    90.
    Jordan, R., Hoffmann, A. A., Dillon, S. K. & Prober, S. M. Evidence of genomic adaptation to climate in Eucalyptus microcarpa: Implications for adaptive potential to projected climate change. Mol. Ecol. 26, 6002–6020 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    91.
    Wogan, G. O. U., Yuan, M. L., Mahler, D. L. & Wang, I. J. Genome-wide epigenetic isolation by environment in a widespread Anolis lizard. Mol. Ecol. 29, 40–55 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    92.
    Schmid, M. W. et al. Contribution of epigenetic variation to adaptation in Arabidopsis. Nat. Commun. 9, 4446 (2018).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    93.
    Rey, O. et al. Linking epigenetics and biological conservation: towards a conservation epigenetics perspective. Funct. Ecol. 34, 414–427 (2020).
    Article  Google Scholar 

    94.
    Mace, G. M. et al. Aiming higher to bend the curve of biodiversity loss. Nat. Sustain. 1, 448–451 (2018).
    Article  Google Scholar 

    95.
    Jetz, W. et al. Essential biodiversity variables for mapping and monitoring species populations. Nat. Ecol. Evolution 3, 539–551 (2019).
    Article  Google Scholar 

    96.
    Crandall, E. D., Taffel, J. R. & Barber, P. H. High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae). Heredity 104, 563–572 (2010).
    CAS  PubMed  Article  Google Scholar 

    97.
    Faurby, S. & Barber, P. H. Theoretical limits to the correlation between pelagic larval duration and population genetic structure. Mol. Ecol. 21, 3419–3432 (2012).
    PubMed  Article  Google Scholar 

    98.
    Álvarez-Noriega, M. et al. Global biogeography of marine dispersal potential. Nat. Ecol. Evol. 4, 1196–1203, https://doi.org/10.1038/s41559-020-1238-y (2020).
    Article  PubMed  Google Scholar 

    99.
    Mueller, T. & Fagan, W. F. Search and navigation in dynamic environments—from individual behaviors to population distributions. Oikos 117, 654–664 (2008).
    Article  Google Scholar 

    100.
    Willoughby, J. R. et al. Biome and migratory behaviour significantly influence vertebrate genetic diversity. Biol. J. Linn. Soc. 121, 446–457 (2017).
    Article  Google Scholar 

    101.
    Martin, A. E. & Fahrig, L. Habitat specialist birds disperse farther and are more migratory than habitat generalist birds. Ecology 99, 2058–2066 (2018).
    PubMed  Article  Google Scholar 

    102.
    Tellier, A. Persistent seed banking as eco‐evolutionary determinant of plant nucleotide diversity: novel population genetics insights. N. Phytol. 221, 725–730 (2019).
    CAS  Article  Google Scholar 

    103.
    Ayre, D., O’Brien, E., Ottewell, K. & Whelan, R. The accumulation of genetic diversity within a canopy-stored seed bank. Mol. Ecol. 19, 2640–2650 (2010).
    PubMed  Article  Google Scholar 

    104.
    Campbell, D. R., Brody, A. K., Price, M. V., Waser, N. M. & Aldridge, G. Is plant fitness proportional to seed set? An experiment and a spatial model. Am. Nat. 190, 818–827 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    105.
    Angeloni, F., Ouborg, N. J. & Leimu, R. Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol. Conserv. 144, 35–43 (2011).
    Article  Google Scholar 

    106.
    Nei, M., Maruyama, T. & Chakraborty, R. The Bottleneck effect and genetic variability in populations. Evolution 29, 1–10 (1975).
    PubMed  Article  Google Scholar 

    107.
    Kimura, M. The neutral theory of molecular evolution (Cambridge University Press: Cambridge [Cambridgeshire], 1983).

    108.
    Nagylaki, T. The effective size of a subdivided population. Genetics 149, 1599–1604 (1997).
    Google Scholar 

    109.
    Poirier, M.-A., Coltman, D. W., Pelletier, F., Jorgenson, J. & Festa-Bianchet, M. Genetic decline, restoration and rescue of an isolated ungulate population. Evol. Appl. 12, 1318–1328 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    110.
    Dures, S. G. et al. A century of decline: loss of genetic diversity in a southern African lion-conservation stronghold. Divers. Distrib. 25, 870–879 (2019).
    Article  Google Scholar 

    111.
    Nakagawa, S. & Cuthill, I. C. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82, 591–605 (2007).
    PubMed  Article  PubMed Central  Google Scholar 

    112.
    Burnham, K. P. & Anderson, D. R. In Sociological Methods & Research 33, (Sage PublicationsSage CA, Thousand Oaks, 2002). More