More stories

  • in

    Allelochemical run-off from the invasive terrestrial plant Impatiens glandulifera decreases defensibility in Daphnia

    Holt, R. D. Predation, apparent competition, and the structure of prey communities. Theor. Popul. Biol. 12, 197–229 (1977).Article 
    CAS 

    Google Scholar 
    Dugatkin, L. A. & Godin, J. G. J. Prey approaching predators: A cost-benefit perspective. Ann. Zool. Fennici 29, 233–252 (1992).
    Google Scholar 
    Portalier, S. M. J., Fussmann, G. F., Loreau, M. & Cherif, M. The mechanics of predator–prey interactions: First principles of physics predict predator–prey size ratios. Funct. Ecol. 33, 323–334 (2019).Article 

    Google Scholar 
    Achrai, B., Bar-On, B. & Wagner, H. D. Biological armors under impact—effect of keratin coating, and synthetic bio-inspired analogues. Bioinsp. Biomim. 10, 016009 (2015).Article 
    CAS 

    Google Scholar 
    Stankowich, T. & Campbell, L. A. Living in the danger zone: Exposure to predators and the evolution of spines and body armor in mammals. Evolution 70, 1501–1511 (2016).Article 

    Google Scholar 
    Tollrian, R. & Harvell, C. D. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65, 323–340 (1990).Article 

    Google Scholar 
    Nordlund, D. A. & Lewis, W. J. Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J. Chem. Ecol. 2, 211–220 (1976).Article 

    Google Scholar 
    Poulin, R. X. et al. Chemical encoding of risk perception and predator detection among estuarine invertebrates. Proc. Natl. Acad. Sci. USA 115, 662–667 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Tollrian, R. & Dodson, S. I. Inducible defenses in Cladocera: Constraints, costs, and multipredator environments. Ecol. Evol. Inducible Defenses 177, 177–202 (1999).Article 

    Google Scholar 
    Von Elert, E. & Loose, C. J. Predator-induced diel vertical migration in Daphnia: Enrichment and preliminary chemical characterization of a kairomone exuded by fish. J. Chem. Ecol. 22, 885–895 (1996).Article 

    Google Scholar 
    Barry, M. J. Effects of endosulfan on Chaoborus-induced life-history shifts and morphological defenses in Daphnia pulex. J. Plankton Res. 22, 1705–1718 (2000).Article 
    ADS 
    CAS 

    Google Scholar 
    Riessen, H. P. & Gilbert, J. J. Divergent developmental patterns of induced morphological defenses in rotifers and Daphnia: Ecological and evolutionary context. Limnol. Oceanogr. 64, 541–557 (2019).Article 
    ADS 

    Google Scholar 
    Sperfeld, E., Nilssen, J. P., Rinehart, S., Schwenk, K. & Hessen, D. O. Ecology of predator-induced morphological defense traits in Daphnia longispina (Cladocera, Arthropoda). Oecologia 192, 687–698 (2020).Article 
    ADS 

    Google Scholar 
    Tollrian, R. Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: Morphological effects of Chaoborus kairomone concentration and their quantification. J. Plankton Res. 15, 1309–1318 (1993).Article 

    Google Scholar 
    Laforsch, C. & Tollrian, R. Inducible defenses in multipredator environments: Cyclomorphosis in Daphnia cucullata. Ecology 85, 2302–2311 (2004).Article 

    Google Scholar 
    Petrusek, A., Tollrian, R., Schwenk, K., Haas, A. & Laforsch, C. A ‘crown of thorns’ is an inducible defense that protects Daphnia against an ancient predator. Proc. Natl. Acad. Sci. USA 106, 2248–2252 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Engel, K. & Tollrian, R. Inducible defences as key adaptations for the successful invasion of Daphnia lumholtzi in North America?. Proc. R. Soc. B Biol. Sci. 276, 1865–1873 (2009).Article 

    Google Scholar 
    Barry, M. J. & Bayly, I. A. E. Further studies on predator induction of crests in australian Daphnia and the effects of crests on predation. Mar. Freshw. Res. 36, 519–535 (1985).
    Google Scholar 
    Rabus, M. & Laforsch, C. Growing large and bulky in the presence of the enemy: Daphnia magna gradually switches the mode of inducible morphological defences. Funct. Ecol. 25, 1137–1143 (2011).Article 

    Google Scholar 
    Herzog, Q. & Laforsch, C. Modality matters for the expression of inducible defenses: Introducing a concept of predator modality. BMC Biol. 11, 113 (2013).Article 

    Google Scholar 
    Riessen, H. P. et al. Changes in water chemistry can disable plankton prey defenses. Proc. Natl. Acad. Sci. USA 109, 15377–15382 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Tollrian, R., Duggen, S., Weiss, L. C., Laforsch, C. & Kopp, M. Density-dependent adjustment of inducible defenses. Sci. Rep. 5, 12736 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Weiss, L. C. et al. Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia. Curr. Biol. 28, 327-332.e3 (2018).Article 
    CAS 

    Google Scholar 
    Hanazato, T. Pesticide effects on freshwater zooplankton: An ecological perspective. Environ. Pollut. 112, 1–10 (2001).Article 
    CAS 

    Google Scholar 
    Coors, A. & DeMeester, L. Erratum: Synergistic, antagonistic and additive effects of multiple stressors: Predation threat, parasitism and pesticide exposure in Daphnia magna. J. Appl. Ecol. 46, 1138 (2009).
    Google Scholar 
    Schriever, C. A., von der Ohe, P. C. & Liess, M. Estimating pesticide runoff in small streams. Chemosphere 68, 2161–2171 (2007).Article 
    ADS 
    CAS 

    Google Scholar 
    Lobstein, A. et al. Quantitative determination of naphthoquinones of Impatiens species. Phytochem. Anal. 12, 202–205 (2001).Article 
    CAS 

    Google Scholar 
    Kisielius, V. et al. The invasive butterbur contaminates stream and seepage water in groundwater wells with toxic pyrrolizidine alkaloids. Sci. Rep. 10, 19784 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Yoneyama, K. & Natsume, M. 4.13 Allelochemicals for Plant—Plant and Plant—Microbe Interactions. Interactions (Elsevier Inc., 2010).Griffiths, M. R., Strobel, B. W., Hama, J. R. & Cedergreen, N. Toxicity and risk of plant-produced alkaloids to Daphnia magna. Environ. Sci. Eur. 33, 10 (2021).Article 
    CAS 

    Google Scholar 
    Callaway, R. M. & Ridenour, W. M. Novel weapons: Invasive success and the evolution of increased competitive ability. Front. Ecol. Environ. 2, 436–443 (2004).Article 

    Google Scholar 
    Beerling, D. J. & Perrins, J. M. Impatiens glandulifera Royle (Impatiens Roylei Walp.). J. Ecol. 81, 367–382 (1993).Article 

    Google Scholar 
    Roy, B., Popay, A.I., Champion, P.D., James, T.K. & Rahman, A. An Illustrated Guide to Common Weeds of New Zealand. 2nd Edn. (New Zealand Plant Protection Society, 2004). Ruckli, R., Hesse, K., Glauser, G., Rusterholz, H. P. & Baur, B. Inhibitory potential of naphthoquinones leached from leaves and exuded from roots of the invasive plant Impatiens glandulifera. J. Chem. Ecol. 40, 371–378 (2014).Article 
    CAS 

    Google Scholar 
    Gruntman, M., Pehl, A. K., Joshi, S. & Tielbörger, K. Competitive dominance of the invasive plant Impatiens glandulifera: Using competitive effect and response with a vigorous neighbour. Biol. Invasions 16, 141–151 (2014).Article 

    Google Scholar 
    Bieberich, J. et al. Species- and developmental stage-specific effects of allelopathy and competition of invasive Impatiens glandulifera on cooccurring plants. PLoS ONE 13, e0205843 (2018).Article 

    Google Scholar 
    Wright, D. A., Dawson, R., Cutler, S. J., Cutler, H. G. & Orano-Dawson, C. E. Screening of natural product biocides for control of non-indigenous species. Environ. Technol. 28, 309–319 (2007).Article 
    CAS 

    Google Scholar 
    Kayashima, T., Mori, M., Yoshida, H., Mizushina, Y. & Matsubara, K. 1,4-naphthoquinone is a potent inhibitor of human cancer cell growth and angiogenesis. Cancer Lett. 278, 34–40 (2009).Article 
    CAS 

    Google Scholar 
    Jentzsch, J. et al. New antiparasitic bis-naphthoquinone derivatives. Chem. Biodivers. 17, e1900597 (2020).Article 
    CAS 

    Google Scholar 
    Mitchell, M. J., Brescia, A. I., Smith, S. L. & Morgan, E. D. Effects of the compounds 2-methoxynaphthoquinone, 2-propoxynaphthoquinone, and 2-isopropoxynaphthoquinone on ecdysone 20-monooxygenase activity. Arch. Insect Biochem. Physiol. 66, 45–52 (2007).Article 
    CAS 

    Google Scholar 
    Westfall, B. A., Russell, R. L. & Auyong, T. K. Depressant agent from walnut hulls. Science 134, 1617 (1961).Article 
    ADS 
    CAS 

    Google Scholar 
    Diller, J. G. P. et al. The Beauty is a beast: Does leachate from the invasive terrestrial plant Impatiens glandulifera affect aquatic food webs?. Ecol. Evol. 12, e8781 (2022).Article 

    Google Scholar 
    Elendt, B. P. Selenium deficiency in Crustacea—an ultrastructural approach to antennal damage in Daphnia magna Straus. Protoplasma 154, 25–33 (1990).Article 
    CAS 

    Google Scholar 
    Ebert, D. The trade-off between offspring size and number in Daphnia magna: The influence of genetic, environmental and maternal effects. Arch. Fur Hydrobiol. 90, 453–473 (1993).
    Google Scholar 
    Trotter, B., Ramsperger, A. F. R. M., Raab, P., Haberstroh, J. & Laforsch, C. Plastic waste interferes with chemical communication in aquatic ecosystems. Sci. Rep. 9, 5889 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Laforsch, C., Beccara, L. & Tollrian, R. Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnol. Oceanogr. 51, 1466–1472 (2006).Article 
    ADS 

    Google Scholar 
    Miner, B. E., de Meester, L., Pfrender, M. E., Lampert, W. & Hairston, N. G. Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proc. R. Soc. B Biol. Sci. 279, 1873–1882 (2012).Article 

    Google Scholar 
    Altshuler, I. et al. An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integr. Comp. Biol. 51, 623–633 (2011).Article 
    CAS 

    Google Scholar 
    Diel, P., Kiene, M., Martin-Creuzburg, D. & Laforsch, C. Knowing the enemy: Inducible defences in freshwater zooplankton. Diversity 12, 147 (2020).Article 
    CAS 

    Google Scholar 
    Pestana, J. L. T., Loureiro, S., Baird, D. J. & Soares, A. M. V. M. Pesticide exposure and inducible antipredator responses in the zooplankton grazer, Daphnia magna Straus. Chemosphere 78, 241–248 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Grant, J. W. G. & Bayly, I. A. E. Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol. Oceanogr. 26, 201–218 (1981).Article 
    ADS 

    Google Scholar 
    Dodson, S. I. Zooplankton competition and predation: An experimental test of the size-efficiency hypothesis. Ecology 55, 605–613 (1974).Article 

    Google Scholar 
    Klotz, L. O., Hou, X. & Jacob, C. 1,4-naphthoquinones: From oxidative damage to cellular and inter-cellular signaling. Molecules 19, 14902–14918 (2014).Article 

    Google Scholar 
    Subramoniam, T. Crustacean ecdysteriods in reproduction and embryogenesis. Comp. Biochem. C Physiol. Pharmacol. Toxicol. Endocrinol. 125, 135–156 (2000).Article 
    CAS 

    Google Scholar 
    De Coen, W. M. & Janssen, C. R. The missing biomarker link: Relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ. Toxicol. Chem. 22, 1632–1641 (2003).Article 

    Google Scholar 
    Palma, P. et al. Effects of atrazine and endosulfan sulphate on the ecdysteroid system of Daphnia magna. Chemosphere 74, 676–681 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Mount, D. I. & Norberg, T. J. A seven-day life cycle Cladoceran toxicity test. Environ. Toxicol. Chem. 3, 425–434 (1984).Article 
    CAS 

    Google Scholar 
    Elnabarawy, M. T., Welter, A. N. & Robideau, R. R. Relative sensitivity of three daphnid species to selected organic and inorganic chemicals. Environ. Toxicol. Chem. 5, 393–398 (1986).Article 
    CAS 

    Google Scholar 
    Jaikumar, G., Baas, J., Brun, N. R., Vijver, M. G. & Bosker, T. Acute sensitivity of three Cladoceran species to different types of microplastics in combination with thermal stress. Environ. Pollut. 239, 733–740 (2018).Article 
    CAS 

    Google Scholar 
    Gama-Flores, J. L., Salas, M. E. H., Sarma, S. S. S. & Nandini, S. Demographic responses of Cladocerans (Cladocera) in relation to different concentrations of humic substances. J. Environ. Sci. Heal. Part A Toxic/Hazardous Subst. Environ. Eng. 54, 1311–1317 (2019).CAS 

    Google Scholar 
    Cohen, J. E., Pimm, S. L., Yodzis, P. & Saldana, J. Body sizes of animal predators and animal prey in food webs. J. Anim. Ecol. 62, 67–78 (1993).Article 

    Google Scholar 
    Hunt, R. J. & Swift, M. Predation by larval damselflies on Cladocerans. J. Freshw. Ecol. 25, 345–351 (2010).Article 

    Google Scholar 
    Riessen, H. P. & Trevett-Smith, J. B. Turning inducible defenses on and off: Adaptive responses of Daphnia to a gape-limited predator. Ecology 90, 3455–3469 (2009).Article 

    Google Scholar 
    Pijanowska, J. Cyclomorphosis in Daphnia: An adaptation to avoid invertebrate predation. Hydrobiologia 198, 41–50 (1990).Article 

    Google Scholar 
    Gu, L. et al. Coping with antagonistic predation risks: Predator-dependent unique responses are dominant in Ceriodaphnia cornuta. Mol. Ecol. 31, 3951–3962 (2022).Article 
    CAS 

    Google Scholar 
    Jeziorski, A. et al. The jellification of north temperate lakes. Proc. R. Soc. B Biol. Sci. 2014, 282 (2014).
    Google Scholar 
    Ponti, B., Piscia, R., Bettinetti, R. & Manca, M. Long-term adaptation of Daphnia to toxic environment in Lake Orta: The effects of short-term exposure to copper and acidification. J. Limnol. 69, 217–224 (2010).Article 

    Google Scholar 
    Wright, D. A., Mitchelmore, C. L., Dawson, R. & Cutler, H. G. The influence of water quality on the toxicity and degradation of juglone (5-hydroxy 1,4-naphthoquinone). Environ. Technol. 28, 1091–1101 (2007).Article 
    CAS 

    Google Scholar  More

  • in

    Comparing avian species richness estimates from structured and semi-structured citizen science data

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Schumaker, N. H. Using landscape indices to predict habitat connectivity. Ecology 77, 1210–1225 (1996).Article 

    Google Scholar 
    Pacifici, M. et al. Assessing species vulnerability to climate change. Nat. Clim. Chang. 5, 215–224 (2015).Article 
    ADS 

    Google Scholar 
    Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).Article 

    Google Scholar 
    Clavero, M., Brotons, L., Pons, P. & Sol, D. Prominent role of invasive species in avian biodiversity loss. Biol. Conserv. 142, 2043–2049 (2009).Article 

    Google Scholar 
    Soroye, P., Ahmed, N. & Kerr, J. T. Opportunistic citizen science data transform understanding of species distributions, phenology, and diversity gradients for global change research. Glob. Change Biol. 24, 5281–5291 (2018).Article 
    ADS 

    Google Scholar 
    Gotelli, N. J. & Colwell, R. K. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391 (2001).Article 

    Google Scholar 
    Dickinson, J. L., Zuckerberg, B. & Bonter, D. N. Citizen science as an ecological research tool: Challenges and benefits. Annu. Rev. Ecol. Evol. Syst. 41, 149–172 (2010).Article 

    Google Scholar 
    Kelling, S. et al. Using semistructured surveys to improve citizen science data for monitoring biodiversity. Bioscience 69, 170–179 (2019).Article 

    Google Scholar 
    Steen, V. A., Elphick, C. S. & Tingley, M. W. An evaluation of stringent filtering to improve species distribution models from citizen science data. Divers. Distrib. 25, 1857–1869 (2019).Article 

    Google Scholar 
    Crall, A. W. et al. Assessing citizen science data quality: An invasive species case study. Conserv. Lett. 4, 433–442 (2011).Article 

    Google Scholar 
    Bird, T. J. et al. Statistical solutions for error and bias in global citizen science datasets. Biol. Conserv. 173, 144–154 (2014).Article 

    Google Scholar 
    MacKenzie, D. I. et al. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83, 2248–2255 (2002).Article 

    Google Scholar 
    Kellner, K. F. & Swihart, R. K. Accounting for imperfect detection in ecology: A quantitative review. PLoS ONE 9(10), E111436 (2014).Article 
    ADS 

    Google Scholar 
    Weisshaupt, N., Lehikoinen, A., Mäkinen, T. & Koistinen, J. Challenges and benefits of using unstructured citizen science data to estimate seasonal timing of bird migration across large scales. PLoS ONE 16, e0246572 (2021).Article 
    CAS 

    Google Scholar 
    Kéry, M. & Schmid, H. Estimating species richness: Calibrating a large avian monitoring programme. J. Appl. Ecol. 43, 101–110 (2006).Article 

    Google Scholar 
    Chao, A. & Chiu, C. H. Species richness: Estimation and comparison 1–26 (Wiley StatsRef: Statistics Reference Online, 2014).
    Google Scholar 
    Walther, B. A. & Moore, J. L. The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28, 815–829 (2005).Article 

    Google Scholar 
    Chao, A. & Lee, S.-M. Estimating the number of classes via sample coverage. J. Am. Stat. Assoc. 87, 210–217 (1992).Article 
    MATH 

    Google Scholar 
    Walther, B. A. & Morand, S. Comparative performance of species richness estimation methods. Parasitology 116, 395–405 (1998).Article 

    Google Scholar 
    Walther, B. A. & Martin, J. L. Species richness estimation of bird communities: How to control for sampling effort?. Ibis 143, 413–419 (2001).Article 

    Google Scholar 
    Walther, B. A., Cotgreave, P., Price, R., Gregory, R. & Clayton, D. H. Sampling effort and parasite species richness. Parasitol. Today 11, 306–310 (1995).Article 
    CAS 

    Google Scholar 
    Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 345, 101–118 (1994).Article 
    ADS 
    CAS 

    Google Scholar 
    Bean, W. T., Stafford, R. & Brashares, J. S. The effects of small sample size and sample bias on threshold selection and accuracy assessment of species distribution models. Ecography 35, 250–258 (2012).Article 

    Google Scholar 
    Flather, C. Fitting species–accumulation functions and assessing regional land use impacts on avian diversity. J. Biogeogr. 23, 155–168 (1996).Article 

    Google Scholar 
    White, P. E. et al. A comparison of the species–time relationship across ecosystems and taxonomic groups. Oikos 112, 185–195 (2006).Article 

    Google Scholar 
    McGlinn, D. J. & Palmer, M. W. Modeling the sampling effect in the species–time–area relationship. Ecology 90, 836–846 (2009).Article 

    Google Scholar 
    Isaac, N. J. et al. Statistics for citizen science: Extracting signals of change from noisy ecological data. Method Ecol. Evol. 5, 1052–1060 (2014).Article 

    Google Scholar 
    Ding, T. et al. The 2020 CWBF checklist of the birds of Taiwan (Chinese Wild Bird Federation, 2020).
    Google Scholar 
    Lin, M.-M. et al. Bird records database of a Taiwanese non-governmental organization, the Chinese wild bird federation, from 1972 to 2017. TW. J. Biodivers. 21, 83–101 (2019).
    Google Scholar 
    Dokter, A. M., Desmet, P., Van Hoey, S. (2022) bioRad: Biological analysis and visualization of weather radar data: v0. 6.0Strimas-Mackey, M. et al. (2020) Best practices for using eBird Data. Version 1.0. Cornell Laboratory of Ornithology, Ithaca, New York, 10.5281/zenodo.3620739Robinson, O. J. et al. Using citizen science data in integrated population models to inform conservation. Biol. Conserv. 227, 361–368 (2018).Article 

    Google Scholar 
    Callaghan, C. T., Martin, J. M., Major, R. E. & Kingsford, R. T. Avian monitoring–comparing structured and unstructured citizen science. Wildl. Res. 45, 176–184 (2018).Article 

    Google Scholar 
    Robinson, W. D., Hallman, T. A. & Hutchinson, R. A. Benchmark bird surveys help quantify counting accuracy in a citizen-science database. Front. Ecol. Evol. 9, 568278 (2021).Article 

    Google Scholar 
    Neate-Clegg, M. H., Horns, J. J., Adler, F. R., Aytekin, M. Ç. K. & Şekercioğlu, Ç. H. Monitoring the world’s bird populations with community science data. Biol. Conserv. 248, 108653 (2020).Article 

    Google Scholar 
    Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat 1, 265–270 (1984).
    Google Scholar 
    Hsieh, T., Ma, K. & Chao, A. iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).Article 

    Google Scholar 
    Team, R. C. (2013).R: A language and environment for statistical computing.James, G., Witten, D., Hastie, T. & Tibshirani, R. An Introduction to Statistical Learning Vol. 112 (Springer, 2013).Book 
    MATH 

    Google Scholar 
    Magurran, A. E. & McGill, B. J. Biological diversity: Frontiers in measurement and assessment (OUP Oxford, 2010).
    Google Scholar 
    Spiess, A.-N. (2018) Package ‘propagate’RC Team, C Worldwide. The R stats package (R Foundation for Statistical Computing, 2002).
    Google Scholar 
    Guralnick, R. & Van Cleve, J. Strengths and weaknesses of museum and national survey data sets for predicting regional species richness: Comparative and combined approaches. Divers. Distrib. 11, 349–359 (2005).Article 

    Google Scholar 
    Dar, T. A. et al. Bird community structure in Phakot and Pathri Rao watershed areas in Uttarakhand. India. Int. J. Environ. Sci. 34, 193–205 (2008).
    Google Scholar 
    Azevedo, G. H. et al. Effectiveness of sampling methods and further sampling for accessing spider diversity: A case study in a Brazilian Atlantic rainforest fragment. Insect. Conserv. Divers. 7, 381–391 (2014).Article 

    Google Scholar 
    Bonter, D. N. & Cooper, C. B. Data validation in citizen science: A case study from project feederwatch. Front. Ecol. Environ. 10, 305–307 (2012).Article 

    Google Scholar 
    Gómez-Martínez, C. et al. Forest fragmentation modifies the composition of bumblebee communities and modulates their trophic and competitive interactions for pollination. Sci. Rep. 10, 1–15 (2020).Article 

    Google Scholar 
    Sullivan, B. L. et al. eBird: A citizen-based bird observation network in the biological sciences. Biol. Conserv. 142, 2282–2292 (2009).Article 

    Google Scholar 
    Newson, S. E., Woodburn, R. J., Noble, D. G., Baillie, S. R. & Gregory, R. D. Evaluating the breeding bird survey for producing national population size and density estimates. Bird Study 52, 42–54 (2005).Article 

    Google Scholar 
    Robbins, C. S. Effect of time of day on bird activity. Stud. Avian Biol. 6, 275–286 (1981).
    Google Scholar 
    Farmer, R. G., Leonard, M. L. & Horn, A. G. Observer effects and avian-call-count survey quality: Rare-species biases and overconfidence. Auk 129, 76–86 (2012).Article 

    Google Scholar 
    Gardiner, M. M. et al. Lessons from lady beetles: Accuracy of monitoring data from US and UK citizen-science programs. Front. Ecol. Environ. 10, 471–476 (2012).Article 

    Google Scholar 
    Swanson, A., Kosmala, M., Lintott, C. & Packer, C. A generalized approach for producing, quantifying, and validating citizen science data from wildlife images. Conserv. Biol. 30, 520–531 (2016).Article 

    Google Scholar 
    Ratnieks, F. L. et al. Data reliability in citizen science: Learning curve and the effects of training method, volunteer background and experience on identification accuracy of insects visiting ivy flowers. Methods Ecol. Evol. 7, 1226–1235 (2016).Article 

    Google Scholar 
    Lopez, L. C. S., de Aguiar Fracasso, M. P., Mesquita, D. O., Palma, A. R. T. & Riul, P. The relationship between percentage of singletons and sampling effort: A new approach to reduce the bias of richness estimates. Ecol. Indicators 14, 164–169 (2012).Article 

    Google Scholar 
    Bunge, J. & Fitzpatrick, M. Estimating the number of species: A review. J. Am. Stat. Assoc. 88, 364–373 (1993).
    Google Scholar 
    SoberónM, J. & LlorenteB, J. The use of species accumulation functions for the prediction of species richness. Conserv. Biol. 7, 480–488 (1993).Article 

    Google Scholar 
    Magurran, A. E. Species abundance distributions over time. Ecol. Lett. 10, 347–354 (2007).Article 

    Google Scholar 
    de Caprariis, P., Lindemann, R. & Haimes, R. A relationship between sample size and accuracy of species richness predictions. J. Int. Assoc. Math. Geol. 13, 351–355 (1981).Article 

    Google Scholar 
    Klemann-Junior, L., Villegas Vallejos, M. A., Scherer-Neto, P. & Vitule, J. R. S. Traditional scientific data vs. uncoordinated citizen science effort: A review of the current status and comparison of data on avifauna in Southern Brazil. PLoS ONE 12, e0188819. https://doi.org/10.1371/journal.pone.0188819 (2017).Article 
    CAS 

    Google Scholar 
    Tulloch, A. I. & Szabo, J. K. A behavioural ecology approach to understand volunteer surveying for citizen science datasets. Emu 112, 313–325 (2012).Article 

    Google Scholar 
    Boakes, E. H. et al. Distorted views of biodiversity: Spatial and temporal bias in species occurrence data. PLoS Biol. 8, e1000385 (2010).Article 

    Google Scholar 
    Kamp, J. et al. Unstructured citizen science data fail to detect long-term population declines of common birds in Denmark. Divers. Distrib. 22, 1024–1035. https://doi.org/10.1111/ddi.12463 (2016).Article 

    Google Scholar 
    Lin, Y.-P. et al. Uncertainty analysis of crowd-sourced and professionally collected field data used in species distribution models of Taiwanese moths. Biol. Conserv. 181, 102–110 (2015).Article 

    Google Scholar 
    Fletcher, R. J. Jr. et al. A practical guide for combining data to model species distributions. Ecology 100, e02710 (2019).Article 

    Google Scholar  More

  • in

    Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification

    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.Article 
    CAS 

    Google Scholar 
    Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, Mueller ND, et al. Climate Change and Global Food Systems: Potential Impacts on Food Security and Undernutrition. Annu Rev Pub Health. 2017;38:259–77.Article 

    Google Scholar 
    Brown AR, Lilley M, Shutler J, Lowe C, Artioli Y, Torres R, et al. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev Aquac. 2020;12:1663–88.
    Google Scholar 
    Bates SS, Hubbard KA, Lundholm N, Montresor M, Leaw CP. Pseudo-nitzschia, Nitzschia, and domoic acid: New research since 2011. Harmful Algae. 2018;79:3–43.Article 

    Google Scholar 
    Silver MW, Bargu S, Coale SL. Toxic diatoms and domoic acid in natural and iron enriched waters of the oceanic pacific. Proc Natl Acad Sci. 2010;107:20762–67.Article 
    CAS 

    Google Scholar 
    Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD. Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proc Natl Acad Sci. 2010;107:5887–92.Article 
    CAS 

    Google Scholar 
    Hallegraeff G, Enevoldsen H, Zingone A. Global harmful algal bloom status reporting. Harmful Algae. 2021;102:101992.Article 

    Google Scholar 
    McKibben SM, Peterson W, Wood AM, Trainer VL, Hunter M, White AE. Climatic regulation of the neurotoxin domoic acid. Proc Natl Acad Sci. 2017;114:239–44.Article 
    CAS 

    Google Scholar 
    Clark S, Hubbard KA, Ralston DK, McGillicuddy DJ, Stocke C, Alexander MA, et al. Projected effects of climate change on Pseudo-nitzschia bloom dynamics in the Gulf of Maine. J Mar Syst. 2022;230:103737.Article 

    Google Scholar 
    Trainer VL, Kudela RM, Hunter MV, Adams NG, McCabe RM. Climate extreme seeds a new domoic ccid hotspot on the US West Coast. Front Clim. 2020;2:1–11.Article 

    Google Scholar 
    Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW, Gravenor MB. Changes in marine dinoflagellate and diatom abundance under climate change. Nat Clim Change. 2012;2:271–75.Article 

    Google Scholar 
    Sun J, Hutchins DA, Feng Y, Seubert EL, Caron DA, Fu FX. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol Oceanogr. 2011;56:829–40.Article 
    CAS 

    Google Scholar 
    Zhu Z, Qu P, Fu F, Tennenbaum N, Tatters AO, Hutchins DA. Understanding the blob bloom: warming increases toxicity and abundance of the harmful bloom diatom Pseudo-nitzschia in California coastal waters. Harmful Algae. 2017;67:36–43.Article 
    CAS 

    Google Scholar 
    Radan RL, Cochlan WP. Differential toxin response of Pseudo-nitzschia multiseries as a function of nitrogen speciation in batch and continuous cultures, and during a natural assemblage experiment. Harmful Algae. 2018;73:12–29.Article 
    CAS 

    Google Scholar 
    Wingert CJ, Cochlan WP. Effects of ocean acidification on the growth, photosynthetic performance, and domoic acid production of the diatom Pseudo-nitzschia australis from the California Current System. Harmful Algae. 2021;107:102030.Article 
    CAS 

    Google Scholar 
    Auro ME, Cochlan WP. Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima complex: P. cuspidate and P. fryxelliana. J Phycol. 2013;49:156–69.Article 
    CAS 

    Google Scholar 
    Lundholm N, Clarke A, Ellegaard M. A 100-year record of changing Pseudo-nitzschia species in a sill-fjord in Denmark related to nitrogen loading and temperature. Harmful Algae. 2010;9:449–57.Article 

    Google Scholar 
    Ryan JP, Kudela RM, Birch JM, Blum M, Bower HA, Chavez FP, et al. Causality of an extreme harmful algal bloom in Monterey Bay, California, during the 2014–2016 northeast Pacific warm anomaly. Geophys Res Lett. 2017;44:5571–79.Article 

    Google Scholar 
    McCabe RM, Hickey BM, Kudela RM, Lefebvre KA, Adams NG, Bill BD, et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett. 2016;43:10,366–76.Article 

    Google Scholar 
    Tatters AO, Fu FX, Hutchins DA. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS One. 2012;7:e32116.Article 
    CAS 

    Google Scholar 
    Lundholm N, Hansen PJ, Kotaki Y. Effect of pH on growth and domoic acid production by potentially toxic diatoms of the genera Pseudo-nitzschia and Nitzschia. Mar Ecol Prog Ser. 2004;273:1–15.Article 
    CAS 

    Google Scholar 
    Trimborn S, Lundholm N, Thoms S, Richter KW, Krock B, Hansen P, et al. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiol Plant. 2008;133:92–105.Article 
    CAS 

    Google Scholar 
    Brunson JK, McKinnie SMK, Chekan JR, McCrow JP, Miles ZD, Bertrand EM, et al. Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science. 2018;361:1356–58.Article 
    CAS 

    Google Scholar 
    Boissonneault KR, Henningsen BM, Bates SS, Robertson DL, Milton S, Pelletier J, et al. Gene expression studies for the analysis of domoic acid production in the marine diatom Pseudo-nitzschia multiseries. BMC Mole Biol. 2013;14:1–19.
    Google Scholar 
    Pierrot DE, Lewis E, Wallace DWR MS Excel program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of. Energy, Oak Ridge, TN. 2006; Retrieved from https://doi.org/10.3334/CDIAC/otg.CO2SYS_XLS_CDIAC105a.Brzezinski MA, Nelson DM. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Res Pt I Oceanogr Res Papers. 1995;42:1215–37.Article 
    CAS 

    Google Scholar 
    Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TBH. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Change. 2014;4:1024–30.Article 

    Google Scholar 
    Schaum CE, Barton S, Bestion E, Buckling A, Garcia-Carreras B, Lopez P, et al. Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol. 2017;1:0094.Article 

    Google Scholar 
    Wang Z, Maucher-Fuquay J, Fire SE, Mikulski CM, Haynes B, Doucette GJ, et al. Optimization of solid-phase extraction and liquid chromatography–tandem mass spectrometry for the determination of domoic acid in seawater, phytoplankton, and mammalian fluids and tissues. Anal Chim Acta. 2012;715:71–9.Article 
    CAS 

    Google Scholar 
    Brandenburg KM, Velthuis M, Van de Waal DB. Meta-analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels. Glob Change Biol. 2019;25:2607–18.Article 

    Google Scholar 
    Wohlrab S, John U, Klemm K, Rberlein T, Grivogiannis AMF, Krock B, et al. Ocean acidification increases domoic acid contents during a spring to summer succession of coastal phytoplankton. Harmful Algae. 2020;92:101697.Article 
    CAS 

    Google Scholar 
    Zhong J, Guo Y, Liang Z, Huang Q, Lu H, Pan J, et al. Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs. Sci Total Environ. 2021;771:145167.Article 
    CAS 

    Google Scholar 
    Trainer VL, Bates SS, Lundholm N, Thessen AE, Cochlan WP, Adams NG, et al. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae. 2012;14:271–300.Article 

    Google Scholar 
    Zhu Z, Qu P, Gale J, Fu F, Hutchins DA. Individual and interactive effects of warming and CO2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica, two dominant phytoplankton from the Ross Sea, Antarctica. Biogeosciences. 2017;14:5281–95.Article 
    CAS 

    Google Scholar 
    Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR, et al. Irreversibly increased N2 fixation in Trichodesmium experimentally adapted to high CO2. Nat Commun. 2015;6:8155.Article 

    Google Scholar 
    Walworth NG, Lee MD, Fu FX, Hutchins DA, Webb EA. Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium. P Natl Acad Sci. 2016;113:E7367–74.Article 
    CAS 

    Google Scholar 
    Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun. 2018;9:1719.Article 

    Google Scholar 
    Hutchins DA, Capone DG. The ocean nitrogen cycle: New developments and global change. Nat Rev Microbiol. 2022;20:401–14.Article 
    CAS 

    Google Scholar 
    Xu D, Tong S, Wang B, Zhang X, Wang W, Zhang X, et al. Ocean acidification stimulation of phytoplankton growth depends on the extent of departure from the optimal growth temperature. Mar Pollut Bull. 2022;177:113510.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Sefbom J, Schaum E, Dyhrman ST, Godhe A Studying the acclimation and adaptation of HAB species to changing environmental conditions. In: Wells ML, et al. (eds.). GlobalHAB. 2021. Guidelines for the Study of Climate Change Effects on HABs. Paris: UNESCO-IOC/SCOR, 2021. pp 64–78.Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.Article 
    CAS 

    Google Scholar 
    Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, et al. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol. 2012;2:1195–207.Article 

    Google Scholar 
    Tatters AO, Schnetzer A, Fu F, Lie AY, Caron DA, Hutchins DA. Short‐versus long‐term responses to changing CO2 in a coastal dinoflagellate bloom: Implications for interspecific competitive interactions and community structure. Evolution. 2013;67:1879–91.Article 

    Google Scholar 
    Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. P Roy Soc B-Biol Sci. 2014;281:20141486.
    Google Scholar 
    Moran XAG, Lopez-Urrutia Á, Calvo-Díaz A, Li WKW. Increasing importance of small phytoplankton in a warmer ocean. Glob Change Biol. 2010;16:1137–44.Article 

    Google Scholar 
    Thomas MK, Kremer CT, Klausmeier CA, Litchman EA. Global pattern of thermal adaptation in marine phytoplankton. Science. 2012;338:1085–88.Article 
    CAS 

    Google Scholar 
    Toseland ADSJ, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change. 2013;3:979–84.Article 
    CAS 

    Google Scholar 
    Collins S. Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution. Evol Biol. 2011;38:3–14.Article 

    Google Scholar 
    Qu PP, Fu F, Wang XW, Kling JD, Elghazzawy M, Huh M, et al. Two co‐dominant nitrogen‐fixing cyanobacteria demonstrate distinct acclimation and adaptation responses to cope with ocean warming. Env Microbiol Rep. 2022;14:203–17.Article 
    CAS 

    Google Scholar 
    Lande R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol. 2009;22:1435–46.Article 

    Google Scholar 
    Draghi J, Whitlock MC. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 2012;66:2891–902.Article 

    Google Scholar 
    Collins S, Rost B, Rynearson TA. Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl. 2014;7:140–55.Article 
    CAS 

    Google Scholar 
    Kim H, Spivack AJ, Menden-Deuer S. pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: Implications for bloom formation in an acidified ocean. Harmful Algae. 2013;26:1–11.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Quay P, Morales RL, Swanson LM, Armbrust EV. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J Phycol. 2014;50:243–53.Article 
    CAS 

    Google Scholar 
    Daufresne M, Lengfellner K, Sommer U. Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci. 2009;106:12788–93.Article 
    CAS 

    Google Scholar 
    Atkinson D, Ciotti BJ, Montagnes DJS. Protists decrease in size linearly with temperature: ca. 2.5% °C-1. Proc R Soc Lond B 2003;270:2605–11.Article 

    Google Scholar 
    Tong S, Gao K, Hutchins DA. Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2. Glob Chang Biol 2018;24:3055–64.Article 

    Google Scholar 
    Kelly KJ, Fu FX, Jiang X, Li H, Xu D, Yang N, et al. Interactions between ultraviolet B radiation, warming, and changing nitrogen source may reduce the accumulation of toxic Pseudo-nitzschia multiseries biomass in future coastal oceans. Front Mar Sci. 2021;8:433.Article 

    Google Scholar 
    Sterner R, Elser, J Ecological stoichiometry. In: Levin SA, et al. (eds) The Princeton Guide to Ecology. Princeton Univ. Press, 2009. pp 376–85.Petrou K, Baker KG, Nielsen DA, Hancock AM, Schulz KG, Davidson AT. Acidification diminishes diatom silica production in the Southern Ocean. Nat Clim Change 2019;9:781–86.Article 
    CAS 

    Google Scholar  More

  • in

    The influence of task difficulty, social tolerance and model success on social learning in Barbary macaques

    Heyes, B. Y. C. M. Social learning in animals: Categories and mechanisms. Biol. Rev. 69(2), 207–231. https://doi.org/10.1111/j.1469-185X.1994.tb01506.x (1994).Article 
    CAS 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social processes influencing learning in animals: A review of the evidence. Adv. Study Behav. 38, 105–165. https://doi.org/10.1016/S0065-3454(08)00003-X (2008).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I. & Laland, K. N. Adaptive trade-offs in the use of social and personal information. In Cognitive Ecology II (eds Dukas, R. & Ratcliffe, J. M.) 249–271 (University of Chicago Press, 2009).Chapter 

    Google Scholar 
    Marshall-Pescini, S. & Whiten, A. Social learning of nut-cracking behavior in East African sanctuary-living chimpanzees (Pan troglodytes schweinfurthii). J. Comp. Psychol. 122(2), 186. https://doi.org/10.1037/0735-7036.122.2.186 (2008).Article 

    Google Scholar 
    Hobaiter, C., Poisot, T., Zuberbühler, K., Hoppitt, W. & Gruber, T. Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees. PLoS Biol. 12(9), e1001960. https://doi.org/10.1371/journal.pbio.1001960 (2014).Article 
    CAS 

    Google Scholar 
    Coelho, C. G. et al. Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.). Anim. Cogn. 18(4), 911–919. https://doi.org/10.1007/s10071-015-0861-5 (2015).Article 
    CAS 

    Google Scholar 
    Boyd, R. & Richerson, P. J. Culture and the evolutionary process (University of Chicago press, 1985).
    Google Scholar 
    Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32(1), 4–14. https://doi.org/10.3758/BF03196002 (2004).Article 

    Google Scholar 
    Kendal, R. L. Animal ‘culture wars’: Evidence from the Wild?. Psychologist 21(4), 312–315 (2008).
    Google Scholar 
    Kendal, R. L., Kendal, J. R., Hoppitt, W. & Laland, K. N. Identifying social learning in animal populations: A new ‘option-bias’ method. PLoS ONE 4(8), e6541. https://doi.org/10.1371/journal.pone.0006541 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Giraldeau, L. A., Valone, T. J. & Templeton, J. J. Potential disadvantages of using socially acquired information. Philos. Trans. R. Soc. Lond. Series B. 357(1427), 1559–1566. https://doi.org/10.1098/rstb.2002.1065 (2002).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I., van Bergen, Y. & Laland, K. N. Trade-offs in the adaptive use of social and asocial learning. Adv. Study Behav. 35, 333–379. https://doi.org/10.1016/S0065-3454(05)35008-X (2005).Article 

    Google Scholar 
    Galef, B. G. Jr. Why behaviour patterns that animals learn socially are locally adaptive. Anim. Behav. 49(5), 1325–1334. https://doi.org/10.1006/anbe.1995.0164 (1995).Article 

    Google Scholar 
    Kendal, R. L. et al. Social learning strategies: Bridge-building between fields. Trends Cogn. Sci. 22(7), 651–665. https://doi.org/10.1016/j.tics.2018.04.003 (2018).Article 

    Google Scholar 
    Rendell, L. et al. Cognitive culture: Theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15(2), 68–76. https://doi.org/10.1016/j.tics.2010.12.002 (2011).Article 

    Google Scholar 
    Dindo, M., Thierry, B. & Whiten, A. Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc. R. Soc. B 275(1631), 187–193. https://doi.org/10.1098/rspb.2007.1318 (2008).Article 

    Google Scholar 
    Reader, S. M. & Biro, D. Experimental identification of social learning in wild animals. Learn. Behav. 38(3), 265–283. https://doi.org/10.3758/LB.38.3.265 (2010).Article 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social Learning: An Introduction to Mechanisms, Methods, and Models (Princeton University Press, 2013).Book 

    Google Scholar 
    Byrne, R. W. & Russon, A. E. Learning by imitation: A hierarchical approach. Behav. Brain Sci. 21(5), 667–684. https://doi.org/10.1017/S0140525X9833174X (1998).Article 
    CAS 

    Google Scholar 
    Kendal, R. L. et al. Evidence for social learning in wild lemurs (Lemur catta). Learn. Behav. 38(3), 220–234. https://doi.org/10.3758/LB.38.3.220 (2010).Article 

    Google Scholar 
    Lonsdorf, E. V. & Bonnie, K. E. Opportunities and constraints when studying social learning: Developmental approaches and social factors. Learn. Behav. 38(3), 195–205. https://doi.org/10.3758/LB.38.3.195 (2010).Article 

    Google Scholar 
    Coussi-korbel, S. & Fragaszy, M. On the relation between social dynamics and social learning. Anim. Behav. 50(6), 1441–1453. https://doi.org/10.1016/0003-3472(95)80001-8 (1995).Article 

    Google Scholar 
    Franz, M. & Nunn, C. L. Network-based diffusion analysis: A new method for detecting social learning. Proc. R. Soc. Lond B 276(1663), 1829–1836. https://doi.org/10.1098/rspb.2008.1824 (2009).Article 

    Google Scholar 
    Hoppitt, W., Boogert, N. J. & Laland, K. N. Detecting social transmission in networks. J. Theor. Biol. 263(4), 544–555. https://doi.org/10.1016/j.jtbi.2010.01.004 (2010).Article 
    ADS 
    MATH 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Detecting social learning using networks: A users guide. Am. J. Primatol. 73(8), 834–844. https://doi.org/10.1002/ajp.20920 (2011).Article 

    Google Scholar 
    Hasenjager, M. J., Leadbeater, E. & Hoppitt, W. Detecting and quantifying social transmission using network-based diffusion analysis. J. Anim. Ecol. 90(1), 8–26. https://doi.org/10.1111/1365-2656.13307 (2021).Article 

    Google Scholar 
    Schnoell, A. V. & Fichtel, C. Wild red-fronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Anim. Cogn. 15(4), 505–516. https://doi.org/10.1007/s10071-012-0477-y (2012).Article 

    Google Scholar 
    Coelho, C. Social Dynamics and Diffusion of Novel Behaviour Patterns in Wild Capuchin Monkeys (Sapajus libidinosus) Inhabiting the Serra da Capivara National Park. (Unpublished Doctoral Dissertation) (Durham University, 2015).
    Google Scholar 
    Claidière, N., Messer, E. J., Hoppitt, W. & Whiten, A. Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr. Biol. 23(13), 1251–1255. https://doi.org/10.1016/j.cub.2013.05.036 (2013).Article 
    CAS 

    Google Scholar 
    van Leeuwen, E. J., Staes, N., Verspeek, J., Hoppitt, W. J. & Stevens, J. M. Social culture in bonobos. Curr. Biol. 30(6), R261–R262. https://doi.org/10.1016/j.cub.2020.02.038 (2020).Article 
    CAS 

    Google Scholar 
    Canteloup, C., Hoppitt, W. & van de Waal, E. Wild primates copy higher-ranked individuals in a social transmission experiment. Nat. Commun. 11(1), 1–10. https://doi.org/10.1038/s41467-019-14209-8 (2020).Article 
    CAS 

    Google Scholar 
    Kawai, M. Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6(1), 1–30. https://doi.org/10.1007/BF01794457 (1965).Article 

    Google Scholar 
    Huffman, M. A., Leca, J. B. & Nahallage, C. A. Cultured Japanese macaques: A multidisciplinary approach to stone handling behavior and its implications for the evolution of behavioral tradition in nonhuman primates. In The Japanese Macaques (eds Nakagawa, N. et al.) 191–219 (Springer, 2010). https://doi.org/10.1007/978-4-431-53886-8_9.Chapter 

    Google Scholar 
    Drapier, M. & Thierry, B. Social transmission of feeding techniques in Tonkean macaques?. Int. J. Primatol. 23(1), 105–122. https://doi.org/10.1023/A:1013201924975 (2002).Article 

    Google Scholar 
    Ducoing, A. M. & Thierry, B. Tool-use learning in Tonkean macaques (Macaca tonkeana). Anim. Cogn. 8(2), 103–113. https://doi.org/10.1007/s10071-004-0240-0 (2005).Article 

    Google Scholar 
    Ferrari, P. F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4(9), e302. https://doi.org/10.1371/journal.pbio.0040302 (2006).Article 
    CAS 

    Google Scholar 
    Leca, J. B., Gunst, N. & Huffman, M. A. The first case of dental flossing by a Japanese macaque (Macaca fuscata): Implications for the determinants of behavioral innovation and the constraints on social transmission. Primates 51(1), 13. https://doi.org/10.1007/s10329-009-0159-9 (2010).Article 

    Google Scholar 
    Macellini, S. et al. Individual and social learning processes involved in the acquisition and generalization of tool use in macaques. Philos. Trans. R. Soc. B 367(1585), 24–36. https://doi.org/10.1098/rstb.2011.0125 (2012).Article 
    CAS 

    Google Scholar 
    Redshaw, J. Re-analysis of data reveals no evidence for neonatal imitation in rhesus macaques. Biol. Let. 15(7), 20190342. https://doi.org/10.1098/rsbl.2019.0342 (2019).Article 

    Google Scholar 
    Hook, M. A. et al. Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Appl. Anim. Behav. Sci. 76(2), 165–176. https://doi.org/10.1016/S0168-1591(02)00005-9 (2002).Article 

    Google Scholar 
    Watanabe, K., Urasopon, N. & Malaivijitnond, S. Long-tailed macaques use human hair as dental floss. Am. J. Primatol. 69(8), 940–944. https://doi.org/10.1002/ajp.20403 (2007).Article 

    Google Scholar 
    Gumert, M. D., Kluck, M. & Malaivijitnond, S. The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand. Am. J. Primatol. 71(7), 594–608. https://doi.org/10.1002/ajp.20694 (2009).Article 

    Google Scholar 
    Tan, A. W., Hemelrijk, C. K., Malaivijitnond, S. & Gumert, M. D. Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users. Anim. Cogn. 21(4), 551–563. https://doi.org/10.1007/s10071-018-1188-9 (2018).Article 

    Google Scholar 
    Bandini, E. & Tennie, C. Exploring the role of individual learning in animal tool-use. PeerJ 8, e9877. https://doi.org/10.7717/peerj.9877 (2020).Article 

    Google Scholar 
    Leca, J. B., Gunst, N., & Huffman, M. A. Japanese macaque cultures: Inter-and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour, 251–281. https://www.jstor.org/stable/4536445 (2007).Tanaka, I. Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am. J. Phys. Anthropol. 98(2), 197–201. https://doi.org/10.1002/ajpa.1330980208 (1995).Article 
    CAS 

    Google Scholar 
    Tanaka, I. Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Anim. Behav. 56(5), 1229–1236. https://doi.org/10.1006/anbe.1998.0891 (1998).Article 
    CAS 

    Google Scholar 
    Whiten, A. & van de Waal, E. The pervasive role of social learning in primate lifetime development. Behav. Ecol. Sociobiol. 72(5), 1–16. https://doi.org/10.1007/s00265-018-2489-3 (2018).Article 

    Google Scholar 
    Widdig, A., Streich, W. J. & Tembrock, G. Coalition formation among male Barbary macaques (Macaca sylvanus). Am. J. Primatol. 50(1), 37–51. https://doi.org/10.1002/(SICI)1098-2345(200001)50:1%3c37::AID-AJP4%3e3.0.CO;2-3 (2000).Article 
    CAS 

    Google Scholar 
    Thierry, B. Unity in diversity: Lessons from macaque societies. Evol. Anthropol. 16(6), 224–238. https://doi.org/10.1002/evan.20147 (2007).Article 

    Google Scholar 
    Berghänel, A., Ostner, J., Schröder, U. & Schülke, O. Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Anim. Behav. 81(6), 1109–1116. https://doi.org/10.1016/j.anbehav.2011.02.009 (2011).Article 

    Google Scholar 
    Carne, C., Wiper, S. & Semple, S. Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. Am. J. Primatol. 73(11), 1127–1133. https://doi.org/10.1002/ajp.20979 (2011).Article 

    Google Scholar 
    Molesti, S. & Majolo, B. Cooperation in wild Barbary macaques: Factors affecting free partner choice. Anim. Cogn. 19(1), 133–146. https://doi.org/10.1007/s10071-015-0919-4 (2016).Article 

    Google Scholar 
    Rebout, N., Desportes, C. & Thierry, B. Resource partitioning in tolerant and intolerant macaques. Aggress. Behav. 43(5), 513–520. https://doi.org/10.1002/ab.21709 (2017).Article 

    Google Scholar 
    Amici, F., Caicoya, A. L., Majolo, B. & Widdig, A. Innovation in wild Barbary macaques (Macaca sylvanus). Sci. Rep. 10(1), 1–12. https://doi.org/10.1038/s41598-020-61558-2 (2020).Article 
    CAS 

    Google Scholar 
    Fischer, J. Emergence of individual recognition in young macaques. Anim. Behav. 67(4), 655–661. https://doi.org/10.1016/j.anbehav.2003.08.006 (2004).Article 

    Google Scholar 
    Seyfarth, R. M. & Cheney, D. L. Production, usage, and comprehension in animal vocalizations. Brain Lang. 115(1), 92–100. https://doi.org/10.1016/j.bandl.2009.10.003 (2010).Article 

    Google Scholar 
    Garcia-Nisa, I. Communication and cultural transmission in populations of semi free-ranging Barbary macaques (Macaca sylvanus). (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/14140/ (2021).Hoppitt, W. The conceptual foundations of network-based diffusion analysis: Choosing networks and interpreting results. Philos. Trans. R. Soc. B 372(1735), 20160418. https://doi.org/10.1098/rstb.2016.0418 (2017).Article 

    Google Scholar 
    Hikami, K., Hasegawa, Y. & Matsuzawa, T. Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. J. Comp. Psychol. 104(3), 233. https://doi.org/10.1037/0735-7036.104.3.233 (1990).Article 
    CAS 

    Google Scholar 
    Deaner, R. O., Khera, A. V. & Platt, M. L. Monkeys pay per view: Adaptive valuation of social images by rhesus macaques. Curr. Biol. 15(6), 543–548. https://doi.org/10.1016/j.cub.2005.01.044 (2005).Article 
    CAS 

    Google Scholar 
    Gariépy, J. F. et al. Social learning in humans and other animals. Front. Neurosci. 8, 58. https://doi.org/10.3389/fnins.2014.00058 (2014).Article 

    Google Scholar 
    Barrett, B. J., McElreath, R. L. & Perry, S. E. Pay-off-biased social learning underlies the diffusion of novel extractive foraging traditions in a wild primate. Proc. R. Soc. B 284(1856), 20170358. https://doi.org/10.1098/rspb.2017.0358 (2017).Article 

    Google Scholar 
    Kuester, J. & Paul, A. Group fission in Barbary macaques (Macaca sylvanus) at Affenberg Salem. Int. J. Primatol. 18(6), 941–966. https://doi.org/10.1023/A:1026396113830 (1997).Article 

    Google Scholar 
    Whitehead, H. Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis (University of Chicago Press, 2008).Book 

    Google Scholar 
    Hoppitt, W. (2011). NBDA User Guide V1.2. https://lalandlab.st-andrews.ac.uk/freeware/ 28 Sept 2016.Fleiss, J. L., Levin, B. & Paik, M. C. Statistical Methods for Rates and Proportions 3rd edn. (Wiley, 2003).Book 
    MATH 

    Google Scholar 
    McHugh, M. L. Interrater reliability: the kappa statistic. Biochemia medica: Biochemia medica, 22(3), 276–282. https://hrcak.srce.hr/89395 (2012).Hair, J. F., Anderson, R. E., Babin, B. J. & Black, W. C. Multivariate Data Analysis: A Global Perspective Vol. 7 (Pearson Education, 2010).
    Google Scholar 
    Campbell, L. A., Tkaczynski, P. J., Lehmann, J., Mouna, M. & Majolo, B. Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles. Sci. Rep. 8(1), 1–8. https://doi.org/10.1038/s41598-018-24373-4 (2018).Article 
    CAS 

    Google Scholar 
    Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. Market forces predict grooming reciprocity in female baboons. Proc. R. Soc. Lond. Ser. B 266(1420), 665–670. https://doi.org/10.1098/rspb.1999.0687 (1999).Article 

    Google Scholar 
    Henzi, S. P. et al. Effect of resource competition on the long-term allocation of grooming by female baboons: Evaluating Seyfarth’s model. Anim. Behav. 66(5), 931–938. https://doi.org/10.1006/anbe.2003.2244 (2003).Article 

    Google Scholar 
    Ueno, M. & Nakamichi, M. Grooming facilitates huddling formation in Japanese macaques. Behav. Ecol. Sociobiol. 72(6), 1–10. https://doi.org/10.1007/s00265-018-2514-6 (2018).Article 

    Google Scholar 
    Carter, A. J., Tico, M. T. & Cowlishaw, G. Sequential phenotypic constraints on social information use in wild baboons. Elife 5, e13125. https://doi.org/10.7554/eLife.13125.001 (2016).Article 

    Google Scholar 
    Barelli, C., Reichard, U. H. & Mundry, R. Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar?. Anim. Behav. 82(4), 801–809. https://doi.org/10.1016/j.anbehav.2011.07.012 (2011).Article 

    Google Scholar 
    Schülke, O., Dumdey, N. & Ostner, J. Selective attention for affiliative and agonistic interactions of dominants and close affiliates in macaques. Sci. Rep. 10(1), 1–8. https://doi.org/10.1038/s41598-020-62772-8 (2020).Article 
    CAS 

    Google Scholar 
    Heesen, M., Macdonald, S., Ostner, J. & Schülke, O. Ecological and social determinants of group cohesiveness and within-group spatial position in wild Assamese macaques. Ethology 121(3), 270–283. https://doi.org/10.1111/eth.12336 (2015).Article 

    Google Scholar 
    Ortiz, K. M. Female feeding competition in a folivorous primate (Propithecus verreauxi) with formalized dominance hierarchies: contest or scramble? (Doctoral dissertation). University of Texas, USA. https://repositories.lib.utexas.edu/handle/2152/34120 (2015).Jurczyk, V., Fröber, K. & Dreisbach, G. Increasing reward prospect motivates switching to the more difficult task. Mot. Sci. 5(4), 295–313. https://doi.org/10.1037/mot0000119 (2019).Article 

    Google Scholar 
    Rathke, E. M. & Fischer, J. Differential ageing trajectories in motivation, inhibitory control and cognitive flexibility in Barbary macaques (Macaca sylvanus). Philos. Trans. R. Soc. B 375(1811), 20190617. https://doi.org/10.1098/rstb.2019.0617 (2020).Article 

    Google Scholar 
    Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: Implications for cultural diversity. Evol. Hum. Behav. 36(1), 65–72. https://doi.org/10.1016/j.evolhumbehav.2014.09.002 (2015).Article 

    Google Scholar 
    van de Waal, E., Claidière, N. & Whiten, A. Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys. Anim. Behav. 85(1), 71–76. https://doi.org/10.1016/j.anbehav.2012.10.008 (2013).Article 

    Google Scholar 
    Luncz, L. V. & Boesch, C. Tradition over trend: Neighboring chimpanzee communities maintain differences in cultural behavior despite frequent immigration of adult females. Am. J. Primatol. 76(7), 649–657. https://doi.org/10.1002/ajp.22259 (2014).Article 

    Google Scholar 
    van Leeuwen, E. J., Acerbi, A., Kendal, R. L., Tennie, C. & Haun, D. B. A reappreciation of ‘conformity’. Anim. Behav. 122, e5–e10. https://doi.org/10.1016/j.anbehav.2016.09.010 (2016).Article 

    Google Scholar 
    Horner, V. & Whiten, A. Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim. Cogn. 8(3), 164–181. https://doi.org/10.1007/s10071-004-0239-6 (2005).Article 

    Google Scholar 
    Wood, L. The influence of model-based biases and observer prior experience on social learning mechanisms and strategies. (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/7274/ (2013).van Leeuwen, E. J., Cronin, K. A., Schütte, S., Call, J. & Haun, D. B. Chimpanzees (Pan troglodytes) flexibly adjust their behaviour in order to maximize payoffs, not to conform to majorities. PLoS ONE 8(11), e80945. https://doi.org/10.1371/journal.pone.0080945 (2013).Article 
    CAS 

    Google Scholar 
    Vale, G. L., Flynn, E. G., Lambeth, S. P., Schapiro, S. J. & Kendal, R. L. Public information use in chimpanzees (Pan troglodytes) and children (Homo sapiens). J. Comp. Psychol. 128(2), 215–223. https://doi.org/10.1037/a0034420 (2014).Article 

    Google Scholar 
    Canteloup, C., Cera, M. B., Barrett, B. J. & van de Waal, E. Processing of novel food reveals payoff and rank-biased social learning in a wild primate. Sci. Rep. 11(1), 1–13. https://doi.org/10.1038/s41598-021-88857-6 (2021).Article 
    CAS 

    Google Scholar 
    Boccaletti, S. et al. The structure and dynamics of multilayer networks. Phys. Rep. 544(1), 1–122. https://doi.org/10.1016/j.physrep.2014.07.001 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Kivela, M. et al. Multilayer networks. J. Complex Netw. 2(3), 203e271. https://doi.org/10.1093/comnet/cnu016 (2014).Article 

    Google Scholar 
    Snijders, L. & Naguib, M. Communication in animal social networks: A missing link. Adv. Study Behav. 49, 297–359. https://doi.org/10.1016/bs.asb.2017.02.004 (2017).Article 

    Google Scholar 
    Finn, K. R., Silk, M. J., Porter, M. A. & Pinter-Wollman, N. The use of multilayer network analysis in animal behaviour. Anim. Behav. 149, 7–22. https://doi.org/10.1016/j.anbehav.2018.12.016 (2019).Article 

    Google Scholar  More

  • in

    Unspoilt forests fall to feed the global supply chain

    .readcube-buybox { display: none !important;}
    Agricultural expansion can plunder forests, but it is not the only human activity to do so. Researchers have found that more than one-third of the loss of Earth’s large, intact forests is driven by production for export — especially of wood, minerals and energy1.

    Access options

    /* style specs start */
    style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0 0;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50%0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:””;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
    /* style specs end */Subscribe to Nature+Get immediate online access to Nature and 55 other Nature journal$29.99monthlySubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueAll prices are NET prices.VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00All prices are NET prices.

    Additional access options:

    doi: https://doi.org/10.1038/d41586-023-00119-9

    References

    Subjects

    Conservation biology More

  • in

    Significant changes in soil microbial community structure and metabolic function after Mikania micrantha invasion

    Runyon, J. B., Butler, J. L., Friggens, M. M., Meyer, S. E. & Sing, S. E. Invasive species and climate change. USDA For. Serv. 285, 97–115 (2012).
    Google Scholar 
    Murphy, G. E. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).Article 

    Google Scholar 
    Mollot, G., Pantel, J. H. & Romanuk, T. N. The effects of invasive species on the decline in species richness: a global meta-analysis. Adv. Ecol. Res. 56, 61–83 (2017).Article 

    Google Scholar 
    Gaertner, M., Den Breeyen, A., Hui, C. & Richardson, D. M. Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: A meta-analysis. Prog. Phys. Geog. 33, 319–338 (2009).Article 

    Google Scholar 
    Vilà, M. et al. Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J. Biogeogr. 33, 853–861 (2010).Article 

    Google Scholar 
    Hejda, M., Pysek, P. & Jarosik, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).Article 

    Google Scholar 
    Powell, K. I., Chase, J. M. & Knight, T. M. A synthesis of plant invasion effects on biodiversity across spatial scales. Am. J. Bot. 98, 539–548 (2011).Article 

    Google Scholar 
    Ehrenfeld, J. G. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6, 503–523 (2003).Article 
    CAS 

    Google Scholar 
    Liao, C. et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytol. 177, 706–714 (2008).Article 
    CAS 

    Google Scholar 
    Chabrerie, O., Laval, K., Puget, P., Desaire, S. & Alard, D. Relationship between plant and soil microbial communities along a successional gradient in a chalk grassland in north-western France. Appl. Soil Ecol. 24, 43–56 (2003).Article 

    Google Scholar 
    Harris, J. Soil microbial communities and restoration ecology: Facilitators or followers?. Science 325, 573–574 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Dawson, W. & Schrama, M. Identifying the role of soil microbes in plant invasions. J. Ecol. 104, 1211–1218 (2016).Article 

    Google Scholar 
    Lankau, R. Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol. Invasions 12, 2059–2068 (2010).Article 

    Google Scholar 
    Siefert, A., Zillig, K. W., Friesen, M. L. & Strauss, S. Y. Soil microbial communities alter conspecific and congeneric competition consistent with patterns of field coexistence in three Trifolium congeners. J. Ecol. 106, 1876–1891 (2018).Article 
    CAS 

    Google Scholar 
    Kourtev, P. S., Ehrenfeld, J. G. & Haggblom, M. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152–3166 (2002).Article 

    Google Scholar 
    Li, W. H., Zhang, C. B., Jiang, H. B., Xin, G. R. & Yang, Z. Y. Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil 281, 309–324 (2006).Article 
    CAS 

    Google Scholar 
    Li, W. H., Zhang, C., Gao, G., Zan, Q. & Yang, Z. Relationship between Mikania micrantha invasion and soil microbial biomass, respiration and functional diversity. Plant Soil 296, 197–207 (2007).Article 
    CAS 

    Google Scholar 
    Chen, X. P. et al. Exotic plant Alnus trabeculosa alters the composition and diversity of native rhizosphere bacterial communities of Phragmites australis. Pedosphere 26, 108–119 (2016).Article 

    Google Scholar 
    Yin, L., Liu, B., Wang, H., Zhang, Y. & Fan, W. The rhizosphere microbiome of Mikania micrantha provides insight into adaptation and invasion. Front. Microbiol. 11, 1462 (2020).Article 

    Google Scholar 
    Griffiths, B. S., Ritz, K. & Wheatley, R. E. Relationship between functional diversity and genetic diversity in complex microbial communities. In Microbial Communities (eds Insam, H. & Rangger, A.) 1–9 (Springer, 1997). https://doi.org/10.1007/978-3-642-60694-6_1.Chapter 

    Google Scholar 
    Pérez-Piqueres, A., Edel-Hermann, V., Alabouvette, C. & Steinberg, C. Response of soil microbial communities to compost amendments. Soil Biol. Biochem. 38, 460–470 (2006).Article 

    Google Scholar 
    Grime, J. P. Plant strategies and vegetation processes. Biol. Plant 23, 254–254 (1979).
    Google Scholar 
    Goldberg, D. & Novoplansky, A. On the relative importance of competition in unproductive environments. J. Ecol. 85, 409–418 (1997).Article 

    Google Scholar 
    Goldberg, D. E., Martina, J. P., Elgersma, K. J. & Currie, W. S. Plant size and competitive dynamics along nutrient gradients. Am. Nat. 190, 229–243 (2017).Article 

    Google Scholar 
    Castro-Díez, P., Godoy, O., Alonso, A., Gallardo, A. & Saldaña, A. What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol. Lett. 17, 1–12 (2014).Article 

    Google Scholar 
    Chapuis-Lardy, L., Vanderhoeven, S., Dassonville, N., Koutika, L. S. & Meerts, P. Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biol. Fertil. Soils 42, 481–489 (2006).Article 

    Google Scholar 
    Thorpe, A. S., Archer, V. & DeLuca, T. H. The invasive forb, Centaurea maculosa, increases phosphorus availability in Montana grasslands. Appl. Soil Ecol. 32, 118–122 (2006).Article 

    Google Scholar 
    Hawkes, C. V., Wren, I. F., Herman, D. J. & Firestone, M. K. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol. Lett. 8, 976–985 (2005).Article 

    Google Scholar 
    Zhang, A. M., Chen, Z. H., Zhang, G. N., Chen, L. J. & Wu, Z. J. Soil phosphorus composition determined by 31P NMR spectroscopy and relative phosphatase activities influenced by land use. Eur. J. Soil Biol. 52, 73–77 (2012).Article 

    Google Scholar 
    Souza-Alonso, P., Novoa, A. & Gonzalez, L. Soil biochemical alterations and microbial community responses under Acacia dealbata Link invasion. Soil Biol. Biochem. 79, 100–108 (2014).Article 
    CAS 

    Google Scholar 
    Callaway, M. et al. Exotic invasive plants increase productivity, abundance of ammonia-oxidizing bacteria and nitrogen availability in intermountain grasslands. J. Ecol. 104, 994–1002 (2016).Article 

    Google Scholar 
    Zhao, M. et al. Ageratina adenophora invasions are associated with microbially mediated differences in biogeochemical cycles. Sci. Total Environ. 677, 47–56 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Litton, C. M., Sandquist, D. R. & Cordell, S. Effects of non-native grass invasion on aboveground carbon pools and tree population structure in a tropical dry forest of Hawaii. For. Ecol. Manag. 231, 105–113 (2006).Article 

    Google Scholar 
    Wolkovich, E. M., Lipson, D. A., Virginia, R. A., Cottingham, K. L. & Bolger, D. T. Grass invasion causes rapid increases in ecosystem carbon and nitrogen storage in a semiarid shrubland. Glob. Chang. Biol. 16, 1351–1365 (2010).Article 
    ADS 

    Google Scholar 
    Sardans, J. et al. Plant invasion is associated with higher plant-soil nutrient concentrations in nutrient-poor environments. Glob. Chang. Biol. 23, 1282–1291 (2017).Article 
    ADS 

    Google Scholar 
    Yu, H. et al. Soil nitrogen dynamics and competition during plant invasion: insights from Mikania micrantha invasions in China. New Phytol. 229, 3440–3452 (2021).Article 
    CAS 

    Google Scholar 
    Day, M. D. et al. Biology and impacts of pacific islands invasive species. 13. Mikania micrantha Kunth (Asteraceae). Pac. Sci. 70, 257–285 (2016).Article 

    Google Scholar 
    Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. (eds) 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. CID: 20.500.12592/drpzmz. (Auckland: Invasive Species Specialist Group, 2000).Zhang, L. Y., Ye, W. H., Cao, H. L. & Feng, H. L. Mikania micrantha H.B.K. in China: An overview. Weed Res. 44, 42–49 (2004).Article 

    Google Scholar 
    Manrique, V., Diaz, R., Cuda, J. P. & Overholt, W. A. Suitability of a new plant invader as a target for biological control in Florida. Invas. Plant Sci. Manag. 4, 1–10 (2011).Article 

    Google Scholar 
    Macanawai, A., Day, M., Tumaneng-Diete, T., Adkins, S. & Nausori, F. Impact of Mikania micrantha on crop production systems in Viti Levu, Fiji. Pak. J. Weed Sci. Res. 18, 357–365 (2012).
    Google Scholar 
    Carter, M. R. & Gregorich, E. G. (eds) Soil Sampling and Methods of Analysis 2nd edn. (CRC Press, 2007). https://doi.org/10.1201/9781420005271.Book 

    Google Scholar 
    Liu, X. et al. Will nitrogen deposition mitigate warming-increased soil respiration in a young subtropical plantation?. Agric. For. Meteorol. 246, 78–85 (2017).Article 
    ADS 

    Google Scholar 
    Turner, B. L. & Wright, S. J. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117, 115–130 (2014).Article 
    CAS 

    Google Scholar 
    Sun, S. & Badgley, B. D. Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biol. Biochem. 135, 163–172 (2019).Article 
    CAS 

    Google Scholar 
    Saiya-Cork, K. R., Sinsabaugh, R. L. & Zak, D. R. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309–1315 (2002).Article 
    CAS 

    Google Scholar 
    Dawkins, K. & Esiobu, N. The invasive brazilian pepper tree (Schinus terebinthifolius) is colonized by a root microbiome enriched with Alphaproteobacteria and unclassified Spartobacteria. Front. Microbiol. 9, 876 (2018).Article 

    Google Scholar 
    Carey, C. J., Beman, J. M., Eviner, V. T., Malmstrom, C. M. & Hart, S. C. Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands. Front. Microbiol. 6, 466 (2015).Article 

    Google Scholar 
    Strickland, M. S., Osburn, E., Lauber, C., Fierer, N. & Bradford, M. A. Litter quality is in the eye of the beholder: Initial decomposition rates as a function of inoculum characteristics. Funct. Ecol. 23, 627–636 (2009).Article 

    Google Scholar 
    Kanokratana, P. et al. Insights into the phylogeny and metabolic potential of a primary tropical peat swamp forest microbial community by metagenomic analysis. Microb. Ecol. 61, 518–528 (2011).Article 

    Google Scholar 
    Margesin, R., Jud, M., Tscherko, D. & Schinner, F. Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol. Ecol. 67, 208–218 (2009).Article 
    CAS 

    Google Scholar 
    Xu, Z. W. et al. Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol. Biochem. 104, 152–163 (2017).Article 
    CAS 

    Google Scholar 
    Zhou, X. et al. Warming and increased precipitation have differential effects on soil extracellular enzyme activities in a temperate grassland. Sci. Total Environ. 444, 552–558 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Mao, T. & Minoru, K. Using the KEGG database resource. Curr. Protoc. Bioinform. 38, 1121–11243. https://doi.org/10.1002/0471250953.bi0112s38 (2012).Article 

    Google Scholar 
    Grayston, S. J., Griffith, G. S., Mawdsley, J. L., Campbell, C. D. & Bardgett, R. D. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol. Biochem. 33, 533–551 (2001).Article 
    CAS 

    Google Scholar 
    Chen, W. B. & Chen, B. M. Considering the preferences for nitrogen forms by invasive plants: a case study from a hydroponic culture experiment. Weed Res. 59, 49–57 (2019).CAS 

    Google Scholar 
    Christian, J. M. & Wilson, S. D. Long-term ecosystem impacts of an introduced grass in the northern Great Plains. Ecology 80, 2397–2407 (1999).Article 

    Google Scholar 
    Strickland, M. S., Devore, J. L., Maerz, J. C. & Bradford, M. A. Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob. Chang. Biol. 16, 1338–1350 (2010).Article 
    ADS 

    Google Scholar 
    Bradley, B. A., Houghtonw, R. A., Mustard, J. F. & Hamburg, S. P. Invasive grass reduces aboveground carbon stocks in shrublands of the Western US. Glob. Chang. Biol. 12, 1815–1822 (2006).Article 
    ADS 

    Google Scholar 
    Ogle, S. M., Ojima, D. & Reiners, W. A. Modeling the impact of exotic annual brome grasses on soil organic carbon storage in a northern mixed-grass prairie. Biol. Invasions 6, 365–377 (2004).Article 

    Google Scholar 
    Ni, G. Y. et al. Mikania micrantha invasion enhances the carbon (C) transfer from plant to soil and mediates the soil C utilization through altering microbial community. Sci. Total Environ. 711, 135020. https://doi.org/10.1016/j.scitotenv.2019.135020 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Callaway, R. M., Thelen, G. C., Rodriguez, A. & Holben, W. E. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Klironomos, J. N. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70 (2002).Article 
    ADS 
    CAS 

    Google Scholar 
    Kourtev, P. S., Ehrenfeld, J. G. & Haggblom, M. Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol. Biochem. 35, 895–905 (2003).Article 
    CAS 

    Google Scholar 
    Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).Article 
    CAS 

    Google Scholar 
    Ehrenfeld, J. G., Kourtev, P. & Huang, W. Z. Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol. Appl. 11, 1287–1300 (2001).Article 

    Google Scholar 
    Allison, S. D. & Vitousek, P. M. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141, 612–619 (2004).Article 
    ADS 

    Google Scholar 
    Harner, M. J. et al. Decomposition of leaf litter from a native tree and an actinorhizal invasive across riparian habitats. Ecol. Appl. 19, 1135–1146 (2009).Article 

    Google Scholar 
    Wolkovich, E. M. Nonnative grass litter enhances grazing arthropod assemblages by increasing native shrub growth. Ecology 91, 756–766 (2010).Article 

    Google Scholar 
    Yan, J. et al. Conversion of organic carbon from decayed native and invasive plant litter in Jiuduansha wetland and its implications for SOC formation and sequestration. J. Soils Sediments 20, 675–689 (2020).Article 
    CAS 

    Google Scholar 
    Aerts, R. & de Caluwe, H. Nitrogen deposition effects on carbon dioxide and methane emissions from temperate peatland soils. Oikos 84, 44–54 (1999).Article 

    Google Scholar 
    Shen, C. C. et al. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol. Biochem. 57, 204–211 (2013).Article 
    CAS 

    Google Scholar 
    Kuypers, M. M. M., Marchant, H. K. & Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 16, 263–276 (2018).Article 
    CAS 

    Google Scholar 
    Mothé, G. P. B., Quintanilha-Peixoto, G., Souza, G. R. D., Ramos, A. C. & Intorne, A. C. Overview of the role of nitrogen in copper pollution and bioremediation mediated by plant–microbe interactions. In Soil Nitrogen Ecology (eds Cruz, C. et al.) 249–264. https://doi.org/10.1007/978-3-030-71206-8_12 (Springer, 2021).Chapter 

    Google Scholar 
    Chen, B. M., Peng, S. L. & Ni, G. Y. Effects of the invasive plant Mikania micrantha H.B.K. on soil nitrogen availability through allelopathy in South China. Biol. Invasions 11, 1291–1299 (2009).Article 

    Google Scholar 
    Fan, Y. X. et al. Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol. Fertil. Soils 54, 149–161 (2018).Article 
    CAS 

    Google Scholar 
    Walker, T. W. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).Article 
    ADS 
    CAS 

    Google Scholar 
    Khan, M. S., Zaidi, A., Ahemad, M. & Oves, M. Plant growth promotion by phosphate solubilizing fungi: Current perspective. Arch. Agron. Soil Sci. 56, 73–98 (2010).Article 
    CAS 

    Google Scholar 
    Kouas, S., Labidi, N., Debez, A. & Abdelly, C. Effect of P on nodule formation and N fixation in bean. Agron. Sustain. Dev. 25, 389–393 (2005).Article 
    CAS 

    Google Scholar 
    Bolan, N. S. et al. Dissolved organic matter: biogeochemistry, dynamics, and environmental significance in soils. Adv. Agron. 110, 1–75 (2011).Article 
    CAS 

    Google Scholar 
    Dail, D. B., Davidson, E. A. & Chorover, J. Rapid abiotic transformation of nitrate in an acid forest soil. Biogeochemistry 54, 131–146 (2001).Article 
    CAS 

    Google Scholar 
    Fitzhugh, R. D., Lovett, G. M. & Venterea, R. T. Biotic and abiotic immobilization of ammonium, nitrite, and nitrate in soils developed under different tree species in the Catskill Mountains, New York, USA. Glob. Chang. Biol. 9, 1591–1601 (2003).Article 
    ADS 

    Google Scholar  More

  • in

    Nudibranch predation boosts sponge silicon cycling

    Tréguer, P. J. et al. Reviews and syntheses: The biogeochemical cycle of silicon in the modern ocean. Biogeosciences 18, 1269–1289 (2021).Article 
    ADS 

    Google Scholar 
    Tréguer, P. et al. Influence of diatom diversity on the ocean biological carbon pump. Nat. Geosci. 11, 27–37 (2018).Article 
    ADS 

    Google Scholar 
    Benoiston, A.-S. et al. The evolution of diatoms and their biogeochemical functions. Phil. Trans. R. Soc. B 372, 20160397 (2017).Article 

    Google Scholar 
    de Goeij, J. M. et al. Surviving in a marine desert: The sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).Article 
    ADS 

    Google Scholar 
    Folkers, M. & Rombouts, T. Sponges revealed: a synthesis of their overlooked ecological functions within aquatic ecosystems. In YOUMARES 9—The Oceans: Our Research, Our Future (eds. Jungblut, S. et al.) 181–193 (Springer International Publishing, 2020).Kristiansen, S. & Hoell, E. E. The importance of silicon for marine production. Hydrobiologia 484, 21–31 (2002).Article 
    CAS 

    Google Scholar 
    Henderson, M. J., Huff, D. D. & Yoklavich, M. M. Deep-sea coral and sponge taxa increase demersal fish diversity and the probability of fish presence. Front. Mar. Sci. 7, 593844 (2020).Article 

    Google Scholar 
    McGrath, E. C., Woods, L., Jompa, J., Haris, A. & Bell, J. J. Growth and longevity in giant barrel sponges: Redwoods of the reef or pines in the Indo-Pacific?. Sci. Rep. 8, 15317 (2018).Article 
    ADS 

    Google Scholar 
    Jochum, K. P., Wang, X. H., Vennemann, T. W., Sinha, B. & Muller, W. E. G. Siliceous deep-sea sponge Monorhaphis chuni: A potential paleoclimate archive in ancient animals. Chem. Geol. 300, 143–151 (2012).Article 
    ADS 

    Google Scholar 
    Maldonado, M. et al. Sponge grounds as key marine habitats: A synthetic review of types, structure, functional roles, and conservation concerns. In Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots (eds. Rossi, S. et al.) vol. 1 145–184 (Springer International Publishing, 2017).Maldonado, M. et al. Sponge skeletons as an important sink of silicon in the global oceans. Nat. Geosci. 12, 815–822 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Maldonado, M. et al. Siliceous sponges as a silicon sink: An overlooked aspect of benthopelagic coupling in the marine silicon cycle. Limnol. Oceanogr. 50, 799–809 (2005).Article 
    ADS 
    CAS 

    Google Scholar 
    López-Acosta, M. et al. Sponge contribution to the silicon cycle of a diatom-rich shallow bay. Limnol. Oceanogr. 67, 2431–2447 (2022).Article 
    ADS 

    Google Scholar 
    Maldonado, M. et al. Massive silicon utilization facilitated by a benthic-pelagic coupled feedback sustains deep-sea sponge aggregations. Limnol. Oceanogr. 66, 366–391 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Wulff, J. L. Ecological interactions of marine sponges. Can. J. Zool. 84, 146–166 (2006).Article 

    Google Scholar 
    Pawlik, J. R., Loh, T.-L. & McMurray, S. E. A review of bottom-up vs. top-down control of sponges on Caribbean fore-reefs: What’s old, what’s new, and future directions. PeerJ 6, 4343 (2018).Article 

    Google Scholar 
    Dayton, P. K., Robilliard, G. A., Paine, R. T. & Dayton, L. B. Biological Accommodation in the Benthic Community at McMurdo Sound, Antartica. Ecol. Monogr. 44, 105–128 (1974).Article 

    Google Scholar 
    Meylan, A. Spongivory in hawksbill turtles: A diet of glass. Science 239, 393–395 (1988).Article 
    ADS 
    CAS 

    Google Scholar 
    Wulff, J. Sponge-feeding by Caribbean angelfishes, trunk-fishes, and filefishes. In Sponges in time and space 265–271 (A. A. Balkema, 1994).Santos, C. P., Coutinho, A. B. & Hajdu, E. Spongivory by Eucidaris tribuloides from Salvador, Bahia (Echinodermata: Echinoidea). J. Mar. Biol. Ass. 82, 295–297 (2002).Article 

    Google Scholar 
    Chu, J. W. F. & Leys, S. P. The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri as predators of glass sponges. Invertebr. Biol. 131, 75–81 (2012).Article 

    Google Scholar 
    Maschette, D. et al. Characteristics and implications of spongivory in the Knifejaw Oplegnathus woodwardi (Waite) in temperate mesophotic waters. J. Sea Res. 157, 101847 (2020).Article 

    Google Scholar 
    Knowlton, A. L. & Highsmith, R. C. Nudibranch-sponge feeding dynamics: Benefits of symbiont-containing sponge to Archidoris montereyensis (Cooper, 1862) and recovery of nudibranch feeding scars by Halichondria panicea (Pallas, 1766). J. Exp. Mar. Biol. Ecol. 327, 36–46 (2005).Article 

    Google Scholar 
    Bloom, S. A. Morphological correlations between dorid nudibranch predators and sponge prey. Veliger 18, 289–301 (1976).
    Google Scholar 
    Faulkner, D. & Ghiselin, M. Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar. Ecol. Prog. Ser. 13, 295–301 (1983).Article 
    ADS 

    Google Scholar 
    Bloom, S. A. Specialization and noncompetitive resource partitioning among sponge-eating dorid nudibranchs. Oecologia 49, 305–315 (1981).Article 
    ADS 

    Google Scholar 
    Clark, K. B. Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgolander Wiss. Meeresunters 27, 28–69 (1975).Article 
    ADS 

    Google Scholar 
    Wulff, J. Regeneration of sponges in ecological context: Is regeneration an integral part of life history and morphological strategies?. Integr. Comp. Biol. 50, 494–505 (2010).Article 

    Google Scholar 
    Wu, Y.-C., Franzenburg, S., Ribes, M. & Pita, L. Wounding response in Porifera (sponges) activates ancestral signaling cascades involved in animal healing, regeneration, and cancer. Sci. Rep. 12, 1307 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Turner, T. The marine sponge Hymeniacidon perlevis is a globally-distributed exotic species. Aquat. Invasions 15, 542–561 (2020).Article 

    Google Scholar 
    Ackers, R. G., Moss, D. & Picton, B. E. In Sponges of the British Isles (‘Sponge V’). vol. A Colour Guide and Working Document (Marine Conservation Society, 1992).Lima, P. O. V. & Simone, L. R. L. Anatomical review of Doris verrucosa and redescription of Doris januarii (Gastropoda, Nudibranchia) based on comparative morphology. J. Mar. Biol. Ass. 95, 1203–1220 (2015).Article 

    Google Scholar 
    Avila, C. et al. Biosynthetic origin and anatomical distribution of the main secondary metabolites in the nudibranch mollusc Doris verrucosa. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 97, 363–368 (1990).Article 

    Google Scholar 
    Urgorri, V. & Besteiro, C. The feeding habits of the nudibranchs of Galicia. Iberus 4, 51–58 (1984).
    Google Scholar 
    Aminot, A. & Kerouel, R. In Dosage automatique des nutriments dans les eaux marines: Méthodes en flux continu. Méthodes d’analyse en milieu marin, Ed. Ifremer 188 (2007).Hydes, D. J. & Liss, P. S. Fluorimetric method for the determination of low concentrations of dissolved aluminium in natural waters. Analyst 101, 922 (1976).Article 
    ADS 
    CAS 

    Google Scholar 
    López-Acosta, M., Leynaert, A., Coquille, V. & Maldonado, M. Silicon utilization by sponges: An assessment of seasonal changes. Mar. Ecol. Prog. Ser. 605, 111–123 (2018).Article 
    ADS 

    Google Scholar 
    Grall, J., Le-Loch, F., Guyonnet, B. & Riera, P. Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J. Exp. Mar. Biol. Ecol. 338, 1–15 (2006).Article 
    CAS 

    Google Scholar 
    Cebrian, E., Uriz, M. J., Garrabou, J. & Ballesteros, E. Sponge Mass Mortalities in a warming Mediterranean sea: Are cyanobacteria-harboring species worse off?. PLoS ONE 6, e20211 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    McClintock, J. B. Investigation of the relationship between invertebrate predation and biochemical composition, energy content, spicule armament and toxicity of benthic sponges at McMurdo Sound, Antartica. Mar. Biol. 94, 479–487 (1987).Article 
    CAS 

    Google Scholar 
    Cockburn, T. C. & Reid, R. G. B. Digestive tract enzymes in two Aeolid nudibranchs (opisthobranchia: Gastropoda). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 65, 275–281 (1980).Article 

    Google Scholar 
    De Caralt, S., Uriz, M. & Wijffels, R. Grazing, differential size-class dynamics and survival of the Mediterranean sponge Corticium candelabrum. Mar. Ecol. Prog. Ser. 360, 97–106 (2008).Article 
    ADS 

    Google Scholar 
    Ragueneau, O., De-Blas-Varela, E., Tréguer, P., Quéguiner, B. & Del Amo, Y. Phytoplankton dynamics in relation to the biogeochemical cycle of silicon in a coastal ecosystem of western Europe. Mar. Ecol. Prog. Ser. 106, 157–172 (1994).Article 
    ADS 

    Google Scholar 
    Turon, X., Tarjuelo, I. & Uriz, M. J. Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: Correlation with population structure and investment in defence: Growth and mortality of encrusting sponges. Funct. Ecol. 12, 631–639 (1998).Article 

    Google Scholar 
    Hoppe, W. F. Growth, regeneration and predation in three species of large coral reef sponges. Mar. Ecol. Prog. Ser. 50, 117–125 (1988).Article 
    ADS 

    Google Scholar 
    Ayling, A. L. Growth and regeneration rates in thinly encrusting Demospongiae from temperate waters. Biol. Bull. 165, 343–352 (1983).Article 

    Google Scholar 
    Fillinger, L., Janussen, D., Lundälv, T. & Richter, C. Rapid glass sponge expansion after climate-induced Antarctic ice shelf collapse. Curr. Biol. 23, 1330–1334 (2013).Article 
    CAS 

    Google Scholar 
    Dayton, P. K. et al. Benthic responses to an Antarctic regime shift: Food particle size and recruitment biology. Ecol. Appl. 29, 1 (2019).Article 

    Google Scholar 
    Guy, G. & Metaxas, A. Recruitment of deep-water corals and sponges in the Northwest Atlantic Ocean: Implications for habitat distribution and population connectivity. Mar. Biol. 169, 107 (2022).Article 

    Google Scholar 
    Beucher, C., Treguer, P., Corvaisier, R., Hapette, A. M. & Elskens, M. Production and dissolution of biosilica, and changing microphytoplankton dominance in the Bay of Brest (France). Mar. Ecol. Prog. Ser. 267, 57–69 (2004).Article 
    ADS 

    Google Scholar 
    López-Acosta, M., Leynaert, A. & Maldonado, M. Silicon consumption in two shallow-water sponges with contrasting biological features. Limnol. Oceanogr. 61, 2139–2150 (2016).Article 
    ADS 

    Google Scholar 
    Ellwood, M. J., Wille, M. & Maher, W. Glacial silicic acid concentrations in the Southern Ocean. Science 330, 1088–1091 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Maldonado, M. et al. Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges. Sci. Adv. 6, eaba9322 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Palumbi, S. R. Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science 225, 1478–1480 (1984).Article 
    ADS 
    CAS 

    Google Scholar 
    Broadribb, M., Bell, J. J. & Rovellini, A. Rapid acclimation in sponges: Seasonal variation in the organic content of two intertidal sponge species. J. Mar. Biol. Ass. 101, 983–989 (2021).Article 
    CAS 

    Google Scholar 
    Schönberg, C. H. L. & Barthel, D. Inorganic skeleton of the demosponge Halichondria panacea. Seasonality in spicule production in the Baltic Sea. Mar. Biol. 130, 133–140 (1997).Article 

    Google Scholar 
    Sheild, C. J. & Witman, J. D. The impact of Henricia sanguinolenta (O. F. Müller) (Echinodermata: Asteroidea) predation on the finger sponges, Isodictya spp.. J. Exp. Mar. Biol. Ecol. 166, 107–133 (1993).Article 

    Google Scholar 
    Lewis, J. R., Bowman, R. S., Kendall, M. A. & Williamson, P. Some geographical components in population dynamics: Possibilities and realities in some littoral species. Neth. J. Sea Res. 16, 18–28 (1982).Article 

    Google Scholar 
    Ashton, G. V. et al. Predator control of marine communities increases with temperature across 115 degrees of latitude. Science 376, 1215–1219 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Knowlton, A. & Highsmith, R. Convergence in the time-space continuum: A predator-prey interaction. Mar. Ecol. Prog. Ser. 197, 285–291 (2000).Article 
    ADS 

    Google Scholar  More

  • in

    Precision agriculture management based on a surrogate model assisted multiobjective algorithmic framework

    Study areaThe study area is located in Lintong District, Xi’an City, Shaanxi Province, China (34° 21′ 59.94″, 109° 12′ 51.012″) (Meteorologists, 2020b). The study area is located in northwestern China (Fig. 1), which is a Warm temperate semi-humid continental climate with distinct cold, warm, dry and wet seasons. Winter is cold, windy, foggy, and with little rain or snow. Spring is warm, dry, windy, and variable. The summer is hot and rainy, with prominent droughts and thunderstorms, and high wind. Autumn is cool, the temperature drops rapidly and autumn showers are obvious. The annual average temperature is 13.0–13.7 °C, the coldest January average temperature is −1.2–0 °C, the hottest July average temperature is 26.3–26.6 °C, the annual extreme minimum temperature is −21.2 °C, Lantian December 28, 1991, the annual extreme maximum temperature is 43.4 °C, Chang’an June 19, 1966. Annual precipitation is 522.4–719.5 mm, increasing from north to south. July and September are the two obvious peak precipitation months. The annual sunshine hours range from 1646.1 to 2114.9 h. The dominant wind direction varies from place to place, with the northeast wind in Xi’an, west wind in Zhouzhi and Huxian, east-northeast wind in Gaoling and Lintong, southeast wind in Chang’an, and northwest wind in Lantian. Meteorological disasters include drought, continuous rain, heavy rain, flooding, urban flooding, hail, gale, dry hot wind, high temperature, lightning, sand and dust, fog, haze, cold wave, and low-temperature freeze.
    Figure 1Location of the field of study (The satellite imagery supporting this study was obtained using Baidu Maps (Android version—16.4.0.1195). The URL is (https://map.baidu.com/@14256795.568410998,5210675.606268121,8.67z.).Full size imageWheat (XiNong 805) was planted on September 24, 2019 and matured for harvest on May 28, 2020 (We warrant that we have the right to collect and manage wheat (XiNong 805). In addition, the study is in compliance with relevant institutional, national, and international guidelines.). Among the six strategies in the experiment (Table 1), we focused on strategies 1 and 4, fixed irrigation dates optimization and fixed fertilizer application dates optimization. Based on the custom of the study area, three days of diffuse irrigation were selected for Strategy 1. Three days of fertilization of the urea and three days of irrigation were selected for Strategy 4. The best practice for Strategy 1 was total irrigation of 201 mm for the total season and a total of 7388 kg/ha of wheat was obtained for this simulation, while the best practice for Strategy 4 was total irrigation of 197 mm for the total season and a total fertilizer application of 282 kg/ha for the total season. A total of 7894 kg/ha of wheat was obtained for this simulation.Table 1 Details of the 6 strategies of the experimental setup.Full size tableDSSAT modelDSSAT, one of the most widely used crop growth models, is an integrated computer system developed by the University of Hawaii under the authority of the U.S. Agency for International Development (USAID). It aims to aggregate various crop models and standardize the format of model input and output variables to facilitate the diffusion and application of models7, thereby accelerating the diffusion of agricultural technology and providing decision making and countermeasures for the rational and efficient use of natural resources in developing countries.
    The DSSAT 4.5 model integrates all crop models into the simulation pathway-based CSM (Cropping System Model) farming system model, which uses a set of simulated soil moisture, nitrogen, and carbon dynamics codes, while crop growth and development are stimulated through the CERES37,38, CROPGRO39, CROPSIM, and SUBSOR modules. DSSAT is applicable to single sites or same type zones and can be extrapolated to the regional level through Geographic Information System (GIS).DSSAT–CSM simulates the growth process of crops grown on a uniform land area under prescribed or simulated management40, and the changes in soil water, carbon and nitrogen with under tillage systems. The DSSAT model is a decision support system supported by crop simulation models, which, in addition to data support, provides methods for calculating and solving problems, and provides decision-maker with the results of their decisions. It also provides scientific decisions for farmers to provide different cultivation management measures (e.g., proper fertilization and irrigation for crops) in different climatic years.Inputs and outputs of the modelThe DSSAT model has four main user-editable input files and various output files. The input files include crop management7,41, soil, weather, and cultivar parameter files; the output files include three types: (1) output files, (2) seasonal output files, and (3) diagnostic and management files.Crop management data: Crop management data provides basic information about crop growth. Detailed and accurate parameter provision is the basis for improving the accuracy of model simulation. Crop management parameters include crop variety, soil type, meteorological name, previous season crop, sowing period, sowing density, sowing depth, irrigation amount and time, fertilizer application amount and time, the initial condition of the soil, pest management, tillage frequency and method, etc. Some of these parameters are not easily available in field experiments and can be obtained from other test sites or from existing documentation. On the other hand, if there are missing values in the model, it will increase the simulation error of the model (this situation is hard to avoid). Therefore, in this study, the parameters were selected based on the principle of being both detailed and easily available.Soil data Soil data contains various parameters of the soil section plane, including soil color, soil slope, soil capacity, organic carbon, soil nitrogen content, drainage properties, the proportion of clay, particles, and stones in the soil. Similar to the governing documents, the more complete the parameters the smaller the error value of the simulation. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database at the time of the study. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database.Weather data The DSSAT model uses daily weather data as weather input data for the model. The model requires a minimum of four daily weather data in order to accurately simulate the water cycle in soil plants (Fig. 2). These are:(1) daily solar radiation energy (MJM); (2) daily maximum temperature (°C); (3) daily minimum temperature (°C); and (4) daily precipitation (mm). Weather data were obtained from the China Meteorological Administration. Weather data were obtained from the China Meteorological Administration.Figure 2Precipitation and maximum and minimum temperatures during 2019–2020.Full size imageModel calibration Adjusting the cultivar parameter is very important to accurately simulate the local growing environment. In this experiment, we collected field data for 2019 and 2020, and adjusted the parameters in the cultivar parameter files by trial-and-error method to make the simulation process more closely match the actual local crop growth process.Multi-objective optimization algorithmMulti-objective optimization techniques have been successfully applied in many real-world problems. In general42,43,44, MOPs produce a set of optimal solutions that together represent a trade-off between conflicting objectives, and such solutions are called Pareto optimal solutions (PS). These PS cannot make any solution better without compromising the other solutions. Therefore, when solving multi-objective problems, more PS are needed to find. Some MOPs aim to find all PS or at least a representative subset of them.A multi-objective optimization problem can be stated as follows:$$mathrm{min }Fleft(xright)={({f}_{1}left(xright),dots ,{f}_{k}(x))}^{T}$$
    (1)
    $$mathrm{subject;to};xin Omega$$
    (2)
    where (Omega) is the decision space,(F:Omega to {R}^{k}) consists of (k) real-value objective functions and ({R}^{k}) is called the objective space. The attainable objective set is defined as the set ({F(x)in Omega }).NSGA-II optimizerWe use non-dominated sorting genetic algorithm (NSGA-II) for Multiobjective optimization in R language. The NSGA-II algorithm is a classical multi-objective evolutionary algorithm with remarkable results in solving 2-objective and 3-objective problems45. It maintains the convergence speed and diversity of solutions by fast non-dominated sorting and crowding distance, selects the next population by elite selection strategy.Objective functionThe multi-objective optimization problem varies one or more variables to maximize or minimize two or more objective problems. In the case of crop production, where decision-makers change irrigation and fertilizer application to maximize benefits, this study focuses on when to apply irrigation or fertilizer on the field and how much irrigation or nitrogen fertilizer to apply.There are many crop models available that can be used as optimization objective functions, and DSSAT is definitely the best choice because it is easy to use and well-proven36. The user runs the model by entering defined soil, weather, variety, and crop management files, which are fed into the core of the model, the Crop Simulation Model (CSM). The model simulates the growth, development, and yield of crops grown on a uniform land area under management, as well as changes in soil water, carbon, and nitrogen over time under cropping systems. The CSM itself is a highly modular model system consisting of a number of sub-modules. Researchers have validated the output of these sub-modules as a whole under various crops, climate, and soil conditions.Using DSSAT, it is easy to design a set of objective functions and optimize them, as in our case.$$mathrm{Max}:Y=mathrm{DSSAT}left.left( {i}_{a0},dots ,{i}_{mathrm{aj}},{f}_{mathrm{a}0},dots ,{f}_{mathrm{ad}},{D}_{i}right.right)$$
    (3)
    $$mathrm{Min}:I=sum_{n=0}^{j}{i}_{an}$$
    (4)
    $$mathrm{Min}:F=sum_{m=0}^{d}{f}_{am}$$
    (5)
    where (Y) is yield,(I) is the total amount of irrigation, (F) is the total amount of nitrogen application, ({i}_{an}) is the amount of irrigation at one time, ({f}_{am}) is the amount of nitrogen applied at one time, (j) is a number of applications of irrigation, and (d) is a number of nitrogen applications. ({D}_{i}) is a random date combination of irrigation time and fertilizer application time.All other variables (e.g., climate, soil, location, crop variety) are kept constant during the optimization process. The irrigation unit is mm and the nitrogen application unit is kg/ha, the irrigation and nitrogen application amounts are positive integers by default (integer arithmetic reduces the program running time).Data-driven evolutionary algorithmsIn general, the key to DDEAs is to reduce the required FEs and assist evolution through data. The data is generally utilized through surrogate model. The use of suitable surrogate model can be used in place of real FEs46. Thus, DDEAs have more advantages over EAs in solving expensive problems.In terms of algorithmic framework, DDEAs contain two parts: surrogate model management (SMM) and evolutionary optimization part (EOP)47,48. The SMM part is used in order to obtain better approximations, while EOPs will use surrogate models in EAs to assist evolution. DDEAs can be divided into two types: online DDEAs and offline DDEAs23. Online DDEAs can be evaluated by real FEs with more new data. This new information can provide SMM with more information and construct a more accurate surrogate model49. Since DSSAT can obtain new data through FEs during the EOP process, the method used in this paper is online DDEAs. In contrast, offline DDEAs can only drive evolution through historical data.Radial Basis Function (RBF) network is a single hidden layer feedforward neural network that uses a radial basis function as the activation function for the hidden layer neurons, while the output layer is a linear combination of the outputs of the hidden layer neurons. RBF was used to approximate each objective function. According to the investigation of multi-objective optimization problems with high computational cost, radial basis functions are often used as the surrogate model, mainly because RBF networks can approximate arbitrary nonlinear functions with arbitrary accuracy and have global approximation capability, which fundamentally solves the local optimum problem of BP networks, and the topology is compact, the structural parameters can be learned separately, and the convergence speed is fast.In this paper, a new data-driven approach is proposed and place it in the lower-level optimization of the framework. RBF is utilized as the surrogate model and NSGA-II as the optimizer. Details are described in Algorithm 1.Data-driven method details
    In step 1, the initial parent population is generated by randomly selecting points and the size is (N). In step 2, we run DSSAT (N) times to determine the objective function values of the (N) initial population solutions. Next, the algorithm then loops through the generations. At the beginning of each loop, surrogate models, which one objective train one surrogate and denoted by ({s}_{t}^{left({f}_{1}right)}) , were trained by the already obtained objective function values (step 3.1). The trial offspring ({P}_{i}^{^{prime}}left(tright)={ {x}_{1}^{^{prime}}left(tright),dots ,{x}_{u}^{^{prime}}left(tright)}) are generated by SBX and PM (step 3.2), then the trained surrogate model is used to predict the objective function values of trial offspring (step 3.3). The predicted objective function values are sorting by Pareto non-dominated and crowding distance (step 3.4), then (r) offspring (Q_{i} left( t right) = left{ {x^{primeprime}_{1} left( t right), ldots ,x^{primeprime}_{r} left( t right)} right}) are selected from the trial offspring (step 3.5).The offspring are evaluated by the DSSAT (step 3.6), and after combining the parent population and offspring population (step 3.7), the new parent population are selected by Pareto non-dominated and crowding distance sorting (step 3.8).Maximum extension distanceMED guides a small number of individuals to approximate the entire PF. MED is defined as follow:$$mathrm{MED}left({P}_{t}^{left(qright)}right)=mathrm{ND}left({P}_{t}^{left(qright)}right)times mathrm{TD}left({P}_{t}^{left(qright)}right)$$
    (6)
    where$$mathrm{ND}left({P}_{t}^{left(qright)}right)=underset{z,qne z}{mathrm{min}}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$$$mathrm{TD}left({P}_{t}^{left(qright)}right)=sum_{z=1}^{P}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$({P}_{t}^{left(qright)}) is the qth individual in population Pt at the tth generation. (mathrm{ND}left({P}_{t}^{left(qright)}right)) calculates the minimum distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{ND}left({P}_{t}^{left(qright)}right)) value means a better individual diversity. (mathrm{TD}left({P}_{t}^{left(qright)}right)) calculates the summation of distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{TD}left({P}_{t}^{left(qright)}right)) value means that the solution ({P}_{t}^{left(qright)}) has moved away from other individuals. A larger MED value means that an individual extends the overall boundary and an individual acquires better diversity.Modeling processTo maximize crop yield and optimize the use efficiency of water and fertilizer in a given environment, BSBOP framework is proposed. Crop growth is simulated by DSSAT, the data-driven approach reduces the runtime of the overall framework while finding optimal management strategies. The overall framework includes four main parts: upper-level screening, upper-level optimization, lower-level optimization and lower-level screening (Fig. 3).Figure 3Proposed integrated bi-level screening, bi-level optimization and DSSAT framework.Full size imageUpper-level screening The weather file in DSSAT was loaded by R language. The data are pre-processed with precipitation and solar radiation information to narrow down the date range for irrigation and fertilizer application. In other words, the date ranges for selecting irrigation and fertilization are restricted by the ULS.Upper-level optimization Generating random combinations of dates by the Latin hypercube sampling method (LHS). The upper-level screening starts with referencing the two variables (number of irrigation and nutrient application events). LHS uses these variables to generate a series of uniformly distributed random day combinations. For example, date combinations generated by the LHS could be May 15, July 18 and August 1 for irrigation and May 30, June 30 and July 18 for nutrient application. From the series of uniformly distributed random day combinations, one will be selected and incorporated into the lower-level optimization.Lower-level optimization The agricultural management strategy is optimized by the online data-driven approach proposed in Algorithm 1. Assuming three irrigation and three nitrogen application events are given, these events will be incorporated into the LOP, which consists of the RBF and NSGA-II. The population size of this paper is 105. The number of iterations varies according to the different strategies, and the objective function values are calculated by DSSAT. The main idea of applying Evolutionary multi-objective algorithms(EMO) and RBF to DSSAT is to generate a large number of trial offspring by traditional Simulated Binary Crossover (SBX) and Polynomial Mutation (PM), and then evaluate them using the trained surrogate model50. The objective values of the evaluation were then ranked by Pareto non-dominated and crowding distance, and the top 105 individuals were selected from a large number of trial offspring, after which a small number of individuals out of 105 were selected by Maximum Extension Distance (MED) for real function evaluation, and then combine the parents and offspring to select the next generation of parents by Pareto non-dominated and crowding distance sorting. Furthermore, in the numerical experiments, to ensure the superiority of the algorithm and reduce the experimental complexity, we use a relatively simple radial basis function (RBF) surrogate. The NSGA-II algorithm can be used for both bi-objective and tri-objective problems, so it can optimize the system by starting with the most critical objective and then adding additional objectives. For each solution in the population, the objective functions (1: maximize yield, 2: minimize irrigation application, 3: minimize nitrogen fertilizer application) will be evaluated by invoking the DSSAT model for these dates and the amount of fertilizer irrigation applied. Populations will be tested against the termination criteria (maximum number of iterations allowed). If the termination criteria are not satisfied, the population evolves and is re-evaluated again. The process is repeated until the termination criterion is satisfied and then the local Pareto front of the selected day combination is stored. After each iteration of the UOP, the new local Pareto is combined with the global Pareto frontier. In the next step, if there are any remaining day combinations, the above process is repeated for each new day combination until all generated random day combinations have been processed.Lower-level screening Firstly, the K-means method is used to screen the global Pareto solutions with higher yield. Then, secondary screening takes economic efficiency as the objective and optimizes it by Differential Evolution (DE) algorithm. Finally, the locally appropriate solution is intelligently selected.Optimization strategies and configurationDue to the complexity of the problem, a BSBOP framework was proposed in this study. Due to a large number of variables behind irrigation and fertilization, traversal date for optimization appears to be particularly difficult and time-consuming, assuming that only irrigation is optimized for 120 days of the growth cycle and the decision-maker has 0-150 mm of water per day, then there are ({151}^{120}) different solutions. If both irrigation and fertilization are considered, then there are ({151}^{120}cdot {151}^{120}) different solutions. Therefore, this study tries to reduce the number of variables while minimizing the running time of the algorithm.Here we hypothesize that more precision and effective agricultural management can be implemented through the proposed framework. Not only can crop yields be increased, but also irrigation application and fertilizer application can be reduced, while the solutions obtained have important guidance for decision-makers: such as the selection of irrigation and fertilizer application dates during the growing season of the crop, the selection of irrigation and fertilizer application amounts, and the relationship between economic benefits and application costs. To test this hypothesis, different optimization strategies were developed and evaluated (Table 1). Each optimization strategy was aimed at maximizing yield while minimizing resource wastage.The various strategies are listed below (Table 1). Strategy 1—Fixed irrigation dates: Keeping the number of irrigation days and all parameters constant, only the amount of irrigation on each date is changed, trying to reduce the amount of irrigation as much as possible, make it easy to compare the results with best practices. Strategy 2—Optimal irrigation dates: Traverse through the irrigation dates to optimize irrigation, and try to find a better combination of irrigation dates (optimal dates) and better amount of irrigation over the wheat growth cycle. Strategy 3—Optimal irrigation dates based on surrogate model: RBF is added to Strategy 2, which makes it possible to reduce lots of time. Strategy 4—Fixed fertilizer application date: Using the optimal irrigation date found in Strategy 2 while keeping the number of days of fertilization and all other parameters constant, irrigation and fertilization are optimized in an attempt to minimize the amount of irrigation and fertilizer applied. Strategy 5—Optimal fertilizer application date: while ensuring the optimal irrigation date, traverse the fertilizer application date for optimization, trying to find out the potential yield of the crop. Strategy 6—Optimal fertilizer application date based on surrogate model: RBF is introduced based on Strategy 5. The time consumption was reduced.The stopping criterion in this study is when the optimization results converge visually. The algorithm population size was set to 105, and the generation of offspring used traditional polynomial Mutation. The number of hidden layers of the surrogate model is equal to the dimension of the decision variables, the learning rate is 0.01, the Gaussian kernel function is chosen as the activation function of the hidden layer in the RBF network. The neurons centers are generated by the K-means clustering method. The width parameter of the function is generated by calculating the variance of each cluster. The optimization weight parameters are selected by the recursive least square method. This is because the use of the least square method is likely to encounter situations where matrix inversion is troublesome. Therefore, recursive least squares (RLS) is often used to give a recursive form of the matrix in which the inverse needs to be found, making it computationally easier. More