More stories

  • in

    Family before work: task reversion in workers of the red imported fire ant, Solenopsis invicta in the presence of brood

    Wilson, E. O. The Insect Societies (Oxford University Press, 1971).
    Google Scholar 
    Beshers, S. N. & Fewell, J. H. Models of division of labor in social insects. Annu. Rev. Entomol. 46, 413–440 (2001).CAS 

    Google Scholar 
    Seeley, T. D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 4, 287–293 (1982).
    Google Scholar 
    Tallamy, D. W. Insect parental care. Bioscience 34, 20–24. https://doi.org/10.2307/1309421 (1984).Article 

    Google Scholar 
    Queller, D. C. Extended parental care and the origin of eusociality. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 256, 105–111. https://doi.org/10.1098/rspb.1994.0056 (1994).Article 
    ADS 

    Google Scholar 
    Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta 1,2. Ann. Entomol. Soc. Am. 68, 301–304 (1975).CAS 

    Google Scholar 
    Endler, A. et al. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl. Acad. Sci. USA 101, 2945–2950. https://doi.org/10.1073/pnas.0308447101 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Maisonnasse, A., Lenoir, J. C., Beslay, D., Crauser, D. & Le Conte, Y. E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS ONE 5, e13531. https://doi.org/10.1371/journal.pone.0013531 (2010).Article 
    ADS 
    CAS 

    Google Scholar 
    Schultner, E., Oettler, J. & Helantera, H. The role of brood in eusocial hymenoptera. Q. Rev. Biol. 92, 39–78. https://doi.org/10.1086/690840 (2017).Article 

    Google Scholar 
    Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A. & Omholt, S. W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering? J. Econ. Entomol. 97, 741–747 (2004).
    Google Scholar 
    Calabi, P. & Traniello, J. F. Behavioral flexibility in age castes of the ant Pheidole dentata. J. Insect Behav. 2, 663–677 (1989).
    Google Scholar 
    Gordon, D. W. Dynamics of task switching in harvester ants. Anim. Behav. 38, 194–204 (1989).
    Google Scholar 
    Robinson, G. E. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665. https://doi.org/10.1146/annurev.en.37.010192.003225 (1992).Article 
    CAS 

    Google Scholar 
    Robinson, E. J., Feinerman, O. & Franks, N. R. Flexible task allocation and the organization of work in ants. Proc. R. Soc. B: Biol. Sci. 276, 4373–4380 (2009).
    Google Scholar 
    Nijhout, H. F. & Wheeler, D. E. Juvenile-hormone and the physiological-basis of Insect polymorphisms. Q. Rev. Biol. 57, 109–133. https://doi.org/10.1086/412671 (1982).Article 
    CAS 

    Google Scholar 
    Herb, B. R. et al. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15, 1371–1373. https://doi.org/10.1038/nn.3218 (2012).Article 
    CAS 

    Google Scholar 
    Kensuke, N. Age polyethism, idiosyncrasy and behavioural flexibility in the queenless ponerine ant, Diacamma sp. J. Ethol. 13, 113–123 (1995).
    Google Scholar 
    Kensuke, N. Does behavioral flexibility compensate or constrain colony productivity? Relationship among age structure, labor allocation, and production of workers in ant colonies. J. Insect Behav. 9, 557–569 (1996).
    Google Scholar 
    Shimoji, H., Kasutani, N., Ogawa, S. & Hojo, M. K. Worker propensity affects flexible task reversion in an ant. Behav. Ecol. 74, 1–8 (2020).
    Google Scholar 
    Bernadou, A., Busch, J. & Heinze, J. Diversity in identity: Behavioral flexibility, dominance, and age polyethism in a clonal ant. Behav. Ecol. Sociobiol. 69, 1365–1375 (2015).
    Google Scholar 
    Kohlmeier, P., Feldmeyer, B. & Foitzik, S. Vitellogenin-like A—Associated shifts in social cue responsiveness regulate behavioral task specialization in an ant. PLoS Biol. 16, e2005747 (2018).
    Google Scholar 
    Tripet, F. & Nonacs, P. Foraging for work and age-based polyethism: The roles of age and previous experience on task choice in ants. Ethology 110, 863–877 (2004).
    Google Scholar 
    Kohlmeier, P., Alleman, A. R., Libbrecht, R., Foitzik, S. & Feldmeyer, B. Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers. Mol. Ecol. https://doi.org/10.1111/mec.14971 (2018).Article 

    Google Scholar 
    Levenbook, L. & Bauer, A. C. The fate of the larval storage protein calliphorin during adult development of Calliphora vicina. Insect Biochem. 14, 77–86 (1984).CAS 

    Google Scholar 
    Zhou, X., Oi, F. M. & Scharf, M. E. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. 103, 4499–4504 (2006).ADS 
    CAS 

    Google Scholar 
    Zhou, X., Tarver, M. R., Bennett, G., Oi, F. & Scharf, M. Two hexamerin genes from the termite Reticulitermes flavipes: Sequence, expression, and proposed functions in caste regulation. Gene 376, 47–58 (2006).CAS 

    Google Scholar 
    Hawkings, C., Calkins, T. L., Pietrantonio, P. V. & Tamborindeguy, C. Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta). PLoS ONE 14, e0216800 (2019).CAS 

    Google Scholar 
    Hoffman, E. A. & Goodisman, M. A. Gene expression and the evolution of phenotypic diversity in social wasps. BMC Biol. 5, 1–9 (2007).
    Google Scholar 
    Hunt, J. H., Buck, N. A. & Wheeler, D. E. Storage proteins in vespid wasps: Characterization, developmental pattern, and occurrence in adults. J. Insect Physiol. 49, 785–794 (2003).CAS 

    Google Scholar 
    Colgan, T. J. et al. Polyphenism in social insects: Insights from a transcriptome-wide analysis of gene expression in the life stages of the key pollinator, Bombus terrestris. BMC Genom. 12, 1–20 (2011).
    Google Scholar 
    Cremer, S., Armitage, S. A. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).CAS 

    Google Scholar 
    Cremer, S., Pull, C. D. & Fuerst, M. A. Social immunity: Emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2018).CAS 

    Google Scholar 
    Danihlík, J., Aronstein, K. & Petřivalský, M. Antimicrobial peptides: A key component of honey bee innate immunity: Physiology, biochemistry, and chemical ecology. J. Apic. Res. 54, 123–136 (2015).
    Google Scholar 
    Koch, S. I. et al. Caste-specific expression patterns of immune response and chemosensory related genes in the leaf-cutting ant, Atta vollenweideri. PLoS ONE 8, e81518 (2013).ADS 

    Google Scholar 
    Chardonnet, F. et al. Food searching behaviour of a Lepidoptera pest species is modulated by the foraging gene polymorphism. J. Exp. Biol. 217, 3465–3473 (2014).
    Google Scholar 
    Scheiner, R., Page, R. E. Jr. & Erber, J. Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav. Brain Res. 120, 67–73 (2001).CAS 

    Google Scholar 
    Wang, Z. et al. Visual pattern memory requires foraging function in the central complex of Drosophila. Learn. Mem. 15, 133–142 (2008).
    Google Scholar 
    Zhou, Y., Lei, Y., Lu, L. & He, Y. Temperature-and food-dependent foraging gene expression in foragers of the red imported fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae). Physiol. Entomol. 45, 1–6 (2020).
    Google Scholar 
    Ingram, K. K. et al. Context-dependent expression of the foraging gene in field colonies of ants: The interacting roles of age, environment and task. Proc. R. Soc. B: Biol. Sci. 283, 20160841 (2016).
    Google Scholar 
    Ingram, K. K., Oefner, P. & Gordon, D. M. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol. 14, 813–818 (2005).CAS 

    Google Scholar 
    Lucas, C. & Sokolowski, M. B. Molecular basis for changes in behavioral state in ant social behaviors. Proc. Natl. Acad. Sci. 106, 6351–6356 (2009).ADS 
    CAS 

    Google Scholar 
    Ben-Shahar, Y. The foraging gene, behavioral plasticity, and honeybee division of labor. J. Comp. Physiol. A. 191, 987–994 (2005).CAS 

    Google Scholar 
    Daugherty, T., Toth, A. & Robinson, G. Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol. Ecol. 20, 5337–5347 (2011).CAS 

    Google Scholar 
    Morrison, L. W., Porter, S. D., Daniels, E. & Korzukhin, M. D. Potential global range expansion of the invasive fire ant, Solenopsis invicta. Biol. Invasions 6, 183–191 (2004).
    Google Scholar 
    Valles, S. M., Wetterer, J. K. & Porter, S. D. The red imported fire ant (Hymenoptera: Formicidae) in the West Indies: Distribution of natural enemies and a possible test bed for release of self-sustaining biocontrol agents. Fls. Entomol. 98, 1101–1105 (2015).
    Google Scholar 
    Greenberg, L., Vinson, S. & Ellison, S. Nine-year study of a field containing both monogyne and polygyne red imported fire ants (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 85, 686–695 (1992).
    Google Scholar 
    Keller, L. & Ross, K. G. Selfish genes: A green beard in the red fire ant. Nature 394, 573–575 (1998).ADS 
    CAS 

    Google Scholar 
    Vinson, S. B. Impact of the invasion of the imported fire ant. Insect Sci. 20, 439–455 (2013).
    Google Scholar 
    Tschinkel, W. R. The Fire Ants (Harvard University Press, 2006).
    Google Scholar 
    Cassill, D. L. & Tschinkel, W. R. Task selection by workers of the fire ant Solenopsis invicta. Behav. Ecol. Sociobiol. 45, 301–310 (1999).
    Google Scholar 
    Mirenda, J. T. & Vinson, S. B. Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim. Behav. 29, 410–420 (1981).
    Google Scholar 
    Wilson, E. O. Division of labor in fire ants based on physical castes (Hymenoptera: Formicidae: Solenopsis). J. Kansas Entomol. Soc. 51, 615–636 (1978).
    Google Scholar 
    Sorensen, A., Busch, T. M. & Vinson, S. B. Behavioral flexibility of temporal subcastes in the fire ant, Solenopsis invicta in response to food. Psyche 91, 319–331 (1984).
    Google Scholar 
    Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 2, 301–304 (1975).
    Google Scholar 
    Bajracharya, P., Lu, H. L. & Pietrantonio, P. V. The red imported fire ant (Solenopsis invicta Buren) kept Y not F: Predicted sNPY endogenous ligands deorphanize the short NPF (sNPF) receptor. PLoS ONE 9(10), e109590 (2014).ADS 

    Google Scholar 
    Castillo, P. Short neuropeptide F receptor in the worker brain of the red imported fire ant (Solenopsis invicta Buren) and methodology for RNA interference M.S. thesis, Texas A&M University (2015).Castillo, P. & Pietrantonio, P. V. Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: Indicators for division of labor and nutritional status? PLoS ONE 8, e83966 (2013).ADS 

    Google Scholar 
    Cassill, D. L. & Tschinkel, W. R. Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim. Behav. 3, 801–813 (1995).
    Google Scholar 
    Cassill, D. L., Stuy, A. & Buck, R. G. Emergent properties of food distribution among fire ant larvae. J. Theor. Biol. 3, 371–381 (1998).ADS 

    Google Scholar 
    Dussutour, A. & Simpson, S. J. Communal nutrition in ants. Curr. Biol. 19, 740–744. https://doi.org/10.1016/j.cub.2009.03.015 (2009).Article 
    CAS 

    Google Scholar 
    Petralia, R. S. & Vinson, S. B. Feeding in the larvae of the imported fire ant, Solenopsis invicta: Behavior and morphological adaptations. Ann. Entomol. Soc. Am. 71, 643–648 (1978).
    Google Scholar 
    Petralia, R. S. & Vinson, S. B. Developmental morphology of larvae and eggs of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 72, 472–484 (1979).
    Google Scholar 
    Chen, J. Advancement on techniques for the separation and maintenance of the red imported fire ant colonies. Insect Sci. 14, 1–4 (2007).
    Google Scholar 
    Banks, W. A. et al. (Agricultural Research (Southern Region), Science and Education…, 1981).Valles, S. M. & Porter, S. D. Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Insectes Soc. 2, 199–200 (2003).
    Google Scholar 
    Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101 (2008).CAS 

    Google Scholar 
    Cheng, D., Zhang, Z., He, X. & Liang, G. Validation of reference genes in Solenopsis invicta in different developmental stages, castes and tissues. PLoS ONE 8, e57718. https://doi.org/10.1371/journal.pone.0057718 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Qiu, H.-L., Zhao, C.-Y. & He, Y.-R. On the molecular basis of division of labor in Solenopsis invicta (Hymenoptera: Formicidae) workers: RNA-seq analysis. J. Insect Sci. 17, 48 (2017).
    Google Scholar 
    Chen, J. et al. Role of the foraging gene in worker behavioral transition in the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Pest Manag. Sci. https://doi.org/10.1002/ps.6921 (2022).Article 

    Google Scholar 
    Shorter, J. R. & Tibbetts, E. A. The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus. Insectes Soc. 56, 7–13 (2009).
    Google Scholar 
    Pankiw, T., Page, R. E. Jr. & Kim Fondrk, M. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav. Ecol. Sociobiol. 44, 193–198. https://doi.org/10.1007/s002650050531 (1998).Article 

    Google Scholar 
    Smedal, B., Brynem, M., Kreibich, C. D. & Amdam, G. V. Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J. Exp. Biol. 212, 3795–3801. https://doi.org/10.1242/jeb.035063 (2009).Article 
    CAS 

    Google Scholar 
    Solis, C. R. & Strassmann, J. E. Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera, Vespidae). Funct. Ecol. 4, 531–541. https://doi.org/10.2307/2389321 (1990).Article 

    Google Scholar 
    Traynor, K. S. Decoding Brood Pheromone: The Releaser and Primer Effects of Young and Old Larvae on Honey Bee (Apis mellifera) Workers (Arizona State University, 2014).
    Google Scholar 
    Wagoner, K. M., Spivak, M. & Rueppell, O. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 111, 2520–2530. https://doi.org/10.1093/jee/toy266 (2018).Article 
    CAS 

    Google Scholar 
    Nijhout, H. F. & Wheeler, D. E. Juvenile hormone and the physiological basis of insect polymorphisms. Q. Rev. Biol. 57, 109–133 (1982).CAS 

    Google Scholar  More

  • in

    Mangrove reforestation provides greater blue carbon benefit than afforestation for mitigating global climate change

    Literature search and screeningOur analysis included a systematic literature search and was conducted by following the PRISMA protocol55 (Supplementary Fig. 7). We searched through Web of Science and China National Knowledge Infrastructure (CNKI) platforms by using keywords listed in Supplementary Table 3. A total of 3299 potentially relevant articles were found (Mandarin and English). The availability of peer-reviewed datasets associated with these published articles11,15,56,57,58,59 and online databases (The Sustainable Wetlands Adaptation and Mitigation Program (SWAMP) database, https://www2.cifor.org/swamp) were also considered. We then removed a significant number of articles through title screening, leaving 551 articles for further inspection.For these remaining articles, we used a four-step critique process to screen their title, abstract, and full text. We determined that firstly, they must provide carbon density data for at least one of the four mangrove carbon pools (i.e., aboveground biomass, belowground biomass, sediment organic carbon, or total ecosystem carbon). Secondly, articles needed to state the forest age or the starting date of the restoration action. For those studies providing only age intervals (e.g., 10–25 years, >66 years), we excluded them from the analysis. Thirdly, a description of prior land use was required. From these, mangrove restoration could be divided into two categories—reforestation and afforestation—on whether mangroves previously existed in that location. For reforestation, the initial conditions for inclusion were: (1) abandoned agricultural/aquacultural sites built previously by excavating mangrove forests, (2) clear-felled mangrove lands after wars, timber harvest, and silvicultural management, and (3) mangrove forests with mortality due to spraying of defoliants and hydrological alteration caused by the construction of embankments. We compared the carbon densities of reforested mangroves among sites with different causes of degradation/deforestation, and no significant difference is found (Supplementary Fig. 9). For those reforested mangroves, we assumed they would be protected and conserved by local governments and non-government organizations, so that there will not be human-driven degradation or deforestation in the near future. However, we acknowledge that a fraction of mangrove reforestation is managed for wood production, which means logging would happen at a certain interval after reforestation at these sites. For these logging sites, we used their reported measurements after clear-cut, such as 0-, 5-, 10-, 15-, and 25-year post-harvest sites in Sundarbans, Bangladesh60. On the other hand, the future occurrence of natural-driven deforestation (e.g., cyclones) is difficult to predict, and thus not considered in our study. For afforestation, the initial condition for inclusion was the presence of non-mangrove habitat immediately before afforestation began, such as mudflats, seagrass, saltmarsh, coral reef, or denuded areas. In most cases, reforestation and afforestation were undertaken through active planting without much re-engineering4, but for reforestation, natural regeneration could have, and in many places likely did, augment recruitment61. Moreover, we only considered mangrove succession that started from near-barren land with an insignificant amount of biomass, and introductions of exotic species to degraded areas with sparse trees were not incorporated. Lastly, if the forest age or prior land use type was not given, the articles needed to specify the location of sampling plots (latitude, longitude). With the coordinates matching, prior land use type and establishment dates were sometimes identifiable through remote sensing (Supplementary Fig. 10). For those articles sharing the same restoration sites but showing different aspects of the data collection, we combined the results and considered the collective work as one source. Based on the space-for-time method, data in the control sites before mangrove restoration actions were also collected as a paired site of restoration (e.g., abandoned ponds before mangrove reforestation; mudflats before mangrove afforestation). In total, we obtained data from 379 mangrove restoration sites described by 106 articles.Data extractionWe extracted aboveground living biomass carbon (AGC), belowground living biomass carbon (BGC), sediment carbon (SCS), and total ecosystem carbon (TECS) density from the 106 original data sources. In most cases, numeric values were provided. For those data not provided numerically but graphed, we determined values from figures with the application of GetData Graph Digitizer (http://getdata-graph-digitizer.com/).Among the articles, aboveground and belowground biomass (Mg ha−1) data were obtained using either a harvesting method (empirical) or an allometric method (calculation). Aboveground biomass represented the sum of stem, leaf, and branch dry weight, and we included prop root biomass when Rhizophora spp. were present. For soil coring methods that determined belowground biomass or sediment carbon density, belowground biomass was considered the dry weight of living coarse and fine roots multiplied by the ratio of core area to land surface area62. For allometric methods, trunk diameter at breast height (DBH, ~1.3 m) and tree height were used to calculate aboveground and belowground biomass by species-specific or common allometric equations63. These equations were also used to calculate the belowground biomass when articles provided plot information (DBH, height) but not belowground biomass (Supplementary Table 4). Total biomass was calculated as the sum of aboveground and belowground biomass. Deadwood and pneumatophore biomass were not included in our analysis; these data are rarely provided and/or methods of determination are inconsistent among global studies64. Some articles provided total biomass and shoot/root biomass ratio (S/R), and in such cases, above- and belowground biomass data were obtained through calculation as follows:$${{{{{rm{Aboveground}}}}}},{{{{{rm{biomass}}}}}}={{{{{rm{Total}}}}}},{{{{{rm{biomass}}}}}}times frac{frac{S}{R}}{frac{S}{R}+1}$$
    (1)
    $${{{{{rm{Belowground}}}}}},{{{{{rm{biomass}}}}}}={{{{{rm{Total}}}}}},{{{{{rm{biomass}}}}}}times frac{1}{frac{S}{R}+1}$$
    (2)
    For those articles measuring carbon content, study-specific carbon conversion factors were used to transform biomass to biomass carbon density (Mg C ha−1). If carbon content data were not provided, we converted aboveground and belowground biomass to carbon density by applying a conversion of 0.47 and 0.39, respectively65. The aboveground biomass carbon density was divided by its corresponding age to get the average aboveground biomass carbon accumulation rate (Mg C ha−1 yr−1).For sediment carbon density (SCS, Mg C ha−1), we selected the top 1 m because this depth equated to the most commonly reported depth and could reflect the impact of root mass input in the deeper depth66, which is also consistent with recent blue carbon standing stock assessment guidance64,67. Sediment carbon stock was calculated by multiplying sediment organic carbon content (SOC, %) by bulk density (BD, g cm−3), integrated over depth (cm). For studies that reported sediment carbon stock to More

  • in

    Intra-individual variation of hen movements is associated with later keel bone fractures in a quasi-commercial aviary

    Rufener, C. et al. Keel bone fractures are associated with individual mobility of laying hens in an aviary system. Appl. Anim. Behav. Sci. 217, 48–56 (2019).
    Google Scholar 
    Rentsch, A. K., Rufener, C. B., Spadavecchia, C., Stratmann, A. & Toscano, M. J. Laying hen’s mobility is impaired by keel bone fractures and does not improve with paracetamol treatment. Appl. Anim. Behav. Sci. 216, 19–25 (2019).
    Google Scholar 
    Rodriguez-Aurrekoetxea, A. & Estevez, I. Use of space and its impact on the welfare of laying hens in a commercial free-range system. Poult. Sci. 95, 2503–2513 (2016).CAS 

    Google Scholar 
    Fagan, W. F. et al. Spatial memory and animal movement. Ecol. Lett. 16, 1316–1329 (2013).
    Google Scholar 
    Campbell, D. L. M., Talk, A. C., Loh, Z. A., Dyall, T. R. & Lee, C. Spatial cognition and range use in free-range laying hens. Animals 8, 26 (2018).
    Google Scholar 
    de Jager, M., Weissing, F. J., Herman, P. M. J., Nolet, B. A. & van de Koppel, J. Lévy walks evolve through interaction between movement and environmental complexity. Science 1979(332), 1551–1553 (2011).
    Google Scholar 
    Krause, J., James, R. & Croft, D. P. Personality in the context of social networks. Philos. Trans. R. Soc. B Biol. Sci. 365, 4099–4106 (2010).CAS 

    Google Scholar 
    Ihwagi, F. W. et al. Poaching lowers elephant path tortuosity: Implications for conservation. J. Wildl. Manag. 83, 1022–1031 (2019).
    Google Scholar 
    Shaw, A. K. Causes and consequences of individual variation in animal movement. Mov. Ecol. 8, 1–12 (2020).
    Google Scholar 
    Matthews, S. G., Miller, A. L., Plötz, T. & Kyriazakis, I. Automated tracking to measure behavioural changes in pigs for health and welfare monitoring. Sci. Rep. 7, 1–12 (2017).CAS 

    Google Scholar 
    Berger-Tal, O. & Saltz, D. Using the movement patterns of reintroduced animals to improve reintroduction success. Curr. Zool. 60, 515–526 (2014).
    Google Scholar 
    Stuber, E. F., Carlson, B. S. & Jesmer, B. R. Spatial personalities: A meta-analysis of consistent individual differences in spatial behavior. Behav. Ecol. https://doi.org/10.1093/BEHECO/ARAB147 (2022).Article 

    Google Scholar 
    Sirovnik, J., Würbel, H. & Toscano, M. J. Feeder space affects access to the feeder, aggression, and feed conversion in laying hens in an aviary system. Appl. Anim. Behav. Sci. 198, 75–82 (2018).
    Google Scholar 
    Sirovnik, J., Voelkl, B., Keeling, L. J., Würbel, H. & Toscano, M. J. Breakdown of the ideal free distribution under conditions of severe and low competition. Behav. Ecol. Sociobiol. 75, 1–11 (2021).
    Google Scholar 
    Becot, L., Bedere, N., Burlot, T., Coton, J. & le Roy, P. Nest acceptance, clutch, and oviposition traits are promising selection criteria to improve egg production in cage-free system. PLoS ONE 16, e0251037 (2021).CAS 

    Google Scholar 
    Thompson, M. J., Evans, J. C., Parsons, S. & Morand-Ferron, J. Urbanization and individual differences in exploration and plasticity. Behav. Ecol. 29, 1415–1425 (2018).
    Google Scholar 
    Stamps, J. & Groothuis, T. G. G. The development of animal personality: Relevance, concepts and perspectives. Biol. Rev. 85, 301–325 (2010).
    Google Scholar 
    Salinas-Melgoza, A., Salinas-Melgoza, V. & Wright, T. F. Behavioral plasticity of a threatened parrot in human-modified landscapes. Biol. Conserv. 159, 303–312 (2013).
    Google Scholar 
    Stamps, J. A., Briffa, M. & Biro, P. A. Unpredictable animals: Individual differences in intraindividual variability (IIV). Anim. Behav. 83, 1325–1334 (2012).
    Google Scholar 
    Hertel, A. G., Royauté, R., Zedrosser, A. & Mueller, T. Biologging reveals individual variation in behavioural predictability in the wild. J. Anim. Ecol. 90, 723–737 (2021).
    Google Scholar 
    Biro, P. A. & Adriaenssens, B. Predictability as a personality trait: Consistent differences in intraindividual behavioral variation. Am. Nat. 182, 621–629 (2013).
    Google Scholar 
    Henriksen, R. et al. Intra-individual behavioural variability: A trait under genetic control. Int. J. Mol. Sci. 21, 8069 (2020).CAS 

    Google Scholar 
    Rufener, C. et al. Finding hens in a haystack: Consistency of movement patterns within and across individual laying hens maintained in large groups. Sci. Rep. 8, (2018).Campbell, D. L. M., Karcher, D. M. & Siegford, J. M. Location tracking of individual laying hens housed in aviaries with different litter substrates. Appl. Anim. Behav. 184, 74–79 (2016).
    Google Scholar 
    Weeks, C. A. & Nicol, C. J. Behavioural needs, priorities and preferences of laying hens. Worlds Poult. Sci. J. 62, 296–307 (2006).
    Google Scholar 
    Hartcher, K. M. & Jones, B. The welfare of layer hens in cage and cage-free housing systems. Worlds Poult. Sci. J. 73, 767–782 (2017).
    Google Scholar 
    Zeltner, E. & Hirt, H. Effect of artificial structuring on the use of laying hen runs in a free-range system. Br. Poult. Sci. 44, 533–537 (2010).
    Google Scholar 
    Stratmann, A. et al. Modification of aviary design reduces incidence of falls, collisions and keel bone damage in laying hens. Appl. Anim. Behav. Sci. 165, 112–123 (2015).
    Google Scholar 
    Vandekerchove, D., Herdt, P., Laevens, H. & Pasmans, F. Colibacillosis in caged layer hens: Characteristics of the disease and the aetiological agent. Avian Pathol. 33, 117–125 (2004).CAS 

    Google Scholar 
    Montalcini, C. M., Voelkl, B., Gómez, Y., Gantner, M. & Toscano, M. J. Evaluation of an active LF tracking system and data processing methods for livestock precision farming in the poultry sector. Sensors 22, 659 (2022).ADS 

    Google Scholar 
    Revelle, W. Procedures for psychological, psychometric, and personality research. (2021).Kaiser, H. F. The application of electronic computers to factor analysis. Educ. Psychol. Meas. 20, 141–151 (1960).
    Google Scholar 
    Rufener, C., Baur, S., Stratmann, A. & Toscano, M. J. A reliable method to assess keel bone fractures in laying hens from radiographs using a tagged visual analogue scale. Front. Vet. Sci. 5, 124 (2018).
    Google Scholar 
    Tauson, R., Kjaer, J., Maria, G. A., Cepero, R. & Holm, K.-E. The creation of a common scoring system for the integument and health of laying hens: Applied scoring of integument and health in laying hens. Final report Health from the Laywell project. https://www.laywel.eu/web/pdf/deliverables%2031-33%20health.pdf (2005).Hertel, A. G. et al. A guide for studying among-individual behavioral variation from movement data in the wild. Mov. Ecol. 8, (2020).Nakagawa, S. & Schielzeth, H. Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biol. Rev. 85, 935–956 (2010).
    Google Scholar 
    Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. Behavioural reaction norms: Animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81–89 (2010).
    Google Scholar 
    Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J Stat Softw 67, (2015).Cleasby, I. R., Nakagawa, S. & Schielzeth, H. Quantifying the predictability of behaviour: Statistical approaches for the study of between-individual variation in the within-individual variance. Methods Ecol. Evol. 6, 27–37 (2015).
    Google Scholar 
    Bürkner, P.-C. brms: An R package for bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).
    Google Scholar 
    Vehtari, A., Gelman, A. & Gabry, J. Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Stat. Comput. 27, 1413–1432 (2017).MathSciNet 
    MATH 

    Google Scholar 
    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).MATH 

    Google Scholar 
    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
    Google Scholar 
    Houslay, T. M. & Wilson, A. J. Avoiding the misuse of BLUP in behavioural ecology. Behav. Ecol. 28, 948–952 (2017).
    Google Scholar 
    Hertel, A. G., Niemelä, P. T., Dingemanse, N. J. & Mueller, T. Don’t poke the bear: Using tracking data to quantify behavioural syndromes in elusive wildlife. Anim. Behav. 147, 91–104 (2019).
    Google Scholar 
    Spiegel, O., Leu, S. T., Bull, C. M. & Sih, A. What’s your move? Movement as a link between personality and spatial dynamics in animal populations. Ecol. Lett. 20, 3–18 (2017).ADS 

    Google Scholar 
    Bell, A. M., Hankison, S. J. & Laskowski, K. L. The repeatability of behaviour: A meta-analysis. Anim. Behav. 77, 771–783 (2009).
    Google Scholar 
    Occhiuto, F., Vázquez-Diosdado, J. A., Carslake, C. & Kaler, J. Personality and predictability in farmed calves using movement and space-use behaviours quantified by ultra-wideband sensors. R. Soc. Open Sci. 9, (2022).Moinard, C. et al. Accuracy of laying hens in jumping upwards and downwards between perches in different light environments. Appl. Anim. Behav. Sci. 85, 77–92 (2004).
    Google Scholar 
    Baur, S., Rufener, C., Toscano, M. J. & Geissbühler, U. Radiographic evaluation of keel bone damage in laying hens—Morphologic and temporal observations in a longitudinal study. Front. Vet. Sci. 1, 129 (2020).
    Google Scholar 
    Cordiner, L. S. & Savory, C. J. Use of perches and nestboxes by laying hens in relation to social status, based on examination of consistency of ranking orders and frequency of interaction. Appl. Anim. Behav. Sci. 71, 305–317 (2001).
    Google Scholar 
    Rufener, C. & Makagon, M. M. Keel bone fractures in laying hens: A systematic review of prevalence across age, housing systems, and strains. J. Anim. Sci. 98, S36–S51 (2020).
    Google Scholar 
    Nasr, M. A. F., Nicol, C. J., Wilkins, L. & Murrell, J. C. The effects of two non-steroidal anti-inflammatory drugs on the mobility of laying hens with keel bone fractures. Vet. Anaesth. Analg. 42, 197–204 (2015).CAS 

    Google Scholar 
    Nasr, M., Murrell, J., Wilkins, L. J. & Nicol, C. J. The effect of keel fractures on egg-production parameters, mobility and behaviour in individual laying hens. Anim. Welf. 21, 127–135 (2012).CAS 

    Google Scholar 
    Koolhaas, J. M. & van Reenen, C. G. Animal behavior and well-being symposium: Interaction between coping style/personality, stress, and welfare: Relevance for domestic farm animals. J. Anim. Sci. 94, 2284–2296 (2016).CAS 

    Google Scholar 
    Coppens, C. M., de Boer, S. F. & Koolhaas, J. M. Coping styles and behavioural flexibility: Towards underlying mechanisms. Philos. Trans. R. Soc. B Biol. Sci. 365, 4021 (2010).
    Google Scholar 
    Koolhaas, J. M., de Boer, S. F., Coppens, C. M. & Buwalda, B. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Front. Neuroendocrinol. 31, 307–321 (2010).CAS 

    Google Scholar 
    Finkemeier, M.-A., Langbein, J. & Puppe, B. Personality research in mammalian farm animals: Concepts, measures, and relationship to welfare. Front. Vet. Sci. 5, 131 (2018).
    Google Scholar 
    Martin, J. G. A., Pirotta, E., Petelle, M. B. & Blumstein, D. T. Genetic basis of between-individual and within-individual variance of docility. J. Evol. Biol. 30, 796–805 (2017).CAS 

    Google Scholar 
    Prentice, P. M., Houslay, T. M., Martin, J. G. A. & Wilson, A. J. Genetic variance for behavioural ‘predictability’ of stress response. J. Evol. Biol. 33, 642–652 (2020).
    Google Scholar  More

  • in

    Agricultural spider decline: long-term trends under constant management conditions

    Waters, C. N. et al. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351, 137. https://doi.org/10.1126/science.aad2622 (2016).Article 
    CAS 

    Google Scholar 
    Thomas, J. A. & Morris, M. G. Patterns, mechanisms and rates of extinction among invertebrates in the United Kingdom. Phil. Trans. R. Soc. Lond. B 344, 47–54 (1994).Article 
    ADS 

    Google Scholar 
    Thomas, J. A. et al. Comparative losses of british butterflies, birds, and plants and the global extinction crisis. Science 303, 1879–1881. https://doi.org/10.1126/science.1095046 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    van Klink, R. et al. Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368, 417–420. https://doi.org/10.1126/science.aax9931 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, 21. https://doi.org/10.1371/journal.pone.0185809 (2017).Article 
    CAS 

    Google Scholar 
    Barmentlo, S. H. et al. Experimental evidence for neonicotinoid driven decline in aquatic emerging insects. Proc. Natl. Acad. Sci. USA 118, 8. https://doi.org/10.1073/pnas.2105692118j1of8 (2021).Article 

    Google Scholar 
    Ehlers, B. K., Bataillon, T. & Damgaard, C. F. Ongoing decline in insect-pollinated plants across Danish grasslands. Biol. Lett. 17, 20210493. https://doi.org/10.1098/rsbl.2021.0493 (2021).Article 

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

    Google Scholar 
    Cardoso, P. et al. Scientists’ warning to humanity on insect extinctions. Biol. Conserv. 242, 108426. https://doi.org/10.1016/j.biocon.2020.108426 (2020).Article 

    Google Scholar 
    Montgomery, G. A. et al. Is the insect apocalypse upon us? How to find out. Biol. Conserv. 241, 6. https://doi.org/10.1016/j.biocon.2019.108327 (2020).Article 

    Google Scholar 
    Jactel, H. et al. Insect decline: immediate action is needed. C. R. Biol. 343, 267–293. https://doi.org/10.5802/crbiol.37 (2020).Article 

    Google Scholar 
    Owens, A. C. S. et al. Light pollution is a driver of insect declines. Biol. Conserv. 241, 9. https://doi.org/10.1016/j.biocon.2019.108259 (2020).Article 

    Google Scholar 
    Sanchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020 (2019).Article 

    Google Scholar 
    Michalko, R., Pekar, S. & Entling, M. H. An updated perspective on spiders as generalist predators in biological control. Oecologia https://doi.org/10.1007/s00442-018-4313-1 (2018).Article 

    Google Scholar 
    Nyffeler, M., Sterling, W. & Dean, D. How spiders make a living. Environ. Entomol. 23, 1357–1367 (1994).Article 

    Google Scholar 
    Branco, V. V. & Cardoso, P. An expert-based assessment of global threats and conservation measures for spiders. Glob. Ecol. Conserv. 24, 15. https://doi.org/10.1016/j.gecco.2020.e01290 (2020).Article 

    Google Scholar 
    Gobbi, M., Fontaneto, D. & De Bernardi, F. Influence of climate changes on animal communities in space and time: The case of spider assemblages along an alpine glacier foreland. Glob. Change Biol. 12, 1985–1992. https://doi.org/10.1111/j.1365-2486.2006.01236.x (2006).Article 
    ADS 

    Google Scholar 
    Mammola, S., Goodacre, S. L. & Isaia, M. Climate change may drive cave spiders to extinction. Ecography 41, 233–243. https://doi.org/10.1111/ecog.02902 (2018).Article 

    Google Scholar 
    Potapov, A. M. et al. Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change. Ecology 101, e02957. https://doi.org/10.1002/ecy.2957 (2020).Article 

    Google Scholar 
    Kormann, U. et al. Local and landscape management drive trait-mediated biodiversity of nine taxa on small grassland fragments. Divers. Distrib. 21, 1204–1217. https://doi.org/10.1111/ddi.12324 (2015).Article 

    Google Scholar 
    Hogg, B. N. & Daane, K. M. Ecosystem services in the face of invasion: the persistence of native and nonnative spiders in an agricultural landscape. Ecol. Appl. 21, 565–576. https://doi.org/10.1890/10-0496.1 (2011).Article 

    Google Scholar 
    Galle, R., Happe, A. K., Baillod, A. B., Tscharntke, T. & Batary, P. Landscape configuration, organic management, and within-field position drive functional diversity of spiders and carabids. J. Appl. Ecol. 56, 63–72. https://doi.org/10.1111/1365-2664.13257 (2019).Article 

    Google Scholar 
    Pekár, S. Spiders (Araneae) in the pesticide world: An ecotoxicological review. Pest. Manage. Sci. 68, 1438–1446. https://doi.org/10.1002/ps.3397 (2012).Article 
    CAS 

    Google Scholar 
    Bommarco, R., Miranda, F., Bylund, H. & Bjorkman, C. Insecticides suppress natural enemies and increase pest damage in cabbage. J. Econ. Entomol. 104, 782–791. https://doi.org/10.1603/ec10444 (2011).Article 
    CAS 

    Google Scholar 
    Outhwaite, C. L., Gregory, R. D., Chandler, R. E., Collen, B. & Isaac, N. J. B. Complex long-term biodiversity change among invertebrates, bryophytes and lichens. Nature Ecol. Evol. 4, 384–392. https://doi.org/10.1038/s41559-020-1111-z (2020).Article 

    Google Scholar 
    Rix, M. G. et al. Where have all the spiders gone? The decline of a poorly known invertebrate fauna in the agricultural and arid zones of southern Australia. Austral Entomol. 56, 14–22. https://doi.org/10.1111/aen.12258 (2017).Article 

    Google Scholar 
    Nyffeler, M. & Bonte, D. Where have all the spiders gone? Observations of a dramatic population density decline in the once very abundant garden spider, Araneus diadematus (Araneae: Araneidae), in the Swiss Midland. Insects 11, 12. https://doi.org/10.3390/insects11040248 (2020).Article 

    Google Scholar 
    Bowden, J. J., Hansen, O. L. P., Olsen, K., Schmidt, N. M. & Høye, T. T. Drivers of inter-annual variation and long-term change in High-Arctic spider species abundances. Polar Biol. 41, 1635–1649. https://doi.org/10.1007/s00300-018-2351-0 (2018).Article 

    Google Scholar 
    Samu, F., Németh, J. & Kiss, B. Assessment of the efficiency of a hand-held suction device for sampling spiders: Improved density estimation or oversampling?. Ann. Appl. Biol. 130, 371–378. https://doi.org/10.1111/j.1744-7348.1997.tb06840.x (1997).Article 

    Google Scholar 
    Nentwig, W. et al. Spiders of Europe. Version 07.2022. https://www.araneae.nmbe.ch (2022).Heimer, S. & Nentwig, W. Spinnen Mitteleuropas (Paul Parey, 1991).
    Google Scholar 
    Samu, F. & Szinetár, C. On the nature of agrobiont spiders. J. Arachnol. 30, 389–402. https://doi.org/10.1636/0161-8202(2002)030[0389:Otnoas]2.0.Co;2 (2002).Article 

    Google Scholar 
    Buchar, J. & Růžička, V. Catalogue of Spiders of the Czech Republic (Peres, 2002).
    Google Scholar 
    Samu, F. A general data model for databases in experimental animal ecology. Acta Zool. Acad. Sci. Hung. 45, 273–290 (1999).
    Google Scholar 
    Laliberté, E., Legendre, P. & Shipley, B. FD: Measuring Functional Diversity from Multiple Traits, and Other Tools for Functional Ecology. R package version 1.0–12. (2014).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Zuur, A., Ieno, E., Walker, N., Saveliev, A. & Smith, G. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).Book 
    MATH 

    Google Scholar 
    Vegan. Community Ecology Package. R package Version 2.5–6. The Comprehensive R Archive Network (2019).ter Braak, C. J. F. & Smilauer, P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.1x. (Microcomputer Power, 2018).McRae, L., Deinet, S. & Freeman, R. The diversity-weighted living planet index: Controlling for taxonomic bias in a global biodiversity indicator. PLoS ONE 12, e0169156. https://doi.org/10.1371/journal.pone.0169156 (2017).Article 
    CAS 

    Google Scholar 
    Toju, H. & Baba, Y. G. DNA metabarcoding of spiders, insects, and springtails for exploring potential linkage between above- and below-ground food webs. Zool. Lett. 4, 12. https://doi.org/10.1186/s40851-018-0088-9 (2018).Article 

    Google Scholar 
    Dirzo, R. et al. Defaunation in the anthropocene. Science 345, 401–406. https://doi.org/10.1126/science.1251817 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Lister, B. C. & Garcia, A. Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl. Acad. Sci. USA 115, E10397–E10406. https://doi.org/10.1073/pnas.1722477115 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Harwood, J. D., Sunderland, K. D. & Symondson, W. O. C. Monoclonal antibodies reveal the potential of the tetragnathid spider Pachygnatha degeeri (Araneae: Tetragnathidae) as an aphid predator. Bull. Entomol. Res. 95, 161–167. https://doi.org/10.1079/BER2004346 (2005).Article 
    CAS 

    Google Scholar 
    Samu, F., Beleznai, O. & Tholt, G. A potential spider natural enemy against virus vector leafhoppers in agricultural mosaic landscapes: Corroborating ecological and behavioral evidence. Biol. Control. 67, 390–396. https://doi.org/10.1016/j.biocontrol.2013.08.016 (2013).Article 

    Google Scholar 
    Biteniekyté, M. & Relys, V. Epigeic spider communities of a peat bog and adjacent habitats. Rev. Iber. Aracnol. 15, 81–87 (2008).
    Google Scholar 
    Michalko, R., Kosulic, O., Hula, V. & Surovcova, K. Niche differentiation of two sibling wolf spider species, Pardosa lugubris and Pardosa alacris, along a canopy openness gradient. J. Arachnol. 44, 46–51 (2016).Article 

    Google Scholar 
    Nyffeler, M. & Birkhofer, K. An estimated 400–800 million tons of prey are annually killed by the global spider community. Naturwissenschaften 104, 30. https://doi.org/10.1007/s00114-017-1440-1 (2017).Article 
    CAS 

    Google Scholar 
    Sohlström, E. H. et al. Future climate and land-use intensification modify arthropod community structure. Agric. Ecosyst. Environ. 327, 107830. https://doi.org/10.1016/j.agee.2021.107830 (2022).Article 
    CAS 

    Google Scholar 
    Sallé, A. et al. Climate change alters temperate forest canopies and indirectly reshapes arthropod communities. Front. For. Glob. Change 4, 710854 (2021).Article 

    Google Scholar 
    Høye, T. T. et al. Nonlinear trends in abundance and diversity and complex responses to climate change in Arctic arthropods. Proc. Natl. Acas. Sci. USA 118, e2002557117 (2021).Article 

    Google Scholar 
    Tscharntke, T., Klein, A. M., Kruess, A., Steffan-Dewenter, I. & Thies, C. Landscape perspectives on agricultural intensification and biodiversity: Ecosystem service management. Ecol. Lett. 8, 857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x (2005).Article 

    Google Scholar 
    Kleijn, D., Rundlöf, M., Scheper, J., Smith, H. G. & Tscharntke, T. Does conservation on farmland contribute to halting the biodiversity decline?. Trends Ecol. Evol. 26, 474–481. https://doi.org/10.1016/j.tree.2011.05.009 (2011).Article 

    Google Scholar 
    Swinbank, A. The European Union’s Common Agricultural Policy (CAP) The New Palgrave Dictionary of Economics 1–9 (Palgrave Macmillan, 2016).
    Google Scholar 
    Wissinger, S. Cyclic colonization in predictably ephemeral habitats: A template for biological control in annual crop systems. Biol. Control 10, 4–15 (1997).Article 

    Google Scholar 
    Samu, F., Szita, É. & Botos, E. Short- and longer-term colonization of alfalfa by spiders: A case study into the succession of perennial fields. In European Arachnology 2008 (eds Nentwig, W. et al.) 153–163 (Natural History Museum, 2010).
    Google Scholar 
    Samu, F., Horváth, A., Neidert, D., Botos, E. & Szita, É. Metacommunities of spiders in grassland habitat fragments of an agricultural landscape. Basic Appl. Ecol. 31, 92–103. https://doi.org/10.1016/j.baae.2018.07.009 (2018).Article 

    Google Scholar  More

  • in

    Asynchrony in coral community structure contributes to reef-scale community stability

    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).
    Google Scholar 
    Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).CAS 

    Google Scholar 
    Harley, C. D. G. Climate change, keystone predation, and biodiversity loss. Science 334, 1124–1127 (2011).ADS 
    CAS 

    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).ADS 

    Google Scholar 
    Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).ADS 
    CAS 

    Google Scholar 
    Moreno-Mateos, D. et al. Anthropogenic ecosystem disturbance and the recovery debt. Nat. Commun. 8, 14163 (2017).ADS 
    CAS 

    Google Scholar 
    Newman, E. A. Disturbance ecology in the Anthropocene. Front. Ecol. Evol. 7, 147 (2019).
    Google Scholar 
    Mittelbach, G. G. et al. What is the observed relationship between species richness and productivity?. Ecology 82, 2381–2396 (2001).
    Google Scholar 
    van Nes, E. H. & Scheffer, M. Implications of spatial heterogeneity for catastrophic regime shifts in ecosystems. Ecology 86, 1797–1807 (2005).
    Google Scholar 
    Tylianakis, J. M. et al. Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. Plos Biol. 6, e122 (2008).
    Google Scholar 
    Loreau, M. et al. In Metacommunities: Spatial Dynamics and Ecological Communities (eds Holyoak, M. et al.) (The University of Chicago Press, 2005).
    Google Scholar 
    Loreau, M. From Populations to Ecosystems (Princeton University Press, 2010). https://doi.org/10.1515/9781400834167.vii.Book 

    Google Scholar 
    Moreira, E. F., Boscolo, D. & Viana, B. F. Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE 10, e0123628 (2015).
    Google Scholar 
    Costanza, J. K., Moody, A. & Peet, R. K. Multi-scale environmental heterogeneity as a predictor of plant species richness. Landsc. Ecol. 26, 851–864 (2011).
    Google Scholar 
    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS 
    CAS 

    Google Scholar 
    Nyström, M., Graham, N. A. J., Lokrantz, J. & Norström, A. V. Capturing the cornerstones of coral reef resilience: Linking theory to practice. Coral Reefs 27, 795–809 (2008).ADS 

    Google Scholar 
    Virah-Sawmy, M., Gillson, L. & Willis, K. J. How does spatial heterogeneity influence resilience to climatic changes? Ecological dynamics in southeast Madagascar. Ecol. Monogr. 79, 557–574 (2009).
    Google Scholar 
    Wilson, D. S. Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 73, 1984–2000 (1992).
    Google Scholar 
    Leibold, M. A. et al. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601–613 (2004).
    Google Scholar 
    Briggs, C. J. & Hoopes, M. F. Stabilizing effects in spatial parasitoid–host and predator–prey models: A review. Theor. Popul. Biol. 65, 299–315 (2004).MATH 

    Google Scholar 
    Wang, S., Haegeman, B. & Loreau, M. Dispersal and metapopulation stability. PeerJ 3, e1295 (2015).
    Google Scholar 
    Tilman, D. The ecological consequences of changes in biodiversity: A search for general principles. Ecology 80, 1455–1474 (1999).
    Google Scholar 
    Loreau, M., Mouquet, N. & Gonzalez, A. Biodiversity as spatial insurance in heterogeneous landscapes. Proc. Natl. Acad. Sci. 100, 12765–12770 (2003).ADS 
    CAS 

    Google Scholar 
    Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl. Acad. Sci. 96, 1463–1468 (1999).ADS 
    CAS 

    Google Scholar 
    Bouvier, T. et al. Contrasted effects of diversity and immigration on ecological insurance in marine bacterioplankton communities. PLoS ONE 7, e37620 (2012).ADS 
    CAS 

    Google Scholar 
    Hammond, M., Loreau, M., Mazancourt, C. & Kolasa, J. Disentangling local, metapopulation, and cross-community sources of stabilization and asynchrony in metacommunities. Ecosphere 11, e03078 (2020).
    Google Scholar 
    Lamy, T., Legendre, P., Chancerelle, Y., Siu, G. & Claudet, J. Understanding the spatio-temporal response of coral reef fish communities to natural disturbances: Insights from beta-diversity decomposition. PLoS ONE 10, e0138696 (2015).
    Google Scholar 
    Lamy, T. et al. Species insurance trumps spatial insurance in stabilizing biomass of a marine macroalgal metacommunity. Ecology 100, e02719 (2019).
    Google Scholar 
    Stier, A. C., Shelton, A. O., Samhouri, J. F., Feist, B. E. & Levin, P. S. Fishing, environment, and the erosion of a population portfolio. Ecosphere https://doi.org/10.1002/ecs2.3283 (2020).Article 

    Google Scholar 
    Burgess, S. C. et al. Beyond connectivity: How empirical methods can quantify population persistence to improve marine protected-area design. Ecol. Appl. 24, 257–270 (2014).
    Google Scholar 
    Saenz-Agudelo, P., Jones, G. P., Thorrold, S. R. & Planes, S. Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc. R. Soc. B Biol. Sci. 278, 2954–2961 (2011).
    Google Scholar 
    Wood, S., Paris, C. B., Ridgwell, A. & Hendy, E. J. Modelling dispersal and connectivity of broadcast spawning corals at the global scale. Glob. Ecol. Biogeogr. 23, 1–11 (2014).
    Google Scholar 
    Loreau, M. et al. Biodiversity as insurance: From concept to measurement and application. Biol. Rev. https://doi.org/10.1111/brv.12756 (2021).Article 

    Google Scholar 
    Thibaut, L. M. & Connolly, S. R. Understanding diversity–stability relationships: Towards a unified model of portfolio effects. Ecol. Lett. 16, 140–150 (2013).
    Google Scholar 
    Wilcox, K. R. et al. Asynchrony among local communities stabilises ecosystem function of metacommunities. Ecol. Lett. 20, 1534–1545 (2017).
    Google Scholar 
    Loreau, M. & de Mazancourt, C. Species synchrony and its drivers: Neutral and nonneutral community dynamics in fluctuating environments. Am. Nat. 172, E48–E66 (2008).
    Google Scholar 
    Loreau, M. & Mazancourt, C. Biodiversity and ecosystem stability: A synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).
    Google Scholar 
    Gross, K. et al. Species richness and the temporal stability of biomass production: A new analysis of recent biodiversity experiments. Am. Nat. 183, 1–12 (2014).
    Google Scholar 
    Sullaway, G. H., Shelton, A. O. & Samhouri, J. F. Synchrony erodes spatial portfolios of an anadromous fish and alters availability for resource users. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13575 (2021).Article 

    Google Scholar 
    Adjeroud, M., Augustin, D., Galzin, R. & Salvat, B. Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Mar. Ecol. Prog. Ser. 237, 121–131 (2002).ADS 

    Google Scholar 
    Adjeroud, M. et al. Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28, 775–780 (2009).ADS 

    Google Scholar 
    Pratchett, M. S., Trapon, M., Berumen, M. L. & Chong-Seng, K. Recent Disturbances Augment Community Shifts in Coral Assemblages in Moorea, French Polynesia (SpringerLink, 2011). https://doi.org/10.1007/s00338-010-0678-2.Book 

    Google Scholar 
    Kayal, M. et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7, e47363 (2012).ADS 
    CAS 

    Google Scholar 
    McWilliam, M., Pratchett, M. S., Hoogenboom, M. O. & Hughes, T. P. Deficits in functional trait diversity following recovery on coral reefs. Proc. R. Soc. B 287, 20192628 (2020).
    Google Scholar 
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).ADS 
    CAS 

    Google Scholar 
    Penin, L., Adjeroud, M., Schrimm, M. & Lenihan, H. S. High spatial variability in coral bleaching around Moorea (French Polynesia): Patterns across locations and water depths. C. R. Biol. 330, 171–181 (2007).
    Google Scholar 
    Adam, T. C. et al. Herbivory, connectivity, and ecosystem resilience: Response of a coral reef to a large-scale perturbation. PLoS ONE 6, e23717 (2011).ADS 
    CAS 

    Google Scholar 
    Edmunds, P. et al. Why more comparative approaches are required in time-series analyses of coral reef ecosystems. Mar. Ecol. Prog. Ser. 608, 297–306 (2019).ADS 

    Google Scholar 
    Pérez-Rosales, G. et al. Documenting decadal disturbance dynamics reveals archipelago-specific recovery and compositional change on Polynesian reefs. Mar. Pollut. Bull. 170, 112659 (2021).
    Google Scholar 
    Bruno, J. F. & Selig, E. R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2, e711 (2007).ADS 

    Google Scholar 
    Jackson, J. B. C. et al. Status and trends of Caribbean coral reefs. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland (2014)Edmunds, P. J. Implications of high rates of sexual recruitment in driving rapid reef recovery in Mo’orea, French Polynesia. Sci. Rep. 8, 16615 (2018).ADS 

    Google Scholar 
    Burgess, S. C., Johnston, E. C., Wyatt, A. S. J., Leichter, J. J. & Edmunds, P. J. Response diversity in corals: Hidden differences in bleaching mortality among cryptic Pocillopora species. Ecology https://doi.org/10.1002/ecy.3324 (2021).Article 

    Google Scholar 
    Holbrook, S. J. et al. Recruitment drives spatial variation in recovery rates of resilient coral reefs. Sci. Rep. 8, 7338 (2018).ADS 

    Google Scholar 
    Guest, J. R. et al. A framework for identifying and characterising coral reef “oases” against a backdrop of degradation. J. Appl. Ecol. 55, 2865–2875 (2018).
    Google Scholar 
    Hench, J. L., Leichter, J. J. & Monismith, S. G. Episodic circulation and exchange in a wave-driven coral reef and lagoon system. Limnol. Oceanogr. 53, 2681–2694 (2008).ADS 

    Google Scholar 
    Barry, J. P. & Dayton, P. K. Ecological heterogeneity. Ecol. Stud. https://doi.org/10.1007/978-1-4612-3062-5_14 (1991).Article 

    Google Scholar 
    Edmunds, P. & Bruno, J. The importance of sampling scale in ecology: Kilometer-wide variation in coral reef communities. Mar. Ecol. Prog. Ser. 143, 165–171 (1996).ADS 

    Google Scholar 
    Lough, J. M., Anderson, K. D. & Hughes, T. P. Increasing thermal stress for tropical coral reefs: 1871–2017. Sci. Rep. 8, 6079 (2018).ADS 
    CAS 

    Google Scholar 
    van Oppen, M. J. H. & Lough, J. M. Coral bleaching, patterns, processes, causes and consequences. Ecol. Stud. https://doi.org/10.1007/978-3-319-75393-5_14 (2018).Article 

    Google Scholar 
    Monismith, S. G. Hydrodynamics of coral reefs. Annu. Rev. Fluid Mech. 39, 37–55 (2007).ADS 
    MATH 

    Google Scholar 
    Edmunds P. Of Moorea Coral Reef LTER. MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Corals, ongoing since 2005. knb-lter-mcr.4.33 https://doi.org/10.6073/pasta/1f05f1f52a2759dc096da9c24e88b1e8 (2020).Cowles, J. et al. Resilience: insights from the U.S. Long-term ecological research network. Ecosphere 12, e03434 (2021).
    Google Scholar 
    Beijbom, O. et al. Towards automated annotation of benthic survey images: Variability of human experts and operational modes of automation. PLoS ONE 10, e0130312 (2015).
    Google Scholar 
    Veron, J. E. N. Corals of the world, v. 1–3. Australian Institute of Marine Science (2000)Washburn, L of Moorea Coral Reef LTER. MCR LTER: Coral Reef: Ocean Currents and Biogeochemistry: salinity, temperature and current at CTD and ADCP mooring FOR01 from 2004 ongoing. knb-lter-mcr.30.36doi:10.6073/pasta/124d19950c5234bf1937661989dcced7 (2021).Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).ADS 

    Google Scholar 
    Dean, R. G. & Dalrymple, R. A. Water Wave Mechanics for Engineers and Scientists. Advanced Series on Ocean Engineering Vol. 2 (World Scientific, 1991).
    Google Scholar 
    Carroll, A., Harrison, P. & Adjeroud, M. Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25, 93–97 (2006).ADS 

    Google Scholar 
    Han, X., Adam, T. C., Schmitt, R. J., Brooks, A. J. & Holbrook, S. J. Response of herbivore functional groups to sequential perturbations in Moorea, French Polynesia. Coral Reefs 35, 999–1009 (2016).ADS 

    Google Scholar 
    Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Austral Ecol. 18, 117–143 (1993).
    Google Scholar 
    Clarke, K. R., Somerfield, P. J. & Chapman, M. G. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330, 55–80 (2006).
    Google Scholar 
    RStudio Team. RStudio: Integrated development for R. RStudio, PBC, Boston, MA URL http://www.rstudio.com/ (2021).Oksanen J. et al. vegan: Community ecology package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan (2020).Wickham, et al. Welcome to the Tidyverse. J. Open Source Softw. 4(43), 1686. https://doi.org/10.21105/joss.01686 (2019).Article 
    ADS 

    Google Scholar 
    Corlett, R. T. The Anthropocene concept in ecology and conservation. Trends Ecol. Evol. 30, 36–41 (2015).
    Google Scholar 
    Williams, G. J. et al. Coral reef ecology in the Anthropocene. Funct. Ecol. 33, 1014–1022 (2019).
    Google Scholar 
    Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS 
    CAS 

    Google Scholar 
    Walther, G.-R. Community and ecosystem responses to recent climate change. Philos. Trans. R. Soc. B Biol. Sci. 365, 2019–2024 (2010).
    Google Scholar 
    Cinner, J. E. et al. Bright spots among the world’s coral reefs. Nature 535, 416–419 (2016).ADS 
    CAS 

    Google Scholar 
    Grman, E., Lau, J. A., Schoolmaster, D. R. & Gross, K. L. Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecol. Lett. 13, 1400–1410 (2010).
    Google Scholar 
    Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010).ADS 
    CAS 

    Google Scholar 
    Doak, D. F. et al. The statistical inevitability of stability-diversity relationships in community ecology. Am. Nat. 151, 264–276 (1998).CAS 

    Google Scholar 
    Isbell, F. I., Polley, H. W. & Wilsey, B. J. Biodiversity, productivity and the temporal stability of productivity: Patterns and processes. Ecol. Lett. 12, 443–451 (2009).
    Google Scholar 
    Connell, J. H. Diversity in tropical rain forests and coral reefs author. Science 199, 1302–1310 (1978).ADS 
    CAS 

    Google Scholar 
    Plaisance, L., Caley, M. J., Brainard, R. E. & Knowlton, N. The diversity of coral reefs: What are we missing?. PLoS ONE 6, e25026 (2011).ADS 
    CAS 

    Google Scholar 
    Williams, G. J. et al. Biophysical drivers of coral trophic depth zonation. Mar. Biol. 165, 60 (2018).
    Google Scholar 
    Moritz, C. et al. Long-term monitoring of benthic communities reveals spatial determinants of disturbance and recovery dynamics on coral reefs. Mar. Ecol. Prog. Ser. 672, 141–152 (2021).ADS 

    Google Scholar 
    Dietzel, A. et al. The spatial footprint and patchiness of large scale disturbances on coral reefs. Global Change Biol. 27, 4825–4838 (2021).CAS 

    Google Scholar 
    Leichter, J. et al. Biological and physical interactions on a tropical island coral reef: Transport and retention processes on Moorea, French Polynesia. Oceanography 26, 52–63 (2011).
    Google Scholar 
    Porter, J. W. et al. Population trends among Jamaican reef corals. Nature 294, 249–250 (1981).ADS 

    Google Scholar 
    Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).ADS 
    CAS 

    Google Scholar 
    Whittaker, R. H. & Levin, S. A. The role of mosaic phenomena in natural communities. Theor. Popul. Biol. 12, 117–139 (1977).CAS 

    Google Scholar 
    Karlson, R. H. & Hurd, L. E. Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs 12, 117–125 (1993).ADS 

    Google Scholar 
    Stoddart, D. R. Effects of Hurricane Hattie on the British Honduras reefs and cays, October 30–31, 1961. Atoll Res. Bull. 95, 1–142 (1963).
    Google Scholar 
    Witman, J. D. Physical disturbance and community structure of exposed and protected reefs: A case study from St. John U.S. Virgin Islands. Integr. Comp. Biol. 32, 641–654 (1992).
    Google Scholar 
    Thorson, J. T., Scheuerell, M. D., Olden, J. D. & Schindler, D. E. Spatial heterogeneity contributes more to portfolio effects than species variability in bottom-associated marine fishes. Proc. R. Soc. B 285, 20180915 (2018).
    Google Scholar 
    Mellin, C., MacNeil, M. A., Cheal, A. J., Emslie, M. J. & Caley, M. J. Marine protected areas increase resilience among coral reef communities. Ecol. Lett. 19, 629–637 (2016).
    Google Scholar 
    Beyer, H. L. et al. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 11, e12587 (2018).
    Google Scholar 
    Harrison, H. B., Bode, M., Williamson, D. H., Berumen, M. L. & Jones, G. P. A connectivity portfolio effect stabilizes marine reserve performance. Proc. Natl. Acad. Sci. 117, 25595–25600 (2020).ADS 
    CAS 

    Google Scholar 
    Walter, J. A. et al. The spatial synchrony of species richness and its relationship to ecosystem stability. Ecology https://doi.org/10.1002/ecy.3486 (2021).Article 

    Google Scholar 
    Wang, S., Lamy, T., Hallett, L. M. & Loreau, M. Stability and synchrony across ecological hierarchies in heterogeneous metacommunities: Linking theory to data. Ecography 42, 1200–1211 (2019).
    Google Scholar 
    Catano, C. P., Fristoe, T. S., LaManna, J. A. & Myers, J. A. Local species diversity, β-diversity and climate influence the regional stability of bird biomass across North America. Proc. R. Soc. B 287, 20192520 (2020).
    Google Scholar 
    Roscher, C. et al. Identifying population- and community-level mechanisms of diversity–stability relationships in experimental grasslands. J. Ecol. 99, 1460–1469 (2011).
    Google Scholar 
    Downing, A. L., Brown, B. L. & Leibold, M. A. Multiple diversity–stability mechanisms enhance population and community stability in aquatic food webs. Ecology 95, 173–184 (2014).
    Google Scholar 
    Moran, P. The statistical analysis of the Canadian Lynx cycle. Aust. J. Zool. 1, 291–298 (1953).
    Google Scholar 
    Townsend, D. L. & Gouhier, T. C. Spatial and interspecific differences in recruitment decouple synchrony and stability in trophic metacommunities. Theor. Ecol. 12, 319–327 (2019).
    Google Scholar 
    Yeager, M. E., Gouhier, T. C. & Hughes, A. R. Predicting the stability of multitrophic communities in a variable world. Ecology 101, e02992 (2020).
    Google Scholar 
    Hughes, T. P. et al. Emergent properties in the responses of tropical corals to recurrent climate extremes. Curr. Biol. https://doi.org/10.1016/j.cub.2021.10.046 (2021).Article 

    Google Scholar 
    Jackson, J. B. C. Morphological strategies of sessile animals. In Biology and Systematics of Colonial Organisms (eds Larwood, G. & Rosen, B. R.) 499–555 (Academic, 1979).
    Google Scholar 
    Sammarco, P. W. & Andrews, J. C. Localized dispersal and recruitment in Great Barrier Reef Corals: The helix experiment. Science 239, 1422–1424 (1988).ADS 
    CAS 

    Google Scholar 
    Edmunds, P. J. Unusually high coral recruitment during the 2016 El Niño in Mo’orea, French Polynesia. PLoS ONE 12, e0185167 (2017).
    Google Scholar 
    Bull, G. Distribution and abundance of coral plankton. Coral Reefs 4, 197–200 (1986).ADS 

    Google Scholar 
    Hodgson, G. Abundance and distribution of planktonic coral larvae in Kaneohe Bay, Oahu, Hawaii. Mar. Ecol. Prog. Ser. 26, 61–71 (1985).ADS 

    Google Scholar 
    Edmunds, P. J. Vital rates of small reef corals are associated with variation in climate. Limnol. Oceanogr. 66, 901–913 (2021).ADS 

    Google Scholar  More

  • in

    Integrated biochar solutions can achieve carbon-neutral staple crop production

    Martin-Roberts, E. et al. Carbon capture and storage at the end of a lost decade. One Earth 4, 1569–1584 (2021).Article 
    ADS 

    Google Scholar 
    Liu, Z. et al. Challenges and opportunities for carbon neutrality in China. Nat. Rev. Earth Environ. 3, 141–155 (2022).Article 
    ADS 

    Google Scholar 
    Wang, F. et al. Technologies and perspectives for achieving carbon neutrality. Innovation 2, 100180 (2021).CAS 

    Google Scholar 
    Third National Communication of Climate Change in the People’s Republic of China (Ministry of Ecology and Environment of the People’s Republic of China, 2018).Chen, X. et al. Producing more grain with lower environmental costs. Nature 514, 486–489 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Cui, Z. et al. Pursuing sustainable productivity with millions of smallholder farmers. Nature 555, 363–366 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Liu, B. et al. Promoting potato as staple food can reduce the carbon–land–water impacts of crops in China. Nat. Food 2, 570–577 (2021).Article 

    Google Scholar 
    Jiang, Y. et al. Water management to mitigate the global warming potential of rice systems: a global meta-analysis. Field Crops Res. 234, 47–54 (2019).Article 

    Google Scholar 
    Shang, Z. et al. Can cropland management practices lower net greenhouse emissions without compromising yield? Glob. Change Biol. 27, 4657–4670 (2021).Article 
    CAS 

    Google Scholar 
    Xia, L. et al. Can knowledge-based N management produce more staple grain with lower greenhouse gas emission and reactive nitrogen pollution? A meta-analysis. Glob. Change Biol. 23, 1917–1925 (2016).Article 
    ADS 

    Google Scholar 
    Ju, X. et al. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc. Natl Acad. Sci. USA 106, 3041–3046 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Wang, B. et al. Four pathways towards carbon neutrality by controlling net greenhouse gas emissions in Chinese cropland. Resour. Conserv. Recycl. 186, 106576 (2022).Article 
    CAS 

    Google Scholar 
    Xia, L. et al. Trade-offs between soil carbon sequestration and reactive nitrogen losses under straw return in global agroecosystems. Glob. Change Biol. 12, 5919–5932 (2018).Article 

    Google Scholar 
    Zhao, Y. et al. Economics- and policy-driven organic carbon input enhancement dominates soil organic carbon accumulation in Chinese croplands. Proc. Natl Acad. Sci. USA 115, 4045–4050 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Yan, X., Akiyama, H., Yagi, K. & Akimoto, H. Global estimations of the inventory and mitigation potential of methane emissions from rice cultivation conducted using the 2006 Intergovernmental Panel on Climate Change guidelines. Glob. Biogeochemical Cycles 23, GB2002 (2009).Jiang, Y. et al. Acclimation of methane emissions from rice paddy fields to straw addition. Sci. Adv. 5, eaau9038 (2019).Article 
    ADS 

    Google Scholar 
    Chen, Z. et al. Microbial process-oriented understanding of stimulation of soil N2O emission following the input of organic materials. Environ. Pollut. 284, 117176 (2021).Article 
    CAS 

    Google Scholar 
    Lugato, E., Leip, A. & Jones, A. Mitigation potential of soil carbon management overestimated by neglecting N2O emissions. Nat. Clim. Change 8, 219–223 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Xia, L., Wang, S. & Yan, X. Effects of long-term straw incorporation on the net global warming potential and the net economic benefit in a rice-wheat cropping system in China. Agric. Ecosyst. Environ. 197, 118–127 (2014).Article 

    Google Scholar 
    Xia, L., Ti, C., Li, B., Xia, Y. & Yan, X. Greenhouse gas emissions and reactive nitrogen releases during the life-cycles of staple food production in China and their mitigation potential. Sci. Total Environ. 556, 116–125 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Yang, Y. et al. Restoring abandoned farmland to mitigate climate change on a full Earth. One Earth 3, 176–186 (2020).Article 
    ADS 

    Google Scholar 
    Lehmann, J. et al. Biochar in climate change mitigation. Nat. Geosci. 14, 883–892 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Woolf, D., Amonette, J. E., Street-Perrott, F. A., Lehmann, J. & Joseph, S. Sustainable biochar to mitigate global climate change. Nat. Commun. 1, 56 (2010).Article 
    ADS 

    Google Scholar 
    Jeffery, S., Verheijen, F. G., Kammann, C. & Abalos, D. Biochar effects on methane emissions from soils: a meta-analysis. Soil Biol. Biochem. 101, 251–258 (2016).Article 
    CAS 

    Google Scholar 
    Schmidt, H. P. et al. Biochar in agriculture – a systematic review of 26 global meta-analyses. GCB Bioenergy 13, 1708–1730 (2021).Article 
    CAS 

    Google Scholar 
    Cayuela, M. L. et al. Biochar and denitrification in soils: when, how much and why does biochar reduce N2O emissions? Sci. Rep. 3, 1732 (2013).Article 

    Google Scholar 
    He, Y. et al. Effects of biochar application on soil greenhouse gas fluxes: a meta-analysis. GCB Bioenergy 9, 743–755 (2017).Article 
    CAS 

    Google Scholar 
    Liu, Q. et al. Biochar application as a tool to decrease soil nitrogen losses (NH3 volatilization, N2O emissions, and N leaching) from croplands: options and mitigation strength in a global perspective. Glob. Change Biol. 25, 2077–2093 (2019).Article 
    ADS 

    Google Scholar 
    He, X. et al. Effects of pyrolysis temperature on the physicochemical properties of gas and biochar obtained from pyrolysis of crop residues. Energy 143, 746–756 (2018).Article 
    CAS 

    Google Scholar 
    Yang, Q. et al. Prospective contributions of biomass pyrolysis to China’s 2050 carbon reduction and renewable energy goals. Nat. Commun. 12, 1698 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Smith, P. et al. Biophysical and economic limits to negative CO2 emissions. Nat. Clim. Change 6, 42–50 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    IPCC Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) (WMO, 2018).Ritchie, H., Roser, M. & Rosado, P. CO2 and Greenhouse Gas Emissions (Our World in Data, 2020); https://ourworldindata.org/co2-and-other-greenhouse-gas-emissionsLiu, Y. et al. A quantitative review of the effects of biochar application on rice yield and nitrogen use efficiency in paddy fields: a meta-analysis. Sci. Total Environ. 830, 154792 (2022).Article 
    ADS 
    CAS 

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

    Google Scholar 
    Gu, B. et al. Abating ammonia is more cost-effective than nitrogen oxides for mitigating PM2.5 air pollution. Science 374, 758–762 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Yang, Y., Reilly, E. C., Jungers, J. M., Chen, J. & Smith, T. M. Climate benefits of increasing plant diversity in perennial bioenergy crops. One Earth 1, 434–445 (2019).Article 
    ADS 

    Google Scholar 
    Weller, S. et al. Methane and nitrous oxide emissions from rice and maize production in diversified rice cropping systems. Nutr. Cycling Agroecosyst. 101, 37–53 (2015).Article 
    CAS 

    Google Scholar 
    Rogelj, J. et al. Scenarios towards limiting global mean temperature increase below 1.5 °C. Nat. Clim. Change 8, 325–332 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Gu, B., Zhang, X., Bai, X., Fu, B. & Chen, D. Four steps to food security for swelling cities. Nature 566, 31–33 (2019).Article 
    ADS 
    CAS 

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

    Google Scholar 
    Gu, B., Ju, X., Chang, J., Ge, Y. & Vitousek, P. M. Integrated reactive nitrogen budgets and future trends in China. Proc. Natl Acad. Sci. USA 112, 8792–8797 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).Article 
    ADS 
    CAS 

    Google Scholar 
    Lee, X. J., Ong, H. C., Gan, Y. Y., Chen, W. H. & Mahlia, T. M. I. State of art review on conventional and advanced pyrolysis of macroalgae and microalgae for biochar, bio-oil and bio-syngas production. Energy Convers. Manag. 210, 112707 (2020).Article 
    CAS 

    Google Scholar 
    Nevzorova, T. & Kutcherov, V. Barriers to the wider implementation of biogas as a source of energy: a state-of-the-art review. Energy Strategy Rev. 26, 100414 (2019).Article 

    Google Scholar 
    Xia, S. et al. Pyrolysis behavior and economics analysis of the biomass pyrolytic polygeneration of forest farming waste. Bioresource Technol. 270, 189–197 (2018).Article 
    CAS 

    Google Scholar 
    Liu, Z., Niu, W., Chu, H., Zhou, T. & Niu, Z. Effect of the carbonization temperature on the properties of biochar produced from the pyrolysis of crop residues. BioResources 13, 3429–3446 (2018).Article 
    CAS 

    Google Scholar 
    Hengeveld, E. J., Bekkering, J., van Gemert, W. J. T. & Broekhuis, A. A. Biogas infrastructures from farm to regional scale, prospects of biogas transport grids. Biomass Bioenergy 86, 43–52 (2016).Article 

    Google Scholar 
    Ansari, S. H. et al. Incorporation of solar-thermal energy into a gasification process to co-produce bio-fertilizer and power. Environ. Pollut. 266, 115103 (2020).Article 
    CAS 

    Google Scholar 
    Yang, S. I., Wu, M. S. & Hsu, T. C. Spray combustion characteristics of kerosene/bio-oil part I: experimental study. Energy 119, 26–36 (2017).Article 
    CAS 

    Google Scholar 
    Xia, L. et al. Elevated CO2 negates O3 impacts on terrestrial carbon and nitrogen cycles. One Earth 4, 1752–1763 (2022).Article 
    ADS 

    Google Scholar 
    Gu, B. et al. Atmospheric reactive nitrogen in China: sources, recent trends, and damage costs. Environ. Sci. Technol. 46, 9420–9427 (2012).Article 
    ADS 
    CAS 

    Google Scholar 
    Xia, L. et al. Greenhouse gas emissions and reactive nitrogen releases from rice production with simultaneous incorporation of wheat straw and nitrogen fertilizer. Biogeosciences 13, 4569–4579 (2016).Article 
    ADS 
    CAS 

    Google Scholar  More

  • in

    Global patterns of water storage in the rooting zones of vegetation

    Teuling, A. J., Seneviratne, S. I., Williams, C. & Troch, P. A. Observed timescales of evapotranspiration response to soil moisture. Geophys. Res. Lett. 33, L23403 (2006).Gao, H. et al. Climate controls how ecosystems size the root zone storage capacity at catchment scale. Geophys. Res. Lett. 41, 7916–7923 (2014).Article 

    Google Scholar 
    Milly, P. C. D. Climate, soil water storage, and the average annual water balance. Water Resour. Res. 30, 2143–2156 (1994).Article 

    Google Scholar 
    Hahm, W. J. et al. Low subsurface water storage capacity relative to annual rainfall decouples Mediterranean plant productivity and water use from rainfall variability. Geophys. Res. Lett. 46, 6544–6553 (2019).Article 

    Google Scholar 
    Seneviratne, S. I. et al. Investigating soil moisture–climate interactions in a changing climate: a review. Earth Sci. Rev. 99, 125–161 (2010).Article 

    Google Scholar 
    Thompson, S. E. et al. Comparative hydrology across AmeriFlux sites: the variable roles of climate, vegetation, and groundwater. Water Resour. Res. 47, W00J07 (2011).Fan, Y., Miguez-Macho, G., Jobbágy, E. G., Jackson, R. B. & Otero-Casal, C. Hydrologic regulation of plant rooting depth. Proc. Natl Acad. Sci. USA 114, 10572–10577 (2017).Article 

    Google Scholar 
    Hain, C. R., Crow, W. T., Anderson, M. C. & Tugrul Yilmaz, M. Diagnosing neglected soil moisture source–sink processes via a thermal infrared-based two-source energy balance model. J. Hydrometeorol. 16, 1070–1086 (2015).Article 

    Google Scholar 
    Rempe, D. M. & Dietrich, W. E. Direct observations of rock moisture, a hidden component of the hydrologic cycle. Proc. Natl Acad. Sci. USA 115, 2664–2669 (2018).Article 

    Google Scholar 
    Dawson, T. E., Jesse Hahm, W. & Crutchfield-Peters, K. Digging deeper: what the critical zone perspective adds to the study of plant ecophysiology. N. Phytol. 226, 666–671 (2020).Article 

    Google Scholar 
    McCormick, E. L. et al. Widespread woody plant use of water stored in bedrock. Nature 597, 225–229 (2021).Article 

    Google Scholar 
    Maxwell, R. M. & Condon, L. E. Connections between groundwater flow and transpiration partitioning. Science 353, 377–380 (2016).Article 

    Google Scholar 
    Schlemmer, L., Schär, C., Lüthi, D. & Strebel, L. A groundwater and runoff formulation for weather and climate models. J. Adv. Model. Earth Syst. 10, 1809–1832 (2018).Article 

    Google Scholar 
    Teuling, A. J. et al. Contrasting response of European forest and grassland energy exchange to heatwaves. Nat. Geosci. 3, 722–727 (2010).Article 

    Google Scholar 
    Koirala, S. et al. Global distribution of groundwater–vegetation spatial covariation. Geophys. Res. Lett. 44, 4134–4142 (2017).Article 

    Google Scholar 
    Esteban, E. J. L., Castilho, C. V., Melgaço, K. L. & Costa, F. R. C. The other side of droughts: wet extremes and topography as buffers of negative drought effects in an Amazonian forest. N. Phytol. 229, 1995–2006 (2021).Article 

    Google Scholar 
    Liu, Y., Konings, A. G., Kennedy, D. & Gentine, P. Global coordination in plant physiological and rooting strategies in response to water stress. Glob. Biogeochem. Cycles 35, e2020GB006758 (2021).Article 

    Google Scholar 
    Schenk, H. J. & Jackson, R. B. The global biogeography of roots. Ecol. Monogr. 72, 311–328 (2002).Article 

    Google Scholar 
    Canadell, J. et al. Maximum rooting depth of vegetation types at the global scale. Oecologia 108, 583–595 (1996).Article 

    Google Scholar 
    Weaver, J. E. & Darland, R. W. Soil–root relationships of certain native grasses in various soil types. Ecol. Monogr. 19, 303–338 (1949).Article 

    Google Scholar 
    Chitra-Tarak, R. et al. Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest. N. Phytol. 231, 1798–1813 (2021).Article 

    Google Scholar 
    Schenk, H. J. & Jackson, R. B. Mapping the global distribution of deep roots in relation to climate and soil characteristics. Geoderma 126, 129–140 (2005).Article 

    Google Scholar 
    Franklin, O. et al. Organizing principles for vegetation dynamics. Nat. Plants 6, 444–453 (2020).Article 

    Google Scholar 
    Kleidon, A. & Heimann, M. A method of determining rooting depth from a terrestrial biosphere model and its impacts on the global water and carbon cycle. Glob. Change Biol. 4, 275–286 (1998).Article 

    Google Scholar 
    Schymanski, S. J., Sivapalan, M., Roderick, M. L., Hutley, L. B. & Beringer, J. An optimality-based model of the dynamic feedbacks between natural vegetation and the water balance. Water Resour. Res. 45, W01412 (2009).Wang-Erlandsson, L. et al. Global root zone storage capacity from satellite-based evaporation. Hydrol. Earth Syst. Sci. 20, 1459–1481 (2016).Article 

    Google Scholar 
    Knapp, A. K. & Smith, M. D. Variation among biomes in temporal dynamics of aboveground primary production. Science 291, 481–484 (2001).Article 

    Google Scholar 
    Anderson, M. A two-source time-integrated model for estimating surface fluxes using thermal infrared remote sensing. Remote Sens. Environ. 60, 195–216 (1997).Article 

    Google Scholar 
    Hain, C. R. & Anderson, M. C. Estimating morning change in land surface temperature from MODIS day/night observations: applications for surface energy balance modeling. Geophys. Res. Lett. 44, 9723–9733 (2017).Article 

    Google Scholar 
    Tumber-Dávila, S. J., Schenk, H. J., Du, E. & Jackson, R. B. Plant sizes and shapes above- and belowground and their interactions with climate. New Phytol. https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.18031 (2022).Harmonized World Soil Database Version 1.0 (FAO, 2008).Wieder, W. Regridded Harmonized World Soil Database Version 1.2 (ORNL DAAC, 2014); https://doi.org/10.3334/ORNLDAAC/1247Balland, V., Pollacco, J. A. P. & Arp, P. A. Modeling soil hydraulic properties for a wide range of soil conditions. Ecol. Model. 219, 300–316 (2008).Article 

    Google Scholar 
    Agee, E. et al. Root lateral interactions drive water uptake patterns under water limitation. Adv. Water Resour. 151, 103896 (2021).Article 

    Google Scholar 
    Krakauer, N. Y., Li, H. & Fan, Y. Groundwater flow across spatial scales: importance for climate modeling. Environ. Res. Lett. 9, 034003 (2014).Article 

    Google Scholar 
    Stoy, P. C. et al. Reviews and syntheses: turning the challenges of partitioning ecosystem evaporation and transpiration into opportunities. Biogeosciences 16, 3747–3775 (2019).Article 

    Google Scholar 
    Jackson, R. B., Moore, L. A., Hoffmann, W. A., Pockman, W. T. & Linder, C. R. Ecosystem rooting depth determined with caves and DNA. Proc. Natl Acad. Sci. USA 96, 11387–11392 (1999).Article 

    Google Scholar 
    Pelletier, J. D. et al. A gridded global data set of soil, intact regolith, and sedimentary deposit thicknesses for regional and global land surface modeling. J. Adv. Model. Earth Syst. 8, 41–65 (2016).Article 

    Google Scholar 
    Parmesan, C. & Hanley, M. E. Plants and climate change: complexities and surprises. Ann. Bot. 116, 849–864 (2015).Article 

    Google Scholar 
    Pendergrass, A. G., Knutti, R., Lehner, F., Deser, C. & Sanderson, B. M. Precipitation variability increases in a warmer climate. Sci. Rep. 7, 17966 (2017).Siebert, S. et al. Development and validation of the global map of irrigation areas. Hydrol. Earth Syst. Sci. 9, 535–547 (2005).Article 

    Google Scholar 
    Friedl, M. A. et al. MODIS Collection 5 global land cover: Algorithm refinements and characterization of new datasets. Remote Sens. Environ. 114, 168–182 (2010).Article 

    Google Scholar 
    Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51, 933–938 (2001).Article 

    Google Scholar 
    Mu, Q., Heinsch, F. A., Zhao, M. & Running, S. W. Development of a global evapotranspiration algorithm based on MODIS and global meteorology data. Remote Sens. Environ. 111, 519–536 (2007).Article 

    Google Scholar 
    Fisher, J. B. et al. ECOSTRESS: NASA’s next generation mission to measure evapotranspiration from the international space station. Water Resour. Res. 56, e2019WR026058 (2020).Article 

    Google Scholar 
    Davis, T. W. et al. Simple process-led algorithms for simulating habitats (SPLASH v.1.0): robust indices of radiation, evapotranspiration and plant-available moisture. Geosci. Model Dev. 10, 689–708 (2017).Article 

    Google Scholar 
    Weedon, G. P. et al. The WFDEI meteorological forcing data set: WATCH forcing data methodology applied to ERA-Interim reanalysis data. Water Resour. Res. 50, 7505–7514 (2014).Article 

    Google Scholar 
    Orth, R., Koster, R. D. & Seneviratne, S. I. Inferring soil moisture memory from streamflow observations using a simple water balance model. J. Hydrometeorol. 14, 1773–1790 (2013).Article 

    Google Scholar 
    Stocker, B. cwd v.1.0: R package for cumulative water deficit calculation. Zenodo https://doi.org/10.5281/zenodo.5359053 (2021).Zhang, Y. et al. Model-based analysis of the relationship between sun-induced chlorophyll fluorescence and gross primary production for remote sensing applications. Remote Sens. Environ. 187, 145–155 (2016).Article 

    Google Scholar 
    Duveiller, G. et al. A spatially downscaled sun-induced fluorescence global product for enhanced monitoring of vegetation productivity. Earth Syst. Sci. Data 12, 1101–1116 (2020).Article 

    Google Scholar 
    Joiner, J. et al. Global monitoring of terrestrial chlorophyll fluorescence from moderate-spectral-resolution near-infrared satellite measurements: methodology, simulations, and application to GOME-2. Atmos. Meas. Tech. 6, 2803–2823 (2013).Article 

    Google Scholar 
    Köhler, P., Guanter, L. & Joiner, J. A linear method for the retrieval of sun-induced chlorophyll fluorescence from GOME-2 and SCIAMACHY data. Atmos. Meas. Tech. 8, 2589–2608 (2015).Article 

    Google Scholar 
    Jiang, B. et al. Validation of the surface daytime net radiation product from version 4.0 GLASS product suite. IEEE Geosci. Remote Sens. Lett. 16, 509–513 (2019).Article 

    Google Scholar 
    Muggeo, V. M. R. Estimating regression models with unknown break-points. Stat. Med. 22, 3055–3071 (2003).Article 

    Google Scholar 
    Gilleland, E. & Katz, R. W. extRemes 2.0: an extreme value analysis package in R. J. Stat. Softw. 72, 1–39 (2016).Marthews, T. R., Dadson, S. J., Lehner, B., Abele, S. & Gedney, N. High-resolution global topographic index values for use in large-scale hydrological modelling. Hydrol. Earth Syst. Sci. 19, 91–104 (2015).Article 

    Google Scholar 
    Etopo1, Global 1 Arc-Minute Ocean Depth and Land Elevation from the US National Geophysical Data Center (NGDC) (National Geophysical Data Center, NESDIS, NOAA and US Department of Commerce, 2011); https://doi.org/10.5065/D69Z92Z5Beven, K. J. & Kirkby, M. J. A physically based, variable contributing area model of basin hydrology. Hydrol. Sci. J. 24, 43–69 (1979).Article 

    Google Scholar 
    Hansen, M. C., Townshend, J. R. G., DeFries, R. S. & Carroll, M. Estimation of tree cover using MODIS data at global, continental and regional/local scales. Int. J. Remote Sens. 26, 4359–4380 (2005).Article 

    Google Scholar 
    Stocker, B. D. Global rooting zone water storage capacity and rooting depth estimates. Zenodo https://doi.org/10.5281/zenodo.5515246 (2021).Stocker, B. stineb/mct: v3.0: re-submission to Nature Geoscience. Zenodo https://doi.org/10.5281/zenodo.6239187 (2022). More

  • in

    The applicability of species sensitivity distributions to the development of generic doses for phytosanitary irradiation

    Pimentel, D., Zuniga, R. & Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. https://doi.org/10.1016/j.ecolecon.2004.10.002 (2005).Article 

    Google Scholar 
    Linders, T. E. W. et al. Direct and indirect effects of invasive species: Biodiversity loss is a major mechanism by which an invasive tree affects ecosystem functioning. J. Ecol. https://doi.org/10.1111/1365-2745.13268 (2019).Article 

    Google Scholar 
    Campbell, F. T. The science of risk assessment for phytosanitary regulation and the impact of changing trade regulations. Bioscience https://doi.org/10.1641/0006-3568(2001)051[0148:TSORAF]2.0.CO;2 (2001).Article 

    Google Scholar 
    Paini, D. R. et al. Global threat to agriculture from invasive species. Proc. Natl. Acad. Sci. U. S. A. https://doi.org/10.1073/pnas.1602205113 (2016).Article 

    Google Scholar 
    Westphal, M. I., Browne, M., MacKinnon, K. & Noble, I. The link between international trade and the global distribution of invasive alien species. Biol. Invasions https://doi.org/10.1007/s10530-007-9138-5 (2008).Article 

    Google Scholar 
    Hennessey, M. et al. Phytosanitary Treatments. In The Handbook of Plant Biosecurity (eds Gordh, G. & Mckirdy, S.) 269–308 (Springer, Dordrecht, 2014).
    Google Scholar 
    Melvin Couey, H. & Chew, V. Confidence limits and sample size in quarantine research. J. Econ. Entomol. 79, 887–890 (1986).
    Google Scholar 
    Schortemeyer, M. et al. Appropriateness of probit-9 in the development of quarantine treatments for timber and timber commodities. J. Econ. Entomol. 104, 717–731 (2011).CAS 

    Google Scholar 
    Haack, R. A., Uzunovic, A., Hoover, K. & Cook, J. A. Seeking alternatives to probit 9 when developing treatments for wood packaging materials under ISPM No. 15. EPPO Bull. 41, 39–45 (2011).
    Google Scholar 
    Liqudio, N. J., Griffin, R. L. & Vick, K. W. Quarantine security for commodities: current approaches and potential strategies. In Proceedings of Joint Workshops of the Agricultural Research Service and the Animal and Plant Health Inspection Service, June 5–9 and July 31 -August 5, 1995 56 (1997).Follett, P. A. Phytosanitary irradiation for fresh horticultural commodities: Generic treatments, current issues, and next steps. Stewart Postharvest Rev. 3, 1–7 (2014).MathSciNet 

    Google Scholar 
    Hallman, G. J. & Loaharanu, P. Generic ionizing radiation quarantine treatments against fruit flies (Diptera: Tephritidae) proposed. J. Econ. Entomol. 95, 893–901 (2002).
    Google Scholar 
    Follett, P. A. & Armstrong, J. W. Revised irradiation doses to control melon fly, mediterranean fruit fly, and oriental fruit fly (Diptera: Tephritidae) and a generic dose for tephritid fruit flies. J. Econ. Entomol. 97, 1254–1262 (2004).
    Google Scholar 
    Follett, P. A. & Snook, K. Irradiation for quarantine control of the invasive light brown apple moth (Lepidoptera: Tortricidae) and a generic dose for tortricid eggs and larvae. J. Econ. Entomol. 105, 1971–1978 (2013).
    Google Scholar 
    Hallman, G. J., Arthur, V., Blackburn, C. M. & Parker, A. G. The case for a generic phytosanitary irradiation dose of 250Gy for Lepidoptera eggs and larvae. Radiat. Phys. Chem. 89, 70–75 (2013).ADS 
    CAS 

    Google Scholar 
    Hallman, G. J. Generic phytosanitary irradiation dose of 300 Gy proposed for the Insecta excluding pupal and adult Lepidoptera. Florida Entomol. 99, 206–210 (2016).
    Google Scholar 
    IPPC. ISPM 28. Annex 39. Irradiation treatment for the genus Anastrepha. 1–6 (2021).IPPC. ISPM 28. Annex 7. Irradiation Treatment for fruit flies of the family Tephritidae (generic). 1–6 (2021).Posthuma, L., Suter, G. W. & Traas, T. P. Species sensitivity distributions in ecotoxicology. Species sensitivity distributions in ecotoxicology (CRC Press, 2002). https://doi.org/10.1201/9781420032314.Book 

    Google Scholar 
    Newman, M. C. et al. Applying species-sensitivity distributions in ecological risk assessment: Assumptions of distribution type and sufficient numbers of species. Environ. Toxicol. Chem. 19, 508–515 (2000).CAS 

    Google Scholar 
    van Straalen, N. M. & van Leeuwen, C. J. European history of species sensitivity distributions. In Species Sensitivity Distributions in Ecotoxicology 43–60 (CRC Press, 2001). Doi:https://doi.org/10.1201/9781420032314.ch3.ANZECC & ARMCANZ. Australian and New Zealand guidelines for fresh and marine water quality. aquatic ecosystems. Aust. New Zeal. Environ. Conserv. Counc. Agric. Resour. Manag. Counc. Aust. New Zeal. 1–103 (2000).Aldenberg, T. & Jaworska, J. S. Uncertainty of the hazardous concentration and fraction affected for normal species sensitivity distributions. Ecotoxicol. Environ. Saf. 46, 1–18 (2000).CAS 

    Google Scholar 
    Hallman, G. J. Generic phytosanitary irradiation treatment for “true weevils” (Coleoptera: Curculionidae) infesting fresh commodities. Florida Entomol. 99, 197–201 (2016).
    Google Scholar 
    Follett, P. A. Irradiation for quarantine control of coffee berry borer, hypothenemus hampei (coleoptera: Curculionidae: Scolytinae) in coffee and a proposed generic dose for snout beetles (coleoptera: Curculionoidea). J. Econ. Entomol. 111, 1633–1637 (2018).CAS 

    Google Scholar 
    Earle, N. W., Simmons, L. A. & Nilakhe, S. S. Laboratory studies of sterility and competitiveness of boll weevils irradiated in an atmosphere of nitrogen, carbon dioxide, or air. J. Econ. Entomol. 72, 687–691 (1979).
    Google Scholar 
    Follett, P. A., McQuate, G. T., Sylva, C. D. & Swedman, A. Sensitivity of the quarantine pest rough Sweetpotato weevil, Blosyrus asellus to postharvest irradiation treatment. Proc. Hawaiian Entomol. Soc. 48, 23–27 (2016).
    Google Scholar 
    Hallman, G. J. Ionizing irradiation quarantine treatment against plum curculio (Coleoptera: Curculionidae). J. Econ. Entomol. 96, 1399–1404 (2003).
    Google Scholar 
    Jacklin, S. W., Richardson, E. C. & Yonce, C. E. Substerilizing doses of gamma irradiation to produce population suppression in plum curculio1. J. Econ. Entomol. 63, 1053–1057 (1970).
    Google Scholar 
    Yoshida, T., Fukami, J. I., Fukunaga, K. & Matsuyama, A. Control of harmful insects in timbers by irradiation: doses required for sterilization and inhibition of emergence of the minute pine bark beetle, Cryphalus fulvus. Jpn. J. Appl. Entomol. Zool. 18, 52–58 (1974).
    Google Scholar 
    Follett, P. A. Irradiation as a methyl bromide alternative for postharvest control of Omphisa anastomosalis (Lepidoptera: Pyralidae) and euscepes postfasciatus and cylas formicarius elegantulus (Coleoptera: Curculionidae) in sweet potatoes. J. Econ. Entomol. 99, 32–37 (2006).
    Google Scholar 
    Gould, W. P. & Hallman, G. J. Irradiation disinfestation of diaprepes root weevil (Coleoptera: Curculionidae) and papaya fruit fly (Diptera: Tephritidae). Florida Entomol. 87, 391–392 (2004).
    Google Scholar 
    van Haandel, A. et al. Tolerance of Hylurgus ligniperda (F.) (Coleoptera: Scolytinae) and Arhopalus ferus (Mulsant) (Coleoptera: Cerambycidae) to ionising radiation: a comparison with existing generic radiation phytosanitary treatments. New Zeal. J. For. Sci. 47, 1–9 (2017).Burgess, E. E. & Bennett, S. E. Sterilization of the male alfalfa weevil (Hypera postica: Curculionidae) by X-Radiation. J. Econ. Entomol. 59, 268–270 (1966).
    Google Scholar 
    Wood, D. L. & Stark, R. W. The effects of gamma radiation on the biology and behavior of adult ips confusus (LeConte) (Coleoptera: Scolytidae). Can. Entomol. 98, 1–10 (1966).
    Google Scholar 
    Wang, X. et al. Effect of X-ray (9 MeV) irradiation on the development and propagation of Ips sexdentatus. Plant Quar. 25, 28–31 (2011).
    Google Scholar 
    Zhan, G. et al. Effect of irradiation on development and propagation of larch bark beetle (Coleoptera: Scolytoidea). J. Nucl. Agric. Sci. 25, 1200–1205 (2011).
    Google Scholar 
    Gerstle, C. & Sazo, L. Efecto de las radiaciones de Cesio 137 sobre la fertilidad de hembras de Naupactus xanthographus (Germar) (Coleoptera: Curculionidae). Cienc. e Investig. Agrar. 16, 69–73 (1989).
    Google Scholar 
    Manoto, E. C., Obra, G. B., Reyes, M. R. & Resilva, S. S. Irradiation as a quarantine treatment for ornamentals. IAEA-Tecdoc 1082, 81–91 (1999).
    Google Scholar 
    Duvenhage, A. J. & Johnson, S. A. The potential of irradiation as a postharvest disinfestation treatment against phlyctinus callosus (Coleoptera: Curculionidae). J. Econ. Entomol. 107, 154–160 (2014).CAS 

    Google Scholar 
    Jaynes, A. & Godwin, P. A. Sterilization of the white-pine weevil with gamma radiation. J. Econ. Entomol. 50, 393–395 (1957).CAS 

    Google Scholar 
    Aldryhim, Y. N. & Adam, E. E. Efficacy of gamma irradiation against Sitophilus granarius (L.) (Coleoptera: Curculionidae). J. Stored Prod. Res. 35, 225–232 (1999).
    Google Scholar 
    Follett, P. A. et al. Irradiation quarantine treatment for control of Sitophilus oryzae (Coleoptera: Curculionidae) in rice. J. Stored Prod. Res. 52, 63–67 (2013).
    Google Scholar 
    Hu, T., Chen, C. C. & Peng, W. K. Lethal effect of gamma irradiation on Sitophilus zeamais (Coleoptera: Curculionidae). Formos. Entomol. 23, 145–150 (2003).
    Google Scholar 
    Arthur, V. & Wiendl, F. M. Comportamento e competitividade sexual de adultos de Sphenophorus levis Vaurie, 1978 (col., Curculionidae), uma praga da cana-de-açucar, irradiados com radiações gama do cobaldo-60. Brazilian J. Agric. 68, 57–66 (1993).
    Google Scholar 
    Obra, G. B., Resilva, S. S., Follett, P. A. & Lorenzana, L. R. J. Large-scale confirmatory tests of a phytosanitary irradiation treatment against Sternochetus frigidus (Coleoptera: Curculionidae) in Philippine mango. J. Econ. Entomol. 107, 161–165 (2014).
    Google Scholar 
    Seo, S. T. et al. Mango weevil: Cobalt-60 γ-irradiation of packaged mangoes. J. Econ. Entomol. 67, 504–505 (1974).
    Google Scholar 
    Yoshida, T., Fukami, J. I., Fukunaga, K. & Matsuyama, A. Effects of gamma radiation on Xyleborus perforans (Wollaston) pupae and adults. J. Pestic. Sci. 2, 413–420 (1977).
    Google Scholar 
    Yoshida, T., Fukami, J. I., Fukunaga, K. & Matsuyama, A. Control of the harmful insects in timbers by irradiation: Doses required for kill, sterilization and inhibition of emergence in three species of ambrosia beetles (Xyleborini) in Japan. Jpn. J. Appl. Entomol. Zool. 19, 193–202 (1975).
    Google Scholar 
    Follett, P. A. & McQuate, G. T. Accelerated development of quarantine treatments for insects on poor hosts. J. Econ. Entomol. https://doi.org/10.1603/0022-0493-94.5.1005 (2001).Article 

    Google Scholar 
    Plazzi, F., Ferrucci, R. R. & Passamonti, M. Phylogenetic representativeness: A new method for evaluating taxon sampling in evolutionary studies. BMC Bioinform. 11, 1–15 (2010).
    Google Scholar 
    Moore, D. R. J., Priest, C. D., Galic, N., Brain, R. A. & Rodney, S. I. Correcting for phylogenetic autocorrelation in species sensitivity distributions. Integr. Environ. Assess. Manag. 16, (2020).Carr, G. J. & Belanger, S. E. SSDs revisited: Part I—A framework for sample size guidance on species sensitivity distribution analysis. Environ. Toxicol. Chem. 38, 1514–1525 (2019).CAS 

    Google Scholar 
    Wheeler, J. R., Grist, E. P. M., Leung, K. M. Y., Morritt, D. & Crane, M. Species sensitivity distributions: Data and model choice. Mar. Pollut. Bull. 45, 192–202 (2002).CAS 

    Google Scholar 
    Duboudin, C., Ciffroy, P. & Magaud, H. Acute-to-chronic species sensitivity distribution extrapolation. Environ. Toxicol. Chem. 23, 1774–1785 (2004).CAS 

    Google Scholar 
    Esteves, S. M. et al. Can we predict diatoms herbicide sensitivities with phylogeny? Influence of intraspecific and interspecific variability. Ecotoxicology 26, 1065–1077 (2017).CAS 

    Google Scholar 
    Hiki, K. & Iwasaki, Y. Can we reasonably predict chronic species sensitivity distributions from acute species sensitivity distributions?. Environ. Sci. Technol. 54, 13131–13136 (2020).ADS 
    CAS 

    Google Scholar 
    Baird, D. J. & Van den Brink, P. J. Using biological traits to predict species sensitivity to toxic substances. Ecotoxicol. Environ. Saf. 67, 296–301 (2007).CAS 

    Google Scholar 
    Guénard, G., von der Ohe, P. C., Walker, S. C., Lek, S. & Legendre, P. Using phylogenetic information and chemical properties to predict species tolerances to pesticides. Proc. R. Soc. B Biol. Sci. 281, 1–9 (2014).
    Google Scholar 
    Larras, F., Keck, F., Montuelle, B., Rimet, F. & Bouchez, A. Linking diatom sensitivity to herbicides to phylogeny: A step forward for biomonitoring?. Environ. Sci. Technol. 48, 1921–1930 (2014).ADS 
    CAS 

    Google Scholar 
    Hayashi, T. I. & Kashiwagi, N. A bayesian method for deriving species-sensitivity distributions: Selecting the best-fit tolerance distributions of taxonomic groups. Hum. Ecol. Risk Assess. 16, 251–263 (2010).CAS 

    Google Scholar 
    Xu, F. L. et al. Key issues for the development and application of the species sensitivity distribution (SSD) model for ecological risk assessment. Ecol. Indic. 54, 227–237 (2015).CAS 

    Google Scholar 
    Dowse, R., Tang, D., Palmer, C. G. & Kefford, B. J. Risk assessment using the species sensitivity distribution method: Data quality versus data quantity. Environ. Toxicol. Chem. 32, 1360–1369 (2013).CAS 

    Google Scholar 
    Dias, V. S. et al. Relative tolerance of three morphotypes of the anastrepha fraterculus complex (Diptera: Tephritidae) to cold phytosanitary Treatment. J. Econ. Entomol. 113, 1176–1182 (2020).CAS 

    Google Scholar 
    Myers, S. W., Cancio-Martinez, E., Hallman, G. J., Fontenot, E. A. & Vreysen, M. J. B. Relative tolerance of six Bactrocera (Diptera: Tephritidae) species to phytosanitary cold treatment. J. Econ. Entomol. 109, 2341–2347 (2016).
    Google Scholar 
    Gazit, Y., Akiva, R. & Gavriel, S. Cold tolerance of the Mediterranean fruit fly in date and mandarin. J. Econ. Entomol. 107, 1745–1750 (2014).
    Google Scholar 
    Zhao, J. et al. Gamma radiation as a phytosanitary treatment against larvae and pupae of Bactrocera dorsalis (Diptera: Tephritidae) in guava fruits. Food Control 72, 360–366 (2017).
    Google Scholar 
    Thorley, J. & Schwarz, C. ssdtools: An R package to fit Species sensitivity distributions. J. Open Sour. Softw. 3, 1–2 (2018).
    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoritic Approach 2nd edn. (Springer, 2002). https://doi.org/10.1007/978-0-387-22456-5_7.Book 
    MATH 

    Google Scholar 
    Mazucheli, J., Menezes, A. F. B. & Nadarajah, S. mle.tools: An R package for maximum likelihood bias correction. R. J. 9, 268–290 (2017).
    Google Scholar 
    Cox, D. R. & Snell, E. J. A general definition of residuals. J. R. Stat. Soc. Ser. B 30, 248–265 (1968).MathSciNet 
    MATH 

    Google Scholar 
    Follett, P. A. Irradiation as a quarantine treatment for mango seed weevil (Coleoptera: Curculionidae). Proc. Hawaii. Entomol. Soc. 35, 95–100 (2001).
    Google Scholar  More