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    Macroecological distributions of gene variants highlight the functional organization of soil microbial systems

    1.Gupta A, Sharma VK. Using the taxon-specific genes for the taxonomic classification of bacterial genomes. BMC Genom. 2015;16:1–15.Article 
    CAS 

    Google Scholar 
    2.Gil R, Silva FJ, Pereto J, Moya A. Determination of the Core of a Minimal Bacterial Gene Set. Microbiol Mol Biol Rev. 2004;68:518–37.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Mira A, Martín-Cuadrado AB, D’Auria G, Rodríguez-Valera F. The bacterial pan-genome: a new paradigm in microbiology. Int Microbiol. 2010;13:45–57.CAS 
    PubMed 

    Google Scholar 
    4.Escalas A, Troussellier M, Yuan T, Bouvier T, Bouvier C, Mouchet MA, et al. Functional diversity and redundancy across fish gut, sediment and water bacterial communities. Environ Microbiol. 2017;19:3268–82.PubMed 
    Article 

    Google Scholar 
    5.Jurburg SD, Salles JF. Functional Redundancy and Ecosystem Function — The Soil Microbiota as a Case Study. In: Lo Y-H, Blanco JA, Shovonlal R, editors. Biodiversity in Ecosystems—Linking Structure and Function. BoD–Books on Demand; 2015. p. 29–49.6.Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O’Connor MI, et al. Function and functional redundancy in microbial systems. Nat Ecol Evol. 2018;2:936–43.PubMed 
    Article 

    Google Scholar 
    7.Polz MF, Hunt DE, Preheim SP, Weinreich DM. Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes. Philos Trans R Soc Lond B Biol Sci. 2006;361:2009–21.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Young JPW. Bacteria Are Smartphones and Mobile Genes Are Apps. Trends Microbiol. 2016;24:931–2.CAS 
    PubMed 
    Article 

    Google Scholar 
    9.Boon E, Meehan CJ, Whidden C, Wong DHJ, Langille MGI, Beiko RG. Interactions in the microbiome: communities of organisms and communities of genes. FEMS Microbiol Rev. 2014;38:90–118.CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Escalas A, Hale L, Voordeckers JW, Yang Y, Firestone MK, Alvarez-Cohen L, et al. Microbial Functional Diversity: from Concepts to Applications. Ecol Evol. 2019;5:12000–16.Article 

    Google Scholar 
    11.Barberán A, Casamayor EO, Fierer N. The microbial contribution to macroecology. Front Microbiol. 2014;5:1–8.Article 

    Google Scholar 
    12.Shade A, Dunn RR, Blowes SA, Keil P, Bohannan BJM, Herrmann M, et al. Macroecology to Unite All Life, Large and Small. Trends Ecol Evol. 2018;33:731–44.PubMed 
    Article 

    Google Scholar 
    13.Chase AB, Martiny JB. The importance of resolving biogeographic patterns of microbial microdiversity. Microbiol Aust. 2018;1:5–8.Article 

    Google Scholar 
    14.Shoemaker WR, Locey KJ, Lennon JT. A macroecological theory of microbial biodiversity. Nat Ecol Evol. 2017;1:e1450v4.Article 

    Google Scholar 
    15.Bachy C, Worden AZ. Microbial ecology: finding structure in the rare biosphere. Curr Biol. 2014;24:R315–R317.16.Lynch MDJ, Neufeld JD. Ecology and exploration of the rare biosphere. Nat Rev Microbiol. 2015;13:217–29.CAS 
    PubMed 
    Article 

    Google Scholar 
    17.Pedrós-Alió C. The Rare Bacterial Biosphere. Ann Rev Mar Sci. 2012;4:449–66.PubMed 
    Article 

    Google Scholar 
    18.Rabinowitz D. Seven forms of rarity and their frequency in the flora of the British Isles. In: Soulé ME, editors. Conservation biology: the science of scarcity and diversity. Sinauer Associates; Massachusetts; 1986.19.McGeoch MA, Gaston KJ. Occupancy frequency distributions: patterns, artefacts and mechanisms. Biol Rev Camb Philos Soc. 2002;77:311–31.PubMed 
    Article 

    Google Scholar 
    20.Blackburn TM, Cassey P, Gaston KJ. Variations on a theme: Sources of heterogeneity in the form of the interspecific relationship between abundance and distribution. J Anim Ecol. 2006;75:1426–39.PubMed 
    Article 

    Google Scholar 
    21.Buckley HL, Freckleton RP. Understanding the role of species dynamics in abundance-occupancy relationships. J Ecol. 2010;98:645–58.Article 

    Google Scholar 
    22.Gaston KJ, Blackburn TM, Greenwood JJD, Gregory RD, Quinn RM, Lawton JH. Abundance-occupancy relationships. J Appl Ecol. 2000;37:39–59.Article 

    Google Scholar 
    23.Miranda LE, Killgore KJ. Abundance–occupancy patterns in a riverine fish assemblage. Freshw Biol. 2019;64:2221–33.Article 

    Google Scholar 
    24.Suhonen J, Jokimäki J. Temporally stable species occupancy frequency distribution and abundance-occupancy relationship patterns in urban wintering bird assemblages. Front Ecol Evol. 2019;7:129.Article 

    Google Scholar 
    25.Webb TJ, Barry JP, McClain CR. Abundance–occupancy relationships in deep sea wood fall communities. Ecography. 2017;40:1339–47.Article 

    Google Scholar 
    26.Amend AS, Oliver TA, Amaral-Zettler LA, Boetius A, Fuhrman JA, Horner-Devine MC, et al. Macroecological patterns of marine bacteria on a global scale. J Biogeogr. 2013;40:800–11.Article 

    Google Scholar 
    27.Barberán A, Bates ST, Casamayor EO, Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012;6:343–51.PubMed 
    Article 
    CAS 

    Google Scholar 
    28.Barnes CJ, Burns CA, van der Gast CJ, McNamara NP, Bending GD. Spatio-temporal variation of core and satellite arbuscular mycorrhizal fungus communities in Miscanthus giganteus. Front Microbiol. 2016;7:1–12.
    Google Scholar 
    29.Fillol M, Auguet JC, Casamayor EO, Borrego CM. Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J. 2016;10:665–77.PubMed 
    Article 

    Google Scholar 
    30.Jeanbille M, Gury J, Duran R, Tronczynski J, Agogué H, Saïd OBen, et al. Response of core microbial consortia to chronic hydrocarbon contaminations in coastal sediment habitats. Front Microbiol. 2016;7:1–13.
    Google Scholar 
    31.Lindh MV, Sjöstedt J, Ekstam B, Casini M, Lundin D, Hugerth LW, et al. Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers. Environ Microbiol. 2017;19:1222–36.CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Logares R, Audic SS, Bass D, Bittner L, Boutte C, Christen R, et al. Patterns of Rare and Abundant Marine Microbial Eukaryotes. Curr Biol. 2014;24:813–21.CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Michelland R, Thioulouse J, Kyselková M, Grundmann GL. Bacterial Community Structure at the Microscale in Two Different Soils. Micro Ecol. 2016;72:717–24.CAS 
    Article 

    Google Scholar 
    34.Unterseher M, Jumpponen A, Öpik M, Tedersoo L, Moora M, Dormann CF, et al. Species abundance distributions and richness estimations in fungal metagenomics – Lessons learned from community ecology. Mol Ecol. 2011;20:275–85.PubMed 
    Article 

    Google Scholar 
    35.Grime JP. Benefits of plant diversity to ecosystems: Immediate, filter and founder effects. J Ecol. 1998;86:902–10.Article 

    Google Scholar 
    36.Grime JP. Dominant and subordinate components of plant communities: implications for succession, sta- bility and diversity. In: Gray AJ, Crawley MJ, editors. Colonization, Succession and Stability. Oxford:Blackwell Scientific Publications; 1984. p. 413–28.37.Hanski I. Dynamics of Regional Distribution: the Core and Satellite Species Hypothesis. Oikos. 1982;38:210.Article 

    Google Scholar 
    38.Magurran AE, Henderson PA. Explaining the excess of rare species in natural species abundance distributions. Nature. 2003;422:714–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Newton R, Shade A. Lifestyles of rarity: understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere. Aquat Micro Ecol. 2016;78:51–63.Article 

    Google Scholar 
    40.Shade A, Jones SE, Caporaso JG, Handelsman J, Knight R, Fierer N, et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio. 2014;5:e01371–14.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    41.Shade A, Gilbert JA. Temporal patterns of rarity provide a more complete view of microbial diversity. Trends Microbiol. 2015;23:335–40.CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Koch AL. Oligotrophs versus copiotrophs. BioEssays. 2001;23:657–61.CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Cobo-Simón M, Tamames J. Relating genomic characteristics to environmental preferences and ubiquity in different microbial taxa. BMC Genom. 2017;18:1–11.Article 
    CAS 

    Google Scholar 
    44.Tu Q, Yu H, He Z, Deng Y, Wu L, Van Nostrand JD, et al. GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol Ecol Resour. 2014;14:914–28.CAS 
    PubMed 

    Google Scholar 
    45.Xu X, Wang N, Lipson D, Sinsabaugh R, Schimel J, He L, et al. Microbial macroecology: in search of mechanisms governing microbial biogeographic patterns. Glob Ecol Biogeogr. 2020;29:1870–86.Article 

    Google Scholar 
    46.Reich PB, Knops J, Tilman D, Craine J, Ellsworth D, Tjoelker M, et al. Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature. 2001;410:809–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Field CB, Chapin FS, Chiariello NK, Holland EA, Mooney HA. The Jasper Ridge CO2 Experiment: Design and Motivation. In: Mooney HA, Koch GW, (Editors). Carbon Dioxide and Terrestrial Ecosystems. San Diego, California: Academic Press; 1996. p. 121–45.Chapter 

    Google Scholar 
    48.Luo C, Rodriguez-R LM, Johnston ER, Wu L, Cheng L, Xue K, et al. Soil microbial community responses to a decade of warming as revealed by comparative metagenomics. Appl Environ Microbiol. 2014;80:1777–86.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    49.Mauritz M, Bracho R, Celis G, Hutchings J, Natali SM, Pegoraro E, et al. Nonlinear CO2 flux response to 7 years of experimentally induced permafrost thaw. Glob Chang. Biol. 2017;23:3646–66.
    Google Scholar 
    50.Natali SM, Schuur EAG, Mauritz M, Schade JD, Celis G, Crummer KG, et al. Permafrost thaw and soil moisture driving CO2 and CH4 release from upland tundra. J Geophys Res Biogeosci. 2015;120:525–37.CAS 
    Article 

    Google Scholar 
    51.Yang Y, Gao Y, Wang S, Xu D, Yu H, Wu L, et al. The microbial gene diversity along an elevation gradient of the Tibetan grassland. ISME J. 2014;8:430–40.CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Yang Y, Wu L, Lin Q, Yuan M, Xu D, Yu H, et al. Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob Chang Biol. 2013;19:637–48.PubMed 
    Article 

    Google Scholar 
    53.Zhang Y, Cong J, Lu H, Li G, Xue Y, Deng Y, et al. Soil bacterial diversity patterns and drivers along an elevational gradient on Shennongjia Mountain, China. Micro Biotechnol. 2015;8:739–46.Article 

    Google Scholar 
    54.Zhang Y, Cong J, Lu H, Deng Y, Liu X, Zhou J, et al. Soil bacterial endemism and potential functional redundancy in natural broadleaf forest along a latitudinal gradient. Sci Rep. 2016;6:1–8.Article 
    CAS 

    Google Scholar 
    55.Paula FS, Rodrigues JLM, Zhou J, Wu L, Mueller RC, Mirza BS, et al. Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities. Mol Ecol. 2014;23:2988–99.PubMed 
    Article 

    Google Scholar 
    56.Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EDC, Paula FS, et al. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci USA. 2013;110:988–93.CAS 
    PubMed 
    Article 

    Google Scholar 
    57.He Z, Deng Y, Van Nostrand JD, Tu QC, Xu MY, Hemme CL, et al. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. Isme J. 2010;4:1167–79.CAS 
    PubMed 
    Article 

    Google Scholar 
    58.He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 2007;1:67–77.CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Li X, He Z, Zhou J. Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation. Nucleic Acids Res. 2005;33:6114–23.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Tu Q, He Z, Deng Y, Zhou J. Strain/species-specific probe design for microbial identification microarrays. Appl Environ Microbiol. 2013;79:5085–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Wu L, Liu X, Schadt CW, Zhou J. Microarray-based analysis of subnanogram quantities of microbial community DNAs by using whole-community genome amplification. Appl Environ Microbiol. 2006;72:4931–41.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Wu L, Liu X, Schadt CW, Zhou J. Microarray-based analysis of subnanogram quantities of microbial community DNAs by using whole-community genome amplification. Applied and Environmental Microbiology. 2006;72:4931–41.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    63.Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, et al. Package ‘vegan’. Community ecology package, version. 2013;2:1–295.
    Google Scholar 
    64.Anderson MJ, Bueno AS. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46.
    Google Scholar 
    65.Crow EL, Patil GP. Applications in Ecology. In: Cros E, Shimizu K, editors. Lognormal Distributions. New York and Basel:Marcel Dekker; 1988. p. 303–30.66.Ser-Giacomi E, Zinger L, Malviya S, De Vargas C, Karsenti E, Bowler C, et al. Ubiquitous abundance distribution of non-dominant plankton across the global ocean. Nat Ecol Evol. 2018;2:1243–9.PubMed 
    Article 

    Google Scholar 
    67.Wu L, Ning D, Zhang B, Li Y, Zhang P, Shan X, et al. Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nat Microbiol. 2019;4:1183–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Locey KJ, Lennon JT. Scaling laws predict global microbial diversity. Proc Natl Acad Sci. 2016;113:5970–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Louca S, Mazel F, Doebeli M, Parfrey LW. A census-based estimate of Earth’s bacterial and archaeal diversity. PLoS Biol. 2019;2:1–30.
    Google Scholar 
    70.Tokeshi M. Dynamics of distribution in animal communities: theory and analysis. Res Popul Ecol (Kyoto). 1992;34:249–73.Article 

    Google Scholar 
    71.Logares R, Deutschmann IM, Junger PC, Giner CR, Krabberød AK, Schmidt TSB, et al. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome. 2020;8:55.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Azovsky A, Mazei Y. Do microbes have macroecology? Large-scale patterns in the diversity and distribution of marine benthic ciliates. Glob Ecol Biogeogr. 2013;22:163–72.Article 

    Google Scholar 
    73.Noguez AM, Arita HT, Escalante AE, Forney LJ, García-Oliva F, Souza V. Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest. Glob Ecol Biogeogr. 2005;14:241–8.Article 

    Google Scholar 
    74.Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Papp L, Izsák J, Papp L, Izsak J. Bimodality in Occurrence Classes: a Direct Consequence of Lognormal or Logarithmic Series Distribution of Abundances- A Numerical Experimentation. Oikos. 1997;79:191.Article 

    Google Scholar 
    76.Verberk WCEP, van der Velde G, Esselink H. Explaining abundance-occupancy relationships in specialists and generalists: A case study on aquatic macroinvertebrates in standing waters. J Anim Ecol. 2010;79:589–601.PubMed 
    Article 

    Google Scholar 
    77.Liao J, Cao X, Zhao L, Wang J, Gao Z, Wang MC, et al. The importance of neutral and niche processes for bacterial community assembly differs between habitat generalists and specialists. FEMS Microbiol Ecol. 2016;92:fiw174.PubMed 
    Article 
    CAS 

    Google Scholar 
    78.Slatyer RA, Hirst M, Sexton JP. Niche breadth predicts geographical range size: a general ecological pattern. Ecol Lett. 2013;16:1104–14.PubMed 
    Article 

    Google Scholar 
    79.Fierer N, Barberán A, Laughlin DC. Seeing the forest for the genes: using metagenomics to infer the aggregated traits of microbial communities. Front Microbiol. 2014;5:1–6.Article 

    Google Scholar 
    80.Rivett DW, Bell T. Abundance determines the functional role of bacterial phylotypes in complex communities. Nat Microbiol. 2018;3:767–72.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Guillaumaud N, et al. Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ Microbiol. 2007;9:2211–9.PubMed 
    Article 

    Google Scholar 
    82.Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Freitag T, et al. Maintenance of soil functioning following erosion of microbial diversity. Environ Microbiol. 2006;8:2162–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    83.Mendes LW, Tsai SM, Navarrete AA, de Hollander M, van Veen JA, Kuramae EE. Soil-Borne microbiome: linking diversity to function. Micro Ecol. 2015;70:255–65.CAS 
    Article 

    Google Scholar 
    84.Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome – SM. Science. 2015;348:1261359–1261359.PubMed 
    Article 
    CAS 

    Google Scholar 
    85.Wohl DL, Arora S, Gladstone JR. Functional redundancy supports biodiversity and ecosystem function in a cloased and constant environment. Ecology. 2008;85:1534–40.Article 

    Google Scholar 
    86.Kurm V, Geisen S, Gera Hol WH. A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa. Environ Microbiol. 2019;21:750–8.PubMed 
    Article 

    Google Scholar 
    87.Bergkessel M, Basta DW, Newman DK. The physiology of growth arrest: Uniting molecular and environmental microbiology. Nat Rev Microbiol. 2016;14:549–62.CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Hofer U. Life in the slow lane. Nat Rev Microbiol. 2019;26:266–7.Article 
    CAS 

    Google Scholar 
    89.Baho DL, Peter H, Tranvik LJ. Resistance and resilience of microbial communities – Temporal and spatial insurance against perturbations. Environ Microbiol. 2012;9:2283–92.Article 

    Google Scholar 
    90.Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 2017;11:853–62.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    91.Aanderud ZT, Jones SE, Fierer N, Lennon JT. Resuscitation of the rare biosphere contributes to pulses of ecosystem activity. Front Microbiol. 2015;6:1–11.Article 

    Google Scholar 
    92.Lawson CE, Strachan BJ, Hanson NW, Hahn AS, Hall ER, Rabinowitz B, et al. Rare taxa have potential to make metabolic contributions in enhanced biological phosphorus removal ecosystems. Environ Microbiol. 2015;17:4979–93.CAS 
    PubMed 
    Article 

    Google Scholar 
    93.Zhou J, He Z, Yang Y, Deng Y, Tringe SG, Alvarez-Cohen L. High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio. 2015;6:e02288–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, et al. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 2011;5:1303–13.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    95.Shi Z, Yin H, Van Nostrand JD, Voordeckers JW, Tu Q, Deng Y, et al. Functional Gene Array-Based Ultrasensitive and Quantitative Detection of Microbial Populations in Complex Communities. mSystems. 2019;4:99–117.
    Google Scholar  More

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    Dynamic carbon flux network of a diverse marine microbial community

    Overview of the FluxNet methodThe FluxNet approach is based on a mechanistic model, which includes multiple species/types of phytoplankton, bacteria, dissolved and particulate organic matter (DOM, POM), inorganic nutrients, micronutrients and inhibitors (see Table 1). For phytoplankton—bacteria carbon flux, which is the focus here, phytoplankton produce organic carbon by exudation and death. For exudation, living phytoplankton produce total DOM at constant and photosynthesis-proportional rates (ke, ef), with a composition defined by an exudation fraction (Fe) for each DOM species. These parameters vary by phytoplankton type. For example, for green algae (gre), the constant exudation rate is kegre and the fraction of glucose-containing HMW DOM (gl2) is Fegre,gl2. For one phytoplankton type the total DOM production varies in time with the photosynthesis rate, but the composition is constant. Phytoplankton die by a general death function and inhibition. The death function is time-variable (a bell-shaped function with a maximum at a specific time of year) and does not differentiate between various death mechanisms like zooplankton grazing or viral lysis, but presumably it represents mostly grazing in this case. Upon death, the phytoplankton biomass is converted to POM and DOM, where e.g., the content of chrysolaminarin (chr) for the diatom Rhizosolenia styliformis (rst) is defined by a composition fraction (Fxrst,chr). POM dissolves to DOM at a first-order rate. Bacteria consume DOM using Monod-level kinetics, where e.g. the affinity for Polaribacter (pol) for chrysolaminarin is defined by a half-saturation constant (Kshpol,chr).Table 1 Model components.Full size tableThe novel aspect is the upscaling to hundreds of state variables and thousands of parameters, which is accompanied by several conceptual and practical modeling challenges. To balance mass and account for the action of unobserved components, cryptic or hypothetical species are included [17], like DOM types d01-d15, which may represent e.g., threonine [18]. To simulate a diverse community with a smaller number of drivers (“paradox of the plankton”) and control chaos, interaction via micronutrients and inhibitors, as well as dormancy is included [19,20,21,22]. Parameters are optimized/calibrated to minimize the discrepancy between the model and observations. Which parameters are optimized and the corresponding ranges is based on available information (complete model equations and parameters are in Table S1–S25). For example, the constant DOM production rate (ke) is optimized for all phytoplankton, with a range adopted from a previous modeling study [23]. For rst (Rhizosolenia styliformis), the exudation fractions for most DOM components, like the cryptic species d01 (Ferst,d01), are optimized. Others, like glucose-containing HMW DOM (Ferst,gl2), are fixed based on literature (Table S14). The optimization is challenging because of the many components, nonlinear interactions, and resulting local optima in the objective function. We developed an optimization routine customized for microbial ecosystems with a number of key features.First, the method mimics natural speciation, where a coarse-grained model is gradually de-lumped to a finer resolution, a strategy also used in manual model development [13, 24, 25]. This is illustrated in Fig. 1, which shows how the model starts with just one component in each ecological compartment (Fig. 1E). This model is optimized until a threshold is reached, and then all species are de-lumped/split into two, followed by another round of optimization and so on. During the course of the optimization, with time or model runs, the number of components and parameters increase, and the total error generally decreases, although there can be a transient increase when new species are introduced (Fig. 1A, B). This way the optimization routine works with a smaller model on average and computational effort can be directed to a smaller set of parameters corresponding to newly introduced species, and the performance increases (Fig. 1C).Fig. 1: FluxNet inference method illustration.A Number components and optimized parameters. B Error for entire model (Total) and selected individual observations (rst = R. styliformis, pol = Polaribacter, lam = particulate chrysolaminarin). Best of 128 replicate runs. C Diversification of chrysolaminarin uptake affinity (max. heterotrophy rate/half-saturation constant). D Method performance with and without de-lumping. E Network corresponding to different de-lump levels. See Table 1 for component names and abbreviations.Full size imageAt each de-lumping level, the new species generally inherits the parameter values (i.e., the genome [26]) from the old species. Subsequent optimization then diversifies the population. This is illustrated in Fig. 1C, which shows the uptake affinity of all bacteria species for chr. However, different parameter values can also be specified for the new species, and then they are adopted and overwrite those inherited from the old species. This is used, for example, to assign species-specific cell sizes or prevent species from taking up a substrate. In Fig. 1C, those species that are not capable of assimilating chr, like rei (Reinekea), have an affinity equal to 0. The method thus allows for natural and automated expansion of the model to very large scale, yet provides a way to constrain/curate it based on available information.Second, the routine includes multi-parameter optimization (Nelder-Mead simplex method) on selected subsets of dependent parameters, like those involved in the production and consumption of chrysolaminarin (chr) or directly affecting the photosynthesis of the diatom R. styliformis (rst). Dependence between parameters, like max. photosynthesis rate and nutrient half-saturation constant, are explicitly considered. Also, Monte Carlo scans are performed on selected parameter sets at various points in the process.Application to Helgoland time seriesThe FluxNet method is applied to a four-year time series at Helgoland [27], including near-daily observations of 15 phytoplankton and 38 heterotrophic bacteria types (e.g., species, strains) and various bulk and auxiliary parameters (e.g., Chlorophyll a, DAPI, temperature, nitrate+nitrite, ammonium, phosphate, light extinction) (Tables S19 and S20). Data from more focused studies characterizing DOM and POM are also included [28, 29] (Table S21).In addition to the time-series data, the model is informed by literature information. Model parameters, incl. general properties like phytoplankton exudation fraction or bacteria growth efficiency, are constrained based on past models and data. Also, constraints are implemented for parameters controlling composition, exudation and utilization for the specific components included in the model. Those were based on a literature meta-analysis, where we searched primarily for studies with strains from Helgoland, but included strains from other locations if necessary. These constraints include, for example, for the phytoplankton storage polysaccharide chrysolaminarin, the typical content (~30% for diatoms, none for dinoflagellates) and ability of bacteria to assimilate it (yes for Polaribacter, no for Roseobacters and Reinekea) (Tables S4 and S11). Imposing constraints from the literature generally results in a worse agreement with the observations, but also increased realism of the model. Removing the constraints of phytoplankton composition (Table S4) significantly improves the agreement with observations, but also predicts substantial glycogen content of diatoms (e.g., Fxmhe,gly+ply = 0.19). Removing uptake constraints by bacteria (Table S11) reduces the error, but not significantly, suggesting that there is enough flexibility of the model to reproduce the observations even with this constraint. However, that model also includes features that disagree with literature, like substantial uptake of chr by s11 (Kshs11,chr = 25 L/mmolC/d).Carbon fluxes through and within in the ecosystemThe final model includes 210 components and their behavior and interaction are described by a total of 8200 calibrated parameters of 50 different parameter types (e.g., the composition of each of the 53 microbes is described by 76 fractions Fx, or 4000 total parameters) (Fig. 1), and it constitutes a mass-balancing, mechanistically-constrained, quantitative representation of the ecosystem. It reproduces many of the observed patterns of summary parameters like Chlorophyll a (chl), total bacteria (dap), particulate chrysolaminarin (lam), various high-molecular weight (HMW) DOM compounds, as well as absolute concentrations of individual phytoplankton and bacteria species (Fig. 2A–C). Only subset of the hundreds of model components is shown in Fig. 2B, C, which were selected based on (a) importance (e.g., rst is the dominant OM producer in 2009), (b) availability of data (e.g., chrysolaminarin, [29]) and (c) illustration of co-blooming (panel B) and succession (panel C). All model-data comparisons are presented in the SI (Fig. S1). The model under-predicts total DOM (doc), probably because a large fraction of observed DOM is more refractory allochthonous material, which is not considered in the model.Fig. 2: FluxNet model results and comparison to data.A All model types lumped. Phytoplankton (chl, μgChla/L), POM (poc, incl. microbes, μmolC/L ×0.1*), DOM (doc, μmolC/L ×0.1*), bacteria (dap, 1e6/mL ×3*). Gray shading are spring blooms, defined as the first time of the year the phytoplankton exceeds 3 µgChla/L plus 28 days. B Selected types for 2009 spring bloom. Rhizosolenia styliformis (rst, centric diatom, 1e6/L ×1.2*), Thalassiosira nordenskioeldii (tno, centric diatom, 1e6/L ×0.05*), particulate chrysolaminarin (lam = phr + phytoplankton content, μmolC/L ×0.002*), dissolved chrysolaminarin (chr, μmolC/L ×0.002*, no data available), Polaribacter (pol, DAPI × CARD-FISH, 1e6/mL ×0.1*), NS3a marine group (ns3, 1e6/mL ×0.2*). C Selected types for 2010 spring bloom. Mediopyxis helysia (mhe, centric diatom, 1e6/L), Thalassiosira nordenskioeldii (tno, centric diatom, 1e6/L), glucose-containing HMW DOM (glc, μmolC/L ×0.01*), arabinose-containing HMW DOM (ara, μmolC/L ×3*), Reinekea (rei, 1e6/mL ×5*), Alteromonas (alt, 1e6/mL ×1.5*). Lines are model and symbols are data [27,28,29]. *Individual concentration series scaled to illustrate dynamics. See Fig. S1 for all model-data comparisons. Upside-down triangles mark various bloom stages for networks in (D) and Fig. 4A. D Inferred carbon flux network. Nodes are components. Size indicates in/outflux (μmolC/L/d), color varied randomly within each ecological compartment. Lines are fluxes. Thickness is proportional to log flux (μmolC/L/d), colored based on the source node, lines below a threshold distance are colored gray to highlight most important fluxes. Italic numbers are total fluxes (μmolC/L/d). Flux cut off is 0.01%. See Table 1 for component names and abbreviations. See Movie S1.Full size imageIt is important to understand that the model was calibrated to these observations, so this is not a prediction per se. The main information produced by this analysis (emergent property) are the mass fluxes. Predicted ecosystem-level fluxes can be compared to independent estimates, which were not used as input here. For the period 2009–2012, the gross primary production rate in the model is 28 (±1.2 standard deviation) mmolC/m2/d. Uncertainty of fluxes and parameters are based on top 5% of 128 replicate runs, as in [23]. This flux compares well to a regional estimate of 29 (26–33) mmolC/m2/d for the Transitional East Region of the North Sea for the same period [30]. At the end of March, the bacterial production rate in the model is 0.32 (±0.041), 0.14 (±0.017), 0.20 (±0.025) and 0.45 (±0.057) μmolC/L/d for the 4 years, respectively. This is consistent with measurements of 0.20 μmolC/L/d in 1992 ~30 km from Helgoland [31].These comparisons provide confidence in other aggregate fluxes predicted by the model. The C, N and P fluxes to the sediment bed, via settling of phytoplankton and POM, are 5.8 (±0.91) mmolC/m2/d, 0.87 (±0.14) mmolN/m2/d and 0.054 (±0.0085) mmolP/m2/d, which constitute 20%, 16% and 18% of the input via photosynthesis (C) or external input (N, P) (see Fig. S2). External “new” input of N is 0.66 μmolN/L/d, which is 6.0 time higher than the 0.11 (±0.023) μmolN/L/d released or “recycled” by bacteria.The resulting flux network includes quantitative carbon fluxes between all components at each time point, like 28 days into the 2009 spring bloom (Fig. 2D, Dataset S1 list all fluxes). The dominant source of organic matter is rst at 0.36 (±0.19) μmolC/L/d, 30% of which is dissolved and particulate chrysolaminarin (chr + phr). These instantaneous fluxes exhibit a higher uncertainty than the integrated fluxes discussed in the previous paragraph, which can be explained by small timing differences (Table S26). The DOM is consumed by a diverse consortium of bacteria, mostly Polaribacter (pol) at 0.46 (±0.22) μmolC/L/d, 35% of which is chr. chr has a through-flux of 0.25 (±0.049) μmolC/L/d and a turnover time of 8.8 (±2.0) days. In the model, phytoplankton and bacteria interact via DOM, but the carbon flux can be traced and used to quantify phytoplankton – bacteria associations. Here, the carbon flux via all DOM types from rst to pol is 0.27 (±0.20) μmolC/L/d, 58% of carbon to pol, making this the second-strongest (after ns3) microbial linkage in the system at this time. This who produces/consumes how much of what when information is the main output of the FluxNet method, and it is critical for moving our understanding of microbial ecosystem functioning beyond bulk parameters like respiration and photosynthesis rates towards a higher resolution.Whereas the 2009 spring bloom illustrates co-blooming of phytoplankton and bacteria, the 2010 bloom shows succession of phytoplankton, DOM and bacteria. Several factors control this pattern in the model. Reinekea (rei) is negative for chrysolaminarin (chr) based on literature (Table S11), but is predicted to have a relatively high affinity for other glucose-containing DOM (gl2) (khrei / Kshrei,gl2 = 63 (±22) L/mmolC/d). A substantial fraction of gl2 is produced relatively early by phytoplankton exudation, and it is the primary substrate for rei at bloom stage 14 days. Alteromonas (alt) is predicted to have a low affinity for gl2 (khalt / Kshalt,gl2 = 0.015 (±0.0097) L/mmolC/d), but it is positive for chr based on literature and predicted to have a high affinity (khalt / Kshalt,chr = 52 (±4.7) L/mmolC/d). Chr is a death (i.e. grazing) product of phytoplankton and produced relatively later in the bloom, and it is the primary substrate for alt at this time. The substrate spectra of bacteria emerge in the analysis, within literature constraints, and can be considered a prediction testable with modern experimental techniques [6].Oligotrophic and copiotrophic carbon processingThe network includes concentrations and fluxes for each bacteria type, and a natural question is to what extend they are correlated. There is increasing awareness that high abundance may not necessarily mean high importance and vice versa, including the over-proportional role of rare species in biogeochemical cycles [32]. In the model, there is a strong correlation between concentration and carbon flux of bacteria, but for the same concentration there is also about an order of magnitude variation in flux (Fig. 3). The spread reflects differences in growth rates during the bloom periods. Some species, like the oligotroph SAR11 (s11), have consistently lower flux and others, like the copiotroph Polaribacter (pol), have consistently higher flux. There are also some, like the cryptic alphaproteobacteria (alx), that go in different directions in different years.Fig. 3: Correlation between spring bloom abundance and importance.Concentration and carbon flux for all model bacteria types during spring bloom periods (see Fig. 2 caption for definition). Lines: All(dashed)/Olig.(thick)/Copi.(thin), log Flux = –0.93/–1.03/–0.81 + 0.93/1.00/0.94 × log Conc., R2 = 0.88/0.92/0.92.Full size imageIt is important to realize that, in dynamic systems, microbial interactions and the corresponding networks are not static [3, 33]. The dynamics of the entire Helgoland flux network over the four-year period is illustrated in an animation, which shows the production of DOM and POM during and after phytoplankton blooms and later blooming of bacteria (Movie S1). These features are also evident in the phytoplankton – DOM – bacteria interactions at two selected time points during the 2009 spring bloom (Fig. 4A, B). At the onset of the bloom, the oligotroph SAR11 (s11) consumes the most DOM, primarily the cryptic species d08, which comes mostly from grazing death of green algae (gre) and exudation by rst. After 28 days the copiotroph pol dominates, which consumes primarily chr, a death product of mostly rst. SAR11 continues to be a major carbon processor in the early parts of the bloom, which was unexpected, because it is an inferior competitor at this time (growth rate s11 = 0.051 vs. pol = 0.15 1/d, bloom average), but can be explained by the higher biomass concentration (s11 = 0.68 vs. pol = 0.13 μmolC/L, bloom start). The flux is proportional to concentration and growth rate, and neither measure alone is a good proxy for the importance of a species [4]. Across all four years, oligotrophic bacteria, defined based on below-average growth rates (literature classifications are often ambiguous), dominate carbon processing for the first 18 days, generally past the phytoplankton peak (Fig. 4C).Fig. 4: Carbon processing during the course of blooms.A Phytoplankton—DOM—bacteria carbon flux network for the start and +28 days of 2009 spring bloom. See Fig. 2 legend. Flux cut off is 0.3%. B Cell concentrations, growth rate and relative carbon processing for s11 and pol for 2009 spring bloom. C Fraction of DOM processed by oligotrophic bacteria and exudate fraction in DOM pool for all blooms. Oligotrophs are defined based on literature as shown in Table S23 or based on below-average growth rates (kg). For the later, the oligotrophic fraction or weight given for type i, is based on fOLIi = kgAVEn / (kgAVEn + kgin), n = 5. kg is the net growth rate calculated from biomass change, plus dilution rate.Full size imageThe use of d08 by s11 and chr by pol in 2009 suggests are more general pattern, i.e., use of exudation products earlier by oligotrophs and death (i.e., grazing) products later by copiotrophs. Across all years, the fraction of DOM produced by exudation decreases during the course of the bloom (Fig. 4C), a common feature of phytoplankton blooms [33]. This is reflected in the diet of these bacterial groups, i.e., for oligotrophs (vs. copiotrophs), exudates make up a higher portion of the diet (27 vs. 18%), and they have a higher affinity for exudates (39 vs. 35 L/mmolC/d), which is also consistent with experimental evidence from another system [7].After the model was developed, while this paper was in peer review, metaproteomic data for the Helgoland Island spring bloom in 2016 were published that suggest that algal storage compounds (e.g., chrysolaminarin) are used throughout the bloom, whereas cell wall-related compounds (e.g., fucose-containing) are used at later bloom stages [34]. Our model also predicts an increase in the consumption of cell-wall vs. storage compounds at later bloom stages (Fig. 5), which validates our outcomes, although a direct comparison is not possible because of the different time.Fig. 5: Consumption of cell wall vs. storage compounds during the course of blooms.Total consumption (all bacteria) in µmolC/L/d of cell wall compounds divided by storage compounds. Cell wall compounds = man (mannan) + glo (glucoromannan) + fcs (FCSP). Storage compounds = chr (chrysolaminarin) + gly (glycogen) + sta (starch). Averages for all four years.Full size imagePhytoplankton functional similarity decouples them from bacteriaAn important question is to what extent the patterns recur from year to year [27]. We compare networks of phytoplankton producers, DOM exchanged and bacteria consumers, as well as phytoplankton – bacteria interactions quantified in absolute (μmolC/L/d moving between phytoplankton X to bacteria Y) and relative (% of carbon for bacteria Y supplied by phytoplankton X) terms (Fig. 6A). All networks show significant similarity so there is recurrence from year to year. The recurrence is higher for DOM than phytoplankton, suggesting that different phytoplankton produce similar DOM, which is expected considering similar composition (e.g., chr in diatoms). There are no phytoplankton producers that recur in the top quartile every year, but chr and others are in the top quartile of DOM exchanged (produced and consumed) every year. The recurrence is lower for bacteria consumers suggesting factors beyond DOM shape the bacteria community.Fig. 6: Recurring patterns and comparison of FluxNet and LSA methods.A Similarity of networks for spring blooms. Error bars are 95% confidence limits. Bray-Curtis similarity was calculated as 1 – Bray-Curtis dissimilarity. Text on top of symbols lists components that recur in the top quartile every year, listed in order of average rank. B Carbon flux networks for top recurring bacterial consumer, top four DOM sources and top coupled phytoplankton. (C&D) LSA network (showing top 15% of significant local similarity scores) and sample time series.Full size imageAn important question is how specific interactions are and how tightly networks are interconnected [35, 36], which depends on the mechanisms of interaction and will affect the recurrence. Consistent with the relatively low recurrence of phytoplankton producers, phytoplankton—bacteria coupling shows relatively low recurrence, i.e. low specificity. The primary substrate for the consumer pol is mostly chr and gl2, although it does change from year to year with varying DOM, consistent with the known assimilation capabilities of pol (Polaribacter) [37] (Fig. 6B). However, the primary associated phytoplankton for pol is different each year, although it is always a diatom. The de-coupling of phytoplankton production and bacteria consumption was also concluded from the lower recurrence of phytoplankton and higher recurrence of bacteria abundance in the same dataset [27]. It suggests that carbon processing is resilient to changes in phytoplankton, which may arise from factors like species invasion or climate change.The above discussion focused on one-way/commensal (phytoplankton  > DOM  > bacteria) interactions, but the network also includes specific two-way/mutualistic phytoplankton-bacteria interactions. Phaeocystis (pha) has the highest exudation fraction and Bacteroidetes nvi the highest affinity for DOM d04, whereas nvi has the highest exudation fraction and pha the highest requirement for micronutrient m15. Such mutualism is observed in other systems and the interactions predicted here can be tested experimentally [20]. Alternatively, experimentally-observed interactions could be used as input to the method, as constraints.Robustness of the analysisTo understand the effect of some of the choices made in the model structure we repeated the analysis with added or removed components or processes. Models without micronutrients or inhibitors produce significantly worse fit to the data (Fig. 7A), highlighting the need for a two-way interaction between phytoplankton and bacteria to maintain diversity. Models with more micronutrients or inhibitors are similar to the basecase. Together, these results provide some justification for the complexity (i.e., number of parameters) in the basecase model. The analysis including osmotrophy (aka absorbotrophy, i.e., phytoplankton can perform heterotrophy) produces a better fit to the observations, but that model was not adopted as basecase, because the osmotrophy process is poorly constrained and includes some probably unrealistic features/fluxes, like significant exudation and uptake of the same substance by one phytoplankton species. Importantly, excluding the runs with worse fit to the observations, the main conclusions (as shown in Figs. 4C and 5A) are the same, confirming that the results are reproducible and robust to some of the choices made in model structure.Fig. 7: Reproducibility of main results.A Total error for runs with different models. “w” or “b” indicates performance is significantly worse (open bars, think lines) or better than basecase, p  ns9 interaction ranks in the top 1% for LSA and FluxNet (relative interaction). However, the lack of mechanistic constraints is evident. One of the strongest links for the 2009 spring bloom (rank 13%) is between the diatom Chaetoceros debilis (cde) and Roseobacters (ros) (Fig. 6C, D). The shifted peaks line up nicely, but the bacteria biomass is higher than that of the phytoplankton and genome analysis suggests ros do not assimilate chrysolaminarin [37], which is a major death product of diatoms. Considering this, growth yield and other competing consumers, it is unlikely that cde is a major source of carbon to ros.Summary and outlookModern observational tools are generating high-resolution descriptions of the components of microbial ecosystems, and an ongoing grand challenge is to use these data to understand how systems function. Our method predicts dynamic mass fluxes between marine phytoplankton and bacteria, which provides insights into the functioning of the ecosystem. Specifically, it showed that there is a strong correlation between concentration and flux of bacteria during blooms, but oligotrophs are relatively less important than copiotrophs. However, due to their higher biomass, they are major carbon processors during early phases of blooms, well past the peak. Oligotrophs grow preferentially on exudation products, which are more abundant earlier in the bloom. Also, our results suggest that phytoplankton are functionally similar in terms of what organic carbon species they produce, and that this decouples them from bacteria.FluxNet is an inference method for microbial time series data that serves the same general purpose as existing empirical inference methods, like LSA [38]. In general, both approaches have strengths and weaknesses (see Introduction) and may complement each other. A main advantage of FluxNet is that it produces quantitative concentrations and fluxes, and associated conclusions (e.g., preferential use of exudates by oligotrophs). Also, it is constrained by mass balance and additional information from the literature (i.e., beyond the time series data), which make the results more realistic.The existing FluxNet code can readily be applied at a higher resolution (microdiversity), explicit representation of other ecosystem components, like viruses and zooplankton, and more processes, like photoheterotrophy and mixotrophy. It may also be applied to understand other microbial ecosystems, like the human gut or wastewater treatment plants. For an inference method it is important to be applicable to various types of observations, including modern environmental -omics observations, like transcript, protein and metabolite levels, and the present model will have to evolve in this direction [39]. The present model includes a relatively simple representation of the various processes, and the current biological understanding supports increasing the mechanistic realism (and complexity). For example, the present version assumes constant composition of DOM produced by phytoplankton, but observations show that it changes with physiology and interaction with bacteria [18, 40]. Also, the model assumes simple first-order dissolution of POM to DOM and direct utilization by bacteria, whereas break-down of especially polysaccharides is often mediated by extracellular enzymes [41]. More

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    Heterothermy as a mechanism to offset energetic costs of environmental and homeostatic perturbations

    1.Wingfield, J. C., Vleck, C. M. & Moore, M. C. Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 264, 419–428 (1992).CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Boonstra, R. Coping with changing northern environments: The role of the stress axis in birds and mammals. Integr. Comp. Biol. 44, 95–108 (2004).PubMed 
    Article 

    Google Scholar 
    3.Lind, J. & Cresswell, W. Determining the fitness consequences of antipredation behavior. Behav. Ecol. 16, 945–956 (2005).Article 

    Google Scholar 
    4.Boyles, J. G., Smit, B. & McKechnie, A. E. A new comparative metric for estimating heterothermy in endotherms. Physiol. Biochem. Zool. 84, 115–123 (2011).PubMed 
    Article 

    Google Scholar 
    5.Boyles, J. G. et al. A global heterothermic continuum in mammals. Glob. Ecol. Biogeogr. 22, 1029–1039 (2013).Article 

    Google Scholar 
    6.Canale, C. I., Levesque, D. L. & Lovegrove, B. G. Tropical heterothermy: Does the exception prove the rule or force a re-definition? In Living in a Seasonal World: Thermoregulatory and Metabolic adaptations (eds Ruf, T. et al.) 29–40 (Springer, Berlin, 2012).Chapter 

    Google Scholar 
    7.Dammhahn, M., Landry-Cuerrier, M., Réale, D., Garant, D. & Humphries, M. M. Individual variation in energy-saving heterothermy affects survival and reproductive success. Funct. Ecol. 31, 866–875 (2017).Article 

    Google Scholar 
    8.McGuire, L. P., Jonasson, K. A. & Guglielmo, C. G. Bats on a budget: Torpor-assisted migration saves time and energy. PLoS ONE 9, e115724 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    9.Glazier, D. S. Metabolic level and size scaling of rates of respiration and growth in unicellular organisms. Funct. Ecol. 23, 963–968 (2009).Article 

    Google Scholar 
    10.Turbill, C. & Stojanovski, L. Torpor reduces predation risk by compensating for the energetic cost of antipredator foraging behaviours. Proc. R. Soc. B Biol. Sci. 285, 1–9 (2018).
    Google Scholar 
    11.Angilletta, M. J., Cooper, B. S., Schuler, M. S. & Boyles, J. G. The evolution of thermal physiology in endotherms. Front. Biosci. 2, 861–881 (2010).
    Google Scholar 
    12.Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford University Press, Oxford, 2009).Book 

    Google Scholar 
    13.Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).ADS 
    CAS 
    Article 

    Google Scholar 
    14.Menzies, A. K. et al. Body temperature, heart rate, and activity patterns of two boreal homeotherms in winter: Homeostasis, allostasis, and ecological coexistence. Funct. Ecol. 34, 2292–2301 (2020).Article 

    Google Scholar 
    15.Humphries, M. M. & Careau, V. Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Integr. Comp. Biol. 51, 419–431 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Daly, M., Behrends, P. R., Wilson, M. I. & Jacobs, L. F. Behavioural modulation of predation risk: Moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Anim. Behav. 44, 1–9 (1992).Article 

    Google Scholar 
    17.Price, M. V., Waser, N. M. & Bass, T. A. Effects of moonlight on microhabitat use by desert rodents. J. Mammal. 65, 353–356 (1984).Article 

    Google Scholar 
    18.Roschlau, C. & Scheibler, E. Foraging behaviour of a desert rodent community: Habitat or moon—Which is more influential?. Ethol. Ecol. Evol. 28, 394–413 (2016).Article 

    Google Scholar 
    19.Mandelik, Y., Jones, M. & Dayan, T. Structurally complex habitat and sensory adaptations mediate the behavioural responses of a desert rodent to an indirect cue for increased predation risk. Evol. Ecol. Res. 5, 501–515 (2003).
    Google Scholar 
    20.Gutman, R., Dayan, T., Levy, O., Schubert, I. & Kronfeld-Schor, N. The effect of the lunar cycle on fecal cortisol metabolite levels and foraging ecology of nocturnally and diurnally active spiny mice. PLoS ONE 6, 35–38 (2011).Article 
    CAS 

    Google Scholar 
    21.Upham, N. S. & Hafner, J. C. Do nocturnal rodents in the great basin desert avoid moonlight?. J. Mammal. 94, 59–72 (2013).Article 

    Google Scholar 
    22.Price, M. V. Structure of desert rodent communities: A critical review of questions and approaches. Integr. Comp. Biol. 26, 39–49 (1986).
    Google Scholar 
    23.Bennett, A. M. et al. Acute changes in whole body corticosterone in response to perceived predation risk: A mechanism for anti-predator behavior in anurans? Gen. Comp. Endocrinol. 229, 62–66 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Hernández, M. C., Navarro-Castilla, Á., Planillo, A., Sánchez-González, B. & Barja, I. The landscape of fear: Why some free-ranging rodents choose repeated live-trapping over predation risk and how it is associated with the physiological stress response. Behav. Process. 157, 125–132 (2018).Article 

    Google Scholar 
    25.Thaker, M., Lima, S. L. & Hews, D. K. Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. Horm. Behav. 56, 51–57 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Preparative actions. Endocr. Rev. 21, 55–89 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Mitra, R. & Sapolsky, R. M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. 105, 5573–5578 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Schroder, G. D. Foraging behavior and home range utilization of the bannertial kangaroo rat (Dipodomys spectabilis). Ecology 60, 657–665 (1979).ADS 
    Article 

    Google Scholar 
    29.Andersen, M. C. & Kay, F. R. Banner-tailed kangaroo rat burrow mounds and desert grassland habitats. J. Arid Environ. 41, 147–160 (1999).ADS 
    Article 

    Google Scholar 
    30.Harris, J. H. An experimental analysis of desert rodent foraging ecology. Ecology 65, 1579–1584 (1984).Article 

    Google Scholar 
    31.Lockard, R. B. Seasonal change in the activity pattern of Dipodomys spectabilis. J. Mammal. 59, 563–568 (1978).Article 

    Google Scholar 
    32.Lockard, R. B. & Owings, D. H. Seasonal variation in moonlight avoidance by bannertail kangaroo rats. J. Mammal. 55, 189–193 (1974).CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Dawson, W. R. The relaxation of oxygen consumption to temperature in desert rodents. J. Mammal. 36, 543–553 (1955).Article 

    Google Scholar 
    34.Hart, J. S. Rodents. In Mammals. 1–149 (Academic Press, 1971).35.Quispe, R., Trappschuh, M., Gahr, M. & Goymann, W. Towards more physiological manipulations of hormones in field studies: Comparing the release dynamics of three kinds of testosterone implants, silastic tubing, time-release pellets and beeswax. Gen. Comp. Endocrinol. 212, 100–105 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Sahores, A. et al. Novel, low cost, highly effective, handmade steroid pellets for experimental studies. PLoS ONE 8, e64049 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Sopinka, N. M. et al. Manipulating glucocorticoids in wild animals: Basic and applied perspectives. Conserv. Physiol. 3, cov031 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    38.Akana, S. F. et al. Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. Endocrinology 131, 585–594 (1992).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Bush, V. L., Middlemiss, D. N., Marsden, C. A. & Fone, K. C. F. Implantation of a slow release rorticosterone pellet induces long-term alterations in serotonergic neurochemistry in the rat brain. J. Neuroendocrinol. 15, 607–613 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Meyer, J. S., Micco, D. J., Stephenson, B. S., Krey, L. C. & McEwen, B. S. Subcutaneous implantation method for chronic glucocorticoid replacement therapy. Physiol. Behav. 22, 867–870 (1979).CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Chang, C. C. & Kincl, F. A. Sustained release hormonal preparations: 3. Biological effectiveness of 6-methyl-1717α-acetoxypregna-4,6-diene-3,20-dione. Steroids 12, 689–696 (1968).CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Kratochvíl, P., Benagiano, G. & Kincl, F. A. Sustained release hormonal preparations. 6. Permeability constant of various steroids. Steroids 15, 505–511 (1970).PubMed 
    Article 

    Google Scholar 
    43.Nash, H. A., Robertson, D. N., Moo Young, A. J. & Atkinson, L. E. Steroid release from silastic capsules and rods. Contraception 18, 367–394 (1978).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Borrow, A. P. et al. Chronic variable stress alters hypothalamic–pituitary–adrenal axis function in the female mouse. Physiol. Behav. 209, 112613 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    45.Lajud, N., Roque, A., Cajero, M., Gutiérrez-Ospina, G. & Torner, L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 37, 410–420 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    46.Mateo, J. M. & Cavigelli, S. A. A validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels. Physiol. Biochem. Zool. 78, 1069–1084 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Touma, C., Palme, R. & Sachser, N. Analyzing corticosterone metabolites in fecal samples of mice: A noninvasive technique to monitor stress hormones. Horm. Behav. 45, 10–22 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Torres-Medina, F. et al. Corticosterone implants produce stress-hyporesponsive birds. J. Exp. Biol. 221, jeb173864 (2018).PubMed 
    Article 

    Google Scholar 
    49.Adzic, M. et al. Acute or chronic stress induce cell compartment-specific phosphorylation of glucocorticoid receptor and alter its transcriptional activity in Wistar rat brain. J. Endocrinol. 202, 87–97 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Ellis, M. V. Development of a compact system for field euthanasia of small mammals. J. Mammal. 98, 1211–1214 (2017).Article 

    Google Scholar 
    51.Guglielmo, C. G., McGuire, L. P., Gerson, A. R. & Seewagen, C. L. Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J. Ornithol. 152, 75 (2011).Article 

    Google Scholar 
    52.McGuire, L. P. & Guglielmo, C. G. Quantitative magnetic resonance: A rapid, noninvasive body composition analysis technique for live and salvaged bats. J. Mammal. 91, 1375–1380 (2010).Article 

    Google Scholar 
    53.Warner, D. A., Johnson, M. S. & Nagy, T. R. Validation of body condition indices and quantitative magnetic resonance in estimating body composition in a small lizard. J. Exp. Zool. Part A Ecol. Genet. Physiol. 325, 588–597 (2016).CAS 
    Article 

    Google Scholar 
    54.Boyles, J. G. A brief introduction to methods for describing body temperature in endotherms. Physiol. Biochem. Zool. 92, 365–372 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Monson, G. & Kessler, W. Life history notes on the banner-tailed kangaroo rat, Merriam’s kangaroo rat, and the white-throated wood rat in Arizona and New Mexico. J. Wildl. Manag. 4, 37–43 (1940).Article 

    Google Scholar 
    56.Smit, B., Boyles, J. G., Brigham, R. M. & Mckechnie, A. E. Torpor in dark times: patterns of heterothermy are associated with the lunar cycle in a nocturnal bird. J. Biol. Rhythms 26, 241–248 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Kay, F. R. & Whitford, W. G. The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in southcentral New Mexico. Am. Midl. Nat. 99, 270–279 (1978).Article 

    Google Scholar 
    58.Randall, J. A. Territorial-defense interactions with neighbors and strangers in banner-tailed kangaroo rats. J. Mammal. 70, 308–315 (1989).Article 

    Google Scholar 
    59.Randall, J. A. Mating strategies of a nocturnal, desert rodent (Dipodomys spectabilis). Behav. Ecol. Sociobiol. 28, 215–220 (1991).Article 

    Google Scholar 
    60.Ward, D. W. & Randall, J. A. Territorial defense in the bannertail kangaroo rat (Dipodomys spectabilis): footdrumming and visual threats. Behav. Ecol. Sociobiol. 20, 323–328 (1987).Article 

    Google Scholar 
    61.Brown, J. S., Kotler, B. P., Smith, R. J. & Wirtz, W. O. The effects of owl predation on the foraging behavior of heteromyid rodents. Oecologia 76, 408–415 (1988).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Navarro-Castilla, Á., Barja, I. & Díaz, M. Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination and common genet cues. Curr. Zool. 64, 409–417 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Sargunaraj, F., Kotler, B. P., Juliana, J. R. S. & Wielebnowski, N. Stress as an adaptation II: Does experimental cortisol supplementation affect predation risk assessment in foraging gerbils?. Evol. Ecol. Res. 18, 587–598 (2017).
    Google Scholar 
    64.Voellmy, I. K., Goncalves, I. B., Barrette, M. F., Monfort, S. L. & Manser, M. B. Mean fecal glucocorticoid metabolites are associated with vigilance, whereas immediate cortisol levels better reflect acute anti-predator responses in meerkats. Horm. Behav. 66, 759–765 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Kotler, B. P., Brown, J., Mukherjee, S., Berger-Tal, O. & Bouskila, A. Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc. R. Soc. B Biol. Sci. 277, 1469–1474 (2010).Article 

    Google Scholar 
    66.Pravosudov, V. V. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc. R. Soc. B Biol. Sci. 270, 2599–2604 (2003).CAS 
    Article 

    Google Scholar 
    67.Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    68.Humphries, M. M., Kramer, D. L. & Thomas, D. W. The role of energy availability in mammalian hibernation: An experimental test in free-ranging eastern chipmunks. Physiol. Biochem. Zool. 76, 165–179 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    69.Munro, D., Thomas, D. W. & Humphries, M. M. Torpor patterns of hibernating eastern chipmunks Tamias striatus vary in response to the size and fatty acid composition of food hoards. J. Anim. Ecol. 74, 692–700 (2005).Article 

    Google Scholar 
    70.Ernest, S. K. M. et al. Rodents, plants, and precipitation: Spatial and temporal dynamics of consumers and resources. Oikos 88, 470–482 (2017).Article 

    Google Scholar 
    71.Warne, R. W., Pershall, A. D. & Wolf, B. O. Linking precipitation and C3–C4 plant production to resource dynamics in higher-trophic-level consumers. Ecology 91, 1628–1638 (2010).PubMed 
    Article 

    Google Scholar 
    72.Warne, R. W., Baer, S. G. & Boyles, J. G. Community physiological ecology. Trends Ecol. Evol. 34, 510–518 (2019).PubMed 
    Article 

    Google Scholar  More

  • in

    Aposematism facilitates the diversification of parental care strategies in poison frogs

    1.Clutton-Brock, T. H. The Evolution of Parental Care Vol. 64 (Princeton University Press, 1991).Book 

    Google Scholar 
    2.Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, 2012).Book 

    Google Scholar 
    3.Hansell, M. Bird Nests and Construction Behaviour (Cambridge University Press, 2000).Book 

    Google Scholar 
    4.Doody, J. S., Freedberg, S. & Keogh, J. S. Communal egg-laying in reptiles and amphibians: evolutionary patterns and hypotheses. Q. Rev. Biol. 84, 229–252 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Boness, D. J. & Don Bowen, W. The evolution of maternal care in pinnipeds: new findings raise questions about the evolution of maternal feeding strategies. Bioscience 46, 645–654 (1996).Article 

    Google Scholar 
    6.Salomon, M., Mayntz, D., Toft, S. & Lubin, Y. Maternal nutrition affects offspring performance via maternal care in a subsocial spider. Behav. Ecol. Sociobiol. 65, 1191–1202 (2011).Article 

    Google Scholar 
    7.Summers, K. Mating and aggressive behaviour in dendrobatid frogs from Corcovado National Park, Costa Rica: a comparative study. Behaviour 137, 7–24 (2000).Article 

    Google Scholar 
    8.Li, D. & Jackson, R. R. A predator’s preference for egg-carrying prey: a novel cost of parental care. Behav. Ecol. Sociobiol. 55, 129–136 (2003).Article 

    Google Scholar 
    9.Stiver, K. A. & Alonzo, S. H. Parental and mating effort: is there necessarily a trade-off?. Ethology 115, 1101–1126 (2009).Article 

    Google Scholar 
    10.Ercit, K., Martinez-Novoa, A. & Gwynne, D. T. Egg load decreases mobility and increases predation risk in female black-horned tree crickets (Oecanthus nigricornis). PLoS ONE 9, e110298 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    11.Ghalambor, C. K. & Martin, T. E. Fecundity-survival trade-offs and parental risk-taking in birds. Science 292, 494–497 (2001).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    12.Thorogood, R., Ewen, J. G. & Kilner, R. M. Sense and sensitivity: responsiveness to offspring signals varies with the parents’ potential to breed again. Philos. Trans. R. Soc. B. 278, 2638–2645 (2011).
    Google Scholar 
    13.Stearns, S. C. The Evolution of Life Histories (Oxford University Press, 1992).
    Google Scholar 
    14.Weir, B. J. & Rowlands, I. Reproductive strategies of mammals. Annu. Rev. Ecol. Evol. Syst. 4, 139–163 (1973).Article 

    Google Scholar 
    15.Kvarnemo, C. In Evolutionary Behavioral Ecology (ed. FoxWestneat, C. W.) (Oxford University Press, 2010).
    Google Scholar 
    16.Alonso-Alvarez, C. & Velando, A. Benefits and costs of parental care. The evolution of parental care, 40–61 (2012).17.Farmer, C. Parental care: the key to understanding endothermy and other convergent features in birds and mammals. Am. Nat. 155, 326–334 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Ar, A. & Yom-Tov, Y. The evolution of parental care in birds. Evolution 32, 655–669 (1978).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Gubernick, D. J. Parent and infant attachment in mammals. In Parental care in mammals 243–305 (Springer, 1981).20.Case, T. J. Endothermy and parental care in the terrestrial vertebrates. Am. Nat. 112, 861–874 (1978).Article 

    Google Scholar 
    21.Gross, M. R. & Shine, R. Parental care and mode of fertilization in ectothermic vertebrates. Evolution 35, 775–793 (1981).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Balshine, S. Patterns of parental care in vertebrates. Evol. Parental Care 62, 80 (2012).
    Google Scholar 
    23.Furness, A. I. & Capellini, I. The evolution of parental care diversity in amphibians. Nat. Commun. 10, 1–12 (2019).CAS 
    Article 

    Google Scholar 
    24.Schulte, L. M., Ringler, E., Rojas, B. & Stynoski, J. L. Developments in amphibian parental care research: history, present advances, and future perspectives. Herpetol. Monogr. 34, 71–97 (2020).Article 

    Google Scholar 
    25.Wells, K. D. The Ecology and Behavior of Amphibians (University of Chicago Press, 2010).
    Google Scholar 
    26.Weygoldt, P. Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae). J. Zoolog. Syst. Evol. 25, 51–67 (1987).Article 

    Google Scholar 
    27.Summers, K. & Tumulty, J. in Sexual Selection 289–320 (Elsevier, 2014).28.Lehtinen, R., Lannoo, M. J. & Wassersug, R. J. Phytotelm-breeding anurans: past, present and future research. Misc. Publ. Museum Zool. Univ. Michigan 193, 1–9 (2004).
    Google Scholar 
    29.Brust, D. G. Maternal brood care by Dendrobates pumilio: a frog that feeds its young. J. Herpetol. 27, 96–98 (1993).Article 

    Google Scholar 
    30.Bourne, G. R., Collins, A. C., Holder, A. M. & McCarthy, C. L. Vocal communication and reproductive behavior of the frog Colostethus beebei in Guyana. J. Herpetol. 35, 272–281 (2001).Article 

    Google Scholar 
    31.Schulte, L. M. Feeding or avoiding? Facultative egg feeding in a Peruvian poison frog (Ranitomeya variabilis). Ethol. Ecol. Evol. 26, 58–68. https://doi.org/10.1080/03949370.2013.850453 (2014).Article 

    Google Scholar 
    32.Beck, K. B., Loretto, M.-C., Ringler, M., Hödl, W. & Pašukonis, A. Relying on known or exploring for new? Movement patterns and reproductive resource use in a tadpole-transporting frog. PeerJ 5, e3745 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Pašukonis, A., Loretto, M.-C. & Rojas, B. How far do tadpoles travel in the rainforest? Parent-assisted dispersal in poison frogs. Evol. Ecol. 33, 613–623 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Summers, K. Metabolism and parental care in ectotherms: a comment on Beekman et al. Behav. Ecol. 30, 593–594 (2019).Article 

    Google Scholar 
    35.Santos, J. C. & Cannatella, D. C. Phenotypic integration emerges from aposematism and scale in poison frogs. Proc. Natl. Acad. Sci. 108, 6175–6180 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Stynoski, J. L., Schulte, L. M. & Rojas, B. Poison frogs. Curr. Biol. 25, R1026–R1028 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Rojas, B., Valkonen, J. & Nokelainen, O. Aposematism. Curr. Biol. 25, R350–R351 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Poulton, E. B. The Colours of Animals: Their Meaning and Use, Especially Considered in the Case of Insects (D. Appleton, 1990).
    Google Scholar 
    39.Santos, J. C., Coloma, L. A. & Cannatella, D. C. Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc. Natl. Acad. Sci. 100, 12792–12797 (2003).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Vences, M. et al. Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Org. Divers. Evol. 3, 215–226 (2003).Article 

    Google Scholar 
    41.Daly, J. W. et al. An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 32, 657–663 (1994).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Saporito, R. A., Spande, T. F., Garraffo, H. M. & Donnelly, M. A. Arthropod alkaloids in poison frogs: a review of the dietary hypothesis. Heterocycles 79, 277–297 (2009).CAS 
    Article 

    Google Scholar 
    43.Santos, J. C. et al. Aposematism increases acoustic diversification and speciation in poison frogs. Philos. Trans. R. Soc. B. 281, 20141761 (2014).
    Google Scholar 
    44.Caldwell, J. P. The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). J. Zool. 240, 75–101 (1996).Article 

    Google Scholar 
    45.Summers, K., Symula, R., Clough, M. & Cronin, T. Visual mate choice in poison frogs. Philos. Trans. R. Soc. B. 266, 2141–2145 (1999).CAS 

    Google Scholar 
    46.Duellman, W. E. & Trueb, L. Biology of Amphibians (JHU Press, 1994).
    Google Scholar 
    47.Summers, K. & McKeon, C. S. The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc. Publ. Mus. Zool. Univ. Mich. 193, 55–73 (2004).
    Google Scholar 
    48.Summers, K., Sea McKeon, C. & Heying, H. The evolution of parental care and egg size: a comparative analysis in frogs. Philos. Trans. R. Soc. B. 273, 687–692 (2006).
    Google Scholar 
    49.Wells, K. D. Courtship and parental behavior in a Panamanian poison-arrow frog (Dendrobates auratus). Herpetologica 34, 148–155 (1978).
    Google Scholar 
    50.Summers, K. Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus. Anim. Behav. 37, 797–805 (1989).Article 

    Google Scholar 
    51.Summers, K. Paternal care and the cost of polygyny in the green dart-poison frog. Behav. Ecol. Sociobiol. 27, 307–313 (1990).Article 

    Google Scholar 
    52.Summers, K. & Amos, W. Behavioral, ecological, and molecular genetic analyses of reproductive strategies in the Amazonian dart-poison frog, Dendrobates ventrimaculatus. Behav. Ecol. 8, 260–267 (1997).Article 

    Google Scholar 
    53.Limerick, S. Courtship behavior and oviposition of the poison-arrow frog Dendrobates pumilio. Herpetologica 36, 69–71 (1980).
    Google Scholar 
    54.Pröhl, H. & Hödl, W. Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio. Behav. Ecol. Sociobiol. 46, 215–220 (1999).Article 

    Google Scholar 
    55.Brown, J. L., Morales, V. & Summers, K. A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am. Nat. 175, 436–446 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Yang, Y., Blomenkamp, S., Dugas, M. B., Richards-Zawacki, C. L. & Pröhl, H. Mate choice versus mate preference: inferences about color-assortative mating differ between field and lab assays of poison frog behavior. Am. Nat. 193, 598–607 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Wells, K. D. Behavoral ecology and social organization of a dendrobatid frog (Colostethus inguinalis). Behav. Ecol. Sociobiol. 6, 199–209 (1980).Article 

    Google Scholar 
    58.Luddecke, H. Behavioral aspects of the reproductive biology of the Andean frog Colostethus palmatus (Amphibia: Dendrobatidae). Rev. Acad. Colomb. Cienc. Exact. Fis. Nat. 23, S303–S303 (1999).
    Google Scholar 
    59.Montanarin, A., Kaefer, I. L. & Lima, A. P. Courtship and mating behaviour of the brilliant-thighed frog Allobates femoralis from Central Amazonia: Implications for the study of a species complex. Ethol. Ecol. Evol. 23, 141–150 (2011).Article 

    Google Scholar 
    60.Ursprung, E., Ringler, M., Jehle, R. & Hoedl, W. Strong male/male competition allows for nonchoosy females: High levels of polygynandry in a territorial frog with paternal care. Mol. Ecol. 20, 1759–1771 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Stückler, S. et al. Spatio-temporal characteristics of the prolonged courtship in brilliant-thighed poison frogs, Allobates femoralis. Herpetologica 75, 268–279 (2019).Article 

    Google Scholar 
    62.Symula, R., Schulte, R. & Summers, K. Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis. Philos. Trans. R. Soc. B 268, 2415–2421 (2001).CAS 

    Google Scholar 
    63.Summers, K. Mating strategies in two species of dart-poison frogs: a comparative study. Anim. Behav. 43, 907–919 (1992).Article 

    Google Scholar 
    64.Rojas, B. & Pašukonis, A. From habitat use to social behavior: natural history of a voiceless poison frog, Dendrobates tinctorius. PeerJ 7, e7648 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Maan, M. E. & Cummings, M. E. Poison frog colors are honest signals of toxicity, particularly for bird predators. Am. Nat. 179, E1–E14 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Grant, T. et al. Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull. Am. Mus. Nat. 2006, 1–262 (2006).
    Google Scholar 
    67.Grant, T. et al. Phylogenetic systematics of dart-poison frogs and their relatives revisited (Anura: Dendrobatoidea). S. Am. J. Herpetol. 12, S1–S90 (2017).Article 

    Google Scholar 
    68.Duellman, W. E. Frogs of the genus Colostethus (Anura; Dendrobatidae) in the Andes of northern Peru (2004).69.Fairbairn, D. J. Odd Couples: Extraordinary Differences Between the Sexes in the Animal Kingdom (Princeton University Press, 2013).Book 

    Google Scholar 
    70.Fairbairn, D. J., Blanckenhorn, W. U. & Székely, T. Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (Oxford University Press, 2007).Book 

    Google Scholar 
    71.Vági, B., Végvári, Z., Liker, A., Freckleton, R. P. & Székely, T. Parental care and the evolution of terrestriality in frogs. Philos. Trans. R. Soc. B. 286, 20182737 (2019).
    Google Scholar 
    72.Gosner, K. L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190 (1960).
    Google Scholar 
    73.Kelber, A., Vorobyev, M. & Osorio, D. Animal colour vision–behavioural tests and physiological concepts. Biol. Rev. 78, 81–118 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Renoult, J. P., Kelber, A. & Schaefer, H. M. Colour spaces in ecology and evolutionary biology. Biol. Rev. 92, 292–315 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Endler, J. A. On the measurement and classification of colour in studies of animal colour patterns. Biol. J. Linn. Soc. 41, 315–352 (1990).Article 

    Google Scholar 
    76.Kemp, D. J. et al. An integrative framework for the appraisal of coloration in nature. Am. Nat. 185, 705–724 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Troscianko, J. & Stevens, M. Image calibration and analysis toolbox—a free software suite for objectively measuring reflectance, colour and pattern. Methods. Ecol. Evol. 6, 1320–1331 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Maia, R. & White, T. E. Comparing colors using visual models. Behav. Ecol. 29, 649–659 (2018).Article 

    Google Scholar 
    79.Bergeron, Z. T. & Fuller, R. C. Using human vision to detect variation in avian coloration: how bad is it?. Am. Nat. 191, 269–276 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    80.Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    81.Yang, Z., Kumar, S. & Nei, M. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141, 1641–1650 (1995).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    83.Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series. B. Stat. Methodo. 57, 289–300 (1995).MathSciNet 
    MATH 

    Google Scholar 
    84.Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).Article 

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

    Google Scholar 
    86.Barker, D., Meade, A. & Pagel, M. Constrained models of evolution lead to improved prediction of functional linkage from correlated gain and loss of genes. Bioinformatics 23, 14–20 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    87.Lindstedt, C., Boncoraglio, G., Cotter, S. C., Gilbert, J. D. J. & Kilner, R. M. Parental care shapes evolution of aposematism and provides lifelong protection against predators. bioRxiv 25, 644864 (2019).
    Google Scholar 
    88.Donnelly, M. A. Demographic effects of reproductive resource supplementation in a territorial frog, Dendrobates pumilio. Ecol. Monogr. 59, 207–221 (1989).Article 

    Google Scholar 
    89.Rojas, B. & Endler, J. A. Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius. Evol. Ecol. 27, 739–753 (2013).Article 

    Google Scholar 
    90.Pröhl, H. Territorial behavior in dendrobatid frogs. J. Herpetol. 39, 354–365 (2005).Article 

    Google Scholar 
    91.Speed, M. P., Brockhurst, M. A. & Ruxton, G. D. The dual benefits of aposematism: predator avoidance and enhanced resource collection. Evolution 64, 1622–1633 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    92.Fincke, O. M. Organization of predator assemblages in Neotropical tree holes: effects of abiotic factors and priority. Ecol. Entomol. 24, 13–23 (1999).Article 

    Google Scholar 
    93.Summers, K. The effects of cannibalism on Amazonian poison frog egg and tadpole deposition and survivorship in Heliconia axil pools. Oecologia 119, 557–564 (1999).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    94.McKeon, C. S. & Summers, K. Predator driven reproductive behavior in a tropical frog. Evol. Ecol. 27, 725–737 (2013).Article 

    Google Scholar 
    95.Amézquita, A., Castro, L., Arias, M., González, M. & Esquivel, C. Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex. Evol. Ecol. 27, 769–782 (2013).Article 

    Google Scholar 
    96.Lawrence, J. P. et al. Weak warning signals can persist in the absence of gene flow. PNAS 116, 19037–19045 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Lack, D. The natural regulation of animal numbers. The Natural Regulation of Animal Numbers. (1954).98.Williams, G. C. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (1966).Article 

    Google Scholar 
    99.Brown, J., Morales, V. & Summers, K. Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis. J. Evol. Biol. 21, 1534–1543 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    100.Brown, J. L., Morales, V. & Summers, K. Tactical reproductive parasitism via larval cannibalism in Peruvian poison frogs. Biol. Lett. 5, 148–151 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    101.Brown, J. L., Morales, V. & Summers, K. Home range size and location in relation to reproductive resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Anim. Behav. 77, 547–554 (2009).Article 

    Google Scholar 
    102.Kok, P. J., Willaert, B. & Means, D. B. A new diagnosis and description of Anomaloglossus roraima (La Marca, 1998) (Anura: Aromobatidae: Anomaloglossinae), with description of its tadpole and call. S. Am. J. Herpetol. 8, 29–45 (2013).Article 

    Google Scholar 
    103.Pašukonis, A. et al. The significance of spatial memory for water finding in a tadpole-transporting frog. Anim. Behav. 116, 89–98 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    104.Pašukonis, A., Warrington, I., Ringler, M. & Hödl, W. Poison frogs rely on experience to find the way home in the rainforest. Biol. Lett. 10, 20140642 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    105.Poelman, E. H. & Dicke, M. Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evol. Ecol. 21, 215–227 (2007).Article 

    Google Scholar 
    106.Caldwell, J. P. & de Araujo, M. C. Cannibalistic interactions resulting from indiscriminate predatory behavior in tadpoles of poison frogs (Anura: Dendrobatidae). Biotropica 30, 92–103 (1998).Article 

    Google Scholar 
    107.Gray, H. M., Summers, K. & Ibáñez, R. Kin discrimination in cannibalistic tadpoles of the Green Poison Frog, Dendrobates auratus (Anura, Dendrobatidae). Phyllomedusa (2009).108.Rojas, B. Strange parental decisions: fathers of the dyeing poison frog deposit their tadpoles in pools occupied by large cannibals. Behav. Ecol. Sociobiol. 68, 551–559 (2014).Article 

    Google Scholar 
    109.Schulte, L. M. & Mayer, M. Poison frog tadpoles seek parental transportation to escape their cannibalistic siblings. J. Zool. 303, 83–89, 12472 (2017).110.Ringler, E., Pašukonis, A., Hödl, W. & Ringler, M. Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care. Front. Zool. 10, 67 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    111.Pröhl, H. Variation in male calling behaviour and relation to male mating success in the strawberry poison frog (Dendrobates pumilio). Ethology 109, 273–290 (2003).Article 

    Google Scholar 
    112.Summers, K. & Earn, D. J. The cost of polygyny and the evolution of female care in poison frogs. Biol. J. Linn. Soc. 66, 515–538 (1999).Article 

    Google Scholar 
    113.Ringler, E. et al. Flexible compensation of uniparental care: female poison frogs take over when males disappear. Behav. Ecol. 26, 1219–1225 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    114.Pyron, R. A. & Wiens, J. J. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61, 543–583 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    115.Streicher, J. W. et al. Evaluating methods for phylogenomic analyses, and a new phylogeny for a major frog clade (Hyloidea) based on 2214 loci. Mol. Phylogenet. Evol. 119, 128–143 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    116.Gilbert, J. D. Thrips domiciles protect larvae from desiccation in an arid environment. Behav. Ecol. 25, 1338–1346 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    117.Hime, P. M. et al. Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life. Syst. Biol. 70, 49–66 (2021).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    118.Moen, D. S., Morlon, H. & Wiens, J. J. Testing convergence versus history: convergence dominates phenotypic evolution for over 150 million years in frogs. Syst. Biol. 65, 146–160 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    119.Gomez-Mestre, I., Pyron, R. A. & Wiens, J. J. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66, 3687–3700 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    120.Liu, Y., Day, L. B., Summers, K. & Burmeister, S. S. Learning to learn: advanced behavioural flexibility in a poison frog. Anim. Behav. 111, 167–172 (2016).Article 

    Google Scholar 
    121.Liu, Y., Day, L. B., Summers, K. & Burmeister, S. S. A cognitive map in a poison frog. J. Exp. Biol. 222, jeb97467 (2019).Article 

    Google Scholar 
    122.Liu, Y., Jones, C. D., Day, L. B., Summers, K. & Burmeister, S. S. Cognitive phenotype and differential gene expression in a hippocampal homologue in two species of frog. Integr. Comp Biol. 60, 1007–1023 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Metal bioaccumulation alleviates the negative effects of herbivory on plant growth

    1.Pollard, A. J., Reeves, R. & Baker, A. J. M. Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci. 217–218, 8–17 (2014).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    2.Whiting, S. N. et al. Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor. Ecol. 12, 106–116 (2004).Article 

    Google Scholar 
    3.Baker, A. J. M. Accumulators and excluders—Strategies in the response of plants to heavy metals. J. Plant Nutr. 3, 643–654 (1981).CAS 
    Article 

    Google Scholar 
    4.Ernest, W. H. O. Evolution of metal hyperaccumulation and phytoremediation hype. New Phytol. 146, 357–358 (2000).Article 

    Google Scholar 
    5.Pollard, A. J., Powell, K. D., Harper, F. A. & Smith, J. A. C. The genetic basis of metal hyperaccumulation in plants. Crit. Rev. Plant Sci. 21, 539–566 (2002).CAS 
    Article 

    Google Scholar 
    6.Antosiewicz, D. M. Adaptation of plants to an environmental polluted with heavy metals. Acta Soc. Bot. Pol. 61, 281–299 (1992).CAS 
    Article 

    Google Scholar 
    7.Brooks, R. R., Lee, J., Reeves, R. D. & JaVré, T. Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J. Geochem. Explor. 7, 49–77 (1977).CAS 
    Article 

    Google Scholar 
    8.Jansen, S., Broadley, M., Robbrecht, E. & Smets, E. Aluminium hyperaccumulation in angiosperms: A review of its phylogenetic signifficance. Bot. Rev. 68, 235–269 (2002).Article 

    Google Scholar 
    9.van der Ent, A., Baker, A. J. M., Reeves, R. D., Pollard, J. & Schat, H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 362, 319–334 (2013).Article 
    CAS 

    Google Scholar 
    10.Metali, F., Salim, K. A. & Burslem, D. F. R. P. Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plants. New Phytol. 193, 637–649 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Noret, N., Meerts, P., Vanhaelen, M., Dos Santos, A. & Escarré, J. Do metal-rich plants deter herbivores? A field test of the defence hypothesis. Oecologia 152, 92–100 (2007).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Martens, S. N. & Boyd, R. S. The ecological significance of nickel hyperaccumulation: A plant chemical defense. Oecologia 98, 379–384 (1994).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Boyd, R. S. & Martens, S. N. The significance of metal hyperaccumulation for biotic interactions. Chemoecology 8, 1–7 (1998).CAS 
    Article 

    Google Scholar 
    14.Hanson, B. et al. Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol. 159, 461–469 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Rascio, N. & Navari-Izzo, F. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting?. Plant Sci. 180, 169–181 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Freeman, J. L., Garcia, D., Kim, D., Hopf, A. & Salt, D. E. Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol. 137, 1082–1091 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Vesk, P. A. & Reichman, S. M. Hyperaccumulators and herbivores—A Bayesian meta-analysis of feeding choice trials. J. Chem. Ecol. 35, 289–296 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Pollard, A. J. & Baker, A. J. M. Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens (Brassicaceae). New Phytol. 135, 655–658 (1997).CAS 
    Article 

    Google Scholar 
    19.Ribeiro, S. P. & Brown, V. K. Insect herbivory in tree crowns of Tabebuia aurea and T. ochracea (Bignoniaceae): Contrasting the Brazilian Cerrado with the wetland Pantanal Matogrossense. Selbyana 20, 159–170 (1999).
    Google Scholar 
    20.Strauss, S. Y., Rudgers, J. A., Lau, J. A. & Irwin, R. E. Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17, 278–285 (2002).Article 

    Google Scholar 
    21.Hossain, M. A., Piyatida, P., Teixeria da Silva, J. A. & Fujita, M. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 01–37 (2012).Article 
    CAS 

    Google Scholar 
    22.McNaughton, S. J. Compensatory plant growth as a response to herbivory. Oikos 40, 329–336 (1983).Article 

    Google Scholar 
    23.Kozlov, M. V., Lanta, V., Zverev, V. E. & Zvereva, E. L. Delayed local responses of downy birch to damage by leafminers and leafrollers. Oikos 121, 428–434 (2012).Article 

    Google Scholar 
    24.Maestri, E., Marmiroli, M., Visioli, G. & Marmiroli, N. Metal tolerance and hyperaccumulation: Costs and trade-offs between traits and environment. Environ. Exp. Bot. 68, 1–13 (2010).CAS 
    Article 

    Google Scholar 
    25.Khan, A. et al. Heavy metals effects on plant growth and dietary intake of trace metals in vegetables cultivated in contaminated soil. Int. J. Environ. Sci. Technol. 16, 2295–2304 (2019).CAS 
    Article 

    Google Scholar 
    26.Barceló, J. & Poschenrieder, C. Respuestas de las plantas a la contaminación por metales pesados. Suelo y Planta 2, 345–361 (1992).
    Google Scholar 
    27.Ribeiro, S. P. et al. Plant defense against leaf herbivory based on metal accumulation: Examples from a tropical high altitude ecosystem. Plant Spec. Biol. 32, 147–155 (2017).Article 

    Google Scholar 
    28.Boyd, R. S. & Martens, S. N. Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore. Oikos 70, 21–25 (1994).CAS 
    Article 

    Google Scholar 
    29.Boyd, R. S. & Jhee, E. M. A test of elemental defence against slugs by Ni in hyperaccumulator and non-hyperaccumulator Streptanthus species. Chemoecology 15, 179–185 (2005).CAS 
    Article 

    Google Scholar 
    30.Freeman, J. L. et al. Selenium accumulation protects plants from herbivory by Orthoptera due to toxicity and deterrence. New Phytol. 175, 490–500 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Mathews, S., Ma, L. Q., Rathinasabapathi, C. & Stamps, R. H. Arsenic reduced scale-insect infestation on arsenic hyperaccumulator Pteris vittata L. Environ. Exp. Bot. 65, 282–286 (2009).CAS 
    Article 

    Google Scholar 
    32.Coleman, C. M., Boyd, R. S. & Eubanks, M. D. Extending the elemental defense hypothesis: Dietary metal concentrations below hyperaccumulator levels could harm herbivores. J. Chem. Ecol. 31, 1669–1681 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Scheirs, J., Vandevyvere, I., Wollaert, K., Blust, R. & De Bruyn, L. Plant-mediated effects of heavy metal pollution on host choice of a grass miner. Environ. Pollut. 143, 138–145 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Boyd, R. S. The defence hypothesis of elemental hyperaccumulation: Status, challenges and new directions. Plant Soil 293, 53–176 (2007).Article 
    CAS 

    Google Scholar 
    35.Porto, M. L. & Silva, M. F. F. Tipos de vegetação metalófila em áreas da Serra de Carajás e de Minas Gerais, Brasil. Acta Bot. Bras. 3, 13–21 (1989).Article 

    Google Scholar 
    36.Teixeira, W. A. & Lemos-Filho, J. P. Metais pesados em folhas de espécies lenhosas colonizadoras de uma área de mineração de ferro em Itabirito, Minas Gerais. Rev. Arvore 22, 381–388 (1998).
    Google Scholar 
    37.Lorenzi, H. Árvores Brasileiras: Manual De Identificação e Cultivo de Plantas Arbóreas Nativas Do Brasil Vol. 3 (Nova Odessa: Instituto Plantarum, 2009)38.Pérez, J. F. M. et al. Sistema de manejo para a candeia—Eremanthus erythropappus (DC.) Macleish—a opção do sistema de corte seletivo. Cerne 10, 257–273 (2004).
    Google Scholar 
    39.Keane, B., Collier, M., Shann, J. & Rogstad, S. Metal content of dandelion (Taraxacum officinale) leaves in relation to soil contamination and airborne particulate matter. Sci. Total Environ. 281, 63–78 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Assunção, A. G. L., Schat, H. & Aarts, M. G. M. Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol. 159, 351–360 (2003).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    41.Basta, N. T., Ryan, J. A. & Chaney, R. L. Trace element chemistry in residual-treated soil: Key concepts and metal bioavailability. J. Environ. Qual. 34, 49–63 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Evans, L. J. Chemistry of metal retention by soils—Several processes are explained. Environ. Sci. Technol. 23, 1046–1056 (1989).ADS 
    CAS 
    Article 

    Google Scholar 
    43.Campos, N. B. Aptidão reprodutiva e estrutura da comunidade de um candeial com elevada mortalidade. Dissertation (Federal University of Ouro Preto, 2012).44.Pereira, J. A., Londe, V., Ribeiro, S. P. & De Sousa, H. C. Crown architecture and leaf anatomic traits influencing herbivory on Clethra scabra Pers.: Comparing adaptation to wetlands and drained habitats. Rev. Bras. Bot. 40, 481–490 (2017).Article 

    Google Scholar 
    45.Koslov, M. V., Zverev, V. & Zvereva, E. L. Combined effects of environmental disturbance and climate warming on insect herbivory in mountain birch in subarctic forests: Results of 26-year monitoring. Sci. Total Environ. 601–602, 802–811 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    46.Mendes, G. & Cornelissen, T. G. Effects of plant quality and ant defence on herbivory rates in a neotropical ant-plant. Ecol. Entomol. 2017, 1–8 (2017).
    Google Scholar 
    47.Jhee, E. M., Boyd, R. S. & Eubanks, M. D. Effectiveness of metal-metal and metal-organic compund combinations against Plutella xylostella: Implications for plant elemental defense. J. Chem. Ecol. 32, 239–259 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Boyd, R. S. Plant defense using toxic inorganic ions: Conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci. 195, 88–95 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Bronstein, J. L. Conditional outcomes in mutualistic interactions. TREE 9, 214–217 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    50.Monteiro, I., Viana-Junior, A. B., Solar, R. R. C., Neves, F. S. & DeSouza, O. Disturbance-modulated symbioses in termitophily. Ecol. Evol. 7, 10829–10838 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Trumble, J. T., Kolodnyhirsch, D. M. & Ting, I. P. Plant compensation for arthropod herbivory. Annu. Rev. Entomol. 38, 93–119 (1993).Article 

    Google Scholar 
    52.Stowe, K. A., Marquis, R. J., Hochwender, C. G. & Simms, E. L. The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Syst. 31, 565–595 (2000).Article 

    Google Scholar 
    53.Poveda, K., Steffan-Dewenter, I., Scheu, S. & Tscharntke, T. Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601–605 (2003).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Tozer, K. N. et al. Growth responses of diploid and tetraploid perennial ryegrass (Lolium perenne) to soil-moisture deficit, defoliation and a root-feeding invertebrate. Crop Pasture Sci. 68, 632–642 (2017).Article 

    Google Scholar 
    55.Yuan, J., Wang, P. & Yang, Y. Effects of simulated herbivory on the vegetative reproduction and compensatory growth of Hordeum brevisubulatum at different ontogenic stages. Int. J. Environ. Res. Public Health 16, 1663 (2019).PubMed Central 
    Article 

    Google Scholar 
    56.Seneviratne, M. et al. Heavy metal induced oxidative stress on seed germination and seedling development: A critical review. Environ. Geochem. Health. 41, 1813–1831 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Poschenrieder, C., Tolrà, R. & Barceló, J. Can metals defend plants against biotic stress?. Trends Plant Sci. 11, 288–295 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Coleman, J. E. Zinc proteins: Enzymes, storage proteins, transcription factors, and replication proteins. Annu. Rev. Biochem. 61, 897–946 (1992).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Jansen, S., Watanabe, T., Dessein, S., Smetes, E. & Robbrecht, E. A comparative study of metal levels in leaves of some Al-accumulating Rubiaceae. Ann. Bot. 91, 657–663 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Gall, J. E., Boyd, R. S. & Rajakaruna, N. Transfer of heavy metals through terrestrial food webs: A review. Environ. Monit. Asses. 187, 1–21 (2015).CAS 
    Article 

    Google Scholar 
    61.Poschenrieder, C., Gunsé, B., Corrales, I. & Barceló, J. A glance into aluminum toxicity and resistance in plants. Sci. Total. Environ. 400, 356–368 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Janssens, T. K. S., Roelofs, D. & Van Straalen, N. M. Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Sci. 16, 3–18 (2009).CAS 
    Article 

    Google Scholar 
    63.Hodson, M. E. Effects of heavy metals and metalloids on soil organisms. In Heavy metals in soils: trace metals and metalloids in soils and their bioavailability. Environmental Pollution (ed Alloway, B. J.) Vol. 22, 141–160 (Springer, 2012).64.Rahman, M. et al. Importance of mineral nutrition for mitigating aluminum toxicity in plants on acidic soils: Current status and opportunities. Int. J. Mol. Sci. 19, 1–28 (2018).ADS 

    Google Scholar 
    65.Kidd, P. S., Llugany, M., Poschenrieder, C., Gunsé, B. & Barceló, J. The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot. 52, 1339–1352 (2001).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.Epstein, E. Silicon: Its manifold roles in plants. Ann. Appl. Biol. 155, 155–160 (2009).CAS 
    Article 

    Google Scholar 
    67.Grevenstuk, T. & Romano, A. Aluminium speciation and internal detoxification mechanisms in plants: Where do we stand?. Metallomics 5, 1584–1594 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Panda, S. K., Baluška, F. & Matsumoto, H. Aluminum stress signaling in plants. Plant Signal Behav. 4, 592–597 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Borgström, P., Bommarco, R., Viketoft, M. & Strengbom, J. Below-ground herbivory mitigates biomass loss from above-ground herbivory of nitrogen fertilized plants. Sci. Rep. 10, 12752 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    70.Bojórquez-Quintal, E., Escalante-Magaña, C., Echevarría-Machado, I. & Martínez-Estévez, M. Aluminum, a friend or foe of higher plants in acid soils. Front. Plant Sci. 8, 1–18 (2017).Article 

    Google Scholar 
    71.Massad, T. J. Ontogenetic differences of herbivory on woody and herbaceous plants: A meta-analysis demonstrating unique effects of herbivory on the young and the old, the slow and the fast. Oecologia 172, 1–10 (2013).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Messias, M. C. T. B. et al. Phanerogamic flora and vegetation of Itacolomi State Park, Minas Gerais, Brazil. Biota Neotrop. 17, 1–38 (2017).Article 

    Google Scholar 
    73.Peron, M. V. Listagem preliminar da flora fanerogâmica dos campos rupestres do Parque Estadual do Itacolomi–Ouro Preto/Mariana, MG. Rodriguésia 67, 63–69 (1989).Article 

    Google Scholar 
    74.Almeida, F. F. M. Províncias estruturais brasileiras. In SBG, Simpósio de Geologia do Nordeste, 8, Campina Grande, PB. Atas Campina Grande 363–391 (1977).75.Machado, N., Schrank, A., Noce, C. M. & Gauthier, G. Ages of detrital zircon from Archean-Paleoproterozoic sequences: Implications for Greenstone Belt setting and evolution of a Transamazonian foreland basin in Quadrilatero Ferrifero, southeast Brazil. Earth Planet Sci. Lett. 141, 259–276 (1996).ADS 
    CAS 
    Article 

    Google Scholar 
    76.Ribeiro, S. P. & Basset, Y. Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: The importance of leaf sclerophylly. Ecography 30, 663–672 (2007).Article 

    Google Scholar 
    77.Ribeiro, S. P. & Basset, Y. Effects of sclerophylly and host choice on gall densities and herbivory distribution in an Australian subtropical forest. Austral. Ecol. 441, 219–226 (2016).Article 

    Google Scholar 
    78.Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).MATH 

    Google Scholar 
    79.R Core Team. R: A Language and Environment for Statistical Computing (R Found Stat Comp, 2020) https://www.R-project.org/. More

  • in

    Large-bodied birds are over-represented in unstructured citizen science data

    1.Pocock, M. J., Tweddle, J. C., Savage, J., Robinson, L. D. & Roy, H. E. The diversity and evolution of ecological and environmental citizen science. PLoS ONE 12, e0172579 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    2.Chandler, M. et al. Contribution of citizen science towards international biodiversity monitoring. Biol. Cons. 213, 280–294 (2017).Article 

    Google Scholar 
    3.Chandler, M. et al. Involving citizen scientists in biodiversity observation. In The GEO Handbook on Biodiversity Observation Networks 211–237 (Springer, 2017).4.McKinley, D. C. et al. Citizen science can improve conservation science, natural resource management, and environmental protection. Biol. Cons. 208, 15–28 (2017).Article 

    Google Scholar 
    5.Pereira, H. M. et al. Monitoring essential biodiversity variables at the species level. In The GEO Handbook on Biodiversity Observation Networks 79–105 (Springer, 2017).6.Wiggins, A. & Crowston, K. From conservation to crowdsourcing: A typology of citizen science. in 2011 44th Hawaii International Conference on System Sciences 1–10 (IEEE, 2011).7.Haklay, M. Citizen science and volunteered geographic information: Overview and typology of participation. In Crowdsourcing Geographic Knowledge 105–122 (Springer, 2013).8.Kelling, S. et al. Using semistructured surveys to improve citizen science data for monitoring biodiversity. Bioscience 69, 170–179 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Welvaert, M. & Caley, P. Citizen surveillance for environmental monitoring: Combining the efforts of citizen science and crowdsourcing in a quantitative data framework. Springerplus 5, 1890 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Callaghan, C. T., Rowley, J. J., Cornwell, W. K., Poore, A. G. & Major, R. E. Improving big citizen science data: Moving beyond haphazard sampling. PLoS Biol. 17, e3000357 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    12.Kosmala, M., Wiggins, A., Swanson, A. & Simmons, B. Assessing data quality in citizen science. Front. Ecol. Environ. 14, 551–560 (2016).Article 

    Google Scholar 
    13.Burgess, H. K. et al. The science of citizen science: Exploring barriers to use as a primary research tool. Biol. Cons. 208, 113–120 (2017).Article 

    Google Scholar 
    14.Courter, J. R., Johnson, R. J., Stuyck, C. M., Lang, B. A. & Kaiser, E. W. Weekend bias in citizen science data reporting: Implications for phenology studies. Int. J. Biometeorol. 57, 715–720 (2013).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Sullivan, B. L. et al. The eBird enterprise: An integrated approach to development and application of citizen science. Biol. Cons. 169, 31–40 (2014).Article 

    Google Scholar 
    16.Kelling, S. et al. Can observation skills of citizen scientists be estimated using species accumulation curves?. PLoS ONE 10, e0139600 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    17.Tiago, P., Ceia-Hasse, A., Marques, T. A., Capinha, C. & Pereira, H. M. Spatial distribution of citizen science casuistic observations for different taxonomic groups. Sci. Rep. 7, 1–9 (2017).CAS 
    Article 

    Google Scholar 
    18.Geldmann, J. et al. What determines spatial bias in citizen science? Exploring four recording schemes with different proficiency requirements. Divers. Distrib. 22, 1139–1149 (2016).Article 

    Google Scholar 
    19.Callaghan, C. T. et al. Three frontiers for the future of biodiversity research using citizen science data. Bioscience 71, 55–63 (2021).
    Google Scholar 
    20.Ward, D. F. Understanding sampling and taxonomic biases recorded by citizen scientists. J. Insect Conserv. 18, 753–756 (2014).Article 

    Google Scholar 
    21.Troudet, J., Grandcolas, P., Blin, A., Vignes-Lebbe, R. & Legendre, F. Taxonomic bias in biodiversity data and societal preferences. Sci. Rep. 7, 1–14 (2017).CAS 
    Article 

    Google Scholar 
    22.Martı́n-López, B., Montes, C., Ramı́rez, L. & Benayas, J. What drives policy decision-making related to species conservation? Biol. Conserv. 142, 1370–1380 (2009).23.Boakes, E. H. et al. Distorted views of biodiversity: Spatial and temporal bias in species occurrence data. PLoS Biol 8, e1000385 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    24.Aceves-Bueno, E. et al. The accuracy of citizen science data: A quantitative review. Bull. Ecol. Soc. Am. 98, 278–290 (2017).Article 

    Google Scholar 
    25.Davies, T. K., Stevens, G., Meekan, M. G., Struve, J. & Rowcliffe, J. M. Can citizen science monitor whale-shark aggregations? Investigating bias in mark–recapture modelling using identification photographs sourced from the public. Wildl. Res. 39, 696–704 (2013).Article 

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

    Google Scholar 
    27.van Strien, A. J., van Swaay, C. A. & Termaat, T. Opportunistic citizen science data of animal species produce reliable estimates of distribution trends if analysed with occupancy models. J. Appl. Ecol. 50, 1450–1458 (2013).Article 

    Google Scholar 
    28.Johnston, A., Moran, N., Musgrove, A., Fink, D. & Baillie, S. R. Estimating species distributions from spatially biased citizen science data. Ecol. Model. 422, 108927 (2020).Article 

    Google Scholar 
    29.Tiago, P., Pereira, H. M. & Capinha, C. Using citizen science data to estimate climatic niches and species distributions. Basic Appl. Ecol. 20, 75–85 (2017).Article 

    Google Scholar 
    30.Sullivan, B. L. et al. Using open access observational data for conservation action: A case study for birds. Biol. Cons. 208, 5–14 (2017).Article 

    Google Scholar 
    31.Callaghan, C. T. et al. Citizen science data accurately predicts expert-derived species richness at a continental scale when sampling thresholds are met. Biodivers. Conserv. 29, 1323–1337 (2020).Article 

    Google Scholar 
    32.Birkin, L. & Goulson, D. Using citizen science to monitor pollination services. Ecol. Entomol. 40, 3–11 (2015).Article 

    Google Scholar 
    33.Delaney, D. G., Sperling, C. D., Adams, C. S. & Leung, B. Marine invasive species: Validation of citizen science and implications for national monitoring networks. Biol. Invasions 10, 117–128 (2008).Article 

    Google Scholar 
    34.Schultz, C. B., Brown, L. M., Pelton, E. & Crone, E. E. Citizen science monitoring demonstrates dramatic declines of monarch butterflies in western north america. Biol. Cons. 214, 343–346 (2017).Article 

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

    Google Scholar 
    36.Isaac, N. J., van Strien, A. J., August, T. A., de Zeeuw, M. P. & Roy, D. B. Statistics for citizen science: Extracting signals of change from noisy ecological data. Methods Ecol. Evol. 5, 1052–1060 (2014).Article 

    Google Scholar 
    37.Dickinson, J. L. et al. The current state of citizen science as a tool for ecological research and public engagement. Front. Ecol. Environ. 10, 291–297 (2012).Article 

    Google Scholar 
    38.Bonney, R. et al. Next steps for citizen science. Science 343, 1436–1437 (2014).ADS 
    PubMed 
    Article 

    Google Scholar 
    39.Jordan, R. C., Gray, S. A., Howe, D. V., Brooks, W. R. & Ehrenfeld, J. G. Knowledge gain and behavioral change in citizen-science programs. Conserv. Biol. 25, 1148–1154 (2011).PubMed 
    Article 

    Google Scholar 
    40.Crall, A. W. et al. The impacts of an invasive species citizen science training program on participant attitudes, behavior, and science literacy. Public Underst. Sci. 22, 745–764 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Jordan, R. C., Ballard, H. L. & Phillips, T. B. Key issues and new approaches for evaluating citizen-science learning outcomes. Front. Ecol. Environ. 10, 307–309 (2012).Article 

    Google Scholar 
    42.Evans, C. et al. The neighborhood nestwatch program: Participant outcomes of a citizen-science ecological research project. Conserv. Biol. 19, 589–594 (2005).Article 

    Google Scholar 
    43.Haywood, B. K., Parrish, J. K. & Dolliver, J. Place-based and data-rich citizen science as a precursor for conservation action. Conserv. Biol. 30, 476–486 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Pocock, M. J. et al. A vision for global biodiversity monitoring with citizen science. In Advances in Ecological Research vol. 59, 169–223 (Elsevier, 2018).45.Tiago, P., Gouveia, M. J., Capinha, C., Santos-Reis, M. & Pereira, H. M. The influence of motivational factors on the frequency of participation in citizen science activities. Nat. Conserv. 18, 61 (2017).Article 

    Google Scholar 
    46.Isaac, N. J. & Pocock, M. J. Bias and information in biological records. Biol. J. Lin. Soc. 115, 522–531 (2015).Article 

    Google Scholar 
    47.Angulo, E. & Courchamp, F. Rare species are valued big time. PLoS ONE 4, e5215 (2009).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Booth, J. E., Gaston, K. J., Evans, K. L. & Armsworth, P. R. The value of species rarity in biodiversity recreation: A birdwatching example. Biol. Cons. 144, 2728–2732 (2011).Article 

    Google Scholar 
    49.Rowley, J. J. et al. FrogID: Citizen scientists provide validated biodiversity data on frogs of australia. Herpetol. Conserv. Biol. 14, 155–170 (2019).
    Google Scholar 
    50.Boakes, E. H. et al. Patterns of contribution to citizen science biodiversity projects increase understanding of volunteers recording behaviour. Sci. Rep. 6, 33051 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Garrard, G. E., McCarthy, M. A., Williams, N. S., Bekessy, S. A. & Wintle, B. A. A general model of detectability using species traits. Methods Ecol. Evol. 4, 45–52 (2013).Article 

    Google Scholar 
    52.Denis, T. et al. Biological traits, rather than environment, shape detection curves of large vertebrates in neotropical rainforests. Ecol. Appl. 27, 1564–1577 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Sólymos, P., Matsuoka, S. M., Stralberg, D., Barker, N. K. & Bayne, E. M. Phylogeny and species traits predict bird detectability. Ecography 41, 1595–1603 (2018).Article 

    Google Scholar 
    54.Wood, C., Sullivan, B., Iliff, M., Fink, D. & Kelling, S. eBird: Engaging birders in science and conservation. PLoS Biol 9, 1001220 (2011).Article 
    CAS 

    Google Scholar 
    55.GBIF.org (3rd December 2019). GBIF occurrence download. https://doi.org/10.15468/dl.lpwczr56.Gilfedder, M. et al. Brokering trust in citizen science. Soc. Nat. Resour. 32, 292–302 (2019).Article 

    Google Scholar 
    57.Callaghan, C., Lyons, M., Martin, J., Major, R. & Kingsford, R. Assessing the reliability of avian biodiversity measures of urban greenspaces using eBird citizen science data. Avian Conserv. Ecol. 12, 66 (2017).
    Google Scholar 
    58.Johnston, A. et al. Best practices for making reliable inferences from citizen science data: Case study using eBird to estimate species distributions. BioRxiv 574392 (2019).59.Myhrvold, N. P. et al. An amniote life-history database to perform comparative analyses with birds, mammals, and reptiles: Ecological archives E096–269. Ecology 96, 3109–3109 (2015).Article 

    Google Scholar 
    60.Dale, J., Dey, C. J., Delhey, K., Kempenaers, B. & Valcu, M. The effects of life history and sexual selection on male and female plumage colouration. Nature 527, 367–370 (2015).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).62.Wickham, H. et al. Welcome to the tidyverse. J. Open Source Softw. 4, 1686 (2019).ADS 
    Article 

    Google Scholar 
    63.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Google Scholar 
    64.Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar 
    65.Johnston, A. et al. Species traits explain variation in detectability of UK birds. Bird Study 61, 340–350 (2014).Article 

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

    Google Scholar 
    67.Henckel, L., Bradter, U., Jönsson, M., Isaac, N. J. & Snäll, T. Assessing the usefulness of citizen science data for habitat suitability modelling: Opportunistic reporting versus sampling based on a systematic protocol. Divers. Distrib. 26, 1276–1290 (2020).Article 

    Google Scholar 
    68.Caley, P., Welvaert, M. & Barry, S. C. Crowd surveillance: Estimating citizen science reporting probabilities for insects of biosecurity concern. J. Pest. Sci. 93, 543–550 (2020).Article 

    Google Scholar 
    69.Périquet, S., Roxburgh, L., le Roux, A. & Collinson, W. J. Testing the value of citizen science for roadkill studies: A case study from South Africa. Front. Ecol. Evol. 6, 15 (2018).Article 

    Google Scholar 
    70.Nakagawa, S. & Freckleton, R. P. Model averaging, missing data and multiple imputation: A case study for behavioural ecology. Behav. Ecol. Sociobiol. 65, 103–116 (2011).Article 

    Google Scholar 
    71.Schlossberg, S., Chase, M. & Griffin, C. Using species traits to predict detectability of animals on aerial surveys. Ecol. Appl. 28, 106–118 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Aristeidou, M., Scanlon, E. & Sharples, M. Profiles of engagement in online communities of citizen science participation. Comput. Hum. Behav. 74, 246–256 (2017).Article 

    Google Scholar 
    73.Troscianko, J., Skelhorn, J. & Stevens, M. Quantifying camouflage: How to predict detectability from appearance. BMC Evol. Biol. 17, 1–13 (2017).Article 

    Google Scholar 
    74.Schuetz, J. G. & Johnston, A. Characterizing the cultural niches of North American birds. Proc. Natl. Acad. Sci. 22, 10868–10873 (2019).Article 
    CAS 

    Google Scholar 
    75.Lišková, S. & Frynta, D. What determines bird beauty in human eyes?. Anthrozoös 26, 27–41 (2013).Article 

    Google Scholar 
    76.Tulloch, A. I., Possingham, H. P., Joseph, L. N., Szabo, J. & Martin, T. G. Realising the full potential of citizen science monitoring programs. Biol. Cons. 165, 128–138 (2013).Article 

    Google Scholar 
    77.Kobori, H. et al. Citizen science: A new approach to advance ecology, education, and conservation. Ecol. Res. 31, 1–19 (2016).CAS 
    Article 

    Google Scholar 
    78.Callaghan, C. T., Poore, A. G., Major, R. E., Rowley, J. J. & Cornwell, W. K. Optimizing future biodiversity sampling by citizen scientists. Proc. R. Soc. B 286, 20191487 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Pacifici, K. et al. Integrating multiple data sources in species distribution modeling: A framework for data fusion. Ecology 98, 840–850 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    80.Robinson, O. J. et al. Integrating citizen science data with expert surveys increases accuracy and spatial extent of species distribution models. Divers. Distrib. 26, 976–986 (2020).Article 

    Google Scholar 
    81.van Strien, A. J., Termaat, T., Groenendijk, D., Mensing, V. & Kery, M. Site-occupancy models may offer new opportunities for dragonfly monitoring based on daily species lists. Basic Appl. Ecol. 11, 495–503 (2010).Article 

    Google Scholar 
    82.Van der Wal, R. et al. Mapping species distributions: A comparison of skilled naturalist and lay citizen science recording. Ambio 44, 584–600 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Dennis, E. B., Morgan, B. J., Brereton, T. M., Roy, D. B. & Fox, R. Using citizen science butterfly counts to predict species population trends. Conserv. Biol. 31, 1350–1361 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Stoudt, S., Goldstein, B. R. & De Valpine, P. Identifying charismatic bird species and traits with community science data. bioRxiv. https://doi.org/10.1101/2021.06.05.446577 More

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    Coral conservation strikes a balance

    NATURE INDEX
    24 September 2021

    Coral conservation strikes a balance

    Australia–Fiji collaboration matches community needs with reef protection.

    Clare Watson

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    Clare Watson

    Clare Watson is a freelance writer in Wollongong, Australia.

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    A spear fisherman catches reef fish, a cultural mainstay on Mali Island in Fiji.Credit: Juergen Freund/naturepl.com

    Coral reefs are under threat, and so too are the livelihoods of more 500 million people who depend on them. Global climate change is causing longer and more frequent marine heatwaves, leading to widespread and repeated coral bleaching. Overfishing and pollution exacerbate the problem, adding pressure to these marine biodiversity hotspots that sustain coastal communities.Reef-management programmes that limit or prohibit fishing and other commercial activities are bound to be ineffective if local communities are not involved in their design and management, says Sangeeta Mangubhai, a coral-reef ecologist in Fiji. “If people haven’t been engaged in the management [of conservation strategies], they’re not as likely to understand what the rules are, or they might not comply with it,” she says. Initiatives that are designed to protect coral reefs without incorporating insights from local communities may also affect them in unintended ways, she adds.
    Nature Index 2021 Science cities
    In collaboration with environmental social scientist, Georgina Gurney, Mangubhai is identifying the conditions that support both conservation outcomes and the wellbeing of coastal communities who often have cultural practices and spiritual ties to the sea. Their work explores the social factors that influence coral-reef-management programmes, such as the perceived fairness of payment schemes that direct tourism revenue back to the communities who manage local reefs (G. G. Gurney et al. Environ. Sci. Policy 124, 23–32; 2021).“First and foremost, it’s an ethical and moral issue,” says Gurney. “Conservation should not impinge on the wellbeing of people; it should promote the wellbeing of people.”Based at James Cook University (JCU) in Townsville, a city on the northeastern coast of Queensland, Australia, Gurney has close access to the Great Barrier Reef, which contains the world’s largest coral reef ecosystem. The university has long-standing ties with researchers in nearby Pacific island nations, such as Papua New Guinea, Fiji and New Caledonia.Townsville was the second most-prolific city in the 82 high-quality natural-sciences journals tracked by the Nature Index for research related to the United Nations’ Sustainable Development Goal (SDG) Life below water (SDG14) in 2015–20, with a Share of 15.59, 52% of which is attributed to JCU. Beijing, placed first by output related to SDG14, had a Share of 17.88 for the same period. (For more information on the analyses used in this article, see ‘A guide to Nature Index’.)

    Georgina Gurney and Sangeeta Mangubhai at a fish market in Suva, Fiji.Credit: Isabelle Gurney

    According to Gurney, successful conservation programmes should evaluate social factors alongside ecological outcomes, such as fish stocks and coral health, although this is rarely the case. With Mangubhai and other collaborators, Gurney has developed a framework that combines 90 social and ecological indicators, from coral cover and fish biomass to household incomes derived from the reef, equitable benefit-sharing and conflicts occurring over marine resources (G. G. Gurney et al. Biol. Conserv. 240, 108298; 2019).In principle, the framework standardizes how outcomes of coral-reef programmes are evaluated to improve data collection and enable cross-country comparisons. It has been adopted by the New York-based non-governmental organization, the Wildlife Conservation Society (WCF), and its partners in 7 countries and more than 130 communities across Africa, Asia and the Pacific.Besides improving conservation efforts, Mangubhai, who leads the WCF’s Fiji programme, says the partnership gives equal footing to local conservation scientists and policymakers, empowering them to direct independent research. “If you have these meaningful collaborations, the outcome is going to have so much more of an impact on the ground,” she says.Incorporating an understanding of the social factors that influence coral-reef conservation into marine-management strategies translates to respect for local traditional cultural practices of Indigenous Fijians, says Mangubhai. Temporary closures called tabu, which are used to maintain the productivity of their customary fishing grounds, are a good example. “It’s a real merging of traditional knowledge and other best practices, such as size limits on fish catch, to help communities achieve the outcomes they want for themselves,” she says.

    doi: https://doi.org/10.1038/d41586-021-02409-6This article is part of Nature Index 2021 Science cities, an editorially independent supplement produced with the financial support of third parties. About this content.

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    Rising tide of floating plastics spurs surge in research

    NATURE INDEX
    24 September 2021

    Rising tide of floating plastics spurs surge in research

    Strong government policies and research insights are essential to deliver on a pledge to clean up the sea.

    Michael Eisenstein

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    Michael Eisenstein

    Michael Eisenstein is a freelance writer in Philadelphia, Pennsylvania.

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    A jellyfish swims beneath a slick of floating plastic debris in the Indian Ocean near Sri Lanka.Credit: Alex Mustard/naturepl.com

    Many stories have been written about the ‘Great Pacific garbage patch’, a name evoking a vast Sargasso Sea of plastic bottles and bags. But the reality is that much of this debris has been broken down into a murky suspension of ‘microplastics’ spanning an area three times the size of France.
    Nature Index 2021 Science cities
    These plastic flecks introduce long-lasting chemical pollution into marine and coastal ecosystems, says Daoji Li, an oceanographer at East China Normal University in Shanghai. In 2020, Li and his colleagues found that microplastic debris is highly concentrated in even the deepest underwater trenches (G. Peng et al. Water Res. 168, 115121; 2020). Staving off this influx of pollutants is a target of the United Nations’ Sustainable Development Goal (SDG) Life below water (SDG14), with its aim to “prevent and significantly reduce marine pollution of all kinds” by 2025.Between 4.8 million and 12.7 million tonnes of plastic waste entered the oceans in 2010, according to a study in Science, and those numbers are expected to increase dramatically by 2050 without improvements to waste-management infrastructure (J. Jambeck et al. Science 347, 768–771; 2015). Scientists in China, which is a major producer and importer of plastic waste, are taking the lead in amelioration. According to the 2021 UNESCO Science Report, floating plastic debris was the fastest-growing area of SDG-related research in 2012–19 (see ‘A buoyant field’). Publications from the Chinese mainland on the topic jumped from 7 in the period 2012–15 to 286 in 2016–19, placing it third by volume after the United States and United Kingdom. Much of this work has come from investigators in Beijing, the top-ranked city in the Nature Index for SDG14-related research. (For more information on the analyses used in this article, see ‘A guide to Nature Index’.)

    Source: UNESCO

    Li is sceptical that much can be done to eliminate existing plastic pollution. “But what we can do is stop them entering to the ocean,” he says. His team has developed a monitoring framework that outlines ‘gold-standard’ technologies and assays for detecting and quantifying microplastic contamination.Government action is essential to stem the flow of plastic debris. UNESCO reports that 127 countries have adopted legislation to regulate plastic bags. In 2020, China launched an ambitious effort to ban plastic bags nationwide by 2022 and cut single-use plastic in restaurants by one-third by 2025 — although the COVID-19 pandemic created a surge in demand for delivery that derailed this effort.Despite the many hurdles to overcome, Li feels positive about the future. “I am pretty confident that we could meet the target set for SDG14,” he says, “but when we realize those challenges, we should keep going.”

    Source: UNESCO

    doi: https://doi.org/10.1038/d41586-021-02408-7This article is part of Nature Index 2021 Science cities, an editorially independent supplement produced with the financial support of third parties. About this content.

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    Vancouver, Canada

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    The University of British Columbia (UBC)
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    60048: Physicist, Statistician, theoretical Computer Scientist or similar (f/m/x) – Development of causal inference methods in the field causal Inference and machine learning as part of the EU project XAIDA

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