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    Genomic landscape of a relict fir-associated fungus reveals rapid convergent adaptation towards endophytism

    1.Tigano A, Colella JP, MacManes MD. Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent. Mol Ecol. 2020;29:1300–14.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    2.Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, et al. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol Ecol. 2014;23:753–73.PubMed 

    Google Scholar 
    3.Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88–92.CAS 
    PubMed 

    Google Scholar 
    4.Weiß M, Waller F, Zuccaro A, Selosse MA. Sebacinales-one thousand and one interactions with land plants. New Phytol. 2016;211:20–40.PubMed 

    Google Scholar 
    5.Knapp DG, Németh JB, Barry K, Hainaut M, Henrissat B, Johnson J, et al. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Sci Rep. 2018;8:6321.PubMed 
    PubMed Central 

    Google Scholar 
    6.Martino E, Morin E, Grelet GA, Kuo A, Kohler A, Daghino S, et al. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol. 2018;217:1213–29.CAS 
    PubMed 

    Google Scholar 
    7.Arnold AE. Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev. 2007;21:51–66.
    Google Scholar 
    8.Carroll G. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology. 1988;69:2–9.
    Google Scholar 
    9.Miller JD, Sumarah MW, Adams GW. Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. J Chem Ecol. 2008;34:362–8.CAS 
    PubMed 

    Google Scholar 
    10.White JF Jr, Torres MS. Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant. 2010;138:440–6.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.May G, Nelson P. Defensive mutualisms: do microbial interactions within hosts drive the evolution of defensive traits? Funct Ecol. 2014;28:356–63.
    Google Scholar 
    12.Carroll G. The foraging ascomycete, in: Abstracts of the 16th International Botanical Congress. St Louis, Missouri, USA, 1999.13.Müller MM, Valjakka R, Suokko A, Hantula J. Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol. 2001;10:1801–10.PubMed 

    Google Scholar 
    14.Thomas DC, Vandegrift R, Ludden A, Carroll GC, Roy BA. Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica. 2016;48:381–93.
    Google Scholar 
    15.Naranjo-Ortiz MA, Gabaldón T. Fungal evolution: major ecological adaptations and evolutionary transitions. Biol Rev Camb Philos Soc. 2019;94:1443–76.PubMed 
    PubMed Central 

    Google Scholar 
    16.Oono R, Lutzoni F, Arnold AE, Kaye L, U’Ren JM, May G, et al. Genetic variation in horizontally transmitted fungal endophytes of pine needles reveals population structure in cryptic species. Am J Bot. 2014;101:1362–74.PubMed 

    Google Scholar 
    17.Shao S, Jin Z. In Species Diversity and Extinction (ed. Tepper, GH) Ch. 15. Nova Science Publishers. 2010.18.Yuan ZL, Rao LB, Chen YC, Zhang CL, Wu YG. From pattern to process: species and functional diversity in fungal endophytes of Abies beshanzuensis. Fungal Biol. 2011;115:197–213.PubMed 

    Google Scholar 
    19.Yuan ZL, Verkley GJM. Pezicula neosporulosa sp. nov. (Helotiales, Ascomycota), an endophytic fungus associated with Abies spp. in China and Europe. Mycoscience. 2014;56:205–13.
    Google Scholar 
    20.Sieber T. Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev. 2007;21:75–89.
    Google Scholar 
    21.Levis NA, Martin RA, O’Donnell KA, Pfennig DW. Intraspecific adaptive radiation: competition, ecological opportunity, and phenotypic diversification within species. Evolution. 2017;71:2496–509.PubMed 

    Google Scholar 
    22.Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42:D699–D704.CAS 
    PubMed 

    Google Scholar 
    23.Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–D495.CAS 
    PubMed 

    Google Scholar 
    24.Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–W101.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Blin K, Wolf T, Chevrette MG, Lu XW, Schwalen CJ, Kautsar SA, et al. antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res. 2017;45:W36–W41.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157.PubMed 
    PubMed Central 

    Google Scholar 
    27.Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CAS 
    PubMed 

    Google Scholar 
    29.Enright AJ, Dongen SV, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30:1575–84.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Han MV, Thomas GW, Lugo-Martinez J, Hahn MW. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol. 2013;30:1987–97.CAS 
    PubMed 

    Google Scholar 
    31.Walkowiak S, Rowland O, Rodrigue N, Subramaniam R. Whole genome sequencing and comparative genomics of closely related Fusarium Head Blight fungi: Fusarium graminearum, F. meridionale and F. asiaticum. BMC Genomics. 2016;17:1014.PubMed 
    PubMed Central 

    Google Scholar 
    32.Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26:589–95.PubMed 
    PubMed Central 

    Google Scholar 
    33.Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–9.PubMed 
    PubMed Central 

    Google Scholar 
    34.Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A, et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;43:11.10.1–11.10.33.
    Google Scholar 
    35.Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993;133:693–709.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    37.Hutter S, Vilella AJ, Rozas J. Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinform. 2006;7:409.
    Google Scholar 
    38.Richards JK, Stukenbrock EH, Carpenter J, Liu Z, Cowger C, Faris JD, et al. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PLoS Genet. 2019;15:e1008223.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–67.CAS 
    PubMed 

    Google Scholar 
    40.Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.PubMed 

    Google Scholar 
    41.Looney B, Miyauchi S, Morin E, Drula E, Courty PE, Kohler A, et al. Evolutionary priming and transition to the ectomycorrhizal habit in an iconic lineage of mushroom-forming fungi: is preadaptation a requirement? bioRxiv. 2021. https://doi.org/10.1101/2021.02.23.432530.42.Wey T, Schlegel M, Stroheker S, Gross A. MAT-gene structure and mating behavior of Hymenoscyphus fraxineus and Hymenoscyphus albidus. Fungal Genet Biol. 2016;87:54–63.CAS 
    PubMed 

    Google Scholar 
    43.Zijlstra JD, Van’t Hof P, Baar J, Verkley GJM, Summerbell RC, Paradi I, et al. Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass, Deschampsia flexuosa. Stud Mycol. 2005;53:147–62.
    Google Scholar 
    44.Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Zuccaro A, et al. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proc Natl Acad Sci USA. 2017;114:E9403–E9412.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Gazis R, Kuo A, Riley R, LaButti K, Lipzen A, Lin J, et al. The genome of Xylona heveae provides a window into fungal endophytism. Fungal Biol. 2016;120:26–42.CAS 
    PubMed 

    Google Scholar 
    46.Perotto S, Daghino S, Martino E. Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis? New Phytol. 2018;220:1141–7.PubMed 

    Google Scholar 
    47.Wrzosek M, Ruszkiewicz-Michalska M, Sikora K, Damszel M, Sierota Z. The plasticity of fungal interactions. Mycol Prog. 2017;16:101–8.
    Google Scholar 
    48.Parrent JL, James TY, Vasaitis R, Taylor AF. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol. 2009;9:148.PubMed 
    PubMed Central 

    Google Scholar 
    49.Zhang F, Anasontzis GE, Labourel A, Champion C, Haon M, Kemppainen M, et al. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development. New Phytol. 2018;220:1309–21.CAS 
    PubMed 

    Google Scholar 
    50.Mesny F, Miyauchi S, Thiergart T, Pickel B, Atanasova L, Karlsson M, et al. Genetic determinants of endophytism in the Arabidopsis root mycobiome. Nat Commun. 2021;12:7227.CAS 
    PubMed 

    Google Scholar 
    51.Schulz B, Sucker J, Aust HJ. Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res. 1995;99:1007–15.CAS 

    Google Scholar 
    52.Tanney JB, McMullin DR, Miller JD. Toxigenic Foliar Endophytes from the Acadian Forest. In: Pirttilä A, Frank A (eds) Endophytes of Forest Trees. Forestry Sciences, vol 86. Springer, Cham. 2018;343–81.53.Yue Q, Li Y, Chen L, Zhang X, Liu X, An Z, et al. Genomics-driven discovery of a novel self-resistance mechanism in the echinocandin-producing fungus Pezicula radicicola. Environ Microbiol. 2018;20:3154–67.CAS 
    PubMed 

    Google Scholar 
    54.Rogers RL, Grizzard SL, Titus-McQuillan JE, Bockrath K, Patel S, Wares JP, et al. Gene family amplification facilitates adaptation in freshwater unionid bivalve Megalonaias nervosa. Mol Ecol. 2021;30:1155–73.CAS 
    PubMed 

    Google Scholar 
    55.Mäkinen M, Kuuskeri J, Laine P, Smolander OP, Kovalchuk A, Zeng Z, et al. Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi. BMC Genomics. 2019;20:430.PubMed 
    PubMed Central 

    Google Scholar 
    56.Yang Y, Liu X, Cai J, Chen Y, Li B, Guo Z, et al. Genomic characteristics and comparative genomics analysis of the endophytic fungus Sarocladium brachiariae. BMC Genomics. 2019;20:782.PubMed 
    PubMed Central 

    Google Scholar 
    57.Franco MEE, Wisecaver JH, Arnold AE, Ju YM, Slot JC, Ahrendt S, et al. Secondary metabolism drives ecological breadth in the Xylariaceae. bioRxiv. 2021. https://doi.org/10.1101/2021.06.01.446356.58.Matsuda Y, Yamakawa M, Inaba T, Obase K, Ito S. Intraspecific variation in mycelial growth of Cenococcum geophilum isolates in response to salinity gradients. Mycoscience. 2017;58:369–77.
    Google Scholar 
    59.Taylor JW, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, et al. Sources of fungal genetic variation and associating it with phenotypic diversity. Microbiol Spectr. 2017;5:1–21.CAS 

    Google Scholar 
    60.Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, et al. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol. 2018;220:1161–71.CAS 
    PubMed 

    Google Scholar 
    61.McCutcheon TL, Carroll GC, Schwab S. Genotypic diversity in populations of a fungal endophyte from Douglas Fir. Mycologia. 1993;85:180–6.
    Google Scholar 
    62.Perotto S, Girlanda M, Martino E. Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil. 2002;244:41–53.CAS 

    Google Scholar 
    63.Müller MM, Valjakka R, Hantula J. Genetic diversity of Lophodermium piceae in South Finland. For Pathol. 2007;37:329–37.
    Google Scholar 
    64.Morgenstern K, Polster J-U, Krabel D. Genetic variation between and within two populations of Rhabdocline pseudotsugae in Germany. Can J Res. 2016;46:716–24.CAS 

    Google Scholar 
    65.Atwell S, Corwin JA, Soltis NE, Subedy A, Denby KJ, Kliebenstein DJ. Whole genome resequencing of Botrytis cinerea isolates identifies high levels of standing diversity. Front Microbiol. 2015;6:996.PubMed 
    PubMed Central 

    Google Scholar 
    66.Gasca-Pineda J, Velez P, Hosoya T. Phylogeography of post-Pleistocene population expansion in Dasyscyphella longistipitata (Leotiomycetes, Helotiales), an endemic fungal symbiont of Fagus crenata in Japan. MycoKeys. 2020;65:1–24.PubMed 
    PubMed Central 

    Google Scholar 
    67.Groenewald M, Linde CC, Groenewald JZ, Crous PW. Indirect evidence for sexual reproduction in Cercospora beticola populations from sugar beet. Plant Pathol. 2008;57:25–32.CAS 

    Google Scholar 
    68.Nordborg M, Charlesworth B, Charlesworth D. Increased levels of polymorphism surrounding selectively maintained sites in highly selfing species. Proc R Soc B. 1996;263:1033–9.
    Google Scholar 
    69.Koenig D, Hagmann J, Li R, Bemm F, Slotte T, Neuffer B, et al. Long-term balancing selection drives evolution of immunity genes in Capsella. Elife. 2019;8:e43606.PubMed 
    PubMed Central 

    Google Scholar 
    70.Carbone I, Jakobek JL, Ramirez-Prado JH, Horn BW. Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus. Mol Ecol. 2007;16:4401–17.CAS 
    PubMed 

    Google Scholar 
    71.Drott MT, Debenport T, Higgins SA, Buckley DH, Milgroom MG. Fitness cost of aflatoxin production in Aspergillus flavus when competing with soil microbes could maintain balancing selection. mBio. 2019;10:e02782–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Chen F, Goodwin PH, Khan A, Hsiang T. Population structure and mating-type genes of Colletotrichum graminicola from Agrostis palustris. Can J Microbiol. 2002;48:427–36.CAS 
    PubMed 

    Google Scholar  More

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    Direct pesticide exposure of insects in nature conservation areas in Germany

    Pesticide residuesInsects were collected in Malaise traps during two-week intervals, where pesticide residues from insect bodies were dissolved in the ethanol that was used to preserve the collected samples. Additionally, particles of plants, pollen, nectar or honeydew adhering to the insect bodies can be carriers of chemical pollution. Detected pesticide residues can therefore come from the insects and potentially attached particles. Under natural conditions of sunlight and warm temperatures, chemical stability of pesticide residues in the ethanol solution may have been affected by hydrolysis, for example, which could have caused the degradation of residues during the two-week collection intervals. Only flying insects that are alive can get into the Malaise traps, and therefore pesticide residues in the collected samples are assumed to represent sublethal levels to all trapped species. Additionally, insect collection was performed over an entire season and did not consider explicit spraying events. Therefore, the sampling we performed did not necessarily record maximum exposure levels that could represent lethal levels for individual species and substances. Hence, the quantification of pesticide amounts cannot be used for risk calculations. Instead we evaluate the presence of residues of CUPs on insects. Since detection is possible at low concentrations (see SOM Table A2) we obtained information on trace concentrations of the pesticide residues that insects were exposed to. It is safe to assume that the pesticide loads of insects were especially high following spraying events, and for individuals that were affected and consequently unable to fly. These insects were then not sampled in the Malaise traps.Of the 92 target common CUPs, 47 were detected in the insect samples from 21 nature conservation areas from two sampling dates in May and August 2020: 13 herbicides, 28 fungicides and 6 insecticides. Additionally, metabolites of fipronil, an insecticide registered for biocidal use in the EU, were recorded at three locations. At the 21 sites, insects in the conservation areas were exposed to 16.7 pesticides on average, ranging from 7 to 27 substances. More fungicides than herbicides were recorded and, on average, insects were exposed to less than two insecticides (Table 1). This may in part reflect the application in arable crops where more fungicides than herbicides are applied and insecticides are used less frequently. On the other hand, as insecticides affect insects directly due to their high acute toxicity, exposure to insecticides results in mortality or sublethal effects that impair mobility, leading to an underestimation of insecticide residues in our samples.Table 1 Number of CUP residues detected at 21 nature conservation areas across Germany and the resulting minimal, maximal and mean number of pesticide substances.Full size tableInsects at all 21 sites were exposed to residues of the herbicides metolachlor-S, prosulfocarb and terbuthylazine, and the fungicides azoxystrobin and fluopyram (Table 2). The presence of the six frequently detected herbicides can be explained by the high volume sold in 2019 (see SOM Table A3). They are among the 25 highest-ranking pesticides in terms of selling volume in Germany34. The same is true for the fungicide azoxystrobin. All other seven regularly detected fungicides were sold at lower volumes and their presence in the insect samples could be related to the high persistence of these fungicides, with soil half-lives reaching 500 d (bixafen), 484 d (boscalid) and 309 d (fluopyram). Only kresoxim-methyl, present in 10 sites, is not highly persistent in soil but has an affinity for the waxy plant cuticle, where it binds and accumulates35,36.Table 2 CUP residues frequently recorded at the 21 sites. Only substances that were recorded in ≥ 10 sites are listed.Full size tableThe neonicotinoid insecticide thiacloprid was recorded on insects in 16 of the 21 nature conservation areas. Thiacloprid was banned in the EU for use in field applications from August 2020 onwards, however, the end of use (grace period) was set to 3rd February, 202137. The high incidence of thiacloprid in our samples at many sites across Germany may therefore also reflect the last opportunity for farmers to use their remaining stocks. A ban could thus result in a greater impact to the ecosystem if parallel applications take place on a large scale. Hence, for potent pesticides which are banned from the market, it seems advisable to stop granting grace periods and instead destroy remaining stock rather than dispersing them into the environment despite knowledge of their high environmental risks.On average, in spring (May) residues of 9.6 and in summer (August) 9.3 CUPs were recorded in individual ethanol samples of the three trapping locations in the conservation areas. The minimum number of pesticide residues of 3 (May, site Mülhauser Halde) and 2 (August, Mittelberg) and the maximum of 16 (May, Bottendorfer Hügel) and 18 (August, Wisseler Dünen) were all from samples closer to the centre of the nature protection area, furthest away from adjacent agricultural fields.Seasonality of CUP exposureThe total number of CUP residues recorded on insects was similar for the two sampling intervals with 32 substances in May and 35 in August. However, a higher number of herbicide residues was recorded in May (13) compared to August (9), whereas for fungicides the reverse was the case [August (23), May (14)]. The number of detected insecticide residues was similar, with three and five substances recorded in May and August, respectively. This resulted in a different set of pesticide residue mixtures, driven by seasonality (Fig. 1). Mixtures in May, dominated by herbicides, were more similar to each other than the August mixtures, which contained more fungicides. The extreme positions of the NMDS analysis in August with Brauselay and Mittelberg are driven by the number of fungicide residues recorded. Brauselay is the only site where vineyards bordered the study area. Wine growing in Germany requires frequent fungicide applications.Figure 1CUP mixtures in May (green) and August (red) analysed with NMDS. The position of each location was determined by the composition of pesticide residues found in the ethanol samples. The closer data points are located in the ordination space, the more similar are their composition of pesticides. For abbreviations see Table 1.Full size imageOn the substance level, residues of the herbicides prosulfocarb, metolachlor-S, dimethenamid-P were recorded in more than half of the sites at both sampling intervals, whereas terbuthylazine was frequently present in May but not in August, and flufenacet was detected more frequently later in the year. Fungicide residues of fluopyram, azoxystrobin and boscalid were common in both sampling intervals, but pyraclostrobin, bixafen and dimoxystrobin were characteristic for May samples and fluazinam and kresoxim-methyl for the August samples (SOM Table A4). Although more residues of fungicides were recorded in August, this did not result in an increase in the number of fungicides that are found at many sites. Thirteen out of the 23 fungicides that were recorded in August were detected comparatively sporadic in samples from one to three sites. For insecticides, only thiacloprid was frequently noted, and the remaining substances acetamiprid, dimethoate, tebufenozide, and indoxacarb were found in May, whereas chlorantraniliprole and indoxacarb were recorded in August. The observed patterns reflect the agricultural practice of using herbicides in spring and early summer to establish crops such as cereals, oilseed rape and maize, and fungicides later in the year to control fungal diseases that increase with warmer temperatures.In addition to pesticide applications, seasonality has a direct effect on insect communities that change in composition from spring to autumn38,39,40. Because of shifts in insect community composition and pesticide application schemes, the mixture of pesticide residues present in insect samples changes throughout the year. Thus, it is likely that a finer time resolution than the selected two sampling intervals could reveal additional pesticide residues for the exposure of insects in conservation areas in the agricultural landscape.Influence of surrounding agricultural production areaOur data demonstrate that insects collected with Malaise traps in the nature conservation areas are exposed to pesticides applied in the surrounding agricultural landscape, where various crops are grown and are treated with a variety of pesticides. As the flight range of aerial insects fluctuates from less than one hundred meters to kilometres (for examples from the literature see SOM Table A5), it is not only the neighbouring arable field that may act as a source of contamination. A correlation analysis of the area of arable fields in the surrounding landscape (buffered from 500 to 3500 m) and number of pesticide residues recorded in the insect-trapping ethanol revealed a best fit for a radius of 2000 m around the center of the trapping positions in the conservation area (Fig. 2, all 21 sites, Pearson correlation coefficient = 0.48, p = 0.029). The site Brauselay differed from all nature conservation areas as vineyards were bordering the nature conservation area. Wine growing is a permanent crop characterised by high fungicide use on a comparable small area. When removing Brauselay from the analysis significance increased further (Pearson correlation coefficient = 0.60, p = 0.005; for further details, see SOM Fig. A2 and Table A6). Hence, pesticide residues on insects collected in the nature conservation areas are not only a result of applications on crops in the direct vicinity, but also from pesticide use in a larger area within the agricultural landscape around the conservation areas.Figure 2The number of CUP residues per site detected in insect/ethanol samples increased with the area of agriculture in a radius of 2000 m around the trapping positions (Pearson correlation coefficient = 0.48, p = 0.029).Full size imageBased on the correlation between pesticides and surrounding arable land, a generalized linear mixed model (GLMM) was applied to model the number of detected pesticide residues as a function of landscape factors (amount of agricultural production area, amount of nature conservation area and amount of FFH area in a 2000 m radius) and biomass of insects collected by the Malaise traps, with the study sites included as random effects (Table 3). Neither the area of the nature conservation area nor the FFH area nor biomass of collected insects was related to the number of pesticides recorded in ethanol samples. Only the agricultural production area in a 2000 m vicinity had a significant (p  More

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    Spatial and temporal patterns in the sex ratio of American lobsters (Homarus americanus) in southwestern Nova Scotia, Canada

    1.Hanson, J. M. Predator-prey interactions of American lobster (Homarus americanus) in the southern Gulf of St. Lawrence, Canada. New Zeal. J. Mar. Freshw. Res. 43, 69–88 (2009).
    Google Scholar 
    2.DFO. Canada’s Fisheries Fast Facts 2019. (2020).3.Fisheries and Oceans Canada. Integrated Fishery Management Plan (Summary). Lobster fishing area 27–38. Scotia-Fundy Sector Maritimes Region 2011. DFO Report (2009).4.Howell, W. H., Watson, W. H. & Jury, S. H. Skewed sex ratio in an estuarine lobster (Homarus americanus) population. J. Shellfish Res. 18, 193–201 (1999).
    Google Scholar 
    5.Jury, S. H., Pugh, T. L., Henninger, H., Carloni, J. T. & Watson, W. H. Patterns and possible causes of skewed sex ratios in American lobster (Homarus americanus) populations. Invertebr. Reprod. Dev. https://doi.org/10.1080/07924259.2019.1595184 (2019).Article 

    Google Scholar 
    6.Ogburn, B. M. The effects of sex-biased fisheries on crustacean sex ratios and reproductive output. Invertebr. Reprod. Dev. 63, 200–207 (2019).
    Google Scholar 
    7.Cooper, R., Clifford, R. & Newelll, C. Seasonal abundance of the American lobster, Homarus americanus, in the Boothbay region of Maine. Trans. Am. Fish. Soc. 104, 669–674 (1975).
    Google Scholar 
    8.Pitnick, S. Operational sex ratios and sperm limitation in populations of Drosophila pachea. Behav. Ecol. Sociobiol. 33, 383–391 (1993).
    Google Scholar 
    9.MacDiarmid, A. B. & Butler, M. J. IV. Sperm economy and limitation in spiny lobsters. Behav. Ecol. Sociobiol. 46, 14–24 (1999).
    Google Scholar 
    10.Sato, T. Plausible causes for sperm-store variations in the coconut crab Birgus latro under large male-selective harvesting. Aquat. Biol. 13, 11–19 (2011).
    Google Scholar 
    11.Ogburn, M., Roberts, P., Richie, K., Johnson, E. & Hines, A. Temporal and spatial variation in sperm stores in mature female blue crabs Callinectes sapidus and potential effects on brood production in Chesapeake Bay. Mar. Ecol. Prog. Ser. 507, 249–262 (2014).ADS 

    Google Scholar 
    12.Pardo, L. M., Rosas, Y., Fuentes, J. P., Riveros, M. P. & Chaparro, O. R. Fishery induces sperm depletion and reduction in male reproductive potential for crab species under male-biased harvest strategy. PLoS ONE 10, e0115525 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    13.Pardo, L. M. et al. High fishing intensity reduces females’ sperm reserve and brood fecundity in a eubrachyuran crab subject to sex-and size-biased harvest. ICES J. Mar. Sci. 74, 2459–2469 (2017).
    Google Scholar 
    14.Tremblay, J. M. & Smith, S. J. Lobster (Homarus americanus) catchability in different habitats in late spring and early fall. Mar. Freshw. Res. 52, 1321–1331 (2001).
    Google Scholar 
    15.Karnofsky, E., Atema, J. & RH, E. Field observations of social behavior, shelter use, and foraging in the lobster, Homarus americanus. Biol. Bull. 176, 239–246 (1989).PubMed 

    Google Scholar 
    16.Cowan, D. F., Watson, W., Solow, A. & Mountcastle, A. Thermal histories of brooding lobsters, Homarus americanus, in the Gulf of Maine. Springer 150, 463–470 (2007).
    Google Scholar 
    17.Chang, J., Chen, Y., Holland, D. & Grabowski, J. Estimating spatial distribution of American lobster Homarus americanus using habitat variables. Mar. Ecol. Prog. Ser. 420, 145–156 (2010).ADS 

    Google Scholar 
    18.Anderson, J., Olsen, Z., Wagner Glen Sutton, T., Gelpi, C. & Topping, D. Environmental drivers of the spatial and temporal distribution of spawning blue crabs Callinectes sapidus in the Western Gulf of Mexico. N. Am. J. Fish. Manag. 37, 920–934 (2017).
    Google Scholar 
    19.Crossin, G. T., Al-Ayoub, S. A., Jury, S. H., Howell, W. H. & Watson, W. H. Behavioral thermoregulation in the American lobster Homarus americanus. J. Exp. Biol. 201, 365–374 (1998).PubMed 
    CAS 

    Google Scholar 
    20.Powers, J., Lopez, G., Cerrato, R. & Dove, A. Effects of thermal stress on Long Island Sound lobsters, H. americanus. in Long Island Sound Lobster Research Initiative Working Meeting. University of Connecticut at Avery Point, Groton. (2004).21.Comeau, M. & Savoie, F. Maturity and reproductive cycle of the female American lobster, Homarus americanus, in the southern Gulf of St. Lawrence, Canada. J. Crustac. Biol. https://doi.org/10.1163/20021975-99990290 (2002).Article 

    Google Scholar 
    22.Quinn, B. K. Threshold temperatures for performance and survival of American lobster larvae: A review of current knowledge and implications to modeling impacts of climate change. Fish. Res. 186, 383–396 (2017).
    Google Scholar 
    23.Campbell, A. & Stasko, A. Movement of lobsters (Homarus americanus) tagged in the Bay of Fundy, Canada. Mar. Biol. 92, 393–404 (1986).
    Google Scholar 
    24.Campbell, A. Aggregations of berried lobsters (Homarus americanus) in shallow waters off Grand Manan, eastern Canada. Can. J. Fish. Aquat. Sci. 47, 520–523 (1990).
    Google Scholar 
    25.Watson, W. & Jury, S. H. The relationship between American lobster catch, entry rate into traps and density. Taylor Fr. 9, 59–68 (2013).
    Google Scholar 
    26.Hoegh-Guldberg, O. & Bruno, J. F. The impact of climate change on the world’s marine ecosystems. Science 328, 1523–1528 (2010).ADS 
    PubMed 
    CAS 

    Google Scholar 
    27.Cheng, L. et al. Improved estimates of ocean heat content from 1960 to 2015. Sci. Adv. 3, 10 (2017).
    Google Scholar 
    28.Aiken, D. E. & Waddy, S. L. Environmental influence on recruitment of the American lobster, Homarus americanus: A perspective. Can. J. Fish. Aquat. Sci. 43, 2258–2270 (1986).
    Google Scholar 
    29.Greenan, B. J. W. et al. Climate change vulnerability of American lobster fishing communities in Atlantic Canada. Front. Mar. Sci. 6, 579 (2019).
    Google Scholar 
    30.QGIS Geographic Information System. QGIS Association. http://www.qgis.org/ (2021).31.Tveite, H. NNJoin. http://arken.nmbu.no/~havatv/gis/qgisplugins/NNJoin (2014).32.Hosmer, D. J., Lemeshow, S. & Sturdivant, R. Applied Logistic Regression (John Wiley & Sons, 2013).MATH 

    Google Scholar 
    33.Thakur, K. K. et al. Risk factors associated with soft-shelled lobsters (Homarus americanus) in southwestern Nova Scotia, Canada. FACETS 2, 15–33 (2017).
    Google Scholar 
    34.Dohoo, I., Martin, W. & Stryhn, H. Veterinary Epidemiologic Research (VER Inc., 2009).
    Google Scholar 
    35.Pezzack, D. S. et al. The American lobster Homarus americanus fishery off of south-western Nova Scotia (Lobster Fishing Area 34). Canadian Stock Assessment Secretariat Research Document 99/32 (1999).36.Watson, W. H. & Little, S. A. Differences in the size at maturity of female American lobsters, Homarus americanus, captured throughout the range of the offshore fishery. J. Crustac. Biol. 25, 585–592 (2005).
    Google Scholar 
    37.Pezzack, D., Tremblay, J., Claytor, R., Frail, C. & Smith, S. Stock status and indicators for the lobster fishery in Lobster Fishing Area 34. Canadian Stock Assessment Secretariat Research Document 2006/101 (2006).38.Wu, Y. & Tang, C. Atlas of ocean currents in eastern Canadian waters. Canadian Technical Report of Hydrography and Ocean Sciences. 271 (2011).39.Brickman, D. Could ocean currents be responsible for the west to east spread of aquatic invasive species in Maritime Canadian waters?. Mar. Pollut. Bull. 85, 235–243 (2014).PubMed 
    CAS 

    Google Scholar 
    40.Cowan, D. F., Solow, A. & Beet, A. R. Patterns in abundance and growth of juvenile lobster Homarus americanus. CSIRO https://doi.org/10.1071/MF01191 (2001).Article 

    Google Scholar 
    41.Morse, B. L., Quinn, B. K., Comeau, M. & Rochette, R. Stock structure and connectivity of the American lobster (Homarus americanus) in the southern Gulf of St. Lawrence: Do benthic movements matter?. Can. J. Fish. Aquat. Sci. 75, 2096–2108 (2018).
    Google Scholar 
    42.Staples, K. W., Chen, Y., Townsend, D. W. & Brady, D. C. Spatiotemporal variability in the phenology of the initial intra-annual molt of American lobster (Homarus americanus Milne Edwards, 1837) and its relationship with bottom temperatures in a changing Gulf of Maine. Fish. Oceanogr. 28, 468–485 (2019).
    Google Scholar 
    43.Goñi, R., Quetglas, A. & Reñones, O. Differential catchability of male and female European spiny lobster Palinurus elephas (Fabricius, 1787) in traps and trammelnets. Fish. Res. 65, 295–307 (2003).
    Google Scholar 
    44.Audet, D., Miron, G. & Moriyasu, M. Biological characteristics of a newly established green crab (Carcinus maenas) population in the southern gulf of St. Lawrence, Canada. J. Shellfish Res. 27, 427–441 (2008).
    Google Scholar 
    45.Laurans, M., Fifas, S., Demaneche, S., Brérette, S. & Debec, O. Modelling seasonal and annual variation in size at functional maturity in the European lobster (Homarus gammarus) from self-sampling data. ICES J. Mar. Sci. 66, 1892–1898 (2009).
    Google Scholar 
    46.Cooper, R. & Uzmann, J. Migrations and growth of deep-sea lobsters, Homarus americanus. Science 171, 288–290 (1971).ADS 
    PubMed 
    CAS 

    Google Scholar 
    47.Robichaud, D. A. & Campbell, A. Annual and seasonal size-frequency changes of trap-caught lobsters (Homarus americanus) in the Bay of Fundy. J. Northw. Atl. Fish. Sci 11, 2 (1991).
    Google Scholar 
    48.Waddy, S. L. & Aiken, D. E. Seasonal variation in spawning by preovigerous American lobster (Homarus americanus) in response to temperature and photoperiod manipulation. Can. J. Fish. Aquat. Sci. 49, 1114–1117 (1992).
    Google Scholar 
    49.Campbell, A. & Stasko, A. B. Movements of lobsters (Homarus americanus) tagged in the Bay of Fundy, Canada. Mar. Biol. Int. J. Life Ocean. Coast. Waters 92, 393–404 (1986).
    Google Scholar 
    50.Haakonsen, H. & Anoruo, A. Tagging and migration of the American lobster Homarus americanus. Rev. Fish. Sci. 2, 79–93 (1994).
    Google Scholar 
    51.Lawton, P. & Lavalli, K. Postlarval, juvenile, adolescent and adult ecology. In Biology of the lobster Homarus americanus (ed. Jd, F.) 47–81 (Academic, 1995).
    Google Scholar 
    52.Attard, J. & Hudon, C. Embryonic development and energetic investment in egg production in relation to size of female lobster (Homarus americanus). Can. J. Fish. Aquat. Sci. 44, 1157–1164 (1987).
    Google Scholar 
    53.Krouse, J. Maturity, sex ratio, and size composition of the natural population of American lobster, Homarus americanus, along the Maine coast. Fish. Bull. 71, 165–173 (1973).
    Google Scholar 
    54.Sato, T. Impacts of large male-selective harvesting on reproduction: Illustration with large decapod crustacean resources. Aqua-BioSci. Monogr. 5, 67–102 (2012).CAS 

    Google Scholar 
    55.Raymond, S. M. C. & Todd, C. R. Assessing risks to threatened crayfish populations from sex-based harvesting and differential encounter rates: A new indicator for reproductive state. Ecol. Indic. 118, 106661 (2020).
    Google Scholar 
    56.Estrella, B. & McKiernan, D. Catch-Per-Unit-Effort and Biological Parameters from the Massachusetts Coastal Lobster (Homarus americanus) Resource: Description and Trends (NOAA Technical Report, 1989).
    Google Scholar 
    57.Smolowitz, R., Chistoserdov, A. Y. & Hsu, A. A description of the pathology epizootic shell disease in the American lobster (Homarus americanus) H. Milne Edwards 1837. J. Shellfish Res. 24, 749–756 (2005).
    Google Scholar 
    58.Glenn, R. & Pugh, T. Epizootic shell disease in American lobster (Homarus americanus) in Massachusetts coastal waters: Interactions of temperature, maturity, and intermolt duration. J. Crustac. Biol. 26, 639–645 (2006).
    Google Scholar 
    59.Chistoserdov, A., Quinn, R., Gubbala, S. & Smolowitz, R. Bacterial communities associated with lesions of shell disease in the American lobster Homarus americanus. J. Shellfish Res. 31, 449–462 (2012).
    Google Scholar 
    60.Meres, N. et al. Dysbiosis in epizootic shell disease of the American lobster (Homarus americanus). J. Shellfish Res. 31, 463–472 (2012).
    Google Scholar 
    61.Shields, J. D., Wheeler, K. N. & Moss, J. A. Histological assessment of the lobster (Homarus americanus) in the ‘100 Lobsters’ project. J. Shellfish Res. 31, 439–447 (2012).
    Google Scholar 
    62.Hoenig, J. M. et al. Impact of disease on the survival of three commercially fished species. Ecol. Appl. 27, 2116–2127 (2017).PubMed 

    Google Scholar 
    63.Stevens, B. Effects of epizootic shell disease in American lobster Homarus americanus determined using a quantitative disease index. Dis. Aquat. Organ. 88, 25–34 (2009).PubMed 

    Google Scholar 
    64.Clark, A. S., Jury, S. H., Goldstein, J. S., Langley, T. G. & Watson, W. H. A comparison of American lobster size structure and abundance using standard and ventless traps. Fish. Res. 167, 243–251 (2015).
    Google Scholar 
    65.Jury, S., Kinnison, M., Howell, W., Winsor, H. & Watson, I. The behavior of lobsters in response to reduced salinity. J. Exp. Mar. Biol. Ecol. 180, 23–37 (1994).
    Google Scholar  More

  • in

    Traits of a mussel transmissible cancer are reminiscent of a parasitic life style

    1.Aktipis, A. The Cheating Cell: How Evolution Helps Us Understand and Treat Cancer (Princeton University Press, 2020).Book 

    Google Scholar 
    2.Martinez-Outschoorn, U. E. et al. Stromal–epithelial metabolic coupling in cancer: integrating autophagy and metabolism in the tumor microenvironment. Int. J. Biochem. Cell. B. 43(7), 1045–1051. https://doi.org/10.1016/j.biocel.2011.01.023 (2011).CAS 
    Article 

    Google Scholar 
    3.Ujvari, B. et al. Cancer and life-history traits: lessons from host-parasite interactions. Parasitology 143, 533–541. https://doi.org/10.1017/S0031182016000147 (2016).Article 
    PubMed 

    Google Scholar 
    4.Overstreet, R. M. & Lotz, J. M. Host-symbiont relationships: understanding the change from guest to pest. In The Rasputin Effect: Why Commensals and Symbionts Become Parasitic. Advances in Environmental Microbiology (ed. Hurst, C.) (Springer, Cham, 2016). https://doi.org/10.1007/978-3-319-28170-4_2.Chapter 

    Google Scholar 
    5.Combes, C. Parasitism: The Ecology and Evolution of Intimate Inter-actions (University of Chicago Press, 2001).
    Google Scholar 
    6.Dujon, A. M. et al. Transmissible cancers in an evolutionary Perspective. iScience 23(7), 101269. https://doi.org/10.1016/j.isci.2020.101269 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Murgia, C., Pritchard, J. K., Kim, S. Y., Fassati, A. & Weiss, R. A. Clonal origin and evolution of a transmissible cancer. Cell 126(3), 477–487. https://doi.org/10.1016/j.cell.2006.05.051 (2006).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Rebbeck, C. A., Thomas, R., Breen, M., Leroi, A. M. & Burt, A. Origins and evolution of a transmissible cancer. Evolution 63(9), 2340–2349. https://doi.org/10.1111/j.1558-5646.2009.00724.x (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    9.Pearse, A. M. & Swift, K. Allograft theory: transmission of devil facial-tumor disease. Nature 439(7076), 549. https://doi.org/10.1038/439549a (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    10.Pye, R. J. et al. A second transmissible cancer in Tasmanian devils. Proc. Natl. Acad. Sci. USA 113(2), 374–379. https://doi.org/10.1073/pnas.1519691113 (2016).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Metzger, M. J., Reinisch, C., Sherry, J. & Goff, S. P. Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161(2), 255–263. https://doi.org/10.1016/j.cell.2015.02.042 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    12.Metzger, M. J. et al. Widespread transmission of independent cancer lineages within multiple bivalve species. Nature 534(7609), 705–709. https://doi.org/10.1038/nature18599 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Yonemitsu, M. A. et al. A single clonal lineage of transmissible cancer identified in two marine mussel species in South America and Europe. ELife 8, 1029. https://doi.org/10.7554/eLife.47788 (2019).Article 

    Google Scholar 
    14.Garcia-Souto, D. et al. Mitochondrial genome sequencing of marine leukemias reveals cancer contagion between clam species in the Seas of Southern Europe. BioRxiv https://doi.org/10.1101/2021.03.10.434714 (2021).Article 

    Google Scholar 
    15.Hammel, M. et al. Prevalence and polymorphism of a mussel transmissible cancer in Europe. Mol. Ecol. 2, 1–16. https://doi.org/10.1111/mec.16052 (2021).CAS 
    Article 

    Google Scholar 
    16.Skazina, M. et al. First description of a widespread Mytilus trossulus-derived bivalve transmissible cancer lineage in M. trossulus itself. Sci. Rep. 11(5809), 56930 (2021).
    Google Scholar 
    17.Burioli, E. A. V. et al. Implementation of various approaches to study the prevalence, incidence and progression of disseminated neoplasia in mussel stocks. J. Invertebr. Patho. 168, 107271. https://doi.org/10.1016/j.jip.2019.107271 (2019).CAS 
    Article 

    Google Scholar 
    18.Murray, M., James, Z. H. & Martin, W. B. A study of the cytology and karyotype of the canine transmissible venereal tumour. Res. Vet. Sci. 10(6), 565–572. https://doi.org/10.1016/50034-5288(18)34394-7 (1969).CAS 
    Article 
    PubMed 

    Google Scholar 
    19.Hamede, R. K., McCallum, H. & Jones, M. Biting injuries and transmission of Tasmanian devil facial tumour disease. J. Anim. Ecol. 82(1), 182–190 (2013).Article 

    Google Scholar 
    20.Sunila, I. & Farley, C. Environmental limits for survival of sarcoma cells from the soft-shell clam Mya arenaria. Dis. Aquat. Organ. 7, 111–115. https://doi.org/10.3354/dao007111 (1989).Article 

    Google Scholar 
    21.Carballal, M. J., Barber, B. J., Iglesias, D. & Villalba, A. Neoplastic diseases of marine bivalves. J. Invertebr. Pathol. 131, 83–106. https://doi.org/10.1016/J.JIP.2015.06.004 (2015).Article 
    PubMed 

    Google Scholar 
    22.Carella, F., Figueras, A., Novoa, B. & De Vico, G. Cytomorphology and PCNA expression pattern in bivalves Mytilus galloprovincialis and Cerastoderma edule with haemic neoplasia. Dis. Aquat. Org. 105, 81–87. https://doi.org/10.3354/dao02612 (2013).Article 

    Google Scholar 
    23.Baudoin, M. Host castration as a parasitic strategy. Evolution 29, 335–352. https://doi.org/10.1111/j.1558-5646.1975.tb00213.x (1975).Article 
    PubMed 

    Google Scholar 
    24.Alderman, D. J., Van Banning, P. & Perez-Colomer, A. Two abnormal European oyster (Ostrea edulis) mortalities associated with an abnormal haemocytic condition. Aquaculture 10(4), 335–340. https://doi.org/10.1016/0044-8486(77)90124-7 (1977).Article 

    Google Scholar 
    25.Cosson-Mannevy, M. A., Wong, C. S. & Cretney, W. J. Putative neoplastic disorders in mussels (Mytilus edulis) from southern Vancouver Island waters, British Columbia. J. Invertebr. Pathol. 44(2), 151–160. https://doi.org/10.1016/0022-2011(84)90006-5 (1984).Article 

    Google Scholar 
    26.Brousseau, D. J. Seasonal aspects of sarcomatous neoplasia in Mya arenaria (soft-shell clam) from Long Island Sound. J. Invertebr. Pathol. 50(3), 269–276. https://doi.org/10.1016/0022-2011(87)90092-9 (1987).CAS 
    Article 
    PubMed 

    Google Scholar 
    27.Peters, E. C. Recent investigations on the disseminated sarcomas of marine bivalve molluscs. In: W. S. Fisher, editor. Diseases processes in marine bivalve mollusc. Washington, DC: special publication No. 18, American Fisheries Society. pp. 74–92 (1988).28.Ford, S. E., Barber, B. J. & Marks, E. Disseminated neoplasia in juvenile Eastern oyster Crassostrea virginica, and its relationship to the reproductive cycle. Dis. Aquat. Org. 28, 73–77. https://doi.org/10.3354/dao028073 (1997).Article 

    Google Scholar 
    29.Barber, B. J. Neoplastic diseases of commercially important marine bivalves. Aquat. Living Resour. 17, 449–466. https://doi.org/10.1051/alr:2004052 (2004).Article 

    Google Scholar 
    30.Randriananja, G. Evolution de la maturation de Mytilus edulis sur deux sites d’élevage du pertuis Breton : bouchots et filières. https://archimer.ifremer.fr/doc/00446/55762/57424.pdf (2006).31.Levitan, D. R. Sperm limitation, gamete competition and sexual selection in external fertilizers (eds. Birkhead, T. R., Moller, A. P.) 175–217. Sperm competition and sexual selection (Academic Press, 1998).32.Arzul, I. et al. Effects of temperature and salinity on the survival of Bonamia ostreae, a parasite infecting flat oysters Ostrea edulis. Dis. Aquat. Organ. 85, 67–75. https://doi.org/10.3354/dao02047 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    33.Greaves, M. & Maley, C. C. Clonal evolution in cancer. Nature 481(7381), 306–313. https://doi.org/10.1038/nature10762 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Scott, J. & Marusyk, A. Somatic clonal evolution: a selection-centric perspective. Biochim. Biophys. Acta Rev. Cancer 1867(2), 139–150 (2017).CAS 
    Article 

    Google Scholar 
    35.Moore, M. N. & Lowe, D. M. The cytology and cytochemistry of the hemocytes of Mytilus edulis and their response to experimentally injected carbon particles. J. Invertebr. Pathol. 29, 18–30. https://doi.org/10.1016/0022-2011(77)90167-7 (1977).CAS 
    Article 
    PubMed 

    Google Scholar 
    36.Rasmussen, L. P. D., Hage, E. & Karlog, O. An electron microscope study of the circulating leucocytes of the marine mussel, Mytilus edulis. J. Invertebr. Pathol. 45, 158–167. https://doi.org/10.1016/0022-2011(85)90005-9 (1985).Article 

    Google Scholar 
    37.Carballal, M. J., López, M. C., Azevedo, C. & Villalba, A. Hemolymph cell types of the mussel Mytilus galloprovincialis. Dis. Aquat. Org. 29, 127–135. https://doi.org/10.3354/dao029127 (1997).Article 

    Google Scholar 
    38.Frei, E. 3rd. & Freireich, E. J. Progress and perspectives in the chemotherapy of acute leukemia. Adv. Chemother. 2, 269–298. https://doi.org/10.1016/b978-1-4831-9930-6.50011-3 (1965).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Ellison, R. R. & Murphy, M. L. “Apparent doubling time” of leukemic cells in marrow. Clin. Res. 12, 284 (1964).
    Google Scholar 
    40.Hirt, A., Schmid, A. M., Ammann, R. & Leibungut, K. In pediatric lymphoblastic leukemia of B-Cell origin, a small population of primitive blast cells is noncycling, suggesting them to be leukemia stem cell candidates. Pediatr. Res. 69, 194–199. https://doi.org/10.1203/PDR.0b013e3182092716 (2011).Article 
    PubMed 

    Google Scholar 
    41.Shimomatsuya, T., Tanigawa, N. & Muraoka, R. Proliferative activity of human tumors: assessment using bromodeoxyuridine and flow cytometry. Jpn. J. Cancer Res. 82(3), 357–362. https://doi.org/10.1111/j.1349-7006.1991.tb01854.x (1991).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Ford, S., Schotthoefer, A. & Spruck, C. In vivo dynamics of the microparasite Perkinsus marinus during progression and regression of infections in Eastern oysters. J. Parasitol. 85(2), 273–282. https://doi.org/10.2307/3285632 (1999).CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Caza, F., Bernet, E., Veyrier, F. J., Betoulle, S. & St-Pierre, Y. Hemocytes released in seawater act as Troyan horses for spreading of bacterial infections in mussels. Sci. Rep. 10, 19696 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    44.McCallum, H. I. et al. Does terrestrial epidemiology apply to marine systems?. Trends Ecol. Evol. 19(11), 585–591. https://doi.org/10.1016/j.tree.2004.08.009 (2004).Article 

    Google Scholar 
    45.Ewald, P. W. Evolutionary biology and the treatment of signs and symptoms of infectious disease. J. Theor. Biol. 86(1), 169–176. https://doi.org/10.1016/0022-5193(80)90073-9 (1980).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    46.Poulin, R. Chapter 5-Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions (eds: Brockmann, H. J., Roper, T. J., Naguib, M., Wynne-Edwards, K. E., Mitani, J. C., Simmons, L. W.). Advances in the Study of Behavior, Academic Press 41, 151–186. https://doi.org/10.1016/S0065-3454(10)41005-0 (2010).47.Cremonte, F., Vázquez, N. & Silva, M. R. Gonad atrophy caused by disseminated neoplasia in Mytilus chilensis cultured in the Beagle Channel, Tierra Del Fuego Province, Argentina. J. Shellfish Res. 30, 845–849. https://doi.org/10.2983/035.030.0325 (2011).Article 

    Google Scholar 
    48.Tissot, T. et al. Host manipulation by cancer cells: expectations, facts, and therapeutic implications. BioEssays 38(3), 276–285. https://doi.org/10.1002/bies/201500163 (2016).Article 
    PubMed 

    Google Scholar 
    49.Thomas, F., Guégan, J. F., Michalakis, Y. & Renaud, F. Parasites and host life-history traits: implications for community ecology and species co-existence. Int. J. Parasitol. 30(5), 669–674. https://doi.org/10.1016/s0020-7519(00)00040-0 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    50.Charles, M. Etude des pathogènes, des conditions physiologiques et pathologiques impliqués dans les mortalités anormales de moules (Mytilus sp.). Biologie animale. Normandie Université. https://tel.archives-ouvertes.fr/tel-0.053331 (2019).51.Anderson, R. M. & May, R. M. Population biology of infectious diseases: part I. Nature 280, 361–367. https://doi.org/10.1038/280361a0 (1979).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    52.Kuris, A. M. Trophic interactions: similarity of parasitic castrators to parasitoids. Q. Rev. Biol. 49, 129–148 (1974).Article 

    Google Scholar 
    53.Faure, M. F., David, P., Bonhomme, F. & Bierne, N. Genetic hitchhiking in a subdivided population of Mytilus edulis. BMC Evol. Biol. 8, 164. https://doi.org/10.1186/1471-2148-8-164 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Bierne, N. The distinctive footprints of local hitchhiking in a varied environment and global hitchhiking in a subdivided population. Evolution 64(11), 3254–3272. https://doi.org/10.1111/j.1558-5646.2010.01050.x (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    55.Suquet, M. et al. Anesthesia in Pacific oyster Crassostrea gigas. Aquat. Living Resour. 22, 29–34. https://doi.org/10.1051/alr/2009006 (2009).CAS 
    Article 

    Google Scholar 
    56.Lubet, P. Recherches sur le cycle sexuel et l’émission des gamètes chez les Mytilidés et les Pectinidés. Rev Trav Inst Pêches marit. 23(4), 390–548 (1959).
    Google Scholar 
    57.Bierne, N. et al. Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M galloprovincialis. Mol. Ecol. 12(2), 447–61. https://doi.org/10.1046/j.1365-294x.2003.01730.x (2003).CAS 
    Article 
    PubMed 

    Google Scholar  More

  • in

    Global predictors of language endangerment and the future of linguistic diversity

    1.Rehg, K. L. & Campbell, L. The Oxford Handbook of Endangered Languages (Oxford Univ. Press, 2018).2.Romaine, S. in Language and Poverty (eds Harbert, W. et al.) Ch. 8 (Multilingual Matters, 2009).3.Sallabank, J. & Austin, P. The Cambridge Handbook of Endangered Languages (Cambridge Univ. Press, 2011).4.Sutherland, W. J. Parallel extinction risk and global distribution of languages and species. Nature 423, 276–279 (2003).CAS 
    Article 

    Google Scholar 
    5.Eberhard, D. M., Simons, G. F. & Fennig, C. D. Ethnologue: Languages of the World 22nd edn (SIL International, 2019); https://www.ethnologue.com/6.Moseley, C. Atlas of the World’s Languages in Danger (UNESCO Publishing, 2010); http://www.unesco.org/culture/en/endangeredlanguages/atlas7.Catalogue of Endangered Languages (University of Hawaii at Manoa, 2020); http://www.endangeredlanguages.com8.Campbell, L. & Okura, E. in Cataloguing the World’s Endangered Languages 1st edn (eds Campbell, L. & Belew, A.) 79–84 (Routledge, 2018).9.The IUCN Red List of Threatened Species Version 2019-2 (IUCN, 2019); http://www.iucnredlist.org10.Romaine, S. in The Routledge Handbook of Ecolinguistics (eds Fill, A. F. & Penz, H.) Ch. 3 (Routledge, 2017).11.Crystal, D. Language Death (Cambridge Univ. Press, 2000).12.Simons, G. F. Two centuries of spreading language loss. Proc. Linguist. Soc. Am. 4, 27–38 (2019).Article 

    Google Scholar 
    13.Krauss, M. The world’s languages in crisis. Language 68, 4–10 (1992).Article 

    Google Scholar 
    14.Brondizio, E. S., Settele, J., Díaz, S. & Ngo, H. T. (eds) Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES, 2019).15.Bowern, C. Language vitality: theorizing language loss, shift, and reclamation (Response to Mufwene). Language 93, e243–e253 (2017).Article 

    Google Scholar 
    16.Mufwene, S. S. Language vitality: The weak theoretical underpinnings of what can be an exciting research area. Language 93, e202–e223 (2017).Article 

    Google Scholar 
    17.Hua, X., Greenhill, S. J., Cardillo, M., Schneemann, H. & Bromham, L. The ecological drivers of variation in global language diversity. Nat. Commun. 10, 2047 (2019).Article 

    Google Scholar 
    18.Grenoble, L. A. & Whaley, L. J. in Endangered Languages (eds Grenoble, L. A. & Whaley, L. J.) 22–54 (Cambridge Univ. Press, 1998).19.Cardillo, M., Bromham, L. & Greenhill, S. J. Links between language diversity and species richness can be confounded by spatial autocorrelation. Proc. R. Soc. B 282, 20142986 (2015).Article 

    Google Scholar 
    20.Amano, T. et al. Global distribution and drivers of language extinction risk. Proc. R. Soc. B 281, 20141574 (2014).Article 

    Google Scholar 
    21.Loh, J. & Harmon, D. Biocultural Diversity: Threatened Species, Endangered Languages (WWF, 2014).22.Fishman, J. A. Reversing Language Shift: Theoretical and Empirical Foundations of Assistance to Threatened Languages Vol. 76 (Multilingual Matters, 1991).23.Lewis, M. P. & Simons, G. F. Assessing endangerment: expanding Fishman’s GIDS. Rev. Roum. Linguist. 55, 103–120 (2010).
    Google Scholar 
    24.Hinton, L. in The Green Book of Language Revitalization in Practice (eds Hinton, L. & Hale, K.) 413–417 (Brill, 2001).25.Hobson, J. R. Re-awakening Languages: Theory and Practice in the Revitalisation of Australia’s Indigenous Languages (Sydney Univ. Press, 2010).26.Di Marco, M. et al. A novel approach for global mammal extinction risk reduction. Conserv. Lett. 5, 134–141 (2012).Article 

    Google Scholar 
    27.Cardillo, M., Mace, G. M., Gittleman, J. L. & Purvis, A. Latent extinction risk and the future battlegrounds of mammal conservation. Proc. Natl Acad. Sci. USA 103, 4157–4161 (2006).CAS 
    Article 

    Google Scholar 
    28.Bolam, F. C. et al. How many bird and mammal extinctions has recent conservation action prevented? Conserv. Lett. 14, e12762 (2020).
    Google Scholar 
    29.Balmford, A. Extinction filters and current resilience: the significance of past selection pressures for conservation biology. Trends Ecol. Evol. 11, 193–196 (1996).CAS 
    Article 

    Google Scholar 
    30.Brenzinger, M. Language Death: Factual and Theoretical Explorations with Special Reference to East Africa (Mouton de Gruyter, 1992).31.Aikhenvald, A. Y. in Language Endangerment and Language Maintenance: An Active Approach (eds Bradley, D. & Bradley, M.) 24–33 (Taylor & Francis, 2002).32.Aikhenvald, A. Y. in Lectures on Endangered Languages: 5. Endangered Languages of the Pacific Rim (eds Sakiyama, O. & Endo, F.) 97–142 (ELPR, 2004).33.van Driem, G. in Language Diversity Endangered (ed. Brenzinger, M.) Ch. 14 (Mouton de Gruyter, 2007).34.Muysken, P. in Historicity and Variation in Creole Studies (eds Highfield, A. & Valdman, A.) 52–78 (Karoma, 1981).35.Gal, S. Language Shift: Social Determinants of Linguistic Change in Bilingual Austria (Academic Press, 1979).36.Holmquist, J. Social correlates of a linguistic variable: a study in a Spanish village. Lang. Soc. 14, 191–203 (1985).Article 

    Google Scholar 
    37.Dobrin, L. M. in Endangered Languages: Beliefs and Ideologies in Language Documentation and Revitalization (eds Austin, P. K. & Sallabank, J.) Ch. 7 (British Academy, 2014).38.Sasse, H.-J. in Language Death: Factual and Theoretical Explorations with Special Reference to East Africa (ed Brenzinger M.) 7–30 (Mouton de Gruyter, 1992).39.Wang, Y. & Phillion, J. Minority language policy and practice in China: the need for multicultural education. Int. J. Multicult. Educ. 11, 1–14 (2009).
    Google Scholar 
    40.McCarty, T. L. in Language Policies in Education: Critical Issues (ed. Tollefson, J. W.) 285–307 (2002).41.Wiese, A.-M. & Garcia, E. E. The Bilingual Education Act: language minority students and equal educational opportunity. Biling. Res. J. 22, 1–18 (1998).Article 

    Google Scholar 
    42.Bromham, L., Hua, X., Algy, C. & Meakins, F. Language endangerment: a multidimensional analysis of risk factors. J. Lang. Evol. 5, 75–91 (2020).Article 

    Google Scholar 
    43.Gao, X. & Ren, W. Controversies of bilingual education in China. Int. J. Biling. Educ. Biling. 22, 267–273 (2019).Article 

    Google Scholar 
    44.Dimmendaal, G. J. in Investigating Obsolescence: Studies in Language Contraction and Death (ed. Dorian N. C.) 13-32 (Cambridge Univ. Press, 1989).45.Brenzinger, M. in Language Diversity Endangered (ed. Brenzinger, M.) IX–XVII (Mouton de Gruyter, 2007).46.Kuussaari, M. et al. Extinction debt: a challenge for biodiversity conservation. Trends Ecol. Evol. 24, 564–571 (2009).Article 

    Google Scholar 
    47.Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994).Article 

    Google Scholar 
    48.Meijer, J. R., Huijbregts, M. A., Schotten, K. C. & Schipper, A. M. Global patterns of current and future road infrastructure. Environ. Res. Lett. 13, 064006 (2018).Article 

    Google Scholar 
    49.Laurance, W. F. & Balmford, A. A global map for road building. Nature 495, 308–309 (2013).CAS 
    Article 

    Google Scholar 
    50.Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).CAS 
    Article 

    Google Scholar 
    51.Crawford, J. Language politics in the U.S.A.: the paradox of bilingual education. Soc. Justice 25, 50–69 (1998).
    Google Scholar 
    52.Hallett, D., Chandler, M. J. & Lalonde, C. E. Aboriginal language knowledge and youth suicide. Cogn. Dev. 22, 392–399 (2007).Article 

    Google Scholar 
    53.Taff, A. et al. in The Oxford Handbook of Endangered Languages (eds Rehg, K. & Campbell, L.) 862–883 (Oxford Univ. Press, 2018).54.Dinku, Y. et al. Language Use is Connected to Indicators of Wellbeing: Evidence from the National Aboriginal and Torres Strait Islander Social Survey 2014/15. CAEPR Working Paper no. 132/2019 (CAEPR, 2020); https://doi.org/10.25911/5ddb9fd6394e855.Essegbey, J., Henderson, B. & McLaughlin, F. Language Documentation and Endangerment in Africa (John Benjamins, 2015).56.Davis, J. L. Language affiliation and ethnolinguistic identity in Chickasaw language revitalization. Lang. Commun. 47, 100–111 (2016).Article 

    Google Scholar 
    57.Clyne, M. in Maintenance and Loss of Minority Languages (eds Fase, W. et al.) 17–36 (John Benjamins, 1992).58.Cardillo, M. et al. The predictability of extinction: biological and external correlates of decline in mammals. Proc. R. Soc. B 275, 1441–1448 (2008).Article 

    Google Scholar 
    59.Evans, N. Dying Words: Endangered Languages and What They Have to Tell Us Vol. 22 (John Wiley & Sons, 2011).60.Ndhlovu, F. in Language Planning and Policy: Ideologies, Ethnicities, and Semiotic Spaces of Power (eds Abdelhay, A. et al.) 133–151 (Cambridge Scholars, 2020).61.Hammarström, H., Forkel, R. & Haspelmath, M. Glottolog 4.1. http://glottolog.org (Max Planck Institute for the Science of Human History, 2019).62.Lewis, M. P., Simons, G. F. & Fennig, C. D. Ethnologue: Languages of the World 17th edn http://www.ethnologue.com (SIL International, 2013).63.King, K. A., Schilling-Estes, N., Lou, J. J., Fogle, F. & Soukup, B. Sustaining Linguistic Diversity: Endangered and Minority Languages and Language Varieties (Georgetown Univ. Press, 2008).64.Lee, N. H. & van Way, J. Assessing levels of endangerment in the Catalogue of Endangered Languages (ELCat) using the Language Endangerment Index (LEI). Lang. Soc. 45, 271–292 (2016).Article 

    Google Scholar 
    65.Language Vitality and Endangerment: International Expert Meeting on UNESCO Programme Safeguarding of Endangered Languages (UNESCO, 2003).66.Tershy, B. R., Shen, K.-W., Newton, K. M., Holmes, N. D. & Croll, D. A. The importance of islands for the protection of biological and linguistic diversity. BioScience 65, 592–597 (2015).Article 

    Google Scholar 
    67.Igboanusi, H. Is Igbo an endangered language? Multilingua 25, 443–452 (2006).Article 

    Google Scholar 
    68.Ravindranath, M. & Cohn, A. C. Can a language with millions of speakers be endangered? J. Southeast Asian Linguist. Soc. 7, 64–75 (2014).
    Google Scholar 
    69.Venter, O. et al. Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nat. Commun. 7, 12558 (2016).CAS 
    Article 

    Google Scholar 
    70.Bromham, L., Hua, X., Cardillo, M., Schneemann, H. & Greenhill, S. J. Parasites and politics: why cross-cultural studies must control for relatedness, proximity and covariation. R. Soc. Open Sci. 5, 181100 (2018).Article 

    Google Scholar 
    71.Bromham, L., Skeels, A., Schneemann, H., Dinnage, R. & Hua, X. There is little evidence that spicy food in hot countries is an adaptation to reducing infection risk. Nat. Hum. Behav. https://doi.org/10.1038/s41562-020-01039-8 (2021).72.Purvis, A., Cardillo, M., Grenyer, R. & Collen, B. in Phylogeny and Conservation (eds Purvis, A. et al.) 295–316 (Cambridge Univ. Press, 2005).73.Hurlbert, S. H. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187–211 (1984).Article 

    Google Scholar 
    74.Dow, M. M. Network autocorrelation regression with binary and ordinal dependent variables: Galton’s problem. Cross Cult. Res. 42, 394–419 (2008).Article 

    Google Scholar 
    75.Wurm, M. J., Rathouz, P. J. & Hanlon, B. M. Regularized ordinal regression and the ordinalNet R package. Preprint at https://arxiv.org/abs/1706.05003 (2017).76.Byrd, R. H., Lu, P., Nocedal, J. & Zhu, C. A limited memory algorithm for bound constrained optimization. SIAM J. Sci. Comput. 16, 1190–1208 (1995).Article 

    Google Scholar 
    77.Barro, R. L. & Lee, J.-W. A new data set of educational attainment in the world, 1950–2010. J. Dev. Econ. 104, 184–198 (2013).Article 

    Google Scholar 
    78.Leclerc, J. L’aménagement linguistique dans le monde http://www.axl.cefan.ulaval.ca/monde/index_alphabetique.htm (2019).79.Solt, F. The Standardized World Income Inequality Database, Version 8 https://doi.org/10.7910/DVN/LM4OWF (2019).80.Global Agro-ecological Zones (GAEZ v3.0) (FAO, IIASA, 2010). More

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    Distance sampling surveys reveal 17 million vertebrates directly killed by the 2020’s wildfires in the Pantanal, Brazil

    1.Chiang, F., Mazdiyasni, O. & AghaKouchak, A. Evidence of anthropogenic impacts on global drought frequency, duration, and intensity. Nat. Commun. 12, 2754 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    2.Spinoni, J., Naumann, G., Carrao, H., Barbosa, P. & Vogt, J. World drought frequency, duration, and severity for 1951–2010. Int. J. Climatol. 34, 2792–2804 (2014).
    Google Scholar 
    3.Duane, A., Castellnou, M. & Brotons, L. Towards a comprehensive look at global drivers of novel extreme wildfire events. Clim. Change 165(3), 1–21 (2021).
    Google Scholar 
    4.Krawchuk, M. A., Moritz, M. A., Parisien, M. A., Van Dorn, J. & Hayhoe, K. Global Pyrogeography: The current and future distribution of wildfire. PLoS ONE 4(4), e5102 (2009).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Williams, A. P. et al. Observed impacts of anthropogenic climate change on wildfire in California. Earth’s Fut. 7, 892–910 (2019).ADS 

    Google Scholar 
    6.Garcia, L. C. et al. Record-breaking wildfires in the world’s largest continuous tropical wetland: Integrative Fire Management is urgently needed for both biodiversity and humans. J. Environ. Manag. 293, 112870 (2021).CAS 

    Google Scholar 
    7.Bowman, D. M. J. S. et al. Vegetation fires in the Anthropocene. Nat. Rev. Earth Environ. 1, 500–515 (2020).ADS 

    Google Scholar 
    8.Criado, M. G., Myers-Smith, I. H., Bjorkman, A. D., Lehmann, C. E. R. & Stevens, N. Woody plant encroachment intensifies under climate change across tundra and savanna biomes. Glob. Ecol. Biogeogr. 29(5), 925–943 (2020).
    Google Scholar 
    9.Mancini, L. D., Corona, P. & Salvati, L. Ranking the importance of Wildfires’ human drivers through a multi-model regression approach. Environ. Impact Assess. Rev. 72, 177–186 (2018).
    Google Scholar 
    10.Moreira, F. et al. Landscape – wildfire interactions in southern Europe: Implications for landscape management. J. Environ. Manag. 92(10), 2389–2402 (2011).
    Google Scholar 
    11.Clarke, H. et al. The proximal drivers of large fires: A pyrogeographic study. Front. Earth Sci. 8, 90 (2020).ADS 

    Google Scholar 
    12.Abram, N. J. et al. Connections of climate change and variability to large and extreme forest fires in southeast Australia. Commun. Earth Environ. 2, 1 (2021).ADS 

    Google Scholar 
    13.Daskin, J. H., Aires, F. & Staver, A. C. Determinants of tree cover in tropical floodplains. Proc. R. Soc. B. 286, 20191755 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    14.Kotze, D. C. The effects of fire on wetland structure and functioning. Afr. J. Aquat. Sci. 38(3), 237–247 (2013).
    Google Scholar 
    15.Tedim, F. et al. Defining Extreme Wildfire Events: difficulties, challenges, and impacts. Fire 1, 9 (2018).
    Google Scholar 
    16.Libonati, R. et al. Sistema ALARMES – Alerta de área queimada Pantanal, situação final de 2020 https://www.researchgate.net/publication/350103205_Nota_Tecnica_012021_LASA-UFRJ_Queimadas_Pantanal_2020?channel=doi&linkId=6051109d92851cd8ce483fb1&showFulltext=true (2021).17.Libonati, R., DaCamara, C. C., Peres, F. L., de Carvalho, L. A. S. & Garcia, L. C. Rescue Brazil’s burning Pantanal wetlands. Nature 588, 217–219 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    18.Marengo, J. A. et al. Extreme drought in the Brazilian Pantanal in 2019–2020: Characterization, causes and impacts. Front. Water 3, 639204 (2021).
    Google Scholar 
    19.Marengo, J. A., Alves, L. M. & Torres, R. R. Regional climate change scenarios in the Brazilian Pantanal watershed. Clim. Res. 68(2–3), 201–213 (2016).
    Google Scholar 
    20.Hardesty, J., Myers, R. & Fulks, W. Fire, ecosystems, and people: A preliminary assessment of fire as a global conservation issue. George Wright Forum 22, 78–87 (2005).
    Google Scholar 
    21.Bliege Bird, R., Bird, D. W., Codding, B. F., Parker, C. H. & Jones, J. H. The “fire stick farming” hypothesis: Australian Aboriginal foraging strategies, biodiversity, and anthropogenic fire mosaics. Proc. Natl. Acad. Sci. USA 105(39), 14796–14801 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Beerling, D. J. & Osborne, C. P. The origin of the savanna biome. Glob. Chang. Biol. 12, 2023–2031 (2006).ADS 

    Google Scholar 
    23.Simon, M. F. et al. Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc. Natl. Acad. Sci. USA 106, 20359–20364 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    24.Pott, A. & Pott, V. J. Features and conservation of the Brazilian Pantanal wetland. Wetl. Ecol. Manag. 12, 547–552 (2004).
    Google Scholar 
    25.Ferraz-Vicentini, K. R. & Salgado-Laboriau, M. L. Palynological analysis of a palm swamp in Central Brasil. J. South Am. Earth Sci. 9(3–4), 207–219 (1996).ADS 

    Google Scholar 
    26.Engstrom, R. T. First-order fire effects on animals: review and recommendations. Fire Ecol. 6(1), 115–130 (2010).
    Google Scholar 
    27.Whelan, R. J., Rodgerson, L., Dickman, C. R. & Sutherland, E. F. Critical life processes of plants and animals: Developing a process-based understanding of population changes in fireprone landscapes (Cambridge University Press, 2002).
    Google Scholar 
    28.van Eeden, L. M. et al. Impacts of the unprecedented 2019–2020 bushfires on Australian animals. https://www.wwf.org.au/ArticleDocuments/353/WWF_Impacts-of-the-unprecedented-2019-2020-bushfires-on-Australian-animals.pdf.aspx (2020).29.Pacheco, L. F., Quispe-Calle, L. C., Suárez-Guzmán, F. A., Ocampo, M. & Claure-Herrera, A. J. Muerte de mamíferos por los incendios de 2019 en la Chiquitania. Ecol. Boliv. 56(1), 4–16 (2021).
    Google Scholar 
    30.Berlinck, C. B. et al. The Pantanal is on fire and only a sustainable agenda can save the largest wetland in the world. Braz. J. Biol. 82, e244200 (2021).CAS 
    PubMed 

    Google Scholar 
    31.Andersen, A. N., Woinarski, J. C. Z. & Parr, C. L. Savanna burning for biodiversity: Fire management for faunal conservation in Australian tropical savannas. Austral Ecol. 37, 658–667 (2012).
    Google Scholar 
    32.Komarek, R. Fire and the changing wildlife habitat. Proc. Tall Timbers Fire Ecol. Conf. 2, 35–43 (1963).
    Google Scholar 
    33.Layme, V. M. G., Lima, A. P. & Magnusson, W. E. Effects of fire, food availability and vegetation on the distribution of the rodent Bolomys lasiurus in an Amazonian savanna. J. Trop. Ecol. 20, 183–187 (2004).
    Google Scholar 
    34.Roberts, S. L., van Wagtendonk, J. W., Miles, A. K., Kelt, D. A. & Lutz, J. A. Modeling the effects of fire severity and spatial complexity on small mammals in Yosemite National Park, California. Fire Ecol. 4(2), 83–104 (2008).
    Google Scholar 
    35.Smith, J. K. Wildland Fire in Ecosystems: Effects of Fire on Fauna (Rocky Mountain Research Station, Colorado, 2000).36.Woinarski, J. C. Z. & Legge, S. The impacts of fire on birds in Australia’s tropical savannas. Emu 113(4), 319–352 (2013).
    Google Scholar 
    37.Pires, A. S., Fernandez, F. A., de Freitas, D. & Feliciano, B. R. Influence of edge and fire-induced changes on spatial distribution of small mammals in Brazilian Atlantic Forest fragments. Stud. Neotrop. Fauna Environ. 40(1), 7–14 (2005).
    Google Scholar 
    38.Silveira, L. F., Rodrigues, H. G., Jácomo, A. T. A. & Diniz Filho, J. A. F. Impact of wildfires on the megafauna of Emas National Park, Central Brazil. Oryx 33, 108–114 (1999).39.Tomas, W. M. et al. Checklist of mammals from Mato Grosso do Sul, Brazil. Iheringia, Sér. zool. 107(Suppl), e2017155 (2017).40.Tomas, W. M. et al. Mammals in the Pantanal wetland, Brazil (Pensoft Publishers, 2010).
    Google Scholar 
    41.Burnham, K. P., Anderson, D. R. & Laake, J. L. Estimation of density from line transect sampling of biological populations. Ecol. Monogr. 72, 1–202 (1980).
    Google Scholar 
    42.Jolly, W. M. et al. Climate-induced variations in global wildfire danger from 1979 to 2013. Nat. Commun. 6, 7537 (2015).ADS 
    CAS 
    PubMed 

    Google Scholar 
    43.Thielen, D. Quo vadis Pantanal? Expected precipitation extremes and drought dynamics from changing sea surface temperature. PLoS ONE 15(1), e0227437 (2020).44.Ciemer, C. et al. An early-warning indicator for Amazon droughts exclusively based on tropical Atlantic Sea surface temperatures. Environ. Res. Lett. 15, 094087 (2020).45.Boers, N., Marwan, N., Barbosa, H. M. J. & Kurths, J. A deforestation-induced tipping point for the South American monsoon system. Sci. Rep. 7, 41489 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Bergier, I. et al. Amazon rainforest modulation of water security in the Pantanal wetland. Sci. Total Environ. 619–620, 1116–1125 (2018).ADS 
    PubMed 

    Google Scholar 
    47.Hofmann, G. et al. The Brazilian Cerrado is becoming hotter and drier. Glob. Chang. Biol. 00, 1–14 (2021).
    Google Scholar 
    48.Tomas, W. M. et al. Sustainability Agenda for the Pantanal Wetland: perspectives on a collaborative interface for science, policy, and decision-making. Trop. Conserv. Sci. 12, 1–30 (2019).ADS 

    Google Scholar 
    49.Schulz, C. Physical, ecological and human dimensions of environmental change in Brazil’s Pantanal wetland: Synthesis and research agenda. Sci. Total Environ. 687, 1011–1027 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    50.Harris, M. B. et al. Safeguarding the Pantanal wetlands: Threats and conservation initiatives. Conserv. Biol. 19(3), 714–720 (2005).
    Google Scholar 
    51.Ely, P., Fantin-Cruz, I., Tritico, H. M., Girard, P. & Kaplan, D. Dam-induced hydrologic alterations in the rivers feeding the Pantanal. Front. Environ. Sci. 8, 256 (2020).
    Google Scholar 
    52.Roque, F. O. et al. Simulating land use changes, sediment yields, and pesticide use in the Upper Paraguay River Basin: Implications for conservation of the Pantanal wetland. Agric. Ecosyst. Environ. 314, 107405 (2021).53.Guerra, A. et al. Drivers and projections of vegetation loss in the Pantanal and surrounding ecosystems. Land Use Policy 91, 104388 (2020).54.Berlinck, C. N., Lima, L. H. A. & Carvalho Junior, E. A. R. Historical survey of research related to fire management and fauna conservation in the world and in Brazil. Biota Neotropica 21(3), e20201144 (2021).55.Estado de Mato Grosso do Sul. DECRETO Nº 15.654, de 15 de abril de 2021. Institui o Plano Estadual de Manejo Integrado do Fogo, e Dá Outras Providências. (Diário Oficial do Estado, Mato Grosso do Sul nº 10.477, 2021).56.Marino, E. et al. Forest fuel management for wildfire prevention in Spain: A quantitative SWOT analysis. Int. J. Wildland Fire 23, 373–384 (2014).
    Google Scholar 
    57.Finney, M. A. & Cohen, J. D. Expectation and Evaluation of Fuel Management Objectives (Rocky Mountain Research Station, Colorado, 2003).58.Amiro, B. D., Stocks, B. J., Alexander, M. E., Flannigan, M. D. & Wotton, B. M. Fire, climate change, carbon and fuel management in the Canadian boreal forest. Int. J. Wildland Fire 10(4), 405–413 (2001).
    Google Scholar 
    59.Rocca, M. E., Brown, P. M., MacDonald, L. H. & Carrico, C. M. Climate change impacts on fire regimes and key ecosystem services in Rocky Mountain forests. Forest Ecol. Manag. 327, 290–305 (2014).
    Google Scholar 
    60.Pott, V. J., Pott, A., Lima, L. C. P., Moreira, S. N. & Oliveira, A. K. M. Aquatic macrophyte diversity of the Pantanal wetland and upper basin. Braz. J. Biol. 71(1), 255–563 (2011).CAS 
    PubMed 

    Google Scholar 
    61.Britski, H. A., Silimon, K. Z. S. & Lopes, B. S. Peixes do Pantanal: Manual de Identificação (EMPRAPA, Brasília, 2007).62.Sousa, T. P. et al. Cytogenetic and molecular data Support the occurrence of three Gymnotus species (Gymnotiformes: Gymnotidae) used as live bait in Corumbá, Brazil: Implications for conservation and management of professional fishing. Zebrafish 14(2), 177–186 (2017).PubMed 

    Google Scholar 
    63.Piva, A., Caramaschi, U. & Albuquerque, N. R. A new species of Elachistocleis (Anura: Microhylidae) from the Brazilian Pantanal. Phyllomedusa 16(2), 143–154 (2017).
    Google Scholar 
    64.Strüssmann, C., Ribeiro, R. A. K., Ferreira, V. L., & Beda, A. D. F. Herpetofauna do Pantanal Brasileiro [Herpetofauna of the Brazilian Pantanal]. (Sociedade Brasileira de Herpetologia, Belo Horizonte, 2007).65.Ferreira, V. L. et al. Répteis do Mato Grosso do Sul [Reptiles from Mato Grosso do Sul]. Brazil. Iheringia Sér. Zool. 107(Suppl), e2017153 (2017).66.Nunes, A. P. Quantas espécies de aves ocorrem no Pantanal? [How many bird species do occur in the Pantanal?]. Atualidades Ornitológicas 160, 45–54 (2011).
    Google Scholar 
    67.Tubelis, D. P. & Tomas, W. M. Bird species of the Pantanal wetland, Brazil.. Ararajuba 11(1), 5–37 (2003).
    Google Scholar 
    68.Thomas, L. et al. Distance software: design and analysis of distance sampling surveys for estimating population size. J. Appl. Ecol. 47, 5–14 (2010).PubMed 

    Google Scholar  More

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    Statistical inference, scale and noise in comparative anthropology

    To the Editor — In an insightful Comment Bliege Bird and Codding1 highlight a number of important issues to consider in the analysis of cross-cultural anthropological data. However, a casual reader of the Comment could be forgiven for taking away the message that cross-cultural data in anthropology is inherently flawed, and so is of limited use. We want to emphasize that comparative analysis plays an essential role in all non-experimental sciences, including anthropology and archaeology. This is because when systems cannot be manipulated due to scales of time and space, or issues of logistics or ethics, the only way to evaluate alternative outcomes is by analysing the results of natural experiments. More