More stories

  • in

    Phosphorus supply affects long-term carbon accumulation in mid-latitude ombrotrophic peatlands

    1.Loisel, J. et al. A database and synthesis of northern peatland soil properties and Holocene carbon and nitrogen accumulation. Holocene 24, 1028–1042 (2014).
    Google Scholar 
    2.Loisel, J. et al. Insights and issues with estimating northern peatland carbon stocks and fluxes since the Last Glacial Maximum. Earth Sci. Rev. 165, 59–80 (2017).CAS 

    Google Scholar 
    3.Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, L13402 (2010).4.Scharlemann, J. P., Tanner, E. V., Hiederer, R. & Kapos, V. Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag. 5, 81–91 (2014).CAS 

    Google Scholar 
    5.Chambers, F. M., Barber, K. E., Maddy, D. & Brew, J. A 5500-year proxy-climate and vegetation record from blanket mire at Talla Moss, Borders, Scotland. The Holocene 7, 391–399 (1997).
    Google Scholar 
    6.Charman, D. J., Blundell, A., Chiverrell, R. C., Hendon, D. & Langdon, P. G. Compilation of non-annually resolved Holocene proxy climate records: stacked Holocene peatland palaeo-water table reconstructions from northern Britain. Quat. Sci. Rev. 25, 336–350 (2006).
    Google Scholar 
    7.Swindles, G. T. et al. Widespread drying of European peatlands in recent centuries. Nat. Geosci. 12, 922–928 (2019).CAS 

    Google Scholar 
    8.van der Linden, M. & van Geel, B. Late Holocene climate change and human impact recorded in a south Swedish ombrotrophic peat bog. Palaeogeogr. Palaeoclimatol. Palaeoecol. 240, 649–667 (2006).
    Google Scholar 
    9.Clymo, R. S. The limits to peat bog growth. Philos. Trans. R. Soc. B Biol. Sci. 303, 605–654 (1984).
    Google Scholar 
    10.Hessen, D. O., Ågren, G. I., Anderson, T. R., Elser, J. J. & de Ruiter, P. C. Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85, 1179–1192 (2004).
    Google Scholar 
    11.Damman, A. W. H. Distribution and movement of elements in ombrotrophic peat bogs. Oikos 30, 480–495 (1978).CAS 

    Google Scholar 
    12.Malmer, N. Patterns in the growth and the accumulation of inorganic constituents in the Sphagnum cover on ombrotrophic bogs in Scandinavia. Oikos 53, 105–120 (1988).CAS 

    Google Scholar 
    13.Wang, R. et al. Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100. Glob. Change Biol. 23, 4854–4872 (2017).
    Google Scholar 
    14.Du, E. et al. Imbalanced phosphorus and nitrogen deposition in China’s forests. Atmos. Chem. Phys. 16, 8571–8579 (2016).CAS 

    Google Scholar 
    15.Du, E. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226 (2020).CAS 

    Google Scholar 
    16.Bragazza, L. et al. Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proc. Natl. Acad. Sci. USA 103, 19386–19389 (2006).CAS 

    Google Scholar 
    17.Bragazza, L. et al. High nitrogen deposition alters the decomposition of bog plant litter and reduces carbon accumulation. Glob. Change Biol. 18, 1163–1172 (2012).
    Google Scholar 
    18.Aerts, R., Wallén, B. & Malmer, N. Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. J. Ecol. 80, 131–140 (1992).
    Google Scholar 
    19.Brahney, J., Mahowald, N., Ward, D. S., Ballantyne, A. P. & Neff, J. C. Is atmospheric phosphorus pollution altering global alpine Lake stoichiometry? Glob. Biogeochem. Cycles 29, 1369–1383 (2015).20.Charman, D. J. et al. Drivers of Holocene peatland carbon accumulation across a climate gradient in northeastern North America. Quat. Sci. Rev. 121, 110–119 (2015).
    Google Scholar 
    21.Charman, D. J. et al. Climate-related changes in peatland carbon accumulation during the last millennium. Biogeosciences 10, 929–944 (2013).
    Google Scholar 
    22.Beilman, D. W., MacDonald, G. M., Smith, L. C. & Reimer, P. J. Carbon accumulation in peatlands of West Siberia over the last 2000 years. Glob. Biogeochem. Cycles 23, GB1012 (2009).23.Wang, M., Moore, T. R., Talbot, J. & Richard, P. J. H. The cascade of C:N:P stoichiometry in an ombrotrophic peatland: from plants to peat. Environ. Res. Lett. 9, 024003 (2014).CAS 

    Google Scholar 
    24.Wang, M., Moore, T. R., Talbot, J. & Riley, J. L. The stoichiometry of carbon and nutrients in peat formation. Glob. Biogeochem. Cycles 29, 113–121 (2015).
    Google Scholar 
    25.Gorham, E. & Janssens, J. A. The distribution and accumulation of chemical elements in five peat cores from the mid-continent to the eastern coast of North America. Wetlands 25, 259–278 (2005).
    Google Scholar 
    26.Ratcliffe, J. L. et al. Rapid carbon accumulation in a peatland following Late Holocene tephra deposition, New Zealand. Quat. Sci. Rev. 246, 106505 (2020).
    Google Scholar 
    27.Kylander, M. E. et al. Mineral dust as a driver of carbon accumulation in northern latitudes. Sci. Rep. 8, 6876 (2018).28.Hughes, P. D. M. et al. The impact of high tephra loading on late-Holocene carbon accumulation and vegetation succession in peatland communities. Quat. Sci. Rev. 67, 160–175 (2013).
    Google Scholar 
    29.Limpens, J., Berendse, F. & Klees, H. How phosphorus availability affects the impact of nitrogen deposition on Sphagnum and vascular plants in bogs. Ecosystems 7, 793–804 (2004).CAS 

    Google Scholar 
    30.Fritz, C. et al. Nutrient additions in pristine Patagonian Sphagnum bog vegetation: can phosphorus addition alleviate (the effects of) increased nitrogen loads. Plant Biol. 14, 491–499 (2012).CAS 

    Google Scholar 
    31.White, J. R. & Reddy, K. R. Influence of phosphorus loading on organic nitrogen mineralization of everglades soils. Soil Sci. Soc. Am. J. 64, 1525 (2000).CAS 

    Google Scholar 
    32.Bledsoe, R. B., Goodwillie, C. & Peralta, A. L. Long-term nutrient enrichment of an oligotroph-dominated wetland increases bacterial diversity in bulk soils and plant rhizospheres. mSphere 5, e00035-20 (2020).
    Google Scholar 
    33.Lin, X. et al. Microbial community stratification linked to utilization of carbohydrates and phosphorus limitation in a boreal peatland at Marcell Experimental Forest, Minnesota, USA. Appl. Environ. Microbiol. 80, 3518–3530 (2014).
    Google Scholar 
    34.Sjögersten, S., Cheesman, A. W., Lopez, O. & Turner, B. L. Biogeochemical processes along a nutrient gradient in a tropical ombrotrophic peatland. Biogeochemistry 104, 147–163 (2011).
    Google Scholar 
    35.Cheesman, A. W., Turner, B. L. & Ramesh Reddy, K. Soil phosphorus forms along a strong nutrient gradient in a tropical ombrotrophic wetland. Soil Sci. Soc. Am. J. 76, 1496–1506 (2012).CAS 

    Google Scholar 
    36.Kivimäki, S. K., Sheppard, L. J., Leith, I. D. & Grace, J. Long-term enhanced nitrogen deposition increases ecosystem respiration and carbon loss from a Sphagnum bog in the Scottish Borders. Environ. Exp. Bot. 90, 53–61 (2013).
    Google Scholar 
    37.Moore, T. R., Knorr, K.-H., Thompson, L., Roy, C. & Bubier, J. L. The effect of long-term fertilization on peat in an ombrotrophic bog. Geoderma 343, 176–186 (2019).CAS 

    Google Scholar 
    38.Hill, B. H. et al. Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120, 203–224 (2014).CAS 

    Google Scholar 
    39.Vitousek, P. M. et al. Towards an ecological understanding of biological nitrogen fixation. In The Nitrogen Cycle at Regional to Global Scales (eds. Boyer, E. W. & Howarth, R. W.) 1–45 (Springer Netherlands, 2002).40.Larmola, T. et al. Methanotrophy induces nitrogen fixation during peatland development. Proc. Natl. Acad. Sci. USA 111, 734–739 (2014).CAS 

    Google Scholar 
    41.van den Elzen, E. et al. Symbiosis revisited: phosphorus and acid buffering stimulate N2 fixation but not Sphagnum growth. Biogeosciences 14, 1111–1122 (2017).
    Google Scholar 
    42.van den Elzen, E., Bengtsson, F., Fritz, C., Rydin, H. & Lamers, L. P. M. Variation in symbiotic N2 fixation rates among Sphagnum mosses. PLoS ONE 15, e0228383 (2020).
    Google Scholar 
    43.Toberman, H. et al. Dependence of ombrotrophic peat nitrogen on phosphorus and climate. Biogeochemistry 125, 11–20 (2015).CAS 

    Google Scholar 
    44.Basilier, K., Granhall, U., Stenström, T.-A. & Stenstrom, T.-A. Nitrogen fixation in wet minerotrophic moss communities of a subarctic mire. Oikos 31, 236 (1978).CAS 

    Google Scholar 
    45.Lin, X. et al. Microbial metabolic potential for carbon degradation and nutrient (nitrogen and phosphorus) acquisition in an ombrotrophic peatland. Appl. Environ. Microbiol. 80, 3531–3540 (2014).
    Google Scholar 
    46.Kox, M. A. R. et al. Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum. Plant Soil 406, 83–100 (2016).CAS 

    Google Scholar 
    47.Bubier, J. L., Moore, T. R. & Bledzki, L. A. Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog. Glob. Change Biol. 13, 1168–1186 (2007).
    Google Scholar 
    48.Fritz, C., Lamers, L. P. M., Riaz, M., van den Berg, L. J. L. & Elzenga, T. J. T. M. Sphagnum mosses – masters of efficient N-uptake while avoiding intoxication. PLoS ONE 9, e79991 (2014).
    Google Scholar 
    49.Morris, P. J. et al. Global peatland initiation driven by regionally asynchronous warming. Proc. Natl. Acad. Sci. USA 115, 4851–4856 (2018).CAS 

    Google Scholar 
    50.Schillereff, D. N. et al. Long-term macronutrient stoichiometry of UK ombrotrophic peatlands. Sci. Total Environ. 572, 1561–1572 (2016).CAS 

    Google Scholar 
    51.Sjöström, J. K. et al. Paleodust deposition and peat accumulation rates – bog size matters. Chem. Geol. 554, 119795 (2020).
    Google Scholar 
    52.Kylander, M. E. et al. Potentials and problems of building detailed dust records using peat archives: an example from Store Mosse (the “Great Bog”), Sweden. Geochim. Cosmochim. Acta 190, 156–174 (2016).CAS 

    Google Scholar 
    53.Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycles 22, 1–19 (2008).
    Google Scholar 
    54.Tipping, E. et al. Atmospheric deposition of phosphorus to land and freshwater. Environ. Sci.: Processes Impacts 16, 1608–1617 (2014).CAS 

    Google Scholar 
    55.Wang, R. et al. Significant contribution of combustion-related emissions to the atmospheric phosphorus budget. Nat. Geosci. 8, 48–54 (2015).CAS 

    Google Scholar 
    56.Newman, E. I. Phosphorus inputs to terrestrial ecosystems. J. Ecol. 83, 713–726 (1995).
    Google Scholar 
    57.Worrall, F., Moody, C. S., Clay, G. D., Burt, T. P. & Rose, R. The total phosphorus budget of a peat-covered catchment. J. Geophys. Res. Biogeosci. 121, 1814–1828 (2016).CAS 

    Google Scholar 
    58.Vitousek, P. M., Porder, S., Houlton, B. Z. & Chadwick, O. A. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol. Appl. 20, 5–15 (2010).
    Google Scholar 
    59.Bedford, B. L., Walbridge, M. R. & Aldous, A. Patterns in nutrient availability and plant diversity of temperate North American Wetlands. Ecology 80, 2151–2169 (1999).
    Google Scholar 
    60.Güsewell, S. N: P ratios in terrestrial plants: variation and functional significance: Tansley review. New Phytol. 164, 243–266 (2004).
    Google Scholar 
    61.Yan, J. et al. Preliminary investigation of phosphorus adsorption onto two types of iron oxide-organic matter complexes. J. Environ. Sci. 42, 152–162 (2016).CAS 

    Google Scholar 
    62.Barrow, N. J. Comparing two theories about the nature of soil phosphate. Eur. J. Soil Sci. 72, 679–685 (2021).CAS 

    Google Scholar 
    63.Bridgham, S. D., Pastor, J., Janssens, J. A., Chapin, C. & Malterer, T. J. Multiple limiting gradients in peatlands: a call for a new paradigm. Wetlands 16, 45–65 (1996).
    Google Scholar 
    64.Kuhry, P. & Vitt, D. H. Fossil carbon/nitrogen ratios as a measure of peat decomposition. Ecology 77, 271–275 (1996).
    Google Scholar 
    65.Kuhry, P., Halsey, L. A., Bayley, S. E. & Vitt, D. H. Peatland development in relation to Holocene climatic change in Manitoba and Saskatchewan (Canada). Can. J. Earth Sci. 29, 1070–1090 (1992).CAS 

    Google Scholar 
    66.Malmer, N. & Wallén, B. Input rates, decay losses and accumulation rates of carbon in bogs during the last millennium: internal processes and environmental changes. The Holocene 14, 111–117 (2004).
    Google Scholar 
    67.Malmer, N. & Holm, E. Variation in the C/N-quotient of peat in relation to decomposition rate and age determination with 210 Pb. Oikos 43, 171–182 (1984).CAS 

    Google Scholar 
    68.Larsson, A., Segerstrom, U., Laudon, H. & Nilsson, M. Holocene carbon and nitrogen accumulation rates and contemporary carbon export in discharge: a study from a boreal fen catchment. Holocene 27, 48 (2016), https://doi.org/10.1177/0959683616675936.69.Berendse, F. et al. Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Glob. Change Biol. 7, 591–598 (2001).
    Google Scholar 
    70.Juutinen, S., Bubier, J. L. & Moore, T. R. Responses of vegetation and ecosystem CO2 exchange to 9 years of nutrient addition at Mer Bleue bog. Ecosystems 13, 874–887 (2010).CAS 

    Google Scholar 
    71.Lequy, É., Legout, A., Conil, S. & Turpault, M. P. Aeolian dust deposition rates in Northern French forests and inputs to their biogeochemical cycles. Atmos. Environ. 80, 281–289 (2013).CAS 

    Google Scholar 
    72.Harrison, J. A., Caraco, N. & Seitzinger, S. P. Global patterns and sources of dissolved organic matter export to the coastal zone: results from a spatially explicit, global model. Glob. Biogeochem. Cycles 19, GB4S04 (2005).73.Yu, Z. Holocene carbon flux histories of the world’s peatlands: global carbon-cycle implications. The Holocene 21, 761–774 (2011).
    Google Scholar 
    74.Schlesinger, W. H. & Bernhardt, E. S. Biogeochemistry. (Elsevier, Amsterdam, 2013).
    Google Scholar 
    75.Peñuelas, J. et al. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4, 2934 (2013).76.Larmola, T. et al. Vegetation feedbacks of nutrient addition lead to a weaker carbon sink in an ombrotrophic bog. Glob. Change Biol. 19, 3729–3739 (2013).
    Google Scholar 
    77.Li, F. et al. Organic carbon linkage with soil colloidal phosphorus at regional and field scales: insights from size fractionation of fine particles. Environ. Sci. Technol. 55, 5815–5825 (2021).CAS 

    Google Scholar 
    78.Spohn, M. Increasing the organic carbon stocks in mineral soils sequesters large amounts of phosphorus. Glob. Change Biol. 26, 4169–4177 (2020).
    Google Scholar 
    79.Sjöström, J. Mid-Holocene Mineral Dust Deposition in Raised Bogs in Southern Sweden: Processes and Links. PhD thesis, Stockholm Univ. (2021).80.Gallego-Sala, A. V. et al. Latitudinal limits to the predicted increase of the peatland carbon sink with warming. Nat. Clim. Change 8, 907–913 (2018).CAS 

    Google Scholar 
    81.Wilson, R. M. et al. Stability of peatland carbon to rising temperatures. Nat. Commun. 7, 13723 (2016).CAS 

    Google Scholar 
    82.Dorrepaal, E. et al. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619 (2009).CAS 

    Google Scholar 
    83.Clymo, R. S. & Bryant, C. L. Diffusion and mass flow of dissolved carbon dioxide, methane, and dissolved organic carbon in a 7-m deep raised peat bog. Geochim. Cosmochim. Acta 72, 2048–2066 (2008).CAS 

    Google Scholar 
    84.Morris, P. J., Waddington, J. M., Benscoter, B. W. & Turetsky, M. R. Conceptual frameworks in peatland ecohydrology: looking beyond the two-layered (acrotelm-catotelm) model. Ecohydrology 4, 1–11 (2011).
    Google Scholar 
    85.Rydin, H. & Jeglum, J. The Biology of Peatlands (Oxford University Press, 2013).86.Limpens, J., Heijmans, M. M. P. D. & Berendse, F. The nitrogen cycle in boreal peatlands. Boreal Peatl. Ecosyst. 188, 195–230 (2006).CAS 

    Google Scholar 
    87.Biester, H., Knorr, K.-H., Schellekens, J., Basler, A. & Hermanns, Y.-M. Comparison of different methods to determine the degree of peat decomposition in peat bogs. Biogeosciences 11, 2691–2707 (2014).CAS 

    Google Scholar 
    88.Zaccone, C., Plaza, C., Ciavatta, C., Miano, T. M. & Shotyk, W. Advances in the determination of humification degree in peat since: Applications in geochemical and paleoenvironmental studies. Earth-Sci. Rev. 185, 163–178 (2018).CAS 

    Google Scholar 
    89.Alboukadel Kassambara. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.4.0. https://CRAN.R-project.org/package=ggpubr (CRAN, 2020).90.Legendre, P. & Oksanen, J. lmodel2: Model II Regression. R package version 1.7–3. https://CRAN.R-project.org/package=lmodel2 (CRAN, 2018).91.Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, New York, 2016).
    Google Scholar 
    92.Tipping, E. et al. Long-term increases in soil carbon due to ecosystem fertilization by atmospheric nitrogen deposition demonstrated by regional-scale modelling and observations. Sci. Rep. 7, 1890 (2017).CAS 

    Google Scholar 
    93.Bragazza, L. & Limpens, J. Dissolved organic nitrogen dominates in European bogs under increasing atmospheric N deposition. Glob. Biogeochem. Cycles 18, GB4018 (2004).94.Turunen, J., Roulet, N. T., Moore, T. R. & Richard, P. J. H. Nitrogen deposition and increased carbon accumulation in ombrotrophic peatlands in eastern Canada. Glob. Biogeochem. Cycles 18, 1–12 (2004).
    Google Scholar 
    95.Lund, M., Christensen, T. R., Mastepanov, M., Lindroth, A. & Ström, L. Effects of N and P fertilization on the greenhouse gas exchange in two northern peatlands with contrasting N deposition rates. Biogeosciences 6, 2135–2144 (2009).CAS 

    Google Scholar 
    96.Xu, J., Morris, P. J., Liu, J. & Holden, J. PEATMAP: refining estimates of global peatland distribution based on a meta-analysis. Catena 160, 134–140 (2018).
    Google Scholar  More

  • in

    The significance of region-specific habitat models as revealed by habitat shifts of grey-faced buzzard in response to different agricultural schedules

    Study regionsWe conducted the field survey in the Kyushu of southern Japan (Fig. 2a,b). The rice-transplanting schedule in Kyushu, is generally late (in late June24) because it is necessary to delay rice-transplanting timing after the harvest of wheat as a back crop22,23. However, since the technique of early transplanting was established around 1960, early transplanting (in early April24) has been practiced instead of a back crop of wheat in some areas in Kyushu25,26, so the rice-transplanting schedules differ at the regional scale. We established two study regions with early-transplanting schedules (Karatsu in northern Kyushu; N33.4, E129.9 and Amakusa in central Kyushu; N32.5, E130.1), and two study regions with late-transplanting schedules (Itoshima in northern Kyushu; N33.6, E130.2 and Uki in central Kyushu; N32.6, E130.8) (Fig. 2c–f). Each study region is 10–20 km2, and the distances between the regions are 20–140 km. Climatic conditions between the regions are similar (Supplementary Table S3). The size of each region is much larger than the size of the typical territory of breeding buzzards (approximately 500 m radius from the nest18).Figure 2Map of (a) Japan and (b) the entire study regions, (c) Karatsu, (d) Amakusa, (e) Itoshima and (f) Uki. Squares represent study blocks. Light and dark grey areas indicate waterbodies and residential areas, respectively. Background map source is the black map of Japan (http://www.craftmap.box-i.net/japan/line.php) and the topographic data of Fundamental Geospatial Data developed by the Geospatial Information Authority of Japan (https://www.gsi.go.jp/kiban/).Full size imageBuzzards surveyWe examined the distribution of buzzards in 2019. Buzzards are migratory birds that breed in Japan, northeastern China, and the Russian Far East in summer, and overwinter in the Ryukyu Islands, Southeast Asia, and southern China27. In our study regions, buzzards start breeding in April, soon after returning from their wintering area. Buzzards incubate their eggs from late April until late May when they hatch. Once the eggs hatch, buzzards feed nestlings. Then nestlings start to fledge in late June, but the adults continue feeding their fledglings for several weeks. Buzzards migrate to their wintering grounds around October. The breeding season of buzzards thus overlaps largely with the rice production season, but there is a slight but significant differences in seasonality, i.e., paddies are already planted and flooded before hatching in early rice-transplanting schedules, while not yet flooded in late rice-transplanting schedules.Because breeding buzzards were thought to prefer mosaic landscapes of farmland and forest17,19, we established 62 study blocks that included edges between farmland and forest in each study region (Fig. 2c–f; northern-early: 17 central-early: 11 northern-late: 17 central-late: 17). The study blocks were 400 m square and located at least 700 m apart from each other, a distance determined from the knowledge that buzzards intensively use an area of 200 m from their nests18. To examine the presence/absence of breeding buzzards in each block, we conducted 2 days of 30-min observations during the breeding season (April to July). Using a pilot study, we determined that this observation time was enough to minimize the possibility of missing buzzards. We identified breeding individuals based on displays, feeding behaviors, and territorial behaviors.Land use surveyDuring the brood-rearing period (late June to early July) in 2019, we recorded the land use (forest, grassland, flooded paddies, non-flooded paddies) in each block. We then used these data to create a land use map in each block using QGIS3.16.228 and overlaying it on Google Earth aerial photographs in 2017.Prey species surveyWe surveyed the distribution of prey species in paddies and grasslands in the study regions in 2019 and 2020. Based on the previous studies on the feeding habits of buzzards17,18,19,20,21, we surveyed the distribution of frogs and orthopterans larger than 3 cm as prey of this size is considered their main prey. We established survey transects in paddies and grasslands in our study blocks. We conducted surveys twice each year during the brood-rearing period (late June to early July), when breeding buzzards need a large amount of prey. We walked along the transects and counted the number of prey species observed within 0.5-m of both sides. This survey method is suitable to assess prey availability29 because buzzards visually search for prey (e.g.20,30). A total of 148 20 m-transects were placed in paddies in 34 blocks and 157 15-m transects were placed in grasslands in 37 blocks, and each transect was surveyed in both or either 2019 and 2020. In the paddy transects, we recorded the height and coverage of vegetation, the ditch characteristics (none, concrete ditch, earthen ditch), the surrounding land use (10 m width from the transect: flooded paddy, non-flooded paddy, grassland, forest, stone wall, and road), and flooding or non-flooding in the paddy field adjacent to transects. In grassland transects, we recorded the height and coverage of vegetation and the grassland types on which the transect was located (abandoned land, orchard, farmland, bank, forest edge).Statistical analysisBuzzard modelTo investigate the habitat selection of buzzards, we used a generalized linear model with a binomial error distribution. We used the edge length between the landscape elements and forest as independent variables, because the edge length, rather than the area of the landscape elements, is known to be an important determinant for buzzard distribution19. We prepared a land use map and calculated the edge length between the landscape elements and forest by using the field calculator of QGIS, and values were standardized (mean = 0 and SD = 1).To explore the variation in habitat selection across regions with different transplanting schedules, we first used a model that included the interaction term of transplanting schedules and landscape elements as independent variables. The length of paddy-forest edges, grassland-forest edges, the transplanting schedules, the interaction term of the edge length and the transplanting schedules, and the study regions were included as independent variables (details of independent variables: Supplementary Table S4). The presence/absence of breeding buzzards was included as a dependent variable. We analyzed the full model and all sub-models containing different combinations of all independent variables, including the null model. We regarded models that had ΔAIC values (the difference between the AIC value of the focal model and that of the best-fit model) of  0.6) to avoid serious multicollinearity.We performed all analyses in R 4.0.333, using the glmmTMB packages34 for model fitting, the MuMIn package35 for model selection and averaging, and the ggplot236 for graphic illustration or results. More

  • in

    Biogeochemical feedbacks to ocean acidification in a cohesive photosynthetic sediment

    1.Revelle, R. & Suess, H. E. Carbon dioxide exchange between atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9, 18–27 (1957).ADS 
    CAS 

    Google Scholar 
    2.Frankignoulle, M. A complete set of buffer factors for acid/base CO2 system in seawater. J. Mar. Syst. 5, 111–118 (1994).
    Google Scholar 
    3.Egleston, E. S., Sabine, C. L. & Morel, F. M. M. Revelle revisited: Buffer factors that quantify the response of ocean chemistry to changes in DIC and alkalinity. Glob. Biogeochem. Cycles 24, GB1002 (2010).ADS 

    Google Scholar 
    4.Bates, N. et al. A time-series view of changing surface ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography 27(1), 126–141 (2014).MathSciNet 

    Google Scholar 
    5.Lauvset, S., Gruber, N., Landschützer, P., Olsen, A. & Tjiputra, J. Trends and drivers in global surface ocean pH over the past 3 decades. Biogeosciences 12(5), 1285–1298 (2015).ADS 

    Google Scholar 
    6.Ríos, A. F. et al. Decadal acidification in the Atlantic. Proc. Natl. Acad. Sci. 112(32), 9950–9955 (2015).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Schulz, K. G. & Riebesell, U. Diurnal changes in seawater carbonate chemistry speciation at increasing atmospheric carbon dioxide. Mar. Biol. 160, 1889–1899 (2013).CAS 
    PubMed 

    Google Scholar 
    8.Provoost, P., van Heuven, S., Soetaert, K., Laane, R. W. P. M. & Middelburg, J. J. Seasonal and long-term changes in pH in the Dutch coastal zone. Biogeosciences 7, 3869–3878 (2010).ADS 
    CAS 

    Google Scholar 
    9.Hofmann, G. E. et al. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6, e28983 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Borges, A. V. & Gypens, N. Carbonate chemistry in the coastal zone responds more strongly to eutrophication than ocean acidification. Limnol. Oceanogr. 55, 346–353 (2010).ADS 
    CAS 

    Google Scholar 
    11.Cai, W.-J. et al. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770 (2011).ADS 
    CAS 

    Google Scholar 
    12.Sunda, W. G. & Cai, W.-J. Eutrophication induced CO2-acidification of subsurface coastal waters: Interactive effects of temperature, salinity, and atmospheric pCO2. Environ. Sci. Technol. 46, 10651–10659 (2012).ADS 
    CAS 
    PubMed 

    Google Scholar 
    13.Jury, C. P., Thomas, F. I. M., Atkinson, M. J. & Toonen, R. J. Buffer capacity, ecosystem feedbacks, and seawater chemistry under global change. Water 5, 1303–1325 (2013).CAS 

    Google Scholar 
    14.Hagens, M. et al. Biogeochemical processes and buffering capacity concurrently affect acidification in a seasonally hypoxic coastal marine basin. Biogeosciences 12, 1561–1583 (2015).ADS 

    Google Scholar 
    15.Santschi, P., Höhener, P., Benoit, G. & Buchholtz-ten, B. M. Chemical processes at the sediment–water interface. Mar. Chem. 30, 269–315 (1990).CAS 

    Google Scholar 
    16.Pawlik, J. R. Chemical ecology of the settlement of benthic marine invertebrates. Oceangr. Mar. Biol. Annu. Rev. 30, 273–335 (1992).
    Google Scholar 
    17.Marinelli, R. L. & Woodin, S. A. Experimental evidence for linkages between infaunal recruitment, disturbance, and sediment surface chemistry. Limnol. Oceanogr. 47(1), 221–229 (2002).ADS 
    CAS 

    Google Scholar 
    18.Clements, J. C. & Hunt, H. L. Marine animal behaviour in a high CO2 ocean. Mar. Ecol. Prog. Ser. 536, 259–279 (2015).ADS 
    CAS 

    Google Scholar 
    19.Vopel, K., Laverock, B., Cary, C. & Pilditch, C. A. Effects of warming and CO2 enrichment on O2 consumption, porewater oxygenation and pH of subtidal silt sediment. Aquat. Sci. 83, 8 (2021).CAS 

    Google Scholar 
    20.Green, M. A., Jones, M. E., Boudreau, C. L., Moore, R. L. & Westman, B. A. Dissolution mortality of juvenile bivalves in coastal marine deposits. Limnol. Oceanogr. 49(3), 727–734 (2004).ADS 

    Google Scholar 
    21.Green, M. A., Waldbusser, G., Reilly, S., Emerson, K. & O’Donnell, S. Death by dissolution: Sediment saturation state as a mortality factor for juvenile bivalves. Limnol. Oceanogr. 54(4), 1037–1047 (2009).ADS 
    CAS 

    Google Scholar 
    22.Green, M. A., Waldbusser, G. G., Hubazc, L., Cathcart, E. & Hall, J. Carbonate mineral saturation state as the recruitment cue for settling bivalves in marine muds. Estuaries Coasts 36, 18–27 (2013).CAS 

    Google Scholar 
    23.Clements, J. C., Woodard, K. D. & Hunt, H. L. Porewater acidification alters the burrowing behavior and post-settlement dispersal of juvenile soft-shell clams (Mya arenaria). J. Exp. Mar. Biol. Ecol. 477, 103–111 (2016).
    Google Scholar 
    24.Ries, J. B., Ghazaleh, M. N., Connolly, B., Westfield, I. & Castillo, K. D. Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim. Cosmochim. Acta 192, 318–337 (2016).ADS 
    CAS 

    Google Scholar 
    25.Nimer, N. A., Brownlee, C. & Merrett, M. J. Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol. 120, 105–112 (1999).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Hopkinson, B. M., Meile, C. & Shen, C. Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiol. 162, 1142–1152 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Tachibana, M. et al. Localization of putative carbonic anhydrase in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth. Res. 109, 205–221 (2011).CAS 
    PubMed 

    Google Scholar 
    28.Samukawa, M., Shen, C., Hopkinson, B. M. & Matsuda, Y. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth. Res. 121, 235–249 (2014).CAS 
    PubMed 

    Google Scholar 
    29.Matsuda, Y., Hopkinson, B. M., Nakajima, K., Dupont, C. L. & Tsuji, Y. Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: A gateway to carbon metabolism. Philos. Trans. R. Soc. B 372, 20160403 (2017).
    Google Scholar 
    30.Milligan, A. J. & Morel, F. M. M. A proton buffering role for silica in diatoms. Science 297, 1848–1850 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    31.Subhas, A. V. et al. Catalysis and chemical mechanisms of calcite dissolution in seawater. Proc. Natl. Acad. Sci. 114, 8175–8180 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Middelburg, J. J., Soetaert, K. & Hagens, M. Ocean alkalinity, buffering and biogeochemical processes. Rev. Geophys. 58, e2019RG000681 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Soetaert, K., Hofmann, A. F., Middelburg, J. J., Meysman, F. J. R. & Greenwood, J. The effect of biogeochemical processes on pH. Mar. Chem. 105, 30–51 (2007).CAS 

    Google Scholar 
    34.Zhu, Q., Aller, R. C. & Fan, Y. Two-dimensional pH distributions and dynamics in bioturbated marine sediments. Geochim. Cosmochim. Acta 70, 4933–4949 (2006).ADS 
    CAS 

    Google Scholar 
    35.Vopel, K., Del-Río, C. & Pilditch, C. A. Effects of CO2 enrichment on benthic primary production and inorganic nitrogen fluxes in two coastal sediments. Sci. Rep. 8, 1035 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167, 191–194 (1975).CAS 

    Google Scholar 
    37.Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to best practices for ocean CO2 measurements: PICES Special Publication 3. http://cdiac.ornl.gov/oceans/Handbook_2007.html (2007).38.Lewis, E. & Wallace, D. W. R. Program Developed for CO2 System Calculations. ORNL/CDIAC-105 (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, 1998).
    Google Scholar 
    39.Dickson, A. G. Standard potential of the reaction: AgCl(s) + 12H2(g) = Ag(s) + HCL(aq), and the standard acidity constant of the ion HSO4− in synthetic sea water from 273.15 to 318.15 K. J. Chem. Thermodyn. 22, 113–127 (1990).CAS 

    Google Scholar 
    40.Mehrbach, C., Culberson, C. H., Hawley, J. E. & Pytkowicz, R. N. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897–907 (1973).ADS 
    CAS 

    Google Scholar 
    41.Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissolution of carbonic acid in seawater media. Deep Sea Res. 34(10), 1733–1743 (1987).ADS 
    CAS 

    Google Scholar 
    42.Berg, P. N., Risgaard-Petersen, N. & Rysgaard, S. Interpretation of measured concentration profiles in sediment pore water. Limnol. Oceanogr. 43, 1500–1510 (1998).ADS 
    CAS 

    Google Scholar 
    43.Revsbech, N. P., Nielsen, L. P. & Ramsing, N. B. A novel microsensor for determination of apparent diffusivity in sediments. Limnol. Oceanogr. 43, 986–992 (1998).ADS 
    CAS 

    Google Scholar 
    44.Vopel, K., Pilditch, C. A., Wilson, P. & Ellwood, M. J. Oxidation of surface sediment: Effects of disturbance depth and seawater flow speed. Mar. Ecol. Prog. Ser. 392, 43–55 (2009).ADS 
    CAS 

    Google Scholar 
    45.Broecker, W. S. & Peng, T.-H. Gas exchange rates between air and sea. Tellus 26(1–2), 21–35 (1974).ADS 
    CAS 

    Google Scholar 
    46.Cussler, E. L. Diffusion: Mass Transfer in Fluid Systems (Cambridge University Press, 2009).
    Google Scholar 
    47.Li, Y.-H. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 38(5), 703–714 (1974).ADS 
    CAS 

    Google Scholar 
    48.Ullman, W. J. & Aller, R. C. Diffusion coefficients in nearshore marine sediments. Limnol. Oceanogr. 27(3), 552–556 (1982).ADS 
    CAS 

    Google Scholar 
    49.Jørgensen, B. B. & Revsbech, N. P. Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol. Oceanogr. 30(1), 111–122 (1985).ADS 

    Google Scholar 
    50.Rasmussen, H. & Jørgensen, B. B. Microelectrode studies of seasonal oxygen uptake in a coastal sediment: Role of molecular diffusion. Mar. Ecol. Prog. Ser. 81, 289–303 (1992).ADS 
    CAS 

    Google Scholar 
    51.Nordstrom, D. K., Jenne, E. A. & Ball, J. W. Redox equilibria of iron in acid mine waters. In Chemical Modeling in Aqueous Systems. American Chemical Society Symposium Series Vol. 93 (ed. Jenne, E. A.) 57–79 (American Chemical Society, 1979).
    Google Scholar 
    52.Dushoff, J., Kain, M. P. & Bolker, B. M. I can see clearly now: Reinterpreting statistical significance. Methods Ecol. Evol. 10, 756–759 (2019).
    Google Scholar  More

  • in

    Developing water, energy, and food sustainability performance indicators for agricultural systems

    Case studyThe Zayandeh-Rud basin (Fig. 1), a arid region of Iran, was selected to evaluate the SPIs. The Zayandeh-Rud basin is located in the central part of Iran. It has an area of 26,972 km2 area, where there are multiple water stakeholders such as agriculture, industry, urban and the environment sectors, with agriculture being the main user of the basin. Water resources in the basin are divided into surface water and groundwater. Approximately 100,000 ha among 113,000 ha of the agricultural area is irrigated by Zayandeh-Rud dam, and 3100 mm3 of water resources are used in the agricultural sector. The main surface water source in the basin, Zayandeh-Rud River originates in the Zagros Mountains and is about 350 km long in a west to east direction passing by the city of Isfahan. The Zayandeh-Rud River is an important water source for the agricultural, industrial, health, and urban sectors in Central Iran and the Chaharmahal-Bakhtiari and Isfahan provinces.Figure 1The location of the Zayandeh-Rud basin in Iran.Full size imageMulti-criteria decision makingMulti-criteria decision making includes two categories of multi-objective decision making and multi-criteria decision making, which are implemented to select the best decision among several alternatives or to evaluate decisions. This work applies decision making as a multi-criteria decision to achieve a goal. Each decision includes objectives, alternatives, and criteria. A problem’s goal is first defined. Alternatives are different options for wastewater management in this instance that are assigned weights based on their contribution to achieving the goal. Criteria are also factors that are measured by the purpose of the alternatives23. The AHP method helps achieve a defined goal after completing the steps outlined below.The AHP methodThe Analytical Hierarchy Process (AHP), developed by Saaty24, is a multi-criteria decision-making method for solving complex problems. It combines objective and quantitative evaluation in an integrated manner based on multi-level comparisons, and helps organize the essential aspects of a problem into a hierarchical format. It regularly organizes tangible and intangible factors and offers a structured and a relatively simple solution to decision problems. The AHP method ranks alternatives propose to tackle a decision-making problem. The ranking is based through a sequence of pairwise comparisons of evaluation criteria and sub-criteria.The AHP structureIn a hierarchical structure the communication flow is top-down. First, indicators and evaluation criteria are defined from experts who are asked for their expert opinions. The criteria serve the purpose of determining the relative worth of alternatives entertained to solve a multi-criteria decision-making problem. Thereafter, the problem is divided into criteria and sub-criteria for the evaluation of alternatives. Figure 2 depicts a generic AHP structure depicting a goal to be met with (n) = 4 evaluation criteria, and (m=3) alternatives to cope with a problem (in our case SIPs).Figure 2Goal, criteria, and alternatives in a generic hierarchical structure.Full size imageThe pairwise comparison matrixThe pairwise comparison matrix ((A)), called the Saaty Hierarchy Matrix, measures the importance of each criterion (or sub-criterion) relative to other criteria based on a numeric scale ranging from 1 to 9. Criteria that are extremely preferred, very strongly preferred, strongly preferred, moderately preferred, and equally preferred are assigned the values 9, 7, 5, 3, and 1, respectively, in the scale of preference; intermediate values are assigned to adjacent scales of preference. Thus, the values 8, 6, 4, and 2 are assigned respectively to the adjacent scales (9,7), (7,5), (5,3), and (3,1)24. These numerical assignment of values is made based on the opinion of experts25. The pairwise comparison matrix ((A)), therefore, represents a set of relative weights assigned to the criteria23. The general form of a pairwise comparison matrix when there are (n) evaluation criteria is written in Eq. (1):$$A=left[{a}_{ij}right]=left[begin{array}{cccc}{1=w}_{1}/{w}_{1}& {w}_{1}/{w}_{2}& dots & {w}_{1}/{w}_{n}\ {w}_{2}/{w}_{1}& 1={w}_{2}/{w}_{2}& dots & {w}_{2}/{w}_{n}\ .& .& dots & .\ .& .& dots & .\ .& .& dots & .\ {w}_{n}/{w}_{1}& {w}_{n}/{w}_{2}& …& 1={w}_{n}/{w}_{n}end{array}right]$$
    (1)

    where ({w}_{i}/{w}_{j}) denotes the weight assigned to the (i)-th criterion relative to the (j)-th criterion24. Clearly, ({a}_{ji}=1/{a}_{ij}), with ({a}_{ji}={a}_{ij}=1) when (i=j).The ratio matrixThe ratio matrix ((R)) has elements ({r}_{ij}) is calculated by Eq. (2):$$R=left[{r}_{ij}right]=left[begin{array}{cccc}1& {a}_{12}& dots & {a}_{1n}\ 1/{a}_{12}& 1& dots & {a}_{2n}\ .& .& .& .\ .& .& .& .\ .& .& .& .\ 1/{a}_{1n}& 1/{a}_{2n}& dots & 1end{array}right]$$
    (2)

    clearly, ({r}_{ij}={a}_{ij}) when (jge i), and ({r}_{ij}=1/{a}_{ji}) when (j More

  • in

    Foraging dive frequency predicts body mass gain in the Adélie penguin

    Study site and systemData were collected at Cape Crozier (77°27′S, 169°12′E), Ross Island, one of the largest Adélie penguin breeding colonies (~ 275 000 pairs at the time of the study32), during austral summer 2018–2019. Individuals arrive at Cape Crozier in late October/early November, lay (usually two) eggs in mid-November, and feed their chicks between mid-December and early February. They are one of the few penguin species that can fledge two chicks. During the brood/guard stage, one parent remains with the chick(s) while the other forages at sea. Nest reliefs at Crozier occur every 1–2 days during early chick-rearing and chicks are fed relatively small meals (0.43–0.58 kg) by the attending parent33. After about two weeks, chick demands are too great for adequate provisioning by one parent, so chicks are left on their own (“crèche” stage) while both parents forage simultaneously. Our study period included most of chick-rearing, i.e., all of the guard stage and half the crèche stage, from December 21, 2018 to January 15, 2019.Since 1997, every austral summer, the same subcolony of ~ 200 pairs (152 pairs in the year of study) was surrounded by a plastic fence, leaving only one opening as an access point, where the weighbridge was located30. The weighbridge consisted of an electronic scale, direction indicator, and radio frequency identification (RFID) reader34,35. In 2018–2019, it was installed on November 16 and removed on January 20. A subset of adult individuals were implanted with unique RFID tags beginning in 1997, with a few more added each year30,36. RFID code, date and time, direction, and weight were recorded automatically as the RFID-implanted birds crossed the weighbridge. Adults were captured on the nest during incubation, when they can be approached slowly and gently lifted off their nest. A warm hat was placed over the eggs or small chicks to avoid chilling, while the RFID tag was injected into the bird.All penguin survey, capture and handling methods used for data collection were performed following all relevant guidelines and regulations under the approval and oversight of the Institutional Animal Care and Use Committees of Oregon State University and Point Blue Conservation Science. Additionally, all work was approved and conducted under Antarctic Conservation Act permits issued by the US National Science Foundation and the U.S. Antarctic Program. The study is reported in accordance with ARRIVE guidelines.Diving parametersBetween November 2 and December 7, 2018, we equipped 32 RFID-implanted birds with geolocating dive recorders (“LUL” tags, 22 × 21 × 15 mm, weight = 4 g, from Atesys, Strasbourg, France, hereafter referred to as GDRs) that recorded light every minute, temperature (with a precision of ± 0.5 °C) every 30 s and pressure (with a precision of ± 0.3 m) every second for 12–15 months. Adults were captured using a hand net (2 m long handle) or on the nest during incubation (see above). The GDRs were encapsulated in flexible heat-shrink tubing shaped into a leg strap and attached to the tibio-fibula of each bird in the field using a polyester-coated stainless-steel zip tie to secure the ends of the strap together such that the tag could rotate freely around the leg but not slip over the tarsus joint. Tags were left in place for one year, with 21 recovered at the beginning of the 2019–2020 breeding season. Pressure data were processed in R (v. 3.6.0) with several processes modified from the diveMove package (v. 1.4.5)37. To correct for instrument drift, pressure data were zero offset corrected using the calibrateDepth function38. We used a depth threshold of 3 m to qualify as a dive. Following methods described in previous studies27,39,40, we computed a number of statistics about each dive including dive duration, maximum dive depth, post-dive interval duration, bottom time, the number of undulations (changes of any amplitude in underwater swimming duration from either ascent to descent, or descent to ascent—used for the purposes of categorizing dives) and the number of undulations  > 1 m (changes in underwater swimming direction from ascent to descent  > 1m39). The two undulation metrics are highly correlated (Pearson’s r = 0.92 in our data set). Bottom time was defined as the time spent at  > 60% of maximum depth of dive with  60 h (trip duration during chick-rearing takes 1–2 days on average36,39 but their frequency distribution showed a tail from 60 to 100 h in our data).Figure 2Conceptual visualization of the study design. (a) chick-rearing Adélie penguins breeding in a semi-enclosed subcolony are implanted with a RFID tag and equipped with a leg-mounted time-depth recorder (GDR). (b) Bird ID, departure mass and direction of travel are recorded by the weighbridge as penguins leave the colony to forage at sea. (c) During the foraging trip, the GDR tag records depth every second, enabling the calculation of several dive behavior metrics. (d) Bird ID, return mass and direction of travel are recorded by the weighbridge as penguins return to the colony to feed their chicks.Full size imageBody mass estimationFor each foraging trip, we calculated meal size and body mass change (see Supplementary Information for more details on the weight calculation). Meal size (in kg) is the difference between an individual’s out-mass (departing) and its most recent in-mass (returning from sea), i.e. this is a measure of how much food a parent left in the colony and includes both the food delivered to chicks and the food digested by the parent while attending the nest39. Body mass change (in kg) of individual birds over each foraging trip was calculated as the return mass (post-foraging trip at sea) minus the departure mass (pre-foraging trip at sea). Hence, body mass change measures the amount of food that was collected during the trip at sea (i.e. foraging success43), minus what could have been digested before returning to the colony at the end of this trip (Fig. 2). We further filtered trips based on these two variables, keeping only trips where meal size was  > 0 and  − 0.8 and  1 m per hour, as previous work indicated that undulations in the dive profile represent feeding and/or prey capture16,24,25, (2) dive (underwater) time per hour, (3) dive time per hour during foraging dives only, (4) bottom time per hour, (5) number of foraging dives per hour, (6) Attempts of Catch per Unit Effort (ACPUE, calculated as the number of undulations per trip divided by total bottom duration23,49). We also considered two variables calculated at the scale of dive bouts: (7) mean bout duration, thought to reflect the time spent within a prey patch50,51, (8) number of dives per bout, as an index of the size of the prey patch51,52,53. Dive bouts were defined as successive diving events interrupted by relatively longer surfacing periods. To separate post-dive intervals from inter-bout duration, we used a maximum likelihood approach54 using the diveMove package37 in R, which allowed us to determine a bout-ending-criterion (BEC). In this study, BEC = 47.6 s.Statistical analysesWe first calculated a Pearson correlation matrix using the corrplot package in R and removed highly correlated (r  > 0.7) behavioral covariates, keeping those that were the most correlated with body mass change. To test the hypothesis that some behavioral dive variables can be used to predict the amount of food collected while foraging at sea, we evaluated linear mixed models including body mass change as the dependent variable, each of the selected behavioral variables as independent variables and bird ID as a random effect, as well as a null model (intercept only) using the nlme package55 in R. Once we had determined the most competitive models, and as Adélie penguin’s foraging success can vary according to sex29,36 and chick needs39, and also be influenced by the trip duration56, we added sex, study day (day in the season as a Julian date with Dec 20 = 0) and trip duration (in hours) to the top intrinsic model(s) including potential interactions with the selected behavioral variable(s). A null model was also included in this second model set. Residuals were examined to verify normality, homogeneity of variances, and independence. To evaluate these models and determine the strength of evidence supporting specific effects, we used an information theoretic approach57. Models were ranked using the small-sample-size corrected version of Akaike Information Criterion (AICc), with the best model having the lowest AICc value. We calculated ΔAICc as the difference in AICc between each candidate model and the model with the lowest AICc value, and considered all models within 2 ΔAICc as competitive models57. We determined the strength of evidence supporting specific effects by examining the unstandardized effect sizes (slope coefficients and differences in means) and the associated 95% confidence intervals (CI). If the 95% CI for a parameter in a competitive model (ΔAICc  More

  • in

    Cost-effective surveillance of invasive species using info-gap theory

    1.Jenkins, P. T. Free trade and exotic species introductions. Conserv. Biol. 10, 300–302 (1996).Article 

    Google Scholar 
    2.Sharov, A. A. Bioeconomics of managing the spread of exotic pest species with barrier zones. Risk Anal. 24, 879–892 (2004).Article 

    Google Scholar 
    3.Lodge, D. M. et al. Biological invasions: Recommendations for U.S. policy and management. Ecol. Appl. 16, 2035–2054 (2006).Article 

    Google Scholar 
    4.Yemshanov, D. et al. Optimizing surveillance strategies for early detection of invasive alien species. Ecol. Econ. 162, 87–99 (2019).Article 

    Google Scholar 
    5.Hauser, C. E. & Mccarthy, M. A. Streamlining “search and destroy”: Cost-effective surveillance for invasive species management. Ecol. Lett. 12, 683–692 (2009).Article 

    Google Scholar 
    6.Gottwald, T. R., da Graça, J. V. & Bassanezi, R. B. Citrus Huanglongbing: The pathogen and its impact. Plant Health Prog. https://doi.org/10.1094/PHP-2007-0906-01-RV (2007).Article 

    Google Scholar 
    7.Anderson, D. P. et al. Bio-economic optimisation of surveillance to confirm broadscale eradications of invasive pests and diseases. Biol. Invasions 19, 2869–2884 (2017).Article 

    Google Scholar 
    8.Russell, J. C., Binnie, H. R., Oh, J., Anderson, D. P. & Samaniego-Herrera, A. Optimizing confirmation of invasive species eradication with rapid eradication assessment. J. Appl. Ecol. 54, 160–169 (2017).Article 

    Google Scholar 
    9.Moffitt, L. J., Stranlund, J. K. & Osteen, C. D. Robust detection protocols for uncertain introductions of invasive species. J. Environ. Manag. 89, 293–299 (2008).Article 

    Google Scholar 
    10.Knight, F. H. Risk, Uncertainty, and Profit (Houghton Mifflin Company, 1921).11.Ben-Haim, Y. Uncertainty, probability and information-gaps. Reliab. Eng. Syst. Saf. 85, 249–266 (2004).Article 

    Google Scholar 
    12.Johnson, D. R. & Geldner, N. B. Contemporary decision methods for agricultural, environmental, and resource management and policy. Annu. Rev. Resour. Econ. 11, 19–41 (2019).Article 

    Google Scholar 
    13.Baker, C. M. & Bode, M. Recent advances of quantitative modeling to support invasive species eradication on islands. Conserv. Sci. Pract. 3, e246. https://doi.org/10.1111/csp2.246 (2021).Article 

    Google Scholar 
    14.Bertsimas, D. & Sim, M. The price of robustness. Oper. Res. 52, 35–53 (2004).MathSciNet 
    Article 

    Google Scholar 
    15.Ben-Haim, Y. & Demertzis, M. Decision making in times of knightian uncertainty: An info-gap perspective. Economics 10, 1–29 (2016).Article 

    Google Scholar 
    16.Ben-Haim, Y. Management of invasive species: Info-gap perspectives. in Invasive Species: Risk Assessment and Management (eds. Robinson, A., Walshe, T., Burgman, M. A., Nunn, M.) 266–286 (Cambridge University Press, 2017).17.Davidovitch, L. et al. Info-gap theory and robust design of surveillance for invasive species: The case study of Barrow Island. J. Environ. Manag. 90, 2785–2793 (2009).Article 

    Google Scholar 
    18.Rout, T. M., Thompson, C. J. & McCarthy, M. A. Robust decisions for declaring eradication of invasive species. J. Appl. Ecol. 46, 782–786 (2009).Article 

    Google Scholar 
    19.Foxcroft, L. C. Developing thresholds of potential concern for invasive alien species: Hypotheses and concepts. Koedoe. https://doi.org/10.4102/koedoe.v51i1.157 (2009).Article 

    Google Scholar 
    20.Pitt, J. P. W. Modelling the Spread of Invasive Species Across Heterogeneous Landscapes. (Lincoln University, 2008).21.Mehta, S. V., Haight, R. G., Homans, F. R., Polasky, S. & Venette, R. C. Optimal detection and control strategies for invasive species management. Ecol. Econ. 61, 237–245 (2007).Article 

    Google Scholar 
    22.Mcdonald-madden, E., Peter, W. J. B. & Possingham, H. P. Making robust decisions for conservation with restricted money and knowledge. J. Appl. Ecol. 45, 1630–1638 (2008).Article 

    Google Scholar 
    23.Rout, T. M., Moore, J. L. & Mccarthy, M. A. Prevent, search or destroy? A partially observable model for invasive species management. J. Appl. Ecol. 51, 804–813 (2014).Article 

    Google Scholar 
    24.Yemshanov, D. et al. Robust surveillance and control of invasive species using a scenario optimization approach. Ecol. Econ. 133, 86–98 (2017).Article 

    Google Scholar 
    25.Rödder, D., Solé, M. & Böhme, W. Predicting the potential distributions of two alien invasive Housegeckos (Gekkonidae: Hemidactylus frenatus, Hemidactylus mabouia). North-West. J. Zool. 4, 236–246 (2008).
    Google Scholar 
    26.Hoskin, C. J. The invasion and potential impact of the Asian House Gecko (Hemidactylus frenatus) in Australia. Austral. Ecol. 36, 240–251 (2011).Article 

    Google Scholar 
    27.García-Díaz, P., Ross, J. V., Vall-llosera, M. & Cassey, P. Low detectability of alien reptiles can lead to biosecurity management failure: A case study from Christmas Island (Australia). NeoBiota 45, 75–92 (2019).Article 

    Google Scholar 
    28.Scott, J. K. et al. Zero-tolerance biosecurity protects high-conservation-value island nature reserve. Sci. Rep. 7, 772–779 (2017).ADS 
    Article 

    Google Scholar 
    29.Commonwealth Government of Australia. Approval—Gorgon Gas Development (EPBC Reference: 2008/4178). (2009).30.Jarrad, F. C. et al. Improved design method for biosecurity surveillance and early detection of non-indigenous rats. N. Z. J. Ecol. 35, 132–144 (2011).
    Google Scholar 
    31.Metlay, D. From tin roof to torn wet blanket: Predicting and observing ground water movement at a proposed nuclear waste site. in Prediction: Science, Decision Making, and the Future of Nature (eds. Sarewitz, D. R., Byerly, R., Pielke, R. A.). 276–319. (Island Press, 2000).32.Wintle, B. & Burgman, M. Expert Elicitation for Barrow Island Surveillance System Revision, Project Report. (2015).33.Vanderduys, E. & Kutt, A. Is the Asian house gecko, Hemidactylus frenatus, really a threat to Australia’s biodiversity?. Aust. J. Zool. 60, 361–367 (2013).Article 

    Google Scholar 
    34.McGinnis, S. M. & Stebbins, R. C. A Field Guide to Western Reptiles and Amphibians. 4th edn. (Houghton Mifflin Harcourt, 2018).35.Whittle, P., Jarrad, F., Edwards, K. & Mengersen, K. Design of the quarantine surveillance for non-indigenous species of invertebrates on Barrow Island. Rec. West. Aust. Mus. Suppl. 83, 113–130 (2013).Article 

    Google Scholar 
    36.Ben-Haim, Y. Info-gap Decision Theory: Decisions Under Severe Uncertainty. 2nd edn. (Academic Press, 2006).37.MathWorks. MATLAB R2018b. (MathWorks, 2018).38.Bogich, T. L., Liebhold, A. M. & Shea, K. To sample or eradicate? A cost minimization model for monitoring and managing an invasive species. J. Appl. Ecol. 45, 1134–1142 (2008).Article 

    Google Scholar 
    39.Epanchin-Niell, R. S., Haight, R. G., Berec, L., Kean, J. M. & Liebhold, A. M. Optimal surveillance and eradication of invasive species in heterogeneous landscapes. Ecol. Lett. 15, 803–812 (2012).Article 

    Google Scholar 
    40.Trebitz, A. S. et al. Early detection monitoring for aquatic non-indigenous species: Optimizing surveillance, incorporating advanced technologies, and identifying research needs. J. Environ. Manag. 202, 299–310 (2017).CAS 
    Article 

    Google Scholar 
    41.Molina, R., Horton, T., Trappe, J. & Marcot, B. Addressing uncertainty: How to conserve and manage rare or little-known fungi. Fungal Ecol. 4, 134–146 (2011).Article 

    Google Scholar  More

  • in

    Pleistocene allopatric differentiation followed by recent range expansion explains the distribution and molecular diversity of two congeneric crustacean species in the Palaearctic

    1.Paillard, D. The timing of Pleistocene glaciations from a simple multiple-state climate model. Nature 391, 378–381 (1998).ADS 

    Google Scholar 
    2.Hewitt, G. M. Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359, 183–195 (2004).CAS 

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

    Google Scholar 
    4.Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. & Cosson, J.-F. Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7, 453–464 (1998).CAS 
    PubMed 

    Google Scholar 
    5.Incagnone, G., Marrone, F., Barone, R., Robba, L. & Naselli-Flores, L. How do freshwater organisms cross the ‘dry ocean’? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750, 103–123 (2015).
    Google Scholar 
    6.Schmitt, T. & Varga, Z. Extra-Mediterranean refugia: The rule and not the exception?. Front Zool 9, 22 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    7.Hewitt, G. M. Speciation, hybrid zones and phylogeography—Or seeing genes in space and time. Mol. Ecol. 10, 537–549 (2001).CAS 
    PubMed 

    Google Scholar 
    8.Habel, J. C., Drees, C., Schmitt, T. & Assmann, T. Review refugial areas and postglacial colonizations in the Western Palearctic. In Relict Species (eds Habel, J. C. & Assmann, T.) 189–197 (Springer, 2010).
    Google Scholar 
    9.Hewitt, G. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Lin. Soc. 58, 247–276 (1996).
    Google Scholar 
    10.Marrone, F., Lo Brutto, S. & Arculeo, M. Molecular evidence for the presence of cryptic evolutionary lineages in the freshwater copepod genus Hemidiaptomus G.O. Sars, 1903 (Calanoida, Diaptomidae). Hydrobiologia 644, 115–125 (2010).CAS 

    Google Scholar 
    11.Husemann, M., Schmitt, T., Zachos, F. E., Ulrich, W. & Habel, J. C. Palaearctic biogeography revisited: Evidence for the existence of a North African refugium for Western Palaearctic biota. J. Biogeogr. 41, 81–94 (2014).
    Google Scholar 
    12.García-Vázquez, D., Bilton, D. T., Foster, G. N. & Ribera, I. Pleistocene range shifts, refugia and the origin of widespread species in western Palaearctic water beetles. Mol. Phylogenet. Evol. 114, 122–136 (2017).PubMed 

    Google Scholar 
    13.Perktas, U., Barrowclough, G. F. & Groth, J. G. Phylogeography and species limits in the green woodpecker complex (Aves: Picidae): Multiple Pleistocene refugia and range expansion across Europe and the Near East. Biol. J. Lin. Soc. 104, 710–723 (2011).
    Google Scholar 
    14.Stewart, J. R. & Lister, A. M. Cryptic northern refugia and the origins of the modern biota. Trends Ecol. Evol. 16, 608–613 (2001).
    Google Scholar 
    15.Stewart, J. R., Lister, A. M., Barnes, I. & Dalén, L. Refugia revisited: Individualistic responses of species in space and time. Proc. R. Soc. B Biol. Sci. 277, 661–671 (2010).
    Google Scholar 
    16.Sworobowicz, L., Mamos, T., Grabowski, M. & Wysocka, A. Lasting through the ice age: The role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean. Freshw. Biol. 65, 1028–1046 (2020).CAS 

    Google Scholar 
    17.Provan, J. & Bennett, K. D. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564–571 (2008).PubMed 

    Google Scholar 
    18.Antal, L. et al. Phylogenetic evidence for a new species of Barbus in the Danube River basin. Mol. Phylogenet. Evol. 96, 187–194 (2016).CAS 
    PubMed 

    Google Scholar 
    19.Copilaş-Ciocianu, D., Fišer, C., Borza, P. & Petrusek, A. Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus. Mol. Phylogenet. Evol. 119, 37–49 (2018).PubMed 

    Google Scholar 
    20.Říčanová, Š et al. Multilocus phylogeography of the European ground squirrel: Cryptic interglacial refugia of continental climate in Europe. Mol. Ecol. 22, 4256–4269 (2013).PubMed 

    Google Scholar 
    21.Vörös, J., Mikulíček, P., Major, Á., Recuero, E. & Arntzen, J. W. Phylogeographic analysis reveals northerly refugia for the riverine amphibian Triturus dobrogicus (Caudata: Salamandridae). Biol. J. Linn. Soc. 119, 974–991 (2016).
    Google Scholar 
    22.Wielstra, B. et al. Tracing glacial refugia of Triturus newts based on mitochondrial DNA phylogeography and species distribution modeling. Front. Zool. 10, 13 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    23.Hutchison, D. W. & Templeton, A. R. Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53, 1898–1914 (1999).PubMed 

    Google Scholar 
    24.Schmitt, T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Front. Zool. 4, 11 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    25.Ewart, K. M. et al. Phylogeography of the iconic Australian red-tailed black-cockatoo (Calyptorhynchus banksii) and implications for its conservation. Heredity 125, 85–100 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    26.Hutama, A. et al. Identifying spatially concordant evolutionary significant units across multiple species through DNA barcodes: Application to the conservation genetics of the freshwater fishes of Java and Bali. Glob. Ecol. Conserv. 12, 170–187 (2017).
    Google Scholar 
    27.Médail, F. & Baumel, A. Using phylogeography to define conservation priorities: The case of narrow endemic plants in the Mediterranean Basin hotspot. Biol. Cons. 224, 258–266 (2018).
    Google Scholar 
    28.Previšić, A., Walton, C., Kučinić, M., Mitrikeski, P. T. & Kerovec, M. Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol. Ecol. 18, 634–647 (2009).PubMed 

    Google Scholar 
    29.Brendonck, L. & Riddoch, B. J. Wind-borne short-range egg dispersal in anostracans (Crustacea: Branchiopoda). Biol. J. Linn. Soc. 67, 87–95 (1999).
    Google Scholar 
    30.Horváth, Z., Vad, C. F. & Ptacnik, R. Wind dispersal results in a gradient of dispersal limitation and environmental match among discrete aquatic habitats. Ecography 39, 726–732 (2016).PubMed 

    Google Scholar 
    31.Brochet, A. L. et al. Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia 637, 255 (2009).
    Google Scholar 
    32.Figuerola, J. & Green, A. J. Dispersal of aquatic organisms by waterbirds: A review of past research and priorities for future studies. Freshw. Biol. 47, 483–494 (2002).
    Google Scholar 
    33.Vanschoenwinkel, B. et al. Dispersal of freshwater invertebrates by large terrestrial mammals: A case study with wild boar (Sus scrofa) in Mediterranean wetlands. Freshw. Biol. 53, 2264–2273 (2008).
    Google Scholar 
    34.Brendonck, L., Rogers, D. C., Olesen, J., Weeks, S. & Hoeh, W. R. Global diversity of large branchiopods (Crustacea : Branchiopoda) in freshwater. Hydrobiologia 595, 167–176 (2008).
    Google Scholar 
    35.Dumont, H. J. & Negrea, S. V. Introduction to the Class Branchiopoda. (Backhuys Publishers, 2002).36.Belk, D. Global status and trends in ephemeral pool invertebrate conservation: Implications for Californian fairy shrimp. In Ecology, Conservation, and Management of Vernal Pool Ecosystems—Proceedings from a 1996 conference 147–150 (California Native Plant Society, 1998).37.Jocque, M., Vanschoenwinkel, B. & Brendonck, L. Anostracan monopolisation of early successional phases in temporary waters?. Fundam. Appl. Limnol. 176, 127–132 (2010).
    Google Scholar 
    38.Lukić, D., Horváth, Z., Vad, C. F. & Ptacnik, R. Food spectrum of Branchinecta orientalis—Are anostracans omnivorous top consumers of plankton in temporary waters?. J. Plankton Res. 40, 436–445 (2018).
    Google Scholar 
    39.Lukić, D., Ptacnik, R., Vad, C. F., Pόda, C. & Horváth, Z. Environmental constraint of intraguild predation: Inorganic turbidity modulates omnivory in fairy shrimps. Freshw. Biol. 65, 226–239 (2020).
    Google Scholar 
    40.Waterkeyn, A., Grillas, P., Anton-Pardo, M., Vanschoenwinkel, B. & Brendonck, L. Can large branchiopods shape microcrustacean communities in Mediterranean temporary wetlands?. Mar. Freshw. Res. 62, 46–53 (2011).CAS 

    Google Scholar 
    41.Brendonck, L. & De Meester, L. Egg banks in freshwater zooplankton: Evolutionary and ecological archives in the sediment. Hydrobiologia 491, 65–84 (2003).
    Google Scholar 
    42.Hairston, N. G., Brunt, R. A. V., Kearns, C. M. & Engstrom, D. R. Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76, 1706–1711 (1995).
    Google Scholar 
    43.Lukić, D. et al. High genetic variation and phylogeographic relations among Palearctic fairy shrimp populations reflect persistence in multiple southern refugia during Pleistocene ice ages and postglacial colonisation. Freshw. Biol. 64, 1896–1907 (2019).
    Google Scholar 
    44.Marrone, F., Alfonso, G., Naselli-Flores, L. & Stoch, F. Diversity patterns and biogeography of Diaptomidae (Copepoda, Calanoida) in the Western Palearctic. Hydrobiologia 800, 45–60 (2017).CAS 

    Google Scholar 
    45.Vanschoenwinkel, B. et al. Toward a global phylogeny of the “living fossil’’ crustacean order of the Notostraca. PLos ONE 7, e34998 (2012).46.Boileau, M. & Hebert, P. Genetic consequences of passive dispersal in pond-dwelling Copepods. Evolution 45, 721–733 (1991).PubMed 

    Google Scholar 
    47.Deng, Z., Chen, Y., Ma, X., Hu, W. & Yin, M. Dancing on the top: Phylogeography and genetic diversity of high-altitude freshwater fairy shrimps (Branchiopoda, Anostraca) with a focus on the Tibetan Plateau. Hydrobiologia 848, 2611–2626 (2021).CAS 

    Google Scholar 
    48.Ketmaier, V. et al. Mitochondrial DNA regionalism and historical demography in the extant populations of Chirocephalus kerkyrensis (Branchiopoda: Anostraca). PLoS ONE 7, e30082 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    49.Korn, M. et al. Phylogeny, molecular ecology and taxonomy of southern Iberian lineages of Triops mauritanicus (Crustacea: Notostraca). Org. Divers. Evol. 10, 409–440 (2010).
    Google Scholar 
    50.Stoch, F., Korn, M., Turki, S., Naselli-Flores, L. & Marrone, F. The role of spatial environmental factors as determinants of large branchiopod distribution in Tunisian temporary ponds. Hydrobiologia 782, 37–51 (2016).
    Google Scholar 
    51.Lindholm, M., d’Auriac, M. A., Thaulow, J. & Hobaek, A. Dancing around the pole: Holarctic phylogeography of the Arctic fairy shrimp Branchinecta paludosa (Anostraca, Branchiopoda). Hydrobiologia 772, 189–205 (2016).CAS 

    Google Scholar 
    52.Vörös, J., Alcobendas, M., Martínez-Solano, I. & García-París, M. Evolution of Bombina bombina and Bombina variegata (Anura: Discoglossidae) in the Carpathian Basin: A history of repeated mt-DNA introgression across species. Mol. Phylogenet. Evol. 38, 705–718 (2006).PubMed 

    Google Scholar 
    53.Zharov, A. A. et al. Pleistocene branchiopods (Cladocera, Anostraca) from Transbaikalian Siberia demonstrate morphological and ecological stasis. Water 12, 3063 (2020).
    Google Scholar 
    54.Velonà, A., Luchetti, A., Scanabissi, F. & Mantovani, B. Genetic variability and reproductive modalities in European populations of Triops cancriformis (Crustacea, Branchiopoda, Notostraca). Ital. J. Zool. 76, 366–375 (2009).
    Google Scholar 
    55.Vanschoenwinkel, B., Gielen, S., Vandewaerde, H., Seaman, M. & Brendonck, L. Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography 31, 567–577 (2008).
    Google Scholar 
    56.Hulsmans, A., Moreau, K., Meester, L. D., Riddoch, B. J. & Brendonck, L. Direct and indirect measures of dispersal in the fairy shrimp Branchipodopsis wolfi indicate a small scale isolation-by-distance pattern. Limnol. Oceanogr. 52, 676–684 (2007).ADS 

    Google Scholar 
    57.Vanschoenwinkel, B., Vries, C. D., Seaman, M. & Brendonck, L. The role of metacommunity processes in shaping invertebrate rock pool communities along a dispersal gradient. Oikos 116, 1255–1266 (2007).
    Google Scholar 
    58.Sánchez, M. I., Green, A. J., Amat, F. & Castellanos, E. M. Transport of brine shrimps via the digestive system of migratory waders: Dispersal probabilities depend on diet and season. Mar. Biol. 151, 1407–1415 (2007).
    Google Scholar 
    59.Horváth, Z. et al. Eastern spread of the invasive Artemia franciscana in the Mediterranean Basin, with the first record from the Balkan Peninsula. Hydrobiologia 822, 229–235 (2018).
    Google Scholar 
    60.Muñoz, J., Amat, F., Green, A. J., Figuerola, J. & Gómez, A. Bird migratory flyways influence the phylogeography of the invasive brine shrimp Artemia franciscana in its native American range. PeerJ 1, e200 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    61.Muñoz, J. et al. Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca). Mol. Ecol. 17, 3160–3177 (2008).PubMed 

    Google Scholar 
    62.Sánchez, M. I., Hortas, F., Figuerola, J. & Green, A. J. Comparing the potential for dispersal via waterbirds of a native and an invasive brine shrimp. Freshw. Biol. 57, 1896–1903 (2012).
    Google Scholar 
    63.Viana, D. S., Santamaría, L., Michot, T. C. & Figuerola, J. Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms. Ecography 36, 430–438 (2013).
    Google Scholar 
    64.Green, A. J. et al. Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnol. Oceanogr. 50, 737–742 (2005).ADS 

    Google Scholar 
    65.Kappas, I. et al. Molecular and morphological data suggest weak phylogeographic structure in the fairy shrimp Streptocephalus torvicornis (Branchiopoda, Anostraca). Hydrobiologia 801, 21–32 (2017).CAS 

    Google Scholar 
    66.Rogers, D. C. Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). J. Crustac. Biol. 34, 135–143 (2014).
    Google Scholar 
    67.Angeler, D. G., Viedma, O., Sánchez-Carrillo, S. & Alvarez-Cobelas, M. Conservation issues of temporary wetland Branchiopoda (Anostraca, Notostraca: Crustacea) in a semiarid agricultural landscape: What spatial scales are relevant?. Biol. Cons. 141, 1224–1234 (2008).
    Google Scholar 
    68.Horváth, Z., Vad, C. F., Vörös, L. & Boros, E. Distribution and conservation status of fairy shrimps (Crustacea: Anostraca) in the astatic soda pans of the Carpathian basin: the role of local and spatial factors. J. Limnol. 72, 103–116 (2013).
    Google Scholar 
    69.Svensson, L., Mullarney, K. & Zetterström, D. Collins Bird Guide 2nd edn. (HarperCollins Publishers Ltd., 2009).
    Google Scholar 
    70.Horváth, Z., Vad, C. F., Vörös, L. & Boros, E. The keystone role of anostracans and copepods in European soda pans during the spring migration of waterbirds. Freshw. Biol. 58, 430–440 (2013).
    Google Scholar 
    71.Gill, J. L. Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytol. 201, 1163–1169 (2014).PubMed 

    Google Scholar 
    72.Neretina, A. N. et al. Crustacean remains from the Yuka mammoth raise questions about non-analogue freshwater communities in the Beringian region during the Pleistocene. Sci. Rep. 10, 859 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    73.Chang, D. et al. The evolutionary and phylogeographic history of woolly mammoths: A comprehensive mitogenomic analysis. Sci. Rep. 7, 44585 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    74.Lister, A. M., Sher, A. V., van Essen, H. & Wei, G. The pattern and process of mammoth evolution in Eurasia. Quatern. Int. 126–128, 49–64 (2005).
    Google Scholar 
    75.Vanschoenwinkel, B. et al. Passive external transport of freshwater invertebrates by elephant and other mud-wallowing mammals in an African savannah habitat. Freshw. Biol. 56, 1606–1619 (2011).
    Google Scholar 
    76.Waterkeyn, A., Pineau, O., Grillas, P. & Brendonck, L. Invertebrate dispersal by aquatic mammals: A case study with nutria Myocastor coypus (Rodentia, Mammalia) in Southern France. Hydrobiologia 654, 267–271 (2010).
    Google Scholar 
    77.Belk, D. & Brtek, J. Checklist of the Anostraca. Hydrobiologia 298, 315–353 (1995).
    Google Scholar 
    78.Marrone, F., Korn, M., Stoch, F., Naselli Flores, L. & Turki, S. Updated checklist and distribution of large branchiopods (Branchiopoda: Anostraca, Notostraca, Spinicaudata) in Tunisia. Biogeogr. J. Integr. Biogeogr. 31, 27–53 (2016).79.Mura, G. & Brtek, J. Revised key to families and genera of the Anostraca with notes on their geographical distribution. Crustaceana 73, 1037–1088 (2000).
    Google Scholar 
    80.Atashbar, B., Agh, N., Van Stappen, G., Mertens, J. & Beladjal, L. Combined effect of temperature and salinity on hatching characteristics of three fairy shrimp species (Crustacea: Anostraca). J. Limnol. 73, 574–583 (2014).
    Google Scholar 
    81.Eder, E., Hödl, W. & Gottwald, R. Distribution and phenology of large branchiopods in Austria. Hydrobiologia 359, 13–22 (1997).
    Google Scholar 
    82.Šćiban, M., Marković, A., Lukić, D. & Miličić, D. Autumn populations of Branchinecta orientalis G. O. Sars, 1903 and Chirocephalus diaphanus Prevost, 1803 (Crustacea, Branchiopoda) in the Central European Lowlands (Pannonian Plain, Serbia). North-West. J. Zool. 10, 435–437 (2014).
    Google Scholar 
    83.Alonso, M. A survey of the Spanish Euphyllopoda. Miscelania Zool. 9, 179–208 (1985).
    Google Scholar 
    84.Petkovski, S. On the presence of the genus Branchinecta Verrill, 1869 (Crustacea, Anostraca) in Yugoslavia. Hydrobiologia 226, 17–27 (1991).
    Google Scholar 
    85.Dimentman, C. The rainpool ecosystems of Israel: Geographical distribution of freshwater Anostraca (Crustacea). Israel J. Ecol. Evol. 30, 1–15 (1981).
    Google Scholar 
    86.Eid, E. K. New records of large branchiopods from northern Jordan (Crustacea: Branchiopoda). Zool. Middle East 46, 116–117 (2009).
    Google Scholar 
    87.Mura, G., Ozkutuk, S. R., Aygen, C. & Cottarelli, V. New data on the taxonomy and distribution of anostracan fauna from Turkey. J. Biol. Res. 15, 17–23 (2011).
    Google Scholar 
    88.Rogers, D. C., Quinney, D. L., Weaver, J. & Olesen, J. A new giant species of predatory fairy shrimp from Idaho, USA (Branchiopoda: Anostraca). J. Crustac. Biol. 26, 1–12 (2006).
    Google Scholar 
    89.Rodríguez-Flores, P. C., Jiménez-Ruiz, Y., Forró, L., Vörös, J. & García-París, M. Non-congruent geographic patterns of genetic divergence across European species of Branchinecta (Anostraca: Branchinectidae). Hydrobiologia 801, 47–57 (2017).
    Google Scholar 
    90.Atashbar, B., Agh, N., Van Stappen, G. & Beladjal, L. Diversity and distribution patterns of large branchiopods (Crustacea: Branchiopoda) in temporary pools (Iran). J. Arid. Environ. 111, 27–34 (2014).ADS 

    Google Scholar 
    91.Belk, D. & Esparza, C. E. Anostraca of the Indian Subcontinent. Hydrobiologia 298, 287–293 (1995).
    Google Scholar 
    92.Brtek, J. & Thiéry, A. The geographic distribution of the European Branchiopods (Anostraca, Notostraca, Spinicaudata, Laevicaudata). Hydrobiologia 298, 263–280 (1995).
    Google Scholar 
    93.Horn, W. & Paul, M. Occurrence and distribution of the Eurasian Branchinecta orientalis (Anostraca) in Central Asia (Northwest Mongolia, Uvs Nuur Basin) and in other holarctic areas. Lauterbornia 49, 81–91 (2004).
    Google Scholar 
    94.Marrone, F., Alonso, M., Pieri, V., Augugliaro, C. & Stoch, F. The crustacean fauna of Bayan Onjuul area (Tov Province, Mongolia) (Crustacea: Branchiopoda, Copepoda, Ostracoda). North West. J. Zool. 11, 288–295 (2015).
    Google Scholar 
    95.Mura, G. & Takami, G. A. A contribution to the knowledge of the anostracan fauna of Iran. Hydrobiologia 441, 117–121 (2000).
    Google Scholar 
    96.Naganawa, H. et al. Does the dispersal of fairy shrimps (Branchiopoda, Anostraca) reflect the shifting geographical distribution of freshwaters since the late Mesozoic?. Limnology https://doi.org/10.1007/s10201-019-00589-9 (2019).Article 

    Google Scholar 
    97.Padhye, S. M., Kulkarni, M. R. & Dumont, H. J. Diversity and zoogeography of the fairy shrimps (Branchiopoda: Anostraca) on the Indian subcontinent. Hydrobiologia 801, 117–128 (2017).
    Google Scholar 
    98.Petkovski, S. Taksonomsko-morfološka i zoogeografsko-ekološka studija Anostraca (Crustacea: Branchiopoda) jugoslovenskih zemalja. (Prirodno-matematički fakultet, Novi Sad, 1993).99.Pretus, J. L. A commented check-list of the Balearic Branchiopoda (Crustacea). Limnetica 6, 157–164 (1990).
    Google Scholar 
    100.van den Broeck, M., Waterkeyn, A., Rhazi, L. & Brendonck, L. Distribution, coexistence, and decline of Moroccan large branchiopods. J. Crustacean Biol. 35, 355–365 (2015).
    Google Scholar 
    101.Hijmans, R. J., Philips, S., Leathwick, J. & Elith, J. Package ‘dismo’. 9, 1–68 (2017).102.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. (2014).103.Hijmans, R. J., Cameron, S. E. & Parra, J. L. Climate Date from Worldclim (2004).104.Alfonso, G. & Marrone, F. Branchiopoda Anostraca, Notostraca, Spinicaudata. In Checklist of the Italian fauna (in press).105.Defaye, D., Rabet, N. & Thiéry, A. Atlas et bibliographie des crustaces branchiopodes (Anostraca, Notostraca, Spinicaudata) de France metropolitaine. Collection patrimoines naturels (1998).106.Song, H., Buhay, J. E., Whiting, M. F. & Crandall, K. A. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. PNAS 105, 13486–13491 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    107.Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98 (1999).CAS 

    Google Scholar 
    108.Aguilar, A. et al. High intraspecific genetic divergence in the versatile fairy shrimp Branchinecta lindahli with a comment on cryptic species in the genus Branchinecta (Crustacea: Anostraca). Hydrobiologia 801, 59–69 (2017).
    Google Scholar 
    109.Jeffery, N. W., Elías-Gutiérrez, M. & Adamowicz, S. J. Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. PLoS ONE 6, e18364 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    110.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2017).CAS 
    PubMed 

    Google Scholar 
    111.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    112.Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).113.Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).CAS 
    PubMed 

    Google Scholar 
    114.Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    115.Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).116.Bandelt, H. J., Forster, P. & Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48 (1999).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    117.Leigh, J. W. & Bryant, D. popart: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).
    Google Scholar 
    118.Xia, X. & Kumar, S. DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Mol. Biol. Evol. 35, 1550–1552 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    119.Xia, X. & Lemey, P. Assessing substitution saturation with DAMBE. In The phylogenetic Handbook 615–630 (Cambridge University Press, 2009).120.Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26, 1–7 (2003).CAS 
    PubMed 

    Google Scholar 
    121.Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).ADS 
    CAS 
    PubMed 

    Google Scholar 
    122.Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302 (2017).CAS 

    Google Scholar 
    123.Nychka, D. et al. fields: Tools for Spatial Data (2020).124.Oksanen, J. et al. vegan: Community ecology package. – R package ver. 2.0-4. http://CRAN.R-project.org/package=vegan. (2012). More

  • in

    Reconciling biome-wide conservation of an apex carnivore with land-use economics in the increasingly threatened Pantanal wetlands

    1.Inskip, C. & Zimmermann, A. Human-felid conflict: a review of patterns and priorities worldwide. Oryx 43(1), 18–34 (2009).
    Google Scholar 
    2.Weber, W. & Rabinowitz, A. A global perspective on large carnivore conservation. Conserv. Biol. 10(4), 1046–1054 (1996).
    Google Scholar 
    3.Treves, A. & Karanth, U. K. Human-carnivore conflict and perspectives on carnivore management worldwide. Conserv. Biol. 17(6), 1491–1499 (2003).
    Google Scholar 
    4.Romero-Muñoz, A., Morato, R., Tortato, F. & Kuemmerle, T. Beyond fangs: beef and soybean trade drive jaguar extinction. Front. Ecol. Environ. 18(2), 67–68 (2020).
    Google Scholar 
    5.Packer, C. et al. Conserving large carnivores: dollars and fence. Ecol. Lett. 16(5), 635–641 (2013).CAS 
    PubMed 

    Google Scholar 
    6.Margules, C. R. & Pressey, R. L. Systematic conservation planning. Nature 405, 243–253 (2000).CAS 
    PubMed 

    Google Scholar 
    7.Quigley, H., Foster, R., Petracca, L., Payan, E., Salom, R. & Harmsen, B. Panthera onca. The IUCN Red List of Threatened Species 2017, e.T15953A123791436 (2017).8.Menezes, J. F. S., Tortato, F. R., Oliveira-Santos, L. G., Roque, F. O. & Morato, R. G. Deforestation, fires, and lack of governance are displacing thousands of jaguars in Brazilian Amazon. Conserv. Sci. Pract. 3(8), e477 (2021).
    Google Scholar 
    9.Morato, R. G. et al. Resource selection in an apex predator and variation in response to local landscape characteristics. Biol. Conserv. 228, 233–240 (2018).
    Google Scholar 
    10.Sanderson, E. W. et al. Planning to save a species: the jaguar as a model. Conserv. Biol. 16(1), 1–15 (2002).
    Google Scholar 
    11.De Paula, R. C., Desbiez, A. & Cavalcanti, S. M. C. Plano de Ação Nacional para Conservação da Onça-pintada. Série Espécies Ameaçadas (Instituto Chico Mendes de Conservação da Biodiversidade, Atibaia, 2013).
    Google Scholar 
    12.Seidl, A. F., Silva, J. S. V. & Moraes, A. S. Cattle ranching and deforestation in the Brazilian Pantanal. Ecol. Econ. 36(3), 413–425 (2001).
    Google Scholar 
    13.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 
    14.Tortato, F. R. & Izzo, T. J. Advances and barriers to the development of jaguar-tourism in the Brazilian Pantanal. Perspect. Ecol. Conserv. 15(1), 61–63 (2017).
    Google Scholar 
    15.Tortato, F. R., Hoogesteijn, R. & Elbroch, M. Have natural disasters created opportunities to initiate Big Cat Tourism in South America?. Biotropica 52(3), 400–403 (2020).
    Google Scholar 
    16.Quigley, H. & Crawshaw, P. G. Jr. A conservation plan for the jaguar (Panthera onca) in the Pantanal region of Brazil. Biol. Conserv. 61(3), 149–157 (1992).
    Google Scholar 
    17.Tortato, F. R., Izzo, T. J., Hoogesteijn, R. & Peres, C. A. The numbers of the beast: valuation of jaguar (Panthera onca) tourism and cattle depredation in the Brazilian Pantanal. Glob. Ecol. Conserv. 11, 106–114 (2017).
    Google Scholar 
    18.Junk, W. J. et al. Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aqua Sci. 69, 278–309 (2006).
    Google Scholar 
    19.Guerra, A. et al. Drivers and projections of vegetation loss in the Pantanal and surrounding ecosystems. Land Use Policy 91, 104388 (2020).
    Google Scholar 
    20.Marengo, J. A. et al. Extreme drought in the Brazilian Pantanal in 2019–2020: characterization, causes, and impacts. Front. Water 3, 1–20 (2021).
    Google Scholar 
    21.Berlinck, C. N. et al. The Pantanal is on fire and only a sustainable agenda can save the largest wetland in the world. Brazilian Journal of Biology 82, e244200 (2021).CAS 

    Google Scholar 
    22.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 
    23.Libonati, R., Sander, L. A., Peres, L. F., DaCamara, C. C. & Garcia, L. C. Rescue Brazil’s burning Pantanal wetlands. Nature 588, 217–220 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    24.Hoogesteijn, A. & Hoogesteijn, R. Cattle ranching and biodiversity conservation as allies in South America’s flooded savannas. Great Plains Res. 20, 37–50 (2010).
    Google Scholar 
    25.Ferraz, K. M. P. M. B., Ferraz, S. F. B., De Paula, R. C., Beisiegel, B. & Breitenmoser, C. Species distribution modeling for conservation purposes. Natureza Conservação 10(2), 214–220 (2012).
    Google Scholar 
    26.Zimmermann, A., Walpole, M. J. & Leader-Williams, N. Cattle ranchers’ attitudes to conflicts with jaguar Panthera onca in the Pantanal of Brazil. Oryx 39(4), 406–412 (2005).
    Google Scholar 
    27.Marchini, S. & Macdonald, D. W. Predicting rancher’s intention to kill jaguars: case studies in Amazonia and Pantanal. Biol. Conserv. 147(1), 213–221 (2012).
    Google Scholar 
    28.Abreu, U. G. P., McManus, C. & Santos, A. S. Cattle ranching, conservation and transhumance in Brazilian Pantanal. Pastoralism 1(1), 99–114 (2010).
    Google Scholar 
    29.Alho, C. J. R. & Sabino, J. A conservation agenda for the Pantanal’s biodiversity. Braz. J. Biol. 71(1), 327–335 (2011).CAS 
    PubMed 

    Google Scholar 
    30.Hoogesteijn, R. et al. Conservación de Jaguares fuera de Áreas Protegidas: Turismo de Observación de Jaguares en Propiedades Privadas en El Pantanal. In Conservación de grandes vertebrados en áreas no protegidas de Colombia, Venezuela y Brasil (eds Payan-Garrido, E. et al.) 259–274 (Panthera. Fundación Herencia Ambiental Caribe e Instituto de Investigaciones de Recursos Biológicos Alexander von Humboldt, Cartagena, 2015).
    Google Scholar 
    31.Tyagi, A. et al. Physiological stress responses of tigers due to anthropogenic disturbance especially tourism in two central Indian tiger reserves. Conservation Physiology 7(1), coz045 (2020).
    Google Scholar 
    32.Hayward, M. W. & Hayward, G. J. The impact of tourists on lion Panthera leo behaviour, stress and energetics. Acta Theriol. 54(3), 219–224 (2009).
    Google Scholar 
    33.Romanach, S., Lindsey, P. A. & Woodroffe, R. Determinants of attitudes towards predators in central Kenya and suggestions for increasing tolerance in livestock dominated landscapes. Oryx 41(2), 185–195 (2007).
    Google Scholar 
    34.Hemson, G. S., Maclennan, S., Mills, G., Johnson, P. & Macdonald, D. Community, lions, livestock and money: a spatial and social analysis of attitudes to wildlife and the conservation value of tourism in a human–carnivore conflict in Botswana. Biol. Conserv. 142(11), 2718–2725 (2009).
    Google Scholar 
    35.Mossaz, A., Buckley, R. C. & Castley, J. G. Ecotourism contributions to conservation of African big cats. J. Nat. Conserv. 28, 112–118 (2015).
    Google Scholar 
    36.Macdonald, C. et al. Conservation potential of apex predator tourism. Biol. Conserv. 215, 132–141 (2017).
    Google Scholar 
    37.Campos, Z., Mourão, G. & Magnusson, W. Drought drastically reduces suitable habitat for Yacare caiman. Crocodile Specialist Group Newsl. 39(4), 14–16 (2020).
    Google Scholar 
    38.Marengo, J. A., Oliveira, G. S. & Alves, L. M. Climate change scenarios in the Pantanal. In Dynamics of the Pantanal Wetland in South America (eds Bergier, I. & Assine, M. L.) 227–238 (Springer International Publishing, Heidelberg, 2016).
    Google Scholar 
    39.Thielen, D. et al. Quo vadis Pantanal? Expected precipitation extremes and drought dynamics from changing sea surface temperature. PLOS ONE 15(1), e0227437 (2020).CAS 
    PubMed 
    PubMed Central 

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

    Google Scholar 
    41.Araujo, A. et al. Relationships between variability in precipitation, river levels, and beef cattle production in the Brazilian Pantanal. Wetl. Ecol. Manage. 26(5), 829–848 (2018).
    Google Scholar 
    42.Filho, W. L., Azeiteira, U. M., Salvia, A. L., Fritzen, B. & Libonati, R. Fire in Paradise: why the Pantanal is burning. Environ. Sci. Policy 123, 31–34 (2021).
    Google Scholar 
    43.Brown, J. L. SDM toolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol. Evol. 5(7), 694–700 (2014).
    Google Scholar 
    44.Morato, R. G. et al. Space use and movement of a Neotropical top predator: the endangered jaguar. PLOS ONE 11(12), e0168176 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    45.Fick, S. E. & Hijmans, R. J. Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12), 4302–4315 (2017).
    Google Scholar 
    46.Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190(3–4), 231–259 (2006).
    Google Scholar 
    47.Phillips, S. J. & Dudik, M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31(2), 161–175 (2008).
    Google Scholar 
    48.Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E. & Blair, M. E. Opening the black box: an open-source release of Maxent. Ecography 40(7), 887–893 (2017).
    Google Scholar 
    49.Pinto, M. M., Libonati, R., Trigo, R. M., Trigo, I. F. & DaCamara, C. C. A deep learning approach for mapping and dating burned areas using temporal sequences of satellite images. ISPRS J. Photogramm. Remote. Sens. 160, 260–274 (2020).ADS 

    Google Scholar 
    50.LASA – Laboratório de Aplicações de Satélites Ambientais. ALARMES – LASA. https://lasa.ufrj.br/alarmes/ (2021).51.Wickham, H. tidyverse: Easily Install and Load the ‘Tidyverse’. R package version 1.2.1. https://CRAN.R-project.org/package=tidyverse (2017).52.Bray, A. et al. infer: Tidy Statistical Inference. R package version 0.5.4. https://cran.r-project.org/web/packages/infer/index.html (2021).53.Vallejos, R., Osorio, F. & Bevilacqua, M. Spatial Relationships Between Two Georeferenced Variables: with Applications in R (Springer, Berlin, 2020).MATH 

    Google Scholar  More