More stories

  • in

    Integration of palaeo-and-modern food webs reveal slow changes in a river floodplain wetland ecosystem

    1.
    Herwig, B. R., Wahl, D. H., Dettmers, J. M. & Soluk, D. A. Spatial and temporal patterns in the food web structure of a large floodplain river assessed using stable isotopes. Can. J. Fish. Aquat. Sci. 64, 495–508. https://doi.org/10.1139/f07-023 (2007).
    CAS  Article  Google Scholar 
    2.
    Turner, B. L. I. et al. A framework for vulnerability analysis in sustainability science. Proc. Natl. Acad. Sci. USA 100, 8074–8079. https://doi.org/10.1073/pnas.1231335100 (2003).
    ADS  CAS  Article  PubMed  Google Scholar 

    3.
    Sayer, C. D., Davidson, T. A., Jones, J. I. & Langdon, P. G. Combining contemporary ecology and palaeolimnology to understand shallow lake ecosystem change. Freshw. Biol. 55, 487–499. https://doi.org/10.1111/j.1365-2427.2010.02388.x (2010).
    Article  Google Scholar 

    4.
    Randsalu-Wendrup, L. et al. Combining limnology and palaeolimnology to investigate recent regime shifts in a shallow, eutrophic lake. J. Paleolimnol. 51, 437–448. https://doi.org/10.1007/s10933-014-9767-5 (2014).
    ADS  Article  Google Scholar 

    5.
    Kattel, G. R., Dong, X. & Yang, X. A century-scale, human-induced ecohydrological evolution of wetlands of two large river basins in Australia (Murray) and China (Yangtze). Hydrol. Earth Syst. Sci. 20, 2151–2168. https://doi.org/10.5194/hess-20-2151-2016 (2016).
    ADS  Article  Google Scholar 

    6.
    Kingsford, R. T. & Thomas, R. F. Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia. Environ. Manage. 34, 383–396. https://doi.org/10.1007/s00267-004-0250-3 (2004).
    CAS  Article  PubMed  Google Scholar 

    7.
    Gell, P. A. & Reid, M. A. Muddied waters: The case for mitigating sediment and nutrient flux to optimize restoration response in the Murray-Darling Basin, Australia. Front. Ecol. Evolut. https://doi.org/10.3389/fevo.2016.00016 (2016).
    Article  Google Scholar 

    8.
    Davis, J. et al. When trends intersect: The challenge of protecting freshwater ecosystems under multiple land use and hydrological intensification scenarios. Sci. Total Environ. 534, 65–78. https://doi.org/10.1016/j.scitotenv.2015.03.127 (2015).
    ADS  CAS  Article  PubMed  Google Scholar 

    9.
    Davis, J. A. & Froend, R. Loss and degradation of wetlands in southwestern Australia: Underlying causes, consequences and solutions. Wetlands Ecol. Manage. 7, 13–23 (1999).
    Article  Google Scholar 

    10.
    Wright, I. A., Chessman, B. C., Eairweather, P. G. & Benson, L. J. Measuring the impact of sewage effluent on the macroinvertebrate community of an upland stream: The effect of different levels of taxonomic resolution and quantification. Aust. J. 20, 142–149 (1995).
    Google Scholar 

    11.
    Wright, I. A., Belmer, N. & Davies, P. J. Coal mine water pollution and ecological impairment of one of Australia’s most ‘protected’ high conservation-value rivers. Water Air Soil Pollut. https://doi.org/10.1007/s11270-017-3278-8 (2017).
    Article  Google Scholar 

    12.
    Forsberg, B. R., Melack, J. M., Richey, J. E. & Pimentel, T. P. Regional and seasonal variability in planktonic photosynthesis and planktonic community respiration in Amazon floodplain lakes. Hydrobiologia 800, 187–206. https://doi.org/10.1007/s10750-017-3222-3 (2017).
    CAS  Article  Google Scholar 

    13.
    Kennard, M. J., Arthington, A. H., Pusey, B. J. & Harch, B. D. Are alien fish a reliable indicator of river health?. Freshw. Biol. 50, 174–193. https://doi.org/10.1111/j.1365-2427.2004.01293.x (2005).
    Article  Google Scholar 

    14.
    Froend, R. H. & Mccomb, A. J. Distribution, productivity and reproductive phenology of emergent macrophytes in relation to water regimes at wetlands of South-western Australia. Aust. J. Mar. Freshwater Res. 45, 1491–1508 (1994).
    Article  Google Scholar 

    15.
    Koehn, J. Carp (Cyprinus carpio) as a powerful invader. Freshw. Biol. 49, 882–894 (2004).
    Article  Google Scholar 

    16.
    Hardy, C. M., Krull, E. S., Hartley, D. M. & Oliver, R. L. Carbon source accounting for fish using combined DNA and stable isotope analyses in a regulated lowland river weir pool. Mol. Ecol. 19, 197–212. https://doi.org/10.1111/j.1365-294X.2009.04411.x (2010).
    CAS  Article  PubMed  Google Scholar 

    17.
    Brett, M. T., Kainz, M. J., Taipale, S. J. & Seshan, H. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc. Natl. Acad. Sci. USA 106, 21197–21201. https://doi.org/10.1073/pnas.0904129106 (2009).
    ADS  Article  PubMed  Google Scholar 

    18.
    Mendonca, R. et al. Bimodality in stable isotope composition facilitates the tracing of carbon transfer from macrophytes to higher trophic levels. Hydrobiologia 710, 205–218. https://doi.org/10.1007/s10750-012-1366-8 (2013).
    CAS  Article  Google Scholar 

    19.
    Doody, T. M. et al. Quantifying water requirements of riparian river red gum (Eucalyptus camaldulensis) in the Murray-Darling Basin, Australia—Implications for the management of environmental flows. Ecohydrology 8, 1471–1487. https://doi.org/10.1002/eco.1598 (2015).
    Article  Google Scholar 

    20.
    Jenkins, K. M. & Boulton, A. J. Detecting impacts and setting restoration targets in arid-zone rivers: Aquatic micro-invertebrate responses to reduced floodplain inundation. J. Appl. Ecol. 44, 823–832. https://doi.org/10.1111/j.1365-2664.2007.01298.x (2007).
    Article  Google Scholar 

    21.
    Reid, M. A. & Ogden, R. W. Factors affecting diatom distribution in floodplain lakes of the southeast Murray Basin, Australia and implications for palaeolimnological studies. J. Paleolimnol. 41, 453–470. https://doi.org/10.1007/s10933-008-9236-0 (2008).
    Article  Google Scholar 

    22.
    Rawcliffe, R. et al. Back to the future: Using palaeolimnology to infer long-term changes in shallow lake food webs. Freshw. Biol. 55, 600–613. https://doi.org/10.1111/j.1365-2427.2009.02280.x (2010).
    Article  Google Scholar 

    23.
    Carpenter, S., Walker, B., Anderies, J. M. & Abel, N. From metaphor to measurement: Resilience of what to what?. Ecosystems 4, 765–781. https://doi.org/10.1007/s10021-001-0045-9 (2014).
    Article  Google Scholar 

    24.
    Randsalu-Wendrup, L., Conley, D. J., Carstensen, J. & Fritz, S. C. Paleolimnological records of regime shifts in lakes in response to climate change and anthropogenic activities. J. Paleolimnol. https://doi.org/10.1007/s10933-016-9884-4 (2016).
    Article  Google Scholar 

    25.
    Jones, J. I. & Waldron, S. Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshw. Biol. 48, 1396–1407 (2003).
    Article  Google Scholar 

    26.
    Vander Zanden, M. J., Clayton, M. K., Moody, E. K., Solomon, C. T. & Weidel, B. C. Stable isotope turnover and half-life in animal tissues: A literature synthesis. PLoS ONE 10, e0116182. https://doi.org/10.1371/journal.pone.0116182 (2015).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    27.
    Mao, Z., Gu, X., Zeng, Q., Zhou, L. & Sun, M. Food web structure of a shallow eutrophic lake (Lake Taihu, China) assessed by stable isotope analysis. Hydrobiologia 683, 173–183. https://doi.org/10.1007/s10750-011-0954-3 (2011).
    CAS  Article  Google Scholar 

    28.
    Burford, M. A., Cook, A. J., Fellows, C. S., Balcombe, S. R. & Bunn, S. E. Sources of carbon fuelling production in an arid floodplain river. Mar. Freshw. Res. 59, 224–234 (2008).
    CAS  Article  Google Scholar 

    29.
    Phillips, D. L. Converting isotope values to diet composition: The use of mixing models. J. Mammal. 93, 342–352. https://doi.org/10.1644/11-mamm-s-158.1 (2012).
    Article  Google Scholar 

    30.
    Ventura, M. et al. Effects of increased temperature and nutrient enrichment on the stoichiometry of primary producers and consumers in temperate shallow lakes. Freshw. Biol. 53, 1434–1452. https://doi.org/10.1111/j.1365-2427.2008.01975.x (2008).
    CAS  Article  Google Scholar 

    31.
    Torres, I. C., Inglett, P. W., Brenner, M., Kenney, W. F. & Reddy, K. R. Stable isotope (δ13C and δ15N) values of sediment organic matter in subtropical lakes of different trophic status. J. Paleolimnol. 47, 693–706. https://doi.org/10.1007/s10933-012-9593-6 (2012).
    ADS  Article  Google Scholar 

    32.
    Kattel, G. et al. Tracking a century of change in trophic structure and dynamics in a floodplain wetland: Integrating palaeoecological and palaeoisotopic evidence. Freshw. Biol. 60, 711–723. https://doi.org/10.1111/fwb.12521 (2015).
    CAS  Article  Google Scholar 

    33.
    Kattel, G., Gell, P., Zawadzki, A. & Barry, L. Palaeoecological evidence for sustained change in a shallow Murray River (Australia) floodplain lake: Regime shift or press response?. Hydrobiologia 787, 269–290. https://doi.org/10.1007/s10750-016-2970-9 (2016).
    CAS  Article  Google Scholar 

    34.
    Gippel, C. J. & Blackham, D. Review of environmental impacts of flow regulation and other water resource developments in the river murray and lower darling river system. Final report by Fluvial Systems Pty Ltd, Stockton, to Murray-Darling Basin Commission, Canberra, ACT (2002).

    35.
    Lloyd, L. N. Kings Billabong operating plan. Report to the Mallee CMA. Lloyd Environmental, Syndal, Victoria. Final Draft 22 March 2012 (2012).

    36.
    Battarbee, R. W. Palaeolimnological approaches to climate change, with special regard to the biological record. Quatern. Sci. Rev. 19, 107–124 (2004).
    ADS  Article  Google Scholar 

    37.
    Shiel, R. J. & Dickson, A. Cladocera recorded from Australia. T. Roy. Soc. South Aust. 119, 29–40 (1995).
    Google Scholar 

    38.
    Szeroczyńska, K. & Sarmaja-Korjonen, K. Atlas of subfossil Cladocera from Central and Northern Europe (Friends of the Lower Vistula Society, Poland, 2007).
    Google Scholar 

    39.
    Grimm, E. C. CONISS: A FORTRAN 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Comput. Geosci. 13, 13–35. https://doi.org/10.1016/0098-3004(87)90022-7 (1987).
    ADS  Article  Google Scholar 

    40.
    Schilder, J. et al. The stable isotopic composition of Daphnia ephippia reflects changes in δ13C and δ18O values of food and water. Biogeosciences 12, 3819–3830. https://doi.org/10.5194/bg-12-3819-2015 (2015).
    ADS  CAS  Article  Google Scholar 

    41.
    Morlock, M. A. et al. Seasonality of cladoceran and bryozoan resting stage δ13C values and implications for their use as palaeolimnological indicators of lacustrine carbon cycle dynamics. J. Paleolimnol. 57, 141–156. https://doi.org/10.1007/s10933-016-9936-9 (2016).
    Article  Google Scholar 

    42.
    Kattel, G. R., Battarbee, R. W., Mackay, A. W. & Birks, H. J. B. Recent ecological change in a remote Scottish mountain loch: An evaluation of a Cladocera-based temperature transfer-function. Palaeogeogr. Palaeoclimatol. Palaeoecol. 259, 51–76. https://doi.org/10.1016/j.palaeo.2007.03.052 (2008).
    Article  Google Scholar 

    43.
    Vandekerkhove, J. et al. Use of ephippial morphology to assess richness of anomopods: Potentials and pitfalls. J. Limnol. 63(Suppl), 75–80 (2004).
    Article  Google Scholar 

    44.
    Haines, E. B. & Montague, C. L. Food sources of estuarine invertebrates analyzed using 13C/12C ratios. Ecology 60, 48–56 (1979).
    Article  Google Scholar 

    45.
    Appleby, P. G. Chronostratigraphic Techniques in Recent Sediments 171–203 (Kluwer Academic Publishers, Dordrecht, 2001).
    Google Scholar 

    46.
    Blaauw, M. & Hegaard, E. Estimation of age-depth relationships. In Tracking Environmental Change Using Lake Sediments (eds Birks, H. J. B., Juggins, S., Lotter, A. & Smol, J. P.) 379–413 (Springer, Dordrecht, 2012).
    Google Scholar 

    47.
    Oakes, J. M., Rysgaard, S., Glud, R. N. & Eyre, B. D. The transformation and fate of sub-Arctic microphytobenthos carbon revealed through 13 C-labeling. Limnol. Oceanogr. 61, 2296–2308. https://doi.org/10.1002/lno.10377 (2016).
    ADS  CAS  Article  Google Scholar 

    48.
    Eyre, B. D., Oakes, J. M. & Middelburg, J. J. Fate of microphytobenthos nitrogen in subtropical subtidal sediments: A 15 N pulse-chase study. Limnol. Oceanogr. 61, 2108–2121. https://doi.org/10.1002/lno.10356 (2016).
    ADS  CAS  Article  Google Scholar 

    49.
    Le Clercq, M., van der Plicht, J. & Groning, M. In Proceedings of the 16th International 14C Conference, Radiocarbon. (eds W.G. Mook & J. van der Plicht) 295–297.

    50.
    Böhlke, J. K. & Coplen, T. B. Reference and Inter-Comparison Materials for Stable Isotopes of Light Elements. Proceedings of a Consultants Meeting Held in Vienna 1–3 December 1993 (IAEA, Vienna, 1995).
    Google Scholar 

    51.
    Phillips, D. L. & Gregg, J. W. Source partitioning using stable isotopes: Coping with too many sources. Oecologia 136, 261–269. https://doi.org/10.1007/s00442-003-1218-3 (2003).
    ADS  Article  PubMed  Google Scholar 

    52.
    Fry, B. Stable isotope diagrams of freshwater food webs. Ecology 72, 2293–2297 (1991).
    Article  Google Scholar 

    53.
    Fry, B. & Sherr, E. B. PC measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. Mar. Sci. 27, 13–47 (1984).
    CAS  Google Scholar 

    54.
    McCutchan, J. H., Lewis, W. M., Kendall, C. & McGrath, C. C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390 (2003).
    CAS  Article  Google Scholar 

    55.
    Minagawa, M., Winter, D. A. & Kaplan, I. R. Comparison of Kjeldahl and combustion methods for measurement of nitrogen isotope ratios in organic matter. Anal. Chem. 56, 1859–1861. https://doi.org/10.1021/ac00275a023 (2002).
    Article  Google Scholar 

    56.
    Roberts, J. & Kleinert, H. Managing Typha and Phragmites, Report for workshop held 16th June 2014, North Central Catchment Management Authority, Australia. (2015).

    57.
    CarpFactsheet. Pest Smart. https://pestsmart.org.au/pestsmart-factsheet-carp/ (2017).

    58.
    Minagawa, M., Winter, D. A. & Kaplan, I. R. Comparison of Kjeldahl and combustion methods for measurement of nitrogen isotope ratios in organic matter. Anal. Chem. 56(11), 1859–1861. https://doi.org/10.1021/ac00275a023 (1984).
    CAS  Article  Google Scholar 

    59.
    Powell, S. J., Letcher, R. A. & Croke, B. F. W. Modelling floodplain inundation for environmental flows: Gwydir wetlands, Australia. Ecol. Model. 211, 350–362. https://doi.org/10.1016/j.ecolmodel.2007.09.013 (2008).
    Article  Google Scholar 

    60.
    Chiew, F., Young, W. J. & Cai, W. Current drought and future hydroclimate projections in southeast Australia and implications for water resources management. Stoch. Environ. Res. Risk Assess. 25, 601–612. https://doi.org/10.1007/s00477-010-0424-x (2011).
    Article  Google Scholar 

    61.
    Powell, J. M. Watering the Garden State. (Allen & Unwin, 1989).

    62.
    Jeppesen, E., Leavitt, P. R., De Meester, L. & Jensen, J. P. Functional ecology and palaeolimnology: Using cladoceran remains to reconstruct anthropogenic impact. Trends Ecol. Evol. 16, 191–198 (2001).
    CAS  Article  Google Scholar 

    63.
    Dadswell, M. (Bureau of Immigration and Population Research, Canberra, 1980). http://www.dadswell.id.au/history/tree10/italian_essay.pdf.

    64.
    Scheffer, M. & Jeppesen, E. Regime shifts in shallow lakes. Ecosystems 10, 1–3. https://doi.org/10.1007/s10021-006-9002-y (2007).
    Article  Google Scholar 

    65.
    Meyers, P. A. & Teranes, J. L. Sediment organic matter. In Tracking Environmental Changes Using Lake Sediments, Physical and Chemical Techniques Vol. II (eds Last, W. M. & Smol, J. P.) 239–269 (Kluwer, 2001).

    66.
    Xu, D. et al. Variations of food web structure and energy availability of shallow lake with long-term eutrophication: A case study from Lake Taihu, China. Clean: Soil, Air, Water 44, 1306–1314. https://doi.org/10.1002/clen.201300837 (2016).
    CAS  Article  Google Scholar 

    67.
    Kong, X. et al. Changes in food web structure and ecosystem functioning of a large, shallow Chinese lake during the 1950s, 1980s and 2000s. Ecol. Model. 319, 31–41. https://doi.org/10.1016/j.ecolmodel.2015.06.045 (2016).
    CAS  Article  Google Scholar 

    68.
    Cole, J. J. et al. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proc. Natl. Acad. Sci. USA 108, 1975–1980. https://doi.org/10.1073/pnas.1012807108 (2011).
    ADS  Article  PubMed  Google Scholar 

    69.
    Rosenblatt, A. E. & Schmitz, O. J. Climate change, nutrition, and bottom-up and top-down food web processes. Trends Ecol. Evol. 31, 965–975. https://doi.org/10.1016/j.tree.2016.09.009 (2016).
    Article  PubMed  Google Scholar 

    70.
    Kosten, S. et al. Effects of submerged vegetation on water clarity across climates. Ecosystems 12, 1117–1129. https://doi.org/10.1007/s10021-009-9277-x (2009).
    Article  Google Scholar 

    71.
    Masson, S., Angeli, N., Guillard, J. & Pinel-Alloul, B. Diel vertical and horizontal distribution of crustacean zooplankton and young of the year fish in a sub-alpine lake: An approach based on high frequency sampling. J. Plankton Res. 23, 1041–1060 (2001).
    Article  Google Scholar 

    72.
    Burks, R. L., Lodge, D. M., Jeppesen, E. & Lauridsen, T. L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshw. Biol. 47, 343–365 (2002).
    Article  Google Scholar 

    73.
    Karlsson, J. et al. Light limitation of nutrient-poor lake ecosystems. Nature 460, 506–509. https://doi.org/10.1038/nature08179 (2009).
    ADS  CAS  Article  PubMed  Google Scholar 

    74.
    Cloern, J. E., Canuel, E. A. & Harris, D. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnol. Oceanogr. 47, 713–729 (2002).
    ADS  CAS  Article  Google Scholar 

    75.
    Robertson, A. I., Bunn, S. E., Boon, P. I. & Walker, K. F. Sources, sinks and transformations of organic carbon in Australian floodplain rivers. Mar. Freshw. Res. 50, 1393–1398 (1999).
    Article  Google Scholar 

    76.
    Adis, J. & Victoria, R. L. C3 or C4 macrophytes: a specific carbon source for the development of semi-aquatic and terrestrial arthropods in central Amazonian river-floodplains according to delta13C values. Isotopes Environ. Health Stud. 37, 193–198. https://doi.org/10.1080/10256010108033295 (2001).
    CAS  Article  PubMed  Google Scholar 

    77.
    Johnson, B. J. et al. Carbon isotope evidence for an abrupt reduction in grasses coincident with European settlement of Lake Eyre, South Australia. Holocene 15, 888–896. https://doi.org/10.1191/0959683605hl861ra (2005).
    ADS  Article  Google Scholar 

    78.
    Wang, J., Gu, B., Ewe, S. M. L., Wang, Y. & Li, Y. Stable isotope compositions of aquatic flora as indicators of wetland eutrophication. Ecol. Eng. 83, 13–18. https://doi.org/10.1016/j.ecoleng.2015.06.007 (2015).
    Article  Google Scholar 

    79.
    Persson, A. et al. Effects of enrichment on simple aquatic food webs. Am. Nat. 157, 669–674 (2001).
    Article  Google Scholar 

    80.
    Gell, P. et al. Accessing limnological change and variability using fossil diatom assemblages, south-east Australia. River Res. Appl. 21, 257–269. https://doi.org/10.1002/rra.845 (2005).
    Article  Google Scholar 

    81.
    Gell, P. & Reid, M. Assessing change in floodplain wetland condition in the Murray Darling Basin, Australia. Anthropocene 8, 39–45. https://doi.org/10.1016/j.ancene.2014.12.002 (2014).
    Article  Google Scholar  More

  • in

    Extreme environmental conditions reduce coral reef fish biodiversity and productivity

    1.
    Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).
    ADS  CAS  PubMed  Google Scholar 
    2.
    Blowes, S. A. et al. The geography of biodiversity change in marine and terrestrial assemblages. Science 366, 339–345 (2019).
    ADS  CAS  PubMed  Google Scholar 

    3.
    Mace, G. M., Norris, K. & Fitter, A. H. Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol. evolution 27, 19–26 (2012).
    Google Scholar 

    4.
    Vellend, M. The Theory of Ecological Communities (MPB-57) Vol. 75 (Princeton University Press, 2016).

    5.
    Kraft, N. J. et al. Community assembly, coexistence and the environmental filtering metaphor. Funct. Ecol. 29, 592–599 (2015).
    Google Scholar 

    6.
    Leibold, M. A. et al. The metacommunity concept: a framework for multi‐scale community ecology. Ecol. Lett. 7, 601–613 (2004).
    Google Scholar 

    7.
    Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261 (2017).
    ADS  CAS  PubMed  Google Scholar 

    8.
    Schweiger, A. K. et al. Plant spectral diversity integrates functional and phylogenetic components of biodiversity and predicts ecosystem function. Nat. Ecol. Evol. 2, 976 (2018).
    PubMed  Google Scholar 

    9.
    Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).
    PubMed  Google Scholar 

    10.
    Scheffers, B. R. et al. The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).
    PubMed  Google Scholar 

    11.
    García, F. C., Bestion, E., Warfield, R. & Yvon-Durocher, G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc. Natl Acad. Sci. USA 115, 10989–10994 (2018).
    PubMed  Google Scholar 

    12.
    Pörtner, H. O. & Farrell, A. P. Physiology and climate change. Science 322, 690–692 (2008).
    PubMed  Google Scholar 

    13.
    Deutsch, C., Ferrel, A., Seibel, B., Pörtner, H.-O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015).
    ADS  CAS  PubMed  Google Scholar 

    14.
    Bozinovic, F. & Pörtner, H. Physiological ecology meets climate change. Ecol. Evol. 5, 1025–1030 (2015).
    PubMed  PubMed Central  Google Scholar 

    15.
    Barneche, D. R., Jahn, M. & Seebacher, F. Warming increases the cost of growth in a model vertebrate. Funct. Ecol. 33, 1256–1266 (2019).
    Google Scholar 

    16.
    Brown, J. H., Hall, C. A. & Sibly, R. M. Equal fitness paradigm explained by a trade-off between generation time and energy production rate. Nat. Ecol. Evol. 2, 262 (2018).
    PubMed  Google Scholar 

    17.
    Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat. Clim. Change 3, 979 (2013).
    ADS  CAS  Google Scholar 

    18.
    Barneche, D. R. & Allen, A. P. The energetics of fish growth and how it constrains food‐web trophic structure. Ecol. Lett. 21, 836–844 (2018).
    PubMed  Google Scholar 

    19.
    Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).
    Google Scholar 

    20.
    Barnes, A. D. et al. Energy flux: the link between multitrophic biodiversity and ecosystem functioning. Trends Ecol. Evol. 33, 186–197 (2018).
    PubMed  PubMed Central  Google Scholar 

    21.
    Brandl, S. J. et al. Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Front. Ecol. Environ. 17, 445–454 (2019).
    Google Scholar 

    22.
    Spalding, M. et al. Mapping the global value and distribution of coral reef tourism. Mar. Policy 82, 104–113 (2017).
    Google Scholar 

    23.
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).
    ADS  CAS  PubMed  Google Scholar 

    24.
    Pratchett, M. S., Hoey, A. S., Wilson, S. K., Messmer, V. & Graham, N. A. Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3, 424–452 (2011).
    Google Scholar 

    25.
    Brandl, S. J., Emslie, M. J. & Ceccarelli, D. M. Habitat degradation increases functional originality in highly diverse coral reef fish assemblages. Ecosphere 7, e01557 (2016).
    Google Scholar 

    26.
    Fontoura, L. et al. Climate‐driven shift in coral morphological structure predicts decline of juvenile reef fishes. Glob. Change Biol. 26, 557–567 (2020).
    ADS  Google Scholar 

    27.
    Bellwood, D. R., Hoey, A. S., Ackerman, J. L. & Depczynski, M. Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob. Change Biol. 12, 1587–1594 (2006).
    ADS  Google Scholar 

    28.
    Robinson, J. P. et al. Productive instability of coral reef fisheries after climate-driven regime shifts. Nat. Ecol. Evol. 3, 183 (2019).
    PubMed  Google Scholar 

    29.
    Wismer, S., Tebbett, S. B., Streit, R. P. & Bellwood, D. R. Young fishes persist despite coral loss on the Great Barrier Reef. Commun. Biol. 2, 456 (2019).
    PubMed  PubMed Central  Google Scholar 

    30.
    Taylor, B. M. et al. Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching. Glob. Change Biol. 26, 1285–1294 (2020).
    ADS  Google Scholar 

    31.
    Morais, R. A. et al. Severe coral loss shifts energetic dynamics on a coral reef. Funct. Ecol. 34, 1507–1518 (2020).
    Google Scholar 

    32.
    Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).
    ADS  PubMed  Google Scholar 

    33.
    Comte, L. & Olden, J. D. Climatic vulnerability of the world’s freshwater and marine fishes. Nat. Clim. Change 7, 718 (2017).
    ADS  Google Scholar 

    34.
    Munday, P. L., McCormick, M. I. & Nilsson, G. E. Impact of global warming and rising CO2 levels on coral reef fishes: what hope for the future? J. Exp. Biol. 215, 3865–3873 (2012).
    CAS  PubMed  Google Scholar 

    35.
    Munday, P. L., Jones, G. P., Pratchett, M. S. & Williams, A. J. Climate change and the future for coral reef fishes. Fish. Fish. 9, 261–285 (2008).
    Google Scholar 

    36.
    Donelson, J., Munday, P., McCormick, M. & Pitcher, C. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2, 30 (2012).
    ADS  Google Scholar 

    37.
    Ern, R., Huong, D., Cong, N., Bayley, M. & Wang, T. Effect of salinity on oxygen consumption in fishes: a review. J. Fish. Biol. 84, 1210–1220 (2014).
    CAS  PubMed  Google Scholar 

    38.
    Johansen, J. & Jones, G. Increasing ocean temperature reduces the metabolic performance and swimming ability of coral reef damselfishes. Glob. Change Biol. 17, 2971–2979 (2011).
    ADS  Google Scholar 

    39.
    Rummer, J. L. et al. Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob. Change Biol. 20, 1055–1066 (2014).
    ADS  Google Scholar 

    40.
    Nilsson, G. E., Crawley, N., Lunde, I. G. & Munday, P. L. Elevated temperature reduces the respiratory scope of coral reef fishes. Glob. Change Biol. 15, 1405–1412 (2009).
    ADS  Google Scholar 

    41.
    Eme, J. & Bennett, W. A. Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. J. Therm. Biol. 34, 220–225 (2009).
    Google Scholar 

    42.
    Gardiner, N. M., Munday, P. L. & Nilsson, G. E. Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS ONE 5, e13299 (2010).
    ADS  PubMed  PubMed Central  Google Scholar 

    43.
    Bernal, M. A. et al. Species-specific molecular responses of wild coral reef fishes during a marine heatwave. Sci. Adv. 6, eaay3423 (2020).
    ADS  PubMed  PubMed Central  Google Scholar 

    44.
    Mora, C. & Ospina, A. Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific). Mar. Biol. 139, 765–769 (2001).
    Google Scholar 

    45.
    Feary, D. A. et al. Latitudinal shifts in coral reef fishes: why some species do and others do not shift. Fish. Fish. 15, 593–615 (2014).
    Google Scholar 

    46.
    Bernal, M. A. et al. Phenotypic and molecular consequences of stepwise temperature increase across generations in a coral reef fish. Mol. Ecol. 27, 4516–4528 (2018).
    CAS  PubMed  Google Scholar 

    47.
    Grenchik, M., Donelson, J. & Munday, P. Evidence for developmental thermal acclimation in the damselfish, Pomacentrus moluccensis. Coral Reefs 32, 85–90 (2013).
    ADS  Google Scholar 

    48.
    Miller, D. D., Ota, Y., Sumaila, U. R., Cisneros‐Montemayor, A. M. & Cheung, W. W. Adaptation strategies to climate change in marine systems. Glob. Change Biol. 24, e1–e14 (2018).
    Google Scholar 

    49.
    Brandl, S. J., Goatley, C. H., Bellwood, D. R. & Tornabene, L. The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biol. Rev. 93, 1846–1873 (2018).
    PubMed  Google Scholar 

    50.
    Brandl, S. J., Casey, J. M., Knowlton, N. & Duffy, J. E. Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecol. Evol. 7, 7069–7079 (2017).
    PubMed  PubMed Central  Google Scholar 

    51.
    Ahmadia, G. N., Tornabene, L., Smith, D. J. & Pezold, F. L. The relative importance of regional, local, and evolutionary factors structuring cryptobenthic coral-reef assemblages. Coral Reefs 37, 279–293 (2018).
    ADS  Google Scholar 

    52.
    Coker, D. J., DiBattista, J. D., Sinclair-Taylor, T. H. & Berumen, M. L. Spatial patterns of cryptobenthic coral-reef fishes in the Red Sea. Coral Reefs https://doi.org/10.1007/s00338-017-1647-9 (2017).

    53.
    Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).
    ADS  CAS  PubMed  Google Scholar 

    54.
    Miller, P. J. Miniature Vertebrates. The Implications of Small Body Size Vol. 69 (Oxford University Press, 1996).

    55.
    Depczynski, M. & Bellwood, D. Microhabitat utilisation patterns in cryptobenthic coral reef fish communities. Mar. Biol. 145, 455–463 (2004).
    Google Scholar 

    56.
    Bellwood, D. R. et al. Coral recovery may not herald the return of fishes on damaged coral reefs. Oecologia 170, 567–573 (2012).
    ADS  PubMed  Google Scholar 

    57.
    Depczynski, M. & Bellwood, D. R. Shortest recorded vertebrate lifespan found in a coral reef fish. Curr. Biol. 15, R288–R289 (2005).
    CAS  PubMed  Google Scholar 

    58.
    Tornabene, L., Valdez, S., Erdmann, M. & Pezold, F. Support for a ‘Center of Origin’in the Coral Triangle: cryptic diversity, recent speciation, and local endemism in a diverse lineage of reef fishes (Gobiidae: Eviota). Mol. Phylogenet. Evol. 82, 200–210 (2015).
    PubMed  Google Scholar 

    59.
    NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua 11µm Day/Night Sea Surface Temperature Data. https://oceandata.sci.gsfc.nasa.gov/MODIS-Aqua/Mapped/Daily/4km/sst (2018).

    60.
    Howells, E. J. et al. Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol. 29, 899–911 (2020).
    CAS  PubMed  Google Scholar 

    61.
    Howells, E. J., Abrego, D., Meyer, E., Kirk, N. L. & Burt, J. A. Host adaptation and unexpected symbiont partners enable reef‐building corals to tolerate extreme temperatures. Glob. Change Biol. 22, 2702–2714 (2016).
    ADS  Google Scholar 

    62.
    Riegl, B. M. & Purkis, S. J. (Eds.) in Coral Reefs of the Gulf 1–4, (Springer, 2012).

    63.
    Purkis, S. J. & Riegl, B. M. in Coral Reefs of the Gulf: Adaptation to Climatic Extremes (eds Riegl, B. M. & Purkis, S. J.) 33–50 (Springer Netherlands, 2012).

    64.
    Price, A., Sheppard, C. & Roberts, C. The Gulf: its biological setting. Mar. Pollut. Bull. 27, 9–15 (1993).
    Google Scholar 

    65.
    Eagderi, S., Fricke, R., Esmaeili, H. & Jalili, P. Annotated checklist of the fishes of the Persian Gulf: Diversity and conservation status. Iran. J. Ichthyol. 6, 1–171 (2019).
    Google Scholar 

    66.
    Casey, J. M. et al. Reconstructing hyperdiverse food webs: gut content metabarcoding as a tool to disentangle trophic interactions on coral reefs. Methods Ecol. Evol. 10, 1157–1170 (2019).
    Google Scholar 

    67.
    Depczynski, M. & Bellwood, D. R. The role of cryptobenthic reef fishes in coral reef trophodynamics. Mar. Ecol. Prog. Ser. 256, 183–191 (2003).
    ADS  Google Scholar 

    68.
    Pratchett, M. S., Wilson, S. K. & Munday, P. L. in Ecology of Fishes on Coral Reefs (ed. Mora, C.) 127 (Cambridge University Press, 2015).

    69.
    Krupp, F. & Müller, T. The status of fish populations in the northern Arabian Gulf two years after the 1991 Gulf War oil spill. Cour. Forschungsinst. Senckenb. 166, 67–75 (1994).
    Google Scholar 

    70.
    Bishop, J. History and current checklist of Kuwait’s ichthyofauna. J. Arid Environ. 54, 237–256 (2003).
    ADS  Google Scholar 

    71.
    Feary, D. A., Burt, J. A., Cavalcante, G. H. & Bauman, A. G. in Coral Reefs of the Gulf: Adaptation to Climatic Extremes (eds Riegl, B. M. & Purkis, S. J.) 163–170 (Springer Netherlands, 2012).

    72.
    Donelson, J. M., Munday, P. L., MCCORMICK, M. I. & Nilsson, G. E. Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Glob. Change Biol. 17, 1712–1719 (2011).
    ADS  Google Scholar 

    73.
    Ohlberger, J. Climate warming and ectotherm body size—from individual physiology to community ecology. Funct. Ecol. 27, 991–1001 (2013).
    Google Scholar 

    74.
    Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).
    PubMed  Google Scholar 

    75.
    Peig, J. & Green, A. J. The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct. Ecol. 24, 1323–1332 (2010).
    Google Scholar 

    76.
    Sullam, K. E. et al. Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177, 245–257 (2015).
    ADS  PubMed  Google Scholar 

    77.
    Whelan, C. J., Brown, J. S., Schmidt, K. A., Steele, B. B. & Willson, M. F. Linking consumer–resource theory and digestive physiology: application to diet shifts. Evolut. Ecol. Res. 2, 911–934 (2000).
    Google Scholar 

    78.
    Petchey, O. L. Prey diversity, prey composition, and predator population dynamics in experimental microcosms. J. Anim. Ecol. 69, 874–882 (2000).
    PubMed  Google Scholar 

    79.
    Merrick, R. L., Chumbley, M. K. & Byrd, G. V. Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: a potential relationship. Can. J. Fish. Aquat. Sci. 54, 1342–1348 (1997).
    Google Scholar 

    80.
    Hondorp, D. W., Pothoven, S. A. & Brandt, S. B. Influence of Diporeia density on diet composition, relative abundance, and energy density of planktivorous fishes in southeast Lake Michigan. Trans. Am. Fish. Soc. 134, 588–601 (2005).
    Google Scholar 

    81.
    Shraim, R. et al. Environmental extremes are associated with dietary patterns in Arabian Gulf Reef fishes. Front. Mar. Sci. 4, 285 (2017).
    Google Scholar 

    82.
    Agorreta, A. et al. Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Mol. Phylogenet. Evol. 69, 619–633 (2013).
    PubMed  Google Scholar 

    83.
    Thacker, C. E. & Roje, D. M. Phylogeny of Gobiidae and identification of gobiid lineages. Syst. Biodivers. 9, 329–347 (2011).
    Google Scholar 

    84.
    Kovačić, M., Bogorodsky, S. V. & Mal, A. O. Two new species of Coryogalops (Perciformes: Gobiidae) from the Red Sea. Zootaxa 3881, 513–531 (2014).
    PubMed  Google Scholar 

    85.
    Rishworth, G. M., Strydom, N. A. & Perissinotto, R. Fishes associated with living stromatolite communities in peritidal pools: predators, recruits and ecological traps. Mar. Ecol. Prog. Ser. 580, 153–167 (2017).
    ADS  CAS  Google Scholar 

    86.
    Munday, P. L. & Jones, G. P. The ecological implications of small body size among coral-reef fishes. Oceanogr. Mar. Biol. Annu. Rev. 36, 373–411 (1998).
    Google Scholar 

    87.
    Sandblom, E. et al. Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat. Commun. 7, 11447 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    88.
    Norin, T. & Metcalfe, N. B. Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. Philos. Trans. R. Soc. B 374, 20180180 (2019).
    Google Scholar 

    89.
    Sheldon, K. S., Yang, S. & Tewksbury, J. J. Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. Ecol. Lett. 14, 1191–1200 (2011).
    PubMed  Google Scholar 

    90.
    Crossland, C., Hatcher, B. & Smith, S. Role of coral reefs in global ocean production. Coral Reefs 10, 55–64 (1991).
    ADS  Google Scholar 

    91.
    Gove, J. M. et al. Near-island biological hotspots in barren ocean basins. Nat. Commun. 7, 10581 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    92.
    De Goeij, J. M. et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).
    ADS  PubMed  Google Scholar 

    93.
    Wild, C. et al. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428, 66–70 (2004).
    ADS  CAS  PubMed  Google Scholar 

    94.
    Hamner, W., Jones, M., Carleton, J., Hauri, I. & Williams, D. M. Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bull. Mar. Sci. 42, 459–479 (1988).
    Google Scholar 

    95.
    Hatcher, B. G. Coral reef primary productivity: a beggar’s banquet. Trends Ecol. Evol. 3, 106–111 (1988).
    CAS  PubMed  Google Scholar 

    96.
    Bacon, P., Gurney, W., Jones, W., McLaren, I. & Youngson, A. Seasonal growth patterns of wild juvenile fish: partitioning variation among explanatory variables, based on individual growth trajectories of Atlantic salmon (Salmo salar) parr. J. Anim. Ecol. 74, 1–11 (2005).
    Google Scholar 

    97.
    Coles, S. L. Coral species diversity and environmental factors in the Arabian Gulf and the Gulf of Oman: a comparison to the Indo-Pacific region. Atoll Res. Bull. 507, 1–19 (2003).
    Google Scholar 

    98.
    Morais, R. A. & Bellwood, D. R. Pelagic subsidies underpin fish productivity on a degraded coral reef. Curr. Biol. 29, 1521–1527 (2019).
    CAS  PubMed  Google Scholar 

    99.
    Riegl, B. Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE). Mar. Biol. 140, 29–40 (2002).
    Google Scholar 

    100.
    Riegl, B. & Purkis, S. Coral population dynamics across consecutive mass mortality events. Glob. Change Biol. 21, 3995–4005 (2015).
    ADS  Google Scholar 

    101.
    Burt, J., Al-Harthi, S. & Al-Cibahy, A. Long-term impacts of coral bleaching events on the world’s warmest reefs. Mar. Environ. Res. 72, 225–229 (2011).
    CAS  PubMed  Google Scholar 

    102.
    Burt, J. A., Paparella, F., Al-Mansoori, N., Al-Mansoori, A. & Al-Jailani, H. Causes and consequences of the 2017 coral bleaching event in the southern Persian/Arabian Gulf. Coral Reefs 38, 567–589 (2019).
    ADS  Google Scholar 

    103.
    Coker, D. J., Wilson, S. K. & Pratchett, M. S. Importance of live coral habitat for reef fishes. Rev. Fish. Biol. Fish. 24, 89–126 (2014).
    Google Scholar 

    104.
    Pratchett, M. S., Baird, A. H., Bauman, A. G. & Burt, J. A. Abundance and composition of juvenile corals reveals divergent trajectories for coral assemblages across the United Arab Emirates. Mar. Pollut. Bull. 114, 1031–1035 (2017).
    CAS  PubMed  Google Scholar 

    105.
    Munday, P. L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Change Biol. 10, 1642–1647 (2004).
    ADS  Google Scholar 

    106.
    Burt, J. A. et al. Biogeographic patterns of reef fish community structure in the northeastern Arabian Peninsula. ICES J. Mar. Sci. 68, 1875–1883 (2011).
    Google Scholar 

    107.
    Brose, U. et al. Predator traits determine food-web architecture across ecosystems. Nat. Ecol. Evol. 3, 919 (2019).
    PubMed  Google Scholar 

    108.
    Ackerman, J. L. & Bellwood, D. R. Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar. Ecol.-Prog. Ser. 206, 227–237 (2000).
    ADS  Google Scholar 

    109.
    Beitinger, T. L., Bennett, W. A. & McCauley, R. W. Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ. Biol. Fishes 58, 237–275 (2000).
    Google Scholar 

    110.
    Leray, M. et al. A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front. Zool. 10, 34 (2013).
    PubMed  PubMed Central  Google Scholar 

    111.
    Geller, J., Meyer, C., Parker, M. & Hawk, H. Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all‐taxa biotic surveys. Mol. Ecol. Resour. 13, 851–861 (2013).
    CAS  PubMed  Google Scholar 

    112.
    Sherwood, A. R. & Presting, G. G. Universal primers amplify a 23S rDNA plastid marker in eukaryotic algae and cyanobacteria. J. Phycol. 43, 605–608 (2007).
    Google Scholar 

    113.
    Hamsher, S. E., Evans, K. M., Mann, D. G., Poulíčková, A. & Saunders, G. W. Barcoding diatoms: exploring alternatives to COI-5P. Protist 162, 405–422 (2011).
    CAS  PubMed  Google Scholar 

    114.
    Cannon, M. et al. In silico assessment of primers for eDNA studies using PrimerTree and application to characterize the biodiversity surrounding the Cuyahoga River. Sci. Rep. 6, 22908 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    115.
    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    116.
    Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996 (2013).
    CAS  PubMed  Google Scholar 

    117.
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).
    Google Scholar 

    118.
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
    CAS  Google Scholar 

    119.
    Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).
    Google Scholar 

    120.
    Edgar, R. C. & Flyvbjerg, H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31, 3476–3482 (2015).
    CAS  PubMed  Google Scholar 

    121.
    Edgar, R. C. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv https://doi.org/10.1101/081257 (2016).

    122.
    Yilmaz, P. et al. The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42, D643–D648 (2013).
    PubMed  PubMed Central  Google Scholar 

    123.
    Bürkner, P.-C. Advanced Bayesian multilevel modeling with the R Package brms. The R Journal 10, 395–411 (2018).
    Google Scholar 

    124.
    Wasserman, S. & Faust, K. Social Network Analysis: Methods and Applications Vol. 8 (Cambridge University Press, 1994).

    125.
    Newman, M. E. Modularity and community structure in networks. Proc. Natl Acad. Sci. USA 103, 8577–8582 (2006).
    ADS  CAS  PubMed  Google Scholar 

    126.
    Beckett, S. J. Improved community detection in weighted bipartite networks. R. Soc. Open Sci. 3, 140536 (2016).
    ADS  MathSciNet  PubMed  PubMed Central  Google Scholar 

    127.
    Hsieh, T., Ma, K. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).
    Google Scholar 

    128.
    Brandl, S. J. et al. Supplemental materials for demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).
    ADS  CAS  PubMed  Google Scholar 

    129.
    Morais, R. A. & Bellwood, D. R. Global drivers of reef fish growth. Fish. Fish. 19, 874–889 (2018).
    Google Scholar 

    130.
    Allen, K. R. Relation between production and biomass. J. Fish. Board Can. 28, 1573–1581 (1971).
    Google Scholar 

    131.
    Pauly, D. On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES J. Mar. Sci. 39, 175–192 (1980).
    Google Scholar 

    132.
    Gislason, H., Daan, N., Rice, J. C. & Pope, J. G. Size, growth, temperature and the natural mortality of marine fish. Fish. Fish. 11, 149–158 (2010).
    Google Scholar 

    133.
    Morais, R. A. & Bellwood, D. R. Principles for estimating fish productivity on coral reefs. Coral Reefs https://doi.org/10.1007/s00338-020-01969-9 (2020).

    134.
    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2019).

    135.
    Wickham, H. Tidyverse: easily install and load’tidyverse’packages. R package version 1, https://CRAN.R-project.org/package=tidyverse (2017).

    136.
    Oksanen, J. et al. The vegan package. Commun. Ecol. Package 10, 719 (2007).
    Google Scholar 

    137.
    Csardi, G. & Nepusz, T. The igraph software package for complex network research. InterJournal, Complex Syst. 1695, 1–9 (2006).
    Google Scholar 

    138.
    Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R News 8, 8–11 (2008).
    Google Scholar 

    139.
    Kay, M. tidybayes: Tidy data and geoms for Bayesian models. R package version 1, https://doi.org/10.5281/zenodo.1468151 (2018).

    140.
    Chen, T., He, T., Benesty, M., Khotilovich, V. & Tang, Y. Xgboost: extreme gradient boosting. R package version 0.4-2, 1–4 (2015).

    141.
    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Package “emmeans”: estimated marginal means, aka least-squares means. Compr. R. Arch. Netw. 1–67 (2019). http://CRAN.R-project.org/package=emmeans.

    142.
    Bauer, R. Oceanmap: a plotting toolbox for 2D oceanographic data. R package, version 0.0 9, https://CRAN.R-project.org/package=oceanmap (2017).

    143.
    Pierce, D. & Pierce, M. D. Package ‘ncdf4’. https://cran.r-project.org/web/packages/ncdf4/index.html (2019).

    144.
    Hijmans, R. J. et al. Raster package in R. https://cran.r-project.org/web/packages/raster/index.html (2013).

    145.
    Schiettekatte, N. M., Brandl, S. J. & Casey, J. M. fishualize: Color palettes based on fish species. https://cran.r-project.org/web/packages/fishualize/fishualize.pdf (2019). More

  • in

    Interactions between the imperiled West Indian manatee, Trichechus manatus, and mosquitoes (Diptera: Culicidae) in Everglades National Park, Florida, USA

    1.
    Manguin, S. & Boete, C. Global impact of mosquito biodiversity, human vector-borne diseases and environmental change. In The Importance of Biological Interactions in the Study of Biodiversity (ed. López-Pujol, J.) 27–50 (InTechOpen, London, 2011).
    Google Scholar 
    2.
    Downes, J. A. The biting habits of blood-feeding flies and their significance in classification. Annu. Rev. Entomol. 3, 249–266 (1958).
    Google Scholar 

    3.
    Reeves, L. E. et al. Identification of Uranotaenia sapphirina as a specialist of annelids broadens known mosquito host use patterns. Commun. Biol. 1, 92 (2018).
    PubMed  PubMed Central  Google Scholar 

    4.
    Borkent, A. & Belton, P. Attraction of female Uranotaenia lowii (Diptera: Culicidae) to frog calls in Costa Rica. Can. Entomol. 138, 91–94 (2006).
    Google Scholar 

    5.
    Toma, T., Miyagi, I. & Tamashiro, M. Blood meal identification and feeding habits of Uranotaenia species collected in the Ryukyu Archipelago. J. Am. Mosq. Control 30, 215–218 (2014).
    Google Scholar 

    6.
    Sorokin, A. & Steigerwald, E. Ameerega trivittata (three-striped poison frog) ecto-parasitism. Herpetol. Rev. 48, 407–408 (2017).
    Google Scholar 

    7.
    Okudo, H. et al. A crab-hole mosquito, Ochlerotatus baisasi, feeding on mudskipper (Gobiidae: Oxudercinae) in the Ryukyu Islands, Japan. J. Am. Mosq. Control 20, 134–137 (2004).
    Google Scholar 

    8.
    Miyake, T. et al. Bloodmeal host identification with inferences to feeding habits of a fish-fed mosquito, Aedes baisasi. Sci. Rep. 9, 4002 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    9.
    Unlu, I., Kramer, W. L., Roy, A. F. & Foil, L. D. Detection of West Nile virus RNA in mosquitoes and identification of mosquito blood meals collected at alligator farms in Louisiana. J. Med. Entomol. 47, 625–633 (2010).
    CAS  PubMed  Google Scholar 

    10.
    Reeves, L. E., Connelly, C. R. & Krysko, K. L. Crocodylus acutus (American crocodile) ectoparasites. Herpetol. Rev. 50, 131–132 (2019).
    Google Scholar 

    11.
    Cupp, E. W. et al. Identification of reptilian and amphibian blood meals from mosquitoes in an Eastern equine encephalomyelitis virus focus in central Alabama. Am. J. Trop. Med. Hyg. 71, 272–276 (2004).
    PubMed  PubMed Central  Google Scholar 

    12.
    Burkett-Cadena, N. D. et al. Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. Am. J. Trop. Med. Hyg. 79, 809–815 (2008).
    PubMed  PubMed Central  Google Scholar 

    13.
    Reeves, L. E. et al. Interactions between the invasive Burmese python, Python bivittatus Kuhl, and the local mosquito community in Florida, USA. PLoS ONE 13, e0190633 (2018).
    PubMed  PubMed Central  Google Scholar 

    14.
    Buck, C. et al. Isolation of St. Louis encephalitis virus from a killer whale. Clin. Diagn. Virol. 1, 109–112 (1993).
    CAS  PubMed  Google Scholar 

    15.
    Leger, J. S. et al. West Nile infection in killer whale, Texas, USA, 2007. Emerg. Infect. Dis. 17(8), 1531–1533 (2011).
    Google Scholar 

    16.
    Schaefer, A. M. et al. Serological evidence of exposure to selected viral, bacterial, and protozoal pathogens in free-ranging Atlantic bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon, Florida, and Charleston, South Carolina. Aquat. Mamm. 35, 163–170 (2009).
    Google Scholar 

    17.
    Jett, J. & Ventre, J. Orca (Orcinus orca) captivity and vulnerability to mosquito-transmitted viruses. J. Mar. Anim. Ecol. 5, 9–16 (2012).
    Google Scholar 

    18.
    Hribar, L., DeMay, D. J. & Lund, U. J. The association between meteorological variables and the abundance of Aedes taeniorhynchus in the Florida Keys. J. Vector Ecol. 35, 339–346 (2010).
    PubMed  Google Scholar 

    19.
    Yee, D. A., Himel, E., Reiskind, M. H. & Vamosi, S. M. Implications of saline concentrations for the performance and competitive interactions of the mosquitoes Aedes aegypti (Stegomyia aegypti) and Aedes albopictus (Stegomyia albopictus). Med. Vet. Entomol. 28, 60–69 (2014).
    CAS  PubMed  Google Scholar 

    20.
    Darsie, R. F. Jr. & Morris, C. D. Keys to the Adult Females and Fourth Instar Larvae of the Mosquitoes of Florida (Diptera, Culicidae) (Florida Mosquito Control Association, Buckingham, 2003).
    Google Scholar 

    21.
    Hoyer, I. J., Blosser, E. M., Acevedo, C., Reeves, L. E. & Burkett-Cadena, N. D. Mammal decline, linked to invasive Burmese python, shifts host use of vector mosquito towards reservoir hosts of a zoonotic disease. Biol. Lett. 13, 20170353 (2017).
    PubMed  PubMed Central  Google Scholar 

    22.
    Cummins, B., Cortez, R., Foppa, I. M., Walbeck, J. & Hyman, J. H. A spatial model of mosquito host-seeking behavior. PLOS Comput. Biol. 8, e1002500 (2012).
    ADS  MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

    23.
    Gillies, M. T. & Wilkes, T. J. The range of attraction of single baits for some West African mosquitoes. Bull. Entomol. Res. 60, 225–235 (1970).
    CAS  PubMed  Google Scholar 

    24.
    Lehane, M. J. The Biology of Blood-Sucking in Insects 2nd edn. (Cambridge University Press, Cambridge, 2005).
    Google Scholar 

    25.
    Edman, J. A. Host-feeding patterns of Florida mosquitoes (Diptera: Culicidae) VI. Culex (Melanoconion). J. Med. Entomol. 15, 521–525 (1979).
    CAS  PubMed  Google Scholar 

    26.
    Burkett-Cadena, N. D., Hoyer, I., Blosser, E. & Reeves, L. Human-powered pop-up resting shelter for sampling cavity-resting mosquitoes. Acta Trop. 190, 288–292 (2019).
    PubMed  Google Scholar 

    27.
    Reeves, L. E., Hoyer, I., Acevedo, C. & Burkett-Cadena, N. D. Host associations of Culex (Melanoconion) atratus (Diptera: Culicidae) and Culex (Melanoconion) pilosus from Florida, USA. Insects 10, 239 (2019).
    PubMed Central  Google Scholar 

    28.
    Blosser, E., Stenn, T., Acevedo, C. & Burkett-Cadena, N. D. Host use and seasonality of Culex (Melanoconion) iolambdis (Diptera: Culicidae) from eastern Florida, USA. Acta Trop. 164, 352–359 (2016).
    PubMed  Google Scholar 

    29.
    Weaver, S. C., Ferro, C., Barrera, R., Boshell, J. & Navarro, J.-C. Venezuelan equine encephalitis. Annu. Rev. Entomol. 49, 141–174 (2004).
    CAS  PubMed  Google Scholar 

    30.
    King, W. V., Bradley, G. H. & McNeel, T. E. The Mosquitoes of the Southeastern States, United States Department of Agriculture Miscellaneous Publication No. 336. (Agricultural Research Service, 1944).

    31.
    DeMay, D. J. & Hribar, L. J. Mosquito fauna of Key Largo, Florida. J. Am. Mosq. Control 24, 471–477 (2008).
    Google Scholar 

    32.
    Bidlingmayer, W. L. & Haeger, J. S. Distribution and abundance. In Bionomics and physiology of Aedes taeniorhynchus and Aedes sollicitans, the salt marsh mosquitoes of Florida, Bulletin 852 (ed. Nayar, J. K.) 14–17 (Florida Agricultural Experiment Station, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, 1985).
    Google Scholar 

    33.
    Kline, D. L. & LeMire, G. F. Field evaluation of heat as an attractant to traps baited with carbon dioxide and octenol for Aedes taeniorhynchus. J. Am. Mosq. Control Assoc. 11, 454–456 (1995).
    CAS  PubMed  Google Scholar 

    34.
    Edman, J. A. Host-feeding patterns of Florida mosquitoes (Diptera: Culicidae) I. Aedes, Anopheles, Coquillettidia, Mansonia and Psorophora. J. Med. Entomol. 8, 687–695 (1971).
    CAS  PubMed  Google Scholar 

    35.
    O’Meara, G. F. & Edman, J. A. Autogenous egg production in the salt-marsh mosquito, Aedes taeniorhynchus. Biol. Bull. 149, 384–396 (1975).
    PubMed  Google Scholar 

    36.
    Edman, J. A. Blood-feeding behavior. In Bionomics and physiology of Aedes taeniorhynchus and Aedes sollicitans, the salt marsh mosquitoes of Florida, Bulletin 852 (ed. Nayar, J. K.) 95–103 (Florida Agricultural Experiment Station, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, 1985).
    Google Scholar 

    37.
    Dorcas, M. E. et al. Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park. Proc. Natl. Acad. Sci. USA 14, 2418–2422 (2012).
    ADS  Google Scholar 

    38.
    McCleery, R. A. et al. Marsh rabbit mortalities tie pythons to the precipitous decline of mammals in the Everglades. Proc. R. Soc. B 282, 20150120 (2015).
    PubMed  Google Scholar 

    39.
    Willson, J. D., Dorcas, M. E. & Snow, R. W. Identifying plausible scenarios for the establishment of invasive Burmese pythons (Python molurus) in Southern Florida. Biol. Invasions 13, 1493–1504 (2011).
    Google Scholar 

    40.
    Ramasamy, R. & Surendran, S. N. Global climate change and its potential impact on disease transmission by salinity-tolerant mosquito vectors in coastal zones. Front. Physiol. 3, 198 (2012).
    PubMed  PubMed Central  Google Scholar 

    41.
    Lobuda, M. & Kozuch, O. Amplification of arbovirus transmission by mosquito intradermal probing and interrupted feeding. Acta Virol. 33, 63–67 (1989).
    Google Scholar 

    42.
    Styer, L. M. et al. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLOS Pathog. 3, e132 (2007).
    PubMed Central  Google Scholar 

    43.
    Sulzner, K. et al. Health assessment and seroepidemiologic survey of potential pathogens in wild Antillean manatees (Trichechus manatus manatus). PLoS ONE 7, e44517 (2012).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    44.
    Keller, M., Long, M. T., Francis-Floyd, R. & Isaza, R. A serologic survey of Florida manatees (Trichechus manatus latirostris) for West Nile virus and development of a competitive inhibition ELISA. In Proceedings of 35th Annual International Associations for Aquatic Animal Medicine Conference, Galveston, TX (2004).

    45.
    Dalton, L. M., Dickerson, S. & Wigdahl, D. A serosurvey for West Nile virus at SeaWorld San Antonio, San Antonio, TX. In Proceedings of 35th Annual International Associations for Aquatic Animal Medicine Conference, Galveston, TX (2004).

    46.
    Del Piero, F., Stremme, D. W., Habecker, P. L. & Cantile, C. West Nile flavivirus polioencephalomyelitis in a harbor seal (Phoca vitulina). Vet. Pathol. 43, 58–61 (2006).
    PubMed  Google Scholar 

    47.
    McBride, M. P. et al. Eastern equine encephalitis in a harbor seal. J. Zoo. Wildl. Med. 39, 631–637 (2008).
    PubMed  Google Scholar 

    48.
    Parker, B. M. Density and distribution of Dirofilaria immitis (Nematoda: Filarioidea) third-stage larvae in Aedes sollicitans and Aedes taeniorhynchus (Diptera: Culicidae). J. Med. Entomol. 37, 695–700 (2000).
    CAS  PubMed  Google Scholar 

    49.
    Hribar, L. J. et al. Isolation of West Nile virus from mosquitoes (Diptera: Culicidae) in the Florida Keys, Monroe County, Florida. Caribb. J. Sci. 40, 362–367 (2004).
    Google Scholar 

    50.
    Smith, D. R., Arrigo, N. C., Leal, G., Muehlberger, L. E. & Weaver, S. C. Infection and dissemination of Venezuelan equine encephalitis virus in the epidemic mosquito vector, Aedes taeniorhynchus. Am. J. Trop. Med. Hyg. 77, 176–187 (2007).
    PubMed  Google Scholar 

    51.
    Mayne, B. & Griffitts, T. H. D. Anopheles atropos D. & K.: A new potential carrier of malaria organisms. Public Health Rep. 46, 3107–3115 (1931).
    Google Scholar 

    52.
    De Mucha Macias, J. & Gonzalez, M. Venezuelan equine encephalitis. Study of a strain isolated in Mexico. Rev. Investig. Salud Publica 27, 85–110 (1967).
    Google Scholar 

    53.
    Scherer, W. F. et al. Ecologic studies of Venezuelan encephalitis virus in southeastern México. III. Infection of mosquitoes. Am. J. Trop. Med. Hyg. 20, 969–979 (1971).
    CAS  PubMed  Google Scholar 

    54.
    Scott, M. D., Irvine, A. B. & Wells, R. S. A long-term study of bottlenose dolphins on the west coast of Florida. In The Bottlenose Dolphin (eds Leatherwood, S. & Reeves, R. R.) 235–244 (Academic Press, New York, 1990).
    Google Scholar 

    55.
    Mate, B. R. et al. Satellite-monitored movements and dive behavior of a bottlenose dolphin (Tursiops truncatus) in Tampa Bay, Florida. Mar. Mammal Sci. 11, 452–463 (1995).
    Google Scholar 

    56.
    Lothrop, H. D. & Reisen, W. K. Landscape affects the host-seeking patterns of Culex tarsalis (Diptera: Culicidae) in the Coachella Valley of California. J. Med. Entomol. 38, 325–332 (2001).
    CAS  PubMed  Google Scholar 

    57.
    Van Bressem, M.-F. et al. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis. Aquat. Organ. 86, 143–157 (2009).
    PubMed  Google Scholar 

    58.
    Bossart, G. D., Fair, P., Schaefer, A. M. & Reif, J. S. Health and environmental risk assessment project for bottlenose dolphins Tursiops truncatus from the southeastern USA. I. Infectious diseases. Dis. Aquat. Mamm. 125, 141–153 (2017).
    CAS  Google Scholar 

    59.
    Bossart, G. D. & Duignan, P. J. Emerging viruses in marine mammals. CAB Rev. 13, 052 (2018).
    Google Scholar  More

  • in

    Evolutionary history of zoogeographical regions surrounding the Tibetan Plateau

    1.
    Royden, L. H., Burchfiel, B. C. & van der Hilst, R. D. The geological evolution of the Tibetan Plateau. Science321, 1054–1058 (2008).
    CAS  PubMed  Google Scholar 
    2.
    Wang, C. et al. Outward-growth of the Tibetan Plateau during the Cenozoic: a review. Tectonophysics621, 1–43 (2014).
    Google Scholar 

    3.
    Yin, A. Cenozoic tectonic evolution of Asia: a preliminary synthesis. Tectonophysics488, 293–325 (2010).
    Google Scholar 

    4.
    An, Z., Kutzbach, J. E., Prell, W. L. & Porter, S. C. Evolution of Asian monsoons and phased uplift of the Himalaya–Tibetan plateau since Late Miocene times. Nature411, 62–66 (2001).
    CAS  Google Scholar 

    5.
    Holt, B. G. et al. An update of Wallace’s zoogeographic regions of the world. Science339, 74–78 (2013).
    CAS  PubMed  Google Scholar 

    6.
    Kreft, H. & Jetz, W. A framework for delineating biogeographical regions based on species distributions. J. Biogeogr.37, 2029–2053 (2010).
    Google Scholar 

    7.
    Favre, A. et al. The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev.90, 236–253 (2015).
    PubMed  Google Scholar 

    8.
    Ficetola, G. F., Mazel, F. & Thuiller, W. Global determinants of zoogeographical boundaries. Nat. Ecol. Evol.1, 89 (2017).
    PubMed  Google Scholar 

    9.
    He, J., Kreft, H., Lin, S., Xu, Y. & Jiang, H. Cenozoic evolution of beta diversity and a Pleistocene emergence for modern mammal faunas in China. Glob. Ecol. Biogeogr.27, 1326–1338 (2018).
    Google Scholar 

    10.
    Zhang, P. et al. Phylogeny, evolution, and biogeography of Asiatic Salamanders (Hynobiidae). Proc. Natl Acad. Sci. USA103, 7360–7365 (2006).
    CAS  PubMed  Google Scholar 

    11.
    Che, J. et al. Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc. Natl Acad. Sci. USA107, 13765–13770 (2010).
    CAS  PubMed  Google Scholar 

    12.
    Meng, J. & McKenna, M. C. Faunal turnovers of Palaeogene mammals from the Mongolian Plateau. Nature394, 364–367 (1998).
    CAS  Google Scholar 

    13.
    Pisano, J. et al. Out of Himalaya: the impact of past Asian environmental changes on the evolutionary and biogeographical history of Dipodoidea (Rodentia). J. Biogeogr.42, 856–870 (2015).
    Google Scholar 

    14.
    Mosbrugger, V., Favre, A., Muellner-Riehl, A. N., Päckert, M. & Mulch, A. Cenozoic evolution of geo-biodiversity in the Tibeto-Himalayan region. in Mountains, Climate and Biodiversity (eds Hoorn, C., Perrigo, A. & Antonelli, A.) 429–448 (Wiley-Blackwell, 2018).

    15.
    Li, J. et al. Diversification of rhacophorid frogs provides evidence for accelerated faunal exchange between India and Eurasia during the Oligocene. Proc. Natl Acad. Sci. USA110, 3441–3446 (2013).
    CAS  PubMed  Google Scholar 

    16.
    Klaus, S., Morley, R. J., Plath, M., Zhang, Y. P. & Li, J. T. Biotic interchange between the Indian subcontinent and mainland Asia through time. Nat. Commun.7, 12132 (2016).
    CAS  PubMed  PubMed Central  Google Scholar 

    17.
    Jiang, D., Klaus, S., Zhang, Y. P., Hillis, D. M. & Li, J. T. Asymmetric biotic interchange across the Bering land bridge between Eurasia and North America. Natl Sci. Rev.6, 739–745 (2019).
    Google Scholar 

    18.
    Deng, T. et al. Out of Tibet: Pliocene woolly rhino suggests high-plateau origin of ice age megaherbivores. Science333, 1285–1288 (2011).
    CAS  PubMed  Google Scholar 

    19.
    Mazel, F. et al. Global patterns of β-diversity along the phylogenetic time-scale: the role of climate and plate tectonics. Glob. Ecol. Biogeogr.26, 1211–1221 (2017).
    Google Scholar 

    20.
    Antonelli, A. et al. Amazonia is the primary source of Neotropical biodiversity. Proc. Natl Acad. Sci. USA115, 6034–6039 (2018).
    CAS  PubMed  Google Scholar 

    21.
    Daru, B. H., Elliott, T. L., Park, D. S. & Davies, T. J. Understanding the processes underpinning patterns of phylogenetic regionalization. Trends Ecol. Evol.32, 845–860 (2017).
    PubMed  Google Scholar 

    22.
    Hazzi, N. A., Moreno, J. S., Ortiz-Movliav, C. & Palacio, R. D. Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proc. Natl Acad. Sci. USA115, 7985–7990 (2018).
    CAS  PubMed  Google Scholar 

    23.
    Daru, B. H., van der Bank, M. & Davies, T. J. Unravelling the evolutionary origins of biogeographic assemblages. Divers. Distrib.24, 313–324 (2018).
    Google Scholar 

    24.
    Cowman, P. F., Parravicini, V., Kulbicki, M. & Floeter, S. R. The biogeography of tropical reef fishes: endemism and provinciality through time. Biol. Rev.92, 2112–2130 (2017).
    PubMed  Google Scholar 

    25.
    Graham, R. W. et al. Spatial response of mammals to late quaternary environmental fluctuations. Science272, 1601–1606 (1996).
    CAS  PubMed  Google Scholar 

    26.
    Hopkins, M. J., Bapst, D. W., Simpson, C. & Warnock, R. C. The inseparability of sampling and time and its influence on attempts to unify the molecular and fossil records. Paleobiology44, 561–574 (2018).
    Google Scholar 

    27.
    Silvestro, D. et al. Fossil biogeography: a new model to infer dispersal, extinction and sampling from palaeontological data. Philos. Trans. R. Soc. B371, 20150225 (2016).
    Google Scholar 

    28.
    Dornburg, A., Moore, J., Beaulieu, J. M., Eytan, R. I. & Near, T. J. The impact of shifts in marine biodiversity hotspots on patterns of range evolution: evidence from the Holocentridae (squirrelfishes and soldierfishes). Evolution69, 146–161 (2015).
    PubMed  Google Scholar 

    29.
    Siqueira, A. C., Bellwood, D. R., Cowman, P. F. & Gaither, M. Historical biogeography of herbivorous coral reef fishes: the formation of an Atlantic fauna. J. Biogeogr.46, 1611–1624 (2019).
    Google Scholar 

    30.
    Kidwell, S. M. & Holland, S. M. The quality of the fossil record: implications for evolutionary analyses. Annu. Rev. Ecol. Evol. S33, 561–588 (2002).
    Google Scholar 

    31.
    Tomašových, A. & Kidwell, S. M. Fidelity of variation in species composition and diversity partitioning by death assemblages: time-averaging transfers diversity from beta to alpha levels. Paleobiology35, 94–118 (2009).
    Google Scholar 

    32.
    Crisp, M. D. & Cook, L. G. How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective. Annu. Rev. Ecol. Evol. S44, 303–324 (2013).
    Google Scholar 

    33.
    Bacon, C. D. et al. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc. Natl Acad. Sci. USA112, 6110–6115 (2015).
    CAS  PubMed  Google Scholar 

    34.
    White, A. E., Dey, K. K., Mohan, D., Stephens, M. & Price, T. D. Regional influences on community structure across the tropical-temperate divide. Nat. Commun.10, 2646 (2019).
    PubMed  PubMed Central  Google Scholar 

    35.
    Kreft, H. & Jetz, W. Comment on “An update of Wallace’s zoogeographic regions of the world”. Science341, 343 (2013).
    CAS  PubMed  Google Scholar 

    36.
    Ali, J. R. & Aitchison, J. C. Gondwana to Asia: Plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma). Earth-Sci. Rev.88, 145–166 (2008).
    Google Scholar 

    37.
    Renner, S. S. Multiple Miocene Melastomataceae dispersal between Madagascar, Africa and India. Philos. Trans. R. Soc. B359, 1485–1494 (2004).
    Google Scholar 

    38.
    Kamei, R. G. et al. Discovery of a new family of amphibians from northeast India with ancient links to Africa. Proc. R. Soc. B: Biol. Sci.279, 2396–2401 (2012).
    Google Scholar 

    39.
    Wu, F., Miao, D., Chang, M. M., Shi, G. & Wang, N. Fossil climbing perch and associated plant megafossils indicate a warm and wet central Tibet during the late Oligocene. Sci. Rep.7, 878 (2017).
    PubMed  PubMed Central  Google Scholar 

    40.
    Deng, T. & Ding, L. Paleoaltimetry reconstructions of the Tibetan Plateau: progress and contradictions. Natl Sci. Rev.2, 417–437 (2015).
    CAS  Google Scholar 

    41.
    Li, Q. & Wang, X. Into Tibet: an early Pliocene dispersal of fossil zokor (Rodentia: Spalacidae) from Mongolian Plateau to the hinterland of Tibetan Plateau. PLoS ONE10, e0144993 (2015).
    PubMed  PubMed Central  Google Scholar 

    42.
    Li, Q., Stidham, T. A., Ni, X. & Li, L. Two new Pliocene hamsters (Cricetidae, Rodentia) from southwestern Tibet (China), and their implications for rodent dispersal ‘into Tibet’. J. Vertebr. Paleontol.37, e1403443 (2018).
    Google Scholar 

    43.
    Mulch, A. & Chamberlain, C. P. The rise and growth of Tibet. Nature439, 670–671 (2006).
    CAS  PubMed  Google Scholar 

    44.
    Su, T. et al. Uplift, climate and biotic changes at the Eocene-Oligocene transition in Southeast Tibet. Natl Sci. Rev.6, 495–504 (2018).
    Google Scholar 

    45.
    Guo, Z. et al. Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature416, 159–163 (2002).
    CAS  PubMed  Google Scholar 

    46.
    Sun, J. et al. Late Oligocene–Miocene mid-latitude aridification and wind patterns in the Asian interior. Geology38, 515–518 (2010).
    CAS  Google Scholar 

    47.
    Miao, Y., Herrmann, M., Wu, F., Yan, X. & Yang, S. What controlled Mid–Late Miocene long-term aridification in Central Asia? — Global cooling or Tibetan Plateau uplift: a review. Earth-Sci. Rev.112, 155–172 (2012).
    Google Scholar 

    48.
    Wu, S. D. et al. Evolution of Asian interior arid-zone biota: evidence from the diversification of Asian Zygophyllum (Zygophyllaceae). PLoS ONE10, e0138697 (2015).
    PubMed  PubMed Central  Google Scholar 

    49.
    Qiu, Z. & Li, C. Evolution of Chinese mammalian faunal regions and elevation of the Qinghai-Xizang (Tibet) Plateau. Sci. China Ser. D.48, 1246–1258 (2005).
    Google Scholar 

    50.
    Sun, X. & Wang, P. How old is the Asian monsoon system?—Palaeobotanical records from China. Palaeogeogr. Palaeocl.222, 181–222 (2005).
    Google Scholar 

    51.
    Li, Y. et al. Mammalian evolution in Asia linked to climate changes. in Late Cenozoic Climate Change in Asia: Loess, Monsoon and Monsoon-arid Environment Evolution (ed. An, Z.) 435–490 (Springer, 2014).

    52.
    Scotese, C. R. & Wright, N. PALEOMAP Paleodigital Elevation Models (PaleoDEMS) for the Phanerozoic. (2018). Retrieved from https://www.earthbyte.org/paleodem-resource-scotese-and-wright-2018/. (accessed in June 22, 2019).

    53.
    Lanier, H. C. & Olson, L. E. Inferring divergence times within pikas (Ochotona spp.) using mtDNA and relaxed molecular dating techniques. Mol. Phylogenetics Evol.53, 1–12 (2009).
    CAS  Google Scholar 

    54.
    Chan, Y. C. et al. Mitochondrial genome sequences effectively reveal the phylogeny of Hylobates gibbons. PLoS ONE5, e14419 (2010).
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Mercer, J. M. & Roth, V. L. The effects of Cenozoic global change on squirrel phylogeny. Science299, 1568–1572 (2003).
    CAS  PubMed  Google Scholar 

    56.
    Xing, Y. & Ree, R. H. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc. Natl Acad. Sci. USA114, 3444–3451 (2017).
    Google Scholar 

    57.
    He, D. & Chen, Y. Molecular phylogeny and biogeography of the highly specialized grade schizothoracine fishes (Teleostei: Cyprinidae) inferred from cytochrome b sequences. Chin. Sci. Bull.52, 777–788 (2007).
    CAS  Google Scholar 

    58.
    Lei, F., Qu, Y. & Song, G. Species diversification and phylogeographical patterns of birds in response to the uplift of the Qinghai-Tibet Plateau and Quaternary glaciations. Curr. Zool.60, 149–161 (2014).
    Google Scholar 

    59.
    Svenning, J.-C., Eiserhardt, W. L., Normand, S., Ordonez, A. & Sandel, B. The influence of paleoclimate on present-day patterns in biodiversity and ecosystems. Annu. Rev. Ecol. Evol. S46, 551–572 (2015).
    Google Scholar 

    60.
    He, J., Kreft, H., Gao, E., Wang, Z. & Jiang, H. Patterns and drivers of zoogeographical regions of terrestrial vertebrates in China. J. Biogeogr.44, 1172–1184 (2017).
    Google Scholar 

    61.
    Rolland, J. et al. The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity. Nat. Ecol. Evol.2, 459–464 (2018).
    PubMed  Google Scholar 

    62.
    Saladin, B. et al. Environment and evolutionary history shape phylogenetic turnover in European tetrapods. Nat. Commun.10, 249 (2019).
    PubMed  PubMed Central  Google Scholar 

    63.
    Marshall, C. R. Five palaeobiological laws needed to understand the evolution of the living biota. Nat. Ecol. Evol.1, 165 (2017).
    PubMed  Google Scholar 

    64.
    Hunt, G. & Slater, G. Integrating paleontological and phylogenetic approaches to macroevolution. Annu. Rev. Ecol. Evol. S47, 189–213 (2016).
    Google Scholar 

    65.
    Matzke, N. J. Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Front. Biogeogr.5, 242–248 (2013).
    Google Scholar 

    66.
    Roll, U. et al. The global distribution of tetrapods reveals a need for targeted reptile conservation. Nat. Ecol. Evol.1, 1677–1682 (2017).
    PubMed  Google Scholar 

    67.
    Upham, N. S., Esselstyn, J. A. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol.17, e3000494 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    68.
    Jetz, W. et al. Global distribution and conservation of evolutionary distinctness in birds. Curr. Biol.24, 919–930 (2014).
    CAS  PubMed  Google Scholar 

    69.
    Tonini, J. F. R., Beard, K. H., Ferreira, R. B., Jetz, W. & Pyron, R. A. Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv.204, 23–31 (2016).
    Google Scholar 

    70.
    Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol.2, 850–858 (2018).
    PubMed  Google Scholar 

    71.
    Schliep, K. phangorn: phylogenetic analysis in R. Bioinformatics27, 592–593 (2011).
    CAS  PubMed  Google Scholar 

    72.
    R Core Team. R: a language and environment for statistical computing. https://www.Rproject.org/ (R Foundation for Statistical Computing, Vienna, Austria, 2019).

    73.
    Blois, J. L. & Hadly, E. A. Mammalian response to Cenozoic climatic change. Annu. Rev. Earth Planet. Sci.37, 181–208 (2009).
    CAS  Google Scholar 

    74.
    Kocsis, Á. T. & Raja, N. B. chronosphere: earth system history variables. https://doi.org/10.1111/2041-210X.13161 (2019).

    75.
    Baselga, A. & Orme, C. D. L. betapart: an R package for the study of beta diversity. Methods Ecol. Evol.3, 808–812 (2012).
    Google Scholar 

    76.
    Dapporto, L. et al. recluster: an unbiased clustering procedure for beta‐diversity turnover. Ecography36, 1070–1075 (2013).
    Google Scholar 

    77.
    Oksanen, J. et al. vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan (2019).

    78.
    He, J., Lin, S., Li, J., Yu, J. & Jiang, H. Evolutionary history of zoogeographical regions surrounding the Tibetan Plateau, Dryad, Dataset, https://doi.org/10.5061/dryad.5x69p8d10 (2020). More

  • in

    Proliferation of Aedes aegypti in urban environments mediated by the availability of key aquatic habitats

    1.
    Messina, J. et al. A global compendium of human dengue virus occurrence. Sci. Data 1, 140004 (2014).
    PubMed  PubMed Central  Google Scholar 
    2.
    Brady, O. J. & Hay, S. I. The global expansion of dengue: how Aedes aegypti mosquitoes enabled the first pandemic arbovirus. Annu. Rev. Entomol. 65, 191–208 (2020).
    CAS  PubMed  Google Scholar 

    3.
    Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    4.
    Brady, O. J. et al. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl. Trop. Dis. 6, e1760 (2012).
    PubMed  PubMed Central  Google Scholar 

    5.
    PAHO/WHO. Zika cases and congenital syndrome associated with Zika virus reported by countries and territories in the Americas (Cumulative Cases), 2015–2017. World Health Organization. Available at: https://www.paho.org/hq/index.php?option=com_content&view=article&id=12390:zika-cumulative-cases&Itemid=42090&lang=en.

    6.
    Faria, N. R. et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546, 406–410 (2017).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    7.
    Delaney, A. et al. Population-based surveillance of birth defects potentially related to Zika Virus Infection—15 States and U.S. Territories, 2016. MMWR. Morb. Mortal. Wkly. Rep. 67, 91–96 (2018).

    8.
    Shapiro-Mendoza, C. K. et al. Pregnancy Outcomes After Maternal Zika Virus Infection During Pregnancy ? U.S. Territories, January 1, 2016? April 25, 2017. MMWR. Morb. Mortal. Wkly. Rep. 66, 615–621 (2017).

    9.
    PAHO & WHO. Epidemiological update: Yellow fever. Pan Am. Heal. Organ. World Heal. Organ. 1–4 (2019).

    10.
    Garske, T. et al. Yellow fever in Africa: estimating the burden of disease and impact of mass vaccination from outbreak and serological data. PLoS Med. 11, e1001638 (2014).
    PubMed  PubMed Central  Google Scholar 

    11.
    Nathan, N., Barry, M., Van Herp, M. & Zeller, H. Shortage of vaccines during a yellow fever outbreak in Guinea. Lancet 358, 2129–2130 (2001).
    CAS  PubMed  Google Scholar 

    12.
    Weitzel, T., Vial, P., Perret, C. & Aguilera, X. Shortage of yellow fever vaccination: a travel medicine emergency for Chilean travellers. Travel Med. Infect. Dis. 28, 1–2 (2019).
    PubMed  Google Scholar 

    13.
    Gershman, M. D. et al. Addressing a yellow fever vaccine shortage—United States, 2016–2017. MMWR. Morb. Mortal. Wkly. Rep. 66, 457–459 (2017).
    PubMed  PubMed Central  Google Scholar 

    14.
    Barrett, A. D. T. Yellow fever in Angola and beyond—the problem of vaccine supply and demand. N. Engl. J. Med. 375, 301–303 (2016).
    PubMed  Google Scholar 

    15.
    Cunha, M. S. et al. Epizootics due to yellow fever Virus in São Paulo State, Brazil: viral dissemination to new areas (2016–2017). Sci. Rep. 9, 5474 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    16.
    Kraemer, M. U. G. et al. Spread of yellow fever virus outbreak in Angola and the Democratic Republic of the Congo 2015–16: a modelling study. Lancet Infect. Dis. 17, 330–338 (2017).
    PubMed  PubMed Central  Google Scholar 

    17.
    Couto-Lima, D. et al. Potential risk of re-emergence of urban transmission of yellow fever virus in Brazil facilitated by competent Aedes populations. Sci. Rep. 7, 4848 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    18.
    Hamlet, A. et al. The seasonal influence of climate and environment on yellow fever transmission across Africa. PLoS Negl. Trop. Dis. 12, e0006284 (2018).
    PubMed  PubMed Central  Google Scholar 

    19.
    Roiz, D. et al. Integrated Aedes management for the control of Aedes-borne diseases. PLoS Negl. Trop. Dis. 12, e0006845 (2018).
    PubMed  PubMed Central  Google Scholar 

    20.
    Trewin, B. J. et al. The elimination of the dengue vector, Aedes aegypti, from Brisbane, Australia: The role of surveillance, larval habitat removal and policy. PLoS Negl. Trop. Dis. 11, e0005848 (2017).
    PubMed  PubMed Central  Google Scholar 

    21.
    Wilson, A. L. et al. The importance of vector control for the control and elimination of vector-borne diseases. PLoS Negl. Trop. Dis. 14, e0007831 (2020).
    CAS  PubMed  PubMed Central  Google Scholar 

    22.
    Wilder-Smith, A. et al. Epidemic arboviral diseases: priorities for research and public health. Lancet Infect. Dis. 17, e101–e106 (2017).
    PubMed  Google Scholar 

    23.
    Kraemer, M. U. G. et al. The global compendium of Aedes aegypti and Ae. albopictus occurrence. Sci. Data 2, 150035 (2015).
    PubMed  PubMed Central  Google Scholar 

    24.
    Brown, J. E. et al. Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito. Evolution. 68, 514–525 (2014).
    CAS  PubMed  Google Scholar 

    25.
    Wilke, A. B. B., Beier, J. C. & Benelli, G. Complexity of the relationship between global warming and urbanization: an obscure future for predicting increases in vector-borne infectious diseases. Curr. Opin. Insect Sci. 35, 1–9 (2019).
    PubMed  Google Scholar 

    26.
    Wilke, A. B. B., Benelli, G. & Beier, J. C. Beyond frontiers: on invasive alien mosquito species in America and Europe. PLoS Negl. Trop. Dis. 14, e0007864 (2020).
    PubMed  PubMed Central  Google Scholar 

    27.
    Johnson, M. T. J. & Munshi-South, J. Evolution of life in urban environments. Science. 358, eaam8327 (2017).
    PubMed  Google Scholar 

    28.
    Knop, E. Biotic homogenization of three insect groups due to urbanization. Glob. Chang. Biol. 22, 228–236 (2016).
    ADS  PubMed  Google Scholar 

    29.
    McKinney, M. L. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260 (2006).
    Google Scholar 

    30.
    Gubler, D. J. Dengue, urbanization and globalization: the unholy trinity of the 21st Century. Trop. Med. Health 39, S3–S11 (2011).
    Google Scholar 

    31.
    Wilke, A. B. B. et al. Urbanization creates diverse aquatic habitats for immature mosquitoes in urban areas. Sci. Rep. 9, 15335 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    32.
    Stoddard, P. K. Managing Aedes aegypti populations in the first Zika transmission zones in the continental United States. Acta Trop. 187, 108–118 (2018).
    CAS  PubMed  Google Scholar 

    33.
    Estep, A. S. et al. Quantification of permethrin resistance and kdr alleles in Florida strains of Aedes aegypti (L.) and Aedes albopictus (Skuse). PLoS Negl. Trop. Dis. 12, e0006544 (2018).
    PubMed  PubMed Central  Google Scholar 

    34.
    Mundis, S. J., Estep, A. S., Waits, C. M. & Ryan, S. J. Spatial variation in the frequency of knockdown resistance genotypes in Florida Aedes aegypti populations. Parasit. Vectors 13, 241 (2020).
    CAS  PubMed  PubMed Central  Google Scholar 

    35.
    Achee, N. L. et al. Alternative strategies for mosquito-borne arbovirus control. PLoS Negl. Trop. Dis. 13, e0006822 (2019).
    PubMed  PubMed Central  Google Scholar 

    36.
    Wilke, A. B. B., Beier, J. C. & Benelli, G. Transgenic mosquitoes: fact or fiction?. Trends Parasitol. 34, 456–465 (2018).
    PubMed  Google Scholar 

    37.
    Koenraadt, C. J. M. et al. Spatial and temporal patterns in pupal and adult production of the dengue vector Aedes aegypti in Kamphaeng Phet Thailand. Am. J. Trop. Med. Hyg. 79, 230–238 (2008).
    PubMed  Google Scholar 

    38.
    Barnes, A., Tun-Lin, W. & Kay, B. H. Understanding productivity, a key to Aedes aegypti surveillance. Am. J. Trop. Med. Hyg. 53, 595–601 (1995).
    PubMed  Google Scholar 

    39.
    Maciel-de-Freitas, R., Marques, W. A., Peres, R. C., Cunha, S. P. & De Oliveira, R. L. Variation in Aedes aegypti (Diptera: Culicidae) container productivity in a slum and a suburban district of Rio de Janeiro during dry and wet seasons. Mem. Inst. Oswaldo Cruz 102, 489–496 (2007).
    PubMed  Google Scholar 

    40.
    Powell, J. R. & Tabachnick, W. J. History of domestication and spread of Aedes aegypti: a review. Mem. Inst. Oswaldo Cruz 108, 11–17 (2013).
    PubMed  PubMed Central  Google Scholar 

    41.
    Paul, K. K. et al. Risk factors for the presence of dengue vector mosquitoes, and determinants of their prevalence and larval site selection in Dhaka Bangladesh. PLoS ONE 13, 1–19 (2018).
    Google Scholar 

    42.
    Johnson, T. L. et al. Modeling the environmental suitability for Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in the Contiguous United States. J. Med. Entomol. 54, 1605–1614 (2017).
    PubMed  PubMed Central  Google Scholar 

    43.
    Paploski, I. A. D. et al. Storm drains as larval development and adult resting sites for Aedes aegypti and Aedes albopictus in Salvador Brazil. Parasit. Vectors 9, 1–8 (2016).
    Google Scholar 

    44.
    Souza, R. L. et al. Effect of an intervention in storm drains to prevent Aedes aegypti reproduction in Salvador Brazil. Parasit. Vectors 10, 1–6 (2017).
    Google Scholar 

    45.
    WHO. Multi-country study of Aedes aegypti pupal productivity survey methodology: findings and recommendations. Available at: https://www.who.int/tdr/publications/documents/aedes_aegypti.pdf (2006).

    46.
    WHO. A Review of Entomological Sampling Methods and Indicators for Dengue Vectors. Available at: https://apps.who.int/iris/bitstream/handle/10665/68575/TDR_IDE_DEN_03.1.pdf;jsessionid=FAA7E1FD4786376A60693A419CA43B5F?sequence=1 (2003).

    47.
    Dowling, Z., Ladeau, S. L., Armbruster, P., Biehler, D. & Leisnham, P. T. Socioeconomic status affects mosquito (Diptera: Culicidae) larval habitat type availability and infestation level. J. Med. Entomol. 50, 764–772 (2013).
    PubMed  Google Scholar 

    48.
    Wilke, A. B. B. et al. Community composition and year-round abundance of vector species of mosquitoes make Miami-Dade County, Florida a receptive gateway for arbovirus entry to the United States. Sci. Rep. 9, 8732 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    49.
    da Cruz Ferreira, D. A. et al. Meteorological variables and mosquito monitoring are good predictors for infestation trends of Aedes aegypti, the vector of dengue, chikungunya and Zika. Parasit. Vectors 10, 78 (2017).
    PubMed  PubMed Central  Google Scholar 

    50.
    Dunphy, B. M. et al. Long-term surveillance defines spatial and temporal patterns implicating Culex tarsalis as the primary vector of West Nile virus. Sci. Rep. 9, 1–10 (2019).
    Google Scholar 

    51.
    Wilk-da-silva, R. et al. Wing morphometric variability in Aedes aegypti (Diptera: Culicidae) from different urban built environments. Parasit. Vectors 11, 561 (2018).
    PubMed  PubMed Central  Google Scholar 

    52.
    Wilke, A. B. B., Wilk-da-Silva, R. & Marrelli, M. T. Microgeographic population structuring of Aedes aegypti (Diptera: Culicidae). PLoS ONE 12, e0185150 (2017).
    PubMed  PubMed Central  Google Scholar 

    53.
    Medley, K. A., Westby, K. M. & Jenkins, D. G. Rapid local adaptation to northern winters in the invasive Asian tiger mosquito Aedes albopictus: a moving target. J. Appl. Ecol. 56, 2518–2527 (2019).
    Google Scholar 

    54.
    Pichler, V. et al. Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe. PLoS Negl. Trop. Dis. 13, e0007554 (2019).
    PubMed  PubMed Central  Google Scholar 

    55.
    Wilke, A. B. B., Vasquez, C., Mauriello, P. J. & Beier, J. C. Ornamental bromeliads of Miami-Dade County, Florida are important breeding sites for Aedes aegypti (Diptera: Culicidae). Parasit. Vectors 11, 283 (2018).
    PubMed  PubMed Central  Google Scholar 

    56.
    Santos, C. B., Leite, G. R. & Falqueto, A. Does native bromeliads represent important breeding sites for Aedes aegypti (L.) (Diptera: Culicidae) in urbanized areas? Neotrop. Entomol. 40, 278–281 (2011).
    CAS  PubMed  Google Scholar 

    57.
    Mocellin, M. G. et al. Bromeliad-inhabiting mosquitoes in an urban botanical garden of dengue endemic Rio de Janeiro—are bromeliads productive habitats for the invasive vectors Aedes aegypti and Aedes albopictus?. Mem. Inst. Oswaldo Cruz 104, 1171–1176 (2009).
    PubMed  PubMed Central  Google Scholar 

    58.
    Ceretti-Junior, W. et al. Species composition and ecological aspects of immature mosquitoes (Diptera: Culicidae) in Bromeliads in urban parks in the City of São Paulo Brazil. J. Arthropod. Borne. Dis. 10, 102–112 (2016).
    PubMed  Google Scholar 

    59.
    Chitolina, R. F., Anjos, F. A., Lima, T. S., Castro, E. A. & Costa-Ribeiro, M. C. V. Raw sewage as breeding site to Aedes (Stegomyia) aegypti (Diptera, culicidae). Acta Trop. 164, 290–296 (2016).
    CAS  PubMed  Google Scholar 

    60.
    Che-Mendoza, A. et al. Operational guide for assessing the productivity of Aedes aegypti breeding sites. World Heal. Organ. 1, 1–30 (2011).
    Google Scholar 

    61.
    MacCormack-Gelles, B., Lima Neto, A. S. & Sousa, G. S. Evaluation of the usefulness of Aedes aegypti rapid larval surveys to anticipate seasonal dengue transmission between 2012–2015 in Fortaleza. Brazil. Acta Trop. 205, 105391 (2020).
    PubMed  Google Scholar 

    62.
    Islam, S., Haque, C. E., Hossain, S. & Rochon, K. Role of container type, behavioural, and ecological factors in Aedes pupal production in Dhaka, Bangladesh: an application of zero-inflated negative binomial model. Acta Trop. 193, 50–59 (2019).
    PubMed  Google Scholar 

    63.
    Wilke, A. B. B. et al. Mosquito adaptation to the extreme habitats of urban construction sites. Trends Parasitol. 35, 607–614 (2019).
    PubMed  Google Scholar 

    64.
    Ajelli, M. et al. Host outdoor exposure variability affects the transmission and spread of Zika virus: Insights for epidemic control. PLoS Negl. Trop. Dis. 11, e0005851 (2017).
    PubMed  PubMed Central  Google Scholar 

    65.
    Mutebi, J.-P. et al. Zika virus MB16-23 in mosquitoes, Miami-Dade County, Florida, USA, 2016. Emerg. Infect. Dis. 24, 808–810 (2018).
    PubMed Central  Google Scholar 

    66.
    Wilke, A. B. B., Carvajal, A., Vasquez, C., Petrie, W. D. & Beier, J. C. Urban farms in Miami-Dade county, Florida have favorable environments for vector mosquitoes. PLoS ONE 15, e0230825 (2020).
    CAS  PubMed  PubMed Central  Google Scholar 

    67.
    Paules, C. I. & Fauci, A. S. Yellow fever—once again on the radar screen in the Americas. N. Engl. J. Med. 376, 1397–1399 (2017).
    PubMed  Google Scholar 

    68.
    Abdul-Ghani, R. et al. Impact of population displacement and forced movements on the transmission and outbreaks of Aedes-borne viral diseases: Dengue as a model. Acta Trop. 197, 105066 (2019).
    PubMed  Google Scholar 

    69.
    PAHO. Reported Cases of Dengue Fever in The Americas. Pan-American Health Organization. Available at: http://www.paho.org/data/index.php/en/mnu-topics/indicadores-dengue-en/dengue-nacional-en/252-dengue-pais-ano-en.html.

    70.
    Poletti, P. et al. Transmission potential of chikungunya virus and control measures: the case of Italy. PLoS ONE 6, e18860 (2011).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    71.
    Gould, E. A., Gallian, P., De Lamballerie, X. & Charrel, R. N. First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality!. Clin. Microbiol. Infect. 16, 1702–1704 (2010).
    CAS  PubMed  Google Scholar 

    72.
    Gjenero-Margan, I. et al. Autochthonous dengue fever in Croatia, August–September 2010. Euro Surveill 16, 1–4 (2011).
    Google Scholar 

    73.
    Rosenberg, R. et al. Vital signs: trends in reported vectorborne disease cases—United States and Territories, 2004–2016. MMWR. Morb. Mortal. Wkly. Rep. 67, 496–501 (2018).
    PubMed  PubMed Central  Google Scholar 

    74.
    Bureau of Transportation Statistics. 2016 Annual and December U.S. Airline Traffic Data. Available at: https://www.bts.gov/newsroom/2017-traffic-data-us-airlines-and-foreign-airlines-us-flights (2017).

    75.
    International Air Transport Association. Worldwide annual air passenger numbers. Available at: https://www.iata.org/pressroom/pr/Pages/2018-09-06-01.aspx (2017).

    76.
    Likos, A. et al. Local mosquito-borne transmission of Zika Virus—Miami-Dade and Broward Counties, Florida, June–August 2016. MMWR. Morb. Mortal. Wkly. Rep. 65, 1032–1038 (2016).
    PubMed  Google Scholar 

    77.
    Centers for Disease Control and Prevention. Imported Human disease cases Reported to CDC by county of residence. Available at: https://wwwn.cdc.gov/arbonet/Maps/ADB_Diseases_Map/index.html (2020).

    78.
    Florida Department of Health. Mosquito-Borne Illness Advisory. Available at: http://miamidade.floridahealth.gov/_newsroom/2019/_documents/2019-12-23-advisory.pdf (2019).

    79.
    Wilke, A. B. B., Vasquez, C., Petrie, W., Caban-Martinez, A. J. & Beier, J. C. Construction sites in Miami-Dade County, Florida are highly favorable environments for vector mosquitoes. PLoS ONE 13, e0209625 (2018).
    CAS  PubMed  PubMed Central  Google Scholar 

    80.
    Wilke, A. B. B., Vasquez, C., Petrie, W. & Beier, J. C. Tire shops in Miami-Dade County, Florida are important producers of vector mosquitoes. PLoS ONE 14, e0217177 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    81.
    Wilke, A. B. B. et al. Cemeteries in Miami-Dade County, Florida are important areas to be targeted in mosquito management and control efforts. PLoS ONE 15, e0230748 (2020).
    CAS  PubMed  PubMed Central  Google Scholar 

    82.
    Darsie, Jr., R. F. & Morris, C. D. Keys to the Adult Females and Fourth Instar Larvae of the Mosquitoes of Florida (Diptera, Culicidae). Technical Bulletin of the Florida Mosquito Control Association vol. 1 (Bulletin of the Florida mosquito control association, 2000).

    83.
    Tobin, J. Estimation of relationships for limited dependent variables. Econometrica 26, 24 (1958).
    MathSciNet  MATH  Google Scholar 

    84.
    McDonald, J. F. & Moffitt, R. A. The uses of tobit analysis. Rev. Econ. Stat. 62, 318 (1980).
    Google Scholar 

    85.
    Yee, D. A. Tires as habitats for mosquitoes: a review of studies within the Eastern United States: Table 1. J. Med. Entomol. 45, 581–593 (2008).
    PubMed  Google Scholar 

    86.
    Reiter, P. & Sprenger, D. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. J. Am. Mosq. Control Assoc. 3, 494–501 (1987).
    CAS  PubMed  Google Scholar 

    87.
    Dinh, E. T. N. & Novak, R. J. Diversity and abundance of mosquitoes inhabiting waste tires in a subtropical swamp in urban Florida. J. Am. Mosq. Control Assoc. 34, 47–49 (2018).
    PubMed  Google Scholar  More

  • in

    Author Correction: Remote sensing northern lake methane ebullition

    Author notes
    A. Serafimovich
    Present address: Deutscher Wetterdienst, Offenbach, Germany

    Affiliations

    Water and Environmental Research Center, University of Alaska Fairbanks, Fairbanks, AK, USA
    M. Engram & K. M. Walter Anthony

    International Arctic Research Center, University of Alaska Fairbanks, Fairbanks, AK, USA
    K. M. Walter Anthony

    GFZ German Research Centre for Geosciences, Potsdam, Germany
    T. Sachs, K. Kohnert & A. Serafimovich

    Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany
    K. Kohnert

    Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Permafrost Research Center, Potsdam, Germany
    G. Grosse

    Institute of Geosciences, University of Potsdam, Potsdam, Germany
    G. Grosse

    Geophysical Institute, University of Alaska Fairbanks, Fairbanks, AK, USA
    F. J. Meyer

    Authors
    M. Engram

    K. M. Walter Anthony

    T. Sachs

    K. Kohnert

    A. Serafimovich

    G. Grosse

    F. J. Meyer

    Corresponding author
    Correspondence to M. Engram. More

  • in

    Assessing the response of micro-eukaryotic diversity to the Great Acceleration using lake sedimentary DNA

    1.
    Adrian, R. et al. Lakes as sentinels of climate change. Limnol. Oceanogr. 54, 2283–2297 (2009).
    ADS  PubMed  PubMed Central  Google Scholar 
    2.
    Keeler, B. L. et al. Linking water quality and well-being for improved assessment and valuation of ecosystem services. Proc. Natl Acad. Sci. USA 109, 18619–18624 (2012).
    ADS  CAS  PubMed  Google Scholar 

    3.
    Reid, A. J. et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. 94, 849–873 (2019).
    PubMed  Google Scholar 

    4.
    Jenny, J.-P. et al. Human and climate global-scale imprint on sediment transfer during the Holocene. Proc. Natl Acad. Sci. USA 116, 22972–22976 (2019).
    ADS  CAS  PubMed  Google Scholar 

    5.
    Boyle, J. F., Chiverrell, R. C., Davies, H. & Alderson, D. M. An approach to modelling the impact of prehistoric farming on Holocene landscape phosphorus dynamics. Holocene 25, 203–214 (2015).
    ADS  Google Scholar 

    6.
    Steffen, W., Crutzen, P. J. & McNeill, J. R. The anthropocene: are humans now overwhelming the great forces of nature. AMBIO J. Hum. Environ. 36, 614–621 (2007).
    CAS  Google Scholar 

    7.
    Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O. & Ludwig, C. The trajectory of the anthropocene: the great acceleration. Anthr. Rev. 2, 81–98 (2015).
    Google Scholar 

    8.
    Lewis, S. L. & Maslin, M. A. Defining the anthropocene. Nature 519, 171–180 (2015).
    ADS  CAS  PubMed  Google Scholar 

    9.
    Jenny, J.-P. et al. Urban point sources of nutrients were the leading cause for the historical spread of hypoxia across European lakes. Proc. Natl Acad. Sci. USA 113, 12655–12660 (2016).
    CAS  PubMed  Google Scholar 

    10.
    O’Beirne, M. D. et al. Anthropogenic climate change has altered primary productivity in Lake Superior. Nat. Commun. 8, 15713 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    11.
    Smol, J. P. Under the radar: long-term perspectives on ecological changes in lakes. Proc. R. Soc. B Biol. Sci. 286, 20190834 (2019).
    CAS  Google Scholar 

    12.
    Payne, R. J. Seven reasons why protists make useful bioindicators. Acta Protozool. 52, 105–113 (2013).

    13.
    Domaizon, I., Winegardner, A., Capo, E., Gauthier, J. & Gregory-Eaves, I. DNA-based methods in paleolimnology: new opportunities for investigating long-term dynamics of lacustrine biodiversity. J. Paleolimnol. 58, 1–21 (2017).
    ADS  Google Scholar 

    14.
    Gilbert, M. T. P., Bandelt, H.-J., Hofreiter, M. & Barnes, I. Assessing ancient DNA studies. Trends Ecol. Evol. 20, 541–544 (2005).
    PubMed  Google Scholar 

    15.
    Pedersen, M. W. et al. Ancient and modern environmental DNA. Philos. Trans. R. Soc. B Biol. Sci. 370, 20130383 (2015).
    Google Scholar 

    16.
    Coolen, M. J. L. et al. Evolution of the plankton paleome in the Black Sea from the Deglacial to Anthropocene. Proc. Natl Acad. Sci. USA 110, 8609–8614 (2013).
    ADS  CAS  PubMed  Google Scholar 

    17.
    Capo, E. et al. Long-term dynamics in microbial eukaryotes communities: a palaeolimnological view based on sedimentary DNA. Mol. Ecol. 25, 5925–5943 (2016).
    CAS  PubMed  Google Scholar 

    18.
    Capo, E. et al. Tracking a century of changes in microbial eukaryotic diversity in lakes driven by nutrient enrichment and climate warming. Environ. Microbiol. 19, 2873–2892 (2017).
    CAS  PubMed  Google Scholar 

    19.
    Capo, E. et al. How does environmental inter-annual variability shape aquatic microbial communities? A 40-year annual record of sedimentary DNA from a Boreal Lake (Nylandssjön, Sweden). Front. Ecol. Evol. 7, 245 (2019).
    ADS  Google Scholar 

    20.
    Coolen, M. J. L. et al. Combined DNA and lipid analyses of sediments reveal changes in Holocene haptophyte and diatom populations in an Antarctic lake. Earth Planet. Sci. Lett. 223, 225–239 (2004).
    ADS  CAS  Google Scholar 

    21.
    Boere, A. C. et al. Late-Holocene succession of dinoflagellates in an Antarctic fjord using a multi-proxy approach: paleoenvironmental genomics, lipid biomarkers and palynomorphs. Geobiology 7, 265–281 (2009).
    CAS  PubMed  Google Scholar 

    22.
    Kopf, R. K., Finlayson, C. M., Humphries, P., Sims, N. C. & Hladyz, S. Anthropocene baselines: assessing change and managing biodiversity in human-dominated aquatic ecosystems. BioScience 65, 798–811 (2015).
    Google Scholar 

    23.
    Smol, J. P. Pollution of Lakes and Rivers: A Paleoenvironmental Perspective (Wiley-Blackwell, 2008).

    24.
    McGill, B. J., Dornelas, M., Gotelli, N. J. & Magurran, A. E. Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol. Evol. 30, 104–113 (2015).
    PubMed  Google Scholar 

    25.
    Adl, S. M. et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66, 4–119 (2019).
    PubMed  PubMed Central  Google Scholar 

    26.
    Dornelas, M. et al. Assemblage Time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).
    ADS  CAS  PubMed  Google Scholar 

    27.
    Charles, S. C. The value of microorganisms. Environ. Ethics 27, 375–390 (2005).
    Google Scholar 

    28.
    Bodelier, P. Toward understanding, managing, and protecting microbial ecosystems. Front. Microbiol. 2, 1–8 (2011).
    Google Scholar 

    29.
    Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl Acad. Sci. USA 105, 11512–11519 (2008).
    ADS  CAS  PubMed  Google Scholar 

    30.
    Woodward, G., Perkins, D. M. & Brown, L. E. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos. Trans. R. Soc. B Biol. Sci. 365, 2093–2106 (2010).
    Google Scholar 

    31.
    Nogués-Bravo, D., Araújo, M. B., Romdal, T. & Rahbek, C. Scale effects and human impact on the elevational species richness gradients. Nature 453, 216–219 (2008).
    ADS  PubMed  Google Scholar 

    32.
    Leu, M., Hanser, S. E. & Knick, S. T. The human footprint in the West: a large-scale analysis of anthropogenic impacts. Ecol. Appl. 18, 1119–1139 (2008).
    PubMed  Google Scholar 

    33.
    Müller, B., Lotter, A. F., Sturm, M. & Ammann, A. Influence of catchment quality and altitude on the water and sediment composition of 68 small lakes in Central Europe. Aquat. Sci. 60, 316–337 (1998).
    Google Scholar 

    34.
    Weckström, K. et al. Impacts of climate warming on Alpine lake biota over the past decade. Arct. Antarct. Alp. Res. 48, 361–376 (2016).
    Google Scholar 

    35.
    Sadro, S., Melack, J. M., Sickman, J. O. & Skeen, K. Climate warming response of mountain lakes affected by variations in snow. Limnol. Oceanogr. Lett. 4, 9–17 (2019).
    Google Scholar 

    36.
    More, K. D., Giosan, L., Grice, K. & Coolen, M. J. L. Holocene paleodepositional changes reflected in the sedimentary microbiome of the Black Sea. Geobiology 17, 436–448 (2019).
    PubMed  Google Scholar 

    37.
    Li, F., Zhang, X., Xie, Y. & Wang, J. Sedimentary DNA reveals over 150 years of ecosystem change by human activities in Lake Chao, China. Environ. Int. 133, 105214 (2019).
    CAS  PubMed  Google Scholar 

    38.
    Jones, J. & Brett, M. T. in Global Environmental Change (ed. Freedman, B.) 273–279 (Springer Netherlands, 2014).

    39.
    De Senerpont Domis, L. N., Van de Waal, D. B., Helmsing, N. R., Van Donk, E. & Mooij, WolfM. Community stoichiometry in a changing world: combined effects of warming and eutrophication on phytoplankton dynamics. Ecology 95, 1485–1495 (2014).
    Google Scholar 

    40.
    Paerl, H. W. & Huisman, J. Blooms like it hot. Science 320, 57–58 (2008).
    CAS  PubMed  Google Scholar 

    41.
    Schindler, D. E., Carpenter, S. R., Cole, J. J., Kitchell, J. F. & Pace, M. L. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277, 248–251 (1997).
    CAS  Google Scholar 

    42.
    Anderson, N. J., Heathcote, A. J. & Engstrom, D. R., Globocarb Data Contributors. Anthropogenic alteration of nutrient supply increases the global freshwater carbon sink. Sci. Adv. 6, eaaw2145 (2020).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    43.
    Laplace-Treyture, C. & Feret, T. Performance of the Phytoplankton Index for Lakes (IPLAC): a multimetric phytoplankton index to assess the ecological status of water bodies in France. Ecol. Indic. 69, 686–698 (2016).
    CAS  Google Scholar 

    44.
    Carpenter, S. R. Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proc. Natl Acad. Sci. USA 102, 10002–10005 (2005).
    ADS  CAS  PubMed  Google Scholar 

    45.
    Jensen, J. P., Jeppesen, E., Olrik, K. & Kristensen, P. Impact of nutrients and physical factors on the shift from cyanobacterial to chlorophyte dominance in shallow Danish Lakes. Can. J. Fish. Aquat. Sci. 51, 1692–1699 (1994).
    Google Scholar 

    46.
    Naselli-Flores, L. & Barone, R. Phytoplankton dynamics and structure: a comparative analysis in natural and man-made water bodies of different trophic state. Hydrobiologia 438, 65–74 (2000).
    CAS  Google Scholar 

    47.
    Fee, E. J. A relation between lake morphometry and primary productivity and its use in interpreting whole-lake eutrophication experiments. Limnol. Oceanogr. 24, 401–416 (1979).
    ADS  CAS  Google Scholar 

    48.
    Engstrom, D. R., Schottler, S. P., Leavitt, P. R. & Havens, K. E. A reevaluation of the cultural eutrophication of Lake Okeechobee using multiproxy sediment records. Ecol. Appl. 16, 1194–1206 (2006).
    PubMed  Google Scholar 

    49.
    Londeix, L., Herreyre, Y., Turon, J.-L. & Fletcher, W. Last glacial to holocene hydrology of the Marmara Sea inferred from a dinoflagellate cyst record. Rev. Palaeobot. Palynol. 158, 52–71 (2009).
    Google Scholar 

    50.
    Waibel, A., Peter, H. & Sommaruga, R. Importance of mixotrophic flagellates during the ice-free season in lakes located along an elevational gradient. Aquat. Sci. 81, 45 (2019).
    PubMed  PubMed Central  Google Scholar 

    51.
    Edwards, K. F. Mixotrophy in nanoflagellates across environmental gradients in the ocean. Proc. Natl Acad. Sci. USA 116, 6211–6220 (2019).
    CAS  PubMed  Google Scholar 

    52.
    Magurran, A. E., Dornelas, M., Moyes, F., Gotelli, N. J. & McGill, B. Rapid biotic homogenization of marine fish assemblages. Nat. Commun. 6, 8405 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    53.
    Knop, E. Biotic homogenization of three insect groups due to urbanization. Glob. Change Biol. 22, 228–236 (2016).
    ADS  Google Scholar 

    54.
    Rahel, F. J. Homogenization of fish faunas across the United States. Science 288, 854–856 (2000).
    ADS  CAS  PubMed  Google Scholar 

    55.
    Nielsen, T. F., Sand‐Jensen, K., Dornelas, M. & Bruun, H. H. More is less: net gain in species richness, but biotic homogenization over 140 years. Ecol. Lett. 22, 1650–1657 (2019).
    Google Scholar 

    56.
    Petsch, D. K. Causes and consequences of biotic homogenization in freshwater ecosystems. Int. Rev. Hydrobiol. 101, 113–122 (2016).
    Google Scholar 

    57.
    Monchamp, M.-E. et al. Homogenization of lake cyanobacterial communities over a century of climate change and eutrophication. Nat. Ecol. Evol. 2, 317 (2018).
    PubMed  Google Scholar 

    58.
    Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6, 8568 (2015).
    ADS  PubMed  PubMed Central  Google Scholar 

    59.
    Litchman, E. Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems: Invasive microbes. Ecol. Lett. 13, 1560–1572 (2010).
    PubMed  Google Scholar 

    60.
    Wilkinson, D. M. Have we underestimated the importance of humans in the biogeography of free-living terrestrial microorganisms? J. Biogeogr. 37, 393–397 (2010).
    Google Scholar 

    61.
    Jenny, J.-P. et al. Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Glob. Change Biol. 22, 1481–1489 (2016).
    ADS  Google Scholar 

    62.
    Birks, H. H. & Birks, H. J. B. Multi-proxy studies in palaeolimnology. Veg. Hist. Archaeobot. 15, 235–251 (2006).
    Google Scholar 

    63.
    Gast, R. J., Dennett, M. R. & Caron, D. A. Characterization of Protistan assemblages in the Ross Sea, Antarctica, by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 70, 2028–2037 (2004).
    CAS  PubMed  PubMed Central  Google Scholar 

    64.
    Van de Peer, Y., De Rijk, P., Wuyts, J., Winkelmans, T. & De Wachter, R. The European small subunit ribosomal RNA database. Nucleic Acids Res. 28, 175–176 (2000).
    PubMed  PubMed Central  Google Scholar 

    65.
    Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).
    PubMed  PubMed Central  Google Scholar 

    66.
    Mangot, J.-F. et al. Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes: Short-term dynamics of small eukaryotes. Environ. Microbiol. 15, 1745–1758 (2013).
    CAS  PubMed  Google Scholar 

    67.
    Taib, N., Mangot, J.-F., Domaizon, I., Bronner, G. & Debroas, D. Phylogenetic affiliation of SSU rRNA genes generated by massively parallel sequencing: new insights into the freshwater protist diversity. PLoS ONE 8, e58950 (2013).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    68.
    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).
    CAS  PubMed  PubMed Central  Google Scholar 

    69.
    Guillou, L. et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604 (2013).
    CAS  PubMed  Google Scholar 

    70.
    McKnight, D. T. et al. Methods for normalizing microbiome data: an ecological perspective. Methods Ecol. Evol. 10, 389–400 (2019).
    Google Scholar 

    71.
    Oksanen, J. et al. vegan: Community Ecology Package. R package version 1.17–10 (2011).

    72.
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 

    73.
    Anderson, M. J. Distance-Based Tests for Homogeneity of Multivariate Dispersions. Biometrics 62, 245–253 (2006).
    MathSciNet  PubMed  MATH  Google Scholar 

    74.
    Therneau, T., Atkinson, B. & Ripley, B. (2019). rpart: Recursive Partitioning and Regression Trees. R package version 4.1–13. (2018).

    75.
    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
    PubMed  PubMed Central  Google Scholar  More

  • in

    Intermittent meromixis controls the trophic state of warming deep lakes

    1.
    Smith, V. H. & Schindler, D. W. Eutrophication science: where do we go from here?. Trends Ecol. Evol. 24, 201–207 (2009).
    PubMed  Google Scholar 
    2.
    Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).
    PubMed  Google Scholar 

    3.
    Carpenter, S. et al. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. Appl. 8, 559–568 (1998).
    Google Scholar 

    4.
    Cohen, A. S. et al. Climate warming reduces fish production and benthic habitat in Lake Tanganyika, one of the most biodiverse freshwater ecosystems. Proc. Natl. Acad. Sci. 113, 9563–9568 (2016).
    ADS  CAS  PubMed  Google Scholar 

    5.
    Fernández, J. E., Peeters, F. & Hofmann, H. Importance of the autumn overturn and anoxic conditions in the hypolimnion for the annual methane emissions from a temperate lake. Environ. Sci. Technol. 48, 7297–7304 (2014).
    ADS  Google Scholar 

    6.
    Friedrich, J. et al. Investigating hypoxia in aquatic environments: diverse approaches to addressing a complex phenomenon. Biogeosciences 11, 1215–1259 (2014).
    ADS  Google Scholar 

    7.
    Vollenweider, R. A. Advances in Defining Critical Loading Levels for Phosphorus in Lake Eutrophication (Mem. dell’Istituto Ital. di Idrobiol. Dott, Marco Marchi Verbania Pallanza, 1976).
    Google Scholar 

    8.
    Jenny, J.-P. et al. Inherited hypoxia: a new challenge for reoligotrophicated lakes under global warming. Glob. Biogeochem. Cycles 28, 1413–1423 (2014).
    ADS  CAS  Google Scholar 

    9.
    Matzinger, A. et al. Eutrophication of ancient Lake Ohrid: global warming amplifies detrimental effects of increased nutrient inputs. Limnol. Oceanogr. 52, 338–353 (2007).
    ADS  CAS  Google Scholar 

    10.
    Meire, L., Soetaert, K. E. R. & Meysman, F. J. R. Impact of global change on coastal oxygen dynamics and risk of hypoxia. Biogeosciences 10, 2633–2653 (2013).
    ADS  CAS  Google Scholar 

    11.
    Pachauri, R. K. et al. Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change (IPCC, 2014).

    12.
    O’Reilly, C. M. et al. Rapid and highly variable warming of lake surface waters around the globe. Geophys. Res. Lett. 42, 10773–10781 (2015).
    ADS  Google Scholar 

    13.
    Schmid, M., Hunziker, S. & Wüest, A. Lake surface temperatures in a changing climate: a global sensitivity analysis. Clim. Change 124, 301–315 (2014).
    ADS  Google Scholar 

    14.
    Paerl, H. W. & Huisman, J. Blooms like it hot. Science 320, 57–58 (2008).
    CAS  Google Scholar 

    15.
    Müller, B., Bryant, L. D., Matzinger, A. & Wüest, A. Hypolimnetic oxygen depletion in eutrophic lakes. Environ. Sci. Technol. 46, 9964–9971 (2012).
    PubMed  Google Scholar 

    16.
    Adrian, R. et al. Lakes as sentinels of climate change. Limnol. Oceanogr. 54, 2283–2297 (2009).
    ADS  PubMed  PubMed Central  Google Scholar 

    17.
    Butcher, J. B., Nover, D., Johnson, T. E. & Clark, C. M. Sensitivity of lake thermal and mixing dynamics to climate change. Clim. Change 129, 295–305 (2015).
    ADS  CAS  Google Scholar 

    18.
    Kirillin, G. Modeling the impact of global warming on water temperature and seasonal mixing regimes in small temperate lakes. Boreal Environ. Res. 15, 279–293 (2010).
    Google Scholar 

    19.
    Straile, D., Jöhnk, K. & Rossknecht, H. Complex effects of winter warming on the physicochemical characteristics of a deep lake. Limnol. Oceanogr. 48, 1432–1438 (2003).
    ADS  CAS  Google Scholar 

    20.
    Woolway, R. I. & Merchant, C. J. Worldwide alteration of lake mixing regimes in response to climate change. Nat. Geosci. 12, 271–276 (2019).
    ADS  CAS  Google Scholar 

    21.
    Boehrer, B., Fukuyama, R. & Chikita, K. Stratification of very deep, thermally stratified lakes. Geophys. Res. Lett. 35, 8–12 (2008).
    Google Scholar 

    22.
    Boehrer, B. & Schultze, M. Stratification of lakes. Rev. Geophys. 46, 1–27 (2008).
    Google Scholar 

    23.
    Boehrer, B., Rohden, C. Von & Schultze, M. Ecology of Meromictic Lakes. 228 (2017).

    24.
    Hall, K. J. & Northcote, T. G. Meromictic lakes. In Encyclopedia of Lakes and Reservoirs 519–524 (Springer, 2012).

    25.
    Søndergaard, M., Jensen, J. P. & Jeppesen, E. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506–509, 135–145 (2003).
    Google Scholar 

    26.
    Hupfer, M. & Lewandowski, J. Oxygen controls the phosphorus release from lake sediments—a long-lasting paradigm in limnology. Int. Rev. Hydrobiol. 93, 415–432 (2008).
    CAS  Google Scholar 

    27.
    Yankova, Y., Neuenschwander, S., Köster, O. & Posch, T. Abrupt stop of deep water turnover with lake warming: drastic consequences for algal primary producers. Sci. Rep. 7, 13770 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    28.
    Lehmann, M. et al. Powering up the “biogeochemical engine”: the impact of exceptional ventilation of a deep meromictic lake on the lacustrine redox, nutrient, and methane balances. Front. Earth Sci. 3, 45 (2015).
    ADS  Google Scholar 

    29.
    Anneville, O., Gammeter, S. & Straile, D. Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshw. Biol. 50, 1731–1746 (2005).
    CAS  Google Scholar 

    30.
    Posch, T., Köster, O., Salcher, M. M. & Pernthaler, J. Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat. Clim. Change 2, 809 (2012).
    ADS  CAS  Google Scholar 

    31.
    Winder, M. Lake warming mimics fertilization. Nat. Clim. Change 2, 771 (2012).
    ADS  CAS  Google Scholar 

    32.
    Coats, R., Perez-Losada, J., Schladow, G., Richards, R. & Goldman, C. The warming of Lake Tahoe. Clim. Change 76, 121–148 (2006).
    ADS  Google Scholar 

    33.
    Kraemer, B. M. et al. Morphometry and average temperature affect lake stratification responses to climate change. Geophys. Res. Lett. 42, 4981–4988 (2015).
    ADS  Google Scholar 

    34.
    Verburg, P., Hecky, R. E. & Kling, H. Ecological consequences of a century of warming in Lake Tanganyika. Science 301, 505–507 (2003).
    ADS  CAS  PubMed  Google Scholar 

    35.
    North, R. P., North, R. L., Livingstone, D. M., Köster, O. & Kipfer, R. Long-term changes in hypoxia and soluble reactive phosphorus in the hypolimnion of a large temperate lake: consequences of a climate regime shift. Glob. Change Biol. 20, 811–823 (2014).
    ADS  Google Scholar 

    36.
    Salmaso, N. Effects of climatic fluctuations and vertical mixing on the interannual trophic variability of Lake Garda, Italy. Limnol. Oceanogr. 50, 553–565 (2005).
    ADS  Google Scholar 

    37.
    Kõiv, T., Nõges, T. & Laas, A. Phosphorus retention as a function of external loading, hydraulic turnover time, area and relative depth in 54 lakes and reservoirs. Hydrobiologia 660, 105–115 (2011).
    Google Scholar 

    38.
    Walker, K. F. & Likens, G. E. Meromixis and a reconsidered typology of lake circulation patterns. Int. Vereinigung für Theor. und Angew. Limnol. Verhandlungen 19, 442–458 (1975).
    Google Scholar 

    39.
    Rogora, M. et al. Climatic effects on vertical mixing and deep-water oxygen content in the subalpine lakes in Italy. Hydrobiologia https://doi.org/10.1007/s10750-018-3623-y (2018).
    Article  Google Scholar 

    40.
    Valerio, G., Pilotti, M., Barontini, S. & Leoni, B. Sensitivity of the multiannual thermal dynamics of a deep pre-alpine lake to climatic change. Hydrol. Process. 29, 767–779 (2015).
    ADS  Google Scholar 

    41.
    Rapuc, W. et al. Holocene-long record of flood frequency in the Southern Alps (Lake Iseo, Italy) under human and climate forcing. Glob. Planet. Change 175, 160–172 (2019).
    ADS  Google Scholar 

    42.
    Gächter, R. & Müller, B. Why the phosphorus retention of lakes does not necessarily depend on the oxygen supply to their sediment surface. Limnol. Oceanogr. 48, 929–933 (2003).
    ADS  Google Scholar 

    43.
    Katsev, S. & Dittrich, M. Modeling of decadal scale phosphorus retention in lake sediment under varying redox conditions. Ecol. Model. 251, 246–259 (2013).
    CAS  Google Scholar 

    44.
    Garibaldi, L., Mezzanotte, V., Brizzio, M. C., Rogora, M. & Mosello, R. The trophic evolution of Lake Iseo as related to its holomixis. J. Limnol. 58, 10 (1999).
    Google Scholar 

    45.
    Leoni, B. et al. Long-term studies for evaluating the impacts of natural and anthropic stressors on limnological features and the ecosystem quality of Lake Iseo. Adv. Oceanogr. Limnol. https://doi.org/10.4081/aiol.2019.8622 (2019).
    Article  Google Scholar 

    46.
    Wilhelm, S. & Adrian, R. Impact of summer warming on the thermal characteristics of a polymictic lake and consequences for oxygen, nutrients and phytoplankton. Freshw. Biol. 53, 226–237 (2008).
    CAS  Google Scholar 

    47.
    Pilotti, M., Valerio, G. & Leoni, B. Data set for hydrodynamic lake model calibration: a deep prealpine case. Water Resour. Res. 49, 7159–7163 (2013).
    ADS  Google Scholar 

    48.
    Hutchinson, G. E. Treatise on limnology; geography, physics of lakes. In Treatise on Limnology; Geography, Physics of Lakes (Wiley, New York, 1975).

    49.
    Livingstone, D. M. A change of climate provokes a change of paradigm: taking leave of two tacit assumptions about physical lake forcing. Int. Rev. Hydrobiol. 93, 404–414 (2008).
    Google Scholar 

    50.
    Livingstone, D. M. Impact of secular climate change on the thermal structure of a large temperate central European lake. Clim. Change 57, 205–225 (2003).
    Google Scholar 

    51.
    Peeters, F., Livingstone, D. M., Goudsmit, G.-H., Kipfer, R. & Forster, R. Modeling 50 years of historical temperature profiles in a large central European lake. Limnol. Oceanogr. 47, 186–197 (2002).
    ADS  Google Scholar 

    52.
    Foley, B., Jones, I. D., Maberly, S. C. & Rippey, B. Long-term changes in oxygen depletion in a small temperate lake: effects of climate change and eutrophication. Freshw. Biol. 57, 278–289 (2011).
    Google Scholar 

    53.
    Salmaso, N., Boscaini, A., Capelli, C. & Cerasino, L. Ongoing ecological shifts in a large lake are driven by climate change and eutrophication: evidences from a three-decade study in Lake Garda. Hydrobiologia 824, 177–195 (2018).
    CAS  Google Scholar 

    54.
    Vinçon-Leite, B., Lemaire, B. J., Khac, V. T. & Tassin, B. Long-term temperature evolution in a deep sub-alpine lake, Lake Bourget, France: how a one-dimensional model improves its trend assessment. Hydrobiologia 731, 49–64 (2014).
    Google Scholar 

    55.
    Livingstone, D. M. An example of the simultaneous occurrence of climate-driven “sawtooth” deep-water warming/cooling episodes in several Swiss lakes. SIL Proc. 1922–2010(26), 822–828 (1997).
    Google Scholar 

    56.
    Martin-Creuzburg, D., von Elert, E. & Hoffmann, K. H. Nutritional constraints at the cyanobacteria—Daphnia magna interface: the role of sterols. Limnol. Oceanogr. 53, 456–468 (2008).
    ADS  Google Scholar 

    57.
    Zadereev, E. S., Boehrer, B. & Gulati, R. D. Introduction: meromictic lakes, their terminology and geographic distribution. In: Ecology of Meromictic Lakes, Vol. 228, 1–11 (Springer, 2017).

    58.
    Bryhn, A. C., Girel, C., Paolini, G. & Jacquet, S. Predicting future effects from nutrient abatement and climate change on phosphorus concentrations in Lake Bourget, France. Ecol. Model. 221, 1440–1450 (2010).
    CAS  Google Scholar 

    59.
    Kourzeneva, E., Asensio, H., Martin, E. & Faroux, S. Global gridded dataset of lake coverage and lake depth for use in numerical weather prediction and climate modelling. Tellus A Dyn. Meteorol. Oceanogr. 64, 15640 (2012).
    Google Scholar 

    60.
    Downing, J. A. et al. The global abundance and size distribution of lakes, ponds, and impoundments. Limnol. Oceanogr. 51, 2388–2397 (2006).
    ADS  Google Scholar 

    61.
    Cael, B. B., Heathcote, A. J. & Seekell, D. A. The volume and mean depth of Earth’s lakes. Geophys. Res. Lett. 44, 209–218 (2017).
    ADS  Google Scholar 

    62.
    Brett, M. T. & Benjamin, M. M. A review and reassessment of lake phosphorus retention and the nutrient loading concept. Freshw. Biol. 53, 194–211 (2007).
    Google Scholar 

    63.
    Bryhn, A. C. A morphometrically based method for predicting water layer boundaries in meromictic lakes. Hydrobiologia 636, 413–419 (2009).
    CAS  Google Scholar 

    64.
    Rempfer, J. et al. The effect of the exceptionally mild European winter of 2006–2007 on temperature and oxygen profiles in lakes in Switzerland: a foretaste of the future?. Limnol. Oceanogr. 55, 2170–2180 (2010).
    ADS  CAS  Google Scholar 

    65.
    Jenny, J. P. et al. Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Glob. Change Biol. 22, 1481–1489 (2016).
    ADS  Google Scholar 

    66.
    Kraemer, B. M., Mehner, T. & Adrian, R. Reconciling the opposing effects of warming on phytoplankton biomass in 188 large lakes. Sci. Rep. 7, 10762 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    67.
    Bonomi, G. & Gerletti, M. Lake Iseo: a first limnological survey (temperature, chemistry, plankton and benthos). Mem. 1st. Ital. Idrobiol. 22, 149–175 (1967).
    Google Scholar 

    68.
    Pilotti, M., Simoncelli, S. & Valerio, G. A simple approach to the evaluation of the actual water renewal time of natural stratified lakes. Water Resour. Res. 50, 2830–2849 (2014).
    ADS  Google Scholar 

    69.
    Ambrosetti, W. & Barbanti, L. Evolution towards meromixis of Lake Iseo (Northern Italy) as revealed by its stability trend. J. Limnol. 64, 1 (2005).
    Google Scholar 

    70.
    Hupfer, M., Reitzel, K., Kleeberg, A. & Lewandowski, J. Long-term efficiency of lake restoration by chemical phosphorus precipitation: scenario analysis with a phosphorus balance model. Water Res. 97, 153–161 (2016).
    CAS  PubMed  Google Scholar 

    71.
    Hesslein, R. H. An in situ sampler for close interval pore water studies1. Limnol. Oceanogr. 21, 912–914 (1976).
    ADS  CAS  Google Scholar 

    72.
    Psenner, R., Pucsko, R. & Sage, M. Fractionation of Organic and Inorganic Phosphorus Compounds in Lake Sediments, An Attempt to Characterize Ecologically Important Fractions (Die Fraktionierung Organischer und Anorganischer Phosphorverbindungen von Sedimenten, Versuch einer Definition Okologisch Wichtiger Fraktionen). Arch. fur Hydrobiol. 1 (1984).

    73.
    Hupfer, M., Gächter, R. & Giovanoli, R. Transformation of phosphorus species in settling seston and during early sediment diagenesis. Aquat. Sci. 57, 305–324 (1995).
    Google Scholar 

    74.
    Reitzel, K., Hansen, J., Andersen, F. Ø, Hansen, K. S. & Jensen, H. S. Lake restoration by dosing aluminum relative to mobile phosphorus in the sediment. Environ. Sci. Technol. https://doi.org/10.1021/ES0485964 (2005).
    Article  PubMed  Google Scholar 

    75.
    Berg, P., Risgaard-Petersen, N. & Rysgaard, S. Interpretation of measured concentration profiles in sediment pore water. Limnol. Oceanogr. 43, 1500–1510 (1998).
    ADS  CAS  Google Scholar 

    76.
    Yuan-Hui, L. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 38, 703–714 (1974).
    ADS  Google Scholar 

    77.
    R Core Team. R: a language and environment for statistical computing (2013).

    78.
    Messager, M. L., Lehner, B., Grill, G., Nedeva, I. & Schmitt, O. Estimating the volume and age of water stored in global lakes using a geo-statistical approach. Nat. Commun. 7, 13603 (2016).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    79.
    Håkanson, L. The importance of lake morphometry for the structure and function of lakes. Int. Rev. Hydrobiol. 90, 433–461 (2005).
    Google Scholar  More