More stories

  • in

    Energetic and health effects of protein overconsumption constrain dietary adaptation in an apex predator

    1.Fuller, A. et al. Physiological mechanisms in coping with climate change. Phys. Biochem. Zool. 83, 713–720. https://doi.org/10.1086/652242 (2010).Article 

    Google Scholar 
    2.Raubenheimer, D., Simpson, S. J. & Tait, A. H. Match and mismatch: Conservation physiology, nutritional ecology and the timescales of biological adaptation. Philos. Trans. R. Soc. B 367, 1628–1646. https://doi.org/10.1098/rstb.2012.0007 (2012).CAS 
    Article 

    Google Scholar 
    3.Tracy, C. R. et al. The importance of physiological ecology in conservation biology. Integr. Comp. Biol. 46, 1191–1205. https://doi.org/10.1093/icb/icl054 (2006).Article 
    PubMed 

    Google Scholar 
    4.Parker, K. L., Barboza, P. S. & Gillingham, M. P. Nutrition integrates environmental responses of ungulates. Funct. Ecol. 23, 57–69. https://doi.org/10.1111/j.1365-2435.2009.01528.x (2009).Article 

    Google Scholar 
    5.Morris, J. G. Idiosyncratic nutrient requirements of cats appear to be diet-induced evolutionary adaptations. Nutr. Res. Rev. 15, 153–168. https://doi.org/10.1079/NRR200238 (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    6.Hofmann, R. R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: A comparative view of their digestive system. Oecologia 78, 443–457. https://doi.org/10.1007/BF00378733 (1989).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    7.Rode, K. D., Chapman, C. A., McDowell, L. R. & Stickler, C. Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus Ascanius). Biotropica 38, 625–634. https://doi.org/10.1111/j.1744-7429.2006.00183.x (2006).Article 

    Google Scholar 
    8.Birnie-Gauvin, K., Peiman, K. S., Raubenheimer, D. & Cooke, S. J. Nutritional physiology and ecology of wildlife in a changing world. Cons Phys. 5, cox030. https://doi.org/10.1093/conphys/cox030 (2017).CAS 
    Article 

    Google Scholar 
    9.Rode, K. D. & Robbins, C. T. Why bears consume mixed diets during fruit abundance. Can. J. Zool. 78, 1640–1645. https://doi.org/10.1139/z00-082 (2000).Article 

    Google Scholar 
    10.Robbins, C. T. et al. Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos 116, 1675–1683. https://doi.org/10.1111/j.0030-1299.2007.16140.x (2007).Article 

    Google Scholar 
    11.Erlenbach, J. A., Rode, K. D., Raubenheimer, D. & Robbins, C. T. Macronutrient optimization and energy maximization determine diets of brown bears. J. Mamm. 95, 160–168. https://doi.org/10.1644/13-MAMM-A-161 (2014).Article 

    Google Scholar 
    12.Nie, Y. et al. Giant pandas are macronutritional carnivores. Curr. Biol. 29, 1677–1682. https://doi.org/10.1016/j.cub.2019.03.067 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Sponheimer, M., Clauss, M. & Codron, D. Dietary evolution: The panda paradox. Curr. Biol. 29, R417–R419. https://doi.org/10.1016/j.cub.2019.04.045 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Stirling, I. & McEwan, E. H. The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can. J. Zool. 53, 1021–1027. https://doi.org/10.1139/z75-117 (1975).CAS 
    Article 
    PubMed 

    Google Scholar 
    15.Liu, S. P. et al. Population genomics reveal recent speciation and rapid evolutionary adaptation in Polar Bears. Cell 157, 785–794. https://doi.org/10.1016/j.cell.2014.03.054 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Kohl, K. D., Coogan, S. C. P. & Raubenheimer, D. Do wild carnivores forage for prey or for nutrient? Evidence for nutrient-specific foraging in vertebrate predators. BioEssays 37, 701–709. https://doi.org/10.1002/bies.201400171 (2015).Article 
    PubMed 

    Google Scholar 
    17.Machovsky-Capuska, G. E. & Raubenheimer, D. The nutritional ecology of marine apex predators. Ann. Rev. Mar. Sci. 12, 361–387. https://doi.org/10.1146/annurev-marine-010318-095411 (2020).Article 
    PubMed 

    Google Scholar 
    18.Hewson-Hughes, A. K., Colyer, A., Simpson, S. J. & Raubenheimer, D. Balancing macronutrient intake in a mammalian carnivore: Disentangling the influences of flavor and nutrition. R. Soc. Open 3, 160081. https://doi.org/10.1098/rsos.160081 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    19.McKinney, M. A., Atwood, T. C., Iverson, S. J. & Peacock, E. Temporal complexity of southern Beaufort Sea polar bear diets during a period of increasing land use. Ecosphere 8, e01633. https://doi.org/10.1002/ecs2.1633 (2017).Article 

    Google Scholar 
    20.Rode, K. D. et al. Spring fasting behavior in a marine apex predator provides an index of ecosystem productivity. Glob. Change Biol. 24, 410–423. https://doi.org/10.1111/gcb.13933 (2018).ADS 
    Article 

    Google Scholar 
    21.Rode, K. D. et al. Variation in the response of an arctic top predator experiencing habitat loss: Feeding and reproductive ecology of two polar bear populations. Glob. Change Biol. 20, 76–88. https://doi.org/10.1111/gcb.12339 (2014).ADS 
    Article 

    Google Scholar 
    22.Rode, K. D. et al. Seal body condition and atmospheric circulation patterns in the Chukchi Sea influence polar bear body condition, recruitment, and feeding ecology. Glob. Change Biol. https://doi.org/10.1111/gcb.15572 (2021).Article 

    Google Scholar 
    23.Yurkowski, D. J., Hussey, N. E., Semeniuk, C., Ferguson, S. H. & Fisk, A. T. Effects of fat extraction and the utility of fat normalization models on δ13C and δ15N values in Arctic marine mammal tissues. Pol. Biol. 38, 131–143. https://doi.org/10.1007/s00300-014-1571-1 (2014).Article 

    Google Scholar 
    24.Hilderbrand, G. V., Jenkins, S. G., Schwartz, C. C., Hanley, T. A. & Robbins, C. T. Effect of seasonal differences in dietary meat intake on changes in body mass and composition in wild and captive brown bears. Can. J. Zool. 77, 1623–1630. https://doi.org/10.1139/z99-133 (1999).Article 

    Google Scholar 
    25.McCullough, D. R. & Ullrey, D. E. Proximate mineral and gross energy composition of white-tailed deer. J. Wildl. Manag. 47, 430–441. https://doi.org/10.2307/3808516 (1983).Article 

    Google Scholar 
    26.Pritchard, G. T. & Robbins, C. T. Digestive and metabolic efficiencies of grizzly and black bears. Can. J. Zool. 68, 1645–1651. https://doi.org/10.1139/z90-244 (1990).Article 

    Google Scholar 
    27.LaDouceur, E. E. B., Garner, M. M., Davis, B. & Tseng, F. A retrospective study of end-stage renal disease in captive polar bears (Ursus maritimus). J. Zoo Wildl. Med. 45, 69–77. https://doi.org/10.1638/2013-0071R.1 (2014).Article 
    PubMed 

    Google Scholar 
    28.Derocher, A. E. & Stirling, I. Aspects of survival in juvenile polar bears. Can. J. Zool. 74, 1246–1252. https://doi.org/10.1139/z96-138 (1996).Article 

    Google Scholar 
    29.Hedberg, G. E. et al. Milk composition in free-ranging polar bears (Ursus maritimus) as a model for captive rearing milk formula. Zoo Biol. 30, 550–565. https://doi.org/10.1002/zoo.20375 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    30.Jensen, K. et al. Nutrient-specific compensatory feeding in a mammalian carnivore, the mink, Neovison vison. Br. J. Nutr. 112, 1226–1233. https://doi.org/10.1017/S0007114514001664 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Rosen, D. A. S. & Trites, A. W. Examining the potential for nutritional stress in young Stellar sea lions: Physiological effects of prey composition. J. Comp. Phys. B 175, 265–273. https://doi.org/10.1007/s00360-005-0481-5 (2005).CAS 
    Article 

    Google Scholar 
    32.Kirsch, P. E., Iverson, S. J. & Bowen, W. D. Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Phys. Biochem. Zool. 73, 45–59. https://doi.org/10.1086/316723 (2000).CAS 
    Article 

    Google Scholar 
    33.Zhao, L., Schell, D. M. & Castellini, M. A. Dietary macronutrients influence 13C and 15N signatures of pinnipeds: Captive feeding studies with harbor seals (Phoca vitulina). Physiol. Part A Mol. Integr. Phys. 143, 469–478. https://doi.org/10.1016/j.cbpa.2005.12.032 (2006).CAS 
    Article 

    Google Scholar 
    34.Diaz Gomez, M., Rosen, D. A. S. & Trites, A. W. Net energy gained by northern fur seals (Callorhinus ursinus) is impacted more by diet quality than diet diversity. Can. J. Zool. 94, 12–135. https://doi.org/10.1139/cjz-2015-0143 (2016).CAS 
    Article 

    Google Scholar 
    35.Le Bellego, L., van Milgen, J. & Noblet, J. Effect of high temperature and low-protein diets on performance of growing pigs. J. Anim. Sci. 79, 1259–1271. https://doi.org/10.2527/2001.7951259x (2002).Article 

    Google Scholar 
    36.Anton, S. D. et al. Effects of popular diets without specific calorie targets on weight loss outcomes: Systematic review of findings from clinical trials. Nutrients 9, 822. https://doi.org/10.3390/nu9080822 (2017).Article 
    PubMed Central 

    Google Scholar 
    37.Bininda-Emonds, O. R. P., Gittleman, J. L. & Purvis, A. Building large trees by combining phylogenetic information: A complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74, 143–175. https://doi.org/10.1017/S0006323199005307 (1999).CAS 
    Article 
    PubMed 

    Google Scholar 
    38.Plantinga, E. A., Bosch, G. & Hendriks, W. H. Estimation of the dietary nutrient profile of free-roaming feral cats: Possible implications for nutrition of domestic cats. Br. J. Nutr. 106, S35–S48. https://doi.org/10.1017/S0007114511002285 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Hewson-Hughes, A. K. et al. Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris. Behav. Ecol. 24, 293–304. https://doi.org/10.1093/beheco/ars168 (2013).Article 
    PubMed 

    Google Scholar 
    40.Trites, A. W. & Donnelly, C. P. The decline of Steller sea lions Eumetopias jubatus in Alaska: A review of the nutritional stress hypothesis. Mamm. Rev. 33, 3–28. https://doi.org/10.1046/j.1365-2907.2003.00009.x (2003).Article 

    Google Scholar 
    41.Hauser, D. D. W., Allen, C. S., Rich, H. B. Jr. & Quinn, T. P. Resident harbor seals (Phoca vitulina) in Iliamna Lake, Alaska: Summer diet and partial consumption of adult sockeye salmon (Oncorhynchus nerka). Aquat. Mamm. 34, 303–309. https://doi.org/10.1578/AM.34.3.2008.303 (2008).Article 

    Google Scholar 
    42.Jia, Y. et al. Long-term high intake of whole proteins results in renal damage in pigs. J. Nutr. 140, 1646–1652. https://doi.org/10.3945/jn.110.123034 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Wakefield, A. P., House, J. D., Ogborn, M. R., Weiler, H. A. & Aukema, H. M. A diet of 35% of energy from protein leads to kidney damage in female Sprague–Dawley rats. Br. J. Nutr. 106, 656–663. https://doi.org/10.1017/S0007114511000730 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Ko, G.-J., Rhee, C. M., Kalantar-Zadeh, K. & Joshi, S. The effects of high-protein diets on kidney health and longevity. J. Am. Soc. Nephrol. 31, 1667–1679. https://doi.org/10.1681/ASN.2020010028 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    45.Bӧswald, L. F., Kienzle, E. & Dobenecker, B. Observation about phosphorus and protein supply in cats and dogs prior to the diagnosis of chronic kidney disease. J. Phys. Anim. Nutr. 102, 31–36. https://doi.org/10.1111/jpn.12886 (2017).CAS 
    Article 

    Google Scholar 
    46.Ioannou, G. N., Morrow, O. B., Connole, M. L. & Lee, S. P. Association between dietary nutrient composition and the incidence of cirrhosis or liver cancer in the united states population. Hepatology 50, 175–184. https://doi.org/10.1002/hep.22941 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Tryland, M. et al. Plasma biochemical values from apparently healthy free-ranging polar bears from Svalbard. J. Wildl. Dis. 38, 566–575. https://doi.org/10.7589/0090-3558-38.3.566 (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Thiemann, G. W., Iverson, S. J. & Stirling, I. Polar bear diets and Arctic marine food webs: Insights from fatty acid analysis. Ecol. Monogr. 78, 591–613. https://doi.org/10.1890/07-1050.1 (2008).Article 

    Google Scholar 
    49.Ryg, M., Smith, T. G. & Oritsland, N. A. Seasonal changes in body mass and body composition of ringed seals (Phoca hispida) on Svalbard. Can. J. Zool. 68, 470–475. https://doi.org/10.1139/z90-069 (1990).Article 

    Google Scholar 
    50.Ferguson, S. H. et al. Demographic, ecological, and physiological responses of ringed seals to an abrupt decline in sea ice availability. Peer J. 5, e2957. https://doi.org/10.7717/peerj.2957 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    51.Atwood, T. C. et al. Rapid environmental change drives increased land use by an Arctic marine predator. PLoS One 11, 30155932. https://doi.org/10.1371/journal.pone.0155932 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    52.Molnar, P. K. et al. Fasting season length sets temporal limits for global polar bear persistence. Nat. Clim. Change 10, 732–738. https://doi.org/10.1038/s41558-020-0818-9 (2020).ADS 
    Article 

    Google Scholar 
    53.Rode, K. D., Robbins, C. T., Nelson, L. & Amstrup, S. C. Can polar bears use terrestrial foods to offset lost ice-based hunting opportunities?. Front. Ecol. Environ. 13, 138–145. https://doi.org/10.1890/140202 (2015).Article 

    Google Scholar 
    54.McArt, S. H. et al. Summer nitrogen availability as a bottom-up constraint on moose in south-central Alaska. Ecology 90, 1400–1411. https://doi.org/10.1890/08-1435.1 (2009).Article 
    PubMed 

    Google Scholar 
    55.Lahtinen, M., Clinnick, D., Mannermaa, K., Salonen, J. S. & Viranta, S. Excess protein enabled dog domestication during severe Ice Age winters. Sci. Rep. 11, 7. https://doi.org/10.1038/s41598-020-78214-4 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    56.Regehr, E. V., Hostetter, N. J., Wilson, R. R. & Rode, K. D. Integrated population modeling provides the first empirical estimates of vital rates and abundance for polar bears in the Chukchi Sea. Sci. Rep. 8, 16780. https://doi.org/10.1038/s41598-018-34824-7 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Crawford, J. A., Quakenbush, L. T. & Citta, J. J. A comparison of ringed seal and bearded seal diet, condition, and productivity between historical (1975–19480 and recent (2003–2012) periods in the Alaskan Bering and Chukchi Seas. Progr. Oceanogr. 136, 133–150. https://doi.org/10.1016/j.pocean.2015.05.011 (2015).ADS 
    Article 

    Google Scholar 
    58.Germain, L. R., McCarthy, M. D., Koch, P. L. & Harvey, J. T. Stable carbon and nitrogen isotopes in multiple tissues of wild and captive harbor seals (Phoca vitulina) off the California coast. Mar. Mamm. Sci. 28, 542–560. https://doi.org/10.1111/j.1748-7692.2011.00516.x (2011).CAS 
    Article 

    Google Scholar 
    59.Erlenbach, J. A. Nutritional and landscape ecology of brown bears (Ursus arctos). PhD dissertation. Washington State University, Pullman, WA, USA (2020).60.Laidre, K. L., Stirling, I., Estes, J. A., Kochnev, A. & Roberts, J. Historical and potential future importance of large whales as food for polar bears. Front. Ecol. Environ. 16, 515–524. https://doi.org/10.1002/fee.1963 (2018).Article 

    Google Scholar 
    61.Newsome, S. D., Koch, P. L., Etnier, M. A. & Aurioles-Gamboa, D. Using carbon and nitrogen isotope values to investigate maternal strategies in northeast Pacific otariids. Mar. Mamm. Sci. 22, 556–572. https://doi.org/10.1111/j.1748-7692.2006.00043.x (2006).Article 

    Google Scholar 
    62.Stock, B. C. et al. Analyzing mixing systems using a new generation of Bayesian tracker mixing models. Peer J. 6, e5096. https://doi.org/10.7717/peerj.5096 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Rode, K. D. et al. Isotopic incorporation and the effects of fasting and dietary fat content on isotopic discrimination in large carnivorous mammals. Phys. Biochem. Zool. 89, 182–197. https://doi.org/10.1086/686490 (2016).CAS 
    Article 

    Google Scholar 
    64.Merrill, A. L. & Watt, B. K. Energy Value of Foods: Basis and Derivation, Revised. Agriculture Handbook 74 (United States Department of Agriculture, 1973).65.Dyck, M. G. & Morin, P. In vivo digestibility trials of a captive polar bear (Ursus maritimus) feeding on harp seal (Pagophilus growenlandicus) and Arctic charr (Salvelinus alpinus). Pak. J. Zool. 43, 759–767 (2011).CAS 

    Google Scholar  More

  • in

    Tracking the rising extinction risk of sharks and rays in the Northeast Atlantic Ocean and Mediterranean Sea

    1.McClenachan, L., Cooper, A. B., Carpenter, K. E. & Dulvy, N. K. Extinction risk and bottlenecks in the conservation of charismatic marine species. Conserv. Lett. 5, 1–8 (2011).
    Google Scholar 
    2.Dulvy, N. K., Jennings, S., Rogers, S. I. & Maxwell, D. L. Threat and decline in fishes: An indicator of marine biodiversity. Can. J. Fish. Aquat. Sci. 63, 1267–1275 (2006).Article 

    Google Scholar 
    3.CBD & UNEP. Strategic Plan for Biodiversity 2011–2020 and the Aichi Targets ‘Living in Harmony with Nature’. 2pp. https://www.cbd.int/doc/strategic-plan/2011-2020/Aichi-Targets-EN.pdf (Secretariat of the Convention on Biological Diversity, Montreal, Quebec, 2011).4.Butchart, S. H. M. et al. Improvements to the Red List Index. PLoS ONE 2, 1–8 (2007).Article 

    Google Scholar 
    5.Butchart, S. H. M. et al. Measuring global trends in the status of biodiversity: Red List Indices for birds. PLoS Biol. 2, 2294–2304 (2004).CAS 
    Article 

    Google Scholar 
    6.Butchart, S. H. M. et al. Using Red List Indices to measure progress towards the 2010 target and beyond. Philos. Trans. R. Soc. B Biol. Sci. 360, 255–268 (2005).CAS 
    Article 

    Google Scholar 
    7.Hoffmann, M. et al. The changing fates of the world’s mammals. Philos. Trans. R. Soc. B Biol. Sci. 366, 2598–2610 (2011).Article 

    Google Scholar 
    8.Marler, P. N. & Marler, T. E. An assessment of Red List data for the cycadales. Trop. Conserv. Sci. 8, 1114–1125 (2015).Article 

    Google Scholar 
    9.Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science (80-. ) 321, 560–563 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Gärdenfors, U. Classifying threatened species at national versus global levels. Trends Ecol. Evol. 16, 511–516 (2001).Article 

    Google Scholar 
    11.Szabo, J. K., Butchart, S. H. M., Possingham, H. P. & Garnett, S. T. Adapting global biodiversity indicators to the national scale: A Red List Index for Australian birds. Biol. Conserv. 148, 61–68 (2012).Article 

    Google Scholar 
    12.Juslén, A., Hyvärinen, E. & Virtanen, L. K. Application of the Red-List Index at a national level for multiple species groups. Conserv. Biol. 27, 398–406 (2013).PubMed 
    Article 

    Google Scholar 
    13.Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science (80-. ) 330, 1503–1509 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    14.IPBES. Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. 56pp. https://ipbes.net/document-library-catalogue/summary-policymakers-global-assessment-laid-out (IPBES Secretariat, Bonn, Germany, 2019).15.Dulvy, N. K., Sadovy, Y. & Reynolds, J. D. Extinction vulnerability in marine populations. Fish Fish. 4, 25–64 (2003).Article 

    Google Scholar 
    16.Lawson, J. M. et al. Global extinction risk and conservation of Critically Endangered angel sharks in the Eastern Atlantic and Mediterranean Sea. Int. Counc. Explor. Seas J. Mar. Sci. 77, 12–29 (2020).
    Google Scholar 
    17.WGEF. Report of the Working Group on Elasmobranch Fishes (WGEF). 671pp. https://www.ices.dk/community/groups/pages/wgef.aspx (ICES CM, Lisbon, Portugal, 2018).18.Dulvy, N. K., Allen, D. J., Ralph, G. M. & Walls, R. H. L. The conservation status of sharks, rays and chimaeras in the Mediterranean Sea. 14pp. https://portals.iucn.org/library/node/47636 (IUCN, Malaga, Spain, 2016)19.Cavanagh, R. D. & Gibson, C. Overview of the Conservation Status of Cartilaginous Fishes (Chondrichthyans) in the Mediterranean Sea (IUCN, 2007). https://doi.org/10.2305/IUCN.CH.2007.MRA.3.en.Book 

    Google Scholar 
    20.Gibson, C., Valenti, S. V., Fowler, S. L. & Fordham, S. V. The Conservation Status of Northeast Atlantic Chondrichthyans: Report of the IUCN Shark Specialist Group Northeast Atlantic Regional Red List Workshop (IUCN Species Survival Commission Shark Specialist Group, 2008).
    Google Scholar 
    21.Nieto, A. et al. European Red List of Marine Fishes. 88pp. https://doi.org/10.2779/082723 (Publications Office of the European Union, Luxembourg, 2015).22.Barrett, J. H., Locker, A. M. & Roberts, C. M. The origins of intensive marine fishing in medieval Europe: The English evidence. Proc. R. Soc. B Biol. Sci. 271, 2417–2421 (2004).Article 

    Google Scholar 
    23.Rousseau, Y., Watson, R. A., Blanchard, J. L. & Fulton, E. A. Evolution of global marine fishing fleets and the response of fished resources. Proc. Natl. Acad. Sci. U.S.A. 116, 12238–12243 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Fernandes, P. G. et al. Coherent assessments of Europe’s marine fishes show regional divergence and megafauna loss. Nat. Ecol. Evol. 1, 1–9 (2017).Article 

    Google Scholar 
    25.Walls, R. H. L. & Dulvy, N. K. Eliminating the dark matter of data deficiency by predicting the conservation status of Northeast Atlantic and Mediterranean Sea sharks and rays. Biol. Conserv. 246, 1–14 (2020).Article 

    Google Scholar 
    26.Kyne, P. M. et al. The thin edge of the wedge: Extremely high extinction risk in wedgefishes and giant guitarfishes. Aquat. Conserv. Mar. Freshw. Ecosyst. 30, 1337–1361 (2020).Article 

    Google Scholar 
    27.Jennings, S., Reynolds, J. D. & Mills, S. C. Life history correlates of responses to fisheries exploitation. Proc. R. Soc. B Biol. Sci. 265, 333–339 (1998).Article 

    Google Scholar 
    28.Frisk, M. G., Miller, T. J. & Fogarty, M. J. Estimation and analysis of biological parameters in elasmobranch fishes: A comparative life history study. Can. J. Fish. Aquat. Sci. 58, 969–981 (2001).Article 

    Google Scholar 
    29.Hutchings, J. A., Myers, R. A., García, V. B., Lucifora, L. O. & Kuparinen, A. Life-history correlates of extinction risk and recovery potential. Ecol. Appl. 22, 1061–1067 (2012).PubMed 
    Article 

    Google Scholar 
    30.Dulvy, N. K. et al. Extinction risk and conservation of the world’s sharks and rays. Elife 3, 1–35 (2014).Article 

    Google Scholar 
    31.Cardoso, P. Package ‘red’. 32pp. Available at: https://cran.r-project.org/web/packages/red/red.pdf (2020).32.Pacoureau, N. et al. Half a century of global decline in oceanic sharks and rays. Nature 589, 567–571 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    33.IUCN 2021. The IUCN Red List of Threatened Species. Version 2021–1. Web page: https://www.iucnredlist.org. Accessed 7 April 2021.34.European Environment Agency. Red List Index for European species. 23pp. https://www.eea.europa.eu/data-and-maps/indicators/red-list-index-for-european-species/red-list-index-for-european (EEA, Copenhagen, Denmark, 2010).35.Bolam, F. C. et al. How many bird and mammal extinctions has recent conservation action prevented?. bioRxiv https://doi.org/10.1101/2020.02.11.943902 (2020).Article 

    Google Scholar 
    36.GFCM. Recommendation GFCM/29/2005/1 on the Management of Certain Fisheries Exploiting Demersal and Deep-Water Species and the Establishment of a Fisheries Restricted Area Below 1000 m. 2pp. https://www.cbd.int/doc/meetings/mar/soiom-2016-01/other/soiom-2016-01-gfcm-02-en.pdf (2005).37.Morato, T., Watson, R., Pitcher, T. J. & Pauly, D. Fishing down the deep. Fish Fish. 7, 23–33 (2006).Article 

    Google Scholar 
    38.Abernethy, K. E., Trebilcock, P., Kebede, B., Allison, E. H. & Dulvy, N. K. Fuelling the decline in UK fishing communities?. ICES J. Mar. Sci. 67, 1076–1085 (2010).Article 

    Google Scholar 
    39.Campana, S. E. Transboundary movements, unmonitored fishing mortality, and ineffective international fisheries management pose risks for pelagic sharks in the Northwest Atlantic. Can. J. Fish. Aquat. Sci. 73, 1599–1607 (2016).Article 

    Google Scholar 
    40.Queiroz, N. et al. Global spatial risk assessment of sharks under the footprint of fisheries. Nature 572, 461–466 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Fredston-Hermann, A., Selden, R., Pinsky, M., Gaines, S. D. & Halpern, B. S. Cold range edges of marine fishes track climate change better than warm edges. Glob. Change Biol. 26, 2908–2922 (2020).ADS 
    Article 

    Google Scholar 
    42.Yan, H. F. et al. Overfishing and habitat loss drives range contraction of iconic marine fishes to near extinction. Sci. Adv. 7, 1–11 (2021).Article 

    Google Scholar 
    43.De Oliveira, J. A., Ellis, J. R. & Dobby, H. Incorporating density dependence in pup production in a stock assessment of NE Atlantic spurdog Squalus acanthias. ICES J. Mar. Sci. 70, 1341–1353 (2013).Article 

    Google Scholar 
    44.Bailey, D. M., Collins, M. A., Gordon, J. D. M., Zuur, A. F. & Priede, I. G. Long-term changes in deep-water fish populations in the northeast Atlantic: A deeper reaching effect of fisheries?. Proc. R. Soc. B Biol. Sci. 276, 1965–1969 (2009).CAS 
    Article 

    Google Scholar 
    45.IUCN. IUCN Red List Categories and Criteria: Version 3.1. Second Edition. iv + 32pp. https://www.iucnredlist.org/resources/grid (IUCN, Gland, Switzerland and Cambridge, UK, 2012).46.Godfray, H. C. J. et al. Food security: The challenge of feeding 9 billion people. Science (80-. ) 327, 812–818 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    47.Smith, A. D. M. & Garcia, S. M. Fishery management: Contrasts in the Mediterranean and the Atlantic. Curr. Biol. 24, 810–812 (2014).Article 
    CAS 

    Google Scholar 
    48.Caddy, J. F. Practical issues in choosing a framework for resource assessment and management of Mediterranean and Black Sea fisheries. Mediterr. Mar. Sci. 10, 83–119 (2009).Article 

    Google Scholar 
    49.Colloca, F. et al. Rebuilding Mediterranean fisheries: A new paradigm for ecological sustainability. Fish Fish. 14, 89–109 (2013).Article 

    Google Scholar 
    50.Pauly, D. Anecdotes and the shifting baseline syndrome of fisheries. Trends Ecol. Evol. 10, 430 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    51.Brander, K. Disappearance of common skate Raia batis from Irish Sea. Nature 290, 48–49 (1981).ADS 
    Article 

    Google Scholar 
    52.Vasilakopoulos, P., Maravelias, C. D. & Tserpes, G. The alarming decline of Mediterranean fish stocks. Curr. Biol. 24, 1643–1648 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Oliver, S., Braccini, M., Newman, S. J. & Harvey, E. S. Global patterns in the bycatch of sharks and rays. Mar. Policy 54, 86–97 (2015).Article 

    Google Scholar 
    54.Harrison, A. L. et al. The political biogeography of migratory marine predators. Nat. Ecol. Evol. 2, 1571–1578 (2018).PubMed 
    Article 

    Google Scholar 
    55.White, C. & Costello, C. Close the high seas to fishing?. PLoS Biol. 12, 1–5 (2014).Article 
    CAS 

    Google Scholar 
    56.Donald, P. F. et al. International conservation policy delivers benefits for birds in Europe. Science (80-. ) 317, 810–813 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    57.Demirel, N., Zengin, M. & Ulman, A. First large-scale eastern Mediterranean and black sea stock assessment reveals a dramatic decline. Front. Mar. Sci. 7, 1–13 (2020).Article 

    Google Scholar 
    58.Clarke, M. W. Sharks, skates and rays in the northeast Atlantic: Population status, advice and management. J. Appl. Ichthyol. 25, 3–8 (2009).Article 

    Google Scholar 
    59.Abudaya, M. et al. Speak of the devil ray (Mobula mobular) fishery in Gaza. Rev. Fish Biol. Fish. 28, 229–239 (2018).Article 

    Google Scholar 
    60.CMS. Appendices I and II of the Convention on the Conservation of Migratory Species of Wild Animals (CMS). 16pp. Available at: https://www.cms.int/en/species/appendix-i-ii-cms (2020).61.Jabado, R. W. et al. The Conservation Status of Sharks, Rays, and Chimaeras in the Arabian Sea and Adjacent Waters (Environment Agency – Abu Dhabi, UAE and IUCN Species Survival Commission Shark Specialist Group, 2017).
    Google Scholar 
    62.Iglésias, S. P., Toulhoat, L. & Sellos, D. Y. Taxonomic confusion and market mislabelling of threatened skates: Important consequences for their conservation status. Aquat. Conserv. Mar. Freshw. Ecosyst. 20, 319–333 (2010).Article 

    Google Scholar 
    63.Ferretti, F., Myers, R. A., Serena, F. & Lotze, H. K. Loss of large predatory sharks from the Mediterranean Sea. Conserv. Biol. 22, 952–964 (2008).PubMed 
    Article 

    Google Scholar 
    64.Iglésias, S. P. & Mollen, F. H. Cold case: The early disappearance of the Bramble shark (Echinorhinus brucus) in European and adjacent waters. Oceans Past News 10, 1–5 (2018).
    Google Scholar 
    65.IUCN. Guidelines for Application of IUCN Red List Criteria at Regional and National Levels: Version 4.0 (IUCN, 2012).
    Google Scholar 
    66.CBD. Indicators for Assessing Progress Towards the 2010 Target: Change in Status of Threatened Species. Convention on Biological Diversity, UNEP/CBD/AHTEG-2010-Ind/1/INF/9. 10pp. Available at: https://www.cbd.int/meetings/TEGIND-01 (2004).67.Brooks, T. M. et al. Harnessing biodiversity and conservation knowledge products to track the Aichi targets and sustainable development goals. Biodiversity 16, 157–174 (2015).Article 

    Google Scholar 
    68.Bland, L. M. et al. Toward reassessing data-deficient species. Conserv. Biol. 31, 531–539 (2017).PubMed 
    Article 

    Google Scholar 
    69.Bland, L. M. et al. Cost-effective assessment of extinction risk with limited information. J. Appl. Ecol. 52, 861–870 (2015).Article 

    Google Scholar 
    70.White, W. T., Kyne, P. M. & Harris, M. Lost before found: A new species of whaler shark Carcharhinus obsolerus from the Western Central Pacific known only from historic records. PLoS ONE 14, 1–24 (2019).
    Google Scholar 
    71.Mace, G. M. et al. Aiming higher to bend the curve of biodiversity loss. Nat. Sustain. 1, 448–451 (2018).Article 

    Google Scholar 
    72.IUCN. IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission (IUCN, 2001).
    Google Scholar 
    73.Regan, T. J. et al. The consistency of extinction risk classification protocols. Conserv. Biol. 19, 1969–1977 (2005).Article 

    Google Scholar 
    74.Hiddink, J. G., Shepperson, J., Bater, R., Goonesekera, D. & Dulvy, N. K. Near disappearance of the Angelshark Squatina squatina over half a century of observations. Conserv. Sci. Pract. 1, 1–9 (2019).Article 

    Google Scholar 
    75.Bom, R. A., van de Water, M., Camphuysen, K. C. J., van der Veer, H. W. & van Leeuwen, A. The historical ecology and demise of the iconic Angelshark Squatina squatina in the southern North Sea. Mar. Biol. 167, 1–10 (2020).Article 

    Google Scholar 
    76.Shephard, S., Wögerbauer, C., Green, P., Ellis, J. R. & Roche, W. K. Angling records track the near extirpation of angel shark Squatina squatina from two Irish hotspots. Endanger. Species Res. 38, 153–158 (2019).Article 

    Google Scholar 
    77.Martin, C. S. et al. Spatio-temporal patterns in demersal elasmobranchs from trawl surveys in the eastern English Channel (1988–2008). Mar. Ecol. Prog. Ser. 417, 211–228 (2010).ADS 
    Article 

    Google Scholar 
    78.Burt, G. J., Ellis, J. R., Harley, B. F. & Kupschus, S. The FV Carhelmar Beam Trawl Survey of the Western English Channel (1989–2011): History of the Survey, Data Availability and the Distribution and Relative Abundance of Fish and Commercial Shellfish. CEFAS, Norwich, UK. Science Series, Technical Report no. 151. 139pp. (2013).79.Marandel, F., Lorance, P. & Trenkel, V. M. Determining long-term changes in a skate assemblage with aggregated landings and limited species data. Fish. Manag. Ecol. 26, 365–373 (2019).Article 

    Google Scholar 
    80.IUCN Standards and Petitions Subcommittee. Guidelines for Using the IUCN Red List Categories and Criteria, Version 11. Prepared by the Standards and Petitions Subcommittee. 87pp. Available at: http://www.iucnredlist.org/documents/RedListGuidelines.pdf (2014).81.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.r-project.org/. (2018).82.Bates, D. et al. Package ‘lme4’. 126pp. Available at: https://cran.r-project.org/web/packages/lme4/index.html (2020).83.Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R Statistics for Biology and Health (Springer, 2009). https://doi.org/10.1007/978-0-387-87458-6.Book 
    MATH 

    Google Scholar 
    84.Zuur, A. F., Hilbe, J. M. & Ieno, E. N. A Beginner’s Guide to GLM and GLMM with R: A Frequentist and Bayesian Perspective for Ecologists (Highland Statistic Ltd., 2013).
    Google Scholar 
    85.Gelman, A. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 27, 2865–2873 (2008).MathSciNet 
    PubMed 
    Article 

    Google Scholar 
    86.Hurvich, C. M. & Tsai, C.-L. Regression and time series model selection in small samples. Biometrika 76, 297–307 (1989).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    87.Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).PubMed 
    Article 

    Google Scholar 
    88.Bartoń, K. Package ‘MuMIn’. 75pp. Available at: https://cran.r-project.org/web/packages/MuMIn/index.html (2019).89.John, A. et al. Package ‘car’. 149pp. Available at: https://cran.r-project.org/web/packages/car/index.html (2020).90.Zuur, A. F., Ieno, E. N. & Smith, G. M. Analysing Ecological Data. Statistics for Biology and Health (Springer, 2007). https://doi.org/10.1198/016214508000000715.Book 
    MATH 

    Google Scholar  More

  • in

    Author Correction: Drivers of seedling establishment success in dryland restoration efforts

    School of Environmental Studies, University of Victoria, Victoria, British Columbia, CanadaNancy ShackelfordEcology and Evolutionary Biology, University of Colorado Boulder, Boulder, CO, USANancy Shackelford, Nichole Barger, Julie E. Larson & Katharine L. SudingDepartamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal, BrazilGustavo B. PaternoDepartment of Ecology and Ecosystem Management, Restoration Ecology Research Group, Technical University of Munich, Freising, GermanyGustavo B. PaternoUS Geological Survey, Southwest Biological Science Center, Moab, UT, USADaniel E. Winkler & Stephen E. FickSchool of Biological Sciences, The University of Western Australia, Crawley, Western Australia, AustraliaTodd E. EricksonKings Park Science, Department of Biodiversity Conservation and Attractions, Kings Park, Western Australia, AustraliaTodd E. Erickson & Peter J. GolosDepartment of Biology, University of Nevada, Reno, Reno, NV, USAElizabeth A. LegerUSDA Agricultural Research Service, Eastern Oregon Agricultural Research Center, Burns, OR, USALauren N. Svejcar, Chad S. Boyd & Kirk W. DaviesCollege of Science and Engineering, Flinders University, Bedford Park, South Australia, AustraliaMartin F. BreedDepartment of Animal and Range Sciences, New Mexico State University, Las Cruces, NM, USAAkasha M. FaistSchool of Natural Sciences and ARC Training Centre for Forest Value, University of Tasmania, Hobart, Tasmania, AustraliaPeter A. HarrisonProgram in Ecology, University of Wyoming, Laramie, WY, USAMichael F. CurranUSDA FS – Southern Research Station, Research Triangle Park, NC, USAQinfeng GuoDepartment of Nature Conservation and Landscape Planning, Anhalt University of Applied Sciences, Bernburg, GermanyAnita Kirmer & Sandra DullauSchool of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USADarin J. LawDepartment of Agricultural Sciences, South Eastern Kenya University, Kitui, KenyaKevin Z. MgangaUS Geological Survey, Southwest Biological Science Center, Flagstaff, AZ, USASeth M. Munson & Hannah L. FarrellUS Department of Agriculture – Agricultural Research Service Rangeland Resources and Systems Research Unit, Fort Collins, CO, USALauren M. PorenskyInstituto Nacional de Tecnología Agropecuaria, Estación Experimental Agropecuaria Catamarca, Catamarca, ArgentinaR. Emiliano QuirogaCátedra de Manejo de Pastizales Naturales, Facultad de Ciencias Agrarias, Universidad Nacional de Catamarca, Catamarca, ArgentinaR. Emiliano QuirogaMTA-DE Lendület Functional and Restoration Ecology Research Group, Debrecen, HungaryPéter TörökTennessee Department of Environment and Conservation, Division of Water Resources, Nashville, TN, USAClaire E. WainwrightHirola Conservation Programme, Nairobi, KenyaAli AbdullahiUSDA Natural Resources Conservation Service, Merced Field Office, Merced, CA, USAMatt A. BahmNational Park Service, Southeast Utah Group, Moab, UT, USAElizabeth A. BallengerThe Nature Conservancy of Oregon, Burns, OR, USAOwen W. BaughmanPlant Conservation Unit, Biological Sciences, University of Cape Town, Rondebosch, South AfricaCarina BeckerUniversity of Castilla-La Mancha, Campus Universitario, Albacete, SpainManuel Esteban Lucas-BorjaUniversity of Northern British Columbia, 3333 University Way, Prince George, British Columbia, CanadaCarla M. Burton & Philip J. BurtonInstitute of Applied Sciences, Malta College for Arts, Sciences and Technology, Fgura, MaltaEman Calleja & Alex CaruanaPlant Conservation Unit, Department of Biological Sciences, University of Cape Town, Rondebosch, South AfricaPeter J. CarrickUSDA, Agricultural Research Service, Great Basin Rangelands Research Unit, Reno, NV, USACharlie D. ClementsLendület Seed Ecology Research Group, Institute of Ecology and Botany, Centre for Ecological Research, Debrecen, HungaryBalázs Deák, Réka Kiss & Orsolya ValkóMurrang Earth Sciences, Ngunnawal Country, Canberra, Australian Capital Territory, AustraliaJessica DrakeGreat Ecology, Denver, CO, USAJoshua EldridgeUSDA-ARS Pest Management Research Unit, Northern Plains Agricultural Research Laboratory, Sidney, MT, USAErin EspelandGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyMagda GarbowskiDepartment of Ecology, Brandenburg University of Technology, Cottbus, GermanyEnrique G. de la RivaBiodiversity Management Branch, Environmental Resource Management Department, Cape Town, South AfricaPenelope A. GreyGreening Australia, Melbourne, Victoria, AustraliaBarry HeydenrychDepartment of Conservation Ecology & Entomology, Stellenbosch University, Stellenbosch Central, Stellenbosch, South AfricaPatricia M. HolmesNatural Resource Management and Environmental Sciences, Cal Poly State University, San Luis Obispo, CA, USAJeremy J. JamesDepartment of Biology, University of Nebraska-Kearney, Kearney, NE, USAJayne Jonas-BrattenNegaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, Glencoe, IL, USAAndrea T. KramerDepartment of Botany, University of Granada, Granada, SpainJuan LoriteInteruniversity Institute for Earth System Research, University of Granada, Granada, SpainJuan LoriteNew Zealand Department of Conservation, Christchurch, New ZealandC. Ellery MayenceDepartamento de Biología y Geología, Física y Química inorgánica, ESCET, Universidad Rey Juan Carlos, Madrid, SpainLuis Merino-MartínÖMKi – Research Institute of Organic Agriculture, Budapest, HungaryTamás MigléczHadison Park, Kimberley, South AfricaSuanne Jane MiltonWolwekraal Conservation and Research Organisation (WCRO), Prince Albert, South AfricaSuanne Jane MiltonUS Department of Agriculture, Agricultural Research Service, Forage and Range Research Laboratory, Utah State University, Logan, UT, USAThomas A. MonacoUniversity of California, Riverside, Riverside, CA, USAArlee M. MontalvoDepartment of Environment and Agronomy, National Institute for Agricultural and Food Research and Technology (INIA-CSIC), Madrid, SpainJose A. Navarro-CanoForest and Rangeland Stewardship Department, Colorado State University, Fort Collins, CO, USAMark W. PaschkeInstituto Nacional de Tecnología Agropecuaria (INTA), Universidad Nacional de la Patagonia Austral (UNPA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Santa Cruz, ArgentinaPablo Luis PeriUSDA – NRCS, Bozeman, MT, USAMonica L. PokornyUSDA Agricultural Research Service, Fort Keogh Livestock and Range Research Laboratory, Miles City, MT, USAMatthew J. RinellaPlant Science, Western Cape Department of Agriculture, Elsenburg, South AfricaNelmarie SaaymanRed Rock Resources LLC, Miles City, MT, USAMerilynn C. SchantzBush Heritage Australia, Eurardy, Western Australia, AustraliaTina ParkhurstDeptartment of Ecology, Evolution, and Behavior, University of Minnesota, St Paul, MN, USAEric W. SeabloomHolden Arboretum, Kirtland, OH, USAKatharine L. StubleDepartment of Natural Resources and Environmental Science, University of Nevada, Reno, NV, USAShauna M. UselmanDepartment of Wildland Resources & Ecology Center, Utah State University, Logan, UT, USAKari VeblenDepartment of Biology, University of Regina, Regina, Saskatchewan, CanadaScott WilsonCentre of eResearch and Digital Innovation, Federation University Australia, Ballarat, Victoria, AustraliaMegan WongSchool of Geography and Ocean Science, Nanjing University, Nanjing, ChinaZhiwei XuInstitute of Arctic and Alpine Research, University of Colorado Boulder, Boulder, CO, USAKatharine L. Suding More

  • in

    Climatic suitability of the eastern paralysis tick, Ixodes holocyclus, and its likely geographic distribution in the year 2050

    Tick paralysis is a common tick-borne illness in humans and animals throughout the world, caused by neurotoxins produced in the salivary glands of ticks and secreted into a host during the course of feeding by females and immature stages19. Fifty-nine ixodid and fourteen argasid ticks are currently believed to be involved in the transmission of tick paralysis worldwide19, 20. In Australia, I. holocyclus is considered to be the leading tick species implicated in the transmission of tick paralysis primarily in dogs, but also other species, viz. cats, sheep, cattle, goats, swine and horses. Humans are also occasionally affected, and the disease can be fatal2, 21. A second tick species, I. cornuatus has also been implicated in the transmission of tick paralysis in Australia; however, it is also considered a minor player in this disease22. Given the differences in their biology, distribution, and natural history of these two species, we focused on estimating the spatial distribution of I. holocyclus in the present study. We recognize, however, that it is important to consider the distributions of both species for proper epidemiological planning and management of tick paralysis in Australia.Ecological niche modeling is a well-tested approach for estimating species distributions based on abiotic factors13, 23. Several new recommendations have been made in recent years for proper construction of niche models; such as the appropriate thinning of occurrence data24, consideration of an accessible area for a species being studied (M)25, thorough exploration of model complexity26, 27, and use of multiple statistical criteria for model selection28, 29. We carefully considered all these recommendations to produce a robust spatial distribution model for I. holocyclus. The resulting replicated models were fairly consistent in predicting suitability for I. holocyclus, as indicated by moderate range estimates (Fig. 2B). Further, the MOP analysis indicated satisfactory performance of the present-day model with extrapolation only in small areas outside the predicted suitable areas. These qualities, along with the model’s very low omission rate (0.044%) gives high confidence in the predicted suitable area for this species in Australia. It will be essential, however, to confirm the actual presence of I. holocyclus outside the traditionally known areas through acarological surveys to assess our findings.The present-day spatial distribution predicted in this study (Fig. 2A) indicates that the geographic areas suitable for I. holocyclus match the currently known distribution of this species along the eastern seaboard, but the suitability also extends through most of the coastal areas in the south, and up to the Kimbolton Peninsula in Western Australia in the north. Highly suitable areas are present around and south of Perth, extending towards Albany, Western Australia. Most areas in Tasmania are also highly suitable for this species. The current distribution in the Eastern Seaboard may be wider than the traditionally known extents in some areas compared to Roberts30. It is likely that I. holocyclus will succeed in establishing permanent populations if introduced into areas that are currently free of them along the southern and northern coasts, and along the southwestern coast of Western Australia and Tasmania. Appropriate prevention of tick movement including pet inspections and quarantine will be necessary to avoid introductions.Future potential distribution of I. holocyclus in year 2050 based on both low- and high-emissions scenarios indicate moderate increases in climatic suitability from the present-day prediction (Fig. 4A,B); but noticeably also moderate to low loss of climatically suitable areas in 2050. This loss could be at least partly attributed to potential future temperature and precipitation conditions exceeding suitable ranges for these ticks in these areas, limiting their ability to survive. Predicted loss of suitable areas in future can also be observed to be irregular, and in some areas, particularly along northern Queensland and in Northern Territory, enveloped between stretches of suitable areas. Our use of relatively coarse resolution data (1 km2) limits our ability to thoroughly interpret such phenomenon, but this is likely due to variations in the geography in these areas that respond differently to future climate, as well as the potential increase in ocean temperature and subsequent influences on areas along the coast that may render them unsuitable for this species. Despite the noticeable loss in climatically suitable areas, likely no net loss in area will accrue for this species by 2050.Teo et al.31 assessed present and future potential distribution for I. holocyclus using both CLIMEX32, 33 and a novel, as-yet unpublished “climatic-range” approach to determine the suitability on monthly intervals. CLIMEX allows users to specify different upper and lower thresholds for climatic parameters, some of which were derived for their study from laboratory evaluations of I. holocyclus34. The present-day distribution reported in that study resembles our results in identification of a relatively narrow area along the East Coast as suitable; however, much of the northern and northeastern areas along the coast, the coasts of South Australia and southwestern Australia, and Tasmania are reported unsuitable. Their future predictions (2050) of the species’ potential distribution were based on two GCMs (CSIRO MK3 and MIROC-H) climate models, were also markedly different from our predictions, anticipating rather dramatic distributional loss for the species. Such model transfers are challenging, with many factors potentially producing inconsistencies35. However, the two studies reflect two fundamentally different classes of ecological niche models; CLIMEX is deterministic, whose predictions are largely constrained by user supplied threshold values for model inputs of physiological tolerance limits of a species33, whereas Maxent is a machine-learning correlative approach, in which known occurrences of a species is used in conjunction with environmental layers to determine conditions that meet a species’ environmental requirements, and therefore the suitability of geographic spaces. Although the former (CLIMEX) approach is appealing conceptually, scaling environmental dimensions between the micro-scales of physiological measurements and the macro-scales of geography is well-known to present practical and conceptual challenges36.Different ixodid ticks employ different life-history strategies in response to adverse environmental conditions, including behavioral adaptations, active uptake of atmospheric moisture, restriction of water-loss, and tolerance towards extreme temperatures37. Precisely which of these mechanisms I. holocyclus utilizes, if any at all, for its survival during diverse temperature and humidity conditions is not clearly known, but it is likely to involve multiple mechanisms. In this sense, the threshold values used by Teo et al.31, based purely on laboratory observations may have been overly restrictive, leading to a conservative distributional estimate for this species. Further, because relationships between abiotic variables and species’ occurrences are fairly complex and highly dimensional, a physiological thresholding approach wherein values are set independently for different abiotic parameters may not capture species’ relationships with environments adequately. The correlative approaches employed in the present study are data-driven, and as such may capture more of this complexity, with fewer problems of scaling across orders of magnitude of space and time.In conclusion, ticks are poikilothermic ectoparasites, whose survival, reproduction and other biological functions are regulated by ambient climatic conditions. Although ixodid ticks are known to regulate their body temperatures by moving about their habitat (vegetation), attempts to model their spatial distribution has resulted in models largely based on climate variables. Nevertheless, other factors such as host availability play a significant role in tick distribution, which unfortunately cannot be readily included in correlative ecological niche models largely because such data are rarely available. These suitability predictions, in addition to being entirely based on large-scale climate, also do not reveal the highly likely heterogeneity in abundance or density in different geographic areas within the realized climatically suitable areas. For these reasons, the distribution maps produced in this study must be used with some caution, and perhaps as a guide to target sampling and not as a substitute for thorough acarological surveys. More

  • in

    Mangroves and coastal topography create economic “safe havens” from tropical storms

    Data constructionWe construct an annual panel dataset from 2000 to 2012 of 2549 coastal communities within 102 countries. Population counts from 2000 to 2012 for each community were calculated from the Landscan population database27 and coastal communities were defined as the lowest level administration units with an ocean coastline of each country using the Global Administrative Areas Database v2.7. Using the National Oceanic and Atmospheric Administration’s (NOAA) global nighttime lights data, we examine trends in economic activity before and after a cyclone event. The growth rate in average annual luminosity from nighttime lights trends with economic growth and has been used as an effective proxy for local economic activity22,24,28,29,30,31,32.However, trends in nighttime luminosity should not be interpreted as a measure of economic growth. Instead, we focus on tracking the dynamic impacts of nighttime luminosity (e.g. deviations from trends) that indicates whether an exposed community’s economic activity recovers or suffers permanent damage. The average elevation of each coastal community was calculated using a void-filled Shuttle Radar Topography Mission (SRTM) data at 3 arc-seconds, or approximately 90 m2 at the equator33. The SRTM has the potential to result in an overestimation of elevation in heavily built environment areas or areas of dense high forest canopies compared against locations without such trees. However, during the timeframe of our analysis, the SRTM product was the most appropriate and available product.The mangrove coverage dataset was adapted from the Continuous Global Mangrove Forest Cover for the 21st Century (CGMFC-21) database for the years 2000 to 201212. The coastline length of each community, based on Global Self-Consistent, Hierarchical, High-Resolution Shoreline Database v2.3.5 full resolution data34, was used to normalize the area of mangroves offshore of each coastal community creating a measurement for the “width” of mangroves per meter of coastline.Tropical storm locations for all years were recreated from the International Best Track Archive for Climate Stewardship (IBTrACS) Annual Tropical Cyclone Best Track Database35. Precise measurements of exposure, combined with high-resolution luminosity data, allows to distinguish the heterogeneous impacts of cyclones on exposed communities and the capacity for mangroves to shelter coastal economic activity at different elevations and for different mangrove widths. The intensity of exposure is measured by the distance of the cyclone’s “eye” from the exposed village’s nearest boundary.Tropical cyclone wind profile36, villages passing within 100 km of the cyclone’s eye were likely to experience maximum wind velocity and surface level pressure whereas those villages passing within more distant bands—i.e., 100–200 km and 200–300 km, were likely to experience similar surface level pressure but a non-linear reduction in wind velocity. Binning wind velocities in this way recognizes the highly non-linear relationship between wind velocity and on-the-ground damages from cyclone events37. We therefore expect the capacity for mangroves and elevation to shelter economic activity also to depend on this intensity of exposure.Our full sample encompasses nearly 400 million individuals in 102 countries and 2549 mangrove-holding communities (Table 1). Based on 2019 fiscal year World Bank categorizations, most of our sample resides in developing countries (85.1%) with 46.7% in lower-middle income (gross national income/per capita between $996 and $3895) and 35.3% in upper-middle income countries (gross national income/ per capita between $3896 and $12,056). We also find that most mangrove coverage in our sample exists within developing countries (88.7%) and overwhelmingly in upper-middle income countries (56.0%) in the Latin America and Caribbean (LAC) and East Asian and Pacific (EAP) developing regions. While only 14.9% of our sample’s global population resides in LAC countries, these countries account for 39.8% of mangrove holdings in our sample whereas the 45.5% of the population residing in EAP countries only account for 30.3% of mangrove coverage.Empirical strategyWe use a distributed-lag autoregressive model to measure the initial and permanent effect of cyclone exposure on economic activity in coastal communities. The growth in economic activity for each coastal community is proxied by the difference in logs between years, (growth={ln}left(luminosit{y}_{t}right)-{ln}left(luminosit{y}_{t-1}right)). Our estimating equation is$$growt{h}_{i,j,t}=sumlimits_{L=0}^{n}{[beta }_{L} x {C}_{i,j,t-L}]+{gamma }_{j}+{delta }_{t}+eta {X}_{i,j,t}+{epsilon }_{i,j,t}$$
    (1)

    where the (beta) coefficients capture the marginal effects, across three bins of cyclone exposure, on the growth rate of luminosity for the (j{^{prime}}th) administrative unit, within country (i), and in time (t-L) where (t) is the observed year and L is the number of lags ranging from (0 ; to ;n). Here, ({C}_{i,j,t}) is a vector of cyclone exposures binned by the distance from the cyclone’s “eye” to the nearest boundary of the exposed community ( More

  • in

    Study on environmental behaviour of fluopyram in different banana planting soil

    Chemicals and reagentsThe fluopyram standard was purchased from the Environmental Protection Monitoring Institute of the Ministry of Agriculture of China at a concentration of 1000 mg/L. Analytical grade acetonitrile, acetone, dichloromethane, and sodium chloride were purchased from the Guangzhou Chemical Reagent Factory. Chromatographic grade Methanol and n-hexane were available from Thermo Fisher Scientific. Purified water was prepared using a Milli-Q reverse osmosis system (Millipore, Milford, MA, USA). Strata Florisil (FL-PR) 500 mg/6 mL SPE manufactured by Strata™ (5.0 mL n-hexane–acetone (9:1, V/V) solution pre-rinsing cartridge).A standard solution of 1000 μg/mL fluopyram was diluted in n-hexane, and the matrix extract of the blank sample was obtained by the extraction method. The matrix standard solutions of 0.025, 0.05, 0.10, 0.15 and 0.50 μg/mL were obtained by the step dilution. All prepared solutions were stored at temperature of 4 °C until further use.Soil sample collectionHainan latosol was collected from the Bailian banana experimental base in Chengmai (Hainan), Yunnan sandy soil was collected from Taoyuan banana experimental base in Longtou Street, Kunming (Yunnan) and Fujian plain alluvial soil was collected from the Zhangzhou banana experimental base (Fujian). 5–10 soil sampling points were randomly selected in each banana experimental base; the soil samples were collected from depths of 0–10 cm, and debris such as gravel, weeds, and plant roots were removed from each sample. The soil samples were obtained by the quarter method after mixing, dried, and stored after 20 mesh screening.Extraction and purification of flupyramSoil sample extraction was conducted as follows: in a 200 mL conical flask, 20.0 g of the drying soil sample and 40.0 mL acetonitrile was added. After shaking on a reciprocating shaker for 2 h, the mixture was filtered through filter paper. The filtrate was transferred to a stoppered measuring cylinder with 6.0 g NaCl. The stopper was inserted, and the mixture was vigorously shaken for 2 min. The mixture was left at 25 ± 2 °C for more than 30 min to separate the acetonitrile and aqueous solutions. Meanwhile, 10.0 mL of the supernatant were accurately transferred into a 100 mL round-bottom flask and concentrated by a rotatory evaporator at 40 °C to near dryness, which was dissolved in a 5.0 mL n-hexane–acetone (9:1, v/v) solution, vortexed, and mixed well for purification.Water sample extraction is shown below. A 20 mL water sample was transferred to a separatory funnel with 40.0 mL dichloromethane. After vigorously shaking it for 2 min and then letting it stand for 30 min, the lower layer solution was collected in a 100 mL round-bottom flask. The collected fluid was concentrated by a rotatory evaporator at 40 °C to near dryness and dissolved in 5.0 mL n-hexane–acetone (9:1, v/v) solution, vortexed, and mixed well for purification.Sample purification is described below. A 5.0 mL n-hexane–acetone (9:1, v/v) was used to preach the Strata Florisil (FL-PR) 500 mg/6 mL extraction column. When the leaching solvent level reached the surface of the column adsorption layer, the solution sample was immediately poured into the column be purified. Then, the purified solution was collected in a 100 mL round-bottom flask. A 5.0 mL n-hexane–acetone (9:1, v/v) solution was used to rinse the round-bottom flask residuum, after which the rinse solution was applied to elute the Florisil column. The rinsing and elution steps were repeated three times. The collected fluid was concentrated by a rotatory evaporator at 40 °C to near dryness and dissolved in 2.5 mL n-hexane for analysis.Instrumental conditionThe test was performed using the Theomer DSQII gas chromatography-mass spectrometer (GC–MS) with Xcalibur 2.0, software for data acquisition and analysis. A SLB-5MS analytical column (30 m × 0.25 mm × 0.25 μm) was used as chromatographic column. The injection volume was 1 μL without split injection, the carrier gas was helium (He, ≥ 99.999% purity), and the carrier gas flow rate was set to 1.0 mL/min. The protective gas was nitrogen (N2, ≥ 99.999% purity), and the injection port temperature was 250 °C. The chromatographic column temperature program was set as follows: the initial temperature at 80 °C was maintained for 1 min; then it was raised to 240 °C at a speed of 20 °C/min and maintained for 3 min; finally, the temperature was raised at a rate of 50 °C/min until 280 °C, where it was maintained for 7 min.The MS was operated in electron ionisation (EI) mode with an ionising energy of 70 eV. MS data were acquired in both full scan (m/z 50–500) mode for identification and selected ion monitoring (SIM) mode for quantification. The temperatures of the ion source and transfer line were 250 °C and 280 °C, respectively. The retention time of fluopyram was 10.59 min. The quantifier ions were m/z 223, and the qualifier ions were m/z 195 and m/z 173.Analytical method validationFirst, we addressed the linearity. The matrix standard of fluopyram was prepared in the range of 0.025–0.50 μg/mL and the determination was carried out, with the concentration of fluopyram matrix standard solution as the abscissa and the peak area obtained from the GC–MS as the ordinate. Linearity was calculated by plotting the relationship between the concentration and the peak area.The sensitivity analysis relied on the LOD and the limit of quantitation (LOQ). To evaluate the sensitivity of the method, they were obtained by adding the standard solution of fluopyram at the lowest concentration level in line with the requirements of the analytical method for blank samples. The LOD was the corresponding concentration when the signal-to-noise ratio (S/N) was 3, and S/N = 10 corresponds to the LOQ.Accuracy and precision were estimated as well. To determine the reliability of the method, fluopyram standard solutions with different concentrations were added to the blank sample for the recovery experiment. Fluopyram standard solutions with concentrations of 0.008, 0.600, and 1.000 mg/kg were added to the blank samples. This procedure was repeated five times for each concentration. The samples were subjected to extract, purify and analysis under the method the same conditions as described above. The recovery was calculated for the accuracy of the method, and the RSD was calculated for the precision.Soil dissipation experimentIn a number of 100 mL clean and sterilized conical flasks with covers, 20.0 g of soil was added (net weight converted by water content); then, 0.1 mL 1000 μg/mL fluopyram standard solution was pipetted into the conical flasks. Ultrapure water was added. The water was controlled to occupy 60% of the total volume. The flasks were shaken on a constant temperature oscillator for 2 min to mix the fluopyram evenly. Then, they were placed in an artificial climate incubator and exposed to light at 25 ± 2 °C for 12 h per day. According to the different soil types, they were divided into three treatment groups: Hainan, Yunnan, and Fujian. Each treatment group had three parallels and three blanks. The detection intervals were 2 h, 1, 3, 7, 14, 21, 28, 42 and 60 day, while the detection of fluopyram was performed based on the interval according to the shown methods. The dissipation kinetics of fluopyram in banana planting soil conformed to the first-order kinetic equation Ct = C0e−kt, where Ct is a pesticide concentration (mg/kg) at different times (day), C0 is an initial concentration (mg/kg), and k is the dissipation rate constant. The half-life of fluopyram is determined using Eq. (1).$$T_{1/2} = , ln 2/k$$
    (1)
    Soil adsorption experimentUsing the oscillation balance method, 5.0 g of soil was put into the 250 mL conical flasks with cover, which contained 25 mL fluopyram aqueous solutions with mass concentrations of 0.02, 0.1, 0.5, 2.5 and 4.0 mg/L (containing 0.01 mol/L CaCl2), respectively. The soils were divided into three treatment groups: Hainan, Yunnan, and Fujian (based on the different soil types). The fluopyram aqueous solution and the blank soil aqueous solution (both containing 0.01 mol/L CaCl2) were used as controls. Each treatment group had three replicates. The conical flasks were then placed in a constant temperature oscillator at 25 ± 2 °C for 24 h to prepare the suspension. The suspension was transferred to a centrifuge tube for high-speed centrifugation, and 80% of the total volume of the supernatant was used for determination. The fluopyram in the supernatant was extracted and determined under the methods as described above, and the Freundlich equation model (see Eq. 2) was used to describe the adsorption law for fluopyram in soil.$${text{Freundlich: }}C_{s} = K_{f} times C_{e}^{1/n}$$
    (2)
    where Cs is adsorption content of pesticide in soil (mg/kg), Ce is concentration of the pesticide in aqueous solution at adsorption equilibrium (mg/L), Kf is the soil adsorption coefficient of the Freundlich model (L/kg), indicating the pesticide adsorption capacity of the soil and 1/n is a slope rate of the curve between Cs and Ce, reflecting the heterogeneity of the adsorbent surface.The relationship between the adsorption free energy of soil to pesticides (ΔG, kJ/mol) and the soil adsorption coefficient Koc is expressed using Eq. (3).$$Delta G , = – RTln K_{oc}$$
    (3)
    where Koc is the soil adsorption coefficient (Koc = Kf/OC × 100) expressed by organic carbon content (L/kg), OC is soil organic carbon content (%), R is the molar gas constant (J/K mol), and T is absolute temperature (K).Soil leaching experimentA plexiglass tube with an inner diameter of 5 cm and a length of 40 cm was used as a packed column. A layer of cotton, a 1 cm thick quartz sand layer, and a layer of filter paper were added at the bottom of the column. Dry soil (700–800.0 g) was weighed for filling, and the column was fully wetted with ultrapure water to prepare a 30 ± 0.2 cm high leaching soil column. 0.1 mL of 1000 μg/mL fluopyram solution was further added to 5.0 g of soil. After the solution completely volatilized, it was evenly spread on the top of the soil column, and a layer of filter paper and a layer of 1 cm thick quartz sand were added to the top of the soil. During the test, ultrapure water was used for washing the soil column for 10 h at a speed of 30 mL/h, and the leaching solution was collected. After washing, the soil column was removed and was cut into four sections of 1–5, 5–10, 10–20 and 20–30 cm. The residues of fluopyram in the soil samples and leaching solutions were extracted and determined under the methods as described above. According to the three soil types, they were divided into Hainan, Yunnan and Fujian treatment groups, where each group received another parallel treatment. More

  • in

    Comparative assessment of amino acids composition in two types of marine fish silage

    Degree of hydrolysisOrganic silages prepared from fat fish (FFS) and lean fish (LFS) had a characteristic tawny brown colour which was accompanied with a strong characteristic salty-fishy odour. At the end of 5 DoF, both FFS and LFS exhibited sluggish liquefaction which increased progressively concomitant with the DoF (Table S1). Liquefaction is an indicator of tissue hydrolysis due to the action of acid. During 35 DoF, the degree of hydrolysis (measured in terms of liquefaction volume) increased progressively with the DoF in both types of ensilages and was relatively higher in LFS compared to FFS on all sampled DoF (Table S1). In general, lipolysis supersedes the proteolysis in all major biochemical processes23. A relatively higher degree of hydrolysis recorded in LFS may be attributed to the presence of a greater proportion of light muscles compared to dark muscles. Relatively greater susceptibility of light muscles to hydrolysis compared to dark muscles might be due to lower lipid content in the former23.Irrespective of fish type, the measured pH values in both types of ensilages (FFS and LFS) were similar (data not shown) and the values showed a progressive increase from 1.0 ± 0.03 (0 DoF) to 6.0 ± 0.03 (35 DoF). Such an increasing trend in pH with the advancement in DoF could be attributable to gradual solubilisation of boney material with the advancement fermentation time24,25,26.Changes in principal biochemical constituentsDuring the 35 DoF, the concentrations of total protein (TP) in both FFS and LFS progressively increased with the DoF and showed significant differences with the advancement of DoF (p  phenylalanine (2.6 ± 0.033)  > serine (2.4 ± 0.033)  > aspartic acid (2.3 ± 0.033)  > alanine (2.1 ± 0.033)  > histidine (1.8 ± 0.033)  > valine (1.6 ± 0.033)  > methionine (1.5 ± 0.033)  > isoleucine (1.5 ± 0.033)  > threonine (1.4 ± 0.033)  > cysteine (0.946 ± 0.033).Figure 1Composition of total amino acids (mg/g) in two types of fish ensilages (FFS—fat fish silage; LFS—lean fish silage) during 35 days of fermentation (DoF). Data are mean ± SD. * p  glutamic acid (4.97 ± 0.033)  > arginine (4.5 ± 0.033)  > phenylalanine (3.38 ± 0.033)  > aspartic acid (2.92 ± 0.033)  > alanine (2.23 ± 0.033)  > methionine (2.19 ± 0.033)  > lysine (1.882 ± 0.033)  > serine (1.881 ± 0.033)  > tyrosine (1.410 ± 0.033)  > glycine (1.219 ± 0.033)  > threonine (0.953 ± 0.033)  > valine (0.945 ± 0.033)  > isoleucine (0.864 ± 0.033)  > histidine (0.417 ± 0.033).A comparative assessment of profiles of TAA in both FSS and LFS during all DoF revealed a similar pattern, albeit with obvious differences in the concentration of few amino acids (Fig. 1). It has been hypothesised that the occurrence of decarboxylation that follows transamination of amino acids as a consequence of increase in pH during fermentation is known to cause a decrement in the concentration of few amino acids, especially valine and isoleucine34. During the present study, the concentrations of histidine, valine, isoleucine, glycine and lysine were significantly higher (p  leucine (3.09 ± 0.003)  > glutamic acid (2.61 ± 0.003)  > alanine (1.83 ± 0.003)  > phenylalanine (1.79 ± 0.003)  > cysteine (1.67 ± 0.003)  > histidine (1.56 ± 0.003)  > aspartic acid (1.54 ± 0.003)  > serine (1.32 ± 0.003)  > lysine (1.16 ± 0.003)  > threonine (1.09 ± 0.003)  > valine (1.07 ± 0.003)  > isoleucine (1.06 ± 0.003) followed by methionine (0.93 ± 0.003)  > tyrosine (0.92 ± 0.003)  > tryptophan (0.72 ± 0.003)  > asparagine (0.57 ± 0.003)  > glutamine (0.15 ± 0.003).Figure 2Composition of free amino acids (mg/g) in two types of fish ensilages (FFS—fat fish silage; LFS—lean fish silage) during 35 days of fermentation (DoF). Data are mean ± SD. * p  More

  • in

    Early life neonicotinoid exposure results in proximal benefits and ultimate carryover effects

    1.Mineau, P. & Palmer, C. Neonicotinoid Insecticides and Birds: The Impact of the Nation’s Most Widely Used Insecticides on Birds. (American Bird Conservancy, USA, 2013).2.Simon-Delso, N. et al. Systemic insecticides (Neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. 22, 5–34. https://doi.org/10.1007/s11356-014-3470-y (2015).CAS 
    Article 

    Google Scholar 
    3.Jeschke, P., Nauen, R., Schindler, M. & Elbert, A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 59, 2897–2908. https://doi.org/10.1021/jf101303g (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Tomizawa, M. & Casida, J. E. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotining receptors. Annu. Rev. Entomol. 48, 339–364. https://doi.org/10.1146/annurev.ento.48.091801.112731 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    5.Woodcock, B. A. et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 1–8. https://doi.org/10.1038/ncomms12459 (2016).CAS 
    Article 

    Google Scholar 
    6.Pisa, L. et al. An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: Impacts on organisms and ecosystems. Environ. Sci. Pollut. Res. 28, 1–49. https://doi.org/10.1007/s11356-017-0341-3 (2017).CAS 
    Article 

    Google Scholar 
    7.Li, Y., Miao, R. & Khanna, M. Neonicotinoids and decline in bird biodiversity in the United States. Nat. Sustain. 3, 1027–1035. https://doi.org/10.1038/s41893-020-0582-x (2020).Article 

    Google Scholar 
    8.Eng, M. L., Stutchbury, B. J. & Morrissey, C. A. Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Sci. Rep. 7, 1. https://doi.org/10.1038/s41598-017-15446-x (2017).CAS 
    Article 

    Google Scholar 
    9.Eng, M. L., Stutchbury, B. J. & Morrissey, C. A. A neonicotinoid insecticide reduces fueling and delays migration in songbirds. Science 80(365), 1177–1180. https://doi.org/10.1126/science.aaw9419 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Lopez-Antia, A., Ortiz-Santaliestra, M. E., Mougeot, F. & Mateo, R. Imidacloprid-treated seed ingestion has lethal effect on adult partridges and reduces both breeding investment and offspring immunity. Environ. Res. 136, 97–107. https://doi.org/10.1016/j.envres.2014.10.023 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Pandey, S. P. & Mohanty, B. The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide mancozeb disrupt the pituitary-thyroid axis of a wildlife bird. Chemosphere 122, 227–234. https://doi.org/10.1016/j.chemosphere.2014.11.061 (2015).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    12.Tokumoto, J. et al. Effects of exposure to clothianidin on the reproductive system of male quails. J. Vet. Med. Sci. 75, 755–760. https://doi.org/10.1292/jvms.12-0544 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Addy-Orduna, L. M., Brodeur, J. C. & Mateo, R. Oral acute toxicity of imidacloprid, thiamethoxam and clothianidin in eared doves: A contribution for the risk assessment of neonicotinoids in birds. Sci. Total Environ. 650, 1216–1223. https://doi.org/10.1016/j.scitotenv.2018.09.112 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Berheim, E. H. et al. Effects of Neonicotinoid Insecticides on Physiology and Reproductive Characteristics of Captive Female and Fawn White-tailed Deer. Sci. Rep. 9, 1–10. https://doi.org/10.1038/s41598-019-40994-9 (2019).CAS 
    Article 

    Google Scholar 
    15.Wang, Y. et al. Unraveling the toxic effects of neonicotinoid insecticides on the thyroid endocrine system of lizards. Environ. Pollut. 258, 113731. https://doi.org/10.1016/j.envpol.2019.113731 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    16.Khalil, S. R., Awad, A., Mohammed, H. H. & Nassan, M. A. Imidacloprid insecticide exposure induces stress and disrupts glucose homeostasis in male rats. Environ. Toxicol. Pharmacol. 55, 165–174. https://doi.org/10.1016/j.etap.2017.08.017 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    17.Abou-Donia, M. B. et al. Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. J. Toxicol. Environ. Heal. – Part A Curr. Issues 71, 119–130. https://doi.org/10.1080/15287390701613140 (2008).CAS 
    Article 

    Google Scholar 
    18.Gawade, L., Dadarkar, S. S., Husain, R. & Gatne, M. A detailed study of developmental immunotoxicity of imidacloprid in Wistar rats. Food Chem. Toxicol. 51, 61–70. https://doi.org/10.1016/j.fct.2012.09.009 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    19.Mohanty, B., Pandey, S. P. & Tsutsui, K. Thyroid disrupting pesticides impair the hypothalamic-pituitary-testicular axis of a wildlife bird. Amandava amandava. Reprod. Toxicol. 71, 32–41. https://doi.org/10.1016/j.reprotox.2017.04.006 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Sun, Q. et al. Imidacloprid Promotes High Fat Diet-Induced Adiposity in Female C57BL/6J Mice and Enhances Adipogenesis in 3T3-L1 Adipocytes via the AMPK(alpha)-Mediated Pathway. J. Agric. Food Chem. 65, 6572–6581. https://doi.org/10.1021/acs.jafc.7b02584 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Sun, Q. et al. Imidacloprid promotes high fat diet-induced adiposity and insulin resistance in male C57BL/6J mice. J. Agric. Food Chem. 64, 9293–9306. https://doi.org/10.1021/acs.jafc.6b04322 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Park, Y. et al. Imidacloprid, a neonicotinoid insecticide, potentiates adipogenesis in 3T3-L1 adipocytes. J. Agric. Food Chem. 61, 255–259. https://doi.org/10.1021/jf3039814 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    23.Ricklefs, R. E., Stark, J. M. & Konarzewski, M. Internal constraints on growth in birds. in Avian Growth and Development. Evolution within the Altricial-Precocial Spectrum (eds Starck, J. M. & Ricklefs, R.E.) 266–287 (Oxford Ornithology Series, Oxford, 1998).
    Google Scholar 
    24.Bobek, S., Jastrzebski, M. & Pietras, M. Age-related changes in oxygen consumption and plasma thyroid hormone concentration in the young chicken. Gen. Comput. Endocrinol. 31, 169–174. https://doi.org/10.1016/0016-6480(77)90014-4 (1977).CAS 
    Article 

    Google Scholar 
    25.Metcalfe, N. B. & Monaghan, P. Compensation for a bad start: Grow now, pay later?. Trends Ecol. Evol. 16, 254–260. https://doi.org/10.1016/S0169-5347(01)02124-3 (2001).Article 
    PubMed 

    Google Scholar 
    26.Criscuolo, F., Monaghan, P., Nasir, L. & Metcalfe, N. B. Early nutrition and phenotypic development: “catch-up” growth leads to elevated metabolic rate in adulthood. Proc. Biol. Sci. 275(1642), 1565–1570. https://doi.org/10.1098/rspb.2008.0148 (2008).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Monaghan, P. Early growth conditions, phenotypic development and environmental change. Philos. Trans. R. Soc. B Biol. Sci. 363, 1635–1645. https://doi.org/10.1098/rstb.2007.0011 (2008).Article 

    Google Scholar 
    28.Lee, W. S., Monaghan, P. & Metcalfe, N. B. The pattern of early growth trajectories affects adult breeding performance. Ecology 93, 902–912. https://doi.org/10.1890/11-0890.1 (2012).Article 
    PubMed 

    Google Scholar 
    29.Zera, A. J. & Harshman, L. G. The Physiology of Life History Trade-Offs in Animals. Annu. Rev. Ecol. Syst. 32, 95–126. https://doi.org/10.1146/annurev.ecolsys.32.081501.114006 (2001).Article 

    Google Scholar 
    30.Botías, C., David, A., Hill, E. M. & Goulson, D. Quantifying exposure of wild bumblebees to mixtures of agrochemicals in agricultural and urban landscapes. Environ. Pollut. 222, 73–82. https://doi.org/10.1016/j.envpol.2017.01.001 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Hladik, M. L. & Kolpin, D. W. First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA. Environ. Chem. 13, 12. https://doi.org/10.1071/EN15061 (2016).CAS 
    Article 

    Google Scholar 
    32.Morrissey, C. A. et al. Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: A review. Environ. Int. 74, 291–303. https://doi.org/10.1016/j.envint.2014.10.024 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    33.McNabb, F. M. A. The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit. Rev. Toxicol. 37(1–2), 163–193. https://doi.org/10.1080/10408440601123552 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    34.Gobeli, A., Crossley, D., Johnson, J. & Reyna, K. The effects of neonicotinoid exposure on embryonic development and organ mass in northern bobwhite quail (Colinus virginianus). Comp. Biochem. Physiol. Part – C Toxicol. Pharmacol. 195, 9–15. https://doi.org/10.1016/j.cbpc.2017.02.001 (2017).CAS 
    Article 

    Google Scholar 
    35.Mineau, P. & Callaghan, C. Neonicotinoid insecticides and bats: an assessment of the direct and indirect risks. (Canadian Wildlife Federation, 2018).36.Wilson, J. D., Morris, A. J., Arroyo, B. E., Clark, S. C. & Bradbury, R. B. A review of the abundance and diversity of invertebrate and plant foods of granivorous birds in northern Europe in relation to agricultural change. Agric. Ecosyst. Environ. 75, 13–30. https://doi.org/10.1016/S0167-8809(99)00064-X (1999).Article 

    Google Scholar 
    37.Peig, J. & Green, A. J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883–1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x (2009).Article 

    Google Scholar 
    38.Spencer, K., Buchanan, K., Goldsmith, A. & Catchpole, C. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44, 132–139. https://doi.org/10.1016/S0018-506X(03)00124-7 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Ayyanath, M.-M., Cutler, G. C., Scott-Dupree, C. D. & Sibley, P. K. Transgenerational Shifts in Reproduction Hormesis in Green Peach Aphid Exposed to Low Concentrations of Imidacloprid. PLoS One 8, e74532. https://doi.org/10.1371/journal.pone.0074532 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    40.Calabrese, E. J. & Baldwin, L. A. Toxicology rethinks its central belief. Nature 421, 691–692. https://doi.org/10.1038/421691a (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    41.Lopez-Antia, A., Ortiz-Santaliestra, M. E., Mougeot, F. & Mateo, R. Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology 22, 125–138. https://doi.org/10.1007/s10646-012-1009-x (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    42.Rix, R. R., Ayyanath, M. M. & Christopher Cutler, G. Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J. Pest Sci. (2004) 89, 581–589. https://doi.org/10.1007/s10340-015-0716-5 (2016).Article 

    Google Scholar 
    43.von Engelhardt, N. & Groothuis, T. G. G. Maternal hormones in avian eggs. in Hormones and Reproduction of Vertebrates: Birds, 1st edn. (eds Norris, D. & Lopez, K.) 91–127. https://doi.org/10.1016/C2009-0-01697-3 (Academic Press, 2011).Chapter 

    Google Scholar 
    44.Hulbert, A. J. Thyroid hormones and their effects: A new perspective. Biol. Rev. Camb. Philos. Soc. 75, 519–631. https://doi.org/10.1017/s146479310000556x (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    45.Darras, V. M. et al. Partial Food Restriction Increases Hepatic Inner Ring Deiodinating Activity in the Chicken and the Rat. Gen. Comp. Endocrinol. 100, 334–338. https://doi.org/10.1006/gcen.1995.1164 (1995).CAS 
    Article 
    PubMed 

    Google Scholar 
    46.Klandorf, H. & Harvey, S. Food intake regulation of circulating thyroid hormones in domestic fowl. Gen. Comp. Endocrinol. 60, 162–170. https://doi.org/10.1016/0016-6480(85)90310-7 (1985).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Reyns, G. E., Janssens, K. A., Buyse, J., Kühn, E. R. & Darras, V. M. Changes in thyroid hormone levels in chicken liver during fasting and refeeding. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 132(1), 239–245. https://doi.org/10.1016/s1096-4959(01)00528-0.CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Harvey, S. & Klandorf, H. Reduced adrenocortical function and increased thyroid function in fasted and refed chickens. J. Endocrinol. 98, 129–135. https://doi.org/10.1677/joe.0.0980129 (1983).CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Rimbach, R., Pillay, N. & Schradin, C. Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases. J. Exp. Biol. 220, 837–843. https://doi.org/10.1242/jeb.151449 (2017).Article 
    PubMed 

    Google Scholar 
    50.Scott, I. & Evans, P. R. The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: Implications for BMR/body mass relationships. Comp. Biochem. Physiol. Comp. Physiol. 103(2), 329–332. https://doi.org/10.1016/0300-9629(92)90589-I (1992).CAS 
    Article 
    PubMed 

    Google Scholar 
    51.Mesnage, R., Biserni, M., Genkova, D., Wesolowski, L. & Antoniou, M. N. Evaluation of neonicotinoid insecticides for oestrogenic, thyroidogenic and adipogenic activity reveals imidacloprid causes lipid accumulation. J. Appl. Toxicol. 38, 1483–1491. https://doi.org/10.1002/jat.3651 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Lindström, J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14(9), 343–348. https://doi.org/10.1016/S0169-5347(99)01639-0 (1999).Article 
    PubMed 

    Google Scholar 
    53.Vézina, F., Love, O. P., Lessard, M. & Williams, T. D. Shifts in metabolic demands in growing altricial nestlings illustrate context-specific relationships between basal metabolic rate and body composition. Physiol. Biochem. Zool. 82, 248–257. https://doi.org/10.1086/597548 (2009).Article 
    PubMed 

    Google Scholar 
    54.Swanson, D. L., Mckechnie, A. E. & Vézina, F. How low can you go ? An adaptive energetic framew ork for interpreting basal metabolic rate variation in endotherms. J. Comp. Physiol. B 187, 1039–1056. https://doi.org/10.1007/s00360-017-1096-3 (2017).Article 
    PubMed 

    Google Scholar 
    55.Hao, C., Eng, M. L., Sun, F. & Morrissey, C. A. Part-per-trillion LC-MS/MS determination of neonicotinoids in small volumes of songbird plasma. Sci. Total Environ. 644, 1080–1087. https://doi.org/10.1016/j.scitotenv.2018.06.317 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    56.Taliansky-Chamudis, A., Gómez-Ramírez, P., León-Ortega, M. & García-Fernández, A. J. Validation of a QuECheRS method for analysis of neonicotinoids in small volumes of blood and assessment of exposure in Eurasian eagle owl (Bubo bubo) nestlings. Sci. Total Environ. 595, 93–100. https://doi.org/10.1016/j.scitotenv.2017.03.246 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    57.Lemon, W. C. The energetics of lifetime reproductive success in the zebra finch Taeniopygia guttata. Physiol. Zool. 66, 946–963. https://doi.org/10.1086/physzool.66.6.30163748 (1993).Article 

    Google Scholar 
    58.Chastel, O., Lacroix, A. & Kersten, M. Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows (Passer domesticus). J. Avian Biol. 34, 298–306. https://doi.org/10.1034/j.1600-048X.2003.02528.x (2003).Article 

    Google Scholar 
    59.Hicks, O. et al. The role of parasitism in the energy management of a free-ranging bird. J. Exp. Biol. 221(24), jeb190066. https://doi.org/10.1242/jeb.190066 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Guglielmo, C. G., McGuire, L. P., Gerson, A. R. & Seewagen, C. L. Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J. Ornithol. 152, 75–85. https://doi.org/10.1007/s10336-011-0724-z (2011).Article 

    Google Scholar 
    61.Le Pogam, A. et al. Wintering snow buntings elevate cold hardiness to extreme levels but show no changes in maintenance costs. Physiol. Biochem. Zool. 93, 417–433. https://doi.org/10.1086/711370 (2020).Article 
    PubMed 

    Google Scholar 
    62.Lighton, J. R. B. Measuring Metabolic Rates, 2nd edn. https://doi.org/10.1093/oso/9780198830399.001.0001 (Oxford University Press, Oxford, 2018).Book 

    Google Scholar 
    63.Gessaman, J. A. & Nagy, K. A. Energy metabolism: Errors in gas-exchange conversion factors. Physiol. Zool. 61, 507–513. https://doi.org/10.1086/physzool.61.6.30156159 (1988).Article 

    Google Scholar 
    64.R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical  Computing, Vienna, Austria, 2017).65.Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x (2010).Article 

    Google Scholar  More