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    Contribution to the reproductive ecology of Notoscopelus resplendens (Richardson, 1845) (Myctophidae) in the Central-Eastern Atlantic

    1.
    Benoit-Bird, K. J. & Au, W. W. L. Energy: Converting from acoustic to biological resource units. J. Acoust. Soc. Am. 111, 2070 (2002).
    ADS  PubMed  Article  Google Scholar 
    2.
    Simard, Y. & Mackas, D. L. Mesoscale aggregations of euphausiid sound scattering layers on the continental shelf of Vancouver Island. Can. J. Fish. Aquat. Sci. 46, 1238–1249 (1989).
    Article  Google Scholar 

    3.
    Ariza, A., Garijo, J. C., Landeira, J. M., Bordes, F. & Hernández-León, S. Migrant biomass and respiratory carbon flux by zooplankton and micronekton in the subtropical northeast Atlantic Ocean (Canary Islands). Prog. Oceanogr. https://doi.org/10.1016/j.pocean.2015.03.003 (2015).
    Article  Google Scholar 

    4.
    Ariza, A. et al. Vertical distribution, composition and migratory patterns of acoustic scattering layers in the Canary Islands. J. Mar. Syst. https://doi.org/10.1016/j.jmarsys.2016.01.004 (2016).
    Article  Google Scholar 

    5.
    Hays, G. C. A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503, 163–170 (2003).
    Article  Google Scholar 

    6.
    Yatsu, A., Sassa, C., Moku, M. & Kinoshita, T. Night-time vertical distribution and abundance of small epipelagic and mesopelagic fishes in the upper 100 m layer of the Kuroshio–Oyashio Transition Zone in Spring. Fish. Sci. 71, 1280–1286 (2005).
    CAS  Article  Google Scholar 

    7.
    Olson, R. J. et al. Bioenergetics, Trophic Ecology, and Niche Separation of Tunas. (Advances in Marine Biology, 2016).

    8.
    Hudson, J. M., Steinberg, D. K., Sutton, T. T., Graves, J. E. & Latour, R. J. Myctophid feeding ecology and carbon transport along the northern Mid-Atlantic Ridge. Deep Res. Part I Oceanogr. Res. Pap. https://doi.org/10.1016/j.dsr.2014.07.002 (2014).
    Article  Google Scholar 

    9.
    Guidi, L. et al. A new look at ocean carbon remineralization for estimating deepwater sequestration. Global Biogeochem. Cy. 29, 1044–1059 (2015).
    ADS  CAS  Article  Google Scholar 

    10.
    van Noord, J. E. Diet of five species of the family Myctophidae caught off the Mariana Islands. Ichthyol. Res. 60, 89–92 (2013).
    Article  Google Scholar 

    11.
    Lam, V. & Pauly, D. Mapping the global biomass of mesopelagic fishes. Sea Around Us Proj. Newsl. 30, 4 (2005).
    Google Scholar 

    12.
    Irigoien, X. et al. Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nat. Commun. 5, 3271 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    13.
    Hulley, P. A. Results of the research cruises of FRV” Walther Herwig” to South America. LVIII. Family Myctophidae (Osteichthyes, Myctophiformes). Arch. für Fischereiwiss. 31, 1–300 (1981).
    Google Scholar 

    14.
    Hulley, P. A. Myctophidae. In Check-List of the FISHES of the Eastern Tropical Atlantic (CLOFETA) (eds Quero, J. C., Hureau, J. C., Karrer, C., Post, A. & Saldanha, L.) 398–467 (1990).

    15.
    Lubimova, T. G., Shust, K. V. & Popkov, V. V. Specific features in the ecology of Southern Ocean mesopelagic fish of the family Myctophidae. In Biological Resources of the Arctic and Antarctic (Collected Papers) 337 (1987).

    16.
    Catul, V., Gauns, M. & Karuppasamy, P. K. A review on mesopelagic fishes belonging to family Myctophidae. Rev. Fish Biol. Fish. 21, 339–354 (2011).
    Article  Google Scholar 

    17.
    Cherel, Y., Fontaine, C., Richard, P. & Labat, J. P. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol. Oceanogr. 55, 324–332 (2010).
    ADS  CAS  Article  Google Scholar 

    18.
    Pérez-Rodríguez, A. An Integrative Study to the Functioning of the Flemish Cap Demersal Community (University of Vigo, Vigo, 2012).
    Google Scholar 

    19.
    Battaglia, P. et al. Feeding habits of the Atlantic bluefin tuna, Thunnus thynnus (L. 1758), in the central Mediterranean Sea (Strait of Messina). Helgol. Mar. Res. 67, 97–107 (2013).
    ADS  Article  Google Scholar 

    20.
    Rosas-Luis, R., Villanueva, R. & Sánchez, P. Trophic habits of the Ommastrephid squid Illex coindetii and Todarodes sagittatus in the northwestern Mediterranean Sea. Fish. Res. 152, 21–28 (2014).
    Article  Google Scholar 

    21.
    Hedd, A., Montevecchi, W. A., Davoren, G. K. & Fifield, D. A. Diets and distributions of Leach’s storm-petrel (Oceanodroma leucorhoa) before and after an ecosystem shift in the Northwest Atlantic. Can. J. Zool. 87, 787–801 (2009).
    CAS  Article  Google Scholar 

    22.
    Ohizumi, H., Kuramochi, T., Kubodera, T., Yoshioka, M. & Miyazaki, N. Feeding habits of Dall’s porpoises (Phocoenoides dalli) in the subarctic North Pacific and the Bering Sea basin and the impact of predation on mesopelagic micronekton. Deep Sea Res. Part I Oceanogr. Res. Pap. 50, 593–610 (2003).
    ADS  Article  Google Scholar 

    23.
    Lisovenko, L. A. & Prut’ko, V. G. Reproductive biology of Diaphus suborbitalis (Myctophidae) in the equatorial part of the Indian Ocean. 2. Fecundity and reproductive potential. J. Ichthyol. 27, 1–12 (1987).
    Google Scholar 

    24.
    Shotton, R. Lanternfishes: A potential fishery in the Northern Arabian Sea. Review of the state of world fishery resources: Marine fisheries. FAO Fisheries Circular, (920). (1997).

    25
    Olivar, M. P. et al. Vertical distribution, diversity and assemblages of mesopelagic fishes in the western Mediterranean. Deep Res. Part I Oceanogr. Res. Pap. 62, 53–69 (2012).
    ADS  Article  Google Scholar 

    26.
    Battaglia, P. et al. Diet of the spothead lanternfish Diaphus metopoclampus (Cocco, 1829) (Pisces: Myctophidae) in the central Mediterranean Sea. Ital. J. Zool. 81, 530–543 (2014).
    CAS  Article  Google Scholar 

    27.
    Lisovenko, L. A. & Prutko, V. G. Reproductive biology of Diaphus suborbitalis (Myctophidae) in the equatorial part of the Indian Ocean. 1. Nature of oogenesis and type of spawning. J. Ichthyol. 26, 619–629 (1986).
    Google Scholar 

    28.
    Dalpadado, P. Reproductive biology of the lanternfish Benthosema pterotum from the Indian Ocean. Mar. Biol. 98, 307–316 (1988).
    Article  Google Scholar 

    29.
    Hussain, S. M. The reproductive biology of the lantern fish Benthosema fibulatum from the northern Arabian Sea. Fish. Res. 13, 381–393 (1992).
    Article  Google Scholar 

    30.
    Gartner, J. V. Patterns of reproduction in the dominant lanternfish species (Pisces: Myctophidae) of the eastern Gulf of Mexico, with a review of reproduction among tropical-subtropical Myctophidae. Bull. Mar. Sci. 52, 721–750 (1993).
    Google Scholar 

    31.
    Gjosaeter, J. Life history and ecology of the myctophid fish Notoscopelus elongatus Kroeyeri from the northeast Atlantic. Ser. Havundersokelser Fisk. Skr. 17, 133–142 (1981).
    Google Scholar 

    32.
    Kawaguchi, K., Mauchline, J. & Mauchline, J. Biology of myctophid fishes (Family Myctophidae) in the rockall trough, Northeastern Atlantic Ocean Biology of Myctophid Fishes (Family Myctophidae) in the Rockall Trough, Northeastern Atlantic Ocean. Biol. Oceanogr. 1, 337–373 (1982).
    Google Scholar 

    33
    Hussain, S. M. & Ali-Khan, J. Fecundity of Benthosema fibulatum and Benhosema pterotum from the northern Arabian sea. Deep Sea Res. Part A Oceanogr. Res. Pap. 34, 1293–1299 (1987).
    ADS  Article  Google Scholar 

    34.
    Young, J. W., Blaber, S. J. M. & Rose, R. Reproductive biology of three species of midwater fishes associated with the continental slope of eastern Tasmania, Australia. Mar. Biol. 95, 323–332 (1987).
    Article  Google Scholar 

    35.
    Prosch, R. M. Reproductive biology and spawning of the myctophid Lampanyctodes hectoris and the sternoptychid Maurolicus muelleri in the Southern Benguela ecosystem. S. Afr. J. Mar. Sci. 10, 241–252 (1991).
    Article  Google Scholar 

    36.
    Clarke, T. A. Fecundity and other aspects of reproductive effort in mesopelagic fishes from the North Central and Equatorial Pacific. Biol. Oceanogr. 3, 147–165 (1984).
    Google Scholar 

    37.
    Flynn, A. J. & Paxton, J. R. Spawning aggregation of the lanternfish Diaphus danae (family Myctophidae) in the north-western Coral Sea and associations with tuna aggregations. Mar. Freshw. Res. 63, 1255–1271 (2012).
    Article  Google Scholar 

    38.
    García-Seoane, E., Bernal, A. & Saborido-Rey, F. Reproductive ecology of the glacier lanternfish Benthosema glaciale. Hydrobiologia 727, 137–149 (2014).
    Article  Google Scholar 

    39.
    Sassa, C., Ohshimo, S., Tanaka, H. & Tsukamoto, Y. Reproductive biology of Benthosema pterotum (Teleostei: Myctophidae) in the shelf region of the East China Sea. J. Mar. Biol. Assoc. UK 94, 423–433 (2014).
    Article  Google Scholar 

    40.
    Sassa, C., Tanaka, H. & Ohshimo, S. Comparative reproductive biology of three dominant myctophids of the genus Diaphus on the slope region of the East China Sea. Deep. Res. Part I Oceanogr. Res. Pap. 115, 145–158 (2016).
    ADS  Article  Google Scholar 

    41.
    Eschmeyer, W. N., Fricke, R. & R, van der L. Catalog of Fishes, electronic version (3 January 2017). San Francisco, CA (California Academy of Sciences). (2018).

    42
    Collins, M. A. et al. Latitudinal and bathymetric patterns in the distribution and abundance of mesopelagic fish in the Scotia Sea. Deep. Res. Part II Top. Stud. Oceanogr. 59–60, 189–198 (2012).
    ADS  Article  Google Scholar 

    43.
    Albikovskaya, L. K. Some aspects of the biology and distribution of glacier lanternfish (Benthosema glaciale) over the slopes of Flemish Cap and eastern Grand Bank. NAFO Sci. Counc. Stud. 12, 37–42 (1988).
    Google Scholar 

    44.
    Nafpaktitis, B. G. Review of the lanternfish genus Notoscopelus (family myctophidae) in the north Atlantic and the Mediterranean. Bulletin of Marine Science vol. 25 (1975).

    45.
    Hulley, P. A. & Paxton, J. R. Myctophiformes—Myctophidae/Neoscopelidae. In FAO Species Identification Guide for Fisheries Purposes: The Living Marine Resources of the Eastern Central Atlantic (eds Carpenter, K.E. & De Angelis, N.) 1922–1923, Rome (2016).

    46.
    Sarmiento-Lezcano, A. N., Triay-Portella, R., Castro, J. J., Rubio-Rodríguez, U. & Pajuelo, J. G. Age-based life-history parameters of the mesopelagic fish Notoscopelus resplendens (Richardson, 1845) in the Central Eastern Atlantic. Fish. Res. https://doi.org/10.1016/j.fishres.2018.03.016 (2018).
    Article  Google Scholar 

    47.
    Sutton, T. T. et al. A global biogeographic classification of the mesopelagic zone. Deep Sea Res. Part I Oceanogr. Res. Pap. https://doi.org/10.1016/j.dsr.2017.05.006 (2017).
    Article  Google Scholar 

    48.
    Moser, H. G. & Ahlstrom, E. H. Myctophidae: lanternfishes. In The Early Stages of Fishes in the California Current Region. Cal. Coop. Ocean. Fish. (CalCOFI). (ed. Moser, H. G.) 387–475 (1996).

    49.
    Bordes, F. et al. Catálogo de especies meso y batipelágicas. Peces, moluscos y crustáceos. Colectadas con arrastre en las Islas Canarias, durante las campañas realizadas a bordo de B/E ‘La Bocaina’. Instituto Canarios de Ciencias Marinas (ICCM), Agencia Canaria de Investig. in 326 (2009).

    50.
    Bordes Caballero, F. et al. Epi- and mesopelagic fishes, acoustic data, and SST images collected off Lanzarote, Fuerteventura and Gran Canaria, Canary Islands, during cruise ‘La Bocaina 04–97’. In Informes Técnicos del Instituto Canario de Ciencias Marinas. 1–45 (1999).

    51.
    Wienerroither, R. M. Species composition of mesopelagic fishes in the area of the Canary Islands, Eastern Central Atlantic. Informes Técnicos del Instituto Canario de Ciencias Marinas. (2003).

    52.
    Fulton, T. W. The Sovereignty of the Sea: An Historical Account of the Claims of England to the Dominion of the British Seas and of the Evolution of the Territorial Waters, with Special Reference to the Rights of Fishing and the Naval Salute (W. Blackwood, Edinburgh, 1911).
    Google Scholar 

    53.
    Brown-Peterson, N. J., Wyanski, D. M., Saborido-Rey, F., Macewicz, B. J. & Lowerre-Barbieri, S. K. A standardized terminology for describing reproductive development in fishes. Mar. Coast. Fish. 3, 52–70 (2011).
    Article  Google Scholar 

    54.
    Brown-Peterson, N. J., Overstreet, R. M., Lotz, J. M., Franks, J. S. & Burns, K. M. Reproductive biology of cobia, Rachycentron canadum, from coastal waters of the southern United States. Fish. Bull. 99, 15–28 (2001).
    Google Scholar 

    55.
    Luna, L. G. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology 3rd edn. (McGraw-Hill Book Company, New York, 1968).
    Google Scholar 

    56.
    De Vlaming, V. Oocyte Developmental Pattern and Hormonal Involvement Among Teleosts. (1983).

    57.
    Murua, H. et al. Procedures to estimate fecundity of wild collected marine fish in relation to fish reproductive strategy. J. Northwest Atl. Fish. Sci. 33, 33–54 (2003).
    Article  Google Scholar 

    58.
    Kiesbu, O. S. Oogenesis in cod, Gadus morhua L., studied by light and electron microscopy. J. Fish Biol. 34, 735–745 (1989).
    Article  Google Scholar 

    59.
    Hunter, J. R., Lo, N. C. H. & Leong, J. H. Batch Fecundity in multiple spawning fishes. NOAA Tech. Rep. NMFS 36, 67–77 (1985).
    Google Scholar 

    60.
    R Core Team. R: A Language and Environment for Statistical Computing. (2018).

    61.
    Sassa, C. & Hirota, Y. Seasonal occurrence of mesopelagic fish larvae on the onshore side of the Kuroshio off southern Japan. Deep. Res. Part I 81, 49–61 (2013).
    Article  Google Scholar 

    62.
    QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation. (2020). https://www.qgis.org/es/site/.

    63.
    Wienerroither, R., Uibleina, F., Bordes, F. & Moreno, T. Composition, distribution, and diversity of pelagic fishes around the Canary Islands, Eastern Central Atlantic. Mar. Biol. Res. 5, 328–344 (2009).
    Article  Google Scholar 

    64.
    Olivar, M. P. et al. Variation in the diel vertical distributions of larvae and transforming stages of oceanic fishes across the tropical and equatorial Atlantic. Prog. Oceanogr. 160, 83–100 (2018).
    ADS  Article  Google Scholar 

    65.
    Clarke, T. A. Sex ratios and sexual differences in size among mesopelagic fishes from the central Pacific Ocean. Mar. Biol. 73, 203–209 (1983).
    Article  Google Scholar 

    66.
    Herring, P. J. The Biology of the Deep Ocean (Oxford University Press, Oxford, 2002).
    Google Scholar 

    67.
    Dalpadado, P. Aspects of the Biology of Benthosema pterotum (Myctophidae) from the Indian Ocean (University of Bergen, Bergen, 1983).
    Google Scholar 

    68.
    Filin, A. A. Growth, size and age composition of the Notoscopelus kroeyerii (Myctophidae). J. Ichthyol. 37, 27–32 (1997).
    Google Scholar 

    69.
    Greely, T. M., Gartner, J. V. J. & Torres, J. J. Age and growth of Electrona antarctica (Pisces: Myctophidae), the dominant mesopelagic fish in the Southern Ocean. Mar. Biol. 133, 145–158 (1999).
    Article  Google Scholar 

    70.
    Hulley, P. A. Myctophidae. In Fishes of the North-eastern Atlantic and the Mediterranean (eds Whitehead, P.J.P. et al.) 429–483 (1986).

    71.
    Kawaguchi, K. & Shimizu, H. Taxonomy and distribution of the lanternfishes, genus Diaphus (Pisces, Myctophidae) in the western Pacific, eastern Indian Oceans and the southeast Asian Seas. Bull. Ocean Res. Inst. Univ. Tokyo 10, 1–145 (1978).
    Google Scholar 

    72.
    Herring, P. J. Sex with the lights on? A review of bioluminescent sexual dimorphism in the sea. J. Mar. Biol. Assoc. UK 87, 829–842 (2007).
    CAS  Article  Google Scholar 

    73.
    Barnes, A. T. & Case, J. F. The luminescence of lanternfish (Myctophidae): Spontaneous activity and responses to mechanical, electrical, and chemical stimulation. J. Exp. Mar. Biol. Ecol. 15, 203–221 (1974).
    Article  Google Scholar 

    74.
    Clarke, T. A. Some aspects of the ecology of lanternfishes (Myctophidae) in the Pacific Ocean near Hawaii. Fish. Bull. 71, 401–434 (1973).
    Google Scholar 

    75.
    Karnella, C. The Ecology of Lanterfishes (Myctophidae) in the Bermuda ‘Ocean Acre’ (George Washington University, Washington, 1983).
    Google Scholar 

    76.
    Sabatés, A. & Masò, M. Effect of a shelf slope front on the spatial distribution of mesopelagic fish larvae in the western Mediterranean. Deep. Res. I(37), 1085–1098 (1990).
    ADS  Article  Google Scholar 

    77.
    Alekseyeva, Y. I. & Alekseyev, F. Y. Some aspects of reproductive biology of the lanternfishes, Myctophum punctatum and Notoscopelus resplendens (Myctophidae), from the eastern tropical Atlantic. J. Ichthyol. 23, 56–63 (1983).
    Google Scholar 

    78.
    Davison, P. C., Checkley, D. M., Koslow, J. A. & Barlow, J. Carbon export mediated by mesopelagic fishes in the northeast Pacific Ocean. Prog. Oceanogr. https://doi.org/10.1016/j.pocean.2013.05.013 (2013).
    Article  Google Scholar  More

  • in

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    Occurrence, distribution, and health risk assessment of quinolone antibiotics in water, sediment, and fish species of Qingshitan reservoir, South China

    1.
    Yu, Z. Y. Analysis of current situation of antibiotic abuse and countermeasures. Econ. Res. Guide. 145(35), 314–315 (2011) (in Chinese).
    ADS  Google Scholar 
    2.
    Adachi, F. et al. Occurrence of fluoroquinolones and fluoroquinolone-resistance genes in the aquatic environment. Sci. Total Environ. 444(444C), 508–514 (2013).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    3.
    Wu, T. T. et al. Investigation of the typical antibiotics in the sediments of the Yongjiang River, Nanning City, South China. China Environ. Sci. 33(2), 336–344 (2013) (in Chinese).
    CAS  Google Scholar 

    4.
    Ruan, Y. F. et al. Distribution characteristics of typical antibiotics in surface water and sediments from freshwater aquaculture water in Tianjin suburban areas, China. J. Agro-Environ. Sci. 30(12), 2586–2593 (2011) (in Chinese).
    CAS  Google Scholar 

    5.
    Liang, X. et al. The distribution and partitioning of common antibiotics in water and sediment of the Pearl River Estuary, South China. Chemosphere 92(11), 1410–1416 (2013).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Shi, H. The Analysis Method of Twenty Antibiotics in the Sediment and its Application (East China Normal University, Shanghai, 2014) (in Chinese).
    Google Scholar 

    7.
    Zhang, W. R. The Distribution of Typical Antibiotics Strains in the Sediment Environments of Dalian (Dalian University, Dalian, 2014) (in Chinese).
    Google Scholar 

    8.
    Xu C. Contamination of Antibiotics and antibiotics resistance genes in water, soil and sediment of the Three Gorges Reservoir. 2017. Wuhan: the Wuhan Botanical Garden of the Chinese Academy of Sciences (in Chinese).

    9.
    Yang, Y. T. et al. Preliminary investigation of three quinolones in the muscle tissues of four fishes collected from the markets in Guangzhou City. J. Environ. Health 26(2), 109–111 (2009).
    CAS  Google Scholar 

    10.
    Wang, H. et al. Antibiotic residues in meat, milk and aquatic products in Shanghai and human exposure assessment. Food Control 80, 217–225 (2017).
    CAS  Article  Google Scholar 

    11.
    Naik, O. A. et al. Characterization of multiple antibiotic resistance of culturable microorganisms and metagenomic analysis of total microbial diversity of marine fish sold in retail shops in Mumbai, India. Environ. Sci. Pollut. Res. Int. 25(7), 6228–6239 (2017).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    12.
    Uchida, K. et al. Monitoring of antibiotic residues in aquatic products in urban and rural areas of Vietnam. J. Agric. Food Chem. 64(31), 6133–6138 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    13.
    Bakeraustin, C. et al. Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia and South Carolina, USA. J. Food Prot. 71(12), 2552–2558 (2008).
    CAS  Article  Google Scholar 

    14.
    Richardson, B. J., Lam, P. K. S. & Martin, M. Emerging chemicals of concern: Pharmaceuticals and personal care products (PPCPs) in Asia, with particular reference to Southern China. Mar. Pollut. Bull. 50(9), 913–920 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    Liu, X. Pollution Level, Source and Ecological Risk of Typical Antibiotics in the Dongting Lake, China (Shandong Normal University, Jinan, 2017) (in Chinese).
    Google Scholar 

    16.
    Turiel, E., Bordin, G. & Rodrı́guez, A. R. Trace enrichment of (fluoro)quinolone antibiotics in surface waters by solid-phase extraction and their determination by liquid chromatography-ultraviolet detection. J. Chromatogr. A 1008(2), 145–155 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    17.
    Ying G G. Antibiotic use and pollution in the river basins of China. The 30th Academic Annual Meeting of China Chemical Society. 2016 (in Chinese).

    18.
    Sun, K. Contamination Characteristics and Ecological Risk Assessment of Typical Antibiotics in the Water of the Hongze Lake (Nanjing Agricultural University, Nanjing, 2015) (in Chinese).
    Google Scholar 

    19.
    Wang J W. Distribution characteristics and ecological risk assessment of antibiotics in surface water of Xi’an section of Weihe river. 2018. Xi’an: Xi’an University of Technology (in Chinese).

    20.
    Chen, L. et al. Investigation and evaluation of water quality of Qingshtan reservoir in Guilin city. Guangdong Agric. Sci. 40(5), 160–164 (2013) (in Chinese).
    CAS  Google Scholar 

    21.
    Zheng, Y. L. et al. Change of Inflow Runoff into the Qingshitan Reservoir in Guilin City. Water Conserv. Sci. Technol. Econ. 18(8), 46–48 (2012) (in Chinese).
    Google Scholar 

    22.
    Liang, Y. et al. Characteristics and risk assessment of organochlorine pesticide residues in surface sediments collected at the Qingshitan Reservoir. Toxicol. Environ. Chem. Rev. 98(5–6), 658–668 (2016).
    CAS  Article  Google Scholar 

    23.
    Cheng, Y. P. et al. Pollution characteristics and potential ecological risk assessment of heavy metals in sediments of Qingshitan reservoir. Yangtze River 48(10), 24–29 (2017) (in Chinese).
    Google Scholar 

    24.
    Kall, J. Limnology: Inland Water Ecosystem (Higher Education Press, Beijing, 2011).
    Google Scholar 

    25.
    Miu, Z. L., Zong, F. S. & Jiang, Y. P. Study on Hydrographic Karst and Tourism Resources in Guilin (China University of Geosciences Press, Wuhan, 2004) (in Chinese).
    Google Scholar 

    26.
    Qi, S. S. & Yang, X. Study on ecological restoration mode of reservoir eutrophication by fish cage culture. Environ. Sci. Manag. 37(11), 151–154 (2012) (in Chinese).
    CAS  Google Scholar 

    27.
    Xu, W. H. et al. Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using highperformance liquid chromatography-electrospray ionization tandem mass spectrometry. Environ. Pollut. 145, 672–679 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    28.
    Liang, X. M. et al. Occurrence of antibiotics in typical aquaculture of the Pearl River Estuary. Ecol. Environ. Sci. 22(2), 304–310 (2013) (in Chinese).
    Google Scholar 

    29.
    Zhou, L. J. et al. Trends in the occurrence of human and veterinary antibiotics in the sediments of the Yellow River, Hai River and Liao River in northern China. Environ. Pollut. 159(7), 1877–1885 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    30.
    He, X. T. et al. Residues and health risk assessment of sulfonamides in sediment and fish from typical marine aquaculture regions of Guangdong province, China. Environ. Sci. 35(7), 2728–2735 (2014) (in Chinese).
    Google Scholar 

    31.
    Lu, R. K. Soil Argrochemistry Analysis Protocoes (Agriculture Science Press, Beijing, 1999) (in Chinese).
    Google Scholar 

    32.
    Xu, J. Application of High Performance Liquid Chromatography in Analysis of Antibiotics in Seafood (Harbin, Harbin Institute of Technology, 2016) (in Chinese).
    Google Scholar 

    33.
    European Commission. Technical Guidance Document on Risk Assessment in support of Commission Directive 93/67/EEC on risk assessment for new notified substances. 2003.

    34.
    Vryzas, Z. et al. Determination and aquatic risk assessment of pesticide residues in riparian drainage canals in northeastern Greece. Ecotoxicol. Environ. Saf. 74(2), 174–181 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Backhaus, T., Scholze, M. & Grimme, L. H. The single substance and mixture toxicity of quinolones to the bioluminescent bacterium Vibrio fischeri. Aquat. Toxicol. 49(1), 49–61 (2000).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    36.
    Ma, Y. et al. Occurrences and regional distributions of 20 antibiotics in water bodies during groundwater recharge. Sci. Total Environ. 518–519, 498–506 (2015).
    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

    37.
    Zhang, P. W. et al. Spatial, temporal distribution characteristics and potential risk of PPCPs in surface sediments from Taihu Lake. Environ. Sci. 37(9), 3348–3355 (2016) (in Chinese).
    Google Scholar 

    38.
    Piao, H. S. et al. Estimation of sorption coefficients of organic compounds with KOW. Environ. Sci. Technol. 4, 8–13 (1999) (in Chinese).
    Google Scholar 

    39.
    Guérit, I. et al. Environmental risk assessment: a critical approach of the European TGD in an insitu application. Ecotoxicol. Environ. Saf. 71(1), 291–300 (2008).
    PubMed  Article  CAS  Google Scholar 

    40.
    Ren, K. J. et al. Residues characteristics of fluoroquinolones (FQs) in the river sediments and fish tissues in a drinking water protection area of Guangdong Province. Acta Sci. Circum. 36(3), 760–766 (2016) (in Chinese).
    CAS  Google Scholar 

    41.
    Wang, L. et al. Incorporating fish habitat requirements of the complete life cycle into ecological flow regime estimation of rivers. Ecohydrology 13(4), e2204 (2020).
    Article  Google Scholar 

    42.
    Brown, K. D. et al. Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico. Sci. Total Environ. 366(2), 772–783 (2006).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    43.
    Chang, X. et al. Determination of antibiotics in sewage from hospitals, nursery and slaughter house, wastewater treatment plant and source water in Chongqing region of Three Gorge Reservoir in China. Environ. Pollut. 158(5), 1444–1450 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    44.
    Hirsch, R. et al. Occurrence of antibiotics in the aquatic environment. Sci. Total Environ. 225(1/2), 109–111 (1999).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    45.
    Guo, X. et al. Research progress on environmental exposure levels and environmental fate of veterinary antibiotics. Environ. Sci. Technol. 37(09), 76–86 (2014) (in Chinese).
    Google Scholar 

    46.
    Jiang, L. et al. Occurrence, distribution and seasonal variation of antibiotics in the Huangpu River, Shanghai. China. Chemosphere 82(6), 822–828 (2011).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    47.
    Li, J. et al. Distribution characteristics and ecological risk assessment of antibiotic pollution in Xiaoqing River watershed. J. Agro-Environ. Sci. 35(7), 1384–1391 (2016) (in Chinese).
    Google Scholar 

    48.
    Wu, X. et al. Occurrence, distribution and ecological risk of aantibiotics in surface water of the Gonghu Bay, Taihu Lake. Environ. Sci. 37(12), 4596–4604 (2016) (in Chinese).
    Google Scholar 

    49.
    Zhu, T. et al. Research on pollution and health risk by antibiotics in source water of Shiyan Reservoir in Shenzhen. J. Environ. Health 30(11), 1003–1006 (2013) (in Chinese).
    Google Scholar 

    50.
    Gao, L. et al. Research on pollution characteristics of antibiotics in Qinghe River in Beijing. Ecol. Sci. 33(1), 83–92 (2014) (in Chinese).
    Google Scholar 

    51.
    Nowara, A., Burhenne, J. & Spiteller, M. Binding of fluoroquinolone carboxylic acid derivatives to clay minerals. J. Agric. Food Chem. 45(4), 1459–1463 (1997).
    CAS  Article  Google Scholar 

    52.
    Li, B. Y. Study on Adsorption and Biodegradation of Norfloxacin in Soil (Zhengzhou University, Zhengzhou, 2010) (in Chinese).
    Google Scholar 

    53.
    Liu C, Li Y. Research Progress of Adsorption and Degradation of Ciprofloxacin in Soil. Beijing Agriculture. 2016, (4) (in Chinese).

    54.
    Wang, L. P., Zhang, M. K. & Zheng, S. A. Adsorption–desorption characteristics and biological effects of enrofloxacin in agricultural soils. Chin. J. Soil Sci. 39(2), 393–397 (2008) (in Chinese).
    CAS  Google Scholar 

    55.
    Jing, L. D. et al. Study on degradation kinetics of Ofloxacin at sediment–water interface. J. Southwest Univ. Nation. (Natural Science Edition). 42(4), 409–413 (2016) (in Chinese).
    CAS  Google Scholar 

    56.
    Dai, J. F. et al. Water quality analysis and segmentation of the pollution loads in different spatial scales of the upstream of Lijiang River. China Rural Water Hydropower 4, 67–71 (2017) (in Chinese).
    Google Scholar 

    57.
    Huang, J. et al. Residual levels of fluoroquinolones in freshwater fish from aquatic products markets in Guiyang. J. Environ. Health 34(2), 139–141 (2017) (in Chinese).
    Google Scholar 

    58.
    Sun, Y. C. Analysis and Distribution Characteristics of FQs in Environmental Water and Aquatic Product and its Effect on Environmental Stress (Harbin, Harbin Institute of Technology, 2014) (in Chinese).
    Google Scholar 

    59.
    Zhang, L. Y. Optimization of Quinolone Antibiotics Detection Method and in Water Photolysis and Hydrolysis Characteristics Research (Jilin Agricultural University, Jilin, 2016) (in Chinese).
    Google Scholar 

    60.
    Carrasquillo, A. J. et al. Sorption of ciprofloxacin and oxytetracycline zwitterions to soils and soil minerals: influence of compound structure. Environ. Sci. Technol. 42(20), 7634–7642 (2008).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    61.
    Zou, S. et al. Occurrence and distribution of antibiotics in coastal water of the Bohai Bay, China: impacts of river discharge and aquaculture activities. Environ. Pollut. 159(10), 2913–2920 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    62.
    Fu, H. et al. Impacts of p H on adsorption of quinolones by PAC. China Water Wastewater 33(17), 64–67 (2017) (in Chinese).
    Google Scholar 

    63.
    Huang, S. et al. Study on the relationships among pH, dissolved oxygen and chlorophyll a I: aquaculture water. Chin. J. Environ. Eng. 5(6), 1201–1208 (2011) (in Chinese).
    CAS  Google Scholar 

    64.
    Chen, S. et al. Formation, harmfulness, prevention, control and treatment of waters eutrophication. Environ. Sci. Technol. 22(2), 11–15 (1999) (in Chinese).
    Google Scholar 

    65.
    Pang, H. L. Studies on the Sorption Behavior of two Fluoroquinolones on Marine Sediments (Ocean University of China, Qingdao, 2012) (in Chinese).
    Google Scholar 

    66.
    Qin, Y. et al. Pollution characteristics and ecological risk assessment of typical antibiotics in the surface water of Hunhe River. Res. Environ. Sci. 28(3), 361–368 (2015) (in Chinese).
    CAS  Google Scholar 

    67.
    Syberg, K. et al. On the use of mixture toxicity assessment in REACH and the water framework directive: a review. Hum. Ecol. Risk Assess. 15(6), 1257–1272 (2009).
    CAS  Article  Google Scholar 

    68.
    Liu, K. et al. Investigation on the typical quinolone antibiotics in the surface sediments of Jiaozhou bay China. Mar. Environ. Sci. 36(05), 655–661 (2017) (in Chinese).
    Google Scholar 

    69.
    Zhang, J. et al. Health risk assessment of antibiotics in the centralized drinking water source in the three gorges reservoir area. Environ. Sci. Technol. 41(8), 192–198 (2018) (in Chinese).
    Google Scholar 

    70.
    No. 235 Announcement of the Ministry of Agriculture. Maximum residue limits of veterinary drugs in animal foods. China Swine Industry 2010(8), 10–12 (2002) (in Chinese).
    Google Scholar 

    71.
    National Health and Family Planning Commission of PRC. Outline of China’s food and nutrition development (2014–2020). Chron. Pathematol. J. 36(2), 111–113 (2014) (in Chinese).
    Google Scholar 

    72.
    Zhang, Q. P., Li, J. & Wang, C. M. Residual level and safety assessment of quinolone antibiotics in aquatic products in Suzhou. Chin. J. Health Lab. Technol. 22(10), 2417–2418 (2012) (in Chinese).
    CAS  Google Scholar 

    73.
    Wu, X. L. Pollution Characteristics and Health Risk of Quinolones in Vegetables in the Pearl River Delta Region (Jinan University, Guangzhou, 2011) (in Chinese).
    Google Scholar 

    74.
    Li, W., Shi, Y., Gao, L., Liu, J. & Cai, Y. Occurrence of antibiotics in water, sediments, aquatic plants, and animals from Baiyangdian Lake in North China. Chemosphere 89(11), 1307–1315 (2012).

    75.
    Minh, T. B. et al. Antibiotics in the Hong Kong metropolitan area: Ubiquitous distribution and fate in Victoria Harbour. Mar. Pollut. Bull. 58(7), 1052–1062 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    76.
    Riva, F., Zuccato, E., Davoli, E., Fattore, E. & Castiglioni, S. Risk assessment of a mixture of emerging contaminants in surface water in a highly urbanized area in Italy. J. Hazard. Mater. 361, 103–110 (2019).

    77.
    Watkinson, A. J., Murby, E. J., Kolpin, D. W. & Costanzo, S. D. The occurrence of antibiotics in an urban watershed: From wastewater to drinking water. Sci. Total Environ. 407(8), 2711–2723 (2009).

    78.
    Batt, A. L., Bruce, I. B. & Aga, D. S. Evaluating the vulnerability of surface waters to antibiotic contamination from varying wastewater treatment plant discharges. Environ. Pollut. 142(2), 295–302 (2006).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    79.
    Golet, E. M., Strehler, A., Alder, A. C. & Giger, W. Determination of fluoroquinolone antibacterial agents in sewage sludge and sludge-treated soil using accelerated solvent extraction followed by solid-phase extraction. Anal. Chem. 74(21), 5455–5462 (2002).

    80.
    Gibs, J. et al. Occurrence and partitioning of antibiotic compounds found in the water column and bottom sediments from a stream receiving two wastewater treatment plant effluents in Northern New Jersey, 2008. Sci. Total Environ. 458–460, 107–116 (2013).
    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

    81.
    Wang, G. Q. & Sun, T. Antibiotic residues in aquatic products of Hongze lake investigation and research. Guangdong Chem. 38(1), 151–153 (2011) (in Chinese).
    CAS  Google Scholar 

    82.
    Yang, Y. T. & Luan, L. J. Residues and health risk assessment of Quinolones in fishes from the markets in Jining City. J. Anhui Agric. Sci. 43(26), 141–143 (2015) (in Chinese).
    CAS  Google Scholar  More

  • in

    Unchartered waters: the unintended impacts of residual chlorine on water quality and biofilms

    Chlorine residual impacted discolouration
    Unexpectedly, flushing of the High-chlorine system (by incrementally increasing the flow rate) produced a significantly greater discolouration response (assessed via turbidity) than the Medium- or Low-chlorine systems across all stages of flushing, of both tests (Fig. 2). Compared to the other regimes, the High-chlorine system also had a greater final concentration of iron (known to be associated with discolouration) at the end of Flush 1 and a greater rate of iron mobilisation during Flush 2 (Fig. 2). Conversely, the Low-chlorine regime consistently resulted in the lowest impact on water quality with the lowest discolouration and metal concentrations. Even after just 28 days of growth, material was mobilised from the High-chlorine regime at sufficient volumes to approach or breach the water quality standards for discolouration and iron concentrations (Fig. 2 and Supplementary Table 1). This contradicts the common perception of residual chlorine impacts on water quality and also studies of cast iron pipes, which suggest increasing oxidant concentration (disinfectant or dissolved oxygen) in drinking water decreases iron release26,27. Although surprising, High-chlorine repeatedly resulted in the greatest discolouration and Low-chlorine the least; as observed during the flushing of test 1, test 2 (Fig. 2) and preliminary tests (Supplementary Fig. 2).
    Fig. 2: Discolouration responses to elevated shear stress during the flushing of the chlorine regimes.

    Discolouration was determined primarily by a Turbidity (506 ≤ n ≤ 1091) with consideration of b Iron (n = 3) and c Manganese (n = 3) concentrations. Flush1 refers to the flushing phase of test 1, Flush2 indicates data from the flushing phase of test 2. Data normalised to well-mixed concentrations (0.09 Pa) of each system, mean ± standard deviation plotted. Linear regressions in each plot had R2 values of a 0.82 ≤ R2 ≤ 0.99, b 0.89 ≤ R2 ≤ 1.00 and c 0.76 ≤ R2 ≤ 0.98. High-chlorine: metal concentrations only available for final flushing step for Flush1. Chlorine regimes differed in their turbidity (ANCOVA on raw data: F ≥ 2869, p  More

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    Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

    LX3 enhances larval pathogen eradication by antibiotics
    Prophylactic administration of OTC to honey bees is a common practice in beekeeping for the prevention of AFB. To evaluate the efficacy of this long-standing apiculture management strategy, we monitored a 2-week treatment regimen with OTC under natural field conditions in honey bee hives experiencing low-grade chronic infection with P. larvae (Fig. 1a). Using a qPCR-based approach to enumerate pathogen load, P. larvae abundance was found to be significantly lower in honey bee larvae (primary target of AFB) at week 1 and week 2 of OTC treatment (Kruskal–Wallis with Dunn’s multiple comparisons, P = 0.0071 and P = 0.0005, respectively) compared to baseline levels at day 0 (Fig. 1b). In contrast, no observable differences in P. larvae abundance were found in adult honey bees (active vector of AFB) at any time point during this treatment (Kruskal–Wallis with Dunn’s multiple comparisons, P = 0.9999, P = 0.6367, respectively; Fig. 1c).
    Fig. 1: LX3 enhances larval pathogen eradication by antibiotics.

    Experimental hives were subjected to standard antibiotic treatment with oxytetracycline (OTC) for 2 weeks and then supplemented for 4 weeks with either pollen patties containing LX3 (LX3) or pollen patties containing vehicle (VEH). No treatment control (NTC) hives received no further treatment after OTC. a Schematic diagram outlining the experimental design. b, c Molecular-based quantification of P. larvae in honey bee larvae (whole body) and adults (dissected abdomen) collected just prior to the start of OTC exposure (A.0), and then after 1 (A.1) and 2 (A.2) weeks of exposure. Data are depicted as median ± 95% confidence intervals (Kruskal–Wallis with Dunn’s multiple comparisons) at different time points. Each data point represents either one individual (adults) or three pooled individuals (larvae) sampled equally from a total of n = 6 hives. d, e Molecular-based quantification of P. larvae in larvae (whole body) and adults (dissected whole abdomens) at the start of the supplementation period (S.0; corresponding to 3 days post A.2 time point), and then after 2 (S.2) and 4 (S.4) weeks. Data are depicted as mean ± standard deviation (two-way ANOVA with Sidak’s multiple comparisons) at different time points with each data point representing either one individual (adults) or three pooled individuals (larvae) sampled equally from n = 4 hives per treatment group. f, g Capped brood counts during OTC treatment (n = 6 hives) and subsequent supplementation period (n = 4 hives per treatment group). Data represents the median (line in box), IQR (box), and minimum/maximum (whiskers) of relative change in brood counts normalized by hive. Statistics shown for one-way and two-way ANOVA, respectively, with Sidak’s multiple comparisons for both. **P  More

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    Modelled sensitivity

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    Phytoplankton dynamics in a changing Arctic Ocean

    1.
    AMAP. Snow, Water, Ice and Permafrost in the Arctic (SWIPA) 2017 (AMAP, 2017).
    2.
    Notz, D. & Stroeve, J. Observed Arctic sea-ice loss directly follows anthropogenic CO2 emission. Science 354, 747–750 (2016).
    CAS  Article  Google Scholar 

    3.
    Haine, T. W. N. et al. Arctic freshwater export: status, mechanisms, and prospects. Glob. Planet. Change 125, 13–35 (2015).
    Article  Google Scholar 

    4.
    Aagaard, K. & Carmack, E. C. The role of sea ice and other fresh water in the Arctic circulation. J. Geophys. Res. 94, 14485–14498 (1989).
    Article  Google Scholar 

    5.
    Aagaard, K., Coachman, L. K. & Carmack, E. On the halocline of the Arctic Ocean. Deep Sea Res. Pt A 28, 529–545 (1981).
    Article  Google Scholar 

    6.
    Polyakov, I. V. et al. Greater role for Atlantic inflows on sea-ice loss in the Eurasian Basin of the Arctic Ocean. Science 356, 285–291 (2017).
    CAS  Article  Google Scholar 

    7.
    Aagaard, K. & Coachman, L. K. Toward an ice-free Arctic ocean. Eos Trans. Amer. Geophys. Union 56, 484–486 (1975).
    Article  Google Scholar 

    8.
    Kwok, R. Arctic sea ice thickness, volume, and multiyear ice coverage: losses and coupled variability (1958–2018). Environ. Res. Lett. 13, 105005 (2018).
    Article  Google Scholar 

    9.
    Post, E. et al. Ecological consequences of sea-ice decline. Science 341, 519–524 (2013).
    CAS  Article  Google Scholar 

    10.
    Post, E. et al. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358 (2009).
    CAS  Article  Google Scholar 

    11.
    Gregory, A. C. et al. Marine viral macro- and micro-diversity from pole to pole. Cell 177, 1109–1123 (2019).
    CAS  Article  Google Scholar 

    12.
    Arrigo, K. R., van Dijken, G. & Pabi, S. Impact of a shrinking Arctic ice cover on marine primary production. Geophys. Res. Lett. 35, L19603 (2008).
    Article  Google Scholar 

    13.
    Kahru, M., Lee, Z.-P., Mitchell, B. G. & Nevison, C. D. Effects of sea ice cover on satellite-detected primary production in the Arctic ocean. Biol. Lett. 12, 20160223 (2016).
    Article  Google Scholar 

    14.
    Bélanger, S., Babin, M. & Tremblay, J.-É. Increasing cloudiness in Arctic damps the increase in phytoplankton primary production due to sea ice receding. Biogeosciences 10, 4087–4101 (2013).
    Article  Google Scholar 

    15.
    Kahru, M., Brotas, V., Manzano-Sarabio, M. & Mitchell, B. G. Are phytoplankton blooms occurring earlier in the Arctic? Glob. Change Biol. 17, 1733–1739 (2010).
    Article  Google Scholar 

    16.
    Ardyna, M. et al. Recent Arctic Ocean sea-ice loss triggers novel fall phytoplankton blooms. Geophys. Res. Lett. 41, 6207–6212 (2014).
    Article  Google Scholar 

    17.
    Arrigo, K. R. & van Dijken, G. L. Continued increases in Arctic Ocean primary production. Prog. Oceanogr. 136, 60–70 (2015).
    Article  Google Scholar 

    18.
    Lewis, K. M., van Dijken, G. & Arrigo, K. R. Changes in phytoplankton concentration, not sea ice, now drive increased Arctic Ocean primary production. Science 369, 198–202 (2020).
    CAS  Article  Google Scholar 

    19.
    Olson, M. B. & Strom, S. L. Phytoplankton growth, microzooplankton herbivory and community structure in the southeast Bering Sea: insight into the formation and temporal persistence of an Emiliania huxleyi bloom. Deep Sea Res. Pt. 2 49, 5969–5990 (2002).
    CAS  Article  Google Scholar 

    20.
    Sherr, E. B., Sherr, B. F. & Ross, C. Microzooplankton grazing impact in the Bering Sea during spring sea ice conditions. Deep Sea Res. Pt. 2 94, 57–67 (2013).
    CAS  Article  Google Scholar 

    21.
    Forest, A. et al. Biogenic carbon flows through the planktonic food web of the Amundsen Gulf (Arctic Ocean): a synthesis of field measurements and inverse modeling analyses. Prog. Oceanogr. 91, 410–436 (2011).
    Article  Google Scholar 

    22.
    Franzè, G. & Lavrentyev, P. J. Microbial food web structure and dynamics across a natural temperature gradient in a productive polar shelf system. Mar. Ecol. Prog. Ser. 569, 89–102 (2017).
    Article  CAS  Google Scholar 

    23.
    Menden-Deuer, S., Lawrence, C. & Franzè, G. Herbivorous protist growth and grazing rates at in situ and artificially elevated temperatures during an Arctic phytoplankton spring bloom. PeerJ 6, e5264 (2018).
    Article  CAS  Google Scholar 

    24.
    Carmack, E. C. & Wassmann, P. Food webs and physical-biological coupling on pan-Arctic shelves: unifying concepts and comprehensive perspectives. Prog. Oceanogr. 71, 446–477 (2006).
    Article  Google Scholar 

    25.
    Harrison, W. G. & Cota, G. F. Primary production in polar waters: relation to nutrient availability. Polar Res. 10, 87–104 (1991).
    Article  Google Scholar 

    26.
    Sakshaug, E. in The Organic Carbon Cycle in the Arctic Ocean (eds Stein, R. & MacDonald, R. W.) 57–81 (Springer, 2004).

    27.
    Michel, C., Nielsen, T. G., Nozais, C. & Gosselin, M. Significance of sedimentation and grazing by ice micro- and meiofauna for carbon cycling in annual sea ice (northern Baffin Bay). Aquat. Microb. Ecol. 30, 57–68 (2002).
    Article  Google Scholar 

    28.
    Krause, J. W. et al. Biogenic silica production and diatom dynamics in the Svalbard region during spring. Biogeosciences 15, 6503–6517 (2018).
    CAS  Article  Google Scholar 

    29.
    Ardyna, M., Gosselin, M., Michel, C., Poulin, M. & Tremblay, J.-É. Environmental forcing of phytoplankton community structure and function in the Canadian High Arctic: contrasting oligotrophic and eutrophic regions. Mar. Ecol. Prog. Ser. 442, 37–57 (2011).
    CAS  Article  Google Scholar 

    30.
    Taylor, R. L. et al. Colimitation by light, nitrate, and iron in the Beaufort Sea in late summer. J. Geophys. Res. 118, 3260–3277 (2013).
    Article  Google Scholar 

    31.
    Tremblay, J.-É. et al. Global and regional drivers of nutrient supply, primary production and CO2 drawdown in the changing Arctic Ocean. Prog. Oceanogr. 139, 171–196 (2015).
    Article  Google Scholar 

    32.
    Tremblay, J.-É. & Gagnon, J. in Influence of Climate Change on the Changing Arctic and Sub-Arctic Conditions (eds J. C. J. Nihoul & A. G. Kostianoy) 73–93 (Springer, 2009).

    33.
    Michel, C. et al. Arctic Ocean outflow shelves in the changing Arctic: a review and perspectives. Prog. Oceanogr. 139, 66–88 (2015).
    Article  Google Scholar 

    34.
    Bourgault, D. et al. Turbulent nitrate fluxes in the Amundsen Gulf during ice-covered conditions. Geophys. Res. Lett. 38, L15602 (2011).
    Article  CAS  Google Scholar 

    35.
    Randelhoff, A., Fer, I., Sundfjord, A., Tremblay, J.-É. & Reigstad, M. Vertical fluxes of nitrate in the seasonal nitracline of the Atlantic sector of the Arctic Ocean. J. Geophys. Res. Oceans 121, 5282–5295 (2016).
    CAS  Article  Google Scholar 

    36.
    Toole, J. M. et al. Influences of the ocean surface mixed layer and thermohaline stratification on Arctic Sea ice in the central Canada Basin. J. Geophys. Res. Oceans 115, C10018 (2010).
    Article  Google Scholar 

    37.
    Lind, S., Ingvaldsen, R. B. & Furevik, T. Arctic warming hotspot in the northern Barents Sea linked to declining sea-ice import. Nat. Clim. Change 8, 634–639 (2018).
    Article  Google Scholar 

    38.
    Mioduszewski, J., Vavrus, S. & Wang, M. Diminishing Arctic sea ice promotes stronger surface winds. J. Climate 31, 8101–8119 (2018).
    Article  Google Scholar 

    39.
    Bendif, E. M. et al. Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa. Nat. Commun. 10, 4234 (2019).
    Article  CAS  Google Scholar 

    40.
    Oziel, L. et al. Faster Atlantic currents drive poleward expansion of temperate marine species in the Arctic Ocean. Nat. Commun. 11, 1705 (2020).
    CAS  Article  Google Scholar 

    41.
    Neukermans, G., Oziel, L. & Babin, M. Increased intrusion of warming Atlantic water leads to rapid expansion of temperate phytoplankton in the Arctic. Glob. Change Biol. 24, 2545–2553 (2018).
    Article  Google Scholar 

    42.
    Oziel, L. et al. Role for Atlantic inflows and sea ice loss on shifting phytoplankton blooms in the Barents Sea. J. Geophys. Res. 122, 5121–5139 (2017).
    Article  Google Scholar 

    43.
    Paulsen, M. L. et al. Synechococcus in the Atlantic gateway to the Arctic Ocean. Front. Mar. Sci. 3, 191 (2016).
    Article  Google Scholar 

    44.
    Winter, A., Henderiks, J., Beaufort, L., Rickaby, R. E. M. & Brown, C. W. Poleward expansion of the coccolithophore Emiliania huxleyi. J. Plankton Res. 36, 316–325 (2014).
    CAS  Article  Google Scholar 

    45.
    Wassmann, P. et al. The contiguous domains of Arctic Ocean advection: trails of life and death. Prog. Oceanogr. 139, 42–65 (2015).
    Article  Google Scholar 

    46.
    Kortsch, S., Primicerio, R., Fossheim, M., Dolgov, A. V. & Aschan, M. Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proc. Royal Soc. B 282, 20151546 (2015).
    Article  Google Scholar 

    47.
    Frainer, A. et al. Climate-driven changes in functional biogeography of Arctic marine fish communities. Proc. Natl Acad. Sci. USA 114, 12202–12207 (2017).
    CAS  Article  Google Scholar 

    48.
    Fossheim, M. et al. Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat. Clim. Change 5, 673–677 (2015).
    Article  Google Scholar 

    49.
    Beaugrand, G. et al. Prediction of unprecedented biological shifts in the global ocean. Nat. Clim. Change 9, 237–243 (2019).
    Article  Google Scholar 

    50.
    Carmack, E. C. et al. Freshwater and its role in the Arctic marine system: sources, disposition, storage, export, and physical and biogeochemical consequences in the Arctic and global oceans. J. Geophys. Res. Biogeosci. 121, 675–717 (2016).
    CAS  Article  Google Scholar 

    51.
    Marchese, C. et al. Changes in phytoplankton bloom phenology over the North Water (NOW) polynya: a response to changing environmental conditions. Polar Biol. 40, 1721–1737 (2017).
    Article  Google Scholar 

    52.
    Mayot, N. et al. Springtime export of Arctic sea ice influences phytoplankton production in the Greenland Sea. J. Geophys. Res. Oceans 125, e2019JC015799 (2020).
    Article  Google Scholar 

    53.
    Carmack, E. C. The alpha/beta ocean distinction: a perspective on freshwater fluxes, convection, nutrients and productivity in high-latitude seas. Deep Sea Res. Pt. 2 54, 2578–2598 (2007).
    Article  Google Scholar 

    54.
    Blais, M. et al. Contrasting interannual changes in phytoplankton productivity and community structure in the coastal Canadian Arctic Ocean. Limnol. Oceanogr. 62, 2480–2497 (2017).
    Article  Google Scholar 

    55.
    Meire, L. et al. High export of dissolved silica from the Greenland Ice Sheet. Geophys. Res. Lett. 43, 9173–9182 (2016).
    CAS  Article  Google Scholar 

    56.
    Hawkings, J. R. et al. Ice sheets as a significant source of highly reactive nanoparticulate iron to the oceans. Nat. Commun. 5, 3929 (2014).
    CAS  Article  Google Scholar 

    57.
    Hawkings, J. et al. The Greenland Ice Sheet as a hot spot of phosphorus weathering and export in the Arctic. Glob. Biogeochem. Cycle 30, 191–210 (2016).
    CAS  Article  Google Scholar 

    58.
    Arrigo, K. R. et al. Melting glaciers stimulate large summer phytoplankton blooms in southwest Greenland waters. Geophys. Res. Lett. 44, 6278–6285 (2017).
    Article  Google Scholar 

    59.
    Meire, L. et al. Marine-terminating glaciers sustain high productivity in Greenland fjords. Glob. Change Biol. 23, 5344–5357 (2017).
    Article  Google Scholar 

    60.
    Boone, W. et al. Coastal freshening prevents fjord bottom water renewal in northeast Greenland: a mooring study from 2003 to 2015. Geophys. Res. Lett. 45, 2726–2733 (2018).
    Article  Google Scholar 

    61.
    Le Fouest, V. et al. Modeling plankton ecosystem functioning and nitrogen fluxes in the oligotrophic waters of the Beaufort Sea, Arctic Ocean: a focus on light-driven processes. Biogeosciences 10, 4785–4800 (2013).
    Article  Google Scholar 

    62.
    Le Fouest, V., Manizza, M., Tremblay, B. & Babin, M. Modelling the impact of riverine DON removal by marine bacterioplankton on primary production in the Arctic Ocean. Biogeosciences 12, 3385–3402 (2015).
    Article  CAS  Google Scholar 

    63.
    Tremblay, J.-É. et al. Impact of river discharge, upwelling and vertical mixing on the nutrient loading and productivity of the Canadian Beaufort Shelf. Biogeosciences 11, 4853–4868 (2014).
    Article  Google Scholar 

    64.
    Ardyna, M. et al. Shelf-basin gradients shape ecological phytoplankton niches and community composition in the coastal Arctic Ocean (Beaufort Sea). Limnol. Oceanogr. 62, 2113–2132 (2017).
    Article  Google Scholar 

    65.
    Fichot, C. G. et al. Pan-Arctic distributions of continental runoff in the Arctic Ocean. Sci. Rep. 3, 1053 (2013).
    Article  CAS  Google Scholar 

    66.
    Matsuoka, A. et al. Pan-Arctic optical characteristics of colored dissolved organic matter: tracing dissolved organic carbon in changing Arctic waters using satellite ocean color data. Remote Sens. Environ. 200, 89–101 (2017).
    Article  Google Scholar 

    67.
    Arrigo, K. R. et al. Phytoplankton blooms beneath the sea ice in the Chukchi Sea. Deep Sea Res. Pt. 2 105, 1–16 (2014).
    Article  Google Scholar 

    68.
    Arrigo, K. R. et al. Massive phytoplankton blooms under Arctic sea ice. Science 336, 1408 (2012).
    CAS  Article  Google Scholar 

    69.
    Kelly, R. et al. Recent burning of boreal forests exceeds fire regime limits of the past 10,000 years. Proc. Natl Acad. Sci. USA 110, 13055–13060 (2013).
    CAS  Article  Google Scholar 

    70.
    French, N. H. F. et al. Fire in Arctic tundra of Alaska: past fire activity, future fire potential, and significance for land management and ecology. Int. J. Wildland Fire 24, 1045–1061 (2015).
    Article  Google Scholar 

    71.
    Masrur, A., Petrov, A. N. & DeGroote, J. Circumpolar spatio-temporal patterns and contributing climatic factors of wildfire activity in the Arctic tundra from 2001–2015. Environ. Res. Lett. 13, 014019 (2018).
    Article  Google Scholar 

    72.
    Evangeliou, N. et al. Open fires in Greenland in summer 2017: transport, deposition and radiative effects of BC, OC and BrC emissions. Atmos. Chem. Phys. 19, 1393–1411 (2019).
    CAS  Article  Google Scholar 

    73.
    Lutsch, E. et al. Unprecedented atmospheric ammonia concentrations detected in the high Arctic from the 2017 Canadian wildfires. J. Geophys. Res. Atmos. 124, 8178–8202 (2019).
    CAS  Article  Google Scholar 

    74.
    Skiles, S. M., Flanner, M., Cook, J. M., Dumont, M. & Painter, T. H. Radiative forcing by light-absorbing particles in snow. Nat. Clim. Change 8, 964–971 (2018).
    Article  Google Scholar 

    75.
    Light, B., Eicken, H., Maykut, G. A. & Grenfell, T. C. The effect of included participates on the spectral albedo of sea ice. J. Geophys. Res. Oceans 103, 27739–27752 (1998).
    Article  Google Scholar 

    76.
    Holland, M. M., Bailey, D. A., Briegleb, B. P., Light, B. & Hunke, E. Improved sea ice shortwave radiation physics in CCSM4: the impact of melt ponds and aerosols on Arctic sea ice. J. Climate 25, 1413–1430 (2011).
    Article  Google Scholar 

    77.
    Marks, A. A., Lamare, M. L. & King, M. D. Optical properties of sea ice doped with black carbon – an experimental and radiative-transfer modelling comparison. Cryosphere 11, 2867–2881 (2017).
    Article  Google Scholar 

    78.
    Dentener, F. et al. Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob. Biogeochem. Cycle 20, GB4003 (2006).
    Article  CAS  Google Scholar 

    79.
    Mahowald, N. et al. Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts. Glob. Biogeochem. Cycle 22, GB4026 (2008).
    Article  CAS  Google Scholar 

    80.
    Torres-Valdés, S., Tsubouchi, T., Davey, E., Yashayaev, I. & Bacon, S. Relevance of dissolved organic nutrients for the Arctic Ocean nutrient budget. Geophys. Res. Lett. 43, 6418–6426 (2016).
    Article  CAS  Google Scholar 

    81.
    AMAP Assessment 2018: Arctic Ocean Acidification (AMAP, 2018).

    82.
    Yamamoto-Kawai, M., McLaughlin, F. A., Carmack, E. C., Nishino, S. & Shimada, K. Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326, 1098–1100 (2009).
    CAS  Article  Google Scholar 

    83.
    Qi, D. et al. Increase in acidifying water in the western Arctic Ocean. Nat. Clim. Change 7, 195–199 (2017).
    CAS  Article  Google Scholar 

    84.
    Terhaar, J., Kwiatkowski, L. & Bopp, L. Emergent constraint on Arctic Ocean acidification in the twenty-first century. Nature 582, 379–383 (2020).
    CAS  Article  Google Scholar 

    85.
    Hoppe, C. J. M. et al. Resistance of Arctic phytoplankton to ocean acidification and enhanced irradiance. Polar Biol. 41, 399–413 (2018).
    CAS  Article  Google Scholar 

    86.
    Hoppe, C. J. M., Schuback, N., Semeniuk, D. M., Maldonado, M. T. & Rost, B. Functional redundancy facilitates resilience of subarctic phytoplankton assemblages toward ocean acidification and high irradiance. Front. Mar. Sci. 4, 229 (2017).
    Article  Google Scholar 

    87.
    Hoppe, C. J. M., Wolf, K. K. E., Schuback, N., Tortell, P. D. & Rost, B. Compensation of ocean acidification effects in Arctic phytoplankton assemblages. Nat. Clim. Change 8, 529–533 (2018).
    CAS  Article  Google Scholar 

    88.
    Hussherr, R. et al. Impact of ocean acidification on Arctic phytoplankton blooms and dimethyl sulfide concentration under simulated ice-free and under-ice conditions. Biogeosciences 14, 2407–2427 (2017).
    CAS  Article  Google Scholar 

    89.
    White, E., Hoppe, C. J. M. & Rost, B. The Arctic picoeukaryote Micromonas pusilla benefits from ocean acidification under constant and dynamic light. Biogeosciences 17, 635–647 (2020).
    CAS  Article  Google Scholar 

    90.
    Yoshimura, T. et al. Impacts of elevated CO2 on particulate and dissolved organic matter production: microcosm experiments using iron-deficient plankton communities in open subarctic waters. J. Oceanogr. 69, 601–618 (2013).
    CAS  Article  Google Scholar 

    91.
    Thoisen, C., Riisgaard, K., Lundholm, N., Nielsen, T. G. & Hansen, P. J. Effect of acidification on an Arctic phytoplankton community from Disko Bay, West Greenland. Mar. Ecol. Prog. Ser. 520, 21–34 (2015).
    CAS  Article  Google Scholar 

    92.
    Coello-Camba, A., Agustí, S., Holding, J., Arrieta, J. M. & Duarte, C. M. Interactive effect of temperature and CO2 increase in Arctic phytoplankton. Front. Mar. Sci. 1, 49 (2014).
    Article  Google Scholar 

    93.
    Perovich, D. K. & Polashenski, C. Albedo evolution of seasonal Arctic sea ice. Geophys. Res. Lett. 39, L08501 (2012).
    Article  Google Scholar 

    94.
    Perovich, D. K. The Optical Properties of Sea Ice (Office of Naval Research, 1996).

    95.
    Hill, V. J., Cota, G. & Stockwell, D. Spring and summer phytoplankton communities in the Chukchi and Eastern Beaufort Seas. Deep Sea Res. Pt 2 52, 3369–3385 (2005).
    Article  Google Scholar 

    96.
    Perrette, M., Yool, A., Quartly, G. D. & Popova, E. E. Near-ubiquity of ice-edge blooms in the Arctic. Biogeosciences 7, 515–524 (2011).
    Article  Google Scholar 

    97.
    Janout, M. A. et al. Sea-ice retreat controls timing of summer plankton blooms in the Eastern Arctic Ocean. Geophys. Res. Lett. 12, 12493–12501 (2016).
    Article  Google Scholar 

    98.
    Sakshaug, E. Biomass and productivity distributions and their variability in the Barents Sea. ICES J. Mar. Sci. 54, 341–350 (1997).
    Article  Google Scholar 

    99.
    Subba Rao, D. V. & Platt, T. Primary production of arctic waters. Polar Biol. 3, 191–201 (1984).
    Article  Google Scholar 

    100.
    Pabi, S., van Dijken, G. L. & Arrigo, K. R. Primary production in the Arctic Ocean, 1998–2006. J. Geophys. Res. 113, C08005 (2008).
    Article  CAS  Google Scholar 

    101.
    Arrigo, K. R. & van Dijken, G. L. Secular trends in Arctic Ocean net primary production. J. Geophys. Res. 116, C09011 (2011).
    Google Scholar 

    102.
    Fortier, M., Fortier, L., Michel, C. & Legendre, L. Climatic and biological forcing of the vertical flux of biogenic particles under seasonal Arctic sea ice. Mar. Ecol. Prog. Ser. 225, 1–16 (2002).
    Article  Google Scholar 

    103.
    Mundy, C. J. et al. Role of environmental factors on phytoplankton bloom initiation under landfast sea ice in Resolute Passage, Canada. Mar. Ecol. Prog. Ser. 497, 39–49 (2014).
    Article  Google Scholar 

    104.
    Duerksen, S. W. et al. Large, omega-3 rich, pelagic diatoms under Arctic Sea ice: sources and Implications for food webs. PLoS ONE 9, e114070 (2014).
    Article  CAS  Google Scholar 

    105.
    Galindo, V. et al. Contrasted sensitivity of DMSP production to high light exposure in two Arctic under-ice blooms. J. Exp. Mar. Biol. Ecol. 475, 38–48 (2016).
    CAS  Article  Google Scholar 

    106.
    Galindo, V. et al. Under-ice microbial dimethylsulfoniopropionate metabolism during the melt period in the Canadian Arctic Archipelago. Mar. Ecol. Prog. Ser. 524, 39–53 (2015).
    CAS  Article  Google Scholar 

    107.
    Galindo, V. et al. Biological and physical processes influencing sea ice, under-ice algae, and dimethylsulfoniopropionate during spring in the Canadian Arctic Archipelago. J. Geophys. Res. Oceans 119, 3746–3766 (2014).
    CAS  Article  Google Scholar 

    108.
    Ardyna, M. et al. Ecological drivers controlling spring phytoplankton blooms in the Arctic Ocean. Elem. Sci. Anth. 8, 30 (2020).
    Article  Google Scholar 

    109.
    Assmy, P. et al. Leads in Arctic pack ice enable early phytoplankton blooms below snow-covered sea ice. Sci. Rep. 7, 40850 (2017).
    CAS  Article  Google Scholar 

    110.
    Mayot, N. et al. Assessing phytoplankton activities in the seasonal ice zone of the Greenland Sea over an annual cycle. J. Geophys. Res. Oceans 123, 8004–8025 (2018).
    Article  Google Scholar 

    111.
    Strass, V. H. & Nöthig, E.-M. Seasonal shifts in ice edge phytoplankton blooms in the Barents Sea related to the water column stability. Polar Biol. 16, 409–422 (1996).
    Article  Google Scholar 

    112.
    Pavlov, A. K. et al. Altered inherent optical properties and estimates of the underwater light field during an Arctic under-ice bloom of Phaeocystis pouchetii. J. Geophys. Res. Oceans 122, 4939–4961 (2017).
    Article  Google Scholar 

    113.
    Lalande, C. et al. Variability in under-ice export fluxes of biogenic matter in the Arctic Ocean. Glob. Biogeochem. Cycle 28, 571–583 (2014).
    CAS  Article  Google Scholar 

    114.
    Yager, P. L. et al. Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol. Oceanogr. 46, 790–801 (2001).
    CAS  Article  Google Scholar 

    115.
    Hill, V. J., Light, B., Steele, M. & Zimmerman, R. C. Light availability and phytoplankton growth beneath Arctic sea ice: integrating observations and modeling. J. Geophys. Res. Oceans 123, 3651–3667 (2018).
    Article  Google Scholar 

    116.
    Lewis, K. M. et al. Photoacclimation of Arctic Ocean phytoplankton to shifting light and nutrient limitation. Limnol. Oceanogr. 64, 284–301 (2019).
    CAS  Article  Google Scholar 

    117.
    Grebmeier, J. M. Shifting patterns of life in the Pacific Arctic and sub-Arctic seas. Annu. Rev. Mar. Sci. 4, 63–78 (2012).
    Article  Google Scholar 

    118.
    Grebmeier, J. M., Moore, S. E., Overland, J. E., Frey, K. E. & Gradinger, R. Biological response to recent Pacific Arctic sea ice retreats. Eos Trans. Amer. Geophys. Union 91, 161–162 (2010).
    Article  Google Scholar 

    119.
    Tamelander, T., Kivimäe, C., Bellerby, R. G. J., Renaud, P. E. & Kristiansen, S. Base-line variations in stable isotope values in an Arctic marine ecosystem: effects of carbon and nitrogen uptake by phytoplankton. Hydrobiologia 630, 63–73 (2009).
    CAS  Article  Google Scholar 

    120.
    Degen, R. et al. Patterns and drivers of megabenthic secondary production on the Barents Sea shelf. Mar. Ecol. Prog. Ser. 546, 1–16 (2016).
    Article  Google Scholar 

    121.
    Wassmann, P. & Reigstad, M. Future Arctic Ocean seasonal ice zones and implications for pelagic-benthic coupling. Oceanography 24, 220–231 (2011).
    Article  Google Scholar 

    122.
    Fujiwara, A. et al. Changes in phytoplankton community structure during wind-induced fall bloom on the central Chukchi shelf. Polar Biol. 41, 1279–1295 (2018).
    Article  Google Scholar 

    123.
    Uchimiya, M. et al. Coupled response of bacterial production to a wind-induced fall phytoplankton bloom and sediment resuspension in the Chukchi Sea Shelf, Western Arctic Ocean. Front. Mar. Sci. 3, 231 (2016).
    Article  Google Scholar 

    124.
    Goñi, M. A. et al. Particulate organic matter distributions in surface waters of the Pacific Arctic shelf during the late summer and fall season. Mar. Chem. 211, 75–93 (2019).
    Article  CAS  Google Scholar 

    125.
    Juranek, L., Takahashi, T., Mathis, J. & Pickart, R. Significant biologically mediated CO2 uptake in the Pacific Arctic during the late open water season. J. Geophys. Res. Oceans 124, 821–843 (2019).
    CAS  Article  Google Scholar 

    126.
    Not, F. et al. Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnol. Oceanogr. 50, 1677–1686 (2005).
    CAS  Article  Google Scholar 

    127.
    Ardyna, M. et al. Parameterization of vertical chlorophyll a in the Arctic Ocean: impact of the subsurface chlorophyll maximum on regional, seasonal, and annual primary production estimates. Biogeosciences 10, 4383–4404 (2013).
    Article  CAS  Google Scholar 

    128.
    Wassmann, P., Peinert, R. & Smetacek, V. Patterns of production and sedimentation in the boreal and polar Northeast Atlantic. Polar Res. 10, 209–228 (1991).
    Article  Google Scholar 

    129.
    Martin, J. et al. Prevalence, structure and properties of subsurface chlorophyll maxima in Canadian Arctic waters. Mar. Ecol. Prog. Ser. 412, 69–84 (2010).
    CAS  Article  Google Scholar 

    130.
    Coupel, P. et al. The impact of freshening on phytoplankton production in the Pacific Arctic Ocean. Prog. Oceanogr. 131, 113–125 (2015).
    Article  Google Scholar 

    131.
    Huot, Y., Babin, M. & Bruyant, F. Photosynthetic parameters in the Beaufort Sea in relation to the phytoplankton community structure. Biogeosciences 10, 3445–3454 (2013).
    Article  Google Scholar 

    132.
    Monier, A. et al. Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J. 9, 990–1002 (2014).
    Article  CAS  Google Scholar 

    133.
    McLaughlin, F. A. & Carmack, E. C. Deepening of the nutricline and chlorophyll maximum in the Canada Basin interior. Geophys. Res. Lett. 37, L24602 (2010).
    Article  Google Scholar 

    134.
    Gran, H. H. Das Plankton des norwegischen Nordmeeres (Fiskeridirektoratets havforskningsinstitutt, 1902).

    135.
    Poulin, M. et al. The pan-Arctic biodiversity of marine pelagic and sea-ice unicellular eukaryotes: a first-attempt assessment. Mar. Biodiv. 41, 13–28 (2011).
    Article  Google Scholar 

    136.
    Lovejoy, C., von Quillfeldt, C., Hopcroft, R. R., Poulin, M. & Thaler, M. in State of the Arctic Marine Biodiversity Report (eds T Barry. et al.) 62–83 (Conservation of Arctic Flora and Fauna International Secretariat, 2017).

    137.
    Tremblay, G. et al. Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: strong numerical dominance by picoeukaryotes. Aquat. Microb. Ecol. 54, 55–70 (2009).
    Article  Google Scholar 

    138.
    Berge, J. et al. Diel vertical migration of Arctic zooplankton during the polar night. Biol. Lett. 5, 69–72 (2009).
    Article  Google Scholar 

    139.
    Lovejoy, C. et al. Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J. Phycol. 43, 78–89 (2007).
    CAS  Article  Google Scholar 

    140.
    Stoecker, D. K. & Lavrentyev, P. J. Mixotrophic plankton in the polar seas: a pan-Arctic review. Front. Mar. Sci. 5, 292 (2018).
    Article  Google Scholar 

    141.
    Balzano, S. et al. Diversity of cultured photosynthetic flagellates in the northeast Pacific and Arctic Oceans in summer. Biogeosciences 9, 4553–4571 (2012).
    CAS  Article  Google Scholar 

    142.
    Joli, N. et al. Need for focus on microbial species following ice melt and changing freshwater regimes in a Janus Arctic Gateway. Sci. Rep. 8, 9405 (2018).
    Article  CAS  Google Scholar 

    143.
    Okolodkov, Y. B. The global distributional patterns of toxic, bloom dinoflagellates recorded from the Eurasian Arctic. Harmful Algae 4, 351–369 (2005).
    Article  Google Scholar 

    144.
    Brosnahan, M. L., Fischer, A. D., Lopez, C. B., Moore, S. K. & Anderson, D. M. Cyst-forming dinoflagellates in a warming climate. Harmful Algae 91, 101728 (2020).
    Article  Google Scholar 

    145.
    Lefebvre, K. A. et al. Prevalence of algal toxins in Alaskan marine mammals foraging in a changing arctic and subarctic environment. Harmful Algae 55, 13–24 (2016).
    CAS  Article  Google Scholar 

    146.
    Lovejoy, C., Legendre, L., Martineau, M. J., Bacle, J. & von Quillfeldt, C. H. Distribution of phytoplankton and other protists in the North Water. Deep Sea Res. Pt 2 49, 5027–5047 (2002).
    Article  Google Scholar 

    147.
    Booth, B. C. et al. Dynamics of Chaetoceros socialis blooms in the North Water. Deep Sea Res. Pt 2 49, 5003–5025 (2002).
    CAS  Article  Google Scholar 

    148.
    Schoemann, V., Becquevort, S., Stefels, J., Rousseau, V. & Lancelot, C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea. Res. 53, 43–66 (2005).
    CAS  Article  Google Scholar 

    149.
    Smith, W. O. et al. Importance of Phaeocystis blooms in the high-latitude ocean carbon cycle. Nature 352, 514–516 (1991).
    Article  Google Scholar 

    150.
    Simo-Matchim, A. G., Gosselin, M., Poulin, M., Ardyna, M. & Lessard, S. Summer and fall distribution of phytoplankton in relation to environmental variables in Labrador fjords, with special emphasis on Phaeocystis pouchetii. Mar. Ecol. Prog. Ser. 572, 19–42 (2017).
    CAS  Article  Google Scholar 

    151.
    Crawford, D. W., Cefarelli, A. O., Wrohan, I. A., Wyatt, S. N. & Varela, D. E. Spatial patterns in abundance, taxonomic composition and carbon biomass of nano- and microphytoplankton in Subarctic and Arctic Seas. Prog. Oceanogr. 162, 132–159 (2018).
    Article  Google Scholar 

    152.
    Nöthig, E.-M. et al. Summertime plankton ecology in Fram Strait—a compilation of long- and short-term observations. Polar Res. 34, 23349 (2015).
    Article  CAS  Google Scholar 

    153.
    Hodal, H., Falk-Petersen, S., Hop, H., Kristiansen, S. & Reigstad, M. Spring bloom dynamics in Kongsfjorden, Svalbard: nutrients, phytoplankton, protozoans and primary production. Polar Biol. 35, 191–203 (2012).
    Article  Google Scholar 

    154.
    Hátún, H. et al. The subpolar gyre regulates silicate concentrations in the North Atlantic. Sci. Rep. 7, 14576 (2017).
    Article  CAS  Google Scholar 

    155.
    Slagstad, D., Wassmann, P. F. J. & Ellingsen, I. Physical constrains and productivity in the future Arctic Ocean. Front. Mar. Sci. 2, 85 (2015).
    Article  Google Scholar 

    156.
    Hegseth, E. N. et al. in The Ecosystem of Kongsfjorden, Svalbard (eds Hop, H. & Wiencke, C.) 173–227 (Springer International Publishing, 2019).

    157.
    Lacour, T. et al. Decoupling light harvesting, electron transport and carbon fixation during prolonged darkness supports rapid recovery upon re-illumination in the Arctic diatom Chaetoceros neogracilis. Polar Biol. http://doi.org/d6rs (2019).

    158.
    Kvernvik, A. C. et al. Fast reactivation of photosynthesis in arctic phytoplankton during the polar night. J. Phycol. 54, 461–470 (2018).
    CAS  Article  Google Scholar 

    159.
    McMinn, A. & Martin, A. Dark survival in a warming world. Proc. Biol. Sci. 280, 20122909 (2013).
    CAS  Google Scholar 

    160.
    Joli, N., Monier, A., Logares, R. & Lovejoy, C. Seasonal patterns in Arctic prasinophytes and inferred ecology of Bathycoccus unveiled in an Arctic winter metagenome. ISME J. 11, 13727 (2017).
    Article  Google Scholar 

    161.
    Vader, A., Marquardt, M., Meshram, A. R. & Gabrielsen, T. M. Key Arctic phototrophs are widespread in the polar night. Polar Biol. 38, 13–21 (2015).
    Article  Google Scholar 

    162.
    McMinn, A. & Martin, A. Dark survival in a warming world. Proc. Biol. Sci. 280, 20122909 (2013).
    CAS  Google Scholar 

    163.
    van de Poll, W., Abdullah, E., Visser, R., Fischer, P. & Buma, A. Taxon-specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring. Limnol. Oceanogr. 65, 903–914 (2019).
    Article  Google Scholar 

    164.
    Boyd, P. W., Lennartz, S. T., Glover, D. M. & Doney, S. C. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5, 71–79 (2014).
    Article  Google Scholar 

    165.
    Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).
    Article  Google Scholar 

    166.
    Vancoppenolle, M. et al. Future Arctic Ocean primary productivity from CMIP5 simulations: uncertain outcome, but consistent mechanisms. Glob. Biogeochem. Cycle 27, 605–619 (2013).
    CAS  Article  Google Scholar 

    167.
    Tedesco, L., Vichi, M. & Scoccimarro, E. Sea-ice algal phenology in a warmer Arctic. Sci. Adv. 5, eaav4830 (2019).
    CAS  Article  Google Scholar 

    168.
    Babin, M. et al. Estimation of primary production in the Arctic Ocean using ocean colour remote sensing and coupled physical-biological models: strengths, limitations and how they compare. Prog. Oceanogr. 139, 197–220 (2015).
    Article  Google Scholar 

    169.
    Lacour, T., Larivière, J. & Babin, M. Growth, Chl a content, photosynthesis, and elemental composition in polar and temperate microalgae. Limnol. Oceanogr. 201, 43–58 (2016).
    Google Scholar 

    170.
    Lacour, T. et al. The role of sustained photoprotective non-photochemical quenching in low temperature and high light acclimation in the bloom-forming Arctic diatom Thalassiosira gravida. Front. Mar. Sci. 5, 354 (2018).
    Article  Google Scholar 

    171.
    Graham, R. M. et al. Winter storms accelerate the demise of sea ice in the Atlantic sector of the Arctic Ocean. Sci. Rep. 9, 9222 (2019).
    Article  CAS  Google Scholar 

    172.
    Berge, J. et al. Unexpected levels of biological activity during the polar night offer new perspectives on a warming Arctic. Curr. Biol. 25, 2555–2561 (2015).
    CAS  Article  Google Scholar 

    173.
    Berge, J. et al. In the dark: a review of ecosystem processes during the Arctic polar night. Prog. Oceanogr. 139, 258–271 (2015).
    Article  Google Scholar 

    174.
    Kipp, L. E., Charette, M. A., Moore, W. S., Henderson, P. B. & Rigor, I. G. Increased fluxes of shelf-derived materials to the central Arctic Ocean. Sci. Adv. 4, eaao1302 (2018).
    Article  CAS  Google Scholar 

    175.
    Abram, N. J. et al. Early onset of industrial-era warming across the oceans and continents. Nature 536, 411 (2016).
    CAS  Article  Google Scholar 

    176.
    Osman, M. B. et al. Industrial-era decline in subarctic Atlantic productivity. Nature 569, 551–555 (2019).
    CAS  Article  Google Scholar 

    177.
    Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).
    CAS  Article  Google Scholar 

    178.
    Rahmstorf, S. et al. Exceptional twentieth-century slowdown in Atlantic Ocean overturning circulation. Nat. Clim. Change 5, 475–480 (2015).
    Article  Google Scholar 

    179.
    Caesar, L., Rahmstorf, S., Robinson, A., Feulner, G. & Saba, V. Observed fingerprint of a weakening Atlantic Ocean overturning circulation. Nature 556, 191–196 (2018).
    CAS  Article  Google Scholar 

    180.
    Thornalley, D. J. R. et al. Anomalously weak Labrador Sea convection and Atlantic overturning during the past 150 years. Nature 556, 227–230 (2018).
    CAS  Article  Google Scholar 

    181.
    Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).
    CAS  Article  Google Scholar 

    182.
    Bakker, P. et al. Fate of the Atlantic Meridional Overturning Circulation: strong decline under continued warming and Greenland melting. Geophys. Res. Lett. 43, 12,252–12,260 (2016).
    Article  Google Scholar 

    183.
    Takahashi, T. et al. Climatological mean and decadal change in surface ocean pCO2, and net sea-air CO2 flux over the global oceans. Deep Sea Res. Pt 2 56, 554–577 (2009).
    CAS  Article  Google Scholar 

    184.
    Stock, C. A. et al. Reconciling fisheries catch and ocean productivity. Proc. Natl Acad. Sci. USA 114, E1441–E1449 (2017).
    CAS  Article  Google Scholar 

    185.
    Cavalieri, D. J., Parkinson, C., Gloersen, P. & Zwally, H. J. Sea Ice Concentrations From Nimbus-7 SMMR and DMSP SSM/I Passive Microwave Data Version 1 (NASA National Snow and Ice Data Center Distributed Active Archive Center, 1996); https://nsidc.org/data/NSIDC-0051/versions/1

    186.
    Tschudi, M., Meier, W. N., Stewart, J. S., Fowler, C. & Maslanik, J. EASE-Grid Sea Ice Age Version 4 (NASA National Snow and Ice Data Center Distributed Active Archive Center, 2019); https://doi.org/10.5067/UTAV7490FEPB

    187.
    Anderson, L. G. & Macdonald, R. W. Observing the Arctic Ocean carbon cycle in a changing environment. Polar Res. 34, 26891 (2015).
    Article  CAS  Google Scholar 

    188.
    Horner, R. & Schrader, G. C. Contributions of ice Algae, phytoplankton, and benthic microalgae to primary production in nearshore regions of the Beaufort Sea. Arctic 35, 485–503 (1982).
    Article  Google Scholar 

    189.
    Mundy, C. J. et al. Contribution of under-ice primary production to an ice-edge upwelling phytoplankton bloom in the Canadian Beaufort Sea. Geophys. Res. Lett. 36, L17601 (2009).
    Article  Google Scholar 

    190.
    Oziel, L. et al. Environmental factors influencing the seasonal dynamics of under-ice spring blooms in Baffin Bay. Elem. Sci. Anth. 7, 34 (2019).
    Article  Google Scholar 

    191.
    Ferland, J., Gosselin, M. & Starr, M. Environmental control of summer primary production in the Hudson Bay system: the role of stratification. J. Mar. Syst. 88, 385–400 (2011).
    Article  Google Scholar 

    192.
    Lalande, C., Nöthig, E. M. & Fortier, L. Algal export in the Arctic Ocean in times of global warming. Geophys. Res. Lett. 46, 5959–5967 (2019).
    Article  Google Scholar 

    193.
    Lalande, C., Grebmeier, J. M., Hopcroft, R. R. & Danielson, S. L. Annual cycle of export fluxes of biogenic matter near Hanna Shoal in the northeast Chukchi Sea. Deep Sea Res. Pt 2 177, 104730 (2020).
    CAS  Article  Google Scholar 

    194.
    Silkin, V., Pautova, L., Giordano, M., Kravchishina, M. & Artemiev, V. Interannual variability of Emiliania huxleyi blooms in the Barents Sea: in situ data 2014–2018. Mar. Pollut. Bull. 158, 111392 (2020).
    CAS  Article  Google Scholar  More

  • in

    Protein metabolism and physical fitness are physiological determinants of body condition in Southern European carnivores

    1.
    Labocha, M. K., Schutz, H. & Hayes, J. P. Which body condition index is best?. Oikos 123(1), 111–119 (2014).
    Article  Google Scholar 
    2.
    Wilder, S. M., Raubenheimer, D. & Simpson, S. J. Moving beyond body condition indices as an estimate of fitness in ecological and evolutionary studies. Funct. Ecol. 30(1), 108–115 (2016).
    Article  Google Scholar 

    3.
    Grémillet, D. et al. Energetic fitness: Field metabolic rates assessed via 3D accelerometry complement conventional fitness metrics. Funct. Ecol. 32(5), 1203–1213 (2018).
    Article  Google Scholar 

    4.
    Hill, G. E. Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol. Lett. 14(7), 625–634 (2011).
    PubMed  Article  Google Scholar 

    5.
    Coon, C. A., Nichols, B. C., McDonald, Z. & Stoner, D. C. Effects of land-use change and prey abundance on the body condition of an obligate carnivore at the wildland-urban interface. Landsc. Urban Plan. 192, 103648 (2019).
    Article  Google Scholar 

    6.
    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 (2009).
    Article  Google Scholar 

    7.
    Barnett, C. A., Suzuki, T. N., Sakaluk, S. K. & Thompson, C. F. Mass-based condition measures and their relationship with fitness: in what condition is condition?. J. Zool. 296(1), 1–5 (2015).
    Article  Google Scholar 

    8.
    Warner, D. A., Johnson, M. S. & Nagy, T. R. Validation of body condition indices and quantitative magnetic resonance in estimating body composition in a small lizard. J. Exp. Zool. A. Physiol. 325(9), 588–597 (2016).
    CAS  Article  Google Scholar 

    9.
    Stevenson, R. & Woods, W. A. Condition indices for conservation: new uses for evolving tools. Int. Comp. Biol. 46(6), 1169–1190 (2006).
    CAS  Article  Google Scholar 

    10.
    Homyack, J. A. Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl. Res. 37(4), 332–342 (2010).
    Article  Google Scholar 

    11.
    Hayes, J. P. & Shonkwiler, J. S. Morphometric indicators of body condition, worthwhile or wishful thinking? In Body Composition Analysis of Animals, a Handbook of Non-destructive Methods (ed. Spearman, J. R.) 8–38 (Cambridge Univ. Press, Cambridge, 2001).
    Google Scholar 

    12.
    Peig, J. & Green, A. J. The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct. Ecol. 24(6), 1323–1332 (2010).
    Article  Google Scholar 

    13.
    Larivière, S. et al. Influence of food shortage during the summer on body composition and reproductive hormones in the red fox, Vulpes vulpes. Can. J. Zool. 79(3), 471–477 (2001).
    Article  Google Scholar 

    14.
    Parker, K. L., Barboza, P. S. & Gillingham, M. P. Nutrition integrates environmental responses of ungulates. Funct. Ecol. 23(1), 57–69 (2009).
    Article  Google Scholar 

    15.
    Risco, D. et al. Biometrical measurements as efficient indicators to assess wild boar body condition. Ecol. Indic. 88, 43–50 (2018).
    Article  Google Scholar 

    16.
    Gosler, A. G., Greenwood, J. J. & Perrins, C. Predation risk and the cost of being fat. Nature 377(6550), 621 (1995).
    ADS  CAS  Article  Google Scholar 

    17.
    Higginson, A. D., McNamara, J. M. & Houston, A. I. The starvation-predation trade-off predicts trends in body size, muscularity, and adiposity between and within taxa. Am. Nat. 179(3), 338–350 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    18.
    Houston, A. I., Stephens, P. A., Boyd, I. L., Harding, K. C. & McNamara, J. M. Capital or income breeding? A theoretical model of female reproductive strategies. Behav. Ecol. 18(1), 241–250 (2006).
    Article  Google Scholar 

    19.
    Pond, C. M. & Ramsay, M. A. Allometry of the distribution of adipose tissue in Carnivora. Can. J. Zool. 70(2), 342–347 (1992).
    Article  Google Scholar 

    20.
    Kohl, K. D., Coogan, S. C. & Raubenheimer, D. Do wild carnivores forage for prey or for nutrients? Evidence for nutrient-specific foraging in vertebrate predators. BioEssays 37(6), 701–709 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    21.
    Mangipane, L. S. et al. Dietary plasticity in a nutrient-rich system does not influence brown bear (Ursus arctos) body condition or denning. Polar Biol. 41(4), 763–772 (2018).
    Article  Google Scholar 

    22.
    Caspersen, C. J., Powell, K. E. & Christenson, G. M. Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 100(2), 126 (1985).
    CAS  PubMed  PubMed Central  Google Scholar 

    23.
    Graham, A. L. et al. Fitness consequences of immune responses, strengthening the empirical framework for ecoimmunology. Func. Ecol. 25(1), 5–17 (2011).
    Article  Google Scholar 

    24.
    Martin, L. B., Weil, Z. M. & Nelson, R. J. Seasonal changes in vertebrate immune activity, mediation by physiological trade-offs. Phil. Trans. R. Soc. B 363(1490), 321–339 (2007).
    Article  Google Scholar 

    25.
    Kindermann, C., Narayan, E. J. & Hero, J. M. Does physiological response to disease incur cost to reproductive ecology in a sexually dichromatic amphibian species?. Comp. Biochem. Physiol. A. 203, 220–226 (2017).
    CAS  Article  Google Scholar 

    26.
    Whiteman, J. P. et al. Heightened immune system function in polar bears using terrestrial habitats. Physiol. Bioch. Zool 92(1), 1–11 (2019).
    Article  Google Scholar 

    27.
    Garrow, J. S. & Webster, J. Quetelet’s index (W/H2) as a measure of fatness. Int. J. Obes. 9(2), 147–153 (1984).
    Google Scholar 

    28.
    Fulton, T. W. Rate of growth of sea fishes (ed. Fulton, T. W.) (Neill & Company, Edinburgh, 1902).

    29.
    Nash, R. D., Valencia, A. H. & Geffen, A. J. The origin of Fulton’s condition factor: setting the record straight. Fisheries 31(5), 236–238 (2006).
    Google Scholar 

    30.
    Cren, E. D. The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J. Anim. Ecol. 20, 201 (1951).
    Article  Google Scholar 

    31.
    Jakob, E. M., Marshall, S. D. & Uetz, G. W. Estimating fitness, a comparison of body condition indices. Oikos 77(1), 61–67 (1996).
    Article  Google Scholar 

    32.
    Jolicoeur, P. Linear regressions in fishery research, some comments. J. Fish. B. Can. 32(8), 1491–1494 (1975).
    Article  Google Scholar 

    33.
    Green, A. J. Mass/length residuals: measures of body condition or generators of spurious results?. Ecol. 82(5), 1473–1483 (2001).
    Article  Google Scholar 

    34.
    Lindsjö, J., Fahlman, Å & Törnqvist, E. Animal welfare from mouse to moose – implementing the principles of the 3Rs in wildlife research. J. Wildl. Dis. 52(2S), S65–S77 (2016).
    PubMed  Article  Google Scholar 

    35.
    Guyton, A. C., Hall, J. E. Textbook of medical physiology (ed. Guyton, A. C., Hall, J. E) 11th ed. (Elsevier Saunders, Amsterdam, 2006).

    36.
    McCue, M. D. Starvation physiology, reviewing the different strategies animals use to survive a common challenge. Comp. Bioch. Physiol. A 156, 1–18 (2010).
    Article  CAS  Google Scholar 

    37.
    Russell, K., Lobley, G. E. & Millward, D. J. Whole-body protein turnover of a carnivore, Felis silvestris catus. Br. J. Nutr. 89(1), 29–37 (2003).
    CAS  PubMed  Article  Google Scholar 

    38.
    Delgiudice, G. D., Seal, U. S. & Mech, L. D. Effects of feeding and fasting on wolf blood and urine characteristics. J. Wildl. Manage. 51, 1 (1987).
    Article  Google Scholar 

    39.
    Domingo-Roura, X., Newman, C., Calafell, F. & Macdonald, D. W. Blood biochemistry reflects seasonal nutritional and reproductive constraints in the Eurasian badger (Meles meles). Phys. Biochem. Zool. 74, 450–460 (2001).
    CAS  Article  Google Scholar 

    40.
    Karasov, W. H., del Rio, C. M. Physiological ecology, how animals process energy, nutrients, and toxins (ed. Karasov, W. H., del Rio, C. M.) 1–739 (Princeton University Press, Princeton, 2007).

    41.
    Schmidt, W., Maassen, N., Trost, F. & Böning, D. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur. J. Appl. Physiol. Occ. Physiol. 57(4), 490–498 (1988).
    CAS  Article  Google Scholar 

    42.
    Brocherie, F. et al. Association of hematological variables with team-sport specific fitness performance. PLoS ONE 10(12), e0144446 (2015).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    43.
    McGowan, C. Clinical pathology in the racing horse, the role of clinical pathology in assessing fitness and performance in the racehorse. Vet. Clin. N. Am. 24(2), 405–421 (2008).
    Google Scholar 

    44.
    Warton, D. I., Wright, I. J., Falster, D. S. & Westoby, M. Bivariate line-fitting methods for allometry. Biol. Rev. 81(2), 259–291 (2006).
    PubMed  Article  PubMed Central  Google Scholar 

    45.
    Nussey, D. H., Froy, H., Lemaitre, J. F., Gaillard, J. M. & Austad, S. N. Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12(1), 214–225 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    46.
    Bowers, E. K. et al. Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon). Proc. R. Soc. B 279(1739), 2891–2898 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    47.
    Lobo, A., Marti, J. I. & Gimenez-Cassina, C. C. Regional scale hierarchical classification of temporal series of AVHRR vegetation index. Int. J. Rem. Sens. 18(15), 3167–3193 (1997).
    Article  Google Scholar 

    48.
    Alcaraz, D., Paruelo, J. & Cabello, J. Identification of current ecosystem functional types in the Iberian Peninsula. Glob. Ecol. Biogeogr. 15(2), 200–212 (2006).
    Article  Google Scholar 

    49.
    Oftedal, O. T. & Gittleman, J. L. Patterns of energy output during reproduction in carnivores. In Carnivore Behavior, Ecology, and Evolution (ed. Gittleman, J. L.) (Springer, New York, 1989).
    Google Scholar 

    50.
    Franzmann, A. W. & Schwartz, C. C. Evaluating condition of Alaskan black bears with blood profiles. J. Wildl. Manage. 52(1), 63–70 (1988).
    CAS  Article  Google Scholar 

    51.
    McGuire, L. P. et al. Common condition indices are no more effective than body mass for estimating fat stores in insectivorous bats. J. Mammal. 99(5), 1065–1071 (2018).
    Article  Google Scholar 

    52.
    Stocker, R., Glazer, A. N. & Ames, B. N. Antioxidant activity of albumin-bound bilirubin. Proc. Nat. Acad. Sci. 84(16), 5918–5922 (1987).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    53.
    Beaulieu, M. & Costantini, D. Biomarkers of oxidative status: missing tools in conservation physiology. Conserv. Physiol. 2(1), 014 (2014).
    Article  CAS  Google Scholar 

    54.
    Tothova, C., Nagy, O. & Kovac, G. Serum proteins and their diagnostic utility in veterinary medicine, a review. Vet. Med. 61(9), 475–496 (2016).
    Article  Google Scholar 

    55.
    Peck, H. E., Costa, D. P. & Crocker, D. E. Body reserves influence allocation to immune responses in capital breeding female northern elephant seals. Funct. Ecol. 30(3), 389–397 (2016).
    Article  Google Scholar 

    56.
    Deng, P., Jones, J. C. & Swanson, K. S. Effects of dietary macronutrient composition on the fasted plasma metabolome of healthy adult cats. Metabolomics 10(4), 638–650 (2014).
    CAS  Article  Google Scholar 

    57.
    Wilkens, M. R., Firmenich, C. S., Schnepel, N. & Muscher-Banse, A. S. A reduced protein diet modulates enzymes of vitamin D and cholesterol metabolism in young ruminants. J. Ster. Biochem. Mol. Biol. 186, 196–202 (2019).
    CAS  Article  Google Scholar 

    58.
    Oliveira, R. et al. Toward a genome-wide approach for detecting hybrids: informative SNPs to detect introgression between domestic cats and European wildcats (Felis silvestris). Heredity 115(3), 195–205 (2015).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    59.
    Sikes, R. S. & Gannon, W. L. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92, 235–253 (2011).
    Article  Google Scholar 

    60.
    Chinnadurai, S. K., Strahl-Heldreth, D., Fiorello, C. V. & Harms, C. A. Best-practice guidelines for field-based surgery and anesthesia of free-ranging wildlife I Anesthesia and analgesia. J. Wildl. Dis. 52, S14–S27 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    61.
    Santos, N. et al. Characterization and minimization of the stress response to trapping in free-ranging wolves (Canis lupus): insights from physiology and behavior. Stress 20(5), 513–522 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    62.
    Harris, S. Age determination in the red fox (Vulpes vulpes): an evaluation of technique efficiency as applied to a sample of suburban foxes. J. Zool. 184(1), 91–117 (1978).
    Article  Google Scholar 

    63.
    Gipson, P., Ballard, W., Nowak, R. & Mech, D. Accuracy and precision of estimating age of gray wolves by tooth wear. J. Wildl. Manage. 64(3), 752–758 (2000).
    Article  Google Scholar 

    64.
    Anders, U., von Koenigswald, W., Ruf, I. & Smith, B. H. Generalized individual dental age stages for fossil and extant placental mammals. Paläontol. Z. 85(3), 321–339 (2011).
    Article  Google Scholar 

    65.
    Santos, N. et al. Hematology and serum biochemistry values of free-ranging Iberian wolves (Canis lupus) trapped by leg-hold snares. Eur. J. Wildl. Res. 61(1), 135–141 (2015).
    Article  Google Scholar 

    66.
    Anchinmane, V. & Sankhe, S. Evaluation of hemoglobin estimation with non-cyanide alkaline haematin D-575 method. Int. J. Res. Med. Sci. 44(10), 4297–4299 (2016).
    Article  Google Scholar 

    67.
    R Core Team. R, A language and environment for statistical computing. R Foundation for Statistical Computing (2019). https://www.R-project.org

    68.
    Delignette-Muller, M. L. & Dutang, C. fitdistrplus: an R package for fitting distributions. J. Stat. Softw. 64(4), 1–34 (2015).
    Article  Google Scholar 

    69.
    Anderson, T. W. & Darling, D. A. Asymptotic theory of certain “goodness-of-fit” criteria based on stochastic processes. Ann. Math. Stat. 23, 193–212 (1952).
    MathSciNet  MATH  Article  Google Scholar 

    70.
    Zar, J. H. Encyclopedia of Biostatistics (ed. Zar, J. H.) (Wiley, Hoboken, 2005).

    71.
    Pouillot, R. & Delignette-Muller, M. L. Evaluating variability and uncertainty in microbial quantitative risk assessment using two R packages. Int. J. Food Microb. 142(3), 330–340 (2010).
    Article  Google Scholar 

    72.
    Vose, D. Risk analysis: a quantitative guide (ed. Vose, D.) 1–735 (Wiley, Hoboken, 2008).

    73.
    Warton, D. I. & Hui, F. K. C. The arcsine is asinine: the analysis of proportions in ecology. Ecol. 92, 3–10 (2011).
    Article  Google Scholar 

    74.
    Su, Y. S., Yajima, M. R2jags: Using R to run ‘JAGS’. R package version 0.5–7, 34 (2015).

    75.
    Plummer, M. JAGS version 4.3. 0 user manual [Computer software manual]. Retrieved from sourceforge.net/projects/mcmc-jags/files/Manuals/4.x, 2 (2017).

    76.
    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7(4), 457–472 (1992).
    MATH  Article  Google Scholar  More