More stories

  • in

    Zinc isotopes from archaeological bones provide reliable tropic level information for marine mammals

    1.Horstmann‐Dehn, L., Follmann, E. H., Rosa, C., Zelensky, G. & George, C. Stable carbon and nitrogen isotope ratios in muscle and epidermis of arctic whales. Mar. Mamm. Sci. 28, E173–E190 (2012).Article 

    Google Scholar 
    2.Winder, M. & Schindler, D. E. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85, 2100–2106 (2004).Article 

    Google Scholar 
    3.Misarti, N., Finney, B. P., Maschner, H. & Wooller, M. J. Changes in northeast Pacific marine ecosystems over the last 4500 years: evidence from stable isotope analysis of bone collagen from archaeological middens. Holocene 19, 1139–1151 (2009).Article 

    Google Scholar 
    4.Szpak, P., Buckley, M., Darwent, C. M. & Richards, M. P. Long-term ecological changes in marine mammals driven by recent warming in northwestern Alaska. Glob. Chang. Biol. 24, 490–503 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Michener, R. H. & Kaufman, L. in Stable Isotopes in Ecology and Environmental Science (eds Michener, R. & Lajtha, K.), 238–282 (Oxford, 2007).6.Dunton, K. H., Saupe, S. M., Golikov, A. N., Schell, D. M. & Schonberg, S. V. Trophic relationships and isotopic gradients among arctic and subarctic marine fauna. Mar. Ecol. Prog. Ser. 56, 89–97 (1989).Article 

    Google Scholar 
    7.Ramsay, M. A. & Hobson, K. A. Polar bears make little use of terrestrial food webs: evidence from stable-carbon isotope analysis. Oecologia 86, 598–600 (1991).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    8.Hobson, K. A. & Welch, H. E. Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar. Ecol. Prog. Ser. 84, 9–18 (1992).Article 
    CAS 

    Google Scholar 
    9.Evershed, R. P. et al. in Stable Isotopes in Ecology and Environmental Science (eds Michener, R. & Lajtha, K.) 480–540 (Oxford, 2007).10.Jaouen, K. et al. Exceptionally high δ15N values in collagen single amino acids confirm Neandertals as high-trophic level carnivores. Proc. Natl Acad. Sci. USA 116, 4928–4933 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    11.Heuser, A., Tütken, T., Gussone, N. & Galer, S. J. Calcium isotopes in fossil bones and teeth − Diagenetic versus biogenic origin. Geochim. Cosmochim. Acta 75, 3419–3433 (2011).Article 
    CAS 

    Google Scholar 
    12.Martin, J. E., Vance, D. & Balter, V. Natural variation of magnesium isotopes in mammal bones and teeth from two South African trophic chains. Geochim. Cosmochim. Acta 130, 12–20 (2014).Article 
    CAS 

    Google Scholar 
    13.Jaouen, K., Beasley, M., Schoeninger, M., Hublin, J. J. & Richards, M. P. Zinc isotope ratios of bones and teeth as new dietary indicators: results from a modern food web (Koobi Fora, Kenya). Sci. Rep. 6, 26281 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    14.Martin, J. E., Tacail, T., Adnet, S., Girard, C. & Balter, V. Calcium isotopes reveal the trophic position of extant and fossil elasmobranchs. Chem. Geol. 415, 118–125 (2015).Article 
    CAS 

    Google Scholar 
    15.Jaouen, K., Szpak, P. & Richards, M. P. Zinc isotope ratios as indicators of diet and trophic level in arctic marine mammals. PLoS ONE 11, e0152299 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    16.Bourgon, N. et al. Zinc isotopes in Late Pleistocene fossil teeth from a Southeast Asian cave setting preserve paleodietary information. Proc. Natl Acad. Sci. USA 117, 4675–4681 (2020).PubMed 
    Article 
    CAS 

    Google Scholar 
    17.Jaouen, K. What is our toolbox of analytical chemistry for exploring ancient hominin diets in the absence of organic preservation? Quat. Sci. Rev. 197, 307–318 (2018).Article 

    Google Scholar 
    18.Minagawa, M. & Wada, E. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta 48, 1135–1140 (1984).Article 
    CAS 

    Google Scholar 
    19.Vander Zanden, M. J. & Rasmussen, J. B. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 46, 2061–2066 (2001).Article 

    Google Scholar 
    20.Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718 (2002).Article 

    Google Scholar 
    21.Moynier, F., Fujii, T., Shaw, A. S. & Le Borgne, M. Heterogeneous distribution of natural zinc isotopes in mice. Metallomics 5, 693–699 (2013).PubMed 
    Article 
    CAS 

    Google Scholar 
    22.Balter, V. et al. Contrasting Cu, Fe, and Zn isotopic patterns in organs and body fluids of mice and sheep, with emphasis on cellular fractionation. Metallomics 5, 1470–1482 (2013).PubMed 
    Article 
    CAS 

    Google Scholar 
    23.Mahan, B., Moynier, F., Jørgensen, A. L., Habekost, M. & Siebert, J. Examining the homeostatic distribution of metals and Zn isotopes in Göttingen minipigs. Metallomics 10, 1264–1281 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    24.Jaouen, K. et al. Dynamic homeostasis modeling of Zn isotope ratios in the human body. Metallomics 11, 1049–1059 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    25.Jaouen, K. et al. Zinc isotope variations in archeological human teeth (Lapa do Santo, Brazil) reveal dietary transitions in childhood and no contamination from gloves. PLoS ONE 15, e0232379 (2020).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    26.McMahon, K. W., Hamady, L. L. & Thorrold, S. R. Ocean ecogeochemistry: a review. Oceanogr. Mar. Biol. 51, 327–374 (2013).
    Google Scholar 
    27.Rau, G. H., Sweeney, R. E. & Kaplan, I. R. Plankton 13C:12C ratio changes with latitude: differences between northern and southern oceans. Deep Sea Res. Part I Oceanogr. Res. 29, 1035–1039 (1982).Article 
    CAS 

    Google Scholar 
    28.McMahon, K. W., Hamady, L. L. & Thorrold, S. R. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol. Oceanogr. 58, 697–714 (2013).Article 
    CAS 

    Google Scholar 
    29.Hedges, R. E., Clement, J. G., Thomas, C. D. L. & O’Connell, T. C. Collagen turnover in the adult femoral mid‐shaft: modeled from anthropogenic radiocarbon tracer measurements. Am. J. Phys. Anthropol. 133, 808–816 (2007).PubMed 
    Article 

    Google Scholar 
    30.Szpak, P., Savelle, J. M., Conolly, J. & Richards, M. P. Variation in late Holocene marine environments in the Canadian Arctic Archipelago: evidence from ringed seal bone collagen stable isotope compositions. Quat. Sci. Rev. 211, 136–155 (2019).Article 

    Google Scholar 
    31.Szpak, P. & Buckley, M. Sulfur isotopes (δ34S) in Arctic marine mammals: indicators of benthic vs. pelagic foraging? Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps13493 (2020).32.Reeves, R. R. in Ringed Seals in the North Atlantic (eds Heide-Jørgensen, M. P. & Lydersen, C.) 9–45 (NAMMCO Scientific Publications, 1998).33.Koehler, G., Kardynal, K. J. & Hobson, K. A. Geographical assignment of polar bears using multi-element isoscapes. Sci. Rep. 9, 9390 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Moody, J. F. & Hodgetts, L. M. Subsistence practices of pioneering Thule–Inuit: a faunal analysis of Tiktalik. Arct. Anthropol. 50, 4–24 (2013).Article 

    Google Scholar 
    35.Dyke, A. S. et al. An assessment of marine reservoir corrections for radiocarbon dates on walrus from the Foxe Basin region of Arctic Canada. Radiocarbon 61, 67–81 (2019).Article 
    CAS 

    Google Scholar 
    36.Derocher, A. E., Wiig, Ø. & Andersen, M. Diet composition of polar bears in Svalbard and the western Barents Sea. Polar Biol. 25, 448–452 (2002).Article 

    Google Scholar 
    37.Hobson, K. A. et al. A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep Sea Res. Part II Top. Stud. Oceanogr. 49, 5131–5150 (2002).Article 
    CAS 

    Google Scholar 
    38.Iverson, S. J., Stirling, I. & Lang, S. L. C. in Top Predators in Marine Ecosystems (eds Boyd, I. L., Wanless, S. & Camphuysen, C. J.) 98–117 (Cambridge University Press, 2006).39.Thiemann, G. W., Iverson, S. J. & Stirling, I. Polar bear diets and arctic marine food webs: insights from fatty acid analysis. Ecol. Monogr. 78, 591–613 (2008).Article 

    Google Scholar 
    40.Stein, R. & MacDonald, R. W. The Organic Carbon Cycle in the Arctic Ocean (Springer, 2004).41.Lynch‐Stieglitz, J., Stocker, T. F., Broecker, W. S. & Fairbanks, R. G. The influence of air‐sea exchange on the isotopic composition of oceanic carbon: Observations and modeling. Glob. Biogeochem. Cycles 9, 653–665 (1995).Article 

    Google Scholar 
    42.Hobson, K. A., Ambrose, W. G. Jr & Renaud, P. E. Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Mar. Ecol. Prog. Ser. 128, 1–10 (1995).Article 

    Google Scholar 
    43.France, R., Loret, J., Mathews, R. & Springer, J. Longitudinal variation in zooplankton δ13C through the Northwest Passage: inference for incorporation of sea-ice POM into pelagic foodwebs. Polar Biol. 20, 335–341 (1998).Article 

    Google Scholar 
    44.Søreide, J. E., Hop, H., Carroll, M. L., Falk-Petersen, S. & Hegseth, E. N. Seasonal food web structures and sympagic–pelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Prog. Oceanogr. 71, 59–87 (2006).Article 

    Google Scholar 
    45.Saupe, S. M., Schell, D. M. & Griffiths, W. B. Carbon-isotope ratio gradients in western arctic zooplankton. Mar. Biol. 103, 427–432 (1989).Article 
    CAS 

    Google Scholar 
    46.Schell, D. M., Barnett, B. A. & Vinette, K. A. Carbon and nitrogen isotope ratios in zooplankton of the Bering, Chukchi and Beaufort seas. Mar. Ecol. Prog. Ser. 162, 11–23 (1998).Article 
    CAS 

    Google Scholar 
    47.Tamelander, T., Kivimäe, C., Bellerby, R. G., 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).Article 
    CAS 

    Google Scholar 
    48.Pomerleau, C. et al. Spatial patterns in zooplankton communities across the eastern Canadian sub-Arctic and Arctic waters: insights from stable carbon (δ13C) and nitrogen (δ15N) isotope ratios. J. Plankton Res. 33, 1779–1792 (2011).Article 
    CAS 

    Google Scholar 
    49.Pomerleau, C. et al. Pan-Arctic concentrations of mercury and stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in marine zooplankton. Sci. Total Environ. 551, 92–100 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    50.De la Vega, C., Jeffreys, R. M., Tuerena, R., Ganeshram, R. & Mahaffey, C. Temporal and spatial trends in marine carbon isotopes in the Arctic Ocean and implications for food web studies. Glob. Chang. Biol. 25, 4116–4130 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Goni, M. A., Yunker, M. B., Macdonald, R. W. & Eglinton, T. I. Distribution and sources of organic biomarkers in arctic sediments from the Mackenzie River and Beaufort Shelf. Mar. Chem. 71, 23–51 (2000).Article 
    CAS 

    Google Scholar 
    52.Parsons, T. R. et al. Autotrophic and heterotrophic production in the Mackenzie River/Beaufort Sea estuary. Polar Biol. 9, 261–266 (1989).Article 

    Google Scholar 
    53.Dehn, L. A. et al. Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol. 30, 167–181 (2007).Article 

    Google Scholar 
    54.Butt, C. M., Mabury, S. A., Kwan, M., Wang, X. & Muir, D. C. Spatial trends of perfluoroalkyl compounds in ringed seals (Phoca hispida) from the Canadian Arctic. Environ. Toxicol. Chem. 27, 542–553 (2008).PubMed 
    Article 
    CAS 

    Google Scholar 
    55.Dittmar, T. & Kattner, G. The biogeochemistry of the river and shelf ecosystem of the Arctic Ocean: a review. Mar. Chem. 83, 103–120 (2003).Article 
    CAS 

    Google Scholar 
    56.Pons, M. L. et al. A Zn isotope perspective on the rise of continents. Geobiology 11, 201–214 (2013).PubMed 
    Article 
    CAS 

    Google Scholar 
    57.Isson, T. T. et al. Tracking the rise of eukaryotes to ecological dominance with zinc isotopes. Geobiology 16, 341–352 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    58.Samanta, M., Ellwood, M. J. & Strzepek, R. F. Zinc isotope fractionation by Emiliania huxleyi cultured across a range of free zinc ion concentrations. Limnol. Oceanogr. 63, 660–671 (2018).Article 
    CAS 

    Google Scholar 
    59.Köbberich, M. & Vance, D. Zn isotope fractionation during uptake into marine phytoplankton: implications for oceanic zinc isotopes. Chem. Geol. 523, 154–161 (2019).Article 
    CAS 

    Google Scholar 
    60.Maréchal, C. N., Nicolas, E., Douchet, C. & Albarède, F. Abundance of zinc isotopes as a marine biogeochemical tracer. Geochem. Geophys. Geosyst. 1, 1015 (2000).Article 

    Google Scholar 
    61.John, S. G. The Marine Biogeochemistry of Zinc Isotopes. [Doctoral Thesis]. (Massachusetts Institute of Technology, 2007).62.Conway, T. M. & John, S. G. The biogeochemical cycling of zinc and zinc isotopes in the North Atlantic Ocean. Glob. Biogeochem. Cycles 28, 1111–1128 (2014).Article 
    CAS 

    Google Scholar 
    63.Wyatt, N. J. et al. Biogeochemical cycling of dissolved zinc along the GEOTRACES South Atlantic transect GA10 at 40°S. Glob. Biogeochem. Cycles 28, 44–56 (2014).Article 
    CAS 

    Google Scholar 
    64.John, S. G. & Conway, T. M. A role for scavenging in the marine biogeochemical cycling of zinc and zinc isotopes. Earth Planet. Sci. Lett. 394, 159–167 (2014).Article 
    CAS 

    Google Scholar 
    65.Sieber, M. et al. Cycling of zinc and its isotopes across multiple zones of the Southern Ocean: insights from the Antarctic Circumnavigation Expedition. Geochim. Cosmochim. Acta 268, 310–324 (2020).Article 
    CAS 

    Google Scholar 
    66.Samanta, M., Ellwood, M. J., Sinoir, M. & Hassler, C. S. Dissolved zinc isotope cycling in the Tasman Sea, SW Pacific Ocean. Mar. Chem. 192, 1–12 (2017).Article 
    CAS 

    Google Scholar 
    67.Little, S. H., Vance, D., Walker-Brown, C. & Landing, W. M. The oceanic mass balance of copper and zinc isotopes, investigated by analysis of their inputs, and outputs to ferromanganese oxide sediments. Geochim. Cosmochim. Acta 125, 673–693 (2014).Article 
    CAS 

    Google Scholar 
    68.Zhao, Y., Vance, D., Abouchami, W. & De Baar, H. J. Biogeochemical cycling of zinc and its isotopes in the Southern Ocean. Geochim. Cosmochim. Acta 125, 653–672 (2014).Article 
    CAS 

    Google Scholar 
    69.Liao, W. H. et al. Zn isotope composition in the water column of the Northwestern Pacific Ocean: the importance of external sources. Glob. Biogeochem. Cycles 34, e2019GB006379 (2020).CAS 

    Google Scholar 
    70.Vance, D., de Souza, G. F., Zhao, Y., Cullen, J. T. & Lohan, M. C. The relationship between zinc, its isotopes, and the major nutrients in the North-East Pacific. Earth Planet. Sci. Lett. 525, 115748 (2019).Article 
    CAS 

    Google Scholar 
    71.Jensen, L. T. et al. Biogeochemical cycling of dissolved zinc in the Western Arctic (Arctic GEOTRACES GN01). Glob. Biogeochem. Cycles 33, 343–369 (2019).Article 
    CAS 

    Google Scholar 
    72.DeNiro, M. J. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317, 806–809 (1985).Article 
    CAS 

    Google Scholar 
    73.Ambrose, S. H. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 17, 431–451 (1990).Article 

    Google Scholar 
    74.Muir, D. C. G. et al. Can seal eating explain elevated levels of PCBs and organochlorine pesticides in walrus blubber from eastern Hudson Bay (Canada)? Environ. Pollut. 90, 335–348 (1995).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    75.Young, B. G. & Ferguson, S. H. Seasons of the ringed seal: pelagic open-water hyperphagy, benthic feeding over winter and spring fasting during molt. Wildl. Res. 40, 52–60 (2013).Article 
    CAS 

    Google Scholar 
    76.Matley, J. K., Fisk, A. T. & Dick, T. A. Foraging ecology of ringed seals (Pusa hispida), beluga whales (Delphinapterus leucas) and narwhals (Monodon monoceros) in the Canadian High Arctic determined by stomach content and stable isotope analysis. Polar Res. 34, 24295 (2015).Article 
    CAS 

    Google Scholar 
    77.Michel, C., Ingram, R. G. & Harris, L. R. Variability in oceanographic and ecological processes in the Canadian Arctic Archipelago. Prog. Oceanogr. 71, 379–401 (2006).Article 

    Google Scholar 
    78.Tremblay, J. É., Gratton, Y., Carmack, E. C., Payne, C. D. & Price, N. M. Impact of the large‐scale Arctic circulation and the North Water Polynya on nutrient inventories in Baffin Bay. J. Geophys. Res. 107, 3112 (2002).Article 

    Google Scholar 
    79.Ingram, R. G., Bâcle, J., Barber, D. G., Gratton, Y. & Melling, H. An overview of physical processes in the North Water. Deep Sea Res. Part II Top. Stud. Oceanogr. 49, 4893–4906 (2002).Article 

    Google Scholar 
    80.Pauly, D., Trites, A. W., Capuli, E. & Christensen, V. Diet composition and trophic levels of marine mammals. ICES J. Mar. Sci. 55, 467–481 (1998).Article 

    Google Scholar 
    81.Woollett, J. Oakes Bay 1: a preliminary reconstruction of a Labrador Inuit seal hunting economy in the context of climate change. Geogr. Tidsskr. 110, 245–259 (2010).Article 

    Google Scholar 
    82.Stirling, I. & Archibald, W. R. Aspects of predation of seals by polar bears. J. Fish. Res. Board Can. 34, 1126–1129 (1977).Article 

    Google Scholar 
    83.Pilfold, N. W., Derocher, A. E., Stirling, I. & Richardson, E. Polar bear predatory behaviour reveals seascape distribution of ringed seal lairs. Popul. Ecol. 56, 129–138 (2014).Article 

    Google Scholar 
    84.Elorriaga-Verplancken, F., Aurioles-Gamboa, D., Newsome, S. D. & Martínez-Díaz, S. F. δ15N and δ13C values in dental collagen as a proxy for age-and sex-related variation in foraging strategies of California sea lions. Mar. Biol. 160, 641–652 (2013).Article 
    CAS 

    Google Scholar 
    85.Hauser, D. D., Laidre, K. L., Suydam, R. S. & Richard, P. R. Population-specific home ranges and migration timing of Pacific Arctic beluga whales (Delphinapterus leucas). Polar Biol. 37, 1171–1183 (2014).Article 

    Google Scholar 
    86.Harwood, L. A., Smith, T. G., Auld, J., Melling, H. & Yurkowski, D. J. Seasonal movements and diving of ringed seals, Pusa hispida, in the Western Canadian Arctic, 1999–2001 and 2010–11. Arctic 68, 193–209 (2015).Article 

    Google Scholar 
    87.Ferguson, S. H., Taylor, M. K., Born, E. W., Rosing-Asvid, A. & Messier, F. Activity and movement patterns of polar bears inhabiting consolidated versus active pack ice. Arctic 54, 49–54. (2001).Article 

    Google Scholar 
    88.Lunn, N. J. et al. Polar bear management in Canada 1997–2000. In: Proc. 13th Working Meeting of the IUCN/SSC Polar Bear Specialist Group, 23–28 June 2001, Nuuk, Greenland. Occasional Paper 26 (eds Lunn, N. J., Schliebe, S. & Born, E. W.) 41–52 (IUCN, 2002).89.Ronald, K. & Dougan, J. L. The ice lover: biology of the harp seal (Phoca groenlandica). Science 215, 928–933 (1982).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    90.Sergeant, D. E. Harp seals, man and ice. Can. Spec. Publ. Fish. Aquat. Sci. 114, (1991).91.Ogloff, W. R., Yurkowski, D. J., Davoren, G. K. & Ferguson, S. H. Diet and isotopic niche overlap elucidate competition potential between seasonally sympatric phocids in the Canadian Arctic. Mar. Biol. 166, 103 (2019).Article 
    CAS 

    Google Scholar 
    92.Mansfield, A. W. Seals of arctic and eastern Canada. Fish. Res. Board Canada Bull. 137 (1963).93.Sergeant, D. E. Migrations of harp seals Pagophilus groenlandicus (Erxleben) in the Northwest Atlantic. J. Fish. Res. Board Can. 22, 433–464 (1965).Article 

    Google Scholar 
    94.Richard, P. R., Heide-Jørgensen, M. P., Orr, J. R., Dietz, R. & Smith, T. G. Summer and autumn movements and habitat use by belugas in the Canadian High Arctic and adjacent areas. Arctic 54, 207–222 (2001).
    Google Scholar 
    95.Maréchal, C. N., Télouk, P. & Albarède, F. Precise analysis of copper and zinc isotopic compositions by plasma-source mass spectrometry. Chem. Geol. 156, 251–273 (1999).Article 

    Google Scholar 
    96.Moynier, F., Albarède, F. & Herzog, G. F. Isotopic composition of zinc, copper, and iron in lunar samples. Geochim. Cosmochim. Acta 70, 6103–6117 (2006).Article 
    CAS 

    Google Scholar 
    97.Toutain, J. P. et al. Evidence for Zn isotopic fractionation at Merapi volcano. Chem. Geol. 253, 74–82 (2008).Article 
    CAS 

    Google Scholar 
    98.Copeland, S. R. et al. Strontium isotope ratios (87Sr/86Sr) of tooth enamel: a comparison of solution and laser ablation multicollector inductively coupled plasma mass spectrometry methods. Rapid Commun. Mass Spectrom. 22, 3187–3194 (2008).PubMed 
    Article 
    CAS 

    Google Scholar 
    99.Brown, T. A., Nelson, D. E., Vogel, J. S. & Southon, J. R. Improved collagen extraction by modified Longin method. Radiocarbon 30, 171–177 (1988).Article 
    CAS 

    Google Scholar 
    100.Qi, H., Coplen, T. B., Geilmann, H., Brand, W. A. & Böhlke, J. K. Two new organic reference materials for δ13C and δ15N measurements and a new value for the δ13C of NBS 22 oil. Rapid Commun. Mass Spectrom. 17, 2483–2487 (2003).PubMed 
    Article 
    CAS 

    Google Scholar 
    101.Szpak, P., Metcalfe, J. Z. & Macdonald, R. A. Best practices for calibrating and reporting stable isotope measurements in archaeology. J. Archaeol. Sci. Rep. 13, 609–616 (2017).
    Google Scholar 
    102.R Core Team, R version 3.6.1 (R Foundation for Statistical Computing, Vienna, Austria, 2018).103.Haug, T. et al. Trophic level and fatty acids in harp seals compared with common minke whales in the Barents Sea. Mar. Biol. Res. 13, 919–932 (2017).Article 

    Google Scholar  More

  • in

    Some biological properties of spiny eel (Mastacembelus mastacembelus, Banks & Solander, 1794) living in the Upper Euphrates River Basin, Turkey

    1.Eschmeyer, W. N. & Fong, J. D. Species of fish by family/subfamily. https://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp#Mastacembelidae [Accessed 10 February 2021] (2021).2.Johnson, G. D. & Patterson, C. Percomorph phylogeny: A survey of Acanthomorphs and a new proposal. Bull. Mar. Sci. 52, 554–626 (1993).
    Google Scholar 
    3.Britz, R. & Kottelat, M. Descriptive osteology of the family Chaudhuriidae (Teleostei, Synbranchiformes, Mastacembeloidei), with a discussion of its relationships. Am. Mus. Novit. 3418, 1–62 (2003).Article 

    Google Scholar 
    4.Brown, K. J., Britz, R., Bills, R., Rüber, L. & Day, J. J. Pectoral fin loss in the Mastacembelidae: A new species from Lake Tanganyika. J. Zool. 284, 286–293 (2011).Article 

    Google Scholar 
    5.Kara, C., Güneş, H., Gürlek, M. E. & Alp, A. Adıyaman bölgesi akarsularında dikenli yılan balığı (Mastacembelus mastacembelus Banks & Solander 1794)’nın dağılımı ve bazı morfometrik özellikleri. AquaSt. 3, 3–11 (2014) (in Turkish).
    Google Scholar 
    6.Dağlı, M. & Erdemli, A. Ü. An investigation on the fish fauna of Balıksuyu Stream (Kilis, Turkey). Int. J. Nat. Eng. Sci. 3, 19–24 (2009).
    Google Scholar 
    7.Geldiay, R. & Balık, S. Türkiye Tatlısu Balıkları. VI. Baskı, Ege Üniversitesi Su Ürünleri Yayınları, (Ege Üniversitesi Basımevi, Bornova-Izmir, 2009) (in Turkish).8.Vreven, E. J. & Teugels, G. G. Redescription of Mastacembelus liberiensis Baulenger, 1898 and description of a new West African spiny-eel (Synbranchiformes: Mastacembelidae) from the Konkoure River basin, Guinea. J. Fish Biol. 67, 332–369 (2005).Article 

    Google Scholar 
    9.Jalali, B., Barzegar, M. & Nezamabadi, H. Parasitic fauna of the spiny eel, Mastacembelus mastacembelus Banks et Solander (Teleostei: Mastacembelidae) in Iran. Iran. J. Vet. Res. 9, 158–161 (2008).
    Google Scholar 
    10.Çakmak, E. Dikenli yılan balığı (Mastacembelus mastacembelus)’nın morfolojik ve moleküler özelliklerinin belirlenmesi. Kahramanmaraş Sütçü İmam Üniversitesi, Fen Bilimleri Enstitüsü, Master Thesis, (Kahramanmaraş, 2008) (in Turkish).11.Çakmak, E. & Alp, A. Morphological differences among the Mesopotamian spiny eel, Mastacembelus mastacembelus (Banks & Solander 1794), populations. Turk. J. Fish. Aquat. Sci. 10, 7–92 (2010).Article 

    Google Scholar 
    12.Şahinöz, E., Doğu, Z. & Aral, F. Development of embryos in Mastacembelus mastacembelus (Bank & Solender, 1794) (Mesopotamian spiny eel) (Mastacembelidae). Aquac. Res. 37, 1611–1616 (2006).Article 

    Google Scholar 
    13.Pala, G., Tellioğlu, A., Eroğlu, M. & Şen, D. The digestive system content of Mastacembelus mastacembelus (Banks & Solander, 1794) inhabiting in Karakaya Dam Lake (Malatya-Turkey). Turk. J. Fish. Aquat. Sci. 10, 229–233 (2010).Article 

    Google Scholar 
    14.Eroğlu, M. & Şen, D. Otolith size-total length relationship in spiny eel, Mastacembelus mastacembelus (Banks & Solander, 1794) inhabiting in Karakaya Dam Lake (Malatya, Turkey). J. FisheriesSciences.com 3, 342–351 (2009).
    Google Scholar 
    15.Eroğlu, M. & Şen, D. Relationships between fish age and otolith size in spiny eel: Mastacembelus mastacembelus (Banks & Solander, 1794). Bitlis Eren Univ. J. Sci. Technol. 2, 15–18 (2012).Article 

    Google Scholar 
    16.Eroğlu, M. & Şen, D. Reproduction biology of Mastacembelus simack (Walbaum, 1792) inhabiting Karakaya Dam Lake (Malatya, Turkey). Int. J. Nat. Eng. Sci. 1, 69–73 (2007).
    Google Scholar 
    17.Oymak, S. A., Kırankaya, ŞG. & Doğan, N. Growth and reproduction of Mesopotamian spiny eel (Mastacembelus mastacembelus Banks and Solander, 1794) in Ataturk Dam Lake (Şanlıurfa), Turkey. J. Appl. Ichthyol. 25, 488–490 (2009).Article 

    Google Scholar 
    18.Gümüş, A., Şahinöz, E., Doğu, Z. & Polat, N. Age and growth of the Mesopotamian spiny eel, Mastacembelus mastacembelus (Banks & Solender, 1794), from southeastern Anatolia. Turk. Zool. Derg. 34, 399–407 (2010).
    Google Scholar 
    19.Anonymous. Keban Baraj Gölü limnoloji raporu. DSİ 9. Bölge Müdürlüğü, Su Ürünleri Başmühendisliği. (Keban-Elazığ, 1994) (in Turkish).20.Yüksel, F., Demirol, F. & Gündüz, F. Leslie population estimation for Turkish crayfish (Astacus leptodactylus Esch., 1823) in the Keban Dam Lake, Turkey. Turk. J. Fish. Aquat. Sci. 13, 835–839 (2013).Article 

    Google Scholar 
    21.Google Maps. https://www.google.com/maps/@38.8025012,38.9170508,9z [Accessed 10 February 2021] (2021).22.Lagler, K. F., Bardach, J. E., Miller, R. R. & Passino, D. R. M. Ichthyology (Wiley, 1977).23.Zar, J. H. Biostatistical Analysis 4th edn. (Prentice-Hall, 1999).24.Pauly, D. Some Simple Methods for the Assessment of Tropical Fish Stocks (FAO, 1984).25.Sparre, P. & Venema, S. C. Introduction to Tropical Fish Stock Assessment. FAO Fisheries Technical Paper, 306/1, Rev. 2, (Rome, 1998).26.Munro, J. L. & Pauly, D. A simple method for comparing the growth of fishes and invertebrates. FishByte 1, 5–6 (1983).
    Google Scholar 
    27.Gayanilo, F. C., Sparre, P. & Pauly, D. FAO-ICLARM Stock Assessment Tools II (FiSAT II). User’s Guide. FAO Computerized Information Series (Fisheries). No. 8, Revised version, (FAO, Rome, 2005).28.Kılıç, H. M. Sultansuyu Deresi, Beyler Deresi ve Karakaya Barajı’nda yaşayan dikenli yılanbalığı (Mastacembelus simack)’nın biyoloik özelliklerinin incelenmesi. Osmangazi Universitesi, Fen Bilimleri Enstitüsü, Master Thesis, (Eskişehir, 2002) (in Turkish).29.Pazira, A., Abdoli, A., Kouhgardi, E. & Yousefifard, P. Age structure and growth of the Mesopotamian spiny eel, Mastacembelus mastacembelus (Banks & Solander in Russell, 1974) (Mastacembelidae), in southern Iran. Zool. Middle East 35, 43–47 (2005).Article 

    Google Scholar 
    30.Korkut, A. Y., Kop, A., Demirtaş, N. & Cihaner, A. Balık beslemede gelişim performansının izlenme yöntemleri. EgeJFAS 24, 201–205 (2007) (in Turkish).
    Google Scholar  More

  • in

    Nitrogen fixation and denitrification activity differ between coral- and algae-dominated Red Sea reefs

    1.Galloway, J. N. et al. The nitrogen cascade. Bioscience 53, 341–356 (2003).
    Google Scholar 
    2.Mackenzie, F. T. Our Changing Planet: An Introduction to Earth System Science and Global Environmental Change (1998). https://downloads.globalchange.gov/ocp/ocp1998/ocp1998.pdf3.Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: How can it occur?. Biogeochemistry 13, 87–115 (1991).
    Google Scholar 
    4.Webb, K. L., DuPaul, W. D., Wiebe, W., Sottile, W. & Johannes, R. E. Enewetak (Eniwetok) Atoll: aspects of the nitrogen cycle on a coral reef. Limnol. Oceanogr. 20, 198–210 (1975).ADS 
    CAS 

    Google Scholar 
    5.Lesser, M. P. et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346, 143–152 (2007).ADS 
    CAS 

    Google Scholar 
    6.Hoegh-Guldberg, O. Environmental and economic importance of the world’s coral reefs. Mar. Freshw. Res. 50, 839–866 (1999).
    Google Scholar 
    7.Bell, P. R. F. Eutrophication and coral reefs-some examples in the Great Barrier Reef lagoon. Water Res. 26, 553–568 (1992).CAS 

    Google Scholar 
    8.Sorokin, Y. I. Microbiological Aspects of the Productivity of Coral Reefs. In Biology and Geology of Coral Reefs (eds. Jones, O. A. & Endean, R.) 17–46 (Academic press, Inc., 1973).9.O’Neil, J. M. & Capone, D. G. Nitrogen Cycling in Coral Reef Environments. In Nitrogen in the Marine Environment 949–989 (2008). https://doi.org/10.1016/B978-0-12-372522-6.00021-910.Cardini, U. et al. Budget of primary production and dinitrogen fixation in a highly seasonal red sea coral reef. Ecosystems 19, 771–785 (2016).
    Google Scholar 
    11.Scheffers, S. R., Nieuwland, G., Bak, R. P. M. & Van Duyl, F. C. Removal of bacteria and nutrient dynamics within the coral reef framework of Curaçao (Netherlands Antilles). Coral Reefs 23, 413–422 (2004).
    Google Scholar 
    12.Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: the key to understanding holobiont functioning?. Trends Microbiol. 23, 490–497 (2015).PubMed 

    Google Scholar 
    13.Koop, K. et al. ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull. 42, 91–120 (2001).CAS 
    PubMed 

    Google Scholar 
    14.Capone, D. G., Dunham, S. E., Horrigan, S. G. & Duguay, L. E. Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar. Ecol. Prog. Ser. 80, 75–88 (1992).ADS 
    CAS 

    Google Scholar 
    15.Hoffmann, F. et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11, 2228–2243 (2009).CAS 
    PubMed 

    Google Scholar 
    16.Wiebe, W. J., Johannes, R. E. & Webb, K. L. Nitrogen fixation in a coral reef community. Science 188, 257–259 (1975).ADS 
    CAS 
    PubMed 

    Google Scholar 
    17.Larkum, A. W. D., Kennedy, I. R. & Muller, W. J. Nitrogen fixation on a coral reef. Mar. Biol. 98, 143–155 (1988).
    Google Scholar 
    18.Kimes, N. E., Van Nostrand, J. D., Weil, E., Zhou, J. & Morris, P. J. Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies. Environ. Microbiol. 12, 541–556 (2010).CAS 
    PubMed 

    Google Scholar 
    19.Yang, S., Sun, W., Zhang, F. & Li, Z. Phylogenetically diverse denitrifying and ammonia-oxidizing bacteria in corals Alcyonium gracillimum and Tubastraea coccinea. Mar. Biotechnol. 15, 540–551 (2013).CAS 

    Google Scholar 
    20.Tilstra, A. et al. Denitrification aligns with N2 fixation in red sea corals. Sci. Rep. 9, 19460 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.El-Khaled, Y. et al. In situ eutrophication stimulates dinitrogen fixation, denitrification, and productivity in Red Sea coral reefs. Mar. Ecol. Prog. Ser. 645, 55–66 (2020).ADS 
    CAS 

    Google Scholar 
    22.O’Neil, J. M. & Capone, D. G. Nitrogen cycling in coral reef environments. Nitrog. Mar. Environ. https://doi.org/10.1016/B978-0-12-372522-6.00021-9 (2008).Article 

    Google Scholar 
    23.Muscatine, L. & Porter, J. W. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460 (1977).
    Google Scholar 
    24.Wafar, M., Wafar, S. & David, J. J. Nitrification in reef corals. Limnol. Oceanogr. 35, 725–730 (1990).ADS 
    CAS 

    Google Scholar 
    25.Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science (80-) 333, 418–422 (2011).ADS 
    CAS 

    Google Scholar 
    26.Hughes, T. P. et al. Coral reefs in the anthropocene. Nature 546, 82–90 (2017).ADS 
    CAS 
    PubMed 

    Google Scholar 
    27.Fabricius, K. E. Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. In Coral Reefs: An Ecosystem in Transition (eds. Dubinsky, Z. & Stambler, N.) 493–505 (2011). https://doi.org/10.1007/978-94-007-0114-4_28.28.Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).ADS 
    CAS 
    PubMed 

    Google Scholar 
    29.Lapointe, B. E., Brewton, R. A., Herren, L. W., Porter, J. W. & Hu, C. Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study. Marine Biology 166, (Springer, 2019).30.Hughes, T. P. et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17, 360–365 (2007).CAS 
    PubMed 

    Google Scholar 
    31.Williams, I. D., Polunin, N. V. C. & Hendrick, V. J. Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Mar. Ecol. Prog. Ser. 222, 187–196 (2001).ADS 

    Google Scholar 
    32.Mumby, P. J., Hastings, A. & Edwards, H. J. Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–101 (2007).ADS 
    CAS 
    PubMed 

    Google Scholar 
    33.Roth, F. et al. High rates of carbon and dinitrogen fixation suggest a critical role of benthic pioneer communities in the energy and nutrient dynamics of coral reefs. Funct. Ecol. https://doi.org/10.1111/1365-2435.13625 (2020).Article 
    PubMed 

    Google Scholar 
    34.Done, T. J. Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247, 121–132 (1992).
    Google Scholar 
    35.Hughes, T. P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science (80-) 265, 1547–1551 (1994).ADS 
    CAS 

    Google Scholar 
    36.McManus, J. W. & Polsenberg, J. F. Coral-algal phase shifts on coral reefs: ecological and environmental aspects. Prog. Oceanogr. 60, 263–279 (2004).ADS 

    Google Scholar 
    37.Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).
    Google Scholar 
    38.White, A. T., Vogt, H. P. & Arin, T. Philippine coral reefs under threat: the economic losses caused by reef destruction. Mar. Pollut. Bull. 40, 598–605 (2000).CAS 

    Google Scholar 
    39.McClanahan, T. R., Hicks, C. C. & Darling, E. S. Malthusian overfishing and efforts to overcome it on Kenyan coral reefs. Ecol. Appl. 18, 1516–1529 (2008).PubMed 

    Google Scholar 
    40.Nyström, M. et al. Confronting feedbacks of degraded marine ecosystems. Ecosystems 15, 695–710 (2012).
    Google Scholar 
    41.Woodhead, A. J., Hicks, C. C., Norström, A. V., Williams, G. J. & Graham, N. A. J. Coral reef ecosystem services in the Anthropocene. Funct. Ecol. 33, 1023–1034 (2019).
    Google Scholar 
    42.McClanahan, T., Polunin, N. & Done, T. Ecological states and the resilience of coral reefs. Conserv. Ecol. 6 (2), 18, (2002).
    43.Munday, P. L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Chang. Biol. 10, 1642–1647 (2004).ADS 

    Google Scholar 
    44.Williams, G. J. & Graham, N. A. J. Rethinking coral reef functional futures. Funct. Ecol. 33, 942–947 (2019).
    Google Scholar 
    45.Norström, A. V., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 293–306 (2009).ADS 

    Google Scholar 
    46.Brandl, S. J. et al. Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Front. Ecol. Environ. 17, 445–454 (2019).
    Google Scholar 
    47.Roth, F. et al. High summer temperatures amplify functional differences between coral- and algae-dominated reef communities. Ecology https://doi.org/10.1002/ecy.3226 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    48.Bednarz, V. N., Cardini, U., Van Hoytema, N., Al-Rshaidat, M. M. D. & Wild, C. Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea. Mar. Ecol. Prog. Ser. 519, 141–152 (2015).ADS 

    Google Scholar 
    49.Rix, L. et al. Seasonality in dinitrogen fixation and primary productivity by coral reef framework substrates from the northern Red Sea. Mar. Ecol. Prog. Ser. 533, 79–92 (2015).ADS 
    CAS 

    Google Scholar 
    50.den Haan, J. et al. Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef. Coral Reefs 33, 1003–1015 (2014).ADS 

    Google Scholar 
    51.Roth, F. et al. Coral reef degradation affects the potential for reef recovery after disturbance. Mar. Environ. Res. 142, 48–58 (2018).CAS 
    PubMed 

    Google Scholar 
    52.Holmes, G. & Johnstone, R. W. The role of coral mortality in nitrogen dynamics on coral reefs. J. Exp. Mar. Biol. Ecol. 387, 1–8 (2010).CAS 

    Google Scholar 
    53.Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science (80-) 318, 1737–1742 (2007).ADS 
    CAS 

    Google Scholar 
    54.Van Hooidonk, R. et al. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci. Rep. 6, 1–8 (2016).
    Google Scholar 
    55.Osborne, K. et al. Delayed coral recovery in a warming ocean. Glob. Chang. Biol. 23, 3869–3881 (2017).ADS 
    PubMed 

    Google Scholar 
    56.Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).ADS 
    CAS 
    PubMed 

    Google Scholar 
    57.Pogoreutz, C. et al. Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching. Glob. Chang. Biol. 23, 3838–3848 (2017).ADS 
    PubMed 

    Google Scholar 
    58.Bednarz, V. N. et al. Dinitrogen fixation and primary productivity by carbonate and silicate reef sand communities of the Northern Red Sea. Mar. Ecol. Prog. Ser. 527, 47–57 (2015).ADS 

    Google Scholar 
    59.Shashar, N., Feldstein, T., Cohen, Y. & Loya, Y. Nitrogen fixation (acetylene reduction) on a coral reef. Coral Reefs 13, 171–174 (1994).ADS 

    Google Scholar 
    60.Patriquin, D. G. & McClung, C. R. Nitrogen accretion, and the nature and possible significance of N2 fixation (acetylene reduction) in a Nova Scotian Spartina alterniflora Stand. Mar. Biol. 47, 227–242 (1978).
    Google Scholar 
    61.Shieh, W. Y. & Lin, Y. M. Nitrogen fixation (acetylene reduction) associated with the zoanthid Palythoa tuberculosa Esper. J. Exp. Mar. Biol. Ecol. 163, 31–41 (1992).CAS 

    Google Scholar 
    62.Bednarz, V. N. et al. Contrasting seasonal responses in dinitrogen fixation between shallow and deep-water colonies of the model coral Stylophora pistillata in the northern Red Sea. PLoS ONE 13, 1–13 (2018).
    Google Scholar 
    63.Schöttner, S. et al. Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environ. Microbiol. 13, 1815–1826 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    64.Zumft, W. G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533–616 (1997).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    65.Compaoré, J. & Stal, L. J. Effect of temperature on the sensitivity of nitrogenase to oxygen in two heterocystous cyanobacteria. J. Physcol. 46, 1172–1179 (2010).
    Google Scholar 
    66.Littler, M. & Littler, D. The nature of turf and boring algae and their interactions on reefs. Smithson. Contrib. to Mar. Sci. 213–217 (2013).67.Rosenberg, G. & Ramus, J. Uptake of inorganic nitrogen and seaweed surface area: volume ratios. Aquat. Bot. 19, 65–72 (1984).CAS 

    Google Scholar 
    68.Fong, P., Rudnicki, R. & Zedler, J. B. Algal community response to nitrogen and phosphorus loading in experimental mesocosms: Management recommendations for southern California lagoons. (1987).69.Fong, C. R., Gaynus, C. J. & Carpenter, R. C. Complex interactions among stressors evolve over time to drive shifts from short turfs to macroalgae on tropical reefs. Ecosphere 11(5), e03130 (2020).70.Roth, F., Stuhldreier, I., Sánchez-Noguera, C., Morales-Ramírez, T. & Wild, C. Effects of simulated overfishing on the succession of benthic algae and invertebrates in an upwelling-influenced coral reef of Pacific Costa Rica. J. Exp. Mar. Bio. Ecol. 468, 55–66 (2015).
    Google Scholar 
    71.Stuhldreier, I., Bastian, P., Schönig, E. & Wild, C. Effects of simulated eutrophication and overfishing on algae and invertebrate settlement in a coral reef of Koh Phangan, Gulf of Thailand. Mar. Pollut. Bull. 92, 35–44 (2015).CAS 
    PubMed 

    Google Scholar 
    72.Yamamuro, M., Kayanne, H. & Minagawa, M. Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol. Oceanogr. 40, 617–621 (1995).ADS 
    CAS 

    Google Scholar 
    73.Tilstra, A. et al. Seasonality affects dinitrogen fixation associated with two common macroalgae from a coral reef in the northern Red Sea. Mar. Ecol. Prog. Ser. 575, 69–80 (2017).ADS 
    CAS 

    Google Scholar 
    74.El-Khaled, Y. C. et al. Simultaneous measurements of dinitrogen fixation and denitrification associated with coral reef substrates: advantages and limitations of a combined acetylene assay. Front. Mar. Sci. 7, 411 (2020).
    Google Scholar 
    75.Davey, M., Holmes, G. & Johnstone, R. High rates of nitrogen fixation (acetylene reduction) on coral skeletons following bleaching mortality. Coral Reefs 27, 227–236 (2008).ADS 

    Google Scholar 
    76.Larkum, A. W. D. High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci. Mar. Biol. 97, 503–506 (1988).CAS 

    Google Scholar 
    77.Pogoreutz, C. et al. Nitrogen fixation aligns with nifH abundance and expression in two coral trophic functional groups. Front. Microbiol. 8, 1–7 (2017).
    Google Scholar 
    78.Arrigo, K. K. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2004).ADS 

    Google Scholar 
    79.Mills, M. M., Ridame, C., Davey, M., La Roche, J. & Geider, R. J. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004).ADS 
    CAS 
    PubMed 

    Google Scholar 
    80.Redfield, A. C. The biological control of chemical factors in the environment. Am. Sci. 46, 205–221 (1958).CAS 

    Google Scholar 
    81.Porter, J. W., Muscatine, L., Dubinsky, Z. & Falkowski, P. G. Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, stylophora pistillata. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 222, 161–180 (1984).ADS 

    Google Scholar 
    82.Veal, C. J., Holmes, G., Nunez, M., Hoegh-Guldberg, O. & Osborn, J. A comparative study of methods for surface area and three dimensional shape measurement of coral skeletons. Limnol. Oceanogr. Methods 8, 241–253 (2010).
    Google Scholar 
    83.Falkowski, P. P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. Population control in symbiotic corals. Bioscience 43, 606–611 (1993).
    Google Scholar 
    84.Eyre, B. D., Glud, R. N. & Patten, N. Mass coral spawning: a natural large-scale nutrient addition experiment. Limnol. Oceanogr. 53, 997–1013 (2008).ADS 
    CAS 

    Google Scholar 
    85.Tilstra et al. Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability, Royal Society Open Science, https://doi.org/10.1098/rsos.201835 (2021).86.D’Angelo, C. & Wiedenmann, J. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sustain. 7, 82–93 (2014).
    Google Scholar 
    87.Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Chang. 3, 160–164 (2013).ADS 
    CAS 

    Google Scholar 
    88.Ferrier-Pagès, C., Godinot, C., D’Angelo, C., Wiedenmann, J. & Grover, R. Phosphorus metabolism of reef organisms with algal symbionts. Ecol. Monogr. 86, 262–277 (2016).
    Google Scholar 
    89.Muscatine, L., Falkowski, P. G., Porter, J. W. & Dubinsky, Z. Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. B Biol. Sci. 222, 181–202 (1984).ADS 
    CAS 

    Google Scholar 
    90.Conti-Jerpe, I. E. et al. Trophic strategy and bleaching resistance in reef-building corals. Sci. Adv. 6(15), eaaz5443 (2020).91.Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17 (2009).PubMed 

    Google Scholar 
    92.Muscatine, L., Porter, J. W. & Kaplan, I. R. Resource partitioning by reef corals as determined from stable isotope composition. Pac. Sci. 48, 304–312 (1994).
    Google Scholar 
    93.Her, J.-J. & Huang, J.-S. Influences of carbon source and C/N ratio on nitrate/nitrite denitrification and carbon breakthrough. Bioresour. Technol. 54, 45–51 (1995).CAS 

    Google Scholar 
    94.Chen, S. et al. Organic carbon availability limiting microbial denitrification in the deep vadose zone. Environ. Microbiol. 20, 980–992 (2018).CAS 
    PubMed 

    Google Scholar 
    95.Schlichter, D., Svoboda, A. & Kremer, B. P. Functional autotrophy of Heteroxenia fuscescens (Anthozoa: Alcyonaria): carbon assimilation and translocation of photosynthates from symbionts to host. Mar. Biol. 78, 29–38 (1983).CAS 

    Google Scholar 
    96.Babbin, A. R. et al. Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical stony corals. ISME J. https://doi.org/10.1038/s41396-020-00845-2 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    97.Pupier, C. A. et al. Divergent capacity of scleractinian and soft corals to assimilate and transfer diazotrophically derived nitrogen to the reef environment. Front. Microbiol. 10, 1860 (2019).98.Muscatine, L. The role of symbiotic algae in carbon and energy flux in coral reefs. In Coral Reefs (ed. Dubinsky, Z.) 75–87 (1990).99.van Woesik, R., Irikawa, A., Anzai, R. & Nakamura, T. Effects of coral colony morphologies on mass transfer and susceptibility to thermal stress. Coral Reefs 31, 633–639 (2012).ADS 

    Google Scholar 
    100.Patterson, M. R. & Sebens, K. P. Forced convection modulates gas exchange in cnidarians. Proc. Natl. Acad. Sci. U. S. A. 86, 8833–8836 (1989).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    101.Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373 (1994).
    Google Scholar 
    102.Graham, N. A. J. & Nash, K. L. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326 (2013).ADS 

    Google Scholar 
    103.Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003).ADS 
    CAS 
    PubMed 

    Google Scholar 
    104.Graham, N. A. J. et al. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl. Acad. Sci. U. S. A. 103, 8425–8429 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    105.Sano, M., Shimizu, M. & Nose, Y. Long-term effects of destruction of hermatypic corals by Acanthaster plana infestation on reef fish communities at Iriomote Island, Japan. Mar. Ecol. Prog. Ser. 37, 191–199 (1987).ADS 

    Google Scholar 
    106.Lindahl, U., Öhman, M. C. & Schelten, C. K. The 1997/1998 mass mortality of corals: effects on fish communities on a Tanzanian coral reef. Mar. Pollut. Bull. 42, 127–131 (2001).CAS 
    PubMed 

    Google Scholar 
    107.Jones, G. P., McCormick, M. I., Srinivasan, M. & Eagle, J. V. Coral decline threatens fish biodiversity in marine reserves. Proc. Natl. Acad. Sci. U. S. A. 101, 8251–8253 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    108.Idjadi, J. A. & Edmunds, P. J. Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar. Ecol. Prog. Ser. 319, 117–127 (2006).ADS 

    Google Scholar 
    109.Bracewell, S. A., Clark, G. F. & Johnston, E. L. Habitat complexity effects on diversity and abundance differ with latitude: an experimental study over 20 degrees. Ecology 99, 1964–1974 (2018).PubMed 

    Google Scholar 
    110.Cinner, J. E. et al. Linking social and ecological systems to sustain coral reef fisheries. Curr. Biol. 19, 206–212 (2009).CAS 
    PubMed 

    Google Scholar 
    111.Sheppard, C., Dixon, D. J., Gourlay, M., Sheppard, A. & Payet, R. Coral mortality increases wave energy reaching shores protected by reef flats: examples from the Seychelles. Estuar. Coast. Shelf Sci. 64, 223–234 (2005).ADS 

    Google Scholar 
    112.Karcher, D. B. et al. Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea. PeerJ 8, e8737 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    113.Adey, W. H. & Goertemiller, T. Coral reef algal turfs: master producers in nutrient poor seas. Phycologia 26, 374–386 (1987).
    Google Scholar 
    114.Fong, P. & Paul, V. J. Coral reef algae. In Coral Reefs: An Ecosystem in Transition (eds. Dubinsky, Z. & Stambler, N.) 241–272 (Springer, 2011). https://doi.org/10.1007/978-94-007-0114-4_17.115.Hoey, A. S. & Bellwood, D. R. Suppression of herbivory by macroalgal density: a critical feedback on coral reefs?. Ecol. Lett. 14, 267–273 (2011).PubMed 

    Google Scholar 
    116.Jessen, C. & Wild, C. Herbivory effects on benthic algal composition and growth on a coral reef flat in the Egyptian Red Sea. Mar. Ecol. Prog. Ser. 476, 9–21 (2013).ADS 
    CAS 

    Google Scholar 
    117.Haas, A. F. & Wild, C. Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat. Biol. 10, 131–138 (2010).
    Google Scholar 
    118.Roth et al. Nutrient pollution enhances productivity and framework dissolution in algae- but not in coral-dominated reef communities. Marine Pollution Bulletin. 168, 112444 (2021).119.Haas, A. F. et al. Influence of coral and algal exudates on microbially mediated reef metabolism. PeerJ 2013, 1–28 (2013).
    Google Scholar 
    120.Roach, T. N. F. et al. A multiomic analysis of in situ coral-turf algal interactions. Proc. Natl. Acad. Sci. U. S. A. 117, 13588–13595 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    121.van Oppen, M. J. H. & Blackall, L. L. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17, 557–567 (2019).PubMed 

    Google Scholar 
    122.Liang, J. et al. Distinct bacterial communities associated with massive and branching scleractinian corals and potential linkages to coral susceptibility to thermal or cold stress. Front. Microbiol. 8, 1–10 (2017).ADS 

    Google Scholar 
    123.Fung, T., Seymour, R. M. & Johnson, C. R. Alternative stable states and phase shifts in coral reefs under anthropogenic stress. Ecology 92, 967–982 (2011).PubMed 

    Google Scholar 
    124.Bruno, J. F., Sweatman, H., Precht, W. F., Selig, E. R. & Schutte, V. G. W. Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90, 1478–1484 (2009).PubMed 

    Google Scholar 
    125.Tilot, V., Leujak, W., Ormond, R. F. G., Ashworth, J. A. & Mabrouk, A. Monitoring of South Sinai coral reefs: influence of natural and anthropogenic factors. Aquat. Conserv. Mar. Freshw. Ecosyst. https://doi.org/10.1002/aqc.942 (2008).Article 

    Google Scholar 
    126.Riegl, B. & Piller, W. E. Coral frameworks revisited-reefs and coral carpets in the northern Red Sea. Coral Reefs 18, 241–253 (1999).
    Google Scholar 
    127.Benayahu, Y., Jeng, M. S., Perkol-Finkel, S. & Dai, C. F. Soft corals (Octocorallia: Alcyonacea) from Southern Taiwan. II. Species diversity and distributional patterns. Zool. Stud. 43, 548–560 (2004).
    Google Scholar 
    128.Ninio, R., Meekan, M., Done, T. & Sweatman, H. Temporal patterns in coral assemblages on the Great Barrier Reef from local to large spatial scales. Mar. Ecol. Prog. Ser. 194, 65–74 (2000).ADS 

    Google Scholar 
    129.Fox, H. E., Pet, J. S., Dahuri, R. & Caldwell, R. L. Recovery in rubble fields: long-term impacts of blast fishing. Mar. Pollut. Bull. 46, 1024–1031 (2003).CAS 
    PubMed 

    Google Scholar 
    130.Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Chang. 3, 683–687 (2013).ADS 
    CAS 

    Google Scholar 
    131.Rasser, M. W. & Riegl, B. Holocene coral reef rubble and its binding agents. Coral Reefs 21, 57–72 (2002).ADS 

    Google Scholar 
    132.Dalsgaard, T., Thamdrup, B. & Canfield, D. E. Anaerobic ammonium oxidation (anammox) in the marine environment. Res. Microbiol. 156, 457–464 (2005).CAS 
    PubMed 

    Google Scholar 
    133.Brunner, B. et al. Nitrogen isotope effects induced by anammox bacteria. Proc. Natl. Acad. Sci. 110, 18994–18999 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    134.Zhang, Y. et al. The functional gene composition and metabolic potential of coral-associated microbial communities. Sci. Rep. 5, 1–11 (2015).
    Google Scholar 
    135.Richter, C., Wunsch, M., Rasheed, M., Kötter, I. & Badran, M. I. Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413, 726–730 (2001).ADS 
    CAS 
    PubMed 

    Google Scholar 
    136.Hill, J. & Wilkinson, C. Methods for ecological monitoring of coral reefs. Aust. Inst. Mar. Sci. Townsv. https://doi.org/10.1017/CBO9781107415324.004 (2004).Article 

    Google Scholar 
    137.Kohler, K. E. & Gill, S. M. Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 32, 1259–1269 (2006).ADS 

    Google Scholar 
    138.Haas, A., El-Zibdah, M. & Wild, C. Seasonal monitoring of coral-algae interactions in fringing reefs of the Gulf of Aqaba, Northern Red Sea. Coral Reefs 29, 93–103 (2010).ADS 

    Google Scholar 
    139.Bahartan, K. et al. Macroalgae in the coral reefs of Eilat (Gulf of Aqaba, Red Sea) as a possible indicator of reef degradation. Mar. Pollut. Bull. 60, 759–764 (2010).CAS 
    PubMed 

    Google Scholar 
    140.Voolstra, C. R. et al. Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Glob. Chang. Biol. 26, 4328–4343 (2020).ADS 
    PubMed 

    Google Scholar 
    141.Hynes, R. K. & Knowles, R. Inhibition by acetylene of ammonia oxidation in Nitrosomonas europaea. FEMS Microbiol. Lett. 4, 319–321 (1978).CAS 

    Google Scholar 
    142.Oremland, R. S. & Capone, D. G. Use of ‘specific’ inhibitors in biogeochemistry and microbial ecology. Adv. Microb. Ecol. https://doi.org/10.1007/978-1-4684-5409-3_8 (1988).Article 

    Google Scholar 
    143.Haines, J. R., Atlas, R. M., Griffiths, R. P. & Morita, R. Y. Denitrification and nitrogen fixation in Alaskan continental shelf sediments. Appl. Environ. Microbiol. 41, 412–421 (1981).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    144.Joye, S. B. & Paerl, H. W. Contemporaneous nitrogen fixation and denitrification in intertidal microbial mats: rapid response to runoff events. Mar. Ecol. Prog. Ser. 94, 267–274 (1993).ADS 
    CAS 

    Google Scholar 
    145.Miyajima, T., Suzumura, M., Umezawa, Y. & Koike, I. Microbiological nitrogen transformation in carbonate sediments of a coral-reef lagoon and associated seagrass beds. Mar. Ecol. Prog. Ser. 217, 273–286 (2001).ADS 

    Google Scholar 
    146.Falkowski, P. G. Enzymology of Nitrogen Assimilation Nitrogen in the Marine Environment (Academic Press, 1983). https://doi.org/10.1016/b978-0-12-160280-2.50031-6.147.den Haan, J. et al. Nitrogen and phosphorus uptake rates of different species from a coral reef community after a nutrient pulse. Sci. Rep. 6, 28821 (2016).ADS 

    Google Scholar 
    148.Grover, R., Maguer, J. F., Allemand, D. & Ferrier-Pagès, C. Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol. Oceanogr. 48, 2266–2274 (2003).ADS 
    CAS 

    Google Scholar 
    149.Knapp, A. N. The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Front. Microbiol. 3, 374 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    150.Dilworth, M. J. Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochim. Biophys. Acta 127, 285–294 (1966).CAS 
    PubMed 

    Google Scholar 
    151.Schöllhorn, R. & Burris, R. H. Acetylene as a competitive inhibitor of N-2 fixation. Proc. Natl. Acad. Sci. U. S. A. 58, 213–216 (1967).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    152.Balderston, W. L., Sherr, B. & Payne, W. J. Blockage by acetylene of nitrous-oxide reduction in pseudomonas-perfectomarinus. Appl. Environ. Microbiol. 31, 504–508 (1976).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    153.Yoshinari, T. & Knowles, R. Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem. Biophys. Res. Commun. 69, 705–710 (1976).CAS 
    PubMed 

    Google Scholar 
    154.Lavy, A. et al. A quick, easy and non-intrusive method for underwater volume and surface area evaluation of benthic organisms by 3D computer modelling. Methods Ecol. Evol. 6, 521–531 (2015).
    Google Scholar 
    155.Gutierrez-Heredia, L., Benzoni, F., Murphy, E. & Reynaud, E. G. End to end digitisation and analysis of three-dimensional coral models, from communities to corallites. PLoS ONE 11, e0149641 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    156.Hughes, D. J. et al. Coral reef survival under accelerating ocean deoxygenation. Nat. Clim. Chang. 10, 296–307 (2020).ADS 
    CAS 

    Google Scholar 
    157.Mulholland, M. R., Bronk, D. A. & Capone, D. G. Dinitrogen fixation and release of ammonium and dissolved organic nitrogen by Trichodesmium IMS101. Aquat. Microb. Ecol. 37, 85–94 (2004).
    Google Scholar 
    158.Clarke, K. R. & Gorley, R. N. PRIMER v6: Use manual/Tutorial. PRIMER-E:Plymouth (2006).
    159.Anderson, M., Gorley, R. & Clarke, K. PERMANOVA+ for PRIMER. Guide to software and statistical methods. (2008).160.R Core Team. R: A language and environment for statistical computing. (2017).161.RStudio Team. RStudio: Integrated Development for R. (2020).162.Wilson, S. T., Böttjer, D., Church, M. J. & Karl, D. M. Comparative assessment of nitrogen fixation methodologies, conducted in the oligotrophic north pacific ocean. Appl. Environ. Microbiol. 78, 6516–6523 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    163.Yu, K., Seo, D. C. & Delaune, R. D. Incomplete acetylene inhibition of nitrous oxide reduction in potential denitrification assay as revealed by using 15N-Nitrate tracer. Commun. Soil Sci. Plant Anal. 41, 2201–2210 (2010).CAS 

    Google Scholar 
    164.Groffman, P. M. et al. Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol. Appl. 16, 2091–2122 (2006).PubMed 

    Google Scholar 
    165.Maldonado, M., Ribes, M. & van Duyl, F. C. Nutrient Fluxes Through Sponges. Biology, Budgets, and Ecological Implications. Advances in Marine Biology Vol. 62 (Elsevier Ltd., 2012).
    Google Scholar 
    166.Roth, F. et al. An in situ approach for measuring biogeochemical fluxes in structurally complex benthic communities. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13151 (2019).Article 

    Google Scholar  More

  • in

    Novel thermal habitat in lakes

    1.Kraemer, B. M. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-021-01060-3 (2021).Article 

    Google Scholar 
    2.Woolway, R. I. et al. Nat. Rev. Earth Environ. 1, 388–403 (2020).Article 

    Google Scholar 
    3.Woolway, R. I. et al. Nature 589, 402–407 (2021).CAS 
    Article 

    Google Scholar 
    4.Sharma, S. et al. Nat. Clim. Change 9, 227–231 (2019).Article 

    Google Scholar 
    5.Maberly, S. C. et al. Nat. Commun. 11, 1232 (2020).CAS 
    Article 

    Google Scholar 
    6.Winslow, L. A., Read, J. S., Hansen, G. J. A., Rose, K. C. & Robertson, D. M. Limnol. Oceanogr. 62, 2168–2178 (2017).Article 

    Google Scholar 
    7.O’Reilly, C. M. et al. Geophys. Res. Lett. 42, 10773–10781 (2015).
    Google Scholar 
    8.Rose, K. C., Winslow, L. A., Read, J. S. & Hansen, G. J. A. Limnol. Oceanogr. Lett. 1, 44–53 (2016).Article 

    Google Scholar 
    9.Winslow, L. A., Read, J. S., Hansen, G. J. A. & Hanson, P. C. Geophys. Res. Lett. 42, 355–361 (2015).Article 

    Google Scholar 
    10.Bartosiewicz, M. et al. Limnol. Oceanogr. Lett. 4, 132–144 (2019).CAS 
    Article 

    Google Scholar 
    11.Reid, A. J. et al. Biol. Rev. 94, 849–873 (2019).Article 

    Google Scholar 
    12.Woolway, R. I. & Maberly, S. C. Nat. Clim. Change 10, 1124–1129 (2020).Article 

    Google Scholar 
    13.Winder, M. & Schindler, D. E. Glob. Change Biol. 10, 1844–1856 (2004).Article 

    Google Scholar 
    14.Burrows, M. T. et al. Nat. Clim. Change 9, 959–963 (2019).Article 

    Google Scholar 
    15.Jacobson, P. C., Stefan, H. G. & Pereira, D. L. Can. J. Fish. Aquat. Sci. 67, 2002–2013 (2010).CAS 
    Article 

    Google Scholar 
    16.Thackeray, S. J. et al. Glob. Change Biol. 16, 3304–3313 (2010).Article 

    Google Scholar 
    17.Addo-Bediako, A., Chown, S. L. & Gaston, K. J. P. R. Soc. B 267, 739–745 (2000).CAS 
    Article 

    Google Scholar 
    18.Vadeboncoeur, Y., McIntyre, P. B. & Vander Zanden, M. J. BioScience 61, 526–537 (2011).Article 

    Google Scholar 
    19.Thompson, L. M. et al. Fisheries 46, 8–21 (2021).Article 

    Google Scholar  More

  • in

    Spatial ecology of cane toads (Rhinella marina) in their native range: a radiotelemetric study from French Guiana

    1.Crystal-Ornelas, R. & Lockwood, J. L. Cumulative meta-analysis identifies declining but negative impacts of invasive species on richness after 20 yr. Ecology 101, e03082. https://doi.org/10.1002/ecy.3082 (2020).Article 
    PubMed 

    Google Scholar 
    2.Emery-Butcher, H. E., Beatty, S. J. & Robson, B. J. The impacts of invasive ecosystem engineers in freshwaters: A review. Freshw. Biol. 65, 999–1015. https://doi.org/10.1111/fwb.13479 (2020).Article 

    Google Scholar 
    3.Simberloff, D. Maintenance management and eradication of established aquatic invaders. Hydrobiologia 848, 2399–2420. https://doi.org/10.1007/s10750-020-04352-5 (2021).Article 

    Google Scholar 
    4.Weidlich, E. W. A., Flórido, F. G., Sorrini, T. B. & Brancalion, P. H. S. Controlling invasive plant species in ecological restoration: A global review. J. Appl. Ecol. 57, 1806–1817. https://doi.org/10.1111/1365-2664.13656 (2020).Article 

    Google Scholar 
    5.Simberloff, D. Invasive species in Conservation biology for all (eds Sodhi, N. S. & Ehrlich, P. R.) 131–152 (Oxford University Press, 2010).6.Hoddle, M. S. Restoring balance: Using exotic species to control invasive exotic species. Conserv. Biol. 18, 38–49 (2004).Article 

    Google Scholar 
    7.Turvey, N. D. Cane toads: a tale of sugar, politics and flawed science. (Sydney University Press, 2013).8.Shine, R. Cane toad wars. (University of California Press, 2018).9.Seebacher, F. & Alford, R. A. Movement and microhabitat use of a terrestrial amphibian (Bufo marinus) on a tropical island: Seasonal variation and environmental correlates. J. Herpetol. 33, 208–214. https://doi.org/10.2307/1565716 (1999).Article 

    Google Scholar 
    10.Brown, G. P., Phillips, B. L., Webb, J. K. & Shine, R. Toad on the road: Use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biol. Conserv. 133, 88–94. https://doi.org/10.1016/j.biocon.2006.05.020 (2006).Article 

    Google Scholar 
    11.Brown, G. P., Shilton, C., Phillips, B. L. & Shine, R. Invasion, stress, and spinal arthritis in cane toads. Proc. Natl. Acad. Sci. 104, 17698–17700. https://doi.org/10.1073/pnas.0705057104 (2007).ADS 
    Article 
    PubMed 

    Google Scholar 
    12.Brown, G. P., Kelehear, C. & Shine, R. Effects of seasonal aridity on the ecology and behaviour of invasive cane toads in the Australian wet–dry tropics. Funct. Ecol. 25, 1339–1347. https://doi.org/10.1111/j.1365-2435.2011.01888.x (2011).Article 

    Google Scholar 
    13.Brown, G. P., Phillips, B. L. & Shine, R. The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front. Proc. R. Soc. B Biol. Sci. 281, 20141385. https://doi.org/10.1098/rspb.2014.1385 (2014).Article 

    Google Scholar 
    14.Brown, G., Kelehear, C., Pizzatto, L. & Shine, R. The impact of lungworm parasites on rates of dispersal of their anuran host, the invasive cane toad. Biol. Invasions 18, 103–114 https://doi.org/10.1007/s10530-015-0993-1 (2015).Article 

    Google Scholar 
    15.Phillips, B. L., Brown, G. P. & Shine, R. Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. J. Evol. Biol. 23, 2595–2601. https://doi.org/10.1111/j.1420-9101.2010.02118.x (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    16.Phillips, B. L., Brown, G. P., Travis, J. M. J. & Shine, ,. R. Reid’s paradox revisited: The evolution of dispersal kernels during range expansion. Am. Nat. 172, S34–S48. https://doi.org/10.1086/588255 (2008).Article 
    PubMed 

    Google Scholar 
    17.Phillips, B. L., Brown, G. P., Webb, J. K. & Shine, R. Invasion and the evolution of speed in toads. Nature 439, 803. https://doi.org/10.1038/439803a (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Alford, R. A., Brown, G. P., Schwarzkopf, L., Phillips, B. L. & Shine, R. Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species. Wildl. Res. 36, 23–28 (2009).Article 

    Google Scholar 
    19.Tingley, R. & Shine, R. Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the Australian semi-desert. PLoS ONE 6, e25979. https://doi.org/10.1371/journal.pone.0025979 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Pizzatto, L., Both, C., Brown, G. & Shine, R. The accelerating invasion: dispersal rates of cane toads at an invasion front compared to an already-colonized location. Evol. Ecol. 31, 533–545. https://doi.org/10.1007/s10682-017-9896-1 (2017).Article 

    Google Scholar 
    21.Lindström, T., Brown, G. P., Sisson, S. A., Phillips, B. L. & Shine, R. Rapid shifts in dispersal behavior on an expanding range edge. Proc. Natl. Acad. Sci. 110, 13452. https://doi.org/10.1073/pnas.1303157110 (2013).ADS 
    Article 
    PubMed 

    Google Scholar 
    22.Pettit, L. J., Greenlees, M. J. & Shine, R. Is the enhanced dispersal rate seen at invasion fronts a behaviourally plastic response to encountering novel ecological conditions? Biol. Lett. 12, 20160539. https://doi.org/10.1098/rsbl.2016.0539 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Pettit, L., Greenlees, M. & Shine, R. The impact of transportation and translocation on dispersal behaviour in the invasive cane toad. Oecologia 184, 411–422. https://doi.org/10.1007/s00442-017-3871-y (2017).ADS 
    Article 
    PubMed 

    Google Scholar 
    24.Pettit, L. J., Greenlees, M. J. & Shine, R. The behavioural consequences of translocation: how do invasive cane toads (Rhinella marina) respond to transport and release to novel environments? Behav. Ecol. Sociobiol. 71, 15. https://doi.org/10.1007/s00265-016-2245-5 (2016).Article 

    Google Scholar 
    25.Finnerty, P. B., Shine, R. & Brown, G. P. The costs of parasite infection: Effects of removing lungworms on performance, growth and survival of free-ranging cane toads. Funct. Ecol. 32, 402–415. https://doi.org/10.1111/1365-2435.12992 (2018).Article 

    Google Scholar 
    26.Blennerhassett, R. A., Bell-Anderson, K., Shine, R. & Brown, G. P. The cost of chemical defence: the impact of toxin depletion on growth and behaviour of cane toads (Rhinella marina). Proc. R. Soc. B Biol. Sci. 286, 20190867. https://doi.org/10.1098/rspb.2019.0867 (2019).CAS 
    Article 

    Google Scholar 
    27.Ward-Fear, G., Greenlees, M. J. & Shine, R. Toads on lava: Spatial ecology and habitat use of invasive cane toads (Rhinella marina) in Hawai’i. PLoS ONE 11, e0151700. https://doi.org/10.1371/journal.pone.0151700 (2016).CAS 
    Article 

    Google Scholar 
    28.Slade, R. W. & Moritz, C. Phylogeography of Bufo marinus from its natural and introduced ranges. Proc. R. Lond. Ser. B Biol. Sci. 265, 769–777. https://doi.org/10.1098/rspb.1998.0359 (1998).CAS 
    Article 

    Google Scholar 
    29.Acevedo, A. A., Lampo, M. & Cipriani, R. The cane or marine toad, Rhinella marina (Anura, Bufonidae): two genetically and morphologically distinct species. Zootaxa 4103, 574–586. https://doi.org/10.11646/zootaxa.4103.6.7 (2016).Article 

    Google Scholar 
    30.Freeland, W. J. & Kerin, S. H. Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl. Res. 18, 431–443 (1991).Article 

    Google Scholar 
    31.Seebacher, F. & Alford, R. A. Shelter microhabitats determine body temperature and dehydration rates of a terrestrial amphibian (Bufo marinus). J. Herpetol. 36, 69–75. https://doi.org/10.2307/1565804 (2002).Article 

    Google Scholar 
    32.Schwarzkopf, L. & Alford, R. A. Desiccation and shelter-site use in a tropical amphibian: Comparing toads with physical models. Funct. Ecol. 10, 193–200. https://doi.org/10.2307/2389843 (1996).Article 

    Google Scholar 
    33.Heise-Pavlov, S. R. & Longway, L. J. Diet and dietary selectivity of Cane Toads (Rhinella marina) in restoration sites: a case study in Far North Queensland, Australia. Ecol. Manag. Restor. 12, 230–233. https://doi.org/10.1111/j.1442-8903.2011.00603.x (2011).Article 

    Google Scholar 
    34.Jørgensen, C. B. 200 years of amphibian water economy: From Robert Townson to the present. Biol. Rev. 72, 153–237. https://doi.org/10.1017/S0006323196004963 (1997).Article 
    PubMed 

    Google Scholar 
    35.Kosmala, G. K., Brown, G. P., Shine, R. & Christian, K. Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion. Ecol. Evol. 10, 13071–13079. https://doi.org/10.1002/ece3.6895 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Hopkins, G. R. & Brodie, E. D. Occurrence of amphibians in saline habitats: A review and evolutionary perspective. Herpetol. Monogr. 29, 1–27 (2015).Article 

    Google Scholar 
    37.Yasumiba, K., Alford, R. A. & Schwarzkopf, L. Seasonal reproductive cycles of cane toads and their implications for control. Herpetologica 72, 288–292. https://doi.org/10.1655/Herpetologica-D-15-00048.1 (2016).Article 

    Google Scholar 
    38.Brodie, S., Yasumiba, K., Towsey, M., Roe, P. & Schwarzkopf, L. Acoustic monitoring reveals year-round calling by invasive toads in tropical Australia. Bioacoustics 30, 125–141. https://doi.org/10.1080/09524622.2019.1705183 (2020).Article 

    Google Scholar 
    39.Evans, M., Yáber, C. & Hero, J.-M. Factors influencing choice of breeding site by Bufo marinus in its natural habitat. Copeia 1996, 904–912. https://doi.org/10.2307/1447653 (1996).Article 

    Google Scholar 
    40.DeVore, J. L., Shine, R. & Ducatez, S. Urbanization and translocation disrupt the relationship between host density and parasite abundance. J. Anim. Ecol. 89, 1122–1133. https://doi.org/10.1111/1365-2656.13175 (2020).Article 
    PubMed 

    Google Scholar 
    41.Météo-France. Données publiques. https://donneespubliques.meteofrance.fr/ (2021).42.Kelehear, C. & Shine, R. Non-reproductive male cane toads (Rhinella marina) withhold sex-identifying information from their rivals. Biol. Lett. 15, 20190462. https://doi.org/10.1098/rsbl.2019.0462 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Higginson, A. D. & Ruxton, G. D. Foraging mode switching: the importance of prey distribution and foraging currency. Anim. Behav. 105, 121–137. https://doi.org/10.1016/j.anbehav.2015.04.014 (2015).Article 

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

    Google Scholar 
    45.Schwarzkopf, L. & Alford, R. A. Nomadic movement in tropical toads. Oikos 96, 492–506. https://doi.org/10.1034/j.1600-0706.2002.960311.x (2002).Article 

    Google Scholar 
    46.R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2020).47.Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Team, R. C. nlme: Linear and nonlinear mixed effects models. R package version 3.1-140 (2019).48.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    49.Fox, J. & Weisberg, S. An R Companion to Applied Regression. Third edn, (Sage, 2019).50.Lenth, R. Emmeans: Estimated marginal means, aka least-squares means. R package version 1.3.2 (2019).51.Pettit, L., Ducatez, S., DeVore, J. L., Ward-Fear, G. & Shine, R. Diurnal activity in cane toads (Rhinella marina) is geographically widespread. Sci. Rep. 10, 5723. https://doi.org/10.1038/s41598-020-62402-3 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Doody, J. S., McHenry, C. R., Rhind, D. & Clulow, S. Novel habitat causes a shift to diurnal activity in a nocturnal species. Sci. Rep. 9, 230. https://doi.org/10.1038/s41598-018-36384-2 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Webb, J. K., Letnic, M., Jessop, T. S. & Dempster, T. Behavioural flexibility allows an invasive vertebrate to survive in a semi-arid environment. Biol. Lett. 10, 20131014. https://doi.org/10.1098/rsbl.2013.1014 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.González-Bernal, E., Brown, G. P., Crowther, M. S. & Shine, R. Sex and age differences in habitat use by invasive cane toads (Rhinella marina) and a native anuran (Cyclorana australis) in the Australian wet–dry tropics. Austral Ecol. 40, 953–961. https://doi.org/10.1111/aec.12279 (2015).Article 

    Google Scholar 
    55.Lettoof, D. C. et al. Cane toads beneath bird rookeries: utilization of a natural disturbance by an invasive species. Curr. Zool. 64, 433–439. https://doi.org/10.1093/cz/zox041 (2018).Article 
    PubMed 

    Google Scholar 
    56.Biesinger, Z., Bolker, B. M. & Lindberg, W. J. Predicting local population distributions around a central shelter based on a predation risk-growth trade-off. Ecol. Model. 222, 1448–1455. https://doi.org/10.1016/j.ecolmodel.2011.02.009 (2011).Article 

    Google Scholar 
    57.Wright, T. F., Eberhard, J. R., Hobson, E. A., Avery, M. L. & Russello, M. A. Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol. Ecol. Evol. 22, 393–404. https://doi.org/10.1080/03949370.2010.505580 (2010).Article 

    Google Scholar 
    58.Lima, S. L. & Dill, L. M. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619–640. https://doi.org/10.1139/z90-092 (1990).Article 

    Google Scholar 
    59.Godin, J.-G.J. & Smith, S. A. A fitness cost of foraging in the guppy. Nature 333, 69–71. https://doi.org/10.1038/333069a0 (1988).ADS 
    Article 

    Google Scholar 
    60.Heithaus, M. R. et al. State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J. Anim. Ecol. 76, 837–844. https://doi.org/10.1111/j.1365-2656.2007.01260.x (2007).Article 
    PubMed 

    Google Scholar 
    61.Brown, G. P., Kelehear, C. & Shine, R. The early toad gets the worm: cane toads at an invasion front benefit from higher prey availability. J. Anim. Ecol. 82, 854–862. https://doi.org/10.1111/1365-2656.12048 (2013).Article 
    PubMed 

    Google Scholar 
    62.Lampo, M. & Bayliss, P. Density estimates of cane toads from native populations based on mark-recapture data. Wildl. Res. 23, 305–315. https://doi.org/10.1071/wr9960305 (1996).Article 

    Google Scholar 
    63.Urban, M. C., Phillips, B. L., Skelly, D. K. & Shine, R. A toad more traveled: The heterogeneous invasion dynamics of cane toads in Australia. Am. Nat. 171, E134–E148. https://doi.org/10.1086/527494 (2008).Article 
    PubMed 

    Google Scholar 
    64.Ducatez, S., Tingley, R. & Shine, R. Using species co-occurrence patterns to quantify relative habitat breadth in terrestrial vertebrates. Ecosphere 5, art152, https://doi.org/10.1890/ES14-00332.1 (2014).65.Baldwin, J. M. A new factor in evolution. Am. Nat. 30, 441–451 (1896).Article 

    Google Scholar 
    66.Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P. & Lefebvre, L. Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl. Acad. Sci. USA 102, 5460–5465. https://doi.org/10.1073/pnas.0408145102 (2005).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    67.Letnic, M., Webb, J. K., Jessop, T. S., Florance, D. & Dempster, T. Artificial water points facilitate the spread of an invasive vertebrate in arid Australia. J. Appl. Ecol. 51, 795–803. https://doi.org/10.1111/1365-2664.12232 (2014).Article 

    Google Scholar 
    68.Urban, M. C., Phillips, B. L., Skelly, D. K. & Shine, R. The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc. R. Soc. B Biol. Sci. 274, 1413–1419. https://doi.org/10.1098/rspb.2007.0114 (2007).Article 

    Google Scholar 
    69.Zug, G. R. & Zug, P. B. The marine toad, Bufo marinus: A natural history resumé of native populations. Smithsonian Contrib. Zool. 284, 1–58, https://doi.org/10.5479/si.00810282.284 (1979).Article 

    Google Scholar 
    70.Kosmala, G., Christian, K., Brown, G. & Shine, R. Locomotor performance of cane toads differs between native-range and invasive populations. R. Soc. Open Sci. 4, 170517. https://doi.org/10.1098/rsos.170517 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.Gruber, J., Brown, G., Whiting, M. J. & Shine, R. Geographic divergence in dispersal-related behaviour in cane toads from range-front versus range-core populations in Australia. Behav. Ecol. Sociobiol. 71, 38. https://doi.org/10.1007/s00265-017-2266-8 (2017).Article 

    Google Scholar  More

  • in

    Ancient DNA, lipid biomarkers and palaeoecological evidence reveals construction and life on early medieval lake settlements

    1.Menotti, F. & O’Sullivan, A. The Oxford Handbook of Wetland Archaeology. (Oxford University Press, 2013)2.O’Sullivan, A. The Archaeology of Lake Settlement in Ireland. (Discovery Programme, 1998)3.Crone, A. Forging a chronological framework for Scottish crannogs; the radiocarbon and dendrochronological evidence. In Lake Dwellings After Robert Munro. Proceedings from the Munro International Seminar: The Lake Dwellings of Europe (Midgley, M.S., Sanders, J. eds.) (University of Edinburgh, 2012).4.Lane, A., M. & Redknap, M. Llangorse Crannog: Excavation of an Early Medieval Royal Site in the Kingdom of Brycheiniog. (Oxbow Books, 2019).5.Hertz, J. The excavation of Solvig a Danish crannog in southern Denmark. Further excavation at Solvig. Chateau Gaillard 6, 84–105 (1974).
    Google Scholar 
    6.Barber, J. & Crone, B. A. Crannogs: A diminishing resource? A survey of the crannogs of south-west Scotland and excavations at Buiston crannog. Antiquity 67, 520–533 (1993).Article 

    Google Scholar 
    7.Henderson, J. & Cavers, G. Proc. Soc. An Iron age crannog in south-west Scotland: Underwater survey and excavation at Lough Arthur. Antiq. Scot. 141, 103–124 (2011).8.Garrow, D. & Sturt, F. Neolithic crannogs: Rethinking settlement, monumentality and deposition in the Outer Hebrides and beyond. Antiquity 93, 664–684 (2019).Article 

    Google Scholar 
    9.O’Brien, C.E., Selby, K.A., Ruiz, Z., Brown, A.G., Dinnin, M Caseldine, C., Langdon, P.G. & Stuijts, I. Sediment-based multi-proxy approach to the archaeology of crannogs: A case study from Central Ireland. Holocene 15, 707–719 (2005).10.O’Sullivan, A. Crannogs Lake Dwellings of Early Ireland. (Country House, 2000).11.Wood-Martin, W. G. The Lake Dwellings of Ireland (Figgis and Co., 1886).
    Google Scholar 
    12.Fredengren, C. Crannogs: A study of people’s interaction with lakes, with particular reference to Lough Gara in the north-west of Ireland (Wordwell Press, 2002).
    Google Scholar 
    13.Stratigos, M. J. & Noble, G. Crannogs, castles and lordly residences: New research and dating of crannogs in north-east Scotland. Proc. Soc. Antiq. Scot. 144, 205–222 (2014).
    Google Scholar 
    14.Tóth, M., Hardenbroek, M. van., Bleicher, N. & Heiri, O. Pronounced early human impact on lakeshore environments documented by aquatic invertebrate remains in waterlogged Neolithic settlement deposits. Q. Sci. Rev. 205, 126–142. https://doi.org/10.1016/j.quascirev.2018.12.015 (2019).15.Chen, W. & Ficetola, G. F. Conditionally autoregressive models improve occupancy analyses of autocorrelated data: An example with environmental DNA. Mol. Ecol. Resour. 19, 163–175 (2019).Article 

    Google Scholar 
    16.Prost, K., Birk, J.J,. Lehndorff, E., Gerlach, R. & Amelung, W. Steroid biomarkers revisited—Improved source identification of faecal remains in archaeological soil material. PLoS ONE 12(1), 1/30 (2017).17.Selby, K. A. & Brown, A. G. The holocene development, spatial variations and anthropogenic record of a shallow lake system in central Ireland as recorded by diatom stratigraphy. J. Palaeolimnol. 38, 419–440 (2007).ADS 
    Article 

    Google Scholar 
    18.Hawksworth, D. L., Van Geel, B. & Wiltshire, E. J. The enigma of the Diporotheca palynomorph. Rev. Palaeobot. Palynol. 235, 94–98 (2016).Article 

    Google Scholar 
    19.Alsos, I. G. et al. Plant DNA metabarcoding of lake sediments: How does it represent the contemporary vegetation. PLoS ONE 13(4), e0195403. https://doi.org/10.1371/journal.pone.0195403 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Giguet-Covex, C., Pansu, J., Arnaud, F., Rey, P-J., Griggo, C., Gielly, L. Domaizon, I., Coissac, E. David, F., Choler P., Poulenard, J. & Taberlet, P. Long livestock farming history and human landscape shaping revealed by lake sediment DNA.Nat. Commun. 5, 1–7 (2014).21.Sabatier, P. et al. Long-term relationships among pesticide applications, mobility, and soil erosion in a vineyard watershed. Proc. Natl. Acad. Sci. U.S.A. 111, 15647–15652 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    22.Crone, A. Crannogs and chronologies. Procs. Antiq. Soc. Scotland 123, 245–254. http://journals.socantscot.org/index.php/psas/article/view/9462 (1993).23.Lammers, Y., Clark, C., Erséus, C., Brown, A.G., Edwards, M. E., Gielly, L., Haflidason, H., Mangerud, J., Rota, E., Svendsen, J-I., & Alsos, I.G. Earthworms in late glacial and holocene records discovered in DNA bycatch. Boreas 48, 317–329 (2018).24.McClatchie, M., Mccormick, F. M., Kerr, T. R. & O’Sullivan, A. Early medieval farming and food production: A review of the archaeobotanical evidence from archaeological excavations in Ireland. Veg. Hist. Archaeobotany 24, 179–186 (2015).Article 

    Google Scholar 
    25.McCormick, F., & Murray, E. Knowth and the Zooarchaeology of Early Christian Ireland, Excavations at Knowth 3. (Royal Irish Academy Monographs in Archaeology, 2007).26.Soderberg, J. Wild cattle: Red deer in the religious texts, iconography, and archaeology of early Medieval Ireland. Int. J. Hist. Arch. 8, 167–183 (2004).Article 

    Google Scholar 
    27.Rymer, L. The history and ethnobotany of bracken. J. Linn. Soc. 76, 151–176 (1976).Article 

    Google Scholar 
    28.Stuart, J. Notice of a group of artificial islands in the Lough of Dowalton, Wigtownshire and other artificial islands or crannogs throughout Scotland. Procs. Soc. Antiq. Scot. 10, 31–34 (1866).
    Google Scholar 
    29.Dixon, N. The history of crannog survey and excavation in Scotland. Int. J. Nautical Arch. 20, 1–8 (1991).Article 

    Google Scholar 
    30.Jones, D. & Haggar, R. J. Impact of nitrogen and organic manures on yield, botanical composition and herbage quality of two contrasting grassland field margins. Biol. Agric. Hortic. 14, 107–123 (1997).Article 

    Google Scholar 
    31.O’Sullivan, A. The Social and Idealogical Role of Crannogs in Early Medieval Ireland. PhD Thesis. (UCD, 2004).32.Bourke, C. The Excavations of an Early Medieval Crannog at Newtownlow, County Westmeath (December Publications, 2015).
    Google Scholar 
    33.Jones, M. Feast: Why Humans Share Food. (Oxford University Press).34.Bronk Ramsey, C. Deposition models for chronological records. Q. Sci. Rev. 27, 42–60 (2008).ADS 
    Article 

    Google Scholar 
    35.Reimer, P. J. et al. The IntCal20 Northern hemisphere radiocarbon age calibratin curve. Radiocarbon 1, 1–33 (2020).
    Google Scholar 
    36.Kotov S, Pälike H. QAnalySeries—A cross-platform time series tuning and analysis tool. In AGU Fall Meeting. https://doi.org/10.1002/essoar.10500226.1 (2018)37.Croudace, I. W., Rindby, A. & Rothwell, R. G. ITRAX: Description and evaluation of a new multi-function X-ray core scanner. Geol. Soc. Lond. Spec. Public. 267, 51–63 (2006).ADS 
    CAS 
    Article 

    Google Scholar 
    38.Pirrie, D. & Rollinson. G. K. Unlocking the application of automated mineralogy. Geol. Today 27, 226–235 (2011).39.Pirrie, D., Rollinson, G. K., Andersen, J. C., Wootton, D. & Moorhead, S. Soil forensics as a tool to test reported artefact find sites. J. Archaeol. Sci. 41, 461–473 (2014).CAS 
    Article 

    Google Scholar 
    40.Taberlet, P., Coissac, E., Pompanon, F., Gielly, L., Miquel, C., Valentini, A., Vermat, T., Gérard, C., Brochmann, C. & Willerslev E. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucl. Acids Res. e14 (2007).41.Boyer, F., Mercier, C., Bonin, A,. Le Bras, Y., Taberlet, P. & Coissac E. Obitools: A unix-inspired software package for DNA metabarcoding. Mol. Ecol. Resour. 16, 176–182 (2016).42.De Barba, M. et al. DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: Application to omnivorous diet. Mol. Ecol. Resour. 14, 306–323 (2014).Article 

    Google Scholar 
    43.Ficetola, G. F., Taberlet, P. & Coissac, E. How to limit false positives in environmental DNA and metabarcoding?. Mol. Ecol. Resour. 16, 604–607 (2016).CAS 
    Article 

    Google Scholar 
    44.Lahoz-Monfort, J.J., Guillera-Arroita, G. & Tingley, G., R. Statistical approaches to account for false positive errors in environmental DNA samples. Mol. Ecol. Resour. 16, 673–685 (2016).45.Bull, I., Lockheart, M., Elhmmali, M. Roberts, D. E. & Evershed, R. The origin of faeces by means of biomarker detection. Environ. Int. 27, 647–654 (2002).46.Mackay, H., Davies, K.L., Robertson, J., Roy, L., Bull, I.D. Whitehouse, N.J., Crone, A., Cavers, G., McCormick, F., Brown, A.G. & Henderson, A.C.G. Characterising life in settlements and structures: Incorporating faecal lipid biomarkers within a multiproxy case study of a wetland village. J. Archaeol. Sci. 121 (2020).47.Battarbee, R. W. Diatom analysis. In Handbook of Holocene Palaeoecology and Palaeohydrology (ed. Berglund, B. E.) 527–570 (Wiley, 1986).
    Google Scholar 
    48.Krammer, K., Lange-Bertalot, H. Bacillariophyceae. 1–4. Süßwasserflora von Mitteleuropa, Band 2/1–2/3. (Gustav Fischer, 1999–2004).49.Brooks, S.J., Langdon, P.G. & Heiri, O. The Identification and Use of Palaearctic Chironomidae Larvae in Palaeoecolgy. QRA Technical Guide No. 10. (Quaternary Research Association, 2007).50.Tóthm, M., van Hardenbroek, M., Bleicher, N. & Heiri, O. Pronounced early human impact on lakeshore environments documented by aquatic invertebrate remains in waterlogged Neolithic settlement deposits. Q. Sci. Rev. 205, 126–142 (2019).ADS 
    Article 

    Google Scholar 
    51.Moog, O. Fauna Aquatica Austriaca. Wasserwirtshcaftskataster, Bundesministerium für Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft, Vienna (2002)52.Bennion, H. A diatom-total phosphorus transfer function for shallow, eutrophic ponds in southeast England. Hydrobiologia 275(276), 391–410 (1994).Article 

    Google Scholar  More

  • in

    Ecosystem energy exchange

    Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain
    the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in
    Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles
    and JavaScript. More

  • in

    Susceptibility of anurans, lizards, and fish to infection with Dracunculus species larvae and implications for their roles as paratenic hosts

    This study demonstrated that several anuran genera (Xenopus, Lithobates [Rana], Hyla, and Anaxyrus [Bufo]), as well as Nile monitor lizards, green anoles, and featherfin catfish, are susceptible to infection with D. insignis and/or D. medinensis L3s. We also found that D. insignis and D. medinensis larvae can persist in anuran tissues for at least eight and two months, respectively, although the number of L3s recovered from each infected animal was generally low. Regardless, these data show that these animals could serve as paratenic hosts if they ingest infected copepods in nature and are subsequently ingested by an appropriate definitive host.We exposed animals using two different methods (group batch or by mouth [PO]), but aimed to primarily batch expose animals as that better mimics natural exposure. A few anuran species (i.e., American toads, Cope’s gray treefrogs, and adult African clawed frogs) were exposed to D. medinensis-infected copepods PO, as they had metamorphosed into adults before D. medinensis larvae became available for use and would be unlikely to ingest all copepods autonomously. Our primary goal in this study was to determine susceptibility to Dracunculus infection.Six anurans that were exposed as tadpoles underwent metamorphosis to froglets before being necropsied. Dracunculus L3s were recovered from two of these animals, supporting previous findings that D. insignis larvae can persist in anuran tissues through metamorphosis14. The persistence of larvae in the tissues through metamorphosis may facilitate Dracunculus transmission from aquatic to terrestrial food chains. This could be an important factor in transmission, as the majority of definitive hosts of Dracunculus nematodes are terrestrial. This study found that, in addition to X. laevis and Lithobates spp. (which have previously been infected with Dracunculus spp. larvae), Anaxyrus sp. and Hyla sp. can also become infected with Dracunculus L3s14,21. The infection of Anaxyrus sp. and Hyla sp. is particularly interesting, as members of these genera transition to a terrestrial or arboreal existence as adults, compared to Xenopus sp. and Lithobates spp. which remain completely or predominantly aquatic, even as adults. This transition to a terrestrial habitat could carry infectious larvae further from water sources, making them available to definitive hosts more widely across the landscape. However, the role of these animals in Dracunculus transmission would still depend on many other factors, including the natural history of these amphibian species, diets of definitive hosts, and how long Dracunculus L3s persist in paratenic hosts, as terrestrial anurans would be unlikely to acquire new infections after metamorphosis.During a previous experimental study, D. insignis L3s persisted in amphibian paratenic hosts for up to 37 DPI, at which time the animals were necropsied16. In this long-term infection trial, we found that D. insignis larvae persisted for at least 244 days (approximately eight months), while D. medinensis larvae persisted for at least 58 days (approximately two months). These results demonstrate that infection of a paratenic host can extend the time that L3s may persist in the environment well beyond the lifespan of a copepod21. As we had a limited supply of D. medinensis L3s, we were unable to conduct sufficient trials to determine whether D. insignis may persist longer in paratenic hosts than D. medinensis. If this difference was found to exist, it could contribute to the higher proportion of wild-caught adult frogs found to be infected with D. insignis than with D. medinensis during field surveys18,19. Further testing with an increased sample size would be required to determine whether the persistence of larvae actually differs between Dracunculus species or paratenic host species.No Dracunculus larvae were recovered from the two adult African clawed frogs that were fed D. medinensis L3s that had been recovered from other paratenic hosts. It is likely that our very small sample size (two animals) and the prolonged period before necropsy (4 months) explain these negative results. In our persistence trials, there was attrition over time so these animals should have been examined earlier after exposure. Future efforts to investigate transmission of Dracunculus between different paratenic hosts should use larger sample sizes and shorter infection periods. It would also be interesting to know if predatory animals, such as Nile monitor lizards, which can experimentally become infected with Dracunculus sp. larvae could become infected by ingesting other paratenic hosts.Fish were investigated for their potential role in Dracunculus transmission, as many fish species consume copepods as part of a natural diet25,26. Despite this, Dracunculus larvae have not been recovered during multiple studies screening wild-caught fish17,19. Dracunculus insignis L3s have rarely been recovered from previous experimental trials with fish16. When larvae were recovered from fish, larval recovery rates were very low (0.6–2.0% recovery; 1–2 larvae per fish) and only 3/43 (7.0%) of the fish harbored Dracunculus larvae upon necropsy16. In a separate trial, fish experimentally functioned as short-term transport hosts of D. medinensis and D. insignis to infect domestic ferrets7. Our findings from this trial were surprising, as we recovered up to 6 D. medinensis L3s from the tissues of three out of four (75%) exposed featherfin catfish. This fish species is common in the Chari River Basin area in Chad, Africa where high numbers of D. medinensis infections are reported in domestic dogs living in fishing villages, and is consumed by both people and dogs17. Dogs in these villages often eat discarded small fish or fish viscera4. Although our sample size was small, our current findings are evidence that some fish species may be more capable of serving as paratenic hosts for Dracunculus than those that have been previously tested. This finding further supports the continuation of the screening of wild fish muscle tissues for Dracunculus larvae.Lizards were included in this study because large, subcutaneous nematodes (believed to be Dracunculus sp.) were historically reported from Nile monitor lizards and these lizards are consumed by people20,22. However, a lack of contemporary reports and recent work in Chad, Africa, determining that large, subcutaneous nematodes recovered from wild Nile monitor lizards were not Dracunculus sp. but actually most similar to Ochoterenella sp., suggest that monitor lizards in this region are not definitive hosts for D. medinensis17. This current study confirms that Nile monitor and green anole lizards could become infected with Dracunculus larvae. As the diet of Nile monitor lizards can include amphibians and fish, were those prey to contain Dracunculus larvae, it is possible that monitors could serve as paratenic hosts, either by ingestion of larvae in fish intestines or in tissues of amphibians or fish, although these modes of transmission to paratenic hosts have not been confirmed23,24. It is unlikely that green anoles would become naturally infected with Dracunculus spp. due to their diet and primarily arboreal habitat; however, their infection demonstrates that multiple, distantly related lizard species are susceptible to experimental infection.Although anoles were exposed to both D. insignis and D. medinensis larvae, it is most likely that the recovered larvae were D. insignis, as only two D. medinensis-infected copepods were administered (in addition to 23 D. insignis-infected copepods). Species identity of these larvae could not be confirmed, however, as Dracunculus larvae can only be identified to species using molecular diagnostic techniques, which would destroy the sample, and these larvae were used in an experimental infection trial after recovery. Exposure of a ferret PO to the four larvae recovered from this anole (as part of a separate study) did not yield an infection, which is unsurprising given the low dose of larvae used. A previous study has shown that as few as 10 Dracunculus larvae may lead to infection of a ferret when administered interperitoneally (IP) (which was a more effective infection route than PO inoculation), therefore, four larvae administered PO would be unlikely to yield infection of a ferret27,28.In all trials, infection occurred only in those animals that were inoculated with or exposed to at least 20 copepods per individual, suggesting an impact of parasite dose-dependent infection probability for Dracunculus infection in paratenic hosts. As copepod infection rate during this study was estimated to be (ge) 25%, it is likely that animals ingesting 20 copepods would consume at least 5 Dracunculus sp. larvae. Previous studies demonstrated that 10 larvae (administered IP) were sufficient to infect a ferret, but that percent recovery was higher with IP infection than PO27,28. It is likely that a similar minimum infectious dose also exists for paratenic hosts and may differ by paratenic host species and mode of infection. Parasite dose-dependent infection probability of Dracunculus spp. merits further investigation, as understanding this relationship could help researchers to more effectively study transmission in the laboratory by performing experimental infection trials with greater reliability.Despite the variable sample sizes and exposure routes in this study, we demonstrated that a wide range of animals (anurans, fish, and lizards) were susceptible to infection with D. insignis and/or D. medinensis L3s. Importantly, one exposed fish species (Synodontis eupterus) was susceptible, opening up further concerns that certain fish species could serve as transport and paratenic hosts of Dracunculus species. Nile monitor lizards and anoles were successfully infected with L3s, demonstrating the first experimental infection of lizards with Dracunculus larvae. Dracunculus larvae remained L3s in the tissues of tested anurans for up to 244 days, extending the known persistence time of infectious larvae. Although no larvae were recovered from frogs that were fed L3s recovered from other paratenic hosts, continued investigation into the possibility of paratenic host to paratenic host transmission would be particularly interesting in determining if some predatory frogs (tadpoles or adults), fish, or lizards may concentrate higher numbers of L3s over time through predation of other infected paratenic hosts. Despite this study not determining how infectious larvae recovered from each of these paratenic hosts would be to another host, our findings contribute to a better understanding of the ability of these paratenic hosts to harbor Dracunculus L3s. This information is valuable to understanding how transmission to animal definitive hosts may be occurring, in addition to informing GWEP management decisions aiming to decrease transmission of D. medinensis to humans and animals. More