Philippa Kaur

1.
Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984).
CAS  Article  Google Scholar 
2.
Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019).
CAS  PubMed  Article  Google Scholar 

3.
LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570-2580.e6 (2018).
CAS  PubMed  Article  Google Scholar 

4.
Cunning, R., Silverstein, R. N. & Baker, A. C. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs 37, 145–152 (2018).
ADS  Article  Google Scholar 

5.
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 

6.
Porter, J. W. Primary productivity in the sea: Reef corals in situ. In Primary Productivity in the Sea. Environmental Science Research (ed. Falkowski, P. G.) 403–410 (Springer, Boston, 1980).
Google Scholar 

7.
Patterson, M. R., Sebens, K. P. & Olson, R. O. In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol. Oceanogr. 36, 936–948 (1991).
ADS  CAS  Article  Google Scholar 

8.
Wangpraseurt, D. et al. Spectral effects on Symbiodinium photobiology studied with a programmable light engine. PLoS ONE 9, e112809 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

9.
Kühl, M. et al. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159–172 (1995).
ADS  Article  Google Scholar 

10.
Burriesci, M. S., Raab, T. K. & Pringle, J. R. Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J. Exp. Biol. 215, 3467–3477 (2012).
CAS  PubMed  PubMed Central  Article  Google Scholar 

11.
Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17 (2009).
PubMed  Article  Google Scholar 

12.
Holcomb, M., Tambutté, E., Allemand, D. & Tambutté, S. Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2, e375 (2014).
PubMed  PubMed Central  Article  CAS  Google Scholar 

13.
Agostini, S., Fujimura, H., Hayashi, H. & Fujita, K. Mitochondrial electron transport activity and metabolism of experimentally bleached hermatypic corals. J. Exp. Mar. Biol. Ecol. 475, 100–107 (2016).
CAS  Article  Google Scholar 

14.
Imbs, A. B. & Yakovleva, I. M. Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: and experimental approach. Coral Reefs 31, 31–41 (2012).
ADS  Article  Google Scholar 

15.
Dunn, S. R., Pernice, M., Green, K., Hoegh-Guldberg, O. & Dove, S. G. Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out?. PLoS ONE 7, e39024 (2012).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

16.
Blackstone, N. Mitochondria and the redox control of development in cnidarians. Semin. Cell Dev. Biol. 20, 330–336 (2009).
CAS  PubMed  Article  Google Scholar 

17.
McDonald, A. E., Vanlerberghe, G. C. & Staples, J. F. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 212, 2627–2634 (2009).
CAS  PubMed  Article  Google Scholar 

18.
McDonald, A. E. & Gospodaryov, D. V. Alternative NAD(P)H dehydrogenase and alternative oxidase: proposed physiological roles in animals. Mitochondrion 45, 7–17 (2019).
CAS  PubMed  Article  Google Scholar 

19.
Raven, J. A. & Beardall, J. Consequences of the genotypic loss of mitochondrial Complex I in dinoflagellates and of phenotypic regulation of Complex I content in other photosynthetic organisms. J. Exp. Bot. 68, 2683–2692 (2017).
CAS  Article  Google Scholar 

20.
Oakley, C. A., Hopkinson, B. M. & Schmidt, G. W. Mitochondrial terminal alternative oxidase and its enhancement by thermal stress in the coral symbiont Symbiodinium. Coral Reefs 33, 543–552 (2014).
ADS  Article  Google Scholar 

21.
Nelson, H. R. & Altieri, A. H. Oxygen: The universal currency on coral reefs. Coral Reefs 38, 177–189 (2019).
ADS  Article  Google Scholar 

22.
Iglesias-prieto, A. R., Govind, N. S. & Trench, R. K. Isolation and characterization of three membrane bound chlorophyll-protein complexes from four dinoflagellate species. Philos. Trans. R. Soc. Lond. B 340, 381–392 (1993).
CAS  Article  Google Scholar 

23.
Aihara, Y., Takahashi, S. & Minagawa, J. Heat induction of cyclic electron flow around photosystem I in the symbiotic dinoflagellate Symbiodinium. Plant Physiol. 171, 522–529 (2016).
CAS  PubMed  PubMed Central  Article  Google Scholar 

24.
Leggat, W., Badger, M. & Yellowlees, D. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol. 121, 1247–1255 (1999).
CAS  PubMed  PubMed Central  Article  Google Scholar 

25.
Raven, J. A., Suggett, D. J. & Giordano, M. Inorganic carbon concentrating mechanisms in free-living and symbiotic dinoflagellates and chromerids. J. Phycol. https://doi.org/10.1111/jpy.13050 (2020).
Article  PubMed  PubMed Central  Google Scholar 

26.
Barott, K. L. et al. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc. Natl. Acad. Sci. USA 112, 607–612 (2015).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

27.
Mayfield, A. B., Hsiao, Y. Y., Chen, H. K. & Chen, C. S. Rubisco expression in the dinoflagellate Symbiodinium sp. is influenced by both photoperiod and endosymbiotic lifestyle. Mar. Biotechnol. 16, 371–384 (2014).
CAS  PubMed  Article  PubMed Central  Google Scholar 

28.
Tremblay, P., Grover, R., Maguer, J. F., Legendre, L. & Ferrier-Pagès, C. Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation. J. Exp. Biol. 215, 1384–1393 (2012).
CAS  PubMed  Article  PubMed Central  Google Scholar 

29.
Maor-Landaw, K., van Oppen, M. J. H. & McFadden, G. I. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae). Ecol. Evol. 10, 451–466 (2020).
PubMed  Article  PubMed Central  Google Scholar 

30.
Roth, M. S. The engine of the reef: photobiology of the coral-algal symbiosis. Front. Microbiol. 5, 1–22 (2014).
ADS  Article  Google Scholar 

31.
Roberty, S., Béraud, E., Grover, R. & Ferrier-Pagès, C. Coral productivity is co-limited by bicarbonate and ammonium availability. Microorganisms 8, 640 (2020).
PubMed Central  Article  PubMed  Google Scholar 

32.
Tchernov, D. et al. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. USA 101, 13531–13535 (2004).
ADS  CAS  PubMed  Article  Google Scholar 

33.
Cardol, P., Forti, G. & Finazzi, G. Regulation of electron transport in microalgae. Biochim. Biophys. Acta 1807, 912–918 (2011).
CAS  PubMed  Article  Google Scholar 

34.
Papageorgiou, G. C. Chlorophyll a Fluorescence. A Signature of Photosynthesis (Springer, Dordrecht, 2004).
Google Scholar 

35.
Hennige, S. J., Suggett, D. J., Warner, M. E., McDougall, K. E. & Smith, D. J. Photobiology of Symbiodinium revisited: Bio-physical and bio-optical signatures. Coral Reefs 28, 179–195 (2009).
ADS  Article  Google Scholar 

36.
Reynolds, J. M. C., Bruns, B. U., Fitt, W. K. & Schmidt, G. W. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc. Natl. Acad. Sci. USA 105, 17206 (2008).
CAS  Article  Google Scholar 

37.
Roberty, S., Bailleul, B., Berne, N., Franck, F. & Cardol, P. PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol. 204, 81–91 (2014).
CAS  PubMed  Article  Google Scholar 

38.
Dang, K. V., Pierangelini, M., Roberty, S. & Cardol, P. Alternative photosynthetic electron transfers and bleaching phenotypes upon acute heat stress in Symbiodinium and Breviolum spp. (Symbiodiniaceae) in culture. Front. Mar. Sci. 6, 1–10 (2019).
Article  Google Scholar 

39.
Hoogenboom, M. O., Campbell, D. A., Beraud, E., DeZeeuw, K. & Ferrier-Pagès, C. Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts. PLoS ONE 7, e30167 (2012).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

40.
Szabó, M. et al. Non-intrusive assessment of photosystem II and photosystem I in whole coral tissues. Front. Mar. Sci. 4, 269 (2017).
Article  Google Scholar 

41.
Enríquez, S., Méndez, E. R. & Iglesias-Prieto, R. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50, 1025–1032 (2005).
ADS  Article  Google Scholar 

42.
Gilmore, A. M. et al. Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem. Photobiol. 77, 515 (2003).
CAS  PubMed  Article  Google Scholar 

43.
Maxwell, K. & Johnson, G. N. Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 51, 659–668 (2000).
CAS  PubMed  Article  Google Scholar 

44.
Sandmann, G., Reck, H., Kessler, E. & Böger, P. Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch. Microbiol. 134, 23–27 (1983).
CAS  Article  Google Scholar 

45.
Schreiber, U. Redox changes of ferredoxin, P700, and plastocyanin measured simultaneously in intact leaves. Photosynth. Res. 134, 343–360 (2017).
CAS  PubMed  PubMed Central  Article  Google Scholar 

46.
Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. USA 102, 4913–4918 (2005).
ADS  CAS  PubMed  Article  Google Scholar 

47.
Witt, H. et al. Species-specific differences of the spectroscopic properties of P700: Analysis of the influence of non-conserved amino acid residues by site-directed mutagenesis of photosystem I from Chlamydomonas reinhardtii. J. Biol. Chem. 278, 46760–46771 (2003).
CAS  PubMed  Article  Google Scholar 

48.
Klughammer, C. & Schreiber, U. An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192, 261–268 (1994).
CAS  Article  Google Scholar 

49.
Bailleul, B., Cardol, P., Breyton, C. & Finazzi, G. Electrochromism: A useful probe to study algal photosynthesis. Photosynth. Res. 106, 179–189 (2010).
CAS  PubMed  Article  Google Scholar 

50.
Vega De Luna, F., Dang, K. V., Cardol, M., Roberty, S. & Cardol, P. Photosynthetic capacity of the endosymbiotic dinoflagellate Cladocopium sp. is preserved during digestion of its jellyfish host Mastigias papua by the anemone Entacmaea medusivora. FEMS Microbiol. Ecol. 95, 1–7 (2019).
Google Scholar 

51.
Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006).
CAS  PubMed  Article  PubMed Central  Google Scholar 

52.
Hume, B. C. C. et al. An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6, e4816 (2018).
PubMed  PubMed Central  Article  CAS  Google Scholar 

53.
Hume, B. C. C. et al. SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080 (2019).
CAS  PubMed  PubMed Central  Article  Google Scholar 

54.
Shafir, S., Van Rijn, J. & Rinkevich, B. Nubbing of coral colonies: a novel approach for the development of inland broodstocks. Aquar. Sci. Conserv. 3, 183–190 (2001).
Article  Google Scholar 

55.
Hoadley, K. D. et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9, 1–15 (2019).
CAS  Article  Google Scholar 

56.
Heyward, A. J. & Collins, J. D. Fragmentation in Montipora ramosa: the genet and ramet concept applied to a reef coral. Coral Reefs 4, 35–40 (1985).
ADS  Article  Google Scholar 

57.
Raz-Bahat, M., Erez, J. & Rinkevich, B. In vivo light-microscopic documentation for primary calcification processes in the hermatypic coral Stylophora pistillata. Cell Tissue Res. 325, 361–368 (2006).
PubMed  Article  Google Scholar 

58.
Warner, M. E., Fitt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96, 8007–8012 (1999).
ADS  CAS  PubMed  Article  Google Scholar 

59.
Rehman, A. U. et al. Symbiodinium sp. cells produce light-induced intra- and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis. New Phytol. 212, 472–484 (2016).
CAS  PubMed  Article  Google Scholar 

60.
Hill, R. & Ralph, P. J. Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence. Symbiosis 46, 45–56 (2008).
CAS  Google Scholar 

61.
Einbinder, S. et al. Novel adaptive photosynthetic characteristics of mesophotic symbiotic microalgae within the reef-building coral, Stylophora pistillata. Front. Mar. Sci. 3, 1–9 (2016).
Article  Google Scholar 

62.
Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007).
ADS  CAS  Article  Google Scholar 

63.
Ferrier-Pagès, C., Gattuso, J. P., Dallot, S. & Jaubert, J. Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellae coral Stylophora pistillata. Coral Reefs 19, 103–113 (2000).
Article  Google Scholar 

64.
Peltier, G., Tolleter, D., Billon, E. & Cournac, L. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106, 19–31 (2010).
CAS  PubMed  Article  PubMed Central  Google Scholar 

65.
Pierangelini, M., Thiry, M. & Cardol, P. Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming. New Phytol. https://doi.org/10.1111/nph.16738 (2020).
Article  PubMed  PubMed Central  Google Scholar 

66.
Bailleul, B. et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524, 366–369 (2015).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

67.
Badger, M. R. et al. Electron flow to oxygen in higher plants and algae: Rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos. Trans. R. Soc. B 355, 1433–1446 (2000).
CAS  Article  Google Scholar 

68.
Fan, D. Y. et al. Obstacles in the quantification of the cyclic electron flux around photosystem I in leaves of C3 plants. Photosynth. Res. 129, 239–251 (2016).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

69.
Szabó, M. et al. Effective light absorption and absolute electron transport rates in the coral Pocillopora damicornis. Plant Physiol. Biochem. 83, 159–167 (2014).
ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

70.
Kato, H. et al. Characterization of a giant photosystem I supercomplex in the symbiotic dinoflagellate Symbiodiniaceae. Plant Physiol. https://doi.org/10.1104/pp.20.00726 (2020).
Article  PubMed  PubMed Central  Google Scholar 

71.
Alric, J. Cyclic electron flow around photosystem I in unicellular green algae. Photosynth. Res. 106, 47–56 (2010).
CAS  PubMed  Article  Google Scholar 

72.
Melis, A. & Jeanette, J. S. Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc. Natl. Acad. Sci. USA. 77, 4712–4716 (1980).
ADS  CAS  PubMed  Article  Google Scholar  More

1.
Bé, A. W. An ecological, zoogeographic and taxonomic review of Recent planktonic foraminifera. In Oceanic micropaleontology (ed. Ramsay, A. T. S.) 1–100 (Academic Press, New York, 1977).
Google Scholar 
2.
Schiebel, R. & Hemleben, C. Planktic Foraminifera in the Modern Ocean (Springer, Berlin, 2017).
Google Scholar 

3.
Taylor, B. J. et al. Distribution and ecology of planktic foraminifera in the North Pacific: implications for paleo-reconstructions. Quat. Sci. Rev. 191, 256–274 (2018).
ADS  Article  Google Scholar 

4.
Schiebel, R. Planktic foraminiferal sedimentation and the marine calcite budget. Global Biogeochem. Cycles 16, 3-1-3–21 (2002).
Article  CAS  Google Scholar 

5.
Kucera, M. Chapter six planktonic foraminifera as tracers of past oceanic environments. Dev. Mar. Geol. 1, 213–262 (2007).
Google Scholar 

6.
Fox, L., Stukins, S., Hill, T. & Miller, C. G. Quantifying the Effect of Anthropogenic Climate Change on Calcifying Plankton. Sci. Rep. 10, 1620 (2020).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

7.
De Moel, H. et al. Planktic foraminiferal shell thinning in the Arabian Sea due to anthropogenic ocean acidification?. Biogeosci. Discuss. 6, 1811–1835 (2009).
ADS  Article  Google Scholar 

8.
Moy, A. D., Howard, W. R., Bray, S. G. & Trull, T. W. Reduced calcification in modern Southern Ocean planktonic foraminifera. Nat. Geosci. 2, 276–280 (2009).
ADS  Article  CAS  Google Scholar 

9.
Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).
ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

10.
Wefer, G., Berger, W. H., Bijma, J. & Fischer, G. Clues to ocean history: a brief overview of proxies. In Use of Proxies in Paleoceanography 1–68 (Springer, Berlin, 1999). http://doi.org/10.1007/978-3-642-58646-0_1

11
Bé, A. W. H., Bishop, J. K. B., Sverdlove, M. S. & Gardner, W. D. Standing stock, vertical distribution and flux of planktonic foraminifera in the Panama Basin. Mar. Micropaleontol. 9, 307–333 (1985).
ADS  Article  Google Scholar 

12.
Pados, T. & Spielhagen, R. F. Species distribution and depth habitat of recent planktic foraminifera in Fram Strait, Arctic Ocean. Polar Res. 33, 22483 (2014).
Article  Google Scholar 

13.
Salmon, K. H., Anand, P., Sexton, P. F. & Conte, M. Upper ocean mixing controls the seasonality of planktonic foraminifer fluxes and associated strength of the carbonate pump in the oligotrophic North Atlantic. Biogeosciences 12, 223–235 (2015).
ADS  Article  Google Scholar 

14.
Žarić, S., Donner, B., Fischer, G., Mulitza, S. & Wefer, G. Sensitivity of planktic foraminifera to sea surface temperature and export production as derived from sediment trap data. Mar. Micropaleontol. 55, 75–105 (2005).
ADS  Article  Google Scholar 

15.
Schiebel, R., Waniek, J., Bork, M. & Hemleben, C. Planktic foraminiferal production stimulated by chlorophyll redistribution and entrainment of nutrients. Deep Sea Res. Part I 48, 721–740 (2001).
Article  CAS  Google Scholar 

16.
Venancio, I. M. et al. Planktonic foraminifera shell fluxes from a weekly resolved sediment trap record in the southwestern Atlantic: evidence for synchronized reproduction. Mar. Micropaleontol. 125, 25–35 (2016).
ADS  Article  Google Scholar 

17.
Erez, J. & Honjo, S. Comparison of isotopic composition of planktonic foraminifera in plankton tows, sediment traps and sediments. Palaeogeogr. Palaeoclimatol. Palaeoecol. 33, 129–156 (1981).
Article  Google Scholar 

18.
Deuser, W. G., Ross, E. H., Hemleben, C. & Spindler, M. Seasonal changes in species composition, numbers, mass, size, and isotopic composition of planktonic foraminifera settling into the deep Sargasso Sea. Palaeogeogr. Palaeoclimatol. Palaeoecol. 33, 103–127 (1981).
Article  Google Scholar 

19.
Deuser, W. G. & Ross, E. H. Seasonally abundant planktonic foraminifera of the Sargasso Sea: succession, deep-water fluxes, isotopic compositions, and paleoceanographic implications. J. Foraminifer. Res. 19, 268–293 (1989).
Article  Google Scholar 

20.
Sautter, L. R. & Thunell, R. C. Seasonal succession of planktonic Foraminifera: results from a four-year time-series sediment trap experiment in the Northeast Pacific. J. Foraminifer. Res. 19, 253–267 (1989).
Article  Google Scholar 

21.
Curry, W. B., Thunell, R. C. & Honjo, S. Seasonal changes in the isotopic composition of planktonic foraminifera collected in Panama Basin sediment traps. Earth Planet. Sci. Lett. 64, 33–43 (1983).
ADS  Article  CAS  Google Scholar 

22.
Thunell, R. C. & Honjo, S. Seasonal and interannual changes in planktonic foraminiferal production in the North Pacific. Nature 328, 335–337 (1988).
ADS  Article  Google Scholar 

23.
Smart, S. M. et al. Ground-truthing the planktic foraminifer-bound nitrogen isotope paleo-proxy in the Sargasso Sea. Geochim. Cosmochim. Acta 235, 463–482 (2018).
ADS  Article  CAS  Google Scholar 

24.
King, A. L. & Howard, W. R. Seasonality of foraminiferal flux in sediment traps at Chatham rise, SW Pacific: implications for paleotemperature estimates. Deep Res. Part I Oceanogr. Res. Pap. 48, 1687–1708 (2001).
ADS  Article  Google Scholar 

25.
Levanon-Spanier, I., Padan, E. & Reiss, Z. Primary production in a desert-enclosed sea—the Gulf of Elat (Aqaba), Red Sea. Deep Sea Res Part A. Oceanogr. Res. Pap. 26, 673–685 (1979).
ADS  Article  CAS  Google Scholar 

26.
Reiss, Z. & Hottinger, L. The Gulf of Aqaba: ecological micropaleontology (Springer, Berlin, 1984).
Google Scholar 

27.
Lazar, B. et al. Recent environmental changes in the chemical–biological oceanography of the Gulf of Aqaba (Eilat). In Aqaba-Eilat, the Improbable Gulf. Environment, Biodiversity and Preservation 49–61 (2008).

28.
Erez, J., Almogi-Labin, A. & Avraham, S. On the life history of planktonic Foraminifera: lunar reproduction cycle in Globigerinoides sacculifer (Brady). Paleoceanography 6, 295–306 (1991).
ADS  Article  Google Scholar 

29.
Zarubin, M., Lindemann, Y. & Genin, A. The Dispersion-Confinement mechanism: phytoplankton dynamics and the spring bloom in a deeply-mixing subtropical sea. Prog. Oceanogr. 155, 13–27 (2017).
ADS  Article  Google Scholar 

30.
Kimor, B. & Golandsky, B. Microplankton of the Gulf of Elat: Aspects of seasonal and bathymetric distribution. Mar. Biol. 42, 55–67 (1977).
Article  Google Scholar 

31.
Winter, A., Reiss, Z. & Luz, B. Distribution of living coccolithophore assemblages in the Gulf of Elat (Aqaba). Mar. Micropaleontol. 4, 197–223 (1979).
ADS  Article  Google Scholar 

32.
Lindell, D. & Post, A. Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. Limnol. Oceanogr. 40, 1130–1141 (1995).
ADS  Article  Google Scholar 

33.
Labiosa, R. G., Arrigo, K. R., Genin, A., Monismith, S. G. & Van Dijken, G. The interplay between upwelling and deep convective mixing in determining the seasonal phytoplankton dynamics in the Gulf of Aqaba: evidence from SeaWiFS and MODIS. Limnol. Oceanogr. 48, 2355–2368 (2003).
ADS  Article  Google Scholar 

34.
Meeder, E. et al. Nitrite dynamics in the open ocean – clues from seasonal and diurnal variations. Mar. Ecol. Prog. Ser. 453, 11–26 (2012).
ADS  Article  CAS  Google Scholar 

35.
Carlson, D. F., Fredj, E. & Gildor, H. The annual cycle of vertical mixing and restratification in the Northern Gulf of Eilat/Aqaba (Red Sea) based on high temporal and vertical resolution observations. Deep. Res. Part I(84), 1–17 (2014).
Google Scholar 

36.
Shaked, Y. Iron redox dynamics in the surface waters of the Gulf of Aqaba, Red Sea. Geochim. Cosmochim. Acta 72, 1540–1554 (2008).
ADS  Article  CAS  Google Scholar 

37.
Almogi-Labin, A. Population dynamics of planktic Foraminifera and Pteropoda—Gulf of Aqaba, Red Sea. Proc. R. Netherl. Acad. Sci. B 87, 481–511 (1984).
Google Scholar 

38.
Chernihovsky, N., Torfstein, A. & Almogi-Labin, A. Seasonal flux patterns of planktonic foraminifera in a deep, oligotrophic, marginal sea: Sediment trap time series from the Gulf of Aqaba, northern Red Sea. Deep Sea Res Part I Oceanogr. Res. Pap. 140, 78–94 (2018).
ADS  Article  CAS  Google Scholar 

39.
Torfstein, A., Kienast, S. S., Yarden, B., Rivlin, A., Isaacs, S. & Shaked, Y. Bulk and export production fluxes in the Gulf of Aqaba, Northern Red Sea. ACS Earth Space Chem. 4(8), 1461–1479 (2020).
Article  CAS  Google Scholar 

40.
Shaked, Y. & Genin, A. Israel National Monitroing Program at the Gulf of Eilat Annual Report. (2018).

41.
Genin, A., Lazar, B. & Brenner, S. Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo. Nature 377, 507–510 (1995).
ADS  Article  CAS  Google Scholar 

42.
Torfstein, A. & Kienast, S. S. No Correlation between atmospheric dust and surface ocean chlorophyll-a in the oligotrophic Gulf of Aqaba, Northern Red Sea. J. Geophys. Res. Biogeosciences 123, 391–405 (2018).
ADS  Article  Google Scholar 

43.
Meilland, J. et al. Highly replicated sampling reveals no diurnal vertical migration but stable species-specific vertical habitats in planktonic foraminifera. J. Plankton Res. https://doi.org/10.1093/plankt/fbz002 (2019).
Article  Google Scholar 

44.
Iluz, D. et al. Short-term variability in primary productivity during a wind-driven diatom bloom in the Gulf of Eilat (Aqaba). Aquat. Microb. Ecol. 56, 205–215 (2009).
Article  Google Scholar 

45.
Jonkers, L., Brummer, G.-J.A., Peeters, F. J. C., van Aken, H. M. & De Jong, M. F. Seasonal stratification, shell flux, and oxygen isotope dynamics of left-coiling N. pachyderma and T. quinqueloba in the western subpolar North Atlantic. Paleoceanography 25, 1–13 (2010).
Google Scholar 

46.
Jonkers, L. & Kučera, M. Global analysis of seasonality in the shell flux of extant planktonic Foraminifera. Biogeosciences 12, 2207–2226 (2015).
ADS  Article  Google Scholar 

47.
Hemleben, C., Spindler, M. & Anderson, O. R. Modern Planktonic Foraminifera (Springer, Berlin, 2012).
Google Scholar 

48.
Brummer, G.-J.A., Hemleben, C. & Spindler, M. Planktonic foraminiferal ontogeny and new perspectives for micropalaeontology. Nature 319, 50–52 (1986).
ADS  Article  Google Scholar 

49.
Boltovsky, E. Globigerinita clarkei (Rögl & Bolli) – an unfairly ignored small planktic foraminifer. Boreas 20, 151–154 (2008).
Article  Google Scholar 

50.
Takagi, H. et al. Characterizing photosymbiosis in modern planktonic foraminifera. Biogeosciences 16, 3377–3396 (2019).
ADS  Article  CAS  Google Scholar 

51.
Grigoratou, M. et al. A trait-based modelling approach to planktonic foraminifera ecology. Biogeosciences 16, 1469–1492 (2019).
ADS  Article  Google Scholar 

52.
Spindler, M., Hemleben, C., Salomons, J. B. & Smit, L. P. Feeding behavior of some planktonic foraminifers in laboratory cultures. J. Foraminifer. Res. 14, 237–249 (1984).
Article  Google Scholar 

53.
Spindler, M., Hemleben, C., Bayer, U., Bé, A. & Anderson, O. Lunar periodicity of reproduction in the planktonic foraminifer Hastigerina pelagica. Mar. Ecol. Prog. Ser. 1, 61–64 (1979).
ADS  Article  Google Scholar 

54.
Jonkers, L., Reynolds, C. E., Richey, J. & Hall, I. R. Lunar periodicity in the shell flux of planktonic foraminifera in the Gulf of Mexico. Biogeosciences 12, 3061–3070 (2015).
ADS  Article  Google Scholar 

55.
Bijma, J., Erez, J. & Hemleben, C. Lunar and semi-lunar reproduction cycles in some spinose planktonic foraminifers. J. Foraminifer. Res. 20, 117–127 (1990).
Article  Google Scholar 

56.
Lin, H.-L. The seasonal succession of modern planktonic foraminifera: sediment traps observations from southwest Taiwan waters. Cont. Shelf Res. 84, 13–22 (2014).
ADS  Article  Google Scholar 

57.
Lončarić, N., Brummer, G. J. A. & Kroon, D. Lunar cycles and seasonal variations in deposition fluxes of planktic foraminiferal shell carbonate to the deep South Atlantic (central Walvis Ridge). Deep Res. Part I Oceanogr. Res. Pap. 52, 1178–1188 (2005).
ADS  Article  Google Scholar 

58.
Davis, C. V. et al. Extensive morphological variability in asexually produced planktic foraminifera. Sci. Adv. https://doi.org/10.1126/sciadv.abb8930 (2020).
Article  PubMed  PubMed Central  Google Scholar 

59.
Takagi, H., Kurasawa, A. & Kimoto, K. Observation of asexual reproduction with symbiont transmission in planktonic foraminifera. J. Plankton Res. https://doi.org/10.1093/plankt/fbaa033 (2020).
Article  Google Scholar 

60.
Hottinger, L., Halicz, E. & Reiss, Z. Recent Foraminiferida from the Gulf of Aqaba, Red Sea. Opera Sazu, Ljubljana, Slovania (1993).

61.
Brummer, G. J. A. & Kroon, D. Planktonic foraminifers as tracers of ocean-climate history: Ontogeny, relationships and preservation of modern species and stable isotopes, phenotypes and assemblage distribution in different water masses (Free University Press, 1988).

62.
Sprintall, J. & Tomczak, M. Evidence of the barrier layer in the surface layer of the tropics. J. Geophys. Res. 97, 7305 (1992).
ADS  Article  Google Scholar 

63.
Trauth, M. H. MATLAB Recipes for Earth Sciences MATLAB Recipes for Earth Sciences 2nd edn. (Springer, Berlin, 2007). https://doi.org/10.1007/978-3-540-72749-1.
Google Scholar  More

1.
Thomson, W. On Holtenia, a genus of vitreous sponges. Proc. R. Soc. Lond. 18(114–122), 32–35 (1869).
Google Scholar 
2.
Carter, H. J. Descriptions and figures of deep-sea sponges and their spicules from the Atlantic Ocean dredged up on board HMS Porcupine chiefly in 1869. Ann. Mag. Nat. Hist. 4(14), 207–221 (1874).
Article  Google Scholar 

3.
Bett, B. J. & Rice, A. L. The influence of hexactinellid sponge (Pheronema carpenteri) spicules on the patchy distribution of macrobenthos in the porcupine seabight (bathyal ne atlantic). Ophelia 36(3), 217–226 (1992).
Article  Google Scholar 

4.
Buhl-Mortensen, L. et al. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar. Ecol. 31(1), 21–50 (2010).
ADS  Article  Google Scholar 

5.
Maldonado, M., et al. Sponge grounds as key marine habitats: a synthetic review of types, structure, functional roles, and conservation concerns. In: Marine Animal Forests (eds Rossi, S., Bramanti, L., Gori, A., Orejas Saco del Valle, C.) (Springer, Berlin, 2016).
Google Scholar 

6.
Klitgaard, A. B. & Tendal, O. S. Distribution and species composition of mass occurrences of large-sized sponges in the northeast Atlantic. Prog. Oceanogr. 61(1), 57–98 (2004).
ADS  Article  Google Scholar 

7.
van Soest, R. W. M. et al. Sponge diversity and community composition in Irish bathyal coral reefs. Contrib. Zool. 76(2), 121–142 (2007).
Article  Google Scholar 

8.
Meyer, H. K., Roberts, E. M., Rapp, H. T. & Davies, A. J. Spatial patterns of arctic sponge ground fauna and demersal fish are detectable in autonomous underwater vehicle (AUV) imagery. Deep Sea Res. Part I Oceanogr. Res. Pap. 153, 103137 (2019).
Article  Google Scholar 

9.
Beazley, L. et al. Predicted distribution of the glass sponge Vazella pourtalesii on the Scotian Shelf and its persistence in the face of climatic variability. PLoS ONE 13(10), e0205505 (2018).
PubMed  PubMed Central  Article  CAS  Google Scholar 

10.
Hawkes, N. et al. Glass sponge grounds on the Scotian Shelf and their associated biodiversity. Mar. Ecol. Prog. Ser. 614, 91–109 (2019).
ADS  Article  Google Scholar 

11.
Kutti, T., Bannister, R. J. & Fosså, J. H. Community structure and ecological function of deep-water sponge grounds in the Traenadypet MPA—Northern Norwegian continental shelf. Cont. Shelf Res. 69, 21–30 (2013).
ADS  Article  Google Scholar 

12.
Cathalot, C. et al. Cold-water coral reefs and adjacent sponge grounds: hotspots of benthic respiration and organic carbon cycling in the deep sea. Front. Mar. Sci. 2(37), 1–12 (2015).
Google Scholar 

13.
Klitgaard, A. B. The fauna associated with outer shelf and upper slope sponges (Porifera, Demospongiae) at the Faroe Islands, northeastern Atlantic. Sarsia 80(1), 1–22 (1995).
Article  Google Scholar 

14.
Kazanidis, G., Henry, L. A., Roberts, J. M. & Witte, U. F. Biodiversity of Spongosorites coralliophaga (Stephens, 1915) on coral rubble at two contrasting cold-water coral reef settings. Coral Reefs 35(1), 193–208 (2016).
ADS  Article  Google Scholar 

15.
Freese, J. L. & Wing, B. L. Juvenile red rockfish, Sebastes sp., associations with sponges in the Gulf of Alaska. Mar. Fish. Rev. 65(3), 38–42 (2003).
Google Scholar 

16.
Kenchington, E., Power, D. & Koen-Alonso, M. Associations of demersal fish with sponge grounds on the continental slopes of the northwest Atlantic. Mar. Ecol. Prog. Ser. 477, 217–230 (2013).
ADS  Article  Google Scholar 

17.
Pile, A. J. & Young, C. M. The natural diet of a hexactinellid sponge: benthic–pelagic coupling in a deep-sea microbial food web. Deep Sea Res. Part I Oceanogr. Res. Pap. 53(7), 1148–1156 (2006).
ADS  Article  Google Scholar 

18.
Kahn, A. S., Yahel, G., Chu, J. W., Tunnicliffe, V. & Leys, S. P. Benthic grazing and carbon sequestration by deep-water glass sponge reefs. Limnol. Oceanogr. 60(1), 78–88 (2015).
ADS  CAS  Article  Google Scholar 

19.
Vad, J. et al. Potential impacts of offshore oil and gas activities on deep-sea sponges and the habitats they form. Adv. Mar. Biol. 79, 33–60 (2018).
PubMed  Article  Google Scholar 

20.
Kutti, T. et al. Metabolic responses of the deep-water sponge Geodia barretti to suspended bottom sediment, simulated mine tailings and drill cuttings. J. Exp. Mar. Biol. Ecol. 473, 64–72 (2015).
CAS  Article  Google Scholar 

21.
Edge, K. J. et al. Sub-lethal effects of water-based drilling muds on the deep-water sponge Geodia barretti. Environ. Pollut. 212, 525–534 (2016).
CAS  PubMed  Article  Google Scholar 

22.
Kazanidis, G. et al. Distribution of deep-sea sponge aggregations in an area of multisectoral activities and changing oceanic conditions. Front. Mar. Sci. 6, 163 (2019).
Article  Google Scholar 

23.
Vieira, R. P. et al. Deep-sea sponge aggregations (Pheronema carpenteri) in the Porcupine Seabight (NE Atlantic) potentially degraded by demersal fishing. Prog. Oceanogr. 183, 102189 (2020).
Article  Google Scholar 

24.
Hentschel, U. et al. Microbial diversity of marine sponges. In Sponges (Porifera) (ed. Müller, W. E. G.) 59–88 (Springer, Berlin, 2003).
Google Scholar 

25.
Taylor, M. W., Hill, R. T., Piel, J., Thacker, R. W. & Hentschel, U. Soaking it up: the complex lives of marine sponges and their microbial associates. ISME J. 1(3), 187 (2007).
PubMed  Article  Google Scholar 

26.
Reiswig, H. M. Bacteria as food for temperate-water marine sponges. Can. J. Zool. 53(5), 582–589 (1975).
Article  Google Scholar 

27.
Vacelet, J. & Boury-Esnault, N. Carnivorous sponges. Nature 373(6512), 333 (1995).
ADS  CAS  Article  Google Scholar 

28.
Bart, M.C. et al.Dissolved organic carbon (DOC) is essential to balance the metabolic demands of North-Atlantic deep-sea sponges. https://doi.org/10.1101/2020.09.21.305086 (2020).

29.
Rix, L. et al. Coral mucus fuels the sponge loop in warm-and cold-water coral reef ecosystems. Sci. Rep. 6(1), 1–11 (2016).
Article  CAS  Google Scholar 

30.
de Goeij, J. M., Lesser, M. P. & Pawlik, J. R. Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In Climate Change, Ocean Acidification and Sponges (eds Carballo, J. L. & Bell, J. J.) (Springer, Berlin, 2017).
Google Scholar 

31.
Hansell, D. A., Carlson, C. A., Repeta, D. J. & Schlitzer, R. Dissolved organic matter in the ocean: a controversy stimulates new insights. Oceanography 22(4), 202–211 (2009).
Article  Google Scholar 

32.
Wendt, D. E. & Johnson, C. H. Using latent effects to determine the ecological importance of dissolved organic matter to marine invertebrates. Integr. Comp. Biol. 46(5), 634–642 (2006).
CAS  PubMed  Article  Google Scholar 

33.
Azam, F. et al. The ecological role of water-column microbes in the sea. Mari. Ecol. Prog. Ser. 10, 257–263 (1983).
ADS  Article  Google Scholar 

34.
Yahel, G., Sharp, J. H., Marie, D., Häse, C. & Genin, A. In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: Bulk DOC is the major source for carbon. Limnol. Oceanogr. 48(1), 141–149 (2003).
ADS  Article  Google Scholar 

35.
de Goeij, J. M., van den Berg, H., van Oostveen, M. M., Epping, E. H. & Van Duyl, F. C. Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar. Ecol. Prog. Ser. 357, 139–151 (2008).
ADS  Article  CAS  Google Scholar 

36.
Mueller, B. et al. Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC). PLoS ONE 9(2), e90152 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

37.
Reiswig, H. M. Partial carbon and energy budgets of the bacteriosponge Verohgia fistularis (Porifera: Demospongiae) in Barbados. Mar. Ecol. 2(4), 273–293 (1981).
ADS  CAS  Article  Google Scholar 

38.
Morganti, T., Coma, R., Yahel, G. & Ribes, M. Trophic niche separation that facilitates co-existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes. Limnol. Oceanogr. 62(5), 1963–1983 (2017).
ADS  CAS  Article  Google Scholar 

39.
McMurray, S. E., Stubler, A. D., Erwin, P. M., Finelli, C. M. & Pawlik, J. R. A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar. Ecol. Prog. Ser. 588, 1–14 (2018).
ADS  CAS  Article  Google Scholar 

40.
Ribes, M. et al. Functional convergence of microbes associated with temperate marine sponges. Environ. Microbiol. 14(5), 1224–1239 (2012).
CAS  PubMed  Article  Google Scholar 

41.
Hoer, D. R., Gibson, P. J., Tommerdahl, J. P., Lindquist, N. L. & Martens, C. S. Consumption of dissolved organic carbon by Caribbean reef sponges. Limnol. Oceanogr. 63(1), 337–351 (2018).
ADS  CAS  Article  Google Scholar 

42.
de Goeij, J. M., Moodley, L., Houtekamer, M., Carballeira, N. M. & Van Duyl, F. C. Tracing 13C-enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge Halisarca caerulea: Evidence for DOM-feeding. Limnol. Oceanogr. 53(4), 1376–1386 (2008).
ADS  Article  Google Scholar 

43.
de Goeij, J. M. et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342(6154), 108–110 (2013).
ADS  PubMed  Article  CAS  Google Scholar 

44.
Rix, L. et al. Differential recycling of coral and algal dissolved organic matter via the sponge loop. Funct. Ecol. 31(3), 778–789 (2017).
Article  Google Scholar 

45.
de Goeij, J. M. et al. Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding. J. Exp. Biol. 212(23), 3892–3900 (2009).
PubMed  Article  Google Scholar 

46.
Achlatis, M. et al. Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter. Proc. R. Soc. B 286(1916), 20192153 (2019).
CAS  PubMed  Article  Google Scholar 

47.
Gooday, A. J. Biological responses to seasonally varying fluxes of organic matter to the ocean floor: a review. J. Oceanogr. 58(2), 305–332 (2002).
CAS  Article  Google Scholar 

48.
Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K. & Arbizu, P. M. Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23(9), 518–528 (2008).
PubMed  Article  Google Scholar 

49.
Gantt, S. E. et al. Testing the relationship between microbiome composition and flux of carbon and nutrients in Caribbean coral reef sponges. Microbiome 7(1), 124 (2019).
PubMed  PubMed Central  Article  Google Scholar 

50.
Maldonado, M., Ribes, M. & van Duyl, F. C. Nutrient fluxes through sponges: biology, budgets, and ecological implications. In Advances in Marine Biology (eds Becerro, M. A. et al.) 113–182 (Academic Press, Cambridge, 2012).
Google Scholar 

51.
van Duyl, F. C., Hegeman, J., Hoogstraten, A. & Maier, C. Dissolved carbon fixation by sponge–microbe consortia of deep water coral mounds in the northeastern Atlantic Ocean. Mar. Ecol. Prog. Ser. 358, 137–150 (2008).
ADS  Article  CAS  Google Scholar 

52.
van Duyl, F. C. et al. Dark CO2 fixation into phospholipid-derived fatty acids by the cold-water coral associated sponge Hymedesmia (Stylopus) coriacea (Tisler Reef, NE Skagerrak). Mar. Biol. Re. 16(1), 1–17 (2020).
Article  Google Scholar 

53.
Hoffmann, F. et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11(9), 2228–2243 (2009).
CAS  PubMed  Article  Google Scholar 

54.
Radax, R. et al. Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ. Microbiol. 14(5), 1308–1324 (2012).
CAS  PubMed  Article  Google Scholar 

55.
Landry, Z., Swan, B. K., Herndl, G. J., Stepanauskas, R. & Giovannoni, S. J. SAR202 genomes from the dark ocean predict pathways for the oxidation of recalcitrant dissolved organic matter. MBio 8(2), e00413-e417 (2017).
CAS  PubMed  PubMed Central  Article  Google Scholar 

56.
Kazanidis, G., van Oevelen, D., Veuger, B. & Witte, U. F. Unravelling the versatile feeding and metabolic strategies of the cold-water ecosystem engineer Spongosorites coralliophaga (Stephens, 1915). Deep Sea Res. Part I Oceanogr. Res. Pap. 141, 71–82 (2018).
ADS  CAS  Article  Google Scholar 

57.
Corredor, J. E., Wilkinson, C. R., Vicente, V. P., Morell, J. M. & Otero, E. Nitrate release by Caribbean reef sponges 1, 2. Limnol. Oceanogr. 33(1), 114–120 (1988).
ADS  CAS  Article  Google Scholar 

58.
Leys, S. P., Kahn, A. S., Fang, J. K. H., Kutti, T. & Bannister, R. J. Phagocytosis of microbial symbionts balances the carbon and nitrogen budget for the deep-water boreal sponge Geodia barretti. Limnol. Oceanogr. 63(1), 187–202 (2018).
ADS  CAS  Article  Google Scholar 

59.
Phillips, N. W. Role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bull. Mar. Sci. 35(3), 283–298 (1984).
Google Scholar 

60.
Haas, A. F. & Wild, C. Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat. Biol. 10(2), 131–138 (2010).
Article  Google Scholar 

61.
Nelson, C. E. et al. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 7(5), 962 (2013).
CAS  PubMed  PubMed Central  Article  Google Scholar 

62.
van Oevelen, D. et al. The cold-water coral community as hotspot of carbon cycling on continental margins: a food-web analysis from Rockall Bank (northeast Atlantic). Limnol. Oceanogr. 54(6), 1829–1844 (2009).
ADS  Article  Google Scholar 

63.
Vrede, K., Heldal, M., Norland, S. & Bratbak, G. Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl. Environ. Microbiol. 68(6), 2965–2971 (2002).
CAS  PubMed  PubMed Central  Article  Google Scholar 

64.
Hansell, D. A. & Carlson, C. A. Marine dissolved organic matter and the carbon cycle. Oceanography 14(4), 41–49 (2001).
Article  Google Scholar 

65.
Djerassi, C. & Lam, W. K. Phospholipid studies of marine organisms. Part 25. Sponge phospholipids. Accounts Chem. Res. 24(3), 69–75 (1991).
CAS  Article  Google Scholar 

66.
Alexander, B. E. et al. Cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems. PLoS ONE 9(10), e109486 https://doi.org/10.1371/journal.pone.0109486 (2014).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

67.
Bayer, K. et al. Microbial strategies for survival in the glass sponge Vazella pourtalesii. BioRxiv https://doi.org/10.1101/2020.05.28.122663 (2020).
Article  Google Scholar 

68.
Fuller, S. D. Diversity of marine sponges in the Northwest Atlantic. PhD dissertation, Dalhousie University, Halifax (2011).

69.
Tjensvoll, I., Kutti, T., Fosså, J. H. & Bannister, R. J. Rapid respiratory responses of the deep-water sponge Geodia barretti exposed to suspended sediments. Aquat. Biol. 19(1), 65–73 (2013).
Article  Google Scholar 

70.
Guillard, R. R. Culture of phytoplankton for feeding marine invertebrates. in Culture of Marine Invertebrate Animals. (eds Smith, W. L., Chanley, M. H.) 29–60. (Springer, Boston, MA, 1975).
Google Scholar 

71.
Miller, J.H. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory. (Cold Spring Harbor, NY 1972).

72.
Alexander, B. E. et al. Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage?. PeerJ 3, e820 (2015).
PubMed  PubMed Central  Article  CAS  Google Scholar 

73.
Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37(8), 911–917 (1959).
CAS  PubMed  Article  Google Scholar 

74.
Boschker, H. T. S. Linking microbial community structure and functioning: stable istope (13C) labeling in combination with PLFA analysis. in Molecular Microbial Ecology Manual, 2nd edition (eds. Kowalchuk, G. A., de Bruijn, F. J., Head, I. M., Akkermans, A. D. L., van Elsas, J. D.) 1673–1688 (Kluwer, Dordrecht, The Netherlands, 2004).
Google Scholar 

75.
de Kluijver, A. Fatty acid analysis sponges. protocols.io. https://doi.org/10.17504/protocols.io.bhnpj5dn (2020).

76.
Soetaert, K., Provoost, P., & van Rijswijk, P. RLims: R functions for Lab Analysis using GC-FID and GC-c-IRMS, NIOZ Yerseke, v1.03 (2015).

77.
Clarke, K. R. & Gorley, R. N. PRIMER v6: User Manual (Tutorial Plymouth, United Kingdom, 2006).
Google Scholar 

78.
Anderson, M. J., Gorley, R. N. & Clarke, K. R. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods (PRIMER-E. Plymouth, UK, 2008).
Google Scholar  More

1.
Early, R. et al. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 7, 1–9 (2016).
2.
Seebens, H. et al. Global rise in emerging alien species results from increased accessibility of new source pools. Proc. Natl Acad. Sci. USA 115, E2264–E2273 (2018).
CAS  PubMed  Article  Google Scholar 

3.
Seebens, H. et al. Global trade will accelerate plant invasions in emerging economies under climate change. Glob. Chang. Biol. 21, 4128–4140 (2015).
ADS  PubMed  Article  Google Scholar 

4.
Simberloff, D. et al. Impacts of biological invasions: what’s what and the way forward. Trends Ecol. Evol. 28, 58–66 (2013).
PubMed  Article  Google Scholar 

5.
Vilà, M. et al. How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front. Ecol. Environ. 8, 135–144 (2010).
Article  Google Scholar 

6.
Van Kleunen, M., Dawson, W., Schlaepfer, D., Jeschke, J. M. & Fischer, M. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol. Lett. 13, 947–958 (2010).
PubMed  Google Scholar 

7.
Enserink, M. Biological invaders sweep in. Science 285, 1834–1836 (1999).
CAS  Article  Google Scholar 

8.
Hulme, P. E. Phenotypic plasticity and plant invasions: is it all Jack? Funct. Ecol. 22, 3–7 (2008).
Article  Google Scholar 

9.
Murray, B. R., Thrall, P. H., Gill, A. M. & Nicotra, A. B. How plant life-history and ecological traits relate to species rarity and commonness at varying spatial scales. Austral Ecol. 27, 291–310 (2002).
Article  Google Scholar 

10.
Davidson, A. M., Jennions, M. & Nicotra, A. B. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol. Lett. 14, 419–431 (2011).
PubMed  Article  Google Scholar 

11.
Bazin, É., Mathé-Hubert, H., Facon, B., Carlier, J. & Ravigné, V. The effect of mating system on invasiveness: Some genetic load may be advantageous when invading new environments. Biol. Invasion. 16, 875–886 (2014).
Article  Google Scholar 

12.
Zheng, Y. et al. Are invasive plants more competitive than native conspecifics? Patterns vary with competitors. Sci. Rep. 5, 1–8 (2015).
Google Scholar 

13.
Callaway, R. M. & Aschehoug, E. T. Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290, 521–523 (2000).
ADS  CAS  PubMed  Article  Google Scholar 

14.
Guisan, A., Petitpierre, B., Broennimann, O., Daehler, C. & Kueffer, C. Unifying niche shift studies: insights from biological invasions. Trends Ecol. Evol. 29, 260–269 (2014).
PubMed  Article  Google Scholar 

15.
Gallagher, R. V., Beaumont, L. J., Hughes, L. & Leishman, M. R. Evidence for climatic niche and biome shifts between native and novel ranges in plant species introduced to Australia. J. Ecol. 98, 790–799 (2010).
Article  Google Scholar 

16.
Petitpierre, B. et al. Climatic niche shifts are rare among terrestrial plant invaders. Science 335, 1344–1348 (2012).
ADS  CAS  PubMed  Article  Google Scholar 

17.
Holway, D. A., Lach, L., Suarez, A. V., Tsutsui, N. D. & Case, T. J. The causes and consequences of ant invasions. Annu. Rev. Ecol. Syst. 33, 181–233 (2002).
Article  Google Scholar 

18.
Hölldobler, Bert, E. O. W. The Ants. (Havard University Press, 1990).

19.
Meurisse, N., Rassati, D., Hurley, B. P., Brockerhoff, E. G. & Haack, R. A. Common pathways by which non-native forest insects move internationally and domestically. J. Pest Sci. 92, 13–27 (2018).
Article  Google Scholar 

20.
Bertelsmeier, C., Luque, G. M., Hoffmann, B. D. & Courchamp, F. Worldwide ant invasions under climate change. Biodivers. Conserv. 24, 117–128 (2015).
Article  Google Scholar 

21.
Fitzpatrick, M. C., Weltzin, J. F., Sanders, N. J. & Dunn, R. R. The biogeography of prediction error: why does the introduced range of the fire ant over-predict its native range? Glob. Ecol. Biogeogr. 16, 24–33 (2007).
Article  Google Scholar 

22.
Bradshaw, C. J. A. et al. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 7, 1–8 (2016).

23.
Bertelsmeier, C., Ollier, S., Liebhold, A. & Keller, L. Recent human history governs global ant invasion dynamics. Nat. Ecol. Evol. 1, 0184 (2017).
PubMed  PubMed Central  Article  Google Scholar 

24.
Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).
PubMed  Article  Google Scholar 

25.
Essl, F. et al. Socioeconomic legacy yields an invasion debt. Proc. Natl Acad. Sci. USA 108, 203–207 (2011).
ADS  CAS  PubMed  Article  Google Scholar 

26.
Rouget, M. et al. Invasion debt-quantifying future biological invasions. Divers. Distrib. 22, 445–456 (2016).
Article  Google Scholar 

27.
Soberon, J. & Peterson, A. T. Interpretation of models of fundamental ecological niches and species’ distributional Areas. Biodivers. Inform. 2, 0–10 (2005).
Article  Google Scholar 

28.
Keane, R. M. & Crawley, M. J. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 (2002).
Article  Google Scholar 

29.
Shea, K. & Chesson, P. Community ecology theory as a framework for biological invasions. Trends Ecol. Evol. 163, 170–176 (2002).
Article  Google Scholar 

30.
Bocsi, T. et al. Plants’ native distributions do not reflect climatic tolerance. Divers. Distrib. 22, 615–624 (2016).
Article  Google Scholar 

31.
Bolnick, D. I. et al. Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc. R. Soc. B Biol. Sci. 277, 1789–1797 (2010).
Article  Google Scholar 

32.
Torres, U. et al. Using niche conservatism information to prioritize hotspots of invasion by non-native freshwater invertebrates in New Zealand. Divers. Distrib. 24, 1802–1815 (2018).
Article  Google Scholar 

33.
Blonder, B., Lamanna, C., Violle, C. & Enquist, B. J. The n-dimensional hypervolume. Glob. Ecol. Biogeogr. 23, 595–609 (2014).
Article  Google Scholar 

34.
Godefroid, M., Rasplus, J. Y. & Rossi, J. P. Is phylogeography helpful for invasive species risk assessment? The case study of the bark beetle genus Dendroctonus. Ecography 39, 1197–1209 (2016).
Article  Google Scholar 

35.
Bujan, J., Roeder, K. A., Yanoviak, S. P. & Kaspari, M. Seasonal plasticity of thermal tolerance in ants. Ecology 101, 1–6 (2020).
Article  Google Scholar 

36.
Bujan, J. & Kaspari, M. Nutrition modifies critical thermal maximum of a dominant canopy ant. J. Insect Physiol. 102, 1–6 (2017).
CAS  PubMed  Article  Google Scholar 

37.
Alexander, J. M. & Edwards, P. J. Limits to the niche and range margins of alien species. Oikos 119, 1377–1386 (2010).
Article  Google Scholar 

38.
Pearman, P. B., Guisan, A., Broennimann, O. & Randin, C. F. Niche dynamics in space and time. Trends Ecol. Evol. 23, 149–158 (2008).
PubMed  Article  Google Scholar 

39.
Tingley, R., Vallinoto, M., Sequeira, F. & Kearney, M. R. Realized niche shift during a global biological invasion. Proc. Natl Acad. Sci. USA 111, 10233–10238 (2014).
ADS  CAS  PubMed  Article  Google Scholar 

40.
Medley, K. A. Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Glob. Ecol. Biogeogr. 19, 122–133 (2010).
Article  Google Scholar 

41.
Kolbe, J. J. et al. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431, 177–181 (2004).
ADS  CAS  PubMed  Article  Google Scholar 

42.
Angetter, L. S., Lotters, S. & Rodder, D. Climate niche shift in invasive species: the case of the brown anole. Biol. J. Linn. Soc. 104, 943–954 (2011).
Article  Google Scholar 

43.
Colautti, R. I. & Lau, J. A. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol. Ecol. 24, 1999–2017 (2015).
PubMed  Article  Google Scholar 

44.
Bertelsmeier, C. & Keller, L. Bridgehead effects and role of adaptive evolution in invasive populations. Trends Ecol. Evol. 33, 527–534 (2018).
PubMed  Article  Google Scholar 

45.
Srivastava, V., Lafond, V. & Griess, V. C. Species distribution models (SDM): applications, benefits and challenges in invasive species management. CAB Rev. 14, 1–13 (2019).

46.
Pili, A. N., Tingley, R., Sy, E. Y., Diesmos, M. L. L. & Diesmos, A. C. Niche shifts and environmental non-equilibrium undermine the usefulness of ecological niche models for invasion risk assessments. Sci. Rep. 10, 1–18 (2020).
Article  CAS  Google Scholar 

47.
Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).
PubMed  PubMed Central  Article  Google Scholar 

48.
Kirchhof, S. et al. Thermoregulatory behavior and high thermal preference buffer impact of climate change in a Namib Desert lizard. Ecosphere 8, e02033 (2017).

49.
Woods, H. A., Dillon, M. E. & Pincebourde, S. The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change. J. Therm. Biol. 54, 86–97 (2015).
PubMed  Article  Google Scholar 

50.
Chapman, D. S., Scalone, R., Štefanić, E. & Bullock, J. M. Mechanistic species distribution modeling reveals a niche shift during invasion. Ecology 98, 1671–1680 (2017).
PubMed  Article  Google Scholar 

51.
Janicki, J., Narula, N., Ziegler, M., Guénard, B. & Economo, E. P. Visualizing and interacting with large-volume biodiversity data using client-server web-mapping applications: The design and implementation of antmaps.org. Ecol. Inform. 32, 185–193 (2016).
Article  Google Scholar 

52.
Guénard, B., Weiser, M. D., Gómez, K., Narula, N. & Economo, E. P. The Global Ant Biodiversity Informatics (GABI) database: Synthesizing data on the geographic distribution of ant species (Hymenoptera: Formicidae). Myrmecological N. 24, 83–89 (2017).
Google Scholar 

53.
Pearson, R. G., Raxworthy, C. J., Nakamura, M. & Townsend Peterson, A. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34, 102–117 (2007).
Article  Google Scholar 

54.
Pagad, S., Genovesi, P., Carnevali, L., Scalera, R. & Clout, M. IUCN SSC invasive species specialist group: Invasive alien species information management supporting practitioners, policy makers and decision takers. Manag. Biol. Invasion. 6, 127–135 (2015).
Article  Google Scholar 

55.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Article  Google Scholar 

56.
Dray, S. & Dufour, A.-B. The ade4 Package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).

57.
Broennimann, O. et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr. 21, 481–497 (2012).
Article  Google Scholar 

58.
Di Cola, V. et al. ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography 40, 774–787 (2017).
Article  Google Scholar 

59.
Schoener, T. W. The Anolis Lizards of Bimini: resource partitioning in a complex fauna were invaded by anoline lizards. Ecol. Soc. Am. 49, 704–726 (1968).
Google Scholar 

60.
Warren, D. L., Glor, R. E. & Turelli, M. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62, 2868–2883 (2008).
PubMed  Article  Google Scholar 

61.
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. 57, 289–300 (1995).
MathSciNet  MATH  Google Scholar 

62.
Bates, O. K., Ollier, S. & Bertelsmeier, C. Smaller climatic niche shifts in invasive than non-invasive alien ant species. GitHub. https://doi.org/10.5281/zenodo.4041296 (2020).

63.
Team, R. C. R.: A Language and Environment for Statistical Computing. (2019). More

1.
Trathan, P. N. & Hill, S. L. in Biology and Ecology of Antarctic krill (ed. Siegel, V.) 321–350 (Springer, 2016).
2.
Atkinson, A. et al. A re-appraisal of the total biomass and annual production of Antarctic krill. Deep Sea Res. Pt. 1. 56, 727–740 (2009).
Article  Google Scholar 

3.
Bar-On, Y. N., Philips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).
CAS  Article  Google Scholar 

4.
Atkinson, A. et al. Sardine cycles, krill declines, and locust plagues: revisiting ‘wasp-waist’ food webs. Trends Ecol. Evol. 29, 309–316 (2014).
Article  Google Scholar 

5.
Cavan, E. L. et al. The importance of Antarctic krill in biogeochemical cycles. Nat. Commun. 10, 4742 (2019).
CAS  Article  Google Scholar 

6.
Nicol, S. et al. Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish. Fish 11, 203–209 (2010).
Article  Google Scholar 

7.
Schmidt, K. et al. Zooplankton gut passage mobilizes lithogenic iron for ocean productivity. Curr. Biol. 26, 2667–2673 (2016).
CAS  Article  Google Scholar 

8.
Nicol, S. & Foster, J. in Biology and Ecology of Antarctic krill 387–421 (Springer, 2016).

9.
Kawaguchi, S & Nicol, S. in Fisheries and Aquaculture Vol. 9. (eds Lovrich, G. & Thiel, M.) 137–158, https://doi.org/10.1093/oso/9780190865627.003.0006. (Oxford University Press, 2020).

10.
Turner, J. & Overland, J. Contrasting climate change in the two polar regions. Polar Res. 26, 146–164 (2009).
Article  Google Scholar 

11.
Rogers, A. D. et al. Antarctic futures: an assessment of climate-driven changes in ecosystem structure, function, and service provisioning in the southern ocean. Annul Rev. Mar. Sci 12, 87–120 (2019).
Article  Google Scholar 

12.
Kawaguchi, S., Nicol, S. & Press, A. J. Direct effects of climate change on the Antarctic krill fishery. Fisheries Manag. Ecol. 16, 424–427 (2009).
Article  Google Scholar 

13.
Trathan, P. N. et al. Krill biomass in the Atlantic. Nature 367, 201–202 (1995).
Article  Google Scholar 

14.
Constable, A. J. & de la Mare, W. K. A generalised yield model for evaluating the yield and the long-term status of fish stocks under conditions of uncertainty. CCAMLR Sci. 3, 31–54 (1996).
Google Scholar 

15.
Hill, S. L. et al. Is current management of the Antarctic krill fishery in the Atlantic sector of the Southern Ocean precautionary? CCAMLR Sci. 23, 31–51 (2016).
Google Scholar 

16.
Hewitt, R. P. et al. Options for allocating the precautionary catch limit of krill among small-scale management units in the Scotia Sea. CCAMLR Sci 11, 81–97 (2004).
Google Scholar 

17.
Watters, G. M., Hill, S. L., Hinke, J. T., Matthews, J. & Reid, K. Decision-making for ecosystem-based management: evaluating options for a krill fishery with an ecosystem dynamics model. Ecol. Appl. 23, 710–725 (2013).
CAS  Article  Google Scholar 

18.
Trathan, P. N. et al. Managing fishery development in sensitive ecosystems: identifying penguin habitat use to direct management in Antarctica. Ecosphere 9, e02392 (2018).
Article  Google Scholar 

19.
Watters, G. M., Hinke, J. T. & Reiss, C. Long-term observations from Antarctica demonstrate that mismatched scales of fisheries management and predator-prey interaction lead to erroneous conclusions about precaution. Sci. Rep. 10, 2314 (2020).
CAS  Article  Google Scholar 

20.
Reiss, C. S., Cossio, A. M., Loeb, V. & Demer, D. A. Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES J. Mar. Sci. 65, 497–508 (2008).
Article  Google Scholar 

21.
Fielding, S. et al. Interannual variability in Antarctic krill (Euphausia superba) density at South Georgia, Southern Ocean: 1997–2013. ICES J. Mar. Sci. 71, 2578–2588 (2014).
Article  Google Scholar 

22.
Brierley, A. S. & Reid, K. Krill and the diversity of science and society: An introduction to the Third International Symposium on Krill. J. Crust. Biol. 38, 651–655 (2018).
Google Scholar 

23.
Report of the Thirty-Sixth Meeting of the Scientific Committee of the Commission for the Conservation of Antarctic Marine Living Resources. (CCAMLR, Hobart, Australia, 2017).

24.
SC-CCAMLR Report of the thirty-eight Meeting of the Scientific Committee, of the Commission for the Conservation of Antarctic Marine Living Resources. (CCAMLR Hobart, Australia, 2019).

25.
Spiridonov, V. Spatial and temporal variability in reproductive timing of Antarctic krill (Euphausia superba Dana). Polar Biol. 15, 161–174 (1995).
Article  Google Scholar 

26.
Siegel, V. Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biol. 29, 1–22 (2005).
Article  Google Scholar 

27.
Schmidt, K., Atkinson, A., Venables, H. & Pond, D. W. Early spawning of Antarctic krill in the Scotia Sea is fueled by ‘superfluous’ feeding on non-ice associated phytoplankton blooms. Deep Sea Res. II 59, 159–172 (2012).
Article  Google Scholar 

28.
Ross, R. B. & Quetin, L. B. Energetic cost to develop to the first feeding stage of Euphausia superba Dana and the effect of delays in food availability. J. Exp. Mar. Biol. Ecol. 133, 103–127 (1989).
Article  Google Scholar 

29.
Meyer, B. et al. The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill. Nat. Ecol. Evol 1, 1853–1861 (2017).
Article  Google Scholar 

30.
Brierley, A. S., Demer, D. A., Hewitt, R. P. & Watkins, J. L. Concordance of inter-annual fluctuations in densities of krill around South Georgia and Elephant Islands: biological evidence of same year teleconnections across the Scotia Sea. Mar. Biol. 134, 675–681 (1999).
Article  Google Scholar 

31.
Reiss, C. S. in Biology and Ecology of Antarctic krill 101–144 (Springer, 2016).

32.
Quetin, L. B., Ross, R. M., Fritsen, C. H. & Vernet, M. Ecological responses of Antarctic krill to environmental variability: can we predict the future? Ant. Sci. 19, 253–266 (2007).
Article  Google Scholar 

33.
Saba, G. K. et al. Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula. Nat. Commun. 5, 4318 (2014).
CAS  Article  Google Scholar 

34.
Murphy, E. J. et al. Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centered food web. Phil. Trans. R. Soc. B 362, 113–148 (2007).
CAS  Article  Google Scholar 

35.
Kinzey, D. et al. Selectivity and two biomass measures in an age-based assessment of Antarctic krill (Euphausia superba). Fish. Res. 168, 72–84 (2015).
Article  Google Scholar 

36.
Siegel, V. & Loeb, V. et al. Recruitment of Antarctic krill (Euphausia superba) and possible causes for its variability. Mar. Ecol. Prog. Ser. 123, 45–56 (1995).
Article  Google Scholar 

37.
Loeb, V. J. & Santora, J. A. Climate variability and spatiotemporal dynamics of five Southern Ocean krill species. Prog. Oceanogr. 134, 93–122 (2015).
Article  Google Scholar 

38.
Atkinson, A. et al. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat. Clim. Change 9, 142–147 (2019).
Article  Google Scholar 

39.
Thorpe, S. E., Tarling, G. A. & Murphy, E. J. Circumpolar patterns in Antarctic krill larval recruitment: an environmentally driven model. Mar. Ecol. Prog. Ser. 613, 77–96 (2019).
Article  Google Scholar 

40.
Ryabov, A. B. et al. Competition-induced starvation drives large-scale population cycles in Antarctic krill. Nat. Ecol. Evol 1, 1–8 (2017).
Article  Google Scholar 

41.
Makarov, R. R. & Menshenina, L. L. On the distribution of euphausiid larvae in the Antarctic waters. Okeanologija Akademija Nauk SSSR. Okeanograficeskaja Komissija, Moskva 29, 825–831 (1989).
Google Scholar 

42.
Perry, F. A. et al. Habitat partitioning in Antarctic krill: spawning hotspots and nursery areas. PLoS ONE 14, e0219325 (2019).
CAS  Article  Google Scholar 

43.
Siegel, V & Watkins, J. N. in Biology and Ecology of Antarctic krill 21–100 (Springer, 2016).

44.
Hofmann, E. E. & Hüsrevoğlu, Y. S. A circumpolar modelling study of habitat control of Antarctic krill (Euphausia superba) reproductive success. Deep-Sea Res II 50, 3121–3142 (2003).
Article  Google Scholar 

45.
King, M. Fisheries Biology, Assessment and Management 341 (Fishing News Books, Blackwell Science, Oxford, 1995).

46.
Rombolá, E. R. et al. Variability of euphausiid larvae densities during the 2011, 2012, and 2014 summer seasons in the Atlantic sector of the Antarctic. Polar Sci. 19, 86–93 (2019).
Article  Google Scholar 

47.
Conroy, J. A., Reiss, C. S., Gleiber, M. R. & Steinberg, D. K. Linking Antarctic krill larval supply and recruitment along the Antarctic Peninsula. Integr. Comp. Biol. https://doi.org/10.1093/icb/icaa111 (2020).
Article  Google Scholar 

48.
Siegel, V. et al. Distribution and abundance of Antarctic krill (Euphausia superba) along the Antarctic Peninsula. Deep Sea Res. I 77, 63–74 (2013).
Article  Google Scholar 

49.
Lumpkin, R. & Centurioni, L. Global Drifter Program quality-controlled 6-hour interpolated data from ocean surface drifting buoys. NOAA National Centers for Environmental Information. Dataset. https://doi.org/10.25921/7ntx-z961 (2019)

50.
Siegel, V. in Antarctic Ocean and Resources Variability 219–230 (Springer, 1988).

51.
Trathan, P. N. et al. Spatial variability of Antarctic krill in relation to mesoscale hydrography. Mar. Ecol. Prog. Ser. 98, 61–71 (1993).
Article  Google Scholar 

52.
Jazdzewski, K. et al. Biological and populational studies on krill near South Shetland Islands, Scotia Sea and South Georgia in the summer 1976. Polskie Archiwum Hydrobiologii 25, 607–631 (1978).
Google Scholar 

53.
Reiss, C. S. et al. Overwinter habitat selection by Antarctic krill under varying sea-ice conditions: implications for top predators and fishery management. Mar. Ecol. Prog. Ser. 568, 1–16 (2017).
CAS  Article  Google Scholar 

54.
Piñones, A. et al. Modeling the remote and local connectivity of Antarctic krill populations along the western Antarctic Peninsula. Mar. Ecol. Prog. Ser. 481, 69–92 (2013).
Article  Google Scholar 

55.
Taki, K., Hayashi, T. & Naganobu, M. Characteristics of seasonal variation in diurnal vertical migration and aggregation of Antarctic krill (Euphausia superba) in the Scotia Sea, using Japanese fishery data. CCAMLR Sci. 12, 163–172 (2005).
Google Scholar 

56.
Barlow, K. E. et al. Are penguins and seals in competition for Antarctic krill at South Georgia? Mar. Biol. 140, 205–213 (2002).
Article  Google Scholar 

57.
Reid, K., Trathan, P. N., Croxall, J. P. & Hill, H. J. Krill caught by predators and nets: differences between species and techniques. Mar. Ecol. Prog. Ser. 140, 13–20 (1996).
Article  Google Scholar 

58.
Jackson, J. A. et al. Global diversity and oceanic divergence of humpback whales (Megaptera novaeangliae). Proc. Roy. Soc. B-Biol. Sci 281, 20133222 (2014).
Article  Google Scholar 

59.
Herr, H. et al. Horizontal niche partitioning of humpback and fin whales around the West Antarctic Peninsula: evidence from a concurrent whale and krill survey. Polar Biol. 39, 799–818 (2016).
Article  Google Scholar 

60.
Viquerat, S. & Herr, H. Mid-summer abundance estimates of fin whales Balaenoptera physalus around the South Orkney Islands and Elephant Island. ESR 32, 515–524 (2017).
Article  Google Scholar 

61.
Zerbini, A. N. et al. Assessing the recovery of an Antarctic predator form historical exploitation. Roy. Soc. Open Sci 6, 190368 (2019).
Article  Google Scholar 

62.
Reid, K. et al. Widening the net: spatio-temporal variability in the krill population structure across the Scotia Sea. Deep-Sea Res. II 51, 1275–1287 (2004).
Article  Google Scholar 

63.
Atkinson, A. et al. Oceanic circumpolar habitats of Antarctic krill. Mar. Ecol. Prog. Ser. 362, 1–23 (2008).
CAS  Article  Google Scholar 

64.
Hill, S. L., Trathan, P. H. & Agnew, D. J. The risk to fishery performance associated with spatially resolved management of Antarctic krill (Euphausia superba) harvesting. ICES J. Mar. Sci 66, 2148–2154 (2009).
Article  Google Scholar 

65.
Tarling, G. A., Ward, P. & Thorpe, S. E. Spatial distributions of Southern Ocean mesozooplankton communities have been resilient to long-term surface warming. Global Change Biol. https://doi.org/10.1111/gcb.13834 (2017).

66.
Stammerjohn, S. S., Massom, R. A., Rind, D. & Martinson, D. G. Regions of rapid sea ice change: an inter-hemispheric seasonal comparison. Geophys. Res. Lett. 39, L06501 (2012).
Article  Google Scholar 

67.
Henley, S. F. et al. Variability and change in the west Antarctic Peninsula marine system: research priorities and opportunities. Prog. Oceanogr. https://doi.org/10.1016/j.pocean.2019.03.003 (2019).

68.
Turner, J. et al. Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature. 535, 411–415 (2016).
CAS  Article  Google Scholar 

69.
Swart, N. C. & Fyfe, J. C. Observed and simulated changes in the Southern Hemisphere surface westerly wind-stress. Geophys. Res. Letters 39, L16711 (2012).
Article  Google Scholar 

70.
Datwyler, C. et al. Teleconnection stationality, variability and trends of the Southern Annular Mode (SAM) during the last millennium. Clim. Dyn. 51, 2321–2339 (2017).
Article  Google Scholar 

71.
Stammerjohn, S. E. et al. Trends in Antarctic annual sea ice retreat and advance and their relation to El Niño–Southern Oscillation and Southern Annular Mode variability. J. Geophys. Res. 113, C03S90 (2008).
Article  Google Scholar 

72.
SC-CCAMLR Report of the twenty-ninth Meeting of the Scientific Committee, of the Commission for the Conservation of Antarctic Marine Living Resources. (CCAMLR Hobart, Australia, 2010).

73.
Cox, M. J. et al. No evidence for a decline in the density of Antarctic krill Euphausia superba Dana, 1850, in the Southwest Atlantic sector between 1976 and 2016. J. Crust. Biol. 38, 656–661 (2018).
Google Scholar 

74.
Loeb, V. et al. Effects of sea ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).
CAS  Article  Google Scholar 

75.
Trivelpiece, W. Z. et al. Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc. Natl Acad. Sci. USA 108, 7625–7628 (2011).
CAS  Article  Google Scholar 

76.
Huang, T. et al. Relative changes in krill abundanceiInferred from Antarctic Fur Seal. PLoS ONE 6, e27331 (2011).
CAS  Article  Google Scholar 

77.
Atkinson, A., Siegel, V., Pakhomov, E. A. & Rothery, P. Long term decline in krill stock and increase in salps within the Southern Ocean. Nature 432, 100–103 (2004).
CAS  Article  Google Scholar 

78.
Forcada, J. & Hoffman, J. I. Climate change selects for heterozygosity in a declining fur seal population. Nature 511, 462–465 (2014).
CAS  Article  Google Scholar 

79.
McMahon, K. W. et al. Divergent trophic responses of sympatric penguin species to historic anthropogenic exploitation and recent climate change. Proc. Natl Acad Sci. USA 116, 25721–25727 (2019).
CAS  Article  Google Scholar 

80.
Hill, S. L., Atkinson, A., Pakhomov, E. A. & Siegel, V. Evidence for a decline in the population density of Antarctic krill Euphausia superba Dana 1850, still stands: A comment on Cox et al. J. Crust. Biol 39, 316–322 (2019).
Article  Google Scholar 

81.
Cox, M. J. et al. Clarifying trends in the density of Antarctic krill Euphausia superba Dana, 1850 in the South Atlantic. A response to Hill et al. J. Crust. Biol. 39, 323–327 (2019).
Article  Google Scholar 

82.
Hill, S. L. et al. Reference points for predators will progress ecosystem‐based management of fisheries. Fish. Fish. 21, 368–378 (2020).
Article  Google Scholar 

83.
Fuentes, V. et al. Glacial melting: an overlooked threat to Antarctic krill. Sci. Reps 6, 27234 (2016).
CAS  Article  Google Scholar 

84.
Flores et al. The response of Antarctic krill to climate change: Implications for management and research priorities. Mar. Ecol. Prog. Ser. 458, 1–19 (2012).
Article  Google Scholar 

85.
Ross, R. M. et al. Palmer LTER: Patterns of distribution of five dominant zooplankton species in the epipelagic zone west of the Antarctic Peninsula, 1993–2004. Deep Sea Res. II 55, 2086–2105 (2008).
Article  Google Scholar 

86.
Loeb, V. J. et al. ENSO and variability of the Antarctic Peninsula pelagic marine ecosystem. Ant. Sci. 21, 135–148 (2009).
Article  Google Scholar 

87.
Beaugrand, G. & Kirby, R. R. How do marine pelagic species respond to climate change? Theories and observations. Annu. Rev. Mar. Sci. 10, 169–197 (2018).
Article  Google Scholar 

88.
Tarling, G. A. & Thorpe, S. E. Oceanic swarms of Antarctic krill perform satiation sinking. Proc. R. Soc. B 284, 20172015 (2017).
Article  CAS  Google Scholar 

89.
Hill, S. L., Phillips, T. & Atkinson, A. Potential climate change effects on the habitat of Antarctic krill in the Weddell Quadrant of the Southern Ocean. PLoS ONE 8, e72246 (2013).
CAS  Article  Google Scholar 

90.
Piñones, A. & Fedorov, A. V. Projected changes of Antarctic krill habitat by the end of the 21st century. Geophys. Res. Lett. 43, 8580–8589 (2016).
Article  Google Scholar 

91.
Murphy, E. J. et al. Restricted regions of enhanced growth of Antarctic krill in the circumpolar Southern Ocean. Sci. Reps 7, 6963 (2017).
Article  CAS  Google Scholar 

92.
Atkinson, A. et al. Natural growth rates in Antarctic krill (Euphausia superba): II. Predictive models based on food, temperature, body length, sex, and maturity stage. Limnol. Oceanogr. 51, 973–987 (2006).
Article  Google Scholar 

93.
Kawaguchi, S. et al. Risk maps for Antarctic krill under projected Southern Ocean acidification. Nat. Clim. Change 3, 343–347 (2013).
Article  CAS  Google Scholar 

94.
Kawaguchi, S. & Nicol, S. Learning about Antarctic krill from the fishery. Ant. Sci. 19, 219–230 (2007).
Article  Google Scholar 

95.
Warner, A. J., Hays, G. C. & Hays, G. Sampling by the Continuous Plankton Recorder survey. Prog. Oceanogr. 34, 237–256 (1994).
Article  Google Scholar 

96.
Petersen, W. FerryBox systems: State-of-the-art in Europe and future development. J. Mar. Syst. 140 A, 4–12 (2014).
Article  Google Scholar 

97.
Brierley, A. S. et al. Use of moored acoustic instruments to measure short-term variability in abundance of Antarctic krill. Limnol. Oceanogr.: Methods 4, 18–29 (2006).
Article  Google Scholar 

98.
Guihen, D. et al. An assessment of the use of ocean gliders to undertake acoustic measurements of zooplankton: the distribution and density of Antarctic krill (Euphausia superba) in the Weddell Sea. Limnol. Oceanogr.: Methods 12, 373–389 (2014).
Article  Google Scholar 

99.
Meinig, C. et al. Public private partnerships to advance regional ocean observing capabilities: A Saildrone and NOAA-PMEL case study and future considerations to expand to global scale observing. Front. Mar. Sci. 6, 448 (2019).
Article  Google Scholar 

100.
Park, Y. H. & Durand, I. Altimetry-derived Antarctic circumpolar current fronts. SEANOE. https://doi.org/10.17882/59800 (2019).

101.
Park, Y.-H. et al. Observations of the Antarctic Circumpolar Current over the Udintsev Fracture Zone, the narrowest choke point in the Southern Ocean. J. Geophys. Res.: Oceans. 124 https://doi.org/10.1029/2019JC015024 (2019)

102.
Ikeda, T. Development of the larvae of the Antarctic krill (Euphausia superba Dana) observed in the laboratory. J. Exp. Mar. Biol. Ecol. 75, 107–117 (1984).
Article  Google Scholar 

103.
Tarling, G. A. et al. Growth and shrinkage in Antarctic krill Euphausia superba is sex-dependent. Mar. Ecol. Prog. Ser. 547, 61–78 (2016).
Article  Google Scholar 

104.
Guinet, C. et al. Calibration procedures and first dataset of Southern Ocean chlorophyll a profiles collected by elephant seals equipped with a newly developed CTD-fluorescence tags. Earth Syst. Sci. Data 5, 15–29 (2013).
Article  Google Scholar 

105.
Thiebot, J-B et al. Jellyfish and other gelata as food for four penguin species—insights from predator-borne videos. Front. Ecol. Environ. https://doi.org/10.1002/fee.1529 (2017).

106.
Watanabe, Y. Y. & Takahashi, A. Linking animal-borne video to accelerometers reveals prey capture variability. Proc Natl Acad. Sci. USA 10, 2199–2204 (2013).
Article  Google Scholar  More

1.
Fu, B. et al. Three Gorges Project: efforts and challenges for the environment. Prog. Phys. Geog. 34, 741–754 (2010).
Article  Google Scholar 
2.
Yuan, X. et al. The littoral zone in the Three Gorges Reservoir, China: challenges and opportunities. Environ. Sci. Pollut. R. 20, 7092–7102 (2013).
Article  Google Scholar 

3.
Xu, X., Tan, Y. & Yang, G. Environmental impact assessments of the Three Gorges Project in China: issues and interventions. Earth Sci. Rev. 124, 115–125 (2013).
ADS  Article  Google Scholar 

4.
Zhang, Q. & Lou, Z. The environmental changes and mitigation actions in the Three Gorges Reservoir region China. Environ. Sci. Policy 14, 1132–1138 (2011).
Article  Google Scholar 

5.
Huang, Y. et al. Nutrient estimation by HJ-1 satellite imagery of Xiangxi Bay, Three Gorges Reservoir China. Environ. Earth Sci. 75, 633 (2016).
Article  CAS  Google Scholar 

6.
Willison, J. H. M., Li, R. & Yuan, X. Conservation and ecofriendly utilization of wetlands associated with the Three Gorges Reservoir. Environ. Sci. Pollut. R. 20, 6907–6916 (2013).
Article  Google Scholar 

7.
Liu, L., Liu, D., Johnson, D. M., Yi, Z. & Huang, Y. Effects of vertical mixing on phytoplankton blooms in Xiangxi Bay of Three Gorges Reservoir: implications for management. Water Res. 46, 2121–2130 (2012).
CAS  PubMed  Article  PubMed Central  Google Scholar 

8.
Ren, C., Wang, L., Zheng, B., Qian, J. & Ton, H. Ten-year change of total phosphorous pollution in the Min River, an upstream tributary of the Three Gorges Reservoir. Environ. Earth Sci. 75, 1015 (2016).
Article  CAS  Google Scholar 

9.
Li, C., Zhong, Z., Geng, Y. & Schneider, R. Comparative studies on physiological and biochemical adaptation of Taxodium distichum and Taxodium ascendens seedlings to different soil water regimes. Plant Soil. 329, 481–494 (2010).
CAS  Article  Google Scholar 

10.
Schoonover, J. E., Williard, K. W., Zaczek, J. J., Mangun, J. C. & Carver, A. D. Agricultural sedmient reduction by giant cane and forests riparian buffers. Water Air Soil Poll. 169, 303–315 (2006).
ADS  CAS  Article  Google Scholar 

11.
Wang, C., Li, C., Wei, H., Xie, Y. & Han, W. Effects of long-term periodic submergence on photosynthesis and growth of Taxodium distichum and Taxodium ascendens saplings in the hydro-fluctuation zone of the Three Gorges Reservoir of China. PLoS ONE 11, e162867 (2016).
Google Scholar 

12.
Yang, F., Wang, Y. & Chan, Z. Perspectives on screening winter-flood-tolerant woody species in the riparian protection forests of the three gorges reservoir. PLoS ONE 9, e108725 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

13.
Ye, C., Cheng, X., Zhang, Y., Wang, Z. & Zhang, Q. Soil nitrogen dynamics following short-term revegetation in the water level fluctuation zone of the Three Gorges Reservoir China. Ecol. Eng. 38, 37–44 (2012).
Article  Google Scholar 

14.
Capon, S. J. et al. Riparian ecosystems in the 21st century: hotspots for climate change adaptation?. Ecosystems 16, 359–381 (2013).
Article  Google Scholar 

15.
Gregory, S. V., Swanson, F. J., McKee, W. A. & Cummins, K. W. An ecosystem perspective of riparian zones. Bioscience 41, 540–551 (1991).
Article  Google Scholar 

16.
Zhang, M. et al. Leaf litter traits predominantly control litter decomposition in streams worldwide. Glob. Ecol. Biogeogr. 28, 1469–1486 (2019).
Article  Google Scholar 

17.
Ferreira, V., Encalada, A. C. & Graça, M. A. S. Effects of litter diversity on decomposition and biological colonization of submerged litter in temperate and tropical streams. Freshw. Sci. 31, 945–962 (2012).
Article  Google Scholar 

18.
Jabiol, J. & Chauvet, E. Fungi are involved in the effects of litter mixtures on consumption by shredders. Freshw. Biol. 57, 1667–1677 (2012).
Article  Google Scholar 

19.
Yang, Z., Liu, D., Ji, D. & Xiao, S. Influence of the impounding process of the Three Gorges Reservoir up to water level 172.5 m on water eutrophication in the Xiangxi Bay. Sci. China Technol. Sci. 53, 1114–1125 (2010).
ADS  CAS  Article  Google Scholar 

20.
Berglund, S. L. & Ågren, G. I. When will litter mixtures decompose faster or slower than individual litters? A model for two litters. Oikos 121, 1112–1120 (2012).
Article  Google Scholar 

21.
De Marco, A., Meola, A., Maisto, G., Giordano, M. & Virzo De Santo, A. Non-additive effects of litter mixtures on decomposition of leaf litters in a Mediterranean maquis. Plant Soil 344, 305–317 (2011).
CAS  Article  Google Scholar 

22.
Gartner, T. B. & Cardon, Z. G. Decomposition dynamics in mixed-species leaf litter. Oikos 104, 230–246 (2004).
Article  Google Scholar 

23.
Gessner, M. O. et al. Diversity meets decomposition. Trends Ecol. Evol. 25, 372–380 (2010).
PubMed  Article  Google Scholar 

24.
Schimel, J. P. & Hättenschwiler, S. Nitrogen transfer between decomposing leaves of different N status. Soil Biol. Biochem. 39, 1428–1436 (2007).
CAS  Article  Google Scholar 

25.
Lecerf, A. et al. Incubation time, functional litter diversity, and habitat characteristics predict litter-mixing effects on decomposition. Ecology 92, 160–169 (2011).
Article  Google Scholar 

26.
Wu, D., Li, T. & Wan, S. Time and litter species composition affect litter-mixing effects on decomposition rates. Plant Soil. 371, 355–366 (2013).
CAS  Article  Google Scholar 

27.
Swan, C. M., Healey, B. & Richardson, D. C. The role of native riparian tree species in decomposition of invasive tree of heaven (Ailanthus altissima) leaf litter in an urban stream. Ecoscience 15, 27–35 (2008).
Article  Google Scholar 

28.
Leroy, C. J. & Marks, J. C. Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshw. Biol. 51, 605–617 (2006).
Article  Google Scholar 

29.
Xie, Y., Xie, Y., Hu, C., Chen, X. & Li, F. Interaction between litter quality and simulated water depth on decomposition of two emergent macrophytes. J. Limnol. 75, 36–43 (2015).
Google Scholar 

30.
Sun, Z., Mou, X. & Liu, J. S. Effects of flooding regimes on the decomposition and nutrient dynamics of Calamagrostis angustifolia litter in the Sanjiang Plain of China. Environ. Earth Sci. 66, 2235–2246 (2012).
Article  Google Scholar 

31.
Wang, C., Xie, Y., Ren, Q. & Li, C. Leaf decomposition and nutrient release of three tree species in the hydro-fluctuation zone of the Three Gorges Dam Reservoir China. Environ. Sci. Pollut. R. 25, 23261–23275 (2018).
CAS  Article  Google Scholar 

32.
Xiao, L., Zhu, B., Nsenga Kumvimba, M. & Jiang, S. Plant soaking decomposition as well as nitrogen and phosphorous release in the water-level fluctuation zone of the Three Gorges Reservoir. Sci. Total Environ. 592, 527–534 (2017).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

33.
Djukic, I. et al. Early stage litter decomposition across biomes. Sci. Total Environ. 628–629, 1369–1394 (2018).
ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

34.
Bray, S. R., Kitajima, K. & Mack, M. C. Temporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate. Soil Biol. Biochem. 49, 30–37 (2012).
CAS  Article  Google Scholar 

35.
Graça, M. A. S. et al. A conceptual model of litter breakdown in low order streams. Int. Rev. Hydrobiol. 100, 1–12 (2015).
Article  CAS  Google Scholar 

36.
Lecerf, A., Risnoveanu, G., Popescu, C., Gessner, M. O. & Chauvet, E. Decomposition of diverse litter mixtures in streams. Ecology 88, 219–227 (2007).
Article  Google Scholar 

37.
Martínez, A., Larrañaga, A., Pérez, J., Descals, E. & Pozo, J. Temperature affects leaf litter decomposition in low-order forest streams: field and microcosm approaches. FEMS Microbiol. Ecol. 87, 257–267 (2014).
PubMed  Article  CAS  PubMed Central  Google Scholar 

38.
Kelley, R. H. & Jack, J. D. Leaf litter decomposition in an ephemeral karst lake (Chaney Lake, Kentucky, U.S.A). Hydrobiologia 482, 41–47 (2002).
Article  Google Scholar 

39.
Austin, A. T. & Vitousek, P. M. Precipitation, decomposition and litter decomposability of Metrosideros polymorpha in native forests on Hawai’i. J. Ecol. 88, 138–139 (2000).
Article  Google Scholar 

40.
Taylor, A. R., Schröter, D., Pflug, A. & Wolters, V. Response of different decomposer communities to the manipulation of moisture availability: potential effects of changing precipitation patterns. Glob. Change Biol. 10, 1313–1324 (2004).
ADS  Article  Google Scholar 

41.
Xie, Y., Xie, Y., Xiao, H., Chen, X. & Li, F. Controls on litter decomposition of emergent macrophyte in dongting lake wetlands. Ecosystems 20, 1383–1389 (2017).
CAS  Article  Google Scholar 

42.
Fernandes, I., Seena, S., Pascoal, C. & Cássio, F. Elevated temperature may intensify the positive effects of nutrients on microbial decomposition in streams. Freshw. Biol. 59, 2390–2399 (2014).
CAS  Article  Google Scholar 

43.
Ferreira, V. & Chauvet, E. Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Glob. Change Biol. 17, 551–564 (2011).
ADS  Article  Google Scholar 

44.
Liu, C. et al. Mixing litter from deciduous and evergreen trees enhances decomposition in a subtropical karst forest in southwestern China. Soil Biol. Biochem. 101, 44–54 (2016).
Article  CAS  Google Scholar 

45.
Wu, F. et al. Admixture of alder (Alnus formosana) litter can improve the decomposition of eucalyptus (Eucalyptus grandis) litter. Soil Biol. Biochem. 73, 115–121 (2014).
CAS  Article  Google Scholar 

46.
Kominoski, J. S. et al. Nonadditive effects of leaf litter species diversity on breakdown dynamics in a Detritus-based stream. Ecology 88, 1167–1176 (2007).
CAS  PubMed  Article  PubMed Central  Google Scholar 

47.
Sanpera-Calbet, I. S. I. S., Lecerf, A. & Chauvet, E. Leaf diversity influences in-stream litter decomposition through effects on shredders. Freshw. Biol. 54, 1671–1682 (2009).
Article  Google Scholar 

48.
Ostrofsky, M. L. A comment on the use of exponential decay models to test nonadditive processing hypotheses in multispecies mixtures of litter. J. N. Am. Benthol. Soc. 26, 23–27 (2007).
Article  Google Scholar 

49.
Zanne, A. E. et al. A deteriorating state of affairs: how endogenous and exogenous factors determine plant decay rates. J. Ecol. 103, 1421–1431 (2015).
CAS  Article  Google Scholar 

50.
Hieber, M. & Gessner, M. O. Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83, 1026–1038 (2002).
Article  Google Scholar 

51.
Schindler, M. H. & Gessner, M. O. Functional leaf traits and biodiversity effects on litter decomposition in a stream. Ecology 90, 1641–1649 (2009).
PubMed  Article  Google Scholar 

52.
Gessner, M. O. & Chauvet, E. Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75, 1807–1817 (1994).
Article  Google Scholar 

53.
Sommaruga, R., Crosa, D. & Mazzeo, N. Study on the Decomposition of Pistia stratiotes L. (Araceae) in Cisne Reservoir, Uruguay. Hydrobiologia 78, 263–272 (1993).
CAS  Google Scholar 

54.
Fraser, L. H., Carty, S. M. & Steer, D. A test of four plant species to reduce total nitrogen and total phosphorus from soil leachate in subsurface wetland microcosms. Bioresour. Technol. 94, 185–192 (2004).
CAS  PubMed  Article  Google Scholar 

55.
Ball, B. A., Bradford, M. A. & Hunter, M. D. Nitrogen and phosphorus release from mixed litter layers is lower than predicted from single species decay. Ecosystems 12, 87–100 (2009).
CAS  Article  Google Scholar 

56.
Olson, J. S. Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44(2), 322–331 (1963).
Article  Google Scholar  More

A researcher scales the 100.8-metre tree named Menara in northern Borneo. The rarity of strong winds in the region has helped its rainforest to reach great heights. Credit: A. Shenkin et al./Front. For. Glob. Change (CC BY 4.0)

Ecology
15 October 2020

Scientists find that strong winds constrain tropical forest height, but island’s gentle breezes allow trees to stretch tall.

Relatively gentle winds on Borneo could explain why the island hosts the world’s tallest tropical forest — including the tallest known tree in the tropics, the 100-metre giant named Menara.
Last year, an international team described Menara, a yellow meranti (Shorea faguetiana) growing in a research plot in Malaysian Borneo. Now, a team composed of many of the same scientists and led by Tobias Jackson at the University of Oxford, UK, has used laser scanning to create a 3D model of several dozen trees in the plot and to measure their heights.
The researchers also placed strain gauges on the trees’ trunks to assess how much they bend in the wind, and modelled how much stress they could sustain. The results suggest that in tropical forests, the strongest winds put a limit on tree growth.
Large conifers in temperate forests, such as California’s coastal redwoods (Sequoia sempervirens), can grow even taller than Menara, but they are probably limited by factors other than wind speeds, because they have much thicker trunks, Jackson says. More

1.
Saunders, D. A., Hobbs, R. J. & Margules, C. R. Biological consequences of ecosystem fragmentation: a review. Conserv. Biol. 5, 18–32. https://doi.org/10.1002/ajp.23076 (1991).
Article  Google Scholar 
2.
Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419 (2003).
Article  Google Scholar 

3.
Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, 1–10. https://doi.org/10.1126/sciadv.1500052 (2015).
Article  Google Scholar 

4.
Alamgir, M. et al. High-risk infrastructure projects pose imminent threats to forests in Indonesian Borneo. Sci. Rep. 9(140), 1–10. https://doi.org/10.1038/s41598-018-36594-8 (2019).
CAS  Article  Google Scholar 

5.
Hansen, M. C. et al. The fate of tropical forest fragments. Sci. Adv. 6, 1–10. https://doi.org/10.1126/sciadv.aax8574 (2020).
Article  Google Scholar 

6.
Onderdonk, D. A. & Chapman, C. A. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int. J. Primatol. 21, 587–611. https://doi.org/10.1023/A:1005509119693 (2000).
Article  Google Scholar 

7.
Das, J., Biswas, J., Bhattacherjee, P. C. & Rao, S. S. Canopy bridges: an effective conservation tactic for supporting gibbon populations in forest fragments. Gibbons 1, 467–475. https://doi.org/10.1007/978-0-387-88604-6 (2009).
Article  Google Scholar 

8.
Taylor, A. C., Walker, F. M., Goldingay, R. L., Ball, T. & van der Ree, R. Degree of landscape fragmentation influences genetic isolation among populations of a gliding mammal. PLoS ONE 6, 1–9. https://doi.org/10.1371/journal.pone.0026651 (2011).
CAS  Article  Google Scholar 

9.
Sarma, K., Kumar, A., MuraliKrishna, C., Tripathi, O. P. & Gajurel, P. R. Ground feeding observations on corn (Zea mays) by eastern hoolock gibbon (Hoolock leuconedys). Curr. Sci. 104, 587–589 (2013).
Google Scholar 

10.
Chapman, C. A. et al. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am. J. Phys. Anthropol. 131, 525–534. https://doi.org/10.1002/ajpa.20477 (2006).
Article  PubMed  Google Scholar 

11.
Donaldson, A. & Cunneyworth, P. Case study: canopy bridges for primate conservation. Handb. Road Ecol. 1, 341–343. https://doi.org/10.1002/9781118568170.ch41 (2015).
Article  Google Scholar 

12.
Hernández-pérez, E. Rope bridges: a strategy for enhancing habitat connectivity of the Black Howler Monkey (Alouatta pigra). Neotrop. Primates 22, 94–96 (2015).
Google Scholar 

13.
Gregory, T., Carrasco-Rueda, F., Alonso, A., Kolowski, J. & Deichmann, J. L. Natural canopy bridges effectively mitigate tropical forest fragmentation for arboreal mammals. Sci. Rep. 7, 1–11. https://doi.org/10.1038/s41598-017-04112-x (2017).
CAS  Article  Google Scholar 

14.
Ni, Q. et al. Microhabitat use of the western black-crested gibbon inhabiting an isolated forest fragment in southern Yunnan, China: implications for conservation of an endangered species. Primates 59, 45–54. https://doi.org/10.1007/s10329-017-0634-7 (2018).
Article  PubMed  Google Scholar 

15.
Al-Razi, H., Maria, M. & Muzaffar, S. Mortality of primates due to roads and power lines in two forest patches in Bangladesh. Zoologia 36, 1–6. https://doi.org/10.3897/zoologia.36.e33540 (2019).
Article  Google Scholar 

16.
Birot, H., Campera, M., Imron, M. A. & Nekaris, K. A. I. Artificial canopy bridges improve connectivity in fragmented landscapes: the case of Javan slow lorises in an agroforest environment. Am. J. Primatol. 82, 1–10. https://doi.org/10.1002/ajp.23076 (2020).
Article  Google Scholar 

17.
Forman, R. T. T. & Alexander, L. E. Roads and their major ecological effects. Annu. Rev. Ecol. Syst. 29, 207–231. https://doi.org/10.1146/annurev.ecolsys.29.1.207 (1998).
Article  Google Scholar 

18.
Sarma, K. & Kumar, A. The day range and home range of the Eastern Hoolock Gibbon Hoolock leuconedys (Mammalia: Primates: Hylobatidae) in lower dibang valley district in Arunachal Pradesh India. J. Threat. Taxa 8, 8641–8651. https://doi.org/10.11609/jott.2739.8.4.8641-8651 (2016).
Article  Google Scholar 

19.
Estrada, A. et al. Impending extinction crisis of the world’s primates: why primates matter. Sci. Adv. https://doi.org/10.1126/sciadv.1600946 (2017).
Article  PubMed  PubMed Central  Google Scholar 

20.
Balbuena, D., Alonso, A., Panta, M., Garcia, A. & Gregory, T. Mitigating tropical forest fragmentation with natural and semi-artificial canopy bridges. Diversity https://doi.org/10.3390/d11040066 (2019).
Article  Google Scholar 

21.
Valladares-Padua, C. B., Junior, L. C. & Padua, S. A pole bridge to avoid primates road kils. Neotrop. Primates 3, 13 (1995).
Google Scholar 

22.
Weston, N., Goosem, M., Marsh, H., Cohen, M. & Wilson, R. Using canopy bridges to link habitat for arboreal mammals: successful trials in the Wet Tropics of Queensland. Aust. Mammal. 33, 93–105. https://doi.org/10.1071/AM11003 (2011).
Article  Google Scholar 

23.
Gregory, T. et al. Methods to establish canopy bridges to increase natural connectivity in linear infrastructure development. Soc. Pet. Eng. J. https://doi.org/10.2118/165598-MS (2013).
Article  Google Scholar 

24.
Teixeira, F. Z., Printes, R. C., Fagundes, J. C. G., Alonso, A. C. & Kindel, A. Canopy bridges as road overpasses for wildlife in urban fragmented landscapes. Biota Neotrop. 13, 117–123. https://doi.org/10.1590/S1676-06032013000100013 (2013).
Article  Google Scholar 

25.
Yokochi, K. & Bencini, R. A remarkably quick habituation and high use of a rope bridge by an endangered marsupial, the western ringtail possum. Nat. Conserv. 11, 79–94. https://doi.org/10.3897/natureconservation.11.4385 (2015).
Article  Google Scholar 

26.
Mittermeier, R. A., Rylands, A. B. & Wilson, D. E. Handbook of the Mammals of the World Vol. 3 (Lynx Edicions, Barcelona, 2013).
Google Scholar 

27.
Wilson, D. E. & Lacher, T. E. Handbook of the Mammals of the World Vol. 6 (Lynx Edicions, Barcelona, 2016).
Google Scholar 

28.
Ancrenaz, M. Orang-utan Bridges in Lower Kinabatangan: Field surveys between Abai and Batu Puteh. https://www.arcusfoundation.org/wp%E2%80%90content/uploads/2010/01/Kinabatangan%E2%80%90Orangutan%E2%80%90Rope%E2%80%90Bridges%E2%80%90Ancrenaz%E2%80%902010.pdf (2010).

29.
Goossens, B. & Ambu, L. N. Sabah wildlife department and 10 years of research: Towards a better conservation of Sabah’s wildlife. J. Oil Palm Environ. 3, 38–51. https://doi.org/10.5366/jope.2012.05 (2012).
Article  Google Scholar 

30.
Kumar, A., Devi, A., Gupta, A. K. & Sarma, K. Population, behavioural ecology and conservation of Hoolock Gibbon in Northeast India. Rare Anim. India 1, 242–266 (2013).
Google Scholar 

31.
Yap, J. L., Ruppert, N. & Rosely, N. F. N. Activities, habitat use and diet of wild Dusky Langurs, Trachypithecus obscurus in different habitat types in Penang, Malaysia. J. Sustain. Sci. Manag. 14, 71–85 (2019).
Google Scholar 

32.
Arjun Oli. Banke National Park builds canopy bridge to reduce wild animal road accidents. myRepublica https://myrepublica.nagariknetwork.com/news/banke-national-park-builds-canopy-bridge-to-reduce-wild-animal-road-accidents (2019).

33.
Lekshmi Priya S. Kerala Sanctuary builds ‘canopy bridges’, saves animals from road hits!. The Better India https://www.thebetterindia.com/185838/kerala-forest-department-chinnar-wildlife-sanctuary-canopy-bridges-india (2019).

34.
Chivers, D. J. Malayan Forest Primates: Ten Years’ Study in Tropical Rain Forest (Plenum Press, New York, 1982).
Google Scholar 

35.
Cheyne, S. M., Thompson, C. J. H. & Chivers, D. J. Travel adaptations of Bornean Agile Gibbons Hylobates albibarbis (Primates: Hylobatidae) in a degraded secondary forest, Indonesia. J. Threat. Taxa 5, 3963–3968. https://doi.org/10.11609/JoTT.o3361.3963-8 (2013).
Article  Google Scholar 

36.
Campbell, C. O., Cheyne, S. M. & Rawson, B. M. Best practice guidelines for the rehabilitation and translocation of gibbons. IUCN SSC Primate Spec. Group https://doi.org/10.2305/IUCN.CH.2015.SSC-OP.51.en (2015).
Article  Google Scholar 

37.
Saralamba, C. & Menpreeda, W. Increasing connectivity through artificial canopy bridge for the gibbons: a case study on the activity budget. Abstract for The 87th Annual Meeting of the American Association of Physical Anthropologists, Austin (Texas) (2018).

38.
Chan, B. P. L., Fellowes, J. R., Geissmann, T., & Jianfeng, Z. Hainan Gibbon Status Survey and Conservation Action Plan: VERSION I (Last Updated November 2005). Kadoorie Farm & Botanic Garden Technical Report No.3 (2005).

39.
Chan, B. P. L. Hainan gibbon Nomascus hainanus (Thomas, 1892). In Primates in Peril: The World’s 25 Most Endangered Primates 2014–2016. (eds Schwitzer, C., et al.). IUCN SSC Primate Spec. Gr. (PSG), Int. Primatol. Soc. (IPS), Conserv. Int. (CI), Bristol Zool. Soc. Arlington, VA. 67–69 (2015).

40.
Chan, B. P. L., Lo, Y. F. P. & Mo, Y. New hope for the Hainan gibbon: formation of a new group outside its known range. Oryx 54, 296. https://doi.org/10.1017/S0030605320000083 (2020).
Article  Google Scholar 

41.
Zeng, X. et al. Hainan Gibbon Conservation Action Plan 2016–2020. https://www.gibbons.asia/wp-content/uploads/2017/03/Hainan-Gibbon-Action-Plan-2016-2020.pdf (2016).

42.
Zheng, Y., Cai, Q., Cheng, S. & Li, X. Characteristics on intensity and precipitation of super typhoon Rammasun (1409) and reason why it rapidly intensified offshore. Torrential Rain Disast. 33, 333–341 (2014).
Google Scholar 

43.
Chivers, D. J. The Siamang in Malaya. A Field Study of a Primate in Tropical Rainforest. Karger (1974).

44.
Cristóbal-Azkarate, J. & Arroyo-Rodríguez, V. Diet and Activity Pattern of Howler Monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of Habitat Fragmentation and Implications for Conservation. Am. J. Primatol. 69, 1013–1029. https://doi.org/10.1002/ajp.20420 (2007).
Article  PubMed  Google Scholar 

45.
Arroyo-Rodríguez, V. & Mandujano, S. Conceptualization and measurement of habitat fragmentation from the primates’ perspective. Int. J. Primatol. 30, 497–514 (2009).
Article  Google Scholar 

46.
Fan, P., Scott, M. B., Fei, H. & Ma, C. Locomotion behavior of cao vit gibbon (Nomascus nasutus) living in karst forest in Bangliang Nature Reserve, Guangxi, China. Integr. Zool. 8, 356–364. https://doi.org/10.1111/j.1749-4877.2012.00300.x (2013).
Article  PubMed  Google Scholar 

47.
Mass, V. et al. Lemur bridges provide crossing structures over roads within a forested mining concession near moramanga, toamasina province, Madagascar. Conserv. Evid. 8, 11–18 (2011).
Google Scholar 

48.
Naresh Mitra. Guwahati: Natural bridge reunites hoolock gibbons after 100 years. Times of India https://timesofindia.indiatimes.com/city/guwahati/natural-bridge-reunites-hoolock-gibbons-after-100-years/articleshow/69998213.cms (2019).

49.
Fleagle, J. G. Locomotion and posture. In Malayan Forest Primates: Ten Years’ Study in Tropical Rain Forest (ed. Chivers, D. J.) 191–207 (Plenum Press, New York, 1980).
Google Scholar  More