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    Molecular detection of tick-borne pathogens in ticks collected from pets in selected mountainous areas of Tatra County (Tatra Mountains, Poland)

    1.
    Siuda, K. Kleszcze Polski (Acari: Ixodida). Część II. Systematyka i Rozmieszczenie (Polskie Towarzystwo Parazytologiczne, Warsaw, 1993).
    Google Scholar 
    2.
    Nowak-Chmura, M. & Siuda, K. Ticks of Poland. Review of contemporary issues and latest research. Ann. Parasitol. 58(3), 125–155 (2012).
    PubMed  Google Scholar 

    3.
    Stańczak, J., Cieniuch, S., Lass, A., Biernat, B. & Racewicz, M. Detection and quantification of Anaplasma phagocytophilum and Babesia spp. in Ixodes ricinus ticks from urban and rural environment, northern Poland, by real-time polymerase chain reaction. Exp. Appl. Acarol. 66(1), 63–81. https://doi.org/10.1007/s10493-015-9887-2 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    4.
    Filippova, N.A. Ixodid ticks of the subfamily Ixodinae. (Izdatielstwo Nauka (Fauna SSSR. Paukoobraznyje) 4, 1977).

    5.
    Nijhof, A. M. et al. Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector. Borne. Zoonot. Dis. 7, 585–595. https://doi.org/10.1089/vbz.2007.0130 (2007).
    Article  Google Scholar 

    6.
    Siuda, K. & Nowak-Chmura, M. Fauna of ticks (Ixodida) in the Beskid Wyspowy. In Arthropods: Human and Animal Parasites (eds Buczek, A. & Błaszak, C. Z.) 13–24 (Akapit, New York, 2011).
    Google Scholar 

    7.
    Nowak-Chmura, M. Fauna kleszczy (Ixodida) Europy Środkowej (Wydawnictwo Naukowe Uniwersytetu Pedagogicznego, Kraków, 2013).
    Google Scholar 

    8.
    Król, N., Obiegala, A., Pfeffer, M., Lonc, E. & Kiewra, D. Detection of selected pathogens in ticks collected from cats and dogs in the Wrocław Agglomeration, South-West Poland. Parasit. Vectors 9(1), 351. https://doi.org/10.1186/s13071-016-1632-0 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Siuda, K., Nowak, M., Gierczak, M., Wierzbowska, I. & Faber, M. Kleszcze (Acari: Ixodida) pasożytujące na psach i kotach domowych w Polsce. Wiad. Parazytol. 53, 155 (2007).
    Google Scholar 

    10.
    Day, M. J. One health: The importance of companion animal vector-borne diseases. Parasit. Vectors 4, 49. https://doi.org/10.1186/1756-3305-4-492011 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    11.
    Rijpkema, S., Golubić, D., Molkenboer, M., Verbeek-De Kruif, N. & Schellekens, J. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp. Appl. Acarol. 20, 23–30 (1996).
    CAS  PubMed  Article  Google Scholar 

    12.
    Wójcik-Fatla, A., Szymańska, J., Wdowiak, L., Buczek, A. & Dutkiewicz, J. Coincidence of three pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin makroregion. Ann. Agric. Environ. Med. 16(1), 151–158 (2009).
    PubMed  Google Scholar 

    13.
    Massung, R. F. et al. Nested PCR assay for detection of granulocytic ehrlichiae. J. Clin. Microbiol. 36(4), 1090–1095 (1998).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    14.
    Persing, D. H. et al. Detection of Babesia microti by polymerase chain reaction. J. Clin. Microbiol. 30, 2097–2103 (1992).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    15.
    Sroka, J., Szymańska, J. & Wójcik-Fatla, A. The occurence of Toxoplasma gondii and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from east Poland with the use of PCR. Ann. Agric. Environ. Med. 16(2), 313–319 (2009).
    PubMed  Google Scholar 

    16.
    Claerebout, E. et al. Ticks and associated pathogens collected from dogs and cats in Belgium. Parasit. Vectors. 6, 183. https://doi.org/10.1186/1756-3305-6-183 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    17.
    Schreiber, C. et al. Pathogens in ticks collected from dogs in Berlin/Brandenburg, Germany. Parasit. Vectors. 7, 535. https://doi.org/10.1186/s13071-014-0535-1 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    18.
    Davies, S. et al. Prevalence of ticks and tick-borne pathogens: Babesia and Borrelia species in ticks infesting cats of Great Britain. Vet. Parastiol. 15(244), 129–135. https://doi.org/10.1016/j.vetpar.2017.07.033 (2017).
    Article  Google Scholar 

    19.
    Geurden, T. et al. Detection of tick-borne pathogens in ticks from dogs and cats in different European countries. Ticks. Tick. Borne. Dis. 9(6), 1431–1436. https://doi.org/10.1016/j.ttbdis.2018.06.013 (2018).
    PubMed  Article  Google Scholar 

    20.
    Zajkowska, P. Ticks (Acari:Ixodida) attacking domestic dogs in the Malopolska voivodeship, Poland in Arthropods: In the contemporary world (eds. Buczek, A. & Błaszak Cz.). 87–99 (Koliber, 2015).

    21.
    Zygner, W., Jaros, S. & Wędrychowicz, H. Prevalence of Babesia canis, Borrelia afzelii, and Anaplasma phagocytophilum infection in hard ticks removed from dogs in Warsaw (central Poland). Vet. Parasitol. 153(1–2), 139–142. https://doi.org/10.1016/j.vetpar.2008.01.036 (2008).
    PubMed  Article  Google Scholar 

    22.
    Welc-Falęciak, R., Rodo, A., Siński, E. & Bajer, A. Babesia canis and other tick-borne infections in dogs in Central Poland. Vet. Parasitol. 166(3–4), 191–198. https://doi.org/10.1016/j.vetpar.2009.09.038 (2009).
    PubMed  Article  Google Scholar 

    23.
    Kocoń, A., Nowak-Chmura, M., Kłyś, M. & Siuda K. Ticks (Acari: Ixodida) attacking domestic cats (Felis catus L.) in southern Poland in Arthropods: In Urban and Suburban Environments (eds. Buczek, A. & Błaszak Cz.). 51–61 (Koliber, 2017).

    24.
    Roczeń-Karczmarz, M. et al. Comparison of the occurrence of tick-borne diseases in ticks collected from vegetation and animals in the same area. Med. Weter. 74(8), 484–488. https://doi.org/10.21521/mw.6107 (2018).
    Article  Google Scholar 

    25.
    Matysek, M. Kleszcze w Tatrach. 2(44), 46–57 (Tatry, 2013).

    26.
    Haitlinger, R. Przyczynek do znajomości Acarina drobnych ssaków subalpejskiej strefy Tatr. Wiad Parazytol. 26(6), 715 (1980).
    Google Scholar 

    27.
    Siuda, K., et al. Ryzyko atakowania przez kleszcze Ixodes ricinus ludzi w atrakcyjnych turystycznie obszarach województwa małopolskiego. Streszczenia Materiałów II Konferencji “Medycyna Podróży”. Białystok 12–14.05.2005, 44 (2005).

    28.
    Siuda, K., Lenčáková, D., Stanko, M., Nowak, M. & Pet’ko, B. Ixodes ricinus ticks as vectors of Lyme Borreliosis in the Carpathians Region of Poland. Konferencia Slovenska Parazitologicka Spoločnosi, Zoonózy, ich pôvodcovia a vectory, Smolenice, Slovakia, 4–6.04.2005. Zbornik abstraktov, 52 (2005).

    29.
    Siuda, K. & Nowak, M. Tick fauna (Ixodida) of the Polish Carpathian Mountains. In 12th International Congress of Acarology, Amsterdam, The Netherlands, 21–26.08.2006. Abstract Book Bruin J., 192 (2006).

    30.
    Danielová, V. et al. Extension of Ixodes ricinus ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. Int. J. Med. Microbiol. 296, 48–53. https://doi.org/10.1016/j.ijmm.2006.02.007 (2006).
    PubMed  Article  Google Scholar 

    31.
    Majláth, I. & Majláthová, V. Atlas kliešťov Slovenska. 41–47 (2015).

    32.
    Tarageľová, V. R., Mahríková, L., Selyemová, D., Václav, R. & Derdáková, M. Natural foci of Borrelia lusitaniae in a mountain region of Central Europe. Ticks. Tick. Borne. Dis. 7(2), 350–356. https://doi.org/10.1016/j.ttbdis.2015.12.006 (2016).
    PubMed  Article  Google Scholar 

    33.
    Asman, M. et al. Detection of protozoans Babesia microti and Toxoplasma gondii and their co-existence in ticks (Acari: Ixodida) collected in Tarnogórski district (Upper Silesia, Poland). Ann. Agric. Environ. Med. 22(1), 80–83. https://doi.org/10.5604/12321966.1141373 (2015).
    PubMed  Article  Google Scholar 

    34.
    Pet’ko, B., et al. Epizootiological aspect of Lyme borreliosis in the city agglomerations of the Carpathian regions of Slovakia and Poland and their peripheral part in Stawonogi. Pasożyty i nosicele (eds. Buczek, A. & Błaszak Cz.). 157–164, (KGM, 2001).

    35.
    Asman, M. et al. Anaplasma phagocytophilum, Babesia microti, Borrelia burgdorferi sensu lato, and Toxoplasma gondii in Ixodes ricinus (Acari, Ixodida) ticks collected from Slowinski National Park (Northern Poland). J. Vector. Ecol. 42(1), 200–202. https://doi.org/10.1111/jvec.12258 (2017).
    PubMed  Article  Google Scholar 

    36.
    Asman, M. et al. The occurrence of three tick-borne pathogens in Ixodes ricinus ticks collected from the area of the Kraków-Częstochowa Upland (Southern Poland). Acarologia. 58(4), 969–975. https://doi.org/10.24349/acarologia/20184301 (2018).
    Article  Google Scholar 

    37.
    Asman, M., Witecka, J., Solarz, K., Zwonik, A. & Szilman, P. Occurrence of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in Ixodes ricinus ticks collected from selected areas of Opolskie Province in south-west Poland. Ann. Agric. Environ. Med. 26(4), 544–547. https://doi.org/10.26444/aaem/110214 (2019).
    CAS  PubMed  Article  Google Scholar  More

  • in

    Arctic fires re-emerging

    1.
    Kasischke, E. S. et al. Can. J. Res. 40, 1313–1324 (2010).
    Article  Google Scholar 
    2.
    Walker, X. J. et al. Nature 572, 520–523 (2019).
    Article  Google Scholar 

    3.
    Smolyanitsky, V. November 2019–April 2020 Arctic Seasonal Review (WMO, 2020); https://go.nature.com/2FdYUyX

    4.
    Hu, Y., Fernandez-Anez, N., Smith, T. E. & Rein, G. Int. J. Wildland Fire 27, 293–312 (2018).
    Article  Google Scholar 

    5.
    Alaska Division of Forestry AK Fire Info: Alaska Wildland Fire Information https://go.nature.com/3hal6HB (2020).

    6.
    Prosperi, P. et al. Clim. Change 161, 415–432 (2020).
    Article  Google Scholar 

    7.
    Kirdyanov, A. V. et al. Environ. Res. Lett. 15, 034061 (2020).
    Article  Google Scholar 

    8.
    Olefeldt, D. et al. Nat. Commun. 7, 13043 (2016).
    Article  Google Scholar 

    9.
    Gibson, C. M. et al. Nat. Commun. 9, 3041 (2018).
    Article  Google Scholar 

    10.
    Usup, A., Hashimoto, Y., Takahashi, H. & Hayasaka, H. Tropics 14, 1–19 (2004).
    Article  Google Scholar 

    11.
    Turetsky, M. R. et al. Nat. Geosci. 13, 138–143 (2020).
    Article  Google Scholar 

    12.
    Xu, W. et al. Remote Sens. Environ. 193, 138–149 (2017).
    Article  Google Scholar 

    13.
    Wooster, M. J., Xu, W. & Nightingale, T. Remote Sens. Environ. 120, 236–254 (2012).
    Article  Google Scholar 

    14.
    Kirillina, K., Shvetsov, E. G., Protopopova, V. V., Thiesmeyer, L. & Yan, W. Environ. Res. Lett. 15, 035009 (2020).
    Article  Google Scholar  More

  • in

    No protofeathers on pterosaurs

    1.
    Wellnhofer, P. The Illustrated Encyclopedia of Pterosaurs (Salamander Books, 1991).
    2.
    Unwin, D. M. The Pterosaurs from Deep Time (Pi, 2005).

    3.
    Kellner, A. W. A. et al. The soft tissue of Jeholopterus (Pterosauria, Anurognathidae, Batrachognathinae) and the structure of the pterosaur wing membrane. Proc. R. Soc. B 277, 321–329 (2010).
    Article  Google Scholar 

    4.
    Witton, M. P. Pterosaurs. Natural History, Evolution, Anatomy (Princeton Univ. Press, 2013).

    5.
    Yang, Z. et al. Pterosaur integumentary structures with complex feather-like branching. Nat. Ecol. Evol. 4, 24–30 (2019).
    Article  Google Scholar 

    6.
    Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).
    Article  Google Scholar 

    7.
    Benton, M. J., Dhouially, D., Jiang, B. & McNamara, M. The early origin of feathers. Trends Ecol. Evol. 34, 856–859 (2019).
    Article  Google Scholar 

    8.
    Xu, X. Feather evolution: Looking up close and through deep time. Sci. Bull. 64, 563–564 (2019).
    Article  Google Scholar 

    9.
    Unwin, D. M. & Bakhurina, N. N. Sordes pilosus and the nature of the pterosaur flight apparatus. Nature 371, 62–64 (1994).
    Article  Google Scholar 

    10.
    Frey, E., Tischlinger, H., Buchy, M. C. & Martill, D. M. in Evolution and Palaeobiology of Pterosaurs Vol. 217 (eds Buffetaut, E. & Mazin, J.-M.) 233–266 (Geological Society of London, Special Publications, 2003).

    11.
    Li, Q. et al. Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507, 350–353 (2014).
    CAS  Article  Google Scholar 

    12.
    Pinheiro, F. L. et al. Chemical characterization of pterosaur melanin challenges color inferences in extinct animals. Sci. Rep. 9, 15947 (2019).
    Article  Google Scholar 

    13.
    Campione, N. E., Barrett, P. M. & Evans, D. C. in The Evolution of Feathers (eds Foth, C. & Rauhut, O. W. M.) 213–243 (Springer, 2020).

    14.
    Czerkas, S. A. & Ji, Q. in Feathered Dinosaurs and the Origin of Flight (ed. Czerkas, S. J.) 15–41 (The Dinosaur Museum, 2002).

    15.
    Ji, Q. & Yuan, C. Discovery of two kinds of protofeathered pterosaurs in the Mesozoic Daohugou biota in the Ningcheng region and its stratigraphic and biologic significances. Geol. Rev. 48, 221–224 (2002).
    Google Scholar 

    16.
    Wang, X. L., Zhou, Z. H., Zhang, F. C. & Xu, X. A nearly completely articulated rhamphorhynchoid pterosaur with exceptionally well-preserved wing membranes and ‘hairs’ from Inner Mongolia, northeast China. Chin. Sci. Bull. 47, 226–230 (2002).
    Article  Google Scholar 

    17.
    Jäger, K. R. K., Tischlinger, H., Oleschinski, G. & Sander, P. M. Goldfuß was right: soft part preservation in the Late Jurassic pterosaur Scaphognathus crassirostris revealed by reflectance transformation imaging and ultraviolet light and the auspicious beginnings of paleo-art. Palaeontol. Electron. 21.3.3T (2019).

    18.
    Lü, J. & Hone, D. W. E. A new Chinese anurognathid pterosaur and the evolution of pterosaurian tail lengths. Acta Geol. Sin. 86, 1317–1325 (2012).
    Article  Google Scholar 

    19.
    Bennett, S. C. New interpretation of the wings of the pterosaur Rhamphorhynchus muensteri based on the Zittel and Marsh specimens. J. Paleontol. 89, 845–869 (2016).
    Article  Google Scholar 

    20.
    Hone, D., Henderson, D. M., Therrien, F. & Habib, M. B. A specimen of Rhamphorhynchus with soft tissue preservation, stomach contents and a putative coprolite. PeerJ 3, e1191 (2015).
    Article  Google Scholar 

    21.
    Pan, Y. et al. Molecular evidence of keratin and melanosomes in feathers of the Early Cretaceous bird Eoconfuciusornis. Proc. Natl Acad. Sci. USA 113, E7900–E7907 (2016).
    CAS  Article  Google Scholar 

    22.
    Alibardi, L. Adaptation to the land: the skin of reptiles in comparison to that of amphibians and endotherm amniotes. J. Exp. Zool. 298B, 12–41 (2003).
    CAS  Article  Google Scholar  More

  • in

    Divergent forest sensitivity to repeated extreme droughts

    1.
    Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).
    CAS  Article  Google Scholar 
    2.
    Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013).
    CAS  Article  Google Scholar 

    3.
    IPCC Special Report on Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds Field, C. B. et al.) (Cambridge Univ. Press, 2012).

    4.
    Schwalm, C. R. et al. Reduction in carbon uptake during turn of the century drought in western North America. Nat. Geosci. 5, 551–556 (2012).
    CAS  Article  Google Scholar 

    5.
    Phillips, O. L. et al. Drought sensitivity of the Amazon rainforest. Science 323, 1344–1347 (2009).
    CAS  Article  Google Scholar 

    6.
    Allen, C. D., Breshears, D. D. & McDowell, N. G. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 129 (2015).
    Article  Google Scholar 

    7.
    Dai, A. Drought under global warming: a review. Wiley Interdiscip. Rev. Clim. Change 2, 45–65 (2011).
    Article  Google Scholar 

    8.
    Cook, B. I., Smerdon, J. E., Seager, R. & Coats, S. Global warming and 21st century drying. Clim. Dyn. 43, 2607–2627 (2014).
    Article  Google Scholar 

    9.
    Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).
    CAS  Article  Google Scholar 

    10.
    Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).
    Article  Google Scholar 

    11.
    Zscheischler, J. et al. A few extreme events dominate global interannual variability in gross primary production. Environ. Res. Lett. 9, 035001 (2014).
    Article  Google Scholar 

    12.
    Miao, S., Zou, C. B. & Breshears, D. D. Vegetation responses to extreme hydrological events: sequence matters. Am. Nat. 173, 113–118 (2008).
    Article  Google Scholar 

    13.
    Anderegg, W. R. L. et al. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349, 528–532 (2015).
    CAS  Article  Google Scholar 

    14.
    Schwalm, C. R. et al. Global patterns of drought recovery. Nature 548, 202–205 (2017).
    CAS  Article  Google Scholar 

    15.
    Holling, C. S. Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4, 1–23 (1973).
    Article  Google Scholar 

    16.
    Gunderson, L. H. et al. Ecological resilience—in theory and application. Annu. Rev. Ecol. Syst. 31, 425–439 (2000).
    Article  Google Scholar 

    17.
    Ingrisch, J. & Bahn, M. Towards a comparable quantification of resilience. Trends Ecol. Evol. 33, 251–259 (2018).
    Article  Google Scholar 

    18.
    Bartlett, M. K. et al. Global analysis of plasticity in turgor loss point, a key drought tolerance trait. Ecol. Lett. 17, 1580–1590 (2014).
    Article  Google Scholar 

    19.
    Martínez‐Vilalta, J. et al. Hydraulic adjustment of Scots pine across Europe. New Phytol. 184, 353–364 (2009).
    Article  Google Scholar 

    20.
    Hacke, U. G., Stiller, V., Sperry, J. S., Pittermann, J. & McCulloh, K. A. Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol. 125, 779–786 (2001).
    CAS  Article  Google Scholar 

    21.
    Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012).
    CAS  Article  Google Scholar 

    22.
    Schymanski, S. J., Roderick, M. L., Sivapalan, M., Hutley, L. B. & Beringer, J. A canopy-scale test of the optimal water-use hypothesis. Plant Cell Environ. 31, 97–111 (2008).
    Google Scholar 

    23.
    Zhang, T., Niinemets, Ü., Sheffield, J. & Lichstein, J. W. Shifts in tree functional composition amplify the response of forest biomass to climate. Nature 556, 99–102 (2018).
    CAS  Article  Google Scholar 

    24.
    Anderegg, W. R. et al. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).
    CAS  Article  Google Scholar 

    25.
    Royer, P. D. et al. Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. J. Ecol. 99, 714–723 (2011).
    Article  Google Scholar 

    26.
    Raffa, K. F. et al. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 58, 501–517 (2008).
    Article  Google Scholar 

    27.
    Anderegg, W. R., Trugman, A. T., Bowling, D. R., Salvucci, G. & Tuttle, S. E. Plant functional traits and climate influence drought intensification and land–atmosphere feedbacks. Proc. Natl Acad. Sci. USA 116, 14071–14076 (2019).

    28.
    Cailleret, M. et al. A synthesis of radial growth patterns preceding tree mortality. Glob. Change Biol. 23, 1675–1690 (2017).
    Article  Google Scholar 

    29.
    Camarero, J. J., Gazol, A., Sangüesa-Barreda, G., Oliva, J. & Vicente-Serrano, S. M. To die or not to die: early warnings of tree dieback in response to a severe drought. J. Ecol. 103, 44–57 (2015).
    CAS  Article  Google Scholar 

    30.
    Jump, A. S. et al. Structural overshoot of tree growth with climate variability and the global spectrum of drought-induced forest dieback. Glob. Change Biol. 23, 3742–3757 (2017).
    Article  Google Scholar 

    31.
    Saatchi, S. et al. Persistent effects of a severe drought on Amazonian forest canopy. Proc. Natl Acad. Sci. USA 110, 565–570 (2013).
    CAS  Article  Google Scholar 

    32.
    Konings, A. G., Williams, A. P. & Gentine, P. Sensitivity of grassland productivity to aridity controlled by stomatal and xylem regulation. Nat. Geosci. 10, 284–288 (2017).
    CAS  Article  Google Scholar 

    33.
    Carnicer, J. et al. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc. Natl Acad. Sci. USA 108, 1474–1478 (2011).
    CAS  Article  Google Scholar 

    34.
    Brienen, R. J. W. et al. Long-term decline of the Amazon carbon sink. Nature 519, 344–348 (2015).
    CAS  Article  Google Scholar 

    35.
    Lenton, T. M. et al. Tipping elements in the Earth’s climate system. Proc. Natl Acad. Sci. USA 105, 1786–1793 (2008).
    CAS  Article  Google Scholar 

    36.
    Duffy, P. B., Brando, P., Asner, G. P. & Field, C. B. Projections of future meteorological drought and wet periods in the Amazon. Proc. Natl Acad. Sci. USA 112, 13172–13177 (2015).
    CAS  Article  Google Scholar 

    37.
    Johnson, D. M., McCulloh, K. A., Woodruff, D. R. & Meinzer, F. C. Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Sci. 196, 48–53 (2012).
    Article  CAS  Google Scholar 

    38.
    Morris, H. et al. A global analysis of parenchyma tissue fractions in secondary xylem of seed plants. New Phytol. 209, 1553–1565 (2016).
    CAS  Article  Google Scholar 

    39.
    DeSoto, L. et al. Low growth resilience to drought is related to future mortality risk in trees. Nat. Commun. 11, 1–9 (2020).
    Article  CAS  Google Scholar 

    40.
    Fisher, R. A. et al. Vegetation demographics in Earth system models: a review of progress and priorities. Glob. Change Biol. 24, 35–54 (2018).
    Article  Google Scholar 

    41.
    Kennedy, D. et al. Implementing plant hydraulics in the Community Land Model, version 5. J. Adv. Model. Earth Syst. 11, 485–513 (2019).
    Article  Google Scholar 

    42.
    Trugman, A. T. et al. Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol. Lett. 21, 1552–1560 (2018).
    CAS  Article  Google Scholar 

    43.
    Trugman, A. T. et al. Climate and plant trait strategies determine tree carbon allocation to leaves and mediate future forest productivity. Glob. Change Biol. 25, 3395–3405 (2019).
    Article  Google Scholar 

    44.
    Scheiter, S., Langan, L. & Higgins, S. I. Next-generation dynamic global vegetation models: learning from community ecology. New Phytol. 198, 957–969 (2013).
    Article  Google Scholar 

    45.
    Vicente-Serrano, S. M., Beguería, S., López-Moreno, J. I., Angulo, M. & El Kenawy, A. A new global 0.5 gridded dataset (1901–2006) of a multiscalar drought index: comparison with current drought index datasets based on the Palmer Drought Severity Index. J. Hydrometeorol. 11, 1033–1043 (2010).
    Article  Google Scholar 

    46.
    Beguería, S., Vicente-Serrano, S. M. & Angulo-Martínez, M. A multiscalar global drought dataset: the SPEIbase: a new gridded product for the analysis of drought variability and impacts. Bull. Am. Meteorol. Soc. 91, 1351–1356 (2010).
    Article  Google Scholar 

    47.
    Beguería, S., Vicente-Serrano, S. M., Reig, F. & Latorre, B. Standardized Precipitation Evapotranspiration Index (SPEI) revisited: parameter fitting, evapotranspiration models, tools, datasets and drought monitoring. Int. J. Climatol. 34, 3001–3023 (2014).
    Article  Google Scholar 

    48.
    Vicente-Serrano, S. M. et al. Response of vegetation to drought time-scales across global land biomes. Proc. Natl Acad. Sci. USA 110, 52–57 (2013).
    CAS  Article  Google Scholar 

    49.
    Gazol, A., Camarero, J. J., Anderegg, W. R. L. & Vicente-Serrano, S. M. Impacts of droughts on the growth resilience of Northern Hemisphere forests. Glob. Ecol. Biogeogr. 26, 166–176 (2017).
    Article  Google Scholar 

    50.
    Klesse, S. et al. Sampling bias overestimates climate change impacts on forest growth in the southwestern United States. Nat. Commun. 9, 5336 (2018).
    CAS  Article  Google Scholar 

    51.
    Bechtold, W. A. & Patterson, P. L. The Enhanced Forest Inventory and Analysis Program—National Sampling Design and Estimation Procedures General Technical Report SRS-80 (USDA, 2005).

    52.
    Bechtold, W. & Scott, C. T. in The Enhanced Forest Inventory and Analysis Program—National Sampling Design and Estimation Procedures General Technical Report SRS-80 (eds Bechtold, W. A. & Patterson, P. L.) 37–52 (USDA, 2005).

    53.
    Woudenberg, S. W. et al. The Forest Inventory and Analysis Database: Database Description and Users Manual Version 4.0 for Phase 2 General Technical Report RMRS-GTR-245 (USDA, 2010).

    54.
    Jacobi, W. R., Kearns, H. S. J. & Johnson, D. W. Persistence of pinyon pine snags and logs in southwestern Colorado. West. J. Appl. For. 20, 247–252 (2005).
    Article  Google Scholar 

    55.
    Shaw, J. D. et al. Arizona’s Forest Resources, 2001–2014 Resource Bulletin RMRS-RB-25 (USDA, 2018).

    56.
    Shaw, J. D., Steed, B. E. & DeBlander, L. T. Forest inventory and analysis (FIA) annual inventory answers the question: what is happening to pinyon-juniper woodlands? J. For. 103, 280–285 (2005).
    Google Scholar 

    57.
    Breshears, D. D. et al. Regional vegetation die-off in response to global-change-type drought. Proc. Natl Acad. Sci. USA 102, 15144–15148 (2005).
    CAS  Article  Google Scholar 

    58.
    Williams, A. P. et al. Forest responses to increasing aridity and warmth in the southwestern United States. Proc. Natl Acad. Sci. USA 107, 21289–21294 (2010).
    CAS  Article  Google Scholar 

    59.
    Anderegg, W. R. et al. Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol. 208, 674–683 (2015).
    Article  Google Scholar 

    60.
    Jackson, T. J. & Schmugge, T. J. Vegetation effects on the microwave emission of soils. Remote Sens. Environ. 36, 203–212 (1991).
    Article  Google Scholar 

    61.
    Tian, F. et al. Remote sensing of vegetation dynamics in drylands: evaluating vegetation optical depth (VOD) using AVHRR NDVI and in situ green biomass data over West African Sahel. Remote Sens. Environ. 177, 265–276 (2016).
    Article  Google Scholar 

    62.
    Liu, Y. Y. et al. Recent reversal in loss of global terrestrial biomass. Nat. Clim. Change 5, 470–474 (2015).
    Article  Google Scholar 

    63.
    Momen, M. et al. Interacting effects of leaf water potential and biomass on vegetation optical depth. J. Geophys. Res. Biogeosci. 122, 3031–3046 (2017).
    Article  Google Scholar 

    64.
    Konings, A. G. & Gentine, P. Global variations in ecosystem-scale isohydricity. Glob. Change Biol. 23, 891–905 (2017).
    Article  Google Scholar 

    65.
    Van de Griend, A. A. & Wigneron, J.-P. The b-factor as a function of frequency and canopy type at H-polarization. IEEE Trans. Geosci. Remote Sens. 42, 786–794 (2004).
    Article  Google Scholar 

    66.
    Konings, A. G., Rao, K. & Steele-Dunne, S. C. Macro to micro: microwave remote sensing of plant water content for physiology and ecology. New Phytol. https://doi.org/10.1111/nph.15808 (2019).

    67.
    Du, J. et al. A global satellite environmental data record derived from AMSR-E and AMSR2 microwave earth observations. Earth Syst. Sci. Data Discuss. https://doi.org/10.5194/essd-2017-27 (2017).

    68.
    Du, J., Kimball, J. S., Jones, L. A. & Member, S. Passive microwave remote sensing of soil moisture based on dynamic vegetation scattering properties for AMSR-E. IEEE Trans. Geosci. Remote Sens. 54, 597–608 (2015).
    Article  Google Scholar 

    69.
    Du, J. et al. A global satellite environmental data record derived from AMSR-E and AMSR2 microwave Earth observations. Earth Syst. Sci. Data 9, 791–808 (2017).
    Article  Google Scholar 

    70.
    Jones, L. A. et al. Satellite microwave remote sensing of daily land surface air temperature minima and maxima from AMSR-E. IEEE J. Sel. Top. Appl. Earth Obs. Remote Sens. 3, 111–123 (2010).
    Article  Google Scholar 

    71.
    Olson, D. M. et al. Terrestrial Ecoregions of the World: A New Map of Life on Earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933–938 (2001).
    Article  Google Scholar 

    72.
    Zar, J. H. in Biostatistical Analysis 1st edn, 185–205 (Prentice-Hall International, 1984).

    73.
    Fox, J. et al. Package ‘car’ (R Foundation for Staistical Computing, 2012).

    74.
    Fox, J., Friendly, M. & Weisberg, S. Hypothesis tests for multivariate linear models using the car package. R J. 5, 39–52 (2013).
    Article  Google Scholar 

    75.
    Dormann, C. F. et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30, 609–628 (2007).
    Article  Google Scholar 

    76.
    Pinheiro, J. et al. nlme: linear and nonlinear mixed effects models. R package v.3.1-117 (R Foundation for Statistical Computing, 2014).

    77.
    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012). More

  • in

    Climate change disturbs wildlife microbiomes

    1.
    Baquero, F. & Nombela, C. Clin. Microbiol. Infec. 18(Suppl. 4), 2–4 (2012).
    2.
    Roughgarden, J., Gilbert, S. F., Rosenberg, E., Zilber-Rosenberg, I. & Lloyd, E. A. Biol. Theory 13, 44–65 (2018).
    Article  Google Scholar 

    3.
    Greenspan, S. E. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-020-0899-5 (2020).

    4.
    Caporaso, J. G. et al. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).
    CAS  Article  Google Scholar 

    5.
    Cho, I. & Blaser, M. J. Nat. Rev. Genet. 13, 260–270 (2012).
    CAS  Article  Google Scholar 

    6.
    Walke, J. B. et al. ISME J. 8, 2207–2217 (2014).
    CAS  Article  Google Scholar 

    7.
    Antwis, R. E. et al. PLoS ONE 9, e85563 (2014).
    Article  Google Scholar 

    8.
    Heiman, M. L. & Greenway, F. L. Mol. Metab. 5, 317–320 (2016).
    CAS  Article  Google Scholar 

    9.
    Romero, G. Q. et al. Nat. Commun. 11, 3215 (2020).
    CAS  Article  Google Scholar 

    10.
    Sabagh, L. T. et al. Copeia 2012, 683–689 (2012).
    Article  Google Scholar  More

  • in

    A framework for in situ molecular characterization of coral holobionts using nanopore sequencing

    1.
    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377. https://doi.org/10.1038/nature21707 (2017).
    ADS  CAS  Article  PubMed  Google Scholar 
    2.
    LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580. https://doi.org/10.1016/j.cub.2018.07.008 (2018).
    CAS  Article  PubMed  Google Scholar 

    3.
    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340. https://doi.org/10.1146/annurev-micro-102215-095440 (2016).
    CAS  Article  PubMed  Google Scholar 

    4.
    Peixoto, R. S., Rosado, P. M., Leite, D. C. D., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. https://doi.org/10.3389/Fmicb.2017.00341 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    5.
    Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073. https://doi.org/10.1111/j.1462-2920.2006.01148.x (2006).
    CAS  Article  PubMed  Google Scholar 

    6.
    Lesser, M. P. et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346, 143–152. https://doi.org/10.3354/meps07008 (2007).
    ADS  CAS  Article  Google Scholar 

    7.
    Ben-Haim, Y. et al. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. System. Evol. Microbiol. 53, 309–315. https://doi.org/10.1099/ijs.0.02402-0 (2003).
    CAS  Article  Google Scholar 

    8.
    Johnston, E. C. et al. A genomic glance through the fog of plasticity and diversification in Pocillopora. Sci. Rep. https://doi.org/10.1038/S41598-017-06085-3 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    9.
    Shearer, T. L., Van Oppen, M. J., Romano, S. L. & Worheide, G. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol. Ecol. 11, 2475–2487 (2002).
    CAS  Article  Google Scholar 

    10.
    Hellberg, M. E. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol. Biol. 6, 24. https://doi.org/10.1186/1471-2148-6-24 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    11.
    Wares, J. P. Mitochondrial cytochrome b sequence data are not an improvement for species identification in scleractinian corals. PeerJ 2, e564. https://doi.org/10.7717/peerj.564 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    12.
    Arrigoni, R. et al. A new sequence data set of SSU rRNA gene for Scleractinia and its phylogenetic and ecological applications. Mol. Ecol. Resour. 17, 1054–1071. https://doi.org/10.1111/1755-0998.12640 (2017).
    CAS  Article  PubMed  Google Scholar 

    13.
    Suzuki, G. & Nomura, K. Species boundaries of Astreopora corals (Scleractinia, Acroporidae) inferred by mitochondrial and nuclear molecular markers. Zool. Sci. 30, 626–632. https://doi.org/10.2108/zsj.30.626 (2013).
    CAS  Article  PubMed  Google Scholar 

    14.
    Gelin, P., Postaire, B., Fauvelot, C. & Magalon, H. Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites. Mol. Phylogenet. Evol. 109, 430–446. https://doi.org/10.1016/j.ympev.2017.01.018 (2017).
    CAS  Article  PubMed  Google Scholar 

    15.
    LaJeunesse, T. C. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: In search of a “species” level marker. J. Phycol. 37, 866–880. https://doi.org/10.1046/j.1529-8817.2001.01031.x (2001).
    CAS  Article  Google Scholar 

    16.
    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. https://doi.org/10.7717/peerj.4816 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    17.
    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. https://doi.org/10.1111/1755-0998.13004 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    18.
    Arif, C. et al. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol. Ecol. 23, 4418–4433. https://doi.org/10.1111/mec.12869 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    19.
    Smith, E. G., Ketchum, R. N. & Burt, J. A. Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. Isme J. 11, 1500–1503. https://doi.org/10.1038/ismej.2016.206 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    20.
    Ziegler, M. et al. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J. Biogeogr. 44, 674–686. https://doi.org/10.1111/jbi.12913 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    21.
    Mouchka, M. E., Hewson, I. & Harvell, C. D. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 50, 662–674. https://doi.org/10.1093/icb/icq061 (2010).
    Article  PubMed  Google Scholar 

    22.
    Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio https://doi.org/10.1128/mBio.00560-16 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    23.
    Neave, M. J., Apprill, A., Ferrier-Pages, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324. https://doi.org/10.1007/s00253-016-7777-0 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    24.
    Hernandez-Agreda, A., Gates, R. D. & Ainsworth, T. D. Defining the Core Microbiome in Corals’ Microbial Soup. Trends Microbiol. 25, 125–140. https://doi.org/10.1016/j.tim.2016.11.003 (2017).
    CAS  Article  PubMed  Google Scholar 

    25.
    Roder, C., Bayer, T., Aranda, M., Kruse, M. & Voolstra, C. R. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol. Ecol. 24, 3501–3511. https://doi.org/10.1111/mec.13251 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    26.
    Pogoreutz, C. et al. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8, 2240–2252. https://doi.org/10.1002/ece3.3830 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    27.
    Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. Isme J. 11, 186–200. https://doi.org/10.1038/ismej.2016.95 (2017).
    Article  PubMed  Google Scholar 

    28.
    Menegon, M. et al. On site DNA barcoding by nanopore sequencing. PLoS ONE 12, e0184741. https://doi.org/10.1371/journal.pone.0184741 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    29.
    Parker, J., Helmstetter, A. J., Devey, D., Wilkinson, T. & Papadopulos, A. S. T. Field-based species identification of closely-related plants using real-time nanopore sequencing. Sci. Rep. 7, 8345. https://doi.org/10.1038/s41598-017-08461-5 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    30.
    Pomerantz, A. et al. Real-time DNA barcoding in a rainforest using nanopore sequencing: opportunities for rapid biodiversity assessments and local capacity building. Gigascience https://doi.org/10.1093/gigascience/giy033 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    31.
    Santos, A., van Aerle, R., Barrientos, L. & Martinez-Urtaza, J. Computational methods for 16S metabarcoding studies using Nanopore sequencing data. Comput. Struct. Biotechnol. J. 18, 296–305. https://doi.org/10.1016/j.csbj.2020.01.005 (2020).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    32.
    Berntson, E. A., Bayer, F. M., McArthur, A. G. & France, S. C. Phylogenetic relationships within the Octocorallia (Cnidaria:Anthozoa) based on nuclear 18S rRNA sequences. Mar. Biol. 138, 235–246. https://doi.org/10.1007/s002270000457 (2001).
    CAS  Article  Google Scholar 

    33.
    Pootakham, W. et al. High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci. Rep. 7, 2774. https://doi.org/10.1038/s41598-017-03139-4 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    34.
    Hume, B. et al. Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar. Pollut. Bull. 72, 313–322. https://doi.org/10.1016/j.marpolbul.2012.11.032 (2013).
    CAS  Article  PubMed  Google Scholar 

    35.
    Hume, B. C. et al. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci. Rep. 5, 8562. https://doi.org/10.1038/srep08562 (2015).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    36.
    Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100. https://doi.org/10.1093/bioinformatics/bty191 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    37.
    Noonan, S. H. C., Fabricius, K. E. & Humphrey, C. Symbiodinium community composition in scleractinian corals is not affected by life-long exposure to elevated carbon dioxide. PLoS ONE https://doi.org/10.1371/journal.pone.0063985 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    38.
    Bayer, T. et al. Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps10197 (2013).
    Article  Google Scholar 

    39.
    Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. Isme J. 10, 2280–2292. https://doi.org/10.1038/ismej.2016.9 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    40.
    Morrow, K. M. et al. Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. Isme J. 9, 894–908. https://doi.org/10.1038/ismej.2014.188 (2015).
    CAS  Article  PubMed  Google Scholar 

    41.
    Morrow, K. M., Bromhall, K., Motti, C. A., Munn, C. B. & Bourne, D. G. Allelochemicals produced by brown macroalgae of the lobophora genus are active against coral larvae and associated bacteria, supporting pathogenic shifts to vibrio dominance. Appl. Environ. Microb. https://doi.org/10.1128/AEM.02391-16 (2017).
    Article  Google Scholar 

    42.
    Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, C. R. Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci. Rep. 7, 40579. https://doi.org/10.1038/srep40579 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    43.
    Cardenas, A. et al. Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton. Isme J. 12, 59–76. https://doi.org/10.1038/ismej.2017.142 (2018).
    CAS  Article  PubMed  Google Scholar 

    44.
    Pollock, F. J. et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. https://doi.org/10.1038/S41467-018-07275-X (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    45.
    Cardenas, A., Rodriguez, L. M., Pizarro, V., Cadavid, L. F. & Arevalo-Ferro, C. Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease. Isme J. 6, 502–512. https://doi.org/10.1038/ismej.2011.123 (2012).
    CAS  Article  PubMed  Google Scholar 

    46.
    Gajigan, A. P., Diaz, L. A. & Conaco, C. Resilience of the prokaryotic microbial community of Acropora digitifera to elevated temperature. Microbiologyopen https://doi.org/10.1002/mbo3.478 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    47.
    Shnit-Orland, M., Sivan, A. & Kushmaro, A. Shewanella corallii sp. nov., a marine bacterium isolated from a Red Sea coral. Int. J. System. Evol. Microbiol. 60, 2293–2297. https://doi.org/10.1099/ijs.0.015768-0 (2010).
    CAS  Article  Google Scholar 

    48.
    Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. 105, 629–640. https://doi.org/10.1016/j.marpolbul.2015.12.045 (2016).
    CAS  Article  PubMed  Google Scholar 

    49.
    Paramasivam, N. et al. Bacterial Consortium of Millepora dichotoma exhibiting unusual multifocal lesion event in the gulf of Eilat Red Sea. Microb Ecol 65, 50–59. https://doi.org/10.1007/s00248-012-0097-8 (2013).
    Article  PubMed  Google Scholar 

    50.
    Paramasivam, N., Ben-Dov, E., Arotsker, L. & Kushmaro, A. Eilatimonas milleporae gen. nov., sp. nov., a marine bacterium isolated from the hydrocoral Millepora dichotoma. Int. J. Syst. Evol. Microbiol. 63, 1880–1884. https://doi.org/10.1099/ijs.0.043976-0 (2013).
    CAS  Article  PubMed  Google Scholar 

    51.
    Spring, S., Lunsdorf, H., Fuchs, B. M. & Tindall, B. J. The photosynthetic apparatus and its regulation in the aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp nov. PLoS ONE https://doi.org/10.1371/journal.pone.0004866 (2009).
    Article  PubMed  PubMed Central  Google Scholar 

    52.
    Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. Isme J. 8, 31–39. https://doi.org/10.1038/ismej.2013.127 (2014).
    CAS  Article  PubMed  Google Scholar 

    53.
    Sekar, R., Mills, D. K., Remily, E. R., Voss, J. D. & Richardson, L. L. Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl. Environ. Microbiol. 72, 5963–5973. https://doi.org/10.1128/AEM.00843-06 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    54.
    Blackall, L. L., Wilson, B. & van Oppen, M. J. Coral-the world’s most diverse symbiotic ecosystem. Mol. Ecol. 24, 5330–5347. https://doi.org/10.1111/mec.13400 (2015).
    Article  PubMed  Google Scholar 

    55.
    LaJeunesse, T. C. “Species” radiations of symbiotic Dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition (vol 22, pg 570, 2005). Mol. Biol. Evol. 22, 1158–1158. https://doi.org/10.1093/molbev/msi042 (2005).
    CAS  Article  Google Scholar 

    56.
    Hume, B. C. et al. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc. Natl. Acad. Sci. USA 113, 4416–4421. https://doi.org/10.1073/pnas.1601910113 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    57.
    Thornhill, D. J., Lewis, A. M., Wham, D. C. & LaJeunesse, T. C. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68, 352–367. https://doi.org/10.1111/evo.12270 (2014).
    CAS  Article  PubMed  Google Scholar  More

  • in

    Urban resources limit pair coordination over offspring provisioning

    1.
    Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, Oxford, 2012).
    Google Scholar 
    2.
    Williams, G. C. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (1966).
    Article  Google Scholar 

    3.
    Trivers, R. L. Sexual Selection and the Descent of Man 136–179 (Aldine Press, Chicago, 1972).
    Google Scholar 

    4.
    Lessells, C. M. The Evolution of Parental Care (Oxford Univeristy Press, Oxford, 2012).
    Google Scholar 

    5.
    Houston, A. I., Székely, T. & McNamara, J. M. Conflict between parents over care. Trends Ecol. Evol. 20, 33–38 (2005).
    Article  Google Scholar 

    6.
    Lessells, C. M. The evolutionary outcome of sexual conflict. Philos. Trans. R. Soc. B Biol. Sci. 361, 301–317 (2006).
    CAS  Article  Google Scholar 

    7.
    Houston, A. I. & Davies, N. B. The evolution of cooperation and life history in the dunnock, Prunella modularis. Behav. Ecol. Ecol. Conseq. Adapt. Behav. 20, 471–487 (1985).
    Google Scholar 

    8.
    McNamara, J. M., Gasson, C. E. & Houston, A. I. Incorporating rules for responding into evolutionary games. Nature 401, 368–371 (1999).
    ADS  CAS  PubMed  Google Scholar 

    9.
    McNamara, J. M., Houston, A. I., Barta, Z. & Osorno, J. L. Should young ever be better off with one parent than with two?. Behav. Ecol. 14, 301–310 (2003).
    Article  Google Scholar 

    10.
    Lessells, C. M. & McNamara, J. M. Sexual conflict over parental investment in repeated bouts: Negotiation reduces overall care. Proc. R. Soc. B Biol. Sci. 279, 1506–1514 (2012).
    CAS  Article  Google Scholar 

    11.
    Johnstone, R. A. & Hinde, C. A. Negotiation over offspring care – how should parents respond to each other’s efforts?. Behav. Ecol. 17, 818–827 (2006).
    Article  Google Scholar 

    12.
    Royle, N. J., Hartley, I. R. & Parker, G. A. Sexual conflict reduces offspring fitness in zebra finches. Nature 416, 733–736 (2002).
    ADS  CAS  Article  Google Scholar 

    13.
    Johnstone, R. A. et al. Reciprocity and conditional cooperation between great tit parents. Behav. Ecol. 25, 216–222 (2014).
    Article  Google Scholar 

    14.
    Savage, J. L., Browning, L. E., Manica, A., Russell, A. F. & Johnstone, R. A. Turn-taking in cooperative offspring care: By-product of individual provisioning behavior or active response rule?. Behav. Ecol. Sociobiol. 71, 162 (2017).
    Article  Google Scholar 

    15.
    Raihani, N. J., Nelson-Flower, M. J., Moyes, K., Browning, L. E. & Ridley, A. R. Synchronous provisioning increases brood survival in cooperatively breeding pied babblers. J. Anim. Ecol. 79, 44–52 (2010).
    Article  Google Scholar 

    16.
    Mariette, M. M. & Griffith, C. S. The adaptive significance of provisioning and foraging coordination between breeding partners. Am. Nat. 185, 270–280 (2015).
    Article  Google Scholar 

    17.
    Bebbington, K. & Hatchwell, B. J. Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav. Ecol. 27, 652–659 (2016).
    Article  Google Scholar 

    18.
    Leniowski, K. & Węgrzyn, E. Synchronisation of parental behaviours reduces the risk of nest predation in a socially monogamous passerine bird. Sci. Rep. 8, 7385 (2018).
    ADS  CAS  Article  Google Scholar 

    19.
    Shen, S. F., Chen, H. C., Vehrencamp, S. L. & Yuan, H. W. Group provisioning limits sharing conflict among nestlings in joint-nesting Taiwan yuhinas. Biol. Lett. 6, 318–321 (2010).
    Article  Google Scholar 

    20.
    Savage, J. L. & Hinde, C. A. What can we quantify about carer behavior?. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00418 (2019).
    Article  Google Scholar 

    21.
    Baldan, D., Curk, T., Hinde, C. A. & Lessells, C. M. Alternation of nest visits varies with experimentally manipulated workload in brood-provisioning great tits. Anim. Behav. 156, 139–146. https://doi.org/10.1016/j.anbehav.2019.08.004 (2019).
    Article  Google Scholar 

    22.
    Griffioen, M., Müller, W. & Iserbyt, A. A fixed agreement—consequences of brood size manipulation on alternation in blue tits. PeerJ 7, e6826. https://doi.org/10.7717/peerj.6826 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    23.
    Iserbyt, A., Fresneau, N., Kortenhoff, T., Eens, M. & Muller, W. Decreasing parental task specialization promotes conditional cooperation. Sci. Rep. 7, 20 (2017).
    Article  Google Scholar 

    24.
    Baldan, D., Hinde, C. A. & Lessells, C. M. Turn-taking between provisioning parents: Partitioning alternation. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00448 (2019).
    Article  Google Scholar 

    25.
    Lejeune, L. et al. Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00356 (2019).
    Article  Google Scholar 

    26.
    Longcore, T. & Rich, C. Ecological light pollution. Front. Ecol. Environ. 2, 191–198. https://doi.org/10.1890/1540-9295(2004)002[0191:Elp]2.0.Co;2 (2004).
    Article  Google Scholar 

    27.
    Warren, P. S., Katti, M., Ermann, M. & Brazel, A. Urban bioacoustics: It’s not just noise. Anim. Behav. 71, 491–502. https://doi.org/10.1016/j.anbehav.2005.07.014 (2006).
    Article  Google Scholar 

    28.
    McCarthy, M. P., Best, M. J. & Betts, R. A. Climate change in cities due to global warming and urban effects. Geophys. Res. Lett. https://doi.org/10.1029/2010gl042845 (2010).
    Article  Google Scholar 

    29.
    Chamberlain, D. E. et al. Avian productivity in urban landscapes: A review and meta-analysis. Ibis 151, 1–18. https://doi.org/10.1111/j.1474-919X.2008.00899.x (2009).
    Article  Google Scholar 

    30.
    Pollock, C. J., Capilla-Lasheras, P., McGill, R. A. R., Helm, B. & Dominoni, D. M. Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus). Sci. Rep. 7, 5014. https://doi.org/10.1038/s41598-017-04575-y (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Seress, G. et al. Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecol. Appl. 28, 1143–1156. https://doi.org/10.1002/eap.1730 (2018).
    Article  PubMed  Google Scholar 

    32.
    Seress, G., Sándor, K., Evans, K. L. & Liker, A. Food availability limits avian reproduction in the city: An experimental study on great tits Parus major. J. Anim. Ecol. 00, 1–11. https://doi.org/10.1111/1365-2656.13211 (2020).
    Article  Google Scholar 

    33.
    Wilkin, T. A., King, L. E. & Sheldon, B. C. Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. J. Avian Biol. 40, 135–145. https://doi.org/10.1111/j.1600-048X.2009.04362.x (2009).
    Article  Google Scholar 

    34.
    Peach, W. J., Mallord, J. W., Ockendon, N., Orsman, C. J. & Haines, W. G. Depleted suburban house sparrow Passer domesticus population not limited by food availability. Urban Ecosyst. 21, 1053–1065. https://doi.org/10.1007/s11252-018-0784-4 (2018).
    Article  Google Scholar 

    35.
    Schoech, S. J. et al. Food supplementation: A tool to increase reproductive output? A case study in the threatened Florida Scrub-Jay. Biol. Cons. 141, 162–173. https://doi.org/10.1016/j.biocon.2007.09.009 (2008).
    Article  Google Scholar 

    36.
    Sol, D., Lapiedra, O. & González-Lagos, C. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101–1112. https://doi.org/10.1016/j.anbehav.2013.01.023 (2013).
    Article  Google Scholar 

    37.
    Isaksson, C. & Andersson, S. Carotenoid diet and nestling provisioning in urban and rural great tits Parus major. J. Avian Biol. 38, 564–572. https://doi.org/10.1111/j.2007.0908-8857.04030.x (2007).
    Article  Google Scholar 

    38.
    New, T. R. Insect Conservation and Urban Environments (Springer, Berlin, 2015).
    Google Scholar 

    39.
    Helden, A., Stamp, G. & Leather, S. Urban biodiversity: Comparison of insect assemblages on native and non-native trees. Urban Ecosyst. 15, 611–624. https://doi.org/10.1007/s11252-012-0231-x (2012).
    Article  Google Scholar 

    40.
    Tallamy, D. W. & Shropshire, K. J. Ranking lepidopteran use of native versus introduced plants. Conserv. Biol. 23, 941–947 (2009).
    Article  Google Scholar 

    41.
    Burghardt, K. T., Tallamy, D. W., Philips, C. & Shropshire, K. J. Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1, art11. https://doi.org/10.1890/es10-00032.1 (2010).
    Article  Google Scholar 

    42.
    Marciniak, B., Nadolski, J., Nowakowska, M., Loga, B. & Bańbura, J. Habitat and annual variation in arthropod abundance affects blue tit Cyanistes caeruleus reproduction. Acta Ornithol. 42, 53–62 (2007).
    Article  Google Scholar 

    43.
    Neil, K. & Wu, J. Effects of urbanization on plant flowering phenology: A review. Urban Ecosyst. 9, 243–257. https://doi.org/10.1007/s11252-006-9354-2 (2006).
    Article  Google Scholar 

    44.
    Lessells, C. M. & Stephens, D. W. Central place foraging: Single-prey loaders again. Anim. Behav. 31, 238–243 (1983).
    Article  Google Scholar 

    45.
    Orians, G. H. & Pearson, N. E. On the Theory of Central Place Foraging. Analysis of Ecological Systems 155–177 (Ohio State University Press, Columbus, 1979).
    Google Scholar 

    46.
    Arnold, K. E., Ramsay, S. L., Henderson, L. & Larcombe, S. D. Seasonal variation in diet quality: Antioxidants, invertebrates and blue tits Cyanistes caeruleus. Biol. J. Lin. Soc. 99, 708–717. https://doi.org/10.1111/j.1095-8312.2010.01377.x (2010).
    Article  Google Scholar 

    47.
    Ouyang, J. Q., Baldan, D., Munguia, C. & Davies, S. Genetic inheritance and environment determine endocrine plasticity to urban living. Proc. R. Soc. B Biol. Sci. 286, 20191215. https://doi.org/10.1098/rspb.2019.1215 (2019).
    CAS  Article  Google Scholar 

    48.
    Newhouse, M. J., Marra, P. P. & Johnson, L. S. Reproductive success of house wrens in suburban and rural landscapes. Wilson J. Ornithol. 120, 99–104 (2008).
    Article  Google Scholar 

    49.
    Potti, J., Dávila, J. A., Tella, J. L., Frías, Ó & Villar, S. Gender and viability selection on morphology in fledgling pied flycatchers. Mol. Ecol. 11, 1317–1326. https://doi.org/10.1046/j.1365-294X.2002.01545.x (2002).
    CAS  Article  PubMed  Google Scholar 

    50.
    Balogh, A. L., Ryder, T. B. & Marra, P. P. Population demography of Gray Catbirds in the suburban matrix: Sources, sinks and domestic cats. J. Ornithol. 152, 717–726. https://doi.org/10.1007/s10336-011-0648-7 (2011).
    Article  Google Scholar 

    51.
    Stillfried, M. et al. Do cities represent sources, sinks or isolated islands for urban wild boar population structure?. J. Appl. Ecol. 54, 272–281. https://doi.org/10.1111/1365-2664.12756 (2017).
    Article  Google Scholar 

    52.
    Holmes, R. T. Foraging patterns of forest birds: Male–female differences. Wilson Bull. 98, 196–213 (1986).
    Google Scholar 

    53.
    Chaves, F. G., Vecchi, M. B. & Alves, M. A. S. Intersexual differences in the foraging behavior of Formicivora littoralis (Thamnophilidae), an endangered Neotropical bird. Stud. Neotrop. Fauna Environ. 52, 179–186. https://doi.org/10.1080/01650521.2017.1335275 (2017).
    Article  Google Scholar 

    54.
    Mänd, R., Rasmann, E. & Mägi, M. When a male changes his ways: Sex differences in feeding behavior in the pied flycatcher. Behav. Ecol. 24, 853–858. https://doi.org/10.1093/beheco/art025 (2013).
    Article  Google Scholar 

    55.
    Kölliker, M., Brinkhof, M. W. G., Heeb, P., Fitze, P. S. & Richner, H. The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267, 2127–2132 (2000).
    Article  Google Scholar 

    56.
    Naef-Daenzer, B. Patch time allocation and patch sampling by foraging great and blue tits. Anim. Behav. 59, 989–999 (2000).
    CAS  Article  Google Scholar 

    57.
    Jarrett, C., Powell, L. L., McDevitt, H., Helm, B. & Welch, A. J. Bitter fruits of hard labour: Diet metabarcoding and telemetry reveal that urban songbirds travel further for lower-quality food. Oecologia 193, 377–388. https://doi.org/10.1007/s00442-020-04678-w (2020).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    58.
    Gering, J. C. & Blair, R. B. Predation on artificial bird nests along an urban gradient: Predatory risk or relaxation in urban environments?. Ecography 22, 532–541. https://doi.org/10.1111/j.1600-0587.1999.tb01283.x (1999).
    Article  Google Scholar 

    59.
    Fischer, J. D., Cleeton, S. H., Lyons, T. P. & Miller, J. R. Urbanization and the predation paradox: The role of trophic dynamics in structuring vertebrate communities. Bioscience 62, 809–818. https://doi.org/10.1525/bio.2012.62.9.6 (2012).
    Article  Google Scholar 

    60.
    Vincze, E. et al. Does urbanization affect predation of bird nests? A meta-analysis. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00029 (2017).
    Article  Google Scholar 

    61.
    Griggio, M. & Hoi, H. An experiment on the function of the long-term pair bond period in the socially monogamous bearded reedling. Anim. Behav. 82, 1329–1335. https://doi.org/10.1016/j.anbehav.2011.09.016 (2011).
    Article  Google Scholar 

    62.
    Griffith, S. C. Cooperation and coordination in socially monogamous birds: Moving away from a focus on sexual conflict. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00455 (2019).
    Article  Google Scholar 

    63.
    Alberti, M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 30, 114–126. https://doi.org/10.1016/j.tree.2014.11.007 (2015).
    Article  PubMed  Google Scholar 

    64.
    Liebl, A. L. & Martin, L. B. Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird. Proc. Biol. Sci. 279, 4375–4381. https://doi.org/10.1098/rspb.2012.1606 (2012).
    Article  PubMed  PubMed Central  Google Scholar 

    65.
    Sepp, T., McGraw, K. J., Kaasik, A. & Giraudeau, M. A review of urban impacts on avian life-history evolution: Does city living lead to slower pace of life?. Glob. Change Biol. 24, 1452–1469. https://doi.org/10.1111/gcb.13969 (2018).
    ADS  Article  Google Scholar 

    66.
    Patricelli, G. L. & Blickley, J. L. Avian communication in urban noise: Causes and consequences of vocal adjustment. Auk 123, 639–649. https://doi.org/10.1093/auk/123.3.639 (2006).
    Article  Google Scholar 

    67.
    Grabarczyk, E. E. & Gill, S. A. Anthropogenic noise affects male house wren response to but not detection of territorial intruders. PLoS One 14, e0220576. https://doi.org/10.1371/journal.pone.0220576 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    68.
    Schroeder, J., Nakagawa, S., Cleasby, I. R. & Burke, T. Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7, e39200. https://doi.org/10.1371/journal.pone.0039200 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    69.
    Halfwerk, W. et al. Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl. Acad. Sci. 108, 14549–14554. https://doi.org/10.1073/pnas.1109091108 (2011).
    ADS  Article  PubMed  Google Scholar 

    70.
    Mariette, M. M. Acoustic cooperation: Acoustic communication regulates conflict and cooperation within the family. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00445 (2019).
    Article  Google Scholar 

    71.
    Johnstone, R. A. & Savage, J. L. Conditional cooperation and turn-taking in parental care. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00335 (2019).
    Article  Google Scholar 

    72.
    Ihle, M., Pick, J. L., Winney, I. S., Nakagawa, S. & Burke, T. Measuring up to reality: Null models and analysis simulations to study parental coordination over provisioning offspring. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00142 (2019).
    Article  Google Scholar 

    73.
    Ihle, M. et al. Rearing success does not improve with apparent pair coordination in offspring provisioning. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00405 (2019).
    Article  Google Scholar 

    74.
    Seress, G., Lipovits, A., Bokony, V. & Czuni, L. Quantifying the urban gradient: A practical method for broad measurements. Landsc. Urban Plan. 131, 42–50. https://doi.org/10.1016/j.landurbplan.2014.07.010 (2014).
    Article  Google Scholar 

    75.
    75Johnson, L. S. in The Birds of North America (ed Editor A. F. Poole) (2014).

    76.
    Pearse, A. T., Cavitt, J. F. & Cully, J. F. effects of food supplementation on female nest attentiveness and incubation mate feeding in two sympatric wren species. Wilson Bull. 116, 23–30 (2004).
    Article  Google Scholar 

    77.
    Greenewalt, C. H. & Jones, F. M. Photographic studies of the feeding of nestling house wrens. Proc. Am. Philos. Soc. 99, 200–204 (1955).
    Google Scholar 

    78.
    Welbers, A. A. M. H. et al. Artificial light at night reduces daily energy expenditure in breeding great tits (Parus major). Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00055 (2017).
    Article  Google Scholar 

    79.
    Baldan, D. & Griggio, M. Pair coordination is related to later brood desertion in a provisioning songbird. Anim. Behav. 156, 147–152. https://doi.org/10.1016/j.anbehav.2019.08.002 (2019).
    Article  Google Scholar 

    80.
    Pinheiro J, Bates D, DebRoy S, Sarkar D & Team, R. C. nlme: Linear and nonlinear mixed effects models. (2019).

    81.
    Rolinski, S., Horn, H., Petzoldt, T. & Paul, L. Identifying cardinal dates in phytoplankton time series to enable the analysis of long-term trends. Oecologia 153, 997–1008 (2007).
    ADS  Article  Google Scholar 

    82.
    Douma, J. C. & Weedon, J. T. Analysing continuous proportions in ecology and evolution: A practical introduction to beta and Dirichlet regression. Methods Ecol. Evol. 10, 1412–1430. https://doi.org/10.1111/2041-210x.13234 (2019).
    Article  Google Scholar 

    83.
    Martin, E. mclogit: Multinomial logit models, with or without random effects or overdispersion (2020).

    84.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 48 (2015).
    Article  Google Scholar 

    85.
    Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Lawrence Erlbaum Associates, Hillsdale, 1988).
    Google Scholar 

    86.
    Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol. https://doi.org/10.3389/fpsyg.2013.00863 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    87.
    Lenth, R. emmeans: Estimated marginal means, aka least-squares means. (2020). More

  • in

    Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies

    1.
    Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty P. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. N Phytol. 2019;223:1–11.
    Article  CAS  Google Scholar 
    2.
    Miller RM, Jastrow JD, Reinhardt DR. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia. 1995;103:17–23.
    CAS  PubMed  Article  Google Scholar 

    3.
    Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read DJ. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot. 2004;82:1016–45.
    Article  Google Scholar 

    4.
    Bago B, Pfeffer PE, Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 2000;124:949–58.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    5.
    Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, et al. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci. 2010;107:10938–42.
    CAS  PubMed  Article  Google Scholar 

    6.
    Giri B, Saxena B. Response of arbuscular mycorrhizal fungi to global climate change and their role in terrestrial ecosystem C and N cycling. In: Varma A, Prasad R, Tuteja N editors. Mycorrhiza—function, diversity, state of the art. Cham: Springer International Publishing; 2017. p. 305–27.

    7.
    Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI. Symbiotic options for the conquest of land. Trends Ecol Evol. 2015;30:477–86.
    PubMed  Article  Google Scholar 

    8.
    Martin FM, Uroz S, Barker DG. Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science. 2017;356:eaad4501.
    PubMed  Article  CAS  Google Scholar 

    9.
    Brundrett MC. Coevolution of roots and mycorrhizas of land plants. N Phytol. 2002;154:275–304.
    Article  Google Scholar 

    10.
    Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J, West SA, et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc Natl Acad Sci. 2018;115:5229–34.
    CAS  PubMed  Article  Google Scholar 

    11.
    Gange AC, Stagg PG, Ward LK. Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol Lett. 2002;5:11–5.
    Article  Google Scholar 

    12.
    Koricheva J, Gange AC, Jones T. Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology. 2009;90:2088–97.
    PubMed  Article  Google Scholar 

    13.
    Hart MM, Reader RJ, Klironomos JN. Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol. 2003;18:418–23.
    Article  Google Scholar 

    14.
    Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, et al. Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. N Phytol. 2014;203:233–44.
    CAS  Article  Google Scholar 

    15.
    Gerz M, Bueno CG, Zobel M, Moora M. Plant community mycorrhization in temperate forests and grasslands: relations with edaphic properties and plant diversity. J Veg Sci. 2016;27:89–99.
    Article  Google Scholar 

    16.
    He X, Critchley C, Bledsoe C. Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). CRC Crit Rev Plant Sci. 2003;22:531–67.
    Article  Google Scholar 

    17.
    Smith, Sally E., and David J. Read. Mycorrhizal symbiosis. 3rd edn. (Academic press, London, 2008).

    18.
    Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science. 2017;356:1175–8.
    CAS  PubMed  Article  Google Scholar 

    19.
    Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL. Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza. 2000;9:331–6.
    CAS  Article  Google Scholar 

    20.
    Azcón R, Ambrosano E, Charest C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci. 2003;165:1137–45.
    Article  CAS  Google Scholar 

    21.
    Ramírez-Viga TK, Aguilar R, Castillo-Argüero S, Chiappa-Carrara X, Guadarrama P, Ramos-Zapata J. Wetland plant species improve performance when inoculated with arbuscular mycorrhizal fungi: a meta-analysis of experimental pot studies. Mycorrhiza. 2018;28:477–93.
    PubMed  Article  Google Scholar 

    22.
    Weremijewicz J, Janos DP. Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. N Phytol. 2013;198:203–13.
    CAS  Article  Google Scholar 

    23.
    Bücking H, Shachar-Hill Y. Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. N Phytol. 2005;165:899–912.
    Article  CAS  Google Scholar 

    24.
    Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, et al. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci. 2012;109:2666–71.
    CAS  PubMed  Article  Google Scholar 

    25.
    Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, et al. Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. N Phytol. 2014;203:646–56.
    CAS  Article  Google Scholar 

    26.
    Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J. Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Front Plant Sci. 2015;6:1–11.
    Article  Google Scholar 

    27.
    Zheng C, Ji B, Zhang J, Zhang F, Bever JD. Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. N Phytol. 2015;205:361–8.
    CAS  Article  Google Scholar 

    28.
    Varga S, Kytöviita M. Mycorrhizal benefit differs among the sexes in a gynodioecious species. Ecology. 2010;91:2583–93.
    PubMed  Article  Google Scholar 

    29.
    Merrild MP, Ambus P, Rosendahl S, Jakobsen I. Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. N Phytol. 2013;200:229–40.
    CAS  Article  Google Scholar 

    30.
    Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. N Phytol. 2015;205:1632–45.
    CAS  Article  Google Scholar 

    31.
    Weremijewicz J, Sternberg L, da SLO, Janos DP. Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. N Phytol. 2016;212:461–71.
    CAS  Article  Google Scholar 

    32.
    Werner GDA, Kiers ET. Partner selection in the mycorrhizal mutualism. N Phytol. 2015;205:1437–42.
    Article  Google Scholar 

    33.
    Bachelot B, Lee CT. Dynamic preferential allocation to arbuscular mycorrhizal fungi explains fungal succession and coexistence. Ecology. 2018;99:372–84.
    PubMed  Article  Google Scholar 

    34.
    Wyatt GAK, Kiers ET, Gardner A, West SA. A biological market analysis of the plant-mycorrhizal symbiosis. Evolution. 2014;68:2603–18.
    PubMed  Article  Google Scholar 

    35.
    Noë R, Kiers ET. Mycorrhizal markets, firms, and co-ops. Trends Ecol Evol. 2018;33:777–89.
    PubMed  Article  Google Scholar 

    36.
    Bender SF, Wagg C, van der Heijden MGA. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol. 2016;31:440–52.
    PubMed  Article  Google Scholar 

    37.
    Konvalinková T, Jansa J. Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci. 2016;7:1–11.
    Article  Google Scholar 

    38.
    Whiteside MD, Werner GDAA, Caldas VEA, van’t Padje A, Dupin SE, Elbers B, et al. Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Curr Biol. 2019;29:2043–50.e8.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    39.
    Bailey RE, Nie S. Alloyed semiconductor quantum dots: tuning the optical properties without changing the particle size. J Am Chem Soc. 2003;125:7100–6.
    CAS  PubMed  Article  Google Scholar 

    40.
    Jang E, Jun S, Pu L. High quality CdSeS nanocrystals synthesized by facile single injection process and their electroluminescence. Chem Commun. 2003;24:2964–5.

    41.
    Declerck S, Fortin JA, Strullu DG (eds). In vitro culture of mycorrhizas. Berlin, Heidelberg: Springer; 2005.

    42.
    Engelmoer DJP, Behm JE, Kiers ET. Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol. 2014;23:1584–93.
    CAS  PubMed  Article  Google Scholar 

    43.
    Ness RLL, Vlek PLG. Mechanism of calcium and phosphate release from hydroxy-apatite by mycorrhizal hyphae. Soil Sci Soc Am J. 2000;64:949–55.
    CAS  Article  Google Scholar 

    44.
    Tang I-M, Krishnamra N, Charoenphandhu N, Hoonsawat R, Pon-On W. Biomagnetic of apatite-coated cobalt ferrite: a core–shell particle for protein adsorption and pH-controlled release. Nanoscale Res Lett. 2010;6:19.
    PubMed  PubMed Central  Google Scholar 

    45.
    Kawashita M, Taninai K, Li Z, Ishikawa K, Yoshida Y. Preparation of low-crystalline apatite nanoparticles and their coating onto quartz substrates. J Mater Sci Mater Med. 2012;23:1355–62.
    CAS  PubMed  Article  Google Scholar 

    46.
    Sun S, Chan LS, Li Y-L. Flower-like apatite recording microbial processes through deep geological time and its implication to the search for mineral records of life on Mars. Am Miner. 2014;99:2116–25.
    Article  Google Scholar 

    47.
    Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333:880–2.
    CAS  PubMed  Article  Google Scholar 

    48.
    R core team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. https://www.r-project.org/.

    49.
    Walker C. A simple blue staining technique for arbuscular mycorrhizal and other root-inhabiting fung. Inoculum. 2005;56:68–9.
    Google Scholar 

    50.
    Rossow MJ, Sasaki JM, Digman MA, Gratton E. Raster image correlation spectroscopy in live cells. Nat Protoc. 2010;5:1761–74.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Whiteside MD, Digman MA, Gratton E, Treseder KK. Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biol Biochem. 2012;55:7–13.
    CAS  Article  Google Scholar 

    52.
    Bates D, Mächler M, Bolker B, Walker S. “Fitting Linear Mixed-Effects Models Using lme4.” Journal of Statistical Software. 2015. 67;1:1–48.

    53.
    Kuznetsova A, Brockhoff PB, Christensen RHB (2017). “lmerTest Package: Tests in Linear Mixed Effects Models.” Journal of Statistical Software. 2017. 82;13:1–26.

    54.
    Fox J, Weisberg S. An R companion to applied regression. 2nd edn (Sage Publications, Inc, Thousand Oaks CA, 2016).

    55.
    Javot H, Pumplin N, Harrison MJ. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ. 2007;30:310–22.
    CAS  PubMed  Article  Google Scholar 

    56.
    Konečný J, Hršelová H, Bukovská P, Hujslová M, Jansa J. Correlative evidence for co-regulation of phosphorus and carbon exchanges with symbiotic fungus in the arbuscular mycorrhizal Medicago truncatula. PLoS ONE. 2019;14:1–24.
    Article  CAS  Google Scholar 

    57.
    Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife. 2017;6:1–33.
    Article  Google Scholar 

    58.
    Burleigh SH, Cavagnaro T, Jakobsen I. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot. 2002;53:1593–601.
    CAS  PubMed  Article  Google Scholar 

    59.
    Smith SE. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 2003;133:16–20.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    60.
    Grønlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I. The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant. 2013;149:234–48.
    PubMed  Article  CAS  Google Scholar 

    61.
    Smith SE, Smith FA, Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. N Phytol. 2004;162:511–24.
    Article  Google Scholar 

    62.
    Watts-Williams SJ, Jakobsen I, Cavagnaro TR, Grønlund M. Local and distal effects of arbuscular mycorrhizal colonization on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot. 2015;66:4061–73.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Pel R, Dupin S, Schat H, Ellers J, Kiers ET, van Straalen NM. Growth benefits provided by different arbuscular mycorrhizal fungi to Plantago lanceolata depend on the form of available phosphorus. Eur J Soil Biol. 2018;88:89–96.
    CAS  Article  Google Scholar 

    64.
    Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA. Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia. 2006;147:348–58.
    PubMed  Article  Google Scholar 

    65.
    Lu R, Drubin DG, Sun Y. Clathrin-mediated endocytosis in budding yeast at a glance. J Cell Sci. 2016;129:1531–6.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    66.
    Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J Microsc. 2000;198:246–59.
    CAS  PubMed  Article  Google Scholar 

    67.
    Read ND, Kalkman ER. Does endocytosis occur in fungal hyphae? Fungal Genet Biol. 2003;39:199–203.
    CAS  PubMed  Article  Google Scholar 

    68.
    Epp E, Nazarova E, Regan H, Douglas LM, Konopka JB, Vogel J, et al. Clathrin- and arp2/3-independent endocytosis in the fungal pathogen Candida albicans. MBio. 2013;4:e00476–13.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    Colin Y, Nicolitch O, Turpault MP, Uroz S. Mineral types and tree species determine the functional and taxonomic structures of forest soil bacterial communities. Appl Environ Microbiol. 2017;83:1–23.
    Article  Google Scholar 

    70.
    Fontaine L, Thiffault N, Paré D, Fortin J-A, Piché Y. Phosphate-solubilizing bacteria isolated from ectomycorrhizal mycelium of Picea glauca are highly efficient at fluorapatite weathering. Botany. 2016;94:1183–93.
    CAS  Article  Google Scholar 

    71.
    Alloush GA, Clark RB. Maize response to phosphate rock and arbuscular mycorrhizal fungi in acidic soil. Commun Soil Sci Plant Anal. 2001;32:231–54.
    CAS  Article  Google Scholar 

    72.
    Powell CL, Daniel J. Mycorrhizal fungi stimulate uptake of soluble and insoluble phosphate fertilizer from a phosphate‐deficient soil. N Phytol. 1978;80:351–8.
    CAS  Article  Google Scholar 

    73.
    Jakobsen I, Hammer EC. Nutrient dynamics in arbuscular mycorrhizal networks. In: Horton TR, editor. Mycorrhizal networks. Dordrecht: Springer Netherlands; 2015. p. 91–131.

    74.
    Marler MJ, Zabinski CA, Callaway RM. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology. 1999;80:1180–6.
    Article  Google Scholar 

    75.
    Carey EV, Marler MJ, Callaway RM. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol. 2004;172:133–41.
    Article  Google Scholar 

    76.
    van der Heijden MGA. Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett. 2004;7:293–303.
    Article  Google Scholar 

    77.
    van der Heijden MGA, Horton TR. Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol. 2009;97:1139–50.
    Article  Google Scholar 

    78.
    Digman MA, Brown CM, Sengupta P, Wiseman PW, Horwitz AR, Gratton E. Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophys J. 2005;89:1317–27.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    79.
    Nieves DJ, Li Y, Fernig DG, Levy R. Photothermal raster image correlation spectroscopy of gold nanoparticles in solution and on live cells. R Soc Open Sci. 2015;2:140454.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    80.
    Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. N Phytol. 1997;135:575–85.
    Article  Google Scholar 

    81.
    Johnson NC, Wilson JA, Bowker MA, Wilson JA, Miller RM. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci. 2010;107:2093–8.
    CAS  PubMed  Article  Google Scholar 

    82.
    Argüello A, O’Brien MJ, van der Heijden MGA, Wiemken A, Schmid B, Niklaus PA. Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism. Ecol Lett. 2016;19:648–56.
    PubMed  Article  Google Scholar 

    83.
    Noë R, Hammerstein P. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol. 1994;35:1–11.
    Article  Google Scholar 

    84.
    Werner GDA, Strassmann JE, Ivens ABF, Engelmoer DJP, Verbruggen E, Queller DC, et al. Evolution of microbial markets. Proc Natl Acad Sci. 2014;111:1237–44.
    CAS  PubMed  Article  Google Scholar 

    85.
    Musat N, Musat F, Weber PK, Pett-Ridge J. Tracking microbial interactions with NanoSIMS. Curr Opin Biotechnol. 2016;41:114–21.
    CAS  PubMed  Article  Google Scholar 

    86.
    Bücking H, Mensah JA, Fellbaum CR. Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. Commun Integr Biol. 2016;9:1–4.
    Article  CAS  Google Scholar 

    87.
    Roger A, Colard A, Angelard C, Sanders IR. Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J. 2013;7:2137–46.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    88.
    Wagg C, Jansa J, Schmid B, van der Heijden MGA. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett. 2011;14:1001–9.
    PubMed  Article  Google Scholar 

    89.
    Douglas AE. Conflict, cheats and the persistence of symbioses. N Phytol. 2008;177:849–58.
    Article  Google Scholar  More