More stories

  • in

    Livestock grazing impact differently on the functional diversity of dung beetles depending on the regional context in subtropical forests

    1.Herrero, M. et al. Livestock and the environment: What have we learned in the past decade?. Annu. Rev. Environ. Resour. 40, 177–202 (2015).
    Google Scholar 
    2.Robinson, T. P. et al. Mapping the global distribution of livestock. PLoS ONE 9, e96084 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    3.Firbank, L. G., Petit, S., Smart, S., Blain, A. & Fuller, R. J. Assessing the impacts of agricultural intensification on biodiversity: A British perspective. Philos. Trans. R. Soc. B: Biol. Sci. 363, 777–787 (2007).
    Google Scholar 
    4.Laurance, W. F., Sayer, J. & Cassman, K. G. Agricultural expansion and its impacts on tropical nature. Trends Ecol. Evol. 29, 107–116 (2014).PubMed 

    Google Scholar 
    5.Steinfeld, H., de Haan, C. & Blackburn, H. Livestock—Environment Interactions 88 (WRENmedia, 1997).
    Google Scholar 
    6.Eldridge, D. J., Poore, A. G. B., Ruiz-Colmenero, M., Letnic, M. & Soliveres, S. Ecosystem structure, function, and composition in rangelands are negatively affected by livestock grazing. Ecol. Appl. 26, 1273–1283 (2016).PubMed 

    Google Scholar 
    7.Schieltz, J. M. & Rubenstein, D. I. Evidence based review: Positive versus negative effects of livestock grazing on wildlife. What do we really know?. Environ. Res. Lett. 11, 113003 (2016).ADS 

    Google Scholar 
    8.Cornwell, W. K. & Ackerly, D. D. Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol. Monogr. 79, 109–126 (2009).
    Google Scholar 
    9.Kraft, N. J. B. et al. Community assembly, coexistence and the environmental filtering metaphor. Funct. Ecol. 29, 592–599 (2015).
    Google Scholar 
    10.Keddy, P. A. Assembly and response rules: Two goals for predictive community ecology. J. Veg. Sci. 3, 157–164 (1992).
    Google Scholar 
    11.Pärtel, M., Zobel, M., Zobel, K., van der Maarel, E. & Partel, M. The species pool and its relation to species richness: Evidence from Estonian plant communities. Oikos 75, 111–117 (1996).
    Google Scholar 
    12.Temperton, V., Hobbs, R. J., Nuttle, T. & Halle, S. Assembly Rules and Restoration Ecology. Bridging the Gap Between Theory and Practice (Island Press, 2004).
    Google Scholar 
    13.Leibold, M. A. Similarity and local co-existence of species in regional biotas. Evol. Ecol. 12, 95–110 (1998).
    Google Scholar 
    14.Hortal, J. et al. Ice age climate, evolutionary constraints and diversity patterns of European dung beetles: Ice age determines European scarab diversity. Ecol. Lett. 14, 741–748 (2011).PubMed 

    Google Scholar 
    15.de Bello, F., Lepš, J. & Sebastià, M.-T. Variations in species and functional plant diversity along climatic and grazing gradients. Ecography 29, 801–810 (2006).
    Google Scholar 
    16.Reymond, A., Purcell, J., Cherix, D., Guisan, A. & Pellissier, L. Functional diversity decreases with temperature in high elevation ant fauna: Functional diversity in high elevation ant. Ecol. Entomol. 38, 364–373 (2013).
    Google Scholar 
    17.Safi, K. et al. Understanding global patterns of mammalian functional and phylogenetic diversity. Philos. Trans. R. Soc. B 366, 2536–2544 (2011).
    Google Scholar 
    18.Mason-Romo, E. D., Farías, A. A. & Ceballos, G. Two decades of climate driving the dynamics of functional and taxonomic diversity of a tropical small mammal community in western Mexico. PLoS ONE 12, e0189104 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    19.Wen, Z. et al. Functional diversity overrides community-weighted mean traits in linking land-use intensity to hydrological ecosystem services. Sci. Total Environ. 682, 583–590 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    20Corbelli, J. M. et al. Integrating taxonomic, functional and phylogenetic beta diversities: Interactive effects with the biome and land use across taxa. PLoS ONE 10, e0126854 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    21.Flynn, D. F. B. et al. Loss of functional diversity under land use intensification across multiple taxa. Ecol. Lett. 12, 22–33 (2009).PubMed 

    Google Scholar 
    22.Spector, S. Scarabaeine dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae): An invertebrate focal taxon for biodiversity research and conservation. Coleopt. Bull. 60, 71–83 (2006).
    Google Scholar 
    23.Gardner, T. A. et al. The cost-effectiveness of biodiversity surveys in tropical forests: Cost-effectiveness of biodiversity surveys. Ecol. Lett. 11, 139–150 (2008).PubMed 

    Google Scholar 
    24.Mason, N. W. H., Mouillot, D., Lee, W. G. & Wilson, J. B. Functional richness, functional evenness and functional divergence: The primary components of functional diversity. Oikos 111, 112–118 (2005).
    Google Scholar 
    25.Villéger, S., Mason, N. W. H. & Mouillot, D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89, 2290–2301 (2008).PubMed 

    Google Scholar 
    26.Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).PubMed 

    Google Scholar 
    27.Audino, L. D., Louzada, J. & Comita, L. Dung beetles as indicators of tropical forest restoration success: Is it possible to recover species and functional diversity?. Biol. Cons. 169, 248–257 (2014).
    Google Scholar 
    28.Barragán, F., Moreno, C. E., Escobar, F., Halffter, G. & Navarrete, D. Negative impacts of human land use on dung beetle functional diversity. PLoS ONE 6, e17976 (2011).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Correa, C. M. A., Braga, R. F., Puker, A. & Korasaki, V. Patterns of taxonomic and functional diversity of dung beetles in a human-modified variegated landscape in Brazilian Cerrado. J. Insect Conserv. 23, 89–99 (2019).
    Google Scholar 
    30.Gómez-Cifuentes, A., Munevar, A., Gimenez, V. C., Gatti, M. G. & Zurita, G. A. Influence of land use on the taxonomic and functional diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina. J. Insect Conserv. 21, 147–156 (2017).
    Google Scholar 
    31.Guerra Alonso, C. B., Zurita, G. A. & Bellocq, M. I. Dung beetles response to livestock management in three different regional contexts. Sci. Rep. 10, 3702 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32de Siqueira Neves, F. et al. Successional and seasonal changes in a community of dung beetles (Coleoptera: Scarabaeinae) in a Brazilian tropical dry forest. Nat. Conserv. 08, 160–164 (2010).
    Google Scholar 
    33Kottek, M., Grieser, J., Beck, C., Rudolf, B. & Rubel, F. World Map of the Köppen-Geiger climate classification updated. Meteorol. Z. 15, 259–263 (2006).
    Google Scholar 
    34.Brown, A. La situación ambiental Argentina 2005 (Fundación Vida Silvestre Argentina, 2006).
    Google Scholar 
    35.Larsen, T. H., Lopera, A. & Forsyth, A. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Coleopt. Bull. 60, 315–324 (2006).
    Google Scholar 
    36Vaz-de-Mello, F. Z. A Multilingual Key to the Genera and Subgenera of the Subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae) (Magnolia Press, 2011).
    Google Scholar 
    37.Braun-Blanquet, J. Fitosociología [Phytosociology]. Bases para el estudio de las comunidades vegetales [Basis for the study of plant communities] 820 (Editorial H. Blume, 1979).
    Google Scholar 
    38.Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Google Scholar 
    39Scholtz, C. H., Davis, A. L. V. & Kryger, U. Evolutionary Biology and Conservation of Dung Beetles (Pensoft, 2009).
    Google Scholar 
    40.Simmons, L. W. & Ridsdill-Smith, J. Reproductive competition and its impact on the evolution and ecology of dung beetles. In Ecology and Evolution of Dung Beetles (eds Simmons, L. W. & Ridsdill-Smith, T. J.) 1–20 (Wiley, 2011). https://doi.org/10.1002/9781444342000.ch1.Chapter 

    Google Scholar 
    41.Vaz-de-Mello, F. Scarabaeidae in Catálogo Taxonômico da Fauna do Brasil. Catálogo Taxonômico da Fauna do Brasil. http://fauna.jbrj.gov.br/fauna/faunadobrasil/128171 (2018).42.Zunino, M. Food relocation behaviour: A multivalent strategy of Coleoptera. In Advances in Coleopterology (eds Zunino, M. et al.) 297–314 (AEC, 1991).
    Google Scholar 
    43.LaBarbera, M. Analyzing body size as a factor in ecology and evolution. Ann. Rev. Ecol. Syst. 20, 97–117 (1989).
    Google Scholar 
    44Soto, C. S., Giombini, M. I., Giménez Gómez, V. C. & Zurita, G. A. Phenotypic differentiation in a resilient dung beetle species induced by forest conversion into cattle pastures. Evol. Ecol. 33, 385–402 (2019).
    Google Scholar 
    45.Laliberté, E., Legendre, P. & Shipley, B. Package ‘FD’. Measuring Functional Diversity (FD) from Multiple Traits, and Other Tools for Functional Ecology (2014).46.Gower, J. C. A general coefficient of similarity and some of its properties. Biometrics 27, 857 (1971).
    Google Scholar 
    47.Pavoine, S., Vallet, J., Dufour, A.-B., Gachet, S. & Daniel, H. On the challenge of treating various types of variables: Application for improving the measurement of functional diversity. Oikos 118, 391–402 (2009).
    Google Scholar 
    48.Moran, P. A. P. Notes on continuous stochastic phenomena. Biometrika 37, 17–23 (1950).MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    49.Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems: Data exploration. Methods Ecol. Evol. 1, 3–14 (2010).
    Google Scholar 
    50.Lavorel, S. et al. Assessing functional diversity in the field—Methodology matters!. Funct. Ecol. 22, 134–147 (2008).
    Google Scholar 
    51.Oksanen, J. et al. vegan: Community Ecology Package (2017).52.Clarke, K. R. & Green, R. H. Statistical design and analysis for a ‘biological effects’ study. Mar. Ecol. Prog. Ser. 46, 213–226 (1988).ADS 

    Google Scholar 
    53.da Silva, P. G. & Cassenote, S. Environmental drivers of species composition and functional diversity of dung beetles along the Atlantic Forest-Pampa transition zone. Austral. Ecol. 44, 786–799 (2019).
    Google Scholar 
    54.Giraldo, C., Escobar, F., Chará, J. D. & Calle, Z. The adoption of silvopastoral systems promotes the recovery of ecological processes regulated by dung beetles in the Colombian Andes: Ecological processes regulated by dung beetles. Insect Conserv. Divers. 4, 115–122 (2011).
    Google Scholar 
    55.Nichols, E. et al. Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales. Ecology 94, 180–189 (2013).PubMed 

    Google Scholar 
    56Gómez-Cifuentes, A., Giménez Gómez, V. C., Moreno, C. E. & Zurita, G. A. Tree retention in cattle ranching systems partially preserves dung beetle diversity and functional groups in the semideciduous Atlantic forest: The role of microclimate and soil conditions. Basic Appl. Ecol. 34, 64–74 (2019).
    Google Scholar 
    57.Cerullo, G. R., Edwards, F. A., Mills, S. C. & Edwards, D. P. Tropical forest subjected to intensive post-logging silviculture maintains functionally diverse dung beetle communities. For. Ecol. Manage. 444, 318–326 (2019).
    Google Scholar 
    58.Filloy, J., Zurita, G. A., Corbelli, J. M. & Bellocq, M. I. On the similarity among bird communities: Testing the influence of distance and land use. Acta Oecol. 36, 333–338 (2010).ADS 

    Google Scholar 
    59.Chown, S. L., Sørensen, J. G. & Terblanche, J. S. Water loss in insects: An environmental change perspective. J. Insect Physiol. 57, 1070–1084 (2011).CAS 
    PubMed 

    Google Scholar 
    60.Duncan, F. D. & Byrne, M. J. Discontinuous gas exchange in dung beetles: Patterns and ecological implications. Oecologia 122, 452–458 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    61.Lobo, J. M., Lumaret, J.-P. & Jay-Robert, P. Sampling dung beetles in the French Mediterranean area: Effects of abiotic factors and farm practices. Pedobiología 42(3), 252–266 (1998).
    Google Scholar 
    62.Navarrete, D. & Halffter, G. Dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity in continuous forest, forest fragments and cattle pastures in a landscape of Chiapas, Mexico: The effects of anthropogenic changes. Biodivers. Conserv. 17, 2869–2898 (2008).
    Google Scholar 
    63.Verdú, J. R., Arellano, L. & Numa, C. Thermoregulation in endothermic dung beetles (Coleoptera: Scarabaeidae): Effect of body size and ecophysiological constraints in flight. J. Insect Physiol. 52, 854–860 (2006).PubMed 

    Google Scholar 
    64.Davis, A. J., Huijbregts, H. & Krikken, J. The role of local and regional processes in shaping dung beetle communities in tropical forest plantations in Borneo. Glob. Ecol. 9, 281–292 (2000).
    Google Scholar 
    65.Tuff, K. T., Tuff, T. & Davies, K. F. A framework for integrating thermal biology into fragmentation research. Ecol. Lett. 19, 361–374 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.Davis, A. L. V. Habitat fragmentation in southern Africa and distributional response patterns in five specialist or generalist dung beetle families (Coleoptera). Afr. J. Ecol. 32, 192–207 (1994).
    Google Scholar 
    67.Halffter, G. & Arellano, L. Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34, 144–154 (2002).
    Google Scholar 
    68.Hill, C. Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles. J. Trop. Ecol. 12, 449–460 (1996).
    Google Scholar 
    69.Supp, S. R. & Ernest, S. K. M. Species-level and community-level responses to disturbance: A cross-community analysis. Ecology 95, 1717–1723 (2014).PubMed 

    Google Scholar 
    70.Davis, A. L. V., Scholtz, C. H. & Deschodt, C. Multi-scale determinants of dung beetle assemblage structure across abiotic gradients of the Kalahari-Nama Karoo ecotone, South Africa. J. Biogeogr. 35, 1465–1480 (2008).
    Google Scholar 
    71.Nervo, B., Tocco, C., Caprio, E., Palestrini, C. & Rolando, A. The effects of body mass on dung removal efficiency in dung beetles. PLoS ONE 9, e107699 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Bui, V. B., Ziegler, T. & Bonkowski, M. Morphological traits reflect dung beetle response to land use changes in tropical karst ecosystems of Vietnam. Ecol. Ind. 108, 105697 (2020).
    Google Scholar 
    73.Giménez Gómez, V. C., Verdú, J. R. & Zurita, G. A. Thermal niche helps to explain the ability of dung beetles to exploit disturbed habitats. Sci. Rep. 10, 13364 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    74.Verdú, J. R., Alba-Tercedor, J. & Jiménez-Manrique, M. Evidence of different thermoregulatory mechanisms between two sympatric Scarabaeus species using infrared thermography and micro-computer tomography. PLoS ONE 7, e33914 (2012).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    75.Gómez-Cifuentes, A., Vespa, N., Semmartín, M. & Zurita, G. Canopy cover is a key factor to preserve the ecological functions of dung beetles in the southern Atlantic Forest. Appl. Soil. Ecol. 154, 103652 (2020).
    Google Scholar 
    76.Fernández, P. D. et al. Understanding the distribution of cattle production systems in the South American Chaco. J. Land Use Sci. 15, 52–68 (2020).
    Google Scholar 
    77Grau, H. R. & Aide, M. Globalization and land-use transitions in Latin America. Ecol. Soc. 13, 16 (2008).
    Google Scholar 
    78.Mastrangelo, M. E. & Gavin, M. C. Trade-offs between cattle production and bird conservation in an agricultural frontier of the Gran Chaco of Argentina. Conserv. Biol. 26, 1040–1051 (2012).PubMed 

    Google Scholar 
    79.Macchi, L. et al. Thresholds in forest bird communities along woody vegetation gradients in the South American Dry Chaco. J. Appl. Ecol. 56, 629–639 (2019).
    Google Scholar 
    80.Díaz, S. & Cabido, M. Vive la différence: Plant functional diversity matters to ecosystem processes. Trends Ecol. Evol. 16, 646–655 (2001).
    Google Scholar 
    81.Slade, E. M., Mann, D. J., Villanueva, J. F. & Lewis, O. T. Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. J. Anim. Ecol. 76, 1094–1104 (2007).PubMed 

    Google Scholar 
    82.Ortega-Martínez, I. J., Moreno, C. E. & Escobar, F. A dirty job: manure removal by dung beetles in both a cattle ranch and laboratory setting. Entomol. Exp. Appl. 161, 70–78 (2016).
    Google Scholar  More

  • in

    Ozone damage costs billions

    Tropospheric ozone is formed through the oxidation of precursor pollutants (nitrogen oxide gases and volatile organic compounds) in the presence of sunlight. This surface ozone — a major pollutant — contributes negatively to air quality, posing risks to human health. Many plant species are also sensitive to ozone, exhibiting reduced growth and seed production, and accelerated ageing. Such impacts translate to high crop yield losses, threatening food security, especially in light of rising ozone concentrations and exposure observed across Asia. More

  • in

    Egg-laying increases body temperature to an annual maximum in a wild bird

    1.Perrins, C. M. Eggs, egg formation and the timing of breeding. Ibis (Lond. 1859). 138, 2–15. https://doi.org/10.1111/j.1474-919X.1996.tb04308.x (1996).Article 

    Google Scholar 
    2.Monaghan, P. & Nager, R. G. Why don’t birds lay more eggs? Trends Ecol. Evol. 12, 270–274. https://doi.org/10.1016/S0169-5347(97)01094-X (1997).CAS 
    Article 

    Google Scholar 
    3.Alisauskas, R., DeVink, J.-M. Breeding costs, nutrient reserves, and cross-seasonal effects: dealing with deficits in sea ducks. pp. 125–168 (2015).4.Ebeid, T., Tumova Prague (Czech Republic). Katedra Chovu Prasat a Drubeze) E (Ceska ZU. In press. Physiological aspects of oviposition and its role in egg quality. A review. Sci. Agric. Bohem. (Czech Republic). v. 35.5.Johnson, A. The avian ovary and follicle development: some comparative and practical insights. Turkish J. Vet. Anim. Sci. 38, 660–669 (2014).CAS 
    Article 

    Google Scholar 
    6.Bédécarrats, G. Y., Baxter, M. & Sparling, B. An updated model to describe the neuroendocrine control of reproduction in chickens. Gen. Comp. Endocrinol. 227, 58–63. https://doi.org/10.1016/j.ygcen.2015.09.023 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    7.Brommer, J. E., Rattiste, K. & Wilson, A. J. Exploring plasticity in the wild: laying date-temperature reaction norms in the common gull Larus canus. Proc. R. Soc. B Biol. Sci. 275, 687–693. https://doi.org/10.1098/rspb.2007.0951 (2008).Article 

    Google Scholar 
    8.Schaper, S. V. et al. Increasing Temperature, Not Mean Temperature, Is a Cue for Avian Timing of Reproduction. Am. Nat. 179, E55–E69. https://doi.org/10.1086/663675 (2012).Article 
    PubMed 

    Google Scholar 
    9.Shave, A., Garroway, C. J., Siegrist, J. & Fraser, K. C. Timing to temperature: Egg-laying dates respond to temperature and are under stronger selection at northern latitudes. Ecosphere 10, e02974. https://doi.org/10.1002/ecs2.2974 (2019).Article 

    Google Scholar 
    10.Verhagen, I., Tomotani, B. M., Gienapp, P. & Visser, M. E. Temperature has a causal and plastic effect on timing of breeding in a small songbird. J. Exp. Biol. https://doi.org/10.1242/jeb.218784 (2020).Article 
    PubMed 

    Google Scholar 
    11.Caro, S. P., Schaper, S. V., Hut, R. A., Ball, G. F. & Visser, M. E. The case of the missing mechanism: How does temperature influence seasonal timing in endotherms?. PLoS Biol. 11, e1001517–e1001517. https://doi.org/10.1371/journal.pbio.1001517 (2013).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    12.Bobr, L. W. & Sheldon, B. L. Analysis of ovulation-oviposition patterns in the domestic fowl by telemetry measurement of deep body temperature. Aust. J. Biol. Sci. 30, 243–257. https://doi.org/10.1071/bi9770243 (1977).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Kadono, H., Besch, E. L. & Usami, E. Body temperature, oviposition, and food intake in the hen during continuous light. J. Appl. Physiol. 51, 1145–1149. https://doi.org/10.1152/jappl.1981.51.5.1145 (1981).CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Yang, J., Morgan, J. L., Kirby, J. D., Long, D. W. & Bacon a W.,. Circadian rhythm of the preovulatory surge of luteinizing hormone and its relationships to rhythms of body temperature and locomotor activity in turkey hens. Biol. Reprod. 62, 1452–1458. https://doi.org/10.1095/biolreprod62.5.1452 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    15.Zivkovic, B. D., Underwood, H. & Siopes, T. Circadian ovulatory rhythms in Japanese quail: role of ocular and extraocular pacemakers. J. Biol. Rhythms 15, 172–183. https://doi.org/10.1177/074873040001500211 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    16.Ward, S. Energy expenditure of female barn swallows Hirundo rustica during egg formation. Physiol. Zool. 69, 930–951. https://doi.org/10.1086/physzool.69.4.30164236 (1996).Article 

    Google Scholar 
    17.Nilsson, J. -Å. & Råberg, L. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128, 187–192. https://doi.org/10.1007/s004420100653 (2001).ADS 
    Article 
    PubMed 

    Google Scholar 
    18.Vézina, F. & Williams, T. D. Metabolic costs of egg production in the European starling (Sturnus vulgaris). Physiol. Biochem. Zool. 75, 377–385. https://doi.org/10.1086/343137 (2002).Article 
    PubMed 

    Google Scholar 
    19.Götmark, F. The Effects of Investigator Disturbance on Nesting Birds BT – Current Ornithology. In ed. D.M. Power, pp. 63–104. Springer. https://doi.org/10.1007/978-1-4757-9921-7_3 (1992).20.Lyngs, P. Status of the Danish Breeding population of Eiders Somateria mollissima 1988–93. Dansk Ornitol. Foren. Tidsskr. 94, 12–18 (2000).
    Google Scholar 
    21.Bolduc, F. & Guillemette, M. Human disturbance and nesting success of Common Eiders: interaction between visitors and gulls. Biol. Conserv. 110, 77–83. https://doi.org/10.1016/S0006-3207(02)00178-7 (2003).Article 

    Google Scholar 
    22.Christensen, T. K. Female pre-nesting foraging and male vigilance in Common Eider Somateria mollissima. Bird Study 47, 311–319. https://doi.org/10.1080/00063650009461191 (2000).Article 

    Google Scholar 
    23.Guillemette, M. Foraging before spring migration and before breeding in common eiders: Does hyperphagia occur?. Condor 103, 633–638 (2001).Article 

    Google Scholar 
    24.Guillemette, M. & Ouellet, J. Temporary flightlessness as a potential cost of reproduction in pre-laying Common Eiders Somateria mollissima. Ibis (Lond. 1859). 147, 301–306. https://doi.org/10.1111/j.1474-919x.2005.00402.x (2005).Article 

    Google Scholar 
    25.Rigou, Y. & Guillemette, M. Foraging effort and pre-laying strategy in breeding common eiders. Waterbirds Int. J. Waterbird Biol. 33, 314–322 (2010).
    Google Scholar 
    26.Watson, M. D., Robertson, G. J. & Cooke, F. Egg-laying time and laying interval in the common eider. Condor 95, 869–878. https://doi.org/10.2307/1369424 (1993).Article 

    Google Scholar 
    27.Guillemette, M., Woakes, A. J., Flagstad, A. & Butler, P. J. Effects of data-loggers implanted for a full year in female common eiders. Condor 104, 448–452 (2002).Article 

    Google Scholar 
    28.Franzmann, N. E. Ederfuglens (Somateria m. mollissima) ynglebiologi of populationsdynamik pa° Christiansø 1973–1977. Ph.D. Diss. Copenhagen 1980.29.Pelletier, D., Guillemette, M., Grandbois, J.-M. & Butler, P. J. It is time to move: linking flight and foraging behaviour in a diving bird. Biol. Lett. 3, 357–359. https://doi.org/10.1098/rsbl.2007.0088 (2007).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Coulson, J. C. The population dynamics of the Eider Duck Somateria mollissima and evidence of extensive non-breeding by adult ducks. Ibis (Lond. 1859). 126, 525–543. https://doi.org/10.1111/j.1474-919X.1984.tb02078.x (2008).Article 

    Google Scholar 
    31.Sabourin, M. Comportement d’incubation de l’Eider à duvet (Somateria mollissima) et effet du dérangement humain dans deux colonies de l’Estuaire du Saint-Laurentle. Mémoire de maîtrise Université (2003).32.Waltho, C., Coulson, J. Egg laying, parasitism, ‘jumbo clutches’ and egg stealing. In The Common Eider, pp. 7–10. POYSER (2015).33.Guillemette, M., Ydenberg, R. C. & Himmelman, J. H. The role of energy intake rate in prey and habitat selection of common eiders Somateria mollissima in winter: a risk-sensitive interpretation. J. Anim. Ecol. 61, 599. https://doi.org/10.2307/5615 (1992).Article 

    Google Scholar 
    34.Canty, A. & Ripley, B. boot: Bootstrap R (S-Plus) functions. R Packag Vers 1, 3–20 (2017).
    Google Scholar 
    35.Carpenter J, Bithell J. Bootstrap confidence intervals: when, which, what? A practical guide for medical statisticians. Stat. Med. 19, 1141–1164 2000. https://doi.org/10.1002/(SICI)1097-0258(20000515)19:93.0.CO;2-F36.Jenssen, B., Ekker, M. & Bech, C. Thermoregulation in winter-acclimatized Common Eiders (Somateria mollissima) in air and water. Can. J. Zool. 67, 669–673. https://doi.org/10.1139/z89-096 (1989).Article 

    Google Scholar 
    37.Winget, C. M., Averkin, E. G. & Fryer, T. B. Quantitative measurement by telemetry of ovulation and oviposition in the fowl. Am. J. Physiol. 209, 853–858. https://doi.org/10.1152/ajplegacy.1965.209.4.853 (1965).CAS 
    Article 
    PubMed 

    Google Scholar 
    38.Cain, J. R. & Wilson, W. O. Multichannel telemetry system for measuring body temperature: circadian rhythms of body temperature, locomotor activity and oviposition in chickens. Poult. Sci. 50, 1437–1443. https://doi.org/10.3382/ps.0501437 (1971).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Khalil, A., Matsui, K. & Takeda, K. Responses to abrupt changes in feeding and illumination in laying hens. Turkish J. Vet. Anim. Sci. https://doi.org/10.3906/vet-0901-25 (2010).Article 

    Google Scholar 
    40.Kadono, H. & Yamade, T. Changes of body temperature related to oviposition and ovulation induced by LH in the domestic hen. Nihon Juigaku Zasshi. 47, 55–61. https://doi.org/10.1292/jvms1939.47.55 (1985).CAS 
    Article 
    PubMed 

    Google Scholar 
    41.Piccione, G. & Refinetti, R. Thermal chronobiology of domestic animals. Front. Biosci. 8, s258–s264. https://doi.org/10.2741/1040 (2003).Article 
    PubMed 

    Google Scholar 
    42.Peters DG, Rose RW. The oestrous cycle and basal body temperature in the common wombat (Vombatus ursinus). Reproduction 57, 453–460 (in press). doi:https://doi.org/10.1530/jrf.0.057045343.Rose, R. W. & Jones, S. M. The association between basal body temperature, plasma progesterone and the oestrous cycle in a marsupial, the Tasmanian bettong (Bettongia gaimardi). J. Reprod. Fertil. 106, 67–71. https://doi.org/10.1530/jrf.0.1060067 (1996).CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Graham, C. E., Warner, H., Misener, J., Collins, D. C. & Preedy, J. R. The association between basal body temperature, sexual swelling and urinary gonadal hormone levels in the menstrual cycle of the chimpanzee. J. Reprod. Fertil. 50, 23–28. https://doi.org/10.1530/jrf.0.0500023 (1977).CAS 
    Article 
    PubMed 

    Google Scholar 
    45.Nyakudya, T. T., Fuller, A., Meyer, L. C. R., Maloney, S. K. & Mitchell, D. Body temperature and physical activity correlates of the menstrual cycle in Chacma Baboons (Papio hamadryas ursinus). Am. J. Primatol. 74, 1143–1153. https://doi.org/10.1002/ajp.22073 (2012).Article 
    PubMed 

    Google Scholar 
    46.Suthar, V. S., Burfeind, O., Bonk, S., Dhami, A. J. & Heuwieser, W. Endogenous and exogenous progesterone influence body temperature in dairy cows. J. Dairy Sci. 95, 2381–2389. https://doi.org/10.3168/jds.2011-4450 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Giersch, G. E. W. et al. Menstrual cycle and thermoregulation during exercise in the heat: A systematic review and meta-analysis. J. Sci. Med. Sport 23, 1134–1140. https://doi.org/10.1016/j.jsams.2020.05.014 (2020).Article 
    PubMed 

    Google Scholar 
    48.Farmer, C. G. Parental care: The key to understanding endothermy and other convergent features in birds and mammals. Am. Nat. 155, 326–334. https://doi.org/10.1086/303323 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Koteja, P. Energy assimilation, parental care and the evolution of endothermy. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267, 479–484. https://doi.org/10.1098/rspb.2000.1025 (2000).CAS 
    Article 

    Google Scholar 
    50.Portugal, S. J. et al. Associations between resting, activity, and daily metabolic rate in free-living endotherms: No universal rule in birds and mammals. Physiol. Biochem. Zool. 89, 251–261. https://doi.org/10.1086/686322 (2016).Article 
    PubMed 

    Google Scholar 
    51.Guillemette, M., Pelletier, D., Grandbois, J.-M. & Butler, P. J. Flightlessnessand the energetic cost of wing molt in a large sea duck. Ecology 88, 2936–2945. https://doi.org/10.1890/06-1751.1 (2007).Article 
    PubMed 

    Google Scholar 
    52.Parker, H. & Holm, H. Patterns of nutrient and energy expenditure in female common eiders nesting in the high arctic. Auk 107, 660–668. https://doi.org/10.2307/4087996 (1990).Article 

    Google Scholar 
    53.Guillemette, M. & Ouellet, J.-F. Temporary flightlessness in pre-laying Common Eiders Somateria mollissima: Are females constrained by excessive wing-loading or by minimal flight muscle ratio?. Ibis (Lond. 1859). 147, 293–300. https://doi.org/10.1111/j.1474-919x.2005.00401.x (2005).Article 

    Google Scholar 
    54.Vézina, F., Speakman, J. R. & Williams, T. D. Individually variable energy management strategies in relation to energetic costs of egg production. Ecology 87, 2447–2458. https://doi.org/10.1890/0012-9658(2006)87[2447:ivemsi]2.0.co;2 (2006).Article 
    PubMed 

    Google Scholar 
    55.Bevan, R. M., Butler, P. J., Woakes, A. J. & Prince, P. A. The energy expenditure of free-ranging black-browed albatross. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 350, 119–131. https://doi.org/10.1098/rstb.1995.0146 (1995).ADS 
    Article 

    Google Scholar 
    56.Bevan, R. et al. Heart rates and abdominal temperatures of free-ranging South Georgian shags, Phalacrocorax georgianus. J. Exp. Biol. 200, 661–675 (1997).CAS 
    Article 

    Google Scholar 
    57.Woakes, A. J., Butler, P. J. & Bevan, R. M. Implantable data logging system for heart rate and body temperature: Its application to the estimation of field metabolic rates in Antarctic predators. Med. Biol. Eng. Comput. 33, 145–151. https://doi.org/10.1007/BF02523032 (1995).CAS 
    Article 
    PubMed 

    Google Scholar 
    58.Lewden, A. et al. Body surface rewarming in fully and partially hypothermic king penguins. J. Comp. Physiol. B 190, 597–609. https://doi.org/10.1007/s00360-020-01294-1 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    59.Wilson, R. P. & Grémillet, D. Body temperatures of free-living African penguins (Spheniscus demersus) and bank cormorants (Phalacrocorax neglectus). J. Exp. Biol. 199, 2215–2223 (1996).CAS 
    Article 

    Google Scholar 
    60.Schmidt, A., Alard, F. & Handrich, Y. Changes in body temperature in king penguins at sea: The result of fine adjustments in peripheral heat loss?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R608–R618. https://doi.org/10.1152/ajpregu.00826.2005 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    61.Sherer, J., Wunder, B. A. Thermoregulation of a semi-aquatic mammal, the muskrat, in air and water. 24, 249–256 (1979).62.Dyck, A. P. & MacArthur, R. A. Seasonal patterns of body temperature and activity in free-ranging beaver (Castor canadensis). Can. J. Zool. 70, 1668–1672. https://doi.org/10.1139/z92-232 (1992).Article 

    Google Scholar 
    63.Kolka, M. A. & Stephenson, L. A. Resetting the thermoregulatory set-point by endogenous estradiol or progesterone in women. Ann. N. Y. Acad. Sci. 813, 204–206. https://doi.org/10.1111/j.1749-6632.1997.tb51694.x (1997).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    64.Ubuka, T. & Bentley, G. E. Neuroendocrine control of reproduction in birds. In Hormones and reproduction of Vertebrates (ed Norris DO & Lopez KH), pp. 1–25 (2011).65.van der Klein, S. A. S., Zuidhof, M. J. & Bédécarrats, G. Y. Diurnal and seasonal dynamics affecting egg production in meat chickens: A review of mechanisms associated with reproductive dysregulation. Anim. Reprod. Sci. 213, 106257. https://doi.org/10.1016/j.anireprosci.2019.106257 (2020).Article 
    PubMed 

    Google Scholar 
    66.Tanabe, Y. Production, evolution and reproductive endocrinology of ducks. Asian-Australas. J. Anim. Sci. 5, 173–181. https://doi.org/10.5713/ajas.1992.173 (1992).Article 

    Google Scholar 
    67.Johnson, A. L. Chapter 3 – Organization and Functional Dynamics of the Avian Ovary. In (eds DO Norris, KHBT-H and R of V Lopez), pp. 71–90. Academic Press (2011). https://doi.org/10.1016/B978-0-12-374929-1.10003-468.Bluhm, C. K., Phillips, R. E. & Burke, W. H. Serum levels of luteinizing hormone (LH), prolactin, estradiol, and progesterone in laying and nonlaying canvasback ducks (Aythya valisineria). Gen. Comp. Endocrinol. 52, 1–16. https://doi.org/10.1016/0016-6480(83)90152-1 (1983).CAS 
    Article 
    PubMed 

    Google Scholar 
    69.Bluhm, C. K., Phillips, R. E. & Burke, W. H. Serum levels of luteinizing hormone, prolactin, estradiol and progesterone in laying and nonlaying mallards (Anas platyrhynchos). Biol. Reprod. 28, 295–305. https://doi.org/10.1095/biolreprod28.2.295 (1983).CAS 
    Article 
    PubMed 

    Google Scholar 
    70.Sockman, K. W. & Schwabl, H. Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen. Comp. Endocrinol. 114, 257–268. https://doi.org/10.1006/gcen.1999.7252 (1999).CAS 
    Article 
    PubMed 

    Google Scholar 
    71.Proszkowiec, M. & Rzasa, J. Variation in the ovarian and plasma progesterone and estradiol levels of the domestic hen during a pause in laying. Folia Biol. (Praha) 49, 285–289 (2001).CAS 

    Google Scholar 
    72.Proszkowiec-Weglarz, M., Rzasa, J., Słomczyńska, M. & Paczoska-Eliasiewicz, H. Steroidogenic activity of chicken ovary during pause in egg laying. Reprod. Biol. 5, 205–225 (2005).PubMed 

    Google Scholar 
    73.Nakayma, T., Suzuki, M. & Ishizuka, N. Action of progesterone on preoptic thermosensitive neurones. Nature 258, 80. https://doi.org/10.1038/258080a0 (1975).ADS 
    Article 

    Google Scholar 
    74.Hampl, R., Stárka, L. & Janský, L. Steroids and thermogenesis. Physiol. Res. 55, 123–131 (2006).CAS 
    PubMed 

    Google Scholar 
    75.Splawinski, J. A., Górka, Z., Zacny, E. & Wojtaszek, B. Hyperthermic effects of arachidonic acid, prostaglandins E2 and F2α in rats. Pflügers Arch. 374, 15–21. https://doi.org/10.1007/BF00585692 (1978).CAS 
    Article 
    PubMed 

    Google Scholar 
    76.Gray, D. A., Marais, M. & Maloney, S. K. A review of the physiology of fever in birds. J. Comp. Physiol. B 183, 297–312. https://doi.org/10.1007/s00360-012-0718-z (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    77.Hertelendy, F. & Biellier, H. V. Evidence for a physiological role of prostaglandins in oviposition by the hen. J. Reprod. Fertil. 53, 71–74. https://doi.org/10.1530/jrf.0.0530071 (1978).CAS 
    Article 
    PubMed 

    Google Scholar 
    78.Etches, R. J., Kelly, J. D., Anderson-Langmuir, C. E. & Olson, D. M. Prostaglandin production by the largest preovulatory follicles in the domestic hen (Gallus domesticus). Biol. Reprod. 43, 378–384. https://doi.org/10.1095/biolreprod43.3.378 (1990).CAS 
    Article 
    PubMed 

    Google Scholar 
    79.Takahashi, T., Tajima, H., Nakagawa-Mizuyachi, K., Nakayama, H. & Kawashima, M. Changes in prostaglandin F2α receptor bindings in the hen oviduct uterus before and after oviposition. Poult. Sci. 90, 1767–1773. https://doi.org/10.3382/ps.2010-01329 (2011).CAS 
    Article 
    PubMed 

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

    Google Scholar 
    81.Nakao, N., Ono, H. & Yoshimura, T. Thyroid hormones and seasonal reproductive neuroendocrine interactions. Reproduction 136, 1–8. https://doi.org/10.1530/REP-08-0041 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    82.Sechman, A. The role of thyroid hormones in regulation of chicken ovarian steroidogenesis. Gen. Comp. Endocrinol. 190, 68–75. https://doi.org/10.1016/J.YGCEN.2013.04.012 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    83.Gabrielsen, G., Mehlum, F., Karlsen, H., Andresen & Parker, H. Energy cost during incubation and thermoregulation in female Common Eider (Somateria mollissima). Nor. Polarinstitutt Skr. 195 (1991).84.Ardia, D. R., Pérez, J. H. & Clotfelter, E. D. Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proc. R. Soc. B Biol. Sci. 277, 1881–1888. https://doi.org/10.1098/rspb.2009.2138 (2010).Article 

    Google Scholar 
    85.Hepp, G. R. & Kennamer, R. A. Warm is better: Incubation temperature influences apparent survival and recruitment of wood ducks (Aix sponsa). PLoS ONE 7, e47777 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    86.Ipek, A., Sahan, U. & Sozcu, A. The effects of different eggshell temperatures between embryonic day 10 and 18 on broiler performance and susceptibility to ascites. Rev. Bras. Ciência Avícola 17, 387–394. https://doi.org/10.1590/1516-635X1703387-394 (2015).Article 

    Google Scholar 
    87.Haftorn, S. & Reinertsen, R. E. Regulation of body temperature and heat transfer to eggs during incubation. Ornis Scand. Scandinavian J. Ornithol. 13, 1–10. https://doi.org/10.2307/3675966 (1982).Article 

    Google Scholar 
    88.Vehrencamp, S. Body temperatures of incubating versus non-incubating roadrunners. Condor 84, 203 (1982).Article 

    Google Scholar 
    89.Evans, S. S., Repasky, E. A. & Fisher, D. T. Fever and the thermal regulation of immunity: The immune system feels the heat. Nat. Rev. Immunol. 15, 335–349. https://doi.org/10.1038/nri3843 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    90.Hupton, G., Portocarrero, S., Newman, M. & Westneat, D. F. Bacteria in the reproductive tracts of red-wingedblackbirds. Condor 105, 453–464. https://doi.org/10.1650/7246 (2003).Article 

    Google Scholar 
    91.White, J. et al. Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol. Lett. 13, 1515–1524. https://doi.org/10.1111/j.1461-0248.2010.01542.x (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    92.Hansen, C. M., Meixell, B. W., Van Hemert, C., Hare, R. F. & Hueffer, K. Microbial infections are associated with embryo mortality in arctic-nesting geese. Appl. Environ. Microbiol. 81, 5583–5592. https://doi.org/10.1128/AEM.00706-15 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    93.Barrow, P. A. & Lovell, M. A. Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathol. 20, 335–348. https://doi.org/10.1080/03079459108418769 (1991).CAS 
    Article 
    PubMed 

    Google Scholar 
    94.Mitchell, D. et al. Revisiting concepts of thermal physiology: Predicting responses of mammals to climate change. J. Anim. Ecol. 87, 956–973. https://doi.org/10.1111/1365-2656.12818 (2018).Article 
    PubMed 

    Google Scholar 
    95.van Heerwaarden, B. & Sgrò, C. M. Male fertility thermal limits predict vulnerability to climate warming. Nat. Commun. 12, 2214. https://doi.org/10.1038/s41467-021-22546-w (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    96.Guillemette, M., Polymeropoulos, E. T., Portugal, S. J. & Pelletier, D. It takes time to be cool: On the relationship between hyperthermia and body cooling in a migrating seaduck. Front. Physiol. 8, 532. https://doi.org/10.3389/fphys.2017.00532 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    97.Stillman, J. H. Heat waves, the new normal: Summertime temperature extremes will impact animals, ecosystems, and human communities. Physiology 34, 86–100. https://doi.org/10.1152/physiol.00040.2018 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    98.Schou, M. F. et al. Extreme temperatures compromise male and female fertility in a large desert bird. Nat. Commun. 12, 666. https://doi.org/10.1038/s41467-021-20937-7 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    99.Stevenson, I. R. & Bryant, D. M. Climate change and constraints on breeding. Nature 406, 366–367. https://doi.org/10.1038/35019151 (2000).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar  More

  • in

    Competition between the tadpoles of Japanese toads versus frogs

    The average water temperature and pH in tanks was 19.29 ± 0.10 °C (SE, range: 17.0–22.5) and 8.59 ± 0.01 (SE, range 8.2–8.9) respectively. There was no significant difference among treatments (water temperature: F = 0.0086, df = 5, p = 1.0000, pH: F = 0.0063, df = 5, p = 1.0000).Intraspecific competition (density = 5, 15, 50 tadpoles per tank)The density of conspecifics did not have any significant effect on survival to metamorphosis of B. j. formosus (treatment: Wald chi-square = 3.468, df = 2, p = 0.1766; block: Wald chi-square = 7.770, df = 4, p = 0.1004; Fig. 1a). However, conspecific density had a significant effect on the combined responses of variables (larval period, metamorph SUL, metamorph mass) of B. j. formosus (MANOVA treatment: Wilks’ Lambda = 0.0181, F = 10.7224, df = 6, 10, p = 0.0007; block: Wilks’ Lambda = 0.2028, F = 0.9326, df = 12, 13.52, p = 0.5441). Higher densities of conspecifics increased the duration of the larval period (treatment: F = 6.678, df = 2, 9.30, p = 0.0159; block: F = 0.817, df = 4, 0.40, p = 0.7574; Fig. 1b), and decreased size at metamorphosis (SUL—treatment: F = 49.729, df = 2, 6.94, p  More

  • in

    Heterogeneity within and among co-occurring foundation species increases biodiversity

    1.Fernández, M. H. & Vrba, E. S. Rapoport effect and biomic specialization in African mammals: revisiting the climatic variability hypothesis. J. Biogeogr. 32, 903–918 (2005).
    Google Scholar 
    2.Tokeshi, M. & Arakaki, S. Habitat complexity in aquatic systems: fractals and beyond. Hydrobiologia 685, 27–47 (2012).
    Google Scholar 
    3.Connell, J. H. Diversity in tropical rain forests and coral reefs. Science 199, 1302–1310 (1978).ADS 
    CAS 
    PubMed 

    Google Scholar 
    4.Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. 96, 1463–1468 (1999).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Tilman, D., Reich, P. B. & Knops, J. M. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    6.Willig, M. R., Kaufman, D. M. & Stevens, R. D. Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Ann. Rev. Ecol. Evol. Syst. 34, 273–309 (2003).
    Google Scholar 
    7.Stein, A., Gerstner, K. & Kreft, H. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol. Lett. 17, 866–880 (2014).PubMed 

    Google Scholar 
    8.Thomsen, M. S. et al. Secondary foundation species enhance biodiversity. Nat. Ecol. Evol. 2, 634–639 (2018).PubMed 

    Google Scholar 
    9.Mac Arthur, R. H. & Wilson, E. O. The theory of island biogeography. Vol. 1 (Princeton university press, 2001).10.Guégan, J.-F., Lek, S. & Oberdorff, T. Energy availability and habitat heterogeneity predict global riverine fish diversity. Nature 391, 382–384 (1998).ADS 

    Google Scholar 
    11.Heidrich, L. et al. Heterogeneity–diversity relationships differ between and within trophic levels in temperate forests. Nat. Ecol. Evol. 4, 1204–1212 (2020).PubMed 

    Google Scholar 
    12.Kerr, J. T. & Packer, L. Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature 385, 252–254 (1997).ADS 
    CAS 

    Google Scholar 
    13.Ranjard, L. et al. Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity. Nat. Commun. 4, 1–10 (2013).
    Google Scholar 
    14.Fahrig, L. et al. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol. Lett. 14, 101–112 (2011).PubMed 

    Google Scholar 
    15.Ben‐Hur, E. & Kadmon, R. Heterogeneity–diversity relationships in sessile organisms: a unified framework. Ecol. Lett. 23, 193–207 (2020).PubMed 

    Google Scholar 
    16.Tews, J. et al. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J. Biogeogr. 31, 79–92 (2004).
    Google Scholar 
    17.Tuanmu, M. N. & Jetz, W. A global, remote sensing‐based characterization of terrestrial habitat heterogeneity for biodiversity and ecosystem modelling. Global Ecol. Biogeogr. 24, 1329–1339 (2015).
    Google Scholar 
    18.MacArthur, R. H. & MacArthur, J. W. On bird species diversity. Ecology 42, 594–598 (1961).
    Google Scholar 
    19.Allouche, O., Kalyuzhny, M., Moreno-Rueda, G., Pizarro, M. & Kadmon, R. Area–heterogeneity tradeoff and the diversity of ecological communities. Proc. Natl Acad. Sci. 109, 17495–17500 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Fahrig, L. Rethinking patch size and isolation effects: the habitat amount hypothesis. J. Biogeogr. 40, 1649–1663 (2013).
    Google Scholar 
    21.Gómez, J., Valladares, F. & Puerta-Piñero, C. Differences between structural and functional environmental heterogeneity caused by seed dispersal. Funct. Ecol. 18, 787–792 (2004).
    Google Scholar 
    22.Azevedo, J. C., Jack, S. B., Coulson, R. N. & Wunneburger, D. F. Functional heterogeneity of forest landscapes and the distribution and abundance of the red-cockaded woodpecker. Forest Ecol. Manag. 127, 271–283 (2000).
    Google Scholar 
    23.Watson, D. M. & Herring, M. Mistletoe as a keystone resource: an experimental test. Proc. Royal Soc. B: Biol. Sci. 279, 3853–3860 (2012).
    Google Scholar 
    24.Ellison, A. M. et al. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front. Ecol. Environ. 3, 479–486 (2005).
    Google Scholar 
    25.Altieri, A. H., Silliman, B. R. & Bertness, M. D. Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. Am. Natur. 169, 195–206 (2007).PubMed 

    Google Scholar 
    26.Angelini, C. et al. Foundation species’ overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern US salt marshes. Proc. Royal Soc. B: Biol. Sci. 282, 20150421 (2015).27.Angelini, C. & Silliman, B. R. Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree-epiphyte system. Ecology 95, 185–196 (2014).PubMed 

    Google Scholar 
    28.Bishop, M. J., Byers, J. E., Marcek, B. J. & Gribben, P. E. Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. Ecology 93, 1388–1401 (2012).PubMed 

    Google Scholar 
    29.Bishop, M. J., Fraser, J. & Gribben, P. E. Morphological traits and density of foundation species modulate a facilitation cascade in Australian mangroves. Ecology 94, 1927–1936 (2013).PubMed 

    Google Scholar 
    30.Thomsen, M. S., Metcalfe, I., South, P. & Schiel, D. R. A host-specific habitat former controls biodiversity across ecological transitions in a rocky intertidal facilitation cascade. Marine Freshwater Res. 67, 144–152 (2016).
    Google Scholar 
    31.Gribben, P. E. et al. Positive and negative interactions control a facilitation cascade. Ecosphere 8, e02065 (2017).
    Google Scholar 
    32.Shurin, J. B. et al. A cross‐ecosystem comparison of the strength of trophic cascades. Ecol. Lett. 5, 785–791 (2002).
    Google Scholar 
    33.Thomsen, M. S. Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquat. Invas. 5, 341–346 (2010).
    Google Scholar 
    34.Gribben, P. E. et al. Facilitation cascades in marine ecosystems: a synthesis and future directions. Oceanogr. Marine Biol. 57, 127–168 (2019).
    Google Scholar 
    35.Gotelli, N. J. & Colwell, R. K. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391 (2001).
    Google Scholar 
    36.Thomsen, M. S. et al. Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrat. Comparat. Biol. 50, 158–175 (2010).
    Google Scholar 
    37.Thomsen, M. S. et al. Modified kelp seasonality and invertebrate diversity where an invasive kelp co-occurs with native mussels. Marine Biol. 165, 173 (2018).
    Google Scholar 
    38.Borst, A. C. et al. Food or furniture: separating trophic and non‐trophic effects of Spanish moss to explain its high invertebrate diversity. Ecosphere 10, e02846 (2019).
    Google Scholar 
    39.Bologna, P. A. & Heck, K. L. Jr. Macrofaunal associations with seagrass epiphytes: relative importance of trophic and structural characteristics. J. Exp. Marine Biol. Ecol. 242, 21–39 (1999).
    Google Scholar 
    40.Huston, M. A. & Huston, M. A. Biological diversity: the coexistence of species. (Cambridge University Press, 1994).41.Borer, E. T. et al. Finding generality in ecology: a model for globally distributed experiments. Methods Ecol. Evol. 5, 65–73 (2014).
    Google Scholar 
    42.Fraser, L. H. et al. Coordinated distributed experiments: an emerging tool for testing global hypotheses in ecology and environmental science. Front. Ecol. Environ. 11, 147–155 (2013).
    Google Scholar 
    43.Thompson, K., Askew, A., Grime, J., Dunnett, N. & Willis, A. Biodiversity, ecosystem function and plant traits in mature and immature plant communities. Funct. Ecol. 19, 355–358 (2005).
    Google Scholar 
    44.Duffy, J. E. et al. Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach. Ecol. Lett. 18, 696–705 (2015).PubMed 

    Google Scholar 
    45.Arft, A. et al. Responses of tundra plants to experimental warming: meta‐analysis of the international tundra experiment. Ecol. Monogr. 69, 491–511 (1999).
    Google Scholar 
    46.Thomas, M. A. & Klaper, R. Genomics for the ecological toolbox. Trends Ecol. Evol. 19, 439–445 (2004).PubMed 

    Google Scholar 
    47.Thomsen, M. S. et al. A sixth‐level habitat cascade increases biodiversity in an intertidal estuary. Ecol. Evol. 6, 8291–8303 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    48.Ricklefs, R. E. Environmental heterogeneity and plant species diversity: a hypothesis. Am. Natur. 111, 376–381 (1977).
    Google Scholar 
    49.Lundholm, J. T. Plant species diversity and environmental heterogeneity: spatial scale and competing hypotheses. J. Vegetation Sci. 20, 377–391 (2009).
    Google Scholar 
    50.Tamme, R., Hiiesalu, I., Laanisto, L., Szava‐Kovats, R. & Pärtel, M. Environmental heterogeneity, species diversity and co‐existence at different spatial scales. J. Vegetation Sci. 21, 796–801 (2010).
    Google Scholar 
    51.Hughes, A. R., Gribben, P. E., Kimbro, D. L. & Bishop, M. J. Additive and site-specific effects of two foundation species on invertebrate community structure. Mar. Ecol. Prog. Series 508, 129–138 (2014).ADS 

    Google Scholar 
    52.Yakovis, E. & Artemieva, A. Cockles, barnacles and ascidians compose a subtidal facilitation cascade with multiple hierarchical levels of foundation species. Sci. Rep. 7, 1–11 (2017).CAS 

    Google Scholar 
    53.Thomsen, M. S., Stæhr, P. A., Nejrup, L. & Schiel, D. R. Effects of the invasive macroalgae Gracilaria vermiculophylla on two co-occurring foundation species and associated invertebrates. Aquat. Invas. 8, 133–145 (2013).
    Google Scholar 
    54.Littler, M. M. Morphological form and photosynthetic performances of marine macroalgae: tests of a functional/form hypothesis. Botan. Marina 22, 161–165 (1980).
    Google Scholar 
    55.Padilla, D. K. & Allen, B. J. Paradigm lost: reconsidering functional form and group hypotheses in marine ecology. J. Exp. Mar. Biol. Ecol. 250, 207–221 (2000).CAS 
    PubMed 

    Google Scholar 
    56.Wainwright, P. C. Functional morphology as a tool in ecological research. Ecol. Morphol.: Int. Organismal Biol. 42, 59 (1994).
    Google Scholar 
    57.Angelini, C. & Briggs, K. Spillover of secondary foundation species transforms community structure and accelerates decomposition in oak savannas. Ecosystems, 18, 780–791 (2015).
    Google Scholar 
    58.Gutiérrez, J. L., Bagur, M. & Palomo, M. G. Algal epibionts as co-engineers in mussel beds: effects on abiotic conditions and mobile interstitial invertebrates. Diversity 11, 17 (2019).
    Google Scholar 
    59.He, Q., Bertness, M. D. & Altieri, A. H. Global shifts towards positive species interactions with increasing environmental stress. Ecol. Lett. 16, 695–706 (2013).PubMed 

    Google Scholar 
    60.Watson, D. M. Mistletoe—a keystone resource in forests and woodlands worldwide. Ann. Rev. Ecol. Syst. 32, 219–249 (2001).
    Google Scholar 
    61.Mújica, E., Raventós, J., González, E. & Bonet, A. Long-term hurricane effects on populations of two epiphytic orchid species from Guanahacabibes Peninsula. Cuba. Lankesteriana Int. J. Orchidol. 13, 47–55 (2013).
    Google Scholar 
    62.Lobelle, D., Kenyon, E. J., Cook, K. J. & Bull, J. C. Local competition and metapopulation processes drive long-term seagrass-epiphyte population dynamics. PLoS ONE 8, e57072 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Svirski, E., Beer, S. & Friedlander, M. Gracilaria conferta and its epiphytes: Interrelationship between the red seaweed and Ulva cf. lactuca. Hydrobiologia 260, 391–396 (1993).
    Google Scholar 
    64.Cummins, S., Roberts, D. & Zimmerman, K. Effects of the green macroalga Enteromorpha intestinalis on macrobenthic and seagrass assemblages in a shallow coastal estuary. Marine Ecol. Prog. Series 266, 77–87 (2004).ADS 

    Google Scholar 
    65.Holmquist, J. G. Disturbance and gap formation in a marine benthic mosaic: influence of shifting macroalgal patches on seagrass structure and mobile invertebrates. Marine Ecol. Prog. Series 158, 121–130 (1997).ADS 

    Google Scholar 
    66.Siciliano, A., Schiel, D. R. & Thomsen, M. S. Effects of local anthropogenic stressors on a habitat cascade in an estuarine seagrass system. Marine Freshwater Res. 70, 1129–1142 (2019).
    Google Scholar 
    67.Field, R. et al. Spatial species‐richness gradients across scales: a meta‐analysis. J. Biogeogr. 36, 132–147 (2009).
    Google Scholar 
    68.Šímová, I., Li, Y. M. & Storch, D. Relationship between species richness and productivity in plants: the role of sampling effect, heterogeneity and species pool. J. Ecol. 101, 161–170 (2013).
    Google Scholar 
    69.Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).PubMed 

    Google Scholar 
    70.Berlow, E. L. Strong effects of weak interactions in ecological communities. Nature 398, 330–334 (1999).ADS 
    CAS 

    Google Scholar 
    71.Darling, E. S. & Côté, I. M. Quantifying the evidence for ecological synergies. Ecol. Lett. 11, 1278–1286 (2008).PubMed 

    Google Scholar 
    72.Paine, R. T., Tegner, M. J. & Johnson, E. A. Compounded perturbations yield ecological surprises. Ecosystems 1, 535–545 (1998).
    Google Scholar 
    73.Christensen, M. R. et al. Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob. Change Biol. 12, 2316–2322 (2006).ADS 

    Google Scholar 
    74.Strain, E. M. et al. A global analysis of complexity–biodiversity relationships on marine artificial structures. Glob. Ecol. Biogeogr. 30, 140–153 (2021).
    Google Scholar 
    75.Richardson, J. T. Eta squared and partial eta squared as measures of effect size in educational research. Educ. Res. Rev. 6, 135–147 (2011).
    Google Scholar 
    76.Clarke, K. R., Gorley, R., Somerfield, P. J. & Warwick, R. Change in marine communities: an approach to statistical analysis and interpretation. (Primer-E Ltd, 2014).77.Gartner, A., Tuya, F., Lavery, P. S. & McMahon, K. Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. J. Exp. Marine Biol. Ecol. 439, 143–151 (2013).
    Google Scholar 
    78.Green, D. S. & Crowe, T. P. Context-and density-dependent effects of introduced oysters on biodiversity. Biol. Invasions 16, 1145–1163 (2014).
    Google Scholar 
    79.Lawton, J. H. Are there general laws in ecology? Oikos 84, 177–192 (1999).
    Google Scholar 
    80.Borer, E. et al. What determines the strength of a trophic cascade? Ecology 86, 528–537 (2005).
    Google Scholar 
    81.Vellend, M. Conceptual synthesis in community ecology. Quart. Rev. Biol. 85, 183–206 (2010).PubMed 

    Google Scholar 
    82.Chase, J. M. & Leibold, M. A. Ecological niches: linking classical and contemporary approaches. (University of Chicago Press, 2003).83.Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).ADS 
    PubMed 

    Google Scholar 
    84.Anderson, M. J. A new method for non‐parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 
    85.Veech, J. A. & Crist, T. O. Habitat and climate heterogeneity maintain beta‐diversity of birds among landscapes within ecoregions. Glob. Ecol. Biogeogr. 16, 650–656 (2007).
    Google Scholar 
    86.Turner, M. G. Landscape ecology: the effect of pattern on process. Ann. Rev. Ecol. Syst. 20, 171–197 (1989).
    Google Scholar 
    87.Wilson, M. V. & Shmida, A. Measuring beta diversity with presence-absence data. J. Ecol. 72, 1055–1064 (1984).
    Google Scholar 
    88.Jost, L. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439 (2007).PubMed 

    Google Scholar 
    89.Socolar, J. B., Gilroy, J. J., Kunin, W. E. & Edwards, D. P. How should beta-diversity inform biodiversity conservation? Trends Ecol. Evol. 31, 67–80 (2016).PubMed 

    Google Scholar 
    90.McAfee, D., Cole, V. J. & Bishop, M. J. Latitudinal gradients in ecosystem engineering by oysters vary across habitats. Ecology 97, 929–939 (2016).PubMed 

    Google Scholar 
    91.Altieri, A. H. & Irving, A. D. Species coexistence and the superior ability of an invasive species to exploit a facilitation cascade habitat. PeerJ 5, e2848 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    92.Lindenmayer, D., Franklin, J. & Fischer, J. General management principles and a checklist of strategies to guide forest biodiversity conservation. Biol. Conser. 131, 433–445 (2006).
    Google Scholar 
    93.Le Roux, D. S., Ikin, K., Lindenmayer, D. B., Manning, A. D. & Gibbons, P. Single large or several small? Applying biogeographic principles to tree-level conservation and biodiversity offsets. Biol. Conser. 191, 558–566 (2015).
    Google Scholar 
    94.Wernberg, T. et al. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep. 8, 1–8 (2018).
    Google Scholar 
    95.Macintosh, D. J. & Ashton, E. C. A review of mangrove biodiversity conservation and management. Centre for tropical ecosystems research. (University of Aarhus, 2002).96.Grabowski, J. H. et al. Economic valuation of ecosystem services provided by oyster reefs. Bioscience 62, 900–909 (2012).
    Google Scholar 
    97.Renzi, J. J., He, Q. & Silliman, B. R. Harnessing positive species interactions to enhance coastal wetland restoration. Front. Ecol. Evol. 7, 131 (2019).
    Google Scholar 
    98.Silliman, B. R. et al. Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc. Natl Acad. Sci. 112, 14295–14300 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    99.Bulleri, F. et al. Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversity. PLoS Biol. 16, e2006852 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    100.Brancalion, P. H. et al. Global restoration opportunities in tropical rainforest landscapes. Sci. Adv. 5, eaav3223 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    101.Burns, K. Meta-community structure of vascular epiphytes in a temperate rainforest. Botany 86, 1252–1259 (2008).
    Google Scholar 
    102.Chapman, M. & Blockley, D. Engineering novel habitats on urban infrastructure to increase intertidal biodiversity. Oecologia 161, 625–635 (2009).ADS 
    CAS 
    PubMed 

    Google Scholar 
    103.Schneider-Mayerson, M. Some islands will rise: Singapore in the Anthropocene. Resilience: J. Environ. Human. 4, 166–184 (2017).
    Google Scholar 
    104.Wangpraseurt, D. et al. Bionic 3D printed corals. Nat. Commun. 11, 1–8 (2020).
    Google Scholar 
    105.de Alvarenga, R. A. F., Galindro, B. M., de Fátima Helpa, C. & Soares, S. R. The recycling of oyster shells: an environmental analysis using Life Cycle Assessment. J. Environ. Manag. 106, 102–109 (2012).CAS 

    Google Scholar 
    106.Morris, J. P., Backeljau, T. & Chapelle, G. Shells from aquaculture: a valuable biomaterial, not a nuisance waste product. Rev. Aqua. 11, 42–57 (2019).
    Google Scholar 
    107.Hylander, K. & Nemomissa, S. Home garden coffee as a repository of epiphyte biodiversity in Ethiopia. Front. Ecol. Environ. 6, 524–528 (2008).
    Google Scholar 
    108.Franken, R. J. et al. Effects of interstitial refugia and current velocity on growth of the amphipod Gammarus pulex Linnaeus. J. North Am. Bentholog. Soc. 25, 656–663 (2006).
    Google Scholar 
    109.Bishop, M. et al. Facilitation of molluscan assemblages in mangroves by the fucalean alga Hormosira banksii. Marine Ecol. Prog. Series 392, 111–122 (2009).ADS 

    Google Scholar 
    110.Macreadie, P. I., Kimbro, D. L., Fourgerit, V., Leto, J. & Hughes, A. R. Effects of Pinna clams on benthic macrofauna and the possible implications of their removal from seagrass ecosystems. J. Molluscan Studies 80, 102–106 (2014).
    Google Scholar 
    111.Thomsen, M. S. et al. Earthquake-driven destruction of an intertidal habitat cascade. Aquat. Botany 164, 103217 (2020).
    Google Scholar 
    112.Enochs, I. C., Toth, L. T., Brandtneris, V. W., Afflerbach, J. C. & Manzello, D. P. Environmental determinants of motile cryptofauna on an eastern Pacific coral reef. Marine Ecol. Prog. Series 438, 105–118 (2011).ADS 

    Google Scholar  More

  • in

    Fungal fruit body assemblages are tougher in harsh microclimates

    1.McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185 (2006).PubMed 

    Google Scholar 
    2.Urban, M. C. et al. Improving the forecast for biodiversity under climate change. Science 353, 6304 (2016).
    Google Scholar 
    3.Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Chang. 1, 401–406 (2011).ADS 

    Google Scholar 
    4.Zeuss, D., Brandl, R., Brändle, M., Rahbek, C. & Brunzel, S. Global warming favours light-coloured insects in Europe. Nat. Commun. 5, 1–10 (2014).
    Google Scholar 
    5.Senf, C., Sebald, J. & Seidl, R. Increasing canopy mortality affects the future demographic structure of Europe’s forests. One Earth 4, 749–755 (2021).
    Google Scholar 
    6.Zellweger, F. et al. Forest microclimate dynamics drive plant responses to warming. Science 368, 772–775 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    7.Scharenbroch, B. C. & Bockheim, J. G. Impacts of forest gaps on soil properties and processes in old growth northern hardwood-hemlock forests. Plant Soil 294, 219–233 (2007).CAS 

    Google Scholar 
    8.de Frenne, P. et al. Global buffering of temperatures under forest canopies. Nat. Ecol. Evol. 3, 744–749 (2019).PubMed 

    Google Scholar 
    9.Kermavnar, J. et al. Effects of various cutting treatments and topographic factors on microclimatic conditions in Dinaric fir-beech forests. Agric. For. Meteorol. 295, 108186 (2020).ADS 

    Google Scholar 
    10.Brown, M. J., Parker, G. G. & Posner, N. E. A survey of ultraviolet-B radiation in forests. J. Ecol. 82, 843 (1994).
    Google Scholar 
    11.Thom, D. et al. Effects of disturbance patterns and deadwood on the microclimate in European beech forests. Agric. For. Meteorol. 291, 108066 (2020).ADS 

    Google Scholar 
    12.Frank, A. et al. Risk of genetic maladaptation due to climate change in three major European tree species. Glob. Change Biol. 23, 5358–5371 (2017).ADS 

    Google Scholar 
    13.Maxime, C. & Hendrik, D. Effects of climate on diameter growth of co-occurring Fagus sylvatica and Abies alba along an altitudinal gradient. Trees 25, 265–276 (2011).
    Google Scholar 
    14.Vitasse, Y. et al. Contrasting resistance and resilience to extreme drought and late spring frost in five major European tree species. Glob. Change Biol. 25, 3781–3792 (2019).ADS 

    Google Scholar 
    15.Seidl, R. et al. Forest disturbances under climate change. Nat. Clim. Chang. 7, 395–402 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Penone, C. et al. Specialisation and diversity of multiple trophic groups are promoted by different forest features. Ecol. Lett. 22, 170–180 (2019).PubMed 

    Google Scholar 
    17.Müller, J. et al. Primary determinants of communities in deadwood vary among taxa but are regionally consistent. Oikos 129, 1579–1588 (2020).
    Google Scholar 
    18.Krah, F.-S. et al. Independent effects of host and environment on the diversity of wood-inhabiting fungi. J. Ecol. 106, 1428–1442 (2018).
    Google Scholar 
    19.Nagy, L. G. et al. Six key traits of fungi: Their evolutionary origins and genetic bases. Microbiol. Spect. 5, 4 (2017).
    Google Scholar 
    20.Baldrian, P. Forest microbiome: Diversity, complexity and dynamics. FEMS Microbiol. Rev. 41, 109–130 (2017).CAS 
    PubMed 

    Google Scholar 
    21.Raudaskoski, M. & Salonen, M. Interrelationships between vegetative development and basidiocarp initiation. in The Ecology and Physiology of the Fungal Mycelium: Symposium of the British Mycological Society, vol. 8, p. 291 (Cambridge University Press, 1984).22.Kües, U. & Liu, Y. Fruiting body production in Basidiomycetes. Appl. Microbiol. Biotechnol. 54, 141–152 (2000).PubMed 

    Google Scholar 
    23.Sakamoto, Y. Influences of environmental factors on fruiting body induction, development and maturation in mushroom-forming fungi. Fungal Biol. Rev. 32, 236–248 (2018).
    Google Scholar 
    24.Luo, L., Zhang, S., Wu, J., Sun, X. & Ma, A. Heat stress in macrofungi: Effects and response mechanisms. Appl. Microbiol. Biotechnol. 1, 1–10 (2021).
    Google Scholar 
    25.Krah, F., Hess, J., Hennicke, F., Kar, R. & Bässler, C. Transcriptional response of mushrooms to artificial sun exposure. Ecol. Evol. 11, 10538–10546 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    26.Krah, F.-S. et al. European mushroom assemblages are darker in cold climates. Nat. Commun. 10, 2890 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Bässler, C. et al. Global analysis reveals an environmentally driven latitudinal pattern in mushroom size across fungal species. Ecol. Lett. https://doi.org/10.1111/ele.13678 (2021).Article 
    PubMed 

    Google Scholar 
    28.Bässler, C. et al. Mean reproductive traits of fungal assemblages are correlated with resource availability. Ecol. Evol. 6, 582–592 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    29.Abrego, N., Norberg, A. & Ovaskainen, O. Measuring and predicting the influence of traits on the assembly processes of wood-inhabiting fungi. J. Ecol. 105, 1070–1081 (2016).
    Google Scholar 
    30.Sánchez-García, M. et al. Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi. Proc. Natl. Acad. Sci. 117, 32528–32534 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    31.Hibbett, D. S. & Binder, M. Evolution of complex fruiting–body morphologies in homobasidiomycetes. Proc. R. Soc. Lond. B 269, 1963–1969 (2002).CAS 

    Google Scholar 
    32.Hibbett, D. S., Pine, E. M., Langer, E., Langer, G. & Donoghue, M. J. Evolution of gilled mushrooms and puffballs inferred from ribosomal DNA sequences. Proc. Natl. Acad. Sci. 94, 12002–12006 (1997).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Halbwachs, H., Simmel, J. & Bässler, C. Tales and mysteries of fungal fruiting: How morphological and physiological traits affect a pileate lifestyle. Fungal Biol. Rev. 30, 36–61 (2016).
    Google Scholar 
    34.Wilson, A. W., Binder, M. & Hibbett, D. S. Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis. Evol. Int. J. Org. Evol. 65, 1305–1322 (2011).
    Google Scholar 
    35.Cordero, R. J. B. & Casadevall, A. Functions of fungal melanin beyond virulence. Fungal Biol. Rev. 31, 99–112 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    36.Zamora-Camacho, F. J., Reguera, S. & Moreno-Rueda, G. Bergmann’s Rule rules body size in an ectotherm: Heat conservation in a lizard along a 2200-metre elevational gradient. J. Evol. Biol. 27, 2820–2828 (2014).CAS 
    PubMed 

    Google Scholar 
    37.Kalmus, H. Physiology and ecology of cuticle colour in insects. Nature 148, 693 (1941).ADS 

    Google Scholar 
    38.Law, S. J. et al. Darker ants dominate the canopy: Testing macroecological hypotheses for patterns in colour along a microclimatic gradient. J. Anim. Ecol. 89, 347–359 (2020).PubMed 

    Google Scholar 
    39.Bogert, C. M. Thermoregulation in reptiles, a factor in evolution. Evolution 3, 195–211 (1949).CAS 
    PubMed 

    Google Scholar 
    40.R Core Team. R: A Language and Environment for Statistical Computing. (R Core Team, 2015).41.Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).MATH 

    Google Scholar 
    42.Olou, B. A., Yorou, N. S., Striegel, M., Bässler, C. & Krah, F.-S. Effects of macroclimate and resource on the diversity of tropical wood-inhabiting fungi. For. Ecol. Manage. 436, 79–87 (2019).
    Google Scholar 
    43.Moser, M. Fungal growth and fructification under stress conditions. Ukrainian Bot. J. 50, 5–11 (1993).
    Google Scholar 
    44.Walter, H. et al. Vegetation of the Earth in Relation to Climate and the Eco-Physiological Conditions (English Universities Press, 1973).
    Google Scholar 
    45.Botti, D. A phytoclimatic map of Europe. Cybergeo Eur. J. Geogr. https://doi.org/10.4000/cybergeo.29495 (2018).Article 

    Google Scholar 
    46.Sofo, A., Manfreda, S., Fiorentino, M., Dichio, B. & Xiloyannis, C. The olive tree: A paradigm for drought tolerance in Mediterranean climates. Hydrol. Earth Syst. Sci. 12, 293–301 (2008).ADS 

    Google Scholar 
    47.Poorter, H., Niinemets, Ü., Poorter, L., Wright, I. J. & Villar, R. Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. New Phytol. 182, 565–588 (2009).PubMed 

    Google Scholar 
    48.Ellenberg, H. H. Spring areas and adjacent swamps. in Vegetation ecology of central Europe 313–313 (Cambridge University Press, 1988).49.Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: A third universal response to warming?. New Phytol. 26, 285–291 (2011).
    Google Scholar 
    50.Stamets, P. Growing Gourmet and Medicinal Mushrooms (Ten Speed Press, 2011).
    Google Scholar 
    51.Cordero, R. J. B. et al. Impact of yeast pigmentation on heat capture and latitudinal distribution. Curr. Biol. 28, 2657-2664.e3 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Graham, J. H. et al. Species richness, equitability, and abundance of ants in disturbed landscapes. Ecol. Ind. 9, 866–877 (2009).
    Google Scholar 
    53.Palladini, J. D., Jones, M. G., Sanders, N. J. & Jules, E. S. The recovery of ant communities in regenerating temperate conifer forests. For. Ecol. Manage. 242, 619–624 (2007).
    Google Scholar 
    54.Punttila, P., Haila, Y., Niemelä, J. & Pajunen, T. Ant communities in fragments of old-growth taiga and managed surroundings. Ann. Zool. Fenn. 31, 131–144 (1994).
    Google Scholar 
    55.Entling, W., Schmidt-Entling, M. H., Bacher, S., Brandl, R. & Nentwig, W. Body size–climate relationships of European spiders. J. Biogeogr. 37, 477–485 (2010).
    Google Scholar 
    56.Gotelli, N. J. Null model analysis of species co-occurrence patterns. Ecology 81, 2606–2621 (2000).
    Google Scholar 
    57.Tucker, C. M., Shoemaker, L. G., Davies, K. F., Nemergut, D. R. & Melbourne, B. A. Differentiating between niche and neutral assembly in metacommunities using null models of beta-diversity. Oikos 125, 778–789 (2015).
    Google Scholar 
    58.Shipley, B. et al. Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180, 923–931 (2016).ADS 
    PubMed 

    Google Scholar 
    59.Krah, F.-S. & Bässler, C. What can intraspecific trait variability tell us about fungal communities and adaptations?. Mycol. Prog. 20, 905–910 (2021).
    Google Scholar 
    60.Norros, V. & Halme, P. Growth sites of polypores from quantitative expert evaluation: Late-stage decayers and saprotrophs fruit closer to ground. Fungal Ecol. 28, 53–65 (2017).
    Google Scholar 
    61.Senf, C. et al. Canopy mortality has doubled in Europe’s temperate forests over the last three decades. Nat. Commun. 9, 4978 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    62.Bässler, C., Seifert, L. & Müller, J. The BIOKLIM project in the National Park Bavarian Forest: Lessons from a biodiversity survey. Silva Gabreta 21, 81–93 (2015).
    Google Scholar 
    63.Halme, P. & Kotiaho, J. S. The importance of timing and number of surveys in fungal biodiversity research. Biodivers. Conserv. 21, 205–219 (2012).
    Google Scholar 
    64.Crous, P. W. et al. MycoBank: An online initiative to launch mycology into the 21st century. Stud. Mycol. 50, 19–22 (2004).
    Google Scholar 
    65.van den Broek, E. L. & van Rikxoort, E. M. Evaluation of color representation for texture analysis. in Paper presented at 16th Belgium-Dutch Conference on Artificial Intelligence, BNAIC 2004, Groningen, Netherlands 35–42 (2004).66.Bernicchia, A. Fungi Europaei, Volume 10. Polyporaceae sl. (Alassio, Italia: Edizioni Candusso, 2005).67.Kembel, S. Community Phylogenetic Analysis with Picante Installing Picante 1–18 (Springer, 2009).
    Google Scholar 
    68.Gotelli, N. J. & Graves, G. R. Null Models in Ecology (Springer, 1996).
    Google Scholar 
    69.Hochberg, Y. & Tamhane, A. C. Multiple Comparison Procedures (Wiley, 1987).MATH 

    Google Scholar 
    70.Dormann, C. G., Elith, J., Bacher, S., Buchmann, C. & Lautenback, S. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 35, 001–020 (2012).
    Google Scholar 
    71.Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Google Scholar 
    72.Purhonen, J. et al. Morphological traits predict host-tree specialization in wood-inhabiting fungal communities. Fungal Ecol. 46, 100863 (2020).
    Google Scholar 
    73.Heilmann-Clausen, J. & Christensen, M. Does size matter?: On the importance of various dead wood fractions for fungal diversity in Danish beech forests. For. Ecol. Manage. 201, 105–117 (2004).
    Google Scholar 
    74.Lenth, R. V. Least-squares means: The R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).
    Google Scholar  More

  • in

    Effects of reduced salinity caused by reclamation on population and physiological characteristics of the sesarmid crab Chiromantes dehaani

    1.Chen, L. et al. Spatiotemporal dynamics of coastal wetlands and reclamation in the Yangtze estuary during past 50 years (1960s–2015). Chin. Geogr. Sci. 28(3), 386–399 (2018).
    Google Scholar 
    2.Lv, W. et al. Effect of freshwater inflow on self-restoration of macrobenthic diversity in seaward intertidal wetlands influenced by reclamation projects in the Yangtze estuary, China. Mar. Pollut. Bull. 138, 177–186 (2019).CAS 
    PubMed 

    Google Scholar 
    3.Lv, W. et al. Loss and selfrestoration of macrobenthic diversity in reclamation habitats of estuarine islands in Yangtze Estuary, China. Mar. Pollut. Bull. 103, 128–136 (2016).CAS 
    PubMed 

    Google Scholar 
    4.Matsuda, O. & Kokubu, H. Recent coastal environmental management based on new concept of Satoumi which promotes land-ocean interaction: A case study in Japan. Estuar. Coast. Shelf S 183, 179–186 (2016).ADS 

    Google Scholar 
    5.Wang, J. et al. Exotic Spartina alterniflora provides compatible habitats for native estuarine crab Sesarma dehaani in the Yangtze River estuary. Ecol. Eng. 34, 57–64 (2008).CAS 

    Google Scholar 
    6.Lee, S. Y. & Khim, J. S. Hard science is essential to restoring soft-sediment intertidal habitats in burgeoning East Asia. Chemosphere 168, 765–776 (1998).ADS 

    Google Scholar 
    7.Wang, L. The complete larval development of Sesarma dehaani. J. Shanghai Fisheries Univ. 10(3), 199–206 (2001).CAS 

    Google Scholar 
    8.Liu, Z. et al. Different effects of reclamation methods on macrobenthos community structure in the Yangtze Estuary, China. Mar. Pollut. Bull. 127, 429–436 (2018).CAS 
    PubMed 

    Google Scholar 
    9.Henry, R. P., Lucu, C., Onken, H. & Weihrauch, D. Multiple functions of the crustacean gill: Osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Front. Physiol. 3, 431 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.McNamara, J. C. & Faria, S. C. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: A review. J. Comp. Physiol. B. 182(8), 997–1014 (2012).CAS 
    PubMed 

    Google Scholar 
    11.Thabet, R., Ayadi, H., Koken, M. & Leignel, V. Homeostatic responses of crustaceans to salinity changes. Hydrobiologia 799(1), 1–20 (2017).CAS 

    Google Scholar 
    12.Boonsanit, P. & Pairohakul, S. Effects of salinity on haemolymph osmolality, gill Na+/K+ ATPase and antioxidant enzyme activities in the male mud crab Scylla olivacea (Herbst, 1796). Mar. Biol. Res. 17(1), 86–97 (2021).
    Google Scholar 
    13.Wang, R. et al. Osmotic and ionic regulation and Na+/K+-ATPase, carbonic anhydrase activities in mature Chinese mitten crab, Eriocheir sinensis H. Milne Edwards, 1853 (Decapoda, Brachyura) exposed to different salinities. Crustaceana 85(12–13), 1431–1447 (2012).
    Google Scholar 
    14.Garçon, D. P. et al. Na+, K+-ATPase activity in the posterior gills of the blue crab, Callinectes ornatus (Decapoda, Brachyura): Modulation of ATP hydrolysis by the biogenic amines spermidine and spermine. J. Membr. Biol. 244, 9–20 (2011).PubMed 

    Google Scholar 
    15.Jiang, S. & Xu, Q. Influence of salinity stress on the activity of gill Na+/K+-ATPase in swimming crab(Portunus trituberculatus). J. Fish. China 35(10), 1475–1480 (2011).CAS 

    Google Scholar 
    16.Mo, J. L., Devos, P. & Trausch, G. Active absorption of Cl– and Na+ in posterior gills of Chinese crab, Eriocheir sinensis: modulation by dopamine and cAMP. J. Crust. Biol. 23, 505–512 (2003).
    Google Scholar 
    17.Charmantier, G. Ontogeny of osmoregulation in crustaceans: A review. Invertebr. Reprod. Dev. 33(2–3), 177–190 (1998).CAS 

    Google Scholar 
    18.Vargas-Chacoff, L. et al. Effects on the metabolism, growth, digestive capacity and osmoregulation of juvenile of sub-Antarctic Notothenioid fish Eleginops maclovinus acclimated at different salinities. Fish Physiol. Biochem. 41, 1369–1381 (2015).CAS 
    PubMed 

    Google Scholar 
    19.Wang, R. et al. The response of digestive enzyme activity in the mature Chinese mitten crab, Eriocheir sinensis (Decapoda: Brachyura), to gradual increase of salinity. Sci. Mar. 77(2), 323–329 (2013).
    Google Scholar 
    20.Li, E. et al. Comparison of digestive and antioxidant enzymes activities, haemolymph oxyhemocyanin contents and hepatopancreas histology of white shrimp, Litopenaeus vannamei, at various salinities. Aquaculture 274, 80–86 (2008).CAS 

    Google Scholar 
    21.Asaro, A., del Valle, J. C. & López Mañanes, A. A. Amylase, maltase and sucrase activities in hepatopancreas of the euryhaline crab Neohelice granulata (Decapoda: Brachyura: Varunidae): Partial characterization and response to low environmental salinity. Sci. Mar. 75, 517–524 (2011).CAS 

    Google Scholar 
    22.Sǒderhǎll, I. et al. Hemocyte production andmaturation in an invertebrate animal; proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus. Dev. Comp. Immunol. 97(8), 661–672 (2004).
    Google Scholar 
    23.Liu, S., Jiang, X., Mou, H., Wang, H. & Guan, H. Effects of immunopoiysaccharide on LSZ, ALP, ACP and POD activities of Penaeus chinensis serum. Oceanol. Limnol. Sin. 30(3), 278–283 (1999).CAS 

    Google Scholar 
    24.Ma, Z., Zhang, F. & Jing, A. Overview and graph theory of the immune system of crustacean. Aquacul. Sci. Technol. 11(8), 19–23 (2010).CAS 

    Google Scholar 
    25.Gu, Q. & He, L. Analysis of hemolymph osmotic pressure in crab (Eriocheir sinensis H. Milne Edwards) during oogenesis. Acta Zool. Sin. 36(2), 165–171 (1990).
    Google Scholar 
    26.Esser, L. J. & Cumberlidge, N. Evidence that salt water may not be a barrier to the dispersal of Asian freshwater crabs (Decapoda: Brachyura: Gecarcinucidae and potamidae). Raffles B. Zool. 59(2), 259–268 (2011).
    Google Scholar 
    27.Novo, M. S., Miranda, R. B. & Bianchini, A. Sexual and seasonal variations in osmoregulation and ionoregulation in the estuarine crab Chasmagnathus granulatus (Crustacea, Decapoda). J. Exp. Mar. Biol. Ecol. 323(2), 118–137 (2005).CAS 

    Google Scholar 
    28.Huong, D. T. T., Yang, W., Okuno, A. & Wilder, M. N. Changes in free amino acids in the hemolymph of giant freshwater prawn Macrobrachium rosenbergii exposed to varying salinities: Relationship to osmoregulatory ability. Comp. Biochem. Phys. A 128(2), 317–326 (2001).CAS 

    Google Scholar 
    29.Malmsten, M. & Larsson, A. Immobilization of trypsin on porous glycidyl methacrylate beads: Effects of polymer hydrophilization. Colloid. Surf. B 18, 277–284 (2000).CAS 

    Google Scholar 
    30.Hosoi, M. et al. Effect of salinity change on free amino acid content in Pacific oyster. Fish. Sci. 69(2), 395–400 (2003).CAS 

    Google Scholar 
    31.Wang, G. D., Xu, K. F., Tian, X. L., Dong, S. L. & Fang, Z. H. Changes in plasma osmolality, cortisol and amino acid levels of tongue sole (Cynoglossus semilaevis) at different salinities. J. Ocean Univ. China 14(5), 881–887 (2015).ADS 
    CAS 

    Google Scholar 
    32.Johnston, D. & Freeman, J. Dietary preference and digestive enzyme activities as indicators of trophic resource utilization by six species of crab. Biol. Bull. 208, 36–46 (2005).CAS 
    PubMed 

    Google Scholar 
    33.Zhang, Y. & Tong, C. Stomach content characteristics and feeding preference of Chiromantes dehaani in the salt marsh of Yangtze estuary. Chinese J. Ecol. 37(7), 2059–2066 (2018).
    Google Scholar 
    34.Ye, Y. et al. Comparative study on some traits of male and female Eriocheir sinensis raised in pond. Contemp. Aquacult. 38(4), 7–8 (2000).
    Google Scholar 
    35.Han, S. & Guan, W. Growth and maturity of Chiromantes dehaani in Dazhi River Estuary. Trans. Oceanol. Limnol. 15(1), 51–65 (2012).
    Google Scholar 
    36.Li, W., Guan, Y. & Yu, Z. Effects of salinity variation on outbreak of white spot syndrome and immunocompetence in Penaeus japonicas. Mar. Environ. Sci. 21(4), 6–9 (2002).
    Google Scholar 
    37.Pan, L. & Jiang, L. The effect of sudden changes in salinity and pH on immune activity of two species of shrimps. J. Ocean Univ. Qingdao 32(6), 903–910 (2002).CAS 

    Google Scholar 
    38.Gamperl, A. K., Vijayan, M. M. & Boutilier, R. G. Experimental control of stress hormone levels in fishes: Techniques and applications. Rev. Fish Biol. Fish. 4(2), 215–255 (1994).
    Google Scholar 
    39.Weerd, J. H. V. & Komen, J. The effects of chronic stress on growth in fish: A critical appraisal. Comp. Biochem. Phys. A 120(1), 107–112 (1998).
    Google Scholar 
    40.Barton, B. A., Schreck, C. B. & Barton, L. D. Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis. Aquat. Organ. 2(3), 173–185 (1987).CAS 

    Google Scholar 
    41.Zhao, Q., Qin, F., Li, C. & Jin, S. Preliminary study on the activities of enzymes in haemolymph of three species of marine crabs. J. Ningbo Univ. 22(1), 33–38 (2009).CAS 

    Google Scholar 
    42.Lv, W. et al. Macrobenthic diversity in protected, disturbed, and newly formed intertidal wetlands of a subtropical estuary in China. Mar. Pollut. Bull. 89, 259–266 (2014).CAS 
    PubMed 

    Google Scholar 
    43.Ma, Z., Jing, K., Tang, S. & Chen, J. Shorebirds in the eastern intertidal areas of Chongming island during the 2001 northern migration. Stilt 41, 6–10 (2002).
    Google Scholar 
    44.Sui, L., Wille, M., Cheng, Y., Wu, X. & Sorgeloos, P. Larviculture techniques of Chinese mitten crab Eriocheir sinensis. Aquaculture 315(1–2), 16–19 (2011).
    Google Scholar 
    45.Luo, M. et al. Community characteristics of macrobenthos in waters around the nature reserve of the Chinese sturgeon Acipenser sinensis and the adjacent waters in Yangtze River estuary. J. Appl. Ichthyol. 27, 425–432 (2011).
    Google Scholar 
    46.Yang, Z., Zhu, L., Zhao, X. & Cheng, Y. Effects of salinity stress on osmotic pressure, free amino acids, and immune-associated parameters of the juvenile Chinese mitten crab, Eriocheir sinensis. Aquaculture 549, 737776 (2022).
    Google Scholar 
    47.Tian, L., Tan, P., Yang, L., Zhu, W. & Xu, D. Effects of salinity on the growth, plasma ion concentrations, osmoregulation, non-specific immunity, and intestinal microbiota of the yellow drum (Nibea albiflora). Aquaculture 528, 735470 (2020).CAS 

    Google Scholar  More

  • in

    Fire-prone Rhamnaceae with South African affinities in Cretaceous Myanmar amber

    1.Lloyd, G. T. et al. Dinosaurs and the Cretaceous terrestrial revolution. Proc. R. Soc. B 275, 2483–2490 (2008).PubMed 
    PubMed Central 

    Google Scholar 
    2.Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007).CAS 
    PubMed 

    Google Scholar 
    3.Herrera-Flores, J. A., Stubbs, T. L. & Benton, M. J. Ecomorphological diversification of squamates in the Cretaceous. R. Soc. Open Sci. 8, 201961 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    4.Benton, M. J. The origins of modern biodiversity on land. Phil. Trans. R. Soc. B 365, 3667–3679 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    5.Roelants, K. et al. Global patterns of diversifcation in the history of modern amphibians. Proc. Natl Acad. Sci. USA 104, 887–892 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    6.Grosberg, R. K., Vermeij, G. J. & Wainwright, P. C. Biodiversity in water and on land. Curr. Biol. 22, 900–903 (2012).
    Google Scholar 
    7.Condamine, F. L., Silvestro, D., Koppelhus, E. B. & Antonelli, A. The rise of angiosperms pushed conifers to decline during global cooling. Proc. Natl Acad. Sci. USA 117, 28867–28875 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Buggs, R. J. The deepening of Darwin’s abominable mystery. Nat. Ecol. Evol. 1, 0169 (2017).
    Google Scholar 
    9.Friis, E. M., Crane, P. R., Pedersen, K. R., Stampanoni, M. & Marone, F. Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms. Nature 528, 551–554 (2015).PubMed 

    Google Scholar 
    10.Friis, E. M., Crane, P. R. & Pedersen, K. R. Early Flowers and Angiosperm Evolution (Cambridge Univ. Press, 2011).11.Friis, E. M., Pedersen, K. R. & Crane, P. R. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 251–293 (2006).
    Google Scholar 
    12.Soltis, P. S., Folk, R. A. & Soltis, D. E. Darwin review: angiosperm phylogeny and evolutionary radiations. Proc. R. Soc. B 286, 20190099 (2019).PubMed Central 

    Google Scholar 
    13.Bond, W. J. & Scott, A. C. Fire and the spread of flowering plants in the Cretaceous. New Phytol. 188, 1137–1150 (2010).PubMed 

    Google Scholar 
    14.Bond, W. J. & Midgley, J. J. Fire and the angiosperm revolutions. Int. J. Plant Sci. 173, 569–583 (2012).
    Google Scholar 
    15.Belcher, C. M. & Hudspith, V. A. Changes to Cretaceous surface fire behaviour influenced the spread of the early angiosperms. New Phytol. 213, 1521–1532 (2017).CAS 
    PubMed 

    Google Scholar 
    16.He, T., Lamont, B. B. & Pausas, J. G. Fire as a key driver of Earth’s biodiversity. Biol. Rev. 94, 1983–2010 (2019).PubMed 

    Google Scholar 
    17.Cruickshank, R. D. & Ko, K. Geology of an amber locality in the Hukawng Valley, Northern Myanmar. J. Asian Earth Sci. 21, 441–455 (2003).
    Google Scholar 
    18.Shi, G. H. et al. Age constraint on Burmese amber based on U–Pb dating of zircons. Cretac. Res. 37, 155–163 (2012).
    Google Scholar 
    19.Yu, T. et al. An ammonite trapped in Burmese amber. Proc. Natl Acad. Sci. USA 166, 11345–11350 (2019).
    Google Scholar 
    20.Xing, L. D. & Qiu, L. Zircon U–Pb age constraints on the Hkamti amber biota in northern Myanmar. Palaeogeogr. Palaeoclimatol. Palaeoecol. 558, 109960 (2020).
    Google Scholar 
    21.Xia, F. Y., Yang, G., Zhang, Q. & Shi, G. L. Amber Lives Through Time and Space (Beijing Science Press, 2015).22.Poinar, G. O. & Brown, A. E. A green algae (Chaetophorales: Chaetophoraceae) in Burmese amber. Hist. Biol. 33, 323–327 (2019).
    Google Scholar 
    23.Liu, Z. J., Huang, D., Cai, C. Y. & Wang, X. The core eudicot boom registered in Myanmar amber. Sci. Rep. 8, 16765 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    24.Poinar, G. O. & Chambers, K. L. Tropidogyne pentaptera sp. nov., a new mid-Cretaceous fossil angiosperm flower in Burmese amber. Palaeodiversity 10, 135–140 (2017).
    Google Scholar 
    25.Poinar, G. O. & Chambers, K. L. Palaeoanthella huangii gen. and sp. nov., an Early Cretaceous flower (Angiospermae) in Burmese amber. SIDA 21, 2087–2092 (2005).
    Google Scholar 
    26.Goldblatt, P. An analysis of the flora of Southern Africa: its characteristics, relationships, and orgins. Ann. Mo. Bot. Gard. 65, 369–436 (1978).
    Google Scholar 
    27.Verboom, G. A. et al. in Fynbos: Ecology, Evolution and Conservation of a Megadiverse Region (eds Allsopp, N. et al.) 93–118 (Oxford Univ. Press, 2014).28.Hauenschild, F., Favre, A., Michalak, I. & Muellner-Riehl, A. N. The influence of the Gondwanan breakup on the biogeographic history of the ziziphoids (Rhamnaceae). J. Biogeogr. 45, 2669–2677 (2018).
    Google Scholar 
    29.Onstein, R. E. & Linder, H. P. Beyond climate: convergence in fast evolving sclerophylls in Cape and Australian Rhamnaceae predates the mediterranean climate. J. Ecol. 104, 665–677 (2016).
    Google Scholar 
    30.Brown, S., Scott, A. C., Glasspool, I. J. & Collinson, M. E. Cretaceous wildfires and their impact on the Earth system. Cretac. Res. 36, 162–190 (2012).
    Google Scholar 
    31.Richardson, J. E. et al. Rapid and recent origin of species richness in the Cape flora of South Africa. Nature 412, 181–183 (2001).CAS 
    PubMed 

    Google Scholar 
    32.Pillans, N. S. The genus Phylica. J. S. Afr. Bot. 8, 1–164 (1942).
    Google Scholar 
    33.Rebelo, T. et al. in The vegetation of South Africa, Lesotho and Swaziland (eds Mucina, L. & Rutherford, M. C.) 52–219 (South African National Biodiversity Institute, 2006).34.Gimingham, C. H. & Cowling, R. The ecology of fynbos: nutrients, fire and diversity. J. Ecol. 81, 195–196 (1993).
    Google Scholar 
    35.Richardson, J. E., Fay, M. F., Cronk, Q. C. B. & Cronk, M. W. Species delimitation and the origin of populations in island representatives of Phylica (Rhamnaceae). Evolution 57, 816–827 (2003).PubMed 

    Google Scholar 
    36.Richardson, J. E. Molecular Systematics of the Genus Phylica L. With an Emphasis on the Island Species (Edinburgh Univ. Press, 1999).37.Schirarend, C. & Köhler, E. World Pollen and Spore Flora: Rhamnaceae Juss (Scandinavian Univ. Press, 1993).38.Medan, D. & Schirarend, C. in Flowering plants · Dicotyledons (ed. Kubitzki, K.) 320–338 (Springer, 2004).39.Gotelli, M. M., Galati, B. G. & Medan, D. Morphological and ultrastructural studies of floral nectaries in Rhamnaceae. J. Torrey Bot. Soc. 144, 63–73 (2017).
    Google Scholar 
    40.Friedrich, O., Norris, R. D. & Erbacher, J. Evolution of middle to Late Cretaceous oceans–a 55 m.y. record of Earth’s temperature and carbon cycle. Geology 40, 107–110 (2012).CAS 

    Google Scholar 
    41.Lenton, T. M., Daines, S. J. & Mills, B. J. W. COPSE reloaded: an improved model of biogeochemical cycling over Phanerozoic time. Earth Sci. Rev. 178, 1–28 (2018).CAS 

    Google Scholar 
    42.Huber, B. T., Hodell, D. A. & Hamilton, C. P. Middle-Late Cretaceous climate of the southern high latitudes: stable isotopic evidence for minimal equator-to-pole thermal gradients. Geol. Soc. Am. Bull. 107, 1164–1191 (1995).
    Google Scholar 
    43.Belcher, C. M., Yearsley, J. M., Hadden, R. M., Mcelwain, J. C. & Rein, G. Baseline intrinsic flammability of Earth’s ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proc. Natl Acad. Sci. USA 107, 22448–22453 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Berner, R. A., Beerling, D. J., Dudley, R., Robinson, J. M. & Wildman, R. A. Phanerozoic atmospheric oxygen. Annu. Rev. Earth Planet. Sci. 31, 105–134 (2003).CAS 

    Google Scholar 
    45.Glasspool, I. J. & Scott, A. C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat. Geosci. 3, 627–630 (2010).CAS 

    Google Scholar 
    46.Poulsen, C. J., Tabor, C. & White, J. D. Long-term climate forcing by atmospheric oxygen concentrations. Science 348, 1238–1241 (2015).CAS 
    PubMed 

    Google Scholar 
    47.Hudspith, V. A. & Belcher, C. M. Fire biases the production of charred flowers: implications for the Cretaceous fossil record. Geology 45, 727–730 (2017).
    Google Scholar 
    48.Scott, A. C. Charcoal recognition, taphonomy and uses in palaeoenvironmental analysis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 291, 11–39 (2010).
    Google Scholar 
    49.Scott, A. C. The use of charcoal to interpret Cretaceous wildfires and volcanic activity. Glob. Geol. 22, 217–241 (2019).
    Google Scholar 
    50.Scott, A. C., Cripps, J. A., Nichols, G. J. & Collinson, M. E. The taphonomy of charcoal following a recent heathland fire and some implications for the interpretation of fossil charcoal deposits. Palaeogeogr. Palaeoclimatol. Palaeoecol. 164, 1–31 (2000).
    Google Scholar 
    51.Whtilock, C., Higuera, P. E., McWethy, D. B. & Briles, C. E. Paleoecological perspectives on fire ecology: revisiting the fire-regime concept. Open Ecol. J. 3, 6–23 (2010).
    Google Scholar 
    52.Bond, W. J. & Keeley, J. E. Fire as global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol. Evol. 20, 387–394 (2005).PubMed 

    Google Scholar 
    53.Bowman, D. M. J. S. et al. Fire in the Earth system. Science 324, 481–484 (2009).CAS 
    PubMed 

    Google Scholar 
    54.Crisp, M. D., Burrows, G. E., Cook, L. G., Thornhill, A. H. & Bowman, D. M. J. S. Flammable biomes dominated by eucalypts originated at the Cretaceous–Paleogene boundary. Nat. Commun. 2, 193 (2011).PubMed 

    Google Scholar 
    55.Pausas, J. G. & Keeley, J. E. A burning story: the role of fire in the history of life. Bioscience 59, 593–601 (2009).
    Google Scholar 
    56.Scott, A. C. Burning Planet. The Story of Fire Through Time (Oxford Univ. Press, 2018).57.Scott, A. C. Fire: A Very Short Introduction (Oxford Univ. Press, 2020).58.Scott, A. C., Bowman, D. J. M. S., Bond, W. J., Pyne, S. J. & Alexander M. Fire on Earth: An Introduction (J. Wiley & Sons Press, 2014).59.Keeley, J. E., Pausas, J. G., Rundel, P. W., Bond, W. J. & Bradstock, R. A. Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406–411 (2011).CAS 
    PubMed 

    Google Scholar 
    60.Lenton,T. M. in Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. Belcher, C. M.) 289–308 (J. Wiley & Sons Press, 2013).61.Herendeen, P. S., Magallon-Puebla, S., Lupia, R., Crane, P. R. & Kobylinska, J. A preliminary conspectus of the Allon flora from the Late Cretaceous (Late Santonian) of the central Georgia, USA. Ann. Mo. Bot. Gard. 86, 407–471 (1999).
    Google Scholar 
    62.He, T., Pausas, J. G., Belcher, C. M., Schwilk, D. W. & Lamont, B. B. Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol. 194, 751–759 (2012).PubMed 

    Google Scholar 
    63.Cornwell, W. K. et al. Flammability across the gymnosperm phylogeny: the importance of litter particle size. New Phytol. 206, 672–681 (2015).PubMed 

    Google Scholar 
    64.Lamont, B. B. & He, T. Fire-adapted Gondwanan angiosperm floras evolved in the Cretaceous. BMC Evol. Biol. 12, 223 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    65.He, T., Lamont, B. B. & Manning, J. A. Cretaceous origin for fire adaptations in the Cape flora. Sci. Rep. 6, 34880 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.He, T., Lamont, B. B. & Downes, K. S. Banksia born to burn. New Phytol. 191, 184–196 (2011).PubMed 

    Google Scholar 
    67.Midgley, J. & Bond, W. Pushing back in time, the role of fire in plant evolution. New Phytol. 191, 5–7 (2011).PubMed 

    Google Scholar 
    68.Scott, A. C. The Pre-Quaternary history of fire. Palaeogeogr. Palaeoclimatol. Palaeoecol. 164, 281–329 (2000).
    Google Scholar 
    69.Midgley, J. J., Kruger, L. M. & Skelton, R. How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae “fire-resisters”. S. Afr. J. Bot. 77, 381–386 (2011).
    Google Scholar 
    70.Lamont, B. B., Groom, P. K., Williams, M. & He, T. LMA, density and thickness: recognizing different leaf shapes and correcting for their non-laminarity. New Phytol. 207, 942–947 (2015).PubMed 

    Google Scholar 
    71.Lamont, B. B., He, T. & Yan, Z. Evolutionary history of fire-stimulated resprouting, flowering, seed release and germination. Biol. Rev. 94, 903–928 (2019).PubMed 

    Google Scholar 
    72.Schwilk, D. W. & Kerr, B. Genetic niche-hiking: an alternative explanation for the evolution of flammability. Oikos 99, 431–442 (2002).
    Google Scholar 
    73.Kilian, D. & Cowling, R. M. Comparative seed biology and co-existence of two fynbos shrub species. J. Veg. Sci. 3, 637–646 (1992).
    Google Scholar 
    74.Hall, S. A., Newton, R. J., Holmes, P. M., Gaertner, M. & Esler, K. J. Heat and smoke pre‐treatment of seeds to improve restoration of an endangered Mediterranean climate vegetation type. Austral Ecol. 42, 354–366 (2017).
    Google Scholar 
    75.Ruprecht, E., Fenesi, A., Fodor, E. I., Kuhn, T. & Tklyi, J. Shape determines fire tolerance of seeds in temperate grasslands that are not prone to fire. Perspect. Plant Ecol. 17, 397–404 (2015).
    Google Scholar 
    76.Mohr, B. A. R. & Friis, E. M. Early angiosperms from the Lower Cretaceous Crato Formation (Brazil), a preliminary report. Int. J. Plant Sci. 161, 155–167 (2000).
    Google Scholar 
    77.Forest, F. et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760 (2007).CAS 
    PubMed 

    Google Scholar 
    78.Linder, H. P. Evolution of diversity: the Cape flora. Trends Plant Sci. 10, 536–541 (2005).CAS 
    PubMed 

    Google Scholar 
    79.Linder, H. P. The radiation of the Cape flora, southern Africa. Biol. Rev. 78, 597–638 (2003).CAS 
    PubMed 

    Google Scholar 
    80.Poinar, G. O. Burmese amber: evidence of Gondwanan origin and Cretaceous dispersion. Hist. Biol. 31, 1304–1309 (2019).
    Google Scholar 
    81.Oliveira, I. D. S. et al. Earliest onychophoran in amber reveals Gondwanan migration patterns. Curr. Biol. 26, 2594–2601 (2016).CAS 
    PubMed 

    Google Scholar 
    82.Poinar, G. O., Lambert, J. B. & Wu, Y. Araucarian source of fossiliferous Burmese amber: spectroscopic and anatomical evidence. J. Bot. Res. Inst. Tex. 1, 449–455 (2007).
    Google Scholar 
    83.Cai, C. Y. et al. Basal polyphagan beetles in mid-Cretaceous amber from Myanmar: biogeographic implications and long-term morphological stasis. Proc. R. Soc. B 286, 2175 (2019).
    Google Scholar 
    84.Zhang, W., Li, H., Shih, C., Zhang, A. & Ren, D. Phylogenetic analyses with four new Cretaceous bristletails reveal inter-relationships of Archaeognatha and Gondwana origin of Meinertellidae. Cladistics 34, 384–406 (2018).PubMed 

    Google Scholar 
    85.Westerweel, J. et al. Burma Terrane part of the Trans-Tethyan Arc during collision with India according to palaeomagnetic data. Nat. Geosci. 12, 5–6 (2019).
    Google Scholar 
    86.Metcalfe, I. in Biogeography and Geological Evolution of SE Asia (eds Hall, R. & Holloway, J. D.) 25–41 (Backhuys Publishers Press,1998).87.Li, J., Wu, Y., Peng, J. & Batten, D. J. Palynofloral evolution on the northern margin of the Indian Plate, southern Xizang, China during the Cretaceous period and its phytogeographic significance. Palaeogeogr. Palaeoclimatol. Palaeoecol. 515, 107–122 (2019).
    Google Scholar 
    88.Smith, A. G., Smith, D. G. & Funnell B. M. Atlas of Mesozoic and Cenozoic Coastlines (Cambridge Univ. Press, 2004).89.Klages, J. P. et al. Temperate rainforests near the South Pole during peak Cretaceous warmth. Nature 580, 81–86 (2020).CAS 
    PubMed 

    Google Scholar 
    90.Coetzee, J. A. & Muller, J. The phytogeographic significance of some extinct Gondwana pollen types from the Tertiary of the southwestern Cape (South Africa). Ann. Mo. Bot. Gard. 71, 1088–1099 (1984).
    Google Scholar 
    91.De Villiers, S. E. & Cadman, A. The palynology of Tertiary sediments from a palaeochannel in Namaqualand, South Africa. Palaeontol. Afr. 34, 69–99 (1997).
    Google Scholar 
    92.De Villiers, S. E. & Cadman, A. An analysis of the palynomorphs obtained from Tertiary sediments at Koingnaas, Namaqualand, South Africa. J. Afr. Earth Sci. 33, 17–47 (2001).
    Google Scholar 
    93.Sandersen, A., Scott, L., McLachlan, I. R. & Hancox, P. J. Cretaceous biozonation based on terrestrial palynomorphs from two wells in the offshore Orange Basin of South Africa. Palaeontol. Afr. 46, 21–41 (2011).
    Google Scholar 
    94.Hooghiemstra, H., Lézine, A. M., Leroy, S. A. G., Dupont, L. & Marret, F. Late Quaternary palynology in marine sediments: a synthesis of the understanding of pollen distribution patterns in the NW African setting. Quat. Int. 148, 29–44 (1988).
    Google Scholar 
    95.Scholtz, A. The palynology of the upper lacustrine sediments of the Arnot Pipe, Banke, Namaqualand. Ann. S. Afr. Mus. 95, 1–109 (1985).
    Google Scholar 
    96.Sciscio, L. et al. Fluctuations in Miocene climate and sea levels along the south-western South African coast: inferences from biogeochemistry, palynology and sedimentology. Palaeontol. Afr. 48, 2–18 (2013).
    Google Scholar 
    97.Roberts, D. L. et al. Miocene fluvial systems and palynofloras at the southwestern tip of Africa: implications for regional and global fluctuations in climate and ecosystems. Earth Sci. Rev. 124, 184–201 (2013).
    Google Scholar 
    98.Roberts, D. L. et al. Palaeoenvironments during a terminal Oligocene or early Miocene transgression in a fluvial system at the southwestern tip of Africa. Glob. Planet. Change 150, 1–23 (2017).
    Google Scholar 
    99.Grimaldi, D., Engel, M. S. & Nascimbene, P. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am. Mus. Novit. 3361, 1–72 (2002).
    Google Scholar 
    100.Mao, Y. et al. Various amberground marine animals on Burmese amber with discussions on its age. Palaeoentomology 1, 91–103 (2018).
    Google Scholar 
    101.Smith, R. D. & Ross, A. J. Amberground pholadid bivalve borings and inclusions in Burmese amber: implications for proximity of resin-producing forests to brackish waters, and the age of the amber. Earth Env. Sci. Trans. R. Soc. Edinb. 107, 239–247 (2018).
    Google Scholar 
    102.Schmidt, A. R. & Dilcher, D. L. Aquatic organisms as amber inclusions and examples from a modern swamp forest. Proc. Natl Acad. Sci. USA 104, 16581–16585 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    103.Cole, L. E., Bhagwat, S. A. & Willis, K. J. Fire in the swamp forest: palaeoecological insights into natural and human-induced burning in intact tropical peatlands. Front. For. Glob. Change 2, 48 (2019).
    Google Scholar 
    104.Labandeira, C. C. in Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization. The Paleontological Society Papers (eds Laflamme, M. et al.) 163–216 (Cambridge Univ. Press, 2014).105.Seyfullah, L. J. et al. Production and preservation of resins–past and present. Biol. Rev. 93, 1684–1714 (2018).PubMed 

    Google Scholar 
    106.Putz, M. K. & Taylor, E. L. Wound response in fossil trees assemblages from Antarctica and its potential as a palaeoenvironmental indicator. IAWA J. 17, 77–88 (1996).
    Google Scholar 
    107.McKellar, R. C. et al. Insect outbreaks produce distinctive carbon isotope signatures in defensive resins and fossiliferous ambers. Proc. R. Soc. B 278, 3219–3224 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    108.Pausas, J. G. Generalized fire response strategies in plants and animals. Oikos 128, 147–153 (2019).
    Google Scholar 
    109.Schmidt, A. R. et al. Arthropods in amber from the Triassic Period. Proc. Natl Acad. Sci. USA 109, 14796–14801 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    110.Silvestro, D. et al. Fossil data support a pre-Cretaceous origin of flowering plants. Nat. Ecol. Evol. 5, 449–457 (2021).PubMed 

    Google Scholar 
    111.Donoghue, P. Evolution: the flowering of land plant evolution. Curr. Biol. 29, 753–756 (2019).
    Google Scholar 
    112.Thulin, M. et al. Family relationships of the enigmatic rosid genera Barbeya and Dirachma from the Horn of Africa region. Plant Syst. Evol. 213, 103–119 (1998).
    Google Scholar 
    113.Wilf, P., Carvalho, M. R., Gandolfo, M. A. & Cúneo, N. R. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355, 71–75 (2017).CAS 
    PubMed 

    Google Scholar  More