More stories

  • in

    Barrier properties of fungal fruit body skins, pileipelles, contribute to protection against water loss

    1.Nobel, P. S. Physicochemical and Environmental Plant Physiology (Academic Press, 2005).
    Google Scholar 
    2.Hsiao, T. C. Plant responses to water stress. Annu. Rev. Plant Physiol. 24, 519–570 (1973).CAS 
    Article 

    Google Scholar 
    3.Schönherr, J. Resistance of plant surfaces to water loss : transport properties of cutin, suberin and associated lipids. In Encyclopedia Plant Physiology, NS Vol. 12B (eds Lange, O. L. et al.) 154–179 (Springer, 1982).
    Google Scholar 
    4.Lendzian, K. J. Gas permeability of plant cuticles: oxygen permeability. Planta 155, 310–315 (1982).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Langenfeld-Heyser, R. Physiological functions of lenticels. In Trees—Contributions to Modern Tree Physiology (eds Rennenberg, H. et al.) 43–56 (Backhuys, 1997).
    Google Scholar 
    6.Riederer, M. & Schreiber, L. Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52, 2023–2032 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Kerstiens, G. Parameterization, comparison, and validation of models quantifying relative change of cuticular permeability with physicochemical properties of diffusants. J. Exp. Bot. 57, 2525–2533 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Schönherr, J. Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J. Exp. Bot. 57, 2471–2491 (2006).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    9.Groh, B., Hübner, C. & Lendzian, K. J. Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215, 794–801 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Lendzian, K. J. Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. J. Exp. Bot. 57, 2535–2546 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Renault, H. et al. (2017) A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nat. Commun. 8, 14713 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Haas, K. Phytochemische und rasterelektronenmikroskopische Untersuchungen zum Oberflächenwachs von Laubmoosen (Bryatae) (Grauer, 1999).
    Google Scholar 
    13.Clémençon, H., Emmett, V. & Emmett, E. E. Cytology and Plectology of the Hymenomycetes (J Cramer, 2012).
    Google Scholar 
    14.Moore, D., Gange, A. C., Gange, E. G. & Boddy, L. Fruit bodies: their production and development in relation to environment. In Ecology of Saprotrophic Basidiomycetes (eds Boddy, L. et al.) 79–103 (Elsevier Academic Press, 2008).
    Google Scholar 
    15.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).Article 

    Google Scholar 
    16.Sakamoto, Y. Influences of environmental factors on fruiting body induction, development and maturation in mushroom-forming fungi. Fungal Biol. Rev. 32, 236–248 (2018).Article 

    Google Scholar 
    17.Straatsma, G., Ayer, F. & Egli, S. Species richness, abundance, and phenology of fungal fruit bodies over 21 years in a Swiss forest plot. Mycol. Res. 105(5), 515–523 (2001).Article 

    Google Scholar 
    18.Kües, U. & Liu, Y. Fruiting body production in basidiomycetes. Appl. Microbiol. Biotechnol. 54, 141–152 (2000).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Beluhan, S. & Ranogajec, A. Chemical composition and non-volatile components of Croatian wild edible mushrooms. Food Chem. 124, 1076–1082 (2011).CAS 
    Article 

    Google Scholar 
    20.Beecher, T. M., Magan, N. & Burton, K. S. Water potentials and soluble carbohydrate concentrations in tissues of freshly harvested and stored mushrooms (Agaricusbisporus). Postharvest Biol. Technol. 22, 121–131 (2001).CAS 
    Article 

    Google Scholar 
    21.Bonnier G, Mangin L (1884) Recherches sur la respiration et la transpiration des champignons. Ann. Sc. Natur., sér. VI, t. XVII:210–30522.Moser, M. Transpirationsschutz bei höheren Pilzen. Schweizerische Zeitschrift für Pilzkunde 42(4), 50–54 (1964).
    Google Scholar 
    23.Pieschel, E. Über die Transpiration und die Wasserversorgung der Hymenomyceten. Bot. Archiv. VIII, 64–104 (1924).
    Google Scholar 
    24.Seybold, A. Weitere Beiträge zur Transpirationsanalyse. IV. Über die Transpiration der Hutpilze. Planta 16, 518–525 (1932).Article 

    Google Scholar 
    25.Becker, M., Kerstiens, G. & Schönherr, J. Water permeability of plant cuticles: permeance, diffusion and partition coefficients. Trees 1, 54–60 (1986).CAS 
    Article 

    Google Scholar 
    26.Schreiber, L. & Schönherr, J. Water and Solute Permeability of Plant Cuticles. Measurement and Data Analysis (Springer, 2009).
    Google Scholar 
    27.Schönherr, J. & Lendzian, K. J. A simple and inexpensive method of measuring water permeability of isolated plant cuticular membranes. Z Pflanzenphysiol 102, 321–327 (1981).Article 

    Google Scholar 
    28.Weast, R. C. CRC Handbook of Chemistry and Physics: Humidity Constant (CRC Press, 1983).
    Google Scholar 
    29.Riederer, M. & Schneider, G. Comparative study of the composition of waxes extracted from isolated leaf cuticules and from whole leaves of Citrus: evidence for selective extraction. Physiol. Plant 77, 373–384 (1989).CAS 
    Article 

    Google Scholar 
    30.Lendzian, K. J. & Kerstiens, G. Sorption and transport of gases and vapors in plant cuticles. Rev. Environ. Cont. Tox. 121, 65–128 (1991).CAS 

    Google Scholar 
    31.Kerstiens, G., Federholzner, R. & Lendzian, K. J. Dry deposition and cuticular uptake of pollutant gases. Agric. Ecosyst. Environ. 42, 239–253 (1992).CAS 
    Article 

    Google Scholar 
    32.Metzler, H. & Krause, B. Angewandte Statistik (Dt Verlag Wiss, 1983).
    Google Scholar 
    33.Baur, P. Lognormal distribution of water permeability and organic solute mobility in plant cuticles. Plant Cell Environ. 20, 167–177 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Stamets, P. Growing Gourmet and Medicinal Mushrooms (Ten Speed Press, 1993).
    Google Scholar 
    35.Moser, M. Fungal growth and fructification under stress conditions. Ukrainian Botanical J. 50, 5–12 (1993).
    Google Scholar 
    36.Pinna, S., Gevry, M. F., Côté, M. & Sirois, L. Factors influencing fructification phenology of edible mushrooms in a boreal mixed forest of Eastern Canada. For. Ecol. Manag. 260(3), 294–301 (2010).Article 

    Google Scholar 
    37.Buller, A. H. R. Researches on Fungi. II. Further Investigations Upon the Production and Liberation of Spores in Hymenomyctes (Hafner Publishing Co, 1922).
    Google Scholar 
    38.Kües, U. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64, 316–353 (2000).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Money, N. More g’s than the space shuttle: ballistospore discharge. Mycologia 90, 547–558 (1998).Article 

    Google Scholar 
    40.Husher, J. et al. Evaporative cooling of mushrooms. Mycologia 91, 351–352 (1999).Article 

    Google Scholar 
    41.Dressaire, E., Yamada, L., Song, B. & Roper, M. Mushrooms use convectively created airflows to disperse their spores. Proc. Natl. Acad. Sci. U. S. A. 113, 2833–2838 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.De Groot, P. W., Schaap, P. J., Sonnenberg, A. S., Visser, J. & Van Griensven, L. J. The Agaricus bisporus hypAgene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J. Mol. Biol. 257, 1008–1018 (1996).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Wösten, H. A. B. & Wessels, J. G. H. The emergence of fruiting bodies in basidiomycetes. In Growth, Differentiation and Sexuality. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research), Vol. 1 (eds. Kües, U. & Fischer, R.) (Springer, 2006).44.Itoh, Y. H., Sugai, A., Uda, I. & Itoh, T. The evolution of lipids. Adv. Space Res. 28, 719–724 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Segré, D., Ben-Eli, D., Deamer, D. W. & Lancet, D. The lipid world. Origins Life Evol. Biosphere 31, 119–145 (2001).ADS 
    Article 

    Google Scholar 
    46.Samson, R. A., Stalpers, J. A. & Verkerke, W. A simplified technique to prepare fungal specimens for scanning electronmicroscopy. Cytobios 24, 7–11 (1979).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Revisiting traditional SSR based methodologies available for elephant genetic studies

    1.Whyte, I. Studying elephant movements, in studying elephants, in African Wildl. Found. Tech. Ser. 7. African Wildl. Found. (ed Kangwana, K.) 75–89 (1996).2.Rasmussen, L. E. L. & Krishnamurthy, V. How chemical signals integrate Asian elephant society: The known and the unknown. Zoo Biol. 19, 405–423 (2000).CAS 
    Article 

    Google Scholar 
    3.Nair, S., Balakrishnan, R., Seelamantula, C. S. & Sukumar, R. Vocalizations of wild Asian elephants (Elephas maximus ): structural classification and social context. J. Acoust. Soc. Am. 126, 2768–2778 (2009).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Stoeger, A. S. & Manger, P. Vocal learning in elephants: neural bases and adaptive context. Curr. Opin. Neurobiol. 28, 101–107 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Moss, C. J. & Poole, J. H. Relationships and social structure in African elephants. Primate Soc. Relationsh.: An Integr. Approach 315-325 (1983).
    Google Scholar 
    6.Foerder, P., Galloway, M., Barthel, T., Moore, D. E. & Reiss, D. Insightful problem solving in an asian elephant. PLoS ONE 6, e23251 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Lee, P. C. Allomothering among African elephant. Animal Behaviour 35, 278-291 (1987).8.Byrne, R. W., Bates, L. & Moss, C. J. Comparative cognition & behavior reviews. Elephant Cogn. 4, 65–79 (2009).
    Google Scholar 
    9.Bates, L. A., Poole, J. H. & Byrne, R. W. Elephant cognition. Curr. Biol. 18, 544–546 (2008).Article 
    CAS 

    Google Scholar 
    10.Vance, E. A., Archie, E. A. & Moss, C. J. Social networks in African elephants. Comput. Math. Organ. Theory 15, 273–293 (2009).Article 

    Google Scholar 
    11.de Silva, S. & Wittemyer, G. A comparison of social organization in Asian elephants and African savannah elephants. Int. J. Primatol. 33, 1125–1141 (2012).Article 

    Google Scholar 
    12.Shoshani, J. Understanding proboscidean evolution: a formidable task. Trends Ecol. Evol. 13, 480–487 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Rohland, N. et al. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol. 5, 1663–1671 (2007).CAS 
    Article 

    Google Scholar 
    14.de Flamingh, A. Genetic structure of the savannah elephant population (Loxodonta africana (Blumenbach 1797)) in the Kavango-Zambezi Transfrontier Conservation Area. ProQuest Diss. Theses 102 (2013).15.Grubb, P., Groves, C. P., Dudley, J. P. & Shoshani, J. Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2, 1–4 (2000).Article 

    Google Scholar 
    16.Roca, A. L., Georgiadis, N., Pecon-Slattery, J. & O’Brien, S. J. Genetic evidence for two species of elephant in Africa. Science 293, 1473–1477 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Roca, A. L. et al. Elephant natural history: a genomic perspective. Annu. Rev. Anim. Biosci. 3, 139–167 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Wasser, S. K. et al. Assigning African elephant DNA to geographic region of origin: applications to the ivory trade. Proc. Natl. Acad. Sci. U. S. A. 101, 14847–14852 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Ishida, Y. et al. Distinguishing forest and savanna African elephants using short nuclear DNA sequences. J. Hered. 102, 610–616 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Comstock, K. E. et al. Patterns of molecular genetic variation among African elephant populations. Mol. Ecol. 11, 2489–2498 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Palkopoulou, E. et al. A comprehensive genomic history of extinct and living elephants. Proc. Natl. Acad. Sci. U. S. A. 115, E2566–E2574 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Shoshani, J. & Eisenberg, J. F. Elephas maximus. Mamm. Species 182, 1–8 (1982).Article 

    Google Scholar 
    23.Sukumar, R. The Living Elephants (Oxford University Press, 2003).
    Google Scholar 
    24.Sukumar, R. A brief review of the status, distribution and biology of wild Asian elephants Elephas maximus. Int. Zoo Yearb. 40, 1–8 (2006).Article 

    Google Scholar 
    25.Olivier, R. Distribution and status of the Asian elephant. Oryx 14(4), 379–424. https://doi.org/10.1017/S003060530001601X (1978).Article 

    Google Scholar 
    26.Santiapillai, C. The Asian elephant conservation: a global strategy. Gajah 18, 21–39 (1997).
    Google Scholar 
    27.Sukumar, R. Ecology of the Asian elephant in Southern India. i. movement and habitat utilization patterns. J. Trop. Ecol. 5, 1–18 (1989).Article 

    Google Scholar 
    28.Vidya, T. N. C., Fernando, P., Melnick, D. J. & Sukumar, R. Population genetic structure and conservation of Asian elephants (Elephas maximus) across India. Anim. Conserv. 8, 377–388 (2005).Article 

    Google Scholar 
    29.Fleischer, R. C., Perry, E. A., Muralidharan, K., Stevens, E. E. & Wemmer, C. M. Phylogeography of the Asian elephant (Elephas maximus) based on mitochondrial DNA. Evolution (N. Y.) 55, 1882–1892 (2001).CAS 

    Google Scholar 
    30.Fernando, P., Pfrender, M. E., Encalada, S. E. & Lande, R. Mitochondrial DNA variation, phylogeography and population structure of the Asian elephant. Heredity (Edinb). 84, 362–372 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Fernando, P. Elephants in Sri Lanka: past, present, and future. Loris 22, 38–44 (2000).
    Google Scholar 
    32.Hendavitharana, W., Dissanayake, S. & de Silva, M. The survey of elephants in Sri Lanka. Gajah 12, 1–30 (1994).
    Google Scholar 
    33.Eggert, L. S., Rasner, C. A. & Woodruff, D. S. The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Hungarian Q. 49, 1993–2006 (2008).
    Google Scholar 
    34.Ishida, Y., Georgiadis, N. J., Hondo, T. & Roca, A. L. Triangulating the provenance of African elephants using mitochondrial DNA. Evol. Appl. 6, 253–265 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Liu, C. Z., Wang, L., Xia, X. J. & Jiang, J. Q. Characterization of the complete mitochondrial genome of cape elephant shrew, Elephantulus edwardii. Mitochondrial DNA Part B Resour. 3, 738–739 (2018).Article 

    Google Scholar 
    36.Fernando, P. et al. DNA analysis indicates that Asian elephants are native to Borneo and are therefore a high priority for conservation. PLoS Biol. 1, 110–115 (2003).CAS 
    Article 

    Google Scholar 
    37.Ahlering, M. A. et al. Genetic diversity, social structure, and conservation value of the elephants of the Nakai Plateau, Lao PDR, based on non-invasive sampling. Conserv. Genet. 12, 413–422 (2011).Article 

    Google Scholar 
    38.Goossens, B. et al. Habitat fragmentation and genetic diversity in natural populations of the Bornean elephant: implications for conservation. BIOC 196, 80–92 (2016).
    Google Scholar 
    39.Shoshani, J., Golenberg, E. M. & Yang, H. Elephantidae phylogeny: Morphological versus molecular results. Acta Theriol. (Warsz) 43, 89–122 (1998).Article 

    Google Scholar 
    40.Vidya, T. N. C. & Sukumar, R. Amplification success and feasibility of using microsatellite loci amplified from dung to population genetic studies of the Asian elephant (Elephas maximus). Curr. Sci. 88, 489–492 (2005).CAS 

    Google Scholar 
    41.Vidya, T. N. C., Varma, S., Dang, N. X., Van Thanh, T. & Sukumar, R. Minimum population size, genetic diversity, and social structure of the Asian elephant in Cat Tien National Park and its adjoining areas, Vietnam, based on molecular genetic analyses. Conserv. Genet. 8, 1471–1478 (2007).Article 

    Google Scholar 
    42.Suwattana, D., Jirasupphachok, J., Kanchanapangka, S. & Koykul, W. Tetranucleotide microsatellite markers for molecular testing in Thai domestic elephants (Elephas maximus indicus). Thai J. Vet. Med. 40, 405–409 (2010).
    Google Scholar 
    43.Eggert, L. S. et al. Using genetic profiles of African forest elephants to infer population structure, movements, and habitat use in a conservation and development landscape in Gabon. Conserv. Biol. 28, 107–118 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Kinuthia, J. et al. The selection of a standard STR panel for DNA profiling of the African elephant (Loxodonta africana) in Kenya. Conserv. Genet. Resour. 7, 305–307 (2015).Article 

    Google Scholar 
    45.Hedges, S. Monitoring elephant populations and assessing threats. Universities Press (India) Pvt. Ltd., Hyderabad, India 259–292 (2012).46.Eggert, L. S., Ramakrishnan, U., Mundy, N. I. & Woodruff, D. S. Polymorphic microsatellite DNA markers in the African elephant (Loxondonta africana) and their use in the Asian elephant (Elephas maximus). Mol. Ecol. 9, 2222–2224 (2000).Article 

    Google Scholar 
    47.Nyakaana, S., Arctander, P. & Siegismund, H. R. Population structure of the African savannah elephant inferred from mitochondrial control region sequences and nuclear microsatellite loci. Heredity (Edinb). 89, 90–98 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Kongrit, C. et al. Isolation and characterization of dinucleotide microsatellite loci in the Asian elephant (Elephas maximus). Mol. Ecol. Resour. 8, 175–177 (2007).Article 
    CAS 

    Google Scholar 
    49.Fernando, P., Vidya, T. N. C. & Melnick, D. J. Isolation and characterization of tri- and tetranucleotide microsatellite loci in the Asian elephant, Elephas maximus. Mol. Ecol. Resour. 8, 232–233 (2001).Article 

    Google Scholar 
    50.Archie, E. A., Moss, C. J. & Alberts, S. C. Characterization of tetranucleotide microsatellite loci in the African Savannah Elephant (Loxodonta africana africana). Mol. Ecol. Notes 3, 244–246 (2003).CAS 
    Article 

    Google Scholar 
    51.Lieckfeldt, D., Schmidt, A. & Pitra, C. Isolation and characterization of microsatellite loci in the great bustard, Otis tarda. Mol. Ecol. Notes 1, 133–134 (2001).CAS 
    Article 

    Google Scholar 
    52.Nyakaana, S., Okello, J. B. A., Muwanika, V. & Siegismund, H. R. Six new polymorphic microsatellite loci isolated and characterized from the African savannah elephant genome. Mol. Ecol. Notes 5, 223–225 (2005).CAS 
    Article 

    Google Scholar 
    53.Okello, J. B. A. et al. Population genetic structure of savannah elephants in Kenya: conservation and management implications. J. Hered. 99, 443–452 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Nyakaana, S. & Arctander, P. Isolation and characterization of microsatellite loci in the African elephant, Loxodonta africana. Mol. Ecol. 10, 1436–1437 (1998).
    Google Scholar 
    55.Comstock, K. E., Wasser, S. K. & Ostrander, E. A. Polymorphic microsatellite DNA loci identified in the African elephant (Loxodonta africana). Mol. Ecol. 9, 1004–1006 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Hartl, G. B., Hartl, K. F., Hemmer, W. & Nadlinger, K. Electrophoretic and chromosomal variation in captive Asian elephants (Elephas maximus). Zoo Biol. 14, 87–95 (1995).Article 

    Google Scholar 
    57.Bourgeois, S. et al. Single-nucleotide polymorphism discovery and panel characterization in the African forest elephant. Ecol. Evol. 8, 2207–2217 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    58.Sharma, R. et al. Two different high throughput sequencing approaches identify thousands of De Novo genomic markers for the genetically depleted Bornean elephant. PLoS ONE 7, e49533 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Reddy, P. C. et al. Comparative sequence analyses of genome and transcriptome reveal novel transcripts and variants in the Asian elephant Elephas maximus. J. Biosci. 40, 891–907 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Mondol, S. et al. New evidence for hybrid zones of forest and savanna elephants in Central and West Africa. Mol. Ecol. 24, 6134–6147 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Hou, Z. C. et al. Elephant transcriptome provides insights into the evolution of eutherian placentation. Genome Biol. Evol. 4, 713–725 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    62.Tollis, M. et al. Elephant Genomes Reveal Insights into Differences in Disease Defense Mechanisms between Species. bioRxiv 2020.05.29.124396 (2020).63.Rohland, N. et al. Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants. PLoS Biol. 8, 16–19 (2010).Article 
    CAS 

    Google Scholar 
    64.Lynch, V. J. et al. Elephantid genomes reveal the molecular bases of woolly mammoth adaptations to the Arctic. Cell Rep. 12, 217–228 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Yang, H., Golenberg, E. M. & Shoshani, J. Phylogenetic resolution within the elephantidae using fossil DNA sequence from the American mastodon (Mammut americanum) as an outgroup. Proc. Natl. Acad. Sci. U. S. A. 93, 1190–1194 (1996).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Orlando, L., Hänni, C. & Douady, C. J. Mammoth and elephant phylogenetic relationships: Mammut americanum, the missing outgroup. Evol. Bioinforma. 3, 45–51 (2007).CAS 
    Article 

    Google Scholar 
    67.Eggert, L. S., Eggert, J. A. & Woodruff, D. S. Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Mol. Ecol. 12, 1389–1402 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Vidya, T. N. C. Evolutionary history and population genetic structure of Asian elephants in India. Indian J. Hist. Sci. 51, 391–405 (2016).
    Google Scholar 
    69.Schuttler, S. G., Whittaker, A., Jeffery, K. J. & Eggert, L. S. African forest elephant social networks: fission-fusion dynamics, but fewer associations. Endanger. Species Res. 25, 165–173 (2014).Article 

    Google Scholar 
    70.Ahlering, M. A. et al. Identifying source populations and genetic structure for savannah elephants in human-dominated landscapes and protected areas in the Kenya-Tanzania borderlands. PLoS ONE 7, e52288 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Vidya, T. N. C., Fernando, P., Melnick, D. J. & Sukumar, R. Population differentiation within and among Asian elephant (Elephas maximus) populations in southern India. Heredity (Edinb). 94, 71–80 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Sukumar, R., Ramakrishnan, U. & Santosh, J. A. Impact of poaching on an Asian elephant population in Periyar, southern India: a model of demography and tusk harvest. Anim. Conserv. 1, 281–291 (1998).Article 

    Google Scholar 
    73.Mondol, S., Mailand, C. R. & Wasser, S. K. Male biased sex ratio of poached elephants is negatively related to poaching intensity over time. Conserv. Genet. 15, 1259–1263 (2014).Article 

    Google Scholar 
    74.Breuer, T., Maisels, F. & Fishlock, V. The consequences of poaching and anthropogenic change for forest elephants. Conserv. Biol. 30, 1019–1026 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Mailand, C. & Wasser, S. K. Isolation of DNA from small amounts of elephant ivory. Nat. Protoc. 2, 2228–2232 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Lee, E. et al. The identification of elephant ivory evidences of illegal trade with mitochondrial cytochrome b gene and hypervariable D-loop region. J. Forensic Leg. Med. 20, 174–178 (2015).Article 

    Google Scholar 
    77.Chakraborty, S., Boominathan, D., Desai, A. A. & Vidya, T. N. C. Using genetic analysis to estimate population size, sex ratio, and social organization in an Asian elephant population in conflict with humans in Alur, southern India. Conserv. Genet. 15, 897–907 (2014).Article 

    Google Scholar 
    78.Fernando, P. & Pastorini, J. Range-wide status of Asian elephants. Gajah 35, 15–20 (2011).
    Google Scholar 
    79.Ishida, Y., Gugala, N. A., Georgiadis, N. J. & Roca, A. L. Evolutionary and demographic processes shaping geographic patterns of genetic diversity in a keystone species, the African forest elephant (Loxodonta cyclotis). Ecol. Evol. 8, 4919–4931 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Kongrit, C. Genetic tools for the conservation of wild Asian elephants. Int. J. Biol. 9, 1 (2017).Article 

    Google Scholar 
    81.McComb, K., Shannon, G., Sayialel, K. N. & Moss, C. Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. Proc. Natl. Acad. Sci. U. S. A. 111, 5433–5438 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Prithiviraj, F. & Melnick, D. J. Molecular sexing eutherina mammals. Mol. Ecol. Notes 1, 350–353 (2001).Article 

    Google Scholar 
    83.Vandebona, H. et al. DNA fingerprints of the Asian elephant in Sri Lanka, Elephas maximus maximus, using multilocus probe 33.15 (Jeffreys). J. Natl. Sci. Found. Sri Lanka 32, 83–96 (2004).CAS 
    Article 

    Google Scholar 
    84.Gugala, N. A., Ishida, Y., Georgiadis, N. J. & Roca, A. L. Development and characterization of microsatellite markers in the African forest elephant (Loxodonta cyclotis). BMC Res. Notes 9, 4–9 (2016).Article 
    CAS 

    Google Scholar 
    85.Zhang, L. et al. Asian elephants in China: estimating population size and evaluating habitat suitability. PLoS ONE 10, 1–13 (2015).
    Google Scholar 
    86.Vartia, S. et al. A novel method of microsatellite genotyping-by-sequencing using individual combinatorial barcoding. R. Soc. Open Sci. 3, 150565 (2016).ADS 
    MathSciNet 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    87.Tighe, A. J. et al. Testing PCR amplification from elephant dung using silica-dried swabs. Pachyderm 59, 56–65 (2018).
    Google Scholar 
    88.Bourgeois, S. et al. Improving cost-efficiency of faecal genotyping: new tools for elephant species. PLoS ONE 14, e0210811 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Hedges, S., Johnson, A., Ahlering, M., Tyson, M. & Eggert, L. S. Accuracy, precision, and cost-effectiveness of conventional dung density and fecal DNA based survey methods to estimate Asian elephant (Elephas maximus) population size and structure. Biol. Conserv. 159, 101–108 (2013).Article 

    Google Scholar 
    90.Moßbrucker, A. M. et al. Non-invasive genotyping of Sumatran elephants : implications for conservation The Sumatran elephant (Elephas maximus sumatranus) is one of three currently recognized subspecies. Trop. Conserv. Sci. 8, 745–759 (2015).Article 

    Google Scholar 
    91.Ishida, Y. et al. Short amplicon microsatellite markers for low quality elephant DNA. Conserv. Genet. Resour. 4, 491–494 (2012).Article 

    Google Scholar 
    92.Thitaram, C. et al. Evaluation and selection of microsatellite markers for an identification and parentage test of Asian elephants (Elephas maximus). Conserv. Genet. 9, 921–925 (2008).CAS 
    Article 

    Google Scholar 
    93.Lorenz, T. C. Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. J. Vis. Exp. 2, 1–15. https://doi.org/10.3791/3998 (2012).CAS 
    Article 

    Google Scholar 
    94.Litt, M. & Luty, J. A. Hypervariable amplification. Am. J. Hum. Genet. 44, 397–401 (1989).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    95.Park, Y. J., Lee, J. K. & Kim, N. S. Simple sequence repeat polymorphisms (SSRPs) for evaluation of molecular diversity and germplasm classification of minor crops. Molecules 14, 4546–4569 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    96.Vieira, M. L. C., Santini, L., Diniz, A. L. & Munhoz, C. D. F. Microsatellite markers: what they mean and why they are so useful. Genet. Mol. Biol. 39, 312–328 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Stafne, E. T., Clark, J. R., Weber, C. A., Graham, J. & Lewers, K. S. Simple sequence repeat (SSR) markers for genetic mapping of raspberry and blackberry. J. Am. Soc. Hortic. Sci. 130, 722–728 (2005).CAS 
    Article 

    Google Scholar 
    98.Tommasini, L. et al. The development of multiplex simple sequence repeat (SSR) markers to complement distinctness, uniformity and stability testing of rape (Brassica napus L.) varieties. Theor. Appl. Genet. 106, 1091–1101 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    99.Norrgard, K. Forensics, DNA Fingerprinting, and CODIS. Nat. Educ. 1, 35 (2008).
    Google Scholar 
    100.Maroju, P. A. et al. Schrodinger’s scat: A critical review of the currently available tiger (Panthera Tigris) and leopard (Panthera pardus) specific primers in India, and a novel leopard specific primer. BMC Genet. 17, 1–6 (2016).Article 

    Google Scholar 
    101.Waits, L. P. & Pearkau, D. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J. Wildl. Manag. 69, 1419–1433 (2005).Article 

    Google Scholar 
    102.Baird, N. A. et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, 1–7 (2008).Article 
    CAS 

    Google Scholar 
    103.Miller, M. R., Dunham, J. P., Amores, A., Cresko, W. A. & Johnson, E. A. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 17, 240–248 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    104.Delord, C. et al. A cost-and-time effective procedure to develop SNP markers for multiple species: a support for community genetics. Methods Ecol. Evol. 9, 1959–1974 (2018).Article 

    Google Scholar 
    105.Magwanga, R. O. et al. GBS mapping and analysis of genes conserved between Gossypium tomentosum and Gossypium hirsutum cotton cultivars that respond to drought stress at the seedling stage of the BC2F2generation. Int. J. Mol. Sci. 19, 1614 (2018).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    106.Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, 1–10 (2011).Article 
    CAS 

    Google Scholar 
    107.Chandrasekara, C. H. W. M. R. B., Wijesundera, W. S. S., Perera, H. N., Chong, S. S. & Rajan-Babu, I. S. Cascade screening for fragile X syndrome/CGG repeat expansions in children attending special education in Sri Lanka. PLoS ONE 10, 1–10 (2015).
    Google Scholar 
    108.Felsenstein, J. 2002. {PHYLIP}(Phylogen. I. P. ver. 3. 6a3.—P. by the author. PHYLIP(Phylogeny Inference Package) ver. 3.6a3. (2002).109.Nei, M. & Li, W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. U. S. A. 76, 5269–5273 (1979).ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    Article 

    Google Scholar 
    110.Rambaut, A. FigTree ver.1. 3.1: tree figure drawing tool. http://tree.bio.ed.ac.uk/software/figtree. (2009). More

  • in

    Keeping an eye on the use of eye-lens weight as a universal indicator of age for European wild rabbits

    1.Stearns, S. C. The Evolution of Life Histories (Oxford University Press, 1992).
    Google Scholar 
    2.Caughley, G. & Sinclair, A. R. E. Wildlife Ecology and Management (Blackwell Science, 1994).
    Google Scholar 
    3.Servanty, S. et al. Influence of harvesting pressure on demographic tactics: Implications for wildlife management. J. Appl. Ecol. 48(4), 835–843 (2011).Article 

    Google Scholar 
    4.Marboutin, E., Bray, Y., Péroux, R., Mauvy, B. & Lartiges, A. Population dynamics in European hare: Breeding parameters and sustainable harvest rates. J. Appl. Ecol. 40(3), 580–591 (2003).Article 

    Google Scholar 
    5.Stoneberg, R. P. & Jonkel, C. L. Age determination of black bears by cementum layers. J. Wildlife Manage. 30(2), 411–414 (1966).Article 

    Google Scholar 
    6.Roth, V. L. & Shoshani, J. Dental identification and age determination in Elephas maximus. J. Zool. 214, 567–588 (1988).Article 

    Google Scholar 
    7.Dutta, S. & Sengupta, P. Men and mice: Relating their ages. Life Sci. 152, 244–248 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Dimmick, R. W. & Pelton, M. R. Criteria of sex and age. In Research and Management Techniques for Wildlife and Habitats 5th edn, (ed. Bookhout, T.
    A.) 169–214 (The Wildlife Society, Bethesda, MA, US, 1994).
    Google Scholar 
    9.Morris, P. A review of mammalian age determination methods. Mamm. Rev. 2, 69–103 (1972).Article 

    Google Scholar 
    10.Augusteyn, R. C. On the relationship between rabbit age and lens dry weight: Improved determination of the age of rabbits in the wild. Mol. Vis. 13, 2030–2034 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Augusteyn, R. C. Growth of the lens: In vitro observations. Clin. Exp. Optom. 91(3), 226–239 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Augusteyn, R. C. Growth of the eye lens: I. Weight accumulation in multiple species. Mol. Vis. 20, 410–426 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    13.Lord, D. R. The lens as an indicator of age in cottontail rabbits. J. Wildl. Manage. 23, 358–360 (1959).Article 

    Google Scholar 
    14.Forsyth, D. M., Garel, M. & McLeod, S. R. Estimating age and age class of harvested hog deer from eye lens mass using frequentist and Bayesian methods. Wildlife biol. 22(4), 137–143 (2016).Article 

    Google Scholar 
    15.Dudzinski, M. L. & Mykytowycz, R. The eye lens as an indicator of age in the wild rabbit in Australia. CSIRO Wildl. Res. 6, 156–159 (1961).Article 

    Google Scholar 
    16.Myers, K. & Gilbert, N. Determination of age of wild rabbits in Australia. J. Wildl. Manage. 32, 841–849 (1968).Article 

    Google Scholar 
    17.Wheeler, S. H. & King, D. R. The use of eye-lens weights for aging wild rabbits, Oryctolagus cuniculus (L.) in Australia. Aust. Wildl. Res. 7, 79–84 (1980).Article 

    Google Scholar 
    18.Tablado, Z., Revilla, E. & Palomares, F. Breeding like rabbits: Global patterns of variability and determinants of European wild rabbit reproduction. Ecography 32, 310–320. https://doi.org/10.1111/j.1600-0587.2008.05532.x (2009).Article 

    Google Scholar 
    19.Ferreira, C. et al. Biometrical analysis reveals major differences between the two subspecies of the European rabbit. Biol. J. Linn. Soc. 116, 106–116 (2015).Article 

    Google Scholar 
    20.Branco, M., Monnerot, M., Ferrand, N. & Templeton, A. R. Postglacial dispersal of the European rabbit (Oryctolagus cuniculus) on the Iberian Peninsula reconstructed from nested clade and mismatch analyses of mitochondrial DNA genetic variation. Evolution 56, 792–803. https://doi.org/10.1111/j.0014-3820.2002.tb01390.x (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Gómez, A. & Lunt, D. H. Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula. In Phylogeography in Southern European Refugia (eds Weiss, S. & Ferrand, N.) 155–188 (Springer, 2006).
    Google Scholar 
    22.Geraldes, A. et al. Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula. Mol. Ecol. 17, 4489–4499 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Carneiro, M., Ferrand, N. & Nachman, M. W. Recombination and speciation: Loci near centromeres are more differentiated than loci near telomeres between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 181, 593–606 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Rafati, N. et al. A genomic map of clinal variation across the European rabbit hybrid zone. Mol. Ecol. 27, 1457–1478. https://doi.org/10.1111/mec.14494 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Vaquerizas, P. H. et al. The paradox of endangered European rabbits regarded as pests in the Iberian Peninsula: Subspecies differences in trends matter. Endang. Species Res. 43, 99–102 (2020).Article 

    Google Scholar 
    26.Arques, J. & Peiró, V. Estructura de Sexos y Edades de una población de Conejos (Oryctolagus cuniculus) del sudeste de España. Mediterránea. Serie de Estudios Biológicos 18, 1–33 (2005).
    Google Scholar 
    27.Trout, R. C. & Smith, G. C. The reproductive productivity of the wild rabbit (Oryctolagus cuniculus) in southern England on sites with different soils. J. Zool. 237(3), 411–422 (1995).Article 

    Google Scholar 
    28.Boussès, P., Arthur, C. & Chapuis, J. L. Rôle du facteur trophique sur la biologie des populations de lapins (Oryctolagus cuniculus L.) des Iles Kerguelen. Revue d’écologie 43, 329–343 (1988).
    Google Scholar 
    29.Bonino, N. & Donadio, E. Body parameters and sexual dimorphism in the European wild rabbit (Oryctolagus cuniculus) introduced in Argentina. Mastozool. Neotrop. 17(1), 123–127 (2010).
    Google Scholar 
    30.Carneiro, M. et al. Rabbit genome analysis reveals a polygenic basic for phenotypic change during domestication. Science 345(6200), 1074–1079 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Myers, K. The rabbit in Australia. In Dynamics of Numbers in Populations (eds den Boer, P. J. & Gradwell, G. R.) 478–506 (Proceedings of the NATO Advanced Study Institute Oosterbeek, 1970).
    Google Scholar 
    32.Delibes-Mateos, M., Villafuerte, R., Cooke, B. & Alves, P. C. Oryctolagus cuniculus (Linnaeus, 1758). In Lagomorphs: Pikas, Rabbits and Hares of the World (eds Smith, A. T. et al.) 99–104 (John Hopkins University Press, 2018).
    Google Scholar 
    33.Carneiro, M. et al. The genomic architecture of population divergence between subspecies of the European rabbit. PLoS. Genet. 10(8), e1003519. https://doi.org/10.1371/journal.pgen.1003519 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Bonino, N. & Soriguer, R. Genetic lineages of feral populations of the Oryctolagus cuniculus (Leporidae, Lagomorpha) in Argentina. Mammalia 72, 355–357 (2008).Article 

    Google Scholar 
    35.Branco, M. & Ferrand, N. Biochemical and population genetics of the rabbit, Oryctolagus cuniculus, carbonic anhydrases I and II, from the Iberian Peninsula and France. Biochem. Genet. 41, 391–404. https://doi.org/10.1023/B:BIGI.0000007774.39262.8e (2003).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Geraldes, A., Ferrand, N. & Nachman, M. W. Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 173, 919–933 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Lo Valvo, M., Scala, A. & Scalisi, M. Biometric characterization and taxonomic considerations of European rabbit Oryctolagus cuniculus (Linnaeus 1758) in Sicily (Italy). World Rabbit Sci. 22(3), 207–214. https://doi.org/10.4995/wrs.2014.1467 (2014).Article 

    Google Scholar 
    38.Miller, G. S. Catalogue of the Mammals of Western Europe in the Collection of the British Museum (Trustees of the British Museum, 1912).
    Google Scholar 
    39.Sharples, C. M., Fa, J. E. & Bell, D. J. Geographical variation in size in the European rabbit Oryctolagus cuniculus (Lagomorpha: Leporidae) in western Europe and North Africa. Zool. J. Linn. Soc-Lond. 117, 141–158. https://doi.org/10.1111/j.1096-3642.1996.tb02153.x (1996).Article 

    Google Scholar 
    40.Carro, F., Ortega, M. & Soriguer, R. C. Is restocking a useful tool for increasing rabbit densities?. Global Ecol. Conserv. 17, e00560. https://doi.org/10.1016/j.gecco.2019.e00560 (2019).Article 

    Google Scholar 
    41.Angulo, E. & Villafuerte, R. Modelling hunting strategies for the conservation of wild rabbit populations. Biol. Conserv. 115, 291–301 (2003).Article 

    Google Scholar 
    42.Delibes-Mateos, M., Delibes, M., Ferreras, P. & Villafuerte, R. Key role of European rabbits in the conservation of the Western Mediterranean Basin Hotspot. Conserv. Biol. 22, 1106–1117 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Garrido, J. L., Ferreres, J. & Gortázar, C. Las especies cinegéticas españolas en el siglo XXI. (eds. Garrido, J. L., Ferreres, J. & Gortázar, C.)
    (Independently published, Ciudad Real, Spain, 2019).
    Google Scholar 
    44.Ríos-Saldaña, C. et al. Control of the European rabbit in central Spain. Eur. J. Wildlife Res. 59, 573–580. https://doi.org/10.1007/s10344-013-0707-x (2013).Article 

    Google Scholar 
    45.Lees, A. C. & Bell, D. J. A conservation paradox for the 21st century: The European wild rabbit Oryctolagus cuniculus, an invasive alien and an endangered native species. Mammal Rev. 38, 304–320 (2008).Article 

    Google Scholar 
    46.Cooke, B. D. Rabbits: Manageable environmental pests or participants in new Australian ecosystems?. Wildlife Res. 39, 279–289 (2013).ADS 
    Article 

    Google Scholar 
    47.Calvete, C., Angulo, E. & Estrada, R. Conservation of European wild rabbit populations when hunting is age and sex selective. Biol. Conserv. 121(4), 623–634 (2005).Article 

    Google Scholar 
    48.Delibes-Mateos, M., Ramírez, E., Ferreras, P. & Villafuerte, R. Translocations as a risk for the conservation of European wild rabbit Oryctolagus cuniculus lineages. Oryx 42(2), 259–264 (2008).Article 

    Google Scholar 
    49.Andersen, J. & Jensen, B. Studies on the European hare. XXVIII. The weight of the eye lens in the European hares of known age. Acta Theriol. 17, 87–92 (1972).Article 

    Google Scholar 
    50.Suchentrunck, F., Willing, R. & Hartl, G. B. On eye lens weights and other age criteria of the Brown hare (Lepus europaeus Pallas, 1778). Z. Säugetierkd. 56, 365–374 (1991).
    Google Scholar 
    51.Villafuerte, R. et al. Large-scale assessment of myxomatosis prevalence in European wild rabbits (Oryctolagus cuniculus) 60 years after first outbreak in Spain. Res. Vet. Sci. 114, 281–286 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Rouco, C., Villafuerte, R., Castro, F. & Ferreras, P. Effect of artificial warren size on a restocked European wild rabbit population. Anim. Conserv. 14, 117–123 (2011).Article 

    Google Scholar 
    53.Southern, N. The ecology and population dynamics of the wild rabbit (Oryctolagus cuniculus). Ann. Appl. Biol. 27, 509–514 (1940).Article 

    Google Scholar 
    54.Dunnet, G. M. Growth rate of young rabbits, Oryctolagus cuniculus (L.). CSIRO Wildl. Res. 1, 66–67 (1956).Article 

    Google Scholar 
    55.Ferreira, A. & Ferreira, A. J. Post-weaning growth of endemic Iberian wild rabbit subspecies, Oryctolagus cuniculus algirus, kept in a semi-extensive enclosure: Implications for management and conservation. World Rabbit Sci. 22, 129–136. https://doi.org/10.4995/wrs.2014.1673 (2014).Article 

    Google Scholar 
    56.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (Vienna,
    Austria, 2020).
    Google Scholar 
    57.du Sert, N. P. et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 18(7), e3000411. https://doi.org/10.1371/journal.pbio.3000411 (2020).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    58.Burnham, K. P. & Anderson, D. R. Monte Carlo insights and extended examples. In Model Selection and Multimodel Inference, (eds. Burnham K. P. &
    Anderson D. R.) https://doi.org/10.1007/978-0-387-22456-5_5). (Springer, New York, NY, US, 2002).59.Pastore, M. Overlapping: A R package for estimating overlapping in empirical distributions. J. Open Source Softw. 32, 1023 (2018).ADS 
    Article 

    Google Scholar 
    60.Pastore, M. & Calcagnì, A. Measuring distribution similarities between samples: A distribution-free overlapping Index. Front. Psychol. 10, 1089 https://doi.org/10.3389/fpsyg.2019.01089 (2019).Article 

    Google Scholar 
    61.Williams, C. & Moore, R. Phenotypic adaptation and natural selection in the wild rabbit, Oryctolagus cuniculus, Australia. J. Anim. Ecol. 58(2), 495–507. https://doi.org/10.2307/4844 (1989).Article 

    Google Scholar  More

  • in

    New lineages of photobionts in Bolivian lichens expand our knowledge on habitat preferences and distribution of Asterochloris algae

    1.Fernández-Brime, S., Muggia, L., Maier, S., Grube, M. & Wedin, M. Bacterial communities in an optional lichen symbiosis are determined by substrate, not algal photobionts. FEMS Microbiol. Ecol. 95, fiz012 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    2.Grube, M. et al. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J. 9, 412–424 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Spribille, T. et al. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488–492 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Peksa, O. & Škaloud, P. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol. Ecol. 20, 3936–3948 (2011).PubMed 
    Article 

    Google Scholar 
    5.Řídká, T., Peksa, O., Rai, H., Upreti, D. K. & Škaloud, P. Photobiont diversity in Indian Cladonialichens, with special emphasis on the geographical patterns. In Terricolous Lichens in India, Volume 1: Diversity Patterns and Distribution Ecology (eds Rai, H. & Upreti, D. K.) 53–71 (Springer, New York, 2014).
    Google Scholar 
    6.Rolshausen, G. et al. Expanding the mutualistic niche: Parallel symbiont turnover along climatic gradients. Proc. R. Soc. B 287, 1924 (2020).Article 

    Google Scholar 
    7.Kosecka, M. et al. Trentepohlialean algae (Trentepohliales, Ulvophyceae) show preference to selected mycobiont lineages in lichen symbioses. J. Phycol. 56, 979–993 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Muggia, L., Pérez-Ortega, S., Kopun, T., Zellnig, G. & Grube, M. Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Ann. Bot. 114, 463–475 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Vančurová, L., Muggia, L., Peksa, O., Řídká, T. & Škaloud, P. The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (lichenized Ascomycota). Mol. Ecol. 27, 3016–3033 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    10.Beck, A., Kasalicky, T. & Rambold, G. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol. 153, 317–326 (2002).Article 

    Google Scholar 
    11.Nelsen, M. P. & Gargas, A. Actin type intron sequences increase phylogenetic resolution: An example from Asterochloris (Chlorophyta: Trebouxiophyceae). Lichenologist 38, 435–440 (2006).Article 

    Google Scholar 
    12.Nelsen, M. P. & Gargas, A. Dissociation and horizontal transmission of co-dispersed lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol. 177, 264–275 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Škaloud, P. & Peksa, O. Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris. Mol. Phylogenet. Evol. 54, 36–46 (2010).PubMed 
    Article 

    Google Scholar 
    14.Škaloud, P., Steinová, J., Řídká, T., Vančurová, L. & Peksa, O. Assembling the challenging puzzle of algal biodiversity: Species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). J. Phycol. 51, 507–527 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    15.Steinová, J., Škaloud, P., Yahr, R., Bestová, H. & Muggia, L. Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol. Phylogenet. Evol. 134, 226–237 (2019).PubMed 
    Article 

    Google Scholar 
    16.Vančurová, L., Peksa, O., Němcová, Y. & Škaloud, P. Vulcanochloris (Trebouxiales, Trebouxiophyceae), a new genus of lichen photobiont from La Palma, Canary Islands, Spain. Phytotaxa 219, 118–132 (2015).Article 

    Google Scholar 
    17.Vančurová, L. et al. Symbiosis between river and dry lands: Phycobiont dynamics on river gravel bars. Algal Res. 51, 102062. https://doi.org/10.1016/j.algal.2020.102062 (2020).Article 

    Google Scholar 
    18.Yahr, R., Vilgalys, R. & Depriest, P. T. Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol. Ecol. 13, 3367–3378 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Tschermak-Woess, E. Asterochloris phycobiontica gen. et spec. nov., der Phycobiont der Flechte Varicellaria carneonivea. Plant Syst. Evol. 135, 279–294 (1980).Article 

    Google Scholar 
    20.Moya, P. et al. Molecular phylogeny and ultrastructure of the lichen microalga Asterochloris mediterranea sp. Nov. from Mediterranean and Canary Islands ecosystems. Int. J. Syst. Evol. Microbiol. 65(6), 1838–1854 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    21.Kim, J. I. et al. Asterochloris sejongensis sp. nov. (Trebouxiophyceae, Chlorophyta) from King George Island, Antarctica. Phytotaxa 295, 60–70 (2017).Article 

    Google Scholar 
    22.Kim, J. I. et al. Taxonomic study of three new Antarctic Asterochloris(Trebouxio-phyceae) based on morphological and molecular data. Korean Soc. Phycol. 35(1), 17–32 (2020).CAS 

    Google Scholar 
    23.Pino-Bodas, R. & Stenroos, S. Global biodiversity patterns of the photobionts associated with the genus Cladonia (Lecanorales, Ascomycota). Microb. Ecol. https://doi.org/10.1007/s00248-020-01633-3 (2020).Article 
    PubMed 

    Google Scholar 
    24.Fernandez-Mendoza, F. et al. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol. 20, 1208–1232 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Helms, G. Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Göttingen, Doctoral thesis. Germany: Georg-August Universität Göttingen (2003).26.Kroken, S. & Taylor, J. W. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103, 645–660 (2000).CAS 
    Article 

    Google Scholar 
    27.Leavitt, S. D. et al. Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen- forming family Parmeliaceae (Ascomycota). Mol. Ecol. 24, 3779–3797 (2015).PubMed 
    Article 

    Google Scholar 
    28.Magain, N., Miadlikowska, J., Goffinet, B., Sérusiaux, E. & Lutzoni, F. Macroevolution of Specificity in Cyanolichens of the Genus Peltigera Section Polydactylon (Lecanoromycetes, Ascomycota). Syst. Biol. 66, 74–99 (2016).
    Google Scholar 
    29.Mark, K. et al. Contrasting cooccurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol. 227, 1362–1375 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.O’Brien, H. E., Miadlikowska, J. & Lutzoni, F. Assessing population structure and host specialization in lichenized cyanobacteria. New Phytol. 198, 557–566 (2013).PubMed 
    Article 

    Google Scholar 
    31.Piercey-Normore, M. D. & DePriest, P. T. Algal switching among lichen symbionts. Am. J. Bot. 88, 1490–1498 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Yahr, R., Vilgalys, R. & DePriest, P. T. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol. 171, 847–860 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Muggia, L. et al. The symbiotic playground of lichen thalli—A highly flexible photobiont association in rock inhabiting lichens. FEMS Microbiol. Ecol. 85, 313–323 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    34.Sadowska-Deś, A. D. et al. Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia. Mol. Phylogenet. Evol. 76, 202–210 (2014).PubMed 
    Article 

    Google Scholar 
    35.Wirtz, N. et al. Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol. 160, 177–183 (2003).Article 

    Google Scholar 
    36.Ertz, D., Guzow-Krzemińska, B., Thor, G., Łubek, A. & Kukwa, M. Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci Rep. 8, 4952 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Marshall, W. A. & Chalmers, M. O. Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography 20, 585–594 (1997).Article 

    Google Scholar 
    38.Printzen, C., Domaschke, S., Fernandez-Mendoza, F. & Perez-Ortega, S. Biogeography and ecology of Cetraria aculeata, a widely distributed lichen with a bipolar distribution. MycoKeys 6, 33–53 (2013).Article 

    Google Scholar 
    39.Pardo-De la Hoz, C. J. et al. Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus Peltigera. Front. Microbiol. 9, 2770–2770 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Singh, G. et al. Fungal–algal association patterns in lichen symbiosis linked to macroclimate. New Phytol. 214, 317–329 (2017).PubMed 
    Article 

    Google Scholar 
    41.Cordeiro, L. M. C. et al. Molecular studies of photobionts of selected lichens from the coastal vegetation of Brazil. FEMS Microbiol. Ecol. 54, 381–390 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Pullaiah, T. (ed.) (2019) Biodiversity in Bolivia in: Global Biodiversity Volume 4: Selected Countries in the Americas and Australia, Chapter 1. 1–574 (Apple Academic Press, 2001).43.Ibisch, P. L. & Mérida, G. Biodiversity: the richness of Bolivia. State of knowledge and conservation. 1–638 (Ministry of Sustainable Development, Editorial FAN, 2004).44.Werth, S. & Sork, V. L. Ecological specialization in Trebouxia (Trebouxiophyceae) photobionts of Ramalina menziesii (Ramalinaceae) across six range-covering ecoregions of western North America. Am. J. Bot. 101, 1127–1140 (2014).PubMed 
    Article 

    Google Scholar 
    45.Rolshausen, G., Dal Grande, F., Sadowska-Deś, A. D., Otte, J. & Schmitt, I. Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualistmediated niche expansions. Ecography 41, 1380–1392 (2018).Article 

    Google Scholar 
    46.Blaha, J., Baloch, E. & Grube, M. High photobiont diversity insymbioses of the euryoecious lichen Lecanora rupicola (Lecanoraceae, Ascomycota). Biol. J. Linn. Soc. 88, 283–293 (2006).Article 

    Google Scholar 
    47.Vargas Castillo, R. & Beck, A. Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biol. 116, 665–676 (2012).PubMed 
    Article 

    Google Scholar 
    48.Bačkor, M., Klemová, K., Bačkorová, M. & Ivanova, V. Comparison of the phytotoxic effects of usnic acid on cultures of free-living alga Scenedesmus quadricauda and aposymbiotically grown lichen photobiont Trebouxia erici. J. Chem. Ecol. 36, 405–411 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    49.Galloway, D. J. Lichen biogeography. In: Nash T. H. (ed.) Lichen Biology, 315–335 (Cambridge University Press, 2008).50.Dal Grande, F. et al. Environment and host identity structure communities of green algal symbionts in lichens. New Phytol. 217, 277–289 (2017).Article 
    CAS 

    Google Scholar 
    51.Dal Grande, F., Widmer, I., Wagner, H. H. & Scheidegger, C. Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol. Ecol. 21, 3159–3172 (2012).Article 

    Google Scholar 
    52.Otálora, M. A. G. et al. Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Mol. Phylogenet. Evol. 56, 1089–1095 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    53.Ruprecht, U., Fernández-Mendoza, F., Türk, R. & Fryday, A. High levels of endemism and local differentiation in the fungal and algal symbionts of saxicolous lecideoid lichens along a latitudinal gradient in southern South America. Lichenologist 52, 287–303 (2020).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    54.Ahti, T., Cladoniaceae in Flora Neotropica Monograph 78. 2–362 (New York Botanical Garden Press, 2000).55.Parnmen, S., Leavitt, S. D., Rangsiruji, A. & Lumbsch, H. T. Identification of species in the Cladia aggregata group using DNA barcoding (Ascomycota: Lecanorales). Phytotaxa 115, 1–14 (2013).Article 

    Google Scholar 
    56.Guzow-Krzemińska, B. et al. New species and records of lichens from Bolivia. Phytotaxa 397, 257–279 (2019).Article 

    Google Scholar 
    57.Sipman, H. J. M. Survey of Lepraria species with lobed thallus margins in the tropics. Herzogia 17, 23–35 (2004).
    Google Scholar 
    58.Saag, L., Saag, A. & Randlane, T. World survey of the genus Lepraria (Stereocaulaceae, lichenized Ascomycota). Lichenologist 41, 25–60 (2009).Article 

    Google Scholar 
    59.Guzow-Krzemińska, B. et al. Phylogenetic placement of Lepraria cryptovouauxii sp. nov. (Lecanorales, Lecanoromycetes, Ascomycota) with notes on other Lepraria species from South America. MycoKeys 53, 1–22 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Orange, A., James, P. W. & White, F. J. Microchemical Methods for the Identification of Lichens. 1–101 (British Lichen Society, 2001).61.Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst. Evol. 216, 243–249 (1999).CAS 
    Article 

    Google Scholar 
    62.White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics in PCR Protocols: A Guide to Methods and Applications (eds Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J.) 345–322 (Academic Press, 1990).63.Sherwood, A. R., Garbary, D. J. & Sheath, R. G. Assessing the phylogenetic position of the Prasiolales (Chlorophyta) using rbcL and 18S rRNA gene sequence data. Phycologia 39, 139–146 (2000).Article 

    Google Scholar 
    64.Nelsen, M. P., Rivas Plata, E., Andrew, C. J., Lücking, R. & Lumbsch, H. T. Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J. Phycol. 47, 282–290 (2011).PubMed 
    Article 

    Google Scholar 
    65.Widmer, I., Dal Grande, F., Cornejo, C. & Scheidegger, C. Highly variable microsatellite markers for the fungal and algal symbionts of the lichen Lobaria pulmonaria and challenges in developing biont-specific molecular markers for fungal associations. Fungal Biol. 114, 538–544 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    66.Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    Article 

    Google Scholar 
    67.Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Okonechnikov, K., Golosova, O. & Fursov, M. UGENE team. Unipro GENE: A unified bioinformatics toolkit. Bioinformatics 28, 1166–1167 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    Article 

    Google Scholar 
    73.Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE): 1–8 (2010).74.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2016).
    Google Scholar 
    75.Rambaut, A. FigTreev1.4.2. Retrieved from: http://tree.bio.ed.ac.uk/software/figtree/ (2006–2014).76.Oksanen, et al., vegan: Community ecology package manual. Retrieved from https://cran.rproject.org/package=vegan (2017).77.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).Article 

    Google Scholar 
    78.Borcard, D., Legendre, P., Avois-Jacquet, C. & Tuomisto, H. Dissecting the spatial structure of ecological data at multiple scales. Ecology 85, 1826–1832 (2004).Article 

    Google Scholar 
    79.Lefeuvre, P. BoSSA: A bunch of structure and sequence analysis manual. Retrieved from https://cran.r-project.org/package=BoSSA (2018).80.McArdle, B. H. & Anderson, M. J. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82, 290–297 (2001).Article 

    Google Scholar 
    81.Stenroos, S., Pino-Bodas, R., Hyvönen, J., Lumbsch, T. H. & Ahti, T. Phylogeny of family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. Cladistics 35, 351–384 (2019).Article 

    Google Scholar 
    82.R Core Team. R: A Language and Environment for Statistical Computing.83.https://www.R-project.org/ (2017).84.RStudio Team. RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL http://www.rstudio.com/ (2018).85.Aktas, C. Manipulating DNA Sequences and Estimating Unambiguous Haplotype Network with Statistical Parsimony. Retrieved from https://CRAN.R project.org/package=haplotypes (2020).86.Piel, W. H., Chan, L., Dominus, M. J., Ruan, J., Vos, R. A., and V. Tannen. TreeBASE v. 2: A Database of Phylogenetic Knowledge. In: e-BioSphere (2009) More

  • in

    Substituting chemical P fertilizer with organic manure: effects on double-rice yield, phosphorus use efficiency and balance in subtropical China

    1.Kazunori, M. et al. Prediction of future methane emission from irrigated rice paddies in central Thailand under different water management practices. Sci. Total Environ. 566, 641–651 (2016).
    Google Scholar 
    2.FAOSTAT. http://www.fao.org/statistics/zh. (2018).3.Xu, L. et al. Effects of different fertilization treatment on paddy soil nutrients in red soil hilly region. J. Nat. Resour. 27, 1890–1898 (2012) (In Chinese).
    Google Scholar 
    4.National Bureau of Statistics of China. China Statistical Yearbook (China Statistics Press, 2010) (In Chinese).
    Google Scholar 
    5.Li, H. G. et al. Past, present, and future use of phosphorus in Chinese agriculture and its influence on phosphorus losses. Ambio 44, S274–S285 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    6.Withers, P. J. A. et al. Stewardship to tackle global phosphorus inefficiency: The case of Europe. Ambio 44(Suppl. 2), 193–206 (2015).CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    7.Huang, Q. H. et al. Effects of long-term organic amendments on soil organic carbon in a paddy field: A case study on red soil. J. Integr. Agric. 13, 570–576 (2014).Article 

    Google Scholar 
    8.Wang, H. et al. Effects of long-term application of organic fertilizer on improving organic matter content and retarding acidity in red soil from China. Soil Tillage Res. 195, 104382 (2019).Article 

    Google Scholar 
    9.Qaswar, M. et al. Yield sustainability, soil organic carbon sequestration and nutrients balance under long-term combined application of manure and inorganic fertilizers in acidic paddy soil. Soil Tillage Res. 198, 104569 (2020).Article 

    Google Scholar 
    10.Blake, L. et al. Phosphorus content in soil, uptake by plants and balance in three European long-term field experiments. Nutr. Cycl. Agroecosyst. 56, 263–275 (2000).Article 

    Google Scholar 
    11.Dawe, D., Dobermann, A., Ladha, J. K. & Zhen, Q. X. Do organic amendments improve yield trends and profitability in intensive rice systems?. Field Crop. Res. 83, 191–213 (2003).Article 

    Google Scholar 
    12.Nziguheba, G., Merckx, R. & Palm, C. A. Soil phosphorus dynamics and maize response to different rates of phosphorus fertilizer applied to an acrisol in Western Kenya. Plant Soil 243, 1–10 (2002).CAS 
    Article 

    Google Scholar 
    13.Xu, M. G. et al. Effects of organic manure application with chemical fertilizers on nutrient absorption and yield of rice in hunan of Southern China. Agric. Sci. China 7, 1245–1252 (2008).Article 

    Google Scholar 
    14.Bi, L. et al. Long-term effects of organic amendments on the rice yields for double rice cropping systems in subtropical China. Agric. Ecosyst. Environ. 129, 534–541 (2009).Article 

    Google Scholar 
    15.Zhao, B. Q. et al. Long-term fertilizer experiment network in China: Crop yields and soil nutrient trends. Agron. J. 102, 216–230 (2010).CAS 
    Article 

    Google Scholar 
    16.Gao, Y. et al. Phosphorus and carbon competitive sorption-desorption and associated non-point loss respond to natural rainfall events. J. Hydrol. 517, 447–457 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    17.Powers, S. M. et al. Long-term accumulation and transport of anthropogenic phosphorus in three river basins. Nat. Geosci. 9, 353–356 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    18.Abe, S. S. et al. Excessive application of farmyard manure reduces rice yield and enhances environmental pollution risk in paddy fields. Arch. Agron. Soil Sci. 62, 1208–1221 (2016).Article 

    Google Scholar 
    19.Sato, S. & Comerford, N. B. Influence of soil pH on inorganic phosphorus sorption and desorption in a humid Brazilian ultisol. Rev. Bras. Ciênc. Solo 29, 685–694 (2005).CAS 
    Article 

    Google Scholar 
    20.Shasheen, S. & Tsadilas, C. Phosphorus sorption and availability to canola grown in an alfisol amended with various soil amendments. Commun. Soil Sci. Plan. 44, 89–103 (2013).Article 
    CAS 

    Google Scholar 
    21.Shepherd, M. A. & Withers, P. J. Applications of poultry litter and triple superphosphate fertilizer to a sandy soil: Effects on soil phosphorus status and profile distribution. Nutr. Cycl. Agroecosyst. 54, 233–242 (1999).Article 

    Google Scholar 
    22.Morteza, Y., Javad, S. & Mahmood, S. S. On dealing with the pollution costs in agriculture: A case study of paddy fields. Sci. Total Environ. 556, 310–318 (2016).Article 
    CAS 

    Google Scholar 
    23.Zhang, N.M., Li, C.X. & Li, Y.H. Accumulation and releasing risk of phosphorus in soils in Dianchi watershed. Soils 39, 665–667. (2007). (in Chinese). 24.Zhang, Z. J., Zhang, J. Y., He, R., Wang, Z. D. & Zhu, Y. M. Phosphorus interception in floodwater of paddy field during the rice-growing season in TaiHu Lake Basin. Environ. Pollut. 145, 425–433 (2007) (In Chinese).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Hua, L. et al. Risks of phosphorus runoff losses from five Chinese paddy soils under conventional management practices. Agric. Ecosyst. Environ. 245, 112–123 (2017).CAS 
    Article 

    Google Scholar 
    26.Challinor, A. J. et al. A meta-analysis of crop yield under climate change and adaptation. Nat. Clim. Change 4, 287–291 (2014).ADS 
    Article 

    Google Scholar 
    27.Shi, W. et al. Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol. 197, 825–837 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Andriamananjara, A. et al. Farmyard manure application in weathered upland soils of Madagascar sharply increase phosphate fertilizer use efficiency for upland rice. Field Crop. Res. 222, 94–100 (2018).Article 

    Google Scholar 
    29.Andriamananjara, A. et al. Farmyard manure improves phosphorus use efficiency in weathered P deficient soil. Nutr. Cycl. Agroecosyst. 115, 407–425 (2019).CAS 
    Article 

    Google Scholar 
    30.Seufert, V., Ramankutty, N. & Foley, J. A. Comparing the yields of organic and conventional agriculture. Nature 485, 229-U113 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Xin, X. et al. Yield, phosphorus use efficiency and balance response to substituting long-term chemical fertilizer use with organic manure in a wheat-maize system. Field Crop. Res. 208, 27–33 (2017).Article 

    Google Scholar 
    32.Aggarwal, R. K. & Power, J. F. Use of crop residue and manure to conserve water and enhance nutrient availability and pearl millet yields in an arid tropical region. Soil Tillage Res. 41, 43–51 (1997).Article 

    Google Scholar 
    33.Rehman, A., Ullah, A., Nadeem, F. & Farooq, M. Sustainable nutrient management. In Innovations in Sustainable Agriculture 167–211 (Springer, 2019).34.Whalen, J. K., Chang, C., Clayton, G. W. & Carefoot, J. P. Cattle manure amendments can increase the pH of acid soils. Soil Sci. Soc. Am. J. 64, 962–966 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    35.Mowrer, J., Endale, D. M., Schomberg, H. H., Norris, S. E. & Woodroof, R. H. Liming potential of poultry litter in a long-term tillage comparison study. Soil Tillage Res. 196, 104446 (2020).Article 

    Google Scholar 
    36.Miller, J., Beasley, B., Drury, C., Larney, F. & Hao, X. Y. Influence of long-term application of composted or stockpiled feedlot manure with straw or wood chips on soil cation exchange capacity. Compos. Sci. Util. 24, 54–60 (2016).CAS 
    Article 

    Google Scholar 
    37.Liang, Y. et al. Organic manure stimulates biological activity and barley growth in soil subject to secondary salinization. Soil Biol. Biochem. 37, 1185–1195 (2005).CAS 
    Article 

    Google Scholar 
    38.Güsewell, S. N:P ratios in terrestrial plants: Variation and functional significance. New Phytol. 164, 243–266 (2004).Article 

    Google Scholar 
    39.Khan, F. et al. Effect of different levels of nitrogen and phosphorus on the phenology and yield of maize varieties. Am. J. Plant Sci. 5, 2582–2590 (2014).CAS 
    Article 

    Google Scholar 
    40.Luo, X. et al. Nitrogen: Phosphorous supply ratio and allometry in five alpine plant species. Ecol. Evol. 6, 8881–8892 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Güsewell, S. Responses of wetland graminoids to the relative supply of nitrogen and phosphorus. Plant Ecol. 176, 35–55 (2005).Article 

    Google Scholar 
    42.Hu, B. et al. Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat. Plants 5, 401–413 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Zhang, W. F. et al. Efficiency, economics, and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutr. Cycl. Agroecosyst. 80, 131–144 (2008).Article 

    Google Scholar 
    44.Andriamananjara, A. et al. Land management modifies the temperature sensitivity of soil organic carbon, nitrogen and phosphorus dynamics in a Ferralsol. Appl. Soil Ecol. 138, 112–122 (2019).Article 

    Google Scholar 
    45.Nziguheba, G., Merckx, R., Palm, C. A. & Rao, M. R. Organic residues affect phosphorus availability and maize yields in a Nitisol of Western Kenya. Biol. Fertil. Soils 32, 328–339 (2000).CAS 
    Article 

    Google Scholar 
    46.Peretyazhko, T. & Sposito, G. Iron(III) reduction and phosphorous solubilization in humid tropical forest soils. Geochim. Cosmochim. Acta 69, 3643–3652 (2005).ADS 
    CAS 
    Article 

    Google Scholar 
    47.Wright, A. L. Soil phosphorus stocks and distribution in chemical fractions for long-term sugarcane, pasture, turfgrass, and forest systems in Florida. Nutr. Cycl. Agroecosyst. 83, 223–231 (2009).CAS 
    Article 

    Google Scholar 
    48.Zhong, X. et al. The evaluation of phosphorus leaching risk of 23 Chinese soils I. Leaching criterion. Acta Ecol. Sin. 24, 2275–2280 (2004).
    Google Scholar 
    49.Wang, S. et al. Phosphorus loss potential and phosphatase activity under phosphorus fertilization in long-term paddy wetland agroecosystems. Soil Sei. Soc. Am. J. 6, 161–167 (2012).Article 
    CAS 

    Google Scholar 
    50.Haynes, R. J. & Mokolobate, M. S. Amelioration of Al toxicity and P deficiency in acid soils by additions of organic residues: A critical review of the phenomenon and the mechanisms involved. Nutr. Cycl. Agroecosyst. 59, 47–63 (2001).CAS 
    Article 

    Google Scholar 
    51.Ayaga, G., Todd, A. & Brookes, P. C. Enhanced biological cycling of phosphorus increases its availability to crops in low-input sub-Saharan farming systems. Soil Biol. Biochem. 38, 81–90 (2006).CAS 
    Article 

    Google Scholar 
    52.Nie, J., Zhou, J., Wang, H., Chen, X. & Du, C. Effect of long-term rice straw return on soil glomalin, carbon and nitrogen. Pedosphere 17, 295–302 (2007).CAS 
    Article 

    Google Scholar 
    53.Yu, Y. et al. Responses of paddy soil bacterial community assembly to different long-term fertilizations in southeast China. Sci. Total Environ. 656, 625–633 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Murphy, J. & Riley, J. P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. A. 27, 31–36 (1962).CAS 
    Article 

    Google Scholar 
    55.Kitson, R. E. & Mellon, M. G. Colorimetric determination of phosphorus as molybdivanadophosporic acid. Ind. Eng. Chem. Anal. Ed. 16, 379–383 (1944).CAS 
    Article 

    Google Scholar 
    56.Soon, Y. K. & Kalra, Y. P. A comparison of plant tissue digestion methods for nitrogen and phosphorus analyses. Can. J. Soil Sci. 75, 243–245 (1995).CAS 
    Article 

    Google Scholar  More

  • in

    The serotonin transporter gene and female personality variation in a free-living passerine

    1.Réale, D., Dingemanse, N. J., Kazem, A. J. N. & Wright, J. Evolutionary and ecological approaches to the study of personality. Philos. Trans. R. Soc. B. 365, 3937–3946 (2010).Article 

    Google Scholar 
    2.Dingemanse, N. J. & Wright, J. Criteria for acceptable studies of animal personality and behavioural syndromes. Ethology 126, 865–869 (2020).Article 

    Google Scholar 
    3.Wilson, D. S. Adaptive individual differences within single populations. Philos. Trans. R. Soc. B. 353, 199–205 (1998).Article 

    Google Scholar 
    4.Van Oers, K., De Jong, G., Van Noordwijk, A. J., Kempenaers, B. & Drent, P. J. Contribution of genetics to the study of animal personalities: A review of case studies. Behaviour 142, 1185–1206 (2005).Article 

    Google Scholar 
    5.Dochtermann, N. A., Schwab, T. & Sih, A. The contribution of additive genetic variation to personality variation: Heritability of personality. Proc. R. Soc. B. 282, 20142201 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Dochtermann, N. A., Schwab, T., Berdal, M. A., Dalos, J. & Royauté, R. The heritability of behavior: A meta-analysis. J. Hered. 110, 403–410 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Smith, B. R. & Blumstein, D. T. Fitness consequences of personality: A meta-analysis. Behav. Ecol. 19, 448–455 (2008).Article 

    Google Scholar 
    8.Moiron, M., Laskowski, K. L. & Niemelä, P. T. Individual differences in behaviour explain variation in survival: a meta-analysis. Ecol. Lett. 23, 399–408 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Dingemanse, N. J. & Wolf, M. Recent models for adaptive personality differences: A review. Philos. Trans. R. Soc. B. 365, 3947–3958 (2010).Article 

    Google Scholar 
    10.Dingemanse, N. J. & Réale, D. What is the evidence that natural selection maintains variation in animal personalities? In Animal Personalities: Behavior, Physiology, and Evolution (eds Carere, C. & Maestripieri, D.) 201–220 (Chicago University Press, 2013).
    Google Scholar 
    11.Oers, K. V. & Mueller, J. C. Evolutionary genomics of animal personality. Philos. Trans. R. Soc. B. 365, 3991–4000 (2010).Article 

    Google Scholar 
    12.Laine, V. N. & van Oers, K. The quantitative and molecular genetics of individual differences in animal personality. In Personality in Nonhuman Animals (eds Vonk, J. et al.) 55–72 (Springer, 2017).
    Google Scholar 
    13.Bubac, C. M., Miller, J. M. & Coltman, D. W. The genetic basis of animal behavioural diversity in natural populations. Mol. Ecol. 29, 1957–1971 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. Behavioural reaction norms: Animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81–89 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Brommer, J. E. & Class, B. The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Front. Zool. 12, S2 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    16.Nussey, D. H., Wilson, A. J. & Brommer, J. E. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831–844 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).Article 

    Google Scholar 
    18.Gienapp, P., Laine, V. N., Mateman, A. C., van Oers, K. & Visser, M. E. Environment-dependent genotype-phenotype associations in avian breeding time. Front. Genet. 8, 1–9 (2017).Article 
    CAS 

    Google Scholar 
    19.Korsten, P. et al. Association between DRD4 gene polymorphism and personality variation in great tits: A test across four wild populations. Mol. Ecol. 19, 832–843 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Mueller, J. C. et al. Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations. Mol. Ecol. 22, 2797–2809 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Riyahi, S., Sánchez-Delgado, M., Calafell, F., Monk, D. & Senar, J. C. Combined epigenetic and intraspecific variation of the DRD4 and SERT genes influence novelty seeking behavior in great tit Parus major. Epigenetics 10, 516–525 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Mueller, J. C., Partecke, J., Hatchwell, B. J., Gaston, K. J. & Evans, K. L. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Mol. Ecol. 22, 3629–3637 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Holtmann, B. et al. Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis). Mol. Ecol. 25, 706–722 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Class, B. & Brommer, J. E. Senescence of personality in a wild bird. Behav. Ecol. Sociobiol. 70, 733–744 (2016).Article 

    Google Scholar 
    25.Class, B., Brommer, J. E. & van Oers, K. Exploratory behavior undergoes genotype–age interactions in a wild bird. Ecol. Evol. 9, 8987–8994 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Savitz, J. B. & Ramesar, R. S. Genetic variants implicated in personality: A review of the more promising candidates. Am. J. Med. Genet. Neuropsychiatr. Genet. 131B, 20–32 (2004).Article 

    Google Scholar 
    27.Craig, I. W. & Halton, K. E. Genetics of human aggressive behaviour. Hum. Genet. 126, 101–113 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Miller-Butterworth, C. M., Kaplan, J. R., Barmada, M. M., Manuck, S. B. & Ferrell, R. E. The serotonin transporter: Sequence variation in Macaca fascicularis and its relationship to dominance. Behav. Genet. 37, 678–696 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Jannini, E. A., Burri, A., Jern, P. & Novelli, G. Genetics of human sexual behavior: Where we are, where we are going. Sex. Med. Rev. 3, 65–77 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Timm, K., Van Oers, K. & Tilgar, V. SERT gene polymorphisms are associated with risk-taking behaviour and breeding parameters in wild great tits. J. Exp. Biol. 221, jeb171595 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Timm, K., Koosa, K. & Tilgar, V. The serotonin transporter gene could play a role in anti-predator behaviour in a forest passerine. J. Ethol. 37, 221–227 (2019).Article 

    Google Scholar 
    32.Edwards, H. A., Hajduk, G. K., Durieux, G., Burke, T. & Dugdale, H. L. No association between personality and candidate gene polymorphisms in a wild bird population. PLoS ONE 10, 1–13 (2015).
    Google Scholar 
    33.Van Dongen, W. F. D., Robinson, R. W., Weston, M. A., Mulder, R. A. & Guay, P. J. Variation at the DRD4 locus is associated with wariness and local site selection in urban black swans. BMC Evol. Biol. 15, 1–11 (2015).Article 

    Google Scholar 
    34.Sibley, C. G. Behavioral mimicry in the titmice (Paridae) and certain other birds. Wilson Bull. 67, 128–132 (1955).
    Google Scholar 
    35.Thys, B. et al. The female perspective of personality in a wild songbird: Repeatable aggressiveness relates to exploration behaviour. Sci. Rep. 7, 1–10 (2017).CAS 
    Article 

    Google Scholar 
    36.Thys, B., Lambreghts, Y., Pinxten, R. & Eens, M. Nest defence behavioural reaction norms: Testing life-history and parental investment theory predictions. R. Soc. Open Sci. 6, 182180 (2019).PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    37.Thys, B., Pinxten, R. & Eens, M. Long-term repeatability and age-related plasticity of female behaviour in a free-living passerine. Anim. Behav. 172, 45–54 (2021).Article 

    Google Scholar 
    38.Grunst, A. S. et al. Variation in personality traits across a metal pollution gradient in a free-living songbird. Sci. Total Environ. 630, 668–678 (2018).CAS 
    PubMed 
    Article 
    ADS 
    PubMed Central 

    Google Scholar 
    39.Graffelman, J. Exploring diallelic genetic markers: The HardyWeinberg package. J. Stat. Softw. 64, 1–23 (2015).Article 

    Google Scholar 
    40.Solé, X., Guinó, E., Valls, J., Iniesta, R. & Moreno, V. SNPStats: A web tool for the analysis of association studies. Bioinformatics 22, 1928–1929 (2006).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    41.Benjamini, Y. & Hocherg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).MathSciNet 
    MATH 

    Google Scholar 
    42.Therneau, T. coxme: Mixed effects Cox models. R package version 2.2-16. https://CRAN.R-project.org/package=coxme (2020).43.Balding, D. J. A tutorial on statistical methods for population association studies. Nat. Rev. Genet. 7, 781–791 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.van de Pol, M. & Wright, J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77, 753–758 (2009).Article 

    Google Scholar 
    45.Araya-Ajoy, Y. G., Mathot, K. J. & Dingemanse, N. J. An approach to estimate short-term, long-term and reaction norm repeatability. Methods Ecol. Evol. 6, 1462–1473 (2015).Article 

    Google Scholar 
    46.Sinnwell, J., Therneau, T. & Schaid, D. The kinship 2 R Package for Pedigree Data. Hum. Hered. 78, 91–93 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Wilson, A. J. et al. An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13–26 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).Article 

    Google Scholar 
    49.Deans, C. & Maggert, K. A. What do you mean, “Epigenetic”?. Genetics 199, 887–896 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Hirschhorn, J. N., Lohmueller, K., Byrne, E. & Hirschhorn, K. A comprehensive review of genetic association studies. Genet. Med. 4, 45–61 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Hedrick, P. W. Genetic polymorphism in heterogeneous environments: The age of genomics. Annu. Rev. Ecol. Evol. Syst. 37, 67–93 (2006).Article 

    Google Scholar 
    52.Krams, I. et al. Hissing calls improve survival in incubating female great tits (Parus major). Acta Ethol. 17, 83–88 (2014).Article 

    Google Scholar 
    53.Munafò, M. R., Yalcin, B., Willis-Owen, S. A. & Flint, J. Association of the dopamine D4 receptor (DRD4) gene and approach-related personality traits: Meta-analysis and new data. Biol. Psychiatry 63, 197–206 (2008).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    54.Chamary, J. V., Parmley, J. L. & Hurst, L. D. Hearing silence: Non-neutral evolution at synonymous sites in mammals. Nat. Rev. Genet. 7, 98–108 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Sauna, Z. E. & Kimchi-Sarfaty, C. Understanding the contribution of synonymous mutations to human disease. Nat. Rev. Genet. 12, 683–691 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Pastinen, T. Genome-wide allele-specific analysis: Insights into regulatory variation. Nat. Rev. Genet. 11, 533–538 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Vergnes, M., Depaulis, A. & Boehrer, A. Parachlorophenylalanine-induced serotonin depletion increases offensive but not defensive aggression in male rats. Physiol. Behav. 36, 653–658 (1986).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Lesch, K. P. & Merschdorf, U. Impulsivity, aggression, and serotonin: A molecular psychobiological perspective. Behav. Sci. Law 18, 581–604 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Seo, D., Patrick, C. J. & Kennealy, P. J. Role of serotonin and dopamine system interactions in the neurobiology of impulsive aggression and its comorbidity with other clinical disorders. Aggress. Violent Behav. 13, 383–395 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Thys, B., Eens, M., Pinxten, R. & Iserbyt, A. Pathways linking female personality with reproductive success are trait- and year-specific. Behav. Ecol. 32, 114–123 (2020).Article 

    Google Scholar  More

  • in

    Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa

    1.Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Hurricanes and caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86, 174–184 (2005).Article 

    Google Scholar 
    2.Harvell, D. et al. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20, 172–195 (2007).Article 

    Google Scholar 
    3.Silverman, J., Lazar, B., Cao, L., Caldeira, K. & Erez, J. Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys. Res. Lett. 36, 1–5 (2009).Article 

    Google Scholar 
    4.Jackson, J., Donovan, M., Cramer, K. & Lam, W. Status and Trends of Caribbean Coral Reefs 1970–2012 (2012).5.IPCC. Climate Change 2014 Synthesis Report. IPCC Fifth Assessment Report 151 (2014).6.Zaneveld, J. R. et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7, 1–12 (2016).Article 

    Google Scholar 
    7.Bruno, J. F., Petes, L. E., Drew Harvell, C. & Hettinger, A. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 6, 1056–1061 (2003).Article 

    Google Scholar 
    8.Danovaro, R. et al. Sunscreens cause coral bleaching by promoting viral infections. Environ. Health Perspect. 116, 441–447 (2008).CAS 
    Article 

    Google Scholar 
    9.Díaz, M. & Madin, J. Macroecological relationships between coral species’ traits and disease potential. Coral Reefs 30, 73–84 (2011).ADS 
    Article 

    Google Scholar 
    10.Bruno, J. F. The coral disease triangle. Nat. Clim. Chang. 5, 302–303 (2015).ADS 
    Article 

    Google Scholar 
    11.Muller, E. M. et al. Low pH reduces the virulence of black band disease on Orbicella faveolata. PLoS ONE 12, e0178869 (2017).Article 

    Google Scholar 
    12.Thurber, R. V., Payet, J. P., Thurber, A. R. & Correa, A. M. S. Virus-host interactions and their roles in coral reef health and disease. Nat. Rev. Microbiol. 15, 205–216 (2017).CAS 
    Article 

    Google Scholar 
    13.Pollock, F. J., Morris, P. J., Willis, B. L. & Bourne, D. G. The urgent need for robust coral disease diagnostics. PLoS Pathog. 7 (2011).14.Beeden, R., Maynard, J. A., Marshall, P. A., Heron, S. F. & Willis, B. L. A framework for responding to coral disease outbreaks that facilitates adaptive management. Environ. Manag. 49, 1–13 (2012).ADS 
    Article 

    Google Scholar 
    15.Walton, C. J., Hayes, N. K. & Gilliam, D. S. Impacts of a regional, multi-year, multi-species coral disease outbreak in Southeast Florida. Front. Mar. Sci. 5 (2018).16.Harvell, C. D. et al. Emerging marine diseases: Climate links and anthropogenic factors. Manter Lab. 580 (1999).17.Wilkinson, C. Status of Coral Reefs of the World: 2008. (2008).18.Ruiz-Moreno, D. et al. Global coral disease prevalence associated with sea temperature anomalies and local factors. Dis. Aquat. Organ. 100, 249–261 (2012).Article 

    Google Scholar 
    19.Bruckner, A. W. Proceedings of the Caribbean Acropora Workshop: Potential Application of the U.S. Endangered Species Act as a Conservation Strategy. in Proceedings of the Caribbean Acropora Workshop 199 (2003).20.Casas, V. et al. Widespread association of a Rickettsiales-like bacterium with reef-building corals. Environ. Microbiol. 6, 1137–1148 (2004).Article 

    Google Scholar 
    21.Aronson, R. B. & Precht, W. F. White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460, 25–38 (2001).Article 

    Google Scholar 
    22.Gladfelter, W. B. White-band disease in Acropora palmata: Implications for the structure and growth of shallow reefs. Bull. Mar. Sci. 32, 639–643 (1982).
    Google Scholar 
    23.Richardson, L. L. Coral diseases: What is really known?. TREE 13, 438–443 (1998).CAS 
    PubMed 

    Google Scholar 
    24.Richardson, L. L. et al. Florida’s mystery coral-killer identified. Sci. Corresp. 392, 557–558 (1998).CAS 

    Google Scholar 
    25.Richardson, L. & Voss, J. Changes in a coral population on reefs of the northern Florida Keys following a coral disease epizootic. Mar. Ecol. Prog. Ser. 297, 147–156 (2005).ADS 
    Article 

    Google Scholar 
    26.Berkelmans, R., De’ath, G., Kininmonth, S. & Skirving, W. J. A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: Spatial correlation, patterns, and predictions. Coral Reefs 23, 74–83 (2004).Article 

    Google Scholar 
    27.Burge, C. A. et al. Climate change influences on marine infectious diseases: Implications for management and society. Ann. Rev. Mar. Sci. 6, 249–277 (2014).Article 

    Google Scholar 
    28.Maynard, J. et al. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat. Clim. Chang. 5, 688–694 (2015).ADS 
    Article 

    Google Scholar 
    29.Roth, L., Kramer, P. R., Doyle, E. & and O’Sullivan, C. Caribbean SCTLD Dashboard. ArcGIS Online (2020). https://www.agrra.org/coral-disease-outbreak/.30.Alvarez-Filip, L., Estrada-Saldívar, N., Pérez-Cervantes, E., Molina-Hernández, A. & González-Barrios, F. J. A rapid spread of the stony coral tissue loss disease outbreak in the Mexican Caribbean. PeerJ https://doi.org/10.7717/peerj.8069 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front. Mar. Sci. 7, 163 (2020).Article 

    Google Scholar 
    32.Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the florida reef tract. Front. Mar. Sci. 6, 1–18 (2019).ADS 
    Article 

    Google Scholar 
    33.Weil, E. & Rogers, C. S. Coral reef diseases in the Atlantic-Caribbean. In Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) 465–491 (Springer, 2011). https://doi.org/10.1007/978-94-007-0114-4.
    Google Scholar 
    34.Rippe, J. P., Kriefall, N. G., Davies, S. W. & Castillo, K. D. Differential disease incidence and mortality of inner and outer reef corals of the upper Florida Keys in association with a white syndrome outbreak. Bull. Mar. Sci. 95, 305–316 (2019).Article 

    Google Scholar 
    35.Neely, K. Ex-Situ Disease Treatment Trials. 1–3 (2018). https://floridadep.gov/sites/default/files/Ex-Situ-Disease-Treatment-Trials.pdf.36.Neely, K. Ex Situ Disease Treatment Trials Final Report. 1–3 (2019). Available at: https://floridadep.gov/sites/default/files/DEPLabTrialsFINALReport2019.01508comp_0.pdf.37.Miller, C. V., May, L. A., Moffitt, Z. J. & Woodley, C. M. Exploratory Treatments for Stony Coral Tissue Loss Disease: Pillar Coral (Dendrogyra cylindrus). (2020). https://doi.org/10.7289/V5/TM-NOS-NCCOS-24538.Favero, M., Balut, K., Levine, M. & Circle, M. Amoxicillin Trihydrate Stability in Correlation with Coral Ointment Batch #18006-B and Simulated Seawater. 1–9 (2019). https://floridadep.gov/sites/default/files/AmoxicillinStabilityinBothSeawaterBatch18006-B_FINAL_508C_0.pdf.39.Aeby, G. S. et al. First record of black band disease in the Hawaiian archipelago: Response, outbreak status, virulence, and a method of treatment. PLoS ONE 10, 1–17 (2015).Article 

    Google Scholar 
    40.Walker, B. K. & Brunelle, A. Southeast Florida large ( >2 meter) diseased coral colony intervention summary report. 1–164 (2018). https://floridadep.gov/sites/default/files/Large-Coral-Disease-Intervention-Summary-Report.pdf.41.Combs, I. Characterizing the Impacts of Scleractinian Tissue Loss Disease Outbreak on Corals in Southeast Florida. (2019).42.Combs, I. R., Studivan, M. S., Eckert, R. J. & Voss, J. D. Quantifying impacts of stony coral tissue loss disease on corals in Southeast Florida through surveys and 3D photogrammetry. PLoS One (In the press).43.Voss, J. D., Shilling, E. N. & Combs, I. R. Intervention and fate tracking for corals affected by stony coral tissue loss disease in the northern Florida Reef Tract. 1–23 (2019). Available at: https://floridadep.gov/sites/default/files/VossSEFLDiseaseReport2018_FINAL_508compliant.pdf.44.Veron, J. E. N. Corals of the World. (2000).45.NOAA. Stony Coral Tissue Loss Disease Case Definition. Florida Keys National Marine Sanctuary (2018).46.Banks, K. W. et al. The Reef Tract of Continental Southeast Florida (Miami-Dade, Broward and Palm Beach Counties, USA). in Coral Reefs of the USA 175–220 (2008).47.González-Barrios, F. J. & Álvarez-Filip, L. A framework for measuring coral species-specific contribution to reef functioning in the Caribbean. Ecol. Indic. 95, 877–886 (2018).Article 

    Google Scholar 
    48.R Core Team. R: A language and environment for statistical computing. (2020).49.Wickham, H. Package ‘ggplot2’: Create Elegant Data Visualizations Using the Grammar of Graphics. 277 (2020).50.Hope, R. M. Package ‘ Rmisc ’: Ryan Miscellaneous. (2016).51.Kassambara, A. Package ‘ rstatix ’: Pipe-Friendly Framework for Basic Statistical Tests. (2020).52.Derek, O., Wheeler, P. & Dinno, A. Package ‘ FSA ’: Simple Fisheries Stock Assessment Methods. (2020).53.Sweet, M. J., Croquer, A. & Bythell, J. C. Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis. Proc. R. Soc. B Biol. Sci. 281, 20140094–20140094 (2014).CAS 
    Article 

    Google Scholar 
    54.Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by Stony Coral Tissue Loss Disease. PeerJ 8, e9289 (2020).Article 

    Google Scholar 
    55.Voss, J. D., Mills, D. K., Myers, J. L., Remily, E. R. & Richardson, L. L. Black band disease microbial community variation on corals in three regions of the wider Caribbean. Microb. Ecol. 54, 730–739 (2007).CAS 
    Article 

    Google Scholar 
    56.Sekar, R., Kaczmarsky, L. & Richardson, L. Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar. Ecol. Prog. Ser. 362, 85–98 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    57.Sato, Y., Willis, B. L. & Bourne, D. G. Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J. 4, 203–214 (2010).Article 

    Google Scholar 
    58.Miller, A. W. & Richardson, L. L. A meta-analysis of 16S rRNA gene clone libraries from the polymicrobial black band disease of corals. FEMS Microbiol. Ecol. 75, 231–241 (2010).Article 

    Google Scholar 
    59.Hudson, H. First Aid for Massive Corals Infected With Black Band Disease, Phormidium corallyticum: An Underwater Aspirator and Post-Treatment Sealant to Curtail Reinfection. In AAUS 20th Symposium Proceedings 2000 (2000).60.Randall, C. J. et al. Testing methods to mitigate Caribbean yellow-band disease on Orbicella faveolata. PeerJ 2018, 1–20 (2018).
    Google Scholar 
    61.Walker, B. K. & Pitts, K. SE FL Reef-building-coral Response to Amoxicillin Intervention and Broader-scale Coral Disease Intervention. 1–17 (2019). https://floridadep.gov/sites/default/files/WalkerMCAVDiseaseExperimentSummaryReportJune2019_final_14Aug2019.pdf.62.Neely, K. Florida Keys Coral Disease Strike Team: FY 2019/2020 Final Report. 1–17 (2020). Available at: https://floridadep.gov/sites/default/files/FloridaKeysCoralDiseaseStrikeTeam_FY19-20FinalReport.pdf.63.Paterson, I. K., Hoyle, A., Ochoa, G., Baker-Austin, C. & Taylor, N. G. H. Optimising antibiotic usage to treat bacterial infections. Sci. Rep. 6, 1–10 (2016).Article 

    Google Scholar  More

  • in

    Environmental factors shape the epiphytic bacterial communities of Gracilariopsis lemaneiformis

    1.Roth-Schulze, A. J. et al. Functional biogeography and host specificity of bacterial communities associated with the Marine Green Alga Ulva spp. Mol. Ecol. 27, 1952–1965 (2018).PubMed 
    Article 

    Google Scholar 
    2.Teagle, H., Hawkins, S. J., Moore, P. J. & Smale, D. A. The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J. Exp. Mar. Biol. Ecol. 492, 81–98 (2017).Article 

    Google Scholar 
    3.Goecke, F., Labes, A., Wiese, J. & Imhoff, J. F. Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 409, 267–300 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Singh, R. P. & Reddy, C. R. K. Seaweed-microbial interactions: Key functions of seaweed-associated bacteria. FEMS Microbiol. Ecol. 88, 213–230 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Ramanan, R., Kim, B. H., Cho, D. H., Oh, H. M. & Kim, H. S. Algae-bacteria interactions: Evolution, ecology and emerging applications. Biotechnol. Adv. 34, 14–29 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Ismail, A. et al. Antimicrobial activities of bacteria associated with the brown alga padina pavonica. Front. Microbiol. 7, 1–13 (2016).
    Google Scholar 
    7.Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C. & Webb, E. A. The role of B vitamins in marine biogeochemistry. Ann. Rev. Mar. Sci. 6, 339–367 (2014).PubMed 
    Article 

    Google Scholar 
    8.Karthick, P. & Mohanraju, R. Antimicrobial potential of epiphytic bacteria associated with seaweeds of little Andaman, India. Front. Microbiol. 9, 1–11 (2018).Article 

    Google Scholar 
    9.El Shafay, S. M., Ali, S. S. & El-Sheekh, M. M. Antimicrobial activity of some seaweeds species from Red sea, against multidrug resistant bacteria. Egypt. J. Aquat. Res. 42, 65–74 (2016).Article 

    Google Scholar 
    10.Dobretsov, S. V. & Qian, P. Y. Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18, 217–228 (2002).Article 

    Google Scholar 
    11.Mieszkin, S., Callow, M. E. & Callow, J. A. Interactions between microbial biofilms and marine fouling algae: A mini review. Biofouling 29, 1097–1113 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Burke, C., Thomas, T., Lewis, M., Steinberg, P. & Kjelleberg, S. Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J. 5, 590–600 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    13.Tujula, N. A. et al. Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J. 4, 301–311 (2010).PubMed 
    Article 

    Google Scholar 
    14.Burke, C., Steinberg, P., Rusch, D., Kjelleberg, S. & Thomas, T. Bacterial community assembly based on functional genes rather than species. Proc. Natl. Acad. Sci. 108, 14288–14293 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Roth-Schulze, A. J., Zozaya-Valdés, E., Steinberg, P. D. & Thomas, T. Partitioning of functional and taxonomic diversity in surface-associated microbial communities. Environ. Microbiol. 18, 4391–4402 (2016).PubMed 
    Article 

    Google Scholar 
    16.Selvarajan, R. et al. Distribution, interaction and functional profiles of epiphytic bacterial communities from the rocky intertidal seaweeds, South Africa. Sci. Rep. 9, 1–13 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    17.Aires, T., Serrão, E. A. & Engelen, A. H. Host and environmental specificity in bacterial communities associated to two highly invasive marine species (genus Asparagopsis). Front. Microbiol. 7, 1–14 (2016).Article 

    Google Scholar 
    18.Lachnit, T., Fischer, M., Künzel, S., Baines, J. F. & Harder, T. Compounds associated with algal surfaces mediate epiphytic colonization of the marine macroalga Fucus vesiculosus. FEMS Microbiol. Ecol. 84, 411–420 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Nylund, G. M. et al. The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol. Ecol. 71, 84–93 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    20.Campbell, A. H., Marzinelli, E. M., Gelber, J. & Steinberg, P. D. Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front. Microbiol. 6, 1–10 (2015).Article 

    Google Scholar 
    21.Munday, P. L. Competitive coexistence of coral-dwelling fishes: The lottery hypothesis revisited. Ecology 85, 623–628 (2004).Article 

    Google Scholar 
    22.Geange, S. W., Poulos, D. E., Stier, A. C. & McCormick, M. I. The relative influence of abundance and priority effects on colonization success in a coral-reef fish. Coral Reefs 36, 151–155 (2017).ADS 
    Article 

    Google Scholar 
    23.Stratil, S. B., Neulinger, S. C., Knecht, H., Friedrichs, A. K. & Wahl, M. Temperature-driven shifts in the epibiotic bacterial community composition of the brown macroalga Fucus vesiculosus. Microbiologyopen 2, 338–349 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Stratil, S. B., Neulinger, S. C., Knecht, H., Friedrichs, A. K. & Wahl, M. Salinity affects compositional traits of epibacterial communities on the brown macroalga Fucus vesiculosus. FEMS Microbiol. Ecol. 88, 272–279 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Zhang, Y. et al. Effect of salinity on the microbial community and performance on anaerobic digestion of marine macroalgae. J. Chem. Technol. Biotechnol. 92, 2392–2399 (2017).CAS 
    Article 

    Google Scholar 
    26.Liao, L. & Xu, Y. Effects of nitrogen nutrients on growth and epiphytic bacterial composition in sea weed Gracilaria lemaneiformis. Fish. Sci. 28, 130–135 (2009).ADS 
    CAS 

    Google Scholar 
    27.Zozaya-Valdés, E., Roth-Schulze, A. J. & Thomas, T. Effects of temperature stress and aquarium conditions on the red macroalga Delisea pulchra and its associated microbial community. Front. Microbiol. 7, 1–10 (2016).Article 

    Google Scholar 
    28.Nemergut, D. R. et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342–356 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Liu, X. et al. Isolation and pathogenicity identification of bacterial pathogens in bleached disease and their physiological effects on the red macroalga Gracilaria lemaneiformis. Aquat. Bot. 153, 1–7 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    30.Xie, X. et al. Large-scale seaweed cultivation diverges water and sediment microbial communities in the coast of Nan’ao Island, South China Sea. Sci. Total Environ. 598, 97–108 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Yang, Y. et al. Cultivation of seaweed Gracilaria in Chinese coastal waters and its contribution to environmental improvements. Algal Res. 9, 236–244 (2015).Article 

    Google Scholar 
    32.Lindström, E. S. & Langenheder, S. Local and regional factors influencing bacterial community assembly. Environ. Microbiol. Rep. 4, 1–9 (2012).PubMed 
    Article 

    Google Scholar 
    33.Hellweger, F. L., Van Sebille, E. & Fredrick, N. D. Biogeographic patterns in ocean microbes emerge in a neutral agent-based model. Science (80-. ). 345, 1346–1349 (2014).34.Longford, S. R. et al. Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat. Microb. Ecol. 48, 217–229 (2007).Article 

    Google Scholar 
    35.Lachnit, T., Meske, D., Wahl, M., Harder, T. & Schmitz, R. Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ. Microbiol. 13, 655–665 (2010).PubMed 
    Article 

    Google Scholar 
    36.Pei, P. et al. Effects of biological water purification grid on microbial community of culture environment and intestine of the shrimp Litopenaeus vannamei. Aquac. Res. 50, 1300–1312 (2019).CAS 
    Article 

    Google Scholar 
    37.Shade, A. & Handelsman, J. Beyond the Venn diagram: The hunt for a core microbiome. Environ. Microbiol. 14, 4–12 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Spoerner, M., Wichard, T., Bachhuber, T., Stratmann, J. & Oertel, W. Growth and thallus morphogenesis of Ulva mutabilis (chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J. Phycol. 48, 1433–1447 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Kessler, R. W., Weiss, A., Kuegler, S., Hermes, C. & Wichard, T. Macroalgal–bacterial interactions: Role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta). Mol. Ecol. 27, 1808–1819 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Malmstrom, R. R., Kiene, R. P. & Kirchman, D. L. Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico. Limnol. Oceanogr. 49, 597–606 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Holmström, C., Egan, S., Franks, A., McCloy, S. & Kjelleberg, S. Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol. Ecol. 41, 47–58 (2002).PubMed 
    Article 

    Google Scholar 
    42.Holmström, C. & Kjelleberg, S. The effect of external biological factors on settlement of marine invertebrate and new antifouling technology. Biofouling 8, 147–160 (1994).Article 

    Google Scholar 
    43.Lachnit, T., Blümel, M., Imhoff, J. F. & Wahl, M. Specific epibacterial communities on macroalgae : Phylogeny matters more than habitat. Aquat. Biol. 5, 181–186 (2009).Article 

    Google Scholar 
    44.Fan, X. et al. The effect of nutrient concentrations, nutrient ratios and temperature on photosynthesis and nutrient uptake by Ulva prolifera : Implications for the explosion in green tides. J. Appl. Phycol. 26, 537–544 (2014).CAS 
    Article 

    Google Scholar 
    45.Van Alstyne, K. L. Seawater nitrogen concentration and light independently alter performance, growth, and resource allocation in the bloom-forming seaweeds Ulva lactuca and Ulvaria obscura ( Chlorophyta ). Harmful Algae 78, 27–35 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    46.Lachnit, T., Wahl, M. & Harder, T. Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26, 247–255 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Su, H. et al. Persistence and spatial variation of antibiotic resistance genes and bacterial populations change in reared shrimp in South China. Environ. Int. 119, 327–333 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Ekwanzala, M. D., Dewar, J. B. & Momba, M. N. B. Environmental resistome risks of wastewaters and aquatic environments deciphered by shotgun metagenomic assembly. Ecotoxicol. Environ. Saf. 197, 110612 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    49.Numberger, D. et al. Characterization of bacterial communities in wastewater with enhanced taxonomic resolution by full-length 16S rRNA sequencing. Sci. Rep. 9, 1–14 (2019).CAS 
    Article 

    Google Scholar 
    50.Teklehaimanot, G. Z., Genthe, B., Kamika, I. & Momba, M. N. B. Prevalence of enteropathogenic bacteria in treated effluents and receiving water bodies and their potential health risks. Sci. Total Environ. 518–519, 441–449 (2015).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    51.Kelley, S. E. Experimental studies of the evolutionary significance of sexual reproduction. V. A field test of the sib-competition hypotheses. Evolution (N. Y). 43, 1066 (1989).52.Browne, L. & Karubian, J. Rare genotype advantage promotes survival and genetic diversity of a tropical palm. New Phytol. 218, 1658–1667 (2018).PubMed 
    Article 

    Google Scholar 
    53.Gressler, V. et al. Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chem. 120, 585–590 (2010).CAS 
    Article 

    Google Scholar 
    54.Gu, D. et al. Purification of R-phycoerythrin from Gracilaria lemaneiformis by centrifugal precipitation chromatography. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 1087–1088, 138–141 (2018).55.Su, Y. bin et al. Pyruvate cycle increases aminoglycoside efficacy and provides respiratory energy in bacteria. Proc. Natl. Acad. Sci. U. S. A. 115, E1578–E1587 (2018).56.Hollants, J., Leliaert, F., De Clerck, O. & Willems, A. What we can learn from sushi: A review on seaweed-bacterial associations. FEMS Microbiol. Ecol. 83, 1–16 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    57.AQSIQ. Specifications for Oceanographic Survey. Part 4: Survey of Chemical Parameters in Sea Water. 16–26 (Standards Press of China, 2007).58.Burke, C., Kjelleberg, S. & Thomas, T. Selective extraction of bacterial DNA from the surfaces of macroalgae. Appl. Environ. Microbiol. 75, 252–256 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Xu, Y., Le, G. & Zhang, Y. Comparison with several methods to isolate epiphytic bacteria from Gracilaria lemaneiformis (Rhodophyta). Microbiol. China 34, 123–126 (2007).
    Google Scholar 
    60.Pei, P. et al. Analysis of the bacterial community composition of the epiphytes on diseased Gracilaria lemaneiformis using PCR-DGGE fingerprinting technology. J. Fish. Sci. China 25 (2018).61.Takahashi, S., Tomita, J., Nishioka, K., Hisada, T. & Nishijima, M. Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9 (2014).62.Bokulich, N. A. et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Liu, T. et al. Joining Illumina paired-end reads for classifying phylogenetic marker sequences. BMC Bioinform. 21, 1–13 (2020).Article 

    Google Scholar 
    64.Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Edgar, R. C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    66.Cole, J. R. et al. Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, 633–642 (2014).Article 
    CAS 

    Google Scholar 
    67.Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).Article 
    CAS 

    Google Scholar 
    68.Wang, Y. et al. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl. Environ. Microbiol. 78, 8264–8271 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Somerfield, P. J. Identification of the Bray-Curtis similarity index: Comment on Yoshioka (2008). Mar. Ecol. Prog. Ser. 372, 303–306 (2008).ADS 
    Article 

    Google Scholar 
    70.Higgins, M. A., Robbins, G. A., Maas, K. R. & Binkhorst, G. K. Use of bacteria community analysis to distinguish groundwater recharge sources to shallow wells. J. Environ. Qual. 49, 1530–1540 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Yang, J., Ma, L., Jiang, H., Wu, G. & Dong, H. Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan Lakes. Sci. Rep. 6, 6–11 (2016).ADS 
    Article 
    CAS 

    Google Scholar 
    72.Langille, M. G. I. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More