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    Long-term enclosure at heavy grazing grassland affects soil nitrification via ammonia-oxidizing bacteria in Inner Mongolia

    Pan, H. et al. Archaea and bacteria respectively dominate nitrification in lightly and heavily grazed soil in a grassland system. Biol. Fert. Soils. 54(1), 41–54 (2018).Article 

    Google Scholar 
    Pan, H. et al. Understanding the relationships between grazing intensity and the distribution of nitrifying communities in grassland soils. Sci. Total Environ. 634, 1157–1164 (2018).Article 
    ADS 

    Google Scholar 
    Dong, L., Li, J. J., Sun, J. & Yang, C. Soil degradation influences soil bacterial and fungal community diversity in overgrazed alpine meadows of the Qinghai-Tibet plateau. Sci. Rep. 11, 11538 (2021).Article 
    ADS 

    Google Scholar 
    Oduor, C. O. et al. Enhancing soil organic carbon, particulate organic carbon and microbial biomass in semi-arid rangeland using pasture enclosures. BMC Ecol. 18, 45 (2018).Article 

    Google Scholar 
    Wang, S. Z., Fan, J. W., Li, Y. Z. & Huang, L. Effects of grazing exclusion on biomass growth and species diversity among various grassland types of the Tibetan Plateau. Sustainability 11(6), 1705 (2019).Article 

    Google Scholar 
    Simpson, A. C., Zabowski, D., Rochefort, R. M. & Edmonds, R. L. Increased microbial uptake and plant nitrogen availability in response to simulated nitrogen deposition in alpine meadows. Geoderma 336, 68–80 (2019).Article 
    ADS 

    Google Scholar 
    Qasim, S. et al. Influence of grazing enclosure on vegetation biomass and soil quality. Int. Soil Water Conserv. 5(1), 62–68 (2017).Article 

    Google Scholar 
    Hirobe, M. et al. Effects of livestock grazing on the spatial heterogeneity of net soil nitrogen mineralization in three types of Mongolian grasslands. J. Soils Sediment. 13, 1123–1132 (2013).Article 

    Google Scholar 
    Luo, Y. K., Wang, C. H., Shen, Y., Sun, W. & Dong, K. H. The interactive effects of mowing and N addition did not weaken soil net N mineralization rates in semiarid grassland of Northern China. Sci. Rep. 9, 13457 (2019).Article 
    ADS 

    Google Scholar 
    Wu, H. et al. Feedback of grazing on gross rates of N mineralization and inorganic N partitioning in steppe soils of Inner Mongolia. Plant Soil. 340(1–2), 127–139 (2011).Article 

    Google Scholar 
    Xu, Y. Q., Li, L. H., Wang, Q. B., Chen, Q. S. & Cheng, W. X. The patterns between nitrogen mineralization and grazing intensities in an Inner Mongolian typical steppe. Plant Soil. 300, 289–300 (2007).Article 

    Google Scholar 
    Wang, X. et al. Grazing improves C and N cycling in the Northern Great Plains: A meta-analysis. Sci. Rep. 6, 33190 (2016).Article 
    ADS 

    Google Scholar 
    Pang, R., Sun, Y., Xu, X. L., Song, M. H. & Ouyang, H. Effects of clipping and shading on 15NO3− and 15NH4+ recovery by plants in grazed and ungrazed temperate grasslands. Plant Soil. 433(1–2), 339–352 (2018).Article 

    Google Scholar 
    Sun, Y., Schleuss, P. M., Pausch, J., Xu, X. L. & Kuzyakov, Y. Nitrogen pools and cycles in Tibetan Kobresia pastures depending on grazing. Biol. Fert. Soils. 54(5), 569–581 (2018).Article 

    Google Scholar 
    Andrioli, R. J., Distel, R. A. & Didone, N. G. Influence of cattle grazing on nitrogen cycling in soils beneath Stipa tenuis, native to central Argentina. J. Arid. Environ. 74(3), 419–422 (2010).Article 
    ADS 

    Google Scholar 
    Norman, J. S., Lin, L. & Barrett, J. E. Paired carbon and nitrogen metabolism by ammonia-oxidizing bacteria and archaea in temperate forest soils. Ecosphere 6(10), 1–11 (2016).
    Google Scholar 
    Mukhtar, H., Lin, Y. P., Lin, C. M. & Petway, J. R. Assessing thermodynamic parameter sensitivity for simulating temperature responses of soil nitrification. Environ. Sci.-Proc. Imp. 21(9), 1596–1608 (2019).
    Google Scholar 
    Rütting, T., Schleusner, P., Hink, L. & Prosser, J. I. The contribution of ammonia-oxidizing archaea and bacteria to gross nitrification under different substrate availability. Soil Biol. Biochem 160, 108353 (2021).Article 

    Google Scholar 
    Pan, H. et al. Management practices have a major impact on nitrifier and denitrifier communities in a semiarid grassland ecosystem. J. Soils Sediment. 16, 896–908 (2016).Article 

    Google Scholar 
    Szukics, U. et al. Management versus site effects on the abundance of nitrifiers and denitrifiers in European mountain grasslands. Sci. Total Environ. 648, 745–753 (2019).Article 
    ADS 

    Google Scholar 
    Chen, Q., Hooper, D. U. & Lin, S. Shifts in species composition constrain restoration of overgrazed grassland using nitrogen fertilization in Inner Mongolian steppe, China. PLoS ONE 6(3), e16909 (2011).Article 
    ADS 

    Google Scholar 
    Raison, R. J., Connell, M. J. & Khanna, P. K. Methodology for studying fluxes of soil mineral-N in situ. Soil Biol. Biochem. 19, 521–530 (1987).Article 

    Google Scholar 
    Kurola, J., Salkinoja-Salonen, M., Aarnio, T., Hultman, J. & Romantschuk, M. Activity, diversity and population size of ammonia-oxidizing bacteria in oil-contaminated land farming soil. FEMS Microbiol. Lett. 250, 33–38 (2005).Article 

    Google Scholar 
    Tran, H. T. et al. Bacterial community progression during food waste composting containing high dioctyl terephthalate (DOTP) concentration. Chemosphere 265, 129064 (2021).Article 
    ADS 

    Google Scholar 
    Hook, P. B. & Burke, I. C. Evaluation of a method for estimating net nitrogen mineralization in a semiarid grassland. Soil Sci. Soc. Am. J. 59, 831–837 (1995).Article 
    ADS 

    Google Scholar 
    Liu, T. Z., Nan, Z. B. & Hou, F. J. Grazing intensity effects on soil nitrogen mineralization in semi-arid grassland on the Loess Plateau of northern China. Nutr. Cyc. Agroecosyst. 91(1), 67–75 (2011).Article 

    Google Scholar 
    Li, J. P., Ma, H. B., Xie, Y. Z., Wang, K. B. & Qiu, K. Y. Deep soil C and N pools in long-term fenced and overgrazed temperate grasslands in northwest China. Sci. Rep. 9, 16088 (2019).Article 
    ADS 

    Google Scholar 
    Di, H. J. et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2(9), 621–624 (2009).Article 
    ADS 

    Google Scholar 
    Li, J. P., Zheng, Z. R., Xie, H. T., Zhao, N. X. & Gao, Y. B. Increased soil nutrition and decreased light intensity drive species loss after eight years grassland enclosures. Sci. Rep. 7, 44525 (2017).Article 
    ADS 

    Google Scholar 
    Luo, C. Y. et al. Effect of warming and grazing on litter mass loss and temperature sensitivity of litter and dung mass loss on the Tibetan plateau. Glob. Change Biol. 16, 1606–1617 (2010).Article 
    ADS 

    Google Scholar 
    Shahzad, T. et al. Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol. Biochem. 80, 146–155 (2015).Article 

    Google Scholar 
    Xie, Z. et al. Identifying response groups of soil nitrifiers and denitrifiers to grazing and associated soil environmental drivers in Tibetan alpine meadows. Soil Biol. Biochem. 77, 89–99 (2014).Article 

    Google Scholar 
    Clark, I. M., Hughes, D. J., Fu, Q. L., Abadie, M. & Hirsch, P. R. Metagenomic approaches reveal differences in genetic diversity and relative abundance of nitrifying bacteria and archaea in contrasting soils. Sci. Rep. 11, 15905 (2021).Article 
    ADS 

    Google Scholar 
    He, J. Z. et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364–2374 (2007).Article 

    Google Scholar 
    Meyer, A. et al. Influence of land use intensity on the diversity of ammonia oxidizing bacteria and archaea in soils from grassland ecosystems. Microb. Ecol. 67(1), 161–166 (2014).Article 

    Google Scholar 
    Zhu, X. X. et al. Effects of warming, grazing/cutting and nitrogen fertilization on greenhouse gas fluxes during growing seasons in an alpine meadow on the Tibetan Plateau. J. Agric. Meteorol. 214–215, 506–514 (2015).Article 

    Google Scholar 
    Jia, Z. J. & Cornrad, R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11(7), 1658–1671 (2009).Article 

    Google Scholar 
    Verhamme, D. T., Prosser, J. I. & Nicol, G. W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071 (2011).Article 

    Google Scholar 
    Zhou, X. H. et al. Diversity, abundance and community structure of ammonia-oxidizing archaea and bacteria in riparian sediment of Zhenjiang ancient canal. Ecol. Eng. 90, 447–458 (2016).Article 

    Google Scholar 
    Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976–979 (2009).Article 
    ADS 

    Google Scholar 
    Clark, D. R. et al. Mineralization and nitrification: Archaea dominate ammonia-oxidising communities in grassland soils. Soil Biol. Biochem. 143, 107725 (2020).Article 

    Google Scholar 
    Long, X. N., Chen, C. R., Xu, Z. H., Linder, S. & He, J. Z. Abundance and community structure of ammonia oxidizing bacteria and archaea in a Sweden boreal forest soil under 19-year fertilization and 12-year warming. J. Soils Sediment. 12, 1124–1133 (2012).Article 

    Google Scholar 
    Wessén, E. & Hallin, S. Abundance of archaeal and bacterial ammonia oxidizers-possible bioindicator for soil monitoring. Ecol. Indic. 11, 1696–1698 (2011).Article 

    Google Scholar 
    Yang, Y. et al. Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob. Change Biol. 19(2), 637–648 (2013).Article 
    ADS 

    Google Scholar 
    Zhang, C. J. et al. Impacts of long-term nitrogen addition, watering and mowing on ammonia oxidizers, denitrifiers and plant communities in a temperate steppe. Appl. Soil Ecol. 130, 241–250 (2018).Article 

    Google Scholar 
    Alves, R. J. E., Minh, B. Q., Urich, T., Haeseler, A. V. & Schleper, C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat. Commun. 9, 1517 (2018).Article 
    ADS 

    Google Scholar 
    DeLong, E. F. Everything in moderation archaea as ‘non extremophiles’. Curr. Opin. Genet. Dev. 8(6), 649–654 (1998).Article 

    Google Scholar 
    Jia, Z. J. et al. Evidence for niche differentiation of nitrifying communities in grassland soils after 44 years of different field fertilization scenarios. Pedoshpere 30(1), 87–97 (2019).
    Google Scholar 
    Wang, X. L. et al. Long-term fertilization effects on active ammonia oxidizers in an acidic upland soil in China. Soil Biol. Biochem. 84, 28–37 (2015).Article 

    Google Scholar 
    Li, Y. Y., Chapman, S. J., Nicol, G. W. & Yao, H. Y. Nitrification and nitrifiers in acidic soils. Soil Biol. Biochem. 116, 290–301 (2018).Article 

    Google Scholar 
    Olivera, N. L., Prieto, L., Bertiller, M. B. & Ferrero, M. A. Sheep grazing and soil bacterial diversity in shrub lands of the Patagonian Monte, Argentina. J. Arid. Environ. 125, 16–20 (2016).Article 
    ADS 

    Google Scholar  More

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    Long-term maintenance of a heterologous symbiont association in Acropora palmata on natural reefs

    Hoegh-Guldberg O, Smith JG. The effect of sudden changes in temperature, light, and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata (Esper) and Seriatopora hysterix (Dana). J Exp Mar Biol Ecol. 1989;129:279–303.Article 

    Google Scholar 
    Glynn PW. Coral reef bleaching: ecological perspectives. Coral Reefs. 1993;12:1–17.Article 

    Google Scholar 
    Berkelmans R, van Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B: Biol Sci. 2006;273:2305–12.Article 

    Google Scholar 
    Cunning R, Gillette P, Capo T, Galvez K, Baker AC. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs. 2015;34:155–60.Article 

    Google Scholar 
    Scharfenstein HJ, Chan WY, Buerger P, Humphrey C, van Oppen MJH. Evidence for de novo acquisition of microalgal symbionts by bleached adult corals. ISME J. 2022;16:1676–9.Article 

    Google Scholar 
    Goulet TL. Most corals may not change their symbionts. Mar Ecol Prog Ser. 2006;321:1–7.Article 

    Google Scholar 
    Jones A, Berkelmans R. Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE. 2010;5:e10437.Article 

    Google Scholar 
    van Oppen MJH, Oliver JK, Putnam HM, Gates RD. Building coral reef resilience through assisted evolution. Proc R Soc B: Biol Sci. 2015;112:2307–13.
    Google Scholar 
    Buerger P, Alvarez C, Coppin CW, Pearce SL, Chakravarti LJ, Oakeshott JG, et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci Adv. 2020;6:eaba2498.Kuffner IB, Toth LT. A geological perspective on the degradation and conservation of western Atlantic coral reefs. Conserv Biol: J Soc Conserv Biol. 2016;30:706–15.Article 

    Google Scholar 
    Young CN, Schopmeyer SA, Lirman D. A review of reef restoration and Coral propagation using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Mar Sci. 2012;88:1075–98.Article 

    Google Scholar 
    Reich HG, Kitchen SA, Stankiewicz KH, Devlin-Durante M, Fogarty ND, Baums IB. Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium fitti) among closely related coral hosts. Mol Ecol. 2021;30:3500–14.Article 

    Google Scholar 
    Baums IB, Devlin-Durante MK, Lajeunesse TC. New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol. 2014;23:4203–15.Article 

    Google Scholar 
    Gantt SE, Keister E, Manfroy A, Merck D, Fitt W, Muller E, et al. Wild and nursery-raised corals: comparative physiology of two framework coral species. Coral Reefs. (In Press).Hume BCC, Smith EG, Ziegler M, Hugh J, Warrington M, Burt J, et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour. 2019;19:1063–80.Article 

    Google Scholar 
    Randall CJ, Negri AP, Quigley KM, Foster T, Ricardo GF, Webster NS, et al. Sexual production of corals for reef restoration in the Anthropocene. Mar Ecol Prog Ser. 2020;635:203–32.Article 

    Google Scholar 
    Bay LK, Cumbo VR, Abrego D, Kool JT, Ainsworth TD, Willis BL. Infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae. Diversity. 2011;3:356–74.Article 

    Google Scholar 
    Abrego D, van Oppen MJH, Willis BL. Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol. 2009;18:3518–31.Article 

    Google Scholar 
    Cunning R, Silverstein RN, Baker AC. Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B: Biol Sci. 2015;282:20141725.Chamberland VF, Petersen D, Latijnhouwers KRW, Snowden S, Mueller B, Vermeij MJA. Four-year-old Caribbean Acropora colonies reared from field-collected gametes are sexually mature. Bull Mar Sci. 2016;92:263–4.Silverstein RN, Correa AMS, Baker AC. Specificity is rarely absolute in coral–algal symbiosis: implications for coral response to climate change. Proc R Soc B: Biol Sci. 2012;279:2609–18.Article 

    Google Scholar  More

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    Re-examining extreme carbon isotope fractionation in the coccolithophore Ochrosphaera neapolitana

    Laboratory cultureOchrosphaera neapolitana (RCC1357) was precultured in K/2 medium without Tris buffer8 using artificial seawater (ASW) supplemented with NaHCO3 and HCl to yield an initial DIC of 2050 µM. In triplicate, 1-L bottles were filled with 150 mL of seawater medium with air in the bottle headspace and inoculated with a mid-log phase preculture at an initial cell concentration of 104 cells mL−1. Cultures were grown at 18 °C under a warm white LED light at 100 ± 20 µE on a 16h-light/8h-dark cycle. Bottles were orbitally shaken at 60 rpm to keep cells in suspension. Cell growth was monitored with a Multisizer 4e particle counter and sizer (Beckman Coulter). At ~1.4 × 105 cells mL−1, cells were diluted up to 300 mL to 2–3 × 104 cells mL−1 and harvested after 2 days of more exponential growth up to 7.9 ± 0.6 × 104 cells mL−1. More detailed culture results are listed in the Supplementary Note 1.Immediately after harvesting, pH was measured using a pH probe calibrated with Mettler Toledo NBS standards (it should be noted here that high ionic strength calibration standards would be optimal for pH measurement of liquids like seawater). There was a carbonate system shift during the batch culture and more details are shown in Supplementary Fig. S1. Cells in 50 mL were pelleted by centrifuging at ~1650 × g for 5 min. Seawater supernatant was analyzed for DIC and δ13CDIC by injecting 3.5 mL into an Apollo analyzer and injecting 1 mL into He-flushed glass vials containing H3PO4 for the Gas Bench.For seawater DIC, an Apollo SciTech DIC-C13 Analyzer coupled to a Picarro CO2 analyzer was calibrated with in-house NaHCO3 standards dissolved in deionized water at different known concentrations and δ13C values from −4.66 to −7.94‰. δ13CDIC in media were measured with a Gas Bench II with an autosampler (CTC Analytics AG, Switzerland) coupled to ConFlow IV Interface and a Delta V Plus mass spectrometer (Thermo Fischer Scientific). Pelleted cells were snap-frozen with N2 (l) and stored at −80 °C. For PIC analysis, pellet was resuspended in 1 mL methanol and vortexed. After centrifugation, the methanol phase with extracted organics was removed and the pellet containing the coccoliths was dried at 60 °C overnight. About 300 mg of dried coccolith powder were placed in air-tight glass vials, flushed with He and reacted with five drops of phosphoric acid at 70 °C. PIC δ13C and δ18O were measured by the same Gas Bench system. The system and abovementioned in-house standards were calibrated using international standards NBS 18 (δ13C = −5.01‰, δ18O = +23.00‰) and NBS 19 (δ13C = +1.95‰, δ18O = +2.2‰). The analytical error for DIC concentration and δ13C is More

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    Assessing the drivers of gut microbiome composition in wild redfronted lemurs via longitudinal metacommunity analysis

    Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: An integrative view. Cell 148, 1258–1270 (2012).Article 

    Google Scholar 
    Cryan, J. F. et al. The microbiota-gut-brain axis. Physiol. Rev. 99, 1877–2013 (2019).Article 

    Google Scholar 
    Parfrey, L. W., Walters, W. A. & Knight, R. Microbial eukaryotes in the human microbiome: Ecology, evolution, and future directions. Front. Microbiol. 2, 1–6 (2011).Article 

    Google Scholar 
    Caporaso, J. G. et al. Moving pictures of the human microbiome. Genome Biol. 12, R50 (2011).Article 

    Google Scholar 
    Björk, J. R., Dasari, M., Grieneisen, L. & Archie, E. A. Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research. Am. J. Primatol. 81, 1–23 (2019).Article 

    Google Scholar 
    Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012).Article 
    ADS 

    Google Scholar 
    Miller, E. T., Svanbäck, R. & Bohannan, B. J. M. Microbiomes as metacommunities: Understanding host-associated microbes through metacommunity ecology. Trends Ecol. Evol. 33, 926–935 (2018).Article 

    Google Scholar 
    McKenney, E. A., Koelle, K., Dunn, R. R. & Yoder, A. D. The ecosystem services of animal microbiomes. Mol. Ecol. 27, 2164–2172 (2018).Article 

    Google Scholar 
    Koskella, B., Hall, L. J. & Metcalf, C. J. E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat. Ecol. Evol. 1, 1606–1615 (2017).Article 

    Google Scholar 
    Sarkar, A. et al. Microbial transmission in animal social networks and the social microbiome. Nat. Ecol. Evol. 4, 1020–1035 (2020).Article 

    Google Scholar 
    Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).Article 
    ADS 

    Google Scholar 
    Degnan, P. H. et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc. Natl. Acad. Sci. 109, 13034–13039 (2012).Article 
    ADS 

    Google Scholar 
    Bennett, G. et al. Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta). Am. J. Primatol. 78, 883–892 (2016).Article 

    Google Scholar 
    Amato, K. R. et al. Patterns in gut microbiota similarity associated with degree of sociality among sex classes of a neotropical primate. Microb. Ecol. 74, 250–258 (2017).Article 

    Google Scholar 
    Raulo, A. et al. Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality. J. Anim. Ecol. 87, 388–399 (2017).Article 

    Google Scholar 
    Springer, A. et al. Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux’s sifakas (Propithecus verreauxi). Ecol. Evol. 7, 5732–5745 (2017).Article 

    Google Scholar 
    Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. Elife 2015, 1–18 (2015).
    Google Scholar 
    Moeller, A. H. et al. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2, e1500997 (2016).Article 
    ADS 

    Google Scholar 
    Perofsky, A. C., Lewis, R. J., Abondano, L. A., Di Fiore, A. & Meyers, L. A. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. Proc. R. Soc. B Biol. Sci. 284, 20172274 (2017).Article 

    Google Scholar 
    Raulo, A. et al. Social networks strongly predict the gut microbiota of wild mice. ISME J. 15, 2601–2613 (2021).Article 

    Google Scholar 
    Arrieta, M. C., Stiemsma, L. T., Amenyogbe, N., Brown, E. & Finlay, B. The intestinal microbiome in early life: Health and disease. Front. Immunol. 5, 1–18 (2014).Article 

    Google Scholar 
    Ren, T., Grieneisen, L. E., Alberts, S. C., Archie, E. A. & Wu, M. Development, diet and dynamism: Longitudinal and cross-sectional predictors of gut microbial communities in wild baboons. Environ. Microbiol. 18, 1312–1325 (2016).Article 

    Google Scholar 
    Jagsi, R. et al. Seasonal cycling in the gut microbiome of the Hadza Hunter-Gatherers of Tanzania. Science 357, 802–806 (2017).Article 

    Google Scholar 
    Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1786 (2018).Article 
    ADS 

    Google Scholar 
    Murillo, T., Schneider, D., Fichtel, C. & Daniel, R. Dietary shifts and social interactions drive temporal fluctuations of the gut microbiome from wild redfronted lemurs. ISME Commun. 2, 3 (2022).Article 

    Google Scholar 
    Laforest-Lapointe, I. & Arrieta, M.-C. Microbial eukaryotes: A missing link in gut microbiome studies. mSystems 3, e00201-17 (2018).Article 

    Google Scholar 
    Mann, A. E. et al. Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 14, 609–622 (2020).Article 

    Google Scholar 
    Vlčková, K. et al. Relationships between gastrointestinal parasite infections and the fecal microbiome in free-ranging western lowland gorillas. Front. Microbiol. 9, 1–12 (2018).Article 

    Google Scholar 
    Renelies-Hamilton, J. et al. Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal. Infect. Genet. Evol. 74, 104010 (2019).Article 

    Google Scholar 
    Martínez-Mota, R., Righini, N., Mallott, E. K., Gillespie, T. R. & Amato, K. R. The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra). Am. J. Primatol. 83, e23330 (2021).Article 

    Google Scholar 
    Pereira, M. E., Kaufman, R., Kappeler, P. M. & Overdoff, D. J. Female dominance does not characterize all of the lemuridae. Folia Primatol. 55, 96–103 (1990).Article 

    Google Scholar 
    Ostner, J. & Kappeler, P. M. Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?. Anim. Behav. 58, 1069–1078 (1999).Article 

    Google Scholar 
    Kappeler, P. M. & Fichtel, C. A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest. In Long-Term Field Studies of Primates 101–121 (Springer, 2012).Chapter 

    Google Scholar 
    Koch, F., Ganzhorn, J. U., Rothman, J. M., Chapman, C. A. & Fichtel, C. Sex and seasonal differences in diet and nutrient intake in Verreaux’s sifakas (Propithecus verreauxi). Am. J. Primatol. 79, 1–10 (2017).Article 

    Google Scholar 
    Scholz, F. & Kappeler, P. M. Effects of seasonal water scarcity on the ranging behavior of Eulemur fulvus rufus. Int. J. Primatol. 25, 599–613 (2004).Article 

    Google Scholar 
    Amoroso, C. R., Kappeler, P. M., Fichtel, C. & Nunn, C. L. Water availability impacts habitat use by red-fronted lemurs (Eulemur rufifrons): An experimental and observational study. Int. J. Primatol. 41, 61–80 (2020).Article 

    Google Scholar 
    Clough, D., Heistermann, M. & Kappeler, P. M. Host intrinsic determinants and potential consequences of parasite infection in free-ranging red-fronted lemurs (Eulemur fulvus rufus). Am. J. Phys. Anthropol. 142, 441–452 (2010).Article 

    Google Scholar 
    Ostner, J., Kappeler, P. & Heistermann, M. Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 62, 627–638 (2008).Article 

    Google Scholar 
    Heistermann, M., Palme, R. & Ganswindt, A. Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am. J. Primatol. 68, 257–273 (2006).Article 

    Google Scholar 
    Kappeler, P. M. & Fichtel, C. Female reproductive competition in Eulemur rufifrons: Eviction and reproductive restraint in a plurally breeding Malagasy primate. Mol. Ecol. 21, 685–698 (2012).Article 

    Google Scholar 
    Ostner, J., Kappeler, P. M. & Heistermann, M. Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 52, 485–495 (2002).Article 

    Google Scholar 
    Clough, D. Gastro-intestinal parasites of red-fronted lemurs in Kirindy Forest, western Madagascar. J. Parasitol. 96, 245–251 (2010).Article 

    Google Scholar 
    Gogarten, J. F. et al. Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny. Mol. Ecol. Resour. 20, 204–215 (2020).Article 

    Google Scholar 
    Barton, R. A. Allogrooming as mutualism in diurnal lemurs. Primates 28, 539–542 (1987).Article 

    Google Scholar 
    Noguera, J. C., Aira, M., Pérez-Losada, M., Domínguez, J. & Velando, A. Glucocorticoids modulate gastrointestinal microbiome in a wild bird. R. Soc. Open Sci. 5, 171743 (2018).Article 
    ADS 

    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, 1–11 (2013).Article 

    Google Scholar 
    Stoeck, T. et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19, 21–31 (2010).Article 

    Google Scholar 
    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 

    Google Scholar 
    Yarza, P. et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12, 635–645 (2014).Article 

    Google Scholar 
    Guillou, L. et al. The Protist Ribosomal Reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, 597–604 (2013).Article 

    Google Scholar 
    Gao, X., Lin, H., Revanna, K. & Dong, Q. A Bayesian taxonomic classification method for 16S rRNA gene sequences with improved species-level accuracy. BMC Bioinform. 18, 1–10 (2017).Article 

    Google Scholar 
    Reitmeier, S. et al. Handling of spurious sequences affects the outcome of high-throughput 16S rRNA gene amplicon profiling. ISME Commun. 1, 1–12 (2021).Article 

    Google Scholar 
    Shutt, K., Setchell, J. M. & Heistermann, M. Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): Validation of a fecal glucocorticoid assay and methods for practical application in the field. Gen. Comp. Endocrinol. 179, 167–177 (2012).Article 

    Google Scholar 
    Hämäläinen, A., Heistermann, M., Fenosoa, Z. S. E. & Kraus, C. Evaluating capture stress in wild gray mouse lemurs via repeated fecal sampling: Method validation and the influence of prior experience and handling protocols on stress responses. Gen. Comp. Endocrinol. 195, 68–79 (2014).Article 

    Google Scholar 
    Rudolph, K., Fichtel, C., Heistermann, M. & Kappeler, P. M. Dynamics and determinants of glucocorticoid metabolite concentrations in wild Verreaux’s sifakas. Horm. Behav. 124, 104760 (2020).Article 

    Google Scholar 
    Heitlinger, E., Ferreira, S. C. M., Thierer, D., Hofer, H. & East, M. L. The intestinal eukaryotic and bacterial biome of spotted hyenas: The impact of social status and age on diversity and composition. Front. Cell Infect. Microbiol. 7, 262 (2017).Article 

    Google Scholar 
    Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: Keep it maximal. J. Mem. Lang. 68, 255–278 (2013).Article 

    Google Scholar 
    Mallick, H. et al. Multivariable association discovery in population-scale meta-omics studies. PLoS Comput. Biol. 17, 1–27 (2021).Article 

    Google Scholar 
    De Cáceres, M., Legendre, P. & Moretti, M. Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684 (2010).Article 

    Google Scholar 
    Silk, J., Cheney, D. & Seyfarth, R. A practical guide to the study of social relationships. Evol. Anthropol. 22, 213–225 (2013).Article 

    Google Scholar 
    Ostner, J., Nunn, C. L. & Schülke, O. Female reproductive synchrony predicts skewed paternity across primates. Behav. Ecol. 19, 1150–1158 (2008).Article 

    Google Scholar 
    Bailey, M. T. et al. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain Behav. Immun. 25, 397–407 (2011).Article 

    Google Scholar 
    Bailey, M. T. et al. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect. Immun. 78, 1509–1519 (2010).Article 

    Google Scholar 
    Stothart, M. R. et al. Stress and the microbiome: Linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biol. Lett. 12, 20150875 (2016).Article 

    Google Scholar 
    Vlčková, K. et al. Impact of stress on the gut microbiome of free-ranging western lowland gorillas. Microbiol 164, 40–44 (2018).Article 

    Google Scholar 
    Chu, H. & Mazmanian, S. K. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 14, 668–675 (2013).Article 

    Google Scholar 
    Zheng, D., Liwinski, T. & Elinav, E. Interaction between microbiota and immunity in health and disease. Cell Res. 30, 492–506 (2020).Article 

    Google Scholar 
    Ley, R. E. Prevotella in the gut: Choose carefully. Nat. Rev. Gastroenterol. Hepatol. 13, 69–70 (2016).Article 

    Google Scholar 
    Manara, S. et al. Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species. Genome Biol. 20, 299 (2019).Article 

    Google Scholar 
    Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).Article 

    Google Scholar 
    Maltz, R. M. et al. Prolonged restraint stressor exposure in outbred CD-1 mice impacts microbiota, colonic inflammation, and short chain fatty acids. PLoS ONE 13, 1–19 (2018).Article 

    Google Scholar 
    Ostner, J. & Heistermann, M. Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus). Gen. Comp. Endocrinol. 131, 274–283 (2003).Article 

    Google Scholar 
    Peckre, L. R., Defolie, C., Kappeler, P. M. & Fichtel, C. Potential self-medication using millipede secretions in red-fronted lemurs: Combining anointment and ingestion for a joint action against gastrointestinal parasites?. Primates 59, 483–494 (2018).Article 

    Google Scholar 
    Jenkins, T. P. et al. Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition. PLoS ONE 12, 1–18 (2017).Article 

    Google Scholar 
    Rosa, B. A. et al. Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome 6, 1–19 (2018).Article 

    Google Scholar 
    Reynolds, L. A., Finlay, B. B. & Maizels, R. M. Cohabitation in the intestine: Interactions among helminth parasites, bacterial microbiota, and host immunity. J. Immunol. 195, 4059–4066 (2015).Article 

    Google Scholar 
    Toro-Londono, M. A., Bedoya-Urrego, K., Garcia-Montoya, G. M., Galvan-Diaz, A. L. & Alzate, J. F. Intestinal parasitic infection alters bacterial gut microbiota in children. PeerJ 2019, 1–24 (2019).
    Google Scholar 
    Vacca, M. et al. The controversial role of human gut Lachnospiraceae. Microorganisms 8, 1–25 (2020).Article 

    Google Scholar 
    Wei, Z. et al. The effects of non-fiber carbohydrate content and forage type on rumen microbiome of dairy cows. Animals 11, 1–17 (2021).Article 

    Google Scholar 
    Kaakoush, N. O. Insights into the role of Erysipelotrichaceae in the human host. Front. Cell Infect. Microbiol. 5, 1–4 (2015).Article 

    Google Scholar 
    Ricaboni, D. et al. ‘Colidextribacter massiliensis’ gen. nov., sp. nov., isolated from human right colon. New Microbes New Infect. 17, 27–29 (2017).Article 

    Google Scholar 
    Qin, P. et al. Characterization a novel butyric acid-producing bacterium Collinsella aerofaciens subsp. shenzhenensis subsp. nov. Microorganisms 7, 78 (2019).Article 

    Google Scholar 
    Wei, Y. et al. Commensal bacteria impact a protozoan’s integration into the murine gut microbiota in a dietary nutrient-dependent manner. Appl. Environ. Microbiol. 86, e00303-20 (2020).Article 
    ADS 

    Google Scholar 
    Perofsky, A. C., Ancel Meyers, L., Abondano, L. A., Di Fiore, A. & Lewis, R. J. Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes. Mol. Ecol. 30, 6759–6775 (2021).Article 

    Google Scholar 
    Pyritz, L., Kappeler, P. M. & Fichtel, C. Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): Processes and influence of ecological and reproductive seasonality. Int. J. Primatol. 32, 1325–1347 (2011).Article 

    Google Scholar 
    Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353 (2013).Article 

    Google Scholar 
    Hippe, H., Hagelstein, A., Kramer, I., Swiderski, J. & Stackebrandt, E. Phylogenetic analysis of Formivibrio citricus, Propionivibrio dicarboxylicus, Anaerobiospirillum thomasii, Succinirnonas amylolytica and Succinivibrio dextrinosolvens and proposal of Succinivibrionaceae fam. nov. Int. J. Syst. Evol. Microbiol. 49, 779–782 (1999).Article 

    Google Scholar 
    Grieneisen, L. E., Livermore, J., Alberts, S., Tung, J. & Archie, E. A. Group living and male dispersal predict the core gut microbiome in wild baboons. Integr. Comp. Biol. 57, 770–785 (2017).Article 

    Google Scholar 
    Amoroso, C. R., Kappeler, P. M., Fichtel, C. & Nunn, C. L. Fecal contamination, parasite risk, and waterhole use by wild animals in a dry deciduous forest. Behav. Ecol. Sociobiol. 73, 1–11 (2019).Article 

    Google Scholar 
    Vandeputte, D. et al. Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates. Gut 65, 57–62 (2016).Article 

    Google Scholar 
    Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016).Article 
    ADS 

    Google Scholar 
    Sonnenburg, J. L. & Bäckhed, F. Diet-microbiota interactions as moderators of human metabolism. Nature 535, 56–64 (2016).Article 
    ADS 

    Google Scholar 
    Zmora, N., Suez, J. & Elinav, E. You are what you eat: Diet, health and the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. 16, 25–56 (2018).
    Google Scholar 
    Ortmann, S., Bradley, B. J., Stolter, C. & Ganzhorn, J. U. Estimating the quality and composition of wild animal diets—a critical survey of methods. In Feeding Ecology in Apes and Other Primates. Ecological, Physical, and Behavioral Aspects (eds Hohmann, G. et al.) 395–418 (Cambridge University Press, 2006).
    Google Scholar  More

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    Trioecy is maintained as a time-stable mating system in the pink sea urchin Toxopneustes roseus from the Mexican Pacific

    According to the information that exists so far regarding reproduction in echinoderms, this is the first work in which the occurrence of trioecy in sea urchins is reported. This is also the first report of trioecy among members of the phylum Echinodermata, one of the most widespread taxa, both latitudinally and bathymetrically. Our results show that trioecy in this population of T. roseus is temporally stable, since the three sexes were observed together throughout the year in each month of sampling. Hermaphroditic individuals also presented the same gametogenic developmental pattern as females and males. Finally, during the spawning period of the population they contributed to the reproductive process by releasing mature gametes, which evidenced their full functionality within the studied population.We were unable to obtain evidence of self-fertilization in the studied hermaphrodites; but self- fertilization in the gonads and gonadal ducts of a hermaphrodite individual of Echinocardium cordatum was recorded in 193543. However, the embryos produced did not complete development successfully, probably due to the premature fertilization within the gonad43. Also, the cases of fully functional hermaphrodites of Arbacia punctulata have been reported44,45. The gametes of the hermaphrodites were fertilized as soon as they were released into seawater and the development of self-fertilized eggs was absolutely normal in time and morphology. After nine days, typical pluteus larvae were obtained and both the eggs and sperm of the hermaphrodites functioned ordinarily with gametes from other males and females.Therefore, we consider that there are no reasons to think that in the case of Toxopneustes roseus hermaphrodites cannot carry out self-fertilization. According to the analysis of the gonad developmental stages, their gametes were released into seawater. Theoretically, those gametes would be able to follow the normal course of fertilization, interacting among them and with gametes of females and males.The trioecic condition has been recorded so far only in some animals, such as a few nematode species and a hydra9,10,14,46,47,48. In marine invertebrates, it has been reported in one anemone under laboratory conditions and in one bivalve mollusk15,16. The coexistence of males, females and hermaphrodites has been considered an evolutionarily transitory state; for example, androdioecy (male / hermaphrodite) in nematodes such as Caenorhabditis elegans is believed to have evolved from dioecy (male / female) through a trioic intermediate. Consequently, it is very difficult to find the ecological or evolutionary causes that lead a species or population to present three sexes simultaneously49.In the species in which trioecy has been studied and monitored, it is noticeable that their populations are subjected to strong environmental stress in situ or under laboratory manipulation50,51,52. For example, some nematodes of the genus Tokorhabditis are extremophilic species that live in the Californian Mono Lake, which is characterized by being hypersaline and exhibiting high levels of arsenic10,50. In the case of Auanema freiburgensis the flexible sex determination and mating system and, consequently, its trioecy can be critical for resilience at the population level in patchy, resource-limited environments49. These results thus demonstrate that life-history, ecology and environment can play defining roles in the development of sexual systems and determine the continued presence of trioecy in the nematode. In the case of Hydra viridissima, it unlike most European species, is a “warm crisis” hydra, since it usually reproduces asexually, but when the temperatures rise to, or are maintained at high levels (≥ 20 °C), it reproduces sexually14,53. In experimental conditions, the population studied essentially behaved as androdioecic and only at the end of the research period, when the temperature was the highest (~ 25 °C), a few females appeared and joined the other existing sexes, thus generating the condition of trioecy14. Trioecy has been identified in another non-described species (e.g., Rhabditis sp. JU1783) isolated from star fruit, although it is closely related to A. rhodensis and A. freiburgensis and likely to belong to the same genus11,12. Little is known about the ecology of Auanema, as A. rhodensis has been isolated from a tick and a beetle, and A. freiburgensis from dung and a rotting plant of the genus Petasites12,47,51.Regarding the sea anemone Aiptasia diaphana, it is mainly found in isolated fouling communities, and no hermaphrodites exist in natural populations that could reproduce asexually or sexually54. However, under laboratory conditions, a single founder individual (asexual clone) produced not only males and females, but also hermaphroditic individuals. In addition, A. diaphana can fertilize within and between cloning lines, producing larval-swimming planules, which could explain the success of the species as an invader of artificial marine substrates. The condition of trioecy was also identified in individuals of this anemone manipulated in the laboratory, to create age-homogeneous populations of asexual propagules (pedal lacerations) and ontogenetic patterns of sexual differentiation were documented15.In the case of the marine bivalve Semimytilus algosus, there was not an obvious explanation for the occurrence of its trioecy, despite the intense analyses of factors such as motility versus a sessile way of life or reproductive density within a population, which could have relevance for gamete interactions16. In many respects, S. algosus is a “typical” marine intertidal mussel, since it is sessile in adulthood, occurs at high densities in wild populations, and has a very large population. S. algosus also co-occurs with other species that are close relatives within the Mytilidae family and have evolved and conserved their dioecy16.Toxopneustes roseus is another typical species of sea urchin, which has a wide latitudinal distribution throughout the tropical eastern Pacific and co-inhabits with other species of sea urchins and echinoderms that have a similar distribution and in which hermaphroditism has not been reported40,55,56,57. Regarding its population density, T. roseus is not considered among the most abundant species in the study area and its densities are relatively low (between 0.04 and 1.2 ind.m2). However, it cannot be considered a rare species in terms of abundance58,59.All of the above makes it difficult to clearly explain the reasons for the occurrence of trioecy in this species; however, certain aspects of its early development are known that could indicate the factors behind the development of this reproductive mating system in the pink sea urchin. In recent experiments carried out with gametes, larvae, and embryos of a population of T. roseus from the same area as our study, it was found that the increase in temperature above the normal values of its habitat has a deleterious effect on the success of early development60. There exists experimental evidence that at an increase of temperature to 32 °C, which is 2 °C above the maximum values registered in the study area, fertilization occurred at a very low percentage. There was also a deleterious effect on embryos, resulting in abnormal development and the lowest percentage of larval survival also occurred at 32 °C60. The same kind of experiments has been performed on other species from the study area, such as the irregular sea urchin Ryncholampas pacificus and the intertidal Echinometra vanbrunti. The deleterious effects on these species were observed only at 34 °C, which was the highest temperature tested (unpublished data). At 32 °C, however, there was no evidence of negative effects in the case on E. vanbrunti, and there was just arrested development, but no abnormalities in the case of R. pacificus. These results indicate that T. roseus is much more sensitive to the rise in temperature than other cohabiting sea urchins, and probably lives near its upper thermal limit. In that context, the continuous ocean warming could threaten the permanence of the species in the study area, since the early stages of development constitute a bottleneck for successful recruitment and later population maintenance in populations that carry out reproduction by means of external fertilization.Within the phylum Echinodermata, when stressful conditions appear in the habitat or the environment becomes hostile, the species can generally resort to asexual reproduction by fission (ophiuroids) or fission and autotomy (holothuroids and asteroids) to increase the abundance of populations in a relatively short time or counteract a threat with numbers61. This does not apply to sea urchins since they are unable to reproduce asexually. The only way for sea urchins to reproduce asexually would be by cloning larvae, but this process would also require that sexual reproduction occurs first62. Therefore, any reproductive strategy that a sea urchin population could develop to respond to drastic changes in their area must involve sexual reproduction. In this regard, in an experimental evolution study with the nematode Caenorhabditis elegans, in which partial selfing, exclusive selfing, and predominant outcrossing were compared, it was evidenced that monoecious populations only have hermaphrodites and, therefore, reproduction is carried out exclusively by self-fertilization. However, in trioic populations that have males, females, and a small number of hermaphrodites, reproduction is predominantly carried out by external crossing49. Also populations that underwent some degree of interbreeding during the evolutionary experiments (trioic and androdioic populations), maintained more genetic diversity than expected solely under genetic drift or under genetic drift and directional selection49. In this sense, it is possible that high levels of interbreeding, such as that which occurs in trioic populations, develop with populations that have sufficient deleterious recessive alleles to avoid extinction, since selection is less efficient to purge them. Trioecy, therefore, becomes an efficient system to select characteristics of the genome that allows a population that only reproduces sexually to adequately cope with significant changes in the environment that could threaten the permanence of the species in that habitat. Interbreeding (gonochorism, self-incompatible hermaphroditism) also favors genetic diversity and offers greater potential to adapt to changing environments63. The costs and advantages of crossing over selfing depend on environmental factors and, therefore, selection may favor transitions between mating systems. Androdioecy, gynodioecy, and trioecy are evolutionarily unstable intermediate strategies, but they offer important systems for testing models of the causes and consequences of the mating system in the evolution of populations63.However, the question remains why T. roseus has developed trioecy, when in the same habitat there are other sea urchins with very similar life-histories that only maintain dioecy. In the case of the bivalve Semimytilus algosus; which presents the same situation as we have with T. roseus, it was proposed that the trioecy of the species may be related to the sex determination mechanism, considering what it is known about the nematodes of the genus Auanema10,16,46. In Auanema, the male versus non-male (hermaphrodite or female) decision is determined genetically (XO for males, and XX for females and hermaphrodites)9,64. The hermaphrodite versus female decision, however, is determined by the environment of the mother. For A. freiburgensis the maternal social environment is determinant, whereas for A. rhodensis it is the age of the mother9,12,51,65. Therefore, in Auanema, environmental sex determination and genetic sex determination interact to produce trioecy.Although there is apparently no clear cause of strong, stressful conditions in the habitat of T. roseus that could threaten the survival of this species, according to the United States Environmental Protection Agency (EPA, 2021), sea surface temperature increased during the twentieth century and continues to rise. From 1901 to 2020, the global temperature rose at an average rate of 0.004 °C per decade, resulting in a total increase of 0.5 °C to date. Additionally, regional studies based on continuous monitoring, which have not yet been published, have shown that between 2002 and 2020 there has been an increase of approximately 1 °C above the historical average of the sea surface temperature in the study area.The foregoing discussion leads us to speculate that the studied population of T. roseus lives at the limit of its thermal tolerance, and the constant increase in ocean temperature due to global warming constitutes a threat to its survival and a constant source of stress for the population. This is because its early-development stages are more vulnerable to high temperature than other sea urchins that live in the same area and its population density is also significantly lower58.Phylogenetically T. roseus belongs to Family Toxopneustidae and although no other species within the genus Toxopneustes has shown hermaphroditism, this condition was reported in Tripneustes gratilla, which belongs to the same family36. Toxopneustids belong to the Order Camarodonta, and almost all the species of sea urchins in which hermaphroditism has been reported belong to this Order except for a couple that belong to the Arbacioida. At the same time, this order is contained in the Superorder Echinacea along with Camarodonta, according to the last exhaustive analysis resolving the position of the clades within Echinoidea66. In this context, theoretically T. roseus at some point underwent the environmental pressure of its early stage living under constantly rising temperatures, along with its low population densities in the study area. Consequently, it was able to develop hermaphroditism and, therefore, trioecy, similarly to what occurred to Hydra viridissima under conditions of extreme high temperature14. We hypothesize that these permanent conditions generate a constant source of strong environmental stress, which is the determining factor that keeps trioecy stable in the species in which it has been studied, and, thus, trioecy remains stable in this population of T. roseus.The mechanism of sex determination in echinoids, as well as in other echinoderms, is still unknown, although the sex ratio, which is generally close to 1:1, suggests that it occurs through sex chromosomes67. It is known that in mammals, sex determination is dictated by the presence or absence of the Y-chromosomal gene SRY. SRY functions as the primary sex-determining gene by activating testis formation, and in its absence, the embryo will form ovaries. SRY only exists in mammals; however it evolved as a duplication of the Sox gene family, which exists in all metazoans68.In vertebrates, Sox genes are involved in sex determination, neurogenesis, skeletonogenesis, eye development, pituitary development, pancreas formation, and neural crest and notochord formation69. In invertebrates, they are involved in processes such as metamorphosis, eye development, neural crest formation, and ectoderm formation70. In the sea urchin Strongylocentrotus purpuratus, SoxB1 was determined to be expressed in the primordial gut during development and is closely related in sequence to Sox genes of the mouse embryo71. An investigation of sex determination was carried out in the sea urchin Strongylocentrotus purpuratus using RNA-seq and quantitative mRNA measurements, but the mechanisms that govern sexual determination of the species could not be clearly established72. However; the results show that the male fate factors Dmrt and SoxH are expressed early and meiosis initiates early. Also, gonad-specific transcripts involved in egg and sperm biology, are first activated before rudiment formation in the larvae of this sea urchin. The study provided additional evidence for the hypothesis that in sea urchins, sex determination occurs genetically72. Another research with the sea cucumber Apostichopus japonicus, which integrated genome-wide association study and analyzes of sex-specific variations evidenced that the species exhibits genetic sexual determination73. Furthermore, analysis of homozygous and heterozygous genotypes of abundant sex-specific SNPs in females and males, confirmed that A.japonicus might have a XX/XY sex determination system73.On the other hand, it has been proposed that a deviation from the 1:1 sex ratio in echinoids could reflect environmental conditions that influence sex determination67. For example, a relatively large proportion of Lytechinus variegatus and Tripneustes ventricosus (as Tripneustes esculentus) hermaphrodites was recorded in southern Florida during an unusually cold winter, suggesting that adverse winter conditions in some way affected sex determination in juveniles74,75. Also relatively large number of Strongylocentrotus purpuratus hermaphrodites was reported in Bahía de Todos los Santos, Mexico, where extreme seasonal fluctuations in temperature (from about 12–24 °C) are recorded76. However, posterior studies did not find a single hermaphrodite of Strongylocentrotus purpuratus in more than 500 individuals analyzed77,78.Considering that sex determination in sea urchins is highly probable to occur genetically and the possibility that the environment may also influence sex determination, we think that in the case of Toxopneustes roseus, genetic sex determination and environmental sex determination are interacting to maintain the condition of trioecy stable. We propose that, especially because the cases in which environmental conditions have assumed to influence sex determination, extreme temperatures are invoked as the main affecting factor. However, more detailed studies are needed in terms of sexual determination and experimental evolution to be able to verify our assumption.In general, the efforts that have been made to explain the evolution of the sexes and the origin of hermaphroditism and trioecy are still scarce, and critical questions remain to be answered. The case of trioecy detected in T. roseus may constitute an important model to seek these answers about the evolution of sexual systems and the environmental mechanisms that trigger trioecy in marine macroinvertebrates and, in particular, in echinoderms. More

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    Recent global decline in rainfall interception loss due to altered rainfall regimes

    Savenije, H. H. G. The importance of interception and why we should delete the term evapotranspiration from our vocabulary. Hydrol. Process. 18, 1507–1511 (2004).Article 
    ADS 

    Google Scholar 
    Gerrits, A. M. J., Pfister, L. & Savenije, H. H. G. Spatial and temporal variability of canopy and forest floor interception in a beech forest. Hydrol. Process. 24, 3011–3025 (2010).Article 
    ADS 

    Google Scholar 
    Porada, P., Van Stan, J. T. & Kleidon, A. Significant contribution of non-vascular vegetation to global rainfall interception. Nat. Geosci. 11, 563–567 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    van der Ent, R. J., Wang-Erlandsson, L., Keys, P. W. & Savenije, H. H. G. Contrasting roles of interception and transpiration in the hydrological cycle – Part 2: moisture recycling. Earth Syst. Dyn. 5, 471–489 (2014).Article 
    ADS 

    Google Scholar 
    Lian, X. et al. Partitioning global land evapotranspiration using CMIP5 models constrained by observations. Nat. Clim. Change 8, 640–646 (2018).Article 
    ADS 

    Google Scholar 
    Coenders-Gerrits, A. M. et al. Uncertainties in transpiration estimates. Nature 506, E1–E2 (2014).Article 
    CAS 

    Google Scholar 
    Chang, L.-L. et al. Why do large-scale land surface models produce a low ratio of transpiration to evapotranspiration? J. Geophys. Res. Atmos. 123, 9109–9130 (2018).Article 

    Google Scholar 
    Zwieback, S., Chang, Q., Marsh, P. & Berg, A. Shrub tundra ecohydrology: rainfall interception is a major component of the water balance. Environ. Res. Lett. 14, 055005 (2019).Article 
    ADS 

    Google Scholar 
    Cuartas, L. A. et al. Interception water-partitioning dynamics for a pristine rainforest in Central Amazonia: Marked differences between normal and dry years. Agric. For. Meteorol. 145, 69–83 (2007).Article 
    ADS 

    Google Scholar 
    Yue, K. et al. Global patterns and drivers of rainfall partitioning by trees and shrubs. Glob. Change Biol. 27, 3350–3357 (2021).Article 

    Google Scholar 
    Pastorello, G. et al. The FLUXNET2015 dataset and the ONEFlux processing pipeline for eddy covariance data. Sci. Data 7, 225 (2020).Article 

    Google Scholar 
    Tramontana, G. et al. Predicting carbon dioxide and energy fluxes across global FLUXNET sites with regression algorithms. Biogeosciences 13, 4291–4313 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Jung, M., Reichstein, M. & Bondeau, A. Towards global empirical upscaling of FLUXNET eddy covariance observations: validation of a model tree ensemble approach using a biosphere model. Biogeosciences 6, 2001–2013 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Li, X. et al. Spatiotemporal pattern of terrestrial evapotranspiration in China during the past thirty years. Agric. For. Meteorol. 259, 131–140 (2018).Article 
    ADS 

    Google Scholar 
    Koppa, A., Rains, D., Hulsman, P., Poyatos, R. & Miralles, D. G. A deep learning-based hybrid model of global terrestrial evaporation. Nat. Commun. 13, 1912 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Zheng, C. & Jia, L. Global canopy rainfall interception loss derived from satellite Earth observations. Ecohydrology 13, e2186 (2019).
    Google Scholar 
    Muzylo, A. et al. A review of rainfall interception modelling. J. Hydrol. 370, 191–206 (2009).Article 
    ADS 

    Google Scholar 
    Miralles, D. G., Gash, J. H., Holmes, T. R. H., de Jeu, R. A. M., & Dolman, A. J. Global canopy interception from satellite observations. J. Geophys. Res. 115, D16122 (2010).Article 
    ADS 

    Google Scholar 
    Martens, B. et al. GLEAM v3: satellite-based land evaporation and root-zone soil moisture. Geosci. Model Dev. 10, 1903–1925 (2017).Article 
    ADS 

    Google Scholar 
    Oleson, K. et al. Technical Description of Version 4.5 of the Community Land Model (CLM) Report NCAR/TN-503+STR, https://doi.org/10.5065/D6RR1W7M (2013).Gash, J. An analytical model of rainfall interception by forests. Q. J. Roy. Meteor. Soc. 105, 43–55 (1979).Article 
    ADS 

    Google Scholar 
    Fan, Y. et al. Reconciling canopy interception parameterization and rainfall forcing frequency in the Community Land Model for simulating evapotranspiration of rainforests and oil palm plantations in Indonesia. J. Adv. Model. Earth Syst. 11, 732–751 (2019).Article 
    ADS 

    Google Scholar 
    Návar, J. Modeling rainfall interception loss components of forests. J. Hydrol. 584, 124449 (2019).Article 

    Google Scholar 
    Kang, M., Kwon, H., Cheon, J. H. & Kim, J. On estimating wet canopy evaporation from deciduous and coniferous forests in the Asian monsoon climate. J. Hydrometeorol. 13, 950–965 (2012).Article 
    ADS 

    Google Scholar 
    Llorens, P., Domingo, F., Garcia-Estringana, P., Muzylo, A. & Gallart, F. Canopy wetness patterns in a Mediterranean deciduous stand. J. Hydrol. 512, 254–262 (2014).Article 
    ADS 

    Google Scholar 
    Czikowsky, M. J. & Fitzjarrald, D. R. Detecting rainfall interception in an Amazonian rain forest with eddy flux measurements. J. Hydrol. 377, 92–105 (2009).Article 
    ADS 

    Google Scholar 
    Renninger, H. J., Phillips, N. & Salvucci, G. D. Wet- vs. dry-season transpiration in an Amazonian rain forest palm iriartea deltoidea. Biotropica 42, 470–478 (2010).Article 

    Google Scholar 
    Zhao, W. et al. Physics-constrained machine learning of evapotranspiration. Geophys. Res. Lett. 46, 14496–14507 (2019).Article 
    ADS 

    Google Scholar 
    Zabret, K. & Šraj, M. How characteristics of a rainfall event and the meteorological conditions determine the development of stemflow: A case study of a birch tree. Front. Glob. Change 4, 663100 (2022).Article 

    Google Scholar 
    Calder, I. R. Dependence of rainfall interception on drop size: 1. Development of the two-layer stochastic model. J. Hydrol. 185, 363–378 (1996).Article 
    ADS 

    Google Scholar 
    Niinemets, Ü. A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol. Res. 25, 693–714 (2010).Article 

    Google Scholar 
    Gordon, D. A. R., Coenders-Gerrits, M., Sellers, B. A., Sadeghi, S., & Van Stan II, J. T. Rainfall interception and redistribution by a common North American understory and pasture forb, Eupatorium capillifolium (Lam. dogfennel). Hydrol. Earth Syst. Sci. 24, 4587–4599 (2020).Article 
    ADS 

    Google Scholar 
    Ciruzzi, D. M. & Loheide, S. P. II Monitoring tree sway as an indicator of interception dynamics before, during, and following a storm. Geophys. Res. Lett. 48, e2021GL094980 (2021).Article 
    ADS 

    Google Scholar 
    Karimi, P., Bastiaanssen, W. G. & Molden, D. Water Accounting Plus (WA+)–a water accounting procedure for complex river basins based on satellite measurements. Hydrol. Earth Syst. Sci. 17, 2459–2472 (2013).Article 
    ADS 

    Google Scholar 
    del Campo, A. D., González-Sanchis, M., Lidón, A., Ceacero, C. J. & García-Prats, A. Rainfall partitioning after thinning in two low-biomass semiarid forests: Impact of meteorological variables and forest structure on the effectiveness of water-oriented treatments. J. Hydrol. 565, 74–86 (2018).Article 

    Google Scholar 
    Lian, X. et al. Multifaceted characteristics of dryland aridity changes in a warming world. Nat. Rev. Earth Environ. 2, 232–250 (2021).Article 
    ADS 

    Google Scholar 
    Piao, S. et al. Characteristics, drivers and feedbacks of global greening. Nat. Rev. Earth Environ. 1, 14–27 (2020).Article 
    ADS 

    Google Scholar 
    Feng, X. et al. Revegetation in China’s Loess Plateau is approaching sustainable water resource limits. Nat. Clim. Change 6, 1019–1022 (2016).Article 
    ADS 

    Google Scholar 
    Dawson, T. E. & Goldsmith, G. R. The value of wet leaves. N. Phytol. 219, 1156–1169 (2018).Article 

    Google Scholar 
    Aparecido, L. M. T., Miller, G. R., Cahill, A. T. & Moore, G. W. Comparison of tree transpiration under wet and dry canopy conditions in a Costa Rican premontane tropical forest. Hydrol. Process. 30, 5000–5011 (2016).Article 
    ADS 

    Google Scholar 
    Huang, L. & Zhang, Z. Effect of rainfall pulses on plant growth and transpiration of two xerophytic shrubs in a revegetated desert area: Tengger Desert, China. CATENA 137, 269–276 (2016).Article 

    Google Scholar 
    Fathizadeh, O., Hosseini, S., Zimmermann, A., Keim, R. & Boloorani, A. D. Estimating linkages between forest structural variables and rainfall interception parameters in semi-arid deciduous oak forest stands. Sci. Total Environ. 601, 1824–1837 (2017).Article 
    ADS 

    Google Scholar 
    Zhang, Z.-S., Zhao, Y., Li, X.-R., Huang, L. & Tan, H.-J. Gross rainfall amount and maximum rainfall intensity in 60-minute influence on interception loss of shrubs: a 10-year observation in the Tengger Desert. Sci. Rep. 6, 26030 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    de Groen, M. M. & Savenije, H. H. G. A monthly interception equation based on the statistical characteristics of daily rainfall. Water Resour. Res. 42, W12417 (2006).Article 
    ADS 

    Google Scholar 
    Chinita, M. J., Richardson, M., Teixeira, J. & Miranda, P. M. A. Global mean frequency increases of daily and sub-daily heavy precipitation in ERA5. Environ. Res. Lett. 16, 074035 (2021).Article 
    ADS 

    Google Scholar 
    Donat, M. G., Lowry, A. L., Alexander, L. V., O’Gorman, P. A. & Maher, N. More extreme precipitation in the world’s dry and wet regions. Nat. Clim. Change 6, 508–513 (2016).Article 
    ADS 

    Google Scholar 
    IPCC. The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (eds Masson-Delmotte, V. et al) (Cambridge Univ. Press, 2021).Ficklin, D. L., Null, S. E., Abatzoglou, J. T., Novick, K. A. & Myers, D. T. Hydrological intensification will increase the complexity of water resource management. Earth’s Futur. 10, e2021EF002487 (2022).Article 
    ADS 

    Google Scholar 
    Haslwanter, A., Hammerle, A. & Wohlfahrt, G. Open-path vs. closed-path eddy covariance measurements of the net ecosystem carbon dioxide and water vapour exchange: a long-term perspective. Agric. For. Meteorol. 149, 291–302 (2009).Article 
    ADS 

    Google Scholar 
    Migliavacca, M. et al. The three major axes of terrestrial ecosystem function. Nature 598, 468–472 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Zhang, W. et al. The effect of relative humidity on eddy covariance latent heat flux measurements and its implication for partitioning into transpiration and evaporation. Preprint at https://doi.org/10.2139/ssrn.4106267 (2022).van Dijk, A. I. J. M. et al. Rainfall interception and the coupled surface water and energy balance. Agric. For. Meteorol. 214–215, 402–415 (2015).Article 

    Google Scholar 
    Barr, A. G., Morgenstern, K., Black, T. A., McCaughey, J. H. & Nesic, Z. Surface energy balance closure by the eddy-covariance method above three boreal forest stands and implications for the measurement of the CO2 flux. Agric. Meteorol. 140, 322–337 (2006).Article 

    Google Scholar 
    Reichstein, M. et al. Deep learning and process understanding for data-driven Earth system science. Nature 566, 195–204 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Zhi, W. et al. From hydrometeorology to river water quality: can a deep learning model predict dissolved oxygen at the continental scale? Environ. Sci. Technol. 55, 2357–2368 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Kraft, B., Jung, M., Körner, M. & Reichstein, M. Hybrid modeling: fusion of a deep approach and physics-based model for global hydrological modeling. Int. Arch. Photogramm. Remote Sens. Spat. Inf. Sci. 43, 1537–1544 (2020).Article 

    Google Scholar 
    Hoffmann, L. et al. From ERA-Interim to ERA5: the considerable impact of ECMWF’s next-generation reanalysis on Lagrangian transport simulations. Atmos. Chem. Phys. 19, 3097–3124 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Wang, D., Wang, G. & Anagnostou, E. N. Evaluation of canopy interception schemes in land surface models. J. Hydrol. 347, 308–318 (2007).Article 
    ADS 

    Google Scholar 
    Wang, G. & Eltahir, E. A. Modeling the biosphere–atmosphere system: The impact of the subgrid variability in rainfall interception. J. Clim. 13, 2887–2899 (2000).Article 
    ADS 

    Google Scholar 
    Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).Article 
    ADS 

    Google Scholar 
    Le Quéré, C. et al. Global carbon budget 2018. Earth Syst. Sci. Data 10, 2141–2194 (2018).Article 
    ADS 

    Google Scholar  More

  • in

    Machine learning prediction of connectivity, biodiversity and resilience in the Coral Triangle

    Ravindran, S. Coral reefs at a tipping point. Proc. Natl Acad. Sci. 113, 5140–5141 (2016).CAS 

    Google Scholar 
    Lenton, T. M. et al. Climate tipping points—too risky to bet against. Nature 575, 592–595 (2019).CAS 

    Google Scholar 
    Veron, J. E. N. et al. Delineating the Coral Triangle. Galaxea J. Coral Reef. Stud. 11, 91–100 (2009).
    Google Scholar 
    Hoegh-Guldberg, O. et al. Coral Reefs Under Rapid Climate Change and Ocean Acidification. Science 318, 1737–1742 (2007).CAS 

    Google Scholar 
    Brown, C., Corcoran, E. & Herkenrath, P. Marine and coastal ecosystems and human well-being: a synthesis report based on the findings of the Millennium Ecosystem Assessment. (2006).Heinze, C. et al. The quiet crossing of ocean tipping points. Proc. Natl Acad. Sci. 118, e2008478118 (2021).CAS 

    Google Scholar 
    Barber, P. H. The challenge of understanding the Coral Triangle biodiversity hotspot. J. Biogeogr. 36, 1845–1846 (2009).
    Google Scholar 
    Ekman, S. Zoogeography of the Sea. (Sidgwick & Jackson, 1953).Ladd, H. S. Origin of the Pacific island molluscan fauna. Am. J. Sci. 256, 137–150 (1960).
    Google Scholar 
    Woodland, D. J. Zoogeography of the Siganidae (Pisces): an interpretation of distribution and richness patterns. Bull. Mar. Sci. 33, 713–717 (1983).
    Google Scholar 
    Loveland, T. R. & Merchant, J. M. Ecoregions and ecoregionalization: geographical and ecological perspectives. Environ. Manag. 34, S1–S13 (2004).
    Google Scholar 
    Levins, R. Some Demographic and Genetic Consequences of Environmental Heterogeneity for Biological Control. Bull. Entomol. Soc. Am. 15, 237–240 (1969).
    Google Scholar 
    Obura, D. The Diversity and Biogeography of Western Indian Ocean Reef-Building Corals. PLoS One. 7, e45013 (2012).CAS 

    Google Scholar 
    Fontoura, L. et al. Protecting connectivity promotes successful biodiversity and fisheries conservation. Science 375, 336–340 (2022).CAS 

    Google Scholar 
    Roberts, C. M. Connectivity and Management of Caribbean Coral Reefs. Science 278, 1454–1457 (1997).CAS 

    Google Scholar 
    Ayre, D. J. & Hughes, T. P. Climate change, genotypic diversity and gene flow in reef-building corals: Gene flow in reef building corals. Ecol. Lett. 7, 273–278 (2004).
    Google Scholar 
    Graham, N. A. et al. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl Acad. Sci. 103, 8425–8429 (2006).CAS 

    Google Scholar 
    McClanahan, T. R. et al. Prioritizing Key Resilience Indicators to Support Coral Reef Management in a Changing Climate. PLoS One. 7, e42884 (2012).CAS 

    Google Scholar 
    Gilmour, J. P., Smith, L. D., Heyward, A. J., Baird, A. H. & Pratchett, M. S. Recovery of an Isolated Coral Reef System Following Severe Disturbance. Science 340, 69–71 (2013).
    Google Scholar 
    Grayson, N., Clements, C. S., Towner, A. A., Beatty, D. S. & Hay, M. E. Did the historic overharvesting of sea cucumbers make coral more susceptible to pathogens? Coral Reefs. 41, 447–453 (2022).
    Google Scholar 
    Spalding, M. D. et al. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience 57, 573–583 (2007).
    Google Scholar 
    Berline, L., Rammou, A.-M., Doglioli, A., Molcard, A. & Petrenko, A. A Connectivity-Based Eco-Regionalization Method of the Mediterranean Sea. PLoS ONE. 9, e111978 (2014).
    Google Scholar 
    Ser-Giacomi, E., Rossi, V., López, C. & Hernández-García, E. Flow networks: A characterization of geophysical fluid transport. Chaos Interdiscip. J. Nonlinear Sci. 25, 036404 (2015).
    Google Scholar 
    Thompson, D. M. et al. Variability in oceanographic barriers to coral larval dispersal: Do currents shape biodiversity? Prog. Oceanogr. 165, 110–122 (2018).
    Google Scholar 
    Treml, E. A., Halpin, P. N., Urban, D. L. & Pratson, L. F. Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landsc. Ecol. 23, 19–36 (2008).
    Google Scholar 
    Liu, G., Bracco, A., Quattrini, A. M. & Herrera, S. Kilometer-Scale Larval Dispersal Processes Predict Metapopulation Connectivity Pathways for Paramuricea biscaya in the Northern Gulf of Mexico. Front. Mar. Sci. 8, 790927 (2021).
    Google Scholar 
    Fountalis, I., Dovrolis, C., Bracco, A., Dilkina, B. & Keilholz, S. δ-MAPS: from spatio-temporal data to a weighted and lagged network between functional domains. Appl. Netw. Sci. 3, 21 (2018).
    Google Scholar 
    Falasca, F., Bracco, A., Nenes, A. & Fountalis, I. Dimensionality Reduction and Network Inference for Climate Data Using δ‐MAPS: Application to the CESM Large Ensemble Sea Surface Temperature. J. Adv. Model. Earth Syst. 11, 1479–1515 (2019).
    Google Scholar 
    Novi, L., Bracco, A. & Falasca, F. Uncovering marine connectivity through sea surface temperature. Sci. Rep. 11, 8839 (2021).CAS 

    Google Scholar 
    Kleypas, J. A., Castruccio, F. S., Curchitser, E. N. & Mcleod, F. The impact of ENSO on coral heat stress in the western equatorial Pacific. Glob. Change Biol. 21, 2525–2539 (2015).
    Google Scholar 
    GLOBAL_REANALYSIS_001_030. Global Ocean Physics Reanalysis GLORYS12V1 1/12° product. MERCATOR GLORYS12V1 (global-reanalysis-001-030-monthly). E.U. Copernicus Marine Service Information (CMEMS). https://doi.org/10.48670/moi-00021.Lellouche, J.-M. et al. The Copernicus Global 1/12° Oceanic and Sea Ice GLORYS12 Reanalysis. Front. Earth Sci. 9, 698876 (2021).
    Google Scholar 
    Treml, E. A. & Halpin, P. N. Marine population connectivity identifies ecological neighbors for conservation planning in the Coral Triangle: Ecological neighbors in conservation. Conserv. Lett. 5, 441–449 (2012).
    Google Scholar 
    Meyers, G. Variation of Indonesian throughflow and the El Niño-Southern Oscillation. J. Geophys. Res. Oceans 101, 12255–12263 (1996).
    Google Scholar 
    Wolfram Research (2012), FindGraphCommunities, Wolfram Language function. https://reference.wolfram.com/language/ref/FindGraphCommunities.html (updated 2015).MacArthur, R. H. & Wilson, E. O. The theory of island biogeography. In The Theory of Island Biogeography (Princeton university press, 2016).Brin, S. & Page, L. The anatomy of a large-scale hypertextual Web search engine. Comput. Netw. ISDN Syst. 30, 107–117 (1998).
    Google Scholar 
    Wolfram Research (2010), PageRankCentrality, Wolfram Language function. https://reference.wolfram.com/language/ref/PageRankCentrality.html (Updated 2015).NOAA Coral Reef Watch program, 20180813, NOAA Coral Reef Watch Version 3.1 Daily Global 5km Satellite Coral Bleaching Heat Stress Monitoring Product Suite: NOAA Coral Reef Watch program, College Park, Maryland, USA. https://coralreefwatch.noaa.gov/product/5km/.Liu, G. et al. Reef-Scale Thermal Stress Monitoring of Coral Ecosystems: New 5-km Global Products from NOAA Coral Reef Watch. Remote Sens. 6, 11579–11606 (2014).
    Google Scholar 
    Liu, G. et al. NOAA Coral Reef Watch’s 5km Satellite Coral Bleaching Heat Stress Monitoring Product Suite Version 3 and Four-Month Outlook Version 4. 32, 7 (2017).Claar, D. C., Szostek, L., McDevitt-Irwin, J. M., Schanze, J. J. & Baum, J. K. Global patterns and impacts of El Niño events on coral reefs: A meta-analysis. PLOS ONE 13, e0190957 (2018).
    Google Scholar 
    Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264 (2019).CAS 

    Google Scholar 
    Darling, E. S. et al. Social–environmental drivers inform strategic management of coral reefs in the Anthropocene. Nat. Ecol. Evol. 3, 1341–1350 (2019).
    Google Scholar 
    Dance, A. These corals could survive climate change—and help save the world’s reefs. Nature 575, 580–582 (2019).CAS 

    Google Scholar 
    Renema, W. et al. Hopping Hotspots: Global Shifts in Marine Biodiversity. Science 321, 654–657 (2008).CAS 

    Google Scholar 
    Weiss, T. L., Denniston, R. F., Wanamaker, A. D., Villarini, G. & von der Heydt, A. S. El Niño–Southern Oscillation–like variability in a late Miocene Caribbean coral. Geology 45, 643–646 (2017).
    Google Scholar 
    Watanabe, T. et al. Permanent El Niño during the Pliocene warm period not supported by coral evidence. Nature 471, 209–211 (2011).CAS 

    Google Scholar 
    Von Der Heydt, A. S. & Dijkstra, H. A. The impact of ocean gateways on ENSO variability in the Miocene. Geol. Soc. Lond. Spec. Publ. 355, 305–318 (2011).
    Google Scholar 
    Yasuhara, M. et al. Past and future decline of tropical pelagic biodiversity. Proc. Natl Acad. Sci. 117, 12891–12896 (2020).CAS 

    Google Scholar 
    Falasca, F., Crétat, J., Bracco, A., Braconnot, P. & Marti, O. Climate change in the Indo-Pacific basin from mid- to late Holocene. Clim. Dyn. 59, 753–766 (2022).
    Google Scholar 
    Treml, E. A., Ford, J. R., Black, K. P. & Swearer, S. E. Identifying the key biophysical drivers, connectivity outcomes, and metapopulation consequences of larval dispersal in the sea. Mov. Ecol. 3, 17 (2015).
    Google Scholar 
    Hackerott, S., Martell, H. A. & Eirin-Lopez, J. M. Coral environmental memory: causes, mechanisms, and consequences for future reefs. Trends Ecol. Evol. 36, 1011–1023 (2021).
    Google Scholar 
    Ogle, K. et al. Quantifying ecological memory in plant and ecosystem processes. Ecol. Lett. 18, 221–235 (2015).
    Google Scholar 
    Peterson, G. D. Contagious Disturbance, Ecological Memory, and the Emergence of Landscape Pattern. Ecosystems 5, 329–338 (2002).
    Google Scholar 
    Thomas, L., López, E. H., Morikawa, M. K. & Palumbi, S. R. Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef‐building corals. Mol. Ecol. 28, 3371–3382 (2019).
    Google Scholar 
    Dziedzic, K. E., Elder, H., Tavalire, H. & Meyer, E. Heritable variation in bleaching responses and its functional genomic basis in reef‐building corals (Orbicella faveolata). Mol. Ecol. 28, 2238–2253 (2019).
    Google Scholar 
    Ainsworth, T. D. et al. Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352, 338–342 (2016).CAS 

    Google Scholar 
    Harrison, H. B., Bode, M., Williamson, D. H., Berumen, M. L. & Jones, G. P. A connectivity portfolio effect stabilizes marine reserve performance. Proc. Natl Acad. Sci. 117, 25595–25600 (2020).CAS 

    Google Scholar 
    Leeuwenburgh, O. & Stammer, D. The Effect of Ocean Currents on Sea Surface Temperature Anomalies. J. Phys. Oceanogr. 31, 2340–2358 (2001).
    Google Scholar 
    Box, G. E., Jenkins, G. M. & Reinsel, G. C. Time series analysis: forecasting and control. (Wiley, 2011).Falasca, F. & Bracco, A. Exploring the tropical Pacific manifold in models and observations. Phys. Rev. X 12, 021054 (2022).CAS 

    Google Scholar 
    NOAA (National Oceanic and Atmospheric Administration), (2019a). Nino regions. https://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/nino_regions.shtml.NOAA (National Oceanic and Atmospheric Administration), (2019b). Cold and warm episodes by season. https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php.Baird, A. et al. Coral Spawning Database. 10552719 Bytes https://doi.org/10.25405/DATA.NCL.13082333.V1 (2020).UNEP-WCMC, WorldFish Centre, WRI, TNC (2021). Global distribution of warm-water coral reefs, compiled from multiple sources including the Millennium Coral Reef Mapping Project. Version 4.1. Includes contributions from IMaRS-USF and IRD (2005), IMaRS-USF (2005) and Spalding et al. (2001). Cambridge (UK): UN Environment World Conservation Monitoring Centre. Data https://doi.org/10.34892/t2wk-5t34.IMaRS-USF, IRD (Institut de Recherche pour le Developpement) (2005). Millennium Coral Reef Mapping Project. Validated maps. Cambridge (UK): UNEP World Conservation Monitoring Centre.IMaRS-USF (Institute for Marine Remote Sensing-University of South Florida) (2005). Millennium Coral Reef Mapping Project. Unvalidated maps. These maps are unendorsed by IRD, but were further interpreted by UNEP World Conservation Monitoring Centre. Cambridge (UK): UNEP World Conservation Monitoring Centre.Spalding, M., Ravilious, C. & Green, E. World atlas of coral reefs. Choice Rev. Online. 39, 39-2540–39–2540 (2002).
    Google Scholar  More

  • in

    Varied response of carbon dioxide emissions to warming in oxic, anoxic and transitional soil layers in a drained peatland

    Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, L13402 (2010).
    Google Scholar 
    Joosten, H., Tapio-BiströmM, L. & Susanna, T. Peatlands: guidance for climate change mitigation through conservation, rehabilitation and sustainable use. Food and Agriculture Organization of the United Nations and Wetlands International. FAO (2012).IUCN. Issues brief: peatlands and climate change. www.icun.org (2017).Joosten, H. Peatlands, Climate Change Mitigation and Biodiversity Conservation. An Issue Brief on the Importance of Peatlands for Carbon and Biodiversity Conservation and the Role of Drained Peatlands as Greenhouse Gas Emission Hotspots (Nordic Council of Ministers, 2015).Moore, T. R. & Knowles, R. The influence of water table levels on methane and carbon dioxide emissions from peatland soils. Can. J. Soil Sci. 69, 33–38 (1989).CAS 

    Google Scholar 
    Tfaily, M. M. et al. Organic matter transformation in the peat column at Marcell Experimental Forest: humification and vertical stratification. J. Geophys. Res. Biogeosci. 119, 661–675 (2014).CAS 

    Google Scholar 
    Clymo, R. S. & Bryant, C. L. Diffusion and mass flow of dissolved carbon dioxide, methane, and dissolved organic carbon in a 7-m deep raised peat bog. Geochim. Cosmochim. Acta 72, 2048–2066 (2008).CAS 

    Google Scholar 
    Clymo, R. S. The limits to peat bog growth. Philos. Trans. R. Soc. B 303, 605–654 (1984).
    Google Scholar 
    Qin, S. et al. Temperature sensitivity of SOM decomposition governed by aggregate protection and microbial communities. Sci. Adv. 5, eaau1218. 1211–1219 (2019).
    Google Scholar 
    Dorrepaal, E. et al. Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460, 616–619 (2009).CAS 

    Google Scholar 
    Luo, Z. K., Wang, G. C. & Wang, E. L. Global subsoil organic carbon turnover times dominantly controlled by soil properties rather than climate. Nat. Commun. 10, 3688 (2019).
    Google Scholar 
    Wilson, R. M. et al. Stability of peatland carbon to rising temperatures. Nat. Commun. 7, 13723 (2016).CAS 

    Google Scholar 
    Sihi, D., Inglett, P. W. & Inglett, K. S. Carbon quality and nutrient status drive the temperature sensitivity of organic matter decomposition in subtropical peat soils. Biogeochemistry 131, 103–119 (2016).CAS 

    Google Scholar 
    Wang, Q., Liu, S. & Tian, P. Carbon quality and soil microbial property control the latitudinal pattern in temperature sensitivity of soil microbial respiration across Chinese forest ecosystems. Glob. Chang. Biol. 24, 2841–2849 (2018).
    Google Scholar 
    Cheng, L. et al. Warming enhances old organic carbon decomposition through altering functional microbial communities. ISME J. 11, 1825–1835 (2017).
    Google Scholar 
    Luan, J., Wu, J., Liu, S., Roulet, N. & Wang, M. Soil nitrogen determines greenhouse gas emissions from northern peatlands under concurrent warming and vegetation shifting. Commun. Biol. 2, 132 (2019).
    Google Scholar 
    Meyer, N. et al. Nitrogen and phosphorus supply controls soil organic carbon mineralization in tropical topsoil and subsoil. Soil Biol. Biochem. 119, 152–161 (2018).CAS 

    Google Scholar 
    Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007).CAS 

    Google Scholar 
    Moni, C. et al. Temperature response of soil organic matter mineralisation in arctic soil profiles. Soil Biol. Biochem. 88, 236–246 (2015).CAS 

    Google Scholar 
    Xu, X., Sherry, R. A., Niu, S., Zhou, J. & Luo, Y. Long-term experimental warming decreased labile soil organic carbon in a tallgrass prairie. Plant Soil 361, 307–315 (2012).CAS 

    Google Scholar 
    Broder, T., Blodau, C., Biester, H. & Knorr, K. H. Peat decomposition records in three pristine ombrotrophic bogs in southern Patagonia. Biogeosciences 9, 1479–1491 (2012).CAS 

    Google Scholar 
    Adamczyk, M., Perez-Mon, C., Gunz, S. & Frey, B. Strong shifts in microbial community structure are associated with increased litter input rather than temperature in High Arctic soils. Soil Biol. Biochem. 151, 108054 (2020).CAS 

    Google Scholar 
    Hug, L. A. et al. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1, 22 (2013).
    Google Scholar 
    Yun, J. L., Ju, Y. W., Deng, Y. C. & Zhang, H. X. Bacterial community structure in two permafrost wetlands on the Tibetan Plateau and Sanjiang Plain, China. Microb. Ecol. 68, 360–369 (2014).
    Google Scholar 
    Zhong, Q. et al. Water table drawdown shapes the depth-dependent variations in prokaryotic diversity and structure in Zoige peatlands. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fix049 (2017).Article 

    Google Scholar 
    Karhu, K. et al. Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513, 81–84 (2014).CAS 

    Google Scholar 
    Thiessen, S., Gleixner, G., Wutzler, T. & Reichstein, M. Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass – An incubation study. Soil Biol. Biochem. 57, 739–748 (2013).CAS 

    Google Scholar 
    Walker, T. W. N. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Chang. 8, 885–899 (2018).CAS 

    Google Scholar 
    Dungait, J. A. J., Hopkins, D. W., Gregory, A. S. & Whitmore, A. P. Soil organic matter turnover is governed by accessibility not recalcitrance. Glob. Chang. Biol. 18, 1781–1796 (2012).
    Google Scholar 
    Conant, R. T. et al. Temperature and soil organic matter decomposition rates – synthesis of current knowledge and a way forward. Global Chang. Biol. 17, 3392–3404 (2011).
    Google Scholar 
    Hietz, P. et al. Long-term change in the nitrogen cycle of tropical forests. Science 4, 334 (2011).
    Google Scholar 
    Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Agren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).CAS 

    Google Scholar 
    Sistla, S. A., Asao, S. & Schimel, J. P. Detecting microbial N-limitation in tussock tundra soil: Implications for Arctic soil organic carbon cycling. Soil Biol. Biochem. 55, 78–84 (2012).CAS 

    Google Scholar 
    Chen, L. et al. Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency. Nat. Commun. 9, 3951 (2018).
    Google Scholar 
    Soong, J. L. et al. Five years of whole-soil warming led to loss of subsoil carbon stocks and increased CO2 efflux. Sci. Adv. 7, eabd1343 (2021).Chen, L. et al. Determinants of carbon release from the active layer and permafrost deposits on the Tibetan Plateau. Nat. Commun. 7, 13046 (2016).CAS 

    Google Scholar 
    Girkin, N. T. et al. Interactions between labile carbon, temperature and land use regulate carbon dioxide and methane production in tropical peat. Biogeochemistry 147, 87–97 (2019).
    Google Scholar 
    Swails, E. et al. Will CO2 emissions from drained tropical peatlands decline over time? Links between soil organic matter quality, nutrients, and C mineralization rates. Ecosystems 21, 868–885 (2017).
    Google Scholar 
    Ismawi, S., Gandaseca, S. & Ahmed, O. Effects of deforestation on soil major macro-nutrient and other selected chemical properties of secondary tropical peat swamp forest. Int. J. Phys. Sci. 7, 2225–2228 (2012).CAS 

    Google Scholar 
    Kimura, S., Melling, L. & Goh, K. Influence of soil aggregate size on greenhouse gas emission and uptake rate from tropical peat soil in forest and different oil palm development years. Geoderma 185, 1–5 (2012).
    Google Scholar 
    Takakai, F. et al. Effects of agricultural land-use change and forest fire on N2O emission from tropical peatlands, Central Kalimantan, Indonesia. Soil Sci. Plant Nutr. 52, 662–674 (2006).CAS 

    Google Scholar 
    Knoblauch, C., Beer, C., Sosnin, A., Wagner, D. & Pfeiffer, E. M. Predicting long-term carbon mineralization and trace gas production from thawing permafrost of Northeast Siberia. Glob. Chang. Biol. 19, 1160–1172 (2013).
    Google Scholar 
    Treat, C. C. et al. Temperature and peat type control CO2 and CH4 production in Alaskan permafrost peats. Glob. Chang. Biol. 20, 2674–2686 (2014).CAS 

    Google Scholar 
    Hobbie, S. E., Schimel, J. P., Trumbore, S. E. & Randerson, J. Controls over carbon storage and tureover in high-latitude soils. Glob. Chang. Biol. 6, 196–210 (2000).
    Google Scholar 
    Keller, J. K., Bauers, A. K., Bridgham, S. D., Kellogg, L. E. & Iversen, C. M. Nutrient control of microbial carbon cycling along an ombrotrophic-minerotrophic peatland gradient. J. Geophys. Res. https://doi.org/10.1029/2005jg000152 (2006).Chen, H. et al. A historical overview about basic issues and studies of mires (in Chinese). Sci. Sin. 51, 15–26 (2020).
    Google Scholar 
    Ridl, J. et al. Plants rather than mineral fertilization shape microbial community structure and functional potential in legacy contaminated soil. Front. Microbiol. 7, 1–10 (2016).
    Google Scholar 
    Kane, E. S. et al. Response of anaerobic carbon cycling to water table manipulation in an Alaskan rich fen. Soil Biol. Biochem. 58, 50–60 (2013).CAS 

    Google Scholar 
    Carrell, A. A. et al. Experimental warming alters the community composition, diversity, and N2 fixation activity of peat moss (Sphagnum fallax) microbiomes. Glob. Chang. Biol. 25, 2993–3004 (2019).
    Google Scholar 
    Lamit, L. J. et al. Patterns and drivers of fungal community depth stratification in Sphagnum peat. FEMS Microbiol. Ecol. 93, fix082 (2017).
    Google Scholar 
    Harrison, R. B., Footen, P. W. & Strahm, B. D. Deep soil horizons: contribution and importance to soil carbon pools and in assessing whole-ecosystem response to management and global change. Forest Sci. 57, 67–76 (2011).
    Google Scholar 
    Krüger, J. P., Leifeld, J., Glatzel, S., Szidat, S. & Alewell, C. Biogeochemical indicators of peatland degradation – a case study of a temperate bog in northern Germany. Biogeosciences 12, 2861–2871 (2015).
    Google Scholar 
    Franzén, L. G. Increased decomposition of subsurface peat in Swedish raised bogs: are temperate peatlands still net sinks of carbon? Mires Peat 1, 3 (2006).
    Google Scholar 
    Eilers, K. G., Lauber, C. L., Knight, R. & Fierer, N. Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol. Biochem. 42, 896–903 (2010).CAS 

    Google Scholar 
    de Graaff, M. A., Jastrow, J. D., Gillette, S., Johns, A. & Wullschleger, S. D. Differential priming of soil carbon driven by soil depth and root impacts on carbon availability. Soil Biol. Biochem. 69, 147–156 (2014).
    Google Scholar 
    Peay, K. G., Kennedy, P. G. & Brun, T. D. Fungal community ecology: a hybrid beast with a molecular master. BioScience 58, 799–810 (2008).
    Google Scholar 
    Gillabel, J., Cebrian, B., Six, J. & Merckx, R. Experimental evidence for the attenuating effect of SOM protection on temperature sensitivity of SOM decomposition. Glob. Chang. Biol. 16, 2789–2798 (2010).
    Google Scholar 
    Pries, C. E. H., Castanha, C., Porras, R. C. & Torn, M. S. The whole-soil carbon flux in response to warming. Science 355, 1420–1423 (2017).
    Google Scholar 
    Hicks Pries, C. E., Schuur, E. A. G. & Crummer, K. G. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using δ13C and ∆14C. Global Chang. Biol. 19, 649–661 (2013).
    Google Scholar 
    Tian, J. et al. Aerobic environments in combination with substrate additions to soil significantly reshape depth-dependent microbial distribution patterns in Zoige peatlands, China. Appl.Soil Ecol. 170, 104252 (2022).
    Google Scholar 
    Feng, W. et al. Enhanced decomposition of stable soil organic carbon and microbial catabolic potentials by long-term field warming. Glob. Chang. Biol. 00, 1–12 (2017).
    Google Scholar 
    Feng, W. et al. Methodological uncertainty in estimating carbon turnover times of soil fractions. Soil Biol. Biochem. 100, 118–124 (2016).CAS 

    Google Scholar 
    Liang, J. et al. Methods for estimating temperature sensitivity of soil organic matter based on incubation data: A comparative evaluation. Soil Biol. Biochem. 80, 127–135 (2015).CAS 

    Google Scholar 
    Cai, A., Feng, W., Zhang, W. & Xu, M. Climate, soil texture, and soil types affect the contributions of fine-fraction-stabilized carbon to total soil organic carbon in different land uses across China. J. Environ. Manag. 172, 2–9 (2016).CAS 

    Google Scholar 
    Liu, L. et al. Response of anaerobic mineralization of different depths peat carbon to warming on Zoige plateau. Geoderma 337, 1218–1226 (2019).CAS 

    Google Scholar 
    Waldrop, M. et al. Molecular investigations into a globally important carbon pool: permafrost protected carbon in Alaskan soils. Glob. Chang. Biol. 16, 2543–2554 (2014).
    Google Scholar 
    Mooshammer, M., Wanek, W., Zechmeister-Boltenstern, S. & Richter, A. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front. Microbiol. 5, 22 (2014).
    Google Scholar 
    Blagodatskaya, E. & Kuzyakov, Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol. Fertil. Soils 45, 115–131 (2008).
    Google Scholar 
    Chen, H. et al. The carbon stock of alpine peatlands on the Qinghai–Tibetan Plateau during the Holocene and their future fate. Quat. Sci. Rev. 95, 151–158 (2014).
    Google Scholar 
    Sun, G. A study on the mineral formation law, classifictation and reserves of the peat in the Rouergai Plateau. J. Nat. Res. 7, 334–345 (1992).
    Google Scholar 
    Liu, L. et al. Responses of peat carbon at different depths to simulated warming and oxidizing. Sci. Total Environ. 548-549, 429–440 (2016).CAS 

    Google Scholar 
    Liu, L. et al. Water table drawdown reshapes soil physicochemical characteristics in Zoige peatlands. Catena 170, 119–128 (2018).CAS 

    Google Scholar 
    Liu, L. et al. Carbon stock stability in drained peatland after simulated plant carbon addition: Strong dependence on deeper soil. Sci. Total Environ. 848, 157539 (2022).CAS 

    Google Scholar 
    Yang, Z. et al. Soil properties and species composition under different grazing intensity in an alpine meadow on the eastern Tibetan Plateau, China. Environ. Monit. Assess 188, 678 (2016).
    Google Scholar 
    Simpson, M. J. & Simpson, A. J. The chemical ecology of soil organic matter molecular constituents. J. Chem. Ecol. 38, 768–784 (2012).CAS 

    Google Scholar 
    Lalonde, K., Mucci, A., Ouellet, A. & Gelinas, Y. Preservation of organic matter in sediments promoted by iron. Nature 483, 198–200 (2012).CAS 

    Google Scholar 
    Deforest, J. L., zak, D. R., Pregitzer, K. S. & Burtonf, A. J. Atomspheric nitrate deposition and enhanced dissolved organic carbon leaching: test of a potential mechanism. Soil Sci. Soc. Am. J. 69, 1233–1237 (2005).CAS 

    Google Scholar 
    Schadel, C. et al. Circumpolar assessment of permafrost C quality and its vulnerability over time using long-term incubation data. Glob. Chang. Biol. 20, 641–652 (2014).
    Google Scholar 
    Bell, M. & Lawrence, D. Soil carbon sequestration – myths and mysteries. Department of Primary Industries and Fisheries, Queensland Government (2009).Schadel, C., Luo, Y., David Evans, R., Fei, S. & Schaeffer, S. M. Separating soil CO2 efflux into C-pool-specific decay rates via inverse analysis of soil incubation data. Oecologia 171, 721–732 (2013).
    Google Scholar 
    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).CAS 

    Google Scholar 
    Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).CAS 

    Google Scholar 
    White, T. J. in PCR-Protocols: A Guide to Methods and Applications (Academic Press, 1990).Bell, C. et al. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J. Vis. Exp. 81, e50961 (2013).
    Google Scholar 
    DeForest, J. L. The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol. Biochem. 41, 1180–1186 (2009).CAS 

    Google Scholar 
    Amundson, R. The carbon budget in soils. Annu. Rev. Earth Planet. Sci. 29, 535–562 (2001).CAS 

    Google Scholar 
    Trumbore, S. E. Potential responses of soil organic carbon to global environmental change. Proc. Natl Acad. Sci. USA 94, 8284–8291 (1997).CAS 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org (2017).Oksanen, J. et al. vegan: community ecology package. R Packag version 24-1 (2016).Asshauer, K. P., Wemheuer, B., Daniel, R. & Meinicke, P. Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31, 2882–2884 (2015).CAS 

    Google Scholar  More