More stories

  • in

    Governance modes

    Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard
    Provided by the Springer Nature SharedIt content-sharing initiative More

  • in

    Carbon impacts

    Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard
    Provided by the Springer Nature SharedIt content-sharing initiative More

  • in

    Original karst tiankeng with underground virgin forest as an inaccessible refugia originated from a degraded surface flora in Yunnan, China

    Zhu, X. China’s karst tiankeng and its value for science and tourism. Sci. Technol. Rev. 19, 60–63 (2001).
    Google Scholar 
    Zhu, X. et al. A brift study on karst tiankeng. Carsol. Sin. 22, 51–65 (2003).
    Google Scholar 
    Zhu, X. & Waltham, T. Tiankeng: Definition and description. Cave Karst Sci. 32, 75–79 (2005).
    Google Scholar 
    Zhu, X. & Chen, W. Tiankengs in the karst of China. Cave Karst Sci. 32, 55–56 (2005).
    Google Scholar 
    Shui, W., Chen, Y., Wang, Y., Su, Z. & Zhang, S. Origination, study progress and prospect of karst tiankeng research in China. Acta Geogr. Sin. 70, 431–446 (2015).
    Google Scholar 
    Alexander, K. Cave un-roofing as a large-scale geomorphic process. Carsol. Sin. 4, 1–11 (2006).
    Google Scholar 
    Palmer, A. & Palmer, M. Hydraulic processes in the origin of tiankengs. Speleogenesis Evol. Karst Aquifers 4, 8 (2006).
    Google Scholar 
    Waltham, T. Collapse processes at the tiankengs of Xingwen. Cave Karst Sci. 32, 107–110 (2005).
    Google Scholar 
    White, W. & White, E. Size scales for closed depression landforms: The place of tiankengs. Cave Karst Sci. 32, 111–118 (2005).
    Google Scholar 
    Chen, W., Zhu, X., Zhu, D. & Ma, Z. Karst geological relics and development of Xiaozhai Tiankeng and Tianjinxia Fissure Gorge, Fengjie, Chongqing. J. Mountain Sci. 22, 22–29 (2004).CAS 

    Google Scholar 
    Yue, Y., Wang, K., Zhang, W., Chen, H. & Wang, M. Relationships between soil and environment in Peak-Cluster Depression areas of karst region based on canonical correspondence analysis. Environ. Sci. 29, 1400–1405 (2008).
    Google Scholar 
    Huang, B., Cai, W., Xue, Y. & Zhu, X. Research on tourism resource characteristics of tiankeng group in Dashiwei, Guangxi. Geogr. Geo-Inf. Sci. 20, 109–112 (2004).CAS 

    Google Scholar 
    Zhu, X. Discovery of erosional tiankeng in Houping, Wulong and its value of science and tourism. Carsol. Sin. 2, 93–98 (2006).
    Google Scholar 
    Yuan, D. The development of modern karstology in China. Geol. Rev. 52, 733–736 (2006).CAS 

    Google Scholar 
    Gunn, J. Turloughs and tiankengs: Distinctive doline forms. Cave Karst Sci. 32, 83–84 (2005).
    Google Scholar 
    Klimchou, A. Cave un-roofing as a large-scale geomorphic process. Cave Karst Sci. 32, 93–98 (2005).
    Google Scholar 
    Zhu, X., Chen, W. & Erin, L. Wulong karst systems and as an indicator of local tectonic uplift. Carsol. Sin. 26, 119–125 (2007).
    Google Scholar 
    Shui, W. & Wang, X. Geological expedition and analysis on formation and evolvement of erosive Karst Tiankeng: A case study of Xingwen World Geopark. Adv. Mater. Res. 250–253, 2002–2006 (2011).Article 

    Google Scholar 
    Su, S., Huang, K. & Ma, B. Diversity study on pteridophyte flora in the area of Dashiwei Tiankeng group of Leye County. Hubei Agric. Sci. 51, 948–950 (2012).
    Google Scholar 
    Huang, K. & Su, S. Resource investigation and application research of pteridophyte flora resource in the area of Dashiwei Tiankeng Group. Anhui Agric. Sci. Bull. 21, 74–80 (2015).CAS 

    Google Scholar 
    Su, Y., Xue, Y., Fan, B., Mo, F. & Feng, H. Plant community structure and species diversity in Liuxing tiankeng of Guangxi. Acta Botan. Boreali-Occiden. Sin. 36, 2300–2306 (2016).
    Google Scholar 
    Li, W., Xiang, Y., Du, Y. & Wu, X. Underground forest communities in Zhanyi, Yunnan Province. For. Sci. Technol. 20–25 (2001).Jian, X. et al. Interspecific relationships of grassland plant community’s dominant species in moderate-degraded tiankeng of Yunnan, China. Chin. J. Appl. Ecol. 29, 1–14. https://doi.org/10.13287/j.1001 (2018).Article 

    Google Scholar 
    Chen, W., Zhu, D. & Zhu, X. Characteristics and evaluation of karst landscape in tiankeng-difeng scenery site, Fengjie, Chongqing. Geogr. Geo-Inf. Sci. 20, 80–83 (2004).CAS 

    Google Scholar 
    Wang, J. & Guo, C. Comparison between the positive and negative topographic ecosystem in karst mountainous areas and its bearing capability. Guizhou Agric. Sci. 35, 85–87 (2007).MathSciNet 

    Google Scholar 
    Tony, W. Tiankengs of the world, outside China. Speleogenesis Evol. Karst Aquifers 4, 1–12 (2006).
    Google Scholar 
    Su, Y., Tang, Q., Mo, F. & Xue, Y. Karst tiankengs as refugia for indigenous tree flora amidst a degraded landscape in southwestern China. Sci. Rep. 7, 1–10 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    Bátori, Z. et al. A comparison of the vegetation of forested and non-forested solution dolines in Hungary: A preliminary study. Biologia 69, 1339–1348 (2014).Article 
    CAS 

    Google Scholar 
    Bátori, Z. et al. The conservation value of karst dolines for vascular plants in woodland habitats of Hungary: Refugia and climate change. Int. J. Speleol. 43, 15–26 (2014).Article 

    Google Scholar 
    Bátori, Z. et al. Importance of karst sinkholes in preserving relict, mountain, and wet-woodland plant species under sub-Mediterranean climate: A case study from southern Hungary. J. Cave Karst Stud. Natl. Speleol. Soc. Bull. 74, 127–134 (2012).Article 

    Google Scholar 
    Bátori, Z. et al. Large-and small-scale environmental factors drive distributions of cool-adapted plants in karstic microrefugia. Ann. Bot. 119, 301–309 (2017).PubMed 
    Article 

    Google Scholar 
    Vilisics, F. et al. Small scale gradient effects on isopods (Crustacea: Oniscidea) in karstic sinkholes. Biologia 66, 499–505 (2011).Article 

    Google Scholar 
    Dolinar, B. & Vreš, B. Pregled flore Mišje doline in zgornjega porečja Rašice (Dolenjska, Slovenija). Hladnikia 30, 3–37 (2012).
    Google Scholar 
    Raschmanová, N., Miklisová, D., Ľubomír, K. & Šustr, V. Community composition and cold tolerance of soil Collembola in a collapse karst doline with strong microclimate inversion. Biologia 70, 802–811 (2016).Article 

    Google Scholar 
    Macarthur, R. & Wilson, E. The Theory of Island Biogeography (Princeton University Press, 1967).
    Google Scholar 
    Kreft, H. & Jetz, W. Global patterns and determinants of vascular plant diversity. Proc. Natl. Acad. Sci. U. S. A. 104, 5925 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhou, F. & Yu, S. Study on the plant diversity of island-like habitats in Karst Mountain Areas. Guizhou For. Sci. Technol. 40, 18–22 (2012).CAS 

    Google Scholar 
    Hu, F., Lou, Q. & Sun, Y. Community composition and species diversity of different island habitat on Karst Mountainous in Central Guizhou. Guizhou Sci. 29, 23–28 (2011).
    Google Scholar 
    Culver, D. Karst environment. Z. Geomorphol. Suppl. 60, 103–117 (2016).Article 

    Google Scholar 
    Daily, G. Restoring value to the world’s degraded lands. Science 269, 350–354 (1995).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Bartgis, R. The endangered sedge Scirpus ancistrochaetus and the flora of sinkhole ponds in Maryland and West Virginia. Castanea 57, 46–51 (1992).
    Google Scholar 
    Yu, X., Li, Y. & Ma, Z. A preliminary study on flora diversity of karst microhabitat in Shilin Park, Yunnan, China. J. Mountain Sci. 25, 438–447 (2007).
    Google Scholar 
    Dang, G., Feng, H., Tang, Q., Mo, F. & Xue, Y. New recorded species in Guangxi, China. J. Guangxi Normal Univ. (Nat. Sci. Edit.) 34, 147–150 (2016).
    Google Scholar 
    Eigenbrod, F., Gonzalez, P., Dash, J. & Steyl, I. Vulnerability of ecosystems to climate change moderated by habitat intactness. Glob. Change Biol. 21, 275–286 (2015).ADS 
    Article 

    Google Scholar 
    Cornell, H. & Lawton, J. Species interactions, local and regional processes, and limits to the richness of ecological communities: A theoretical perspective. J. Anim. Ecol. 61, 1–12 (1992).Article 

    Google Scholar 
    Helmus, M., Mahler, D. & Losos, J. Island biogeography of the Anthropocene. Nature 513, 543–546 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Yuan, T., Zhang, H., Ou, Z. & Tan, Y. Effects of topography on the diversity and distribution pattern of ground plants in karst montane forests in Southwest Guangxi, China. Chin. J. Appl. Ecol. 25, 2803–2810 (2014).
    Google Scholar 
    Wen, L. et al. The succession characteristics and its driving mechanisms of plant community in karst region, Southwest China. Acta Ecol. Sin. 35, 5822–5833 (2015).Article 

    Google Scholar 
    Zhang, Z., Hu, G. & Ni, J. Erratum to: Effects of topographical and edaphic factors on the distribution of plant communities in two subtropical Karst forests, Southwestern China. J. Mt. Sci. 10, 337–338 (2013).Article 

    Google Scholar 
    Du, H. et al. Plant community characteristics and its coupling relationships with soil in depressions between karst hills, North Guangxi, China. Chin. J. Plant Ecol. 37, 197–208 (2013).Article 

    Google Scholar 
    Liu, S., Zhang, B., Yang, Q., Hu, C. & Su, C. Species composition and diversity of plant communities in Xiaoyanwan Garden of Xingwen Karst National Geopark, Sichuan Province. Subtrop. Plant Sci. 38, 37–40 (2009).
    Google Scholar 
    Tan, C. The preliminary discussion about Haifeng’s wetland ecosystem. For. Sci. Technol. 1–8 (2002).Ma, K. & Liu, Y. Measurement of biodiversity: The measurement of α diversity. Chin. Biodivers. 2, 231–239 (1995).
    Google Scholar 
    Pielou, E. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144 (1966).ADS 
    Article 

    Google Scholar 
    Simpson, E. Measurement of diversity. Nature 163, 688 (1949).ADS 
    MATH 
    Article 

    Google Scholar  More

  • in

    Low level of anthropization linked to harsh vertebrate biodiversity declines in Amazonia

    Study areaThe study was conducted on two rivers in north-eastern Amazonia sensu lato, including the Guiana Shield and the Amazon River drainage (Fig. 2). The climate of the entire study area is homogeneous and the region is covered by dense, uniform lowland primary rainforest51. The altitude is in the range of 0–860 m a.s.l. The regional climate is equatorial, and the annual rainfall ranges from 3600 mm in the northeast to 2000 mm in the southwest. The Maroni River is 612 km long from its source to its estuary, and its watershed covers a surface of >68,000 km2 in Suriname and French Guiana. The Oyapock River (length, 404 km; area, 26,800 km2) is located in the state of Amapa in Brazil and in French Guiana.The foregoing river basins host nearly 400 freshwater fish species and more than 180 mammal species52,53. Most of the mammal species have a large distribution range, covering the entire study area53. The fish species have a less homogeneous distribution and a distinct upstream-downstream composition gradient54,55. Here, only large rivers were considered and most fish species were widespread over the whole study area. As habitat availability increases with river size, species richness is expected to increase upstream to dowsntream31,32. The Oyapock and Maroni river basins are among the last remaining wilderness areas on Earth17. Nevertheless, ecological disturbances are increasing there because of a growing human population and the development of small-scale gold mining activity. These disturbances have caused limited but diffuse deforestation23,56. The deforested areas currently comprise 0.67% of all Maroni and Oyapock catchments.SamplingEnvironmental DNA (eDNA) was collected from water samples at 74 locations (hereafter, sites) along the main channel and the large tributaries of the Maroni and Oyapock rivers (Fig. 2). Thirty-seven sites were sampled at each river basin. The minimum and maximum distances between adjacent sites were 1.07 and 50.20 km, respectively. The mean and median distances between adjacent sites were 10.18 and 9.14 km, respectively, and the standard deviation (SD) was 7.79 km. The sites were located from sea level to 157 m a.s.l. At all sites, the river was wider than 20 m and deeper than 1 m (Strahler orders 4–8; Supplementary Fig. 5). The physicochemical properties of the water slightly varied among sites. The temperature, pH, and conductivity were in the ranges of 28.4–33.2 °C, 6.5–7.6, and 16.9–54.6 µS/cm, respectively, at all sites except two estuarine locations where the conductivity was relatively high because of seawater incursion (Supplementary Data 2).The eDNA samples were collected during the dry seasons (October–November) of 2017 and 2018 for Maroni and Oyapock, respectively. At both rivers, the sites were sequentially sampled from downstream to upstream at a rate of 1–4 sites per day depending on the distance and travel time between sites. Following the protocol of ref. 45, we collected the eDNA by filtering two replicates of 34 L of water per site. A peristaltic pump (Vampire Sampler; Buerkle GmbH, Bad Bellingen, Germany) and single-use tubing were used to pump the water into a single-use filtration capsule (VigiDNA, pore size 0.45 μm; filtration surface 500 cm2, SPYGEN, Bourget-du-Lac, France). The tubing input was placed a few centimetres below the water surface in zones with high water flow as recommended by Cilleros et al.43. Sampling was performed in turbulent areas with rapid hydromorphologic units to ensure optimal eDNA homogeneity throughout the water column. To avoid eDNA cross-contamination among sites, the operator remained on emerging rocks downstream from the filtration area. At the end of filtration, the capsule was voided, filled with 80 mL CL1 preservation buffer (SPYGEN), and stored in the dark up to one month before the DNA extraction. No permits were required for the eDNA sampling and the access to all sites was legally permitted. The study complies with access and benefit permits ABSCH-IRCC-FR-246820-1 and ABSCH-IRCC-FR-245902-1, authorizing collection, transport and analysis of all environmental DNA samples used in this study.Laboratory procedures and bioinformatic analysesFor the DNA extraction, each filtration capsule was agitated on an S50 shaker (Ingenieurbüro CAT M. Zipperer GmbH, Ballrechten-Dottingen, Germany) at 800 rpm for 15 min, decanted into a 50 mL tube, and centrifuged at 15,000 × g and 6 °C for 15 min. The supernatant was removed with a sterile pipette, leaving 15 mL of liquid at the bottom of the tube. Subsequently, 33 mL of ethanol and 1.5 mL of 3 M sodium acetate were added to each 50 mL tube, and the mixtures were stored at −20 °C for at least one night. The tubes were then centrifuged at 15,000 × g and 6 °C for 15 min, and the supernatants were discarded. Then, 720 µL of ATL buffer from a DNeasy Blood & Tissue Extraction Kit (Qiagen, Hilden, Germany) was added. The tubes were vortexed, and the supernatants were transferred to 2 mL tubes containing 20 µL proteinase K. The tubes were then incubated at 56 °C for 2 h. DNA extraction was performed using a NucleoSpin Soil kit (Macherey-Nagel GmbH, Düren, Germany) starting from step six of the manufacturer’s instructions. Elution was performed by adding 100 µL of SE buffer twice. After the DNA extraction, the samples were tested for inhibition by qPCR following the protocol in ref. 57. Briefly, quantitative PCR was performed in duplicate for each sample. If at least one of the replicates showed a different Ct (Cycle threshold) than expected (at least 2 Cts), the sample was considered inhibited and diluted 5-fold before the amplification.For the fish, the “teleo” primers58 (forward: 3ʹ-ACACCGCCCGTCACTCT-5ʹ; reverse: 3ʹ-CTTCCGGTACACTTACCATG-5ʹ) were used as they efficiently discriminated local fish species43,45. For the mammals, the 12S-V5 vertebrate marker59 (forward: 3ʹ-TAGAACAGGCTCCTCTAG-5ʹ; reverse: 3ʹ-TTAGATACCCCACTATGC-5ʹ) was used as it also effectively distinguishes local mammal species44,60. The DNA amplifications were performed in a final volume of 25 μL containing 1 U AmpliTaq Gold DNA Polymerase (Applied Biosystems, Foster City, CA, USA), 0.2 μM of each primer, 10 mM Tris-HCl, 50 mM KCl, 2.5 mM MgCl2, 0.2 mM of each dNTP, and 3 μL DNA template. Human blocking primer was added to the mixture for the “teleo”58 (5′-ACCCTCCTCAAGTATACTTCAAAGGAC-C3-3′) and the “12S-V5” primers61 (5′-CTATGCTTAGCCCTAAACCTCAACAGTTAAATCAACAAAACTGCT-C3-3′) at final concentrations of 4 μM and 0.2 μg/μL bovine serum albumin (BSA; Roche Diagnostics, Basel, Switzerland). Twelve PCR replicates were performed per field sample. The forward and reverse primer tags were identical within each PCR replicate. The PCR mixture was denatured at 95 °C for 10 min, followed by 50 cycles of 30 s at 95 °C, 30 s at 55 °C for the “teleo” primers and 50 °C for the 12S-V5 primers, 1 min at 72 °C, and a final elongation step at 72 °C for 7 min. This step was conducted in a dedicated room for DNA amplification that is kept under negative air pressure and is physically separated from the DNA extraction rooms maintained under positive air pressure. The purified PCR products were pooled in equal volumes to achieve an expected sequencing depth of 500,000 reads per sample before DNA library preparation.For the fish analyses, 10 libraries were prepared using a PCR-free library protocol (https://www.fasteris.com/metafast) at Fasteris, Geneva, Switzerland. Four libraries were sequenced on an Illumina HiSeq 2500 (2 × 125 bp) (Illumina, San Diego, CA, USA) with a HiSeq SBS Kit v4 (Illumina), three were sequenced on a MiSeq (2 × 125 bp) (Illumina) with a MiSeq Flow Cell Kit Version3 (Illumina), and three libraries were sequenced on a NextSeq (2 × 150 bp + 8) (Illumina) with a NextSeq Mid kit (Illumina). The libraries run on the NextSeq were equally distributed in four lanes. Sequencing was performed according to the manufacturer’s instructions at Fasteris. For the mammal analyses, eight libraries were prepared using a PCR-free library protocol (https://www.fasteris.com/metafast) at Fasteris. Two libraries were sequenced on an Illumina HiSeq 2500 (2 × 125 bp) (Illumina) using a HiSeq Rapid Flow Cell v2 and a HiSeq Rapid SBS Kit v2 (Illumina), three libraries were prepared on a MiSeq (2 × 125 bp) (Illumina) with a MiSeq Flow Cell Kit Version3 (Illumina), and three libraries were prepared using a NextSeq (2 × 150 bp + 8) (Illumina) and a NextSeq Mid kit (Illumina). The libraries run on the NextSeq were equally distributed in four lanes. As different sequencing platforms were used (MiSeq and NextSeq for the Maroni and HiSeq 2500 and MiSeq for the Oyapock; Supplementary Fig. 6 and Supplementary Data 3), the possible influences of the platforms on the sequencing results were verified. To this end, we compared the differences in species numbers between the sample replicates assigned to the same platform (accounting for replicate effect only) against those of the sample replicates assigned to different platforms (accounting for replicate and platform effects). As there were more sites with their two replicates sequenced with the same platform than sites with their replicates sequenced with different platforms (see Supplementary Fig. 6), sites with replicates on the same platform were randomly selected for the comparisons. We repeated this procedure 50 times. The number of species between replicates sequenced on the same platform and those sequenced on different platforms did not differ for >98.5% of all fish and mammal samples (Supplementary Fig. 7 and Supplementary Note 2). Similar to these results, a previous study on 16 S rRNA amplicon has shown that the samples were not influenced by the Illumina sequencing platform used62.To monitor for contaminants, 13 negative extraction controls were performed for each of the primers (“teleo” and “12S-V5”); one control was amplified twice. All of them were amplified and sequenced by the same methods as the samples and in parallel to them. Therefore, for the negative extraction controls, 168 amplifications were prepared with the “teleo” primers (13 negative controls; one amplified and sequenced twice) and 156 amplifications with the “12S-V5” primers (13 negative controls). Fourteen negative PCR controls (ultrapure water; 12 replicates) were amplified and sequenced in parallel to the samples. Eight were amplified with the “teleo” primers and six were amplified with the “12S-V05” primers. Thus, for the PCR negative controls, there were 96 amplifications with the “teleo” primers and 72 amplifications with the Vert01 primers. Sequencing information for the controls is shown in Supplementary Data 3c.An updated version of the reference database from ref. 43 was used. There were 265 Guianese species for the fish analyses (ref. 47). The GenBank nucleotide database was consulted, but it contained little information on the Guianese fish species. Most of the sequences were derived from ref. 43. For the mammal analyses, the vertebrate database was built using ecoPCR software63 from the releases 134 and 138 of the European Nucleotide Archive (ENA), for the Maroni and Oyapock river samples, respectively. The two releases were compared, and it was established that the new mammal species added to each version did not originate from French Guiana. Hence, the results were not influenced by the EMBL release number. The relevant metabarcoding fragment was extracted from this database with ecoPCR63 and OBITools64. Therefore, the reference database comprised the local database of French Guianese mammals60, which references 576 specimens from 164 species as well as all available vertebrate species in EMBL.The sequence reads were analyzed with the OBITools package according to the protocol described by Valentini et al.58. Briefly, the forward and reverse reads were assembled with the illuminapairedend programme. The ngsfilter programme was then used to assign the sequences to each sample. A separate dataset was created for each sample by splitting the original dataset into several files with obisplit. Sequences shorter than 20 bp or occurring less than 10 times per sample were discarded. The obiclean program was used to identify amplicon sequence variants (ASVs) that have likely arisen due to PCR or sequencing errors. It uses the information of sequence counts and sequence similarities to classify whether a sequence is a variant (“internal”) of a more abundant (“head”) ASV64. After this step, we matched the ASV with the reference database to obtain the taxonomic assignation for each ASV. Sequences labelled by the obiclean programme as ‘internal’’ and probably corresponding to PCR errors were discarded. The ecotag programme was then used for taxonomic assignment of molecular operational taxonomic units (MOTUs). The taxonomic assignments from ecotag were corrected to avoid overconfidence in assignments. Species-level assignments were validated only for ≥98% sequence identity with the reference database. Sequences below this threshold were discarded.Measuring disturbance intensity using GIS dataIn riverine systems, the disturbances may accumulate because of hydrologic connectivity, which is the downstream transfer of matter and pollutants4. Hence, the upstream sub-basin drainage network was considered to determine the size of the upstream sub-basin affecting local biodiversity (Fig. 1). The sub-basins were delineated by applying a flow accumulation algorithm to the SRTM global 30 m digital elevation model65. Deforestation was measured over 14 upstream spatial extents with radii of 0.5, 1.5, 3, 5, 10, 15, 20, 30, 40, 50, 60, 70, 80, and 90 km for each sampling site. Then, these 14 upstream spatial extents were intersected with the sub-basin drainage network. In addition, mammals and fish can also be affected by disturbances other than those mediated by hydrologic connectivity. Thus, deforestation was also measured upstream and downstream from the eDNA sampling sites using the same foregoing 14 radii.At each sampling site, deforestation intensity was quantified for each of the 14 spatial extents. We summed upstream (only accounting for disturbances mediated by river hydrologic connectivity) or upstream and downstream (not only considering disturbances mediated by hydrologic connectivity) deforested surfaces from Landsat satellite image datasets. Forest loss surfaces were obtained from the Global Forest Change dataset66. The Global Forest Change dataset identifies areas deforested between 2001 and 2017 on a 30 m spatial scale. To incorporate deforested areas prior to 2000, tree canopy cover data for that year were also used. Except for river courses, all pixels with More

  • in

    Revisiting biocrystallization: purine crystalline inclusions are widespread in eukaryotes

    We express our gratitude to Lukáš Falteisek, Richard Dorrell, Jan Petrášek, Stanislav Volsobě, Kateřina Schwarzerová and Jana Krtková for constructive discussions. English has been kindly corrected by William Bourland. Furthermore, we thank to Dovilė Barcytė, William Bourland, Antonio Calado, Dora Čertnerová, Yana Eglit, Ivan Fiala, Martina Hálová, Miroslav Hyliš, Dagmar Jirsová, Petr Kaštánek, Viktorie Kolátková, Alena Kubátová, Alexander Kudryavtsev, Frederik Leliaert, Julius Lukeš, Jan Mach, Joost Mansour, Jan Mourek, Yvonne Němcová, Fabrice Not, Vladimír Scholtz, Alastair Simpson, Pavel Škaloud, Jan Šťastný, Róbert Šuťák, Daria Tashyreva, Dana Savická, Jan Šobotník, Zdeněk Verner, Jan Votýpka for kindly providing cultures and taxonomic identifications. More

  • in

    Indigenous knowledge reveals history of fire-prone California forest

    Controlled fires can be used to reduce the risk of wildfires.Credit: David Hoffmann/Alamy

    Indigenous oral accounts have helped scientists to reconstruct a 3,000-year history of a large fire-prone forest in California. The results suggest that parts of the forest are denser than ever before, and are at risk of severe wildfires1. The research is part of a growing effort to combine Indigenous knowledge with other scientific data to improve understanding of ecosystem histories.Wildfires are a substantial threat to Californian forests. Clarke Knight, a palaeo-ecosystem scientist at the US Geological Survey in Menlo Park, California, and her colleagues wanted to understand how Indigenous communities helped shape the forest by managing this risk in the state’s lush western Klamath Mountains. Specifically, they studied Indigenous peoples’ use of cultural burning — small, controlled fires that keep biomass low and reduce the risk of more widespread burning. The results are published in the Proceedings of the National Academy of Science.“When I was a little kid, my grandmother used to burn around the house,” says Rod Mendes, fire chief for the Yurok Tribe fire department, whose family is part of the Karuk Tribe of northern California. The Karuk and Yurok tribes have called the Klamath Mountains home for thousands of years. “She was just keeping the place clean. Native people probably did some of the first prescribed fire operations in history,” says Mendes.Understanding how Indigenous tribes used fire is essential for managing forests to reduce wildfire risk, says Knight. “We need to listen to Native people and learn and understand why they managed the landscape the way they did,” adds Mendes.Collaboration for corroborationTo map the region’s forest history, the team drew on historical accounts and oral histories from Karuk, Yurok and Hoopa Valley Tribe members collected by study co-author Frank Lake, a US Forest Service research ecologist in Arcata, California, and a Karuk descendant, as part of his PhD thesis in 2007. These accounts described the tribes’ fire and land use. For instance, members lit small fires to keep trails clear; this also reduced the amount of vegetation, preventing expansion of wildfires from lightning strikes. Larger fires, called broadcast burning, were used to improve visibility, hunting and nut-harvesting conditions in the forest. The effects of fire on the vegetation lasted for decades.Knight says that it was important to collaborate with the tribes given their knowledge of the region. The Karuk Resources Advisory Board approved a proposal for the study before it began. “In a way, it’s decolonizing the existing academic model that hasn’t been very inclusive of Indigenous histories,” says Lake.The researchers also analysed sediment cores collected near two low-elevation lakes in the Klamath Mountains that are culturally important to the tribes. Layers of pollen in the cores were used to infer the approximate tree density in the area at various times, and modelling helped date the cores so they could estimate how that density changed.The team also measured charcoal in the cores’ layers, which helped to map fluctuations in the amount of fire in the region. Burn scars on tree stumps pointed to specific instances of fire in between 1700-1900. Because the stumps’ rings serve as an ecological calendar, the researchers were able to compare periods of fire with corresponding tree-density data. They then pieced together how this density fluctuated with fire incidence. Although these empirical methods could not specifically confirm that the fires were lit by the tribes, patterns suggested when this was more probable, says Knight. For instance, increased burning in cool, wet periods, when fires caused by lightning were probably less common, suggested a human influence.Combining multiple lines of evidence, Knight and her team show that the tree density in this region of Klamath Mountains started to increase as the area was colonized, partly because the European settlers prevented Indigenous peoples from practising cultural burning. In the twentieth century, total fire suppression became a standard management practice, and fires of any kind were extinguished or prevented — although controlled burns are currently used in forest management. The team reports that in some areas, the tree density is higher than it has been for thousands of years, owing in part to fire suppression.Healthy forestA dense forest isn’t necessarily a healthy one, says Knight. The Douglas-fir, which dominate the low-land Klamath forests, are less fire resilient and more prone to calamitous wildfires. “This idea that we simply should let nature take its course is just not supported by this work,” she says. She adds that one of the study’s strengths is the multiple lines of evidence showing that past Indigenous burning helped to manage tree density.Fire ecologist Jeffrey Kane at the California State Polytechnic University Humboldt in Arcata says that the study’s findings of increased tree density are not surprising. He has made similar observations in the Klamath region. “There’s a lot more trees than were there just 120 years ago,” he says.Dominick DellaSala, chief scientist at forest-protection organization Wild Heritage in Talent, Oregon, points out that the results suggesting record tree densities cannot be applied to the entire Klamath region, owing to the limited range of the study’s lakeside data.Knight, however, says that the results can be extrapolated to other similar low-elevation lake sites that have similar vegetation types.More Indigenous voicesPalaeoecology studies are increasingly incorporating Indigenous knowledge — but there’s still a long way to go, says physical geographer Michela Mariani at the University of Nottingham, UK. In Australia, Mariani has also found that tree density began to increase after British colonization hampered cultural burning. “It’s very important that we now include Indigenous people in the discussion in fire management moving on,” Mariani says. “They have a deeper knowledge of the landscape we simply don’t have.”Including Indigenous voices in research is also crucial for decolonizing conventional scientific methods, Lake emphasizes. It “becomes a form of justice for those Indigenous people who have long been excluded, marginalized and not acknowledged”, he says. More

  • in

    Hydrology, biogeochemistry and metabolism in a semi-arid mediterranean coastal wetland ecosystem

    Gibbs, J. P. Wetland loss and biodiversity conservation. Conserv. Biol. 14, 314–317 (2000).Article 

    Google Scholar 
    Turner, R. K. et al. Ecological-economic analysis of wetlands: Scientific integration for management and policy. Ecol. Econ. 35, 7–23 (2000).Article 

    Google Scholar 
    Zedler, J. B. & Kercher, S. Wetland resources: Status trends ecosystem services and restorability. Annu. Rev. Environ. Resour. 15, 39–74 (2005).Article 

    Google Scholar 
    Euliss, N. H., Smith, L. M., Wilcox, D. A. & Browne, B. A. Lining ecosystem processes with wetland management goals: Chartering a course for a sustainable future. Wetlands 28, 553–562 (2008).Article 

    Google Scholar 
    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change. 26, 152–158 (2014).Article 

    Google Scholar 
    Macreadie, P. J. et al. The future of blue carbon. Nat. Commun. 10, 3998 (2019).ADS 
    Article 

    Google Scholar 
    RAMSAR. Wise use of wetlands, Ramsar Handbooks, 4th edition (2010).Kingsford, R. T., Basset, A. & Jackson, L. Wetlands: Conservation’s poor cousins. Aquat. Conserv. 26, 892–916 (2016).Article 

    Google Scholar 
    Beck, M. W., Heck, K. L. & Able, K. W. The Identification, Conservation, and Management of Estuarine and Marine Nurseries for Fish and Invertebrates: A better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51, 633–641 (2001).Article 

    Google Scholar 
    Canu, D. M. et al. Adressing sustainability of clam farming in the Venice Lagoon. Ecol. Soc. 16, 26 (2010).
    Google Scholar 
    Canu, D. M., Solidoro, C., Cossarini, G. & Giorgi, F. Effect of global change on bivalve rearing activity and the need for adaptive management. Clim. Res. 42, 13–26 (2011).Article 

    Google Scholar 
    Newton, A. et al. Anthropogenic pressures on Coastal Wetlands. Front. Ecol. Evol. 8, 144 (2020).Article 

    Google Scholar 
    Ayache, F. et al. Environmental characteristics landscape history and pressures on three coastal lagoons in the Southern Mediterranean Region: Merja Zerga (Morocco) Ghar El Melh (Tunisia) and Lake Manzala (Egypt). Hydrobiologia 622, 15–43 (2009).CAS 
    Article 

    Google Scholar 
    Solidoro, C. et al. Response of Venice Lagoon ecosystem to natural and anthropogenic pressures over the last 50 years. In Coastal Lagoons—Critical Habitats of Environmental Change (eds. Kennish, M. J. & Paerl, H. W.) 483–511 (2010).Newton, A. et al. Assessing quantifying and valuing the ecosystem services of coastal lagoons. J. Nat. Conserv. 44, 50–65 (2018).Article 

    Google Scholar 
    Newton, A. et al. An overview of ecological status vulnerability and future perspectives of European large shallow semi-enclosed coastal systems lagoons and transitional waters. Estuar. Coast. Shelf Sci. 140, 95–122 (2014).ADS 
    Article 

    Google Scholar 
    Béjaoui, B. et al. Random Forest model and TRIX used in combination to assess and diagnose the trophic status of Bizerte Lagoon, southern Mediterranean. Ecol. Indic. 71, 293–301 (2016).Article 

    Google Scholar 
    Ramdani, M. et al. North African wetland lakes: Characterization of nine sites included in the CASSARINA Project. Aquat. Ecol. 35, 281–302 (2001).Article 

    Google Scholar 
    Junk, W. J. et al. Current state of knowledge regarding the world’s wetlands and their future under global climate change: A synthesis. Aquat. Sci. 75, 151–167 (2013).CAS 
    Article 

    Google Scholar 
    Ouni, H. et al. Numerical modeling of hydrodynamic circulation in Ichkeul Lake-Tunisia. Energy Rep. 6, 208–213 (2020).Article 

    Google Scholar 
    Hollis, G. E. et al. Modeling and management of the internationally important wetland at Garaet Ichkeul Tunisia. Numéro 4 de IWRB special publication, International Waterfowl Research Bureau, ISSN 0962–6271 Volume 4 de International Waterfowl Research Bureau Slimbridge: IWRB special publication (ed. International Waterfowl Research Bureau) 1–121 (1986).Casagranda, C. & Boudouresque, C. F. A first quantification of the overall biomass, from phytoplankton to birds, of a Mediterranean brackish lagoon: Revisiting the ecosystem of Lake Ichkeul (Tunisia). Hydrobiologia 637, 73–85 (2010).Article 

    Google Scholar 
    Hamdi, N., Touihri, M. & Charfi, F. Diagnostic Écologique du Parc National Ichkeul (Tunisie) après la construction des barrages: Cas des oiseaux d’eau. Rev. Ecol-Terre Vie. 67, 41–62 (2012).
    Google Scholar 
    UNESCO. Biosphere Reserve Information Tunisia Ichkeul, UNESCO-MAB. Biosphere Reserves Directory. (2009a).UNESCO. Ichkeul National Park http://whc.unesco.org/en/list/8/ (2009b).RAMSAR. Convention and Wetlands International. Information Sheet on Ramsar Wetlands Tunisia Ichkeul, Ramsar Sites Information Service. (2009).Tamisier, A., et al. Modelling aquatic ecosystems: Benefits, costs and risks, for a field biologist. Ichkeul Lake, Tunisia, a case study. In Limnology and Aquatic birds, Monitoring, modeling and management (eds. Comin, F. A., Herrera, J. A. & Ramirez, J.) 185–203 (2001).Giordani, G. et al. Nutrient fluxes in transitional zones of the Italian coast. LOICZ Reports & Studies No. 28, ii+157 pages, LOICZ, Texel, the Netherlands. (2005).Thomson, A. J., Giannopoulos, G., Pretty, J., Baggs, E. M. & Richardson, D. J. Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Phil. Trans. R. Soc. B367, 1157–1168 (2012).Article 

    Google Scholar 
    Chen, N., Wu, J., Chen, Z., Lu, T. & Wang, L. Spatial-temporal variation of dissolved N2 and denitrification in an agricultural river network, southeast China. Agric. Ecosyst. Environ. 189, 1–10 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    Loeks, B. M. & Cotner, J. B. Upper Midwest lakes are supersaturated with N2. Proc. Natl. Acad. Sci. USA 117, 17063–17067 (2020).Article 

    Google Scholar 
    Thomann, R. V., DiToro, D. M., Winfield, R. P. & O’Connor, D. J. Mathematical modelling of phytoplankton in Lake Ontario. Part 1. Model development and verification. U.S. Environmental Protection Agency, EPA-660/3-75-005, Corvallis, Oreg. 77 (1975).DiToro, D. M. & Connolly, J. P. Mathematical models of water quality in large lakes. Part 2: Lake Erie. U.S. Environmental Protection Agency, Duluth, Minnesota. EPA-600/3-80-065. 231. (1980)Jacobsen, O. S. & Jorgensen, S. E. A submodel for nitrogen release from sediments. Ecol. Model. 1, 147–151 (1975).CAS 
    Article 

    Google Scholar 
    Jorgensen, S. E., Kamp-Neilsen, L. & Jacobsen, O. S. A submodel for anaerobic mud-water exchange of phosphate. Ecol. Model. 1, 133–146 (1975).Article 

    Google Scholar 
    Jorgensen, S. E. An Eutrophication model for a lake. Ecol. Model. 2, 147–165 (1976).Article 

    Google Scholar 
    Jorgensen, S. E., Mejer, H. & Friis, M. Examination of a Lake model. Ecol. Model. 4, 253–278 (1978).Article 

    Google Scholar 
    Chapelle, A., Mesnage, V., Mazouni, N., Deslous-Paoli, J. M. & Picot, B. Modélisation des cycles de l’azote et du phosphore dans les sédiments d’une lagune soumise à une exploitation conchylicole. Oceanol. Acta. 17, 609–620 (1994).CAS 

    Google Scholar 
    Raillard, O. & Ménesguen, A. An ecosystem box model for estimating the carrying capacity of a macrotidal shellfish system. Mar. Ecol. Prog. Ser. 115, 117–130 (1994).ADS 
    Article 

    Google Scholar 
    Kremer, H. H. et al. Land–ocean interactions in the coastal zone: Science plan and implementation strategy, IGBP Report 51, IHDP Report 18. International Geosphere-Biosphere Programme. (2005).Strobl, R., Zaldivar, C. J., Somma, F., Stips, A. & Garcia, G. E. Application of the LOICZ Methodology to the Mediterranean Sea EUR 23936 EN. Luxembourg (Luxembourg): OPOCE. JRC52454. (2009).Swaney, D. P. & Giordani, G (Eds.). Proceedings of the LOICZ Workshop on Biogeochemical Budget Methodology and Applications, Providence RI, November 9–10, 2007. LOICZ Reports and Studies no. 37. GKSS Research Centre, Geesthacht. http://www.loicz.org/imperia/md/content/loicz/print/rsreports/biogeochemical_budget_methodology_and_applications.pdf (2011).Swaney, D. P., Smith, S. V. & Wulff, F. The LOICZ Biogeochemical Modeling Protocol and its Application to Estuarine Ecosystems. In Teratise on Estuarine and Coastal Ecosystem Science, Academic Press, Elsevier (eds. Bauer, J. E. & Bianchi, T. S.) 136–159 (2011).Glaeser, B., Kannen, A. & Kremer, H. Introduction: The future of coastal areas. Challenges for planning practice and research. Gaia-Ecol. Perspect. Sci. Soc. 18, 145–149 (2009).
    Google Scholar 
    Glaeser, B., Bruckmeier, K., Glaser, M. & Krause, G. Social-ecological systems analysis in coastal and marine areas: A path toward integration of interdisciplinary knowledge. In Current Trends in Human Ecology. Cambridge Scholars Publishing (eds. Lopes, P. & Begossi, A.) 183–203 (2009b).Glaser, M. & Glaeser, B. The social dimension in the management of social ecological change. In Treatise on Estuarine and Coastal Science, Vol. 11: Integrated Management of Estuaries and Coasts. München: Elsevier (eds. Kremer, H. & Pinckney, J.) 59 (2011).Glaser, M. & Glaeser, B. Towards a framework for cross-scale and multi-level analysis of coastal and marine social-ecological systems dynamics. Reg. Environ. Change. 14, 2039–2052 (2014).Article 

    Google Scholar 
    Vybernaite-Lubiene, I. et al. Biogeochemical budgets of nutrients and metabolism in the curonian lagoon (Southeast Baltic Sea): Spatial and temporal variations. Water 14, 164 (2022).CAS 
    Article 

    Google Scholar 
    Yazidi, A., Saidi, S., Ben, M. N. & Darragi, F. Contribution of GIS to evaluate surface water pollution by heavy metals: Case of Ichkeul Lake (Northern Tunisia). J. Afr. Earth. Sci. 134, 166–173 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Goudling, M. et al. Ecosystem-based management of Amazon fisheries and wetlands. Fish Fish. 20, 138–158 (2018).
    Google Scholar 
    Mitsch, W. J. & Gosselink, J. G. Wetlands 5th edn. (Wiley, 2015).
    Google Scholar 
    World Bank 2022.Affouri, H. & Sahraoui, O. The sedimentary organic matter from a Lake Ichkeul core (far northern Tunisia): Rock-Eval and biomarker approach. J. Afr. Earth. Sci. 129, 248–259 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Vanderkelen, I., van Lipzig, N. P. M. & Thiery, A. Modelling the water balance of Lake Victoria (East Africa)–Part 1: Observational analysis. Hydrol. Earth Syst. Sci. 22, 1–17 (2018).Article 

    Google Scholar 
    Coe, M. T. & Foley, J. A. Human and natural impacts on the water resources of the Lake Chad basin. J. Geophys. Res. Atmos. 106, 3349–3356 (2001).ADS 
    Article 

    Google Scholar 
    Gao, H., Bohn, T. J., Podest, E., McDonald, K. C. & Lettenmaier, D. P. On the causes of the shrinking of Lake Chad. Environ. Res. Lett. 6, 34021 (2011).Article 

    Google Scholar 
    Prange, M., Wilke, T. & Wesselingh, F. P. The other side of sea level change. Commun. Earth Environ. 1, 69 (2020).ADS 
    Article 

    Google Scholar 
    Glausiusz, J. Environmental Science: New life for the DeaSea?. Nature 464, 1118–1120 (2010).CAS 
    Article 

    Google Scholar 
    Gronewold, A. D. & Stow, C. A. Water Loss from the Great Lakes. Science 343, 1084–1085 (2014).ADS 
    Article 

    Google Scholar 
    Mei, X., Dai, Z., Du, J. & Chen, J. Linkage between Three Gorges Dam impacts and the dramatic recessions in China’s largest freshwater lake, Poyang Lake. Sci. Rep. 5, 18197 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    Micklin, P. The aral sea disaster. Ann. Rev. Earth Planet. Sci. 35, 47–72 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    Feng, L., Han, X., Hu, C. & Chen, X. Four decades of wetland changes of the largest freshwater lake in China: Possible linkage to the Three Gorges Dam?. Remote Sens. Environ. 176, 43–55 (2016).ADS 
    Article 

    Google Scholar 
    Downing, J. A. et al. The global abundance and size distribution of lakes, ponds, and impoundments. Limnol. Oceanogr. 51, 2388–2397 (2006).ADS 
    Article 

    Google Scholar 
    Awange, J. L. et al. The falling lake victoria water level: GRACE, TRIMM and CHAMP satellite analysis of the lake basin. Water Resour. Manag. 22, 775–796 (2008).Article 

    Google Scholar 
    Carroll, M. L., Townshend, R. H. G., DiMiceli, C. M., Loboda, T. & Sohlberg, R. A. Shrinkage lakes of the Artic: Spatial relationships and trajectory of change. Geophys. Res. Lett. 38, 20406 (2011).ADS 
    Article 

    Google Scholar 
    Lefebvre, G. et al. Predicting the vulnerability of seasonally-flooded wetlands to climate change across the Mediterranean Basin. Sci. Total Environ. 692, 546–555 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Touaylia, S., Ghannem, S., Toumi, H., Béjaoui, M. & Garrido, J. Assessment of heavy metals status in northern Tunisia using contamination indices: Case of the Ichkeul steams system. Int. J. Environ. Res. Public Health. 3, 209–217 (2016).
    Google Scholar 
    Aouissi, J., Benabdallah, S., Lili, C. Z. & Cudennec, C. Modelling water quality to improve agricultural practices and land management in a Tunisian catchment using soil and water assessment tool. J. Environ. Qual. 43, 18–25 (2014).Article 

    Google Scholar 
    Aouissi, J., Lili, C. Z., Benabdallah, S. & Cudennec, C. Assessing the hydrological impacts of agricultural changes upstream of the Tunisian World Heritage sea-connected Ichkeul Lake. Proc. Int. Assoc. Hydrol. Sci. 365, 61–65 (2015).
    Google Scholar 
    Fathalli, A. et al. Molecular and phylogenetic characterization of potentially toxic cyanobacteria in Tunisian freshwaters. Syst. Appl. Microbiol. 34, 303–310 (2011).CAS 
    Article 

    Google Scholar 
    Ouchir, N., Morin, S., Ben, A. L., Boughdiri, M. & Aydi, A. Periphytic diatom communities in tributaries around Lake Ichkeul, northern Tunisia: A preliminary assessment. Afr. J. Aquat. Sci. 42, 65–73 (2017).Article 

    Google Scholar 
    Chislock, M. F., Doster, E., Zitomer, R. A. & Wilson, A. E. Eutrophication: Causes, consequences, and controls in aquatic ecosystems. Nat. Educ. Knowl. 4, 10 (2013).
    Google Scholar 
    Paerl, H. W. & Huisman, J. Climate change: A catalyste for global expansion of harmful cyanobacteria blooms. Environ. Microb. Rep. 1, 27–37 (2009).CAS 
    Article 

    Google Scholar 
    Paerl, H. W., Nathan, S. H. & Calandrino, E. S. Controlling harmful cyanobacteria blooms in a world experiencing anthropogenic and climatic-induced change. Sci. Total Environ. 409, 1739–1745 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    O’Neil, J. M., Davis, T. M., Burford, M. A. & Gobler, C. J. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14, 313–334 (2012).Article 

    Google Scholar 
    Ben, S. F. et al. Pesticides in Ichkeul Lake-Bizerte Lagoon Watershed in Tunisia: Use, occurrence, and effects on bacteria and free-living marine nematodes. Environ. Sci. Pollut. Res. 23, 36–48 (2016).Article 

    Google Scholar 
    Bourhane, Z. et al. Microbial diversity alteration reveals biomarkers of contamination in soil-river-lake continuum. J. Hazard. Mater. 421, 126789 (2022).CAS 
    Article 

    Google Scholar 
    Kolzau, S. et al. Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from Ambient nutrient concentrations. PLoS ONE 9, e96065 (2014).ADS 
    Article 

    Google Scholar 
    Abidi, M., Ben, A. R. & Gueddari, M. Assessment of the trophic status of the South Lagoon of Tunis (Tunisia, Mediterranean Sea); a Geochemical and Statistical Approaches. J. Chem. (2018).Saunders, D. L. & Kaffl, J. Denitrification rates in the sediments of Lake Memphremagog, Canda–USA. Water Res. 35, 1897–1904 (2001).CAS 
    Article 

    Google Scholar 
    Davidson, E. A. & Seitzinger, S. The enigma of progress in denitrification research. Ecol. Appl. 16, 2057–2063 (2006).Article 

    Google Scholar 
    Medina-Galvan, J. et al. Comparing the biogeochemical functioning of two arid subtropical coastal lagoons: The effect of wastewater discharges. Ecosyst. Health Sustain. 7, 1 (2021).Article 

    Google Scholar 
    Piehler, M. F. & Smyth, A. R. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere. 2, 1–17 (2011).ADS 
    Article 

    Google Scholar 
    Loeks-Johson, B. M. & Cotner, J. B. Upper Midwest lakes are supersaturated with N2. Proc. Natl. Acad. Sci. U S A. 117, 17063–17067 (2020).Reddy, K. R., Patrick, W. H. & Lindau, C. W. Nitrification-denitrification at the plant root sediment interface in Wetlands. Limnol. Oceanogr. 34, 1004–1013 (1989).ADS 
    CAS 
    Article 

    Google Scholar 
    Adrian, A. et al. Lakes as sentinels of climate change. Limnol. Oceanogr. 54, 2283–2297 (2009).ADS 
    Article 

    Google Scholar 
    Seo, C. D. & DeLaune, R. D. Fungal and bacterial mediated denitrification in wetlands: Influence of sediment redox condition. Water Res. 44, 2441–2450 (2010).CAS 
    Article 

    Google Scholar 
    Montzka, S. A., Dlugokencky, I. J. & Butler, J. H. Non-CO2 greenhouse gases and climate change. Nature 476, 43–50 (2011).CAS 
    Article 

    Google Scholar 
    Sferratore, A., Billen, G. & Garnier, J. The S Modeling nutrient (N, P, Si ) budget in the Seine watershed: Application of the River Strahler model using data from local to global scale resolution Modeling nutrient (N, P, Si) budget in the Seine watershed: Application of the River Strahler model using data from local to global scale resolution. Glob. Biogeochem. Cycles. 19, 20 (2005).Article 

    Google Scholar 
    Béjaoui, B. et al. 3D modeling of phytoplankton seasonal variation and nutrient budget in a Southern Mediterranean Lagoon. Mar. Pollut. Bull. 114, 962–976 (2017).Article 

    Google Scholar 
    Shaiek, M., Fassatoui, C. & Romdhane, M. S. Past and present fish species recorded in the estuarine Lake Ichkeul, northern Tunisia. Afr. J. Aquat. Sci. 41, 171–180 (2016).Article 

    Google Scholar 
    INM. Données climatiques de la région de Bizerte. Institut National de Météorologie, Tunis, Tunisie. (2017).Rodier, J. et al. L’analyse de l’eau, Eaux naturelles, eaux résiduaires, eau de mer, Dunod Paris. (1996).Lorenzen, C. J. Determination of chlorophyll and pheopigments by spectrophotometric equations. Limnol. Oceanogr. 12, 343–346 (1967).ADS 
    CAS 
    Article 

    Google Scholar 
    Parsons, T. R., Maita, Y. & Lalli, C. M. A manual of chemical and biological methods for seawater analysis. Geol. Mag. 122, 570–570 (1980).
    Google Scholar 
    Redfield, A. C. The biological control of chemical factors in the environment. Sci. Prog. 11, 150–170 (1960).CAS 

    Google Scholar 
    Gordon, D. C. et al. LOICZ biogeochemical modelling guidelines. LOICZ Rep and Stud. 5, 1–96 (1996).
    Google Scholar 
    Seitzinger, S. P. Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. Limnol. Oceanogr. 33, 702–724 (1988).ADS 
    CAS 

    Google Scholar 
    Atkinson, M. J. & Smith, S. V. C:N: P ratios of benthic marine plants. Limnol. Oceanogr. 28, 568–574 (1983).ADS 
    CAS 
    Article 

    Google Scholar 
    APHA (American Public Health Association) Standard Methods for the Examination of Water and Wastewater. 18th Edition, American Public Health Association (APHA), American Water Works Association (AWWA) and Water Pollution Control Federation (WPCF), Washington DC (1992). More

  • in

    Repeated introduction of micropollutants enhances microbial succession despite stable degradation patterns

    Schwarzenbach RP, Escher BI, Fenner K, Hofstetter TB, Johnson CA, Von Gunten U, et al. The challenge of micropollutants in aquatic systems. Science (80-). 2006;313:1072–7.Article 

    Google Scholar 
    Deblonde T, Cossu-Leguille C, Hartemann P. Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health. 2011;214:442–8.Article 

    Google Scholar 
    Wang M, Cernava T. Overhauling the assessment of agrochemical-driven interferences with microbial communities for improved global ecosystem integrity. Environ Sci Ecotechnol. 2020;4:100061.Article 

    Google Scholar 
    Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, et al. A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ. 2014;473–474:619–41.Article 

    Google Scholar 
    Wang Z, Zhang XH, Huang Y, Wang H. Comprehensive evaluation of pharmaceuticals and personal care products (PPCPs) in typical highly urbanized regions across China. Environ Pollut. 2015;204:223–32.Article 

    Google Scholar 
    Eggen RIL, Hollender J, Joss A, Schärer M, Stamm C. Reducing the discharge of micropollutants in the aquatic environment: the benefits of upgrading wastewater treatment plants. Environ Sci Technol. 2014;48:7683–9.Article 

    Google Scholar 
    Vila-Costa M, Cerro-Gálvez E, Martínez-Varela A, Casas G, Dachs J. Anthropogenic dissolved organic carbon and marine microbiomes. ISME J. 2020;14:2646–8.Article 

    Google Scholar 
    da Silva GCX, Medeiros de Abreu CH, Ward ND, Belúcio LP, Brito DC, Cunha HFA, et al. Environmental impacts of dam reservoir filling in the East Amazon. Front Water. 2020;2:11.Article 

    Google Scholar 
    Kuroda K, Murakami M, Oguma K, Muramatsu Y, Takada H, Takizawa S. Assessment of groundwater pollution in Tokyo using PPCPs as sewage markers. Environ Sci Technol. 2012;46:1455–64.Article 

    Google Scholar 
    Liu WR, Zhao JL, Liu YS, Chen ZF, Yang YY, Zhang QQ, et al. Biocides in the Yangtze River of China: spatiotemporal distribution, mass load and risk assessment. Environ Pollut. 2015;200:53–63.Article 

    Google Scholar 
    Roberts J, Kumar A, Du J, Hepplewhite C, Ellis DJ, Christy AG, et al. Pharmaceuticals and personal care products (PPCPs) in Australia’s largest inland sewage treatment plant, and its contribution to a major Australian river during high and low flow. Sci Total Environ. 2016;541:1625–37.Article 

    Google Scholar 
    Rodea-Palomares I, Gonzalez-Pleiter M, Gonzalo S, Rosal R, Leganes F, Sabater S, et al. Hidden drivers of low-dose pharmaceutical pollutant mixtures revealed by the novel GSA-QHTS screening method. Sci Adv. 2016;2:1–12.Article 

    Google Scholar 
    Yang X, Chen F, Meng F, Xie Y, Chen H, Young K, et al. Occurrence and fate of PPCPs and correlations with water quality parameters in urban riverine waters of the Pearl River Delta, South China. Environ Sci Pollut Res. 2013;20:5864–75.Article 

    Google Scholar 
    Cerro-Gálvez E, Dachs J, Lundin D, Fernández-Pinos MC, Sebastián M, Vila-Costa M. Responses of coastal marine microbiomes exposed to anthropogenic dissolved organic carbon. Environ Sci Technol. 2021;55:9609–21.Article 

    Google Scholar 
    Martinez-Varela A, Cerro-Gálvez E, Auladell A, Sharma S, Moran MA, Kiene RP, et al. Bacterial responses to background organic pollutants in the northeast subarctic Pacific Ocean. Environ Microbiol. 2021;23:4532–46.Article 

    Google Scholar 
    Bob A, Shen D, Li S, Zhang L, Rashid A, Sun Q, et al. Strong impact of micropollutants on prokaryotic communities at the horizontal but not vertical scales in a subtropical reservoir, China. Sci Total Environ. 2020;721:137767.Article 

    Google Scholar 
    Tlili A, Corcoll N, Arrhenius Å, Backhaus T, Hollender J, Creusot N, et al. Tolerance patterns in stream biofilms link complex chemical pollution to ecological impacts. Environ Sci Technol. 2020;54:10745–53.Article 

    Google Scholar 
    Chalew TEA, Halden RU. Environmental exposure of aquatic and terrestrial biota to triclosan and triclocarban. J Am Water Resour Assoc. 2009;45:4–13.Article 

    Google Scholar 
    Zhang W, Yin K, Chen L. Bacteria-mediated bisphenol A degradation. Appl Microbiol Biotechnol. 2013;97:5681–9.Article 

    Google Scholar 
    Staples CA, Dorn PB, Klecka GM, O’Block ST, Harris LR. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere. 1998;36:2149–73.Article 

    Google Scholar 
    Choi YJ, Lee LS. Aerobic soil biodegradation of bisphenol (BPA) alternatives bisphenol S and bisphenol AF compared to BPA. Environ Sci Technol. 2017;51:13698–704.Article 

    Google Scholar 
    McMurry LM, Oethinger M, Levy SB. Triclosan targets lipid synthesis [4]. Nature. 1998;394:531–2.Article 

    Google Scholar 
    Cabana H, Jiwan JLH, Rozenberg R, Elisashvili V, Penninckx M, Agathos SN, et al. Elimination of endocrine disrupting chemicals nonylphenol and bisphenol A and personal care product ingredient triclosan using enzyme preparation from the white rot fungus Coriolopsis polyzona. Chemosphere. 2007;67:770–8.Article 

    Google Scholar 
    Hu A, Ju F, Hou L, Li J, Yang X, Wang H, et al. Strong impact of anthropogenic contamination on the co-occurrence patterns of a riverine microbial community. Environ Microbiol. 2017;19:4993–5009.Article 

    Google Scholar 
    Boyd TJ, Smith DC, Apple JK, Hamdan LJ, Osburn CL, Montgomery MT. Evaluating PAH biodegradation relative to total bacterial carbon demand in coastal ecosystems: Are PAHs truly recalcitrant? In: Van Dijk T. (ed). Microbial Ecology Research Trends. Nova Science Publishers, 2008. pp 1–38.Okere UV, Cabrerizo A, Dachs J, Ogbonnaya UO, Jones KC, Semple KT. Effects of pre-exposure on the indigenous biodegradation of 14C-phenanthrene in Antarctic soils. Int Biodeterior Biodegrad. 2017;125:189–99.Article 

    Google Scholar 
    Coll C, Bier R, Li Z, Langenheder S, Gorokhova E, Sobek A. Association between aquatic micropollutant dissipation and river sediment bacterial communities. Environ Sci Technol. 2020;54:14380–92.Article 

    Google Scholar 
    Bender EA, Case TJ, Gilpin ME. Perturbation experiments in community ecology: Theory and practice. Ecology. 1984;65:1–13.Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, et al. Fundamentals of microbial community resistance and resilience. Front Microbiol. 2012;3:1–19.Article 

    Google Scholar 
    Buerger S, Spoering A, Gavrish E, Leslin C, Ling L, Epstein SS. Microbial scout hypothesis, stochastic exit from dormancy, and the nature of slow growers. Appl Environ Microbiol. 2012;78:3221–8.Article 

    Google Scholar 
    Lee SH, Sorensen JW, Grady KL, Tobin TC, Shade A. Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fire. ISME J. 2017;11:1447–59.Article 

    Google Scholar 
    Lennon JT, den Hollander F, Wilke-Berenguer M, Blath J. Principles of seed banks and the emergence of complexity from dormancy. Nat Commun. 2021;12:1–16.Article 

    Google Scholar 
    Philippot L, Griffiths BS, Langenheder S. Microbial community resilience across ecosystems and multiple disturbances. Microbiol Mol Biol Rev. 2021;85:e00026–20.Article 

    Google Scholar 
    Hu A, Li S, Zhang L, Wang H, Yang J, Luo Z, et al. Prokaryotic footprints in urban water ecosystems: a case study of urban landscape ponds in a coastal city, China. Environ Pollut. 2018;242:1729–39.Article 

    Google Scholar 
    Im J, Löffler FE. Fate of bisphenol A in terrestrial and aquatic environments. Environ Sci Technol. 2016;50:8403–16.Article 

    Google Scholar 
    Sun Q, Li M, Ma C, Chen X, Xie X, Yu CP. Seasonal and spatial variations of PPCP occurrence, removal and mass loading in three wastewater treatment plants located in different urbanization areas in Xiamen, China. Environ Pollut. 2016;208:371–81.Article 

    Google Scholar 
    Sun Q, Wang Y, Li Y, Ashfaq M, Dai L, Xie X, et al. Fate and mass balance of bisphenol analogues in wastewater treatment plants in Xiamen City, China. Environ Pollut. 2017;225:542–9.Article 

    Google Scholar 
    Sun Q, Li Y, Chou PH, Peng PY, Yu CP. Transformation of bisphenol A and alkylphenols by ammonia-oxidizing bacteria through nitration. Environ Sci Technol. 2012;46:4442–8.Article 

    Google Scholar 
    Zaayman M, Siggins A, Horne D, Lowe H, Horswell J. Investigation of triclosan contamination on microbial biomass and other soil health indicators. FEMS Microbiol Lett. 2017;364:1–6.Article 

    Google Scholar 
    Xie J, Zhao N, Zhang Y, Hu H, Zhao M, Jin H. Occurrence and partitioning of bisphenol analogues, triclocarban, and triclosan in seawater and sediment from East China Sea. Chemosphere. 2022;287:132218.Article 

    Google Scholar 
    Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon HB, et al. Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotoxicol Environ Saf. 2015;122:565–72.Article 

    Google Scholar 
    Kalyuzhny M, Shnerb NM. Dissimilarity-overlap analysis of community dynamics: opportunities and pitfalls. Methods Ecol Evol. 2017;8:1764–73.Article 

    Google Scholar 
    Wang J, Pan F, Soininen J, Heino J, Shen J. Nutrient enrichment modifies temperature-biodiversity relationships in large-scale field experiments. Nat Commun. 2016;7:1–9.
    Google Scholar 
    Hildebrand F, Tito RY, Voigt AY, Bork P, Raes J. Correction to: LotuS: an efficient and user-friendly OTU processing pipeline [Microbiome, 2, (2014), 30]. Microbiome. 2014;2:1–7.Article 

    Google Scholar 
    Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.Article 

    Google Scholar 
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.Article 

    Google Scholar 
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Methods. 2010;7:335–6.Article 

    Google Scholar 
    Klappenbach JA, Saxman PR, Cole JR, Schmidt TM. Rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res. 2001;29:181–4.Article 

    Google Scholar 
    Wu L, Yang Y, Chen S, Zhao M, Zhu Z, Yang S, et al. Long-term successional dynamics of microbial association networks in anaerobic digestion processes. Water Res. 2016;104:1–10.Article 

    Google Scholar 
    Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79.Article 

    Google Scholar 
    Stegen JC, Lin X, Fredrickson JK, Konopka AE. Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol. 2015;6:1–15.Article 

    Google Scholar 
    Webb CO, Ackerly DD, Kembel SW. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics. 2008;24:2098–2100.Article 

    Google Scholar 
    Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21.Article 

    Google Scholar 
    Letunic I, Bork P. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:2–5.Article 

    Google Scholar 
    Anderson MJ. Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci. 2001;58:626–39.Article 

    Google Scholar 
    Oksanen AJ, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, et al. Vegan: community ecology package. Encyclopedia of Food and Agricultural Ethics. 2019; 2395–6.Bashan A, Gibson TE, Friedman J, Carey VJ, Weiss ST, Hohmann EL, et al. Universality of human microbial dynamics. Nature. 2016;534:259–62.Article 

    Google Scholar 
    Vila JCC, Liu YY, Sanchez A. Dissimilarity–overlap analysis of replicate enrichment communities. ISME J. 2020;14:2505–13.Article 

    Google Scholar 
    Ahlmann-Eltze C, Patil I. ggsignif: significance Brackets for ‘ggplot2’. R package version 0.6.1. 2021.Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43.Article 

    Google Scholar 
    Glassman SI, Martiny JBH. Broadscale ecological patterns are robust to use of exact. mSphere. 2018;3:e00148–18.Article 

    Google Scholar 
    Lindström ES, Östman Ö. The importance of dispersal for bacterial community composition and functioning. PLoS One. 2011;6:e25883.Article 

    Google Scholar 
    Shen D, Langenheder S, Jürgens K. Dispersal modifies the diversity and composition of active bacterial communities in response to a salinity disturbance. Front Microbiol. 2018;9:2188.Article 

    Google Scholar 
    Zhou NA, Lutovsky AC, Andaker GL, Gough HL, Ferguson JF. Cultivation and characterization of bacterial isolates capable of degrading pharmaceutical and personal care products for improved removal in activated sludge wastewater treatment. Biodegradation. 2013;24:813–27.Article 

    Google Scholar 
    Thelusmond JR, Strathmann TJ, Cupples AM. Carbamazepine, triclocarban and triclosan biodegradation and the phylotypes and functional genes associated with xenobiotic degradation in four agricultural soils. Sci Total Environ. 2019;657:1138–49.Article 

    Google Scholar 
    Danzl E, Sei K, Soda S, Ike M, Fujita M. Biodegradation of bisphenol A, bisphenol F and bisphenol S in seawater. Int J Environ Res Public Health. 2009;6:1472–84.Article 

    Google Scholar 
    Zaborowska M, Wyszkowska J, Borowik A. Soil microbiome response to contamination with Bisphenol A, Bisphenol F and Bisphenol S. Int J Mol Sci. 2020;21:3529.Article 

    Google Scholar 
    Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, et al. Competitive and cooperative metabolic interactions in bacterial communities. Nat Commun. 2011;2:587–9.Article 

    Google Scholar 
    Pacheco AR, Moel M, Segrè D. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. Nat Commun. 2019;10:103.Article 

    Google Scholar 
    Oh S, Choi D, Cha C-J. Ecological processes underpinning microbial community structure during exposure to subinhibitory level of triclosan. Sci Rep. 2019;9:4598.Article 

    Google Scholar 
    Hagberg A, Gupta S, Rzhepishevska O, Fick J, Burmølle M, Ramstedt M. Do environmental pharmaceuticals affect the composition of bacterial communities in a freshwater stream? A case study of the Knivsta river in the south of Sweden. Sci Total Environ. 2021;763:142991.Article 

    Google Scholar 
    Gao H, LaVergne JM, Carpenter CMG, Desai R, Zhang X, Gray K, et al. Exploring co-occurrence patterns between organic micropollutants and bacterial community structure in a mixed-use watershed. Environ Sci Process Impacts. 2019;21:867–80.Article 

    Google Scholar 
    Wolff D, Krah D, Dötsch A, Ghattas AK, Wick A, Ternes TA. Insights into the variability of microbial community composition and micropollutant degradation in diverse biological wastewater treatment systems. Water Res. 2018;143:313–24.Article 

    Google Scholar 
    Bajić D, Vila JCC, Blount ZD, Sánchez A. On the deformability of an empirical fitness landscape by microbial evolution. Proc Natl Acad Sci USA. 2018;115:11286–91.Article 

    Google Scholar 
    Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and Processes of Microbial Community Assembly. Microbiol Mol Biol Rev. 2013;77:342–56.Article 

    Google Scholar 
    Zhou J, Ning D. Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev. 2017;81:1–32.Article 

    Google Scholar 
    Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.Article 

    Google Scholar 
    Svoboda P, Lindström ES, Ahmed Osman O, Langenheder S. Dispersal timing determines the importance of priority effects in bacterial communities. ISME J. 2018;12:644–6.Article 

    Google Scholar 
    Bernstein HC. Reconciling ecological and engineering design principles for building microbiomes. mSystems. 2019;4:1–5.Article 

    Google Scholar 
    Borchert E, Hammerschmidt K, Hentschel U, Deines P. Enhancing microbial pollutant degradation by integrating eco-evolutionary principles with environmental biotechnology. Trends Microbiol. 2021;29:908–18.Article 

    Google Scholar 
    Rocca JD, Muscarella ME, Peralta AL, Izabel-Shen D, Simonin M. Guided by microbes: applying community coalescence principles for predictive microbiome engineering. mSystems. 2021;6:e00538–21.Article 

    Google Scholar 
    Nemergut DR, Knelman JE, Ferrenberg S, Bilinski T, Melbourne B, Jiang L, et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME J. 2016;10:1147–56.Article 

    Google Scholar 
    Frost LS, Leplae R, Summers AO, Toussaint A, Edmonton A. Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol. 2005;3:722–32.Ullastres A, Merenciano M, Guio L, Gonz J. Transposable elements: a toolkit for stress and environmental adaptation in bacteria. Stress Environ Regul Gene Expr Adapt Bact. 2016;1:137–45.
    Google Scholar 
    Chang CY, Vila JCC, Bender M, Li R, Mankowski MC, Bassette M, et al. Engineering complex communities by directed evolution. Nat Ecol Evol. 2021;5:1011–23.Article 

    Google Scholar  More