More stories

  • in

    Searching the web builds fuller picture of arachnid trade

    Our online sampling methods largely follow protocols detailed in3,4, though we limited our online searches to online shops and did not extend to social media. Large portions of code are directly re-used from those papers, although we provide modified code with this paper additionally. For keyword searches and data review we used R v.4.1.149 via RStudio v.1.4.110350, and made wide use of functions supplied by the anytime v.0.3.951, assertthat v.0.2.152, dplyr v.1.0.753, glue v.1.4.254, lazyeval v.0.2.255, lubridate v.1.7.1056, magrittr v.2.0.157, 17urr v.0.3.458, reshape2 v.1.4.459, stringr v.1.4.060, and tidyr v.1.1.361 other specific package uses are listed during the methods description. We used the grateful v.0.0.362 package to generate citations for all R packages. Code and data used to produce figures and summary data are also available at: 10.5281/zenodo.5758541.Website sampling and searchWe searched for contemporary arachnid selling websites using the Google search engine and targeted nine languages (English, French, Spanish, German, Portuguese, Japanese, Czech, Polish, Russian). Terms were created to be inclusive, so only spiders and scorpions were on the initial search string as specialist groups may exist for either, but are unlikely for smaller arachnid groups, which were often listed under “other” in online shops. Terms were selected to be encompassing so that any sites listing variants of “spider” or mentioning arachnid in the chosen language were selected. Whilst some groups such as tarantulas are more popular as pets such sites will not omit translations of spider and should also be captured in the search, hence Terraristika (as was shown in previous analysis of amphibians and reptiles) listed the greatest number of species, despite not being a specialist site. We used the localised versions of each of these languages with the following Boolean search strings:

    English: (Spider OR scorpion OR arachnid) AND for sale

    French: (Araignée OR scorpion OR arachnide) AND à vendre

    Spanish: (Araña OR escorpión OR arácnido) AND en venta

    German: (Arachnoid OR Spinne OR Skorpion OR Spinnentier) AND zum Verkauf

    Portuguese: (Aranha OR escorpião OR aracnídeo) AND à venda

    Japanese: (クモ OR サソリ OR クモ型類) AND (中村彰宏 OR 販売)

    Czech: (Pavouk OR Štír OR pavoukovec) AND prodej

    Polish: (Pająk OR Skorpion OR pajęczak) AND sprzedaż

    Russian: Продажа пауков OR скорпионов

    We undertook these searches in a private window in the Firefox v.92.0.1 browser63 to limit the impacts of search history. These keywords were used to identify sites which may be selling arachnids, which could then be checked before a comprehensive scrape.For each language, we downloaded the first 15 pages of results between 2021-06-06 and 2021-07-07 (or fewer in the result that the search returned fewer than 15 pages: German 8 pages and Spanish 14 pages). This resulted in ~1270 sites that could potentially be selling arachnids. After removing duplicates and simplifying the URLs (so all ended in.com,.org,. co.uk etc.; Code S1), we reviewed each site for the following criteria (2021-07-31 to 2021-08-02): whether they sell arachnids, the type of site (trade or classified ads), the order arachnids were listed in (e.g., date or alphabetical), the best search method for gather species appearances (see below for hierarchical search methods), a refined target URL listing species inventory, the number of pages within the website potentially required to cycle through, and if the search method required a crawl, whether the site explicitly forbade crawling data collection and whether we could limit the crawl’s scope with a filter on downstream URLs. Finally, we assigned all suitable sites with a unique ID. We have made a censored version of the website review results available in Data S1. In addition to the systematic search for arachnid trade, we added 43 websites discovered ad hoc from links on previously discovered sites (many listed online shops), those listed in other journal articles on invertebrate trade (i.e.,6) or from discussion with informed colleagues (between 2021-08-07 and 2021-09-15). After reviewing these ad hoc sites (2021-08-07 to 2021-09-15), we had a combined total of 111 sites to attempt to search for the appearance of arachnid species.Our searches of websites took one of five forms (Code S2), designed to minimise server load and limit the number of irrelevant pages searched, while ensuring we captured the pages listing species. We prioritised using the lowest/simplest search method possible for each site.Single page or PDFFor websites that listed their entire arachnid stock on a single page, we retrieved that single page using the downloader v.0.4 package64. In cases where the inventory was listed in a PDF, we manually downloaded the PDF and used pdftools v.3.0.165 to assess the text.CycleSome websites had large stocklists split across multiple pages that could be accessed sequentially. In these cases, we used the downloader v.0.4 package64 to retrieve each page, as we cycled from page 1 to the terminal page identified during the website review stage. Two sites required a slight modification to the page cycling process: as the sequential pages were not defined by pages, but by the number of adverts displayed. In these instances, we cycled through all adverts 20 adverts at a time (i.e., matching the default number displayed at a time by the site). For all cycling we implemented a 10 s cooldown between requests to limit server load.Level 1 crawlFor websites that split their stock between multiple pages, but with no sequential ordering, we used a level 1 crawl, via the Rcrawler v.0.1.9.1 package66 to access them all. For example, where a site had an “arachnid for sale” page, but full species names existed only in linked pages (e.g., “tarantulas”, “scorpions”).Cycle and level 1 crawlSome websites required a combined approach, where stock was split sequentially across pages, and the species identities (i.e., scientific names) required accessing the pages linked to from the sequential pages. In these cases, we ran the initial sequential sampling followed by a level 1 crawl.Level 2 crawlWhere level 1 crawls were insufficient to cover all species sold on a site, we used a level 2 crawl to reach all pages listing species. This tended to be the case on websites with multiple categories to classify and split their stock (e.g., “arachnid”—“spider”—“tarantula”).For all crawls, we used a cooldown of 20 s between requests to limit server load, and where possible we limited the scope of the crawl (i.e., linked pages to be retrieved) using a key phrase common to all stock listing pages (e.g., “/category=arachnid/”).In addition to the sampling of contemporary sites, we explored the archived pages available for https://www.terraristik.com via the Internet Archive (2002–201967). Terraristika had been previously shown as a major contributor to traded species lists4, and the website’s age and accessibility via the internet archive meant it was one of the few websites where temporal sampling was feasible. We used pages retrieved via the Internet Archive’s Wayback machine API68, via code created for3,4. The code used was based on the wayback v.0.4.0 package69, but additionally made httr v.1.4.270, jsonlite v.1.7.271, downloader v.0.464, lubridate v.1.7.1056, and tibble v.3.1.3 packages72 (Code S3).Keyword generationWe relied on multiple sources to build a list of arachnid species (spiders, scorpions and uropygi). For spiders we used the WSC (ref. 18; https://wsc.nmbe.ch/dataresources; accessed 2021-09-18). We filtered the WSC dataset to remove subspecies, then used a combination of rvest v.1.0.173, dplyr v.1.0.753, and stringr v.1.4.0 packages60 (see Code S4) to query the online version of the WSC database to retrieve all synonyms for each species. Where the synonyms were listed with an abbreviated genus, we replace the abbreviation with the first instance of a genus that matched the first letter of the abbreviation.We combined the WSC data with a list manually retrieved from the Scorpion Files74 (https://www.ntnu.no/ub/scorpion-files/index.php; accessed 2021-09-19). For the uropygi species, we combined species listings from Integrated Taxonomic Information System (ITIS75; https://www.itis.gov/servlet/SingleRpt/RefRpt?search_type=source&search_id=source_id&search_id_value=1209 and https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&anchorLocation=SubordinateTaxa&credibilitySort=TWG%20standards%20met&rankName=ALL&search_value=82710&print_version=SCR&source=from_print#SubordinateTaxa; accessed 2021-09-19) and the Western Australian Museum76 (http://www.museum.wa.gov.au/catalogues-beta/browse/uropygi; accessed 2021-09-19). We were unable to source reliable data on all scorpion and uropygi synonyms; therefore, we used all names listed from all sources, but made note of those names considered nomen dubium. Our final keyword list contained 52,111 species, 94,184 different species names, with mean of 1.81 SE ± 0.01 terms per species (range 1–61). For summaries of total species, we relied on the species classed as accepted by the species databases (WSC, Scorpion Files, ITIS and the Western Australian Museum).Keyword searchWe successfully retrieved 3020 pages from 103 websites (mean = 28.78 SE ± 11.42, range: 1–1077), and used a further 4668 previously archived pages. To prepare each of the retrieved web pages for keyword searching, we removed all double spaces, html elements, and non-alpha-numeric characters, replacing them with single spaces (Code S5). For this process we used rvest v.1.0.173, XML v.3.99.0.877, and xml2 v.1.3.278 packages. This process increased the chances that genus and species epithets would appear in a compatible format when compared to our keyword list. The process was not able to repair abbreviated genera, or aid detection where genus and species epithet were not reported side-by-side.Due to the large number of species we were forced to adapt previous searching methods, instead implementing a hierarchical genus-species search (Code S6). We searched each retrieved page for any mention of genera, then only searched for species that were contained within that genus. We did not differentiate whether the genus was currently accepted or old, so if a species had ever belonged to a genus it was included in the second stage of the search. The specifics of the keyword search used case-insensitive fixed string matching (via the stringr v.1.4.0 package60). While collation string matching would have helped detect species with differently coded ligatures or diacritic marks, the occurrence of ligature and diacritic marks are infrequent in scientific names and did not warrant the considerably increased computational costs.Via the keyword search we recorded all instances of genus matches, species matches, the website ID, and the page number. We also collected the words surrounding a genus match (3 prior and four after) as a means of exploring common terms that may be used to describe the genera.We provide the compiled outputs from searching contemporary and historic pages in Data S2–S4. Prior to combining these two datasets into a final list of traded species, and summarising the overall patterns, we cleaned out instances of spurious genera and species detections. Predominantly this included short genera names that could appear at the start of longer words (e.g., terms such as: “rufus”, “Dia”, “Diana”, “Mala”, “Inca”, “Pero”, “May”, “Janus”, “Yukon”, “Lucia”, “Zora”, “Beata”, “Neon”, “Prima”, “Meta”, “Patri”, “Enna”, “Maso”, “Mica”, “Perro”; we already implemented a filter that required genera to be preceded by a space and thus these were not part of the species name). We are confident these genera should be excluded, as none had species detected within them.Trade database and third-party dataWe downloaded United States Fish and Wildlife Service’s LEMIS data compiled by79,80 from https://doi.org/10.5281/zenodo.3565869 (Data S5). We filtered the LEMIS data to records where the class was listed as Arachnida (Code S6).We downloaded the Gross imports data from the CITES trade database from the website and filtered to Class Arachnid, years 1975–202181 (accessed 2021-09-15; Data S6), and downloaded the CITES appendices filtered to arachnids82 (Data S7).We downloaded the IUCN Redlist assessments for arachnids from https://www.iucnredlist.org83 (accessed 2021-09-15; Data S8).Species summary and visualisationWe compiled all sources of trade data (online, LEMIS, CITES) into a single dataset detailing which genera/species had been detected in each source (Data S9 and Code S7). We used two criteria to determine detection, whether there was an exact match with an accepted genus/species or whether there was a match to any historically used genera/species name. Because of splits in genera, the “ANY genera” matching is likely overly generous. For broad summaries we rely on the “ANY species” name matching.We used cowplot v.1.1.184, ggplot2 v.3.3.585, ggpubr v.0.4.086, ggtext v.0.1.187, scales v.1.1.188, scico v.1.2.089, and UpSetR v.1.4.090 to generate summary visuals (Code S8; Code S9). We added additional details to the upset plot and modified the position of plot labels using Affinity Designer v.1.10.391. We also used Affinity Designer to create the Uropygid silhouette for Fig. 1. We obtained public domain licensed spider and scorpion silhouettes from http://phylopic.org/ (https://phylopic.org/image/d7a80fdc0-311f-4bc5-b4fc-1a45f4206d27/; http://phylopic.org/image/4133ae32-753e-49eb-bd31-50c67634aca1/).Descriptions and coloursWe explored the lag time between species descriptions, and their detection in LEMIS or online trade (Code S10). We relied on the description dates provided alongside the lists of species names. Unlike the broader summaries, we restricted explorations of lag times to species detected only via exact matches (operating under the assumption that newly described species traded swiftly after description would be using the modern accepted name). We distinguished between those species detected only in the complementary data, as the earliest trade date was not known; therefore, our summaries of lag time are based on those species detected in a particular year either via LEMIS or temporal online trade.Following a visual inspection of sites where we often noticed listings with either colour or localities (e.g., “Chilobrachys spp. “Electric Blue” 0.1.3. Chilobrachys sp. “Kaeng Krachan” 0.1.0. Chilobrachys spp. “Prachuap Khiri Khan”: Data S9). We explored the words that surrounded detected genera. After using the forcats v.0.5.192, stringr v.1.4.060, and tidytext v.0.3.193 package to compile common terms and remove English stop words, we determine colour was frequently mentioned (Code S11). To filter out non-colour words, we used wikipedia’s list of colours (https://en.wikipedia.org/wiki/List_of_colors:_N%E2%80%93Z). Once cleaned, we further removed terms that are ambiguously colour related (e.g., “space”, “racing”, “photo”, “boy”, “bean”, “blaze”, “jungle”, “mountain”, “dune”, “web”, “colour”, “rainforest”, “tree”, “sea”). We then summarised this data as the counts of instances where a genus appeared alongside a given colour term (n.b., counts are therefore impacted by any underlying imbalances in how many times a site mentioned a genus). We plotted all colours using the same hex codes listed on the wikipedia page, with the exception of “cobalt”, “grey”, “metallic”, “slate”, “electric”, “dark”, “sheen”, and “chocolate” that required manual linking to a hex code.Summary of trade numbersWe summarised LEMIS data using a number of filters (Code S12). Following3,4,94, we limited our summaries to items that feasibly can be considered to represent whole individuals (LEMIS code = Dead animal BOD, live eggs (EGL), dead specimen (DEA), live specimen (LIV), specimen (SPE), whole skin (SKI), entire animal trophy (TRO)). We describe the portion of trade that is prevented (i.e., seized, where disposition == “S”). We classed non-commercial trade as anything listed as for Biomedical research (M), Scientific (S), or Reintroduction/introduction into the wild (Y). For captive vs. wild summaries, we treated all Animals bred in captivity (C and F), Commercially bred (D), and Specimens originating from a ranching operation (R) as originating from captivity. We only included animals listed as Specimens taken from the wild (W) in wild counts. The few instances that fell outside of our defined captive vs. wild categorisation are treated as other. For summaries of wild capture per genus, we relied entirely on LEMIS’s listings of genera, making no effort to determine synonymisations. We did filter out those listed only as “Non-CITES entry” or NA. We used the countrycode v.1.3.095 package to help plot the LEMIS countries of origin. Taxonomy represents an ongoing challenge, we were limited to recognising the species listed in the aforementioned databases, generating synonym lists from these sources, and attempting to reconcile these lists. Rapid rates of species description means that compiling comprehensive lists can be challenging, and species may be traded under junior synonyms or old names, and newer descriptions may not have been added to sites96. We were also limited to platforms that advertised using text not images, as images can be challenging to identify accurately.MappingMapping species is challenging due to the lack of standardised data on species distributions. Spider distributions were mapped based on the data in the World Spider Catalogue (Data S12). Firstly, the localities associated with each species were collated into four spreadsheets based on the data provided in the WSC (WSC18; https://wsc.nmbe.ch/dataresources; accessed 2021-09-18), these listed (1) country, (2) region, (3) “to” (where the range was given as one country to another) and (4) Island.Before processing any “introduced” localities were removed, the four sheets were then checked for any simple spelling errors (in islands file) or mislistings (i.e., regions in the islands file). Country data were cross-referenced with the names of country provided by Thematic Mapper to standardise them (https://thematicmapping.org/; Data S11). This was done by uploading data into Arcmap and using joins and connects to connect it to the standard country name file, and any which could not be paired were corrected to ensure all could be successfully digitised.Regions were digitised based on accepted names of different regions and included 33 different regions (see supplements) for each of these the standard accepted area within each of these regions was searched online to determine the accepted boundaries. These were then selected from the Thematic mapper, exported and labelled with the corresponding region. Once this was completed for all 33 regions they were merged and exported to a geodatabase. The spreadsheet listing regional preferences of each species was also uploaded to Arcmap 10.3, then exported into the geodatabase, then connected to a regional map using joins and relates to connect the regional preferences from the spreadsheet to the shapefiles. The new dbf was then exported to provide a listing of each species and each country in the region it was connected to, and then copied into the same csv as the corrected country listings.For preferences listed as “to” we first separated each country listed in the “to” listings into a separate column, then developed a list of species and each of the countries listed in the “to” list (which was frequently between 5–6). These were then corrected to the standard names from thematic mapper for both countries and the regions used in the previous section. We then merged the countries and regions file and added fields of geometry in ArcMap to provide a centroid for each designated area. This table was then exported and joined and connected to the species in the “to” file. This data was then converted to point form and turned to a point file, then a minimum convex polygon (convex hulls) developed for each species to connect the regions between all those listed. These species specific minimum convex polygons were then intersected with the countries from Thematic mapper, and then dissolve was used to form a shapefile that just listed species and all the countries between those ranges. This was then exported and merged with the listings from countries and regions.The islands file included both independent islands (which needed names corrected, or archipelago names given) and those that fall within a national designation. For those islands we replaced the island name with that of the country, as listings of species may be particularly poor, and tiny non-independent islands are not visible in the global-scale analysis.This forth database table was then merged with the former three, and remove duplicates used to remove any duplicate entries, as species often had individual countries listed in additions to regions or “to”. This was then uploaded into Arcmap and exported to a geodatabase file then connected to the original Thematic mapper file and exported to the geodatabase to yield 134,187 connections between species and countries. This was then connected to our main analysis to include the trade status, and CITES and IUCN Redlist status for each species for further analysis.Scorpion data was considerably messier than that on the world spider catalogue. Firstly, we downloaded all scorpion data from iNaturalist and GBIF97,98 (search; scorpions), removed duplicates, then cross-referenced these with the thematic mapper file within Quantum GIS. Species listed in regions where they were clearly not native (i.e., a species listed in the UK when the rest of that species or genus were in Australia) were removed, and all extinct species were excluded.In addition, all the “update files” were downloaded from the “Scorpion files”, the PDFs collated then using smallpdf tools the tables were extracted into excel form and cleaned to include just species and country listing. This was added to the countries listed for species within99 and100 though this was restricted to a subset of species. The data were all collated into an excel file with the species name, and country listing. This was then added to all the data from https://scorpiones.pl/maps/. These maps have a good coverage of species countries, but are apparently no longer being updated (Jan Ove Rein pers comm 2021) hence the need for further data to provide complete and updated and comprehensive coverage for all species. Country names were then standardised based on the Thematic Mapper standards (Data S13 and Data S11). Species names were then cross-referenced to those listed in the Scorpion files, any not matching were checked as synonyms and converted to the accepted name (though the only collated data for Scorpion synonyms was on French-language Wikipedia, i.e., see https://fr.wikipedia.org/wiki/Bothriurus). Once all country and species names were corrected this provided a listing of 4059 species-country associations. These were then associated with country files in the same way as spiders. We plotted spider and scorpion species/genera, as well as LEMIS origins, using ggplot285, combining Thematic world border data (https://thematicmapping.org/) with summaries of species/genera/and trade levels. Species listed in a single-country (and thus more likely to be country endemic) were also counted using summary statistics, so that species most vulnerable to trade could be noted separately.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

  • in

    Integrated strategic planning and multi-criteria decision-making framework with its application to agricultural water management

    Abbasi, N., Bahramloo, R. & Movahedan, M. Strategic planning for remediation and optimization of irrigation and drainage networks: a case study of Iran. J. Agric. Agric. Sci. Proc. 4, 211–221 (2015).
    Google Scholar 
    Abdelhaleem, F., Basiouny, M. & Mahmoud, A. Application of remote sensing and geographic information systems in irrigation water management under water scarcity conditions in Fayoum, Egypt. J. Environ. Manag. 299, 113683 (2021).Article 

    Google Scholar 
    Akbari-Alashti, H., Bozorg-Haddad, O., Fallah-Mehdipour, E. & Mariño, M. A. Multi-reservoir real-time operation rules: a new genetic programming approach. Proc. Instit. Civil Eng. Water Manag. 167(10), 561–576 (2014).Article 

    Google Scholar 
    Akhmouch, A. & Correia, F. N. The 12 OECD principles on water governance: when science meets policy. J. Utilities Policy. 43, 14–20 (2016).Article 

    Google Scholar 
    Amblard, L. & Mann, C. Understanding collective action for the achievement of EU water policy objectives in agricultural landscapes: insights from the institutional design principles and integrated landscape management approaches. J. Environ. Sci. Policy. 125, 76–86 (2021).Article 

    Google Scholar 
    Babaeian, F., Delavar, M., Morid, S. & Srinivasan, R. Robust climate change adaptation pathways in agricultural water management. J. Agric. Water Manag. 252, 106904 (2021).Article 

    Google Scholar 
    Barbosa, M. C., Alam, K. & Mushtaq, S. Water policy implementation in the state of São Paulo, Brazil: key challenges and opportunities. J. Environ. Sci. Policy. 60, 11–18 (2016).Article 

    Google Scholar 
    Barrett, S. M. Implementation studies: time for a revival? Personal reflections on 20 years of implementation studies. J. Public Admin. 82(2), 249–269 (2004).MathSciNet 
    Article 

    Google Scholar 
    Baumgartner, R. J. & Korhonen, J. Strategic thinking for sustainable development. J. Sustain. Dev. 18(2), 71–75 (2010).Article 

    Google Scholar 
    Biswas, S. Measuring performance of healthcare supply chains in India: a comparative analysis of multi-criteria decision making methods. J. Decis. Making Appl. Manag. Eng. 3(2), 162–189 (2020).Article 

    Google Scholar 
    Biswas, S., Majumder, S., Pamucar, D. & Suman, D. An extended LBWA framework in picture fuzzy environment using actual score measures application in social enterprise systems. J. Enterp. Inform. Syst. (IJEIS) 17(4), 37–68 (2021).Article 

    Google Scholar 
    Biswas, S., Pamucar, D., Chowdhury, P. & Kar, S. A new decision support framework with picture fuzzy information: comparison of video conferencing platforms for higher education in India. J. Disc. Dyn. Nat. Soc. (2021).Bozorg-Haddad, O., Moradi-Jalal, M., Mirmomeni, M., Kholghi, M. K. H. & Mariño, M. A. Optimal cultivation rules in multi-crop irrigation areas. J. Irrig. Drain. 58(1), 38–49 (2009).Article 

    Google Scholar 
    Bozorg-Haddad, O., Loáiciga, H. A. & Zolghadr-Asli, B. A handbook on multi-attribute decision-making methods chapter (Wiley, 2021).MATH 
    Book 

    Google Scholar 
    Buckley, J. J. Fuzzy hierarchical analysis. J. Fuzzy Sets Syst. 17(3), 233–247 (1985).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Chang, H. H. & Huang, W. C. Application of a quantification SWOT analytical method. J. Math. Comput. Model. 43, 158–169 (2006).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Chen, C. T. Extension of the TOPSIS for group decision-making under fuzzy environment. J. Fuzzy Sets Syst. 114(1), 1–9 (2000).MATH 
    Article 

    Google Scholar 
    Conrad, C., Usman, M., Morper-Bush, L. & Schönbrodt-Stitt, S. Remote sensing-based assessments of land use, soil and vegetation status, crop production and water use in irrigation systems of the Aral Sea Basin. J. Water Sec. 11, 100078 (2020).Article 

    Google Scholar 
    David, F. R. Strategic management: concepts and cases (Prentice Hall, 2011).
    Google Scholar 
    Fallah-Mehdipour, E., Bozorg-Haddad, O., Beygi, S. & Mariño, M. A. Effect of utility function curvature of Young’s bargaining method on the design of WDNs. J. Water Resour. Manag. 25(9), 2197–2218 (2011).Article 

    Google Scholar 
    Fanghua, H. & Guanchun, C. Fuzzy multi-criteria group decision-making model based on weighted borda scoring method for watershed ecological risk management: a case study of three Gorges reservoir area of China. J. Water Resour. Manag. 24(10), 2139–2165 (2010).Article 

    Google Scholar 
    Gallego-Ayala, J. & Juızo, D. Strategic implementation of integrated water resources management in Mozambique: an A’WOT analysis. J. PhysChem. Earth. 36(14–15), 1103–1111 (2011).ADS 
    Article 

    Google Scholar 
    Gao, C. Y. & Peng, D. H. Consolidating SWOT analysis with nonhomogeneous uncertain preference information. J. Knowl. Based Syst. 24, 796–808 (2011).Article 

    Google Scholar 
    Gosling, S. N. & Arnell, N. W. A global assessment of the impact of climate change on water scarcity. J. Clim. Change. 134, 371–385 (2016).ADS 
    Article 

    Google Scholar 
    Gurel, M. & Tat, M. SWOT analysis: a theoretical review. J. Int. Soc. Res. 10(51), 994–1006 (2017).Article 

    Google Scholar 
    Hamdy, A., & Trisorio-Liuzzi, G. Water management strategies to combat drought in the semiarid regions. Water management for drought mitigation in the Mediterranean at the regional conference on arab water, Cairo, Egypt (2004).Hartmann, T. & Spit, T. Frontiers of land and water governance in urban regions. J. Water Int. 39(6), 791–797 (2014).Article 

    Google Scholar 
    He, L., Bao, J., Daccache, A., Wang, S. & Guo, P. Optimize the spatial distribution of crop water consumption based on a cellular automata model: a case study of the middle Heihe River basin, China. J. Sci. Total Environ. 720, 137569 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Hwang, C.L. & Yoon, K. Methods for multiple attribute decision making. In: Multiple attribute decision making: lecture notes in economics and mathematical systems, Springer, Heidelberg, Germany, vol 186 (1981).Hwang, F. P., Chen, S. J. & Hwang, C. L. Fuzzy multiple attribute decision making: methods and applications (Springer, 1992).MATH 

    Google Scholar 
    Islam, M. S., Sadiq, R. & Rodriguez, M. J. Evaluating water quality failure potential in water distribution systems: a fuzzy-TOPSIS-OWA-based methodology. J. Water Resour. Manag. 27(7), 2195–2216 (2013).Article 

    Google Scholar 
    Karabasevic, D., Zavadskas, E. K., Turskis, Z. & Stanujkic, D. The framework for the selection of personnel based on the SWARA and ARAS methods under uncertainties. J. Inform. 27(1), 49–65 (2016).Article 

    Google Scholar 
    Keršuliene, V., Zavadskas, E. K. & Turskis, Z. Selection of rational dispute resolution method by applying new step-wise weight assessment ratio analysis (Swara). J. Bus. Econ. Manag. 11(2), 243–258 (2010).Article 

    Google Scholar 
    Kim, S. et al. Developing spatial agricultural drought risk index with controllable geo-spatial indicators: a case study for South Korea and Kazakhstan. J. Disast. Risk Reduct. 54, 102056 (2021).Article 

    Google Scholar 
    Kousar, S., Zafar, A., Kausar, N., Pamucar, D. & Kattel, P. Fruit production planning in semiarid zones: a novel triangular intuitionistic fuzzy linear programming approach. J. Math. Prob. Eng. (2022).Lautze, J., de Silva, S., Giordano, M. & Sanford, L. Putting the cart before the horse: Water governance and IWRM. J. Nat. Resour. Forum Unit. Nat. Develop. 35(1), 1–8 (2011).Lee, K. L. & Lin, S. C. A fuzzy quantified SWOT procedure for environmental evaluation of an international distribution center. J. Inform. Sci. 178, 531–549 (2008).Article 

    Google Scholar 
    Loucks, D. P. Sustainable water resources management. Water International. Taylor & Francis, Milton Park (2000).Malczeweski, J. GIS and multicriteria decision analysis (Wiley, 1999).
    Google Scholar 
    Meza, I. et al. Drought risk for agricultural systems in South Africa: drivers, spatial patterns, and implications for drought risk management. J. Sci. Total Environ. 799, 149505 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    OECD. OECD principles on water governance. OECD Publishing (2015).Pahl-Wostl, C., Holtz, G., Kastens, B. & Knieper, C. Analyzing complex water governance regimes: the management and transition framework. J. Environ. Sci. Policy. 13(7), 571–581 (2010).Article 

    Google Scholar 
    Pahl-Wostl, C. et al. Environmental flows and water governance: managing sustainable water uses. J. Curr. Opin. Environm. Sustain. 5(3), 341–351 (2013).Article 

    Google Scholar 
    Pamucar, D., Torkayesh, A.E. & Biswas, S. Supplier selection in healthcare supply chain management during the COVID-19 pandemic: a novel fuzzy rough decision-making approach. J. Ann. Oper. Res. doi:https://doi.org/10.1007/s10479-022-04529-2(2022).Panchal, D., Chatterjee, P., Pamucar, D. & Yazdani, M. A novel fuzzy-based structured framework for sustainable operation and environmental friendly production in coal-fired power industry. J. Intell. Syst. doi: https://doi.org/10.1002/int.22507(2021).Peldschus, F., Zavadskas, E. K., Turskis, Z. & Tamosaitiene, J. Sustainable assessment of construction site by applying game theory. J. Eng. Econ. 21(3), 223–237 (2010).
    Google Scholar 
    Pérez-Blanco, C. & Gómez, C. Drought management plans and water availability in agriculture: a risk assessment model for a Southern European basin. J. Weather Clim. Extrem. 4, 11–18 (2014).Article 

    Google Scholar 
    Portoghese, I., Giannoccaro, G., Giordano, R. & Pagano, A. Modeling the impact of volumetric water pricing in irrigation districts with conjunctive use of water of surface and groundwater resources. J. Agric. Water Manag. 244, 106561 (2020).Article 

    Google Scholar 
    Rani, P., Mishra, A. R., Saha, A., Hezam, I. M. & Pamucar, D. Fermatean fuzzy Heronian mean operators and MEREC-based additive ratio assessment method: an application to food waste treatment technology selection. J. Intell. Syst. 37(3), 2612–2647 (2021).Article 

    Google Scholar 
    Rogers, P., & Hall, A.W. Effective water governance. J. Tech. Comm. Background Papers.7, Global Water Partnership (GWP) (2003).Rouillard, J. & Rinaudo, J. From State to user-based water allocations: an empirical analysis of institutions developed by agricultural user associations in France. J. Agric. Water Manag. 239, 106269 (2020).Article 

    Google Scholar 
    Ruzgys, A., Volvačiovas, R., Ignatavičius, Č & Turskis, Z. Integrated evaluation of external wall insulation in residential buildings using SWARA-TODIM MCDM method. J. Civil Eng. Manag. 20(1), 103–110 (2014).Article 

    Google Scholar 
    Saaty, T. L. A scaling method for priorities in hierarchical structures. J. Math. Psychol. 15, 234–281 (1977).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Saaty, T. L. The analytic hierarchy process (McGraw-Hill, 1980).MATH 

    Google Scholar 
    Saaty, T. L. The analytic hierarchy process: planning, priority setting, resource allocation (RWS Publication, 1996).MATH 

    Google Scholar 
    Saaty, T. L. Decision making with the analytic hierarchy process. Int. J. Serv. Sci. 1(1), 83–98 (2008).
    Google Scholar 
    Soltanjalili, M., Bozorg-Haddad, O. & Mariño, M. A. Effect of breakage level one in design of water distribution networks. J. Water Resour. Manag. 25(1), 311–337 (2011).Article 

    Google Scholar 
    Srdjevic, Z., Bajcetic, R. & Srdjevic, B. Identifying the criteria set for multi criteria decision making based on SWOT/PESTLE analysis: a case study of reconstructing a water intake structure. J. Water Resour. Manag. 26(12), 3379–3393 (2012).Article 

    Google Scholar 
    Stewart, R. A., Mohamed, S. & Daet, R. Strategic implementation of IT/IS projects in construction: a case study. J. Autom. Const. 11, 681–694 (2002).Article 

    Google Scholar 
    Thaler, T., Nordbeck, R. & Seher, W. Cooperation in flood risk management: understanding the role of strategic planning in two Austrian policy instruments. J. Environ. Sci. Policy. 114, 170–177 (2020).Article 

    Google Scholar 
    Thomson, J. et al. Spatial conservation action planning in heterogeneous landscapes. J. Biol. Conser. 250, 108735 (2020).Article 

    Google Scholar 
    Tortajada, C. Water governance: some critical issues. J. Water Resour. Develop. 26(2), 297–307 (2010).Article 

    Google Scholar 
    Tropp, H. Water governance: trends and needs for new capacity development. J. Water Policy. 9(2), 19–30 (2007).Article 

    Google Scholar 
    Van Laarhoven, P. J. & Pedrycz, W. A fuzzy extension of Saaty’s priority theory. J. Fuzzy Sets Syst. 11(1–3), 229–241 (1983).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Venot, J., Reddy, V. R. & Umapathy, D. Coping with drought in irrigated South India: Farmers’ adjustments in Nagarjuna Sagar. J. Agric. Water Manag. 97(10), 1434–1442 (2010).Article 

    Google Scholar 
    Vermillion, D.L. Irrigation sector reform in Asia: from patronage under participation to empowerment with partnership. In Asian Irrigation in Transition. New Delhi: Sage publications. https://www.cabdirect.org/cabdirect/abstract/20073076323(2003).Yazdani, M., Wen, Z., Liao, H., Banaitis, A. & Turskis, Z. A grey combined compromise solution (CoCoSo-G) method for supplier selection in construction management. J. Civil Eng. Manag. 25(8), 858–874 (2019).Article 

    Google Scholar 
    Yuksel, I. & Dagdeviren, M. Using the analytic network process (ANP) in a SWOT analysis: a case study for a textile firm. J. Inform. Sci. 177, 3364–3382 (2007).MATH 
    Article 

    Google Scholar 
    Zadeh, L. A. Fuzzy sets. J. Inform. Control. 8(3), 338–353 (1965).MATH 
    Article 

    Google Scholar 
    Zavadskas, E. K., Mardani, A., Turskis, Z., Jusoh, A. & Nor, K. M. Development of TOPSIS method to solve complicated decision-making problems: an overview on developments from 2000 to 2015. J. Inform. Technol. Dec. Making. 15(03), 645–682 (2016).Article 

    Google Scholar 
    Zuo, Q., Wu, Q., Yu, L., Li, Y. & Fan, Y. Optimization of uncertain agricultural management considering the framework of water, energy and food. J. Agric. Water Manag. 253, 106907 (2021).Article 

    Google Scholar  More

  • in

    Online pet shops are crawling with spiders captured in the wild

    Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain
    the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in
    Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles
    and JavaScript. More

  • in

    Plant growth-promoting rhizobacteria Burkholderia vietnamiensis B418 inhibits root-knot nematode on watermelon by modifying the rhizosphere microbial community

    Jones, J. T. et al. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathol. 14, 946–961. https://doi.org/10.1111/mpp.12057 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Collange, B., Navarrete, M., Peyre, G., Mateille, T. & Tchamitchian, M. Root-knot nematode (Meloidogyne) management in vegetable crop production: The challenge of an agronomic system analysis. Crop Prot. 30, 1251–1262. https://doi.org/10.1016/j.cropro.2011.04.016 (2011).Article 

    Google Scholar 
    Nyaku, S. T., Affokpon, A., Danquah, A. & Brentu, F. C. in Nematology–concepts, diagnosis and control (eds Mohammad Manjur Shah & Mohammad Mahamood) 153–182 (IntechOpen, 2017).Desaeger, J., Wram, C. & Zasada, I. New reduced-risk agricultural nematicides-rationale and review. J. Nematol. 52, 1 (2020).Article 

    Google Scholar 
    Dong, L. & Zhang, K. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288, 31–45. https://doi.org/10.1007/s11104-006-9009-3 (2006).CAS 
    Article 

    Google Scholar 
    Singh, S., Singh, B. & Singh, A. Nematodes: A threat to sustainability of agriculture. Procedia Environ. Sci. 29, 215–216. https://doi.org/10.1016/j.proenv.2015.07.270 (2015).Article 

    Google Scholar 
    Oka, Y. Mechanisms of nematode suppression by organic soil amendments—A review. Appl. Soil Ecol. 44, 101–115. https://doi.org/10.1016/j.apsoil.2009.11.003 (2010).Article 

    Google Scholar 
    Yue, X., Li, F. & Wang, B. Activity of four nematicides against Meloidogyne incognita race 2 on tomato plants. J. Phytopathol. 168, 399–404. https://doi.org/10.1111/jph.12904 (2020).CAS 
    Article 

    Google Scholar 
    Huang, W.-K. et al. Mutations in Acetylcholinesterase2 (ace 2) increase the insensitivity of acetylcholinesterase to fosthiazate in the root-knot nematode Meloidogyne incognita. Sci. Rep. 6, 1–9. https://doi.org/10.1038/srep38102 (2016).CAS 
    Article 

    Google Scholar 
    Yoon, Y., Kim, E.-S., Hwang, Y.-S. & Choi, C.-Y. Avermectin: Biochemical and molecular basis of its biosynthesis and regulation. Appl. Microbiol. Biotechnol. 63, 626–634. https://doi.org/10.1007/s00253-003-1491-4 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wolstenholme, A. J. & Rogers, A. Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131, S85–S95. https://doi.org/10.1017/S0031182005008218 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Haydock, P., Woods, S., Grove, I. & Hare, M. in Plant nematology (eds Roland N Perry & Maurice Moens) 459–479 (CABI, 2013).Forghani, F. & Hajihassani, A. Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Front. Plant Sci. 11, 1. https://doi.org/10.3389/fpls.2020.01125 (2020).Article 

    Google Scholar 
    Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Mhatre, P. H. et al. Plant growth promoting rhizobacteria (PGPR): a potential alternative tool for nematodes bio-control. Biocatal. Agr. Biotechnol. 17, 119–128. https://doi.org/10.1016/j.bcab.2018.11.009 (2019).Article 

    Google Scholar 
    Eissa, M. F. & Abd-Elgawad, M. M. in Biocontrol agents of phytonematodes (eds Tarique Hassan Askary & Paulo Roberto Martinelli) 217–243 (CABI, 2015).Luo, T., Hou, S., Yang, L., Qi, G. & Zhao, X. Nematodes avoid and are killed by Bacillus mycoides-produced styrene. J. Invertebr. Pathol. 159, 129–136. https://doi.org/10.1016/j.jip.2018.09.006 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Siddiqui, I. & Shaukat, S. Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production. J. Phytopathol. 152, 48–54. https://doi.org/10.1046/j.1439-0434.2003.00800.x (2004).Article 

    Google Scholar 
    Li, W. et al. Broad spectrum anti-biotic activity and disease suppression by the potential biocontrol agent Burkholderia ambifaria BC-F. Crop Protect. 21, 129–135. https://doi.org/10.1016/S0261-2194(01)00074-6 (2002).Article 

    Google Scholar 
    Khanna, K. et al. Role of plant growth promoting Bacteria (PGPRs) as biocontrol agents of Meloidogyne incognita through improved plant defense of Lycopersicon esculentum. Plant. Soil 436, 325–345. https://doi.org/10.1007/s11104-019-03932-2 (2019).CAS 
    Article 

    Google Scholar 
    Subedi, P., Gattoni, K., Liu, W., Lawrence, K. S. & Park, S.-W. Current utility of plant growth-promoting rhizobacteria as biological control agents towards plant-parasitic nematodes. Plants 9, 1167. https://doi.org/10.3390/plants9091167 (2020).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Oka, Y. et al. New strategies for the control of plant-parasitic nematodes. Pest Manag. Sci. 56, 983–988. https://doi.org/10.1002/1526-4998(200011)56:11%3c983::AID-PS233%3e3.0.CO;2-X (2000).CAS 
    Article 

    Google Scholar 
    Ralmi, N. H. A. A., Khandaker, M. M. & Mat, N. Occurrence and control of root knot nematode in crops: A review. Aust. J. Crop Sci. 11, 1649 (2016).Article 

    Google Scholar 
    Topalović, O. & Heuer, H. Plant-nematode interactions assisted by microbes in the rhizosphere. Curr. Issues Mol. Biol. 30, 75–88 (2019).Article 

    Google Scholar 
    Olanrewaju, O. S., Ayangbenro, A. S., Glick, B. R. & Babalola, O. O. Plant health: Feedback effect of root exudates-rhizobiome interactions. Appl. Microbiol. Biotechnol. 103, 1155–1166. https://doi.org/10.1007/s00253-018-9556-6 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Handley, K. M. et al. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. ISME J. 7, 800–816. https://doi.org/10.1038/ismej.2012.148 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Tang, Y. et al. Changes in nitrogen-cycling microbial communities with depth in temperate and subtropical forest soils. Appl. Soil Ecol. 124, 218–228. https://doi.org/10.1016/j.apsoil.2017.10.029 (2018).ADS 
    Article 

    Google Scholar 
    Babić, K. H. et al. Influence of different Sinorhizobium meliloti inocula on abundance of genes involved in nitrogen transformations in the rhizosphere of alfalfa (Medicago sativa L.). Environ. Microbiol. 10, 2922–2930 (2008).Article 

    Google Scholar 
    Ke, X. et al. Effect of inoculation with nitrogen-fixing bacterium Pseudomonas stutzeri A1501 on maize plant growth and the microbiome indigenous to the rhizosphere. Syst. Appl. Microbiol. 42, 248–260. https://doi.org/10.1016/j.syapm.2018.10.010 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hogan, G. et al. Microbiome analysis as a platform R&D tool for parasitic nematode disease management. ISME J. 13, 2664–2680. https://doi.org/10.1038/s41396-019-0462-4 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wu, Y. et al. Draft genome sequence of Stenotrophomonas maltophilia strain B418, a promising agent for biocontrol of plant pathogens and root-knot nematode. Genome Announc. 3, e00015-00015. https://doi.org/10.1128/genomeA.00015-15 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, Y. et al. Isolation and identification of nematicidal active substance from Burkholderia vietnamiensis B418. Plant Prot. 40, 65–69 (2014).
    Google Scholar 
    Li, S., Li, J., Xu, W., Chen, K. & Yang, H. Field efficacy test of biocontrol agent YKT41 and B418 against eggplant root-knot nematode disease. Shandong Sci. 24, 10–13 (2011).CAS 

    Google Scholar 
    Wang, Y., Wang, Z., Liu, B., Pan, M. & Li, J. Field trial of Burkholderia vietnamiensis and its composite microbial flora on cucumber root-knot nematode. Shandong Sci. 31, 39. https://doi.org/10.3976/j.issn.1002-4026.2018.01.007 (2018).Article 

    Google Scholar 
    Saad, A.-F.S., Massoud, M. A., Ibrahim, H. S. & Khalil, M. S. Management study for the root-knot nematodes, Meloidogyne incognita on tomatoes using fosthiazate and arbiscular mycorrhiza fungus. J. Adv. Agric. Res. 16, 137–147 (2011).
    Google Scholar 
    Huang, W.-K. et al. Efficacy evaluation of fungus Syncephalastrum racemosum and nematicide avermectin against the root-knot nematode Meloidogyne incognita on cucumber. PLoS ONE 9, e89717. https://doi.org/10.1371/journal.pone.0089717 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jayakumar, J. & Ramakrishnan, S. Evaluation of avermectin and its combination with nematicide and bioagents against root knot nematode, Meloidogyne incognita in tomato. J. Biol. Control 23, 317–319 (2009).
    Google Scholar 
    Moosavi, M. & Zare, R. in Biocontrol Agents of Phytonematodes (eds Tarique Hassan Askary & Paulo Roberto Martinelli) 423–445 (CABI, 2015).Berendsen, R. L., Pieterse, C. M. & Bakker, P. A. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486. https://doi.org/10.1016/j.tplants.2012.04.001 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Reinhold-Hurek, B., Bünger, W., Burbano, C. S., Sabale, M. & Hurek, T. Roots shaping their microbiome: Global hotspots for microbial activity. Annu. Rev. Phytopathol. 53, 403–424. https://doi.org/10.1146/annurev-phyto-082712-102342 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Ahemad, M. & Kibret, M. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. J. King Saud Univ.-Sci. 26, 1–20. https://doi.org/10.1016/j.jksus.2013.05.001 (2014).Article 

    Google Scholar 
    Ciccillo, F. et al. Effects of two different application methods of Burkholderia ambifaria MCI 7 on plant growth and rhizospheric bacterial diversity. Environ. Microbiol. 4, 238–245. https://doi.org/10.1046/j.1462-2920.2002.00291.x (2002).Article 
    PubMed 

    Google Scholar 
    Jo, H. et al. Response of soil bacterial community and pepper plant growth to application of Bacillus thuringiensis KNU-07. Agronomy 10, 551. https://doi.org/10.3390/agronomy10040551 (2020).CAS 
    Article 

    Google Scholar 
    Wang, J. et al. Traits-based integration of multi-species inoculants facilitates shifts of indigenous soil bacterial community. Front. Microbiol. 9, 1692. https://doi.org/10.3389/fmicb.2018.01692 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Welbaum, G. E., Sturz, A. V., Dong, Z. & Nowak, J. Managing soil microorganisms to improve productivity of agro-ecosystems. Crit. Rev. Plant Sci. 23, 175–193. https://doi.org/10.1080/07352680490433295 (2004).CAS 
    Article 

    Google Scholar 
    Mendes, R., Garbeva, P. & Raaijmakers, J. M. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634–663. https://doi.org/10.1111/1574-6976.12028 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Li, J. et al. Trichoderma harzianum inoculation reduces the incidence of clubroot disease in Chinese cabbage by regulating the rhizosphere microbial community. Microorganisms 8, 1325. https://doi.org/10.3390/microorganisms8091325 (2020).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Song, L. et al. Regular biochar and bacteria-inoculated biochar alter the composition of the microbial community in the soil of a Chinese fir plantation. Forests 11, 951. https://doi.org/10.3390/f11090951 (2020).Article 

    Google Scholar 
    Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100. https://doi.org/10.1126/science.1203980 (2011).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Palaniyandi, S. A., Yang, S. H., Zhang, L. & Suh, J.-W. Effects of actinobacteria on plant disease suppression and growth promotion. Appl. Microbiol. Biotechnol. 97, 9621–9636. https://doi.org/10.1007/s00253-013-5206-1 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Zhou, D. et al. Rhizosphere microbiomes from root knot nematode non-infested plants suppress nematode infection. Microbial Ecol. 78, 470–481. https://doi.org/10.1007/s00248-019-01319-5 (2019).CAS 
    Article 

    Google Scholar 
    Zou, Y. et al. Metagenomic insights into the effect of oxytetracycline on microbial structures, functions and functional genes in sediment denitrification. Ecotox. Environ. Safe. 161, 85–91. https://doi.org/10.1016/j.ecoenv.2018.05.045 (2018).CAS 
    Article 

    Google Scholar 
    Kong, Z. et al. Seasonal dynamics of the bacterioplankton community in a large, shallow, highly dynamic freshwater lake. Can. J. Microbiol. 64, 786–797. https://doi.org/10.1139/cjm-2018-0126 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bach, E. M., Williams, R. J., Hargreaves, S. K., Yang, F. & Hofmockel, K. S. Greatest soil microbial diversity found in micro-habitats. Soil Biol. Biochem. 118, 217–226. https://doi.org/10.1016/j.soilbio.2017.12.018 (2018).CAS 
    Article 

    Google Scholar 
    Wang, W. et al. Predatory Myxococcales are widely distributed in and closely correlated with the bacterial community structure of agricultural land. Appl. Soil Ecol. 146, 103365. https://doi.org/10.1016/j.apsoil.2019.103365 (2020).Article 

    Google Scholar 
    Schmidt, J. E., Kent, A. D., Brisson, V. L. & Gaudin, A. C. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome 7, 1–18. https://doi.org/10.1186/s40168-019-0756-9 (2019).Article 

    Google Scholar 
    Hu, W., Strom, N., Haarith, D., Chen, S. & Bushley, K. E. Mycobiome of cysts of the soybean cyst nematode under long term crop rotation. Front. Microbiol. 9, 386. https://doi.org/10.3389/fmicb.2018.00386 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, W.-H. & Liu, Q.-Z. Changes in fungal community and diversity in strawberry rhizosphere soil after 12 years in the greenhouse. J. Integ. Agric. 18, 677–687. https://doi.org/10.1016/S2095-3119(18)62003-9 (2019).Article 

    Google Scholar 
    Qiu, W. et al. Organic fertilization assembles fungal communities of wheat rhizosphere soil and suppresses the population growth of Heterodera avenae in the field. Front. Plant Sci. 11, 1225. https://doi.org/10.3389/fpls.2020.01225 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Schardl, C. L., Leuchtmann, A. & Spiering, M. J. Symbioses of grasses with seedborne fungal endophytes. Annu. Rev. Plant Biol. 55, 315–340. https://doi.org/10.1146/annurev.arplant.55.031903.141735 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Edgington, S., Thompson, E., Moore, D., Hughes, K. A. & Bridge, P. Investigating the insecticidal potential of Geomyces (Myxotrichaceae: Helotiales) and Mortierella (Mortierellacea: Mortierellales) isolated from Antarctica. Springerplus 3, 1–8. https://doi.org/10.1186/2193-1801-3-289 (2014).Article 

    Google Scholar 
    Yi, X. et al. Comparison of the abundance and community structure of N-Cycling bacteria in paddy rhizosphere soil under different rice cultivation patterns. Int. J. Mol. Sci. 19, 3772. https://doi.org/10.3390/ijms19123772 (2018).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Duval, S. et al. Electron transfer precedes ATP hydrolysis during nitrogenase catalysis. Proc. Natl. Acad. Sci. USA 110, 16414–16419. https://doi.org/10.1073/pnas.1311218110 (2013).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pham, V. T. et al. The plant growth-promoting effect of the nitrogen-fixing endophyte Pseudomonas stutzeri A15. Arch. Microbiol. 199, 513–517. https://doi.org/10.1007/s00203-016-1332-3 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Ouyang, Y., Evans, S. E., Friesen, M. L. & Tiemann, L. K. Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: a meta-analysis of field studies. Soil Biol. Biochem. 127, 71–78. https://doi.org/10.1016/j.soilbio.2018.08.024 (2018).CAS 
    Article 

    Google Scholar 
    Dynarski, K. A. & Houlton, B. Z. Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytol. 217, 1050–1061. https://doi.org/10.1111/nph.14905 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kastl, E.-M., Schloter-Hai, B., Buegger, F. & Schloter, M. Impact of fertilization on the abundance of nitrifiers and denitrifiers at the root–soil interface of plants with different uptake strategies for nitrogen. Biol. Fert. Soils 51, 57–64. https://doi.org/10.1007/s00374-014-0948-1 (2015).CAS 
    Article 

    Google Scholar 
    Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95. https://doi.org/10.1038/nature11336 (2012).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Southey, J. in Laboratory methods for work with plants and soil nematodes (ed JF Southey) 42–44 (HMSO, 1986).Ladner, D. C., Tchounwou, P. B. & Lawrence, G. W. Evaluation of the effect of ecologic on root knot nematode, Meloidogyne incognita, and tomato plant, Lycopersicon esculenum. Int. J. Environ. Res. Public Health 5, 104–110. https://doi.org/10.3390/ijerph5020104 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Niu, D.-D. et al. Application of PSX biocontrol preparation confers root-knot nematode management and increased fruit quality in tomato under field conditions. Biocontrol Sci. Technol. 26, 174–180. https://doi.org/10.1080/09583157.2015.1085489.18 (2016).Article 

    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucl. Acids Res. 41, e1–e1. https://doi.org/10.1093/nar/gks808 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Buee, M. et al. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184, 449–456. https://doi.org/10.1111/j.1469-8137.2009.03003.x (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Rösch, C., Mergel, A. & Bothe, H. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl. Environ. Microbiol. 68, 3818–3829. https://doi.org/10.1128/AEM.68.8.3818-3829.2002 (2002).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Throbäck, I. N., Enwall, K., Jarvis, Å. & Hallin, S. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol. Ecol. 49, 401–417. https://doi.org/10.1016/j.femsec.2004.04.011 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200. https://doi.org/10.1093/bioinformatics/btr381 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. https://doi.org/10.1038/nmeth.f.303 (2010).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acids Res. 41, D590–D596. https://doi.org/10.1093/nar/gks1219 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21. https://doi.org/10.1186/s13059-014-0550-8 (2014).CAS 
    Article 

    Google Scholar 
    Lozupone, C. & Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005 (2005).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parks, D. H., Tyson, G. W., Hugenholtz, P. & Beiko, R. G. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124. https://doi.org/10.1093/bioinformatics/btu494 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders

    Duarte C, Middelburg JJ, Caraco N. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences. 2005;2:1–8.CAS 
    Article 

    Google Scholar 
    Kloareg B, Quatrano RS. Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Ocean Mar Biol Annu Rev. 1988;26:259–315.
    Google Scholar 
    Fletcher HR, Biller P, Ross AB, Adams JMM. The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res. 2017;22:79–86.Article 

    Google Scholar 
    Deniaud-Bouët E, Hardouin K, Potin P, Kloareg B, Hervé C. A review about brown algal cell walls and fucose-containing sulfated polysaccharides: Cell wall context, biomedical properties and key research challenges. Carbohydr Polym. 2017;175:395–408.PubMed 
    Article 
    CAS 

    Google Scholar 
    Haug A, Larsen B, Smidsrød O. Uronic acid sequence in alginate from different sources. Carbohydr Res. 1974;32:217–225.CAS 
    Article 

    Google Scholar 
    Bruhn A, Janicek T, Manns D, Nielsen MM, Balsby TJS, Meyer AS, et al. Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitata—seasonal variation and impact of environmental factors. J Appl Phycol. 2017;29:3121–3137.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ponce NMA, Stortz CA. A comprehensive and comparative analysis of the fucoidan compositional data across the Phaeophyceae. Front Plant Sci. 2020;11:556312.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fleurence J. The enzymatic degradation of algal cell walls: A useful approach for improving protein accessibility? J Appl Phycol. 1999;11:313–314.CAS 
    Article 

    Google Scholar 
    Verhaeghe EF, Fraysse A, Guerquin-Kern JL, Wu TD, Devès G, Mioskowski C, et al. Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem. 2008;13:257–269.CAS 
    PubMed 
    Article 

    Google Scholar 
    Schiener P, Black KD, Stanley MS, Green DH. The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol. 2015;27:363–373.CAS 
    Article 

    Google Scholar 
    Deniaud-Bouët E, Kervarec N, Michel G, Tonon T, Kloareg B, Hervé C. Chemical and enzymatic fractionation of cell walls from Fucales: Insights into the structure of the extracellular matrix of brown algae. Ann Bot. 2014;114:1203–1216.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Michel G, Tonon T, Scornet D, Cock JM, Kloareg B. Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: Insights into the origin and evolution of storage carbohydrates in Eukaryotes. N. Phytol. 2010;188:67–81.CAS 
    Article 

    Google Scholar 
    Mann K. Ecology of coastal waters—A systems approach, Berkeley: University of California Press; 1982.Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T. The seaweed holobiont: Understanding seaweed-bacteria interactions. FEMS Microbiol Rev. 2013;37:462–476.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kirchman DL. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100.CAS 
    PubMed 

    Google Scholar 
    Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: The food connection. Front Microbiol. 2011;2:93.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–611.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wietz M, Wemheuer B, Simon H, Giebel HA, Seibt MA, Daniel R, et al. Bacterial community dynamics during polysaccharide degradation at contrasting sites in the Southern and Atlantic Oceans. Environ Microbiol. 2015;17:3822–3831.CAS 
    PubMed 
    Article 

    Google Scholar 
    Arnosti C, Wietz M, Brinkhoff T, Hehemann J-H, Probant D, Zeugner L, et al. The biogeochemistry of marine polysaccharides: sources, inventories, and bacterial drivers of the carbohydrate cycle. Ann Rev Mar Sci. 2020;13:9.1–9.28.
    Google Scholar 
    Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:490–495.Article 
    CAS 

    Google Scholar 
    Barbeyron T, Brillet-Guéguen L, Carré W, Carrière C, Caron C, Czjzek M, et al. Matching the diversity of sulfated biomolecules: Creation of a classification database for sulfatases reflecting their substrate specificity. PLoS One. 2016;11:1–33.Article 
    CAS 

    Google Scholar 
    Tang K, Lin Y, Han Y, Jiao N. Characterization of potential polysaccharide utilization systems in the marine Bacteroidetes Gramella flava JLT2011 using a multi-omics approach. Front Microbiol. 2017;8:220.PubMed 
    PubMed Central 

    Google Scholar 
    Zhu Y, Chen P, Bao Y, Men Y, Zeng Y, Yang J, et al. Complete genome sequence and transcriptomic analysis of a novel marine strain Bacillus weihaiensis reveals the mechanism of brown algae degradation. Sci Rep. 2016;6:38248.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thomas F, Bordron P, Eveillard D, Michel G. Gene expression analysis of Zobellia galactanivorans during the degradation of algal polysaccharides reveals both substrate-specific and shared transcriptome-wide responses. Front Microbiol. 2017;8:1808.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ficko-Blean E, Préchoux A, Thomas F, Rochat T, Larocque R, Zhu Y, et al. Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nat Commun. 2017;8:1685.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Koch H, Dürwald A, Schweder T, Noriega-Ortega B, Vidal-Melgosa S, Hehemann JH, et al. Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides. ISME J. 2019;13:92–103.CAS 
    PubMed 
    Article 

    Google Scholar 
    Bunse C, Koch H, Breider S, Simon M, Wietz M. Sweet spheres: succession and CAZyme expression of marine bacterial communities colonizing a mix of alginate and pectin particles. Environ Microbiol. 2021;23:3130–3148.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hehemann JH, Arevalo P, Datta MS, Yu X, Corzett CH, Henschel A, et al. Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes. Nat Commun. 2016;7:12860.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gralka M, Szabo R, Stocker R, Cordero OX. Trophic interactions and the drivers of microbial community assembly. Curr Biol. 2020;30:R1176–R1188.CAS 
    PubMed 
    Article 

    Google Scholar 
    Jiménez DJ, Dini-Andreote F, DeAngelis KM, Singer SW, Salles JF, van Elsas JD. Ecological insights into the dynamics of plant biomass-degrading microbial consortia. Trends Microbiol. 2017;25:788–796.PubMed 
    Article 
    CAS 

    Google Scholar 
    Kang S, Kim JK. Reuse of red seaweed waste by a novel bacterium, Bacillus sp. SYR4 isolated from a sandbar. World J Microbiol Biotechnol. 2015;31:209–217.PubMed 
    Article 

    Google Scholar 
    Jonnadula R, Verma P, Shouche YS, Ghadi SC. Characterization of Microbulbifer strain CMC-5, a new biochemical variant of Microbulbifer elongatus type strain DSM6810T isolated from decomposing seaweeds. Curr Microbiol. 2009;59:600–607.CAS 
    PubMed 
    Article 

    Google Scholar 
    Martin M, Barbeyron T, Martin R, Portetelle D, Michel G, Vandenbol M. The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol. 2015;6:1487.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dogs M, Wemheuer B, Wolter L, Bergen N, Daniel R, Simon M, et al. Rhodobacteraceae on the marine brown alga Fucus spiralis are abundant and show physiological adaptation to an epiphytic lifestyle. Syst Appl Microbiol. 2017;40:370–382.CAS 
    PubMed 
    Article 

    Google Scholar 
    Brunet M, le Duff N, Fuchs B, Amann R, Barbeyron T, Thomas F. Specific detection and quantification of the marine flavobacterial genus Zobellia on macroalgae using novel qPCR and CARD-FISH assays. Syst Appl Microbiol. 2021;44:126269.CAS 
    PubMed 
    Article 

    Google Scholar 
    Barbeyron T, L’Haridon S, Corre E, Kloareg B, Potin P. Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol. 2001;51:985–997.CAS 
    PubMed 
    Article 

    Google Scholar 
    Barbeyron T, Thiébaud M, Le Duff N, Martin M, Corre E, Tanguy G, et al. Zobellia roscoffensis sp. nov. and Zobellia nedashkovskayae sp. nov., two flavobacteria from the epiphytic microbiota of the brown alga Ascophyllum nodosum, and emended description of the genus Zobellia. Int J Syst Evol Microbiol. 2021;71:004913.Nedashkovskaya OI, Suzuki M, Vancanneyt M, Cleenwerck I, Lysenko AM, Mikhailov VV, et al. Zobellia amurskyensis sp. nov., Zobellia laminariae sp. nov. and Zobellia russellii sp. nov., novel marine bacteria of the family Flavobacteriaceae. Int J Syst Evol Microbiol. 2004;54:1643–1648.CAS 
    PubMed 
    Article 

    Google Scholar 
    Nedashkovskaya O, Otstavnykh N, Zhukova N, Guzev K, Chausova V, Tekutyeva L, et al. Zobellia barbeyronii sp. nov., a new member of the family Flavobacteriaceae, isolated from seaweed, and emended description of the species Z. amurskyensis, Z. laminariae, Z. russellii and Z. uliginosa. Diversity. 2021;13:520.CAS 
    Article 

    Google Scholar 
    Chernysheva N, Bystritskaya E, Stenkova A, Golovkin I. Comparative genomics and CAZyme genome repertoires of marine Zobellia amurskyensis KMM 3526T and Zobellia laminariae KMM 3676T. Mar Drugs. 2019;17:661.CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Chernysheva N, Bystritskaya E, Likhatskaya G, Nedashkovskaya O, Isaeva M. Genome-wide analysis of PL7 alginate lyases in the genus Zobellia. Molecules. 2021;26:2387.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Barbeyron T, Thomas F, Barbe V, Teeling H, Schenowitz C, Dossat C, et al. Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacteria: Example of the model algae-associated bacterium Zobellia galactanivorans DsijT. Environ Microbiol. 2016;18:4610–4627.CAS 
    PubMed 
    Article 

    Google Scholar 
    Potin P, Sanseau A, Le Gall Y, Rochas C, Kloareg B. Purification and characterization of a new k‐carrageenase from a marine Cytophaga‐like bacterium. Eur J Biochem. 1991;201:241–247.CAS 
    PubMed 
    Article 

    Google Scholar 
    Lami R, Grimaud R, Sanchez-Brosseau S, Six C, Thomas F, West NJ, et al. Marine bacterial models for experimental biology. In: Boutet A, Schierwater B, editors. Handbook of Marine Model Organisms in Experimental Biology. London: Taylor & Francis Ltd; 2021.Dudek M, Dieudonné A, Jouanneau D, Rochat T, Michel G, Sarels B, et al. Regulation of alginate catabolism involves a GntR family repressor in the marine flavobacterium Zobellia galactanivorans DsijT. Nucleic Acids Res. 2020;48:7786–7800.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thomas F, Lundqvist LCE, Jam M, Jeudy A, Barbeyron T, Sandström C, et al. Comparative characterization of two marine alginate lyases from Zobellia galactanivorans reveals distinct modes of action and exquisite adaptation to their natural substrate. J Biol Chem. 2013;288:23021–23037.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thomas F, Barbeyron T, Tonon T, Génicot S, Czjzek M, Michel G. Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides. Environ Microbiol. 2012;14:2379–94.CAS 
    PubMed 
    Article 

    Google Scholar 
    Jam M, Flament D, Allouch J, Potin P, Thion L, Kloareg B, et al. The endo-β-agarases AgaA and AgaB from the marine bacterium Zobellia galactanivorans: Two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem J. 2005;385:703–713.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hehemann JH, Correc G, Thomas F, Bernard T, Barbeyron T, Jam M, et al. Biochemical and structural characterization of the complex agarolytic enzyme system from the marine bacterium Zobellia galactanivorans. J Biol Chem. 2012;287:30571–30584.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Labourel A, Jam M, Jeudy A, Hehemann JH, Czjzek M, Michel G. The β-glucanase ZgLamA from Zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin. J Biol Chem. 2014;289:2027–2042.CAS 
    PubMed 
    Article 

    Google Scholar 
    Labourel A, Jam M, Legentil L, Sylla B, Hehemann JH, Ferrières V, et al. Structural and biochemical characterization of the laminarinase ZgLamCGH16 from Zobellia galactanivorans suggests preferred recognition of branched laminarin. Acta Crystallogr. 2015;D71:173–184.
    Google Scholar 
    Dorival J, Ruppert S, Gunnoo M, Orłowski A, Chapelais-Baron M, Dabin J, et al. The laterally-acquired GH5 ZgEngAGH5_4 from the marine bacterium Zobellia galactanivorans is dedicated to hemicellulose hydrolysis. Biochem J. 2018;475:3609–3628.PubMed 
    Article 

    Google Scholar 
    Groisillier A, Labourel A, Michel G, Tonon T. The mannitol utilization system of the marine bacterium Zobellia galactanivorans. Appl Environ Microbiol. 2015;81:1799–1812.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Fournier JB, Rebuffet E, Delage L, Grijol R, Meslet-Cladière L, Rzonca J, et al. The vanadium iodoperoxidase from the marine Flavobacteriaceae species Zobellia galactanivorans reveals novel molecular and evolutionary features of halide specificity in the vanadium haloperoxidase enzyme family. Appl Environ Microbiol. 2014;80:7561–7573.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Grigorian E, Groisillier A, Thomas F, Leblanc C, Delage L. Functional characterization of a L-2-haloacid dehalogenase from Zobellia galactanivorans DsijT suggests a role in haloacetic acid catabolism and a wide distribution in marine environments. Front Microbiol. 2021;12:725997.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhu Y, Thomas F, Larocque R, Li N, Duffieux D, Cladière L, et al. Genetic analyses unravel the crucial role of a horizontally acquired alginate lyase for brown algal biomass degradation by Zobellia galactanivorans. Environ Microbiol. 2017;19:2164–2181.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zablackis E, Perez J. A partially pyruvated carrageenan from hawaiian Grateloupia filicina (Cryptonemiales, Rhodophyta). Bot Mar. 1990;33:273–276.CAS 
    Article 

    Google Scholar 
    Filisetti-Cozzi T, Carpita N. Measurement of uronic acids without interference from neutral sugars. Anal Biochem. 1991;197:15162.Article 

    Google Scholar 
    Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal Biochem. 1973;54:484–489.CAS 
    PubMed 
    Article 

    Google Scholar 
    Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’Incecco A, Piccoli A, Totani L, et al. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology. 2007;17:541–552.CAS 
    PubMed 
    Article 

    Google Scholar 
    Jung SY, Oh TK, Yoon JH. Tenacibaculum aestuarii sp. nov., isolated from a tidal flat sediment in Korea. Int J Syst Evol Microbiol. 2006;56:1577–1581.CAS 
    PubMed 
    Article 

    Google Scholar 
    ZoBell C. Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res. 1941;4:75.
    Google Scholar 
    Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1.CAS 
    PubMed 
    Article 

    Google Scholar 
    Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–419.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vallenet D, Calteau A, Dubois M, Amours P, Bazin A, Beuvin M, et al. MicroScope: An integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res. 2020;48:D579–D589.CAS 
    PubMed 

    Google Scholar 
    Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Thomas F, Barbeyron T, Michel G. Evaluation of reference genes for real-time quantitative PCR in the marine flavobacterium Zobellia galactanivorans. J Microbiol Methods. 2011;84:61–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–26.CAS 
    PubMed 
    PubMed Central 
    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 
    CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. 2018. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.Lex A, Gehlenborg N, Strobelt H. UpSet: Visualization of intersecting sets. IEEE Trans Vis Comput Graph. 2014;20:1983–1992.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Krassowski M. krassowski/complex-upset. 2020. https://doi.org/10.5281/zenodo.3700590.Murtagh F, Legendre P. Ward’s hierarchical clustering method: clustering criterion and agglomerative algorithm. J Classif. 2014;31:274–295.Article 

    Google Scholar 
    Wickham H Use R! ggplot2: Elegant graphics for data analysis. 2nd ed. London: Springer; 2016.Kidby DK, Davidson DJ. Ferricyanide estimation of sugars in the nanomole range. Anal Biochem. 1973;55:321–325.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. DbCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–W101.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen X, Hu Y, Yang B, Gong X, Zhang N, Niu L, et al. Structure of lpg0406, a carboxymuconolactone decarboxylase family protein possibly involved in antioxidative response from Legionella pneumophila. Protein Sci. 2015;24:2070–2075.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Enke TN, Datta MS, Schwartzman J, Cermak N, Schmitz D, Barrere J, et al. Modular assembly of polysaccharide-degrading marine microbial communities. Curr Biol. 2019;29:1528–1535.e6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pollak S, Gralka M, Sato Y, Schwartzman J, Lu L, Cordero OX. Public good exploitation in natural bacterioplankton communities. Sci Adv. 2021;7:eabi4717.Pontrelli S, Szabo R, Pollak S, Schwartzman J, Ledezma D, Cordero OX, et al. Metabolic cross-feeding structures the assembly of polysaccharide degrading communities. Sci Adv. 2022;8:eabk3076.Holdt SL, Kraan S. Bioactive compounds in seaweed: Functional food applications and legislation. J Appl Phycol. 2011;23:543–597.CAS 
    Article 

    Google Scholar 
    Kawamura-Konishi Y, Watanabe N, Saito M, Nakajima N, Sakaki T, Katayama T, et al. Isolation of a new phlorotannin, a potent inhibitor of carbohydrate-hydrolyzing enzymes, from the brown alga Sargassum patens. J Agric Food Chem. 2012;60:5565–5570.CAS 
    PubMed 
    Article 

    Google Scholar 
    Garbary DJ, Brown NE, MacDonell HJ, Toxopeux J. Ascophyllum and its symbionts — A complex symbiotic community on North Atlantic shores. Algal and Cyanobacteria Symbioses. 2017:547–572.Pluvinage B, Grondin JM, Amundsen C, Klassen L, Moote PE, Xiao Y, et al. Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont. Nat Commun. 2018;9:1043.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Reintjes G, Arnosti C, Fuchs BM, Amann R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 2017;11:1640–1650.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hollants J, Leliaert F, de Clerck O, Willems A. What we can learn from sushi: A review on seaweed-bacterial associations. FEMS Microbiol Ecol. 2013;83:1–16.CAS 
    PubMed 
    Article 

    Google Scholar 
    Thomas F, Le Duff N, Wu TD, Cébron A, Uroz S, Riera P, et al. Isotopic tracing reveals single-cell assimilation of a macroalgal polysaccharide by a few marine Flavobacteria and Gammaproteobacteria. ISME J. 2021;15:3062–3075.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Datta MS, Sliwerska E, Gore J, Polz MF, Cordero OX. Microbial interactions lead to rapid micro-scale successions on model marine particles. Nat Commun. 2016;7:11965.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Enke TN, Leventhal GE, Metzger M, Saavedra JT, Cordero OX. Microscale ecology regulates particulate organic matter turnover in model marine microbial communities. Nat Commun. 2018;9:2743.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Sichert A, Cordero OX. Polysaccharide-bacteria Interactions from the lens of evolutionary ecology. Front Microbiol. 2021;12:705082.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sichert A, Corzett CH, Schechter M, Unfried F, Markert S, Becher D, et al. Verrucomicrobia use hundreds of enzymes to digest the algal polysaccharide fucoidan. Nat Microbiol. 2020;5:1026–1039.CAS 
    PubMed 
    Article 

    Google Scholar 
    Reisky L, Préchoux A, Zühlke MK, Bäumgen M, Robb CS, Gerlach N, et al. A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan. Nat Chem Biol. 2019;15:803–812.CAS 
    PubMed 
    Article 

    Google Scholar 
    Mabeau S, Kloareg B, Joseleau J-P. Fractionation and analysis of fucans from brown algae. Phytochemistry. 1990;29:2441–2445.CAS 
    Article 

    Google Scholar 
    Küpper FC, Kloareg B, Guern J, Potin P. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 2001;125:278–291.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Küpper FC, Müller DG, Peters AF, Kloareg B, Potin P. Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J Chem Ecol. 2002;28:2057–2081.PubMed 
    Article 

    Google Scholar 
    Leonard S, Hommais F, Nasser W, Reverchon S. Plant–phytopathogen interactions: bacterial responses to environmental and plant stimuli. Environ Microbiol. 2017;19:1689–1716.PubMed 
    Article 

    Google Scholar 
    Sato K, Naito M, Yukitake H, Hirakawa H, Shoji M, McBride MJ, et al. A protein secretion system linked to bacteroidete gliding motility and pathogenesis. PNAS. 2010;107:276–281.CAS 
    PubMed 
    Article 

    Google Scholar 
    Eckroat TJ, Greguske C, Hunnicutt DW. The type 9 secretion system is required for Flavobacterium johnsoniae biofilm formation. Front Microbiol. 2021;12:660887.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xie S, Tan Y, Song W, Zhang W, Qi Q, Lu X. N-glycosylation of a cargo protein C-terminal domain recognized by the type IX secretion system in Cytophaga hutchinsonii affects protein secretion and localization. Appl Environ Microbiol. 2022;88:e0160621.PubMed 
    Article 

    Google Scholar  More

  • in

    Barcoding and species delimitation of Iranian freshwater crabs of the Potamidae family (Decapoda: Brachyura)

    Yeo, D. C. J. et al. Global diversity of crabs (Crustacea: Decapoda: Brachyura). In Freshwater Animal Diversity Assessment (eds Balian, E. V. et al.). Hydrobiologia Vol. 595, 275–286 (2008).Álvarez, F. et al. Revision of the higher taxonomy of Neotropical freshwater crabs of the family Pseudothelphusidae, based on multigene and morphological analyses. Zool. J. Linn. Soc. 193, 973–1001 (2021).Article 

    Google Scholar 
    Ng, D. J. J. & Yeo, D. C. J. Terrestrial scavenging behaviour of the Singapore freshwater crab, Johora singaporensis (Crustacea: Brachyura: Potamidae). Nat. Singap. 6, 207–210 (2013).
    Google Scholar 
    Dobson, M. Freshwater crabs in Africa. Freshw. Forum 21, 3–26 (2004).
    Google Scholar 
    Dobson, M., Magana, A. M., Mathooko, J. M. & Ndegwa, F. K. Distribution and abundance of freshwater crabs (Potamonautes spp.) in rivers draining Mt Kenya, East Africa. Fundam. Appl. Limnol. 168, 271–279 (2007).Article 

    Google Scholar 
    Cumberlidge, N. et al. Freshwater crabs and the biodiversity crisis: Importance, threats, status, and conservation challenges. Biol. Conserv. 142, 1665–1673 (2009).Article 

    Google Scholar 
    Jouladeh-Roudbar, A., Ghanavi, H. R. & Doadrio, I. Ichthyofauna from Iranian freshwater: Annotated checklist, diagnosis, taxonomy, distribution and conservation. Assessment 21, 1–303 (2020).
    Google Scholar 
    Brandis, D., Storch, V. & Türkay, M. Taxonomy and zoogeography of the freshwater crabs of Europe, North Africa, and the Middle East (Crustacea, Decapoda, Potamidae). Senckenberg. Biol. 80, 5–56 (2000).
    Google Scholar 
    Keikhosravi, A. & Schubart, C. D. Description of a new freshwater crab species of the genus Potamon (Decapoda, Brachyura, Potamidae) from Iran, based on morphological and genetic characters. In Advances in Freshwater Decapod Systematics and Biology 115–133 (BRILL, 2014). https://doi.org/10.1163/9789004207615_008.Keikhosravi, A. & Schubart, C. D. Revalidation and redescription of Potamon elbursi Pretzmann, 1976 (Brachyura, Potamidae) from Iran, based on morphology and genetics. Open Life Sci. 9, 114–123 (2014).Article 

    Google Scholar 
    Keikhosravi, A., Naderloo, R. & Schubart, C. D. Morphological and molecular diversity in the freshwater crab Potamon ruttneri-P. gedrosianum species complex (Decapoda, Brachyura) indicate the need for taxonomic revision. Crustaceana 89, 129–139 (2016).Article 

    Google Scholar 
    Parvizi, E., Naderloo, R., Keikhosravi, A., Solhjouy-Fard, S. & Schubart, C. D. Multiple Pleistocene refugia and repeated phylogeographic breaks in the southern Caspian Sea region: Insights from the freshwater crab Potamon ibericum. J. Biogeogr. 45, 1234–1245 (2018).Article 

    Google Scholar 
    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Aust. J. Zool. https://doi.org/10.1071/ZO9660275 (1994).Article 

    Google Scholar 
    Kearse, M. et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).Article 

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

    Google Scholar 
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
    Article 

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

    Google Scholar 
    Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).CAS 
    Article 

    Google Scholar 
    Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783 (1985).Article 

    Google Scholar 
    Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876 (2013).CAS 
    Article 

    Google Scholar 
    Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).CAS 
    Article 

    Google Scholar 
    Masters, B. C., Fan, V. & Ross, H. A. Species delimitation—A geneious plugin for the exploration of species boundaries. Mol. Ecol. Resour. 11, 154–157 (2011).Article 

    Google Scholar  More

  • in

    Detection of spatial avoidance between sousliks and moles by combining field observations, remote sensing and deep learning techniques

    Our study combining field data and aerial imagery analysis clearly showed that the spotted souslik avoids close coexistence with another burrowing species, i.e. the European mole, in the period of low population abundance. This is the first study on this subject described in the available literature, as attention has been paid mainly to other parameters of the habitat so far14,18,20. The present results can (1) make a new contribution to the knowledge of the ecology of burrowing mammals and their interspecies relationships, (2) contribute to better designs of conservation and assessment of the quality of habitats of endangered burrowing mammals, and (3) indicate new possibilities of using remote sensing and deep learning methods in ecology and conservation. Below we will try to address each of these issues.The interaction between underground animals is not a new idea in ecology (e.g.22); however, this issue has not been analyzed for the mole and the souslik so far. This was probably related to the fact that the potential negative or positive relationships between these species are not intuitively obvious. The spatial distribution of underground tunnels of these animals is completely different: the mole builds an extensive network of horizontal tunnels close to the ground surface, while the souslik usually builds one deep nest burrow with a vertical entrance and possibly a small number of shallow safety burrows near the nest burrow. Moreover, the food preferences of the souslik and the mole differ, i.e. the former is mainly a herbivore, while the latter is an obligatory predator. There are also clear differences in the annual cycle: the mole is active all year round, and the souslik hibernates in an underground nest for about half a year from October to March. Thus, it seems that the emergence of competitive relationships between these two species is unlikely. Our study shows, however, that these species avoid each other in space, which raises the question of the mechanism of this relationship. Based on the knowledge of the biology of both species, some hypothetical mechanisms can be proposed.Although they are colonial animals, sousliks inhabit burrows alone (except for mother and offspring) and they have a strong behavioural trait of a negative reaction to the presence of other animals in their burrows and their close vicinity14,23. The negative reaction to other sousliks is a reflection of the intraspecific competition in the population and the territoriality of individuals. It is regulated by odour signals and the social structure of the population30,31. Koshev32 described aggressive reactions of free-ranging European sousliks to other vertebrate species that appeared near burrows: towards the reptile Lacerta trilineata, the bird Corvus frugilegus, and the mammal Mustela nivalis. Theoretically, the mole can get into the souslik’s burrow unintentionally when digging new tunnels. For souslik, the presence of moles in their nest burrow means a violation of its strictly defended territory and is probably a highly stressful episode. It can therefore be assumed that sousliks should choose places outside areas of frequent occurrence of other burrowing mammals to set up a nest burrow.It remains an open question whether avoidance of areas where the mole is often present may be important for the souslik during winter hibernation. Theoretically, the presence of moles in souslik burrows during hibernation may disturb this process and cause waking up and energy-consuming increases in metabolism, which may reduce winter survival. It is also unknown whether the mole can be a predator for the souslik during winter hibernation. Remains of rodent species were found in the digestive tracts of moles33; therefore, at least theoretically, the mole may use such a food source. On the other hand, remains of vertebrates, including the remains of moles, were sometimes found in the stomachs of sousliks18. The relationship between the souslik and the mole may therefore be more complex and require further research focused on this issue. It is possible that the moles can avoid the souslik colonies as well. This scenario seems also realistic, since the moles home ranges are likely much more dynamic than that of sousliks, that likely benefit from dwelling within an existing colony of the conspecifics.The spotted souslik protection requires the designation of special areas of conservation16. A number of various conservation activities are also routinely undertaken for this species, including regular monitoring of the population size, habitat monitoring, mowing, reduction of predation risk, and application of more invasive methods such as reintroduction. Similar activities are also performed for a closely related species, i.e. the European souslik Spermophilus citellus, in Europe. Importantly, in the current guidelines of souslik conservation, the issue of the competition with other species and its impact on spatial distribution is not considered. In turn, there is evidence in the literature that interspecies interactions may be important for the souslik population21. In periods of low abundance, when the survival of the population is at risk, the sousliks may have different habitat preferences than in periods of the abundant population20. It seems, therefore, that nowadays, when the souslik most often forms small populations, more attention should be paid to a wider range of factors and threats that may determine longer term population trends or the health condition, survival, and abundance of their colonies.Our study indicates that, in the period of low population abundance, the presence of other burrowing species may be an important factor determining the distribution of sousliks. This observation shows that in addition to the assessment of the area and condition of the habitat the presence of other potentially competitive species should also be taken into account in the analysis of population survival. In such a case, the actual area of habitats suitable for sousliks in a given location may turn out to be much lower than assumed. In our study area, the habitat suitable for the souslik was reduced from 105 ha to approx. 65 ha, i.e. by nearly 38%, but it probably is even smaller (compare Fig. 8). This observation has consequences for improvement of the reintroduction methods of sousliks (or other burrowing mammals), which are constantly of scientific interest20,34,35. Our results indicate that the reintroduction of sousliks should be carried out in places where there is the lowest probability of competition for resources including even shelter or space with other burrowing species and where adequate space for the settlement of the population is ensured.So far, investigations of the distribution of small burrowing mammals have been based on laborious field studies involving site inspections by trained observers (e.g.36,37,38). Our results show that, in certain conditions, high-resolution imagery can be successfully used to support studies of the distribution of such animals. As reported by other authors (e.g.7,10,12), however, such animals must produce clear signs of their presence in the environment. Evidence of the presence of the European mole, i.e. mounds of soil, in short vegetation habitats has shown that remote sensing can detect moles and their area of occupancy successfully. The advantage of these markers of the presence of moles is that the mounds are redundant and quite durable and can be visible in the environment for up to several months.By combining field research and remote sensing, it is also possible to study more sophisticated ecological issues, e.g. interspecies interactions. In this work, the remote estimation of the distribution of moles facilitated estimation of the actual habitat available to the souslik and excluded areas with the lowest probability of its occurrence. As a result, the population may be monitored more economically. Since the conservation guidelines recommend monitoring souslik populations by means of laborious inspections of transects, the indication of areas with no burrows may significantly reduce the amount of fieldwork without negative consequences for the accuracy of results. Some areas of the souslik occurrence are large, e.g. Świdnik (105 ha) or Pastwiska nad Huczwą (150 ha), and every 10 ha to be monitored means one day’s work for one observer (according to the calculations presented in the results). Our study showed that when the area of the occurrence of moles is excluded from the monitoring (Fig. 8), the error in estimating the size of the souslik population will be relatively small (0.9–8.7%). At the same time, the time devoted to the research can be limited by 14% or 38%, respectively. This suggests that our method can contribute to improved monitoring and management of these protected species, especially that souslik monitoring requires considerable research effort and has to be carried out twice a year.However, mole mounds may be underestimated by remote sensing, which can be seen in Fig. 7. Small mole mounds that are easily identified during field research may not be noticed by remote sensing. Such underestimation does not constitute a critical threat to the determination of the mole area according to the scheme shown in Fig. 8, since its marks are highly redundant. However, since there is currently little research on this subject, we recommend combining field research and remote sensing in assessments similar to ours. Finally, it is worth noting that, for a better understanding of the issue of the interactions between souslik and other burrowing species, it is advisable to use another remote sensing technique—telemetry. Telemetry studies are successfully conducted in Bulgarian souslik populations34 and their combination with studies of habitat selectivity dependent on other burrowing species may provide new and valuable insight into this issue. More

  • in

    Tropical tree mortality has increased with rising atmospheric water stress

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

    Google Scholar 
    Hubau, W. et al. Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature 579, 80–87 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zuleta, D., Duque, A., Cardenas, D., Muller-Landau, H. C. & Davies, S. J. Drought-induced mortality patterns and rapid biomass recovery in a terra firme forest in the Colombian Amazon. Ecology 98, 2538–2546 (2017).PubMed 
    Article 

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

    Google Scholar 
    Powers, J. S. et al. A catastrophic tropical drought kills hydraulically vulnerable tree species. Glob. Chang. Biol. 26, 3122–3133 (2020).PubMed 
    Article 

    Google Scholar 
    Bennett, A. C. et al. Resistance of African tropical forests to an extreme climate anomaly. Proc. Natl Acad. Sci. USA 118, e2003169118 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brodribb, T. J., Powers, J., Cochard, H. & Choat, B. Hanging by a thread? Forests and drought. Science 368, 261–266 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    McDowell, N. G. et al. Pervasive shifts in forest dynamics in a changing world. Science 368, (2020).Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Matthews, H. D. et al. An integrated approach to quantifying uncertainties in the remaining carbon budget. Commun. Earth Environ. 2, 7 (2021).Article 

    Google Scholar 
    Girardin, C. A. J. et al. Nature-based solutions can help cool the planet—if we act now. Nature 593, 191–194 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Friedlingstein, P. et al. Earth Syst. Sci. Data 14, 1917–2005 (2022)
    Google Scholar 
    Choat, B. et al. Triggers of tree mortality under drought. Nature 558, 531–539 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rowland, L. et al. Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528, 119–122 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lloyd, J. & Farquhar, G. D. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Phil. Trans. R. Soc. B 363, 1811–1817 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    O’Sullivan, O. S. et al. Thermal limits of leaf metabolism across biomes. Glob. Chang. Biol. 23, 209–223 (2017).PubMed 
    Article 

    Google Scholar 
    Grossiord, C. et al. Plant responses to rising vapor pressure deficit. New Phytol. 226, 1550–1566 (2020).PubMed 
    Article 

    Google Scholar 
    Rifai, S. W., Li, S. & Malhi, Y. Coupling of El Niño events and long-term warming leads to pervasive climate extremes in the terrestrial tropics. Environ. Res. Lett. 14, 105002 (2019).CAS 
    Article 

    Google Scholar 
    Rifai, S. W. et al. ENSO drives interannual variation of forest woody growth across the tropics. Phil. Trans. R. Soc. B 373, 20170410 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Smith, M. N. et al. Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nat. Plants 6, 1225–1230 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Malhi, Y. et al. Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proc. Natl Acad. Sci. USA 106, 20610–20615 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McDowell, N., Allen, C. D. & Anderson‐Teixeira, K. Drivers and mechanisms of tree mortality in moist tropical forests. New Phytol. 219, 851–869 (2018).PubMed 
    Article 

    Google Scholar 
    McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178, 719–739 (2008).PubMed 
    Article 

    Google Scholar 
    Bauman, D. et al. Tropical tree growth sensitivity to climate is driven by species intrinsic growth rate and leaf traits. Glob. Chang. Biol. 28, 1414–1432 (2022).PubMed 
    Article 

    Google Scholar 
    Esquivel-Muelbert, A. et al. Tree mode of death and mortality risk factors across Amazon forests. Nat. Commun. 11, 5515 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anderegg, W. R. L., Anderegg, L. D. L., Kerr, K. L. & Trugman, A. T. Widespread drought-induced tree mortality at dry range edges indicates that climate stress exceeds species’ compensating mechanisms. Glob. Chang. Biol. 25, 3793–3802 (2019).PubMed 
    Article 

    Google Scholar 
    Aguirre-Gutiérrez, J. et al. Drier tropical forests are susceptible to functional changes in response to a long-term drought. Ecol. Lett. 22, 855–865 (2019).PubMed 
    Article 

    Google Scholar 
    Aguirre-Gutiérrez, J. et al. Long-term droughts may drive drier tropical forests towards increased functional, taxonomic and phylogenetic homogeneity. Nat. Comm. 11, 3346 (2020).Article 

    Google Scholar 
    Meir, P., Mencuccini, M. & Dewar, R. C. Drought-related tree mortality: addressing the gaps in understanding and prediction. New Phytol. 207, 28–33 (2015).PubMed 
    Article 

    Google Scholar 
    Sullivan, M. J. P. et al. Long-term thermal sensitivity of Earth’s tropical forests. Science 368, 869–874 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yuan, W. et al. Increased atmospheric vapor pressure deficit reduces global vegetation growth. Sci. Adv. 5, eaax1396 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McMahon, S. M., Arellano, G. & Davies, S. J. The importance and challenges of detecting changes in forest mortality rates. Ecosphere 10, e02615 (2019).Article 

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

    Google Scholar 
    Trugman, A. T., Anderegg, L. D. L., Anderegg, W. R. L., Das, A. J. & Stephenson, N. L. Why is tree drought mortality so hard to predict? Trends Ecol. Evol. 36, 520–532 (2021).PubMed 
    Article 

    Google Scholar 
    Phillips, O. L. et al. Drought–mortality relationships for tropical forests. New Phytol. 187, 631–646 (2010).PubMed 
    Article 

    Google Scholar 
    Aleixo, I. et al. Amazonian rainforest tree mortality driven by climate and functional traits. Nat. Clim. Change 9, 384–388 (2019).Article 

    Google Scholar 
    Lingenfelder, M. & Newbery, D. M. On the detection of dynamic responses in a drought-perturbed tropical rainforest in Borneo. Plant Ecol. 201, 267–290 (2009).Article 

    Google Scholar 
    McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011).PubMed 
    Article 

    Google Scholar 
    Zuleta, D. et al. Individual tree damage dominates mortality risk factors across six tropical forests. New Phytol. 233, 705–721 (2022).PubMed 
    Article 

    Google Scholar 
    Fontes, C. G. et al. Dry and hot: the hydraulic consequences of a climate change-type drought for Amazonian trees. Phil. Trans. R. Soc. B 373, 20180209 (2018).Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).PubMed 
    Article 

    Google Scholar 
    Peters, J. M. R. et al. Living on the edge: a continental-scale assessment of forest vulnerability to drought. Glob. Chang. Biol. 27, 3620–3641 (2021).PubMed 
    Article 

    Google Scholar 
    Yang, J., Cao, M. & Swenson, N. G. Why functional traits do not predict tree demographic rates. Trends Ecol. Evol. 33, 326–336 (2018).PubMed 
    Article 

    Google Scholar 
    Espírito-Santo, F. D. B. et al. Size and frequency of natural forest disturbances and the Amazon forest carbon balance. Nat. Commun. 5, 3434 (2014).PubMed 
    Article 

    Google Scholar 
    Chambers, J. Q. et al. The steady-state mosaic of disturbance and succession across an old-growth Central Amazon forest landscape. Proc. Natl Acad. Sci. USA 110, 3949–3954 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rifai, S. W. et al. Landscape-scale consequences of differential tree mortality from catastrophic wind disturbance in the Amazon. Ecol. Appl. 26, 2225–2237 (2016).PubMed 
    Article 

    Google Scholar 
    López, J., Way, D. A. & Sadok, W. Systemic effects of rising atmospheric vapor pressure deficit on plant physiology and productivity. Glob. Chang. Biol. 27, 1704–1720 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brando, P. M. et al. Abrupt increases in Amazonian tree mortality due to droughttextendashfire interactions. Proc. Natl Acad. Sci. USA 111, 6347–6352 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Phillips, O. L. et al. Pattern and process in Amazon tree turnover, 1976–2001. Phil. Trans. R. Soc. Lond. B 359, 381–407 (2004).CAS 
    Article 

    Google Scholar 
    Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change 8, 579–587 (2018).Article 

    Google Scholar 
    Andrus, R. A., Chai, R. K., Harvey, B. J., Rodman, K. C. & Veblen, T. T. Increasing rates of subalpine tree mortality linked to warmer and drier summers. J. Ecol. 109, 2203–2218 (2021).Article 

    Google Scholar 
    Murphy, H. T., Bradford, M. G., Dalongeville, A., Ford, A. J. & Metcalfe, D. J. No evidence for long-term increases in biomass and stem density in the tropical rain forests of Australia. J. Ecol. 101, 1589–1597 (2013).Article 

    Google Scholar 
    Bennett, A. C., McDowell, N. G., Allen, C. D. & Anderson-Teixeira, K. J. Larger trees suffer most during drought in forests worldwide. Nat. Plants 1, 15139 (2015).PubMed 
    Article 

    Google Scholar 
    Chitra-Tarak, R. et al. Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest. New Phytol. 231, 1798–1813 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anderegg, W. R. L. et al. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl Acad. Sci. USA 113, 5024–5029 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Taylor, T. C., Smith, M. N., Slot, M. & Feeley, K. J. The capacity to emit isoprene differentiates the photosynthetic temperature responses of tropical plant species. Plant Cell Environ. 42, 2448–2457 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Arellano, G., Zuleta, D. & Davies, S. J. Tree death and damage: a standardized protocol for frequent surveys in tropical forests. J. Veg. Sci. 32, e12981 (2021).Article 

    Google Scholar 
    Bradford, M. G., Murphy, H. T., Ford, A. J., Hogan, D. L. & Metcalfe, D. J. Long-term stem inventory data from tropical rain forest plots in Australia. Ecology 95, 2362 (2014).Article 

    Google Scholar 
    Johnson, D. J. et al. Climate sensitive size-dependent survival in tropical trees. Nat. Ecol. Evol. 2, 1436–1442 (2018).PubMed 
    Article 

    Google Scholar 
    Needham, J., Merow, C., Chang-Yang, C.-H., Caswell, H. & McMahon, S. M. Inferring forest fate from demographic data: from vital rates to population dynamic models. Proc. Biol. Sci. 285, 20172050 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Lewis, S. L. et al. Tropical forest tree mortality, recruitment and turnover rates: calculation, interpretation and comparison when census intervals vary. J. Ecol. 92, 929–944 (2004).Article 

    Google Scholar 
    Reeves, J., Chen, J., Wang, X. L., Lund, R. & Lu, Q. Q. A review and comparison of changepoint detection techniques for climate data. J. Appl. Meteorol. Climatol. 46, 900–915 (2007).Article 

    Google Scholar 
    Clark, J. S., Bell, D. M., Kwit, M. C. & Zhu, K. Competition-interaction landscapes for the joint response of forests to climate change. Glob. Chang. Biol. 20, 1979–1991 (2014).PubMed 
    Article 

    Google Scholar 
    Oliva, J., Stenlid, J. & Martínez-Vilalta, J. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol. 203, 1028–1035 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Franklin, J. F., Shugart, H. H. & Harmon, M. E. Tree death as an ecological process. Bioscience 37, 550–556 (1987).Article 

    Google Scholar 
    Yanoviak, S. P. et al. Lightning is a major cause of large tree mortality in a lowland neotropical forest. New Phytol. 225, 1936–1944 (2020).PubMed 
    Article 

    Google Scholar 
    Preisler, Y., Tatarinov, F., Grünzweig, J. M. & Yakir, D. Seeking the ‘point of no return’ in the sequence of events leading to mortality of mature trees. Plant Cell Environ. 44, 1315–1328 (2020).PubMed 
    Article 

    Google Scholar 
    Aragão, L. E. O. C. et al. Spatial patterns and fire response of recent Amazonian droughts. Geophys. Res. Lett. 34, L07701 (2007).Article 

    Google Scholar 
    Malhi, Y. et al. The linkages between photosynthesis, productivity, growth and biomass in lowland Amazonian forests. Glob. Chang. Biol. 21, 2283–2295 (2015).PubMed 
    Article 

    Google Scholar 
    Hutchinson, M. F., Xu, T., Kesteven, J. L., Marang, I. J. & Evans, B. J.ANUClimate v2.0, NCI Australia. https://doi.org/10.25914/60a10aa56dd1b (2021).Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Carscadden, K. A. et al. Niche breadth: causes and consequences for ecology, evolution, and conservation. Q. Rev. Biol. 95, 179–214 (2020).Article 

    Google Scholar 
    Swenson, N. G. et al. A reframing of trait–demographic rate analyses for ecology and evolutionary biology. Int. J. Plant Sci. 181, 33–43 (2020).Article 

    Google Scholar 
    Morueta-Holme, N. et al. Habitat area and climate stability determine geographical variation in plant species range sizes. Ecol. Lett. 16, 1446–1454 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brum, M. et al. Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest. J. Ecol. 107, 318–333 (2019).Article 

    Google Scholar 
    Chitra-Tarak, R. et al. The roots of the drought: hydrology and water uptake strategies mediate forest-wide demographic response to precipitation. J. Ecol. 106, 1495–1507 (2018).Article 

    Google Scholar 
    Boria, R. A., Olson, L. E., Goodman, S. M. & Anderson, R. P. Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol. Modell. 275, 73–77 (2014).Article 

    Google Scholar 
    Farquhar, G. D., von Caemmerer, S. & Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90 (1980).CAS 
    PubMed 
    Article 

    Google Scholar 
    Duursma, R. A. Plantecophys—an R package for analysing and modelling leaf gas exchange data. PLoS ONE 10, e0143346 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    De Kauwe, M. G. et al. A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytol. 210, 1130–1144 (2016).PubMed 
    Article 

    Google Scholar 
    Bloomfield, K. J. et al. The validity of optimal leaf traits modelled on environmental conditions. New Phytol. 221, 1409–1423 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    McElreath, R. Statistical Rethinking: A Bayesian Course with Examples in R and STAN (CRC Press, 2020).“RStan: the R interface to Stan.” R package version 2.21.2. http://mc-stan.org/ (Stan Development Team, 2020).Bürkner, P.-C. brms: An R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).Article 

    Google Scholar 
    R Core Team. R: a language and environment for statistical computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2021).Dinerstein, E. et al. An ecoregion-based approach to protecting half the terrestrial realm. Bioscience 67, 534–545 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More