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    Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei)

    1.Weber, A. W. & Vedder, A. Population dynamics of the Virunga gorillas: 1959–1978. Biol. Conserv. 26, 341–366 (1983).Article 

    Google Scholar 
    2.Granjon, A.-C. et al. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 23, 455–465 (2020).Article 

    Google Scholar 
    3.Gray, M. et al. Virunga Massif Mountain Gorilla Census—2010 Summary Report (IGCP & Partners, 2010).
    Google Scholar 
    4.Gray, M. et al. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 158, 230–238 (2013).Article 

    Google Scholar 
    5.Robbins, M. M. et al. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One 6, e19788 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Hickey, J. R., Granjon, A.-C. & Vigilant, L. Virunga 2015–2016 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Illegal Activities (IGCP & Partners, 2019).
    Google Scholar 
    7.Kalpers, J. et al. Gorillas in the crossfire: Population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37, 326–337 (2003).Article 

    Google Scholar 
    8.Robbins, M. M., Gray, M., Kagoda, E. & Robbins, A. M. Population dynamics of the Bwindi mountain gorillas. Biol. Conserv. 142, 2886–2895 (2009).Article 

    Google Scholar 
    9.Hickey, J. R., Uzabaho, E. & Akantorana, M. Bwindi-Sarambwe EM 2018 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Human Activities 40 (GVTC, IGCP & Partners, 2019).
    Google Scholar 
    10.Roy, J. et al. Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei). Biol. Conserv. 180, 249–261 (2014).Article 

    Google Scholar 
    11.McNeilage, A. J. Mountain Gorillas in the Virunga Volcanoes: Ecology and Carrying Capacity (University of Bristol, 1995).
    Google Scholar 
    12.Caillaud, D., Ndagijimana, F., Giarrusso, A. J., Vecellio, V. & Stoinski, T. S. Mountain gorilla ranging patterns: Influence of group size and group dynamics. Am. J. Primatol. 76, 730–746 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Caillaud, D. et al. Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Sci. Adv. 6, eaba0724 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Watts, D. P. Causes and consequences of variation in male mountain gorilla life histories and group membership. In Primate Males (ed. Kappeler, P. M.) 169–179 (Cambridge University Press, 2000).
    Google Scholar 
    15.Robbins, M. M., Robbins, A. M., Gerald-Steklis, N. & Steklis, H. D. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav. Ecol. Sociobiol. 61, 919–931 (2007).Article 

    Google Scholar 
    16.Robbins, A. M. et al. Impact of male Infanticide on the social structure of mountain gorillas. PLoS One 8, e78256 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Grueter, C. C. et al. Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Sci. Rep. 8, 16718 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Eckardt, W., Stoinski, T. S., Rosenbaum, S. & Santymire, R. Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei). Ecol. Evol. 9, 5248–5259 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Harcourt, A. H., Parks, S. A. & Woodroffe, R. Human density as an influence on species/area relationships: Double jeopardy for small African reserves?. Biodivers. Conserv. 10, 1011–1026 (2001).Article 

    Google Scholar 
    20.Citterio, C. V. et al. Abomasal nematode community in an alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. J. Parasitol. 92, 918–927 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Hudson, P. J. Macroparasites: Observed patterns. Ecol. Infect. Dis. Nat. Popul. 20, 144–176 (1995).
    Google Scholar 
    22.Albon, S. D. et al. The role of parasites in the dynamics of a reindeer population. Proc. R. Soc. Lond. B Biol. Sci. 269, 1625–1632 (2002).CAS 
    Article 

    Google Scholar 
    23.Anderson, R. M. & May, R. M. Age-related changes in the rate of disease transmission: Implications for the design of vaccination programmes. Epidemiol. Infect. 94, 365–436 (1985).CAS 

    Google Scholar 
    24.Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Anderson, R. M. & May, R. M. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J. Anim. Ecol. 47, 219–247 (1978).Article 

    Google Scholar 
    26.Arneberg, P., Skorping, A., Grenfell, B. & Read, A. F. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 265, 1283–1289 (1998).Article 

    Google Scholar 
    27.Gillespie, T. R. & Chapman, C. A. Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. Am. J. Primatol. 70, 222–230 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Mbora, D. N. M. & McPeek, M. A. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J. Anim. Ecol. 78, 210–218 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.dos Santos, C. N. et al. Seasonal dynamics of cyathostomin (Nematoda–Cyathostominae) infective larvae in Brachiaria humidicola grass in tropical southeast Brazil. Vet. Parasitol. 180, 274–278 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Silangwa, S. M. & Todd, A. C. Vertical migration of trichostrongylid larvae on grasses. J. Parasitol. 50, 278–285 (1964).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Callinan, A. P. L. & Westcott, J. M. Vertical distribution of trichostrongylid larvae on herbage and in soil. Int. J. Parasitol. 16, 241–244 (1986).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Crofton, H. D. The ecology of immature phases of trichostrongyle nematodes: II. The effect of climatic factors on the availability of the infective larvae of Trichostrongylus retortaeformis to the host. Parasitology 39, 26–38 (1948).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Zanet, S. et al. Higher risk of gastrointestinal parasite infection at lower elevation suggests possible constraints in the distributional niche of Alpine marmots. PLoS One 12, e0182477 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Derek Scasta, J. Livestock parasite management on high-elevation rangelands: Ecological interactions of climate, habitat, and wildlife. J. Integr. Pest Manag. 6, 20 (2015).Article 

    Google Scholar 
    35.Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M. & Yoshida, K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111–125 (1997).Article 

    Google Scholar 
    36.MacIntosh, A. J. J., Hernandez, A. D. & Huffman, M. A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51, 353–364 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Pafčo, B. et al. Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?. Parasitol. Res. 116, 3401–3410 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Rothman, J. M., Pell, A. N. & Bowman, D. D. Host-parasiteecology of the helminths in mountain gorillas. J. Parasitol. 94, 834–840 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Müller-Graf, C. D. M., Collins, D. A. & Woolhouse, M. E. J. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112, 489–497 (1996).PubMed 
    Article 

    Google Scholar 
    40.Alexander, J. & Stimson, W. H. Sex hormones and the course of parasitic infection. Parasitol. Today 4, 189–193 (1988).Article 

    Google Scholar 
    41.Bundy, D. A. P. Gender-dependent patterns of infections and disease. Parasitol. Today 4, 186–189 (1988).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Zuk, M. Reproductive strategies and disease susceptibility: An evolutionary viewpoint. Parasitol. Today 6, 231–233 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Nunn, C. & Altizer, S. Infectious Diseases in Primates: Behavior (Ecology and Evolution. Oxford University Press, Oxford, 2006).Book 

    Google Scholar 
    44.Wilson, K. et al. Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases 6–44 (2002).45.Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. & Hudson, P. J. Peak shift and epidemiology in a seasonal host–nematode system. Proc. R. Soc. B Biol. Sci. 272, 1163–1169 (2005).CAS 
    Article 

    Google Scholar 
    46.Terio, K. A. et al. Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania. Am. J. Primatol. 80, e22572 (2018).Article 

    Google Scholar 
    47.Gillespie, T. R., Nunn, C. L. & Leendertz, F. H. Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Am. J. Phys. Anthropol. 137, 53–69 (2008).Article 

    Google Scholar 
    48.Collett, M. G. et al. Gastric Ollulanus tricuspis infection identified in captive cheetahs (Acinonyx jubatus) with chronic vomiting: Case report. J. S. Afr. Vet. Assoc. 71, 251–255 (2000).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    49.Dennis, M. M., Bennett, N. & Ehrhart, E. J. Gastric adenocarcinoma and chronic gastritis in two related Persian cats. Vet. Pathol. 43, 358–362 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Smetana, H. F. & Orihel, T. C. Gastric papillomata in Macaca speciosa induced by Nochtia nochti (Nematoda: Trichostrongyloidea). J. Parasitol. 55, 349–351 (1969).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Nybelin, O. Anoplocephala gorillae n. sp. Ark Zool. 19, 1–3 (1924).
    Google Scholar 
    52.Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. & Patton, S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J. Zool. Wildl. Med. 31, 322–328 (2000).CAS 
    Article 

    Google Scholar 
    53.Ashford, R. W., Lawson, H., Butynski, T. M. & Reid, G. D. F. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J. Zool. 239, 507–514 (1996).Article 

    Google Scholar 
    54.Kalema-Zikusoka, G., Rothman, J. M. & Fox, M. T. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates 46, 59–63 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Owiunji, I, et al. The biodiversity of the Virunga Volcanoes. https://programs.wcs.org/portals/49/media/file/volcanoes_biodiv_survey.pdf (2005).56.Langdale-Brown, I., Osmaston, H. & Wilson, J. G. The Vegetation of Uganda and Its Bearing on Land-Use (Governmentt of Uganda, 1964).
    Google Scholar 
    57.Ashford, R. W., Reid, G. D. F. & Butynski, T. M. The intestinal faunas of man and mountain gorillas in a shared habitat. Ann. Trop. Med. Parasitol. 84, 337–340 (1990).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Shutt, K. et al. Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management. Biol. Conserv. 172, 72–79 (2014).Article 

    Google Scholar 
    59.Kayiranga, A. et al. Analysis of climate and topography impacts on the spatial distribution of vegetation in the Virunga Volcanoes Massif of East-Central Africa. Geosciences 7, 17 (2017).ADS 
    Article 

    Google Scholar 
    60.Cousins, D. & Huffman, M. A. Medicinal properties in the diet of gorillas: An ethno-phramacological evaluation. Afr. Stud. Monogr. 23, 65–89 (2002).
    Google Scholar 
    61.Woolhouse, M. E. J. Patterns in parasite epidemiology: The peak shift. Parasitol. Today 14, 428–434 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Hayes, K. S., Bancroft, A. J. & Grencis, R. K. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 201, 75–88 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Maizels, R. M. et al. Helminth parasites—masters of regulation. Immunol. Rev. 201, 89–116 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Proudman, C. J., Holmes, M. A., Sheoran, A. S., Edwards, S. E. R. & Trees, A. J. Immunoepidemiology of the equine tapeworm Anoplocephala perfoliata: Age-intensity profile and age-dependency of antibody subtype responses. Parasitology 114, 89–94 (1997).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Gergócs, V., Garamvölgyi, Á., Homoródi, R. & Hufnagel, L. Seasonal change of oribatid mite communities (Acari, Oribatida) in three different types of microhabitats in an oak forest. Appl. Ecol. Environ. Res. 9, 181–195 (2011).Article 

    Google Scholar 
    66.Dobson, A. & Foufopoulos, J. Emerging infectious pathogens of wildlife. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 1001–1012 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Xue, Y. et al. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348, 242–245 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Reed, D. H. & Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237 (2003).Article 

    Google Scholar 
    69.Pafčo, B. et al. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 8, 5933 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    70.McNeilage, A. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virunga. In Mountain Gorillas: Three Decades of Research at Karisoke (Cambridge University Press, 2001).
    Google Scholar 
    71.Sinayitutse, E. et al. Daily defecation outputs of mountain gorillas (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Primates https://doi.org/10.1007/s10329-020-00874-7 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Burgunder, J. et al. Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 129, 257–268 (2017).Article 

    Google Scholar 
    73.Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T. & Austad, K. M. Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 68, 397–409 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Anderson, R. M. & Schad, G. A. Hookworm burdens and faecal egg counts: An analysis of the biological basis of variation. Trans. R. Soc. Trop. Med. Hyg. 79, 812–825 (1985).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Warnick, L. D. Daily variability of equine fecal strongyle egg counts. Cornell Vet. 82, 453–463 (1992).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Tomczuk, K. et al. Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions. Parasitol. Res. 113, 2401–2406 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Williamson, R., Beveridge, I. & Gasser, R. Coprological methods for the diagnosis of Anoplocephala perfoliata infection of the horse. Aust. Vet. J. 76, 618–621 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.Cringoli, G. et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 12, 1723–1732 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Guschanski, K. et al. Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol. Conserv. 142, 290–300 (2009).Article 

    Google Scholar 
    80.Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).MATH 
    Book 

    Google Scholar 
    81.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    82.R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).83.Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Engqvist, L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70, 20 (2005).Article 

    Google Scholar 
    85.Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge University Press, 2007).
    Google Scholar 
    86.Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).Article 

    Google Scholar 
    87.Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    88.Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).MATH 

    Google Scholar 
    89.Barton, K. MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn (2020). More

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    The chosen few—variations in common and rare soil bacteria across biomes

    1.Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, et al. Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev. 2013;77:342–56.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 2017;11:853–62.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Rivett DW, Bell T. Abundance determines the functional role of bacterial phylotypes in complex communities. Nat Microbiol. 2018;3:767–72.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK. The contribution of species richness and composition to bacterial services. Nature. 2005;436:1157–60.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Starke R, Capek P, Morais D, Callister SJ, Jehmlich N. The total microbiome functions in bacteria and fungi. J Proteom. 2020;213:1–5.Article 
    CAS 

    Google Scholar 
    6.Saleem M, Hu J, Jousset A. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst. 2019;50:145–68.Article 

    Google Scholar 
    7.Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, Heijden van der MGA. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun. 2019;10:1–10.CAS 
    Article 

    Google Scholar 
    8.Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:1–8.Article 
    CAS 

    Google Scholar 
    9.Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol. 2020;4:210–20.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Aanderud ZT, Jones SE, Fierer N, Lennon JT. Resuscitation of the rare biosphere contributes to pulses of ecosystem activity. Front Microbiol. 2015;6:1–11.Article 

    Google Scholar 
    11.Song H-K, Song W, Kim M, Tripathi BM, Kim H, Jablonski P, et al. Bacterial strategies along nutrient and time gradients, revealed by metagenomic analysis of laboratory microcosms. FEMS Microbiol Ecol. 2017;93:1–13.Article 
    CAS 

    Google Scholar 
    12.Jiao S, Chen W, Wei G. Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. Mol Ecol. 2017;26:5305–5317.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, et al. A global atlas of the dominant bacteria found in soil. Science. 2018;359:320–5.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Yu X, Polz MF, Alm EJ. Interactions in self-assembled microbial communities saturate with diversity. ISME J. 2019;13:1602–17.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Li P, Liu J, Jiang C, Wu M, Liu M, Li Z. Distinct successions of common and rare bacteria in soil under humic acid amendment—a microcosm study. Front Microbiol. 2019;10:1–14.Article 

    Google Scholar 
    16.Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, Schmidt SK, et al. Global patterns in the biogeography of bacterial taxa. Environ Microbiol. 2011;13:135–44.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Bickel S, Chen X, Papritz A, Or D. A hierarchy of environmental covariates control the global biogeography of soil bacterial richness. Sci Rep. 2019;9:1–10.CAS 
    Article 

    Google Scholar 
    18.Clarke RT, Murphy JF. Effects of locally rare taxa on the precision and sensitivity of RIVPACS bioassessment of freshwaters. Freshw Biol. 2006;51:1924–40.Article 

    Google Scholar 
    19.Kurm V, Putten WH, van der, Boer W, de, Naus‐Wiezer S, Hol WHG. Low abundant soil bacteria can be metabolically versatile and fast growing. Ecology. 2017;98:555–64.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Kurm V, Putten WH, van der, Hol WHG. Cultivation-success of rare soil bacteria is not influenced by incubation time and growth medium. PLoS ONE. 2019;14:1–14.Article 
    CAS 

    Google Scholar 
    21.Meyer KM, Memiaghe H, Korte L, Kenfack D, Alonso A, Bohannan BJM. Why do microbes exhibit weak biogeographic patterns? ISME J. 2018;12:1404–13.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Escalas A, Hale L, Voordeckers JW, Yang Y, Firestone MK, Alvarez‐Cohen L, et al. Microbial functional diversity: from concepts to applications. Ecol Evol. 2019;9:12000–16.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Barberán A, Ramirez KS, Leff JW, Bradford MA, Wall DH, Fierer N. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol Lett. 2014;17:794–802.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Dee LE, Cowles J, Isbell F, Pau S, Gaines SD, Reich PB. When do ecosystem services depend on rare species? Trends Ecol Evol. 2019;34:746–58.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Pueyo S, He F, Zillio T. The maximum entropy formalism and the idiosyncratic theory of biodiversity. Ecol Lett. 2007;10:1017–28.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Bahram M, Hildebrand F, Forslund SK, Anderson JL, Soudzilovskaia NA, Bodegom PM, et al. Structure and function of the global topsoil microbiome. Nature. 2018;560:233–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Zhou J, Deng Y, Shen L, Wen C, Yan Q, Ning D, et al. Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun. 2016;7:1–10.
    Google Scholar 
    28.Thompson LR, Jex AR, Campbell AH, Linz AM, Berry A, Williams AE, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Bickel S, Or D. Soil bacterial diversity mediated by microscale aqueous-phase processes across biomes. Nat Commun. 2020;11:1–9.
    Google Scholar 
    30.Xu X, Thornton PE, Post WM. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr. 2013;22:737–49.Article 

    Google Scholar 
    31.Serna-Chavez HM, Fierer N, van Bodegom PM. Global drivers and patterns of microbial abundance in soil: global patterns of soil microbial biomass. Glob Ecol Biogeogr. 2013;22:1162–72.Article 

    Google Scholar 
    32.Wang G, Or D. A hydration-based biophysical index for the onset of soil microbial coexistence. Sci Rep. 2012;2:1–5.
    Google Scholar 
    33.Li CH, Lee CK. Minimum cross entropy thresholding. Pattern Recognit. 1993;26:617–625.Article 

    Google Scholar 
    34.Walt S, van der, Schönberger JL, Nunez-Iglesias J, Boulogne F, Warner JD, Yager N, et al. scikit-image: image processing in Python. PeerJ. 2014;2:1–18.
    Google Scholar 
    35.Homem-de-Mello T, Rubinstein RY. Estimation of rare event probabilities using cross-entropy. Proc Winter Simul Conf. 2002;1:310–19.Article 

    Google Scholar 
    36.Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 2018;6:1–14.Article 

    Google Scholar 
    37.Šťovíček A, Kim M, Or D, Gillor O. Microbial community response to hydration-desiccation cycles in desert soil. Sci Rep. 2017;7:1–9.Article 
    CAS 

    Google Scholar 
    38.Zhao M, Heinsch FA, Nemani RR, Running SW. Improvements of the MODIS terrestrial gross and net primary production global data set. Remote Sens Environ. 2005;95:164–76.Article 

    Google Scholar 
    39.Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: new climate surfaces for global land areas. Int J Climatol. 2017;37:4302–15.Article 

    Google Scholar 
    40.Schoolfield RM, Sharpe PJH, Magnuson CE. Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. J Theor Biol. 1981;88:719–31.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Beck HE, Wood EF, Pan M, Fisher CK, Miralles DG, van Dijk AIJM, et al. MSWEP V2 Global 3-hourly 0.1° precipitation: methodology and quantitative assessment. Bull Am Meteorol Soc. 2019;100:473–500.Article 

    Google Scholar 
    42.Wang G, Or D. Hydration dynamics promote bacterial coexistence on rough surfaces. ISME J. 2013;7:395–404.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Kim M, Or D. Individual-based model of microbial life on hydrated rough soil surfaces. PLoS ONE. 2016;11:1–31.
    Google Scholar 
    44.Hermsen R, Okano H, You C, Werner N, Hwa T. A growth-rate composition formula for the growth of E.coli on co-utilized carbon substrates. Mol Syst Biol. 2015;11:1–6.Article 
    CAS 

    Google Scholar 
    45.García FC, Bestion E, Warfield R, Yvon-Durocher G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc Natl Acad Sci. 2018;115:10989–94.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    46.Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, Schimel JP, et al. Water balance creates a threshold in soil pH at the global scale. Nature. 2016;540:567–9.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Treves DS, Xia B, Zhou J, Tiedje JM. A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Micro Ecol. 2003;45:20–8.CAS 
    Article 

    Google Scholar 
    48.Campbell BJ, Yu L, Heidelberg JF, Kirchman DL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci. 2011;108:12776–81.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Stauffer D. Scaling theory of percolation clusters. Phys Rep. 1979;54:1–74.Article 

    Google Scholar 
    50.Scher H, Zallen R. Critical density in percolation processes. J Chem Phys. 1970;53:3759–61.CAS 
    Article 

    Google Scholar 
    51.Hengl T, de Jesus JM, Heuvelink GB, Gonzalez MR, Kilibarda M, Blagotić A, et al. SoilGrids250m: global gridded soil information based on machine learning. PloS ONE. 2017;12:1–40.Article 
    CAS 

    Google Scholar 
    52.Chase AB, Arevalo P, Brodie EL, Polz MF, Karaoz U, Martiny JBH. Maintenance of sympatric and allopatric populations in free-living terrestrial bacteria. mBio. 2019;10:1–11.Article 

    Google Scholar 
    53.Fisher CK, Mehta P. The transition between the niche and neutral regimes in ecology. Proc Natl Acad Sci. 2014;111:13111–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Ratzke C, Barrere J, Gore J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol. 2020;4:376–83.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Doud DFR, Bowers RM, Schulz F, Raad MD, Deng K, Tarver A, et al. Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. ISME J. 2020;14:659–75.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Shade A, Jones SE, Caporaso JG, Handelsman J, Knight R, Fierer N, et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio. 2014;5:1–9.Article 
    CAS 

    Google Scholar 
    57.Kaminsky R, Morales SE. Conditionally rare taxa contribute but do not account for changes in soil prokaryotic community structure. Front Microbiol. 2018;9:1–6.Article 

    Google Scholar 
    58.Price PB, Sowers T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci U S A. 2004;101:4631–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Author Correction: Priority list of biodiversity metrics to observe from space

    Faculty of Geo-Information Science and Earth Observation (ITC), University of Twente, Enschede, the NetherlandsAndrew K. Skidmore, Elnaz Neinavaz, Abebe Ali, Roshanak Darvishzadeh, Marcelle C. Lock & Tiejun WangDepartment of Earth and Environmental Science, Macquarie University, Sydney, New South Wales, AustraliaAndrew K. Skidmore & Marcelle C. LockDepartment of Forest Resources Management, University of British Columbia, Vancouver, British Columbia, CanadaNicholas C. CoopsDepartment of Geography and Environmental Studies, Wollo University, Dessie, EthiopiaAbebe AliRemote Sensing Laboratories, Department of Geography, University of Zurich, Zurich, SwitzerlandMichael E. SchaepmanEuropean Space Research Institute (ESRIN), European Space Agency, Frascati, ItalyMarc PaganiniInstitute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, Amsterdam, the NetherlandsW. Daniel KisslingBiodiversity Centre, Finnish Environment Institute (SYKE), Helsinki, FinlandPetteri VihervaaraInstitute of Geographical Sciences, Freie Universität Berlin, Berlin, GermanyHannes FeilhauerRemote Sensing Center for Earth System Research, University of Leipzig, Leipzig, GermanyHannes FeilhauerNatureServe, Arlington, VA, USAMiguel FernandezGeorge Mason University, Fairfax, VA, USAMiguel FernandezGerman Centre for Integrative Biodiversity Research (iDiv), Leipzig, GermanyNéstor FernándezInstitute of Biology, Martin Luther University Halle-Wittenberg, Halle (Saale), GermanyNéstor FernándezGoogle, Zurich, SwitzerlandNoel GorelickTour du Valat, Arles, FranceIlse GeijzendorfferEarth Observation Center (EOC), Remote Sensing Technology Institute, German Aerospace Center (DLR), Oberpfaffenhofen, GermanyUta Heiden & Stefanie HolzwarthDepartment of Visitor Management and National Park Monitoring, Bavarian Forest National Park Administration, Grafenau, GermanyMarco HeurichAlbert Ludwigs University of Freiburg, Freiburg, GermanyMarco HeurichGBIF Secretariat, Copenhagen, DenmarkDonald HobernCollege of Marine Science, University of South Florida, St Petersburg, FL, USAFrank E. Muller-KargerFlemish Institute for Technological Research (VITO), Mol, BelgiumRuben Van De KerchoveComputational Landscape Ecology, Helmholtz Centre for Environmental Research (UFZ), Leipzig, GermanyAngela LauschGeography Department, Humboldt University of Berlin, Berlin, GermanyAngela LauschTechnische Universität Braunschweig, Braunschweig, GermanyPedro J. LeitãoHumboldt-Universität zu Berlin, Berlin, GermanyPedro J. LeitãoWageningen Environmental Research, Wageningen University & Research, Wageningen, the NetherlandsCaspar A. MücherUN Environment World Conservation Monitoring Centre, Cambridge, UKBrian O’ConnorDepartment of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, ItalyDuccio RocchiniDepartment of Applied Geoinformatics and Spatial Planning, Faculty of Environmental Sciences, Czech University of Life Sciences, Prague, Czech RepublicDuccio RocchiniEarth Science Division, NASA, Washington DC, USAWoody TurnerUnilever Europe B.V., Rotterdam, the NetherlandsJan Kees VisInstitute of Geography and Geology, University of Wuerzburg, Würzburg, GermanyMartin WegmannLand Systems and Sustainable Land Management, Geographisches Institut, Universität Bern, Bern, SwitzerlandVladimir Wingate More

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    Effects of long-term integrated agri-aquaculture on the soil fungal community structure and function in vegetable fields

    Effects of the two planting systems on soil fungal diversityIn this study, 561,254 sequences were generated from 15 samples obtained from 5 treatments. Base sequences with a length of 201–300 bp accounted for 97.82% of all sequences (Table S1a,b). Rarefaction curves at a similarity level of 97% indicated that the number of sequences extracted from most samples tended to plateau above 10,000. The number of sequences extracted in the test exceeded 30,000, suggesting that the sequencing data were close to saturation, sequencing depth was reasonable, and the results reflected true sample conditions (Fig. 1). The coverage of all samples was above 99.84%. The range of reads in each sample was between 34,390 and 43,510. The range of Operational Taxonomic Units (OTUs) in each sample was between 145 and 318 (Table 1).Figure 1α-Diversity comparison. Rarefaction curves for OTUs were calculated using Mothur (v1.27.0) with reads normalized to more than 30,000 for each sample using a distance of 0.03 OTU.Full size imageTable 1 Comparison of α-diversity indices in TPP and VEE soil samples.Full size tableThe analysis of alpha diversity showed that with increasing planting time, soil fungal OTUs, the Chao index, and the ACE index in TPP-treated plots increased and then decreased with time. In the VEE-IPBP-treated plots, these 3 indexes increased with time and were 56.94%, 33.81%, and 32.50% higher than those in the TPP-treated plots, respectively, after 6 years of implementation (p  More

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    Distinguishing anthropogenic and natural contributions to coproduction of national crop yields globally

    1.Pellegrini, P. & Fernández, R. J. Crop intensification, land use, and on-farm energy-use efficiency during the worldwide spread of the green revolution. Proc. Natl. Acad. Sci. U. S. A. 115(10), 2335–2340 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Ray, D. K., Ramankutty, N., Mueller, N. D., West, P. C. & Foley, J. A. Recent patterns of crop yield growth and stagnation. Nat. Commun. 3(1), 1293 (2012).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    3.Palomo, I., Felipe-Lucia, M. R., Bennett, E. M., Martín-López, B. & Pascual, U. Chapter six—disentangling the pathways and effects of ecosystem service co-production. In Advance Ecology Research (eds Woodward, G. & Bohan, D. A.) 245–283 (Academic Press, 2016).
    Google Scholar 
    4.Lavorel, S., Locatelli, B., Colloff, M. J. & Bruley, E. Co-producing ecosystem services for adapting to climate change. Philos. T. Roy. Soc. B. 375(1794), 20190119 (2020).Article 

    Google Scholar 
    5.Boerema, A., Rebelo, A. J., Bodi, M. B., Esler, K. J. & Meire, P. Are ecosystem services adequately quantified?. J. Appl. Ecol. 54(2), 358–370 (2017).Article 

    Google Scholar 
    6.Maes, J. et al. An indicator framework for assessing ecosystem services in support of the EU Biodiversity Strategy to 2020. Ecosyst. Serv. 17, 14–23 (2016).Article 

    Google Scholar 
    7.Jones, L. et al. Stocks and flows of natural and human-derived capital in ecosystem services. Land Use Policy 52, 151–162 (2016).Article 

    Google Scholar 
    8.Barot, S., Yé, L., Abbadie, L., Blouin, M. & Frascaria-Lacoste, N. Ecosystem services must tackle anthropized ecosystems and ecological engineering. Ecol. Eng. 99, 486–495 (2017).Article 

    Google Scholar 
    9.Remme, R. P., Edens, B., Schröter, M. & Hein, L. Monetary accounting of ecosystem services: a test case for Limburg province, the Netherlands. Ecol. Econ. 112, 116–128 (2015).Article 

    Google Scholar 
    10.Gaiser, T. & Stahr, K. Soil organic carbon, soil formation and soil fertility. In Ecosystem Services and Carbon Sequestration in the Biosphere (eds Lal, R. et al.) 407–418 (Springer, 2013).
    Google Scholar 
    11.FAO and ITPS. Status of the World’s Soil Resources (SWSR)—Main Report (Food and Agriculture Organization of the United Nations and Intergovernmental Technical Panel on Soils, 2015).
    Google Scholar 
    12.Dainese, M. et al. A global synthesis reveals biodiversity-mediated benefits for crop production. Sci. Adv. 5(10), eaax0121 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.Bommarco, R., Kleijn, D. & Potts, S. G. Ecological intensification: harnessing ecosystem services for food security. Trends Ecol. Evol. 28(4), 230–238 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Zabel, F., Putzenlechner, B. & Mauser, W. Global agricultural land resources—a high resolution suitability evaluation and its perspectives until 2100 under climate change conditions. PLoS ONE 9(9), e107522 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Pelletier, N. et al. Energy intensity of agriculture and food systems. Annu. Rev. Environ. Resour. 36(1), 223–246 (2011).Article 

    Google Scholar 
    16.Díaz, S. et al. The IPBES conceptual framework—connecting nature and people. Curr. Opin. Environ. Sustain. 14, 1–16 (2015).Article 

    Google Scholar 
    17.Bennett, E. M. Research frontiers in ecosystem service science. Ecosystems 20(1), 31–37 (2017).Article 

    Google Scholar 
    18.Woods, J., Williams, A., Hughes, J. K., Black, M. & Murphy, R. Energy and the food system. Philos. T. Roy. Soc. B. 365(1554), 2991–3006 (2010).Article 

    Google Scholar 
    19.Foley, J. A. et al. Global consequences of land use. Science 309(5734), 570–574 (2005).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Seppelt, R., Manceur, A. M., Liu, J., Fenichel, E. P. & Klotz, S. Synchronized peak-rate years of global resources use. Ecol. Soc. 19(4), 50 (2014).Article 

    Google Scholar 
    21.Meyfroidt, P. et al. Middle-range theories of land system change. Glob. Environ. Chang. 53, 52–67 (2018).Article 

    Google Scholar 
    22.Fitter, A. H. Are ecosystem services replaceable by technology?. Environ. Res. Econ. 55(4), 513–524 (2013).Article 

    Google Scholar 
    23.Cohen, F., Hepburn, C. J. & Teytelboym, A. Is natural capital really substitutable?. Annu. Rev. Environ. Resour. 44(1), 425–448 (2019).Article 

    Google Scholar 
    24.Ekins, P., Simon, S., Deutsch, L., Folke, C. & De Groot, R. A framework for the practical application of the concepts of critical natural capital and strong sustainability. Ecol. Econ. 44(2–3), 165–185 (2003).Article 

    Google Scholar 
    25.Lassaletta, L., Billen, G., Grizzetti, B., Anglade, J. & Garnier, J. 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environ. Res. Lett. 9(10), 105011 (2014).ADS 
    Article 

    Google Scholar 
    26.Levers, C., Butsic, V., Verburg, P. H., Müller, D. & Kuemmerle, T. Drivers of changes in agricultural intensity in Europe. Land Use Policy 58, 380–393 (2016).Article 

    Google Scholar 
    27.Coomes, O. T., Barham, B. L., MacDonald, G. K., Ramankutty, N. & Chavas, J.-P. Leveraging total factor productivity growth for sustainable and resilient farming. Nat. Sustain. 2(1), 22–28 (2019).Article 

    Google Scholar 
    28.Fuglie, K. R&D capital, RD spillovers, and productivity growth in world agriculture. Appl. Econ. Perspect. Policy 40(3), 421–444 (2018).Article 

    Google Scholar 
    29.Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254 (2012).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.German, R. N., Thompson, C. E. & Benton, T. G. Relationships among multiple aspects of agriculture’s environmental impact and productivity: a meta-analysis to guide sustainable agriculture. Biol. Rev. 92(2), 716–738 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Lee, H. & Lautenbach, S. A quantitative review of relationships between ecosystem services. Ecol. Indic. 66, 340–351 (2016).Article 

    Google Scholar 
    32.Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333(6042), 616–620 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    33.Erb, K.-H. et al. A conceptual framework for analysing and measuring land-use intensity. Curr. Opin. Environ. Sustain. 5(5), 464–470 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Loos, J. et al. Putting meaning back into “sustainable intensification”. Front. Ecol. Environ. 12(6), 356–361 (2014).Article 

    Google Scholar 
    35.Kleijn, D. et al. Ecological intensification: bridging the gap between science and practice. Trends Ecol. Evol. 34(2), 154–166 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Stirzaker, R., Biggs, H., Roux, D. & Cilliers, P. Requisite simplicities to help negotiate complex problems. Ambio 39(8), 600–607 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Kuemmerle, T. et al. Challenges and opportunities in mapping land use intensity globally. Curr. Opin. Environ. Sustain. 5(5), 484–493 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Garibaldi, L. A., Aizen, M. A., Klein, A. M., Cunningham, S. A. & Harder, L. D. Global growth and stability of agricultural yield decrease with pollinator dependence. Proc. Natl. Acad. Sci. U. S. A. 108(14), 5909–5914 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Bengtsson, J. Biological control as an ecosystem service: partitioning contributions of nature and human inputs to yield. Ecol. Entomol. 40(S1), 45–55 (2015).Article 

    Google Scholar 
    40.Seppelt, R., Arndt, C., Beckmann, M., Martin, E. A. & Hertel, T. Deciphering the biodiversity-production mutualism in the global food security debate. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2020.06.012 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Poore, J. & Nemecek, T. Reducing food’s environmental impacts through producers and consumers. Science 360(6392), 987–992 (2018).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Beckmann, M. et al. Conventional land-use intensification reduces species richness and increases production: a global meta-analysis. Glob. Chang. Biol. 25(6), 1941–1956 (2019).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Garibaldi, L. A. et al. Farming approaches for greater biodiversity, livelihoods, and food security. Trends Ecol. Evol. 32(1), 68–80 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Monfreda, C., Ramankutty, N. & Foley, J. A. Farming the planet: 2. Geographic distribution of crop areas, yields, physiological types, and net primary production in the year 2000. Glob. Biogeochem. Cycles 22(1), 1–19 (2008).Article 
    CAS 

    Google Scholar 
    45.IFA, IFDC, IPI, PPI, FAO. Fertilizer Use by Crop (FAO, 2002).
    Google Scholar 
    46.IFA. Assessment of Fertilizer Use by Crop at the Global Level 2006/07–2007/08 (IFA, 2009).
    Google Scholar 
    47.IFA. Assessment of Fertilizer Use by Crop at the Global Level 2010–2010/11 (IFA, 2013).
    Google Scholar 
    48.IFA and IPNI. Assessment of Fertilizer Use by Crop at the Global Level (IFA and IPNI, 2017).
    Google Scholar 
    49.FAO. Crops. http://www.fao.org/faostat/en/#data/QC (2018).50.FAO. Capital Stock. http://www.fao.org/faostat/en/#data/CS (2018).51.U.S. Bureau of Labor Statistics. CPI Inflation Calculator. https://data.bls.gov/cgi-bin/cpicalc.pl?cost1=1.00&year1=200001&year2=201401 (2020).52.FAO. Livestock Manure. http://www.fao.org/faostat/en/#data/EMN (2018).53.FAO. Food Balance Sheets: A Handbook 95 (FAO, 2001).
    Google Scholar 
    54.World Bank. The World by Income and Region. https://datatopics.worldbank.org/world-development-indicators/the-world-by-income-and-region.html (2019).55.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
    Google Scholar 
    56.RStudio Team. RStudio: Integrated Development for R (RStudio, Inc., 2018).
    Google Scholar 
    57.Cook, R. D. Detection of influential observation in linear regression. Technometrics 19(1), 15–18 (1977).MathSciNet 
    MATH 

    Google Scholar 
    58.Natural Earth. Admin 0—Countries. Version 4.0.0 (accessed 22 October 2017); https://www.naturalearthdata.com/ (2017). More

  • in

    Understanding anatomical plasticity of Argan wood features at local geographical scale in ecological and archaeobotanical perspectives

    Sampling, preparation and treatment of modern reference materialA total of 53 modern wood samples were analyzed. The modern reference samples were collected in 2014 during the annual archaeological field mission, from 36 individuals (Table S1). For some trees, two wood samples of different diameters were collected in order to take into account anatomical variability within individual.The collected individuals showed different conditions of growth described in the introduction section and detailed in the Table 1. With the agreement of the Tifigit inhabitants and local authorities, wood sampling was achieved but samples were not collected from trunks, to avoid injuring trees of major symbolic, ecological and economic importance. Only section samples with perfect axial symmetry were retained to avoid any impact of biomechanical constraints (formation of reaction wood) on wood characters.Once collected, the samples were air-dried during a month at the laboratory. The samples were separately wrapped in tin foil and buried in the sand and then charred without oxygen, at 450 °C for 15 to 20 min depending on the size of the sample. As a result, samples were enriched in carbon (content  > 90%)20,26, reached their maximal shrinkage27, and thus are considered to become morphologically comparable to charcoal produced in medieval fires27,28,29,30,31. The minimum and the maximum diameter of wood samples were measured (mm) using a digital measuring calliper before and after carbonization. The diameter used in the following analyses is the mean of the two measurements carried out before carbonization.Archaeological materialTwenty archaeological charcoal fragments of Argan tree identified during a previous analysis session13 were included in this study (Table S2). All the Argan charcoal fragments were collected in the medieval archaeological deposits of Îgîlîz13. They come from various contexts, for the most part from living units, and belong to the period of highest human activity at the site, between the late 11th and early thirteenth centuries.Quantitative eco-anatomical analysis of wood applied to the Argan treeThe approach consists in measuring constitutive elements of wood and aims to understand variations according to intrinsic (inferred by the branch diameter mainly age of tree18, linked to the existence of growth rings that are often difficult to distinguish) and environmental parameters affecting the cambial activity and thus, rate of growth and wood development20,28,29,30. This high resolution analysis of wood structure, particularly of conductive elements, allows addressing numerous questions that have been successfully solved in the case of the olive tree and the grapevine, such as phenology, ecology, climate, impact of human activities and agricultural practices20,24,25,31,32,33.Argania spinosa wood is diffuse-porous with a dendritic and diagonal arrangement of vessel elements in transversal section34. The axial parenchyma bands are in tangential alignment and composed of multicellular strands. In radial alignment, woody rays are 1–3 cells wide and of heterocellular composition (Fig. 6).Figure 6Wood anatomical features of the Argan tree (in blue) and measured anatomical characters (in red).Full size imageTo apply a quantitative eco-anatomy approach to the Argan tree, both modern charred samples and archaeological charcoal are broken manually in transverse anatomical section. The following wood constitutive elements and anatomical characters related to sap conduction and reserve storage are observed and measured under a reflected-light microscope connected with an image analysis system (DFC300 FX Leica camera and LAS Leica software) (Fig. 6): (1) vessel density (DVS—number of vessels / mm2), (2) vessel surface area (SVS, µm2), (3) ray density (DRA—number of rays / mm2), (4) axial parenchyma density (DPA, number of bands / mm2), (5) Density of wood fenestrated zones bordered on one side by the radial alignment of axial parenchyma cells and on the other side, tangentially, by rays (DWF—number of fenestrated zones / mm2).These anatomical features were measured several times (see ‘Statistical analyses’ section) following radial lines from the cambium inwards the sample and crossing a small number of growth rings (i.e. functional rings from a sap conduction point of view). Moreover, the hydraulic conductivity or vascular conductivity (CD) was assessed using the following formula: CD = (SVS/π)2/DVS (after32,35,36,37). Finally, the ratio ‘Conductive surface / total wood area’ (SC) was calculated.Statistical analysesIn order to determine the number of measurements required for an optimal assessment of anatomical features, a rarefaction method was carried out from the analysis of test wood samples. For each one, repeated measurements of anatomical characters (Surface vessel area (SVS), Density of vessels (DVS), Ray density (DRA), Axial parenchyma density (DPA) and Density of wood fenestrated zones (DWF)) were performed following the aforementioned method and the cumulative mean value was then calculated for each character20,29. For each test sample and anatomical character, the number of measurements of a character required for an optimal assessment was quantified as the minimum number of measurements required to stabilize the mean value (rarefaction curve or cumulative mean curve).Furthermore, different measurement sessions were carried out with the aim of testing possible errors and reproducibility of measurements taken by one or various observers, respectively. The data sets produced were tested using the PCA performed to evaluate the Argan anatomical variability. The ARG8-2 sample was used as test sample. In addition to the initial measurements. The ARG8-2 sample was analyzed 4 times: twice by one operator (ARG8-2 (1-OP1) and ARG8-2 (2-OP1)) and twice by another (ARG8-2 (3-OP2) and ARG8-2 (3-OP2)) at different times. The additional data were incorporated into the PCA as additional individuals for comparison with initial anatomical features of ARG8-2.After showing that measurement errors have no impact on the validity of results and the measurements are reproducible, quantitative eco-anatomical data were processed using a principal component analysis (PCA) in order to evaluate anatomical plasticity in the reference modern material, to appreciate relationships between characters and wood sample caliber and to confront archaeological data to the reference model. PCA was applied on 53 reference modern samples and 7 quantitative variables (anatomical characters) to: (1) validate the hypothesis that there is a significant relationship between the size of the branch and anatomy, as previously demonstrated by analyses of wood development and structure18,20,38 and dendrochronology39; (2) identify the anatomical characters most affected by the age of the branch and, in that case, model the ‘anatomical characters—caliber of the branch’ relationship; (3) develop predictive model that might estimate the minimum branch caliber from eco-anatomical data of archaeological charcoal.Finally, data from analysis of the 20 archaeological charcoal fragments were included in PCA as additional statistical samples. They do not contribute to the development of the reference model, but are compared to the modern reference samples in order to infer the ecological conditions under which Argan trees grew during the Middle Ages. More

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    Changes in taxonomic and functional diversity of plants in a chronosequence of Eucalyptus grandis plantations

    1.Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science (80- ) 287, 1770–1774 (2000).CAS 
    Article 

    Google Scholar 
    2.Wall, D. H. & Nielsen, U. N. Biodiversity and ecosystem services: is it the same below ground?. Nat. Educ. Knowl. 12, 3–8 (2012).
    Google Scholar 
    3.FAO. Global Forest Resources Assessment 2015: Desk Reference. http://www.fao.org/3/a-i4808e.pdf (2015).4.Filloy, J., Zurita, G. A., Corbelli, J. M. & Bellocq, M. I. On the similarity among bird communities: testing the influence of distance and land use. Acta Oecol. 36, 333–338 (2010).ADS 
    Article 

    Google Scholar 
    5.Santoandré, S., Filloy, J., Zurita, G. A. & Bellocq, M. I. Ant taxonomic and functional diversity show differential response to plantation age in two contrasting biomes. For. Ecol. Manag. 437, 304–313 (2019).Article 

    Google Scholar 
    6.Calviño-Cancela, M. Effectiveness of eucalypt plantations as a surrogate habitat for birds. For. Ecol. Manag. 310, 692–699 (2013).Article 

    Google Scholar 
    7.Santoandré, S., Filloy, J., Zurita, G. A. & Bellocq, M. I. Taxonomic and functional β-diversity of ants along tree plantation chronosequences differ between contrasting biomes. Basic Appl. Ecol. 41, 1–12 (2019).Article 

    Google Scholar 
    8.Corbelli, J. M. et al. Integrating taxonomic, functional and phylogenetic beta diversities: interactive effects with the biome and land use across taxa. PLoS ONE 10, 1–17 (2015).Article 
    CAS 

    Google Scholar 
    9.Phifer, C. C., Knowlton, J. L., Webster, C. R., Flaspohler, D. J. & Licata, J. A. Bird community responses to afforested eucalyptus plantations in the Argentine pampas. Biodivers. Conserv. https://doi.org/10.1007/s10531-016-1126-6 (2016).Article 

    Google Scholar 
    10.Tererai, F., Gaertner, M., Jacobs, S. M. & Richardson, D. M. Eucalyptus invasions in riparian forests: effects on native vegetation community diversity, stand structure and composition. For. Ecol. Manag. 297, 84–93 (2013).Article 

    Google Scholar 
    11.Brancalion, P. H. S. et al. Intensive silviculture enhances biomass accumulation and tree diversity recovery in tropical forest restoration. Ecol. Appl. 29, 1–12 (2019).Article 

    Google Scholar 
    12.Zhang, C., Liu, G., Xue, S. & Wang, G. Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biol. Biochem. 97, 40–49 (2016).CAS 
    Article 

    Google Scholar 
    13.Zhu, Y., Wang, Y. & Chen, L. Effects of non-native tree plantations on the diversity of understory plants and soil macroinvertebrates in the Loess Plateau of China. Plant Soil 446, 357–368 (2019).Article 
    CAS 

    Google Scholar 
    14.Zhang, W. et al. Plant functional composition and species diversity affect soil C, N, and P during secondary succession of abandoned farmland on the Loess Plateau. Ecol. Eng. 122, 91–99 (2018).Article 

    Google Scholar 
    15.Munévar, A., Rubio, G. D. & Andrés, G. Changes in spider diversity through the growth cycle of pine plantations in the semi-deciduous Atlantic forest: the role of prey availability and abiotic conditions. For. Ecol. Manag. 424, 536–544 (2018).Article 

    Google Scholar 
    16.Vega, E., Baldi, G., Jobbágy, E. G. & Paruelo, J. Land use change patterns in the Río de la Plata grasslands: the influence of phytogeographic and political boundaries. Agric. Ecosyst. Environ. 134, 287–292 (2009).Article 

    Google Scholar 
    17.Ntshuxeko, V. E. & Ruwanza, S. Physical properties of soil in Pine elliottii and Eucalyptus cloeziana plantations in the Vhembe biosphere, Limpopo Province of South Africa. J. For. Res. https://doi.org/10.1007/s11676-018-0830-3 (2018).Article 

    Google Scholar 
    18.Kerr, T. F. & Ruwanza, S. Does Eucalyptus grandis invasion and removal affect soils and vegetation in the Eastern Cape Province, South Africa?. Austral. Ecol. 41, 328–338 (2016).Article 

    Google Scholar 
    19.Zhang, D. J., Zhang, J., Yang, W. Q. & Wu, F. Z. Potential allelopathic effect of Eucalyptus grandis across a range of plantation ages. Ecol. Res. 25, 13–23 (2010).Article 

    Google Scholar 
    20.Díaz, S. & Cabido, M. Vive la difference: plant functional diversity matters to ecosystem processes: plant functional diversity matters to ecosystem processes. Trends Ecol. Evol. 16, 646–655 (2001).Article 

    Google Scholar 
    21.Petchey, O. L. & Gaston, K. J. Functional diversity: back to basics and looking forward. Ecol. Lett. 9, 741–758 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Luck, G. W., Lavorel, S., Mcintyre, S. & Lumb, K. Improving the application of vertebrate trait-based frameworks to the study of ecosystem services. J. Anim. Ecol. 81, 1065–1076 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Lindenmayer, D. et al. Richness is not all: how changes in avian functional diversity reflect major landscape modification caused by pine plantations. Divers. Distrib. 21, 836–847 (2015).Article 

    Google Scholar 
    24.Whittaker, R. H. Vegetation of the Siskiyou Mountains, Oregon and California. Ecol. Monogr. 30, 280–338 (1960).Article 

    Google Scholar 
    25.Swenson, N. G. Functional and Phylogenetic Ecology in R. Use R! (2014). https://doi.org/10.1007/978-1-4614-9542-0.26.Vaccaro, A. S., Filloy, J. & Bellocq, M. I. What land use better preserves taxonomic and functional diversity of birds in a grassland biome?. Avian Conserv. Ecol. 14, 1 (2019).Article 

    Google Scholar 
    27.Blair, J., Nippert, J. & Briggs, J. Grassland Ecology. Ecology and the Environment vol. 8 (Springer, 2014).28.Nic Lughadha, E. et al. Measuring the fate of plant diversity: towards a foundation for future monitoring and opportunities for urgent action. Philos. Trans. R. Soc. B Biol. Sci. 360, 359–372 (2005).CAS 
    Article 

    Google Scholar 
    29.Marteinsdóttir, B. & Eriksson, O. Trait-based filtering from the regional species pool into local grassland communities. J. Plant Ecol. 7, 347–355 (2014).Article 

    Google Scholar 
    30.Salgado Negret, B. La Ecología Funcional como aproximación al estudio, manejo y conservación de la biodiversidad: protocolos y aplicaciones. La ecología funcional como aproximación al estudio, manejo y conservación de la biodiversidad: protocolos y aplicaciones (2015).31.Barbier, S., Gosselin, F. & Balandier, P. Influence of tree species on understory vegetation diversity and mechanisms involved—a critical review for temperate and boreal forests. For. Ecol. Manag. 254, 1–15 (2008).Article 

    Google Scholar 
    32.Zhang, D., Zhang, J., Yang, W., Wu, F. & Huang, Y. Plant and soil seed bank diversity across a range of ages of Eucalyptus grandis plantations afforested on arable lands. Plant Soil 376, 307–325 (2014).CAS 
    Article 

    Google Scholar 
    33.Zhang, C. & Fu, S. Allelopathic effects of eucalyptus and the establishment of mixed stands of eucalyptus and native species. For. Ecol. Manag. 258, 1391–1396 (2009).Article 

    Google Scholar 
    34.Florentine, S. K. & Fox, J. E. D. Allelopathic effects of Eucalyptus victrix L. on Eucalyptus species and grasses. Allelopath. J. 11, 77–83 (2003).
    Google Scholar 
    35.Jobbágy, E. et al. Forestación en pastizales: hacia una visión integral de sus oportunidades y costos ecológicos. Agrociencia X, 109–124 (2006).36.Ruwanza, S., Gaertner, M., Esler, K. J. & Richardson, D. M. Allelopathic effects of invasive Eucalyptus camaldulensis on germination and early growth of four native species in the Western Cape South Africa. South. For. 77, 91–105 (2015).Article 

    Google Scholar 
    37.Suggitt, A. J. et al. Habitat microclimates drive fi ne-scale variation in extreme temperatures. Oikos https://doi.org/10.1111/j.1600-0706.2010.18270.x (2011).Article 

    Google Scholar 
    38.Zellweger, F., Roth, T., Bugmann, H. & Bollmann, K. Beta diversity of plants, birds and butterflies is closely associated with climate and habitat structure. Glob. Ecol. Biogeogr. 26, 898–906 (2017).Article 

    Google Scholar 
    39.Silveira, L. & Alonso, J. Runoff modifications due to the conversion of natural grasslands to forests in a large basin in Uruguay. Hidrol. Process. 329, 320–329 (2009).ADS 
    Article 

    Google Scholar 
    40.Mendoza, C. A., Gallardo, J. F., Turrión, M. B., Pando, V. & Aceñolaza, P. G. Dry weight loss in leaves of dominant species in a successional sequence of the Mesopotamian Espinal (Argentina). For. Syst. 26, 1–10 (2017).
    Google Scholar 
    41.Rodriguez, E. E., Aceñolaza, P. G., Perea, E. L. & Galán de Mera, A. A phytosociological analysis of Butia yatay (Arecaceae) palm groves and gallery forests in Entre Rios, Argentina. Aust. J. Bot. https://doi.org/10.1071/BT16140 (2017).Article 

    Google Scholar 
    42.Piwczyński, M., Puchałka, R. & Ulrich, W. Influence of tree plantations on the phylogenetic structure of understorey plant communities. For. Ecol. Manag. 376, 231–237 (2016).Article 

    Google Scholar 
    43.Csecserits, A. et al. Tree plantations are hot-spots of plant invasion in a landscape with heterogeneous land-use. Agric. Ecosyst. Environ. 226, 88–98 (2016).Article 

    Google Scholar 
    44.Amazonas, N. T. et al. High diversity mixed plantations of Eucalyptus and native trees: an interface between production and restoration for the tropics. For. Ecol. Manag. 417, 247–256 (2018).Article 

    Google Scholar 
    45.Verstraeten, G. et al. Understorey vegetation shifts following the conversion of temperate deciduous forest to spruce plantation. For. Ecol. Manag. 289, 363–370 (2013).Article 

    Google Scholar 
    46.Grass, I., Brandl, R., Botzat, A., Neuschulz, E. L. & Farwig, N. Contrasting taxonomic and phylogenetic diversity responses to forest modifications: comparisons of taxa and successive plant life stages in south African scarp forest. PLoS ONE 10, 1–20 (2015).Article 
    CAS 

    Google Scholar 
    47.Wu, J. et al. Should exotic Eucalyptus be planted in subtropical China: insights from understory plant diversity in two contrasting Eucalyptus chronosequences. Environ. Manag. 56, 1244–1251 (2015).ADS 
    Article 

    Google Scholar 
    48.Jin, D. et al. High risk of plant invasion in the understory of eucalypt plantations in South China. Sci. Rep. 5, 18492 (2016).ADS 
    Article 
    CAS 

    Google Scholar 
    49.Haughian, S. R. & Frego, K. A. Short-term effects of three commercial thinning treatments on diversity of understory vascular plants in white spruce plantations of northern New Brunswick. For. Ecol. Manag. 370, 45–55 (2016).Article 

    Google Scholar 
    50.Smith, G. F., Iremonger, S., Kelly, D. L., O’Donoghue, S. & Mitchell, F. J. G. Enhancing vegetation diversity in glades, rides and roads in plantation forests. Biol. Conserv. 136, 283–294 (2007).Article 

    Google Scholar 
    51.Aceñolaza, P. G., Rodriguez, E. E. & Diaz, D. Efecto de prácticas de manejo silvícola sobre la diversidad vegetal bajo plantaciones de Eucalyptus grandis. In 4to Congreso Forestal Argentino y Latinoamericano (2013).52.Connell, J. H. & Slatyer, R. O. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Nat. 111, 1119–1144 (1977).Article 

    Google Scholar 
    53.Pedley, S. M. & Dolman, P. M. Multi-taxa trait and functional responses to physical disturbance. J. Anim. Ecol. 83, 1542–1552 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Birkhofer, K., Smith, H. G., Weisser, W. W., Wolters, V. & Gossner, M. M. Land-use effects on the functional distinctness of arthropod communities. Ecography (Cop.) https://doi.org/10.1111/ecog.01141 (2015).Article 

    Google Scholar 
    55.Mangels, J., Fiedler, K., Schneider, F. D. & Blu, N. Diversity and trait composition of moths respond to land-use intensification in grasslands : generalists replace specialists. Biodivers. Conserv. https://doi.org/10.1007/s10531-017-1411-z (2017).Article 

    Google Scholar 
    56.Morello, J., Matteucci, S. D., Rodriguez, A. F. & Silva, M. Ecorregiones y complejos ecosistemicos argentino. (2012).57.Cabrera, Á. Fitogeografía de la República Argentina. Bol. Soc. Argent. Bot. 14, 1–42 (1971).
    Google Scholar 
    58.Rodriguez, E. E., Aceñolaza, P. G., Picasso, G. & Gago, J. Plantas del bajo Rio Uruguay: árboles, arbustos, herbáceas, lianas y epifitas. (2018).59.Bilenca, D. & Miñarro, F. Identificación de Áreas Valiosas de Pastizal (AVPs) en las Pampas y Campos de Argentina Uruguay y sur de Brasil. Vasa https://doi.org/10.1007/s13398-014-0173-7.2 (2004).Article 

    Google Scholar 
    60.Inta. Plan de Tecnologia Regional 2009–2011. INTA Cent. Reg. Entre Rios (2011).61.Aguerre, M. et al. Manual para productores de Eucaliptos de la Mesopotamia Argentina. (1995).62.Aparicio, J. L., Larocca, F. & Dalla Tea, F. Silvicultura de establecimiento de Eucalyptus grandis. IDIA XXI, Revista de Información sobre Investigación y Desarrollo Agropecuario 66–69 (2005).63.Vilela, E., Leite, H. G. & Jaffe, K. Level of economic damage for leaf-cutting ants (Hymenoptera: Formicidae) in Eucalyptus plantations in Brazil. Sociobiology 42, 1–10 (2015).
    Google Scholar 
    64.Larroca, F., Dalla Tea, F. & Aparicio, J. L. Técnicas de implantación y manejo de eucaliptus para pequeños y medianos forestadores en Entre Ríos y Corrientes. in XIX Jornadas Forestales de Entre Ríos. (2004).65.Burkart, A. Flora ilustrada de la provincia de Entre Ríos. (INTA, 1969).66.Burkart, A. Flora ilustrada de Entre Ríos (Argentina). Parte 2 Gramíneas. Colección Científica del INTA (1969).67.Peyras, M., Vespa, N. I., Bellocq, M. I. & Zurita, G. A. Quantifying edge effects : the role of habitat contrast and species specialization. J. Insect Conserv. 17, 807–820 (2013).Article 

    Google Scholar 
    68.Werenkraut, V., Fergnani, P. N. & Ruggiero, A. Ants at the edge: a sharp forest-steppe boundary influences the taxonomic and functional organization of ant species assemblages along elevational gradients in northwestern Patagonia (Argentina). Biodivers. Conserv. 24, 287–308 (2015).Article 

    Google Scholar 
    69.Diaz, S., Cabido, M. & Casanoves, F. Plant functional traits and environmental filters at a regional scale. J. Veg. Sci. 9, 113–122 (1998).Article 

    Google Scholar 
    70.Grime, J. P. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902–910 (1998).Article 

    Google Scholar 
    71.Carreño-Rocabado, G. et al. Land-use intensification effects on functional properties in tropical plant communities. Ecol. Appl. https://doi.org/10.1007/s11548-012-0737-y (2015).Article 

    Google Scholar 
    72.Pérez-Harguindeguy, N. et al. New Handbook for standardized measurment of plant functional traits worldwide. Aust. J. Bot. 61, 167–234 (2013).Article 

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

    Google Scholar 
    74.Legendre, P. & Legendre, L. F. J. Numerical Ecology. (Elsevier, 2012).75.Kembel, S. W. et al. Package ‘ picante ’: Integrating Phylogenies and Ecology. Cran-R 1–55 (2018). https://doi.org/10.1093/bioinformatics/btq166 >.License.76.Swenson, N. G., Anglada-Cordero, P. & Barone, J. A. Deterministic tropical tree community turnover: evidence from patterns of functional beta diversity along an elevational gradient. Proc. R. Soc. B Biol. Sci. 278, 877–884 (2011).Article 

    Google Scholar 
    77.Cribari-Neto, F. & Zeileis, A. Journal of Statistical Software. J. Stat. Softw. 34, 1–24 (2010).Article 

    Google Scholar 
    78.Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).MATH 

    Google Scholar 
    79.Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).Article 

    Google Scholar 
    80.Grace, J. B. Structural Equation Modeling and Natural Systems. (Cambridge University Press, 2006).81.Fan, Y. et al. Applications of structural equation modeling (SEM) in ecological studies: an updated review. Ecol. Process. 5, 19 (2016).ADS 
    Article 

    Google Scholar 
    82.Lefcheck, J. S. piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).Article 

    Google Scholar 
    83.Lefcheck, J., Byrnes, J. & Grace, J. Package ‘ piecewiseSEM ’. R (2019).84.Brown, A. M. et al. The fourth-corner solution – using predictive models to understand how species traits interact with the environment. Methods Ecol. Evol. 5, 344–352 (2014).Article 

    Google Scholar 
    85.Hastie, T., Tibshirani, R. & Friedman, J. The Elements of Statistical Learning: Data Mining, Inference and Prediction. (2009).86.Barton, K. Package ‘MuMIn’.Multi-Model Inference. (2018).87.Dawson, S. K. et al. Plant traits of propagule banks and standing vegetation reveal flooding alleviates impacts of agriculture on wetland restoration. J. Appl. Ecol. 54, 1907–1918 (2017).Article 

    Google Scholar 
    88.QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. (2019). http://qgis.osgeo.org More