More stories

  • in

    Strong positively diversity–productivity relationships in the natural sub-alpine meadow communities across time are up to superior performers

    Study site
    Our study site is the species-rich sub-alpine meadows located in the eastern part of the Qinghai-Tibetan plateau, Hezuo, China (34°55′N, 102°53′E) with mean elevation approximately 3000 m above sea level. Although the Tibetan Plateau Monsoon and Asian Monsoon28 brings rain, the study region has cold and dry climate, with mean annual temperature of 2.4° C and mean annual precipitation of just 530 mm23. The vegetation is dominated by herbaceous species such as Elymus nutans Griseb (Poaceae), Kobresia humilis (C.A. Mey.) Serg. (Cyperaceae) and Thermopsis lanceolata R. Br. (Fabaceae)23. Human impacts include agricultural exploitation and pastoralism are the primary current land use, which in places have caused serious land degradation. In response, local governments have stopped further agricultural exploitation and constructed fences to restrict livestock grazing. These efforts gave rise to successional chronosequences, such as the ones we use in our study.
    We identified a chronosequence of fields that had been undisturbed for 4-, 6-, 10-, 13-, and 40-years (the control)19,23. All our sample sites, except for the control meadows, had been used for agriculture to grow highland barley in the recent past, with cessation of cultivation within the last 4–13 years. The time since last agricultural use was determined by interviews with local farmers. There are 1–10 km apart among the five meadows and all meadows possessed comparable topographic characteristics (e.g., orientation and slope), soil types and climate (Fig. 1A). This chronosequence is one of the same chronosequence in our previous work23 and we have observed that species richness increased from 61 to 82 species during succession, with 50 species sharing among all five successional meadows. Species composition was similar between 4-year and 6-year meadows, with 60 species sharing between these two meadows. Similar patterns were found in late successional meadows, with 70 species shared among 10-year, 13-year and undisturbed meadows.
    Figure 1

    Location map of our study sites and our quadrat sampling design. (A) locations of five sites representing each of the five successional ages (4-, 6-, 10-, 13-year and undisturbed grassland), (B) the 30 0.5 × 0.5 m2 quadrats sampling design in each of the five successional meadows. The map of Fig. 1A was obtained from Google Earth online version (https://earth.google.com/, access on 12/10/2018). Figure labels on the map were added using Google Earth online toolkit and text labels using Windows image processing software Paint.

    Full size image

    Field sampling
    The vegetation in each field was sampled in August 2013. An area of 120 × 120 m2 was randomly selected in each meadow. Within this area, thirty 0.5 × 0.5 m2 quadrats were regularly arranged in six parallel transects, with 20 m intervals between each two adjacent quadrats (detail please see Fig. 1B). To determine species richness and abundances, in each quadrat we recorded all the aboveground ramets and identified them to species.
    To determine aboveground biomass, we removed all the ramets in each quadrat and took them to the laboratory, where they were oven-dried at 100℃ for 2 days and then weighed. Productivity is typically the amount of carbon fixed per unit time, not standing biomass. Here we follow methods of previous diversity–productivity studies in grasslands29,30, which have used aboveground biomass as proxy for productivity.
    Functional trait data collection
    We quantified the carbon economy of leaves by measuring specific leaf area (SLA, cm2 g−1). We quantified light capture strategy via photosynthesis rate (A, u mol−1). We estimated resistance to abiotic stress via leaf proline content (Pro, mg/kg), seed mass (SM, g) and seed germination rate (SG, %). Importantly, the functional traits for the same species at each successional age separately if they occurred in multiple meadows were measured to ensure that successional age-related intraspecific variation was appropriately incorporated into our analyses. All functional traits were determined as described in our previous work19,22,23 and the detailed procedures were given in the Supplementary Material.
    Statistical methods
    First, we compared variation during successional change in the proportion of total biomass for the three main functional groups of plants: forbs (dominant in early succession), legumes, and graminoids (both dominant in later succession) to check whether there are significant turnovers in the dominant plant taxa from early to late succession. Then, we used Spearman correlation analysis to quantify whether significantly positive correlations between empirical species diversity (S, numbers of species richness per square meters) and productivity (aboveground biomass per square meters, P) can be observed in each successional meadow.
    For each of the five functional traits (SLA, A, Pro, Sm, and SG), we calculated two functional diversity indices: the community-weighted mean (CWM) and functional diversity (FD) represented by Rao’s quadratic entropy (RaoQ).
    The two indices were calculated as follows:

    $$ {CWM} = sumlimits_{i = 1}^{n} {p_{ij} times t_{ij} } $$
    (1)

    where pij is the relative abundance of the species i in each 0.5 × 0.5 m2 quadrat j, and tijis the mean trait value of the species i in each successional meadow j.

    $$ RaoQ_{i} = sumlimits_{i = 1}^{n} {sumlimits_{i = 1}^{n} {p_{i} times p_{k} times d_{ik} } } $$
    (2)

    where pi and pkare the relative abundance of species i and k in each 0.5 × 0.5m2 quadrat j respectively and dik is the dissimilarity coefficient based on Euclidean distance between two species i and k in the multivariate trait space of each successional meadow j.
    Then, a variance partitioning analysis was used to test the relative contributions of species richness, the CWM and FD represented by RaoQ of these five traits to productivity in each successional meadow. We also used variance partitioning to allocate changes in productivity in each successional meadow arising from four complementary components: (a) variation explained by species richness, (b) variation explained CWM of each of the five traits, (c) variation explained by FD of each of the five traits only, and (d) “unexplained variation”31. Across all successional meadows, species richness, and aboveground biomass, CWM and FD of all five traits (SLA, A, Pro, SM, and SG) were strongly right-skewed, so we log-transformed species richness, and aboveground biomass, CWM and FD of all five traits to meet the assumption of normality required by variance partitioning. At each successional meadow, variance partitioning was done using the function of “varpart” in “vegan” package in R32. All analyses above were performed in R (R Core Team 2019). More

  • in

    Marine heatwaves and the collapse of marginal North Atlantic kelp forests

    1.
    Frölicher, T. L. & Laufkötter, C. Emerging risks from marine heat waves. Nat. Commun.9, 650 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 
    2.
    Coumou, D. & Rahmstorf, S. A decade of weather extremes. Nat. Clim. Change2, 491–496 (2012).
    ADS  Google Scholar 

    3.
    Gaines, S. D. & Denny, M. W. The largest, smallest, highest, lowest, longest, and shortest: Extremes in ecology. Ecology74, 1677–1692 (1993).
    Google Scholar 

    4.
    Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr.141, 227–238 (2016).
    ADS  Google Scholar 

    5.
    Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change9, 306–312 (2019).
    ADS  Google Scholar 

    6.
    Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change8, 579–587 (2018).
    ADS  Google Scholar 

    7.
    Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun.9, 1324 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 

    8.
    Oliver, E. C. J. et al. The unprecedented 2015/16 Tasman Sea marine heatwave. Nat. Commun.8, 16101 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    9.
    IPCC. The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press, Cambridge, 2013).

    10.
    Jentsch, A. & Beierkuhnlein, C. External geophysics, climate and environment. C. R. Geosci.340 (2008).

    11.
    Wernberg, T., Smale, D. A. & Thomsen, M. S. A decade of climate change experiments on marine organisms: Procedures, patterns and problems. Glob. Change Biol.18, 1491–1498 (2012).
    ADS  Google Scholar 

    12.
    Kordas, R. L., Harley, C. D. G. & O’Connor, M. I. Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Biol. Ecol.400, 218–226 (2011).
    Google Scholar 

    13.
    Hobday, A. J. et al. Categorizing and naming marine heatwaves. Oceanography31, 162–173 (2018).
    Google Scholar 

    14.
    Wernberg, T. et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change3, 78–82 (2013).
    ADS  Google Scholar 

    15.
    Wernberg, T., Krumhansl, K. A., Filbee-Dexter, K. & Pedersen, M. F. In World Seas: An Environmental Evaluation, Vol III: Ecological Issues and Environmental Impacts (ed. Sheppard, C.) (Academic Press, Cambridge, 2019).

    16.
    Lüning, K., Yarish, C. & Kirkman, H. Seaweeds: Their Environment, Biogeography, and Ecophysiology (Wiley, Hoboken, 1990).
    Google Scholar 

    17.
    Assis, J., Araújo, M. B. & Serrão, E. A. Projected climate changes threaten ancient refugia of kelp forests in the North Atlantic. Glob. Change Biol.24, e55–e66 (2018).
    ADS  Google Scholar 

    18.
    Wilson, K. L., Skinner, M. A. & Lotze, H. K. Projected 21st-century distribution of canopy-forming seaweeds in the Northwest Atlantic with climate change. Divers. Distrib. 25, 582–602. (2019).
    Article  Google Scholar 

    19.
    Fernández, C. The retreat of large brown seaweeds on the north coast of Spain: The case of Saccorhiza polyschides. Eur. J. Phycol.46, 352–360 (2011).
    Google Scholar 

    20.
    Filbee-Dexter, K., Feehan, C. J. & Scheibling, R. E. Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Mar. Ecol. Prog. Ser.543, 141–152 (2016).
    ADS  CAS  Google Scholar 

    21.
    Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science (80-).353, 169–172 (2016).
    ADS  CAS  Google Scholar 

    22.
    Rogers-Bennett, L. & Catton, C. A. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep.9, 1–9 (2019).
    CAS  Google Scholar 

    23.
    Arafeh-Dalmau, N. et al. Extreme marine heatwaves alter kelp forest community near its equatorward distribution limit. Front. Mar. Sci.6, 499 (2019).
    Google Scholar 

    24.
    Starko, S. et al. Environmental heterogeneity mediates scale-dependent declines in kelp diversity on intertidal rocky shores. PLoS ONE14, e0213191 (2019).
    CAS  PubMed  PubMed Central  Google Scholar 

    25.
    Cavanaugh, K. C., Reed, D. C., Bell, T. W., Castorani, M. C. N. & Beas-Luna, R. Spatial variability in the resistance and resilience of giant kelp in southern and Baja California to a multiyear heatwave. Front. Mar. Sci.6, 413 (2019).
    Google Scholar 

    26.
    Simonson, E., Scheibling, R. & Metaxas, A. Kelp in hot water: I. Warming seawater temperature induces weakening and loss of kelp tissue. Mar. Ecol. Prog. Ser.537, 89–104 (2015).
    ADS  CAS  Google Scholar 

    27.
    Nepper-Davidsen, J., Andersen, D. T. & Pedersen, M. F. Effects of simulated heat wave scenarios on Saccharina latissima: Prolonged exposure to sub-lethal temperatures may cause irreversible damage. Mar. Ecol. Prog. Ser. 630, 25–39 (2020).
    ADS  Google Scholar 

    28.
    Hollarsmith, J. A., Buschmann, A. H., Camus, C. & Grosholz, E. D. Varying reproductive success under ocean warming and acidification across giant kelp (Macrocystis pyrifera) populations. J. Exp. Mar. Biol. Ecol.522, 151247 (2020).
    Google Scholar 

    29.
    Straub, S. C. Effects of marine heatwaves on canopy forming seaweeds and marine forests (University of Western Australia, Perth, 2019).
    Google Scholar 

    30.
    Wernberg, T. et al. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep.8, 1851 (2018).
    ADS  PubMed  PubMed Central  Google Scholar 

    31.
    Bernhardt, J. R. & Leslie, H. M. Resilience to climate change in coastal marine ecosystems. Ann. Rev. Mar. Sci.5, 371–392 (2013).
    PubMed  Google Scholar 

    32.
    Filbee-Dexter, K. & Wernberg, T. Rise of Turfs: A new battlefront for globally declining kelp forests. Bioscience68, 64–76 (2018).
    Google Scholar 

    33.
    Krause-Jensen, D. & Duarte, C. M. Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci.9, 737–742 (2016).
    ADS  CAS  Google Scholar 

    34.
    Norderhaug, K. M. & Christie, H. Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure. Estuar. Coast. Shelf Sci.95, 135–144 (2011).
    ADS  Google Scholar 

    35.
    Bertocci, I., Araújo, R., Oliveira, P. & Sousa-Pinto, I. Potential effects of kelp species on local fisheries. J. Appl. Ecol.52, 1216–1226 (2015).
    Google Scholar 

    36.
    Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser.612, 209–215 (2019).
    ADS  Google Scholar 

    37.
    Albretsen, J., Aure, J., Sætre, R. & Danielssen, D. S. Climatic variability in the Skagerrak and coastal waters of Norway. ICES J. Mar. Sci.69, 758–763 (2012).
    Google Scholar 

    38.
    Andersen, G. S., Steen, H., Christie, H., Fredriksen, S. & Emil Moy, F. Seasonal patterns of sporophyte growth, fertility, fouling, and mortality of Saccharina latissima in Skagerrak, Norway: Implications for Forest Recovery. J. Mar. Biol.2011, 690375 (2011).
    Google Scholar 

    39.
    Krumhansl, K. & Scheibling, R. Detrital production in Nova Scotian kelp beds: Patterns and processes. Mar. Ecol. Prog. Ser.421, 67–82 (2011).
    ADS  Google Scholar 

    40.
    Brady-Campbell, M. M., Campbell, D. B. & Harlin, M. M. Productivity of kelp (Laminaria spp.) near the southern limit in the Northwestern Atlantic Ocean. Mar. Ecol. Prog. Ser.18, 79–88 (1984).
    ADS  Google Scholar 

    41.
    Grace, S. P. Ecomorphology of the Temperate Scleractinian Astrangia poculata: Coral–Macroalgal Interactions in Narragansett Bay (University of Rhode Island, South Kingstown, 2004).
    Google Scholar 

    42.
    Moy, F. E. & Christie, H. Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar. Biol. Res.8, 309–321 (2012).
    Google Scholar 

    43.
    Lee, J.-A. & Brinkhuis, B. H. Reproductive phenology of Laminaria saccharina (L.) Lamour. (Phaeophyta) at the southern limit of its distribution in the northwestern Atlantic Ocean. J. Phycol.22, 276–285 (1986).
    Google Scholar 

    44.
    Feehan, C. J., Grace, S. P. & Narvaez, C. A. Ecological feedbacks stabilize a turf-dominated ecosystem at the southern extent of kelp forests in the Northwest Atlantic. Sci. Rep.9, 7078 (2019).
    ADS  PubMed  PubMed Central  Google Scholar 

    45.
    Sjøtun, K. Seasonal lamina growth in two age groups of Laminaria saccharina (L.) Lamour. in Western Norway. Bot. Mar.36, 433–442 (1993).
    Google Scholar 

    46.
    Martinez, E. A., Cardenas, L. & Pinto, R. Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Nino 1982/831. J. Phycol.39, 504–508 (2003).
    Google Scholar 

    47.
    Edwards, M. & Estes, J. Catastrophe, recovery and range limitation in NE Pacific kelp forests: A large-scale perspective. Mar. Ecol. Prog. Ser.320, 79–87 (2006).
    ADS  Google Scholar 

    48.
    Ummenhofer, C. C. & Meehl, G. A. Extreme weather and climate events with ecological relevance: A review. Philos. Trans. R. Soc. B Biol. Sci.372, 20160135 (2017).
    Google Scholar 

    49.
    Hobday, A. J. & Pecl, G. T. Identification of global marine hotspots: Sentinels for change and vanguards for adaptation action. Rev. Fish Biol. Fish.24, 415–425 (2014).
    Google Scholar 

    50.
    Sjøtun, K., Fredriksen, S., Lein, T. E., Rueness, J. & Sivertsen, K. Population studies of Laminaria hyperborea from its northern range of distribution in Norway. Hydrobiologia260–261, 215–221 (1993).
    Google Scholar 

    51.
    O’Brien, J. M. & Scheibling, R. E. Low recruitment, high tissue loss, and juvenile mortality limit recovery of kelp following large-scale defoliation. Mar. Biol.165, 171 (2018).
    Google Scholar 

    52.
    Borum, K., Pedersen, M. F., Krause-Jensen, D. & Christensen, N. Biomass, photosynthesis and growth of Laminaria saccharina in a high-arctic fjord, NE Greenland. Mar. Biol.141, 11–19 (2002).
    Google Scholar 

    53.
    Nielsen, M. M. et al. Growth dynamics of Saccharina latissima (Laminariales, Phaeophyceae) in Aarhus Bay, Denmark, and along the species’ distribution range. Mar. Biol.161, 2011–2022 (2014).
    CAS  Google Scholar 

    54.
    tom Dieck, I. Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta): Ecological and biogeographical implications. Mar. Ecol. Prog. Ser.100, 253–264 (1993).
    ADS  Google Scholar 

    55.
    Bolton, J. J. & Lüning, K. Optimal growth and maximal survival temperatures of Atlantic Laminaria species (Phaeophyta) in culture. Mar. Biol.66, 89–94 (1982).
    Google Scholar 

    56.
    Andersen, G. S., Pedersen, M. F. & Nielsen, S. L. Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales, Phaeophyceae). J. Phycol.49, 689–700 (2013).
    CAS  PubMed  Google Scholar 

    57.
    Jump, A. S. & Penuelas, J. Running to stand still: Adaptation and the response of plants to rapid climate change. Ecol. Lett.8, 1010–1020 (2005).
    Google Scholar 

    58.
    Niu, S. et al. Plant growth and mortality under climatic extremes: An overview. Environ. Exp. Bot.98, 13–19 (2014).
    Google Scholar 

    59.
    Bennett, S., Wernberg, T., Arackal Joy, B., de Bettignies, T. & Campbell, A. H. Central and rear-edge populations can be equally vulnerable to warming. Nat. Commun.6, 10280 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    60.
    Gorman, D. & Connell, S. D. Recovering subtidal forests in human-dominated landscapes. J. Appl. Ecol.46, 1258–1265 (2009).
    Google Scholar 

    61.
    Burek, K., O’Brien, J. & Scheibling, R. Wasted effort: Recruitment and persistence of kelp on algal turf. Mar. Ecol. Prog. Ser.600, 3–19 (2018).
    ADS  Google Scholar 

    62.
    Norderhaug, K. M. et al. Effects of climate and eutrophication on the diversity of hard bottom communities on the Skagerrak coast 1990–2010. Mar. Ecol. Prog. Ser.530, 29–46 (2015).
    ADS  CAS  Google Scholar 

    63.
    Gorgula, S. & Connell, S. Expansive covers of turf-forming algae on human-dominated coast: The relative effects of increasing nutrient and sediment loads. Mar. Biol.145, 613–619 (2004).
    Google Scholar 

    64.
    Bennett, S., Duarte, C. M., Marbà, N. & Wernberg, T. Integrating within-species variation in thermal physiology into climate change ecology. Philos. Trans. R. Soc. B Biol. Sci.374, 20180550 (2019).
    Google Scholar 

    65.
    Lüning, K. Temperature tolerance and biogeography of seaweeds: The marine algal flora of Helgoland (North Sea) as an example. Helgoländer Meeresunters. 38, 305–317 (1984).
    Google Scholar 

    66.
    Lee, J. A. & Brinkhuis, B. H. Seasonal light and temperature interaction effects on development of Laminaria saccharina (Phaeophyta) gametophytes and juvenile sporophytes. J. Phycol.24, 181–191 (1988).
    Google Scholar 

    67.
    Pedersen, M. F. et al. Detrital carbon production and export in high latitude kelp forests. Oecologia192, 227–239 (2020).
    ADS  PubMed  Google Scholar 

    68.
    Schlegel, R. W. & Smit, A. J. heatwaveR: Detect Heatwaves and Cold-Spells. (2019).

    69.
    Wasko, C. & Sharma, A. Quantile regression for investigating scaling of extreme precipitation with temperature. Water Resour. Res.50, 3608–3614 (2014).
    ADS  Google Scholar 

    70.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw.67, 1–48 (2015).
    Google Scholar 

    71.
    Schlegel, R. W. Marine Heatwave Tracker. https://doi.org/10.5281/zenodo.3787872 (2020).
    Article  Google Scholar  More

  • in

    Unique inducible filamentous motility identified in pathogenic Bacillus cereus group species

    Isolation of an environmental contaminant with preferential expansion on C. jejuni cell lawns
    We observed a contaminant colony that paradoxically grew preferentially on small, spot-plated lawns of C. jejuni cells on Mueller Hinton (MH) agar (1.5% w/v). The MH plate had previously been inoculated with C. jejuni cells spotted and incubated microaerobically at 38 °C overnight before being stored for several days aerobically at room temperature. Transfer of contaminant cells onto new, similarly prepared spot-plated lawns of C. jejuni resulted in the contaminant again growing preferentially atop the C. jejuni lawns, with minimal growth on the rich agar in between spots of C. jejuni lawns (Fig. 1a). The contaminant was isolated for further study and the strain named ML-A2C4.
    Fig. 1: Identification of the filamentous motile environmental isolate as Bacillus mobilis ML-A2C4.

    a ML-A2C4 filamentous growth on C. jejuni lawn spots (small circles). b ML-A2C4 growth on a control 1.5% agar MH plate (left) and on a MH plate spread with a full confluent C. jejuni lawn (center) after 48 h aerobic incubation at 30 °C. The red box shows a close-up view of the filaments at the growth edge (right). c Quantification of the visible growth diameter on control MH plates (black bars) and plates with C. jejuni lawns (red bars) over time (n = 5) with error bars indicating standard deviation (SD). Statistical analysis was performed for growth diameter on C. jejuni lawn plates versus control plates using the Student’s t test with Welch’s correction, and for 48 vs. 24 h using repeated measures one-way ANOVA, with ****p  More

  • in

    The first evidence for Late Pleistocene dogs in Italy

    1.
    Larson, G. et al. Rethinking dog domestication by integrating genetics, archaeology, and biogeography. Proc. Natl. Acad. Sci. U. S. A.109, 8878–8883 (2012).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 
    2.
    Shannon, L. M. Genetic structure in village dogs reveals a Central Asian domestication origin. Proc. Natl. Acad. Sci. U. S. A.112, 13639–13644 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    3.
    Skoglund, P., Ersmark, E., Palkopoulou, E. & Dalén, L. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr. Biol.25, 1–5 (2015).
    Google Scholar 

    4.
    Thalmann, O. et al. Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science342, 871–874 (2013).
    ADS  CAS  PubMed  Google Scholar 

    5.
    Frantz, L. A. et al. Genomic and archaeological evidence suggests a dual origin of domestic dogs. Science352, 1228–1231 (2016).
    ADS  CAS  PubMed  Google Scholar 

    6.
    Germonpré, M. et al. Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J. Archaeol. Sci.36, 473–490 (2009).
    Google Scholar 

    7.
    Germonpré, M. et al. Palaeolithic dogs and the early domestication of the wolf: a reply to the comments of Crockford and Kuzmin (2012). J. Archaeol. Sci.40, 786–792 (2013).
    Google Scholar 

    8.
    Gremonpré, M. et al. Palaeolithic dogs and Pleistocene wolves revisited: a reply to Morey (2014). J. Archaeol. Sci.54, 210–216 (2015).
    Google Scholar 

    9.
    Germonpré, M. et al. Palaeolithic and prehistoric dogs and Pleistocene wolves from Yakutia: identification of isolated skulls. J. Archaeol. Sci.78, 1–19 (2017).
    Google Scholar 

    10.
    Crockford, S. J. & Kuzmin, Y. V. Comments on Germonpré et al. (2012) Journal of Archaeological Science 36, 2009 “Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes”, and Germonpré, Lázki cková-Galetová, and Sablin, Journal of Archaeological Science 39, 2012 “Palaeolithic dog skulls at the Gravettian Predmostí site, the Czech Republic”. J. Archaeol. Sci.39, 2797–2801 (2012).
    Google Scholar 

    11.
    Morey, D. F. In search of Paleolithic dogs: a quest with mixed results. J. Archaeol. Sci.52, 300–307 (2014).
    CAS  Google Scholar 

    12.
    Botigué, L. R. et al. Ancient European dog genomes reveal continuity since the Early Neolithic. Nat. Commun.8, 16082 (2017).
    ADS  PubMed  PubMed Central  Google Scholar 

    13.
    Camarós, E., Münzel, S. C., Cueto, M., Rivals, F. & Conard, N. J. The evolution of Paleolithic hominin–carnivore interaction written in teeth: stories from the Swabian Jura (Germany). J. Archaeol. Sci.6, 798–809 (2016).
    Google Scholar 

    14.
    Ovodov, N. D. et al. A 33,000-year-old incipient dog from the Altai Mountains of Siberia: evidence of the earliest domestication disrupted by the Last Glacial Maximum. PLoS ONE6, e22821 (2011).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    15.
    Sablin, M. & Khlopachev, G. The earliest Ice Age dogs: evidence from Eliseevichi. Curr. Anthropol.43, 795–799 (2002).
    Google Scholar 

    16.
    Boudadi-Maligne, M. & Escarguel, G. A biometric re-evaluation of recent claims for Early Upper Palaeolithic wolf domestication in Eurasia. J. Archaeol. Sci.45, 80–89 (2014).
    Google Scholar 

    17.
    Drake, A. G., Coquerelle, M. & Colombeau, G. 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic. Sci. Rep.5, 8299 (2015).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    18.
    Morey, D. F. & Jeger, R. Paleolithic dogs: why sustained domestication then?. J. Archaeol. Sci.3, 420–428 (2015).
    Google Scholar 

    19.
    Napierala, H. & Uerpmann, H. P. A ‘new’ palaeolithic dog from central Europe. Intl. J. Osteoarchaeol.22, 127–137 (2012).
    Google Scholar 

    20.
    Perri, A. R. A wolf in dog’s clothing: initial dog domestication and Pleistocene wolf variation. J. Archaeol. Sci.68, 1–4 (2016).
    Google Scholar 

    21.
    Janssens, L. et al. A new look at an old dog: Bonn-Oberkassel reconsidered. J. Archaeol. Sci.92, 126–138 (2018).
    Google Scholar 

    22.
    Pionnier-Capitan, M. et al. New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe. J. Archaeol. Sci.38, 2123–2140 (2011).
    Google Scholar 

    23.
    Boudadi-Maligne, M., Mallye, J. B., Langlais, M. & Barshay-Szdmit, C. Des restes de chiens magdaléniens à l’abri du Morin (Gironde, France) Implications socio-économiques d’une innovation zootechnique. Paleo23, 39–54 (2012).
    Google Scholar 

    24.
    Thalmann, O. & Perri, A. R. Paleogenomics 273–306 (Springer, Cham, 2018).
    Google Scholar 

    25.
    Mariotti Lippi, M., Foggi, B., Aranguren, B., Ronchitelli, A. & Revedin, A. Multistep food plant processing at Grotta Paglicci (Southern Italy) around 32,600 cal B.P.. Proc. Natl. Acad. Sci. U. S. A.112, 12075–12080 (2015).
    ADS  PubMed  PubMed Central  Google Scholar 

    26.
    Mezzena, F. & Palma di Cesnola, A. Industria acheulena “in situ” nei depositi esterni della Grotta Paglicci (Rignano Garganico – Foggia). Riv. Sci. Preist.26, 3–30 (1971).
    Google Scholar 

    27.
    Crezzini, J. et al. A spotted hyaena den in the Middle Palaeolithic of Grotta Paglicci (Gargano promontory, Apulia, Southern Italy). Archaeol. Anthropol. Sci.8, 227–240 (2016).
    Google Scholar 

    28.
    Palma di Cesnola, A. L’Aurignacien et le Gravettien ancien de la grotte Paglicci au Mont Gargano. L’Anthropologie110, 355–370 (2006).
    Google Scholar 

    29.
    PalmadiCesnola, A. Le Paléolithique supérieur en Italie (Jérôme Millon, Grenoble, 2001).
    Google Scholar 

    30.
    Berto, C., Boscato, P., Boschin, F., Luzi, E. & Ronchitelli, A. Paleoenvironmental and paleoclimatic context during the Upper Paleolithic (late Upper Pleistocene) in the Italian Peninsula. The small mammal record from Grotta Paglicci (Rignano Garganico, Foggia, Southern Italy). Quat. Sci. Rev.168, 30–41 (2017).
    ADS  Google Scholar 

    31.
    Boschin, F. et al. The palaeoecological meaning of macromammal remains from archaeological sites exemplified by the case study of Grotta Paglicci (Upper Palaeolithic, southern Italy). Quat. Res.90, 470–482 (2018).
    CAS  Google Scholar 

    32.
    Borgia, V., Boschin, F. & Ronchitelli, A. Bone and antler working at Grotta Paglicci (Rignano Garganico, Foggia, southern Italy). Quat. Int.403, 23–39 (2016).
    Google Scholar 

    33.
    Condemi, S. et al. I resti umani rinvenuti a Paglicci (Rignano Garganico – FG): nota preliminare. Annali dell’Uiversità di Ferrara, Museologia Scientifica e Naturalistica10(2), 233–238 (2014).
    Google Scholar 

    34.
    Arrighi, S., Borgia, V., d’Errico, F. & Ronchitelli, A. I ciottoli decorati di Paglicci: raffigurazioni e utilizzo. Riv. Sci. Preist.58, 39–58 (2008).
    Google Scholar 

    35.
    Arrighi, S., Borgia, V., d’Errico, F., Ricci, S. & Ronchitelli, A. Manifestazioni d’arte inedite e analisi tecnologica dell’arte mobiliare di Grotta Paglicci (Rignano Garganico – Foggia). Preist. Alpina46, 49–58 (2012).
    Google Scholar 

    36.
    Arrighi, S. et al. Grotta Paglicci (Rignano Garganico, Foggia): analisi sulle materie coloranti. Preist. Alpina46, 91–92 (2012).
    Google Scholar 

    37.
    Ronchitelli, A. et al. When technology joins symbolic behaviour: the gravettian burials at Grotta Paglicci (Rignano Garganico – Foggia – southern Italy). Quat. Int.359–360, 423–441 (2015).
    Google Scholar 

    38.
    Cassoli, P. F., Fiore, I. & Tagliacozzo, A. Butchering and exploitation of large mammals in the Epigravettian levels of Grotta Romanelli (Apulia, Italy). Anthropozoologica25–26, 309–318 (1997).
    Google Scholar 

    39.
    Sardella, R. et al. Grotta Romanelli (southern Italy, Apulia): legacies and issues in excavating a key site for the Pleistocene of the Mediterranean. Riv. Ital. Paleontol. Strat.124, 247–264 (2018).
    Google Scholar 

    40.
    Sardella, R. et al. Grotta Romanelli (Lecce, Southern Italy) between past and future: new studies and perspectives for an archaeo-geosite symbol of the Palaeolithic in Europe. Geoheritage11, 1413–1432 (2019).
    Google Scholar 

    41.
    Calcagnile, L. et al. New radiocarbon dating results from the Upper Paleolithic–Mesolithic levels in Grotta Romanelli (Apulia, southern Italy). Radiocarbon61, 1211–1220 (2019).
    CAS  Google Scholar 

    42.
    Cassoli, P.F., Gala, M. & Tagliacozzo, A. In Grotta Romanelli nel centenario della sua scoperta (1900–2000). Conference Proceedings (eds Fabbri, P.F., Ingravallo, E., Mangia, A.) 91–111 (Congedo Editore, Galatina, 2003).

    43.
    Tagliacozzo, A. Grotta Romanelli nel centenario della sua scoperta (1900–2000). Conference Proceedings (eds Fabbri, P.F., Ingravallo, E., Mangia, A.) 169–216 (Congedo Editore, Galatina, 2003).

    44.
    Boschin, F., Bernardini, F., Zanolli, C. & Tuniz, C. MicroCT imaging of red fox talus: a non-invasive approach to evaluate age at death. Archaeometry57, 194–211 (2015).
    CAS  Google Scholar 

    45.
    Boschin, F., Zanolli, C., Bernardini, F., Princivalle, F. & Tuniz, C. A Look from the inside: MicroCT analysis of burned bones. Ethnobiol. Lett.6, 41–49 (2015).
    Google Scholar 

    46.
    Geiger, M. et al. Unaltered sequence of dental, skeletal, and sexual maturity in domestic dogs compared to the wolf. Zool. Lett.2, 16 (2016).
    Google Scholar 

    47.
    Payne, S. & Bull, G. Components of variation in measurements of pig bones and teeth, and the use of measurements to distinguish wild from domestic pig remains. Archaeozoologia2, 27–66 (1988).
    Google Scholar 

    48.
    Zanolli, C. et al. Inner tooth morphology of Homo erectus from Zhoukoudian. New evidence from an old collection housed at Uppsala University, Sweden. J. Hum. Evol.116, 1–13 (2018).
    PubMed  Google Scholar 

    49.
    Zanolli, C. et al. Evidence for increased hominid diversity in the Early to Middle Pleistocene of Indonesia. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-019-0860-z (2019).
    Article  PubMed  Google Scholar 

    50.
    Maricic, T., Whitten, M. & Pääbo, S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS ONE5, e14004 (2010).
    ADS  PubMed  PubMed Central  Google Scholar 

    51.
    Hefner, R. & Geffen, E. Group size and home range of the Arabian wolf (Canis lupus) in Southern Israel. J. Mammal.80, 611–619 (1999).
    Google Scholar 

    52.
    Gaubert, P. et al. Reviving the African Wolf Canis lupus lupaster in North and West Africa: a mitochondrial lineage ranging more than 6,000 km wide. PLoS ONE7, e42740 (2012).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    53.
    Prothero, D. R. et al. Size and shape stasis in late Pleistocene mammals and birds from Rancho La Brea during the Last Glacial-Interglacial cycle. Quat. Sci. Rev.56, 1–10 (2012).
    ADS  Google Scholar 

    54.
    Payne, S. Paleolithic site of Douara Cave and Paleogeography of Palmyra Basin in Syria, part III: animal bones and further analysis of archeological materials 1–108 (University of Tokyo Press, Tokyo, 1983).
    Google Scholar 

    55.
    Mecozzi, B. & Lucenti, S. B. The Late Pleistocene Canis lupus (Canidae, Mammalia) from Avetrana (Apulia, Italy): reappraisal and new insights on the European glacial wolves, I. J. Geosci.137, 138–150 (2018).
    Google Scholar 

    56.
    Rustioni, M., Ferretti, M. P., Mazza, P., Pavia, M. & Varola, A. The vertebrate fauna from Cardamone (Apulia, southern Italy): an example of Mediterranean mammoth fauna. Deinsea9, 395–404 (2003).
    Google Scholar 

    57.
    Sardella, R. et al. The wolf from Grotta Romanelli (Apulia, Italy) and its implications in the evolutionary history of Canis lupus in the Late Pleistocene of Southern Italy. Quat. Int.328–329, 179–195 (2014).
    Google Scholar 

    58.
    Trut, L. N. The Genetics of the Dog 15–42 (CABI Publishing, New York, 2001).
    Google Scholar 

    59.
    Hare, B., Wobber, V. & Wrangham, R. The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Anim. Behav.83, 573–585 (2012).
    Google Scholar 

    60.
    Lord, K. A., Larson, G., Coppinger, R. P. & Karlsson, E. The history of farm foxes undermines the animal domestication syndrome. Trends Ecol.35, 125–136 (2020).
    Google Scholar 

    61.
    Marshall-Pescini, S., Cafazzo, S., Virány, Z. & Range, F. Integrating social ecology in explanation of wolf-dog behavioural differences. Curr. Opin. Behav. Sci.16, 80–86 (2017).
    Google Scholar 

    62.
    Leonard, J. A., Vilà, C., Fox-Dobbs, K., Koch, P. L. & Wayne, R. K. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr. Biol.17, 1146–1150 (2007).
    CAS  PubMed  Google Scholar 

    63.
    Hare, B., Brown, M., Williamson, C. & Tommasello, M. The domestication of social cognition in dogs. Science298, 1634–1636 (2002).
    ADS  CAS  PubMed  Google Scholar 

    64.
    Wobber, V. et al. Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals. Interact. Stud.10, 206–224 (2009).
    Google Scholar 

    65.
    Riedel, A. I resti animali della grotta delle Ossa (Škocjan). Atti del Museo Civico di Storia Naturale di Trieste30, 125–208 (1977).
    Google Scholar 

    66.
    Detry, C. & Cardoso, J. L. On some remains of dog (Canis familiaris) from the Mesolithic shell-middens of Muge, Portugal. J. Archaeol. Sci.37, 2762–2774 (2010).
    Google Scholar 

    67.
    von den Driesch, A. A guide to measurement of animal bones from archaeological sites. Peabody Mus. Bull.1, 1–148 (1976).
    Google Scholar 

    68.
    Tuniz, C. et al. The ICTP-Elettra X-ray laboratory for cultural heritage and archaeology. Nucl. Instrum. Methods Phys. Res. A711, 106–110 (2013).
    ADS  CAS  Google Scholar 

    69.
    Fajardo, R. J., Ryan, T. M. & Kappelman, J. Assessing the accuracy of high resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. Am. J. Phys. Anthropol.118, 1–10 (2002).
    PubMed  Google Scholar 

    70.
    Coleman, M. N. & Colbert, M. W. CT thresholding protocols for taking measurements on three-dimensional models. Am. J. Phys. Anthropol.133, 723–725 (2007).
    PubMed  Google Scholar 

    71.
    Bouxsein, M. et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res.25, 1468–1486 (2010).
    PubMed  Google Scholar 

    72.
    Shipman, P., Foster, G. & Schoeninger, M. Burnt bones and teeth: an experimental study of color, morphology, crystal structure and shrinkage. J. Archaeol. Sci.11, 307–325 (1984).
    Google Scholar 

    73.
    Ghezzo, E. & Rook, L. Cuon alpinus (Pallas, 1811) (Mammalia, Carnivora) from Equi (Late Pleistocene, Massa-Carrara, Italy): anatomical analysis and palaeoethological contextualisation. Rend. Fis. Acc. Lincei25, 492–504 (2014).
    Google Scholar 

    74.
    Gunz, P. & Mitteroecker, P. Semilandmarks: a method for quantifying curves and surfaces. Hystrix24, 103–109 (2013).
    Google Scholar 

    75.
    Adams, D.C., Collyer, D.L., Kaliontzopoulou, A. & Sherratt, E. Geomorph: software for geometric morphometric analyses. R package version 3.0.5. https://cran.r-project.org/package=geomorph (2017).

    76.
    Schlager, S. Statistical Shape and Deformation Analysis 217–256 (Academic Press, London, 2017).
    Google Scholar 

    77.
    Mitteroecker, P. & Bookstein, F. L. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol. Biol.38, 100–114 (2011).
    Google Scholar 

    78.
    Dray, S. & Dufour, A. B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw.22, 1–20 (2007).
    Google Scholar 

    79.
    Bookstein, F. L. Morphometric Tools for Landmark Data: Geometry and Biology (Cambridge University Press, Cambridge, 1991).
    Google Scholar 

    80.
    Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. U. S. A.110, 15758–15763 (2013).
    ADS  CAS  PubMed  PubMed Central  Google Scholar 

    81.
    Meyer, M. & Kircher, M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. https://doi.org/10.1101/pdb.prot5448 (2010).
    Article  PubMed  Google Scholar 

    82.
    Peltzer, G. et al. EAGER: efficient ancient genome reconstruction. Genome Biol.17, 60 (2016).
    PubMed  PubMed Central  Google Scholar 

    83.
    Kim, K. S., Lee, S. E., Jeong, H. W. & Ha, J. H. The complete nucleotide sequence of the domestic dog (Canis familiaris) mitochondrial genome. Mol. Phylogenet. Evol.10, 210–220 (1998).
    CAS  PubMed  Google Scholar 

    84.
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics25, 1754–1760 (2009).
    CAS  PubMed  PubMed Central  Google Scholar 

    85.
    Schubert, M. et al. Improving ancient DNA read mapping against modern reference genomes. BMC Genom.13, 178 (2012).
    CAS  Google Scholar 

    86.
    Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics25, 2078–2079 (2009).
    PubMed  PubMed Central  Google Scholar 

    87.
    Jonsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. & Orlando, L. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics29, 1682–1684 (2013).
    CAS  PubMed  PubMed Central  Google Scholar 

    88.
    Loog, L. et al. Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia. Mol Ecol.00, 1–15. https://doi.org/10.1111/mec.15329 (2019).
    Article  Google Scholar 

    89.
    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol.33, 1870–1874 (2016).
    CAS  PubMed  Google Scholar 

    90.
    Edgar, C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res.32, 1792–1797 (2004).
    CAS  PubMed  PubMed Central  Google Scholar 

    91.
    Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol.10, e1003537 (2014).
    PubMed  PubMed Central  Google Scholar 

    92.
    Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. Tracer v1.6. https://tree.bio.ed.ac.uk/software/tracer (2014)

    93.
    Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon51, 337–360 (2009).
    Google Scholar 

    94.
    Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon55, 1869–1887 (2013).
    CAS  Google Scholar 

    95.
    Street, M., Napierala, H. & Janssens, L. The late Palaeolithic dog from Bonn-Oberkassel in context. Rheinische Ausgrabungen72, 253–274 (2015).
    Google Scholar 

    96.
    Bronk Ramsey, C., Higham, T., Bowles, A. & Hedges, R. Improvements to the pretreatment of bones at Oxford. Radiocarbon46(1), 155–163 (2004).
    Google Scholar 

    97.
    Fedi, M. E., Cartocci, A., Manetti, M., Taccetti, F. & Mandò, P. A. The 14C AMS facility at LABEC, Florence. Nucl. Instrum. Methods Phys. Res. B259, 18–22 (2007).
    ADS  CAS  Google Scholar 

    98.
    Boschin, F. Exploitation of carnivores, lagomorphs and rodents at Grotta Paglicci during the Epigravettian: the dawn of a new subsistence strategy?. J. Archaeol. Sci. Rep.26, 101871 (2019).
    Google Scholar  More

  • in

    A large-scale assessment of lakes reveals a pervasive signal of land use on bacterial communities

    1.
    Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, et al. Lakes as sentinels of climate change. Limnol Oceanogr. 2009;54:2283–97.
    PubMed  PubMed Central  Google Scholar 
    2.
    Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr. 2009;54:2298–314.
    Google Scholar 

    3.
    Arbuckle KE, Downing JA. The influence of watershed land use on lake N: P in a predominantly agricultural landscape. Limnol Oceanogr. 2001;46:970–5.
    Google Scholar 

    4.
    Taranu ZE, Gregory-Eaves I. Quantifying relationships among phosphorus, agriculture, and lake depth at an inter-regional scale. Ecosystems. 2008;11:715–25.
    Google Scholar 

    5.
    Heisler J, Glibert PM, Burkholder JM, Anderson DM, Cochlan W, Dennison WC, et al. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae. 2008;8:3–13.
    PubMed  PubMed Central  Google Scholar 

    6.
    Scavia D, David Allan J, Arend KK, Bartell S, Beletsky D, Bosch NS, et al. Assessing and addressing the re-eutrophication of Lake Erie: Central basin hypoxia. J Gt Lakes Res. 2014;40:226–46.
    Google Scholar 

    7.
    Bastviken D, Cole J, Pace M, Tranvik L. Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cycles. 2004;18:1–12.
    Google Scholar 

    8.
    Novotny EV, Murphy D, Stefan HG. Increase of urban lake salinity by road deicing salt. Sci Total Environ. 2008;406:131–44.
    PubMed  Google Scholar 

    9.
    Dugan HA, Bartlett SL, Burke SM, Doubek JP, Krivak-Tetley FE, Skaff NK, et al. Salting our freshwater lakes. Proc Natl Acad Sci USA. 2017;114:4453–8.
    PubMed  Google Scholar 

    10.
    Hobbie SE, Finlay JC, Janke BD, Nidzgorski DA, Millet DB, Baker LA. Contrasting nitrogen and phosphorus budgets in urban watersheds and implications for managing urban water pollution. Proc Natl Acad Sci. 2017;114:4177–82.
    PubMed  Google Scholar 

    11.
    Shade A, Kent AD, Jones SE, Newton RJ, Triplett EW, McMahon KD. Interannual dynamics and phenology of bacterial communities in a eutrophic lake. Limnol Oceanogr. 2007;52:487–94.
    Google Scholar 

    12.
    Kara EL, Hanson PC, Hu YH, Winslow L, McMahon KD. A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA. ISME J. 2013;7:680–4.
    PubMed  Google Scholar 

    13.
    Marmen S, Blank L, Al-Ashhab A, Malik A, Ganzert L, Lalzar M, et al. The role of land use types and water chemical properties in structuring the microbiome of a connected lake system. Front Microbiol. 2020;11:1–16.
    Google Scholar 

    14.
    Environment Canada Whole organism responses and intersex severity in rainbow darter (Etheostoma caeruleum) following exposures to municipal wastewater in the Grand River basin, ON, Canada. Part A, Municipal Water Use Rep. 2011;159:2011–301.
    Google Scholar 

    15.
    Huot Y, Brown CA, Potvin G, Antoniades D, Baulch HM, Beisner BE, et al. The NSERC Canadian Lake Pulse Network: a national assessment of lake health providing science for water management in a changing climate. Sci Total Environ. 2019;695:133668.
    PubMed  Google Scholar 

    16.
    Lu Y, Wang R, Zhang Y, Su H, Wang P, Jenkins A, et al. Ecosystem health towards sustainability. Ecosyst Heal Sustain. 2015;1:1–15.
    Google Scholar 

    17.
    Hering D, Borja A, Carvalho L, Feld CK. Assessment and recovery of European water bodies: Key messages from the WISER project. Hydrobiologia 2013;704:1–9.
    Google Scholar 

    18.
    U.S. Environmental Protection Agency. National Lake Assessment: a collaborative survey of the Nation’s Lakes. Washington, DC: EPA 841-R-09-001; 2009.

    19.
    Ecological Stratification Working Group. A national ecological framework for Canada. Urbana-Champaign, Illinois: Ecological Stratification Working Group; 1996.

    20.
    Glaz P, Gagné JP, Archambault P, Sirois P, Nozais C. Impact of forest harvesting on water quality and fluorescence characteristics of dissolved organic matter in eastern Canadian Boreal Shield lakes in summer. Biogeosciences. 2015;12:6999–7011.
    Google Scholar 

    21.
    Patton C, Kryskalla J. Methods of analysis by the U.S. Geological Survey National Water Quality Laboratory—evaluation of alakline digestion as an alternative to kjedahl digestion for determination of total and dissolved nitrogen and phosphorous. Denver, Colorado: Water-Resources Investigations Report 03; 2003.

    22.
    U.S. Environmental Protection Agency. Method 200.7: determination of metals and trace elements in water and wastes by inductively coupled plasma-atomic emission spectrometry. Cincinatti, Ohio: U.S. Environmental Protection Agency; 1994.

    23.
    U.S. Environmental Protection Agency. Method 300.1: determination of inorganic anions in drinking water by ion chromatography. Cincinatti, Ohio; 1997.

    24.
    Wu Y. Barcode Demultiplex for Illumina I1, R1, R2 fastq.gz files. 2014.

    25.
    Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10.
    Google Scholar 

    26.
    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
    PubMed  PubMed Central  Google Scholar 

    27.
    Rohwer RR, Hamilton JJ, Newton RJ, McMahon KD. TaxAss: leveraging a custom freshwater database achieves fine-scale taxonomic resolution. mSphere. 2018;3:1–14.
    Google Scholar 

    28.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.
    Google Scholar 

    29.
    McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.
    PubMed  PubMed Central  Google Scholar 

    30.
    Price MN, Dehal PS, Arkin AP. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.
    PubMed  PubMed Central  Google Scholar 

    31.
    Dray S, Dufour A-B. The ade4 Package: implementing the duality diagram for ecologists. J Stat Softw. 2007;22:1–20.
    Google Scholar 

    32.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, et al. Vegan: community ecology package. 2016. https://cran.r-project.org; https://github.com/vegandevs/vegan.

    33.
    Hair J, Tatham R, Anderson R, Black W. Multivariate data analysis. 5th ed. London: Prentice-Hall; 1998.
    Google Scholar 

    34.
    R Development Core Team T. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2009.
    Google Scholar 

    35.
    Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team T. nlme: linear and nonlinear mixed effect models. R package version. 3.1-141; 2019.

    36.
    Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–51.
    Google Scholar 

    37.
    Rosseel Y. Lavaan: an R package for structural equation modeling. J Stat Softw. 2012;48:1–37.
    Google Scholar 

    38.
    Albanese D, Filosi M, Visintainer R, Riccadonna S, Jurman G, Furlanello C. Minerva and minepy: a C engine for the MINE suite and its R, Python and MATLAB wrappers. Bioinformatics. 2013;29:407–8.
    PubMed  Google Scholar 

    39.
    Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.
    PubMed  PubMed Central  Google Scholar 

    40.
    Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019;13:1722–36.
    PubMed  PubMed Central  Google Scholar 

    41.
    Barberán A, Bates ST, Casamayor EO, Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 2012;6:343–51.
    PubMed  Google Scholar 

    42.
    Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79.
    PubMed  PubMed Central  Google Scholar 

    43.
    Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, Daae FL, et al. Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol. 2002;4:349–60.
    PubMed  Google Scholar 

    44.
    Abed RMM, Kohls K, De Beer D. Effect of salinity changes on the bacterial diversity, photosynthesis and oxygen consumption of cyanobacterial mats from an intertidal flat of the Arabian Gulf. Environ Microbiol. 2007;9:1384–92.
    PubMed  Google Scholar 

    45.
    Lozupone CA, Knight R. Global patterns in bacterial diversity. Proc Natl Acad Sci USA. 2007;104:11436–40.
    PubMed  Google Scholar 

    46.
    Wu QL, Zwart G, Schauer M, Kamst-Van Agterveld MP, Hahn MW. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol. 2006;72:5478–85.
    PubMed  PubMed Central  Google Scholar 

    47.
    Wang J, Yang D, Zhang Y, Shen J, van der Gast C, Hahn MW, et al. Do patterns of bacterial diversity along salinity gradients differ from those observed for macroorganisms? PLoS ONE. 2011;6:e27597.
    PubMed  PubMed Central  Google Scholar 

    48.
    Kelly VR, Lovett GM, Weathers KC, Findlay SEG, Strayer DL, Burns DJ, et al. Long-term sodium chloride retention in a rural watershed: legacy effects of road salt on streamwater concentration. Environ Sci Technol. 2008;42:410–5.
    PubMed  Google Scholar 

    49.
    Corsi SR, Graczyk DJ, Geis SW, Booth NL, Richards KD. A fresh look at road salt: aquatic toxicity and water-quality impacts on local, regional, and national scales. Environ Sci Technol. 2010;44:7376–82.
    PubMed  PubMed Central  Google Scholar 

    50.
    Levine SN, Schindler DW. Influence of nitrogen to phosphorus supply ratios and physicochemical conditions on cyanobacteria and phytoplankton species composition in the Experimental Lakes Area, Canada. Can J Fish Aquat Sci. 1999;56:451–66.
    Google Scholar 

    51.
    Stockner JG, Shortreed KS. Response of Anabaena and Synechococcus to manipulation of nitrogen: phosphorus ratios in a lake fertilization experiment. Limnol Oceanogr. 1988;33:1348–61.
    Google Scholar 

    52.
    Thad Scott J, McCarthys MJ. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr. 2010;55:1265–70.
    Google Scholar 

    53.
    Håkanson L, Blenckner T, Bryhn AC, Hellström SS. The influence of calcium on the chlorophyll-phosphorus relationship and lake Secchi depths. Hydrobiologia. 2005;537:111–23.
    Google Scholar 

    54.
    Eiler A, Heinrich F, Bertilsson S. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J. 2012;6:330–42.
    PubMed  Google Scholar 

    55.
    Peura S, Bertilsson S, Jones RI, Eiler A. Resistant microbial cooccurrence patterns inferred by network topology. Appl Environ Microbiol. 2015;81:2090–7.
    PubMed  PubMed Central  Google Scholar 

    56.
    Logares R, Tesson SVM, Canbäck B, Pontarp M, Hedlund K, Rengefors K. Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes. Environ Microbiol. 2018;20:2231–40.
    PubMed  Google Scholar 

    57.
    Lindström ES, Kamst-Van Agterveld MP, Zwart G. Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol. 2005;71:8201–6.
    PubMed  PubMed Central  Google Scholar 

    58.
    Lauber CL, Hamady M, Knight R, Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol. 2009;75:5111–20.
    PubMed  PubMed Central  Google Scholar 

    59.
    Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, et al. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol. 2012;14:2457–66.
    PubMed  PubMed Central  Google Scholar 

    60.
    Findlay DL, Kasian SEM. Phytoplankton community responses to acidification of lake 223, experimental lakes area, northwestern Ontario. Water Air Soil Pollut. 1986;30:719–26.
    Google Scholar 

    61.
    Findlay DL, Kasian SEM. The effect of incremental pH recovery on the Lake 223 phytoplankton community. Can J Fish Aquat Sci. 1996;53:856–64.
    Google Scholar 

    62.
    Maberly SC. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshw Biol. 2008;35:579–98.
    Google Scholar 

    63.
    Tong Y, Lin G, Ke X, Liu F, Zhu G, Gao G, et al. Comparison of microbial community between two shallow freshwater lakes in middle Yangtze basin, East China. Chemosphere. 2005;60:85–92.
    PubMed  Google Scholar 

    64.
    Romina Schiaffino M, Unrein F, Gasol JM, Massana R, Balagué V, Izaguirre I. Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshw Biol. 2011;56:1973–91.
    Google Scholar 

    65.
    Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, et al. Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol. 2009;25:225–33.
    Google Scholar 

    66.
    Canfield DE, Bachmann RW. Prediction of total phosphorus concentrations, chlorophyll a, and Secchi depths in natural and artificial lakes. Can J Fish Aquat Sci. 1981;38:414–23.
    Google Scholar 

    67.
    Meeuwig JJ, Peters RH. Circumventing phosphorus in lake management: a comparison of chlorophyll a predictions from land-use and phosphorus-loading models. Can J Fish Aquat Sci. 1996;53:1795–806.
    Google Scholar 

    68.
    Yang L, Lei K, Meng W, Fu G, Yan W. Temporal and spatial changes in nutrients and chlorophyll-α in a shallow lake, Lake Chaohu, China: an 11-year investigation. J Environ Sci (China). 2013;25:1117–23.
    Google Scholar 

    69.
    Kraemer SA, Soucy JPR, Kassen R. Antagonistic interactions of soil pseudomonads are structured in time. FEMS Microbiol Ecol. 2017;93:1–9.
    Google Scholar  More

  • in

    Why deforestation and extinctions make pandemics more likely

    NEWS
    07 August 2020

    Researchers are redoubling efforts to understand links between species loss and emerging diseases — and use that information to predict and stop future outbreaks.

    Jeff Tollefson

    Search for this author in:

    Controlling deforestation (shown here, in a tropical rainforest in the Congo Basin) could decrease the risk of future pandemics, experts say.Credit: Patrick Landmann/Science Photo Library

    As humans diminish biodiversity by cutting down forests and building more infrastructure, they’re increasing the risk of disease pandemics such as COVID-19. Many ecologists have long suspected this, but a new study helps to reveal why: while some species are going extinct, those that tend to survive and thrive — rats and bats, for instance — are more likely to host potentially dangerous pathogens that can make the jump to humans.
    The analysis of around 6,800 ecological communities on 6 continents adds to a growing body of evidence that connects trends in human development and biodiversity loss to disease outbreaks — but stops short of projecting where new disease outbreaks might occur.
    “We’ve been warning about this for decades,” says Kate Jones, an ecological modeller at University College London and an author on the study, published on 5 August in Nature1. “Nobody paid any attention.”
    Jones is one of a cadre of researchers that has long been delving into relationships among biodiversity, land use and emerging infectious diseases. Their work has mostly flown below the radar, but now, as the world reels from the COVID-19 pandemic, efforts to map risks in communities across the globe and to project where diseases are most likely to emerge are taking centre stage.

    Last week, the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) hosted an online workshop on the nexus between biodiversity loss and emerging diseases. The organization’s goal now is to produce an expert assessment of the science underlying that connection ahead of a United Nations summit in New York that’s planned for September, where governments are expected to make new commitments to preserve biodiversity.
    Others are calling for a more wide-ranging course of action. On 24 July, an interdisciplinary group of scientists, including virologists, economists and ecologists, published an essay in Science2, arguing that governments can help reduce the risk of future pandemics by controlling deforestation and curbing the wildlife trade, which involves the sale and consumption of wild — and often rare — animals that can host dangerous pathogens.
    Most efforts to prevent the spread of new diseases tend to focus on vaccine development, early diagnosis and containment, but that’s like treating the symptoms without addressing the underlying cause, says Peter Daszak, a zoologist at the non-governmental organization EcoHealth Alliance in New York, who chaired the IPBES workshop. He says COVID-19 has helped to clarify the need to investigate biodiversity’s role in pathogen transmission.
    The latest work by Jones’s team bolsters the case for action, Daszak says. “We’re looking for ways to shift behaviour that would directly benefit biodiversity and reduce health risks.”
    Concentrating risk
    Previous research has shown that outbreaks of diseases such as severe acute respiratory syndrome (SARS) and bird influenza that cross over from animals to humans have increased in the past few decades3,4. This phenomenon is likely to be the direct result of increased contact between humans, wildlife and livestock, as people move into undeveloped areas. These interactions happen more frequently on the frontier of human expansion because of changes to the natural landscape and increased encounters with animals. A study published in April by researchers at Stanford University in California found that deforestation and habitat fragmentation in Uganda increased direct encounters between primates and people, as primates ventured out of the forest to raid crops and people ventured in to collect wood5.
    But a key question over the past decade has been whether the decline in biodiversity that inevitably accompanies human expansion on the rural frontier increases the pool of pathogens that can make the jump from animals to humans. Work by Jones and others6 suggests that the answer in many cases is yes, because a loss in biodiversity usually results in a few species replacing many — and these species tend to be the ones hosting pathogens that can spread to humans.
    For their latest analysis, Jones and her team compiled more than 3.2 million records from several hundred ecological studies at sites around the world, ranging from native forests to cropland to cities. They found that the populations of species known to host diseases transmissible to humans — including 143 mammals such as bats, rodents and various primates — increased as the landscape changed from natural to urban, and as biodiversity generally decreased.

    The next step for Jones’s team is to examine the likelihood of disease transmission to the human population. The group has already made this type of evaluation for Ebola virus outbreaks in Africa, creating risk maps based on development trends, the presence of probable host species, and socio-economic factors that determine the pace at which a virus might spread once it enters the human population7. The group’s risk maps accurately captured where outbreaks occurred in the Democratic Republic of the Congo (DRC) in the past few years, suggesting that it is possible to understand and project risks on the basis of relationships between factors such as land use, ecology, climate and biodiversity.
    Some researchers urge caution when communicating that biodiversity hotspots are where outbreaks are likely to occur. “My worry, frankly, is that people are going to cut down the forests more if this is where they think the next pandemic is going to come from,” says Dan Nepstad, a tropical ecologist and founder of the Earth Innovation Institute based in San Francisco, California, a non-profit organization that campaigns for sustainable development. Efforts to preserve biodiversity will only work, he says, if they address the economic and cultural factors that drive deforestation and the rural poor’s dependency on hunting and trading wild animals.
    Ibrahima Socé Fall, an epidemiologist and head of the World Health Organization’s emergency operations in Africa, agrees that understanding the ecology — as well as the social and economic trends — of the rural frontier will be crucial to projecting the risk of future disease outbreaks. “Sustainable development is crucial,” he says. “If we continue to have this level of deforestation, disorganized mining and unplanned development, we are going to have more outbreaks.”
    Coordinating efforts
    One message that the IPBES’s upcoming report is likely to deliver is that scientists and policymakers need to treat the rural frontier more holistically, addressing issues of public health, the environment and sustainable development in tandem. In the wake of the COVID-19 pandemic, many scientists and conservationists have emphasized curbing the wildlife trade — an industry worth an estimated US$20 billion annually in China, where the first coronavirus infections appeared. China has temporarily suspended its trade. But Daszak says the industry is just one piece in a larger puzzle that involves hunting, livestock, land use and ecology.

    Wildlife markets like this one in Bali, Indonesia, sustain the livelihoods of many people. But they are also under scrutiny as hotspots for pathogen transmission.Credit: Amilia Roso/The Sydney Morning Herald via Getty

    “Ecologists should be working with infectious-disease researchers, public-health workers and medics to track environmental change, assess the risk of pathogens crossing over and reduce risky human activities,” he says.
    Daszak was an author of last month’s essay in Science, which argued that governments could substantially reduce the risk of future pandemics such as COVID-19 by investing in efforts to curb deforestation and the wildlife trade, as well as in efforts to monitor, prevent and control new virus outbreaks from wildlife and livestock. The team estimated that the cost of these actions would ring in at $22 billion to $33 billion annually, including $19.4 billion for ending trade in wild meat in China — a step that not all experts think is desirable or necessary — and up to $9.6 billion to help curb tropical deforestation. The total investment would be two orders of magnitude less than the $5.6-trillion price tag estimated for the COVID-19 pandemic, the team estimates.

    Fall says the key is to align efforts by government and international agencies focused on public health, animal health, the environment and sustainable development. The latest Ebola outbreak in the DRC, which began in 2018 and ended last month, had its roots not just in disease but also in deforestation, mining, political instability and the movement of people. The goal must be to focus resources on the riskiest areas and manage interactions between people and animals, both wild and domestic, Fall says.
    With the right collaboration between human health, animal health and environmental authorities, Fall says, “you have some mechanisms for early warnings”.

    doi: 10.1038/d41586-020-02341-1

    References

    1.
    Gibb, R. et al. Nature https://doi.org/10.1038/s41586-020-2562-8 (2020).

    2.
    Dobson, A. P. et al. Science 369, 379–381 (2020).

    3.
    Jones, K. E. et al. Nature 451, 990–993 (2008).

    4.
    Smith, K. F. et al. J. R. Soc. Interface 11, 20140950 (2014).

    5.
    Bloomfield, L. S. P., McIntosh, T. L. & Lambin, E. Landscape Ecol. 35, 985–1000 (2020).

    6.
    Faust, C. L. et al. Ecol. Lett. 21, 471–483 (2018).

    7.
    Redding, D. W. et al. Nature Commun. 10, 4531 (2019).

    Download references

    Latest on:

    An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

    Related Articles More

  • in

    Satellites find penguins by following the poo

    A space-based sensor has detected new colonies of emperor penguins on Antarctic sea ice. Credit: Christopher Walton

    Ecology
    07 August 2020

    Images from space bolster the population count, but the birds remain vulnerable to climate change.

    From their vantage point high above Antarctica, sharp-eyed satellites have spotted eight previously unknown colonies of emperor penguins. The discovery boosts emperor penguin numbers by 5–10%.
    The iconic birds breed and raise their young on sea ice frozen to Antarctica’s shoreline. These habitats are threatened by climate change, so scientists have been working to get a complete census of emperor penguins (Aptenodytes forsteri) to assess how the bird’s populations might change.
    Peter Fretwell and Philip Trathan at the British Antarctic Survey in Cambridge, UK, used the European Space Agency’s Sentinel-2 satellites to search for dark smudges of guano-stained ice. They identified eight newfound penguin colonies located around the rim of the continent; one was on sea ice frozen around icebergs grounded far offshore. Using the images, the authors also pinpointed three colonies that had been reported in the 1960s and 1980s but not confirmed since.
    The findings bring the total number of emperor penguin colonies to 61. Many are in areas vulnerable to climate change. More