More stories

  • in

    Climatic windows for human migration out of Africa in the past 300,000 years

    Late Quaternary climate reconstructionsPrecipitationOur reconstructions of Late Quaternary precipitation are based on outputs from a statistical emulator of the HadCM3 general circulation model62. The emulator was developed using 72 3.75° × 2.5° resolution snapshot climate simulations of HadCM3, covering the last 120k years and in 2k year time steps from 120k to 22k years ago and 1k-year time steps from 21k years ago to the present, where each time slice represents climatic conditions averaged across a 30-year post-spin-up period28,63. The emulator is based on grid-cell-specific linear regressions between the local time series of HadCM3 climate data and four time-dependent forcings, given by the mean global atmospheric CO2 concentration and three orbital parameters: eccentricity, obliquity, and precession. The values of these four predictors are known well beyond the last 120k years; thus, applying them to the calibrated grid-cell-specific linear regressions allows for the statistical extrapolation of global climate up to 800k years into the past62. The emulated climate data have been shown to correspond closely to the original HadCM3 simulations for the last 120k years, and to match long-term empirical climate reconstructions well62.Here, we used precipitation data from the emulator, denoted ({bar{{{{bf{P}}}}}}_{{{{{rm{HadCM3}}}}}_{{{{rm{em}}}}}}(t)), of the last 300k years at 1k-year time steps, (tin {{{{bf{T}}}}}_{300k}). The data were spatially downscaled from their native 3.75° × 2.5° grid resolution, and subsequently bias-corrected, in two steps, similar to the approach described in ref. 64, whose description we follow here. Both steps use variations of the delta method65, under which a high-resolution, bias-corrected reconstruction of precipitation at sometime t is obtained by applying the difference between lower-resolution present-day simulated and high-resolution present-day observed climate—the correction term—to the simulated climate at time t. The delta method has been used to downscale and bias-correct palaeoclimate simulations before (e.g. for the WorldClim database66), and, despite its conceptual simplicity, has been shown to outperform alternative methods commonly used for downscaling and bias-correction67.A key limitation of the delta method is that it assumes the present-day correction term to be representative of past correction terms. This assumption is substantially relaxed in the dynamic delta method used in the first step of our approach to downscale ({bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}(t)) to a ~1° resolution. This method involves the use of a set of high-resolution climate simulations that were run for a smaller but climatically diverse subset of T300k. Simulations at this resolution are computationally very expensive, and therefore running substantially larger sets of simulations is not feasible; however, these selected data can be very effectively used to generate a suitable time-dependent correction term for each (tin {{{{bf{T}}}}}_{300k}). In this way, we can increase the resolution of the original climate simulations by a factor of ∼9, while simultaneously allowing for the temporal variability of the correction term. In the following, we describe the approach in detail.We used high-resolution precipitation simulations from the HadAM3H model63, generated for the last 21,000 years in 9 snapshots (2k year time intervals from 12k to 6k years ago, and 3k year time intervals otherwise) at a 1.25° × .83° grid resolution, denoted ({bar{{{{bf{P}}}}}}_{{{{rm{HadAM}}}}3{{{rm{H}}}}}(t)), where (tin {{{{bf{T}}}}}_{21k},)represents the nine time slices for which simulations are available. These data were used to downscale ({bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}(t)) to a 1.25° × 0.83° resolution by means of the multiplicative dynamic delta method, yielding$${bar{{{{bf{P}}}}}}_{ sim 1^circ }(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}^{ boxplus }(t)cdot frac{{bar{{{{bf{P}}}}}}_{{{{rm{HadAM}}}}3{{{rm{H}}}}}(hat{t})}{{bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}^{ boxplus }(hat{t})}.$$
    (1)
    The ⊞-notation indicates that the coarser-resolution data were interpolated to the grid of the higher-resolution data, for which we used an Akima cubic Hermite interpolant68, which, unlike the bilinear interpolation, is continuously differentiable but, unlike the bicubic interpolation, avoids overshoots. The time (hat{t}in {{{{bf{T}}}}}_{21k}) is chosen as the time at which climate was, in a sense specified below, close to that at time (tin {{{{bf{T}}}}}_{300k}). In contrast to the classical delta method (for which (hat{t}=0) for all (t)), this approach does not assume that the resolution correction term, ((frac{{bar{{{{bf{P}}}}}}_{{{{rm{HadAM}}}}3{{{rm{H}}}}}(hat{t})}{{bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}^{ boxplus }(hat{t})})), is constant over time. Instead, the finescale heterogeneities that are applied to the coarser-resolution ({bar{{{{bf{P}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}(t)) are chosen from the wide range of patterns simulated for the last 21k years. The strength of the approach lies in the fact that the last 21k years account for a substantial portion of the glacial-interglacial range of climatic conditions present during the whole Late Quaternary. Following ref. 64, we used global CO2, a key indicator of the global climatic state, as the metric according to which (hat{t}) is chosen; i.e. among the times for which HadAM3H simulations are available, (hat{t}) is the time at which global CO2 was closest to the respective value at the time of interest, t.In the second step of our approach, we used the classical multiplicative delta method to bias-correct and further downscale ({{{{bf{P}}}}}_{ sim 1^circ }(t)) to a hexagonal grid69 with an internode spacing of ~55 km (~0.5°),$${bar{{{{bf{P}}}}}}_{ sim 0.5^circ }(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{P}}}}}}_{ sim 1^circ }^{ boxplus }(t)cdot frac{{bar{{{{bf{P}}}}}}_{{{{rm{obs}}}}}(0)}{{bar{{{{bf{P}}}}}}_{ sim 1^circ }^{ boxplus }(0)},$$
    (2)
    where ({{{{bf{P}}}}}_{{{{rm{obs}}}}}(0)) denotes present-era (1960–1990) observed precipitation70.We reconstructed land configurations for the last 300k years using present-day elevation71 and a time series of Red Sea sea level72. For locations that are currently below sea level, the delta method does not work. For these locations, precipitation was extrapolated using a inverse distance weighting approach. With the exception of a brief window from 124–126k years ago, sea level in the past was lower than it is today; thus, present-day coastal patterns are spatially extended as coastlines move, but not removed. For all (tin {{{{bf{T}}}}}_{300k}), maps of annual precipitation ({bar{{{{bf{P}}}}}}_{ sim 0.5^circ }(t)) with the appropriate land configuration are available as Supplementary Movie 1.Based on these data representing 30-year climatological normals at 1k-year time steps between 300k years ago and the present, we generated, for each millennium, 100 maps representing 10-year average climatologies as follows. We used 3.75° × 2.5° climate simulations from the HadCM3B-M2.1 model, providing a 1000-years-long annual time series of annual precipitation for each millennium between 21k years ago and the present73. Millennia were simulated in parallel; thus, the 1000-years-long time series representing each millennium is in itself continuous, but the beginnings and ends of the time series of successive millennia generally do not coincide. For (tin {{{{bf{T}}}}}_{21k}), we denote the available 1000 successive maps of annual precipitation by ({{{{bf{P}}}}}_{{{{rm{HM}}}}}^{(1)}(t),ldots ,{{{{bf{P}}}}}_{{{{rm{HM}}}}}^{(1000)}(t)). We used these data to compute the relative deviation of the climatic average of each decade within a given millennium, and the climatic average of the 30-year period containing the specific decade as$${{{{boldsymbol{epsilon }}}}}_{HM}^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}frac{{sum }_{i=1+(d-1)cdot 10}^{dcdot 10}{{{{bf{P}}}}}_{{{{rm{HM}}}}}^{(i)}(t)}{{sum }_{n=1+(d-2)cdot 10}^{(d+1)cdot 10}{{{{bf{P}}}}}_{{{{rm{HM}}}}}^{(n)}(t)},d=1,ldots ,100$$
    (3)
    Finally, we applied these ratios of 10-year to 30-year climatic averages to the previously derived 1k-year time step climatologies to obtain, for each (tin ,{{{{bf{T}}}}}_{300k}), 100 sets of 10-year average annual precipitation,$${{{{bf{P}}}}}_{ sim 0.5^circ }^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{P}}}}}}_{ sim 0.5^circ }(t)cdot {{{{boldsymbol{epsilon }}}}}_{HM}^{(d), boxplus }(hat{t}),,d=1,ldots ,100$$
    (4)
    where, analogous to our approach in Eq. (1),(, boxplus ) denotes the interpolation to the ~55 km hexagonal grid, and where (hat{t}) is chosen as the time at which global CO2 was closest to the respective value at time t.AridityThe Köppen aridity index used here is defined as the ratio of annual precipitation (in mm) to the sum of mean annual temperature (in °C) and a constant of 33 °C (cf. Eq. (8)). This measure of aridity was found to be the most reliable one of a set of alternative indices in palaeoclimate contexts30.Decadal-scale mean annual temperature data between 300k years ago and the present were created using analogous methods to those previously applied to reconstruct precipitation. 3.75° × 2.5° resolution emulator-derived simulations of mean annual temperature of the past 300k years at 1k time steps62, denoted ({bar{{{{bf{T}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}(t)), were first downscaled by means of the additive dynamic delta method, using 1.25° × 0.83° HadAM3H simulations of mean annual temperature of the past 21k years, denoted ({bar{{{{bf{T}}}}}}_{{{{rm{HadAM}}}}3{{{rm{H}}}}}(t)), yielding, analogous to Eq. (1),$${bar{{{{bf{T}}}}}}_{ sim 1^circ }(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{T}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}^{ boxplus }(t)+left({bar{{{{bf{T}}}}}}_{{{{rm{HadAM}}}}3{{{rm{H}}}}}(hat{t})-{bar{{{{bf{T}}}}}}_{{{{rm{HadCM}}}}{3}_{{{{rm{em}}}}}}^{ boxplus }(hat{t})right).$$
    (5)
    Analogous to Eq. (2), Next, present-day observed mean annual temperature, ({bar{{{{bf{T}}}}}}_{{{{rm{obs}}}}}(0)), was used to further downscale and bias-correct the data by means of the additive delta method to obtain$${bar{{{{bf{T}}}}}}_{ sim 0.5^circ }(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{T}}}}}}_{ sim 1^circ }^{ boxplus }(t)+left({bar{{{{bf{T}}}}}}_{{{{rm{obs}}}}}(0)-{bar{{{{bf{T}}}}}}_{ sim 1^circ }^{ boxplus }(hat{t})right).$$
    (6)
    For all (tin {{{{bf{T}}}}}_{300k}), maps of mean annual temperature ({bar{{{{bf{T}}}}}}_{ sim 0.5^circ }(t)) with the appropriate land configuration are available as Supplementary Movie 1.Finally, we incorporated HadCM3B-M2 simulations of mean annual temperature of the past 21k years, ({{{{bf{T}}}}}_{{{{rm{HM}}}}}^{(1)}(t),ldots ,{{{{bf{T}}}}}_{{{{rm{HM}}}}}^{(1000)}(t)) for (tin {{{{bf{T}}}}}_{21k}), to obtain 10-year average mean annual temperature,$$begin{array}{c}{{{{bf{T}}}}}_{ sim 0.5^circ }^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}{bar{{{{bf{T}}}}}}_{ sim 0.5^circ }(t)+{left(mathop{sum }limits_{i=1+(d-1)cdot 10}^{dcdot 10}{bar{{{{bf{T}}}}}}_{{{{rm{HM}}}}}^{(i)}(t)-mathop{sum }limits_{n=1+(d-2)cdot 10}^{(d+1)cdot 10}{bar{{{{bf{T}}}}}}_{{{{rm{HM}}}}}^{(n)}(t)right)}^{ boxplus },\ d=1,ldots ,100end{array}$$
    (7)
    Based on these data, the Köppen aridity index at the same spatial and temporal resolution is calculated as$${{{{bf{A}}}}}_{ sim 0.5^circ }^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}frac{{{{{bf{P}}}}}_{ sim 0.5^circ }^{(d)}(t)}{{{{{bf{T}}}}}_{ sim 0.5^circ }^{(d)}(t)+33}.$$
    (8)
    Comparison with empirical proxiesLong-term proxy records
    Long-term proxy records allow us to assess whether simulations capture key qualitative dynamics observed in the empirical data. The lack of direct long-term time series reconstructions of annual precipitation and mean annual temperature makes it necessary to use proxies related to these two climate variables. Proxies providing temporal coverage beyond the last glacial maximum are not only extremely sparse in North Africa and Southwest Asia, but even the few records that exist are affected by environmental factors other than the specific climate variables considered here. For example, reconstructions of past wetness and aridity use proxies that reflect not only rainfall conditions but also the interaction of precipitation with other local and non-local hydro-climatic variables, e.g. river discharge or hydrological catchment across a larger area. Here, we have not attempted to correct for such processes, but assumed that the simulated climate at the site where the empirical record was taken provide a suitable approximation of the potentially broader climatic conditions relevant for the proxy data. Realistic climate simulations would therefore be expected to match major qualitative trends of the empirical records, rather than exhibit a perfect correlation with the data. We compared our precipitation simulations against three long-term humidity-related empirical proxies (Fig. 4a). Proxy 174 provides a time series of Dead Sea lake levels, for which wet and dry periods are associated with high-stand and low-stand conditions, respectively. Proxy 219 from the southern tip of the Arabian Peninsula was obtained from a marine sediment core that allows for reconstructing past changes in aridity over land from the stable hydrogen isotopic composition of leaf waxes (δDwax). Proxy 318 is an XRF-derived humidity index from a core near the Northwest African coast. Temperature simulations were compared against two long-term records of δ18O, which varies over time as a result of temperature fluctuations (in addition to other factors), from the Peqiin and Soreq caves in Northern Israel75 (Fig. 4e). Overall, the simulated data capture key phases observed in the empirical records well for both precipitation (Fig. 4b–d) and temperature proxies (Fig. 4f–h).Fig. 4: Comparison of our data to long-term proxy records.a Geographical locations of empirical proxies on a map of present-day annual precipitation. b–d Comparisons of simulated annual precipitation against the three wetness proxies. e Geographical locations of empirical proxies on a map of present-day mean annual temperature. f, g Comparisons of simulated mean annual temperature against the two δ18O records. Black lines represent the simulated climatological normals at 1k-year intervals (Eqs. (2) and (6)), grey shades represent the 10th and 90th percentile of the decadal simulations (n = 100; Eqs. (4) and (7)).Full size image

    Pollen-based reconstructions
    Pollen records used to empirically reconstruct past climate do not reach as far back in time as the above-described proxy records and are not available at the same temporal resolution; however, in contrast to those proxies, they can be used to quantitatively estimate local annual precipitation and mean annual temperature directly. Here, we used the dataset of pollen-based reconstructions of precipitation and temperature for the mid-Holocene (6k years ago) and the last glacial maximum (21k years ago)76 (Fig. 5a). Our precipitation and temperature data are overall in good agreement with the empirical reconstructions (Fig. 5b–e). During the mid-Holocene, our simulations suggest slightly less precipitation at low levels than most of the empirical records (Fig. 5d), while our data match the empirical reconstruction available from a very arid location during the last glacial maximum very well (Fig. 5e).Fig. 5: Comparison of our data to pollen-based climate reconstructions from the mid-Holocene and the last interglacial period.a Geographical locations and timings of pollen records. b–e Comparisons of our data against empirical reconstructions. Vertical centre measures and error bars represent the empirical reconstructed values and their uncertainties, respectively; horizontal centre measures and error bars represent simulated climatological normals at 1k-year intervals (Eqs. (2) and (6)) and the 10th and 90th percentile of the simulated decadal data (n = 100; Eqs. (4) and (7)), respectively.Full size image

    Interglacial palaeolakes on the Arabian Peninsula
    Finally, we plotted time series of our precipitation simulations in three locations in which palaeolakes have been dated to the last interglacial period, following the approach in ref. 24, in which the authors tested whether their climate simulations predicted higher rainfall during the last interglacial period than at present at palaeolake sites on the Arabian Peninsula. Figure 6 shows the locations of three palaeolakes in the northeast (western Nefud near Taymal; proxy 1), the centre (at Khujaymah; proxy 2), and the southwest (at Saiwan; proxy 3) of the peninsula24 (described in detail in refs. 23,77), and our precipitation data in these locations. In two out of the three locations, our data predict that more rainfall occurred at the estimated timings of the palaeolakes than at any point in time since; in the third location, slightly more rainfall than during the dated time interval is simulated only for a period around 8k years ago.Fig. 6: Comparison of our data against the dates of three palaeolakes on the Arabian peninusla.a Geographical locations of the lakes. b–d Time series of our precipitation data. Black lines represent the simulated climatological normals at 1k-year intervals (Eqs. (2) and (6)), grey shades represent the 10th and 90th percentile of the decadal simulations (n = 100; Eq. (4)). Horizontal error bars represent the estimated dates of the lakes24.Full size image
    Determining the minimum precipitation and aridity tolerance required for out-of-Africa exitsWe denote by ({{{bf{X}}}}={({lambda }_{1},{phi }_{1}),({lambda }_{2},{phi }_{2}),ldots },)the set of longitude and latitude coordinates of the hexagonal grid with an internode spacing of ~55 km (~0.5°)69 that are contained in the longitude window [15°E, 70°E] and the latitude window [5°N, 43°N] (shown in Fig. 3). We denote by ({{{bf{E}}}}) the set of the present-day elevation values of the coordinates in ({{{bf{X}}}}) (in meters)78, i.e. ({{{bf{E}}}}({x}_{i})) is a positive number in a point ({x}_{i}=({lambda }_{i},{phi }_{i})) if ({x}_{i}) is currently above sea level, and negative if ({x}_{i}) is currently below sea level. We denote by (s(t)) the sea level (in meters) at the time (tin {{{{bf{T}}}}}_{300k}) (where ({{{{bf{T}}}}}_{300k}) represents the last 300k years in 1k time steps), for which we used a long-term reconstruction of Red Sea sea level72. In particular, we have (s(0)=0) at present day. For each millennium (tin {{{{bf{T}}}}}_{300k}), we denote by (bar{{{{bf{X}}}}}(t)) the subset of points in (X) that are above sea level:$$bar{{{{bf{X}}}}}(t)mathop{=}limits^{{{{rm{def}}}}}{xin {{{bf{X}}}}:{{{bf{E}}}}(x), > , s(t)}$$
    (9)
    Based on the precipitation map ({{{{bf{P}}}}}_{ sim 0.5^circ }^{(d)}(t)) for a decade (d=1,ldots ,100) in millennium (t) (Eq. (4)), and a given precipitation threshold value (p) (in mm year−1), we denote by ({mathop{{{{bf{X}}}}}limits^{=}}_{p}^{(d)}(t)) the subset of (bar{{{{bf{X}}}}}(t)) that would be suitable grid cells for humans assuming that they cannot survive in areas where precipitation levels are below (p):$${mathop{{{{bf{X}}}}}limits^{=}}_{p}^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}left{xin bar{{{{bf{X}}}}}(t):{{{{bf{P}}}}}_{ sim 0.5^circ }^{(d)}(t)ge pright}$$
    (10)
    We then determined whether there was a connected path in ({mathop{{{{bf{X}}}}}limits^{=}}_{p}^{(d)}(t)) between an initial point, for which we used ({x}_{{{{rm{start}}}}}=(32.6^circ {{{rm{E}}}},10.2^circ {{{rm{N}}}})), and any point in a set of coordinates outside of Africa, defined as ({{{{bf{X}}}}}_{{{{rm{end}}}}}mathop{=}limits^{{{{rm{def}}}}}{(lambda ,phi )in {{{bf{X}}}}:lambda, > , 65^circ {{{rm{E}}}},{{{rm{or}}}},phi , > , 37^circ N}). This was defined to be the case if there was a finite sequence$${x}_{{{{rm{start}}}}}to {x}_{1}to {x}_{2}to ldots to {x}_{n}in {{{{bf{X}}}}}_{{{{rm{end}}}}}$$
    (11)
    of points ({x}_{i}in {mathop{{{{bf{X}}}}}limits^{=}}_{p}^{(d)}(t)) such that the distance between any two successive points ({x}_{i}) and ({x}_{i+1}) was less or equal to the maximum internode spacing of the grid (X). Based on this approach, the critical precipitation threshold below which no connected path exists for the precipitation map ({{{{bf{P}}}}}_{ sim 0.5^circ }^{(d)}(t)) was determined using the following bisection method. Beginning with ({hat{p}}_{0}=1000) mm y−1 and ({check{p}}_{0}=0) mm y−1, for which a connected path between ({x}_{{{{rm{start}}}}}) and ({{{{bf{X}}}}}_{{{{rm{end}}}}}) exists, respectively, for all and for no (t) and (d), the values ({hat{p}}_{k}) and ({check{p}}_{k}) were iteratively defined as$$ , left.begin{array}{c}{check{p}}_{k+1}mathop{=}limits^{{{{rm{def}}}}}frac{{{hat{p}}_{k}+{check{p}}_{k}}}{2}\ {hat{p}}_{k+1}mathop{=}limits^{{{{rm{def}}}}}{hat{p}}_{k}hfillend{array}right},{{{rm{if}}}},{{{rm{a}}}},{{{rm{connected}}}},{{{rm{path}}}},{{{rm{exists}}}},{{{rm{for}}}},p=frac{{{hat{p}}_{k}+{check{p}}_{k}}}{2}\ , left.begin{array}{c}{check{p}}_{k+1}mathop{=}limits^{{{{rm{def}}}}}{check{p}}_{k}hfill\ {hat{p}}_{k+1}mathop{=}limits^{{{{rm{def}}}}}frac{{{hat{p}}_{k}+{check{p}}_{k}}}{2}end{array}right}, {{{rm{else}}}}$$
    (12)
    For all (k), the sought critical precipitation threshold, denoted ({p}_{{{{rm{crit}}}}}^{(d)}(t)), is bounded above by ({hat{p}}_{k}) and bounded below by ({check{p}}_{k}). For (kto infty ), both values converge to ({p}_{{{{rm{crit}}}}}^{(d)}(t)). Here, we defined$${p}_{{{{rm{crit}}}}}^{(d)}(t)mathop{=}limits^{{{{rm{def}}}}}frac{,{hat{p}}_{10}+{check{p}}_{10}}{2},$$
    (13)
    which lies within 1 mm y−1 of the true limit value.To specifically determine the precipitation tolerance required for a northern (Fig. 1a) or southern (Fig. 1b) exit, we rendered the passage of the respective other route impassable by removing appropriate cells from the grid. When investigating the southern route, we additionally assumed that no sea level and precipitation constraints applied within a ~40 km radius around the centre of the Bab al-Mandab strait.For aridity, the procedure is identical, with the exception that ({mathop{{{{bf{X}}}}}limits^{=}}_{p}^{(d)}(t)) is defined based on the relevant aridity map, ({{{{bf{A}}}}}_{ sim 0.5^circ }^{(d)}(t)), and the value 4.0 is used for the initial upper threshold (denoted ({hat{p}}_{0}) above).Width of the Strait of Bab al-MandabSimilar to ref. 52, we reconstructed the minimum distance required to cover on water in order to reach the Arabian peninsula (present-day west coast of Yemen) from Africa (present-day Djibouti and southeast Eritrea). We used a 0.0083° (~1 km at the equator) map of elevation and bathymetry78 and a time series of Red Sea sea level72 to reconstruct very-high-resolution land masks for the last 300k years. For each point in time, we determined the set of connected land masses, and the distances between the closest points of any two land masses. The result can be graph-theoretically represented by a complete graph whose nodes represent connected land masses and whose edge weights correspond to the minimum distances between land masses. The path involving the minimum continuous distance on water was then determined by solving the minmax path problem whose solution is the path between the two nodes representing Africa and the Arabian Peninsula that minimises the maximum weight of any of its edges (Fig. 1b grey shades).Analyses were conducted using Matlab R2019a79.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

  • in

    National climate and biodiversity strategies are hamstrung by a lack of maps

    1.Khan, M. & Schmidt-Traub, G. Use of Spatial Information in National Climate Strategies. An Analysis of Nationally Determined Contributions (NDCs) (SDSN, 2020); https://resources.unsdsn.org/use-of-spatial-information-in-national-climate-strategies2.Cadena, M. et al. Nature is counting on us: Mapping Progress to Achieve the Aichi Biodiversity Targets. NBSAP Forum https://go.nature.com/3B9vo5Z (2019).3.Díaz, S. et al. Science 366, eaax3100 (2019).Article 

    Google Scholar 
    4.First Draft of the Post-2020 Global Biodiversity Framework CBD/WG2020/3/3 (CBD, 2021); https://www.cbd.int/doc/c/abb5/591f/2e46096d3f0330b08ce87a45/wg2020-03-03-en.pdf5.Clark, M. A. et al. Science 370, 705–708 (2020).CAS 
    Article 

    Google Scholar 
    6.Soterroni, A. C. et al. Env. Res. Lett. 13, 074021 (2018).Article 

    Google Scholar 
    7.Wallbott, L., Siciliano, G. & Lederer, M. Ecol. Soc. 24, 24 (2019).Article 

    Google Scholar 
    8.Brauman, K. A. et al. Global trends in nature’s contributions to people. Proc. Natl Acad. Sci. USA 117, 32799–32805 (2020).CAS 
    Article 

    Google Scholar 
    9.Jung, M. et al. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-021-01528-7 (2021).10.Sala, E. et al. Nature 592, 397–402 (2021).CAS 
    Article 

    Google Scholar 
    11.Global Biodiversity Outlook 5 (Secretariat of the Convention on Biological Diversity, 2020); https://go.nature.com/3z6jZls12.Schmidt-Traub, G. et al. Natl Sci. Rev. https://doi.org/gnr8 (2020).13.Schmidt-Traub, G., Adams, J. & Zhu, C. The EU and China must cooperate to green commodity supply chains. China Dialogue https://go.nature.com/3rfOpPN (2020).14.G7 2030 Nature Compact. G7 https://go.nature.com/3ilGLzj (2021). More

  • in

    Occurrence of Mycoplasma spp. in wild birds: phylogenetic analysis and potential factors affecting distribution

    1.Luttrell, M. P. & Fischer, J. R. Mycoplasmosis. In Infectious Diseases of Wild Birds (eds Thomas, N. J. et al.) 317–331 (Blackwell Publishing Ltd, 2007).Chapter 

    Google Scholar 
    2.Luttrell, M. P., Kleven, S. H. & Mahnke, G. M. Mycoplasma synoviae in a released pen-raised wild turkey. Avian Dis. 36, 169–171 (1992).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Forrester, C. A. et al. Mycoplasma gallisepticum in pheasants and the efficacy of tylvalosin to treat the disease. Avian Pathol. 40, 581–587 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Welchman, D. D. E. B., Bradbury, J. M., Cavanagh, D. & Aebischer, N. J. Infectious agents associated with respiratory disease in pheasants. Vet. Rec. 150, 658–664 (2002).Article 

    Google Scholar 
    5.de Welchman, D. B. et al. Demonstration of Ornithobacterium rhinotracheale in pheasants (Phasianus colchicus) with pneumonia and airsacculitis. Avian Pathol. 42, 171–178 (2013).Article 

    Google Scholar 
    6.Cookson, K. C. & Shivaprasad, H. L. Mycoplasma gallisepticum infection in chukar partridges, pheasants, and peafowl. Avian Dis. 38, 914–921 (2016).Article 

    Google Scholar 
    7.Bencina, D., Mrzel, O., Rois Zorman, O., Bidovec, A. & Dovc, A. Characterisation of Mycoplasma gallisepticum strains involved in respiratory disease in pheasants and peafowl. Vet. Rec. 152, 230–234 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Bradbury, J. M., Yavari, C. A. & Dare, C. M. Mycoplasmas and respiratory disease in pheasants and partridges. Avian Pathol. 30, 391–396 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Bradbury, J. M., Yavari, C. A. & Dare, C. M. Detection of Mycoplasma synoviae in clinically normal pheasants. Vet. Rec. 148, 72–74 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Wrobel, E. R., Wilcoxen, T. E., Nuzzo, J. T. & Seitz, J. Seroprevalence of avian pox and Mycoplasma gallisepticum in raptors in central Illinois. J. Raptor Res. 50, 289–294 (2016).Article 

    Google Scholar 
    11.Sawicka, A., Durkalec, M., Tomczyk, G. & Kursa, O. Occurrence of Mycoplasma gallisepticum in wild birds: A systematic review and meta-analysis. PLoS ONE 15, e0231545 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Hartup, B. K., Kollias, G. V. & Ley, D. H. Mycoplasmal conjunctivitis in songbirds from New York. J. Wildl. Dis. 36, 257–264 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Ley, D. H., Berkhoff, J. E. & Mclaren, J. M. Mycoplasma gallisepticum isolated from house finches (Carpodacus mexicanus) with conjunctivitis. Avian Dis. 40, 480–483 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Fischer, J. R., Stallknecht, D. E., Luttrell, M. P., Dhondt, A. A. & Converse, K. A. Mycoplasmal conjunctivitis in wild songbirds: The spread of a new contagious disease in a mobile host population. Emerg. Infect. Dis. 3, 69–72 (1997).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Farmer, K. L., Hill, G. E. & Roberts, S. R. Susceptibility of wild songbirds to the house finch strain of Mycoplasma gallisepticum. J. Wildl. Dis. 41, 317–325 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Dhondt, A. A., Dhondt, K. V., Hochachka, W. M. & Schat, K. A. Can American goldfinches function as reservoirs for Mycoplasma gallisepticum? J. Wildl. Dis. 49, 49–54 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Fry, M. A. Effects of Mycoplasma gallisepticum on experimentally infected Eastern bluebirds (Sialia sialis). Honors Theses 1116 (2019). https://egrove.olemiss.edu/hon_thesis/1116. (Accessed 10 November 2020).18.Balenger, S. L. Costs associated with Mycoplasma gallisepticum infection of Eastern bluebirds (Sialia sialis). Integr. Comp. Biol. 59, e1–e260 (2019).Article 

    Google Scholar 
    19.Forsyth, M. H. et al. Mycoplasma sturni sp. nov., from the conjunctiva of a European starling (Sturnus vulgaris). Int. J. Syst. Bacteriol. 46, 716–719 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Ley, D. H., Geary, S. J., Edward Berkhoff, J., McLaren, J. M. & Levisohn, S. Mycoplasma sturni from blue jays and northern mockingbirds with conjunctivitis in Florida. J. Wildl. Dis. 34, 403–406 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Ley, D. H., Anderson, N., Dhondt, K. V. & Dhondt, A. A. Mycoplasma sturni from a California house finch with conjunctivitis did not cause disease in experimentally infected house finches. J. Wildl. Dis. 46, 994–999 (2010).PubMed 
    Article 

    Google Scholar 
    22.Ley, D. H., Moresco, A. & Frasca, S. Conjunctivitis, rhinitis, and sinusitis in cliff swallows (Petrochelidon pyrrhonota) found in association with Mycoplasma sturni infection and cryptosporidiosis. Avian Pathol. 41, 395–401 (2012).PubMed 
    Article 

    Google Scholar 
    23.Wellehan, J. F. X. et al. Mycoplasmosis in captive crows and robins from Minnesota. J. Wildl. Dis. 37, 547–555 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Poveda, J. B., Giebel, J., Flossdorf, J., Meier, J. & Kirchhoff, H. Mycoplasma buteonis sp. nov., Mycoplasma falconis sp. nov., and Mycoplasma gypis sp. nov., three species from birds of prey. Int. J. Syst. Bacteriol. 44, 94–98 (1994).Article 

    Google Scholar 
    25.Ruder, M. G., Feldman, S. H., Wünschmann, A. & Mcruer, L. Association of Mycoplasma corogypsi and polyarthritis in a black vulture (Coragyps atratus) in Virginia. J. Wildl. Dis. 45, 808–816 (2009).PubMed 
    Article 

    Google Scholar 
    26.Van Wettere, A. J., Ley, D. H., Scott, D. E., Buckanoff, H. D. & Degernes, L. A. Mycoplasma corogypsi associated polyarthritis and tenosynovitis in black vultures (Coragyps atratus). Vet. Pathol. 50, 291–298 (2013).PubMed 
    Article 

    Google Scholar 
    27.Erdélyi, K., Tenk, M. & Dán, Á. Mycoplasmosis associated perosis type skeletal deformity in a saker falcon nestling in Hungary. J. Wildl. Dis. 35, 586–590 (1999).PubMed 
    Article 

    Google Scholar 
    28.Fischer, L. et al. Description, occurrence and significance of Mycoplasma seminis sp. nov. isolated from semen of a gyrfalcon (Falco rusticolus). Vet. Microbiol. 247, 108789 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Ziegler, L. et al. Mycoplasma hafezii sp. nov., isolated from the trachea of a peregrine falcon (Falco peregrinus). Int. J. Syst. Evol. Microbiol. 69, 773–777 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Lecis, R. et al. Identification and characterization of novel Mycoplasma spp. belonging to the hominis group from griffon vultures. Res. Vet. Sci. 89, 58–64 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Lierz, M., Hagen, N., Hernadez-Divers, S. J. & Hafez, H. M. Occurrence of mycoplasmas in freeranging birds of prey in Germany. J. Wildl. Dis. 44, 845–850 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Volokhov, D. V. et al. Mycoplasma anserisalpingitidis sp. nov., isolated from European domestic geese (Anser anser domesticus) with reproductive pathology. Int. J. Syst. Evol. Microbiol. 70, 2369–2381 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Dobos-Kovács, M., Varga, Z., Czifra, G. & Stipkovits, L. Salpingitis in geese associated with Mycoplasma sp. strain 1220. Avian Pathol. 38, 239–243 (2009).PubMed 
    Article 

    Google Scholar 
    34.Gyuranecz, M. et al. Isolation of Mycoplasma anserisalpingitidis from swan goose (Anser cygnoides) in China. BMC Vet. Res. 16, 1–7 (2020).Article 
    CAS 

    Google Scholar 
    35.Kovács, Á. B. et al. The core genome multi-locus sequence typing of Mycoplasma anserisalpingitidis. BMC Genomics 21, 403 (2020).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    36.Carnaccini, S. et al. A novel Mycoplasma sp. associated with phallus disease in goose breeders: Pathological and bacteriological findings. Avian Dis. 60, 437–443 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Landman, W. J. M. Is Mycoplasma synoviae outrunning Mycoplasma gallisepticum? A viewpoint from the Netherlands. Avian Pathol. 43, 2–8 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Kursa, O., Tomczyk, G. & Sawicka, A. Prevalence and phylogenetic analysis of Mycoplasma synoviae strains isolated from Polish chicken layer flocks. J. Vet. Res. 63, 41–49 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Catania, S. et al. Two strains of Mycoplasma synoviae from chicken flocks on the same layer farm differ in their ability to produce eggshell apex abnormality. Vet. Microbiol. 193, 60–66 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Kang, M. S., Gazdzinski, P. & Kleven, S. H. Virulence of recent isolates of Mycoplasma synoviae in turkeys. Avian Dis. 46, 102–110 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Lin, M. Y. & Kleven, S. H. Pathogenicity of two strains of Mycoplasma gallisepticum in turkeys. Avian Dis. 26, 360–364 (1982).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Kleven, S. H. Mycoplasmas in the etiology of multifactorial respiratory disease. Poult. Sci. 77, 1146–1149 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Stallknecht, D. E., Johnson, D. C., Emory, W. H. & Kleven, S. H. Wildlife surveillance during a Mycoplasma gallisepticum epornitic in domestic turkeys. Avian Dis. 26, 883–890 (1982).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Gharaibeh, S. & Hailat, A. Mycoplasma gallisepticum experimental infection and tissue distribution in chickens, sparrows and pigeons. Avian Pathol. 40, 349–354 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Benčina, D., Dorrer, D. & Tadina, T. Mycoplasma species isolated from six avian species. Avian Pathol. 16, 653–664 (1987).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Tsai, H. J. & Lee, C. Y. Serological survey of racing pigeons for selected pathogens in Taiwan. Acta Vet. Hung. 54, 179–189 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Michiels, T. et al. Prevalence of Mycoplasma gallisepticum and Mycoplasma synoviae in commercial poultry, racing pigeons and wild birds in Belgium. Avian Pathol. 45, 244–252 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.May, M., Balish, M. & Blanchard, A. The Order Mycoplasmatales. In The Prokaryotes (eds Rosenberg, E. et al.) 515–550 (Springer, 2004).
    Google Scholar 
    49.Lierz, M., Obon, E., Schink, B., Carbonell, F. & Hafez, H. M. The role of Mycoplasmas in a conservation project of the lesser kestrel (Falco naumanni). Avian Dis. 52, 641–645 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Bolske, G. & Morner, T. Isolation of a Mycoplasma sp. from three buzzards (Buteo spp.). Avian Dis. 26, 406–411 (1982).CAS 
    PubMed 
    Article 

    Google Scholar 
    51.Kempf, I., Chastel, C., Ferris, S., Gesbert, F. & Blanchard, A. Isolation and characterisation of a mycoplasma from a kittiwake (Rissa tridactyla). Vet. Rec. https://doi.org/10.1136/vr.146.6.168 (2000).Article 
    PubMed 

    Google Scholar 
    52.Cockerham, S. et al. Microbial ecology of the western gull (Larus occidentalis). Microb. Ecol. 78, 665–676 (2019).PubMed 
    Article 

    Google Scholar 
    53.Liao, F. et al. Characteristics of microbial communities and intestinal pathogenic bacteria for migrated Larus ridibundus in southwest China. Microbiology https://doi.org/10.1002/mbo3.693 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Shimizu, T., Ern, H. & Nagatomo, H. Isolation and characterization of Mycoplasma columbinum and Mycoplasma columborale, two new species from pigeons. Int. J. Syst. Bacteriol. 28, 538–546 (1978).Article 

    Google Scholar 
    55.Nagatomo, H., Kato, H., Shimizu, T. & Katayama, B. Isolation of mycoplasmas from fantail pigeons. J. Vet. Med. Sci. 59, 461–462 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Sawicka, A., Tomczyk, G., Kursa, O. & Stenzel, T. Occurrence and relevance of Mycoplasma spp. in racing and ornamental pigeons in Poland. Avian Dis. 63, 468 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Möller Palau-Ribes, F. et al. Description and prevalence of Mycoplasma ciconiae sp. nov. isolated from white stork nestlings (Ciconia ciconia). Int. J. Syst. Evol. Microbiol. 66, 3477–3484 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    58.Goldberg, D. R. et al. The occurrence of mycoplasmas in selected wild North American waterfowl. J. Wildl. Dis. 31, 364–371 (1995).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Bradbury, J. M. et al. Isolation of mycoplasma cloacale from a number of different avian hosts in great Britain and France. Avian Pathol. 16, 183–186 (1987).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Poveda, J. B. et al. An epizootiological study of avian mycoplasmas in Southern Spain. Avian Pathol. 19, 627–633 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Brown, D. R., Whitcomb, R. F. & Bradbury, J. M. Revised minimal standards for description of new species of the class Mollicutes (division Tenericutes). Int. J. Syst. Evol. Microbiol. 57, 2703–2719 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Volokhov, D. V., Simonyan, V., Davidson, M. K. & Chizhikov, V. E. RNA polymerase beta subunit (rpoB) gene and the 16S–23S rRNA intergenic transcribed spacer region (ITS) as complementary molecular markers in addition to the 16S rRNA gene for phylogenetic analysis and identification of the species of the family Mycoplasmataceae. Mol. Phylogenet. Evol. 62, 515–528 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Hartup, B. K. & Kollias, G. V. Field investigation of Mycoplasma gallisepticum infections in house finch (Carpodacus mexicanus) eggs and nestlings. Avian Dis. 43, 572 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Paessler, M. et al. Disseminated Mycoplasma orale infection in a patient with common variable immunodeficiency syndrome. Diagn. Microbiol. Infect. Dis. 44, 201–204 (2002).PubMed 
    Article 

    Google Scholar 
    65.Nikfarjam, L. & Farzaneh, P. Prevention and detection of Mycoplasma contamination in cell culture. Cell J. 13, 203–212 (2012).PubMed 

    Google Scholar 
    66.Trinh, P., Zaneveld, J. R., Safranek, S. & Rabinowitz, P. M. One health relationships between human, animal, and environmental microbiomes: A mini-review. Front. Public Health 6, 1–9 (2018).Article 

    Google Scholar 
    67.Baron, S. A., Diene, S. M. & Rolain, J. Human microbiomes and antibiotic resistance. Hum. Microbiome J. 10, 43–52 (2018).Article 

    Google Scholar 
    68.Diaz-torres, M. L. et al. Determining the antibiotic resistance potential of the indigenous oral microbiota of humans using a metagenomic approach. FEMS Microbiol. Lett. 258, 257–262 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Sommer, M. O. A., Dantas, G. & Church, G. M. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325, 1128–1131 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Atterby, C. et al. Increased prevalence of antibiotic-resistant E. coli in gulls sampled in Southcentral Alaska is associated with urban environments. Infect. Ecol. Epidemiol. 6, 32334 (2016).PubMed 

    Google Scholar 
    71.Allen, H. K., Donato, J., Wang, H. H. & Cloud-hansen, K. A. Call of the wild: Antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251–259 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Wang, J. et al. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zool. Res. 38, 55–80 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Brittingham, M. C., Temple, S. A. & Duncan, R. M. A survey of the prevalence of selected bacteria in wild birds. J. Wildl. Dis. 24, 299–307 (1988).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Škaraban, J., Matjašič, T., Janžekovič, F., Wilharm, G. & Trček, J. Cultivable bacterial microbiota from choanae of free-living birds captured in Slovenia. Folia Biol. Geol. 58, 105 (2017).Article 

    Google Scholar 
    75.Stenkat, J., Krautwald-Junghanns, E., Schmitz Ornes, A., Eilers, A. & Schmidt, V. Aerobic cloacal and pharyngeal bacterial flora in six species of free-living birds. J. Appl. Microbiol. https://doi.org/10.1111/jam.12636 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Ferguson-Noel, N., Armour, N. K., Noormohammadi, A. H., El-Gazzar, M. & Bradbury, J. M. Mycoplasmosis. In Diseases of Poultry (ed. Swayne, D. E.) (Wiley, 2020).
    Google Scholar 
    77.Ely, C. R. et al. Circumpolar variation in morphological characteristics of greater white-fronted geese Anser albifrons. Bird Study 52, 104–119 (2005).Article 

    Google Scholar 
    78.Deng, X. et al. Spring migration duration exceeds that of autumn migration in far east asian greater white-fronted geese (Anser albifrons). Avian Res. 10, 1–11 (2019).Article 

    Google Scholar 
    79.Kölzsch, A. et al. Towards a new understanding of migration timing : slower spring than autumn migration in geese refl ects different decision rules for stopover use and departure. Oikos https://doi.org/10.1111/oik.03121 (2016).Article 

    Google Scholar 
    80.Gonzalez, L. M. Origin and formation of the Spanish imperial eagle (Aquila adalberti). J. Ornithol. 149, 151–159 (2008).Article 

    Google Scholar 
    81.Shamoun-Baranes, J. et al. The effect of wind, season and latitude on the migration speed of white storks Ciconia ciconia, along the eastern migration route. J. Avian Biol. 34, 97–104 (2003).Article 

    Google Scholar 
    82.Birds of the World. Cornell Laboratory of Ornithology (2020). https://birdsoftheworld.org/bow/home. (Accessed 17 August 2020).83.Lierz, M. et al. Prevalence of mycoplasmas in eggs from birds of prey using culture and a genus-specific mycoplasma polymerase chain reaction. Avian Pathol. 36, 145–150 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Raviv, Z. & Kleven, S. H. The development of diagnostic real-time Taqman PCRs for the four pathogenic avian mycoplasmas. Avian Dis. 53, 103–107 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    85.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Mangiafico, S. rcompanion: Functions to support extension education program evaluation. R package version 2.3.26. (2020).87.Wickham, H., Romain, F., Lionel, H. & Müller, K. dplyr: A grammar of data manipulation. R package version 0.8.1. (2019).88.Wickham, H. ggplot2 Vol. 35 (Springer, 2016).MATH 
    Book 

    Google Scholar 
    89.R Core Team. R: A Language and Environment for Statistical Computing. Version 4.0.4. (Foundation for Statistical Computing, 2021). https://www.r-project.org/. (Accessed 20 October 2020).90.Fair, J. M. et al. (eds) Guidelines to the Use of Wild Birds in Research 3rd edn. (The Ornithological Council, 2010).
    Google Scholar  More

  • in

    Conservation needs to break free from global priority mapping

    1.Evans, M. Environ. Conserv. https://doi.org/10.1017/S0376892921000114 (2021).2.Brooks, T. M. et al. Science 313, 58–61 (2006).CAS 
    Article 

    Google Scholar 
    3.Margules, C. R. & Pressey, R. L. Nature 405, 243–253 (2000).CAS 
    Article 

    Google Scholar 
    4.Myers, N. Bioscience 53, 916–917 (2003).Article 

    Google Scholar 
    5.Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Nature 403, 853–858 (2000).CAS 
    Article 

    Google Scholar 
    6.Hulme, M. Glob. Environ. Change 20, 558–564 (2010).Article 

    Google Scholar 
    7.Kullberg, P. & Moilanen, A. Nat. Conserv. 12, 3–10 (2014).Article 

    Google Scholar 
    8.McIntosh, E. J., Pressey, R. L., Lloyd, S., Smith, R. J. & Grenyer, R. Annu. Rev. Environ. Resour. 42, 677–697 (2017).Article 

    Google Scholar 
    9.Turnhout, E., Dewulf, A. & Hulme, M. Curr. Opin. Environ. Sustain. 18, 65–72 (2016).Article 

    Google Scholar 
    10.Evans, M. C., Davila, F., Toomey, A. & Wyborn, C. Nat. Ecol. Evol. 1, 1588 (2017).Article 

    Google Scholar 
    11.Halpern, B. S., Regan, H. M., Possingham, H. P. & McCarthy, M. A. Ecol. Lett. 9, 2–11 (2006).Article 

    Google Scholar 
    12.Mokany, K. et al. Proc. Natl Acad. Sci. USA 117, 9906–9911 (2020).CAS 
    Article 

    Google Scholar 
    13.Moffette, F., Alix-Garcia, J., Shea, K. & Pickens, A. H. Nat. Clim. Change 11, 172–178 (2021).Article 

    Google Scholar 
    14.zu Ermgassen, E. K. H. J. et al. Environ. Res. Lett. 15, 035003 (2020).Article 

    Google Scholar 
    15.Schmidt-Traub, G. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-021-01533-w (2021).16.Obermeister, N. Sustain. Sci. 14, 843–856 (2019).Article 

    Google Scholar 
    17.Sinclair, S. P. et al. Conserv. Lett. 11, e12459 (2018).Article 

    Google Scholar 
    18.Mammides, C. et al. Biol. Conserv. 198, 78–83 (2016).Article 

    Google Scholar 
    19.Turnhout, E. & Boonman-Berson, S. Ecol. Soc. 16, 35 (2011).Article 

    Google Scholar 
    20.Malavasi, M. Biol. Conserv. 252, 108843 (2020).Article 

    Google Scholar 
    21.Lahsen, M. & Turnhout, E. Environ. Res. Lett. 16, 025008 (2021).Article 

    Google Scholar 
    22.Barnes, M. D., Glew, L., Wyborn, C. & Craigie, I. D. Nat. Ecol. Evol. 2, 759–762 (2018).Article 

    Google Scholar 
    23.Popkin, G. Science https://doi.org/gpzx (24 October 2019).24.Tengö, M. et al. Curr. Opin. Environ. Sustain. 26–27, 17–25 (2017).Article 

    Google Scholar 
    25.Temper, L., del Bene, D. & Martinez-Alier, J. J. Political Ecol. 22, 255–278 (2015).
    Google Scholar  More

  • in

    The Chinese pond mussel Sinanodonta woodiana demographically outperforms European native mussels

    This study contributes to the understanding of the population dynamics of S. woodiana and its native counterparts during the early stages of invasion. It documents a self-sustaining population of S. woodiana in an area with cold and long winters and extends the known limits of its thermal tolerance. Comparison of demographic profiles shows a more favourable population structure in S. woodiana than in the native mussels, indicating possible future dominance shifts. This study also shows that S. woodiana is a habitat generalist concerning bottom sediments, and points to intentional introductions of adult individuals as an important and underappreciated route of dispersal of this invasive species.Thermal tolerance of S. woodiana
    The introduction of Sinanodonta woodiana in 2000 resulted in a long-term establishment of its reproducing population, as evidenced by a high proportion of females carrying glochidia (17 out of 21 in 2018) and the presence of juveniles (the smallest individual of 33 mm shell-length was collected in 2019). While the populations of native mussels might have been augmented with glochidia attached to the stocking fishes, this was less likely in S. woodiana. The species was not recorded in the vicinity before13, and given the distance of over 500 km over which the founding individuals were transported, their local availability was unlikely. In any case, as the stocking fishes originated only from local sources, which did not include heated-water hatcheries, any S. woodiana glochidia would have also been from locally-adapted populations.Winters in the study area are relatively cold and long. In 2000–2019, the mean temperature of the coldest month was − 3.7 °C, and the lowest mean monthly temperature was − 10.8 °C. The absolute minimum temperature was − 31.1 °C. Ice formed each year, on average for 73 days, with a maximum of 104 days. As far as we know, these are the most extreme climatic conditions in which an established population of this species was documented to date. Sinanodonta woodiana has been reported from Sweden, but no reproduction was observed there30. The populations in the Yenisei and Ob River basins inhabit heated water effluents9,31. The other population in northern Poland in a thermally-unpolluted water body is in a milder climate24. Thus, our study extends the known limits of cold tolerance of S. woodiana, indicating a shift in its realized niche32 or an ongoing in situ adaptation11.Furthermore, with the ongoing climate change, the abiotic conditions in the invaded range of S. woodiana increasingly match its physiological optimum33. In our study area during the time since mussel introduction, the mean annual temperature increased by 0.8 °C, the number of days with ice formation decreased by 21, and the number of days with temperatures over 15 °C (coinciding with the production of ripe glochidia by S. woodiana15) increased by nine. Sinanodonta woodiana survives at water temperatures up to 38 °C34 and has a higher tolerance to thermal stress than the native mussels21. In heated water bodies it reproduces throughout the year18 and occupies habitats with higher temperature ranges than the native unionids14, indicating that climate warming will increase its competitive advantage. Additionally, high mobility of S. woodiana and its tendency to burrow deeply into the sediments may help it better survive during drought episodes.As shown in our study, in suboptimal thermal conditions, S. woodiana can persist at low abundances for decades. Outbreaks of such sleeper populations (sensu35) are likely to be triggered by changes in the environment, e.g., rising temperatures.Population structure of S. woodiana in relation to native unionidsOver four study years, the relative frequency of S. woodiana increased from 2 to 9%. A comparison of shell-length distributions, approximating population age-structure, shows that smaller-sized mussels contributed a higher proportion of individuals in S. woodiana than in the native mussels in all study years, and this difference was increasing over time. This increase over time was possibly related to the removal of S. woodiana individuals, as hand-sampling tends to be biased towards larger individuals. On the other hand, the high mobility of this species and its striking burrowing behaviour, which lowers its detectability, might have counterbalanced this effect, as illustrated by the largest S. woodiana individual, with a shell length of 22.5 cm, found in the last study year. Nevertheless, it is possible that without the removal of individuals, the size structure would also shift towards larger sizes in S. woodiana, and its relative abundance at the study sites would increase even faster. Interestingly, a higher contribution of smaller-sized individuals in S. woodiana than in the native mussels was also observed in24, where no mussels were removed before the study. Thus, in both these studies, S. woodiana not only established viable populations but also showed higher potential for population growth than the native mussels. This is not surprising given that S. woodiana grows faster, matures earlier and produces more glochidia per female than the native unionids17,18,19,36. At increasing relative frequencies, its direct effects on the native unionids: competition for food, bottom space and host fish, filtering out sperm and larvae, and transmission of diseases6 will play an increasing role, and a dominance shift can be expected. This, in turn, is expected to affect ecosystem functioning, including changes in water transparency and nutrient availability25,37, benthic habitat modification38,39, and reduction in the condition of fish40. Additionally, S. woodiana invasion threatens the endangered European bitterling Rhodeus amarus16, and its massive die-offs negatively impact water quality and reverberate to terrestrial ecosystems41,42.The increasing prevalence of S. woodiana in invaded areas17,23,43,44 supports its predicted ability to effectively compete with native mussels. Our present study shows that demographic profiles of co-occurring mussel populations can indicate future dominance shifts already at initial invasion stages. However, as in many alien species45,46, the time-lag between the establishment of S. woodiana and the expression of its impacts can last decades, explaining why, despite its striking body-size (“a football-sized invasive mussel”47), the threats from its invasion are largely underestimated.Tolerance of S. woodiana for bottom sediment typeDespite a large number of studies documenting the spread of S. woodiana (for a recent summary, see, e.g.,11,48), not much is known on its preferences concerning bottom sediments. Sinanodonta woodiana is mainly reported from ponds and reservoirs, which suggests its preference for muddy sediments. However, its presence in these habitats is related to its mode of dispersal rather than habitat preferences. Basing on a study in a heated lakes system with various habitats, Kraszewski and Zdanowski14 suggested a preference of S. woodiana for sandy bottom substrates. The patchy distribution of sandy and muddy bottom substrates allowed us to test this hypothesis in the present study.According to expectations, based on the known preferences of the native species49, A. cygnea occurred predominantly at sites with a muddy bottom, U. pictorum at sites with a sandy bottom, and A. anatina occurred at similar densities on both bottom types. Contrary to expectations, however, S. woodiana did not show a preference for either bottom type. Although its overall density was higher at sites with a sandy than a muddy bottom, this difference was not significant. Sinanodonta woodiana can utilize a broad range of host-fish species15,16,17 and survive in a broad range of water-body types13. Our study indicates that it is also a habitat generalist concerning bottom sediments and adds to the suit of the known tolerances of this species.Intentional human-mediated dispersalThe global spread of S. woodiana is primarily due to the trade in freshwater fish7,9. Our study points to intentional introductions for water filtration as an additional route of dispersal of this species. Large individual sizes and arguably beautiful colouration of S. woodiana add to its perceived attractiveness, and some people are willing to undertake considerable efforts to obtain individuals of this species. Occasional long-distance translocations can cause the bridgehead effect46,50, in which the establishment of populations in new locations facilitates the further dispersal of the species and leads to a self-accelerating invasion process. The way humans interact with invasive species is one of the main determinants of their spread and establishment51,52. Our local interviews indicate that individuals from the study pond have already been transferred to nearby water bodies, and their filtering ability is highly appreciated. The propensity of people to acquire and translocate Sinanodonta mussels has been noted before13,17,24,53,54,55 and is probably more important than previously appreciated.Management implicationsEradication of established invasive bivalve populations is extremely difficult6. An apparently successful attempt to eradicate S. woodiana from invaded fish ponds involved lowering the water level and poisoning the fish and mussels10,47, but usually such measures cannot be applied. An alternative is the removal of individuals by hand harvesting. To be effective, however, it should cover the whole surface of the invaded water body and be repeated regularly. A related, commonly used practice in field research on invasive species is to remove the collected individuals from the study area. Our study shows that at least in S. woodiana, this is not likely to have any practical effect. We took out all individuals collected during four annual surveys from collection sites covering approximately 8% of the surface area of the pond. The relative frequency of S. woodiana increased while its densities and shell-length distributions remained unchanged. This was not unexpected, given a small proportion of the population sampled, combined with the high reproduction rates and mobility of this species. As sampling rarely includes more than 10% of the studied populations, alternatively to removing individuals from a study area, long-term studies involving marking and releasing them back might be considered. Knowledge of the biology of S. woodiana in the wild (e.g., growth rates, longevity, behavioural responses) is scarce, limiting our ability to manage and reduce its further spread.The priority, however, is to prevent introductions of S. woodiana to non-invaded water bodies. Fish trade remains its dominant dispersal route, so effective biosecurity measures are necessary. Well-coordinated monitoring programmes are needed for evidence-based management decisions56. Public participation is key to successful management of invasive species. Publicly accessible educational programmes explaining the problems of invasive species and increasing the appreciation of the native ones are required, especially when the invasive species elicit favourable reactions from people51, as is the case with S. woodiana.Sinanodonta woodiana does not yet have the status of a recognized pest. For example, it is not included in the list of invasive alien species of European Union concern57 and there are no regulations concerning this species in most countries. Our study documents the potential of S. woodiana to demographically outcompete native unionids. Combined with its recognized impacts and rates of spread, it highlights the need to urgently call the attention of policymakers and the public to the threats posed by S. woodiana to the integrity of freshwater ecosystems. More

  • in

    Study of energetic properties of different tree organs in six Olea europaea L. cultivars

    1.European Commission. COM(2014) A policy framework for climate and energy in the period from 2020 to 2030. 1–18 (2012).2.Miranda, T. et al. Characterization and combustion of olive pomace and forest residue pellets. Fuel Process. Technol. 103, 91–96 (2012).CAS 
    Article 

    Google Scholar 
    3.Paiano, A. & Lagioia, G. Energy potential from residual biomass towards meeting the EU renewable energy and climate targets. The Italian case. Energy Policy 91, 161–173 (2020).Article 

    Google Scholar 
    4.Mehmood, M. A. et al. Biomass production for bioenergy using marginal lands. Sustain. Prod. Consum. 9, 3–21 (2017).Article 

    Google Scholar 
    5.Italian National Institute of Statistics ISTAT. Cultivations. At http://dati.istat.it/Index.aspx?DataSetCode=DCSP_COLTIVAZIONI (2020).6.Barbanera, M. et al. Characterization of pellets from mixing olive pomace and olive tree pruning. Renew. Energy 88, 185–191 (2016).CAS 
    Article 

    Google Scholar 
    7.Demirbas, A. Combustion characteristics of different biomass fuels. Prog. Energy Combust. Sci. 30, 219–230 (2004).CAS 
    Article 

    Google Scholar 
    8.Telmo, C. & Lousada, J. Heating values of wood pellets from different species. Biomass Bioenerg. 35, 2634–2639 (2011).CAS 
    Article 

    Google Scholar 
    9.Zeng, W., Tang, S. & Xiao, Q. Calorific values and ash contents of different parts of Masson pine trees in southern China. J. For. Res. 25, 779–786 (2014).Article 

    Google Scholar 
    10.Yan, P., Xu, L. & He, N. Variation in the calorific values of different plants organs in China. PLoS ONE 13, e0199762 (2018).Article 

    Google Scholar 
    11.FAO. Crops. At http://www.fao.org/faostat/en/#data/QC (2019).12.Gorzynik-Debicka, M. et al. Potential health benefits of olive oil and plant polyphenols. Int. J. Mol. Sci. 19, 686 (2018).Article 

    Google Scholar 
    13.Various authors. Handbook for a sustainable management of the olive groves. At https://olive4climate.eu/wp-content/uploads/Olive-4-Climate-Handbook.pdf (2017).14.Beccali, M., Columba, P., D’Alberti, V. & Franzitta, V. Assessment of bioenergy potential in Sicily: A GIS-based support methodology. Biomass Bioenerg. 33, 79–87 (2009).Article 

    Google Scholar 
    15.Gucci, R. & Cantini, C. Pruning and Training Systems for Modern Olive Growing (Csiro Publishing, Clayton, 2000).Book 

    Google Scholar 
    16.Fernandez, E. R. et al. Evolution and sustainability of the olive production systems. Options Méditerranéennes Séries A Mediterranean Seminars 106, 11–42 (2013).
    Google Scholar 
    17.Di Blasi, C., Tanzi, V. & Lanzetta, M. A study on the production of agricultural residues in Italy. Biomass Bioenerg. 12, 321–331 (1997).Article 

    Google Scholar 
    18.Brunori, A. et al. Biomass and volume modeling in Olea europaea L. cv “Leccino”. Trees Struct. Funct. 31, 1859–1874 (2017).Article 

    Google Scholar 
    19.Alves, C. A. et al. Gaseous and speciated particulate emissions from the open burning of wastes from tree pruning. Atmos. Res. 226, 110–121 (2019).CAS 
    Article 

    Google Scholar 
    20.Repullo, M. A., Carbonell, R., Hidalgo, J., Rodríguez-Lizana, A. & Ordóñez, R. Using olive pruning residues to cover soil and improve fertility. Soil Tillage Res. 124, 36–46 (2012).Article 

    Google Scholar 
    21.Directive (EU) 2018/2001 of the European Parliament and of the Council of 11 December 2018 on the promotion of the use of energy from renewable sources (2018).22.Nardino, M. et al. Annual and monthly carbon balance in an intensively managed Mediterranean olive orchard. Photosynthetica 51, 63–74 (2013).CAS 
    Article 

    Google Scholar 
    23.Romero-García, J. M. et al. Biorefinery based on olive biomass. State of the art and future trends. Bioresour. Technol. 159, 421–432 (2014).Article 

    Google Scholar 
    24.Werther, J., Saenger, M., Hartge, E. U., Ogada, T. & Siagi, Z. Combustion of agricultural residues. Prog. Energy Combust. Sci. 26, 1–27 (2000).CAS 
    Article 

    Google Scholar 
    25.Lehtikangas, P. Quality properties of pelletised sawdust, logging residues and bark. Biomass Bioenerg. 20, 351–360 (2001).Article 

    Google Scholar 
    26.Motisi, A. et al. Le cultivar di Olivo (Olea europaea L.) siciliane della collezione costituita dal dipartimento di colture arboree di Palermo presso l’azienda ‘Campo Carboj’ dell’Ente di Sviluppo Agricolo della regione Siciliana. Italus Hortus 13, 137–144 (2006).
    Google Scholar 
    27.Caruso, T. & D’Anna, F. Catalogo accessioni di Olivo Pesco Fragolina di bosco. Fondo Europeo agricolo per lo sviluppo rurale: l’Europa investe nelle zone rurali. (Tipografia Paruzzo Caltanissetta, 2015).
    Google Scholar 
    28.Caruso, T., Cartabellotta, D. & Antonio, M. Cultivar Di Olivo Siciliane. Identificazione, Validazione, Caratterizzazione morfologica e Molecolare e Qualità Degli Oli. Contiene manuale per la caratterizzazione primaria di cultivar di olivo siciliane. Palermo, Italy (2007).29.UNI EN ISO 14775 Solid Biofuels – Determination Of Ash Content. 14775 Solid Biofuels – Determination Of Ash Content (2010).30.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/ (2020).31.Sirna, A. LCA methodology in two self-consumption wood energy chains. PhD thesis, University of Tuscia, Italy (2012).32.Requejo, A., Feria, M. J., Vargas, F. & Rodríguez, A. Total use of olive tree prunings by means of hydrothermal and combustion processes. BioResources 7, 118–134 (2012).CAS 

    Google Scholar 
    33.Cuevas, M. et al. Drying kinetics and effective water diffusivities in olive stone and olive-tree pruning. Renew. Energy 132, 911–920 (2019).Article 

    Google Scholar 
    34.Garcia-Maraver, A., Rodriguez, M. L., Serrano-Bernardo, F., Diaz, L. F. & Zamorano, M. Factors affecting the quality of pellets made from residual biomass of olive trees. Fuel Process. Technol. 129, 1–7 (2015).CAS 
    Article 

    Google Scholar 
    35.Lama-Muñoz, A. et al. Characterization of the lignocellulosic and sugars composition of different olive leaves cultivars. Food Chem. 329, 127153 (2020).Article 

    Google Scholar 
    36.Garcia-Maraver, A., Salvachúa, D., Martínez, M. J., Diaz, L. F. & Zamorano, M. Analysis of the relation between the cellulose, hemicellulose and lignin content and the thermal behavior of residual biomass from olive trees. Waste Manag. 33, 2245–2249 (2013).CAS 
    Article 

    Google Scholar 
    37.Telmo, C. & Lousada, J. The explained variation by lignin and extractive contents on higher heating value of wood. Biomass Bioenerg. 35, 1663–1667 (2011).CAS 
    Article 

    Google Scholar 
    38.Demirbaş, A. Fuel properties and calculation of higher heating values of vegetable oils. Fuel 77, 1117–1120 (1998).Article 

    Google Scholar 
    39.Demirbaş, A. Relationships between heating value and lignin, moisture, ash and extractive contents of biomass fuels. Energy Explor. Exploit. 20, 105–111 (2002).Article 

    Google Scholar 
    40.García-Maraver, A., Terron, L. C., Ramos-Ridao, A. & Zamorano, M. Effects of mineral contamination on the ash content of olive tree residual biomass. Biosyst. Eng. 118, 167–173 (2014).Article 

    Google Scholar 
    41.Velázquez-Martí, B., Fernández-González, E., López-Cortés, I. & Salazar-Hernández, D. M. Quantification of the residual biomass obtained from pruning of trees in Mediterranean olive groves. Biomass Bioenerg. 35, 3453–3464 (2011).Article 

    Google Scholar 
    42.Spinelli, R. & Picchi, G. Industrial harvesting of olive tree pruning residue for energy biomass. Bioresour. Technol. 101, 730–735 (2010).CAS 
    Article 

    Google Scholar 
    43.García Martín, J. F. et al. Energetic valorisation of olive biomass: Olive-tree pruning, olive stones and pomaces. Processes 8, 511 (2020).Article 

    Google Scholar 
    44.Regione Sicilia, Dipartimento dell’Energia. Rapporto Energia 2015 Monitoraggio sull’energia in Sicilia. 1–168. At http://www.catastoenergetico.regione.sicilia.it/D/NEWS/Rapporto%20Energia%202015.pdf (2015). More

  • in

    Near-daily reconstruction of tropical intertidal limpet life-history using secondary-ion mass spectrometry

    Ecology of Yellowfoot limpetIn the Tropical Pacific, sympatric limpets (Cellana melanostoma, Cellana exarata, Cellana sandwicensis, Cellana talcosa) inhabit the Hawaiian rocky intertidal ecosystem, where they graze on crustose coralline algae (CCA) and epibenthic microorganisms. Distribution ranges from the splash zone (upper-intertidal) to subtidal zone, and across the entire Hawaiian Archipelago26. They are dispersed across the majority of seamounts, atolls, and islands, however, not all species are present in every rocky intertidal locality, which reflects species-specific micro-habitat preferences.The reproduction cycles for each species appears to vary in time and space, and on-going long-term monitoring efforts are in progress to define this critical life-history trait. Previous studies on the yellowfoot limpet C. sandwicensis, reveal that reproduction is highly synchronized from December to March27,29. Gametogenesis also occurs from June to August, however, the level synchronicity and intensity of this second spawn period are inconsistent.These limpets are gonochoristic and considered to be sequential hermaphrodites44. The sex ratio is near 1:1(M:F) during spawning season, however, we have directly observed populations to maintain disproportionate sex ratios.Development of this broad-cast spawning limpet has been described from egg to post-larvae, where settlement occurs in less than 4 days post-fertilization29. This short larval duration ensures recruitment to the same localized intertidal environment, and reduces likelihood of hybridization between sympatric species with similar life-histories26.For wild limpets, growth rates shift through ontogeny—average monthly growth decreasing from 4–5 mm shell length (SL) as juveniles to 2–3 mm SL as adults27. Limpets also exhibit seasonal growth patterns—influenced by temperature and feeding28,37. Currently, growth rates of large individuals ( >50 mm SL) and species longevity are absent in the literature.Regional climate and coastal oceanographyKa’alawai is located on the south-facing shoreline of Oahu Island, Hawai’i (21°15’20.7“N 157°47’30.8“W). This area, defined as a rocky intertidal zone, is primarily comprised of basalt outcrops, boulders and benches, and supports a diverse community of epibenthic flora and fauna. The area is relatively easy to access by foot, and has been continuously exposed to various anthropogenic factors, which includes development, urban run-off, and subsistence fishing.The microclimate of the region is characterized by mild, wet winters (January to March) and dry, hot summers (July to September). The mean daily atmospheric temperature range and mean daily sea-surface temperature range are 18.44–31.38 °C and 22.67–30.18 °C, respectively. The annual precipitation is low relative to windward sides of the island, with maximum rainfall of 6.35 cm (data sources: US climate station USC00519397: Waikiki 717.2; PacIOOS Nearshore Sensor 04 (NS04): Waikiki Aquarium). Although freshwater input from precipitation along this coastline is considered to be marginal, the mixing of submarine groundwater discharge generates a unique geochemical profile for surface seawater at Ka’alawai. In particular, the mean surface salinity for this study site has been reported to be 25.4 ‰, which reflects this highly localized land-sea interaction45.The coastal oceanography of this region is predominantly influenced by wave, wind, and tidal forces. The south-shore region experiences a mixed tidal cycle—having both diurnal and semi-diurnal sinusoidal constituents per lunar day—with a tidal range of 58 cm and 91 cm during neap tide and spring tide, respectively; The trade winds from north-easterly direction (between 22.5°–67.5°) account for ~63% of the year with mean annual intensity around 5 m/s;46 and South swells with wave amplitudes of ~3 m are generated by storms in the Tasmanian Sea during Northern Hemisphere Summer47,48.Modern and historical specimensOn June 28th of 2018, live Yellowfoot limpet (Cellana sandwicensis) specimens CW1 and CW2 were collected from the rocky intertidal zone at Ka’alawai, Oahu, Hawai’i (Fig. 7). The animals were immediately sacrificed/dissected using scalpel blade, and measured for shell dimensions using a caliper. Limpets were weighed to determine gonadosomatic index, and gonads were preserved for histological examination. Shells were rinsed in an ultrasonic bath and air-dried.Fig. 7: Study site map.Hawaiian limpet specimens (Cellana sandwicensis) were collected along the rocky intertidal shoreline of Ka’alawai (Oahu, Hawaii). Instrumental sea-surface temperatures were measured in-situ by PacIOOS Nearshore Sensor 04 (NS04) at the Waikiki Aquarium.Full size imageA historical specimen BPBM (identification number 250851-200492) was loaned from the Bernice Pauahi Bishop Museum Malacology Department Collection. This specimen’s geographical and ecological origin is unknown, but was identified as C. sandwicensis by its characteristic shell morphology49. This specimen was selected for its large size to estimate life-expectancy of this limpet species, as well as to evaluate this method for paleoclimatology studies.Permission was not required to obtain specimens used in this study, and limpets were collected at a size exceeds the legal minimum shell length of 31.8 mm (Hawaii State Law is enforced by Department of Land and Natural Resources). Ethical approval was not required to conduct analysis.Characterization of shell microstructureShell microstructure was identified before isotopic analysis could be attempted. Each shell was cross-sectioned from anterior to posterior direction using a low speed saw (Isomet 1000, Buehler) equipped with a 0.5 mm diamond coated blade. Parallel cuts were made at the apex or maximal growth-axis to obtain two replicate 1.3 mm thick-sections per specimen. The first replicate thick-sections, prepared for micro-sampling, were further cut into More

  • in

    Tree diversity and soil chemical properties drive the linkages between soil microbial community and ecosystem functioning

    1.Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature. 2006;440:165–73. https://doi.org/10.1038/nature04514.CAS 
    Article 
    PubMed 

    Google Scholar 
    2.Stocker TF, et al. IPCC, 2013: Climate Change 2013: 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, United Kingdom and New York, NY, USA; 2013.3.Lal R. Soil carbon sequestration impacts on global climate change and food security. Science. 2004;304:1623–7. https://doi.org/10.1126/science.1097396.CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Trumbore SE. Potential responses of soil organic carbon to global environmental change. Proc Natl Acad Sci USA. 1997;94:8284–91. https://doi.org/10.1073/pnas.94.16.8284.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Schlesinger WH, Andrews JA. Soil respiration and the global carbon cycle. Biogeochemistry. 2000;48:7–20. https://doi.org/10.1023/A:1006247623877.CAS 
    Article 

    Google Scholar 
    6.Singh BK, Bardgett RD, Smith P, Reay DS. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol. 2010;8:779–90. https://doi.org/10.1038/nrmicro2439.CAS 
    Article 
    PubMed 

    Google Scholar 
    7.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;7:10541 https://doi.org/10.1038/ncomms10541.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Liu Y-R, Delgado-Baquerizo M, Wang JT, Hu HW, Yang Z, He JZ. New insights into the role of microbial community composition in driving soil respiration rates. Soil Biol Biochem. 2018;118:35–41. https://doi.org/10.1016/j.soilbio.2017.12.003.9.McGuire KL, Treseder KK. Microbial communities and their relevance for ecosystem models: Decomposition as a case study. Soil Biol Biochem. 2010;42:529–35. https://doi.org/10.1016/j.soilbio.2009.11.016.10.Monson RK, Lipson DL, Burns SP, Turnipseed AA, Delany AC, Williams MW. et al. Winter forest soil respiration controlled by climate and microbial community composition. Nature. 2006;439:711–4. https://doi.org/10.1038/nature04555.CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Wieder WR, Bonan GB, Allison SD. Global soil carbon projections are improved by modelling microbial processes. Nature Clim Change. 2013;3:909–12. https://doi.org/10.1038/nclimate1951.12.Delgado‐Baquerizo M, Maestre FT, Reich PB, Trivedi P, Osanai Y, Liu YR, et al. Carbon content and climate variability drive global soil bacterial diversity patterns. Ecol Monogr. 2016;86:373–90.Article 

    Google Scholar 
    13.Maaroufi NI, Long JR de. Global change impacts on forest soils: linkage between soil biota and carbon-nitrogen-phosphorus stoichiometry. Front For Glob Change. 2020;3. https://doi.org/10.3389/ffgc.2020.00016.14.Gottschall F, Davids S, Newiger-Dous TE, Auge H, Cesarz S, Eisenhauer N. Tree species identity determines wood decomposition via microclimatic effects. Ecol Evol. 2019;9:12113–27. https://doi.org/10.1002/ece3.5665.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.Durán J, Delgado-Baquerizo M. Vegetation structure determines the spatial variability of soil biodiversity across biomes. Sci Rep. 2020;10:21500. https://doi.org/10.1038/s41598-020-78483-z.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Beugnon R, et al. Abiotic and biotic drivers of scale-dependent tree trait effects on soil microbial biomass and soil carbon concentration (in press).17.Pei Z, Eichenberg D, Bruelheide H, Kröber W, Kühn P, Li Y, et al. Soil and tree species traits both shape soil microbial communities during early growth of Chinese subtropical forests. Soil Biol Biochem. 2016;96:180–90. https://doi.org/10.1016/j.soilbio.2016.02.004.18.Xu S, Eisenhauer N, Ferlian O, Zhang J, Zhou G, Lu X. et al. Species richness promotes ecosystem carbon storage: evidence from biodiversity-ecosystem functioning experiments. Proc Biol Sci. 2020;287:20202063. https://doi.org/10.1098/rspb.2020.2063.CAS 
    Article 
    PubMed 

    Google Scholar 
    19.Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI. et al. Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun. 2015;6:6707. https://doi.org/10.1038/ncomms7707.CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA. et al. Persistence of soil organic matter as an ecosystem property. Nature. 2011;478:49–56. https://doi.org/10.1038/nature10386.CAS 
    Article 
    PubMed 

    Google Scholar 
    21.Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP. et al. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep. 2017;7:44641. https://doi.org/10.1038/srep44641.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Huang Y, Ma Y, Zhao K, Niklaus PA, Schmid B, He JS. Positive effects of tree species diversity on litterfall quantity and quality along a secondary successional chronosequence in a subtropical forest. J Plant Ecol. 2017;10:28–35. https://doi.org/10.1093/jpe/rtw115.Article 

    Google Scholar 
    23.Fornara DA, Tilman D. Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol. 2008;96:314–22. https://doi.org/10.1111/j.1365-2745.2007.01345.x.CAS 
    Article 

    Google Scholar 
    24.Chen C, Chen HYH, Chen X, Huang Z. Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration. Nat Commun. 2019;10:1332. https://doi.org/10.1038/s41467-019-09258-y.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Thoms C, Gattinger A, Jacob M, Thomas FM, Gleixner G. Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol Biochem. 2010;42:1558–65. https://doi.org/10.1016/j.soilbio.2010.05.030.CAS 
    Article 

    Google Scholar 
    26.Rousk J, Brookes PC, Bååth E. Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biol Biochem. 2010;42:926–34. https://doi.org/10.1016/j.soilbio.2010.02.009.27.Miltner A, Bombach P, Schmidt-Brücken B, Kästner M. SOM genesis: microbial biomass as a significant source. Biogeochemistry. 2012;111:41–55. https://doi.org/10.1007/s10533-011-9658-z.CAS 
    Article 

    Google Scholar 
    28.Delgado-Baquerizo M, Reich PB, Khachane AN, Campbell CD, Thomas N, Freitag TE. et al. It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environ Microbiol. 2017;19:1176–88. https://doi.org/10.1111/1462-2920.13642.CAS 
    Article 
    PubMed 

    Google Scholar 
    29.Fanin N, Barantal S, Fromin N, Schimann H, Schevin P, Hättenschwiler S. Distinct microbial limitations in litter and underlying soil revealed by carbon and nutrient fertilization in a tropical rainforest. PLoS ONE. 2012;7:e49990. https://doi.org/10.1371/journal.pone.0049990.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Louca S, Parfrey LW, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome. Science. 2016;353:1272–7. https://doi.org/10.1126/science.aaf4507.CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Cao J, Jia X, Pang S, Hu Y, Li Y, Wang Q. Functional structure, taxonomic composition and the dominant assembly processes of soil prokaryotic community along an altitudinal gradient. Appl Soil Ecol. 2020;155:103647. https://doi.org/10.1016/j.apsoil.2020.103647.Article 

    Google Scholar 
    32.Bao Y, Guo Z, Chen R, Wu M, Li Z, Lin X. et al. Functional community composition has less environmental variability than taxonomic composition in straw-degrading bacteria. Biol Fertil Soils. 2020;56:869–74. https://doi.org/10.1007/s00374-020-01455-y.CAS 
    Article 

    Google Scholar 
    33.Galand PE, Pereira O, Hochart C, Auguet JC, Debroas D. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 2018;12:2470–8. https://doi.org/10.1038/s41396-018-0158-1.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Kuang J, Huang L, He Z, Chen L, Hua Z, Jia P. et al. Predicting taxonomic and functional structure of microbial communities in acid mine drainage. ISME J. 2016;10:1527–39. https://doi.org/10.1038/ismej.2015.201.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Jurburg SD, Salles JF. Functional Redundancy and Ecosystem Function—The Soil Microbiota as a Case Study. In: Lo Y-H, Blanco JA, Roy S, editors. Biodiversity in Ecosystems—Linking Structure and Function. Rijeka, Croatia, InTech; 2015.36.Chen Q-L, Ding J, Li CY, Yan ZZ, He JZ, Hu HW. Microbial functional attributes, rather than taxonomic attributes, drive top soil respiration, nitrification and denitrification processes. Sci Total Environ. 2020;734:139479. https://doi.org/10.1016/j.scitotenv.2020.139479.CAS 
    Article 
    PubMed 

    Google Scholar 
    37.Trivedi P, Delgado-Baquerizo M, Trivedi C, Hu H, Anderson IC, Jeffries TC. et al. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships. ISME J. 2016;10:2593–604. https://doi.org/10.1038/ismej.2016.65.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    38.Hale L, Feng W, Yin H, Guo X, Zhou X, Bracho R. et al. Tundra microbial community taxa and traits predict decomposition parameters of stable, old soil organic carbon. ISME J. 2019;13:2901–15. https://doi.org/10.1038/s41396-019-0485-x.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Chen J, Sinsabaugh RL. Linking microbial functional gene abundance and soil extracellular enzyme activity: Implications for soil carbon dynamics. Glob Change Biol. 2021;27:1322–5. https://doi.org/10.1111/gcb.15506.Article 

    Google Scholar 
    40.Allison SD, Wallenstein MD, Bradford MA. Soil-carbon response to warming dependent on microbial physiology. Nat Geosci. 2010;3:336–40. https://doi.org/10.1038/ngeo846.41.Eisenhauer N, Bessler H, Engels C, Gleixner G, Habekost M, Milcu A. et al. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology. 2010;91:485–96. https://doi.org/10.1890/08-2338.1.CAS 
    Article 
    PubMed 

    Google Scholar 
    42.Bonner MT, Shoo LP, Brackin R, Schmidt S. Relationship between microbial composition and substrate use efficiency in a tropical soil. Geoderma. 2018;315:96–103. https://doi.org/10.1016/j.geoderma.2017.11.026.CAS 
    Article 

    Google Scholar 
    43.Bárány A, Szili-Kovács T, Krett G, Füzy A, Márialigeti K, Borsodi AK. Metabolic activity and genetic diversity of microbial communities inhabiting the rhizosphere of halophyton plants. Acta Microbiol Immunol Hung. 2014;61:347–61. https://doi.org/10.1556/AMicr.61.2014.3.8.CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Chodak M, Klimek B, Niklińska M. Composition and activity of soil microbial communities in different types of temperate forests. Biol Fertil Soils. 2016;52:1093–104. https://doi.org/10.1007/s00374-016-1144-2.CAS 
    Article 

    Google Scholar 
    45.Lagomarsino A, Knapp BA, Moscatelli MC, De Angelis P, Grego S, Insam H. Structural and functional diversity of soil microbes is affected by elevated [CO2] and N addition in a poplar plantation. J Soils Sediments. 2007;7:399–405. https://doi.org/10.1065/jss2007.04.223.46.Crowther TW, et al. The global soil community and its influence on biogeochemistry. Science. 2019;365. https://doi.org/10.1126/science.aav0550.47.Hall EK, Bernhardt ES, Bier RL, Bradford MA, Boot CM, Cotner JB. et al. Understanding how microbiomes influence the systems they inhabit. Nat Microbiol. 2018;3:977–82. https://doi.org/10.1038/s41564-018-0201-z.CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Malik AA, Martiny J, Brodie EL, Martiny AC, Treseder KK, Allison SD. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J. 2020;14:1–9. https://doi.org/10.1038/s41396-019-0510-0.CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Sainte-Marie J, Barrandon M, Saint-André L, Gelhaye E, Martin F, Derrien D. C-STABILITY an innovative modeling framework to leverage the continuous representation of organic matter. Nat Commun. 2021;12:810. https://doi.org/10.1038/s41467-021-21079-6.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    50.Bruelheide H, Nadrowski K, Assmann T, Bauhus J, Both S, Buscot F. et al. Designing forest biodiversity experiments: general considerations illustrated by a new large experiment in subtropical C hina. Methods Ecol Evol. 2014;5:74–89. https://doi.org/10.1111/2041-210X.12126.Article 

    Google Scholar 
    51.Yu G, Chen Z, Piao S, Peng C, Ciais P, Wang Q. et al. High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region. Proc Natl Acad Sci USA. 2014;111:4910–5. https://doi.org/10.1073/pnas.1317065111.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Bradstreet RB. Determination of Nitro Nitrogen by Kjeldahl Method. Anal Chem. 1954;26:235–6.CAS 
    Article 

    Google Scholar 
    53.Frostegård Å, Tunlid A, Bååth E. Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods. 1991;14:151–63. https://doi.org/10.1016/0167-7012(91)90018-L.54.Ruess L, Chamberlain PM. The fat that matters: Soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol Biochem. 2010;42:1898–910. https://doi.org/10.1016/j.soilbio.2010.07.020.55.Scheu S. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol Biochem. 1992;24:1113–8. https://doi.org/10.1016/0038-0717(92)90061-2.Article 

    Google Scholar 
    56.Schöps R, Goldmann K, Herz K, Lentendu G, Schöning I, Bruelheide H. et al. Land-use intensity rather than plant functional identity shapes bacterial and fungal rhizosphere communities. Front Microbiol. 2018;9:2711. https://doi.org/10.3389/fmicb.2018.02711.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Nawaz A, et al. DNA- and RNA- Derived Fungal Communities in Subsurface Aquifers Only Partly Overlap but React Similarly to Environmental Factors. Microorganisms. 2019;7. https://doi.org/10.3390/microorganisms7090341.58.Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7. https://doi.org/10.1038/s41587-019-0209-9.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    59.Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j. 2011;17:10. https://doi.org/10.14806/ej.17.1.200.60.Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. https://doi.org/10.1038/nmeth.3869.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    61.McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217. https://doi.org/10.1371/journal.pone.0061217.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    62.Lahti L, Shetty S, Blake T, Salojarvi J. Microbiome R package. Tools Microbiome Anal R. 2017;1:504.63.Liang Y, Liu X, Singletary MA, Wang K, Mattes TE. Relationships between the Abundance and Expression of Functional Genes from Vinyl Chloride (VC)-Degrading Bacteria and Geochemical Parameters at VC-Contaminated Sites. Environ Sci Technol. 2017;51:12164–74. https://doi.org/10.1021/acs.est.7b03521.CAS 
    Article 
    PubMed 

    Google Scholar 
    64.Zheng B, Zhu Y, Sardans J, Peñuelas J, Su J. QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci. 2018;61:1451–62. https://doi.org/10.1007/s11427-018-9364-7.CAS 
    Article 
    PubMed 

    Google Scholar 
    65.Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol. 2003;69:3593–9. https://doi.org/10.1128/aem.69.6.3593-3599.2003.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.Rosseel Y. Lavaan: An R package for structural equation modeling and more. Version 0.5–12 (BETA). J Stat Softw. 2012;48:1–36.Article 

    Google Scholar 
    67.Paterson E, Osler G, Dawson LA, Gebbing T, Sim A, Ord B. Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: Independent of the presence of roots and mycorrhizal fungi. Soil Biol Biochem. 2008;40:1103–13. https://doi.org/10.1016/j.soilbio.2007.12.003.68.Kramer S, Dibbern D, Moll J, Huenninghaus M, Koller R, Krueger D. et al. Resource Partitioning between Bacteria, Fungi, and Protists in the Detritusphere of an Agricultural Soil. Front Microbiol. 2016;7:1524. https://doi.org/10.3389/fmicb.2016.01524.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    69.Berg B. Litter decomposition and organic matter turnover in northern forest soils. Forest Ecol Manag. 2000;133:13–22. https://doi.org/10.1016/S0378-1127(99)00294-7.Article 

    Google Scholar 
    70.Moretto AS, Distel RA, Didoné NG. Decomposition and nutrient dynamic of leaf litter and roots from palatable and unpalatable grasses in a semi-arid grassland. Appl Soil Ecol. 2001;18:31–7. https://doi.org/10.1016/S0929-1393(01)00151-2.Article 

    Google Scholar 
    71.Kyker-Snowman E, Wieder WR, Frey SD, Grandy AS. Stoichiometrically coupled carbon and nitrogen cycling in the MIcrobial-MIneral Carbon Stabilization model version 1.0 (MIMICS-CN v1.0). Geosci Model Dev. 2020;13:4413–34. https://doi.org/10.5194/gmd-13-4413-2020.CAS 
    Article 

    Google Scholar 
    72.Buckeridge KM, Mason KE, McNamara NP, Ostle N, Puissant J, Goodall T. et al. Environmental and microbial controls on microbial necromass recycling, an important precursor for soil carbon stabilization. Commun Earth Environ. 2020;1:36. https://doi.org/10.1038/s43247-020-00031-4.Article 

    Google Scholar 
    73.Cesarz S, Craven D, Auge H, Bruelheide H, Castagneyrol B, Hector A, et al.. Biotic and abiotic drivers of soil microbial functions across tree diversity experiments. bioRXiv 2020. https://doi.org/10.1101/2020.01.30.927277.74.Tedersoo L, Bahram M, Cajthaml T, Põlme S, Hiiesalu I, Anslan S. et al. Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J. 2016;10:346–62. https://doi.org/10.1038/ismej.2015.116.CAS 
    Article 
    PubMed 

    Google Scholar 
    75.Huang Y, Chen Y, Castro-Izaguirre N, Baruffol M, Brezzi M, Lang A. et al. Impacts of species richness on productivity in a large-scale subtropical forest experiment. Science. 2018;362:80–3. https://doi.org/10.1126/science.aat6405.CAS 
    Article 
    PubMed 

    Google Scholar 
    76.Chapman SK, Newman GS, Hart SC, Schweitzer JA, Koch GW. Leaf litter mixtures alter microbial community development: mechanisms for non-additive effects in litter decomposition. PLoS ONE. 2013;8:e62671. https://doi.org/10.1371/journal.pone.0062671.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    77.Eisenhauer N, Dobies T, Cesarz S, Hobbie SE, Meyer RJ, Worm K. et al. Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. Proc Natl Acad Sci USA. 2013;110:6889–94. https://doi.org/10.1073/pnas.1217382110.Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    78.Brandt BW, Kelpin FDL, van Leeuwen IMM, Kooijman SALM. Modelling microbial adaptation to changing availability of substrates. Water Res. 2004;38:1003–13. https://doi.org/10.1016/j.watres.2003.09.037.CAS 
    Article 
    PubMed 

    Google Scholar 
    79.Hooper DU, BIGNELL DE, BROWN VK, BRUSSARD L, MARK DANGERFIELD J, WALL DH, et al. Interactions between Aboveground and Belowground Biodiversity in Terrestrial Ecosystems: Patterns, Mechanisms, and Feedbacks. BioScience. 2000;50:1049.Article 

    Google Scholar 
    80.Domke GM, Oswalt SN, Walters BF, Morin RS. Tree planting has the potential to increase carbon sequestration capacity of forests in the United States. Proc Natl Acad Sci USA. 2020;117:24649–51. https://doi.org/10.1073/pnas.2010840117.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Tong X, Brandt M, Yue Y, Ciais P, Rudbeck Jepsen M, Penuelas J. et al. Forest management in southern China generates short term extensive carbon sequestration. Nat Commun. 2020;11:129. https://doi.org/10.1038/s41467-019-13798-8.CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    82.Veldkamp E, Schmidt M, Powers JS, Corre MD. Deforestation and reforestation impacts on soils in the tropics. Nat Rev Earth Environ. 2020;1:590–605. https://doi.org/10.1038/s43017-020-0091-5.Article 

    Google Scholar 
    83.Lewis SL, Wheeler CE, Mitchard ETA, Koch A. Restoring natural forests is the best way to remove atmospheric carbon. Nature. 2019;568:25–8. https://doi.org/10.1038/d41586-019-01026-8.CAS 
    Article 
    PubMed 

    Google Scholar  More