More stories

  • in

    Sustainability of soil organic carbon in consolidated gully land in China’s Loess Plateau

    SCALE model
    Combining the processes of biogeochemical transformation, soil erosion/deposition and resultant landscape evolution, and bioturbation by soil fauna, the governing equations, which conserves SOC mass, can be expressed as24:

    $$begin{aligned} frac{ partial }{ partial t } int _{0}^{Z} mathbf{C } dz =int _{0}^{Z} mathbf{g } dz – nabla cdot mathbf{q }_C + int _{0}^{Z} nabla cdot big [D(z) nabla mathbf{C } big ] dz end{aligned}$$
    (1)

    where (mathbf{C }) is the SOC concentration ([M L^{-3}]), (mathbf{C } = [ C_l,C_h,C_b]^T) represents the fast (or litter), slow (or humus), and microbial biomass pool, respectively; (mathbf{g }) is the rate of the biogeochemical transformation process, which is a function of the fast (or litter), slow (or humus), and microbial biomass pool; (nabla cdot mathbf{q }_C) is the surface SOC flux associated with soil transport; and (D(z)) is the bioturbation diffusivity. When the vertical column is discretized into several layers, the equations can be written as:

    $$begin{aligned} text {Top soil layer: }&frac{ partial big ( mathbf{C }_1 z_1 big ) }{ partial t } = mathbf{g }_1 z_1 – nabla cdot mathbf{q }_C end{aligned}$$
    (2a)

    $$begin{aligned} text {Sublayers: }&frac{ partial mathbf{C }_n }{ partial t } = mathbf{g }_n + nabla cdot big [D(z) nabla mathbf{C } big ] dz end{aligned}$$
    (2b)

    where the subscripts 1 and n denote the surface soil layer and the (n{mathrm{^{th}}}) layer below-surface, respectively. Other details of these equations can be found in24.
    The mechanisms of soil transport and the resultant landscape evolution can be categorized into two groups: overland flow-driven transport and diffusion-driven transport from other disturbances (e.g., wind, animal, and raindrop splash). The 2-D mass conservation equation of soil transport and the resultant landscape evolution follows Exner equation:

    $$begin{aligned} frac{partial eta }{partial t} = U -nabla cdot q_d – nabla cdot q_s end{aligned}$$
    (3)

    where (eta) is soil surface elevation [L]; U is the rate of tectonic uplift or glacial rebound ([L T^{-1}]); (q_d) is the volume flux of sediment per unit width by hillslope diffusion ([L^2 T^{-1}]); (q_s) is the volume flux of sediment per unit width by overland flow ([L^2 T^{-1}]).
    The diffusion-driven transport (nabla cdot q_d) is a combination of wind erosion, animal disturbance, soil creep, raindrop splash, and biogenic transport. The 2-D equation of (q_d) is expressed as a linear relationship with slope47:

    $$begin{aligned} q_d = – D_{x} frac{ partial eta }{partial x} – D_{y} frac{ partial eta }{partial y} end{aligned}$$
    (4)

    where (D_x) and (D_y) are the soil diffusion coefficient in x and y direction, respectively ([L^2 T^{-1}]). The overland flow-driven transport (nabla cdot q_s) is a combined form of the divergence of stream-power but limited by the detachment capacity48:

    $$begin{aligned} nabla cdot q_s = min Bigg ( D_c, frac{q_{s,out} – sum q_{s, in}}{d_s} Bigg ) end{aligned}$$
    (5)

    where (D_c) is the detachment capacity, which is the upper limit of of local erosion rate ([L/S]); (q_{s,out}) is the sediment flux out of a cell and (sum q_{s, in}) is the total sediment flux into a cell assumed at sediment transport capacity.
    The rate of change of SOC on the surface driven by soil transport is (nabla cdot q_s), which has a linear relationship with soil transport flux:

    $$begin{aligned} nabla cdot mathbf{q }_{C} = nabla cdot ( k_{soc} mathbf{C }_{1} q_d) + nabla cdot ( k_{soc} mathbf{C }_{1} q_s) end{aligned}$$
    (6)

    where (mathbf{C } = [C_l , C_h , C_b ]^T), and the subscript 1 denotes the surface soil layer; (q_d) and (q_s) are soil transport flux of diffusion and overland flow; (k_{soc}) is an enrichment ratio, which represents a preferential transport (mobilization and deposition) of SOC. The SOC fluxes driven by diffusion and overland flow sediment transport are:

    $$begin{aligned} nabla cdot ( k_{soc} mathbf{C }_{1} q_d)= & {} – frac{partial }{partial x} bigg (k_{soc} mathbf{C }_{1} D_{x} frac{ partial eta }{partial x} bigg ) – frac{partial }{partial y} bigg (k_{soc} mathbf{C }_{1} D_{y} frac{ partial eta }{partial y}bigg ) end{aligned}$$
    (7)

    $$begin{aligned} nabla cdot big (k_{soc} mathbf{C }_{1} q_s big )= & {} left{ begin{array}{ll} k_{soc} mathbf{C }_{1} D_c , &{}quad mathrm{if} D_c < frac{q_{s,out} - sum q_{s, in}}{d_s} \ frac{ k_{soc} mathbf{C }_{1,out} q_{s,out} - sum big ( k_{soc}mathbf{C }_{1,in} q_{s, in} big ) }{d_s} , &{}quad mathrm{otherwise} end{array} right. end{aligned}$$ (8) The initial conditions include land surface elevation, SOC profiles, soil moisture, and surface water depth for each grid box. Table S1 (in Supplementary Information) lists variables associated with initial conditions. We simulate the SOC surface transport and vertical transformation at a daily time step with 2 (times) 2 (mathrm{m}^2) spatial resolution on the surface and a range of vertical grid sizes varying from 5 to 60 (text{cm}). The initial elevation is from lidar (Light Detection and Ranging) DEM (digital elevation model) with a 2-m resolution, collected by a drone in 2015. The SOC profiles at each 2-D grid are estimated by combining the surface SOC contents from the field survey in 2016 and SOC profiles from soil cores sampled at a nearby site 2-km away (see Section below). We assume that the initial soil thickness is 1-m because the most active soil thickness49 regarding SOC and soil moisture are within the top 1 (text{m}), and the deeper SOC contents are quite uniform19,20, indicating a relatively stable condition. Also, we neglect bedrock weathering, and therefore, the soil thickness change is only from the surface soil erosion or deposition. The SOC stock and soil thickness change in the results are compared with the initial SOC stock in the top 1 m. Other initial values such as soil moisture profile and surface water depth (i.e., initial values assigned spatially uniform at each grid point) have a short-time memory in that the impacts only last for a few days to weeks and are predominantly determined by the external forcing and resulting dynamics (more information in Supplementary Information Table S1). Initial soil organic carbon profiles SOC in a natural setting exponentially decreases with soil depth. Here we assume the following relationship between SOC content and soil depth: $$begin{aligned} SOC(Z) = a e^{-bZ} + c end{aligned}$$ (9) where (text{SOC}(text{Z})) represents SOC content at depth (text{Z}); (text{Z}) is zero at the surface, and positive downward; (a), (b), and (c) are positive and constant parameters, where (a+c) represents surface SOC content, (b) represents the decay rate, and (c) represents the relative stable or immobile SOC at depth. Parameters (b) and (c) in this study are estimated from twenty deep cores—ten sites at hills of the Reference Watershed, eight sites at GLC Watershed in the hills, and two sites in the consolidated gully land (Figure S7a). The SOC contents are shown as dots in Figure S6 (in Supplementary Information). We assume the exponential decay rate ((b)) and the immobile SOC ((c)) are spatially uniform in the cornfield in the consolidated gully area and natural field, respectively. We use the least square non-linear method to fit the sample points, and the fitted curves are solid lines in Figure S6 (in Supplementary Information) with the corresponding relationships obtained as: $$begin{aligned} text {For trees/shrubs: }&SOC(Z) = 8.04 e^{-9.63Z}+2.55 end{aligned}$$ (10a) $$begin{aligned} text {For crops: }&SOC(Z) = 3.71 e^{-7.06Z}+2.27 end{aligned}$$ (10b) hence in the natural area, (b= 9.63) and (c = 2.55); and in the cornfield, (b = 7.06) and (c = 2.27). The parameter (a) varies spatially. Soil samples near the soil surface were collected across the whole area of both the GLC and Reference Watershed in 2016. To ensure that the sampling sites are uniformly distributed and represent all land cover types in each watershed, we superimposed an 80-m (times) 80-m grid on the DEM map. In each grid cell, we selected one representative site to collect soil samples; in consolidated gullies, adjacent sampling sites were spaced at an interval of  40-m because of the relatively narrow width. SOC was measured in a laboratory by using the dichromate oxidation method50. In the GLC Watershed, soil samples were collected at 89 locations with 178 samples (0–10 cm and 10–20 cm); in the Reference Watershed, soil samples were collected at 72 locations with 144 samples (Figure 2a, in Supplementary Information). We used Kriging51 to interpolate the SOC content in each 2-D grid box in the two watersheds. Then (a) is back-calculated with the given values of the two layers at 5 cm and 15 cm (the middle point of the two layers, respectively). The final surface SOC (which equals (a+c)) is shown in Figure S7a (in Supplementary Information). Forcing data To explore the co-evolution of the landscape and the vertical profiles of SOC over the decadal time scale, we target a 50-years simulation. The meteorological data is collected from the China National Field Observation Station in An’sai ((36^{circ } 51^{prime } 30^{prime prime } N), (109^{circ } 19^{prime } 23^{prime } E); data source: http://asa.cern.ac.cn), 44 km away to the northwest from the two watersheds, with a 10 years record from 2008 to 2017, which is the best available data for the simulation. The mean annual precipitation is 560 mm. These data are used to train a stochastic Weather Generator52, which is used to create an ensemble of another 40 years of data (Figure S7c in Supplementary Information). Landcover is also obtained from the field survey in 2015 (Figure S7b in Supplementary Information). It is essential for simulating surface water runoff and the input of SOC from plant residues. Different types of landcover provide different fractions that control the surface water runoff velocity, and such fraction is represented by Manning’s coefficient (Table S2 in Supplementary Information). The plant residues include dead leaves, roots, stems, and corn stover after harvest. Here, we estimate plant residues as a function of the Normalized Difference Vegetation Index (NDVI) (Figure S3a) which is obtained from Landsat satellite data (see more information in the Section below). Litter input estimation The NDVI is collected from Landsat satellite data for a full 2 years period, 2016 and 2017. It is spatially divided into three areas, the consolidated gully land, the GLC Watershed, and the Reference Watershed. The spatial distribution of NDVIs for the two watersheds are nearly identical, so we took the spatial means of NDVI for the two watersheds excluding the consolidated gully to represent the natural area (Figure S3a in Supplementary Information). During the growing season, the NDVIs in a natural area (Figure S3(a1) in Supplementary Information) are smaller than the one in the consolidated gully (Figure S3a2 in Supplementary Information). This is because the crop inside the consolidated gully has higher vegetation density. We assume the rate of litterfall has an exponentially increasing relationship with NDVI (Figure S3b in Supplementary Information). As the NDVI increases, the plant residues increase in general. When a plant’s growth slows down, the NDVI increase also slows down and is close to the maximum, but on the other hand, the litterfall rate increases much faster near the end of the growing season. This characterization allows us to fill in the gap due to the lack of litterfall data about the various land vegetation types, including the cornfield in the consolidated gully. Governing equations of SOC transformation The equation below shows the SOC transformation, which is directly affected by litter input and decomposition rate29: $$begin{aligned} frac{partial big ( C_l + C_h + C_b big ) }{partial t} = I_{litter} - big (r_r K_l C_l+r_r K_h C_h big ) end{aligned}$$ (11) where (C_l), (C_h), and (C_b) are defined in Eq. 1; (I_{litter}) is the litter input from the sum of above-ground litter fall and below-ground root-litter ([M L^{-2}T^{-1} ]); (r_r) defines the fraction of decomposed organic carbon to (hbox {CO}_2) ([-]) ((0 le r_r le 1-r_h)), which typically ranges between 0.6 and 0.8; (K_l) and (K_h) are rates of carbon decomposition in fast and slow pool, respectively ([T^{-1}]). They are regulated by soil moisture and carbon-nitrogen ((C/N)) ratio as shown below29: $$begin{aligned}&K_l = varphi (C/N) f_d(theta ) k_l C_b end{aligned}$$ (12a) $$begin{aligned}&K_h =varphi (C/N) f_d(theta ) k_h C_b end{aligned}$$ (12b) where (k_l) and (k_h) represent the rate of decomposition as a simplified term that encompasses different organic components in the litter and humus pool, respectively ([L^3 T^{-1} M^{-1}]); (varphi (C/N)) is a ratio that is from the reduction of the decomposition rate if the immobilization (controlled by nitrogen content) fails to meet the nitrogen demand by the microbes ([-]). (varphi approx 1) in agricultural fields where nitrogen supply is usually sufficient from fertilizers; (f_d(theta )) ([-]) represents the soil moisture effects on decomposition29. The optimal soil moisture condition is the field capacity which provides the highest (f_d)29, meaning that very dry or very wet conditions will result in a smaller (f_d), and hence reduce the decomposition rate. The decomposition rates for litter (or fast) pool and humus (or slow) pool from the equations are (r_r K_l) and (r_r K_h), respectively. In this study, we test the different mean residence times on the surface soil layer (5-cm) by assigning a new decay rate of the decomposition parameter (k_h) in humus (or slow) pool. A complete list of parameters can be found in Supplementary Information Table S2. More

  • in

    Identifying the sources of structural sensitivity in partially specified biological models

    Quantifying structural sensitivity in models with uncertain component functions
    In general, we consider a system of the form:

    $$begin{aligned} dot{{mathbf{x }}}={mathbf{G}} left( h_1left( {mathbf{x}} right) ,h_2left( {mathbf{x}} right) ,ldots ,h_pleft( {mathbf{x}} right) , f_1left( {mathbf{x}} right) ,f_2left( {mathbf{x}} right) ,ldots ,f_{m-p}left( {mathbf{x}} right) right) , end{aligned}$$
    (1)

    where ({mathbf {x}}in {mathbb {R}}) is the vector of d state variables, (h_i, f_i:{mathbb {R}}^{d_i}rightarrow {mathbb {R}}) are the m different component functions describing the inflows and outflows of biomass, energy or individuals due to certain biological processes, with ({mathbf{G}} :{mathbb {R}}^mrightarrow {mathbb {R}}^d) being a composition function describing the general topology of the system. We consider that the precise mathematical formulation of the functions (f_i) are known (or at least postulated) with the only related uncertainty being the precise choice of their parameters. The functions (h_1,ldots h_p) are considered to have unspecified functional form. Instead, they are represented by bounds on their derivatives matching the qualitative properties we would expect from such a function. For example, the per-capita reproduction rate of a population is generally decreasing, at least at large population numbers, while a feeding term described by a Holling type II functional response of a predator should be increasing and decelerating. The (h_i) may also have quantitative bounds on their values:

    $$begin{aligned} h_i^{text {low}}left( {mathbf{x}} right)1)), an important question remains: which of the unknown functions contribute the most to the degree of structural sensitivity in the system? The degree of structural sensitivity does not distinguish between the various sources of uncertainty and therefore cannot quantify the relative contributions of the unknown functions to the uncertainty in the model dynamics.
    To determine the contribution of each unknown function (h_i), one can allow the error terms (left( varepsilon _1,varepsilon _2,ldots ,varepsilon _pright)) to vary with the goal of investigating how the degree of sensitivity varies with them. For the purpose of this section, let us denote the initial error terms by (varepsilon _i^0). We might be tempted to use the dependence on the (varepsilon _i) to perform global optimisation under certain constraints to find the best possible reduction of (left( varepsilon _1,varepsilon _2,ldots ,varepsilon _pright)). However, one should bear in mind that this analysis would depend on the base functions (hat{h}_i) considered. While these functions are ideally fitted to experimental data, they are only accurate within the error terms (varepsilon _i^0). Excessively reducing the (varepsilon _i) will force all admissible functions to conform strongly in their shape to these base functions far beyond their demonstrated accuracy of fit.
    The dependence of the degree of sensitivity on (varepsilon _i) should therefore only be evaluated locally by calculating the gradient (left( frac{partial Delta }{partial varepsilon _1},ldots ,frac{partial Delta }{partial varepsilon _p}right) |_{left( varepsilon _1^0,ldots varepsilon _p^0right) }) giving the direction for the best local reduction of the errors. To adjust for the fact that the error terms may be of different orders of magnitude, when handling the vectors of error terms we should use the norm

    $$begin{aligned} left| varvec{varepsilon }right| = sqrt{sum _{i=1}^{p} left( frac{varepsilon _i }{varepsilon _i^0}right) ^2}. end{aligned}$$
    (9)

    Working in this norm, the gradient needs to be weighted by the initial error terms to provide the direction for the best local reduction of the error terms, this is described by the following structural sensitivity gradient.
    Definition 2
    The structural sensitivity gradient in a model with p unknown functions each having an error of magnitude (varepsilon ^0_i) is defined as

    $$begin{aligned} left( -varepsilon _1^0cdot frac{partial Delta }{partial varepsilon _1},ldots ,-varepsilon _p^0cdot frac{partial Delta }{partial varepsilon _p}right) |_{left( varepsilon _1=varepsilon _1^0,ldots ,varepsilon _p=varepsilon _p^0right) }, end{aligned}$$
    (10)

    where (Delta left( varepsilon _1,ldots ,varepsilon _pright)) is the degree of structural sensitivity of the system considered as a function of the error terms (varepsilon _i).
    One possible problem with the structural sensitivity gradient is that the degree of structural sensitivity in the system may not be an increasing function of the magnitude of the errors. Consider the case that the exact system is structurally unstable, e.g. at a bifurcation point. Then no matter how small the error terms are, there may still be very high levels of structural sensitivity, while larger error terms may cause the level of uncertainty to decrease5. In this case, the structural sensitivity gradient will indicate that one or more of the functions has a negative contribution to the uncertainty of the system, and cannot be taken as a basis for sensitivity analysis.
    An alternative approach to quantifying the individual impact of unknown functions which avoids this issue is the computation of partial degrees of sensitivity with respect to each (h_k). To do this, we fix every unknown function except (h_k), a set which we denote ({mathbf{H}} _{sim k}), by fixing the (x_j^*), (h_ileft( {mathbf{x}} ^*right)), and (frac{partial h_i}{partial x_j} left( {mathbf{x}} ^* right)) that are consequently determined by the isocline equations. Denoting by (V_k) the cross-sections of V where only (h_k) varies, and the cross-sections for ({mathbf{H}} _{sim k}) by (V_{sim k}), the local partial degree of structural sensitivity can be defined as follows.
    Definition 3
    The local partial degree of structural sensitivity with respect to (h_k), is the degree of structural sensitivity in the model when (h_k) is unspecified and all other functions (h_i in {mathbf{H}} _{sim k}) are fixed:

    $$begin{aligned} Delta _k({mathbf{H}} _{sim k}):= 4 cdot int _{V_{k_{text {stable}}}} rho _{mathbf{H} _kvert {mathbf{H}} _{sim k}} , d{mathbf{H}} _k cdot left( 1 – int _{V_{k_{text {stable}}}} rho _{mathbf{H} _kvert {mathbf{H}} _{sim k}} , d{mathbf{H}} _k right) , end{aligned}$$
    (11)

    where (rho _{mathbf{H} _kvert {mathbf{H}} _{sim k}}) is the conditional probability density function on ({mathbf{H}} _{sim k}):

    $$begin{aligned} rho _{mathbf{H} _kvert {mathbf{H}} _{sim k}} = frac{rho }{int _V rho d{mathbf{H}} _{sim k }}, end{aligned}$$

    with (rho) the (joint) probability distribution over V.
    The local partial sensitivity (Delta _k({mathbf{H}} _{sim k})) is a function of ({mathbf{H}} _{sim k}) in that it depends upon the particular values at which the elements of (V_{sim k}) are fixed. As with the degree of structural sensitivity, it can be interpreted as either the probability that the stability of the given equilibrium will be different for two independent choices of the function (h_k) when the (h_{sim k}) are fixed at the given values, or in terms of variance as (Delta _k({mathbf{H}} _{sim k})=4cdot {text {Var}}_k(Yvert {mathbf{H}} _{sim k})) (Y is the Bernoulli variable for stability). If the joint probability distribution (rho) is uniform in V, then (Delta _k({mathbf{H}} _{sim k})) can be expressed purely in terms of the fraction of the volume of (V_k) which gives a stable equilibrium:

    $$begin{aligned} Delta _k({mathbf{H}} _{sim k}) = 4 cdot frac{int _{V_{k_{text {stable}}}} d{mathbf{H}} _k}{int _{V_k} d{mathbf{H}} _k} cdot left( 1 – frac{int _{V_{k_{text {stable}}}} d{mathbf{H}} _k}{int _{V_k} d{mathbf{H}} _k} right) . end{aligned}$$
    (12)

    To obtain a global measure for the sensitivity of the model to (h_k), we can take the average of (Delta _k) over (V_{sim k}).
    Definition 4
    The partial degree of structural sensitivity with respect to (h_k) is given by

    $$begin{aligned} bar{Delta }_k := int _{V_{sim k}} rho _{mathbf{H} _{sim k}} cdot Delta _k({mathbf{H}} _{sim k}) , d{mathbf{H}} _{sim k} end{aligned}$$
    (13)

    where (rho _{mathbf{H} _{sim k}}) is the marginal probability density function of ({mathbf{H}} _{sim k}).
    Recalling the variance-based interpretation of the degree of sensitivity, we obtain (bar{Delta }_k = 4cdot E_{sim k}({text {Var}}_kleft( Yvert {mathbf{H}} _{sim k}right) )). In other words, (bar{Delta }_k) gives the scaled average variance when all functions except (h_k) are fixed. We can also relate the partial degree of structural sensitivity to indices used in conventional variance-based sensitivity analysis. Dividing (bar{Delta }_k) by the overall degree of structural sensitivity in the model gives us (frac{bar{Delta }_k}{Delta }=frac{E_{sim k}({text {Var}}_kleft( Yvert {mathbf{H}} _{sim k}right) )}{{text {Var}}(Y)}=S_{T_k}), the total effect index23 of (h_k) on the stability of the equilibrium. This is a measure of the total contribution of (h_k) to the sensitivity—both alone and in conjunction with the other functions ({mathbf{H}} _{sim k}). However, since the space of valid functions V is in general not a hypercube, the functions (h_i) are not independent factors, and a total decomposition of variance is not possible. Indeed, even if the joint probability distribution (rho) is uniform, the marginal probability distribution (rho _{mathbf{H} _{sim k}}) will generally not be: instead it will equal the volume of the corresponding cross-section (V_k) for ({mathbf{H}} _{sim k}), divided by the volume of V. An alternative to using the partial degrees of sensitivity would be to consider the first-order sensitivity indices (S_k=frac{{text {Var}}_kleft( E_{mathbf{H} _{sim k}}left( Yvert h_k right) right) }{{text {Var}}(Y)}). However, these do not take into account possible joint effects of the (h_i) on the structural sensitivity of the system, so a small (S_k) does not indicate that (h_k) is not a source of sensitivity, whereas (bar{Delta }_k=0) means that (h_k) does not contribute to the structural sensitivity in the system at all.
    Similarly to the gradient of the total degree of sensitivity (Delta) as a function of the respective error tolerances, the vector (left( -bar{Delta }_{h_1},ldots , -bar{Delta }_{h_p}right)) needs to be scaled by the elements of (varepsilon ^0) to give us the optimal direction of decrease in (Delta) if the error terms (varepsilon _i) are subject to a proportional reduction. This is described by (left( -varepsilon _1^0 bar{Delta }_{h_1},ldots , -varepsilon _p^0bar{Delta }_{h_p}right)).
    Outline of an iterative framework of experiments for reducing structural sensitivity
    When dealing with partially specified models, an important practical task is the reduction of the overall uncertainty in the system by decreasing the uncertainty in the system processes (i.e. the unknown model functions). Here we propose an iterative process of such a reduction based on improving our empirical knowledge of the uncertain functions (h_k).
    As a starting point, we assume that experiments have produced data on the unknown functions (h_1,ldots ,h_p), to which we can fit some base functions (hat{h}_1,ldots ,hat{h}_p) with initial errors (varepsilon _1^0,ldots ,varepsilon _p^0). We assume that it is possible to perform additional experiments on all uncertain processes in order to obtain more data such that the (varepsilon _i) can be decreased, but with the natural constraint that the total error can only be reduced by a magnitude of (0 More

  • in

    Deglacial to Holocene variability in surface water characteristics and major floods in the Beaufort Sea

    1.
    Serreze, M. C., Holland, M. M. & Stroeve, J. Perspectives on the Arctic’s shrinking sea-ice cover. Science 315, 1533–1536 (2007).
    CAS  Article  Google Scholar 
    2.
    Screen, J. A. & Simmonds, I. The central role of diminishing sea ice in recent Arctic temperature amplification. Nature 464, 1334–1337 (2010).
    CAS  Article  Google Scholar 

    3.
    Dai, A., Luo, D., Song, M. & Liu, J. Arctic amplification is caused by sea-ice loss under increasing CO2. Nat. Commun. 10, 121–133 (2019).
    Article  CAS  Google Scholar 

    4.
    Kim, K. et al. Vertical feedback mechanism of winter Arctic amplification and sea ice loss. Sci. Rep. 9, 1184 (2019).
    Article  CAS  Google Scholar 

    5.
    Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).
    CAS  Article  Google Scholar 

    6.
    Mundy, C. J. et al. Contribution of under-ice primary production to an ice-edge upwelling phytoplankton bloom in the Canadian Beaufort Sea. Geophys. Res. Lett. 36, L17601 (2009).
    Article  Google Scholar 

    7.
    Sévellec, F., Fedorov, A. V. & Liu, W. Arctic sea-ice decline weakens the Atlantic Meridional Overturning Circulation. Nat. Clim. Chang. 7, 604–610 (2017).
    Article  Google Scholar 

    8.
    Stroeve, J., Holland, M. M., Meier, W., Scambos, T. & Serreze, M. Arctic sea ice decline: faster than forecast. Geophys. Res. Lett. 34, L09501 (2007).
    Article  Google Scholar 

    9.
    Routson, C. C. et al. Mid-latitude net precipitation decreased with Arctic warming during the Holocene. Nature 568, 83–87 (2019).
    CAS  Article  Google Scholar 

    10.
    Parkinson, C. L. & Cavalieri, D. J. Arctic sea ice variability and trends, 1979–2006. J. Geophys. Res. 113, C07003 (2008).
    Article  Google Scholar 

    11.
    Stroeve, J. C. et al. Trends in Arctic sea ice extent from CMIP5, CMIP3 and observations. Geophys. Res. Lett. 39, L16502 (2012).
    Article  Google Scholar 

    12.
    Matsumura, S. & Kosaka, Y. Arctic–Eurasian climate linkage induced by tropical ocean variability. Nat. Commun. 10, 1–8 (2019).
    CAS  Article  Google Scholar 

    13.
    Kaufman, D. S. et al. Holocene thermal maximum in the western Arctic (0-180°W). Quat. Sci. Rev. 23, 529–560 (2004).
    Article  Google Scholar 

    14.
    Holmes, R. M. et al. A circumpolar perspective on fluvial sediment flux to the Arctic ocean. Global Biogeochem. Cycles 16, 1098 (2002).
    Article  CAS  Google Scholar 

    15.
    Duk-Rodkin, A. & Hughes, O. L. Tertiary-quaternary drainage of the pre-glacial Mackenzie basin. Quat. Int. 22–23, 221–241 (1994).
    Article  Google Scholar 

    16.
    McManus, J. F., Francois, R., Gherardl, J. M., Keigwin, L. & Drown-Leger, S. Collapse and rapid resumption of Atlantic meridional circulation linked to deglacial climate changes. Nature 428, 834–837 (2004).
    CAS  Article  Google Scholar 

    17.
    Peltier, W. R., Vettoretti, G. & Stastna, M. Atlantic meridional overturning and climate response to Arctic Ocean freshening. Geophys. Res. Lett. 33, L06713 (2006).
    Google Scholar 

    18.
    Broecker, W. S. et al. Routing of meltwater from the Laurentide Ice Sheet during the Younger Dryas cold episode. Nature 341, 318–321 (1989).
    Article  Google Scholar 

    19.
    Keigwin, L. D. et al. Deglacial floods in the Beaufort Sea preceded Younger Dryas cooling. Nat. Geosci. 11, 599–604 (2018).
    CAS  Article  Google Scholar 

    20.
    Leydet, D. J. et al. Opening of glacial Lake Agassiz’s eastern outlets by the start of the Younger Dryas cold period. Geology 46, 155–158 (2018).
    CAS  Article  Google Scholar 

    21.
    Fisher, T. G. & Lowell, T. V. Testing northwest drainage from Lake Agassiz using extant ice margin and strandline data. Quat. Int. 260, 106–114 (2012).
    Article  Google Scholar 

    22.
    Tarasov, L. & Peltier, W. R. Arctic freshwater forcing of the Younger Dryas cold reversal. Nature 435, 662–665 (2005).
    CAS  Article  Google Scholar 

    23.
    Murton, J. B., Bateman, M. D., Dallimore, S. R., Teller, J. T. & Yang, Z. Identification of Younger Dryas outburst flood path from Lake Agassiz to the Arctic Ocean. Nature 464, 740–743 (2010).
    CAS  Article  Google Scholar 

    24.
    Fisher, T. G., Waterson, N., Lowell, T. V. & Hajdas, I. Deglaciation ages and meltwater routing in the Fort McMurray region, northeastern Alberta and northwestern Saskatchewan, Canada. Quat. Sci. Rev. 28, 1608–1624 (2009).
    Article  Google Scholar 

    25.
    Fisher, T. G., Smith, D. G. & Andrews, J. T. Preboreal oscillation caused by a glacial Lake Agassiz flood. Quat. Sci. Rev. 21, 873–878 (2002).
    Article  Google Scholar 

    26.
    Jin, Y. K. ARA04C cruise report: barrow, US—Beaufort Sea, CAN—Nome, US 6-24 September 2013 (Korea Polar Research Institute, Incheon, 2013).

    27.
    Gamboa, A., Montero-Serrano, J. -C., St-Onge, G., Rochon, A. & Desiage, P. -A. Mineralogical, geochemical, and magnetic signatures of surface sediments from the Canadian Beaufort Shelf and Amundsen Gulf (Canadian Arctic). Geochem. Geophys. Geosyst. 18, 488–512 (2017).
    CAS  Article  Google Scholar 

    28.
    Belt, S. T. et al. A novel chemical fossil of palaeo sea ice: IP25. Org. Geochem. 38, 16–27 (2007).
    CAS  Article  Google Scholar 

    29.
    Brown, T. A., Belt, S. T., Tatarek, A. & Mundy, C. J. Source identification of the Arctic sea ice proxy IP 25. Nat. Commun. 5, 4197 (2014).
    CAS  Article  Google Scholar 

    30.
    Müller, J. et al. Towards quantitative sea ice reconstructions in the northern North Atlantic: a combined biomarker and numerical modelling approach. Earth Planet. Sci. Lett. 306, 137–148 (2011).
    Article  CAS  Google Scholar 

    31.
    Smik, L., Cabedo-Sanz, P. & Belt, S. T. Semi-quantitative estimates of paleo Arctic sea ice concentration based on source-specific highly branched isoprenoid alkenes: A further development of the PIP25 index. Org. Geochem. 92, 63–69 (2016).
    CAS  Article  Google Scholar 

    32.
    Lü, X. et al. Hydroxylated isoprenoid GDGTs in Chinese coastal seas and their potential as a paleotemperature proxy for mid-to-low latitude marginal seas. Org. Geochem. 89, 31–43 (2015).
    Article  CAS  Google Scholar 

    33.
    Volkman, J. K. A review of sterol markers for marine and terrigenous organic matter. Org. Geochem. 9, 83–99 (1986).
    CAS  Article  Google Scholar 

    34.
    Fahl, K. & Stein, R. Biomarkers as organic-carbon-source and environmental indicators in the late quaternary Arctic Ocean: problems and perspectives. Mar. Chem. 63, 293–309 (1999).
    CAS  Article  Google Scholar 

    35.
    Fahl, K. & Stein, R. Modern seasonal variability and deglacial/Holocene change of central Arctic Ocean sea-ice cover: new insights from biomarker proxy records. Earth Planet. Sci. Lett. 351, 123–133 (2012).
    Article  CAS  Google Scholar 

    36.
    Rampen, S. W., Abbas, B. A., Schouten, S. & Damsté, J. S. S. A comprehensive study of sterols in marine diatoms (Bacillariophyta): implications for their use as tracers for diatom productivity. Limnol. Oceanogr. 55, 91–105 (2010).
    CAS  Article  Google Scholar 

    37.
    Hopmans, E. C. et al. A novel proxy for terrestrial organic matter in sediments based on branched and isoprenoid tetraether lipids. Earth Planet. Sci. Lett. 224, 107–116 (2004).
    CAS  Article  Google Scholar 

    38.
    Weijers, J. W. H., Schouten, S., van den Donker, J. C., Hopmans, E. C. & Sinninghe Damsté, J. S. Environmental controls on bacterial tetraether membrane lipid distribution in soils. Geochim. Cosmochim. Acta 71, 703–713 (2007).
    CAS  Article  Google Scholar 

    39.
    Blaga, C. I. et al. Branched glycerol dialkyl glycerol tetraethers in lake sediments: can they be used as temperature and pH proxies? Org. Geochem. 41, 1225–1234 (2010).
    CAS  Article  Google Scholar 

    40.
    De Jonge, C. et al. In situ produced branched glycerol dialkyl glycerol tetraethers in suspended particulate matter from the Yenisei River, Eastern Siberia. Geochim. Cosmochim. Acta 125, 476–491 (2014).
    Article  CAS  Google Scholar 

    41.
    Zhang, Z., Metzger, P. & Sachs, J. P. Co-occurrence of long chain diols, keto-ols, hydroxy acids and keto acids in recent sediments of Lake El Junco, Galápagos Islands. Org. Geochem. 42, 823–837 (2011).
    CAS  Article  Google Scholar 

    42.
    de Bar, M. W. et al. Constraints on the application of long chain diol proxies in the Iberian Atlantic margin. Org. Geochem. 101, 184–195 (2016).
    Article  CAS  Google Scholar 

    43.
    Lattaud, J. et al. The C32 alkane-1,15-diol as a proxy of late Quaternary riverine input in coastal margins. Clim. Past 13, 1049–1061 (2017).
    Article  Google Scholar 

    44.
    Lattaud, J. et al. The C32 alkane-1,15-diol as a tracer for riverine input in coastal seas. Geochim. Cosmochim. Acta 202, 146–158 (2017).
    CAS  Article  Google Scholar 

    45.
    Pico, T., Mitrovica, J. X. & Mix, A. C. Sea level fingerprinting of the Bering Strait flooding history detects the source of the Younger Dryas climate event. Sci. Adv. 6, eaay2935 (2020).
    CAS  Article  Google Scholar 

    46.
    Jakobsson, M. et al. Post-glacial flooding of the Bering Land Bridge dated to 11 cal ka BP based on new geophysical and sediment records. Clim. Past 13, 991–1005 (2017).
    Article  Google Scholar 

    47.
    Laskar, J. et al. A long-term numerical solution for the insolation quantities of the Earth. Astron. Astrophys. 428, 261–285 (2004).
    Article  Google Scholar 

    48.
    Niebauer, H. J. & Alexander, V. Oceanographic frontal structure and biological production at an ice edge. Cont. Shelf Res. 4, 367–388 (1985).
    Article  Google Scholar 

    49.
    Smith, W. O. & Nelson, D. M. Phytoplankton bloom produced by a receding ice edge in the Ross Sea: spatial coherence with the density field. Science. 227, 163–166 (1985).
    CAS  Article  Google Scholar 

    50.
    Ackley, S. F. & Sullivan, C. W. Physical controls on the development and characteristics of Antarctic sea ice biological communities-a review and synthesis. Deep Sea Res. I 41, 1583–1604 (1994).
    Article  Google Scholar 

    51.
    Strass, V. H. & Nöthig, E. M. Seasonal shifts in ice edge phytoplankton blooms in the Barents Sea related to the water column stability. Polar Biol. 16, 409–422 (1996).
    Article  Google Scholar 

    52.
    Collins, L. G. et al. Evaluating highly branched isoprenoid (HBI) biomarkers as a novel Antarctic sea-ice proxy in deep ocean glacial age sediments. Quat. Sci. Rev. 79, 87–98 (2013).
    Article  Google Scholar 

    53.
    Belt, S. T. et al. Identification of paleo Arctic winter sea ice limits and the marginal ice zone: optimised biomarker-based reconstructions of late Quaternary Arctic sea ice. Earth Planet. Sci. Lett. 431, 127–139 (2015).
    CAS  Article  Google Scholar 

    54.
    Smik, L., Belt, S. T., Lieser, J. L., Armand, L. K. & Leventer, A. Distributions of highly branched isoprenoid alkenes and other algal lipids in surface waters from East Antarctica: further insights for biomarker-based paleo sea-ice reconstruction. Org. Geochem. 95, 71–80 (2016).
    CAS  Article  Google Scholar 

    55.
    Ribeiro, S. et al. Sea ice and primary production proxies in surface sediments from a High Arctic Greenland fjord: spatial distribution and implications for palaeoenvironmental studies. Ambio 46, 106–118 (2017).
    CAS  Article  Google Scholar 

    56.
    Wagner, A., Lohmann, G. & Prange, M. Arctic river discharge trends since 7ka BP. Glob. Planet. Change 79, 48–60 (2011).
    Article  Google Scholar 

    57.
    North Greenland Ice Core Project Members. High resolution record of Northern Hemisphere climate extending into the last interglacial period. Nature 431, 147–151 (2004).
    Article  CAS  Google Scholar 

    58.
    Broecker, W. S. Was the Younger Dryas triggered by a flood? Science 312, 1146–1148 (2006).
    CAS  Article  Google Scholar 

    59.
    Not, C. & Hillaire-Marcel, C. Enhanced sea-ice export from the Arctic during the Younger Dryas. Nat. Commun. 3, 1–5 (2012).
    Article  CAS  Google Scholar 

    60.
    Fagel, N., Not, C., Gueibe, J., Mattielli, N. & Bazhenova, E. Late Quaternary evolution of sediment provenances in the Central Arctic Ocean: mineral assemblage, trace element composition and Nd and Pb isotope fingerprints of detrital fraction from the Northern Mendeleev Ridge. Quat. Sci. Rev. 92, 140–154 (2014).
    Article  Google Scholar 

    61.
    Scott, D. B., Schell, T., St-Onge, G., Rochon, A. & Blasco, S. Foraminiferal assemblage changes over the last 15,000 years on the Mackenzie-Beaufort Sea Slope and Amundsen Gulf, Canada: implications for past sea ice conditions. Paleoceanography 24, PA2219 (2009).
    Article  Google Scholar 

    62.
    Keigwin, L. D., Donnelly, J. P., Cook, M. S., Driscoll, N. W. & Brigham-Grette, J. Rapid sea-level rise and Holocene climate in the Chukchi Sea. Geology 34, 861–864 (2006).
    Article  Google Scholar 

    63.
    Hill, J. C. & Driscoll, N. W. Paleodrainage on the Chukchi shelf reveals sea level history and meltwater discharge. Mar. Geol. 254, 129–151 (2008).
    CAS  Article  Google Scholar 

    64.
    England, J. H. & Furze, M. F. A. New evidence from the western Canadian Arctic Archipelago for the resubmergence of Bering Strait. Quat. Res. 70, 60–67 (2008).
    CAS  Article  Google Scholar 

    65.
    Dyke, A. S. & Savelle, J. M. Holocene history of the Bering Sea bowhead whale (Balaena mysticetus) in its Beaufort Sea summer grounds off Southwestern Victoria Island, Western Canadian Arctic. Quat. Res. 55, 371–379 (2001).
    Article  Google Scholar 

    66.
    Dyke, A. S., Dale, J. E. & McNeely, R. N. Marine molluscs as indicators of environmental change in glaciated North America and greenland during the last 18 000 Years. Geogr. Phys. Quat. 50, 125–184 (1996).
    Google Scholar 

    67.
    Belt, S. T., Smik, L., Köseoglu, D., Knies, J. & Husum, K. A novel biomarker-based proxy for the spring phytoplankton bloom in Arctic and sub-arctic settings–HBI T25. Earth Planet. Sci. Lett. 523, 115703 (2019).
    CAS  Article  Google Scholar 

    68.
    Fietz, S., Huguet, C., Rueda, G., Hambach, B. & Rosell-Melé, A. Hydroxylated isoprenoidal GDGTs in the Nordic Seas. Mar. Chem. 152, 1–10 (2013).
    CAS  Article  Google Scholar 

    69.
    Klotsko, S., Driscoll, N. & Keigwin, L. Multiple meltwater discharge and ice rafting events recorded in the deglacial sediments along the Beaufort Margin, Arctic Ocean. Quat. Sci. Rev. 203, 185–208 (2019).
    Article  Google Scholar 

    70.
    Sachs, J. P. et al. An Arctic Ocean paleosalinity proxy from δ2H of palmitic acid provides evidence for deglacial Mackenzie River flood events. Quat. Sci. Rev. 198, 76–90 (2018).
    Article  Google Scholar 

    71.
    Spielhagen, R. F., Erlenkeuser, H. & Siegert, C. History of freshwater runoff across the Laptev Sea (Arctic) during the last deglaciation. Glob. Planet. Change 48, 187–207 (2005).
    Article  Google Scholar 

    72.
    Nørgaard-pedersen, N. et al. Arctic Ocean during the Last Glacial Maximum: Atlantic and polar domains of surface water mass distribution and ice cover. Paleoceanography 18, 1–19 (2003).
    Article  Google Scholar 

    73.
    Stein, R. et al. The last deglaciation event in the eastern central Arctic. Ocean Sci. 264, 692–696 (1994).
    CAS  Google Scholar 

    74.
    Poore, R. Z., Osterman, L., Hole, W. & Hole, W. Late Pleistocene and Holocene meltwater events in the western Arctic Ocean. Geology 27, 759–762 (1999).
    CAS  Article  Google Scholar 

    75.
    Stein, R., Fahl, K. & Müller, J. Proxy reconstruction of Cenozoic Arctic Ocean sea ice history–from IRD to IP25. Polarforschung 82, 37–71 (2012).
    Google Scholar 

    76.
    Häggi, C. et al. Modern and late Pleistocene particulate organic carbon transport by the Amazon River: Insights from long-chain alkyl diols. Geochim. Cosmochim. Acta 262, 1–19 (2019).
    Article  CAS  Google Scholar 

    77.
    Breckenridge, A. The Tintah-Campbell gap and implications for glacial Lake Agassiz drainage during the Younger Dryas cold interval. Quat. Sci. Rev. 117, 124–134 (2015).
    Article  Google Scholar 

    78.
    Praetorius, S. et al. The role of Northeast Pacific meltwater events in deglacial climate change. Sci. Adv. 6, eaay2915 (2020).
    Article  Google Scholar 

    79.
    Boden, P., Fairbanks, G., Wright, D. & Burckle, H. High-resolution stable isotope records from southwest Sweden: the drainage of the Baltic Ice Lake and Younger Dryas ice margin oscillations. Paleoceanography 12, 39–49 (1997).
    Article  Google Scholar 

    80.
    Schell, T. M., Scott, D. B., Rochon, A. & Blasco, S. Late quaternary paleoceanography and paleo-sea ice conditions in the Mackenzie Trough and Canyon, Beaufort Sea. Can. J. Earth Sci. 45, 1399–1415 (2008).
    Article  Google Scholar 

    81.
    Andrews, J. T. & Dunhill, G. Early to mid-Holocene Atlantic water influx and deglacial meltwater events, Beaufort Sea slope, Arctic Ocean. Quat. Res. 61, 14–21 (2004).
    CAS  Article  Google Scholar 

    82.
    Winterfeld, M. et al. Deglacial mobilization of pre-aged terrestrial carbon from degrading permafrost. Nat. Commun. 9, 3666 (2018).
    Article  CAS  Google Scholar 

    83.
    Meyer, V. D. et al. Permafrost-carbon mobilization in Beringia caused by deglacial meltwater runoff, sea-level rise and warming. Environ. Res. Lett. 14, 085003 (2019).
    CAS  Article  Google Scholar 

    84.
    Stein, R., Fahl, K., Dittmers, K., Nissen, F. & Stepanets, O. V. Holocene siliciclastic and organic carbon fluxes in the Oh and Yenisei estuaries and the adjacent inner Kara Sea: Quantification, variability, and paleoenvironmental implications. In Siberian River Run-off in the Kara Sea: Characterisation, Quantification, Variability and Environmental Significance 401–432 (Elsevier, Amsterdam, 2003).

    85.
    Stein, R. & Fahl, K. The Kara Sea: distribution, sources, variability and burial of organic carbon. in The Organic Carbon Cycle in the Arctic Ocean 213–237 (Springer-Verlag, Berlin, 2004). .

    86.
    Pearce, C. et al. Heinrich 0 on the east Canadian margin: source, distribution, and timing. Paleoceanography 30, 1613–1624 (2015).
    Article  Google Scholar 

    87.
    Blaauw, M. & Christeny, J. A. Flexible paleoclimate age-depth models using an autoregressive gamma process. Bayesian Anal 6, 457–474 (2011).
    Google Scholar 

    88.
    Blaauw, M. & Christen, J. A. Bacon Manual—v2.3.3 (2013).

    89.
    Reimer, P. J. et al. Intcal13 and Marine13 Radiocarbon Age Calibration Curves 0–50,000 Years Cal Bp. Radiocarbon 55, 1869–1887 (2013).
    CAS  Article  Google Scholar 

    90.
    Brown, T. A. & Belt, S. T. Novel tri- and tetra-unsaturated highly branched isoprenoid (HBI) alkenes from the marine diatom Pleurosigma intermedium. Org. Geochem. 91, 120–122 (2016).
    CAS  Article  Google Scholar 

    91.
    Boon, J. J. et al. Black Sea sterol—a molecular fossil for dinoflagellate blooms. Nature 277, 125–127 (1979).
    CAS  Article  Google Scholar 

    92.
    Versteegh, G., Bosch, H. & De Leeuw, J. Potential palaeoenvironmental information of C24 to C36 mid-chain diols, keto-ols and mid-chain hydroxy fatty acids; a critical review. Org. Geochem. 27, 1–13 (1997).
    CAS  Article  Google Scholar 

    93.
    Rampen, S. W. et al. Long chain 1,13- and 1,15-diols as a potential proxy for palaeotemperature reconstruction. Geochim. Cosmochim. Acta 84, 204–216 (2012).
    CAS  Article  Google Scholar 

    94.
    Stein, R. & Macdonald, R. W. The Organic Carbon Cycle in the Arctic Ocean (Springer-Verlag, Berlin, 2004).

    95.
    Wu, J. et al. Biomarker data of sediment core ARA04C/37, Beaufort Sea, Arctic Ocean. PANGAEA https://doi.org/10.1594/PANGAEA.915048 (2020).

    96.
    Peltier, W. R., Argus, D. F. & Drummond, R. Space geodesy constrains ice age terminal deglaciation: the global ICE-6G_C (VM5a) model. J. Geophys. Res. Solid Earth 120, 450–487 (2015).
    Article  Google Scholar  More

  • in

    Light environments affect herbivory patterns but not reproductive performance of a multivoltine specialist moth, Pareuchaetes pseudoinsulata

    1.
    Muth, N. Z., Kluger, E. C., Levy, J. H., Edwards, M. J. & Niesenbaum, R. A. Increased per capita herbivory in the shade: necessity, feedback, or luxury consumption?. Ecoscience 15, 182–188 (2008).
    Article  Google Scholar 
    2.
    Karolewski, P., Giertych, M. J., Żmuda, M., Jagodziński, A. M. & Oleksyn, J. Season and light affect constitutive defenses of understory shrub species against folivorous insects. Acta Oecol. 53, 19–32 (2013).
    ADS  Article  Google Scholar 

    3.
    Łukowski, A., Giertych, M. J., Zadworny, M., Mucha, J. & Karolewski, P. Preferential feeding and occupation of sunlit leaves favors defense response and development in the flea beetle, Altica brevicollis coryletorum: a pest of Corylus avellana. PLoS ONE 10(4), e0126072 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    4.
    Uyi, O. O., Zachariades, C., Heshula, L. U. & Hill, M. P. Developmental and reproductive performance of a specialist herbivore depend on seasonality of, and light conditions experienced by, the host plant. PLoS ONE 13(1), e0190700 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    5.
    Moore, L. V., Myers, J. H. & Eng, R. Western tent caterpillars prefer the sunny side of the tree but why?. Oikos 51, 321–326 (1988).
    Article  Google Scholar 

    6.
    Sipura, M. & Tahvanainen, J. Shading enhances the quality of willow leaves to leaf beetles: but does it matter?. Oikos 91, 550–558 (2000).
    Article  Google Scholar 

    7.
    Henriksson, J. et al. Effects of host shading on consumption and growth of the geometrid Epirrita autumnata: interactive roles of water, primary and secondary compounds. Oikos 103, 3–16 (2003).
    CAS  Article  Google Scholar 

    8.
    Diaz, R. et al. Differential performance of Tropical Soda Apple and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae) in open and shaded habitats. Environ. Entomol. 40, 1437–1447 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    9.
    Uyi, O. O., Uwagiahanor, B. I. & Ejomah, A. J. The nocturnal larvae of a specialist folivore prefer Chromolaena odorata (L.) foliage from a sunny environment, but does it matter?. Arthropod Plant Interact. 11, 603–611 (2017).
    Article  Google Scholar 

    10.
    Moran, P. J. & Showler, A. T. Plant responses to water deficit and shade stresses in pigweed and their influence on feeding and oviposition by the beet armyworm (Lepidoptera: Noctuidae). Environ. Entomol. 34, 929–937 (2005).
    Article  Google Scholar 

    11.
    Uyi, O. O., Zachariades, C., Hill, M. P. & Conlong, D. The nocturnal larvae of a specialist folivore perform better on Chromolaena odorata leaves from a shaded environment. Entomol. Exp. Appl. 156, 187–199 (2015).
    Article  Google Scholar 

    12.
    Bryant, J. P., Chapin, F. S. III. & Klein, D. R. Carbon: nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368 (1983).
    CAS  Article  Google Scholar 

    13.
    Bryant, J. P., Chapin, F. S. III., Reichardt, P. B. & Clausen, T. P. Response of winter chemical defence in Alaska paper birch and green alder to manipulation of plant carbon: nutrient balance. Oecologia 72, 510–514 (1987).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    14.
    Herms, D. A. & Mattson, W. J. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283–335 (1992).
    Article  Google Scholar 

    15.
    Barber, N. A. & Marquis, R. J. Light environment and impact of foliage quality on herbivorous insect attack and bird predation. Oecologia 166, 401–409 (2011).
    ADS  PubMed  Article  PubMed Central  Google Scholar 

    16.
    Barbehenn, R. V., Chen, Z., Karowe, D. N. & Spickard, A. C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2. Glob. Change Biol. 10, 1565–1575 (2004).
    ADS  Article  Google Scholar 

    17.
    Barbehenn, R. V., Karowe, D. N. & Spickard, A. Effects of elevated atmospheric CO2 on the nutritional ecology of C3 and C4 grass-feeding caterpillars. Oecologia 140, 86–95 (2004).
    ADS  PubMed  Article  PubMed Central  Google Scholar 

    18.
    Caswell, H., Reed, F. C., Stephenson, S. N. & Werner, P. Photosynthetic pathways and selective herbivory: a hypothesis. Am. Nat. 107, 465–480 (1973).
    CAS  Article  Google Scholar 

    19.
    Nokelainen, O., van Ripley, B. S., Bergen, E., Osborne, C. P. & Brakefield, P. M. Preference for C4 shade grasses increases hatchling performance in the butterfly, Bicyclus safitza. Ecol. Evol. 6, 5246–5255 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    20.
    Uyi, O. O. & Igbinosa, I. B. The status of Chromolaena odorata and its biocontrol in West Africa,in Zachariades, C., Strathie, L.W., Day, M.D. & Muniappan, R. (eds). Proceedings of the Eighth International Workshop on Biological Control and Management of Chromolaena odorataand other Eupatorieae, Nairobi, Kenya, 1–2 November 2010. Agricultural Research Council—Plant Protection Research Institute, Pretoria, South Africa, pp. 86–98 (2013).

    21.
    Uyi, O. O. et al. Chromolaena odorata invasion in Nigeria: a case for coordinated biological control. Manag. Biol. Invasions 5, 377–393 (2014).
    Article  Google Scholar 

    22.
    Zachariades, C., Day, M., Muniappan, R. & Reddy, G. V. P. Chromolaena odorata (L.) King and Robinson (Asteraceae). In Biological Control of Tropical Weeds Using Arthropods (eds Muniappan, R. et al.) 130–160 (Cambridge University Press, Cambridge, 2009).
    Google Scholar 

    23.
    Zhang, L. L. & Wen, D. Z. Structural and physiological responses of two invasive weeds, Mikania micrantha and Chromolaena odorata to contrasting light and soil water conditions. J. Plant. Res. 122, 69–79 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    24.
    Muniappan, R., Sundaramurthy, V. T. & Virktamath, C. A. Distribution of Chromolaena odorata (Asteraceae) and bionomics and utilization of food by Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae) in India, in: Delfosse, E. S. (ed) Proceedings of the Seventh International Symposium on Biological Control of Weeds, 6–11 March, 1988, Rome, Italy, pp 401–409 (1989).

    25.
    Cruttwell, R. E. The insects of Eupatorium odoratum L. in Trinidad and their potential as agents for biological control. PhD Dissertation, University of the West Indies, Trinidad (1972).

    26.
    Cock, M. W. J. & Holloway, J. D. The history of, and prospects for, the biological control of Chromolaena odorata (Compositae) by Pareuchaetes pseudoinsulata Rego Barros and allies (Lepidoptera, Arctiidae). Bull. Entomol. Res. 72, 193–205 (1982).
    Article  Google Scholar 

    27.
    Uyi, O., Egbon, I. N. & Igbinosa, I. B. Discovery of, and studies on Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae) in southern Nigeria. Int. J. Trop. Insect Sci. 31, 199–203 (2011).
    Article  Google Scholar 

    28.
    Seibert, T. F. Biological control of the weed, Chromolaena odorata (Asteraceae) by Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae) in Guam and the Northern Mariana Islands. Entomophaga 35, 531–539 (1989).
    Article  Google Scholar 

    29.
    Braimah, H., Ekyem, S.O., Issah, U.S. & Mochiah, M. Social perceptions and ecological impacts following biological control of Chromolaena odorataby Pareuchaetes pseudoinsulatain the forest region of Ghana, in: Zachariades, C., Strathie, L. W., Day, M. D. & Muniappan, R. (eds) Proceedings of the Eighth International Workshop on Biological Control and Management of Chromolaena odorataand other Eupatorieae, Nairobi, Kenya, 1–2 November 2010.Agricultural Research Council—Plant Protection Research Institute, Pretoria, South Africa pp. 110–116 (2013).

    30.
    Olckers, T. & Hulley, P. E. Host specificity tests on leaf-feeding insects: aberrations from the use of excised leaves. African Entomol. 2, 68–70 (1994).
    Google Scholar 

    31.
    Blossey, B. & Nötzold, R. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83, 887–889 (1995).
    Article  Google Scholar 

    32.
    Friberg, M. & Wiklund, C. Butterflies and plants: preference/performance studies in relation to plant size and the use of intact plants vs. cuttings. Entomol. Exp. Appl. 160, 201–208 (2016).
    CAS  Article  Google Scholar 

    33.
    Uyi, O. O., Hill, M. P. & Zachariades, C. Variation in host plant has no effect on the performance and fitness-related traits of the specialist herbivore, Pareuchaetes insulata. Entomol. Exp. Appl. 153, 64–75 (2014).
    Article  Google Scholar 

    34.
    Bakr, E. M. A new software for measuring leaf area, and area damaged by Tetranychus urticae Koch. J. Appl. Entomol. 129, 173–175 (2005).
    Article  Google Scholar 

    35.
    implications for insect defoliation. Steinbauer, M.J. Specific leaf weight as an indicator of juvenile leaf toughness in Tasmanian bluegum (Eucalyptus globulus ssp. globulus). Austral. For. 64, 32–37 (2001).
    Article  Google Scholar 

    36.
    Watanabe, F. S. & Olsen, S. R. Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci. Soc. Am. Proc. 29, 677–678 (1965).
    ADS  CAS  Article  Google Scholar 

    37.
    Marais, J. P. Evaluation of acid hydrolysis procedures for the rapid determination of total non-structural carbohydrates in plant species. Agrochemophysica 11, 1–3 (1979).
    CAS  Google Scholar 

    38.
    Lockett, C. J., Dhileepan, K., Robinson, M. & Pukallus, K. J. Impact of a biological control agent, Chiasmia assimilis, on prickly acacia (Acacia nilotica ssp. indica) seedlings. Biol. Control 62, 183–188 (2012).
    Article  Google Scholar 

    39.
    Mäntylä, E., Klemola, T., Sirkiä, P. & Laaksonen, T. Low light reflectance may explain the attraction of birds to defoliated trees. Behav. Ecol. 19, 325–330 (2008).
    Article  Google Scholar 

    40.
    Uyi, O. O., Zachariades, C. & Hill, M. P. The life history traits of the arctiine moth Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. Afr. Entomol. 22, 611–624 (2014).
    Article  Google Scholar 

    41.
    Awmack, C. S. & Leather, S. R. Host plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47, 817–844 (2002).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    42.
    Łukowski, A., Giertych, M. J., Walczak, U., Baraniak, E. & Karolewski, P. Light conditions affect the performance of Yponomeuta evonymellus on its native host Prunus padus and the alien Prunus serotina. Bull. Entomol. Res. 107, 208–216 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    43.
    Behmer, S. T. Insect herbivore nutrient regulation. Annu. Rev. Entomol. 54, 165–187 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    44.
    Simpson, S. J. & Raubenheimer, D. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity (Princeton University Press, Princeton, 2012).
    Google Scholar 

    45.
    Lee, K. P., Cory, J. S., Wilson, K., Raubenheimer, D. & Simpson, S. J. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. Lond. B 273, 823–829 (2006).
    CAS  Google Scholar 

    46.
    Clissold, F. J. The biomechanics of chewing and plant fracture: mechanisms and implications. Adv. Insect Physiol. 34, 317–372 (2007).
    Article  Google Scholar 

    47.
    Raubenheimer, A. D., Lee, K. P. & Simpson, S. J. Does Bertrand’s rule apply to macronutrients?. Proc. R. Soc. B 272, 2429–2434 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    48.
    Boersma, M. & Elser, J. J. Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87, 1325–1330 (2006).
    PubMed  Article  PubMed Central  Google Scholar 

    49.
    Zehnder, C. & Hunter, M. D. More is not necessarily better: the impact of limiting and excessive nutrients on herbivore population growth rates. Ecol. Entomol. 34, 535–543 (2009).
    Article  Google Scholar 

    50.
    Lee, K. P., Behmer, S. T., Simpson, S. J. & Raubenheimer, D. A geometric analysis of nutrient regulation in the generalist caterpillar, Spodoptera littoralis (Boisduval). J. Insect Physiol. 48, 655–665 (2002).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    51.
    Clissold, F. J., Sanson, G. D. & Read, J. The paradoxical effects of nutrient ratios and supply rates on an outbreaking insect herbivore, the Australian plague locust. J. Anim. Ecol. 75, 1000–1013 (2006).
    CAS  PubMed  Article  PubMed Central  Google Scholar  More

  • in

    Daily mapping of Australian Plague Locust abundance

    1.
    Stige, L. C., Chan, K.-S., Zhang, Z., Frank, D. & Stenseth, N. C. Thousand-year-long Chinese time series reveals climatic forcing of decadal locust dynamics. Proc. Natl. Acad. Sci. 104, 16188–16193 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 
    2.
    Walker, F. Catalogue of the Specimens of Dermaptera Saltatoria in Collection of the British Museum. Part III. 485–594 (British Museum (Natural History), 1870).

    3.
    Wright, D. E. Analysis of the development of major plagues of the Australian plague locust Chortoicetes terminifera (Walker) using a simulation model. Aust. J. Ecol. 12, 423–437 (1987).
    Article  Google Scholar 

    4.
    Deveson, E. D. & Walker, P. W. Not a one-way trip: Historical distribution data for Australian plague locusts support frequent seasonal exchange migrations. J. Orthoptera Res. 14, 91–105 (2005).
    Article  Google Scholar 

    5.
    Wang, H. Quantitative assessment of Australian plague locust habitats in the inland of eastern Australia using RS and GIS technologies in Remote Sensing for Agriculture, Ecosystems, and Hydrology XVI vol. 9239 92390D (International Society for Optics and Photonics, 2014).

    6.
    Chapuis, M.-P. et al. Challenges to assessing connectivity between massive populations of the Australian plague locust. Proc. R. Soc. B Biol. Sci. 278, 3152–3160 (2011).
    Article  Google Scholar 

    7.
    Murray, D. A. H., Clarke, M. B. & Ronning, D. A. Estimating invertebrate pest losses in six major Australian grain crops. Aust. J. Entomol. 52, 227–241 (2013).
    Article  Google Scholar 

    8.
    Zhang, L., Lecoq, M., Latchininsky, A. & Hunter, D. Locust and grasshopper management. Annu. Rev. Entomol. 64, 15–34 (2019).
    CAS  PubMed  Article  Google Scholar 

    9.
    Adriaansen, C., Woodman, J., Deveson, E. & Drake, V. The Australian Plague Locust: risk and response. Environ. Hazards Risks Disasters Biol https://doi.org/10.1016/B978-0-12-394847-2.00005-X (2016).
    Article  Google Scholar 

    10.
    Farrow, R. A. & Longstaff, B. C. Comparison of the annual rates of increase of locusts in relation to the incidence of plagues. Oikos 2, 207–222 (1986).
    Article  Google Scholar 

    11.
    Wardhaugh, K. G. The effects of temperature and moisture on the inception of diapause in eggs of the Australian plague locust, Chortoicetes terminifera Walker (Orthoptera: Acrididae). Aust. J. Ecol. 5, 187–191 (1980).
    Article  Google Scholar 

    12.
    Wardhaugh, K. G. Diapause strategies in the Australian plague locust (Chortoicetes terminifera Walker). In The evolution of insect life cycles 89–104 (Springer, Berlin, 1986).
    Google Scholar 

    13.
    Clark, D. P. Flights after sunset by the Australian plague locust, Chortoicetes terminifera (Walker) and their significance in dispersal and migration. Aust. J. Zool. 19, 159–176 (1971).
    Article  Google Scholar 

    14.
    Farrow, R. A. Origin and decline of the 1973 plague locust outbreak in central western New South Wales. Aust. J. Zool. 25, 455–489 (1977).
    Article  Google Scholar 

    15.
    Wang, B. et al. Future climate change likely to reduce the Australian plague locust (Chortoicetes terminifera) seasonal outbreaks. Sci. Total Environ. 668, 947–957 (2019).
    ADS  CAS  PubMed  Article  Google Scholar 

    16.
    Veran, S. et al. Modeling spatiotemporal dynamics of outbreaking species: influence of environment and migration in a locust. Ecology 96, 737–748 (2015).
    PubMed  Article  Google Scholar 

    17.
    Maywald, G., Kriticos, D., Sutherst, R. & Bottomley, W. DYMEX model builder version 3: user’s guide. (2007).

    18.
    Meynard, C. N. et al. Climate-driven geographic distribution of the desert locust during recession periods: Subspecies’ niche differentiation and relative risks under scenarios of climate change. Glob. Change Biol. 23, 4739–4749 (2017).
    ADS  Article  Google Scholar 

    19.
    Piou, C. et al. Coupling historical prospection data and a remotely-sensed vegetation index for the preventative control of Desert locusts. Basic Appl. Ecol. 14, 593–604 (2013).
    Article  Google Scholar 

    20.
    Tratalos, J. A., Cheke, R. A., Healey, R. G. & Stenseth, N. C. Desert locust populations, rainfall and climate change: Insights from phenomenological models using gridded monthly data. Clim. Res. 43, 229–239 (2010).
    Article  Google Scholar 

    21.
    Tian, H. et al. Reconstruction of a 1,910-y-long locust series reveals consistent associations with climate fluctuations in China. Proc. Natl. Acad. Sci. 108, 14521–14526 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    22.
    Ehrlén, J. & Morris, W. F. Predicting changes in the distribution and abundance of species under environmental change. Ecol. Lett. 18, 303–314 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    23.
    Croft, S., Chauvenet, A. L. & Smith, G. C. A systematic approach to estimate the distribution and total abundance of British mammals. PLoS ONE 12, e0176339 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    24.
    Woodman, J. D. High-temperature survival is limited by food availability in first-instar locust nymphs. Aust. J. Zool. 58, 323–330 (2011).
    Article  Google Scholar 

    25.
    Guisan, A., Edwards, T. C. & Hastie, T. Generalized linear and generalized additive models in studies of species distributions: Setting the scene. Ecol. Model. 157, 89–100 (2002).
    Article  Google Scholar 

    26.
    Yee, T. W. & Mitchell, N. D. Generalized additive models in plant ecology. J. Veg. Sci. 2, 587–602 (1991).
    Article  Google Scholar 

    27.
    Bučas, M. et al. Empirical modelling of benthic species distribution, abundance, and diversity in the Baltic Sea: Evaluating the scope for predictive mapping using different modelling approaches. ICES J. Mar. Sci. 70, 1233–1243 (2013).
    Article  Google Scholar 

    28.
    Heersink, D. K. et al. Statistical modeling of a larval mosquito population distribution and abundance in residential Brisbane. J. Pest Sci. 89, 267–279 (2016).
    Article  Google Scholar 

    29.
    Jeffrey, S. J., Carter, J. O., Moodie, K. B. & Beswick, A. R. Using spatial interpolation to construct a comprehensive archive of Australian climate data. Environ. Model. Softw. 16, 309–330 (2001).
    Article  Google Scholar 

    30.
    Tozer, C. R., Kiem, A. S. & Verdon-Kidd, D. C. On the uncertainties associated with using gridded rainfall data as a proxy for observed. Hydrol. Earth Syst. Sci. 16, 1481–1499 (2012).
    ADS  Article  Google Scholar 

    31.
    Gregg, P. Development of the Australian Plague Locust, Chortoicetes terminifera, in relation to weather I. Effects of constant temperature and humidity. Aust. J. Entomol. 22, 247–251 (1983).
    Article  Google Scholar 

    32.
    Pruess, K. P. Day-degree methods for pest management. Environ. Entomol. 12, 613–619 (1983).
    Article  Google Scholar 

    33.
    McVicar, T. R., Briggs, P. R., King, E. A. & Raupach, M. R. A review of predictive modelling from a natural resource management perspective: the role of remote sensing of the terrestrial environment (CSIRO Land and Water CSIRO Earth Observation Centre, Canberra, 2003).
    Google Scholar 

    34.
    Grundy, M. J. et al. Soil and landscape grid of Australia. Soil Res. 53, 835–844 (2015).
    Article  Google Scholar 

    35.
    Cressie, N. & Wikle, C. K. Statistics for spatio-temporal data (John Wiley & Sons, New York, 2015).
    Google Scholar 

    36.
    James, G., Witten, D., Hastie, T. & Tibshirani, R. An introduction to statistical learning (Springer, Berlin, 2013).
    Google Scholar 

    37.
    Nelder, J. A. & Wedderburn, R. W. Generalized linear models. J. R. Stat. Soc. Ser. Gen. 135, 370–384 (1972).
    Article  Google Scholar 

    38.
    Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    39.
    Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S (Springer-Verlag, Berlin, 2002). https://doi.org/10.1007/978-0-387-21706-2.
    Google Scholar 

    40.
    Wood, S. N., Goude, Y. & Shaw, S. Generalized additive models for large data sets. J. R. Stat. Soc. Ser. C Appl. Stat. 64, 139–155 (2015).
    MathSciNet  Article  Google Scholar 

    41.
    Clark, D. P. The influence of rainfall on the densities of adult Chortoicetes terminifera (Walker) in central western New South Wales, 1965–73. Aust. J. Zool. 22, 365–386 (1974).
    Article  Google Scholar 

    42.
    Shelford, V. E. The ecology of North America. Ecol. N. Am. 2, 2 (1963).
    Google Scholar 

    43.
    Deveson, E. D. Satellite normalized difference vegetation index data used in managing Australian plague locusts. J. Appl. Remote Sens. 7, 075096 (2013).
    ADS  Article  Google Scholar 

    44.
    Kuhnert, P. M. & Lucchesi, L. Vizumap: An R package for visualizing uncertainty in spatial data (Zenodo, Boca Raton, 2018). https://doi.org/10.5281/zenodo.1479951.
    Google Scholar 

    45.
    Lucchesi, L. R. & Wikle, C. K. Visualizing uncertainty in areal data with bivariate choropleth maps, map pixelation and glyph rotation. Stat 6, 292–302 (2017).
    MathSciNet  Article  Google Scholar 

    46.
    Benfekih, L., Chara, B. & Doumandji-Mitiche, B. Influence of anthropogenic impact on the habitats and swarming risks of Dociostaurus maroccanus and Locusta migratoria (Orthoptera, Acrididae) in the Algerian Sahara and the semi-arid zone. J. Orthoptera Res. 11, 243–250 (2002).
    Article  Google Scholar 

    47.
    Štrumbelj, E. & Kononenko, I. Explaining prediction models and individual predictions with feature contributions. Knowl. Inf. Syst. 41, 647–665 (2014).
    Article  Google Scholar 

    48.
    Escorihuela, M. J. et al. SMOS based high resolution soil moisture estimates for desert locust preventive management. Remote Sens. Appl. Soc. Environ. 11, 140–150 (2018).
    Google Scholar 

    49.
    Myneni, R. B. & Williams, D. L. On the relationship between FAPAR and NDVI. Remote Sens. Environ. 49, 200–211 (1994).
    ADS  Article  Google Scholar 

    50.
    Hu, G. et al. Long-term seasonal forecasting of a major migrant insect pest: the brown planthopper in the Lower Yangtze River Valley. J. Pest Sci. 92, 417–428 (2019).
    Article  Google Scholar  More

  • in

    Combined pigment and metatranscriptomic analysis reveals highly synchronized diel patterns of phenotypic light response across domains in the open oligotrophic ocean

    1.
    Eberhard S, Finazzi G, Wollman F-A. The dynamics of photosynthesis. Annu Rev Genet. 2008;42:463–515.
    CAS  PubMed  Article  PubMed Central  Google Scholar 
    2.
    Dubinsky Z, Stambler N. Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications. Aquat Micro Ecol. 2009;56:163–76.
    Article  Google Scholar 

    3.
    Wright SW, Jeffrey SW. Pigment markers for phytoplankton production. In: Volkman JK (ed). Marine organic matter: biomarkers, isotopes and DNA. Berlin, Heidelberg: Springer Berlin Heidelberg; 2006. p. 71–104.

    4.
    Armstrong GA. Eubacteria show their true colors: genetics of carotenoid pigment biosynthesis from microbes to plants. J Bacteriol. 1994;176:4795–802.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    5.
    Ottesen EA, Young CR, Eppley JM, Ryan JP, Chavez FP, Scholin CA, et al. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc Natl Acad Sci USA. 2013;110:E488–97.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Ottesen EA, Young CR, Gifford SM, Eppley JM, Marin R, Schuster SC, et al. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science. 2014;345:207–12.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    7.
    Aylward FO, Eppley JM, Smith JM, Chavez FP, Scholin CA, DeLong EF. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc Natl Acad Sci USA. 2015;112:5443–8.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    8.
    Kolody BC, McCrow JP, Allen LZ, Aylward FO, Fontanez KM, Moustafa A, et al. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. ISME J. 2019;13:2817–33.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Neveux J, Dupouy C, Blanchot J, Le Bouteiller A, Landry MR, Brown SL. Diel dynamics of chlorophylls in high-nutrient, low-chlorophyll waters of the equatorial Pacific (180°): interactions of growth, grazing, physiological responses, and mixing. J Geophys Res Ocean. 2003;108:8140. https://doi.org/10.1029/2000JC000747.

    10.
    Le Bouteiller A, Herbland A. Diel variation of chlorophyll a as evidence from a 13-day station in the equatorial Atlantic ocean. Oceano Acta. 1982;5:433–41.
    Google Scholar 

    11.
    Litchman E. Resource Competition and the ecological success of phytoplankton. In: Falkowski PG, Knoll AH (eds). Evolution of primary producers in the sea. Burlington: Academic Press; 2007. p. 351–75.

    12.
    Graff JR, Behrenfeld MJ. Photoacclimation responses in subarctic atlantic phytoplankton following a natural mixing-restratification event. Front Mar Sci. 2018;5:209.
    Article  Google Scholar 

    13.
    Behrenfeld MJ, Boss E, Siegel DA, Shea DM. Carbon-based ocean productivity and phytoplankton physiology from space. Global Biogeochem Cycles. 2005;19:GB1006. https://doi.org/10.1029/2004GB002299.

    14.
    Tomkins M, Martin AP, Nurser AJG, Anderson TR. Phytoplankton acclimation to changing light intensity in a turbulent mixed layer: a Lagrangian modelling study. Ecol Model. 2020;417:108917.
    CAS  Article  Google Scholar 

    15.
    Wilson ST, Aylward FO, Ribalet F, Barone B, Casey JR, Connell PE, et al. Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera. Nat Microbiol. 2017;2:17118.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    16.
    Emerson S, Quay P, Karl D, Winn C, Tupas L, Landry M. Experimental determination of the organic carbon flux from open-ocean surface waters. Nature. 1997;389:951–4.
    CAS  Article  Google Scholar 

    17.
    Sarmiento JL, Slater R, Barber R, Bopp L, Doney SC, Hirst AC, et al. Response of ocean ecosystems to climate warming. Glob Biogeochem Cycles. 2004;18:GB3003.
    Article  CAS  Google Scholar 

    18.
    Popendorf KJ, Fredricks HF, Van, Mooy BAS. Molecular ion-independent quantification of polar glycerolipid classes in marine plankton using triple quadrupole MS. Lipids. 2013;48:185–95.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    19.
    Becker KW, Collins JR, Durham BP, Groussman RD, White AE, Fredricks HF, et al. Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean. Nat Commun. 2018;9:5179.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    20.
    Collins JR, Edwards BR, Fredricks HF, Van Mooy BAS. LOBSTAHS: an adduct-based lipidomics strategy for discovery and identification of oxidative stress biomarkers. Anal Chem. 2016;88:7154–62.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    21.
    Hummel J, Segu S, Li Y, Irgang S, Jueppner J, Giavalisco P. Ultra performance liquid chromatography and high resolution mass spectrometry for the analysis of plant lipids. Front Plant Sci. 2011;2:54.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    22.
    Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem. 2006;78:779–87.
    CAS  Article  Google Scholar 

    23.
    Kuhl C, Tautenhahn R, Böttcher C, Larson TR, Neumann S. CAMERA: an integrated strategy for compound spectra extraction and annotation of LC/MS data sets. Anal Chem. 2012;84:283–9.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    24.
    Harke MJ, Frischkorn KR, Haley ST, Aylward FO, Zehr JP, Dyhrman ST. Periodic and coordinated gene expression between a diazotroph and its diatom host. ISME J. 2019;13:118–31.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    25.
    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    26.
    Alexander H, Rouco M, Haley ST, Wilson ST, Karl DM, Dyhrman ST. Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean. Proc Natl Acad Sci USA. 2015;112:E5972–9.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    27.
    Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The marine microbial eukaryote transcriptome sequencing project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12:e1001889.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    28.
    Meinicke P. UProC: tools for ultra-fast protein domain classification. Bioinformatics. 2014;31:1382–8.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    29.
    Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics. 2010;26:589–95.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    30.
    Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014;31:166–9.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    31.
    Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    32.
    Aylward FO, Boeuf D, Mende DR, Wood-Charlson EM, Vislova A, Eppley JM, et al. Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone. Proc Natl Acad Sci USA. 2017;114:11446 LP–11451.
    Article  CAS  Google Scholar 

    33.
    Gifford SM, Becker JW, Sosa OA, Repeta DJ, DeLong EF. Quantitative transcriptomics reveals the growth- and nutrient-dependent response of a streamlined marine methylotroph to methanol and naturally occurring dissolved organic matter. MBio. 2016;7:e01279–16.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    34.
    Mende DR, Bryant JA, Aylward FO, Eppley JM, Nielsen T, Karl DM, et al. Environmental drivers of a microbial genomic transition zone in the ocean’s interior. Nat Microbiol. 2017;2:1367–73.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Kiełbasa SM, Wan R, Sato K, Horton P, Frith MC. Adaptive seeds tame genomic sequence comparison. Genome Res. 2011;21:487–93.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    36.
    Thaben PF, Westermark PO. Detecting rhythms in time series with RAIN. J Biol Rhythms. 2014;29:391–400.
    PubMed  PubMed Central  Article  Google Scholar 

    37.
    Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289–300.
    Google Scholar 

    38.
    Coenen AR, Hu SK, Luo E, Muratore D, Weitz JS. A primer for microbiome time-series analysis. Front Genet. 2020;11:310.
    PubMed  PubMed Central  Article  Google Scholar 

    39.
    Fuhrman JA, Eppley RW, Hagström Å, Azam F. Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern California Bight. Mar Ecol Prog Ser. 1985;27:9–20.
    Article  Google Scholar 

    40.
    Behrenfeld MJ, Falkowski PG. A consumer’s guide to phytoplankton primary productivity models. Limnol Oceanogr. 1997;42:1479–91.
    Article  Google Scholar 

    41.
    Post AF, Dubinsky Z, Wyman K, Falkowski PG. Kinetics of light-intensity adaptation in a marine planktonic diatom. Mar Biol. 1984;83:231–8.
    Article  Google Scholar 

    42.
    Falkowski PG, Kolber Z. Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Funct Plant Biol. 1995;22:341–55.
    Article  Google Scholar 

    43.
    Vaulot D, Marie D. Diel variability of photosynthetic picoplankton in the equatorial Pacific. J Geophys Res Ocean. 1999;104:3297–310.
    CAS  Article  Google Scholar 

    44.
    Nicholson DP, Wilson ST, Doney SC, Karl DM. Quantifying subtropical North Pacific gyre mixed layer primary productivity from Seaglider observations of diel oxygen cycles. Geophys Res Lett. 2015;42:4032–9.
    CAS  Article  Google Scholar 

    45.
    Yentsch CS. Distribution of chlorophyll and phaeophytin in the open ocean. Deep Sea Res Oceanogr Abstr. 1965;12:653–66.
    Article  Google Scholar 

    46.
    Yentsch CS, Reichert CA. The effects of prolonged darkness on photosynthesis, respiration, and chlorophyll in the marine flagellate Dunaliella euchlora. Limnol Oceanogr. 1963;8:338–42.
    Article  Google Scholar 

    47.
    Glooschenko WA, Curl H Jr., Small LF. Diel periodicity of chlorophyll a concentration in Oregon coastal waters. J Fish Res Board Can. 1972;29:1253–9.
    CAS  Article  Google Scholar 

    48.
    Cosper E. Influence of light intensity on diel variations in rates of growth, respiration and organic release of a marine diatom: comparison of diurnally constant and fluctuating light. J Plankton Res. 1982;4:705–24.
    Article  Google Scholar 

    49.
    Fouilland E, Courties C, Descolas-Gros C. Size-fractionated phytoplankton carboxylase activities in the Indian sector of the Southern Ocean. J Plankton Res. 2000;22:1185–201.
    CAS  Article  Google Scholar 

    50.
    Ragni M, d’Alcalà MR. Circadian variability in the photobiology of Phaeodactylum tricornutum: pigment content. J Plankton Res. 2007;29:141–56.
    CAS  Article  Google Scholar 

    51.
    Bidigare RR, Buttler FR, Christensen SJ, Barone B, Karl DM, Wilson ST. Evaluation of the utility of xanthophyll cycle pigment dynamics for assessing upper ocean mixing processes at Station ALOHA. J Plankton Res. 2014;36:1423–33.
    CAS  Article  Google Scholar 

    52.
    Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In Methods in Enzymology (vol 148). Academic Press; 1987. p. 350–82.

    53.
    Salomon E, Bar-Eyal L, Sharon S, Keren N. Balancing photosynthetic electron flow is critical for cyanobacterial acclimation to nitrogen limitation. Biochim Biophys Acta. 2013;1827:340–7.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    54.
    Ünlü C, Drop B, Croce R, van Amerongen H. State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc Natl Acad Sci USA. 2014;111:3460–5.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    55.
    MacIntyre HL, Kana TM, Anning T, Geider RJ. Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol. 2002;38:17–38.
    Article  Google Scholar 

    56.
    Karl DM, Church MJ. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat Rev Microbiol. 2014;12:699–713.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    57.
    Armstrong GA. Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. J Photochem Photobio B Biol. 1998;43:87–100.
    CAS  Article  Google Scholar 

    58.
    Foy RH, Smith RV. The role of carbohydrate accumulation in the growth of planktonic Oscillatoria species. Br Phycol J. 1980;15:139–50.
    Article  Google Scholar 

    59.
    Cuhel RL, Ortner PB, Lean DRS. Night synthesis of protein by algae. Limnol Oceanogr. 1984;29:731–44.
    CAS  Article  Google Scholar 

    60.
    Lacour T, Sciandra A, Talec A, Mayzaud P, Bernard O. Diel variations of carbohydrates and neutral lipids in nitrogen‐sufficient and nitrogen‐starved cyclostat cultures of Isochrysis sp. 1. J Phycol. 2012;48:966–75.
    PubMed  Article  PubMed Central  Google Scholar 

    61.
    Lorenzen CJ. A note on the chlorophyll and phaeophytin content of the chlorophyll maximum. Limnol Oceanogr. 1965;10:482–3.
    Article  Google Scholar 

    62.
    Jeffrey SW. Profiles of photosynthetic pigments in the ocean using thin-layer chromatography. Mar Biol. 1974;26:101–10.
    CAS  Article  Google Scholar 

    63.
    Head EJH, Horne EPW. Pigment transformation and vertical flux in an area of convergence in the North Atlantic. Deep Sea Res Part II Top Stud Oceanogr. 1993;40:329–46.
    Article  Google Scholar 

    64.
    Sun M-Y, Lee C, Aller RC. Anoxic and oxic degradation of 14C-labeled chloropigments and a 14C-labeled diatom in Long Island Sound sediments. Limnol Oceanogr. 1993;38:1438–51.
    CAS  Article  Google Scholar 

    65.
    Champalbert G, Neveux J, Gaudy R, Le Borgne R. Diel variations of copepod feeding and grazing impact in the high-nutrient, low-chlorophyll zone of the equatorial Pacific Ocean (0°; 3° S, 180°). J Geophys Res Ocean. 2003;108:8145. https://doi.org/10.1029/2001JC000810.

    66.
    Holzwarth AR, Müller MG, Reus M, Nowaczyk M, Sander J, Rögner M. Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA. 2006;103:6895–6900.
    CAS  Article  Google Scholar 

    67.
    van Grondelle R, Dekker JP, Gillbro T, Sundstrom V. Energy transfer and trapping in photosynthesis. Biochim Biophys Acta. 1994;1187:1–65.
    CAS  Article  Google Scholar 

    68.
    Shimoda Y, Ito H, Tanaka A. Arabidopsis STAY-GREEN, Mendel’s green cotyledon gene, encodes magnesium-dechelatase. Plant Cell. 2016;28:2147–60.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    69.
    Oster U, Tanaka R, Tanaka A, Rüdiger W. Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J. 2000;21:305–10.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    70.
    Vavilin D, Vermaas W. Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. Biochim Biophys Acta. 2007;1767:920–9.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    71.
    Pružinská A, Tanner G, Anders I, Roca M, Hörtensteiner S. Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron–sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci USA. 2003;100:15259–64.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    72.
    Baroli I, Niyogi KK. Molecular genetics of xanthophyll–dependent photoprotection in green algae and plants. Philos Trans R Soc Lond Ser B Biol Sci. 2000;355:1385–94.
    CAS  Article  Google Scholar 

    73.
    Andersen RA, Bidigare RR, Keller MD, Latasa M. A comparison of HPLC pigment signatures and electron microscopic observations for oligotrophic waters of the North Atlantic and Pacific Oceans. Deep Sea Res Part II Top Stud Oceanogr. 1996;43:517–37.
    CAS  Article  Google Scholar 

    74.
    Obata M, Taguchi S. The xanthophyll-cycling pigment dynamics of Isochrysis galbana (Prymnesiophyceae) during light-dark transition. Plankt Benthos Res. 2012;7:101–10.
    Article  Google Scholar 

    75.
    Sajilata MG, Singhal RS, Kamat MY. The carotenoid pigment zeaxanthin—a review. Compr Rev Food Sci Food Saf. 2008;7:29–49.
    CAS  Article  Google Scholar 

    76.
    Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylidès C, Havaux M. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA. 2012;109:5535–40.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    77.
    Goss R. Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta. 2003;217:801–12.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    78.
    Viviani DA, Karl DM, Church MJ. Variability in photosynthetic production of dissolved and particulate organic carbon in the North Pacific Subtropical Gyre. Front Mar Sci. 2015;2:73.
    Article  Google Scholar 

    79.
    Elling FJ, Becker KW, Könneke M, Schröder JM, Kellermann MY, Thomm M, et al. Respiratory quinones in Archaea: phylogenetic distribution and application as biomarkers in the marine environment. Environ Microbiol. 2016;18:692–707.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    80.
    Becker KW, Elling FJ, Schröder JM, Lipp JS, Goldhammer T, Zabel M, et al. Isoprenoid quinones resolve the stratification of redox processes in a biogeochemical continuum from the photic zone to deep anoxic sediments of the Black Sea. Appl Environ Microbiol. 2018;84:e2736–17.

    81.
    Nowicka B, Kruk J. Occurrence, biosynthesis and function of isoprenoid quinones. Biochim Biophys Acta. 2010;1797:1587–605.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    82.
    Kruk J, Trebst A. Plastoquinol as a singlet oxygen scavenger in photosystem II. Biochim Biophys Acta. 2008;1777:154–62.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    83.
    Szymańska R, Kruk J. Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in arabidopsis and is converted to plastochromanol by tocopherol cyclase. Plant Cell Physiol. 2010;51:537–45.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    84.
    Agrawal S, Jaswal K, Shiver AL, Balecha H, Patra T, Chaba R. A genome-wide screen in Escherichia coli reveals that ubiquinone is a key antioxidant for metabolism of long chain fatty acids. J Biol Chem. 2017;292:20086–99.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    85.
    Ksas B, Légeret B, Ferretti U, Chevalier A, Pospíšil P, Alric J, et al. The plastoquinone pool outside the thylakoid membrane serves in plant photoprotection as a reservoir of singlet oxygen scavengers. Plant Cell Environ. 2018;41:2277–87.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    86.
    Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant. 2003;119:355–64.
    CAS  Article  Google Scholar 

    87.
    Long SP, Humphries S, Falkowski PG. Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol. 1994;45:633–62.
    CAS  Article  Google Scholar 

    88.
    Triantaphylidès C, Havaux M. Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 2009;14:219–28.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    89.
    Pospíšil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta. 2012;1817:218–31.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    90.
    Lichtenthaler HK. Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res. 2007;92:163–79.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    91.
    Shi T, Ilikchyan I, Rabouille S, Zehr JP. Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501. ISME J. 2010;4:621.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    92.
    Muñoz-Marín M, del C, Shilova IN, Shi T, Farnelid H, Cabello AM, et al. The transcriptional cycle is suited to daytime N2 fixation in the unicellular cyanobacterium “Candidatus Atelocyanobacterium thalassa” (UCYN-A). MBio. 2019;10:e02495–18.
    PubMed  PubMed Central  Google Scholar 

    93.
    Ashworth J, Coesel S, Lee A, Armbrust EV, Orellana MV, Baliga NS. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proc Natl Acad Sci USA. 2013;110:7518–23.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    94.
    Smith SR, Gillard JTF, Kustka AB, McCrow JP, Badger JH, Zheng H, et al. Transcriptional orchestration of the global cellular response of a model pennate diatom to diel light cycling under iron limitation. PLOS Genet. 2016;12:e1006490.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    95.
    Nymark M, Valle KC, Brembu T, Hancke K, Winge P, Andresen K, et al. An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS ONE. 2009;4:e7743.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    96.
    Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, et al. Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol. 2006;7:R76.
    PubMed  PubMed Central  Article  Google Scholar 

    97.
    Waldbauer JR, Rodrigue S, Coleman ML, Chisholm SW. Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS ONE. 2012;7:e43432.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    98.
    Kana TM, Geider RJ, Critchley C. Regulation of photosynthetic pigments in micro-algae by multiple environmental factors: a dynamic balance hypothesis. N Phytol. 1997;137:629–38.
    CAS  Article  Google Scholar 

    99.
    Escoubas J-M, Lomas M, LaRoche J, Falkowski PG. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA. 1995;92:10237–41.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    100.
    Van Mooy BAS, Devol AH. Assessing nutrient limitation of Prochlorococcus in the North Pacific Subtropical Gyre by using an RNA capture method. Limnol Oceanogr. 2008;53:78–88.
    Article  Google Scholar 

    101.
    Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, et al. Processes and patterns of oceanic nutrient limitation. Nat Geosci. 2013;6:701–10.
    CAS  Article  Google Scholar 

    102.
    Muratore D, Boysen AK, Harke MJ, Becker KW, Casey JR, Coesel SN, et al. Community-scale synchronization and temporal partitioning of gene expression, metabolism, and lipid biosynthesis in oligotrophic ocean surface waters. 2020. https://www.biorxiv.org/content/10.1101/2020.05.15.098020v1.

    103.
    Saito MA, Bertrand EM, Dutkiewicz S, Bulygin VV, Moran DM, Monteiro FM, et al. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proc Natl Acad Sci USA. 2011;108:2184–9.
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    104.
    Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet F, et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature. 2008;457:467.
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    105.
    White AE, Barone B, Letelier RM, Karl DM. Productivity diagnosed from the diel cycle of particulate carbon in the North Pacific Subtropical Gyre. Geophys Res Lett. 2017;44:3752–60.
    CAS  Article  Google Scholar  More

  • in

    Genome-wide genetic diversity yields insights into genomic responses of candidate climate-selected loci in an Andean wetland plant

    1.
    IPBES. Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, Bonn, 2019).
    Google Scholar 
    2.
    Eizaguirre, C. & Baltazar-Soares, M. Evolutionary conservation-evaluating the adaptive potential of species. Evol. Appl. 7, 963–967 (2014).
    PubMed Central  Article  Google Scholar 

    3.
    Razgour, O. et al. Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections. Proc. Natl. Acad. Sci. USA 116, 10418–10423 (2019).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    4.
    Frankham, R., Ballou, J. D. & Briscoe, D. A. Introduction to Conservation Genetics (Cambridge University Press, Cambridge, 2010).
    Google Scholar 

    5.
    Hoffmann, A. A., Sgro, C. M. & Kristensen, T. N. Revisiting adaptive potential, population size, and conservation. Trends Ecol. Evol. 32, 506–517 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    6.
    Allendorf, F. W., Luikart, G. H. & Aitken, S. N. Conservation and the Genetics of POPULATIONS (Wiley Blackwell, Malden, 2012).
    Google Scholar 

    7.
    Caballero, A. & Garcia-Dorado, A. Allelic diversity and its implications for the rate of adaptation. Genetics 195, 1373–1384 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    8.
    Lopez-Cortegano, E. et al. Optimal management of genetic diversity in subdivided populations. Front. Genet. 10, 843 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    9.
    Frankham, R. Genetics and extinction. Biol. Conserv. 126, 131–140 (2005).
    Article  Google Scholar 

    10.
    Mable, B. K. Conservation of adaptive potential and functional diversity: Integrating old and new approaches. Conserv. Genet. 20, 89–100 (2019).
    Article  CAS  Google Scholar 

    11.
    Holderegger, R., Kamm, U. & Gugerli, F. Adaptive vs. neutral genetic diversity: Implications for landscape genetics. Landsc. Ecol. 21, 797–807 (2006).
    Article  Google Scholar 

    12.
    Kirk, H. & Freeland, J. R. Applications and implications of neutral versus non-neutral markers in molecular ecology. Int. J. Mol. Sci. 12, 3966–3988 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    13.
    Yildirim, Y., Tinnert, J. & Forsman, A. Contrasting patterns of neutral and functional genetic diversity in stable and disturbed environments. Ecol. Evol. 8, 12073–12089 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    14.
    Reed, D. H. & Frankham, R. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55, 1095–1103 (2001).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    15.
    Willi, Y. & Hoffmann, A. A. Demographic factors and genetic variation influence population persistence under environmental change. J. Evol. Biol. 22, 124–133 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    16.
    Matuszewski, S., Hermisson, J. & Kopp, M. Catch me if you can: Adaptation from standing genetic variation to a moving phenotypic optimum. Genetics 200, 1255–1272 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    17.
    Kirkpatrick, M. & Barton, N. H. Evolution of a species’ range. Am. Nat. 150, 1–23 (1997).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    18.
    Bridle, J. R., Polechova, J., Kawata, M. & Butlin, R. K. Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol. Lett. 13, 485–494 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    19.
    Tigano, A. & Friesen, V. L. Genomics of local adaptation with gene flow. Mol. Ecol. 25, 2144–2164 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    20.
    Jacob, S. et al. Gene flow favours local adaptation under habitat choice in ciliate microcosms. Nat. Ecol. Evol. 1, 1407–1410 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    21.
    Leffler, E. M. et al. Revisiting an old riddle: What determines genetic diversity levels within species?. PLoS Biol. 10, e1001388 (2012).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    22.
    Corbett-Detig, R. B., Hartl, D. L. & Sackton, T. B. Natural selection constrains neutral diversity across a wide range of species. PLoS Biol. 13, e1002112 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    23.
    Ellegren, H. & Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433 (2016).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    24.
    Zhu, Z. B., Yuan, D. J., Luo, D. H., Lu, X. T. & Huang, S. Enrichment of minor alleles of common SNPs and improved risk prediction for Parkinson’s disease. PLoS ONE 10, e0133421 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    25.
    Lei, X. Y., Yuan, D. J., Zhu, Z. B. & Huang, S. Collective effects of common SNPs and risk prediction in lung cancer. Heredity 121, 537–547 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    26.
    Huang, S. New thoughts on an old riddle: What determines genetic diversity within and between species?. Genomics 108, 3–10 (2016).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    27.
    Hoffmann, A. A. & Willi, Y. Detecting genetic responses to environmental change. Nat. Rev. Genet. 9, 421–432 (2008).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    28.
    Sgro, C. M., Lowe, A. J. & Hoffmann, A. A. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4, 326–337 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    29.
    Luikart, G., England, P. R., Tallmon, D., Jordan, S. & Taberlet, P. The power and promise of population genomics: From genotyping to genome typing. Nat. Rev. Genet. 4, 981–994 (2003).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    30.
    Pfeiffer, V. W. et al. Partitioning genetic and species diversity refines our understanding of species-genetic diversity relationships. Ecol. Evol. 8, 12351–12364 (2018).
    PubMed  PubMed Central  Google Scholar 

    31.
    Forester, B. R., Lasky, J. R., Wagner, H. H. & Urban, D. L. Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Mol. Ecol. 27, 2215–2233 (2018).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    32.
    Dolédec, S. & Chessel, D. Co-Inertia analysis—An alternative method for studying species environment relationships. Freshw. Biol. 31, 277–294 (1994).
    Article  Google Scholar 

    33.
    Legendre, P. & Legendre, L. Numerical Ecology (Elsevier, Amsterdam, 2012).
    Google Scholar 

    34.
    Mackintosh, A. et al. The determinants of genetic diversity in butterflies. Nat. Commun. 10, 3466 (2019).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    35.
    Franks, S. J. & Hoffmann, A. A. Genetics of climate change adaptation. Ann. Rev. Genet. 46, 185–208 (2012).

    36.
    Scheben, A., Yuan, Y. X. & Edwards, D. Advances in genomics for adapting crops to climate change. Curr. Plant Biol. 6, 2–10 (2016).
    Article  Google Scholar 

    37.
    Manel, S. et al. Genomic resources and their influence on the detection of the signal of positive selection in genome scans. Mol. Ecol. 25, 170–184 (2016).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    38.
    Gomulkiewicz, R. & Houle, D. Demographic and genetic constraints on evolution. Am. Nat. 174, E218–E229 (2009).
    PubMed  Article  Google Scholar 

    39.
    Willi, Y., Van Buskirk, J. & Hoffmann, A. A. Limits to the adaptive potential of small populations. Annu. Rev. Ecol. Evol. S. 37, 433–458 (2006).
    Article  Google Scholar 

    40.
    Lehnert, S. J. et al. Genomic signatures and correlates of widespread population declines in salmon. Nat. Commun. 10, 2996 (2019).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    41.
    Vellend, M. et al. Drawing ecological inferences from coincident patterns of population- and community-level biodiversity. Mol. Ecol. 23, 2890–2901 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    42.
    Bertin, A. et al. Genetic variation of loci potentially under selection confounds species-genetic diversity correlations in a fragmented habitat. Mol. Ecol. 26, 431–443 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    43.
    Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, e19379 (2011).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    44.
    Troncoso, A. J., Bertin, A., Osorio, R., Arancio, G. & Gouin, N. Comparative population genetics of two dominant plant species of high Andean wetlands reveals complex evolutionary histories and conservation perspectives in Chile’s Norte Chico. Conserv. Genet. 18, 1047–1060 (2017).
    Article  Google Scholar 

    45.
    Vigneau, E. & Qannari, E. M. Clustering of variables around latent components. Commun. Stat-Simul. C. 32, 1131–1150 (2003).
    MathSciNet  MATH  Article  Google Scholar 

    46.
    Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Article  Google Scholar 

    47.
    Vigneau, E., Chen, M. K. & Qannari, E. M. ClustVarLV: An R package for the clustering of variables around latent variables. R J. 7, 134–148 (2015).
    Article  Google Scholar 

    48.
    Oksanen, J. et al.Vegan: Community Ecology Packagehttps://cran.r-project.org/web/packages/vegan/index.html (2018).

    49.
    Dray, S. & Dufour, A. B. The ade4 package: Implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).
    Article  Google Scholar 

    50.
    Dyer, R. Gstudio: An R Package for the Spatial Analysis of Population Genetic Datahttps://github.com/dyerlab/gstudio/ (2017).

    51.
    Lumley, T. & Miller, A. Leaps: Regression Subset Selectionhttps://cran.r-project.org/web/packages/leaps/index.html (2009).

    52.
    Mazerolle, M. J. AICcmodavg: Model Selection and Multimodel Inference Based on (Q)AIC(c)https://cran.r-project.org/web/packages/AICcmodavg/index.html (2020). More