More stories

  • in

    Gamma diversity and under-sampling together generate patterns in beta-diversity

    1.Cornell, H. V. & Harrison, S. P. What are species pools and when are they important?. Annu. Rev. Ecol. Evol. Syst. 45, 45–67 (2014).Article 

    Google Scholar 
    2.Vellend, M. Conceptual synthesis in community ecology. Q. Rev. Biol. 85, 183–206 (2010).Article 

    Google Scholar 
    3.Vellend, M. The Theory of Ecological Communities Vol. 57 (Princeton University Press, 2020).
    Google Scholar 
    4.Whittaker, R. H. Vegetation of the Siskiyou mountains, Oregon and California. Ecol. Monogr. 30, 279–338 (1960).Article 

    Google Scholar 
    5.Chase, J. M. & Myers, J. A. Disentangling the importance of ecological niches from stochastic processes across scales. Philos. Trans. R. Soc. B: Biol. Sci. 366, 2351–2363 (2011).Article 

    Google Scholar 
    6.Jankowski, J. E., Ciecka, A. L., Meyer, N. Y. & Rabenold, K. N. Beta diversity along environmental gradients: Implications of habitat specialization in tropical montane landscapes. J. Anim. Ecol. 78, 315–327 (2009).Article 

    Google Scholar 
    7.Janzen, D. H. Why mountain passes are higher in the tropics. Am. Nat. 101, 233–249 (1967).
    Google Scholar 
    8.Ghalambor, C. K., Huey, R. B., Martin, P. R., Tewksbury, J. J. & Wang, G. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr. Comp. Biol. 46, 5–17 (2006).Article 

    Google Scholar 
    9.Tuomisto, H. & Ruokolainen, K. Comment on “disentangling the drivers of β diversity along latitudinal and elevational gradients”. Science 335, 1573 (2012).ADS 
    Article 
    CAS 

    Google Scholar 
    10.Harrison, S. Local and regional diversity in a patchy landscape: Native, alien, and endemic herbs on serpentine. Ecology 80, 70–80 (1999).Article 

    Google Scholar 
    11.Vellend, M. Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85, 3043–3055 (2004).Article 

    Google Scholar 
    12.Pardini, R., de Souza, S. M., Braga-Neto, R. & Metzger, J. P. The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape. Biol. Conserv. 124, 253–266 (2005).Article 

    Google Scholar 
    13.Kraft, N. J. et al. Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333, 1755–1758 (2011).ADS 
    Article 
    CAS 

    Google Scholar 
    14.Qian, H., Chen, S., Mao, L. & Ouyang, Z. Drivers of β-diversity along latitudinal gradients revisited. Glob. Ecol. Biogeogr. 22, 659–670 (2013).Article 

    Google Scholar 
    15.Marathe, A., Priyadarsanan, D. R., Krishnaswamy, J. & Shanker, K. Spatial and climatic variables independently drive elevational gradients in ant species richness in the Eastern Himalaya. PLoS ONE 15, e0227628 (2020).Article 
    CAS 

    Google Scholar 
    16.Måsviken, J., Dalerum, F. & Cousins, S. A. Contrasting altitudinal variation of alpine plant communities along the Swedish mountains. Ecol. Evol. 10, 4838–4853 (2020).Article 

    Google Scholar 
    17.Bruun, H. H. et al. Effects of altitude and topography on species richness of vascular plants, bryophytes and lichens in alpine communities. J. Veg. Sci. 17, 37–46 (2006).Article 

    Google Scholar 
    18.Xu, W., Chen, G., Liu, C. & Ma, K. Latitudinal differences in species abundance distributions, rather than spatial aggregation, explain beta-diversity along latitudinal gradients. Glob. Ecol. Biogeogr. 24, 1170–1180 (2015).Article 

    Google Scholar 
    19.Mori, A. S. et al. Community assembly processes shape an altitudinal gradient of forest biodiversity. Glob. Ecol. Biogeogr. 22, 878–888 (2013).Article 

    Google Scholar 
    20.Stegen, J. C. et al. Stochastic and deterministic drivers of spatial and temporal turnover in breeding bird communities. Glob. Ecol. Biogeogr. 22, 202–212 (2013).Article 

    Google Scholar 
    21.Kim, T. N., Bartel, S., Wills, B. D., Landis, D. A. & Gratton, C. Disturbance differentially affects alpha and beta diversity of ants in tallgrass prairies. Ecosphere 9, e02399 (2018).Article 

    Google Scholar 
    22.de Castro, F. S., Silva, P. G. D., Solar, R., Fernandes, G. W. & Neves, F. S. Environmental drivers of taxonomic and functional diversity of ant communities in a tropical mountain. Insect Conserv. Divers. 13, 393–403 (2020).Article 

    Google Scholar 
    23.Rodríguez, P. & Arita, H. T. Beta diversity and latitude in North American mammals: Testing the hypothesis of covariation. Ecography 27, 547–556 (2004).Article 

    Google Scholar 
    24.Agosti, D. & Alonso, L. The ALL protocol: A standard protocol for the collection of ground-dwelling ants. In Ants: Standard Methods for Measuring and Monitoring Biodiversity (eds Agosti, D. et al.) 204–206 (Smithsonian Institution Press, 2000).
    Google Scholar 
    25.Gotelli, N. J., Ellison, A. M., Dunn, R. R. & Sanders, N. J. Counting ants (Hymenoptera: Formicidae): Biodiversity sampling and statistical analysis for myrmecologists. Myrmecol. News 15, 13–19 (2011).
    Google Scholar 
    26.Greenslade, P. Sampling ants with pitfall traps: Digging-in effects. Insectes Soc. 20, 343–353 (1973).Article 

    Google Scholar 
    27.R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).
    Google Scholar  More

  • in

    Shape-changing chains for morphometric analysis of 2D and 3D, open or closed outlines

    2D mandible outlinesIn17, elliptical Fourier analysis (EFA) is employed to investigate the lateral shape difference between 106 fossil mandibles of 5 groups: A. robustus ((n=7)), H. erectus ((n=12)), H. heidelbergensis ((n=4)), H. neanderthalensis ((n=22)), and H. sapiens ((n=61)). In the presented work, the authors apply the shape-changing chain method to the same dataset. Twelve samples were suppressed, including all 7 A. robustus samples, 4 H. neanderthalensis samples, and one H. sapiens sample. Therefore, 94 mandible profiles of 4 groups of the ancient human are analyzed: H. erectus ((n=12)), H. heidelbergensis ((n=4)), H. neanderthalensis ((n=18)), and H. sapiens ((n=60)). The dataset is in the form of Cartesian coordinates of points along the mandible boundary. Note that the shape-changing chain method does not require pre-alignment of curves or removal of the size factor. However, the mandible profile dataset the authors obtained had already lost the information of the original sample sizes. Therefore, only normalized mandibular shapes are compared herein. Figure 5 illustrates the mean shape of each group of profiles by aligning all profiles in the set using a standard Procrustes superimposition (PS) which includes translation, scaling, and rotation of the profiles27.Figure 5Mean mandibular shapes of samples from H. erectus (red circles), H. heidelbergensis (blue triangles), H. neanderthalensis (green squares), and H. sapiens (black diamonds).Full size imageUsing the relative angle method ((k=150), (T=20^circ)), five apices are reserved, constituting six sub-profiles for each profile. An illustration of the location of the apices on a mandible profile is shown in Fig. 6. Each sub-profile is then matched with a shape-changing chain individually. The determination of segment type vector of each sub-profile refers to the growth mechanism of mandible proposed by Enlow et al.28. As shown in Fig. 6, the mechanism of mandible growth involves bone resorption (indicated by the arrows pointing towards the mandible contour) and bone deposition (indicated by the arrows pointing out of the mandible contour). Although the whole mandible’s displacement direction is forwards and downwards, the reconstruction of the ascending limb is generally backwards and upwards. G-segments and C-segments are employed to approximate the growing portions in target profiles and characterize the difference in profile lengths.Figure 6A profile ((j=1)) from the H. erectus group: Five apices (red circle) are located using the relative angle method ((k=150), (T=20^circ)) and divide the profile into six sub-profiles. The arrows represent the growth pattern of the mandible28.Full size imageNote that the growths of the inferior edge of the mandibular body and the posterior edge of the mandibular ramus are more significant than the rest parts of the mandible profile. The 94 mandible profiles are then matched with a shape-changing chains using the following scheme. The segment vectors for the first, second, third, and sixth sub-profiles are defined as (left[{text{MGM}}right]) alike, and the segment vectors for the fourth and fifth sub-profiles are both defined as (left[{text{MCGM}}right]), where the C-segments and G-segments are used to capture the difference in arc lengths. Therefore, the overall segment vector is$$mathbf{V}=left[text{M G M M G M M G M M C G M M C G M M G M} , right]text{,}$$where there are a total of 20 segments—12 M-segments, 2 C-segments, and 6 G-segments. After the segment type vector is defined, the shape-changing chain is generated to match the target mandible profiles and then is optimized for each sub-profile. The maximum and mean error of all profiles of the final matching result are ({E}_{text{max}}=8.0863) and (overline{E }=0.6009) units, respectively. Figure 7 shows the best (a), the average (b), and the worst match (c) according to ({tilde{E }}_{j}). Note that in the worst match, the G-segment at the condyle (head) of the mandible causes the largest matching error. This is because the third primary segmentation point (between the two M-segments that follow) identified using the relative angle method for this specific profile is not at the tip of the condyle as the majority of the profiles.Figure 7The fitting result of 94 human mandibles. (a) The best match (the 4th profile—H. erectus, ({tilde{E }}_{4}=0.3924)); (b) The match with error closest to (overline{E }) (the 6th profile—H. erectus, ({tilde{E }}_{6}=0.6006)); (c) The worst match (the 13th profile—H. heidelbergenis, ({tilde{E }}_{13}=1.0771)).Full size imageThe orientation difference between two neighboring segments reflects the rotational angle between them, and thus are employed in the statistical analysis in the next step. Denote the direction of a vector (mathbf{u}={left{{u}_{x},{u}_{y}right}}^{T}) as (angle left(mathbf{u}right)), then the orientation change between the ({e}{text{th}}) and the ({(e+1)}{text{th}}) segments on the ({j}{text{th}}) profile is calculated as the difference between the direction of the last piece on the ({e}{text{th}}) segment and the direction of the first piece on the ({(e+1)}{text{th}}) segment$${sigma }_{j}^{e}=angle left({overline{mathbf{z}} }_{{j}_{2}}^{e+1}-{overline{mathbf{z}} }_{{j}_{1}}^{e+1}right)-angle left({overline{mathbf{z}} }_{{j}_{{m}_{j}^{e}+1}}^{e}-{overline{mathbf{z}} }_{{j}_{{m}_{j}^{e}}}^{e}right), forall e=1,dots ,q-1 j=1,dots ,p.$$
    (10)
    In the mandible example, 19 angular variables are generated from 20 segments. As in17, a stepwise discrimination analysis (DA) is conducted (in IBM SPSS 22) to figure out the relationship among the four homo groups. DA is a supervised classification method and returns (g-1) canonical components among (g) groups of samples29. Figure 8 shows the convex hull of four homo genus plotted with the first and the second canonical components. The three main groups: H. erectus, H. neanderthalensis, and H. sapiens, are separated from each other in the direction of the first canonical component. H. heidelbergensis and H. neanderthalensis have an overlap in the direction of the second canonical component. In stepwise DA, leave-one-out cross-validation (LOOCV) is applied to verify the stability of the linear model. As a result, the prediction accuracy is 91.5% and the cross-validation accuracy is 80.9%. This DA result suggests that the shape-changing chain method is useful in analyzing 2D shapes. The classification matrices of original prediction and LOOCV are presented in Table 2, showing the details of discrimination of the four mandibular shape groups.Figure 8Canonical plot of the 94 human mandibles from four groups (H. erectus, H. heidelbergensis, H. neanderthalensis, and H. sapiens) based on the orientation changes between segments (19 variables).Full size imageTable 2 Classification matrices of the original DA and cross-validated prediction of 94 human mandibles.Full size tableNote that the classification results as shown in Fig. 8 and Table 2 are in accordance with the results obtained with EFA in17. The high misclassification rate of H. heidelbergensis and its distribution on the canonical plot are also in keep with the mainstream opinion that H. heidelbergensis is a chronospecies evolving from H. erectus and is considered as the most recent common ancestor (MRCA) between H. sapiens and H. neanderthalensis. In the work of Lestrel et al. based on EFA, 20 harmonics are employed to match 106 mandibular shapes, producing 82 Fourier descriptors17. Then, 12 distances from the centroid to specified points on each mandible’s contour are used in statistical analysis. Compared to their study, the shape-changing chain method generates only a total of 28 variables (20 orientations of all segments and 8 arc lengths of C-segments and G-segments). The differences of orientations between neighboring segments is then calculated and generates 19 variables to be analyzed in stepwise DA. Table 3 shows a comparison of the variables generated in the approximation of curves and used for statistical analysis with the shape-changing chain method and EFA. The shape-changing chain method performs a satisfying approximation result of the mandibular shapes with much fewer variables compared with EFA.Table 3 Numbers of variables used in the shape-changing chain method and in EFA17 for fitting and analyzing human mandible profiles.Full size table2D leaf outlinesLeaf classification is a typical problem that has been studied with various methods, such as artificial neural networks (ANN)30, image moments31, and EFA9. In addition, many leaves have a symmetrical shape creating issues for effective EFA12. Using the shape-changing chain method, the fitting result reveals the growth of portions on the contour and the rotation between them. This kind of information can be used in statistical analysis. Although other methods which also make use of non-shape information (size, color, etc.) have been very convenient and efficient in recognizing leaf genera, leaf matching and classification remains a problem to test the ability of the shape-changing chain method to fit and compare profiles with complicated and largely varying shapes. In this example, nine groups of 145 leaves are studied (see the groups and the number of samples in each group in Table 3). The original scanned and binarized images of the nine genera of leaves are shown in Fig. s1. The contours are traced using the Moore-Neighbor method32 and then smoothed with the MATLAB cubic spline interpolation (see Fig. s2). All leaf profiles of their original sizes are analyzed. The arc lengths of the profiles range from 1141.5 units to 8433.1 units, the areas of the leaves range from (6.1671times {10}^{4}) units2 to (1.4615times {10}^{6}) units2.Applying the relative angle method, a number of apices are recognized on each leaf contour. These apices are the primary segmentation points that determine the boundaries of sub-profiles on leaf contours. Note that the shapes of leaves from different groups vary significantly, therefore the point interval and angle threshold used for locating apices varies from group to group. For some groups, the numbers of apices identified on different samples may be different too. Table 4 shows the parameters used for identifying apices as well as the minimum and maximum numbers of apices identified on samples for each group.Table 4 Parameters used for identifying apices on leaf contours and the number of apices identified for each group.Full size tableIn order to maintain homology, supplementary segmentation points are added to divide all sample profiles into the same number of portions. There is no need to add more segmentation points on the profile that contains the most number of apices (red oak, (j=101)), therefore the total number of segmentation points on each profile is determined to be 34, dividing each profile into 35 portions. In order to reduce the matching error, supplementary segmentation points are distributed as evenly as possible in sub-profiles formed by the primary segmentation points (original apices) using a method developed based on a genetic algorithm (GA). In this problem, the locations of the supplemented segmentation points on the ({j}{text{th}}) profile are determined through the fitness function determined as follows$${F}_{j}=sum_{e=1}^{q}{left({k}_{j}^{e+1}-{k}_{j}^{e}-frac{{N}_{j}-1}{q}right)}^{2}.$$
    (11)
    In Eq. (11), the number of pieces contained in the ({j}{text{th}}) profile (({N}_{j}-1)) divided by the number of portions (q) yields the average number of pieces in each portion. (({k}_{j}^{e+1}-{k}_{j}^{e})) is the number of pieces contained in the ({e}{text{th}}) portion confined by the ({e}{text{th}}) and the ({(e+1)}{text{th}}) segmentation points on the ({j}{text{th}}) profile. After encoding the locations of all segmentation points in the GA and several rounds of optimization based on a certain scale of crossover and mutation, the set of supplementary segmentation points that minimizes the fitness function, Eq. (11), is determined. The original apices (red circles) and supplementary segmentation points (green circles) distributed on samples from different groups are shown in Fig. 9. In this example, each profile is finally divided into 35 portions.Figure 9The original apices (red circles) and supplementary segmentation points (green circles) on leaf contours. (a) Cherry, (b) Dogwood, (c) Gum, (d) Hickory, (e) Mulberry, (f) Red maple, (g) Red oak, (h) Sugar maple, (i) White oak. For each group, the sample that contains the most original apices is presented.Full size imageThe length of each portion varies among profiles, thus M-segments are not applicable. In addition, some portions still contain local burrs and sharp corners, which would not be matched well by C-segments. Therefore, each portion is matched by a G-segment, and the segment vector contains 35 G-segments. The maximum and mean error of 145 leaf profiles are ({E}_{text{max}}=60.6063) and (overline{E }=8.7062) units, respectively. Figure 10 shows the best, the average, and the worst matching results of the leaves according to ({tilde{E }}_{j}). More matches of nine genera of leaves are illustrated in Fig. s3. The result show that given the distribution of apices (primary segmentation points that determine sub-profiles), the GA strategy can automatically determine the distribution of supplementary segmentation points along a profile. With the segmentation points generated from this process, the shape-changing chain matches the leaf contours with small error compared to the random segmentation in the previous study.Figure 10The fitting results of 145 leaves. (a) The best match (the 62nd profile—hickory, ({tilde{E }}_{62}=0.8748)); (b) The average match (the 88th profile—red maple, ({tilde{E }}_{88}=4.0866)); c The worst match (the 110th profile—red oak, ({tilde{E }}_{107}=9.7866)).Full size imageFor classification analysis, 34 orientation differences between neighboring segments are calculated using Eq. (10). Three more variables are employed: The number of primary segmentation points, the number of burrs (detected using the relative angle method with (k=50) and (T=30^circ)), and the arc length of each profile. This sums up to a total of 37 variables. A stepwise DA is performed to classify the 145 leaf samples, and 22 out of the 37 variables are selected for analysis. The variances of the first three canonical functions are 73.5%, 13.3%, and 7.5%, which add up to 94.3% in total. Figures 11 and 12 illustrate the 2D and 3D canonical plots of the nine genus of leaves based on the first three canonical components. The plots show that gum, red maple, and white oak are distinctively separated from other groups. Cherry and mulberry are partially overlapped in the directions of canonical Roots 1 and 2 for their similar overall shapes and serrated edges. There is also an overlap between dogwood and hickory in the directions of canonical Roots 1 and 3 for their similar shapes and smooth edges. The prediction accuracy is 98.6%, and the leave-one-out cross-validation is 97.9%. Only two samples of cherry are misidentified as mulberry, and one sample of hickory is discriminated as dogwood. The DA results reveal that the shape-changing method is capable of fitting a large number of profiles that have complicated shapes and different sizes, as well as generating useful variables for statistical analysis. The leave-one-out cross-validation accuracy suggests that this method is also effective with fewer variables. In addition, the shape-changing chain method enables direct observation and comparison of variables that have physical meanings, such as the relative angles between segments.Figure 11The 2D Canonical plots of nine genus of leaves based on 22 variables.Full size imageFigure 12The 3D Canonical plot of nine genus of leaves based on 22 variables.Full size image3D cranial suture curvesThe shape-changing chain method is now applied to 3D suture curves on human infants’ skulls from a study of coronal synostosis18,19. The dataset contains 63 samples categorized into 4 groups, including left unicoronal synostosis (LUCS, (n=8)), right unicoronal synostosis (RUCS, (n=19)), bicoronal synostosis (BCS, (n=16)), and unaffected cases ((n=20)). The original data of each sample consist of 209 anatomical landmarks and curve semilandmarks located on the skull surface, especially along some anatomical lines as sutures. In this work, three curves that characterize the skull deformation are selected for analysis: the coronal suture curve, the lambdoid suture curve, and the sagittal curve which is comprised of anatomical landmarks and curve semilandmarks located on the metopic suture, the sagittal suture, and the mid-line on the occipital bone. Figure 13 shows the three suture curves on a skull surface.Figure 13The location of the coronal suture (magenta), sagittal curve (blue) and the lambdoid suture (red) on a human infant skull. The intersection points between sutures, P1 and P2, divide the sagittal curve into three sub-profiles and the lambdoid suture into two sub-profiles.Full size imageBCS occurs when the coronal sutures on both sides of the skull fuse prematurely, causing the overall head shape to become broad and short. In this case, the relative location of the lambdoid suture on the skull will move forward compared to the unaffected cases, but its shape is not affected as obviously as the coronal suture or the sagittal curve which are directly affected by coronal synostosis. In order to investigate the relative location and orientation in addition to the shape of the suture curves, a standard Procrustes superimposition is performed on the original data so that all skulls represented by the 209 landmarks and semilandmarks are scaled to the same size and aligned. Figure 14 illustrates the mean shapes of the sagittal curves and the lambdoid sutures of each group. It can be observed that for BCS cases, the sagittal curve is shorter in the anterior–posterior direction, the coronal suture becomes wider in the left–right direction, and the lambdoid suture is longer and positioned relatively forward. These differences are in accordance with the overall wider and shorter BCS skull shape. As for LUCS and RUCS cases, all three curves display a symmetrical shape deformation or orientation change about the skull symmetry plane (X = 0).Figure 14Mean shapes of (a) the sagittal curves, (b) the coronal suture, and (c) the lambdoid sutures of four groups: LUCS (red dotted line), BCS (blue solid line), RUCS (green dotted dashed line), and unaffected cases (black dashed line). Notice the symmetry of the suture curves about the skull symmetry plane (X = 0).Full size imageThe anatomical landmarks P1 and P2 (Fig. 13) which are the intersection points between the sutures, are selected as the primary segmentation points. Thus, the sagittal curve, the coronal suture, and the lambdoid suture are divided into three, two, and two sub-profiles, respectively. Since the coronal suture and the lambdoid suture grow symmetrically about the skull symmetry plane, their segment type vectors for two sub-profiles should be symmetric, respectively. In addition, each segment type vector should contain a G- or H-segment to characterize the growth. The segment type vectors of the three curves are designated as:

    Sagittal curve: (left[begin{array}{cc}{text{M}}& {text{G}}end{array}right]), (left[begin{array}{cc}{text{M}}& {text{H}}end{array}right]), (left[begin{array}{cc}{text{M}}& {text{G}}end{array}right]);

    Coronal suture:(left[begin{array}{ccc}{text{M}}& {text{G}}& {text{H}}end{array}right]), (left[begin{array}{ccc}{text{H}}& {text{G}}& {text{M}}end{array}right]);

    Lambdoid suture: (left[begin{array}{cc}{text{G}}& {text{H}}end{array}right]), (left[begin{array}{cc}{text{H}}& {text{G}}end{array}right]).

    In spatial cases, the orientation of each segment is given by 3 parameters, and each G- or H-segment is characterized by an additional length parameter. Therefore, this matching scheme generates 21, 22, and 16 parameters to describe the shape variances for the sagittal curves, the coronal suture curves, and the lambdoid suture curves, respectively. Note that the suture curves are relatively smooth, thus the average value of the maximum error on all segments ({overline{E} }_{j}) is very significant of the matching error of the chain at the ({j}{text{th}}) profile. Therefore, this parameter is chosen to assess the error in this application. Figure 15 shows the best, the average, and the worst matches of the sagittal curves, the coronal sutures, and lambdoid sutures. The overall mean error ((overline{E })) of the sagittal curves, the coronal sutures, and the lambdoid sutures are 0.8728, 0.5060, and 0.3666 units, respectively.Figure 15The fitting results of (a–c) sagittal curves, (d–f) coronal sutures, and (g–i) lambdoid sutures from 63 samples. The left column (a, d, g) is the best match of each group, the middle column (b, e, h) is the average match of each group, and the right column (c, f, i) is the worst match of each group. (a) ({overline{E} }_{s-52}=0.5122) (unaffected); (b) ({overline{E} }_{s-19}=0.8681) (BCS); (c) ({overline{E} }_{s-46}=1.6055) (unaffected); (d) ({overline{E} }_{c-12}=0.2507) (BCS); (e) ({overline{E} }_{c-54}=0.5082) (unaffected); (f) ({overline{E} }_{c-42}=0.9636) (RUCS); g ({overline{E} }_{l-29}=0.1225) (BCS); (h) ({overline{E} }_{l-37}=0.3687) (BCS); (i) ({overline{E} }_{l-28}=1.0997) (RUCS).Full size imageIn order to represent the orientation of the spatial chain, the ({e}{text{th}}) segment at the ({j}{text{th}}) profile is characterized by a unit vector that points from the starting point to the endpoint of the segment as$${mathbf{u}}_{j}^{e}=frac{{overline{mathbf{z}} }_{{j}_{{m}_{j}^{e}+1}}^{e}-{overline{mathbf{z}} }_{{j}_{1}}^{e}}{Vert {overline{mathbf{z}} }_{{j}_{{m}_{j}^{e}+1}}^{e}-{overline{mathbf{z}} }_{{j}_{1}}^{e}Vert }.$$
    (12)
    Since each vector ({mathbf{u}}_{j}^{e}) contains three Cartesian coordinates, each sagittal curve, coronal suture, and lambdoid suture is thus characterized by 18, 18, and 12 variables, respectively. For lambdoid sutures, its relative location which is characterized by the coordinates of point P2 is also analyzed. Therefore, the total number of variables analyzed for a lambdoid suture is 15. This is much fewer than the 209 landmarks and semilandmarks analyzed in the work of Heuzé et al.19. Stepwise DA is conducted with the variables above, and LOOCV is performed to verify the stability of the linear model. In stepwise DA, 6, 7, and 8 variables are selected to be analyzed for sagittal curves, coronal sutures, and lambdoid sutures, respectively. Figure 16 illustrates the canonical plots of the three set of curves. As shown in Fig. 16, all three set of suture curves display strong separation among four classes on the 2D canonical plots. Besides, the LUCS and RUCS curves are distributed in the opposite directions from the BCS and unaffected ones along the first canonical component, while the BCS and unaffected curves differ in the direction of the second canonical component. These plots confirm the symmetrical shape deformation of the suture curves of LUCS and RUCS cases, and the changes in the lengths and relative locations of the suture curves of BCS as observed in Fig. 14.Figure 16The 2D canonical plots of the suture curves selected from 63 skull samples. (a) The sagittal curves based on 6 variables. (b) The coronal sutures based on 7 variables. (c) The lambdoid sutures based on 8 variables.Full size imageThe original DA prediction accuracy and cross-validated accuracy are both 100% for the sagittal curves, which indicates that the shape difference of the sagittal curves can efficiently distinguish specific diagnosis of coronal synostosis. The original DA prediction accuracy and cross-validated accuracy for the coronal sutures are 98.4% and 96.8%, respectively. There are two cases (BCS and RUCS) misclassified as unaffected case. As for the lambdoid sutures, the original DA prediction accuracy and cross-validated accuracy are both 98.4%. The only misclassified case in both predictions is that one BCS lambdoid suture is categorized as unaffected. This suggests that the coronal suture and the lambdoid suture is subjected to both shape deformation and location transformation due to coronal synostosis.These matching and classification results show that the shape-changing chain is efficient in fitting and analyzing 3D curves with a very moderate number of variables compared to other parametric methods. For example, Zhou et al. employed discrete cosine transform (DCT) to analyze the same three sets of suture curves33. In their work, 12, 6, and 6 harmonics are employed to fit the sagittal curves, the coronal suture curves, and the lambdoid suture curves, resulting in 36, 18, and 18 coefficients to be analyzed. Table 5 shows a comparison of the variables used to match the curves and perform statistical analysis with the two methods. A comparison of the classification accuracies of the two methods is not provided because Zhou et al. employed between-group principal component analysis (bgPCA) while the presented work uses stepwise DA. Note that the variables obtained in DCT are mathematical coefficients which are hard to interpret, while the variables in the shape-changing chain method represent the orientations, lengths, or locations of segments, providing direct information of the variance of the curve shapes.Table 5 Numbers of variables used in the shape-changing chain method and in DCT33 for fitting and analyzing suture curves.Full size table More

  • in

    Bird population declines and species turnover are changing the acoustic properties of spring soundscapes

    Bird dataNorth America: we used annual bird count data collated under the North American Breeding Bird Survey (NA-BBS: https://www.pwrc.usgs.gov/bbs/) from 1996 to 2017. NA-BBS survey routes, consisting of 50 survey points (hereafter sites) evenly distributed over ~24.5 miles, are distributed across the United States and Canada and are usually surveyed in June. At each site, skilled volunteers conduct a three-minute point count, recording all birds seen or heard within a 400-m radius59.Europe: we used annual bird count data from 23 survey schemes across 22 countries collated under the Pan-European Common Bird Monitoring Scheme (PECBMS: https://pecbms.info) from 1998 to 2018. In each scheme, skilled volunteers carry out either line transects, point counts or territory mapping at survey sites during the breeding season and record all birds encountered60 (Supplementary Table 5); while methods vary between survey schemes, they are consistent within schemes across the time period included here.Where count data were reported for subspecies, these were aggregated to species level and any records of hybrid species or specifying genus only were removed. The longitude and latitude of each survey site (just the first site of each NA-BBS survey route) were also provided by NA-BBS and PECBMS. Not all sites were surveyed in every year and only sites surveyed at least three times during the defined time period were included in analyses. Note that similar results were found when restricting data to sites surveyed in at least 10 years during the defined period.Sound recordingsSound files for all species detected on NA-BBS and PECBMS surveys were downloaded from Xeno Canto, an online database of sound recordings of wild birds from around the world (http://www.xeno-canto.org). Specifically, we identified all files longer than 30 s, with associated metadata categorising them as high quality (category “A”) and as either “song”, “call” or “drumming” types; sound files whose type category including the term “wingbeat”, “flap”, “begging”, “alarm” or “night” types were excluded. Sound files downloaded for NA-BBS species were restricted to those recorded in North America and those from PECBMS to recordings made in Europe. If no sound files met these requirements for a given species, we downloaded all files of shorter duration for that species that met the quality and type criteria and stitched repeats of these together to produce files longer than 30 s. Where more than 50 sound files for a given species met our criteria for inclusion, a random selection of 50 was taken for use in subsequent analyses. We used multiple sound files for each species to capture, where possible, between-individual variation in song and call structure, with the sound file(s) for inclusion in specific soundscapes randomly subsampled from this set. If no sound files for a species were available, the sites where that species was detected were removed from subsequent analyses; this represented More

  • in

    Scientists say Australian plan to cull up to 10,000 wild horses doesn’t go far enough

    NEWS
    01 November 2021

    Scientists say Australian plan to cull up to 10,000 wild horses doesn’t go far enough

    A fast-growing population of feral horses in an alpine national park needs to be substantially reduced in number, researchers argue.

    Bianca Nogrady

    0

    Bianca Nogrady

    Bianca Nogrady is a freelance science journalist based in Sydney, Australia.

    View author publications

    You can also search for this author in PubMed
     Google Scholar

    Share on Twitter
    Share on Twitter

    Share on Facebook
    Share on Facebook

    Share via E-Mail
    Share via E-Mail

    Brumbies roam a wintry landscape near Yarangobilly in Australia’s Kosciuszko National Park.Credit: Perry Duffin/EPA-EFE/Shutterstock

    Up to 10,000 feral horses might be killed or removed from Australia’s largest alpine national park under a draft plan to control the rapidly growing population of non-native animals. Scientists have welcomed the idea of removing them, but are alarmed that the plan still allows for thousands to remain, threatening endangered species and habitats.The proposed cull, in Kosciuszko National Park, New South Wales (NSW), contrasts with a ban on lethal control measures in the United States, where large populations of wild horses known as mustangs also cause problems.
    Australian scientists call for ‘feral horse’ culls in alpine national park
    The draft plan, released last month, recommends reducing the park’s population of wild horses, known in Australia as brumbies, from an estimated 14,000 to about 3,000 through a combination of mostly ground-based shooting, as well as rounding up and rehoming.But the Australian Academy of Science argues that the number of horses should be rapidly reduced below 3,000. In an open letter with 69 signatories including scientists and institutions sent to the NSW environment minister on Friday, they note that “alpine wetlands continue to degrade even with very small numbers of feral horses. Kosciusko cannot begin to recover from drought, extensive bushfires and overgrazing if, as currently proposed, 3,000 feral horses remain.”Capitulating to lobby groupsResearchers say the draft plan capitulates to a small but vocal group that has lobbied the government to protect horses because of the animals’ heritage value. The plan would allow the remaining brumbies to roam over one-third of the park. That would include threatened alpine sphagnum bogs and the habitats of endangered and vulnerable species such as a fish called the stocky galaxias (Galaxias tantangara), the alpine tree frog (Litoria verreauxii alpina) and the broad-toothed rat (Mastacomys fuscus).Australia has no native mammals with hard hooves, and so horses do more damage to delicate vegetation and soils than soft-footed species, such as kangaroos and wallabies, as well as creating problems through over-grazing.
    Ancient DNA points to origins of modern domestic horses
    David Watson, an ecologist at Charles Sturt University in Albury–Wodonga — which straddles NSW and the neighbouring state of Victoria — says the NSW government “couldn’t have picked a worse place” to allow feral horses to roam. He makes the point that Australia’s alpine environment covers just 1% of the continent and has many endemic and threatened species that are found nowhere else.“These areas are just too fragile to have large herbivores trampling around in them,” adds Don Driscoll, an ecologist at Deakin University in Melbourne.Management of feral horses has been a long-running issue in Australia’s mountainous alpine region, which extends across three states. The Australian Capital Territory, which shares a border with Kosciuszko National Park, has a zero-tolerance approach to feral horses and uses methods including aerial shooting.Victoria also shares an alpine border with New South Wales, but its latest management plan, released on 1 November, recommends using culling and other measures to remove all feral horses in the most delicate alpine environments, and the steady reduction of numbers elsewhere.Brumbies and mustangsThe NSW state government had previously tried to control the brumbies by rehoming them on private land, but was never able to find a place for more than a few hundred horses a year, rehoming only about 1,000 since 2002. Jamie Pittock, an environmental scientist at the Australian National University in Canberra, says that the government’s acknowledgement that the exponentially growing population cannot be managed with rehoming alone is at least “a step forward”.But Watson says that 3,000 horses would breed rapidly enough that 1,000 would still need to be removed or killed every few years, meaning that even a small population will create a continuing headache in terms of damage to the park and removal requirements.
    Ancient horses went dark to hide in forests
    A spokesperson for the NSW National Parks and Wildlife Service said the proposed target of 3,000 horses would maintain the “environmental values of the park” and that removing horses from two thirds of the park would provide “effective protection” for threatened species. They did not respond to Nature’s specific questions about scientists’ criticisms of the draft plan.The United States is grappling with similar issues with mustangs in national parks, says ecosystem scientist John Derek Scasta at the University of Wyoming in Laramie. “The goal is to get within an agreed-upon number of horses that are sustainable,” he says, but not everybody agrees on what that number is.Because legislation bans culling, the US Bureau of Land Management instead relies on rounding up, sterilization, rehoming or paying to keep the horses on either private or federal holdings. But Scasta says rising numbers, and the costs of looking after them, might mean the United States has to face its own reckoning with wild horses in the not-too-distant future.

    doi: https://doi.org/10.1038/d41586-021-02977-7

    Related Articles

    Australian scientists call for ‘feral horse’ culls in alpine national park

    Ancient DNA points to origins of modern domestic horses

    Ancient horses went dark to hide in forests

    Subjects

    Government

    Policy

    Environmental sciences

    Conservation biology

    Latest on:

    Government

    Scientists’ fears of racial bias surge amid US crackdown on China ties
    News 29 OCT 21

    Why hundreds of scientists are weighing in on a high-stakes US abortion case
    News 26 OCT 21

    Brazil’s scientists face 90% budget cut
    Correspondence 25 OCT 21

    Policy

    UK research funding to grow slower than hoped
    News 28 OCT 21

    The advocacy frontier
    Outlook 27 OCT 21

    The fluoride wars rage on
    Outlook 27 OCT 21

    Environmental sciences

    Machine learning enables global solar-panel detection
    News & Views 27 OCT 21

    Air quality: WHO guidelines could deepen inequities
    Correspondence 26 OCT 21

    Marine urban sprawl is gobbling up Earth’s coastlines
    Research Highlight 26 OCT 21

    Jobs

    Epidemiologist / Postdoc

    German Cancer Research Center in the Helmholtz Association (DKFZ)
    Heidelberg, Germany

    PhD Student in Liquid Biopsy

    German Cancer Research Center in the Helmholtz Association (DKFZ)
    Germany

    PhD (f/m/d) Data-driven Continuum Modelling of Infected Cell Dynamics on the Tissue Scale / Master’s degree in physics, computer science, bioinformatics, computational biology, data science, machine learning or relevant discipline / …

    Helmholtz-Zentrum Dresden-Rossendorf (HZDR)
    Görlitz, Germany

    PhD (f/m/d) Generative Machine Learning of Time-Lapse Virological Imaging Data / Master’s degree in Computer science, Bioinformatics, Computational biology, Data science, Machine learning or relevant discipline / Engage with our …

    Helmholtz-Zentrum Dresden-Rossendorf (HZDR)
    Görlitz, Germany More

  • in

    Venatorbacter cucullus gen. nov sp. nov a novel bacterial predator

    1.Pérez, J., Moraleda-Muñoz, A., Marcos-Torres, F. J. & Muñoz-Dorado, J. Bacterial predation: 75 years and counting!. Environ. Microbiol. 18, 766–779 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Linares-Otoya, L. et al. Diversity and antimicrobial potential of predatory bacteria from the Peruvian coastline. Mar. Drugs. 15, E308. https://doi.org/10.3390/md15100308 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    3.Pasternak, Z. et al. By their genes ye shall know them: Genomic signatures of predatory bacteria. ISME J. 7, 756–769 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Sockett, R. E. Predatory lifestyle of Bdellovibrio bacteriovorus. Ann. Rev. Microbiol. 63, 523–539 (2009).CAS 
    Article 

    Google Scholar 
    5.Korp, J., Vela Gurovic, M. S. & Nett, M. Antibiotics from predatory bacteria. Beilstein J. Org. Chem. 12, 594–607 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Johnke, J., Fraune, S., Bosch, T. C. G., Hentschel, U. & Schulenburg, H. Bdellovibrio and like organisms are predictors of microbiome diversity in distinct host groups. Microb. Ecol. 79, 252–257 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Vila, J., Moreno-Morales, J. & Ballesté-Delpierre, C. Current landscape in the discovery of novel antibacterial agents. Clin. Microbiol. Infect. https://doi.org/10.1016/j.cmi.2019.09.015 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Hobley, L. et al. Dual predation by bacteriophage and Bdellovibrio bacteriovorus can eradicate Escherichia coli prey in situations where single predation cannot. J. Bacteriol. 202, e00629-19. https://doi.org/10.1128/JB.00629-19 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    9.El-Shibiny, A., Connerton, P. L. & Connerton, I. F. Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens. Appl. Environ. Microbiol. 71, 1259–1266 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Wilkinson, D. A. et al. Updating the genomic taxonomy and epidemiology of Campylobacter hyointestinalis. Sci. Rep. 8, 2393. https://doi.org/10.1038/s41598-018-20889-x (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Lee, M. D. GToTree: A user-friendly workflow for phylogenomics. Bioinformatics 35, 4162–4164 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 10, e1002195 (2011).MathSciNet 
    Article 
    CAS 

    Google Scholar 
    13.Edgar, R. C. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 5, 113 (2004).Article 
    CAS 

    Google Scholar 
    14.Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. TrimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Hyatt, D., LoCascio, P. F., Hauser, L. J. & Uberbacher, E. C. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28, 2223–2230 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Shen, W. & Xiong, J. TaxonKit: A cross-platform and efficient NCBI taxonomy toolkit. bioRxiv. (Accessed 1 June 2021); https://www.biorxiv.org/content/10.1101/513523v1 (2019).
    17.Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490 (2010).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Tange, O. GNU Parallel. (Accessed 1 June 2021); https://zenodo.org/record/1146014#.YOHaiJhKiUk (2018).19.Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Czech, L. et al. Role of the extremolytes ectoine and hydroxyectoine as stress protectants and nutrients: Genetics, phylogenomics, biochemistry, and structural Analysis. Genes (Basel). 9, E177. https://doi.org/10.3390/genes9040177 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Gregson, B. H., Metodieva, G., Metodiev, M. V., Golyshin, P. N. & McKew, B. A. Differential protein expression during growth on medium versus long-chain alkanes in the obligate marine hydrocarbon-degrading bacterium Thalassolituus oleivorans MIL-1. Front. Microbiol. 9, 3130 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Pasternak, Z., Ben Sasson, T., Cohen, Y., Segev, E. & Jurkevitch, E. A new comparative-genomics approach for defining phenotype-specific indicators reveals specific genetic markers in predatory bacteria. PLoS One. 10, e0142933. https://doi.org/10.1371/journal.pone.0142933 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Yakimov, M. M. et al. Thalassolituus oleivorans gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int. J. Syst. Evol. Microbiol. 54, 141–148 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Wang, Y., Yu, M., Liu, Y., Yang, X. & Zhang, X. H. Bacterioplanoides pacificum gen. nov., sp. nov., isolated from seawater of South Pacific Gyre. Int. J. Syst. Evol. Microbiol. 66, 5010–5015 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Bowditch, R. D., Baumann, L. & Baumann, P. Description of Oceanospirillum kriegii sp. nov. and O. jannaschii sp. nov. and assignment of two species of Alteromonas to this genus as O. commune comb. nov. and O. vagum comb. nov. Curr. Microbiol. 10, 221–229 (1984).CAS 
    Article 

    Google Scholar 
    26.Dong, C., Chen, X., Xie, Y., Lai, Q. & Shao, Z. Complete genome sequence of Thalassolituus oleivorans R6-15, an obligate hydrocarbonoclastic marine bacterium from the Arctic Ocean. Stand Genom. Sci. 9, 893–901 (2014).Article 

    Google Scholar 
    27.Choi, A. & Cho, J.-C. Thalassolituus marinus sp. nov., a hydrocarbon utilizing marine bacterium. Int. J. Syst. Evol. Microbiol. 63, 2234–2238 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Alain, K., Harder, J., Widdel, F. & Zengler, K. Anaerobic utilization of toluene by marine alpha- and gammaproteobacteria reducing nitrate. Microbiology 158, 2946–2957 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Liu, J., Wu, W., Chen, C., Sun, F. & Chen, Y. Prokaryotic diversity, composition structure, and phylogenetic analysis of microbial communities in leachate sediment ecosystems. Appl. Microbiol. Biotechnol. 91, 1659–1675 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Yakimov, M. M., Timmis, K. N. & Golyshin, P. N. Obligate oil-degrading marine bacteria. Curr. Opin. Biotechnol. 18, 257–266 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.McKew, B. A. et al. Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic bacteria. Environ. Microbiol. 9, 1562–1571 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Satomi, M., Kimura, B., Hamada, T., Harayama, S. & Fujii, T. Phylogenetic study of the genus Oceanospirillum based on 16S rRNA and gyrB genes: emended description of the genus Oceanospirillum, description of Pseudospirillum gen. nov., Oceanobacter gen. nov. and Terasakiella gen. nov. and transfer of Oceanospirillum jannaschii and Pseudomonas stanieri to Marinobacterium as Marinobacterium jannaschii comb. nov. and Marinobacterium stanieri comb. no. Int. J. Syst. Evol. Microbiol. 52, 739–747 (2002).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    33.Qin, Q. L. et al. A proposed genus boundary for the prokaryotes based on genomic insights. J. Bacteriol. 196, 2210–2215 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Nicholson, A. C. et al. Division of the genus Chryseobacterium: Observation of discontinuities in amino acid identity values, a possible consequence of major extinction events, guides transfer of nine species to the genus Epilithonimonas, eleven species to the genus Kaistella, and three species to the genus Halpernia gen. nov., with description of Kaistella daneshvariae sp. nov. and Epilithonimonas vandammei sp. nov. derived from clinical specimens. Int. J. Syst. Evol. Microbiol. 70, 4432–4450 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Yarza, P. et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12, 635–645 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Barco, R. A. et al. A genus definition for Bacteria and Archaea based on a standard genome relatedness index. MBio 11, e02475-192020. https://doi.org/10.1128/mBio.02475-19 (2020).Article 

    Google Scholar 
    37.Andersson, J. O. & Andersson, S. G. Insights into the evolutionary process of genome degradation. Curr. Opin. Genet. Dev. 9, 664–671 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Wall, D. & Kaiser, D. Type IV pili and cell motility. Mol. Microbiol. 32, 1–10 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Jenal, U. & Malone, J. Mechanisms of cyclic-di-GMP signaling in bacteria. Ann. Rev. Genet. 40, 385–407 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Dow, J. M., Fouhy, Y., Lucey, J. F. & Ryan, R. P. The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants. Mol. Plant Microbe Interact. 19, 1378–1384 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Hobley, L. et al. Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus. PLoS Pathog. 8, e1002493. https://doi.org/10.1371/journal.ppat.1002493 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Seccareccia, I., Kovács, Á. T., Gallegos-Monterrosa, R. & Nett, M. Unraveling the predator-prey relationship of Cupriavidus necator and Bacillus subtilis. Microbiol. Res. 192, 231–238 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Mu, D. S. et al. Bradymonabacteria, a novel bacterial predator group with versatile survival strategies in saline environments. Microbiome 8, 1262020 (2020).Article 

    Google Scholar 
    44.Zepeda, V. K. et al. Terasakiispira papahanaumokuakeensis gen. nov., sp. nov., a gammaproteobacterium from Pearl and Hermes Atoll, Northwestern Hawaiian Islands. Int. J. Syst. Evol. Microbiol. 65, 3609–3617 (2015).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    45.Terasaki, Y. Transfer of five species and two subspecies of Spirillum to other genera (Aquaspirillum and Oceanospirillum), with emended descriptions of the species and subspecies. Int. J. Syst. Evol. Microbiol. 29, 130–144 (1979).
    Google Scholar 
    46.Baker, D. A. & Park, R. W. Changes in morphology and cell wall structure that occur during growth of Vibrio sp. NCTC4716 in batch culture. J. Gen. Microbiol. 86, 12–28 (1975).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Ng, L. K., Sherburne, R., Taylor, D. E. & Stiles, M. E. Morphological forms and viability of Campylobacter species studied by electron microscopy. J. Bacteriol. 164, 338–343 (1985).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Reshetnyak, V. I. & Reshetnyak, T. M. Significance of dormant forms of Helicobacter pylori in ulcerogenesis. World J. Gastroenterol. 23, 4867–4878 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Loc Carrillo, C. et al. Bacteriophage therapy to reduce Campylobacter jejuni colonization of broiler chickens. Appl. Environ. Microbiol. 71, 6554–6563 (2005).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Clinical and Laboratory Standards Institute. Methods for determining bactericidal activity of antimicrobial agents; approved guideline M26-A. Clin. Lab. Stand. Inst. 19, 7 (1999).
    Google Scholar 
    51.Legat, A., Gruber, C., Zangger, K., Wanner, G. & Stan-Lotter, H. Identification of polyhydroxyalkanoates in Halococcus and other haloarchaeal species. Appl. Microbiol. Biotechnol. 87, 1119–1127 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    53.Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526 (1993).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791 (1985).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Rodriguez-R, L. M. & Konstantinidis, K. T. Bypassing cultivation to identify bacterial species. Microbe 9, 111–118 (2014).
    Google Scholar 
    56.Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Blue carbon as a natural climate solution

    1.Nesshöver, C. et al. The science, policy and practice of nature-based solutions: an interdisciplinary perspective. Sci. Total Environ. 579, 1215–1227 (2017).Article 

    Google Scholar 
    2.Chausson, A. et al. Mapping the effectiveness of nature-based solutions for climate change adaptation. Glob. Chang. Biol. 26, 6134–6155 (2020).Article 

    Google Scholar 
    3.Pires, J. C. M. Negative emissions technologies: a complementary solution for climate change mitigation. Sci. Total Environ. 672, 502–514 (2019).Article 

    Google Scholar 
    4.McLaren, D. A comparative global assessment of potential negative emissions technologies. Process Saf. Environ. Prot. 90, 489–500 (2012).Article 

    Google Scholar 
    5.Anderson, K. & Peters, G. The trouble with negative emissions. Science 354, 182–183 (2016).Article 

    Google Scholar 
    6.Nellemann, C. et al. Blue Carbon — The Role of Healthy Oceans in Binding Carbon (UN Environment, 2009).7.Barbier, E. B. et al. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193 (2011).Article 

    Google Scholar 
    8.Himes-Cornell, A., Grose, S. O. & Pendleton, L. Mangrove ecosystem service values and methodological approaches to valuation: where do we stand? Front. Mar. Sci. 5, 376 (2018).Article 

    Google Scholar 
    9.Friess, D. A. et al. in Oceanography and Marine Biology Vol. 58 Ch. 3 (CRC, 2020).10.Lovelock, C. E. & Duarte, C. M. Dimensions of blue carbon and emerging perspectives. Biol. Lett. 15 https://doi.org/10.1098/rsbl.2018.0781 (2019).11.Duarte, C. M., Losada, I. J., Hendriks, I. E., Mazarrasa, I. & Marbà, N. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Chang. 3, 961–968 (2013).Article 

    Google Scholar 
    12.Duarte, C. M., Middelburg, J. J. & Caraco, N. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2, 1–8 (2005).Article 

    Google Scholar 
    13.Mcleod, E. et al. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front. Ecol. Environ. 9, 552–560 (2011).Article 

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

    Google Scholar 
    15.Macreadie, P. I. et al. Vulnerability of seagrass blue carbon to microbial attack following exposure to warming and oxygen. Sci. Total Environ. 686, 264–275 (2019).Article 

    Google Scholar 
    16.Sippo, J. Z., Lovelock, C. E., Santos, I. R., Sanders, C. J. & Maher, D. T. Mangrove mortality in a changing climate: an overview. Estuar. Coast. Shelf Sci. 215, 241–249 (2018).Article 

    Google Scholar 
    17.Lovelock, C. E. et al. Assessing the risk of carbon dioxide emissions from blue carbon ecosystems. Front. Ecol. Environ. 15, 257–265 (2017).Article 

    Google Scholar 
    18.Zhao, Q. et al. Where marine protected areas would best represent 30% of ocean biodiversity. Biol. Conserv. 244, 108536 (2020).Article 

    Google Scholar 
    19.Duarte, C. M. et al. Rebuilding marine life. Nature 580, 39–51 (2020).Article 

    Google Scholar 
    20.Bayraktarov, E. et al. The cost and feasibility of marine coastal restoration. Ecol. Appl. 26, 1055–1074 (2016).Article 

    Google Scholar 
    21.Van, T. T. et al. Changes in mangrove vegetation area and character in a war and land use change affected region of Vietnam (Mui Ca Mau) over six decades. Acta Oecol. 63, 71–81 (2015).Article 

    Google Scholar 
    22.Dung, L. V., Tue, N. T., Nhuan, M. T. & Omori, K. Carbon storage in a restored mangrove forest in Can Gio Mangrove Forest Park, Mekong Delta, Vietnam. For. Ecol. Manage. 380, 31–40 (2016).Article 

    Google Scholar 
    23.Nam, V. N., Sasmito, S. D., Murdiyarso, D., Purbopuspito, J. & MacKenzie, R. A. Carbon stocks in artificially and naturally regenerated mangrove ecosystems in the Mekong Delta. Wetl. Ecol. Manag. 24, 231–244 (2016).Article 

    Google Scholar 
    24.Reynolds, L. K., Waycott, M., McGlathery, K. J. & Orth, R. J. Ecosystem services returned through seagrass restoration. Restor. Ecol. 24, 583–588 (2016).Article 

    Google Scholar 
    25.Das, S. Ecological restoration and livelihood: contribution of planted mangroves as nursery and habitat for artisanal and commercial fishery. World Dev. 94, 492–502 (2017).Article 

    Google Scholar 
    26.Kiesel, J. et al. Effective design of managed realignment schemes can reduce coastal flood risks. Estuar. Coast. Shelf Sci. 242, 106844 (2020).Article 

    Google Scholar 
    27.McNally, C. G., Uchida, E. & Gold, A. J. The effect of a protected area on the tradeoffs between short-run and long-run benefits from mangrove ecosystems. Proc. Natl Acad. Sci. USA 108, 13945–13950 (2011).Article 

    Google Scholar 
    28.Chow, J. Mangrove management for climate change adaptation and sustainable development in coastal zones. J. Sustain. For. 37, 139–156 (2018).Article 

    Google Scholar 
    29.Dasgupta, S., Islam, M. S., Huq, M., Huque Khan, Z. & Hasib, M. R. Quantifying the protective capacity of mangroves from storm surges in coastal Bangladesh. PLoS ONE 14, e0214079 (2019).Article 

    Google Scholar 
    30.Sutton-Grier, A. E. & Moore, A. Leveraging carbon services of coastal ecosystems for habitat protection and restoration. Coast. Manag. 44, 259–277 (2016).Article 

    Google Scholar 
    31.Owuor, M. A., Mulwa, R., Otieno, P., Icely, J. & Newton, A. Valuing mangrove biodiversity and ecosystem services: a deliberative choice experiment in Mida Creek, Kenya. Ecosyst. Serv. 40, 101040 (2019).Article 

    Google Scholar 
    32.Mcowen, C. J. et al. A global map of saltmarshes. Biodivers. Data J. 5, e11764 (2018).Article 

    Google Scholar 
    33.Bunting, P. et al. The global mangrove watch — a new 2010 global baseline of mangrove extent. Remote Sens. 10, 1669 (2018).Article 

    Google Scholar 
    34.Jayathilake, D. R. M. & Costello, M. J. A modelled global distribution of the seagrass biome. Biol. Conserv. 226, 120–126 (2018).Article 

    Google Scholar 
    35.McKenzie, L. J. et al. The global distribution of seagrass meadows. Environ. Res. Lett. 15, 74041 (2020).Article 

    Google Scholar 
    36.Trumbore, S. E. Potential responses of soil organic carbon to global environmental change. Proc. Natl Acad. Sci. USA 94, 8284–8291 (1997).Article 

    Google Scholar 
    37.Hamilton, S. E. & Friess, D. A. Global carbon stocks and potential emissions due to mangrove deforestation from 2000 to 2012. Nat. Clim. Chang. 8, 240–244 (2018).Article 

    Google Scholar 
    38.Ouyang, X. & Lee, S. Y. Improved estimates on global carbon stock and carbon pools in tidal wetlands. Nat. Commun. 11, 317 (2020).Article 

    Google Scholar 
    39.Kauffman, J. B. et al. Total ecosystem carbon stocks of mangroves across broad global environmental and physical gradients. Ecol. Monogr. 90, e01405 (2020).Article 

    Google Scholar 
    40.Simard, M. et al. Mangrove canopy height globally related to precipitation, temperature and cyclone frequency. Nat. Geosci. 12, 40–45 (2019).Article 

    Google Scholar 
    41.Hutchison, J., Manica, A., Swetnam, R., Balmford, A. & Spalding, M. Predicting global patterns in mangrove forest biomass. Conserv. Lett. 7, 233–240 (2014).Article 

    Google Scholar 
    42.Atwood, T. B. et al. Global patterns in mangrove soil carbon stocks and losses. Nat. Clim. Chang. 7, 523–528 (2017).Article 

    Google Scholar 
    43.Sanderman, J. et al. A global map of mangrove forest soil carbon at 30 m spatial resolution. Environ. Res. Lett. 13, 55002 (2018).Article 

    Google Scholar 
    44.Traganos, D. et al. Towards global-scale seagrass mapping and monitoring using Sentinel-2 on Google Earth Engine: the case study of the Aegean and Ionian Seas. Remote Sens. 10, 1227 (2018).Article 

    Google Scholar 
    45.Hossain, M. S. & Hashim, M. Potential of Earth Observation (EO) technologies for seagrass ecosystem service assessments. Int. J. Appl. Earth Obs. Geoinf. 77, 15–29 (2019).Article 

    Google Scholar 
    46.Atwood, T. B., Witt, A., Mayorga, J., Hammill, E. & Sala, E. Global patterns in marine sediment carbon stocks. Front. Mar. Sci. 7, 165 (2020).Article 

    Google Scholar 
    47.Coastal carbon atlas. Coastal Carbon Research Coordination Network. CCRCN https://ccrcn.shinyapps.io/CoastalCarbonAtlas/_w_8595a9b5/#tab-6425-6 (2019).48.UNEP-WCMC. Ocean data viewer: global distribution of seagrasses. UNEP https://doi.org/10.34892/x6r3-d211 (2018).49.Hammerstrom, K. K., Kenworthy, W. J., Fonseca, M. S. & Whitfield, P. E. Seed bank, biomass, and productivity of Halophila decipiens, a deep water seagrass on the west Florida continental shelf. Aquat. Bot. 84, 110–120 (2006).Article 

    Google Scholar 
    50.Pergent-Martini, C. et al. Descriptors of Posidonia oceanica meadows: use and application. Ecol. Indic. 5, 213–230 (2005).Article 

    Google Scholar 
    51.Esteban, N., Unsworth, R. K. F., Gourlay, J. B. Q. & Hays, G. C. The discovery of deep-water seagrass meadows in a pristine Indian Ocean wilderness revealed by tracking green turtles. Mar. Pollut. Bull. 134, 99–105 (2018).Article 

    Google Scholar 
    52.York, P. H. et al. Dynamics of a deep-water seagrass population on the Great Barrier Reef: annual occurrence and response to a major dredging program. Sci. Rep. 5, 13167 (2015).Article 

    Google Scholar 
    53.Serrano, O. et al. Australian vegetated coastal ecosystems as global hotspots for climate change mitigation. Nat. Commun. 10, 4313 (2019).Article 

    Google Scholar 
    54.Chmura, G. L., Anisfeld, S. C., Cahoon, D. R. & Lynch, J. C. Global carbon sequestration in tidal, saline wetland soils. Glob. Biogeochem. Cycles 17, 1111 (2003).Article 

    Google Scholar 
    55.Hengl, T. et al. SoilGrids250m: global gridded soil information based on machine learning. PLoS ONE 12, e0169748 (2017).Article 

    Google Scholar 
    56.Rogers, K. et al. Wetland carbon storage controlled by millennial-scale variation in relative sea-level rise. Nature 567, 91–95 (2019).Article 

    Google Scholar 
    57.Rovai, A. S. et al. Global controls on carbon storage in mangrove soils. Nat. Clim. Chang. 8, 534–538 (2018).Article 

    Google Scholar 
    58.Worthington, T. A. et al. A global biophysical typology of mangroves and its relevance for ecosystem structure and deforestation. Sci. Rep. 10, 14652 (2020).Article 

    Google Scholar 
    59.Maher, D. T., Call, M., Santos, I. R. & Sanders, C. J. Beyond burial: lateral exchange is a significant atmospheric carbon sink in mangrove forests. Biol. Lett. 14, 20180200 (2018).Article 

    Google Scholar 
    60.Santos, I. R., Maher, D. T., Larkin, R., Webb, J. R. & Sanders, C. J. Carbon outwelling and outgassing vs. burial in an estuarine tidal creek surrounded by mangrove and saltmarsh wetlands. Limnol. Ocean 64, 996–1013 (2019).Article 

    Google Scholar 
    61.Kelleway, J. J. et al. A national approach to greenhouse gas abatement through blue carbon management. Glob. Environ. Chang. 63, 102083 (2020).Article 

    Google Scholar 
    62.Goldberg, L., Lagomasino, D., Thomas, N. & Fatoyinbo, T. Global declines in human-driven mangrove loss. Glob. Chang. Biol. 68, 5844–5855 (2020).Article 

    Google Scholar 
    63.Richards, D. R. & Friess, D. A. Rates and drivers of mangrove deforestation in Southeast Asia, 2000–2012. Proc. Natl. Acad. Sci. 113, 344–349 (2016).Article 

    Google Scholar 
    64.Thomas, N. et al. Distribution and drivers of global mangrove forest change, 1996–2010. PLoS ONE 12, e0179302 (2017).Article 

    Google Scholar 
    65.Worthington, T. & Spalding, M. Mangrove restoration potential: a global map highlighting a critical opportunity (OECD, 2018).66.Kearney, M. S., Riter, J. C. A. & Turner, R. E. Freshwater river diversions for marsh restoration in Louisiana: twenty-six years of changing vegetative cover and marsh area. Geophys. Res. Lett. 38, 16405 (2011).Article 

    Google Scholar 
    67.Lee, S. Y., Hamilton, S., Barbier, E. B., Primavera, J. & Lewis, R. R. Better restoration policies are needed to conserve mangrove ecosystems. Nat. Ecol. Evol. 3, 870–872 (2019).Article 

    Google Scholar 
    68.Lovelock, C. E. & Brown, B. M. Land tenure considerations are key to successful mangrove restoration. Nat. Ecol. Evol. 3, 1135 (2019).Article 

    Google Scholar 
    69.Herr, D., Blum, J., Himes-Cornell, A. & Sutton-Grier, A. An analysis of the potential positive and negative livelihood impacts of coastal carbon offset projects. J. Environ. Manag. 235, 463–479 (2019).Article 

    Google Scholar 
    70.Mojica Vélez, J. M., Barrasa García, S. & Espinoza Tenorio, A. Policies in coastal wetlands: key challenges. Environ. Sci. Policy 88, 72–82 (2018).Article 

    Google Scholar 
    71.Zeng, Y. et al. Economic and social constraints on reforestation for climate mitigation in Southeast Asia. Nat. Clim. Chang. 10, 842–844 (2020).Article 

    Google Scholar 
    72.van Katwijk, M. M. et al. Global analysis of seagrass restoration: the importance of large-scale planting. J. Appl. Ecol. 53, 567–578 (2016).Article 

    Google Scholar 
    73.Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl Acad. Sci. USA 106, 12377–12381 (2009).Article 

    Google Scholar 
    74.Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996 (2006).Article 

    Google Scholar 
    75.Tan, Y. M. et al. Seagrass restoration is possible: insights and lessons from Australia and New Zealand. Front. Mar. Sci. 7, 617 (2020).Article 

    Google Scholar 
    76.Greiner, J. T., McGlathery, K. J., Gunnell, J. & McKee, B. A. Seagrass restoration enhances ‘blue carbon’ sequestration in coastal waters. PLoS ONE 8, e72469 (2013).Article 

    Google Scholar 
    77.Orth, R. J. et al. Restoration of seagrass habitat leads to rapid recovery of coastal ecosystem services. Sci. Adv. 6, eabc6434 (2020).Article 

    Google Scholar 
    78.Cunha, A. H. et al. Changing paradigms in seagrass restoration. Restor. Ecol. 20, 427–430 (2012).Article 

    Google Scholar 
    79.Rezek, R. J., Furman, B. T., Jung, R. P., Hall, M. O. & Bell, S. S. Long-term performance of seagrass restoration projects in Florida, USA. Sci. Rep. 9, 15514 (2019).Article 

    Google Scholar 
    80.Worthington, T. A. et al. Harnessing big data to support the conservation and rehabilitation of mangrove forests globally. One Earth 2, 429–443 (2020).Article 

    Google Scholar 
    81.Kandus, P. et al. Remote sensing of wetlands in South America: status and challenges. Int. J. Remote Sens. 39, 993–1016 (2018).Article 

    Google Scholar 
    82.Gallant, A. L. The challenges of remote monitoring of wetlands. Remote Sens. 7, 10938–10950 (2015).Article 

    Google Scholar 
    83.Unsworth, R. K. F. et al. Sowing the seeds of seagrass recovery using hessian bags. Front. Ecol. Evol. 7, 311 (2019).Article 

    Google Scholar 
    84.Duarte, C. M., Dennison, W. C., Orth, R. J. W. & Carruthers, T. J. B. The charisma of coastal ecosystems: addressing the imbalance. Estuaries Coasts 31, 233–238 (2008).Article 

    Google Scholar 
    85.de los Santos, C. B. et al. Recent trend reversal for declining European seagrass meadows. Nat. Commun. 10, 3356 (2019).Article 

    Google Scholar 
    86.Hamilton, S. E. & Casey, D. Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC-21). Glob. Ecol. Biogeogr. 25, 729–738 (2016).Article 

    Google Scholar 
    87.Pendleton, L. et al. Estimating global “blue carbon” emissions from conversion and degradation of vegetated coastal ecosystems. PLoS ONE 7, e43542 (2012).Article 

    Google Scholar 
    88.Deegan, L. A. et al. Coastal eutrophication as a driver of salt marsh loss. Nature 490, 388–392 (2012).Article 

    Google Scholar 
    89.Cardoso, P. G., Raffaelli, D. & Pardal, M. A. The impact of extreme weather events on the seagrass Zostera noltii and related Hydrobia ulvae population. Mar. Pollut. Bull. 56, 483–492 (2008).Article 

    Google Scholar 
    90.Rogers, K. Accommodation space as a framework for assessing the response of mangroves to relative sea-level rise. Singap. J. Trop. Geogr. 42, 163–183 (2021).Article 

    Google Scholar 
    91.Marbà, N. & Duarte, C. M. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Glob. Chang. Biol. 16, 2366–2375 (2010).Article 

    Google Scholar 
    92.Lefcheck, J. S., Wilcox, D. J., Murphy, R. R., Marion, S. R. & Orth, R. J. Multiple stressors threaten the imperiled coastal foundation species eelgrass (Zostera marina) in Chesapeake Bay, USA. Glob. Chang. Biol. 23, 3474–3483 (2017).Article 

    Google Scholar 
    93.Arias-Ortiz, A. et al. A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat. Clim. Chang. 8, 338–344 (2018).Article 

    Google Scholar 
    94.Kendrick, G. A. et al. A systematic review of how multiple stressors from an extreme event drove ecosystem-wide loss of resilience in an iconic seagrass community. Front. Mar. Sci. 6, 455 (2019).Article 

    Google Scholar 
    95.Duke, N. C. et al. Large-scale dieback of mangroves in Australia’s Gulf of Carpentaria: a severe ecosystem response, coincidental with an unusually extreme weather event. Mar. Freshw. Res. 68, 1816–1829 (2017).Article 

    Google Scholar 
    96.Taillie, P. J. et al. Widespread mangrove damage resulting from the 2017 Atlantic mega hurricane season. Environ. Res. Lett. 15, 64010 (2020).Article 

    Google Scholar 
    97.Asbridge, E., Lucas, R., Rogers, K. & Accad, A. The extent of mangrove change and potential for recovery following severe Tropical Cyclone Yasi, Hinchinbrook Island, Queensland, Australia. Ecol. Evol. 8, 10416–10434 (2018).Article 

    Google Scholar 
    98.Hickey, S. M. et al. Is climate change shifting the poleward limit of mangroves? Estuaries Coasts 40, 1215–1226 (2017).Article 

    Google Scholar 
    99.Saintilan, N., Wilson, N. C., Rogers, K., Rajkaran, A. & Krauss, K. W. Mangrove expansion and salt marsh decline at mangrove poleward limits. Glob. Chang. Biol. 20, 147–157 (2014).Article 

    Google Scholar 
    100.Whitt, A. A. et al. March of the mangroves: drivers of encroachment into southern temperate saltmarsh. Estuar. Coast. Shelf Sci. 240, 106776 (2020).Article 

    Google Scholar 
    101.Cavanaugh, K. C. et al. Sensitivity of mangrove range limits to climate variability. Glob. Ecol. Biogeogr. 27, 925–935 (2018).Article 

    Google Scholar 
    102.Cavanaugh, K. C. et al. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proc. Natl Acad. Sci. USA 111, 723–727 (2014).Article 

    Google Scholar 
    103.Coldren, G. A., Langley, J. A., Feller, I. C. & Chapman, S. K. Warming accelerates mangrove expansion and surface elevation gain in a subtropical wetland. J. Ecol. 107, 79–90 (2019).Article 

    Google Scholar 
    104.Yando, E. S. et al. Salt marsh–mangrove ecotones: using structural gradients to investigate the effects of woody plant encroachment on plant–soil interactions and ecosystem carbon pools. J. Ecol. 104, 1020–1031 (2016).Article 

    Google Scholar 
    105.Doughty, C. L. et al. Mangrove range expansion rapidly increases coastal wetland carbon storage. Estuaries Coasts 39, 385–396 (2016).Article 

    Google Scholar 
    106.Lovelock, C. E. et al. Sea level and turbidity controls on mangrove soil surface elevation change. Estuar. Coast. Shelf Sci. 153, 1–9 (2015).Article 

    Google Scholar 
    107.Woodroffe, C. D. et al. Mangrove sedimentation and response to relative sea-level rise. Ann. Rev. Mar. Sci. 8, 243–266 (2016).Article 

    Google Scholar 
    108.Lovelock, C. E. & Reef, R. Variable impacts of climate change on blue carbon. One Earth 3, 195–211 (2020).Article 

    Google Scholar 
    109.Saintilan, N. et al. Thresholds of mangrove survival under rapid sea level rise. Science 368, 1118–1121 (2020).Article 

    Google Scholar 
    110.Nicholls, R. J. Coastal flooding and wetland loss in the 21st century: changes under the SRES climate and socio-economic scenarios. Glob. Environ. Chang. 14, 69–86 (2004).Article 

    Google Scholar 
    111.Schuerch, M. et al. Future response of global coastal wetlands to sea-level rise. Nature 561, 231–234 (2018).Article 

    Google Scholar 
    112.Adame, M. F. et al. Future carbon emissions from global mangrove forest loss. Glob. Chang. Biol. 27, 2856–2866 (2021).Article 

    Google Scholar 
    113.Griscom, B. W. et al. Natural climate solutions. Proc. Natl Acad. Sci. USA 114, 11645–11650 (2017).Article 

    Google Scholar 
    114.Friedlingstein, P. et al. Global Carbon Budget 2020. Earth Syst. Sci. Data 12, 3269–3340 (2020).Article 

    Google Scholar 
    115.Morris, R. L., Boxshall, A. & Swearer, S. E. Climate-resilient coasts require diverse defence solutions. Nat. Clim. Chang. 10, 485–487 (2020).Article 

    Google Scholar 
    116.Macreadie, P. I. et al. The future of blue carbon science. Nat. Commun. 10, 3998 (2019).Article 

    Google Scholar 
    117.Wylie, L., Sutton-Grier, A. E. & Moore, A. Keys to successful blue carbon projects: lessons learned from global case studies. Mar. Policy 65, 76–84 (2016).Article 

    Google Scholar 
    118.Howard, J. F. et al. Clarifying the role of coastal and marine systems in climate mitigation. Front. Ecol. Environ. 15, 42–50 (2017).Article 

    Google Scholar 
    119.Lenihan, H. S. & Peterson, C. H. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oysters reefs. Ecol. Appl. 8, 128–140 (1998).Article 

    Google Scholar 
    120.Ellison, A. M., Felson, A. J. & Friess, D. A. Mangrove rehabilitation and restoration as experimental adaptive management. Front. Mar. Sci. 7, 327 (2020).Article 

    Google Scholar 
    121.Lester, S. E., Dubel, A. K., Hernan, G., McHenry, J. & Rassweiler, A. Spatial planning principles for marine ecosystem restoration. Front. Mar. Sci. 7, 328 (2020).Article 

    Google Scholar 
    122.Herr, D. & Landis, E. Coastal blue carbon ecosystems: opportunities for nationally determined contributions. Policy brief (IUCN, 2016).123.Apple Newsroom. Conserving mangroves, a lifeline for the world. Apple (22 April 2019) https://www.apple.com/newsroom/2019/04/conserving-mangroves-a-lifeline-for-the-world124.Hochard, J. P., Hamilton, S. & Barbier, E. B. Mangroves shelter coastal economic activity from cyclones. Proc. Natl Acad. Sci. USA 116, 12232–12237 (2019).Article 

    Google Scholar 
    125.Herr, D., von Unger, M., Laffoley, D. & McGivern, A. Pathways for implementation of blue carbon initiatives. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 116–129 (2017).Article 

    Google Scholar 
    126.Friess, D. A. et al. in Sustainable Development Goals: Their Impacts on Forests and People Ch. 14 (eds Katila, P. et al.) 445–481 (Cambridge Univ. Press, 2019).127.Waltham, N. J. et al. UN Decade on Ecosystem Restoration 2021–2030 — what chance for success in restoring coastal ecosystems? Front. Mar. Sci. 7, 71 (2020).Article 

    Google Scholar 
    128.Convention on Biological Diversity. Conference of the Parties Decision X/2: strategic plan for biodiversity 2011–2020. CBD https://www.cbd.int/decision/cop/?id=12268 (2011).129.United Nations. Transforming our world: the 2030 Agenda for Sustainable Development (UN, 2015).130.Brander, L. M. et al. The global costs and benefits of expanding marine protected areas. Mar. Policy 116, 103953 (2020).Article 

    Google Scholar 
    131.Howard, J. F. et al. The potential to integrate blue carbon into MPA design and management. Aquat. Conserv. 27, 100–115 (2017).Article 

    Google Scholar 
    132.Needelman, B. A. et al. The science and policy of the Verified Carbon Standard methodology for tidal wetland and seagrass restoration. Estuaries Coasts 41, 2159–2171 (2018).Article 

    Google Scholar 
    133.Michaelowa, A., Hermwille, L., Obergassel, W. & Butzengeiger, S. Additionality revisited: guarding the integrity of market mechanisms under the Paris Agreement. Clim. Policy 19, 1211–1224 (2019).Article 

    Google Scholar 
    134.Intergovernmental Panel on Climate Change. 2013 Supplement to the 2006 IPCC guidelines for national greenhouse gas inventories: wetlands (IPCC, 2014).135.United Nations Environment Programme. Out of the blue: the value of seagrasses to the environment and to people (UNEP, 2020).136.Murdiyarso, D. et al. The potential of Indonesian mangrove forests for global climate change mitigation. Nat. Clim. Chang. 5, 1089–1092 (2015).Article 

    Google Scholar 
    137.Jones, T. et al. Madagascar’s mangroves: quantifying nation-wide and ecosystem specific dynamics, and detailed contemporary mapping of distinct ecosystems. Remote Sens. 8, 106 (2016).Article 

    Google Scholar 
    138.Holmquist, J. R. et al. Uncertainty in United States coastal wetland greenhouse gas inventorying. Environ. Res. Lett. 13, 115005 (2018).Article 

    Google Scholar 
    139.Maher, D. T., Drexl, M., Tait, D. R., Johnston, S. G. & Jeffrey, L. C. iAMES: an inexpensive, automated methane ebullition sensor. Environ. Sci. Technol. 53, 6420–6426 (2019).Article 

    Google Scholar 
    140.Primavera, J. H. & Esteban, J. M. A. A review of mangrove rehabilitation in the Philippines: successes, failures and future prospects. Wetl. Ecol. Manag. 16, 345–358 (2008).Article 

    Google Scholar 
    141.Silliman, B. R. et al. Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc. Natl Acad. Sci. USA 112, 14295–14300 (2015).Article 

    Google Scholar 
    142.Enwright, N. M., Griffith, K. T. & Osland, M. J. Barriers to and opportunities for landward migration of coastal wetlands with sea-level rise. Front. Ecol. Environ. 14, 307–316 (2016).Article 

    Google Scholar 
    143.Burkholz, C., Garcias-Bonet, N. & Duarte, C. M. Warming enhances carbon dioxide and methane fluxes from Red Sea seagrass (Halophila stipulacea) sediments. Biogeosciences 17, 1717–1730 (2020).Article 

    Google Scholar 
    144.Bianchi, T. S. et al. Historical reconstruction of mangrove expansion in the Gulf of Mexico: linking climate change with carbon sequestration in coastal wetlands. Estuar. Coast. Shelf Sci. 119, 7–16 (2013).Article 

    Google Scholar 
    145.Apostolaki, E. T. et al. Exotic Halophila stipulacea is an introduced carbon sink for the eastern Mediterranean Sea. Sci. Rep. 9, 9643 (2019).Article 

    Google Scholar 
    146.Bell, J. & Lovelock, C. E. Insuring mangrove forests for their role in mitigating coastal erosion and storm-surge: an Australian case study. Wetlands 33, 279–289 (2013).Article 

    Google Scholar 
    147.Reguero, B. G. et al. Financing coastal resilience by combining nature-based risk reduction with insurance. Ecol. Econ. 169, 106487 (2020).Article 

    Google Scholar 
    148.Thomas, S. Blue carbon: knowledge gaps, critical issues, and novel approaches. Ecol. Econ. 107, 22–38 (2014).Article 

    Google Scholar 
    149.International Partnership for Blue Carbon. Blue carbon partnership. IPBC https://bluecarbonpartnership.org (2017).150.Boon, P. I. & Prahalad, V. Ecologists, economics and politics: problems and contradictions in applying neoliberal ideology to nature conservation in Australia. Pac. Conserv. Biol. 23, 115–132 (2017).Article 

    Google Scholar 
    151.Adame, M. F. et al. The undervalued contribution of mangrove protection in Mexico to carbon emission targets. Conserv. Lett. 11, e12445 (2018).Article 

    Google Scholar 
    152.Bell-James, J. & Lovelock, C. E. Legal barriers and enablers for reintroducing tides: an Australian case study in reconverting ponded pasture for climate change mitigation. Land Use Policy 88, 104192 (2019).Article 

    Google Scholar 
    153.Gattuso, J.-P. et al. Ocean solutions to address climate change and its effects on marine ecosystems. Front. Mar. Sci. 5, 337 (2018).Article 

    Google Scholar 
    154.Saderne, V. et al. Role of carbonate burial in blue carbon budgets. Nat. Commun. 10, 1106 (2019).Article 

    Google Scholar 
    155.Duarte, C. M., Wu, J., Xiao, X., Bruhn, A. & Krause-Jensen, D. Can seaweed farming play a role in climate change mitigation and adaptation? Front. Mar. Sci. 4, 100 (2017).
    Google Scholar 
    156.Froehlich, H. E., Afflerbach, J. C., Frazier, M. & Halpern, B. S. Blue growth potential to mitigate climate change through seaweed offsetting. Curr. Biol. 29, 3087–3093.e3 (2019).Article 

    Google Scholar 
    157.Ritchie, H. & Roser, M. CO2 and greenhouse gas emissions. Our World in Data https://ourworldindata.org/co2-and-other-greenhouse-gas-emissions (2017).158.Smith, S. V. Marine macrophytes as a global carbon sink. Science 211, 838–840 (1981).Article 

    Google Scholar 
    159.Intergovernmental Panel on Climate Change. Special report on the ocean and cryosphere in a changing climate (IPCC, 2019).160.Verified Carbon Standard. VM0007 REDD+ methodology framework (REDD+MF) (VCS, 2020).161.Carnell, P. E. et al. Mapping ocean wealth Australia: the value of coastal wetlands to people and nature. The Nature Conservancy https://doi.org/10.21153/carnell2019mapping (2019).162.Jänes, H. et al. Stable isotopes infer the value of Australia’s coastal vegetated ecosystems from fisheries. Fish Fish. 21, 80–90 (2020).Article 

    Google Scholar 
    163.Jänes, H. et al. Quantifying fisheries enhancement from coastal vegetated ecosystems. Ecosyst. Serv. 43, 101105 (2020).Article 

    Google Scholar 
    164.Huang, B. et al. Quantifying welfare gains of coastal and estuarine ecosystem rehabilitation for recreational fisheries. Sci. Total Environ. 710, 134680 (2020).Article 

    Google Scholar  More

  • in

    A large invasive consumer reduces coastal ecosystem resilience by disabling positive species interactions

    1.Vilà, M. et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Vitousek, P. M., DAntonio, C. M., Loope, L. L., Westbrooks, R. & D’Antonio, C. M. Biological invasions as global environmental change. Am. Sci. 84, 468–478 (1996).ADS 

    Google Scholar 
    3.Pejchar, L. & Mooney, H. A. Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 24, 497–504 (2009).PubMed 
    Article 

    Google Scholar 
    4.Ehrenfeld, J. G. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol. Syst. 41, 59–80 (2010).Article 

    Google Scholar 
    5.Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G. & Dickman, C. R. Invasive predators and global biodiversity loss. Proc. Natl Acad. Sci. USA 113, 11261–11265 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Gallardo, B., Clavero, M., Sánchez, M. I. & Vilà, M. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22, 151–163 (2016).ADS 
    Article 

    Google Scholar 
    7.Didham, R. K., Tylianakis, J. M., Hutchison, M. A., Ewers, R. M. & Gemmell, N. J. Are invasive species the drivers of ecological change? Trends Ecol. Evol. 20, 470–474 (2005).PubMed 
    Article 

    Google Scholar 
    8.Simberloff, D. How common are invasion-induced ecosystem impacts? Biol. Invasions 13, 1255–1268 (2011).Article 

    Google Scholar 
    9.Guy-Haim, T. et al. Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions: a global review and meta-analysis. Glob. Change Biol. https://doi.org/10.1111/gcb.14007 (2018).10.Vander Zanden, M. J., Casselman, J. M. & Rasmussen, J. B. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401, 464–467 (1999).ADS 
    Article 
    CAS 

    Google Scholar 
    11.Bartomeus, I., Vilà, M. & Santamaría, L. Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155, 761–770 (2008).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Aizen, M. A., Morales, C. L. & Morales, J. M. Invasive mutualists erode native pollination webs. PLoS Biol. 6, 0396–0403 (2008).CAS 
    Article 

    Google Scholar 
    13.Olesen, J. M., Eskildsen, L. I. & Venkatasamy, S. Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers. Distrib. 8, 181–192 (2002).Article 

    Google Scholar 
    14.Carvalheiro, L. G., Barbosa, E. R. M. & Memmott, J. Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study. J. Appl. Ecol. 45, 1419–1427 (2008).Article 

    Google Scholar 
    15.Anderson, C. B., Griffith, C. R., Rosemond, A. D., Rozzi, R. & Dollenz, O. The effects of invasive North American beavers on riparian plant communities in Cape Horn, Chile. Biol. Conserv. 128, 467–474 (2006).Article 

    Google Scholar 
    16.Walsh, J. R., Carpenter, S. R. & Vander Zanden, M. J. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc. Natl Acad. Sci. USA 113, 201600366 (2016).
    Google Scholar 
    17.Wiles, G. J., Bart, J., Beck, R. E. & Aguon, C. F. Impacts of the Brown Tree Snake: patterns of decline and species persistence in Guam’s Avifauna. Conserv. Biol. 17, 1350–1360 (2003).Article 

    Google Scholar 
    18.Ludyanskiy, M., McDonald, D. & MacNeill, D. Impact of the Zebra Mussei, a Bivalve Invader. BioScience 43, 533–544 (1993).Article 

    Google Scholar 
    19.Byrnes, J. E., Reynolds, P. L. & Stachowicz, J. J. Invasions and extinctions reshape coastal marine food webs. PLoS ONE 2, 1–7 (2007).Article 

    Google Scholar 
    20.Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125 (2003).Article 

    Google Scholar 
    21.Stachowicz, J. J. Mutualism, facilitation, and the structure of ecological communities. BioScience 51, 235 (2001).Article 

    Google Scholar 
    22.Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B Biol. Sci. 273, 2305–2312 (2006).Article 

    Google Scholar 
    23.Bulleri, F., Bruno, J. F., Silliman, B. R. & Stachowicz, J. J. Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct. Ecol. 30, 70–78 (2016).Article 

    Google Scholar 
    24.Angelini, C. et al. Foundation species’ overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes. Proc. R. Soc. B Biol. Sci. 282, 20150421 (2015).Article 

    Google Scholar 
    25.Anthelme, F., Cavieres, L. A. & Dangles, O. Facilitation among plants in alpine environments in the face of climate change. Front. Plant Sci. 5 (2014).26.Angelini, C. & Silliman, B. R. Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree-epiphyte system. Ecology 95, 185–196 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.van der Heide, T. et al. A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336, 1432–1434 (2012).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    28.Nummi, P. & Holopainen, S. Whole-community facilitation by beaver: ecosystem engineer increases waterbird diversity: ecosystem engineer increases waterbird diversity. Aquat. Conserv. Mar. Freshw. Ecosyst. 24, 623–633 (2014).Article 

    Google Scholar 
    29.Rosell, F., Bozser, O., Collen, P. & Parker, H. Ecological impact of beavers Castor fiber and Castor canadensis and their ability to modify ecosystems. Mammal. Rev. 35, 248–276 (2005).Article 

    Google Scholar 
    30.He, Q., Bertness, M. D. & Altieri, A. H. Global shifts towards positive species interactions with increasing environmental stress. Ecol. Lett. 16, 695–706 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Schuerch, M. et al. Future response of global coastal wetlands to sea-level rise. Nature 561, 231–234 (2018).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Jackson, J. B. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Lotze, H. K. et al. Depletion, degredation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809 (2006).ADS 
    CAS 
    Article 

    Google Scholar 
    35.Grosholz, E. Ecological and evolutionary consequences of coastal invasions. Trends Ecol. Evol. 17, 22–27 (2002).Article 

    Google Scholar 
    36.Syvitski, J. P. M. et al. Sinking deltas due to human activities. Nat. Geosci. 2, 681–686 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    37.He, Q. & Silliman, B. R. Climate change, human impacts, and coastal ecosystems in the anthropocene. Curr. Biol. 29, R1021–R1035 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Barbier, E. B. et al. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193 (2011).Article 

    Google Scholar 
    39.Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    40.Angelini, C. et al. A keystone mutualism underpins resilience of a coastal ecosystem to drought. Nat. Commun. 7, 12473 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Bruno, J. F. & Bertness, M. D. Habitat modification and facilitation in benthic marine communities. in Marine Community Ecology (eds Bertness, M. D., Gaines, S. & Hay, M.) 201–216 (Sinauer, 2001).42.De Fouw, J. et al. Drought, mutualism breakdown, and landscape-scale degradation of seagrass beds. Curr. Biol. 26, 1051–1056 (2016).PubMed 
    Article 
    CAS 

    Google Scholar 
    43.Ellison, A. M., Farnsworth, E. J. & Twilley, R. R. Facultative mutualism between red mangroves and root‐fouling sponges in belizean mangal. Ecology https://doi.org/10.2307/2265744 (1996).44.Arkema, K. K. et al. Coastal habitats shield people and property from sea-level rise and storms. Nat. Clim. Change 3, 913–918 (2013).ADS 
    Article 

    Google Scholar 
    45.McKee, K. L., Mendelssohn, I. A. & Materne, M. D. Acute salt marsh dieback in the Mississippi River deltaic plain: a drought-induced phenomenon? Glob. Ecol. Biogeogr. 13, 65–73 (2004).Article 

    Google Scholar 
    46.Alber, M., Swenson, E. M., Adamowicz, S. C. & Mendelssohn, I. A. Salt Marsh Dieback: an overview of recent events in the US. Estuar. Coast. Shelf Sci. 80, 1–11 (2008).ADS 
    Article 

    Google Scholar 
    47.Wang, H., Fu, R., Kumar, A. & Li, W. Intensification of summer rainfall variability in the southeastern United States during recent decades. J. Hydrometeorol. 11, 1007–1018 (2010).ADS 
    Article 

    Google Scholar 
    48.Stiven, A. E. & Gardner, S. A. Population processes in the ribbed mussel Geukensia demissa (Dillwyn) in a North Carolina salt marsh tidal gradient: spatial pattern, predation, growth and mortality. J. Exp. Mar. Biol. Ecol. 160, 81–102 (1992).Article 

    Google Scholar 
    49.Angelini, C. & Silliman, B. R. Patch size-dependent community recovery after massive disturbance. Ecology 93, 101–110 (2012).PubMed 
    Article 

    Google Scholar 
    50.Mendelssohn, I. & Morris, J. Ecophysiological controls on the productivity of Spartina alterniflora. in Concepts and Controversies in Tidal Marsh Ecology (eds Weinstein, M. & Kreeger, D.) 59–80 (Kluwer Academic Publishers, 1999).51.Bertness, M. D. Ribbed mussels and Spartina alterniflora production in a New England marsh. Ecology 65, 1794–1807 (1984).Article 

    Google Scholar 
    52.Siemann, E., Carrillo, J. A., Gabler, C. A., Zipp, R. & Rogers, W. E. Experimental test of the impacts of feral hogs on forest dynamics and processes in the southeastern US. Ecol. Manag. 258, 546–553 (2009).Article 

    Google Scholar 
    53.Campbell, T. A. & Long, D. B. Feral swine damage and damage management in forested ecosystems. Ecol. Manag. 257, 2319–2326 (2009).Article 

    Google Scholar 
    54.Barrios-Garcia, M. N. & Ballari, S. A. Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol. Invasions 14, 2283–2300 (2012).Article 

    Google Scholar 
    55.Graves, H. B. Behavior and ecology of wild and feral swine (Sus-Scrofa). J. Anim. Sci. 58, 482–492 (1984).Article 

    Google Scholar 
    56.Wood, G. W. & Roark, N. D. Food habits of feral hogs in coastal South Carolina. J. Wildl. Manag. 44, 506–511 (1980).Article 

    Google Scholar 
    57.Sharp, S. J. & Angelini, C. The role of landscape composition and disturbance type in mediating salt marsh resilience to feral hog invasion. Biol. Invasions https://doi.org/10.1007/s10530-019-02018-5 (2019).58.Crotty, S. M. et al. Foundation species patch configuration mediates salt marsh biodiversity, stability and multifunctionality. Ecol. Lett. 21, 1681–1692 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Zhu, Z. et al. Historic storms and the hidden value of coastal wetlands for nature-based flood defence. Nat. Sustain. https://doi.org/10.1038/s41893-020-0556-z (2020).60.Thomsen, M. S. et al. Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integr. Comp. Biol. 50, 158–175 (2010).PubMed 
    Article 

    Google Scholar 
    61.Silliman, B. R. et al. Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc. Natl Acad. Sci. USA 112, 14295–14300 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Silliman, B. R. et al. Field experiments and meta-analysis reveal wetland vegetation as a crucial element in the coastal protection paradigm. Curr. Biol. 29, 1800–1806 (2019). e3.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Neumann, B., Vafeidis, A. T., Zimmermann, J. & Nicholls, R. J. Future coastal population growth and exposure to sea-level rise and coastal flooding—a global assessment. PLoS ONE 10, e0118571 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Rogers, K. et al. Wetland carbon storage controlled by millennial-scale variation in relative sea-level rise. Nature 567, 91–95 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Rogers, H. S. et al. Effects of an invasive predator cascade to plants via mutualism disruption. Nat. Commun. 8, 14557 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Albins, M. & Hixon, M. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar. Ecol. Prog. Ser. 367, 233–238 (2008).ADS 
    Article 

    Google Scholar 
    67.Albins, M. Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar. Ecol. Prog. Ser. 522, 231–243 (2015).ADS 
    Article 

    Google Scholar 
    68.Ling, S. D. Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156, 883–894 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    69.Johnson, C. R. et al. Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J. Exp. Mar. Biol. Ecol. 400, 17–32 (2011).Article 

    Google Scholar 
    70.Ling, S. D., Johnson, C. R., Frusher, S. D. & Ridgway, K. R. Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc. Natl Acad. Sci. USA 106, 22341–22345 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Persico, E. P., Sharp, S. J. & Angelini, C. Feral hog disturbance alters carbon dynamics in southeastern US salt marshes. Mar. Ecol. Prog. Ser. 580, 57–68 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    72.Shaffer, G. P. et al. System response, nutria herbivory, and vegetation recovery of a wetland receiving secondarily-treated effluent in coastal Louisiana. Ecol. Eng. 79, 120–131 (2015).Article 

    Google Scholar 
    73.Fleming, P. A. et al. Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function?: loss of Australian digging mammals and ecosystem function. Mammal. Rev. 44, 94–108 (2014).Article 

    Google Scholar 
    74.Woinarski, J. C. Z., Burbidge, A. A. & Harrison, P. L. Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc. Natl Acad. Sci. USA 112, 4531–4540 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Croll, D. A. Introduced predators transform subarctic islands from grassland to tundra. Science 307, 1959–1961 (2005).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Siero, E. et al. Grazing away the resilience of patterned ecosystems. Am. Nat. 193, 472–480 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Crotty, S. M. & Angelini, C. Geomorphology and species interactions control facilitation cascades in a salt marsh ecosystem. Curr. Biol. 30, 1562–1571.e4 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.Geisser, H. & Reyer, H.-U. Efficacy of hunting, feeding, and fencing to reduce crop damage by wild boars. J. Wildl. Manag. 68, 939–946 (2004).Article 

    Google Scholar 
    79.Engeman, R. M. et al. Feral swine management for conservation of an imperiled wetland habitat: Florida’s vanishing seepage slopes. Biol. Conserv. 134, 440–446 (2007).Article 

    Google Scholar 
    80.Bevins, S. N., Pedersen, K., Lutman, M. W., Gidlewski, T. & Deliberto, T. J. Consequences associated with the recent range expansion of nonnative feral swine. BioScience 64, 291–299 (2014).Article 

    Google Scholar 
    81.McClure, M. L. et al. Modeling and mapping the probability of occurrence of invasive wild pigs across the contiguous United States. PLoS ONE 10, 1–17 (2015).
    Google Scholar 
    82.Oldfield, C. A. & Evans, J. P. Twelve years of repeated wild hog activity promotes population maintenance of an invasive clonal plant in a coastal dune ecosystem. Ecol. Evol. 6, 2569–2578 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Ford, M. A. & Grace, J. B. Effects of vertebrate herbivores on soil processes, plant biomass, litter accumulation and soil elevation changes in a coastal marsh. J. Ecol. 86, 974–982 (1998).Article 

    Google Scholar 
    84.Hensel, M. J. S. & Silliman, B. R. Consumer diversity across kingdoms supports multiple functions in a coastal ecosystem. Proc. Natl Acad. Sci. USA 110, 20621–20626 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Silliman, B. R. et al. Are the ghosts of nature’s past haunting ecology today? Curr. Biol. 28, R532–R537 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    86.Morse, N. B. et al. Novel ecosystems in the Anthropocene: a revision of the novel ecosystem concept for pragmatic applications. Ecol. Soc. 19, art12 (2014).Article 

    Google Scholar 
    87.Goigel Turner, M. Effects of grazing by feral horses, clipping, trampling, and burning on a Georgia salt marsh. Estuaries. 10, 54–60 (2014).Article 

    Google Scholar 
    88.Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.4.4. https://CRAN.R-project.org/package=DHARMa (2021).89.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2017).90.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    91.Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar 
    92.AgiSoft PhotoScan Professional. (AgiSoft, 2016).93.Rasband, W. S. ImageJ. (U.S. National Institutes of Health, 1997).94.Kuenzler, E. J. Structure and energy flow of a mussel population in a Georgia salt marsh. Limnol. Oceanogr. 6, 191–204 (1961).ADS 
    Article 

    Google Scholar 
    95.Length, R. V. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.0. https://CRAN.R-project.org/package=emmeans (2021).96.Guichard, F., Halpin, P. M., Allison, G. W., Lubchenco, J. & Menge, B. A. Mussel disturbance dynamics: signatures of oceanographic forcing from local interactions. Am. Nat. 161, 889–904 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.Silliman, B. R., van de Koppel, J., Bertness, M. D., Stanton, L. E. & Mendelssohn, I. A. Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310, 1803–1806 (2005).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Microevolutionary dynamics show tropical valleys are deeper for montane birds of the Atlantic Forest

    1.Mittelbach, G. G. et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10, 315–331 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Pyron, R. A., Alexander Pyron, R. & Wiens, J. J. Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc. R. Soc. B Biol. Sci. 280, 20131622 (2013).Article 

    Google Scholar 
    3.Pyron, R. A. Temperate extinction in squamate reptiles and the roots of latitudinal diversity gradients. Glob. Ecol. Biogeogr. 23, 1126–1134 (2014).Article 

    Google Scholar 
    4.Ghalambor, C. K., Huey, R. B., Martin, P. R., Tewksbury, J. J. & Wang, G. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integr. Comp. Biol. 46, 5–17 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Stevens, G. C. The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am. Nat. 133, 240–256 (1989).Article 

    Google Scholar 
    6.Sunday, J. M., Bates, A. E. & Dulvy, N. K. Global analysis of thermal tolerance and latitude in ectotherms. Proc. Biol. Sci. 278, 1823–1830 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    7.Janzen, D. H. Why mountain passes are higher in the tropics. Am. Nat. 101, 233–249 (1967).Article 

    Google Scholar 
    8.Cadena, C. D. et al. Latitude, elevational climatic zonation and speciation in New World vertebrates. Proc. R. Soc. B Biol. Sci. 279, 194–201 (2012).Article 

    Google Scholar 
    9.Eo, S. H., Wares, J. P. & Carroll, J. P. Population divergence in plant species reflects latitudinal biodiversity gradients. Biol. Lett. 4, 382–384 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Polato, N. R. et al. Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains. Proc. Natl Acad. Sci. USA 115, 12471–12476 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.McCain, C. M. Vertebrate range sizes indicate that mountains may be ‘higher’ in the tropics. Ecol. Lett. 12, 550–560 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Chan, W.-P. et al. Seasonal and daily climate variation have opposite effects on species elevational range size. Science 351, 1437–1439 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Shah, A. A. et al. Climate variability predicts thermal limits of aquatic insects across elevation and latitude. Funct. Ecol. 31, 2118–2127 (2018).14.Kozak, K. H. & Wiens, J. J. Climatic zonation drives latitudinal variation in speciation mechanisms. Proc. Biol. Sci. 274, 2995–3003 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    15.Smith, B. T., Seeholzer, G. F., Harvey, M. G., Cuervo, A. M. & Brumfield, R. T. A latitudinal phylogeographic diversity gradient in birds. PLoS Biol. 15, e2001073 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    16.Hewitt, G. The genetic legacy of the quaternary ice ages. Nature 405, 907–913 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    17.Smith, B. T., Bryson, R. W. Jr, Houston, D. D. & Klicka, J. An asymmetry in niche conservatism contributes to the latitudinal species diversity gradient in New World vertebrates. Ecol. Lett. 15, 1318–1325 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Bull, R. A. S. et al. Why replication is important in landscape genetics: American black bear in the Rocky Mountains. Mol. Ecol. 20, 1092–1107 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Peterman, W. E. ResistanceGA: an R package for the optimization of resistance surfaces using genetic algorithms. Methods Ecol. Evol. 9, 1638–1647 (2018).Article 

    Google Scholar 
    20.Burney, C. W. & Brumfield, R. T. Ecology predicts levels of genetic differentiation in neotropical birds. Am. Nat. 174, 358–368 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Kipp, F. A. Der Handflügel-Index als flugbiologisches Maß. Vogelwarte 20, 77–86 (1959).
    Google Scholar 
    22.Stotz, D. F., Fitzpatrick, J. W., Parker, T. A., III & Moskovits, D. K. Neotropical Birds: Ecology and Conservation (Univ. Chicago Press, 1996).23.Weir, J. T. & Schluter, D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315, 1574–1576 (2007).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    25.Bradburd, G. S., Coop, G. M. & Ralph, P. L. Inferring continuous and discrete population genetic structure across space. Genetics 210, 33–52 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Batalha-Filho, H., Cabanne, G. S. & Miyaki, C. Y. Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Mol. Phylogenet. Evol. 65, 892–902 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Raposo do Amaral, F. et al. Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds. Evolution 75, 2371–2387 (2021).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Dunbar, M. B. & Brigham, R. M. Thermoregulatory variation among populations of bats along a latitudinal gradient. J. Comp. Physiol. B 180, 885–893 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Gaitán-Espitia, J. D. et al. Geographic variation in thermal physiological performance of the intertidal crab Petrolisthes violaceus along a latitudinal gradient. J. Exp. Biol. 217, 4379–4386 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    30.Molina-Montenegro, M. A. & Naya, D. E. Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species. PLoS ONE 7, e47620 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Louthan, A. M., Doak, D. F. & Angert, A. L. Where and when do species interactions set range limits? Trends Ecol. Evol. 30, 780–792 (2015).PubMed 
    Article 

    Google Scholar 
    32.Macedo, G., Silva, M., do Amaral, F. R. & Maldonado-Coelho, M. Symmetrical discrimination despite weak song differentiation in 2 suboscine bird sister species. Behav. Ecol. 30, 1205–1215 (2019).Article 

    Google Scholar 
    33.Dhondt, A. A. Interspecific Competition in Birds (OUP, 2012).34.Freeman, B. G. Competitive interactions upon secondary contact drive elevational divergence in tropical birds. Am. Nat. 186, 470–479 (2015).PubMed 
    Article 

    Google Scholar 
    35.Zuloaga, J. & Kerr, J. T. Over the top: do thermal barriers along elevation gradients limit biotic similarity? Ecography 40, 478–486 (2017).Article 

    Google Scholar 
    36.Botero, C. A., Dor, R., McCain, C. M. & Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Mol. Ecol. 23, 259–268 (2014).PubMed 
    Article 

    Google Scholar 
    37.Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392–395 (2018).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Harvey, M. G. et al. The evolution of a tropical biodiversity hotspot. Science 370, 1343–1348 (2020).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Thom, G. et al. Climatic dynamics and topography control genetic variation in Atlantic Forest montane birds. Mol. Phylogenet. Evol. 148, 106812 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Rabosky, D. L. & Glor, R. E. Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc. Natl Acad. Sci. USA 107, 22178–22183 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Weir, J. T. & Price, T. D. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177, 462–469 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Harvey, M. G. et al. Positive association between population genetic differentiation and speciation rates in New World birds. Proc. Natl Acad. Sci. USA 114, 6328–6333 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Eaton, D. A. R. & Overcast, I. ipyrad: interactive assembly and analysis of RADseq datasets. Bioinformatics 36, 2592–2594 (2016).44.Harvey, M. G., Smith, B. T., Glenn, T. C., Faircloth, B. C. & Brumfield, R. T. Sequence capture versus restriction site associated DNA sequencing for shallow systematics. Syst. Biol. 65, 910–924 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Cumer, T. et al. Double-digest RAD-sequencing: do pre- and post-sequencing protocol parameters impact biological results? Mol. Genet. Genomics 296, 457–471 (2021).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Nei, M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590 (1978).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Jombart, T. & Ahmed, I. adegenet 1.3–1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Gehara, M. et al. Estimating synchronous demographic changes across populations using hABC and its application for a herpetological community from northeastern Brazil. Mol. Ecol. 26, 4756–4771 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Phillips, S. J. & Dudík, M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31, 161–175 (2008).Article 

    Google Scholar 
    51.Blonder, B., Lamanna, C., Violle, C. & Enquist, B. J. The n-dimensional hypervolume. Glob. Ecol. Biogeogr. 23, 595–609 (2014).Article 

    Google Scholar 
    52.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Soft. 67, 1–48 (2015).53.Clarke, R. T., Rothery, P. & Raybould, A. F. Confidence limits for regression relationships between distance matrices: estimating gene flow with distance. J. Agric. Biol. Environ. Stat. 7, 361 (2002).Article 

    Google Scholar 
    54.Pavlidis, P., Laurent, S. & Stephan, W. msABC: a modification of Hudson’s ms to facilitate multi-locus ABC analysis. Mol. Ecol. Resour. 10, 723–727 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Csilléry, K., François, O. & Blum, M. G. B. abc: an R package for approximate Bayesian computation (ABC). Methods Ecol. Evol. 3, 475–479 (2012).Article 

    Google Scholar 
    56.Orme, D. et al. The caper package: comparative analysis of phylogenetics and evolution in R. R. Package Version 5, 1–36 (2013).
    Google Scholar 
    57.Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    58.Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Blomberg, S. P., Garland, T. Jr & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Pavoine, S. adiv: An r package to analyse biodiversity in ecology. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13430 (2020).Article 

    Google Scholar  More