More stories

  • in

    Solar geoengineering can alleviate climate change pressures on crop yields

    1.Lawrence, M. G. et al. Evaluating climate geoengineering proposals in the context of the Paris Agreement temperature goals. Nat. Commun. 9, 3734 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    2.MacMartin, D. G., Ricke, K. L. & Keith, D. W. Solar geoengineering as part of an overall strategy for meeting the 1.5 °C Paris target. Phil. Trans. R. Soc. A 376, 20160454 (2018).ADS 

    Google Scholar 
    3.Crutzen, P. J. Albedo enhancement by stratospheric sulfur injections: a contribution to resolve a policy dilemma? Climatic Change 77, 211–220 (2006).ADS 
    CAS 

    Google Scholar 
    4.Ahlm, L. et al. Marine cloud brightening—as effective without clouds. Atmos. Chem. Phys. 17, 13071–13087 (2017).ADS 
    CAS 

    Google Scholar 
    5.Muri, H. et al. Climate response to aerosol geoengineering: a multimethod comparison. J. Clim. 31, 6319–6340 (2018).ADS 

    Google Scholar 
    6.Kravitz, B. et al. The Geoengineering Model Intercomparison Project (GeoMIP). Atmos. Sci. Lett. 12, 162–167 (2011).ADS 

    Google Scholar 
    7.Robock, A., Oman, L. & Stenchikov, G. L. Regional climate responses to geoengineering with tropical and Arctic SO2 injections. J. Geophys. Res. Atmos. 113, D16101 (2008).ADS 

    Google Scholar 
    8.Tjiputra, J. F., Grini, A. & Lee, H. Impact of idealized future stratospheric aerosol injection on the large-scale ocean and land carbon cycles. J. Geophys. Res. Biogeosci. 121, 2015JG003045 (2016).
    Google Scholar 
    9.Russell, L. M. et al. Ecosystem impacts of geoengineering: a review for developing a science plan. Ambio 41, 350–369 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Xia, L. et al. Solar radiation management impacts on agriculture in China: a case study in the Geoengineering Model Intercomparison Project (GeoMIP). J. Geophys. Res. Atmos. 119, 8695–8711 (2014).ADS 

    Google Scholar 
    11.Zhan, P., Zhu, W., Zhang, T., Cui, X. & Li, N. Impacts of sulfate geoengineering on rice yield in china: results from a multimodel ensemble. Earth Future 7, 395–410 (2019).ADS 

    Google Scholar 
    12.Parkes, B., Challinor, A. & Nicklin, K. Crop failure rates in a geoengineered climate: impact of climate change and marine cloud brightening. Environ. Res. Lett. 10, 084003 (2015).13.Yang, H. et al. Potential negative consequences of geoengineering on crop production: a study of Indian groundnut. Geophys. Res. Lett. 43, 11786–11795 (2016).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    14.Pongratz, J., Lobell, D. B., Cao, L. & Caldeira, K. Crop yields in a geoengineered climate. Nat. Clim. Change 2, 101–105 (2012).ADS 
    CAS 

    Google Scholar 
    15.Proctor, J., Hsiang, S., Burney, J., Burke, M. & Schlenker, W. Estimating global agricultural effects of geoengineering using volcanic eruptions. Nature 560, 480–483 (2018).ADS 
    CAS 

    Google Scholar 
    16.Tjiputra, J. F. et al. Evaluation of the carbon cycle components in the Norwegian Earth System Model (NorESM). Geosci. Model Dev. 6, 301–325 (2013).ADS 

    Google Scholar 
    17.MacMartin, D. G. & Kravitz, B. Mission-driven research for stratospheric aerosol geoengineering. Proc. Natl Acad. Sci. USA 116, 1089–1094 (2019).ADS 
    CAS 

    Google Scholar 
    18.Lombardozzi, D. L. et al. Simulating agriculture in the community land model version 5. J. Geophys. Res. Biogeosci. 125, e2019JG005529 (2020).ADS 

    Google Scholar 
    19.Popp, A. et al. Land-use futures in the shared socio-economic pathways. Glob. Environ. Change 42, 331–345 (2017).
    Google Scholar 
    20.O’Neill, B. C. et al. The scenario model intercomparison project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 (2016).ADS 

    Google Scholar 
    21.IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).22.FAOSTAT (FAO, 2019); http://www.fao.org/faostat/en/?#data/QC23.Tai, A. P. K., Martin, M. V. & Heald, C. L. Threat to future global food security from climate change and ozone air pollution. Nat. Clim. Change 4, 817–821 (2014).ADS 
    CAS 

    Google Scholar 
    24.Hsiao, J., Swann, A. L. S. & Kim, S.-H. Maize yield under a changing climate: the hidden role of vapor pressure deficit. Agric. For. Meteorol. 279, 107692 (2019).ADS 

    Google Scholar 
    25.Grossiord, C. et al. Plant responses to rising vapor pressure deficit. New Phytol. https://doi.org/10.1111/nph.16485 (2020).26.Rigden, A. J., Mueller, N. D., Holbrook, N. M., Pillai, N. & Huybers, P. Combined influence of soil moisture and atmospheric evaporative demand is important for accurately predicting US maize yields. Nat. Food 1, 127–133 (2020).
    Google Scholar 
    27.Konings, A. G., Williams, A. P. & Gentine, P. Sensitivity of grassland productivity to aridity controlled by stomatal and xylem regulation. Nat. Geosci. 10, 284–288 (2017).ADS 
    CAS 

    Google Scholar 
    28.Novick, K. A. et al. The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nat. Clim. Change 6, 1023–1027 (2016).ADS 
    CAS 

    Google Scholar 
    29.Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2: Tansley review. New Phytol. 165, 351–372 (2004).
    Google Scholar 
    30.Bishop, K. A., Leakey, A. D. B. & Ainsworth, E. A. How seasonal temperature or water inputs affect the relative response of C3 crops to elevated CO2: a global analysis of open top chamber and free air CO2 enrichment studies. Food Energy Secur. 3, 33–45 (2014).
    Google Scholar 
    31.Ainsworth, E. A. et al. A meta-analysis of elevated CO2 effects on soybean (Glycine max) physiology, growth and yield. Glob. Change Biol. 8, 695–709 (2002).ADS 

    Google Scholar 
    32.Leakey, A. D. B. Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel. Proc. R. Soc. B 276, 2333–2343 (2009).CAS 

    Google Scholar 
    33.Ainsworth, E. A. & Rogers, A. The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270 (2007).CAS 

    Google Scholar 
    34.National Research Council Climate Intervention: Reflecting Sunlight to Cool Earth (National Academies, 2015); https://doi.org/10.17226/1898835.Lutsko, N. J., Seeley, J. T. & Keith, D. W. Estimating impacts and trade-offs in solar geoengineering scenarios with a moist energy balance model. Geophys. Res. Lett. 47, e2020GL087290 (2020).ADS 

    Google Scholar 
    36.Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).ADS 

    Google Scholar 
    37.Tilmes, S. et al. The hydrological impact of geoengineering in the geoengineering model intercomparison project (GeoMIP). J. Geophys. Res. Atmos. 118, 11,036–11,058 (2013).
    Google Scholar 
    38.Lawrence, D. M. et al. The community land model version 5: description of new features, benchmarking, and impact of forcing uncertainty. J. Adv. Model. Earth Syst. 11, 4245–4287 (2019).ADS 

    Google Scholar 
    39.Fisher, R. A. et al. Parametric controls on vegetation responses to biogeochemical forcing in the CLM5. J. Adv. Model. Earth Syst. 11, 2879–2895 (2019).ADS 

    Google Scholar 
    40.Bonan, G. B. et al. Model structure and climate data uncertainty in historical simulations of the terrestrial carbon cycle (1850–2014). Glob. Biogeochem. Cycles 33, 1310–1326 (2019).ADS 
    CAS 

    Google Scholar 
    41.Osborne, T., Rose, G. & Wheeler, T. Variation in the global-scale impacts of climate change on crop productivity due to climate model uncertainty and adaptation. Agric. For. Meteorol. 170, 183–194 (2013).ADS 

    Google Scholar 
    42.Peng, B. et al. Improving maize growth processes in the community land model: implementation and evaluation. Agric. For. Meteorol. 250–251, 64–89 (2018).ADS 

    Google Scholar 
    43.Buzan, J. R. & Huber, M. Moist heat stress on a hotter earth. Annu. Rev. Earth Planet. Sci. 48, 623–655 (2020).ADS 
    CAS 

    Google Scholar 
    44.Wieder, W. R. et al. Beyond static benchmarking: using experimental manipulations to evaluate land model assumptions. Glob. Biogeochem. Cycles 33, 1289–1309 (2019).ADS 
    CAS 

    Google Scholar 
    45.Mercado, L. M. et al. Impact of changes in diffuse radiation on the global land carbon sink. Nature 458, 1014–1017 (2009).ADS 
    CAS 

    Google Scholar 
    46.Cheng, S. J. et al. Variations in the influence of diffuse light on gross primary productivity in temperate ecosystems. Agric. For. Meteorol. 201, 98–110 (2015).ADS 

    Google Scholar 
    47.Shao, L. et al. The fertilization effect of global dimming on crop yields is not attributed to an improved light interception. Glob. Change Biol. 26, 1697–1713 (2020).ADS 

    Google Scholar 
    48.Vattioni, S. et al. Exploring accumulation-mode H2SO4 versus SO2 stratospheric sulfate geoengineering in a sectional aerosol–chemistry–climate model. Atmos. Chem. Phys. 19, 4877–4897 (2019).ADS 
    CAS 

    Google Scholar 
    49.Levis, S., Badger, A., Drewniak, B., Nevison, C. & Ren, X. CLMcrop yields and water requirements: avoided impacts by choosing RCP 4.5 over 8.5. Climatic Change 146, 501–515 (2018).ADS 

    Google Scholar 
    50.Fricko, O. et al. The marker quantification of the Shared Socioeconomic Pathway 2: a middle-of-the-road scenario for the 21st century. Glob. Environ. Change 42, 251–267 (2017).
    Google Scholar 
    51.Lauvset, S. K., Tjiputra, J. & Muri, H. Climate engineering and the ocean: effects on biogeochemistry and primary production. Biogeosciences 14, 5675–5691 (2017).ADS 

    Google Scholar 
    52.Hurtt, G. C. et al. Harmonization of land-use scenarios for the period 1500–2100: 600 years of global gridded annual land-use transitions, wood harvest, and resulting secondary lands. Climatic Change 109, 117–161 (2011).ADS 

    Google Scholar 
    53.West, T. O. et al. Cropland carbon fluxes in the United States: increasing geospatial resolution of inventory-based carbon accounting. Ecol. Appl. 20, 1074–1086 (2010).
    Google Scholar 
    54.Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616–620 (2011).ADS 
    CAS 

    Google Scholar 
    55.Farquhar, G., von Caemmerer, Svon & Berry, J. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90 (1980).CAS 

    Google Scholar 
    56.Collatz, G. J., Ribas-Carbo, M. & Berry, J. A. Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Funct. Plant Biol. 19, 519–538 (1992).
    Google Scholar 
    57.Medlyn, B. E. et al. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob. Change Biol. 17, 2134–2144 (2011).ADS 

    Google Scholar 
    58.Long, S. P., Ainsworth, E. A., Leakey, A. D. B., Nösberger, J. & Ort, D. R. Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312, 1918–1921 (2006).ADS 
    CAS 

    Google Scholar 
    59.The NCAR Command Language (NCL, Version 6.5.0) (UCAR, NCAR, CISL, TDD, 2018); https://doi.org/10.5065/D6WD3XH5 More

  • in

    A pan-African spatial assessment of human conflicts with lions and elephants

    After preprocessing the data, methods consisted of spatial analyses to map areas at risk of conflict; statistical analyses to identify the most important factors affecting lion and elephant population numbers; economic analyses to estimate the EAA of building and maintaining mitigation fences in areas under severe and high risk of conflict, and fragmentation analyses to assess the impact of fences on migratory mammal species. We describe each step in detail below (see Supplementary Fig. 2 for a flowchart of the analysis). All spatial data were converted to vectors for analysis to reduce commission errors (when a species is mistakenly thought to be present) when converting the species-range maps from vector to raster. Data preprocessing was carried out using the open source database PostgreSQL 11.4 (https://www.postgresql.org/about/) with the GIS extensions of PostGIS 2.5 (https://postgis.net/); conflict mapping and range fragmentation analyses used PostgreSQL 11.4 and PostGIS 2.5, and Python v. 3.7.060; statistical and economic analyses used R v. 3.6.061; sensitivity analyses used PostgreSQL 11.4 and PostGIS 2.5, and Python v. 3.7.060 and R v. 3.6.061.PreprocessingHuman pressuresHuman pressure layers were independently generated from this study. We used Gridded Population of the World Version 4 (GPWv4) as a layer for human population density62. GPWv4 is a minimally modelled data set consisting of estimates of human population (number of persons per raster grid cell) based on non-spatial population data (i.e., tabular counts of population listed by administrative area) and spatially explicit administrative boundary data. Population input data are collected at the most detailed spatial resolution available from the results of the 2010 round of Population and Housing Censuses. The input data are then extrapolated to 2020 using calculated growth rates to produce future population estimates. A proportional allocation gridding algorithm, utilizing ~13.5 million national and subnational administrative units, assigned population counts to 30 arcsecond (~1 km at the equator) grid cells. The population density rasters were created by dividing the population count raster for a given target year by the land-area raster.We used the most recent version of the Gridded Livestock of the World database63, reflecting the compiled and harmonized subnational livestock distribution data for 2010, to extract information on cattle density. The data set provides global population densities of cattle, buffaloes, horses, sheep, goats, pigs, chickens, and ducks in each land pixel at a spatial resolution of 0.083333 decimal degrees (~10 km at the equator). Detailed livestock census statistics are mined from agricultural yearbooks or through direct contacts with ministries or statistical bureaus. The census statistics are usually found in the form of numbers per administrative unit that must be linked to corresponding geographic information system boundaries. Densities are estimated in each census polygon by dividing the number of animals from the census by the surface area of the administrative unit polygon (estimated in an Albert equal-area projection), corrected by a mask excluding unsuitable areas. Livestock densities were then extracted from the subnational census data and were used as the dependent variable in Random Forest models to estimate a density value in each pixel, based on raster predictor variables.We used spatially detailed crop maps available from the Copernicus Global Land Cover map at ~0.001° (~100 m) resolution64. The land-cover map is a discrete map with ten continuous cover fractions (nine base land-cover classes and seasonal water) to provide spatial information about land for a diversity of applications, including biodiversity conservation. Cropland (as percentage of 100 m pixel that is covered by cropland) refers to cultivated and managed agriculture, but does not include perennial woody crops that are classified under the appropriate forest or shrub land-cover type64. Cropland also refers to both irrigated and rainfed agriculture. The land-cover map was generated by compiling the 5-daily PROBA-V multi-spectral image data with a Ground Sampling Distance of ~0.001° as the primary earth observation data and PROBA-V UTM daily multi-spectral image data with a Ground Sampling Distance of ~0.003° (~300 m) as the secondary earth observation data. Next, the 5-daily PROBA-V 100 m and daily 300 m datasets were fused using a Kalman filtering approach. The global overall accuracy of the product for the base year 2015 was calculated through an independent pre-validation and reached 80%.Species-range mapsUpdated range maps showing current distribution for lions and elephants were provided by the International Union for Conservation of Nature (IUCN) Cat and African Elephant Specialist Groups65. In addition to the range maps, the specialist groups provided information on the number of African lions (2018) and elephants (2016) within sites where they are still extant. We also obtained species-range maps for all terrestrial mammal species in orders Cetartiodactyla, Perissodactyla, Primates, and Carnivora occurring in Africa from the IUCN Red List portal (www.iucnredlist.org/). Mammal species in these orders include migratory mammal species (e.g., the common wildebeest Connochaetes taurinus), which might be negatively affected by mitigation fences, e.g., by potentially blocking migratory routes.Protected areasThe data on protected areas were based on the May 2019 release of the World Database on Protected Areas66 (retrieved from http://www.protectedplanet.net). To prevent overestimation of the area coverage of protected areas caused by overlapping designations, we merged polygons into a single layer. We only included in the analysis IUCN categories Ia (Strict Nature Reserve), Ib (Wilderness Area), II (National Park), III (Natural Monument or Feature), and IV (Habitat/Species Management Area), because we wanted to prevent fences from excluding people from protected areas that had been modified by the interaction of nature and people over time (e.g., V, Protected Landscape/Seascape).Mapping potential risk of conflictA database on the spatial distribution of conflict locations between humans and lions and elephants is not available across Africa. We therefore mapped the most prominent factors known to affect conflict: human population density (for both lion and elephant), crop raiding (elephants), and cattle killing (lions)8. Furthermore, spatial modelling of range contractions in carnivores showed that contractions were significantly more likely in regions with high rural human population density, cattle density, and/or cropland4. Therefore, we only retained areas where human, cattle, and crop densities were in the first decile (in our case, the first decile is the decile with the highest human population, crop, and cattle densities) by PostgreSQL/PostGIS. Using only the highest decile likely resulted in a conservative map of spatial conflict.We further classified areas at the highest potential conflict into low, moderate, high, or severe risk of conflict. Specifically, areas at severe risk of conflict are those where the highest human population, crop, and cattle densities all overlap; areas at high risk of conflict are those with overlaps between the highest densities of human population and either crops or cattle; areas at moderate risk of conflict are the areas where the highest crop and cattle densities overlap; and areas at low risk of conflict are those with only one human pressure, i.e., the highest human population, or crop, or cattle density. The remainder was considered as being at no risk of conflict, as it did not meet any of the above criteria, but note the conservative nature of our analysis (see above).The lion and elephant range maps and the protected area layer were intersected to select all protected areas that contain parts of lion and elephant range and/or were adjacent to the species-range maps. The identified protected areas were then merged with the species-range maps to create a new extended range layer (see for an example in Supplementary Fig. 1). These extended range maps were used (i) to identify potential areas where lions and elephants could be restored, and (ii) to avoid interrupting ecological processes (e.g., migrations) and/or causing unintended consequences (e.g., fragment populations) to other biodiversity in neighbouring protected areas.We then identified areas at risk of conflict by intersecting the extended range map layer for lions and elephants with the classified conflict map. In all cases, the intersections were carried out so that the classified conflict areas were either adjacent to, or within a distance of 10 km from, the edge of the extended range map layer. We set this distance to consider the wide-ranging behaviour of both lions and elephants, to account for the fact that conflict decreases at greater distances from protected area boundaries37,38, and to account for the fact that future human pressures will likely increase before conservation actions take place2.We assessed how robust our results were to commission (where human pressure is mistakenly assumed to exist) and omission (where human pressure is mistakenly assumed to be absent) errors in the human pressure maps by carrying out a sensitivity analysis that randomly varied the distances between the extended range maps and the human pressure maps. We first used Latin hypercube sampling, which is a form of sampling used to reduce the number of runs necessary for a Monte Carlo simulation to achieve a reasonably accurate random distribution67, to randomly vary 100 times the distance values between the extended range and human pressure maps. Specifically, we divided the low, moderate, high, and severe conflict lines into 100 m segments, calculated the minimum distance for each segment to human pressure within a 10, 20, and 30 km buffer distance from the edge of the extended range map layer, and then randomly varied that distance 100 times across ±10% of the value. We then averaged the resulting 100 randomly created distance values for each segment and identified which segments fell outside of the analyzed buffer distances of 10, 20, and 30 km. We tested for 20 and 30 km buffer distances, as we wanted to assess the variability of the fencing distance to different buffer sizes. We also estimated the certainty of lion and elephant presence by identifying segments of the perimeter of the range maps of lion and elephant that overlapped with protected areas. We did this as we had information on certain presence of both species from within protected areas, as opposed to areas extending outside of protected areas.Statistical analysesWe used an information theoretic approach68 and Bayesian information criterion to calculate statistical models. We used generalized linear mixed models with a negative‐binomial error distribution to account for over-dispersed count data and a log‐link function to examine factors affecting lion (n = 77) and elephant (n = 191) population sizes in Africa. Generalized linear mixed models were fitted with both random and fixed effects, to capture the data structure. Country was included as a random intercept to represent the hierarchical structure of the data. All variables listed in Supplementary Table 8 were fitted as fixed effects, i.e., with constant regression coefficients across countries. The site-specific variables were calculated only for sites where lions and elephants are currently present and not for the extended ranges. For transboundary sites that stretch across countries, we used the value for Gross Domestic Product, Conservation expenditure, and the Ibrahim Index of African Governance, for the country making the largest area contribution to the site. We compared and ranked models using the Bayesian information criterion68. To avoid multicollinearity among variables, we only selected variables with the strongest effect on population numbers that correlated at r 0.7 was selected as an input into the modelling process. We assessed each model’s relative probability, using Bayesian information criterion weights and the structural goodness-of-fit from the percentage of deviance explained by the model. We determined the magnitude and direction of the coefficients for the independent variables with multi-model averaging implemented in the R package glmulti69. The relative importance of each predictor variable was measured as the sum of the weights over the six top‐ranked models with Bayesian information criterion values closer to that of the best model containing the parameter of interest. Finally, we used a 10-fold cross-validation (a bootstrap resampling procedure using 1000 iterations) to assess the predictive ability of the top-ranked model.Range fragmentation analysesWe assessed how the proposed mitigation fences affected species-range connectivity by calculating the perimeter length-to-area ratio for mammal species in orders Cetartiodactyla, Perissodactyla, Primates, and Carnivora, whose ranges were identified as intersecting with areas at severe risk of conflict. Minimizing the perimeter length-to-area ratio is an important method of optimizing protected area design, resulting in compact reserves with high connectivity that can enhance persistence of the species. The smaller the ratio, the greater the clumping and connectivity of the species ranges. Specifically, we calculated the ratios of perimeter length to area for the ranges of 20 migratory mammalian species (i) under current conditions without fences and (ii) under future conditions where the identified mitigation fences would pass through their ranges. In the latter case, we used a 20 m buffer around the identified fences to account for further habitat clearance due to maintaining clearances around the fences for management purposes.Economic analysesWe used EAA to estimate the return on investment of building and maintaining mitigation fences to reduce cattle loss and crop damage. EAA calculates the constant annual cash flow generated by a project over its lifespan if it were an annuity and the annuity can then be compared to other projects of similar or different lifespan. Therefore, the measure potentially provides an important means for funders/donors to compare different investment opportunities. EAA is calculated by dividing the NPV of a project by the present value of annuity factor39. We started by calculating NPV in countries with areas at severe and high risk of conflict as:$${{NPV}}={sum }_{i}^{n}frac{{R}_{i}}{{left(1+dright)}^{i}}-Z$$
    (1)
    where ({R}_{i}) is net cash flow, (d) is the discount rate specific to each country (Supplementary Table 9), n is the number of time periods, (i) is the cash flow period, and (Z) is the initial investment of building the fences. NPV was calculated over a 10-year investment period. ({R}_{i}) was calculated as:$${R}_{i}=B-C$$
    (2)
    where (B) is the economic benefit derived from mitigation fences and (C) is the cost of maintaining mitigation fences. The economic benefits of mitigation fences for countries with severe risk of conflict refer to the potential reduction in cattle loss (for lions) and crop damage (for elephants) derived from building fences:$$B=L+E$$
    (3)
    where (L) represents the economic benefits of reducing cattle loss and (E) measures the economic benefits of reducing crop damage. For countries with high risk of conflict, the benefit ((B)) is derived from one or the other, i.e., (B) = (L) or (B) = (E).$$L=v * w * P$$
    (4)
    where (v) is the number of cattle that are not lost because of the presence of fences, (w) is the average weight in kg of adult cattle in that country, and (P) is the price of meat per kg paid to producers in that country in 2017 (data can be downloaded from http://www.fao.org/faostat/en/#data/PP). (v) was calculated as the percentage of total cattle present in the 10 km buffer adjacent to severe and high conflict areas, which could potentially be killed, based on published estimates across Africa45. Estimates range from 0.8 to 2.6% of cattle losses, and we decided to use a conservative 1% loss in the analysis (see below for how we accounted for uncertainty in model parameters). (w) was based on the average weight of an adult cow with estimates available at a regional level (west Africa: 262 kg; central Africa: 281 kg; east Africa: 283 kg; and southern Africa: 339 kg)70.$$E=left(d * Aright) * y * P$$
    (5)
    where (d) is the percentage of crop area damaged by elephants; data are taken from published estimates (ranging from 0.2 to 4% and we used a conservative 1% in the analysis)44; (A) is the total area in km2 available as crops in the 10 km buffer adjacent to the areas at severe and high risk of conflict; (y) is the yield (ton/km2) for the crop known to be targeted by elephants (cassava, maize, millet, banana, sorghum, groundnuts)44, which covered the largest area size in that country in 2017 (data calculated from: http://www.fao.org/faostat/en/#data/PP); and (P) is the price per ton paid to producers for that crop in that country in 2017 (data can be downloaded from http://www.fao.org/faostat/en/#data/PP). Although there might be several crops available within the buffer, this information is currently not available at the continental scale. Therefore, we decided to use the most common cultivated crop known to be targeted by elephants in each country.The cost of maintaining mitigation fences ((C)) was calculated as:$$C=f * c$$
    (6)
    where f is the fence length in that country and (c) is the cost for maintaining the fence. We obtained cost estimates of building (Z) and maintaining ((c)) the fences from Pekor et al.33. We used the median estimated current cost of USD 9522 per km for building fences and the median stated annual budget cost of USD 487 per km for adequate fence inspection and maintenance. This is the most up-to-date information validated through peer review on the costs (converted to 2017 USD) across Africa33. Cost estimates varied across surveyed conservation areas because of fence height and materials but included relevant costs of electrification and predator-proof structures33. The data were collected from 29 partially fenced ( More

  • in

    Precision conservation for a changing climate

    The author wishes to thank N. Haan, G. P. Robertson and N. Haddad for their valuable comments. Financial support was provided by USDA/NIFA (awards 2019-67012-29595 and 2015-68007-23133), the US National Science Foundation’s Long-term Ecological Research Program (award 1637653), the US Department of Energy, Office of Science, Office of Biological and Environmental Research (awards DESC0018409 and DE-FC02-07ER64494), and Michigan State University AgBioResearch. More

  • in

    Controversial forestry experiment will be largest-ever in United States

    A clear-cut slope in the Elliott State Forest, Oregon.Credit: Matthew Betts

    Despite lingering tensions among environmentalists and loggers, a plan to launch the largest forestry experiment in the United States — and perhaps the world — last month cleared a major hurdle. Controversially, the study would allow logging in a new research forest, in an attempt to answer a grand question: in a world where wood remains a necessary resource, but biodiversity is declining, what’s the best way to balance timber production with conservation?“We all love wood, and we all need wood,” says Thomas DeLuca, dean of the College of Forestry at Oregon State University (OSU) in Corvallis. “We have to find ways to produce it sustainably, and this project could help us do that.”
    These scientists are setting a forest on fire — and studying it with drones
    If the project — proposed by DeLuca and other researchers at OSU — launches successfully, the newly created Elliott State Research Forest in southwestern Oregon would occupy a roughly 33,000-hectare parcel of land. This would be divided into more than 40 sections, in which scientists would test several forest-management strategies, some including extensive logging. The advisory committee for the project, which comprises environmentalists, hunters, loggers and members of local Indigenous tribes, approved the latest research proposal on 22 April.The plan comes as US President Joe Biden and other international leaders are strengthening commitments to conserve land and biodiversity before a meeting of the United Nations Convention on Biological Diversity later this year. In time, the Elliott research forest could help policymakers to determine how best to define and implement those pledges, says DeLuca.A contested forestFor decades, the land that makes up the Elliott State Forest has been mired in controversy. Logging is big business in the US Pacific Northwest, and this particular state-owned piece of land contains old-growth forest filled with valuable Douglas firs (Pseudotsuga menziesii) and other trees. Other sections have been actively logged and replanted since 1930. It also hosts threatened species such as the spotted owl (Strix occidentalis) and the marbled murrelet (Brachyramphus marmoratus), a seabird that nests in old-growth forests. In 2012, a lawsuit aimed at protecting the marbled murrelet brought commercial logging in the forest to a halt.

    Source: Deanne Carlson, OSU/Oregon Geospatial Enterprise Office; Design: Nature

    The state of Oregon considered various options for the land, before OSU researchers stepped forward with a plan in 2018. Their proposal to convert the property into a research forest would allow logging to resume at a lower level — but in the service of science and conservation, the scientists say. According to the plan, the profit from logging in the Elliott forest — around US$5 million to $7 million annually, says DeLuca — would help to pay for the experiment’s infrastructure and operations.There are dozens of research forests around the globe, including in the United States, and scientists have used them to study everything from ecology and soils to acid rain and the effects of rising atmospheric carbon dioxide levels. But the Elliott research forest would be larger than most of its predecessors, and advocates say that it would provide scientists with the first opportunity to test ecological forestry at such a large scale.A sea change for forestryAs currently designed, the project would leave more than 40% of the forest — a section of old growth that has been regenerating naturally since the area last burnt, a century and a half ago — untouched by logging. In the remaining area, researchers would run a series of replicated experiments, carrying out 4 types of land management across 40 small watersheds. On some plots, selective logging of individual trees would take place across the entire area. On others, clear-cutting would take place on half of the land, with the other half reserved for conservation. Other types of experimental plot would mix these two approaches (see ‘A grand experiment’). To understand the impacts of each management type, scientists would measure a variety of parameters, including levels of carbon in the forest; stream health; and insect, bird and fish diversity.So far, around 20 OSU researchers are involved in the project’s design, but the university hopes eventually to attract more scientists from across the world, who would run their own projects.

    Old-growth areas such as this one would be protected as reserves under a plan to convert the Elliott State Forest into an experimental forest.Credit: Matthew Betts

    The scale and approach of the experiment proposed by OSU would represent a sea change in forestry research, says Sue Baker, a forest ecologist at the University of Tasmania in Hobart, Australia, who is setting up a retrospective study looking at similar questions in Tasmanian forests. “I can’t think of anything similar anywhere in the world where people have been able to manipulate the forest landscape at this scale,” says Baker.More hurdles aheadSince its creation in 1930, the Elliott State Forest has been legally obliged to generate revenue for Oregon’s public schools through logging. Before OSU can take it over, the state must compensate the school fund to the tune of $221 million (the value of the forest); it has so far allocated less than half of that amount.And other hurdles remain. The university must finish a detailed management plan that will lay out rules governing the forest, and it must craft a separate plan for managing threatened and endangered species; this will need to be approved by the US Fish and Wildlife Service.
    How much can forests fight climate change?
    The OSU team has spent the past few years trying to build a broad — and unlikely — coalition for the effort, through public meetings and engagement with local Indigenous tribes, industry, environmentalists and other members of the project’s advisory panel, whose support will be crucial as state leaders weigh their final decision. But tensions haven’t disappeared entirely. Many environmentalists continue to question the logic of clear-cutting forests that absorb and store carbon in the middle of a climate crisis. Rather than perpetuating a long and damaging legacy of clear-cutting, the Elliott forest could be used to pioneer new forestry methods that restore biodiversity and boost carbon storage, says Josh Laughlin, executive director of Cascadia Wildlands, a conservation group based in Eugene, Oregon. “Let’s not make the same mistakes we’ve made over the past 100 years.”Given OSU’s long-standing ties to the timber industry, and controversies surrounding its management of existing research forests, it will also need to overcome scepticism about its role as a land steward, says Bob Van Dyk, a policy director at the Wild Salmon Center, an environmental group based in Portland, Oregon. In 2019, for instance, OSU’s College of Forestry authorized clear-cutting on 6.5 hectares of one of its forests, felling trees that were hundreds of years old.
    When will the Amazon hit a tipping point?
    DeLuca acknowledges that there have been mistakes in the past, but says the university has a solid academic record, and is committed to building a world-class research facility with the Elliott forest. “If we are able to demonstrate practices that accommodate the broadest array of species while still generating timber for meeting human resource needs, we can have a much larger impact,” says DeLuca.Everything will depend on the final management plan, but for now, Van Dyk and other members of the advisory board have unanimously given a provisional green light to the latest proposal. “It’s a good project, and we don’t get many chances to do something that is truly novel and interesting,” he says. More

  • in

    Our radical changes to Earth’s greenery began long ago — with farms, not factories

    A nineteenth-century illustration of a harvest in ancient Greece. Farming intensified around 2000 BC, when the rate of change in Earth’s plant life sped up. Credit: Docutres/Index/Heritage Images/Alamy

    Ecology
    20 May 2021
    Our radical changes to Earth’s greenery began long ago — with farms, not factories

    Humanity’s imprint on plant species and abundance began roughly 4,000 years ago, when agriculture took off.

    Share on Twitter
    Share on Twitter

    Share on Facebook
    Share on Facebook

    Share via E-Mail
    Share via E-Mail

    Human activity began to transform the number and variety of plant species on Earth thousands of years ago, long before the Industrial Revolution, and might have had an even greater impact on vegetation than did the last ice age.Ice entombed much of the planet from roughly 115,000 to some 20,000 years ago. Then, massive glaciers around the world started to retreat and global temperatures rose, resulting in dramatic alterations to Earth’s ecosystems.To investigate how the abundance and composition of global vegetation changed after that thaw, Ondřej Mottl and Suzette Flantua at the University of Bergen in Norway and their colleagues analysed 1,181 fossilized pollen samples from the past 18,000 years. The pollen came from all continents except Antarctica.The researchers found that global vegetation has been transformed, first by the climate changes that accompanied the end of the last glacial period. However, starting about 4,000 years ago, when agriculture intensified, the pace of change in global vegetation accelerated, reaching or exceeding the rate of change at the end of the most recent ice age.

    Science (2021)

    Ecology More

  • in

    Seasonal change is a major driver of soil resistomes at a watershed scale

    1.D’Costa, V. M. et al. Antibiotic resistance is ancient. Nature. 477, 457–461 (2011).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    2.Allen, H. K. et al. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251–259 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Udikovic-Kolic, N., Wichmann, F., Broderick, N. A. & Handelsman, J. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc. Natl Acad. Sci. USA. 111, 15202–15207 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Chen, Q. L. et al. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ. Int. 92–93, 1–10 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    5.Gillings, M. R. & Stokes, H. W. Are humans increasing bacterial evolvability? Trends Ecol. Evol. 27, 346–352 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Zhu, Y. G. et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl Acad. Sci. USA. 110, 3435–3440 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Woods, L. C. et al. Horizontal gene transfer potentiates adaptation by reducing selective constraints on the spread of genetic variation. Proc. Natl Acad. Sci. USA. 117, 26868–26875 (2020).8.World Health Organization. Antimicrobial resistance: global report on surveillance. World Health Organization. (2014).9.Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science. 337, 1107–1111 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Zhu, G. et al. Air pollution could drive global dissemination of antibiotic resistance genes. ISME J. 15, 270–281 (2021).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Xiang, Q. et al. Agricultural activities affect the pattern of the resistome within the phyllosphere microbiome in peri-urban environments. J. Hazard Mater. 382, 121068 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Wang, F. H. et al. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ. Sci. Technol. 48, 9079–9085 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Ding, J. et al. Long-term application of organic fertilization causes the accumulation of antibiotic resistome in earthworm gut microbiota. Environ. Int. 124, 145–152 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Zhou, S. Y. et al. Phyllosphere of staple crops under pig manure fertilization, a reservoir of antibiotic resistance genes. Environ. Pollut. 252, 227–235 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Wang, F. H., Qiao, M., Chen, Z., Su, J. Q. & Zhu, Y. G. Antibiotic resistance genes in manure-amended soil and vegetables at harvest. J. Hazard Mater. 299, 215–221 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Marti, R. et al. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl. Environ. Microb. 79, 5701–5709 (2013).CAS 
    Article 

    Google Scholar 
    17.Zhu, Y. G. et al. Continental-scale pollution of estuaries with antibiotic resistance genes. Nat. Microbiol. 2, 16270 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Du, S. et al. Large-scale patterns of soil antibiotic resistome in Chinese croplands. Sci. Total Environ. 712, 136418 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Pruden, A., Pei, R. T., Storteboom, H. & Carlson, K. H. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 40, 7445–7450 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    20.Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature. 560, 233–237 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Hu, H. W. et al. Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes. Environ. Microbiol. 20, 3186–3200 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Han, X. M. et al. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol. Biochem. 126, 91–102 (2018).CAS 
    Article 

    Google Scholar 
    23.Hu, H. W. et al. Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure. FEMS Microbiol. Ecol. 92, fiv169 (2016).24.Zhang, Y. J. et al. Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environ. Pollut. 231, 1621–1632 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Zhou, J. et al. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 5, 1303–1313 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 7, 335–336 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26, 2460–2461 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microb. 73, 5261–5267 (2007).CAS 
    Article 

    Google Scholar 
    29.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.Su, J. Q. et al. Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ. Sci. Technol. 49, 7356–7363 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Ouyang, W. Y., Huang, F. Y., Zhao, Y., Li, H. & Su, J. Q. Increased levels of antibiotic resistance in urban stream of Jiulongjiang River, China. Appl. Microbiol. Biotechnol. 99, 5697–5707 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Roberts D. W. labdsv: ordination and multivariate analysis for ecology. R package version 1.8-0. 2016. https://CRAN.R-project.org/package=labdsv.33.Oksanen J. et al. Vegan: community ecology package. R package version 2.2-0. 2014. http://CRAN.R-project.org/package=vegan.34.Jiao, S. et al. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome. 6, 1–13 (2018).35.Sloan, W. T. et al. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol. 8, 732–740 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Ning, D., Deng, Y., Tiedje, J. M. & Zhou, J. A general framework for quantitatively assessing ecological stochasticity. Proc. Natl Acad. Sci. USA. 116, 16892–16898 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.De Caceres, M. & Legendre, P. Associations between species and groups of sites: indices and statistical inference. Ecology. 90, 3566–3574 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Doerks, T., Copley, R. R., Schultz, J., Ponting, C. P. & Bork, P. Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12, 47–56 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Wickham H. ggplot2: elegant graphics for data analysis. (Springer-Verlag, 2009).40.Kassambara A. ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.2. 2018. https://CRAN.R-project.org/package=ggpubr.41.Ahlmann-Eltze C. ggsignif: significance brackets for ‘ggplot2’. R package version 0.4. 0. 2018. https://CRAN.R-project.org/package=ggsignif.42.Zhao, F. K. et al. Soil contamination with antibiotics in a typical peri-urban area in eastern China: seasonal variation, risk assessment, and microbial responses. J. Environ. Sci. (China). 79, 200–212 (2019).Article 

    Google Scholar 
    43.Zhang, Y., Snow, D. D., Parker, D., Zhou, Z. & Li, X. Intracellular and extracellular antimicrobial resistance genes in the sludge of livestock waste management structures. Environ. Sci. Technol. 47, 10206–10213 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Mao, D. et al. Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environ. Sci. Technol. 48, 71–78 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Xiang, Q. et al. Spatial and temporal distribution of antibiotic resistomes in a peri-urban area is associated significantly with anthropogenic activities. Environ. Pollut. 235, 525–533 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    46.Forsberg, K. J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature. 509, 612–616 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Li, B. et al. Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 9, 2490–2502 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Hu, H. W. et al. Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ. Microbiol. 18, 3896–3909 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    49.Birgander, J., Rousk, J. & Olsson, P. A. Comparison of fertility and seasonal effects on grassland microbial communities. Soil Biol. Biochem. 76, 80–89 (2014).CAS 
    Article 

    Google Scholar 
    50.Fournier, B. et al. Higher spatial than seasonal variation in floodplain soil eukaryotic microbial communities. Soil Biol. Biochem. 147, 107842 (2020).CAS 
    Article 

    Google Scholar 
    51.Zhang, K., Delgado-Baquerizo, M., Zhu, Y. G. & Chu, H. Space is more important than season when shaping soil microbial communities at a large spatial scale. Msystems. 5, e00783–19 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Ladau, J. & Eloe-Fadrosh, E. A. Spatial, temporal, and phylogenetic scales of microbial ecology. Trends Microbiol. 27, 662–669 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

  • in

    Germination response to water availability in populations of Festuca pallescens along a Patagonian rainfall gradient based on hydrotime model parameters

    1.Zárate, M. A. & Tripaldi, A. The aeolian system of central Argentina. Aeolian Res. 3, 401–417 (2012).ADS 
    Article 

    Google Scholar 
    2.Chapin III, F. S. Functional role of growth forms in ecosystem and global processes. In Scaling Physiology Process (ed. Ehleringer J. R. & Field C. B.) 287–312. (Elsevier Inc., 1993). https://doi.org/10.1016/C2009-0-03319-4.
    Google Scholar 
    3.Jump, A. S., Mátyás, C. & Peñuelas, J. The altitude-for-latitude disparity in the rangeretractions of woody species. Trends Ecol. Evol. (Amst.) 24, 694–701. https://doi.org/10.1016/j.tree.2009.06.007 (2009).Article 

    Google Scholar 
    4.Donohue, K., Rubio de Casas, R., Burghardt, L., Kovach, K. & Willis, C. G. Germination, postgermination adaptation, and species ecological ranges. Annu. Rev. Ecol. Evol. Syst. 41, 293–319 (2010).Article 

    Google Scholar 
    5.O’Connor, T. Local extinction in perennial grasslands: A life-history approach. Am. Nat. 137, 753–773 (1991).Article 

    Google Scholar 
    6.Rotundo, J. L., Aguiar, M. R. & Benech-Arnold, R. Understanding erratic seedling emergence in perennial grasses using physiological models and field experimentation. Plant Ecol. 216, 143–156 (2015).Article 

    Google Scholar 
    7.Duncan, C., Schultz, N. L., Good, M. K., Lewandrowski, W. & Cook, S. The risk-takers and-avoiders: Germination sensitivity to water stress in an arid zone with unpredictable rainfall. AoB Plants. 11(6), plz066 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Pendleton, B. & Meyer, S. Habitat-correlated variation in blackbrush (Coleogyne ramosissima: Rosaceae) seed germination response. J. Arid Environ. 59, 229–243 (2004).ADS 
    Article 

    Google Scholar 
    9.Chamorro, D. et al. Germination sensitivity to water stress in four shrubby species across the Mediterranean Basin. Plant Biol. 19(1), 23–31 (2017).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    10.Bewley, J. D. & Black, M. Seeds. In Seeds. (ed. Bewley, J. D. & Black, M.) 1–33. https://doi.org/10.1007/978-1-4899-1002-8. eBook ISBN978-1-4899-1002-8 (Springer, Boston, MA, 1994).
    Google Scholar 
    11.Bradford, K. J. Water relations in seed germination. In Seed Development and Germination (eds Kigel, J. & Galili, G.) 351–396 (Marcel Dekker Inc, 1995).
    Google Scholar 
    12.Batlla, D. & Benech-Arnold, R. L. The role of fluctuations in soil water content on the regulation of dormancy changes in buried seeds of Polygonum aviculare L. Seed Sci. Res. 16(1), 47–59 (2006).Article 
    CAS 

    Google Scholar 
    13.Luna, B. & Chamorro, D. Germination sensitivity to water stress of eight Cistaceae species from the Western Mediterranean. Seed Sci. Res. 26(2), 101 (2016).Article 

    Google Scholar 
    14.Bradford, K. J. Threshold models applied to seed germination ecology. New Phytol. 165, 338–341 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Garcia-Huidobro, J., Monteith, J. & Squire, G. Time, temperature and germination of pearl millet (Pennisetum typhoides S. & H.) I. Constant temperature. J. Exp. Bot. 33, 288–296 (1982).Article 

    Google Scholar 
    16.Bradford, K. J. A water relations analysis of seed germination rates. Plant Physiol. 94, 840–849 (1990).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    17.Bradford, K. J. & Still, D. W. Applications of hydrotime analysis in seed testing. Seed Technol. 26(1), 75–85 (2004).
    Google Scholar 
    18.Gummerson, R. J. The effect of constant temperature and osmotic potentials on the germination of sugar beet. J. Exp. Bot. 37, 729–741 (1986).Article 

    Google Scholar 
    19.Bradford, K. J. Applications of hydrothermal time to quantifying and modeling seed germination and dormancy. Weed Sci. 50, 248–260 (2002).Article 
    CAS 

    Google Scholar 
    20.Batlla, D. & Agostinelli, A. M. Thermal regulation of secondary dormancy induction in Polygonum aviculare seeds: A quantitative analysis using the hydrotime model. Seed Sci. Res. 27(3), 231–242 (2017).Article 
    CAS 

    Google Scholar 
    21.Farahinia, P., Sadat-Noori, S. A., Mortazavian, M. M., Soltani, E. & Foghi, B. Hydrotime model analysis of Trachyspermum ammi (L.) Sprague seed germination. J. Appl. Res. Med. Aroma. 5, 88–91 (2017).
    Google Scholar 
    22.Wang, R., Bai, Y. & Tanino, K. Germination of winterfat (Eurotia lanata (Pursh) Moq.) seeds at reduced water potentials: Testing assumptions of hydrothermal time model. Environ. Exp. Bot. 53(1), 49–683 (2005).Article 

    Google Scholar 
    23.Alvarado, V. & Bradford, K. J. A hydrothermal time model explains the cardinal temperatures for seed germination. Plant Cell Environ. 25(8), 1061–1069 (2002).Article 

    Google Scholar 
    24.Bakhshandeh, E. & Gholamhossieni, M. Modelling the effects of water stress and temperature on seed germination of radish and cantaloupe. J. Plant Growth Regul. 38(4), 1402–1411 (2019).Article 
    CAS 

    Google Scholar 
    25.Bakhshandeh, E. & Jamali, M. Population-based threshold models: A reliable tool for describing aged seeds response of rapeseed under salinity and water stress. Environ. Exp. Bot. 176, 104077 (2020).Article 
    CAS 

    Google Scholar 
    26.Leva, P. E. Variación regional de las características agroecológicas y genéticas de Bromus pictus y Poa ligularis en estepas patagónicas (Universidad Nacional de Buenos Aires, 2010).
    Google Scholar 
    27.Palazzesi, L., Barreda, V. & Prieto, A. Análisis evolutivo de la vegetación cenozoica en las provincias de Chubut y Santa Cruz (Argentina) con especial atención en las comunidades herbáceo-arbustivas. Revista del Museo Argentino de Ciencias Naturales nueva serie 5(2), 151–161 (2014).
    Google Scholar 
    28.León, R. J., Bran, D., Collantes, M., Paruelo, J. M. & Soriano, A. Grandes unidades de vegetación de la Patagonia extra andina. Ecol. Austral. 8, 125–144 (1998).
    Google Scholar 
    29.Villalba, R. et al. Large-scale temperature changes across the southern Andes: 20th-century variations in the context of the past 400 years. Clim. Change. 59(1), 177–232 (2003).Article 

    Google Scholar 
    30.Godagnone, R., Bran, D. Inventario integrado de los recursos de la Provincia de Río Negro. (INTA, Argentina, Río Negro, 2009).
    Google Scholar 
    31.Soriano, A. La vegetación del Chubut. Revista Argentina de Agronomía. 17, 30–66 (1950).
    Google Scholar 
    32.Bertiller, M. B. & Coronato, F. Seed bank patterns of Festuca pallescens in semiarid Patagonia (Argentina): A possible limit to bunch reestablishment. Biodivers. Conserv. 3(1), 57–67 (1994).Article 

    Google Scholar 
    33.Defossé, G., Bertiller, M. & Robberecht, R. Germination characteristics of Festuca pallescens, a Patagonian bunchgrass with reclamation potential. Seed Sci. Technol. (Switzerland). 23(3), 715–723 (1995).
    Google Scholar 
    34.Bertiller, M. B., Elissalde, N. O., Rostagno, C. M. & Defossé, G. E. Environmental patterns and plant distribution along a precipitation gradient in western Patagonia. J. Arid Environ. 29, 85–97 (1993).Article 

    Google Scholar 
    35.Bran, D., Ayesa, J., López, C. Regiones ecológicas de Río Negro. Comunicación Técnica No 59. (INTA, EEA Bariloche, 2000).
    Google Scholar 
    36.Oliva, G. et al. Monitoring drylands: The MARAS system. J. Arid Environ. 161, 55–63 (2019).ADS 
    Article 

    Google Scholar 
    37.López, A. S., Marchelli, P., Batlla, D., López, D. R. & Arana, M. V. Seed responses to temperature indicate different germination strategies among Festuca pallescens populations from semi-arid environments in North Patagonia. Agric. For. Meteorol. 272, 81–90 (2019).ADS 
    Article 

    Google Scholar 
    38.Gaitán, J. J. et al. Evaluating the performance of multiple remote sensing indices to predict the spatial variability of ecosystem structure and functioning in Patagonian steppes. Ecol. Indic. 34, 181–191 (2013).Article 

    Google Scholar 
    39.Moore, R. P. Tetrazolium tests for diagnosing causes for seed weaknesses and for predicting and understanding performance. In Proceedings of the Association of Official Seed Analysts. Association of Official Seed Analysts, vol. 56, 70–73. https://www.jstor.org/stable/23432057 (1966).40.Michel, B. E. Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiol. 72(1), 66–70 (1983).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    41.Di Rienzo, J. A., et al. InfoStat versión 2020 & Centro de Transferencia InfoStat. FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar.42.Volis, S., Mendlinger, S. & Ward, D. Adaptive traits of wild barley plants of Mediterranean and desert origin. Oecologia 133(2), 131–138 (2002).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Krichen, K., Mariem, H. B. & Chaieb, M. Ecophysiological requirements on seed germination of a Mediterranean perennial grass (Stipa tenacissima L.) under controlled temperatures and water stress. S. Afr. J. Bot. 94, 210–217 (2014).Article 

    Google Scholar 
    44.Petrů, M. & Tielbörger, K. Germination behaviour of annual plants under changing climatic conditions: Separating local and regional environmental effects. Oecologia 155(4), 717–728 (2008).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Cavallaro, V. et al. Evaluation of variability to drought and saline stress through the germination of different ecotypes of carob (Ceratonia siliqua L.) using a hydrotime model. Ecol. Eng. 95, 557–566 (2016).Article 

    Google Scholar 
    46.Tognetti, P. M., Mazia, N. & Ibáñez, G. Seed local adaptation and seedling plasticity account for Gleditsia triacanthos tree invasion across biomes. Ann. Bot. 124(2), 307–318 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Allen, P. S., Meyer, S. E. & Khan, M. A. Hydrothermal time as a tool in comparative germination studies. In Seed biology: advances and applications. Proceedings of the Sixth International Workshop on Seeds, Merida, Mexico, 1999. (ed. Black, M., Bradford, J. K. & Vazquez-Ramos, J.) 401–410. https://doi.org/10.1079/9780851994048.0401 (2000).48.Hu, X. W., Fan, Y., Baskin, C. C., Baskin, J. M. & Wang, Y. R. Comparison of the effects of temperature and water potential on seed germination of Fabaceae species from desert and subalpine grassland. Am. J. Bot. 102(5), 649–660 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Ramírez-Tobías, H., Peña-Valdivia, C., Trejo, C., Aguirre, J. & Vaquera, H. Seed germination of Agave species as influenced by substrate water potential. Biol. Res. 47, 1–9 (2014).Article 
    CAS 

    Google Scholar 
    50.Couso, L. Mecanismos de tolerancia a sequía y sus efectos sobre la habilidad competitiva de pastos de la estepa patagónica (Universidad Nacional de Buenos Aires, 2011).
    Google Scholar 
    51.López, D. R. Una aproximación Estructural-Funcional 1 del Modelo de Estados y Transiciones para el estudio de la dinámica de la vegetación en estepas de Patagonia norte (Universidad Nacional del Comahue, San Carlos de Bariloche, 2011).
    Google Scholar 
    52.Leva, P. E., Aguiar, M. R. & Premoli, A. C. Latitudinal variation of genecological traits in native grasses of Patagonian rangelands. Aust. J. Bot. 61(6), 475–485 (2013).Article 

    Google Scholar 
    53.López, D. R. & Cavallero, L. The role of nurse functional types in seedling recruitment dynamics of alternative states in rangelands. Acta Oecol. 79, 70–80 (2017).ADS 
    Article 

    Google Scholar 
    54.Coronato, F. R. & Bertiller, M. B. Precipitation and landscape related effects on soil moisture in semi-arid rangelands of Patagonia. J. Arid Environ. 34(1), 1–9 (1996).ADS 
    Article 

    Google Scholar 
    55.Coronato, F. R. & Bertiller, B. Climatic controls of soil moisture dynamics in an arid steppe of northern Patagonia, Argentina. Arid Land Res. Manag. 11, 277–288 (1997).
    Google Scholar 
    56.Heber, U., Santarius, K. A. Water stress during freezing. In Water and Plant Life. Ecological Studies (Analysis and Synthesis), vol. 19 (eds. Lange, O. L. et al.) 253–257. https://doi.org/10.1007/978-3-642-66429-8_16 (Springer, Berlin, Heidelberg, 1976).57.López, A. S., López, D. R., Caballe, G., Siffredi, G. L. & Marchelli, P. Local adaptation along a sharp rainfall gradient occurs in a native Patagonian grass, Festuca pallescens, regardless of extensive gene flow. Environ. Exp. Bot. 171, 103933 (2020).Article 
    CAS 

    Google Scholar 
    58.López, A. S., Azpilicueta, M. M., López, D. R., Siffredi, G. L. & Marchelli, P. Phylogenetic relationships and intraspecific diversity of a North Patagonian Fescue: Evidence of differentiation and interspecific introgression at peripheral populations. Folia Geobot. 53, 115–131. https://doi.org/10.1007/s12224-017-9304-1 (2018).Article 

    Google Scholar 
    59.Smith, S., Riley, E., Tiss, J. & Fendenhein, D. Geographical variation in predictive seedling emergence in a perennial desert grass. J. Ecol. 88, 139–149 (2000).Article 

    Google Scholar 
    60.Bohara, H. et al. Influence of poultry litter and biochar on soil water dynamics and nutrient leaching from a very fine sandy loam soil. Soil Tillage Res. 189, 44–51 (2019).Article 

    Google Scholar  More

  • in

    Ecological and biogeographic drivers of biodiversity cannot be resolved using clade age-richness data

    1.Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. The global diversity of birds in space and time. Nature 491, 444–448 (2012).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    2.Alroy, J. The shifting balance of diversity among major marine animal groups. Science 321, 1191–1194 (2010).ADS 
    Article 
    CAS 

    Google Scholar 
    3.Sakamoto, M., Benton, M. J. & Venditti, C. Dinosaurs in decline tens of millions of years before their final extinction. Proc. Nat. Acad. Sci. USA 113, 5036–5040 (2016).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Schluter, D. & Pennell, M. W. Speciation gradients and the distribution of biodiversity. Nature 546, 48–55 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Beaulieu, J. M. & O’Meara, B. C. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65, 583–601 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Silvestro, D., Schitzler, J., Liow, L. H., Antonelli, A. & Salamin, N. Bayesian estimation of speciation and extinction from incomplete fossil occurrence data. Syst. Biol. 63, 349–367 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Maliet, O., Hartig, F. & Morlon, H. A model with many small shifts for estimating species-specific diversification rates. Nat. Ecol. Evolution 3, 1086–1092 (2019).Article 

    Google Scholar 
    8.Etienne, R. S. et al. Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proc. R. Soc. B. Biol. Sci. 279, 1300–1309 (2011).Article 

    Google Scholar 
    9.Alfaro, M. E. et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Nat. Acad. Sci. USA 106, 13410–13414 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Raup, D. M. Mathematical models of cladogenesis. Paleobiology 11, 42–52 (1985).Article 

    Google Scholar 
    11.Magallon, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. Evolution 55, 1762–1780 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Yan, H.-F. et al. What explains high plant richness in East Asia? Time and diversification in the tribe Lysimachieae (Primulaceae). N. Phytol. 219, 436–448 (2018).Article 

    Google Scholar 
    13.Lu, H. P., Yeh, Y. C., Shiah, F. K., Gong, G. C. & Hsieh, C. H. Evolutionary constraints on species diversity in marine bacterioplankton communities. ISME J. 13, 1032–1041 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Miller, E. C., Hayashi, K. T., Song, D. Y. & Wiens, J. J. Explaining the ocean’s richest biodiversity hotspot and global patterns of fish diversity. Proc. R. Soc. B. Biol. Sci. 285, 20181314 (2018).15.Tedesco, P. A., Paradis, E., Leveque, C. & Hugueny, B. Explaining global-scale diversification patterns in actinopterygian fishes. J. Biogeogr. 44, 773–783 (2017).Article 

    Google Scholar 
    16.Lenzner, B. et al. Role of diversification rates and evolutionary history as a driver of plant naturalization success. New Phytol. 229, 2998–3008 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Gohli, J. et al. Biological factors contributing to bark and ambrosia beetle species diversifcation. Evolution 71, 1258–1272 (2017).PubMed 
    Article 

    Google Scholar 
    18.Wiens, J. J., Lapoint, R. T. & Whiteman, N. K. Herbivory increases diversification across insect clades. Nat. Comm. 6, 8370 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    19.Castro-Insua, A., Gomez-Rodriguez, C., Wiens, J. J. & Baselga, A. Climatic niche divergence drivers patterns of diversification and richness among mammal families. Sci. Rep. 8, 8781 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    20.Dorchin, N., Harris, K. M. & Stireman, J. O. Phylogeny of the gall midges (Diptera, Cecidomyiidae, Cecidomyiinae): systematics, evolution of feeding modes and diversification rates. Mol. Phyl. Evol. 140, 106602 (2019).Article 

    Google Scholar 
    21.Lu, L. et al. Why is fruit colour so variable? Phylogenetic analyses reveal relationships between fruit-colour evolution, biogeography and diversification. Glob. Ecol. Biogeogr. 28, 891–903 (2019).Article 

    Google Scholar 
    22.Hernandez-Hernandez, T. & Wiens, J. J. Why are there so many flowering plants? A multi-scale analysis of plant diversification. Am. Nat. 195, 948–963 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Paradis, E. Analysis of diversification: combining phylogenetic and taxonomic data. Proc. R. Soc. B. Biol. Sci. 270, 2499–2505 (2003).Article 

    Google Scholar 
    24.Ricklefs, R. E. Global variation in the diversification rate of passerine birds. Ecology 87, 2468–2478 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Ricklefs, R. E. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22, 601–610 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Alroy, J. Geographical, environmental, and intrinsic biotic controls on Phanerozoic marine diversification. Paleontology 53, 1211–1235 (2010).Article 

    Google Scholar 
    27.Chao, A. & Jost, L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93, 2533–2547 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Sepkoski, J. J. A kinetic-model of phanerozoic taxonomic diversity III. post-paleozoic families and mass extinctions. Paleobiology 10, 246–267 (1984).Article 

    Google Scholar 
    29.Budd, G. E. & Mann, R. P. History is written by the victors: the effect of the push of the past on the fossil record. Evolution 72, 2276–2291 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.Nee, S., May, R. M. & Harvey, P. H. The reconstructed evolutionary process. Philos. Trans. R. Soc. Lond. B. 344, 305–311 (1994).ADS 
    CAS 
    Article 

    Google Scholar 
    31.Diaz, L. F. H., Harmon, L. J., Sugawara, M. T. C., Miller, E. T. & Pennell, M. W. Macroevolutionary diversification rates show time dependency. Proc. Nat. Acad. Sci. USA 116, 7403–7408 (2019).Article 
    CAS 

    Google Scholar 
    32.Gingerich, P. D. Rates of evolution on the time scale of the evolutionary process. Genetica 112-113, 127–144 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Uyeda, J. C., Hansen, T. F., Arnold, S. J. & Pienaar, J. The million-year wait for macroevolutionary bursts. Proc. Nat. Acad. Sci. USA 108, 15908–15913 (2011).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Sepkoski, J. J. A kinetic model of Phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology 4, 223–251 (1978).Article 

    Google Scholar 
    35.Raup, D. M., Gould, S. J., Schopf, T. J. M. & Simberloff, D. Stochastic models of phylogeny and evolution of diversity. J. Geol. 81, 525–542 (1973).ADS 
    Article 

    Google Scholar 
    36.Foote, M. Pulsed origination and extinction in the marine realm. Paleobiology 31, 6–20 (2005).Article 

    Google Scholar 
    37.Stanley, S. M. Macroevolution: Pattern and Process. (Freeman, 1979).38.Strathmann, R. R. & Slatkin, M. The improbability of animal phyla with few species. Paleobiology 9, 97–106 (1983).Article 

    Google Scholar 
    39.Marshall, C. R. Five paleobiological laws needed to understand the evolution of the living biota. Nat. Ecol. Evolut. 1, 0165 (2017).Article 

    Google Scholar 
    40.Louca, S. & Pennell, M. W. Phylogenies of extant species are consistent with an infinite array of diversification histories. Nature 580, 502–505 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    41.Kozak, K. H. & Wiens, J. J. Testing the relationships between diversification, species richness, and trait evolution. Syst. Biol. 65, 975–988 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Wiens, J. J. & Scholl, J. P. Diversification rates, clade ages, and macroevolutionary methods. Proc. Nat. Acad. Sci. USA 116, 24400 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Wiens, J. J. Faster diversification on land than sea helps explain global biodiversity patterns among habitats and animal phyla. Ecol. Lett. 18, 1234–1241 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Nee, S. Birth-death models in macroevolution. Ann. Rev. Ecol. Evol. Syst. 37, 1–17 (2006).Article 

    Google Scholar 
    45.Scholl, J. P. & Wiens, J. J. Diversification rates and species richness across the Tree of Life. Proc. R. Soc. Lond. B 283, 20161334 (2016).
    Google Scholar 
    46.Aze, T. et al. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biol. Rev. 86, 900–927 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Foote, M., Cooper, R. A., Crampton, J. S. & Sadler, P. M. Diversity-dependent evolutionary rates in early Palaeozoic zooplankton. Proc. R. Soc. Lond. B 285, 20180122 (2018).
    Google Scholar 
    48.Sadler, P. M., Cooper, R. A. & Melchin, M. J. Sequencing the graptoloid clade: building a global diversity curve from local range charts, regional composites and global time-lines. Proc. Yorks. Geol. Soc. 58, 329–343 (2011).Article 

    Google Scholar 
    49.Grassle, J. F. The Ocean Biogeographic Information System (OBIS): an on-line, worldwide atlas for accessing, modeling and mapping marine biological data in a multidimensional geographic context. Oceanography 13, 5–7 (2000).Article 

    Google Scholar 
    50.Le Loeuff, J. Paleobiogeography and biodiversity of Late Maastrichtian dinosaurs: how many dinosaur species went extinction at the Cretaceous–Tertiary boundary? Bull. Soc. Geìol. Fr. 183, 547–559 (2012).Article 

    Google Scholar 
    51.Benson, R. B. J. Dinosaur macroevolution and macroecology. Ann. Rev. Ecol. Evol. Syst. 49, 379–408 (2018).Article 

    Google Scholar 
    52.Adrain, J. M. A synopsis of Ordovician trilobite distribution and diversity. Geol. Soc. Lond. Memoirs. 38, 297–336 (2013).Article 

    Google Scholar 
    53.Gradstein, F. M., Ogg, J. G., Schmitz, M. D. & Ogg, G. M. The Geological Timescale 2012. (Elsevier, 2012).54.Benson, R. B. J. et al. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biol. 12, e1001853 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    55.Alroy, J. et al. Phanerozoic trends in the global diversity of marine invertebrates. Science 321, 97–100 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Rabosky, D. L. Ecological limits on clade diversification in higher taxa. Am. Nat. 173, 662–674 (2009).PubMed 
    Article 

    Google Scholar 
    57.Foote, M. Symmetric waxing and waning of invertebrate genera. Paleobiology 33, 517–529 (2007).Article 

    Google Scholar 
    58.Quental, T. B. & Marshall, C. R. How the Red Queen drives terrestrial mammals to extinction. Science 341, 290–292 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar  More