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    The impact of industrial agglomeration on urban green land use efficiency in the Yangtze River Economic Belt

    Research areaThe YREB covers Shanghai, Jiangsu, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Chongqing, Sichuan, Guizhou, and Yunnan. It includes the Yangtze River Delta urban agglomerations (YRDUA), Yangtze River midstream urban agglomeration (YRMUA), and Chengdu-Chongqing urban agglomeration (CCUA). With a regional area of 2.05 million km2, the YREB runs through the eastern, central and western regions in China32. In 2019, the total GDP of YREB is 45.8 trillion yuan, accounting for 46.2% of the national GDP. The YREB plays a pivotal strategic support and leading role in the overall situation of stable economic growth in China33. At the same time, the contradiction between the shortage of land resources and economic growth in the YREB is very prominent. Therefore, this paper selects 107 cities in YREB as the research sample. The specific geographic locations are shown in Fig. 2. This article uses ARCGIS 10.2 version to draw the map. The URL link is http://demo.domain.com:6080/arcgis/services.Figure 2The geographic location of the YREB in China.Full size imageResearch methodsGlobal Malmquist–Luenberger indexUGLUE refers to the effective utilization degree of land elements under certain input of other elements. The green utilization of urban land mainly comes from three aspects: first, improve the utilization intensity of the existing actual input land, that is, increase the input intensity of other elements of the unit land area. Second, reduce the input of land in the production process to avoid excessive waste of land. Third, promote the optimal allocation of land elements among production units. Technical efficiency refers to the maximum degree that all factor inputs need to expand or shrink in equal proportion when all production units reach the production frontier. However, for production units with high technical efficiency, the factor allocation structure may not be reasonable. The land factors may still have the problem of under-input or over-input, resulting in the reduction of UGLUE.Pastor and Lovell34 proposed a global index, which uses all the inspection periods of each decision-making unit as a benchmark to construct the production frontier. According to the current benchmark construction period t, the production possibility set reference set is defined as follows:$$P_{C}^{t} (x^{t} ) = left{ {left. {(y^{t} ,b^{t} )} right|x^{t} {kern 1pt} can{kern 1pt} , produce{kern 1pt} , b^{t} ,y^{t} } right}$$
    (1)
    The global benchmark is defined as: (P_{G} = P_{C}^{1} , cup ,P_{C}^{2} , cup , cdots ,P_{C}^{t}), The subscripts C and G represent the current benchmark and the global benchmark respectively. The ML index of decision-making unit i is calculated based on the current reference benchmark:$$ML^{S} (x^{t} ,y^{t} ,b^{t} ,x^{t + 1} ,y^{t + 1} ,b^{t + 1} ) = frac{{1 + D_{C}^{S} (x^{t} ,y^{t} ,b^{t} )}}{{1 + D_{C}^{S} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} )}}$$
    (2)
    Among them, the superscript S indicates two adjacent periods, t period and t + 1 period. The subscript C indicates the current benchmark, which is a simplified directional distance function. (ML^{s} > 1), indicates that the productivity increases. (ML^{s} < 1), indicates that the productivity decreases.According to Hofmann et al.35, the GMLI is defined as follows:$$GMLI^{t,t + 1} (x^{t} ,y^{t} ,b^{t} ,x^{t + 1} ,y^{t + 1} ,b^{t + 1} ) = frac{{1 + D_{G}^{T} (x^{t} ,y^{t} ,b^{t} )}}{{1 + D_{G}^{T} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} )}}$$ (3) Among them, (D_{G}^{T} (x,y,b) = max left{ {alpha |(y - alpha y,b - alpha b) in P_{G} (x)} right}). (GMLI^{t,t + 1} > 1) indicates that the productivity has increased. (GMLI^{t,t + 1} < 1) indicates that the productivity decreases. The GMLI is further broken down as follows:$$begin{aligned} & GMLI^{t,t + 1} (x^{t} ,y^{t} ,b^{t} ,x^{t + 1} ,y^{t + 1} ,b^{t + 1} ) = frac{{1 + D_{G}^{T} (x^{t} ,y^{t} ,b^{t} )}}{{1 + D_{G}^{T} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} )}} \ & quad = frac{{1 + D_{G}^{t} (x^{t} ,y^{t} ,b^{t} )}}{{1 + D_{G}^{t + 1} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} )}} times left[ {frac{{(1 + D_{G}^{T} (x^{t} ,y^{t} ,b^{t} ))/(1 + D_{C}^{T} (x^{t} ,y^{t} ,b^{t} ))}}{{(1 + D_{G}^{T} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} ))/(1 + D_{C}^{T} (x^{t + 1} ,y^{t + 1} ,b^{t + 1} ))}}} right] \ & quad = frac{{TE^{t + 1} }}{{TE^{t} }} times left( {frac{{BPG_{t + 1}^{t + 1} }}{{BPG_{t}^{t + 1} }}} right) = EC_{t}^{t + 1} times BPC_{t}^{t + 1} \ end{aligned}$$ (4) Among them, TE is the change of technological progress. EC is the change of technological efficiency. The change of technological progress reflects the change of the highest technical level. The improvement of the highest technical level often requires the introduction and innovation of advanced technology, which often requires a large amount of investment. The change of technical efficiency reflects the gap with the highest technical level. Narrowing the gap with the highest technical level often requires improvements in internal management and governance structures. (BPG_{t}^{t + 1}) is the “best practitioner gap” between the current period and overall technological frontier. (BPC_{t}^{t + 1}) measures the changes in the “best practitioner gap” between two periods (technological changes). (BPC_{t}^{t + 1} , > , 1 ,) indicates technological progress. (BPC_{t}^{t + 1} < 1) indicates technology regress.Econometric techniques of industrial agglomeration on UGLUEIn recent years, many scholars used the traditional SPM for empirical analysis, which is a basic measurement model suitable for panel data. Therefore, this article firstly uses the traditional SPM to analyze the impact of industrial agglomeration on UGLUE. The formula is:$$begin{aligned} ln UGLUE_{it} & = alpha_{0} + alpha_{1} ln RZI_{it} + alpha_{2} ln RZI_{it} *ln RZI_{it} + alpha_{3} ln RDI_{it} + alpha_{4} ln EC_{it} \ & quad + alpha_{5} ln GDP_{it} + alpha_{6} ln TEC_{it} + alpha_{7} ln ROAD_{it} + alpha_{8} ln GOV_{it} + varepsilon_{it} \ end{aligned}$$ (5) Among them, ε is the disturbance term. i represents the city, i in this paper involves 107 cities in YREB. t represents the time, and the range of t in this paper is from 2007 to 2016. UGLUE is the explained variable, which represents the UGLUE. RZI and RDI are explanatory variables, representing industrial specialization agglomeration and industrial diversification agglomeration. EC is the industrial structure. GDP is the level of economic development. TEC is the level of technology. ROAD is the level of infrastructure. GOV is the degree of government intervention. (alpha_{1}) to (alpha_{8}) is the coefficient of each variable.Formula (5) assumes that the UGLUE changes with the changes of various influencing factors in the current period. That is, there is no time lag effect. But in reality, land use often has a time lag effect. The previous level has a non-negligible impact on the current results. Therefore, this paper selects the dynamic panel model for empirical analysis. However, there is often a two-way causal relationship between industrial agglomeration and UGLUE, which may cause endogenous bias. For example, cities with higher UGLUE levels tend to have higher levels of economic development, which promotes industrial agglomeration in this city. Therefore, this paper adopts the method of system GMM for regression analysis of dynamic panel model. Compared with mixed OLS, system GMM can make full use of sample information, select appropriate lag terms as instrumental variables36. It can effectively solve the endogeneity problem between industrial agglomeration and UGLUE. Based on the above analysis, this paper introduces the first-order lag term of UGLUE on the basis of formula (5). The DPM is as follows:$$begin{aligned} ln UGLUE_{it} & = beta_{0} + tau ln UGLUE_{i(t - 1)} + beta_{1} ln RZI_{it} + beta_{2} ln RZI_{it} times ln RZI_{it} + beta_{3} ln RDI_{it} \ & quad + beta_{4} ln EC_{it} + beta_{5} ln GDP_{it} + beta_{6} ln TEC_{it} + beta_{7} ln ROAD_{it} + beta_{8} ln GOV_{it} + varepsilon_{{{text{it}}}} \ end{aligned}$$ (6) Among them, (tau) is the first-order lag coefficient of UGLUE, reflecting the time lag effect of UGLUE.Variable descriptionExplained variableThe GMLI is used to measure the UGLUE of 107 cities in YREB. According to existing research37, the following core evaluation index of UGLUE are selected (see Table 1). Regarding input indicators, we mainly choose land element input M, labor element input L, and capital element input K as input indicators. Regarding output indicators, we choose the added value of the secondary and tertiary industries in the municipal area as the expected output, and use the GDP deflator to convert it into a comparable value. At the same time, pollution indicators such as industrial wastewater emissions, industrial sulfur dioxide emissions, and industrial smoke (dust) emissions are selected as undesired output. Since the GMLI reflects the growth rate of UGLUE, this paper assumes that the GMLI in 2006 is 1, and then multiplies the calculated GMLI year by year to obtain the development level of UGLUE in each city from 2007 to 2016.Table 1 Input and output index.Full size tableExplanatory variablesIndustrial specialization index ZI is usually used to measure the specialization level of urban industries. The specialization index is represented by the share of the employment of the industry in the total employment of the city:$$ZI_{i} = Max_{j} (S_{ij} )$$ (7) Nextly, we use the relative specialization index to make a horizontal comparison of the specialization level between different cities:$$RZI_{i} = Max(S_{ij} /S_{j} )$$ (8) The most common measure of the level of industrial diversification is the Herfindahl–Hirschman Index (HHI). For city i, the HHI is the sum of the square sum of employment shares of all industries in the city. The diversification index is the reciprocal of the HHI:$$DZ_{i} = frac{1}{{sumlimits_{j} {S_{ij}^{2} } }}$$ (9) The expression of relative diversification index is as follows:$$RDI_{i} = {1 mathord{left/ {vphantom {1 {sumlimits_{j} {left| {S_{ij} - S_{j} } right|} }}} right. kern-0pt} {sumlimits_{j} {left| {S_{ij} - S_{j} } right|} }}$$ (10) Among them, Sij is the employment proportion of j industry in city i, and Sj is the proportion of the total employment of the national j industry. The greater value of RZI and RDI, the higher level of industrial specialization and diversification.Control variablesRegarding control variables, we choose the following variables as control variables.Industrial structure (EC): The continuous optimization of industrial structure promotes the improvement of UGLUE through three aspects: saving land, increasing land income and promoting the optimal allocation of land resources. This paper selects the added value of the tertiary industry as a percentage of GDP (take the logarithm) to express.Technological level (TEC): The higher the technological innovation level of a city is, the more it promotes the use of input elements and the transformation of innovation results, thereby improving the UGLUE. This paper selects the proportion of science and technology expenditure to fiscal expenditure (take the logarithm) to represent.Economic development level (GDP): The continuous economic development promote the rational allocation of various production factors and increase the level of urban land output, thereby improving the UGLUE. This paper selects GDP per capita (take the logarithm) to express.Road infrastructure level (ROAD): The continuous improvement of infrastructure reduces transportation costs and transaction costs, and promotes communication externalities between producers, consumers, and between producers and consumers. This paper selects the average road area per capita (take the logarithm) to express.Government behavior (GOV): Fiscal expenditure is an important means for the government to carry out macro-control. Appropriate fiscal expenditure makes up for market shortages, improves factor flow and resource allocation efficiency, and realizes positive economic externalities. This paper selects the proportion of fiscal expenditure to GDP (take the logarithm) to express. We can see the meaning of specific variables from Table 2.Table 2 The descriptive statistics of variables.Full size tableData sourceThe object of this thesis is the 107 cities in YREB from 2007 to 2016. The urban construction land area data comes from the "China Urban Construction Statistical Yearbook", and the rest of the index data all come from the "China City Statistical Yearbook". The URL link is https://www.cnki.net/. In order to maintain the integrity of the data, this article uses the average method to fill in the missing values. In addition, because Chaohu City began to be under the jurisdiction of Hefei City in 2011, Bijie City and Tongren City in Guizhou Province only became prefecture-level cities in 2011. The three cities and Pu'er City are taken from the sample to maintain the continuity of data. More

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    Human activities favour prolific life histories in both traded and introduced vertebrates

    Data collectionWe obtained trade data from two different sources: the United States Fish and Wildlife Service (USFWS) Law Enforcement Management Information System (LEMIS)31 and the International Union for Conservation of Nature (IUCN) Red List32. We used the former to obtain data on the live wildlife trade in general and the latter for data on the pet trade specifically. We then matched trade data with our previously compiled global scale datasets of life history traits and introductions in mammals, reptiles and amphibians25,26.We obtained data on the US live wildlife trade from LEMIS by a Freedom of Information Act Request on 12/08/2019. We requested summary data on all US imports and exports of wildlife across all available years (1999-2019) and all trade purposes, including information on species identities and shipment contents (e.g. live individuals, meat, skins, etc.). For each species, we summed the total number of recorded shipments of live individuals (including individuals that died in transit, and live eggs) as a measure of trade frequency. We classified species as in trade if there was at least one shipment of live individuals recorded in the LEMIS database, and as not traded otherwise. The LEMIS dataset is geographically limited to trade by the US, and therefore may not capture the full diversity of species involved in the wildlife trade. For example, the LEMIS database may be missing some species involved in the substantial trade in live wildlife between South–East Asian countries50. However, the US represents one of the most dominant players in the global market for live wildlife16, and by summing both imports and exports we capture demand for species in countries beyond the US to some extent. Supplementary Fig. 2 illustrates the frequency of trade between the US and countries represented in the US LEMIS dataset. LEMIS data should be considered a minimum estimate of the diversity of species involved in the wildlife trade since they mostly record only legal trade (although confiscated shipments are recorded), and shipments are sometimes not identified to the species level16,51,53,53. The LEMIS database also contains some mis-spelled and incorrectly identified species due to human input errors52. To minimise the effect of misidentified shipments on our species level classifications of US trade status, we discarded all LEMIS records that were not identified to the species level (i.e. those identified using genus, common or generic names only), and manually checked the LEMIS data for synonyms and alternate spellings when we could not automatically match any records in LEMIS with species in our life history datasets. Species classified as traded on the basis of a single recorded live shipment in LEMIS are most vulnerable to species level misclassification due to misidentified shipments. The vast majority of traded species have multiple shipments recorded in LEMIS (259/312 [83%] of traded mammals, 265/285 [93%] of traded reptiles and 72/75 [96%] of traded amphibians), reducing the potential impact of shipment level misidentification over the reliability of species level trade classifications. However, to investigate the robustness of our findings to possible errors in species identification in LEMIS, we re-ran our key analyses excluding species classified as traded on the basis of a single live shipment. We found qualitatively the same effects of life history traits on the probability of trade when removing these species as in our full sample (Supplementary Tables 25–27). Despite its limitations, LEMIS is an invaluable resource for identifying broad scale trends in the wildlife trade since few other countries maintain such detailed records, and it is the only large-scale international trade dataset that includes both CITES- and non-CITES-listed species16,41. Including non-CITES listed species in our analyses is important because CITES-listed species represent only a small minority of those in trade14 and are likely to be a biased sample in terms of life history traits, since species vulnerable to extinction typically have slower life histories40.We obtained separate data on the pet trade from the IUCN Red List. The IUCN has assessed the vast majority of mammal, reptile and amphibian species (91%, 79% and 86% respectively54). Here, we classified a species as involved in the pet trade if the IUCN species account included at least one clear description of involvement in the pet trade. Otherwise, we considered a species as not involved in the pet trade. Although LEMIS records the purpose of trade, it uses broad categories (e.g. ‘Commercial’, ‘Personal’, ‘Breeding in captivity’), none of which refers specifically to nor necessarily equates to trade for pets. Therefore, we sought this additional data on the pet trade from the IUCN Red List instead of following the approach of some previous studies which have used LEMIS data as a proxy for the pet trade (e.g. Refs. 15,19). In contrast, the IUCN Red List contains clear textual descriptions of use and trade for many species, allowing us to identify which species are traded specifically for pets32. The IUCN data has further complementary strengths compared with LEMIS in that it is global in scope and includes both legal and illegal trade. We obtained data from the IUCN Red List by manually searching the binomial name of each species in our samples and consulting the ‘Threats’ and ‘Use and Trade’ sections of the species accounts. We classified species as in the pet trade if the information clearly stated this was the case (e.g. “It has been recorded in the pet trade”, “This species appears in the international pet trade”). We discounted descriptions where the information was uncertain (e.g. the species is described as “probably” or “possibly” traded for pets). We did not count as pets those species that the IUCN categorises as used for “Pets/display animals, horticulture” but which are used only for zoos or captive display, such as beluga whales (Delphinapterus leucas). All species described as pets by the IUCN are ‘exotic’, i.e. those without a long history of domestication14, since the IUCN does not list domesticated species.We matched trade data with our previously published global scale datasets on life history traits and introductions25,26. Internationally traded species may or not be released in the wild outside their native range: some may remain in the confines of captivity (e.g. in zoos or kept by private owners). We defined a species as introduced if there was at least one reliable record of its release, by humans, into the wild outside of its native range, either accidentally or intentionally25,26. We included only species with complete data for the same life history traits as used in our prior analyses (mammals: body mass, gestation period, weaning age, neonatal body mass, litter size, litters per year, age at first reproduction and reproductive lifespan; reptiles: body mass, hatchling mass, clutch size, clutches per year, age of sexual maturity, reproductive lifespan and parity; amphibians: snout-vent length, egg size, clutch size, age of sexual maturity and reproductive lifespan) to facilitate direct comparisons with previous results and to allow us to account for covariation between life history traits55. Species with complete life history data represent 7.8%, 3.5% and 1.6% of the total estimated number of species of mammals, reptiles and amphibians respectively56,57,58. These samples are not random as they over-represent orders containing many species of interest and utility to humans (e.g. ungulates, primates, crocodilians) (Supplementary Tables 28–30). However, these biases are unlikely to undermine our results since we examine life history effects on trade and introduction within these samples. Trade and introduction data do not necessarily cover the same time periods: the US dataset covers only the years 1999-present and the IUCN descriptions also typically refer to recent trade. In contrast, our introduction dataset includes both historical and recent introductions25,26. Therefore, the goal of our analyses is not to test causal hypotheses on the direct relationship between trade and introduction but rather to investigate whether the same life history traits predispose species towards both trade and introduction across diverse taxa, locations and circumstances. When combining the datasets and phylogenies59,60,61,62,63, we resolved species name mis-matches by referring to taxonomic information from the IUCN Red List32, the Global Biodiversity Information Facility (GBIF33) and the Integrated Taxonomic Information System (ITIS64). Table 1 summarises final sample sizes and Supplementary Table 1 the degree of overlap between the trade datasets. Most species in the pet trade are also in the general live wildlife trade, but many more species are traded by the US for general purposes than are involved in the pet trade specifically.Finally, we obtained data for a proxy measure of species detectability in order to control for a potential confounding effect on relationships between life history traits and introduction: larger bodied and longer-lived species may be more likely to be recorded by human observers when introduced compared with smaller and shorter-lived species. We obtained data on species occurrence records, geographic range size and population density, assuming that highly detectable species will have a disproportionately large number of recorded observations than expected based on the size of their geographic ranges and average population densities, following similar approaches by e.g. Refs. 65,66. We obtained occurrence records from the Global Biodiversity Information Facility (GBIF33) via the R package rgbif67 selecting only records resulting from human observation. We obtained range sizes (in decimal degrees squared) from the IUCN Red List32 and processed them for analysis using functions from the rgdal package68, excluding areas of uncertain presence (i.e. limiting range to presence code 1, ‘extant’). We obtained population density estimates from the TetraDENSITY database (version 134), a global database of population density estimates for terrestrial vertebrates. Most species in the TetraDENSITY dataset are represented by estimates from multiple different studies (median = 3, range 1–408). We collapsed density estimates to the species level by taking the median value across studies, including all estimates regardless of sampling method to maximise sample size, and converting all units to individuals/km2 to ensure comparability.Statistical analysesTo investigate relationships between life history traits and trade, we run models treating US or pet trade as the outcome variable and life history traits as the predictors. For all analyses, all life history variables were included in the same models to account for covariation among life history traits55. For US trade, where data on trade frequency are available, we run models both in which trade is treated as a binary variable (traded vs. not traded) and as a count variable (frequency of live shipments, including zero values), while for the pet trade, we have no data on trade frequency and so we treat pet trade as a binary variable only. To investigate the effects of life history traits on introduction, we run models in which introduction is the outcome variable and life history traits are the predictors. In introduction models, we only include traded species (running separate models for the set of species in US trade and the set of species in the pet trade). This approach allows us to disentangle effects associated with trade and introduction and thus identify at which stage(s) life history biases emerge. We also run introduction models in which frequency of US trade is included as an additional predictor alongside life history traits, anticipating that highly traded species are more likely to be introduced. Finally, to investigate possible confounding effects of species detectability on relationships between life history traits and introduction, we investigate effects of number of observations, geographic range size and, where sample sizes allowed, population density on the probability of introduction. If highly detectable species are more likely to be recorded as introduced, we expect to find a positive effect of the number of observations (while accounting for geographic range size and population density) on the probability of introduction. If this effect confounds relationships between body mass/lifespan and introduction, the effect of these life history traits on the probability of introduction should disappear when detectability measures are included in the models alongside life history traits. All analyses were conducted using the R statistical programming environment (Version 4.2.069). Plots were coloured using palettes from the viridis package70.To estimate effects of predictor variables, we fit generalized linear mixed models (GLMMs) using Markov chain Monte-Carlo (MCMC) estimation, implemented in the MCMCglmm package35,36. For analyses with binary outcome variables (traded vs. not traded, introduced vs. not introduced) we fit probit models, while for analyses with US trade frequency as the outcome variable we fit hurdle models. Hurdle models estimate two latent variables: the probability that the outcome is zero (on the logit scale), and the probability of the outcome modelled as a Poisson distribution for non-zero values71. This method therefore allows us to estimate effects of life history traits on the probability and frequency of trade in the same model. While the binary component of a hurdle model estimates the probability that outcomes are zero, when reporting results we reverse the sign of coefficients from the binary model for ease of interpretation, so that effects can be interpreted as the probability that the outcome is not zero. Therefore, here predictors with consistent effects on the probability and frequency of trade in hurdle models will have the same sign (so that if, for example, litter size has a positive effect on both the probability and frequency of trade, both coefficients for litter size from the hurdle model will be positive).Datasets comprising biological measures from multiple related species violate the fundamental statistical assumption that observations are independent of one another, since closely related species are more phenotypically similar than expected by chance due to their shared evolutionary history72. To account for the non-independence of species due to shared ancestry, we included a phylogenetic random effect in all models, represented by a variance-covariance (VCV) matrix derived from the phylogeny. The off-diagonal elements of the VCV matrix contain the amount of shared evolutionary history for each pair of species35,37,38 based on the branch lengths of the phylogeny (here proportional to time)59,61,62,63,63. This approach allows us to estimate phylogenetic signal using the heritability (H2) parameter, which measures the proportion of total variance in the latent variable attributable to the phylogeny35,37,38. Heritability is interpreted in the same way as Pagel’s λ in phylogenetic generalized least squares regression35,37,38,72. Specifically, phylogenetic signal is constrained between 0, indicating no phylogenetic effect so that species can be treated as independent, and 1, indicating that similarity between species is directly proportional to their amount of shared evolutionary history35,38,72. As hurdle models estimate two latent variables, for each hurdle model we report two heritability estimates, one for the binary and one for the Poisson component. All continuous independent variables were log-10 transformed due to positively skewed distributions. Although GLMMs do not require normally distributed predictor variables, log-transforming positively skewed life history predictors in phylogenetic comparative analyses allows us to model life history evolution on proportional rather than absolute scales. This is important as it facilitates biologically meaningful comparisons between species across large scales of life history variation73. Further, log-transforming positively skewed predictors helps to meet assumptions of the underlying Brownian motion model of evolutionary change, which assumes that phenotypic change along branches of the phylogeny is normally distributed74.We calculated variance inflation factors (VIFs) using functions from the car R package75 to check for multicollinearity between predictor variables. Where any model reported a variance inflation factor of 5 or above, indicating potentially problematic levels of collinearity76, we re-ran the model removing the variable with the highest VIF iteratively until all the remaining variables had VIFs of More

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    Plant nitrogen retention in alpine grasslands of the Tibetan Plateau under multi-level nitrogen addition

    Study siteThe field experiment was conducted at Namco Station (30°47’N, 90°58’E, altitude 4730 m) of the Institute of Tibetan Plateau Research, Chinese Academy of Sciences (ITPCAS), which is located in the alpine steppes of TP in China. The experiment was permitted by ITPCAS, complied with local and national guidelines and regulations. From 2006 to 2017, the mean annual temperature (MAT) and mean annual precipitation (MAP) was about − 0.6 °C and 406 mm, respectively. Monthly mean temperature varied from − 10.8 °C in January to 9.1 °C in July and most of the precipitation occurred from May to October37,38. During our six-year observations (2010, 2011, 2012, 2013, 2015 and 2017), climate change during the growing season from May to September varied differently, with the annual precipitation ranged from 255.9 mm to 493.8 mm and the MAT from 6.7 to 7.4 °C. Androsace tapete, Kobresia pygmaea, Stipa purpurea and Leontopodium pusillum were the dominant plant species at the alpine steppe.Experimental design and treatmentsThe long-term experiment began in May, 2010. Three homogenous plots were randomly arranged as replicates at the alpine steppe and six subplots (~ 13 m2) were distributed in each plot by a cycle, with a 2 m buffer zone between each adjacent subplot (Appendix S1: Fig. S1). In this experiment, six treatments of N fertilization rate (0, 1, 2, 4, 8, and 16 g N m−2 yr−1) were clockwise applied in each subplot. The subplots of 0 g N m−2 yr−1 were control group. We sprayed NH4NO3 solution on the first day of each month in the growing season (from May to September) each year. After fertilizing, we rinsed plant residual fertilizer with a little deionized water (no more than 2 mm rainfall). For the control groups, we added equivalent amount of water. The experiment was conducted from 2010 to 2017 (it should be pointed out that there was no fertilization in 2014 and 2016).Sampling and measurementsThe samples were collected with the training and permission of ITPCAS and involved plants that are common species and not endangered or protected. The identification of the plants was done by referring to a book of Chen and Yang39. Pictures of the corresponding specimens can be seen on the website of ITPCAS (http://itpcas.cas.cn/kxcb/kxtp/nmc_normal_plant/).Vegetation samples were collected in August in 2011 and repeated at the same time in 2012, 2013, 2015 and 2017. We established one 50 × 50 cm quadrat in each subplot, clipped aboveground biomass (AGB) and sorted species by families. The biomass was used to measure ANPP (g m−2 yr−1). Following aboveground portion collected, we used three soil cores (5 cm diameter) to collect the belowground roots at 0–30 cm depth and mixed into one sample, which were used to assess belowground net primary productivity (BNPP, g m−2 yr−1). The roots were cleaned with running water to remove sand and stones.Both plant and root samples were dried at 75 °C for 48 h and then ground into powder (particle size ~ 5 μm) by a laboratory mixer mill (MM400, Retsch). To determine N and C content of plants, we weighed the samples into tin capsules and measured with the elemental analyzer (MAT253, Finnigan MAT GmbH, Germany).Estimation of the critical N rate (Ncr), N retention fraction (NRF), N retention capacity and N-induced C gainAccording to the N saturation hypothesis, plant productivity increases gradually during N addition, reaches a maximum at the Ncr, and eventually declines16,17. We considered the Ncr to be the rate where ANPP no longer remarkably changed with N addition (Fig. 1).We defined plant N retention fraction (NRF, %; Eq. 1) as the aboveground N storage caused by unit N addition rate, and N retention capacity (g N m−2 yr−1; Eq. 2) was the increment of N storage due to exogenous N addition compared to the control40. The equations are as following:$$N;retention;fraction = frac{{ANPP_{tr} times N;content_{tr} – ANPP_{ck} times N;content_{ck} }}{N;rate}$$
    (1)
    $$N;retention;capacity = ANPP_{tr} times N;content_{tr} – ANPP_{ck} times N;content_{ck}$$
    (2)
    where ANPPtr and N contenttr (%) refer to those in the treatment (tr) groups, and ANPPck and N contentck refer to those in the control (ck) groups. These expressions are also used in the following equations (Eqs. 3–5).The N-induced C gain (g C m−2 yr−1; Eq. 3) was estimated by the increment of C storage owing to exogenous N addition compared to the control40. Maximum N retention capacity (MNRC, Eq. 4) and maximum N-induced C gain (Eq. 5) mean the maximum N and C storage increment in plant caused by exogenous N input at Ncr, respectively. The formulas are as following:$$N{text{-}}induced;C;gain = ANPP_{tr} times C;content_{tr} – ANPP_{ck} times C;content_{ck}$$
    (3)
    $$MNRC = ANPP_{max } times N;content_{max } – ANPP_{ck} times N;content_{ck}$$
    (4)
    $$Maximum;N{text{-}}induced;C;gain = ANPP_{max } times C;content_{max } – ANPP_{ck} times C;content_{ck}$$
    (5)
    where ANPPmax, N contentmax and C contentmax refer to the value of ANPP, N content and C content at Ncr, respectively.Data synthesisTo evaluate N limitation and saturation on the TP more accurately, we searched papers from the Web of Science (https://www.webofscience.com) and the China National Knowledge Infrastructure (https://www.cnki.net). The keywords used by article searching were: (a) N addition, N deposition or N fertilization, (b) grassland, steppe or meadow. Article selection was based on the following conditions. First, the experimental site must be conducted in a grassland ecosystem. Second, the experiment had at least three N addition levels and a control group. Third, if the experiment lasted for many years, we analyzed data with multi-year average. Based on the above, we collected 89 independent experimental cases. Among these, 27 cases were located on the TP alpine grasslands, 25 in the Inner Mongolia (IM) grasslands and 37 in other terrestrial grasslands (detailed information sees Appendix S2: Table S1).We extracted ANPP data and N addition rate of these cases and estimated Ncr and ANPPmax (Appendix S2: Fig. S2). We then calculated NRF, N retention and C gain of each group of data for further analysis (Appendix S2: Table S2). Most of the 89 cases did not have data on N and C content. To facilitate the calculation, we summarized N and C content from 40 articles in the neighboring areas of the cases and divided the N and C content into seven intervals according to the N addition rate (Appendix S2: Table S3 and Fig. S3). The unit of N addition rate was unified to “g N m−2 yr−1”. All the original data were obtained directly from texts and tables of published papers. If the data were displayed only in graphs, Getdata 2.20 was used to digitize the numerical data. For the estimation of N retention and C gain of the TP at current N deposition rates and future at Ncr, we fitted the exponential relationship to the data from 27 cases on the TP, and then substituted N rates into the fitted equations (Eq. 6):$$y = a times left[ {1 – exp left( { – bx} right)} right].$$
    (6)
    We also included MAT, MAP, soil C:N ratio, fencing management (fencing or grazing) and grassland type (meadow, steppe and desert steppe) of the experiment sites for exploring the drivers affecting N limitation (Appendix S2: Table S1). When climatic data were missing from the article, MAT and MAP were obtained from the WorldClim (http://www.worldclim.org).Species were usually divided into four functional groups (grasses, sedges, legumes and forbs) to study the response of species composition to N addition in previous study41. We synthesized 13 TP experimental cases (including our field experiment) from the data synthesis and each case included at least three functional groups (detailed references see Appendix S2).Statistical analysisThere were 42 species in our field experiment. We divided them by family into eleven groups: Asteraceae (forbs), Poaceae (grasses), Leguminosae (legumes), Rosaceae (forbs), Boraginaceae (forbs), Caryophyllaceae (forbs), Cyperaceae (sedges), Labiatae (forbs), Primulaceae (forbs), Scrophulariaceae (forbs) and Others. Due to species in the group of Others contributed only 1.22% of AGB, we analyzed AGB and foliar stoichiometry among other ten families (Appendix S1: Table S1). In Namco steppe, forbs, grasses, sedges and legumes accounted for 78.0%, 7.4%, 8.2% and 5.2% of the AGB respectively (Appendix S1: Table S1 and Fig. S2). Such a large number of forbs suggested that our experiment was conducted on a severely degraded grassland.For our field data, two-way ANOVAs were used to analyze the effects of year, N fertilization rate and their interactions on species AGB. One-way ANOVAs were used to test the response of ANPP, BNPP, root:shoot ratio, species foliar C content, N content and C:N ratio to N addition rate. Duncan’s new multiple range test was used to compare the fertilization influences at each rate in these ANOVAs. Prior to the above ANOVAs, we performed homogeneity of variance test and transformed the data logarithmically when necessary. Simple regression was used to estimate the relevance among ANPP, NRF, N retention capacity and C gain with N addition rates.Structural equation modeling (SEM) was used to explore complex relationships among multiple variables. To quantify the contribution of drivers such as climate and soil to Ncr, ANPP, NRF and MNRC, we constructed SEM based on existing ecological knowledge and the possible relationships between variables. We considered environmental factors (MAT, MAP and soil C:N) and ANPPck as explanatory variables, and Ncr, NRF and MNRC as response variables. We included the ANPPck in the SEM rather than the ANPPmax because we wonder whether there was a relationship between ANPP in the absence of exogenous N input and the ecosystem N retention in the presence of N saturation. This has important implications for assessing N input. Before constructing the SEM, we excluded collinearity between the factors. In addition, Student’s t-test and one-way ANOVAs were performed to explain the effect of fencing management and grassland type on above response variables, respectively. The SEM was constructed using the R package “piecewiseSEM”42. Fisher’s C was used to assess the goodness-of-model fit, and AIC was for model comparison.Given the influence of extreme values in the data synthesis, we calculated the geometric mean of Ncr, NRF, N retention and N-induced C gain. All statistical analyses were performed with SPSS 26.0 and RStudio (Version 1.2.1335) based on R version 3.6.2 (R Core Team, 2019). More