Climate Change Altering Species Composition and Abundance Peer Review Article
Introduction
Global warming has exerted a profound influence on institute species diverseness at the community level (Arft et al., 1999; Klein et al., 2004; Elmendorf et al., 2012; Pauli et al., 2012; Steinbauer et al., 2018), and will go along to influence ecosystem processes, functioning, and ecosystem services to man society (Hector and Bagchi, 2007; Naeem et al., 2010; Hooper et al., 2012; Tilman et al., 2014; Isbell et al., 2017; Liu et al., 2018). For example, plant species loss may significantly reduce principal productivity and institute litter decomposition rates (Hector and Bagchi, 2007; Hooper et al., 2012). Consequently, examining the responses of plant communities to warming is disquisitional to accurately predict futurity changes in ecosystem backdrop.
Prior studies have revealed significant changes in species richness and relative abundance of found communities in response to warming particularly in alpine and arctic ecosystems (Grabherr et al., 1994; Klein et al., 2004; Walker et al., 2006; Elmendorf et al., 2012). For instance, experimental warming is reported to increase principal productivity and the relative affluence of grasses at the expense of the sedges and forbs in alpine meadows (Ganjurjav et al., 2016; Liu et al., 2018). A rapid loss of plant species has besides been recorded in tall meadows (Klein et al., 2004; Wang et al., 2012; Zhang et al., 2015, 2017). Analogous results have been obtained in arctic regions (Chapin et al., 1995; Walker et al., 2006). Nevertheless, nearly of these reports have focused on changes in constitute productivity or species diverseness at the community level (Klein et al., 2004), or on changes in relative abundance at the plant functional type level (Chapin et al., 1996; Ganjurjav et al., 2016; Liu et al., 2018). Moreover, most of these studies have reported the number of species lost but not the identity of the species that were lost.
Every bit a result, the result of global warming on species diversity at the species level is incompletely understood. The paucity of data at the species level is likely to result in misleading conclusions for iii reasons. Kickoff, it fosters the assumption that changes at the species level are consistent with changes at the institute functional blazon level. This supposition is almost probably incorrect considering information technology is unlikely that all of the species inside a specific functional type will change in abundance in the aforementioned way. For case, it is possible that ane species will increment its relative affluence fifty-fifty if the functional type to which information technology belongs decreases in overall abundance. Also, it is also possible that some species will increment in abundance while others will decrease, such that the abundance of the functional type to which they belong remains unchanged (Klanderud and Totland, 2005). 2d, the assumption that changes at the species level are consistent with changes at the plant functional type level leads to the speculation that species loss occurs simply in the plant functional types that decrease in relative abundance. Theoretically, this speculation is likely to be true just if the species decreasing in affluence are more likely to be lost, a speculation that thus far has not been tested. Third, in the context of global warming, it leads to the speculation that species loss is the result of warming-induced changes in species richness. This would be untrue if warming-induced changes in species identity differ amidst treatments. Specifically, if only species richness is considered, species loss could be masked by species invasion. Consequently, overlooking information at the species level can limit our ability to accurately predict future ecosystem operation, particularly when the selection effect (i.e., species identity effect) of species multifariousness on ecosystem functioning dominates the biodiversity—ecosystem functioning human relationship.
Here, we present data apropos changes in community species diversity, the relative abundance for four plant functional types (i.east., legumes, grasses, sedges, and forbs) and each plant species, and species identity in an tall meadow in eastern Tibetan Plateau, which is considered among the most sensitive ecosystems to climate change (Piao et al., 2012; Zhang et al., 2017). Nosotros employ the data to test the null hypothesis that warming-induced changes are consequent amongst the community level (as indicated by aboveground plant biomass, species richness, species variety, and evenness), the functional type level, and the species level. To test this hypothesis, we examined (1) whether changes in relative affluence are consistent among different plant functional types, (ii) whether changes in relative abundance are consistent amid different plant species within specific plant functional types, and (three) whether species loss occurs in the functional types whose relative abundances decreased by warming.
Materials and Methods
Report Site
This written report was conducted in an alpine meadow in Hongyuan County, Sichuan province, China (32°48′ N, 102°33′ E), in the eastern office of Tibetan Plateau. The elevation is ~3500 m above sea level. The climate is characterized by a short Jump and Autumn, cool mild Summer, and a long, cold Winter. The annual mean temperature is 1.7°C, with the minimum and maximum monthly hateful temperature is −9.3 and 11.ane°C in January and July, respectively. The annual mean precipitation is ~756 mm (but fluctuates significantly amid years, mostly ranging between 450 and 900 mm), over fourscore% of which occurs during May to September (Cao et al., 2018).
The meadow has been intensively grazed (due east.m., yak Bos grunniens, Hequ equus caballus Equus caballus, and Tibetan sheep Ovis aries) for decades. Local residents currently use the meadow as either summer pasture (grazing in the growing flavor from May to September only) or winter pasture (grazing in the non-growing flavour from October to April only). Our experiments were performed in a winter pasture. The vegetative cover of the meadow is more than 90%, and the average institute top is ~thirty cm. The vegetation is dominated by an aggregation of forbs (e.g., Saussurea nigrescens, Polygonum viviparum, Potentilla anserine, and Anemone trullifolia var. linearis), sedges (e.g., Kobresia setchwanensis and Carex spp.), and grasses (e.g., Deschampsia caespitosa, Festuca ovina, and Elymus nutans). Forth with a diversity of plant species (Xiang et al., 2009), many arthropods, such every bit pollinators (Hu et al., 2019), herbivores (Eleven et al., 2013), and dung decomposers (Wu et al., 2011) co-be in the meadow.
Experimental Design
During October 2014, 6 15 (length) × 15 (width) × two.v thou (superlative) open top chambers (OTCs) were randomly deployed in a fenced, apartment area of about 1.0 ha. Each OTC was large plenty to include the local species pool, microhabitat variation in our study site. The sides of all OTCs were covered with thin (<0.i mm) steel screen with a mesh size of 0.2 × 0.2 mm (Supplementary Figure 1A). Three of the chambers were additionally covered with 8 mm thick transparent tempered glass. Moreover, the roof of these three chambers was discontinuously covered past 250 0.three m (width) transparent glass strips with an angle of 45°, with a 0.6 m infinite between strips (Supplementary Figure 1A), which was judged sufficient to forestall any strong airflow stack result in the large warmed OTCs (Wilson and Tamura, 1968). Although ane-tertiary of the roof area of these chambers was covered by glass strips, these chambers are referred to every bit OTCs (Supplementary Figures 1A,B). All the six chambers were placed one m into the soil, and steel screens (with a mesh size of 0.half-dozen × 0.half dozen mm) were placed 1 m into the soil along their sides to foreclose rodents from entering (Supplementary Figures 1A,B). The three OTCs with transparent tempered glass are designated as "warmed chambers" and the other three (with only steel screens) as "non-warmed chambers". It should be noted that the non-warmed chambers were constructed and installed to remove the confounding upshot of the concrete setting of OTCs (if whatsoever) on plant reproduction. It was observed (Xiaoli Hu, personal observation) that the steel sheets prevented arthropods inbound in both the warmed and non-warmed chambers, except for a few high-flying species such as honeybees (Apis mellifera and Apis cerana) that are abundant because of apiculture in the study site (Mu et al., 2014). Consistently, plant pollination was generally non express, every bit indicated by the indistinguishable departure (judged on the ground of a generalized linear model with binomial errors, P = 0.9) in seed set rate (sound seed number/total seed number) of the self-incompatible species Saussurea nigrescens among warmed chambers (0.65, due north = 15, sd = 0.18), non-warmed chambers (0.63, north = 21, sd = 0.21), and field sites outside chambers (0.68, northward =12, sd = 0.17). In addition, all six chambers were subject to horse grazing in the not-growing flavour (early Oct) in each study year from 2015 to 2018, making the study meadow a wintertime pasture (Supplementary Figure 2).
Measurements for more than 4-years using HOBO PRO (Onset Computer Corporation, USA) for air temperature and humidity and Watchdog2000 (Spectrum Technologies, Inc., USA) for soil temperature and moisture indicated that the mean almanac temperature was 0.3–0.5°C higher (at xxx cm above ground surface) and 0.2–0.v°C higher (at a 5 cm soil depth) in the warmed chambers compared to the non-warmed chambers (come across Table S1 and Figure S2 of Hu et al., 2020). During the non-growing season, the mean temperature was 0.iv–0.half dozen°C college (at 30 cm higher up footing surface) and 0.viii–i.i°C college (at v cm soil depth) in the warmed compared to the non-warmed chambers, whereas temperature increases were 0.03–0.47°C and −0.2–0.8°C, respectively during the growing season (encounter Tabular array S1 in Hu et al., 2020). The vapor force per unit area deficit, which was calculated based on air temperature and humidity measurements, was 2.6–three.7% higher in the warmed than in the non-warmed chambers during the growing seasons of 2018 and 2019. Moreover, soil moisture was two–three% (5/5) college at a 5 cm soil depth in the non-warmed compared to the warmed chambers (see Table S1 in Hu et al., 2020). In addition, transparency, which was calculated equally inside-bedchamber low-cal intensity/exterior bedchamber light intensity (measured using light meters; TES-1336A, Taiwan, Cathay) in the eye July of 2018, was slightly lower in the warmed chambers (94.4%, n = 45) compared to the non-warmed chambers (97.ix%, n = 45) (Hu et al., 2020).
Vegetation Sampling
Each chamber was subdivided into 9 5 × 5 thousand subplots. Species abundance was determined during early on-August each year using a quadrat sampling method (Pauli et al., 2015). Specifically, for each sampling (each year), we randomly placed five 100 × 100 cm quadrats in five of the ix subplots. Later, we divided each quadrat into 10 × 10 cm grids and recorded species presence and abundance following the protocols described by Pauli et al. (2015). In order to determine whether species loss occurred during the experiment, we extensively surveyed the entire establish community within each chamber, recording the presence of all plant species. Species that did not emerge for two consecutive years were designated equally "lost."
In the eye of August of each study year when most establish species completed reproduction, all aboveground plant parts were clipped to the ground surface and harvested in 16 1 × ane m quadrats that were randomly deployed in each sleeping room. The harvests were carefully sorted into four dissimilar functional types (i.due east., legumes, grasses, sedges, and forbs), and and so dried for 72 h at 75°C and weighed.
Data Analysis
At the community level, nosotros determined species diversity for each quadrat by calculating Shannon diverseness (i.due east., Loma number i) [i.e., )] and Shannon evenness (Hill ratio) (i.eastward., Eastward = D/S), where p i is the relative abundance (species-specific abundance/total abundance per quadrat) of the i th species out of S species) (Chao et al., 2014). Generalized linear mixed models (GLMMs) were used to decide the effect of warming on aboveground plant biomass, species richness, Shannon variety, and Shannon evenness (with Poisson errors for species richness, beta errors for Shannon evenness, and Gaussian errors for aboveground biomass and Shannon diversity). In each model, "treatment" (warmed vs. not-warmed) was set every bit the fixed factor, and "year" and "bedroom" as random factors. GLMMs were performed using the package "lme4" (Bates et al., 2015) and "R2jags" (Su and Masanao, 2020).
At the functional type level, the differences in the relative affluence and relative biomass (i.e., plant functional type-specific aboveground found biomass/total biomass) were determined between the warmed and non-warmed chambers, using GLMMs (with a binomial error structure) with "treatment" as the fixed factor and "year" and "chamber" as random factors. At the species level, the warming outcome on relative species abundance was determined using GLMMs (with a binomial error structure) with "handling" as the fixed factor and "yr" and "chamber" equally random factors. Merely those species occurring in both warmed and non-warmed chambers were considered.
To further examine changes in the establish customs composition during the experiment from 2015 to 2018, nosotros conducted a two-way permutational analysis of variances (PERMANOVA) on the Bray-Curtis dissimilarity matrix including the relative abundance for all species [with log(n + 1) transformation]. The PERMANOVA was run with 999 permutations using the "adonis2" part in the R package vegan v. ii.five–4 (Oksanen et al., 2014). The dissimilarity in species compositions between warmed and non-warmed chambers was besides computed using non-metric multidimensional scaling (NMDS) with Bray-Curtis distance and the "metaMDS" function in the R bundle vegan v. 2.5–four (Oksanen et al., 2014).
All analyses were performed using R 3.5.3 (R Cadre Squad, 2019).
Results
Changes at the Community Level
Experimental warming significantly increased aboveground found biomass starting in 2016 (Figure one). However, the divergence in species richness, Shannon diversity (equally indicated by the Loma number 1) and Shannon evenness between the warmed and not-warmed chambers were statistically not significant (Figure 2). Moreover, the PERMANOVA and NMDS analysis showed that the overall warming-induced change in species limerick was significantly unlike betwixt 2015 and 2018 (Tabular array 1; Effigy 3).
Figure 1. Aboveground biomass in both non-warmed and warmed chambers from 2015 to 2018. Different letters indicate a significant deviation (P < 0.05) between warmed and non-warmed chambers for each experimental twelvemonth.
Effigy ii. Establish species diversity in both non-warmed and warmed chambers from 2015 to 2018. (A) Species richness; (B) Shannon multifariousness (Hill number 1); (C) Shannon evenness (Hill ratio). No meaning divergence in each variable was found between non-warmed and warmed chambers for each study year.
Table 1. Summary of 2-way PERMANOVAs (F and P-values) on Bray-Curtis community limerick from 2015 to 2018.
Figure 3. Results of non-metric multidimensional scaling (NMDS) showing community dissimilarity between not-warmed and warmed chambers and years (2015–2018). Dissimilarity (Bray-Curtis) was estimated using the relative affluence of each species.
Changes at the Functional Type Level
Warming-induced changes in relative abundance differed significantly among the four establish functional groups (Table 2). Warming increased the relative affluence of grasses from 3 to xvi%, only decreased the relative abundance of forbs from 89 to 79% in 2018. In contrast, the relative abundance in the sedge and the legume functional groups did not significantly alter (Tabular array 2; Figure 4A). The relative biomass at the functional type level changed in a consistent way with respect to relative abundance (Tabular array 2; Figure 4B).
Tabular array ii. Summary of the GLMMs showing the warming issue on the relative affluence and biomass of sixteen species and four functional groups.
Figure 4. Divergence in relative abundance (A) and relative biomass (B) betwixt non-warmed and warmed chambers for each functional type (i.e., Legume, Grass, Sedge, and Forbs) from 2015 to 2018. Positive and negative values indicate an increase or a decrease in the warmed chambers. *P < 0.05; **P < 0.01; ***P < 0.001.
Changes at the Species Level
Species belonging to the aforementioned institute functional type showed unlike responses in relative abundance to warming (Table ii; Effigy v). Specifically, in the forb grouping, warming significantly decreased the relative affluence of Saussurea nigrescens (Table 2; Figure 5B), but significantly increased the abundance of Geranium pylzowianum, Potentilla anserine, and Euphrasia pectinate (Tabular array ii; Figures 5C,F,I) past 2018. Similarly, for the grasses, the relative abundance of Festuca ovina significantly increased, only remained unchanged for Koeleria macrantha (Table two; Figures 5K,L). In the instance of sedges, relative affluence decreased overall. However, Carex atrofusca significantly increased relative abundance as a effect of warming (Table ii; Figure 5N)
Figure 5. Relative abundance of 10 forbs (Gentiana abaensis, Saussurea nigrescens, Geranium pylzowianum, Polygonum viviparum, Anemone rivularis, Potentilla anserine, Potentilla discolor, Anemone trullifolia var. linearis, Euphrasia pectinate, and Anaphalis flavescens, A–J), two grasses (Festuca ovina and Koeleria macrantha, K,L), two sedges (Kobresia setchwanensis and Carex atrofusca, M,Northward), and two legumes (Oxytropis kansuensis and Lathyrus quinquenervius, O,P) in both non-warmed and warmed chambers from 2015 to 2018. Fault bars = 1 standard mistake of mean. Different letters indicate a significant difference (P < 0.05) between warmed and not-warmed chambers.
Over the study years, four forb species (i.e., Tibetia himalaica, Carum carvi, Microula sikkimensis, and Sanguisorba filiformis) were lost in both the not-warmed and warmed chambers. Two species (i.eastward., the perennial sedge Blysmus sinocompressus and the perennial forb species Saussurea stella) were lost in the warmed chambers, and the forb species Angelica apaensis was lost in the non-warmed chambers.
Word
Our results indicate that a warmed alpine meadow customs has a higher primary productivity (every bit indicated by aboveground plant biomass), and warming-induced changes in the relative affluence differ significantly amidst plant functional types. These responses are consistent with previous studies addressing the effect of experimental warming on grassland communities (Arft et al., 1999; Wang et al., 2012; Zhang et al., 2015; Ganjurjav et al., 2016). Importantly, data show that species inside the aforementioned plant functional blazon can respond differently to warming. These observations signal that reporting changes at the customs or functional blazon level is bereft to predict changes at the species level. In addition, species loss occurred in both types of chambers and unlike species were lost in unlike chamber types, such that reporting a change in species richness is insufficient for describing the change at the institute community level. Thus, reporting the identity of lost species and agreement how they are lost are important when attempting to predict what species are more likely to go locally extinct under warming climatic weather condition, a finding that has significance regarding conservation biology.
Although the warming-induced increase in aboveground institute biomass is consistent with previous warming studies in similar alpine meadows (Ganjurjav et al., 2016; Liu et al., 2018), changes in species diversity are less pronounced in this as opposed to other studies. For example, Chapin et al. (1995) showed that experimental warming reduced species richness by 30–50% in a tussock tundra; Klein et al. (2004) reported that warming over a menstruation of 4 years resulted in a 26–36% decrease in species richness in Tibetan alpine meadow; and Sternberg et al. (1999) reported that manipulated warming decreased species richness past 10% in a calcareous grassland. In our report, warming did not significantly change species richness, Shannon diversity, or Shannon evenness over a 4-twelvemonth period. This event contrasts with those of previous warming experiments conducted in alpine and arctic regions (Klein et al., 2004; Wang et al., 2012; Zhang et al., 2017). There are three possible explanations for why the warming-induced decrease in species richness is much smaller in our report system. First, the temperature increase in our experiment is smaller than that in other studies. Greater temperature increases oft induce more pronounced changes in plant species variety (Wang et al., 2019). Second, our experimental chambers are much larger than those used in previous studies. Large chambers might buffer the changes in species richness occurring at smaller and more homogeneous scales, i.e., larger chambers are likely to be more than heterogeneous in their microclimate and micro-soil conditions compared to smaller ones (Vellend et al., 2013; Suggitt et al., 2018). 3rd, in the nowadays study, the experimental control was non-warmed chambers compared to dispersal-unlimited field sites used in many other studies (e.m., Klein et al., 2004; Zhang et al., 2017). These chambers (including the warmed ones) were taller than those used in other warming studies (Klein et al., 2004, 0.4 m; Zhang et al., 2017, 0.4 thousand; Ganjurjav et al., 2016, 0.45 1000), which could accept significantly reduced or even prevented seed dispersal. Thus, seed dispersal would exist equally confined in this study, whereas information technology was more confined in the warmed chambers than open sites in the other studies.
The difference in relative abundance among functional types reported hither is also consequent with similar studies in our study region. Ganjurjav et al. (2016) and Liu et al. (2018) both reported a customs shift from ane dominated by forbs to one dominated by grasses in response to warming, whereas other studies indicated that sedge and legume species remain relatively unchanged in response to warming (Klanderud and Totland, 2005; Ganjurjav et al., 2016; Liu et al., 2018). These observations suggest that constitute growth is normally limited by the depression temperatures in tall meadows and that increased temperatures probable increase aboveground plant biomass and plant tiptop, which collectively increases interspecific contest for light. Tall grasses can competitively shade and exclude short forb and sedge species that tend to exist rosette-like and brusk. Moreover, although soil moisture was on average loftier in our meadow study site, warming reduced soil moisture to a low level (<20% v/five) during the dry season (usually in August). This reduction in soil moisture might have express the growth of sedge species and some forb species that are adapted to moist soil weather condition (e.g., B. sinocompressus and S. stella; meet besides Klanderud, 2008; Little et al., 2015; Cao et al., 2017), just favored the growth of drought-tolerant species such equally D. caespitosa and Festuca spp. (this study; see as well Klanderud, 2008; Little et al., 2015).
Importantly, individual species differed in their responses to warming both in direction and amplitude fifty-fifty for those within the aforementioned plant functional type. As noted, contrasting responses to warming have been observed in all plant functional types. This ascertainment is attributable to differences in institute traits even those within the same functional type. For example, virtually forb species decreased in relative affluence probably because of competitive exclusion by tall grass species. Still, iii forbs (i.e., G. pylzowianum, P. anserine, and East. pectinate) increased substantially in their relative abundance in the warmed chambers. The abundance increase in Thou. pylzowianum and P. anserine is consequent with previous studies (Klanderud, 2008; Li et al., 2011), and can be attributed to their belowground storage organ (tubers) and the habit of climbing growing, which allows individuals to vegetatively overgrow other plants, thereby avoiding shade compared to plants growing in not-warmed chambers. The increase in the abundance of E. pectinate is also consistent with previous findings (Nyléhn and Totland, 1999; Klanderud, 2008). The underlying machinery for its success is that this species is an almanac root hemi-parasitic forb that can absorb h2o and nutrients from monocot species. Consequently, it increases in abundance in tandem with the affluence of grass species. It could be argued that species with different traits should not be placed within the same functional grouping. However, assigning species to too many different functional groups presents additional issues. Even so, it is articulate that subtle differences amidst the species assigned to any functional species group tin can outcome in substantive differences in response to warming, whether induced experimentally or experienced under natural field atmospheric condition.
Although differences in species richness were statistically indistinguishable between warmed and not-warmed treatments, species loss was demonstrably manifest as indicated by the fact that both warmed and not-warmed chambers experienced species loss and that dissimilar species were lost in the two different types of chambers. A number of factors may contribute to this observation. For example, in both warmed and non-warmed chambers, the loss of the forb species Carum carvi and Microula sikkimensis might have been the result of reduced disturbance and increased plant density during the experiment, considering these species usually abound in ruderal or bare areas. The loss of the forbs Tibetia himalaica and Sanguisorba filiformis might be due to the shading of tall grasses because these ii species are brusk and rare. The loss of the forb species Saussurea stella and the sedge species Blysmus sinocompressus in warmed chambers may perhaps be the result of decreasing soil moisture and their competitive exclusion past tall plants. Both of these species are short and often grow in high-moisture microhabitats (Xiaoli Hu, Personal Observation; Flora of Red china, http://world wide web.iplant.cn/). Finally, the loss of the forb species Angelica apaensis in non-warmed chambers may reverberate its demographic stochasticity considering this species is extremely rare.
In summary, the results presented here evidence that a small increase in mean annual temperature and a winter-biased higher temperature during the non-growing flavor induces significant changes in an alpine meadow plant customs, equally evidenced by shifts in the relative affluence and biomass of unlike institute functional types. The results also betoken that changes in species relative affluence and biomass are not necessarily consistent with those of plant functional types, indicating that the data from plant functional types can obscure important information most the differential responses of private species to climate alter. Peradventure more than important, whether species loss occurs cannot be deduced from changes in species richness. Collectively, species-level information is necessary to accurately predict plant community responses to global change. Future studies should consider the behavior of individual species when predicting changes in ecosystem functioning or service, or making policy decisions concerning biodiversity protection and conservation.
Data Availability Statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries tin can be directed to the corresponding author.
Author Contributions
SS started the project and designed research, and drafted the manuscript. XH, WZ, and XL performed research. SS, XH, and KN analyzed data and wrote the manuscript. All authors contributed to the article and approved the submitted version.
Funding
This work was financially supported by National Science Foundation of China (31530007, 32071605, and 31325004).
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed every bit a potential conflict of interest.
Acknowledgments
We give thanks Xinwei Wu, Xinqiang Xi, Liang Zhang, Fengqun Meng, Bin Lan, Rui Cao, Lei Hu, Dongbo Li, Tan Li for field and lab assistance and Qinghai-Tibetan Research Base of Southwest University of Nationalities for providing research convenience.
Supplementary Fabric
The Supplementary Material for this commodity can be found online at: https://www.frontiersin.org/manufactures/ten.3389/fevo.2021.569422/full#supplementary-material
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Source: https://www.frontiersin.org/articles/10.3389/fevo.2021.569422/full
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