Paleorecords reveal the increased temporal instability of species diversity under biodiversity loss
Introduction
Biodiversity provides the basis for the resilience of plant and animal communities to environmental perturbations (Isbell et al., 2011; Kiessling, 2005). The ongoing modern biodiversity crisis (Beaugrand et al., 2015; Panetta et al., 2018; Urban, 2015) highlights the urgent need to better understand the extent to which ecosystems will be resistant to future environmental perturbations. Several assessments have predicted that ∼15–35% of plant and animal species will become extinct as global average temperatures rise ∼2–3 °C above pre-industrial levels (Thomas et al., 2004; Urban, 2015). Many empirical studies have linked recent climate change to the temporal trajectory of biodiversity change (Harrison et al., 2015; Steinbauer et al., 2018); however, contrary to expectations, attempts to determine whether biodiversity tracks climatic warming over time have indicated both increases and decreases in biodiversity during recent decades (Brown et al., 2001; Harrison et al., 2015; Ricklefs, 1987). In the context of natural warming, it is still unclear how the species diversity of biological communities responds to climate change, and whether, and how these effects vary across contrasting ecosystems or along environmental gradients.
Most records of the effects of environmental drivers (e.g., climatic warming, drought, climatic variability) on biodiversity are based on decadal-scale ecological data (Engels et al., 2020). In many natural settings, it has proven difficult to disentangle natural variability from the effects of human-induced ecosystem change (Willis and Birks, 2006), as a result of the short timescales typically employed. Considering that modern biodiversity patterns are the product of long-term climate changes in the geological past, appropriate empirical assessments of the rate at which communities respond to climate change require long-term surveys of species communities (Willis and Birks, 2006). However, such surveys are scarce (Kidwell and Tomasovych, 2013; Martin and PelÁEz-Campomanes, 2014; Willis and Birks, 2006), and in particular it remains unclear whether the degree of species diversity loss and compositional turnover is mediated by the climatological context.
Paleorecords that cover much longer timescales, such as several centuries to millennia, provide a broader temporal context for examining the extent to which biodiversity varies with spatiotemporal changes in climate (Engels et al., 2020; Martin and PelÁEz-Campomanes, 2014; Willis and Birks, 2006). Recent research has revealed a rapid and significant increase (∼35%) in plant diversity in eastern Colombia during the Paleocene-Eocene Thermal Maximum (Jaramillo et al., 2010). In addition, a well-dated fossil record from northern California indicated a relatively minor reduction in small mammal diversity (∼20%) and the increasing dominance of generalist species in response to climate change during the last deglacial (Blois et al., 2010). These findings provide important knowledge of the responses to natural warming on geological time scales with a large resolution, focusing mainly on mammals and plants. Therefore, the fossil record that preserves high-resolution and greater number of taxa, especially invertebrates, and provides information on community dynamics, such as on whether individual species are added to or lost from communities, is also needed. Among the terrestrial invertebrates, terrestrial mollusks as the important decomposers within soil communities (Mason, 1970) are a diverse and abundant group of invertebrates inhabiting various soil environments (Dong et al., 2019; Nekola, 2003). They are abundantly preserved as fossils, for example in loess sediments, and they can be identified at the species level (Horsák et al., 2018; Richter et al., 2019; Rousseau and Wu, 1997; Sümegi et al., 2015; Wu et al., 2002). These characteristics make mollusks a unique model taxon for exploring past shifts in biodiversity (Rousseau et al., 1993) and their long-term linkages with climate change.
Here we present three high-resolution mollusk fossil sequences dating back 25 kyr, along with environmental gradients in the Chinese Loess Plateau (CLP) (Fig. 1). Our aim was to determine the response of mollusk communities to the last deglacial, which was characterized by rapid and frequent climatic fluctuations but an overall warming trend. During the last glacial maximum (LGM), mean annual temperatures were as much as ∼5–7 °C colder than today, but by ∼16 kyr B.P. the climate began to warm. Holocene climates were relatively stable, with temperatures ∼2 °C higher than today during ∼8-4 kyr B.P. (the Holocene climatic optimum) (Shakun et al., 2012), which is equivalent to modern warming predicted for the current century.
The three loess sites (Linxia, Jingchuan, and Yaoxian) are located in temperate steppe along a climatic and vegetation gradient from southeast to northwest, spanning ranges of ∼4 °C and 300 mm in mean annual temperature and precipitation, under the influence of the East Asian summer monsoon (EASM) (Liu, 1985). The northernmost site (Linxia) lies at the northern limit of the EASM and is characterized by low-diversity mollusk communities. For each site, we sampled mollusk fossils at 3-cm intervals from loess-paleosol profiles spanning the last 25 kyr (Figs. S1 and S2). We used a multiple index definition of biodiversity (the number of species, S; Shannon-Wiener index, H′) that includes components of species richness and evenness, together with redundancy analysis (RDA), to explore the rate and magnitude of diversity changes along the specified environmental gradients.
Section snippets
Study area and sites
The Chinese Loess Plateau (CLP) is located in the northern marginal zone of the East Asian summer monsoon (EASM) and is characterized by a steep climatic gradient. At present, mean annual temperature (Tann) increases from ∼6 to ∼13 °C, and mean annual precipitation (Pann) from ∼300 to ∼650 mm from northwest to southeast (Fig. 1). About 70% of the precipitation falls in the summer and autumn seasons when the EASM circulation transports tropical and subtropical moisture inland (Qian, 1991).
The
Temporal trend of mollusk species diversity since the last deglacial warming
We analyzed 255 mollusk fossil samples from three loess sections (81, 90 and 84 samples from Linxia, Jingchuan, and Yaoxian, respectively), comprising 28 mollusk species and 54,400 individuals (Fig. 2, Fig. 3). We used previously established chronological frameworks, based on 24 optically stimulated luminescence (OSL) dates (Fig. S3), which ensured that the fossil records spanned the Last Glacial Maximum (LGM), the last deglacial warming, and the Holocene epoch (Dong et al., 2015), with an
Climate-driven shift in soil-fauna-flora community composition
Temperature and precipitation are the two most important factors affecting soil faunal and floral communities (Chen and Gao, 1987; Wu et al., 2018). The mean temperature in the Chinese Loess Plateau (CLP) has been estimated to have increased by at least ∼5–7 °C since the last glacial maximum (LGM) to the early to mid-Holocene, which was ∼2 °C higher compared to the present (Lu et al., 2007; Wang et al., 2001). The loess magnetic susceptibility (MS) record exhibits substantial variations
Conclusions
The biodiversity and stability of terrestrial plant and animal communities are threatened by recent environmental disturbances. It is unclear whether the temporal stability of biodiversity in the face of climate change varies with environmental gradients in different communities due to the lack of long-term data. Here we report three centennial-resolution temporal sequences of mollusk diversity changes along environmental gradients in East Asia since the last deglacial warming. The results,
Author contributions
Y.D., N.W., and H.L. conceived the study, Y.D., N.W., F.L., L.H., and H.L. undertook the fieldwork, Y.D., N.W., F.L., L.H., and H.L. collected the mollusk data, Y.D. and L.H. identified and counted the mollusk species, Y.D. performed statistical analyses, Y.D., N.W., F.L., L.H., H.L., and N.C.S. wrote the text; N.C.S. contributed to the interpretation of the results and writing of the text. All authors commented on the interpretation of the results and gave final approval for publication.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Dr. Bin Wu, Dr. Daojing Wang and Dr. Wenwen Wen for their assistance with fieldwork, Dr. Jan Bloemendal and Dr. Chris Oldknow for editing the text. We also thank Dr. Robert Martin, Dr. Anthony R. Ives, Dr. Hong Qian, and Dr. Zhiheng Wang for their valuable comments and suggestions which considerably improved the manuscript. We also appreciate the helpful reviews and comments provided by Dr. T. Pearce and anonymous reviewers. This work was supported by the “Strategic Priority Research
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