Peatland degradation in Asia threatens the biodiversity of testate amoebae (Protozoa) with consequences for protozoic silicon cycling

Highlights

• Peatland degradation caused a significant loss of testate amoeba (TA) biodiversity.

• Unexpectedly, this loss was accompanied by an increase in TA biosilicification.

• TA biodiversity was not coupled to protozoic biogeochemical silicon (Si) cycling.

• New insights into microbial biogeochemical Si cycling on a continental scale.

Abstract

Anthropogenic peatland degradation is a global threat. As peatlands store large amounts of carbon (C) their potential for mitigation of climate change has been emphasized recently. Global C cycling is linked to silicon (Si) fluxes from the continents into the oceans. These fluxes in turn are driven by biosilicification, the incorporation of inorganic Si into living organisms, in terrestrial ecosystems. Biosilicification by testate amoeba (TA) communities and its potential for Si cycling has been highlighted since the beginning of the 21st century. However, the effects of peatland degradation on TA biodiversity and corresponding protozoic biosilicification on a continental scale remained unresolved so far. We show that TA biodiversity in Asian peatlands is strongly affected by the grade of human impact. This biodiversity decline was accompanied by an unexpected increase in protozoic biosilicification. Our findings provide new insights into the interactions between the biodiversity of soil microorganisms and biogeochemical Si cycling.

Introduction

Wetlands and peatlands are assumed to play an important role in the mitigation of climate change, because of their potential in carbon (C) sequestration (Lal et al., 2018, Leifeld and Menichetti, 2018). In addition, these ecosystems have been found to store large amounts of phytogenic silica, i.e., silicon (Si) stored in plant biomass (Struyf et al., 2010a, Struyf et al., 2010b). Si fluxes from terrestrial ecosystems into the oceans control C cycling on a global scale, because Si bioavailability is a key factor for the reproduction of marine diatoms, which in turn are able to fix large quantities of carbon dioxide (CO₂) via photosynthesis (Struyf and Conley, 2012). Thus, an understanding of Si cycling in peatlands is crucial to evaluate their role in C-Si interactions. In this context, the incorporation of inorganic Si into living organisms in the form of biogenic silica (biosilicification) has established a biological Si cycle, which controls global Si cycling (Derry et al., 2005, Struyf and Conley, 2009).

Anthropogenic desilication, i.e., the loss of Si in ecosystems caused by intensified land use (agriculture, forestry), has been identified as threat for global Si cycling. For example, in agricultural plant-soil systems Si exports via crop harvesting and increased erosion rates lead to pronounced Si losses causing a depletion of bio-available Si in agricultural soils (Struyf et al., 2010a, Struyf et al., 2010b, Vandevenne et al., 2012). As Si is beneficial for many plants, the loss of Si can result in inferior plant performance with consequences for ecosystem functioning (Katz et al., 2021). Most research on Si cycling in ecosystems is limited to the plant factor, i.e., Si cycling by vegetation. Information on Si cycling by other organisms like protozoa is still rare, although the potential of, e.g., testate amoebae (TA), for the terrestrial Si cycle has been emphasized since the beginning of the 21st century (Puppe, 2020).

TA are a diverse group of unicellular protists that build a test (shell), in which a single amoeboid cell is enclosed. They can be allocated to three different groups: (i) Arcellinida with lobose (finger-shaped) pseudopodia, (ii) Euglyphida with filose (thin thread-like) pseudopodia, and (iii) Amphitremida with anastomosing (network-like) pseudopodia and a shell with two openings (Meisterfeld, 2002, Adl et al., 2019). TA occur worldwide in various terrestrial and aquatic habitats and are particularly abundant in peatlands. Numerous studies have shown that TA are sensitive to environmental conditions such as hydrology in peatlands (represented by water-table depth, WTD), water quality, eutrophication in lakes and land-use change, which makes them useful as indicators for environmental changes (Mitchell et al., 2008, Roe and Patterson, 2014, Qin et al., 2020). The shells of TA are proteinaceous or composed of building blocks that can be either self-synthesized (idiosomes) or collected from the environment (xenosomes). Mostly, idiosomes consist of hydrated amorphous silica (SiO₂·nH₂O), which is formed in TA from monomeric silicic acid (H₄SiO₄). Although several studies have been focused on biosilicification by idiosomic TA in various terrestrial ecosystem sites (Puppe, 2020), knowledge on Si cycling by TA, corresponding control factors, and human impacts remains scarce, especially on a larger, e.g., continental, scale.

In Asia, most peatlands expanded rapidly as a result of Asian monsoon-driven hydrological changes occurring at the end of the Last Glacial Maximum (Xie et al., 2013, Treat et al., 2019). Asia has a relatively large area of peatland including both the most extensive peatland region (The West Siberian Lowland) and the largest single peatland (The Great Vasyugan Mire) on Earth (Beilman et al., 2009, Sheng et al., 2004). Asian peatlands occur extensively across Siberia, Far East, Kamchatka peninsula, northern China, Korea, and Japan. Some peatlands extend to mountains in the sub-tropical zone and even in tropical Asia (Qin et al., 2021a). The estimated coverage area of Asian peatlands was almost 1.6 × 10⁶ km² in 1990, which is corresponding to about 40% of the Earth’s total peatland area (Joosten, 2010).

Due to the fact that Asia has a large number of poverty stricken and low-developed regions, many peatlands have been damaged for development of agriculture, industry, and tourism by changes in hydrology and land-use (Qin et al., 2020). These human impacts mainly include drainage, Sphagnum harvest, peat cutting (Qin et al., 2021b), pasture (Noble et al., 2018), and fire events (Holden et al., 2015, Qin et al., 2017). This is aggravated by the fact that peatland restoration is quite difficult and often hampered by socioeconomic factors (Brown, 2020, Holden et al., 2011, Parry et al., 2014). Furthermore, the relevance of microbial organisms as key players in peatland functioning for the recovery of ecosystem services remains largely unclear (Ritson et al., 2021). As unicellular organisms including TA, the top predators in microbial food webs, control ecological processes in peatlands, knowledge on their response to perturbations related to land use and climate change is crucial. In this context, biogeochemical Si cycling by TA represents one important part of microbial functioning. However, research on how human activities affect the biodiversity of TA and corresponding protozoic biosilicification in peatlands is still rare (Qin et al., 2020).

In our study, we used published and previously unpublished data of 50 Asian peatlands including information on TA (abundance of different TA taxa) and environmental properties of peatlands that are known as most important controls for TA communities, i.e., water table depth, pH, and moisture contents (Mitchell et al., 2008, Qin et al., 2021a). To this data set we added information on climate (temperature and precipitation for the period 1991 to 2020) and peatland degradation (grade of human impact). Furthermore, we quantified biosilicification by idiosomic TA and analyzed interactions between TA biodiversity, peatland properties, climate, and human impacts with protozoic biosilicification. In doing so, we aimed at deeper insights into the effects of peatland degradation on TA communities and consequences for protozoic Si cycling on a continental scale. This knowledge will help us to assess the global relevance of peatlands for TA biodiversity on the one hand and protozoic biosilicification on the other hand, which is crucial to unravel the effects of human perturbations on microbial biodiversity and corresponding biogeochemical dynamics under global change.