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Effects of Mowing Frequency on Soil Nematode Diversity and Community Structure in a Chinese Meadow Steppe

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Effects of Mowing Frequency on Soil Nematode Diversity and Community Structure in a Chinese Meadow Steppe sustainability Article Effects of Mowing Frequency on Soil Nematode Diversity and Community Structure in a Chinese Meadow Steppe Jinling Zhao 1,2,† , Jiale Chen 3,†, Honghui Wu 3,*, Linghao Li 1 and Fengjuan Pan 4,* 1 State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China; [email protected] (J.Z.); [email protected] (L.L.) 2 College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China 3 Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China; [email protected] 4 Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, China * Correspondence: [email protected] (H.W.); [email protected] (F.P.) † Jinling Zhao and Jiale Chen contributed equally to this work. Abstract: Soil nematodes are one of the most important components in terrestrial ecosystems and the critical factor driving the belowground process. The grasslands of Northeast China have been subject to mowing for ages, which theoretically should have had substantial effects on the processes associated with soil nematodes. However, relevant studies have barely been conducted to date. This study examined variations in soil nematode abundance, biomass, diversity, and community structure, with respect to varying mowing frequencies. The results showed that a higher mowing frequency significantly reduced the abundance of soil nematodes, biomass, diversity, and community structure stability in the ecosystem, while intermediate mowing frequency enhanced these parameters to different extents. Our findings indicate that the changing patterns of the nematode indices with mowing frequency conform to the intermediate disturbance theory. This study provides a theoretical Citation: Zhao, J.; Chen, J.; Wu, H.; basis for formulating grassland-related management measures and maintaining the stability of Li, L.; Pan, F. Effects of Mowing grassland ecosystems. Frequency on Soil Nematode Diversity and Community Structure Keywords: grassland; nematodes; biodiversity; mowing frequency in a Chinese Meadow Steppe. Sustainability 2021, 13, 5555. https://doi.org/10.3390/su13105555 1. Introduction Academic Editor: Chunjiang An Grassland ecosystems are the single largest terrestrial biosphere in the world and play a crucial role in primary production and ecosystem functioning [1]. They support Received: 9 April 2021 the livelihood of over one-fifth of the world’s population and maintain the largest soil Accepted: 26 April 2021 Published: 17 May 2021 carbon and nitrogen pools on Earth. More and more studies show that most ecological functions are substantially dependent on belowground processes, notably carbon and Publisher’s Note: MDPI stays neutral nitrogen cycling, in which soil nematodes are the predominant driving force [2]. with regard to jurisdictional claims in Soil nematodes may appear at various trophic levels of the soil food chain, being highly published maps and institutional affil- sensitive to changes in vegetation-soil-related aspects [3], which is largely due to their high iations. diversity at species to trophic level. Four trophic or feeding habit-associated groups are most predominant in the free-living soil nematodes, namely bacterivores, fungivores, plant parasitic nematodes, and omnivores/predators [4]. These groups differ substantially in ecological functioning and have rather differential, niche widths in soils. Bacterivores and fungivores consume soil microbes in large amounts, thus imposing significant impacts on Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. soil organic matter decomposition and nutrient release, while plant parasitic nematodes This article is an open access article have direct impacts on vegetation growth, because they mainly feed on fresh organs that distributed under the terms and are most important in the primary production of plant communities, such as leaves and conditions of the Creative Commons fine roots. They also use root exudation and thus affect the rhizospheric absorption of Attribution (CC BY) license (https:// nutrients and water [5]. Omnivores and predatory nematodes have significant impacts on creativecommons.org/licenses/by/ soil fauna appearing at lower food chain positions, and thus alleviate the feeding activity 4.0/). of soil animals on microbes [6]. Sustainability 2021, 13, 5555. https://doi.org/10.3390/su13105555 https://www.mdpi.com/journal/sustainability Sustainability 2021, 13, 5555 2 of 10 A number of studies show that soil nematode abundance and biomass vary signifi- cantly with season and site-specific conditions, which is due mainly to variations in soil temperature, moisture, aeration, and soil carbon availability [7–9]. By contrast, the genus diversity is much more related to the plant species composition and the shoot to root ratio of the vegetation in question [2,10–13], with dominant plant species in particular [14]. It is likely that the soil nematode should be affected by mowing and the response might be altered by the frequency of mowing. This is because mowing has a notable effect on soil temperature, moisture, aeration, and soil carbon availability, and the frequency of mowing mediates the magnitude of these responses [15,16]. Studies have shown that moderate cutting can increase the diversity of vegetation [15]. On the other hand, heavy mowing will also increase the pH of the soil, reducing the carbon distribution in the above-ground part and the abundance of soil biomass. Therefore, different levels of cutting have different effects on the environmental factors of soil nematodes [16–18]. However, few studies have investigated the effect of mowing and its frequency on soil nematodes. Studies on soil nematode ecology in grassland ecosystems are conducted mostly in North American prairies and much less in Eurasian steppes. Although most of these studies examined the effects of livestock grazing on the abundance aspect, only a few dealt with its impacts on the ecological functional aspects [3]. By contrast, our knowledge about the effects of mowing on soil nematode communities in grasslands is extremely limited. The Hulun Buir steppe of Inner Mongolia is a temperate meadow steppe in nature, which is highly representative of the Eurasian steppe. Mowing is the most dominant human practice in this region, especially in the last several decades. Because the soil is more fine-textured and xeric, while water-logging occurs frequently in wet years, the meadow steppe is assumed to be unique and significant in terms of soil animal-related aspects. However, studies on soil nematode communities with respect to mowing have been poorly documented [1]. In the present study, we examined the impact of mowing frequency on the soil nematode community structure and genus diversity in a grassland ecosystem of north- eastern Inner Mongolia. Three objectives were addressed, including: (1) to quantitatively evaluate the effect of mowing frequency on the individual density and cumulative biomass of soil nematodes at trophic group and community levels; (2) to estimate the change trend of soil nematode diversity and community structure, under different mowing frequencies, and (3) to unravel the relations and controls with respect to mowing-resultant variations in community structure and diversity of soil nematodes. 2. Materials and Methods 2.1. Site Description The field survey was conducted in a meadow steppe ecosystem located in north- eastern Inner Mongolia (49◦330 N and 120◦050 E). The relief is gently undulating, be- ing between 670 and 677 m in elevation. The continental climate is prevalent, gen- erally being muted and semi-arid. The mean annual temperature varies between −5 and 2 ◦C, and the frost-free period lasts around 110 days. The annual precipitation av- erages about 376 mm, with 80% falling in summer. The vegetation is dominated by Leymus chinensis, a widespread, rhizomatous grass species. Important companion species include Stipa baicalensis, Carex duriuscula, Galium verum, Bupleurum scorzonerifolium, and Filifolium sibiricum. Chestnut soil is predominant, which is equivalent to Castanozems in the soil taxonomic system of the FAO, being neutral to slightly alkaline and sandy-loam in texture [18,19]. The experiment was built on a meadow, fenced in 2005 to avoid the influence of large herbivores. The mowing treatments were started in 2005, with six treat- ments being randomly arranged: high mowing frequency (M1), with the pasture being mowed once a year; intermediate mowing frequency (M2 and M3), mowed once every 2 and 3 years; low mowing frequency (M6 and M12), mowed once every 6 and 12 years; and control (CK), not mowed throughout. In each treatment, five replicates were set in an Sustainability 2021, 13, 5555 3 of 10 even manner, each with an area of 0.4 ha. Pastures under all treatments were mowed in mid-August of the relevant years. 2.2. Extraction and Identification of Soil Nematodes Soils were sampled from a 0–20 cm soil layer with a 5 cm diameter auger in August 2018. Ten soil samples were collected from each replication, and a composite soil sample was derived from 5 sampling spots across each replicate of a treatment. Due to the limitation of laboratory space, nematodes in M3 and M12 were extracted 5 days late. Soil nematodes were extracted by a modified Baermann funnel method, with 100 g of fresh soil being used for one sampling spot [20,21]. The nematodes were submerged in hot water
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