Spatial ecology of soil nematodes: Perspectives from global to micro scales

Journal Pre-proof Spatial ecology of soil nematodes: perspectives from global to micro scales

Ting Liu, Feng Hu, Huixin Li PII:

S0038-0717(19)30229-9

DOI:

https://doi.org/10.1016/j.soilbio.2019.107565

Article Number:

107565

Reference:

SBB 107565

To appear in:

Soil Biology and Biochemistry

Received Date:

22 November 2018

Accepted Date:

09 August 2019

Please cite this article as: Ting Liu, Feng Hu, Huixin Li, Spatial ecology of soil nematodes: perspectives from global to micro scales, Soil Biology and Biochemistry (2019), https://doi.org/10. 1016/j.soilbio.2019.107565

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Spatial ecology of soil nematodes: perspectives from global to micro scales

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Ting Liua,b, Feng Hua,b and Huixin Lia,b,*

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a

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Nanjing, 210095, China

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b

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Nanjing, 210095, China

College of Resources and Environmental Sciences, Nanjing Agricultural University, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization,

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*Corresponding

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Address: No. 1 Weigang, Nanjing, Jiangsu Province, China 210095

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Email: [email protected]

author

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1

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Abstract

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Soil spatial heterogeneity is a major determinant of biological diversity and functions.

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Among soil biota, nematodes are considered as excellent models for understanding spatial soil

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ecology due to their wide niche breadth in diet, lifestyle and living habitat. Their distribution,

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community composition and functional diversity in heterogeneous environments provide

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insight into identification of factors that driving spatial heterogeneity of populations and

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activities of soil organisms. In this review, we synthesize current knowledge on spatial ecology

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of soil nematodes providing new testable hypotheses and proposing new roads for future

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research. We evaluate recent studies on the latitudinal patterns of soil nematodes and

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summarize key determinants of nematode spatial distribution from global to micro (millimeter)

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scales based on the studies published over the past few decades. We found relative contribution

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of drivers influencing nematode distribution vary across spatial scales, and soil properties (e.g.,

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soil organic matter) operating at all spatial scales thus can be considered as key drivers. We

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suggest two biological interactions, i.e., nematode-prey interactions as well as nematode-host

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interactions, which are expected to act as powerful determinants of the patchy distribution of

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microbes and plants from micro to field scales. We outline some directions for future research,

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including vector-mediated dispersal ecology, distribution pattern of functional traits at large

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scales, global change-induced distribution of populations, diversity and functional traits. The

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ultimate goals of this review are to extend our knowledge of nematode spatial ecology and to

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push forward the research on soil spatial ecology to meet global challenges.

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Keywords: Soil nematodes; Spatial distribution; Dispersal; Latitudinal pattern; Aboveground;

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Belowground

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1. Introduction

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The spatial distribution of soil organisms is less studied as compared to plants and animals,

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and reveals a major disparity among the fields of ecology since soil biota are arguably the most

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diverse and abundant group of organisms on the Earth (Bardgett and Van Der Putten, 2014). A

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number of studies published in the last 20 years has demonstrated that soil organisms exhibit

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spatially predictable, aggregated patterns over scales ranging from hectares to square

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millimeters (Ettema and Wardle, 2002; Fierer and Jackson, 2006; Decaëns, 2010; Wall et al.,

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2012), overriding the long-standing view that everything is everywhere. These studies also

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show strong evidence that spatial patterns of soil biota and their determinant factors have

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profound impacts on multiple ecosystem functions, such as decomposition, nutrient supply, and

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the growth and community structure of plants (Ettema and Wardle, 2002). However, studying

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spatial ecology of soil biota is still challenging due to the limited knowledge of their taxonomy

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and enormous differences in the life-forms, functions and sizes of soil species (Bardgett and 2

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Van Der Putten, 2014; Coleman et al., 2017).

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This paper focuses on the spatial patterns of soil nematodes, factors driving their

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distributions and the effects of nematode spatial patterns on soil microbial and plant

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communities. As the most numerous micro or mesofauna in the soil (Neher, 2001), the

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nematodes are widely adopted in the spatial ecology research due to several distinctive

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attributes. First, nematode feeding group identification can be easily deduced from the mouth

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structure (Bongers and Ferris, 1999). Our knowledge of their taxonomy, feeding roles and

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functional traits is more abundant as compared to our understanding of other soil fauna (e.g.,

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mites and collembolans) (Neher, 2001). Besides, nematodes occupy all consumer trophic levels

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within the soil food web and comprise multiple feeding groups (Yeates et al., 1993), thus they

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are expected to be tightly linked with plants, microbes and many other soil organisms.

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Moreover, nematodes are ubiquitous in the world’s soils because they have successfully

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adapted to nearly all soil environments, from tropical to polar regions (Powers et al., 1995;

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Maslen and Convey, 2006; Porazinska et al., 2012; Kerfahi et al., 2016), from agricultural to

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desert ecosystems (Pen-Mouratov et al., 2003; Liang et al., 2009; Neher, 2010), and from

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macroaggregate to microaggregate fractions (Lazarova et al., 2004; Briar et al., 2011; Zhang et

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al., 2016).

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For the past 20 years, nematodes have been used as bioindicators in soil ecological studies.

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Their composition and structure responds quickly to abiotic and biotic factors, which may alter

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the habitat of soil nematodes and therefore drive their distributions (Bongers and Ferris, 1999;

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Yeates and Bongers, 1999; Neher, 2010; Ferris et al., 2012). Spatial heterogeneity of nematode

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distribution is observed from global to micro scales, and it is strongly associated with various

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environmental factors, dispersal processes, and intrinsic population processes such as

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reproduction and competition (Ettema and Wardle, 2002). An explicit analysis of these patterns

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is required to improve our understanding of determinants controlling nematodes and other soil

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organisms across temporal and spatial scales. This review provides insights as to how these

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complex factors (i.e., environmental factors and intrinsic population processes) contribute to

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the spatial distribution of soil nematodes and ecological interactions between nematodes,

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microbes and plants.

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2. Distribution patterns at different spatial scales

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Spatial patterning of soil nematodes occur both vertically, through the soil profile, and

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horizontally. Here, we focus on horizontal patterns from global to micro scales and shortly

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discuss the vertical patterns (< 1m) at micro to fine scales. We will not dissociate agricultural

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and natural ecosystems and discuss each ecosystem separately, because there are many similar

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patterns available between the two ecosystems and different ecosystems largely focus on

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different scales. For example, studies conducted at continental and global scales are largely 3

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derived from natural ecosystems and all studies about the effect of plant community and

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diversity on nematode spatial distribution at local and field scales are derived from natural

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ecosystems. These studies suggest that nematodes are usually not randomly distributed but

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exhibit aggregated patterns over scales ranging from global to micro, which are scale-dependent

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and controlled by environmental factors and population processes (Fig. 1).

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2.1 Continental to global scales (> 1000 kilometers)

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Our knowledge of the macroecology and biogeography of soil nematodes has advanced in

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recent years, but the latitudinal patterns of nematode diversity or abundance are still

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controversial. Some of the studies observe clear latitudinal patterns. Wu et al. (2016) showed

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that nematode taxonomic diversity decreased with the increase in the latitude along the Chinese

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coast (continental-scale, ranges from 20°N to 40°N). A meta-analysis studied global-scale

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distribution of mangrove nematodes observed a higher genus richness at lower latitudes, closer

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to the equator (Brustolin et al., 2018). A survey of nematode diversity at two contrasting

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latitudes of North American meridian found that species richness was higher in the tropical

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rainforest than the temperate forest (Porazinska et al., 2012). These studies have provided

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evidence to support the view that the ‘classic’ biogeographical patterns of macrobiota (e.g.,

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plant, mammals and amphibians) also exist for soil nematodes. In contrast, using more than

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6700 georeferenced samples, van den Hoogen et al. (2019) observed the highest nematode

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abundances in the tundra, followed by boreal forests and temperate broadleaf forests, while the

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lowest abundances were observed in Mediterranean forests, Antarctic sites and hot deserts. This

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result reveals a latitudinal pattern of nematode abundance, providing evidence that soil

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nematode abundance is higher in Arctic and sub-Arctic regions than in temperate or tropical

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regions. The authors suggest that the result may attribute to high soil organic carbon stocks at

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high altitudes compared to lowland regions, because low temperatures and high moisture

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content in high-latitude regions restrict annual decomposition rates (van den Hoogen et al.,

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2019).

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Other studies report that nematode abundance is high along most of the latitudinal

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gradients (5544-23185 individuals kg-1 dry soil) and decline sharply in polar regions (1290 kg-1

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dry soil) (Nielsen et al., 2014). For example, an early review concluded that nematodes were

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most diverse and abundant in temperate regions, followed by tropical habitats, with the fewest

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species and smallest populations in the Arctic and Antarctic (Procter, 1984). Similarly, a meta-

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analysis found that the abundance and genus richness of soil nematodes were higher in

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temperate than tropical forests, and the maximum nematode abundance and genus richness

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were recorded at latitudes between 30° and 55° (Song et al., 2017). It is interesting that Kerfahi

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et al. (2016) observed a similar alpha diversity of soil nematodes between equatorial rain forest

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and High Arctic tundra. The similarity in alpha diversity between the tropical and polar regions 4

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may be because the authors collect only five samples in each site, since undersampling may

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lead to weak patterns (Meyer et al., 2018). It has been suggested that the lower nematode

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diversity in tropics than in temperate forests and other regions may be because the habitats

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above the mineral soil are seldom studied, because 62% of the diversity exists in litter and

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understory habitats but not in soils (Powers et al., 2009). These findings indicate that the

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latitudinal distribution of nematodes may not follow the ‘classic’ trend observed in large

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organisms such as plants, mammals, amphibians and plant-feeding insects (Wu et al., 2011;

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Nielsen et al., 2014; Kerfahi et al., 2016). Lack of universal pattern has also been observed in

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other soil organisms, such as earthworms, mites, protists and mycorrhizal fungi (Finlay, 2002;

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Fierer and Jackson, 2006; Öpik et al., 2006; Maraun et al., 2007; Tedersoo et al., 2012).

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There is a growing recognition in soil ecology that most soil organisms are restricted in

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their global distributions, challenging the view that everything is everywhere (Callaway and

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Maron, 2006; Wu et al., 2011; Tedersoo et al., 2012; Bates et al., 2013). The spatial distribution

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of nematodes at global scales is mainly driven by geographical factor (e.g., geographic isolation)

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(Sohlenius and Boström, 2005), and environmental factors, such as climate (e.g., temperature,

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precipitation), vegetation type and soil properties (e.g., soil organic matter and pH, Table 1)

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(Nielsen et al., 2014; Wu et al., 2016). Among these factors, geographic barrier and climate

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variables should be considered as integrators, because both of them can influence the vegetation

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type and local soil properties first, which has consequences for soil invertebrates that inhabit

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this environment (Nielsen et al., 2014; Monroy et al., 2012). Although nematode trophic groups

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differ in dietary specialization and life-history strategies (r- and K-strategists), their abundance

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have been reported to be consistent in latitudinal trends and were all determined by the

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availability of soil organic matter, which showed the same pattern as total nematode abundance

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(van den Hoogen et al., 2019). Generally, nematodes feeding on bacteria are the most abundant

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and diverse group, distribute across all soil habitats on the earth, followed by herbivorous and

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omnivorous nematodes, while fungivorous and predatory nematodes are the least abundant and

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diverse feeding groups (Yeates, 2003; Neher et al., 2005; Neilson et al., 2014; Kerfahi et al.,

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2016; Wu et al., 2016; van den Hoogen et al., 2019).

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It is increasingly recognized that evolutionary history may leave a detectable signal in

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large-scale patterns of species diversity (Emerson and Gillespie, 2008; Fritz and Rahbek, 2012).

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Therefore, the unclear patterns of nematode distribution along latitude or at global scale can be

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partly due to the lack of knowledge of nematode evolution, which depends a lot on phylogenetic

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analysis. By incorporating information on evolutionary history, we suggest that the phylogeny-

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based approaches may provide a novel view of the nematode communities, which may

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compensate species richness-based approaches to test the hypotheses related to spatial patterns,

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such as the latitudinal gradient, species-area and distance-decay relationships (Fig. 2). For

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example, the taxonomic diversity and phylogenetic diversity of nematodes respond differently 5

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to the increase in latitude (Wu et al. 2016). The phylogenetic distance of soil nematodes does

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not change along environmental gradients (Li et al., 2014), which differs from a general

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phenomenon observed in many organisms that the similarity of species richness is decreased

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with geographic distance (Nekola and White, 1999; Soininen et al., 2007).

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2.2 Local to field scales (meter to kilometers)

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The spatial heterogeneity of nematodes at the local and field scales is often related to soil

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properties (e.g., soil organic carbon, pH, texture, soil moisture and bulk density) (Table 1). For

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example, the distribution of herbivorous nematode Pratylenchus across variable landscape of a

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typical dryland wheat farm (> 1000 m) is highly aggregated and patchy. The most important

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factor affecting Pratylenchus population is the amount of soil organic carbon, which shows a

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negative relationship with the herbivorous nematode (Kandel et al., 2018). The herbivorous

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nematode community in a sugarcane field (16 × 21 m) is positively correlated with soil pH, Na+

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content and organic carbon (Godefroid et al., 2013). In a cultivated ecosystem, spatial

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distributions of bacterivorous, fungivorous, omnivorous and predatory nematodes are

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positively correlated with soil pH and texture (percentage of sand and silt) (Robertson and

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Freckman, 1995). These case studies provide evidence that soil organic carbon and pH seems

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to be the most important soil properties driving the distribution of soil nematodes at local scale.

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Specialist nematodes are largely constrained to specific habitats. Herbivorous nematodes

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display a wide variety of interactions with their hosts, and some of them can be detected in soils

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grown with specific plants (Yeates et al., 1993). For example, Meloidogyne and Heterodera are

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abundant in tomato (Ferris et al., 1996; Bulluck Iii et al., 2002) and soybean fields (Baird and

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Bernard, 1984; Pan et al., 2010). Tobrilus is an algivorous nematode (Yeates et al., 1993) and

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ubiquitous in paddy rice fields because of the abundance of its preferred food, e.g., algae and

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diatoms, in the water and on the soil surface during flooding (Okada et al., 2011; Liu et al.,

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2016a). Hirschmanniella is a large-bodied herbivorous genus found in the paddy rice fields of

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China (Liu et al., 2016c), Japan (Okada et al., 2011) and many other Asian countries (Timsina

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and Connor, 2001). The bacterivorous genus Rhabdolaimus is abundant at the karst mountain

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peaks of southwest China (Zhao et al., 2015a) and also the dominant taxon in hot springs in the

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Granada province of Spain (Ocaña, 1991), where soils experience severe dry-wet cycles, high

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salt contents and extremely high temperatures. These examples suggest that local environment

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and food resource play a very important role in constraining the distribution of specialist

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nematodes.

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Plant communities can drive the distribution of soil nematodes in the natural ecosystems,

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either by directly attracting herbivorous nematodes or by returning plant residues to attract

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specific feeding groups (Veen et al., 2010; Bardgett and Van Der Putten, 2014; Gutiérrez et al.,

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2016; Liu et al., 2016b). In a semi-natural grassland, Viketoft (2007) found that plants induced 6

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spatial distribution of nematodes by attracting different herbivorous and bacterivorous

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nematodes to specific plant species. In a savanna parkland where woody plant clusters

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distributed irregularly (20-140 m apart) in the grassland, Biederman and Boutton (2010)

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observed that densities of omnivorous and predatory nematodes in woody clusters were lower

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than those in grassland and edge communities. The effect of spatial patterning of plants on

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nematode distribution is apparent related to the plant diversity and community structure.

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Generally, soils with more diverse plant species have more diverse nematodes, and different

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plant species or functional groups support different nematode feeding groups (De Deyn., 2004;

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Viketoft., 2005; Viketoft., 2009), for example, legumes increase bacterivorous nematodes while

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forbs favor fungivorous nematodes (Viketoft., 2009).

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Ecosystem type has a strong influence on nematode assemblages. In China, bacterivorous

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and herbivorous nematodes have greater species richness and populations in agricultural soils

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(Hu and Qi, 2010; Pan et al., 2010; Jiang et al., 2013; Lu et al., 2016; Zhong et al., 2016),

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whereas omnivorous and predatory nematodes are more common in forest than agricultural

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soils (Zhang et al., 2012; Zhao et al., 2014; Li et al., 2015). Similarly, in Poland, herbivorous

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and bacterivorous nematodes are most abundant in agricultural soils, omnivorous nematodes

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are more common in grasslands than agricultural soils, while fungivorous nematodes are more

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abundant in forest than agricultural soils (Neher, 2010). This can be due to the fact that most of

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the bacterivorous taxa are r-strategies (cp 1-2) with short generation time and high fecundity.

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They are tolerant to disturbances in agriculture and their reproduction and activity can be

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favored greatly with the application of fertilizers (Bongers and Ferris, 1999). In contrast,

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omnivorous and predatory taxa are K-strategies (cp 3-5) with long generation time and low

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fecundity, thus these species are sensitive to disturbance (Bongers and Ferris, 1999).

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Spatial distribution of soil nematodes at the agricultural field may exist both because of

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and in spite of human activities (e.g., tillage, cropping and fertilization), depending on

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nematode genus and feeding groups. Bacterivorous, omnivorous and predatory nematodes are

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more aggregated in the agroecosystem with many years of soil tillage and monoculture

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cropping (Robertson and Freckman, 1995). In contrast, the distribution of herbivorous

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nematodes is less influenced by tillage and crop rotation (Robertson and Freckman, 1995). In

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soybean fields, no tillage promotes aggregation of plant parasitic nematodes, whereas

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conventional tillage results in more uniformly distributed nematode populations (Gavassoni et

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al., 2001). It appears that agricultural management is less important for the aggregation of plant

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parasitic nematodes than free-living soil nematodes, which can be related to the feeding and

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life history strategies of nematodes. Considering the feeding habit of plant parasitic nematodes,

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it is reasonable to speculate that they are likely to be uniformly distributed after the agricultural

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management, since crops are evenly distributed in the agricultural field.

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2.3 Micro to fine scales (millimeter to centimeters)

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Nematode spatial heterogeneity at distances < 1 m is described by considering soil layers.

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In general, nematodes exhibit patchy distribution within the soil profile due to substrate

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availability and soil properties. For example, nematode population density decreases

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significantly with soil depth, which is related to the decline in soil organic matter and change

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in other soil properties such as moisture, pH, nitrogen, texture and bulk density (Ou et al., 2005;

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Tong et al., 2010; Salame and Glazer, 2015; Scharroba et al., 2016) (Table 1). There is also a

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strong correlation between nematode community and vertical distribution of plant roots and

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biomass (Yeates, 1999; Powers et al., 2009). Furthermore, the spatial distribution of nematodes

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through the soil profile depends upon which feeding group is studied. For example,

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bacterivorous nematodes dominate in the plough layer (0-10 cm) of a wheat field, whereas

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herbivorous nematodes increase in deeper soil layers (40-70 cm) and are the dominant group in

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the 40-50 cm depth (Scharroba et al., 2012). Herbivorous nematodes, especially root-feeding

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nematodes are more clumped in deeper layers (Smiley et al., 2008), and relate closely to plant

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roots (Ferris and McKenry, 1974) and soil properties (e.g., temperature and moisture) (Brodie,

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1976).

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At the microscale, due to the limited mobility of soil nematodes and the complexity of the

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soil matrix, distribution patterns of soil nematodes are mainly determined by the porosity of

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soil aggregates, biotic interactions, root exudates and the distribution of substrate hotspots in

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the water-filled part of the pore space (Ettema and Wardle, 2002; Viketoft, 2013; Bardgett and

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Van Der Putten, 2014; Quist et al., 2017). The large macroaggregates (> 1000 µm) support

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large-bodied nematodes, such as herbivorous, omnivorous and predatory nematodes, whereas

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inter-aggregate soil and space (< 250 µm) favor small-bodied bacterivorous nematodes (Briar

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et al., 2011). Small macroaggregates (250-1000 µm) have more juvenile nematodes, because

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they offer juveniles a refuge from predators or represent a place of preferential nematode

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production (Briar et al., 2011). In a soil microcosm study with centimeter-scale (< 2 cm)

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measurements, Liu et al. (2018) found that network associations or interactions within

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nematode communities were lower in systems, where root exudates and straw residues were

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mixed together than in those where the two resources were presented in patches. Moreover,

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root exudates also contribute to microscale spatial patterns in nematode communities, serving

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to attract specific groups in the rhizosphere, such as bacterivorous Chronogaster, fungivorous

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Ditylenchus and Aphelenchus, and herbivorous Tylenchorhynchus (Liu et al., 2018).

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3. Dispersal as a key driver of nematode spatial distribution

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Dispersal is a vital process during the life-history of an organism (Bonte and Dahirel,

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2017), which is one of the key factors driving distribution of nematodes from micro to global

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scales (Fig. 1). However, the active dispersal of soil nematodes through soil matrix is generally 8

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limited to a few centimeters (< 10 cm in 48h) without the assistance of other transporters (Moyle

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and Kaya, 1981). Therefore, nematodes are often passively dispersed. Nematodes own several

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characteristics that facilitate their long-distance dispersal and account for their local, field and

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global distribution. The small size makes them easy to transport, while the evolved cryptobiotic

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capabilities (e.g., cryobiosis, anhydrobiosis, osmbiosis and aerobiosis) enable them to survive

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in adverse habitats (Keilin, 1959; Treonis and Wall, 2005).

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3.1 Continental to global scales (> 1000 kilometers)

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Transport of soil containing nematodes by wind, water, insects, birds and plants is believed

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to encourage the spread of nematodes across large geographical regions (Wallace, 1963; Poinar

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Jr, 1983; Procter, 1984; Nkem et al., 2006; Ptatscheck et al., 2018). Ptatscheck et al. (2018)

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observed that the wind-mediated dispersal rate of nematodes was up to > 3000 individuals m-2

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in four weeks, which was higher than other soil fauna like rotifers, collembolans, tardigrades

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and mites. Although nematodes may reach a new habitat with the assistance of various

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transporters, whether they can successfully colonize in the new environment depending on the

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quality of habitat, and adaptation to competitors, predators and parasites. In that case, most of

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soil nematodes detected at geographically distant sites are dissimilar. For example, only the

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family Cephalobidae is found distributed at all 12 sites around the world, whereas most of the

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other nematode families are restricted in distributions (Nielsen et al., 2014). Kerfahi et al. (2016)

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used molecular techniques to compare nematode community composition between Arctic and

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tropical regions and found that only 5% of nematode OTUs overlapped between two sites.

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Similarly, using molecular techniques, Porazinska et al. (2012) found that nematode

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communities were unique without even a single common species between the tropical rainforest

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and temperate rainforest.

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Some nematode species are reported to be globally distributed such as bacterivorous

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nematode Cephalobidae is a cosmopolitan family found in almost all soil habitats around the

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world, including ponds, polar, tundra, mine tailing, and deserts regions (Freckman and Virginia,

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1997; Pen-Mouratov et al., 2003; Bert et al., 2007; Li et al., 2014). Fungivorous nematodes

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belonging to Aphelenchoidae is another cosmopolitan family that tolerates many stressful

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environments, including those with elevated concentrations of heavy metals (Zhao and Neher,

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2013; Gutiérrez et al., 2016) and acidic soil conditions (Korthals et al., 1996; Háněl, 2001). The

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globally detected nematodes can be dispersed across larger distances, thriving in a wide variety

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of environmental conditions and feeding on a variety of foods. However, we believe that

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analyses of soil nematodes at higher taxonomic resolution (e.g., species level) will show

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different results as observed from the above studies. It has been reported that environmental

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specificity of prokaryotic taxa was not common at the higher taxonomic level (e.g., species),

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but emerged at lower taxonomic level (e.g., family) (Tamames et al., 2010). Besides, diversity 9

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in the genera of microorganisms has been greatly underestimated and their cosmopolitan

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perception has been challenged by molecular studies in historical biogeography, phylogeny and

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population genetics (Salgado-Salazar et al., 2013; Vanormelingen et al. 2007).

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3.2 Micro to field scales (millimeter to kilometers)

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The active dispersal of nematodes in the soil matrix is limited to 10 cm during 48h (Moyle

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and Kaya, 1981). Intrinsic population processes, such as reproduction and competition, are

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important drivers for active dispersal of nematodes at small scales. Some of the plant parasitic

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nematodes feed on the same plant cell for a long time and deposit all their eggs at the same

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location, resulting in highly aggregated spatial pattern of these species (Rossi et al., 1996). In

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contrast, other plant parasitic species move throughout the soil, thus their eggs been more

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widely distributed (Rossi et al.,1996). Competition can shape the evolution of dispersal through

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density-dependence since interactions become stronger when density increases (Lambin, 2001).

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Intraspecific and interspecific competitions are both important triggers for the active dispersal

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of soil nematodes, and species-specific differences in density-dependent dispersal existing in

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nematode species (De Meester et al, 2015). Other intrinsic population processes such as feeding

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habits and life history strategies are also important drivers for their active dispersal on

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microscales. Quist et al. (2017) found that feeding preference was a main determinant of

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microscale patchiness among terrestrial nematode. Moreover, using Taylor’s power law

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analysis, Park et al. (2013) observed that soil nematodes showed a higher degree of aggregation

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at the functional guild level than at the individual taxonomic group level. These population

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processes can drive active dispersion of nematodes at micro to fine scales, which are supposed

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to be clumped, uniform or random dispersion, depending on the feeding groups (Fig. 3).

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The passive dispersal of soil nematodes at the micro to field scales relies a lot on large-

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bodied soil fauna. The earthworms and gastropods (e.g., slugs and snails) assist dispersal of

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nematodes by transportation of nematodes on the surface or in the digestive tract (Shapiro et

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al., 1993; Sudhaus, 2018). With the help of insect hosts, entomopathogenic nematodes exhibit

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dispersal at the distances of 2-8 cm in the soils, suggesting that nematode distribution may be

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associated with the patchy distribution of hosts (Ruan et al., 2018; Spiridonov et al., 2007). In

339

an artificial chamber (2.5-5 cm), beetles are observed as important vector of plant parasitic

340

nematodes, as they will secrete ascarosides to attract dispersal of fourth-stage nematode larvae

341

and facilitate their movement into the beetle trachea (Zhao et al., 2016). The more mobile

342

animals, such as arthropods, ants and even large animals can drive spatial patterns of nematodes

343

at the local and field scales. For example, the movement of arthropods over the soil surface

344

increases dispersal and spatial distributions of entomopathogenic nematodes over a distance of

345

2 m in a potato field (Bal et al. 2017). In a grassland of The Netherland, soil disturbances by

346

ants and rabbits greatly influence spatial distributions of plant pathogenic nematodes (Olff et 10

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al., 2000). These examples suggest that soil nematodes can be dispersed by other organisms

348

through digestive tract, trachea or surface, among which transportation via ingestion is of

349

ecological interest. To date, the phenomenon that nematodes can be digested accidentally by

350

other organisms during feeding has been detected in several studies (Shapiro et al., 1993;

351

Sudhaus, 2018; Türke et al., 2018), but how nematodes can pass through their digestive tract

352

without injury merits further study.

353 354

4. Microbes and plants are influenced by nematode spatial patterning from micro to field

355

scales

356

The spatial pattern of nematodes is largely driven by microbes and plants, which provide

357

them with food resources. The interactions of nematodes associated with microbes (i.e.,

358

bacterivorous and fungivorous nematodes) and plants (i.e., herbivorous nematodes) can also

359

influence the spatial patterning of different microbial or plant species in a community (Cobb,

360

1914; Wardle, 2002; Bezemer et al., 2005; Bardgett and Van Der Putten, 2014). For example,

361

plant species promote herbivorous nematodes that contribute to their local decline. However,

362

in the past 30 years very few studies have been conducted to explore how patchy distribution

363

of soil nematodes and nematode activity drove spatial patterning of microbes and plants and

364

measure patterns in both nematodes and microbes or plants. The main obstacle may be that the

365

spatial patterns of soil nematodes and microbes have not been clearly determined. In this review,

366

we suggest two major pathways that nematodes may regulate the spatial distribution of

367

microbes and plants through feedbacks. These pathways are more likely to be biological

368

interactions but are expected to act as powerful determinants of the patchy distributions of

369

microbial and plant communities from micro to field scales. Future studies are encouraged to

370

test whether these interactions can drive the distribution of microbes and plants and explore

371

their corresponding patterns.

372

“Nematode-prey interactions”: Nematode predation has a strong impact on the

373

populations and community structure of soil microbes. Many studies conducted in pots or fields

374

observe positive relationships between nematode abundance and microbial biomass (Fu et al.,

375

2005; Blanc et al., 2006: Rønn et al., 2015). Jiang et al. (2017) showed that bacterivorous

376

nematodes enhanced bacterial diversity, and their abundance (especially the dominant genus

377

Protorhabditis) was positively correlated with bacterial biomass. Nematode selective grazing

378

can also change the bacterial and fungal community composition, because nematodes show

379

clear feeding preference on specific species (Ruess et al., 2000; Shtonda and Avery, 2006;

380

Salinas et al., 2007; Avery and You, 2012; Weber and Traunspurger, 2013; Liu et al., 2017).

381

For example, fungivorous nematodes show preference for particular fungal species (i.e.,

382

Epicoccum sp. and Monocillium sp.) in a chamber device (Ruess et al., 2000). Similarly,

383

bacterivorous nematodes show strong preference for plant growth-promoting rhizobacteria 11

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(PGPR) Pseudomonas fluorescens over other three soil-dwelling bacterial species in the culture

385

plate (Liu et al., 2017). Although these predator-prey interactions are largely detected in

386

controlled experiments, we suppose that they can have potential implications for predicting

387

spatial patterns of nematodes and microbes from micro to field scales. According to the spatial

388

patterns in aboveground predator-prey systems (Bohan et al., 2000; Fauchald et al., 2000), we

389

expect obvious patterns of spatial correlation (overlap) between nematode and microbial

390

populations. This may match with the intermediate disturbance hypothesis that highest

391

microbial species richness or populations occur at levels of moderate predation of soil

392

nematodes (Shea et al., 2004).

393

“Nematode-host interactions”: Nematodes that form associations with plant roots (e.g.,

394

root-associated nematodes, root pathogenic nematodes and some fungivorous nematodes) can

395

influence plant community through exhibiting differential feeding patterns on different plant

396

species. It has been suggested that root-associated nematodes could enhance plant species

397

diversity and vegetation succession by decreasing the nutrient uptake of dominant plant species

398

and improving the growth of subdominants, while root pathogenic nematodes do so by

399

suppressing dominant host plant species (De Deyn et al., 2003). Similarly, van der Putten and

400

Peters (1997) observed that herbivorous nematodes changed plant community structure by

401

reducing the competitive ability of their host to benefit the successional plant species. In a

402

grassland, animal disturbances influence spatial distributions of root pathogenic nematodes,

403

which further favor the grass Festuca rubra over the sedge Carex arenaria in disturbed patches

404

(Olff et al., 2000). Although these case studies are conducted at field scale without direct

405

measurements of spatial patterns, we can speculate that nematode grazing on plant species will

406

cause plant suppression and redistribution of soil water and nutrients. These are expected to

407

change the fragmentation of plant patches at the local field (Adler et al., 2001; Sommer, 2001),

408

either by decreasing or increasing the spatial heterogeneity of plant species, depending on the

409

spatial heterogeneity of nematode and its grazing strategy (Fig. 4).

410 411

5. Conclusions and prospects

412

In this review, we have summarized current knowledge of distribution patterns of soil

413

nematodes, their key drivers at different scales and potential impacts on spatial distributions of

414

belowground and aboveground communities. Some of the key findings are listed below: (1)

415

The relative contribution of drivers influencing nematode distribution vary across spatial scales,

416

and soil properties (e.g., soil organic matter) operate at all spatial scales thus can be considered

417

as key drivers. (2) Nematode diversity shows no consistent latitudinal trends at a global scale,

418

which may be attributed to methodological biases. The biases include undersampling in both

419

horizontal (inadequate sample size) and vertical dimensions (neglect of sampling in litter and

420

understory habitats), lowering taxonomic resolution of morphological identification, and lack 12

Journal Pre-proof 421

of knowledge of nematode evolution history. (3) Human activities driving spatial distribution

422

of soil nematodes in agriculture may differ between plant parasitic and free-living soil

423

nematodes at local and field scales. (4) The active dispersal of nematodes through soil matrix

424

is generally limited to a few centimeters, thus nematodes are largely passively dispersed at large

425

scales. (5) The overwhelming majority of nematode family or genus are restricted in global

426

distributions, and the nomination of cosmopolitan nematodes (e.g., the family Cephalobidae)

427

may be controversial if soil nematodes are analyzed at higher taxonomic resolution (e.g.,

428

species level). Although our knowledge of spatial ecology of soil nematodes has improved

429

greatly over the past couple of decades, there are still many research challenges to overcome

430

before we can achieve a better understanding of this field.

431

The molecular analysis of nematode assemblages should be promoted and optimized to

432

increase the analytical capacity of characterizing nematode communities. To date, identification

433

of soil nematodes is largely dependent on morphological characters and microscope approaches.

434

The time-consuming and high requirements of well-trained nematologists greatly reduce

435

identification efficiencies, which may result in undersampling and identification of

436

cosmopolitan nematodes. This is because undersampling can be a main factor leading to a

437

weaker biogeographic patterns (Meyer et al., 2018). Scientists also argue that globally

438

distributed nematodes may belong to different species when identified with molecular methods,

439

therefore, cosmopolitan nematodes should be named carefully. A combination of molecular and

440

morphological methods needs to be promoted to facilitate precise understanding of the spatial

441

patterning of nematodes at the continental and global scales (Geisen et al., 2018).

442

Our knowledge of the passive dispersal of soil nematodes at large scales is just the tip of

443

the iceberg. To date research has focused on the wind-mediated dispersal of nematodes (Carroll

444

and Viglierchio, 1981; Nkem et al., 2006; Ptatscheck et al., 2018), whereas other driving forces

445

such as water, birds, insects and human beings influencing dispersal of soil nematodes remains

446

unclear (Johansson et al., 1996; Finlay et al., 2002; Bullock et al., 2018). Since nematodes live

447

in water films, they are easily attached to animals. Therefore, vector-mediated dispersal should

448

be of great importance for the long-term transportation of soil nematodes, meriting future

449

research to reveal their corresponding patterns and mechanisms.

450

We still lack an understanding of the spatial patterning of nematode functional traits (e.g.,

451

adult body size, metabolic rate and biomass) in natural ecosystems or disturbed landscapes. In

452

the latitudinal gradient, many terrestrial animals show trends in line with predictions from

453

Bergmann’s (body size is large in cold climates and small in warm climates) and Allen’s rules

454

(body form is linear in warm climates and more rounded and compact in cold climates) (Diniz-

455

Filho et al., 2009; Chown and Gaston, 2010; McCollin et al., 2015; Torres-Romero et al., 2016).

456

Despite growing knowledge on the body size variation of soil nematodes in recent years

457

(Turnbull et al., 2014; George and Lindo, 2015; Liu et al., 2015; Zhao et al., 2015b), question 13

Journal Pre-proof 458

still remains as to how their body size and other functional traits (e.g., biomass and metabolic

459

rate) change with latitude. Functional approaches can result in spatial patterns that are distinctly

460

different from those based on traditional taxonomic approaches and inform us about how

461

communities are structured (Stuart-Smith et al., 2013).

462

There has been an increase in understanding of the influence of global environmental

463

changes on soil biota (Blankinship et al., 2011; García-Palacios et al., 2015), but how global

464

changes would influence spatial distribution of nematode populations, diversity (especially the

465

vulnerable species) and functional traits remains to be explored. Many climate events around

466

the world occur heterogeneously, e.g., fires occurring on visually homogenous forest are patchy

467

in temperature (Gimeno-García et al., 2004). The spatial heterogeneity of disturbance may

468

result in a range of habitats of different favorability for soil biota, for example, soil fauna

469

tolerant to fire or drought are expected to clump to patches and migrate to deeper soil layers

470

(Gongalsky et al., 2012). Evaluating how soil nematodes respond to global changes on spatial

471

hierarchy will improve our understanding of species tolerating extreme conditions and improve

472

our ability to predict species distribution under future climatic conditions.

473 474

Acknowledgments

475

This work was supported by the National Natural Science Foundation of China (No.

476

41701271, No. 41877057 and No. 41571244), and the Fundamental Research Funds for the

477

Central Universities.

478 479

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Figure captions

2

Fig. 1 Determinants of spatial heterogeneity of soil nematodes from global to micro scales.

3

Spatial heterogeneity of nematodes occurs on nested scales and it is shaped as spatial hierarchy

4

of environmental factors and intrinsic population processes. The blue color intensity indicates

5

the strength of the factor at different spatial scales. The green color intensity indicates the

6

environmental gradients.

7

Fig. 2 Phylogeny-based spatial patterns of soil nematodes in terms of the latitudinal gradient

8

and distance-decay hypotheses. (a) Nematode taxonomic diversity is decreased while

9

phylogenetic diversity is increased with increasing latitude along the Chinese coast (results

10

from Wu et al. 2016). (b) The similarity of species richness is decreased with geographic

11

distance in many organisms (Nekola and White, 1999; Soininen et al., 2007), while the

12

phylogenetic distance of the co-occurring soil nematodes is not increased along an

13

environmental gradient (results from Li et al., 2014). (c) Bacterivorous, herbivorous,

14

omnivorous and predatory nematodes tend to be phylogenetically clustered with geographic

15

distance, whereas fungivorous nematodes tend to be phylogenetically heterogeneous with

16

geographic distance (results from Li et al., 2014).

17

Fig. 3 Hypothetical dispersion patterns of nematodes at micro to fine scales. We suggest that

18

bacterivorous and fungivorous nematodes are more likely to be clumped in their distribution

19

because most of them are in low cp-class (cp 1-2) with small body size and high brood size

20

(Bongers and Ferris, 1999). These nematodes can deposit a lot of eggs in the nutrient patches

21

in a very short duration due to their rapid reproduction rate. The omnivorous and predatory

22

nematodes (cp 3-5) are large-bodied thus can move easily in the soil matrix. They also have a

23

varied diet of soil organisms and a slow reproduction rate (Bongers and Ferris, 1999), which

24

may allow them to be randomly distributed. We expect that the dispersion pattern of

25

herbivorous nematodes will be complex (either clumped, uniform or random) because of their

26

various feeding and reproduction strategies. For example, some of the herbivorous nematodes

27

deposit all their eggs at the same location, resulting in highly aggregated spatial pattern of these

28

species, whereas other herbivorous species move throughout the soil, thus their eggs been more

29

widely distributed (Rossi et al.,1996). 1

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Fig. 4 Hypothetical spatial heterogeneity of plants influenced by nematode grazing at the local

31

to field scales. (a) Nematode selective grazing on dominant plant species will cause a decrease

32

of spatial heterogeneity of plants. (b) The spatial heterogeneity of plants is expected to increase

33

following nematode grazing, if the spatial heterogeneity of nematodes is stronger than the

34

spatial heterogeneity of plants. (c) The spatial heterogeneity of plants is expected to decrease

35

following nematode grazing, if the spatial heterogeneity of plants is stronger than the spatial

36

heterogeneity of nematodes. The orange dots indicate herbivorous nematodes.

37

2

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Figure 1

39

40 41

3

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Figure 2

43

44

4

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Figure 3

46

5

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Figure 4

48

6

Journal Pre-proof Highlights 

Different drivers contribute to nematode distribution at different spatial scales



Soil properties are a key driver of nematode distribution at all spatial scales



Nematode diversity shows no consistent latitudinal trends at a global scale



Undersampling limits precise knowledge of nematode spatial patterns at large scales



DNA-based identification holds promise for resolving spatial ecology of nematodes

Journal Pre-proof Table 1 Soil properties contribute to the spatial distribution of soil nematodes at different scales. Scales Regional to global

Soil properties Bulk density Moisture Nitrogen pH Soil organic carbon

Representative references Nielsen et al. (2014) Nielsen et al. (2014) Nielsen et al. (2014) Wu et al. (2016) Chen et al. (2015); van den Hoogen et al. (2019)

Local to field

Bulk density Moisture pH

Robertson and Freckman (1995) Ettema et al. (1998) Robertson and Freckman (1995); Melakeberhan et al. (2004); Godefroid et al. (2013) Robertson and Freckman (1995); Rossi and Quénéhervé (1998) Chen et al. (2015); Kandel et al. (2018)

Texture Soil organic carbon

Micro to fine

Bulk density Moisture Nitrogen pH Texture Soil organic carbon

Ferris et al. (2006) Tong et al. (2010); Salame and Glazer (2015) Liang et al. (2005); Ou et al. (2005) Liang et al. (2005) Salame and Glazer (2015) Ferris et al. (2006); Liang et al. (2005); Ou et al. (2005); Powers et al. (1995); Biederman and Boutton (2010)