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. 2022 Jan 26;12:1428. doi: 10.1038/s41598-022-05472-9

Nematode community structure along elevation gradient in high altitude vegetation cover of Gangotri National Park (Uttarakhand), India

Priyanka Kashyap 1, Shahid Afzal 3, Anjum Nasreen Rizvi 2,✉, Wasim Ahmad 3, V P Uniyal 1, Dhriti Banerjee 2
PMCID: PMC8792017  PMID: 35082340

Abstract

The study was undertaken to understand the dynamics of soil nematode communities association along elevation gradient and associated variables in high-altitude regions of Western Himalaya. The diversity and distribution pattern of soil nematodes were investigated at four elevation ranges (Elv1, Elv2, Elv3, and Elv4 each of 500 m class) along altitudinal gradient (3000–5000 m). The nematode community comprised 58 genera of which 37 genera showed sensitivity towards altitudinal variation and the community structure also varied among elevation classes. It was found that elevation significantly affect the nematodes trophic group, diversity composition, and the nematode indices. Nematode generic richness and evenness index indicated a relatively low biodiversity of soil nematodes is supported at higher altitudes. Moreover, maturity indices reflected lower sustenance of k-strategic nematodes at higher elevations. Structure index depicted fewer connections in the soil food web at higher elevations. Nematode faunal profile showed low nutrient and low disturbance in the region. Carbon footprint of the whole nematode assemblage declined along the elevation. Overall substantial differences in the nematode composition, abundance, trophic structure, and contribution to belowground carbon cycling were observed with change in elevation. These findings could be utilized as useful tool in the long-term monitoring and to understand the region's soil health.

Subject terms: Ecology, Zoology

Introduction

Soil nematodes represent an essential component of the soil faunal community even in the cold ecosystem and can withstand extreme climatic conditions1–3. They play crucial role in important soil ecological processes and influences multiple ecosystem functions4–6, and are considered potential bio monitoring instrument for ecosystem health7,8. Identifying mechanisms for ecosystem health monitoring is very crucial in fragile ecosystems like Himalayan landscape which are under constant threat of climate change. Although in the Indian Himalayan region there are numerous studies on taxonomy, diversity, pest interaction and plant association of nematodes in agroecosystems9–12, but only a few studies focused on highlighting the relationship of soil nematodes fauna with elevation gradient in the forest ecosystem of North-Western Himalaya13,14.

In the Gangotri landscape, very few taxonomic studies on soil nematode fauna from lower elevation have been reported. However, no attempt has yet been made to study the community structure of nematodes which provide information on the ecological conditions of soils. Therefore, characterization of soil nematode community of such high-altitude wilderness can provide a glimpse of current micro-environmental conditions which may be utilized in the future climate and habitat change studies. It may also elucidate the details of the decomposition pathways therein for long-term monitoring and to understand the region's soil health.

Previous studies have highlighted the elevation pattern of nematode abundance and diversity across temperate forest ecosystems14,15, cold desert ecosystems13,16, alpine grasslands17and sub-arctic vegetations18. To the best of our knowledge, no research so far has been carried out to investigate the elevation pattern of soil nematode diversity across high altitude alpine forest ecosystems. So we tried to gain insights about the elevation pattern of soil nematodes along high altitude (3000–5000 m) alpine forest ecosystem.

Here, we specifically aim to answer the following questions.

What is the response of soil nematodes to the increasing elevation? How does the different nematode trophic groups (Bacterivores, Fungivores, Plant parasites, Predators, Omnivores) respond to elevation? Does nematode diversity, abundance and derived functional indices (MI, PPI, CI, SI and EI) which are proxies of their function change with increasing elevation?

Results

Soil abiotic characteristics and climatic variables

Soil nitrogen content, soil moisture and electric conductivity was significantly higher in the lower elevation Elv1 and lowest in highest alpine region of Elv3 and Elv4 (Fig. 1). Additionally, organic carbon was lower in high altitude alpine than lower elevation class Elv1. The pH varied from acidic to alkaline along the elevation gradient. Soil samples from Elv1 and Elv2were found to be acidic but Elv3 and Elv4 with alpine scrub soils were alkaline. There was no significant difference in phosphorous content. MAP and MAT significantly decreased towards high elevation.

Figure 1.

Figure 1

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Soil parameter across elevation. Elv—Elevation class; (A) N—Nitrogen content (%); (B) OC—soil organic carbon (%); (C) SM—soil moisture (%); (D) Soil pH; (E) EC—electric conductivity (µS cm−1) and (F) P—phosphorus content (%) across elevation classes. Different small case letters across a panel denote significant differences.

Soil nematode community across elevation

From 60 samples, 28,723 nematodes were assigned to 58 genera belonging to five trophic groups viz. bacterivores-23, fungivores-11, plant parasites-7, omnivores-7 and predators-10 (Table 1). Dissimilarity test based on the Bray–Curtis distance showed that soil inhabiting nematode community structure and taxonomic composition along elevation gradient were significantly different (PERMANOVA, p value = 0.001, Fig. 2). Only those genera were plotted that contributed the most to the Bray–Curtis measures between the elevation classes. They are not necessarily different, however to test the significance we compared nematode abundance of these genera across different elevation class with the Kruskal–Wallis test (Table 1). Out of 58 nematode genera, 37genera significantly differed (p < 0.05) among various elevation classes (Table 1). 53 genera were recorded from Elv1 (3000–3500 m), 43 from alpine range Elv2 (3501–4000 m) and 39 and 30 genera were recorded from alpine elevation range Elv3 (4001–4500 m) and Elv4 (4501–5000 m) respectively. The mean abundance of soil nematodes varied from 352.6 to 729.3per 100 g soil (Fig. 3).

Table 1.

Relative abundance of nematode genera in different elevation classes (mean ± standard error).

Genera Functional guild Elv1 Elv2 Elv3 Elv4
Bacteriovores
Acrobeles BF2 6.79 ± 1.55 5.19 ± 1.07 7.31 ± 1.37 5.22 ± 0.78
Acrobeloides BF2 1.92 ± 0.56a 5.93 ± 1.54ab 11 ± 1.75b 6.32 ± 1.2ab
Amphidelus BF2 0.00 ± 0 0.00 ± 0 0.45 ± 0.28 0.34 ± 0.17
Anaplectus BF2 0.57 ± 0.22a 0.15 ± 0.1ab 0.00 ± 0b 0.00 ± 0b
Cephalobus BF2 1.07 ± 0.49ab 4.38 ± 1.02a 0.15 ± 0.1b 0.41 ± 0.14b
Cervidellus BF2 1 ± 0.69a 1.6 ± 0.61ab 6.12 ± 1.47bc 12.29 ± 2.51c
Chiloplacus BF2 2.12 ± 0.67 4.48 ± 0.67 4.01 ± 0.93 7.34 ± 1.08
Cryptonchus BF2 0.06 ± 0.04 0.00 ± 0 0.00 ± 0 0.00 ± 0
Eucephalobus BF2 0.59 ± 0.34 0.39 ± 0.21 1.33 ± 0.41 1.65 ± 0.4
Mesorhabditis BF1 0.53 ± 0.22 0.15 ± 0.1 0.51 ± 0.24 0.00 ± 0
Monhystera BF2 0.26 ± 0.12 0.43 ± 0.21 0.24 ± 0.16 0.00 ± 0
Nothacrobeles BF2 0.55 ± 0.19 0.56 ± 0.23 0.66 ± 0.36 0.84 ± 0.57
Panagrolaimus BF1 0.37 ± 0.14ab 0.00 ± 0a 2.23 ± 0.47b 1.7 ± 0.47b
Protorhabditis BF1 0.06 ± 0.04 0.00 ± 0 0.00 ± 0 0.00 ± 0
Plectus BF2 11.75 ± 2.25a 5.73 ± 2.18b 6.043 ± 0.40ab 5.43 ± 0.52ab
Prismatolaimus BF3 11.35 ± 2.98a 3.01 ± 1.16ab 7.13 ± 2.91ab 1.96 ± 0.55b
Pseudacrobeles BF2 0.98 ± 0.22 0.27 ± 0.19 1.71 ± 0.57 1.46 ± 0.61
Rhabdolaimus BF3 0.5 ± 0.16 1.03 ± 0.51 2.85 ± 1.12 3.22 ± 0.82
Rogerus BF2 0.56 ± 0.41 0.24 ± 0.13 0.00 ± 0 0.00 ± 0
Stegelletina BF2 1.01 ± 0.45a 1.95 ± 0.42ab 3.29 ± 0.86ab 4.73 ± 0.7b
Teratocephalus BF3 2.17 ± 0.69 1.09 ± 0.54 1.59 ± 0.54 3.13 ± 0.4
Tylocephalus BF2 0.09 ± 0.07 0.00 ± 0 0.00 ± 0 0.00 ± 0
Wilsonema BF2 7.94 ± 2.1a 5.52 ± 1.15a 1.7 ± 0.56b 1.24 ± 0.45b
Fungivores
Aphelenchoides FF2 2.85 ± 0.75 3.11 ± 0.82 5.94 ± 1.37 3.73 ± 0.62
Aphelenchus FF2 0.74 ± 0.3 3.71 ± 1.2 4.31 ± 1.25 0.77 ± 0.35
Axonchium FF5 0.69 ± 0.16a 0.27 ± 0.19b 0.00 ± 0b 0.00 ± 0b
Basiria PP2 0.84 ± 0.34a 0.86 ± 0.29a 0.00 ± 0b 0.00 ± 0b
Coslenchus PP2 1.45 ± 0.7a 0.00 ± 0b 0.00 ± 0b 2.78 ± 0.86a
Ditylenchus FF2 0.00 ± 0a 0.00 ± 0ab 1.43 ± 0.61bc 2.3 ± 0.56c
Dorylaimellus FF4 1.23 ± 0.29a 1.53 ± 0.43a 0.00 ± 0b 0.00 ± 0b
Filenchus PP2 0.00 ± 0a 0.00 ± 0a 0.92 ± 0.41a 3.21 ± 0.64b
Paraphelenchus FF2 0.00 ± 0a 0.00 ± 0ab 1.8 ± 0.77b 3.13 ± 0.66c
Tylencholaimus FF4 0.66 ± 0.17a 0.62 ± 0.16ab 0.37 ± 0.25bc 0.00 ± 0c
Tylenchus FF2 2.42 ± 0.9a 2.35 ± 0.5a 0.00 ± 0b 0.00 ± 0b
Plant parasites
Helicotylenchus PP3 1.26 ± 0.56ab 2.23 ± 0.44a 0.07 ± 0.05b 3.41 ± 1.6ab
Hemicycliophora PP3 1.25 ± 0.68a 3.39 ± 0.56b 0.56 ± 0.28a 1.25 ± 0.86a
Hoplolaimus PP3 1.26 ± 0.38a 2.7 ± 0.44a 0.51 ± 0.35b 0.00 ± 0b
Merlinius PP3 0.84 ± 0.43a 0.00 ± 0b 0.00 ± 0b 0.00 ± 0b
Paratylenchus PP3 0.89 ± 0.4a 0.51 ± 0.35b 0.00 ± 0c 0.00 ± 0c
Pratylenchus PP3 0.74 ± 0.31a 0.00 ± 0b 0.00 ± 0b 0.00 ± 0b
Tylenchorhynchus PP3 1.03 ± 0.35 2.7 ± 0.59 1.39 ± 0.42 3.07 ± 0.63
Omnivores
Dorylaimoides Om4 1.48 ± 0.46a 5.57 ± 0.75b 0.24 ± 0.17c 0.00 ± 0c
Dorylaimus Om4 1.82 ± 0.29a 0.23 ± 0.23b 0.00 ± 0b 0.00 ± 0b
Eudorylaimus Om4 5.64 ± 0.93 6.75 ± 1.19 5.06 ± 0.83 5.57 ± 0.92
Mesodorylaimus Om4 0.00 ± 0a 0.00 ± 0a 3.71 ± 1.39b 0.00 ± 0a
Moshajia Om4 2.3 ± 0.46a 3.23 ± 0.47a 0.57 ± 0.26b 0.00 ± 0b
Oriverutus Om4 0.38 ± 0.17a 0.00 ± 0b 0.00 ± 0b 0.00 ± 0b
Thornenema Om5 1.16 ± 0.24a 1.31 ± 0.28ab 0.57 ± 0.26bc 0.00 ± 0c
Predators
Actinolaimus Pr5 1.76 ± 0.23a 1.13 ± 0.32b 0.74 ± 0.36bc 0.00 ± 0c
Aporcelaimellus Pr5 4.87 ± 0.41a 4.45 ± 0.47ab 3.7 ± 0.59ab 1.52 ± 0.62b
Campydora Pr4 0.28 ± 0.12a 0.00 ± 0b 0.00 ± 0b 0.00 ± 0b
Clarkus Pr4 0.57 ± 0.22a 0.19 ± 0.19b 0.00 ± 0b 0.00 ± 0b
Coomansus Pr4 0.14 ± 0.08 0.85 ± 0.54 1.39 ± 0.31 0.68 ± 0.36
Discolaimus Pr5 3.06 ± 0.6a 3.04 ± 1.26b 1.22 ± 0.83c 0.00 ± 0c
Discolaimoides Pr5 1.21 ± 0.38 1.76 ± 0.4 5.42 ± 0.97 5.06 ± 0.86
Mylonchulus Pr4 0.17 ± 0.12 0.00 ± 0 0.00 ± 0 0.00 ± 0
Prionchulus Pr4 0.21 ± 0.12a 0.24 ± 0.13a 1.62 ± 0.53a 6.24 ± 1.2b
Tripyla Pr3 0.65 ± 0.27a 0.6 ± 0.15a 0.00 ± 0b 0.00 ± 0b
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Means (%) followed by different superscript letters are significantly different by the post hoc-test (p < 0.05). Means followed by different superscript letters reflects significant differences. Bf: bacterial feeders, Ff: fungal feeders Hr: herbivores, Om: omnivores, Pr: predators and subscript 1–5 represent C–P scale.

Figure 2.

Figure 2

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Bray–Curtis dissimilarity (NMDS ordination) of nematode communities based on abundances of nematode genera. Each point displays the community found in an individual sample (n = 15 samples per elevation class × 4 classes = 60). Points that are close proximity have more similar communities than points that are distant from each other. Colors show Elevation class (Where Elv1: 3000–3500 m; Elv2: 3501–4000 m; Elv3: 4001–4500 m; Elv4: 4501–5000 m). Names of nematode genera are overlaid.

Figure 3.

Figure 3

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Nematode Abundance of various feeding (trophic) groups across elevation. (A) BF (Bacterial Feeders); (B) FF (Fungal Feeders); (C) He (Herbivores); (D) Om (Omnivores); (E) Pr (Predators); (F) Nem (Total Nematode Abundance). Different small case letters across a panel denote significant differences.

There were differences in soil nematode composition among various elevation classes with a significant difference (p < 0.05) in the relative abundance of bacterivores (Acrobeloides, Anaplectus, Cephalobus, Cervidellus, Stegelletina, Wilsonema, Prismatolaimus, Plectus and Panagrolaimus); omnivores (Dorylaimoides, Dorylaimus, Mesodorylaimus, Moshajia and Thornenema) and predators (Actinolaimus, Aporcelaimellus, Campydora, Clarkus, Discolaimus, Prionchulus and Tripyla) some Plant parasites and fungivores (Table 1.). Bacterivores (Anaplectus, Rogerus); fungivores (Dorylaimellus, Axonchium, and predator (Tripyla) were absent in the alpine scrub region of higher elevational range whereas Protorhabditis, Campydora, Mylonchulus and Oriverutus were only present in lower elevation class (Elv1).

Trophic group and c–p group association across elevation

Trophic groups differed significantly among various elevation classes (p < 0.05) except fungivores (Fig. 3). Bacterivores was the most diverse and abundant trophic group across elevation classes, whereas, fungivores were least abundant in highest elevation classes Elv4 (51.73 ± 5.41). Plant parasites were least abundant in Elv3 (10.07 ± 3.11) and were observed in larger numbers in lower elevation classes with subalpine vegetation. Abundance of bacterivores, plant parasites, omnivores and predators were significantly higher in Elv1 among various elevation classes. Nematodes found were also classified into five c–p groups (1–5) according to their colonizer-persister life strategy (Fig. 4). Throughout the elevation classes we found CP 2 nematodes contributing major proportion. However, we found an increasing trend of CP 2 with increasing elevation class and decreasing pattern of CP 5 with increasing elevation class (Fig. 4).

Figure 4.

Figure 4

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Relative abundance (%) of nematode C–P groups at four different elevation classes.

Nematode community indices across elevation

Maturity indices, significantly varied with elevation with higher values found at Elv1 lower than those found at Elv4 (Table 2). PPI remained unaffected by change in elevation. EI values was significantly higher at elevation Elv3 and Elv4 as compared to Elv1 and Elv2, on the other hand opposite trend was found for SI. CI of soil nematodes were different but not statistically significant among elevation classes. The mean Shannon index (H’) varied among elevation classes with highest value in Elv2 and lowest in Elv3, but the difference was not significant. Evenness index (J′) significantly differed. Nematode Generic Richness (GR) of the overall nematode community was higher at Elv1followed by Elv2, Elv3, Elv4 along the gradient and differences were statistically significant (p < 0.05). Nematode faunal profile based on EI-SI, an indicator of ecosystem functioning, for all the elevation classes falls under quadrant C i.e. low nutrient and low disturbance except some of the points of Elv 4 falls under quadrant D (low nutrient and high disturbance) and Elv2 in quadrant 2 (High nutrient, low disturbance) (Fig. 5). Nematode composite structure and various trophic metabolic footprints (Ba, Pp, Pr and Om) significantly varied with elevation, with higher values found at lower elevations (Table 3). Whereas, enrichment and fungivore metabolic footprint remained unaffected by elevation (Table 3).

Table 2.

Soil nematode community indices across elevation classes.

Elv1 Elv2 Elv3 Elv4
MI 2.9 5 ± 0.38a 2.97 ± 0.45a 2.66 ± 0.26b 2.51 ± 0.16b
ΣMI 2.91 ± 0.32a 2.92 ± 0.35a 2.67 ± 0.25b 2.55 ± 0.15b
MI25 2.97 ± 0.37a 2.97 ± 0.47a 2.71 ± 0.23a 2.53 ± 0.17b
PPI 2.61 ± 0.32 2.82 ± 0.11 3.08 ± 0.02 3.07 ± 0.08
EI 18.37 ± 13.56b 15.22 ± 10.71b 28.88 ± 12.03a 26.37 ± 7.54a
SI 77.16 ± 12.11a 75.77 ± 11.25a 68.74 ± 9.92b 59.85 ± 10.21b
CI 64.87 ± 16.72 92.36 ± 17.82 61.27 ± 23.22 73.44 ± 29.62
H′ 2.78 ± 0.11 2.84 ± 0.06 2.66 ± 0.07 2.71 ± 0.04
λ 0.9 ± 0.01 0.92 ± 0.01 0.91 ± 0.01 0.92 ± 0.01
J′ 0.93 ± 0.01a 0.91 ± 0.01b 0.9 ± 0.02ab 0.91 ± 0.01b
Generic richness 27.8 ± 2.59a 23.13 ± 0.9ab 19.8 ± 0.91ab 19.47 ± 0.7b
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Means followed by different superscript letters reflects significant differences by the post hoc-test (p < 0.05).

Figure 5.

Figure 5

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Food web diagnostic across Elevation classes. Elv1: 3000–3500 m; Elv2: 3501–4000 m; Elv3: 4001–4500 m; Elv4: 4501–5000 m.

Table 3.

Soil nematode metabolic footprints across elevation classes.

Elv1 Elv2 Elv3 Elv4
Composite footprint 509.63 ± 391.34a 222.24 ± 11.56b 176.13 ± 143.62b 113.24 ± 31.60b
Enrichment footprint 8.12 ± 8.45a 6.57 ± 7.43a 11.86 ± 6.52a 9.12 ± 3.14a
Structure footprint 439.95 ± 384.64a 175.3 ± 122.26b 138.5 ± 142.11b 74.73 ± 27.21b
Plant parasite footprint 16.11 ± 21.03a 14.83 ± 8.67a 2.01 ± 3.23b 4.03 ± 4.95b
Fungivore footprint 18.86 ± 15.68a 13.44 ± 9.18a 20.74 ± 6.32a 17.04 ± 7.19a
Bacterivore footprint 81.3 ± 32.71a 32.71 ± 14.57b 41.34 ± 14.83b 33.51 ± 16.88b
Predator footprint 272.96 ± 291.2a 128.83 ± 104.19b 91.5 ± 120.98b 45.07 ± 23.67c
Omnivore footprint 121.41 ± 68.32a 32.44 ± 29.61b 20.54 ± 14.32b 13.59 ± 8.06b
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Means followed by different superscript letters reflects significant differences by the post hoc-test (p < 0.05).

Association of soil nematode assemblages with Soil physicochemical parameters across elevation

The nematode communities were determined mainly by pH, nitrogen, soil moisture, soil organic carbon contents, and electric conductivity which are mostly related to elevation and vegetation. Soil properties significantly correlated with nematode trophic groups (Fig. 6). Electric conductivity showed significant correlation with fungal feeders. However, various trophic groups showed neutral response with phosphorus content. Abundance of bacterivores showed positive correlation with soil moisture, soil organic carbon and nitrogen content but negatively correlated with soil pH. Omnivores and predators showed positive responses to organic carbon and soil moisture content (Fig. 6). The principal component analysis explains 36.0% of these variations. The first axis explains 25.5% and the second axis explains 10.5% (Fig. 7). The study showed that plots with higher nitrogen, soil moisture and organic carbon are associated with higher faunal diversity of bacterial feeders and genera such as Anaplectus, Plectus, Teratocephalus, Mesorhabditis, and Wilsonema. The analysis also highlighted that majority of genera showed a negative relation with pH and elevation. However some genera such as Cervidellus, Chiloplacus, Filenchus, Prionchulus, Discolaimoides and Paraphelenchus showed positive correlation with elevation pH and elevation.

Figure 6.

Figure 6

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Association of Nematode trophic groups with soil physicochemical parameters. Correlation coefficients (p < 0.05) of trophic groups and soil physicochemical parameters. (PH: Soil pH; EC: Electrical Conductivity (µS cm−1); OC: Organic Carbon; N: Nitrogen content; P: Phosphorous content; SM: Soil moisture; BF: Bacterivores; FF: Fungivores; Hr: Herbivores; Om—Omnivores; Pr—Predators; Nem—Total Nematode Abundance).

Figure 7.

Figure 7

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Principal Component Analysis (PCA) of soil Nematode genera trophic groups and soil attributes along elevation. Soil variables elevation trophic group and nematode genera are marked by arrows. Percentage of variance explained was 23.5% and 10.7% for Dim 1 and Dim 2 respectively.

Discussion

Elevation classes signify the variations in plant species assemblages19 as a factor of climate, habitat and other environmental variations in nature20. In current study, it was observed that soil inhabiting nematode diversity and abundance decreased along the elevation gradient in high altitude region of Gangotri National Park, which is in consistent with findings of previous studies14,16,21. It may be due to harsh climatic condition at the higher elevation causing shift in soil abiotic and biotic status which ultimately led to decline in nematode abundance at higher elevation class. In disparity to this, at mid elevation maximum soil nematode diversity pattern have been documented from cold desert13. However, some previous studies on soil nematodes along elevation gradient did not find any distinct pattern3,22. Moreover, the current investigation showed evidences of significant association of soil nematode trophic group composition and structure with elevation classes in the western Himalayan landscape. It was also observed that among all trophic groups, bacterivores were dominating at all elevation classes although with significant differences at different altitudes. Abundance of plant parasites, omnivores and predators significantly declined along elevation gradient which is in accordance with the previous study in subarctic vegetation18. Interestingly previous studies resonate these outcomes specifically in forest areas23,24.

The elevation association of nematodes were in agreement with similar studies in the Beskydy Mountains spruce forests, and Changbai Mountain China25–27. Yet another study in forest ecosystem linked higher diversity and generic richness at lower elevation forest vegetation soils with its resilient and sustainable ecosystem28. So it may be anticipated that the soil ecosystem in lower elevations may be more suitable for sustaining ecosystem balance and soil biota thus resulting in higher generic diversity. Our results depicted that nematode composition in highest elevation class Elv4 is close to Elv3 showing similar nematode composition. It may be concluded that altitude is a significant factor for soil nematode diversity at every elevation class having different local environment and physicochemical properties which affect soil biota specifically, soil nematodes present at various trophic levels in the soil food web.

Diversity of soil nematodes were not solely dependent on altitude but rather on an interactive network of biotic and abiotic compositions of its immediate environment which shifts along the elevation gradient. Ecology of soil nematodes communities are significantly affected by variations in biotic and abiotic factors, external stressors altering the habitat conditions in both forest and agroecosystems29–33. External stressors as grazing, forest fire, nutrient supplement (as nitrates phosphates) and alterations in plant types affects the abundance and community composition of the taxa34–38. Moreover, soil parameters are also strongly associated with altitude, vegetation, climate and habitat parameters39–41. However, reflecting the current results, several studies stated that elevationis vital aspects for determining nematode community composition21,42and the aboveground floral composition varies with elevation which is propounded to affect soil inhabiting nematodes by altering abiotic factors43–46. In the present study, soil pH levels were found to affect the tropic structure in the study area. Abundance of Plant parasites, omnivores and predatory nematodes were inclined towards more acidic to neutral soils analogous to findings of Keith et al.47Apart from pH, soil nematodes were also driven by nitrogen, soil moisture, soil organic carbon contents and electric conductivity which are seldom related to elevation changes along the gradient. Total nematode abundance and bacterivores were significantly associated with nitrogen, soil organic carbon and soil moisture in the current findings. This result was alike numerous studies where bacterivores were higher in nitrogen-rich soil48–50.

The maturity indices of soil nematode communities vary from low to high from disturbed to undisturbed soil ecosystems51. The present study showed comparatively high disturbance among the highest elevation class with alpine scrubs than the lower elevation class with sub-alpine forest based on maturity indices. EI and SI provided information on soil food web dynamics and energy flow in the system52,53 of the present study. It was found that lower elevation range are comparatively nutrient richer than alpine region along elevation which may be due to the adverse conditions at higher elevation directly and indirectly affecting the abiotic and biotic condition and restricted resource entry in the region. Also structural index values differed among ranges which basically indicates higher tropic group nematodes metabolic activity which has crucial function in soil food web52,54. Omnivorous and predatory nematodes are known to have a long-life cycle and therefore are highly sensitive to disturbances51. But any change in the system affects high trophic level nematodes viz. the predators and this affects the above and belowground stoichiometry55. This sensitivity of high trophic soil inhabiting nematodes provides the potential to be used as tool in long-term monitoring and climate change studies to understand the changing soil ecosystem.

Results showed EI-SI for all elevation classes falls under quadrant D i.e. low nutrient and low disturbance except some of the samples from Elv4 fall in quadrant C indicating low nutrient with higher disturbance which is also confirmed by nematode maturity indices. Previous works stated that high SI value of forest soil is owing to high trophic level linkage and high abundance of higher trophic group viz omnivores and predators in soil biota56,57. Similar results on EI–SI are known from alpine meadows of the Tatra National Park Slovak Republic58. Composition of various nematode species is responsible for maintaining a structured soil food web59. Whereas, the mean values of CI in the present study vary (61.27–92.27) among elevation classes indicating variations in dominant groups (bacterial/fungal) of decomposition pathway. Carbon footprint of soil nematodes is lowest at elevations alpine dry scrub. Similar results of carbon assimilation are also reported from temperate vegetation cover along elevation gradient of Pir-Panjal range in Western Himalayas14.

Differential nutrient levels among elevation classes and changes in the associated trophic groups of nematodes were evident in the study area. Also nematode diversity and generic richness were relatively higher at a low elevation class of sub-alpine forest and lowest at high elevation alpine dry scrub. Thus nematode diversity and abundance are inversely correlated with elevation. It is known that lower nutrient levels slow down the microbial growth thus directly decelerates the decomposition48,50,52,60–64. However, decomposition rates are not regulated by a single parameter rather a combination of temperature, substrate quality, nutrient levels and anaerobic conditions like oxygen and moisture62,63 which are mostly associated with altitude and habitat conditions. Among various elevation classes of Gangotri National Park, there are substantial differences in taxonomic composition, energy flow channels and nematode community structure which provide basis to understand the role of soil nematodes in key soil ecological processes in the region.

Conclusion

The current study presented commendable association among high altitudes soil inhabiting nematode communities of GNP western Himalaya with elevation, soil physicochemical characteristics and soil nutrient levels. Our study showed high nematode richness and abundance in lower altitudinal ranges than the higher ranges. The strong relationship of soil nematode composition and trophic groups with food web dynamics and metabolic footprint can be used in ecological monitoring of the high-altitude ecosystem of western Himalaya. However, before suggesting potential bio indicators, it is essential to establish the ecology of Himalayan soil inhabiting nematode through further extensive systematic studies across the landscape. However, it can be useful in assessing preliminary ecosystem health of forest in the region.

Material and methods

Study area

The current study is based on samples collected from the wide altitudinal (3000–5000 m) gradients of Gangotri National Park (GNP) of Uttarakhand in the Western Himalaya. Gangotri National Park lies between 30° 50′ N, 78° 45′ E and 31° 12′ N, 79° 02′ E in the upper catchment of the River Bhagirathi in the Uttarkashi district (Uttarakhand). It covers an area of 2390 km2 and a wide altitudinal gradient of 1200–6000 m.

The high-altitude regions of GNP comprise of two major valleys: Gangotri and Nelang Valleys. Gangotri Valley gives rise to River Bhagirathi and Nelang Valley gives rise to one of its largest tributaries River Jadhganga which confluences at Bhairongathi in the Uttarkashi district. The highest elevations covered with ice and bare rocks alpine steppes at altitudes > 3800 m and relatively drier upper region > 3700 m of Gangotri Valley forms a transition zone between moist and arid regions in addition to a stunted tree line between 3700–3800 m. Vegetation of the sub-alpine region is dominated by Himalayan Birch (Betula utilis) and sub-alpine Mixed conifer forests of West Himalayan Fir (Abies pindrow), Deodar (Cedrus deodara) and Blue Pine (Pinus wallichiana) classified by Champion and Seth65. Deodar primarily dominates the natural vegetation at lower elevations; Blue Pine and Himalayan Birch from mid elevations to tree-line; and alpine scrubs at moist and dry region of the transition zones (Artemisia sp, Juniperus). However Alpine Dry Scrubs (Caragana sp., Eurotia sp., Rhamnus sp., Artemisia sp. and Lonicera sp.) dominates the cold desert regions of Nelang (4000–5000 m) characterized by rocky terrains, dry soil, very low temperature and scarce rainfall with scanty and specialized vegetation.

Sampling protocol

Random samplings were conducted along a stratified altitudinal gradient in the study area. Altogether 60 soil samples along elevation gradient (3000–5000 m) were collected in October 2018. Elevation was categorized equally in 500 m class (4 classes) along the altitudinal gradient (Elv1: 3000–3500 m; Elv2: 3501–4000 m; Elv3: 4001–4500 m; Elv4: 4501–5000 m). Three samples per site and a total of 15 samples from each class were collected (3 samples × 5 sites × 4 elevation classes). Five soil cores were taken which constituted one composite sample of 500 gm. At each sampling site beneath the host plant leaf litter (if present) and upper layer of soil were removed. Soil samples were collected at a depth of 0 to 15 cm using a soil auger with a diameter of 3 cm. These samples were then packed in an airtight polythene bag and transferred to the laboratory for further analysis.

Soil physiochemical parameters and climatic variables

Soil physiochemical parameters viz. Soil pH, Electrical Conductivity (µS cm−1), Organic Carbon, N content, NaHCO3 extractable P and soil moisture were estimated using standard methods using 350 gm soil sample. Soil pH was determined using a pH meter with glass electrodes according to Singh et al.66, Electrical Conductivity (µS cm−1) was assessed following Jackson method67, whereas, soil organic carbon was estimated by Walkley and Black68 method. Total N content was estimated by alkaline potassium permanganate according to Kjeldahl69, and NaHCO3 extractable P (1954) was estimated using spectrophotometer following Olsen et al.70. Lastly, soil moisture content was estimated using standard gravimetric method (replicates were weighed and oven-dried for a day until thoroughly dried and then reweighed again). Temperature and precipitation (mean annual) variables were extracted at a spatial resolution of 30 arc-seconds from WorldClim version 2.1 climate data71.

Nematode extraction and identification

The nematodes were extracted from 100 gm soil samples following Cobb’s sieving and decantation72 and modified Baermann’s funnel techniques. The extracted nematodes were fixed in hot triethanolamine-glycerol fixative. Post fixation individual soil nematodes samples placed in petridish were counted under a dissecting microscope. Nematode abundance was expressed as the total number of nematodes per 100 gm of soil sample. To compute the composition of the soil inhabiting nematode community, at least 100 individuals of soil nematodes in each sample were randomly selected after counting21. If the total number of nematodes in a sample was less than 100, then all the nematodes were identified upto generic level under microscope (Olympus BX51 DIC Microscope) and were assigned to respective trophic groups73. However, the members of the family Tylenchidae owing to their delicate stylet were assigned to fungal feeders according to several authors14,74. Nematode genera were also allotted to colonizer–persister (cp) groups75.

Data analysis

Maturity indices were calculated based on a c–p scale assigned to different genera of nematode communities ranging from r-strategist colonizers to K-strategist persisters (cp1–cp5). Maturity Index (MI) and Plant Parasite Index (PPI) were calculated following Bongers74. MI-free-living nematodes with cp1-5 excluding plant parasitic nematodes75,76, MI25-free living nematodes with cp2-5 excluding nematode with cp1 and plant parasitic nematode; ΣMI25-free-living nematodes and plant parasitic nematodes including nematode with cp-177,78. Enrichment index (EI) = (e/e + b) × 100, Structure index (SI) = (s/s + b) × 100 and Channel Index (CI) = (0.8Fu2/{3.2Ba1 + 0.8Fu2} ×  100) were calculated to provide information on soil food web dynamics and stability53. Structure Index is an excellent means to understand whether a system is mature or structured where high value represents structured and low value represents a disturbed ecosystem. Channel index provides data on contribution of bacterial and fungal feeders in the decomposition pathway. The b component is calculated as Σkbnb where kb is the weighting assigned to guilds indicating basal characteristics of the soil food web (0.8[Ba2 + Fu2]) and nb is the nematode abundance in the guilds. Similarly, enrichment and structure components were calculated using guilds indicating enrichment ([3.2Ba1] + [0.8Fu2]) and structure (Ba3–Ba5, Fu3–Fu5, Ca2–Ca5) respectively52, where Ba1-5 represent bacterivores of C–P group 1–5, Fu2-5 represent fungivores of C–P group 2–5 and Ca2-5 represent predators of C–P group 1–5 All the nematode functional indices were calculated using the online program NINJA79.

Shannon–Wiener diversity index (H'); evennessindex (J′); and Genera richness (GR) were used for quantification of diversity. The metabolic footprint (carbon assimilation) which are proxies of magnitude of ecosystem services and functions provided by nematodes to the soil food web were calculated with the help of equations provided by Andrassy80: W = (D2 × L)/(1.6 × 106) and Ferris81:F = Σ(Nt (0.1(Wt/mt) + 0.273 (Wt0.75)) using the NINJA online program77.

As our data was not normal even after transformation therefore, Kruskal–Wallis Analysis of Variance (ANOVA) was used to detect significant differences in nematode abundance, diversity, nematode specific indices and soil properties among different elevational classes. Multiple comparisons among elevational classes were performed by using the Dunn test. Spearman's rank correlation coefficient and its significance at p < 0.05 level among various soil physicochemical parameters, climatic variables and nematode trophic groups were calculated. To establish a relation between physicochemical properties of soil, climatic variables, trophic groups and nematode genera Principal component analysis (PCA) was used. Non-Metric Multidimensional Scaling (NMDS) was performed to investigate the position of soil nematode community in ordination space along elevation gradient. Permutational Multivariate Analysis of Variance (PERMANOVA) was used to test if nematode composition differs along elevation gradients using ‘adonis’ and ‘betadisper’ functions of vegan package (R 3.6)82. Pairwise multi-level comparisons were conducted with dissimilarity matrix using ‘pairwise.adonis’ function to assess differences between elevations. All analyses were performed in R (version 3.6) statistical platform (R core team)83. Figures 1, 3 and 4 were prepared with the help of software GraphPad Prism8.0.2584.

Acknowledgements

The authors express their sincere gratitude to Dr. V.B. Mathur former Director Wildlife Institute of India WII and Dr. G.S. Rawat former Dean WII; Dr. S. Sathyakumar Nodal Scientist DST-NMSHE and team; and Dr. Kailash Chandra, Former Director Zoological Survey of India Kolkata, for their guidance and support. We are thankful to the Uttarakhand Forest Department for granting the research permission, necessary support and cooperation. We would also like to thank project assistant Gunjan Gulati and field assistants Neeraj, Naresh, Akhil, Uttam and Anil who assisted us in field work. The authors are grateful to the National Mission on Himalayan Studies NMHS Ministry of Environment Forests and Climate Change Government of India; and Department of Science and Technology DST Government of India DST Grant No.: DST/SPLICE/CCP/NMSHE/TF-2/WII/2014[G] dated 26.08.2014 for providing funding support.

Abbreviations

MI

Maturity Index

CI

Channel Index

EI

Enrichment Index

SI

Structure Index

Author contributions

P.K.: conducted survey, Manuscript drafting, Data Analysis, Taxonomy; S.A. contributed in writing, editing and designing figures of the manuscript; A.N.R.: contributed in research design, editing of manuscript, Taxonomy; W.A., V.P.U. and D.B.: contributed to writing and editing the manuscript.

Funding

National Mission on Himalayan Studies NMHS Ministry of Environment Forests and Climate Change Government of India; and Department of Science and Technology DST Government of India DST grant no.: DST/SPLICE/CCP/ NMSHE/TF-2/WII/2014[G] dated 26.08.2014 for providing funding support.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Hoschitz M, Kaufmann R. Nematode community composition in five alpine habitats. Nematology. 2004;6:737–747. [Google Scholar]
  • 2.Treonis AM, Wall DH. Soil nematodes and desiccation survival in the extreme arid environment of the Antarctic dry valleys. Integr. Comp. Biol. 2005;45:741–750. doi: 10.1093/icb/45.5.741. [DOI] [PubMed] [Google Scholar]
  • 3.Tong FC, Xiao Y, Wang QL. Soil Nematode community structure on the northern slope of Changbai Mountain Northeast China. J. For. Res. 2010;21:93–98. [Google Scholar]
  • 4.Yeates GW. Nematodes as soil indicators functional and biodiversity aspects. Biol. Fertil. Soils. 2003;37:199–210. [Google Scholar]
  • 5.Bakonyi G, Nagy P, Kovács-Láng E, Kovács E, Barabás S, Répási V, Seres A. Soil Nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Appl. Soil. Ecol. 2007;37(1–2):31–40. [Google Scholar]
  • 6.Van Eekeren N, De Boer H, Hanegraaf M, Bokhorst J, Nierop D, Bloem J, Schouten T, De Goede R, Brussaard L. Ecosystem services in grassland associated with biotic and abiotic soil parameters. Soil Biol. Biochem. 2010;42(9):1491–1504. [Google Scholar]
  • 7.Kitagami Y, Kanzaki N, Matsuda Y. Distribution and community structure of soil nematodes in coastal Japanese pine forests were shaped by harsh environmental conditions. Appl. Soil. Ecol. 2017;119:91–98. [Google Scholar]
  • 8.Salamun P, Hanzelova V, Miklisova D, Sestinova O, Findorakova L, Kovacik P. The effects of vegetation cover on soil Nematode communities in various biotopes disturbed by industrial emissions. Sci. Total Environ. 2017;592:106–114. doi: 10.1016/j.scitotenv.2017.02.238. [DOI] [PubMed] [Google Scholar]
  • 9.Kashyap P, Bhardwaj M, Uniyal VP. Bibliography on the soil Nematodes of the Indian Himalayan Region. In: Sathyakumar S, editor. Bibliography on the Fauna and Micro Flora of the Indian Himalayan Region. ENVIS Bulletin: Wildlife and Protected Areas. Wildlife Institute of India; 2016. pp. 239–256. [Google Scholar]
  • 10.Kumar S, Rawat S. First report on the root-knot Nematode Meloidogyneenterolobii (Yang and Eisenback 1988) infecting guava (Psidiumguajava) in Udham Singh Nagar of Uttarakhand India. Int. J. Curr. Microbiol. Appl. Sci. 2018;7(4):1720–1724. [Google Scholar]
  • 11.Kayani MZ, Mukhtar T, Hussain MA. Interaction between Nematode inoculum density and plant age on growth and yield of cucumber and reproduction of Meloidogyne incognita. Pak. J. Zool. 2018;50(3):897–902. [Google Scholar]
  • 12.Rizvi AN, Sen D, Maity P, Kumar H. Nematoda (soil inhabiting Nematodes) In: Chandra K, Gupta D, Gopi KC, Tripathy B, Kumar V, editors. Faunal Diversity of Indian Himalaya. Director Zool Surv India; 2018. pp. 115–134. [Google Scholar]
  • 13.Devetter M, Hanel L, Rehakova K, Anddolezal J. Diversity and feeding strategies of soil microfauna along elevation gradients in Himalayan cold deserts. PLoS ONE. 2017;12(11):e0187646. doi: 10.1371/journal.pone.0187646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Afzal S, Nesar H, Imran Z, Ahmad W. Altitudinal gradient affect abundance, diversity and metabolicfootprint of soil nematodesin Banihal-Pass of Pir-Panjalmountain range. Sci. Rep. 2021;11:16214. doi: 10.1038/s41598-021-95651-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Dong K, et al. Soil nematodes show a mid-elevation diversity maximum and elevational zonation on Mt. Norikura, Japan. Sci. Rep. 2017;7:3028. doi: 10.1038/s41598-017-03655-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Powers LE, Ho MC, Freckman DW, Virginia RA. Distribution, community structure and microhabitats of soil invertebrates along an elevational gradient in Taylor Valley Antarctica. Arct. Alp. Res. 1998;30:133–141. [Google Scholar]
  • 17.Kergunteuil A, Campos-Herrera R, Sánchez-Moreno S, Vittoz P, Rasmann ST. Abundance, diversity, and metabolic footprint of soil nematodes is highest in high elevation alpine grasslands. Front. Ecol. Evol. 2016;4:84. [Google Scholar]
  • 18.Veen GF, et al. Coordinated responses of soil communities to elevation in three subarctic vegetation types. Oikos. 2017;126:1586–1599. [Google Scholar]
  • 19.Burrows CJ. Processes of Vegetation Change. Unwin Hyman; 1990. p. 1. [Google Scholar]
  • 20.De Kort H, Prunier JG, Ducatez S, Honnay O, Baguette M, Stevens VM, Blanchet S. Life history, climate and biogeography interactively affect worldwide genetic diversity of plant and animal populations. Nat. Commun. 2021;12:516. doi: 10.1038/s41467-021-20958-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Liu J, Yang Q, Siemann E, Huang W, Ding J. Latitudinal and altitudinal patterns of soil nematode communities under tallow tree (Triadicasebifera) in China. Plant Ecol. 2019;220:965–976. [Google Scholar]
  • 22.Qing X, Bert W, Steel H, Quisado J, de Ley IT. Soil and litter nematode diversity of Mount Hamiguitan, the Philippines, with description of Bicirronemahamiguitanense n. sp (Rhabditida: Bicirronematidae) Nematology. 2015;17:325–344. [Google Scholar]
  • 23.Wasilewska L. Soil invertebrates as bioindicators with special reference to soil inhabiting nematodes. Russ. J. Nematol. 1997;5:113–126. [Google Scholar]
  • 24.Mladenov A, Lazarova S, Peneva V. Distribution patterns of Nematode communities in an urban forest in Sofia Bulgaria. In: Peneva L, Niemelä J, Kotze DJ, Chipev N, editors. Ecology of the City of Sofia. Species and Communities in an Urban Environment. Sofia Bulgaria Pen-soft Publishers; 2004. pp. 281–297. [Google Scholar]
  • 25.Hánel L. Comparison of soil Nematode communities in three spruce forests at the Bobín Mount Czech Republic. Biológia. 1996;51:485–493. [Google Scholar]
  • 26.Hanel L. Soil Nematodes in five spruce forests of the Beskydymountains Czech Republic. Fundam. Appl. Nematol. 1996;19(1):15–24. [Google Scholar]
  • 27.Zhang S, Chen D, Sun D, Wang X, Smith JL, Du G. Impacts of altitude and position on the rates of soil nitrogen mineralization and nitrification in alpine meadows on the eastern Qinghai-Tibetan Plateau China. Biol. Fertil. Soils. 2012;48(4):393–400. [Google Scholar]
  • 28.Yeates GW. Abundance diversityand resilience of Nematode assemblage in forest soils. Can. J. For. Res. 2007;37:216–225. [Google Scholar]
  • 29.Mulder C, Zwart DD, Van Wijnen HJ, Schouten AJ, Andbreure AM. Observational and simulated evidence of ecological shifts within the soil Nematode community of agroecosystems under conventional and organic farming. Funct. Ecol. 2003;17(4):516–525. [Google Scholar]
  • 30.Butenko KO, Gongalsky KB, Korobushkin DI, Ekschmitt K, Zaitsev AS. Forest fires alter the trophic structure of soil nematode communities. Soil Biol. Biochem. 2017;109:107–117. [Google Scholar]
  • 31.Tibbett M, Gil-Martínez M, Fraser T, Green ID, Duddigan S, De Oliveira VH, Raulund-Rasmussen K, Sizmur T, Diaz A. Long-term acidification of pH neutral grasslands affects soil biodiversity fertility and function in a heathland restoration. CATENA. 2019;180:401–415. [Google Scholar]
  • 32.Zhang S, Cui S, Mclaughlin NB, Liu P, Hu N, Liang W, Wu D, Liang A. Tillage effects outweigh seasonal effects on soil Nematode community structure. Soil Tillage Res. 2019;192:233–239. [Google Scholar]
  • 33.Liang S, Kou X, Li Y, Lü X, Wang J, Li Q. Soil Nematode community composition and stability under different nitrogen additions in a semiarid grassland. Glob. Ecol. Conserv. 2020;22:e00965n. [Google Scholar]
  • 34.Olatunji OA, Gong S, Tariq A, Pan K, Sun X, Chen W, Zhang L, Dakhil MA, Huang D, Tan X. The effect of phosphorus addition, soil moisture, and plant type on soil nematode abundance and community composition. J. Soil. Sediment. 2019;19:1139–1150. [Google Scholar]
  • 35.Wang J, Li M, Zhang X, Liu X, Li L, Shi X, Hu H, Pan G. Changes in soil nematode abundance and composition under elevated [CO2] and canopy warming in a rice paddy field. Plant Soil. 2019;445(1):425–437. [Google Scholar]
  • 36.Zhang ZW, Li Q, Zhang HY, Hu YY, Hou SL, Wei HW, Yin JX, Lu XT. The impacts of nutrient addition and livestock exclosure on the soil Nematode community in degraded grassland. Land Degrad. Dev. 2019;30(13):1574–1583. [Google Scholar]
  • 37.Bastow J. The impacts of a wildfire in a semiarid grassland on soil Nematode abundances over 4 years. Biol. Fertil. Soils. 2020;56:675–685. [Google Scholar]
  • 38.Renčo M, Gomoryova E, Cerevková A. The effect of soil type and ecosystems on the soil nematode and microbial communities. Helminthologia. 2020;57(2):129. doi: 10.2478/helm-2020-0014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Saeed S, Barozai MYK, Ahmad A, Shah SH. Impact of altitude on soil physical and chemical properties in SraGhurgai (Takatu mountain range) Quetta Balochistan. Int. J. Sci. Eng. Res. 2014;5(3):730–735. [Google Scholar]
  • 40.Zhang XY, Li QW, Gao JQ, Hu YH, Song MH, Yue Y. Effects of rainfall amount and frequency on soil nitrogen mineralization in Zoigê alpine wetland. Eur. J. Soil Biol. 2020;97:103170. [Google Scholar]
  • 41.Juan Y, Tian L, Sun W, Qiu W, Curtin D, Gong L, Liu Y. Simulation of soil freezing-thawing cycles under typical winter conditions: Implications for nitrogen mineralization. J. Soils Sediments. 2020;20(1):143–152. [Google Scholar]
  • 42.Cutz-Pool LQ, Palacios-Vargas JG, Cano-Santana Z, Castaño-Meneses G. Diversity patterns of Collembola in an elevational gradient in the NW slope of Iztaccíhuatl volcano state of Mexico, Mexico. Entomol. News. 2010;121:249–261. [Google Scholar]
  • 43.Baniyamuddin M, Tomar VVS, Ahmad W. Functional diversity of soil inhabiting nematodes in natural forests of Arunachal Pradesh India. Nematol. Mediterr. 2007;35:109–121. [Google Scholar]
  • 44.Hanel L. Nematode assemblages indicate soil restoration on colliery spoils afforested by planting different tree species and by natural succession. Appl. Soil. Ecol. 2008;40:86–99. [Google Scholar]
  • 45.Rizvi AN. Community analysis of soil inhabiting nematodes in natural Sal forests of Dehradun India. Int. J. Nematol. 2008;18:181–190. [Google Scholar]
  • 46.Keith AM, Broker RW, Osler GHR, Chapman SJ, Burslem DFRP, Wal R. Strong impacts of below-ground tree inputs on soil nematode trophic composition. Soil Biol. Biochem. 2009;41:1060–1065. [Google Scholar]
  • 47.Keith AM, Van Der Wal R, Brooker RW, Osler GHR, Chapman SJ, Burslem DFRP. Birch invasion of heather moorland increases nematode diversity and trophic complexity. Soil Biol. Biochem. 2006;38:3421–3430. [Google Scholar]
  • 48.Forge T, Simard S. Structure of nematode communities in forest soils of southern British Columbia relationships to nitrogen mineralization and effects of clearcut harvesting and fertilization. Biol. Fertil. Soils. 2001;34:170–178. [Google Scholar]
  • 49.Savin MC, Gorres JH, Neher DA, Amador JA. Biogeophysical factors influencing soil respiration and mineral nitrogen content in an old field soil. Soil Biol. Biochem. 2001;33:429–438. [Google Scholar]
  • 50.Postma-Blaauw MB, De Vries FT, De Goede RGM, Bloem J, Faber JH, Brussaard L. Within trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia. 2005;142:428–439. doi: 10.1007/s00442-004-1741-x. [DOI] [PubMed] [Google Scholar]
  • 51.Bongers T, Ferris H. Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol. Evol. 1999;14:224–228. doi: 10.1016/s0169-5347(98)01583-3. [DOI] [PubMed] [Google Scholar]
  • 52.Ferris H, Bongers T, De Goede RGM. A framework for soil food web diagnostics extension of the nematode faunal analysis concept. Appl. Soil. Ecol. 2001;18:13–29. [Google Scholar]
  • 53.Ferris, H., Bongers, A.M.T. & De Goede, R. Nematode faunal analyses to assess food web enrichment and connectance. Nematology monographs and perspectives. In Proceedings of the Fourth International Congress of Nematology, Brill 503–510 (2004).
  • 54.Ferris H, Zheng L, Walker MA. Resistance of grape rootstocks to plant-parasitic nematodes. J. Nematol. 2012;44:377–386. [PMC free article] [PubMed] [Google Scholar]
  • 55.Quist CW, Van Der Putten WH, Thakur MP. Soil predator loss alters aboveground stoichiometry in a native but not in a related range-expanding plant when exposed to periodic heat waves. Soil Biol. Biochem. 2020;150:107999. [Google Scholar]
  • 56.Ferris H, Matute MM. Structural and functional succession in the nematode fauna of a soil food web. Appl. Soil. Ecol. 2003;23:93–110. [Google Scholar]
  • 57.Tomar WWS, Ahmad W. Food web diagnostics and functional diversity of soil inhabiting nematodes in a natural woodland. Helminthologia. 2009;46:183–189. [Google Scholar]
  • 58.Hanel N. Soil Nematodes in alpine meadows of the Tatra National Park (Slovak Republic) Helminthologia. 2017;54(1):48–67. [Google Scholar]
  • 59.Hanel L, Cerevkova A. Diversity of soil Nematodes in meadows of the White Carpathians. Helminthologia. 2006;43:109–116. [Google Scholar]
  • 60.Neely CL, Beare MH, Hargrove WL, Coleman DC. Relationships between fungal and bacterial substrate-induced respiration biomass and plant residue decomposition. Soil Biol. Biochem. 1991;23(10):947–954. [Google Scholar]
  • 61.Moller J, Miller M, Kjoller A. Fungal–bacterial interaction on beech leaves: Influence on decomposition and dissolved organic carbon quality. Soil Biol. Biochem. 1999;31(3):367–374. [Google Scholar]
  • 62.Banerjee S, Kirkby CA, Schmutter D, Bissett A, Kirkegaard JA, Richardson AE. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil. Soil Biol. Biochem. 2016;97:188–198. [Google Scholar]
  • 63.Nottingham AT, Hicks LC, Ccahuana AJ, Salinas N, Baath E, Meir P. Nutrient limitations to bacterial and fungal growth during cellulose decomposition in tropical forest soils. Biol. Fertil. Soils. 2018;54(2):219–228. [Google Scholar]
  • 64.Albright MB, et al. Soil bacterial and fungal richness forecast patterns of early pine litter decomposition. Front. Microbiol. 2020;11:542220. doi: 10.3389/fmicb.2020.542220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Champion HG, Seth SK. Revised Forest Types of India. Manager of Publications Government of India Delhi; 1968. [Google Scholar]
  • 66.Singh D, Chhonkar PK, Pandey RN. Manual on Soil, Plant and Water Analysis. Westville Publishing House; 2005. [Google Scholar]
  • 67.Jackson ML. Soil Chemical Analysis. Prentice-Hall of India Pvt. Ltd; 1973. p. 498. [Google Scholar]
  • 68.Walkley A, Black IA. An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 1934;37:29–37. [Google Scholar]
  • 69.Kjeldahl J. New method for the determination of nitrogen. Chem. News. 1883;48(1240):101–102. [Google Scholar]
  • 70.Olsen SR, Cole W, Watanable FS, Dean LA. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Methods Soil Anal. Circ. 1954;939(1883):1–56. [Google Scholar]
  • 71.Fick SE, Hijmans RJ. WorldClim 2: New 1km spatial resolution climate surfaces for globalland areas. Int. J. Climatol. 2017;37(12):4302–4315. [Google Scholar]
  • 72.Cobb, N.A. Estimating the Nematode population of the soil. In Agricultural Technical Circular No. 1 48 (United States Department of Agriculture Bureau of Plant Industry, 1918).
  • 73.Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS. Feeding habits in soil Nematode families and genera—An outline for soil ecologists. J. Nematol. 1993;25:315–331. [PMC free article] [PubMed] [Google Scholar]
  • 74.Forge T, Simard S. Structure of nematode communities in forest soils of southern British Columbia: Relationships to nitrogen mineralization and effects of clearcut harvesting and fertilization. Biol. Fertil. Soils. 2001;34:170–178. doi: 10.1007/s003740100390. [DOI] [Google Scholar]
  • 75.Bongers T. The maturity index an ecological measure of environmental disturbance based on nematode species composition. Oecologia. 1990;83:14–19. doi: 10.1007/BF00324627. [DOI] [PubMed] [Google Scholar]
  • 76.Bongers T, Bongers M. Functional diversity of nematodes. Appl. Soil. Ecol. 1998;10:239–251. [Google Scholar]
  • 77.Bongers T, De Goede RGM, Korthals GW, Yeates GW. Proposed changes of c–p classification for nematodes. Russ. J. Nematol. 1995;3:61–62. [Google Scholar]
  • 78.Neher DA, Campbell CL. Nematode communities and microbial biomass in soils with annual and perennial crops. Appl. Soil. Ecol. 1994;1(1):17–28. [Google Scholar]
  • 79.Sieriebriennikov B, Ferris H, de Goede RG. NINJA: An automated calculation system for nematode-based biological monitoring. Eur. J. Soil Biol. 2014;61:90–93. [Google Scholar]
  • 80.Andrassy IT. Determination of volume and weight of nematodes. Acta Zool. Acad. Sci. Hung. 1956;2:1–15. [Google Scholar]
  • 81.Ferris H. Form and function: Metabolic footprints of nematodes in the soil food web. Eur. J. Soil Biol. 2010;46:97–104. [Google Scholar]
  • 82.Oksanen, J.B. et al. vegan: Community ecology package. R package version 5–6 (2020).
  • 83.R Core Team. R: A Language and Environment for Statistical Computing (2019). Retrieved from https://www.R-project.org.
  • 84.Figures 1, 3 and 4 was prepared using GraphPad Prism version 8.0.2 for Windows, GraphPadSofware, La Jolla California USA. www.graphpad.com.

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