Diversity and feeding strategies of soil microfauna along elevation gradients in Himalayan cold deserts

Abstract

High-elevation cold deserts in Tibet and Himalaya are one of the most extreme environments. One consequence is that the diversity of macrofauna in this environment is often limited, and soil microorganisms have a more influential role in governing key surface and subsurface bioprocesses. High-elevation soil microfauna represent important components of cold ecosystems and dominant consumers of microbial communities. Still little is known about their diversity and distribution on the edge of their reproductive and metabolic abilities. In this study, we disentangle the impact of elevation and soil chemistry on diversity and distribution of rotifers, nematodes and tardigrades and their most frequent feeding strategies (microbial filter-feeders, bacterivores, fungivores, root-fungal feeders, omnivores) along two contrasting altitudinal gradients in Indian NW Himalaya (Zanskar transect from 3805 to 4714 m a.s.l.) and southwestern Tibet (Tso Moriri transect from 4477 to 6176 m a.s.l.), using a combination of multivariate analysis, variation partitioning and generalized additive models. Zanskar transect had higher precipitation, soil moisture, organic matter and available nutrients than dry Tso Moriri transect. In total, 40 species of nematodes, 19 rotifers and 1 tardigrade were discovered. Species richness and total abundance of rotifers and nematodes showed mid-elevation peaks in both investigated transects. The optimum for rotifers was found at higher elevation than for nematodes. Diversity and distribution of soil microfauna was best explained by soil nitrogen, phosphorus and organic matter. More fertile soils hosted more diverse and abundant faunal communities. In Tso Moriri, bacterivores represented 60% of all nematodes, fungivores 35%, root-fungal feeders 1% and omnivores 3%. For Zanskar the respective proportions were 21%, 13%, 56% and 9%. Elevational optima of different feeding strategies occurred in Zanskar in one elevation zone (4400-4500 m), while in Tso Moriri each feeding strategy had their unique optima with fungivores at 5300 m (steppes), bacterivores at 5500 m (alpine grassland), filter-feeders at 5600 m and predators and omnivores above 5700 m (subnival zone). Our results shed light on the diversity of microfauna in the high-elevation cold deserts and disentangle the role of different ecological filters in structuring microfaunal communities in the rapidly-warming Himalayas.

Fig 1. Altitudinal changes in soil physico-chemical properties in Zanskar and Tso Moriri.

Generalized Additive Models were used to analyse altitudinal responses. Redundancy analysis biplots show interrelationships between soil variables and elevation. For units, see Table 1. Explained variation (R²) and estimated Type I errors (P values *<0.05, **<0.01, ***<0.001) are shown in parentheses.

Fig 2. The CCA ordination of soil microfauna.

The most explaining environmental variables were determined by forward selection (red arrows) for (A) Zanskar and (B) Tso Moriri mountain ranges. Source data are log-transformed, species are represented by blue dots (for full names, see S1 Table). Feeding groups, altitude and other environmental variables are passively projected into the CCA ordination diagram (green arrows). The isolines of species richness of samples (grey lines) are fitted using the Loess smoothing splines.

Fig 3. Altitudinal changes in abundance and richness of rotifers and nematodes along two gradients (Zanskar and Tso Moriri) in Indian NW Himalaya.

Generalized Additive Models were used to analyse altitudinal responses of soil microfauna. Abundances were log-transformed. Explained variation (R²) and estimated Type I errors (P values *<0.05, **<0.01, ***<0.001) are shown in parenthesis.

Fig 4. Altitudinal changes in abundance of microfaunal feeding groups along two mountain transects (Zanskar and Tso Moriri) in Indian NW Himalayas.

Generalized Additive Models were used to analyse altitudinal responses of omnivorous nematodes (Omnivores), filter-feeding rotifers (Filter-feeders), fungivorous nematodes (Fungivores), bacterivorous nematodes (Bacterivores), predacious nematodes (Predators) and root-fungal feeding nematodes (Root-fungal feeders). Explained variation (R²) and estimated Type I errors (P values *<0.05, **<0.01, ***<0.001) are shown in parenthesis.

Fig 5. Conditional inference trees showing a significant effect of environmental factors on abundance of individual microfaunal feeding groups.

In each split of the tree, all predictors are tested and the one that best discriminates between higher and lower values is selected. Each split of the tree is described by the factors associated with the split (ovals), the permutation-based significance of the split (P-value) (ovals) and the level at which the split occurs (line between ovals and boxes). The Box-and-Whisker plot and number of plots (n) is given at each terminal node.