Urban land-use impacts on composition and spatiotemporal variations in abundance and biomass of earthworm community

Jihang Li·Zhe Zhang·Hong Wang·Shaojun Wang,2·Qibo Chen

Abstract Soil fauna can sensitively respond to alterations in soil environment induced by land-use changes.However,little is known about the impact of urban land-use changes on earthworm communities.In this study,three land-use types(i.e.,forest,nursery and abandoned lands)were chosen to identify differences in diversity,abundance and biomass of earthworm community in Kunming City.Urban land-use had a pronounced difference in species composition,evenness and diversity of earthworm communities.Forest land had the highest density,biomass and diversity of the earthworm communities.Total abundance was dominated by endogeic species in nursery land(70%)and abandoned land(80%),whereas in the forest land,the earthworm community comprised epigeic,endogeic and anecic species.Temporal changes in earthworm density and biomass were also significantly affected by land-use change.Total density and biomass of earthworms in the forest and nursery lands were highest in September,but highest in the abandoned land in October.The influence of soil physicochemical properties on the earthworm density and biomass also varied with land-use types.Soil temperature significantly affected earthworm density and biomass in the three land-use types.Soil pH was positively correlated with earthworm biomass in the forest land,but negatively associated with earthworm density in the abandoned land.Soil organic matter was positively correlated only with density and biomass of earthworms in the nursery and abandoned lands.Our results suggest that the species composition,abundance and biomass of earthworm communities can be determined by the modification of soil properties associated with urban land-use type.

Keywords Biomass·Density·Earthworm community·Soil physicochemical properties·Spatiotemporal dynamics

Introduction

Earthworms, an important functional component in ecosystems,are known as ecosystem engineers.They are one of the few large soil fauna(e.g.,earthworms,ants and termites)that affect crucial processes contributing to soil fertility(Decae¨ns et al.1999;Wang and Ruan 2008).Earthworms can loosen soil,improve structure and permeability of soil through burrowing and feeding(Emmerling et al.2015;Bohlen et al.2004)and stimulate nutrient cycling and biological activities in the soil through digestion,decomposition,secretion and excretion(Tian et al.2000;Araujo et al.2004;Sheehan et al.2006).As a result,earthworms can affect plant growth, productivity and vegetation succession(Zhang et al.2007;Wang et al.2008;Dempsey et al.2013).

Different land-use types have diverse vegetation covers,and above-and belowground litter inputs,which affect physicochemical environment and microbial diversity of the soil(Birkhofer et al.2012).The earthworm community can sensitively respond to these changes(Bini et al.2013;Dempsey et al.2013).Therefore,these changes can ultimately influence composition,diversity and spatiotemporal distribution of earthworm communities,and even lead to the succession of plant communities(Hale et al.2006;Groffman et al.2015).At present,some studies have focused on the effect of land-use change on soil fauna,but few have directly involved earthworms(Li et al.2013).Even fewer have examined the effect of urban land-use changes on earthworm communities.

The pattern of urban land-use in Kunming has undergone profound changes,and thus can significantly affect earthworm communities.In the present study,we explored the effect of three land-use types(i.e.,forest,nursery,abandoned lands) on the abundance and diversity of earthworm community in the Kunming City to answer three main questions:(1)How do species diversity and the spatiotemporal abundance and biomass of the earthworm community differ among the three land-uses?(2)How are soil changes (e.g., temperature, moisture, pH, organic matter,total nitrogen,hydrolyzable nitrogen of soil)associated with the diversity, abundance and biomass of earthworm community in the three land-uses?

Materials and methods

Site description and experimental design

This study was conducted in the Kunming City(25°02′11′′N,102°42′31′′E),southwest China in the middle of the Yunnan Guizhou Plateau.It has a subtropical plateau monsoon climate.Annual mean temperature and average rainfall are about 15°C and 1450 mm,respectively(from 1971 to 2000,data from China Meteorological Administration).Precipitation shows a strong seasonal variation with a rainy season(about 85%rainfall of annual precipitation)from May to October,and a dry season(only about 15%rainfall of all year)from November to April of next year.The baseband soil is red soil,and has medium soil fertility and soil structure,with soil pH value between 4.0 and 7.5 and soil organic matter content between 1.5 and 5.0%.

Three land-use types(i.e.,forest,nursery and abandoned lands)were selected to survey the composition,diversity and spatiotemporal distribution of earthworm density and biomass in Kunming.Each land-use type with similar initial conditions,soil types,and management history was replicated three times with spatial interspersion(at least 50 m apart).The first site was forest land with 84%coverage;dominant species in the tree layer were Photinia serrulata and Pinus Yunnanensis (10 m average tree height).The shrub layer was dominated by Bougainvillea spectabilis with mean height of 0.2-0.5 m.Nursery land had 56%coverage with Parakmeria yunnanensis as the dominant tree species was with mean height of 3.5 m.The third site was abandoned land with 34%coverage.The main plant species were Taraxacum mongolicum,Taraxacum mongolicum,and Bidens pilosa,with a mean tree height of 0.2 m.

Measurement of earthworm density and biomass and soil properties

Earthworms and soil were sampled in 2014 in September in the forest,in October in the nursery and in November in abandoned lands. Earthworms were sampled in each replicated site from three random samples(25×25 cm,at least 5 m apart)from three soil depths(i.e.,0-5,5-10,and 10-5 cm)using the hand sorting method,then identified,counted and released in the field.Soil temperature in each soil layer in each sampling plot was measured with a soil thermometer before earthworm collection.

The soil samples were collected from the three soil depths at the points of earthworm sampling.The soils were thoroughly mixed,air-dried,ground and passed through fine mesh(0.2 mm)sieves and kept in a plastic bag for further chemical analysis.The soil moisture content at depths was determined gravimetrically after drying approximately 20 g of fresh soil at 105°C for 48 h.Soil pH was determined using a glass electrode in a mixture of 1 part soil to 2.5 parts water(w/v).Total nitrogen concentrations in soil were measured by the Kjeldahl digestion method.Soil hydrolyzed nitrogen was measured with the alkali solution diffusion method.Soil organic matter was determined using the potassium dichromate volumetric method with a heated oil bath.

Data analyses

We quantified the abundance and diversity of the earthworm community using species richness(S), evenness index(E),and the Shannon-Wiener index(H′)(Wang et al.2015). To gain an understanding of the mechanism underlying changes in density,biomass and diversity of earthworm communities,we tested how land-use change affected soil properties(e.g.,temperature,moisture,pH,organic matter,total nitrogen,hydrolyzed nitrogen of soil).We also assessed the associations between these soil variables with the abundance and biomass of soil earthworms using a Pearson correlation analysis.We used a 3-way analysis of variance(ANOVA)to determine the effects of land-use types,sampling time and depth on earthworm abundance and biomass.SPSS version 21 was used for all statistical analyses(SPSS Inc.,Chicago,IL,USA).

Results

Species composition and diversity of earthworm community

In this study,the composition of the earthworm community varied significantly among the three types of land-use(P ＜0.05, Table 1). The epigeic (Drawida sulcata),endogeic(Amynthas divergens yunnanensis)and anecic(Metaphire californica)earthworms were the dominant species in the forest land.In contrast,the main earthworm species in the nursery land were endogeic(A.divergens and A.divergens yunnanensis)and anecic(M.browni)earthworms,but an endogeic species(A.doliari)was dominant in the abandoned land.Land-use change also had a significant effect on the diversity of earthworm community(P ＜0.05, Fig.1); species richness, evenness and the Shannon-Wiener index were higher in the forest land than in the nursery and the abandoned lands(Fig.1).

Spatiotemporal distribution of earthworm abundance and biomass

In this study,land-use types(P ＜0.01),sampling time(P ＜0.01)and depth(P ＜0.05)significantly affected the density and biomass of earthworms(Table 2).The ranking for total density of the earthworm community by land-use types was forest land(177 individuals m-2)＞nursery land(74 indiv. m-2)＞abandoned land (43 indiv. m-2)(Table 1).The total earthworm biomass was also higher in forest land (35.75 g m-2) than in the nursery(10.12 g m-2)and abandoned land(13.08 g m-2)(Figs.2,3).The abandoned land had the lowest total earthworm density,while nursery land had the lowest total earthworm biomass.

Fig.1 Species richness (S), evenness index (E), and Shannon-Weiner index(H′)measures of diversity for the earthworm communities in the three land-use types.Values with the same letter were not significantly different(P ＞0.05,ANOVA with Tukey's HSD test;bars indicate SE;n=3)

Table 2 The effects (F statistics) of land-use type (L), month(M)and depth(D)of soil sampling on total density(individuals m-2)and total biomass(g m-2)of soil earthworms in Kunming City

The land-use change showed an extremely significant impact on the temporal variations in density and biomass ofearthworms(P ＜0.01,Table 1).The pattern of temporal variations in earthworm density and biomass varied with land use types (Fig.2). The ranking for the monthly dynamics of earthworm density and biomass in forest and nursery land was September ＞October ＞November.In contrast,the earthworm density and biomass increased from September to October,and decreased from October to November in the abandoned land.

Table 1 Species abundance and percentage of earthworm community by ecological type across three land-use types in Kunming City

Fig.2 Temporal change in average of total earthworm density and biomass in three land-use types.Values with the same letter are not significantly different(P ＞0.05;bars indicate SE;n=3.ANOVA with Tukey's HSD test)

Fig.3 The spatial dynamics in average of total earthworm density and biomass along three land use types.Values with the same letter were not significantly different(P ＞0.05;bars indicate SE;n=3.ANOVA with Tukey's HSD test)

Sampling depth significantly affected earthworm density(P ＜0.05)and biomass(P ＜0.01)(Table 2).Density and biomass decreased with increasing soil depth,but the range in the vertical variation varied with land-use types(Fig.3).The reduction of earthworm abundance and biomass along the soil profile was sharper in forest land than in the nursery and abandoned lands(Fig.3).

Soil properties across the different land-use types

The effect of land-use on soil physiochemical properties at the same soil depth varied with different soil variables(Table 3).A significant difference in temperature,pH and organic matter of soil was found among the three land-use types (P ＜0.05), but not for soil total nitrogen, soil hydrolyze nitrogen and soil moisture content(P ＞0.05).The effect of land-use on the vertical variation in soil physicochemical properties for the same land-use varied with different soil variables(Table 3).Soil organic matter,total nitrogen and soil hydrolyze nitrogen differed among the three soil layers in the forest land,while in the nursery land,only soil moisture significantly declined along the soil profile.Moreover,in the abandoned land,soil temperature and hydrolyze nitrogen significantly declined along the soil layers,but soil moisture,pH,soil organic matter and total nitrogen moisture content did not.

Relationship between soil properties and earthworm abundance and biomass

Pearson correlation analysis showed an association of earthworm abundance and biomass with soil physicochemical properties across the three land-uses(Table 4).In the forest land,earthworm density and biomass had an extreme positive correlation with soil temperature(P ＜0.01),and earthworm biomass was positively related with soil pH(P ＜0.05).Earthworm density and biomass in the nursery land were significantly related with soil temperature and soil organic matter(P ＜0.05).Earthworm density and biomass was significantly associated with temperature (P ＜0.01) and organic matter in the soil(P ＜0.05)in the abandoned land,while earthworm density was negatively correlated with soil pH at the site(P ＜0.05).

Table 3 Soil physicochemical properties across three land-use types in Kunming City

Table 4 Correlation of soil properties to earthworm density and biomass across three land-uses in Kunming City

Discussion

Different land-uses support diverse vegetation types and coverage,which leads to obvious differences in material and energy inputs above-and belowground(Bertin et al.2003), which in turn may alter the soil physical and chemical environments(Cerda`1998;Omondi et al.2010;Gong et al.2015).The changes in soil physicochemical properties can affect soil fauna(Wardle et al.2004;Uren 2007;Jouquet et al.2009;Wang et al.2010).In this study,we found a pronounced effect of urban land-use on the composition,diversity and spatiotemporal distribution of the earthworm community,which is sensitive to changes in the soil environment (e.g., moisture, temperature, pH,texture and organic matter)(Wang et al.2017).Therefore,the soil environment factors that are modified by urban land-use induce a significant effect on earthworm community.

We found that the composition and diversity of earthworm community were affected by the urban land-use.The earthworm community composition was largely dominated by endogeic species in the nursery(70%)and abandoned land(80%),while that in forest land was constituted by epigeic(17%),endogeic(54%)and anecic(29%)earthworm species.The nursery and abandoned lands do not provide enough organic matter in shallower or deeper soil layer for earthworm species,which leads to paucity of epigeic and anecic earthworms.In contrast,forest land not only provides abundant trophic resources(e.g.,litter)for epigeic species,but also organic matter(e.g.,humus and roots)in deeper soil layers for endogeic and anecic species(Decae¨ns et al.2003).Furthermore,the forest site has more diverse food resources than in nursery and abandoned lands to sustain a greater diversity of earthworm species.Thus,the difference in food resource offered by three land-use types results in diverse characteristics of earthworm community.

The earthworm abundance and biomass differed significantly among the three land-use types.Forest land had higher density and biomass of earthworms than in the nursery and abandoned lands,similar to the findings of Du et al.(2008)in Xishuangbanna and Zhang et al.(2012).The complex vegetation composition and high vegetation canopy in the forest land provide suitable microenvironment(e.g.,temperature and moisture)for growth and reproduction of earthworms(Blakemore 2000).Furthermore,the thicker litter layer in forest sites is a rich organic source of nutrients for earthworms.(Ha¨ttenschwiler et al.2005;Ruan et al.2005).

Soil microhabitats and soil properties along the soil profile determine the vertical distribution pattern in quantity and biomass of earthworms in different land-use types(Baker 1998;Du et al.2008).In forest and abandoned lands,the higher earthworm number and biomass in shallow soil layers were closely associated with larger pH,organic matter and total nitrogen in the soil layer.In nursery land,the lower pH,organic matter,temperature,and total nitrogen along the soil depths led to the decline in vertical variation of earthworm density and biomass.These results indicate that the vertical change in earthworm abundance and biomass is closely related to the spatial alterations in soil nutrient factors.

Generally,temporal variations in temperature and rainfall contribute to seasonal changes in the soil faunal community(Wang et al.2007,2010),including earthworms(Du et al.2008).In the present study,the density and biomass of earthworms in forest and nursery lands tended to decrease monthly(September ＞October ＞November).September and October had higher precipitation and appropriate temperature,in comparison with the dry month(November).Soil moisture and temperature are of crucial importance to earthworm activity(Plum and Filser 2005).Water accounts for 70-90%of earthworm biomass,which can portect excessive loss of water(Zhang et al.2005).Earthworm activity is enhanced in moist soil,but in dry soil they can enter a state of dormancy or diapause,or even die.Temperatures above a certain threshold can also be lethal to cocoons and adult earthworms(Edwards and Bohlen 1996).

Earthworm density and biomass are closely related to changes in soil physicochemical properties(Wang et al.2010).In the present study,variation in soil temperature induced by urban land-use change resulted critically affected the quantity and biomass of earthworms.Because soil moisture did not differ among the three land-uses,it had no significant effect on earthworm abundance and biomass.Soil pH is significantly correlated with earthworm density and biomass,as suitable soil pH has a crucial influence on the activity of earthworms (Dlamini and Haynes 2004;Yu et al.2007;Gonza´lez et al.2007).Soil organic matter can stimulate the growth of earthworms(Eisenhauer et al.2007;Zhang et al.2012).Thus,earthworm density and biomass in nursery and abandoned lands were significantly related with soil organic matter.Soil organic matter in forest land had no significant impact on the earthworm abundance and biomass,likely because the food and soil nutrients were sufficient for earthworm demand.Therefore,alterations in the soil environment induced by land-use change can significantly influence the dynamics of earthworm populations.

Conclusions

In this study,we observed a pronounced effect of three urban land-use types(i.e.,forest,nursery and abandoned lands)on the composition and diversity of the earthworm communities in Kunming City.Earthworms were sensitive to differences in vegetation cover and litter among the land-uses.In particular,the abundance,biomass and species diversity of earthworms were higher in the forest,likely due to its more abundant organic matter.Variations in soil physicochemical properties(e.g.,pH,organic matter,temperature,total nitrogen)among the land-uses significantly influenced the quantity,biomass and diversity of earthworm community. Our results indicated that the composition and diversity of earthworm community can be significantly affected by urban land-use through modification of soil physicochemical properties.

AcknowledgementsThis research was supported by the China 948 Program of National Forestry Bureau(2015-4-39),the National Science Foundation of China(No.41461052;31660191),Yunnan education department project(2017YJS089).