Community Structure of Epilithic Moss Mites and Their Response to Environmental Factors in Different Grades of Rocky Desertification Habitats

Abstract

This research has been undertaken to reveal the changes in the community structure of epilithic moss mites and the response of these mites to environmental factors under different grades of rocky desertification environment. In this study, epilithic moss mites were collected in a demonstration area for rocky desertification management in Bijie Salaxi, with the following rocky desertification grades as habitat gradients: without rocky desertification, potential rocky desertification, light rocky desertification, moderate rocky desertification, and severe rocky desertification. The differences in the number of individuals, taxa, diversity index, dominance index, richness index, evenness index, and the effects of environmental factors on moss mite communities were revealed by one-way ANOVA, correlation analysis, and redundancy analysis for different grades of these mites. The results show that a total of 11,563 epilithic moss mites were captured in the study area, belonging to three orders, 100 families, and 171 genera, with Nanorchestes and Trichogalumna as the dominant taxa. With the deepening of rocky desertification, the dominant number of Nanorchestes and Trichogalumna increased. Still, the percentage of very rare genera also decreased, and there were differences in the composition of the dominant genus taxa in different grades of rocky desertification. Different grades of rocky desertification habitats had significant effects on the diversity index and richness index of moss mite species but not on the number of taxa, individuals, dominance index, and evenness index. The overall epilithic moss mite communities in different habitats were moderately dissimilar. Air temperature and rock temperature had strong effects on each index of moss mite diversity, whereas light factors and air humidity had a weak impact on these indices. Amongst the communities, those of Scheloribates are more sensitive to rock temperature variation, while Blattisocius, Ledermuelleria and Camerobia correlate more with a light variation. Parholaspulus, Blattisocius, Camerobia, Haplochthonius, Gymnodamaeus, etc. were more sensitive to changes in air humidity. The research shows that there are differences in moss mite community structure under different rocky desertification grades, rocky desertification has caused some effects on moss mite community structure, and the use of mite dominant taxa genera can give preliminary indications of the rocky desertification environment; meanwhile, there is a specific correlation between mite taxa and habitat environment changes.

1. Introduction

The southern China karst, represented in Guizhou province, is the leading distribution area of the karst ecosystem in China [1,2]. With the increase in rock desertification, the structure and function of the regional ecosystem are gradually degraded, and the biodiversity is affected accordingly. As a pioneer plant for ecological restoration [3,4], mosses are characterized by a simple structure, tiny form and wide distribution [5], there being about 20,000–25,000 species worldwide and about 3500 species in China [6]. Bryophytes contribute significantly to overall plant diversity as well as to ecosystem functions and processes, such as carbon fixation, nitrogen cycling, soil and water conservation and soil moisture regulation [7]. Bryophytes are the dominant ground cover in various ecosystems, influencing the performance and distribution of other plants [8], while providing a rich food source and good habitat for the micro-arthropods that survive in them [9,10].

Mites belong to the phylum Arthropoda, Arachnida, and the subclass Acari and are the most diverse group in Arachnida. They are widely distributed throughout the world and live in a variety of environments [11]. Research on the structural characteristics and biodiversity of mite communities in different habitats has attracted widespread attention. Scientific studies on mites first began in the late 19th and early 20th centuries and domestic studies in China began in the 1950s [12]. The study sites include North America [13], South America [14], Europe [15], Australia [16], South Africa [17], Russia [18] and China [19]. These study environments include broad-leaved forests [20], grasslands [21], deserts [22], farmlands [23], parks [24] and dwellings [25]; the study contents include mite community structure [26], species diversity and their interactions with habitat types [27], soil physical and chemical properties [28], climatic factors [29], heavy metal pollution [30] and land use practices [31].

As a complete ecosystem with limited space that integrates ground and underground processes, the moss layer has a very important ecological value [32]. The study of mites in moss has led to the discovery of new species there from the initial number of species already known [33]. This further develops the study of the relationship between mites and environmental factors, such as humidity and temperature, in the moss [34]. The content of research then changed to focus on the food chain and food network in the moss layer [35]. Today, the research of miniature ecosystems has gradually developed, including research on the interactions between moss, mites, bacteria, and algae [36].

In recent years, research results on mites in soil have become more abundant in China; however, the adaptation mechanism and species diversity of mites in the specific habitat of epilithic mosses in rocky desertification areas need to be explored in depth. This paper is a study of mites of epilithic mosses within different grades of rocky desertification, aiming to understand the species, number, community structure and diversity of mites of epilithic mosses and to provide scientific information for biodiversity conservation in karst areas.

2. Materials and Methods

2.1. Study Area

The study area is located in Salaxi town, Qixingguan district, Bijie city, Guizhou province and is the site of the National 13th Five-Year Plan Key Research and Development Program (2016YFC0502601). The coordinates of the site are 27°12′30″–27°16′50″ N, 105°03′10″–105°05′08″ E and the total area is 8627.19 hm², with rocky desertification accounting for 64.83%. The study area belongs to the karst plateau mountain environment, with elevations ranging from 1495 to 2200 m, dominated by high and middle mountain landform types. Permian limestone, tuff and sand shale are mainly exposed in the area, with a large number of crest depressions being distributed here. Due to the large area of exposed bedrock in the limestone area, the soil parent material is loose and weathering is fast, thus soil erosion is serious. The soil type is mainly zoned loam with a small amount of yellowish-brown loam and weathered lime soil. The territory belongs to the subtropical humid monsoon climate, with abundant rainfall, but of uneven precipitation distribution and large annual differences, the maximum annual rainfall being 1056.6 mm, the minimum annual rainfall being 766.5 mm and the average annual rainfall being 859 mm. The annual rainfall distribution is most concentrated from July to September, which accounts for about 52.6% of the total. The annual average temperature is 12 °C, the annual average sunshine hours are 1261 h and the frost-free period is 258 d. The vegetation is subtropical evergreen coniferous and broad-leaved forest, as well as deciduous broad-leaved forest. However, due to human destruction, the native vegetation has been significantly destroyed and now the vine and thorn scrub is mainly green ganger, oak, firethorn and rhododendron. Additionally, there are scattered sparse residual forests and young forests of mainly pine, fir, aspen etc. on the local slopes and valleys. The demonstration area is dominated by light rock desertification, followed by moderate rock desertification, with the least severe rock desertification showing a light-moderate rock desertification landscape, which is typical for a mountainous karst plateau area of light-moderate rock desertification.

2.2. Sample Site Set-Up and Sample Collection

In the study area, comprehensive investigation and research were conducted, and five different grades of rock desertification were selected, namely, without rock desertification (WRD), potential rock desertification (PRD), light rock desertification (LRD), moderate rock desertification (MRD) and severe rock desertification (SRD), with reference to the classification standard of rock desertification [37]. Six replicate sample plots (20 m × 20 m) were established for each grade and a total of 30 fixed sample plots were set up. In October 2021, three 1 m × 1 m sample plots were selected in accordance with the “S” sampling method and one square 10 × 10 cm of moss was collected from each sample plot at intervals of 5 m [38,39]. The moss mite samples were collected in each sample area with little human interference, relatively uniform moss thickness and relatively flat terrain. All samples were placed in individual cotton bags and numbered and then brought back to the laboratory for the separation and identification of mites. Meanwhile, altitude, longitude and latitude were measured and recorded by a GPSmap60CSx meter; temperature and humidity were measured and recorded by a TASITA622A meter; rock temperature was measured and recorded by a TASITA601B meter and luminosity was measured and recorded by a SMARTSENSORAS813 meter.

2.3. Isolation and Identification of Moss Mites

The samples were separated by the Tullgren method, the temperature of separation was strictly controlled at about 32 °C and heated continuously for 48 h [40,41]. Then the Petri dishes containing soil animals were viewed under an Olympus microscope and the mites were separated from arthropods with small brushes and soft forceps. The separated specimens were fixed and cleaned with 75% alcohol and the cleaned mite specimens were preserved in finger-shaped tubes containing lactic acid solution for transparency. The experimental procedure involved making slides of the mite specimens after transparency and then placing them under a microscope for observation and identification.

The main references used for identification were: “A Manual of Acarology (Third Edition)” by Krantz and Walter [42], “Acarology” by Li and Li [43], “Acarina Subfamily Search” by Baker and Camin [44], “Pictorial Keys to Soil Animals of China” by Yin [45], “Soil gamasid mites in Northeast China” by Yin [46] and “Introduction to acaroid mites in China” by Li and Shen [47]. All specimens were identified to genus-level units (except if mites and specimens were of incomplete body size) and the number of individual mites was counted at the same time. The classification system of “A Manual of Acarology” (Third Edition) was mainly adopted for the mite classification order in the paper.

2.4. Data Processing and Calculation

2.4.1. Community Dominance

More than 10% of the total number of individuals are dominant taxa (++++), 1% to 10% are common taxa (+++), 1% to 0.5% are rare taxa (++) and less than 0.5% are very rare taxa (+) [48].

2.4.2. Biodiversity Index Calculation [49]

Simpson dominance index (D):

$$D=\sum {\left(n_i/N\right)}^2$$

(1)

Shannon–Wiener Diversity Index (H′):

$$H^{\prime }=-{\displaystyle \sum }_{i=1}^s\left(P_i\ln P_i\right)$$

(2)

Margalef richness Index (M):

$$M=\left(S-1/\ln N\right)$$

(3)

Pielou evenness index (E)

$$E=H^{\prime }/H_{max}=H^{\prime }\ln S$$

(4)

where: N is the total number of individuals in the community, S represents the total number of taxa genera of moss mites, P_i represents the ratio of the number of individuals of class i moss mites to the total number of individuals, and n_i is the number of individuals of taxon i.

The Jaccard similarity coefficient (q) was used to characterize the similarity between communities and was calculated as:

q = c/(a + b − c)q = c/(a + b − c)

where: a denotes the number of taxa genera of community a, b denotes the number of taxa genera of community b and c denotes the number of taxa genera common to both communities. The formula specifies the similarity level as follows: 0 < q < 0.25, very dissimilar; 0.25 ≤ q < 0.5, moderately dissimilar; 0.5 ≤ q < 0.75, moderately similar; 0.75 ≤ q < 1.00, very similar.

2.4.3. Analysis

Multiple diversity indices and Jaccard similarity indices were calculated using PAST 4.10 software [50]. The data were tested for normal distribution using IBM SPSS Statistics 22.0 software and log(x+1) transformation was performed for data that did not follow normal distribution. Subsequently, one-way ANOVA was used to test the significance of differences between different rock desertification classes (p < 0.05) and the LSD method and Tamhane’s T2 method were used for multiple comparisons. Redundancy analysis was used to visualize the relationship between moss mite species and environmental factors. Prior to that, to determine a reasonable analytical model, the data were first subjected to a detrended correspondence analysis, which showed that, as the gradient length of the first axis was >3.0, the RDA linear response model was selected [51]. Correlation ranking plots were performed in Canoco 5.0 software. To explore the response of specific moss mite species to environmental changes, Mantel test correlation heat maps were plotted using the R 4.1.3 “ggcor” packages [52]. In this case, Bray–curtis distance was used for both mite and environmental factor data and Spearman correlation coefficients were used for species and environmental factors, with 9999 permutations being performed to test significance. The top 50 moss mite taxa in terms of number of individuals were selected for the chord diagram using R 4.1.3 “circlize” packages [53]. Histograms of diversity indices and Euclidean distance cluster analysis were plotted using Origin 2021.0.

3. Results

3.1. Community Composition and Distribution of Moss Mites in Different Grades of Rock Desertification

A total of 11,563 moss mites belonging to 171 genera in 100 families of three orders (Appendix A) were captured in a survey of moss mites sampled from five rocky desertification grades. Amongst these, 17 families and 38 genera of Mesostigmata, 12 families and 13 genera of Trombidiformes and 71 families and 120 genera of Sarcoptiformes were identified. Moss mites were found in each rock desertification level: 101 genera in 68 families of three orders for without rock desertification, 96 genera in 66 families of three orders for potential rock desertification, 79 genera in 62 families of three orders for light rock desertification, 54 genera in 42 families of three orders for moderate rock desertification and 54 genera in 39 families of three orders for severe rock desertification. The number of species showed a gradual decrease with the deepening of rock desertification.

In the habitats without rocky desertification, the dominant taxa of mites were Scheloribates and Scutovertex and the extremely rare genera were Atropacarus, Epicrius, Geolaelaps, Camerobia, Epilohmannoides etc. The percentages of dominant, common, rare and extremely rare genera were 34.03%, 49.27%, 7.30% and 9.40%, respectively.

In the habitats of potential rocky desertification, the dominant taxa of mites were Scutovertex and Scheloribates and the extremely rare genera were Carabodes, Arctoseius, Zercon, Licnodamaeus, Laelaspis etc. The percentages of dominant, common, rare and extremely rare genera were 38.61%, 50.78%, 2.47% and 8.14%, respectively.

In the habitats light rocky desertification, the dominant taxa of mites were Scheloribates and Scutovertex and the extremely rare genera were Megeremaeus, Eremella, Gymnodamaeus, Polypterozetes, Microtrombidium etc. The percentages of dominant, common, rare and extremely rare genera were 32.64%, 55.11%, 5.77% and 6.48% respectively.

In the habitats moderate rocky desertification, the dominant taxa of mites were Trichogalumna, Nanorchestes and Tectocepheus and the extremely rare genera were Oxyoppia, Bdella, Carabodes, Protokalumna, Eulohmannia etc. The percentages of dominant, common, rare and extremely rare genera were 54.86%, 38.52%, 1.43% and 5.20%, respectively.

In the habitats severe rocky desertification, the dominant taxa of mites were Trichogalumna, Nanorchestes and Scutovertex and the extremely rare genera were Cornigamasus, Xylobates, Rhysotritia, Perxylobates, Eohypochthonius etc. The percentages of dominant, common, rare and extremely rare genera were 61.06%, 31.48%, 2.76% and 4.70%, respectively.

It is clear that, as rock desertification progresses, the dominant number of Nanorchestes and Trichogalumna increases, while the percentage share of very rare genera decreases, there being some variation in the genus composition of dominant taxa in different rock desertification grades.

3.2. Diversity and Similarity of Moss Mite Communities in Different Rocky Desertification Grades

In epilithic moss habitats of different rocky desertification grades, the number of mite taxa was largest in the potential rocky desertification grade, in the order of PRD > LRD > WRD > MRD > SRD. The number of individual mites was highest in the severe rock desertification grade, in the order of SRD > MRD > PRD > LRD > WRD. Mite diversity index with the highest potential rock desertification grade was in the order of PRD > WRD > LRD > SRD > MRD. Mite dominance index was highest in severe rock desertification grade, in the order of SRD > MRD > WRD > LRD > PRD. Mite richness index was highest with potential rock desertification grade, in the order of PRD > WRD > LRD > MRD > SRD. The mite evenness index was highest with potential rock desertification grade, in the order of PRD > WRD > LRD > SRD > MRD. Meanwhile, the rocky desertification rank had a significant effect (p < 0.05) on the diversity index and richness index of moss mite species, while the effects on the number of taxa, individuals, dominance index and evenness index were not significant (p > 0.05) (Figure 1). The top ten taxa in the number of epilithic moss mites were Scutovertex, Nanorchestes, Trichogalumna, Scheloribates, Tectocepheus, Tyrophagus, Camisia, Platynothrus, Epilohmannoides and Nothrus (Figure 2). The results of the study show that different levels of rocky desertification affected mite diversity within the habitat, as well as the number of mites between each habitat to some extent. Classification is a means for scholars to understand nature.

The purpose of this classification of biological communities is to reveal ecological relationships and reflect ecological laws and shows, to some extent, the formation and development of community types and their close relationship with the surrounding environment [54]. The results of Jaccard similarity analysis of epilithic moss mite communities at different levels of rock desertification are shown in

Table 1. Similarity index of epilithic moss mite communities of different rocky desertification grades.

	WRD	PRD	LRD	MRD	SRD
WRD		0.417	0.429	0.348	0.325
PRD	0.417		0.496	0.339	0.389
LRD	0.429	0.496		0.385	0.415
MRD	0.348	0.339	0.385		0.421
SRD	0.325	0.389	0.415	0.421

Note: 0 < q < 0.25, Extremely dissimilar; 0.25 ≤ q < 0.5, moderately dissimilar; 0.5 ≤ q < 0.75, moderately similar; 0.75 ≤ q < 1.00, extremely similar. WRD: without rock desertification, PRD: potential rock desertification, LRD: light rock desertification, MRD: moderate rock desertification and SRD: severe rock desertification.

which demonstrates that the epilithic moss mite communities in the study area are generally at a moderately dissimilar level and the Jaccard similarity index values are in the range of 0.25–0.5. Amongst these, the highest mite community similarity index was 0.4957 in light rock desertification and potential rock desertification environments. The lowest mite community similarity index was 0.325 in the severe rocky desertification and without rocky desertification environments (Table 1).

In the Euclidean distance intergroup mean clustering ranking of epilithic moss mite communities (Figure 3), according to 60% similarity, these communities in the study area can be divided into four groups, in which the similarity between without rocky desertification grade and light rocky desertification grade is above 64%. According to the 40% similarity, the communities can be divided into two groups. The figure shows that, within moderate rock desertification, severe rock desertification and the other three grades of rock desertification, there are community structure differences, the degree of similarity being low. This difference may be caused by differences in environmental factors, such as rock temperature, air temperature and humidity and light in the microhabitats where moss mite species are located, while the deepening of rock desertification increases this variability.

3.3. Response of Epilithic Moss Mites to Environmental Factors in Different Grades of Rocky Desertification

The purpose of this research is to identify the response of epilithic moss mites to environmental changes in different rocky desertification grades. The number of taxa, number of individuals, diversity index, dominance index, richness index and evenness index were used as response variables and altitude, light, rock temperature and air temperature and humidity were used as explanatory variables for the redundancy analysis. The results of the two-dimensional ranking between the characteristics of the mite community of epilithic mosses and environmental factors (Figure 4) show that altitude was positively correlated with the number of mite taxa, the number of individuals and the Simpson dominance index and negatively correlated with the diversity indices of the other three species. Light was positively correlated with the number of individuals and the Simpson dominance index. Air humidity was strongly and positively correlated with the number of moss mite individuals at a very small angle, shown in Figure 4. Air temperature was positively correlated with the number of individuals of moss mite species and negatively correlated with the Simpson dominance index, Shannon diversity index and Margalef species richness index. Rock temperature had a positive correlation with the number of individuals, Pielou evenness index and Shannon diversity index. This shows that air temperature and rock temperature have stronger effects on each index of moss mite diversity and the light factor and air humidity have weaker effects on each index of moss mite. It also reflects how the response of epilithic moss mites to temperature change is more sensitive and the response degree is higher.

Scheloribates had the highest correlation with rock temperature at a highly significant level (p < 0.01) and Licnocepheus had an elevated correlation with rock temperature (p < 0.05) as seen in (Figure 5). Blattisocius, Camerobia, Haplochthonius, Pheroliodes, Tegeozetes, Ametroproctus and Scheloribates had a higher correlation with altitude (p < 0.05). Blattisocius, Ledermuelleria, Camerobia, Haplochthonius, Tegeozetes and Ametroproctus were more correlated with light (p < 0.05), whereas Rhodacarus, Trhypochthonius, Podopterotegaeus, Cosmogalumna and Suidasia were more correlated with air temperature (p < 0.05). Parholaspulus, Blattisocius, Camerobia, Haplochthonius, Gymnodamaeus, Tegeozetes and Ametroproctus correlated higher with air humidity (p < 0.05).

It has been found that mites are often used as indicator organisms for soil nutrients and environmental disturbances and indicator species analysis has been successfully applied in ecological restoration studies [55].

4. Discussion

4.1. Diversity of Epilithic Moss Mites in Different Rock Desertification Grades

The α-diversity, β-diversity and γ-diversity of mite communities are influenced by large-scale environmental factors, such as geographic location, natural hazards and climate [56,57,58] and are also limited by microhabitats such as lichens, mosses, bark and soil surfaces [59]. It was found that the number of individuals and family taxa of mites in the microhabitat of mosses was richer and the community characteristics were more prominent than in the environments of soils [60] and forests [61], which are also the study area of rocky desertification.

In environments with different degrees of rock desertification, stony moss mites showed different community diversity as well as variability. The present study shows that the number of species gradually decreased with the increase in rock desertification. The reason for this phenomenon could be that the extremes of the ecological environment have a negative impact on the survival of the species. It has been shown that the extreme arid mountain environment limits the development of small arthropod communities, such as mites [62]. The increase in the grade of desertification has caused a gradual increase in the number of Nanorchestes and Trichogalumna, while the percentage of very rare genera has been decreasing. According to the results of existing studies, Nanorchestes is found in abundance in mossy habitats on the Antarctic continental archipelago [63] and Scheloribates and Trichogalumna are present in high numbers in both moderate and severe rocky desertification environments [64]. Therefore, the author hypothesized that mites are more adaptable to the environment, especially these special environments. Meanwhile, in the rocky desert environment, the widely dispersed moss layer may be an important biological reservoir for small arthropods such as mites, playing an essential function in the ecological improvement of the soil and the soil surface environment.

Overall, the diversity and richness indices of moss mite species were significantly different amongst the five classes of rocky desertification habitats, while the differences in the number of taxa, individuals, dominance index and evenness index were not significant. This indicates that the special environment of rocky desertification, which is a combination of natural forces and anthropogenic disturbance, has a certain degree of influence on moss mite community structure, although the difference is not significant. Recently, scholars have been conducting scientific studies on soil mites in rocky desertification areas. For example, Chen et al. [65] compared the differences in soil mite community structure in karst areas with various rock desertification types and found that the number of families and genera of soil mites tended to decrease as the rock desertification grade increased, but the change in diversity index was not significant. The number of soil mite individuals and taxa genera showed an overall increasing trend with the increase in years of land abandonment, as well as in the natural recovery state, according to a study by Xiao et al. [66] on the characteristics and differences of soil mite community structures in abandoned land in rock desertification areas over different years. Due to the influence of rock desertification, however, this trend was not large. With the lowering degree of rock desertification, the diversity and evenness indexes steadily grew. The present study also shows that different grades of rocky desertification environment had less effect on the number of individuals, taxa, dominance index and evenness index of epilithic moss mites. This could be because mites, as a free-living micro-arthropod group with a wide range of morphology, behavior and habitats, are less responsive to the medium-scale classification of stone desertification geographical systems and so do not perform well.

4.2. Response of Epilithic Moss Mites to Environmental Factors in Different Rocky Desertification Grades

The community structure and species diversity of mites are influenced by the superposition and interaction of environmental elements in ecosystems [67]. Temperature fluctuations caused by seasonal shifts, according to Kamczyc et al. [68], have a substantial impact on mite survival, reproduction and taxon abundance, altering the ecological function of the area. Long-term positive or negative ecological feedbacks, according to Vissa et al. [69], are dependent on the climatic circumstances that induce changes in mite community structure, the temperature effect. The results of the redundancy analysis in this study show that rock temperature was positively correlated with mite population and diversity and was one of the important factors influencing their extinction and growth. This result supports the conclusion of previous studies to some extent. Humidity also influenced the survival rate and development rate of mites to a certain extent. Due to the tiny size of mites, prolonged evaporative water loss poses a great obstacle to their survival and development. Wehner et al. [70] found that air humidity had no effect on moss microhabitat species distribution, but that humidity boosted diversity, which was more obvious in moss microhabitats. The results of Jakšová et al. [71] show that, as moisture gradients rose, the mean abundance of mites and total species abundance increased, implying that seasonal changes in mite community composition were more pronounced at sites with lower soil moisture. The strong positive correlation between atmospheric moisture and the number of moss mite individuals in this study also reflected this pattern. The most important function of light on mites is to govern their stagnation physiology; for example, Tetranychus cinnabarinus can grow and reproduce constantly in extended sunshine, but it stagnates in short sunlight and individuals do not feed or reproduce. Badejo and Akinwole [72] also found that mite densities were lower in high-light areas than in low-light areas, which confirms the thesis of this work.

5. Conclusions

In the context of rocky desertification in Bijie Sala Creek, the epilithic moss microhabitats of different rocky desertification grades had abundant mite species, dominated by Nanorchestes and Trichogalumna, these being representative of their species. With the change in rock desertification grade, the variability of biological indices, such as moss mite community and diversity, did not show any obvious change and the community similarity was at a moderate level. Scheloribates were more sensitive to rock temperature changes, while Blattisocius, Ledermuelleria, Camerobia etc. were more correlated with light changes. Parholaspulus, Blattisocius, Camerobia, Haplochthonius, Gymnodamaeus etc. were more closely correlated with air humidity variation.