Diversity and Community Structure of Typhlocybinae in the Typical Karst Rocky Ecosystem, Southwest China

Abstract

In karst ecosystems, different geographic environmental conditions can lead to different lithospheric conditions, thus determining community composition and altering biotic interactions. Guizhou Province is a typical ecologically fragile karst area located in the South China Karst. To explore the relationship between biodiversity and environmental changes in different karst habitats, the community structure of typhlocybinae (Hemiptera, Auchenorrhyncha, and Cicadellidae) in three typical karst areas in Guizhou Province (the Zhenfeng–Huajiang Demonstration Zone, the Bijie Salaxi Demonstration Zone, and the Shibing Yuntai Mountain Nature Reserve) was analyzed. These areas are characterized by differences in terms of their geographic environment. For field investigations, typhlocybinae specimens were collected from five common leafhopper host plants—Juglans regia L., Rhus chinensis Mill., Prunus persica (L.) Batsch, Prunus salicina Lindl., and Debregeasia orientalis C.J. Chen—in the three study areas. A total of 4078 typhlocybinae specimens were captured, belonging to 6 tribes, 40 genera, and 121 species. Among them, Alnetoidia dujuanensis, Limassolla lingchuanensis, and Singapora shinshana were the dominant species. The numbers of typhlocybinae specimens from each region were as follows: Shibing, 2170 (53.2%); Bijie, 973 (23.9%); and Huajiang, 935 (22.9%). The number of leafhoppers collected in areas with serious rocky desertification was low, and the number increased with the increase in vegetation coverage. The order of the influence of environmental factors on the community structure of the leafhoppers in the three study areas was Huajiang > Bijie > Shibing. This order is consistent with the ranking of rocky desertification grades in the three study areas. The order based on the number of units at different taxonomic levels was as follows: Bijie (6 tribes, 32 genera, and 68 species) > Huajiang (6 tribes, 22 genera, and 58 species) > Shibing (5 tribes, 21 genera, and 48 species). The results show that environmental factors, such as climate and host plant leaf traits, had various effects on the characteristics and diversity of the leafhopper communities in different grades of rocky desertification areas. This study demonstrates that there are differences in species diversity in different grades of karst rocky desertification areas and provides a theoretical basis for future rocky desertification control and regional ecological restoration.

1. Introduction

Organisms are closely related to the environment, and together they make up an indivisible whole. Thus, the interaction between species diversity and ecosystems is an important aspect of biodiversity investigations [1]. Studies have shown that higher biodiversity significantly enhances ecosystem multifunctionality [2,3]. For karst ecosystems with unique hydrogeological structures, rocky desertification is the main reason for reduced biodiversity [4]. China is the country with the largest distribution of karst landscapes; for example, the carbonate rock outcrop area in the South China Karst region, which is dominated by the Yunnan–Kweichow Plateau, is 1.3 × 106 km² [5]. As a typical karst ecological environment region, Guizhou Province (103°36′–109°35′ E, 24°37′–29°13′ N) is located in the center of the South China Karst. It is characterized by complex topographic and climatic changes and strong environmental heterogeneity. Thus, complex and variable microhabitats formed there [6,7]. In a karst area with unique hydrogeological structures, severe soil erosion and rocky desertification are the main factors affecting the safety of the ecological environment and restricting economic development [8,9]. In recent years, many scholars have studied the biology and environment of the karst rocky desertification area in Guizhou, but there are few studies on the relationship between insects and the environment [10,11,12].

As a result of their abundance and range, and as the most diverse group in the animal kingdom, insects are an important part of terrestrial ecosystems. In addition, insect biodiversity has become an important global issue [13]. Leafhoppers (Hemiptera, Auchenorrhyncha, and Cicadellidae) are distributed worldwide and include around 2550 genera, with more than 21,000 species, including almost 2000 species in China [14,15,16]. Typhlocybinae is the second largest taxon in the Cicadellidae family after Deltocephalinae, and it has the largest number of available distribution records in China [14,17]. As phytophagous insects, leafhoppers live by sucking plant sap, and their small body size makes it difficult for them to migrate long distances [18,19]. Therefore, biological factors, such as plant species, leaf width, leaf length, and water content, are significant factors in their community structure. At present, the research on leafhoppers is mainly focused on classification, phylogeny, hazards, and prevention [20], and there are few studies on their distribution characteristics in karst desertification areas and possible correlations with the environment.

Leafhoppers are extremely sensitive to changes in their living environment, so the distribution characteristics of leafhopper community structure and composition can be used as important indicators for ecological monitoring and vegetation restoration [20]. The study of the correlation between leafhoppers and the environment has positive significance in terms of exploring ecosystem stability, the adaptation of organisms to the environment, environmental protection, and agroforestry production [21]. The diversity and community distribution of leafhoppers in karst rocky desertification areas are closely related to the ecological environment [20]. Exploring the community structure and biodiversity of leafhoppers in karst areas not only enriches the Cicadellidae species data but also helps in monitoring and evaluating environmental change trends and ecological restoration effects in different grades of rocky desertification areas [22]. Habitat conditions, such as plant traits, climatic characteristics, and soil conditions, obviously differ among karst habitats, but it is not clear how these affect the spatial distribution and community characteristics of leafhoppers. In order to establish the effects of environmental differences on leafhoppers, this study analyzed the community structure and diversity characteristics of typhlocybinae on host plants in different regions with different grades of karst rocky desertification. The response mechanisms of typhlocybinae to environmental changes are discussed so as to provide basic information and a theoretical basis for rocky desertification management in karst areas.

2. Materials and Methods

2.1. Study Sites

With reference to the standard classification of rock desertification [23], three typical karst regions in Guizhou were selected as study areas: the Huajiang Demonstration Zone (Huajiang), the Bijie Salaxi Demonstration Zone (Bijie), and the Shibing Yuntai Mountain Nature Reserve (Shibing). Within these areas, different climatic conditions, vegetation types, rocky desertification grades, and other habitat conditions are present (Figure 1). The sampling sites were geographically distant, and in all of them, areas with strong anthropogenic disturbance were avoided.

The Huajiang Demonstration Zone (105°34′59″–105°43′06″ E, 25°37′18″–25°42′37″ N) is located along the Beipan River in southwestern Guizhou Province. The altitude is approximately 400–1400 m, the average annual temperature is approximately 16 °C, and the average annual precipitation is 1100 mm. It has a subtropical dry and hot valley climate [24]. The vegetation is dominated by broad-leaved forests, mixed coniferous and broad-leaved forests, and shrubs. As a result of long-term soil erosion in the region, the base rock in the demonstration area is exposed, with an area of more than 70%, which belongs to moderate–severe rocky desertification [25,26].

The Bijie Salaxi Demonstration Zone (105°01′11″–105°08′38″ E, 27°11′09″–27°17′28″ N) is located in the Liuchong River Basin, Qixingguan District, northwestern Guizhou Province. The altitude is approximately 1500~2200 m, the average annual temperature is approximately 13 °C, and the average annual precipitation is 984.40 mm. It has a northern subtropical humid monsoon climate [27]. The vegetation is dominated by broad-leaved forests, coniferous forests, and shrubs [28]. Because of the influence of human factors, most of the native vegetation has been destroyed; thus, vegetation coverage is low. Therefore, it is an area characterized by light–moderate rocky desertification [29].

The Shibing Yuntai Mountain Nature Reserve (108°01′36″–108°10′52″ E, 27°13′56″–27°04′51″ N) is located in the upper middle part of the Wuyang River Basin in Shibing County, central–eastern Guizhou Province. The altitude is approximately 600–1250 m, the average annual temperature is approximately 16 °C, and the average annual precipitation is 1060–1200 mm. It has a mid-subtropical warm and humid climate [30,31]. The area has a mild climate and abundant rainfall, with lush vegetation [32]. It is a typical karst forest ecosystem and a without-potential rocky desertification area [33].

2.2. Sample Setup and Sampling

On the basis of the plant species in the three study areas, samples were collected once a month in September 2020 and May and July 2021, on a total of nine occasions. Five widespread host plants were selected: Juglans regia L., Rhus chinensis Mill., Prunus persica (L.) Batsch., Prunus salicina Lindl., and Debregeasia orientalis C.J. Chen. One sample plot was selected for each host plant in each study area based on the habit and environmental conditions of typhlocybinae, for a total of 15 sample plots (

Table 1. Overview of the sample plots.

Study Areas	Host Plant	Altitude (m)	Latitude	Longitude
	Juglans regia	1200	25°42′29″ N	105°36′50″ E
	Rhus chinensis	1280	25°41′36″ N	105°37′46″ E
Huajiang	Prunus persica	1193	25°40′43″ N	105°38′57″ E
	Prunus salicina	1190	25°37′43″ N	105°41′8″ E
	Debregeasia orientalis	1240	25°39′56″ N	105°38′1″ E
	Juglans regia	1960	27°14′5″ N	105°5′51″ E
	Rhus chinensis	1760	27°14′43″ N	105°6′16″ E
Bijie	Prunus persica	1959	27°15′49″ N	105°5′13″ E
	Prunus salicina	1766	27°14′51″ N	105°5′52″ E
	Debregeasia orientalis	1700	27°13′25″ N	105°5′47″ E
	Juglans regia	950	27°2′39″ N	108°7′23″ E
	Rhus chinensis	952	27°2′53″ N	108°7′25″ E
Shibing	Prunus persica	1000	27°12′48″ N	108°11′5″ E
	Prunus salicina	1140	27°13′35″ N	108°1′54″ E
	Debregeasia orientalis	912	27°7′51″ N	108°2′27″ E

). Four host plants of the same species with a uniform height were selected for leafhopper specimen sampling in each plot. Sampling was performed during the warmer hours of the day (between 9:00 and 18:00), on a sunny day between the 25th and 30th days of the month. In the case of rain, sampling was postponed for one day. The samples were always collected by the same person.

Specimens were collected using the sweeping method: a net with a diameter of 30 cm, a depth of 50 cm, and a rod length of 150 cm was swept back and forth on the host plant. In order to avoid the flight of leafhoppers, after 15 sweeps of each plant, the leafhoppers were collected with a centrifuge tube with a diameter of 1.5 cm containing absolute ethanol. Collection was performed on each plot three times, with 60 nets at a time, for a total of 180 nets. For this process, the collector held and tightened the middle of the net with one hand so that the leafhopper was at the bottom of the net, and then they extended the centrifuge tube into the net to collect the insect. During the collection process, dead leafhoppers at the bottom of the net were collected into a centrifuge tube using a brush. Leaf specimens were collected from 6–15 healthy unbroken leaves (the number of samples depended on the size of the leaves) growing on the sunny side of the plant. Then, they were stored in sealed bags, placed in a portable minifridge together with the leafhopper specimens, and maintained at a temperature below 5 °C. The samples were brought back to the laboratory and immediately placed in a 4 °C fridge. After each sample collection, labels were produced to record the geographical coordinates, temperature, humidity, elevation, and vegetation type of the sample site (Table 1 and Figure 2). Altitude, longitude, and latitude were measured and recorded using a GPSmap60CSx meter, and temperature and humidity were measured and recorded using a TASITA622A meter.

2.3. Sample Identification

In the laboratory, male typhlocybinae specimens were sorted from leafhopper specimens, and the abdomens were removed and soaked in a 5–10% NaOH solution for 8–12 h. After being washed with water, the genitals were dissected under an Olympus SZX16 stereoscope to observe their characteristics and identify the specimens according to the 3I Interactive Keys and Taxonomic Databases (http://dmitriev.speciesfile.org/, accessed on 1 August 2021) and the leafhopper taxonomy-related literature [34,35,36,37]. All specimens were deposited in the Cicadellidae specimen room, the School of Karst Science, Guizhou Normal University.

2.4. Species Diversity Analysis

Six leaves of similar size were selected from each host plant, and their blade length (BL), maximum blade width (BW), and blade thickness (BT) were measured using a vernier caliper (EDHG-300-IP54). The fresh weight (FW) of the leaves was measured using an electronic balance (AXA-C3-6553), and then the leaves were put into an oven at 105 °C for 30 min. After drying at 70 °C to a constant weight, the dry weight (DW) was measured, and the leaf water content (LWC) was calculated [38] as follows:

$$LWC(\%)=\frac{FW-DW}{FW}\times 100\%$$

(1)

where FW is the fresh weight, and DW is the dry weight.

A statistical analysis of the collected leafhopper specimens was carried out to determine the dominant species using the relative frequency. More than 5% of the total catch according to the number of individuals indicated the dominant taxa (+++), 1~5% of the total catch according to the number of individuals indicated the common taxa (++), and less than 1% of the total catch according to the number of individuals indicated the rare taxa (+) [39].

The Shannon–Wiener diversity index (H’) [40], the Margalef species richness index (R) [41], Pieluo’s uniformity index (J’) [42], and the Simpson dominance index (C) [43] were used to analyze the typhlocybine leafhopper community structure diversity. Before the correlation analysis, a detrended correspondence analysis (DCA) was performed using species data [44]. The gradient length value was 0.35, so RDA was selected (if the gradient length was greater than 4.0, CCA was selected, and if the gradient length was lower than 3.0, RDA was selected). A redundancy analysis (RDA) of the leafhopper biodiversity indices (the number of genera (GN), the number of species (SN), the number of individuals (IN), the Shannon–Wiener diversity index (H’), the Margalef species richness index (R), Pieluo’s uniformity index (J’), and the Simpson dominance index (C)) and the corresponding environmental factors (temperature (T), humidity (H), days of precipitation (PD), host plant blade length (BL), blade width (BW), and leaf water content (LWC)) in the study areas were used to establish the main factors influencing the community structure of typhlocybine leafhoppers. The data analysis was completed and visualized using Microsoft Excel 2016, SPSS 22.0, and Canoco 5 [45,46,47]. All 41 genera of the leafhopper groups were selected for a chord diagram using R 4.1.3 “circlize” packages [48].

$$H’=-{\displaystyle \sum _{i=1}^S{p}_i}\ln p_i,p_i=N_i/N$$

(2)

$$R=(S-1)/\ln N$$

(3)

$$J’=H’/\ln S$$

(4)

$$C={\displaystyle \sum _{i=1}^S\left(N_i/N\right)}$$

(5)

Here, N_i is the number of individuals of species i, N is the total number of individuals, and S is the total number of species.

3. Results

3.1. Environmental Variables

The mean temperature in the three study areas was in the order of July > September > May, and the monthly average temperature was significantly lower in Bijie than in Huajiang and Shibing (

Table 2. Climate data in each plot ((JR): Juglans regia, (RC): Rhus chinensis, (PP): Prunus persica, (PS): Prunus salicina, and (DO): Debregeasia orientalis).

Month	Host Plants	Huajiang			Bijie			Shibing
		Temperature (°C)	Humidity (%)	Precipitation Days	Temperature (°C)	Humidity (%)	Precipitation Days	Temperature (°C)	Humidity (%)	Precipitation Days
September	JR	22.70	74.68	22	19.79	80.57	24	24.16	78.46	22
	RC	24.94	69.47	22	19.14	82.00	24	24.03	77.57	22
	PP	23.05	72.58	22	19.78	80.26	24	23.4	77.15	22
	PS	23.00	72.59	22	19.69	80.97	24	23.74	77.10	22
	DO	24.25	70.86	22	19.48	81.46	24	23.36	77.05	22
May	JR	21.48	70.97	13	16.71	79.62	24	19.96	83.48	23
	RC	23.21	69.46	13	16.23	78.48	24	19.25	82.66	23
	PP	22.55	69.88	13	16.01	78.37	24	19.00	83.30	23
	PS	22.51	69.72	13	16.77	78.24	24	19.21	82.42	23
	DO	22.74	69.11	13	16.50	77.73	24	19.24	82.45	23
July	JR	25.29	80.78	19	22.82	81.37	12	27.92	78.68	10
	RC	27.21	77.52	19	20.12	79.48	12	27.12	78.02	10
	PP	24.11	78.63	19	20.11	80.25	12	26.12	77.67	10
	PS	24.14	78.35	19	21.67	79.24	12	26.37	77.24	10
	DO	24.51	77.56	19	20.45	79.14	12	27.00	77.38	10

). It can be seen in Figure 2 that there were differences in days with humidity and in the three study areas. The air humidity in May and July was in the order of Shibing > Bijie > Huajiang, while in September, the highest humidity was in Bijie, followed by Shibing and Huajiang. In September, there was no obvious difference in days with precipitation in the three study areas. In May, the most days with rainfall occurred in the Huajiang study area, while July exhibited the opposite trend.

The monthly variation in the host plant blade length in the three study areas was in the order of July > September > May (Figure 3a). The host plants in the Huajiang study area had the longest blade length as compared with those in the other study areas, while the blade width was the lowest (Figure 3b). As a result of the low temperature and weak evapotranspiration, the leaf water content was slightly higher in Bijie than in the other two study areas. The water content of the host plant leaves in different months was in the order of May > September > July, contrary to the change in temperature (Figure 3c).

3.2. Typhlocybinae Community

A total of 4078 typhlocybinae specimens were captured in the three study areas, belonging to 6 tribes, 40 genera, and 121 species. The statistical analysis showed that (Supplementary Materials Table S1), in terms of species composition, Empoascini, Zyginellini, Typhlocybini, and Erythroneurini were more abundant in the study areas, with the number of individuals accounting for approximately 99.0% of the total, while Alebrini and Dikraneurini accounted for less than 1.0%. In terms of the composition of the various genera of typhlocybine leafhoppers (Figure 4), individuals representing Alnetoidia, Limassolla, Empoasca, and two others were dominant; 8 genera, including Tautoneura, Aguriahana, and Zyginella, were common; and the remaining 26 genera were rare, including Typhlocyba and Baaora. The dominant, common, and rare groups among the total number of typhlocybine leafhoppers genera accounted for 12.8, 20.5, and 66.7%, respectively (Figure 5a). The total number of individuals among typhlocybine leafhoppers accounted for 70.3, 22.9, and 6.8%, respectively. In terms of species (Figure 5b), A. dujuanensis, L. lingchuanensis, and S. shinshana were dominant in the three study areas, accounting for 45.4% of the total number of individuals. Fifteen species, including E. rybiogon, Z. minuta, and T. unicolor, were common, accounting for 37.2% of the total number of individuals. Aguriahana triangularis, T. babai, and 103 other species were rare, accounting for 17.4% of the total number of individuals. The dominant, common, and rare species among the total number of typhlocybine leafhopper species accounted for 2.5, 12.4, and 85.1%, respectively. It is clear that the proportions of rare genera and species were relatively high and that those of dominant genera and species were lower in the three study areas.

In the study area, the numbers of individuals were as follows: Shibing: 2170 leafhoppers, 53.2%; Bijie: 973 leafhoppers, 23.9%; and Huajiang: 935 leafhoppers, 22.9%. The order of the number of taxonomic levels was as follows: Bijie (6 tribes, 32 genera, and 68 species) > Huajiang (6 tribes, 22 genera, and 58 species) > Shibing (5 tribes, 21 genera, and 48 species) (Figure 6). In terms of time, the distribution was in the order of July > May > September, and the number of taxonomic levels was in the order of May (6 families, 29 genera, and 61 species) > September (6 tribes, 21 genera, and 64 species) > July (4 tribes, 21 genera, and 64 species).

From the first site (Huajiang), a total of 935 typhlocybinae specimens were collected, with numbers in the following order: J. regia (411 individuals, 44.0%) > P. persica (174 individuals, 18.6%) > D. orientalis (139 individuals, 14.75%) > P. salicina (134 individuals, 14.3%) > R. chinensis (77 individuals, 8.2%). In terms of genus, the proportions of dominant, common, and rare genera in the Huajiang study area were 31.8, 31.9, and 36.3%, respectively. In terms of species, the dominant species in Huajiang were A. agrillacea, A. juglandis, Zorka agnesae, and Z. minuta collected from J. regia; S. shinshana collected from P. persica; and A. suzukii and A. remmi collected from P. salicina, from a total of 490 samples, accounting for 52.4% of the total number of individuals. Fourteen species, including E. rybiogon and A. dujuanensis, were common, with 336 samples, accounting for 35.9% of the total number of individuals. Aguriahana tripoda, Dayus takagii, and 37 other species were rare, with 109 samples, accounting for 11.7% of the total number of individuals.

From the second site (Bijie), a total of 973 typhlocybinae specimens were collected: J. regia: 323 individuals, 33.2%; D. orientalis: 208 individuals, 21.8%; P. persica: 177 individuals, 18.2%; R. chinensis: 140 individuals, 14.4%; and P. salicina: 116 individuals, 11.9%. In terms of genus, the proportions of dominant, common, and rare genera in Bijie were 22.3, 30.0, and 47.7%, respectively. In terms of species, E. rybiogon, Alebroides dworakowskae, and seven other species were dominant, with 514 samples, accounting for 52.8% of the total number of individuals. Agnesiella juglandis, A. dujuanensis, and 13 other species were common, with 334 samples, accounting for 34.3% of the total number of individuals. A. agrillacea, Empoascanara sipra, and 48 other species were rare, with 125 samples, accounting for 12.9% of the total number of individuals.

From the third site (Shibing), a total of 2170 typhlocybinae specimens were collected: J. regia: 1140 individuals, 52.5%; R. chinensis: 550 individuals, 25.3%; P. persica: 202 individuals, 9.3%; D. orientalis: 169 individuals, 7.8%; and P. salicina: 109 individuals, 5.0%. In terms of genus, there were fewer dominant and common genera in Shibing and more rare genera, accounting for 19.0, 23.8, and 57.2% of the total genera, respectively. In terms of species, A. dujuanensis, L. lingchuanensis, and S. shinshana were dominant, accounting for 44.5, 21.1, and 8.2% of the total number of individuals, respectively. A. juglandis, E. rybiogon, and eight other species were common, with 383 samples, accounting for 17.6% of the total number of individuals. Finally, 37 species, including A. agrillacea and Arboridia echinata, were rare, with 185 samples, accounting for 8.6% of the total number of individuals.

3.3. Diversity Analysis

3.3.1. Community Diversity Analysis of Typhlocybinae in Different Study Areas

On the basis of the statistical results (Figure 7), the community diversity analysis of the specimens from the three study areas showed that the Shannon–Wiener diversity index (H’) and the Margalef species richness index (R) were in the order of Bijie > Huajiang > Shibing. The Shannon–Wiener diversity index (H’) and the Margalef species richness index (R) were very similar for Bijie and Shibing, and their values for Shibing were significantly lower, indicating a low community diversity and biota species richness in Shibing. Pieluo’s uniformity index (J’) showed that Huajiang was relatively uniform, followed by Bijie, and Shibing was the most heterogeneous. The Simpson dominance index (C) for Huajiang and Bijie was low, and the values were relatively similar, while the C value for Shibing was significantly higher. This was due to the large number of A. dujuanensis and L. lingchuanensis individuals in Shibing, which have a clear advantage in the study area.

3.3.2. Community Diversity Analysis of Typhlocybinae in Different Host Plants

On different host plants (Figure 8), the spatial distribution of the species richness index (R) was in the order of P. salicina > D. orientalis > P. persica > J. regia > R. chinensis; the uniformity index (J’) was in the order of D. orientalis > P. salicina > P. persica > J. regia > R. chinensis; and the dominance index (C) was in the order of R. chinensis > J. regia > P. persica > P. salicina > D. orientalis. The highest diversity of typhlocybinae was found on P. salicina, followed by D. orientalis, P. persica, J. regia, and R. chinensis. The evenness of typhlocybinae on the five host plants was negatively correlated with dominance, indicating that the more prominent the dominant species, the lower the species evenness.

3.4. Correlation Analysis

The main environmental factors, including temperature, humidity, and precipitation days, were measured in the sample area of the study area. A redundancy analysis (RDA) was used to analyze the data of biological factors, including genus, species, individual number, and diversity index, and the geographic environmental factors, including climate and vegetation, so as to explore the main environmental factors affecting the occurrence and reproduction of typhlocybine leafhoppers in the study area.

The first and second axes of RDA (Figure 9A) explained 95.39% of the relationship between the community structure of the leafhoppers and the geographic environmental factors in the study areas. It can be seen that the geographical factors in the study areas had an obvious influence on the community and diversity of the leafhoppers. The results show that temperature (T), precipitation days (PD), and host plant blade width (BW) and blade length (BL) had a significant influence on typhlocybine leafhopper species diversity, while humidity (H) and plant water content (LWC) had a smaller effect (Figure 8). BW and BL were positively correlated with genus number (GN), species number (SN), individual number (IN), the Margalef species richness index (R), and the Simpson dominance index (C), but they were negatively correlated with Pieluo’s uniformity index (J’) and the Shannon–Wiener diversity index (H’). Temperature (T) was positively correlated with the number of individuals (IN) and C, while the remaining indices were negatively correlated. The correlation between PD and each environmental factor exhibited an opposite trend to the correlation between T and each environmental factor. PD had a negative correlation with IN and C and a positive correlation with the other indices.

The order of the cumulative interpretation rate from the redundancy analysis in the three study areas was Huajiang > Bijie > Shibing. This indicates that the community structure of leafhoppers in Huajiang and Bijie is easily affected by environmental factors, while the typhlocybinae community structure in Shibing is less affected by environmental factors. This is consistent with the ranking of rocky desertification in the three study areas. In the Huajiang study area, the first and second RDA axes explained 80.43% and 16.43% of all the information, respectively, for a total of 99.40%. The leafhopper species diversity was mainly affected by climate (H, T) and leaf length (Figure 9B). On the second site (Bijie), the first and second axes explained 77.61% and 20.27% of the relationship between typhlocybinae leafhopper diversity and environmental factors, respectively (Figure 9C). The leafhopper species diversity was mainly affected by temperature (T), precipitation days (PD), leaf width (BW), and leaf length (BL). On the third site (Shibing), the first axis interpretation rate was 90.91%, and the second axis interpretation rate was 6.14% (Figure 9D). Except for humidity and leaf water content, the other environmental factors had a greater influence on the community structure of the leafhoppers. In general, in the niches of the different study areas, the environmental factors other than LWC had obvious effects on the community structure of leafhoppers.

4. Discussion

On the basis of the field collection data, the temporal and spatial dynamics of typhlocybinae in the study areas were obtained. The results show that there were some differences in the typhlocybine leafhopper species collected in the different study areas and different months. In contrast, leafhopper species in the same study area were highly consistent, which is consistent with the collected data from the field sampling of other leafhopper insects [49,50]. That is to say, the community structure and diversity of leafhoppers differ with changes in ecological environment conditions.

Environmental factors, such as soil, vegetation, topography, altitude, and latitude, in different geographic environments can have an impact on insect species diversity [51]. In this study, the factors affecting the species diversity of typhlocybinae communities in the different ecological landscapes differed. The influence of the geographic environment on the population structure of typhlocybine leafhoppers in the three study areas was in the order of Huajiang > Bijie > Shibing, which is consistent with the classification of rocky desertification. In other words, the more serious the rocky desertification, the more fragile the ecological environment and the greater the impact on the population structure and biodiversity of typhlocybine leafhoppers. This confirms that habitat fragmentation and vegetation degradation are important indicators of rocky desertification in the karst region centered on the Yunnan–Kweichow Plateau, and with the degradation of vegetation, biomass also decreases [52]. Therefore, in areas suffering from more serious rocky desertification, the number of plant-eating leafhoppers also decreased. It can be seen that ecological landscape attributes largely determine the species diversity of organisms [53]. The species diversity of typhlocybine leafhoppers is affected by the environment to a higher degree in more ecologically fragile situations. In a study of insect diversity on old experimentally fragmented farmland in northeastern Kansas, USA, Edward found that the more fragmented the ecosystem, the lower the insect richness, which is consistent with the findings of the present study [54]. Therefore, insects can be used as indicator organisms to monitor the fragile ecological environment. Moreover, data from these studies can help provide ecological restoration suggestions and a basis for governance [55].

The temporal distribution of the influence of the geographic environment on typhlocybine leafhoppers in the three study areas was in the order of May > July > September, mainly due to changes in climate and vegetation in different seasons. The temperature in each study area was low in May, and the climate in Huajiang was dry and hot in July. The climatic factors in these two months restricted the reproduction of typhlocybinae, so the geographic environment had a great influence on the diversity of the leafhopper community. In September, the temperature and humidity in the study area were suitable, and the influence on the diversity of the leafhopper community was weakened. The distribution of the number of leafhoppers in the three study areas was in the order of July > May > September. Orthopterans are often thermophilic and particularly sensitive to temperature changes, which is in accordance with the results of this study [56,57]. In fact, climatic factors, such as humidity, temperature, and precipitation, are affected by latitude, longitude, altitude, and aspect, so the relationship between climate and leafhopper species richness is complex [58,59]. In addition, plant diversity varies from season to season, and plant diversity affects insect diversity [60].

There was a high correlation between plant and insect diversity [61]. In terms of different host plants, plants as hosts and food sources for leafhoppers had the strongest influence on typhlocybinae community diversity compared to the other environmental factors, while on the same host plants, precipitation days and temperature were the main factors affecting species diversity. Insects select specific habitats according to their feeding preferences, so the dominant species on different host plants differ [62]. Leafhoppers are small and do not easily migrate. Some leafhoppers parasitizing tall trees will live on the host plant their entire lives [18]. Therefore, plant species determines which leafhopper species appear in a site [63]. Many studies on the relationship between leafhoppers and plants have shown that there is a positive correlation between host plants and leafhopper species richness [64,65,66]. In addition, leafhopper species can adapt to multiple dominant host plants [67,68]; for example, S. shinshana, which can live on P. persica and P. salicina, was significantly dominant in the study area.

Numerous studies of insect species diversity and the environment show a high correlation between insect species diversity and climatic factors [69,70]. However, for leafhoppers, there is a high correlation between host plants and community species diversity in terms of both their temporal and spatial distributions. This is the same conclusion as that reached by Zhang and Feng (2018) in their study of insect diversity in Inner Mongolia [71]. Climate factors also have some influence on the species diversity of typhlocybinae, but to a relatively small extent [59]. Yuan (2014) reached the same conclusion in a study of typhlocybinae from 11 regions in central and southern China. In that study, it was found that latitude and altitude had a greater effect on the total and endemic species richness of typhlocybinae, while temperature and humidity had a smaller effect. Altogether, these results suggest that habitat quality, especially plant traits and species, plays an important role in the community composition and diversity of phytophagous leafhoppers compared to climate.

5. Conclusions

In this study, the community structure and species diversity of typhlocybine leafhoppers on different plants in three karst rocky desertification areas of Guizhou were investigated. The diversity of the typhlocybine leafhopper community structure and its correlation with the geographic environment in different rocky desertification areas were determined. The results show that there were differences in the number, species, and diversity of leafhoppers in different grades of rocky desertification under different ecological environments. Therefore, changes in the biomass and species of leafhoppers, as an abundant insect with a rich species diversity, can reflect the evolution of regional geographic environments and provide a reference for ecological restoration in fragile areas. This research only revealed the response of leafhoppers to changes in the surrounding environment to a certain extent. The main biological and nonbiological factors affecting the formation and distribution of insect communities in different grades of karst rocky desertification areas need further exploration and research.