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. 2021 Nov 8;12(11):1002. doi: 10.3390/insects12111002

Morphological Adaptation of Cave-Dwelling Ground Beetles in China Revealed by Geometric Morphometry (Coleoptera, Carabidae, Trechini)

Mengzhen Chen 1,†, Wanru Guo 1,†, Sunbin Huang 1,2, Xiaozhu Luo 1,3, Mingyi Tian 1,*, Weixin Liu 1,*
Editor: Markus Friedrich
PMCID: PMC8623905  PMID: 34821802

Abstract

Simple Summary

Cavernicolous ground beetles dwelling in China are one of the most diverse and underground-adapted coleopteran group in the world. The tribe Trechini is, among them, the most representative group constituting over 170 known species with a narrow and elongated body and long appendages or a stout body and short appendages. However, very little information about their morphology has been explored. The aim of this study was to analyze the morphological adaptations of this group using geometric morphological methods. The beetles were divided into four different morphological types, including aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling, and the analysis is based on the morphology of their head, pronotum, and elytra. Our findings indicate that the overall morphological variation of cave trechine beetles has gradually specialized from an anophthalmic to semi-aphaenopsian to aphaenopsian type. Different types have different directions of variation in the head, pronotum, and elytra, but the pronotum is more differentiated and morphologically diverse than the head and elytra.

Abstract

Cave-dwelling ground beetles in China represent the most impressive specific diversity and morphological adaptations of the cavernicolous ground beetles in the world, but they have not been systematically examined in quantitative terms. The present study focuses on the application of geometric morphological methods to address the morphological adaptations of the tribe Trechini, the most representative group in China. We have employed a geometric morphometry analysis of the head, pronotum, and elytra of 53 genera of Trechini, including 132 hypogean and 8 epigean species. Our results showed that the overall morphological variation of cave carabids has gradually specialized from an anophthalmic to semi-aphaenopsian to aphaenopsian type. There were extremely significant differences (p < 0.01) among four different adaptive types including aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling Trechini when their adaptability to a cave environment was used as the basis for grouping. Furthermore, there were differences in the phenotypic tree of the head, pronotum, and elytra, and an integrated morphology. To the best of our knowledge, this is the first report on the analysis of the head, pronotum, and elytra of four different adaptive types of ground beetles in order to clarify the morphological adaptations of cavernicolous carabids to the cave environment.

Keywords: adaptive type, cave environment, morphological variation, phenotypic development

1. Introduction

China is very rich in cave-dwelling ground beetles. At present, 202 species of cave carabids belonging to 8 tribes and 71 genera have been recorded, among which the Trechini is the most diverse group including 175 species from 63 genera [1,2]. All of them are troglobionts and completely lack eyes, except for four troglophiles with more or less degenerated eyes [3]. In addition to the disappearance of their eyes, cavernicolous carabids underwent morphological modifications during long-term adaptation to the subterranean environment. These are manifested in the loss of pigment and metathoracic wings, as well as their more slender body and thin legs [4,5]. According to the adaptability of characteristic appearances and biological information, cave trechine beetles were divided into three morphological types [6,7,8]: aphaenopsian, semi-aphaenopisan, and anophthalmic (Figure 1). The former means that these carabids have an extreme elongation of their body and appendages, while the latter refers to their stout body and shorter appendages. The semi-aphaenopsian is considered to be a transitional type, with morphological characteristics lying between the above two. The surface-dwelling trechine beetles have darker body color and compound eyes (Figure 1).

Figure 1.

Figure 1

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Morphological characteristics of four different adaptive types of ground beetles. (a) Surface-dwelling (Sinotrechiama yunnanus); (b) anophthalmic (Sinotroglodytes yanwangi); (c) semi-aphaenopsian (Aspidaphaenops dudou); and (d) aphaenopsian (Giraffaphaenops clarkei).

Geometric morphometry is an approach that relies on the quantitative analysis of the geometry of the target structure and the further performance of statistical analyses [9]. Different types of data, such as landmark coordinates, outline curves, and surfaces are used to define the shape [10]. The original morphological information is usually obtained through Cartesian coordinates, which are used to remove the interference of non-morphological variation in the analysis so that the punctuation overprint analysis of all samples can be visualized and displayed [11]. Geometric morphometry began to be used in the 1980s, and in the 21st century it has been widely used in entomology, medicine, archaeology, and other fields [12,13,14]. Recently, geometric morphometry has developed from two-dimensional to three-dimensional. Three-dimensional scanning, electron microscope scanning, micro-CT scanning, etc., provide advanced technical support for the development of geometric morphometry [15,16,17].

The application of geometric morphometry to coleopteran insects is very extensive. It is often used to explore morphological differences between species with sexual dimorphism [18,19], intersubspecies, sister groups [20,21], and high-level categories [22,23]. It is also possible to infer the ancestral form of an existing taxa in order to study its origin and evolution [24]. Geometric morphometry has gradually been applied to different groups of Coleoptera, including Carabidae [25,26,27], Lucanidae, Chrysomelidae [28], Scarabaeidae [29,30,31], and Silphidae [32]. However, studies of the geometric morphometry of cave-dwelling ground beetles have rarely been reported [33].

Based on a geometric morphometric approach, the present paper provides, for the first time, an analysis of the head, pronotum, and elytra of four different adaptive types of ground beetles in order to clarify the morphological adaptations of cavernicolous carabids to the cave environment. In addition, the phenotypic relationship was obtained with a clustering analysis in the genetic category to explore the morphological evolution of cave-dwelling ground beetles.

2. Materials and Methods

2.1. Studied Materials

For the materials used in this study, we implemented the following principles: (1) Sampling as many genera and species as possible, including type species. (2) We did not deal with subgenus separately; species taxonomic treatment was based on the latest publications. (3) We used bibliographic data to obtain the morphological adaptation types of known taxa, e.g., [34,35,36,37,38].

A total of 140 species in 53 genera of Trechini (49 genera and 132 species from caves and 4 genera and 8 species of surface-dwelling beings) were examined in this study (Table A1). Among them, 97 specimens were deposited at South China Agricultural University, e.g., [39,40,41].

2.2. Geometric Morphometric Approach

2.2.1. Image Acquisition

Photographs of existing samples were taken with a Keyence VHX-5000 digital microscope (Figure S1). Due to the lack of specimens for 44 species, images were obtained from related original literature, e.g., [42,43,44] (Figure S1). For Minimaphaenops (Enshiaphaenops) senecali Deuve, 2016, we gathered the data from the specimen we collected as well as the additional figure of the type specimen from the original publication. After editing using Adobe Photoshop CS6, we imported the data into tps-Util 1.78 [45].

2.2.2. Landmark Data

The shape of the head, pronotum, and elytra and the positions of stable pores on the elytra were chosen as morphological indicators. We selected the configurations of 50 semilandmarks of each object, except for the stable pores on the elytra, which were represented by 6 landmarks (Figure 2). The landmarks and semilandmarks in each image were digitized using the tps-Dig 2.31 software (Landmark Data S1). The Tps-Small 1.34 software [46] was used to detect the data correlation of the.tps files after the landmarks to verify whether the data correlation met the requirements.

Figure 2.

Figure 2

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Landmark and semilandmark configurations of ground beetle specimens. (a) The right side of the head (50 positions); (b) right side of the pronotum (50 positions); and (c) right side of the elytra (56 positions).

2.2.3. Statistical Analysis

The morphological data obtained by the standardized processing of different cave environment-adapted types were imported into the MorphoJ 1.07A software. Generalized Procrustes Analysis (GPA) was used to perform Procrustes superimposition on the overall samples to extract shape variables [47,48]. We used calculational processing to ensure that the sum of the squares of the distances between landmarks of the same serial number was minimized. Additionally, we calculated the overall average shape to compare the degree of difference between the individual and overall average shape (measured by Procrustes distance). On this basis, we applied principal component analysis (PCA).

We selected the first two principal components (PC) to construct scatterplots to show the morphological differences of carabids in different cave environment adaptation types. An energy map of the extreme points of the coordinate origin arrangement was obtained from a thin-plate spline (TPS) analysis using the MorphoJ 1.07A software, where differences in the landmarks were displayed in a visual form.

On the basis of PCA, we set the different cave environment adaptation types as the basis for grouping and performed canonical variate analysis (CVA). The results were displayed through the Mahalanobis distance and Procrustes distance.

2.2.4. Clustering Analysis

The original TPS file was split into 53 subfiles according to genera using the tps-Util 1.78 software; then we used the tps-Super 2.05 software to calculate the average form of each genus. Procrustes distances between genera were preformed using the tps-Small 1.34 software; then we used the unweighted group averaging method (UPGMA) in the NTSYSpc 2.10e software [49] to analyze the Procrustes distance matrix.

3. Results

3.1. Internal Correlation of the Original Data

The original data were converted from camber Kendall space to Euclidean tangent space. For the head, pronotum, and elytra, the correlation coefficients of the data before and after the conversion were 0.999995, 0.999992, and 1.000000, respectively, which met the requirements.

3.2. PCA of the Morphological Variation in Head, Pronotum and Elytra

Principal component analysis was performed on the morphological data of the head, pronotum, and elytra for 141 species of carabid beetles, with 96, 96, and 108 principal components being obtained, respectively. Among them, the first principal component (PC1) accounted for 89.86%, 84.95%, and 39.35% of the overall variance, while the second principal component (PC2) accounted for 3.94%, 7.75%, and 27.20%, respectively. Using PC1 and PC2, which affect the morphological variation, as the abscissa and ordinate, respectively, a scatterplot of the morphological variation was obtained, and a 90% equal frequency ellipse was constructed based on the cave adaptation type of these carabid beetles (Figure 3a,c,e).

Figure 3.

Figure 3

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Principal component analysis (PCA) of four different adaptive types of ground beetles: (a,b) head; (c,d) pronotum; (e,f) elytra. (a,c,e) represent scatterplot; (b,d,f) represent the energy map.

From the perspective of the morphological variation of the head (Figure 3a) and pronotum (Figure 3c), it was found that the aphaenopsian had no overlap and could be distinguished well from anophthalmic and surface-dwelling carabid beetles. The semi-aphaenopsian carabid beetle type was between the aphaenopsian and anophthalmic types and was more similar to the anophthalmic type because of its larger overlaps. The latter was closer to the surface-dwelling carabid beetles. Regarding the morphological variation of the elytra (Figure 3e), these four types overlapped more overall. No significant differences were found between elytra of the semi-aphaenopsian, aphaenopsian, and anophthalmic types.

The energy map of the coordinate origin and the extreme points of the PCA scatterplot of carabid beetles’ head, pronotum, and elytra (Figure 3b,d,f) show that the length/width ratio of the head and pronotum has a tendency to decrease significantly, while their lateral edges expand outward in the positive direction of PC1. The widest point of the head moves to the front, but the front edge of the pronotum tends to be wider than the rear edge. Elytra tend to be more slender and the scutellum appears to be narrower. The anterior of the edge side of the elytra has a tendency to undergo adduction, with the shoulders disappearing and the position of the hair pores moving to the distal end of the elytra. In the positive direction of PC2, the posterior edge of the head is sunken inward and the front and caudal corners of the pronotum tend to become acute from an obtuse angle. The first four elytra hair pores are more scattered and the last three are closer together.

3.3. CVA of the Morphological Variation in Head, Pronotum, and Elytra

According to the results of the PCA, CVA was used to analyze the morphological variation in the distances of the head, pronotum, and elytra among all the genera of carabid beetles. The results showed that the Mahalanobis distance and Procrustes distance between aphaenopsian and surface-dwelling types were largest when adaptability to a cave environment was used as the basis for grouping. For the head, pronotum, and elytra, the maximum Mahalanobis distance (Table 1) was 28.5719, 20.8313, and 20.7926, respectively, while the maximum Procrustes distance (Table 2) was 0.3429, 0.3258, and 0.1032, respectively.

Table 1.

Mahalanobis distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.

Aphaenopsian Semi-Aphaenopsian Anophthalmic
Semi-aphaenopsian 11.1596//8.9433//12.6030
Anophthalmic 13.9436//10.7282//15.3457 6.6324//7.6456//7.0232
Surface-dwelling 28.5719//20.8313//20.7926 23.0163//16.3761//18.8595 22.5005//16.7463//16.2172
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Table 2.

Procrustes distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.

Aphaenopsian Semi-Aphaenopsian Anophthalmic
Semi-aphaenopsian 0.1319//0.1409//0.0516
Anophthalmic 0.2451//0.2342//0.0854 0.1227//0.0995//0.0485
Surface-dwelling 0.3429//0.3258//0.1032 0.2275//0.1981//0.0644 0.109//0.101//0.0589
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The Mahalanobis distance (Table 3) and Procrustes distance (Table 3) of the head, pronotum, and elytra were tested to determine the significance of the differences. It was shown that the four different types (aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling carabid beetles) had high significant differences from each other (p < 0.01).

Table 3.

P-values of the differences in Mahalanobis and Procrustes distances for the four adaptive types of ground beetles (10,000 permutation test, consistent for the head, pronotum, and elytra).

Aphaenopsian Semi-Aphaenopsian Anophthalmic
Semi-aphaenopsian <0.0001
Anophthalmic <0.0001 <0.0001
Surface-dwelling <0.0001 <0.0001 <0.0001
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3.4. The Phenotypic Evolutionary Relationship between Cave Trechini Genera

Based on the Procrustes distance matrix of the average morphology among 53 genera of carabid beetles, a cluster analysis was performed to construct a morphological phenotypic tree, including the head, pronotum, elytra, and all three (Figure 4). The results revealed that there were differences between the four phenotypic trees, but the variation trend of the head and the integrated morphological phenotypic tree was relatively close. When the 53 genera branched for the first time, the aphaenopsian and semi-aphaenopsian genera clustered into a clade, while the anophthalmic and surface-dwelling genera of carabid beetles clustered into another clade.

Figure 4.

Figure 4

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Phenotypic tree of ground beetle genera based on the Procrustes distance. (a) Head, (b) pronotum, (c) elytra, and (d) integrated morphology. Anphaenopsian: red letters; semi-anphaenopsian: green letters; anophthalmic: blue letters; surface-dwelling: purple letters.

In the head phenotypic tree (Figure 4a), Sidublemus was the first to be differentiated into a single branch. Dongodytes, Sinaphaenops, Giraffaphaenops, and Pilosaphaenops were all found to be closely related. However, Shuangheaphaenops, Uenotrechus, Xuedytes, Yanzaphaenops, and Minimaphaenops were mixed together with mostly semi-aphaenopsian genera carabid beetles. From the integrated phenotypic tree (Figure 4d), it could be seen that Giraffaphaenops and Xuedytes were the earliest to differentiate, and they were located far from other genera. The relationship between Yanzaphaenops of the aphaenopsian and semi-aphaenopsian group was relatively close, while Wanhuaphaenops of the anophthalmic group had a close relationship to those of the aphaenopsian group.

In the pronotum phenotypic tree (Figure 4b), all the aphaenopsian group except for Yanzaphaenops was combined into a clade with Wanhuaphaenops, Shenaphaenops, and Huoyanodytes. The remaining three types of carabids genera were clustered together, while about 1/3 of the anophthalmic type were grouped with surface-dwelling carabid beetles in another clade. The result of the elytra phenotypic tree (Figure 4c) showed that Dianotrechus was the first to be differentiated into a single branch. The aphaenopsian group and a small part of the semi-aphaenopsian group were clustered into a clade. Among them, Dongodytes is closely related to Xuedytes, but the same highly specialized Sinaphaenops was far away from the other genera in the aphaenopsian group. Part of the semi-aphaenopsian and anophthalmic groups were grouped together with surface-dwelling carabids.

4. Discussion

4.1. Morphological Variation Direction of Cave-Adapted Trechine Beetles

The highly specialized morphological characteristics of cave-dwelling ground beetles have long attracted the attention of researchers [50]. Most previous studies in this area have focused on changes in the morphology of cave-dwelling ground beetles after their long-term adaptation to cave life [51,52,53]. The present research is the first to attempt to study the morphological adaptation and variation direction of cave-dwelling ground beetles using geometric morphological analysis.

In the extreme environment of caves, animals often show the adaptive characteristics of convergent evolution due to environmental pressure [54,55]. Luo et al. [56,57] found that the cave-dwelling S. wangorum shows a distinct head posterior constriction and elongated pronotum combined with long and slender legs. Our results showed that the more slender their body is the higher the degree to which the ground beetles had adapted to the cave environment. This is mainly manifested in the fact that the widest point of the head gradually moves to the front, while the anterior edge of the pronotum tends to be narrower than the posterior edge in surface-dwelling compared to aphaenopsian carabids. Surprisingly, there is little available information concerning the elytra vitiation of cavernicolous carabids or other beetles [58]. We found that the position of the hair pores gradually moved towards the edge of the elytra, except for the scutellum, with the elytra becoming slenderer in cave carabids. One of the reasons why elytra is slenderer is a consequence of reducing or the disappearance of hind wings (also known as humeral calli) [59], and this situation is more distinct among the cave-dwelling species, especially the highly specialized ones.

In addition, aphaenopsian species mostly wander on stalactite walls or roofs in complete darkness [60], while semi-aphaenopsian species run on low rock walls or along the ground [61]. Anophthalmic species often live under small rocks or under damp dead wood in caves, and their habits are relatively close to those of surface-dwelling species [62,63,64]. It is speculated that the extension of the head and pronotum of cave-adapted ground beetles effectively increases the flexibility of the head, which may help this species to find prey in caves where food is scarce [65]. In contrast, surface-dwelling carabids may face great survival challenges [66,67] and their strong bodies will help them to fight and escape when faced with threats.

4.2. Geometric Morphology Analysis to Judge the Phylogeny of Cavernicolous Carabids

The molecular phylogeny of cave Trechini in China was analyzed based on two mitochondrial and two nuclear genes [68]. The preliminary study showed that the Chinese cave Trechini of Carabidae does not form a monophyletic lineage but rather is composed of four main independent evolutionary clades, each of which contains at least one highly convergent troglomorphic species.

In our study, certain differences exist in the morphological phenotypic trees of the head, pronotum, and elytra based on the Procrustes distance of carabids. For example, typical aphaenopsian genera—such as Dongodytes, Giraffaphaenops, Sinaphaenops, and Xuedytes—show extreme morphological specialization, but they are not clustered into same clade phylogenetically (Figure 4) [69]. Moreover, the semi-aphaenopsian genera of Shenaphaenops and Huoyanodytes and the anophthalmic type of Wanhuaphaenops are more closely related to the aphaenopsian type. A similar situation was also found in the Pyrenean subterranean Trechini, where the phylogenetic relationship between species of the same morphological type was not found to be close [70]. It may therefore be inferred that various Trechini lineages were settled multiple times independently in caves and underwent parallel morphological changes.

Furthermore, we did not classify the subgenus as an independent taxon in the present study, but the morphological differences between some subgenera in the same genus are relatively considerable. These differences may have a certain impact on the results of overall average shape.

Moreover, the length between the clade of Giraffaphaenops + Xuedytes and other genera is extensive in the integrated morphological phenotypic tree (Figure 4). This may have been caused by long periods of geographical isolation, or there may still be large gaps between these two genera and others. Future geometric morphometry of research for these groups could focus on adding the missing new genera and combining molecular phylogeny and biogeography for analysis.

Acknowledgments

We greatly appreciated Huang Zhengzhong (Institute pf Zoology, Chinese Academy of Science) and Ge Zhentai (South China Agricultural University), who provided help with using the geometric morphology analysis software. We would like to thank the caving team members of SCAU for their assistance with fieldwork.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/insects12111002/s1, Figure S1: Photographs of samples, Landmark Data S1: Semi-landmarks of samples.

Click here for additional data file. (54.7MB, zip)

Appendix A

Table A1.

Basal information of the studied specimens used in the geometric morphometric analysis.

No. Species Locality Adaptive Type
1 Dongodytes (Dongodytes) baxian Tian, 2011 Guangxi, Du’an County aphaenopsian
2 D. (D.) elongatus Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
3 D. (D.) fowleri Deuve, 1993 Guangxi, Bama County aphaenopsian
4 D. (D.) giraffa Uéno, 2005 Guangxi, Tian’e County aphaenopsian
5 D. (D.) grandis Uéno, 1998 Guangxi, Fengshan County aphaenopsian
6 D. (D.) lani Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
7 D. (D.) tonywhitteni Yang, Huang & Tian, 2018 Guangxi, Bama County aphaenopsian
8 D. (D.) troglodytes Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
9 D. (Dongodytodes) brevipenis Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
10 D. (D.) deharvengi Tian, 2011 Guangxi, Du’an County aphaenopsian
11 D. (D.) inexpectatus Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
12 D. (D.) jinzhuensis Tian, Yin & Huang, 2014 Guangxi, Du’an County aphaenopsian
13 D. (D.) yaophilus Tian, Yin & Huang, 2014 Guangxi, Dahu County aphaenopsian
14 Giraffaphaenops clarkei Deuve, 2002 Guangxi, Leye County aphaenopsian
15 G. yangi Tian & Luo, 2015 Guangxi, Tianlin County aphaenopsian
16 M. (Enshiaphaenops) senecali Deuve, 2016 Hubei, Enshi Autonomous Prefecture aphaenopsian
17 M. (Minimaphaenops) lipsae Deuve, 1999 Chongqing, Fengjie County aphaenopsian
18 Pilosaphaenops pilosulus Deuve & Tian, 2008 Guangxi, Huanjiang County aphaenopsian
19 P. whitteni Tian, 2010 Guangxi, Huanjiang County aphaenopsian
20 Shuangheaphaenops elegans Tian, 2017 Guizhou, Suiyang County aphaenopsian
21 Sinaphaenops (Dongaphaenops) xuxiakei Deuve & Tian, 2014 Guizhou, Pan County aphaenopsian
22 S. (Sinaphaenops) banshanicus Tian, Chen & Tang, 2017 Guizhou, Guiding County aphaenopsian
23 S. (S.) gracilior Uéno & Ran, 1998 Guizhou, Libo County aphaenopsian
24 S. (S.) lipoi Chen, Huang & Tian, 2020 Guizhou, Guiyang City aphaenopsian
25 S. (S.) mirabilissimus Uéno & Wang, 1991 Guizhou, Libo County aphaenopsian
26 S. (S.) mochongensis Tian & Huang, 2015 Guizhou, Duyun City aphaenopsian
27 S. (S.) orthogenys Uéno, 2002 Guizhou, Sandu County aphaenopsian
28 S. (S.) wangorum Uéno & Ran, 1998 Guizhou, Libo County aphaenopsian
29 S. (S.) yaolinensis Tian, Chen & Yang, 2017 Guizhou, Duyun City aphaenopsian
30 S. (Thaumastaphaenops) bidraconis Uéno, 2002 Guizhou, Ziyun County aphaenopsian
31 S. (T.) pulcherrimus Magrini, Vanni & Zanon, 1997 Guizhou, Ziyun County aphaenopsian
32 Uenotrechus deuvei Tian & Chen, 2017 Guangxi, Du’an County aphaenopsian
33 U. gejianbangi Tian & Wei, 2017 Guangxi, Huanjiang County aphaenopsian
34 U. liboensis Deuve & Tian, 1999 Guizhou, Maolan County aphaenopsian
35 U. nandanensis Deuve & Tian, 2010 Guizhou, Nandan County aphaenopsian
36 Xuedytes bellus Tian & Huang, 2017 Guangxi, Du’an County aphaenopsian
37 Yanzaphaenops hirundinis Uéno, 2005 Hubei, Shennongjiia aphaenopsian
38 Aspidaphaenops dudou Tian & Huang, 2018 Guizhou, Xingyi County semi-aphaenopsian
39 A. masakii Uéno, 2006 Guizhou, Xingyi County semi-aphaenopsian
40 A. reflexus Uéno, 2006 Guizhou, Ceheng County semi-aphaenopsian
41 A. volatidraconis Uéno, 2006 Guizhou, Xingyi County semi-aphaenopsian
42 A. xiongda Tian & Huang, 2018 Guizhou, Anlong County semi-aphaenopsian
43 Boreaphaenops angustus Uéno, 2002 Hubei, Shennongjiia semi-aphaenopsian
44 Guiaphaenops deuvei Tian, Feng & Wei, 2017 Guangxi, Lingyun County semi-aphaenopsian
45 G. lingyunensis Deuve, 2002 Guangxi, Lingyun County semi-aphaenopsian
46 Guizhaphaenops (Guizhaphaenops) giganteus Uéno, 2000 Guangxi, Shuicheng County semi-aphaenopsian
47 G. (G.) lipsorum Deuve, 1999 Yunnan, Zhenxiong County semi-aphaenopsian
48 G. (G.) pouillyi Deuve & Queinnec, 2014 Guizhou, Pan County semi-aphaenopsian
49 G. (G.) striatus Uéno, 2000 Guizhou, Liupanshui City semi-aphaenopsian
50 G. (G.) zhijinensis Uéno & Ran, 2004 Guizhou, Zijin County semi-aphaenopsian
51 G. (G.) zorzini Vigna Taglianti, 1997 Guangxi, Shuicheng County semi-aphaenopsian
52 G. (Semiaphaenops) lipsorum zunyiensis Deuve & Tian, 2018 Yunnan, Zhenxiong County semi-aphaenopsian
53 G. (S.) martii Deuve, 2001 Yunnan, Zhenxiong County semi-aphaenopsian
54 G. (S.) yudongensis Deuve & Tian, 2016 Yunnan, Zhenxiong County semi-aphaenopsian
55 Huoyanodytes tujiaphilus Tian & Huang, 2016 Hunan, Longshan County semi-aphaenopsian
56 Jiangxiaphaenops longiceps Uéno & Clarke, 2007 Jiangxi, Shangrao City semi-aphaenopsian
57 Luoxiaotrechus deuvei Tian & Yin, 2013 Hunan, You County semi-aphaenopsian
58 L. yini Tian & Huang, 2015 Jiangxi, Pingxiang City semi-aphaenopsian
59 Plesioaphaenops annae Deuve & Tian, 2011 Guangxi, Longlin County semi-aphaenopsian
60 Shenaphaenops humeralis Uéno, 1999 Guangxi, Shuicheng County semi-aphaenopsian
61 Shiqianaphaenops majusculus Uéno, 1999 Guizhou, Shiqian County semi-aphaenopsian
62 Toshiaphaenops globipennis Uéno, 1999 Hubei, Xianfeng County semi-aphaenopsian
63 T. ovicollis Uéno, 1999 Hunan, Longshan County semi-aphaenopsian
64 Zhijinaphaenops gravidulus Uéno & Ran, 2002 Guizhou, Zijin County semi-aphaenopsian
65 Z. haozhicus Deuve & Tian, 2018 Guizhou, Zijin County semi-aphaenopsian
66 Z. jingliae Deuve & Tian, 2015 Guizhou, Xifeng County semi-aphaenopsian
67 Z. lii Uéno & Ran, 2002 Guizhou, Zijin County semi-aphaenopsian
68 Z. liuae Deuve & Tian, 2015 Guizhou, Xifeng County semi-aphaenopsian
69 Z. multisetifer Deuve & Tian, 2018 Guizhou, Bijie City semi-aphaenopsian
70 Z. pubescens Uéno & Ran, 2002 Guizhou, Zijin County semi-aphaenopsian
712 Z. wenganicus Deuve & Tian, 2018 Guizhou, Wengan County semi-aphaenopsian
72 Z. zunyicus Deuve & Tian, 2018 Guizhou, Zhunyi City semi-aphaenopsian
73 Bathytrechus rueci Uéno, 2005 Guangxi, Leye County anophthalmic
74 Cathaiaphaenops (Amygdalotrechus) amplipennis Uéno, 2000 Hubei, Xianfeng County anophthalmic
75 C. (A.) chuandongziensis Deuve, 1999 Hubei, Banqiao Town anophthalmic
76 C. (A.) cychroides Deuve & Tian, 2016 Hubei, Lichuan City anophthalmic
77 C. (A.) draconis Deuve, 1999 Chongqing, Fengjie County anophthalmic
78 C. (A.) enshiensis Deuve & Tian, 2016 Hubei, Banqiao Town anophthalmic
79 C. (A.) lagredeae Deuve, 2016 Hubei, Enshi Autonomous Prefecture anophthalmic
80 C. (A.) lynchae Deuve & Tian, 2008 Hubei, Jianshi County anophthalmic
81 C. (A.) vignatagliantii Deuve, 1999 Chongqing, Fengjie County anophthalmic
82 C. (Cathaiaphaenops) delprati Deuve, 1996 Hunan, Longshan County anophthalmic
83 Cimmeritodes (Cimmeritodes) huangi Deuve, 1996 Hunan, Longshan County anophthalmic
84 C. (Dianocimmerites) crassifemoralis Deuve & Tian, 2016 Yunnan, Zhenxiong County anophthalmic
85 C. (Shimenrites) shimenensis Deuve & Tian, 2017 Hunan, Shimen County anophthalmic
86 C. (Xiangcimmerites) zhongfangensis Deuve & Tian, 2016 Hunan, Zhongfang County anophthalmic
87 C. (Zhecimmerites) parvus Tian & Li, 2016 Anhui, Chaohu City anophthalmic
88 C. (Z.) zhejiangensis Deuve & Tian, 2015 Zhejiang, Changshan County anophthalmic
89 Deuveaphaenops (Deuveaphaenops) qimenxicus Tian & Huang, 2017 Chongqing, Wulong District anophthalmic
90 D. (Furongius) gelaophilus Tian & Huang, 2017 Guizhou, Zhunyi City anophthalmic
91 Dianotrechus gueorguievi Tian, 2016 Yunnan, Anning City anophthalmic
92 Dongoblemus kemadongicus Deuve & Tian, 2016 Yunnan, Zhenxiong County anophthalmic
93 Graciliblemus lipingensis Deuve & Tian, 2016 Guizhou, Liping County anophthalmic
94 Jiulongotrechus pubescens Tian, Huang & Wang, 2015 Guizhou, Tongren City anophthalmic
95 Junaphaenops tumidipennis Uéno, 1997 Yunnan, Kunming City anophthalmic
96 Libotrechus duanensis Lin & Tian, 2014 Guangxi, Dahu County anophthalmic
97 L. nishikawai Uéno, 1998 Guizhou, Libo County anophthalmic
98 Microblemus rieae Uéno, 2007 Zhejiang, Jinghua City anophthalmic
99 Oodinotrechus (Oodinotrechus) kishimotoi Uéno, 1998 Guizhou, Libo County anophthalmic
100 O. (O.) liyoubangi Tian, 2014 Guangxi, Huanjiang County anophthalmic
101 O. (Pingleotrechus) yinae Sun & Tian, 2015 Guangxi, Pingle County anophthalmic
102 Qianaphaenops (Qianaphaenops) emersoni Tian & Clarke, 2012 Guizhou, Yanhe County anophthalmic
103 Q. (Q.) longicornis Uéno, 2000 Guizhou, Fenggang County anophthalmic
104 Q. (Q.) pilosus Uéno, 2000 Guizhou, Jiangkou County anophthalmic
105 Q. (Q.) rotundicollis Uéno, 2000 Guizhou, Sinan County anophthalmic
106 Q. (Q.) tenuis Uéno, 2000 Guizhou, Fenggang County anophthalmic
107 Q. (Qiandongaphaenops) variabilis Tian, Huang & Wang, 2015 Guizhou, Cengong County anophthalmic
108 Q. (Tiankengius) xigouicus Tian & Huang, 2018 Shanxi, Hanzhong City anophthalmic
109 Qianotrechus (Qianotrechus) fani Uéno, 2003 Sichuan, Gulin County anophthalmic
110 Q. (Q.) laevis Uéno, 2000 Guizhou, Zhengan County anophthalmic
111 Q. (Q.) magnicollis Uéno, 2000 Guizhou, Suiyang County anophthalmic
112 Q. (Q.) tenuicollis cheni Uéno, 2003 Guizhou, Suiyang County anophthalmic
113 Q. (Sanwangius) rowselli, Tian & Chen, 2019 Chongqing, Wulong District anophthalmic
114 Satotrechus longlinensis Deuve & Tian, 2011 Guangxi, Longlin County anophthalmic
115 S. rieae Uéno, 2006 Guizhou, Anlong County anophthalmic
116 Shenoblemus minusculus Tian & Fang, 2020 Anhui, Huangshan City anophthalmic
117 Shilinotrechus fusiformis Uéno, 2003 Yunnan, Shilin County anophthalmic
118 S. intricatus Huang & Tian, 2015 Yunnan, Yiliang County anophthalmic
119 Shuaphaenops parvicollis Uéno, 1999 Chongqing, Jinfoshan anophthalmic
120 Sichuanotrechus albidraconis Uéno, 2006 Sichuan, Jiangyou City anophthalmic
121 S. dakangensis Huang & Tian, 2015 Sichuan, Jiangyou City anophthalmic
122 Sidublemus solidus Tian & Yin, 2013 Hunan, Guidong County anophthalmic
123 Sinotroglodytes bedosae Deuve, 1996 Hunan, Longshan County anophthalmic
124 S. hygrophilus Uéno, 2009 Hunan, Sangzhi County anophthalmic
125 S. yanwangi Huang, Tian & Faille, 2020 Hubei, Yichang City anophthalmic
126 Superbotrechus bennetti Deuve & Tian, 2009 Hubei, Yichang City anophthalmic
127 Tianeotrechus trisetosus Tian & Tang, 2016 Guangxi, Tian’e County anophthalmic
128 Tianzhuaphaenops jinshanensis Zhao & Tian, 2016 Guizhou, Tianzhu County anophthalmic
129 Wanhuaphaenops zhangi Tian & Wang, 2016 Hunan, Chenzhou City anophthalmic
130 Wanoblemus wui Tian & Fang, 2016 Anhui, Xuancheng City anophthalmic
131 Wulongoblemus tsuiblemoides Uéno, 2007 Zhejiang, Jiangshan City anophthalmic
132 Yunotrechus diannanensis Tian & Huang, 2014 Yunnan, Maguan County anophthalmic
133 Agonotrechus spinangulus Belousov, Kabak & Liang, 2019 Sichuan, Muli County surface-dwelling
134 Protrechiama crassipes Uéno, 1997 Sichuan, Meigu County surface-dwelling
135 Sinotrechiama yunnanus Belousov, Kabak & Liang, 2019 Yunnan, Dayao County surface-dwelling
136 Trechus aghiazicus Belousov & Kabak, 2019 Xinjiang, Zhaosu County surface-dwelling
137 T. cratocephalus Belousov & Kabak, 2019 Xinjiang, Zhaosu County surface-dwelling
138 T. saluki Belousov & Kabak, 2019 Xinjiang, Xinyuan County surface-dwelling
139 T. torgaut Belousov & Kabak, 2019 Xinjiang, Hejing County surface-dwelling
140 T. tsanmensis Belousov & Kabak, 2019 Xinjiang, Xinyuan County surface-dwelling
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Author Contributions

Conceptualization, M.T., S.H., X.L. and W.L; methodology, M.C.; software, M.C.; validation, W.G. and W.L.; formal analysis, M.C., W.G. and W.L.; investigation, M.T., S.H., M.C. and W.L.; resources, M.T., S.H., M.C. and W.L.; data curation, M.T., S.H., M.C., W.G. and W.L.; writing—original draft preparation, M.C., W.G. and W.L; writing—review and editing, M.T., S.H., M.C., W.L., W.G. and X.L.; visualization, W.L. and W.G.; supervision, M.T. and W.L.; project administration, M.T. and W.L.; funding acquisition, M.T. and W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 41871039.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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