Research Article |
Corresponding author: Huateng Huang ( huanghuateng@snnu.edu.cn ) Corresponding author: Li-Bin Ma ( libinma@foxmail.com ) Academic editor: Zhu-Qing He
© 2022 Ning Wang, Huateng Huang, Li-Bin Ma.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wang N, Huang H, Ma L-B (2022) The intraspecific variation of morphology and coloration of field crickets: a taxonomic revision of Chinese Gymnogryllus Saussure, 1877 and Phonarellus Gorochov, 1983 (Orthoptera, Gryllidae, Gryllini). ZooKeys 1129: 85-107. https://doi.org/10.3897/zookeys.1129.87706
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After extensive sampling of specimens from species found in China, we examined the intraspecific morphological variation of several characters used for species delimitation in two closely related cricket genera, Gymnogryllus Saussure, 1877 and Phonarellus Gorochov, 1983. We found that the characters (male genitalia in Gymnogryllus odonopetalus Xie & Zheng, 2003 and Phonarellus ritsemae (Saussure, 1877), and coloration of the hind leg in Phonarellus minor (Chopard, 1959)) exhibit considerable amounts of variation within species, and are thus not reliable characters for species differentiation. Therefore, we revised the taxonomy of these two genera. Five synonyms are proposed: G. yunnanensis (= G. odonopetalus) syn. nov., G. striatus (= G. odonopetalus) syn. nov., G. longus (= G. odonopetalus) syn. nov., G. tumidulus (= G. odonopetalus) syn. nov., and P. flavipes (= P. minor) syn. nov. All species mentioned above are described and illustrated. Keys and a distribution map are provided.
Cricket, genitalia, Grylloidea, morphological diversity, new synonym, taxonomy
Gymnogryllus Saussure, 1877 and Phonarellus Gorochov, 1983 have species in China that are difficult to distinguish based on morphology, and we found that some of the “different” species co-occur at the same collection site and at the same time. Many of these species were proposed based on a limited number of specimens (e.g.,
Gymnogryllus was established by Saussure in 1877 with Gryllus elegans Guérin-Méneville, 1834 as the type species. It is distinguished from other genera of the tribe Gryllini by the face (distinctly longer than wide), oblique veins (slightly curved), and the ovipositor (short and armed with a small hook in the anterior of the lower valvae). Species of this genus have a similar appearance, and the male genitalia features are the primary characteristics for species identification. Currently, 45 species are reported worldwide, from India to Australia, and most of them are found in tropical Southeast Asia (Indian subcontinent, western Himalayas, Burma, Vietnam, and Malaysia) (
Gorochov established the genus Phonarellus for species originally belonging to Gymnogryllus and designated Gymnogryllus minor Chopard, 1959 as the type species (Gorochov, 1983). Compared to Gymnogryllus, species of Phonarellus are smaller, the cercus base is of light color, and the apical area of the genitalia is obviously different between both genera. We recognize the genus by its contrasting coloration of antennae (proximal segments colored light and most of the hind portion colored dark, sometimes completely white), ocelli almost arranged in a line, shiny and smooth pronotum, and somewhat leathery elytra (Fig.
Living photos of some Phonarellus and Gymnogryllus species A, B male of P. minor (with varing proportion of black areas on hind legs) C female of P. minor D male of P. ritsemae E male of G. odonopetalus F female of G. odonopetalus (Photos A–D were provided by Zhang, Tao, and E, F were photographed by He, Zhixin).
To address the problems with species of Chinese Gymnogryllus and Phonarellus, we collected more than 100 specimens (35 specimens of Gymnogryllus and 130 specimens of Phonarellus) and examined their morphological characteristics. Based on our results, we consider that four species in Gymnogryllus are junior synonyms of G. odonopetalus, and P. flavipes is a junior synonym of P. minor. The diagnostic characteristics previously proposed for species identification are unreliable because of extensive variation. New checklists of Chinese Gymnogryllus and Phonarellus species, with keys to species and distribution maps (Fig.
Most specimens were attracted to a high-pressure mercury lamp (500W) in the field. The specimens were preserved in analytical-grade ethanol during fieldwork and then pinned and dry-preserved in laboratory. After softening, dissecting needles were used to pull out the male genitalia from the gonopore. The dissected genitalia complexes were prepared by placing them into a concentrated solution of alkaline protease (0.2 g/ml, AOBOX, China) with a water bath temperature of 40–50 °C for 48 hours. Identification of involved species is mainly based on male morphology. Whole bodies were photographed with a VHX-6000 digital microscope (Keyence, Osaka, Japan). Figures of genitalia and body details were produced using a ToupCam Digital camera and bundled software (ToupTek, Hangzhou, China).
All specimens were measured using ToupCam Digital camera (E3ISPM05000KPA) and bundled software (ToupTek, Hangzhou, China). All the measurements are in millimeters (mm). Nomenclature of male genitalia follows
We used 42 P. minor specimens with at least one intact hind leg. Photos of these posterior femora were taken with a VHX-6000 digital microscope (Keyence, Osaka, Japan) and processed in ImageJ. We used the Threshold function in ImageJ ver.1.53k (
We used a ToupCam Digital camera (E3ISPM05000KPA) and bundled software (ToupTek, Hangzhou, China) to measure the distances between the first and second oblique veins at the base of 42 specimens. The distributions were graphed in Microsoft Excel (Microsoft Office 2016).
Acronyms used for the institutions where those examined materials are deposited:
NWAFU Entomological Museum of Northwest A&F University, Yangling, China;
SEM (IEAS) Shanghai Entomological Museum, CAS, Shanghai, China.
Genus Gymnogryllus Saussure, 1877
Gymnogryllus contractus Liu, Yin & Liu, 1995
Chinese name. 狭膜裸蟋
Distribution. Yunnan.
Gymnogryllus odonopetalus Xie & Zheng, 2003
Gymnogryllus yunnanensis Ma & Zhang, 2011, syn. nov.
Gymnogryllus striatus Ma & Zhang, 2011, syn. nov.
Gymnogryllus longus Ma & Zhang, 2011, syn. nov.
Gymnogryllus tumidulus Ma & Zhang, 2011, syn. nov.
Chinese name. 齿瓣裸蟋
Distribution. Yunnan, Guangxi, Guangdong.
Gymnogryllus dolichodens Ma & Zhang, 2011
Chinese name. 长突裸蟋
Distribution. Yunnan.
Gymnogryllus extrarius Ma & Zhang, 2011
Chinese name. 外突裸蟋
Distribution. Yunnan.
Genus Phonarellus Gorochov, 1983
Phonarellus minor (Chopard, 1959)
Phonarellus flavipes Xia, Liu & Yin, 1991, syn. nov.
Chinese name. 小音蟋
Distribution. Guangxi, Hainan, Guangdong, Yunnan.
Phonarellus ritsemae (Saussure, 1877)
Chinese name. 利特音蟋
Distribution. Guangxi, Zhejiang, Yunnan, Guangdong, Hong Kong.
Phonarellus zebripes He, 2022
Chinese name. 斑腿音蟋
Distribution. Yunnan.
Orthoptera: Grylloidea; Gryllidae; Gryllinae
Gymnogryllus
Brunner von Wattenwyl 1893: 197;
Brachytrypus (Gymnogryllus) Saussure, 1877: 291.
Gryllus elegans (= Gymnogryllus leucostictus). Brachytrypus (Gymnogryllus) Saussure, 1877: 291.
India, Australia, western Himalayas, Burma, Vietnam, Malaysia, China.
Body large. Head, pronotum and much of hind femur blackish brown; rest of body of light color. Light brown bands uniformly distributed over posterior peduncle. Forewings not reaching tip of abdomen; hind wings largely surpassing abdomen. Mirror inclined rectangular. The length of the apical field of forewings varies among individuals. Subgenital plate shaped as hook. Genitalia large, in caudal view, epiphallus arch-shaped and the apically armed with a pair of long teeth. The space between the teeth and the shape of them varied among individuals (Fig.
Eight species of Gymnogryllus are reported from China, and six of them have been found in Yunnan. Among them, G. longus, G. tumidulus, G. yunnanensis, and G. striatus have been described for differences in the angle of the epiphallic apex and the length of the apical field of tegmen. However, they are similar to G. odonopetalus in appearance and can be collected from the same location at the same time. We compared specimens collected from the same site and concluded that these two features present intraspecific variation and are unreliable for species delimitation. We consider that all four taxa are synonyms of G. odonopetalus.
1 | Mirror narrow | G . contractus |
– | Mirror much broad | 2 |
2 | Forewings extended to tip of abdomen | G . dolichodens |
– | Forewings not extended to tip of abdomen | 3 |
3 | Epistomal suture curved upward medially, frons with light angular patch | G . odonopetalus |
– | Epistomal suture straight, frons uniform colored | G . extrarius |
Gymnogryllus odonopetalus Xie & Zheng, 2003: 496, 498.
Gymnogryllus yunnanensis Ma & Zhang, 2011: 31–40, syn. nov.
Gymnogryllus longus Ma & Zhang, 2011: 31–40, syn. nov.
Gymnogryllus tumidulus Ma & Zhang, 2011: 31–40, syn. nov.
Gymnogryllus striatus Ma & Zhang, 2011: 31–40, syn. nov.
Type locality: Menglun, Xishuangbanna, Yunnan, China. Deposited at Museum of Flora and Fauna of Shaanxi Normal University, Xi’an, China (
China: 1 male (holotype), Yunnan, Xishuangbanna, Menglun, Sept. 8, 1999, Xie, Lingde coll. (
(Fig.
Male (N = 30): BL 27.73–29.42; HW 6.42–6.84; PL 4.86–5.32; FWL 18.62–21.32; HLL 16.27–17.12; HTL 9.43–10.14; EW 1.56–1.79; PW 7.62–7.98; HWL 6.04–6.84; DVL 4.62–4.96; ML 3.72–3.98; CL 8.15–8.54; FTL 5.42–5.76; MTL 6.29–6.45.
Male
(Figs
Pronotum disc rectanglur, anterior margin concave, posterior margin sinuated; a longitudinal groove in middle of pronotum, about 2/3 the length of the pronotum. Fore margin of pronotum rough and densely pubescent. Tegmen reaching tip of abdomen; with three oblique veins, outmost nearly vertical and straight, two internal inclined and longer than outmost; and them converging diagonal vein. Diagonal vein curved and anteriorly forked. Chord veins three, the internal two extremely curved, connected at bottom. Between diagonal vein and the most internal chord vein armed with two transverse veins. Mirror large, inclined rectangular. Apical field triangular, about 2/5 the length of tegmina, variable among individuals, armed with rectangular cells.
Fore tibiae with inner and outer tympanum, inner tympanum small and ovoid, outer longer-oval. Hind femora brown with light stripes. Distal of hind tibiae with five dorsal spurs on both sides; apical spurs six, the inner apical spurs three (the dorsal one longest, the ventral one shortest and 1/4 length of the longest one, the middle one about 2/3 length of the longest), and the outer apical spurs three (equal length of the dorsal one and the ventral one, about 2/3 length of the middle one). Subgenital plate hook-like. Cercus straight and short; with long hair sparse and short hair dense.
Genitalia
(Figs
Intraspecific variation of genitalia in G. odonopetalus A–F genitalia from six individuals in lateral view (Note: the red arrows point to the posterior of epiphallus, highlighting variations among individuals; the blue circles indicate the protuberance of mid-ectoparamere) G–L genitalia of the same six individuals in dorsal view (Note: the green circles indicate the median lobe of the epiphallus posterior).
Coloration
(Fig.
Female (Figs
Hence, the species G. odonopetalus has some charecters showing intraspecific variation even within specimens collected from the same place and time. In lateral view, the angle between the apical teeth and the posterior edge of the medial lobe of epiphallus is variable among individuals (red arrows in Fig.
Phonarellus
Gorochov, 1983: 323;
Gymnogryllus minor.
Afghanistan, Bangladesh, Burkina Faso, China, Gabon, India, Japan, Kenya, Mali, Sierre Leone, Vietnam.
Ocelli positioned in an almost straight line. Antenna ornamented with white ring-like pattern. Scapus conspicuously narrower than the half-width of the rostrum. Apical field shorter than mirror or slightly longer. Both tympana present. Hind tibiae shorter than half the length of hind femur. Epiphallus with large lateral lobes but without median lobe. Cerci usually dark with light proximally. We regard all species as belonging to Phonarellus, whose characters are as follows: ovipositor well developed and rather long; ectoparamere short.
Four species of this genus have been reported from China (P. ritsemae, P. minor, P. flavipes, and P. zebripes). Phonarellus flavipes has been described for its yellow hind legs and the interval between the anterior of the first and second oblique veins. But these characters can also be found in P. minor living side by side with P. flavipes. Studying a large number of specimens of these three taxa from Yunnan and Guangdong, we tested whether the color of hind legs is a valid trait for species delimitation, and provided a description of P. ritsemae.
1 | Body bicolored, head reddish with most of the remainder dark | P. minor |
– | Body almost uniformly dark | 2 |
2 | Hind femora uniformly dark | P. ritsemae |
– | Hind femora black and white | P . zebripes |
Gymnogryllus minor
Chopard, 1959: 1;
Gymnogryllus kashmirensis Bhowmik, 1977: 24, misidentification.
Phonarellus (Phonarellus) minor:
Phonarellus minor:
Gymnogryllus (Phonarellus) minor:
Phonarellus flavipes
Type locality: Asia-Tropical, Indian Subcontinent, India, Kerala, Malabar Coast, Mahé. Deposited at Muséum National d’Histoire Naturelle, Paris, France (not examined).
China: 36 males and 28 females, Yunnan, Mengla, Shangyong, Longmen, 1030 m, May 13, 2013, Ma, Libin coll. (
(Fig.
BL 12.86–14.23; HW 3.54–3.75; PL 2.26–2.39; PW 4.12–4.56; FWL 9.13–9.68; HWL 7.45–8.23; MTL 3.24–3.46; CL 4.67–5.31; HTL 4.73–5.21; HLL 8.11–8.42; OL 7.28–7.64.
Body bicolored; head and legs often yellow or yellowish-brown, remainders always dark brown. Body size small for the genus. Both proximal and anterior notch of epiphallus arc-like and posterior notch almost right angular. Coloration of hind legs variable.
(Figs
Disc of pronotum laterally widened and with hind margin slightly wider than fore margin; anterior margin broadly concave, posterior margin almost straight. Oblique veins three, the outmost one short and two internal of them longer and inclined; the top of them close each other. Diagonal vein straight. Chord veins three, the internal two veins extremely bent, connected at the bottom. Between the diagonal vein and the most internal chord vein armed with a transverse vein. The most internal chord vein linking with mirror by two transverse veins. Mirror small; the basal margin of mirror angle-like, dividing vein angular and the width of mirror nearly equal to the length. Field area short, close to the length of mirror, or slightly longer than mirror. Hind wings long and the uncovered portions longer than the half-length of forewings.
Fore tibiae with inner tympanum small and ovoid; the outer one large and oblong. Hind tibiae short, half the length of hind femur. Inner dorsal spurs of hind tibiae curved distally and longer than the outer ones. The length and number of dorsal spurs varied, while the basal spurs rather short, they numbered five or six of both the inner and outer; while spurs vary in length, the number of inner and outer spurs always 4:4. Inner apical spurs longer than outer ones. The median one of outer apical spurs longest and the remaining ones almost equal in length, and the bottom one of inner apical spurs shortest and the remaining ones in similar length. Inner dorsal spines of the first hind tarsus numbered 5–7 and outer ones numbered 7–9. Cercus thickness proximally and tapering. Subgenital plate simple and cucullate with acute apex.
Genitalia
(Fig.
Female (Fig.
Coloration
(Fig.
The original description of P. flavipes does not mention genital characters.
Distance between the first and second oblique vein of P. minor (Note: The data in the graph were measured from 42 samples. All the data can be roughly divided into three groups: distance less than 0.6 mm, distance greater than 1.2 mm, and distance between 0.7 mm and 1 mm, among which, individuals with distance less than 0.6 mm are the majority. The figure of the veins on the right, from top to bottom, represents the maximum, median and minimum distances, respectively. Units: mm).
This figure shows that the distribution of the area-to-total area ratio of the black area of P. minor (Note: The data in the graph were measured from 42 samples. In the figure, miscellaneous colors, i.e., individuals with black proportions between 30% and 90%, accounted for the majority, while light-colored individuals, i.e., individuals with black proportions no higher than 20%, and black individuals, i.e., individuals with black proportions higher than 90%, were very few and only one in our sampling respectively.).
Phonarellus minor (Chopard, 1959) (A–J) A–D bodies of P. minor (A, C males B, D females; scale bar: 10mm A, B specimens with dark colored hind legs C, D specimens with light-colored hind legs) E–G genitalia (E dorsally viewed F laterally viewed G ventrally viewed) H color variation of hind legs from dark to light I variable intervals at the base of oblique veins (Note: The red line point to the first and second oblique veins. The distance between the two veins in the rightmost figure is the smallest (see Fig.
Liogryllus ritsemae
Saussure, 1877: 304;
Acheta ritsemae:
Gryllus ritsemae: Hisumatsu 1952: 43.
Tartarogryllus ritsemae: Chopard 1961: 272; Randell 1964: 1582; Leroy 1966: 39; Chopard 1967: 73.
Phonarellus ritsemae: Yin and Liu, 1995: 138–139;
Type locality: Japan. Deposited at National Nature Historical Museum, Leiden, Netherlands (not examined).
China: 1 female, Yunnan, Mengla, Shangyong, Longmen, May 13, 2013, Ma, Libin (
China (Yunnan, Guangdong, Guangxi, Hong Kong), Japan..
Male (N = 22): BL 13.07–15.16; HW 3.76–4.15; PL 2.74–2.81; PW 4.05–4.25; FWL 7.88–10.05; HFL 8.97–9.62; HTL 4.74–5.75; Female (N = 6): BL 15.65–16.48; HW 3.83–4.06; PL 2.51–2.75; PW 3.85–4.06; FWL 8.86–9.92; HFL 8.83–10.71; HTL 4.95–5.63.
Male
(Figs
Genitalia
(Figs
Intraspecific variation of genitalia of P. ritsemae A–C genitalia of three individuals in ventral view D–F drawing of ectoparamere in ventral view G–I Genitalia of the same three individuals in lateral view (Note: The blue circles of the A–C graph point to the ectoparamere, highlighting variations among individuals; the red arrows in the G–I graph point to the teeth of epiphallic posterior).
Female (Fig.
Coloration
(Figs
Species delimitation is the foundation for biodiversity research, and finding robust and reliable characters for species identification is crucial for taxonomy. However, one difficulty faced by morphology-based species delimitation is distinguishing intraspecific variation from interspecific difference. When only a few specimens are accessible, we might mistake variation within species as species difference. Then, species identification might be unstable, leading to confusion in future taxonomic work. Here, we examined a large number of specimens in two cricket genera Gymnogryllus and Phonarellus. With multiple specimens, we revealed a considerable amount of morphological variation within species.
Notably, both genera possess intraspecific variation in male genitalia, features which are primary characters for species identification in insects (
We also observed intraspecific polymorphism with regard to body color in P. minor. Body color plays an essential role in adapting to environmental changes, resisting diseases, and avoiding predators (
Based on our discovery of intraspecific variation, we considered some diagnostic features previously used as characters for separating species in these two genera invalid. The new species checklist showed five synonymus (G. yunnanensis, G. striatus, G. longus, G. tumidulus and P. minor), which reduces the number of Chinese species of the genera Gymnogryllus and Phonarellus to four and three, respectively. Our work highlights the importance of extensive specimen collection and considering intraspecific variation in species identification.
We appreciate Dr Peng, Zhong (Shanghai Normal University) for providing specimens. We also thank Zhang, Tao and He, Zhixin for their specimen photos and Ma, Ge for her pictures. This work is supported by the National Natural Science Foundation of China (no. 32070474, 31750002).
The distance between the first and second oblique veins at the base varies of 42 specimens of the P. minor
Data type: statistical data
The area to total area ratio of the black area of the posterior femora of 42 specimens of the P. minor
Data type: statistical data