DNA Barcoding Reveals Species Diversity and Host Associations of Dryinidae Wasps (Insecta, Hymenoptera): A Case Study from the Xisha Islands in the South China Sea
1
Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China
2
State Key Laboratory of Plant Diversity and Specialty Crops, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China
3
South China National Botanical Garden, Guangzhou 510650, China
4
Tropical Entomology Research Center, Via De Gasperi 10, 01100 Viterbo, Italy
*
Author to whom correspondence should be addressed.
Animals 2024, 14(24), 3587; https://doi.org/10.3390/ani14243587
Submission received: 11 October 2024
/
Revised: 25 November 2024
/
Accepted: 10 December 2024
/
Published: 12 December 2024
(This article belongs to the Section Ecology and Conservation)
Simple Summary
Dryinidae are a diverse family of parasitoids, and they are important natural enemies of Auchenorrhyncha (Hemiptera) pests. A comprehensive understanding of the diversity and host interaction networks of these parasitoids is critical to their application in biological control programs and their conservation. However, traditional methods such as morphological identification and rearing are insufficient to understand the diversity and host associations of dryinids. In this paper, we assessed the effectiveness of DNA barcode techniques for surveying dryinid diversity and their host associations on the Xisha Islands. Based on the analyses of the mitochondrial cytochrome c oxidase subunit I (COI) sequences of adults and larvae, we recognized 11 dryinid species, including an undescribed species and one re-instated species, on the Xisha Islands. We also confirmed the host associations of each dryinid species and constructed a dryinid–hopper interaction network which suggests that the population sizes of some dryinid species are extremely small and further conservation assessments of dryinids for the Xisha Islands are needed. Our study demonstrates that DNA barcoding methods are potent for assessing parasitoid diversity and their host associations.
Abstract
Dryinidae are a cosmopolitan group of important parasitoids that attack the nymphs and adults of Auchenorrhyncha (Hemiptera) pests. Effective application of these parasitoids as biological control agents against Auchenorrhyncha and the development of conservation strategies depend upon a comprehensive understanding of the diversity and host interaction networks of these parasitoids. However, traditional morphology-based identification and rearing methods are inadequate to understand the diversity and host associations of dryinids due to their extreme sexual dimorphism, species rarity, and unique biology. To address this, we assessed the effectiveness of DNA barcode techniques for surveying dryinid diversity and their host associations on the Xisha Islands in the South China Sea. By analyzing the mitochondrial cytochrome c oxidase subunit I (COI) sequencies of adults and larvae of dryinids collected on six islets of the Xisha Islands, we recognized 11 dryinid species, including an undescribed species and one re-instated species, A. malaysianum Olmi, 1987, stat. rev. Additionally, we confirmed the host associations of each dryinid species and constructed a dryinid–hopper interaction network. This network was mostly composed of specialists, suggesting that the population sizes of some dryinid species were extremely small and highlighting the need for further conservation assessments of dryinids on the Xisha Islands. Overall, our study demonstrates the efficacy of DNA barcoding methods for assessing parasitoid diversity and their host associations, which are crucial for guiding conservation and management efforts for these important insects.
1. Introduction
Dryinidae is a cosmopolitan wasp family, with over 1900 species found worldwide [1,2,3]. These wasps are parasitoids and predators of Auchenorrhyncha (Hemiptera) pests, which can cause serious problems in crops such as rice, sugarcane, and fruits via direct feeding or by transmitting pathogens [4]. By parasitism and predation, these wasps are promising biological control agents that can be used to reduce the populations of leafhopper pests [5], and some species have been implemented in biological control programs [4].
Despite their importance in controlling pests, the diversity of these parasitoids and their host associations remain poorly understood, which has hampered their application in biological control and the development of conservation strategies [6,7]. Sexual dimorphism is extreme in Dryinidae, and many species were described based primarily on a single sex due to the difficulty in associating females with males [8,9,10]. This practice (i.e., describing a new species based on a single sex) would lead to an inaccurate understanding of the real diversity of these parasitoids [3]. Furthermore, the host associations of dryinid wasps are even more difficult to determine because this usually requires rearing the wasps from their hosts, which is challenging due to the difficulty of keeping the parasitized host alive until the emergence of the wasp(s) or because many dryinid wasps themselves are extremely rare, and it is rarely possible to locate and collect live parasitized hosts [7].
With the application of DNA barcoding methods, however, the aforementioned obstacle could be overcome. Studies have demonstrated that DNA barcoding is potent in species delimitation and uncovering the female–male association of the same species, especially in sexually dimorphic dryinids, which would enhance our understanding of their diversity [2,3,9,10,11]. Most dryinids are ectoparasitoids of the nymphs or adults of their host, and the larvae of the wasps insert their heads into the host’s coelom to feed on the hemolymph and tissues of the host from outside, with the rest of their body protruding between two of the host’s sclerites [4]. This specialized biology provides a rich resource for confirming the host associations of Dryinidae using DNA barcoding techniques. By analyzing the mitochondrial cytochrome c oxidase subunit I (COI) gene of the wasp adult and larva, the hosts of several dryinid species have been discovered [7,10]. This approach should be further tested on a broad scale to evaluate its efficacy.
Oceanic islands, due to their isolated habitat and the sensitivity of their biota, provide excellent opportunities for exploring questions related to biodiversity and conservation [12]. Previously, DNA barcoding was used to confirm the host of the first Dryinidae species (Gonatopus viet Olmi, 1986) on the Xisha Islands in the South China Sea [7]. During recent expeditions to the Xisha Islands, we collected a large number of Dryinidae and parasitized hopper specimens, which provided us with plenty of material to assess the diversity of dryinids and evaluate their conservational status. Thus, this study aims to investigate the diversity and host association of dryinid wasps on the Xisha Islands using DNA barcoding.
2. Materials and Methods
2.1. Insect Collection
This work is based upon specimens collected by sweep nets and yellow pan traps during two field trips to the Xisha Islands (Paracel Islands), which are a series of coral islets in the South China Sea. Samples of Dryinidae and their hosts were collected in various habitats (Figure S1) on six islets (Figure 1 (The sampling map was drawn using Q-GIS software (3.38.3) [13]); Table S1). The two field trips were carried out from 17 April to 12 May in 2019 and 4–16 January in 2024. Yellow pan traps (yellow plastic bowl, 4 cm height × 15 cm inside diameter, filled with soapy water, Figure S2A) were placed on the ground for 24 h to allow for the collection of insects which were preserved in 100% alcohol. A bottom-sealed emergence tent (dimensions: L 110 cm × H 110 cm × W 110 cm; built from a white fabric with an opening attached to a collecting bottle on the top and a dome-shaped zipper on the side for access, Figure S2B) was used to collect the specimens obtained with a sweep net. A sweep net was used to collect random insects on vegetation, and the material collected was placed into the emergence tent to allow most of the insects to become trapped in a collecting bottle filled with 100% alcohol. This method is efficient in collecting a large amount of insect specimens and can cover a large sampling area in a short time period. The specimens collected by both sampling methods were then used for DNA sequencing and morphological examinations.
2.2. Species Identification
Adult dryinid wasps and parasitized hosts (larva or adult) were first sorted into morphospecies. Representative specimens of each wasp and host species (Table 1) were selected for DNA sequencing and morphological examination. The wasp larva of each parasitized host specimen (Table 2) was also used for DNA analysis to confirm its identity. Each parasitized host specimen was photographed to record the position of the attached wasp larva (called a thylacium) using a Nikon SMZ25 microscope with a Nikon DS-Ri 2 digital camera system (Nikon Corporation, Tokyo, Japan) before DNA extraction. Genomic DNA of the adult wasps, their hosts (larva or adult), and wasp larva was extracted from the whole body, a single hind leg, and the cuticle, respectively, using a TIANamp Micro DNA Kit (Tiangen Biotech, Beijing, China) as described previously [3,7]. The sequences of the COI gene were acquired as described in Chen et al. [3]. All sequences generated in this study were deposited in GenBank under accession numbers listed in Table 1 and Table 2.
Voucher specimens (Table 1) were deposited in the insect collection of South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China (SCBG). Species of adult dryinid wasps were first identified based on morphological characteristics using the available keys present in Xu et al. [14] and Olmi and Xu [15], and then the genetic distance among species based on the COI sequences were analyzed to confirm their identities. Sequences were aligned by codons using MUSCLE implemented in Geneious 11.0.3, and the K2P distances within and between species were calculated.
Species descriptions followed the terminology used by Olmi et al. [1]. Body length was measured in millimeters from the anterior-most portion of the head (excluding the antenna) to the tip of the metasoma (excluding the sting, if exserted). Other measurements presented are relative. The abbreviations used in the text are as follows. POL: distance between inner edges of the lateral ocelli; OL: distance between inner edges of a lateral ocellus and the median ocellus; OOL: distance from the outer edge of a lateral ocellus to the eye; OPL: distance from the posterior edge of a lateral ocellus to the occipital carina; TL: distance from the posterior edge of an eye to the occipital carina.
Multifocal images of voucher specimens were produced using a Nikon SMZ25 microscope with a Nikon DS-Ri 2 digital camera system (Melville, NY, USA). The female chela and male genitalia were dissected using insect pins and gold–palladium coated for examination in a JSM-6360LV scanning electron microscope (JEOL, Tokyo, Japan). The chela and genitalia were then mounted on the point together with the original specimen. Images were then post-processed with Adobe Photoshop CS6 Extended (Adobe, San Jose, CA, USA).
Species of adult hosts were identified to the lowest possible taxonomic level by leafhopper and planthopper taxonomists (Qingquan Xue and Yixin Huang, see Acknowledgements), while the identity of nymphal hosts was confirmed by comparison of COI sequences. DNA sequences of wasp larvae were blasted against the GenBank database to check for identification and were also compared with a reference COI data set of Chinese Dryinidae (including the sequences of adult wasps newly generated in this study) compiled by the first author. Sequences with similarity greater than or equal to 97% were considered as the same species, because intraspecific pairwise distances of COI sequences in Dryinidae are generally less than 3% [2,3]. To display affinities among the studied dryinid wasps (adults and larvae), sequences were aligned by codon using MUSCLE and analyzed using RAxML as implemented in Geneious 11.0.3 to generate a maximum likelihood (ML) tree. The GTRGAMMA +I model was used as the best nucleotide substitution model, which was determined with ModelFinder [16] with the merge option enabled. Automatic bootstrapping criterion was selected as the appropriate number of bootstraps; 1000 replicates were run. The COI sequence of Chrysis principalis Smith, 1874 (Hymenoptera, Chrysididae) (GenBank: KY430781) was used as an outgroup based on the phylogenetic topologies recovered by Tribull [17].
2.3. Parasitoid–Host Networks
We used the package bipartite [18] to plot the parasitoid–host interaction network and calculate the network-level indices in R4.4.1 [19]. Three network-level indices were calculated to illustrate the structural properties of the network [20]. Connectance is the fraction of all possible links that are realized in a network, and it increasies with network generalization [21]. Network-level specialization (H’2) describes the degree of specialization or partitioning among two parties in the entire network [22], ranging from 0 (low specialization) to 1 (high specialization). Nestedness quantifies the degree of interactions of specialized species in a network.
3. Results
3.1. Wasp Adult Identification
The thirteen newly generated COI sequences of the adult wasps ranged from 675 bp to 681 bp. When analyzed in the BOLD system [23] and GenBank database, the blast results of the sequences generated in this study returned no matching sequences, with similarities that were all less than 93.5%. The intraspecific pairwise distances ranged from 0 to 1%, while the interspecific distances ranged between 7.5% and 20.4% (Table S2). Thus, based on both morphology and COI sequences, the adult wasp specimens collected on the six sampled islets were identified into seven morphospecies, including one probably undescribed species (description provided below), two known species of the genus Anteon Jurine, three known species, and an unidentified species (only male specimens, which are not identifiable morphologically) of the genus Gonatopus Ljungh (Table 2; Figures S3–S10). Anteon malaysianum Olmi, 1987 was first described from Malaysia but later was treated as a synonym of Anteon yasumatsui Olmi, 1984, due subtle differences in their mesoscutum but almost identical chela of the female foreleg [24]. In this study, the COI sequences, along with morphological characteristics such as the color of the antennae and legs and the sculpture of the mesosoma, indicate that A. malaysianum is a different species from A. yasumatsui. Therefore, we treat A. malaysianum Olmi, 1987, stat. rev., as a valid species. With the help of DNA barcoding, the male of Gonatopus validus (Olmi, 1984) was first discovered.
We here provide a description of the specimen to facilitate its identification in the future.
Anteon sp.
Material examined. CHINA: Hainan, Shansha, Chenhang Island, 16°26′59.982″ N, 111°42′39.054″ E, 10.i.2024, sweep, Huayan Chen leg., DNA: PP600740, SCBG_E0009677 (SCBG).
Description. Female, holotype. Body length 2.8 mm; fully winged (Figure 2A). Head black with mandible light yellow; antenna yellow; mesosoma and metasoma black; legs yellow with proximal extremity of coxae dark brown to black. Antenna clavate; antennomeres in the following proportions: 11:6:4:3.5:3.5:3.5:4:4:5:8. Head (Figure 2B,C) dull, largely granulate with smooth areas below eyes; vertex without two oblique keels connecting lateral ocelli to occipital carina; frontal line absent; OL = 6; OOL = 8; OPL = 6; POL = 9; TL = 8; greatest breadth of lateral ocellus shorter than OPL (1:3); occipital carina complete. Pronotum largely granulate, with the anterior surface about as long as the dorsal surface; dorsal surface shiny posteriorly, much shorter than mesoscutum (9:14); pronotal tubercle reaching tegula. Mesoscutum and mesoscutellum shiny, largely smooth. Notauli incomplete, present at the anterior 0.5 of the mesoscutum, foveate (Figure 2B). Metanotum shiny, smooth. Metapectal–propodeal complex with strong transverse keel between disc and propodeal declivity; disc reticulate rugose; propodeal declivity reticulate rugose, without longitudinal keels (Figure 2D). Forewing hyaline; distal part (Rs) of the stigmal vein (2r-rs&Rs) shorter than the proximal (2r-rs) part (3:5). Protarsomeres in the following proportions: 6:2:4:5:13. Protarsomere 2 produced into a hook. Enlarged claw (Figure 2F) with proximal prominence bearing one long bristle. Protarsomere 5 (Figure 2F) with basal part shorter than distal part, with one row of 11 lamellae, in addition to scattered hairs and bristles; distal apex with four lamellae. Tibial spurs 1/1/2.
3.2. Wasp Larva Identification
In total, 67 parasitized hosts representing two families and nine species were subjected to a molecular analysis of the wasp larva. Each host specimen bore a single wasp larva. Based on the comparison of the COI sequences of each wasp larva with a reference COI data set of Chinese Dryinidae and a species delimitation threshold of 97% similarity, the 67 wasp larvae were sorted into nine species, including one known species of Anteon and four known and four unidentifiable (male only) species of Gonatopus (Table 2). The affinities among the larvae and adults of the studied species are shown in Figure 3. Of the four unidentifiable species of Gonatopus, the COI sequences of three species were matched with male specimens collected outside of the Xisha Islands, indicating a more comprehensive reference COI data set of adult wasps would facilitate the identification of the wasp larvae.
Anteon malaysianum was found to parasitize the female adult of Balclutha incisa (Kirschbaum), with the thylacium positioned between the pro- and mesothoraxes. Four species of Gonatopus (G. nearcticus, G. validus, Gonatopus sp-HK, and Gonatopus sp-WZ) were found parasitizing the adult of their host(s), whereas the other four species (G. viet, G. yasumatsui, Gonatopus sp1, and Gonatopus sp-BJ) were found parasitizing both the adults and nymphs. The thylacium position of the eight Gonatopus species is on the dorsal or ventral metasoma (Table 2; Figure 4).
3.3. Parasitoid–Host Interactions
Parasitoid–host interactions are presented in the bipartite network of species that occur on the Xisha Islands. A total of 67 links were established based on nine dryinid species and nine hopper species (Figure 4; Table 2). The majority of the dryinid species (78%) parasitize one single hopper species, with the exception of Gonatopus viet, which parasitizes three species. Gonatopus yasumatsui was the species with the highest occurrence (41%) of all interactions, followed by G. viet and Gonatopus sp-BJ. Only two hopper species, B. incisa and Cemus nigromaculosus (Muir, 1917), were parasitized by two different wasp species, while the remaining seven hopper species were each parasitized by only one wasp species each. Among the nine hopper species, B. incisa was the most susceptible to parasitism. Overall, the network exhibited a low connectance (0.14), a low nestedness (28.47), and a high specialization (0.98) (Table S4).
4. Discussion
In this study, we discovered and identified eleven species of dryinid wasps from the Xisha Islands. This identification was achieved through a comprehensive analysis that incorporated both adult wasp morphology and DNA sequences from both adults and larvae. Specifically, seven species were identified based on adult wasps, while nine species were identified from the larvae. The application of DNA barcoding significantly enhanced our understanding of the diversity of dryinid species inhabiting the Xisha Islands, particularly in the genera Anteon and Gonatopus, which are two of the most speciose genera of Dryinidae.
For the genus Anteon, the validity of A. malaysianum was reinstated and an undescribed species was discovered. The undescribed Anteon species is morphologically similar to A. yasumatsui in body size and chela structure, but it is different from A. yasumatsui in having antennomeres four to seven times broader than long and coxae that are dark brown to black. The intraspecific pairwise distances between this undescribed species and A. yasumatsui is 7.5%, also suggesting that it is a distinctive species different from A. yasumatsui and probably representing a new species. However, we only have one specimen of this undescribed species, and more material is needed to confirm its identity. Traditionally, the morphological taxonomy of Anteon depends heavily on the chela of the female foreleg [1,13,14]. However, the validity of a species defined by the traditionally used characteristics, such as the length of notaulus and the structure of female chela, should be tested by rearing adult wasps from their host(s) or DNA analysis [2]. Among the three Anteon species found in this study, the female chelae are morphologically uniform, but their identities were confirmed by the combined analyses of the COI sequences and other morphological characteristics such as the color of the antennae and legs and the sculpture of the mesosoma. This indicates that DNA barcoding can aid in identifying valuable diagnostic morphological characteristics, thereby enhancing morphological species delimitation. DNA barcoding also serves as the bridge that facilitates the recognition of the members of the opposite sex [2,3,9,10,11]. For example, sexual dimorphism is particularly extreme in the genus Gonatopus: females of most species are wingless and males are fully winged. The adult males alone of many Gonatopus species are not identifiable, and most species have been described based solely on their females [1]. The sexual association of many Gonatopus species has previously been confirmed by rearing, although a few species have been confirmed with DNA sequences [9]. In this study, we confirmed the female–male association of two Gonatopus species, G. nearcticus and G. validus. In addition, the male of G. validus was discovered for the first time, indicating that DNA barcoding is a powerful tool to enhance the sexual association of the same species.
In total, 67 wasp larvae had their DNA barcodes sequenced and analyzed, leading to the identification of nine dryinid wasp species. However, only five of these species could be definitively assigned to a specific species. A more comprehensive reference COI data set of adult dryinid wasps in the future will help to confirm the host association of the four unidentifiable species of Gonatopus identified in this study [7]. Additional morphological characteristics of the developing wasp larvae within the host can also be used in genus and species determination. The position of the thylacium is generally characteristic of a dryinid taxa [25], but it can vary depending on the species and size of the host(s) [4]. Our findings are congruent with this perspective. The leafhoppers parasitized by Anteon species usually have the thylacium situated between the prothorax and mesothorax [1], which was the placement observed for A. malaysianum, whereas the thylacium position of the eight Gonatopus species was variable but always on the metasomal segments, positioned ventrally or dorsally.
The accurate identification of the host is just as important as the accurate identification of the parasitoid and allows for the categorization of the parasitoid as a generalist (parasitizes many host species) or specialist (parasitizes a single host species, genus, or family). The host of A. malaysianum was previously unrecorded, as it was treated as a synonym of A. yasumatsui, which has been reported to parasitize multiple host species [6]. In this study, we confirmed that B. incisa is the host of A. malaysianum. The host (F. daluoensis) of G. validus was discovered for the first time in this study. Additionally, using DNA barcoding, the host of G. viet was initially identified as Stirellus capitatus [7], but two additional host species, Deltocephalus vulgaris Dash & Viraktamath, 1998 and Exitianus nanus Distant, 1908, were discovered in this study, indicating that G. viet is a generalist. Although G. nearcticus and G. yasumatsui were recorded to parasitize B. saltuella and B. incisa, respectively, in this study, they previously have been reported as generalists [6]. Previous studies suggest that many dryinid species can parasitize different groups of hosts, and the current records of monophagous parasitism may be due to the insufficient investigation of parasitoid–host associations [7,26,27]. At least one study also suggested that unstable ecological conditions could lead to dryinid wasps colonizing accidental hosts [28]. Considering the small islet areas (Table 1) and limited host species available on the Xisha Islands, we would expect a generalist bias in the dryinid community, but we found more specialists (most species only parasitize one single host species) than generalists. This pattern may be due to our limited sample sizes, as some parasitoid–host interactions were found based on one or a few specimens. Nevertheless, our findings at least indicate that the population sizes of some dryinid species are extremely small on the Xisha Islands.
Island species usually have a small population size, and thus are more vulnerable to extinction [12], especially for species at high trophic levels. The dryinid–hopper interaction network of the Xisha Islands had a low connectance and nestedness, but a high specialization, suggesting that the network is unstable and some specialists are at risk of extinction. However, this conclusion should be viewed with some caution because the metrics measured from such interaction networks are sensitive to sampling bias, and our sampling effort was limited. The climate of the Xisha Islands can be categorized into two seasons, the dry season (October to March) and the rainy season (April to September), and studies have found that at least plant–pollinator networks show seasonal variations [29], which is most likely true for the parasitoid–host networks, as well. Nevertheless, the methods we used in this study provide an opportunity to recognize the interacting relationships of species at high trophic levels, which may help to develop better conservation strategies. Dryinids are the natural enemies of hoppers, which are pests of various plants on the islands; therefore, dryinids are important biological control agents to keep hopper pests in check [5]. One of the strategies to make use of dryinids in pest biological control is to develop conservation plans for local species. An accurate species identification and the confirmation of host associations are essential for developing conservation strategies.
5. Conclusions
By using an integrated taxonomic approach that combines morphological identification with DNA barcoding methods, we recognized 11 dryinid species present on the Xisha Islands, including a new species of Anteon. Furthermore, the hosts of most of the dryinid species and the characteristics of their interaction network were identified via DNA sequence analyses. Our study demonstrates the effectiveness of DNA barcoding methods in uncovering parasitoid diversity and assessing their host associations, which are crucial for devising conservation management strategies, particularly for taxa inhabiting oceanic islands.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani14243587/s1, Figure S1: Different habitats of the Xisha Islands. (A) Forest. (B) Mixed forest, shrub and herbaceous community. (C) Costal shrub and herbaceous community. (D) Herbaceous community; Figure S2: (A) Yellow pan trap. (B) Bottom-sealed emergence tent used with a sweep net and collecting tube. Figure S3. Anteon malaysianum Olmi, 1987, female (SCBG_E0009679). (A) Habitus, lateral view. (B) Head and mesosoma, dorsal view. (C) Head and mesosoma, lateral view. (D) Wings. (E) Head, frontal view. (F) Chela; Figure S4. Anteon yasumatsui Olmi, 1984, female (SCBG_E0009680). (A) Habitus, lateral view. (B) Head and mesosoma, dorsal view. (C) Head and mesosoma, lateral view. (D) Wings. (E) Head, frontal view. (F) Chela; Figur S5. Gonatopus nearcticus (Fenton, 1905), female (SCBG_E0009681). (A) Habitus, dorsal view. (B) Habitus, lateral view. (C) Mesosoma, dorsal view. (D) Mesosoma, lateral view. (E) Head, frontal view. (F) Chela; Figure S6. Gonatopus nearcticus (Fenton, 1905), male (SCBG_E0009682). (A) Habitus, larteral view. (B) Head and mesosoma, dorsal view. (C) Head and mesosoma, lateral view. (D) Wings. (E) Head, frontal view. (F) Antenna; Figure S7. Gonatopus validus (Olmi, 1984), female (SCBG_E0009674). (A) Habitus, dorsal view. (B) Habitus, lateral view. (C) Head and mesosoma, dorsal view. (D) Head and mesosoma, lateral view. (E) Head, frontal view. (F) Chela; Figure S8. Gonatopus validus (Olmi, 1984), male (SCBG_E0009671). (A) Habitus, lateral view. (B) Head and mesosoma, dorsal view. (C) Head and mesosoma, lateral view. (D) Wings. (E) Antenna. (F) Genitalia, ventral view; Figure S9. Gonatopus yasumatsui Olmi 1984, female (SCBG_E0009678). (A) Habitus, dorsal view. (B) Habitus, lateral view. (C) Head and mesosoma, dorsal view. (D) Head and mesosoma, lateral view. (E) Head, frontal view. (F) Chela; Figure S10. Gonatopus sp1, male (SCBG_E0009670). (A) Habitus, larteral view. (B) Head and mesosoma, dorsal view. (C) Head and mesosoma, lateral view. (D) Wings. (E) Head, frontal view. (F) Antenna; Table S1. Geographic coordinates and area of sampled islets; Table S2. Intraspecific pairwise distance of Dryinidae adults based on COI sequences (%); Table S3. Interspecific pairwise distance of Dryinidae adults based on COI sequences (%); Table S4. Network metrics of the parasitoid-host network on the Xisha Islands.
Author Contributions
Conceptualization: H.C. and M.O.; methodology: H.C.; investigation: H.C., M.O., J.W., Q.S. and S.L.; data analyses: H.C. and Q.S.; writing—original draft preparation: H.C. and M.O.; writing—review and editing: H.C., M.O., J.W., Q.S. and S.L.; supervision: J.W. and S.L.; funding acquisition: J.W. and S.L. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by the National Key R&D Program of China (Key Special Project for Marine Environmental Security and Sustainable Development of Coral Reefs 2021-400) and by the South China Botanical Garden, Chinese Academy of Sciences (Grant No: QNXM-01).
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
All data are available in this paper.
Acknowledgments
We thank Qingquan Xue (Northwest A&F University) and Yixin Huang (Anhui Normal University) for identifying some of the hopper species. We also extend our sincerest thanks to Zachary Lahey (USDA-ARS, U.S. Vegetable Laboratory) for improving the manuscript, to Guangyi Dai from the Institutional Center for Shared Technologies and Facilities of South China Botanical Garden–CAS for the SEM guidance, and to Lifang Xiao (Institute of Zoology, Guangdong Academy of Sciences) for the help with data analyses. The scientific expedition in 2019 was organized by South China Sea Institution of Sun Yat-sen University.
Conflicts of Interest
The authors declare no conflicts of interest.
References
- Olmi, M.; Copeland, R.S.; van Noort, S. Dryinidae of the Afrotropical region (Hymenoptera, Chrysidoidea). Zootaxa 2019, 4630, 1–619. [Google Scholar] [CrossRef] [PubMed]
- Olmi, M.; Chen, H.-Y.; Guglielmino, A.; Ødegaard, F.; Vollaro, M.; Capradossi, L.; Liu, J.-X. DNA barcoding of Aphelopus Dalman (Hymenoptera, Dryinidae) from China, with descriptions of four new species. Eur. J. Taxon. 2022, 794, 40–71. [Google Scholar] [CrossRef]
- Chen, H.-Y.; Olmi, M.; Ødegaard, F.; Capradossi, L.; Liu, J.-X. DNA Barcoding Unveils New Species of the Sexually Dimorphic Genus Anteon Jurine (Hymenoptera, Dryinidae) from China. Insects 2024, 15, 18. [Google Scholar] [CrossRef]
- Virla, E.G.; Moya-Raygoza, G.; Guglielmino, A. A review of the biology of the pincer wasps (Hymenoptera: Dryinidae). Austral Entomol. 2023, 62, 274–299. [Google Scholar] [CrossRef]
- He, J.; Xu, Z. Hymenoptera Dryinidae. Fauna Sinica, 29th ed.; Science Press: Beijing, China, 2002; p. 464. [Google Scholar]
- Guglielmino, A.; Olmi, M.; Bückle, C. An updated host-parasite catalogue of world Dryinidae (Hymenoptera: Chrysidoidea). Zootaxa 2013, 3740, 1–113. [Google Scholar] [CrossRef]
- Chen, H.-Y.; Olmi, M.; Pang, H.; Liu, J.-X. Application of DNA barcoding confirms the host of Gonatopus viet Olmi, 1986 (Hymenoptera, Dryinidae). ZooKeys 2020, 944, 115–120. [Google Scholar] [CrossRef]
- Olmi, M. The Dryinidae and Embolemidae (Hymenoptera: Chrysidoidea) of Fennoscandia and Denmark; Fauna Entomologica Scandinavica: Leiden, The Netherlands, 1994; p. 100. [Google Scholar]
- Mita, T.; Matsumoto, Y. First description of the male of Gonatopus javanus (R.C.L. Perkins) determined by mitochondrial COI sequence (Hymenoptera: Dryinidae). Entomol. Sci. 2012, 15, 214–218. [Google Scholar] [CrossRef]
- Olmi, M.; Mita, T.; Guglielmino, A.; Vollaro, M.; Vári, G. Application of DNA barcoding confirms the female, male, larva and host of Bocchus scobiolae Nagy, 1967 (Hymenoptera: Dryinidae). Zootaxa 2021, 4969, 563–572. [Google Scholar] [CrossRef]
- Mita, T.; Sanada–Morimura, S.; Matsumura, M.; Matsumoto, Y. Genetic variation of two apterous wasps Haplogonatopus apicalis and H. oratorius (Hymenoptera: Dryinidae) in East Asia. Appl. Entomol. Zool. 2013, 48, 119–124. [Google Scholar] [CrossRef]
- Paulay, G. Biodiversity on oceanic islands: Its origin and extinction. Am. Zool. 1994, 34, 134–144. [Google Scholar] [CrossRef]
- Available online: https://qgis.org (accessed on 7 April 2024).
- Xu, Z.; Olmi, M.; He, J. Dryinidae of the Oriental region (Hymenoptera: Chrysidoidea). Zootaxa 2013, 3614, 1–460. [Google Scholar] [CrossRef] [PubMed]
- Olmi, M.; Xu, Z. Dryinidae of the Eastern Palaearctic region (Hymenoptera: Chrysidoidea). Zootaxa 2015, 3996, 1–253. [Google Scholar] [CrossRef] [PubMed]
- Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef]
- Tribull, C.M. Phylogenetic relationships among the subfamilies of Dryinidae (Hymenoptera, Chrysidoidea) as reconstructed by molecular sequencing. J. Hymenopt. Res. 2015, 45, 15–29. [Google Scholar] [CrossRef]
- Dormann, C.F. Using Bipartite to Describe and Plot Two-Mode Networks in R; R Package Version 4; The R Project for Statistical Computing: Vienna, Austria, 2020; pp. 1–28. [Google Scholar]
- Available online: https://www.r-project.org (accessed on 22 May 2024).
- Vizentin-Bugoni, J.; Maruyama, P.K.; Debastiani, V.J.; Duarte, L.S.; Dalsgaard, B.; Sazima, M. Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network. J. Anim. Ecol. 2016, 85, 262–272. [Google Scholar] [CrossRef]
- Dunne, J.A.; Williams, R.J.; Martinez, N.D. Food-web structure and network theory: The role of connectance and size. PNAS 2002, 99, 12917–12922. [Google Scholar] [CrossRef]
- Blüthgen, N.; Menzel, F.; Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol. 2006, 6, 9. [Google Scholar] [CrossRef] [PubMed]
- Ratnasingham, S.; Hebert, P.D.N. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol. Ecol. Notes 2007, 7, 355–364. [Google Scholar] [CrossRef]
- Olmi, M. A contribution to the knowledge of Oriental Dryinidae (Hymenoptera: Chrysidoidea), with descriptions of two new species from India and Thailand. Orient. Insects 2005, 39, 345–352. [Google Scholar] [CrossRef]
- Waloff, N. Biology and behavior of some species of Dryinidae (Hym.). J. Entomol. 1974, 49, 97–109. [Google Scholar]
- Guglielmino, A.; Olmi, M. A host-parasite catalog of world Dryinidae (Hymenoptera: Chrysidoidea). Contrib. Entomol. Int. 1997, 2, 165–298. [Google Scholar]
- Becerra-Chiron, I.M.; Moya-Raygoza, G.; Muñoz-Urias, A. Host-Dryinidae (Hymenoptera) interactions on edge gases of maize agroecosystem throughout winter in Mexico. J. Hymenopt. Res. 2017, 57, 155–166. [Google Scholar] [CrossRef]
- Klejdysz, T.; Klukowski, Z.; Pruszyński, G.; Kubasik, W. New data and a checklist of Dryinidae (Hymenoptera) from Poland, and their role in controlling leafhopper and planthopper crop pests (Hemiptera: Cicadomorpha, Fulgoromorpha). Pol. J. Entomol. 2018, 87, 41–55. [Google Scholar] [CrossRef]
- Wang, X.; Zeng, T.; Wu, M.-S.; Zhang, D.-X. Seasonal dynamic variation of pollination network is associated with the number of species in flower in an oceanic island community. J. Plant Ecol. 2020, 13, 657–666. [Google Scholar] [CrossRef]
Figure 1.
Sampling sites and distribution of Dryinidae species collected in the Xisha Islands.
Figure 2.
Anteon sp., female (SCBG_E0009677). (A) Habitus, lateral view. (B) Head and anterior mesosoma, dorsal view. (C) Mesosoma, lateral view. (D) Posterior mesosoma, dorsal view. (E) Head, frontal view. (F) Chela.
Figure 2.
Anteon sp., female (SCBG_E0009677). (A) Habitus, lateral view. (B) Head and anterior mesosoma, dorsal view. (C) Mesosoma, lateral view. (D) Posterior mesosoma, dorsal view. (E) Head, frontal view. (F) Chela.
Figure 3.
Maximum Likelihood tree showing relationships between the studied dryinid species based on codon-aligned nucleotide sequences of COI. Bootstrap values of 50 and above are indicated at nodes. The scale bar represents 0.06 substitutions per site.
Figure 3.
Maximum Likelihood tree showing relationships between the studied dryinid species based on codon-aligned nucleotide sequences of COI. Bootstrap values of 50 and above are indicated at nodes. The scale bar represents 0.06 substitutions per site.
Figure 4.
Bipartite network representations of Dryinidae (left column) andhopper (right column) associations on the Xisha Islands. The rectangles represent dryinid species (left column) and host species (right column), and the connecting lines represent interactions between wasp and host species. The width of rectangles is proportional to species abundance, while the width of lines indicates interaction frequency.
Figure 4.
Bipartite network representations of Dryinidae (left column) andhopper (right column) associations on the Xisha Islands. The rectangles represent dryinid species (left column) and host species (right column), and the connecting lines represent interactions between wasp and host species. The width of rectangles is proportional to species abundance, while the width of lines indicates interaction frequency.
Table 1.
List of sequenced adult parasitoids and hosts.
| Code | Family | Species | Sex | Locality | GenBank Accession No. |
|---|---|---|---|---|---|
| Parasitoid | |||||
| SCBG_E0009677 | Dryinidae | Anteon sp. | female | Chenhang Is. | PP600740 |
| SCBG_E0009673 | Dryinidae | Anteon malaysianum Olmi, 1987 | female | Jinqin Is. | PP600741 |
| SCBG_E0009676 | Dryinidae | Anteon malaysianum Olmi, 1987 | female | Chenhang Is. | PP600742 |
| SCBG_E0009679 | Dryinidae | Anteon malaysianum Olmi, 1987 | female | Ganquan Is. | PP600743 |
| SCBG_E0009680 | Dryinidae | Anteon yasumatsui Olmi, 1984 | female | Ganquan Is. | PP600744 |
| SCBG_E0009681 | Dryinidae | Gonatopus nearcticus (Fenton, 1905) | female | Jinyin Is. | PP600745 |
| SCBG_E0009682 | Dryinidae | Gonatopus nearcticus (Fenton, 1905) | male | Jinyin Is. | PP600746 |
| SCBG_E0009671 | Dryinidae | Gonatopus validus (Olmi, 1984) | male | Yongxing Is. | PP600747 |
| SCBG_E0009674 | Dryinidae | Gonatopus validus (Olmi, 1984) | female | Lincoln Is. | PP600748 |
| SCBG_E0009675 | Dryinidae | Gonatopus validus (Olmi, 1984) | male | Lincoln Is. | PP600749 |
| SCBG_E0009672 | Dryinidae | Gonatopus yasumatsui Olmi 1984 | female | Jinqin Is. | PP600750 |
| SCBG_E0009678 | Dryinidae | Gonatopus yasumatsui Olmi 1984 | female | Chenhang Is. | PP600751 |
| SCBG_E0009670 | Dryinidae | Gonatopus sp1 | male | Yongxing Is. | PP600752 |
| SCAU_3011792 | Dryinidae | Gonatopus sp-BJ | male | Beijing | PP600753 |
| SCAU_3048892 | Dryinidae | Gonatopus sp-HK | male | Haikou | PP600754 |
| SCAU_3044110 | Dryinidae | Gonatopus sp-WZ | male | Wenzhou | PP600755 |
| Host | |||||
| SCBG_E0009800 | Cicadellidae | Balclutha incisa (Matsumura, 1902) | female | Jinqin Is. | PP600756 |
| SCBG_E0009803 | Cicadellidae | Balclutha incisa (Matsumura, 1902) | female | Jinqin Is. | PP600757 |
| SCBG_E0009808 | Cicadellidae | Balclutha incisa (Matsumura, 1902) | male | Jinqin Is. | PP600758 |
| SCBG_E0009824 | Cicadellidae | Balclutha incisa (Matsumura, 1902) | male | Chenhang Is. | PP600759 |
| SCBG_E0009827 | Cicadellidae | Balclutha saltuella (Kirschbaum, 1868) | female | Jinyin Is. | PP600760 |
| SCBG_E0009828 | Cicadellidae | Balclutha saltuella (Kirschbaum, 1868) | male | Jinyin Is. | PP600761 |
| SCBG_E0009950 | Cicadellidae | Cicadulina bipunctata (Melichar 1904) | male | Jinqin Is. | PP600762 |
| SCBG_E0009777 | Cicadellidae | Deltocephalus vulgaris Dash & Viraktamath, 1998 | male | Yongxing Is. | PP600763 |
| SCBG_E0009811 | Cicadellidae | Exitianus nanus (Distant, 1908) | male | Lincoln Is. | PP600764 |
| SCBG_E0009955 | Cicadellidae | Exitianus nanus (Distant, 1908) | female | Lincoln Is. | PP600765 |
| SCBG_E0009825 | Cicadellidae | Stirellus capitatus (Distant, 1918) | male | Yongxing Is. | PP600766 |
| SCBG_E0009781 | Delphacidae | Cemus nigromaculosus (Muir, 1917) | male | Yongxing Is. | PP600767 |
| SCBG_E0009791 | Delphacidae | Cemus nigromaculosus (Muir, 1917) | male | Yongxing Is. | PP600768 |
| SCBG_E0009832 | Delphacidae | Falcotoya daluoensis Ding, 2006 | female | Lincoln Is. | PP600769 |
| SCBG_E0009833 | Delphacidae | Sogatella kolophon (Kirkaldy, 1907) | female | Jinqin Is. | PP600770 |
Note: Is. = Island.
Table 2.
List of sequenced parasitoid nymphs.
| Code | Parasitoid Species | Host Species | Host Instar/Sex | Thylacium Position | Locality | GenBank Accession No. |
|---|---|---|---|---|---|---|
| SCBG-E0009800 | A. malaysianum | B. incisa | adult/female | between pro- and mesothorax | Jinqin Is. | PP738802 |
| SCBG-E0009895 | A. malaysianum | B. incisa | adult/female | between pro- and mesothorax | Chenhang Is. | PP738803 |
| SCBG-E0009827 | G. nearcticus | B. saltuella | adult/female | between T2 and T3 | Jinyin Is. | PP738804 |
| SCBG-E0009828 | G. nearcticus | B. saltuella | adult/male | between T2 and T3 | Jinyin Is. | PP738805 |
| SCBG-E0009834 | G. nearcticus | B. saltuella | adult/female | between T1 and T2 | Jinqin Is. | PP738806 |
| SCBG-E0009946 | G. nearcticus | B. saltuella | adult/female | between T2 and T3 | Jinqin Is. | PP738807 |
| SCBG-E0009947 | G. nearcticus | B. saltuella | adult/male | between T3 and T4 | Jinqin Is. | PP738808 |
| SCBG-E0009832 | G. validus | F. daluoensis | adult/female | between S2 and S3 | Lincoln Is. | PP738809 |
| SCBG-E0009777 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Yongxing Is. | PP738810 |
| SCBG-E0009778 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Yongxing Is. | PP738811 |
| SCBG-E0009942 | G. viet | D. vulgaris | adult/male | between S3 and S4 | Yongxing Is. | PP738812 |
| SCBG-E0009943 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Yongxing Is. | PP738813 |
| SCBG-E0009944 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Yongxing Is. | PP738814 |
| SCBG-E0009779 | G. viet | D. vulgaris | adult/male | between S5 and S6 | Lincoln Is. | PP738815 |
| SCBG-E0009780 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Lincoln Is. | PP738816 |
| SCBG-E0009787 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Ganquan Is. | PP738817 |
| SCBG-E0009789 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Ganquan Is. | PP738818 |
| SCBG-E0009788 | G. viet | D. vulgaris | adult/male | between S4 and S5 | Chenhang Is. | PP738819 |
| SCBG-E0009948 | G. viet | D. vulgaris | adult/male | between S3 and S4 | Jinqin Is. | PP738820 |
| SCBG-E0009811 | G. viet | E. nanus | nymph/male | between S4 and S5 | Lincoln Is. | PP738821 |
| SCBG-E0009825 | G. viet | S. capitatus | nymph/female | between S3 and S4 | Yongxing Is. | PP738822 |
| SCBG-E0009945 | G. viet | S. capitatus | nymph/female | between S5 and S6 | Lincoln Is. | PP738823 |
| SCBG-E0009797 | G. yasumatsui | B. incisa | adult/female | between T2 and T3 | Jinqin Is. | PP738824 |
| SCBG-E0009798 | G. yasumatsui | B. incisa | adult/female | between T3 and T4 | Jinqin Is. | PP738825 |
| SCBG-E0009799 | G. yasumatsui | B. incisa | adult/female | between T3 and T4 | Jinqin Is. | PP738826 |
| SCBG-E0009801 | G. yasumatsui | B. incisa | adult/male | between T3 and T4 | Jinqin Is. | PP738827 |
| SCBG-E0009802 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Jinqin Is. | PP738828 |
| SCBG-E0009803 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Jinqin Is. | PP738829 |
| SCBG-E0009804 | G. yasumatsui | B. incisa | nymph/male | between S4 and S5 | Jinqin Is. | PP738830 |
| SCBG-E0009805 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Jinqin Is. | PP738831 |
| SCBG-E0009806 | G. yasumatsui | B. incisa | nymph/male | between S3 and S4 | Jinqin Is. | PP738832 |
| SCBG-E0009807 | G. yasumatsui | B. incisa | nymph/male | between S4 and S5 | Jinqin Is. | PP738833 |
| SCBG-E0009808 | G. yasumatsui | B. incisa | nymph/male | between S5 and S6 | Jinqin Is. | PP738834 |
| SCBG-E0009809 | G. yasumatsui | B. incisa | nymph/male | between S3 and S4 | Jinqin Is. | PP738835 |
| SCBG-E0009810 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Jinqin Is. | PP738836 |
| SCBG-E0009812 | G. yasumatsui | B. incisa | adult/male | between T2 and T3 | Chenhang Is. | PP738837 |
| SCBG-E0009813 | G. yasumatsui | B. incisa | nymph/female | between S3 and S4 | Chenhang Is. | PP738838 |
| SCBG-E0009814 | G. yasumatsui | B. incisa | nymph/female | between T7 and T8 | Chenhang Is. | PP738839 |
| SCBG-E0009815 | G. yasumatsui | B. incisa | nymph/female | between S3 and S4 | Chenhang Is. | PP738840 |
| SCBG-E0009816 | G. yasumatsui | B. incisa | nymph/female | between S5 and S6 | Chenhang Is. | PP738841 |
| SCBG-E0009817 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Chenhang Is. | PP738842 |
| SCBG-E0009818 | G. yasumatsui | B. incisa | nymph/female | between S3 and S4 | Chenhang Is. | PP738843 |
| SCBG-E0009819 | G. yasumatsui | B. incisa | nymph/female | between S2 and S3 | Chenhang Is. | PP738844 |
| SCBG-E0009820 | G. yasumatsui | B. incisa | nymph/female | between S3 and S4 | Chenhang Is. | PP738845 |
| SCBG-E0009821 | G. yasumatsui | B. incisa | nymph/female | between S4 and S5 | Chenhang Is. | PP738846 |
| SCBG-E0009823 | G. yasumatsui | B. incisa | nymph/male | between T4 and T5 | Chenhang Is. | PP738847 |
| SCBG-E0009824 | G. yasumatsui | B. incisa | nymph/male | between T3 and T4 | Chenhang Is. | PP738848 |
| SCBG-E0009826 | G. yasumatsui | B. incisa | adult/female | between T2 and T3 | Jinyin Is. | PP738849 |
| SCBG-E0009896 | G. yasumatsui | B. incisa | adult/female | between T4 and T5 | Yongxing Is. | PP738850 |
| SCBG-E0009781 | Gonatopus sp1 | C. nigromaculosus | adult/male | between T3 and T4 | Jinqin Is. | PP738851 |
| SCBG-E0009782 | Gonatopus sp1 | C. nigromaculosus | adult/female | between T3 and T4 | Chenhang Is. | PP738852 |
| SCBG-E0009792 | Gonatopus sp1 | C. nigromaculosus | adult/female | between T1 and T2 | Yongxing Is. | PP738853 |
| SCBG-E0009793 | Gonatopus sp1 | C. nigromaculosus | nymph/male | between T2 and T3 | Yongxing Is. | PP738854 |
| SCBG-E0009829 | Gonatopus sp1 | C. nigromaculosus | adult/male | between S3 and S4 | Yongxing Is. | PP738855 |
| SCBG-E0009830 | Gonatopus sp1 | C. nigromaculosus | adult/male | between S3 and S4 | Yongxing Is. | PP738856 |
| SCBG-E0009783 | Gonatopus sp-BJ | C. nigromaculosus | adult/male | between T3 and T4 | Jinyin Is. | PP738857 |
| SCBG-E0009784 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T3 and T4 | Jinyin Is. | PP738858 |
| SCBG-E0009786 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T3 and T4 | Chenhang Is. | PP738859 |
| SCBG-E0009822 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T4 and T5 | Chenhang Is. | PP738860 |
| SCBG-E0009790 | Gonatopus sp-BJ | C. nigromaculosus | adult/male | between T4 and T5 | Yongxing Is. | PP738861 |
| SCBG-E0009791 | Gonatopus sp-BJ | C. nigromaculosus | adult/male | between T2 and T3 | Yongxing Is. | PP738862 |
| SCBG-E0009795 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T4 and T5 | Yongxing Is. | PP738863 |
| SCBG-E0009796 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T3 and T4 | Yongxing Is. | PP738864 |
| SCBG-E0009831 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T3 and T4 | Yongxing Is. | PP738865 |
| SCBG-E0009949 | Gonatopus sp-BJ | C. nigromaculosus | nymph/male | between T4 and T5 | Jinqin Is. | PP738866 |
| SCBG-E0009950 | Gonatopus sp-HK | C. bipunctata | adult/male | between T4 and T5 | Jinqin Is. | PP738867 |
| SCBG-E0009833 | Gonatopus sp-WZ | S. kolophon | adult/female | between T2 and T3 | Jinqin Is. | PP738868 |
Note: S = sternite, T = tergite, Is. = Island.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Chen, H.; Olmi, M.; Wang, J.; Sun, Q.; Luo, S. DNA Barcoding Reveals Species Diversity and Host Associations of Dryinidae Wasps (Insecta, Hymenoptera): A Case Study from the Xisha Islands in the South China Sea. Animals 2024, 14, 3587. https://doi.org/10.3390/ani14243587
AMA Style
Chen H, Olmi M, Wang J, Sun Q, Luo S. DNA Barcoding Reveals Species Diversity and Host Associations of Dryinidae Wasps (Insecta, Hymenoptera): A Case Study from the Xisha Islands in the South China Sea. Animals. 2024; 14(24):3587. https://doi.org/10.3390/ani14243587
Chicago/Turabian StyleChen, Huayan, Massimo Olmi, Jun Wang, Qilin Sun, and Shixiao Luo. 2024. "DNA Barcoding Reveals Species Diversity and Host Associations of Dryinidae Wasps (Insecta, Hymenoptera): A Case Study from the Xisha Islands in the South China Sea" Animals 14, no. 24: 3587. https://doi.org/10.3390/ani14243587
APA StyleChen, H., Olmi, M., Wang, J., Sun, Q., & Luo, S. (2024). DNA Barcoding Reveals Species Diversity and Host Associations of Dryinidae Wasps (Insecta, Hymenoptera): A Case Study from the Xisha Islands in the South China Sea. Animals, 14(24), 3587. https://doi.org/10.3390/ani14243587
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
