A new species of Cheiloneurus Westwood (Hymenoptera, Encyrtidae) as a hyperparasitoid of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley, in China

Zhuomiao Li; Tingting Yao; Zhihong Xu; Ling Meng; Baoping Li

doi:10.3897/zookeys.974.55528

Research Article

A new species of Cheiloneurus Westwood (Hymenoptera, Encyrtidae) as a hyperparasitoid of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley, in China

Zhuomiao Li^‡, Tingting Yao^‡, Zhihong Xu^§, Ling Meng^‡, Baoping Li^‡

‡ Nanjing Agricultural University, Nanjing, China

§ Zhejiang Agriculture & Forestry University, Lin’an, China

Corresponding author: Baoping Li ( lbp@njau.edu.cn )

Academic editor: Andreas Köhler

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: Li Z, Yao T, Xu Z, Meng L, Li B (2020) A new species of Cheiloneurus Westwood (Hymenoptera, Encyrtidae) as a hyperparasitoid of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley, in China. ZooKeys 974: 23-29. https://doi.org/10.3897/zookeys.974.55528

ZooBank: urn:lsid:zoobank.org:pub:87F93B60-FD12-44CA-BE72-BCF1B20FCABA

Abstract

A new species, Cheiloneurus nankingensis sp. nov., from Eastern China is described. It is similar to C. arabiacus Hayat but distinct from it in a number of morphological characters. It is a hyperparasitoid with the encyrtid wasp Aenasius arizonensis Girault, 1915 as the primary host and the cotton mealybug Phenacoccus solenopsis Tinsley, 1898 (Hemiptera: Pseudococcidae) as the secondary host. A key to all seven species of Cheiloneurus known from China is presented.

Keywords

Aenasius arizonensis, bambawalei, biological control, hyperparasitism, Nanjing

Introduction

Hyperparasitoids are specialized natural enemies of primary parasitoids but their negative effects on biological control have often been overlooked. Hyperparasitoids may directly impact their primary parasitoid by parasitizing their offspring and host-feeding (Sullivan 1987; Godfray 1994). Besides, the presence of hyperparasitoids may cause dispersal and patch leaving of their primary parasitoids to further influence biological control efficacy (Cusumano et al. 2019). Hyperparasitoids are often mistakenly regarded as primary parasitoids when they are collected from reared herbivorous hosts that have been parasitized. For example, while Cheiloneurus (Encyrtidae) has been recorded as a hyperparasitoid of the cotton mealybug Phenacoccus solenopsis Tinsley, 1898 (Hemiptera, Pseudococcidae) in North America (Fuchs et al. 1991), it was considered as a primary parasitoid of the mealybug in China (Li et al. 2020).

Phenacoccus solenopsis, native to North America, has spread to Asia over the past two decades (Tong et al. 2018). Since entering China, it has spread over a wide area and caused serious concern over its damage to a variety of economic crop plants (Wang et al. 2020). Biological control with natural enemies provides an alternative approach to managing this invasive pest. Numerous species of parasitoid wasps have been known attacking P. solenopsis in invaded Asia countries (Hayat 2009; Chen et al. 2011; Li et al. 2020). Yet few hyperparasitoids of the mealybug have been discovered in these areas.

Here, a hyperparasitoid wasp new to science is named Cheiloneurus nankingensis sp. nov. It was collected from rearing mummified P. solenopsis mealybugs on okra Abelmoschus esculentus (Linn.) Moench. Laboratory observation showed that C. nankingensis adults produce offspring when attacking the mealybugs that had been parasitized by Aenasius arizonensis Girault, 1915, but failed to do so when confined with healthy mealybugs, indicating that A. arizonensis is the host. This host parasitoid, having been synonymized with A. bambawalei Hayat, 2009, belongs to the subfamily Tetracneminae in Encyrtidae (Fallahzadeh et al. 2014). It was originally recorded in the USA and is now widespread in Asia where it is generally considered to be a potential biological control agent of the invasive cotton mealybug (Chen et al. 2011; Fallahzadeh et al. 2014; Aga et al. 2016; Li et al. 2020). Yet, its potential may be compromised by hyperparasitoids.

Cheiloneurus includes more than 140 species over the world, and all species, for which their biologies are known, are hyperparasitoids, attacking a wide range of parasitoid wasp taxa (Trjapitzin and Zuparko 2004). Six species of Cheiloneurus have been recorded from across mainland China, mostly with mealybugs as their secondary hosts; their primary hosts are unknown, except for C. claviger Thomson, 1876, which parasitizes Microterys encyrtid wasps (Xu and Huang 2004; Mita et al. 2016).

Materials and methods

Sample individuals of the cotton mealybug were collected from okra plants in a vegetable field and then maintained on potato Solanum tuberosum L. seedlings in an insectary. Parasitized mealybug mummies were individually placed in glass vials in which a cotton ball soaked with a 10% honey solution was provided as supplementary food. Cheiloneurus adults were mounted on slides following the methods described by Noyes (1982) for identification under a stereoscope (Nikon SMZ25, with NIS-Elements BR software for taking measurements and Zerene Stacker for processing photographs).

The terminology follows Noyes and Hayat (1984).

The following abbreviations are used in the description: POL, distance between the posterior ocelli; OOL, distance between a posterior ocellus and the corresponding eye margin; F1, F2, …, F6, first through sixth funicle segments; NAU, Nanjing Agricultural University, Nanjing, China.

Taxonomy

Cheiloneurus nankingensis Li & Xu, sp. nov.

http://zoobank.org/0A0CAA90-9BAD-4A04-8E4A-64851CE36387

Fig. 1[female], Fig. 2[male]

Type materials

Holotype. ♀; China, Jiangsu province: Nanjing city, NAU-affiliated Pailou Experiment station; alt. 18 m; 32°01'10"N, 118°51'21"E; October 2019; Zhuomiao Li leg. Paratypes. ♀; 15 individuals, same data as for holotype.

Deposition

The type specimens are deposited in the Department of Plant Protection, School of Agriculture and Food Science, Zhejiang Agri & Forest University, Li-an district, Hangzhou city, Zhejiang, China.

Etymology

The species name is derived from the name of the city, Nanjing, where the holotype was collected.

Distribution

All specimens were collected in an eastern suburb of Nanjing city, Jiangsu province, East China.

Figure 1.

Cheiloneurus nankingensis sp. nov. (female, holotype) A mesosoma, dorsal view B metasoma, dorsal view C antennae D mandibles E fore wing F head, front view G head, ventral view. Scale bars: 0.10 mm.

Description

Female. Holotype, body length 1.54 mm; other females ranged from 1.1 to 1.8 mm. Head dark brown, with purple sheen; ocelli reddish brown; compound eye dark brown; scape, pedicel yellowish brown; funicle and clava black, except first funicle segment with narrow strip of yellowish brown on ventral margin; pronotum and mesoscutum black with yellowish green sheen and silvery white setae; tegulae, axillae, scutellum yellowish brown except middle third of scutellum yellowish white; ventral and lateral sides of thorax dark brown with dark purple sheen; propodeum dark brown. Fore wing infuscated, with basal third, apex narrowly and rectangular area behind stigmal vein, hyaline; hyaline area in basal third with oblique infuscate streak; veins brown; hind wing hyaline. Fore and mid legs yellowish brown except middle part of mid tibia brown; hind femora and tibia brown except tibial base white.

Head: in dorsal view, 0.77 × as broad as high; head width 3.29 × frontovertex width; occipital margin rounded; ocelli arranged in equilateral triangle; POL and OOL 2.02 × and 0.30 × as long as diameter of anterior ocellus respectively; anterior ocellus separated with posterior ocelli by distance 1.01 × as long as POL; frontovertex with scaly reticulations. In frontal view, 0.79 × as broad as high; toruli separated by 1.93 × their own longest diameters; upper margin below lowest level of compound eye; toruli separated from clypeus by distance 0.73 × as long as longest diameter of torulus; mandible tridentate, teeth acute; maxillary palpi with four segments with rounded apex.

Antennae: scape cylindrical, 8.27 × as long as broad; pedicel 2.23 × as long as wide and 1.26 × as long as F1. F6 shortest segment; F1 and F2 longer than wide, the ratio of length to width 1.60 and 1.13, respectively; F3–F6 wider than long, the ratio of length to width 0.87, 0.67, 0.67, 0.64, respectively; club 1.78 × as long as broad, slightly shorter than preceding three funicle segments combined, clava with second suture slightly oblique.

Mesosoma: mesoscutum with striated or scaly reticulations and usually with distinct silvery white setae; notauli virtually absent; axillae and scutellum flat and usually with sculpture scaly; apex of scutellum with a tuft of bristles (bristles are easily lost at making slide but their swelling bases are recognizable); hind margin of scutellum reaching base of propodeum; mesopleura smooth, reaching base of abdomen; propodeum smooth.

Fore wings: 3.01 × as long as broad, with uniform cilia except basal third; submarginal vein with about five setae; submarginal vein 3.90 × as long as stigmal vein; linea calva closed anteriorly by two or three lines of setae and posteriorly closed by 11 or 12 lines of hyaline setae.

Legs: a row of spines at apex of mid tibia; tibial spur 0.96 × as long asbasitarsus ; basitarsus longer than tarsal segments 2–4.

Metasoma: oblong in dorsal view. Ovipositor sheaths yellow. Exserted part of ovipositor sheaths (from slide) 0.15 × gaster length.

Measurements (from slide): length of mid tibia 0.65 mm, mesosoma 0.73 mm, metasoma 0.70 mm, forewing 1.25 mm.

Figure 2.

Cheiloneurus nankingensis sp. nov. (male) A fore wing B antennae C head, front view D head, ventral view E mesosoma, dorsal view F metasoma, dorsal view. Scale bars: 0.10 mm.

Male. Length 1.07 mm. Body black. Antennae slender with radicle, scape and pedicel dark yellowish brown; funicle and clava black. Oval compound eye and ocelli black. Legs yellowish brown.

Head: in frontal view, approximately triangular with scaly reticulations, 0.97 × as broad as high; POL and OOL 3.00 × and 0.92 × as long as diameter of anterior ocellus, respectively; toruli separated by 0.83 × their own longest diameters; mandible bidentate; toruli diameters 0.69 × and 2.26 × as long as POL and OOL, respectively; distance between compound eyes 3.45 × as long as that between toruli.

Antennae: scape cylindrical, 6.53 × and 0.46 × as long as broad and head height, respectively; pedicel triangular; clava unsegmented, longer than F5–F6 combined; scape 3.35, 1.62, 1.95, 2.13, 2.14, 2.15, 2.18, and 1.05 times as long as pedicel, F1–F6, and clava, respectively; F1 slightly longer than F2–F6 separately; F2–F6 nearly same length; ratio of length to width 2.57, 2.20, 2.30, 2.22, 2.15, and 2.18 for F1 to F6, respectively.

Mesosoma: In dorsal view, 1.35 × as long as width; mesoscutum, axillae, and scutellum with sculpture scaly and similar to head sculpture; scutellum 0.97 × as long as height; setae and notauli virtually absent.

Fore wings: 2.42 × as long as broad; submarginal vein with about 13 setae; postmarginal and submarginal veins 0.58 × and 10.65 × as long as stigmal vein.

Legs: mid tibia with row of spines apically; spur 1.08 × as long as basitarsus.

Metanotum: nearly triangular in dorsal view. Shorter than thorax.

Measurements (from slide): mesosoma length 0.55 mm, metasoma length 0.43 mm, antennae 0.86 mm, and mid tibia length 0.43 mm.

Diagnosis

This new species resembles C. arabiacus Hayat, (2014) but differs from it in the following respects (compared with C. arabiacus in brackets): without an infuscate area below proximal half of parastigma (with it); scape cylindrical (slightly expanded in the middle); pedicel as long as F1 (longer than F1–F2 combined); F3 quadrate or slightly broader than long (F3 longer than broad); F4–F6 broader than long (F4, F5 quadrate); clava shorter than F4–F6 combined (longer than F4–F6 combined); head in frontal view higher than broad (broader than high); mandible with three acute teeth (with two acute and one round teeth).

Biology

Little has been known about biology of this new species. It is a hyperparasitoid with the encyrtid wasp A. arizonensis as the host, which is a primary and solitary parasitoid of the cotton mealybug P. solenopsis. This hyperparasitoid attacks only mealybugs that have already been parasitized by A. arizonensis and the number of offspring hyperparasitoids ermerging from a mummified mealybug ranges from one to 18. The prevalence of hyperparasitism by this wasp across the range of the cotton mealybug remains to be investigated.

Key to females of Cheiloneurus species known from China

1	Scutellum without a tuft of bristles at apex	C. exitiosus Perkins, 1906
–	Scutellum with a tuft of bristles at apex	2
2	Scape cylindrical; clava slightly broader than funicle	3
–	Scape slightly expanded in the middle; clava clearly broader than funicle	5
3	F1–F6 longer than wide, entirely whitish	4
–	Only F1–F2 longer than wide; funicle blackish	C. nankingensis sp. nov.
4	Pedicel as long as F1; clava as long as F4–F6 combined	C. quercus Mayr, 1876
–	Pedicel longer than F1; clava as long as F3–F6 combined	C. sinensis Özdikmen, 2011
5	Fore wing apex narrowly hyaline; funicle entirely blackish	C. axillaris Hayat, Alam & Agarwal, 1975
–	Fore wing apex narrowly not hyaline; some funicular segments whitish	6
6	F4–F5 whitish with a brown stripe on ventral margin	C. chinensis Shi, 1993
–	F4–F5 entirely whitish	C. claviger Thomson, 1876

Acknowledgements

We thank Jirui Wang at Zhejiang Agri & Forest University for processing the specimen deposition and offering suggestions for the study, Changhai Sun and Xinyu Ge for help with the photography, Jingya Liu for help in rearing mealybugs, and Jiajia Zhao for the information about the mealybug infestation site. This work was supported by the National Key R&D Program of China (2017YFE0104900).

References

Aga TM, Tambe VJ, Nagrare VS, Naikwadi B (2016) Parasitoid, Aenasius arizonensis (Girault) (Hymenoptera: Encyrtidae): Its biology, morphometrics, host stage preference and use in biological control. Journal of Biological Control 30(2): 91–98. https://doi.org/10.18641/jbc/30/2/95751

Chen HY, He LF, Zhen CH, Li P, Yi JH, Xu ZF (2011) Survey on the natural enemies of mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) from Guangdong and Hainan, China. Journal of Environmental Entomology 33(2): 269–272. https://en.cnki.com.cn/Article_en/CJFDTotal-KCTD201102023.htm

Cusumano A, Harvey JA, Bourne ME, Poelman EH, Boer J (2019) Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests. Pest Management Science 76: 432–443. https://doi.org/10.1002/ps.5679

Fallahzadeh M, Japoshvili G, Abdimaleki R, Saghaei N (2014) New records of Tetracneminae (Hymenoptera, Chalcidoidea, Encyrtidae) from Iran. Turkish Journal of Zoology 38: 515–518. https://doi.org/10.3906/zoo-1309-28

Fuchs TW, Stewart JW, Minzenmayer R, Rose M (1991) First record of Phenacoccus solenopsis Tinsley in cultivated cotton in the United States. Southwestern Entomologist 16: 215–221.

Godfray HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey, 221 pp. https://doi.org/10.1515/9780691207025

Hayat M (2009) Description of a new species of Aenasius Walker (Hymenoptera: Encyrtidae), India. Biosystematica 3: 21–26.

Hayat M, Ahmad Z, Khan FR (2014) Encyrtidae (Hymenoptera: Chalcidoidea) from the Kingdom of Saudi Arabia. Zootaxa 3793(1): 22–24. https://doi.org/10.11646/zootaxa.3793.1.1

Li J, Deng J, Chen H, Yang L, Zhou Z, Jiaqng J, Huang L, Gui F, Chen J (2020) Investigation on the occurrence of parasitic wasps of Phenacoccus solenopsis Tinsley in Guangxi. Journal of Southern Agriculture 51(4): 853–861.

Mita T, Handa H, Higashiura Y, Japoshvili G (2016) First report of Cheiloneurus exitiosus (Perkins, 1906) and Helegonatopus dimorphus (Hoffer, 1954) (Hymenoptera: Encyrtidae) from Japan, with remarks on their abundance in rice paddies. Biodiversity Data Journal 4: e9230. https://doi.org/10.3897/BDJ.4.e9230

Noyes JS (1982) Collecting and preserving chalcid wasp (Hymenoptera: Chalcidoidea). Journal of Natural History 16: 315–334. https://doi.org/10.1080/00222938200770261

Noyes JS, Hayat M (1984) A review of the genera of Indo-Pacific Encyrtidae (Hymenoptera: Chalcidoidea). Bulletin of the British Museum (Natural History), Entomology 48(3): 131–395. https://www.biodiversitylibrary.org/page/2288550

Sullivan DJ (1987) Insect hyperparasitism. Annual Review of Entomology 32: 49–70. https://doi.org/10.1146/annurev.en.32.010187.000405

Trjapitzin VA, Zuparko RL (2004) A synopsis of the genus Cheiloneurus Westwood, 1833 (Hymenoptera: Chalcidoidea: Encyrtidae) of the New World. Russian Entomological Journal 13: 257–266.

Tong H, Ao Y, Li Z, Wang Y, Jiang M (2018) Invasion biology of the cotton mealybug, Phenacoccus solenopsis Tinsley: current knowledge and future directions. Journal of Integrative Agriculture 17: 60345–60347. http://lib.cqvip.com/Qikan/Article/Detail?id=7001765165.

Xu Z, Huang J (2004) Chinese Fauna of Parasitic Wasps on Scale Insects. Shanghai Scientific & Technical Publishers, Shanghai, 524 pp.

Wang Y, Dai T, Tian H, Wang F, Zhang G (2020) Range expansion of the invasive cotton mealybug, Phenacoccus solenopsis Tinsley: an increasing threat to agricultural and horticultural crops in China. Journal of Integrative Agriculture 19(3): 881–885. https://doi.org/10.1016/S2095-3119(19)62765-6