JHR 65: 141-148 (2018) gee, JOURNAL OF Se eret pesca
doi: 10.3897/jhr.65.24872 RESEARCH ARTICLE (ME Hymenoptera

http://jhr.pensoft.net The Insertional Society of ymenoptersts. RESEARCH

A new species of Anagyrus (Hymenoptera, Encyrtidae)
from Malaysia, parasitoid of Lanceacoccus sp.
(Hemiptera, Pseudococcidae)

Guo-Hao Zu', Xu Zhang’, Cheng-De Li?, Yan-Zhou Zhang?

| College of Horticulture and Landscape, Tianjin Agricultural University, 22 Jinjing Road, Tianjin, 300384,

China 2. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of
Sciences, 1 West Beichen Road, Beijing 100101, China 3 School of Forestry, Northeast Forestry University, 26
Hexing Road, Harbin, 150040, China

Corresponding author: Yan-Zhou Zhang (zhangyz@ioz.ac.cn)

Academic editor: P Jansta | Received 13 March 2018 | Accepted 17 July 2018 | Published 27 August 2018
http://zoobank. org/090 D44AE-6E5E-4767-A864-58E6 1 8ACIC30

Citation: Zu G-H, Zhang X, Li C-D, Zhang Y-Z (2018) A new species of Anagyrus (Hymenoptera, Encyrtidae) from
Malaysia, parasitoid of Lanceacoccus sp. (Hemiptera, Pseudococcidae). Journal of Hymenoptera Research 65: 141-148.
https://doi.org/10.3897/jhr.65.24872

Abstract
A new species of Anagyrus Howard, 1896 (Hymenoptera: Encyrtidae), A. minipedicellus Zu & Zhang
sp. n., is described from Borneo of Malaysia as a parasitoid of Lanceacoccus sp. (Hemiptera: Pseudococ-

cidae), and DNA barcoding of the new species is given.

Keywords

Chalcidoidea, Tetracneminae, Anagyrini, new species, Sabah

Introduction

Anagyrus Howard, 1896 is one of the most diverse genus of Encyrtidae, containing
282 species worldwide (Noyes 2017), which are mainly endoparasitoids of mealy-
bugs (Hemiptera: Pseudococcidae), but some Australian species have been recorded as
parasitoids of coccinellid (Coleoptera: Coccinellidae) (Noyes and Hayat 1994, Noyes
2000). The members of the genus are very important as biological control agents and
19 species have been used in biological control (Noyes 2000).

Copyright Guo-Hao Zu et al. 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.

142 Guo-Hao Zu et al. / Journal of Hymenoptera Research 65: 141-148 (2018)

The genus has got comparatively little attention in Malaysia. Noyes and Hayat (1994)
reviewed 74 species of Oriental Anagyrus and 8 species were reported from Malaysia: A.
chrysos Noyes & Hayat, 1994, A. ephyra Noyes & Hayat, 1994, A. luci Noyes & Hayat,
1994, A. malayensis Noyes & Hayat, 1994, A. saccharicola Timberlake, 1932, A. subtilis
Noyes & Hayat, 1994, A. thailandicus (Myartseve, 1979) and A. tricolor (Girault, 1913),
among them A. ephyra, A. malayensis and A. subtilis were described from Malaysia.

In the present paper, A. minipedicellus Zu & Zhang, sp. n. is described as new to
science, and a key to Malaysian species of Anagyrus is provided.

Material and methods

All the specimens in the present study were collected from Mt. Trus Madi by rearing,
then dissected and mounted in Canada balsam on slides following the method de-
scribed by Noyes (1982). Morphological terminology and abbreviations follow those
of Noyes and Hayat (1994) and Noyes (2000) with some modifications. Photographs
were taken with a digital CCD camera attached to an Olympus BX51 compound mi-
croscope, and most measurements were made from slide-mounted specimens using an

eye-piece reticle, except body length, AOL, OCL, OD, OOL, POL.

Molecular studies

Eight individuals of A. minipedicellus were used to obtain their DNA barcodes. Total
genomic DNA was extracted using the DNeasy Blood & Tissue Kit (Qiagen) follow-
ing the manufacturer's protocols. Polymerase chain reactions (PCR) were carried out in
50 pL reaction volumes using TaKaRa ExTaq Polymerase kit. Final volumes included
5 wL of 10xBuffer, 25 mM MgCl2, 2.5 mM dNTP mixture, 10 pmol of each primer,
1U of ExTag and 5 uL of genomic DNA. The COI gene fragment was amplified using
the primers FWPTF1 (Li et al. 2010) and Lep-R1 (Hebert et al. 2004). The PCR cycle
program for COI followed Hebert et al. (2003). Sequencing was performed directly
from positive products in both directions using BigDye v3.1 on an ABI 3730xl DNA
Analyzer (Applied Biosystems).

The following abbreviations are used in the text:

F1-6 funicular segments 1—6

AOL ~~ minimum distance between a posterior ocellus and anterior ocellus
OCL ~~ minimum distance between a posterior ocellus and occipital margin
OD longest diameter of an ocellus

OOL ~~ minimum distance between a posterior ocellus and eye margin
POL ~~ minimum distance between posterior ocelli

MT length of mid tibia

OL length of the ovipositor

IZCAS Institute of Zoology, Chinese Academy of Sciences, Beijing, China

A new species of Anagyrus (Hymenoptera, Encyrtidae) from Malaysia... 143

Systematics

Key to species of Anagyrus from Malaysia (females)

1 POre WinieviNtscatenin APICAND# De. u.iiansproutedeisutenatonttconsaanecnd A. thailandicus
-. Bore swatie Ny aline say. ttt. aste- ane laseneansuneuclghsisnc ands dc Betees ae alone Mae nlonsairated Sauauiets 2
2 Hedduuinicolorous, dark. brown, On black )..2.0%5 dian ke divol Sap reautteh Sen tvucyeitosb ois 3
— Fleadtateleast partially, Orance sc. cust stouinewunvncaseetiee te loeuth sioeskadbeolvasenSeleinett, 5
3 miitenna with: BI =Podark: DrOWMs. 00. vos tote apetcewsees aeeeacterseee A, tricolor
Z Antenna with at least F4 and F5 yellow or white..........eceesseeseeeneeeeeeeeeeeees 4
4 Ovipositor clearly exserted, the exserted part at least about 2/3 length of mid
tibial spur; occipital margin behind posterior ocelli with a sharp raised ca-
PUBL eer tee rete con ce car ee a os eee anette eee ou eC eee Sees ete canta A. malayensis
- Ovipositor not or hardly exserted; occipital margin behind posterior ocelli
Siakp DULewithOutaMaised.catinal:t..ep wee NO ean Mite alee A, luci
5 Only F1 dark brown, remaining segments of funicle white... eee 6
— Funicle with at least FI-F3 completely or partially dark brown............0..... 7,
6 Body quite flattened and elongate; fore wing nearly 2.5x as long as broad;
ovipositor about 1.5x as long as mid tibia... eee A, saccharicola
— Body stout, not elongate and not dorsoventrally flattened; fore wing about 2x
as long as broad; ovipositor slightly shorter than mid tibia............ A. chrysos
vi F1 clearly longer than pedicel; F6 brown ................ A. minipedicellus sp. n.
F1 at least slightly shorter than pedicel; F6 yellow or white... eee 8
8 Ovipositor about 0.69x as long as mid tibia; F1 much shorter than any other
finteri arise give nits he. se tsa sece - sc ealewna since hacker tela ektssee ato ccastesccets A, subtilis

- Ovipositor about 1.17x as long as mid tibia; F1 similar to others ...A. ephyra

Anagyrus minipedicellus Zu & Zhang, sp. n.
http://zoobank.org/CE3B 1297-EAE9-473A-BCF7-EE75B78BB162
Figs 1-18

Holotype. & [on slide], MALAYSIA, Sabah, Mt. Trus Madi, 5°26'27"N; 116°27'0"W,
c. 1180m, 8.1I.2017, Guo-Hao Zu, rearing from Lanceacoccus sp. (Hemiptera: Pseu-
dococcidae) (Fig. 1) (IZCAS).

Paratypes. 42, 43 [49 24 on slides], the same data as holotype (IZCAS). 159,
35 [22, 14 on slides], MALAYSIA, Sabah, Mt. Trus Madi, 5°26'27"N; 116°27'0"W,
c. 1180m, 3.IV.2017, Xu Zhang rearing from Lanceacoccus sp. (Hemiptera: Pseudoc-
occidae) (IZCAS).

Diagnosis. Female. Length, excluding ovipositor, 1.38-1.83 mm. Body stout
(Fig. 2); head generally orange with interantennal prominence and gena below mid eye
level dark brown; scape dark brown, with a white subapical band; pedicel and funicle
generally dark brown; clava white; mesosoma and metasoma mostly dark brown, ex-
cept mesopleuron orange; frontovertex nearly 0.4x head width; clypeal margin slightly

144 Guo-Hao Zu et al. / Journal of Hymenoptera Research 65: 141-148 (2018)

Figures 1-3. | Lanceacoccus sp.; A. minipedicellus sp. n.: 2. habitus, lateral view (female, paratype) 3 habitus,
lateral view (male, paratype). Scale bars: 1mm.

emarginate; antennal scape strongly broadened, about twice as long as broad; pedicel
shorter and narrower than F1; all funicular segments at least 1.5x as long as broad; fore
wing completely hyaline, 2.15x as long as broad; costal cell broad, with four complete
lines of setae ventrally; ovipositor about 0.7x as long as mid tibia.

Male (length, 1.22—1.33 mm): Color similar to female (Fig. 3), except head com-
pletely black, flagellum black, gradually becoming yellowish distad; antenna with scape
about twice as long as broad, all funicular segments much longer than broad, F1 the
longest; scale-like sensilla present only on F6; frontovertex nearly half head width; fore
wing 2.08x as long as broad, costal cell ventrally with four lines of setae; metasoma short-
er than mesosoma; phallobase without digiti; aedeagus about 1.6x as long as mid tibia.

Description. Female. Holotype. Length, 1.83 mm (excluding ovipositor). Head
generally orange, interantennal prominence dark brown, gena dark brown to mid eye
level, occiput mostly dark brown. Antenna with radicle dark brown; scape dark brown

A new species of Anagyrus (Hymenoptera, Encyrtidae) from Malaysia... 145

with a white subapical band; pedicel and funicle black, funicle gradually becoming
paler distad and ventrally paler, clava white. Mesosoma dark brown; mesopleuron or-
ange. Wings hyaline. Legs generally yellowish white, except dorsal and ventral margins
of fore coxa, fore and mid femora, hind tibia dark brown, mid coxa mostly dark brown,
hind coxa brown, all tarsi yellowish brown. Metasoma dark brown.

Head. Frontovertex 0.37x head width, with very fine scale-like sculpture; setae on
frontovertex about half as long as diameter of anterior ocellus; ocelli forming an angle
of about 85°; posterior ocellus slightly closer to occipital margin than to eye margin;
eye reaching occipital margin, with dense, dark brown setae, each seta about 1.5x as
long as a facet width; head, in frontal view (Fig. 4), slightly (1.12x) wider than high;
antennal torulus with its dorsal margin well above lower margin of eyes and separated
from mouth margin by about its own height; antennal scrobes moderately deep; cl-
ypeal margin slightly emarginate. Antennal scape (Fig. 6) strongly broadened and flat-
tened, 1.9x as long as broad; pedicel short, 1.45x as long as broad, 0.75x as long as F1;
all funicular segments at least 1.5x as long as broad and subequal in length; clava 3.3x
as long as broad, shorter than preceding three funicular segments combined; funicle
with linear sensilla on all segments. Measurements (um): head high 600; head width
670; frontovertex width 250; OD 66; POL 110; OOL 29; OCL 23; AOL 58; eye
length 420; malar space 180; length and (width) — radicle 90; scape 360 (190); pedicel
90 (62); F1 120 (80); F2 130 (80); F3 130 (80); F4 130 (80); F5 120 (80); F6 120
(78); clava 330 (100).

Mesosoma (Fig. 5) dorsally with fine sculpture as on frontovertex; posterior mar-
gin of pronotum broadly concave; scutellum 1.13x as wide as long, pointed apically,
and almost as long as mesoscutum. Fore wing (Fig. 7) moderately broad, about 2.2x
as long as width; linea calva interrupted by 3 rows of setae and closed posteriorly by
2-3 rows of setae; costal cell broad, about 5.2x as wide as submarginal vein and 11x
as long as broad, ventrally with four complete lines of setae; stigmal vein longer than
marginal and postmarginal veins combined; hind wing (Fig. 8) 3x as long as broad.
Length of mid tibial spur (Fig. 9) 0.28x mid tibia and shorter than corresponding basi-
tarsus. Measurements (um): fore wing length 1825; fore wing width 850; submarginal
vein 710; marginal vein 38; postmarginal vein 58; stigmal vein 130; hind wing length
1125; hind wing width 375; MT 760; mid tibial spur 210; mid basitarsus 250.

Metasoma 0.86x as long as mesosoma; ovipositor (Fig. 11) 0.70x as long as mid
tibia, hardly exserted. Measurements (um): ovipositor length 535; gonostylus length
115; last tergite length 640; last tergite width 610.

Variation. Length of female, excluding ovipositor, varies from 1.38-1.83 mm,
scape in smaller species as in Fig. 6B, colour of F6 in some specimens is paler, ventral
1/3 dark brown, dorsal 2/3 nearly white mixed with brown, otherwise very little in
material available.

Male. Length 1.22—1.33 mm. Color is similar to that of female except head
completely black, flagellum gradually going from dark brown to yellowish. Antenna
(Fig. 14) with scape about 2.02x as long as broad, all funicular segments much longer
than broad, F1 the longest; longest flagellar setae about 1.5x as long as diameter of
corresponding segments; scale-like sensilla present only on F6; antennal torulus with

146 Guo-Hao Zu et al. / Journal of Hymenoptera Research 65: 141-148 (2018)

Figures 4-11. A. minipedicellus sp. n., holotype female: 4 head, frontal view 5 mesosoma, dorsal view
6 antenna (A holotype, B paratype) 7 fore wing 8 hind wing 9 legs 10 hypopygium II ovipositor. Scale
bars: 100m.

lower margin slightly below lower margin of eye and separated from mouth margin by
about 1.46x its own height; frontovertex nearly (Fig. 12) 0.49x head width. Fore wing
(Fig. 15) 2.08x as long as broad, costal cell ventrally with four lines of setae. Metasoma
shorter than mesosoma; phallobase (Fig. 18) without digiti; aedeagus about 1.57x as
long as mid tibia. Otherwise similar to female.

Host. Lanceacoccus sp. (Hemiptera: Pseudococcidae).

Etymology. The specific name refers to the small pedicel of female antennae.

Comments. This species is similar to A. alami Hayat, 1970 in the short and nar-
row pedicel. However, it can be easily separated from A. alami by its dark brown body
(generally yellowish in alami), F1 1.33x as long as pedicel (twice in A. alami), MT
1.42x as long as OL (1.05x in borneensis).

A new species of Anagyrus (Hymenoptera, Encyrtidae) from Malaysia... 147

Figures |2-18. A. minipedicellus sp. n., paratype male: 12 head, frontal view 13 mesosoma, lateral view
14 antenna 15 fore wing 16 hind wing 17 legs 18 genitalia. Scale bars: 100pm.

It is also probably close to A. subtilis Noyes & Hayat, 1994 and A. aceris Noyes &
Hayat, 1994, but differs in the short pedicel, which is 0.75x as long as F1 (at least longer
than F1 in A. subtilis and A. aceris), normal F1, which is similar to other funicular seg-
ments (Fl much shorter than any other funicular segments in A. subtilis), dark brown
radicle (orange in A. subtilis), subparallel eye margins (diverging ventrally in A. aceris)
and generally orange mesosoma (dorsum of mesosoma dark brown in A. aceris).

Molecular studies

The COI sequences the eight individuals of A. minipedicellus were successfully generat-
ed with high quality. All sequences have been deposited in GenBank (Accession Num-
bers: MH587108—MH587115). Only one base pair changes was detected between

148 Guo-Hao Zu et al. / Journal of Hymenoptera Research 65: 141-148 (2018)

the eight individuals sequenced for COI. Blasting the COI sequences gave no close
matches (over 90%) both on BOLD and GenBank. In GenBank, a COI sequence of
Anagyrus (Anagyrus nr. pseudococci PLCO02, Accession No. KU499515) differs from
those of the new species by about 14%.

Acknowledgements

This project was supported by the Scientific Project of Tianjin Municipal Education
Commission (No. 2017KJ185). We are grateful to Dr. Xu-Bo Wang (Beijing Forestry
University) for the identification of host species.

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