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Desc ip ion o wo new Quad as ichus
(Hymenop e a: Eulophidae) ea ed om
Li chiomyia chinensis (Dip e a: Cecidomyiidae) on
comme cial lychee (Li chi chinensis; Sapindaceae)
in Taiwan
Michael W. Ga es , Yi-Min Chao , Sheng-Feng Lin & Man-Miao Yang
To ci e his a icle: Michael W. Ga es , Yi-Min Chao , Sheng-Feng Lin & Man-Miao Yang (2020)
Desc ip ion o wo new Quad as ichus (Hymenop e a: Eulophidae) ea ed om Li chiomyia
chinensis (Dip e a: Cecidomyiidae) on comme cial lychee (Li chi�chinensis; Sapindaceae) in
Taiwan, Jou nal o Na u al His o y, 54:9-12, 635-646, DOI: 10.1080/00222933.2020.1779367
To link o his a icle: h ps://doi.o g/10.1080/00222933.2020.1779367
Published online: 23 Sep 2020.
Submi you a icle o his jou nal
A icle iews: 11
View ela ed a icles
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Desc ip ion o wo new Quad as ichus (Hymenop e a:
Eulophidae) ea ed om Li chiomyia chinensis (Dip e a:
Cecidomyiidae) on comme cial lychee (Li chi chinensis;
Sapindaceae) in Taiwan
Michael W. Ga es
a
, Yi-Min Chao
b
, Sheng-Feng Lin
b
and Man-Miao Yang
b
a
Sys ema ic En omology Labo a o y, Ag icul u al Resea ch Se ice, U.S. Depa men o Ag icul u e, C/o
Smi hsonian Ins i u ion, Na ional Museum o Na u al His o y, Washing on, DC, USA;
b
Depa men o
En omology, Na ional Chung Hsing Uni e si y, Taichung, Taiwan
ABSTRACT
The lychee gall midge, Li chiomyia chinensis Yang and Luo (Dip e a:
Cecidomyiidae), in aded Taiwan in 2008. This ly induces blis e -
galls on he lea es o lychee, Li chi chinensis Sonn (Sapindaceae),
and causes signi ican yield losses. A p esen , i s na u al enemy
complex is la gely undocumen ed; hus, he o e all aim o ongoing
esea ch is o in es iga e he na u al enemies on L. chinensis in
di e en a eas and seasons in Taiwan. We desc ibe wo species
ha pa asi ise his gall midge: Quad as ichus lasallei, sp. n. and
Quad as ichus johnlasallei, sp. n. ha demons a e biocon ol
po en ial o his pes .
h p://www.zoobank.o g/u n:lsid:zoobank.o g:ac :A5E93071-D935-4F60-BCF9-225C50389ABF
h p://www.zoobank.o g/u n:lsid:zoobank.o g:ac :261FC598-03CC-44A1-9379-F665B2DF0AA0
ARTICLE HISTORY
Recei ed 8 Decembe 2019
Accep ed 3 June 2020
Published online
23 Sep embe 2020
Published in p in
23 Sep embe 2020
KEYWORDS
Biocon ol; pa asi oids;
lychee gall midge
In oduc ion
The lychee gall midge (Li chiomyia chinensis; Dip e a: Cecidomyiidae), o iginally
desc ibed om Can on (cu en ly Guangzhou), China, was eco ded om Chiayi,
Taiwan in 2008 (Hung e al. 2008). I now occu s in lychee (Li chi chinensis Sonn
(Sapindaceae)) o cha ds h oughou Taiwan as well as Aus alia (Yeh e al. 2012a).
The adul emale lays eggs in young shoo s, and newly ha ched la ae induce blis e -
galls on lea es o lychee, an e e g een, sub opical ui ee. In 2018, lychee
p oduc ion was 78,668 onnes wi h a alue o 139.5 million USD (Zeng 2012;
Council o Ag icul u e 2018, 2019). He eina e , he abb e ia ion L. chinensis will
e e only o Li chiomyia chinensis while Li chi chinensis will be spelled ully. Galls
can lead o dec eased pho osyn hesis, and p o ide a pa hway o pa hogen in ec ion
(Hung e al. 2008). The in es a ion o L. chinensis can dec ease lychee p oduc ion by
mo e han 60% (Yeh e al. 2012b).
Pes icides a e used o con ol he popula ion o L. chinensis in Taiwan, bu o e -
lapping gene a ions and asynch onous de elopmen o L. chinensis dec ease hei
CONTACT Michael W. Ga es [email p o ec ed]
JOURNAL OF NATURAL HISTORY
2020, VOL. 54, NOS. 9–12, 635–646
h ps://doi.o g/10.1080/00222933.2020.1779367
© 2020 In o ma UK Limi ed, ading as Taylo & F ancis G oup
Published online 23 Sep 2020
e icacy. The e o e, he use o biological con ol agen s as a po en ial al e na i e o
pes icides could p o e e icacious, as demons a ed o o he gall-inducing pes s
(Aebi e al. 2006; P o aso e al. 2007).
In his pape we ea wo new species o Quad as ichus (Hymenop e a: Eulophidae)
ea ed om L. chinensis: lasallei, sp. n. and johnlasallei, sp. n. Quad as ichus (Gi aul (1913
[1967]) con ains many species associa ed wi h galls induced by gall midges (Dip e a:
Cecidomyiidae), gall wasps (Hymenop e a: Cynipidae), and e en o he Quad as ichus
(Hymenop e a: Eulophidae). Species associa ed wi h gall induce s a e usually endopa -
asi oids, bu one Eu opean species Q. sajoi (Szelényi) is a p eda o o e iophyid mi es
wi hin galls (G aham 1991; La Salle 1994), and ano he phy ophagous on young mango
s ems (Na end an 2007). Quad as ichus e y h inae Kim is an in asi e pes which induces
galls on co al bean ees (E y h ina spp.: Fabaceae) (Kim e al. 2004). In addi ion o being
associa ed wi h galls, species o Quad as ichus ha e a ious hos s: Cu culionidae and
Bup es idae (Coleop e a: G aham 1991; La Salle 1994; Noyes 2019), and lea -mining
Ag omyzidae o G acilla iidae (Reina and La Salle 2003, 2004). The nomencla u al his o y
o Quad as ichus is somewha con olu ed (G aham 1987; Bouček 1988; G aham & La Salle
1991, LaSalle 1994) and will con inue o pose challenges un il a global e ision o he
g oup is comple ed.
Much o he ecen in e es in species o Quad as ichus globally has been d i en by
he eme gence o in asi e gall-inducing species. The p ima y example is Q. e y h inae
Kim which induces galls on co al bean ees (E y h ina spp.: Fabaceae) (Kim e al. 2004)
and has sp ead om i s hypo hesised na i e ange in A ica (Messing e al. 2009) in o
many opical egions (de ailed by Jansen-Gonázlez e al. 2019). Mos ecen ly, Jansen-
Gonázlez e al. (2019) epo ed on a second E y h ina-galling species de ec ed in Cos a
Rica ha keys o Q. ba dus in he key o P insloo and Kelly (2009) bu di e s biologically
in galling s ems a he han lea es. The second example is he bene icial Q. mendeli
Kim & LaSalle ha was ea ed om galls o Lep ocybe in asa Fishe & LaSalle in
Aus alia. The la e is an in asi e gall induce on Eucalyp us ha has sp ead no ably
h oughou he Medi e anean and Middle Eas egions, in o SE Asia and B azil (Kim
e al. 2008).
Quad as ichus species a e ecognised by a single do sal se a on he subma ginal ein
(SMV), one adno aula se a on midlobe o mesoscu um in pos e io hal (less commonly
2–3), p opodeum lacking Y-shaped pa aspi acula ca ina, ce cal se ae unequal in leng h,
wi h one dis inc ly longe and sinua e, an enna wi h all unicula segmen s longe han
b oad, scu ellum wi h submedian lines, p opodeal spi acles close o me ano um wi h ims
exposed, o iposi o shea hs no , o only sligh ly, p ojec ing beyond epipygium (G aham
1991).
Anysis-g oup species, o which he new species desc ibed he ein belong (see species
ea men s below), a e cha ac e ised by being mos ly black wi h yellow ma kings (some-
imes only base o gas e ), o en i ely yellow, non-me allic; ons wi h a median a ea
ins ead o median longi udinal ca ina; lines delimi ing sc obes sligh ly la e ally con e -
gen do sally; mala sulcus dis inc ly cu ed, no o ea e; scu ellum wi hou o se bo de
along i s hind edge (G aham 1991; Reina and La Salle 2004).
Species known om China include anysis (Walke ), ci ella Reina and LaSalle, e y h inae
Kim, p e idis G aham, and sajoi (Szelenyi). Taiwan includes ci ella Reina and LaSalle,
e y h inae Kim, li iomyzae Hansson & LaSalle (Noyes 2019). Howe e , desc ibed species
636 M. W. GATES ET AL.
in ela ed gene a (Ap os oce us: 42 species, Te as ichus: 34 species) which may con ain
misplaced Quad as ichus mus be examined in o de o ob ain a be e unde s anding o
SE Asian di e si y o he genus.
Ma e ials and me hods
E hanol-p ese ed specimens we e dehyd a ed h ough inc easing concen a ions o
e hanol, and ans e ed o hexame hyldisilazane (HMDS) (He a y and Hawks 1998) be o e
poin -moun ing. MWG iden i ied pa asi oids using a Leica M205 C s e eomic oscope wi h
10X ocula s and a Leica LED ing ligh sou ce o poin -moun ed specimen obse a ion. All
specimens we e de e mined o genus by sigh iden i ica ion o using G aham (1991). We
used se e al species keys o de e mine whe he ou ma e ial belonged o any desc ibed
species (G aham 1991; Reina & La Salle 2004; Na end an 2007) wi h de ails below unde
each speci ic ea men . Whe e possible, all species iden i ica ions we e co obo a ed by
compa ison wi h au ho i a i ely iden i ied specimens in he Smi hsonian Na ional
Museum o Na u al His o y. Habi us images we e cap u ed using a Mac opod P o 3D
sys em (Canon 6D Ma k II body) wi h a Canon EF 70–200 mm elepho o wi h a 10x
objec i e lens (Mac oscopic Solu ions, LLC). Ou image se ies was me ged in o a single in-
ocus, composi e image wi h he p og am Ze ene S acke ( e . 1.04). Pos -imaging p o-
cessing was comple ed wi h he edi ing ools in Ze ene S acke . Image edi ing o bo h he
SEM and he habi us pho os was done in Adobe Pho oshop CS6 wi h a Wacom In uos P o
able on a MacBook P o. Pla e layou was done in Adobe Illus a o CS6. In he diagnosis
and ecogni ion sec ions, compa a i e ea u es o p e iously desc ibed axa p ecede
hose o he newly desc ibed species, which a e in pa en heses.
Te minology used in his pape ollows Gibson (1997) and G aham (1987). OOL,
ocella –ocula dis ance; OD, ocella diame e ; POL, pos -ocella dis ance; F, unicle seg-
men ; CC, cos al cell; SMV, subma ginal ein; MV, ma ginal ein; STV, s igmal ein; PMV,
pos ma ginal ein; F1–4, unicula segmen 1–4. Abb e ia ions o museums a e CNCI,
Canadian Na ional Collec ion o Insec s, O awa, On a io, Canada; NCHU, Na ional Chun
Hsing Uni e si y Collec ion, Taichung, Taiwan; NHMUK, Na u al His o y Museum, London,
UK; USNM, Uni ed S a es Na ional Museum o Na u al His o y, Washing on, D.C., USA.
Resul s and discussion
Quad as ichus lasallei, sp. n. (Figs 1, 2)
Female holo ype
Leng h: 3.0 mm. Colou : Head, body, and legs pale yellow, lagellome es ligh b own
wi h pale yellow, especially apically (Figu e 1(b)). Fo e wing hyaline, ena ion yellow.
Head, in on al iew (Figu e 2(a)), 1.4 X as b oad as high, 1.5 X as b oad as on o e ex
a i s na owes ; mala space 0.8 X as long as an eye, he sulcus cu ed, wi hou
a iangula o ea benea h he eye; POL 1.1 X OOL, OOL 2.8 X OD; mandible biden a e
wi h a unca ion; head inely se ose, eyes spa sely se ose, se ae sho , ~1 omma idial
diame e (Figu e 2(a)); lowe ma gins o o uli app oxima ely one o ulus diame e below
lowe eye ma gins; clypeus shallowly ema gina e (Figu e 2(a)).
JOURNAL OF NATURAL HISTORY 637
An enna (Figu e 2(d–h)) wi h scape 5.2 X as long as b oad, a li le sho e han he
heigh o eye, almos eaching e ex; pedicel app oxima ely 2.5 X as long as b oad, 1.5
X as long as basal unicle segmen ; one ans e se anellus p esen ; unicle h ee-
segmen ed, segmen s abou equal in size, o p og essi ely dec easing a li le in size, F1
3.3 X, F2 3.8 X, F3 3.8 X as long as b oad; cla a 5.0 X as long as b oad; apical spine sho ,
dis inc ly sho e han apical segmen (Figu e 2(h)); sensilla spa se, lagellum a he
spa sely se ose (Figu e 2(g–h)).
Mesosoma (Figu e 2(b–c)) 1.7 X as long as b oad; mesoscu um in p o ile gen ly con ex
do sally, in do sal iew gen ly ounded la e ally; mesoscu al midlobe jus longe han
b oad, wi h ace o median line pos e omedially (di icul o see wi hou high magni ica-
ion), wi h 1 adno aula se a a each side in pos e io hi d; mesoscu um wi h e y ine
linea e sculp u e; scu ellum con ex in p o ile, 1.5 X b oade han long wi h subla e al and
submedian lines (di icul o see wi hou high magni ica ion); sculp u e much as in
mesoscu um; scu ellum wi h 2 pai s o se ae; do sellum con ex, smoo h, medially abou
as long as p opodeum; p opodeum wi h median ca ina indis inc , wi h cu ed spi acula
sulcus mesad eminiscen o pa aspi acula ca ina, wi h e y ine e icula e sculp u e;
spi acles less han hei own diame e om an e io p opodeal ma gin (Figu e 2(c)); calli
each wi h 2 se ae.
Fo e wing (Figu e 1(b)) 2.2 X as long as b oad; cos al cell 16 X as long as b oad, 0.8
X leng h ma ginal ein, ase ose; subma ginal ein wi h 1 do sal se a; ma ginal ein 5.7
X as long as s igmal ein, he pos ma ginal ein no appa en ; subcubi al line o se ae
ex ending basally as a as basal se al line, closing speculum pos e io ly; longes ma ginal
cilia (a he apex o ma ginal ein) abou 0.6 X as long as longes se ae on ma ginal.
Me asoma 1.2 X longe han mesosoma, somewha ci cula in do sal iew, jus longe
han b oad, b oadly ounded apically; epipygium 1.6 X as long as b oad; hypopygium
eaching o abou hal he leng h o gas e ; o iposi o shea hs sho ha dly p o uding
apically; one ce cal se a wice leng h o he s and kinked.
Figu e 1. (a) Quad as ichus johnlasallei, la e al habi us, emale. (b) Quad as ichus lasallei, la e al
habi us, emale.
638 M. W. GATES ET AL.
Figu e 2. Quad as ichus lasallei, emale: a, an e ola e al head; b, do sal mesosoma; c, p opodeum; g,
la e al lagellum; h, la e al cla a. Q. lasallei, male: d, la e al lagellum; e, la e al cla a; , la e al scape.
JOURNAL OF NATURAL HISTORY 639
Male
Leng h: 1.9 mm. Colou : much as in emale excep ollowing b own: e ex; p ono um
do sally, mesoscu um in an e io hal , excep along no auli; do sellum, p opodeum,
me apleu on, gas al e ga 3–8. Di e ing s uc u ally om he emale mainly in he
an enna (Figu e 2(d– )): scape wi h a linea en al plaque, placed in apical hal and
ex ending om nea apex o beyond mid leng h o scape (Figu e 2( )); a single anellus
p esen ; unicle ou -segmen ed, F1 1.0 X F2 2.0 X, F3 2.7 X, F4 2.8X as long as b oad, each
b oades basally and na owing apically; cla a 5.0 X as long as b oad; lagellum spa sely
se ose, he se ae on unicle segmen s ai ly long, sligh ly cu ed, basal do sal who ls on
F1–4 eaching beyond ollowing segmen . Some cla a sensilla s ongly ecu ed (Figu e 2
(d–e)).
Va ia ion
One male has addi ional b own colou a ion an e io ly on gas al e gum 1, enci cling
pe iole base.
E ymology
Named in honou o ou iend and colleague, D John La Salle, o his good humou
and lo e o Chalcidoidea. He will be missed.
Biology
La a is a koinobion endopa asi oid o ma u e la a o lychee gall midge, Li chiomyia
chinensis.
Diagnosis and ecogni ion. This species is ecognised by emale comple ely yellow,
clypeus sligh ly ema gina e (bo h sexes), and male wi h s ongly ecu ed sensilla on
cla a.
This species keys o he anysis-g oup o a la ge ex en , ul ima ely o couple 20 in
G aham 1991 whe e i spli s he diagnos ic ea u es wi h h ee o i e cha ac e s leading
o Q. anysis. Howe e , Q. lasallei di e s om Q. anysis in comple ely pale yellow colou a-
ion in emale (a eas o b own/black on head and me asoma, mesosoma mos ly black),
scape eaching he le el o e ex (no eaching e ex), clypeus no ched (no sub un-
ca e), and ecu ed sensilla on male cla a (s aigh ). Biologically, Q. anysis is known om
Mona h opalpus buxi Laboulbène (Dip e a: Cecidomyiidae) ha mines he lea es o Buxus
spp. (box; Buxaceae) h oughou Eu ope and No h Ame ica. In he key o Na end an
(2007), his species uns o Q. longicla a us Na end an, bu di e s in cla al spine 0.2 X he
leng h o cla a (0.52 X) and emale comple ely yellow (la gely black). The biology and
male a e unknown o Q. longicla a us. Finally, in he Reina and La Salle (2004) key o Old
Wo ld species o he anysis-g oup, Q. lasallei uns o Q. ci ella Reina & LaSalle, as bo h
sha e F1 sho e han F2, and speculum ex ending ~0.2–0.3 X leng h ma ginal ein, bu all
gas al e ga yellow (da k b own band on gas al e ga 3–4) and p opodeum dis inc ly
e icula e (sculp u e much smoo he ). Fu he , Q. ci ella is an idiobion ec opa asi oid o
he lea mine Phyllocnis is ci ella S ain on (Lepidop e a: G acilla iidae) whe eas Q. lasallei
is a koinobion endopa asi oid o L. chinensis.
640 M. W. GATES ET AL.
Type ma e ial examined
Female holo ype, 1 emale: TAIWAN: Changhua Co.: Fenyuan Township, No. 139
Fongshan Rd., 24°00ʹ9.2”N 120°37ʹ32.3”E, 19.IX.2018, Heyieh, Coll. Yi-Min Chao; sp. 2,
emale #6; USNMENT01525925 (NCHUC). 2 emale, 3 male pa a ypes, same da a as
holo ype (NCHU). 2 emale, 3 male pa a ypes, same da a as holo ype, excep seconda y
labels a e sp. 2, emale #5, USNMENT01525926 (1 , USNM); sp. 2 emale #6,
USNMENT01525927 (1 , NHMUK); sp. 2 male #7, USNMENT01525928 (1 m, USNM); sp.
2 male #7, USNMENT01525929 (1 m, NHMUK); sp. 2 male #7, USNMENT01525924 (1 m,
CNCI). 1 emale pa a ype, same locali y and collec o as holo ype, excep da e 13.
XI.2018 (1 , NCHU). 1 emale pa a ype: Nan ou Co.: Cao un Township, Jianxing Rd.,
23°59ʹ39.7”N 120°46ʹ18.1”E, 6.IX.2018, Coll. Yi-Min Chao; sp. 1 male #4,
USNMENT01525920 (1 , CNCI). 1 emale, 4 male pa a ypes: TAIWAN: Taichung Ci y:
Taiping Dis ., Guangxing Rd., No.60 2140 h S. Ln., 24°07ʹ42.4”N 120°44ʹ17.1”E, 21.
XI.2018, em. 29.XI.2018, Coll. Yi-Min Chao (1 , 2 m, NCHU); same collec ed da e excep
em. 27.XI.2018 (2 , NCHU).
Quad as ichus johnlasallei, sp. n. (Figs 1, 3)
Female Holo ype. Leng h: 4.0 mm. Colou : Head, mesosoma, o e coxa, o iposi o
shea hs, and gas e do sally da k b own (excep as no ed beyond); an enna, middle and
hind legs, gas e (an e odo sal qua e , an e ola e al wo- hi ds, an e o en al wo- hi ds,
do sola e ally on gas al e gum 5) pale yellow (Figu e 1(a)). Fo e wing hyaline, ena ion
yellow.
Head, in on al iew (Figu e 3(a)), 1.5 X as b oad as high, 1.7 X as b oad as on o e ex
a i s na owes ; mala space 0.6 X as long as an eye, he sulcus sligh ly cu ed, wi hou
a iangula o ea benea h he eye; POL 3.2 X OOL, OOL 1.3 X OD; mandible iden a e;
head inely se ose, eyes e y spa sely se ose, se ae sho , <1 omma idial diame e (Figu e
3(a)); lowe ma gins o o uli app oxima ely wo o ulus diame e abo e lowe eye
ma gins; clypeus biloba e (Figu e 3(a)).
An enna (Figu e 3(d–h)) wi h scape 3.6 X as long as b oad, longe han he leng h o an
eye, jus exceeding e ex; pedicel app oxima ely 2.5 X as long as b oad, 1.5 X as long as
basal unicle segmen ; one ans e se anellus p esen ; unicle h ee-segmen ed, F1 jus
sho e han he subequal F2–F3, F1 2.6 X, F2 3.8 X, F3 3.8 X as long as b oad; cla a 5.0 X as
long as b oad; apical spine ~0.8 X leng h apical segmen ; sensilla spa se, lagellum a he
spa sely se ose (Figu e 3(d–e)).
Mesosoma (Figu e 3(b–c)) 1.3 X as long as b oad; mesoscu um in p o ile gen ly con ex
do sally, in do sal iew gen ly ounded la e ally; mesoscu al midlobe app oxima ely as
long as b oad, wi h ine median line; wi h 2 adno aula se ae a each side, in pos e io hal ;
mesoscu um wi h e y ine linea e sculp u e; scu ellum con ex in p o ile, 1.2 X b oade
han long wi h submedian lines; sculp u e as in mesoscu um; scu ellum wi h 2 pai s o
se ae; do sellum con ex, smoo h, medially abou as long as p opodeum; p opodeum
wi hou median ca ina, wi h cu ed spi acula sulcus mesad eminiscen o pa aspi acula
ca ina, wi h e y ine e icula e sculp u e; spi acles ~1x hei own diame e om an e io
p opodeal ma gin; cali each wi h 2 se ae.
Fo e wing (Figu e 1(a)) 2.2 X as long as b oad; cos al cell 15.0 X as long as b oad, 0.7
X leng h o ma ginal ein, ase ose; subma ginal ein wi h 1 do sal se a; ma ginal ein 3.0
JOURNAL OF NATURAL HISTORY 641
X as long as s igmal ein, he pos ma ginal ein 0.3 X s igmal; subcubi al line o se ae
ex ending basally as a as basal se al line, closing speculum pos e io ly; longes ma ginal
cilia ~1.4 X as long as longes se ae on ma ginal ein.
Me asoma elonga e, 2.6 X longe han mesosoma, 2.0 X longe han b oad, ape ed
apically; epipygium 2.3 X longe han b oad; hypopygium eaching o abou 0.3 X he
leng h o gas e ; o iposi o shea hs sho , ha dly p o uding apically; one ce cal se a wice
leng h o he s and cu ed.
Figu e 3. Quad as ichus johnlasallei, emale: (a) an e io head; (b) do sola e al mesosoma; (c) do so-
la e al p opodeum; (d) la e al lagellum; (e) la e al cla a. Q. johnlasallei, male: ( ) la e al scape; (g)
la e al an enna; (h) la e al cla a.
642 M. W. GATES ET AL.
