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JHR 61: 75-83 (2017) JOURNAL OF *0eerrviewed opevaccersjoural
doi: |0.3897/jhr.6 1.20742 (ME Hymenopter a

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

A new species of Hexacladia Ashmead (Hymenoptera,
Encyrtidae) and new record of Hexacladia smithii
Ashmead as parasitoids of Dichelops furcatus (Fabricius)
(Hemiptera, Pentatomidae) in Argentina

avier Torréns!', Patricio Fidalgo', Celina Fernandez', Eduardo Punschke?
g

I Centro Regional de Investigaciones Cientificas y Transferencia Tecnolégica de La Rioja (CRILAR), Provincia
de La Rioja, UNLAR, SEGEMAR, UNCa, CONICET, Entre Rios y Mendoza s/n, (5301) Anillaco, La Rioja,
Argentina 2 Facultad de Ciencias Agrarias, Universidad Nacional de Rosario, Campo Experimental J. Villari-
no, C.C. 14 (S2125ZAA) Zavalla — Santa Fe, Argentina

Corresponding author: Javier Torréns (jtorrens@crilar-conicet.gob.ar)

Academic editor: Petr Jansta | Received 1 September 2017 | Accepted 13 November 2017 | Published 20 December 2017
Attp.//zoobank.org/BB6690DD-7EC4-45 10-812F-EADFO5ED22E 1

Citation: Torréns J, Fidalgo P, Fernandez C, Punschke E (2017) A new species of Hexacladia Ashmead (Hymenoptera,
Encyrtidae) and new record of Hexacladia smithii Ashmead as parasitoids of Dichelops furcatus (Fabricius) (Hemiptera,
Pentatomidae) in Argentina. Journal of Hymenoptera Research 61: 75-83. https://doi.org/10.3897/jhr.61.20742

Abstract

Pentatomid adults of the species Dichelops furcatus (F.), collected on stubble of soybean, Glycine max (Lin-
naeus) Merril, in Santa Fe province of Argentina, were found parasitized by two encyrtid wasp species
(Hymenoptera: Encyrtidae). One of the encyrtids is described as Hexacladia dichelopsis Torréns & Fidalgo,
sp. n., from both sexes, and the other species H. smithii Ashmead, is recorded for the first time from
D. furcatus in Argentina. Both species are gregarious endoparasitoids which carry out the whole develop-
ment (larval and pupal) in their living hosts; they emerge as imagoes, by cutting their way out through the
dorsal wall of the abdomen. Including the newly described H. dichelopsis, seven species of the genus are

recorded from South America, and an identification key to separate them is presented.

Keywords
Hexacladia, new species, parasitoids, Dichelops furcatus

Copyright Javier Torréns 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.

76 Javier Torréns et al. / Journal of Hymenoptera Research 61: 75-83 (2017)

Introduction

Members of the genus Hexacladia Ashmead are gregarious parasitoids of the late
nymphs or adult stages of Pentatomidae, Coreidae, Pyrrhocoridae and Scutelleridae
(Hemiptera) (Burks 1972, Noyes 2010), emerging from the living host. Hexacladia
is unique amongst Encyrtidae in having a relatively slender, distinct petiole; the very
high placement of the antennae, a dome-like scutellum, characteristic infuscation and
setation of the fore wing and branched antenna of the males makes the genus very easy
to recognize (Noyes 2010).

Six species of Hexacladia have been recorded from South America: H. blanchardi De
Santis (Argentina and Brazil), H. /inci Rasplus (Peru), 1. smithii Ashmead (Argentina,
Brazil and Venezuela), H. townsendi (Crawford) (Peru, Ecuador and Venezuela), H.
supina Noyes (Ecuador), H. impiros Noyes (Ecuador and Peru) (De Santis 1963, 1979,
1980, De Santis and Fidalgo 1994, Rasplus et al. 1990, Noyes 2010, 2017). H. smithii
is the species with many hosts mentioned in the literature, and also the most widely dis-
tributed being found in Argentina, Brazil, Costa Rica, México, Nicaragua, Puerto Rico,
Trinidad and Tobago, USA and Venezuela (Gordh 1979, Noyes 2010, 2017).

Dichelops furcatus (F.) known as “chinche furcada” or “chinche de los cuernos” is
considered a corn pest because it injects toxins into the stem during feeding. These
toxins damage the vigor of the seedlings producing a detention of its growth, malfor-
mations in some cases and even death by intense attacks in the most susceptible stages
(Canale and Ferreira 2013). D. furcatus has been recorded as the primary host of two
encyrtids, Ooencyrtus submetallicus (Noyes 2010), and Hexacladia smithii in Southern
Brazil (Panizzi and Da Silva 2010).

Herein we describe Hexacladia dichelopsis sp. n. and provide a key to separate the
seven species of Hexacladia now known from South America. We also present a new
record of H. smithii as parasitoid of D. furcatus in Argentina.

Methods

Both species of Hexacladia emerged from diapausing adults of D. furcatus on soybean
stubble. The material was collected in the Experimental field J. Villarino of the Faculty of
Agronomic Sciences in Zavalla, province of Santa Fe (Argentina). The collection date was
August 2015, March and May 2016. In total, 33 females and 2 males of H. dichelopsis sp.
n. and 4 females and 4 males of H. smithii were collected. The material was preserved in
alcohol and then mounted; some of them were slide-mounted in Canada balsam.

For morphological terms and species identification we followed Burks (1972),
Noyes (2010) and Cuezzo and Fidalgo (1997). The abbreviations used are: Fn = flagel-
lar segment n; LOL = shortest distance between posterior ocellus and anterior ocellus
in frontal view, OOL = shortest distance between posterior ocellus and eye margin in
dorsal view and POL = shortest distance between posterior ocelli in dorsal view.

A new species of Hexacladia Ashmead (Hymenoptera, Encyrtidae) and new record... ies

Specimens are deposited in the Instituto Fundacion Miguel Lillo, Tucuman, Ar-
gentina (IFML); Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’,, Bue-
nos Aires, Argentina (MACN); and the Entomology collection of CRILAR, Anillaco,
La Rioja (CRILAR-En).

Results

Key to the South American species of Hexacladia Ashmead (modified from
Burks 1972)

1 Male; funicular segments of antenna with branches (Fig. 9)... cesses 2.
Female; funicular segments of antenna without branches (Fig. 10) ............. 5
2 Fore wings comparatively short, 1.3x as long as mesosoma (Figs 1, 2) ........ 3
= Fore wings normally developed, nearly 2.5x as long as mesosoma (Figs 11,
| 2531 Re el dred crore Perel oh eo rvs Perro sre 1 A sft Sas 4
3 Fore wings with marginal fringe uneven, largely or completely absent...........
ricci ated tle ah soba iste dhah a he tce a ye eee hah Pe aber ase Ue linci Rasplus

— Fore wings with marginal fringe present and complete except perhaps for
a short strip immediately distad of apex of venation or towards anal angle
CST) Naeltta ts eclvatal eo satet Be aes dei side ted plarsetetibauite slut ale thay Sa dichelopsis sp. n.
4 Branch of F6 extremely short, 0.1x length of segment itself. Female un-
Ke ONVH Me aut ect ackba sl acco dadbrs babecasstbanlis ehdiducytanedephieatsuhaklg blanchardi De Santis
Branch of F6 at least as long as segment itself... smithii Ashmead

Wn |

Fore wings comparatively short, 1.3x as long as mesOsoMa .........sceeeeseeeeeeee 6
= Fore wings normally developed, nearly 2.5x as long as mesosoma.............++ ¥E

ON

Fore wings with marginal fringe uneven, largely or completely absent...........
aah tek ieee ate ac Pu i tate Pune lt see aL terete ee Pa linci Rasplus
— Fore wings with marginal fringe present and complete except perhaps for a
short strip immediately distad of apex of venation or towards anal angle (Fig.
oi Lene te eae Ye Ree RTS fe ee te ROT RABAT 3 dichelopsis sp. n.
7 Fore wings with marginal fringe uneven, largely or completely absent......... 8
- Fore wings with marginal fringe present and complete except perhaps for a
short strip immediately distad of apex of venation or towards anal angle.....9
8 Costal cell of fore wing dorsally naked, or virtually so; with at most only one
getarveritrallylal eww, orice becedvtneede emetic ns nacehiertee supina Noyes
- Costal cell of fore wing with up to 9 setae dorsally and 7 ventrally...
BS coh Sic ctteo RN ga Racleaee Mncaatteartalon nto te dace aeons isa = smithii Ashmead
9 Each lateral projection of hypopygium broadened, flattened and rounded
apically, paddle-like. Male unknown... eee eeeseeeeeseeeees impiros Noyes
- Hypopygium apically with a pair of long, curved lateral processes either side
of a deep, median invagination. Male unknown........ townsendi (Crawford)

78 Javier Torréns et al. / Journal of Hymenoptera Research 61: 75-83 (2017)

Hexacladia dichelopsis Torréns & Fidalgo, sp. n.
http://zoobank.org/83FD4672-A94D-437C-8F6E-68F4673E84E6
Figs 1-10

Diagnosis. Distinguished from other species by the following combination of charac-
ters: general body color dark brown to black (Figs 1, 2); small wings, fore wing 1.3x as
long as length of mesosoma (Figs 1, 2); female with costal cell with four or five setae,
distal third of the upper margin without marginal setae, dark areas of the wing disc
well evident; male with costal cell with abundant setae (25 to 27), basal third with
eight to nine setae, distal third of the upper margin with marginal setae and dark areas
of the wing disc poorly defined; male with F7 2.0x as long as F6, branch of F6 0.5x
length of F6.

Description. Female (holotype): length, 2.3mm. General body color dark brown
to black dorsally, being paler toward head, scape and pedicel, axilla, metanotum, apex
of tibiae and tarsi, propodeum and base of first tergite of gaster; entire body lighter
ventrally, femora and metasoma slightly darker than the rest; setae on dorsum of meso-
soma translucent (Figs 2, 6). Wings largely hyaline, but fore wing with two brown
areas, the first and smaller behind base of parastigma, with about 40 strong dark brown
setae, the distal area is most extensive, begins behind marginal vein and occupies most
of wing apex, alar disc between the two brown areas with light setae (Fig 8).

Head 1.3x as broad as high. POL 2.1x LOL; POL 1.3x OOL. Head with fine,
raised, imbricate-reticulate sculpture, well-marked and moderately deep on frons
and vertex, and slightly marked and irregular on face and gena; anterior ocellus
connected to toruli by a shallow groove; interantennal area narrow and smooth;
frontovertex and face with inconspicuous, decumbent setae, each slightly shorter
than diameter of anterior ocellus (Fig. 6). Eyes separated by 1.7x their height. Malar
space 0.9x height of eye. Antenna 9-segmented, flagellar segments cylindrical. Fla-
gellum 1.6x as long as head height; length of F1 0.6x length of scape, and 2.8x as
long as broad; clava 3.4x as long as broad. Antenna (Fig. 10) apically with slightly
curved setae in all segments, more dense on funicle; funicle with linear sensilla only
on F3-F6 (Fig. 10).

Mesosoma with fine, raised, polygonally-reticulate to imbricate-reticulate sculp-
ture on mesoscutum (Figs 2, 4). Pronotum with small and decumbent setae, head over-
lapping the pronotum. Mesoscutum 1.7x as broad as long, with small and decumbent
setae (Fig. 4). Scutellum 1.1x as long as maximum width; axilla and scutellum with
coarse reticulate sculpture slightly deeper than that on mesoscutum, and with semi-
erect and longer setae than the mesoscutum; scutellum humped, strongly and fairly
evenly curved in profile (Fig. 4); propodeum with a group of about 1 1-14 setae outside
spiracle. Fore wing 3.1x as long as broad, costal cell with seven or eight setae dorsally,
linea calva broad and open posteriorly, basal cell with five to eight setae, submarginal
vein with 11 bristle-like setae, postmarginal vein slightly shorter than stigmal vein,
marginal fringe present, stigmal vein without uncus and with three or four placoid
sensilla; hind wing 3.7x as long as broad.

A new species of Hexacladia Ashmead (Hymenoptera, Encyrtidae) and new record... 79

0.5 mm

Figures 1-10. Hexacladia dichelopsis sp. n.: | habitus (male) 2 habitus (female) (magnified apex of hy-
popygium, lateral and ventral view) 3 mesosoma (male, dorsal) 4 mesosoma (female, dorsal) 5 head (male,
frontal) 6 head (female, frontal) 7 fore wing (male, lateral) 8 fore wing (female, lateral) 9 antenna (male,
lateral) 10 antenna (female, lateral).

Metasoma 1.5x as long as broad. Hypopygium very nearly reaching apex of meta-
soma; apically with a pair of short lateral processes either side of a wide, shallow, median
invagination; with about 6 hypopygial hairs (Fig. 2). Ovipositor not observed.

80 Javier Torréns et al. / Journal of Hymenoptera Research 61: 75-83 (2017)

Variation. The length of the female varies between 2.2—2.6 mm. ‘The coloration
in some specimens are darker than holotype, otherwise very little variation in material
examined.

Male. Similar to female except for following: The length of the male varies 1.7—1.9
mm. General body color and head darker than female (Figs 1, 3, 5), fore wing with ar-
eas paler, with costal cell with abundant setae (25 to 27), basal third with eight to nine
setae, stigmal vein with four or five placoid sensilla (Fig. 7) ; antenna with funicle seg-
ments longer than broad and with a elongate dorsal branch (Fig. 9); F1 a little longer
than F2 and F3; F4 longer than F5 and F6; F7 is the longest flagellomere; branch of
F1 2.0x as long as F1 and as long as F1 and F2 together; branch of F6 0.5x length of
F6. Length:width of the antennal segments in the following relationship: scape (48:7),
pedicel (9:8), Fl and branch of Fl (14:5 and 29:3), F2 and branch of F2 (13:5 and
31: 2,5), F3 and branch of F3 (13:5 and 30:2), F4 and branch of F4 (19:5 and 20:2),
F5 and branch of F5 (16:5 and 14:2), F6 and branch of F6 (16:6 and 9:2), F7 (35:7).

Material examined. Holotype 9: ARGENTINA, Santa Fé, Zavalla, Campo ex-
perimental Villarino, Fac. Cs. Agrarias, 2.v.2016., E. Punschke, ex. diapausing adult of
Dichelops furcatus on soybean stubble (MACN). Paratypes (11 99 and 23 dQ): same
locality as holotype, 2.viii.2015 (MACN, 11 @ and 2 3), 2.v.2016 (IFML, 1199,
IFML; CRILAR-En, 10 99).

Hexacladia smithii Ashmead, 1891
Figs 11-16

Hexacladia smithii Ashmead, 1891:457, lectotype designated by Burks (1972).
Hexacladia mexicana Girault, 1917, lectotype designated by Cuezzo and Fidalgo
(1997). Synonymized under smithii by Cuezzo and Fidalgo (1997).

Diagnosis. Distinguished from other species by the following combination of char-
acters: female with general body color and head mostly dark, reddish brown (Figs 12,
14, 16); presence of subapically curved and slightly flattened setae dorsally on F1; fore
wing fully developed, reaching apex of gaster, with marginal fringe absent, dark areas
of the wing disc well evident; costal cell dorsally with fewer than 10 setae and ventrally
with at least 2 or 3; hypopygium apically with a pair of short lateral processes either
side of wide, shallow, median invagination. Male similar to female but body color
mostly dark brown (Figs 11, 13, 15); antenna with all funicle segments branched,
branch of FG at least as long as segment itself; fore wing with marginal fringe present,
although occasionally slightly reduced.

Material examined. ARGENTINA, Santa Fé, Zavalla, Campo experimental Vil-
larino, Fac. Cs. Agrarias, 2.viii.2015, E. Punschke, ex. diapausing adult of Dichelops
furcatus on soybean stubble (CRILAR-En, 19 and 14; MACN, 19 and 13; IFML,
229 and 243). ARGENTINA, Tucuman, S. M. de Tucuman, 3.v.1993, P. Fidalgo
(IFML, 19).

A new species of Hexacladia Ashmead (Hymenoptera, Encyrtidae) and new record... 81

Figures | 1-16. Hexacladia smithii: \\ habitus (male) 12 habitus (female) 13 mesosoma (male, dorsal)
14 mesosoma (female, dorsal) 15 head (male, frontal) 16 head (female, frontal).

Discusion

Hexacladia dichelopsis sp. n. differs from H. linci (morphologically the closest species)
in: general body color dark brown to black, including head; funicle including clava and
scape dark brown (versus general body color brown, pleura yellowish to brown, yellow-
ish face and funicle, the first two flagellomeres and scape dorsally darker, apex of clava
black); antenna of the female with F1 as long as following three segments, with slightly
curved setae (versus F1 almost as long as following four segments, with straight setae),
antenna of the male with branch of F6 0.5x length of F6 (branch of F6 as long as F6
or longer than the flagellomere); fore wing with continuous marginal fringe (versus ab-
sent or discontinuous marginal fringe), basal third of wings with setae present (versus
basal third of wings without setae). Following the description of Rasplus et al. (1990)
the shape of distal margin of hypopygium is similar in both species. What about shape
of distal margin of hypopygium.

Two species were previously recorded from Argentina, Hexacladia smithii and H.
blanchardi; H. dichelopsis differ from H. smithii mainly by its coloration, length and
setation of fore wing. While the male differ from that of H. blanchardi in: antenna of

82 Javier Torréns et al. / Journal of Hymenoptera Research 61: 75-83 (2017)

male with branch of F1 two times longer than the F1 and branch of F6 0.5x length of
the F6 (versus branch of F1 11 to 12 times longer than F1 and branch of F6 rudimen-
tary); F7 two times longer than F6 (versus F7 1.2x longer than FG); fore wings 1.1—1.2
mm, reaching half of metasoma (versus 1.9 mm, reaching to the apex of metasoma);
basal third of wings with eight to nine setae (versus basal third of wings densely setose).

Concerning the parasitoidism data, it was not possible to separate the parasi-
toidism of both species; there were few occasions when the host were found so the rate
of parasitoidism is only an estimation and correspond to both species combined: five to
eight adults per diapausing Dichelops furcatus emerged and reached up to 10% during
2015 and up to 7.5% in 2016. The development from collection of parasitized host to
emergency of adult parasitoids took approximately 30 days.

Acknowledgements

This work was made possible by funds provided by CONICET and the Project PICT
2324 provided by Agencia Nacional de Promocién Cientifica y Tecnolégica. We would
like to thank the Faculty of Agronomic Sciences of the National University of Rosario
(Santa Fé, Argentina) for allowing us to work in their experimental field to collect the
studied material; and the anonymous reviewers for their constructive comments and
suggestions of this paper.

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