molecular and morphological diagnoses of ﬁve species of...

Molecular and morphological diagnoses of five speciesof Trichogramma: biological control agents of Chrysodeixischalcites (Lepidoptera: Noctuidae) and Tuta absoluta(Lepidoptera: Gelechiidae) in the Canary Islands

Andrew Polaszek • Paul F. Rugman-Jones •

Richard Stouthamer • Estrella Hernandez-Suarez •

Tomas Cabello • Modesto del Pino Perez

Received: 1 September 2010 / Accepted: 15 April 2011 / Published online: 12 May 2011

� International Organization for Biological Control (IOBC) 2011

Abstract Prospecting for potential natural enemies of

the invasive lepidopteran tomato pest Tuta absoluta

(Meyrick) (Lepidoptera: Gelechiidae) and the banana

pest Chrysodeixis chalcites (Esper) (Lepidoptera: Noc-

tuidae) on the Canary Islands archipelago, where no

Trichogramma species were previously recorded, has

led to the discovery of five distinct species. T. achaeae

Nagaraja & Nagarkatti, T. bourarachae Pintureau &

Babault, T. euproctidis (Girault) and T. evanescens

Westwood are relatively widespread species. The fifth is

close to T. brassicae Bezdenko, but differs sufficiently

in the sequence of the ITS2 region of ribosomal RNA to

warrant further investigation as a species probably new

to science. Each species is treated in detail in order to

facilitate identification in future using molecular and/or

morphological characters, or a combination of both. All

species are newly recorded for the Canary Islands, and

the distribution of each within the islands and elsewhere

is provided. Known host records are given within the

Canary Islands and elsewhere. The most common

species found, T. achaeae, is already being used in

biological control programmes against T. absoluta in

mainland Spain and field trials are ongoing to evaluate

its effectiveness as a biological control agent of

C. chalcites in banana crops.

Keywords Trichogramma achaeae �T. bourarachae � T. evanescens � T. euproctidis �Tuta absoluta � Chrysodeixis chalcites � Musa

acuminata � Solanum lycopersicum � Egg parasitoid �Ooparasitoid � Invasive pest � Canary Islands

Introduction

The South American tomato pinworm Tuta absoluta

(Meyrick) (Lepidoptera: Gelechiidae) is a major pest

of tomato and other solanaceous crops that has spread

from Central America to most of South America

(EPPO 2005) and was accidentally introduced into

Spain in 2006 (Urbaneja et al. 2007; EPPO 2008) and

Handling Editor: Dirk Babendreier

A. Polaszek (&)

Department of Entomology, Natural History Museum,

London SW7 5BD, UK

e-mail: [email protected]

P. F. Rugman-Jones � R. Stouthamer

Entomology, University of California,

Riverside, CA 92521, USA

E. Hernandez-Suarez � M. del Pino Perez

Department of Proteccion Vegetal, Instituto Canario de

Investigaciones Agrarias, P.B. 60, 38200 La Laguna,

Tenerife, Islas Canarias, Spain

T. Cabello

Centro de Investigacion en Biotecnologıa

Agroalimentaria, Universidad de Almerıa,

Ctra Sacramento s/n, 04120 Almerıa, Spain

123

BioControl (2012) 57:21–35

DOI 10.1007/s10526-011-9361-y

subsequently into other European countries. It is

regarded as an established pest in Spain (EPPO 2008)

much of Southern Europe and North Africa, and is

rapidly spreading east across the Mediterranean

(FERA 2010; Roditakis et al. 2010) and into Northern

Europe.

Tuta absoluta is extremely difficult to control

using chemical insecticides because larvae mine

within plant tissue and are thus protected at least

from contact insecticides (Branco and Franca 1993),

but also because of the development of resistance

(Lietti et al. 2005; Siqueira et al. 2000). For these

reasons biocontrol using parasitoids has been inves-

tigated on many occasions as a potentially suitable

control method both in Latin America (Bueno 2005),

including the use of Trichogramma species there

(Domingues et al. 2003; Faria et al. 2008; Freitas

et al. 1994; Villas-Boas and Franca 1996) and more

recently in Europe (Cabello et al. 2009b). Although

several species of autochthonous predators have been

evaluated as biological control agents in Spain,

particularly the mirid bugs Nesidiocoris tenuis

(Reuter) (Urbaneja et al. 2008) and the damsel bug

Nabis pseudoferus Remane (Cabello et al. 2009a) the

establishment into the crops is often too slow to avoid

damage to the crop, and consequently chemical

treatments are needed.

The golden twin-spot moth or tomato looper,

Chrysodeixis chalcites (Esper) (Lepidoptera: Noctui-

dae) is one of the most damaging pests of banana

crops (Musa acuminata) in the Canary Islands,

inflicting serious economic damage to the youngest

leafpipes, leaves and fruits (Perera and Molina 2007;

Cabello 2009; del Pino et al. 2011). It is a subtropical

species, occurring in Africa, Oceania, Southern

Europe and South Asia, attacking a large number of

cultivated plants (Cayrol 1972). In Southern Spain

C. chalcites has had an important economic impact in

the Guadalquivir Valley (Cabello 1986), la Vega of

Granada (Cabello 1988) and in greenhouses in the

province of Almerıa (Cabello et al. 1996). It is

considered a major pest in Israel and Egypt (Harakly

and Farag 1975), Italy (Zandigiacomo 1990), Bul-

garia and Turkey (Loginova 1992; Uygun and Ozgur

1980), The Netherlands (Vos and Rutten 1995) and

Belgium (Veire 1993).

Control of C. chalcites has failed for reasons

similar to those for the failure of T. absoluta control.

C. chalcites adults deposit eggs individually (Cayrol

1972) or in small groups (Harakly and Farag 1975) and

always highly dispersed in the crop. The inefficiency of

applied synthetic and biological insecticides has been

demonstrated (Alonso 2009; del Pino et al. 2011), and

resistance of C. chalcites to several pesticides has been

recorded, e.g. in Israel (Broza and Sneh 1994). Several

publications deal with natural enemies such as Mete-

orus gyrator (Thunberg) (Hymenoptera: Braconidae)

(Bell et al. 2000), Cotesia marginiventris (Cresson)

(Hymenoptera: Braconidae) (Messelink 2002; Lobo

Lima and van Harten 1985), Podisus maculiventris

(Say) and P. nigrispinus (Dallas) (Heteroptera: Pent-

atomidae) (Vacante et al. 1996; De Clercq et al. 1998;

Bolckmans and Tetteroo 2002) but biological control is

not yet commercially available (Cabello 2009; del Pino

et al. 2011).

Foreign exploration was therefore instigated in

2008 for parasitoids suitable for the control of C. chal-

cites and T. absoluta, for use initially in Spain, but

which also would be appropriate for application

elsewhere in the increasing range of T. absoluta

in particular. The Canary Islands archipelago was

selected as an appropriate area for exploration, having

a wide range of diverse ecosystems, many approxi-

mating to both the original and invasive ranges of

T. absoluta.

Materials and methods

Study site

The Canary Islands are a volcanic archipelago which

includes seven islands and four islets. Although

politically part of Spain, they are situated in the

eastern subtropical North Atlantic (27�370–29�270N,

13�200–18�200W) near the Western Sahara region of

West Africa. The Canarian archipelago experiences a

Mediterranean-type climate of hot, dry summers and

wet, warm winters. It is, however, characterised by a

pronounced ecological heterogeneity. Whereas the

easternmost islands of the Canaries, Fuerteventura

and Lanzarote, exhibit a desert-like climate and

vegetation, in the western islands of Gran Canaria,

Tenerife, El Hierro, La Gomera and La Palma the

altitudinal zonation of vegetation is particularly

marked, and strongly differentiated between the

22 A. Polaszek et al.

123

windward and leeward sides of the islands (Fernan-

dez-Palacios and Nicholas 1995).

Field collection of Trichogramma

Parasitoids were obtained from Lepidoptera eggs

collected on leaves of banana (Musa acuminata

Colla), tomato (Solanum lycopersicum L.), squash

(Cucurbita maxima Duch. ex Lam.), sweet pepper

(Capsicum annuum L.), green beans (Phaseolus

vulgaris L.) and some associated weeds (Nicotiana

glauca Graham, Solanum nigrum L.). Any emergent

parasitoids were either collected directly into 96%

ethanol in 1.5 ml Eppendorfs, or allowed to mate

and exposed to fresh Ephestia kuehniella Zeller

eggs in the laboratory in order to initiate a culture.

After possible mating and oviposition, these indi-

viduals were also collected into 96% ethanol.

Preserved specimens were carefully labelled with

details of the original collection locality, host egg

species and host plant, and date of collection.

Specimens were then sent to the first author (AP)

for identification.

Collection localities

Specimens of Trichogramma species were success-

fully obtained from the localities in Table 1.

Morphological identification

Dried specimens were initially mounted on card

squares and then on microscope slides using the

method described by Noyes (1982) with some

modifications as follows: for maceration, specimens

were heated in 10% KOH at 80�C for 10 min. This

was done without prior dissection, except for removal

of the wings. Following neutralisation with glacial

acetic acid, specimens were washed in distilled water

for 1 h, then dehydrated for 5 min in graded alcohols

of the following concentrations: 35, 70, 85, 100%.

After clearing in clove oil and allowing for evapo-

ration of alcohol, specimens were dissected in

Canada Balsam. The antennae, head, genitalia (males

only) and remaining body parts were mounted

separately on a single slide, together with the

previously mounted wings. For male mounts, the

aedeagus was removed from the genital capsule.

Identification of Trichogramma species relies very

heavily on examination of the male genitalia and to a

lesser extent the male antennae. For this reason males

were preferentially selected for this complex and

time-consuming procedure. Where possible, females

corresponding to species suggested by male identifi-

cation were later selected and mounted. Species were

initially identified based on morphology, using a

combination of the following published taxonomic

accounts: Lin (1994), Nagaraja and Nagarkatti (1970),

Nagarkatti and Nagaraja (1971), Pinto (1999), Pintu-

reau and Babault (1988) and Pintureau (2008). The

collections of the Natural History Museum (London)

contain extensive reference material of Trichogram-

ma species, including four of the five species in this

study, as well as paratypes of two of them. All

available relevant material was examined.

For preparation of the figures below, a fore wing,

the antennae and genitalia were scanned with a Leitz

Dialux compound microscope using Nomarski Dif-

ferential Interference contrast illumination, enabling

separate scanning of the upper and lower parts of

the antennae and genitalia. Scanned sections were

stacked and combined using AutoMontage� soft-

ware, and the final images edited with Adobe

Photoshop CS4�.

All specimens from the morphological study are

deposited in the Natural History Museum, London,

UK (NHM). Three voucher specimens of the T. achae-

ae population used subsequently for biocontrol of

Table 1 Collection localities of Trichogramma species in the

Canary Islands

Island Locality Coordinates

Gran Canaria Arucas 28�0705800N 15�3005400W

El Hierro Frontera 27�4605100N 18�1301100W

La Palma El Remo 28�3302100N 17�5301700W

Fuencaliente 28�2804300N 17�5104200W

Brena Baja 28�3604400N 17�4503100W

Los Llanos 28�3702700N 17�5505300W

Tenerife Caldera del Rey 28�0403100N 16�4301500W

Cueva del Polvo 28�1304400N 16�4905700W

Guargacho 28�0105200N 16�3903200W

Guıa de Isora 28�1102200N 16�4803400W

Hoya Meleque 28�2402200N 16�3303100W

Pajalillos 28�3104200N 16�2301300W

Valle de Guerra 28�3202600N 16�2300700W

Molecular and morphological diagnoses of five species of Trichogramma 23

123

T. absoluta in Spain also had DNA extracted using a

non-destructive protocol which is also preserved (at

-80�C) in the Molecular Collections Facility (MCF)

at NHM (Figs. 1, 2).

Morphological terminology follows Pinto (1999).

The specialised terminology of the male genitalia

and antenna is given in Figs. 3–8 (modified from

Pinto 1999). Host records are based largely on

those in the Universal Chalcidoidea Database (http://

www.nhm.ac.uk/research-curation/research/projects/

chalcidoids), modified by Polaszek (2010) and the

present study.

Molecular identification

39 samples were selected from the original samples

and sent to the 2nd and 3rd authors PFR-J and RS

(UC Riverside, USA) for DNA extraction and

amplification of the ITS2 region. DNA was extracted

from single female wasps using the Chelex method.

The wasps were crushed in a 0.5 ml micro-centrifuge

tube with a closed Pasteur pipette and ground in 60 ll

5% Chelex-100 and 2 ll of Proteinase K (20 mg

ml-1), followed by incubation for 1 h at 55�C, and

finally for 10 min at 99�C.

The polymerase chain reaction (PCR) was used to

amplify the ITS2 region of each specimen using

primers described in Stouthamer et al. (1999). Reac-

tions were performed in 25 ll volumes containing: 19

Thermopol Reaction Buffer (New England BioLabs,

Ipswich, MA, USA); 200 lM each of dATP, dCTP,

and dGTP; 400 lM dUTP; 0.2 lM each primer; 1 U

Taq polymerase (NEB); 2 ll template DNA (concen-

tration not determined). Amplification was achieved

using a Mastercycler ep gradient S (Eppendorf North

America Inc., New York, NY, USA), programmed for:

3 min at 95�C; followed by 37 cycles of 45 s at 94�C,

45 s at 53�C, and 1 min at 72�C; and a final step of

3 min at 72�C. PCR products were visualized after

electrophoresis on 1.5% agarose gel stained with

ethidium bromide, to confirm amplification.

Species were identified based on the size of their

ITS2 PCR product (e.g. Kumar et al. 2009; Silva

et al. 1999; Sumer et al. 2009; Thomson et al. 2003).

The PCR products of a subset of 14 samples were

directly sequenced in both directions at the Institute

for Integrative Genome Biology, University of

California, Riverside, USA. Sequences were aligned

manually using BioEdit version 7.0.9.0 (Hall 1999),Fig

.1

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ases

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ign

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ies


123

http://www.nhm.ac.uk/research-curation/research/projects/chalcidoids



and compared to the ITS2 sequences of known

Trichogramma spp. (Figs. 1, 2). Positions 1–82 in the

manually aligned sequence are identical to the result

obtained by aligning in BioEdit with the option

‘‘accessory application—ClustalW multiple align-

ment’’ using default parameters. Complete ITS2

sequences of 16 specimens, including all the species

treated here, have been deposited in Genbank under

accession numbers JF415934–JF415939.

Results

Morphological examination of antennae, male geni-

talia and wings enabled three morphospecies to be

easily distinguished: T. achaeae, T. bourarachae and

T. euproctidis. All three are new records for the

Canary Islands, from where no Trichogramma

species had been recorded previously. T achaeae,

described originally from India, proved in laboratory

experiments to be a very promising candidate for the

inundative biological control of T. absoluta (Cabello

et al. 2009a) and subsequently also in field experi-

ments (Vila et al. 2010). T. evanescens and T. near

brassicae could also be distinguished to some

extent morphologically, but with some difficulty.

PCR confirmed the presence of the three morpholog-

ically distinct species, and indicated the presence of

the two others: T. evanescens and two specimens of

an unknown species near T. brassicae.

In just two collections out of the 39 examined was

there disagreement between the results of the molec-

ular and morphological identification. One of these

concerned T. bourarachae (evident from morphol-

ogy) identified with PCR as T. euproctidis, and the

second a collection of T. achaeae misidentified as

T. evanescens. It seems most probable that these two

collections originally contained a mixture of species,

possibly due to contamination. Overall, the congru-

ence between morphological and molecular (PCR)

identification (95%) was extremely high.

All five species can be distinguished by their ITS2

sequences (Figs. 1, 2) but also based on the size of the

amplified PCR product: T. euprocidis: 377–378 nt;

T. evanescens; 430–432 nt; T. near brassicae; 411 nt;

T. achaeae; 518–519 nt; T. bourarachae:*560 nt. The

sequence of T. evanescens from the Canary Islands

differs very slightly from ‘‘standard’’ T. evanescens,

represented in Figs. 1 and 2 by the specimen from

Oman. T. near brassicae differs by approximately 7%

in ITS2 sequence from the standard T. brassicae,

represented in Figs. 1 and 2 by the specimen from

Turkey.

Discussion

Trichogramma in the Canary Islands

It is perhaps surprising that after just a few months of

field collecting, five Trichogramma species have been

discovered in the Canary Islands where no Trichogram-

ma species had been recorded previously. Furthermore,

the species have particular characteristics regarding

their known previous distribution. T. achaeae was

described from Bangalore in Southern India (Nagaraja

and Nagarkatti 1970), but has since been recorded from

many localities around the world, including (recorded

here for the first time) Hawaii. It appears, therefore, to be

a good coloniser, being highly adaptive. This ability

raises legitimate concerns about its possible non-target

effects in areas of its spread, either accidental or

deliberately (Desneux et al. 2010). Of the possible

non-target Lepidoptera genera listed by these authors,

Fig. 2 Bases 150–180 in the aligned ITS2 fragment for four Trichogramma species


123

Figs. 3–8 Morphological

terminology for antennal

(Fig. 3) and male genitalia

(Figs. 4–8) characters

(after Pinto 1999)


123

none has so far been recorded as a host of T. achaeae (see

below), but host range testing will be necessary prior to

future field releases.

T. bourarachae was described from Morocco, and

is now known additionally from Egypt, Tunisia,

Portugal (Polaszek 2010) and the Canary Islands.

T. euproctidis and T. evanescens are very widespread

Old World species, although many published records

are certainly based on misidentifications. Finally,

T. near brassicae appears to be a new species,

possibly endemic to the Canary Islands, but requiring

further study.

T. achaeae as a biocontrol agent of Chrysodeixis

chalcites and Tuta absoluta

The frequency of T. achaeae attacking eggs of

C. chalcites in the field suggests good potential for

this species as a control agent in banana crops, and

field trials against this host are ongoing (del Pino,

unpublished data). However, against T. absoluta,

T. achaeae is already proving an effective biocontrol

agent (Cabello et al. 2009a). Desneux et al. (2010)

found that the release of T. achaeae at a rate of

50 adults m-2 two times a week during the first

ten weeks of the tomato growing season significantly

reduced the number of T. absoluta larvae, leaf mines

and damaged fruits, compared with control plots. Vila

et al. (2010) found that releases of 25 T. achaeae

adults m-2 per week during seven weeks also

provides significant control of T. absoluta. These

application rates appear to be high, but are within

what is commonly used in inundative biological

control programs in other crops (Mills 2010). For use

in the field T. achaeae is mass-reared on eggs of

Ephestia kuhniella, and parasitized eggs are distrib-

uted to growers in user-friendly dispensers (Desneux

et al. 2010) (Figs. 9–13, 14–18).

Species accounts

Trichogramma achaeae Nagaraja & Nagarkatti

1970 (Figs. 9, 14, 19)

Synonymy

Trichogramma achaea Nagaraja & Nagarkatti

Diagnosis. Flagellum of male antenna (Fig. 9)

2.1 ± 0.19 length of scape (n = 9). Flagellar length/

flagellar width (not including setae) 5.9 ± 0.6 (n = 9);

max. flagellar setal length/basal flagellar width

2.7 ± 0.4 (n = 9). Terminal placoid sensilla extend-

ing beyond the end of the flagellum. Genital capsule

length (Fig. 14a) 2.8 ± 0.39 width (n = 9), sides very

slightly narrowed at level of IVP. AD/GL = 0.2

(n = 9); AW/GW = 0.5 ± 0.2 (n = 9); DAL/GL =

0.5 (n = 9). IVP (Fig. 10a) very small. DLA (Fig. 14b)

originating at middle of GC, linguiform and parallel-

sided for some of its length; rounded at apex. Shoulders

not present at base of DLA. Aedeagus (Fig. 14c) length

equal to GL; 1.9 ± 0.39 apodemes (n = 7).

Distribution. Asia: China, India, New Caledonia,

Russia; Europe: France (introduced), Portugal

(Acores), Russia, Spain (introduced to mainland.

Canary Islands: El Hierro, Gran Canaraia, La Palma,

Tenerife); Africa: Cape Verde; Americas: Argentina,

Barbados, Chile, Trinidad & Tobago, Hawaii, USA.

Hosts. Diptera: Anthomyiidae: Atherigona soccata;

Lepidoptera: Gelechiidae: Pectinophora gossypiella;

Sitotroga cerealella, Tuta absoluta; Geometridae: Boar-

mia variegata; Noctuidae: Achaea janata; Anticarsia

gemmatalis; Chrysodeixis chalcites; Cornitoplusia sp.;

Earias sp.; E. insulana; E. vittella; Helicoverpa armi-

gera; H. zea; Mamestra brassicae; Spodoptera sp.;

Tiracola plagiata; Trichoplusia ni; Notodontidae: Clos-

tera cupreata; Oecophoridae: Opisina arenosella;

Pieridae: Eurema sp. Pyralidae (including Crambridae):

Chilo partellus; Corcyra cephalonica; Loxostege sticti-

calis; Sphingidae: Acherontia styx; Agrius convolvuli;

Tortricidae: Cydia koenigana, Laspeyresia koenig-

ana; Yponomeutidae: Plutella xylostella.Nymphalidae:

Danaus plexippus; Lyceanidae: Lampides boeticus:

Material examined (specimens marked with ‘‘*’’

were confirmed by sequencing ITS2): Paratypes 9 #:

India: West Bengal, Kalimpong iv.1965 (V.R. Pha-

lak) ex egg Achaea janata CIE 2801 (NHM). 1#*

Spain: Islas Canarias, Tenerife, Valle de Guerra,

26/01/2009 UTM 28R 0364467 3157871 Solanum

lycopersicum F05/09-55 ex C. chalcites; 1$ 1#

Tenerife, Guargacho 23/10/2008 GU05-06 Musa

acuminata ex C. chalcites; 1#* Tenerife, Guıa de

Isora, 10/03/2009 UTM 28R 0322368 3119543 TF18/

09-29 Nicotiana glauca ex Cornitoplusia sp.; 1#* La

Palma, Fuencaliente, 18/05/2009 UTM 28R 0219803

3153587 M. acuminata LP10/09-07 ex C. chalcites;

1#* same data but 20/03/2009 LP04/09-05; 1#

same data but S. lycopersicum LP11/09-96; 1#* La

Palma, Fuencaliente, 24/04/2009 UTM 28R 0219803


123

Figs. 9–13 Trichogramma male antennae, inner (a) and outer (b) aspects. Figure 9 T. achaeae; Fig. 10 T. bourarachae;

Fig. 11 T. euproctidis; Fig. 12 T. evanescens; Fig. 13 T. near brassicae


123

3153587 S. lycopersicum LP10/09-07 ex C. chalcites;

1# same data but LP09/09-29; 1# same data but

25/07/2008 LP17-21; 1#* same data but 04/06/2009

LP16/09-37; 2#* same data but Phaseolus vulgaris

LP17/09-44; 1# same data but LP17/09-61; 2#* La

Palma, Los Llanos, 14/07/2009 N. glauca LP21/09-

32 ex C. chalcites; 2#* La Palma, El Remo, 18/05/

2009 UTM 28R 0217434 3162190 Capsicum annuum

LP12/09-04 ex C. chalcites; 1#* same data but

20/03/2009 LP02/09-01; 1# same data but LP13/09-

Figs. 14–18 Trichogramma species, male genitalia. a Parameres, volsellae, intervolsellar process; b dorsal lamina; c: aedeagus.

Figure 14 T. achaeae; Fig. 15 T. bourarachae; Fig. 16 T. euproctidis; Fig. 17 T. evanescens; Fig. 18 T. near brassicae


123

13; 1$ 1# same data but 30/09/2008 LP22-21; 1#

same data but 30/09/2008 LP22-01 M. acuminata ex

C. chalcites; 2#* La Palma, Brena Alta, 24/04/2009

28R UTM 0230252 3168161 M. acuminata LP08/09-

12 ex C. chalcites; 1# same data but 05/08/2009

LP23/09-51; 1$*1# Gran Canaria, Arucas, 11/05/

2009 UTM 28R 0449402 3112042 S. lycopersicum

GC09/09-16 ex C. chalcites; 1$ 3#* El Hierro,

Frontera, 14/12/2008 M. acuminata, HR10/08-09 ex

C. chalcites; 2#* same data but 22/01/2009 HR01/

09-07, HR01/09-10.

Trichogramma bourarachae Pintureau & Babault

1988 (Figs. 10, 15, 20)

Diagnosis. Flagellum of male antenna (Fig. 10) 2.09

length of scape (n = 4). Flagellar length/flagellar width

(not including setae) 5.9 ± 0.6 (n = 4); max. flagellar

setal length/basal flagellar width 2.3 ± 0.2 (n = 3).

Terminal placoid sensilla extending beyond the end

of the flagellum. Genital capsule length (Fig. 15a)

3.7 ± 0.39 the width (n = 4), sides strongly narrowed

at level of IVP. AD/GL = 0.2 (n = 4); AW/GW = 0.6

(n = 4); DAL/GL = 0.5 (n = 4). IVP (Fig. 15a) small.

DLA (Fig. 15b) originating in basal third of GC, narrow

and pointed at apex. Shoulders not present at base

of DLA. Aedeagus (Fig. 15c) length equal to GL;

2.4 ± 0.29 apodemes (n = 4).

Distribution. Europe: Portugal; Spain (including

Canary Islands, Tenerife). Africa: Egypt, Morocco,

Tunisia.

Hosts. Lepidoptera: Lymantriidae: Euproctis

chrysorrhoea; Noctuidae: Chrysodeixis chalcites;

Helicoverpa armigera; Nymphalidae: Vanessa cardui;

Figs. 19–23 Trichogramma species, fore wing. Figure 19 T. achaeae; Fig. 20 T. bourarachae; Fig. 21 T. euproctidis; Fig. 22T. evanescens; Fig. 23 T. near brassicae


123

Pyralidae: Ectomyelois ceratoniae; Ephestia kuehni-

ella; Palpita unionalis; Yponomeutidae: Prays oleae;

Neuroptera: Chrysopidae: Chrysoperla carnea.


were confirmed by sequencing ITS2): Paratype 1#:

Marocco: Baume (B.Pintureau, M. Babault) ex egg

E. kuehniella (NHM). 1#* Spain: Islas Canarias,

Tenerife, Valle de Guerra, 28/07/2009 UTM 28R

0364195 3154856 N. glauca TF43/09-25 ex C. chalcites;

1$ Tenerife, Cueva del Polvo 16/03/2009 UTM

28R 0320185 3123941 N. glauca TF20/09-08 ex

C. chalcites; same data but: 1# N. glauca TF20/09-19

ex Cornitoplusia sp.; 2$*1#* N. glauca TF20/09-33 ex

C. chalcites.

Trichogramma euproctidis (Girault, 1911)

(Figs. 11, 16, 21)

Synonymy

Pentarthron euproctidis Girault

Trichogramma turkestanica Meyer

Trichogramma meyeri Sorokina



flagellar width (not including setae) 5.9 ± 0.6

(n = 10); max. flagellar setal length/basal flagellar

width 3.3 ± 0.4 (n = 10). Terminal placoid sen-

silla extending beyond the end of the flagellum.

Genital capsule length (Fig. 16) 2.7 ± 0.39 the width

(n = 10), sides very slightly narrowed at level of IVP.

AD/GL = 0.2 (n = 9); AW/GW = 0.6 (n = 9);

DAL/GL = 0.6 (n = 9). IVP (Fig. 16a) large, prom-

inent. DLA (Fig. 16b) originating at middle of GC,

triangular and rounded at apex. Shoulders present at

base of DLA. Aedeagus (Fig. 16c) length equal to GL;

2.2 ± 0.19 apodemes (n = 10).

Distribution. Asia: Armenia, China, Japan,

Kazakhstan, Russia, Tadzhikistan, Turkmenistan,

Turkey, Uzbekistan, Vietnam; Europe: Belarus,

Bulgaria, Denmark, France, Greece, Italy, Moldova,

Portugal, Russia, Spain (incl. Canary Islands: Gran

Canaria, Tenerife), Ukraine; Africa: Egypt, Morocco;

Americas: Argentina, Chile, Cuba, Peru.

Hosts. Diptera: Anthomyiidae: Erioischia brassi-

cae; Lepidoptera: Gelechiidae: Sitotroga cerealella;

Lymantriidae: Euproctis chrysorrhoea; Nygmia

phaeorrhoea; Orgyia antiqua; Noctuidae: Agrotis

segetum; Amathes c-nigrum; Chrysodeixis chalcites;

Helicoverpa armigera; Mamestra brassicae; Sesamia

nonagrioides; Syngrapha circumflexa; Nymphalidae:

Vaness cardui; Pieridae: Pieris brassicae; Pyralidae

(incl. Crambidae): Chilo agamenon; Corcyra cepha-

lonica; Ephestia kuehniella; Loxostege sticticalis;

Margaronia quadristigmalis; Mescinia peruella;

Ostrinia nubilale; Sphingidae: Agrius convolvuli;

Tortricidae: Archips rosanus; Cydia pomonella;

Epichoristodes acerbella; Grapholitha molesta;

Lobesia botrana; Yponomeutidae: Plutella maculi-

pennis; Prays oleae. Neuroptera: Chrysopidae:

Chrysoperla carnea.


were confirmed by sequencing ITS2): 1#* Spain:

Islas Canarias, Tenerife, Hoya Meleque, 04/02/2009

UTM 28R 0347304 3143191 Solanum lycopersicum

TF08/09-41 ex Chrysodeixis chalcites; same data but:

1#* 31/03/2009 S. lycopersicum TF26/09-27 ex C.

chalcites; 1#* Tenerife, Guargacho 13/02/2009 UTM

28R 0336906 3101763 Musa acuminata TF10/09-11

ex C. chalcites; same data but: 1# 23/10/2008 Musa

acuminata Gu05-16 ex C. chalcites; 1# Tenerife,

Guıa de Isora 10/03/2009 TF18/09-47 UTM 28R

0322368 3119543 N. glauca ex Cornitoplusia sp.;

same data but: 1# N. glauca TF18/09-38 ex Corni-

toplusia sp.; 2#* 1$* Tenerife, Caldera del Rey

25/06/2009 TF41/09-77 UTM 28R 0330902 3106753

S. lycopersicum ex C. chalcites; same data but:1#*

17/04/2009 S. lycopersicum TF30/09-43 ex C. chal-

cites; 1$ Tenerife, Cueva del Polvo 16/03/2009 UTM

28R 0320185 3123941 TF20/09-33 N. glauca ex

Cornitoplusia sp.

Trichogramma evanescens Westwood, 1833

(Figs. 12, 17, 22)

Synonymy

Calleptiles latipennis Haliday

Calleptiles vitripennis (Walker)

Pentarthron carpocapsae Schreiner

Pentarthron carpocapsai Schreiner

Pteroptrix evanescens (Westwood)

Trichogramma barathrae Skriptshinsky

Trichogramma cacoeciae pini Meyer

Trichogramma carpocapsae (Schreiner)

Trichogramma evanescens piniperda Wolff

Trichogramma pini Meyer


123

Trichogramma piniperdae Wolff (Pintureau (2008)

treats T. piniperda as a valid species)

Trichogramma rhenana Voegele & Russo

Trichogramma rhenanum Voegele & Russo

Trichogramma vitripennis Walker

Trichogramma vitripenne Walker

The true identity of T. evanescens is still uncertain

at the time of writing, but for practical reasons, most

workers follow Pintureau’s interpretation of this

highly cited species (see Pintureau 2008).



flagellar width (not including setae) 5.6 ± 0.1 (n = 4);

max. flagellar setal length/basal flagellar width

3.1 ± 0.2 (n = 4). Terminal placoid sensilla extend-

ing beyond the end of the flagellum. Genital capsule

length (Fig. 17) 2.8 ± 0.29 the width (n = 4), sides

very slightly narrowed at level of IVP. AD/GL = 0.3

(n = 4); AW/GW = 0.6 (n = 4); DAL/GL = 0.6

(n = 4). IVP (Fig. 17a) large, prominent. DLA

(Fig. 17b) originating at middle of GC, triangular and

rounded at apex. Shoulders present at base of DLA.

Aedeagus (Fig. 17c) length equal to GL; 2.2 ± 0.19

apodemes (n = 4).

Distribution. Asia: Armenia, Azerbaijan, China,

Georgia, India, Iran, Israel, Kazakhstan, Oman,

Pakistan, Philippines, Russia, Sri Lanka, Turkey,

Turkmenistan, Uzbekistan, Vietnam; Europe: Aus-

tria, Belarus, Belgium, Bulgaria, Czech Republic,

Denmark, France, Germany, Hungary, Ireland, Italy,

Lithuania, Macedonia, Moldova, Netherlands,

Poland, Portugal (including Madeira), Romania,

Russia, Serbia, Slovakia, Spain (incl. Canary islands:

La Palma, Tenerife), Sweden, Switzerland, Turkey,

Ukraine, United Kingdom, Yugoslavia (former, pre

1991). Africa: Comores, Egypt, Libya, Madagascar,

Mauritius, Morocco.

Hosts. Coleoptera: Bruchidae: Bruchus obtectus;

Chrysomelidae: Cassida deflorata; C. nebulosa; C. no-

bilis; C. vittata; Donacia simplex; Curculionidae:

Rhynchaenus testaceus; Dermestidae: Dermestes mac-

ulatus; Rhynchitidae: Rhynchites auratus; R. betulae;

Tenebrionidae: Tribolium castaneum; Diptera:

Anthomyiidae: Atherigona soccata; Pegomya betae;

P. hyoscyami; Stratiomyiidae: Oxycera sp.; Stratiomys

sp.; Syrphidae: Melanostoma mellinum; Paragus

quadrifasciatus; Syrphus sp.; S. balteatus; S. pyrastri;

S. vitripennis; Tabanidae: Chrysops sp.; C. caecutiens;

C. relictus; Tabanus sp.; Hemiptera: Cimicidae: Cimex

lectularius; Hymenoptera: Pamphiliidae: Acantholyda

erythrocephala; A. posticalis; A. stellata; Cephalcia

abietis; C. arvensis; C. signata; Tenthredinidae: Cal-

iroa cerasi; Croesus septentrionalis; Emphytus tener;

Pteronidea ferruginea; P. ribesii; Lepidoptera: Arctii-

dae: Arctia caja; Diacrisia obliqua; Eilema sp.;

Hyphantria cunea; Spilosoma sp.; Bombycidae:

Rondotia menciana; Danaidae: Danaus chrysippus;

Gelechiidae: Pectinophora sp.; P. gossypiella; Phthor-

imaea operculella; Sitotroga cerealella; Geometridae:

Boarmia grisescens; Bupalus piniarius; Cidaria

bilineata; C. didymata; Crocallis elinguaria; Erannis

defoliaria; Lambdina fiscellaria; Operophtera

brumata; Glyphipterygidae: Anthophila atrilineata;

Lasiocampidae: Cosmotriche potatoria; Dendrolimus

pini; D. punctatus; D. segregatus; D. spectabilis;

Malacosoma disstria; M. neustria; Leptidae: Atherix

sp.; Lycaenidae: Cacyreus marshalli; Thecla betulae;

Virachola livia; Lymantriidae: Arctornis chrysor-

rhoea; Euproctis lunata; E. phaeorrhoea; Laelia

salicis; Lymantria dispar; L. monacha; Nygmia phae-

orrhoea; Orgyia antiqua; O. gonostigma; Stilpnotia

salicis; Noctuidae: Acontia luctuosa; Acronicta aceris;

A. major; A. rumicis; A. tridens; Agrotis exclamationis;

A. ipsilon; A. segetum; Amathes c-nigrum; Antitype

flavicincta; Apopestes spectrum; Autographa sp.;

A. gamma; Barathra brassicae; Catocala elocata;

Chrysodeixis chalcites; Cirrhia gilvago; Discestra

trifolii; Earias sp.; E. cupreoviridis; E. fabia; E. insul-

ana; Euxoa obelisca; E. segetum; Gonospileia glyph-

ica; Helicoverpa armigera; H. assulta; H. virescens;

H. zea; Mamestra sp.; M. brassicae; M. oleracea;

M. trifolii; Naranga aenescens; Noctua pronuba; Oria

musculosa; Panolis flammea; Parallelia algira; Phala-

ena typica; Phlogophora meticulosa; Phytometra

gamma; Plusia gamma; Polia oleracea; P. pisi;

P. suasa; Pyrrhia umbra; Rivula atimeta; Sarrothripus

musculana; Scotia ipsilon; Sesamia cretica; S. non-

agrioides; Spaelotis pronubana; Spodoptera sp.;

S. littoralis; S. litura; Tholera popularis; Trachea

triplicis; Trichoplusia ni; Triphaena pronuba; Noto-

dontidae: Lampronadata cristata; Phalera bucephala;

P. bucephaloides; Thaumetopoea pityocampa; Nymp-

halidae: Nymphalis polychloros; Oecophoridae:

Depressaria nervosa; Endrosis lactella; Opisina

arenosella; Papilionidae: Iphiclides podalirius; Papi-

lio polytes; Pieridae: Aporia crataegi; Leptidea sina-

pis; Pieris sp.; P. brassicae; P. daplidice; P. napi;


123

P. rapae; Pyralidae: (incl. Crambidae): Achroia

grisella; Anagasta sp.; Cadra cautella; Chilo sp.;

C. agamemnon; C. indicus; C. infuscatellus; C. partel-

lus; C. sacchariphagus; C. simplex; C. suppressalis;

Cnaphalocrocis medinalis; C. cephalonica; Crambus

geniculeus; Diatraea sp.; Ectomyelois ceratoniae;

Ephestia sp.; E. calidella; E. cautella; E. elutella;

E. kuehniella; Etiella zinckenella; Evergestis forfical-

is; Galleria sp.; G. mellonella; Glyphodes pyloalis;

Hymenia recurvalis; Loxostege sticticalis; Marasmia

patnalis; Maruca vitrata; Ostrinia furnacalis; O. nu-

bilale; Palpita unionalis; Phlyctaenia forficalis;

Plodia interpunctella; Pyrausta machaeralis; Sale-

bria semirubella; Spectrobates ceratoniae; Saturnii-

dae: Attacus cynthia; A. ricini; Sphingidae: Celerio

lineata; Manduca sexta; Smerinthus populi; Sphinx

pinastri; Tortricidae: Adoxophyes orana; A. reticul-

ana; Archips crataeganus; A. pronubana; A. rosanus;

Cacoecia rosanus; Cacoecimorpha pronubana;

Carpocapsa pomonella; Choristoneura fumiferana;

Clysia ambiguella; Cnephasia longana; Cneph-

asia pumicana; Cydia funebrana; C. pomonella;

Epichoristodes acerbella; Epinotia pygmaeana;

E. tedella; Eupoecilia ambiguella; Grapholitha de-

lineana; Grapholitha funebrana; G. molesta; Gypso-

noma aceriana; Homona coffearia; Laspeyresia

microgrammana; L. molesta; L. nigricana; Lobesia

botrana; Pandemis chondrillana; Pandemis hepar-

ana; Petrova resinella; Rhopobota naevana; Rhya-

cionia buoliana; Sparganothis pilleriana; Tetramoera

schistaceana; Zeiraphera diniana; Yponomeutidae:

Acrolepiopsis assectella; Argyresthia conjugella;

Plutella sp.; P. maculipennis; P. xylostella; P. citri;

Prays oleae; Zygaenidae: Theresimima ampelophaga;

Zygaena sp.; Megaloptera: Sialidae: Sialis lutaria;

Neuroptera: Chrysopidae: Chrysoperla carnea;

C. ventralis; Chrysoperla sp.; Nothochrysa italica.


were confirmed by sequencing ITS2): 1#* Spain:

Islas Canarias, La Palma, El Remo, 18/05/2009 28R

0217434 UTM 3162190 Cucurbita maxima LP13/

09-30 ex Chrysodeixis chalcites; same data but:

1#* 20/03/2009 Nicotiana glauca LP03/09-12 ex

C. chalcites; 1#* Tenerife, Pajalillos 18/02/2009 28R

0364277 UTM 3156545 Solanum lycopersicum

LP12/09-01 ex C. chalcites.

Trichogramma near brassicae (Figs. 13, 18, 23)

Diagnosis. Flagellum of male antenna (Fig. 13) 1.99

length of scape (n = 1). Flagellar length/flagellar

width (not including setae) 4.7; max. flagellar setal

length/basal flagellar width 3.6 (n = 1). Terminal

placoid sensilla extending beyond the end of the

flagellum. Genital capsule length (Fig. 18a) 3.19 the

width (n = 1), sides narrowed at level of IVP. AW/

GW = 0.5 (n = 1); DAL/GL = 0.5 (n = 1). IVP

(Fig. 18a, b) large, prominent. DLA (Fig. 10b) orig-

inating at middle of GC, triangular and rounded at

apex. Shoulders present at base of DLA. Aedeagus

(Fig. 18c).

Distribution. Europe: Spain (Canary Islands: Gran

Canaria).

Host. Lepidoptera: Noctuidae: Chrysodeixis

chalcites.

Material Examined (confirmed by sequencing

ITS2): 2#* Spain: Gran Canaria, Arucas, 11/05/

2009 UTM 28R 0449402 3112042 Musa acuminata

GC07/09-17 ex Chrysodeixis chalcites.

Comments. The authors are currently undertaking

further examination of this species, including cross-

breeding experiments. The species will be formally

described in the near future.

Acknowledgments We are grateful to AgroBio S.L. and

ASPROCAN for their financial support and collaboration

during Trichogramma field collection. The research of M. del

Pino was financially supported by a pre-doctoral fellowship

granted by ‘‘Instituto Nacional de Investigacion y Tecnologıa

Agraria y Alimentaria (INIA)’’. The paper benefited greatly

from comments by two anonymous reviewers

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