Havelka et al 2012 aesa

SYSTEMATICS
Review and Key to the World Parasitoids (Hymenoptera: Braconidae:
Aphidiinae) of Aphis ruborum (Hemiptera: Aphididae) and Its Role as
a Host Reservoir
JAN HAVELKA,1
Zˇ ELJKO TOMANOVIC´ ,2
NICKOLAS G. KAVALLIERATOS,3
EHSAN RAKHSHANI,4
XAVIER PONS,5
ANDJELJKO PETROVIC´ ,2
KEITH S. PIKE,6
AND PETR STARY´ 1
Ann. Entomol. Soc. Am. 105(3): 386Ð394 (2012); DOI: http://dx.doi.org/10.1603/AN11108
ABSTRACT A review and illustrated key of the aphidiine parasitoids of Aphis ruborum (Bo¨rner and
Schilder)arepresentedincludingtheirdistribution.TheparasitoidspectrumofA.ruborumintheWest
Palaearctic is rich, composed of Aphidius colemani Viereck, Aphidius matricariae Haliday, Binodoxys
acalephae (Marshall), Binodoxys angelicae (Haliday), Ephedrus persicae Froggatt, Lipolexis gracilis
Fo¨rster,LysiphlebusconfususTremblayandEady,Lysiphlebusfabarum(Marshall),andPraonabjectum
(Haliday), and supplemented by the introduction of Lysiphlebus testaceipes (Cresson). In the Amer-
icas the parasitoid complex of A. ruborum consists of A. colemani, Aphidius ervi Haliday (South
America),andL.testaceipes(SouthandNorthAmerica).Furthermore,thereservoirroleofA.ruborum
in various ecosystems was investigated in Europe (France) and South America (Chile). Faunal
peculiarities and relationships of the parasitoid taxa are discussed together with a synopsis of their
potential as biocontrol agents.
KEY WORDS Rubus spp., Aphis ruborum, parasitoid complex, key, reservoir
Aphis ruborum (Bo¨rner and Schilder) is a monoecious
holocyclic species associated with wild and cultivated
blackberries (Rubus spp.), and occasionally on straw-
berries (Fragaria spp.) (Blackman and Eastop 2000,
2006). It originally was described as Doralis ruborum
from central Europe (Bo¨rner and Schilder 1931). A.
ruborumalsohasbeenrecordedinAsia(Bodenheimer
1937), Africa (Habib and El-Kady 1961), and South
America (Blackman and Eastop 1984). In 2009 it was
detected for the Þrst time in North America in Wash-
ington State (K.S.P., unpublished data).
Aphid parasitoids are a useful group for the research
on parasitoid reservoirs and respective environmental
relationships. The concept of foci of aphid parasitoids in
nature originally was introduced by Stary´ (1964), and is
nowcommonlyreferredtoasreservoirsorrefugia(Stary´
1970, 1986; Stary´ and Pike 1998; Kavallieratos et al. 2002,
2008). Various studies have been published on tritrophic
associations in crop and noncrop communities, and clas-
siÞcation of parasitoid reservoirs in agroecosystems
(Vo¨lkl and Stary´ 1988; Pike et al. 1997; Stary´ and Havelka
2008; Tomanovic´ et al. 2008, 2009).
It is the aim of the present contribution to summarize
information on the parasitoids of A. ruborum as an aid to
future taxonomic, biological, and biodiversity research,
and to characterize the role of A. ruborum in France and
Chile as a host reservoir of aphidiine parasitoids.
Materials and Methods
Specimens used in the current study were obtained in
the course of Þeld studies by the authors from numerous
countries (i.e., Chile, Czech Republic, France, Greece,
Iran, Iraq, Italy, Montenegro, Pakistan, Portugal, Serbia,
Spain, Turkey, United States), with material now depos-
ited in collections of P. Stary´, Czech Republic; Belgrade
NaturalHistoryMuseum,Serbia;BenakiPhytopatholog-
ical Institute, Greece; University of Zabol, Iran; Univer-
sity of Lleida, Spain; and Washington State University,
UnitedStates.Relevantmaterialalsowasexaminedfrom
Georgia by P. Stary´. The most intensive sampling of A.
ruborumonRubusspp.,consistingofbothliveandmum-
miÞed aphids, was undertaken in France (i.e., Montpel-
lier: gardens, parks; Antibes, Opio, Valbonne: gardens,
maqui forests, gardens; Corse: maqui forests, waste
places) and Chile (i.e., Chillań, Concoń, La Cruz, Los
Andes, Rinconada, Villa Alemana: gardens, parks; Col-
lipulli, N˜ iqueń, San Carlos, Santa Rosa, Parral, Pinto,
Talca: hedges, roadsides) from 1974 to 1986 and 1991Ð
1992, respectively.
1 Laboratory of Aphidology, Institute of Entomology, Biology Cen-
tre, Academy of Sciences of the Czech Republic, Branisˇovska´ 31,
37005 Cˇ eske´ Budeˇjovice, Czech Republic.
2 Institute of Zoology, Faculty of Biology, University of Belgrade,
Studentski trg 16, 11000 Belgrade, Serbia.
3 Corresponding author: Laboratory of Agricultural Entomology,
Department of Entomology and Agricultural Zoology, Benaki Phy-
topathological Institute, 8 Stefanou Delta str. 14561, KiÞssia, Attica,
Greece (e-mail: nick_kaval@hotmail.com).
4 Department of Plant Protection, College of Agriculture, Univer-
sity of Zabol, P. O. Box 98615Ð538, Zabol, I. R. Iran.
5 Universitat de Lleida, Department of Crop and Forest Science,
Centre UdL-IRTA, Rovira Roure 191, 25198, Lleida, Spain.
6 Washington State University, Irrigated Agriculture Research and
Extension Center, 24106 N. Bunn Rd., Prosser, WA 99350.
0013-8746/12/0386Ð0394$04.00/0 ᭧ 2012 Entomological Society of America

Parasitoids were obtained through in-lab rearings of
aphids from infested plants cut in the Þeld and placed
inplasticcages(size250ml)coveredwithnylonmesh.
At the lab samples were subdivided, with part used to
obtain voucher aphids for identiÞcation, and part held
for rearing of parasitoids. Voucher aphids were pre-
served in a solution of 90% ethanol and 75% lactic acid
at a ratio of 2:1 (Eastop and van Emden 1972). Caged
samples were held at 22ЊC until parasitoid emergence;
emerged parasitoids were preserved in ethanol.
In cases where original parasitoid material was not
examined, the review is based on literature records
and marked as “Material not examined”. New material
was obtained from Czech Republic, Montenegro, and
the United States by the authors. In those cases the
reportisfollowedbytheindication“Newhostrecord”.
Parasitoid adults were point- and usually slide-
mounted for detailed examination. Specimens for slides
were washed in distilled water, boiled in 10% KOH for
about 2 min, rewashed, then placed in a drop of Faure-
Berlese medium (Krantz 1978) for dissection or whole
mounting. The morphological terminology used in the
paper follows Sharkey and Wharton (1997).
Results
Aphidiine-Aphis ruborum Associations Worldwide
Aphidius colemani Viereck, 1912
Chile (Stary´ et al. 1993), Greece (Kavallieratos et al.
2001).
Aphidius ervi Haliday, 1834
Chile (Stary´ et al. 1993).
Aphidius matricariae Haliday, 1834
France (Stary´ et al. 1973), Greece (Kavallieratos et
al. 2001), Pakistan (Stary´ et al. 1998).
Aphidius sp.
Turkey (Aslan et al. 2004).
Binodoxys acalephae (Marshall, 1896)
al. 2001), Italy (Stary´ 1966), Spain (Pons and Stary´
2003), Turkey (Du¨zgu¨nes¸ et al. 1982) (Material not
examined).
Binodoxys angelicae (Haliday, 1833)
al. 2001), Italy (Stary´ 1966), Spain (Pons and Stary´
2003), Turkey (Du¨zgu¨nes¸ et al. 1982) (Material not
examined).
Ephedrus persicae Froggatt, 1904
Israel (Mackauer 1959) (Material not examined),
Spain (Stary´ et al. 2004), Turkey (Du¨zgu¨nes¸ et al.
1982) (Material not examined).
Lipolexis gracilis Fo¨rster, 1862
Italy(Stary´ 1966),Spain(MichelenaSavalandOltra
Moscardo´ 1987) (Material not examined).
Lysiphlebus confusus Tremblay and Eady, 1978
al. 2001), Israel (Mackauer 1960) (Material not exam-
ined), Italy (Stary´ 1966), Montenegro (New host re-
cord), Portugal (Cecõ´lio 1995) (Material not exam-
ined), Spain (Stary´ et al. 2004), Turkey (Du¨zgu¨nes¸ et
al. 1982) (Material not examined).
Lysiphlebus fabarum (Marshall, 1896)
Czech Republic (New host record), France (Stary´
et al. 1971), Georgia (Achvlediani 1981), Greece
(Kavallieratos et al. 2001), Iran (Stary´ 1979), Iraq
(Stary´ and Kaddou 1971), Italy (Stary´ 1966), Monte-
negro (New host record), Portugal (Stary´ et al. 1996),
Serbia (Kavallieratos et al. 2004), Spain (Pons and
Stary´ 2003), Turkey (Du¨zgu¨nes¸ et al. 1982) (Material
not examined), United Kingdom (Mu¨ller et al. 1999)
(Material not examined).
Lysiphlebus testaceipes (Cresson, 1880)
(In Comstock 1880).
Chile (Stary´ et al. 1993), France (Stary´ et al. 1988b),
Greece (Kavallieratos et al. 2001), Portugal (Cecõ´lio
1994) (Material not examined), Spain (Pons and Stary´
2003), United States (New host record).
Praon abjectum (Haliday, 1833)
France (Stary´ et al. 1975).
Praon sp.
Turkey (Aslan et al. 2004).
Parasitoid Composition of A. ruborum in France
and Chile. France has a rich spectrum of native aphi-
diines (A. matricariae, B. acalepahe, B. angelicae, L.
confusus, L. fabarum, P. abjectum: 107 specimens ex-
amined) supplemented by one introduced species, L.
testaceipes (141 specimens examined); in contrast,
Chile has a rather narrow spectrum consisting of L.
testaceipes (predominate species), A. colemani, and A.
ervi (462, 3, and 1 specimens examined, respectively).
Discussion
ParasitoidfaunalcomplexesassociatedwithA.rubo-
rum can be grouped as follows: 1) B. angelicae (Eu-
ropean deciduous forest); 2) E. persicae (Far Eastern
May 2012 HAVELKA ET AL.: REVIEW OF APHIDIINE PARASITOIDS OF A. ruborum 387

deciduous forest); 3) A. ervi, A. matricariae, B.
acalephae, L. gracilis, L. confusus, L. fabarum, and P.
abjectum (Eurasian Steppes); 4) A. colemani (East
Mediterranean); and 5) L. testaceipes (Nearctic)
(Stary´ 1970, Kavallieratos et al. 2004). In the western
Palaearctic, the complex is almost the same through-
out. One difference is the apparent absence of A.
colemani in west Mediterranean Europe; its native
home and distribution ranges from the east Mediter-
ranean to central Asia (Stary´ 1975; Kavallieratos et al.
2004, 2010). In the Americas the only known parasi-
toid of A. ruborum is L. testaceipes, which probably has
its origin in North America but also occurs now in
Central and South America (Zamora Mejõ´as et al.
2010). The aphid (A. ruborum) is considered a new
accidental introduction into North America.
A. ruborum in various environments in different
countries and regions, especially in the Mediterra-
nean, has positive biological signiÞcance. Noncrops
have been shown to harbor reservoirs of both native
and introduced parasitoid species. Tizado et al. (1992)
classiÞed the wild reservoirs of aphidiines attacking
aphidsofthegenusAphiswithagriculturalimportance
in the Leo´n Province of Spain. The association of A.
ruborum and native parasitoids was classiÞed as com-
mon in anthropogenic zones such as roadsides.
In southeastern Europe, Kavallieratos et al. (2002)
investigated various parasitoid reservoirs in crop and
noncrop situations, and studied directly the role of
Rubus ulmifolius Schott infested with A. ruborum as a
reservoir for aphid parasitoids and its impact to parasitic
biocontrol of Aphis gossypii Glover in nearby cotton
(Gossypiumsp.).L.fabarumwasthedominatespeciesin
a complex of parasitoids that led to almost 100% parasit-
ismofA.gossypii.Inthissetting,R.ulmifoliuswasahighly
usefulreservoirforparasitoidswithcross-overcapability
to cotton aphid. Tomanovic´ et al. (2009) also discussed
the role of noncrop aphid hosts in southeastern Europe,
Fig. 1–3. (1 and 2) Frontal aspect of head of Lysiphlebus species (females). (1) L. fabarum (Marshall). (2) L. testaceipes
(Cresson); (3) Forewing of A. colemani Viereck.
388 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 105, no. 3

including A. ruborum, the enhancement or population
buildup of economically important parasitoids [e.g., A.
colemani, A. ervi, L. fabarum, L. testaceipes, and Praon
volucre (Haliday)], and tritrophic relationships in agro-
ecosystem-dominated landscapes.
In Portugal, Cecõ´lio (1994) emphasized the positive
role of A. ruborum as a frequent host or host reservoir
for L. testaceipes in forests, Þelds, and roadsides, and
found that parasitism rates generally were high.
In Spain, Pons and Stary´ (2003) investigated the
association of the introduced exotic parasitoid L. tes-
taceipes on R. padi in wheat and A. ruborum in Rubus
sp. (noncrop Þeld margins) relative to the parasitoidÕs
population development and regional expansion in
alfalfa (Medicago sativa L.), wheat, and maize (Zea
mays L.) in the Iberian Peninsula. A. ruborum was found
tobeausefulhostforL.testaceipes,andadeÞnitivefactor
to the parasitoidÕs value as a promising biological control
Fig. 4–13. Forewing of Aphidius, Binodoxys, Ephedrus, Lipolexis, Lysiphlebus, and Praon species (females). (4) A.
matricariae Haliday. (5) A. ervi Haliday. (6) B. acalephae (Marshall). (7) B. angelicae (Haliday). (8) E. persicae Froggatt. (9)
L. gracilis Fo¨rster. (10) L. confusus Tremblay and Eady. (11) L. fabarum (Marshall). (12) L. testaceipes (Cresson). (13) P.
abjectum (Haliday).

agent in a region where native parasitoids are reported
to have low effect on pest species. The contributing role
and key association of A. ruborum-Rubus in the expan-
sion of L. testaceipes in the Iberian Peninsula (coastal
areas to inland mountainous areas) is treated in detail by
Pons et al. (2004) and Stary´ et al. (2004).
A. ruborum as a member of the Aphidinae aphids
was included as a new native host in the host list of the
exotic L. testaceipes almost immediately after its in-
troduction and establishment in Mediterranean
France (Stary´ et al. 1988a,b). Its quick establishment
in France, likely contributed to its further expansion
in the region. A recent example of the expansion is the
parasitization of the invasive aphid, Aphis illinoisensis
Shimer, by L. testaceipes in Algeria (Laamari and
Coeur dÕ Acier 2010; Havelka et al. 2011).
In North America, only one local parasitoid, L. testa-
ceipes, has adapted successfully to A. ruborum. This para-
sitoid is an important agent for natural biological control
of many economically important aphids, including Aphis
craccicora Koch, Aphis fabae, Aphis pomi De Geer, Aphis
spiraecola Patch, Brachycorynella asparagi (Mordvilko),
Brevicoryne brassicae (L.), Diuraphis noxia (Kurdju-
mov), Myzus cerasi (F.), Myzus persicae (Sulzer),
Phorodon humuli (Schrank), Rhopalosiphum insertum
(Walker), Rhopalosiphum padi (L.), Rhopalosiphum
maidis (Fitch), Schizaphis graminum (Rondani), Sito-
bion avenae (F.) (Pike et al. 2000).
Stary´ et al. (1993)reportedonA.ruborumasanexotic
species in Chile, well-established in local ecosystems,
detectable in a range of settings such as roadsides, waste
places,gardens,andingrovesalongirrigationditchesand
channels, which all simultaneously represent transzonal
biocorridors. It was demonstrated in Chile that A. rubo-
rum is not a pest, but an important host reservoir of L.
testaceipes.ThissameaphidisnowinArgentina(DelÞno
et al. 2002), and although there is no Þeld data on asso-
ciatedparasitoidsasyet,wepresumesimilaraphidÐpara-
sitoidrelationshipsaredevelopingasindicatedforneigh-
boring Chile.
The European and Mediterranean Plant Protection
Organization (EPPO) in a recent decision, removed L.
testaceipes from the EPPO “positive list” on grounds it
might displace native parasitoid species because of its
wide host range, expanding geographic distribution, and
its ability to adapt to and thrive in a range of environ-
mentsfromagro-ecosystemstoforests(EPPO2009).We
principally disagree with such an approach because of
host range patterns and their predictability in new areas,
but this discussion exceeds the topics of the presented
paper.
Key to Female Aphidiines Attacking A. ruborum
1. Forewing with eight cells. (Fig. 8) . . . . .
. . . . . . . . . . Ephedrus persicae Froggatt
1Ј. Forewing with Ͻ8 cells (Figs. 3Ð7,
9Ð13) . . . . . . . . . . . . . . . . . . . . . . 2
2 (1Ј). Forewing RS ϩ M vein present (Fig.
13) . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . Praon abjectum (Haliday)
2Ј. Forewing RS ϩ M vein absent (Figs. 3Ð7,
9Ð12) . . . . . . . . . . . . . . . . . . . . . . 3
Fig. 14–22. (14Ð16) Anterolateral aspect of petiole of Aphidius species (females). (14) A. colemani Viereck. (15) A. ervi
Haliday (16) A. matricariae Haliday; (17Ð22) Dorsal aspect of petiole of Binodoxys, Lipolexis, and Lysiphlebus species
(females). (17) B. acalephae (Marshall). (18) B. angelicae (Haliday). (19) L. gracilis Fo¨rster. (20) L. confusus Tremblay and
Eady. (21) L. fabarum (Marshall). (22) L. testaceipes (Cresson).

3 (2Ј). Forewing M & m-cu vein complete (Figs.
3Ð5) or incomplete (Figs. 10Ð12) . . . . 4
3Ј. Forewing M and m-cu vein absent and
only r & RS vein developed (Figs. 6 and
7, 9) . . . . . . . . . . . . . . . . . . . . . . . 9
4 (3). Forewing M & m-cu complete throughout
(Figs. 3Ð6). Ovipositor sheath truncated
at tip (Figs, 23Ð25) . . . . . . . . . . . . . . 5
4Ј. Forewing M & m-cu incomplete (Figs. 10Ð
12). Ovipositor sheath sharply pointed at
tip (Figs. 29Ð31) . . . . . . . . . . . . . . . 7
5 (4). Anterolateral area of petiole rugose (Fig. 15).
. . . . . . . . . . . . . . Aphidius ervi Haliday
5Ј. Anterolateral area of petiole costate (Fig.
14) or costulate (Fig. 16) . . . . . . . . . . 6
Fig. 23–30. (23Ð25) Lateral aspect of genitalia of Aphidius species (females). (23) A. colemani Viereck. (24) A. matricariae
Haliday. (25) A. ervi Haliday. (26 and 27) Lateral aspect of genitalia and last sternal prong of Binodoxys species. (26) B.
acalephae (Marshall). (27) B. angelicae (Haliday); (28Ð31) Lateral aspect of genitalia of Lipolexis and Lysiphlebus species
(females). (28) L. gracilis Fo¨rster. (29) L. confusus Tremblay and Eady. (30) L. fabarum (Marshall). (31) L. testaceipes
(Cresson).

6 (5Ј). Anterolateral area of petiole costate (Fig.
14) . . . . . . . Aphidius colemani Viereck
6Ј. Anterolateral area of petiole costulate (Fig.
16) . . . . . . Aphidius matricariae Haliday
7 (4Ј). Forewing stigma wide triangular; 1.25
times as long as R1 vein (Fig. 12). Petiole
narrow triangular (Fig. 22). Labial pal-
pus with two palpomeres (Fig. 2). . . .
. . . . . Lysiphlebus testaceipes (Cresson)
7Ј. Forewing stigma elongate triangular, as
long as or slightly shorter than R1 vein
(Figs. 11 and 12). Petiole wide triangular
(Figs. 20 and 21). Labial palpus with one
palpomere (Fig. 1) . . . . . . . . . . . . . 8
8 (7Ј). Setae on fringe of forewing longer than
those on surface (Fig. 10). . . . . . . . .
. . . . Lysiphlebus confusus Tremblay and
Eady
8Ј. Setae on fringe of forewing similar to those
on surface (Fig. 11). . . . . . . . . . . . .
. . . . . . Lysiphlebus fabarum (Marshall)
9 (3Ј). Hypopygium without prongs (Fig. 28).
Forewing stigma extends longer than tip
of r and RS vein (Fig. 9). Petiole with
spiracular tubercles only (Fig. 19) . . .
. . . . . . . . . . . Lipolexis gracilis Fo¨rster
9Ј. Hypopygiumwithtwoprongs(Figs.26and
27). Forewing stigma extends not longer
than tip of r and RS vein (Figs. 6 and 7).
Petiole with spiracular and secondary
tubercles (Figs. 17 and 18) . . . . . . . 10
10 (9Ј). Distance between spiracular and second-
ary tubercles shorter than width at spir-
acles (Fig. 17). Ovipositor sheath sub-
quadrangular at base (Fig. 26) . . . . . .
. . . . . . Binodoxys acalephae (Marshall)
10Ј. Distance between spiracular and second-
ary tubercles longer than width at spir-
acles (Fig. 18). Ovipositor sheath
rounded at base (Fig. 27) . . . . . . . . .
. . . . . . . Binodoxys angelicae (Haliday)
Acknowledgments
The research was supported by the grants AVOZ50070508
(Institute of Entomology, Academy of Sciences of the Czech
Republic), III43001 (The Ministry of Education and Science
of the Republic of Serbia), 89-9198 (University of Zabol,
Iran) and by the program “Aphid parasitoids (Hymenoptera:
Braconidae: Aphidiinae): diversity of trophic associations
and their role in agroecosystems” (General Secretariat for
Research and Technology, Ministry of Development of the
Hellenic Republic).
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Received 16 June 2011; accepted 16 January 2012.

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