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 ZELJKO TOMANOVIC,2 NICKOLAS G. KAVALLIERATOS,3 EHSAN RAKHSHANI,4

XAVIER PONS,5 ANDJELJKO PETROVIC,2 KEITH S. PIKE,6 AND PETR STARY1

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 ofAphis ruborum (Borner andSchilder)arepresented including theirdistribution.Theparasitoid spectrumofA. ruborum in theWestPalaearctic is rich, composed of Aphidius colemani Viereck, Aphidius matricariae Haliday, Binodoxysacalephae (Marshall), Binodoxys angelicae (Haliday), Ephedrus persicae Froggatt, Lipolexis gracilisForster,Lysiphlebus confususTremblayandEady,Lysiphlebus fabarum(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 (SouthAmerica), andL. testaceipes(SouthandNorthAmerica).Furthermore, the reservoir roleofA. ruborumin various ecosystems was investigated in Europe (France) and South America (Chile). Faunalpeculiarities and relationships of the parasitoid taxa are discussed together with a synopsis of theirpotential as biocontrol agents.

KEY WORDS Rubus spp., Aphis ruborum, parasitoid complex, key, reservoir

Aphis ruborum (Borner and Schilder) is a monoeciousholocyclic species associated with wild and cultivatedblackberries (Rubus spp.), and occasionally on straw-berries (Fragaria spp.) (Blackman and Eastop 2000,2006). It originally was described as Doralis ruborumfrom central Europe (Borner and Schilder 1931). A.ruborumalsohasbeenrecorded inAsia(Bodenheimer1937), Africa (Habib and El-Kady 1961), and SouthAmerica (Blackman and Eastop 1984). In 2009 it wasdetected for the Þrst time in North America in Wash-ington State (K.S.P., unpublished data).

Aphid parasitoids are a useful group for the researchon parasitoid reservoirs and respective environmentalrelationships. The concept of foci of aphid parasitoids innature originally was introduced by Stary (1964), and isnowcommonlyreferredtoasreservoirsor refugia(Stary1970, 1986; Stary and Pike 1998; Kavallieratos et al. 2002,2008). Various studies have been published on tritrophicassociations in crop and noncrop communities, and clas-

siÞcation of parasitoid reservoirs in agroecosystems(Volkl and Stary 1988; Pike et al. 1997; Stary and Havelka2008; Tomanovic et al. 2008, 2009).

It is the aim of the present contribution to summarizeinformation on the parasitoids ofA. ruborum as an aid tofuture taxonomic, biological, and biodiversity research,and to characterize the role ofA. ruborum in France andChile as a host reservoir of aphidiine parasitoids.

Materials and Methods

Specimens used in the current study were obtained inthe course of Þeld studies by the authors from numerouscountries (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; BelgradeNatural History Museum, Serbia; Benaki Phytopatholog-ical Institute, Greece; University of Zabol, Iran; Univer-sity of Lleida, Spain; and Washington State University,United States. Relevant material also was examined fromGeorgia by P. Stary. The most intensive sampling of A.ruborumonRubus spp., consisting of both live and mum-miÞed aphids, was undertaken in France (i.e., Montpel-lier: gardens, parks; Antibes, Opio, Valbonne: gardens,maqui forests, gardens; Corse: maqui forests, wasteplaces) and Chile (i.e., Chillan, Concon, La Cruz, LosAndes, Rinconada, Villa Alemana: gardens, parks; Col-lipulli, Niquen, San Carlos, Santa Rosa, Parral, Pinto,Talca: hedges, roadsides) from 1974 to 1986 and 1991Ð1992, respectively.

1 Laboratory of Aphidology, Institute of Entomology, Biology Cen-tre, Academy of Sciences of the Czech Republic, Branisovska 31,37005 Ceske Budejovice, 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: [email protected]).

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 andExtension 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 ofaphids from infested plants cut in the Þeld and placedin plastic cages (size 250 ml) covered with nylon mesh.At the lab samples were subdivided, with part used toobtain voucher aphids for identiÞcation, and part heldfor rearing of parasitoids. Voucher aphids were pre-served in a solution of 90% ethanol and 75% lactic acidat a ratio of 2:1 (Eastop and van Emden 1972). Cagedsamples were held at 22�C until parasitoid emergence;emerged parasitoids were preserved in ethanol.

In cases where original parasitoid material was notexamined, the review is based on literature recordsand marked as “Material not examined”. New materialwas obtained from Czech Republic, Montenegro, andthe United States by the authors. In those cases thereport is followed by the indication “New host record”.

Parasitoid adults were point- and usually slide-mounted for detailed examination. Specimens for slideswere washed in distilled water, boiled in 10% KOH forabout 2 min, rewashed, then placed in a drop of Faure-Berlese medium (Krantz 1978) for dissection or wholemounting. The morphological terminology used in thepaper 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 etal. 2001), Pakistan (Stary et al. 1998).

Aphidius sp.

Turkey (Aslan et al. 2004).

Binodoxys acalephae (Marshall, 1896)

France (Stary et al. 1973), Greece (Kavallieratos etal. 2001), Italy (Stary 1966), Spain (Pons and Stary2003), Turkey (Duzgunes et al. 1982) (Material notexamined).

Binodoxys angelicae (Haliday, 1833)

France (Stary et al. 1975), Greece (Kavallieratos etal. 2001), Italy (Stary 1966), Spain (Pons and Stary2003), Turkey (Duzgunes et al. 1982) (Material notexamined).

Ephedrus persicae Froggatt, 1904

Israel (Mackauer 1959) (Material not examined),Spain (Stary et al. 2004), Turkey (Duzgunes et al.1982) (Material not examined).

Lipolexis gracilis Forster, 1862

Italy (Stary 1966), Spain (Michelena Saval and OltraMoscardo 1987) (Material not examined).

Lysiphlebus confusus Tremblay and Eady, 1978

France (Stary et al. 1971), Greece (Kavallieratos etal. 2001), Israel (Mackauer 1960) (Material not exam-ined), Italy (Stary 1966), Montenegro (New host re-cord), Portugal (Cecõlio 1995) (Material not exam-ined), Spain (Stary et al. 2004), Turkey (Duzgunes etal. 1982) (Material not examined).

Lysiphlebus fabarum (Marshall, 1896)

Czech Republic (New host record), France (Staryet 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 andStary 2003), Turkey (Duzgunes et al. 1982) (Materialnot examined), United Kingdom (Muller 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 (Cecõlio1994) (Material not examined), Spain (Pons and Stary2003), 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

Parasitoid faunal complexes associated withA. 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 (EastMediterranean); and 5) L. testaceipes (Nearctic)(Stary 1970, Kavallieratos et al. 2004). In the westernPalaearctic, the complex is almost the same through-out. One difference is the apparent absence of A.colemani in west Mediterranean Europe; its nativehome 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 ofA. ruborum isL. testaceipes,which probably hasits origin in North America but also occurs now inCentral and South America (Zamora Mejõas et al.2010). The aphid (A. ruborum) is considered a newaccidental 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 nativeand introduced parasitoid species. Tizado et al. (1992)classiÞed the wild reservoirs of aphidiines attackingaphids of the genusAphiswith agricultural importancein the Leon 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 andnoncrop situations, and studied directly the role ofRubus ulmifolius Schott infested with A. ruborum as areservoir for aphid parasitoids and its impact to parasiticbiocontrol of Aphis gossypii Glover in nearby cotton(Gossypium sp.).L. fabarumwas thedominate species ina complex of parasitoids that led to almost 100% parasit-ismofA.gossypii. Inthis setting,R.ulmifoliuswasahighlyuseful reservoir for parasitoids with cross-over capabilityto cotton aphid. Tomanovic et al. (2009) also discussedthe 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 populationbuildup of economically important parasitoids [e.g., A.colemani, A. ervi, L. fabarum, L. testaceipes, and Praonvolucre (Haliday)], and tritrophic relationships in agro-ecosystem-dominated landscapes.

In Portugal, Cecõlio (1994) emphasized the positiverole of A. ruborum as a frequent host or host reservoirfor L. testaceipes in forests, Þelds, and roadsides, andfound that parasitism rates generally were high.

In Spain, Pons and Stary (2003) investigated theassociation of the introduced exotic parasitoid L. tes-taceipes on R. padi in wheat and A. ruborum in Rubussp. (noncrop Þeld margins) relative to the parasitoidÕspopulation development and regional expansion inalfalfa (Medicago sativa L.), wheat, and maize (ZeamaysL.) in the Iberian Peninsula.A. ruborumwas foundtobeausefulhost forL. testaceipes,andadeÞnitivefactorto the parasitoidÕs value as a promising biological control

Fig. 4–13. Forewing of Aphidius, Binodoxys, Ephedrus, Lipolexis, Lysiphlebus, and Praon species (females). (4) A.matricariaeHaliday. (5) A. erviHaliday. (6) B. acalephae (Marshall). (7) B. angelicae (Haliday). (8) E. persicae Froggatt. (9)L. gracilis Forster. (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 reportedto have low effect on pest species. The contributing roleand key association of A. ruborum-Rubus in the expan-sion of L. testaceipes in the Iberian Peninsula (coastalareas to inland mountainous areas) is treated in detail byPons 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 theexotic L. testaceipes almost immediately after its in-troduction and establishment in MediterraneanFrance (Stary et al. 1988a,b). Its quick establishmentin France, likely contributed to its further expansionin the region. A recent example of the expansion is theparasitization of the invasive aphid, Aphis illinoisensisShimer, by L. testaceipes in Algeria (Laamari andCoeur dÕ Acier 2010; Havelka et al. 2011).

In North America, only one local parasitoid, L. testa-ceipes,has adapted successfully toA. ruborum.This para-sitoid is an important agent for natural biological controlof many economically important aphids, includingAphiscraccicoraKoch,Aphis fabae, Aphis pomiDe Geer,Aphisspiraecola 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.), Rhopalosiphummaidis (Fitch), Schizaphis graminum (Rondani), Sito-bion avenae (F.) (Pike et al. 2000).

Stary et al. (1993)reportedonA. ruborumasanexoticspecies in Chile, well-established in local ecosystems,detectable in a range of settings such as roadsides, wasteplaces,gardens,andingrovesalongirrigationditchesand

channels, which all simultaneously represent transzonalbiocorridors. It was demonstrated in Chile that A. rubo-rum is not a pest, but an important host reservoir of L.testaceipes.This same aphid is now in Argentina (DelÞnoet al. 2002), and although there is no Þeld data on asso-ciated parasitoids as yet, we presume similar aphidÐpara-sitoidrelationshipsaredevelopingas indicatedforneigh-boring Chile.

The European and Mediterranean Plant ProtectionOrganization (EPPO) in a recent decision, removed L.testaceipes from the EPPO “positive list” on grounds itmight displace native parasitoid species because of itswide host range, expanding geographic distribution, andits ability to adapt to and thrive in a range of environ-ments fromagro-ecosystemstoforests(EPPO2009).Weprincipally disagree with such an approach because ofhost range patterns and their predictability in new areas,but this discussion exceeds the topics of the presentedpaper.

Key to Female Aphidiines Attacking A. ruborum

1. Forewing with eight cells. (Fig. 8) . . . . .. . . . . . . . . . Ephedrus persicae Froggatt

1�. Forewing with �8 cells (Figs. 3Ð7,9Ð13) . . . . . . . . . . . . . . . . . . . . . . 2

2 (1�). Forewing RS � M vein present (Fig.13) . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . Praon abjectum (Haliday)

2�. Forewing RS � 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. erviHaliday (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 Forster. (20) L. confusus Tremblay andEady. (21) L. fabarum (Marshall). (22) L. testaceipes (Cresson).


3 (2�). Forewing M & m-cu vein complete (Figs.3Ð5) or incomplete (Figs. 10Ð12) . . . . 4

3�. Forewing M and m-cu vein absent andonly r & RS vein developed (Figs. 6 and7, 9) . . . . . . . . . . . . . . . . . . . . . . . 9

4 (3). Forewing M & m-cu complete throughout(Figs. 3Ð6). Ovipositor sheath truncatedat tip (Figs, 23Ð25) . . . . . . . . . . . . . . 5

4�. Forewing M & m-cu incomplete (Figs. 10Ð12). Ovipositor sheath sharply pointed attip (Figs. 29Ð31) . . . . . . . . . . . . . . . 7

5 (4). Anterolateral area of petiole rugose (Fig. 15).. . . . . . . . . . . . . . Aphidius ervi Haliday

5�. Anterolateral area of petiole costate (Fig.

14) or costulate (Fig. 16) . . . . . . . . . . 6

Fig. 23–30. (23Ð25) Lateral aspect of genitalia ofAphidius species (females). (23)A. colemaniViereck. (24)A.matricariaeHaliday. (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 Forster. (29) L. confusus Tremblay and Eady. (30) L. fabarum (Marshall). (31) L. testaceipes(Cresson).


6 (5�). Anterolateral area of petiole costate (Fig.14) . . . . . . . Aphidius colemani Viereck

6�. Anterolateral area of petiole costulate (Fig.16) . . . . . . Aphidius matricariae Haliday

7 (4�). Forewing stigma wide triangular; 1.25times as long as R1 vein (Fig. 12). Petiolenarrow triangular (Fig. 22). Labial pal-pus with two palpomeres (Fig. 2). . . .. . . . . Lysiphlebus testaceipes (Cresson)

7�. Forewing stigma elongate triangular, aslong as or slightly shorter than R1 vein(Figs. 11 and 12). Petiole wide triangular(Figs. 20 and 21). Labial palpus with onepalpomere (Fig. 1) . . . . . . . . . . . . . 8

8 (7�). Setae on fringe of forewing longer thanthose on surface (Fig. 10). . . . . . . . .. . . . Lysiphlebus confusus Tremblay and

Eady8�. Setae on fringe of forewing similar to those

on surface (Fig. 11). . . . . . . . . . . . .. . . . . . Lysiphlebus fabarum (Marshall)

9 (3�). Hypopygium without prongs (Fig. 28).Forewing stigma extends longer than tipof r and RS vein (Fig. 9). Petiole withspiracular tubercles only (Fig. 19) . . .. . . . . . . . . . . Lipolexis gracilis Forster

9�. Hypopygium with two prongs (Figs. 26 and27). Forewing stigma extends not longerthan tip of r and RS vein (Figs. 6 and 7).Petiole with spiracular and secondarytubercles (Figs. 17 and 18) . . . . . . . 10

10 (9�). 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)

10�. Distance between spiracular and second-ary tubercles longer than width at spir-acles (Fig. 18). Ovipositor sheathrounded at base (Fig. 27) . . . . . . . . .. . . . . . . Binodoxys angelicae (Haliday)

Acknowledgments

The research was supported by the grants AVOZ50070508(Institute of Entomology, Academy of Sciences of the CzechRepublic), III43001 (The Ministry of Education and Scienceof the Republic of Serbia), 89-9198 (University of Zabol,Iran) and by the program “Aphid parasitoids (Hymenoptera:Braconidae: Aphidiinae): diversity of trophic associationsand their role in agroecosystems” (General Secretariat forResearch and Technology, Ministry of Development of theHellenic Republic).

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Received 16 June 2011; accepted 16 January 2012.
