ORIGINAL ARTICLE

X. Pons Æ B. Lumbierres Æ P. Stary

Expansion of the aphid Myzocallis (Lineomyzocallis) walshii (Monell)on the red oak Quercus rubra, and adaptation of local parasitoidsin the northeastern Iberian Peninsula (Hom., Aphididae, Calaphidinae;Hym., Braconidae, Aphidiinae)

Received: 20 January 2005 / Published online: 31 May 2005� Springer-Verlag 2005

Abstract An ongoing expansion of Myzocallis (L.)walshii (Monell) in the NE Iberian Peninsula was de-tected. The aphid species was recorded in Catalonia,Andorra and Navarra. Adaptation of local native par-asitoids (at least Trioxys pallidus Haliday and T. tenui-caudus Stary) to the new immigrant was documented,together with background information on their hostrange in the native environments. The detection ofparasitoids ofM. walshii is the first published evidence inEurope. The new evidence for M. walshii in the NEIberian Peninsula also supports the warning of theexpansion of the aphid as a pest of Quercus rubra overEurope.

Keywords Aphids Æ Myzocallis walshii Æ Parasitoids ÆQuercus sp. Æ Trioxys pallidus Æ Trioxys tenuicaudus

Introduction

Myzocallis (Lineomyzocallis) walshii (Monell) (Aphid-idae, Calaphidinae, Panaphidini) is native to easternNorth America, where it is generally not considered tobe a pest (L. E. Ehler, personal communication). Itsmain host is the northern red oak Quercus rubra, whichis also of North American origin but has been plantedfor a long time as an originally introduced species inmany parts of Europe. The aphid was detected for thefirst time in Europe on Q. rubra in France in 1988 and

it was predicted that it would expand to other prov-inces of France as well as to other European countries(Remaudiere 1989). This prediction was first verifiedwhen the aphid was found in other provinces of Franceand in Switzerland (Remaudiere and Quednau 1992).Patti and Lozzia (1994) and Barbagallo et al. (1995)observed the aphid in Italy. Mier Durante and NietoNafrıa (1995) reported its presence in northwesternSpain. Nieto Nafrıa et al. (1999) in Belgium, Thiemeand Eggers-Schumacher (2004) in Germany, Ripka(2004) in Hungary and Havelka et al. (unpublished) inthe Czech Republic also reported the presence of theaphid in their respective countries. There is also anunpublished record of M. walshii in Andorra (MierDurante and Nieto Nafrıa, personal communication).Quercus rubra is cultivated for the wood industry in thenorth of the Iberian Peninsula but is also common asan ornamental (Lopez Lillo and Sanchez de LorenzoCaceres 1999).

The present account presents new information aboutthe occurrence of the aphid and its associated parasi-toids in the NE Iberian Peninsula. It contributes to theknowledge of local fauna, and adaptations of localparasitoid species to the new exotic aphid immigrants,and to the exploration of biocontrol agents that arepotentially useful in other areas.

Materials and methods

The research was conducted within a framework of ageneral study on aphids, their parasitoids and theirpredators living on different tree species in urban envi-ronments in the NE Iberian Peninsula.

In 2004, a noticeable infestation of aphids, pre-sumably M. walshii, was recorded on Q. rubra plantedas an ornamental tree in avenues in the town of Girona(Catalonia, SE of the Pyrenees). This infestation pro-duced aesthetic damage to the trees and disturbance tothe public due to the honeydew excretion. Afterdetecting the possible future problem of M. walshii in

X. Pons (&) Æ B. LumbierresCentre UdL-IRTA, Universitat de Lleida, Rovira Roure 191,25198 Lleida, SpainE-mail: xavier.pons@irta.es

P. StaryAcademy of Sciences of the Czech Republic,Institute of Entomology, Branisovska 31,37006 Ceske Budejovice, Czech Republic

J Pest Sci (2006) 79: 17–21DOI 10.1007/s10340-005-0105-6

the region, the survey of aphids on Q. rubra was ex-tended to other urban environments and forest standswhere the tree was planted. A public park in Andorrala Vella (Andorra) and another one in Zarautz-Aya(the Basque Country) were sampled. Northern red oakforest stands were also sampled in Catalonia, Navarraand the Basque Country. Samples were taken in springat all sites and in autumn in Girona, where the abun-dance of aphids on Q. rubra was high. Other oak treespresent in these places were also sampled. This surveywas made in order to bring as much information aboutthe associated aphid species, including M. walshii, andthe potential parasitoids of this new exotic aphid.

Leaves with aphid colonies of northern red oaks andother oak species present in the sampled urban envi-ronments or forest stands were cut with scissors andgently transferred into 250 cc translucent plastic cagescovered with nylon mesh as a ceiling and maintained at20–25�C in the laboratory. Simultaneously, some of theaphids were preserved in 70% ethanol for later identi-fication. Parasitoid rearing cages were inspected twice aweek and parasitoids emerging were collected and pre-served in 70% ethanol until identification. After8 weeks, the cages were eliminated.

The results on the tritrophic associations of Q. rubra,M. walshii and parasitoid species were merged with therecords of the Iberian Peninsula and the nearby areas ofFrance related to the parasitoids associated with theaphid oak species or other arboreal aphid species of thesubfamily Calaphidinae and tribe Panaphidini, to whichM. walshii belongs (Remaudiere and Remaudiere 1997;Nieto Nafrıa et al. 1997; Quednau 1999, 2003). The aimis to provide broader information on the host range ofthe parasitoids that may illustrate some reasons foraccepting M. walshii as a new host in the area.

Vouchers of the aphid species found and their asso-ciated parasitoids are in the Entomology laboratory ofthe University of Lleida (Lleida, Catalonia, Spain) andin Stary’s collection at Ceske Budejovice. Specimens of

M. walshii are also conserved at the Department ofAnimal Biology of the University of Leon (Spain).

Results

Presence of M. walshii and its associated parasitoidsin the NE Iberian Peninsula

Table 1 shows the aphid species associated withQ. rubra and the tritrophic associations betweenQ. rubra, M. walshii and parasitoids in the NE IberianPeninsula. M. walshii was recorded in Catalonia (Gi-rona) and Andorra (Andorra la Vella) on the orna-mental trees planted in avenues or public gardens inurban environments and in the in forest stands innorthern Navarra (Ituren and Santesteban). However,the aphid was not found in the forest stands in Cata-lonia (Vilanova de Sau and Sant Hilari de Sacalm) andin the Basque Country (Oiartzun). Whereas low den-sities of the aphid were recorded in the forest stands, inthe urban environments high densities were recordedand the trees suffered honeydew damage.

Although the target M. walshii was the main aphidspecies found on Q. rubra, other aphid species were alsorecorded: Myzocallis (Agrioaphis) castanicola Baker,Thelaxes suberi (Del Guercio) and Thelaxes dryophila(Schrank), Lachnus sp. and Phylloxera sp. However, noM. walshii was found on other Quercus sp. present at thesampled sites (Table 1).

The parasitoid species associated with M. walshiiwere Trioxys pallidus Haliday and Trioxys tenuicaudusStary (Table 1). The former species was found in anurban environment (Girona, Catalonia) in spring andautumn. Many hyperparasites, mainly chalcids andCharipinae cynipids, emerged from mummies ofM. walshii in Girona, especially at the end of the season.Trioxys tenuicaudus was found in a forest stand(Santesteban, Navarra).

Table 1 Records of M. walshii and other aphid species on Q. rubra and associated parasitoids in the northern Iberian Peninsula in 2004

Date Region Locality Habitat Aphid species Parasitoid species

2 June Catalonia Vilanova de Sau Forest M. (A.) castanicola –Thelaxes sp. –

14 June Navarra Ituren Forest M. (L.) walshii –14 June Navarra Santesteban 1 Forest M. walshii –

M. castanicola –Thelaxes dryophila Adialytus thelaxis

14 June Navarra Santesteban 2 Forest M. walshii –14 June Navarra Santesteban 3 Forest M. walshii Trioxys tenuicaudus15 June Basc Country Oiartzun 1 Forest Thelaxes sp. –15 June Basc Country Oiartzun 2 Forest Phylloxera sp. –30 June Catalonia Girona Urban M. walshii Trioxys pallidus

Thelaxes suberi –7 July Andorra Andorra la Vella Urban M. walshii –25 October Catalonia Girona Urban M. walshii Trioxys pallidus4 November Catalonia Girona Urban M. walshii Trioxys pallidus

Lachnus sp. –

Numbers after one locality mean different stands sampled in that locality

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Review of other tritrophic associations between Quercussp., aphid species and parasitoids

Table 2 shows background information on the aphidsand parasitoids associated with oaks in Spain andnearby France. Associations of parasitoid species withCalaphidinae—Panaphidini arboreal aphids in the re-gion are also included in order to illustrate parasitoidspecies that may potentially accept M. walshii as a host.

Discussion

The detection of M. walshii in Catalonia (in Girona, in acoastal-premountain area southeast of the Pyrenees),Navarra (in a mountain area in the extreme west of thePyrenees) and Andorra (a country in the middle of thePyrenees) documents further sites that show the expan-sion of the aphid over the northeast of the IberianPeninsula, and agrees with the earlier prediction by

Remaudiere (1989) that this exotic aphid would expandall over Europe.

Our results, together with the previous evidence ofthe occurrence of M. walshii in the northwest of theIberian Peninsula, which includes two sites in Galicia(Mier Durante and Nieto Nafrıa 1995; Nieto Nafrıa andMier Durante, unpublished), supports the opinion thatthe aphid has a discontinuous distribution in the IberianPeninsula, as stated by Mier Durante and Nieto Nafrıa(1995). The specificity of M. walshii with Quercus rubrais an apparent reason for the capability of the aphid toexpand over far distant areas and to detect/establish onthe target host species. The northern red oak isincreasingly planted as an ornamental tree in urbanareas in southern Europe and M. walshii may become apotential problem in these environments. Apart from thepresumed long-distance transport of alate aphids by air-streams, the movement of infested plants from nurseriesto cities may also contribute to the expansion of theaphid.

Table 2 Association between Quercus sp., aphid and parasitoid species and other Calaphidinae-Panaphidini and Thelaxinae arborealaphids in Spain and France

Parasitoid species Aphid species Tree species Locality Reference

Adialytus thelaxis(Stary)

Thelaxes suberi(Del Guercio)

Q. ilex Lleida Lumbierres et al. (2005)

Thelaxes sp. Q. pyrenaica Navarra Authors (unpublished)Aphidius sp. Eucallipterus tiliae (Linnaeus) Tilia sp. Lleida Lumbierres et al. (2005)Lysiphlebus testaceipes(Cresson)

Tuberculatus(Tuberculoides)eggleri Borner

Q. ilex Lleida Lumbierres et al. (2005)

Sarucallis kahawaluokalani(Kirkaldy)

Lagerstroemia indica Lleida Lumbierres et al. (2005)

Praon sp. T. suberi Q. ilex Lleida Lumbierres et al. (2005)Hoplocallis picta (Ferrari) Q. ilex Lleida Lumbierres et al. (2005)

Trioxys curvicaudusMackauer

E. tiliae Tilia sp. Lleida Lumbierres et al. (2005)France Stary et al. (1977)Spain Stary and Remaudiere (1973)

Tizado and Nunez (1991)Tuberculatus (Tuberculoides)remaudierei (Nieto Nafrıa)

Q. pirenaica Spain Tizado and Nunez (1992)

H. picta Q. ilex Lleida Lumbierres et al. (2005)Trioxys pallidus(Hal.)

Chromaphis juglandicola(Kaltenbach)

Juglans regia Spain Gonzalez and Michelena (1987)Sanchis et al. (1995)

H. picta Q. ilex Lleida Lumbierres et al. (2005)Spain Tizado and Nunez (2001)

Q. faginea Lleida Authors (unpublished)Q. suber France Stary et al. (1973)Quercus sp Tarragona Authors (unpublished)

Myzocallis (M.) carpini Koch Carpinus sp. France Stary et al. (1973)Q. ilex France Stary et al. (1973)

Myzocallis (A.) castanicola Baker Q. suber France Stary et al. (1971)Myzocallis sp. Q. faginea Spain Gonzalez and Michelena (1987)Tinocallis (Sapocallis) saltans(Nevsky)

Ulmus minor Lleida Lumbierres et al. (2005)Ulmus sp. Lleida Authors (unpublished)

T. suberi Q. ilex Lleida Authors (unpublished)Tuberculatus (Tuberculoides)annulatus (Hartig)

Q. pedunculata France Stary et al. (1971)

T. eggleri Q. ilex Lleida Authors (unpublished)Tuberculatus sp. Quercus sp . Spain Sanchis et al (1995)

Michelena and Oltra (1987)Trioxys tenuicaudus Stary Myzocallis (M.) coryli (Goeze) Corylus avellana Spain Tizado and Nunez (1991)Trioxys sp E. tiliae Tilia sp. Lleida Lumbierres et al. (2005)

Aphid nomenclature according to Remaudiere and Remaudiere (1997), Nieto et al. (1997) and Quednau (1999, 2003)

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The case of M. walshii – Q. rubra represents a situa-tion in which an aphid native in North America acci-dentally spread to Q. rubra in Europe, where the latterwas originally introduced and became established as a‘‘native’’ tree in many areas. Besides M. walshii, there isalso an earlier adaptation to Q. rubra of a native aphid,Myzocallis castanicola, which is common on local oakspecies in Europe (Blackman and Eastop 1994; NietoNafrıa and Mier Durante 1998; Remaudiere, in a letter2004), as is also shown by our finding in Catalonia andNavarra. Something similar occurs with the Thelaxes sp.(T. dryophila and T. suberi), which were found onQ. rubra in Catalonia, Navarra and the Basque Countryin the present study. These two species have a Medi-terranean distribution and are established in the NEIberian Peninsula (Nieto Nafrıa and Mier Durante 1988;Lumbierres et al. 2005) on several species of Quercus sp.

No parasitoids of M. walshii have been previously re-corded in Europe. Therefore, our finding of Trioxys pal-lidus and T. tenuicaudus parasiting M. walshii is the firstreport in this continent. Trioxys pallidus is a quite com-mon species in the urban environments in Catalonia andin other regions of Spain and France. It has been recordedparasitising several species of Panaphidini (see Table 2for references). However, T. tenuicaudus is a less commonspecies. It has been previously recorded in the west of theIberian Peninsula (Tizado and Nunez 1991) parasitisingMyzocallis coryli on hazelnut trees, and has now beenfound in Navarra parasitising M. walshii (Table 1).

The original information obtained is an example ofadaptation of a native local parasitoid spectrum to anew exotic Panaphidini aphid immigrant: the parasitoidsshow an oligophagous host range that also includes thegenus Myzocallis. Myzocallis walshii is a congenericspecies (of another subgenus of the native Myzocallisspecies like M. castanicola) and the parasitoids cover thepotential host as a new host in the area of expansion.Also, in terms of biological control theory, the parasit-oid species that have newly adapted to M. walshii in itsnew area of expansion (the Iberian Peninsula) might alsobe potentially useful as biocontrol agents in other areas.This corroborates with the theory of local faunisticcomplexes of parasitoids and their adaptation to newexotic immigrants (Stary 1968, 1970).

The results achieved for M. walshii and its parasitoidsin the Iberian Peninsula are still tentative, and othernative species of parasitoids such as Trioxys curvicaudus[quite common parasitising Hoplocallis picta (Ferrari)on native oaks and Eucallipterus tiliae (Linnaeus) onlime trees] may be found associated with M. walshii inthe future.

The results are a partial study of local significance butthey should be implemented to a broader study on M.walshii and its distribution, ecology and parasitoidadaptations in Europe. Places in southern Europe whereparasitoids of M. walshii are well established would bepotential sources for parasitoids to be exported to otherareas, such as California (USA), where the aphid hasbeen introduced from eastern North America and which

is currently a target for classical biological control (L. E.Ehler, personal communication).

Acknowledgments Georges Remaudiere (Entomology laboratory,Museum National d¢Histoire Naturelle, Paris) and Nicolas PerezHidalgo (Departamento de Biologıa Animal, University of Leon,Spain) kindly supplied comprehensive published and unpublishedinformation on M. walshii in Europe. Nicolas Perez Hidalgo alsoconfirmed the identification of the M. walshii specimens. Les Ehler(University of California Davis Department of Entomology) gaveus information about M. walshii in California and Alvaro Aunos(Departament de Produccio Vegetal i Ciencia Forestal, Universityof Lleida) about Q. rubra forest stands in the Iberian Peninsula.Thanks are also due Emili Garolera (Catalonia), Carmen Traverand Gabriel Fuentes (Navarra) and Francisco Garın (the BasqueCountry) for his help in locating and sampling forest stands. Theresearch was partially funded by Lleida City Council (ProjecteUdL-IRTA-Ajuntament de Lleida no. 0504-14061). Petr Stary wasfunded by Grant S5007102 (Grant Agency of the Academy ofSciences of the Czech Republic) and by the Entomology InstituteProject Z5007907 (Academy of Sciences of the Czech Republic).

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