1. 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 parasitoids
in the northeastern Iberian Peninsula (Hom., Aphididae, Calaphidinae;
Hym., Braconidae, Aphidiinae)
Received: 20 January 2005 / Published online: 31 May 2005
Ó 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 host
range in the native environments. The detection of
parasitoids of M. walshii is the first published evidence in
Europe. The new evidence for M. walshii in the NE
Iberian Peninsula also supports the warning of the
expansion of the aphid as a pest of Quercus rubra over
Europe.
Keywords Aphids Æ Myzocallis walshii Æ Parasitoids Æ
Quercus sp. Æ Trioxys pallidus Æ Trioxys tenuicaudus
Introduction
Myzocallis (Lineomyzocallis) walshii (Monell) (Aphid-
idae, Calaphidinae, Panaphidini) is native to eastern
North America, where it is generally not considered to
be a pest (L. E. Ehler, personal communication). Its
main host is the northern red oak Quercus rubra, which
is also of North American origin but has been planted
for a long time as an originally introduced species in
many parts of Europe. The aphid was detected for the
first 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
(Remaudie` re 1989). This prediction was first verified
when the aphid was found in other provinces of France
and in Switzerland (Remaudie` re and Quednau 1992).
Patti and Lozzia (1994) and Barbagallo et al. (1995)
observed the aphid in Italy. Mier Durante and Nieto
Nafrı´a (1995) reported its presence in northwestern
Spain. Nieto Nafrı´a et al. (1999) in Belgium, Thieme
and Eggers-Schumacher (2004) in Germany, Ripka
(2004) in Hungary and Havelka et al. (unpublished) in
the Czech Republic also reported the presence of the
aphid in their respective countries. There is also an
unpublished record of M. walshii in Andorra (Mier
Durante and Nieto Nafrı´a, personal communication).
Quercus rubra is cultivated for the wood industry in the
north of the Iberian Peninsula but is also common as
an ornamental (Lo´ pez Lillo and Sa´ nchez de Lorenzo
Ca´ ceres 1999).
The present account presents new information about
the occurrence of the aphid and its associated parasi-
toids in the NE Iberian Peninsula. It contributes to the
knowledge of local fauna, and adaptations of local
parasitoid species to the new exotic aphid immigrants,
and to the exploration of biocontrol agents that are
potentially useful in other areas.
Materials and methods
The research was conducted within a framework of a
general study on aphids, their parasitoids and their
predators 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 planted
as 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 to
the public due to the honeydew excretion. After
detecting the possible future problem of M. walshii in
X. Pons (&) Æ B. Lumbierres
Centre UdL-IRTA, Universitat de Lleida, Rovira Roure 191,
25198 Lleida, Spain
E-mail: xavier.pons@irta.es
P. Stary´
Academy of Sciences of the Czech Republic,
Institute of Entomology, Branisˇ ovska´ 31,
37006 Cˇ eske´ Budeˇ jovice, Czech Republic
J Pest Sci (2006) 79: 17–21
DOI 10.1007/s10340-005-0105-6

2. the region, the survey of aphids on Q. rubra was ex-
tended to other urban environments and forest stands
where the tree was planted. A public park in Andorra
la Vella (Andorra) and another one in Zarautz-Aya
(the Basque Country) were sampled. Northern red oak
forest stands were also sampled in Catalonia, Navarra
and the Basque Country. Samples were taken in spring
at all sites and in autumn in Girona, where the abun-
dance of aphids on Q. rubra was high. Other oak trees
present in these places were also sampled. This survey
was made in order to bring as much information about
the associated aphid species, including M. walshii, and
the potential parasitoids of this new exotic aphid.
Leaves with aphid colonies of northern red oaks and
other oak species present in the sampled urban envi-
ronments or forest stands were cut with scissors and
gently transferred into 250 cc translucent plastic cages
covered with nylon mesh as a ceiling and maintained at
20–25°C in the laboratory. Simultaneously, some of the
aphids were preserved in 70% ethanol for later identi-
fication. Parasitoid rearing cages were inspected twice a
week and parasitoids emerging were collected and pre-
served in 70% ethanol until identification. After
8 weeks, the cages were eliminated.
The results on the tritrophic associations of Q. rubra,
M. walshii and parasitoid species were merged with the
records of the Iberian Peninsula and the nearby areas of
France related to the parasitoids associated with the
aphid oak species or other arboreal aphid species of the
subfamily Calaphidinae and tribe Panaphidini, to which
M. walshii belongs (Remaudie` re and Remaudie` re 1997;
Nieto Nafrı´a et al. 1997; Quednau 1999, 2003). The aim
is to provide broader information on the host range of
the parasitoids that may illustrate some reasons for
accepting 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 of
the University of Lleida (Lleida, Catalonia, Spain) and
in Stary´ ’s collection at Cˇ eske´ Budeˇ jovice. Specimens of
M. walshii are also conserved at the Department of
Animal Biology of the University of Leo´ n (Spain).
Results
Presence of M. walshii and its associated parasitoids
in the NE Iberian Peninsula
Table 1 shows the aphid species associated with
Q. rubra and the tritrophic associations between
Q. rubra, M. walshii and parasitoids in the NE Iberian
Peninsula. M. walshii was recorded in Catalonia (Gi-
rona) and Andorra (Andorra la Vella) on the orna-
mental trees planted in avenues or public gardens in
urban environments and in the in forest stands in
northern 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) and
in the Basque Country (Oiartzun). Whereas low den-
sities of the aphid were recorded in the forest stands, in
the urban environments high densities were recorded
and the trees suffered honeydew damage.
Although the target M. walshii was the main aphid
species found on Q. rubra, other aphid species were also
recorded: Myzocallis (Agrioaphis) castanicola Baker,
Thelaxes suberi (Del Guercio) and Thelaxes dryophila
(Schrank), Lachnus sp. and Phylloxera sp. However, no
M. walshii was found on other Quercus sp. present at the
sampled sites (Table 1).
The parasitoid species associated with M. walshii
were Trioxys pallidus Haliday and Trioxys tenuicaudus
Stary´ (Table 1). The former species was found in an
urban environment (Girona, Catalonia) in spring and
autumn. Many hyperparasites, mainly chalcids and
Charipinae cynipids, emerged from mummies of
M. 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 tenuicaudus
15 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 pallidus
4 November Catalonia Girona Urban M. walshii Trioxys pallidus
Lachnus sp. –
Numbers after one locality mean different stands sampled in that locality
18

3. Review of other tritrophic associations between Quercus
sp., aphid species and parasitoids
Table 2 shows background information on the aphids
and parasitoids associated with oaks in Spain and
nearby France. Associations of parasitoid species with
Calaphidinae—Panaphidini arboreal aphids in the re-
gion are also included in order to illustrate parasitoid
species that may potentially accept M. walshii as a host.
Discussion
The detection of M. walshii in Catalonia (in Girona, in a
coastal-premountain area southeast of the Pyrenees),
Navarra (in a mountain area in the extreme west of the
Pyrenees) and Andorra (a country in the middle of the
Pyrenees) documents further sites that show the expan-
sion of the aphid over the northeast of the Iberian
Peninsula, and agrees with the earlier prediction by
Remaudie` re (1989) that this exotic aphid would expand
all over Europe.
Our results, together with the previous evidence of
the occurrence of M. walshii in the northwest of the
Iberian Peninsula, which includes two sites in Galicia
(Mier Durante and Nieto Nafrı´a 1995; Nieto Nafrı´a and
Mier Durante, unpublished), supports the opinion that
the aphid has a discontinuous distribution in the Iberian
Peninsula, as stated by Mier Durante and Nieto Nafrı´a
(1995). The specificity of M. walshii with Quercus rubra
is an apparent reason for the capability of the aphid to
expand over far distant areas and to detect/establish on
the target host species. The northern red oak is
increasingly planted as an ornamental tree in urban
areas in southern Europe and M. walshii may become a
potential problem in these environments. Apart from the
presumed long-distance transport of alate aphids by air-
streams, the movement of infested plants from nurseries
to cities may also contribute to the expansion of the
aphid.
Table 2 Association between Quercus sp., aphid and parasitoid species and other Calaphidinae-Panaphidini and Thelaxinae arboreal
aphids 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 Bo¨ rner
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 curvicaudus
Mackauer
E. tiliae Tilia sp. Lleida Lumbierres et al. (2005)
France Stary´ et al. (1977)
Spain Stary´ and Remaudie` re (1973)
Tizado and Nu´ n˜ ez (1991)
Tuberculatus (Tuberculoides)
remaudierei (Nieto Nafrı´a)
Q. pirenaica Spain Tizado and Nu´ n˜ ez (1992)
H. picta Q. ilex Lleida Lumbierres et al. (2005)
Trioxys pallidus
(Hal.)
Chromaphis juglandicola
(Kaltenbach)
Juglans regia Spain Gonza´ lez and Michelena (1987)
Sanchis et al. (1995)
H. picta Q. ilex Lleida Lumbierres et al. (2005)
Spain Tizado and Nu´ n˜ ez (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 Gonza´ lez 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 Nu´ n˜ ez (1991)
Trioxys sp E. tiliae Tilia sp. Lleida Lumbierres et al. (2005)
Aphid nomenclature according to Remaudie` re and Remaudie` re (1997), Nieto et al. (1997) and Quednau (1999, 2003)
19

4. 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 latter
was originally introduced and became established as a
‘‘native’’ tree in many areas. Besides M. walshii, there is
also an earlier adaptation to Q. rubra of a native aphid,
Myzocallis castanicola, which is common on local oak
species in Europe (Blackman and Eastop 1994; Nieto
Nafrı´a and Mier Durante 1998; Remaudie` re, in a letter
2004), as is also shown by our finding in Catalonia and
Navarra. Something similar occurs with the Thelaxes sp.
(T. dryophila and T. suberi), which were found on
Q. rubra in Catalonia, Navarra and the Basque Country
in the present study. These two species have a Medi-
terranean distribution and are established in the NE
Iberian Peninsula (Nieto Nafrı´a 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 first
report in this continent. Trioxys pallidus is a quite com-
mon species in the urban environments in Catalonia and
in other regions of Spain and France. It has been recorded
parasitising several species of Panaphidini (see Table 2
for references). However, T. tenuicaudus is a less common
species. It has been previously recorded in the west of the
Iberian Peninsula (Tizado and Nu´ n˜ ez 1991) parasitising
Myzocallis coryli on hazelnut trees, and has now been
found in Navarra parasitising M. walshii (Table 1).
The original information obtained is an example of
adaptation of a native local parasitoid spectrum to a
new exotic Panaphidini aphid immigrant: the parasitoids
show an oligophagous host range that also includes the
genus Myzocallis. Myzocallis walshii is a congeneric
species (of another subgenus of the native Myzocallis
species like M. castanicola) and the parasitoids cover the
potential 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 its
new area of expansion (the Iberian Peninsula) might also
be potentially useful as biocontrol agents in other areas.
This corroborates with the theory of local faunistic
complexes of parasitoids and their adaptation to new
exotic immigrants (Stary´ 1968, 1970).
The results achieved for M. walshii and its parasitoids
in the Iberian Peninsula are still tentative, and other
native species of parasitoids such as Trioxys curvicaudus
[quite common parasitising Hoplocallis picta (Ferrari)
on native oaks and Eucallipterus tiliae (Linnaeus) on
lime trees] may be found associated with M. walshii in
the future.
The results are a partial study of local significance but
they should be implemented to a broader study on M.
walshii and its distribution, ecology and parasitoid
adaptations in Europe. Places in southern Europe where
parasitoids of M. walshii are well established would be
potential sources for parasitoids to be exported to other
areas, such as California (USA), where the aphid has
been introduced from eastern North America and which
is currently a target for classical biological control (L. E.
Ehler, personal communication).
Acknowledgments Georges Remaudie` re (Entomology laboratory,
Muse´ um National d¢Histoire Naturelle, Paris) and Nicola´ s Pe´ rez
Hidalgo (Departamento de Biologı´a Animal, University of Leo´ n,
Spain) kindly supplied comprehensive published and unpublished
information on M. walshii in Europe. Nicola´ s Pe´ rez Hidalgo also
confirmed the identification of the M. walshii specimens. Les Ehler
(University of California Davis Department of Entomology) gave
us information about M. walshii in California and Alvaro Auno´ s
(Departament de Produccio´ Vegetal i Cie` ncia Forestal, University
of Lleida) about Q. rubra forest stands in the Iberian Peninsula.
Thanks are also due Emili Garolera (Catalonia), Carmen Traver
and Gabriel Fuentes (Navarra) and Francisco Garı´n (the Basque
Country) for his help in locating and sampling forest stands. The
research was partially funded by Lleida City Council (Projecte
UdL-IRTA-Ajuntament de Lleida no. 0504-14061). Petr Stary´ was
funded by Grant S5007102 (Grant Agency of the Academy of
Sciences of the Czech Republic) and by the Entomology Institute
Project Z5007907 (Academy of Sciences of the Czech Republic).
References
Barbagallo S, Binazzi A, Bolchi-Serini G, Martelli M, Patti L
(1995) Aphidoidea. In: Mimeli A, Ruffo S, LaPorta S (eds)
Checklist delle specie della fauna di Italia. Fasc. 43. Calderoni,
Bologna, pp 13–38
Blackman RL, Eastop VF (1994) Aphids on the world’s trees. An
identification and information guide. CAB International, Wal-
lingford, pp 1010
Gonza´ lez P, Michelena JM (1987) Relaciones parasitoide-pulgo´ n
(Hym., Aphidiidae; Hom.Aphididae) en la provincia de Alic-
ante. Boln Asoc Esp Entomol 11:249–258
Lo´ pez Lillo A, Sa´ nchez de Lorenzo Ca´ ceres JM (1999) A´ rboles de
Espan˜ a. Manual de identificacio´ n. Ediciones Mundi-Prensa,
Madrid, pp 643
Lumbierres B, Pons X, Stary´ P (2005) Parasitoids and predators of
aphids associated with public green areas of Lleida (NE Iberian
Peninsula). Adv Hort Sci 19 (in press)
Michelena J, Oltra MT (1987) Contribucio´ n al conocimiento de los
Aphidiidae (Hym.) en Espan˜ a: II. Ge´ nero Ephedrus, Praon,
Adialytus, Lysiphlebus, Diaeretiella, Lipolexis, Trioxys. Boln
Asoc Esp Entomol 11:61–68
Mier Durante MP, Nieto Nafrı´a JM (1995) Species of the Spanish
aphid fauna with discontinuous geographical distribution.
J Aphidol 8:72–78
Nieto Nafrı´a JM, Mier Durante MP (1998) Hemiptera, Aphididae
I. Fauna Ibe´ rica vol 11. In: Ramos MA et al. (eds) Museo
Nacional de Ciencias Naturales. CSIC, Madrid, pp 424
Nieto Nafrı´a JM, Latteur G, Mier Durante MP, Tahon J, Pe´ rez
Hidalgo N, Nicolas J (1999) The aphids of Belgium (Hemiptera:
Aphididae). Parasitica (Gembloux) 55:5–38
Nieto Nafrı´a JM, Mier Durante MP, Remaudie` re G (1997) Les
noms des taxa du groupe-famille chez les aphididae (Hemip-
tera). Revue Franc¸ aise d’Entomologie (NS) 19:77–92
Patti I, Lozzia GC (1994) Presenza in Italia dell’Afide neartico della
Quercia rossa, Myzocallis (Lineomyzocallis) walshii (Mon.).
Boll Zool Agr Bachic 26:141–145
Quednau FW (1999) Atlas of the Drepanosiphine aphids of the
World. Part I: Panaphidini Oestlund, 1922—Myzocallidina
Bo¨ rner, 1942 (1930) (Hemiptera: Aphididae: Calaphidinae).
Contrib Am Entomol Inst 31:1–281
Quednau FW (2003) Atlas of the Drepanosiphine aphids of the
World. Part II: Panaphidini Oestlund, 1923—Panaphidina
Oestlund, 1923 (1930) (Hemiptera: Aphididae: Calaphidinae).
Mem Am Entomol Inst 72:1–301
Remaudie` re G (1989) De´ couverte en France de l¢espe` ce ame´ ricaine
Myzocallis (Lineomyzocallis) walshii (Monell) (Hom., Aphidi-
dae). Annls Soc Ent Fr (NS) 25:117
20

5. Remaudie` re G, Quednau FW (1992) Pucerons nouveaux et peu
connus du Mexique. 10e note: Le sous-genre Myzocallis (Li-
neomyzocallis) (Hom.: Aphididae). Annls Soc Ent Fr (NS)
28:27–36
Remaudie` re G, Remaudie` re M (1997) Catalogue des Aphididae du
monde. Homoptera Aphidoidea. INRA, Paris, pp 473
Ripka G (2004) Recent data to the knowledge of the aphid fauna of
Hungary (Homoptera: Aphidoidea). Acta Phytopathol Ento-
mol Hung 39:91–97
Sanchı´s A, Michelena JM, Nieves JL, Rey de Castillo C (1995)
Afidiı´nos (Hymenoptera: Braconidae: Aphidiinae) del centro
peninsular. Boln Asoc Esp Entomol 19:219–228
Stary´ P (1968) Geographic distribution and faunistic complexes of
parasites (Hym., Aphidiidae) in relation to biological control of
aphids (Hom., Aphidoidea). Acta Univ Carolinae, Biologica,
Prague 1967:23–89
Stary´ P (1970) Biology of aphid parasites (Hymenoptera: Aphi-
diidae) with respect to integrated control. Series entomologica
6. Dr. W. Junk N.V. Publishers, The Hague, pp 643
Stary´ P, Remaudie` re G (1973) Some aphid parasitoids (Hym.,
Aphidiidae) from Spain. Entomophaga 28:287–290
Stary´ P, Remaudie` re G, Leclant F (1971) Les Aphidiidae (Hym.) de
France et leurs hotes (Hom., Aphididae). Entomophaga Me´ m
Hors Se´ rie 5:1–72
Stary´ P, Remaudie` re G, Leclant F (1973) Nouvelles donne´ es sur les
Aphidiides de France (Hym.). Annls Soc Ent Fr (NS) 9:309–329
Stary´ P, Remaudie` re G, Leclant F (1977) Nouveaux comple´ ments
sur les Aphidiides (Hym.) de France et leurs hoˆ tes. Annls Soc
Ent Fr (NS) 13:165–184
Thieme T, Eggers-Schumacher HA (2004) Checklist of the Aphi-
dina of Germany. Entomofauna Germanica 6:167–193
Tizado EJ, Nu´ n˜ ez E (1991) Aportacio´ n al conocimiento en Espan˜ a
de los parasitoides de pulgones de la subfamilia Aphidiinae
(Hym. Braconidae). Bol San Veg Plagas 17:545–554
Tizado EJ, Nun˜ ez E (1992) Relaciones parasitoide-pulgo´ n (Hym.,
Braconidae: Aphidiinae) en la provincia de Leo´ n (Espan˜ a). Bol
Soc Portug Entomol (Suppl 3):401–410
21