1. ORIGINAL ARTICLE
X. Pons ร B. Lumbierres ร P. Staryยด
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
ร 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 Staryยด ) 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 ๏ฌrst 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 ร Myzocallis walshii ร Parasitoids ร
Quercus sp. ร Trioxys pallidus ร 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
๏ฌrst 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 ๏ฌrst veri๏ฌed
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
Nafrฤฑยดa (1995) reported its presence in northwestern
Spain. Nieto Nafrฤฑยดa 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 (unpublished) in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unpublished record of M. walshii in Andorra (Mier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 Nafrฤฑยดa, personal communication).
Quercus rubra is cultivated for the wood industry in the
north of the Iberian Peninsula but is also common as
an ornamental (Loยด pez Lillo and Saยด nchez de Lorenzo
Caยด 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 di๏ฌerent 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 (&) ร B. Lumbierres
Centre UdL-IRTA, Universitat de Lleida, Rovira Roure 191,
25198 Lleida, Spain
E-mail: xavier.pons@irta.es
P. Staryยด
Academy of Sciences of the Czech Republic,
Institute of Entomology, Branisห ovskaยด 31,
37006 Cห eskeยด Budeห jovice, Czech Republic
J Pest Sci (2006) 79: 17โ21
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
20โ25ยฐC in the laboratory. Simultaneously, some of the
aphids were preserved in 70% ethanol for later identi-
๏ฌcation. Parasitoid rearing cages were inspected twice a
week and parasitoids emerging were collected and pre-
served in 70% ethanol until identi๏ฌcation. 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 Nafrฤฑยดa 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 Staryยด โs collection at Cห eskeยด Budeห jovice. Specimens of
M. walshii are also conserved at the Department of
Animal Biology of the University of Leoยด 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 su๏ฌered 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
Staryยด (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 โ
Thelaxes sp. โ
14 June Navarra Ituren Forest M. (L.) walshii โ
14 June Navarra Santesteban 1 Forest M. walshii โ
M. castanicola โ
Thelaxes dryophila Adialytus thelaxis
14 June Navarra Santesteban 2 Forest M. walshii โ
14 June Navarra Santesteban 3 Forest M. walshii Trioxys tenuicaudus
15 June Basc Country Oiartzun 1 Forest Thelaxes sp. โ
15 June Basc Country Oiartzun 2 Forest Phylloxera sp. โ
30 June Catalonia Girona Urban M. walshii Trioxys pallidus
Thelaxes suberi โ
7 July Andorra Andorra la Vella Urban M. walshii โ
25 October Catalonia Girona Urban M. walshii Trioxys pallidus
4 November Catalonia Girona Urban M. walshii Trioxys pallidus
Lachnus sp. โ
Numbers after one locality mean di๏ฌerent 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
CalaphidinaeโPanaphidini 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 Nafrฤฑยดa 1995; Nieto Nafrฤฑยดa 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 Nafrฤฑยดa
(1995). The speci๏ฌcity 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
(Staryยด )
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 Boยจ 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 Staryยด et al. (1977)
Spain Staryยด and Remaudie` re (1973)
Tizado and Nuยด nห ez (1991)
Tuberculatus (Tuberculoides)
remaudierei (Nieto Nafrฤฑยดa)
Q. pirenaica Spain Tizado and Nuยด nห ez (1992)
H. picta Q. ilex Lleida Lumbierres et al. (2005)
Trioxys pallidus
(Hal.)
Chromaphis juglandicola
(Kaltenbach)
Juglans regia Spain Gonzaยด lez and Michelena (1987)
Sanchis et al. (1995)
H. picta Q. ilex Lleida Lumbierres et al. (2005)
Spain Tizado and Nuยด nห ez (2001)
Q. faginea Lleida Authors (unpublished)
Q. suber France Staryยด et al. (1973)
Quercus sp Tarragona Authors (unpublished)
Myzocallis (M.) carpini Koch Carpinus sp. France Staryยด et al. (1973)
Q. ilex France Staryยด et al. (1973)
Myzocallis (A.) castanicola Baker Q. suber France Staryยด et al. (1971)
Myzocallis sp. Q. faginea Spain Gonzaยด 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 Staryยด 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 Staryยด Myzocallis (M.) coryli (Goeze) Corylus avellana Spain Tizado and Nuยด nห 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 โ 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
โโnativeโโ 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
Nafrฤฑยดa and Mier Durante 1998; Remaudie` re, in a letter
2004), as is also shown by our ๏ฌnding 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 Nafrฤฑยดa 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 ๏ฌnding of Trioxys pal-
lidus and T. tenuicaudus parasiting M. walshii is the ๏ฌrst
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 Nuยด nห 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 (Staryยด 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 signi๏ฌcance 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,
Museยด um National dยขHistoire Naturelle, Paris) and Nicolaยด s Peยด rez
Hidalgo (Departamento de Biologฤฑยดa Animal, University of Leoยด n,
Spain) kindly supplied comprehensive published and unpublished
information on M. walshii in Europe. Nicolaยด s Peยด rez Hidalgo also
con๏ฌrmed the identi๏ฌcation of the M. walshii specimens. Les Ehler
(University of California Davis Department of Entomology) gave
us information about M. walshii in California and Alvaro Aunoยด s
(Departament de Produccioยด 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 Garฤฑยดn (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 Staryยด 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).
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