BioRisk 4(2): 603-668 (2010) Apeer-rev ‘iewed open-access journa 1]

a Naaser eee BioRis

www.pensoftonline.net/biorisk

Lepidoptera
Chapter | |

Carlos Lopez-Vaamonde', David Agassiz”’, Sylvie Augustin', Jurate De Prins’,
Willy De Prins‘, Stanislav Gomboc’, Povilas Ivinskis®, Ole Karsholt’,
Athanasios Koutroumpas®, Fotini Koutroumpa’, Zdenék Lasttivka’,

Eduardo Marabuto"®, Elisenda Olivella'',; Lukasz Przybylowicz", Alain Roques',
Nils Ryrholm!'?, Hana Sefrova'*, Peter Sima'5, Ian Sims'¢, Sergey Sinev"”,
Bjarne Skulev'’, Rumen Tomov"’, Alberto Zilli#®, David Lees!”

| INRA UR633 Zoologie Forestiére, 2163 Av. Pomme de Pin, 45075 Orléans, France 2. Department of Ento-
mology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK 3 The Garden House, Stafford
Place, Weston-super-Mare, BS23 2QZ, UK 4 Entomology Section, Royal Museum for Central Africa, Leuven-
sesteenweg 13, B-3080 Tervuren, Belgium § Siskovo naselje 19, SI-4000 Kranj, Slovenia 6 Nature Research
Centre, Institute of Ecology, Akademijos str. 2, Lt 08412 Vilnius, Lithuania 1 The Natural History Museum of
Denmark, Zoologisk Museum, Universitetsparken 15, DK-2100 Kobenhavn 0, Denmark 8 National Agricul-
tural Research Foundation (NAGREF), Plant Protection Institute of Volos, PB 10303, Fytokou str, 38001 Volos,

Greece 9 Department of Zoology, Fisheries, Hydrobiology and Apidology, Faculty of Agronomy, Mendel University
in Brno, Zemédeélskd I, CZ-613 00 Brno, Czech Republic 10 CBA - Centro de Biologia Ambiental, Faculdade
Ciéncias Universidade de Lisboa, Campo Grande, edificio C2 - Lisboa, Portugal \\ Museu de Ciéncies Naturals
de Barcelona (Zoologia), Passeig Picasso s/n, E-O8003 Barcelona, Spain \2. Polish Academy of Sciences, Institute of
Systematics and Evolution of Animals, Slawkowska 17, 31-016 Krakow, Poland \3 Department of Natural Scien-
ces, University of Giavle, S-801 76 Gavle, Sweden \4 Department of Crop Science, Breeding and Plant Medicine,

Faculty of Agronomy, Mendel University in Brno, Zemédeélskd 1, CZ-613 00 Brno, Czech Republic 15 Koppert
Biological Systems, Komarnanskd cesta 13, 940 O1 Nové Zamky, Slovakia \6 Syngenta International Research
Centre, Jealott’s Hill, Bracknell, Berkshire RG42 6EY, UK \7 Zoological Institute RAS, Universitetskaya nab. 1,

199034 St.Petersburg, Russia \8 Brondsted 411, DK-3670 Vekso, Denmark \Y University of Forestry, 10 Kliment
Obridski blud., 1756 Sofia, Bulgaria 20 Museo Civico di Zoologia, Via U. Aldrovandi 18, I-00197 Rome, Italy

Corresponding author: Carlos Lopez-Vaamonde (carlos.lopez-vaamonde@orleans.inra.fr)

Academic editor: David Roy | Received 31 August 2009 | Accepted 24 May 2010 | Published 6 July 2010

Citation: Lopez-Vaamonde C et al. (2010) Lepidoptera. Chapter 11. In: Roques A et al. (Eds) Alien terrestrial arthropods
of Europe. BioRisk 4(2): 603-668. doi: 10.3897/biorisk.4.50

Abstract
We provide a comprehensive overview of those Lepidopteran invasions to Europe that result from increas-
ing globalisation and also review expansion of species within Europe. A total of 97 non-native Lepidoptera

species (about 1% of the known fauna), in 20 families and 11 superfamilies have established so far in

Copyright C. Lopez-Vaamonde et al. This is an open access article distributed under the terms of the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

604 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Europe, of which 30 alone are Pyraloidea. In addition, 88 European species in 25 families have expanded
their range within Europe and around 23% of these are of Mediterranean or Balkan origin, invading the
north and west. Although a number of these alien species have been in Europe for hundreds of years, 74%
have established during the 20" century and arrivals are accelerating, with an average of 1.9 alien Lepi-
doptera newly established per year between 2000-2007. For 78 aliens with a known area of origin, Asia
has contributed 28.9%, Africa (including Macaronesian islands, Canaries, Madeira and Azores) 21.6%,
North America 16.5%, Australasia 7.2% and the neotropics just 5.2%. The route for almost all aliens to
Europe is via importation of plants or plant products. Most alien Lepidoptera established in Europe are
also confined to man-made habitats, with 52.5% occuring in parks and gardens. We highlight four species
in particular, Diaphania perspectalis, Cacyreus marshalli, Cameraria ohridella and Paysandisia archon, as the
most important current economic threats.

Keywords

biological invasion, introduction, pest species, Europe, Lepidoptera, globalisation

11.1 Introduction

Apart from the undoubted impact of climate change, various other facets of human
activity, including the increasingly efficient means of transport in the last century,
increased trade and globalisation, are having a dramatic effect on the composition
of European faunas. Lepidoptera, as a mostly alate and largely phytophagous insect
group, are particularly affected, not only by increased transport of the invasive species,
but by increased trade in plants and stored plant products. In addition, many species
are spreading to hostplants not used in their area of origin.

Lists of naturalized non-native Lepidoptera are already available for a number of
European countries (Agassiz 1996a, Essl and Rabitsch 2002, Geiter et al. 2001, Karsholt
and Nielsen 1998, Kenis 2005, Sefrov4 and Lagtttvka 2005). In addition, several de-
tailed case studies have been published on the process of invasion to Europe of several
non-native Lepidoptera species (Nash et al. 1995, Sefrova 2001, Sefrova 2002a, Sefrova
2002b, Sefrov4 and La&tiivka 2001, Whitebread 1990). The first list of terrestrial inver-
tebrate species alien to and within Europe included 272 Lepidoptera species, of which
122 were alien to Europe, 139 alien to countries within Europe, and 11 of cryptogenic
origin (DAISIE 2008). We substantially revise and update this list here, in the first
comprehensive review of known naturalized non-native Lepidoptera known to Europe.

We divided species into two categories:

1. Naturalized exotic species (originating from a continent other than Europe) whose
first introduction into Europe appears to be a direct or indirect (deliberate or acci-
dental) result of human activity (Table 11.1). This includes now well known alien
lepidoptera such as the Neotropical castniid moth Paysandisia archon (Burmeister,

We

ii)

iii)

iv)

Lepidoptera. Chapter 11 605

1880) or the South African lycaenid butterfly Cacyreus marshalli (Butler, 1898).
We also considered in this category species of unknown origin (cryptogenics) such
as the leaf-mining moth Phyllonorycter platani (Staudinger, 1870). It is worth not-
ing that we also included here species introduced into confined environments like
greenhouses which while not apparently spreading of their own accord, have been
introduced with their hostplants, with the potential to spread due to horticultural
trade. For instance, 11 species of aquatic Pyralidae have been introduced acciden-
tally by man from Asia and North America into Europe, mostly as contaminants of
plants. Current climate makes their establishment in the wild unlikely, but global
warming could allow their establishment in the near future.

European species spreading throughout the continent as a result of human activity
(Table 11.2). This category includes the invasive leaf-mining moth Cameraria ohridella
Deschka and Dimi¢, 1986, now understood to be Balkan in origin (Valade et al. 2009).
It is worth noticing that although many aliens are highly invasive our review also
includes naturalised aliens that are not necessarily invasive such as the saturniid

moth Samia cynthia (Drury, 1773).

excluded all the following cases, here giving examples:

Species showing clear range expansions/contractions at a country level, which are
known to follow global climate change trends (Warren et al. 2001). The butterfly
Colotis evagore (Klug, 1829) in Spain (Fric, 2005), the processionary pine moth
Thaumetopoea pityocampa (Denis & Schiffermiiller, 1775), in central Europe (Bat-
tisti et al. 2005) and several British butterfly species (Asher et al. 2001) are classical
examples of this phenomenon. However, it must be noted that 7’ pityocampa has
apparently been introduced through human activity from continental Italy to Sar-
dinia (Luciano et al. 2007).

Naturally-expanding species known as migrants which have established without
clear human assistance, such as the choreutid Tebenna micalis (Mann, 1857) in
Azores (Karsholt and Vieira 2005) and the geometrid Peribatodes secundaria (Denis
& Schiffermiiller, 1775) in Great Britain (Kimber, 2008) as well as rare vagrants
that may or may not sporadically naturalize, such as Acontia crocata Guenée, 1852
in France (Letellier, 2004); Pardasena virgulana (Mabille, 1880) in Great Britain
(Honey, 1994) and Gelechia sabinellus (Zeller, 1839), Eccopsis effractella Zeller,
1848 and Zophodia grossulariella (Hiibner, 1809), all recently recorded from Great
Britain (Agassiz 1978a, Agassiz 1996b, Roche 1982).

New records of species probably overlooked in particular countries for which there
is no clear evidence of range expansion. For instance, in Great Britain the presence
of Bucculatrix ulmifoliae Hering, 1931 and Ocnerostoma spp. (Heath and Emmet
1996, Langmaid et al. 2007).

Deliberate translocations of species between European countries, such as the intro-
duction of the butterflies Avaschnia levana (Linnaeus, 1758) (Frohawk, 1940), Ma-

606 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

culinea arion (Linnaeus, 1758) (Thomas et al. 2009) and Lycaena dispar (Haworth,
1803) (Ford, 1945) into Great Britain. These translocations result from solitary
enthusiasts or are for conservation management purposes including the reintro-
duction of extinct species, but have nothing to do with our subject of biological
invasion, essentially the aspects associated with increased globalisation.

v) Species once apparently established but now extinct (e.g. in Great Britain, the
blastobasid Blastobasis phycidella (Zeller, 1839) and the oecophorid Euclemensia
woodiella (Curtis, 1830) (Emmet 1988, Koster and Sinev 2003)

vi) The large number of living display species (this is the case of butterfly houses),
unless these species are either establishing in the wild, or there is evidence they
have become greenhouse pests (we have no examples). Nevertheless, we highlight
the risks involved in importation of butterflies for butterfly houses and for a new
practice of wedding releases.

Finally, the introduction of exotic host plants by man has indirectly allowed sev-
eral lepidopteran species to expand their distribution range. We consider as alien species
Stigmella speciosa Frey, 1857, Caloptilia rufipennella (Hiibner, 1796) and Phyllonorycter
geniculella (Ragonot, 1874), all feeding on Acer pseudoplatanus in northern Europe; Stig-
mella suberivora (Stainton, 1869) feeding on Quercus ilex in Great Britain; Eupithecia
phoeniceata (Rambur, 1834) feeding on Juniperus and various Cupressaceae in Belgium
and Great Britain, Cydia grunertiana (Ratzeburg, 1868) in Belgium, Denmark and Swe-
den; C. illutana (Maslov, 1988) and C. pactolana (Zeller, 1840) feeding on Larix, the
last two in Great Britain; Thera cupressata (Geyer, 1831), feeding on imported Abies in
Sweden and Cupressaceae in Great Britain, and Lithophane leautieri (Boisduval, 1829)
on Cupressaceae cultivars in Great Britain. Polychrysia moneta (Fabricius, 1787) started to
spread as early as 1891 in Europe, possibly as a result of rise in popularity of ornamental
hostplants such as De/phinium in gardens (Agassiz, 1996a). Other well known examples
of species which have followed the invasion of their host plants are the milkweed but-
terflies, Danaus plexippus (Linnaeus, 1758) and Danaus chrysippus (Linnaeus, 1758). The
larvae of both species feed on ornamental and invasive milkweeds (Apocynaceae) which
have been introduced in some Macaronesian islands and the Iberian Peninsula (Baez,

1998).

We summarise the relative importance of naturalized alien invasives by family, in rela-
tion to their proportion in the relatively well known European fauna, finding great
disparities in their prevalence.

11.2 Diversity of alien lepidopteran species

Lepidoptera is one of the largest insect orders, with around 175,000 described spe-
cies in 128 families and 47 superfamilies (Kristensen and Skalski 1999, Mallet 2007).
About 9,428 native species in 83 families and 31 superfamilies have been recorded in

Lepidoptera. Chapter 11 607

Europe (Karsholt and Kristensen 2003). A total of 97 non-native Lepidoptera species,
in 20 families and 11 superfamilies have established so far in Europe (Table 11.1). Our
analysis reveals that there is a significant correlation between the number of alien spe-
cies and the number of native species per family (Spearman’s rho correlation: r= 0.48,
P < 0.001). In addition, 88 European species in 25 families have expanded their range
within Europe and many of these are of Mediterranean origin, invading northern and
western areas of Europe (Table 11.2).

The 20 families which contain alien species to Europe are: Pyralidae (30 species),
Tortricidae (10), Gracillariidae (8), Tineidae (7), Noctuidae (6), Gelechiidae (6),
Blastobasidae (5), Yponomeutidae (4), Oecophoridae (4), Cosmopterigidae (3), Sat-
urniidae (3), Pterophoridae (2), Nymphalidae (2) and Bucculatricidae, Agonoxenidae,
Lycaenidae, Geometridae, Arctiidae, Nolidae and the alien family Castniidae, each
with one species (Table 11.1).

Agonoxenidae: Sixteen species of agonoxenids are native to Europe. The Asian
species Haplochrois theae (Kusnezov, 1916) represents the only alien. During the 20"
century this was a serious pest on tea plantations in Georgia and to a lesser degree, in
the Krasnodar Territory of Russia (Sinev, 1994).

Arctiidae: One hundred and one species of arctids are native to Europe but only
one species, the North American Fall Webworm, Hyphantria cunea (Drury, 1773), is
alien to the region. The larvae are highly polyphagous, feeding on hundreds of differ-
ent species of deciduous trees on which they form conspicuous webbed nests in late
summer and autumn.

Blastobasidae: Only 41 species of native blastobasid moths have been recorded in
Europe, a large evolutionary radiation of which 26 species occur in Madeira (Karsholt
and Sinev 2004). However, the number of alien species in this family (five) is relatively
high, mainly because the larvae feed usually on dead organic matter. Some species, such
as Blastobasis lacticolella (Rebel, 1940) are pests of stored foodstuffs. Interestingly, all
alien Blastobasidae appear to have colonized continental Europe (mostly Great Britain
and/or mainland Portugal) from Madeira, presumably with the import of ornamental
plants. The common species B. adustella Walsingham, 1894 (originally described as a
form of B. lignea Walsingham) (Sinev, 2007) is another example. However, B. adustella
has widely been treated, erroneously, as a synonym of the Madeira endemic species B.
vittata Wollaston, 1858. Although there are records attributed to B. vittata on the in-
ternet, including from the British Isles, there are no unambigously identified instances
of the introduction of this species outside Madeira at present.

Bucculatricidae: There are 53 native bucculatricids known in Europe. One macaro-
nesian species, Bucculatrix chrysanthemella (Rebel, 1896), was recently introduced from
the Canaries into Italy and France, where it seems to have established populations. ‘This
species has also recently been recorded from Finland, at which latitudes it seems unlikely
to become established (Siloaho, 2008). B. chrysanthemella attacks Paris Daisy (Argyran-
themum frutescens), an economically important ornamental crop in some parts of Europe.

Castniidae: This family has no native species in Europe. The majority of castniid
moths are Neotropical, while some species are also found in Australia and South-east

608 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Asia. The Neotropical Paysandisia archon is the only alien castniid known to occur
in Europe and is currently spreading along the Mediterranean coast attacking a wide
range of palm species. The castniid Riechia acraeoides (Guérin-Meéneville, 1832) is one
of numerous sporadic adventatives included in the previous list (DAISIE 2008) that
we discount here.

Cosmopterigidae: There are 79 species of cosmopterigids native to Europe, with
three species considered as aliens. Two of these are African species that feed on Acacia
in Malta. The larvae feed internally on the leaves, seeds and stems of their hostplants.
There is no evidence that Cosmopterix pulchrimella Chambers, 1875, recently estab-
lished in Cornwall, Great Britain, arrived there directly through human agency.

Gelechiidae: There are 697 species of gelechiids known to occur in Europe. The
larvae of most species are concealed feeders on plant tissues, many of them feeding
internally in seed heads and fruits, some mining and even producing galls. Six alien
gelechiids are known from Europe, among them major agricultural pests such as the
Tomato Leafminer Tuta absoluta (Meyrick, 1917), the cosmopolitan Angoumois Grain
Moth Sitotroga cerealella (Olivier, 1789), which attacks stored whole cereal grains, and
the Pink Bollworm Pectinophora gossypiella (Saunders, 1844), whose larvae bore into
the flowers and seeds of cotton.

Geometridae: There are 1,024 species of geometrids native to Europe, but only
one non-native species appears to have naturalized in Europe. This is Pseudocoremia
suavis (Butler, 1879), an endemic geometrid to New Zealand (Berndt et al. 2004),
which was recorded on five separate occasions in Cornwall in 2007 (James 2008, Skin-
ner 2009), suggesting establishment in the wild. This species, polyphagous on various
gymnosperms, represents a potential risk to European conifer forests.

Gracillariidae: There are 249 species of native gracillariids known in Europe and
eight alien species have been recorded. Among these are pests of economic importance,
such as the Citrus Leafminer Phyllocnistis citrella Stainton, 1856.

Lycaenidae: One hundred and thirty-six species of lycaenids are native to Eu-
rope. The South African Cacyreus marshalli is one of the few butterflies which are
naturalised aliens in Europe (see also under Nymphalidae). ‘This is a pest of cultivated
Pelargonium plants, mainly in Mediterranean region but it was found to be breeding in
Great Britain in 1997 (Lewes, East Sussex), where it became temporally established in
greenhouses until May 1998 but was eradicated (Holloway, 1998).

Noctuidae: This is the most species-rich family of Lepidoptera in Europe, with over
1,435 native species. Six alien noctuids have been recorded so far, including some major
agricultural pests such as Chrysodeixis eriosoma (Doubleday, 1843) and Spodoptera litura
(Linnaeus, 1758). However, on a cautionary note, these genera are known to have strong
migratory tendencies. Indeed we may never know, due to lack of sufficient historical
records, when or whether certain noctuids arrived as invasives to Europe or by artificial
agency. One good example of this is Araeopteron ecphaea (Hampson, 1914) (type locality
Nigeria). It is also interesting to note the African and Austral-Oriental fern-feeding spe-
cies Callopistria maillardi (Guenée, 1862) seems to have been accidentally imported with
Nephrolepis ornamental ferns, but this species has five subspecies and the precise origin

Lepidoptera. Chapter 11 609

of the introduced individuals is unknown. Some records of Chrysodeixis acuta (Walker,
1858) could also represent misidentifications of C. chalcites (Esper, 1789). Following our
exclusion criteria, we have not included singleton records, for example of Acontia crocata
Guenée, 1852, a specimen of which was collected in Irais (Deux-Sevres), France (Letellier,
2004), possibly resulting passively from a plant import from SE Asia (Hacker et al. 2008).
Nolidae: Thirty-five species of nolids are native to Europe, but only one exotic species
has repeatedly been recorded within the region, the Spotted Bollworm, Farias vittella (Fab-
ricius, 1794). The larva of this species feeds on several plants of the family Malvaceae, in
particular Okra (Abelmoschus esculentus) pods, Gossypium (it is one of the most important
pests of cotton) and Hibiscus. It has been found as a vagrant in Great Britain and seems to
also be present in southern Spain (Nash, 2003). Its establishment needs to be confirmed.
Nymphalidae: There are 239 species of nymphalid butterflies native to Europe.
Two non-native danaine species, the Monarch butterfly Danaus plexippus and the Plain
Tiger D. chrysippus have established themselves in the Macaronesian islands and Iberi-
an Peninsula. We have included both species despite them being well known migrants
because their introduction and establishment in Europe has followed the invasion
and establishment in Europe of their Apocynaceae host plants (Asclepias curassavica,
of Neotropical origin and Gomphocarpus fruticosus of Afrotropical origin). Thus, the
Monarch’s range has greatly expanded during the 19th and 20th centuries from North
America and now encompasses numerous Atlantic, Pacific and Indian Ocean islands
and Australia. A number of hypotheses have been developed to explain this great range
expansion (Vane-Wright 1993).
Oecophoridae: There are 120 native species of oecophorids in Europe. Only four al-
ien oecophorids are established in the region, three of which feed on dead plant material.
Pterophoridae: There are 166 native pterophorids known to Europe. Two species,
Megalorhipida leucodactylus (Fabricius, 1794) and Lantanophaga pusillidactylus (Wallk-
er, 1864) are known to be alien to Europe. M. leucodactylus has a circum-tropical dis-
tribution and has established populations in Sicily (Bella and Ferrauo 2005) and Israel.
It has also been recorded in Spain, but its presence there needs confirmation (Gielis,
pers. comm.). The larvae feed on Amaranthaceae, Cucurbitaceae, Goodeniaceae, Legu-
minosae, Nyctaginaceae, Rosaceae and Asteraceae (Vargas, 2007). The Lantana Plume
Moth L. pusillidactylus is also a pantropical species whose origin, as for M. leucodactylus,
is not clear. This species has been introduced with its Verbenaceae hostplant (which is
of neotropical origin), Lantana camara, into Spain, Portugal and southern Italy (Aguiar
and Karsholt 2006, Bella and Marchese 2007, King 2000). The moth is used as the
biocontrol agent against this plant, itself an invasive in many parts of the world.
Pyraloidea (Pyralidae and Crambidae): This superfamily has 898 native spe-
cies known in Europe. Pyraloidea also has the highest number of species (30) alien to
Europe. This is probably due to the high number of alien crambid pyrales that have
larvae feeding on submerged and floating aquatic plants used in aquariums and ponds
(11 species) as well as cosmopolitan pests that feed on stored products (seven species).
These invasives include the North American wax moth Vitula edmandsii (Packard,
1865), whose larvae damage the combs of honeybee and bumblebee nests.

610 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Saturniidae: Seven saturniids are native to Europe. Three Asian species have de-
liberately been introduced into Europe for silk production, but have naturalized from
escapes. This family is also very popular among amateur breeders and sometimes there
are reports of adult moths of a wide number of species in urban areas.

Tineidae: There are 262 species of native tineids in Europe and seven alien species
have also been recorded to the region. At least five of these feed on stored products,
cloths, and detritus, such as the Common Clothes Moth (Tineola bisselliella (Hummel,
1823)), whose larvae feed on clothing and natural fibres.

Tortricidae: About 977 species of tortrix moths have been recorded as native to
Europe. Among the 10 alien species recorded to Europe, there are some economi-
cally important pests, in particular of apple trees, for example the oriental fruit moth
(Grapholita molesta (Busck, 1916)) and the light brown apple moth Epiphyas postvit-
tana (Walker, 1863). Larvae of the latter species are not easily distinguished from the
larvae of other tortricid leafrollers; only DNA-based testing appears to work reliably
for identification. Interestingly, half of the tortricids recorded as alien to Europe (five
out of 10 species) are specialists on Cedrus and have been introduced into southern
France, where plantations of these trees are common.

Yponomeutidae: There are 113 species of ermine moths native to Europe, with
four alien species having been recorded. ‘The larvae tend to form communal webs,
and some species are agricultural forestry pests, such as the Arborvitae Leafminer, Ar-
gyresthia thuiella (Packard, 1871) and Prays citri (Milliére, 1873), a well-known Citrus
pest in the Mediterranean region. Two North American leafminers of the genus Ar-
gyresthia attack Cupressaceae in Europe.

In our analysis, it is interesting that we found a similar number of alien species
to Europe (Table 11.1) as species that have expanded their range within Europe due
to human activity (Table 11.2). Indeed, there is a significant correlation between the
number of alien species per family to Europe and the number of alien species per fam-
ily within Europe (Spearman’s rho correlation: r= 0.39, P = 0.044). However, several
families exhibit some species which have expanded their range within Europe, yet
have very few or no recorded aliens to Europe. For instance, strikingly, Geometridae
features only one species alien to Europe within a fauna of 1,024 species, a number of
which are known migrants, whereas as many as 11 species have been recorded invad-
ing other countries within Europe (Table 11.2). The North American sterrhine ge-
ometrid /daea bonifata (Hulst, 1887) has been intercepted several times with imports
of dried plant material but, as far as known, is not yet established in Europe (Martinez
and Coutin 1985).

The absence of alien species within other species-rich families, such as Coleophori-
dae (533 spp.), Nymphalidae (239 spp.), Psychidae (231 spp.) Nepticulidae (242 spp.)
and Sphingidae (39 spp.) is also notable. In spite of the known high mobility of the
last family, several exotic species (i.e. the American Sphinx drupiferarum Smith, 1797,
Agrius cingulatus (Fabricius, 1775) and the African Polyptychus trisecta (Aurivillius,
1901)) have been recorded (sometimes repeatedly) within the region, with no con-
firmed establishment (Marabuto 2006, Pittaway 1993, Waring et al. 2003).

Lepidoptera. Chapter 11 611

11.3 Temporal trends

The precise date of arrival is not known for two species. An analysis of the 95 species
for which the date of the first record in Europe is known shows that the arrival of alien
Lepidoptera has dramatically accelerated during the second half of the 20th century
(Figure 11.2). This trend is still increasing, with an average of 1.9 alien Lepidoptera
newly established per year in Europe between 2000 and 2007 (Figure 11.2). This aver-
age is twice that during the period 1975 to 1999 (1.1 species per year). The same trend
has been observed for all groups of alien terrestrial invertebrates analysed together
(Roques et al. 2008). This temporal trend might be due to the acceleration of processes
that happened in much wider time frames in the past, such as global climate change
and human assisted transportation via the much faster and more efficient means of
transport nowadays.

Alien species have historically been introduced for centuries, so it should not be
considered that invasive species are necessarily a 20° century phenomenon, although
the poor documention of older cases inevitably also provides more scope for specula-
tion. One such case is Euclemensia woodiella, belonging to a North American oecoph-
orid lineage (Koster and Sinev 2003) found in numbers near Manchester in 1829 and
not since. A much older potential example is the lasiocampid Pachypasa otus (Drury,
1773) with a scattered distribution in southern Italy, whose larva feeds mainly on Cu-
pressus, could even have been introduced by the Romans for “Coan” silk production,
as it possibly represents the “Assyrian Bombyx” mentioned in Naturalis Historia by

Plinus (Good, 1995).

11.4 Biogeographic patterns

For at least 19 alien species, the precise area of origin is not known and these we
consider as cryptogenic. We have classified Phyllonoryctyer platani (Gracillariidae) as
cryptogenic because there are some doubts regarding its origin (Sefrova, 2001). Thus,
P platani is either of North American origin and was introduced to Europe with Amer-
ican Platanus occidentalis, or it originated in Southeastern Europe and Southwestern
and Central Asia, on Platanus orientalis. We have included C. ohridella as alien within
Europe (Table 11.2) since recent genetic studies suggest a Balkan origin as most likely
(Valade et al. 2009).

An analysis of the 78 alien species for which the native area of origin is known,
shows that Asia has contributed the most alien species with 28.9% (28 out of 97 spe-
cies) (Figure 11.3). Africa (including Macaronesian islands, Canaries, Madeira and
Azores) supplied 21.6% of alien species (21 out of 97 species) followed by North
America with 16.5%, Australasia with 7.2%, and the Neotropics, surprisingly few
with 5.2%.

Large differences exist among European countries in the number of alien Lepidop-
tera recorded per country (Figure 11.4). With 42 species, the United Kingdom is the

612 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

% species % species
30 20 10 0 0 10 20 30 40

Pyralidae + Crambidae
Tortricidae
Gracillariidae
Tineidae
Noctuidae
Gelechiidae
Blastobasidae
Oecophoridae
Yponomeutidae
Cosmopterigidae
Saturniidae
Nymphalidae
Pterophoridae
Geometridae
Lycaenidae

rctiidae
Bucculatricidae
olidae
Agonoxenidae
Castniidae
Coleophoridae
Nepticulidae
Psychidae
Scythrididae
Depressariidae
Sesiidae
Zygaenidae
Pieridae
Adelidae

Native species Alien species

1024

oooocococcoce

Figure 11.1. Comparison of the number of species per family of Lepidoptera in the alien and native
entomofauna in Europe. Families are presented in a decreasing order based on the number of alien species.

Only the most important families of native species (> 50 spp.) have been considered.

European country with the highest number of alien Lepidoptera, followed by France
(mainland) with 41 and Spain (mainland) with 39 species. Both Moldavia and Luxem-
burg are the European countries with the lowest number (with one alien species each).
These differences are very likely to result at least partly from variation in sampling ef-
fort and the availability of local taxonomic expertise, but the area and the geographical
location of a country is also a very important factor, in this respect.

11.5 Main pathways and vectors to Europe

As far as we know, most Lepidoptera alien to Europe have been introduced accidentally
(96.9%). A clear exception is some saturniid species that were imported from Asia into
Europe for silk production in the nineteenth century, and subsequently became natu-
ralized, including in urban areas. On the other hand, the Silkmoth Bombyx mori Lin-
naeus, 1758. has not been included in the analysis, because although it is widespread
in captivity throughout Europe, its flightlessness has prevented naturalisation.

The import of ornamental plants (particularly palms, geraniums and azaleas) is most
likely responsible for the introduction of several species such as Paysandisia archon, Ca-
cyreus marshalli and Caloptilia azaleella. Transport also plays an important role in the
dispersal of some species, including ones alien within Europe. For instance, Cameraria

Lepidoptera. Chapter 11 613

Mean number of new alien species
recorded per year during the period

0 0.5 | 1.5 2 2.5
| ! | |

1492-1799 4»
1800-1849
1850-1899 —
1900-1949 —
1950-1974 —
1975-1999 —
2000-2007 —

Time period
Figure | 1.2. Rate of established alien Lepidoptera in Europe since 1492 as mean number of alien Lepi-

doptera recorded per year. Calculations are made on 95 alien species for which the first record is precisely

known. Numbers above bars indicate number of new species recorded per period.

ohridella seems to feed almost exclusively on Aesculus hippocastanum trees planted in urban
areas and parks. The main means of its spread is likely to be wind dispersal, but human
assisted transportation played a major role in the long distance dispersal of this species
(Gilbert et al. 2004). Since the advent of tropical butterfly houses in the 1980s, a potential
new threat has emerged, the use of mass butterfly releases for weddings, a practice increas-
ingly popular in countries such as Italy, where one of us (AZ) has recorded a number of
exotic species flying freely in cities. Usually Monarch butterflies are used, but less scrupu-
lous companies may be using a range of exotics, many of which are likely to find climate
change and the availability of hostplants for some papilionid butterflies, such as Rutaceae
planted in city gardens propitious for establishment of at least temporary populations.

11.6 Most invaded ecosystems and habitats

Most alien Lepidoptera are phytophagous (78.3%), whereas detritivores represent only
21.6% (Table 11.1). The majority of alien Lepidoptera established in Europe are con-
fined to man-made habitats, and only a few species have become established in a more
or less natural environment, mostly in woodlands. Examples of the latter include the

614 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Cryptogenic Africa
19.6% Seem /21.6%

Tropical, subtropical
Central & South America |
5.2%

North Amerie
16.5% ;

. Asia
28.9%

Avetrdasia
7.2%

Figure | 1.3. Regions of origin of the Lepidoptera species alien to Europe

20°W o° 20°E
I i J

70°N

30°N

Number of alien species

|nodata || 10-19 SY 30-42
> a

Figure | 1.4. Colonization of continental European countries and main European islands by Lepidop-

tera species alien to Europe.

Lepidoptera. Chapter 11 615

Percentage of alien lepidopterans
living in the habitat

0 20 40 60

Coastal areas {J 2
Inland surface waters 0
Mires and bogs~ 0
Grasslands ff 3
Heathlands (13
Woodlands and Forests [0 19
Inland without vegetation {J 2
Agricultural lands (00) 25
Parks and gardens [i 5
Buildings, houses [i 33
Greenhouses - | 6
Habitat complexes {i 4

Habitats

Figure 11.5. Main habitats of 97 alien Lepidoptera species established in Europe (note that a species

may live in several habitats).

arctiid Hyphantria cunea, the gracillariid Phyllonorycter issikii in Central Europe and
the saturniid Antheraea yamamai in the Balkans.

In Europe, most alien Lepidoptera species feed on their original hostplants. How-
ever, some species seem to have been able to switch to other hostplants that are often
closely related. For instance, Paysandisia archon specializes on Trithrinax campestris
(Arecaceae) and to a lesser extent on Cocos yalai in its native area (Argentina, Uruguay).

However, in Europe this moth has expanded its host range to many ornamental
exotic palms (Phoenix canariensis, Latania sp.) as well as posing a threat to the native
Chamaerops humilis (Montagud Alario 2004).

About 50.5% of alien Lepidoptera live indoors in domestic, industrial and other
artificial habitats such as 16.5% in greenhouses (Figure 11.5). Six out of the nine species
that feed on stored products show a cosmopolitan distribution. Parks and gardens host
52.6% of alien species, where they are frequently introduced with their native hostplant,
while 25.8% have colonized agricultural land (Figure 11.5).

11.7 Ecological and economic impact

The impact of most alien Lepidoptera species has not been quantified in detail. How-
ever, negative economic impact has been recorded for 16 alien species. The Indian

616 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Figure 11.6. Adult habitus of some lepidopteran species alien to Europe: a Argyresthia thuiella b Parec-
topa robiniella ¢ Phyllonorycter issikii winter form d Phyllonorycter issikii summer form e Phyllonorycter
leucographella € Phyllonorycter platani g Phyllonorycter robiniella h Plodia interpunctella i Tineola bisselliella
j Ephestia kuehniella kk Hyphantria cunea male | Hyphantria cunea female (drawings by Ales Lasttvka).

Lepidoptera. Chapter 11 617

Figure 11.7. Adult habitus of some lepidopteran species alien im Europe: a Coleophora laricella b Coleo-
phora spiraeella ¢ Cameraria ohridella d Caloptilia roscipennella e Leucoptera malifoliella f Acalyptris platani
g Stigmella aurella h Stigmella atricapitella i Stigmella centifoliella j Stigmella pyri k Stigmella speciosa \
Stigmella suberivora m Argyresthia trifasciata; n Ectoedemia heringella. (drawings by Ale’ Lastivka).

618 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Figure 11.8. Alien saturnid orginating from Asia, Antherea yamamai a adult b 2nd instar lar-
va (credit Zdenek Lagttivka)

Meal Moth Plodia interpunctella (Hiibner, 1823) may severely affect grain and grain
products, dried fruits and seeds in households and warehouses. The Common Clothes
Moth Tineola bisselliella is another example of a major pest in houses where it feeds
on clothes, carpets, rugs, and upholstered furniture. However, along with several other
tineids, this species has become rare due to the increase in use of man-made fibres and
the dry environment created by central heating (Kimber, 2008). The most serious alien
lepidopteran pests in orchards in many parts of Europe include Grapholita molesta,
Hyphantria cunea and Prays citri.

Some species can also cause aesthetic impact. Thus, species causing severe infes-
tations can lead to almost complete defoliation of the hostplants. For instance, C.
ohridella causes premature defoliation of the white-flowered horse-chestnut, Aesculus
hippocastanum. ‘The trees do not die but the aesthetic impact is so severe that in some
countries, heavily infested trees have been felled and removed.

Lepidoptera. Chapter 11 619

Figure 11.9. Clearwings (Sesiidae) alien in Europe. a Pennisetia hylaeiformis 3 b Synanthedon
andrenaeformis oe Synynthedon myopaeformis 3. (credit Zdenek Lasttivka)

Little is known, however, about the ecological impact of alien Lepidoptera in natu-
ral areas of Europe (Kenis et al. 2009). Four alien Lepidoptera species seem to have a
potentially important ecological impact: 1) the recently introduced pyralid Diaphania
perspectalis that could represent a serious threat to topiary Box hedges and plants in
nurseries, parks and gardens, and Buxus shrubs growing in the wild; 2) C. ohridella,
that recent studies suggest could have a potential negative impact on native leafminers
via apparent competition and could be adapting to Acer species in some areas (Péré et
al. 2009); 3) the lycaenid Cacyreus marshalli, which threatens both native geraniums
and Geranium-consuming lycaenids (Quacchia et al. 2008); 4) finally, as previously
mentioned, Paysandisia archon represents a serious threat to the conservation of natural
populations of Chamaerops humilis, the only native palm in Europe (Montagud Alario
2004, Sarto i Monteys 2002).

Lastly, we recommend that in order to guarantee the well being of natural eco-
systems and also to keep track of future additions to the European alien Lepidoptera
list, natural areas of special conservation concern like those under the Natura-2000
framework should be monitored more intensively and regularly for the early detection
of potential threats, which according to our results are expected to increase.

620 Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

Figure 11.10. Damage by alien lepidopteran larvae. a mines of Parectopa robiniella on Robi-
nia b 3rd instar larva of Cameraria ohridella extracted from its mine on Aesculus ¢ damage of
Hyphantria cunea on Acer negundo d mines of Phyllonorycter issikii on Tilia e mines of Phyllo-
norycter platani on Platanus (Credit: Hana Sefrova).

Acknowledgements

We would like to thank Leif Aarvik, Giorgio Baldizzone, Jarostaw Buszcko, Martin
Corley, Mirza Dautbasic, Willem Ellis, Eddie John, Natalia Kirichenko, Ferenc Laka-
tos, Phil Lambdon, Paul Sammut and Jaan Viidalepp for sending information about
alien Lepidoptera from their respective countries. We also thank Cees Gielis and Klaus
Sattler for comments on Pterophoridae and Gelechiidae respectively; Shipher Wu and
Shen-Horn Yen for their comments on Callopistria maillardi and Juan Jose Pino Perez
and Antonio Verdugo Paez for their comments on Danaus. David Lees was funded by

a STUDIUM fellowship during preparation of this paper.

Lepidoptera. Chapter 11 621

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641

(QVW-Ld) OFGI

(FOOT) AdUIS pue YoOYsIey jerovew PISOUOIeIRYy | + SNOIOA Poq2y 77721092190]

‘(900Z) NoysIey pur semsy je1999A SurAv9q] FD ‘OVG! ‘wOlyy| eq] V SISYGOISIT

sionpoid parois pue

‘uoreIagaa ToNIT]-Jeo] (AVN-Ld) (SST ‘worseT]o\)

(FOOT) AUIS SUIPNOUT ‘s]JMIspooy PISOUOIeIRYy | SNOIOA DUJaLojoIap

pur qoysreyl “(900Z) ‘Te 39 Aap10D JO MDHEA OPA Ld ‘9961 ‘eOHFY | -HYIOd| V SUC
(YOO) AeUIS (AVW-Ld)

pure qoysieyy “(G00Z) ‘Je 19 sug Jeoveur PISOUOIeIRYy | SNOIOA HES ‘weysurseny

2d ‘(900Z) 4ousreyy pue remsy [e1099A Sutkeooq IN “Al ‘GD WA “Ad AI ‘ZO6I eOUfY| -QIN9q| V DIJASNPD SISVGOISIIT

IEPIseqo}seg

(€O0Z) AUIS
pur Joisoy ‘(91 G6[) AOpryowsad

(2861) C10L “(9F6T)

tuping “(7/6 ]) OpUrYsoreA
“(SOOZ) BYAMISLT pue PAOIZIG
‘(1661) Jesoy-fedueqzoy ‘(S861)
TUTUIOIUOY] ‘(CGG6T) P[PYsoy pue
SINT ‘(8661) UeSpIN pur ioyssey
“(89G61) 21Z9URl “(T86]) UezuerEg
pure oujoddy ‘(Z7907Z) yosuqry pure
JowanyP] ‘(666[) aplulay pue
DIPsery) “(ZOOT) Yosuqey pue

Lepidoptera. Chapter 11

VIJAUV) ‘VAT

(sumenf snunsy SnLopy
snyndoy ‘opunsau
AIP) SdoI1 snonpidap

aD “MS ‘Is “nu “Su
‘OU “Td IW “AW
‘CW ‘IT “LI ‘NH
WH UD “AC ‘UW
‘dd “Md “Ad “ZO

Ne “ST6T

voloury | snoseyd

(QIG6I ‘Aozousny)
avay1 s1oLgI0j dE]
seplusxou0sy

(EZZ1 ‘Aimiq)

Issq ‘(OO0Z) FPPMON pure oyzsng uo snoseyddjog ‘TI ‘SD | HD ‘D9 ‘V9 fLV “TV -ouyg V vauns vidqupy dey
aepinory
AxyUNOD
Wegey pur odoimq aSuri sated
SIDUIIIFIY sIsOP] uaTTV SdIIJUNOD popeauy | UT prOdaI ,.T DATIEN sUIIBay | snIVIS Ayrore,y

6007/90/10 2epdn aseT *([] xipuodde das) STN 02 Joyo suonerasrqge yweugqep ‘(| x1puodde 92s) 99 [¢€ OS] 0
JaJoI suOMeTAaIQge sapod ArUNO’) ‘sa1dads stuaBoI1dAID F adommy 01 vary w :snzeis ‘adomny o7 uarye sa1oads uessidoprday ayi Jo sonstsoioereyo pur is] “4° | | SIQUL

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

642

(Z00Z) ‘Te 9

yprdung ‘(1 661) youdiay “(Z00Z) (€06I
yosuqey pur Jouonyy ‘(SQOZ) Te MS ‘LI ‘AH snoseyd ‘oyieayy) vyavand
39 TH “(Z00Z) Wsqey pue [ssy SD. Ad Ae ZO TY.) AD“¢S6l -oyd| V Sore 0a)
depITyse]er)
(ZI6I ‘Pq2u)
snoseyd snpjauvjauLomnay
(9002) INuTUeS pure IJoisoOy ee LW ‘4007 oud) V saprotasofig
snoseyd GIGI SuanoyD
(9007) NUNS pur JoIsOy VIWIY LW ‘10072 -ouyg| VW VIJAIIVIV VIUIVISY
(1681
“WILYSUISTEA )
(€00Z) simsy oyeueisour0d Jeordoay, | snoseyd xagduats
ADUIS PUL JoIsOy “(HOOT) PIOPPSH | — “wou0d ‘snoseyddjog Id “AD ‘SA AO} Ld “6661 -tisy| -oyg) V studqoviqvupy
seprsisa}dourso’)
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(FOOT) yomssury[op] ‘snquvItGY IVA ‘DUuojstaryT 1S “DISSLI LI (eolLIsWIYy
“(€QOT) ‘Je 19 esourdsy ‘(CQOT) Je] sdosavuvgy ‘xvussqtAgT AWOMUMD UD WA ynos) | snoseyd (6Z81 “erstowing)
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oepriuyse7)
(6261) (eIsou (9681 ‘Pq°U)
YOsoUNITY] “(GOOTZ) ‘Te 39 IzuRIsUOT) suaasagnaf -oreoey[) | snoseyd MaWagqUDshAGI
‘(600Z) [PN pue 10duronbs0_ mnuaqqUnAlaay LIA Td} LI ‘2002 vongy| -o1yg) VW xaVNIING
seplonyepnoong
(AVW-Ld) 4007
(FOOT) AUIS pure IOYsIey Jeroreur eIsquOIvoePy | snoloA ‘AUIS 29 YOYSIEY]
(9007) NoysIey pur remsy je1099A Surkvo9q] FD ‘8661 ‘wOLyy| eq] VY YaQad SISVQOISIT
(AVW-Ld) CSO PsUay’
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Aa]107) pure oyyeArley op sosseg [e1999A Sutkeooq Ld ‘UW ‘Sa Ld ‘0661 eOUfY| -QIN9q| V SIS QOISYIG
AxyUNOS
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SOIUIIIFIY uaITy | selunoo pepeauy | ul proses, | oeaneN = | owiday | sme Ayrure,y

643

(Z00Z) ‘Te 29 elaueqiay
‘(OLOZ) SFISUIAT pure seysnenscE

IS (LW “LT “OISsLI “LI
WOO'Ud Ud “Ta

snoseyd

(LIGI SHAS)

Lepidoptera. Chapter 11

‘(6007) ‘Te 39 PAoURZITELY eaadeer edb “Sd “SH “HO “Dd “TV SA ‘900Z| soidonoan| -ovyd) Vv Micali ecu ed B
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pur Paospas “(FQ07) aMquNyeL,
pue seysnensc “(Z/6T) [YeW €D “MS ‘IS “AS
‘(O881) UeUSpUTT “(S00Z) ‘Su ‘ne ‘OU “(OZV
PMSA pure yoysiey “(9Z6T) “Ld ‘Ld “Id ‘ON “IN
uas[aIN pur yoysrey “(1 S61) CLAW SMI “11 “OIS-LI
zizeurl “(€661) SPISUIAT “(700Z) VSLI ‘LI ‘SI “AH
yosqey pur Jourony “(796T) WH UD “AD Us ‘Sa
AqnaH ‘(S00Z) ‘Te 9 PPpepucarysy Md “Ad °ZD “HO padres (68Z1 SPANO)
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“COT6T) S9PUP “(YOOT) AUIS pue ‘GVW-Ld ‘OZV-Ld
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AIyUNOS
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SIIUIIIFIY ualTy | seljunoos pepeauy | ur proses, | ocaneN = | ouiday | sme Ayrure,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

644

6S8I ‘sudsuo])

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(4002)
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MUO “(Z66T) SPPIPYW “(S002) Su “AVW:-Ld ‘OZV
eAISIA pure yoysiey “(7661) POIeD “Ld ‘Ld (LW ‘OIS-LI
pure offer ‘(QQ0Z) ‘Te 19 A2]702) NQVS-LI ‘LI “TI “WD snoseyd (9C8T ‘uoluTeIs)
‘(Z661) JeMsy pue oyyeared op SHADE) Ud “SH AD “TV Sd “£661 eisy} -omyd| VY | peso stasrusoy gg
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‘(800Z) SuesUITY pur sPysuTsy “Td “IW ‘IT ‘LI ‘NH
(2007) PsUqeY pur s9wSNyy YH “Ud ‘Sa “AC voqraury | snoseyd E98 ‘sustUa|-)
‘(0007Z) PPPMON pure oxzsng VAG OE ‘ZO “HO ‘Od “LV LI ‘061 -oukyd| Vy | mjatuiqos vdoszaung
(9€61) AIS “(G00Z) PHANG]
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SIIMIIIFIY ualTy | selunos pepeauy | ur proses, | caneN = | owidey | sme Ayrure,y

645

Lepidoptera. Chapter 11

(0661) PRIqauTY

“(€OOZ) AoW], (S661) Fellas
‘(4Z00Z) PACIPS “(100Z) PIPATO
‘(QOOT) sesuIny pue srySUTAT
‘(€00Z) ‘Te 39 UeWSIN] ‘(Z00Z)
yosiqey pure Jouonyy ‘(SQOZ) Te
19 DFJIpusaryy ‘(7 00Z) Uousosyy
pure sulig 9q ‘(0007Z) PPeMON pure

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‘IS “SY “OU “Td “IN
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dD ‘NS ‘IS “aS “GVW
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PAs “(Z00Z) ‘Te 9 [Ou “(8961) ‘OIS-LI “UVSALI “LI
PREW “(YS6T) ayfnowuel (7007) “Tl ‘NH ‘WH UD
yosuqey pur sourony “(€861) ‘dD UOOU WA (0281
uazdnyusyxuery “(Sh61) SPA°N Covi} ‘Sa “MC “a ‘ZO snoseyd ‘sesurpneig) suvaryd
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(1661) uezAnyuoyueLy
pur 1018195 (6661) PACYES (8661)
PAOIPS “(9/61) Y2PW “(Z007) MS ‘IS
ypsuqey pur Jowranzy ‘(GQ0Z) ‘Te “AS “SU “Td “IN ‘LI
19 PPP Pur] “(F661) SUL 2d (vqsuvovsk,]) ‘AH YH UD “dD (OS8I 711°Z)
(L002) B49SD “(F66T) “Te? THN usoyary Apureut Wd “MC ‘ZO “Ad snoseyd pyjaqdeusoona
“(OOOT) FEZEAK, puv yerursreg ‘saysng snoaoesoy “HO ‘Dd “Ad ‘LV LI ‘OS8I PISY MAS -ouyg V Lag LouoyyG
(ZOOZ) ‘Te 39 IFYOL “(PZOOZ) FACES
‘(8661) BAFPION “(ZOOT) YOSqeY
pue sJowronyy ‘(ssozd ur) "Te 19 qy)
DOGUIOF) “(800Z) PACYYsoropy pur MS ‘Ts ‘A ‘OU “Td
ADdPOWTY “(OOOT) PPPMON pure ‘L7 ‘NH “YH ‘Td “Aa snoseyd (C96 “eaxeUINy,)
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AqyUNOS
WIgey pur odoimq aSuri sated
SsadUdIaFIY UsITV SatIJUNOD papeauy | UT pro0dar ,,[ DATIEN] sUIISIy | snIVIS Ayrore,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

646

‘O19 ‘Tamopyuns

‘oreiod ‘ozreur “our20N]
‘seadyoryo :spoom pure
speyusureuso ‘sdoio

sjqeiosaa pure pray Aueur (Chg ‘Aepayqnoq)
jo mnsy pure sseryoy snoseyd pulosotsa
(LOOZ) ‘Je 39 Joma ‘snoseyddjod ATystyy railed 4 Ad! Aad ‘Zo07| ewiseyensny}| -owyg] WV six1aposhlg’)

snag) “oodeqoi “euerueq (jeotdonqns
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(POLY

pure oypeg
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0) SuIps0s08)
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sepruseokT
AxyUNOD

WUgey pure odoimq aSuri sated
SIIUIIIFIY ualTy | seljunoos pepeauy | ur proses, | canenN | ouidey | sme Ayrure,y

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(6661) “097T UeA pur UTsTYONy] POLIOUIYy | + SNOJOA PL6| ‘sespoH
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ey seplioydos0QGQ
S (Z86[) zonsuywoq ULNJaLOGLD
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S enndzry ap Z2WOry “(SG6T) eq | suduvs0gduior ‘svidajosy sLd ‘Ld ‘NVO-SA ‘SH] —-SA ‘2881 oud) Vv snddixayd snvunq
8 LIPLVYIANG
& DULNIIVAV) “WiNaLOgav
aS unidissox) ‘snsorunaf
i (7861) zansuywod-eidey “(700Z)| suduvo0qdiuon ‘ungnsv OIS-LI ‘YH snoseyd (ZI ‘sneeuurT)
enindzry ap zaWOy “(S66I) Arg] — wengouvuky ‘svidgasy UD ‘NVO-SA ‘SA} SA ‘Z86T -oyd| oy | suddishuga snpung
oepreydurAyy
snasiquy pue wnidissor
‘spod (snguajnasa snoseyd (P6LI ‘snioriqe.q)
(€007) 4SeN sngasouyjaqgy) PIO} Of “TI Sd Sa “€007 esy| -oyd) Vv DIJAtLA SULADT
sepljoN
OOrl?I
sjeyuoureuso pue sdoid| ‘TJ ‘gq Jeordoay, | snoseyd (CZZI ‘snioriqe.q)
(8261) Ag[py pue noua ‘snoseyddjod Ayysipy) ‘9-4 ‘C7 q) Aq ‘Iv! 4D ‘861 -ovyg| V vangy viatdopods
AxyUNOD
WUgey pur odoimnq aSues sated
SIIUIIIFIY uaITy | seljunos pepeauy | ur proses, | caneN = | ouiday | sme Ayrure,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

648

(asea sTppIW
OLY
(SOOT) ZoUnIePy YON) | snoseyd LOGI ‘uosdwepy
pur o1ang “(6661) sdraqjassy | (dds xzuaoq7) scan wyed ZI UA ‘SA] SA “6661 voupy| -oyd) V yyjaqus sasdiuady
(1681 ‘uosdurepy)
(S007) snoseyd stuuadiynsup
Te 19 FoIwOD “(9BGT) WoT] — sued soem openby| OOTL ‘TL IN ‘AD| dD ‘261 eisy| -ouyg| V DIJaIZISSVSY
sepiquiery + sepryerdg
‘(avaoRIAISV)
sap1o1gqUIsquv
VIADSSAT ‘(eIDETUIPOOL))
suagsandf DjOAaVIS
‘(avooryluPIeuy)
snyqubivUuyy
‘(aeooeuTseIOAN)
vavsodhy viuay()
snsosaqn4 sndAvotuLulo’)
‘suadad "g ‘sisuaulgo (spurysy
‘g ‘vau1s209 “g ‘vsnffip UISITA,
viapgaog ‘(aea0e qe.) Aqyesoy] ad4y (FELT ‘sniorsqe.s)
(9661) ployfinua, vsowlpy ZI JIS} — ‘ yeordos) | snoseyd snggavpomnay
SIPID “(SOOT) ONeEy pur epg ‘psonusanoau vIIIY| “BACT OISLI “| = <L1 ‘2961 | 2ua8ordd1y} -ordyg] O vprdigvojesay
(eorewre/
(8007) ‘Arpesoy ada (POST TOTEM)
Jaquiry ‘(Z00Z) eseysepy pue CvVW GVW ‘qeotdon) | snoseyd snjkpoppypisnd
Bla (9007) oysrey pur remsy vupuutvs DUPIUYT ZI| “Ld ‘OZV-Ld ‘LI ‘SA} = <Ld “€Z61 | 2ue8oidd1D] -or4yq] O vovydouvyuvT
seprioydosarg
AxyUNOD
yeugqey pure odoing oSurs satvads
SdIUIIIFIY ualTy | selunoo pepeauy | ur proses, | caneN | owmdey | sme Ayrure,y

649

(€FG6T) LAseaqis

‘(SOOZ) PAMISET pue PAOIZIS
“(9861) WTRd “(S00Z) PAPLA
pue yoysiey “(86 1) afnouruel

Lepidoptera. Chapter 11

aD “AS ‘OU
‘OZV-Ld ‘Ld “Td ‘AT
‘OISH LEAD AD

(UreqIg

easy)

‘A PEdO]
adAq)
‘jeotdonqns

‘(Z007Z) Ysqey pue Jowonpy (201 “39 Wd ‘Sa Md “Ad “ZO qeordorp)) snozoa (9981 ‘uorureag)
“(986T) F230 “(QEG[) AYsuaIq]] :9vd9"O,J) UTeIS por0IS ‘HO ‘Dd “AG ‘IV] 9D ‘9981 | cruasoiddéry] -tmeq| 9 | varuojvgdas valos07D
at snoseyd (€98T TATE)
(GPG) AOWISeIOr) “(€/G6]) UOIDT (strais ‘saAvaT) IONY WOON WA ‘Sa Sa ‘6P6I eisy| -oidyg] VY sypssaaddns 0714)
€D “MS ‘Ts “AS
‘NY ‘Su ‘OU “AVN
<Ld ‘Ld “Td ‘ON
LW AW ‘NT LT
(S007) PYADISeT pur PACIJIS OISsLl WVS-LE TI
“(EL6T) 19[89O¥ “(6861) NEYO pue “Al ‘OH “YH “AUO (purpsug
ypudiay “(C00Z) stay ‘(Z00Z) UD UD “AD UOO joodrsar]
yosuqey pure Journey “(9861) Udi Ud ‘Sd “Ad AITO]
JaIeOr) (6061) 2Yssniquios) TY KS) WD Aa odAq) | snoroa (LZ81 ‘wosSarry)
2d ‘(SZ61) MANpuse| | s8y ‘sutstes ‘sMsaz pot ‘Og “AG ‘VA ‘IV “IV! GD ‘IZ8T| uesoiddry] -nIneq| 5 yyaynsy vipyy
MS “AS “NU
(7761) HOkd “(S007) Eats] pue ‘OU “AVW-Ld “OZV
PAOLPS “(0661) YHAIPEY ‘(F007) cLd “Td “ON “IN
aidiunyey, pure seysnense ‘(//61) SAL LT AGF OISsEl
TYP “(S00Z) SI49>1 (S007) PIPIA “VS-LL LM “ala
pur yoysiey “($9G6T) ay[fnouruel “AMORNUD “UD “AD (PIpuy
‘(ZOOT) Psugqey pue Jowonyy ‘Ad ‘UOO Ud UW ‘AUTESO]
“(ZE61) Aeldyey “(O1GT) Supuy urea ‘simu ‘sammy ‘Td ‘SH “MC ‘ZO ‘AO oda) | snoseyd (€98T TATEX)
UOA “(9Q0Z) YOUsIeYy pur semMsy| polp :sionposg posoig L{| HD ‘D4 “Ad ‘LV “TV stuasoiddry| -oidyg} 9 VIJAINVI VAPV')
A3yUNOS
WUgey pure odoimq aSuri sated
SdDUIIIFOY ualTy | sernunos popeauy | ur proser,— | caneyy = | ouday | smeig Ayrore,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

650

(7761)

Oe “(€06T) sestedg ‘(S007)
BYADISLT PUP PAOTJIS ‘(8007)
PP “GC6T) wassorag “(ZZ61)
TYP ‘(S00Z) Stuy “(S00Z)
eMaLA pur yoysiey “(Z00Z)
yosuqey pur Jouronyy “(7€6T)

MS ‘IS

“as ‘NY ‘OU “GVW
Ld OZ Ed el
“Td ‘ON “IN (LW

MW ‘AT LT OISsLI
UVScLI “LI ‘ST “aI

aaldyny ‘(pp81) sdureypsu0T ‘NH “AYORAD UD (Auvurser)
-SATIPS 9] ‘(SQGT) OND PUENIED) ‘aD Ud ‘Td ‘Sa “AA ‘AqTeSOT
(9007) NoysIey pure semsy ‘O19 “uTeI3 SIC AC eZ OLAS adAq) | snoroa (96Z1 J9uqnH)
(9681) ‘Je 19 JousTYy-Yeqy | ‘sIMIj porsp ‘sinu pos01¢ HO ‘Dd “AG ‘IV “IV! AC ‘96Z1| euesoiddéry} -nIneq}| 5 yyjainja vissaydy
vopoury | snoseyd (6S81 OITEA)
(986[) Joqeo0ry ATID, dD ‘8961 yVoN| -oiyg] VW sypsaqygo wpiydopy
(8261 “zissesy)
Jeordoay, | snoseyd sypUudovjaul
(48261) ZIssesy squefd spenby dD ‘8261 -eisy| -oidyg) VW mig don
(9007) URWID] qy jeoidoay, | snoseyd ZIGI ‘uosdwepy
pure soqei, “(Z7861) ‘Te 39 [yng siueyd onenby | oo Tf ‘If €9 ‘AC *ZO}| (Id ‘8Z61 -eisy| -oidyg) y | ssuapuvue vpqdopy
(S007) snoseyd (O88 ‘uaTfaus)
"Te 39 Jowor) “(Z786T) “Te 39 [YN siueyd snenby| oorf ‘I{| IN “dD ‘Id “Md ‘ZO} Nd ‘8261 eisy| -oyd) WV syonpiip req doy
(6S81
(Z00Z) ‘Te 39 jepreds ‘(g00Z) Ld “IN ‘LW snoseyd TOTEM) syvsasarsad
WoeTINA\ pue snnyy ‘(ssard ut) [yng €q| ‘Tvgd-Sa ‘Sa ‘NG “Ad! Ld ‘0002 -oyg| VW sysnasdojdiq
(6S81
snoseyd Toyen) sywpadssad
(8007) Premuuey “(8007) Pa IN ‘WA “AG ‘HO] AC “2002 “oMyd) mpuvgavecy
A3yUNOS
Wgey pure odoinq aSuri sated
SIIMIIIFIY ualTy | seljunoos pepeauy | ur proses, | canenN = | sutdey | sme Ayrure,y

651

‘(SOOZ) BAMISLT pue PAOIZIS
‘(9861) “Ted “(ZZ61) THR “(EP6I
—TP61) repeWy “(700Z) PSUqeY

‘ATSNPUT d1e[OIO0YD

dS ‘ON “IN
ALOT LAA

(uede(
:AITEIO]

Lepidoptera. Chapter 11

pur Jouranyy (986) Joeor) Joy sinu jo syzodurt ur ‘a5 We Sig Ad adAq) | snoroa (ZZ81 JT[2Z,)
“(ZG61) TyounTy “(€Q6T) SUG Aq]| AT[eUOTsedD0 ‘syINIy AIG] ‘ZO ‘HD “Ad ‘IV I@G6I PIS AS} -BIeq| V stLvns vsdyvlny
Quejd33a) snoseyd (PC8T ‘oguanr))
(F007) 3S4N puasuojaue WnUuvIOS qq| ad ‘P00z voy] -oidyqg] YW | s7vuogso sapoutsnaT
(eolLFy pur
eisy :soidon
PHO PIO:
JEMEIES
PeISAPTR IAL
(0007) InNurUTeS :ANTEIO] (6S81
‘(COOZ) PIISIA pur qOYsieyy somnased ASSVW adj) | snoseyd TONE) SYVSISUDI
‘(900Z) HOYsTeY pur seMsy| ‘sossvss 41n3 ‘s1osoUOy “Ld ‘Ld ‘LIW ‘SH ‘AO] = AD “661 ) MuaBorddry] -orkyg) O vuLuvasojadsap]
(aeIayIonID) wngtusou1a eoloury | snoseyd E7T8T Touqny
(8661) J2vOF) pur ppng unipidaT ‘Beqqe) dD) dD ‘L661 -ouyg| Vv yyndnd vixtasngy
(8161)
AysmoqnZ-quioza1247 ‘(S00Z) MS ‘Is “AS
BYATIGET PUP PACIJIG “(9861) ‘Ad ‘Su “OU “AVN
wed “(ZZ61) THPW “(S00Z) suey Ld “OZV-1d ‘Ld
“(G00G) PHRTA PueaoysIEy “Td ‘ON “LW “AW
“(TS6T) 21Z9UrL “(ZOOT) YOsHIGeY AVL DISA Avs
pur rowanzy “(796T) Aq “LI ‘LI ‘SI ‘al ‘NH
(9861) ereOS) (S00) “Tee SOA A aS
PPPEPuaae[y ‘(906T) 2y8snsquio1+) “Wd ‘Id ‘Sd “ad AG (AarTes0]
2 ‘(Z€61) F10g “(IZ6T) MOd "19 “UTeI8 AW’ ZO 2925 odAa ou) | snoroa 681 PIIPZ
‘(Q00Z) ousTey pue remnsy ‘siMjj palrp ‘snu posoig ‘dg “Ad ‘Vd ‘LV “IV oruasoid AI) -TM1119C y pyjatugany vuysag dy
AxyunNOoS
Wgey pure odoimq aSuri satvads
S9IUIIIFIY ualTy | selunos pepeauy | ur proses, | caneN = | owidey | sme Ayrure,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

652

(esepeyy

‘uredg
:AN[EIO]
(Ld *Z007) addy) | snor0a (OZ8T “desurpneis)
(0002) ‘Te 39 Aa]10D gp EEA SAREE Od, Ld UD ‘Sa] ‘SA ‘OZ8T | 9uasoiddrD | -nIneq| O vung dvip vapahqy
6S81
snoseyd TOM Sypyoapod
(SOOZ) ‘Je 39 JoIVO4) syueyd onenby G5 6261) eiseyensny| -ovyg] Vv xulodviyg
voloury | snoseyd T88T 22045
(986T) Joxe0r) syueyd onenby qD ‘L961 YyVON| -oiyg| vy |syuenasqo xuhodvsyg
(EN
‘Ayeooy odAy
‘eOLpy pue (TS8I
RISY ‘Sq) | snoseyd TOT[OZ) syvsonjanyf
(9861) Joxv0r) syueyd onenby AD ‘6Z61 | uesoidAry} -ovfyg| 5D xudodvuy
(eoLFy pur
(ZOOZ) YOSHqRY eisy :soidon O88 I
pure Jowonz] ‘(CQ0Z) ‘fe 39 JayeOr) Pyiom pjo) | snoseyd UaTJaUsS syvinuLMUIp
‘(9861) POF “(Z786T) “TE 9 [YN Gq) Td NA ‘ZO ‘LV] =D ‘ZZ61) ouesorddrD] -or4yg} xudodving
feoidoay |snoseyd (6681 “¥TEA\)
(9861) JaIv0F siueyd snenby dD “6261 -eisy| -ouyg} | sywuostss xudodvurg
(8661) Ues|aIN Jeordoay | snoseyd 9/8] ‘UaTpous
pur qoysivy “(f86]) yooouepyy sjueyd onenby qs ‘qo ‘Ma! Na ‘s8Z6l -eisy| -oidyg) YW | syvauyig xutodvung
(€981
(886) easoIeUIdIT, voloury | snoseyd TONE) VIJaqIsun
‘(ZOOT) Psugqey pue Jouronyy suvpon[ LIV! Lv ‘0281 YON} -oyd) V stop ahumeny
AxyUNOS
yeNgey pure odoing aSuri sated
SIIUIIIFIY ualTy | selunoo pepeauy | ur proses, | ocanenN = | smiday | sme Ayrure,y

653

Lepidoptera. Chapter 11

(SCSI

snnIsay ZI snoseyd ‘Q]IAQUIJ\[-ULIONS))
(8007) Aemeig | ‘wasag ‘snsvy ‘snouan?)| “CD‘TD NH “TV4-Sa “Sa Sd ‘0061 eisy| -ouyd) Vv wusad vaviagiuy
oeprrumyes
88] ouosEYy
(1Z61) UPR pyaauytvdsas “dss
‘(Q861) WOssurds *(98G6]) Wye ssou 99q Ul qq eoIOUTy | snoroA (SO8T “preyorg)
‘(L00Z) FIOPTA pur Sroqimy] — spoorq ‘uaqod ‘Aouopy dS ‘ON ‘Td “NC “AC | “8.0761 29°] qUON | bed! V EE ea
POLY
pur voroury
‘ds snqjupiuy ynos
“ds vovjnquog “ds (IyeqUsTIC)
unipodouay’) “ds PIPUyT
vIso]a) “UnAgsvoVInIsod (sorreue7) :AVTTEOO]
(OLOZ ) SSN “(S007) BAPIA DULaYIUPIAT CVW-Ld ‘OZV| Woy) IN| 2442) ersy|snoseyd (SZLI ‘snorqes)
pure 3poysreyy “(G007Z) Sud °C ‘spavayna vag <Ld “IN ‘LI ‘NG “ad ‘8961 sidory,| -odyd] Y | syvadnsas vaprods
(zniZ) vues
“OpIIOUI |
:AITEIO] 1661 ‘ZaruYpS 29
(SOOT) INwIUTES “(€00Z) LW LW ‘€00Z adj) | snoseyd pepreds wnavjnsur
nUIWTeS “(ZQOZ) ‘Te 39 pneuday SISUALLDUDI X1UIOY J WI ‘NVO-SH ‘SH! “WA ‘Z00T | 2HUeSoidAID] -ok{yg] 5D sasqiuasvpnasy
€D “MS ‘Is “as “NU
(ZZ61) YPOZ “(S007) PANE] ‘OU “AVW-Ld “OZV
pure PAoes “(T061) [P9°u “(9861) <Ld ‘Ld “Id “ON
wed “(ZZ61) TW “(1661) URW “IN (LW IW “AW
(S003) SHSM ACO07) EIPEA- pue LAT LT Sia
youystey “(9261) SPISUIAT “(Z00Z) ‘NH “AYOAUD “UD
HeSHqP a PoE tren O61) ‘aD Ud ‘Td ‘Sa “Ad (Aare (E181 seuqnH)
AqnaH “(9861) 12805 “(ZE6T) “Id “ad ‘Z9 ‘HO adi ou)) snoroa yypenoundsaius
SI0g ‘(900Z) Yousiey pur semsy| sionposd yuejd paroig KI ‘OG ‘AG ‘IV ‘TV! ead ‘E181 | cuesoiddry| -ammeq} 5 DIDO
AxyUNOS
Wgey pure odoimq aSurs satvads
S9IUIIIFIY ualTy | selunos pepeauy | ur proses, | canenN = | owiday | sme Ayrure,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

654

(€S6T)

BIOM “(OTGT) weYsursyen, “(€00Z)
Yous ‘(CQOT) PITA pure yoysieyy
‘(9961) PuOUUR “(TQOZ) YoYsIEy

(vipuluinoD VSN)
suoneiuryd eurueq
DYNVEUIWS VILALASUBS
‘UoLpUuapoptg
wuviwyy “unsssvaddy
‘DIUOINAET “VIUIXO]L)
‘SNILY VIZIISUL0T
wigavquafjaig ‘snasiquy
‘spay aunhpsoy

‘(019 vasopavpulvy’))
SWI[e] ‘aVIIVIJIULOLT
‘paylauivonog viuosag

QVWsLd
‘OZV-Ld “Td “IN ‘LI
‘NH “UD “AD ‘NVO

pur ayipaesy “(€/6) rurjodurer) wudy vnk| oll “Sa ‘Sd “MC ‘ZO av snoseyd (9¢81 ‘telog)
‘(900Z) HoysTey pue remsy viziyaus vuanmd|) ITI] ‘HO‘Da ‘AG ‘TV| «Ld ‘OIGT] ery 'O} -oMyd| Vv 1unqoous vuox0dC)
(SOOT) PAISIA pure ioOYsIey SaSSOUT
“(L00Z) YOysresy pure ayxIpoery qm syuryd “(samy aS ‘AVWW-Ld GVW snoseyd (C68 ousday)
“(S00Z) 491909 “(Z661) ‘Te 39 [YN] ‘ures8) sionposd posorg| T{ZT‘II] ‘OZV-ld ‘Id ‘NC] “Ld ‘€Z61 vougy| -oyg) Vy | vdorsomo vuosodc
SepIoULy,
(7061) fend ‘(000)
addnissyaqry uasojorsidoprdaq
‘(€00Z) AUIS pur JoIsoy
(HSB T)FETON “(S00Z) SY sora SUCH PIO aP IS “LI ‘UH “UA svoeeue (ELT ‘Amiq)
‘(Z00Z) Yosuqey pue Jouronyy pean et go aie cee Ol ‘Sd “AC “HO ‘LV “TV eisy| -oud| WV viqquuls IMDS
(8002)

Avert “(ZOOZ) Ysuqey pue Is ‘Su (1981
Jowony ‘(GQ0Z) ‘Je 39 PPyapusarysy 019 VIUYISD) ‘OU NW {LI ‘NH Is snoseyd ‘QT]IAQUsJ[-Ulgn+))
“(ELGT) TRSED “(S6G6T) “TE 3 QFE | Sma ‘snpnosay ‘snsianC) ‘UH “AC ‘Vd “LV] “8981-9981 -oukyd| Yo | munud voviaqquy

AryUNOD
Wegey pure odoinq aSuri sated
SIIMIIIFIY ualTy | selunos pepeauy | ur proses, | eaneN | oudey | sme Ayrure,y

655

Lepidoptera. Chapter 11

(S007) PYANASET

PUR PAOIZIS (FOOT) USSSTIN Pur

uosioiag “(ZEG1) stuoreg ‘(S0G6I)
sapucy ‘(F0G61) SePUSV ‘(ZZ6T)

aD “MS

‘IS “AS ‘NY “OU ‘Ld
“Td ‘ON “IN ‘AT II
‘LI “AI “ST “NH “@D
‘Ad ‘WOO Ud UW

(edomy
‘APEdO]

[PW “(8661) YSPPIN pur yoysreyy ‘Td “Sa “Ad “Nd *ZO addi) ) snor0a (E781 ‘ourun}y)
(6961) AqnIH ‘(6061) Aysmouaiq | soyiopo ‘sionpoid paroig ‘HD ‘A “Dd “AD ‘LV AS ‘P6LT | oruesoiddry |} -nineq| 95 Myayyjassig vjoaul
ao)
MIS ‘Su ‘NY ‘OU “Ld
(ZOO) “Te 39 PYOL, “(S00Z) ‘ON ‘IT ‘AT ‘OISsLI
BYATISET PUL PAOITJIG “(766T) UVS-LI “LI “SI “NH
prdry “(SgG61) voruyO-weyjad YH “AYORAD UD (ueasryed
‘(€861) ESPpPly pue unsydo ‘aD ‘Ud ‘Sa NG -AW[eOO] | SNOIOA LI6I SPHA
“(€661) SEISULAT ‘(Z86T) ‘Te 2° [YN | soysoyps ‘sionpoid pazoig “Ad ‘ZO AD SIV “TV| «=MN ‘9S81| 244) eisy s| -aI0q] V SUIINJSUDAT VAULT
(€00Z) CUPIOY
SOA (6661) ‘Te 19 IPAOL “(S00T) MS “aS ‘NU
eyanageyT pure PAodag “(//61) ‘OU ‘ON “IN AT ‘LI (ROLOWY
TW “(866T) USPPIN Pur afoysreyy “AI ‘NH “dD “Ud ‘TA Ynog)| snoroa ISS “worurers
‘(C86[) JOWWY pur yIesp{ ysy Arp ‘sn Sd “Ad °ZD “Ad ‘LV Al ‘Orsi soidonosnN | -nINeq| VY pyaquaasayvd pauls
‘SIOOPUI puNnoy
uayjo ‘(wntpuadojoos
suhag ‘spu-xyyf (puryary
(800Z) qury “(LO0Z) Joysrey suagdotuq “winaafigas :AqTedOT | snoseyd (ZEG6L SAay[)
pure oyxIpsery ‘(QFG6]) euTIOg Ung IIISM]Og) SUIIT AI ‘6061| 241) eisy| -oidyg| yw | moazoyif saprogotsy
(2u0aT
PIIOIS
(SOOT) PAIOIA pure ioOYsIey :AITEIO] (€98I
‘(LO0Z) JoysIey] pure syIporry CVW-Ld CVW-Ld adAq) | snoroa TOA) Vjjasouoyv
‘(900Z) JousTey pue remsy UNIPIAAT “OZV-Ld ‘LW ‘AD | “6Z61 240F0q oruasoid AI 9q|) DO SIPIIWIVAT
A1yUNOD
WUgey pur odoimq aSuri sated
SIOUIIIFOY uslTy | saijUuNOd popeAaUy | UT pr0dar ,.| SATIeNT «= | SUITBay | snIVIS Ayrore,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

656

(SQOZ) PIIPTA (019 snoseyd (COST TOE)
pur yoysreyy (2966) zssesy) — ‘smpupy) snoseyddjog| ZI ‘TI OZVLd ‘€D] AD ‘TIGT) wsepensmy) -omyg) y | vuvszassod svdgdidq

(€O0TZ) CUSTOY] SOATA,
(6961) IURPD2T “(ZOOTZ) Yosuqey snoseyd 6961 ‘youoyeiq
pure owany “(8861) eW 2d snapay| TIED Ud ‘Od LV| «Ud “8961 vonyy| -oyd| V ppioipas vigourdy
Wd snoseyd 066I ‘Uoquieyy
(0661) ‘Je 39 Uogquiey) snapay) €r) WA | ‘0661-LSOd vouyy| -oidyg| VW stsuatsaayy pyourdy

(TZ6T) CF0TTeAe_) pure

woysuez ‘(C96T) ‘Te 39 uasasAyy,
(S007): 1 8 QPIBPUSAPLS) Su ‘ON (F981
(C961) =ePPP!A “(9Z61) SUE ‘OISSLI “UVS-LI “LI snoseud FEN) Cpe?
SeIPENC) SAATA pur Iepsa¢ eIso> | Aypeadsa ‘snoseyddAjog ‘45 Wi ‘Sa Na! Md ‘0961 -ouyg| WV sapoqstsog dy
Wi snoseyd (PZ6I1 ‘youoyeiq)
(1002) ‘Te 39 AqeJ SPA) UA | ‘1007-LSOd -ouyd| V POONA) RATT
U0I109 ‘SZUNUULOI (L761
(€86[) UouoasKy ‘(900Z) snuity vsoyfiusay snoseyd ‘yOLIAay]) Y4adqoonay
‘Je 19 Josinquiey ‘(6661) A2]pesg DIUMVPVIVIAT “SNLILD) WII Id ‘S961 -oyg| VW vigajgdoqdhay

syuryd snosoeqsoy
MOT Pur ‘SdTIIIQMess
(S007) ‘vutssayand CvVW voloury | snoseyd (098 ‘suswey)
Te 19 TTTH ‘“(Z661) Te 2 [yng vigsoydny ‘Snsq1’) -Ld ‘AD ‘Nada yVoN| -oiyg] VW vuvytsad sisday’y
(0061
LTX ‘ZI snoseyd “WIeYSUISTEA )
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IEPIOIIIIOT,
A3yUNOS

Wgey pure odoimq aSurs sated
SIIMIIIFIY ualTy | selunoos pepeauy | ur proses, | eaneN = | owidey | sme Ayrure,y

~ snoseyd LOOT ‘zZIssesy
6 (Z00Z) zissesy uMouyu) aD} gD ‘€o0z| euesoiddry| -oidyg] 9D putdoasad SDA
(2007) CVW-Ld ‘OZV
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(9007) ‘Te 39 OFuRsI ‘(S661) UD UD UOOM snoseyd (E81
ouyeAred) ap “(T00Z) ‘Te 39 [yng snaizy | OOLL ‘ZI Ud “Sa “NC “TV IT ALS “ody | YW | S4QN]TEJA) 24979 sly
(6661) ‘Te 39 FPOL, (6661)
epunyy pur fearpsayg “(C00Z)
BYATISET PUP PAOIJIG “(Z00Z) MS ‘IS “Td
yosiiqey pur Jowony ‘(f/61) avaoessoidny) Joy10 “IN ‘NH “Aad ‘ZD voloury | snoseyd (LZ81 ‘preyorg)
uozAnyuoyueny ‘(€861) SU 2 Aypeuotseooo ‘ving] ‘HO ‘Dd “AG SEV] «IN ‘TZ61 -oukyd| Vy | marys vigasauduy
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= (6661) ZIssesy sevaoessordn “All aD| dD ‘L661 yHON| -oiyd| V DyGasadday
V sepnnowouody
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vaomnys pure eursdns¢ “(7Z761) YOR
(6861) sepnossired4y “(1 007)
SODAOY] pue souurisosiey ‘(CQ0T)
PITTA pur yoysiey “(1S61) aD “MS ‘Is ‘nu
pizeurl “(€661) sPysutal “(Z00) ‘Su ‘OU ‘OZV-Ld
HUE a Ue AONE A6l} STW “AW ‘IT ‘OISsLI
[durery pue ApH ‘(S007) Te! UVSiLI CLI ‘NH “UD
PPPpurar[y ‘(0961) sueyNd (ne Ud ‘Sa ‘Nd “Ad ‘ZO snoseyd (9161 “Psng)
‘(€¥G61) oyalay -erorery zonsuywog | smu ‘SNUNAT) JCIDCSOY Z1| “HD “Dd ‘V" SLV “TV IS ‘OZ6I eISy -ouy V DISAJOUL YIN OY AVLL)
AxyUNOS
Wgey pure odoimq aSurs satvads
SOIMIIIFIY ualTy | selunoos pepeauy | ur proses, | oeanenN = | ouiday | sme Ayrure,y

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

658

TOUT

vISy pure volyy | snoseyd SCG FYoIOJ
(7661) Uossusag apaqna Unga N or adomy} -okyg DIJIUIULAA] DIULYITT
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snoseyd snyaqguapinbap
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sepriusuiiedy
snoseyd 6P8I IPZ
(SOOT) PIISIA, pur IOYsiey unipodouay) ‘xajdisip adoinyq) -o1dyg pyjainssaa pLogdoao’)
(1861) AyJsaour[ pur youdioy
“(ZO0Z) Yosuqey pue Jowonypy (AV ‘ZD | snoseyd OIGL ‘Pq
‘(‘urur09 ‘siad) auozzIpjeg vavatds MIS “AS ‘TT ‘LI ‘AH “Ad| ‘pur edomys| -o4yg yyjaavaids psoydoao’)
AS ‘Su ‘ON
(8S81) “IN “XI ‘AT SIT “al “UH Shoauad (ZL 8:0 Une)
24q 2 (9007) ‘Te 19 puog ‘aD ‘Id “Ad UH “Nd “Ad| sdpy ueedomy] -o1kyg yyjartsny vsoydoajor)
(9621 UqnH)
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‘ye 19 IEYOT “(GQOT) PIIA pur POLOWy

yoysiey “(Z7OOTZ) Yosuqey pue on YWON WoIZ| snoroA CI6I 3psng

Jaurany] ‘(8007) AUPUIZOL) Jeworeur yueyd Surkesaq

(S00) sHUPM “(ZOOT) YsUqeY
pure Jowonzy ‘(668 T) eUsOjOF

sudypol] pur ses[y

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vOLFY N 29
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SorsJUNOS poprauy oSurs SATIENT

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(8081 Z9uqnH)
DIOLUVI Dua
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A visy | snoseyd (6SZI1 SP22]D)
6 (900Z) ‘Je 39 sonboy StAgsays NUIT €r) al q orodomy} -okyg VIDANIY] VIABIVIAT
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snoseyd (68Z1 ‘SIT[LA 2d)
(L007) ‘Te 39 Jamey wniumsog 94 Aq| ueouesoupspy| -o01kyg | veevsstrmiunyd srqquvsinq
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sdty 01
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& (BYLT. Lao ‘snuyy) snoseyd (6SZ1 SPI2]D)
Ss (TZ61) HOM | Mag ‘snsdan?)) snoseyddjog Z1‘ID -o1dy viavyofap stuUnig
S snoseyd (QSZI ‘snoeuury)
ne (L681) EHOW SNUIT c5) -o1dy vuaviuid sypdng
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S (8781 “qaromepy)

(SOOT) PATSIA pur iOYsIey | sIaMOoP ‘spas ‘stdgsamgis vv
(Z00Z) ‘Te 39

Tyng ‘(€66T) ‘Te 39 UoyIOyNIINY
ura (6861) SU 9d

HH

snssaadn’yy ‘snaadiunf

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(6ST desurpneis)
myjaqamiquas VIY IAAL

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(S861) JUNE -siowyeyD

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snoseyd
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(P61 ‘“ssoqunyy)

VIJALINDXAS DIG ISAOSMAY’)

(PS81
JSBEEPS YOU ET)
Dy apimuvs sdILgqpy
depIYysa}er)
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Ayrurey

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

660

(S861) ‘ye 10 JOU

(S861) ‘ye 20 Jo

(SOOT) BYAMASET pur PAoIjag

sapiouvinyd Laay

snuvyy dopnasd say

vided subjont

CG!

CONTI

eo arall

dS “LT ‘AT “aD

MN ‘NU ‘OU “Td “AW “OIS
CLI LI ‘NH “WOON “UW
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JMS Jo odomnq

snoseyd
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snoseyd
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(QE6T ‘pueypIeW 27)
istuupol sagmsouoy hg
(PZ81

Jouosey) yyjajnsiuasd
Lag souoyyg

(9621 PuqnH)
pyauuadisos vy dOIv’)

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(€007) OUSIOVY SOATA,

‘(000Z) ‘Te 29 2381S “(T00Z)
eYANISe'] PUL PAOCTJIC ‘(/661)
yooeyy pure foaapyy “(F661) ‘Te
19 PYAMSET ‘(8GG1) BYlOS pur
rysmourqey ‘(CQOZ) Ussuaisiry
pure yoysiey “(Z700Z) yostqey
pure souranyy ‘(SQ0Z) ‘Te 29

snuvyy dopnasd say

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AS ‘ON ‘ATT

MN “MS ‘IS “AS
‘Su ‘AU SOU “Td “TN “LT ‘AT

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vyauuadyna vyisdojv’)

IH ‘(0007) euetseydng pue “LI ‘NH “UH “AD “WOO 9861
sult 9d ‘(Y66T) Jory pue |e Ud ‘Td “SH “MC “Ad *ZO sueyyeg | snoseyd ‘PUNT, 2g eYYOso
unng “(€007) ‘Te 39 [yng unursvroddig snjnasay) WI ‘TTX ‘TI ‘HO ‘Ad “Od “Ad “VE CLV uroyinog | -01k4d Ui fees LEI)

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(OP8T ‘TeAnpstog)

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(SOOT) PIISIA pur oysiey snqny OZV-Ld -ovdyg VIILND DIIUWBUYS

snoseyd (8781 ‘yIomep)

(9007) oYsIeyy pur remsy sn34anQ) | OIX'PD‘TD Sd “‘GVW-Ld -okyd| — ajardvoquay vyjausug

Oneupy) (6€61 Tuell)

(SO0Z) ‘Te 2° [TH JOUTU Jeo] xa77 snI4anC) es adomy ‘Ss VIJABULLIY VIWAPAOIIT

IIX TS SETH snoseyd] (PEGI “ZaMY-1]TNIN)

(F007) ‘Te 39 UsxFoYNOIN] ueA snuviyq) “Tl Wa} WOO Ud “UH ‘SH ‘HO sueyjeg J} -oyd suvynd staadiqvoy

seprpnondayy

vynqag (snuNAT ‘SNBVAIVA)

me ‘snglos ‘ns Snqvyyy) snoseyd (9€8T ‘e1S07) CO)

8 (900Z) Youssey pur Jemnsy | svaovsoy Apisour ‘snoseyddjog] 7D ‘TD ‘II uvourioupsyy| -oidyg}| wyjayofyvut viagdoonaT

SS sepmouo0ky
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sepiduiesoise |]

(9781

snoseyd IO[IZ) Vpjaqwjns1dgs

(S00Z) ‘Je 2° [TH DUDIUL SNUIYy -ovdy Lag LouoyyG

(9781

(SOOT) PIIIA pur yOYsreyy snoseyd TOJOZ) Upjazuvssaue

‘(900Z) YoysIey pue semsy VIUVISU) ‘sndvq ‘snILanC) -ovdy Lag souoyyg

WeIIgGey sated

SJoY uaTTV SoIIJUNOD popeauy aSuri sAneN Ayrure,y

depron

Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

662

adoiny S
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JE 19 TTOY “(Z9GT) sokowoH, ‘sajqeiosaa) snoseydéjog| ‘gt ‘94 ‘SA| -Sa ‘SH “MC “AC ‘HD “TV Jesrdonqng| -okyg sypiony viagdopods
ROLY
(SOOT) PIISIA pur yoOYsieyy AAS pue ‘AA | snoseyd (LZ ‘24AG232T)
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eISY (\ 01] snoseyd (Z8Z1 ‘snioriqe.q)
(8007) 2quIny wuniulgdaq qD “Ad ‘Mad “Aq| edomy Ag 2D) -o1dyg DIIUOUL DISMAGHG Of
(1861) MMA “(0007) POLY
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pure yzeaH ‘(6007Z) Yoog stavdoossasdn’y 01 Surpuedxa | snoseyd (6781 ‘feanpstog)
‘(6661) A°Jeg pur Paoupsag ‘stevdavulvy’) IN ‘AD ‘MC| Uvouesoupepy) -odyg tuatnvay aupydogitT
POLY N ‘eISV (SCZ ‘snoevuurT)
(SOOT) PIISIA pur IOYsreyy M X edoing vavdiany vixadnq
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(S007) EYANAgeT pure PAoras SdSNOYsse]s UT sapquiss3A, AS “Id ‘ZD| ueouruoupsyy| -oidyg} — sagiajpqa stxtaposhag’)
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(LS81
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(900Z) Joussey pur remnsy DIISSOAT pur onseoreg| -o1dyg} ‘snoeuury) adv stsarg
sepa
(SOOZ) PYAMISET pure PACES S]MAspoo}j polip MS “AS
‘(ZZ61) THPW ‘(0007Z) ‘Te 19] Sunsayuy ATperoodsa arour Inq ‘OU ‘Ld “Td “ON “IN ‘AT (G78 ‘uoruTelS)
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2 ‘(9681) ‘Je 29 yousry-yeqy SUIM JO SYIOO ‘sjadrey) ‘Tl “Ad ‘ZOD ‘HO Ad “AG ‘LV| éueoursoupeyy| = -0q DIJPAILIAVS SISOAPUT
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(Z6G61) ART pure souof (2e9980,J) N pur eisy | snoseyd (SCZ ‘snoevuurT)
‘(900Z) NoysIey pue remsy unoypayds unipodigomg q orodomy} -okyg VIAIBIV IDAVAD
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WeIIgGey sated
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Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

664

(SE61) YORTA

‘(6861) Youdiey “(9861) Wed
(6261) THAW “(Z007) WsUqrY
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pure ypouraas “(9861) Wed

soy ‘sinu ‘syIMIF pod

oryoeisid ‘qores ‘sinu ‘saxep

‘symmay Arp :sionposd paroig

MS “AS

‘OU ‘ON “IN “AI “AD ‘TA

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apiuoqwias stojahiody

(S007) PyAMAgET]

pue PAOLJOS ‘(SO0Z) eIIDIA pure
yoysiey “(/007) Je 29 TyNg
‘(900Z) oysrey pure em3y

(S007) ‘Te 3° HH

SpNpOl] Petoig

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CVW-Ld ‘OZV-Ld “Td “IN
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|
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(vaafyoVp Ef Pur sisuatAvUYI
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bal
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smnaq ‘(9007) ‘Te 2° [yng

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Apruasedde)
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adoiny 25

(uredg)
adomnyq A\S

spurysy
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ULSUPIIONPIAL

aSuvs sANeNy

snoseyd

-ovdy

snoseyd
-ovdy

snoseyd
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snoseyd
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snoseyd
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(68Z1 ‘UasneyyIog)

stuLsofavdoku
uopayupuls
(LOST ‘sordodseT)
SIULLOIDUBLPUD

uopayupuls
(LOST ‘sordodseT)

stuLdofanpy vigastuuay

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29 [10ry-nosodog)
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Carlos Lopez-Vaamonde et al. / BioRisk 4(2): 603-668 (2010)

666

‘viniag ‘snujy) snonpiosp (PEST “WWrIsI3[sOYy
pure (vsoy ‘snp ‘snuns) snoseyd UOA JOYOSI.J)
(€Z6T) ‘Je 39 Aa]pesrg ssa imay ‘snoseyddjog ral inne q5 adoinyq) -o1d4yg puvso satydoxopy
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SEPIIIVIOL,
(S007) PyADIgET XN “NS ‘TS
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pure uosurqoy “(ZE6T) STuoTed LT AT ‘NT SUVS-LI “AI “WH
“(E98 1) F49pT “(S00Z) “‘AMOND “AD UOO Ud WA
PIISTA pur yoysiey “(7961) ‘Td “Ad “NC “AC “ZO ‘AD SNOJOA (SCZ ‘snovuurT)
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668

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