Invasion of North American Forests
by European Phytophagous Insects
Legacy of the European crucible?
Pekka Niemelii and William J, Mattson
O
ver the last 500 years, nearly
2000 insects andlOOO weedy
plants have invaded North
America (Kim and McPheron 1993,
Sail~r 1983, Stuckey and Barkley
199t1). Many of these inadvertent
"immigrants have become serious agricultural or forest pests (Liebhold
et al. 1995, Wilson and Graham
1983), Kim and McPheron (1993)
calculated that 40% of the major
North American insect pests are of
exotic origin even though as a group
exotic insects constitute just 2 % of
the insect fauna. For example, Haack
and Mattson (1993) discovered that
alien, tree-feeding sawflies in North
America are more prone to cause
outbreaks than are the equivalent
native species. Questions about man,aging these introduced insect species
and concern about continued importation of new ones are timely because of the past severe and everspreading impacts of introduced
insect pests on North American forest ecosystems (Campbell and
Schlarhaum 1994, Liebhold et al.
1995). We have only begun to comprehend the manifold, often insidious effects of alien invaders on the
structure and functioning of the ecological systems (from ecosystems to
Pekka Niemela is a professor of forest
protection, Faculty of Forestry, University of Joensuu, FlN-80101 Joensuu,
Finland. William J. Mattson is chief
insect ecologist at the North Central
Forest Experiment Station, US Forest
Service, Pesticide Research Center,
Michigan State University, East Lansing, MI 48824.
November 1996
European biota may be
much better competitors,
especially under
disturbance and
fragmented conditions,
than their North
American counterparts
biomes) in their newly adopted
homes (D'Antonio and Vitousek
1992).
There has been rather substantial, but nonetheless pieccmcal~ research on general climatic and ecological factors influencing the
invasion success of exotic animals
and plants (Drake et al. 1989, Lodge
1993, Kim and McPheron 1993,
Mooney and Drake 1987, Wilson
and Graham 1983). Consequently,
no comprehensive theory of invasion ecology has emerged. However,
the developing theory of plant-herbivore interactions has greatly increased our understanding of the
role of host plants and host plant
communities in the structuring and
dynamics of forest insects (Price ct
al. 1991, Strong et a1, 1984), We
believe that this knowledge can be
applied to better understand some of
the critical ecological factors underpinning the success of immigrant
herbivorous insects. In this article,
we argue that ancient, fundamental
similarities in forest and faunal composition between North America and
Europe predispose the two continents to successful interchange of
their respective herbivores (Gibbs
and Wainhouse 1986) but that crucial historical, geological, and climatic differences may explain why
European forest insects have been
vastly more successful in invading
North American forests than the reverse.
The North American-European
insect trade imbalance
More than half of the 2000 immigrant insect species in the United
States and Canada are of western
pale arctic origin (i.e., European origin; Sailer 1983, Wheeler and Henry
1992). Of the nearly 400 immigrant
species that live on trees and shrubs
in North America, 75% are from
Europe (Mattson et al. 1994). This
high proportion of European-origin
insects is explained in part by the
high intensity of trade and human
dispersal between North America
and Europe (Lindroth 1957, Sailer
1983, Wheeler and Henry 1992),
The successful interchange of insects between these two areas is not
surprising because they are biogeographically similar (Graham 1993,
Rohrig and Ulrich 1991). One might
expect approximately equivalent
immigration in both directions, given
the heavy exchange of manufactured
goods, plant and animal products,
and people for the last 500 years.
The flux might even be biased toward greater numbers of North
741
American insects having been transported to Europe because of the longstanding and heavy flow of American raw and manufactured products
to Europe. During the seventeenth,
eighteenth, and nineteenth centuries
huge shipments of wood went to
western Europe due to wood crises
in these countries. Perlin (1989) reported that in 1770 alone, timber
and products from more than 3-1 ,000
American trees went just to England.
At the end of the nineteenth century,
the United Kingdom was buying
nearly half, and Germany one-quarter, of the total global export of
wood; their combined annual wood
consumption was 78 x 10 6 m} (Zan
1910). At least 20% of these imports
came from North America. Likewise, millions of nursery plants were
shipped to Europe (Spongberg 1990).
In addition, there was enormous
Europe-bound World War T and
World War II tonnage.
Although there has been widespread establishment in Europe of
exotic botanical gardens and forests
and woodlands comprising many
New World species (Heywood 1989,
Spongberg 1990), surveys of North
American and European forest entomologicalliterature show that more
phytophagous forest insects from
Europe have successfully invaded
North America (approximately 300)
than have invaded Europe from
North America (34; Mattson et a1.
1994).' Of these 34 North American
species (17 Homoptera, 15 Hyw
menoptera, 6 Lepidoptera, 4 Coleoptera, 1 Thysanoptera, and 1
Diptera), most have followed their
introduced North American host
plants, except for five broadly
polyphagous species.
The asymmetrical insect exchange
between North American and European forests is not unusual: Asymmetry apparently characterizes most
if not all biotic interchanges between
biogeographic provinces (Lodge
1993, Vermeij 1991). Vermeij (1991)
summarized four often cited hypotheses that may explain asymmetric
exchange:
• numbers of invaders going
in any direction are proporlW. J. Mattson and P. Niemela, 1996, manuscript in preparation.
742
Table 1. Estimated numbers of insects in the main phytophagous taxa of
}.~(Jrth
America and Europe.
North
American
Phytopbage group
specie~
European
speCIes
Coleoptera
23,640
10,000
732
900
1200
10,800
1324
8000
640
1000
300
1200
11,300
SOOO
1800
795
31
3
700
300
Diptera: Agromyzidac
Diptera: Cecidolllyiidae
HemipteralHomoptera
Hymenoptera: Cynipidae
Hymenoptera: Symphyta
Lepidoptera
Orthoptera
Phasmida
Thysanoptcra
tiona I to the size of conduits
for their passage;
• numbers of invaders reflect
fundamental differences in the
number of species available for
dispersal from the donor environment;
• numbers of successful invaders are determined by the
wealch of ecological opportunities for them on their arrival;
and
• invaders from one donor environment are intrinsically competitively superior to those from
the other donor environment.
The first hypothesis is difficult to
address because there is no easy way
to prove that differences in the volume of traffic in plants, plant products, and people between Europe
and North America a re at the root of
the whopping asymmetry (Simberloff
1989). Nevertheless, some argue that
the asymmetry might be due to a
lopsided movement of nursery plant
material to North America during
the early twentieth century (Wheeler
and Henry 1992). We dispense with
the second hypothesis because the
insect fauna of North America (north
of Mexico) and Europe are estimated
to be the same size (both approximately 100,000 species; Chinery
1993, Schaefer and Kosztarab 1991),
although overall insect species richness per 1000 km 2 (sr, = species/
area j D.25 ) is higher in Europe than in
References
Chinery 1993, Schaefer and Kosztarab 1991
Schaefer and Kosztarab 1991,
Thompson 1990
Skuhruva et at 1984
Chine,:' 1993, Sch<lefer and
Kosztarab 1991
A~kew 19R4,CTOuletandHubner 1993
GauldanuBolton 1988,Smith 197-""
1993
Chinery 1993, Schaefer and
Kosztarab 1991
Chinery 1993, Schaefer and
Kosztarab 1991
Chinery 1993, Schaefer and
Ko~:aarab 1991
Chinery 1993, Schaefer and
Kosztarab 1991
North America (1798 versus 1512),
because North America (north of
Mexico) has approximately twice
the surface area of Europe. In the
case of the primarily herbivorous
taxa, in fact, there are probably
20%-25% more species in North
America than in Europe (Table 1).
Therefore, simple difference", in size
of the donor pools of insect species
cannot account for the preponderance of European to North American transfers. The final two hypotheses (ecological opportunity and
competitive superiority) a re the richest and most likely explanations for
the asymmetry, and therefore we
consider them in detail below.
Different ecological
opportunities for immigrants
The topic of ecological opportunities for phytophagous insect immigrants is broad, encompassing such
concepts as host plant availability,
enemy-free space, competition-free
space, and bioclimatic conditions.
Host availability is especially crucial, and we discuss it first, using
some of the fundamentals of plancherbivore interaction theory.
Theory of herbivore species richness
on plants. The factors influencing
the total numbers of phytophagous
insect species attacking a single species or genus of plants within large
geographical regions are well undcrBioScience Vol. 46 No. 10
stood. For example, insect species
loading increases with both the size
of a plant's geographic range and its
average local ahundance within that
range (Neuvonen and Niemela 1981,
Strong et a1. 1984). Additional intrinsic plant characteristics, such as
size, structural complexity, and biochemical and spectral properties, also
explain much of the variation in
insect species diversity per plant
(Connor et al. 1980, Kennedy and
Southwood 1984, Stronget al. 1984).
Finally, one extrinsic factor, its
degree of taxonomic isolation, is
extremely important because plants
that have abundant close relatives
(confamilial, congeneric) generally
acquire more insect species than otherwise equivalent but taxonomically
(or chemically) isolated species
(Haack and Mattson 1993, Strong et
al. 1984, Tahvanainen and Niemela
19?7). This "system" variable is
important in explaining species richness of the more highly specialized
horhivores (Tahvanainen and )JiemeJa
1987) that have radiated on a given
taxonomic group of plants, because
the adoption of new host plants by
specialists is usually conservative
(i.e., they colonize new species that
resemble their old hosts; Farrell et
a1. 1992). This conservatism is due
to phylogenetic constraints in the
insect's host finding and selection
processes, oviposition, feeding and
digestive processes, and also to factors extrinsic to but correlated with
the host plant, such as natural enemies and its physical environmental preferences (Futuyma 1991).
If one turns this system of knowledge around and examines it from
the viewpoint of invading herbivorous insects, then the probability of
being a successful colonizer is a function of these same factors! size of the
areal distributions of all potential
host plants (primarily congeneric,
and secondarilyconfamilial, species);
their average numerical abundance
in their areas of distribution; their
biochemical, anatomical, and ecological similarity to the native hosts;
and the invading insect's initiating
and concluding feeding on the new
host at exactly the right time (i.e.,
host synchrony; Quiring 1992).
Potential host plants in North
America. The long-standing, close
November 1996
Table 2. Extant North American species of woudy plant genera that went
extinct in Europe during the Pleistocene
(Little 1979, Sauer 1988).
Genera
Extant species
GYlllnospenn<;
Chamaccyparis
Sequoia
faxodium
Thuja
T orreya
Tsuga
Angiosperms
Asimina
Carya
Diospyros
Lindera
Liquidambar
Lirodendron
Magnolia
Morus
Nyssa
P~rsea
Robinia
Sahal
Sapindus
Sassafras
3
1
2
2
2
4
3
11
2
2
1
1
8
2
3
1
4
1
2
1
taxonomic affinity between European and North American flora
(Rohrig and Ulrich 1991), which
were once part of a giant landmass
(Graham 1993), should make insect
exchange between rhe two continents highly successful. However, at
least three factors make North
American forests more suitable for,
and hence more vulnerable to, immigrant European species than vice
versa-their larger number of potential host plants (marc congeneric
and confamilial species than in
Europe), their higher absolute abundance, and their more even, less fragmented distribution. Several European species, especially conifers,
have extremely small, rclictual distributions (Jalas andSuominen 1973)
in the mountains and islands of southern Europe.
At a total flora level, North
America north of Mexico has approximately 50% marc vascular
plant species than Europe (approximately 18,000 versus 12,000; Blarney
and Grey-Wilson 1989, Graham
1993). Narrowing the focus to just
trees (woody species that attain more
than 2 m in height) at comparahle
latitudes in North America north of
Mexico (excluding Florida) and Europe. there are two- to threefold
more gymnosperm genera (16 versus
8) and species (97 versus 30) in North
America than in Europe, and twofold more angiosperm genera (143
versus 78) and spcl.:ies (503 versus
256;. Huntley 1993, Little 1979,
Rohng 1991). North American conifer genera are clearly much more
speciose than the same European
genera (6.06 versus 3.75 species/genus), whereas North American angiosperm genera are only slightly
more speciose (3.52 versus 3.28 species/genus; Huntley 1993). Comparing just eastern deciduous forest regions of the United States to the
ecologically comparable central Europe, Ellenberg (1988) estimated a
twofold difference in the number of
gymnosperm and angiosperm tree
species (18 gymnosperm species in
the United States regions versus 8 in
central Europe, and 106 versus 45
angiosperm species),
The most common explanation
for these differences in plant richness is the higher rate of extinctions
in Europe (Table 2). Frequent tree
extinctions have taken place since
the late Tertiary period, when the
Alps and other mountains were
formed (Sauer 1988), and during the
Pleistocene, when the climate was
more severe and droughty and a much
smaller total area was available for
refugia (Huntley 1993, Rohrig 1991).
Another potential explanation is that
the current differences in species richness between North America and
Europe are caused largely by recent
climatic and soil factors (Adams and
Woodward 1989, Currie 1991).
European and North American
forests still share most of the same
dominant tree genera. Seven 'of
Europe's 8 gymnosperm genera and
37 of its 78 angiosperm genera arc
shared in common with North
America (Huntley 1993). Only 3 million years ago the two continents
were even more similar floristically,
when they shared at least 13 gymnosperm and 52 angiosperm tree genera. Despite these similarities, approximately 20 important tree genera
have gone extinct in Europe but not
North America (Table 2). As a result, many mono- and oligophagous
European insect species undoubtedly
went extinct (as did tree-feeding
mammoths, Mammuthus meridionalis), along \\'ith their host plants
{e.g., Carya, Liriodendron, Robinia,
743
Table 3. Forest and woodland cover in coastal regions of Europe and North
America (Aarne 1993, Lowe et al. 1992, Smith ct al. 1994, Zon 1910).
European forests are simpler and
more fragmented. In spite of theif
many common dominant tree genPercentage
Percentage woodera, the ecological structure of forwoodland cover Percentage woodland land in conifersests in North America and Europe is
Geographic area
-1910
cover-l99Os
1990s
different (Ellenberg 1988, MonkAtlantic Europe
14
31
34
konen and Welsh 1993, Rohrig and
Baltic Europe
43
50
85
Ulrich 1991). Since the Pleistocene,
Mediterranean Europe
23
32
20
European
forest cover has been less
Atlantic United States
56
66
.17
extensive, less diverse, and much
Atlantic Canada
52
77
73
more fragmented (Ellenberg 19S9,
Great Lakes United States
29
36
19
Great Lakes Canada
46
86
63
Huntley 1993, Monkkonen and
Pacific United States
37
38
91
Welsh 1993).111 the last 6000 years,
Pacific Canada
75
65
93
waves of human empires moving ever
northward and westward have
Taxodium, Thuja, and Tsuga, to insects are genera also commonly steadily increased this tendency,
name a few).
occurring in Europe: Prunus > Malus clearing the forests until widespread
Other insects \vere undoubtedly > Betula >Popuius > Salix> Pinus> and severe wood shortages abounded
able to survive by adopting hardier, Quercus> Pyrus > Crataegus > Acer (Perlin 1989, Ponting 1991). For
close confamilial relatives. If such > Ulmus> Alnus· > Picea.
example, approximately 2000 years
host-switching survivors exist, they
On the other hand, the least com- ago, during the Roman empire, many
may yet retain the genetic capacity mon hosts in North America are forest~rich regions such as I\vorth
to recolonize their former pre- Pleis- invariably genera that are not natu- Africa, Cypress, and southern Italy
tocene host plant genera if given the rally represented in Europe (e.g., were permanently transformed into
opportunity. In addition, they may Carya, Chamaecyparis, Robinia, virtually treeless landscapes (less
have the behavioral and physiologi- Pseudotsuga, Thuja, and Tsuga). than 10% ofthe original forests from
cal flexibility to adopt even more, They have been colonized exclusively Morocco to Afghanistan exist todifferent new hosts. By contrast, by oligophagous (six) and polypha- day), while parts of France, Gerequivalent mono- and oligophagous gous (six) species. Although most many, southern England, and Spain
insects on these same "extinct" gen- such "new" hosts (with the excep- became tree-poor landscapes. This
era in North America were not faced tion of Pseudotsuga) formerly oc- pattern continued relentlessly, so that
with the same pressure to adopt new curred in Europe~ each has acquired by 1300 less than 20% of the origihosts during the Pleistocene and in~ only one to three European colonists nal forests of central and western
stead may have even further special- (Mattson et al. 1994). This supports Europe remained (Panting 1991). It
ized, so as to be even less capable of the contention that phytophagc es- finally ended in the middle of the
switching to confamilial plants ex- tablishment in a new environment nineteenth century, when reforestatant in Europe. Therefore, many depends on an abundance of ances- tion became substantive. European
European insects may have a broader tral (congeneric, confamilial) host ecosystems clearly have had a longer
capacity to accommodate to new material. Hence, European insects history of severe human intervenhosts than is evident from their cur- entering North America \-vould be tion, being much more intensively
rent host range in Europe (du Merle more likely to be successful than harvested, manipulated, and manet at. 1992, Roques 1988), and many North American insects entering aged than North American ecosysAmerican insects on genera such as Europe.
tems. The result has been the fragCarya, Liriodendron, MoTUs, Robinia,
The majority of insects invading mentation of European forests into
and others that no longer exist in North American forests have, in fact, small parcels that are low in
Europe may have virtually no pos- been rather diet specialized, con- phytodiversity, often being evensibility of finding a suitable host trary to expectation. For example, aged, mono- and olign-dominant
there.
68% of the European invaders are cultures, an-d are relegated to the
mono- or oligophagous (Mattson et poorest soils andlor microclimates
European aliens adopted close rela- a1. 1994). Even more interesting is (Ellenberg 1988, Ledig 1992).
tives of European hosts. Insects colo- that the introduced European inConsequently, since the time of
nizing a new geographic area are sects have been able to colonize new the first European contact with North
presented with unique opportunities congeneric plants even though such America, most of the coastal nations
to acquire new host plant taxa. Yet American species diverged from their of Europe (except Sweden and Finthe majority of European species in common ancestral Euramerican root land) have had a low percentage of
North America have colonized the stocks more than 38 million years forest cover, ranging between just
same tree genera that they use in ago (Graham 1993, Rohrig 1991). 4% and 26% at the beginning of this
Europe (Mattson et al. 1994, Millions of years of independent century (Table 3). Remarkable efWheeler and Henry 1992). For ex- evolution have not caused the plant forts at rdorestation in the pa~t 150
ample, the 13 most common hosts in species to diverge so far from one years have increased forest cover
North America (ranked according another that they were unrecogniz- substantially. It nm.v ranges from
to their total adventives) for alien able by immigrant inseds.
9% to 51 %, although for most na744
BioScience Vol. 46 No.1 0
tions, forest cover is still less than
35% (Table 3). By contrast, in the
Atlantic coastal United States, forest cover ranges from 31 %-89%l
with only three states being under
59% (Table 3; Smirh et al. 1994). In
the Great Lakes states, forest cover
ranges from 12%-59%, with only
two states below 30%. In the Pacific
states, forest cover ranges from 35 %48%. In coastal Canada, it is even
higher, ranging between 60% and
85% among the various provinces,
with the mean forest cover being
73% on the Atlantic coast and 65%
on the Pacific coast (Table 3).
We hypothesize that as a result of
lower forest cover levels in Europe,
it may have been difficult for North
American insect immigrants arriving in the smaller, isolated, and usuaIry conifer-dominated forest pockets of Europe to quickly discover
suitable host food and cover, and to
rapIdly build and sustain their populations. The opposite is probably
true for European insect immigrants
arriving in North American coastal
areas.
Abundant European weeds in North
America. Most of the 2000 weeds in
North America originated in the Old
World (Stuckey and Barkley 1993).
Heywood (1989) reported that 881
introduced plants are established in
Canada, mostly from Europe,
amounting to 28% of the size of its
native flora. Similarly, 20%-36%
of the flora of the northeastern United
States is introduced (Stuckey and
Barkley 1993). On the other hand,
in northern Europe the percentage
of introduced plants is low, only
between 10% and 15% of the size of
native flora (Heywood 1989). The
presence of such a bundant aliens in
North America is most apparent
during early succession, when they
make up 30%-60% of. the plant
species composition for the first two
decades following disturbance
(Rejmanek 1989).
The importance of alien weeJs to
the success of immigrant forest insects is as yet unmeasured, but they
could be important because many
insects (moths, butterflies, beetles,
flies, aphids, plant bugs) often feed
as adults or juveniles on the pollen,
nectar, and sap of weeJs before ovipositing nn their main woody plant
November 1996
host. If European insect aliens were
to need such maturational, sustenance feeding, they might be likely
to find a weed they recognize in
North America. On the other hand,
the same may not be true for a North
American alien entering Europe.
The recent successful entry of
Tomicus piniperda, a European bark
beetle, into the lower Great Lakes
region of North America illustrates
this principle, although its hosts for
maturational feeding are not technically weeds. Its invasion was undoubtedly enhanced by the abundance of scotch pine (Pinus sylvestris)
Christmas trees (its most common
natural host) and Austrian pine
(Pinus nigra), ornamentals that the
young adult beetles attack for maturation feeding in shoots in the summer. If there had been no scotch or
Austrian pine near the beetles' ports
of entry, their invasion might have
been stopped.
genera per family in North America
than in Europe, one might predict
that insect species loading would be
similar in the two continents or even
slightly higher in North America
(Fernandes 1992, Huntley 1993,
Little 1979).
The limited data do not bear out
this prediction. For example, Strong
et a1. (1984) found that the cosmopolitan bracken fern (Pteridium
aquilinum) has nearly four times as
many consumers in Britain as in
New Mexico (27 versus 7 species))
although the environments are not
equivalent. Zwolfer (1988) discovered that Nearetic thistles have a
much smaller and less diverse insect
fauna than do European thistles.
Likewise, Hendrix et a1. (1988) found
that the ahundance of arthropods on
early successional herbaceous vegetation was several-fold greater in
southern England than in Towa, although they did not enumerate speciosity per se. With respect to trees,
Evans (1987) found that Sitka spruce
(Picea sitchensis), naturalized in Britain, has more species of acquired
phytophagous insects than in its native North America (90 versus 59).
Likewise, the phytophage loading on
Betula pubescens in northern
Fennoscandia is higher than that of
Betula glandulosa in Labrador and
northern Quebec (approximately 100
versus 30-40 insect specics).2 Looking at a specific organ such as pine
cones, the number of cone specialists on Pinus sytlJestris in France (811) is higher than on a comparable
species, Pinus resinosa, in northeastern North America (5-8; Katovich et al. 1989, Roques 1988).
With respect to Fennoscandian
woody plants, Neuvonen and
Niemela (1983) reported that there
were on average nearly five species
of sawfly per plant species, whereas
Haack and Mattson (1993) found
that North American woody plants
averaged approximately only one
sawfly species per plant species. Likewise, comparing sawfly species loading on woody genera in Great Britain with the same genera from
northeastern North America (Figure
1) shows that there are on average
Native insect loading per plant. The
effect of native competitors on the
colonization of plants by immigrants
is largely unknown. But we raise the
issue here, despite the dearth of hard
data, by examining the number of
insect species typically found on
American and European plantsusually called insect species loading
(Strong et al. 1984).
Baseline estimates of insect loaJing on equivalent plants in different
parts of the world are not available.
Dividing the total number of species
of phytophagous insects in Europe
(approximately 32,000) and North
America (approximately 43,000) by
the number of vascular plants in the
respective continents (approximately
12,000 and 18,000), yields approxi·
mately 2.7 and 2.4 insect species,
respectively, per plant species. However, few insects specialize on just
one plant species. Even the more
specialized monophagous feeders
tend to be able to feed on congeneric
species. IIence, the more speciose a
plant genus, the more "specialist"
herbivores its congeneric species are
likely to share, all else being equal.
Oligophagous insects tend to be capable of colonizing confamilial genera, and polyphagous species can
generally colonize plants from many IS. Koponen, 1995, personal communication.
different families. Because there are Zoological Mllsellm, University of Turku,
more species per tree genus and more Turku, Finland.
745
Figure 1. Insect loading in Britain and
eastern North America. The number of
sawfly species on 14 woody plant genera in both Great Britain and the northeastern United States was plotted against
the numb..:r of plant species in each
genus, As an example, the data for
willows (Salix) are shown for each of
the two geographic regions. The lines
represent a log model fit to the data (Y b
= 5,55 + 21.19 log Xb, r = 0.81 for
British data, and Ya = -1.88 + 10,53 log
X.' r = 0.70 for US data). Data derived
from Gauld and Bolton (1988), Haack
and Mattson (1993), and Little (1979).
pation, this could make it more difficult for a North American invader
to colonize European trees. More
significanrly, if higher insect species
loading led to more intense competition in the evolutionary past of European phytophages, then these insects might be more adept than
equivalent North American species
at exploiting their essential resources
and hence at invading. So goes the
argument explaining that competition-steeled continental fauna invaria bly overwhelm the naive, less tightly
integrated, and generalist fauna of
islands (Huston 1994).
Enemy-free space. To understand
whether there mav be differences in
the background ievels of parasites
and predators confronting aliens that
enter either European or Korth
American forests~ we compare natural ent:my levels in both conrincnt<;.
Mills (1992) assessed the parasitoid
guild structure of 43 :K'earctic and
several-fold more sawfly species per 50 Palearctic species of tortricoid
'plant species in Britain.
moths and concluded that they were
Because there are as yet no com- remarkably similar (7.8 and 6.7 parapletely equivalent data for the other sites species per host for Nearetie
groups of herbivores (e.g., aphids and Palearetic, respectively). Hawand lepidopterans), it is not possible kins (1990) made a more general
to say unequivm.:ally that European survey assessing numbers of parasiwoody plants have higher loading of toid species per host insect species in
all herbivore species. However, us- six different herbivore guild classes
ing eastern Canadian Forest Insect in the Nearctic and in the north
and Disease Survey (FIDS) data on 9 Palearctic (largely Britain). His respecies of trees and data on more sults are in accord with those of
than 28 British tree species from .Mills (1992), showing that regardKennedy and Southwood (1984), we less of herbi vore guild class, parasite
plotted and regressed the numbers loading was not significantly differof micro lepidopteran species on the ent between the two regions. On the
numbt:rs of macrolepidoptt:rans per other hand, at a contint:nt-wide level,
host plant (Figure 2) to compare the there are approximately twice as
relative species abundances of these many described s.pecies of parasitic
major folivores. The regressions were and predaceous Hymenoptera in
nonlinear for British and linear for Europe than in North America (apCanadian data, with the latter fall- proximately 35,000 versus 15,000;
ing generally below tht: former, sug- Chinery 1993, Schader and Koszgesting that British trees have higher tarab 1991). However. caution in
loadings of both kinds of lepidopter- drawing firm conclusions is advised
ans. The results are strengthened hy hecause full biological inventories
the fact that the Canadian data cover of the Insecta of the two regions
a much larger area; individual tree have not yet been rendered.
populations spanning more than
It is not easy to dirt:ctly compare
2000 km east to west and at least bird predation pressure facing phy600 km north to south.
tophagous insects in North America
These preliminary data indicate and Europe because songhird densithat insect species loading may be ties vary substantially by forest cover
generally higher on European plants. type and by season. However,
If higher species loading translates Monkkonen and Helle (\989) reto higher average phytophage occu- ported that breeding bird densities
746
i,
j
,~
!
'"
.
@
0
Cl.Bc,"'-,n
~c",,,,,,,,,
"
~
~
.
.--6
,.~~.
..
., ~
•
•
~
--c
•
0
00
150
Figure 2. Insect loading in Great Britain
and Canada. The number of microlepidopteran species \vas plotted against
the number of macrolepidopteran species on more than 28 British and 9
Canadian species of trees. As an exampJe, the data for birches (Betula) arc
shown for each of the two geographic
regions. The lint!~ rt:pn.~st!UL a nonlinear
model fit to the data (Y b = 7.31 + O. 92X o
- O.0023Xu2, r = 0.91) fur Brinsh dara,
and a linear fit (Yo = -2.21 + O.713X" r
= 0.96) for Canadian data. Data derived
from Kennedy and Southwood (1984),
and Canadian Forest Service, Fore~t
Insect and Disease Survey, Petawawa
National Research Institute.
in eastern North American forests
are approximately 25%-50% higher
than in equivalent fores.ts of Europe
(4.5-5.5 versus 3.0-4.5 pairs/hal,
and the densities are even higher in
western North America. Howevn,
it is possible that wintering bird densities are higher in European forests,
putting more predation pressure on
overwintering insect stages .
The evidence suggests, then, thaI
natural enemy pressures facing phytophagous insects in North America
and Europe are probably equivalent, although more exacting and
comprehensive studies are badly
needed. However, even if enemy
pressures are nearly equivalent, one
can still question whether North
American and European insects differ somehow in their innate defenses
against natural enemies, thereby giving one or the other critical advantage when faced ,"vith sil11ilar enemy
pressure in a new environment.
Was Europe a crucible selecting
for disturbance specialists?
It is generally agreed that European
insects (and plants) have been more
successful at invading other regions
of the world than insects (and plants)
from other regIOns have been at in-
BioScience Vol. 46 No. 10
vading Europe (see D'Antonio and
Vitousek 1992, di Castri 1989,
Simberloff 1989). However, there is
no agreement about the underlying
explanation. We address here elements of the fourth hypothesis (i.e.,
competitive superiority) for explaining the exchange asymmetry and
argue that European biota may be
much better competitors, especially
under disturbance and fragmented
conditions, than their North American counterparts. As a result, European immigrants are able to replace
them (Lattin and Oman 1983, Lindroth 1957, Niemela and Spence 1991 ).
Although there are no hard data
demonstrating displacement of
North American forest insects, circumstantial evidence unequivocally
suggests that many European adventives have become the overwhelming dominant, phytophagous insects
in icheir invaded North American
niches. For example, four species of
European sawfly leafminers (Mattson et a1. 1994) have established
themselves on Betula papyrifera in
North America and seem now to be
the dominant folivores over much of
the natural range of this transcontinental tree, except for the far Northwest."' Likewise, the European gypsy
moth (Lymantriadispar) has become
the dominant spring folivore in
northeastern American mixed oak
forests, as have the Eurasian larch
sawfly (Pristiphora erichsonii) and
the larch casebearer (Coleophora
laricella) on eastern larch (Larix
laricina), and the introduced pine
sawfly (Diprion simi/is) on eastern
white pine (Pinus strobus; Liebhold
et a1. 1995), This "hostile takeover"
phenomenon seems to hold also for
a plethora of European plants (Brown
et al. 1987, D'Antonio and Vitousek
1992, di Castri 1989, Heywood
1989, Rejmanek 1989) and also for
European earthworms on North
American glaciated soils, except for
the far Northwest (Hendrix 1995).
Repeated, long-term selection for
aggressive competitive and co]onizing ability. In speculating about reasons for the apparent superiority of
Eurasian organisms in invading other
'J.
Spence, 1995, personal communication.
Biology Department, University of Albt'rta,
Edmontun, CalJada,
November 1996
regions, di Castri (1989) argued that
the roots of this phenomena are
embedded in their catastrophic evolutionary history. Since the Alps were
formed, European biota have been
more severely impacted than other
biota by the cyclical, severe climate
changes driven by the earth's regular
orbital fluctuations (Webb and
Bartlein 1992). For example, the
impact of the several Pleistocene glaciations was much more severe in
Europe than elsewhere because this
continent's unique flanking, eastwest mountain chains from the
Caucasus to the Pyrenees supported
southern glaciers and ice sheets, both
of which diminished the total area
for biota to retreat in front of the
glacial advances and were, moreover, important determinants of an
arid climate in southern and central
Europe (Huntley 1993). At each glacial maximum, the cold, dry, windy
climates eliminated continuous forest cover north of the mountain
chain. South of it, aridity was the
barrier, thus forcing horeal and temperate trees to persist as small populations in many s.patially restricted,
widely scattered midslope mountain
refugia in southern Europe (Huntley
1993, Webb and Bartlein 1992). Such
repeated diminution, fractionation,
and mixing of the woody flora and
fauna caused many extinctions (e.g.,
of forest-dwelling mammoths), but
it also led to speciation opportunities (e.g., of steppe-dwelling, grassfeeding woolly mammoths) among
certain predisposed taxa (Baccetti
1987, Chinery and Cuisin 1994,
Huntley 1993, Vrba 1992).
furthermore, since the retreat of
the last glaciers, but especially during the last 6000 years, humans have
created another crucible of selection
pressures in Europe because their
populations have been large and their
technologies capable of drastically
disrupting, and even wholly eliminating, many ecosystems. Humans
in Europe have radically changed
the entire natural face of their own
continent as well as the rest of the
world (Ellenberg 1988, Monkkonen
and Welsh 1993, Perlin 1989). This
was achieved by anthropogenically
aided invasion of exotic organisms
from the East and Middle East; by
relentless, widespread harvesting;
and by elimination of forests for
settlements, heating, metal and pitch
extraction, manufacturing, grazing,
agriculture, ship building, and wars
(di Castri 1989, Heywood 1989,Jahn
1991, Ledig 1992). Not just the forests, but even the soils supporting
them, have been severely degraded
(Ellenberg 1988, Jahn 1991, Ledig
1992).
Thus, since the end of the
Pliocence, roughly 3 million years
ago, forest cover and composition
have been highly volatile, alternately
contracting to form serpentine necklaces of small refugia, expanding
with global climatic cycles, and finally retreating almost steadily during the last six millennia. Instead of
selection for traits that were adaptive in expansive, species-rich forests, there was selection for suites of
traits having survival value in patchy,
highly fragmented, impoverished
forests: high behavioral, morphological, and physiological plasticity;
uniparental reproduction; larger reproductive potentials; auto- and
alloploidy; strong dispersal capabilities; highly efficacious protection
from competitors and natural enemies; and special stress tolerance
mechanisms, such as extended dormancies (D'Antonio and Vitousek
1992, Lodge 1993, Monkkonen and
Welsh 1993).
The long-distance movements and
commingling of biota caused by habitat disturbances during and after the
Pleistocene were crucibles for triggering increased speciation (Vrba
1992). Besides allopatric speciation,
the movements and commingling
probably incited heightened sympatric speciation opportunities among
insects, who were driven to experiment with new hosts and then diverged on them due to host-induced
isolation, as can occur in leaf- and
treehoppers (Bush 1994, Wood et a1.
1990). Shifting distributions and
commingling may also have spurred
the emergence of novel uniparental
taxa from bisexual taxa, either
though hyhridization (and subsequent backcrossing), which gave rise
to the chance emergence of parthenogenetic hybrid females, or through
the spontaneous emergence of parthenogenetic lines from unfertilized
eggs (Sullini and Nascetti 1990).
Uniparental reproduction (e.g.!
selfing as in mother-SOIl and sibling
747
•
40000
tion, it has 14% of the world's Ylallophaga fcather lice, a mostly
Oil/lera
• 8.rooean SPeCies
nonparrhenogenetic group. Dolling
10000
0 N.American SPeCies
(1991) likewise noted rhar the BritVa- 0.12
ish Isles have roughly 2% of all the
'1',.- O,070X
Symphyla
various world groups of Hemiptera,
AphidO,dea.
as is also true for all Insecta (Chinerv
~
CoocONlea
1000
,;;
1993), but is vastly overrepresented
0Ila8°;·
0
00
(500 species) in Aphidoidea, having
11 % of the world's nearly 4400 speCynipini.
hl
cies!
North America, by contrast,
();
0
100
has approximately 12% of the
0
world's Insecta in all the same taxa,
0
Iii
even the parthenogenetic ones. T\vo
0
exceptions are the Aphidoidea and
the Cynipidae, of which it has 34%
10
and 50% of the known <;pecies. Oaks
100
1000
10000
100000 400000
are one of the most important hosr
I\1..rnber of species in world
plants on which cynipids have radiated,
and Korth America has fiveFigure 3. Insect species abundance in Europe and North America. The number of
species (Y) in the main taxa (i.e., orders) of insects in Europe and North America fold more oak species than does
was plott~d (on log-log scales) against the total number of known species in each Europe (58 versus 10-12 species;
taxon (X) in the world. Parthenogenetic insect orders and subgroups are identified Little 1979).
by their names. For the Hymenoptera, data for their continent and world totals
Polyploidy and parthenogenesis
do flbt include their named subgroups. Two lines are shown, each representing a often occur in tandem, apparently
distinct but hypothetically constant relationship between the mean proportion of conferring unusual competitive suceach of the world's taxa in Europe (Yo = 0.07 X) and North America (Y. = 0.12
X), and the total number of organisms in these taxa in the world, facilitating cess on their carriers~ most of which
perception of outliers. Data derived from sources in Table 1-Arnett (1993), are widespread or nearly cosmopoliBlackman and Eastop (1994), Chinery and Cuisin (1994), Dolling (1991), Kozar tan (Bullini and Nascetti 1990,
Lanteri and Normark 1995, Suoand Drozdjak (1986), and Kosztarab et al. (1990).
malainen et a1. 1976). In Europe, the
bisexual, diploid progenitors of many
matings, and various kinds of par- normally rare. For example, at least curculionid weevils and bagworm
thenogenesis) can be a powerful ad- 100 species of European Curculio- moths have remained localized in
aptation (Craig and Mopper 1993) nidea and several bagworm moths the regions of their ancient glacial
because, among other things, it al- (Psychidae) are parthenogenetic refugia, whereas their parthenogelows continued propagation even at (Bullini and Naseetti 1990, Lanteri netic, polyploid derivatives have
low population levels, such as are and Normark 1995, Suomalainen et expanded into the recently ice-free
typical both in small refugia and in a1. 1976). Moreover, in those groups areas (Suomalainen et a1. 1976). Not
colonizing episodes. Moreover, itcan in which parthenogenesis is gener- surprisingly, Lindroth (1957} and
increase mean reproductive poten- ally the norm throughout the world Suomalainen et a1. (1976) noted that
tial per unit of resource and thus (e.g., Hymenoptera, Aphidoidea), at least 13 of these same weevils
increases rapid exploitation possi- there seem~ to he greater species (e.g., Otiorrhynchus spp. and
bilities when ephemerally favorable richness in Europe than would be Po/ydrosus spp.) and two bagworms
conditions arise. It may also strongly expected (Figure 3). Europe gener- have also been uncommon Iv sucpromote further rapid adaptation and ally has approximately 7% of the cessful at invading North A~erica,
speciation (i.e., novel clonal lines) world's species in most of the major probably because of both their unithrough random mutations (Ledig orders of Insecta (Figure 3), but has parental reproduction and broader
1992, Norris 1992).
substantially higher percentages ecological amplitudes derived from
If the European crucible selected among the groups that are wholly or their polyploidy and high heterozyfor uniparental reproduction because partially parthenogenetic (except for gosity due to apomixis (Bullini and
of its manifold advantages, there the Thysanoptera). For example, Nascctti 1990). Lanteri and Normark
should he a high representation of among the wholly parthenogenetic (1995) noted the same adventive
organisms with uniparental repro- taxa, Europe has approximately 36% success in North America for parduction strategies among European of the known Aphidoidea, 32% of thenogenetic weevils from South
biota. In fact, parthenogenesis is the parasitic and predaceolls Hy- America. The most successful adunusually common in several groups menoptera, 20% of the Cynipidae, ventives on ~orth American woody
of European plants (e.g.,Hieraceum, and 15% of the world's Syrnphyta. plants (Table 4) arc the coccoid scales
Rubus, Sorb us, and Taraxacum; Among the partially parthenogenetic (45 species), which, although priBlarney Grey-Wilson 1989, Huntley groups, it has approximately 11 % marily biparental, are renowned for
1993), as well as in some beetles and of the known Coccoidca, and 13% their seven different kinds of parthemoths in which parthenogenesis IS of the Diptera. Contrary to expecta- nogenesis and the most diverse cluo-
!l
0
ymenop aTa
•
til
•
•
-
•
•• •
~
748
BioScience Vol. 46 No.1 0
rnosome system in any animal group
(Kosztarab 1987).
In another highly successful adventive group, the scolytid beetles,
Atkinson et a1. (1990) confirmed
that most of the 33 introduced species (of which 8 are from Europe) in
North America are habitually inbreeding, facultative parthenogenetics {i.e., in which unfertilized
and fertilized eggs yield males Ithat
mate with mother andlor sister] and
females, respectively}, although little
is known about their ploidy and
heterozygosity. Such a breeding system can lead to the emergence of
many new "clones" perpetuated by
the daughters (Norris 1992). Of the
60 mostly European sawflies in
North America (34 on woody plants),
all afe parthenogenetic (several being thelytokus, or obligatory) and at
least one, Diprion similis, is also
apparently polyploid (Kneter 1993,
Smhh 1993). Even some of the most
notoriuusly successful European
weeds (e.g., Taraxacum and Hieracium) in North America are either
parthenogenetic and/or polyploid
(Hamet-Ahti et al. 1984, Stebbins
1993). Although the advantages derived from uniparental propagation
and/or heterosis arc important and
can help explain the success of many
of the dominating adventive taxa, as
they do for many invertebrates in
Hawaii (Simberloff 1989), they do
not appear to account for the succesS
of leafhoppers, plant bugs, and tortricid moths (Table 4).
Defenses against natural enemies.
Other important adaptations that
may have been forged in the European crucible for enhancing: survival
in small refugia, and in small invasive colonies, are potent defenses
against likely natural enemies-such
as the toxic alkaloids produced by
symbiotic fungal endophytes in the
most widespread European grass in
North America, tall fescue (Festuca
arundinacea, Ball et a1. 1993) and in
other alien grasses, such as Lolium
spp. Alternatively, their greater capacity for tolerating high predation,
such as is the case of many European
grasses in western North America
and elsewhere, may have enhanced
the ability of European plants to
invade North America (D' Antunio
and Vitousek 1992). Unfortunately,
November 1996
Table 4. ~umbers of immigrant insects in the eight dominant taxa (constituting
66% of all known aclventives in North America) on woody plants in North
America and the estimated percentage of parthenugenetic species in each. Data
derived from Mattson ct a1. {1994} and Wheeler and Henry (1992).
Dominant taxa
Number
~cales (Coccoidea:1
Leaf boppers (Cicadellidlle)
Sawflies (Symphyta)
Bark beetles (Scolytidae)
Weevils (Curculionidae)
Plant bugs (Miridae)
Moths (Tortricidae)
Aphids (Aphidoidea)
45
more than 50
o
37
1UO
34
33
29
26
more than 65
more than 50
o
o
25
100
23
we know of no rigorous comparative studies of the kinds and efficacies of defenses that American and
European plants employ against their
phytophages. Nor have there been
comparative studies of the inherent
defenses of American and European
phytophages against their respective
predators and parasites. Such information is needed to resolve the question of whether European insects are
more successful in North America
than l\~orth American insects in Europe because the former are substantially more effective than the latter
at escaping from and defending
against natural enemies in theif new
environments.
High to low latitude
insect transfers
One other very crucial trait of successful colonizers is the capacity for
rapid and perfect synchronization of
the invader's life cycle with that of
the new environment because its
close phenological synchrony with
its newly adopted hosts is vitally
important (Quiring 1992), as is its
entering and terminating diapause
(or dormancy) at the appropriate
times so as to be physiologically
capable of coping with its new local
climatic extremes (Danks 1987,
Tauber et al. 1986).
Tracking photoperiod. Owing to the
vast differences in the latitudes of
the deciduous forests of Europe {approximately 43°_60° N} and North
America (30 -48° N; Figure 4), and
the fact that photoperiod is the major stimulus for inducing and also
for breaking hibernal diapause in
arthropods (Danks 1987, Tauber et
al. 1986), we hypothesize that in0
Percent parthenogenetic
sects going from Europe to North
America are better adapted for getting into environmental synchrony
than vice versa.
For many insects, critical photoperiod (P), the range of daylight
hours (or conversely darkness hours)
that can trigger diapause induction,
varies positively and linearly with
the latitude of population origin
(Danks 1987, Knerer 1993, Tauber
et aJ. 1986). For each ten degrees of
latitude, P" increases by approximately 1.2-1.6 hours. Consequently,
insects coming from 50" N latitude
would be triggered into hibernal diapause by a wider range of day lengths
(P < x + 1.4 hrs) than would an
in~ect coming from 40" N latitude
(Pc < x hrs). Transferring a northern
insect southward would probably
not limit its diapause induction because the southern daylength will
almost certainly be short enough to
trigger diapause (Table 5). Transfer
from south to north may, by contrast, fail because it is likely that day
length will be too long at the insect's
sensitive stage to trigger diapause.
Timely termination of diapause is
also crucial, because the insect must
~,--------
,~~--~~~--~~--~~
Jw
"'."
.....
""-->
-"
~~r
'"'"
<;"pt
O<;;t
Figure 4. The number of hours of daylight at selected latitudes in the North-
ern Hemisphere during the monthsJanuary to October. Data from Eckert and
Clemence (1962).
749
emerge at exactly the right time to
begin feeding on its host plant. If
insects respond to increasing day
length for triggering the terminatiun
of diapause, northern insects diapausing in a more southerly latitude
(where winter days are longer) would
be prone to break diapause early
because of thelr habituation to short
winter days. The opposite would
probably be the case for southern
insects transplanted to more northern latitudes, causing them to emerge
too late for optimal success on their
host plants. For most vernal phytophagous insects, the maxim is it
is ahvay,s better to be early than
late. 4
Tracking host plant physiology. Tn
addition to responding to photoperiod and temperature, another means
for finely tuning synchronization
with/novel host plants and environments is to directly "read" and respond to signals derived from the
plant itself. This approach may he
much more certain than relying solely
on external cues. For example, insects that insert their overwintering
eggs into living plant tissues may be
better able to finely track their host
plant's condition by using and responding to the normal fluxes of
plant water, nutrients, and hormones
in these tissues (Wood et at. 1990).
Wood et a!. (1990) reported that
when treehoppers \-vere forced to
oviposit in novel plants, the eggs
hatched in relation to the phenology
of the adopted rather than the parental host. As plant tissues dehydrate and prepare physiologically
for winter in the late summer, so too
can the eggs. In the late winter and
spring, when the tissues hydrate, the
eggs can begin preparing for emergence.
Hence, synchronization with a
new environment is likely to be more
certain for insects transferring from
high to lower latitudes, and especially so for insects that also have
direct means for sensing host physiological status, such as is true for
endophytic ovipositors. This may
help to explain the remarkable success of two taxa, cicadellid leafhoppers and mirid plant bugs (family
--- - - - -
---~-----
4W. J. Mattson, H. Piene, E. Fuhrer, and D.
Quiring, 1996, manuscript in preparation.
750
Table 5. Consequences of changing photoperiods on the timely induction and
rermination of hibernal diapause.
Summertime consequences
Wintl:r/spring consequences
Latitudinal transfer types
Daylight (Pl Oiapause
exposure
initiation
Daylight (P)
exposure
Higher to low!:r latitudes
P,,,,,, < Pulu
Lower
lO
higher latitudes
Pold
Yes, if development
is not cunailed
l'new ;..
Maybe-if
PH"" < PulJ
p "OW < P«;"",1
Miridae; Table 4), most of which are
endophytic ovipositors (Wheeler and
Henry 1992, Wood et al. 1990)~
Many plant bugs have yet another
useful trait because more than half
(14) of the European adventives are
both predaceous and/or phytophagous (Wheeler and Henry 1992),
making food finding more likely.
There is no direct evidence that
European more than American immigrants successfully enter hibernal
diapause in late summer, but there is
some evidence showing the former's
propensity for propitious diapause
termination. For example, the European species Tomicus piniperda is
perhaps the first scolytid beetle to
emerge in Great Lakes forests (as it
is in Europe) each spring (Haack and
Lawrence 1995). This gives it tremendous advantages in colonizing
the usually scarce, weakened pines
for breeding and egg laying. It may,
in fact, eventually displace the early
spring native beetle, Ips pini (Haack
and Lawrence 1995). The notoriously successful European gypsy
moth, L. dispar~ is also an early
spring insect that tends to emerge in
close synchrony with the bud break
of its favored hosts, the red oak
gcoup (Stoyenoff et al. 1994)~ Likewise, Illost of the members of the
largest group of adventive lepidopterans, the family Tortricidae (Table
5), arc early spring feeders. Two
European thrips that have been particularly damaging in northeastern
American forests are among the first
thrips to colonize the breaking buds
of their hosts, which they do substantially ahead of the native American thrips and ahead of their natural
synchrony with their native host
plants (Raffa et a1. 1992). European
invaders may be more sensitive to
heat sum accumulations in the lare
winter and spring and hence emerge
Uiapause
termination
likely to
he earlier
Ye~,
Likely to be
later
earlier on average than their American ecological counterparts.
Conclusions
To be a successful immigrant herbivorous species is, first and foremost, a function of the ready availability of potential host plants in the
new environment. Potential hosts
must be sufficiently abundant and
closely related taxonomically to ancestral hosts. for these reasons,
North America and Europe are particularly predisposed to one another's
herbivore invaders. The continents
have had similar flora and fauna for
millions of years, owing to their
similar climates and ancient land
bridges. However, North America
has more than twice as many species
and genera of trees (north of 35- N
latitude) than comparable areas of
Europe because many shared genera
became extinct in Europe just before
and during the Pleistocene. Furthermore, the absolute tree abundance
per unit area in North America is at
least twice that in Europe because
Europe has had substantially higher
human populations densities since
the close of the Pleistocene. Moreover, there are more European weeds
in the American landscape than vice
versa. These disparities all enabled
easier colonization of North America
by European insects than the converse, especially for specialized herbivores. Data clearly indicate that
North American tree genera that
have close relatives in Europe (or
other parts of world, as well) have
an increased risk of recruiting immigrant European insect herbivores.
Nevertheless, insects' adoption of
other North American trees remains
possible (especially for polyphages,
such as gvpsy moths and thrips).
Beyond the question of host avail-
BioScience \'01. 46 No. 10
ability, the herbivore's intrinsic capacides for survival and reproduction in the new environment are
crucial. Particularly important may
be the innate predisposition for immediately synchronizing with new
host plants, entering overwintering
conditions soon enough, and breaking dormancy or diapause in a timely
manner so as to be consistently in a
competitive position for occupation
of the new host plants. European
insects may have a fortuitous advantage because high latitude-adapted
insects are inherently more likely
successfully to transfer and to adapt
to mid- to low-latitude light and
temperature regimes than low latitude-adapted insects are to adjust to
high-latitude regimes.
Long-term survival of an immigrant herbivore ultimately depends
on its capacity to reproduce under
low population levels. One efficacious breeding system is uniparental
propagation (e.g., facultative and
obligatory parthenogenesis, and
selfing via polygynous inbreeding),
which is highly adaptive because it
permits small populations to quickly
expand and efficiently exploit
ephemeral resources. Typically
linked to an organism's breeding
system is its genetic endowment,
which in turn leads to a particular
genotype by environmental consequences ..For example, obligatory
parthenogenesis often is linked to
polyploidy and high heterozygosity
(facilitated by apomixis), which can
confer broad ecological tolerances
for coping with new and different
living conditions. These traits are
more common among European than
American phytophagous insects. It
is no coincidence that approximately
40% of all insects adventive on
American woody plants have parthenogenetic capabilities, four times
its estimated representation (11 %)
among native phytophagous taxa in
North America.
Many European organisms appear to be uniquely superior in their
capacity for colonizing disturbed
systems (compared with their ecological analogues elsewhere), probably due to the severe, repeated selection pressures for ruderal (capacity
for inhabiting disturbed habitats)
traits since the end of the Pliocene.
Furthermore, if insect species loadNovemher 1996
ing is truly higher on European plants
(as might be expected if their flora is
50% smaller in terms of species but
their phytophagous fauna is reduced
to a lesser extent [approximately
25%]), then European phytophages
may have been subjected to much
higher interspecific competition for
hundreds of thousands oEyears. As a
result, European phytophagous insects may he more specialized for
sequestering crucial resources (even
though potentially more "polyphagous"), and better able to compete,
than ecologically equivalent American phytophages. This is the same
argument often used to explain the
takeover of loosely packed island
ecosystems by adventive, continental hiota.
The risk of continued immigration of new insects into North
America remains high, especially
from the massive movement of living or freshly cut plant materials
such as nursery stock and whole logs
from similar biogeographical realms
such as South Temperate, North
Temperate, and boreal forested regions. A dangerously high fraction
of the successful colonists poses a
serious threat to the vitality, biodiversity, and stability of North American forests. The rapid, near-wholesale decimation of American elms
(Ulmus americanum) in cities and
forests of eastern North America in
the last 50 years .is the most recent,
dramatic reminder of the economic
and ecological havoc wrought by the
coupled invasion of European
bark beetles and a virulent Eurasian
pathogen. Although the front lines
of this disaster are no longer evident
to most, the evolutionary battle is
not yet over. If one looks closely,
one can see isolated skirmishes quietly playing out: the sudden midsummer wilting death of an isolated
elm and the decaying elm skeletons
still standing at the fringes of lowlands and farm woodlots.
In most cases, the impacts of immigrant insects are less rapid and
much less clear cut. Although they
are highly significant, they are typically and inextricably confounded
with other stresses, such as drought,
native disease pathogens, and pollution. For example, have the recent
drought-precipitated losses of paper
birches in the Great Lakes forests
and cities been accelerated by nearly
annual infestations of European
leafminers? What is more, have the
lcafmincrs also deterred birch's normal regeneration? Have the alarming death and deterioration of the fir
forests in the Appalachians been
heightened through the combined
impacts of the European balsam
woolly adelgid (Adelges piceae) and
acidic deposition? Have natural succession and the composition of eastern American oak forests been significantly and forever altered due to
chronic, heightened defoliation by
the gypsy moth? What are the longterm prospects for American beech
(Fagus grandifolia) as the European
beech bark scale (Cryptococcus
fagisuga) spreads westward, given
its synergistic potential for destruction when coupled to the native plant
pathogens Neetria coccinea and
Armillariella mellea? What is the
likelihood for restoring the place of
the overlumbered white pine (Pinus
strobus) in eastern American forests, given its high susceptibility to
the combined impacts of two alien
phytophages (the introduced pine
sawfly and the Asian rust pathogen
[Cronartium ribicola]) and another
new, chronic debilitant, the omnipresent air pollutant ozone?
And the list goes on, the tip of the
proverbial iceberg of global ecological questions for which we may never
have answers or solutions. Since the
dawn of civilization, humans have
been altering the world's ecological
systems faster than our abilities to
know the ecosystems. Making the
situation even more desperate, the pace
of change has been inexorably
ratcheting upward due to ever-burgeoning world populations (e.g.,
doubling twice in the twentieth century), while international economic
resolve to study them has been plummeting in parallel. However, when
the outrageous economic and ecological costs of the wanton spread of
existing exotics and continued entry
of new ones become common knowledge, it is inevitable that there will
be a public outcry for action to mitigate the potentially dire consequences. This will call for significant new research, innovative
preventative and remedial exotic
management, and certainly heightened international quarantine ef-
751
forts. Because the impacts of exotic
biota in a neVi' environment can
mushroom like a new, runaway pestilence, stopping them sooner rather
than later is always advisable.
Acknowledgments
The authors sincerely thank the following individuals for helpful discussions, for collecting reference
materials, and for generously providing constructive, insightful reviews of earlier versions of this manuscript: E. Fuhrer, R. Haack,]. Kouki,
J. Niemela, S. Kopanen, S. Neuvonen, P. Price, D. Quiring, :M.
Rous}, and J. Spence. The authors
also thank Stephen D'Eon of the
Canadian Forest Service, Forest Insect and Disease Survey Division at
the Petawawa National Forestry Institute, for generously compiling data
about ,the phytophagous insects
found ,on nine species of trees in
eastern Canada.
Refer~nces cited
Aarne M, ed. 1993. Yearbook of forest statistics, 1992. Helsinki (finland): FinnishForest
Research lnstimte.
Adams JM, Woodward FI. 1989. Patterns in
tree species richness as a test of glacial
cxtinction hypothesis. Nature 339: 699-701.
Arnett RH. J 993. American insects, a handbook of the ime,:ts of America north of
Mexico. GaineSVIlle (fL): The Sandhill Crane
Press.
Askew RR. 1984. The biology of gall wasps.
Pages 223-2 71 in Ananthakrishnan Th, ed.
Biology of gall insects. London (UK): Edward Arnold.
Atkinson TH, Rabaglia RJ, Bright DE. 1990.
Newly detected exotic species of Xyleborus
(Coleoptera: Scolytidae) with a revised key
to species in eastern Noeth Ameri(:a. Canadian Entomologist 122: 93-1 04.
Baccctri B, cd. 1987. Evolutionary biology of
orthopteroid insects. Chichester (UK): Ellis
Horwood Ltd.
Ball OM, Pedersen).", LacefIeld GV. 1993. The
tall-fescue endophyte. American Scientist
81:370-380.
Blackman RL, Eastop VP. 1994. Aphids on the
world's trees. an identification and information guide. Wallingford (UK): CAB International.
Blamey M, Grey-Wilson C. 1989. The illustrated flora of Britain and northern Europe.
London (UK): Hodder & StOllghton.
Brown VK, Hendrix SD,Dingle H.1987. Plants
and insects in early old-field succession: comparison of an English site and an American
site. BiologicalJournal of the Linnean Sociely 31: 59-74.
Bullini L, Na.~cetti G. 1990. Speciation by hybridization in phaslTlids alld other insects.
CanadianJournal ofZuologr 68: 1747-1760.
Bush GL 1994. Sympatric speciation in ani-
752
mals: new wine in old bottles. Trends in
Ecology and Evolution 9: 285-288.
Camphell IT, Schlarhaum SE. 1994. Fading
forests: North American tree.s and the threat
of exotic pests. Washington (DC): Natural
Resources Defense Council.
Chinery M. 1993. rnse<:ts of Blitain aud llorthern
Europe. London (UK): W. Collins Sons & Co.
Chincry M, Cuisin L. 19~4.Lespapillonsd'Europe.
Paris (france): Debcbaux et Niestle.
COllilOC EF, Faeth SH, SimberloffD, Dpler PA.
1980. T axonom1c Isolation and thc accumularion of herbivorous insects; a comparison
of introduced and lIative trees. Ecological
E.ntomology 5: 205-211.
Craig TP, Mopper S. 1993. Sex ratio variatinn
in sawflies. Pages 6 J -92 in Wagner M, Raffa
KF, cds. Sawfly life history adaptations to
woody plants. New York: Academic Press.
Currie D.I. 1~91. Energy and large-scale patterns of animal and plant species richness.
American Naturalist 137: 27-49.
D'AntonioCM, Vitousek PM. 1992. Binlogical
invasions by exotic grasses, the grassifire
cycle, and global change. Annual Review of
Ecology and Systematics 23: 63-~7.
Danks HV. 1987. Insect dormancy: an ecological perspective. J\.1onogcaph Serin 1. Ottawa (Canada): Biological Survey Canadian.
di Castei F. 1989. History nf biological invasion
with special emphasis on the Old World.
Pages 1-30 in Drake JA, Mooney HA, di
Castri F, Groves RH, Kruger fJ, Rejmanek
M, V:'illiamsonM, eds. Biological invasions:
a global perspectiw, New Yurk: John Wiley
&Snns.
Dolling \VR.. 1991. The Hemiptera. Oxford
(UK): Oxford University Press.
Drake JA, Mooney HA, di Castri F, Groves RH,
Kruger FJ, Rcjmanek M, WilliamsonM,eds.
1989. Biological invilsions: a globa I perspective. New York: John Wiley & Sum.
du MerlcP,Bcunct5, Cornic]E 1992. Polyphagous potentialities of Choristoneura
murinana (Hb.) (Lept. Tortricidae): a
monophagons foli vore extending its host
range. Journal of Applied Entomolgy 113:
18-40.
Eckert W}, Clemence GM. 1962. Tabb of
sunrisc, sunsCt, and twilight. Washington
(DC): US Gnvecnment Printing Office.
ElIenb",rg H. 1988. Vegetation ecology of central Europe. Cambridge (UK): Cambridge
University Press.
Evans HF. 1987. Sitka spruce insects: past,
present and futuee. Proceedings of the Royal
So(;icty of Edinbuegh 93B: 157-167.
.Farrell BD,Mitrer C, Futuyma DJ. 1992. Diversification at the insect-plant interface: insights
fcom phylogenetics. BioScience 42: 34-42.
Fernandes CW. 1992.1'lant family size and age
effects on insular gall-forming species richness. Global Ecology and Biogeogr~phical
Letters 2: 71-75.
Futuyma V J. 1991. EVDlution of host specificity
in herhivorous in~('cts: genetic, ecnlogical,
and phylogenetic aspects. Pages 431-454 in
Price PW, LewinsoJm TM, Fernandes GW,
Benson WW, eds. PI.mt-animal interactions:
evolutionary ecology in tropical and temperate regions. New York: John Wiley &
Sons.
Gauld I, Bolton B,ed~. 1 988. TbeHymenoptera.
Oxford (UK): Oxford University Press.
GibbsJN, Wainhouse D. 1986. Spread of forest
pests and pathogens in the northern hemi-
sphere. Forestry S9: 142-153.
Goulet H, HllberJT. 1993. Hymenoptera of the
world: an identification guide to families.
Publication nr 1894E. Ottawa (Canada):
Agriculture Canada.
Graham A. 1993. History of the vegetation:
Cretaceou; (Maa,trichtian)-·[·ertiary. Pages
57-70 in flora of North Americ:l Committee, eds. Flora of North AIll&;rit·a north of
Mexico. Vol. I. "Kew York: Oxford University Press.
Haack RA,Lawrence RK. 1995. Spring flight of
Tomicus piniperda in relation to nativc
Michigan pin&; bark beetles and their associated predators. Pages 524-511" in Hain FP,
Salnm SM, Ravlin WF, Payne TL, Ra£faKF,
cds. Behavior, population dynamics and contro! of forest insects. Columbus (OH): Ohio
~tate University.
Hrlack RA, Mattson W. 1993. J.ifc history patterns among North American tree-feeding
sawflies. Pages 503-541" in Wagner MR,
Raffa KF, eds. Sawtly life history adaptions
to woody plants. Boca Raton (FL); Academic Press.
Hamet-Ahti L,Suominenl, Hlvinen I, Dotila P,
Vuokko S. 1984. SllOltleIl Rctkcilykasvio.
Helsinki (Finland): Suomen Luonnnllsunjeiun
Tuki.
Hawkins BA. 1990. Global patterns of parasitoid assemblage size. J oumal of Animal Ecology 59: 57-72.
Hendrix PJ, ed. 1995. Earthworm ecology and
biogeography inNorth Arneri(a. Boca Raton
(FL): Lewis Publishers.
Hendrix SD, Brown VK, Dingk H. 1988. Arthropod guild strUl-'1ure dudn~early old field
succession in a new and old "World site.
Journal of Animal Ecology 57: 1053-1065.
HeywoodVII. 1989. Pilttern~,extcntsandmodes
of invasions by tenestrial plants. Pages 3160 in Drake JA, .:\!looney HA, di Castri r,
Groves RH, Kruger FJ, Rejmanek M,
\l:'illimllson M_ eds. Biologi(al inva~ions: a
global perspective. New York: John Wiley
& Sons.
Huntley B. 199.1. Species-richness in north· temperate zone forests. Jouenal of Biogeographr20: 163-180.
HustnIl MA. 1994. Biolngical diversity: the coexistence of species on changing lanJs(apt's.
Cambridge (UK): Cambridge University Press.
Jahn C. 1991. Tcmperate deciduous forest of
Europe. Pages .177-S02 in Roh rig F., Ulrich E,
eds. Ecosystems ofthe world. Vol. 7. Temperate deciduous forests. New York: Elsevier.
]alas J, Suominen .1, eds. 197.1. Atb .. florae
Europaeae, distribution of vascular plants in
Europe. Vol. 2. Gymnospermae (Pinaceat' to
Ephedraccac). Hclskinki (Finbnd): Committee for Mapping the Flora of Europe.
Katovich SA, Overton RP, Rush PA, Kulman
HM. 1989. R&;d-pine wnclet conc and seed
losses to insects and other factors in an opcngrown plantation and a seed on-hard.Forest
Ecology and Management 29: 115-1.11.
KennedyCEJ,Southwood TRE.1984. Thl;'llUIIlber of species of insects as~ociated with
British trees: fl. rhI11a lysis. JOllrnal of Animal
Ecology 53:455--478.
Kim KC, McPheron BA. 1993. Insect pests and
evolurinn. Page.q 3-25 in Kim KC,McPheron
BA, eds. Evolution of insect Pl;'st·s: patterns
ofvariatinn. New York: John Wiley & Snns.
Kncrcr G. 1993. Life history diversity in sawflies. Pages 33.-S9 in Wagner M, Raffa KF,
BioScience Vol. 46 No. 10
eds. Sawfly life history adaptations to woody
plants. New York: Academic Press.
Kosztarab,.M. 1987. Everything unique or unusual about scale insects (Homoptera:
Coccoidae). Bulletin of the Entomological
Society of America 33: 215-220.
Kosztarab M, O'Brien LB, Stoetzel ME, Dietz L,
Freytag PH. 1990. Problems and needs in the
study of I fomDptera in NorthAmerica. Pages
119-145 inKosztarabM,SchaeferCW,eds.
Systematics of the North American insects
and arachnids: status and need~. Virgina
Agricultural Experiment Station Information Series 90-1. Blacksburg (VA): Virginia
Polytechnic Institute and State University.
K07.ar F, Dro7.djak J. 1986. Some questions
cOIlL'r:rning the knowledge of Palaearctic
Coecoidea (Homoptera). Bollettino del
Laboratorio diEntomologia Agraria Filippo
Silvestri 43: 97-105.
Lanteri AA, Normark BB. 1995. rarthenogenisis
in the tribe Naupactini (Coleoptera:
Curculionidad. Annals of the Entomological Society of America 88: 722-731.
LattinJD, Oman P. 1983. Where are the exotic
insect threats? Pages 93-137 in Wilson CI.,
Graham CL, eds. Exotic plant pt'sts and
North Amcrican agriculture. New York:
Academic Press.
Ledig IT. 1992. Human impacts on genetic divcrsity in forest ecosystems. Oikos 63: 87108.
Liebhold AM, MacDonald WL, Bergdahl D,
Mastro Ve. 1995. Invasion by exotic forest
pests: a threat to forest ecosystems. Forest
Science 41: 1-49.
Lindroth CH. 1957. The fallnal connections
between Europe and North America. New
York: John Wiley and Sons.
Little EL 1979. Checklist of United SWles lrees
(native andnaturalizedl. Handbook nr 541.
W'ashington (DC): USDA Forest Service.
todge DM. 199.1. Biological invasions: lessons
forecolugy. Trends in Ecology & Evolution
8: 133-137.
Lowe lJ, Power K, Gray SL 1992. Canada's
forest inventory 1991. Information Report
PI-X-l1S. Petawawa (Canada): Petawawa
Nationall;orestry Institute, Canadian forest Service.
Mattson Wj, Niemela P, Millers I, Inguanw Y.
1994. Immigrant phytophagous insects on
woody plants in the United States and
Canada: an annotated list. General Tedlllical Report nr KC-169. St. Paul (MN): US
Department of Agriculture.
Mills NJ. 1992. Parasitoid guilds, life-styles,
and host ranges in (he pan1SitOid complexes
oftorrricoid hosts (Lepidoptera: l'ortrlcoiclea).
Environmental Entomology 21: 2.10-2.19.
Monkkonen.M, HeUe P. 1989. Migratory habits
of birds breeding in different stages of forest
succession: a comparison between the
Palaearctic and the Nearctic. Annales
Zoologici Fenllici26: 323-330.
Monkkoncn M, Welsh DA. lY~3. A biogeographical hypothesis on theetfects of human
caused landscape changes on the forest bird
communitit's ofEurupe and North America.
Anna\cs Zoologici Fcnnici 31: 61-70.
Mooney HA, Drake JA. 1986. Ecology of biological invasions of North America and
Hawaii. New York: Springer Vcrlag.
:"Jeuvonen S, Niemela P. 1981. Species richness
of Macrolepidoptera on Finnish decidllollS
trees and shrubs. Oecologia 51: 364-370.
November .1996
___ . 191B. Species richness and faunal similarity of arbore:'!l imect herhivore~. Oikos
40: 452-459.
Kicmcla J, Spence JR. 1991. Distribution and
abundance of an exotic ground-beetle
(Cambidae:l: a test of community impa(;t.
Oikos 62: 351-359.
Korri~D_\1. H92. Xyleborus ambrosia beetles:
a symbiotic ideal extreme biofacies with
evoIved polyphagous privleges at monophagous prices. Symbiosis 14: 229-236.
Perlin J. 1989. A forest iourney. New York:
W.W. Norton & Co.
Panting e. 1991. A green history of the world,
the environment of great civilizations . .:-Jew
York: Pengllin Boob.
Price PW, Lewimuhn TM, Fernandes GW,
Benson \~'W, eds. 1991. Plam-animal interactions: evolutionary ecology in tropical and
temperate regions. New York: John \~'ilt'y
& Sons.
Quiring [). 1~92. Rapid changes in suitability of
whittc spruce for .fI specialist herbivore,
Zeiraphera canadensis, as a fun<.:tiun of leaf
age. Canadian Journal of Zoology 70: 2132211fl.
Raffa KF, Hall OJ, Kearby W, Katovich S.
1992. Seasonal lifc history of introduced
basswood thrips (Thysanoptera: Thripidae)
in Wisconsin, with observations on associatcd thrips. Environmcntal Entomology 21:
771-779.
Reimanek M. 1989. Invasibility of plant communities. Pages 369-388 in Drake JA,
Mooney HA, di Castri F, Groves RH, Kruger
Fj, Rejmanek M, Williamson M, eds. Biological invasion: a global perspective. New
York: John Wiley and Som.
Rohrig E. 1991. Floral composition and its evolutionar), development. Pages 17-24 in
Rohrig E, Ulrich E, eds. Ecosystems of the
world. Vol. 7. Temperatedeciduous forests.
Kew York: FJsevier.
Rohrig E, Ulril'll E, eds. 1991. Ecosystern~ of the
world. Vol. 7. Temperate deciduous forests.
New York: Elsevier.
Roques A. 1988. La specificite des rdatiom
elltre cones de coniferes et insectes infeodes
en europe occidentale un exemple d'etude
des interaction,~ pL8nte~-in~ectes. Doctoral
dissertation. Pan (France): Universite dePau.
Sailer RI. 1983. History' of insect introductions.
Pages 15-38 in Wilson l, Graham CT., ed,~.
Exotic plant pests and North American agriculture. New Yotk: Academic Press.
Sauer JD. 1988. Plant migration: the dynamics
of gengraphic patterning in seed plant species. Berkeley (CAl: University of California
Press.
Schaefer CW, Kosztarab M. 1991. Systematics
of imects and arachnids, status, problems,
and needs in North America. American
Entomoligist 37: 211-216.
Simherloff D. 1989. \Vhich introductions succeed and which fail. Pages 61-75 in Drake
J A, Mooney HA, di Cas[ri F, Groves RH,
Kruger FJ, Retmanek M, Williamson M, eds.
Biological invasion: a global perspective.
New York: Jobn Wiley & Sons.
Skuhrava M, Skuhravy V, Brewer JW. 1984.
Biology of gall midges. Pages 169-222 in
Ananthakrishnan TN, ed. Biology of gall
insccts. London (UK): Edward Arnuld.
Smith DR. 1979. Symphyta. Pages 3-123 in
Krombein KV, Hurd PD, Smith DR, Ruck
BD, cds. Catalogue uf Hymenoptera in
America, north of Mexico. Washington (DC):
Smithsonian Institute.
___ . 1993. Systematics, life history, and
distribution of sawflies. Pages 3-32 in
Wagner M, Raffa KF, eds. Sawfly life history adaptatiuns to woody plants. New York:
Academic Prc,s.
Smith WB,FaulkncrJL,PoweJl DS. 1994. Forest
statistics of the United States, 1992 metric
units. Gcneral Technical Report nr NC-168.
51. Paul (MN): USDA Forest Service.
Spongberg SA. 1990. A reunion of trees. Cambridge (MA): Harvard University Press.
Stebbins GL 1993. Concepts of species and genera. Pages 229-246 in flora of North America
Committee, eds. Flora of North America. Vol.
1. ":"Jew Yurk: Oxford University Press.
StoyenoffJL, WitterJA,Montgomery ME. 1994.
Gypsy moth (Lepidoptera: Lymantriidae)
performances in relation to egg hatch and
feeding initiation times. Environmental Entomology23: 1450-14.'\8.
Strong DR, Lawton JH, Southwuod R. 1984,
Insects on plants: community patterns and
mechanisms. Camhridge (MA): Harvard
University Press.
Stuckey RL, Barkley TM. 1993. Weeds. Pages
193-198 in Flora of North America Committee, ed. Flora of North America. Vol. 1.
New York: Oxford Univenity Pres~.
Suomalainen £, Saura A, LokkiJ. 1976. Evolution of parthenogenetic insects_ Pages 209257 in Hecht MK, Steere WC, Wallace B,
eds. Evolutionary biology. Vol. 9. New York:
plenum Press.
TahvanainenJ,Niemeia P.1987. Biogeographical
and evolutionary aspet:ts uf insen herbivory.
Annales Zoologici Fennici 24: 239-247.
Tallher MJ, Tauher CA, Masaki S. 1986. Seasonal adaptatiom of insects. New York:
Oxford University Press.
Thompson Fe. 1990. Biosystematics information: dipterists ride' the third wave. Pages
179-189 in Ko~ztarab M, SchaeferCW, eds.
Systematics of the North American insects
and arachnids: status and needs. Virginia
Agricultural Experiment Station Information Series 90-1. Blacksburg (VA): Virginia
Polytechnic Imtitute and State University.
Vermeij GJ. 1991. AnatolllY of an inva~ion: the
trans-Arctic interl'hange. Paleobiolugy 17:
281-307.
Vrha ES. 1992. :'vfammals as key to evolutionary
theory. Journal of Mammology 73: 1-28.
Webb T, Barlein PJ. 1992. Global changes during the last 3 mlliion years: climatic controls
and bioticresponse~. Annu:'!l Review ofEcol"
ogy and Systematics 23: 141-173.
Wheeler AG, HenryTJ. 1992. A synthesis of the
Tlolarctic Miridae (Heteroptera)-; dimibn"
tion, biology, and origin with emphasis on
North America. Latham (MD): The Thomas
Say Foundation, Entomological Socicty of
America.
Wilson CL, Graham CL. 1983. Exotic plant
pcsts and North Americanagriculture. New
York: Academic Press.
Wood TK, Olmstead KL, Gutmann S1. 1990.
Insect phenology mediated by host-plant
water relations. Evolution 44: 629-636.
ZonR. 1910. The forest resources of the world.
USDA Forest Service Bulletin nr 83. Washington (DC): US Government Printing Office.
Zwolfer H. 1988. Evolutionary and ecological
relationships of the insect fauna of thi~tles.
Annual Review of Entomology 33: 103-122.
753