Diversity and Distributions, (Diversity Distrib.) (2005) 11, 311–317
Blackwell Publishing, Ltd.
BIODIVERSITY
RESEARCH
Increased resistance to generalist
herbivores in invasive populations of the
California poppy (Eschscholzia californica)
Elizabeth A. Leger1* and Matthew L. Forister2
1
Department of Agronomy and Range Science
and the Center for Population Biology,
University of California, Davis; One Shields
Avenue; Davis, CA 95616, USA 2Section of
Evolution and Ecology and the Center for
Population Biology, University of California,
Davis; One Shields Avenue; Davis, CA 95616,
USA
*Correspondence: Elizabeth A. Leger,
Department of Ecology and Evolution; State
University of New York at Stony Brook; 650 Life
Sciences Building, Stony Brook, NY 11794–5245,
USA. E-mail: [email protected]
ABSTRACT
Escape from enemies in the native range is often assumed to contribute to the successful invasion of exotic species. Following optimal defence theory, which assumes
a trade-off between herbivore resistance and plant growth, some have predicted that
the success of invasive species could be the result of the evolution of lower resistance
to herbivores and increased allocation of resources to growth and reproduction.
Lack of evidence for ubiquitous costs of producing plant toxins, and the recognition
that invasive species may escape specialist, but not generalist enemies, has led to a
new prediction: invasive species may escape ecological trade-offs associated with
specialist herbivores, and evolve increased, rather than decreased, production of defensive compounds that are effective at deterring generalist herbivores in the introduced
range. We tested the performance of two generalist lepidopteran herbivores, Trichoplusia ni and Orgyia vetusta, when raised on diets of native and invasive populations
of the California poppy, Eschscholzia californica. Pupae of T. ni were significantly larger
when reared on native populations. Similarly, caterpillars of O. vetusta performed
significantly better when raised on native populations, indicating that invasive
populations of the California poppy are more resistant to herbivores than native
populations. The chance of successful establishment of some non-indigenous plant
species may be increased by retaining resistance to generalist herbivores, and in some
cases, invasive species may be able to escape ecological trade-offs in their new range and
evolve, as we observed, even greater resistance to generalist herbivores than native plants.
Keywords
Biological invasions, Chile, defence, EICA, ERH, herbivore resistance, invasive species,
Papaveraceae.
Invasive plants appear to have overcome factors that limit the
growth and spread of other species. Their population density and
fecundity stand in contrast to most native species, and an escape
from native enemies is often cited as a major cause for their
success (Elton, 1958; Darwin, 1859; Maron & Vila, 2001; Keane &
Crawley, 2002; Wolfe, 2002; Mitchell & Power, 2003; Torchin
et al., 2003; but see Agrawal & Kotanen, 2003; Müller-Schärer
et al., 2004). It has been assumed that resistance to herbivores
should be costly (e.g. Herms & Mattson, 1992). The term ‘resistance’
is used here to refer to plant traits that affect either the preference
or performance of a herbivore, or both, and thereby reduce damage
received by a plant (Müller-Schärer et al., 2004). The evolution of
increased competitive ability hypothesis (EICA) predicts that
plants introduced into an environment that lacks their usual
herbivores will experience selection favouring individuals
that allocate less energy to resistance and more to growth and
reproduction. The result will be invasive populations characterized by higher growth and fitness relative to populations in the
native range (Blossey & Nötzold, 1995).
The EICA assumes that costs are allocational (i.e. trade-offs
between fitness and resistance that are resource-based), but
researchers are increasingly finding evidence for ecological costs
of resistance (Heil, 2002; Koricheva, 2002; Strauss et al., 2002).
For example, production of high levels of defensive chemicals
can be costly because they can attract specialized herbivores
(Bolter et al., 1997; Agrawal et al., 1999; Renwick, 2002; Nieminen
et al., 2003), repel predatory insects (Agrawal et al., 2002), or
increase susceptibility to pathogens (Felton et al., 1999; Thaler
et al., 1999). If specialized enemies are not introduced along with
the invader, or there are no closely related species naturally
present from which specialized enemies could colonize (e.g.
Conner et al., 1980), one would expect that these types of ecological
interactions would be absent in the invasive range, and introduced plants might be able to maintain resistant traits without
© 2005 Blackwell Publishing Ltd www.blackwellpublishing.com/ddi
DOI: 10.1111/j.1366-9516.2005.00165.x
INTRODUCTION
311
E. A. Leger and M. L. Forister
incurring associated ecological costs (Müller-Schärer et al.,
2004).
Although invasive species may be expected to have reduced
damage from specialists, there is evidence that generalist enemies
attack and negatively affect introduced species (reviews in Maron
& Vila, 2001; Levine et al., 2004). Müller-Schärer et al. (2004)
suggest that if introduced species are not experiencing ecological
costs of resistance (resulting from a lack of specialists), they may
be able to evolve higher levels of herbivore resistance without cost.
Specifically, they predict that invasive species that produce higher
quantities of qualitative plant defences (toxins like alkaloids and
glucosinolates), which are often effective at deterring generalists,
would be at an advantage in an environment where specialist
herbivores are lacking. This advantage should result in invasive
populations with increased resistance to generalist herbivores.
The EICA and Müller-Schärer et al. (2004) present two fundamentally different scenarios regarding the evolution of defensive
traits in invasive plants, with decreased levels of resistance traits
expected in the former, and increased levels of defence expected when
species are introduced without specialist herbivores in the latter.
The California poppy, Eschscholzia californica Cham, a member of the Papaveraceae family, is endemic to the west coast of the
United States and is an invasive plant in other areas of the world
(Stebbins, 1965). We focus on the invasion of E. californica in
Chile, where it was first recorded in the mid 1800s. Thought to be
introduced multiple times through botanical gardens, horticulture, and as a contaminant of agricultural seed, the California
poppy spread quickly, and now occurs in disturbed areas (e.g.
roadsides, dry river beds and washes, and agricultural landscapes)
throughout a 750-kilometer stretch of central Chile (Hillman &
Henry, 1928; Frias et al., 1975; Arroyo et al., 2000). Previous common
garden studies with the California poppy have demonstrated differences in plasticity between native and invasive populations,
with individuals from the invasive range in Chile able to attain
larger sizes and produce more flowers than native individuals when
released from competition with other plants (Leger & Rice, 2003).
In this study, we address the possibility that resistance traits
in California poppy have evolved in the invasive, Chilean range,
by evaluating the performance of generalist herbivorous insects
raised on plants from populations in California and Chile. Excluding Eschscholzia, there are three genera (Argemone, Fumaria,
and Papavar) in the Papaveraceae that are present in Chile, but
Argemone alone is a native (Matthei, 1995). Like other members
of the Papaveraceae, the California poppy has a diverse array of
chemical compounds that might provide resistance to herbivory.
There are 30 known isoquinoline alkaloids in the roots and
shoots of the California poppy, 14 of which have been isolated
from the aerial parts by Fabre et al. (2000), with californidine
and escholtzine in the highest concentrations. No information is
available regarding herbivory in the invasive range (the community
of natural enemies in the native range is not well described either,
as discussed in succeeding discussion), but because the genus
Eschscholzia is taxonomically isolated in Chile, we would not
expect that specialist insects have colonized the California poppy
in the invasive range. It can be assumed, however, that generalist
herbivores are present in Chile. Consequently, we predict that
312
plants from invasive populations would have equal or increased
resistance to generalist herbivores compared to native plants. We
used a bioassay approach to examine this question, raising two
species of generalist herbivores on plants collected from both
regions, grown in a common garden.
METHODS
Natural enemies of the California poppy
There have been no comprehensive studies of the natural
enemies of the California poppy in California, although there are
a number of cases where generalist Lepidoptera have been
reported to use E. californica as a host plant. We observed herbivory
in natural and common garden populations in California, and
saw many cases of floral herbivory, or florivory, by Lepidoptera.
Of six common gardens in California planted in three locations
over the course of 3 years, lepidopteran caterpillars were observed
eating poppy flowers in all six gardens, sometimes in outbreak
numbers. For example, in spring of 2000, many thousands of
caterpillars of the alfalfa looper, Autographa californica Speyer, a
native, polyphagous moth, colonized a common garden in Davis,
California. Of 100 flowers marked for an unrelated experiment, 54
were eaten by A. californica caterpillars (E.A. Leger, unpublished
data). Caterpillars of the western tussock moth, Orgyia vetusta
Boisduval, were also observed eating flowers of E. californica in a
natural population in Bodega Bay, Sonoma County, California
(38°19′ N; 123°03′ W). We did not observe insect herbivory of
adult poppy leaves in any of these common gardens (although
slugs and snails readily ate seedling plants).
Larvae of one other generalist moth, Cnephasia longana
Haworth, have been recorded on the California poppy (Robinson
et al., 2002). In addition, one species that may be a specialist on
California poppies has been observed: larvae of the geometrid
moth Neoterpes edwardsata Packard, have been found on California poppies in Davis, California (DeBenedictis, pers. comm.).
Although complete host records do not exist, N. edwardsata appears to be a species with a restricted host range, and the larvae
resemble flower buds of the California poppy.
Because florivory by lepidopteran caterpillars was the most
common type of herbivory noted in field experiments, we
selected two lepidopteran herbivores for our bioassay: the cabbage
looper, Trichoplusia ni Hübner, and O. vetusta, both generalist
moths found in California. E. californica is among the known
larval host plants for T. ni (Tietz, 1972), and as mentioned previously, larvae of O. vetusta were observed eating poppy flowers
in a wild population. The T. ni individuals used in this study were
from a naïve lab colony with no previous association with the
California poppy. Young caterpillars (2nd or 3rd instar) of O.
vetusta were collected from bush lupines (Lupinus arboreus Sims)
near a natural population of poppies at Bodega Bay.
Experimental design
Plants used in the experiments reported here were from populations collected from a wide variety of environments in both the
Diversity and Distributions, 11, 311–317, © 2005 Blackwell Publishing Ltd
Herbivore resistance of California poppies
Table 1 Source of Eschscholzia californica Cham plants used in this
experiment
Population
County/region
Location
Californian (native)
Antelope Valley*
Plaskett Creek*
Bodega Bay*†
Cedar Grove*†
McLaughlin†
Bear Valley†
Albion†
Los Angeles
Monterey
Sonoma
El Dorado
Lake
Colusa
Mendocino
34°45′ N,
35°55′ N,
38°19′ N,
38°44′ N,
38°52′ N,
39°04′ N,
39°12′ N,
118°15′ W
121°28′ W
123°03′ W
120°39′ W
122°25′ W
122°24′ W
123°45′ W
Chilean (invasive)
La Aguada*†
Talagante*†
Pichilemu*†
Constitución*†
Región IV
Región Metropolitana
Región VI
Región VII
31°38′ S,
33°40′ S,
34°23′ S,
35°27′ S,
71°11′ W
70°55′ W
71°59′ W
72°29′ W
*Populations used in the Trichoplusia ni Hübner bioassay, †populations
used in the Orgyia vetusta Boisduval bioassay.
native and exotic range, see Table 1 for collection localities and
Leger and Rice (2003) for details of seed collection. Experiments
with the two herbivore species were conducted in consecutive
years, and not all plant populations used in the first year were
used in the following year (Table 1 indicates which populations
were used in which years). Populations used in experiments were
represented by 20 to 25 plants, grown from bulk seeds in a common outdoor environment in Davis, Yolo County, California
(38°32′31′′ N, 121°45′48′′ W). All analyses were conducted using
  version 4.0.2 (SAS, 2001) and significance was measured
at the P = 0.05 level.
Flowers were harvested daily and transported to the lab where
caterpillars were being raised. We raised caterpillars on cut
flowers instead of caging insects on individual plants in order to
control for population level differences in plant size, architecture,
and number of flowers per plant. These differences in plant form
and resource availability would have almost certainly led to differences in searching time for foraging caterpillars, and for some
populations, one individual plant would not have provided
sufficient flower tissue to raise caterpillars to maturity. While
searching time is of course a realistic component of herbivore
performance in the wild, we designed these experiments to focus
specifically on differences in plant chemistry and quality that
could affect caterpillar performance. Experiments on the inducibility of defensive compounds in California poppy flowers
(using herbivores to induce damage, and separate herbivores
to assay differences in palatability after damage) have found
no evidence for increased defences after damage (McCall, unpublished data), so cut flowers were likely to have the same
composition as un-cut flowers.
Trichoplusia ni
In the summer of 2002, we raised the larvae of T. ni on a diet of
flowers from eight E. californica populations. Caterpillars were
Diversity and Distributions, 11, 311–317, © 2005 Blackwell Publishing Ltd
reared in Petri dishes on flowers harvested from each population,
in four dishes per population, with five newly hatched caterpillars
placed in each dish. Flowers were replenished daily, or more
often as needed, and care was taken to ensure caterpillars did not
run low on food. The number of caterpillars per dish had no effect
on the final mass of pupae (df = 1,57; F = 0.4511; P = 0.77). We
measured survival, time to pupation, and the final mass of all
caterpillars in each dish; values were averaged in each dish before
analyses were conducted.  was used to test for differences
in time to pupation and final mass.  models were constructed with the following effects: country of origin and population (random effect) nested within country of origin. Differences
in survival were investigated with a logistic regression with the
same factors as the  models.
Orgyia vetusta
In summer of 2003, we raised O. vetusta caterpillars on a diet of
flowers from five native and four invasive populations (Table 1).
Caterpillars were raised in 30 individual mesh cages, with one
caterpillar per cage, and were provided with an abundance of
flowers that were replenished daily. We collected flowers evenly
from all populations, but provided them to caterpillars without
regard to their population of origin. In our previous experiment
with T. ni, there was not a significant effect of population, and
this pooling of populations increased the efficiency of the rearing
process while still allowing us to test for differences in the main
effect of interest (differences between countries).
We measured the initial weight of each caterpillar, their weight
after 2 weeks, and the weight of pupae 1 week after pupation was
initiated. There is a marked sexual dimorphism in O. vetusta,
with the large, flightless females weighing over three times as
much as adult males. This mass difference was not detectable in
early instar larvae, but was discernable after 2 weeks of growth, at
which point the sex of each caterpillar was determined, and verified
after the emergence of adult moths. The distribution of male and
female caterpillars assigned to the two different diet treatments
was nearly identical. Differences in survival were compared using
Pearson’s chi-squared test.  was used to test for differences
in time to pupation, and final biomass. Effects included in the
 models were country of origin, sex of caterpillar, and
initial caterpillar weight, included as a covariate.
Flower chemistry
In addition to rearing experiments with herbivores, we conducted an assay of the carbon and nitrogen content of poppy
flowers, as a preliminary investigation into relevant flower chemistry. Flowers were collected from all plants used in the O. vetusta
bioassay, and dried in a 65° oven for 48 h. Flowers from each
plant (70 plants total) were ground, and total carbon and nitrogen
were analysed by combustion to CO2 and N2 using an automated
C and N analyser.  was used to test for differences in C : N
ratio in invasive and native populations, with country of origin
and population (random effect) nested within country of origin
as effects in the model.
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E. A. Leger and M. L. Forister
RESULTS
Trichoplusia ni
A total of 63 caterpillars in 29 dishes survived the experiment,
with the majority of mortality occurring during the first few days
of growth. There were no differences in survival between caterpillars
raised on invasive or native material, with 51.3% of caterpillars
surviving when raised on a diet of flowers from invasive populations and 52.5% of caterpillars surviving after being reared on
flowers from native populations (df = 1,6; F = 0.0017; P = 0.97).
There was a significant effect of country of origin on caterpillar
mass: caterpillars reared on native populations were significantly
larger than caterpillars reared on invasive populations (1.94 mg
and 1.84 mg, respectively; df = 1,6; F = 10.0665; P = 0.01; β =
0.13) (Fig. 1). Time to pupation was not affected by the country
of origin (df = 1,6; F = 3.9021; P = 0.09; β = 0.26). Population
did not affect either caterpillar mass (df = 6,21; F = 0.1070;
P = 0.99; β = 0.07) or time to pupation (df = 6,21; F = 2.0837;
P = 0.10; β = 0.61), but there were differences in survival between
populations (df = 6,24; F = 3.965; P = 0.01).
Figure 2 Weight of Orgyia vetusta Boisduval at three different
stages: initial weight of caterpillars when removed from the field,
weight of caterpillars two weeks later, and final weight of pupae.
were not significantly different at the end of the experiment
(df = 1,22; F = 1.2008; P = 0.29; β = 0.18) (Fig. 2). Caterpillars
fed with invasive and native material did not differ in the time it
took to pupate (df = 1,22; F = 0.0038; P = 0.95; β = 0.05).
Orgyia vetusta
All of the caterpillars reared on native material survived the
experiment, while 73.3% of caterpillars reared on invasive material survived to adulthood. The caterpillars that died were the
smallest males (as measured 2 weeks into the experiment) that
were being reared on flowers from invasive populations, and
this difference in survival was significant (χ2 = 6.163, P = 0.03).
Caterpillars reared on material from native poppies were significantly larger than those eating material from invasive poppies
after 2 weeks in the lab (22.2 mg and 16.4 mg, respectively;
df = 1,26; F = 4.6605; P = 0.04; β = 0.55) (Fig. 2). Pupal weights
Figure 1 Weight of Trichoplusia ni Hübner pupae reared on poppy
flowers from California (native) and Chile (invasive). Values shown
are LS mean (± SE) pupal weights for each population, and for overall
differences between invasive and native populations. *P < 0.05.
314
Flower chemistry
There was no difference in the C : N ratio of flower tissue
between invasive (16.34 ± 0.77) or native (15.91 ± 0.75 SE) poppies
(df = 1,7; F = 0.1643; P = 0.70; β = 0.05). Populations did not
differ significantly in their C : N ratios (df = 7,61; F = 1.6571;
P = 0.14; β = 0.63).
DISCUSSION
We found small but significant increases in herbivore performance when caterpillars were raised on plants collected from
California, the native range of the California poppy. Although the
experiments described here are not large, the general result that
invasive populations were more resistant to generalist herbivores
than native populations was consistent for bioassays involving
two herbivore species raised on plants collected from a wide
geographical and environmental range.
Pupae of T. ni were larger when reared on native populations
(Fig. 1), O. vetusta survived better on a diet of native populations, and caterpillars reared for 2 weeks on native populations
were larger than those raised on invasive populations (Fig. 2).
O. vetusta pupae were not significantly different in mass by the
end of the experiment, but it should be noted that the smallest
caterpillars reared on invasive populations had died by this point,
while all caterpillars reared on native populations survived the
duration of the experiment. These results suggest that invasive
populations of the California poppy have higher levels of resistance
traits, which could act in the field to reduce damage by generalist
herbivores. Another possible explanation for the difference in
pupal mass and caterpillar survival is that the nutritional quality
of the native poppies is superior. While this possibility cannot be
ruled out, the nearly identical C : N ratios that we found indicate
Diversity and Distributions, 11, 311–317, © 2005 Blackwell Publishing Ltd
Herbivore resistance of California poppies
that the observed differences in caterpillar performance are not
likely the result of differences in nutritional quality, which are
often manifest in higher nitrogen levels (Schoonhoven et al.,
1998).
The results obtained with T. ni and O. vetusta are generally
consistent with the scenario proposed by Müller-Schärer et al.
(2004), in which populations of invasive plants are better
defended than native populations. Because previous studies
investigating size differences between invasive and native populations found that invasive plants were capable of growing larger
than native plants when grown with reduced competition (Leger
& Rice, 2003), there does not seem to be an obvious trade-off
between increased plant size and increased resistance in this
system. Future studies which compare herbivore performance,
alkaloid levels, and plant size or fecundity of specific genotypes
would be informative. Alternately, if costs are allocational, it is
possible that invasive populations have overcome a physiological
barrier that allows them to produce additional defences without
incurring fitness costs.
Of the few systems in which herbivore preference for or
performance or both on invasive and native populations grown
in a common environment has been investigated, two studies
found results consistent with ours: invasive plants with the
fastest growth rates also had the highest herbivore resistance in
S. alterniflora Lois. (Daehler & Strong, 1997). Another common
garden study found that a potential biocontrol agent failed to
establish on star thistle (Centaurea solstitialis L.) from California,
although it was able to establish on native populations from Italy,
and levels of herbivore damage were generally lower on plants
from the introduced range (Clement, 1994). Other studies, however, have found the opposite result: herbivore preference was
greater for invasive populations of Lythrum salicaria L. (Blossey
& Nötzold, 1995; Blossey & Kamil, 1996) and increased performance of some insects but not of others was also observed on invasive
L. salicaria (Blossey & Nötzold, 1995; Willis et al., 1999). Another
study found lower tannin levels in invasive populations of Sapium
sebiferum (L.) Roxb. (Siemann & Rogers, 2001), and increased
herbivore preference for S. sebiferum from invasive populations
(Siemann & Rogers, 2003). Invasive populations of Silene latifolia
Poiret experienced greater damage from seed predators, fungal
pathogens, and aphids than native populations when grown in a
common garden in the native range, but still outperformed
native plants (Wolfe et al., 2004).
Although the evidence from these few studies is mixed, it
might be predicted that some invasive plants would be resistant
to herbivores. Entomologists have kept extensive records of the
colonization of exotic plants by native insects (e.g. Strong, 1979;
Kennedy & Southwood, 1984), and studies have shown that the
fitness of exotic plants may be negatively affected by herbivores
encountered in the new range (Maron & Vila, 2001; Levine et al.,
2004). By colonizing exotic plants, native herbivores may benefit
by escaping their predators and parasitoids that rely on plant
traits to find their prey (this is known as the ‘enemy-free space’
hypothesis) (Jeffries & Lawton, 1984; Berdegue et al., 1996).
Given the fact that exotic plants are colonized by insects that may
exert selective pressures, one would predict that some plants
Diversity and Distributions, 11, 311–317, © 2005 Blackwell Publishing Ltd
might have comparable defences in their native and introduced
ranges.
Recent studies have shown that introduced plants and animals
have a lower diversity of natural enemies, and sometimes experience a smaller effect of enemy damage, than they do in their
native ranges (reviewed in Colautti et al., 2004). It is believed that
this pattern is a result of organisms both escaping from and failing to accumulate enemies upon colonization of a new range.
What remains unknown in these observational studies is why
new enemies fail to accumulate. While it is likely that a certain
amount of time is needed for enemies to discover or adapt to a
new host, it is also possible that invaders retain their herbivore
resistance traits, and some invasive plants may even possess
heightened levels of resistance traits, as we found in invasive
California poppies.
ACKNOWLEDGEMENTS
We thank M. Berenbaum and A. Zangerl for supplying the T. ni
caterpillars and Maraya Cornell for helping to raise them, and
A. McCall for discovering the O. vetusta eating poppy flowers.
E. Espeland, R. Karban, J. Lau, A. McCall, J. Randall, K. Rice, and
J. Rudgers for the improved drafts of the manuscript.
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