Full text of DOI:10.1007/PL00008859

Oecologia (2000) 123:543–549
© Springer-Verlag 2000
Rob Tune · David E. Dussourd
Specialized generalists: constraints on host range
in some plusiine caterpillars
Received: 25 August 1999 / Accepted: 8 December 1999
Abstract Insects that feed on plants with secretory ca-
nals often cut trenches across leaves, thereby depressur-
Introduction
A polyphagous insect can potentially encounter any of a
multitude of possible food plants, each with its own dis-
tinctive allelochemical composition (Bernays and Chap-
man 1994). The insect must decide whether to feed or to
move on. The difficulty of this task has led to the sug-
gestion that polyphagy is uncommon in insects because
of neural constraints. The limited ability of insect herbi-
vores to process information efficiently may favor spe-
cialization and the use of specific cues that indicate ac-
ceptable food (Bernays 1998; Bernays and Funk 1999).
Identifying suitable food may be especially difficult
for cabbage loopers (Trichoplusia ni) and other poly-
phagous members of the subfamily Plusiinae (Lepidopte-
ra: Noctuidae). These caterpillars must not only evaluate
the nutritional and allelochemical composition of a leaf,
they must also determine if a plant requires trenching.
Larvae cut trenches to deactivate canal systems that emit
defensive secretions such as latex or resin (Dussourd
1993; Dussourd and Denno 1994). The larvae nibble
back and forth across the leaf, thereby rupturing canals
and preventing secretion from flowing to their prospec-
tive feeding site. The trench also drains secretion from
this distal section. A larva detecting deterrent substances
should not necessarily abandon a leaf if the plant defense
can be neutralized by trenching.
Cabbage loopers cut trenches in members of the As-
teraceae with latex canals (tribe Lactuceae), Apiaceae
with oil ducts, and Cucurbitaceae with phloem canals
that emit sap (Dussourd and Denno 1994). These three
families are classified in three different orders (Angio-
sperm Phylogeny Group 1998) and have canals that dif-
fer greatly in anatomy and chemical content. Cabbage
loopers also attack many other plant species that do not
release exudates; these plants are not trenched (Dussourd
and Denno 1994). To feed on such disparate hosts and to
recognize which require trenching, the larvae must re-
spond appropriately to diverse chemistries. In addition,
trenching loopers must tolerate persistent contact with
exudates oozing from the leaf. For example, on prickly
izing the canals and eliminating exudation at their distal
feeding site. We compared the trenching ability of three
species of polyphagous plusiines (Lepidoptera: Noctu-
idae) and tested if trenching scores correlate with larval
growth. The three plusiines (Trichoplusia ni, Pseudo-
plusia includens, and Rachiplusia ou) were each tested
on prickly lettuce, Lactuca serriola (Asteraceae), which
has latex canals, and on Italian parsley, Petroselinum
crispum (Apiaceae) with oil ducts. To ascertain how se-
cretory canals affect performance, larvae were tested on
intact leaves and on excised leaves with depleted canals.
T. ni larvae cut trenches in both plant species, whereas P.
includens only trenched prickly lettuce and R. ou only
trenched Italian parsley. Intact leaves of Italian parsley
were acceptable to all three species. Trenching varied in
T. ni and R. ou, but did not correlate significantly with
larval growth. In contrast, trenching was required for
feeding on intact prickly lettuce. Final-instar T. ni all cut
trenches and developed rapidly. P. includens varied in
trenching and performance; their trenching scores corre-
lated with growth. R. ou larvae did not trench or feed
even though most R. ou on intact Italian parsley cut at
least partial trenches. All three plusiine species devel-
oped rapidly on excised leaves of both plant species,
documenting the suitability of these plants when canals
are inactivated. Our results document the efficacy of la-
tex canals as a plant defense and suggest that trenching
ability alone does not permit feeding. Larvae must also
recognize the need to trench and must tolerate deterrent
exudates during the trenching procedure.
Key words Trichoplusia ni · Pseudoplusia includens ·
Rachiplusia ou · Secretory canals · Trenching behavior
R. Tune · D.E. Dussourd (
Department of Biology, University of Central Arkansas,
Conway, AK, 72035, USA
e-mail: dussourd@mail.uca.edu
Tel.: +1-501-4505921, Fax: +1-501-4505914
)
✉

544
lettuce, cabbage loopers repeatedly contact latex during no 1991). With such tiny amounts, it seems unlikely that
trenching and stop to groom ~20 times before complet- exudate viscosity or adhesiveness could deter insect
ing a trench (Dussourd 1999).
feeding, particularly with larger larvae. However, parsley
Over 15 species of polyphagous plusiines that feed on leaves contain furanocoumarins, terpenes, and phenyl-
plants in three or more families occur in North America propanoids (Porter 1989; Knogge et al. 1987), com-
(Eichlin and Cunningham 1978; Lafontaine and Poole pounds that are well known for their antifeedant and tox-
1991). Although extensive host records are available for ic effects on herbivores (Berenbaum 1990; Zangerl 1990;
some species, particularly for pests on agricultural crops Gershenzon and Croteau 1991; Berdegue et al. 1997).
(Eichlin and Cunningham 1978), little is known about These compounds presumably occur at least partly in the
what factors determine their host ranges. In this paper, oil ducts as documented with other umbellifer species
we explore the proposition that host range in plusiines is (Hegnauer 1971; Camm et al. 1976; Zangerl and Bazzaz
determined not just by the suitability of a particular 1992; Stahl-Biskup and Wichtmann 1991).
plant, but also by the ability of larvae to recognize which
plant defenses can be disarmed by trenching and to toler- larvae on intact plants and on excised leaves with depres-
ate exudates while cutting a trench. surized canals. Our goal was to determine if the three
We compared the growth and survivorship of plusiine
We compare the growth and survivorship of three spe- plusiine species differ in trenching, and if differences af-
cies of generalist plusiines: T. ni, Pseudoplusia include- fect larval performance on plants with secretory canals.
ns, and Rachiplusia ou. T. ni, the cabbage looper, is a
cosmopolitan pest on crucifers, lettuce, and other crops;
it reportedly attacks plants in over 30 families (Eichlin Methods
and Cunningham 1978; Sutherland and Greene 1984).
P. includens, the soybean looper, attacks soybean and
Insects and plants
members of over 10 other plant families (Lafontaine and
Poole 1991; Sullivan and Boethel 1994). The third spe-
cies, R. ou, feeds on herbaceous plants in at least seven bias, only adults attracted to lights were used to obtain eggs. Fur-
families (Eichlin and Cunningham 1978; Lafontaine and
Poole 1991). Trichoplusia and Pseudoplusia are classi-
fied in the tribe Argyrogrammatini, whereas R. ou is
placed in the tribe Plusiini (Kitching 1987; Lafontaine
and Poole 1991).
The plusiines were tested on prickly lettuce (Lactuca
serriola, Asteraceae) and Italian parsley (Petroselinum
crispum, Apiaceae). Prickly lettuce and other members
of the tribe Lactuceae have latex canals (laticifers) that
form an intricate network in the plant (Olson et al. 1969;
Fahn 1979). Latex is stored under pressure within living
cells. Damage causes an immediate release of latex,
which flows through the laticifers to the site of injury. (Schery 1972; Craker and Simon 1986). The Italian variety
The latex coagulates upon exposure to air. Early-instar
caterpillars of Spodoptera ornithogalli on prickly lettuce
sometimes become fatally trapped in congealing latex or
Moths were collected in June, July, and August 1998 at Forrest
City and Conway, Arkansas. To minimize any possible host plant
thermore, for each experiment, only a single offspring from each
female was tested on a plant species. This design maximized ge-
netic diversity and allowed us to compare individuals both within
and between caterpillar species.
All prickly lettuce and Italian parsley used in the study were
grown from seeds in a temperature-controlled greenhouse and
were used only once. Plants tested with larvae were from 1 to 5
months old; they all lacked reproductive structures and had not yet
bolted. Although L. serriola is native to the Mediterranean area
(Ryder and Whitaker 1976), it has become abundant in North
America and is attacked by several generalist plusiines that trench
its leaves (Anagrapha falcifera, Autographa precationis, Megalo-
grapha biloba, Trichoplusia ni; Dussourd and Denno 1991, 1994).
P. crispum (syn. P. sativum) is also indigenous to the Mediterra-
nean region, but has been widely cultivated in the United States
(neapolitanum Danert) was selected for our study because the
leaves are broader and thus trenches are easier to detect and score.
Several generalist plusiines, such as A. falcifera, A. precationis,
and T. ni feed on umbellifers and readily accept Italian parsley
have their mouthparts stuck together (Dussourd 1993).
The drying latex also interferes with trenching by larger
T. ni larvae, for example by temporarily gluing legs to-
gether (Dussourd 1999). Lactuceae latex also contains a
(Dussourd and Denno 1994).
Growth experiment
variety of allelochemicals, such as sesquiterpene lac- We compared the growth of final-instar larvae of T. ni, P. includens,
and R. ou over a 24-h test period. Newly emerged larvae from
tones, triterpenes, and sterols (Crosby 1963; Gonzalez
1977), some of which are known to deter feeding by in-
field-collected females were randomly assigned to either prickly
lettuce or Italian parsley. The larvae were reared to the early final
sect herbivores (Rees and Harborne 1985). Prickly let-
tuce is a wild relative of cultivated lettuce, L. sativa; re-
cent molecular evidence suggests that the two should be
classified as a single species (Koopman et al. 1998).
Italian parsley and other umbellifers have canals that
emit droplets of secretion containing essential oils and
resins (Hegnauer 1971). The canals occur as intercellular
spaces that form elongate ducts throughout the plant
(Warning 1934; Esau 1940; Metcalfe and Chalk 1950).
Parsley leaves emit substantially smaller volumes of ex-
instar on excised leaves that were cut in sections to depressurize
secretory canals. Trenching is not required for larval development
on excised leaves (Dussourd 1993; Dussourd and Denno 1994).
Upon reaching the final instar, the larvae were randomly assigned
to be tested on either excised or intact leaves of the same plant
species used for rearing. Larvae were weighed, then were enclosed
either in a plastic cassette with excised leaves or in a mesh sleeve
with intact leaves on a potted plant (one larva per plant). All lar-
vae were offered two newly mature leaves and were tested at
25°C. At the end of the 24-h period, the larvae were reweighed. A
total of nine larvae of each caterpillar species were tested on ex-
cised leaves and on intact leaves of each plant species. The 18 lar-
udate than leaves of prickly lettuce (Dussourd and Den- vae tested with each plant species all came from different females.

545
During the 24-h period, larvae were checked at least three lowed by separate ANOVAs for pupal mass and for time to pupat-
times to score trenches and to replace leaves that were mostly eat- ion. Data analyses were performed with Systat 7.0.1 statistical
en. The following four-point scale was used:
package (SPSS Inc., Chicago, Ill.).
(1) No trench produced during the 24-h period.
(2) Larva left bite marks in a band across the leaf, but the individ-
ual bites were not joined to form a complete trench.
(3) Larva cut a trench that extended across the entire leaf, but the
trench was thicker than 1 mm (measured from leaf base to-
wards tip). A thick trench often indicates that a larva is having
difficulty with exudates and must extend the trench to avoid
placing its mouth into latex exuding from the trench (Dussourd
1999).
Results
Prickly lettuce
In the 24-h experiment, plusiine growth was affected by
an interaction between caterpillar species and leaf treat-
ment (Fig. 1, Table 1). Larval mass change on excised
leaves did not differ significantly between species (one-
way ANOVA, F2,24=0.545, P>0.5). The larvae increased
their weight on average by 103%, a substantial gain for a
24-h period. In contrast, growth on intact leaves varied
substantially between species (F2,24=51.043, P<0.0001;
Fig. 1). T. ni larvae gained significantly more mass than
larvae of R. ou or P. includens, both of which lost
weight. For all three species, mass change was signifi-
cantly higher on excised leaves than on intact leaves
(Fig. 1). Two R. ou larvae that each lost 15% of their ini-
tial weight on intact prickly lettuce were allowed an ad-
ditional 24 h on the same leaves, which were now re-
moved from the plant. The larvae, on average, increased
(4) Larva cut a narrow trench (<1 mm) that extended completely
across the leaf.
For larvae that cut multiple trenches, only the first trench was
scored.
Survival experiment
Our second experiment tested if the three plusiine species can de-
velop on prickly lettuce and Italian parsley. We replicated the pre-
vious experimental design using first-instar larvae and measured
their survival until pupation. Newly emerged larvae were isolated
individually in plastic cassettes with excised leaves or were en-
closed within clip cages on intact leaves. Only a single larva was
tested on each plant. When the larvae outgrew the clip cages, they
were isolated with mesh sleeves that enclosed entire leaves. To
minimize disruption of secretory canals, the clip cages and sleeves
were padded where they attached to the leaves. Early-instar larvae
were transferred to new leaves every 2–3 days, whereas late-instar
larvae were transferred daily. As previously, 18 larvae of each
plusiine species were tested on each plant species; half of the lar-
vae were enclosed with excised leaves, whereas the other half re-
ceived intact leaves. All 18 larvae tested with each plant species
were the offspring of different females.
Performance was measured as percent survival, time from
hatching until pupation, and pupal weight, which was recorded
2 days after pupation. Trenches of late-instar larvae were evaluat-
ed periodically using the four-point scale described previously.
Larvae were tested indoors at 25°C.
Statistical analysis
In the 24-h experiment, we assessed the effects of caterpillar spe-
cies and leaf treatment (excised versus intact leaves) on larval mass
change using two-way ANOVAs. One-way ANOVAs were then
used to analyze effects of caterpillar species on mass change sepa-
rately for excised and intact leaves. Data not conforming to statisti-
cal assumptions of homogeneity of variance were log transformed.
Post hoc comparisons between species were made using Tukey
HSD multiple comparisons. ANOVAs were also used to compare
the mass change of each species on excised versus intact leaves.
Differences among the three plusiine species in trenching
scores were assessed with nonparametric Kruskal-Wallis tests. For
plusiine species that varied in trenching, we tested for correlations
between trenching score and mass change using Spearman rank
correlations.
Fig. 1 Change in mass (mean±SE) of final-instar plusiine larvae
over 24 h. The larvae were offered either excised or intact leaves
of prickly lettuce, Lactuca serriola (n=9 larvae/treatment). Species
that differ significantly (P<0.05 Tukey) in mass change have dif-
ferent letters above the bars (lowercase letters for excised leaves,
uppercase letters for intact leaves). Significant differences within a
species in mass change on excised versus intact leaves are indicat-
ed above the line connecting the contrasted pair (*P<0.05;
**P<0.001; ANOVA)
In the survival experiment, we tested for differences between
species and between leaf treatments (excised versus intact leaves)
in the number of larvae surviving to pupation with Fisher exact
tests (Daniel 1978). We did not use two-way ANOVAs to compare
caterpillar species in pupal mass or time to pupation because the
three plusiine species differed in size; we would therefore ex-
pect differences in development and pupal mass irrespective of
treatment. Instead, we used a multivariate analysis of variance
(MANOVA) for each species to examine the effect of leaf treat-
ment on pupal mass and time to pupation. Pillai’s trace was used
for hypothesis testing. Where significant, MANOVAs were fol-
Table 1 Analysis of variance for the effects of caterpillar species
and leaf treatment (excised vs intact leaves) on mass change of
plusiine larvae enclosed with prickly lettuce leaves for 24 h
Source
df
MS
F
P
Caterpillar species
Leaf treatment
Species×treatment
Error
2
1
2
0.003
0.026
0.004
0.000
18.247
151.522
22.157
<0.001
<0.001
<0.001
48

546
Fig. 2 Correspondence between mass change over 24 h and
trenching score for three plusiine species that were tested on intact
leaves of prickly lettuce, Lactuca serriola. Nine larvae were tested
for each species. Trenching scores: 1 no trench, 2 partial trench,
3 complete trench that was usually thick, 4 complete narrow trench
Fig. 3 Correspondence between mass change and trenching score
for individual soybean loopers, Pseudoplusia includens, on intact
leaves of prickly lettuce, L. serriola
Fig. 4A–C Performance of plusiine larvae reared from egg hatch
to pupation on prickly lettuce, L. serriola (n=9 larvae/treatment).
A Percentage of larvae that pupated. B Pupal mass (mean±SE). C
Time until pupation (mean±SE) for larvae that survived to pupate.
None of the R. ou and only one of the P. includens larvae on intact
leaves pupated
in weight by an astounding 179%, thus compensating for
the earlier period of starvation and documenting how
profoundly excision affects leaf acceptability.
Trenching scores differed significantly between the
three plusiine species (H=20.5, P<0.0001; Fig. 2). T. ni
larvae all cut excellent trenches (one 3 and eight 4s on
the 4-point scale) and gained mass. P. includens larvae head or legs in latex exudate, but all other larvae sur-
varied in trenching scores. Three of the four larvae with vived to pupate. In contrast, on intact leaves, survival
a trenching score of 2 or 3 gained mass, whereas all lar- differed dramatically. Significantly more T. ni pupated
vae that scored 1 lost mass (Fig. 3). Larval mass change than either P. includens or R. ou (P<0.005 for both com-
in P. includens correlated significantly with trenching parisons). P. includens and R. ou larvae both had lower
score (r=0.86, P<0.01). None of the R. ou larvae cut survivorship on intact leaves than on excised leaves
trenches (trenching score=1); all lost weight (Fig. 2).
(P<0.005). Most of the P. includens and all of the R. ou
In the survival experiment, all three species devel- on intact leaves died in the first instar. Two of the R. ou
oped rapidly on excised leaves. Pairwise comparisons larvae were stuck by their legs in exudate. Only a single
between species revealed no significant differences in P. includens larva pupated; this individual was also the
survival to pupation (P>0.05, Fisher exact tests; Fig. 4A). only soybean looper in the experiment that cut trenches
Two first-instar larvae of R. ou died trapped by their (trenching scores 3, 3, 3, and 4).

547
Fig. 5 Change in mass (mean±SE) of final-instar plusiine larvae
over 24 h. The larvae were offered either excised or intact leaves
of Italian parsley, Petroselinum crispum (n=9 larvae/treatment).
Species that differ significantly (P<0.05 Tukey) in mass change
have different letters above the bars (lowercase letters for excised
leaves, uppercase letters for intact leaves). Significant differences
within a species in mass change on excised versus intact leaves are
indicated above the line connecting the contrasted pair (NS not
significant; *P<0.05, **P<0.001, ANOVA)
Table 2 Analysis of variance for the effects of caterpillar species
and leaf treatment (excised vs intact leaves) on mass change of
plusiine larvae enclosed with Italian parsley leaves for 24 h
Fig. 6 Pupal mass (mean±SE) (A) and time until pupation
(mean±SE) (B) for plusiine larvae reared from egg hatch on Ital-
ian parsley, Petroselinum crispum (n=9 larvae/treatment)
df
MS
F
P
Caterpillar species
Leaf treatment
Species×treatment
Error
2
1
2
0.016
0.010
0.004
0.001
21.800
13.588
5.329
<0.001
0.001
0.008
T. ni and R. ou were variable (T. ni: four 1, one 3, four 4;
R. ou: one 1, six 2, two 4). Trenching scores did not cor-
relate significantly with mass change for either T. ni
(r=0.37, P>0.05) or R. ou (r=0.00, P>0.05).
48
Although all T. ni survived, leaf treatment affected
In the survival experiment, all larvae of all three spe-
larval performance as measured by pupal mass and time cies survived to pupate. However, leaf treatment signifi-
to pupation (MANOVA, F2,15=7.516, P=0.005). Pupal cantly affected performance of P. includens (MANOVA,
masses were smaller on intact leaves than on excised F2,15=9.143, P=0.003). Larvae on intact leaves had
leaves, although this difference was not statistically sig- smaller pupal masses (ANOVA, F1,16=5.040, P<0.04)
nificant (ANOVA, F1,16=4.054, P=0.06; Fig. 4B). Time and longer pupation times (ANOVA, F1,16=7.096,
to pupation was significantly longer on intact leaves P<0.02) than larvae on excised leaves (Fig. 6A,B). For
(ANOVA, F1,16=13.846, P<0.005; Fig. 4C).
T. ni and R. ou, pupal mass and development time were
not significantly affected by leaf treatment (MANOVA,
P>0.4 for each species).
Italian parsley
Plusiine growth in the 24-h experiment was affected by Discussion
an interaction between caterpillar species and leaf treat-
ment (Fig. 5, Table 2). All larvae on Italian parsley Unlike many groups of herbivorous insects, plusiines
gained weight, but there were significant differences be- vary enormously in diet and in diet breadth. The larvae
tween species in mass change on both excised feed on a diverse assortment of herbs, plus grasses, coni-
(F2,24=4.130, P<0.05) and intact leaves (F2,24=19.924, fers, poplars and other woody plants (Kitching 1987;
P<0.0001). R. ou larvae had similar mass changes on Lafontaine and Poole 1991). Some plusiines specialize
intact and excised leaves, unlike P. includens and T. ni on a single plant genus, whereas others feed on multiple
larvae which gained more mass on excised leaves genera in a single family or even on an assortment of
(Fig. 5).
families. The factors that allow plusiines to utilize so
Trenching scores varied substantially between species many different hosts and that cause divergence in diet
(H=10.9, P<0.005). All P. includens scored 1, whereas breadth are poorly understood.

548
Previous work has implicated trenching as an impor- for plusiine feeding on this species. Nevertheless, both
tant adaptation allowing polyphagous plusiines to feed T. ni and P. includens gained less weight on intact leaves
on hosts with defensive canal systems (Dussourd 1993; than on excised leaves in the 24-h experiment. P. in-
Dussourd and Denno 1994). The present study docu- cludens larvae, which were never observed to trench Ital-
ments variation among polyphagous species. T. ni larvae ian parsley, also had lower pupal weights and longer de-
cut trenches in both prickly lettuce and Italian parsley, velopment times on intact leaves. Whether the poorer
P. includens only trenched prickly lettuce, whereas R. ou performance of these larvae on intact leaves was due to
only trenched parsley. The behavior of the plusiines dif- secretory canals or to inducible responses, which have
fered markedly even though all three species are general been reported in parsley and another umbellifer (Kom-
feeders on herbaceous plants.
brink and Hahlbrock 1986; Zangerl 1990), is not known.
On prickly lettuce, trenching was mandatory for suc- Certainly, the oil ducts of Italian parsley were less effec-
cessful feeding. All T. ni trenched and gained weight, tive than the latex canals of prickly lettuce at deterring
P. includens larvae varied in trenching and performance, feeding by P. includens and R. ou. Either the greater vol-
whereas all R. ou failed to trench and starved. Excised ume of exudate in prickly lettuce, its chemical composi-
leaves were universally acceptable, documenting that tion or adhesiveness produced a more potent defense.
prickly lettuce provides adequate nutrition for all three
Early- and late-instar larvae performed similarly in our
species. The lack of trenching by R. ou was noteworthy experiments. For example, first-instar larvae of R. ou on
because eight of nine larvae on Italian parsley cut at least intact prickly lettuce all died in the survival experiment,
partial trenches. Prickly lettuce may not have elicited whereas the final-instar larvae all lost weight in the 24-h
trenching because it is an introduced species in North experiment. Performance was similar even though early-
America (Ryder and Whitaker 1976); perhaps insuffi- instar larvae do not have to trench in order to feed. First-
cient time has elapsed for R. ou to evolve adaptations for instar T. ni on intact prickly lettuce, for example, feed be-
exploiting this plant. However, R. ou larvae sleeved on a tween leaf veins, thereby avoiding laticifers concentrated
native congener, Lactuca canadensis, likewise did not in the veins. The larvae do not begin trenching until the
trench (D.E. Dussourd, unpublished data). On both Lac- second instar (Dussourd 1993). Nevertheless, first-instar
tuca species, the larvae left bite marks scattered around larvae of R. ou (also most P. includens) were unable to de-
the leaves, many with orange drops of dried exudate. An velop on intact prickly lettuce. Evidently, both early and
earlier study (Dussourd and Denno 1994) found that late instar larvae contact sufficient latex to deter feeding.
growth of the nontrenching generalist S. ornithogalli on
Feeding on intact prickly lettuce incurred costs even
prickly lettuce was comparable on excised leaves and on for larvae that cut trenches. For example, T. ni in the 24-h
leaf tips beyond trenches cut by T. ni. As with R. ou, experiment had a significantly lower mass change on in-
S. ornithogalli starved on intact prickly lettuce. Evident- tact leaves than on excised leaves. Likewise, larvae in
ly, if R. ou and S. ornithogalli could trench prickly let- the survival experiment took longer to develop a smaller
tuce, they could feed and develop. R. ou larvae fail to pupa on the intact leaves. Poorer performance on intact
utilize this potential host apparently because leaf chemi- leaves can be attributed in part to costs associated with
cals trigger a deterrence response instead of trenching.
trenching. Completing a single trench on prickly lettuce
P. includens was the only species that varied in trench- requires approximately 2 h (Dussourd 1999), time that is
ing on prickly lettuce. Individuals that did not trench all not available for feeding. In addition, trenching uses en-
lost weight in the 24-h experiment, whereas three of four ergy, exposes larvae to defensive compounds when exu-
larvae with trenching scores 2 or better gained weight. dates ooze onto the trench surface, and undoubtedly also
We do not yet know if only some larvae are capable of increases larval visibility to predators.
trenching or if all larvae trench, but only some are stimu-
The discovery of trenching in R. ou extends the previ-
lated to trench prickly lettuce. P. includens now feeds ex- ously known distribution of trenching behavior within the
tensively on soybean, which did not become an important Plusiinae. Specifically, R. ou is the first species known to
field crop in the US until the 1940s; in 1999, 72 million trench within the subtribe Autoplusiina of the tribe Plus-
acres were planted (Abelson and Hines 1999). Soybean iini, which has two other subtribes: Plusiina and Eu-
lacks secretory canals that emit exuclate (Dussourd and chalciina (Lafontaine and Poole 1991). Three genera of
Denno 1994). It is possible that selection for trenching in Plusiina also have trenching species: Anagrapha, Auto-
P. includens has diminished and that larvae lacking this grapha, and Megalographa (Dussourd and Denno 1991,
adaptation can now survive with little or no cost. We 1994). Another plusiine tribe, Argyrogrammatini, con-
have never found a soybean looper on prickly lettuce in tains the trenching genera Anadevidia (Takeuchi and Ta-
nature, although P. includens in the field do trench and mura 1993), Chrysodeixis (Compton 1989), Pseudoplusia
feed on cucumber (Cucumis sativus), which has exuding and Trichoplusia (Dussourd and Denno 1991, 1994). This
phloem sap, and on mulberry (Morus sp.), which emits broad distribution of trenching suggests that the trait ei-
latex (Dussourd and Denno 1994; D.E. Dussourd, unpub- ther appeared early in the evolution of the plusiines or has
lished data).
evolved repeatedly. Only one other noctuid species is
On Italian parsley, trenching scores varied both within known to trench: Amphipyra tragopoginis in the Amphi-
and between caterpillar species, but did not correlate pyrinae cuts trenches in dandelion and prickly lettuce
with performance. Evidently, trenching is not required (Dussourd and Denno 1991). Since the Amphipyrinae is

549
Gershenzon J, Croteau R (1991) Terpenoids. In: Rosenthal GA,
Berenbaum MR (eds) Herbivores: their interactions with sec-
ondary plant metabolites. Academic Press, New York, pp
165–219
distantly related to the Plusiinae (Mitchell et al. 2000),
trenching presumably evolved separately in this group.
In summary, plusiine performance differed within and
between caterpillar species, on different plant species,
and on leaves with intact or severed canals. Trenching
ability proved to be prerequisite, but not sufficient for
plusiine feeding on intact prickly lettuce. The larvae also
must be stimulated to trench and they must persist in
trenching despite latex exudation.
Gonzalez AG (1977) Lactuceae – chemical review. In: Heywood
VH, Harborne JB (eds) The biology and chemistry of the
Compositae. Academic Press, New York, pp 1081–1095
Hegnauer R (1971) Chemical patterns and relationships of Umbel-
liferae. In: Heywood VH (ed) The biology and chemistry of
the Umbelliferae. Academic Press, New York, pp 267–277
Kitching IJ (1987) Spectacles and silver Ys: a synthesis of the sys-
tematics, cladistics and biology of the Plusiinae (Lepidoptera:
Noctuidae). Bull Br Mus Nat Hist (Entomol) 54:75–261
Knogge W, Kombrink E, Schmelzer E, Hahlbrock K (1987) Oc-
currence of phytoalexins and other putative defense-related
substances in uninfected parsley plants. Planta 171:279–287
Kombrink E, Hahlbrock K (1986) Responses of cultured parsley
cells to elicitors from phytopathogenic fungi. Plant Physiol
81:216–221
Acknowledgements Thanks to K.C. Larson, D. Magoulick, H. Dukat,
and two anonymous reviewers for insightful comments that sub-
stantially improved the manuscript, to D. Magoulick for statistical
advice, to G.W. Felton and A. Mitchell for helpful discussion, and
to Sigma Xi and the University of Central Arkansas for financial
support.
Koopman WJM, Guetta E, Van de Wiel CCM, Vosman B, Van den
Berg RG (1998) Phylogenetic relationships among Lactuca
(Asteraceae) species and related genera based on ITS-1 DNA
sequences. Am J Bot 85:1517–1530
Lafontaine JD, Poole RW (1991) Noctuoidea, Noctuidae (part). In:
Dominick RB (ed) The moths of America north of Mexico,
fasc 25.1. Wedge Entomological Research Foundation, Wash-
ington, DC
References
Abelson PH, Hines PJ (1999) The plant revolution. Science
285:367–368
Angiosperm Phylogeny Group (1998) An ordinal classification for
the families of flowering plants. Ann Mo Bot Gard 85:
531–553
Berdegue M, White KK, Trumble JT (1997) Feeding deterrence of Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons.
Spodoptera exigua (Lepidoptera: Noctuidae) larvae by low
Clarendon, Oxford
concentrations of linear furanocoumarins. Environ Entomol Mitchell A, Mitter C, Regier JC (2000) More taxa or more charac-
26:912–919
ters revisited: combining data from nuclear protein-encoding
genes for phylogenetic analyses of Noctuoidea (Insecta: Lepi-
doptera). Syst Bot 49
Berenbaum MR (1990) Evolution of specialization in insect-um-
bellifer associations. Annu Rev Entomol 35:319–343
Bernays EA (1998) The value of being a resource specialist: be- Olson KC, Tibbits TW, Struckmeyer BE (1969) Leaf histogenesis
havioral support for a neural hypothesis. Am Nat 151:451–464
Bernays EA, Chapman RF (1994) Host-plant selection by phy-
tophagous insects. Chapman & Hall, New York
Bernays EA, Funk DJ (1999) Specialists make faster decisions
than generalists: experiments with aphids. Proc R Soc Lond B
266:151–156
Camm EL, Wat C, Towers GHN (1976) An assessment of the roles of
furanocoumarins in Heracleum lanatum. Can J Bot 54:2562–2566
Compton SG (1989) Sabotage of latex defences by caterpillars Ryder EJ, Whitaker TW (1976) Lettuce, Lactuca sativa (Composi-
in Lactuca sativa with emphasis upon laticifer ontogeny. Am J
Bot 56:1212–1216
Porter NG (1989) Composition and yield of commercial essential
oils from parsley. 1. Herb oil and crop development. Flavour
Fragrance J 4:207–219
Rees SB, Harborne JB (1985) The role of sesquiterpene lactones
and phenolics in the chemical defence of the chicory plant.
Phytochemistry 24:2225–2231
feeding on fig trees. S Afr J Sci 85:605–606
Craker LE, Simon JE (eds) (1986) Herbs, spices, and medicinal
tae). In: Simmonds NW (ed) Evolution of crop plants. Long-
man, New York, pp 39–41
plants: recent advances in botany, horticulture, and pharmacol- Schery RW (1972) Plants for man. Prentice Hall, Englewood
ogy, vol 1. Oryx Press, Phoenix
Cliffs, NJ
Crosby DG (1963) The organic constituents of food. I. Lettuce. Stahl-Biskup E, Wichtmann EM (1991) Composition of the essen-
J Food Sci 28:347–355
Daniel WW (1978) Applied nonparametric statistics. Houghton
Mifflin, Boston
tial oils from roots of some Apiaceae in relation to the de-
velopment of their oil duct systems. Flavour Fragrance J
6:249–255
Dussourd DE (1993) Foraging with finesse: caterpillar adaptations Sullivan MJ, Boethel DJ (1994) Loopers. In: Higley LG, Boethel
for circumventing plant defenses. In: Stamp NE, Casey T (eds)
Caterpillars: ecological and evolutionary constraints on forag-
ing. Chapman & Hall, New York, pp 92–131
DJ (eds) Handbook of soybean insect pests. Entomological
Society of America, Lanham, Md, pp 68–70
Sutherland DWS, Greene GL (1984) Cultivated and wild host
plants. In: Lingren PD, Green GL (eds) Suppression and man-
agement of cabbage looper populations. US Dep Agric Tech
Bull 1684:1–13
Dussourd DE (1999) Behavioral sabotage of plant defense: do
vein cuts and trenches reduce insect exposure to exudate?
J Insect Behav 12:501–515
Dussourd DE, Denno RF (1991) Deactivation of plant defense: Takeuchi M, Tamura M (1993) Trenching behavior of the cucum-
correspondence between insect behavior and secretory canal
architecture. Ecology 72:1383–1396
ber looper, Anadevidia peponis (Fab.)(Lepidoptera: Noctu-
idae) on cucurbit host plants. Jpn J Appl Entomol Zool
37:221–226
Dussourd DE, Denno RF (1994) Host range of generalist caterpil-
lars: trenching permits feeding on plants with secretory canals. Warning WC (1934) Anatomy of the vegetative organs of the
Ecology 75:69–78
parsnip. Bot Gaz 96:44–72
Eichlin TD, Cunningham HB (1978) The Plusiinae (Lepidoptera: Zangerl AR (1990) Furanocoumarin induction in wild parsnip: ev-
Noctuidae) of America north of Mexico, emphasizing genitalic
and larval morphology. US Dep Agric Tech Bull 1567:1–122
idence for an induced defense against herbivores. Ecology
71:1926–1932
Esau K (1940) Developmental anatomy of the fleshy storage or- Zangerl AR, Bazzaz FA (1992) Theory and practice in plant de-
gan of Daucus carota. Hilgardia 13:175–209
Fahn A (1979) Secretory tissues in plants. Academic Press, New
York
fense allocation. In: Fritz RS, Simms EL (eds) Plant resistance
to herbivores and pathogens: ecology, evolution and genetics.
University Chicago Press, Chicago, pp 363–391