Herbivore handling of a plant's trichome: The case of Heliconius charithonia (L.) (Lepidoptera : Nymphalidae) and Passiflora Lobata (Killip) Hutch. (Passifloraceae)

Abstract

Trichomes reduce herbivore attack on plants by physically and/or chemically inhibiting movement or other activities. Despite evidence that herbivores are negatively affected by trichomes there also reports of insect counter-adaptations that circumvent the plants defense. This paper reports on a study that investigated the likely mechanisms employed by larvae of the nymphalid butterfly, Heliconius charithonia (L.), that allow it to feed on a host that is presumably protected by hooked trichomes (Passiflora lobata (Killip) Hutch). Evidence were gathered using data from direct observations of larval movement and behavior, faeces analysis, scanning electron microscopy of plant surface and experimental analysis of larval movement on plants with and without trichomes (manually removed). The latter involved a comparison with a non specialist congener, Heliconius pachinus Salvin. Observations showed that H. charithonia larvae are capable of freeing themselves from entrapment on trichome tips by physical force. Moreover, wandering larvae lay silk mats on the trichomes and remove their tips by biting. In fact, trichome tips were found in the faeces. Experimental removal of trichomes aided in the movement of the non specialist but had no noticeable effect on the specialist larvae. These results support the suggestion that trichomes are capable of deterring a non specialist herbivore (H. pachinus). The precise mechanisms that allow the success of H. charithonia are not known, but I suggest that a blend of behavioral as well as physical resistance mechanisms is involved. Future studies should ascertain whether larval integument provides physical resistance to trichomes.

Full text

May - June 2008 247
ECOLOGY, BEHAVIOR AND BIONOMICS
Herbivore Handling of a Plant’s Trichome: The Case of Heliconius
charithonia (L.) (Lepidoptera: Nymphalidae) and Passifl ora lobata (Killip)
Hutch. (Passifl oraceae)
MÁRCIO Z. CARDOSO
Depto. Botânica, Ecologia e Zoologia, Centro de Biociências, Univ. Federal do Rio Grande do Norte, 59072-970
Natal, RN, mzc@cb.ufrn.br
Neotropical Entomology 37(3):247-252 (2008)
Interação Herbívoro-Tricoma: o Caso de Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) e Passifl ora
lobata (Killip) Hutch. (Passifl oraceae)
RESUMO - Apesar de as evidências mostrarem que herbívoros são negativamente afetados pelos
tricomas, há também relatos de contra-adaptações que sobrepujam as defesas das plantas. Este estudo
busca os prováveis mecanismos usados pelas larvas da borboleta ninfalídea Heliconius charithonia
(L.) que permitem que elas se alimentem de uma planta hospedeira que é, presumivelmente, protegida
por tricomas uncinados (curvados) (Passifl ora lobata (Killip) Hutch.). Para isso realizou-se observação
direta de movimento e comportamento da larva, análise de fezes, microscopia eletrônica de varredura
da superfície foliar e análise experimental do movimento de larvas em plantas com e sem tricomas
(removidos manualmente). O experimento foi feito comparando o comportamento dessas larvas
com o de larvas de um não-especialista, Heliconius pachinus Salvin. As larvas de H. charithonia
são capazes de se desvencilhar do aprisionamento pelos tricomas usando força física. Além disso, ao
movimentar-se, a larva espalha fi os de seda sobre os tricomas e retira suas pontas com as mandíbulas.
De fato, pontas de tricoma foram encontradas nas fezes das larvas. A remoção experimental dos
tricomas auxiliou o movimento da larva não-especialista, mas não teve efeitos notáveis sobre a
larva especialista. Os resultados confi rmam que os tricomas são capazes de deter um herbívoro não
especializado (H. pachinus). Os exatos mecanismos responsáveis pelo sucesso de H. charithonia ainda
são desconhecidos, mas sugere-se que a combinação de mecanismos comportamentais e de resistência
física estejam envolvidos e estudos futuros necessitam verifi car a possibilidade de resistência física
no tegumento das larvas.
PALAVRAS-CHAVE: Herbivoria, defesa mecânica, interação inseto-planta
ABSTRACT - Trichomes reduce herbivore attack on plants by physically and/or chemically inhibiting
movement or other activities. Despite evidence that herbivores are negatively affected by trichomes
there also reports of insect counter-adaptations that circumvent the plant’s defense. This paper reports
on a study that investigated the likely mechanisms employed by larvae of the nymphalid butterfl y,
Heliconius charithonia (L.), that allow it to feed on a host that is presumably protected by hooked
trichomes (Passifl ora lobata (Killip) Hutch). Evidence were gathered using data from direct observations
of larval movement and behavior, faeces analysis, scanning electron microscopy of plant surface and
experimental analysis of larval movement on plants with and without trichomes (manually removed). The
latter involved a comparison with a non specialist congener, Heliconius pachinus Salvin. Observations
showed that H. charithonia larvae are capable of freeing themselves from entrapment on trichome tips
by physical force. Moreover, wandering larvae lay silk mats on the trichomes and remove their tips
by biting. In fact, trichome tips were found in the faeces. Experimental removal of trichomes aided in
the movement of the non specialist but had no noticeable effect on the specialist larvae. These results
support the suggestion that trichomes are capable of deterring a non specialist herbivore (H. pachinus).
The precise mechanisms that allow the success of H. charithonia are not known, but I suggest that
a blend of behavioral as well as physical resistance mechanisms is involved. Future studies should
ascertain whether larval integument provides physical resistance to trichomes.
KEY WORDS: Herbivory, mechanical defense, insect-plant interaction

248 Cardoso - Herbivore Handling of a Plant’s Trichome: The Case of Heliconius charithonia (L.) (Lepidoptera...
The surface of many plant species are covered with
protective trichomes that can negatively impact wandering
herbivores by physically obstructing the animal’s movement or
releasing protective chemicals (Levin 1973, Van Dam & Hare
1998, Fordyce & Agrawal 2001). Plants of the genus Passifl ora
L. (Passifl oraceae) are better known for the employment of
cyanogenic-based chemical defense (Spencer 1988) than by
the use of physical defense against herbivores. Yet, in the
Pseudodysosmia Harms section [subgenus Decaloba (DC)
Rchb.)] of the Passifl ora all 18 species bear hollow, hook-
like structures known as uncinate trichomes (MacDougal
1994), that are very effective in deterring caterpillars of the
specialist herbivore Heliconius Kluk (Gilbert 1971). Among
the Passifl oraceae, uncinate trichomes are a unique feature of
the Pseudodysosmia group and are found in no other species in
the Passifl ora genus (MacDougal 1994).
Although butterfl ies in the Heliconiiti group (Heliconius
and related genera) are the major herbivores to attack Passifl ora
(Benson et al. 1975), Gilbert (1971) has shown that Heliconius
larvae die from entrapment in the hooks of the trichomes of
Passifl ora adenopoda DC. In fact, in view of the seemingly
insurmountable trichome defense, he stated that “it is diffi cult
to imagine how heliconiines might circumvent the highly
effective and specifi c mechanical defense of P. adenopoda
without drastic developmental alterations”. In fact, later
studies have found that hooked trichome Passifl ora species
are virtually free of herbivores aside from a small subset of
heliconiiti species (Benson et al. 1975, MacDougal 1994).
Indeed, only two species are commonly listed as herbivores:
Heliconius charithonia (L.) (Fig. 1) and Dione moneta Hübner
(Lepidoptera: Nymphalidae) (Benson et al. 1975, MacDougal
1994). Therefore, although trichomes seem to be highly
effective as a defense, some species have developed the ability
to somehow circumvent the physical barrier, perhaps through
developmental alterations as suggested by Gilbert (1971).
In view of the fact that, in general, some larvae of
Heliconius are unable to cope with the trichomes while
others are apparently unharmed, I set out to examine the
likely mechanisms employed by H. charithonia in order to
survive where other caterpillars perish. This report presents
observational as well as experimental data with the goal of
shedding light on this mechanistical question.
Material and Methods
The study was conducted using individuals collected from
populations housed in glass greenhouses (4 x 6.5 m) at the
University of Texas, Austin. Butterfl ies and the host plant
derive from founders collected in Sirena Station, Corcovado
National Park, Costa Rica. In Sirena, H. charithonia feeds on
Passifl ora lobata (Killip) Hutch., a member of the hooked
trichome clade (Gilbert 1984, MacDougal 1994).
Larval behavior. Observations on larval behavior were made
in the greenhouses directly on a full grown host plant, and in
the laboratory. Larval observations in the laboratory were made
on leaves collected in the greenhouse and kept in a vial with
water to prevent wilting. Larval behavior was observed with
the naked eye or under a scope, with the leaf slightly tilted so
as to see the contact between the caterpillar and the leaf surface.
The goals of these observations were to examine the general
behavior of the caterpillars when moving or foraging on a leaf
with trichomes. Most of these behavioral observations were
made with the specialist herbivore, H. charithonia. A sample
of faeces of H. charithonia larvae was diluted in distilled
water and examined for leaf remains, a technique commonly
employed in studying food choice in grasshoppers (Mulkern
1967). Additionally, opportunistic observations were made
with larvae of other heliconiiti species: Dryas julia (Fabricius),
Agraulis vanillae (L.) and H. erato (L.).
Experimental removal of trichomes. In order to ascertain
whether larval movement is arrested by the trichomes, late
instars (4th and 5th) of the specialist herbivore, H. charithonia,
and of the non-specialist, H. pachinus Salvin, were placed
on isolated P. lobata leaves and followed for several hours.
Selection of H. pachinus was made to increase phylogenetic
Fig. 1. A 5th instar larva of H. charithonia crawling on the leaf of P. lobata. The trichomes are the translucent structures
highlighted by the fl ash burst. The arrows point the sclerotized plates on the larval prolegs. Bar scale is ca. 1 cm. Photo by
Lawrence Gilbert.
→
→

May - June 2008 Neotropical Entomology 37(3) 249
independence, because it belongs to a clade distinct from H.
charithonia (Gilbert 1991).
Prior to larval placement, experimental P. lobata leaves
were subjected to a shaving treatment for trichome removal.
First, peeling was done by putting a stick tape on the leaf
surface and pulling it out repeatedly, until the investigator
deemed necessary. To ensure maximal trichome removal a
shaver was also used. After peeling, it was passed as close
to the surface as possible. Control leaves did not have their
trichomes removed. Treated and untreated leaves were paired
according to their size (as measured by the length of the main
vein). The place where the larva was initially put was recorded
on the leaf surface with a marking pen. Subsequently, larval
movement was monitored for 5h at intervals of 1.5h.
A larval movement was recorded as such every time
the larva moved away from the point where it was last
seen. No movement was recorded when the larva did not
move from the release point or from the point where it was
last recorded. The number of moves made by a larva was
counted and transformed into proportion of moves made
(out of four possible moves), ranging from zero (no moves)
to one (moved in all occasions). Since these data were not
normally distributed I used a Wilcoxon non parametric test
and compared movement rate for each species separately.
Trichome density. Observations of trichome characteristics
were made under a Bausch & Lomb Stereo zoom scope, with
the petiole immersed in water and with the light source aimed
at a 90° angle from the leaf blade. Because trichomes are
translucent and diffi cult to see under direct light, visibility
was improved by spraying a light powder onto the surface of
the leaf. Trichome density was estimated on a representative
leaf by counting the number of trichomes in fi ve randomly
chosen areas (10 x 10 mm quadrats) on both the upper and
lower leaf surfaces. Leaf area was estimated by scanning the
leaf and using imaging software to compute size (NIH Image
for the Macintosh).
Leaf SEM. Leaf samples of P. lobata kept in Sorensen buffer
were fi xed in 2.5% glutaraldehyde and rinsed in a buffer with
distilled water solution three times. Subsequently, samples
were dehydrated by an alcohol graded series (25-100%),
followed by critical point dry, stub mounting and metal coating
for SEM in a Hitachi S-340 scanning electron microscope.
Pictures were taken to characterize trichome morphology and
also to study damage caused by the herbivore. The areas of
the leaf where a larva had been observed under the scope were
marked and cut out for direct inspection.
Results
Larval behavior. In general terms, there is nothing special
about the larval behavior of H. charithonia that sets it apart from
other larvae. The crawling larva lays silk as it moves on the leaf
and, at times, a trichome would seem to disturb the movement.
For example, a leg would get stuck and, yet, the larva would
simply pull it away. Apart from that, the most striking behavior
was that the larva seemed to cut away some trichome tips as it
moved. While performing this task their mandibles would on
Fig. 2. Proportional number of moves made by 4th and
5th instar larvae of H. charithonia (bars on left) and H.
pachinus (bars on right) when left on P. lobata leaves that
had trichomes removed (peeled treatment – gray bars) or in
control leaves with trichomes (intact treatment – black bars).
Larval movements were recorded for 5h at intervals of 1.5h.
Numbers above bars refer to number of larvae tested and
lines are + 1 standard error. Movement rates were compared
between treatments within species using a Wilcoxon test. NS,
not signifi cant; *, P = 0.022.
0
0.2
0.4
0.6
0.8
1
Intact Peeled Intact Peeled
H. charithonia H. pachinus
3
2
4
5
NS
*
Total moves (proportion)
occasion get caught by the tip of the trichomes. Nevertheless,
the larvae would pull their mandibles without any visible harm.
Sometimes, that would make them spit gut contents. Most
interestingly, though, H. charithonia would bit the tips of the
trichomes in front of it. As a consequence, several trichome
tips were found in the faeces sample, confi rming the larvae’s
ability to handle the trichomes.
In some opportunistic observations, larvae of D. julia, A.
vanillae and H. erato were followed on the leaf of P. lobata.
D. julia moved as fast as H. charithonia. Leg pulling ability
was seen on Dryas and Agraulis but not on H. erato. In fact,
the single H. erato larva observed was trapped and dead 24h
later after being put on the leaf.
Experimental removal of trichomes. Removal of trichomes
increased movement of H. pachinus larvae (Fig. 2). On
average, larvae on control (intact) plants moved 12.5%, while
those on peeled leaves moved 75%. These differences were
signifi cant (Wilcoxon, χ2 approximation = 5.25, df = 1, P
= 0.022). In contrast, H. charithonia larvae moved equally
well in both treatments with a tendency to move more in the
treated leaf (62.5% vs. 83%, control vs. treatment; Wilcoxon,
χ2 approximation = 0.42, df = 1, P = 0.52) (Fig. 2)
Trichome density. Trichomes cover the whole plant in P.
lobata. Trichome distribution on leaves varies between upper
and lower surfaces, with more trichomes on the upper than
on the lower surface. On a representative leaf, the average
trichome density on the upper side was 15.8 ± 2.40 trichomes.
mm-2 (n = 5 quadrats), while on the under side the density was
4.4 ± 1.73 trichomes.mm-2 (n = 5), a signifi cant difference
(t-test, t = 8.6, df = 8, P < 0.0001). For an estimated leaf area
of 7.09 cm2, this gives an estimate of 11,202 trichomes on
the upper surface and 3,120 on the lower surface.

250 Cardoso - Herbivore Handling of a Plant’s Trichome: The Case of Heliconius charithonia (L.) (Lepidoptera...
ABC
D
EF
GH I
Fig. 3. Scanning electron micrography of samples of P. lobata leaves. A. General view of the leaf upper surface and
dispersion of hooked trichomes (magnifi cation and scale: 170X, 59 μm); B. Closer view of three trichomes. Notice the
hooked nature of the trichome tip and size differences between them (300X, 33 μm); C. Leaf vein and surface epidermis
covered with larval silk (113X, 88 μm); D. Trichome tip and the larval silk thread attached to it (1008X, 9.5 μm); E. Leaf
vein covered with silk thread (160X, 63 μm); F. Larval silk thread holding on to trichome structure. Notice that at least
three threads seem to tie it down (440X, 23 μm); G-I. Trichomes with tips removed by H. charithonia larva (300X, 33 μm;
160X, 63 μm; 160X, 63 μm, respectively).
Leaf SEM. The SEM pictures show a striking landscape (Fig.
3 A-I). The whole leaf blade is covered with menacing hooked
trichomes. Although trichome measurements were not made,
one can see at least two size classes with the same orientation
(Fig. 3 A,B). Trichomes seem to be densely spread on the leaf
blade (see section on estimates of trichome density), both on
the blade itself (Fig. 3 A,B) and on veins (Fig. 3 A,C,E-I). The
pictures in Fig. 3 also show the areas where the larvae crawled
(Fig. 3 C-I), revealed by the presence of fi ne thread lines. These
fi ne lines are larval silk spun by the caterpillars as a support
for movement, and cover most of the surface, including the
trichomes. In fact, perhaps adding insult to injury, trichomes
may be used as supports for laying down the silk thread (Fig.
3 D-F). One can also see that many trichomes have their
tips removed (Fig. 3 G-I), confi rming observations of larval
behavior made under the scope. Many trichomes present on
the main vein from the lower surface, where the larvae H.
charithonia move frequently, had their tips taken away.
Discussion
The role of trichomes as effective mechanical barriers
to herbivores is well established (Levin 1973, Valverde et
al. 2001, Hanley et al. 2007). In fact, both Gilbert (1971)
and Pillemer & Tingey (1976) demonstrated with stunning
scanning electron images of dead herbivores the dramatic
consequences of entrapment by hooked trichomes. Many
other studies have shown the negative effect of trichomes
on herbivores (e.g., Hoffman & McEvoy 1986, Wilkens
et al 1996, Van Dam & Hare 1998, Medeiros & Moreira
2002) by traits such as trichome presence, density, shape,
length and glandular nature (Voigt et al. 2007). In my study,
trichome presence and shape affected larval movement of
non specialist Heliconius, confi rming its defensive role. On
the other hand, movements by the specialist H. charithonia
were not signifi cantly affected by them, yet larvae tended to
wander more on the treated leaf. In fact, even for specialists,

May - June 2008 Neotropical Entomology 37(3) 251
trichomes may increase handling time and/or time spent
moving on a leaf (Fordyce & Agrawal 2001) and they
therefore incur a cost to the herbivore.
My observations on free ranging caterpillars showed
that they usually stay on the under surface of the leaf, where
trichome density is lower, crawling along the main vein up
to the tip of the leaf. The fact that many hookless trichomes
were found in this area suggests that hook removal may be
an important adaptation that enables H. charithonia to avoid
getting trapped by the trichomes, a behavior that seems to be
restricted to H. charithonia. Moreover, the fact that the larval
faeces contained trichome hooks (and not the whole trichome)
suggests that trichome trimming may be needed in order to
handle trichomes. Finally, the potential harm trichomes may
incur on a specialist was unknowingly demonstrated when
I dropped a H. charithonia larvae on a P. lobata leaf and
accidentally injured it; the larvae subsequently died.
Silk weaving may also be important because it provides a
surface to which the crochets can connect that is independent
of leaf anatomy (e.g., Rathcke & Poole 1975). However
this alone cannot be considered a key characteristic given
that larvae in general are known to weave in order to
create a stable surface on which to crawl (Alexander 1961,
Craig 1997, Sugiura & Yamazaki 2006). Quite possibly,
morphology (eg Medeiros & Moreira 2002, Medeiros &
Bolignon 2007) may be an important component of the suite
that enables H. charithonia to handle the plant’s trichomes.
For example, I noticed that crawling larva of H. charithonia
can actually pull their legs from the hold of the trichome
hook, something that larvae of D. julia and A. vanillae larvae
were also capable of doing. A preliminary inspection on the
legs of several Heliconius larvae did not reveal any noticeable
difference in crochet size, number or arrangement that would
explain this ability. However, the lateral sclerotized proleg
plate (Fig. 1) of H. charithonia is more pigmented, which
may indicate a tougher plate, and is similar in appearance to
the ones in Dryas and Agraulis. Could this help these larvae
avoid entrapment? This hypothesis clearly deserves further
investigation.
Although no specifi c characteristic can be pinpointed
as to how H. charithonia overcomes the host’s defenses, it
seems likely that a suite of behavioral (eg hook removal,
silk spinning) and mechanical traits (eg ability to detach
from trichome hook) allow it do so. It would be interesting
to ascertain whether there are costs associated with the
seemingly ample advantage of exploiting a host that is
unavailable to all other Heliconius. The herbivore offense
by H. charithonia larvae (Karban & Agrawal 2002) suggests
that it forages with fi nesse (sensu Dussourd 1993).
Acknowledgments
I would like to thank Larry Gilbert for enthusiastic
discussions regarding the project and for collecting P.
lobata for the experiments; R. Riess for helping in leaf tissue
preparation and SEM operation; J. MacDougal for providing
publication and discussions on the hooked Passifl ora; G.
Sword for suggesting the fecal analysis and A. Almeida,
A. Freitas and J. Vasconcellos-Neto for improvements to
the manuscript. Butterfl ies and plants were collected under
permits from the Costa Rican government to Larry Gilbert.
Thanks to CAPES for providing a doctoral fellowship.
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Received 17/X/06. Accepted 20/III/08.