Ingested Allelochemicals
in Insect Wonderland:
A Menu of Remarkable Functions
The Virtuosity of Insects in Adoptively
UtilizingPlant Compounds
H
MURRAY
222
s. BLUM
ERBIVORY BY INSECTS is not without its hazards. Many species of
plants synthesize an incredible potpourri of natural products, and these
compounds are often distasteful, emetic, and toxic to a variety of invertebrate and vertebrate herbivores. Ingestion of these allelochemicals by nonadapted
species may reduce fitness appreciably, resulting in insects having longer developmental times, smaller sizes, and, in some cases, reduced fecundity and fertility. In
essence, if specialist insect herbivores feed on plants that contain compounds as
diverse as cyanogens, alkaloids, cardenolides, and nitrophenanthrenes
(Blum
1981), these invertebrates must be able to process these natural products in a
manner that is very beneficial. At a glance, metabolism or elimination or both would
appear to be the most effective way of dealing with the intrusive natural products
that accompany the nutrients that fortify the preferred host plants of these
phytophages. And, while a variety of insect herbivores do metabolize and excrete
many of the natural products that they ingest (Rothschild & Reichstein 1976),
many others appropriate these compounds to subserve an incredible diversity of
significant functions. Indeed, this virtuosity of insects in exploiting plant compounds is so remarkable that it can best be described as better insect living (and
sometimes loving!) through plant chemistry.
The compounds that constitute allclochemical effronteries for most herbivores
have become of critical importance to a variety of specialists that feed on plants
containing these natural products. These phytophages have broken through the
plants' allelochemical defenses, and it is perhaps not surprising that some species of
insects have acquired these proven plant deterrents and utilized them as powerful
defensive allomones against the pathogens and predators with which they share
their fragile world (Bowers 1990). However, in addition to their proven defensive
roles, these compounds have been adapted by selected herbivores for a diversity of
functions including communication, reproduction, antibiosis, and feeding. Life on
toxic plants has provided these specialists with critical nutrients and equally
indispensable natural products that are required for their life support systems.
In the following discussion, allc10chemicals will be treated as non nutritive
organic compounds produced by one organism that affect the population biology,
growth, health and behavior of another species (Reese 1979). Selected
insect-allelochemical interactions are described below, with additional examples in
the references.
AMERICAN
ENTOMOLOGIST
Aggregation of first-instar
nymphs ofR. guttata.
Rothschild (1972), Rothschild and Reichstein (1976), Duffey (1980), Blum
(1981), and Bowers (1990) have documented the sequestrative propensities of a
multitude of insect herbivores that feed on plants fortified with a variety of natural
products. Sequestration can result in these compounds or their metabolites being
stored in different tissues, often rendering the insect distasteful to predators.
Furthermore,
the adults of many species (e.g., Danaus plexippus) sequester
compounds
that had been stored by their immature stages, an evolutionary
development that ensures that nectar-feeding adults will have access to secondary
plant compounds that they did not ingest (Nishio 1980). However, while the
storage of allelochemicals occurs with some frequency, especially among aposematic species, sequestrative
particulars
have often proven to be surprisingly
variable and unpredictable from species to species. Indeed, once an allelochemical
is sequestered, it may be utilized in a variety of ways that reflect the versatility of
these arthropods in adaptively processing plant natural products.
The Virtues of Sequestration
The exocrine glands of some species that synthesize a variety of effective
defensive allomones produce deterrent secretions that may be charged with
ingested plant natural products as well. For example, the metasternal defensive
gland secretion of the large milkweed bug, Oncopeltus fasciatus (Dallas), which
contains large amounts of aldehydic defensive allomones that are synthesized
anew, is also fortified with cardenolides
that have been sequestered from its
milkweed host plant (Duffey & Scudder 1974). The combination
of plant allelochemicals and endogenously
synthesized defensive compounds
undoubtedly
increases the deterrent "punch" of the glandular exudate. The same is true of the
acridid Romalea guttata (Houttuyn), a generalist that enhances the repellency of its
metathoracic glandular secretion by facilely sequestering a variety of plant allelochemicals in the gland (Blum et al. 1990).
Some species of insects discharge defensive exudates that are, for all intents and
purposes, solutions of ingested plant allelochemicals or their metabolites. These
chemical arsenals are especially adaptive for their insect sequestrators since many
of these plant compounds have been demonstrated to be toxins or repellents or both
for a wide range of herbivores. In addition, this biomagnification
of the plant's
allelochemical weaponry results in an effective defensive exudate without requiring
Additives in Defensive Glands
••••••••••••••
Winter 1992
••••••••••••••
223
American chameleon, Anolis
carolinensis, vomiting R. guttata
adult protected by plant
allelochemicals.
that the insect evolve a major biosynthetic pathway for the deterrent compounds.
A variety of insect species have adapted plant allelochemicals, or their simple
metabolites (e.g., oxidation products), to function as the repellent mainstays in
their glandular secretions.
The pyrgomorphid grasshopper Poekilocerus bufonius (Klug) selectively sequesters cardenolides from its milkweed host and utilizes these compounds as the
main deterrents in its bilobed defensive gland (von Euw et al. 1967). P. bufonius
is obviously a selective sequestrator, because only two of the six cardenolides in its
host plant are stored. On the other hand, larvae of the swallowtail butterfly
Atrophaneura alcinous (KIug) sequester all seven of the aristolochic acids found in
the leaves of its host plant, and these compounds, which are biomagnified in the
osmeterial secretion, are the major deterrents for birds in the defensive exudate
(Nishida & Fukami 1989).
Discharges from Specialized
Nonglandular Reservoirs
Some species of insects sequester allelochemicals in nonglandular organs which
nevertheless can evacuate their contents upon demand. The European pine sawfly,
Neodiprion sertifer (Geoffrey), sequesters mono- and sesquiterpenes from its pine
host, and these compounds constitute effective deterrents for a variety of predators
(Eisner et al. 1974). The pine-derived terpenes are stored in the capacious
diverticular pouches of the foregut and can be discharged even when a larva is
enclosed in its cocoon before pupating.
A remarkable defensive system has been evolved by many species of Iygaeids
which sequester the cardenolides from their milkweed host plants in dorsolateral
spaces on the thorax and abdomen (Scudder & Duffey 1972). For example, in O.
fasciatus high concentrations of cardenolides (e.g., 70-110 J..Ig.) may be stored in
these spaces, resulting in a potential predator being exposed to a highly concentrated deterrent discharge. Significantly, the cardenolides are sequestered by a
physical process which may require little or no overt energy expenditure, thus
enabling the lygaeid to "capture" its host plant's allelochemicals at no great cost
(Duffey et al. 1978).
224
AMERICAN
ENTOMOLOGIST
When tactually stimulated, as if by a predator, many insects will either regurgitate or defecate or both as an act of enteric defiance. This behavior can cause the
externalization
of ingested plant natural products, many of which constitute
allelochemical repellents for many species of insects. In essence, the intestines of
insects such as grasshoppers arc cannons primed to "fire" allelochemical "bombs"
at their adversaries. Vomiting has seldom been put to a more effective usc!
Eisner (1970) has demonstrated that the regurgitates from two species of acridids
arc repellent to ants. These enteric discharges arc fortified with plant natural
products that possess deterrent properties. Assuming that these compounds arc not
facilely degraded, they provide the insect with the plant's chemical weaponry that
has already been tried and tested successfully against insects. Detoxication of the
allclochemicals by the herbivore could result in a loss of their repellent properties
and would be maladaptive vis-a-vis predators. On the other hand, these plantderived products could be biotransformed
into more toxic compounds with greater
repellencies than their precursors (Blum 1981). This hypertoxication
would result
from the insect utilizing ingested allelochelmicals as precursors for the generation
of enteric deterrents with greater potencies than the phytochemicals.
Similarly, anal discharges by insects such as grasshoppers can excrete allelochemical deterrents so that the hindgut becomes a defensive organ. Defecation
occurs widely in tactually stimulated insects (e.g., O. fasciatus) and thus may be
regarded as a first line of defense (Blum 1981). In addition, plant natural products
that have accumulated as the meconium of endopterygote pupae can be "fired" at
predators by the freshly emerged adult (Blum 1981). Ultimately, feces charged with
allelochemicals will probably be demonstrated to be a widespread chemical defense
of arthropods.
Regurgitation and Defecation
of Allelochemicals
The malonty of species that sequester plant natural products store these
compounds or their metabolites in a variety of tissues. The acquisition of these
compounds can provide their sequestra tors with considerable protection against
predators, because these allelochemicals often arc known to be unpalatable and
emetic. This biomagnification
of plant allelochemicals belonging to a variety of
chemical classes has been documented for many species of insects (e.g., Arctia caia
[L.]) (Rothschild 1972) as testimony to the virtuosity of these invertebrates as
sequestrators. These insects may selectively sequester only some of the allomones
belonging to a single chemical class while eliminating related compounds rapidly
(Blum 1983). As a consequence, minor compounds may be biomagnified considerably, and the qualitative and quantitative sequestration patterns may bear little
resemblance to the allelochemical fingerprint possessed by the host plant. Significantly, sequestration occurs in sites that will be encountered readily by even the
most cunning predator.
Larvae of the monarch butterfly, Danaus plexippus L., utilize the large volume
of gut fluid as the critical factor in the processing of cardenolides ingested from their
milkweed host plants. This fluid is fortified with polar cardenolides, and during
pupal and adult development
these steroids are rapidly exchanged with the
hemolymph, providing the insect with a readily available source of sequestrable
compounds (Nishio 1980). Larvae can regurgitate gut fluid readily, giving them a
cardenolide-rich shield that can be thrust at predators. In addition, the cardenolides
arc channeled to the cuticle where they can constitute the first line of defense. Larval
exuviae are rich in cardenolides, and the discarding of these tissues at molting
constitutes a form of excretion for these compounds. The prepupal molting fluid is
also rich in card enol ides, again providing the developing insect with a potential
allelochemical
shield (Nishio 1980). The pupal exuvium is also fortified with
cardenolides, but the steroid-rich gut fluid diminishes in volume as it is converted
to hemolymph
in preparation
for the dynamic events which characterize the
processing of these compounds in the eminently aposematic and unpalatable adult.
The cardenolide-rich gut fluid reappears in the teneral adult only to be converted
to hemolymph during subsequent development. Ultimately, these bitter-tasting
steroids arc concentrated
in the wing scales and hemolymph, the latter fluid
Biomagnification
Winter 1992
in Tissues
225
providing the butterfly with a source of these compounds during its adult life
(Nishio 1980). Concentration of cardenolides in the wings provides the imago with
a readily available defense against aggressive avian predators that may discriminate
against monarchs as food after tasting or ingesting wing fragments. The steroid-rich
hemolymph also renders the adult unpalatable
and, in addition, provides the
butterfly with a pool of steroids that can be allocated to different tissues as needed.
Thus, the sequestration
of milkweed steroids by monarch larvae provides all
developmental stages with a formidable chemical defense that has been adapted to
optimally meet the particular requirements of each stage.
Sequestration
in Eggs
The ability of adults to biomagnify allelochemicals, often acquired during their
larval development, provides the imagos with an excellent reservoir from which
these compounds can be allocated as needed. As if closing the sequestrative circle,
evidently the plant natural products ingested and biomagnified by the larvae (e.g.,
D. plexippus) often are sequestered in the oocytes developing in the abdomen of the
female (Nishio 1980). This generational
sequestration
endows the developing
embryo with the chemical defense system of its mother, and its adaptive significance
vis-a.-vis small predators may be considerable.
The sequestration of different classes of allelochemicals in insect eggs is widespread in aposematic species that develop on toxic plants (Brown 1984). In addition
to pyrrolizidine alkaloids, insects sequester cardenolides, aristolochic acids, cannabinoids, quinones, etc., and these compounds are channeled to the eggs as further
testimony to their reproductive value.
A Copulatory
Bonus
Males of several species of ithomiine butterflies sequester ingested pyrrolizidine
alkaloids, which are obtained from flowers (Eupatorieae) and decomposing foliage
(Boraginaceae) (Brown 1984). Males of some species channel about half of the
pyrrolizidine alkaloids to the spermatophore,
which is transferred to the female as
a copulatory bonus. Females, which are rarely found on pyrrolizidine alkaloid
sources, appear to obtain most of their alkaloids from males during copulation.
Females mate frequently, and as a consequence they may obtain considerable amounts
of pyrrolizidine alkaloids, which can be allocated to the different batches of eggs.
In a sense, the transfer of allelochemicals by the male to the female constitutes
the adaptive utilization of the same allomones by both sexes. The seminal ejaculate
becomes the vehicle for allomonal transfer, and the male reproductive glands, which
contribute the allclochemical to the seminal plasma, are actually functioning as
exocrine glands. The copulatory-bonus
strategy, which in effect considerably
increases the reproductive fitness of the female and the male, probably will be found
to be widespread in the Insecta. This is especially true if the sequestration of these
plant natural products in male accessory glands is not energetically prohibitive.
Synergists for Pheromones
226
One of the major alarm pheromones utilized by many species of aphids is (E)B-farnesene, a sesquiterpene that is discharged from the cornicles of stimulated
individuals. For most species of aphids this compound is a powerful releaser of
alarm behavior that may cause aggregations to disperse, causing both adults and
larvae to drop off the food plant. However, in the case of at least one species, (E)B-farnesene is a weak alarm pheromone, but the pheromonal response is substantially increased by synergists in the secretion. Surprisingly, these pheromonal
synergists are not synthesized, but rather they are derived from ingested allelochemicals that have been sequestered and channeled to the cornicles where they
become critical communicative
elements (Dawson et al. 1987).
The turnip aphid, Lipaphis erysimi (Kaltenbach),
responds weakly to (E)B-farnesene, but alarm behavior is increased considerably if a volatile fraction,
derived from the aphids, is combined with the sesquiterpene.
Aerial parts of turnip
(Brassica campestris) and shepherd's purse (Capse/la bursa-pastoris) yielded a
series of isothiocyanates which were also identified in extracts of 1. erysimi. These
AMERICAN EmOMOLOGIIT
compounds, which are products of the aphid's cruciferous host plants, are generated from glucosinolate precursors that are enzymatically metabolized by the aphid.
Whereas compounds such as 3-butenyl isothiocyanate and allyl isothiocyanate are
weak alarm releasers for L. erysimi, they are powerful synergists for (E)-Bfarnesene, producing a five-fold increase in the response (Dawson et al. 1987).
Furthermore, in addition to their pheromonal role, the isothiocyanates are strong
phagostimulants
for L. erysimi. Clearly, for this aphid species, these allelochemicals
are essential for functions as disparate as feeding and communication.
The cuticular coloration of many species of insects is diet dependent and is highly
adaptive as a consequence of the insect's ability to respond to the color of its
background. In many cases, these diet-induced changes result in the insect displaying homochromy (background matching), guaranteeing that it will be appropriately
cryptic in its habitat. On the other hand, aposematic and toxic species may exhibit
heterochromy
(background contrasting) as a response to allelochemicals in their
host plants. It seems certain that the allelochemical bases for the diet-induced
coloration of many lepidopterous and hemipterous species are the carotenoids that
fortify their host plants.
The large white butterfly, Pieris brassicae (L.), is an aposematic species in all
stages and is toxic as well. When reared on standard cabbage leaves, diapausing
pupae are invariably green and contain large amounts of carotenoids and lutein in
particular (Rothschild et al. 1977). These pupae contrast to the background
coloration, and the carotenoid lutein was concentrated in the epidermis and cuticle.
On the other hand, insects reared on an artificial diet virtually lacking in carotenoids
possessed a turquoise-blue
coloration and exhibited no response to background.
However, the normal green heterochromic coloration results iflutein is added to the
artificial diet, and some of these pupae contrast with the background.
For P.
brassicae, about 1 Jlg. of carotenoid is required to produce heterochromy in the
pupal stage (Rothschild et al. 1977).
Carotenoids appear to be of widespread importance in contributing to color
modifications of many lepidopterans as well as species in several other orders. In
particular, these pigments can provide the insect with the homochromic coloration
required to match its background and render it inconspicuous under field conditions. The importance of an insect possessing cryptic coloration is often evident
when these arthropods are reared in the laboratory on diets that are essentially free
ofcarotenoids.
For example, larvae of the tobacco hornworm, Manduca sexta (L.),
are bright blue when reared on an artificial diet, whereas the larvae developing on
leaves in the field are green. Lab-reared larvae would contrast flagrantly with green
leaves and be very conspicuous to omnipresent avian predators, whereas green
larvae, fortified with ingested carotenoids, would be eminently cryptic.
Tissue Colorants
••••••••••••••
Insects, especially those species that are generalist herbivores, may ingest a
variety of toxic plant natural products that must be processed effectively. The
pronounced
mithridatism
that characterizes
so many stenophagous
species of
insects reflects the availability of diverse mechanisms for blunting the toxic effects
of the allelochemicals that fortify their host plants.
Detoxication is one of the major mechanisms for coping with plant allelochemicals, the compounds
frequently being converted from lipophilic substances to
hydrophilic ones that can be readily excreted. Mixed-function
oxidases, and in
particular cytochrome P-450, are frequently involved in the metabolism of plant
natural products, and the levels of these oxidizing enzymes may determine the
degree of tolerance an insect exhibits for a particular allelochemical. For example,
a diversity of plant natural products induces cytochrome P-450 in the southern
armyworm, Spodoptera eridania (Kramer) (Brattsten et al. 1977). Compounds as
structurally disparate as (+ 'oa-pinene and sinigrin rapidly induce enzymatic increases of two- to threefold in larvae. Indeed, the rise in cytochrome P-450 activity
is immediate and proceeds rapidly over much of its course during the first few hours.
Inducers of Detoxifying
••••••••••••••
\Vinrer1992
Enzymes
227
The induction of cytochrome P-450s by dietary allelochemicals may be particularly significant for both generalist and specialist herbivores. In the case of
generalists, ingestion of a potpourri of often highly concentrated natural products
derived from diverse plant species may result in induction of a variety of these
oxidative enzymes, enabling the insect to cope with the manifold allelochemicals
identified with its polyphagous diet. Specialists normally may be faced with high
concentrations of natural products that are characteristic of the food plant species
on which they develop. High levels of appropriate cytochrome P-450s may playa
leading role in adaptively processing the compounds that have been identified as the
chemical arsenal of the plant for nonadapted insect species.
Quenchers of
Phototoxic Phytochemicals
Antibiotic Functions
228
A variety of plant species generates photo-activated compounds that are highly
toxic to insects after ingestion. These phototoxins can act as photosensitizers
generating highly toxic species of oxygen including singlet oxygen and free radicals.
These forms of oxygen manifest their pronounced toxicity by oxidatively transmogrifying a variety of key biochemicals such as nucleic acids.
On the other hand, if a herbivore simultaneously ingests allelochemicals that are
effective quenchers of toxic oxygen species along with the phototoxins, then
survival-and prosperity-are
possible on diets fortified with photo-activated
natural products. The availability of allelochemical antioxidants has enabled some
insect species to utilize some species of food plants that are "forbidden fruits" for
most herbivores.
Larvae of the tobacco hornworm are very sensitive to the phototoxin a-terthienyl,
a thiophene found in many plants in the family Asteraceae. On the other hand, the
concomi tant ingestion of b-carotene (0.1 %) reduces mortali ty from 55% (controls) to
3% (+ carotene) during 48 hours (Aucoin et al. 1990). This carotenoid, which is an
effectivequencher of toxic oxygen species, is concentrated in the tissues of the larvae
where it can serve as a potent antioxidant for photoactivated toxins found in its food
plant. Tissue storage of allelochemical antioxidants may constitute a common
biochemical adaptation for species that develop on plants containing phototoxins.
Many plant natural products exhibit well developed antibiotic activities against
a wide variety of microorganisms, so perhaps it is not surprising that some insects
have utilized these compounds to subserve the role of biocides against diverse
pathogens. Significantly, the phytochemical defenses of plants may be directed
against prokaryotes as well as eukaryotes, so that a specialist herbivore, adapted for
feeding on a toxic plant species, may derive an incidental antibiotic benefit by being
associated with this plant. The already demonstrated range of antimicrobial
activities of allelochemicals against insect-asssociated viruses, fungi, and bacteria
makes it probable that these arthropods have commonly exploited plant compounds as key elements in their phytochemical pharmacopoeia.
a-Pinene, a monoterpene commonly produced by a variety of conifers, is
inhibitory against diverse microorganisms including the insect pathogen Bacillus
thuringiensis. This compound, along with several other monoterpenes, strongly
reduces the infectivity of B. thuringiensis spores for larvae of the Douglas fir tussock
moth Orgyia pseudotsugata (McDunnough) (Andrews et al. 1980). At concentrations approximating those found in fir needles, a-pinene increases the 50% lethal
dose for B. thuringiensis by 700 fold.
A pathogenic fungus Nomuraea rileyi frequently attacks lepidopterous larvae
such as the corn earworm, Helicoverpa zea (Boddie). However, the pathogenicity
of N. rileyi can be diminished considerably if the larvae have ingested a-tomatine,
a characteristic alkaloid of tomato plants (Gallardo et al. 1990). a-Tomatine
increases survivorship of larvae exposed to a LC concentration of fungal conidia;
at the LC90 concentration the alkaloid inhibit~Odevelopment of the fungus. In
addition, because a-tomatine is toxic to larval parasitoids of H. zea (Duffey et al.
1986), it is obvious that this lepidopteran has exploited effectively the chemical
defense of the tomato plant.
AMERICAN
ENTOMOLOGIST
The susceptibility of H. zea to viral pathogens also is influenced by host plant
allelochemicals. A common plant phenolic, chlorogenic acid, is oxidized by foliar
polyphenol oxidases to chlorogenoquinone, a highly reactive alkylating agent, that
binds to the occlusion bodies of a nuclear polyhedrosis virus (Felton & Duffy 1990).
Binding of the oxidized chlorogenic acid to this baculovirus is associated with a
reduction in digestibility and solubility under alkaline conditions with a concomitant decrease in infectivity. It is proposed that the liberation of infective virons in
the midgut, a requirement for successful infection, is impaired by the binding of the
ortho-quinone of chiorogenic acid to the baculovirus. These results demonstrate
that the infectivity of viruses to insects can be compromised by allelochemicals and
enzymes that the insect has appropriated from its host plant. Indeed, for many
herbivores the food plant may constitute both a restaurant and a pharmacy.
Some phytochemicals are present in the plant in a nontoxic form only to be
converted to toxic compounds after ingestion by herbivores, much like a prodrug.
Such is the case for many cyanogens that generate hydrogen cya~ide after the leaf
surface is broken, as would occur during feeding by a phytophage. It now appears
that cyanogenesis in damaged leaves may be inhibited by allelochemicals that arc
compartmentally isolated from the cyanogens in intact leaves.
Leaves of papaya, Carica papaya, contain two cyanogenic glycosides that yield
hydrogen cyanide after hydrolysis with b-glucosidases. However, cyanogenesis is
inhibited quantitatively by the addition of either condensed or hydrolyzable tannins
(Goldstein & Spencer 1985). Herbivores that are adapted for feeding on plants rich
in cyanogens may maximize contact between b-glucosidases and tannins, thus
promoting the possibility that highly toxic hydrogen cyanide will not be generated
after ingestion of leaf materials. It will not prove surprising if other classes of
allelochemicals, yielding toxic compounds only after the plant is damaged and
cellular contents mixed, as would occur in the gut of a herbivore, are prevented from
manifesting their toxicities by concomitant inhibitory allelochemicals.
In some cases, after ingestion of leaf material, insects have channeled a plant
natural product to a defensive gland, where this phytochemical is converted to a
compound that is very suitable as a defensive allomone. This is especially true for
chrysomc1id larvae that feed on species of Salix and Populus (Salicaceae), the leaves
of which generally contain the phenylglucoside salicin, a known feeding deterrent.
Chrysomc1ine larvae exploit salicin in order to generate a defensive allomone that
is a powerful repellent for insects.
The defensive glands of larvae in the genera Chrysomela and Phratora discharge
a secretion that is thoroughly dominated by salicylaldehyde, which has been derived
from the ingested allclochemical salicin (Pasteels et al. 1983). The concentration of
the aldehyde in the exudate is directly correlated with the concentration of salicin
in the larval food plant. The enzyme b-glucosidase, which is required to hydrolyze
salicin to the aldehydic precursor, is concentrated in the larval defensive glands.
Hydrolysis converts salicin to saligenin, which is quite toxic, and glucose. However,
saligenin can be facilely oxidized by an oxidase to salicylaldehyde, which in effect
rapidly removes the toxic intermediate from the glandular system. Although
salicylaldehyde is a rather irritating compound itself, its production occurs in the
isolated defensive glands, which are rich in the two enzymes required to produce the
final aldehydic product.
Chrysomeline larvae (Phratora sp.) are very efficient in processing salicin, most
of which is excreted as salicylaldehyde. In addition, the biosynthesis of this aromatic
aldehyde by these larvae is relatively inexpensive in terms of the energetic expenditure that would be required to resynthesize a defensive compound such as occurs
in other species of chrysomelines (Pasteels et al. 1983). And since salicylaldehyde
is a far more effective repellent than salicin, the biotransformation of the latter into
the former is highly adaptive for the larvae, which may have frequent confrontations with efficient predators such as ants.
Winter 1992
Inhibitors of Toxin Production
• •••••••••••••
Allomonal Precursors
••••••••••••••
229
Defensive froth of adult of
R. guttata. This secretion is
fortified with repellent plant
al/elochemicals.
Metabolites in Primary
Metabolic Pathways
230
Some specialist herbivores metabolize the characteristic allelochemicals of their
host plant and subsequently utilize the products as key intermediates in metabolic
pathways that are of major significance in growth and development. In essence,
these plant natural products, which are sometimes referred to as secondary plant
compounds, have been adapted to function as primary substances in much the same
way as primary nutritional constituents. Indeed, these specialist phytophages
thoroughly exploit their host plants by utilizing not only primary nutrients for
growth but allelochemicals as well.
Larvae of the bruchid beetle Carydes brasiliensis Thunberg develop exclusively
on seeds of the legume Dioc/ea megacarpa, which are fortified with L-canavanine,
a nonprotein amino acid analog of L-arginine. Nonadapted insect species cannot
discriminate between canavanine and arginine and incorporate the former into
proteins, which results in the production of transmogrified proteins of little
functional value-a situation that easily can lead to death. On the other hand, what
AMERICAN ENTOMOLOGIST
is poison for most insects is meat for larvae of C. brasiliensis, which grow rapidly
on their canavanine-fortified diet.
These bruchid larvae readily discriminate between canavanine and arginine, so
that canavanyl proteins are not synthesized (Rosenthal et al. 1978). On the other
hand, larvae of C. brasiliensis metabolize canavanine into products of great
metabolic significance. Canavanine is converted to another toxic amino acid,
canaline, and urea as well. High levels of urease convert the urea into ammonia for
fixation into organic compounds. Additional utilizable nitrogen is generated from
the detoxication of canaline, which yields large amounts of ammonia. In addition,
homoserine, a readily metabolized amino acid, is produced from canaline, thus
conserving the carbon skeleton of canavanine. In essence, the degradation of
canavanine by C. brasiliensis larvae provides ammonia for nitrogen metabolism
and an amino acid that can be readily metabolized.
Similarly, chrysomelid larvae feeding on Salix spp. convert a toxic allelochemical
into a metabolite with considerable importance in growth and development. These
larvae metabolize salicin, a phenylglucoside produced by Salix spp., into a defensive
allomone, as well as glucose (Pasteels et al. 1983). The production of glucose is of
great significance in terms of the growth rate of these larvae, accounting for about
32% of their daily caloric requirements. Clearly, salicin must be regarded as an
allclochemical nutrient.
The incredible dependency that insects can have on allelochemicals is illustrated
by arctiid moths in the genus Creatonotos. Larvae ofthese polyphagous species feed
on some plant species that contain pyrrolizidine alkaloids that are readily sequestered by the developing insects. These compounds are utilized as pheromones by the
adults, and, in addition, they possess a morphogenetic function for the developing
males. The size of the eversible abdominal androconial organs, the coremata, is
determined by the amount of pyrrolizidine alkaloids ingested by the developing
larvae (Boppn~ and Schneider 1985).
If the coremata are regarded as secondary sexual characters of the male moths,
then the pyrrolizidine alkaloids in effect are functioning as male hormones. Under
field conditions great variation in the size of these androconial organs occurs,
indicating that larvae ingested different amounts of the allelochemicals. Since
pyrrolizidine alkaloids also constitute precursors of the pheromones liberated from
the coremata, it is obvious that these compounds play a pivotal role in the
reproductive biology of Creatonotos species.
A Morphogenetic Role
••••••••••••••
For many species of insects, allelochemicals produced by their particular food
plants do not constitute dietary intrusions but rather are essential for feeding. These
compounds have become feeding stimulants for specialist herbivores, which may
starve to death in their absence. Furthermore, pharmacophagous species frequently
sequester these phagostimulatory allelochemicals, which render the insects eminently unpalatable because of their bitter or emetic qualities.
Adults of the turnip sawfly, Athalia rosae (L.), feed voraciously on the leaf
surface of a verbenaceous plant Clerodendron trichotomum that does not constitute a larval food plant. The leaf surface contains clerodendrins, diterpene allelochemicals that are responsible for the bitter taste of the leaves. The clerodendrins,
which are powerful phagostimulants for the adult tenthredinids, are subsequently
sequestered in the cuticle, which then possesses the characteristic bitterness associated with these compounds (Nishida & Fukami 1990). For the adult sawflies the
clerodendrins both promote feeding and provide a cuticular set of "armor" to
protect against aggressive predators.
Similarly, Nishida and Fukami (1990) demonstrated that members of three
genera of chrysomelid leaf beetles utilize triterpene cucurbitacins as phagostimulants that are biomagnified in the adult's body. Adults of Diabrotica sp., Cerotoma
sp., and Aulacophora sp. are induced to feed by cucurbitacins that are selectively
sequestered, rendering the aposematic beetles very bitter. As is the case with the
Phagostimulants
••••••••••••••
~inrer1992
231
sawflies, the allelochemicals characteristic of the host plant are bifunctional for the
chrysomelids, first stimulating feeding resulting in ingestion of these compounds,
after which the plant natural products are sequestered, rendering the beetles very
distasteful. This scenario will be frequently encountered as the fates of bitter-tasting
phagostimulants are studied after their ingestion by specialist herbivores.
Structural Paint
Some insect herbivores create physical structures which may be impregnated
with allelochemicals that have been ingested, sequestered, and ultimately excreted
onto the structure. The consequences of this allelochemical "painting" may be
highly significant for the phytophage. Larvae of the parsnip web worm, Depressaria
pastinacella (Duponchel), may be representative of herbivores that have adapted
phytochemicals to function as agents of deterrence after application to silk-webbed
flowers serving as housing units.
One ofthe hosts of D. pastinacella is wild parsnip, Pastinaca sativa, a species that
produces highly toxic furanocoumarins. Web worms excrete some of these allelochemicals in the frass and, significantly, in the silk glands (Nitao 1990). Indeed,
ingested furanocoumarins are sequestered in the silk glands in high concentrations
before their incorporation into the silk, which is used to web the flowers in which
the larvae reside. Because the webworms are quite sensitive to ultraviolet light, the
presence of UV-absorbing furanocoumarins on their silken housing may be very
adaptive. In addition, because these phytochemicals possess antimicrobial activity
against both fungi and bacteria, the presence of these natural products on the silk
can act as a major barrier to pathogens. And it will not prove surprising if the
allelochemical-treated silk acts as a deterrent to predators as well. Webworm larvae
have insulated themselves from the hostile world around them by erecting an
allelochemical barrier. It is very likely that other specialist herbivores have similarly
exploited the toxic natural products that are characteristic of their host plants.
Pheromonal Precursors
For some species of insects, allelochemicals have assumed a critical communicative function. These species convert ingested plant natural products into compounds that are utilized as either sex or aggregation pheromones. The enzymatic
derivation of these chemical messengers from allelochemical precursors, in specialized metabolic pathways, further emphasizes that these phytochemicals may
ultimately be as important as the host plant's primary nutrients.
Bark beetles in the genera Dendroctonus and Ips utilize monoterpene alcohols,
derived from hydrocarbons produced by their host trees, as aggregation pheromones that launch mass attacks. For example, mature females of Dendroctonus
ponderosae (Hopkins) convert a-pinene into trans- and cis-verbenol as well as
myrtenol (Hunt & Borden 1989). These compounds, which are components of this
scolytid's aggregation pheromone, can be synthesized, for the most part, in the
absence of microorganisms. Similarly, males of Ips paraconfusus (Lanier) biosynthesize their aggregation pheromone by converting the monoterpene hydrocarbon
myrcene to ipsdienol and ipsenol (Hendry et al. 1980). Another pheromonal
component for this species, cis-verbenol, is derived from a-pinene (Renwick ct al.
1976). As was the case for females of D. ponderosae, males of I. paraconfusus
exhibited maximal biosynthetic competence after they had "matured," some weeks
after adult emergence (Hunt & Borden 1989).
Males of some species of butterflies (Nymphalidae) and moths (Arctiidae)
convert plant-produced pyrrolizidine alkaloids into sex pheromones that are
especially critical during courtship. These pheromones, which are externalized on
secondary male sexual structures such as androconia or hair pencils (coremata), are
produced by a wide range of species in the nymphalid subfamilies Danainae and
Ithomiinae as well as at least five genera of arctiids (Boppre 1990). The pyrrolizidine
alkaloids may be obtained from damaged plants by the males, which biotransform
these esters into characteristic pheromones such as danaidone and danaidal. For
these males, the acquisition of the plant's allelochemicals is the key to reproductive
success. Ultimately, for these male lepidopterans, reproductive fitness is identified
232
AMERICAN
ENTOMOLOGIST
with their ability to locate pyrrolizidine
allclochemically exploi ted.
alkaloid-<:ontaining
plants that can be
Allelochemicals have otten been regarded as secondary plant substances whose
principal function is to deter herbivores. On the other hand, the question of how
adapted herbivores cope with these allelochemical effronteries is now being
addressed, and surprisi ng answers are emerging. Once an insect has broken through
the plant's chemical defenses, this phytophage may have access to a veritable
cornucopia of allelochemicals that can be exploited. That this has happened
frequently is evident from the fact that unrelated insect groups utilize different
allelochemicals for the same function. Sequestration of unpalatable compounds
occurs widely in the Insecta, and these compounds have been generally found to
have great deterrent value. A variety of insect species has utilized these proven insect
deterrents as defensive allomones that are secreted from reservoirs upon demand.
These defensive roles for insect-appropriated
allelochemicals contrast markedly
with the roles they play for other species.
The conversion of phytochemicals to pheromones or metabolic intermediates,
important to growth and development, provides additional grounds for regarding
these compounds as key elements in the biology of a variety of species. Additional
roles undoubtedly will be recognized as insects and their allclochemically fortified
host plants are subjected to further analytical scrutiny. These natural products
represent a marvelous resource for insect herbivores. Determining how these
arthropods have exploited the treasure trove of allelochemicals fortifying their
special host plants is a challenge that must be met if we are to understand how an
insect's lifestyle, predicated on an association with highly toxic plants, is both
possible and profitable.
I am grateful to an anonymous reviewer for helpful comments. I am particularly
grateful to David L. Wood who provided the in-depth review I would have
anticipated from one who shares my love for the wondrous hexapods with whom
we share this world.
Andrews, R. E., L. W. Parks & K. D. Spence. 1980. Some effects of Douglas fir terpenes on
certain microorganisms. Appl. Environ. Microbiol. 40: 301-304.
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effect of antioxidants to a phototoxin-sensitive insect herbivore, Manduw sexta. J. Chern.
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Conclusions
••••••••••••••
Acknowledgment
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0
Murray S. Blum is Research Professor of Entomology and Director of the
Laboratory of Chemical Ecology, Department of Entomology, University of
Georgia, Athens, GA 30602. He studies the chemisociality of ants and bees,
emphasizing the roles of their pheromones and al/omones as behavioral regulators.
In addition, he explores the relationships of herbivores and toxic plants in an effort
to describe the herbivory that characterizes these insects.
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ENTOMOLOGIST