Caterpillar Defense Systems: A Literature Review

ByGrant Monahan

2008

Caterpillars are tasty morsels. They are non-sexual, juvenile insects, whose

function is to feed and grow at a rapid pace. Due to their large intake of food,

caterpillars are extremely nutritious; their soft exoskeleton, which accommodates

rapid growth and minimal mobility, makes caterpillars a preferred prey for a variety

of predators.

The predators that most often feed on caterpillars fall into 3 categories:

invertebrate predators, parasitoids, or vertebrate predators. Invertebrate predators

include spiders, wasps, ants, beetles, true bugs, and other kinds of Arthropods.

Invertebrate predators obtain prey by using traps or webs, or may actively search

using chemical or visual cues. Parasitoids include species of wasps, flies, and

nematodes that use caterpillars as food for their developing young, laying eggs on,

in, or near their selected hosts. Many parasitoid larvae feed with in the host keeping

it alive long enough to complete their own development. Parasitoid wasps forage for

prey using mostly chemical cues that are either left by the caterpillar (e.g.,

accumulated frass, traces of silk), or those that are emitted by caterpillar-damaged

plants. Chemical cues provide consistent signals, making caterpillars easier to

locate and relocate (Turlings et.al., 1995; Gentry & Dyer 2002).

Common vertebrate predators of caterpillars include small mammals,

reptiles, and birds. These predators hunt primarily by using visual cues.

Caterpillars are an extremely important part of the diet of migratory birds, which

need to store large quantities of fat and nutrients for their long journeys (Holmes,

et.al. 1979; Stamp 1992). Multiple studies have shown that foraging by

insectivorous birds can dramatically alter the densities of caterpillars on a variety of

host plants (e.g., Marquis and Whelan 1994) and in so doing reduce the amount of

damage these plants suffer.

As caterpillars evolve more effective defenses their enemies evolve higher

tolerance for these defenses, or ways to avoid them. Thus, caterpillars and their

enemies become locked into a co-evolutionary arms race (Ehrlich & Raven 1964).

Because diverse types of predators and parasitoids attack caterpillars, they

have evolved a wide range of defensive adaptations. However, because each type of

predator has its own methods of finding and attacking caterpillars, there is no one

strategy that will protect a caterpillar from all enemies. Thus, it seems likely that

the defensive strategies employed by a given species of Lepidoptera represents a

tradeoff between the need to defend against the most common enemies and

acceptable losses to other kinds of predators. In this paper I will review the

defensive strategies, and where possible, I will illustrate them with examples from

my experimental study, and comment on the trade-offs that occur when a caterpillar

defense is most effective against one particular type of enemy (Monahan 2008).

Caterpillar Defensive Strategies

Gentry and Dyer (2002) pointed out that caterpillar defenses fall into three

categories: 1 those that function to prevent detection by enemies; 2 those that

function to prevent an attack once the larva is detected; and 3 those that function to

help a larva survive or defeat attack by parasitoids. Stage 1 defenses typically

include protective coloration and feeding behaviors that prevent enemies from

encountering the caterpillars. Stage 2 defenses include behaviors that are activated

once the caterpillar has been encountered and also structural and chemical

adaptations that cause the predator or parasitoid to call off its attack. Stage 3

defenses include immune system responses against parasitoid eggs or larvae.

Stage 1 Defenses

Caterpillars have evolved many strategies to camouflage themselves, a

phenomenon referred to as cryptic coloration. Lepidopterous larvae utilize many

different cryptic coloration strategies, which cause the caterpillars to look like leaf

coloration (Figure 1), leaf damage, leaf-edge, twigs, stems, bark, bird droppings,

flowers, pine needles, plant fibers, and grass blades (Wagner 2005). Some

caterpillars such as Synchlora aerata, attach pieces of vegetation and flowers to their

bodies to better blend into their environment (Wagner 2005). Most leaf-feeding

caterpillars exhibit counter shading, which means that the lower part of the body is

a lighter green than the upper body so that the caterpillar’s shadow does not effect

its overall coloration (Wagner 2005). Some caterpillars have hairs and spines that

are designed to look like moss or thorns. In our study, Schizura unicornis displayed

leaf edge crypsis (Figure 2), while Tortricidia testacea mimicked a leaf wound

(Figure 3). In the first three instars Papilio glaucus mimicked a bird dropping, and

we encountered at least 3 caterpillars that exhibited coloration of the host plant

including Paonias myops, which had color that matched the leaves of its host Prunus

serotina (Monahan 2008).

Being brightly colored acts as a warning to enemies if it is coupled with other

harmful defensive strategies, such as spines or hairs that contain venom, or

chemical defenses that impart a noxious smell or taste that cause regurgitation,

sickness, or even death. Bright coloration, which serves, as a warning of potential

harm to predators is known as aposematic coloration. Although such coloration

causes the caterpillar to be seen quite easily, it also warns the enemy not to attack

that larva. This defense is only effective against predators that can learn to

recognize such coloration and therefore is not effective against parasitoids and

invertebrate predators. Some species of caterpillar that have no harmful defensive

strategies mimic the bright coloration of those with harmful defensive strategies to

avoid being attacked by an enemy, a phenomenon known as Batesian mimicry

(Gentry & Dyer 2002, Witz 1989). In our study we encountered at least 3 species

that exhibited aposematic coloration including Automeris io, Parasa chloris (Figure

4), and Acharia stimulea all of which possess urticating spines.

Caterpillars have evolved many strategies to protect themselves while they

feed. These defensive strategies can be broken down into 2 main groups shelter

building (leaf tying, leaf folding, leaf mining, leaf rolling, and silk shelters), and

feeding behavior (gregarious feeding, nocturnal feeding, feeding only on the

underside of leaves, frequently changing leaves, and cutting of partially eaten leaves

to remove evidence of feeding)(Heinrich 1979). These strategies allow caterpillars

to feed relatively free from the sight of predators.

One of the most effective shelter building behaviors against vertebrate

predators is the construction of silk shelters (Figure 5). These caterpillars build a

silk shelter over their bodies. Many such caterpillars have elongated setae that

contact fibers of the shelter. Like a spiders web, the shelter acts as an extension of

the caterpillar’s nervous system. When a predator touches the silk, the caterpillar is

signaled to take evasive or defensive action (Rota & Wagner, 2008; Gentry & Dyer,

2002), often moving quickly to the other side of the leaf through a small hole,

puzzling the foraging predator with its disappearing act.

Leaf folding and leaf rolling conceals the caterpillar from the view of a

predator. The caterpillar puts silk on two parts of the leaf. As the silk dries, it

causes the leaf to fold or roll over the caterpillar, giving it a concealed place to feed.

Loeffler (1996) found that spiders and ants do not use folds as visual cues, and could

not open the fold to reach the concealed prey, but some species of birds use leaf

folds as visual cues, and are capable of opening the folds to reach the concealed

caterpillar. Some caterpillars mine into the leaf, and feed on cells between the two

layers of leaf cuticle. These aptly named leaf miners are protected from all

predators, but only microlepidoptera with their very small caterpillars can employ

this strategy (Gentry & Dyer 2002). In our study we encountered at least 6 as yet

unidentified species that exhibited some form of concealed feeding behavior

(Monahan 2008).

Stage 2 Defenses

Stage 2 defenses include those that are useful and practical once the

caterpillar has been encountered or attacked by a predator or enemy. These include

physical behaviors to deter attack (e.g., thrashing, biting, dropping, frass throwing,

and “freezing”), chemical defenses (e.g., use of an osmeterium, regurgitation,

sequestering plant toxins, and presence of venom), and morphological (structural)

defenses (e.g., presence of hairs and spines).

Behavioral defenses allow caterpillars to escape their predators. Thrashing,

and biting makes it hard for the enemy to capture and secure the caterpillar (Gentry

& Dyer, 2002). Some caterpillars drop off their host plant at the first sign of an

enemy or in response to vibrational cues. This evasive behavior causes the predator

to loose sight of the caterpillar in the safety of the leaf litter below (Gentry & Dyer,

2002). Some species of caterpillar use frass throwing as their primary behavioral

defense. The caterpillar extrudes frass onto the last abdominal segment. Then with

a flick of the abdomen the frass is throw great distances through the air (Wheeler &

Blackwell 1984). The purpose of frass throwing is to remove chemical cues from

the vicinity of the feeding caterpillar, which minimizes detection (Weiss 2006).

Most vertebrate predators hunt using visual cues, such as coloration and movement.

Some species of caterpillar “freeze” when spotted by a predator in order to cause

the predator to lose sight of them (Dyer and Gentry 1999). This defense is effective

when combined with cryptic coloration, so the caterpillar can blend into its

surroundings.

Gentry and Dyer (2002) state that parasitoids differ in the way they attack

their prey. The most obvious of these differences is the means by which each type of

parasitoid lays their eggs. Some flies and most nematodes do not have to come in

contact with the caterpillar to deposit their eggs; instead they lay microtype free

roaming eggs near or in the host microhabitat. This allows some flies and most

nematodes to avoid confrontation, and reduces the effectiveness of behavioral

defense strategies. Behavioral strategies are extremely effective against parasitic

wasps, which must come in contact with their host in order to sting and/or oviposit.

Thrashing, and biting can kill or stun wasps; this is why wasps often target early

instar caterpillars, which are smaller, weaker, and easier to attack (Gentry & Dyer

2002, Dyer 1997).

Many caterpillars use harmful chemical compounds to affect their enemies.

It is well documented that plants and their insect herbivores are locked in co-

evolutionary arms race (Dyer, 1995). The result of this has been that plants have

evolved a wide variety of toxic compounds, known as secondary substances, which

deter insects from eating them. Some caterpillars that specialize in eating these

toxic plants are able to utilize and sequester the toxins, thereby making themselves

toxic to predators (Dyer 1995). These chemical defenses often co-exist with

aposematic coloration. Chemical defenses are often very effective against

vertebrate and invertebrate predators, that either show innate avoidance or that

learns to avoid the brightly colored larvae through aversive conditioning (Dyer

1995)

Some species of caterpillar use an osmeterium to deter predators and

enemies. An osmeterium is a fleshy organ that is concealed within the prothoracic

segment of the caterpillar (Leslie & Berenbaum 1990). When threatened by a

predator this forked shaped organ is extruded from the thorax. The osmeterium is a

flashy bright yellow or orange color and emits a foul smelling secretion that is

noxious to predators. It is bright coloration warns the enemy of the noxious

compounds contained within the caterpillar. Leslie and Berenbaum (1990) state

that the osmeterium is an extremely effective defense against both vertebrate and

invertebrate predators. Some palatable caterpillars also have osmeteria and these

may be Batesian mimics of the distasteful species (Leslie and Berenbaum 1990). In

our study we encountered one species that exhibited an osmeterium, Papilio

glaucus, the adults of which are commonly known as eastern tiger swallowtail

butterflies (Figure 6).

By specializing in eating toxic host plants some caterpillars utilize the toxins

to produce fluids that are harmful to enemies. One strategy caterpillars employ is to

regurgitate a toxic fluid when molested by a predator or parasitoid. Regurgitation

has been shown to be effective against a wide variety of natural enemies including

ants and parasitoids (Gentry & Dyer 2002). Although in some cases the fluid acts as

a repellent, in others it may immobilize an enemy. Some ant species for example get

trapped inside the regurgitant, which may suffocate them by clogging their

spiracles. Caterpillar regurgitant may also contain compounds that are toxic to

parasitoids. Parasitoids employ highly sensitive chemosensory structures to locate

their prey and, regurgitant can over-stimulate them causing temporary chemical

blindness or even death (Gentry & Dyer 2002).

Some caterpillars utilize plant toxins by sequestering them in their bodies,

which causes them to be unpalatable. The most common example of this is the

larvae of Danaus plexippus, which feeds on milkweed (Asclepias) food plants.

Milkweed contains cardenolid toxins that are sequestered by the caterpillar and

stored in its body, which renders the larva unpalatable to vertebrate predators.

This unpalatability coexists with aposematic coloration. Inexperienced birds that

consume a protected larva undergo convulsive regurgitation within minutes and

soon learn to avoid such caterpillars (Brower, et.al., Malcolm 1990).

The presence of venom in caterpillars is a highly effective defensive strategy

against vertebrate predators. The venom in some species has the power to cause

hemorrhaging, kidney failure, destruction of blood cells, and even death. In Peru a

22-year old women from Canada stepped barefoot on five caterpillars. She felt

instant pain in her right foot, which soon spread to her thigh, and caused an

extremely painful headache. The symptoms seemed to disappear in 12 hours, so the

women did not seek medical attention. Back in Canada a few weeks later the

women was treated in the hospital for unexplained bruising of the leg, and later died

due to widespread internal bleeding, and multi-organ failure (Chan et.al., 2008).

Typically caterpillars store venom in glands that lie inside the caterpillar’s

body, and are transported to the predator via hairs and spines. When an enemy

comes in contact with the hairy or spiny caterpillar the hairs or spines break off

injecting venom. Many vertebrate predators learn quickly to avoid species

protected by venom. The moth family Limacodidae, known commonly as slug

caterpillars, is characterized by the presence of venom and stinging spines. There

are about 30 species of Limacodidae in North America, and over 120 species in

Costa Rica. In our study we encountered at least 4 species that utilized venom,

including Acharia stimulea, Phobetron pithecium, Parasa chloris, and Lithacodes

fasciola, all of which are Limacodids.

Many caterpillars have evolved a dense covering of hairs or spines that are

non-toxic. Their function seems to be to cause mechanical obstruction in edibility

for both vertebrate and invertebrate predators. Many vertebrate predators that

attempt to swallow the caterpillar quickly regurgitate and learn not to eat hairy

caterpillars. Hairs and spines can cause a different kind of difficulty for invertebrate

predators. Hemipteran predators use piercing sucking mouthparts that are injected

into the body of the caterpillar and suck out the nutrients and fluids from the inside.

Hairs and spines disrupt the insertion of the piercing sucking mouthparts, making it

difficult if not impossible to ingest the caterpillar (Dyer 1997). Some species of

Cuculid birds (cuckoos and anis) have evolved the ability to tolerate extremely hairy

or spiny caterpillars (Witz 1989, Dyer 1997, Gentry & Dyer 2002). In our study we

encountered at least 6 caterpillars with hairs and spines including two with the

presence of hairs: Phobetron pithecium, and Orgyia leucostigma (Figure 8), and at

least three that had the presence of spines including Automeris io (Figure 7), Acharia

stimulea, and Parasa chloris (Monahan 2008).

Stage 3 Defenses

Stage 3 defenses are activated after the caterpillar has been parasitized.

There are two major strategies employed to prevent the development of parasitoid

eggs. Parasitized caterpillars may change their diet to create a hostile internal

environment for the developing parasitoid, or they may use an immune system

response known as encapsulation (Chapman 1998).

Once a caterpillar has been parasitized diet change can help increase

survival rate. In some cases a caterpillar can change its diet to increase the chance

that the parasitoid emerges without killing it. While unparasitized the caterpillar of

Platyprepia virginalis has a greater survivorship feeding on lupine, but when

parasitized it is more likely to survive by feeding on poison hemlock (Karban &

English Loeb 1997). Some caterpillars change their habitat, moving to warmer areas

where it helps induce “behavioral fever” to eliminate parasitoids (Karban & English

Loeb 1997) A recent study found that wooly bear caterpillar parasitized by tachinid

flies will change their feeding preferences to include a highly toxic plant that helps

the caterpillar defend itself against the larvae (Singer et. al., 2004).

Immune system defenses such as encapsulation are among the most import

stage three defenses. When parasitoid larvae enter the body of a caterpillar they are

instantly surrounded by large numbers of hemocytes (blood cells). The first to

discharge their contents at the surface of the invader are granulocytes. Soon after

plasmatocytes are attracted, and start to accumulate upon the granulocytes. These

cells form a series of layers that wall off the parasitoid larvae, depriving it of oxygen

and nutrients, thereby killing it (Chapman 1998).

Conclusions

So far I have reviewed the various defensive adaptations displayed by

caterpillars to protect them from their enemies. By their sheer quantity, it would

seem that enemies have played a significant role in the evolution of caterpillar life

history strategies. We can examine each of the defensive strategies for their

effectiveness against each type of enemy: invertebrate predators, vertebrate

predators, and parasitoids. Table 1 shows the defenses against enemies that have

been reviewed in this paper and their effectiveness against invertebrate predators,

vertebrate predators, and parasitoids. It is evident that the majority the defenses

are most effective against vertebrate predators. This suggest that vertebrate

predators have played a significant role in the evolution of Lepidopterous larvae and

their feeding strategies.

Invertebrate Predators

Vertebrate Predators

Parasitoids

Crypsis + ++ 0

Aposematic Coloration

0 ++ 0

Silk Shelter 0 ++ 0

Leaf Folding ++ 0 ++

Leaf Mining ++ ++ ++

Thrashing + 0 ++

Frass Throwing + 0 ++

Dropping + ++ 0

Freezing 0 ++ 0

Ostmeterium ++ ++ 0

Regurgitation ++ + ++

Unpalatable + ++ 0

Venom 0 ++ 0

Hairs and Spines + ++ 0

Diet Change 0 0 ++

Encapsulation 0 0 ++

The more metabolic resources a caterpillar spends on maintaining a

defensive strategy the less it has for growth. Highly defensive caterpillars use more

energy for defenses and less for growth, hence making their duration as a larva

longer. If a caterpillar had defenses against all types of natural enemies it would

grow at a very slow pace, potentially making it more vulnerable to predation.

Due to the wide range of predators and their methods of locating and

attacking caterpillars there is no general defensive strategy to insure a caterpillar’s

survival. The co-evolutionary arms race between caterpillars and their predators

causes caterpillars to evolve defenses to protect themselves from their primary

predators, but such evolutionary decisions may have unintended consequences. For

instance a caterpillar that has an effective defense against vertebrate predators is

immediately more appealing to parasitoids. Parasitoids may target well-protected

caterpillars to increase the survival of their larvae because when a vertebrate

predator consumes a larva any larval parasitoids contained within are also killed. If

the defense of a caterpillar deters ingestion by predators then the body of the

caterpillar provides a safe haven for the development of the parasitoids larvae. By

doing this, parasitoids utilize the caterpillar’s defense as its own.

Figures

Figure 1

Lithacodes fasciola exhibits host plant leaf coloration to avoid detection by enemies.

Figure 2

Schizura unicornus mimics the edge of a damaged leaf with both coloration and shape.

Figure 3

The larvae of Torticidia testacea mimics leaf wounds caused by pathogens or herbivore damage

Figure 4

Parasa chloris exhibits bright red warning coloration to warn its enemies of its powerful venom.

Figure 5

When not feeding silk shelter caterpillars (like this species Machimia tentoriferella) utilize the safety of their shelters.

Figure 6

When threatened Papilio glaucus exerts its osmeteria to emit a noxious scent that warns enemies of being unpalatable.

Figure 7

Automeris io utilizes a dense covering of spines to protect itself from enemies.

Figure 8

Orgyia leucostigma utilizes a dense covering of hair to obstruct edibility in both vertebrate and invertebrate predators.

(Miller 2008)

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