Parasites & Natural Enemies
Introduction | Background & Life Cycle of Ophryocystis
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One factor likely to regulate the abundance of monarchs is their interaction with
natural enemies. Many predators, parasites, and parasitoids attack monarch eggs,
larvae, and adults. Predation occurs when one organism (a predator) kills and consumes
another organism (a prey) to obtain energy and nutrients. Predators
such as spiders and ants attack eggs and young larvae feeding on milkweed, whereas
birds and wasps have been observed preying on adult monarch butterflies.
Parasitoids are specialized insects such as small flies and wasps that
lay eggs on other insects. Parsitoid larvae then eat their prey from the inside
out, usually emerging from the prey carcass as a pupa or adult. Smaller organisms
that live and multiply inside their hosts, taking nutrients and resources, are called
parasites. Parasites can be unicellular microbes such
as viruses and bacteria, or larger organisms like mites and nematodes.
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Monarch Defenses and Warning Coloration
Many prey species have mechanisms to avoid predation, including camouflaged coloration
or bright eye-spots to confuse predators. Bright coloration in insects and other
animals (typically yellow, orange, or red) can act as signal, warning other animals
that they are poisonous or distasteful. Such color patterns are called "aposematic."
When an animal attacks, eats, or encounters such a brightly colored animal and gets
stung, bitten, or poisoned, it learns to associate these warning colors with a bad
experience. Monarchs have a chemical defense that is toxic to many natural enemies
- they can sequester poisonous compounds from milkweed called cardenolides, or cardiac
glycosides (Zalucki et al. 1990, Ritland and Brower 1993, Brower et al. 1994, Frick
and Wink 1995). Thus, when an animal eats a monarch and gets sick, it learns to
avoid potential prey with similar coloration. However, research has shown that these
toxins break down over time in adult monarchs, and by several weeks of age the butterflies
are much more palatable to predators (Fink and Brower 1981, Brower and Calvert 1985,
Brower 1988, Alonso M. and Brower 1994, Sakai 1994). In addition, the role of sequestered
chemicals in defending monarchs against parasitoids and pathogens has not been explored.
Monarch larvae and adults display bright warning coloration as a signal to potential
predators.
Predation
Birds such as black-beaked orioles and black-headed grosbeaks are common predators
at monarch overwintering sites. These species can eat large quantities of monarchs
without getting poisoned. This may result from the decay of toxins inside the monarchs’
bodies during the many months of migration and overwintering, or from the specific
feeding behavior of the birds. Orioles slit open the monarchs’ abdomens before
feeding, avoiding most of the toxin-rich cuticle. Grosbeaks, which eat the entire
abdomen, can tolerate higher levels of cardenolides in their digestive tracts. Research
has shown that predation by these two bird species accounts for over 60% of the
total monarch mortality during overwinter, and together they kill 7-44% of the total
monarchs in any one colony (reference).
Predation by birds is one of the most important natural causes of monarch mortality
during the winter. Two bird species, black-headed grosbeaks and black-backed orioles
(L), are the main predators. In some colonies, up to 9% of the butterflies are eaten
by birds during the winter, and this number can be up to 15% when the forest is
disturbed by logging, making it easier for the birds to reach the branches on which
monarchs cluster. Many dead monarchs litter the forest floor in Mexico (R), such
as these victims of bird predation.
Invertebrate predators such as ants, spiders, and wasps attack monarch larvae on
milkweed plants. Less is known regarding invertebrate predation in monarchs, but
wasps have been observed feeding on monarch abdomens at a California overwintering
site (D. Frey, personal communication), and fire ants have been suggested as a major
predator of monarch larvae in Texas (Calvert 1996). Other research suggests that
wasp predators may be sensitive to the chemical defenses of monarch larvae, and
that wasps fed monarch larvae with high cardenolide concentrations had lower reproductive
potential and more deformities in their nests (L.S. Rayor, personal communication)
than wasps that preyed upon less toxic caterpillars.
An assassin bug (L) pierces the cuticle of a monarch larvae and draws out the inner
fluids and tissues. Ants (R) attack a fourth instar larva that crawled onto the
wrong leaf.
Parasitoids
A few species of parasitoids lay their eggs on monarch larvae, including tachinid
flies and braconid wasps. Tachinid fly larvae feed on monarch caterpillars, but
usually don’t kill their hosts until just before the caterpillars pupate. When
a parasitized caterpillar hangs upside down in the pre-pupal "J"-shape,
several fly maggots will emerge from the dorsal anterior end and drop to the ground
on long, gelatinous tendrils. Braconid wasp parasitism is less common, but as many
as 32 tiny adult wasps may emerge from a single monarch carcass. Very little is
known about variation in rates of parasitism and predation by invertebrates throughout
the monarchs' range.
Monarch larva parasitized by tachinid flies (L). Parts of its body turned brown
and transparent shortly before fly maggots emerged. Tachnid fly maggots (R) leave
long tendrils hanging from the body of their host.
Parasites and Diseases
Parasites are small organisms that complete most or all of their life cycle within
a host, and many are capable of a high degree of within-host replication. Not all
parasites kill their hosts, but parasites almost always have negative effects on
host survival and reproduction. Many parasites and pathogens are known to attack
insects, including viruses, bacteria, fungi, protozoans, nematodes, and mites. Several
viral and bacterial pathogens can infect monarchs, including a nuclear polyhedrosis
virus and Pseudomonas bacteria (Brewer and Thomas 1966, Urquhart 1987). Protozoan
parasites such as Ophryocystis elektroscirrha and a microsporidian Nosema
species have also been identified in wild and captive monarchs (McLaughlin and Myers
1970, Leong et al. 1992;1997, Altizer and Oberhauser 1999, O. Taylor, personal communication).
The infective stages of most insect parasites must be consumed orally, although
some can invade though pores or membranous joints in the insect cuticle. Many researchers
are currently exploring the role of parasites and infectious diseases in regulating
insect population size (E.G. Faeth and Simberloff 1981, Bowers et al. 1993, Jaenike
1998).
A fifth instar larva (L) showing signs of bacterial decay shortly after death. The
nuclear polyhedrosis virus that attacks monarchs has been called the "black
death" (R) because infected larvae and pupae turn black and disintegrate following
infection.
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