Parasites and Natural Enemies
Monarchs have many natural enemies—predators, parasitoids, and parasites can harm monarch eggs, larvae, pupae, and adults. Predators vary between different monarch life stages, but little information is available about the extent to which each of those predators influences the population. Fire ants, lacewing larvae, spiders, wasps, and many Hemipteran larvae are among those that have been reported to prey on immature monarchs (eggs, larvae, pupae). Adults have fewer invertebrate predators, but some bird species have evolved to either avoid or tolerate the toxins. Parasitoids are specialized insects such as small flies and wasps that lay eggs on or inside other insects. Parasitoid larvae then eat their prey from the inside out, usually emerging from the prey carcass as a pupa or adult. Parasites are smaller organisms that live and multiply inside their hosts, taking nutrients and resources. Parasites can be unicellular microbes such as viruses and bacteria, or larger organisms like mites and nematodes. See the table at the bottom of this section for a list of reported monarch predators.
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 a 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.
Birds such as black-backed 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 (Calvert et al. 1979). 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.
Invertebrate predators such as ants, spiders, and wasps attack monarch larvae on milkweed plants (Prysby 2004). 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.
Both fly and wasp parasitoids lay their eggs on monarch larvae, but the most important larval parasitoid is probably a fly species in the family Tachinidae. This family includes about 10,000 species, most of which parasitize Lepidoptera (butterflies and moths), although they also parasitize Hymenoptera (ants and bees), Heteroptera (true bugs and their relatives), Coleoptera (beetles), Diptera (flies and mosquitoes), Dermaptera (earwigs), Orthoptera (grasshoppers and crickets), Chilopoda (centipedes), as well as some scorpions and spiders. Research in the Monarch Lab suggests that the species Lespesia archippivora (La) is the most important monarch tachinid parasitoid. It is widespread throughout North and Central America, has been found in Brazil, and was purposely introduced into Hawaii for biocontrol in 1898. Monarch larvae in the continental US and Hawaii are frequently parasitized by La, and the Monarch Larva Monitoring Project documented an overall parasitism rate of ~13% (Oberhauser et al. 2007). For information on how you can contribute data that will aid in our understanding of this important monarch enemy, visit the Monarch Larva Monitoring Project website.
Female La lay eggs on the host integument (skin), and the fly larvae hatch and bore into the host soon after oviposition. La complete their larval development within the host, the maggots emerge from late larvae or pupae, and then pupate in leaf litter and eclose within ~10-14 days. Fly maggots drop to the ground on long, gelatinous tendrils that look like white strings hanging from the monarch.
Less is known about the extent to which other parasitoids attack monarchs, but at least one wasp in the family Braconidae has been reported in monarchs (Arnaud 1978). The closely-related queen, Danaus gilippus is parasitized by two Chalcid wasps,Brachymeria annulata and B. ovata (Prudic and Olson 2005), as well as L. archippivora (Arnaud 1978). Current research in the Monarch Lab demonstrates that the wasp Pteromalus cassotis (in the family Pteromalidae and the same superfamily, Chalcidoidea, as the two Chalcid wasps found in queens) could be an important pupal parasitoid (Oberhauser et al. in press). P. cassotis wasps are tiny, and over 200 can emerge from one monarch pupa. Research from the Monarch Lab has also shown that a closely related generalist parasitoid (Pteromalus puparum) will attempt to parasitize monarch pupae under lab conditions, but their offspring fail to develop in monarch hosts. We are currently investigating the role of monarch's sequestered cardenolides in these host-parasitoid interactions (Stenoien et al. in preparation).
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 disease-causing 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 asOphryocystis 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).
Several Monarch Larva Monitoring Project volunteers have reported a horsehair worm (similar to a nematode) in monarchs collected in the southern US.
Ophryocystis elektroscirrha (OE)
Ophryocystis elektroscirrha is a protozoan parasite that was first recovered from monarch and queen butterflies in Florida in 1966 (McLaughlin and Myers 1970). New infections occur when larvae ingest parasite spores as they feed on contaminated egg shells or milkweed leaves. Most spores are transmitted from infected adults to their offspring (vertical transmission), although horizontal transmission may also occur. Following ingestion, spores lyse in larval guts. Emerging sporozoites then penetrate the intestinal wall, enter the hypoderm, and undergo two phases of vegetative, asexual replication. After host pupation, the parasite undergoes sexual reproduction and forms dormant spores around the scales of the developing adult butterfly (McLaughlin and Myers 1970). Most spores form on the adult abdomen, although spores also develop on the wings, head, and thorax (Leong et. al. 1992; S.M. Altizer, personal observation).
Heavily infected adults have difficulty emerging from their pupal cases and expanding their wings, although adults with low parasite loads appear normal (McLaughlin and Myers 1970; Leong et al. 1992). High parasite doses decrease larval survivorship from hatching to eclosion, and heavily captive adults are smaller and shorter-lived than uninfected adults (Altizer and Oberhauser 1999). Researchers in Sonia Altizer’s lab at the University of Georgia are studying rates of parasitism by OE and its effects on monarchs. For more information about this disease and how you can join in this research, visit monarchparasites.org.
- Predator Table - Predators and Parasitoids known to attack monarchs
- When Butterflies get Bugs - The ABCs of Lepidopteran disease