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Parasites & Natural Enemies

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Monarchs have many natural enemies—predators, parasitoids, and parasites can harm monarch eggs, larvae, pupae, and adults. Predators are organisms that kill and consume other organisms (prey) to obtain energy and nutrients. Predators such as spiders and ants attack eggs and young larvae feeding on milkweed, whereas birds and wasps can prey on adult monarch butterflies. 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.

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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 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.

5th instar - photo by Barbara Powers adult monarch butterfly - photo by Fred Ormand

Monarch larvae (left) and adults (right) display bright warning coloration as a signal to potential predators. (Photos by Barbara Powers and Fred Ormand)

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 (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.

birds eating monarch butterflies - photo by Lincoln Brower adult monarchs on the ground in snow, victims of bird predation - photo by Lincoln Brower

Left: 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, are the main predators. Right: Many dead monarchs litter the forest floor in Mexico, such as these victims of bird predation. (Photos by Lincoln Brower)

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.

stink bug attacking monarch - photo by Duane Miller ants attack a 4th instar monarch larva - monarch lab photo

Left: An assassin bug pierces the cuticle of a monarch larvae and draws out the inner fluids and tissues. (Photo by Duane Miller) Right: Ants attack a fourth instar larva that crawled onto the wrong leaf. (MonarchLab photo)

Parasitoids

Monarch larva with 3 emerged tachinid fly maggots - Photo by Jaap de Roode

Parasitized monarch larva with three tachinid larvae (maggots). (Photo by Jaap de Roode)

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.

tachinid fly larva emerging from monarch chrysalis - Photo by Stephanie Baker mucus threads - photo by Sonia Altizer

Left: Monarch pupa with emerging tachinid larva. Right: Monarch pupae with “gelatinous tendrils” made by tachinid larvae. (Photos by Stephanie Baker and Sonia Altizer)

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.

tachinid pupa next to coin showing size comparison - photo by Sonia Altizer adult tachinid fly

Left: Soon after emerging, the flies pupate, turning reddish-brown. (Photo by Sonia Altizer) Right: Adult tachinid fly. (MonarchLab photo)

Pteromalus puparum wasps (female on top, male on bottom) from monarch pupa - Photo by Wendy Macziewski

Pteromalus puparum wasps (female on top, male on bottom) from monarch pupa. (Photo by Wendy Macziewski)

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 puparum (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 preparation). Pteromalus puparum wasps are tiny, and over 200 can emerge from one monarch pupa.

Parasites and Diseases

blackened 5th instar monarch larva, victim of nucleaer polyhedrosis virus - photo by Diane Rock

A fifth instar larva showing signs of bacterial decay shortly after death. (Photo by Diane Rock)

Horsehair worm that just emerged from a 4th instar monarch larva - Photo by Joyce Pearsall

Horsehair worm that just emerged from a fourth instar monarch larva. (Photo by Joyce Pearsall)

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 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).

Several Monarch Larva Monitoring Project volunteers have reported a horsehair worm (similar to a nematode) in monarchs collected in the southern US.

Ophryocystis elektroscirrha

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).

Life cycle of O. elektroscirrha - figure by Sonia Altizer

Life Cycle of O. elektroscirrha (figure by Sonia Altizer)

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.

Oe-infected pupa - monarch lab photo Oe-infected adult, dissected - monarch lab photo

Left: Clusters of O. electroscirrha spores form dark blotches under the cuticle of developing pupae about 3 days before eclosion. (Monarch Lab photo) Right: A monarch dissected out of its pupal case shows that most spores form in the abdomen of infected butterflies. (MonarchLab photo)

Oe Spores - monarch lab photo

Spores of O. electroscirrha appear as small brown ovals next to the larger butterfly scales. (MonarchLab photo)

References

  • Alonso-Mejia A. Brower L.P. 1994. From model to mimic: Age-dependent unpalatability in monarch butterflies. Experientia (Basel) 50(2). 176-181.
  • Altizer, S. and Oberhauser, K. 1999. Effects of the protozoan parasite, Ophryocystis elektroscirrha, on the fitness of monarch butterflies (Danaus plexippus). Journal of Invertebrate Pathology. In press.
  • Arnaud, P.H. Jr. (1978) A host-parasite catalog of North American Tachinidae (Diptera). U.S. Department of Agriculture Miscellaneous Publication No. 1319, Washington, D.C.
  • Bowers, R.G, Begon, M. and Hodgkinson, D.E. 1993. Host-pathogen population cycles in forest insects? Lessons from simple models reconsidered. Oikos 67(3) 529-538.
  • Brewer, J. and Thomas, G.M. 1966. Causes of death encountered during rearing of Danaus plexippus (Danaidae). Journal of the Lepidopterists' Society. 20(4). 235-238.
  • Brower, L. 1988. Avian predation on the monarch butterfly and its implications for mimicry theory. American Naturalist 131. S4-S6.
  • Brower, L.P. Calvert W.H. 1985. Foraging dynamics of bird predators on overwintering monarch butterflies Danaus plexippus in Mexico. Evolution 39(4). 852-868.
  • Brower L.P. Seiber J.N. Nelson C.J. Lynch S.P. Holland M.M. 1984. Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies, Danaus plexippus reared on milkweed plants in California (USA): 2. Asclepias speciosa. Journal of Chemical Ecology 10(4). 601-640.
  • Calvert, W.H. 1996. Fire ant predation on monarch larvae (Nymphalidae: Danainae) in a central Texas prairie. Journal of the Lepidopterists' Society. 50(2) 149-151.
  • Faeth, S.H. and Simberloff, D. 1981. Population regulation of a new leafmining insect, Cameraria sp., at increased field densities. Ecology 62(3): 620-624.
  • Fink, L.S. and Brower L.P. 1981. Birds can overcome the cardenolide defense of monarch butterflies (Danaus plexippus) in Mexico. Nature 291(5810). 67-70.
  • Frick C. Wink M. 1995. Uptake and sequestration of ouabain and other cardiac glycosides in Danaus plexippus (Lepidoptera: Danaidae): Evidence for a carrier-mediated process. Journal of Chemical Ecology 21(5). 557-575.
  • Jaenike, J. 1998. On the capacity of macroparasites to control insect populations. American Naturalist 151(1) 84-96.
  • Leong KLH. Kaya H.K. Yoshimura M.A. Frey D.F. 1992. The occurrence and effect of a protozoan parasite Ophryocystis elektroscirrha (Neogregarinida: Ophryocystidae) on overwintering monarch butterflies Danaus plexippus (Lepidoptera: Danaidae) from two California winter sites. Ecological Entomology 17(4). 338-342.
  • Leong KLH. Yoshimura M.A. Kaya H.K. and Williams, H. 1997. Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. Journal of Invertebrate Pathology. 69(1) 79-83.
  • McLaughlin, R.E. and Myers, J. 1970. Ophryocystis elektroscirrha sp. n. a neogregarine pathogen of the monarch butterfly Danaus plexippus (L.) and the Florida quen butterfly Danaus gilippus berenice Cramer. Journal of Protozoology. 17. 300-305.
  • Oberhauser, K. S., I. Gebhard, C. Cameron, S. Oberhauser. 2007. Parasitism of monarch butterflies (Danaus plexippus) by Lespesia archippivora (Diptera: Tachinidae). Amer. Midl. Nat. 157:312-328.
  • Prudic, K.L. & Olson, C. (2005) A new parasitoid of Danaus gilippus thersippus (Nymphalidae: Danainae) in Southeastern Arizona. Journal of the Lepidopterists’ Society, 59, 118–119.
  • Ritland, D.B. Brower L.P. 1993. A reassessment of the mimicry relationsihp among viceroys queens and monarchs in Florida. Natural History Museum of Los Angeles County Science Series (38). 129-139.
  • Sakai, W.H. 1994. Avian predation on the monarch butterfly, Danaus plexippus (Nymphalidae: Danainae), at a California overwintering site. Journal of the Lepidopterists' Society 48(2). 148-156.
  • Urquhart, F.A. 1987. The Monarch Butterfly: International Traveler. Nelson-Hall, Chicago, IL. 232 pp.
  • Zalucki, M.P. Brower, L.P. Malcolm, S.B. 1990. Oviposition by Danaus plexippus in relation to cardenolide content of three Asclepias species in the Southeastern USA. Ecological Entomology 15(2). 231-240.