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Natural Enemies

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Monarchs become toxic to predators by sequestering toxins from the milkweed they ingest as larvae, and are brightly colored in both the larval and adult stages to warn predators of this toxicity. Despite the fact that milkweeds are assumed to convey some degree of protection from generalist predators and parasitoids, monarchs of all life stages are vulnerable to predation and disease.

Parasitoids

Tachinid fly larvae Photo Courtesy of Jaap de Roode
Tachinid fly larvae Photo Courtesy of Jaap de Rood

Parasitoids are specialized insects that lay eggs on or inside other insects and develop by feeding in or on a host organism, causing its eventual death. 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.

Flies in the family Tachinidae are one of monarchs’ primary parasitoids. These flies attack larvae, resulting in the death of late-instar larvae or pupae. Data from the Monarch Larva Monitoring Project (MLMP) suggest that there are at least seven tachinid fly species that parasitize monarchs in North America, with an overall parasitism rate of 9.8% (Oberhauser et al., 2017). Females of some tachinid species lay eggs on the host integument (skin), and the fly larvae hatch and bore into the host soon after oviposition. Other species may lay eggs on milkweed foliage, in which Lepidoptera hosts consume and become infected. Fly larvae 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 butterfly, Danaus gilippus is parasitized by two Chalcid wasps, Brachymeria annulata and Brachymeria ovata (Prudic and Olson 2005), as well as the tachinid fly, Lespesia archippivora (Arnaud 1978). 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 of monarch butterflies (Stenoien et al., 2015). These tiny wasps lay eggs inside a monarch chrysalis (up to 200 at a time), which emerge as adult wasps from the monarch pupa casing a few weeks later. Research 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. Recent studies investigated the role of monarchs' sequestered cardenolides in their interactions with parasitoids. Stenoien et al., 2015 found that P. cassotis parasitoids were less likely to attack more toxic monarchs but that once attacked, host toxicity did not effect whether monarchs survived or parasitoids emerged. Monarch toxicity did however influence the performance of the developing parasitoids, such as decreasing the brood size and survival to adulthood. 

More research is needed to understand P. cassotis and the effects this species has on monarch populations. Parasitoids, such as those mentioned here, are often introduced as biological control agents to rid an area of unwanted pests. Bio-control agents often have harmful non-target effects on beneficial species, like monarchs or other pollinators.

Parasites and Disease

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. 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).

Photo Courtesy of Diane Rock

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).Monarch larvae are generally found singly on milkweed plants, unlike the large aggregations of adults in overwintering clusters. Lower larval density in milkweed patches reduces the chance of diseases, such as nuclear polyhedrosis virus and Pseudomonas bacteria, spreading between larvae. These diseases are often fatal to monarchs.




Ophryocystis elektroscirrha

Perhaps the most-studied parasite of monarchs is a protozoan parasite called Ophryocystis elektroschirra (OE). This parasite cannot be transferred between larvae or adults simply by contact. New infections occur when larvae ingest parasite spores that fall from the abdomen of an infected adult to the surface of 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).

While it is often not fatal, OE can have negative effects on survival, mass, and life span of monarchs. 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). Particularly high levels of OE have been documented in resident/non-migratory monarch populations (such as in southern California and Florida). 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.

Monarch scales with OE spores
Photo Courtesy of Sonia Altizer

There is a higher occurrence of this parasite in populations that do not migrate, such as the one in southern Florida. Researchers estimate that high parasite transmission, combined with high virulence, can reduce lifetime reproductive success and reduce non-migratory/resident monarch populations by 50% (Majewska et al., 2019). The eastern migratory population has the lowest occurrence of OE, likely due to the fact that infected monarchs are less likely to make it to their overwintering destinations in Mexico and therefore will not reproduce and spread the parasite. Recent studies about OE and exotic milkweed describe how the year-round presence of tropical milkweed in some parts of the U.S. may be facilitating the spread of this parasite (Majewska et al., 2019). For more information, please read our Potential Risks of Growing Exotic Milkweeds for Monarchs fact sheet.

Predation

Invertebrate predators such as ants, spiders, and wasps attack monarch larvae on milkweed plants (Prysby 2004). Only about 5% of monarchs reach the last larval instar. 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. In a laboratory experiment, one lacewing larva was observed consuming 40 monarch eggs. Chinese mantids and paper wasps have also been observed preying on immature monarchs.

Photo Courtesy of Lincoln Brower

Adults face less danger of being eaten by predators during the breeding season, but there is a much greater risk of being eaten by bird predators in overwintering locations. 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. 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. 

Monarch Defenses and Warning Coloration

Photo Courtesy of Wendy Caldwell

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.