Abstract

Monarch butterflies (Danaus plexippus) have developed various adaptations in order to avoid being caught and eaten by predators. These adaptations are useful during various encounters with predators at different times and localities. These behaviors demonstrate that each tactic has costs as well as benefits and that none work equally well against all enemies, and that many elements of the behavioral repertoire have interlocking consequences (Alcock, 1998). Monarchs have brilliant orange and black color patterns that are utilized for Batesian as well as Mullerian mimicry. The acquisition of chemicals such as cardiac glycosides and pyrrolizidine alkaloids are a major form of defense. Cardiac glycosides, from the monarch larvae’s food is acquired during the larva stage and used throughout their larvae and adult life stages for defense. Although, the concentration of cardiac glycosides decrease as an individual ages so that the individual can change from being an unpalatable model to a palatable mimic (Alonso and Brower, 1994). Pyrrolizidine alkaloids are acquired as an adult and aid in their noxious taste. Migration and the tactics used in the monarch butterfly’s overwintering areas provide additional means for avoiding predation. These include mass clustering to utilize the dilution effect and falling en masse from perches. But even with all these antipredator adaptations, millions of monarch butterflies are caught and eaten every year. The main predators are various bird, mice, and vole species.

Introduction

Predator and prey relationships are numerous and highly developed but they are ever changing. Prey need to find ways to cope with predators in order to survive and reproduce viable offspring. John Alcock (1998) divides predator / prey interactions into four stages: detection, attack, capture, and consumption. Prey species have therefore developed adaptations to avoid being detected, attacked, captured and most importantly consumed. These adaptations are highly variable and quite ingenious. From warning coloration, cypsis, mobbing, rapid erratic flight patterns, alarm signals, false heads, and stinging hairs to chemical sprays, secretions, and tissues. Monarch butterflies (Danaus plexippus) use several behaviors in order to prevent predation. They take advantage of their mass numbers while at overwintering sites, their chemical makeup, and their looks to prevent these four stages. Although these various behaviors may not work with all predators and all times, they do enhance the monarch’s survival. Dilution and startle effects, acquisition of toxic chemicals from foods consumed, and Batesian and Mullerian mimicry are all antipredator behavior used by monarch butterflies. This review article will detail these various tactics that monarch’s have developed in order to survive.

Discussion

Monarch butterflies, Danaus plexippus, migrate each spring from remote winter refuges in the mountains of central Mexico to colonize a huge area of the eastern United States and southern Canada (Brower, 1995). After 3 to 5 generations of population expansion, the autumnal generation migrates back to the same overwintering site. While at these remote mountain peaks, they form tightly packed aggregations of up to 10 million butterflies per hectare (Calvert and Brower, 1986). Obviously these high concentrations make them prime targets for vertebrate predators. Calvert, Hedrick, and Brower (1979) have shown that the risk of dying for any one monarch declines in relation to increases in the number of butterflies clustered within an aggregation site. In addition, the risk to the individual is substantially lower in the colony center than in the periphery. This strategy is called the dilution effect. There has been some disagreement as to whether this is a group selection or individual selection. Hamilton (1970) showed in a computer simulation experiment that selfish avoidance of a predator could lead to aggregation. Another advantage to clustering is the use of a mass startle effect. Roosting butterflies fall from their perches at once en masse in response to a disturbance. This behavior seems to confuse and disorientate bird predators and possibly mouse predators thus allowing the butterflies to escape (Tuskes and Brower, 1978; Calvert, 1994).

The location of the overwintering sites is also an advantage for the monarch butterflies. The sites are found in the dense forests of the Oyamel fir in central Mexico. Monarchs that cluster in opened areas are more susceptible to bird predation than those found in areas of closed forest (Alonso-Mejia et al., 1998). The thick canopy cover provides protection from bird predators, but that may not be the only reason for the choice of location and aggregation behavior. Anderson and Brower (1996) suggest that this has evolved, at least in part, through individual selection to avoid wetting. In their research, they found evidence that the intact Oyamel fir forest serves both as a thermal blanket and a rain umbrella for the overwintering butterflies.

Monarchs also possess defensive chemical compounds that are known to be distasteful and toxic to several vertebrate predators. These compounds include cardiac glycosides and pyrrolizidine alkaloids. The glycosides are sequestered as larvae feed on milkweed plants (Asclepiadaceae) which they do exclusively. These toxins are transferred to the adult stage (Malcolm and Brower, 1989) and cause vomiting in 12 species of birds in 9 families (Fink and Brower, 1981). The pyrrolizidine alkaloids are obtained by the adults from flowers of the Asteraceae (Kelley et al., 1987; Edgar et al., 1976). But there are bird species as well as mice and voles that seem to be unaffected by these toxins, so these defensive chemicals appear to only limit the number of predator species that feed on monarchs.

Birds are the main predators of monarchs especially in the overwintering sites. An estimated 2.034 million butterflies are eaten by birds during this time (Brower and Calvert, 1985). Black-backed orioles (Icterus abeillei) and black-headed grosbeaks (Pheucticus melanocephalus) are the two main bird predators of monarchs at the overwintering sites in Mexico (Fink and Brower, 1981). Fink and Brower (1981) found that the orioles tend to be more effected by the toxins then the grosbeaks. When they force-fed birds powder made from monarch butterflies, all of the orioles vomited but none of the grosbeaks became ill. In observing wild birds they found that the orioles tended to strip out the thoracic muscle and abdominal contents without eating the cuticle in which these compounds are more highly concentrated. The grosbeaks on the other hand, consume the cuticle as well as the internal tissues regardless of the toxic content.

Mice (Peromyscus) are another significant predator of overwintering monarch butterflies. Research done by Brower, Horner, Marty, Moffitt and Villa-R. (1985) estimated that mice living within a 5.6-acre butterfly colony could consume from 330 to 2400 butterflies per day. Their research concluded that the digestive physiology of the mice allows them to ingest substantial amounts of toxic secondary plant compounds without adverse effects even though these cardenolides are toxic to mice when injected. Apparently, they absorb cardenolides poorly through their guts.

The high predation rates of monarch butterflies in overwintering sites in Mexico may also be due to the monarchs having low levels of these chemical toxins. Malcolm and Brower (1989) did research on monarch sequestration of cardenolides. They found that the most toxic milkweed plants (A. asperula, A. viridis, and A. humistrata) that the butterfly larvae fed on are found in the southern part of the USA, which is where the overwintering generation first migrates to and lays their eggs. This first generation of spring monarchs carry the most toxins. As these offspring migrate north they lay eggs on less toxic milkweed (A. syriaca) but these larvae can sequester cardenolides from this species of milkweed more effectively than from any other species of milkweed so their toxic levels are intermediately high. When the autumn generations start their migration to Mexico, they have fairly high levels of cardenolides, but after they have flown a considerable distance the levels drop dramatically. So when they arrive in Mexico, they have low levels of cardiac glycosides making predation more successful.

Alonso-Mejia and Brower (1994) found that there may be another reason cardiac glycosides are low in overwintering monarch butterflies. They showed that the concentrations of these toxins decrease as the butterflies age, regardless either of the initial amounts of cardiac glycosides or their chemical structures. Alonso-Mejia and Brower’s (1994) research shows that the butterflies that emerge in late May will be emetic, but their cardiac glycosides will dwindle below the emetic dosages. Nonetheless, since considerable overlapping of generations occurs over the summer, automimicry is possible: the freshly emerged individual monarchs can serve as noxious models for the older individuals that have lost most of their toxins. Therefore, as monarchs age during their individual lifetimes, they can progress from unpalatable models to palatable automimics. This brings us to the discussion of mimicry in monarch butterflies.

Mimicry comes in two forms. Batesian mimicry (Bates, 1862) is where palatable prey resembles unpalatable and conspicuous prey. Monarchs are considered the unpalatable models for other palatable species such as the viceroy butterfly (Limenitis archippus). Batesian mimicry involves three "players": a predator, a model, and a mimic (Mappes and Alatalo, 1997). The second form is Mullerian mimicry. This is where unpalatable species resemble other unpalatable species, the more advertising the better. Monarchs advertise their noxious taste with very brightly colored orange and black wings. These warning coloration’s advertise to potential predators that they are noxious. It has been found though, that not all predators heed the warning and need to taste first (Ritland, 1998). In the case of blue jays, they learn quickly to avoid toxic prey (Alcock, 1998). A blue jay that eats a poisonous monarch becomes ill and vomits shortly after. This same blue jay will from thereafter avoid the butterfly on sight alone. Research done by Coppinger (1970) has shown that birds avoided novel insects in a manner that showed that the rejection was not learned or innate. He states that the rejection suggests a relationship between the amount of stimulus change and the previous experience of the animal.
 

Conclusion

This review has shown how Monarch butterflies (Danaus plexippus) use various antipredator behaviors to maximize their survival. From avoiding capture by dilution and startle effects, to avoiding consumption by the use of cardiac glycosides and pyrrolizidine alkaloids, and finally by avoiding attacks by the use of Batesian and Mullerian mimicry. The use of all these methods demonstrates how one species, Danaus plexippus, can effectively use several tactics to ensure survival of the species.

References

Alcock, J. 1998. Animal behavior: an evolutionary approach, sixth edition. Massachusetts: Sinauer Associates, Inc.

Alonso-Mejia, A., Brower, L.P. 1994. From model to mimic: age-dependent unpalatability in monarch butterflies. Experientia 50: 176-181.

Alonso-Mejia, A., Montesinos-Patino, E., Rendon-Salinas, E., Brower, L.P., Oyama, K. 1998. Influence of forest canopy closure on rates of bird predation on overwintering monarch butterflies Danaus plexippus L. Biological Conservation 85: 151-159.

Anderson, J.B., Brower, L.P. 1996. Freeze-protection of overwintering monarch butterflies in Mexico: critical role of the forest as a blanket and an umbrella. Ecological Entomology 21: 107-116.

Bates, H.W. 1862. Contributions to an insect fauna of the Amazon valley (Lepidoptera: Heliconidae). Trans. Linnean Society of London 23: 495-556.

Brower, L.P. 1995. Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857-1995. Journal of Lepidopterist’s Society 49: 304-385.

Brower, L.P., Calvert, W.H. 1985. Foraging dynamics of bird predators on overwintering monarch butterflies in Mexico. Evolution 39: 852-868.

Brower, L.P., Horner, B.E., Marty, M.A., Motfitt, C.M., Villa-R, B. 1985. Mice (Peromyscus maniculatus, P. spicilegus, and Microtus mecicanus) as predators of overwintering monarch butterflies (Danaus plexippus) in Mexico. Biotropica 17: 89-99.

Calvert, W.H. 1994. Behavioral response of monarch butterflies (Nymphalidae) to disturbances in their habitat – a group startle response? Journal of the Lepidopterists Society 48: 157-165.

Calvert, W.H., Brower, L.P. 1986. The location of monarch butterfly (Danaus plexippus) overwintering colonies in Mexico in relation to topography and climate. Journal of Lepidopterist’s Society 40: 164-187.

Coppinger, R.P. 1970. The effect of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. II. Reactions of naïve birds to novel insects. The American Naturalist 104: 323-335.

Edgar, J.A., Cockrum, P.A., Frahn, J.L. 1976. Pyrrolizidine alkaloids in Danaus plexippus and Danaus chrysippus. Experientia 32: 1535-1537.

Fink, L.S., Brower, L.P. 1981. Birds can overcome the cardenolide defense of monarch butterflies in Mexico. Nature 291: 67-70.

Hamilton, W.D. 1970. Geometry for the selfish herd. Journal of Theoretical Biology 31: 295-311.

Kelley, R.B., Seiber, J.N., Jones, A.D., Segall, A.D., Brower, L.P. 1987. Pyrrolizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico. Experientia 43: 943-946.

Malcolm, S.B., Brower, L.P. 1989. Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45: 284-295.

Mappes, J., Alatalo, R.V. 1997. Batesian mimicry and signal accuracy. Evolution 51: 2050-2053.

Ritland, D. B. 1998. Mimicry-related predation on two viceroy butterfly (Limenitis archippus) phenotypes. The American Midland Naturalist 140: 1-20.

Tuskes, P.M., Brower, L.P. 1978. Overwintering ecology of the monarch butterfly, Danaus plexippus L., in California. Ecological Entomology 3: 141-153.