| The following is a review of general monarch biology that was written by Karen Oberhauser and Michelle Solensky in 2006, and has been updated with new research findings. The sections covered include
Also, scroll to the end to see a list of great books on monarch biology and conservation
Monarch Biology: A Review
Monarch butterflies (Danaus plexippus) are native to North and South America. In the 1800's, however, they spread to other parts of the world. Monarchs were first seen on Hawaii in the 1840's, and then throughout many South Pacific islands in the 1850's and 1860's (Ackery and Vane-Wright 1984). In the early 1870's, the first monarchs were reported in Australia and New Zealand (Gibbs 1994). It is not clear exactly how and why this emigration occurred. One possibility is that monarchs were transported by ships, either as larvae that found their way onboard from shipyard milkweed plants, or as adult monarchs that happened to land on ocean-going vessels. It is most likely that humans were involved in the process, but it is not known to what extent. Because North American monarchs often fly over 2,200 km during their migration, it is always possible that some made the journey on their own (Vane-Wright 1993).
In the western hemisphere, there are two subspecies of the monarch butterfly: (1) Danaus plexippus plexippus of southern Canada, the USA, Mexico, most Caribbean Islands, Central America and northern South America; and (2) Danaus plexippus erippus of Peru, Bolivia, Chile, Argentina, Uruguay, Paraguay and eastern Brazil. Neither subspecies has been recorded in northwestern Brazil.
The foci of this review are the North American migratory populations, i.e. those monarchs that migrate to overwintering grounds in central Mexico and the west coast of the USA.
Adult monarch nectaring in New York City.
Photo taken by Pat Davis
Monarch Breeding Ecology
Overview: Monarch larvae are specialist herbivores, consuming only host plants in the milkweed family (Asclepiadacea). They utilize most of the over 100 North American species (Woodson 1954) in this family, breeding over a broad geographical and temporal range that covers much of the United States and southern Canada. In a typical year, one generation is produced in the southern part of this range by returning migrants and two to three generations are produced in the northern part.
Monarchs and Milkweed. Milkweed provides monarchs with an effective chemical defense against many predators. Monarchs sequester cardenolides (also called cardiac glycosides) present in milkweed (Brower and Moffit 1974), rendering them poisonous to most vertebrates. However, many invertebrate predators, as well as some bacteria and viruses, may be unharmed by the toxins or able to overcome them. The extent to which milkweed protects monarchs from non-vertebrate predators is not completely understood, but a recent finding that wasps are less likely to prey on monarchs consuming milkweed with high levels of cardenolides suggests that this defense is at least somewhat effective against invertebrate predators (Rayor 2004).
Benefits gained by monarchs from cardenolides are not without cost. Milkweed plants between and even within species vary a great deal in cardenolide concentration, and both the toxin and the sticky latex produced by the plants provide defenses against herbivores. Monarchs appear to be negatively affected by consuming plants with high cardenolide levels, and may actually starve to death when their mandibles are glued together by the latex or if their bodies become mired in a drop of latex formed when the plant is injured (Zalucki and Brower 1992; Malcolm and Zalucki 1996; Zalucki and Malcolm 1999; Zalucki et al. 2001). Larger larvae reduce this risk by chewing a notch at the base of the milkweed leaf midvein, cutting off the flow of sticky latex to the rest of the leaf and allowing more efficient eating (see Figure 1).
||Figure 1. Larger larvae chew a notch at the base of the milkweed leaf midvein, cutting off the flow of sticky latex to the rest of the leaf and allowing more efficient eating. Photo by Karen Oberhauser.
Like other plants, milkweed quality as a host for insects varies. Many insects are nitrogen limited (McNeil and Southwood 1978, Mattson 1980, Scriber 1984, Stansky and Scriber 1985, White 1993). They must consume large quantities of their host plants to accumulate enough nitrogen for growth and development, since animal tissue generally consists of 7-14% nitrogen by dry weight (dw) and plants consist of 0.03-7.0% nitrogen dw (Mattson 1980). Leaf nitrogen levels vary within a season, as plant tissue ages and as plants allocate more resources to reproductive tissue. In addition, plants grow in habitats with different levels of available soil nitrogen. Lavoie and Oberhauser (2004) studied the response of monarch larvae to plants manipulated through fertilizer treatments to contain varying leaf nitrogen levels, and found that they compensated for low nitrogen leaves by consuming more plant tissue per day. If increased consumption makes them more vulnerable to predation or plant defenses, this could result in decreased fitness levels.
The most important northern host plant is Asclepias syriaca (common milkweed - Figure 2), but a number of other species are used as well, including A. incarnata (swamp milkweed - Figure 3) and A. tuberosa (butterfly weed - Figure 4). Central Plains host plants include the vine Cynanchum laeve (sand or honey vine). A northeastern invasive plant in the same genus (C. nigrum) has spread west as far as Wisconsin. This species is attractive to ovipositing females, but monarch larvae do not survive on it (Haribal 1998). In the south, the most important host plants are probably Asclepias oenotheroides (zizotes milkweed), A. viridis (spider milkweed) and A. asperula (antelope horn milkweed), all fairly common throughout Texas and other southern US states.
|Figure 2. The most important host plant for monarchs in the eastern migratory population during the summer breeding season is common milkweed (Asclepias syriaca). Photo by Karen Oberhauser.
||Figure 3. Monarch larvae consume many different milkweed species, including this swamp milkweed (Asclepias incarnata). Photo by http://www.bishopgrandingreenway.com.
||Figure 4. Although monarch larvae will consume butterfly weed (Asclepias tuberosa), the “hairy” leaves make it less desirable as a host plant than other milkweeds. However, the flowers are attractive to monarchs and many other insects as a nectar source. Photo by Karen Oberhauser.
Egg production. It is difficult to tell just how many eggs female butterflies lay during their lives, but the average in the wild is probably 300 to 400. Captive monarch butterflies average about 700 eggs per female over 2 to 5 weeks of egg laying, with a record of 1179 eggs (Oberhauser 1997). Monarch eggs hatch about 4 days after they are laid, but the rate of development in this stage, like all other stages, is temperature dependent, with individuals in warmer environments developing more rapidly (Zalucki 1982). The proteins that are an important constituent of eggs must either be derived from nutrients ingested during the larval stage or obtained from males during mating (Boggs and Gilbert 1979, Oberhauser 1997). While an individual monarch egg (Figure 5) weighs only about 0.460 mg, about 1/1000 the adult mass, females often lay more than their own mass in eggs throughout their lives.
||Figure 5. A monarch egg. Female monarchs always lay their eggs on milkweed plants, usually one at a time, although it is not uncommon to find more than one egg on a plant. Photo by Michelle Solensky.
||Figure 6. Five monarch instars: During the larval period, monarchs pass through five larval instars, shedding their skin between each to allow their amazing growth; they increase their body mass up to 2000 times during this period. Photo by Karen Oberhauser.
||Figure 7. This close-up view of a monarch larva shows the front tentacles (not the true antennae, which are hidden on the lower part of the head), the true legs in the front, and the yellow, black and white striping pattern. Photo by Karen Oberhauser.
Monarch eggs and larvae have a slim change of reaching adulthood; several studies have documented mortality rates of over 90% during the egg and larva stages (Borkin 1982, Zalucki and Kitching 1982, Oberhauser et al. 2001, Prysby and Oberhauser 2004). This mortality stems from both biotic and abiotic sources. Biotic factors that affect monarch survival include natural enemies such as predation, diseases and parasites; and interactions with their milkweed hosts. Abiotic factors include environmental conditions such as adverse weather and pesticides. Many monarchs in natural populations are killed by invertebrate predators that eat the monarchs themselves, or by parasitoids whose larvae develop in and eventually kill the monarch larvae. Diseases caused by bacteria, viruses, fungi and other organisms are also significant sources of monarch mortality.
Prysby (2004) documented overall impacts of natural enemies on monarch survival. By limiting predator access to monarch eggs and larvae with exclosures placed around naturally growing milkweed plants, she showed that both terrestrial and aerial predators represent significant sources of mortality (Figure 8). In addition, she found that monarch eggs were less likely to survive on plants on which ants had been observed, suggesting that ants are important predators. This conclusion is supported by work in Texas by Calvert (1996, 2004), who found that monarchs inside exclosures were much more likely to survive than those outside the structures. Calvert found that invasive fire ants currently kill most of the monarch eggs and larvae present in many areas in Texas, but thinks that pre-fire ant mortality may have been similarly high, since these invasive ants displaced native ants that also preyed on monarchs. In addition to predators, insect parasitoids are important sources of monarch mortality in some locations. Prybsy (2004) and the Monarch Larva Monitoring Project have both documented mortality rates of from 10% to 90% in late instar monarchs due to tachinid fly (family Tachinidae) parasitoids, but these rates are variable from location to location and year to year.
||Figure 8. Monarch eggs and larvae have many invertebrate predators, including this red velvet spider mite, shown here sucking the contents from a monarch egg. Photo by Karen Oberhauser.
Monarch eggs do not hatch in very dry conditions (Dunlap et al. 2000), and dry weather can kill milkweed. Very hot weather also causes mortality; several studies have shown that temperatures above approximately 35oC (95oF) can be lethal to all stages (Zalucki 1982, Malcolm et al. 1987, York and Oberhauser 2003). Likewise, extended periods in which temperatures are below freezing can kill monarchs, although this has been best studied in overwintering adults (Anderson and Brower 1993, 1996; Brower et al. 2004). Threats due to very hot or very cold temperatures are magnified during the breeding season, since monarchs are indirectly affected by conditions that affect milkweed health and survival. Freezing temperatures and extremely dry conditions are especially damaging to milkweed, and thus to monarchs.
Pupae. During the pupa stage the transformation to the adult stage is completed in a process that takes about 9 to 15 days under normal summer temperatures. The ecology of monarch (or any other lepidopteran) pupae is unfortunately poorly-studied, at least partially due to the fact that it is extremely difficult to find monarch pupae in the wild. Their green color provides effective camouflage in a green world, and they appear to seek sheltered spots to undergo this transformation. Important questions on how larvae choose sites for pupation, how far they travel seeking these sites, what habitat characteristics are important in promoting pupal survival, and how much mortality from different sources occurs during this stage remain to be investigated.
Adults (Figure 9). Non-migratory adults live from two to five weeks, while those that migrate may live up to nine months. This difference is due to the fact that overwintering monarchs are not reproductive, and can thus funnel more energy into survival. In addition, the cool conditions in the overwintering sites slow their metabolism.
Figure 9. An adult female monarch butterfly. Photo by Barbara Powers.
Summer generation monarchs first mate when they are 3 to 8 days old (Figure 10) (Oberhauser and Hampton 1995), and females begin laying eggs immediately after their first mating. Monarchs that overwinter do not lay eggs until spring (although they may mate before this). Both sexes can mate several times during their lives (e.g., Oberhauser 1989), and the ability of male monarchs to force unwilling females to copulate makes them unique among the Lepidoptera (Oberhauser 1989; Van Hook 1993; Frey et al. 1998). When females mate with more than one male, it is generally the last male that fertilizes their eggs (Solensky 2003, Oberhauser personal observation).
||Figure 10. A mating pair. Both male and female monarchs often mate several times during their lives, and remain paired for several hours. Photo by Karen Hanson.
Since there is a delay between adult emergence and egg-laying, and also because monarchs reproduce over a relatively long time period, maximizing reproductive success also requires being able to survive predators, environmental extremes and other sources of mortality. Adult survival during the breeding season is another under-studied area of monarch biology, despite its importance to monarch ecology. Full understanding of adult ecology during the breeding stage of their lives will require measuring the effects of nectar availability and quality, the distances that females will fly to find milkweed host plants, the degree to which breeding monarchs remain in one area or move, and the effects of abiotic conditions on adult survival (Oberhauser 2004).
Human-induced mortality during the breeding season. As with many other species, the most important source of human-caused mortality for monarchs is habitat loss, especially the destruction of milkweed and nectar sources. Milkweed is considered a noxious weed in some localities, and is often destroyed. In addition, herbicides used to kill plants in agricultural fields, near roadsides, and in gardens may harm milkweed and nectar sources, and may also kill monarchs directly. This has probably become much more important in agricultural fields with the widespread adoption of herbicide-tolerant crops. In a study conducted in the summer of 2000, Oberhauser et al. (2001) found that most monarchs probably originated in agricultural habitats. However, since that study, most soybeans grown in the upper Midwestern US, the source of most overwintering monarchs (Wassenar and Hobson 1998), are herbicide-tolerant. The increased use of herbicides allowed by herbicide tolerant crops means that fields have many fewer milkweeds than before (Oberhauser unpublished). Monarchs can also be exposed to insecticides used to control insect pests in agricultural fields, forests, and gardens. Many people worry that the use of insecticides to combat mosquito-borne diseases like the West Nile Virus will kill monarchs and other beneficial insects.
The risks to monarchs of corn genetically modified to contain Bt (Bacillus thuringiensis) toxin have received a great deal of attention (Losey et al. 1999; Jesse and Obrycki 2000; Oberhauser et al 2001; Sears et al. 2001; Brower 2001). Bt corn produces a protein that is toxic to lepidopteran larvae, and is effective against European corn borers, important agricultural pests. However, the wind-dispersed pollen produced by Bt corn also carries the toxin. The toxicity of the pollen produced by different corn varieties varies significantly, and the varieties now on the market have lower levels of toxin that some of the earlier varieties (Hellmich et al. 2001; Sears et al. 2001). Most researchers who have assessed the risks of this technology isolated corn pollen from other material shed by the plant (particularly the pollen-bearing anthers) (Hellmich et al. 2001; Sears et al. 2001), but Jesse and Obrycki (2004) found a consistent trend of lower survival in Bt fields than non-Bt fields when larvae were exposed to Bt corn pollen and anthers naturally deposited on milkweed plants within a corn field. This finding suggests that the blanket conclusion that Bt corn poses no risks to monarchs (Sears et al. 2001) should be revisited.
Fall Migration Ecology
Overview: Unlike most temperate insects, monarch butterflies cannot survive extended periods of freezing temperatures, so North American monarchs fly south to spend the winter at roosting sites. In the spring, these overwintering monarchs fly north toward their breeding range. The monarch is the only butterfly to make such a long, two-way migration, flying up to 4830 kilometers in the fall to reach its winter destination (Urquhart and Urquhart 1978). Monarchs east of the Rocky Mountains generally fly to overwintering sites in the mountains of central Mexico, while monarchs west of the Rocky Mountains typically overwinter along the California coast, although recent observations by Pyle (1999) suggests that some western monarchs move south and southeast out of the inland northwest and Great Basin, entering Mexico from Arizona. The magnitude and destination of this movement is not understood. Another unanswered question about the western North American monarch population is the degree to which it is truly migratory, or whether it undergoes an annual range expansion and contraction in California. Wenner and Harris (1993) suggest that many monarchs are year-round residents of California whose offspring are able to spread to surrounding states during the mild summer weather but are forced to return to California or perish when the inhospitable northern winters return. This issue is still being debated.
Stable isotope studies (Wassenaar and Hobson 1998) and recoveries of tagged butterflies (Urquhart and Urquhart 1978, Monarch Watch 2004 and OR Taylor personal communication) suggest that the majority of monarchs that migrate to Mexico originate in the Midwest. However, these studies also show that the overwintering populations are comprised of monarchs coming from a wide geographic area that covers much of the range shown in Figure 11 (below). Unfortunately, similar studies revealing the origins of monarchs overwintering in California have not been conducted.
|| Figure 11. Monarchs fly south and southwest during the fall migration, funneling through Texas to overwintering sites in the mountains of central Mexico. Drawing by Sonia Altizer and Michelle Solensky.
Australian monarchs also exhibit seasonal movement, moving from inland to coastal areas in a north to northeasterly direction during the fall and winter (James 1993). However, because the most spectacular monarch migrations (in terms of distance and numbers of migrants) occur in the eastern North American population, much of the research on monarch migration has focused on this population. These insects, weighing about half a gram, fly from their summer breeding range that covers more than 100 million ha, to winter roosts that cover less than 20 ha. Since the discovery of these winter roosts in Mexico by the scientific community in 1975 (Urquhart 1976), researchers have struggled to understand the cues that cause monarchs to begin their migration, the mechanisms they use to orient and find the overwintering sites and the patterns of fall and spring flight.
Initiation of migration. While non-migratory monarchs become reproductive within a few days of eclosion, late summer and early fall monarchs emerge in reproductive diapause, a state of suspended reproductive development. Diapause is controlled by neural and hormonal changes (Barker and Herman 1976, Herman 1981) triggered by environmental factors that signal the onset of unfavorable conditions, in this case winter. Goehring and Oberhauser (2002) found that decreasing daylength, fluctuating temperatures and senescing host plants each caused an increase in the proportion of monarchs that emerged in reproductive diapause, but the strongest response occurred among monarchs exposed to all three cues. Making use of more than one cue to assess current and near future habitat suitability could be a more optimal strategy for organisms in unpredictable environments.
Perez and Taylor (2004) tested the common assumption that reproductive diapause and migratory behavior in monarchs are coupled by exposing fall migrants to summer daylengths and temperatures. These butterflies exhibited reproductive behavior, but continued to show migratory flight directionality. They argue that while reproductive diapause can be readily reversed in fall migrants, migratory behavior is resistant to changes in environmental conditions. This finding is supported by Borland et al. (2004) and data from the Monarch Larva Monitoring Project (2004); many monarchs appear to become reproductive when they reach the southern US during their fall migration. The importance of this late reproduction to overall monarch population dynamics, and the environmental triggers that promote it, is still undetermined, but it suggests that an increase in the availability of milkweed in gardens and parks may trigger reproduction (Goehring and Oberhauser 2004).
Orientation and migration pathways. Insect orientation in general is poorly understood, and monarchs are no exception. The ability of monarchs that are spread over 100 million ha to converge in a very small area in the mountains of central Mexico is mind-boggling, and may be one of the most compelling mysteries of animal ecology. Other animals use celestial cues (the sun, moon, or stars), the earth’s magnetic field, landmarks (mountain ranges or bodies of water), polarized light, infra-red energy perception, or some combination of these cues to migrate, but the degree to which these cues are used by monarchs is not known. Calvert and Wagner (1999) proposed that mountain ranges and river valleys might be used by monarchs to orient during their migration, but celestial cues and the earth’s magnetic field have been studied the most.
Many researchers agree that the sun is the celestial cue most likely to be used by southward migrating monarchs. Kanz (1977) and Schmidt-Koenig (1985, 1993) suggested that monarchs use the angle of the sun along the horizon in combination with an internal body clock to maintain a southwesterly flight path, and Mouritsen and Frost (2002) confirmed this hypothesis. Because monarchs often migrate on cloudy days, this sun compass must be combined with the use of some other cue. Scientists have suggested that monarchs may use a magnetic compass to orient, as has been demonstrated in some migratory birds (Wiltschko and Wiltschko 1972, Emlen et al. 1976). However, Mouritsen and Frost (2002) showed that migratory monarchs exhibited randomly oriented flight when presented with only magnetic field cues and did not respond to magnetic field shifts, suggesting that monarchs do not use the earth’s magnetic field to orient during migration. They propose that monarchs may use polarized light patterns, which penetrate cloud cover, to orient on cloudy days.
The first large-scale study of the fall monarch migration began in 1937 when Dr. Fred Urquhart recruited volunteers for his insect migration study, which involved putting small paper tags on the leading edge of the monarch forewing and obtaining both release and capture locations for tagged butterflies (Urquhart and Urquhart 1977). In the fall of 1992, a new tagging program was established (Monarch Watch 2001) to continue the study of fall migratory routes. These tagging programs have revealed much information about the patterns and timing of the fall monarch migration. Several studies have shown that monarchs generally migrate in a south to southwest direction (Gibo 1986; Schmidt-Koenig 1985), with a shift from south to southwest as the origin of flight moves from west to east (Rogg et al. 1999). More recently, Wassenaar and Hobson (1998) used stable isotopes to estimate the origin of monarchs overwintering in central Mexico. They found that about half of the monarchs collected from 13 overwintering sites had migrated from the midwestern US, with smaller numbers originating from the northeastern US and Canada. While tagging reveals patterns of individual fall migrants, stable isotope studies show promise for revealing population-level migratory patterns.
Behavior during migration. Like migratory birds, monarchs make frequent stops during migration, forming roosts at night and during inclement weather that range in size from a few dozen to a few thousand individuals. Little is known about this roosting phenomenon, but recently Davis and Garland (2004) used methods from ornithological studies to investigate factors influencing monarch stopover decisions. They found that monarchs commonly stayed at roosting sites for at least 2 days, and proposed that levels of energy reserves may influence monarch migration and stopover decisions, with monarchs staying longer at stopover sites when their lipid reserves are small. Both Borland et al. (2004) and Gibo and McCurdy (1993) found that monarchs collected in the south were heavier than those captured in the north, suggesting that nectaring along the migratory path results in weight gain and increased energy reserve (Figure 12). These findings support the suggestion that energy reserves may influence monarch migration decisions. While orientation mechanisms have gained much attention from researchers, few studies have addressed stopover ecology or characteristics of monarchs that increase migratory success.
||Figure 12. Monarch nectaring on a flower of the northern blazing star (Liatris borealis). Blazing star and other late summer flowers provide necessary nutrients for monarchs during their fall migration. Photo by David Astin.
Monarch Overwintering Ecology
Overview: Monarchs regularly congregate in two major regions of North America during the winter: central Mexico and coastal California (Brower 1995). They also reside in southern Florida throughout the year, but this population receives an influx of migratory individuals from the eastern migratory each fall (Knight 1997; Altizer 2001). The degree to which monarchs from Florida move back into the larger population is not understood.
It has been generally assumed that monarchs spending the summer breeding season west of the Rocky Mountains overwinter along the coast of southern California, although the recent observations by Pyle (1999) described above suggest that there are exceptions to this pattern. The California sites are usually wooded areas dominated by eucalyptus trees, Monterey pines, and Monterey cypresses, and are located in sheltered bays or farther inland. These sites provide moderated microclimate extremes and protection from strong winds. More than 300 different aggregation sites have been reported (Frey and Schaffner 2004; Leong et al., 2004).
North American monarchs that spend the summer breeding season east of the Rocky Mountains overwinter in oyamel fir (Abies religiosa) forests in the Transvolcanic mountains of central Mexico. The location of these overwintering sites was unknown to the scientific community until 1975 when associates of Dr. Fred Urquhart located colonies on Cerro Pelón and Sierra Chincua in the state of Michoacan (Urquhart 1976; Brower 1995). Since then, several more overwintering locations have been located; colonies within the Monarch Butterfly Biosphere Reserve are found in the states of Michoacán and México (Cerro Altamirano, Cerros Chivatí-Huacal, Sierra Chincua, Sierra El Campanario and Cerro Pelón). Outside the Reserve, colonies are found in San Andres, Pizcuaro, Puerto Morillo and Puerto Bermeo (Michoacán) and Palomas, Piedra Herrada and San Francisco Oxtotilpan (México) (Garcia et al. 2004). While scientists have learned much about the phenomenon of monarch overwintering in the past few decades, several basic questions remain. Measuring the density of an organism that congregates by the millions presents a formidable challenge. Scientists also seek to understand the characteristics of the overwintering sites that are most important to monarch survival, and the factors that influence patterns of colony formation and dispersal.
Colony formation and dispersal. Throughout the winter, North American monarchs cluster together, covering whole tree trunks and branches (Figure 13). Calvert (2004b) describes four phases typical of colony development in Mexico sites: recruitment and consolidation, settling and compaction of clusters, expansion and rapid movement, and mating and dispersal. This pattern is similar in California (Frey and Schaffner 2004). Initially monarchs occupy many local habitats, but abandon many of them by late November and join nearby colonies. Before the monarchs disperse, many of them become reproductive, and the colonies are often filled with mating pairs.
||Figure 13. On their wintering grounds in Mexico, monarchs cluster on oyamel fir branches and trunks for much of November through mid-March. Photo by Andy Davis.
The timing of the last phase, mating and dispersal, depends on the timing of completion of reproductive diapause, which varies considerably among individuals. Goehring and Oberhauser (2004) studied post-diapause reproductive development in monarchs overwintering in Mexico. They found a great deal of variation in reproductive status of monarchs collected in late February and early March, with some butterflies fully reproductive while most were still in diapause. Females collected while mating were more likely to have developed oocytes (an indication that they were no longer in diapause) than females collected from clusters. If there is a cause and effect relationship that results in this correlation, it is not clear whether females were more likely to be mating because they were further along in their reproductive development, or if mating actually triggered the end of diapause. Both Van Hook (1993) and Oberhauser and Frey (1999) found that males which began mating first at the end of the overwintering period had shorter wingspans, were lighter, and had poorer wing condition than males that were collected in roosts at the same time. They suggest that these males are unlikely to survive the return migration north, and are thus taking advantage of their last, and only, opportunity to mate.
Overwintering densities. Scientists use many methods to estimate population sizes of insects and other animals, but determining overwintering monarch abundance is particularly challenging because of their mobility and huge numbers. Nearly 30 years after the discovery of the Mexican overwintering sites, scientists are still debating how to best estimate monarch density there. Calvert (2004b) used mark, release, recapture techniques to estimate the population densities of 7 to 61 million monarchs per ha, with higher densities occurring later in the season when the colony had contracted. At a different colony, he measured monarch density on sub-samples of tree branches and trunks to estimate 12 million monarchs per hectare. These numbers are within the ranges suggested by Brower (1977) and Brower et al. (1977), but the large variation suggests that densities probably are not constant across the season and between different colonies.
Garcia et al. (2004) monitored 22 Mexican overwintering sites from 1993 to 2002. Using an estimate of 10 million monarchs per hectare, they found that the overwintering population ranged from 23 million monarchs in 2000-2001 to 176 million in 1996-1997 (Figure 14). They measured the highest mortality (27.7%) during a low population year (1997-1998, 45.5 million monarchs) and suggest that mortality rate may decrease with increasing population size.
Figure 14. A single monarch colony may contain several million monarchs, as seen in this photo taken of the El Rosario (Sierra el Campanario, Michoacan Mexico) colony from the air. Note the orange color of the monarchs and the deforestation that has occurred up to the colony edge.
Photo by Lincoln Brower.
Microclimate conditions in the overwintering sites. Monarchs migrate to specific overwintering sites because they require particular environmental characteristics to survive throughout the winter. Survival of overwintering monarchs in Mexico from November through March depends on a delicate balance of macro- and microclimatic factors that characterize the oyamel fir forests located within the reserve (Calvert and Brower 1986; Alonso et al. 1992, 1997). High humidity and temperatures that fluctuate between 3o and 18o C characterize these forests, and several studies (Calvert and Brower 1981; Calvert and Cohen 1983; Calvert et al. 1982, 1983, 1984, 1986; Alonso-Mejia et al. 1992; Anderson and Brower 1993; Brower 1999) have shown that an intact forest ecosystem promotes winter survival. Butterflies in thinned forests are more likely to get wet during winter storms, and wet monarchs are unable to survive extremely cold temperatures, such as those that occurred during storms in 2002 (Brower et al. 2004) and 2004. In addition, thinned forests become colder at night because heat escapes from them more easily. Thus, an intact forest serves as both an umbrella, protecting the butterflies from snow and rain during winter storms, and a blanket, keeping the butterflies from freezing (Anderson and Brower 1996).
Recent modeling efforts (Bojórquez-Tapia 2003, Missrie 2004) show that preferred habitats of overwintering monarchs share four features: 1) high elevations (most colony sites are located at altitudes over 2890 m); 2) proximity to streams (most sites occur less than 400 m from permanent or ephemeral streams; 3) moderately steep slopes (between 23° and 26°); and 4) south-southwest orientation. In most cases, these conditions occur in oyamel fir forests, but colony sites also exist below these forests, primarily because the butterflies move to lower altitudes (where mixed forest stands occur) as spring advances.
Frey and Schaffner (2004) examined abundance on three temporal scales (spanning 1, 4 and 20 years) for western overwintering sites, using data from the California Department of Fish and Game Natural Diversity Data Base and The Monarch Program Thanksgiving Count (Marriott 2001). During the period 1997 through 2000, from 101 to 141 known sites were surveyed. Numbers of monarchs per site ranged from 0 to 120,000, with large year to year and site to site variation (Frey and Schaffner 2004). Sites near the coast that contained eucalyptus, pine and cypress tended to have more monarchs. Leong et al. (2004) found that higher monarch abundance in central California was associated with high ambient moisture, substantial morning dew and moderate winter temperatures. GIS analyses showed that most winter groves occurred within 2.4 km of the coastline, on slopes with a south to west orientation. Larger winter sites were associated with the lower slope of valleys, bays and coastal inlets. Frey and Schaffner (2004) placed their findings in a continent-wide context by making comparisons between recent population trends in the western and eastern North American populations. While the eastern population is larger than the western by at least two orders of magnitude (Brower 1985), it appears that both populations fluctuate from year to year by about half an order of magnitude. However, because no correlation between abundance in the two populations was found, their patterns may be caused by different factors.
Both Frey and Schaffner (2004) and Leong et al. (2004) advocate the use of these and similar analyses in evaluating land management practices and structuring conservation goals. Leong et al. argue that preservation of the monarch winter aggregations in California will depend on active and long-term habitat management that focuses on enhancement activities, such as tree planting, trimming and, in some cases, removal.
Winter mortality. Monarchs in the overwintering congregations in Mexico and California face numerous threats. In addition, forest degradation and resultant changes in climatic conditions, predation by birds and mice, starvation, desiccation and freezing represent significant sources of mortality. Although monarchs are protected from vertebrate predators by the cardenolides sequestered from the milkweed they consume as larvae, any concentration of potential prey this large is likely to result in predators that evolve to overcome their defenses. Bird predation is an important cause of winter mortality, with mortality rates ranging from 1% to 18% across several colonies studied by Garcia et al. (2004) and from to 7% to 44% in colonies studied by Brower and Calvert (1985). The two main bird predators are the black-headed grosbeak (Pheucticus melanocephalus) and the black-backed oriole (Icterus abeillei). The grosbeaks consume the entire fat-rich abdomens of the monarchs, somehow tolerating the cardenolide toxins stored below the exoskeleton. The orioles slit open the abdomen with their sharp beak and scoop the contents of the abdomen and thorax out with their tongue, thus avoiding the toxins. These different prey consumption methods make it easy to distinguish which species is responsible for the deaths of monarchs found on the forest floor. At least five species of mice, the most conspicuous of which is Peromyscus melanotis, feed on butterflies that have fallen to the ground.
Extreme weather conditions, such as those caused by winter rains and snowstorms, can also kill overwintering monarchs. For example, the intense cold that followed a prolonged period of cloudy, wet weather early in 1992 may have killed up to 80% of monarchs in several overwintering colonies (Brower et al. 2004). Systematic documentation of mortality that followed another severe storm in January 2002 is reported by Brower et al. (2004). They estimated 75-80% mortality at two overwintering colonies, and suggest that similar rates occurred throughout the Mexico sites. Their estimates of the number of monarchs killed per hectare (26-72 million) far exceeded previous estimates of the number of monarchs occupying these sites, but agree with estimates presented by Calvert (2004) for the same time of year. Oberhauser and Peterson (2003) used ecological niche modeling to delineate the environmental conditions that favor survival, and found that occupied sites exhibited cool temperatures and low precipitation during the wintering months. Unfortunately, global climate change models predict more precipitation in these areas over the next decades, suggesting that those kinds of winter storms may become more frequent.
While there is no documentation of the effects of extremely dry years on monarch survival, the fact that individuals are often observed imbibing water that collects as dew on plants or from streams or wet ground suggests that a lack of moisture would increase mortality. Likewise, little is known about factors that increase the risks of starving. Monarchs eat little during the overwintering period, so it is likely that starvation would be more likely under conditions that promote increased metabolism, such as warm ambient air temperatures, or when monarchs do not obtain enough food as larvae.
Forest dynamics and conservation of overwintering sites. The Mexican overwintering sites first achieved protected status under a 1986 presidential decree. While this was an important first step, the decree did not protect all important overwintering sites, failed to compensate local landowners for imposed restrictions on land use and offered no effective economic alternatives to previous means of subsistence (such as agriculture and logging). A consortium of geographers, monarch biologists and Mexican government officials conducted a geographic information system (GIS) analysis of deforestation that occurred between 1971 and 1999. This analysis revealed that 44% of the high quality forest present in 1971 had been degraded and fragmented, resulting in lower quality forest for overwintering monarchs (Brower et al. 2002). The rate of deforestation had accelerated over this period.
In 1998, an international group of scientists and policy makers joined to redefine the protected area and address some of the concerns with the original decree. Missrie (2004) described the 4-year process that led to a new presidential decree and improved protection of the overwintering sites. The boundaries of the expanded Reserve were determined using models based on current knowledge of the biological requirements of monarchs during the winter. As a result of the new decree, the total amount of land that was protected increased from 16,110 ha (4491 and 11,619 in the core and buffer zones, respectively) to 56,259 ha (13,552 and 42,707 ha in the core and buffer zones respectively). The new reserve protects a contiguous area of land, instead of the separate "islands" of land that were protected by the old decree (Missrie 2004). However, as is the case with all conservation laws, effectiveness requires enforcement of the law, and logging and forest degradation are still occurring.
Keiman and Franco (2004) studied the response of the Mexican oyamel fir forests to disturbance. Their finding that trees within forest patches tend to be similar in size, and that homogeneity tends to increase with stand age, along with the fact that monarchs typically form colonies in mature forests, suggests that it will be important to ensure replacement as forest patches age.
Spring Migration Ecology
Monarch butterflies begin to leave their Mexican wintering sites in mid-March, and have usually all departed by the end of March. At this point, many of them have already mated, but both sexes leave the sites and migrate north and mating continues throughout the journey north. Malcolm et al. (1993) and Cockrell et al (1993) reported the dates of first sightings of eggs, larvae and the larval host plants of adult monarchs arriving at different latitudes in eastern North America. These papers established the general pattern of spring movement and demonstrated that recolonization of the northern ranges of the breeding habitat occurs over two generations. The monarchs that overwinter in Mexico fly north to repopulate the southern half of the US, and their offspring complete the journey to the northern US and southern Canada. This second generation recolonizes the entire northern breeding range, utilizing more northern milkweed species (See Figure 15).
||Figure 15. Spring migration: The first part of the spring migration is made by the same adults that flew south in the fall, but these migrants do not recolonize the entire summer breeding range. It is their offspring, laid as eggs in late March and April, that complete the spring journey north. Drawing by Sonia Altizer and Michelle Solensky.
Spring migratory routes are considerably more difficult to identify and study than fall routes because in the spring monarchs are dispersed and consequently less noticeable than the fall migrants which form spectacular roosts. We are still learning a great deal about this portion of the monarchs’ annual cycle from individuals that report their monarch observations as part of Citizen Science programs, such as Journey North (Howard and Davis 2004). This program involves school children and other interested individuals from every US state and seven Canadian provinces, who report their first sightings of monarch butterflies every spring. Through these reports, we can learn about when and where monarchs travel as they migrate north in the spring.
Howard and Davis (2004) described the patterns of spring migration and monarch abundance based on data collected by Journey North participants over a 6-year period from 1997 to 2002. They found a striking regularity of the migratory pattern from year to year, although the average arrival date at different latitudes and the duration of migration varied between years. They suggest that this annual variation may stem from differences in environmental conditions or timing of milkweed emergence, and are continuing to investigate these factors using additional data collected by Journey North participants.
Ackery PR, Vane-Wright RI (1984) Milkweed Butterflies: Their Cladisitics and Biology. Ithaca, NY: Cornell University Press
Alonso-Mejia A, Arellano-Guillermo A, Brower LP (1992) Influence of temperature, surface body moisture and height aboveground on survival of monarch butterflies overwintering in Mexico. Biotropica 24: 415-19
Alonso-Mejía A, Rendón-Salinas E, Montesinos-Patiño E, Brower LP (1997) Use of lipid reserves by monarch butterflies (Danaus plexippus L.) overwintering in Mexico: implications for conservation. Ecological Applications 7: 934-47
Altizer SM (2001) Migratory behaviour and host-parasite co-evolution in natural populations of monarch butterflies infected with a protozoan parasite. Evolutionary Ecology Research 3: 611-32
Anderson JA, Brower LP (1993) Cold-hardiness in the annual cycle of the monarch butterfly. Pp. 157-64 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Anderson JB, Brower LP (1996) Freeze-protection of overwintering monarch butterflies in Mexico: Critical role of the forest as a blanket and an umbrella. Ecological Entomology 21: 107-16
Barker JF, Herman WS (1976) Effect of photoperiod and temperature on reproduction of the Monarch butterfly, Danaus plexippus. Journal of Insect Physiology 22: 1565-68
Boggs CL, Gilbert L (1979) Male contribution to egg production in butterflies: Evidence for transfer of nutrients at mating. Science 206: 83-84
Bojórquez-Tapia LA, Brower LP, Castilleja G, Diaz S, Sanchez-Colón S, Gomez-Priego P, Zuñiga N, Alcantar G, Daniela ME, Solares MJ, Gutiérrez L, Juárez MDL, Hernández M, Calvert WH (2003) Mapping expert knowledge: Redesigning the monarch butterfly reserve. Conservation Biology 17: 67-79
Borkin SS (1982) Notes on shifting distribution patterns and survival of immature Danaus plexippus (Lepidoptera: Danaidae) on the food plant Asclepias syriaca. Great Lakes Entomology 15: 199-207
Borland J, Johnson C, Crumpton T, Thomas T, Saltizer S, Oberhauser K (2004) Characteristics of Fall Migratory Monarch Butterflies, Danaus plexippus, in Minnesota and Texas. Pp. 97-104 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Brower LP (1977) Monarch Migration. Natural History 84: 40-53
Brower LP (1995) Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857-1995. J. Lepid. Soc. 49: 304-85
Brower LP (1999) Biological necessities for monarch butterfly overwintering in relation to the Oyamel forest ecosystem in Mexico. Pp. 11-28 in The 1997 North American Conference on the Monarch Butterfly. Hoth J, Merino L, Oberhauser K, Pisantry I, Price S and Wilkinson T (eds). Commission for Environmental Cooperation, Montreal, Canada
Brower LP (2001) Canary in the cornfield. Orion 20: 32-41
Brower LP, Moffit CM (1974) Palatability dynamics of cardenolides in the monarch butterfly. Nature 249: 280-83
Brower LP, Castilleja G, Peralta A, Lopez-Garcia J, Bojorquez-Tapia L, Diaz S, Melgarejo D, Missrie M (2002) Quantitative changes in forest quality in a principal overwintering area of the monarch butterfly in Mexico: 1971 to 1999. Conservation Biology 16: 346-359
Brower LP, Calvert WH, Hendrick LE, Christian J (1977) Biological observations of an overwintering colony of monarch butterflies (Danaus plexippus, Danaidae) in Mexico. J. Lepi. Soc. 31: 232-42
Brower LP, Kust DR, Rendon-Salinas E, García Serrano E, Kust KR, Miller J, Fernandez del Rey C, Pape K (2004) Catastrophic Winter Storm Mortality of Monarch Butterflies in Mexico during January 2002. Pp. 151-166 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Calvert WH (2004a) The effect of fire ants on monarchs breeding in Texas. Pp. 47-54 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Calvert WH (2004b) Two methods for estimating overwintering monarch population size in Mexico. Pp. 121-128 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Calvert WH, Wagner M (1999) Patterns in the monarch butterfly migration through Texas–1993 to 1995. Pp. 119-25 in The 1997 North American Conference on the Monarch Butterfly. Hoth J, Merino L, Oberhauser K, Pisantry I, Price S and Wilkinson T (eds). Commission for Environmental Cooperation, Montreal, Canada
Calvert WH, Cohen JA (1983) The adaptive significance of crawling up onto foliage for the survival of grounded overwintering monarch butterflies (Danaus plexippus) in Mexico. Ecological Entomology 8: 471-74
Calvert WH, Brower LP (1981) The importance of forest cover for the survival of overwintering monarch butterflies (Danaus plexippus, Danaidae). J. Lepid. Soc. 35: 216-225
Calvert WH, Brower LP (1986) The location of monarch butterfly (Danaus plexippus L.) overwintering colonies in Mexico in relation to topography and climate. J. Lepid. Soc. 40: 164-187
Calvert WH, Hyatt MB, Mendoza-Villasenor NP (1986) The effects of understory vegetation on the survival of overwintering monarch butterflies, (Danaus plexippus L.) in Mexico. Acta Zool. Mex. 18: 1-17
Calvert WH, Zuchowski W, Brower LP (1982) The impact of forest thinning on microclimate in monarch butterfly (Danaus plexippus L.) overwintering areas of Mexico. Bol. Soc. Bot. Mex. 42: 11-18
Calvert WH, Zuchowski W, Brower LP (1983) The effect of rain, snow, and freezing temperatures on overwintering monarch butterflies in Mexico. Biotropica 15: 42-47
Calvert WH, Zuchowski W, Brower LP (1984) Monarch butterfly conservation: interactions of cold weather, forest thinning and storms on the survival of overwintering monarch butterflies (Danaus plexippus L.) in Mexico. Atala 9: 2-6
Cockrell BJ, Malcolm SB, Brower LP (1993) Time, temperature and latitudinal constraints on the annual recolonization of eastern North America by the monarch butterfly. Pp. 233-251 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Davis AK, Garland MS (2004) Stopover ecology of monarchs in coastal Virginia: Using Ornithological Techniques to Study Monarch Migration. Pp. 89-96 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Dunlap B, Hannigan A, Petersen C, Boettcher C, Bradbury S, Evans J, Keith A, Nelson S, Warber J (2000) The Effect of Humidity on the Egg Development and Survivorship of the Monarch Butterfly (Danaus plexippus). Monarch Lab website: http://www.monarchlab.org/research/GD/Chan.html. Accessed 9/13/2004
Emlen ST, Wiltschko W, Demong N, Wiltschko R, Bergman S (1976) Magnetic direction finding in migratory indigo buntings. Science 193: 505-508
Frey D, Leong KLH, Peffer E, Smidt RK, Oberhauser KS (1998) Mating patterns of overwintering monarch butterflies (Danaus plexippus (L.)) in California. J. Lepid. Soc. 52: 84-97
Frey D, Schaffner A (2004) Spatial and Temporal Pattern of Monarch Overwintering Abundance in Western North America. Pp. 167-176 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
García-Serrano E, Lobato Reyes J, Mora Alvarez BX (2004) Locations and Area Occupied by Monarch Butterflies Overwintering in Mexico from 1993 – 2002. Pp. 129-134 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Gibbs G (1994) The Monarch Butterfly. Auckland, New Zealand: Reed Publishing
Gibo DL (1986) Flight strategies of migrating monarch butterflies (Danaus plexippus L.) in southern Ontario. Pp. 172-184 in Insect Flight: Dispersal and Migration. Danthanarayana W (ed). Springer-Verlag, Berlin
Gibo DL, McCurdy JA (1993) Lipid accumulation by migrating monarch butterflies (Danaus plexippus L.). Canadian Journal of Zoology 71: 76-82
Goehring L, Oberhauser KS (2002) Effects of photoperiod, temperature and host plant age on induction of reproductive diapause and development time in Danaus plexippus. Ecological Entomology 27: 674-685
Goehring L, Oberhauser KS (2004) Environmental Factors Influencing Postdiapause Reproductive Development in Monarch Butterflies. Pp. 187-198 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Haribal M (1998) Identification and distribution of oviposition stimulants for monarch butterflies in hosts and nonhosts. Journal of Chemical Ecology 24: 891-903
Hellmich RL, Siegfried BD, Sears MK, Stanley-Horn DE, Daniels MJ, Mattila HR, Spencer T, Bidne KG, Lewis LC (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proc. Natl. Acad. Sci. USA 98: 11925-30
Herman WS (1981) Studies on the adult reproductive diapause of the monarch butterfly, Danaus plexippus. Biol. Bull. 160: 89-106
Howard E, Davis AK (2004) Documenting the Spring Movements of Monarch Butterflies with Journey North, a Citizen Science Program. Pp. 105-116 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
James DG (1993) Migration biology of the Monarch butterfly in Australia. Pp. 189-200 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Jesse LCH, Obrycki JJ (2000) Field deposition of Bt transgenic corn pollen: Lethal effects on the monarch butterfly. Oecologia 125: 241-48
Jesse LCH, Obrycki JJ (2004) Survival of Experimental Cohorts of Monarch Larvae Following Exposure to Transgenic Bt Corn Pollen and Anthers. Pp. 69-78 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Kanz JE (1977) The orientation of migrant and non-migrant monarch butterflies, Danaus plexippus (L.). Psyche 84: 120-41.
Knight AL (1997) A Population Study of Monarch Butterflies in north-central and south Florida. Master’s thesis, University of Florida, Gainesville.
Leong KLH, Sakai WH, Bremer W, Fauerstein D, Yoshimura G (2004) Analysis of the pattern of distribution and abundance of monarch overwintering sites along the California coastline. Pp. 177-186 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399: 214.
Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defense paradox. Entomol. Exp. Appl. 80: 193-196
Malcolm SB, Cockrell BJ, Brower LP (1987) Monarch butterfly voltinism: effects of temperature constraints at different latitudes. Oikos 49: 77–82
Malcolm SB, Cockrell BJ, Brower LP (1993) Spring recolonization of eastern North America by the monarch butterfly: successive brood or single sweep migration? Pp. 253-267 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Mattson WJ Jr. (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11: 119-161
McNeil S, Southwood TRE (1978) The role of nitrogen in the development of insect/plant relationships. Pp. 77-98 in Biochemical Aspects of Plant and Animal Coevolution. Harborne JB (ed). Academic, London, UK
Missrie M (2004) Design and Implementation of a New Protected Area for Overwintering Monarch Butterflies in Mexico. Pp 141-150 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Monarch Larva Monitoring Project (2004) www.mlmp.org. Accessed 9/13/2004
Monarch Watch (2004) www.monarchwatch.org. Accessed 9/13/2004
Mouritsen H, Frost BJ (2002) Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proceedings of the National Academy of Sciences 99: 10162-10166
Oberhauser KS (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behavioral Ecology and Sociobiology 25: 237 46
Oberhauser KS (1997) Fecundity and egg mass of monarch butterflies: effects of age, female size and mating history. Functional Ecology 11: 166-75
Oberhauser KS (2004) Overview of monarch breeding biology. Pp. 3-8 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Oberhauser KS, Hampton R (1995) Relationship between mating and oogenesis in monarch butterflies. Journal of Insect Behavior 8: 701-13
Oberhauser KS, Prysby MD, Mattila HR, Stanley-Horn DE, Sears MK, Dively G, Olson E, Pleasants JM, Lam WF, Hellmich RL (2001) Temporal and spatial overlap between monarch larvae and corn pollen. Proceedings of the National Academy of Sciences 98: 11913-18
Perez SM, Taylor OR (2004) Monarch Butterflies’ Migratory Behavior Persists Despite Changes in Environmental Conditions. Pp. 85-88 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Pyle RM (1999) Chasing Monarchs. Houghton Mifflin, Boston
Prysby M (2004) Natural Enemies and Survival of Monarch Eggs and Larvae. Pp. 27-38 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Prysby M, Oberhauser K (2004) Temporal and geographical variation in monarch densities: Citizen scientists document monarch population patterns. Pp. 9-20 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Rayor LS (2004) Effects of monarch larval host plant chemistry and body size on Polistes wasp predation. Pp. 39-46 in The Monarch Butterfly: Biology and Conservation. Oberhauser KS, Solensky MJ (eds). Cornell University Press, Ithaca, NY
Rogg KA, Taylor OR, Gibo DL (1999) Mark and recapture during the monarch migration: a preliminary analysis. Pp. 133-138 in The 1997 North American Conference on the Monarch Butterfly. Hoth J, Merino L, Oberhauser K, Pisantry I, Price S and Wilkinson T (eds). Commission for Environmental Cooperation, Montreal, Canada
Schmidt-Koenig K (1985) Migration strategies of monarch butterflies. Pp. 786-798 in Migration: Mechanisms and Adaptive Significance. Rankin MA (ed). Contributions in Marine Science, Supplement 27, University of Texas, Austin
Schmidt-Koenig K (1993) Orientation of autumn migration in the monarch butterfly. Pp. 275-83 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Scriber JM (1984) Host-plant suitability. Pp. 159-202 in W. J. Bell, and R. T. Carde (eds.), Chemical ecology of insects. Sinauer, Sunderland, MA
Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, Mattila HR, Siegfried BD, Dively GP (2001) Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. Proceedings of the National Academy of Sciences 98: 11937-42
Slansky F Jr., Scriber JM (1985) Food consumption and utilization. Pp. 87-163 in Comprehensive Insect Physiology, Biochemistry, and Pharmacology, vol. 4. Kerkut GA, Gilbert LI (eds). Pergamon, Oxford, UK
Solensky MJ (2003) Reproductive Fitness in Monarch Butterflies, Danaus plexippus. PhD Thesis. University of Minnesota, St. Paul MN
Urquhart FA (1976) Found at last: The monarch’s winter home. National Geographic Magazine 150: 161-73
Urquhart FA, Urquhart NR (1977) Overwintering areas and migratory routes of the monarch butterfly (Danaus p. plexippus, Lepidoptera: Danaidae) in North America, with special reference to the western population. Can. Entomol. 109: 1583-89
Urquhart FA, Urquhart NR (1978) Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Canadian Journal of Zoology 56: 1759-64
Van Hook T (1993) Non-random mating in monarch butterflies overwintering in Mexico. Pp. 49-60 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Vane-Wright RI (1993) The Columbus Hypothesis: An Explanation for the Dramatic 19th Century Range Expansion of the Monarch Butterfly. Pp. 179-186 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
Wassenaar, L. I. and K. A. Hobson. 1998. Natal origins of migratory monarch butterflies at wintering colonies in Mexico: New isotopic evidence. Proceedings of the National Academy of Sciences 95: 15436-39
Wenner AM, Harris AM (1993) Do California monarchs undergo long-distance directed migration? Pp. 275-283 in Biology and Conservation of the Monarch Butterfly. Malcolm SB, Zalucki MP (eds). Natural History Museum of Los Angeles County, California
White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer-Verlag, New York
Wiltschko W, Wiltschko R (1972) Magnetic compass of European robins. Science 176: 62-64
Woodson RE (1954) The North American species of Asclepias L. Annals of the Missouri Botanical Garden 41: 1-211
York H, Oberhauser KS (2002) Effects of duration and timing of heat stress on monarch butterfly (Lepidoptera: Danaidae) development. Journal of the Kansas Entomological Society 75: 290-298
Zalucki MP (1982) Temperature and rate of development in two species of Danaus, D. plexippus and D. chrysippus. J. Aust. Entomol. Soc. 21: 241–46
Zalucki MP, Brower LP (1992) Survival of first instar larvae of Danaus plexippus L. in relation to cardiac glycoside and latex content of Asclepias humistrata. Chemoecology 3: 81–93
Zalucki MP, Kitching RL (1982) Dynamics of oviposition in Danaus plexippus (Insecta: Lepidoptera) on milkweed, Asclepias spp. Journal of Zoology 198: 103-16.
Zalucki MP, Malcolm SB (1999) Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. Journal of Chemical Ecology 25: 1827-42
Zalucki MP, Brower LP, Alfonso AM (2001) Detrimental effects of latex and cardiac glycosides on survival and growth of first instar Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecological Entomology 26: 212–24.
Karen S. Oberhauser (PhD in Ecology, University of Minnesota) is currently an Assistant Professor in the Department of Fisheries, Wildlife and Conservation Biology at the University of Minnesota in St. Paul, Minnesota, USA.
Michelle J. Solensky (PhD in Ecology, Evolution and Behavior, University of Minnesota) is currently a Professor in the Department of Biology at Jamestown College in Jamestown, ND
If you are aware of any important scientific publications about the ecology of the monarch butterfly that were omitted from this review, or have other suggestions for improving it, please contact the authors at the following e-mail addresses:
Dr. Karen Oberhauser: firstname.lastname@example.org
Dr. Michelle J. Solensky: email@example.com
Great Books on Monarch Biology, Conservation and other Issues
Malcolm, S. B., and M. P. Zalucki. 1993. Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County. Amazon Link
Pyle, R. M. 1999. Chasing monarchs. Migrating with the butterflies of passage. Houghton Mifflin. Amazon Link
Halpern, S. 2001. Four wings and a prayer: caught in the mystery of the monarch butterfly. Random House, New York, NY. Amazon Link
Oberhauser, K., and M. Solensky. 2004. The monarch butterfly. Biology and conservation. Cornell University Press, Ithaca, NY. Amazon Link
Schappert, P. 2004. The last monarch butterfly: conserving the monarch butterfly in a brave new world. Firefly Books, Buffalo, NY. Amazon Link