F. GENERAL BIOLOGY
Like all members of the Lepidoptera (Butterflies and Moths), Monarchs have a life cycle that proceeds through four stages of development: egg, larva (caterpillar), pupa and adult (butterfly). The ratio of males to females in Monarch populations is basically 1:1. Mating between adult butterflies occurs throughout the day, but most matings are observed in late afternoon (2:00 to 6:30 PM) (Opler & Krizek 1984). Female Monarchs lay their fertilized eggs on the leaves of milkweeds, and a single female has the potential to lay as many as 400 eggs (Urquhart 1960). Eggs are laid singly on the leaves of the hostplant, and several eggs are often laid on different leaves of a single plant and on adjacent plants. As a result, although the larvae are not truly colonial, dense aggregations of larvae can occur in large stands of milkweed. For example, in mid-September of 1985, thousands of adults and larva were found in a single buckwheat field that also supported Common Milkweed near Ottawa, Ontario (Hess & Hanks 1986).
In southern Canada, eastern Monarchs produce two to three generations (or broods) each year from June to September. Development from egg to adult butterfly takes about 30 days, although the length of time required for development can be reduced or prolonged by favorable or adverse conditions. In response to factors such as day length, temperature, and the availability and quality of the foodplant, the rate of development may range from about 20 to 45 days.
The success of Monarch breeding from season to season varies greatly from year to year due to climatic conditions, resulting in tremendous swings in the number of Monarchs overwintering in Mexico. This variable reproductive success, in combination with predation and potential weather disasters in Mexico, make the species highly vulnerable.
Monarchs of the eastern and western populations annually migrate south in the fall (to Mexico and California respectively), in order to escape the lethal low temperatures and predictable disappearance of the hostplants in the breeding range during the winter months. The main southward migration begins in Canada in early August and continues through to mid-October, although an extreme southern Ontario single migrants have been recorded as early as July, and ill-fated stragglers have remained as late as December 17. Migrating Monarchs enter a state of reproductive inactivity and avidly seek nectar from flowers to fuel their migration, and to build up a critical fat reserve necessary to sustain the butterflies through the winter (see Gibo and McCurdy 1993). This stored fat is also essential during the northward migration to the Gulf Coast States in the spring, when nectar sources are not available. In order to minimize energy expenditure during migration, Monarchs employ a soaring flight, riding columns of rising warm air in the same way as migrating hawks do, which greatly reduces the need for sustained flapping. They frequently reach high altitudes where strong prevailing winds speed their flight, and glider pilots have observed migrating Monarchs flying over a kilometer above the ground (Gibo 1986).
During the fall migration in southern Ontario, Monarchs cluster together on trees to form overnight roosts in a manner similar to the dense aggregations formed at the overwintering sites. Overnight roosts may contain a few hundred to several thousand individuals, and Monarchs usually form clusters in the same areas year after year. The location of overnight roosts is largely determined by topography, and proximity to abandoned farmlands with abundant nectar resources such as fall Composites (asters and goldenrods). Monarchs migrating south in the fall through southern Ontario build up in numbers along the north shores of Lake Ontario and Lake Erie. Their apparent reluctance to fly over large bodies of water, coupled with the desire to continue moving southwards, probably causes the butterflies to fly southwestward following the shoreline. This inevitably results in large concentrations of Monarchs accumulating on peninsulas jutting out into the lakes, where they have little choice but to eventually proceed southward over open water. Large aggregations and overnight roosts occur at many locations on peninsulas and at other locations along the lakeshores, including Presquile Provincial Park, Long Point, Rondeau Provincial Park and Point Pelee National Park. On September 6, 1993, over 96,000 Monarchs were recorded at Point Pelee, including two overnight roosts of 7,500 and 3,000 individuals (Wormington 1994).
The entire eastern population of the Monarch overwinters annually at about 12 overwintering sites in the Transverse Neovolcanic Belt, a belt of mountain ranges extending across central Mexico. The overwintering sites are all located within a small area of roughly 800 square kilometers, and occur only in Oyamel Fir (Abies religiosa) forest. Oyamel Fir forests are specialized high altitude ecosystems that occur only between elevations of 2,400 to 3,600 meters, and are currently restricted to 13 "islands" of habitat on the highest peaks in Mexico, making up less than one half of 1% of the country's total land area (Brower 1995). It is likely that in the past Monarch overwintering was more widespread in the Oyamel Fir forests; a survey conducted in 1984 found over 60 potential overwintering sites in areas where commercial logging had destroyed much of the original habitat (Brower 1995). The survival of the eastern population of the Monarch is now completely dependent on the preservation and enhancement of the few remaining overwintering areas.
Migrating eastern Monarchs reach the overwintering sites in Mexico in November and late December, where they form dense aggregations made up of tens of millions of individuals, and remain relatively inactive through the winter months. Individual colonies at the overwintering sites occupy less than 0.5 hectares to nearly 3.5 hectares of forest, with a density of approximately 10 million Monarchs per hectare (Calvert & Brower 1986). The overwintering colonies break up in March and early April and the butterflies migrate north to the Gulf Coast of the southeastern United States where the females lay their eggs on milkweeds. One to two generations of Monarchs are produced in the Gulf Coast States in the spring, and it is these offspring of the overwintering generation that continue the northward migration to recolonize the northern breeding range. The continued migration northwards from the southeastern United States in late spring is necessary since southern milkweeds die out in June. Continuing north allows Monarchs to exploit the milkweed resources of central and northeastern North America, enabling the species to produce up to three additional summer generations. These generations are critical to the build up of sufficiently large numbers for survival of the population after losses at the overwintering sites in Mexico. The first returning migrants reach southern Canada near the end of May and in the first week of June. In extreme southern Ontario, at point Pelee, single Monarchs have occasionally been recorded as early as late April, and may represent a minority of individuals that are able to recolonize the breeding range in a single flight from Mexico (see Brower 1995).
Monarchs of the western population undertake a similar migration and overwinter at numerous sites along nearly 1000 kilometers of the California coast, from north of San Francisco to the Mexican border. Over 200 overwintering sites have been recorded in California, and individual colonies may support dozens to tens of thousands of individuals (Lane 1984, 1993). Although colonies in California are much smaller than those in Mexico, even the smallest permanent overwintering sites are believed to be essential to the continued survival of western Monarchs (Malcolm 1993). The vast majority of the overwintering sites are associated with stands of non-native Australian Eucalyptus trees, which were introduced to California in the 1850s (Lane 1993). Eucalyptus were widely planted for landscaping, as windbreaks, and for use as fuel, resulting in a dramatic increase in the amount of suitable Monarch overwintering habitat in California. Monarch colonies in California have dispersed to take advantage of the widespread availability of overwintering habitat following the introduction of Eucalyptus . This dispersal also coincided with the cutting of dense coastal stands of native tree species, such as Monterey Pine (Pinus radiata) and Monterey Cypress (Cupressus macrocarpa), used by overwintering Monarchs prior to the introduction of Eucalyptus, and to a lesser degree in the present day (Lane 1993).
Most overwintering sites in California are not protected, although several are located within state, county or town parks. However, this does not guarantee protection or even recognition of the overwintering sites by those managing the parks. There has been a city ordinance against molestation of overwintering Monarchs in the town of Pacific Grove since 1938. Nevertheless, it affords little protection since it rules only against disturbing the butterflies themselves and does not protect the overwintering habitats, some of which have since been destroyed (Lane 1984). A number of coastal counties have passed ordinances protecting overwintering trees (Malcolm 1993), and in 1988 the California state government allocated two million dollars for acquisition of Monarch overwintering habitat (Snow & Allen 1993).
In Mexico, federal officials have recognized the importance of the overwintering sites, and five forested mountaintops where Monarchs overwinter have been defined as protected natural areas. However, almost all of the land in these protected areas belongs, through land grants that cannot be bought, sold or transferred, to the local residents who live off the land (Snook 1993). Federal agencies in Mexico have to date had little control at a municipal level in protecting the overwintering areas from logging and other forms of disturbance by residents living in these areas. As a result, although legislative protection exists in Mexico, it currently affords little or no protection to the overwintering eastern population. A forest conservation plan, integrating the needs of both the Monarchs and the local populace, has yet to be implemented.
The Monarch is a highly adaptive species, which has been able to withstand dramatic ecological changes in North America resulting from human disturbance in the last 150 years. The clearing of forested lands for agriculture and the creation of roadways, rail lines and other right-of-ways have greatly increased the abundance of Common Milkweed in eastern Canada, and the Monarch has steadily expanded its breeding range to make use of the increasing availability of milkweeds in areas where they were not formerly present. In 1940, Monarch breeding in Ontario was largely confined to the lower Great Lakes region of southern Ontario, south of 44 o latitude. By 1975, following the expansion of Common Milkweed into the forested areas of northern Ontario along roads, highways and powerline corridors, large concentrations of Monarchs were reported along the north shore of Lake Superior from as far north as Thunder Bay, Sault Ste. Marie, and Sudbury (Urquhart & Urquhart 1979). Monarchs are wide-ranging, powerful fliers and are able to seek out and find even the smallest patches of milkweed, including plants growing in city gardens, and along busy roads and highways. They are not limited by human disruption and, as long as the plants are healthy, they will breed readily on milkweeds in area where there is a high level of human activity. Thus, if milkweeds are planted specifically to encourage breeding in urban areas, parks, gardens, and along roadways, the butterflies will undoubtedly find and make use of them.
Weather conditions are the principal factor determining the size and breeding success of the Monarch population (Brower 1995). Cold, wet, overcast conditions in the spring and summer breeding range can prevent adult butterflies from dispersing, mating, laying eggs and nectaring, since they require warm and clear conditions to be active. Adults remain inactive in periods of such weather, and many die without having mated or laid eggs, resulting in fewer and smaller generations of Monarchs. Harsh winters at the overwintering sites in Mexico, with severe winter storms and freezing temperatures, can cause extremely high mortality in the Monarch population. Following winters in which high mortality occurs in Mexico, if the decreased number of Monarchs leaving the overwintering sites in the spring are met with cold, wet weather along the Gulf Coast of the southeastern United States, the number of Monarchs produced in the spring generation and continuing northwards to Canada will be greatly reduced. If the same weather conditions are encountered in the summer breeding range in Canada and the northern United States, the size of the Monarch population will decrease dramatically, producing a greatly diminished fall migration. Dry, hot summers with periods of drought are detrimental to the growth of herbaceous plants, and these conditions will also limit the success of Monarch breeding by reducing the quality and availability of milkweeds for egg laying and larval food, and of nectar sources for adults. Mild winters in Mexico, followed by warm, sunny conditions with moderate amounts of rainfall in the eastern United States and southern Canada provide the best conditions for Monarch breeding success, and produce large fall migrations (Brower 1995).
G. LIMITING FACTORS
Present decline in the eastern population of the Monarch can be attributed to three main factors:
1. Logging and human disturbance at the overwintering sites in Mexico.
The Oyamel Fir forest of Mexico are under rapidly increasing pressure from human disturbance. Legal and illegal commercial logging, harvesting of wood by local inhabitants, livestock grazing, fire, a developing cottage charcoal industry and a number of other human and biological factors are severely threatening the continued existence and integrity of the overwintering sites (see Snook 1993 for detailed discussion). Trees are presently being cut down in the so-called buffer zones around almost all of the core overwintering areas (Brower 1995). This is altering the unique ability of the Oyamel Fir Forest to shelter Monarchs from snow, hail and rainfall, and to insulate them from freezing temperatures (see Calvert & Brower 1981). Current logging practices are creating openings and thinned areas in the forest, which are exposing overwintering Monarchs to winter storms resulting in massive mortalities of millions of butterflies. These openings are also making overwintering Monarchs more vulnerable to predation from birds (Snook 1993). In addition to causing extraordinary mortality in overwintering Monarchs, human disturbance may also be disorienting the butterflies, resulting in unusual clusterings and migratory movements; the butterflies appear to have left the overwintering sites unusually early in the springs of 1994 and 1995 (Brower 1995).
2. Widespread and increasing use of herbicides and insecticides across North America.
Changing agricultural practices and land use patterns in central and eastern North America are resulting in widespread use of herbicides to sustain crops at the expense of all other competing plants, as a method of weed control along roadways, and to specifically eradicate milkweeds. This is contributing to a general decline of breeding habitat and nectar resources essential to the continued survival of the migratory North American Monarch populations. The use of insecticides and biological control agents (e.g.Bacillus thuringiensis or "Bt") to combat lepidopterous pests such as the Gypsy Moth (Lymantria dispar) has also had a negative effect on Monarchs and other non-target species.
3. Predation at the overwintering sites.
Two species of birds, the Black-headed Grosbeak (Pheucticus melanocephalus) and the Black-backed Oriole (Icterus galbula abeillei), feed extensively on Monarchs roosting at the Mexican overwintering sites. Both birds are able to circumvent the toxic properties of the Monarch (see section H), and predation is estimated to occur at a rate of up to 34,000 butterflies killed per day (Snook 1993). At one overwintering colony comprising approximately 20 million Monarchs, nearly 10% (2 million), were killed by bird predation over the winter (Arellano G. et al. 1993). In smaller colonies, mortality due to bird predation may reach as high as 44%, since the birds feed on the perimeter of a colony, and smaller colonies have a proportionally greater surface area, exposing more butterflies to attack (Calvert et al. 1979). The Black-eared Mouse (Peronmyscus melanotis) also feeds extensively on both live and dead Monarchs (Glendinning 1993).
Heavy predation at the overwintering sites may be a fairly recent phenomenon (Fink & Brower 1981); a large proportion of the Monarchs in the eastern population have low levels of toxicity which enable the birds and mice to feed on them (Brower 1995). This reduced toxicity is also a characteristic of Common Milkweed (Brower 1995), which has increased in abundance in the last 150 years due to changing agricultural and land use patterns, and has become the primary hostplant of the eastern population in that time. Heavy predation becomes of increasing concern as Monarch numbers decline due to other factors.
Three factors threaten the continued survival of the western population of the Monarch:
1. Real Estate of development along the California coast.
Almost all of the overwintering sites in California, except for a small number that lie within state, county, and town parks, are threatened by real estate development (Brower 1995). Twenty-one overwintering sites in California have been destroyed, and an additional 7 have been badly damaged, as a result of the building or expansion of motels, hotels, resort complexes, new houses, roads, and even to clear picturesque ocean views desired by wealthy landowners (Malcolm 1993).
2. Active programs to eliminate introduced Eucalyptus trees.
State and federal officials responsible for public lands management favor the eradication of exotic vegetation in California (which would include introduced Australian Eucalyptus trees presently harboring the majority of overwintering colonies of western Monarchs), in order to return the landscape to its original condition and native vegetation (Lane 1993). While only a minority of coastal overwintering sites are on public lands, the possibility of the eradication of Eucalyptus places these sites in jeopardy. In some state parks, Eucalyptus are currently being eradicated, despite the fact that the possibility of eliminating these trees in California is remote (Malcolm 1993).
The impact and significance of a recently discovered protozoan disease has yet to be determined. This protozoan may be a significant factor in the extreme fluctuations in numbers of populations at the California overwintering sites, but such fluctuations have long been recorded and the disease may not be a new threat to Monarch survival (John Lane personal communication).