An official website of the United States government
1. Many migratory animals undergo physiological and behavioural changes to prepare for and sustain long‐distance movements. Because insect migrations are common and diverse, studies that examine how migratory insects meet the energetic demands of long‐distance movements are badly needed. 2. Monarch butterflies (Danaus plexippus) migrate up to 4000 km annually from eastern North America to wintering sites in central Mexico. Autumn generation monarchs undergo physiological and behavioural changes in response to environmental cues to initiate migration. In particular, exposure to cooler temperatures and shorter day lengths in early autumn causes monarchs to enter the hormonally induced state of reproductive diapause. 3. This study examined differences in flight‐associated metabolic rate (MR) and flight performance metrics for monarchs experimentally reared under autumn‐like conditions (typically experienced before the southward migration) relative to monarchs reared under summer‐like conditions. 4. Adult monarchs reared under autumn‐like conditions showed lower post‐flight MRs, greater flight efficiency, and lower measures of reproductive activity relative to monarchs reared under summer‐like conditions. Increases in post‐flight metabolism were associated with monarch body weight, age, and flight velocity. 5. These findings suggest that a trans‐generational shift in flight energetics is an important component of the monarch's complex migratory syndrome, and that physiological changes that accompany reproductive diapause facilitate energy conservation during flight.
more »
« less
Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies
Background: North American monarchs (Danaus plexippus) are well-known for their long-distance migrations; however, some monarchs within the migratory range have adopted a resident lifestyle and breed year-round at sites where tropical milkweed (Asclepias curassavica) is planted in the southern coastal United States. An important question is whether exposure to exotic milkweed alters monarch migratory physiology, particularly the ability to enter and remain in the hormonally-induced state of reproductive diapause, whereby adults delay reproductive maturity. Cued by cooler temperatures and shorter photoperiods, diapause is a component of the monarch’s migratory syndrome that includes directional flight behavior, lipid accumulation, and the exceptional longevity of the migratory generation. Methods: Here, we experimentally test how exposure to tropical milkweed during the larval and adult stages influences monarch reproductive status during fall migration. Caterpillars reared under fall-like conditions were fed tropical versus native milkweed diets, and wild adult migrants were placed in outdoor flight cages with tropical milkweed, native milkweed, or no milkweed. Results: We found that monarchs exposed to tropical milkweed as larvae were more likely to be reproductively active (exhibit mating behavior in males and develop mature eggs in females) compared to monarchs exposed to native milkweed. Among wild-caught fall migrants, females exposed to tropical milkweed showed greater egg development than females exposed to native or no milkweed, although a similar response was not observed for males. Conclusions: Our study provides evidence that exposure to tropical milkweed can increase monarch reproductive activity, which could promote continued residency at year-round breeding sites and decrease monarch migratory propensity.
more »
« less
- Award ID(s):
- 1754392
- PAR ID:
- 10185196
- Date Published:
- Journal Name:
- Insects
- Volume:
- 10
- Issue:
- 8
- ISSN:
- 2075-4450
- Page Range / eLocation ID:
- 253
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Each fall, millions of monarch butterflies across the U.S. and Canada migrate up to 4,000 km to overwinter in the same cluster of mountaintops in central Mexico. In spring, these migrants mate and remigrate northwards to repopulate their northern breeding territory over 2-4 partially overlapping generations. Because each migrant monarch completes only part of this round trip and does not return to the overwintering site, this navigational task cannot be learned from the prior generation. The number of monarchs completing the journey has dramatically declined in the past decades, coincident with the decreased availability of their milkweed host plant. The U.S., Mexico, and Canada have invested tremendous resources into monarch conservation efforts, including enacting specific policy initiatives, public outreach programs, and habitat protection and restoration projects. The US invested over $11 million between 2015-2017 alone [1]. Developing a tracking technology for monarch can be a key in these efforts, providing, for instance, detailed understanding of habitat use during migratory flight and dependence on weather conditions. Furthermore, it can significantly benefit animal research, and agricultural and environmental science.more » « less
-
Neonicotinoids are the most widely used insecticides in North America. Numerous studies document the negative effects of neonicotinoids on bees, and it remains crucial to demonstrate if neonicotinoids affect other non-target insects, such as butterflies. Here we examine how two neonicotinoids (imidacloprid and clothianidin) affect the development, survival, and flight of monarch butterflies, and how these chemicals interact with the monarch’s milkweed host plant. We first fed caterpillars field-relevant low doses (0.075 and 0.225 ng/g) of neonicotinoids applied to milkweed leaves (Asclepias incarnata), and found no significant reductions in larval development rate, pre-adult survival, or adult flight performance. We next fed larvae higher neonicotinoid doses (4–70 ng/g) and reared them on milkweed species known to produce low, moderate, or high levels of secondary toxins (cardenolides). Monarchs exposed to the highest dose of clothianidin (51–70 ng/g) experienced pupal deformity, low survival to eclosion, smaller body size, and weaker adult grip strength. This effect was most evident for monarchs reared on the lowest cardenolide milkweed (A. incarnata), whereas monarchs reared on the high-cardenolide A. curassavica showed no significant reductions in any variable measured. Our results indicate that monarchs are tolerant to low doses of neonicotinoid, and that negative impacts of neonicotinoids depend on host plant type. Plant toxins may confer protective effects or leaf physical properties may affect chemical retention. Although neonicotinoid residues are ubiquitous on milkweeds in agricultural and ornamental settings, commonly encountered doses below 50 ng/g are unlikely to cause substantial declines in monarch survival or migratory performance.more » « less
-
Abstract Insect–pathogen dynamics can show seasonal and inter‐annual variations that covary with fluctuations in insect abundance and climate. Long‐term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence.Monarch butterfliesDanaus plexippusare commonly infected with the protozoanOphryocystis elektroscirrha(OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection.Here we compiled data onOEinfection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration.Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid‐2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result ofOE, highlighting the need to consider the parasite as a potential threat to the monarch population.Increases in infection among eastern North American monarchs post‐2002 suggest that changes to the host’s ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.more » « less
-
Abstract Animals derive resources from their diet and allocate them to organismal functions such as growth, maintenance, reproduction, and dispersal. How variation in diet quality can affect resource allocation to life-history traits, in particular those important to locomotion and dispersal, is poorly understood. We hypothesize that, particularly for specialist herbivore insects that are in co-evolutionary arms races with host plants, changes in host plant will impact performance. From their coevolutionary arms-race with plants, to a complex migratory life history, Monarch butterflies are among the most iconic insect species worldwide. Population declines initiated international conservation efforts involving the replanting of a variety of milkweed species. However, this practice was implemented with little regard for how diverse defensive chemistry of milkweeds experienced by monarch larvae may affect adult fitness traits. We report that adult flight muscle investment, flight energetics, and maintenance costs depend on the host plant species of larvae, and correlate with concentration of milkweed-derived cardenolides sequestered by adults. Our findings indicate host plant species can impact monarchs by affecting fuel requirements for flight.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/insects10080253
