Migratory animals undergo seasonal and often spectacular movements and perform crucial ecosystem services. In response to environmental changes such as habitat loss and climate change, some migratory species have responded by migrating shorter distances or arriving earlier to their spring breeding grounds each year. In cases where humans provide year-round resources, some animals have stopped migrating altogether, instead adopting a resident lifestyle and remaining in the same locations year-round. How these resident populations form and persist, and whether they continue to interact with remaining migratory populations is largely unknown. Importantly, resident populations often experience greater infection pressures by parasites and pathogens than migrants. Given that many migratory taxa face ongoing declines, scientists need to understand whether resident populations positively or negatively impact remaining migratory populations, including through their effects on disease.

This project examined how shifts from migratory to resident behavior, as caused by human-associated environmental change, affect animal-parasite interactions. Research focused on an iconic migratory insect, the monarch butterfly, and its debilitating specialist protozoan parasite. Coincident with declines in the numbers of migratory monarchs in North America in recent decades, year-round resident monarch populations have proliferated in the southeastern U.S., in response to human planting of non-native tropical milkweed. In warmer regions that don’t experience hard freezes, tropical milkweed provides a year-round resource to support monarch reproduction at times of year when the migratory population historically overwinters in Mexico in a non-reproductive state. Using field data, volunteer-based reports, laboratory experiments, and mathematical models, researchers supported by this project asked: (1) How and why do resident populations form and persist; (2) How does parasite transmission differ between migratory and resident populations, and (3) How do interactions between migrants and residents influence their population numbers and parasite transmission? 

Results from this project showed that exposure to tropical milkweed disrupts the monarchs’ fall migration and fosters the formation and persistence of resident behavior. Specifically, monarch caterpillars raised on non-native tropical milkweed had a lower probability of entering their pre-migratory state in the fall. Moreover, adult butterflies that were already migrating in the fall were more likely to drop out of the migration when exposed to tropical milkweed. Field and modeling work showed that the parasite can increase quickly to infect the majority of butterflies in resident populations owing to its three-pronged transmission strategy (parent-to-offspring, environmental, and adult-to-adult transmission). Community science data and field observations showed that parasite infection prevalence reaches high levels in the extreme southern U.S. at sites where tropical milkweed has been planted, and that migrants and residents interact (mix together) at these sites during the spring and fall migration. The high infection prevalence observed in resident monarchs is not due to warmer temperatures in the southern U.S. In fact, laboratory experiments showed that the protozoan parasite does not replicate or survive well when exposed to sustained high heat. Importantly, analysis of multi-decadal trends in parasite infection prevalence across North American monarchs showed that the parasite has more than tripled in baseline prevalence in recent years (now at ~15%) relative to pre-2002 levels (2-5%), likely owing to sustained parasite transmission in resident monarchs and spillover infections from residents to migrants. Thus, the parasite now could cause the deaths of tens of millions of monarchs each year during their annual migration, and could be an emerging threat to the long-term health and persistence of migratory monarchs.

Intellectual Merit:

Results of this project contributed to the fields of host-parasite ecology and partial migration, by examining the population-wide conservation implications of habitat sharing and parasite transmission between residents and migrants. Research findings showed how the break-down of animal migrations in response to human activity increases infection risks for remaining migrants. Given that many animal migrations are affected by human activities, project findings here are broadly relevant to wildlife conservation and public health. Over the length of this project, research products included 3 book chapters, 20 journal articles, 20 research presentations at conferences and universities, support for 4 graduate theses and 1 publicly accessible website.

Broader Impacts:

The conservation status of monarchs will continue to be reviewed periodically by the U.S. Endangered Species Act. Findings of this study contribute to the base of scientific knowledge needed to inform conservation strategies ensuring persistence of monarch migration, including recommendations against the planting of exotic milkweeds that might reduce migratory behavior. This project supported public engagement in science through support for two ongoing community science projects (Project Monarch Health, and the Monarch Larva Monitoring Project). Volunteers who participated in these programs interacted with researchers studying human impacts on ecological systems. The PIs collectively mentored and trained 3 research professionals, 14 undergraduates and 9 graduate students during the course of this project, providing them with opportunities to learn how interdisciplinary science works and to conduct original research.

Last Modified: 10/22/2024
Modified by: Sonia M Altizer