Parasite dynamics in North American monarchs predicted by host density and seasonal migratory culling

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 butterflies Danaus plexippus are commonly infected with the protozoan Ophryocystis 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 on OE infection 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 of OE, 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.

Opposing global change drivers counterbalance trends in breeding North American monarch butterflies

“…Contrasting evidence of no change in the number of tagged monarchs returning to Mexico in the fall suggested otherwise (Taylor et al, 2020), but that finding remains contested due to difficulties in accounting for changing tagging effort through time (Fordyce et al, 2020). In support of our assessment, a recent study of the monarch parasite, Ophryocystis elektroscirrha , has shown that nation‐wide prevalence has increased in the last 15 years, and that this increase is leading to considerable migratory losses and corresponding reductions in winter colony sizes (Majewska et al, 2021). Therefore, conservation attention along the migration routes, and/or actions that reduce parasite transmission, may be more imperative for the monarch's long‐term survival compared to efforts directed at the breeding grounds.…”

Extreme heat reduces host and parasite performance in a butterfly–parasite interaction

“…Our study suggests that nighttime warming and heatwaves that exceed the thermal limits of OE could shift the location of transmission hotspots and the seasonal timing of infection. OE prevalence has increased threefold over the past two decades [ 80 ], in part owing to warmer winters supporting resident monarch populations along the Gulf Coast, which typically have high prevalence owing to year-round breeding [ 79 ]. However, recent record-breaking high temperatures indicate that continued warming in the southeast USA could lead to reductions in summer infection prevalence through decreased host and parasite survival, as well as through indirect temperature effects like reduced availability and increased toxicity of milkweeds [ 81 , 82 ].…”

Dramatic Recent Declines in the Size of Monarch Butterfly (Danaus plexippus) Roosts During Fall Migration

“…First, prevalence of the monarch parasite Ophryocystis elektroscirrha ("OE") has increased ca. 10-fold in North America since the early 2000s (26). Parasite infection reduces monarch wing strength and flight capacity, contributing to migratory dropout (27,28).…”