Migratory monarchs wintering in California experience low infection risk compared to monarchs breeding year-round on non-native milkweed

Abstract

Long-distance migration can lower infection risk for animal populations by removing infected individuals during strenuous journeys, spatially separating susceptible age classes, or allowing migrants to periodically escape from contaminated habitats. Many seasonal migrations are changing due to human activities including climate change and habitat alteration. Moreover, for some migratory populations, sedentary behaviors are becoming more common as migrants abandon or shorten their journeys in response to supplemental feeding or warming temperatures. Exploring the consequences of reduced movement for host-parasite interactions is needed to predict future responses of animal pathogens to anthropogenic change. Monarch butterflies (Danaus plexippus) and their specialist protozoan parasite Ophryocystis elektroscirrha (OE) provide a model system for examining how long-distance migration affects infectious disease processes in a rapidly changing world. Annual monarch migration from eastern North America to Mexico is known to reduce protozoan infection prevalence, and more recent work suggests that monarchs that forego migration to breed year-round on non-native milkweeds in the southeastern and south central Unites States face extremely high risk of infection. Here, we examined the prevalence of OE infection from 2013 to 2016 in western North America, and compared monarchs exhibiting migratory behavior (overwintering annually along the California coast) with those that exhibit year-round breeding. Data from field collections and a joint citizen science program of Monarch Health and Monarch Alert showed that infection frequency was over nine times higher for monarchs sampled in gardens with year-round milkweed as compared to migratory monarchs sampled at overwintering sites. Results here underscore the importance of animal migrations for lowering infection risk and motivate future studies of pathogen transmission in migratory species affected by environmental change.

Responses of migratory species and their pathogens to supplemental feeding

“…In some locations, infection prevalence reached 100%, and volunteer reports showed that monarch winter-breeding occurs exclusively at sites with tropical milkweed. A strikingly similar pattern was observed in the western USA: Resident monarchs breeding year-round in southern California face nine-times higher infection risk compared with migratory monarchs at coastal overwintering sites [46]. High infection prevalence has been attributed to the loss of both migratory escape and culling.…”

“…One of the most popular milkweed in gardens is a non-native species, tropical milkweed (A. curassavica; figure 3), which is attractive, easy to grow and commonly sold in nurseries [47,154]. Unlike most native milkweeds that enter dormancy in the autumn, tropical milkweed persists throughout the year in mild climates [23,46,47]. Tropical milkweed also has high concentrations of secondary compounds called cardenolides that are attractive to monarchs, provide a defence against many predators, and prolong lifespan for infected individuals [155][156][157].…”

Regional climate on the breeding grounds predicts variation in the natal origin of monarch butterflies overwintering in Mexico over 38 years

“…At the same time, monarchs may breed throughout the winter on introduced host plants now grown year-round near the Gulf of Mexico (Satterfield et al, 2015). Year-round breeding has been hypothesized to lead to an increase of parasites (Satterfield et al, 2016), shed as spores by adults on food plants, which are subsequently ingested by larvae causing infection. Heavily infected monarchs are less likely to survive during fall migration (Bartel et al, 2011), which suggests butterflies born in the southwest and southeast regions suffer higher mortality during the migration to Mexico in years with higher regional parasite levels (Satterfield et al, 2015).…”

Patterns of parasitism in monarch butterflies during the breeding season in eastern North America

“…The finding that infection prevalence increases in monarch butterflies over the breeding season (in this study and in Bartel et al ., ) and is highest in year‐round breeding monarchs (Altizer et al ., ; Satterfield et al ., ) suggests consequences for monarch host–parasite dynamics under global environmental change. Anthropogenic habitat changes due to the planting of non‐native milkweed plants in Texas and along the Gulf Coast may result in a longer breeding season and high infection prevalence among monarchs at these sites (Satterfield et al ., ).…”