Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts

Abstract

Monarch butterflies (Danaus plexippus) are parasitized by the protozoan Ophryocystis elektroscirrha throughout their geographical range. Monarchs inhabiting seasonally fluctuating environments migrate annually, and parasite prevalence is lower among migratory relative to non-migratory populations. One explanation for this pattern is that long-distance migration weeds out infected animals, thus reducing parasite prevalence and transmission between generations. In this study we experimentally infected monarchs from a migratory population and recorded their long-distance flight performance using a tethered flight mill. Results showed that parasitized butterflies exhibited shorter flight distances, slower flight speeds, and lost proportionately more body mass per km flown. Differences between parasitized and unparasitized monarchs were generally not explained by individual variation in wing size, shape, or wing loading, suggesting that poorer flight performance among parasitized hosts was not directly caused by morphological constraints. Effects of parasite infection on powered flight support a role for long-distance migration in dramatically reducing parasite prevalence in this and other host-pathogen systems.

Parasitic infection reduces dispersal of ciliate host

“…In several species, infection impairs host locomotion ability (e.g. [2]), presumably because of exploitation of host resources. This is also conceivable here, given the deleterious effects of infection by Holospora sp.…”

“…Typically, infection may be expected to weaken the host and thereby reduce its locomotion ability, such as running speed or, flight velocity (e.g. [2,3]). Alternatively, infected hosts may become more active or have increased locomotion [4].…”

Ecophysiology of avian migration in the face of current global hazards

“…Similarly, our understanding of the impact of infection on movement behaviour is relatively limited. In migratory monarch butterflies, protozoan infections have been shown to reduce flight speed and endurance [55]. Similarly, although the majority of ducks infected with low-pathogenic avian influenza viruses under laboratory conditions show no clinical signs of infection, naturally infected Bewick's swans (Cygnus columbianus bewickii) under field conditions, where birds have to acquire food, avoid predation and thermoregulate, show significant reductions in their pre-migratory fuelling rate and movement behaviours [56].…”

Monarch butterfly migration and parasite transmission in eastern North America

“…Migration is often energetically demanding or stressful (Alerstam et al 2003) and could 4 E-mail: bbartel@uga.edu increase susceptibility to parasites through immunosuppression (e.g., Garamszegi andMøller 2007, Weber andStilianakis 2007). Moreover, parasite infections can reduce dispersal ability through reducing flight speed or endurance, as has been shown in monarch butterflies (Bradley and Altizer 2005) and waterfowl (van Gils et al 2007). Thus, the combined demands of migration and negative effects of parasites could remove infected animals from the population, reducing parasite prevalence.…”

“…Second, heavily infected animals could be removed from the population (''migratory culling'' sensu Bradley and Altizer 2005). Migration is often energetically demanding or stressful (Alerstam et al 2003) and could 4 E-mail: bbartel@uga.edu increase susceptibility to parasites through immunosuppression (e.g., Garamszegi andMøller 2007, Weber andStilianakis 2007).…”