Monarch butterfly migration and parasite transmission in eastern North America

Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies (Danaus plexippus) and a protozoan parasite (Ophryocystis elektroscirrha) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long‐distance migration weeds out infected animals (i.e., migratory culling). We combined field‐sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within‐breeding‐season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.

[1]  G. Hess.  Disease in Metapopulation Models: Implications for Conservation , 1996 .

[2]  L. Brower,et al.  Spring recolonization of eastern North America by the monarch butterfly: successive brood or single sweep migration? , 1993 .

[3]  P. Thrall,et al.  The spatial distribution of plant populations, disease dynamics and evolution of resistance , 2002 .

[4]  M. Zalucki,et al.  Biology and conservation of the monarch butterfly , 1997 .

[5]  A. Peterson,et al.  Modeling current and future potential wintering distributions of eastern North American monarch butterflies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  A. Dobson.  What Links Bats to Emerging Infectious Diseases? , 2005, Science.

[7]  L. Frazer,et al.  Epizootics of wild fish induced by farm fish , 2006, Proceedings of the National Academy of Sciences.

[8]  Lincoln P. Brower,et al.  Catastrophic Winter Storm Mortality of Monarch Butterflies in Mexico during January 2002 , 2007 .

[9]  Craig Loehle,et al.  Social barriers to pathogen transmission in wild animal populations , 1995 .

[10]  Karen S. Oberhauser,et al.  Citizen Science: Creating a Research Army for Conservation , 2008 .

[11]  S. Altizer,et al.  Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite , 2008, Proceedings of the National Academy of Sciences.

[12]  Lise Wilkinson.  Disease transmission by insects: its discovery and 90 years of effort to prevent it , 1994, Medical History.

[13]  S. Altizer,et al.  Transmission of the Protozoan Parasite Ophryocystis elektroscirrha in Monarch Butterfly Populations : Implications for Prevalence and Population-Level Impacts , 2007 .

[14]  A. Nilssen,et al.  Epizootiology of the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera: Oestridae), in reindeer, Rangifer tarandus (L.), in Norway , 1995 .

[15]  J. Gog,et al.  Disease in endangered metapopulations: the importance of alternative hosts , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[16]  E. Howard,et al.  Spring recolonization rate of monarch butterflies in eastern North America: New estimates from citizen-science data , 2005 .

[17]  E. Howard,et al.  Citizen Science Observations of Monarch Butterfly Overwintering in the Southern United States , 2010 .

[18]  S. Altizer,et al.  Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts , 2005 .

[19]  Michael L. Johnson,et al.  Evolution of Dispersal: Theoretical Models and Empirical Tests Using Birds and Mammals , 1990 .

[20]  Mark John Costello.  Ecology of sea lice parasitic on farmed and wild fish. , 2006, Trends in parasitology.

[21]  G. Merriam,et al.  The elements of connectivity where corridor quality is variable , 1990, Landscape Ecology.

[22]  H. Kaya,et al.  Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies , 1997 .

[23]  S. Åkesson,et al.  Long-distance migration: evolution and determinants , 2003 .

[24]  A Townsend Peterson,et al.  Ecological Niches in Sequential Generations of Eastern North American Monarch Butterflies (Lepidoptera: Danaidae): The Ecology of Migration and Likely Climate Change Implications , 2007, Environmental entomology.

[25]  Jonathan H. Epstein,et al.  Bats Are Natural Reservoirs of SARS-Like Coronaviruses , 2005, Science.

[26]  H. Dingle.  Migration: The Biology of Life on the Move , 1996 .

[27]  S. Altizer,et al.  Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies , 2000 .

[28]  M. Zalucki.  TEMPERATURE AND RATE OF DEVELOPMENT IN DANAUS PLEXIPPUS L. AND D. CHRYSIPPUS L. (LEPIDOPTERA:NYMPHALIDAE) , 1982 .

[29]  M. Zalucki.  Sex around the milkweed patch - the significance of patches of host plants in monarch reproduction , 1993 .

[30]  S. Altizer,et al.  Virulence determinants in a natural butterfly-parasite system , 2006, Parasitology.

[31]  J. Myers,et al.  Ophryocystis elektroscirrha sp. n., a Neogregarine Pathogen of the Monarch Butterfly Danaus plexippus (L.) and the Florida Queen Butterfly D. gilippus berenice Cramer1 , 1970 .

[32]  I. Folstad,et al.  Parasite avoidance: the cause of post-calving migrations in Rangifer? , 1991 .

[33]  S. Altizer,et al.  Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction , 2009 .

[34]  Karen S. Oberhauser,et al.  Temporal and geographical variation in monarch densities: Citizen scientists document monarch population patterns , 2004 .

[35]  A. Møller,et al.  Prevalence of avian influenza and host ecology , 2007, Proceedings of the Royal Society B: Biological Sciences.

[36]  A. Simmons,et al.  Dispersal and Seasonal Occurrence of Noctuidonema guyanense, an Ectoparasitic Nematode of Adult Fall Armyworm (Lepidoptera: Noctuidae), in the United States2 , 1991 .

[37]  J. V. van Gils,et al.  Hampered Foraging and Migratory Performance in Swans Infected with Low-Pathogenic Avian Influenza A Virus , 2007, PloS one.

[38]  P. Daszak,et al.  Predicting the global spread of H5N1 avian influenza , 2006, Proceedings of the National Academy of Sciences.

[39]  F. A. Urquhart,et al.  Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico , 1978 .

[40]  S. Altizer,et al.  Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus) , 2009, Oecologia.

[41]  E. Howard,et al.  The fall migration flyways of monarch butterflies in eastern North America revealed by citizen scientists , 2009, Journal of Insect Conservation.

[42]  L. Brower,et al.  Spring migration of monarch butterflies in California , 1993 .

[43]  Martin Wikelski,et al.  How and Why Do Insects Migrate? , 2006, Science.

[44]  Benjamin M. Bolker,et al.  Mechanisms of disease‐induced extinction , 2004 .

[45]  Karen S. Oberhauser,et al.  The Monarch Butterfly: Biology and Conservation , 2004 .

[46]  M. Lewis,et al.  Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations , 2007, Proceedings of the Royal Society B: Biological Sciences.

[47]  Lincoln P. Brower,et al.  Animal Migrations: Endangered Phenomena , 1991 .

[48]  S. Bergström,et al.  Epidemiology: Reactivation of Borrelia infection in birds , 2000, Nature.

[49]  R. Vane‐Wright,et al.  Milkweed Butterflies: Their Cladistics and Biology , 1984 .

[50]  S. Riley.  Large-Scale Spatial-Transmission Models of Infectious Disease , 2007, Science.

[51]  S. Altizer,et al.  Transmission of the protozoan parasite Ophyocystis elektroscirrha in monarch butterfly populations: implications for prevalence and population-level impacts: Biology and Conservation , 2004 .

[52]  Journal of Protozoology , 1953, Nature.

[53]  Martin Wikelski,et al.  Going, Going, Gone: Is Animal Migration Disappearing , 2008, PLoS biology.

[54]  H. Kaya,et al.  Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. , 1997, Journal of invertebrate pathology.

[55]  Nikolaos I. Stilianakis,et al.  Ecologic Immunology of Avian Influenza (H5N1) in Migratory Birds , 2007, Emerging infectious diseases.

[56]  M. Lewis,et al.  Transmission dynamics of parasitic sea lice from farm to wild salmon , 2005, Proceedings of the Royal Society B: Biological Sciences.