Mortality of Wintering Monarch Butterflies: Are Emerging Pathogens the Cause of Declining Populations?
American Association of Zoo Veterinarians Conference 2004

A. Alonso Aguirre1, DVM, MSc, PhD; Ana Lilia Sandoval2, MS; David Ramirez2, BS; Gabriela Jimenez2, BS; David Soriano2, BS; Servando Rodriguez2, BS; Rocio Mondragon2, BS; Marco Bernal3, BS; Eduardo Rendon3, MS; Hector Zepeda2, PhD

1Wildlife Trust, Columbia University, Palisades, NY, USA; 2Laboratorio de Microbiologia Veterinaria, Instituto Politecnico Nacional, Carpio y Plan de Ayala, Col. Casco de Santo Tomas, Mexico; 3Reserva de la Biosfera Mariposa Monarca, Cerrada de Santos Degollado Oriente No. 4, Col. Heroes Ferrocarrileros, Zitacuaro, Michoacan, Mexico

Abstract

The health of ecosystems is directly related to the health of species, in which the presence of disease in individuals and populations can reflect ecosystem health. Habitat fragmentation and destruction have led to ecosystem disruptions, including altered patterns of disease transmission and emerging infectious diseases (EID), the accumulation of toxic pollutants, and the invasion of alien species and pathogens. Using the criteria that define EIDs of humans, EIDs have been identified affecting domestic animals, crops, insects, wildlife and wild plants.1 Knowledge of butterfly diseases is rudimentary; however, there are many agents, including baculoviruses and nuclear polyhedrosis viruses, bacteria, and fungi that may cause disease in butterflies.

The monarch butterfly (Danaus plexippus) is one of the best known North American butterflies, because of its annual migration. Unable to withstand freezing weather in the northern range, in autumn tens of millions fly south, roosting in huge numbers in oyamel fir (Abies religiosa) forest fragments in Mexico. In winter 2003–2004 approximately 10 million butterflies per ha were concentrated on a hibernation range of 11 ha. Monarch butterflies use the same trees year after year, and their journey can cover thousands of miles. Since the larval food plants do not grow in their overwintering sites, the spring generation flies back north to regions where milkweeds of the family Asclepiadaceae are plentiful. Monarch butterflies spend the summer in either the New England-Great Lakes area or the canyons of the eastern Rocky Mountains. It was not until 1976 that the overwintering grounds were discovered. The Great Lakes population spends the months of November–March in the Sierra Madre mountains of central Mexico.3,5

Mortality of monarch butterflies on the wintering grounds may be due to effects of global climate change, deforestation, starvation, desiccation, freezing, and predation by wild birds, the scansorial black eared mouse (Peromyscus melanotis), ladybugs, and ants. Mortality due to predation by wild birds may reach 9–15%. Overwintering monarch butterflies tolerate only a narrow range of temperature and wetness; a combination of freezing temperatures and rain can be lethal. Following a snowstorm in winter 1995–1996, mortality reached 7%, while in January 2002 over 80% of the monarch population was killed.3 Recent studies indicate that infection with the protozoan parasite Ophryocystis elektroscirrha may be related to low survival of infected larval and adult butterflies, induced by the sporozoite, which potentially causes severe damage to the gut, and mortality.2,4

During 2004, we sampled four sites in the Monarch Butterfly Biosphere Reserve, including Las Palomas, El Rosario, Llano de Toro (Sierra Chincua) and Coala (Sierra Chincua). We collected 10 live and 10 moribund or recently dead butterflies from each site for bacteriology, mycology, virology and toxicology. In addition, using pieces of Scotch tape, we collected samples of abdominal scales from 500 live butterflies per site, which then were released unharmed. Bacteriologic analysis focused on anaerobic, aerobic and environmental microorganisms. Several culture media were inoculated for fungal growth and characterization, and three cell lines (Vero, HeLa and HEp-2) were inoculated for virus isolation and identification.

Oocysts of O. elektroscirrha were documented at all sites during two sampling episodes. In January/February 2004, oocyst prevalence was: Palomas - 2.2/1.8%, El Rosario - 7.0/5.0%, Llano de Toro - 3.0/1.4%, Coala - 3.4/2.0%. Bacterial and fungal isolations were similar at all sites, Corynebacterium spp., Bacillus spp., zygomycetes and slow-growth fungi predominating. We currently are attempting to characterize a fungus similar to that found in the abdominal scales of live butterflies. A virus that causes cytopathic effects in Vero cells and plaques on the chorioallantoic membranes of chicken embryos also was isolated. Strong synergism between infection with O. elektroscirrha and a fungus that penetrates wing scales may contribute to severe mortality, perhaps abetted by other potential pathogens, including the virus isolated.

The Mexican government is reviewing the decree that originally protected the overwintering sanctuaries in 1986, and is getting input from many people with scientific knowledge of the locations of overwintering sites and the needs of monarch butterflies. The primary conservation issue is the high rate of oyamel fir deforestation. Supporting programs providing alternative sources of income for landowners are required to secure the long-term survival of this charismatic butterfly species.

Literature Cited

1.  Aguirre AA, RS Ostfeld, GM Tabor, CA House, MC Pearl, eds. 2002. Conservation Medicine: Ecological Health in Practice. Oxford University Press, New York.

2.  Altizer SL, KS Oberhauser. 1999. Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). J. Invert. Pathol. 74: 76–88.

3.  Brower L, G Castilleja, A Peralta, J Lopez-Garcia, L Bojorquez-Tapia, S Diaz, D Melgarejo, M Missrie. 2002. Quantitative changes in forest quality in a principal overwintering area of the monarch butterfly in Mexico 1971–1999. Cons. Biol. 16: 346–59.

4.  Harvell CD, CE Mitchell, JR Ward, S Altizer, AP Dobson, RS Ostfeld, MD Samuel. 2003. Climate warming and disease risks for terrestrial and marine biota. Science. 296: 2158–62.

5.  Urquhart FA. 1987. The Monarch Butterfly: International Traveler. University of Toronto Press. Toronto, Canada.

 

Speaker Information
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A. Alonso Aguirre, DVM, MSc, PhD
Wildlife Trust
Columbia University
Palisades, NY, USA


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