How many monarchs in natural populations are infected with O. elektroscirrha?

(Continued)

Abstract  |  Background  |  Methods   |  Results  |  Discussion  |  Acknowledgments  |  References  |  Appendices  |  Sonia's Research Questions

DISCUSSION

Ophryocystis elektroscirrha has a wide geographic distribution, and the prevalence of heavily infected adult D. plexippus is highly variable among populations (ranging from near zero to almost 100%). Within North America, parasites are most prevalent in southern Florida, where over 70% of the monarchs are heavily infected. Approximately 30% of the migratory population in western North America is heavily infected, whereas the eastern migratory population has < 10% heavily infected adults. Estimates of prevalence from older collections indicate that these differences may have persisted for up to 30 years. Although parasite prevalence varied among years within the eastern migratory population, there was no trend of progressive increases or decreases, as might be expected for a recently introduced pathogen or one that was unable to persist in a host population.

These data are consistent with previous measures of adult parasite loads in several monarch populations (Leong et al., 1992, 1997a), and suggest an association between host migratory behavior and parasite prevalence. The eastern migratory population in North America migrates the farthest distance each year and has the lowest prevalence of heavy infection. Monarchs west of the Rocky Mountains migrate considerably shorter distances (Fig. 1), and monarchs in southern Florida breed year-round and do not migrate (Knight, 1997). Another non-migratory monarch population in Hawaii has been shown to bear extremely high parasite loads (up to 100% heavily infected; Brower et al., 1995, Leong et al., 1997a).

Many factors may be responsible for among-population differences in parasite prevalence, including genetic variation in host or parasite lineages (Read et al., 1995), environmental differences in temperature or humidity (Benz, 1987), and the different host migratory distances. Migration may affect parasite prevalence by influencing the mortality of infected hosts or by affecting disease transmission. For example, theoretical models of host-parasite interactions predict declines in parasite prevalence with increasing host mortality (Anderson & May, 1991). Therefore, if infected hosts suffer disproportionate mortality during migration, prevalence should decrease as migratory distances increase. Second, in the absence of host migration, parasites may accumulate in the hosts' environment over time (Shaw, 1994; Roberts et al., 1995), and hosts that undergo periodic migration may escape infection. Finally, migration and overwintering separate monarch reproductive intervals by up to 6 months, and could reduce the transmission of O. elektroscirrha by limiting the number of times that vertical transmission occurs each year.

If the mortality of infected hosts during migration is responsible for low prevalence in the longest-distance migrants, prevalence of heavy infection may increase in the summer generations due to biparental transmission (Altizer & Augustine, 1997), then decline during the autumn migration. In addition, if no parental transmission occurs at the overwintering sites (when hosts are not reproducing), the frequency of high parasite loads should decline during the overwintering period due to the mortality of infected adults. However, no changes in the prevalence of heavily infected adults were detected among periods of breeding, migration, and overwintering in eastern North America (Fig. 5). Because prevalence in this population is so low and breeding monarchs were sampled near the northern limits of their summer range, these results must be regarded with caution. However, observations from eastern and western migratory populations suggest that this disease does not cause increased mortality during the overwintering period alone, as no significant declines in prevalence were detected during overwintering (Fig. 6).

In contrast, parasite prevalence in summer breeding monarchs in western North America declined with increasing distance between breeding and overwintering sites. Samples collected from locations more distant from overwintering sites were associated with lower average parasite loads and prevalence of heavy infection (Fig. 7). This pattern suggests that heavily infected monarchs may fail to reach breeding sites at the most distant extremes of their range. Deviations from this general pattern indicate that other factors influence the distribution of disease among breeding monarchs in western North America. One factor that may become increasingly important is the sale and transfer of live monarchs for special events by breeders in North America. Depending on the rearing practices involved, large numbers of healthy or infected butterflies may be released and artificially decrease or enhance parasite prevalence in local patches (Brower et al., 1995).

Laboratory studies of O. elektroscirrha transmission demonstrate that low parasite loads (classes 1-3) can result from mating or other contact between healthy and infected adults (Altizer 1998). Temporal changes in the frequency of monarchs with low parasite loads indicate that spore transfer between adults also occurs during phases of migration and overwintering, when monarchs cluster in dense aggregations (Fig. 5). At overwintering colonies, the prevalence of adults with low parasite loads increased throughout the overwintering period (Fig. 6). This increase in the prevalence of monarchs with low parasite loads probably results from contact between healthy and heavily infected butterflies during intervals of high host density. Transfer via direct or indirect contact between adults may be important to the persistence of this parasite in the eastern migratory population, where heavily infected adults (and hence vertical transmission) are rare.

Temporal changes in the frequency of heavily infected adults in southern Florida show a decline in prevalence in October and November 1995, compared with high prevalence in other months of that year (Fig. 8). Recent work by Knight (1997) determined that this decline coincides with an influx of eastern autumn migrants into southern Florida. Moreover, most of the uninfected monarchs in the November sample were, as determined by thin layer chromatography, members of the eastern migratory population (A. J. Knight, pers. comm.). Two other samples of monarchs collected during November in Cuba also contained a mix of migrating and locally breeding butterflies (C. Dockx and L. P. Brower, unpublished) and showed prevalence similar to monarchs collected in November in southern Florida. This evidence suggests that uninfected migrating monarchs enter regions of high parasite prevalence in southern Florida and Cuba in the autumn, temporarily decreasing parasite prevalence.

Among Australian monarchs, prevalence of O. elektroscirrha followed a latitudinal gradient along the eastern coast. Monarchs sampled farther north in Rockhampton (Queensland) had lower parasite prevalence than those collected in New South Wales near Sydney (Fig. 9), and monarchs collected near Brisbane showed intermediate prevalence. The distribution of monarchs in Australia is confined largely to eastern regions of Queensland and New South Wales, and their winter range is restricted to eastern coast (Zalucki 1986). Although stable overwintering colonies have been observed in the Sydney Basin for many years (James, 1993), conditions in the Sydney area also support breeding monarch populations throughout the year (James, 1993). However, conditions near Rockhampton (in Queensland, north of Brisbane) become too hot and dry in summer to maintain a continuous breeding population (M. P. Zalucki, pers. comm.). Thus, variation in parasite prevalence observed in Australian monarchs may reflect host breeding ecology and migratory behavior, with prevalence highest in areas where monarchs are present year-round and lower in regions where monarch populations are ephemeral.

To understand the role of parasites in regulating animal populations, or underlying factors that mediate parasite abundance, more investigations of natural populations are required (Dobson & Hudson, 1995; Gulland, 1995). Observations of between-population variation in prevalence show clearly that parasite prevalence and average parasite loads are lower in migratory than in non-migratory monarch populations. Although fine-scale observations within populations do not indicate that differential mortality of infected hosts during overwintering generates this pattern, other processes related to host movement may still affect pathogen abundance. In particular, the observation that the distance from overwintering to breeding areas is correlated negatively with average parasite loads in western North America suggests that spring migration may be important in regulating disease prevalence. In addition, contact leading to spore transfer between adults at overwintering colonies is likely to sustain O. elektroscirrha in the eastern migratory population, where parental transmission is limited by the low frequency of infected adults.

ACKNOWLEDGMENTS

I thank the following individuals for access to previously collected samples of monarch butterflies, or for assistance with collecting and assessing disease prevalence in more recent samples: Alfonso Alonso-M., James Anderson, Peter Andolfatto, Christine Arnott, Lorelle Berkeley, William Calvert, Paul Cherubini, Christina Dockx, Eneida Montesiños-P., Dennis Frey, Bobby Gendron, Elizabeth Goehring, Kari Geurts, Anthony O’Toole, Gard Otis, Imants Pone, Michelle Prysby, Eduardo Rendon-S., Elizabeth Rutkin, Michelle Solensky, Tonya Van Hook, and Myron Zalucki. I thank Don Alstad, Peter Thrall, David Andow, Linda Kinkel, Janis Antonovics and two anonymous reviewers for insightful discussion and comments on the manuscript. This work was supported in part by NSF Grants DEB-9220829 and ESI-9554476 to Karen Oberhauser, by NSF Grants BMS-7514265, DEB-781065, DEB-8119382, BSR-8500416, and OEB-9221091 to L. P. Brower, and by the following awards to Sonia Altizer.: NSF Grant DEB-9700916, two Minnesota Center for Community Genetics Graduate Research Awards, and two James W. Wilkie Awards for research in natural history from the Bell Museum of Natural History at the University of Minnesota.

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APPENDICES

Appendix A. Location and date of monarch collections used to assess disease prevalence among populations. For samples marked with an asterisk, multiple dates and locations have been combined into a single entry. Note that Mexico is included in North American collections.

¹ Represents from one to eight different overwintering areas in Central Mexico (including Sierra Chincua, Cerro Pelon, Palomas, Sierra El Campanario, Sierra Chivati-Huacal, Cerro Altamirano, and Herrada; for locations, see Calvert & Brower, 1986).

² Represents from 1 to 10 different overwintering locations along the California coastline (including Bolinas, Stinson Beach, Moran Lake, Morro Bay, Pismo Beach, Ellwood, Gaviota, Leo Carillo, Cemetario, and Refugio; L.P. Brower & W. Calvert, unpublished).

Appendix B. Samples of eastern North American migratory monarchs collected during breeding, migratory, and overwintering periods. Unless specified, overwintering sites in Central Mexico include Sierra Chincua, Cerro Pelon, Cerro Altamirano, Sierra El Campanario, Sierra Chivati-Huacal, Herrada, and Palomas. Breeding monarchs in Minnesota and Wisconsin were captured within a 250 kilometer radius of St Paul, Minnesota. Migrating monarchs in Texas were captured in Central Texas.

Appendix C. Collection sites, dates, and sample sizes of breeding monarchs captured in western North America in July and August 1997.

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