Advertisement

Journal of Insect Conservation

, Volume 18, Issue 5, pp 847–853 | Cite as

Monarch–parasite interactions in managed and roadside prairies

  • Elisha K. Mueller
  • Kristen A. Baum
ORIGINAL PAPER

Abstract

Roadsides cover an extensive area within the United States, are actively managed, and have been considered potential areas of habitat for several taxa. For monarch butterflies (Danaus plexippus), roadsides may act as important habitat along their migration route by providing nectar and host plant resources, which is especially important considering the loss and fragmentation of monarch habitat throughout their breeding range. However, the interactions between monarchs and their parasites may be altered in these areas by management regimes. Monarchs are infected by Ophryocystis elektroscirrha (OE), an obligate, spore-forming protist of monarchs and queens, and Lespesia archippivora, a generalist tachinid fly parasitoid. Roadsides could increase parasitism by concentrating monarchs in certain areas or decrease parasitism by modifying habitat (e.g., the roadside management practice of mowing could reduce the availability of OE spores by removing the above ground portion of host plants and generating re-growth), including the distribution and abundance of host plants. In this study, we compared the proportion of infected monarchs between roadside prairies and managed prairies to evaluate the potential of roadside prairies as habitat for monarch butterflies. Our results suggest that the proportion of infected monarchs does not differ between roadside prairies and managed prairies. Thus, roadsides may provide habitat for monarchs that is similar in quality (at least in terms of parasitism rates) to managed prairies. The role of roadsides as habitat for monarchs should be considered when developing roadside management strategies.

Keywords

Danaus plexippus Land use Lespesia archippivora Migratory culling Migratory escape Ophryocystis elektroscirrha 

Notes

Acknowledgments

This research was funded by grants from the Payne County Audubon Society to E. K. Mueller (Helen Miller Award: 2011 and 2012) and the Waters Grant-in-Aid of Research (2012) to E. K. Mueller. We thank the Oklahoma Turnpike Authority and the Oklahoma Department of Transportation for access to roadside sites and information about mowing regimes. We thank S. Andreoli, G. Ingalls, S. McCoshum, K. Monroe, M. Parrish, M. Thompson, J. Tidwell, E. Villert, T. Wade, and G. R. Williams for assistance in the field. We also thank D. Engle, J. Steets, and an anonymous reviewer for comments on an earlier draft of this manuscript.

References

  1. Allworth D (1998) Roadside conservation issues on the Darling Downs. The Growing Idea. Greening Australia, BrisbaneGoogle Scholar
  2. Alonso-Mejía A, Rendon-Salinas E, Montesinos-Patino E, Brower LP (1997) Use of lipid reserves by monarch butterflies overwintering in Mexico: implications for conservation. Ecol Appl 7:934–947CrossRefGoogle Scholar
  3. Altizer SM (2001) Migratory behaviour and host-parasite co-evolution in natural populations of monarch butterflies infected with a protozoan parasite. Evol Ecol Res 3:611–632Google Scholar
  4. Altizer SM, Oberhauser KS (1999) Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). J Invertebr Pathol 74:76–88PubMedCrossRefGoogle Scholar
  5. Altizer SM, Oberhauser KS, Brower LP (2000) Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecol Entomol 25:125–139CrossRefGoogle Scholar
  6. Altizer SM, Oberhauser KS, Geurts KA (2004) Transmission of the protozoan parasite Ophyrocystis elektroscirrha in monarch butterfly populations: implications for prevalence and population-level impacts. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 203–218Google Scholar
  7. Bartel RA, Oberhauser KS, De Roode JC, Altizer SM (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92:342–351PubMedCrossRefGoogle Scholar
  8. Baum KA, Mueller EK (2014) Grassland and roadside management practices affect milkweed abundance and opportunities for monarch recruitment. In: Oberhauser KS, Altizer SM, Nail K (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell University Press, IthacaGoogle Scholar
  9. Baum KA, Sharber WV (2012) Fire creates host plant patches for monarch butterflies. Biol Lett 8:968–971PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bradley CA, Altizer S (2005) Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecol Lett 8:290–300CrossRefGoogle Scholar
  11. Brower LP, Fink LS, Walford P (2006) Fueling the fall migration of the monarch butterfly. Integr Comp Biol 46:1123–1142PubMedCrossRefGoogle Scholar
  12. Carlsson-Graner U, Thrall PH (2002) The spatial distribution of plant populations, disease dynamics and evolution of resistance. Oikos 97:97–110CrossRefGoogle Scholar
  13. Cockrell BJ, Malcolm SB, Brower LP (1993) Time, temperature, and latitudinal constraints on the annual recolonization of eastern North America by the monarch butterfly. In: Malcolm SB, Zalucki MP (eds) Biology and Conservation of the Monarch Butterfly. Natural History Museum of Los Angeles County, Los AngelesCalifornia, pp 233–251Google Scholar
  14. Dankel DJ, Skagen DW, Ulltang O (2008) Fisheries management in practice: review of 13 commercially important fish stocks. Rev Fish Biol Fisher 18:201–233CrossRefGoogle Scholar
  15. De Roode JC, Gold LR, Altizer S (2007) Virulence determinants in a natural butterfly-parasite system. Parasitol 134:657–668CrossRefGoogle Scholar
  16. Etchegaray JB, Nishida T (1975) Reproductive activity, seasonal abundance and parasitism of monarch butterfly, Danaus plexippus (Lepidoptera, Danaidae) in Hawaii. P Hawaii Entomol Soc 22:33–39Google Scholar
  17. Folstad I, Nilssen FI, Halvorsen AC, Andersen O (1991) Parasite avoidance: the cause of post-calving migrations in Rangifer. Can J Zool 69:2423–2429CrossRefGoogle Scholar
  18. Gog J, Woodroffe R, Swinton J (2002) Disease in endangered metapopulations: the importance of alternative hosts. P R Soc B 269:671–676CrossRefGoogle Scholar
  19. Howard E, Davis AK (2009) The fall migration flyways of monarch butterflies in eastern North America revealed by citizen scientists. J Insect Conserv 13:279–286CrossRefGoogle Scholar
  20. Krkosêk M, Lewis MA, Volpe JP (2005) Transmission dynamics of parasitic sea lice from farm to wild salmon. P R Soc B 272:689–696CrossRefGoogle Scholar
  21. Krkosêk M, Lewis MA, Morton A, Frazier LN, Volpe JP (2006) Epizootics of wild fish induced by farm fish. P Natl Acad Sci USA 103:15506–15510CrossRefGoogle Scholar
  22. Leong KLH, Yoshimura MA, Kaya HK, Williams H (1997) Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. J Invertebr Pathol 69:79–83PubMedCrossRefGoogle Scholar
  23. Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335CrossRefGoogle Scholar
  24. Malcolm SB, Cockrell BJ, Brower LP (1993) Spring recolonization of eastern North America by the monarch butterfly: successive brood or single sweep migration? In: Malcolm SB, Zalucki MP (eds) Biology and Conservation of the Monarch Butterfly. Natural History Museum of Los Angeles County, Los Angeles, pp 253–267Google Scholar
  25. Martin TG, Chadès I, Arcese P, Marra PP, Possingham HP, Norris DR (2007) Optimal conservation of migratory species. PLoS ONE 2:e751PubMedCrossRefPubMedCentralGoogle Scholar
  26. Masters AR, Malcolm SB, Brower LP (1988) Monarch butterfly (Danaus plexippus) thermoregulatory behavior and adaptations for overwintering in Mexico. Ecology 69:458–467CrossRefGoogle Scholar
  27. McLaughlin RE, Myers J (1970) Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. J Protozool 17:300–305CrossRefGoogle Scholar
  28. Montgomery DP, Martin DL, Evans CC (2010) Oklahoma roadside vegetation management guidelines, 4th edn. Department of Horticulture & Landscape Architecture. Oklahoma State University, StillwaterGoogle Scholar
  29. Nagano CD, Saki WH, Malcolm SB, Cockrell BJ, Donahue JP, Bower LB (1993) Spring migration of monarch butterflies in California. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 217–232Google Scholar
  30. Navarrete JL, Ramírez MI, Pérez-Salicrup DR (2011) Logging within protected areas: spatial evaluation of the monarch butterfly biosphere reserve, Mexico. Forest Ecol Manag 262:646–654CrossRefGoogle Scholar
  31. Nilssen AC, Haugerud RE (1995) Epizootiology of the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera, Oestridae), in reindeer, Rangifer tarandus (L.), in Norway. Can J Zool 73:1024–1036CrossRefGoogle Scholar
  32. Norris K (2008) Agriculture and biodiversity conservation: opportunity knocks. Conserv Lett 1:2–11CrossRefGoogle Scholar
  33. Oberhauser K (2012) Tachinid flies and monarch butterflies: citizen scientists document parasitism patterns over broad spatial and temporal scales. Am Entomol 58:19–22Google Scholar
  34. Oberhauser K, Gebhard I, Cameron C, Oberhauser S (2007) Parasitism of Monarch Butterflies (Danaus plexippus) by Lespesia archippivora (Diptera: Tachinidae). Am Midl Nat 157:312–328CrossRefGoogle Scholar
  35. Pleasants JM, Oberhauser KS (2012) Milkweed loss in agricultural fields because of herbicide use: effects on the monarch butterfly population. Insect Conserv Diver 6:135–144CrossRefGoogle Scholar
  36. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weiss AE (1980) Interaction among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Evol S 11:41–65CrossRefGoogle Scholar
  37. Prysby MD (2004) Natural enemies and survival of monarch eggs and larvae. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 27–38Google Scholar
  38. Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: west nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 1:5–12PubMedCrossRefPubMedCentralGoogle Scholar
  39. Robbins CS, Fitzpatrick JW, Hamel PB (1992) A warbler in trouble: Dendroica cerulea. In: Hagan JM, Johnston DW (eds) Ecology and conservation of neotropical migrant landbirds. Smithsonian Institution Press, Washington, pp 549–562Google Scholar
  40. Scharlemann JPW, Balmford A, Green RE (2005) The level of threat to restricted-range bird species can be predicted from mapped data on land use and human population. Biol Conserv 123:317–326CrossRefGoogle Scholar
  41. Sheehy J, Taylor CM, Norris DR (2011) The importance of stopover habitat for developing effective conservation strategies for migratory animals. J Ornithol 152:161–168CrossRefGoogle Scholar
  42. Simmons AM, Rogers CE (1991) Dispersal and seasonal occurrence of Noctuidonema guyanense, an ectoparasitic nematode of adult fall armyworms (Lepidoptera, Noctuidae) in the United States. J Entomol Sci 26:136–148Google Scholar
  43. Stapel JO, Ruberson JR, Gross HR Jr, Lewis WJ (1997) Progeny allocation by the parasitoid Lespesia archippivora (Diptera: Tachinidae) in larvae of Spodoptera exigua (Lepidoptera: Noctuidae). Env Entomol 26:265–271Google Scholar
  44. Sternberg ED, Lefèvre T, Rawstern AH, De Roode JC (2011) A virulent parasite can provide protection against a lethal parasitoid. Infect Genet and Evol 11:399–406CrossRefGoogle Scholar
  45. Vitousek PM, Mooney HA, Lubchenco J, Mellilo JM (1997) Human domination of earth’s ecosystem. Science 277:494–499CrossRefGoogle Scholar
  46. Wassenaar LI, Hobson KA (1998) Natal origins of migratory monarch butterflies at wintering colonies in Mexico: New isotopic evidence. Proc Natl Acad Sci USA 95:15436–15439PubMedCrossRefPubMedCentralGoogle Scholar
  47. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: Unraveling migratory connectivity. Trends Ecol Evol 17:76–83CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of ZoologyOklahoma State UniversityStillwaterUSA

Personalised recommendations