Advertisement

Urbanization predicts infection risk by a protozoan parasite in non-migratory populations of monarch butterflies from the southern coastal U.S. and Hawaii

  • Ania A. MajewskaEmail author
  • Dara A. Satterfield
  • Rebecca B. Harrison
  • Sonia Altizer
  • Jeffrey Hepinstall-Cymerman
Research Article
  • 13 Downloads

Abstract

Context

Urbanization can affect the density of hosts, altering patterns of infection risk in wildlife. Most studies examining associations between urbanization and host-parasite interactions have focused on vertebrate wildlife that carry zoonotic pathogens, and less is known about responses of other host taxa, including insects.

Objectives

Here we ask whether urban development predicts infection by a protozoan, Ophyrocystis elektroscirrha, in three populations of monarchs (Danaus plexippus): migratory monarchs in northeastern U.S., non-migratory monarchs in southeastern coastal U.S., and non-migratory monarchs in Hawaii.

Methods

We used impervious surface and developed land cover classes from the National Land Cover Database to derive proportional measures of urban development and an index of land cover aggregation at two spatial scales. Parasite data were from previous field sampling (Hawaii) and a citizen science project focused on monarch infection in North America.

Results

Proportional measures of urban development predicted greater infection prevalence for non-migratory monarchs sampled in the southern coastal U.S. and Hawaii, but not in the northern U.S. Aggregations of low intensity development, dominated by single-family housing, predicted greater infection prevalence in monarchs from the northern and southern coastal U.S. populations, but predicted lower infection prevalence in Hawaii.

Conclusions

Because natural habitats have been reduced by land-use change, plantings for monarchs in residential areas and urban gardens has become popular among the public. Mechanisms that underlie higher infection prevalence in urban landscapes remain unknown. Further monitoring and experimental studies are needed to inform strategies for habitat management to lower infection risk for monarchs.

Keywords

Danaus plexippus Ophryocystis elektroscirrha Host–parasite interaction Gardens Tropical milkweed Pollinator 

Notes

Acknowledgements

We thank Alexa McKay, Andy Davis, Leone Brown, Paola Barriga, Daniel Becker, Cecilia Sanchez, Rachel Smith, Carly Phillips, Anya Brown, David Stallknecht and members of the Yabsley, Altizer and Ezenwa labs for comments and discussion of manuscript drafts. We are also grateful to John Drake and Seth Wenger for discussion of statistical approaches. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Supplementary material

10980_2019_799_MOESM1_ESM.docx (4.2 mb)
Supplementary material 1 (DOCX 4295 kb)
10980_2019_799_MOESM2_ESM.csv (20 kb)
Supplementary material 2 (CSV 20 kb)

References

  1. Ackery PR, Vane-Wright RI (1984) Milkweed butterflies, their cladistics and biology: being an account of the natural history of the Danainae, a subfamily of the Lepidoptera, Nymphalidae. Dept. of Entomology, British Museum (Natural History), London, UKGoogle Scholar
  2. Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565CrossRefGoogle Scholar
  3. Altizer S, Hobson KA, Davis AK, De Roode JC, Wassenaar LI (2015) Do healthy monarchs migrate farther? Tracking natal origins of parasitized vs. uninfected monarch butterflies overwintering in Mexico. PLoS ONE 10:e0141371CrossRefGoogle Scholar
  4. Altizer S, Oberhauser KS (1999) Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). J Invertebr Pathol 74:76–88CrossRefGoogle Scholar
  5. Altizer S, 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. Baldock KC, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Potts SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc Lond Ser B 282:20142849CrossRefGoogle Scholar
  7. Bartel RA, Oberhauser K, de Roode J, Altizer S (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92:342–351CrossRefGoogle Scholar
  8. Batalden RV, Oberhauser KS (2015) Potential changes in eastern North American monarch migration in response to an introduced milkweed, Asclepias curassavica. In: Oberhauser K, Nail K, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic butterfly. Cornell University Press, Ithaca, pp 215–224Google Scholar
  9. Bhattacharya M, Primack RB, Gerwein J (2003) Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol Conserv 109:37–45CrossRefGoogle 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. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102CrossRefGoogle Scholar
  12. Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 161:1349–1350CrossRefGoogle Scholar
  13. Brower LP, Taylor OR, Williams EH, Slayback DA, Zubieta RR, Ramirez MI (2012) Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conserv Divers 5:95–100CrossRefGoogle Scholar
  14. Burnham KP, Anderson D (2003) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  15. Cohen H, Quistberg RD, Philpott SM (2017) Vegetation management and host density influence bee–parasite interactions in urban bardens. Environ Entomol 46:1313–1321CrossRefGoogle Scholar
  16. de la Barrera F, Reyes-Paecke S, Banzhaf E (2016) Indicators for green spaces in contrasting urban settings. Ecol Indic 62:212–219CrossRefGoogle Scholar
  17. De Roode JC, Gold L, Altizer S (2006) Virulence determinants in a natural butterfly–parasite system. Parasitology 134:657–668CrossRefGoogle Scholar
  18. De Roode JC, Pedersen AB, Hunter MD, Altizer S (2008) Host plant species affects virulence in monarch butterfly parasites. J Anim Ecol 77:120–126CrossRefGoogle Scholar
  19. Dolezal AG, Toth AL (2018) Feedbacks between nutrition and disease in honey bee health. Curr Opin Insect Sci 26:114–119CrossRefGoogle Scholar
  20. Dugarov Z, Baldanova D, Khamnueva T (2018) Impact of the degree of urbanization on composition and structure of helminth communities in the Mongolian racerunner (Eremias argus) Peters. J Helminthol 92:178–186CrossRefGoogle Scholar
  21. ESRI (2011) ArcGIS, Release 10 Environmental Systems Research Institute Redlands, CAGoogle Scholar
  22. Flockhart D, Pichancourt JB, Norris DR, Martin TG (2015) Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies. J Anim Ecol 84:155–165CrossRefGoogle Scholar
  23. Fürst M, McMahon DP, Osborne J, Paxton R, Brown M (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366CrossRefGoogle Scholar
  24. Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821CrossRefGoogle Scholar
  25. Garbuzov M, Samuelson EE, Ratnieks FL (2015) Survey of insect visitation of ornamental flowers in Southover Grange garden, Lewes, UK. Insect Sci 22:700–705CrossRefGoogle Scholar
  26. Giraudeau M, Mousel M, Earl S, McGraw K (2014) Parasites in the city: degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus). PLoS ONE 9:e86747CrossRefGoogle Scholar
  27. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957CrossRefGoogle Scholar
  28. Goulson D, Whitehorn P, Fowley M (2012) Influence of urbanisation on the prevalence of protozoan parasites of bumblebees. Ecol Entomol 37:83–89CrossRefGoogle Scholar
  29. Grubbs FE (1950) Sample criteria for testing outlying observations. Ann Math Stat 21:27–58CrossRefGoogle Scholar
  30. Harrison T, Winfree R (2015) Urban drivers of plant–pollinator interactions. Funct Ecol 29:879–888CrossRefGoogle Scholar
  31. Homer C, Dewitz J, Fry J, Coan M, Hossain N, Larson C, Herold N, McKerrow A, Van Driel J, Wickham J (2007) Completion of the 2001 National Land Cover Database for the counterminous United States. Photogramm Eng Remote Sensing 73:337–341Google Scholar
  32. Homer C, Dewitz J, Yang L, Jin S, Danielson P, Xian G, Megown K (2015) Completion of the 2011 National Land Cover Database for the conterminous United States-representing a decade of land cover change information. Photogramm Eng Remote Sensing 81:345–354Google Scholar
  33. Howard E, Aschen H, Davis AK (2010) Citizen science observations of monarch butterfly overwintering in the southern United States. Psyche J Entom 2010:6Google Scholar
  34. Lefèvre T, Oliver L, Hunter MD, de Roode J (2010) Evidence for trans-generational medication in nature. Ecol Lett 13:1485–1493CrossRefGoogle Scholar
  35. Lindsey E, Mehta M, Dhulipala V, Oberhauser K, Altizer S (2009) Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction. Ecol Entomol 34:551–561CrossRefGoogle Scholar
  36. Majewska AA, Sims S, Wenger SJ, Davis AK, Altizer S (2018) Do characteristics of pollinator-friendly gardens predict the diversity, abundance, and reproduction of butterflies? Insect Conserv Divers 11:370–382CrossRefGoogle Scholar
  37. McArt SH, Koch H, Irwin RE, Adler LS (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol Lett 17:624–636CrossRefGoogle Scholar
  38. McArt SH, Urbanowicz C, McCoshum S, Irwin RE, Adler LS (2017) Landscape predictors of pathogen prevalence and range contractions in US bumblebees. Proc R Soc Lond Ser B 284:20172181CrossRefGoogle Scholar
  39. McCallum H, Dobson A (2002) Disease, habitat fragmentation and conservation. Proc R Soc Lond Ser B 269:2041–2049CrossRefGoogle Scholar
  40. McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Computer software program produced by the authors at the University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html
  41. McLaughlin R, Myers J (1970) Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of the monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. J Eukaryot Microbiol 17:300–305Google Scholar
  42. Miller NG, Wassenaar LI, Hobson KA, Norris DR (2012) Migratory connectivity of the monarch butterfly (Danaus plexippus): patterns of spring re-colonization in eastern North America. PLoS ONE 7:e31891CrossRefGoogle Scholar
  43. Motooka P, Castro L, Nelson D, Nagai G, Ching L (2003) Weeds of Hawaii’s pastures and natural areas: an identification and management guide. University of Hawaii Press, HonoluluGoogle Scholar
  44. Nail KR, Stenoien C, Oberhauser K (2015) Immature monarch survival: effects of site characteristics, density, and time. Ann Entomol Soc Am 108:680–690CrossRefGoogle Scholar
  45. Neel MC, McGarigal K, Cushman SA (2004) Behavior of class-level landscape metrics across gradients of class aggregation and area. Landscape Ecol 19:435–455CrossRefGoogle Scholar
  46. Oberhauser KS, Cotter D, Davis D, Decarie R, Behnumea AE, Galino-Leal C, Gallina Tessaro MP, Howard E, Lauriault J, Maczieski W, Malcolm S (2008) North American monarch conservation plan. Commission for Environmental Cooperation, MontrealGoogle Scholar
  47. Oberhauser KS, Prysby MD, Mattila HR, Stanley-Horn DE, Sears MK, Dively G, Olson E, Pleasants JM, Lam W-KF, Hellmich RL (2001) Temporal and spatial overlap between monarch larvae and corn pollen. Proc Natl Acad Sci USA 98:11913–11918CrossRefGoogle Scholar
  48. Oyeyele S, Zalucki M (1990) Cardiac glycosides and oviposition by Danaus plexippus on Asclepias fruticosa in south-east Queensland (Australia), with notes on the effect of plant nitrogen content. Ecol Entomol 15:177–185CrossRefGoogle Scholar
  49. Páez D, Restif O, Eby P, Plowright R (2018) Optimal foraging in seasonal environments: implications for residency of Australian flying foxes in food-subsidized urban landscapes. Philos Trans R Soc Lond Ser B 373:20170097CrossRefGoogle Scholar
  50. Pierce AA, de Roode JC, Altizer S, Bartel RA (2014) Extreme heterogeneity in parasitism despite low population genetic structure among monarch butterflies inhabiting the Hawaiian Islands. PLoS ONE 9:e100061CrossRefGoogle Scholar
  51. Pleasants J (2017) Milkweed restoration in the Midwest for monarch butterfly recovery: estimates of milkweeds lost, milkweeds remaining and milkweeds that must be added to increase the monarch population. Insect Conserv Divers 10:42–53CrossRefGoogle Scholar
  52. Pocius VM, Debinski DM, Pleasants JM, Bidne KG, Hellmich RL (2018) Monarch butterflies do not place all of their eggs in one basket: oviposition on nine Midwestern milkweed species. Ecosphere 9(1):02064CrossRefGoogle Scholar
  53. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353CrossRefGoogle Scholar
  54. Prange S, Gehrt SD, Wiggers EP (2003) Demographic factors contributing to high raccoon densities in urban landscapes. J Wildl Manag 67:324–333CrossRefGoogle Scholar
  55. R package lme4: Linear mixed-effects models using ‘Eigen’ and S4, v. 1.1-15 (2017)Google Scholar
  56. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. (2018) Vienna, AustriaGoogle Scholar
  57. Satterfield DA, Altizer S, Williams M-K, Hall RJ (2017) Environmental persistence influences infection dynamics for a butterfly pathogen. PLoS ONE 12(1):e0169982CrossRefGoogle Scholar
  58. Satterfield DA, Maerz JC, Altizer S (2015) Loss of migratory behaviour increases infection risk for a butterfly host. Proc R Soc Lond Ser B 282:20141734CrossRefGoogle Scholar
  59. Satterfield DA, Maerz JC, Hunter MD, Flockhart DTT, Hobson KA, Norris DR, Streit H, de Roode JC, Altizer S (2018) Migratory monarchs that encounter resident monarchs show life-history differences and higher rates of parasite infection. Ecol Lett 21:1670–1680CrossRefGoogle Scholar
  60. Satterfield DA, Villablanca FX, Maerz JC, Altizer S (2016) Migratory monarchs wintering in California experience low infection risk compared to monarchs breeding year-round on non-native milkweed. Integr Comp Biol 56:343–352CrossRefGoogle Scholar
  61. Schultz CB, Brown LM, Pelton E, Crone EE (2017) Citizen science monitoring demonstrates dramatic declines of monarch butterflies in western North America. Biol Conserv 214:343–346CrossRefGoogle Scholar
  62. Seto KC, Fragkias M, Güneralp B, Reilly MK (2011) A meta-analysis of global urban land expansion. PLoS ONE 6:e23777CrossRefGoogle Scholar
  63. Shapiro AM (2002) The Californian urban butterfly fauna is dependent on alien plants. Divers Distrib 8:31–40CrossRefGoogle Scholar
  64. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, Lipkin WI, Toth AL, Cox-Foster DL (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5(12):e14357CrossRefGoogle Scholar
  65. Sternberg ED, Lefèvre T, Li J, de Castillejo CLF, Li H, Hunter MD, de Roode J (2012) Food plant derived disease tolerance and resistance in a natural butterfly–plant–parasite interactions. Evolution 66:3367–3376CrossRefGoogle Scholar
  66. Taylor OR (2018) Monarch Watch https://www.monarchwatch.org/waystations/. Accessed 11 Dec 2018
  67. Theodorou P, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, Paxton RJ (2016) Pollination services enhanced with urbanization despite increasing pollinator parasitism. Proc R Soc Lond Ser B 283:20160561CrossRefGoogle Scholar
  68. Thogmartin WE, Wiederholt R, Oberhauser K, Drum RG, Diffendorfer JE, Altizer S, Taylor OR, Pleasants J, Semmens D, Semmens B, Erickson R, Libby K, Lopez-Hoffman L (2017) Monarch butterfly population decline in North America: identifying the threatening processes. R Soc Open Sci 4:170760CrossRefGoogle Scholar
  69. Urquhart F, Urquhart N (1978) 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. Can J Zool 56:1759–1764CrossRefGoogle Scholar
  70. Wen M, Zhang X, Harris CD, Holt JB, Croft JB (2013) Spatial disparities in the distribution of parks and green spaces in the USA. Ann Behav Med 45:18–27CrossRefGoogle Scholar
  71. Xian GZ, Homer CG, Dewitz J, Fry J, Hossain N, Wickham J (2011) Change of impervious surface area between 2001 and 2006 in the conterminous United States. Photogramm Eng Remote Sensing 77:758–762Google Scholar
  72. Youngsteadt E, Appler RH, López-Uribe MM, Tarpy DR, Frank SD (2015) Urbanization increases pathogen pressure on feral and managed honey bees. PLoS ONE 10(11):e0142031CrossRefGoogle Scholar
  73. Zalucki MP (1983) Modelling egg laying in the Monarch butterfly Danaus plexippus L. Res Popul Ecol 25:353–365CrossRefGoogle Scholar
  74. Zalucki MP, Brower LP, Malcolm S (1990) Oviposition by Danaus plexippus in relation to cardenolide content of three Asclepias species in the southeastern USA. Ecol Entomol 15:231–240CrossRefGoogle Scholar
  75. Zalucki MP, Clarke AR (2004) Monarchs across the Pacific: the Columbus hypothesis revisited. Biol J Linn Soc 82:111–121CrossRefGoogle Scholar
  76. Zalucki MP, Kitching RL (1982) The analysis and description of movement in adult Danaus plexippus L. (Lepidoptera: Danainae). Behaviour 80:174–197CrossRefGoogle Scholar
  77. Zalucki MP, Parry H, Zalucki J (2016) Movement and egg laying in monarchs: to move or not to move, that is the equation. Austral Ecol 41:154–167CrossRefGoogle Scholar
  78. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar
  79. Zuur AF, Ieno EN, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Center for the Ecology of Infectious DiseaseUniversity of GeorgiaAthensUSA
  3. 3.U.S Fish and Wildlife ServiceManteoUSA
  4. 4.Warnell School of Forestry & Natural ResourcesUniversity of GeorgiaAthensUSA

Personalised recommendations