Skip to main content

Colonization and usage of eight milkweed (Asclepias) species by monarch butterflies and bees in urban garden settings

Abstract

Planting milkweeds on public and private lands has emerged as a central conservation strategy for restoring declining North American migratory populations of the monarch butterfly (Danaus plexippus). Nearly all actionable science on this issue has focused on restoring common milkweed (Asclepias syriaca L.) in rural land types. The aim of this study was to develop recommendations for the best milkweeds for managed gardens intended to support both monarch butterflies and bees. Eight milkweed (Asclepias) species varying in height, form, and leaf shape were grown in a common-garden experiment at a public arboretum. We measured milkweed growth, tillering, and bloom periods, conducted bi-weekly counts of eggs and larvae to assess colonization by wild monarchs, and evaluated suitability for growth of monarch larvae. We also quantified bee visitation and compared the bee assemblages associated with six of the eight species, augmented with additional collections from other sites. Monarchs rapidly colonized the gardens, but did not equally use all of the milkweed species. More eggs and larvae were found on taller, broad-leaved milkweeds, but there was relatively little difference in larval performance, suggesting ovipositional preference for more apparent plants. Asclepias tuberosa and A. fascicularis attracted the greatest number of bees, whereas bee genus diversity was greatest on A. verticillata, A. fascicularis, and A. tuberosa. Milkweeds that do not spread extensively by tillering may be best suited for managed gardens. Combining milkweeds that are preferred by ovipositing monarchs with ones that are particularly attractive to bees may enhance conservation value of small urban gardens.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Agrawal AA (2017) Monarchs and milkweed. A migrating butterfly, a poisonous plant, and their remarkable story of coevolution. Princeton University Press, Princeton

    Book  Google Scholar 

  2. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:132–149

    Article  Google Scholar 

  3. Agrawal AA, Fishbein M, Jetter R, Salminen J-P, Goldstein JB, Freitag AE, Sparks JB (2009) Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867

    Article  Google Scholar 

  4. Agrawal AA, Ali JG, Rasmann S, Fishbein M (2015) Macroevolutionary trends in the defense of milkweeds against monarchs: latex, cardenolides, and tolerance of herbivory. In: Oberhauser KS, Altizer S, Nail K (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell Univ Press, Ithaca, pp 47–59

    Google Scholar 

  5. Baldock KC, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower–visiting insects. Proc R Soc B 282(1803):20142849

    Article  Google Scholar 

  6. Bartholomew CS, Yeargan KV (2001) Phenology of milkweed (Asclepidaceae) growth and monarch (Lepidoptera: Nymphalidae) reproduction in Kentucky and ovipositional preference between common and honeyvine milkweed. J Kans Entomol Soc 74:211–220

    Google Scholar 

  7. Bellamy CC, van der Jagt APN, Barbour S, Smith M, Moseley D (2017) A spatial framework for targeting urban planning for pollinators and people with local stakeholders: a route to healthy, blossoming communities? Environ Res 158:255–268

    CAS  Article  Google Scholar 

  8. Betz RF, Struven RD, Wall JE, Heitler FB (1994) Insect pollinators of 12 milkweed (Asclepias) species. In: 13th North American Prairie Conference vol 13, pp 47–60

  9. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Seetele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    CAS  Article  Google Scholar 

  10. Borders B, Lee-Mäder E (2015) Milkweeds. A conservation practitioner’s guide. The Xerces Society for Invertebrate Conservation. http://www.xerces.org Accessed 17 Nov 2017

  11. 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 5:95–100

    Article  Google Scholar 

  12. Cohen JA, Brower LP (1982) Oviposition and larval success of wild monarch butterflies (Lepidoptera: Danaidae) in relation to host plant size and cardenolide concentration. J Kans Entomol Soc 55:343–348

    Google Scholar 

  13. Colding J, Lundberg J, Folke C (2006) Incorporating green-area user groups in urban ecosystem management. AMBIO 35:237–244

    Article  Google Scholar 

  14. Colla S, Richardson L, Williams P (2011) Bumble bees of the eastern United States. USDA Pollinator Partnership. https://www.fs.fed.us/wildflowers/pollinators/documents/BumbleBeeGuideEast2011.pdf

  15. Cutting BT, Tallamy DW (2015) An evaluation of butterfly gardens for restoring habitat for the monarch butterfly (Lepidoptera: Danaidae). Environ Entomol 44:1329–1344

    Article  Google Scholar 

  16. Davis AK, Dyer LA (2015) Long-term trends in Eastern North American monarch populations: a collection of studies focusing on spring, summer, and fall dynamics. Ann Entomol Soc Am 108:661–663

    Article  Google Scholar 

  17. Doussourd DE, Eisner T (1987) Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898–900

    Article  Google Scholar 

  18. Droege S (2015) The very handy manual: how to catch and identify bees and manage a collection. USGS Native Bee Inventory and Monitoring bees.tennessee.edu/publications/HandyBeeManual.pdf

  19. Dyer LA, Forister ML (2016) Wherefore and whither the modeler: understanding the population dynamics of monarchs will require integrative and quantitative techniques. Ann Entomol Soc Am 109:172–175

    Article  Google Scholar 

  20. Erickson JM (1973) The utilization of various Asclepias species by larvae of the monarch butterfly, Danaus plexippus. Psyche 80:230–244

    Article  Google Scholar 

  21. Fischer SJ, Williams EH, Brower LP, Palmiotto PA (2015) Enhancing monarch butterfly reproduction by mowing fields of common milkweed. Am Midl Nat 173:229–240

    Article  Google Scholar 

  22. Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77:1061–1073

    Article  Google Scholar 

  23. Flockhart DTT, Wassenaar LI, Martin TG, Hobson KA, Wunder MB, Norris DR (2013) Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America. Proc R Soc B 280:20131087

    Article  Google Scholar 

  24. Flockhart DT, Pichancourt JB, Norris RD, Martin TG (2015) Unraveling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies. J Anim Ecol 84:155–165

    Article  Google Scholar 

  25. Garbuzov M, Ratnieks FLW (2014a) Quantifying variation among garden plants in attractiveness to bees and other flower-visiting insects. Func Ecol 28:364 – 374

    Article  Google Scholar 

  26. Garbuzov M, Ratnieks FLW (2014b) Listmania: the strengths and weaknesses of lists of garden plants to help pollinators. Bioscience 64:1019–1026

    Article  Google Scholar 

  27. Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 2:90–98

    Article  Google Scholar 

  28. Gustafsson KM, Agrawal AA, Lewenstein BV, Wolf SA (2015) The monarch butterfly through time and space: the social construction of an icon. Bioscience 65:612–622

    Article  Google Scholar 

  29. Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M (2017) The city as a refuge for insect pollinators. Conserv Biol 31:24–29

    Article  Google Scholar 

  30. Hartzler RG (2010) Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Prot 29:1542–1544

    Article  Google Scholar 

  31. Heinrich B (1976) Resource partitioning among some social insects: bumblebees. Ecology 57:874–889

    Article  Google Scholar 

  32. Hernandez JL, Frankie GW, Thorp RW (2009) Ecology of urban bees: a review of current knowledge and directions for future study. Cities Environ 2:1–15

    Article  Google Scholar 

  33. Holzinger F, Frick C, Wink M (1992) Molecular basis for the insensitivity of the monarch (Danaus plexippus) to cardiac glycosides. FEBS Lett 314:477–480

    CAS  Article  Google Scholar 

  34. Inamine H, Ellner SP, Springer JP, Agrawal AA (2016) Linking the continental migratory cycle of the monarch butterfly to understand its population decline. Oikos 125:1081–1091

    Article  Google Scholar 

  35. Ivey C, Martinez P, Wyatt R (2003) Variation in pollinator effectiveness in swamp milkweed, Asclepias incarnata (Apocynaceae). Am J Bot 90:214–225

    Article  Google Scholar 

  36. Journey North (2017) Monarch butterflies. News Spring 2017. https://www.learner.org/jnorth/monarchs/news/spring-2017/9 Accessed 25 Apr 2017

  37. Kephart SR (1983) The partitioning of pollinators among three species of Asclepias. Ecology 64:120–133

    Article  Google Scholar 

  38. Koh I, Lonsdorf EV, Williams NM, Brittain C, Isaacs R, Gibbs J, Ricketts TH (2016) Modeling the status, trends, and impacts of wild bee abundance in the United States. Proc Nat Acad Sci USA 113:140–145

    CAS  Article  Google Scholar 

  39. Lady Bird Johnson Wildflower Center (2018) Asclepias latifolia. https://www.wildflower.org/plants/result.php?id_plant=ASLA4. Accessed 8 Jan 2018

  40. Liaw S-W (1999) The structure of the gynostegium, breeding system, and pollination ecology of spider milkweed, Asclepias viridis Walter (Apocynaceae). Oklahoma Native Plant Rec 16:10–44

    Article  Google Scholar 

  41. Lundholm JT, Richardson PJ (2010) Habitat analogies for reconciliation ecology in urban and industrial environments. J Appl Ecol 47:966–975

    Article  Google Scholar 

  42. Maclvor JS, Roberto AN, Sodhi DS, Onuferko TM, Cadotte MW (2017) Honey bees are the dominant diurnal pollinator of native milkweed in a large urban park. Ecol Evol 7:8456–8462

    Article  Google Scholar 

  43. Magurran AE (2004) Measuring biological diversity. Blackwell, Malden

    Google Scholar 

  44. 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. https://doi.org/10.1111/icad.12286

    Article  Google Scholar 

  45. Malcolm SB (1995) Milkweeds, monarch butterflies and the ecological significance of cardenolides. Chemoecology 5/6:101–117

    Article  Google Scholar 

  46. Malcolm SB, Brower LP (1989) Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Cell Mol Life Sci 45:284–295

    CAS  Article  Google Scholar 

  47. Malcolm SB, Zalucki MP (1993) Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles

  48. Malcolm SB, Cockrell BJ, Brower LP (1992) Continental host-plant use by a specialist insect herbivore: Milkweeds, cardenolides, and the monarch butterfly. In: Menken SBJ, Visser JH, Harrewijn P (eds) Proceedings of the 8th International Symposium Insect-Plant Relationships. Springer, pp 43–45

  49. Miller JR (2005) Biodiversity conservation and the extinction of experience. Trends Ecol Evol 20:430–434

    Article  Google Scholar 

  50. Monarch Joint Venture (2018) https://monarchjointventure.org/. Accessed 18 Jan 2018

  51. MonarchWatch (2017a) Monarch waystations. https://www.monarchwatch.org/waystations/. Accessed 5 Jan 2018

  52. MonarchWatch (2017b) Biology: parasite control (Ophryocystis electroscirrha). https://www.monarchwatch.org/biology/control.htm. Accessed 14 May 2018

  53. MonarchWatch (2017c) Milkweeds. http://www.monarchwatch.org/milkweed/guide. Accessed 5 Jan 2018

  54. National Oceanic and Atmospheric Administration (2018) Freeze/frost occurrence data. https://www.ncdc.noaa.gov/climatenormals/clim20supp1/states/KY.pdf. Accessed 10 Feb 2018

  55. National Pollinator Garden Network (2018) Million pollinator garden challenge. Available from: http://millionpollinatorgardens.org/. Accessed 18 Jan 2018

  56. National Wildlife Federation (2018) Certified Wildlife Habitat program. https://www.nwf.org/garden-for-wildlife. Accessed 10 Jan 2018

  57. Packer L, Genaro JA, Sheffield CS (2007) The bee genera of eastern Canada. Can J Arthropod Identif. http://www.biology.ualberta.ca/bsc/ejournal/pgs03/pgs_03.html

  58. Palmer MA (2012) Socioenvironmental sustainability and actionable science. Bioscience 62:5–6

    Article  Google Scholar 

  59. Petschenka G, Agrawal AA (2015) Milkweed butterfly resustance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc R Soc B 282:20151865

    Article  Google Scholar 

  60. Pleasants JM (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 10:42–53

    Article  Google Scholar 

  61. Pleasants JM, Oberhauser KS (2013) Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conserv Divers 6:135–144

    Article  Google Scholar 

  62. Pleasants JM, Zalucki MP, Oberhauser KS, Brower LP, Taylor OR, Thogmartin WE (2017) Interpreting surveys to estimate the size of the monarch butterfly population: pitfalls and prospects. PLoS ONE 12(7):e0181245

    Article  Google Scholar 

  63. Pocius VM, Debinski DM, Bidne KG, Hellmich RL, Hunter FK (2017a) Performance of early instar monarch butterflies (Danaus plexippus L.) on nine milkweed species native to Iowa. J Lepid Soc 71:153–161

    Google Scholar 

  64. Pocius VM, Debinski DM, Pleasants JM, Bidne KG, Hellmich RL, Brower LP (2017b) Milkweed matters: Monarch butterfly (Lepidoptera: Nymphalidae) survival and development on nine Midwestern milkweed. Environ Entomol 46:1098–1105

    CAS  Article  Google Scholar 

  65. 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):e02064

    Article  Google Scholar 

  66. Pollinator Health Task Force (2015) National strategy to promote the health of honey bees and other pollinators. White House, Washington

    Google Scholar 

  67. Pollinator Partnership (2018) Ecoregional plant guides. http://pollinator.org/guides. Accessed 10 Jan 2018

  68. Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Beismeijer JG, Breeze TD (2016) Safeguarding pollinators and their values to human wellbeing. Nature 540:220–228

    CAS  Article  Google Scholar 

  69. Rasmann S, Johnson MD, Agrawal AA (2009) Induced responses to herbivory and jasmonate in three milkweed species. J Chem Ecol 35:1326–1334

    CAS  Article  Google Scholar 

  70. Rausher MD (1978) Search image of leaf shape in a butterfly. Science 200:1073–1073

    Article  Google Scholar 

  71. Rausher MD (1981) The effect of native vegetation on the susceptibility of Aristolochia reticulata (Aristolochiaceae) to herbivore attack. Ecology 62:1187–1195

    Article  Google Scholar 

  72. Rendón-Salinas E, Fajardo-Arroyo A, Tavera-Alonso G (2015) Forest surface occupied by monarch butterfly hibernation colonies in December 2014. World Wildlife Fund, https://c402277.ssl.cf1.rackcdn.com/publications/768/files/original/REPORT_Monarch_Butterfly_colonies_Winter_2014. Accessed 6 Feb 2018

  73. Rosenzweig ML (2003) Reconciliation ecology and the future of species diversity. Oryx 37:194–205

    Article  Google Scholar 

  74. Statistix Analytical Software (2013) Statistix 10 User’s Manual. Tallahassee, FL

    Google Scholar 

  75. Thogmartin WE, López-Hoffman L, Rohwedser J, Differndorfer J, Drum R, Semmens D (2017) Restoring monarch butterfly habitat in the Midwestern US: ‘all hands on deck’. Environ Res Lett 12:07405

    Article  Google Scholar 

  76. US Fish and Wildlife Service (2018) Save the monarch butterfly; https://www.fws.gov/savethemonarch/. Accessed 15 Jan 2018

  77. USDA (2018) United States Department of Agriculture Natural Resources Conservation Service; https://plants.usda.gov/java/nameSearch/. Accessed 11 May 2018

  78. Willson MF, Bertin RI (1979) Flower-visitors, nectar production, and inflorescence size of Asclepias syriaca. Can J Bot 57:1380–1388

    Article  Google Scholar 

  79. Willson MF, Bertin RI, Price PW (1979) Nectar production and flower visitors of Asclepias verticillata. Am Midl Nat 102:23–35

    Article  Google Scholar 

  80. Woodson RE Jr (1954) The North American species of Asclepias L. Ann Mo Bot Gard 41:1–211

    Article  Google Scholar 

  81. Wyatt R, Broyles SB (1994) Ecology and evolution of reproduction in milkweeds. Annu Rev Ecol Syst 25:423–441

    Article  Google Scholar 

  82. Yeargan KV, Allard CM (2005) Comparison of common milkweed and honeyvine milkweed (Asclepidaceae) as host plants for monarch larvae (Lepidoptera: Nymphalidae). Kans Entomol Soc 78:247–251

    Article  Google Scholar 

  83. Zalucki MP, Kitching RL (1982) Dynamics of oviposition in Danaus plexippus (Insecta: Lepidoptera) on milkweed, Asclepias spp. J Zool Lond 198:103–116

    Article  Google Scholar 

  84. Zalucki MP, Brower LP, Malcolm SB (1990) Oviposition by Danaus plexippus in relation to cardenolide content of three Asclepias species in the southeastern U.S.A. Ecol Entomol 15:231–240

    Article  Google Scholar 

  85. Zalucki MP, Brower LP, Alonso A (2001) Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecol Entomol 26:212–224

    Article  Google Scholar 

  86. Zaya DN, Pearse IS, Spyreas G (2017) Long-term trends in Midwestern milkweed abundances and their relevance to monarch butterfly declines. Bioscience 67:343–356

    Article  Google Scholar 

Download references

Acknowledgements

We thank the staff at the Arboretum and State Botanical Garden of Kentucky, particularly Jesse Dahl, for help establishing and maintaining the garden plots, and R. Brockman, B. Mach, T.D. McNamara, C.T. Redmond, and L. Wallis (University of Kentucky Entomology) for help with the field work. We thank Blair Leano-Helvey of Idlewild Butterfly Farm for donating larvae used in this study. This research was supported in part by Grants from the U.S. Golf Association, US Department of Agriculture-National Institute of Food and Agriculture-Specialty Crop Research Initiative Grant 2016-51181-235399, Bayer North American Bee Care Center and the University of Kentucky Nursery Research Endowment Fund.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel A. Potter.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The information reported in this paper (No. 18-08-029) is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Baker, A.M., Potter, D.A. Colonization and usage of eight milkweed (Asclepias) species by monarch butterflies and bees in urban garden settings. J Insect Conserv 22, 405–418 (2018). https://doi.org/10.1007/s10841-018-0069-5

Download citation

Keywords

  • Danaus plexippus
  • Pollinator conservation
  • Urban ecology
  • Citizen science
  • Apidae