Journal of Insect Conservation

, Volume 20, Issue 2, pp 223–237 | Cite as

Species distribution models for natural enemies of monarch butterfly (Danaus plexippus) larvae and pupae: distribution patterns and implications for conservation

  • Shaun M. McCoshum
  • Shannon L. Andreoli
  • Carl M. Stenoien
  • Karen S. Oberhauser
  • Kristen A. Baum


Prey populations can be strongly influenced by predators and parasitoids, and migratory prey whose distributions vary geographically throughout their breeding seasons encounter different combinations of predators and parasitoids throughout their range. North American monarch butterflies (Danaus plexippus) are susceptible to a wide variety of natural enemies, but the distribution of these natural enemies has not been quantified. We developed ecological niche models using environmental data to identify areas with suitable abiotic conditions for eight known natural enemies of monarchs, including six predators: Arilus cristatus, Harmonia axyridis, Monomorium minimum, Podisus maculiventris, Polistes spp., and Solenopsis geminata; and two parasitoids: Lespesia archippivora and Pteromalus cassotis. We combined correlated suitable areas for individual predators and parasitoids to identify regions with the most predator and parasitoid species potential. The Gulf Coast, West Coast, Florida, and parts of the eastern United States are predicted to have the most natural enemy species. We suggest that future research should assess monarch mortality rates in these areas, and that monarch conservation strategies consider pressure from natural enemies.


Monarch Natural enemies Niche model Conservation Parasitoid Predator Danaus plexippus 



Thanks to Mona Papeś and Adam Mathews for assistance with MaxEnt and GIS troubleshooting; Elizabeth Howard, who shared Journey North data; Journey North and MLMP volunteers who collected occurrence data that were key to our model development; and two anonymous reviewers for their input.


  1. 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
  2. Arnaud PH (1978) A host-parasite catalog of North American Tachinidae (Diptera). USDA, Misc. Pub 1319Google Scholar
  3. Barbosa PA (1998) Conservation biological control. Academic Press, San DiegoGoogle Scholar
  4. Barron MC, Wratten SD, Barlow ND (2004) Phenology and parasitism of the red admiral butterfly Bassaris gonerilla (Lepidoptera: Nymphalidae). NZ J Ecol 28:105–111Google Scholar
  5. Bartel RA, Oberhauser KS, De Roode JC, Altizer SM (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92:342–351CrossRefPubMedGoogle Scholar
  6. Baum KA, Mueller EK (2015) Grassland and roadside management practices affect milkweed abundance and opportunities for monarch recruitment. In: Oberhauser KS, Nail KR, Altizer S (eds) Monarchs is a changing world biology and conservation of an iconic butterfly. Cornell University, Ithaca, pp 197–206Google Scholar
  7. Baum KA, Sharber WV (2012) Fire creates host plant patches for monarch butterflies. Biol Lett 8:968–971CrossRefPubMedPubMedCentralGoogle Scholar
  8. Beneway DF (1963) A revision of the flies of the genus Lespesia ( =Achaetoneura) in North America (Diptera: Tachinidae). Univ Kans Sci Bull 44:627–677Google Scholar
  9. Bhowmik PC, Bandeen JD (1976) The biology of Canadian Weeds: 19. Asclepias syriaca L. Can J Plant Sci 56:579–589CrossRefGoogle Scholar
  10. Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77CrossRefGoogle Scholar
  11. Borkin S (1982) Notes on shifting distributing patterns and survival of immature Danaus plexippus (Lepidoptera: Danaidae) on the food plant Asclepias syriaca (Monarch butterfly, Wisconsin). Great Lakes Entomologist (USA) 15:199–206Google Scholar
  12. Brower AV, Boyce TM (1991) Mitochondrial DNA variation in monarch butterflies. Evolution 45:1281–1286CrossRefGoogle Scholar
  13. Brower AVZ, Jeansonne MM (2004) Geographical populations and “subspecies” of New World monarch butterflies (Nymphalidae) share a recent origin and are not phylogenetically distinct. Ann Entomol Soc Am 97:519–523CrossRefGoogle Scholar
  14. 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
  15. Brown JL (2014) SDMtoolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5:694–700CrossRefGoogle Scholar
  16. Calvert WH (1996) Fire ant predation on monarch larvae (Nymphalidae: Danainae) in a central Texas prairie. J Lepid Soc 50:149–151Google Scholar
  17. Calvert W (2004) The effect of fire ants on monarchs breeding in Texas. In: The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 47–53Google Scholar
  18. Center for Biological Diversity, Xerces Society, Brower LP (2014) Petition (2014) Petition to protect the monarch butterfly (Danaus plexippus plexippus) under the Endangered Species Act. Submitted to Secretary of the US Department of the Interior by The Center for Biological Diversity and Center for Food Safety, joined by The Xerces Society and Dr. Lincoln Brower, on August 26th, 2014Google Scholar
  19. Cronin JT, Reeve JD (2014) An integrative approach to understanding host–parasitoid population dynamics in real landscapes. Basic Appl Ecol 15:101–113CrossRefGoogle Scholar
  20. Crouch ML (2014) Comments to USDA APHIS on the draft environmental impact statement for determinations of nonregulated status for dicamba resistant soybean and cotton varieties, Monsanto Petitions (10–188–01p and 12-‐185–01p) Center for Food Safety, Science Comments II. Pacific Northwest 808:681–7688Google Scholar
  21. Cutting BT, Tallamy DW (2015) An evaluation of butterfly gardens for restoring habitat for the monarch butterfly (Lepidoptera: Danaidae). Environ Entomol 44:1328–1335CrossRefPubMedGoogle Scholar
  22. Diehl E, Sereda E, Wolters V, Birkhofer K (2013) Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta-analysis. J Appl Ecol 50:262–270CrossRefGoogle Scholar
  23. Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, CambridgeGoogle Scholar
  24. Dosdall LM, Mason PG (2010) Key pests and parasitoids of oilseed rape or canola in North America and the importance of parasitoids in integrated management. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer, New York, pp 167–213CrossRefGoogle Scholar
  25. Dweck HK (2009) Antennal sensory receptors of Pteromalus puparum female (Hymenoptera: Pteromalidae), a gregarious pupal endoparasitoid of Pieris rapae. Micron 40:769–774CrossRefPubMedGoogle Scholar
  26. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57CrossRefGoogle Scholar
  27. Etchegaray JB, Nishida T (1975) Biology of Lespesia archippivora (Diptera: Tachinidae) Proceedings of the Hawaiian Entomological Society 22:41–49Google Scholar
  28. Fischer SJ, Williams EH, Brower LP, Palmiotto PA (2015) Enhancing monarch butterfly reproduction by mowing fields of common milkweed. Am Midl Nat 173:229–240CrossRefGoogle Scholar
  29. 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 84:155–165CrossRefPubMedGoogle Scholar
  30. GBIF (2015a) GBIF Occurrence. doi: 10.15468/dl.8shy70
  31. GBIF (2015b) GBIF Occurrence. doi: 10.15468/dl.iwhog8
  32. GBIF (2015c) GBIF Occurrence. doi: 10.15468/dl.i0aqxd
  33. GBIF (2015d) GBIF Occurrence. doi: 10.15468/dl.w05w2w
  34. GBIF (2015e) GBIF Occurrence. doi: 10.15468/dl.7uvhwj
  35. GBIF (2015f) GBIF Occurrence. doi: 10.15468/dl.d3q0te
  36. (2015) GBIF Occurrence. doi: 10.15468/dl.oz51d0
  37. Gomes DS, Elizalde L, Queiroz JM (2013) Parasitoids of the endangered leafcutter ant Atta robusta Borgmeier in urban and natural areas. Revista Brasileira de Entomologia 57:335–339CrossRefGoogle Scholar
  38. Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039CrossRefPubMedGoogle Scholar
  39. Hartzler RG (2010) Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Prot 29:1542–1544CrossRefGoogle Scholar
  40. Hartzler RG, Buhler DD (2000) Occurrence of common milkweed (Asclepias syriaca) in cropland and adjacent areas. Crop Prot 19:363–366CrossRefGoogle Scholar
  41. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  42. Howard E, Davis AK (2004) Documenting the spring movements of monarch butterflies with Journey North, a citizen science program. Monarch Butterfly Biol Conserv 105:114Google Scholar
  43. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258CrossRefPubMedGoogle Scholar
  44. Huffaker CB, Herman S, Shea K (1963) Experimental studies on predation: complex dispersion and levels of food in an acarine predator-prey interaction. University of Calif, Hillgardia pp 305–330Google Scholar
  45. Kareiva P (1987) Habitat fragmentation and the stability of predator-prey interactions. Nature 326:388–390CrossRefGoogle Scholar
  46. Knight A, Brower LP (2009) The influence of eastern North American autumnal migrant monarch butterflies (Danaus plexippus L.) on continuously breeding resident monarch populations in southern Florida. J Chem Ecol 35:816–823CrossRefPubMedGoogle Scholar
  47. Koch R, Hutchison W, Venette R, Heimpel G (2003) Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol Control 28:265–270CrossRefGoogle Scholar
  48. Koch R, Venette R, Hutchison W (2006) Predicted impact of an exotic generalist predator on monarch butterfly (Lepidoptera: Nymphalidae) populations: a quantitative risk assessment. Biol Invasions 8:1179–1193CrossRefGoogle Scholar
  49. Kruess A (2003) Effects of landscape structure and habitat type on a plant-herbivore-parasitoid community. Ecography 26:283–290CrossRefGoogle Scholar
  50. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201CrossRefPubMedGoogle Scholar
  51. Lei G-C, Hanski I (1997) Metapopulation structure of Cotesia melitaearum, a specialist parasitoid of the butterfly Melitaea cinxia. Oikos 78:91–100CrossRefGoogle Scholar
  52. Leong KL, Yoshimura MA, Kaya H, Williams H (1997) Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. J Invertebr Pathol 69:79–83CrossRefPubMedGoogle Scholar
  53. Lyons JI, Pierce AA, Barribeau SM, Sternberg ED, Mongue AJ, Roode De, Jacobus C (2012) Lack of genetic differentiation between monarch butterflies with divergent migration destinations. Mol Ecol 21:3433–3444CrossRefPubMedGoogle Scholar
  54. Malcolm SB, Cockrell BJ, Brower LP (1987) Monarch butterfly voltinism: effects of temperature constraints at different latitudes. Oikos 49:77–82CrossRefGoogle Scholar
  55. 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, California. pp 253–267Google Scholar
  56. McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194CrossRefPubMedGoogle Scholar
  57. McCoshum SM, Baum KA (2014) Sex ratios and Ophryocystis elektroscirrha infection levels of Danaus plexippus during spring migration through Oklahoma, USA. Entomol Exp Appl 153:266–272CrossRefGoogle Scholar
  58. McPherson JE (1982) The Pentatomoidae (Hemiptera) of northeastern North America with emphasis on the fauna of Illinois. Southern Illinois University Press, CarbondaleGoogle Scholar
  59. Mead FW (1974) The wheel bug Arilus cristatus (Linnaeus) (Hemiptera:Reduviidae). Entomology Circular 143:1–2Google Scholar
  60. Monarch Larva Monitoring Project Accessed 22 April 2015
  61. Mueller EK, Baum KA (2014) Monarch–parasite interactions in managed and roadside prairies. J Insect Conserv 18:847–853CrossRefGoogle Scholar
  62. Nail K, Stenoien C, Oberhauser KS (2015) Immature monarch survival: effects of site characteristics, density, and time. Conservation Biology and Biodiversity (in press)Google Scholar
  63. Noyes JS (2015) Universal Chalcidoidea Database. World Wide Web electronic publication. Accessed 23 June 2015
  64. 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
  65. Oberhauser KS, Nail KR, Altizer S (2015) Lacewings, wasps, and flies—Oh My. In: Oberhauser KS, Nail KR, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic butterfly. Cornell University Press, Ithaca, pp 71–82Google Scholar
  66. Oberhuaser KS (2012) Citizen scientists document parasitism patterns over broad spatial and temporal scales. Am Entomol 58:19–22CrossRefGoogle Scholar
  67. Pierce AA, Altizer S, Chamberlain NL, Kronforst MR, de Roode JC (2015) Unraveling the mysteries of monarch migration and global dispersal through molecular genetic techniques. In: Oberhauser KS, Nail KR, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic butterfly. Cornell University Press, Ithaca, pp 201–220Google Scholar
  68. Pimentel D, Nagel WP, Madden JL (1963) Space-time structure of the environment and the survival of parasite-host systems. Am Nat 97:141–167CrossRefGoogle Scholar
  69. Pleasants J (2015) Monarch butterflies and agriculture. In: Oberhauser KS, Nail KR, Altizer SM (eds) Monarchs in a changing world: biology and conservation of an iconic butterfly. Cornell University Press, Ithaca, pp 169–178Google Scholar
  70. Pleasants JM, Oberhauser KS (2013) Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conserv Divers 6:135–144CrossRefGoogle Scholar
  71. Prysby MD (2004) Natural enemies and survival of monarch eggs and larvae. In: The monarch butterfly: biology and conservation. Cornell University Press, Ithaca. pp 27–38Google Scholar
  72. Prysby MD, Oberhauser KS (1999) Large scale monitoring of monarch populations. In: Hoth J, Pisanty I, Oberhauser K, Merino L, Price S (eds.) Proceedings of the North American conference on the monarch butterfly commission for environmental cooperation, Montreal, pp 379–384Google Scholar
  73. Prysby MD, Oberhauser KS (2004) Temporal and geographic variation in monarch densities: citizen scientists document monarch population patterns. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 9–20 Google Scholar
  74. Pyle RM (2015) Monarchs in the mist: new perspectives on monarch distribution in the Pacific Northwest. In: Oberhauser KS, Nail KR, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic butterfly. Cornell University Press, Ithaca, pp 236–246Google Scholar
  75. Radosavljevic A, Anderson RP (2014) Making better Maxent models of species distributions: complexity, overfitting and evaluation. J Biogeogr 41:629–643CrossRefGoogle Scholar
  76. Rafter JL, Agrawal AA, Preisser EL (2013) Chinese mantids gut toxic monarch caterpillars: avoidance of prey defence? Ecol Entomol 38:76–82CrossRefGoogle Scholar
  77. Ramsay G (1964) Overwintering swarms of the monarch butterfly (Danaus plexippus (L.)) in New Zealand. NZ Entomol 3:10–16CrossRefGoogle Scholar
  78. Rawlins JE, Lederhouse RC (1981) Developmental influences of thermal behavior on monarch caterpillars (Danaus plexippus): an adaptation for migration (Lepidoptera: Nymphalidae: Danainae). J Kansas Entomol Soc 54:387–408Google Scholar
  79. Rayor LS (2004) Effects of monarch larval host plant chemistry and body size on Polistes wasp predation. In: Monarch butterfly biology and conservation. Cornell University Press, Ithaca. pp. 39–46Google Scholar
  80. Redpath SM, Mougeot F, Leckie FM, Elston DA, Hudson PJ (2006) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecol Lett 9:410–418CrossRefPubMedGoogle Scholar
  81. Stapel JO, Ruberson JR, Gross HR, Lewis WJ (1997) Progeny allocation by the parasitoid Lespesia archippivora (Diptera: Tachinidae) in larvae of Spodoptera exigua (Lepidoptera: Noctuidae). Environ Entomol 26:265–271CrossRefGoogle Scholar
  82. Stenoien C, McCoshum SM, Caldwell W, De Anda A, Oberhauser KS (2015) New reports that monarch butterflies (Lepidoptera: Nymphalidae, Danaus plexippus Linnaeus) are hosts for a pupal parasitoid (Hymenoptera: Chalcidoidae, Pteromalus cassotis Walker). J Kans Entomol Soc 88:16–26CrossRefGoogle Scholar
  83. Stireman JO III, O’Hara JE, Wood DM (2006) Tachinidae: evolution, behavior, and ecology. Ann Rev Enotmol 51:525–555CrossRefGoogle Scholar
  84. Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc Lond B Biol Sci 278:1823–1830CrossRefGoogle Scholar
  85. Takagi M (1985) The reproductive strategy of the gregarious parasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae). Oecologia 68:1–6CrossRefGoogle Scholar
  86. Urquhart FA (1976) Found at last-monarchs winter home. Natl Geogr 150:161–173Google Scholar
  87. 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
  88. Van Nouhuys S, Hanski I (1999) Host diet affects extinctions and colonizations in a parasitoid metapopulation. J Anim Ecol 68:1248–1258CrossRefGoogle Scholar
  89. Van Nouhuys S, Hanski I (2002) Colonization rates and distances of a host butterfly and two specific parasitoids in a fragmented landscape. J Anim Ecol 71:639–650CrossRefGoogle Scholar
  90. Vidal O, Rendón-Salinas E (2014) Dynamics and trends of overwintering colonies of the monarch butterfly in Mexico. Biol Conserv 180:165–175CrossRefGoogle Scholar
  91. Walker F (1847) Characters of Undescribed Chalcidites Collected in North America by E. Doubleday, Esq., and Now in the British Museum. Ann Mag Nat Hist 19:392–398Google Scholar
  92. Wassenaar LI, Hobson KA (1998) Natal origins of migratory monarch butterflies at wintering colonies in Mexico: new isotopic evidence. Proc Natl Acad Sci 95:15436–15439CrossRefPubMedPubMedCentralGoogle Scholar
  93. Wilbur HM (1976) Life history evolution in seven milkweeds of the genus Asclepias. J Ecol 64:223–240CrossRefGoogle Scholar
  94. York HA, Oberhauser KS (2002) Effects of duration and timing of heat stress on monarch butterfly (Danaus plexippus) (Lepidoptera: Nymphalidae) development. J Kans Entomol Soc 75:290–298Google Scholar
  95. Zalucki MP (1982) Temperature and rate of development in Danaus plexippus L. and D. chrysippus L. (Lepidoptera:Nymphalidae). Aust J Entomol 21:241–246CrossRefGoogle Scholar
  96. Zalucki M, Kitching R (1982) Temporal and spatial variation of mortality in field populations of Danaus plexippus L. and D. chrysippus L. larvae (Lepidoptera: Nymphalidae). Oecologia 53:201–207CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Cornell UniversityIthacaUSA
  2. 2.Oklahoma State UniversityStillwaterUSA
  3. 3.University of MinnesotaMinneapolisUSA

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