Effects of the parasite, Ophryocystis elektroscirrha, on wing characteristics important for migration in the monarch butterfly

Andrew K. Davis 1  and Jacobus C. de Roode 2
  • 1 Odum School of Ecology, University of Georgia,, Athens, USA
  • 2 Emory University, Biology Dept.,, Atlanta, USA

Abstract

There is mounting evidence that the longterm declines of overwintering monarchs in Mexico are exacerbated by losses during the fall migratory journey. Infection with the protozoan, Ophryocystis elektroscirrha (OE), is known to negatively impact migration success. Here we examine how infections affect specific wing traits of monarchs that are important for migratory success. We used a collection of infected and uninfected monarchs reared under identical conditions, and from the (deceased) specimens, measured wing area (larger monarchs are known to have greater migratory success), wing color (the shade of orange pigmentation in monarchs is a known predictor of migration and flight ability), and the physical density of wings (a measure of wing mass per unit area). We also measured the tear-resistance of wings, using an apparatus that measured the force needed to cause a tear in the wing. Results showed no effect of OE on overall wing size, nor on the shade of orange pigmentation, but a clear effect on measures of physical density and tensile strength. Wings of infected monarchs weighed less per unit area (by 6%), and there was a 20% reduction in tear-resistance of wings. All results were qualitatively similar in a follow-up investigation using freshly-killed specimens. Collectively, this indicates infected monarchs are more prone to wing damage, which would be costly during long-distance migration. As such, this would be one more way in which OE infections reduce migratory success. Given the toll of OE to the monarch population, especially during migration, it would be prudent to focus conservation efforts on mitigating human activities that spread this disease.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • [1] Altizer S., Han B., Bartel R., Animal migrations and infectious disease risk, Science, 2011, 331, 296-302

  • [2] Risely A., Klaassen M., Hoye B.J., Migratory animals feel the cost of getting sick: A meta-analysis across species, Journal of Animal Ecology, 2018, 87(1), 301-14

  • [3] van Gils J.A., Munster V.J., Radersma R., Liefhebber D., Fouchier R.A.M., Klaassen M., Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus, Plos One, 2007, 2(1), 6

  • [4] Cornelius E., Davis A.K., Altizer S., How important are hemoparasites to migratory songbirds? Evaluating physiological measures and infection status in three neotropical migrants during stopover, Physiological and Biochemical Zoology, 2014, 87(5), 719-28

  • [5] Davis A.K., Can a blood-feeding ectoparasitic fly affect songbird migration? Examining body condition and fat reserves of 5 bird species in relation to hippoboscid fly parasitism, Ecological Parasitology and Immunology, 2015, 4 (2015), 7pp

  • [6] Garvin M.C., Szell C.C., Moore F.R., Blood parasites of Nearctic-Neotropical migrant passerine birds during spring trans-gulf migration: Impact on host body condition, Journal of Parasitology, 2006, 92(5), 990-6

  • [7] de Roode J.C., Chi J., Rarick R.M., Altizer S., Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus), Oecologia, 2009, 161(1), 67-75

  • [8] de Roode J.C., Yates A.J., Altizer S., Virulence-transmission trade-offs and population divergence in virulence in a naturally occuring butterfly parasite, Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(21), 7489-94

  • [9] de Roode J.C., Gold L.R., Altizer S., Virulence determinants in a natural butterfly-parasite system, Parasitology, 2007, 134, 657-68

  • [10] Bradley C.A., Altizer S., Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts, Ecology Letters, 2005, 8, 290-300

  • [11] Bartel R.A., Oberhauser K.S., de Roode J.C., Altizer S.M., Monarch butterfly migration and parasite transmission in eastern North America, Ecology, 2011, 92(2), 342-51

  • [12] Flockhart D.T.T., Dabydeen A., Satterfield D.A., Hobson K.A., Wassenaar L.I., Norris D.R., Patterns of parasitism in monarch butterflies during the breeding season in eastern North America, Ecological Entomology, 2018, 43(1), 28-36

  • [13] Thogmartin W.E., Diffendorfer J.E., Lopez-Hoffman L., Oberhauser K., Pleasants J., Semmens B.X., et al., Density estimates of monarch butterflies overwintering in central Mexico, Peerj, 2017, 5, 18

  • [14] Altizer S., Hobson K.A., Davis A.K., De Roode J.C., Wassenaar L.I., Do healthy monarchs migrate farther? Tracking natal origins of parasitized vs. uninfected monarch butterflies overwintering in Mexico, Plos One, 2015, 10(11), 14

  • [15] Altizer S.M., Oberhauser K., Brower L.P., Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies, Ecological Entomology, 2000, 25, 125-39

  • [16] Altizer S., Davis A.K., Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology, Evolution, 2010, 64(4), 1018-28

  • [17] Li Y., Pierce A.A., de Roode J.C., Variation in forewing size linked to migratory status in monarch butterflies, Animal Migration, 2016, 3(1), 27-34

  • [18] Dockx C., Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.), in Cuba, Biological Journal of the Linnean Society, 2007, 92(4), 605-16

  • [19] Davis A.K., Chi J., Bradley C.A., Altizer S., The redder the better: wing color predicts flight performance in monarch butterflies, Plos One, 2012, 7(7), e41323. doi:

    • Crossref
    • Export Citation
  • [20] Hanley D., Miller N.G., Flockhart D.T., Norris D.R., Forewing pigmentation predicts migration distance in wild-caught migratory monarch butterflies, Behavioral Ecology, 2013, 24(5), 1108-13

  • [21] Davis A.K., Intraspecific variation in wing colour is related to larval energy reserves in monarch butterflies (Danaus plexippus), Physiological Entomology, 2014, 39(3), 247-53

  • [22] Davis A.K., Holden M., Measuring intraspecific variation in flight-related morphology of monarch butterflies (Danaus plexippus): who has the best flying gear?, Journal of Insects, 2015, 2015(Article ID 591705), 6 pages

  • [23] Sternberg E.D., Lefevre T., Li J., de Castillejo C.L.F., Li H., Hunter M.D., et al., Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions, Evolution, 2012, 66(11), 3367-76

  • [24] Satterfield D.A., Davis A.K., Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings, Animal Migration, 2014, 2, 1-7

  • [25] Davis A.K., Wing color of monarch butterflies (Danaus plexippus) in eastern North America across life stages: migrants are ‘redder’ than breeding and overwintering stages, Psyche, 2009, DOI: 10.1155/2009/705780

  • [26] Sander S.E., Altizer S., De Roode J.C., Davis A.K., Genetic factors and host traits predict spore morphology for a butterfly pathogen, Insects, 2013, 4(3), 447-62

  • [27] Stavenga D.G., Stowe S., Siebke K., Zeil J., Arikawa K., Butterfly wing colours: scale beads make white pierid wings brighter, Proceedings of the Royal Society of London Series B, 2004, 271(1548), 1577-84

  • [28] Wijnen B., Leertouwer H.L., Stavenga D.G., Colors and pterin pigmentation of pierid butterfly wings, Journal of Insect Physiology, 2007, 53(12), 1206-17

  • [29] Wilts B.D., Pirih P., Stavenga D.G., Spectral reflectance properties of iridescent pierid butterfly wings, Journal of Comparative Physiology A, 2011, 197(6), 693-702

  • [30] Steppan S.J., Flexural stiffness patterns of butterfly wings (Papilionidea), Journal of Research on the Lepidoptera, 2000, 35, 61-77

  • [31] Johnson H., Solensky M.J., Satterfield D.A., Davis A.K., Does skipping a meal matter to a butterfly’s appearance? Effects of larval food stress on wing morphology and color in monarch butterflies, Plos One, 2014, 9(4), e93492. doi:

    • Crossref
    • Export Citation
  • [32] Inamine H., Ellner S.P., Springer J.P., Agrawal A.A., Linking the continental migratory cycle of the monarch butterfly to understand its population decline, Oikos, 2016, 125(8), 1081-91

  • [33] Badgett G., Davis A.K., Population trends of monarchs at a northern monitoring site: analyses of 19 years of fall migration counts at Peninsula Point, MI, Annals of the Entomological Society of America, 2015, 108(5), 700-6

  • [34] Davis A.K., Dyer L., Long-term trends in eastern North American monarch butterflies: a collection of studies focusing on spring, summer, and fall dynamics, Annals of the Entomological Society, 2015, 108(5), 661-3

  • [35] Agrawal A.A., Inamine H., Mechanisms behind the monarch’s decline, Science, 2018, 360(6395), 1294-6

  • [36] Howard E., Davis A.K., Mortality of migrating monarch butterflies from a wind storm on the shore of Lake Michigan, USA, Journal of Research on the Lepidoptera, 2012, 45, 49-54

  • [37] McKenna D.D., McKenna K.M., Malcolm S.B., Berenbaum M.R., Mortality of lepidoptera along roadways in central Illinois, Journal of the Lepidopterists’ Society, 2001, 55(2), 63-8

  • [38] Borland J., Johnson C.C., Crumpton III T.W., Thomas M., Altizer S., Oberhauser K. Characteristics of fall migratory monarch butterflies, Danaus plexippus, in Minnesota and Texas. In: Oberhauser K, Solensky M, editors. The monarch butterfly, Biology and conservation. Ithaca, NY: Cornell University Press; 2004. p. 97-104.

  • [39] McCord J.W., Davis A.K., Characteristics of monarch butterflies (Danaus plexippus) that stopover at a site in coastal South Carolina during fall migration, Journal of Research on the Lepidoptera, 2012, 45, 1-8

  • [40] Combes S.A., Crall J.D., Mukherjee S., Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success, Biology Letters, 2010, 6(3), 426-9

  • [41] Altizer S.M., Oberhauser K., Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus), Journal of Invertebrate Pathology, 1999, 74, 76-88

  • [42] Satterfield D.A., Wright A.E., Altizer S., Lipid reserves and immune defense in healthy and diseased migrating monarchs Danaus plexippus, Current Zoology, 2013, 59(3), 393-402

  • [43] Vickerman D., Michels A., Burrowes P.A., Levels of infection of migrating monarch butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) by the parasite Ophryocystis elektroscirrha (Neogregarinida: Ophryocystidae), and evidence of a new mode of spore transmission between adults, Journal of the Kansas Entomological Society, 1999, 72(1), 124-8

  • [44] Brower L.P., Taylor O.R., Williams E.H., Slayback D.A., Zubieta R.R., Ramirez M.I., Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk?, Insect Conservation and Diversity, 2012, 5(2), 95-100

  • [45] Oberhauser K., Wiederholt R., Diffendorfer J.E., Semmens D., Ries L., Thogmartin W.E., et al., A trans-national monarch butterfly population model and implications for regional conservation priorities, Ecological Entomology, 2017, 42(1), 51-60

  • [46] Pleasants J., 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 Conservation and Diversity, 2017, 10(1), 42-53.

OPEN ACCESS

Journal + Issues

Animal Migration publishes cutting-edge research on the biology of migratory species. It covers all aspects of migratory biology, from genetics and physiology to ecosystem-level interactions between migrants and their environment and everything in between. Migration is a world-wide phenomenon, hence authors from all over the globe are encouraged to submit articles to this OA journal.

Search