Understanding the impact of plant–arthropod interactions, pollination, and canopy light on the rare orchid, small whorled pogonia (Isotria medeoloides)

  • Lisa HorthEmail author


Recent work has warned of a global crisis for terrestrial orchids and an urgent need for conservation. Pollinator declines have been documented globally, which may exacerbate the pollination limitations orchids experience. Small whorled pogonia (Isotria medeoloides) (Pursh) Raf. is a North American terrestrial orchid considered vulnerable by the International Union for the Conservation of Nature, threatened in Canada and USA, and endangered in 20 states. Like many orchids, it has specialized habitat needs and fragmented populations. Here, plants were monitored diurnally and nocturnally throughout the flowering period to evaluate arthropod activity that might impact pollination. Ultraviolet photographs and spectrophotometric data were collected on flowers. Canopy light penetrance was measured at plants. Seed capsule production was evaluated over time. In sum, 41 flowers were monitored for > 300 h, resulting in > 140,000 photographic frames of compiled video. In this extensive monitoring, 33 plant–arthropod interactions were detected, only one likely to facilitate self-pollination, and none that facilitated outcrossing. UV absorbance was identified on petals and sepals, which contrasted starkly with whorl UV reflectance, a previously undescribed form of floral display visible to pollinators. Flowering plants grew in higher light than vegetative ones. Capsule production was highly variable over time, making the species vulnerable to 'bad years' and low effective population size, given the low genetic diversity previously identified, and lack of outcrossing detected here. Imminent attention is warranted for species-level protection, consistent with needs of other terrestrial orchids.


Conservation Endangered species Inbreeding Istoria Orchid Plant–insect interactions Small population 



Thanks to USFWS for funding this research, J. Applegate and R. Floyd for site access and field accommodation, D. Waller and S. Droege for arthropod identification assistance, and two anonymous reviewers for helpful comments.

Author contributions

LH conceived, designed and executed this study and wrote the manuscript. No other person is entitled to authorship.


  1. Argue CL (2012) The pollination biology of North American orchids: 2 North of Florida and Mexico. Springer, New York, pp 167–184CrossRefGoogle Scholar
  2. Barrett S (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284CrossRefGoogle Scholar
  3. Brook BW, O’Grady JJ, Chapman AP, Burgman MA, Akcakaya HR, Frankham R (2000) Predictive accuracy of population viability analysis in conservation biology. Nature 404:385–387CrossRefGoogle Scholar
  4. Brumback WE, Cairns S, Sperduto MS, Fyler CW (2011) Response of an Istoria medeoloides population to canopy thinning. Northeast Nat 18(2):185–196CrossRefGoogle Scholar
  5. Caballero-Villalobos L, Silva-Arias GA, Buzatto CR, Nervo MH, Singer RB (2017) Generalized food-deception pollination in four Cattleya (Orchidaceae: Laeliinae) species from Southern Brazil. Flora 234:195–206CrossRefGoogle Scholar
  6. Cairns S (2001) Isotria medeoloides recovery activities in New Hampshire. U.S Fish and Wildlife Service, HadleyGoogle Scholar
  7. Cameron KM (2003) Vanilloideae. In: Pridgeon A, Cribb P, Chase MW, Rasmussen F (eds) Genera Orchidacearum. Oxford University Press, Oxford, pp 281–334Google Scholar
  8. Cameron KM (2009) On the value of nuclear and mitochondrial gene sequences for reconstruction the phylogeny of vanilloid orchids (Vanilloideae, Orchidaceae). Ann Bot 104:377–385CrossRefGoogle Scholar
  9. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. PNAS USA 108(2):662–667CrossRefGoogle Scholar
  10. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  11. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796CrossRefGoogle Scholar
  12. Cheng J, Shi J, Shangguan F-Z, Dafni A, Deng Z-H, Luo Y-B (2009) The pollination of a self-incompatible, food-mimic orchid, Coelogyne fimbriata (Orchidaceae) by female Vespula wasps. Ann Bot 104:565-571CrossRefGoogle Scholar
  13. Chittka L (1996) Optimal sets of color receptors and color opponent systems for coding of natural objects in insect vision. J Theor Biol 181:179–196CrossRefGoogle Scholar
  14. Darwin CR (1862) On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. John Murray, LondonGoogle Scholar
  15. Darwin CR (1876) The effects of cross and self-fertilization in the vegetable kingdom. John Murray, LondonCrossRefGoogle Scholar
  16. Devlin E (2007) Geographic distribution of genetic variation in the rare orchid Isotria medeoloides. Student thesis. Colby College, Waterville ME pp 1-35Google Scholar
  17. Dressler R (1993) Phylogeny and classification of the orchid family. Cambridge University Press, CambridgeGoogle Scholar
  18. Gómez JM, Torices R, Lorite J, Klingenberg CP, Perfectti F (2016) The role of pollinators in the evolution of corolla shape variation, disparity and integration in a highly diversified plant family with a conserved floral bauplan. Ann Bot 117(5):889–904CrossRefGoogle Scholar
  19. Goodwillie C, Kalisz S, Eckert C (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36:47–79CrossRefGoogle Scholar
  20. Gregory LL (1988) Small whorled pogonia, Isotria medeoloides (Pursh) Raf., in Maine and its relevance to the Critical Areas Program. Planning report No. 24, Critical Areas Program, State Planning Office, Augusta, MEGoogle Scholar
  21. Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142(1):75–84CrossRefGoogle Scholar
  22. Herrera J (2005) Flower size variation in Rosmarinus officinalis. Individuals, populations and habitats. Ann Bot 95:431–437CrossRefGoogle Scholar
  23. Herrera CM, Pellmyer O (2002) Plant animal interactions: An evolutionary approach. Wiley- Blackwell, HobokinGoogle Scholar
  24. Horth L, Campbell L, Bray R (2014) Wild bees preferentially visit Rudbeckia flower heads with exaggerated ultraviolet absorbing floral guides. Bio Open 3:221–230CrossRefGoogle Scholar
  25. Ingvarsson P (2007) A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evol 56:2368–2373CrossRefGoogle Scholar
  26. Jackson RR, Pollard SD, Nelson XJ, Edwards GB, Barrion AT (2001) Jumping spiders (Araneae: Salticidae) that feed on nectar. J. Zool London 255:25–29CrossRefGoogle Scholar
  27. Kalisz S, Horth L, McPeek MA (1997) Fragmentation and the role of seed banks in promoting persistence in isolated populations of Collinsia verna. In: Schwartz, M.W. (ed) Conservation in highly fragmented landscapes. Springer, BostonGoogle Scholar
  28. Knapp WK, Wiegand R (2014) Orchid (Orchidaceae) decline in the Catoctin Mountains, Frederick Country, Maryland as documented by a long-term data set. Biodivers Conserv 23(8):1965–1976CrossRefGoogle Scholar
  29. 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. PNAS 113(1):140–145CrossRefGoogle Scholar
  30. Koopowitz H (2001) Orchids and their conservation. Portland Timber Press, PortlandGoogle Scholar
  31. Krupnick GA, McCormick MK, Mirenda T, Whigham DF (2013) The status and future of orchid conservation in North America. Ann Mo Bot Gard 99:180–198CrossRefGoogle Scholar
  32. Kull T, Hutchings MJ (2006) A comparative analysis of decline in the distribution ranges of orchid species in Estonia and the United Kingdom. Biol Conserv 129(1):31–39CrossRefGoogle Scholar
  33. Lacy R (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection and population subdivision. Cons Biol 1:143–158CrossRefGoogle Scholar
  34. Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40CrossRefGoogle Scholar
  35. Lloyd DG (1979) Some reproductive factors affecting the selection of self-fertilization in plants. Am Nat 113:67–79CrossRefGoogle Scholar
  36. Luer CA (1975) The Native Orchids of the United States and Canada, excluding FL. New York Botanical Garden, BronxGoogle Scholar
  37. Martinelli G, Moraes MA (2013) Livro vermelho da flora do Brasil. CNC-Flora pp 1100 ISBN: 978 85 88742 58 1Google Scholar
  38. McCormick MK, Jacquemyn H (2014) What constrains the distribution of orchid populations? New Phytol 202(2):392–400CrossRefGoogle Scholar
  39. Mehrhoff LA (1983) Pollination in the genus Istoria (Orchidaceae). Amer J Bot 70:1444–1453CrossRefGoogle Scholar
  40. Menzel M, Sletvold N, Ågren J, Hansson B (2015) Inbreeding affects gene expression differently in two self-incompatible Arabidopsis lyrata populations with similar levels of inbreeding depression. Mol Biol Evol 32:2036–2047CrossRefGoogle Scholar
  41. Menges E (1992) Stochastic modeling of extinction in plant populations. In: Fiedler PL, Jain SK (eds) Conservation Biology. Springer, Boston, pp 253–275CrossRefGoogle Scholar
  42. Menges E (2000) Population viability analyses in plants: challenges and opportunities. TREE 15(2):51–55Google Scholar
  43. Montgomery AD (2014) Predicting threatened orchid (Isotria medeoloides [Pursh] Raf.) habitat in the southern Appalachian Region using Maxent. ProQuest LLC, pp 186Google Scholar
  44. Nilsson L (1992) Long pollinia on eyes: hawk-moth pollination of Cynorkis uniflora Lindley (Orchidaceae) in Madagascar. Bot Jour Linn Soc 109:145–160CrossRefGoogle Scholar
  45. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  46. Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 18:121–133CrossRefGoogle Scholar
  47. Pansarin ER, de Barros F (2008) Taxonomic notes of Pogonieae (Orchidaceae): Cleistesiopsis, a new genus segregated from Cleistes, and description of two new South American species, Cleistes batistana and C. elongata. Kew Bull 63:441–448CrossRefGoogle Scholar
  48. Pansarin ER, Salatino A, Pansarin LM, Sazima M (2012) Pollination systems in Pogonieae (Orchidaceae: Vanilloideae): A hypothesis of evolution among reward and rewardless flowers. Flora (Jena) 207:849–861CrossRefGoogle Scholar
  49. Pansarin ER, Aguiar JMRVB, Pansarin LM (2014) Floral biology and histochemical analysis of Vanilla edwallii Hoehne (Orchidaceae: Vanilloideae): an orchid pollinated by Epicharis (Apidae: Centridini). Plant Species Biol 29:242–252CrossRefGoogle Scholar
  50. Pedersen HA (1995) Anthecological observations on Dendrochilum longibracteatum, a species pollinated by facultatively anthophilous insects. Lindleyana 10:19–28Google Scholar
  51. Primack RB (2010) Essentials of Conservation Biology, 5th edn. Sinauer Associates, Sunderland, pp 250–255Google Scholar
  52. Robertson JL, Wyatt R (1990) Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution 44:121–133CrossRefGoogle Scholar
  53. Robertson AW, Kelly D, Ladley JJ (2011) Futile selfing in the trees Fuchsia excorticata (Onagraceae) and Sophora microphylla (Fabaceae): inbreeding depression over 11 years. Int J Plant Sci 172(2):191–198CrossRefGoogle Scholar
  54. Romero GA (1981) Cattleya violacea hosts a flower spider. Amer Orchid Soc Bull 50(1):28–29Google Scholar
  55. Sicard A, Lenhard M (2011) The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann of Bot 107:1433–1443CrossRefGoogle Scholar
  56. Singer RB (2002) The pollination biology of Sauroglossum elatum Lindl. (Orchidaceae: Spiranthinae): moth-pollination and protandry in netotropical Spiranthinae. Bot Jour Linn Soc 138(1):9-16CrossRefGoogle Scholar
  57. Sorenson JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037CrossRefGoogle Scholar
  58. Stebbins GL (1957) Self fertilization and population variability in higher plants. Am Nat 91:337–354CrossRefGoogle Scholar
  59. Stebbins GL (1974) Flowering plants: evolution above the species level. Harvard Univ Press, CambridgeCrossRefGoogle Scholar
  60. Stone JL (2006) AFLP fingerprints of the rare orchid Isotria medeoloides suggest little genetic variation within or among populations. In: Section 2: Summary Small Whorled Pogonia Work (E-2-19), Maine Natural Areas Program report to the U.S. Fish and Wildlife Service Hadley, MA pp 5Google Scholar
  61. Stone JL, Crystal PA, Devlin EE, Downer Downer RH, Cameron DS (2012) Highest genetic diversity at the northern range limit of the rare orchid Isotria medeoloides. Heredity 109:215–221CrossRefGoogle Scholar
  62. Swarts ND, Dixon KW (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:543–556CrossRefGoogle Scholar
  63. The IUCN Red List of Threatened Species. Version 2018-1. Accessed 22 Aug 2018
  64. Treher A, Sharman J, Frances A, Poff K (2015) Istoria medeoloides. The IUCN Red List of Threatened Species 2015: e.T64176265215480Google Scholar
  65. USFWS (1980) Proposal to determine Isotria medeoloides (small whorled pogonia) to be an Endangered Species. Fed Regis 45(178):59909–59914Google Scholar
  66. USFWS (1982) Determination of Isotria medeoloides (small whorled pogonia) to be an endangered species. Fed Regis 47:39827–39831Google Scholar
  67. USFWS (1992) Small Whorled Pogonia (Isotria medeoloides) Recovery Plan, first revision. USFWS Region Five, Newton Corner MA, p 77Google Scholar
  68. USFWS (1994) Final rule to reclassify the plant Isotria medeoloides (small whorled pogonia) from endangered to threatened. Fed Reg 59:50852–50857Google Scholar
  69. USFWS (2007) Initiation of a 5-year review of ten listed northeastern species. Fed Reg 72:4018–4019Google Scholar
  70. USFWS (1985) Small whorled pogonia recovery plan. Newton Corner MA pp 38Google Scholar
  71. USFWS (2008) Small whorled pogonia (Isotria medeoloides). 5-year review: Summary and evaluation. USFWS, NE Field Office, Concord NH. pp 25Google Scholar
  72. van Der Cingel NA (2001) An atlas of orchid pollination: European orchids 1st edn. pp 260. CRC Press Taylor & Francis, Milton ParkGoogle Scholar
  73. van der Pijl L, Dodson CH (1966) Orchid flowers: their pollination and evolution. University of Miami Press, Coral GablesGoogle Scholar
  74. Vitt P, Campbell CS (1997) Reproductive biology of Isotria medeoloides (Orchidaceae). Rhodora 99(897):56–63Google Scholar
  75. Vogt-Schilb H, Munoz F, Franck R, Schatz B (2015) Recent declines and range changes of orchids in Western Europe (France, Belgium and Luxembourg). Biol. Cons. 190:133–141CrossRefGoogle Scholar
  76. Waser NM, Price MV (1983) Pollinator behaviour and natural selection for flower colour in Delphinium nelsonii. Nature 302:422–424CrossRefGoogle Scholar
  77. Waser NM, Price MV (1985) The effect of nectar guides on pollinator preference: Experimental studies with a montane herb. Oecologia 67(1):121–126CrossRefGoogle Scholar
  78. Weakley AS, Ludwig JC, Townsend JF (2012) Flora of Virginia. BRIT Press, Fort Worth, p 1554Google Scholar
  79. Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton, NJ USACrossRefGoogle Scholar
  80. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159Google Scholar
  81. Zhang Z-Q, Li Q-J (2008) Autonomous selfing provides reproductive assurance in an alpine ginger Roscoea schneideriana (Zingiberaceae). Ann Bot 102:531–538CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of BiologyOld Dominion UniversityNorfolkUSA

Personalised recommendations