Journal of Plant Research

, Volume 131, Issue 4, pp 599–610 | Cite as

Delayed selfing ensures reproductive assurance in Utricularia praeterita and Utricularia babui in Western Ghats

  • Anjali Chaudhary
  • S. R. Yadav
  • Rajesh TandonEmail author
Regular Paper


Numerous bladderwort (Utricularia) species are distributed worldwide, but their reproductive biology is rarely investigated. Bladderworts are known to depend on tiny organisms to meet a significant proportion of their energy requirement by trapping them in bladders. However, information on the extent of their reliance on insects for pollination success is limited. We examined the reproductive strategy of two Utricularia species viz. Utricularia praeterita and U. babui, endemic to Western Ghats, India. The main aspects of the investigation involved floral biology, breeding system, pollination mechanism, and reproductive success. Flowers of both the species are structured for outbreeding through entomophilous floral suites, herkogamy, protandrous dichogamy and sensitive lobes of the stigma. With nearly 65% natural fruit-set, both the species appeared to be sufficiently open-pollinated. However, pollinators failed to show in plants of U. praeterita while in U. babui there was an apparent mismatch between the extent of fruit-set and pollinator visits. The study demonstrated that in the absence/insufficient visits of pollinators, the two species resort to autonomous selfing. In U. babui, denser patches of plants appeared to be crucial for attracting the pollinators. Both species are self-compatible, and reproductive success is predominantly achieved by delayed autonomous selfing. The sensitive stigma in the species fails to prevent selfing due to diminished herkogamy during the late anthetic stages. It is inferred that in the pollinator-limited environment, delayed selfing contributes to absolute natural fecundity in U. praeterita, while it produces a mixed progeny in U. babui.


Bladderworts Herkogamy Melittophily Pollinator limitation Protandry Thigmosensitive stigma 



Financial assistance received from the Research and Development Grant (Grant no: RC/2015/9677) to RT is gratefully acknowledged. SRY thanks the University Grants Commission (UGC) for the BSR faculty fellowship awarded to him.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Alkhalaf IA, Hübener T, Porembski S (2009) Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: the role of planktonic algae. Flora 204:700–708CrossRefGoogle Scholar
  2. Araki S, KadonoY (2003) Restricted seed contribution and clonal dominance in a free-floating aquatic plant Utricularia australis R. Br. in southwestern Japan. Ecol Res 18:599–609CrossRefGoogle Scholar
  3. Armbruster WS, Mulder CP, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae sl). Am J Bot 89:37–49CrossRefPubMedGoogle Scholar
  4. Clivati D, Cordeiro GD, Płachno BJ, Miranda VFO (2014) Reproductive biology and pollination of Utricularia reniformis A. St.-Hil. (Lentibulariaceae). Plant Biol 16:677–682CrossRefPubMedGoogle Scholar
  5. Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32–46CrossRefPubMedGoogle Scholar
  6. Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest, CambridgeGoogle Scholar
  7. De Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends Ecol Evol 8:321–325CrossRefPubMedGoogle Scholar
  8. Eckhert C, Schaeffer A (1998) Does self-pollination provide reproductive assurance in Aquilegia canadensis (Ranunculaceae)? Am J Bot 85:919–924CrossRefGoogle Scholar
  9. Feinsinger P, Tiebout HM III, Young BE (1991) Do tropical bird-pollinated plants exhibit density-dependent interactions? field experiments. Ecology 72:1953–1963CrossRefGoogle Scholar
  10. Fetscher AE, Kohn JR (1999) Stigma behavior in Mimulus aurantiacus (Scrophulariaceae). Am J Bot 86:1130–1135CrossRefPubMedGoogle Scholar
  11. Fineran BA (1985) Glandular trichomes in Utricularia: a review of their structure and function. Israel J Bot 34:295–330Google Scholar
  12. Fisher RA (1941) Average excess and average effect of a gene substitution. Ann Eugen 11:53–63CrossRefGoogle Scholar
  13. Fleischmann A (2012) The new Utricularia species described since Peter Taylor’s monograph. Carniv Plant Newsl 41:67–76Google Scholar
  14. Friedman J, Hart KS, Bakker MCD (2017) Losing one’s touch: evolution of the touch-sensitive stigma in the Mimmulus guttatus species complex. Am J Bot 104:335–341CrossRefPubMedGoogle Scholar
  15. Heslop-Harrison J, Heslop-Harrison Y (1970) Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol 45:115–120CrossRefPubMedGoogle Scholar
  16. Hobbhahn N, Küchmeister H, Porembski S (2006) Pollination biology of mass flowering terrestrial Utricularia species (Lentibulariaceae) in the Indian Western Ghats. Plant Biol 8:791–804CrossRefPubMedGoogle Scholar
  17. Husband BC, Barrett SC (1992) Effective population size and genetic drift in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 46:1875–1890CrossRefPubMedGoogle Scholar
  18. IBM Corp. Released (2013) IBM® SPSS® Amos™ Statistics for Windows, Version 22.0. IBM Corp, New YorkGoogle Scholar
  19. Janarthanam MK, Henry AN (1992) Bladderworts of India. The Seshan Printers, CoimbatoreGoogle Scholar
  20. Jérémie J L (Lentibulariaceae (1989) Autogamie dans le genre Utricularia. Bull du Museum Nat D’Histoire Nat Sect B Adansonia 1:17–28Google Scholar
  21. Jin XF, Ye ZM, Wang QF, Yang CF (2015) Relationship of stigma behaviors and breeding system in three Mazus (Phrymaceae) species with bilobed stigma. J Syst Evol 53:259–265CrossRefGoogle Scholar
  22. Juncosa AM, Webster BD (1989) Pollination in Lupinus nanus subsp. latifolius (Leguminosae). Am J Bot 76:59–66CrossRefGoogle Scholar
  23. Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942CrossRefGoogle Scholar
  24. Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247CrossRefPubMedGoogle Scholar
  25. Kausik SB, Raju MVS (1955) A contribution to the floral morphology and embryology of Utricularia reticulata Smith. Proc Plant Sci 41.4:155–166Google Scholar
  26. Khanduri P, Chaudhary A, Uniyal PL, Tandon R (2014) Reproductive biology of Willisia arekaliana (Podostemaceae), a freshwater endemic species of India. Aquat Bot 119:57–65CrossRefGoogle Scholar
  27. Khosla C, Shivanna KR, Mohan Ram HY (1998) Pollination in the aquatic insectivore Utricularia inflexa var. stellaris. Phytomorphology 48:417–425Google Scholar
  28. Knuth P (1899) Handbuch der Blütenbiologie. II. Wilhelm Engelmann, LeipzigGoogle Scholar
  29. Koller-Peroutka M, Lendl T, Watzka M, Adlassnig W (2015) Capture of algae promotes growth and propagation in aquatic Utricularia. Ann Bot 115:227–236Google Scholar
  30. Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74:2145–2160CrossRefGoogle Scholar
  31. Lekhak MM, Yadav SR (2012) Herbaceous vegetation of threatened high altitude lateritic plateau ecosystems of Western Ghats, southwestern Maharashtra, India. Rheedea 22:39–61Google Scholar
  32. Llorens C, Argentina M, Bouret Y, Marmottant P, Vincent O (2012) A dynamical model for the Utricularia trap. J Royal Soc Interface 9:3129–3139CrossRefGoogle Scholar
  33. Lloyd DG (1992) Self-and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380CrossRefGoogle Scholar
  34. Lloyd DG, Schoen DJ (1992) Self-and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci 153:358–369CrossRefGoogle Scholar
  35. Mamut J, Li B, Tan DY (2014) Protogyny and delayed autonomous self-pollination in the desert herb Zygophyllum macropterum (Zygophyllaceae). J Syst Evol 52:75–83CrossRefGoogle Scholar
  36. Mustajärvi K, Siikamäki P, Rytkönen S, Lammi A (2001) Consequences of plant population size and density for plant–pollinator interactions and plant performance. J Ecol 89:80–87CrossRefGoogle Scholar
  37. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  38. Nayar MP (1996) Hot spots of endemic plants of India, Nepal and Bhutan. TBGRI, ThiruvananthapuramGoogle Scholar
  39. Newcombe FC (1922) Significance of the behavior of sensitive stigmas. Am J Bot 9:99–120CrossRefGoogle Scholar
  40. Płachno BJ, Świątek P (2011) Syncytia in plants: cell fusion in endosperm-placental syncytium formation in Utricularia. (Lentibulariaceae) Protoplasma 248:425–435CrossRefPubMedGoogle Scholar
  41. Płachno BJ, Świątek P (2012) Actin cytoskeleton in the extra-ovular embryo sac of Utricularia nelumbifolia (Lentibulariaceae). Protoplasma 249:663–670CrossRefPubMedGoogle Scholar
  42. Płachno BJ, Łukaszek M, Wołowski K, Adamec L, Stolarczyk P (2012) Aging of Utricularia traps and variability of microorganisms associated with that microhabitat. Aquat Bot 97:44–48CrossRefGoogle Scholar
  43. Płachno BJ, Świątek P, Sas-Nowosielskan H, Kozieradzka-Kiszkurno M (2013) Organisation of the endosperm and endosperm–placenta syncytia in bladderworts (Utricularia, Lentibulariaceae) with emphasis on the microtubule arrangement. Protoplasma 250:863–873CrossRefPubMedGoogle Scholar
  44. Płachno BJ, Stpiczyńska M, Davies KL, Świątek P, de Miranda VFO (2017) Floral ultrastructure of two Brazilian aquatic-epiphytic bladderworts: Utricularia cornigera Studnička and U. nelumbifolia Gardner (Lentibulariaceae). Protoplasma 254:353–366CrossRefPubMedGoogle Scholar
  45. Punchihewa RWK (1984) Anthophilous insects and the pollination ecology of Asclepias syriaca. L. and Asclepias incarnata L. in southern Ontano. Dissertation, University of GuelphGoogle Scholar
  46. Schoen DJ, Ashman TL (1995) The evolution of floral longevity: resource allocation to maintenance versus construction of repeated parts in modular organisms. Evolution 1:131–139CrossRefGoogle Scholar
  47. Schoen DJ, Brown AH (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc Natl Acad Sci 88:4494–4497CrossRefPubMedPubMedCentralGoogle Scholar
  48. Schoen DJ, Morgan MT, Bataillon T (1996) How does self-pollination evolve? inferences from floral ecology and molecular genetic variation. Philos Trans Royal Soc B 351:1281–1290CrossRefGoogle Scholar
  49. Srithongchuay T, Bumrungsri S, Sripao-raya E (2008) The pollination ecology of the late-successional tree, Oroxylum indicum (Bignoniaceae) in Thailand. J Trop Ecol 24:477–484CrossRefGoogle Scholar
  50. Tandon R, Manohara TN, Nijalingappa BHM, Shivanna KR (2001) Pollination and pollen-pistil interaction in Oil Palm, Elaeis guineensis. Ann Bot 87:831–838CrossRefGoogle Scholar
  51. Taylor P (1989) The genus Utricularia—a taxonomic monograph. Kew Bull Addit Ser 14:1–724Google Scholar
  52. Vikas, Gautam M, Tandon R, Mohan Ram HY (2009) Pollination ecology and breeding system of Oroxylum indicum (Bignoniaceae) in the foothills of the Western Himalaya. J Trop Ecol 25:93–96CrossRefGoogle Scholar
  53. Watve A (2011) Utricularia praeterita. The IUCN red list of threatened species. Accessed 12 Dec 2017
  54. Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in Angiosperms II. Herkogamy. New Zeal J Bot 24:163–178CrossRefGoogle Scholar
  55. Westermeier AS, Fleischmann A, Müller K, Schäferhoff B, Rubach C, Speck T, Poppinga S (2017) Trap diversity and character evolution in carnivorous bladderworts (Utricularia, Lentibulariaceae). Sci Rep 7:1–24CrossRefGoogle Scholar
  56. Yadav SR, Sardesai MM, Gaikwad SP (2000) Two new species of Utricularia L. (Lentibulariaceae) from Peninsular India. Rheedea 10:107–112Google Scholar
  57. Yadav SR, Sardesai MM, Gaikwad SP (2005) A New Species of Utricularia L. (Lentibulariaceae) from the Western Ghats, India. Rheedea 15:71–73Google Scholar
  58. Yamamoto L, Kadono Y (1990) A study on the reproductive biology of aquatic Utricularia species in southwestern Japan. Acta phytotaxon Geobot 41:189–200Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BotanyUniversity of DelhiNew DelhiIndia
  2. 2.Department of BotanyShivaji UniversityKolhapurIndia

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