Advertisement

Arthropod-Plant Interactions

, Volume 13, Issue 6, pp 865–874 | Cite as

Essential dependence on wild pollination service: a medicinal plant under threat Minthostachys verticillata (Lamiaceae)

  • Evangelina Glinos
  • Eugenia Condat
  • Pablo Mulieri
  • Lorena AshworthEmail author
Original Paper

Abstract

Minthostachys (Benth.) Spach (Lamiaceae) is one of the most important genus in Andean folk medicine. Minthostachys species are harvested in the wild rather than cultivated. Beyond the key socio-cultural role of these species, there have been no studies to evaluate their reproductive requirements as part of their conservation. M. verticillata is a gynodioecious species endemic from Argentina, whose populations are threatened because of overexploitation and habitat loss. The level of reproductive dependence on animal pollination, the diversity and composition of floral visitors’ assemblages, flower morphology, fruit and seed set and the progeny vigour of female and hermaphrodite plants were evaluated. Both sex morphs rely absolutely on animal pollination for seed production and were visited by a similar and diverse assemblage of insects (Diptera, Lepidoptera and Hymenoptera); however, the tachinind fly Ptilodexia cf. cingulipes was the main pollinator. Female plants have smaller flowers, higher fruit set, fruits with more seeds, and a higher percentage of seed germination than hermaphrodites. There were no differences in growth rate and biomass of seedlings produced by female and hermaphrodite plants. Lower reproductive success of hermaphrodites could be due to self-incompatibility or inbreeding depression. These results suggest that it is a fragile system where hermaphrodite plants perform mainly as pollen donors, females as seed producers, and seed production relies almost exclusively on a native tachinid species, which is furthermore parasitoid. This knowledge can be applied in conservation programs in order to promote the sexual reproduction and so the conservation in situ of this key medicinal resource.

Keywords

Minthostachys verticillata Functional dioecy Gynodioecy Reproductive dependence Sexual dimorphism Tachinid pollination service 

Notes

Acknowledgements

We are very grateful to Delia Susana Avalos and Moira Battan for identifying some Diptera specimens and to the authorities of La Quebrada and Los Manantiales nature reserves for allowing us to work there. We thank Ruben La Rossa and Marcela Gonzalez (INTA) for permitting the examination of Ptilodexia cf cingulipes type, and Marcelo Gritti for his technical assistance in editing the photographs. We would also like to thank María Pastor for her help with field work, Gabrielle McLellan for reviewing the English, and two anonymous reviewers and the Editor Dr. Heikki M. Hokkanen who improved the reading of the manuscript. E. Glinos holds a fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) and L. Ashworth and P. Mulieri are researchers from the same institution. This study was supported by a Grant from CONICET [PIP 00371] and Programa Iberoamericano de Ciencia y Tecnología para el Desarrollo RED CYTED-SEPODI (417RT0527).

References

  1. Ashman TL (1994) Reproductive allocation in hermaphrodite and female plants of Sidalcea oregana ssp. spicata (Malvaceae) using four currencies. Am J Bot 81(4):433–438Google Scholar
  2. Ashman TL (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81(9):2577–2591Google Scholar
  3. Ashman TL, Stanton M (1991) Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregano ssp. Spicata (Malvaceae). Ecology 72(3):993–1003Google Scholar
  4. Ashworth L, Quesada M, Casas A, Aguilar R, Oyama K (2009) Pollinator-dependent food production in Mexico. Biol Conserv 142:1050–1057Google Scholar
  5. Asikainen E, Mutikainen P (2005) Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Ann Bot 95:879–886PubMedPubMedCentralGoogle Scholar
  6. Banchio E, Zygadlo J, Valladares GR (2005) Quantitative variations in the essential oil of Minthostachys mollis (Kunth.) Griseb. in response to insects with different feeding habits. J Agric Food Chem 53(17):6903–6906PubMedGoogle Scholar
  7. Barboza GE, Cantero JJ, Núñez C, Pacciaroni A, Ariza-Espinar L (2009) Medicinal plants: a general review and a phytochemical and ethnopharmacological screening of the native Argentine Flora. Kurtziana 34:7–365Google Scholar
  8. Barrett SCH (2002) Sexual interference of the floral kind. Heredity 88:154–159PubMedGoogle Scholar
  9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48Google Scholar
  10. Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Bot Rev 59:112–152Google Scholar
  11. Blanchard EE (1966) Dípteros parásitos de scarabaeoideos argentinos. Rev Inves Agrop, Serie 5. Patol Veget 3:175–229Google Scholar
  12. Cariddi L, Moser M, Andrada M, Demo M, Zygadlo J, Sabini L, Maldonado A (2009) The effect of Minthostachys verticillata essential oil on the immune response of patients allergic to dust mites. Bol Latinoam Caribe Plant Med y Aromat 8(3):224–233Google Scholar
  13. Chacoff NP, Morales C, Garibaldi LA, Ashworth L, Aizen MA (2010) Pollinator dependence of Argentinian agriculture: current status and temporal analysis. Am J Plant Sci Biotechnol 3:106–116Google Scholar
  14. Charlesworth D, Charlesworth A (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997Google Scholar
  15. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary significance. Annu Rev Ecol Syst 18:237–268Google Scholar
  16. Delph LF, Lively CM (1992) Pollinator visitation, floral display and nectar of the sexual morphs of a gynodioecius shrub. Oikos 63:161–170Google Scholar
  17. Development Core Team R (2016) R: a language and environment for statistical computing. R foundation for statistical computing, ViennaGoogle Scholar
  18. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135Google Scholar
  19. Garibaldi LA et al (2013) Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science 339:1608–1611PubMedGoogle Scholar
  20. Gilbert F, Jervis M (1998) Functional, evolutionary and ecological aspects of feeding-related mouthpart specializations in parasitoid flies. Biol J Linn Soc 63(4):495–535Google Scholar
  21. Giorgis MA, Cingolani AM, Chiarini F (2011) Composición florística del Bosque Chaqueño Serrano de la provincia de Córdoba, Argentina. Kurtziana 36:9–43Google Scholar
  22. Guimarães JH (1977) Host-parasite and parasite-host catalogue of South American Tachinidae (Diptera). Arq Zool 28(3):1–131Google Scholar
  23. Harder LD, Wilson WG (1998) A clarification of pollen discounting and its joint effect with inbreeding depression on mating-system evolution. Am Nat 152:684–695PubMedGoogle Scholar
  24. Hong SP, Moon HK (2003) Gynodioecy in Lycopus maackianus Makino (Lamiaceae) in Korea: floral dimorphism and nutlet production. Flora 198:461–467Google Scholar
  25. Husband B, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70PubMedGoogle Scholar
  26. Klatt BK, Holzschuh A, Westphal C, Clough Y, Smit I, Pawelzik E, Tscharntke T (2014) Bee pollination improves crop quality, shelf life and commercial value. Proc R Soc B 281:2013–2440Google Scholar
  27. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313PubMedGoogle Scholar
  28. Lewis D (1941) Male sterility in natural populations of hermaphrodite plants. New Phytol 50:56–63Google Scholar
  29. Lewis D (1942) The evolution of sex in flowering plants. Biol Rev 17:46–67Google Scholar
  30. Lloyd DG (1975) The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325–339Google Scholar
  31. Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. N Z J Bot 24:135–162Google Scholar
  32. Mader E, Spivak M, Evans E (2010) Managing alternative pollinators: a handbook for beekeepers, growers, and conservationists. Natural Resource, Agriculture, and Engineering Service Cooperative Extension, IthacaGoogle Scholar
  33. Martínez GJ (2005) Recolección y Comercialización de Plantas Medicinales en el Departamento Santa María, Provincia de Córdoba, Argentina. Acta Farm Bonaer 24(4):575–584Google Scholar
  34. Martínez GJ, Planchuelo AM, Fuentes E, Ojeda M (2006) A numeric index to establish conservation priorities for medicinal plants in the Paravachasca valley, Córdoba, Argentina. Biodivers Conserv 15:2457–2475Google Scholar
  35. Morales CL (2009) Pollination requirement of raspberry in SW Argentina. Preliminary results. Int J Plant Reprod Biol 1:195–198Google Scholar
  36. Ojeda M, Arroyo A, Borgogno P, Biderbost E, Balzarini M (2004) Yield of peperina (Minthostachys mollis (Kunth.) Griseb.) populations in the year following planting: response to cropping regimen. Span J Agric Res 2:393–399Google Scholar
  37. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326Google Scholar
  38. Orford CA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proc R Soc B 282(1805):20142934PubMedGoogle Scholar
  39. Pinheiro J, Bates D, Debroy S, Sarkar D, Core R, R Core team (2017) nlme: linear and nonlinear mixed effects models. R Package Vers 3:1–131Google Scholar
  40. Rivkin LR, Case AL, Caruso CM (2016) Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae. New Phytol.  https://doi.org/10.1111/nph.13926 CrossRefPubMedGoogle Scholar
  41. Rodriguez-Riaño T, Dafni A (2007) Pollen–stigma interference in two gynodioecious species of Lamiaceae with intermediate individuals. Ann Bot 100:423–431PubMedGoogle Scholar
  42. Santos V, Ávila CJ (2009) Ocorrência de parasitismo em larvas de Liogenys Suturalis Blanchard, 1851 (Coleoptera: Melolonthidae) por Ptilodexia Brauer & Bergenstamm, 1889 (Diptera: Tachinidae). Arq Inst Biol 76(4):745–748Google Scholar
  43. Schippmann U, Leaman DJ, Cunningham AB (2002) Impact of cultivation and gathering of medicinal plants on biodiversity: global trends and issues. Inter-Department Working Group on Biology Diversity for Food and Agriculture, FAO, RomeGoogle Scholar
  44. Schippmann U, Leaman D, Cunningham AB (2006) A comparison of cultivation and wild collection of medicinal and aromatic plants under sustainability aspects. In: Bogers RJ, Craker LE, Lange D (eds) Medicinal and aromatic plants. Springer, Dordrecht, pp 75–95Google Scholar
  45. Schmidt-Lebuhn AN (2008a) Revision of the genus Minthostachys (Labiatae). Mem N Y Bot Gard 98:1–74Google Scholar
  46. Schmidt-Lebuhn AN (2008b) Ethnobotany, biochemistry and pharmacology of Minthostachys (Lamiaceae). J Enthnomaracol 118:343–353Google Scholar
  47. Shykoff JA, Kolokotronis SO, Collin CL, López-Villavicencio M (2003) Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135:1–9PubMedGoogle Scholar
  48. Stireman JO, O’Hara JE, Wood DM (2006) Tachinidae, evolution, behaviour, and ecology. Ann Rev Entomol 51:525–555Google Scholar
  49. Thompson JD, Taraire M (2000) Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris. Evolution 54(5):1510–1520PubMedGoogle Scholar
  50. Thompson JD, Rolland AG, Prugnolle F (2002) Genetic variation for sexual dimorphism in flower size within and between populations of gynodioecious Thymus vulgaris. J Evol Biol 15:362–372Google Scholar
  51. Vasisht K, Sharma N, Karan M (2016) Current perspective in the international trade of medicinal plants material: an update. Curr Pharm Des 22(27):4288–4336PubMedGoogle Scholar
  52. Wilcock C, Neiland MRM (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–277PubMedGoogle Scholar
  53. Woodcock TS, Larson BMH, Kevan PG, Inouye DW, Lunau K (2014) Flies and flowers II: floral attractants and rewards. J Pollinat Ecol 12(8):63–94Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Evangelina Glinos
    • 1
  • Eugenia Condat
    • 2
  • Pablo Mulieri
    • 3
  • Lorena Ashworth
    • 1
    • 4
    Email author
  1. 1.Instituto Multidisciplinario de Biología Vegetal (CONICET – Universidad Nacional de Córdoba)CórdobaArgentina
  2. 2.Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de CórdobaCórdobaArgentina
  3. 3.Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Consejo Nacional de Investigaciones Científicas y TécnicasBuenos AiresArgentina
  4. 4.Laboratorio Nacional de Análisis y Síntesis EcológicaUniversidad Nacional Autónoma de MéxicoMoreliaMexico

Personalised recommendations