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Biodiversity and Conservation

, Volume 28, Issue 6, pp 1389–1409 | Cite as

Pollination insights for the conservation of a rare threatened plant species, Astragalus tragacantha (Fabaceae)

  • L. SchurrEmail author
  • L. Affre
  • F. Flacher
  • T. Tatoni
  • L. Le Mire Pecheux
  • B. Geslin
Original Paper

Abstract

The increase in habitat fragmentation impacts plant-pollinator interactions and threatens the sustainability of plant species. Astragalus tragacantha (Fabaceae), is a rare endangered plant species along the coastal habitats where the plant populations have undergone considerable fragmentation and decline of size. Controlled pollination treatments, the observation of pollinator activity, and pollinator captures, have been conducted to study: (1) the mating system of A. tragacantha and the potential for inbreeding depression and/or outbreeding depression based on controlled pollination treatments, (2) the pollinator composition among populations using a correspondence analysis and a hierarchical clustering, and (3) the link between pollinators and the plant reproductive success using a path-analysis model. In this study, we demonstrated that this plant was not autogamous self-pollinating and depended on pollinators for its reproduction. The absence of difference between manual and open pollinations regarding the reproductive success showed an absence of pollen limitation in our populations. We showed that populations differed in the composition of their pollinator guilds. Some pollinator species were predominant in certain populations. The pollination treatments revealed the existence of a mixed mating system in A. tragacantha populations. We showed an inbreeding depression potentially linked to a predominant pollinator-facilitated selfing, and the existence of outbreeding depression between some distant populations. These differences in pollinator guild and plant mating systems among populations must be considered during the restoration of populations along the Mediterranean coastal habitats in order to enhance the reproductive success and sustainability of A. tragacantha.

Keywords

Mixed mating system Pollination network Plant reproductive success Fragmented populations Inbreeding and outbreeding depressions Path analysis 

Notes

Acknowledgements

We are thankful to Calanques National Park for financial support. We thank A. Baumel for its helpful advices. We are grateful to D. Genoud, M. Aubert and D. Pavon for bee and plant identifications, and to L. Ropars for her support in the field. We thank the two English proofreadings of the manuscript (M. Paul REF 0820L025171 and ‘American Journal Expert’: Certificate Verification Key: 9EED-CE9D-8AE4-6522-49C3). Finally, we show gratitude to the two anonymous reviewers that provided useful comments on original version of the manuscript.

Supplementary material

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References

  1. Affre L, Dumas P-J, Dumas E et al (2015) Regard écologique sur le recul stratégique: atouts et risques pour la diversité végétale péri- urbaine marseillaise. Vertigo Hors série 21:13pGoogle Scholar
  2. Agren J, Schemske DW (1993) Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia Hirsuta and Begonia Semiovata. Evolution (NY) 47:125–135.  https://doi.org/10.2307/2410123 CrossRefGoogle Scholar
  3. Aguilar R, Quesada M, Ashworth L et al (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188.  https://doi.org/10.1111/j.1365-294X.2008.03971.x CrossRefGoogle Scholar
  4. Aizen MA, Ashworth A, Galetto L (2002) Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? J Veg Sci 13:885–892.  https://doi.org/10.1111/J.1654-1103.2002.Tb02118.X CrossRefGoogle Scholar
  5. Åkesson M, Liberg O, Sand H et al (2016) Genetic rescue in a severely inbred wolf population. Mol Ecol 25:4745–4756.  https://doi.org/10.1111/mec.13797 CrossRefGoogle Scholar
  6. Alonso C, Herrera CM, Ashman T (2011) A piece of the puzzle: a method for comparing pollination quality and quantity across multiple species and reproductive events. New Phytol 193:532–542CrossRefGoogle Scholar
  7. Barnosky AD, Hadly EA, Bascompte J et al (2012) Approaching a state shift in Earth’s biosphere. Nature 486:52–58.  https://doi.org/10.1038/nature11018 CrossRefGoogle Scholar
  8. Bauer AA, Clayton MK, Brunet J (2017) Floral traits influencing plant attractiveness to three bee species: consequences for plant reproductive success. Am J Bot 104:772–781.  https://doi.org/10.3732/ajb.1600405 CrossRefGoogle Scholar
  9. Becker T, Voss N, Durka W (2011) Pollen limitation and inbreeding depression in an “old rare” bumblebee-pollinated grassland herb. Plant Biol 13:857–864.  https://doi.org/10.1111/j.1438-8677.2011.00452.x CrossRefGoogle Scholar
  10. Campagne P, Affre L, Baumel A et al (2008) Fine-scale response to landscape structure in Primula vulgaris Huds.: does hedgerow network connectedness ensure connectivity through gene flow? Popul Ecol 51(1):209–219.  https://doi.org/10.1007/s10144-008-0124-2 CrossRefGoogle Scholar
  11. Charlesworth D, Charlesworth B (2012) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Evol Syst 18:237–268CrossRefGoogle Scholar
  12. Cresswell JE (1999) The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius). J Ecol 87:670–677.  https://doi.org/10.1046/j.1365-2745.1999.00385.x CrossRefGoogle Scholar
  13. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity (Edinb) 83:260–270.  https://doi.org/10.1038/sj.hdy.6885530 CrossRefGoogle Scholar
  14. Dick CW, Hardy OJ, Jones FA et al (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Trop Plant Biol 1:20–33.  https://doi.org/10.1007/s12042-007-9006-6 CrossRefGoogle Scholar
  15. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475.  https://doi.org/10.1111/j.1365-294X.2006.03148.x CrossRefGoogle Scholar
  16. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Rev Lit Arts Am 34:487–515.  https://doi.org/10.1146/132419 Google Scholar
  17. Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618.  https://doi.org/10.1111/mec.13139 CrossRefGoogle Scholar
  18. Frankham R, Ballou JD, Eldridge MDB et al (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475.  https://doi.org/10.1111/j.1523-1739.2011.01662.x CrossRefGoogle Scholar
  19. Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Cons 170:56–63CrossRefGoogle Scholar
  20. Frankie GW, Opler PA, Bawa KS (1976) Foraging Behaviour of Solitary Bees: implications for outcrossing of a neotropical forest tree. Br Ecol Soc 64:1049–1057Google Scholar
  21. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764.  https://doi.org/10.1046/j.1365-2656.2002.00641.x CrossRefGoogle Scholar
  22. Geslin B, Baude M, Mallard F et al (2014) Effect of local spatial plant distribution and conspecific density on bumble bee foraging behaviour. Ecol Entomol 39:334–342.  https://doi.org/10.1111/een.12106 CrossRefGoogle Scholar
  23. Geslin B, Aizen MA, Garcia N et al (2017) The impact of honey bee colony quality on crop yield and farmers’ profit in apples and pears. Agric Ecosyst Environ 248:153–161.  https://doi.org/10.1016/j.agee.2017.07.035 CrossRefGoogle Scholar
  24. Guiller C, Affre L, Albert CH et al (2016) How do field margins contribute to the functional connectivity of insect-pollinated plants? Landsc Ecol.  https://doi.org/10.1007/s10980-016-0359-9 Google Scholar
  25. Harder LD, Barrett SCH (1996) Pollen dispersal and mating patterns in animal-pollinated plants. In: Lloyd DG, Barrett SCH (eds) Floral biology. Springer, BostonGoogle Scholar
  26. Hardion L, Baumel A, Dumas P et al (2010) Phylogenetic relationships and infrageneric classification of Astragalus tragacantha L. (Fabaceae), inferred from nuclear ribosomal DNA Internal transcribed spacers data (nrDNA ITS). Ecol Mediterr 36:99–106Google Scholar
  27. Hardion L, Dumas PJ, Abdel-Samad F et al (2016) Geographical isolation caused the diversification of the Mediterranean thorny cushion-like Astragalus L. sect. tragacantha DC. (Fabaceae). Mol Phylogenet Evol 97:187–195.  https://doi.org/10.1016/j.ympev.2016.01.006 CrossRefGoogle Scholar
  28. Hoehn P, Tscharntke T, Tylianakis JM et al (2008) Functional group diversity of bee pollinators increases crop yield. Proc Biol Sci 275(1648):2283–2291.  https://doi.org/10.1098/rspb.2008.0405 CrossRefGoogle Scholar
  29. Johnson WE, Onorato DP, Roelke ME et al (2010) Genetic restoration of the Florida panther. Science 329:1641–1645.  https://doi.org/10.1126/science.1192891 CrossRefGoogle Scholar
  30. Karron JD, Mitchell RJ, Holmquist KG et al (2004) The influence of floral display size on selfing rates in Mimulus ringens. Heredity (Edinb) 92:242–248.  https://doi.org/10.1038/sj.hdy.6800402 CrossRefGoogle Scholar
  31. Karron JD, Holmquist KG, Flanagan RJ et al (2009) Pollinator visitation patterns strongly influence among-flower variation in selfing rate. Ann Bot 103:1379–1383.  https://doi.org/10.1093/aob/mcp030 CrossRefGoogle Scholar
  32. Klein A-M, Vaissiere BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313.  https://doi.org/10.1098/rspb.2006.3721 CrossRefGoogle Scholar
  33. Laffont-Schwob I, Dumas PJ, Pricop A et al (2011) Insights on metal-tolerance and symbionts of the rare species Astragalus tragacantha aiming at phytostabilization of polluted soils and plant conservation. Ecol Mediterr 37(2):57–62Google Scholar
  34. Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579.  https://doi.org/10.1111/2041-210X.12512 CrossRefGoogle Scholar
  35. Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I—functional dimensions. Int J Plant Sci 153:358–369CrossRefGoogle Scholar
  36. Manning A (1956) Some aspects of the foraging behaviour of bumble-bees. Behaviour 9:164–201CrossRefGoogle Scholar
  37. Martin EF (2010) Reproduction, demography, and habitat characterization of Astragalus peckii (Fabaceae), a Rare Central Oregon Endemic. Dissertation, University of Oregon State UniversityGoogle Scholar
  38. Martínez-Sánchez JJ, Segura F, Aguado M et al (2011) Life history and demographic features of Astragalus nitidiflorus, a critically endangered species. Flora Morphol Distrib Funct Ecol Plants 206:423–432.  https://doi.org/10.1016/j.flora.2010.11.006 CrossRefGoogle Scholar
  39. Médail F, Myers N (2004) Mediterranean basin. In: Mittermeier RA, Gil PR, Hoffmann M et al (eds) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX, Monterrey, Conservation International, Washington and Agrupación Sierra Madre, Mexico, pp 144–147Google Scholar
  40. Médail F, Quézel P (1999) Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conserv Biol 13:1510–1513CrossRefGoogle Scholar
  41. Mitchell RJ, Irwin RE, Flanagan RJ et al (2009) Ecology and evolution of plant–pollinator interactions. Ann Bot 103:1355–1363.  https://doi.org/10.1093/aob/mcp122 CrossRefGoogle Scholar
  42. Morandin LA, Winston ML (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol Appl 15:871–881CrossRefGoogle Scholar
  43. Ne’eman G, Shavit O, Shaltiel L et al (2006) Foraging by male and female solitary bees with implications for pollination. J Insect Behav 19:383–401.  https://doi.org/10.1007/s10905-006-9030-7 CrossRefGoogle Scholar
  44. Ne’eman G, Andreas J, Newstrom-Lloyd L et al (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451.  https://doi.org/10.1111/j.1469-185X.2009.00108.x Google Scholar
  45. Ogilvie JE, Griffin SR, Gezon ZJ et al (2017) Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology. Ecol Lett 20:1507–1515.  https://doi.org/10.1111/ele.12854 CrossRefGoogle Scholar
  46. Ollerton J (2017) Pollinator diversity: distribution, ecological function, and conservation. Annu Rev Ecol Evol Syst 48:353–376CrossRefGoogle Scholar
  47. Oostermeijer JGB, Altenburg RGM, Den Nijs HCM (1995) Effects of outcrossing distance and selfing on fitness components in the rare Gentiana pneumonanthe (Gentianaceae). Acta Bot Neerl 44:257–268.  https://doi.org/10.1111/j.1438-8677.1995.tb00784.x CrossRefGoogle Scholar
  48. Salducci MD, Folzer H, Issartel J et al (2019) How can a rare protected plant cope with the metal and metalloid soil pollution resulting from past industrial activities? Phytometabolites, antioxidant activities and root symbiosis involved in the metal tolerance of Astragalus tragacantha. Chemosphere 217:887–896.  https://doi.org/10.1016/j.chemosphere.2018.11.078 CrossRefGoogle Scholar
  49. Schemske DW, Lande R (1985) The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution (NY) 39:41.  https://doi.org/10.2307/2408515 CrossRefGoogle Scholar
  50. Shackelford G, Steward PR, Benton TG et al (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev 88:1002–1021.  https://doi.org/10.1111/brv.12040 CrossRefGoogle Scholar
  51. Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368.  https://doi.org/10.1890/08-1034.1 CrossRefGoogle Scholar
  52. Shipley B (2013) The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94:560–564.  https://doi.org/10.1890/12-0976.1 CrossRefGoogle Scholar
  53. Suehs CM, Affre L, Medail F (2005) Unexpected insularity effects in invasive plant mating systems: the case of Carpobrotus (Aizoaceae) taxa in the Mediterranean Basin. Biol J Linn Soc 85:65–79CrossRefGoogle Scholar
  54. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496.  https://doi.org/10.1016/j.tree.2004.07.003 CrossRefGoogle Scholar
  55. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  56. Terzo M, Rasmont P (2016) Clé des genres d’apoïdes d’Europe Occidentale. UnpublishedGoogle Scholar
  57. Torné-Noguera A, Rodrigo A, Arnan X et al (2014) Determinants of spatial distribution in a bee community: nesting resources, flower resources, and body size. PLoS ONE 9:1–10.  https://doi.org/10.1371/journal.pone.0097255 CrossRefGoogle Scholar
  58. Valsecchi F (1994) Sul complesso Astragalus tragacantha L. (Leguminosae) nel Mediterraneo. Webbia 49:31–41CrossRefGoogle Scholar
  59. Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965.  https://doi.org/10.1046/j.1461-0248.2003.00523.x CrossRefGoogle Scholar
  60. Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49.  https://doi.org/10.1016/j.tree.2014.10.009 CrossRefGoogle Scholar
  61. Wilcove DS, McLellan CH, Dobson AP (1986) Habitat fragmentation in the temperate zone. Conserv Biol Sci Scarcity Divers 11:237–256Google Scholar
  62. Willi Y, Fischer M (2005) Genetic rescue in interconnected populations of small and large size of the self-incompatible Ranunculus reptans. Heredity (Edinb) 95:437–443CrossRefGoogle Scholar
  63. Zurbuchen A, Landert L, Klaiber J et al (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676.  https://doi.org/10.1016/j.biocon.2009.12.003 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Aix Marseille Univ, Univ Avignon, CNRS, IRD, IMBEMarseille Cedex 20France
  2. 2.Université Paris Diderot, Sorbonne Universités, UPMC Univ Paris 6, CNRS, INRA, IRD, UPEC, Institut d’Ecologie et des Sciences de l’Environnement de Paris (iEES-Paris)Paris Cedex 05France
  3. 3.Parc National des CalanquesMarseilleFrance

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