Advertisement

Oecologia

pp 1–7 | Cite as

Interactive effects between donor and recipient species mediate fitness costs of heterospecific pollen receipt in a co-flowering community

  • Gerardo Arceo-GómezEmail author
  • Rainee L. Kaczorowski
  • Cheril Patel
  • Tia-Lynn AshmanEmail author
Community ecology – original research

Abstract

Evaluation of pollen transfer in wild plant communities revealing heterospecific pollen receipt is common, yet experimental hand pollinations have revealed high among-species variation in the magnitude of its effect on recipient fitness. The causes of this among-species variation are unknown, however, prompting the investigation of underlying factors. Here, we conducted a hand-pollination experiment with ten co-flowering species to determine whether the effects of heterospecific pollen receipt are mediated by the pollen donor or recipient species alone, or whether the effects are determined by the interaction between them. We further assessed species traits potentially mediating interactive effects in heterospecific pollen receipt by evaluating the relationship between heterospecific pollen effect size and three different predictors reflecting a unique combination of pollen donor and recipient characteristics. Our results show, for the first time, that the magnitude of the heterospecific pollen receipt effect is determined by the specific combination of donor and recipient species (i.e., interactive effects). However, we were unable to uncover the specific combination of traits mediating these effects. Overall, our study provides strong evidence that an understanding of heterospecific pollen receipt effects based on recipient or donor characteristics alone may be insufficient. This study is an important step toward an understanding of consequences of heterospecific pollen receipt in co-flowering communities.

Keywords

Co-flowering Pollen transfer Pollination Pollen size Stigma area 

Notes

Acknowledgements

We thank Rebecca Hayes, Elizabeth O’Neill, Kiera Doleski, Abigail Rothrauff and Jesse Daniels for their assistance collecting data, UPitt greenhouse staff for plant care. This work was funded by NSF DEB1452386 to TLA. CP was supported by an ETSU student–faculty collaborative grant. UPitt and ETSU provided logistical support.

Author contribution statement

TLA and GAG conceived and designed the experiments. RLK and GAG performed the experiments. CP and RLK processed samples and collected data. GAG and CP analyzed the data. GAG and RLK wrote the manuscript; all authors provided editorial advice.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Arceo-Gómez G, Ashman TL (2011) Heterospecific pollen deposition: does diversity alter the consequences? New Phytol 192:738–746.  https://doi.org/10.1111/j.1469-8137.2011.03831.x CrossRefPubMedGoogle Scholar
  2. Arceo-Gómez G, Ashman TL (2016) Invasion status and phylogenetic relatedness predict cost of heterospecific pollen receipt: implications for native biodiversity decline. J Ecol 104:1003–1008.  https://doi.org/10.1111/1365-2745.12586 CrossRefGoogle Scholar
  3. Arceo-Gómez G, Raguso RA, Geber MA (2015) Can plants evolve tolerance mechanisms to heterospecific pollen effects? An experimental test of the adaptive potential in Clarkia species. Oikos 125:718–725.  https://doi.org/10.1111/oik.02594 CrossRefGoogle Scholar
  4. Arceo-Gómez G, Abdala-Roberts L, Jankowiak A, Kohler C, Meindl GA, Navarro-Fernández CM, Parra-Tabla V, Ashman TL, Alonso C (2016) Patterns of among-and within-species variation in heterospecific pollen receipt: the importance of ecological generalization. Am J Bot 103:396–407.  https://doi.org/10.3732/ajb.1500155 CrossRefPubMedGoogle Scholar
  5. Arceo-Gómez G, Jameel MI, Ashman TL (2018a) Effects of heterospecific pollen from a wind-pollinated and pesticide-treated plant on reproductive success of an insect-pollinated species. Am J Bot 105:836–841.  https://doi.org/10.1002/ajb2.1090 CrossRefPubMedGoogle Scholar
  6. Arceo-Gómez G, Kaczorowski RL, Ashman TL (2018b) A network approach to understanding patterns of coflowering in diverse communities. Int J Plant Sci 179:569–582.  https://doi.org/10.1086/698712 CrossRefGoogle Scholar
  7. Ashman TL, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100:1061–1070.  https://doi.org/10.3732/ajb.1200496 CrossRefPubMedGoogle Scholar
  8. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095818 CrossRefGoogle Scholar
  9. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. P Natl Acad Sci USA 100:9383–9387.  https://doi.org/10.1073/pnas.1633576100 CrossRefGoogle Scholar
  10. Brandvain Y, Haig D (2005) Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am Nat 166:330–338.  https://doi.org/10.1086/432036 CrossRefPubMedGoogle Scholar
  11. Campbell DR, Motten AF (1985) The mechanism of competition for pollination between two forest herbs. Ecology 66:554–563.  https://doi.org/10.2307/1940404 CrossRefGoogle Scholar
  12. CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. P Natl Acad Sci USA 111:4916–4921.  https://doi.org/10.1073/pnas.1323073111 CrossRefGoogle Scholar
  13. Cruden RW, Miller-Ward S (1981) Pollen-ovule ratio, pollen size, and the ratio of stigmatic area to the pollen-bearing area of the pollinator: an hypothesis. Evolution 35:964–974.  https://doi.org/10.1111/j.1558-5646.1981.tb04962.x CrossRefPubMedGoogle Scholar
  14. Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, OxfordGoogle Scholar
  15. Emer C, Vaughan IP, Hiscock S, Memmott J (2015) The impact of the invasive alien plant, Impatiens glandulifera, on pollen transfer networks. PLoS One 10:e0143532.  https://doi.org/10.1371/journal.pone.0143532 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fang Q, Huang SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:1176–1185.  https://doi.org/10.1890/12-1634.1 CrossRefPubMedGoogle Scholar
  17. Forrest J, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440.  https://doi.org/10.1890/09-0099.1 CrossRefPubMedGoogle Scholar
  18. Freestone AL, Inouye BD (2006) Dispersal limitation and environmental heterogeneity shape scale-dependent diversity patterns in plant communities. Ecology 87:2425–2432.  https://doi.org/10.1890/0012-9658(2006)87%5b2425:DLAEHS%5d2.0.CO;2 CrossRefPubMedGoogle Scholar
  19. Harder LD, Cruzan MB, Thomson JD (1993) Unilateral incompatibility and the effects of interspecific pollination for Erythronium americanum and Erythronium albidum (Liliaceae). Can J Bot 71:353–358.  https://doi.org/10.1139/b93-038 CrossRefGoogle Scholar
  20. Hedges L, Olkin I (1985) Statistical models for meta-analysis. Academic Press, New YorkGoogle Scholar
  21. Heslop-Harrison Y (1981) Stigma characteristics and angiosperm taxonomy. Nord J Bot 1:401–420.  https://doi.org/10.1111/j.1756-1051.1981.tb00707.x CrossRefGoogle Scholar
  22. Hiscock SJ, Allen AM (2008) Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus. New Phytol 179:286–317.  https://doi.org/10.1111/j.1469-8137.2008.02457.x CrossRefPubMedGoogle Scholar
  23. Johnson AL, Ashman TL (2018) Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phytol 221:142–154.  https://doi.org/10.1111/nph.15366 CrossRefPubMedGoogle Scholar
  24. Koski MH, Meindl GA, Arceo-Gómez G, Wolowski M, LeCroy KA, Ashman TL (2015) Plant–flower visitor networks in a serpentine metacommunity: assessing traits associated with keystone plant species. Arthropod Plant Int 9:9–21.  https://doi.org/10.1007/s11829-014-9353-9 CrossRefGoogle Scholar
  25. Kwak MM, Jennersten O (1991) Bumblebee visitation and seedset in Melampyrum pratense and Viscaria vulgaris: heterospecific pollen and pollen limitation. Oecologia 86:99–104.  https://doi.org/10.1007/BF00317395 CrossRefPubMedGoogle Scholar
  26. Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol Lett 10:539–550.  https://doi.org/10.1111/j.1461-0248.2007.01055.x CrossRefPubMedGoogle Scholar
  27. Martin FW (1970) Pollen germination on foreign stigmas. B Torrey Bot Club 97:1–6.  https://doi.org/10.2307/2483984 CrossRefGoogle Scholar
  28. Matsumoto T, Takakura KI, Nishida T (2010) Alien pollen grains interfere with the reproductive success of native congener. Biol Invasions 12:1617–1626.  https://doi.org/10.1007/s10530-009-9574-5 CrossRefGoogle Scholar
  29. Mazer SJ, Hove AA, Miller BS, Barbet-Massin M (2010) The joint evolution of mating system and pollen performance: predictions regarding male gametophytic evolution in selfers vs. outcrossers. Perspect Plant Ecol 12:31–41.  https://doi.org/10.1016/j.ppees.2009.06.005 CrossRefGoogle Scholar
  30. Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238.  https://doi.org/10.1080/07352680802205631 CrossRefGoogle Scholar
  31. Murphy SD (2000) Field testing for pollen allelopathy: a review. J Chem Ecol 26:2155–2172.  https://doi.org/10.1023/A:1005572516948 CrossRefGoogle Scholar
  32. Murphy SD, Aarssen LW (1989) Pollen allelopathy among sympatric grassland species: in vitro evidence in Phleum pratense L. New Phytol 112:295–305.  https://doi.org/10.1111/j.1469-8137.1989.tb02385.x CrossRefGoogle Scholar
  33. Olesen JM, Jordano P (2002) Geographic patterns in plant–pollinator mutualistic networks. Ecology 83:2416–2424Google Scholar
  34. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. P Natl Acad Sci USA 104:19891–19896.  https://doi.org/10.1073/pnas.0706375104 CrossRefGoogle Scholar
  35. Pleasants JM, Hellmich RL, Dively GP, Sears MK, Stanley-Horn DE, Mattila HR, Foster JE, Clark P, Jones GD (2001) Corn pollen deposition on milkweeds in and near cornfields. P Natl Acad Sci USA 98:11919–11924.  https://doi.org/10.1073/pnas.211287498 CrossRefGoogle Scholar
  36. Rasband WS (1997) ImageJ. US National Institutes of Health, BethesdaGoogle Scholar
  37. Ritland K, Leblanc M (2004) Mating system of four inbreeding monkeyflower (Mimulus) species revealed using ‘progeny-pair’analysis of highly informative microsatellite markers. Plant Species Biol 19:149–157.  https://doi.org/10.1111/j.1442-1984.2004.00111.x CrossRefGoogle Scholar
  38. SAS Institute (2010) SAS/IML software, version 9.2. SAS Institute, Cary, North Carolina, USAGoogle Scholar
  39. Schoener TW (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51:408–418.  https://doi.org/10.2307/1935376 CrossRefGoogle Scholar
  40. Spira TP (1980) Floral parameters, breeding system and pollinator type in Trichostema (Labiatae). Am J Bot 67:278–284.  https://doi.org/10.1002/j.1537-2197.1980.tb07652.x CrossRefGoogle Scholar
  41. Tur C, Sáez A, Traveset A, Aizen MA (2016) Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: evidence of widespread facilitation in south Andean plant communities. Ecol Lett 19:576–586.  https://doi.org/10.1111/ele.12594 CrossRefPubMedGoogle Scholar
  42. Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59:934–944.  https://doi.org/10.2307/1938545 CrossRefGoogle Scholar
  43. Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183.  https://doi.org/10.1111/j.1471-8286.2004.00829.x CrossRefGoogle Scholar
  44. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100.  https://doi.org/10.1093/bioinformatics/btn358 CrossRefPubMedGoogle Scholar
  45. Willis JH (1993) Partial self-fertilization and inbreeding depression in two populations of Mimulus guttatus. Heredity 71:145–154.  https://doi.org/10.1038/hdy.1993.118 CrossRefGoogle Scholar
  46. Wipf HML, Meindl GA, Ashman TL (2016) A first test of elemental allelopathy via heterospecific pollen receipt. Am J Bot 103:514–521.  https://doi.org/10.3732/ajb.1500187 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesEast Tennessee State UniversityJohnson CityUSA
  2. 2.Department of Biological SciencesUniversity of PittsburghPittsburghUSA

Personalised recommendations