Vegetative sprouting as an additional pathway for a seed size-number trade-off: a field-parameterised simulation approach

Abstract

Studies of perennial plants generally search for a seed size vs. seed number trade-off. Surprisingly, the fact that perennials may replace an investment in large seeds by the allocation to vegetative propagation has not yet been investigated as an additional pathway enabling species coexistence. We focused on the mechanisms of coexistence in Carex elata and C. elongata, two co-occurring clonal sedges dominant in European swamp alder forests. We asked the following questions: i) Is the number of germinated seeds a better predictor of species coexistence than the total number of seeds? ii) What recruitment conditions and competition rules determine vegetative sprouting to be an alternative to large, competitively superior seeds? We measured several species functional traits related to the colonisation and fitness of perennials. To examine the competitive hierarchy between species and microsite species preferences, we analysed the effects of environmental factors and plant densities on fitness-related traits using Structural Equation Modelling (SEM). Then, using a series of spatially explicit simulations partly parameterised based on the field measurement, we evaluated the importance of seed and ramet propagation and recruitment conditions for long-term species coexistence. SEM indicated a competitive hierarchy and a large overlap in microsite preferences between species. As a response to our initial questions we found that: i) Only differences in the numbers of germinated seeds, allowed the two species to coexist. If we consider only differences in the total number of seeds, the superior competitor (Carex elata) outcompeted the inferior competitor (C. elongata) in all scenarios. This is because the former produced about three-times as many seeds as the latter. ii) We show that vegetative sprouting represents an additional pathway for the seed size-number trade-off when the competitive superiority of species is attributed to vegetative propagation. This is another way that a species deals with the omnipresent seeds of other species. Taken together, our study demonstrates that differences in seed performance, coupled with differences in vegetative propagation related to competitive ability, are an additional mechanism allowing the coexistence of perennial plants.

Abbreviations

CFI:

Comparative Fit Index

GLMM:

Generalised Linear Mixed Model

MLM:

Maximum Likelihood Method

RMSEA:

Root Mean Square Error of Approximation Index

SEM:

Structural Equation Modelling

SEVM:

Spatial Eigenvalue Vector Mapping

References

  1. Abrahamson, W.A. 1980. Demography and vegetative reproduction. In: O.T. Solbrig (ed.), Demography and Evolution in Plant Populations. University of California Press, Los Angeles. pp. 89–106.

    Google Scholar 

  2. Baskin, C.C. and Baskin, J.M. 2014. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. 2nd ed. Elsevier/ Academic Press, San Diego.

    Google Scholar 

  3. Beatty, S.W. 1984. Influence of microtopography and canopy species on spatial patterns of forest understory plants. Ecology 65:1406–1419.

    Article  Google Scholar 

  4. Ben-Hur, E., Fragman-Sapir, O., Hadas, R., Singer, A. and Kadmon, R. 2012. Functional trade-offs increase species diversity in experimental plant communities. Ecol. Lett. 15:1276–1282.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Benot, M.-L., Bittebiere, A.-K., Ernoult, A., Clément, B. and Mony, C. 2013. Fine-scale spatial patterns in grassland communities depend on species clonal dispersal ability and interactions with neighbours. J. Ecol. 101:626–636.

    Article  Google Scholar 

  6. Bierzychudek, P. 1982. Life histories and demography of shade-tolerant temperate forest herbs: a review. New Phytol. 90:757–776.

    Article  Google Scholar 

  7. Bollen, K.A. and Long, J.S. 1993. Testing Structural Equation Models. Sage Publications, Newbury Park, CA.

    Google Scholar 

  8. Bruelheide, H. and Udelhoven, P. 2005. Correspondence of the fine-scale spatial variation in soil chemistry and the herb layer vegetation in beech forests. For. Ecol. Manage. 210:205–223.

    Article  Google Scholar 

  9. Bullock, J.M., Hill, B.C., Silvertown, J. and Sutton, M. 1995. Gap colonization as a source of grassland community change: effects of gap size and grazing on the rate and mode of colonization by different species. Oikos 72:273–282.

    Article  Google Scholar 

  10. Cadotte, M.W. 2007. Concurrent niche and neutral processes in the competition-colonization model of species coexistence. Proc. R. Soc. B-Biol. Sci. 274:2739–2744.

    Article  Google Scholar 

  11. Canham, C.D. 1988. An index for understory light levels in and around canopy gaps. Ecology 69:1634–1638.

    Article  Google Scholar 

  12. Charpentier, A., Grillas, P. and Thompson, J.D. 2000. The effects of population size limitation on fecundity in mosaic populations of the clonal macrophyte Scirpus maritimus (Cyperaceae). Am. J. Bot. 87:502–507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Cheplick, G.P. 1995. Life history trade-offs in Amphibromus scabrivalvis (Poaceae): allocation to clonal growth, storage, and cleis-togamous reproduction. Am. J. Bot. 82:621–629.

    Article  Google Scholar 

  14. Cheplick, G.P. 1997. Responses to severe competitive stress in a clonal plant: differences between genotypes. Oikos 79:581–591.

    Article  Google Scholar 

  15. Chesson, P. and Huntly, N. 1997. The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am. Nat. 150:519–553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Douda, J. 2010. The role of landscape configuration in plant composition of floodplain forests across different physiographic areas. J. Veg. Sci. 21:1110–1124.

    Article  Google Scholar 

  17. Douda, J., Boublík, K., Slezák, M., Biurrun, I., Nociar, J., Havrdová, A., Doudová, J., Aćić, S., Brisse, H., Brunet, J., Chytrý, M., Claessens, H., Csiky, J., Didukh, Y., Dimopoulos, P., Dullinger, S., FitzPatrick, Ú., Guisan, A., Horchler, P.J., Hrivnák, R., Jandt, U., Kącki, Z., Kevey, B., Landucci, F., Lecomte, H., Lenoir, J., Paal, J., Paternoster, D., Pauli, H., Pielech, R., Rodwell, J.S., Roelandt, B., Svenning, J.-C., Šibík, J., Šilc, U., Škvorc, Ž., Tsiripidis, I., Tzonev, R.T., Wohlgemuth, T. and Zimmermann, N.E. 2016. Vegetation classification and biogeography of European floodplain forests and alder carrs. Appl. Veg. Sci. 19:147–163.

    Article  Google Scholar 

  18. Douda, J., Doudová-Kochánková, J., Boublík, K. and Drašnarová, A. 2012. Plant species coexistence at local scale in temperate swamp forest: test of habitat heterogeneity hypothesis. Oecologia 169:523–534.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dormann, C.F., McPherson, J.M., Araújo, M.B., Bivand, R., Bolliger, J., Carl, G., Davies, R.G., Hirzel, A., Jetz, W., Kissling, W.D., Kühn, I., Ohlemüller, R., Peres-Neto, P.R., Reineking, B., Schröder, B., Schurr, F.M. and Wilson, R. 2007. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628.

    Article  Google Scholar 

  20. Eckert, C.G. 2002. The loss of sex in clonal plants. Evol. Ecol. 15:501–520.

    Article  Google Scholar 

  21. Egler, F.E. 1954. Vegetation science concepts I. Initial floristic composition, a factor in old-field vegetation development. Vegetatio 4:412–417.

    Google Scholar 

  22. Elias, R.B. and Dias, E. 2009. The effects of landslides on the mountain vegetation of Flores Island, Azores. J. Veg. Sci. 20: 706–717.

    Article  Google Scholar 

  23. Eriksson, O. 2005. Game theory provides no explanation for seed size variation in grasslands. Oecologia 144:98–105.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Eriksson, O. 2011. Niche shifts and seed limitation as mechanisms behind seedling recruitment patterns in clonal plants. Preslia 83:301–314.

    Google Scholar 

  25. Eriksson, O. and Jakobsson, A. 1998. Abundance, distribution and life histories of grassland plants: a comparative study of 81 species. J. Ecol. 86:922–933.

    Article  Google Scholar 

  26. Fang, X., Yuan, J., Wang, G. and Zhao, Z. 2006. Fruit production of shrub, Caragana korshinskii, following above-ground partial shoot removal: mechanisms underlying compensation. Plant Ecol. 187:213–225.

    Article  Google Scholar 

  27. Fischer, M. and van Kleunen, M. 2002. On the evolution of clonal plant life histories. Evol. Ecol. 15:565–582.

    Article  Google Scholar 

  28. Fukami, T. 2004. Assembly history interacts with ecosystem size to influence species diversity. Ecology 85:3234–3242.

    Article  Google Scholar 

  29. Fox, J.W. 2013. The intermediate disturbance hypothesis should be abandoned. Trends Ecol. Evol. 28:86–92.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Frazer, G.W., Canham, C.D. and Lertzman, K.P. 1999. Gap Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Burnaby, British Columbia, Canada: Simon Fraser University and Millbrook, New York, NY: the Institute of Ecosystem Studies.

  31. Geritz, S.A., van der Meijden, E. and Metz, J.A. 1999. Evolutionary dynamics of seed size and seedling competitive ability. Theor. Popul. Biol. 55:324–343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gilbert, B. and Lechowicz, M.J. 2004. Neutrality, niches, and dispersal in a temperate forest understory. PNAS 101:7651–7656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Grace, J.B. 2006. Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge.

  34. Grime, J.P. 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86:902–910.

    Article  Google Scholar 

  35. Grman, E. and Suding, K.N. 2010. Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Rest. Ecol. 18:664–670.

    Article  Google Scholar 

  36. Guo, Q., Brown, J.H., Valone, T.J. and Kachman, S.D. 2000. Constraints of seed size on plant distribution and abundance. Ecology 81:2149–2155.

    Article  Google Scholar 

  37. Handel, S.N. 1985. The intrusion of clonal growth patterns on plant breeding systems. Am. Nat. 125:367–384.

    Article  Google Scholar 

  38. Harper, J.L. 1967. A Darwinian approach to plant ecology. J. Ecol. 55:247–270.

    Article  Google Scholar 

  39. Herben, T., Nováková, Z., Klimešová, J. and Hrouda, L. 2012. Species traits and plant performance: functional trade-offs in a large set of species in a botanical garden. J. Ecol. 100:1522–1533.

    Article  Google Scholar 

  40. Huston, M.A. 1979. A general hypothesis of species diversity. Am. Nat. 113:81–101.

    Article  Google Scholar 

  41. Lande, R.1993. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142:911–927

    Article  PubMed  PubMed Central  Google Scholar 

  42. Lee, T.D. 1988. Patterns of fruit and seed production. In: J. Lovett Doust and L. Lovett Doust (eds.), Plant Reproductive Ecology: Patterns and Strategies. Oxford University Press, New York. pp. 179–202.

    Google Scholar 

  43. Leishman, M.R. 2001. Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 93:294–302.

    Article  Google Scholar 

  44. Meekins, J.F. and McCarthy, B.C. 2000. Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability. J. Ecol. 88:447–463.

    Article  Google Scholar 

  45. Muller-Landau, H.C. 2010. The tolerance-fecundity trade-off and the maintenance of diversity in seed size. PNAS 107:4242–4247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Platt, W.J. 1975. The colonization and formation of equilibrium plant species associations on badger disturbances in a tall-grass prairie. Ecol. Monog. 45:285–305.

    Article  Google Scholar 

  47. Rangel, T.F., Diniz-Filho, J.A.F. and Bini, L.M. 2010. SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33:46–50.

    Article  Google Scholar 

  48. R Core Team 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

  49. Rees, M. 1995. Community structure in sand dune annuals: is seed weight a key quantity? J. Ecol. 83:857–863.

    Article  Google Scholar 

  50. Reynolds, H.L., Mittelbach, G.G., Darcy-Hall, T.L., Houseman, G.R. and Gross, K.L. 2007. No effect of varying soil resource heterogeneity on plant species richness in a low fertility grassland. J. Ecol. 95:723–733.

    Article  Google Scholar 

  51. Rosseel, Y. 2012. lavaan: An R package for structural equation modeling. J. Stat. Softw. 48:1–36.

    Article  Google Scholar 

  52. Scheller, R.M. and Mladenoff, D.J. 2002. Understory species patterns and diversity in old-growth and managed northern hardwood forests. Ecol. Appl. 12:1329–1343.

    Article  Google Scholar 

  53. Schütz, W. 2000. Ecology of seed dormancy and germination in sedges (Carex). Perspect. Plant. Ecol. Evol. Syst. 3:67–89.

    Article  Google Scholar 

  54. Schütz, W. and Rave, G. 2003. Variation in seed dormancy of the wetland sedge, Carex elongata, between populations and individuals in two consecutive years. Seed. Sci. Res. 13:315–322.

    Article  Google Scholar 

  55. Shaffer, M. 1981. Minimum population sizes for species conservation. BioScience 31:131–134.

    Article  Google Scholar 

  56. Shipley, B. 2004. Analysing the allometry of multiple interacting traits. Perspect. Plant. Ecol. Evol. Syst. 6:235–241.

    Article  Google Scholar 

  57. Soetaert, K. and Herman, P.M.J. 2009. A Practical Guide to Ecological Modelling. Using R as a Simulation Platform. Springer, Dordrecht.

  58. Thompson, F.L. and Eckert, C.G. 2004. Trade-offs between sexual and clonal reproduction in an aquatic plant: experimental manipulations vs. phenotypic correlations. J. Evol. Biol. 17:581–592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Tilman, D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75:2–16.

    Article  Google Scholar 

  60. van de Koppel, J. and Crain, C.M. 2006. Scale-dependent inhibition drives regular tussock spacing in a freshwater marsh. Am. Nat. 168:136–147.

    Article  Google Scholar 

  61. van Drunen, W.E. and Dorken, M.E. 2012. Trade-offs between clonal and sexual reproduction in Sagittaria latifolia (Alismataceae) scale up to affect the fitness of entire clones. New Phytol. 196:606–616.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Weiner, J., Campbell, L.G., Pino, J. and Echarte, L. 2009. The allometry of reproduction within plant populations. J. Ecol. 97:1220– 1233.

    Article  Google Scholar 

  63. Weppler, T., Stoll, P. and Stöcklin, J. 2006. The relative importance of sexual and clonal reproduction for population growth in the long-lived alpine plant Geum reptans. J. Ecol. 94:869–879.

    Article  Google Scholar 

  64. Wijesinghe, D.K., John, E.A. and Hutchings, M.J. 2005. Does pattern of soil resource heterogeneity determine plant community structure? An experimental investigation. J. Ecol. 93:99–112.

    Article  Google Scholar 

  65. Williams, R.D., Quimby, Jr. P.C. and Frick, K.E. 1977. Intraspecific competition of purple nutsedge (Cyperus rotundus) under greenhouse conditions. Weed Sci. 25:477–481.

    Article  Google Scholar 

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Correspondence to J. Douda.

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Appendix 1

Fitness-related data measured in field study. C. elo, Carex elongata ; C. ela, C. elata .

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Douda, J., Hulík, J. & Doudová, J. Vegetative sprouting as an additional pathway for a seed size-number trade-off: a field-parameterised simulation approach. COMMUNITY ECOLOGY 17, 205–215 (2016). https://doi.org/10.1556/168.2016.17.2.9

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Keywords

  • Carex elata
  • Carex elongata
  • Competition-colonisation trade-off
  • Functional traits
  • Sedges
  • Spatially explicit models
  • Structural equation models
  • Wetland forests