Advertisement

Oecologia

, Volume 189, Issue 4, pp 1071–1082 | Cite as

Evidence of temporal niche separation via low flowering time overlap in an old-field plant community

  • Ashley M. Jensen
  • Brandon S. SchampEmail author
  • Angela Belleau
Community ecology – original research
  • 161 Downloads

Abstract

Flowering time is a trait that reflects the timing of specific resource requirements by plants. Consequently, several predictions have been made related to how species are assembled within communities according to flowering time. Strong overlap in flowering time among coexisting species may result from clustered abiotic resources, or contribute to improved pollination success. Conversely, low flowering time overlap (asynchrony) among coexisting species may reduce competition for soil, light, or pollinator resources and alleviate interspecific pollen transfer. Here, we present evidence that coexisting species in an old-field community generally overlap less in flowering time than expected under a commonly used and statistically validated null model. Flowering time asynchrony was more pronounced when abundance data were used (compared to presence-absence data), and when analyses focused on species that share bees as pollinators. Control and herbivore-exclusion plots did not differ in flowering time overlap, providing no evidence of the reduction in overlap expected to result from increased competition. Our results varied with the randomization algorithm used, emphasizing that the choice of algorithm can influence the outcome of null models. Our results varied between 2 years, with patterns being less clear in the second year, when both growing season and flowering times were contracted. Finally, we found evidence that further supports a previous finding that higher plot-level flowering time overlap was associated with higher proportions of introduced species. Reduced flowering time overlap among species in our focal community may promote coexistence via temporal niche differentiation and reduced competition for pollinators and other abiotic resources.

Keywords

Co-flowering Coexistence Community assembly Competition Flowering synchrony 

Notes

Acknowledgements

This research was supported by a Northern Ontario Heritage Foundation Internship to A. Jensen, a Natural Sciences and Engineering Research Council Undergraduate Student Research Award to A. Belleau, a Post-Secondary Education Fund for Aboriginal Learners Award to A. Belleau, the Algoma University Summer Work Program, and a Natural Sciences and Engineering Research Council Discovery Grant to B. Schamp (RGPIN-2015-04397). We thank the Ontario Forest Research Institute for use of their Arboretum for this research. We thank R. Gridzak for aiding in data collation and proof-reading, as well as J. Fresque, K. Mercer and K. Le for field work support.

Author contribution statement

BSS designed the study, AMJ conducted the analyses, AB led field data collection, and all three authors contributed to the writing and editing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2019_4386_MOESM1_ESM.docx (180 kb)
Supplementary material 1 (DOCX 180 kb)

References

  1. Anderson RC, Schelfhout S (1980) Phenological patterns among tallgrass prairie plants and their implications for pollinator competition. Am Midl Nat 104:253–263.  https://doi.org/10.2307/2424864 CrossRefGoogle Scholar
  2. Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary consequences. Ecology 85:2408–2421.  https://doi.org/10.1890/03-8024 CrossRefGoogle Scholar
  3. Ashton PS, Givnish TJ, Appanah S (1988) Evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44–66.  https://doi.org/10.1086/284837 CrossRefGoogle Scholar
  4. Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators in Hybanthus prunifolius (Violaceae). Ecology 62:775–788.  https://doi.org/10.2307/1937745 CrossRefGoogle Scholar
  5. Bar-Massada A, Yang Q, Shen G, Wang X (2018) Tree species co-occurrence patterns change across grains: insights from a subtropical forest. Ecosphere 9:1–12.  https://doi.org/10.1002/ecs2.2213 CrossRefGoogle Scholar
  6. Bartomeus I, Bosch J, Vilà M (2008) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Ann Bot 102:417–424.  https://doi.org/10.1093/aob/mcn109 CrossRefGoogle Scholar
  7. Beattie AJ, Breedlove DE, Ehrlich PR (1973) The ecology of the pollinators and predators of Frasera speciosa. Ecology 54:81–91.  https://doi.org/10.2307/1934376 CrossRefGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300Google Scholar
  9. Bernard-Verdier M, Navas ML, Vellend M, Violle C, Fayolle A, Garnier E (2012) Community assembly along a soil depth gradient: contrasting patterns of plant trait convergence and divergence in a Mediterranean rangeland. J Ecol 100:1422–1433.  https://doi.org/10.1111/1365-2745.12003 CrossRefGoogle Scholar
  10. Bjerknes AL, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12.  https://doi.org/10.1016/j.biocon.2007.04.015 CrossRefGoogle Scholar
  11. Brown BJ, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:43–49.  https://doi.org/10.1007/s004420100700 CrossRefGoogle Scholar
  12. Case TJ (1990) Invasion resistance arises in strongly interacting species-rich model competition communities. Proc Natl Acad Sci USA 87:9610–9614.  https://doi.org/10.1073/pnas.87.24.9610 CrossRefGoogle Scholar
  13. Castro-Arellano I, Lacher TE, Willig MR, Rangel TF (2010) Assessment of assemblage-wide temporal niche segregation using null models. Methods Ecol Evol 1:311–318.  https://doi.org/10.1111/j.2041-210X.2010.00031.x Google Scholar
  14. Cleland EE, Clark CM, Collins SL, Fargione JE, Gough L, Gross KL, Pennings SC, Suding KN (2011) Patterns of trait convergence and divergence among native and exotic species in herbaceous plant communities are not modified by nitrogen enrichment. J Ecol 99:1327–1338.  https://doi.org/10.1111/j.1365-2745.2011.01860.x CrossRefGoogle Scholar
  15. Dante SK, Schamp BS, Aarssen LW (2013) Evidence of deterministic assembly according to flowering time in an old-field plant community. Funct Ecol 27:555–564.  https://doi.org/10.1111/1365-2435.12061 CrossRefGoogle Scholar
  16. De Bello F, Carmona CP, Mason NWH, Sebastià MT, Lepš J (2013) Which trait dissimilarity for functional diversity: trait means or trait overlap? J Veg Sci 24:807–819.  https://doi.org/10.1111/jvs.12008 CrossRefGoogle Scholar
  17. Bersier LF, Sugihara G (1997) Species abundance patterns: the problem of testing stochastic models. J Anim Ecol 66:769.  https://doi.org/10.2307/5927 CrossRefGoogle Scholar
  18. Dietzsch AC, Stanley DA, Stout JC (2011) Relative abundance of an invasive alien plant affects native pollination processes. Oecologia 167:469–479.  https://doi.org/10.1007/s00442-011-1987-z CrossRefGoogle Scholar
  19. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439.  https://doi.org/10.1016/j.tree.2007.05.006 CrossRefGoogle Scholar
  20. Fantinato E, Del Vecchio S, Slaviero A, Conti L, Acosta ATR, Buffa G (2016) Does flowering synchrony contribute to the sustainment of dry grassland biodiversity? Flora Morphol Distrib Funct Ecol Plants 222:96–103.  https://doi.org/10.1016/j.flora.2016.04.003 CrossRefGoogle Scholar
  21. Fleming TH, Partridge BL (1984) On the analysis of phenological overlap. Oecologia 62:344–350.  https://doi.org/10.1007/BF00384266 CrossRefGoogle Scholar
  22. Götzenberger L, de Bello F, Bråthen KA, Davison J, Dubuis A, Guisan A, Lepš J, Lindborg R, Moora M, Pärtel M, Pellissier L, Pottier J, Vittoz P, Zobel K, Zobel M (2012) Ecological assembly rules in plant communities-approaches, patterns and prospects. Biol Rev 87:111–127.  https://doi.org/10.1111/j.1469-185x.2011.00187.x CrossRefGoogle Scholar
  23. Götzenberger L, Botta-Dukát Z, Lepš J, Pärtel M, Zobel M, de Bello F (2016) Which randomizations detect convergence and divergence in trait-based community assembly? A test of commonly used null models. J Veg Sci 27:1275–1287.  https://doi.org/10.1111/jvs.12452 CrossRefGoogle Scholar
  24. Heinrich B (1976) Flowering phenologies: bog, woodland, and disturbed habitats. Ecology 57:890–899.  https://doi.org/10.2307/1941055 CrossRefGoogle Scholar
  25. Heithaus ER (1974) The role of plant-pollinator interactions in determining community structure. Ann Missouri Bot Gard 61:675.  https://doi.org/10.2307/2395023 CrossRefGoogle Scholar
  26. Hurlbert SH (1970) Flower number, flowering time, and reproductive isolation among ten species of Solidago (Compositae). Bull Torrey Bot Club 97:189.  https://doi.org/10.2307/2483456 CrossRefGoogle Scholar
  27. Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140.  https://doi.org/10.1016/0169-5347(90)90218-3 CrossRefGoogle Scholar
  28. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492.  https://doi.org/10.1146/annurev.es.02.110171.002341 CrossRefGoogle Scholar
  29. Kipling RP, Warren J (2014) An investigation of temporal flowering segregation in species-rich grasslands. Ecol Res 29:213–224.  https://doi.org/10.1007/s11284-013-1116-z CrossRefGoogle Scholar
  30. Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497.  https://doi.org/10.1146/annurev.ecolsys.36.102403.115320 CrossRefGoogle Scholar
  31. Lavender TM, Schamp BS, Lamb EG (2016) The influence of matrix size on statistical properties of co-occurrence and limiting similarity null models. PLoS One 11:1–17.  https://doi.org/10.1371/journal.pone.0151146 CrossRefGoogle Scholar
  32. Lipson DA, Schadt CW, Schmidt SK (2002) Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microb Ecol 43:307–314.  https://doi.org/10.1007/s00248-001-1057-x CrossRefGoogle Scholar
  33. Macarthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385.  https://doi.org/10.1086/282505 CrossRefGoogle Scholar
  34. McKane RB, Grigal DF, Russelle MP (1990) Spatiotemporal differences in 15N uptake and the organization of an old-field plant community. Ecology 71:1126–1132.  https://doi.org/10.2307/1937380 CrossRefGoogle Scholar
  35. McNickle GG, Lamb EG, Lavender M, Cahill JF, Schamp BS, Siciliano SD, Condit R, Hubbell SP, Baltzer JL (2017) Checkerboard score-area relationships reveal spatial scales of plant community structure. Oikos 000:1–11.  https://doi.org/10.1111/oik.04620 Google Scholar
  36. Mittelbach GG, Gross KL (1984) Experimental studies of seed predation in old-fields. Oecologia 6:7–13.  https://doi.org/10.1007/BF00384455 CrossRefGoogle Scholar
  37. Mosquin T (1971) Competition for pollinators as a stimulus for evolution of flowering time. Oikos 22:398–402.  https://doi.org/10.2307/3543864 CrossRefGoogle Scholar
  38. Packer LA, Genaro JA, Sheffield CS (2007) The bee genera of eastern Canada. Can J Arthropod Identif 3:1–32.  https://doi.org/10.3752/cjai.2007.03 Google Scholar
  39. Parker IM (1997) Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub. Ecology 78:1457–1470.  https://doi.org/10.1890/0012-9658(1997)078%5b1457:PLOCSS%5d2.0.CO;2 CrossRefGoogle Scholar
  40. Parrish JAD, Bazzaz FA (1979) Difference in pollination niche relationships in early and late successional plant communities. Ecology 60:597–610.  https://doi.org/10.2307/1936080 CrossRefGoogle Scholar
  41. Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci 71:2141–2145.  https://doi.org/10.1073/pnas.71.5.2141 CrossRefGoogle Scholar
  42. Pleasants JM (1980) Competition for bumblebee pollinators in Rocky Mountain plant communities. Ecology 61:1446–1459.  https://doi.org/10.2307/1939053 CrossRefGoogle Scholar
  43. Pleasants JM (1990) Null-model tests for competitive displacement: the fallacy of not focusing on the whole community. Ecology 71:1078–1084.  https://doi.org/10.2307/1937376 CrossRefGoogle Scholar
  44. Pojar J (1974) Reproductive dynamics of four plant communities of southwestern British Columbia. Can J Bot 52:1819–1834.  https://doi.org/10.1139/b74-234 CrossRefGoogle Scholar
  45. Poulin B, Wright SJ, Lefebvre G, Calderón O (1999) Interspecific synchrony and asynchrony in the fruiting phenologies of congeneric bird-dispersed plants in Panama. J Trop Ecol 15:213–227.  https://doi.org/10.1017/S0266467499000760 CrossRefGoogle Scholar
  46. Rabinowitz D, Rapp JK, Sork VL, Rathcke BJ, Gary A, Weaver JC, Rapp JK (1981) Phenological properties of wind- and insect-pollinated prairie plants. Ecology 62:49–56.  https://doi.org/10.2307/1936667 CrossRefGoogle Scholar
  47. Rathcke B (1983) Competition and facilitation among plants for pollination. In: Real L (ed) Pollination biology. Academic Press, New York, pp 305–329CrossRefGoogle Scholar
  48. Rathcke B (1988a) Interactions for pollination among coflowering shrubs. Ecology 69:446–457.  https://doi.org/10.2307/1940443 CrossRefGoogle Scholar
  49. Rathcke B (1988b) Flowering phenologies in a shrub community: competition and constraints. J Ecol 76:975–994.  https://doi.org/10.2307/2260627 CrossRefGoogle Scholar
  50. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214.  https://doi.org/10.1146/annurev.es.16.110185.001143 CrossRefGoogle Scholar
  51. Richards MH, Rutgers-Kelly A, Gibbs J, Vickruck JL, Rehan SM, Sheffield CS (2011) Beediversity in naturalizing patches of Carolinian grasslands in southern Ontario, Canada. Can Entomol 143:279–299CrossRefGoogle Scholar
  52. Sargent RD, Ackerly DD (2008) Plant-pollinator interactions and the assembly of plant communities. Trends Ecol Evol 23:123–130.  https://doi.org/10.1016/j.tree.2007.11.003 CrossRefGoogle Scholar
  53. Schamp BS, Chau J, Aarssen LW (2008) Dispersion of traits related to competitive ability in an old-field plant community. J Ecol 96:204–212.  https://doi.org/10.1111/j.1365-2745.2007.0 Google Scholar
  54. Schamp B, Hettenbergerová E, Hájek M (2011) Testing community assembly predictions for nominal and continuous plant traits in species-rich grasslands. Preslia 83:329–346Google Scholar
  55. Schamp BS, Aarssen LW, Piggott GSJ, Dante SK (2016) The impact of non-reproductive plant species on assessments of community structure and species co-occurrence patterns. J Veg Sci 27:668–678.  https://doi.org/10.1111/jvs.12408 CrossRefGoogle Scholar
  56. Schemske DW (1981) Floral convergence and pollinator sharing in two bee-pollinated tropical herbs. Ecology 62:946–954.  https://doi.org/10.2307/1936993 CrossRefGoogle Scholar
  57. Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7.  https://doi.org/10.1023/B:PLSO.0000020933.32473.7e CrossRefGoogle Scholar
  58. Schoener TW (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51:408–418.  https://doi.org/10.2307/1935376 CrossRefGoogle Scholar
  59. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39.  https://doi.org/10.1126/science.185.4145.27 CrossRefGoogle Scholar
  60. Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto C, Carlucci MB, Cianciaruso MV, Dantas VL, de Bello F, Duarte LDS, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kichenin E, Kraft NJB, Lagerström A, Bagousse-Pinguet YL, Li Y, Mason N, Messier J, Nakashizuka T, Overton JM, Peltzer DA, Pérez-Ramos IM, Pillar VD, Prentice HC, Richardson S, Sasaki T, Schamp BS, Schöb C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M, Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol Lett 18:1406–1419.  https://doi.org/10.1111/ele.12508 CrossRefGoogle Scholar
  61. Smythe N (1970) Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. Am Nat 104:25–35.  https://doi.org/10.1086/282638 CrossRefGoogle Scholar
  62. Snow DW (1965) A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15:274–281.  https://doi.org/10.2307/3565124 CrossRefGoogle Scholar
  63. Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Ecology 12:253–279.  https://doi.org/10.1146/annurev.es.12.110181.001345 Google Scholar
  64. Stiles FG (1977) Coadapted competitors: the flowering seasons of hummingbird-pollinated plants in a tropical forest. Science 198:1177–1178.  https://doi.org/10.1126/science.198.4322.1177 CrossRefGoogle Scholar
  65. Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. Proc Natl Acad Sci 103:5841–5845.  https://doi.org/10.1073/pnas.0508073103 CrossRefGoogle Scholar
  66. Stubbs WJ, Wilson JB (2004) Evidence for limiting similarity in a sand dune community. J Ecol 92:557–567.  https://doi.org/10.2307/3237078 CrossRefGoogle Scholar
  67. Taylor DR, Aarssen LW, Loehle C (1990) On the relationship between r/K selection and environmental carrying capacity: a new habitat templet for plant life history strategies. Oikos 58:239–250.  https://doi.org/10.2307/3545432 CrossRefGoogle Scholar
  68. Ulrich W, Gotelli NJ (2010) Null model analysis of species associations using abundance data. Ecology 91:3384–3397.  https://doi.org/10.1890/09-2157.1 CrossRefGoogle Scholar
  69. Waser NM (1978) Interspecific pollen transfer and competition between co-occurring plant species. Oecologia 36:223–236.  https://doi.org/10.1007/BF00349811 CrossRefGoogle Scholar
  70. Wilson JB, Stubbs WJ (2012) Evidence for assembly rules: limiting similarity within a saltmarsh. J Ecol 100:210–221.  https://doi.org/10.1111/j.1365-2745.2011.01891.x CrossRefGoogle Scholar
  71. Zhang WP, Liu GC, Sun JH, Fornara D, Zhang LZ, Zhang FF, Li L (2017) Temporal dynamics of nutrient uptake by neighbouring plant species: Evidence from intercropping. Funct Ecol 31:469–479.  https://doi.org/10.1111/1365-2435.12732 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Ashley M. Jensen
    • 1
  • Brandon S. Schamp
    • 1
    Email author
  • Angela Belleau
    • 1
  1. 1.Department of BiologyAlgoma UniversitySault Ste. MarieCanada

Personalised recommendations