Advertisement

Plant Ecology

, Volume 220, Issue 10, pp 901–915 | Cite as

Consequences of reduced light for flower production in conifer-invaded meadows of the Pacific Northwest, U.S.A

  • Jessica CelisEmail author
  • Charles B. Halpern
  • Ariel Muldoon
Article
First Online:

Abstract

Woody-plant encroachment threatens the biodiversity and ecosystem functioning of grasslands and meadows worldwide. An important but rarely described consequence of the transition to woody-plant dominance is the reduction in flowering of herbaceous species. We modeled community-wide relationships between flowering and light in two tree-invaded meadows (BG and M1) in the western Cascade Range, Oregon (USA). At BG, trees established over two centuries, forming a gradient of encroachment states (open meadow to old forest) and declining levels of light (91% to 8%), with most (85%) of the decline occurring within 2–4 decades of tree establishment. At M1, where trees formed distinct edges, we also tested whether distance from edge can serve as proxy for light in modeling flowering response. Flowering declined significantly with reductions in light at both sites: for a 10-percentage-point reduction in light, probability of flowering decreased by 35% (BG) and 21% (M1), median flowering density (flowers per m2) by 15% and 8%, and median flowering effort (density per unit cover) by 10% and 9%, respectively. At M1, distance to edge was a poorer predictor of flowering due to its nonlinear relationship with light: > 80% of the reduction in light occurred within 4.5 m of the edge. Our results reveal strong, nonlinear relationships of flowering in time (most rapid early in the invasion process) and space (steepest at the forest edge). In a landscape dominated by forests, conifer invasion of mountain meadows can reduce the local and larger-scale diversity of plants and their insect pollinators.

Keywords

Conifer encroachment Flower production Meadow species Light Pollinators 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank K. Dymek and C. Parson for field and lab assistance. F. A. Jones provided guidance on study design. J. Antos, T. Kaye, and two anonymous reviewers provided helpful comments on earlier drafts. Funding was provided by the H. J. Andrews Experimental Forest LTER Program. Celis received scholarships from the Portland Garden Club and the Moldenke Fund for Plant Systematics (Department of Botany and Plant Pathology, OSU).

Supplementary material

11258_2019_952_MOESM1_ESM.docx (7.2 mb)
Supplementary file1 (DOCX 7366 kb)

References

  1. Aarssen LW, Jordan C (2001) Between-species patterns of covariation in plant size, seed size and fecundity in monocarpic herbs. Ecoscience 8:471–477.  https://doi.org/10.1080/11956860.2001.11682677 CrossRefGoogle Scholar
  2. Aarssen LW, Taylor DR (1992) Fecundity allocation in herbaceous plants. Oikos 65:225–232.  https://doi.org/10.2307/3545013 CrossRefGoogle Scholar
  3. Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980.  https://doi.org/10.1111/j.1461-0248.2006.00927.x CrossRefPubMedGoogle Scholar
  4. Aizen MA, Ashworth L, 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 CrossRefGoogle Scholar
  5. Albrecht MA, Becknell RE, Long Q (2016) Habitat change in insular grasslands: woody plant encroachment alters the population dynamics of a rare ecotonal plant. Biol Conserv 196:93–102.  https://doi.org/10.1016/j.biocon.2016.01.032 CrossRefGoogle Scholar
  6. Amiotti NM, Zalba P, Sanchez LF, Peinemann N (2000) The impact of single trees on properties of loess-derived grassland soils in Argentina. Ecology 81:3283–3290.  https://doi.org/10.1890/0012-9658(2000)081[3283:TIOSTO]2.0.CO;2 CrossRefGoogle Scholar
  7. Archer S, Schimel DS, Holland EA (1995) Mechanisms of shrubland expansion: land use, climate or CO2? Clim Change 29:91–99.  https://doi.org/10.1007/BF01091640 CrossRefGoogle Scholar
  8. Bagaria G, Roda F, Clotet M, Miguez S, Pino J (2017) Contrasting habitat and landscape effects on the fitness of a long-lived grassland plant under forest encroachment: do they provide evidence for extinction debt? J Ecol 106:278–288.  https://doi.org/10.1111/1365-2745.12860 CrossRefGoogle Scholar
  9. Baker SC, Spies TA, Wardlaw TJ, Balmer J, Franklin JF, Jordan GJ (2013) The harvested side of edges: effect of retained forests on the re-establishment of biodiversity in adjacent harvested areas. For Ecol Manage 302:107–121.  https://doi.org/10.1016/j.foreco.2013.03.024 CrossRefGoogle Scholar
  10. Barger NN, Archer SA, Campbell JL, Huang C, Morton JA, Knapp AK (2011) Woody plant proliferation in North American drylands: a synthesis of impacts on ecosystem carbon balance. J Geophys Res 116:G00K07.  https://doi.org/10.1029/2010JG001506 CrossRefGoogle Scholar
  11. Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278.  https://doi.org/10.1016/j.jml.2012.11.001 CrossRefGoogle Scholar
  12. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1-7. https://CRAN.Rproject.org/package=lme4. Accessed 14 Feb 2018
  13. Bazzaz FA, Reekie EG (1985) The meaning and measurement of reproductive effort in plants. In: White J (ed) Studies in plant demography: a Festschrift for John L. Harper. Academic Press, LondonGoogle Scholar
  14. Bellow JG, Nair PKR (2003) Comparing common methods for assessing understory light availability in shaded-perennial agroforestry systems. Agric For Meteorol 114:197–211.  https://doi.org/10.1016/S0168-1923(02)00173-9 CrossRefGoogle Scholar
  15. Biesmeijer JC, Roberts SP, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354.  https://doi.org/10.1126/science.1127863 CrossRefPubMedGoogle Scholar
  16. Briggs JM, Knapp AK, Blair JM, Heisler JL, Hoch GA, Lett MA, McCarron JK (2005) An ecosystem in transition: causes and consequences of the conversion of mesic grassland to shrubland. Bioscience 55:243–254.  https://doi.org/10.1641/0006-3568(2005)055[0243:AEITCA]2.0.CO;2 CrossRefGoogle Scholar
  17. Burkle LA, Alarcón R (2011) The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot 98:528–538.  https://doi.org/10.3732/ajb.1000391 CrossRefPubMedGoogle Scholar
  18. Cadenasso ML, Traynor MM, Pickett STA (1997) Functional location of forest edges: gradients of multiple physical factors. Can J For Res 27:774–782.  https://doi.org/10.1139/x97-013 CrossRefGoogle Scholar
  19. Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051.  https://doi.org/10.2307/1940474 CrossRefGoogle Scholar
  20. Cao GX, Wu BX, Xu XJ, Wang X, Yang CP (2017) The effects of local variation in light availability on pollinator visitation, pollen and resource limitation of female production in Hosta ventricosa. Bot Stud 58:24.  https://doi.org/10.1186/s40529-017-0180-z CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ceballos G, Davidson A, List R, Pacheco J, Manzano-Fischer P, Santos-Barrera G, Cruzado J (2010) Rapid decline of a grassland ecosystem and its ecological and conservation implications. PLoS ONE 5:e8562.  https://doi.org/10.1371/journal.pone.0008562 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Celis J (2015) The role of intraspecific functional trait variation in the differential decline of meadow species following conifer encroachment. Thesis, Oregon State University, CorvallisGoogle Scholar
  23. Celis J, Halpern CB, Jones FA (2017) Intraspecific trait variation and the differential decline of meadow species during conifer encroachment. Plant Ecol 218:565–578.  https://doi.org/10.1007/s11258-017-0712-3 CrossRefGoogle Scholar
  24. Dailey MM (2007) Meadow classification in the Willamette National Forest and conifer encroachment patterns in the Chucksney-Grasshopper Meadow Complex, western Cascade Range. Thesis, Oregon State University, Corvallis, OregonGoogle Scholar
  25. Dauber J, Biesmeijer JC, Gabriel D, Kunin WE, Lamborn E, Meyer B, Nielsen A, Potts SG, Roberts SPM, Sõber V, Settele J, Steffan-Dewenter I, Stout JC, Teder T, Tscheulin T, Vivarelli D, Petanidou T (2010) Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach. J Ecol 98:188–196.  https://doi.org/10.1111/j.1365-2745.2009.01590.x CrossRefGoogle Scholar
  26. Dorado J, Vázquez DP (2014) The diversity-stability relationship in floral production. Oikos 123:1137–1143.  https://doi.org/10.1111/oik.00983 CrossRefGoogle Scholar
  27. Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722.  https://doi.org/10.1111/j.1461-0248.2011.01630.x CrossRefPubMedPubMedCentralGoogle Scholar
  28. Engelbrecht BM, Herz HM (2001) Evaluation of different methods to estimate understorey light conditions in tropical forests. J Trop Ecol 17:207–224.  https://doi.org/10.1139/X09-116 CrossRefGoogle Scholar
  29. Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA): imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs. Users’ manual and program documentation, Version 2.0. Simon Fraser University and the Institute of Ecosystem Studies, Burnaby and MillbrookGoogle Scholar
  30. Griffiths R, Madritch M, Swanson A (2005) Conifer invasion of meadows transforms soil characteristics in the Pacific Northwest. For Ecol Manage 208:347–358.  https://doi.org/10.1016/j.foreco.2005.01.015 CrossRefGoogle Scholar
  31. Hadley AS, Betts MG (2011) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544.  https://doi.org/10.1111/j.1469-185X.2011.00205.x CrossRefPubMedGoogle Scholar
  32. Hadley K (1999) Forest history and meadow invasion at the Rigdon Meadows archaeological site, western Cascades, Oregon. Phys Geogr 20:116–133.  https://doi.org/10.1080/02723646.1999.10642672 CrossRefGoogle Scholar
  33. Halpern CB, Antos JA, Kothari S, Olson AM (2019) Past tree influence and prescribed fire exert strong controls on reassembly of mountain grasslands after tree removal. Ecol Appl 29:e01860.  https://doi.org/10.1002/eap.1860 CrossRefPubMedGoogle Scholar
  34. Halpern CB, Antos JA, McKenzie D, Olson, M (2016) Past tree influence and prescribed fire mediate biotic interactions and community reassembly in a grassland-restoration experiment. J Appl Ecol 53:264–273.  https://doi.org/10.1111/1365-2664.12570 CrossRefGoogle Scholar
  35. Halpern CB, Antos JA, Rice JM, Haugo RM, Lang NL (2010) Tree invasion of a montane meadow complex: temporal trends, spatial patterns, and biotic interactions. J Veg Sci 21:717–732.  https://doi.org/10.1111/j.1654-1103.2010.01183.x CrossRefGoogle Scholar
  36. Halpern CB, Haugo RD, Antos JA, Kaas SS, Kilanowski AL (2012) Grassland restoration with and without fire: evidence from a tree-removal experiment. Ecol Appl 22:425–441.  https://doi.org/10.1890/11-1061.1 CrossRefPubMedGoogle Scholar
  37. Hartig F (2017) Package DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.1.5. https://CRAN.R-project.org/package=DHARMa. Accessed 10 Mar 2018
  38. Haugo RD, Halpern CB (2007) Vegetation responses to conifer encroachment in a western Cascade meadow: a chronosequence approach. Botany 88:285–298.  https://doi.org/10.1139/B07-024 CrossRefGoogle Scholar
  39. Haugo RD, Halpern CB (2010) Tree age and tree species shape positive and negative interactions in a montane meadow. Botany 88:488–499.  https://doi.org/10.1139/B10-018 CrossRefGoogle Scholar
  40. Heithecker TD, Halpern CB (2007) Edge-related gradients in microclimate in forest aggregates following structural retention harvests in western Washington. For Ecol Manage 248:163–173.  https://doi.org/10.1016/j.foreco.2007.05.003 CrossRefGoogle Scholar
  41. Helderop E (2015) Diversity, generalization, and specialization in plant-pollinator networks of montane meadows, western Cascades. Thesis, Oregon State University, CorvallisGoogle Scholar
  42. Hickman JC (1976) Non-forest vegetation of the central western Cascade Mountains of Oregon. Northwest Sci 50:145–155Google Scholar
  43. Highland SA, Miller JC, Jones JA (2013) Determinants of moth diversity and community in a temperate landscape: vegetation, topography, and seasonality. Ecosphere 4:129.  https://doi.org/10.1890/ES12-00384.1 CrossRefGoogle Scholar
  44. Jensen K, Meyer C (2001) Effects of light competition and litter on performance of Viola palustris and on species composition and diversity of an abandoned fen meadow. Plant Ecol 155:169–181.  https://doi.org/10.1023/A:1013270628964 CrossRefGoogle Scholar
  45. Johnson PCD (2014) Extension of Nakagawa & Schielzeth's R2 GLMM to random slopes models. Methods Ecol Evol 5:944–946.  https://doi.org/10.1111/2041-210X.12225 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jones KE (2016) Spatio-temporal patterns of tree establishment in the M1 meadow of the HJ Andrews Experimental Forest. Thesis. Oregon State University, CorvallisGoogle Scholar
  47. Jones JA, Hutchinson R, Moldenke A, Pfeiffer V, Helderop E, Thomas E, Griffin J, Reinholtz A (2019) Landscape patterns and diversity of meadow plants and flower-visitors in a mountain landscape. Landsc Ecol 34:997–1014.  https://doi.org/10.1007/s10980-018-0740-y CrossRefGoogle Scholar
  48. Kato E, Hiura T (1999) Fruit set in Styrax obassia (Styracaceae): the effect of light availability, display size, and local floral density. Am J Bot 86:495–501.  https://doi.org/10.2307/2656810 CrossRefPubMedGoogle Scholar
  49. Kilkenny FF, Galloway LF (2008) Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators. Oecologia 155:247–255.  https://doi.org/10.1007/s00442-007-0903-z CrossRefPubMedGoogle Scholar
  50. Lang NL, Halpern CB (2007) The soil seed bank of a montane meadow: consequences of conifer encroachment and implications for restoration. Can J Bot 85:557–569.  https://doi.org/10.1139/B07-051 CrossRefGoogle Scholar
  51. Lettow MC, Brudvig LA, Bahlai CA, Landis DA (2014) Oak savanna management strategies and their differential effects on vegetative structure, understory light, and flowering forbs. For Ecol Manage 329:89–98.  https://doi.org/10.1016/j.foreco.2014.06.019 CrossRefGoogle Scholar
  52. Lindh BC (2008) Flowering of understory herbs following thinning in the western Cascades, Oregon. For Ecol Manage 256:929–936.  https://doi.org/10.1016/j.foreco.2008.05.055 CrossRefGoogle Scholar
  53. Lindh BC, Gray AN, Spies TA (2003) Responses of herbs and shrubs to reduced root competition under canopies and in gaps: a trenching experiment in old-growth Douglas-fir forests. Can J For Res 33:2052–2057.  https://doi.org/10.1139/x03-120 CrossRefGoogle Scholar
  54. Lugassi-Ben-Hamo M, Kitron M, Bustan A, Zaccai M (2010) Effect of shade regime on flower development, yield and quality in lisianthus. Sci Hortic 124:248–253.  https://doi.org/10.1016/j.scienta.2009.12.030 CrossRefGoogle Scholar
  55. Machado J-L, Reich PB (1999) Evaluation of several measures of canopy openness as predictors of photosynthetic photon flux density in deeply shaded conifer-dominated forest understory. Can J For Res 29:1438–1444.  https://doi.org/10.1139/x99-102 CrossRefGoogle Scholar
  56. McCain C, Halpern CB, Lovtang S (2014) Non-forested plant communities of the northern Oregon Cascades. USDA Forest Service Technical Paper R6-ECOL-TP-01-14Google Scholar
  57. Miller EA, Halpern CB (1998) Effects of environment and grazing disturbance on tree establishment in meadows of the central Cascade Range, Oregon, USA. J Veg Sci 9:265–282.  https://doi.org/10.2307/3237126 CrossRefGoogle Scholar
  58. Mustajärvi K, Siikamäki P, Rytkönen S, Lammi A (2001) Consequences of plant population size and density for plant-pollinator interactions and plant performance. J Ecol 89:80–87.  https://doi.org/10.1046/j.1365-2745.2001.00521.x CrossRefGoogle Scholar
  59. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.  https://doi.org/10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  60. Niemandt C, Greve M (2016) Fragmentation metric proxies provide insights into historical biodiversity loss of critically endangered grassland. Agric Ecosyst Environ 235:172–181.  https://doi.org/10.1016/j.agee.2016.10.018 CrossRefGoogle Scholar
  61. NRCS (National Resource Conservation Service) (2018) National cooperative soil characterization database. https://websoilsurvey.sc.egov.usda.gov/App/. Accessed 2 Dec 2018
  62. O’Donnell FC, Caylor KK (2012) A model-based evaluation of woody plant encroachment effects on coupled carbon and water cycles. J Geophys Res 117:G02012.  https://doi.org/10.1029/2011JG001899 CrossRefGoogle Scholar
  63. Paradiso R, De Pascale S (2014) Effects of plant size, temperature, and light intensity on flowering of Phalaenopsis hybrids in Mediterranean greenhouses. Sci World J 2014:420807.  https://doi.org/10.1155/2014/420807 CrossRefGoogle Scholar
  64. Pitelka LF, Stanton DS, Peckenham MO (1980) Effects of light and density on resource allocation in a forest herb, Aster acuminatus (Compositae). Am J Bot 67:942–948.  https://doi.org/10.1002/j.1537-2197.1980.tb07724.x CrossRefGoogle Scholar
  65. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 21 Jan 2018
  66. Ratajczak Z, Nippert JB, Collins SL (2012) Woody encroachment decreases diversity across North American grasslands and savannas. Ecology 93:697–703.  https://doi.org/10.1890/11-1199.1 CrossRefPubMedGoogle Scholar
  67. Rice JM, Halpern CB, Antos JA, Jones JA (2012) Spatio-temporal patterns of tree establishment are indicative of biotic interactions during early invasion of a montane meadow. Plant Ecol 213:555–568.  https://doi.org/10.1007/s11258-012-0021-9 CrossRefGoogle Scholar
  68. Sabatino M, Maceira N, Aizen MA (2010) Direct effects of habitat area on interaction diversity in pollination webs. Ecol Appl 20:1491–1497.  https://doi.org/10.1890/09-1626.1 CrossRefPubMedGoogle Scholar
  69. Scholes RJ, Archer SR (1997) Tree-grass interactions in savannas. Ann Rev Ecol Syst 28:517–544.  https://doi.org/10.1146/annurev.ecolsys.28.1.517 CrossRefGoogle Scholar
  70. Seidel D, Fleck S, Leuschner C, Hammett T (2011) Review of ground-based methods to measure the distribution of biomass in forest canopies. Ann For Sci 68:225–244.  https://doi.org/10.1007/s13595-011-0040-z CrossRefGoogle Scholar
  71. Takaoka S, Swanson FJ (2008) Change in extent of meadows and shrub fields in the central western Cascade Range, Oregon. Prof Geogr 60:527–540. ISSN: 0033-0124Google Scholar
  72. USDA, NRCS. 2019. The PLANTS database. National Plant Data Team, Greensboro, NC. https://plants.usda.gov. Accessed 6 Apr 2019
  73. Vale TR (1981) Tree invasion of montane meadows in Oregon. Am Midl Nat 105:61–69.  https://doi.org/10.2307/242501 CrossRefGoogle Scholar
  74. Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol 6:207–215.  https://doi.org/10.1078/1433-8319-00083 CrossRefGoogle Scholar
  75. Weiner J, Campbell LG, Pino J, Echarte L (2009) The allometry of reproduction within plant populations. J Ecol 97:1220–1233.  https://doi.org/10.1111/j.1365-2745.2009.01559.x CrossRefGoogle Scholar
  76. Welles JM, Cohen S (1996) Canopy structure measurement by gap fraction analysis using commercial instrumentation. J Exp Bot 47:1335–1342.  https://doi.org/10.1093/jxb/47.9.1335 CrossRefGoogle Scholar
  77. Xie XF, Hu YK, Pan X, Liu FH, Song YB, Dong M (2006) Biomass allocation of stoloniferous and rhizomatous plant in response to resource availability: a phylogenetic meta-analysis. Front Plant Sci 7:603.  https://doi.org/10.3389/fpls.2016.00603 CrossRefGoogle Scholar
  78. Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10. https://CRAN.R-project.org/doc/Rnews/. Accessed 15 Mar 2018
  79. Zhao D, Hao Z, Tao J (2012) Effects of shade on plant growth and flower quality in the herbaceous peony (Paeonia lactiflora Pall.). Plant Physiol Biochem 61:187–196.  https://doi.org/10.1016/j.plaphy.2012.10.005 CrossRefPubMedGoogle Scholar
  80. Zuur A, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute for Applied EcologyCorvallisUSA
  2. 2.School of Environmental and Forest SciencesUniversity of WashingtonSeattleUSA
  3. 3.College of ForestryOregon State UniversityCorvallisUSA

Personalised recommendations

Cite article

Buy options