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Biologia

, Volume 74, Issue 5, pp 437–446 | Cite as

Shifts in the timing of the early flowering in plants from a semi-arid ecoregion under climate change

  • Fatih FazliogluEmail author
Original Article
  • 31 Downloads

Abstract

Climate change has been significantly changing ecosystems. Regarding angiosperms, elevated temperature has affected the flowering time of plants across habitats, where earlier flowering was induced. The impacts of climate change on vegetation are expected to be more pronounced in dry regions because of the high irregularity in precipitation and temperature. Assessment of the effects of the long-term climate change on plants is recently possible due to the increased digitization of historical herbarium specimens. For instance, these herbarium specimens can be used to detect changes in flowering time. In this study, the shifts in flowering time of plant species collected from a semi-arid region in the western USA (the Trans-Pecos ecoregion, Texas, USA) was analyzed using a herbarium database. A total of 7163 herbarium records from 172 species were examined. Statistically significant shifts were detected in the flowering day for the early flowering stage of 19 species in the semi-arid region from 1900 to 2017. According to t-test results, 9 species delayed flowering ranging between 17 and 50 days, whereas 10 species flowering started flowering ranging from 31 to 55 days earlier (p ≤ 0.05). Overall, these results contribute to a better understanding of the expression of plant reproductive strategies by revealing the plant responses to warming, and the ability of plants to respond climate change.

Keywords

Arid areas Climate change Herbarium specimens Phenology Reproductive condition 

Notes

Acknowledgments

Information provided here was retrieved from the database of Lundell Plant Diversity Portal of the University of Texas (TEX) and Lundell (LL) herbaria (https://prc-symbiota.tacc.utexas.edu). I would like to thank Dr. Justin S.H. Wan for linguistic advice and proofreading, and Ismail Yigit for ArcGIS guidance. I also would like to thank two anonymous reviewers for their insightful comments.

Compliance with ethical standards

Conflict of interest

The author declares no conflict of interest.

Supplementary material

11756_2018_175_MOESM1_ESM.xlsx (939 kb)
ESM 1 (XLSX 938 kb)

References

  1. Beaumont LJ, Hartenthaler T, Keatley MR, Chambers LE (2015) Shifting time: recent changes to the phenology of Australian species. Clim Res 63:203–214.  https://doi.org/10.3354/cr01294 CrossRefGoogle Scholar
  2. Borchert R, Rivera G (2001) Photoperiodic control of seasonal development and dormancy in tropical stem-succulent trees. Tree Physiol 21:213–221.  https://doi.org/10.1093/treephys/21.4.213 CrossRefGoogle Scholar
  3. Boulter SL, Kitching RL, Howlett BG (2006) Family, visitors and the weather: patterns of flowering in tropical rain forests of northern Australia. J Ecol 94:369–382.  https://doi.org/10.1111/j.1365-2745.2005.01084.x CrossRefGoogle Scholar
  4. Bowers JE (2005) El Nino and displays of spring-flowering annuals in the Mojave and Sonoran deserts. J Torrey Bot Soc 132:38–49. https://doi.org/10.3159/1095-5674(2005)132[38:ENADOS]2.0.CO;2Google Scholar
  5. Bowers JE (2007) Has climatic warming altered spring flowering date of Sonoran desert shrubs? Southwest Nat 52:347–355. https://doi.org/10.1894/0038-4909(2007)52[347:HCWASF]2.0.CO;2Google Scholar
  6. Campbell BD, Grime J (1992) An experimental test of plant strategy theory. Ecology 73:15–29.  https://doi.org/10.2307/1938717 CrossRefGoogle Scholar
  7. CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci U S A 111:4916–4921.  https://doi.org/10.1073/pnas.1323073111 CrossRefGoogle Scholar
  8. Chambers LE (2009) Evidence of climate related shifts in Australian phenology, 18th World Imacs Congress and Modsim09 International Congress on Modelling and Simulation: Interfacing Modelling and Simulation with Mathematical and Computational Sciences, JulyGoogle Scholar
  9. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field? Photosynthesis and growth. Ann Bot 89:907–916.  https://doi.org/10.1093/aob/mcf105. CrossRefGoogle Scholar
  10. Cheplick GP (1995) Genotypic variation and plasticity of clonal growth in relation to nutrient availability in Amphibromus scabrivalvis. J Ecol 83:459–468.  https://doi.org/10.2307/2261599 CrossRefGoogle Scholar
  11. Cleaveland MK, Votteler TH, Stahle DK, Casteel RC, Banner JL (2011) Extended chronology of drought in south central, southeastern and West Texas. Tex Water J 2:54–96Google Scholar
  12. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365.  https://doi.org/10.1016/j.tree.2007.04.003 CrossRefGoogle Scholar
  13. Davis CC, Willis CG, Connolly B, Kelly C, Ellison AM (2015) Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms. Am J Bot 102:1599–1609.  https://doi.org/10.3732/ajb.1500237 CrossRefGoogle Scholar
  14. Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johnston MO, Kelly JK, Moeller DA et al (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43.  https://doi.org/10.1016/j.tree.2009.06.013 CrossRefGoogle Scholar
  15. Etterson JR, Mazer SJ (2016) How climate change affects plants’ sex lives. Science 353:32–33.  https://doi.org/10.1126/science.aag1624 CrossRefGoogle Scholar
  16. Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. PNAS 104:1278–1282.  https://doi.org/10.1073/pnas.0608379104 CrossRefGoogle Scholar
  17. Gonzalez-Megias A, Menendez R (2012) Climate change effects on above- and below-ground interactions in a dryland ecosystem. Philos Trans R Soc Lond Ser B Biol Sci 367:3115–3124.  https://doi.org/10.1098/rstb.2011.0346 CrossRefGoogle Scholar
  18. Gallagher RV, Hughes L, Leishman MR (2009) Phenological trends among Australian alpine species: using herbarium records to identify climate-change indicators. Aust J Bot 57:1–9.  https://doi.org/10.1071/BT08051
  19. Hart R, Salick J, Ranjitkar S, Xu J (2014) Herbarium specimens show contrasting phenological responses to Himalayan climate. PNAS 111:10615–10619.  https://doi.org/10.1073/pnas.1403376111 CrossRefGoogle Scholar
  20. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485.  https://doi.org/10.1038/nature09670 CrossRefGoogle Scholar
  21. [ICARDA] International Center for Agricultural Research in the Dry Areas (2017) Enhancing resilience: helping dryland communities to thrive. ICARDA Annual Report 2016. International Center for Agricultural Research in the Dry Areas, Beirut, LebanonGoogle Scholar
  22. [IPCC] Intergovernmental Panel on Climate Change (2013) In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  23. Jones CA, Daehler CC (2018) Herbarium specimens can reveal impacts of climate change on plant phenology; a review of methods and applications. PeerJ 6:e4576.  https://doi.org/10.7717/peerj.4576 CrossRefGoogle Scholar
  24. Lauenroth WK, Bradford JB (2009) Ecohydrology of dry regions of the United States: precipitation pulses and intraseasonal drought. Ecohydrology 2:173–181.  https://doi.org/10.1002/eco.53 CrossRefGoogle Scholar
  25. Lavoie C (2013) Biological collections in an ever changing world: herbaria as tools for biogeographical and environmental studies. Perspect Plant Ecol Evol Syst 15:68–76.  https://doi.org/10.1016/j.ppees.2012.10.002 CrossRefGoogle Scholar
  26. Lehmann C, Rebele F (2005) Phenotypic plasticity in Calamagrostis epigejos (Poaceae): response capacities of genotypes from different populations of contrasting habitats to a range of soil fertility. Acta Oecol 28:127–140.  https://doi.org/10.1016/j.actao.2005.03.005 CrossRefGoogle Scholar
  27. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189.  https://doi.org/10.1016/S0169-5347(02)02497-7 CrossRefGoogle Scholar
  28. Lin D, Xia J, Wan S (2010) Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. New Phytol 188:187–198.  https://doi.org/10.1111/j.1469-8137.2010.03347.x
  29. Maestre FT, Eldridge DJ, Soliveres S, Kéfi S, Delgado-Baquerizo M, Bowker MA, García-Palacios P, Gaitán J, Gallardo A, Lázaro R et al (2016) Structure and functioning of dryland ecosystems in a changing world. Annu Rev Ecol Evol Syst 47:215–237.  https://doi.org/10.1146/annurev-ecolsys-121415-032311 CrossRefGoogle Scholar
  30. Magi M, Semchenko M, Kalamees R, Zobel K (2011) Limited phenotypic plasticity inrange-edge populations: a comparison of co-occurring populations of two Agrimonia species with different geographical distribution. Plant Biol 13:177–184.  https://doi.org/10.1111/j.1438-8677.2010.00342.x CrossRefGoogle Scholar
  31. Maroco JP, Pereira JS, Chaves MM (2000) Growth, photosynthesis and water-use efficiency of two C4 Sahelian grasses subjected to water deficits. J Arid Environ 45:119–137.  https://doi.org/10.1006/jare.2000.0638 CrossRefGoogle Scholar
  32. Melillo JM, Frey SD, DeAngelis KM, Werner WJ, Bernard MJ, Bowles FP, Pold G, Knorr MA, Grandy AS (2017) Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358:101–105.  https://doi.org/10.1126/science.aan2874 CrossRefGoogle Scholar
  33. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissolli P, Braslavska O, Briede et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976.  https://doi.org/10.1111/j.1365-2486.2006.01193.x CrossRefGoogle Scholar
  34. Miller-Rushing AJ, Primack RB, Primack D, Mukunda S (2006) Photographs and herbarium specimens as tools to document phenological changes in response to global warming. Am J Bot 93:1667–1674.  https://doi.org/10.3732/ajb.93.11.1667 CrossRefGoogle Scholar
  35. Munguia-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol Lett 14:511–521.  https://doi.org/10.1111/j.1461-0248.2011.01601.x CrossRefGoogle Scholar
  36. Munson SM, Long AL (2017) Climate drives shifts in grass phenology across the western U.S. New Phytol 213:1945–1955.  https://doi.org/10.1111/nph.14327 CrossRefGoogle Scholar
  37. Neil KL, Landrum L, Wu J (2010) Effects of urbanization on flowering phenology in the metropolitan phoenix region of USA: findings from herbarium records. J Arid Environ 74:440–444.  https://doi.org/10.1016/j.jaridenv.2009.10.010 CrossRefGoogle Scholar
  38. [NOAA] National Oceanic and Atmospheric Administration, National Centers for Environmental Information (2018) Climate at a Glance: U.S. Time Series, Average Temperature, published January 2018 from http://www.ncdc.noaa.gov/cag. Accessed Jan 2018
  39. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F et al (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692.  https://doi.org/10.1016/j.tplants.2010.09.008 CrossRefGoogle Scholar
  40. Osborne CP, Salomaa A, Kluyver TA, Visser V, Kellogg EA, Morrone O, Vorontsova MS, Clayton WD, Simpson DA (2014) A global database of C4 photosynthesis in grasses. New Phytol 204:441–446.  https://doi.org/10.1111/nph.12942 CrossRefGoogle Scholar
  41. Palmquist KA, Schlaepfer DR, Bradford JB, Lauenroth WK (2016) Spatial and ecological variation in dryland ecohydrological responses to climate change: implications for management. Ecosphere 7:e01590.  https://doi.org/10.1002/ecs2.1590 CrossRefGoogle Scholar
  42. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42.  https://doi.org/10.1038/nature01286 CrossRefGoogle Scholar
  43. Park IW, Schwartz MD (2015) Long-term herbarium records reveal temperature-dependent changes in flowering phenology in the southeastern USA. Int J Biometeorol 59:347–355.  https://doi.org/10.1007/s00484-014-0846-0 CrossRefGoogle Scholar
  44. Pei NC, Kress WJ, Chen BF, Erickson DL, Wong KM, Zhang JL, Ye WH, Huang ZL, Zhang DX (2015) Phylogenetic and climatic constraints drive flowering phenological patterns in a subtropical nature reserve. J Plant Ecol 8:187–196.  https://doi.org/10.1093/jpe/rtv009 CrossRefGoogle Scholar
  45. Primack D, Imbres C, Primack RB, Miller-Rushing AJ, Tredic PD (2004) Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Am J Bot 91:1260–1264.  https://doi.org/10.3732/ajb.91.8.1260 CrossRefGoogle Scholar
  46. Rafferty NE, Nabity PD (2017) A global test for phylogenetic signal in shifts in flowering time under climate change. J Ecol 105:627–633.  https://doi.org/10.1111/1365-2745.12701 CrossRefGoogle Scholar
  47. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993.  https://doi.org/10.1111/j.1461-0248.2006.00950.x CrossRefGoogle Scholar
  48. Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173.  https://doi.org/10.1016/j.agrformet.2012.09.012 CrossRefGoogle Scholar
  49. Runkle J, Kunkel K, Nielsen-Gammon J, Frankson R, Champion S, Stewart B, Romolo L, Sweet W (2017) Texas state climate summary. NOAA Technical Report NESDIS 149-TX, 4 ppGoogle Scholar
  50. Schauberger B, Archontoulis S, Arneth A, Balkovic J, Ciais P, Deryng D, Elliott J, Folberth C, Khabarov N, Müller C et al (2018) Consistent negative response of US crops to high temperatures in observations and crop models. Nat Commun 8:13931.  https://doi.org/10.1038/ncomms13931
  51. Schmidt-Lebuhn AN, Knerr NJ, Kessler M (2013) Non-geographic collecting biases in herbarium specimens of Australian daisies (Asteraceae). Biodivers Conserv 22:905–919.  https://doi.org/10.1007/s10531-013-0457-9 CrossRefGoogle Scholar
  52. Schwartz MD (2013) Phenology: an integrative environmental science. Springer, Netherlands 610 ppCrossRefGoogle Scholar
  53. Skubala P (2018) World scientists’ second warning to humanity: the time for change is now. Bioscience 68:238–239.  https://doi.org/10.1093/biosci/bix125
  54. Springer CJ, Ward JK (2007) Flowering time and elevated atmospheric CO2. New Phytol 176:243–255.  https://doi.org/10.1111/j.1469-8137.2007.02196.x CrossRefGoogle Scholar
  55. Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Bot Neerl 44:363–383.  https://doi.org/10.1111/j.1438-8677.1995.tb00793.x CrossRefGoogle Scholar
  56. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542.  https://doi.org/10.1016/S1360-1385(00)01797-0 CrossRefGoogle Scholar
  57. Temme AA, Liu JC, van Hal J, Cornwell WK, Cornelissen JHC, Aerts R (2017) Increases in CO2 from past low to future high levels result in “slower” strategies on the leaf economic spectrum. Perspect Plant Ecol Evol Syst 29:41–50.  https://doi.org/10.1016/j.ppees.2017.11.003 CrossRefGoogle Scholar
  58. [TPWD] Texas Parks and Wildlife Department (2018) https://tpwd.texas.gov/huntwild/wild/wildlife_diversity/wildscapes/ecoregions/ecoregion_10.phtml. Accessed Jan 2018
  59. [TWDB] Texas Water Development Board (2012) The 2012 state water plan, Chapter 4: Climate of Texas. p 145–155Google Scholar
  60. The IMBIE Team (2018) Mass balance of the Antarctic ice sheet from 1992 to 2017. Nature 558:219–222.  https://doi.org/10.1038/s41586-018-0179-y CrossRefGoogle Scholar
  61. [UN] United Nations Environment Management Group Report (2011) Global drylands: a UN system-wide response. United NationsGoogle Scholar
  62. Walther G, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395.  https://doi.org/10.1038/416389a CrossRefGoogle Scholar
  63. Walvoord MA, Phillips FM (2004) Identifying areas of basin-floor recharge in the trans-Pecos region and the link to vegetation. J Hydrol 292:59–74.  https://doi.org/10.1016/j.jhydrol.2003.12.029 CrossRefGoogle Scholar
  64. Whitford WG (2002) Ecology of desert systems. Academic, LondonGoogle Scholar
  65. Willis CG, Ellwood ER, Primack RB, Davis CC, Pearson KD, Gallinat AS, Yost JM, Nelson G, Mazer SJ, Rossington NL, Sparks TH, Soltis PS (2017) Old plants, new tricks: Phenological research using herbarium specimens. Trends Ecol Evol 32:531–546.  https://doi.org/10.1016/j.tree.2017.03.015 CrossRefGoogle Scholar
  66. Wright DK (2017) Humans as agents in the termination of the African humid period. Front Earth Sci 5:1–14.  https://doi.org/10.3389/feart.2017.00004

Copyright information

© Plant Science and Biodiversity Centre, Slovak Academy of Sciences 2018

Authors and Affiliations

  1. 1.Faculty of Arts and Sciences, Department of Molecular Biology and GeneticsOrdu UniversityOrduTurkey

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