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Photosynthetica

, Volume 56, Issue 3, pp 776–785 | Cite as

Bi-directional acclimation of Cycas micronesica leaves to abrupt changes in incident light in understory and open habitats

  • T. E. MarlerEmail author
Article

Abstract

Leaf gas-exchange responses to shadefleck–sunfleck and sun–cloud transitions were determined for in situ Cycas micronesica K.D. Hill plants on the island of Guam to add cycads to the published gymnosperm data. Sequential sunfleck–shadefleck transitions indicated understory leaves primed rapidly but open field leaves primed slowly. Time needed to reach 90% induction of net CO2 assimilation (PN) was 2.9 min for understory leaves and 13.9 min for open field leaves. Leaf responses to sun–cloud transitions exhibited minimal adjustment of stomatal conductance, so PN rapidly returned to precloud values following cloud–sun transitions. Results indicate bi-directional leaf acclimation behavior enables mature C. micronesica trees to thrive in deep understory conditions in some habitats and as emergent canopy trees in other habitats. These data are the first nonconifer gymnosperm data; the speed of gas-exchange responses to rapid light transitions was similar to some of the most rapid angiosperm species described in the literature.

Additional key words

cycad dynamic leaf photosynthesis fluctuating light phenotypic plasticity photosynthetic induction 

Abbreviations

E

transpiration

gs

stomatal conductance to water

IS60s

photosynthetic induction state following 1 min of induction

PN

net CO2 assimilation

PN initial

PN during initial diffuse light of shadeflecks

PN 60s

PN at 1 min induction

PNmax

maximum PN

RD

dark respiration

t50%

time to reach 50% photosynthetic induction

t90%

time to reach 90% photosynthetic induction

WUE

instantaneous water-use efficiency (PN/E)

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References

  1. Álvarez-Yépiz J.C., Búrquez A., Dovciak M.: Ontogenetic shifts in plant-plant interactions in a rare cycad within angiosperm communities.–Oecologia 175: 725–735, 2014a.CrossRefPubMedGoogle Scholar
  2. Álvarez-Yépiz J.C., Cueva A., Dovciak M., et al.: Ontogenetic resource-use strategies in a rare long-lived cycad along environmental gradients.–Conserv. Physiol. 2: cou034, 2014b.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Andersen P.C.: Leaf gas exchange of 11 species of fruit crops with reference to sun tracking/non-sun-tracking responses.–Can. J. Plant Sci. 71: 1183–1193, 1991.CrossRefGoogle Scholar
  4. Bai K.D., Liao D.B., Jiang D.B. et al.: Photosynthetic induction in leaves of co-occurring Fagus lucida and Castanopsis lamontii saplings grown in contrasting light environments.–Trees 22: 449–462, 2008.CrossRefGoogle Scholar
  5. Brantley S.T. Young D.R.: Linking light attenuation, sunflecks, and canopy architecture in mesic shrub thickets.–Plant Ecol. 206: 225–236, 2010.CrossRefGoogle Scholar
  6. Brenner E.D., Stevenson D.W., Twigg R.W.: Cycads: evolutionary innovations and the role of plant-derived neurotoxins.–Trend. Plant Sci. 8: 446–452, 2003.CrossRefGoogle Scholar
  7. Brodribb T.J., Feild T.S., Jordan G.J.: Leaf maximum photosynthetic rate and venation are linked by hydraulics.–Plant Physiol. 144: 1890–1898, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brummitt N.A., Bachman S.P., Griffiths-Lee J. et al.: Green plants in the red: A baseline global assessment for the IUCN sampled Red List Index for plants.–PLoS ONE 10: e0135152, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Burgess A.J., Retkute R., Preston S.P. et al.: The 4-dimensional plant: Effects of wind-induced canopy movement on light fluctuations and photosynthesis.–Front. Plant Sci. 7: 1392, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Calonje M., Stevenson D.W., Stanberg L.: The World List of Cycads. Available from: http://www.cycadlist.org, 2016.Google Scholar
  11. Chazdon R.L.: Sunflecks and their importance to forest understorey plants.–Adv. Ecol. Res. 18: 1–63, 1988.CrossRefGoogle Scholar
  12. Chazdon R.L., Pearcy R.W.: The importance of sunflecks for forest understory plants.–BioScience 41: 760–766, 1991.CrossRefGoogle Scholar
  13. Chen H.Y.H., Klinka K.: Light availability and photosynthesis of Pseudotsuga menziesii seedlings grown in the open and in the forest understory.–Tree Physiol. 17: 23–29, 1997.CrossRefPubMedGoogle Scholar
  14. Clark D.B., Clark D.A., Grayum M.H.: Leaf demography of a neotropical rain forest cycad, Zamia skinneri (Zamiaceae).–Am. J. Bot. 79: 28–33, 1992.CrossRefGoogle Scholar
  15. Clemente H.S., Marler T.E.: Drought stress influences gasexchange responses of papaya leaves to rapid light transition.–J. Am. Soc. Hortic. Sci. 121: 292–295, 1996.Google Scholar
  16. Fisher J.B., Lindström A., Marler T.E.: Tissue responses and solution movement after stem wounding in six Cycas species.–HortScience 44: 848–851, 2009.Google Scholar
  17. Fragnière Y., Bétrisey S., Cardinaux L. et al.: Fighting their last stand? A global analysis of the distribution and conservation status of gymnosperms.–J. Biogeogr. 42: 809–820, 2015.CrossRefGoogle Scholar
  18. Garcia S., Kovarí k A.: Dancing together and separate again: gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organization.–Heredity 111: 23–33, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Goldstein G., Santiago L.S., Campanello P.I. et al.: Facing shortage or excessive light: how tropical and subtropical trees adjust their photosynthetic behavior and life history traits to a dynamic forest environment.–In: Goldstein G., Santiago L.S. (ed.): Tropical Tree Physiology, Vol. 6. Pp. 319–336. Springer, London 2016.CrossRefGoogle Scholar
  20. Greguss P.: Xylotomy of the Living Cycad. Pp. 260. Akadémiai Kiadó, Budapest 1968.Google Scholar
  21. Han Q., Yamaguchi E., Odaka N. et al.: Photosynthetic induction responses to variable light under field conditions in three species grown in the gap and understory of a Fagus crenata forest.–Tree Physiol. 19: 625–634, 1999.CrossRefPubMedGoogle Scholar
  22. Hutchinson G.E.: Concluding remarks.–Cold Spring Harb. Symp. Quant. Biol. 22: 415–427, 1957.CrossRefGoogle Scholar
  23. Knapp A.K., Smith W.K.: Influence of growth form and water relations on stomatal and photosynthetic responses to variable sunlight in subalpine plants.–Ecology 70: 1069–1082, 1989.CrossRefGoogle Scholar
  24. Knapp A.K., Smith W.K.: Contrasting stomatal responses to variable sunlight in two subalpine herbs.–Am. J. Bot. 77: 226–231, 1990a.CrossRefPubMedGoogle Scholar
  25. Knapp A.K. Smith W.K.: Stomatal and photosynthetic responses to variable sunlight.–Physiol. Plantarum 78: 160–165, 1990b.CrossRefGoogle Scholar
  26. Küppers M., Timm H., Orth F. et al.: Effects of light environment and successional status on lightfleck use by understory trees of temperate and tropical forests.–Tree Physiol. 16: 69–80, 1996.CrossRefPubMedGoogle Scholar
  27. Kursar T.A., Coley P.D.: Photosynthetic induction times in shade-tolerant species with long and short-lived leaves.–Oecologia 93: 165–170, 1993.CrossRefPubMedGoogle Scholar
  28. Marler T.E.: Leaf physiology of shade-grown Cycas micronesica leaves following removal of shade.–Bot. Rev. 70: 63–71, 2004.CrossRefGoogle Scholar
  29. Marler T.E.: Age influences photosynthetic capacity of Cycas micronesica leaves.–Mem. New York Bot. Garden 97: 193–203, 2007.Google Scholar
  30. Marler T., Haynes J., Lindström A.: Cycas micronesica. The IUCN Red List of Threatened Species 2010: e.T61316 A12462113. Available from: http://dx.doi.org/10.2305/ IUCN.UK.2010-3.RLTS.T61316A12462113.en, 2010.Google Scholar
  31. Marler T.E., Lawrence J.H., Cruz, G.N.: Topographic relief, wind direction, and conservation management decisions influence Cycas micronesica K.D. Hill population damage during tropical cyclone.–J. Geogr. Nat. Disasters 6: 178, 2016.Google Scholar
  32. Marler T.E., Willis L.W.: Leaf gas-exchange characteristics of sixteen cycad specie.–J. Am. Soc. Hortic. Sci. 122: 38–42, 1997.Google Scholar
  33. McAusland L., Vialet-Chabrand S., Davey P. et al.: Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency.–New Phytol. 211: 1209–1220, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Naumburg E., Ellsworth D.S.: Photosynthetic sunfleck utilization potential of understory saplings growing under elevated CO2 in FACE.–Oecologia 122: 163–174, 2000.CrossRefPubMedGoogle Scholar
  35. Niklas K.J., Cobb E.D., Marler T.: A comparison between the record height-to-stem diameter allometries of Pachycaulis and Leptocaulis species.–Ann. Bot.-London 97: 79–83, 2006.CrossRefGoogle Scholar
  36. Niklas K.J., Marler T.E.: Carica papaya: a case study into the effects of domestication on plant vegetative growth and reproduction.–Am. J. Bot. 94: 999–1002, 2007.CrossRefPubMedGoogle Scholar
  37. Niklas K.J., Marler T.E.: Sex and population differences in the allometry of an endangered cycad species, Cycas micronesica (Cycadales).–Int. J. Plant Sci. 169: 659–665, 2008.CrossRefGoogle Scholar
  38. Norstog K.J., Nicholls T.J.: The Biology of the Cycads. Pp. 504. Cornell University Press, Ithaca, New York 1997.Google Scholar
  39. Pearcy R.W.: Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments.–Funct. Ecol. 1: 169–178, 1987.CrossRefGoogle Scholar
  40. Pearcy R.W.: Sunflecks and photosynthesis in plant canopies.–Annu. Rev. Plant Phys. 41: 421–453, 1990.CrossRefGoogle Scholar
  41. Pearcy R.W., Way D.A.: Two decades of sunfleck research: looking back to move forward.–Tree Physiol. 32: 1059–1061, 2012.CrossRefPubMedGoogle Scholar
  42. Porcar-Castell A., Palmroth S.: Modelling photosynthesis in highly dynamic environments: the case of sunflecks.–Tree Physiol. 32: 1062–1065, 2012.CrossRefPubMedGoogle Scholar
  43. Smith W.K., Knapp A.K., Reiners W.A.: Penumbral effects on sunlight penetration in plant communities.–Ecology 70: 1603–1609, 1989.CrossRefGoogle Scholar
  44. Soleh M.A., Tanaka Y., Kim S.Y. et al.: Identification of large variation in the photosynthetic induction response among 37 soybean [Glycine max (L.) Merr.] genotypes that is not correlated with steadystate photosynthetic capacity.–Photosynth. Res. 131: 305–315, 2017.CrossRefPubMedGoogle Scholar
  45. Sporne K.R.: The Morphology of Gymnosperms. Pp. 216. Hutchinson University Library, London 1965.Google Scholar
  46. Urban O., Košvancová M., Marek M.V. et al.: Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone.–Tree Physiol. 27: 1207–1215, 2007.CrossRefPubMedGoogle Scholar
  47. Urban O., Šprtová M., Košvancová M. et al.: Comparison of photosynthetic induction and transient limitations during the induction phase in young and mature leaves from three poplar clones.–Tree Physiol. 28: 1189–1197, 2008.CrossRefPubMedGoogle Scholar
  48. Vandermeer J.H.: Niche theory.–Annu. Rev. Ecol. Syst. 3: 107–132, 1972.CrossRefGoogle Scholar
  49. Vico G., Manzoni S., Palmroth S. et al.: Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes.–New Phytol. 192: 640–652, 2011.CrossRefPubMedGoogle Scholar
  50. Way D.A., Pearcy R.W.: Sunflecks in trees and forests: from photosynthetic physiology to global change biology.–Tree Physiol. 32: 1066–1081, 2012.CrossRefPubMedGoogle Scholar
  51. Zhang Y.-J., Cao K.-F., Sack L. et al.: Extending the generality of leaf economic design principles in the cycads, an ancient lineage.–New Phytol. 206: 817–829, 2015.CrossRefPubMedGoogle Scholar
  52. Zhang Q., Chen J.-W., Li B.-G. et al.: Epiphytes and hemiepiphytes have slower photosynthetic response to lightflecks than terrestrial plants: evidence from ferns and figs.–J. Trop. Ecol. 25: 465–472, 2009.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2017

Authors and Affiliations

  1. 1.Western Pacific Tropical Research Center, College of Natural and Applied SciencesUniversity of GuamMangilao, GuamUSA

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