Photosynthetica 2018, 56(3):776-785 | DOI: 10.1007/s11099-017-0730-3

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

T. E. Marler1,*
1 Western Pacific Tropical Research Center, College of Natural and Applied Sciences, University of Guam, Mangilao, Guam, USA

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

Received: November 26, 2016; Accepted: March 15, 2017; Prepublished online: September 1, 2018; Published: August 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Marler, T.E. (2018). Bi-directional acclimation of Cycas micronesica leaves to abrupt changes in incident light in understory and open habitats. Photosynthetica56(3), 776-785. doi: 10.1007/s11099-017-0730-3
Download citation

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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  5. Brantley S.T. Young D.R.: Linking light attenuation, sunflecks, and canopy architecture in mesic shrub thickets.-Plant Ecol. 206: 225-236, 2010. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  10. Calonje M., Stevenson D.W., Stanberg L.: The World List of Cycads. Available from: http://www.cycadlist.org, 2016.
  11. Chazdon R.L.: Sunflecks and their importance to forest understorey plants.-Adv. Ecol. Res. 18: 1-63, 1988. Go to original source...
  12. Chazdon R.L., Pearcy R.W.: The importance of sunflecks for forest understory plants.-BioScience 41: 760-766, 1991. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  20. Greguss P.: Xylotomy of the Living Cycad. Pp. 260. Akadémiai Kiadó, Budapest 1968.
  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. Go to original source...
  22. Hutchinson G.E.: Concluding remarks.-Cold Spring Harb. Symp. Quant. Biol. 22: 415-427, 1957. Go to original source...
  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. Go to original source...
  24. Knapp A.K., Smith W.K.: Contrasting stomatal responses to variable sunlight in two subalpine herbs.-Am. J. Bot. 77: 226-231, 1990a. Go to original source...
  25. Knapp A.K. Smith W.K.: Stomatal and photosynthetic responses to variable sunlight.-Physiol. Plantarum 78: 160-165, 1990b. Go to original source...
  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. Go to original source...
  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. Go to original source...
  28. Marler T.E.: Leaf physiology of shade-grown Cycas micronesica leaves following removal of shade.-Bot. Rev. 70: 63-71, 2004. Go to original source...
  29. Marler T.E.: Age influences photosynthetic capacity of Cycas micronesica leaves.-Mem. New York Bot. Garden 97: 193-203, 2007. Go to original source...
  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. Go to original source...
  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. Go to original source...
  32. Marler T.E., Willis L.W.: Leaf gas-exchange characteristics of sixteen cycad specie.-J. Am. Soc. Hortic. Sci. 122: 38-42, 1997. Go to original source...
  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. Go to original source...
  34. Naumburg E., Ellsworth D.S.: Photosynthetic sunfleck utilization potential of understory saplings growing under elevated CO2 in FACE.-Oecologia 122: 163-174, 2000. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  38. Norstog K.J., Nicholls T.J.: The Biology of the Cycads. Pp. 504. Cornell University Press, Ithaca, New York 1997.
  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. Go to original source...
  40. Pearcy R.W.: Sunflecks and photosynthesis in plant canopies.-Annu. Rev. Plant Phys. 41: 421-453, 1990. Go to original source...
  41. Pearcy R.W., Way D.A.: Two decades of sunfleck research: looking back to move forward.-Tree Physiol. 32: 1059-1061, 2012. Go to original source...
  42. Porcar-Castell A., Palmroth S.: Modelling photosynthesis in highly dynamic environments: the case of sunflecks.-Tree Physiol. 32: 1062-1065, 2012. Go to original source...
  43. Smith W.K., Knapp A.K., Reiners W.A.: Penumbral effects on sunlight penetration in plant communities.-Ecology 70: 1603-1609, 1989. Go to original source...
  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. Go to original source...
  45. Sporne K.R.: The Morphology of Gymnosperms. Pp. 216. Hutchinson University Library, London 1965.
  46. Urban O., Koąvancová 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. Go to original source...
  47. Urban O., ©prtová M., Koąvancová 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. Go to original source...
  48. Vandermeer J.H.: Niche theory.-Annu. Rev. Ecol. Syst. 3: 107-132, 1972. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...