Abstract
Hawaiian lobeliads have radiated into habitats from open alpine bogs to densely shaded rainforest interiors, and show corresponding adaptations in steady-state photosynthetic light responses and associated leaf traits. Shaded environments are not uniformly dark, however, but punctuated by sunflecks that carry most of the photosynthetically active light that strikes plants. We asked whether lobeliads have diversified in their dynamic photosynthetic light responses and how dynamic responses influence daily leaf carbon gain. We quantified gas exchange and dynamic light regimes under field conditions for ten species representing each major Hawaiian sublineage. Species in shadier habitats experienced shorter and less numerous sunflecks: average sunfleck length varied from 1.4 ± 1.7 min for Cyanea floribunda in shaded forest understories to 31.2 ± 2.1 min for Trematolobelia kauaiensis on open ridges. As expected, the rate of photosynthetic induction increased significantly toward shadier sites, with assimilation after 60 s rising from ca. 30% of fully induced rates in species from open environments to 60% in those from densely shaded habitats. Uninduced light use efficiency—actual photosynthesis versus that expected under steady-state conditions—increased from 10 to 70% across the same gradient. In silico transplants—modeling daily carbon gain using one species’ photosynthetic light response in its own and other species’ dynamic light regimes—demonstrated the potential adaptive nature of species differences: understory Cyanea pilosa in its light regimes outperformed gap-dwelling Clermontia parviflora, while Clermontia in its light regimes outperformed Cyanea. The apparent crossover in daily photosynthesis occurred at about the same photon flux density where dominance shifts from Cyanea to Clermontia in the field. Our results further support our hypothesis that the lobeliads have diversified physiologically across light environments in Hawaiian ecosystems and that those shifts appear to maximize the carbon gain of each species in its own environment.
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References
Allen MT, Pearcy RW (2000) Stomatal versus biochemical limitations to dynamic photosynthetic performance in four tropical rainforest shrub species. Oecologia 122:479–486
Baldwin BG, Kyhos DW, Dvorak J, Carr GD (1991) Chloroplast DNA evidence for a North American origin of the Hawaiian silversword alliance (Asteraceae). Proc Natl Acad Sci USA 88:1840–1843
Björkman O, Ludlow MM, Morrow PA (1972) Photosynthetic performance of two rainforest species in their native habitat and analysis of their gas exchange. Carnegie Inst Wash Yearb 71:94–102
Cai ZQ, Rijkers T, Bongers F (2005) Photosynthetic acclimation to light changes in tropical monsoon forest woody species differing in adult stature. Tree Physiol 25:1023–1031
Carlquist S (1970) Hawaii: a natural history. Natural History Press, New York
Chazdon RL (1988) Sunflecks and their importance to forest understory plants. Adv Ecol Res 18:1–63
Chazdon RL, Pearcy RW (1986a) Photosynthetic responses to light variation in rainforest species. 1. Induction under constant and fluctuating light conditions. Oecologia 69:517–523
Chazdon RL, Pearcy RW (1986b) Photosynthetic responses to light variation in rainforest species. 2. Carbon gain and photosynthetic efficiency during lightflecks. Oecologia 69:524–531
Chazdon RL, Pearcy RW (1991) The importance of sunflecks for forest understory plants. BioScience 41:760–766
Chazdon RL, Williams K, Field CB (1988) Interactions between crown structure and light environment in five rain forest Piper species. Am J Bot 75:1459–1471
Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Soc Exp Biol Symp 31:471–505
Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126:345–354
Ellsworth DS, Reich PB (1992) Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments. Funct Ecol 6:423–435
Falster DS, Warton DI, Wright IJ (2006) (S)MATR: standardised major axis tests and routines. Version 2.0. http://www.bio.mq.edu.au/ecology/SMATR/
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Gillespie RG (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science 303:356–359
Givnish TJ (1986) Optimal stomatal conductance, allocation of energy between leaves and roots, and the marginal cost of transpiration. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 171–213
Givnish TJ (1988) Adaptation to sun vs. shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92
Givnish TJ (1997) Adaptive radiation and molecular systematics: aims and conceptual issues. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, New York, pp 1–54
Givnish TJ (1998) Adaptive radiation of plants on oceanic islands: classical patterns, molecular data, new insights. In: Grant P (ed) Evolution on islands. Oxford University Press, New York, pp 281–304
Givnish TJ (2002) On the adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743
Givnish TJ, Sytsma KJ, Hahn WJ, Smith JF (1995) Molecular evolution, adaptive radiation, and geographic speciation in Cyanea (Campanulaceae, Lobelioideae). In: Wagner WL, Funk VA (eds) Hawaiian biogeography: evolution on a hot spot Archipelago. Smithsonian Institution Press, Washington, pp 288–337
Givnish TJ, Montgomery RA, Goldstein G (2004) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: light regimes, static light responses, and whole-plant compensation points. Am J Bot 91:228–246
Horn HS (1971) The adaptive geometry of trees. Princeton University Press, Princeton
King D (1981) Tree dimensions—maximizing the rate of height growth in dense stands. Oecologia 51:351–356
Kirschbaum MUF, Küppers M, Schneider H, Giersch C, Noe S (1998) Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates. Planta 204:16–26
Kitajima K (1994) Relative importance of photosynthetic traits and allocation pattern as correlates of seedling shade tolerance in 13 tropical trees. Oecologia 98:419–428
Lammers TG (1999) Campanulaceae. In: Wagner WL, Herbst DR, Sohmer SH (eds) Manual of the flowering plants of Hawaii. Bishop Museum Publications, Honolulu, pp 420–489
Le Gouallec JL, Cornic G, Blanc P (1990) Relations between sunfleck sequences and photoinhibition of photosynthesis in a tropical rainforest understorey herb. Am J Bot 77:999–1006
Leakey ADB, Scholes JD, Press MC (2005) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482
Lee DW (1989) Canopy dynamics and light climates in a tropical moist deciduous forest in India. J Trop Ecol 5:65–79
Lindqvist C, Motley TJ, Jeffrey JJ, Albert VA (2003) Cladogenesis and reticulation in the Hawaiian endemic mints (Lamiaceae). Cladistics 19:480–495
Montgomery RA, Chazdon RL (2002) Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165–174
Naumburg E, Ellsworth DS (2002) Short-term light and leaf photosynthetic dynamics affect estimates of daily understory photosynthesis in four tree species. Tree Physiol 22:393–401
Naumburg E, Ellsworth DS, Katul GG (2001) Modeling dynamic understory photosynthesis of contrasting species in ambient and elevated carbon dioxide. Oecologia 126:487–499
Pagel M (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol 48:612–622
Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Mol Biol 41:421–453
Pearcy RW, Osteryoung K, Randall D (1982) Carbon dioxide exchange characteristics of C4 Hawaiian Euphorbia species native to diverse habitats. Oecologia 55:333–341
Pfitsch WA, Pearcy RW (1989) Daily carbon gain by Adenocaulon bicolor (Asteraceae), a redwood forest understory herb, in relation to its light environment. Oecologia 80:465–470
Piano F, Craddock EM, Kambysellis MP (1997) Phylogeny of the island populations of the Hawaiian Drosophila grimshawi complex: evidence from combined data. Mol Phyl Evol 7:173–184
Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecol 87:1733–1743
Poorter L, Oberbauer SF (1993) Photosynthesis induction responses of two rainforest tree species in relation to light environment. Oecologia 96:193–199
Price JP, Wagner WL (2004) Speciation in Hawaiian angiosperm lineages: cause, consequence, and mode. Evolution 58:2185–2200
Robichaux RH (1984) Variation in the tissue water relations of two sympatric Hawaiian Dubautia species and their natural hybrid. Oecologia 65:75–81
Robichaux RH, Canfield JE (1985) Tissue elastic properties of eight Hawaiian Dubautia species that differ in habitat and diploid chromosome number. Oecologia 66:77–80
Robichaux RH, Carr GD, Liebman M, Pearcy RW (1990) Adaptive radiation of the Hawaiian silversword alliance (Compositae Madiinae)—ecological, morphological, and physiological diversity. Ann Mo Bot Gard 77:64–72
Robichaux RH, Pearcy RW (1980) Photosynthetic responses of C3 and C4 species from cool shaded habitats in Hawaii. Oecologia 47:106–109
Robichaux RH, Pearcy RW (1984) Evolution of C3 and C4 plants along an environmental moisture gradient—patterns of photosynthetic differentiation in Hawaiian Scaevola and Euphorbia species. Am J Bot 71:121–129
Rundell RJ, Holland BS, Cowie RH (2004) Molecular phylogeny and biogeography of the Hawaiian Succineidae (Gastropoda: Pulmonata). Mol Phyl Evol 31:246–255
Sack L (2004) Responses of temperate woody seedlings to shade and drought: do trade-offs limit potential niche differentiation? Oikos 107:110–127
Sack L, Grubb PJ (2001) Why do species of woody seedlings change rank in relative growth rate between low and high irradiance? Funct Ecol 15:145–154
Sakai AK, Weller SG, Wagner WL, Nepokroeff M, Cullen TM (2006) Adaptive radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), an endemic Hawaiian genus. Ann Mo Bot Gard 93:49–63
Sassenrath-Cole GF, Pearcy RW (1994) Regulation of photosynthetic induction state by the magnitude and duration of low-light exposure. Plant Physiol 105:1115–1123
Seiwa K (2007) Trade-offs between seedling growth and survival in deciduous broadleaved trees in a temperate forest. Ann Bot 99:537–544
Sharkey TD, Seemann JR, Pearcy RW (1986) Contribution of metabolites of photosynthesis to postillumination CO2 assimilation in response to lightflecks. Plant Physiol 82:1063–1068
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York
Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton
Timm HC, Stegemann J, Küppers M (2002) Photosynthetic induction strongly affects the light compensation point of net photosynthesis and coincidentally the apparent quantum yield. Trees Struct Funct 16:47–62
Tinoco-Ojanguren C, Pearcy RW (1993) Stomatal dynamics and its importance to carbon gain in 2 rainforest Piper species. 1. VPD effects on the transient stomatal response to lightflecks. Oeclogia 94:388–394
Tinoco-Ojanguren C, Pearcy RW (1995) A comparison of light quality and quantity effects on the growth and steady-state and dynamic photosynthetic characteristics of 3 tropical tree species. Funct Ecol 9:222–230
Valladares F, Pearcy RW (2002) Drought can be more critical in the shade than in the sun: a field study of carbon gain and photo-inhibition in a Californian shrub during a dry El Nino year. Plant Cell Environ 25:749–759
Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111:505–514
Valladares F, Arrieta S, Aranda I, Lorenzo D, Sanchez-Gomez D, Tena D, Suarez F, Pardos JA (2005) Shade tolerance, photoinhibition sensitivity and phenotypic plasticity of Ilex aquifoliium in continental Mediterranean sites. Tree Physiol 25:1041–1052
Wagner WL, Herbst DR, Sohmer SH (1990) Manual of the flowering plants of Hawai'i. University of Hawaii Press, Bishop Museum Press, Honolulu
Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Aust J Plant Physiol 24:17–25
Young DR, Smith WK (1979) Influence of sunflecks on the temperature and water relations of two subalpine understorey congeners. Oecologia 43:195–205
Acknowledgements
The authors gratefully acknowledge the research support provided by grant IBN-9904366 from the Ecological and Evolutionary Physiology Program of the US National Science Foundation. We thank Hawai‘i Volcanoes National Park, the National Tropical Botanical Garden, the Koke‘e Natural History Museum, Limahuli Garden and the University of Hawai‘i Agricultural Experiment Station in Volcano for important logistical assistance. Ken Wood, Linda Pratt, and Katie Cassel provided invaluable aid in locating populations of several rare species. We are deeply grateful to Wayne Souza of Kaua‘i State Parks, Edwin Pettys of Kaua‘i Division of Forestry and Wildlife, David Foote and Linda Pratt of the US Geological Survey Biological Resources Division, Betsy Gagné, Randy Kennedy, Bill Stormont, and Jon Giffen of Hawai‘i Natural Areas Reserves, Susan Cordell and Julie Denslow of the US Department of Agriculture Forest Service and Sterling Keeley of the University of Hawai‘i for their support in helping us obtain research permits and access to research facilities. Mahalo to Aubrey Kelly, Leilani Durand, Nicole Kuamo‘o and Ken Wood for help and camaraderie in the field and for their commitment in helping to achieve the objectives of this research. We thank Elke Naumburg for sharing the dynamic model, and both Elke Naumburg and Ned Fetcher for advice in model implementation. We thank Megan Kranz-McGuire for her work on the dynamic model simulations and Vlad Bluvstein for his programming assistance in the sunfleck analysis. These experiments comply with current laws of the USA.
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Communicated by Robert Pearcy.
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Montgomery, R.A., Givnish, T.J. Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: dynamic photosynthetic responses. Oecologia 155, 455–467 (2008). https://doi.org/10.1007/s00442-007-0936-3
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DOI: https://doi.org/10.1007/s00442-007-0936-3