Oecologia (1993) 94: 218-228 Oecologia © Springer-Verlag 1993

The dynamics of photosynthetic acclimation to changes in light quantity and quality in three Australian rainforest tree species Matthew H. Turnbuil, David Doley, David J. Yates

Department of Botany and Centre for Conservation Biology, The University of Queensland, St Lucia, Queensland 4072, Australia

Received: 15 July 1992 / Accepted: 25 October 1992

Abstract. Photosynthetic acclimation was studied in seedlings of three subtropical rainforest species represen- ting early (Omalanthus populifolius), middle (Duboisia myo- poroides) and late (Acmena ingens) successional stages in forest development. Changes in the photosynthetic characteristics of pre-existing leaves were observed follow- ing the transfer of plants between deep shade (1-5% of photosynthetically active radiation (PAR), selectively fil- tered to produce a red/far-red (R/FR) ratio of 0.1) and open glasshouse (60% PAR and a R/FR ratio of 1.1 1.2), and vice versa. The extent and rate of response of the photosynthetic characteristics of each species to changes in light environment were recorded in this simulation of gap formation and canopy closure/overtopping. The light regimes to which plants were exposed produced significant levels of acclimation in all the photosynthetic parameters examined. Following transfer from high to low light, the light-saturated rate of photosynthesis was maintained near pre-transfer levels for 7 days, after which it decreased to levels which closely approximated those in leaves which had developed in low light. The decrease in photosynthetic capacity was associated with lower apparent quantum yields and stomatal conductances. Dark respiration was the parameter most sensitive to changes in light environ- ment, and responded significantly during the first 4-7 days after transfer. Acclimation of photosynthetic capacity to increases in irradiance was significant in two of the three species studied, but was clearly limited in comparison with that of new leaves produced in the high light conditions. This limitation was most pronounced in the early-succes- sional-stage species, O. populifolius. It is likely that struc- tural characteristics of the leaves, imposed at the time of leaf expansion, are largely responsible for the limitations in photosynthetic acclimation to increases in irradiance.

Key words: Rainforest - Photosynthetic acclimation - Assimilation rate - Dark respiration - Stomatal conductance

Recent interest in the ecophysiological characteristics of tropical tree species stems from the need to increase our

Correspondence to: M.H. Turnbull

understanding of the relationships between the physiolo- gical responses of individuals and the ecological processes which have been observed in tropical forest systems (Mooney et al. 1980). The environmental heterogeneity caused by turnover in canopy cover has provided the focus for work on germination strategies (Vazquez-Yanes and Orosco-Segovia 1984), plant water relations (Oberbauer et al. 1987; Mulkey et al. 1991b), and the influence of light environment on plant growth, development and survival (Augspurger 1984; Kwesiga and Grace 1986; Lee 1988).

The majority of studies into the responses of tropical tree species to light environment have concentrated on the effects of a range of constant light conditions on the photosynthetic characteristics of selected species (Ober- bauer and Strain 1984, 1985; Kwesiga et al. 1986; Langen- heim et al. 1984; Walters and Field 1987; Turnbull 1991). Such work serves to indicate the potential extent of plasticity in the photosynthetic machinery of the species studied, although few studies have attempted to differ- entiate between the effects of variations in growth irradi- ance and light quality (Kwesiga et al. 1986; Turnbull 1991).

Despite the worth of such base-line studies, their ecological significance is somewhat limited. Plants do not function in constant environmental conditions, especially with respect to light. Within the rainforest community light is a highly variable and often limiting resource (Yates et al. 1988). Not only does the average photon flux density (PFD) incident on leaves in the upper canopy differ from that incident on leaves at the forest floor by two orders of magnitude (Bjorkman and Ludlow 1972; Pearcy 1983), but leaves of plants in the understorey may be exposed to such light levels over a very short time. Hence, of the 0.5-2% of full sunlight received at a given point on the rainforest floor during the course of a day, some 50-80% may be contributed by short-term sunflecks (Chazdon and Fetcher 1984). In addition to this, significant changes in the light environment of understorey plants may result from canopy rearrangements caused by gap formation (e.g. Denslow 1987) and subsequent encroachment into gaps by surviving crown units. Seasonal variation in the transmission of sunlight into canopy gaps, which is a function of gap and solar geometry, also results in con-

219

siderable short- term (in the order of seconds to minutes) and long-term (in the order of days to weeks) changes in the light condit ions to which plants are exposed following gap format ion (Turnbull and Yates 1993; D.A. Vieglais, unpublished data).

Plants in complex systems such as tropical forests must function in spatially and temporal ly variable light condi- tions. Al though the studies on photosynthet ic plasticity referred to above give some indication of the character- istics of leaves which have developed in given light condi- tions, they do little to extend our understanding of the potential for acclimation to large-scale changes in such conditions which may occur at some time after leaf production. Given the product ion costs and longevity of leaves of many rainforest tree species (Williams et al. 1989; Mulkey et al. 1991a; Sobrado 1991) such flexibility in physiology may be significant to the survival of individuals in the unders torey and to overall communi ty functioning. A large body of knowledge exists regarding features of photosynthet ic acclimation in temperate and agricultural species (Grahl and Wild 1975; Prioul et al. 1980; Wild and Wolf 1980; von Caemmerer and Fa rquhar 1984; Besford 1986; Davies et al. 1986; C h o w and Anderson 1987; Sebaa et al. 1987). Recent work involving the transfer of rain- forest plants to high and low light conditions have indi- cated distinct differences in species' capacity to respond to either an increase or decrease in irradiance (Chow et al. 1991; O s u n k o y a and Ash 199l; P o p m a and Bongers 1991; Strauss-Debenedett i and Bazzaz 1991) and point to the need for further work. Studies of this nature may assist a t tempts to categorize tropical tree species into functional groups based on the physiological ecology of plants from differing successional stages in forest development (e.g. Bazzaz and Pickett 1980; Swaine and Whi tmore 1988). To date such at tempts have been hampered by equivocal findings which indicate that photosynthet ic plasticity to light environment may be predicted only to a limited extent on the basis of successional status (Bazzaz and Carlson 1982; Oberbauer and Strain 1984; Walters and Field 1987; Turnbul l 1991).

The aim of this study was to determine the extent and rate of photosynthet ic acclimation in seedlings of tree species from each of three recognized successional stages in sub-tropical rainforest development from eastern Australia. This was achieved by examining photosynthet ic responses to variat ion in P F D and light quality following transfer between light treatments designed to approximate conditions which would be experienced by plants within rainforest understorey and gap sites. Transfers between such treatments involved simultaneous changes in both light quant i ty and quality, and served to mimic the processes of gap format ion and overtopping/self-shading, thus taking into account the importance of light quanti ty and quality changes stressed in previous studies (McKiernan and Baker 1991; Turnbull 1991).

MateriaLs and methods

Plant material

Three species, one from each of early-, mid-, and late-successional stages of sub-tropical rainforest in eastern Australia, were chosen for

study. The plasticity of the photosynthetic response in these species to both light quantity and quality during leaf development has been previously established (Turnbull 1991). Omalanthus populifolius Grah. (Euphorbiaceae) is an early-successional, or short-lived sec- ondary tree which grows to 5 m tall in disturbed sites (where canopy cover is substantially reduced) and near rainforest margins. Duboisia myoporoides R. Br. (Solanaceae) is a mid-stage or long-lived second- ary tree species which grows to 20 m and is common in regrowth sites. Acmena ingens (F. Muell. ex C. Moore).Guymer and B. Hyland (Myrtaceae) is a late-stage or mature-phase tree species which attains 40 m in height. Seedlings and small saplings of A. ingens commonly persist below an intact rainforest canopy. Successional status was allocated to these species according to the scheme used by Hopkins (1975) and Olsen (1990).

Seedlings of each species were collected from montane sub- tropical rainforest in Gambubal State Forest, south east Queensland (27.8 ° S, 152.9 ° E, altitude 1250 m), and taken to The University of Queensland where they were potted in a 2:1 coarse-sand and peat moss mixture. Plants received an application of commercial slow- release fertilizer (Osmocote), and were watered daily via a sprinkler system. At the time of collection, seedlings of A. ingens and D. myoporoides had one or two primary leaves, whilst seedlings of O. populifolius had three or four leaves.

Growth conditions

The light treatments used here were a sub-set of those described previously (Turnbull 1991). Filtered shade treatments were estab- lished in a glasshouse at The University of Queensland, providing 1% and 5% of incident sunlight (these values being the percentages of PAR transmitted by the shades). Transmission characteristics for the materials used were determined using an LI-1800 spectro- radiometer attached to an LI-1800-12 integrating sphere by a quartz fibre probe (Li-Cor Inc., Lincoln, Nebraska, U.S.A.). Filtered shade (with a low red/far-red (R/FR) ratio of approximately 0.2) was provided by a combination of Cinemoid filter 'moss green' no. 22 (Rank Strand, Brentford, UK) and H122 (Lee Filters Ltd., Andover, U.K.), and neutral density shadecloth (Rheem Australia Ltd.) (Yates 1989). These materials were fixed to aluminium frames and placed over enclosures divided by reflective sheeting. The plant-growing area in each of the six enclosures measured 2.5 by 1.4 m. A high light treatment (providing 60 65% of incident sunlight)was established in the open glasshouse adjacent to the shade enclosures. Light quality within the filtered shade treatments closely approximated that of deep shade below a closed canopy with respect to the relative proportions of blue, red and far-red radiation (Holmes and Smith 1977).

Ventilation was provided by overlapping gaps in the wall mat- erial, at three levels from the floor of the ceiling of the 2.2-m tall enclosures. Temperatures in the enclosures were regulated by ther- mostatically-controlled fans and evaporative coolers on one wall of the glasshouse.

Transfer schedule

Five individuals of each species were placed in each treatment and suspended as close to the shading material as possible. The level of each platform was adjusted periodically as the plants grew. Plants were relocated randomly once per week. After 4 months' growth in the original treatments, 2 3 plants of each species were transferred from 5% filtered shade to the open glasshouse, designated as "low to high" (L-H), and from the open glasshouse to 1% filtered shade, designated as "high to low" (H-L). It has been envisaged that plants would also be transferred from 1% filtered shade to the open glasshouse, designated as "very low to high" (VL-H), but this was only possible in the case of O. populifolius, as plant and leaf growth in D. myoporoides and A. ingens were not sufficient to allow accurate photosynthetic determinations.

220

On the day prior to transfer (day 0), and at days 3, 7, 14 and 28 after transfer, determinations of the photosynthetic characteristics of each leaf measured were performed as described below. A final determination was performed between days 55 and 70. Leaf areas were also monitored on each measurement day using a leaf area meter (Delta-T Devices, Cambridge, England), to measure post- transfer changes in leaf morphology (Di Benedetto and Cogliatti 1990; Popma and Bongers 1991). Plants were transported from the glasshouse to the laboratory on the evening before the day on which gas exchange analysis was to be performed, and returned immedi- ately after completion of the laboratory work. During the course of the 55-70 day transfer period, each leaf was exposed to the laborat- ory light source (during photosynthesis measurements) for no more than 12-14 h. It is thus reasonable to discount any influence of exposure to the laboratory light source. Leaf durations under experimental conditions were in the order of 6 months for O. populifolius, 12 months for D. myoporoides, and 24 months for A. ingens [as observed in plants from previous experiments (e.g. Turn- bull 1991)]. Given such longevities it was considered that photo- synthetic characteristics would change little over the transfer time-courses as a consequence of leaf aging.

Following completion of the transfer time-course, the photo- synthetic characteristics of 4 6 fully-expanded (new) leaves which had been produced subsequent to transfer to the new light treatment were also determined.

Gas exchange measurements

Leaf carbon dioxide and water vapour exchange rates were deter- mined using a Binos infra-red CO2/H20 gas analyser (Rosemount GmbH, formerly Leybold Heraeus, Hanau, Germany) using the method described by Turnbull (1991). Measurements were made on the two youngest fully expanded leaves on each of two or three individuals from each treatment at a range of PFDs from 0 to 1000 gmol m -2 s 1 at 335-345 ppm CO2. Water vapour pressure deficit was generally held between 1.2 and 1.6 kPa using a humidified gas supply. The range of relative humidities experienced by leaves in the chamber (50 65%) was considered realistic in light of values experienced by plants in montane sub-tropical environments. Air temperature within the water-cooled leaf chamber was maintained between 24 and 26 ° C. Signals from the gas analysis system were measured every 5 s, derived values calculated, and data stored on computer for analysis. Calculations of gas exchange rates and stomatal conductance were made using the equations given by yon Caemmerer and Farquhar (1981). The computer-based system made it possible to continuously monitor gas exchange and hence photo- synthetic rate. After an initial measurement of dark respiration, the light dependence of CO2 uptake was determined by first taking measurements at approximately 1000 gmol m 2 s -1, and then at progressively lower levels of PFD. A lower initial light level was used for deep shade grown plants in which photoinhibition was detected. Light was provided by a 1000-W multi-vapour metal-halide lamp (General Electric, Cleveland, Ohio, USA), with instantaneous PFD measured using an LI-195 quantum sensor (Li-Cor Inc., Lincoln, Nebraska, USA). At each PFD the leaf was allowed to equilibrate for 15 25 min before data were recorded.

Photosynthetic parameters were calculated on the basis of 90% absorption of PAR by all leaves, an assumption validated by previous work on the absorptance of PAR in rainforest sun- and shade-adapted species (Lee and Graham 1986; Lee et al. 1990; M.H. Turnbull, unpublished data). The initial slope of the light response curve (apparent quantum yield) was calculated by linear regression of four points below 100 gmolm z s- ~ PFD. Light compensation point was calculated by dividing dark respiration rate by apparent quantum yield. Student's t-tests were applied to the data to test the hypothesis that the means of the values obtained at day 0 and day 28 were equal.

The relationship between light quality during growth and sub- sequent photosynthesis in different light qualities was also investig- ated during the experiment, and will be presented elsewhere.

Carbon balance simulations

To assess the potential importance of changes in photosynthetic characteristics following transfer in terms of overall carbon fixation, daily carbon balance calculations were performed. It was intended that values obtained would give a further indication of the direction and extent of overall photosynthetic acclimation to light environ- ment. Photosynthetic carbon fixation over a 24-h period was calcu- lated assuming clear sky conditions for a summer day (photoperiod 16 h, maximum PFD 2000 gmolm -2 s -~. Photon flux density at t hours was calculated using the sinusoidal relationship

S t = Stm sin(r~t/n)

where Stm is the maximum PFD at solar noon and n is the daylength in hours (Monteith and Unsworth 1990). Actual PFD received by leaves in the shade treatments was calculated according to the transmission characteristics of the filtering materials. Instantaneous photosynthetic rate (in gmol CO2 m -2 s-~) was calculated hourly using the simple rectangular hyperbola

F = ~ S t f m / ( O ; S t q- Frn ) - R a

where F is the net rate of leaf photosynthesis, S, is the downward PFD incident upon the leaf surface, ~ is the leaf apparent quantum yield, Fm is the rate of light-saturated leaf photosynthesis and R d is the rate of leaf dark respiration (Charles-Edwards et al. 1986). Daytime carbon fixation was calculated by integrating over time (daylength). Whole-day carbon balance was calculated by sub- tracting night-time dark respiration (assumed to be 0.9 x Rd) from the integral of daytime carbon fixation. Calculations were performed for the time course of each experiment with photosynthetic para- meters averaged between each collection date, assuming individual leaves were uniformly illuminated and that laminae were normal to incident radiation.

Results

All plants survived and cont inued to grow following transfer to the new light condit ions, a l though in all three species significant loss of old leaves was observed follow- ing the high to low light (H-L) transfer. U p o n t ransferf rom low to high light (L-H), only leaves of O. populifolius exhibited any degree of foliar injury, showing limited localized photobleaching. Small post-transfer increases in individual leaf areas were observed in O. populifolius and D. myoporoides after the L-H light transfer, while leaves of A. ingens did not expand further. Significant levels of photosynthet ic accl imation were observed in all species following both the H-L and L-H transfers, as exemplified by changes in the response of assimilat ion rate to in- s tantaneous P F D in D. myoporoides (Fig. 1).

Compar i son of the responses of the three species dur ing the transfer t ime-course was facilitated by sum- marizing photosynthet ic characteristics in terms of para- meters which could be calculated from the photosynthet ic light response data. In this way significant features of the photosynthet ic accl imation process could be compared simultaneously. M a x i m u m light-saturated CO 2 assimil- a t ion rate (Amax) decreased in all species following the H-L transfer, with the majori ty of the response achieved by day 28 in O. populifolius and D. myoporoides, and by day 56 in leaves of A. ingens (Fig. 2). Ama x was main ta ined at (or above) pre-transfer levels for 7 days in D. myoporoides and for 14 days in A. ingens, but decreased steadily in O. populifolius. The extent of accl imation in Amax to the H-L transfer was similar for the three species studied, with

221

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Fig. la, b. Changes in the response of assimilation to PFD for leaves of Duboisia myoporoides following transfer between a neutral shade at 60% PAR and filtered shade at 1% PAR (designated as H-L in the text), and b filtered shade at 1% PAR and neutral shade at 60% PAR (designated as L-H in the text). Each figure represents data for a single leaf. The day on which each response curve was determined is indicated

percentage changes at day 28 (relative to Amax at day 0) of - 5 8 % for O. populifolius, -64% for D. myoporoides and - 4 3 % for A. ingens (Table 1). This response was signific- ant (P_< 0.05) for O. populifotius and D. myoporoides only. Leaves of O. populifolius and D. myoporoides were able to achieve full acclimation in Ama x following transfer to deep shade, as indicated by the similarity in Am, x between transferred leaves at the end of the time-course and new leaves produced subsequently. Am, ~ in A. ingens, however, had not reached 'new leaf' levels by day 56 of the time- course.

Following the L-H transfer A,~a~ increased by 2.5% in O. populifolius, 54% in D. myoporoides and 46% in A. ingens. These increases were significant (P<0.05) for the latter two species (Table 1). Both O. populifolius and A. ingens displayed an initial drop in A~n,. in the first 3 7 days after transfer, followed by recovery of photosynthetic capacity. A drop in Area x was noted in all species between day 28 and the end of the time-course. Am, ~ values in new leaves produced in the high light conditions were con- siderably higher than those in pre-existing leaves at the end of the time-course in O. populifolius and D. myo- poroides, but only marginally so in A. ingens. The response ofO. populifolius leaves to the VL-H (1 60%) transfer, were similar to those following the L-H (5-60%) transfer, although the 52% increase in Ama~ after the initial decrease was significant (P_<0.05) (Table 1). Am,x values in new leaves produced following the VL-H transfer were 4 times greater than in leaves at day 28, and almost identical to new leaves produced on plants from the L-H transfer.

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Fig. 2. The time-course of the response of light-saturated assimil- ation rate (Amox) in mature leaves of Omalanthus populifolius (early- successional stage species), D. myoporoides (mid-successional stage species), and Acmena ingens (late-successional stage species) follow- ing transfer between neutral shade at 60% PAR and filtered shade at 1% PAR (designated as H-L in the text) (closed squares), filtered shade at 5% PAR and neutral shade at 60% PAR (designated as L-H in the text) (open squares), and (for O. populifolius only) filtered shade at 1% PAR and neutral shade at 60% PAR (designated as VL-H in the text) (open circles). Data for new leaves produced following transfer are shown to the right of each time-course (New). Bars indicate +_ SE of the mean

Significant acclimation in maximum stomatal con- ductance (GSmax) was observed for all three species follow- ing the H-L transfer from sun to shade (Fig. 3), with average decreases of 69% in O. populifolius, 58% in D. myoporoides, and 31% in A. ingens (Table 1). Although Gsma x decreased steadily from day 0 in O. populifolius, both D. myoporoides and A. ingens displayed small increases until day 7. The response to the transfer light regime was complete by day 28 in the early- and mid-stage species (O. populifolius and D. myoporoides respectively), but contin- ued until day 56 in the late-stage species A. ingens. In all the species, Gsma x at 70 days after the H-L transfer closely approximated that in new leaves produced after transfer. Changes in Gsm, x following transfer from the filtered shade to open glasshouse treatment (L-H) were limited, and by day 28 Gsma x had decreased by 19% in O. populifolius, and increased by 41% in D. myoporoides and by 7% in A. ingens. In no species was Gsma x at day 28 significantly greater than the value determined at day 0 (Table 1). As for A . . . . new leaves from the L-H transfer had higher levels of

222

Table 1. Percentage change in photosyn- thetic characteristics of mature leaves of Omalanthus populifolius, Duboisia myopor- oides, and Acmena ingens at day 28 after transfer to the new light environment

Parameter Transfer O. populifolius D. myoporoides A. ingens

Ama x H-L -58.4* -64.0* -43.8ns L-H + 2.5ns +53.8* +45.8** VL-H +52.2*

Gsmax H-L - 69.4" - 58.1 * - 31.2' L-H -19.1" +41.0ns + 7.1ns VL-H - 27.3 ns

Quantum H-L -13.1ns - 18.6ns -39.3* yield L-H - 15.1ns +24.5* + 8.3ns

VL-H 0 ns

Raark H-L - 63.6"* - 66.2" - 62.7"* L-H + 165"* + 196"* + 103'* VL-H + 185"*

Amax/Rdark H-L + 6.7ns - 4.2ns +45.3ns L-H - 62.3 * - 49.0 * - 29.6 ns VL-H -48.4*

Transfers were between (a) neutral shade at 60% PAR and filtered shade at 1% PAR (designated as H-L in the text), (b) filtered shade at 5% PAR and neutral shade at 60% PAR (designated as L-H in the text), and (c) filtered shade at 1% PAR and neutral shade at 60% PAR (designated as VL-H in the text), for O. populifolius only. Abbreviations: A . . . . light saturated assimilation rate; Gs . . . . maximum stomatal conductance; R d a r k , dark respiration rate. Mean percentage changes were calculated from data in Figs. 2 6. Results of t-tests comparing averages at day 0 and day 28 are indicated (**P_<0.01; *P_<0.05; ns, not significant)

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Fig. 3. The time-course of the response of maximum stomatal conductance (Gsm,x) in mature leaves of O. populifolius, D. myo- poroides, and A. ingens following transfer between various light treatments. See Fig. 2 for details

Gsma x than those achieved fol lowing the l imited accl ima- t ion of pre-exist ing leaves after 8 weeks, a l though this difference was negligible for A. ingens. The response of O. populifolius to the V L - H transfer closely resembled that of p lants to the L -H transfer.

A p p a r e n t q u a n t u m yield was largely insensitive to long- te rm change fol lowing transfer between light t reat- ments. Fo l lowing the H - L transfer a decrease in appa ren t q u a n t u m yield was measured in all three species, be ing significant in A. ingens only (Fig. 4 and Table 1). Percent- age decreases to day 28 were 13% in O. populifolius, 18% in D. myoporoides and 39% in A. ingens (Table 1). A short- term decrease in q u a n t u m yield, indicat ive of t ransient pho to inh ib i t ion , was expressed in the three species follow- ing transfer from filtered shade to the open glasshouse l ight condi t ions . Recovery was achieved by day 7, after which a small overal l increase was observed in D. myo- poroides and A. ingens. The decrease in appa ren t q u a n t u m yield fol lowing exposure to high light was more pro- nounced and longer- las t ing for O. populifolius in the V L - H transfer, with recovery requir ing 14 days.

Rates of leaf da rk respi ra t ion were significantly influ- enced by bo th increased and decreased growth i r rad iance (Fig. 5). Fo l lowing the H - L transfer, da rk respi ra t ion rates in all species d r o p p e d steadily until the end of the t ime- course, with the ma jo r i ty of the response occurr ing within the first 14 days. By day 56-70, leaves of the three species had resp i ra t ion rates which closely a p p r o x i m a t e d those of new leaves p roduced in the L l ight t rea tment , following decreases to day 28 of 64, 66 and 63% in O. populifolius, D. myoporoides and A. ingens respectively (Table I). The increase in growth i r rad iance which followed the L -H

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F i g . 4 . The time-course of the response of apparent quantum yield in mature leaves of O. populifolius, D. myoporoides and A. ingens following transfer between various light treatments. See Fig. 2 for details

223

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transfer produced a more rapid respiration response than did the H-L transfer, with significant increases (P _< 0.01) in dark respiration of 165% in O. populifolius, 196% in D. myoporoides and 103% in A. ingens. This increase was largely complete by day 3 in O. populifolius and A. ingens. Respiration was greater in new leaves produced in the high light treatment than in pre-existing leaves at the end of the time-course. The increase in respiration in leaves of O. populifolius following the VL-H transfer was identical to that in the L-H transfer. The response of dark respir- ation rate in the three species was closely reflected in the response of their light compensation points (data not shown).

A useful measure of the physiological efficiency of the photosynthetic characteristics of leaves is the relationship between photosynthetic capacity and dark respiration Rdark (Azcon-Bieto and Osmond 1983; Sims and Pearcy 1991). Clear trends emerged in the response of the ratio of Area x to dark respiration rate to the transfers between light regimes (Fig. 6). Following exposure to deep shade (the H-L transfer), an increase in this ratio was observed to day 7 in O. populifolius and day 14 in D. myoporoides and A. ingens, after which it decreased to day 28 in association with the continuing reduction in photosynthetic capacity. Thus the acclimation response of Area x to shading lagged behind that of respiration. By the end of the time-course

the Amax/Rdark ratio was slightly higher than in new leaves produced in the deep shade, due largely to lower photo- synthetic capacities in the new leaves. The L-H transfer produced a rapid and permanent reduction in the Amax/Rdark ratio of 62% in O. populifolius, 49% in D. myoporoides and 30% in A. ingens (Table 1), although some recovery, associated with an increase in A . . . . was noted in O. populifolius and A. ingens.

The importance of the range of acclimatory responses observed above to leaf carbon balance in the new light conditions can be seen in Fig. 7. Following the L-H transfer (Fig. 7a), daily leaf carbon balance exhibited a response very close to that of photosynthetic capacity (see Fig. 2). By day 28, increases of 41.6 and 35.5% were noted in D. myoporoides and A. ingens, respectively (Table 2), although leaves of O. populifolius did not regain pre- transfer levels, and exhibited a decrease of 5.8%. New leaves of all species produced subsequent to transfer had potentials for carbon fixation which were considerably higher than those of pre-existing leaves, commensurate with their high photosynthetic capacities. In contrast to the L-H transfer, daily leaf carbon balance increased following the H-L transfer (Fig. 7b) while Ama x decreased (see Fig. 2). In all species the acclimation response resulted in an increase in net carbon balance from a negative value (of about - 20 mmol C m - z d - 1) to a positive value in 3-7

224

E 0

2 o_

n,,

13

E

t,c I3

E

50

40

30

20

10

0

50

40

30

20

10

0

O. p o p u l i f o i u s . . . . . I n ,

I ' 0 7 14 21 28 56 70 New

D. m y o p o r o i d e s I , I

50

40

,30

20

10

0

' ' ' ' ' 1 1 ' 0 7 14 21 28 56 70 New

A. incjens . . . . [ L , ,

, I ~il ~ 0 7 14 21 28 56 70 New

T ime (days f r o m t r a n s f e r )

Fig. 6. The time-course of the response of the ratio of light saturated assimilation rate (Amax) to dark respiration rate (Rdark) in mature leaves of O. populifolius, D. myoporoides and A. ingeus following transfer between various light treatments. See Fig. 2 for details

days. The extent of this response was similar for the three species (Table 2).

Discussion

Photosynthetic acclimation

The light regime to which plants were exposed produced substantial acclimation in all the photosynthetic para- meters examined. The H-L light transfer was in all cases associated with a decrease in photosynthetic capacity, stomatal conductance, apparent quantum yield and dark respiration (Figs. 2-5). Acclimation following the L-H transfer was more restricted, especially for stomatal con- ductance and quantum yield.

Reduction in quantum yield and photosynthetic capa- city in response to shading has been associated with a rapid decrease in electron transport capacity (von Caem- merer and Farquhar 1984; Davies et al. 1986) and car- boxylase activity (von Caemmerer and Farquhar 1984), although Besford (1986) measured no change in the activ- ity of Calvin cycle enzymes in low light. Observations from the present study indicate that photosynthetic capacity is maintained at close to pre-transfer levels for approxim- ately 7 days after transfer to deep shade, and can therefore respond maximally to large increases in irradiance. Sims and Pearcy (1991) also noted a limited and slow change in Alocasia in response to H-L transfer. Such characteristics may prove critical to the long-term functioning of high- light adapted plants in conditions where light levels may vary significantly for periods of days or weeks (e.g. in canopy gaps; in response to weather patterns).

( a ) O. p o p u l i f o l i u s 700 . . . . . I I ,

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I E 0 / I I ' 0 7 14 21 28 56 70 New (.3

-S 700 , D. m y o p o r o i d e s

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0

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Fig. 7. a The time-course of the response of simulated daily net carbon balance in mature leaves of O. populifolius, D. myoporoides and A. ingens following transfer between filtered shade at 5% PAR and neutral shade at 60% PAR (designated as L-H in the text) (open squares), and (for O. populifolius only) filtered shade at 1% PAR and neutral shade at 60% PAR (designated as VL-H in the text) (open circles), b The time-course of the response of simulated daily net carbon bal- ance following transfer between neutral shade at 60% PAR and filtered shade at 1% PAR (de- signated as H-L in the text) (filled squares). Data for new leaves pro- duced following transfer are shown to the right of each time- course (New). Mean values were calculated using data described in Fig. 2, 4 and 5

225

Table 2. Percentage change in daily net carbon balance of mature leaves of O. populifolius, D. myoporoides and A. inoens at day 28 after transfer to the new light environment

O. populiJblius D. myoporoides A. ingens

H-L +157 +157 +110 L-H - 5.8 +41.6 +35.5 VL-H +37.5

Transfers were between (a) neutral shade at 60% PAR and filtered shade at 1% PAR (designated as H-L in the text), (b) filtered shade at 5% PAR and neutral shade at 60% PAR (designated as L-H in the text), and (c) filtered shade at 1% PAR and neutral shade at 60% PAR (designated as VL-H in the text), for O. populifolius only. Percentage changes were calculated from mean data shown in Figs. 7a, b

Initial photoinhibition, with an associated reduction in quantum yield, is common in rainforest plants transferred from low to high light (Langenheim et al. 1984; Oberbauer and Strain 1985; Chow et al. 1991). However, the rate and extent of recovery of quantum efficiency exhibited by the three species studied here is, by comparison, less common. Although the overall insensitivity of quantum yield to long-term increases in irradiance is indicative of inflexibil- ity in the leaf physiology of the three species studied, this conclusion overlooks the capacity for recovery of photo- synthetic machinery following the photoinhibitory effects of the L-H transfer. This recovery is particularly notable in O. popuIifolius from the VL-H treatment.

All three species displayed a potential for enhancement of photosynthetic capacity in high light, with significant increases in Ama x measured by day 28 in D. myoporoides and A. ingens. This potential was more limited in O. populifolius. Leaves from transferred plants did not reach the assimilation rates of new leaves in high light, indicating the presence of limitations imposed by the light environ- ment from which plants have been transferred. The resist- ance of apparent quantum yield to change following exposure to increased irradiance indicates that increases in carboxylation and electron transport capacity, rather than an enhancement of light harvesting components, may be responsible for the increases in photosynthetic capacity which were observed (Davies et al. 1986; Besford 1986). Although Area x increased significantly in two of the three species, it did so with minimal increase in stomatal con- ductance, a feature which may be important in limiting acclimation potential (see below). In addition, if the capa- city for translocation of assimilates is limited by structural characteristics set at the time of leaf expansion, then the build-up of labile carbohydrates which results from in- creased photosynthetic production may cause end-pro- duct inhibition. Ultimately, this may limit the extent of photosynthetic acclimation to increased irradiances.

The relationship between photosynthetic capacity and respiration rate in leaves is also of interest (Bazzaz 1991). Although some recovery was noted in O. populifolius and A. ingens, no species showed an increase in photosynthetic capacity in pre-existing leaves sufficient to overcome the large increases in dark respiration associated with expos- ure to high-light conditions (Fig. 6). Thus, although

increases in dark respiration were compensated for in absolute terms by increases in Area x in D. myoporoides and A. ingens, all species continued to operate at lower effici- ency (that is, a lower Amax/Rdark ratio) following L-H transition. This limitation is in contrast to findings for Alocasia, in which the ratios of respiration to photo- synthetic capacity adjusted within 3 days to match those of plants grown continuously in the new environment (Sims and Pearcy 1991). However, new leaves of O. popul![olius and D. myoporoides developed photosynthetic capacities which resulted in ratios of Area x to dark respiration that were higher than those of pre-transfer leaves.

The responses of stomatal conductance to changes in light were clearly different in extent following the H-L and L-H transfers, and may in part explain the different acclimation responses of photosynthetic capacity to these transfers. It is likely that structural characteristics in the fully expanded leaves limit increases in the stomatal aperture which would be required for accelerated gas exchange following the L-H transfer. The limited acclima- tion responses in Gsma x to the L-H transfer are consistent with the findings of Strauss-Debenedetti and Bazzaz (1991) for four of the five species of tropical Moraceae they studied, and those of Sebaa et al. (1987) in Lolium.

Dark respiration was the parameter most sensitive to changes in light environment. Considerable adjustment of measured Rdark occurred in response to both an increase and a decrease in irradiance. A rapid decline in Rdark following exposure to deep shade (and an increase follow- ing exposure to high light) in the three species studied conforms with the observations on Lolium by Sebaa et al. (1987) and on Alocasia by Sims and Pearcy (1991). The explanation for these post-transfer changes involves the interaction between at least three components; (i) internal leaf carbohydrate status, (ii) respiration associated with repair processes in photo-damaged leaves and (iii) base levels of maintenance respiration. Following both the H-L and L-H transfers the response of Am~ x lagged behind that of dark respiration rate, indicating that respiration rates in these leaves are likely to be primarily determined by the accumulation of photosynthates and hence the photo- synthetic integral in the period prior to measurement (see Azcon-Bieto and Osmond 1983). In the short term the photosynthetic integral is determined by the immediate light environment to which leaves are exposed. Thus, following the H-L transfer, exposure to very low PFDs immediately reduces photosynthetic production and accu- mulation of assimilates in leaves. The reverse is true for the L-H light transfer, where increased concentrations of labile carbohydrates tend to increase respiration rates, but the effect in this case may be accentuated by structural limitations to the translocation of assimilates away from leaves. This finding, in conjunction with the fact that photosynthetic capacity is largely maintained for 7 days following shading and is slow to respond to increased irradiance, would seem to indicate that dark respiration is not strongly correlated with the maintenance of photo- synthetic capacity (see also Sims and Pearcy 1991). In order to elucidate this more clearly the proportion of the increase in respiration following L-H transfer that is associated with the repair and construction of photo- synthetic machinery would need to be determined. The

226

relationship between light availability and maintenance respiration is also unclear (Freeden and Field 1991), but it would be reasonable to assume that maintenance respir- ation is significantly lower in shade-adapted leaves. This is consistent with the finding that Rdark is lower in L-H acclimated leaves than it is in leaves newly produced in the high light environment (Fig. 7), which indicates that leaf

"O characteristics determined in the original environment impose an upper limit on the increase in Rdark induced by E high irradiance.

In the simulations of canopy opening/closure per- -6 formed here, simultaneous changes in light quality and E quantity, which are typical of natural conditions, must also be considered. Experiments were conducted in

U conjunction with the study to monitor the responses of ~" leaves to the significant changes in the spectral composi- -6 tion of radiation to which they were exposed (Turnbull m 1992). Although responses varied between species, there is strong evidence to suggest that following transfer between .a~.

O the two light treatments, acclimation occurs in the photo- synthetic machinery of pre-existing leaves to accommo-

0 date changes in the spectral composition of light. This o acclimation resulted in measurable changes in the relative photosynthetic performance of leaves when photosyn- thesis was determined using a light source which approx- imated either the pre- or post-transfer light environment (Turnbull 1992). The trend in this response was one of adaptation to the post-transfer light treatment.

Photosynthetic acclimation and leaf carbon balance

Although the increases in daily carbon balance exhibited by the three species following the H-L transfer were limited in absolute terms, they may represent a significant response in terms of the capacity of a given plant to survive deeply shaded understorey conditions (Fig. 7b). H-L ac- climating leaves were able to maintain a slightly positive carbon balance during the time-course. This response would not have been possible had not dark respiration rates decreased to the extent they did. Fully acclimated leaves from the H-L transfer had very similar carbon balance characteristics in deep shade to new leaves pro- duced after transfer. Their potential for a shade tolerating response was thus very high. That new leaves displayed a carbon balance no greater than fully acclimated pre- existing leaves also indicates that the response to very deep shade is not limited in mature leaves.

Leaf carbon balance following the L-H transfer (Fig. 7a) followed closely the response of photosynthetic capacity illustrated in Fig. 2. Thus, carbon balance in high light conditions would appear to be determined strongly by Am,x. This is confirmed by the close relationship which is found when daily carbon balance during the transfer time-courses is plotted against Area x (Fig. 8b). The reason for this close relationship is that at high photon flux densities leaves are operating in the light-saturated por~ tion of their light response for long periods during the day. Dark respiration rates have little influence over net carbon balance in leaves acclimating to high light regimes, as

evidenced by the lack of a relationship between these parameters in Fig. 9b.

( o ) H - L T rons fe r i

20

V 10 • o

[ ]

[ ] • 0

- 1 0

- 2 0 n

I I

0

V

I

0 5 10 15 20

(b) L-H T r o n s f e r I I

6O0

50O ¢p

400 V V

20O O0 O

100 g O

0 I I I

5 10 15 20 -2. -1

AssimilaUonma x (/~mol CO 2 rn s )

Fig. 8a, h. The relationship between daily carbon balance (taken from Fig. 7) and maximum assimilation rate (Ama x ; taken from Fig. 2) during acclimation to transfers between a neutral shade at 60% PAR and filtered shade at 1% PAR (H-L), b filtered shade at 5% PAR and neutral shade at 60% PAR (H-L), and (for O. populifolius only) filtered shade at 1% PAR and neutral shade at 60% PAR (VL-H, diamonds). Data for the three species are plotted together (0. populifolius, circles; D. myoporoides, triangles; A. ingens, squares). Data for new leaves produced following transfer are also included (closed symbols)

In contrast, carbon balance following the H-L transfer (Fig. 7b) mirrored the response displayed by dark respir- ation (Fig. 5) and was thus strongly influenced by underly- ing rates of carbon loss. This influence manifests itself as an inverse relationship between carbon balance and dark respiration rate (Fig. 9a). The relationship between net carbon balance and maximum assimilation rate (Fig. 8a) was, by comparison, very weak. The primary reason for these findings is the converse of that given for the L-H transfer - that leaves operating at very low photon flux densities can not realize their photosynthetic potentials. By far the largest proportion of 10-min averages measured in the understorey of the forest site from which the seedlings were taken were below 10 gmol m- z s- 1 (Turn- bull and Yates, 1993). Such values are only marginally higher than the light compensation points for photosyn- thesis in many of the species which grow at this site (Turnbull 1991). This indicates that the most critical mechanisms involved in acclimation to extreme shade are likely to be those which relate to the minimization of carbon losses, rather than those which may enhance the efficiency of carbon gain (Boardman 1977; Chow et al. 1988). In this context, parameters which describe photo-

(o) H-L Transfer i i i i

20

V V

10 QO

--- [] 0

I 0

? E -io (0 0

V

-o - 2 0 ~3 E

I I I I

• , J 0 . 0 0 . 2 0.4 0 . 6 0 . 8 1 . 0 CD o (b) L-H T r a n s f e r

i i i y l

5 eoo m

e- 5 0 0 o

.t~ Q k. o 4 0 0

0 0 V

o [] 0 []

a 2 0 0 [] 0 O 0

% 1 0 0 0

0 ¢

0 I I I I 0 . 0 0 . 2 0 , 4 0 . 6 0 . 8 1 . 0

- 2 - 1 Dark R e s p i r a t i o n ( / I m o l CO 2 m s )

Fig. 9a, b. The relationship between daily carbon balance (taken from Fig. 7) and dark respiration rate (Reark; taken from Fig. 5) during acclimation to changes in light regime. See Fig. 8 for details

synthetic capacity (Amax) and the efficiency of light use (apparent quantum yield) provide us with less indication of the capacity of a plant for survival in understorey condi- tions than do parameters which indicate rates of leaf and whole-plant carbon loss.

Concluding remarks

The findings of this study, in association with those of an earlier study into the physiological plasticity of these (and three other) Australian rainforest species (Turnbull 1991), are consistent with previous findings that the extent to which a species will acclimate to changes in light may not be predicted easily on the basis of successional status (Walters and Field 1987). The late-stage species A. ingens has been found to have significant physiological plasticity to a wide range of constant light conditions (Turnbull 1991), and in this study was found to have significant potential for acclimation to both increases and decreases in light. In contrast, the early-stage species O. populifolius, which maintains fairly constant photosynthetic capacity and survives over a range of constant light conditions from 1% to full sunlight, here had the most limited acclimation response. The mid-stage species, D. myoporoides, had characteristically high levels of plasticity and potential for acclimation. As stressed by Strauss-Debenedetti and Bazzaz (1991), the classification of the ecophysiological position of species in plant communities is best achieved with an evaluation of both plasticity and acclimation to

227

environmental variables. In this way it is possible to characterize the physiological responses of both existing and future foliar units to environmental heterogeneity. It is essential that both sets of characteristics are incorporated, where possible, into models of forest canopy functioning.

In considering these characteristics, acclimation to either increases in light (which follow gap formation) or decreases in light (associated with gap closure and self- shading) must be considered as functionally different processes. The extent of the responses of Area x and GSma x have been found to be greater following shading than following exposure (Figs. 2 and 3). Clearly, the suite of physiological and structural characteristics which ulti- mately impinge on the gas exchange of leaves are limited in their capacity for enhanced performance. As described above, there is evidence of increased photosynthetic capa- city following the L-H transfer, but minimal increase in stomatal conductance. It would thus appear that struc- tural limitations to increases in gas exchange between the leaf and atmosphere may be significant in determining the acclimation potential of the leaves photosynthetic capa- city, and point to the need for combining both morpho- logical/structural and photosynthetic characteristics in studies of this kind (Osunkoya and Ash 1991). Previous transfer experiments (Strauss-Debenedetti and Bazzaz 1991) have alluded to the possibility of"carry-over effects", which are thought to decrease with continued leaf produc- tion in the new light conditions. Given that the first newly formed leaves of O. populifolius and D. myoporoides plants transferred from low to high light environments had strongly enhanced CO2-fixing capabilities, such limita- tions are unlikely to be significant in these species, al- though they may be significant in the case of A. ingens.

Acknowledgements. The assistance of the Queensland Forest Service is gratefully acknowledged. This work was supported by an Austra- lian Postgraduate Research Award to MHT and by the Australian Research Council (Grant No. A18931866).

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