Redalyc.Drought Under Natural Conditions Affects Leaf Properties

Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela

Taisma, María Angélica; Herrera, Ana Drought under natural conditions affects leaf properties, induces cam and promotes reproduction in plants of talinum triangulare Interciencia, vol. 28, núm. 5, mayo, 2003, pp. 292-297 Asociación Interciencia Caracas, Venezuela

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative DROUGHT UNDER NATURAL CONDITIONS AFFECTS LEAF PROPERTIES, INDUCES CAM AND PROMOTES REPRODUCTION IN PLANTS OF Talinum triangulare

María Angélica Taisma and Ana Herrera

SUMMARY

Talinum triangulare is a perennial, deciduous shrub com- in plants receiving the natural water supply than in watered monly found in tropical seasonally-dry environments. In this study plants. The former had a higher production of flowers and fruits an integrative assessment of the responses of this species to than experimentally watered plants. No significant differences be- drought is provided. Water availability was manipulated under tween the two groups of plants were found in the frequency of natural conditions and seasonal changes followed in a range of pollinator visits. Leaf angle, rolling and reflectance, and the ratio leaf characteristics and reproductive output. The leaf responses reproductive mass/leaf mass showed positive correlations with measured included rolling, paraheliotropic movements, increase in night-time acid accumulation (r2=0.83, 0.64, 0.59 and 0.64, re- reflectance and induction of Crassulacean acid metabolism spectively). The reproductive mass/leaf mass ratio was positively (CAM). Plants growing in a seasonally dry location and subjected correlated with leaf rolling (r2=0.51) and leaf reflectance to the natural rain regime were studied for approximately one (r2=0.79) but not with leaf angle. Results suggest that drought year; 30 plants of this population were frequently watered. Noc- causes the increase in leaf angle, rolling and reflectance, as well turnal acid accumulation and leaf rolling, angle and reflectance as CAM activity, and serves as a cue for the increase in fecundity were higher throughout the year, except during the rainy season, in plants of T. triangulare growing in the field.

RESUMEN

Talinum triangulare es un arbusto perenne y caducifolio que en plantas regadas. Las primeras tuvieron mayor producción de crece comúnmente en ambientes tropicales estacionalmente secos. flores y frutos que las plantas experimentalmente regadas. No se Este estudio aporta un enfoque integrador de las respuestas de encontraron diferencias significativas en la frecuencia de visitas esta especie a la sequía. La disponibilidad de agua fue manipula- de polinizadores a ambos grupos de plantas. El ángulo, da en condiciones naturales y se midieron los cambios estaciona- enrollamiento y reflectividad foliar, y el cociente masa reproducti- les en un grupo de características foliares y órganos reproductiva/masa foliar mostraron correlaciones positivas con la acumula- vos. Las respuestas foliares medidas incluyen enrollamiento, movi- ción nocturna de ácidos (r2=0,83; 0,64; 0,59 y 0,64 respectiva- mientos paraheliotrópicos, aumento de reflectividad e inducción mente). El cociente masa reproductiva/masa foliar se correlacionó del metabolismo ácido de Crasuláceas (CAM). Durante aproxima- positivamente con el enrollamiento foliar (r2=0,51) y la damente un año se estudiaron plantas que crecían en una locali- reflectividad (r2=0,79) pero no con el ángulo foliar. Los resultados dad estacionalmente seca, sujetas al régimen natural de lluvias; sugieren que la sequía ocasiona un aumento en el ángulo, 30 de estas plantas fueron regadas frecuentemente. La acumula- enrollamiento y reflectividad foliar, así como en la actividad del ción nocturna de ácidos y el enrollamiento, ángulo y reflectividad CAM, y actúa como una señal para el aumento de la fecundidad foliar fueron mayores durante todo el año, excepto durante la en plantas de T. triangulare en el campo. época de lluvias, en plantas con suministro natural de agua que

Introduction (Begg, 1980; Ehleringer, Water deficit may cause a al., 1995), while many others 1980). Also, Crassulacean severe reduction in reproduc- do it during the dry season Deciduous plants subjected acid metabolism (CAM) may tive output (Lee and Bazzaz, (Monasterio and Sarmiento, to drought in seasonally-dry be induced by drought in 1986; Lee, 1988); this reduc- 1976), when photosynthetic environments may display a facultative plants and is gen- tion may be due to abortion activity must be lower. range of responses that are erally considered an adaptive of different reproductive parts: In plants of the inducible- thought of as adaptive to wa- response to water deficit be- buds, ovules, fruits or seeds. CAM species, Mesembryanthe- ter deficit. Frequent re- cause its operation increases Many tropical plants, includ- mum crystallinum, an ex- sponses of plants to drought water use efficiency, i.e. the ing herbs and shrubs, flower tremely large seed production include leaf rolling, parahe- ratio between assimilated and set fruit during the rainy during the dry season was cor- liotropic movements and in- CO2 and transpired water season (Monasterio and related with the extension of crease in leaf reflectance (Winter and Smith, 1996). Sarmiento, 1976; Seghieri et the life cycle due to CAM op-

KEYWORDS / Crassulacean Acid Metabolism / Fecundity / Leaf angle / Leaf Rolling / Leaf reflectance / Paraheliotropic movement / Received: 07/04/2002. Modified: 04/28/2003. Accepted: 04/30/2003

María Angélica Taisma. Biolo- and Anatomy, Instituto de Ana Herrera. Biologist, UCV. dress: Apartado 47577, Cara- gist, Universidad Central de Biología Experimental (IBE- Ph.D. in Plant Sciences, Uni- cas 1041 A. e-mail: Venezuela (UCV). D.Sc. in UCV). Address: Apartado versity of London. Professor, [email protected] Botany, UCV. Lecturer, Labo- 47114, Caracas 1041 A. Laboratory of Xerophyte Eco- ratory of Plant Morphology e-mail: [email protected] physiology (IBE-UCV). Ad-

292 0378-1844/03/05/292-06 $ 3.00/0 MAY 2003, VOL. 28 Nº 5 RESUMO

Talinum triangulare é um arbusto perene e caducifólio que regadas. As primeiras tiveram maior produção de flores e frutos cresce comumente em ambientes tropicais com estações secas. que as plantas experimentalmente regadas. Não se encontraram Este estudo aporta um enfoque integrador das respostas desta diferenças significativas na freqüência de visitas de polinizadores espécie à seca. A disponibilidade de água foi manipulada em a ambos grupos de plantas. O ângulo, enrolamento e condições naturais e mediram-se as mudanças de estações num refletividade foliar, e o cociente massa reprodutiva / massa foliar grupo de características foliares e órgãos reprodutivos. As res- mostraram correlações positivas com a acumulação noturna de postas foliares medidas incluem enrolamento, movimentos para- ácidos (r2=0,83; 0,64; 0,59 e 0,64 respectivamente). O cociente heliotrópicos, aumento de refletividade e indução do metabolis- massa reprodutiva / massa foliar se correlacionou positivamente mo ácido de Crassuláceas (CAM). Durante aproximadamente um com o enrolamento foliar (r2=0,51) e a refletividade (r2=0,79), ano estudaram-se plantas que cresciam numa localidade com mas não com o ângulo foliar. Os resultados sugerem que a seca estação seca, sujeitas ao regime natural de chuvas; 30 destas ocasiona um aumento no ângulo, enrolamento e refletividade plantas foram regadas freqüentemente. A acumulação noturna de foliar, assim como na atividade do CAM, e atua como um sinal ácidos e o enrolamento, ângulo e refletividade foliar foram mai- para o aumento da fecundidade em plantas de T. triangulare no ores durante todo o ano, exceto durante a época de chuvas, em campo. plantas com subministro natural de água que em plantas

eration (Winter, 1985). In ing changes in leaf responses which remained under natural exchange was measured since greenhouse-grown plants of and thus establish the possible watering conditions was la- nocturnal sampling was dan- Talinum triangulare with relationship between these re- beled with plastic tags. The gerous due to the presence of CAM induced by drought, fe- sponses, allegedly adaptive to plants were 50cm tall on aver- snakes. Instantaneous water cundity was higher than in drought, and fecundity in age and had profuse lignified use efficiency (IWUE) was watered plants, survival re- plants of T. triangulare. branching. Those individuals calculated as the average of maining unchanged (Taisma that were tagged at the begin- the photosynthetic rate/transpi- and Herrera, 1998). Materials and Methods ning of the experiment re- ration rate, measured every Plants of the shrub T. mained alive on each sampling hour during the light period. triangulare (Jacq.) Willd. Plant material and field site. date. Natural carbon isotopic dis- (Portulacaceae) have a wide Talinum triangulare (Jacq.) Microclimate. Photosynthetic crimination (δ13C). Dried leaf range of responses to water Willd. (Portulacaceae) is a pe- photon flux density (PPFD) and fruit samples were ground deficit which may be adaptive. rennial, deciduous shrub with was measured with an LI-170 in a mill and analyzed for δ13C Well-watered plants present a lignified, non-photosynthetic quantum sensor connected to at the Laboratory of Isotopic typical C3 metabolism and, stems; the leaves can last as an LI-185 meter (LI-COR Ecology, Centro de Energia within a few days of drought, long as two months after the Inc., Lincoln, Nebraska, USA). Nuclear na Agricultura, Uni- switch to CAM, with a low onset of water deficit. The Air temperature was measured versidade de Sâo Paulo, (Pira- night-time CO2 assimilation plant is iteroparous, i.e. it is with thermistors connected to cicaba, Brazil). rate (Herrera et al., 1991) to capable of reproduction several a telethermometer (Yellow Fecundity schedules. On each eventually enter the gas-ex- times during its life span. The Springs Instruments Co., Yel- study date, the number of inflo- change and acidity pattern field work was carried out at low Springs, Ohio, USA). rescences per branch was known as CAM-idling (Winter the Henri Pittier National Park, Gas exchange. Measure- counted on five labeled plants and Smith, 1996). Under Estado Aragua, Venezuela, ments of CO2 and H2O ex- of each treatment. In order to drought, leaves have a parahe- 10º13’N - 67º14’W, at ap- change were made on three determine the mass of buds, liotropic movement whereby proximately 20masl, in a site randomly selected leaves from flowers and fruits per inflores- their angle relative to the hori- near the village of Cuyagua by different individuals per treat- cence, fifty inflorescences per zontal plane increases with a road outside the forest, un- ment on each date, with an treatment were randomly col- drought; also, they appear der full sun exposure. Plants LCA2 IRGA connected to a lected among all plants of each more reflective and the lamina were studied on five dates dur- PLC(B) leaf chamber and an treatment. Fifty flowers and rolls about its margins onto ing 1990-91, covering the dry ASU(MF) air supply unit fruits per treatment were ran- the abaxial surface. By reduc- and rainy seasons and the (Analytical Development Co. domly collected and preserved ing heat load and increasing transitions thereof. Rainfall Ltd., Hoddesdon, U.K.). Leaf in 70% ethanol for determina- water saving, these features, data (Figure 1a) were col- temperature during measure- tion of the number of ovules together with CAM induction, lected at the nearby Ocumare ments was approximately 2ºC per flower, and viable and abor- may help explain how leaves de la Costa weather station; higher than air temperature. Il- tive seeds per fruit. As a mea- can remain green after two mean annual precipitation is lumination was natural and sure of the influence of changes months of drought. 800mm. In an area of approxi- measurements were taken un- in leaf properties on fecundity, The above-mentioned results mately 100m2 with a dense der clear skies. Between 08 the relative reproductive mass and observations suggested the population of T. triangulare, and 16h, PPFD ranged from was calculated in plants, col- present study. Plants of T. the dominant species, 30 indi- 500 to 2000µmol·m-2·s-1, suffi- lected as indicated below, as the triangulare growing in the viduals were watered immedi- cient to saturate light curves in ratio of reproductive mass to field were subjected to either ately after the first measure- T. triangulare (Herrera et al., leaf mass (RRM, as %), the natural rainfall or frequent ments were taken, in Decem- 1991). In December 1990 a where reproductive mass in- watering through the seasons. ber 1990, and weekly thereaf- 24h gas exchange course was cluded peduncles, buds, flow- The objective of the experi- ter, until September 1991. An- done; for the rest of the sam- ers and fruits. A similar cal- ment was to prevent by water- other group of 30 individuals pling period only daytime gas culation was done for indi-

MAY 2003, VOL. 28 Nº 5 293 vidual organs. Total of rolled to unrolled croclimatic conditions in De- seed number/leaf mass lamina area (as %). cember and August were, re- was calculated multi- Pollinator visit fre- spectively: maximum PPFD, plying the numbers of quency. The number of 2000 and 1573µmol·m-2·s-1, seeds/fruit by fruits/ insect visits to a single and air temperature, 40.0 ±1.5 inflorescence by inflo- flower was counted and 33.1 ±1.5ºC. rescences/plant and during 3min between In naturally watered plants, dividing by leaf mass. 07 and 08h, when an- a marked influence of water Biomass allocation. thesis takes place in deficit on the magnitude of

Unlabeled naturally this species. Ten flow- daytime CO2 assimilation rate watered plants (n=5) ers per treatment were (A) was observed during the as well as experimen- observed on each date. period of study, and lower tally watered plants No attempt was made values were found in naturally (n=5) were harvested to distinguish among than experimentally watered on each date and their types of pollinators. plants in February and June organs separated. Dry Statistics. Results (Figure 2). Reductions in A mass (48h at 60ºC) of presented are mean due to water deficit resulted organs was weighed ±SE. Data were ana- in diminished daytime C bal- on an analytical bal- lyzed through linear ance; the average IWUE was ance. Figura 1. a: Monthly rainfall measured at the and non-linear re- higher in naturally than ex- Nocturnal acid ac- Ocumare de la Costa weather station during the gressions and pair- perimentally watered plants in cumulation. Samples year of this study. b: Seasonal changes in nocturnal wise ANOVA by date February (Table I). The rela- acid accumulation (∆H+) of plants of T. triangulare. (n=6) were collected (p<0.05) using the sta- tive recycling of CO2 by at dawn and dusk and Values of ∆H+ are mean ±SE (n=6). Closed sym- tistical package Statis- CAM in naturally watered bols: naturally watered plants; open symbols: ex- kept in liquid N2. tica for Windows 93. plants, calculated with values Boiled aqueous leaf perimentally watered plants. An asterisk indicates of December as % recycling extracts were titrated significant differences between treatments (p<0.05). Results = 100x[(0.5x∆H+)-integrated to pH 7.0 with 10mM night-time A)]/(0.5x∆H+), tak- KOH (Nobel, 1988). Nocturnal acid accu- ing ∆H+ on an area basis (af- Nocturnal acid accumulation was higher in ter Griffiths, 1988) was 83%. mulation (∆H+) was naturally than in ex- Figure 3 shows the seasonal calculated as the dif- perimentally watered changes in the pattern of bio- ference between dawn plants in February and mass allocation of plants in this and dusk values. June but not in August, experiment. Whole plant mass Leaf angle, area re- at the peak of the rainy of naturally watered plants was duction and reflec- season, or in October, not significantly different from tance. Between 20 when watering was that of experimentally watered and 50 randomly se- stopped (Figure 1). Mi- plants, except in October, when lected leaves per treatment were measured for each variable. TABLE I Leaf angle relative to SEASONAL CHANGES IN DAYTIME the horizontal plane CARBON BALANCE AND INSTANTANEOUS was measured with a WATER USE EFFICIENCY OF NATURALLY AND protractor; values EXPERIMENTALLY WATERED PLANTS higher than 90º indi- OF Talinum triangulare cate that leaves be- came pendulous. Re- flectance was esti- Daytime C IWUE mated as the fraction Treatment Month balance (mmol·mol-1) of incident PPFD re- (mmol·m-2) flected by the adaxial surface of leaves; a Naturally Dec 25.1 ±7.2 0.7 ±0.1 measurement was watered Feb 19.1 ±1.5 3.7 ±1.1 taken of the incident Jun 62.7 ±1.6 0.6 ±0.1 PPFD and immedi- Aug 279.6 ±18.3 2.1 ±0.2 ately of the PPFD re- Oct 56.6 ±13.0 1.5 ±0.1 flected by the leaf at times of peak solar Experimentally Feb 98.3 ±9.3 1.7 ±0.6 radiation, placing the watered Jun 109.7 ±3.6 1.3 ±0.1 sensor perpendicular Aug 316.6 ±4.5 1.9 ±0.2 Figure 2. Changes in the daily course of CO2 ex- to the lamina without change (A) during the indicated months in plants Oct 16.6 ±2.7 1.3 ±0.1 modifying leaf angle. of T. triangulare. Closed circles: naturally watered Daytime C balance was obtained integrating the daytime (10-12 The reduction in leaf plants; open circles: experimentally watered plants. h) courses of A; values are mean ±SE (n=3). Values of instanta- area by rolling was Values are mean ±SE (n=3). The filled bar indi- neous water use efficiency are the mean ±SE (n≥10) of the ratio calculated as the ratio cates the lenght of the night. A/transpiration rate.

294 MAY 2003, VOL. 28 Nº 5 Figure 4. a: Relationship between daytime carbon balance and nocturnal acid accumulation in T. triangulare. b: Relationship between daytime carbon balance and relative reproductive mass in T. triangulare. Closed symbols: naturally watered plants; open sym- Figure 5. Seasonal changes in the ratio be- bols: experimentally watered plants. Values tween the mass of reproductive organs and are individual data points. The regression leaf mass (organs indicated in each panel), in lines and the correlation coefficients for all plants of T. triangulare. Closed symbols: natu- data pooled together are shown. rally watered plants; open symbols: experi- Figure 3. Seasonal changes in plants of T. mentally watered plants. Values are mean ±SE ≤ ≤ triangulare growing in the naturally and the (5 n 10). An asterisk indicates significant dif- experimentally watered plots, in whole plant of leaves of either drought in both ferences between treatments (p<0.05). mass (a), the proportion of total plant mass treatment, giving treatments, al- allocated to leaves (b), the shoot/root ratio a mean of -24.6 though low val- (c) and the relative reproductive mass (d). ±0.6‰. ues can be found in experi- plants on any sampling date; Closed symbols: naturally watered plants; The relative mentally watered plants, more rains caused a reduction in open symbols: experimentally watered ≤ ≤ mass of buds, so at intermediate values of pollinator visits of approxi- plants. Values are mean ±SE (5 n 10). An flowers and fruits DH+ (Figure 7). Linear sig- mately three times relative to asterisk indicates significant differences be- per plant was nificant relationships were moderate drought (Table II). tween treatments (p<0.05). equal or larger in found between RRM and roll- naturally than in ing (r2=0.51; p=0.03) and re- Discussion it was higher. The proportion experimentally watered plants flectance (r2=0.79; p=00007) of whole plant mass allocated (Figure 5). The number of but not leaf angle (p=0.12). The results of the present to leaves was higher in experi- ovules per flower was higher As suggested by Figures 1 study confirm previous obser- mentally than in naturally wa- and the seed abortion ratio and 5, significant correlations vations on the induction of tered plants in February as lower in naturally watered were found between ∆H+ of CAM by water deficit done well as October, while the plants (Figure 6). Seed abortion naturally watered plants and under laboratory conditions shoot/root ratio was always ratio of naturally watered plants mass of flowers per leaf mass (Herrera et al., 1991). CAM higher, except in June. The was higher in February than in (r2=0.62; p=0.04) and mass of induction was fully reversed RRM, a measure of how December (the corresponding buds per leaf mass (r2=0.86; by irrigation or by natural much leaves contribute to re- values for experimentally wa- p=0.03). The correlation of rainfall events. Daytime car- production, was higher in tered plants are not available as ∆H+ with the number of bon balance decreased, and naturally than experimentally these had no fruits). The high- ovules per flower and of vi- leaf angle, rolling, reflectance watered plants in February and est number of seeds per leaf able seeds per fruit was very and ∆H+ increased with October. mass occurred in December low (r2=0.07). drought, significant relation- Nocturnal acid accumula- (Figure 6). Differences in fecundity ships occurring between ∆H+ tion and RRM decreased with Taking DH+ as an indicator due to treatment were appar- and the increase in leaf angle an increase in daytime carbon of drought, it can be seen that ently not influenced by fre- and rolling. balance (Figure 4). Values of the angle relative to the hori- quency of pollinator visits, Relative reproductive mass δ13C of fruits from naturally zontal plane, leaf rolling, leaf which showed no significant was highly correlated with watered plants were not sta- reflectance and RRM in- difference between naturally ∆H+, as previously reported in tistically different from those creased significantly with and experimentally watered plants of T. triangulare sub-

MAY 2003, VOL. 28 Nº 5 295 Talinum (Harris posed to nor- and Martin, mal air during 1991). the night pro- The increase duced 10 times caused by wa- more seeds than ter supply in those with CAM

daytime CO2 induced but ex- assimilation posed to CO2- rates resulted in free air during higher total the night (Win- daytime carbon ter and Ziegler, balances but 1992). In the lower RRM. In present study, contrast, in no difference plants of Cakile was found in edentula var. δ13C of fruits lacustris A was and leaves, sug- positively cor- gesting that, al- related with re- though RRM productive out- was highly cor- put (Dudley, related with 1996). By tak- ∆H+, the source ing place dur- of carbon for ing periods of fruit set was water deficit, not different reproduction in from that for Figure 6. Seasonal changes in the number of species such as leaf production. ovules per flower (a), seeds per fruit (b; circles: T. triangulare In T. trian- viable seeds; triangles: aborted seeds) seeds per would depend gulare, dark leaf mass (c) in plants of T. triangulare. Closed on carbon ac- CO2 assimila- symbols: naturally watered plants; open sym- quired by the tion amounts bols: experimentally watered plants. Values for a photosynthesis to only 7% of ≤ ≤ and b are mean ±SE (5 n 10); values for c are of the previous, the net carbon the product of means. An asterisk indicates sig- rather than the gain of plants nificant differences between treatments (p<0.05). current season. in the C3 mo- CAM induc- de (calculated tion by drought from Herrera jected to drought in the may provide an important et al., 1991). greenhouse (Taisma and source of energy for reproduc- Also, values of Herrera, 1998) and with leaf tion. Fruits of M. crystallinum ∆13C in leaves Figure 7. Changes with nocturnal acid accumula- rolling and reflectance. The exhibited higher δ13C values of this species tion in leaf angle relative to the horizontal (a), pro- correlation between RRM and than leaves, indicating that with or with- portion of expanded leaf area (b), proportion of ∆H+ was much higher than carbon used for inflorescence out CAM in- leaf reflectance (c) relative reproductive mass (d) in that reported between the ra- development was primarily duced are not plants of T. triangulare. Values are mean ±SE (n=6 ∆+ ≤ ≤ tio droughted/watered repro- fixed through CAM late in the different (He- for , n=5 for RRM and 20 n 50 for the other ductive biomass and the over- growing season (Winter, rrera, 1999). variables). Closed symbols: naturally watered night malic acid accumulation 1985). Plants of M. crystalli- These results plants; open symbols: experimentally watered in plants of five species of num with CAM induced ex- suggest that in plants. The regression lines and coefficients shown are for the pool of all experimental values. Values this species the of p for the regression lines are 0.0007 for a, 0.01 contribution of TABLE II for b, 0.02 for c and 0.01 for d. dark CO2 up- FREQUENCY OF POLLINATOR VISITS TO FLOWERS OF take to carbon Talinum triangulare GROWING IN THE NATURALLY AND balance of leaves and to re- that experimentally watered THE EXPERIMENTALLY WATERED PLOTS production is very small. plants were more prone to

Probably, a high internal CO2 water stress. Frequency (visits/h) recycling is the feature of Alternatively, the previous Month Naturally Experimentally CAM best related to repro- story of water deficit appar- watered watered ductive output. ently contributed to the accli- Experimentally watered mation of plants of T. trian- December 20 ±3 20 ±3 plants of T. triangulare with a gulare, since naturally wa- February 12 ±2 14 ±2 ∆H+ similar to that of natu- tered plants had higher day-

June 24 ±4 20 ±3 rally watered plants had a sig- time CO2 assimilation rate August 9 ±1 7 ±1 nificantly lower RRM in Oc- (A) and were larger in Octo- October 16 ±2 20 ±3 tober (when watering was al- ber than experimentally wa- ready stopped) than naturally tered plants. This hypothesis Values are mean ±SE (n=10). watered plants, suggesting may be supported by the ob-

296 MAY 2003, VOL. 28 Nº 5 servation that naturally wa- riods of drought reflected a ceived a scholarship from Lovett-Doust J, Lovett-Doust L tered plants apparently allo- decrease in survival, since la- Fundación Gran Mariscal de (Eds.) Plant Reproductive Ecology. Patterns and Strate- cated more biomass to roots beled individuals were alive at Ayacucho. M. Cuberos, M.D. gies. Oxford University Press. than to the shoot. Similarly, the end of the study. In con- Fernández and W. Tezara Oxford, UK. pp. 179-202. in sunflower plants subjected trast, in plants of M. nodiflo- helped with field work. Lee TD, Bazzaz FA (1986) Mater- to an acclimation water deficit rum the relationship between nal regulation of fecundity: pre-treatment A was higher the increase in ∆Η+ and re- REFERENCES non-random ovule abortion in than in watered controls productive output during sum- Cassia fasciculata Michx. 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In the ogy and reflectance in relation mum nodiflorum as influenced ics of reproduction. Based on present work naturally and to water and temperature by CAM induction in the field. stress. In Turner NC, Kramer the markedly seasonal rain re- experimentally watered plants J. Arid Environ. 27: 325-329. gime of the study site, it were visited by pollinators PJ (Eds.) Adaptations of Plants to Water and Temperature Seghieri J, Floret Ch, Pontanier R should be possible to predict with equal frequency, prob- Stress. John Wiley and Sons. (1995) Plant phenology in re- that the number of seeds per ably because of the spatial New York, USA. pp. 295-308 lation to water availability: leaf mass after the experimen- proximity between plots. The Farris MA, Lechowicz MJ (1990) herbaceous and woody species tal year is similar to that decrease in abortion observed Functional interactions among in the savannas of northern traits that determine reproduc- Cameroon. J. Tropical Ecol. found when this study began, in naturally watered plants 11: 237-254. at the peak of the dry season. may be due to the leaf and tive success in a native annual plant. Ecology 71: 548-557. In February, when IWUE whole-plant tolerance respons- Taisma MA, Herrera A (1998) A Griffiths H (1988) Crassulacean relationship between fecundity, was highest in naturally wa- es to drought. acid metabolism: a reappraisal survival and the operation of tered plants, the number of The results suggest that the of physiological plasticity in CAM in T. triangulare. Can. J. flowers was higher and ovule changes brought about by form and function. Adv. Bo- Botany 7: 1-8. abortion ratio lower. An in- drought in the leaf properties tanical Res. 15: 43-92. Winter K (1985) Crassulacean acid crease in IWUE, possibly due studied increased fecundity Harris FS, Martin CE (1991) Plas- metabolism. In Barber J, Baker to the joint effect of the op- without changes in survival of ticity in the degree of CAM- NR (Eds.) Photosynthetic cycling and its relationship to Mechanisms and the Environ- eration of CAM, leaf rolling plants of T. triangulare under drought stress in five species ment. Elsevier. Amsterdam, and increased reflectance and field conditions. Drought of Talinum (Portulacaceae). Netherlands. pp. 329-387. angle, may help explain the serves as a cue to these Oecologia 86: 575-584. Winter K, Smith JAC (1996) Cras- observed increase in these re- changes, the causative agent Herrera A (1999) Effects of photo- sulacean acid metabolism: cur- productive characteristics. Wa- linking leaf responses to re- period and drought on the in- rent status and perspectives. In ter use efficiency contributed production remaining to be duction of CAM and the re- Winter K, Smith JAC (Eds.) production of plants of Ta- Crassulacean acid metabolism. in an important fraction to the investigated. linum triangulare. Can. J. Bo- Biochemistry, Ecophysiology reproductive success of indi- tany 77: 1-6. and Evolution. Springer-Verlag. viduals of Xanthium struma- ACKNOWLEDGEMENTS Herrera A, Delgado J, Paraguatey I Berlin, Germany. pp. 389-436. rium grown in an experimen- (1991) Occurrence of inducible Winter K, Ziegler H (1992) Induc- tal garden (Farris and Lecho- This research was financed Crassulacean acid metabolism tion of crassulacean acid me- wicz, 1990). by grants CDCH (Venezuela) in leaves of Talinum triangula- tabolism in Mesembryanthe- re (Portulacaceae). J. Exp. Bo- mum crystallinum increases re- In this study no evidence 03.10.2252.90 and 03.10.2252.92, tany 42: 493-499. productive success under con- was found that the increase in and CONICIT (Venezuela) Lee TD (1988) Patterns of fruit ditions of drought and salinity reproduction associated to pe- S1-1754. M.A. Taisma re- and seed production. In stress. Oecologia 92: 475-479.

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