Flower production in relation to individual plant age and leaf production among different patches of Corydalis intermedia

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1 Plant Ecology 174: 71 78, Kluwer Academic Publishers. Printed in the Netherlands. 71 Flower production in relation to individual plant age and leaf production among different patches of Corydalis intermedia Bodil Kirstine Ehlers 1,2, * and Jens Mogens Olesen 1 1 Department of Ecology and Genetics, University of Aarhus, Ny Munkegade build. 540, DK-8000 Aarhus C, Denmark; 2 current adress: Centre d Ecologie Fonctionelle et Evolutive, CNRS, 1919 Route de Mende, Montpellier cedex 5, France; *Author for correspondence (fax: ; ehlers@cefe.cnrs-mop.fr, or bodil.ehlers@biology.au.dk) Received 15 October 2002; accepted in revised form 14 August 2003 Key words: Life-history traits, Metapopulations, Perennial plants, Resource allocation, Trade-off Abstract The life history of an organism can be viewed as the combination of allocations made to maintenance, growth, and reproduction. Allocation to these functions are constrained by trade-offs as increased investment to one function may happen at the expense of another. Moreover, because fecundity and survival probabilities are affected by both the state of an individual and by its surrounding environment, optimal allocation to reproduction and growth may vary with both individual size/age and with the habitat in which it lives. In this study we aim to describe how flower production varies with individual plant age and leaf production among different patches of the perennial herb Corydalis intermedia. We take advantage of the construction of the underground storage organ to estimate the age of individual plants which allows us tacitly to relate flower and leaf production to individual age and successional status of the patch. We sampled all individuals present in nine patches from the same forest and estimated their age, flower production and total leaf area. The age distributions showed that each patch was most often dominated by a few and consecutive age classes. In patches where individuals had the oldest mean age, very few or no juvenile age classes were found suggesting that recruitment had ceased. Based on the age distribution of the patches we propose that the dynamics may best be described as metapopulational with colonization of newly formed open forest gaps and a successionally determined extinction as the patch gradually becomes too shaded for recruitment. Both mean flower production, leaf area and age varied significantly among patches. Flower production increased with both increasing age and leaf area. We found no indication of a trade off between reproduction and vegetative growth since flower production showed a positive relation with leaf production even after removing the effect of age. Number of flowers produced by plants of the same age but growing in different patches did not vary indicating that the difference among patches mainly was due to a difference in age distribution. No individuals produced flowers before they reached an estimated age of three years. Production of flowers followed a power function with increasing age. Our data suggests that C. intermedia plants change their allocation strategy with age investing a relatively large amount of energy in flower production immediately after the immature growth phase when recruitment in their patch may be high. Production of flowers then reaches a plateau around the age of 11 years after which number of flowers produced stays constant. Introduction In natural forests the processes of tree senescence, fall and regrowth create a mosaic of glades of different successional stages. Such environmental heterogeneity may create a patchy distribution of habitats for those plants and animals confined to one stage such as open gaps. Due to this forest succession, the dy-

2 72 namics of plant species living in light gaps can be viewed as metapopulational where local patches are interconnected by seed dispersal during episodes of colonization, and where the whole system of patches exists in a balance between extinction and recolonization Hanski 1991; Hanski 1999; Husband and Barret Alternatively, the dynamics of light-gap species may be that of a single extinction-resistant spatially structured population Harrison Depending on which of these population dynamics occurs, different selection pressures may act on dispersal, growth, and reproductive traits. For example, Valverde and Silvertown 1997a, b predicted that high rates of seed dispersal in the forest understorey herb Primula vulgaris would cause a lower overall population growth when a single spatially structured extinction-resistant population was presumed mainly because seeds were dispersed to closing canopy patches of poor seedling establishment, whereas high rates of seed dispersal caused overall population growth rate to increase when local patches were expected to exhibit metapopulation dynamics because of the increased chance of colonizing a new patch. The temperate forest understorey herb Corydalis intermedia Fumariaceae exhibits a patchy distribution as it is confined to the forest floor in light gaps. It has no clonal growth and reproduces only by seeds, which have an elaisome adapted to ant-dispersal myrmecochory Olesen and Ehlers Colonization of open gaps take place via seeds transported by ants. The seed-dispersing ants also respond to the forest dynamics establishing colonies in open sunny gaps and leaving as these become too shaded Smallwood A time-lag between opening of a new canopy gap and colonization by the plant is thus expected since ants must colonize first and secondly import seeds to the patch e.g., Gibson 1993; Olesen InC. cava, which resembles C. intermedia in both habitat and mode of seed dispersal, local populations go extinct a number of years after gap closure Olesen It is likely that the same successionally determined extinction also occurs in patches of C. intermedia. Given a limited amount of resources, an individual plant allocates a fraction of its resources to reproduction and the remaining to survival and growth. Division of resources can be viewed as a trade-off between reproduction and survival e.g., Stearns Since optimal allocation to reproduction and growth depends on the probability of survival and fecundity, which vary with demographic and environmental factors, different age-specific strategies may be selected for e.g., Schaffer 1974; Kozlowski and Wiegert 1986; Huston and Smith 1987; Kozlowski 1991; but see also Ricklefs Due to the morphological construction of the underground storage organ an estimate of the age of individual C. intermedia plants can be obtained by counting the number of old sheaths on the outside of the tuber. A positive relation between the age and the size of the tuber exists, which makes age determination of C. intermedia possible by estimating the volume of the tuber of individual plants for more details see Olesen and Ehlers This provides an excellent opportunity to study the relation between age and reproduction and growth. In this study, we assume that age of the oldest plants growing in a patch also reflects minimum age of the patch cohorts. Allocation to reproduction and survival is expected to vary with patch age because of changing environmental conditions. Within a patch, variation in allocation to reproduction and growth may take place among individual plants of different age if these plants show age-specific allocation strategies regardless of the stage of their patch. In addition, intra-cohort variation in allocation may reflect genetic variation. Thus, variation in growth and reproduction may be found at several levels and this variation may be selected on differently depending on the population dynamics. In the present study we address the following questions: 1 How does flower production vary with leaf production and age of individual plants? 2 Does allocation to flower and leaf production vary among local patches? and 3 How may the population dynamics of Corydalis intermedia best be described? Materials and methods Study species Corydalis intermedia Fumariaceae is an iteroparous geophyte with a non-rameting growth. Flowering begins in early spring March-April and lasts 3 4 weeks. It reproduces mainly through self-fertilization, and in Denmark all flowers usually produce between 7-10 seeds per fruit pers. obs. by J. M. Olesen through 8 years of monitoring. Eastern Denmark and Southern Sweden constitute the northern range of the species distribution Fitter Although seeds have elaisomes experimentally demonstrated to at-

3 73 tract ants unpubl. data flowering and fruiting in Denmark may begin before ants become active, and ant-mediated seed dispersal may therefore be limited in some years. Seeds, which are not collected by ants on the plants drop passively around the mother plant. The elaisome turns black within a day and consequently becomes unattractive to ants pers. obs.. Study site and sampling All plants used in the present study were sampled in Suserup Wood, an old natural forest in the central part of Zealand Eastern DK. In this forest, distribution of C. intermedia plants is very patchy, with up to 200 individuals per m 2. We defined a local patch as an assemblage of plants having more than 3 m to the nearest neighbor assemblage. Within an area of ~ 125 m 2, nine patches of C. intermedia were identified i.e., patches A-I consisting of 15 to 155 individuals. During flowering, all plants in each patch were collected and age, flower production and leaf area were estimated in the laboratory. Estimation of age, reproduction and vegetative growth To estimate age of individual plants we counted the sheaths on the underground tuber of 100 randomly chosen individuals and estimated the volume in cm 3 of their tuber. This gave the relationship: ln Age ln volume, R , P To examine if local environmental conditions may affect the relation ship between tuber volume and age among patches we later sampled 50 individuals from 2 different patches not used in this study within the same forest. One patch was located at the forest edge in a light gap, while the other was situated meter inside the forest under a more closed canopy. Each individual plant had its tuber volume measured and the sheaths on the underground tuber organ counted to get a precise estimate of age. Analysis was performed with age as dependent variable and patch and tuber volume as independent variables. We found as above a highly significant relation ship between age and tuber volume F 1, , P whereas patch and in particular the interaction term between tuber volume and patch was not significant F 1, , P 0.5. This suggest that the relationship between age and tuber volume did not vary among patches within the same forest. Since all the patches used in this study were sampled on a relatively small geographic scale 125 m 2 we assume that local environmental conditions do not vary to an extend which significantly violates the relation between tuber volume and age used in this study. Age of all individuals in the study was hereafter determined by estimating the volume of their underground tuber and using the above relationship see e.g., Olesen and Ehlers 2001 for more details. For all individuals in each of the nine study patches number of flowers per plant was counted, and total leaf area measured. Total leaf area was measured from a photocopy of all leaves of each plant, this copy was scanned into a computer and area estimated by use of the software NIH Image. Growth of leave ceases in April where sampling took place. Total leaf area is used as an estimate of vegetative growth. Since all flowers of C. intermedia produce seeds, number of flowers produced was used as an estimate of seed production. Data analysis To reduce variance in age, flower production, and total leaf area data were ln x 1 transformed. Analysis of variance were performed to examine differences among patches with respect to these variables. Due to the low number of patches examined 9, correlations between mean age, mean flower production and mean leaf area among patches were analyzed by a non-parametric Spearman correlation. Effects of patch, plant age and leaf area on number of flowers were analyzed by an ANCOVA. One way ANOVA was used to test if plants of the same age differed in flower production or in leaf area among patches. All statistical analyses were performed using the software JMP SAS Institute Results Distribution of individual plants age in each of the nine study patches are shown in Figure 1. Most often each patch was dominated by a few consecutive age classes. Among the oldest patches i.e., patches F-I very few young individuals were present suggesting that recruitment had ceased. Flower production and leaf area per plant were highest in the oldest patches Figure 1, Table 1. Significant among-patch differences were found in flower production, leaf area, and age F 8, , P ; F 8, , P ; and F 8,736

4 74 Figure 1. Age distribution of all plants in nine patches of Corydalis intermedia sampled in Suserup wood, Denmark.

5 Table 1. Mean age, flower production and leaf area of Corydalis intermedia plants from nine patches A-I in Suserup wood, Denmark. Patch No. individuals in patch Mean age in years SE Mean no. flowers produced SE Mean total leaf area in cm 2 SE A B C D E F G H I Table 2. Effect of patch, age and leaf area on flower number in Corydalis intermedia analyzed by ANCOVA. Source df Sum of squares F P Patch Age Leaf area Patch*Age Patch*Leaf area Age*Leaf area , P respectively. Among patches both mean flower production and mean leaf area were positively correlated with mean age Spearman r s 0.68, P 0.04 ; r s 0.94, P Mean flower production and mean total leaf area were also positively correlated Spearman r s 0.77, P An ANCOVA was used to analyze the effects of patch, age, and leaf area on flower production Table 2. Flower production varied among patches. A significant patch*leaf area interaction suggests that the relationship between flower production and leaf area varied among patches. Furthermore, a significant age*leaf area interaction was detected for flower production. These interactions are analyzed in further details below. One way ANOVA examining the effect of patch on flower production among even aged plants age 14 to 16 was pooled to increase sample size, sequential bonferoni corrections applied showed that in all age classes except one flower production among plants of similar age did not vary among patches. Only in one age class did we find a significant difference in flower production among patches. Four years old individuals were present in seven of the nine patches sampled and significant difference in flower number among patches were found F 6, , P , flower production among those were lowest in patch A, and B, and highest in D and E. Similar analysis was performed to examine if even aged plants varied their leaf area with patch. Only in one age class plants of age 1 did leaf area among plants of the same age vary with patch F 4, , P One year old individuals were present in five patches and their leaf area were significantly higher in patch D compared to the rest A, C, F and G. In all other age classes i.e., age 2-16 leaf area among plants of the same age did not vary among patches. Thus, even aged plants produced in general the same number of flowers and leaf area irrespective of which patch they were growing in. Differences in both flower production and leaf area among patches are therefore most likely to reflect differences in patch age distributions. Estimation of regression coefficients herafter denoted r of flower production on age and on leaf area for all plants combined showed that flower production increased significantly with both age r 1.13, R , N 460, P and leaf area r 0.53, R , N 557, P and suggested that flower production increased more steeply with age than with leaf area regression coefficient highest for the former. Since both age, flower production, and leaf area were positively correlated a regression of flower production on leaf area was performed after removing the effect of age i.e., regressing flower production on the residuals of leaf area on age. Even after removing effect of age, flower production still showed a significant positive relation with leaf area r 0.11, R , N 446, P Relationships between mean number of flowers per plant, and proportion of flowering plants at a given age are shown in Figure 2, Figure 3. No flowers are produced by individual plants younger than 3 years. After this age number of flowers increases with increasing age until around the age of 11 years after

6 76 did not change their flower production with age, but reproducing individuals below that age had a flower production which followed the power function: Number of flowers 0.01 age Discussion Population dynamics of C. intermedia Figure 2. Mean number of flowers produced by Corydalis intermedia plants in each of the age classes: 3-16 age class were pooled to increase sample size. Figure 3. Proportion of flowering plants at each age class in Corydalis intermedia. which flower production seems to have reached a plateau. To examine if C. intermedia plants changed their allocation with age, flower number of plants older than 2 years i.e., potentially reproducing plants was regressed against age and both a linear and a log to log fit was made. The linear fit explained less of the variation than the log to log fit who gave: log no. flowers log age, R , N 336, P Number of flowers produced by a plant could be described as a power function: Number of flowers age However, Figure 2 shows that flower production does not seem to change with age in individuals older than 11 years old. Therefore, a log to log fit was made for individuals from 3-11 years: log no. flowers log age, R , N 309, P , and for individuals older than 11 years: log no. flowers log age, R , N 27, P Plants older than 11 years Local populations of Corydalis intermedia were dominated by plants in a few consecutive age classes. In this study, we assume that maximum age of individual plants in a local population reflected the age of the patch, and thus its successional stage. That local populations go extinct, due to closure of the canopy, which decreases the quality of the patch, is suggested by the low number, or even absence, of juvenile age classes in patches with highest mean age. This may be due to either a lack of seed influx to such sites, within site seed production, or to poor conditions for establishment. As seeds collected by ants are transported to nests Culver and Beattie 1978; Ohkawara et al. 1997, dispersal between individual patches is probably very limited. However, depending on the feeding behavior of the ants, newly established plant populations may be founded by seeds from many different local populations in the vicinity if the ants collect seeds over extensive areas in the forest. Foraging distance of ants are generally low mean ~1m but with a range of m depending on the ant species Gomez and Espadaler Once established, a plant population may begin to recruit an increasing fraction of its juveniles from that part of its own seed production not harvested by ants. Our data suggest that populations then reach an age where establishment of new individuals ceases. Old populations most likely go extinct because the habitat becomes progressively less suited to germination and seedling establishment. The population dynamics of C. intermedia in Suserup Wood thus appear to function as a metapopulation, where local patches are connected through ant-mediated seed dispersal during colonization episodes. Flower and leaf production in relation to patch and individual plant age Positive relations between age of individual plants and both reproduction and vegetative growth were found. Plants of the same age showed no variation in

7 77 flower production except in age class four, and leaf area except in age class one among patches. This suggests that the difference in flower production and leaf area among patches is mainly due to a difference in the age distribution among patches rather than to a difference among the patches per se. Though we would expect that allocation to reproduction and growth may vary among patches of different successional status, our result indicate that allocation to flower and leaf production is mainly a function of individual plant age regardless the patch in which it grows. However, our sample of study patches only contained one possibly very old patch patch H, mean plant age 9.7 years making it more difficult to detect potential among patch differences in allocation strategies caused by a variation in successional status. Furthermore, it is possible that the geographic scale we studied ~ 125 m 2 is too small to detect any variation in allocation to flower and leaf production which may be caused by abiotic difference in the local environmental conditions e.g., soil composition and nutrients, ph among patches. Age of a plant is closely related to the size of its underground storage organ which conditions energy available for reproduction and growth. Given the expected trade-off between reproduction and growth e.g., Harper 1977; Stearns 1992, two allocation strategies may be expected in an individual plant within a single growing season after Iwasa and Cohen 1989 : First, a plant may divide stored energy between production of leaves and flowers, and store energy obtained from photosynthesis in the tuber for the following season. In this case, a negative relation between leaf area and flower production is expected after the effect of age is removed, as the production of one is happening at the expense of the other. Second, a plant may use at least part of the energy obtained from photosynthesis in the present year for the production of flowers in the same year. In this case a positive relation between reproduction and leaf area may be found. In the present study, no indication of a trade-off between reproduction and growth could be detected since a positive relation between flower number and leaf area was found both before and after removing the effect of age. This suggests that reproducing C. intermedia plants likely use some energy achieved from photosynthesis to the production of flowers in the same season. However, trade-offs between life history traits can be difficult to detect empirically because a variation in the resource pool and the quality of individuals may mask underlying negative correlations e.g., Stearns 1989; Partridge and Sibly 1991 Isawa and Cohen 1989 modeled the optimal growth schedule of perennial plants over a season. In each season plants decide how much energy is being devoted to reproduction and how much is saved for subsequent growth. These decisions depend on energy loss during storage, survival probability, and productivity in future seasons. They found that perennial plants should spent all energy on storage accumulation until it reaches a certain optimal storage size. At this point, excess energy obtained from photosynthesis would most favorably be invested in reproductive tissue. Corydalis intermedia plants did not reproduce before they were at least three years old, indicating that this is the minimum age at which a storage organ permits resource allocation to reproduction. Optimal size of storage organ might vary among individuals, as age of first reproductive event varied. The log to log fit of flower production on age had a slope slightly higher than one. This indicates that individual plants actually change their allocation strategy, investing relatively more in reproduction with increasing age. This change in pattern of resource allocation occurs in the period from plants at the age of three years until the age eleven, during which time the number of flowers produced shows the largest increase. Plants older than 11 years showed little variation in the number of flowers and no significant increase in flower production with increasing age, although the power to detect such a plateau is limited relative to the rest of the age classes due to low sample size N 27. The increased investment in reproduction with increased age immediately after the immature growth phase may be favored by the dynamics of the local patch. Investing a large amount in reproduction as soon as possible would increase the local population growth rate as long as the quality of the patch is favorable to recruitment. Since seed dispersal among patches probably is limited, individuals which produce many seeds at an early age would have a higher proportion of their offspring present in the population before succession of their patch reduces the conditions for seedling establishment. That flower production no longer changes with age in plants older than 11 years may be due to deteriorating local conditions, senescence and/or a specific norm of reaction in this species between reproductive effort and age. Given that size of the underground tu-

8 78 ber keeps increasing with age and the lack of increased reproductive output in plants older that 11 years may indicate a decrease in reproductive effort with age. Further studies are needed to examine if this species show a specific norm of reaction of reproduction as a function of individual age and how this may relate to local environmental conditions and a patch dynamic of colonization and successional determined extinction of local patches. Acknowledgments This study was financed by the Danish Natural Science Research Council. The authors are grateful to Anette Rasmussen for field assistance and to T. Bataillon, and J. D. Thompson for comments on the manuscripts. References Culver D.C. and Beattie A.J Myrmecochory in Viola: Dynamics of seed-ant interactions in some West Virginia species. Journal of Ecology 66: Fitter A An Atlas of the Wild Flowers of Britain and Northern Europe. Collins, London, UK. Gibson W Selective advantages to hemi-parasitic annuals, genus Melampyrum, of a seed-dispersal mutualism involving ants: I. Favorable nest sites. Oikos 67: Gomez C. and Espadaler X Mymechorous dispersal distances: a world survey. Journal of Biogeography 25 3 : Hanski I.A Single species metapopulation dynamics: concepts, models and observations. Biological Journal of the Linnean Society 42: Hanski I.A Metapopulation Ecology. Oxford University Press, Oxford, UK. Harrison S Local extinction in a metapopulation context: an empirical evaluation. Biological Journal of the Linnean Society 42: Harper J.L Population Biology of Plants. Academic Press, London, UK. Husband B.C. and Barrett S.C.H A metapopulation perspective in plant population biology. Journal of Ecology 84: Huston M.A. and Smith T Plant succession: Life history and competition. American Naturalist 130: Iwasa Y. and Cohen D Optimal growth schedule of a perennial plant. American Naturalist 133: Kozlowski J Optimal energy allocation models an alternative to the concepts of reproductive effort and cost of reproduction. Acta Oecologia 12: Kozlowski J. and Wiegert R.G Optimal allocation of energy to growth and reproduction. Theoretical Population Biology 29: Ohkawara K., Ohara M. and Higashi S The evolution of ant-dispersal in a spring-ephemeral Corydalis ambigua Papaveraceae : timing of seed-fall and effects of ants on ground beetles. Ecograpy 20: Olesen J.M A fatal growth pattern and ways of postponing death: corm dynamics in the perennial herb Corydalis cava. Botanical Journal of the Linnean Society 115: Olesen J.M. and Ehlers B.K Age determination of individuals of Corydalis species and other perennial herbs. Nordic Journal of Botany 21: Partridge L. and Sibly R Constraints in the evolution of life histories. Phil. Trans. R. Soc. London. 332: Ricklefs R.E Fitness, reproductive value, age structure, and optimization of life-history patterns. American Naturalist 117: SAS Institute Inc JMP Users Guide, 3rd edition, Cary, North Carolina, USA. Schaffer W.W Selection for optimal life-histories: the effects of age structure. Ecology 55: Smallwood J The effect of shade and competition on emigration rate in the ant Aphaenogaster rudis. Ecology 63: Stearns S.C Trade-offs in life-history evolution. Functional Ecology 3: Stearns S.C The evolution of life histories. Oxford University Press, Oxford, UK. Valverde T. and Silvertown J. 1997a. An integrated model of demography, patch dynamic and seed dispersal in woodland herb Primula vulgaris. Oikos 80: Valverde T. and Silvertown J. 1997b. A metapopulation model for Primula vulgaris, a temperate forest understorey herb. Journal of Ecology 85: