Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought 1

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1 E CoSCIENCE 11 (3): (2004) Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought 1 Romà OGAYA 2 & Josep PEÑUELAS, Unitat d Ecofisiologia CSIC-CEAB-CREAF, CREAF (Center for Ecological Research and Forestry Applications), Edifici C, Universitat Autònoma de Barcelona, Bellaterra Barcelona, Spain, r.ogaya@creaf.uab.es Abstract: A holm oak forest located in the Prades Mountains (northeast of Spain) was subjected to an experimental drought to determine its phenological responses. Soil water availability was reduced by 15% by plastic strips and funnels that partially excluded rain throughfall and by ditch exclusion of water runoff. We monitored eight phenological events: leaf shedding, leaf flushing, flower bud formation, flowering, flower senescence, fruit growth, fruit maturation, and fruit abscission in the three dominant species, Quercus ilex, Phillyrea latifolia, and Arbutus unedo once a week from winter 1999 to winter We also collected litterfall in circular baskets randomly distributed on the ground every 15 d from winter 1999 to winter 2001 and every 2 months from winter 2001 to winter Arbutus unedo showed a higher proportion of individuals flowering and fruiting than Q. ilex and P. latifolia. Arbutus unedo was also the most sensitive species to water availability since drought treatment delayed its phenophases, whereas this treatment did not significantly affect the timing of the other two species phenophases. The flower and fruit production was also greater in A. unedo than in the two other species, but inter-annual variability was high, and no significant drought effect was found in any of the three species. Stem litterfall was greater in drought plots than in control plots during the overall studied period. In a drier environment, as predicted for Mediterranean areas in the near future by global circulation models, drought-resistant species such as P. latifolia could present greater ability to produce reproductive structures than less resistant species such as Q. ilex or A. unedo. This different response among species could produce changes in seedling recruitment and resprouting ability and, in the longer term, in species distribution. Keywords: Arbutus unedo, climate change, drought, flowering, fruiting, litterfall, Mediterranean trees, mushroom, phenology, Phillyrea latifolia, Quercus ilex. Résumé : Nous avons soumis une forêt de chênes verts localisée dans les montagnes Prades, dans le nord-est de l Espagne, à une sécheresse expérimentale afin d en connaître les réponses phénologiques. La disponibilité de l eau du sol a été réduite de 15 % à l aide de bandes de plastique et de tuyaux empêchant partiellement la pluie de pénétrer dans le sol ainsi que par des canaux de drainage évacuant l eau. Nous avons suivi huit événements phénologiques (perte des feuilles, émergence des feuilles, formation des boutons floraux, floraison, sénescence des fleurs, croissance des fruits, maturation des fruits et chute des fruits) chez les trois espèces dominantes, soit Quercus ilex, Phillyrea latifolia et Arbutus unedo. Le suivi a été effectué une fois par semaine à partir de l hiver 1999 jusqu à l hiver Nous avons également recueilli la litière des feuilles tombantes dans des paniers circulaires répartis aléatoirement sur le sol à tous les 15 jours de l hiver 1999 à l hiver 2001 et à tous les deux mois à partir de l hiver 2001 jusqu à l hiver Une plus grande proportion d individus de A. unedo a produit des fleurs et des fruits que Q. ilex et P. latifolia. C est également A. unedo qui s est montré le plus sensible à la disponibilité de l eau. En effet, le traitement de sécheresse a retardé sa phénologie alors qu il n a eu aucun effet significatif sur celle des deux autres espèces. La production de fleurs et de fruits était également supérieure chez A. unedo que chez les autres espèces. La variabilité interannuelle était toutefois élevée et aucun effet significatif de la sécheresse n a été trouvé chez les trois espèces. Pendant toute la période de l étude, la litière des tiges tombantes était plus abondante dans les parcelles soumises à la sécheresse que dans les parcelles témoins. Selon les prévisions des modèles de circulation globale pour la région méditerranéenne, au cours des prochaines années, les espèces résistantes à la sécheresse telles que P. latifolia auraient plus de facilité à produire des structures reproductrices que les espèces moins résistantes comme Q. ilex ou A. unedo. Ces réponses différentielles entre les espèces peuvent conduire à des changements dans le recrutement des plantules et, à long terme, dans la répartition des espèces. Mots-clés : arbres de la région méditerranéenne, Arbutus unedo, champignon, changement climatique, floraison, litière, mise à fruit, phénologie, Phillyrea latifolia, Quercus ilex, sécheresse. Nomenclature: Bolòs & Vigo, Rec ; acc Associate Editor: Maria Luisa Martínez Vázquez. 2 Author for correspondence.

2 OGAYA & PEÑUELAS: PHENOLOGY UNDER DROUGHT Introduction The Mediterranean climate is mainly characterized by a pronounced seasonality. Rainfall is usually concentrated in spring and autumn. The temperature is moderately low in winter and high in summer (Mitrakos, 1980), when a drought period takes place due to the low precipitation and the high temperatures (Di Castri & Mooney, 1973; Terradas & Savé, 1992; Pereira & Chaves, 1995). Avoiding winter cold and summer drought, many Mediterranean plants flower in spring, at the same time as they experience intense vegetative growth. However, some species flower in autumn (Orshan, 1989; de Lillis & Fontanella, 1992; Castro-Díez & Montserrat-Martí, 1998; Picó & Retana, 2001). The development of fruits starts shortly after flowering, but the duration of the fruiting period is highly variable and depends on the species. Evergreen Mediterranean species usually experience a period of intense leaf shedding coinciding with the formation of new leaves (Orshan, 1989; de Lillis & Fontanella, 1992; Castro-Díez & Montserrat-Martí, 1998). Holm oak (Quercus ilex) is a drought-adapted tree widely distributed in the Mediterranean basin. Phillyrea latifolia is a tall shrub common in holm oak forests that is more drought tolerant than Quercus ilex (Lloret & Siscart, 1995; Peñuelas et al., 1998; 2000; Ogaya & Peñuelas, 2003). Arbutus unedo is another tall shrub typical of holm oak forests; in at least some Mediterranean areas, A. unedo shows higher drought sensitivity than P. latifolia (Ogaya et al., 2003). Quercus ilex and P. latifolia flower during spring, which coincides with the peak of vegetative growth (Q. ilex usually experiences a second vegetative growth peak in autumn). In contrast, A. unedo flowers in autumn and usually only shows a peak in vegetative growth during the spring (de Lillis & Fontanella, 1992; Castro-Díez & Montserrat-Martí, 1998). In the Mediterranean region, predicted increases in temperatures and consequent increases of evapotranspiration rates (IPCC, 2001), which are predicted to be greater than those that occurred during the 20 th century, are expected to lead to a reduction in water availability in the near future (Piñol, Terradas & Lloret, 1998; Peñuelas, Filella & Comas, 2002). Climatic environmental changes could be followed by changes in the timing of some phenological events, probably with important ecological consequences, for example, through interactions with other species (Fitter et al., 1995; Peñuelas & Filella, 2001). We studied the effects of an experimental drought on the phenology of these co-occurring Mediterranean woody species to gain further knowledge of the effects of drought on the biology of these species and on their nearfuture performance and potential distribution. Methods STUDY SITE The study was conducted in a holm oak forest in the Prades Mountains in southern Catalonia, Spain (41 13 N, 0 55 E), on a south-facing slope (25%) at 930 m a.s.l. The soil is a stony xerochrept on a bedrock of metamorphic sandstone, and its depth ranges between 35 and 90 cm. 264 The average annual temperature is 12 C, and the annual rainfall is 658 mm. Summer drought is pronounced from approximately mid-june to mid-september. This holm oak forest is very dense (16,616 trees ha -1 ), and it is dominated by Q. ilex (8,633 trees ha -1 ), P. latifolia (3,600 trees ha -1 ), and A. unedo (2,200 trees ha -1 ) with other abundant evergreen species well adapted to dry conditions (Erica arborea, Juniperus oxycedrus, and Cistus albidus) and occasional individuals of deciduous species (Sorbus torminalis and Acer monspessulanum). EXPERIMENTAL DESIGN Eight 15-m 10-m plots were delimited at the same altitude along the slope. Four plots received the drought treatment; the other four were considered control plots. The drought treatment consisted of partial rain exclusion by suspending PVC strips and funnels at a height of m above the soil. Strips and funnels covered approximately 30% of the total plot surface. Moreover, a 0.8-m-deep ditch was excavated along the entire top edge of the upper part of the treatment plots to intercept runoff water supply. Water intercepted by strips, funnels, and ditches was conducted outside the plots, below the bottom edge of the plots. An automatic meteorological station installed between the plots monitored temperature, photosynthetically active radiation, air humidity, and precipitation each half-hour. Soil moisture was measured every 2 weeks throughout the experiment by time domain reflectometry (Tektronix 1502C, Beaverton, Oregon, USA; Zegelin, White & Jenkins, 1989; Gray & Spies, 1995). Three stainless steel cylindrical rods, 25 cm long, were permanently driven into the upper 25 cm of the soil at four randomly selected places in each plot. The time domain reflectometer was connected to the ends of the rods at each measurement. PHENOLOGICAL MEASUREMENTS The monitoring of the timing of phenological events was based on Orshan s pheno-morphological method (Orshan, 1989). We monitored the presence or absence of eight phenological events once a week from winter 1999 to winter 2001: leaf shedding, leaf flushing (period of growth of leaves until full expansion), flower bud formation, flowering (flowers in anthesis), flower senescence (flowers brown or abscissing), fruit growth (growth of fruits until full expansion), fruit maturation (fruit maturation after full expansion), and fruit abscission in the three dominant species (A. unedo, P. latifolia, and Q. ilex). We visually determined the intensity of each phenological event in each plot as the percentage of plants showing the phenological event. We established seven categories: 0%, 5%, 20%, 40%, 60%, 80%, and 95%. Litterfall was collected in 20 circular baskets (27 cm in diameter with a 1.5-mm mesh) randomly distributed on the ground of each one of the eight plots. The fallen litter was collected every 15 d from winter 1999 to winter 2001 and every 2 months from winter 2001 to winter Litterfall was weighed after drying in a oven at 70 C to constant mass. We estimated the proportion of leaf, flower, and fruit litter relative to total remaining leaf biomass and to total

3 ÉCOSCIENCE, VOL. 11 (3), 2004 aboveground tree biomass. Leaf biomass and aboveground tree biomass were estimated by allometric relationships with the stem diameter at 50 cm height measured in Q. ilex and P. latifolia trees growing in the area of study (outside the plots). To estimate the biomass of A. unedo we used the allometric relationship calculated for the same area by Lledó (1990; Table I). The stem diameter of all Q. ilex, P. latifolia, and A. unedo trees growing in the plots was measured each winter. STATISTICAL ANALYSES Repeated-measures ANOVAs were conducted on the shoot, flower, fruit, and leaf litters expressed as percentages of the total aboveground biomass or leaf biomass remaining in the canopy (calculated from allometric relationships) with species, year, and treatment application as independent factors. Data on percentage of litter was arcsine square-root transformed to reach the normality assumptions of the ANOVA. We used the starting time of phenological events as a survival time equivalent to compute survival curves with Kaplan-Meyer non-parametric method. Additionally, for each date ANOVAs were conducted on the percentage of plants presenting each phenological event after arcsine square-root transformation with species and treatment application as independent factors. All analyses were performed with the Statview software package (Abacus Concepts, Cary, North Carolina, USA) and the Statistica software package (StatSoft, Tulsa, Oklahoma, USA). Differences in soil moisture between control and drought plots were significant on most of the sampling dates throughout the 2 y (Figure 1). Control plots had on average 16% higher soil moisture than drought plots in 2000 and 13% in PHENOLOGICAL MEASUREMENTS In the area studied, Q. ilex leaf flushing took place in spring and in autumn 1999, but the autumn new leaves were damaged by freezing temperatures. This species Results METEOROLOGICAL DATA AND SOIL WATER STATUS Mean annual temperature was slightly higher in the second year of experiment set-up (2000: C) than in the first (1999: C). Rainfall was also higher in 2000 (727 mm) than in 1999 (610 mm). In 2000, rainfall was concentrated in late spring and late autumn, whereas in 1999 it was concentrated in early spring and early autumn (Figure 1). Soil moisture showed great fluctuations throughout each year but was 3.3% higher in 2000 than in 1999 (Figure 1), in agreement with rainfall data. Minimum soil moisture values (about 15% volume/volume) were reached in summer, as a consequence of summer drought, and maximum values (about 35% volume/volume) in spring and autumn, coinciding with heavy rainfall periods. TABLE I. Allometric relationships between stem diameter at 50 cm (D50) and leaf biomass (LB) and aboveground biomass (AB) in Quercus ilex, Phillyrea latifolia, and Arbutus unedo (A. unedo relationships taken from Lledó, 1990). Species Allometric relationship r n P Q. ilex ln LB = ln D < P. latifolia ln LB = ln D < A. unedo ln LB = ln D < Q. ilex ln AB = ln D < P. latifolia ln AB = ln D < A. unedo ln AB = ln D < FIGURE 1. Seasonal course of daily mean temperature, soil moisture (0.25 m depth), and precipitation at the study site. Mean soil moisture for each treatment (± SE; n = 4) in panel b, with differences between treatments as follows: *: P < 0.05; **: P < The arrow indicates the start of the drought treatment. 265

4 OGAYA & PEÑUELAS: PHENOLOGY UNDER DROUGHT flowered just after leaf flushing, on the new shoots. Phillyrea latifolia flowered in early spring and flushed its new leaves in late spring. Both species developed their fruits during summer, and fruit maturation took place in the following autumn. Finally, A. unedo developed new leaves in spring and flowered on new shoots during the next autumn. Fruit growth started just after flowering (in late autumn) and lasted 1 y. Fruit maturation took place the autumn of the following year. Quercus ilex did not show important inter-annual variations in timing of phenological events except for fruit production in 1999, when it was negligible. In the other two species, leaf flushing (and also flowering in A. unedo) was delayed in 2000 relative to 1999 (Figure 2). In contrast, flowering in P. latifolia occurred earlier in 2000 than in Drought treatment delayed A. unedo flowering both in 1999 and 2000 (P < 0.05) and fruit growth in 2000 (P < 0.05; Figures 3 and 4). Furthermore, A. unedo from drought plots had lower percentages of fruit-developing trees than those of control plots in both years (P < 0.05; Figure 4). Quercus ilex and P. latifolia did not show any delay in flowering or any change in fruit growth (Figures 3 and 4). Shoot litterfall was higher in drought than in control plots during the overall studied period (P = 0.01) and especially in 1999 (Figure 5). The amount of flower and fruit production, and also leaf shedding, showed high inter-annual variability, but lower fall of flowers and fruits in A. unedo and higher leaf litterfall in P. latifolia were observed in some years under drought conditions (Figure 6). Arbutus unedo experienced larger flower and fruit production (relative to its aboveground biomass) than P. latifolia and Q. ilex during the overall studied period (P < 0.05). Flower and fruit productions were also larger in P. latifolia than in Q. ilex (Figure 6). Discussion The occurrence of phenological events is mainly correlated with air temperature (Spano et al., 1999; Peñuelas & Filella, 2001; García-Mozo et al., 2002; Peñuelas, Filella & Comas, 2002) and with water availability (Kramer, Leinonen & Loustau, 2000; Pardos et al., 2003; Peñuelas et al., 2004). In our study, flowering in P. latifolia took place earlier in 2000 than in 1999, coinciding with higher temperatures in late winter 2000 compared to However, leaf flushing in A. unedo and P. latifolia, and flowering in A. unedo, seemed to be more FIGURE 2. Phenological diagrams of Arbutus unedo, Phillyrea latifolia, and Quercus ilex during the study period. Grey bars indicate the duration of each phenophase in the control plots. 266

5 ÉCOSCIENCE, VOL. 11 (3), 2004 FIGURE 3. Percentage of A. unedo, P. latifolia, and Q. ilex trees flowering during 1999 and 2000, according to treatments (mean ± SE; n = 4). One asterisk indicates significant differences (P < 0.05) between the two treatments for each sampling date (ANOVA). The significance for the overall treatment effect was assessed with a log-rank test. FIGURE 4. Percentage of A. unedo, P. latifolia, and Q. ilex trees developing fruits during 1999 and 2000, according to treatments (mean ± SE; n = 4). One asterisk indicates significant differences (P < 0.05) between the two treatments for each sampling date (ANOVA). The significance for the overall treatment effect was assessed with a log-rank test. dependent on water availability, because their occurrence in 1999 and 2000 coincided with spring rainfall periods. The timing of leaf flushing and flowering in Q. ilex was more constrained. No differences were observed between 1999 and Probably there is another environmental cue, such as day length or radiation, or even an endogenous cue, that sets this event. Fruit production in Q. ilex may be related to water availability, since lower water availability during the first stages of fruit development in 1999 coincided with very low fruit production. To confirm that changes in fruit production are only related to water availability and not to other environmental factors, it is necessary to conduct controlled experiments. Flowering is mainly associated with low vegetative growth (Fitter, 1986; Bazzaz et al., 1987) and with resource competition between reproductive and vegetative structures (Jonasson, Medrano & Flexas, 1997). Yet, Q. ilex and P. latifolia developed new leaves and flowers 267

6 OGAYA & PEÑUELAS: PHENOLOGY UNDER DROUGHT FIGURE 5. Percentage of stem litterfall relative to total aboveground biomass in each plot (mean + SE; n = 4). One asterisk indicates significant differences (P < 0.05) between the two treatments for each sampling date (ANOVA). A significant difference between the two treatments during the overall period of the study is also depicted (repeated-measures ANOVA). during the same season. Only A. unedo did not, thus avoiding competition for the same resources between the synthesis of reproductive and vegetative structures. Drought treatment delayed flowering and fruit development in A. unedo. Another study conducted in the same experimental field area revealed a stronger decrease of stem radial growth rates in A. unedo than in Q. ilex and P. latifolia in response to this experimental decrease in water availability (Ogaya et al., 2003). These results together show a higher drought sensitivity in A. unedo than in Q. ilex or P. latifolia. Higher stem litter in the drought plots could indicate higher drying rates in current-year shoots. Trees under drought conditions seemed unable to maintain the same number of thin shoots as trees in control plots. On the other hand, higher mortality rates were observed in trees growing in the drought plots than in the control ones (Ogaya et al., 2003), so greater shoot litter from dead trees can be expected in these drought plots. Low water availability is mainly associated with a reduction in reproductive effort, as is observed in some FIGURE 6. Percentage of flower and fruit litter relative to the total aboveground biomass, and percentage of leaf litter relative to the total biomass of remaining leaves, in each studied species (mean + SE; n = 4). 268

7 ÉCOSCIENCE, VOL. 11 (3), 2004 Mediterranean plants (Aronson, Kigel & Shmida, 1993). Despite a great inter-annual variability, the drought treatment seemed to reduce the production of reproductive structures in A. unedo, and lower fruit production could reduce the number of young plants of this species. The recruitment of young plants is a key factor determining future species distribution. Arbutus unedo showed a higher reproductive effort than the two other species, and it was again the species most affected by the drought treatment. Quercus ilex (the species showing the lowest reproductive effort) and A. unedo have a strong capacity to produce sprouts. These sprouts obtain water and nutrients from the well-developed root system of previously established individuals, showing higher growth rates and better water status than mature plants (Castell, Terradas & Tenhunen, 1994). Seedlings obtain water and nutrients only from the roots they develop, and P. latifolia recruitment is more dependent on new seedlings despite its capacity to produce sprouts (Herrera et al., 1994). High drought resistance in Q. ilex sprouts and an important seedling mortality in P. latifolia seedlings were observed in the area studied (Lloret, Peñuelas & Ogaya, 2004). In spite of this, the performance of adult trees is still crucial for the longterm presence of any species. An immediate effect is through the mentioned nurturing of resprouts, but under repeated drought episodes these sprouts cannot contribute to maintain the presence of this species in the future. The results presented here show that the decrease in water availability expected for the next decades in the Mediterranean areas (IPCC, 2001) could produce changes in the timing of some phenological events of some species. 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