Environmental and Experimental Botany 53 (2005) 111

Effects of water and a nutrient pulse supply on Rosmarinus ofcinalis growth, nutrient content and owering in the eld
J. Sardans a, , F. Rod b , J. Peuelas a
a

Unitat dEcosiologia CSIC-CEAB-CREAF, CREAF (Center of Ecological Research and Forestry Applications) Edici C, Universitat Autnoma de Barcelona, Bellaterra 08193 (Barcelona), Spain b CREAF (Center of Ecological Research and Forestry Applications), Edici C, Universitat Autnoma de Barcelona, Bellaterra 08193 (Barcelona), Spain Accepted 23 February 2004

Abstract Rosmarinus ofcinalis is a dominant shrub species of calcareous Mediterranean communities that has increased its presence in wide areas due to re frequency increase and eld abandonment. We aimed to study the capacity of adult shrubs to respond to nutrient pulses such as those produced by res and human driven eutrophycation. In a 5 years old post-re Mediterranean shrubland we conducted an experiment to investigate the effects of irrigation and N and P fertilisation on the growth, nutrient status and owering effort of adult plants of the dominant shrub R. ofcinalis in a post-re shrubland. The responses were monitored during the immediate 3 years after fertilisation. P fertilisation increased plant growth, produced a great increase in P aerial mineralomass and P concentration in leaf and stems and had a slight positive effect on owering effort. Irrigation increased plant growth, but did not have signicant effects on nutrient contents and owering. The results show that adult individuals of the Mediterranean shrub R. ofcinalis have a notable capacity to positively respond in growth and in nutritional status to a sudden increase of the limiting nutrient, in this case P, and in a lesser extent, to an increase of water supply. These capacities may be important under the more unpredictable nutrient and water availability conditions expected for the near future; they will allow to take advantage of the pulses of higher nutrient and water availability in the middle of dry periods, thus increasing the community capacity to improve the nutrient retention in the ecosystem. 2004 Elsevier B.V. All rights reserved.
Keywords: Calcareous soil; Flowering; Irrigation; Growth; Mediterranean; Nitrogen; Nutrient content; Nutrient pulse; Phosphorus; Rosmarinus ofcinalis; Shrubland

1. Introduction The summer drought is the most characteristic trait of Mediterranean ecosystems (Mooney and Parsons,
Corresponding author. Tel.: +93-581-13-12; fax: +93-581-41-51. E-mail address: j.sardans@creaf.uab.es (J. Sardans).

1973; Specht, 1979; Mooney, 1989), but the nutrients play an important role too (Kruger, 1979; Specht, 1979; Carreira et al., 1992). Water and nutrient availability are the main abiotic factors that drive the structure and relations in Mediterranean plant communities (Dunn et al., 1977; Rundel, 1982; Witkowski et al., 1990; Barbault and Doucet, 1993; Lebourgeois et al., 1997; Rod et al., 1999). Mediterranean ecosystems

0098-8472/$ see front matter 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2004.02.007

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are also characterised by recurrent res (Trabaud, 1991). Frequent res in wide areas of Mediterranean Basin may result in cumulative nutrient losses through volatilisation, smoke particles, windblown ashes, soil leaching and soil erosion (Tiedmann et al., 1978; Belillas and Rod, 1993; Serrasolsas and Vallejo, 1999). However, re increases N and P availability in the rst moments after re (Kutiel and Shaviv, 1989; Thomas et al., 1999; Gimeno-Garcia et al., 2000). The sudden increase in P availability frequently lasts only a short time due to the fact that such increase principally occurs in soluble P inorganic forms (Kutiel and Kutiel, 1989; Thomas et al., 1999), and therefore, the P losses after re can also be high after re (Soto et al., 1997). On the other hand, in the last decades, the great use of fertilisers and farm residues to increase agricultural yield and air pollution have increased the N and P inputs in those Mediterranean ecosystems (Peuelas and Filella, 2001). The increase of atmospheric CO2 concentration can also vary plant nutrient needs in these Mediterranean ecosystems (Peuelas and Matamala, 1990; Peuelas et al., 2001) and the climate change may affect nutrient availability (Sardans and Peuelas, 2004). Thus, the increase of re frequency, eutrophycation, and atmospheric and climatic changes favour a wide range of nutrient inputs and nutrient availability across the territory, that can trigger species substitution in some Mediterranean areas (Carreira et al., 1992). Henkin et al. (1994) observed that the cattle activity signicantly increased the P availability in the soil top layers of some Mediterranean areas favouring the growth of herbs more than the growth of shrubs. In a Mediterranean area of Galilee a single application of P-fertiliser signicantly retarded regeneration of shrub and produced a 35-fold increased in herbaceous biomass, suggesting a change in the typical Mediterranean succession toward a stable evergreen Mediterranean community (Henkin et al., 1998). The capacity of response of the reproductive effort to nutrient fertilisation in Mediterranean environments has been previously tested and some positive effects have been observed, especially for N supply (McMaster et al., 1982; Herrera, 1992; Vil and Terrades, 1995). The increased of nutrient availability with or without water availability changes can affect the reproductive effort of the dominant species of the Mediterranean shrublands and in this form affect the future composition of these communities.

Rosmarinus ofcinalis is a very widespread shrub in the Mediterranean basin that is dominant in the post-re shrubland communities principally in calcareous soils. It is an obligate seed germinator with abundant owering. Its sunlit character and its high reproductive effort allow it to colonise the bare landscape. Its presence on landscape has been progressively increased in the last decades in wide areas of north-western Mediterranean Basin likely as a consequence of increased re frequency and eld crops abandonment. Furthermore, this species is important in order to maintain the soil structure and fertility both in the rst weeks after a re event and in the rst phases of community building that can last some years. The capacity to respond to different water and nutrient supply levels in the eld is important not only for the growth and persistence of R. ofcinalis but for the capacity to maintain the nutrients in the ecosystem during the initial and middle phases of ecological succession. The capacity to improve the plant tness (growth and reproduction effort) and mineralomasses increments of the adult shrub plants in response to nutrient pulses is determinant of the future productivity of the community and may be an important mechanism to guarantee the preservation of soil quality that permits the future establishment of Mediterranean tree species. We conducted a study in a eld post-re calcareous shrubland dominated by adult plants of R. ofcinalis 5 year after the last re to investigate the effect of a nutrient pulse and water availability on growth, nutrient contents and reproductive effort of adult R. ofcinalis plants in natural conditions. We aimed to gain knowledge on the extent up to which R. ofcinalis is able of responding to sudden nutrient inputs and under different levels of water supply, when plants have already reached their maturity.

2. Material and methods 2.1. Experimental plot The experiment was conducted in a naturally regenerated post-re shrubland that had been burnt three times in the past 20 years. The last re occurred in summer 1985, 5 years before the experiment started. The study site was located on a hill top (slope

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05%) at 300 m above sea level (41 37 N, 1 50 E). A Lithic haploxeroll soil associated with Lithics xerorthens soils (soil taxonomy) are developed over Calcareous-loam eocenic rocks of sedimentary origin. They have a high pH (8.3 0.2) and proportion of carbonates (55.9 1.2%) and active lime (12.2 0.5%). The climate is Mediterranean with a slight continental component. Mean annual rainfall is 517 mm. The vegetation type is a post-re Mediterranean shrubland (Erico Thymalaeetum tinctoreae), dominated by the shrubs R. ofcinalis, Erica multiora and Thymalea tinctorea with young saplings of Pinus halepensis and resprouts of Quercus ilex subsp. rotundifolia. 2.2. Experimental design Two different statistical designs were conducted for factorial ANOVA analyses. In the rst one, there were two factors: NP fertilisation (two levels; with and without) and irrigation (two levels; with and without), which involved four treatments: C (control), NP (N and P fertilisation), W (irrigation), and NPW (N and P fertilisation + irrigation). Each treatment was applied to 10 individuals. In the second factorial design, the factors were: P fertilisation (two levels; with and without) and N fertilisation (two levels; with and without), which involved four treatments: C (Control), P (P fertilisation), N (N fertilisation) and NP (N and P fertilisation). Each treatment was applied to 10 individuals. 2.3. Treatments application The fertilisation treatments were applied in July 1990 at individual level (in a circle of 1 m2 around each plant with a single dose equivalent to 250 kg ha1 of P and 500 kg ha1 of N). The water supply treatment was applied by irrigation of 1 m2 around the individual plant. The dose was equivalent to 24 l m2 in each irrigation application. The application of water irrigation was conducted each week in a unique dose, since MaySeptember, and only in the weeks with natural rainfalls below 20 l m2 . In the rst period of irrigation application (AprilAugust 1991) the water applied by irrigation was 240 mm while the natural rainfall was 196 mm; therefore the irrigated plants received 120% more water than the non-irrigated plants. In the second period (AprilAugust 1992), plants re-

ceived 120 mm by irrigation and 458 mm by natural rainfall; therefore the irrigated plants received 26% more water than the non-irrigated plants. Finally, in the third period (AprilAugust 1993), the water applied by irrigation was 168 mm and the natural rainfall was 247 mm; and therefore irrigated plants received 68% more water than the non-irrigated plants. 2.4. Growth measurements The experimental factor effects on biomass growth were determined by measuring four variables: the absolute and the relative basal diameter and height growths. The initial measurements were taken at the beginning of the experiment establishment. The nal measurements were taken in August 1993, 3 years after treatment application. For this reason, all the growth variables correspond to the accumulated growth of 3 years. 2.5. Biomass sampling and chemical analyses To determine the treatment effects on mineral contents two biomass samplings were conducted; in July 1992 and in July 1993, 2 and 3 years after the fertilisation application. Three different biomass fractions were harvested: current year leaves, 1-year-old leaves and wood. In each individual and in each leaf cohort ve leaf groups were harvested, in the four cardinal sides (at middle plant height) and in the central top of the crown. The harvested stems contain at least the last four annual growths. Biomass fractions were dried at 70 C during 48 h, and then ground with a FRITSCH pulverisette 09202 (Laval Lab Inc. Laval, Canada). The ground samples were submitted to an acid digestion with HNO3 :HClO4 (2:1) to obtain a complete oxidation of the organic matter. The nal solution was analysed by ICP AES (Atomic Emission Spectroscopy with Inductively Coupled Plasma) with an spectrophotometer ICP-AES of the type JOBIN YBON JI 38 (Jobin, France). With this method we analysed the concentrations of P, S, Ca, Mg, Fe and K. The N concentrations of the samplings of 1992 were measured by the Kjeldhal method (Lee and Littleeld, 1997), in a KJELDHAL 1030 AUTOANALYZER (TECATOR, Hgans, Sweden), with previous acid digestion (with H2 SO4 + catalysis re-

J. Sardans et al. / Environmental and Experimental Botany 53 (2005) 111

400
(

active) conducted with a DIGESTION SYSTEM 20 1015 DIGESTER (TECATOR, Hgans, Sweden). 2.6. Flowering measurements The owering effort was measured through periodical ower recounts. Each recount was conducted counting all the owers with open corollas. In a previous study (Sardans, 1997) we found that the owers have the corolla open until their senescence about 20 days in all the treatments. Therefore, during the owering periods the recounts were conducted every 20 days with the aim to count all the owers but avoiding counting the same ower twice. We considered the annual date of maximum owering in each treatment group the date that we counted the largest number of owers. 2.7. Statistical analyses The water and nutrient effects on the studied variables were analysed through factorial ANOVAS by using the Super ANOVA package (Abacus Concepts Inc., Berkeley, 1989). Comparisons between treatments were done by Duncan new multiple range post hoc ANOVA tests.
Absolute basal diameter growth (mm) Absolute height growth (mm)

300

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100

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Relative height growth (%) Relative basal diameter growth (%)
60

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0 16

12

3. Results
0

3.1. Biomass growth 3.1.1. Design: NP fertilisation irrigation Irrigation increased the relative height growth (P = 0.03) and marginally the absolute height growth (P = 0.08) and relative basal stem diameter growth (P = 0.1) (Fig. 1). Irrigation also tended to increase the absolute basal stem diameter growth, but these effects were not signicant (P = 0.13 and P = 0.11, respectively) (Fig. 1). NP fertilisation had a marginal effect, principally, on absolute height growth (P = 0.08) (Fig. 2). No interactions were detected between these two experimental factors. 3.1.2. Design: N fertilisation P fertilisation P fertilisation increased the absolute (P = 0.04) and relative (P = 0.03) height growth and the relative basal diameter growth (P = 0.05) (Fig. 3). The effect

80

60

40

20

Without

With

Irrigation
Fig. 1. Irrigation effects on absolute (mm) and relative (%) height growth (mean S.E., n = 20), and on absolute and relative basal diameter growth (mean S.E.) (*: P < 0.05, (*): P < 0.10).

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400
(

400

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Absolute height growth (mm)
300 200

Absolute height growth (mm)

300

200

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100

0
(

Relative height growth (%)

Relative height growth (%) Absolute basal diameter growth (mm)

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40

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Absolute basal diameter growth (mm)

16

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Relative basal diameter growth (%)

80

Relative basal diameter growth (%)

60

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Without
-1

With
-1

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With

NP fertilisation
(500 kg N ha + 250 kg P ha )
Fig. 2. N plus P fertilisation (500 kg N ha1 + 250 kg P ha1 ) effects on absolute and relative height growth (mean S.E., n = 20) and on absolute and relative basal diameter growth (mean S.E., n = 20) (*: P < 0.05, (*): P < 0.10).

P fertilisation
(250 kg P ha-1)
Fig. 3. P fertilisation (250 kg P ha1 ) effects on absolute (mm) and relative (%) height growth (mean S.E., n = 20), and on absolute and relative basal diameter growth (mean S.E., n = 20) (*: P < 0.05).

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of P fertilisation on absolute basal diameter growth was positive but not signicant (Fig. 3). N fertilisation had not effects on growth (data not shown). No interactions were detected between these two experimental factors. 3.2. Nutrient contents 3.2.1. Design: NP fertilisation irrigation In the sampling of July 1992 the NP fertilisation increased the P concentrations of all biomass fractions analysed (Table 1). NP fertilisation increased the Ca concentrations in the stems and S concentrations in the 1-year-old leaves, and decreased S concentrations in the current-year leaves (Table 1). In the sampling

of July 1993 the NP fertilisation increased P concentrations in the current-year leaves and in the stems (Table 1). In the samplings of July 1992 and 1993 irrigation decreased Fe concentrations in the stems, increased 1-year-old leaves S concentrations in the sampling of July 1992, and decreased Ca stem concentrations in the sampling of July 1993 (Table 1). No interactions were observed between experimental factors. 3.2.2. Design: N fertilisation P fertilisation In the sampling of July 1992 P fertilisation increased P concentrations in the stems in the 1-year-old leaves (Table 1). In the sampling of July 1993 P fertilisation increased P concentrations in the stems and

Table 1 Elemental concentrations (mean S.E., mg g1 , n = 20), which have varied due to experimental factors (P = signicance of the differences between the different levels of the experimental factors) Experimental factor Element and fraction No fertilised 4.38 0.18 0.33 0.01 0.40 1.37 0.56 1.43 0.50 0.07 0.05 0.049 Fertilised 5.02 0.17 0.48 0.04 0.54 1.49 0.70 1.25 0.04 0.04 0.09 0.04 P 0.04 0.003 0.055 0.003 0.018 0.021

Design: NP fertilisation irrigation (sampling July 1992) Ca in stems P in stems NP fertilisation P S P S in in in in 1-year-old leaves 1-year-old leaves current leaves current leaves

No irrigated Irrigation Fe in stems S in 1-year-old leaves 0.26 0.02 1.37 0.07 No fertilised Design: NP fertilisation irrigation (sampling July 1993) NP fertilisation P in current leaves P in stems 0.34 0.06 0.38 0.03 No irrigated Irrigation Ca in stems Fe in stems 7.63 0.25 0.22 0.02 No fertilised Design: N fertilisation P fertilisation (sampling July 1992) P fertilisation P in stems P in 1-year-old leaves N fertilisation S in 1-year-old leaves N in 1-year-old leaves 0.31 0.01 0.35 0.01 1.53 0.05 7.58 0.30 0.38 0.02 10.5 1.2

Irrigated 0.18 0.01 1.48 0.04 Fertilised 0.51 0.06 0.54 0.04 Irrigated 5.94 0.19 0.16 0.02 Fertilised 0.51 0.06 0.51 0.04 1.33 0.06 9.59 0.58 0.48 0.03 15.9 1.5 0.006 0.006 0.018 0.007 0.036 0.027 0.070 0.030 0.019 0.01 0.041 0.041

Design: N fertilisation P fertilisation (sampling July 1993) P fertilisation P in stems Ca in current leaves

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Fig. 4. Number of owers in the moment of maximum annual owering and total annual quantity of owers per individual in the period 19911993 in the different levels of the experimental factors (mean S.E., n = 20). In the year 1992 and in the NP fertilisation. Irrigation design, the date of maximum annual owering was different depending on the level of the experimental factors and consequently two dates are exposed (*: P < 0.05 between the different levels of experimental factors, (*): P < 0.10 between the different levels of the experimental factors).

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Ca concentrations in current-year leaves (Table 1). In the sampling of July 1992 N fertilisation increased N concentrations in 1-year-old leaves and decreased the S concentrations in the 1-year-old leaves (Table 1). No interactions were observed between experimental factors. 3.3. Flowering effort 3.3.1. Design: NP fertilisation irrigation The maximum owering in 1991 and 1993 occurred at the same dates for all the levels of the factors (Fig. 4). In 1992 the maximum owering was delayed in plants without fertilisation and in plants without irrigation (Fig. 4). In 1992, the total annual number of owers in the NP fertilised R. ofcinalis plants was also greater than in the non fertilised ones (Fig. 4). In 1991 and 1993 the NP fertilisation treatment had no signicant effect on the number of owers for individual R. ofcinalis. No interactions were detected between experimental factors (Fig. 4). 3.3.2. Design: N fertilisation P fertilisation N fertilisation had no signicant effect on the timing of maximum owering neither on the annual total number of owers per individual across the 3 years investigated (Fig. 4). P fertilisation had no effects on the timing of maximum owering nor on the annual total number of owers across the 3 years investigated (Fig. 4). No interactions were detected between experimental factors (Fig. 4).

4. Discussion Adult individuals of R. ofcinalis in a typical calcareous Mediterranean shrubland have been shown to increase their growth in response to increased water supply and to a nutrient supply pulse, together or alone. The irrigation effect was signicant even though the 3 years of the experiment were considerably wet for the studied site. Positive effects of irrigation in the eld on Mediterranean shrubs have also been observed in R. ofcinalis (Kandeel, 2001) and in Retama sphaerocarpa (Benayas et al., 2002). The positive effect of the fertilisation was mostly due to P fertilisation, which is in accordance with previous studies in calcareous Mediterranean shrublands (Carreira et al.,

1992; Sardans et al., 2004). The positive effects of the P fertilisation pulse on growth that was still detected 3 years after fertilisation together with the increases in P concentrations show the clear limiting role of P in this shrubland. The presence of diphosphate and triphosphate in the high pH environment of these calcareous soils favours the strong immobilisation of calcareous phosphates. In fact, the limiting role of phosphorus in widespread areas of the different Mediterranean zones of the world has been observed in many studies (Zinke, 1973; Kruger, 1979; Specht, 1979; Witkowski et al., 1990). The increase in growth and in P concentrations at the same time implies an increase in P contents in the aerial biomass of R. ofcinalis that therefore increases the P retention in the ecosystem after a sudden input of this nutrient by fertilisation. This increase in the mineralomass may also allow enhanced future growth. Within certain intervals, the nutrient concentrations are proportional to the photosynthetic capacity, and frequently are good indicators of futures higher growths (Bryant et al., 1983; Mugasha et al., 1991; Ouimet and Fortin, 1992). The decrease of Fe in the stems of P fertilised R. ofcinalis can be interpreted as a result of a greater allocation to leaves due to a higher demands for photosynthetic mechanisms promoted by the improvement of P supply. Changes in nutrient concentrations due to a fertilisation with another nutrient have been observed in similar studies (Ouimet and Fortin, 1992). These changes in the concentrations of nutrients different than the nutrient applied by fertilisation can be due to a variation in metabolism activity, to antagonisms of absorption process and/or to a dilution effect due to a greater growth. The antagonism in the absorption process between P and S, together with the dilution effect may be the cause of the decrease of S concentrations driven by our P fertilisation. The low response due to N fertilisation in these variables in comparison with P fertilisation seems to be driven by the high levels of organic matter and the high mineralization rates of this soil that provide a good N supply. Atmospheric N deposition from the nearby Barcelona conurbation (Rod et al., 2002) may also contribute to enriching the ecosystem with available N. Similarly, on calcareous soils in Mediterranean areas of France, the strongest response to fertilisation was also to P not to N (Bonneau, 1986).

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The widespread presence of calcareous soils in the North-west Mediterranean Basin confers to P an important ecological role. The owering period observed in this experiment ranged between January and May with a maximum in the last days of March and rst days of April. Pacini and Franchi (1984) in a owering phenological study with 700 Mediterranean species observed as the owering periods usually occur since March to June. In 1992 the increase of nutrient availability advanced the period of owering to the last winter weeks. This trend maybe advantageous for the synchronisation with pollinator insects that present the maximum activity in the period previous to the moments of maximum heat. Water addition did not increase the owering effort of R. ofcinalis in our study. This result is different from the results reported for the Mediterranean species such as Pistacea lentiscus that has been found to increase its reproductive effort in the two rst years of irrigation application (Verd and Garc a-Fayos, 1998). The owering effort was more sensitive to N plus P fertilisation than to irrigation. The building of reproductive organs such as owers implies the synthesis of substances (proteins, hormones, substances for insect attraction) that demand P and N. In environmental conditions of low P and/or N supply, in spite of a high water availability, the photosynthetic products would have high C:N and C:P ratios, and in these circumstances the plants allocate more towards somatic organs than towards reproductive ones (Saulnier and Reekie, 1995; Wyka and Galen, 2000).

resource pulses can be important for this species and, in general, for the community resilience capacity in a more unpredictable and contrasted rainfall regime as the one predicted for next decades for the Mediterranean basin (IPCC, 2001), and in response to more frequent nutrient availability pulses due to human pollution and increased re frequency.

Acknowledgements This research was supported by MCYT projects AMB 95-0247, REN 2001-0003, and REN 2003-04871.

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