Sequence of plant responses to droughts of different timescales: lessons from holm oak (Quercus ilex) forests

Figures & data

Table 1. Adaptive morphological, physiological, and phenological mechanisms and/or traits of Quercus ilex for withstanding summer droughts.

	Organ	Adaptive mechanism or trait	Developmental time	Duration
Morphology	Roots	Tap roots reaching water table or water pools in rock fractures	Individual life	Persistent
		Relatively high below-ground biomass	Individual life	Persistent
		Low proportion of fine roots	Seasonal	Transient
	Leaves	Sclerphylly	Seasonal	Transient
Physiology	Leaves	Stomatal closure to reduce xylem tension	Instantaneous	Transient
	Systemic	Osmotic adjustment to maintain cellular turgor	Hours	Transient
Phenology	Stems	Summer growth cessation (bimodal growth pattern)	Seasonal	Transient
	Leaves and shoots	Most growth completed before summer	Seasonal	Persistent
	Buds	Coexistence of several bud cohorts in the canopy	Years	Transient

Figure 1. Monthly average difference between the monthly precipitation and the monthly potential evapotranspiration (the climatic water balance) for two forests dominated by Quercus ilex. Data were obtained from meteorological stations located at Torners Valley in the Prades Mountains (930 m a.s.l; 1998–2014) and at Viladrau in the Montseny Mountains (950 m a.s.l. 1995–2014). Potential Evapotranspiration is calculated with the SPEI package in R, based on monthly temperature and incoming solar radiation. Error bars are the standard errors of the means.

Figure 2. Map of the current distributional range of holm oak (Quercus ilex) in the Mediterranean Basin.

Table 2. Characteristics of reported drought-induced dieback in Quercus ilex forests involving crown defoliation and/or stem mortality based on the values the drought index SPEI, calculated as defined in the text. CD, crown defoliation, SM, stem mortality.

			SPEI
Study	Drought Year	Site	3 May	6 May	3 August	6 August	9 October	12 December	24 December	Bedrock	Reported effects
Lloret et al. (2004)	1985	Sant Llorenç de Munt	−0.13	0.14	−0.85	−0.44	−1.06	−0.22	−0.39	Schists, Breccia	Not available
Lloret et al. (2004)	1994	Sant Llorenç de Munt	0.67	0.53	−1.51	0.10	0.87	−0.99	0.61	Schists (S), Breccia (B)	75.9% of the plants without green foliage (CD) in B and 23.2% in S. Stem mortality (SM) 51.3% in S and 54.6% in B.
Galiano et al. (2012)	2000	Garrotxa	−0.84	−0.59	−0.68	−0.77	−0.96	0.12	−1.14	Conglomerate	73.8% of the trees with some level of CD in patches with much browning
Barbeta et al. (2013)	2005	Prades	−1.90	−1.44	−2.00	−1.87	−1.71	0.43	0.23	Schists	Average of 5.4% stem mortality (SM)
Camarero, Sangüesa-Barreda, et al. (2015)	2005	Arascués	−1.16	−1.19	−1.66	−1.89	−1.84	−1.64	−1.98	Calcareous	Average CD 35%
Barbeta et al. (2015), Ogaya, Barbeta, et al. (2014)	2011	Prades	−0.43	−0.34	−0.47	−0.76	−1.10	0.90	−0.62	Schists	Averages of 3.9% SM and 22.5% CD
Camarero, Sangüesa-Barreda, et al. (2015)	2012	Arascués	−0.44	−1.58	−0.21	−0.44	−0.02	−0.72	−1.83	Calcareous	Average CD 44%. Tree mortality 1.3%
Camarero, Sangüesa-Barreda, et al. (2015)	2012	Formiche Bajo	−1.28	−0.64	−1.25	−1.50	−1.37	−0.56	−0.89	Calcareous	CD ranged between 35% and 60%

The values of the Standarised Precipitation and Evapotranspiration Index (SPEI) (Vicente-Serrano et al. 2010) are calculated at different months and timescales for published reports of episodes of forest dieback that included stem mortality and/or crown defoliation. The SPEI index is a multi-scalar drought index based on the normalisation of the climatic water balance (i.e. the difference between the potential evapotranspiration (PET) and the precipitation (P)) for a given period of time at monthly intervals. The probability density function obtained from the time series of P-PET for a particular location is fitted to a log-logistic distribution for normalisation. The normalised values of P-PET (SPEI value) range from −3 to 3. The average value of SPEI is 0, meaning that for a certain period of time (e.g. from March to June) the climatic water balance is equal to the historical average. Negative SPEI values indicate periods drier than the average, whereas positive values indicate periods with conditions wetter than average. A key advantage of the SPEI (as of its predecessor SPI) is that it is a standardised variable, and it can therefore be compared over time and space.

Figure 3. Correlation heat map between the annual relative change in crown defoliation and the SPEI values for Iberian Quercus ilex forests (1987–2013, 233 plots). The SPEI duration on the x-axis represents the number of months used to calculate the water balance (e.g. an SPEI duration of 3 in June is calculated using the water balance of the previous April and May and the June itself). The y-axis is the month in which the calculation of SPEI departs from. The panel on the right top indicates the correspondence of the colours in the heat map with the Person’s r coefficient of the correlation between SPEI and defoliation.

Figure 4. Time courses of (a) accumulated crown defoliation and (b) annual change in crown defoliation relative to defoliation from the previous years (red lines). Blue bars are the June SPEIs calculated at a timescale of 23 months, which was the best correlated index. Error bars are the standard errors of the means (N = 233).

Table 3. Summary of the effects identified by studies of long-term experimental drought in Quercus ilex forests.

Organ	Aspect	Variable	Drought treatment effect	Exp. drought duration (years)	Reference
Leaf	Carbon relations	iWUE	Unchanged	4	Limousin, Misson, et al. (2010)
Leaf	Carbon relations	Jmax	Unchanged	4	Limousin, Misson, et al. (2010)
Leaf	Carbon relations	Maximum assimilation rate	Unchanged	4	Limousin, Misson, et al. (2010)
Leaf	Carbon relations	Vcmax	Unchanged	4	Limousin, Misson, et al. (2010)
Leaf	Carbon relations	Maximum assimilation rate	Unchanged	9	Martin-Stpaul et al. (2013)
Stem	Carbon relations	Stem CO2 efflux	Unchanged	9	Rodriguez-Calcerrada et al. (2014)
Leaf	Carbon relations	Stomatal conductance	Unchanged	9	Martin-Stpaul et al. (2013)
Leaf	Carbon relations	Maximum PSII quantum yield	Unchanged	10	Ogaya et al. (2011)
Leaf	Carbon relations	Day respiration	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Jmax	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Maximum assimilation rate	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Mesophyllic conductance	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Night respiration	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Ratio mesophyllic/stomatal conductance	Decreased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Ratio day/night respiration	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Stomatal conductance	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Summer maximum assimilation rate	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Summer carbon-use efficiency	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Summer mesophyllic conductance	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Summer stomatal conductance	Increased	13	Sperlich et al. (2015)
Leaf	Carbon relations	Triose–phosphate use	Unchanged	13	Sperlich et al. (2015)
Leaf	Carbon relations	Vcmax	Unchanged	13	Sperlich et al. (2015)
Branch	Carbon relations	Branch NSC	Unchanged	14	Rosas et al. (2013)
Leaf	Carbon relations	Leaf NSC	Unchanged	14	Rosas et al. (2013)
Roots	Carbon relations	Lignotuber NSC	Unchanged	14	Rosas et al. (2013)
Leaf	Carbon relations	Maximum assimilation rate	Unchanged	14	Ogaya, Llusià, et al. (2014)
Leaf	Carbon relations	Stomatal conductance	Unchanged	14	Ogaya, Llusià, et al. (2014)
Leaf	Epigenetics	Fully methylated DNA loci	Decreased	12	Rico et al. (2013)
Leaf	Morphology and allometry	Leaf area	Unchanged	3	Ogaya and Peñuelas (2006)
Leaf	Morphology and allometry	Leaf mass per unit area	Decreased	3	Ogaya and Peñuelas (2006)
Leaf	Morphology and allometry	Leaf thickness	Unchanged	3	Ogaya and Peñuelas (2006)
Several	Morphology and allometry	Ratio of leaf to sapwood area (shoot)	Decreased	6	Limousin, Longepierre, et al. (2010)
Stem	Morphology and allometry	Lumen area	Increased	6	Limousin, Longepierre, et al. (2010)
Stem	Morphology and allometry	Vessel diameter	Unchanged	6	Limousin, Longepierre, et al. (2010)
Stem	Morphology and allometry	Vessel frequency	Unchanged	6	Limousin, Longepierre, et al. (2010)
Stem	Morphology and allometry	Wood density	Decreased	6	Limousin, Longepierre, et al. (2010)
Branch	Morphology and allometry	Branch litterfall	Unchanged	7	Limousin et al. (2012)
Leaf	Morphology and allometry	Leaf area index	Unchanged	7	Limousin et al. (2012)
Leaf	Morphology and allometry	Leaf litterfall	Decreased	7	Limousin et al. (2012)
Several	Morphology and allometry	Ratio of leaf to sapwood area (shoot)	Decreased	7	Limousin et al. (2012)
Branch	Morphology and allometry	Shoot length	Unchanged	7	Limousin et al. (2012)
Several	Morphology and allometry	Ratio of leaf to sapwood area (shoot)	Decreased	9	Martin-Stpaul et al. (2013)
Leaf	Morphology and allometry	Leaf litterfall	Increased	15	Liu et al. (2015)
Leaf	Water relations	Canopy conductance	Decreased	4	Limousin et al. (2009)
Several	Water relations	Daily transpiration (tree level)	Decreased	4	Limousin et al. (2009)
Leaf	Water relations	Midday leaf water potential	Unchanged	4	Limousin et al. (2009)
Several	Water relations	Tree use of precipitation	Increased	4	Limousin et al. (2009)
Several	Water relations	Whole-tree conductivity	Unchanged	4	Limousin et al. (2009)
Stem	Water relations	Pressure causing 50% loss of conductivity	Unchanged	6	Limousin, Misson, et al. (2010)
Leaf	Water relations	Predawn water potential	Decreased	6	Limousin et al. (2009)
Leaf	Water relations	Predawn water potential	Decreased	6	Limousin, Longepierre, et al. (2010)
Stem	Water relations	Slope of the vulnerability curve	Unchanged	6	Limousin, Longepierre, et al. (2010)
Stem	Water relations	Stem specific conductivity	Unchanged	6	Limousin, Longepierre, et al. (2010)
Leaf	Water relations	Predawn water potential	Unchanged	7	Limousin et al. (2012)
Leaf	Water relations	Leaf specific conductivity	Increased	9	Martin-Stpaul et al. (2013)
Stem	Water relations	Stem specific conductivity	Unchanged	9	Martin-Stpaul et al. (2013)
Roots	Water relations	Depth of soil water uptake	Decreased	12	Barbeta et al. (2015)
Roots	Water relations	Midday leaf water potential	Unchanged	12	Barbeta et al. (2015)
Roots	Water relations	Relative groundwater use	Decreased	12	Barbeta et al. (2015)
Leaf	Water relations	Midday leaf water potential	Unchanged	14	Ogaya, Llusià, et al. (2014)
Leaf	Physiology	Nitrogen per unit area	Unchanged	9	Martin-Stpaul et al. (2013)
Leaf	Physiology	Nitrogen per unit mass	Unchanged	9	Martin-Stpaul et al. (2013)
Seed	Phenology	Flowering	Unchanged	2	Ogaya and Peñuelas (2004)
Seed	Phenology	Fruiting	Unchanged	2	Ogaya and Peñuelas (2004)
Leaf	Phenology	Leaf flushing	Unchanged	2	Ogaya and Peñuelas (2004)
Leaf	Phenology	Leaf unfolding	Unchanged	2	Ogaya and Peñuelas (2004)
Leaf	Phenology	Budburst	Delayed	7	Limousin et al. (2012)
Leaf	Phenology	Leaf lifespan	Increased	7	Limousin et al. (2012)
Stem	Production	Stem growth	Decreased	2	Ogaya and Peñuelas (2003)
Stem	Production	Stem growth	Decreased	5	Ogaya and Peñuelas (2007a)
Stem	Production	Stem mortality	Unchanged	5	Ogaya and Peñuelas (2007a)
Seed	Production	Fruit litterfall	Decreased	7	Ogaya and Peñuelas (2007b)
Stem	Production	Stem growth	Unchanged	9	Martin-Stpaul et al. (2013)
Stem	Production	Stem growth	Unchanged	13	Barbeta et al. (2013)
Stem	Production	Stem mortality	Increased	13	Barbeta et al. (2013)
Several	Production	Increase in above-ground biomass	Unchanged	15	Liu et al. (2015)
Seed	Production	Fruit litterfall	Decreased	15	Liu et al. (2015)

Figure 5. Conceptual scheme of the most relevant effects of the long-term drought experiments in Quercus ilex forests at the tree and ecosystemic levels. The span of the rectangles defines the duration of the effects. The rectangles that surpass 12 years indicate effects that lasted till the present day of the experiment. The position on the x-axis represents the approximate time of appearance. Rectangles with dashed contour lines indicate potential effects that require further study.

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