Sensitivity of black alder (Alnus glutinosa [L.] Gaertn.)growth to hydrological changes in wetland forests at the rearedge of the species distribution

Patricia Marıa Rodrıguez-Gonzalez • Filipe Campelo •

Antonio Albuquerque • Rui Rivaes • Teresa Ferreira •

Joao Santos Pereira

Received: 3 April 2013 / Accepted: 17 December 2013 / Published online: 3 January 2014

� Springer Science+Business Media Dordrecht 2013

Abstract Functional responses of riparian species

can be used as surrogates for their vulnerability to

climate-driven changes. In particular, black alder

(Alnus glutinosa [L.] Gaertn.) might be highly

susceptible to changes in habitat at the southern limit

of its biogeographical distribution in the Mediterra-

nean Basin. In this study, the long-term environmental

signal of black alder on a river system in southern

Portugal was determined on trees located in different

geomorphological position across the floodplain. For

all sampled trees, we related radial growth to monthly

precipitation, temperature and streamflow. Tree

growth responded to some degree to climatic vari-

ables, while a marked reduction of tree-ring growth

was observed after extreme hydrologic events leading

to mechanical damage and uprooting, especially when

located near and downstream on the active channel.

Similarly, during the first years of life, tree-ring width

tended to be narrower near to the active channel,

whereas trees at far and less disturbed sites grew faster

and, therefore, showed wider rings. Our results

confirm the potential of black alder growth as a proxy

for hydrologic conditions in a semi-arid basin, and the

possibility of using the response of this species to track

environmental changes. Given the ecological and

economic importance of black alder, and the potential

for rapid changes in its distribution, the identification

of those areas the most at risk of flood damage, and the

adequate management of high priority alder popula-

tions will become progressively more important over

coming years.

Keywords Climate change � Flooding �Functional responses �Mediterranean � Riparian

systems

Introduction

There is an increasing need for a continuous effort on

generating and assessing reliable indicators of envi-

ronmental changes to cope with current multiscale-

driven alterations. Vulnerability of ecosystems and

species is partly a function of the expected rapid rate of

climate change relative to their resilience. However,

multiple stressors, including human development,

have already substantially reduced biological resil-

ience through diverse local impacts that interact with

global alterations (IPCC 2007). By altering rainfall,

Communicated by John Kupfer.

P. M. Rodrıguez-Gonzalez (&) � A. Albuquerque �R. Rivaes � T. Ferreira � J. S. Pereira

Centro de Estudos Florestais, Instituto Superior de

Agronomia, Universidade de Lisboa, Tapada da Ajuda,

1349-017 Lisbon, Portugal

e-mail: patri@isa.ulisboa.pt

F. Campelo

Centro de Ecologia Funcional, Departamento de Ciencias

da Vida, Universidade de Coimbra, P.O. Box 3046,

3001-401 Coimbra, Portugal

123

Plant Ecol (2014) 215:233–245

DOI 10.1007/s11258-013-0292-9

temperature and runoff patterns, climate change may

disrupt biological and sever ecological linkages,

adding to and increasing risks that are already present

in many hydrographic basins (Palmer et al. 2009).

Negative impacts on the southern Mediterranean

ecosystems will include not only warming and drought

but also increased risk of inland flash floods due to

more frequent extreme events (Sanchez et al. 2004;

Giorgi and Lionello 2008; Nunes et al. 2009).

Therefore, historical data and biological proxies are

important to understand past climate and to improve

our capacity to predict climate and to better anticipate

management options (Palmer et al. 2008).

Tree rings have been used as an alternative proxy

for the reconstruction of past environmental condi-

tions especially out of the short period of available

instrumental data (Fritts 1976; Schweingruber 1996;

D’Arrigo et al. 2008). Only very recently, dendro-

chronology has begun to be applied in Mediterranean

areas and some promising results have been achieved

(Cherubini et al. 2003, Touchan et al. 2005). In spite of

the scarcity of long chronologies in the Mediterranean

basin, some studies have successfully used tree-ring

width to reconstruct the drought frequency in this

region (Nicault et al. 2008; Touchan et al. 2011). Most

of the published dendrochronological studies in the

Mediterranean are based on conifers (Grissino-Mayer

1993), because it is possible to obtain tree-ring width

chronologies, using few trees, with a good climatic

signal, and the identification of missing and false rings

in conifers is easier than in hardwood species.

Hardwood species can be also used as proxies of

climate changes in the Mediterranean basin (Campelo

et al. 2009; Gea-Izquierdo et al. 2011), but their

potential has not been fully explored yet.

Riparian tree species are among the least explored

in dendrochronological studies (Grissino-Mayer

1993). Dating riparian species is often a challenge

due to the asymmetrical growth leading to high

frequency of missing rings, and intra-annual density

fluctuations, together with the reduced life span of

many species found in these habitats (Seiwa et al.

2005). Despite these species-specific issues, in recent

decades, riparian tree-ring growth has been success-

fully used as an indicator of geomorphologic processes

on Populus (Willms et al. 2006) and Fraxinus (Dufour

and Piegay 2008). These efforts have a limited, but

worthy development in Mediterranean areas (Strom-

berg and Patten 1996; Rodrıguez-Gonzalez et al.

2010), to help understanding how physical stressors

interact with the increased water scarcity (Ballesteros

et al. 2011) and climate variability that are already

occurring in most Mediterranean areas (Stella et al.

2013).

Black alder (Alnus glutinosa [L.] Gaertn.) is an

important species in the Mediterranean basin where it

reaches the southern limit of its biogeographical

distribution, and thus its occurrence is mostly

restricted to specific habitat conditions (permanent

access to water) rarely found in streams with marked

seasonal flow variation. Southern Iberian Peninsula is

considered to be one of European refuges for the post-

glacial expansion of A. glutinosa (King and Ferris

1998) thereby a valuable reserve of its genetic

heritage. Alnus glutinosa is a foundation species

having a major role in key ecosystem processes like

nutrient cycling (Roy et al. 2007), nitrogen fixation

(Vogel et al. 1997), and in providing services of flood

control and riverbank stabilization (Claessens et al.

2010). It is the dominant species in some priority-

classified European Habitats, (91E0*, 92/43/CEE),

representing a target species for conservation, and it is

also an important species for forestry (Claessens et al.

2010). Recent and predicted trends for Iberian stream-

flows with increasing aridity (Lorenzo-Lacruz et al.

2012) are likely to threaten Southern European forests

of A. glutinosa (Hacke and Sauter 1996). The risk is

escalating due to the cumulative potential effects of

climate changes with direct or indirect anthropic

pressures (i.e., regulation) and natural pressures like

diseases (Worrall et al. 2010), namely those which are

already causing decline and mortality of southern A.

glutinosa populations (Solla et al. 2010). Dendrochro-

nological studies on A. glutinosa have been focused on

soil preference, growth curves or modelling in north-

ern Europe (Johansson 1999; Ozolincius et al. 2005;

Laganis et al. 2008). A recent study quantifying tree

growth and stand productivity in the Iberian wetland

forests has suggested that hydrologic factors may be

critical for A. glutinosa growth trends (Rodrıguez-

Gonzalez et al. 2010). Similarly, Ballesteros et al.

(2010) have also related flash floods to changes in

wood anatomy of A. glutinosa in Central Spain.

However, the processes underlying A. glutinosa

performance responses to environmental conditions

are not fully understood, due to the inexistence of long

time series of environmental data to be used as

explanatory variables (e.g., hydrologic data). In

234 Plant Ecol (2014) 215:233–245

123

particular, the lack of long-term hydrologic data for

some of the most important riparian ecosystems, in

Southern Europe, has precluded studies from assessing

the effect of hydrologic regime on tree growth. In

southern Portugal, a gauge station on the Odelouca

drainage basin, registering daily data since 1961, and

the sampling availability resulting from the clearing of

all the woody vegetation during the filling of a

reservoir created by a newly built dam offered us an

unprecedented spatio temporal setting to take a step

forward in understanding the effect of hydrologic

conditions on tree riparian species.

The occurrence of a species (A. glutinosa) generally

associated with perennial rivers under typical Medi-

terranean conditions opens questions about the spatio-

temporal interplay among climatic and hydrologic

variables as drivers of riparian life-histories. Indeed, in

the Mediterranean region, riparian tree growth is

limited by multiple factors that vary at various scales

(Dufour and Piegay 2008) and show variable shifts

across the year (Stromberg and Patten 1996). For

instance, flooding can create a subsidy, stress or

disturbance (Rodrıguez-Gonzalez et al. 2010) with

different influence on survival and growth between

young and adult trees (Horton et al. 2001; Stella et al.

2010). Due to this complexity, currently the relative

importance of streamflow regime, climatic and geo-

morphic variability on riparian tree growth is poorly

understood in Mediterranean settings (Gonzalez et al.

2012). In this study, we assess the strength of the

climatic and hydrological signal in A. glutinosa

growing in a Mediterranean river system in southern

Portugal. We hypothesized that (1) A. glutinosa

growth is mostly determined by tree permanent access

to water; (2) A. glutinosa stem radial growth trends are

modulated by geomorphic position in the floodplain

river; and (3) the growth difference trends are more

evident for younger trees.

Methods

Study area

The Odelouca drainage basin is located in southern

Portugal (between 37�1004900N, 8�2905400W and

37�2603300N, 8�1201600W) and has 511 km2 of drainage

area and 92 km of slow-running streams (Fig. 1).

Average annual precipitation around 750 mm, is

mostly concentrated in a wet period from October to

March, contrasting with a very dry one in the

remaining months. This seasonal climatic variation

characterizes a typical Mediterranean hydrological

regime across the hydrographic basin. The lithology of

the drainage basin is composed of sedimentary and

metamorphic formations, namely clay shales, grey-

wacke and sandstones. Throughout the whole Odelo-

uca hydrographic basin, riparian woody vegetation is

generally composed of ash (Fraxinus angustifolia

Vahl), willow (Salix salviifolia Brot.), tamarisk (Ta-

marix africana Poir), oleander (Nerium oleander L.)

and alder (A. glutinosa) formations. Upland contigu-

ous forests are dominated by cork oak (Quercus suber

L.) and holm oak (Quercus ilex L. subsp ballota

[Desf.] Samp.).

Data collection

Field sampling

The field campaign was carried out in summer 2009.

Firstly, we performed an intensive survey to locate and

label A. glutinosa trees in Odelouca river across the

downstream 30 km reach of the river course (down-

stream of Benafatima tributary confluence, Fig. 1C),

where the species was naturally distributed. Upstream

of Benafatima tributary, other types of vegetation were

present (listed above), but not A. glutinosa. Within its

natural distribution range, A. glutinosa trees were

selected in nine sampling sites along approximately

13 km river length such that they covered the whole

gradient of geomorphological position across the

channel outwards (different height and distance from

river). The sampling sites were located in an intermit-

tent reach displaying winter flash peak floods and no

superficial flow in summer with just a few remaining

pools. In order to reduce the ’noise’ caused by the

variation of other factors than geomorphological

position, similar sized and aged trees were sampled

across sampling sites (Table 1). Each tree was geore-

ferenced with a submeter precision Trimble� Geo-

XTTM handheld GPS and a number of habitat variables

(height above water level, horizontal distance to river,

flood width) and dendrometric variables (diameter at

breast height [DBH], height, number of stems per tree)

were registered in the field. The flood width was

determined visually in the field as the bankfull width,

and it was measured for each sampled tree. Trees were

Plant Ecol (2014) 215:233–245 235

123

cored with a standard 5 mm increment borer, taking

two or three perpendicular cores at DBH (Makinen

and Vanninen 1999). For stems bigger than 40 cm

DBH, a cross-section (wood disc) per tree was

obtained at DBH after tree felling, to further mea-

surement of tree-ring width on two or three radii per

disc. In multistemmed trees, only the largest stem was

sampled. A total of 60 trees were collected (30 by

coring and 30 by cross-section).

Hydrologic and climatic data

Climatic data for meteorological stations in or near the

Odelouca River basin were obtained from National

Water Authority website database (http://snirh.pt). We

considered stations with available precipitation and

temperature monthly data for an acceptable measuring

period (minimum of 30 years) (Table 2). Hydrologi-

cal data were also obtained from National Water

a

b

c

Fig. 1 a Location of Arade hydrographic basin in Southwestern Europe, b location of studied reach in Odelouca river, belonging to

Arade hydrographic basin, c sampling sites and hydrometric station along Odelouca river, showing main tributaries

236 Plant Ecol (2014) 215:233–245

123

Authority website database (http://snirh.pt) and refer

to Monte dos Pachecos (code 30G/01H) gauge station

daily discharge (m3/s) and monthly flow (hm3) records

(1961–2000) (Table 2). In order to carry out the

hydrologic calculations, Thiessen polygons were built

for the considered meteorological stations to permit

annual and monthly precipitation estimation in each

drainage basin area (Thiessen 1911). Precipitation in

each drainage basin was estimated by summing the

area weighted precipitations of the resulting inter-

ception between Thiessen polygons and each respec-

tive drainage areas. Afterwards, monthly flow (hm3)

and daily discharges (m3/s) were determined for each

river transect corresponding to a tree location. Cal-

culations took into account the existing ratio between

the drainage basin area upstream of Monte dos

Pachecos gauge station and the drainage basin area

upstream of each tree, considering precipitations in

them. Drainage basin area for each tree was defined as

the drainage area upstream from tree GPS position,

and it was created using Watershed Delineation Tools

toolbox script (http://arcscripts.esri.com/) upon a

30 m resolution Digital Elevation Model available

from ESRI-Portugal (www.arcgis.com). Finally, for

each tree, distance to source was calculated using tree

GPS position and river segment lengths from Portu-

guese National SIG Databases in ESRI� ArcGisTM 10.

Data processing

Wood samples processing

Increment cores and discs were air dried, sanded (with

progressively finer grades) to produce a flat and

polished surface where tree-ring boundaries were

easily identified under magnification. Tree-ring struc-

ture was visually examined under stereo-microscope.

Tree rings of all samples were visually cross-dated and

their ring-width measured with an accuracy of

0.01 mm using a linear table Lintab and the TSAP-

Win program (Rinn 2003). The accuracy of the visual

cross-dating and the existence of measurements errors

was examined using the program COFECHA (Holmes

1983). Trees younger than 25 years and showing

Table 1 Near and far trees characterization across study sites

Variable Near trees (n = 11) Far trees (n = 19)

Average Max Min Average Max Min

Height above water level (m) 0.8 1.5 0.2 2.1 3.5 2.0

Horizontal distance to active channel (m) 1.7 6.4 0.0 13.6 30 1.5

Flood width (m) 20.6 40 10 29.9 57 12.5

Diameter at breast height (cm) 32.4 47 20.2 40.3 77 21.7

Tree height (m) 13.3 17 7 14.8 20 9.5

Number of stems per tree 3 8 1 1.5 4 1

Tree age (years) 39 67 26 40.7 56 26

All field measurements were done in summer

Table 2 List and characteristics of climatic and hydrologic data sources used in this study

Station Latitude Longitude Altitude (m) Parameter Units Period

Alferce (30G/01UG) 37.333 -8.491 324 Monthly precipitation mm 1958–2009

Santana da Serra (28H/03UG) 37.502 -8.297 211 Monthly precipitation mm 1936–2009

Sao Barnabe (29I/01UG) 37.359 -8.164 249 Monthly precipitation mm 1964–2009

Sao Marcos da Serra (29G/02G) 37.360 -8.381 139 Monthly precipitation mm 1931–2009

Sobreira (30I/02UG) 37.300 -8.061 442 Monthly precipitation mm 1942–2009

Barragem do Arade (30G/03C) 37.238 -8.375 58 Monthly temperature �C 1962–2009

Monte dos Pachecos (30G/01H) 37.300 -8.467 55 Monthly flow, daily discharge hm3, m3/s 1961–2000

Stations are identified by their name and code at National Water Authority Information System SNIRH (http://snirh.pt)

Plant Ecol (2014) 215:233–245 237

123

correlations with the master chronology below 0.4

were excluded. In total, 30 trees were selected for the

further analysis.

Growth data processing

Trees were grouped into two classes in function of

their position in the floodplain before proceeding to

growth analysis. Trees growing lower and closer

relative to the active channel (\2 m height and\10 m

horizontal distance), where classified as ’near’ trees,

whereas the remaining studied trees (C2 m height,

C10 m horizontal distance) were classified as ’far’

trees. For each tree, a mean tree-ring series was

obtained by averaging all radii. To remove age-related

growth trends and competition effects a one-step

detrending was applied to each mean tree-ring series,

using the packages dplR (Bunn 2008) and detrendeR

(Campelo et al. 2012) from the R freeware program

(http://cran.r-project.org). A smoothing cubic spline

curve of 30 years length (50 % frequency cut-off) was

fitted to each individual ring-width series and detr-

ended the original series by calculating ratios. Auto-

regressive modelling was performed on the detrended

series. Finally, a residual chronology was obtained for

each class (’near’ and ’far’) by averaging residual

series using a biweight robust estimate of the mean to

reduce the influence of outliers (Briffa and Jones

1990). The expressed population signal (EPS) was

used to indicate how well a chronology represents the

growth signal of a perfect chronology (Wigley et al.

1984).

Data analysis

Growth curves

For each class, tree-ring width series (showing pith)

were aligned by cambial age and averaged to produce

a mean growth curve. Afterwards, these mean growth

curves were smoothed with a spline curve of 20 years

length (50 % frequency cut-off) to better illustrate the

variation of tree growth with cambial age and distance

to the active channel. These two age-aligned smoothed

curves are directly comparable and could be used to

compare the growth rates between floodplain posi-

tions. Repeated measures ANOVA was used to test the

null hypothesis of no differences in growth over time

among classes.

Climatic and hydrological signal

We investigated the climatic and hydrological signal

for both tree classes of geomorphic position, using

Pearson correlations between tree-ring width residual

chronologies (near and far) and monthly precipitation,

monthly mean temperature and monthly maximum of

daily discharge (Table 2).

Pointer years

Pointer years have long been used by dendrochronol-

ogists as a method to identify annual growth reactions

due to rapid changes in environment. A given year is

considered as a pointer year, when tree growth in that

particular year was significantly different from growth

in adjacent years. In the present study, we used the so-

called ’normalisation in a moving window’ method

proposed originally by Cropper (1979) to determine

pointer years statistically. This technique consists of

two steps: (i) normalisation of tree-ring width mea-

surements and (ii) calculation of event years to

identify pointer years. The standardization was per-

formed using a window of 5 years’ length according to

the formula:

Zi ¼ Xi � Mwð Þ=SDw;

where Zi is the standardized tree-ring width for the

year i, Xi is the tree-ring width for the year i, Mw is the

mean ring width within the window of 5 years length

and the SDw is the standard deviation of tree-ring

width within the window (5 years). Finally, a given

year was considered as pointer year when more than

70 % of the series (trees) of a species showed change

in the standardised tree growth greater than 10 %

(|Zi| [ 0.1). To determine how climatic and hydro-

logic factors influence alder growth, we related the

tree-ring growth during pointer years with tempera-

ture, and precipitation data during the current and

previous year and with hydrologic data (winter flow)

from the previous year.

Linear mixed models

Linear mixed-effects models were implemented using

the function lme from the R package nlme (Pinheiro

and Bates 2000) to model the relationship between

environmental variables and tree growth. This

238 Plant Ecol (2014) 215:233–245

123

modelling approach was selected because it enabled us

to include the sampling site 9 tree interaction as a

random effect, accounting for the hierarchical struc-

ture of our sampling design (trees nested within

sampling sites), and producing the appropriate error

terms of the explanatory variables in a single model.

For model selection, we took an information-theoretic

approach, using Akaike information criterion (AIC) to

compare a suite of competing models (Burnham and

Anderson 2002). The best model was selected using

the lowest AIC value from a set of candidates, and

alternate models were assessed using differences from

the minimum AIC (Di) and associated Akaike weights

(wi). The best model in each candidate set has the

lowest Di and highest weight. For each response factor

tested (residual growth values), we constructed a set of

candidate models that included all additive combina-

tions of the explanatory variables considered.

Results

General growth patterns

For the original 154 radii (60 trees) measured to

analyse tree growth, the mean ring width was 3.70 mm

(ranging from 0.07 to 21.77 mm), whereas the 30 trees

selected in the present study had a mean tree-ring

width of 4.01 mm (0.07 to 21.77 mm). Trees grew

slower at sites closer and lower located relative to the

active channel (‘‘near’’ trees) and faster at sites distant

from the active channel (‘‘far’’ trees). For the period

1960–2009, the mean tree-ring width of near and far

trees was 3.69 and 4.55 mm, respectively. This

difference is particularly clear for young trees.

According to the EPS value obtained for near and far

trees, 6 and 7 are the theoretical number of trees

needed to acquire an EPS value of 0.85, respectively.

Growth curves aligned by cambial age (25 trees

showing pith) showed that trends in annual increment

growth during the first 15 years of life were signifi-

cantly different (p = 0.03, F(1,40) = 5.083) for trees

growing in sites located in different position relative to

the active river channel (Fig. 2). The greatest absolute

range in growth between near and far sites is for young

(approx. 2–5 years) trees and the differences in growth

rate decrease with age, being practically null at age 15

(Fig. 2).

Climatic and hydrological signal

A significant negative correlation was found between

March maximum of daily discharge for both near

(r = -0.46, p \ 0.01) and far trees (r = -0.51,

p \ 0.01) annual growth. A similar correlation was

obtained between precipitation in March and annual

growth for both near (r = -0.37, p \ 0.05) and far

trees (r = -0.52, p \ 0.001). Additionally, trees

growing far from the river channel showed a signif-

icant negative correlation (r = -0.30, p \ 0.05)

between temperature in June and annual growth.

Pointer years

Four negative (1965, 1968, 1984 and 1996) and three

positive (1960, 1966 and 1994) pointer years were

detected for near trees, whereas far trees had four

negative (1968, 1981, 1996 and 1999) and four

positive (1966, 1967, 1970 and 2002) pointer years

(Fig. 3). Most of the pointer years are different

between near and far trees, only 1966, 1968 and

1996 were point years common two both groups of

trees (Fig. 3). Tree-ring width during pointer years

was not associated with climate data (temperature and

precipitation). Alder growth in pointer years was

associated with hydrologic regime. Hydrologic data

(both flow and discharge) from Monte dos Pachecos

station showed that the large floods corresponding to

return periods of 20 and 100 years (Rivaes et al. 2013)

occurred during the period 1961–2000. In particular,

average winter flow in the negative pointer years for

near trees (volume sum from October to April) was

ring

wid

th (

mm

)

0

1

2

3

4

5

6

7

8

9

10

cambial age (years)2 4 6 8 10 12 14 16 18 20 22 24

Far

Near

Fig. 2 Smoothed growth curves of mean raw ring-width series

of black alder trees aligned by cambial age for ’near’ (\2 m

height and \10 m horizontal distance to river active channel)

and ’far’ (C2 m height, C10 m horizontal distance to river

active channel)

Plant Ecol (2014) 215:233–245 239

123

found to be 74 % higher (258.598 hm3) than the

average winter flow for the period 1961–2000

(148.622 hm3).

Linear mixed models

Model selection using different combination of

dependent and explanatory variables showed that the

set of models for residual growth values in negative

pointer years for near trees [Y], depending on

hydrological (winter flow in negative pointer years

[Nnpy_V]) and geomorphological (height from chan-

nel, [Height_w]; and Flood width [Flood_W] vari-

ables were stronger than the null model (no

predictors). In particular, the results show that the

models including the predictor variable Height_w,

accounted for 80 % of the collective Akaike weight,

and the best model was 43 % likely given the

candidate set of models (Table 3). The sign of the

model parameters (Height_w [ 0) show that trees

located higher from water level where benefited in

terms of stem radial growth than trees located down

inside the active channel, particularly in years that

corresponded with higher return period floods (CT100;

Table 4).

1940 1950 1960 1970 1980 1990 2000 2010

Near

1940 1950 1960 1970 1980 1990 2000 2010

Far

Fig. 3 Raw ring-width

series of analysed samples

showing negative (red) and

positive (green) pointer

years for ’near’ (\2 m

height and\10 m horizontal

distance to river active

channel) and ’far’ (C2 m

height, C10 m horizontal

distance to river active

channel) black alder trees.

(Color figure online)

Table 3 Model comparison results, considering the following

variables: Y = average residual growth in negative pointer

years for near trees, X = height from channel, negative pointer

years flow, flood width. Akaike information criteria (AIC); Di

is the AIC difference of model i, calculated as the difference

between the AIC of model i and the AIC of the best model, wi

is Akaike weight of model i, given the set of models

Model AIC Di (-Di/2) exp(-Di/2) wi

m2 -4.505 0 0.000 1.000 0.429

m5 -3.055 1.45 -0.725 0.484 0.208

m7 -2.527 1.978 -0.989 0.372 0.160

m8 -1.093 3.412 -1.706 0.182 0.078

m1 -0.699 3.806 -1.903 0.149 0.064

m4 0.976 5.481 -2.741 0.065 0.028

m3 1.296 5.801 -2.901 0.055 0.024

m6 2.975 7.48 -3.740 0.024 0.011

240 Plant Ecol (2014) 215:233–245

123

Discussion

As the study site is located in the southern Iberian area,

under Mediterranean climate with a marked seasonal

and interannual variability (Gasith and Resh 1999),

and given that we sampled black alder trees at the limit

of its distribution range, we expected that both climate

and local environmental conditions driving water

availability would strongly shape riparian signatures.

Stem radial growth of A. glutinosa growth was

affected by climate to some degree, but patterns of

radial growth were mainly influenced by hydrologic

regime and geomorphology of the channel, and by the

relative position of the tree in relation to the active

channel. Previous works suggested that local hydrol-

ogy (Rodrıguez-Gonzalez et al. 2008) associated with

the edaphic factors (Rodrıguez-Gonzalez et al. 2010)

can be the major drivers for distribution and growth of

wetland trees in southwestern Iberian Peninsula.

However, a temporal analysis of hydrological data

series is imperative to contrast tree responses to flood

intensity and frequency (Ballesteros et al. 2011). In the

studied hydrographic basin, A. glutinosa was only

naturally growing along downstream reaches, where

Odelouca river receives inflow from two tributaries

having their catchments at Monchique mountainous

system. The annual precipitation (1,000–1,400 mm;

http://sniamb.apambiente.pt/webatlas/) in the head-

waters of those tributaries seems to have ensured the

maintenance of the necessary soil humidity for A.

glutinosa trees growing and completing their life

cycle. Alnus glutinosa forms two well-developed

physiological root types, a surface nutritional system

and a deep-growing system (McVean 1954). Also, soil

texture in the floodplain of the study area is loam,

composed of 23 % clay, 40 % Lime and 37 % sand,

(Rivaes et al. 2013; http://www.iiama.upv.es/

RipFlow/), providing good aeration (Rodrıguez-Gon-

zalez et al. 2010) and enough water retention (Jo-

hansson 1999) for A. glutinosa requirements. For the

larger part of the year, trees in this river probably reach

subsurface flow and groundwater table with their deep

roots (Eschenbach and Kappen 1999) so they would be

able to maintain water support. Nevertheless, the

negative correlation revealed on far trees growth to

June temperature suggests that high temperatures

during the peak of growth could decrease tree growth

due to water loss by evapotranspiration, being this

more evident for trees located higher (far trees) from

the phreatic level. This result is in accordance with the

high transpiration rates observed for this species (Es-

chenbach and Kappen 1999).

Hydrologic variables proved to be the most likely

drivers of growth reduction in negative pointer years.

Floods inducing hypoxic conditions are known to

constrain tree growth in woody plants (Kozlowski

1997). Negative pointer years seem to occur during the

next growing season after extraordinary large floods,

but we admit that the suppression of tree growth

should not be attributed to the effect of flooding-

induced hypoxic conditions. The duration of the

largest floods registered during the studied period in

this river ranges from some hours to days, a common

pattern on arid regions, where floods use to be brief

(Yair and Kossovsky 2002). An example is the great

flood that occurred on 10th March of 1996 that reached

980 m3/s at Monte dos Pachecos station in a single

day. This discharge is close to the 100 year flood

(1050 m3/s) for this drainage basin (Rivaes et al.

2013). Alnus glutinosa is a relatively tolerant species

to waterlogging (Niinemets and Valladares 2006)

especially, if it occurs outside the vegetation growing

season (Iremonger and Kelly 1988), therefore, the

effects of those short winter hypoxic conditions on tree

growth would be negligible. Instead, the observed ring

width reduction after extreme hydrologic events might

be related to mechanical damage on tree stems and

roots. Firstly, alder wood is much softer than many

other Iberian riparian trees requiring relatively small

impact energies to generate wood scars (Ballesteros

Table 4 Model parameters (explanatory variables), significance (p), slope and number of model parameters (including intercept) for

the best three alternative models having Di \ 2 (m2, m5, m7)

Model Parameter p Slope Parameter p Slope n Parameters

m2 Height_w 0.024 [0 – – – 2

m5 Height_w 0.021 [0 Nnpy_V 0.488 \0 3

m7 Height_w 0.031 [0 Flood_Width 0.890 \0 3

Significant values of p \ 0.05 are displayed in bold

Plant Ecol (2014) 215:233–245 241

123

et al. 2010). Secondly, growth reduction is likely to be

driven indirectly by uprooting due to flash flood

impacts of flow and debris. After an intense flood,

trees may suffer a reduction of the effective absorbing

surface being forced to divert resources to rebuild

damaged root systems, thus adjusting root-shoot

allocation in the following growing season. Uprooting

resistance in trees is related to root architecture

including root depth and length (Stokes et al. 1996).

As roots are usually more flexible than the soil,

physical stress causes the roots to bend or stretch and

eventually to break proximally before the soil/root

connection is disrupted distally (Read and Stokes

2006; Karrenberg et al. 2003). Additionally, although

A. glutinosa is a diffuse porous species, thus presum-

ably less susceptible to cavitation than ring-porous, its

roots are vulnerable to drought (Hacke and Sauter

1996), due to high transpiration rates (Eschenbach and

Kappen 1999). Uprooting might induce soil/root

disconnection causing drought-like embolism that

could seriously limit tree function and thus growth

reduction.

Geomorphological position of the trees seemed to

modulate the effect of floods in tree response, on both

adult and young trees. For adult trees, the most

contributing variable to stem radial growth in negative

pointer years was height from active channel, having a

positive effect on near trees. For young trees, average

growth was negatively affected by their proximity, and

their lower position inside the active channel. One

critical factor for seedling survival in riparian species

is the susceptibility to desiccation during summer

droughts (Cooper et al. 1999; Johnson 2000; Stella and

Battles 2010). However, when growth trends were

analysed by cambial age, thus independently of the

calendar years, ’far’ trees, those located at the

floodplain area, displayed higher annual growth rate

at the younger life stages (1–15 years) than ’near’

trees, those growing inside the active channel. ’Near’

trees likely suffer more with the erosion and burial by

sediments and coarse substrates provoked by flow

pulses (Johnson 2000). In this river, during ordinary

floods (each 1.5 years) water level reaches 3–4 m

height at Monte dos Pachecos gauge station, and it

becomes greater in many deep vee sectors of the

valley. Frequent flood impact together with sediments

and debris could affect crown area of shorter trees

(Johansson 1999), particularly when they are growing

down inside the channel. In a study comparing root

anchorage among Alnus incana, Salix elaeagnos and

Populus nigra saplings, Karrenberg et al. (2003) found

that the uprooting resistance and the critical stress (the

force per unit area that is necessary to induce root

system failure) for Alnus was minimum and signif-

icantly inferior than for Salicaceae. In fact, Alnus

species generally show fewer adaptations than Salic-

aceae to the levels and frequency of disturbance

conditions that characterize the active channel of

rivers, colonizing preferably more stabilized sub-

strates (Karrenberg et al. 2002). The results obtained

for both adult and young trees; reinforce the idea that

local soil and hydrologic conditions were the main

drivers of A. glutinosa growth trends in Odelouca river

basin.

Conclusions

The present study provided new findings to understand

how physical stressors interact with the hydrologic

variability already occurring in the Mediterranean

area. In this paper we showed that the hydrological

variables are useful predictors of Alnus growth, and

that the growth patterns changed along a narrow strip

between the upper limit of water supply and the lower

maximum disturbance. As result of climate changes,

extreme events like droughts and floods are expected

to increase intensity in the near future (Giorgi and

Lionello 2008; Nunes et al. 2009). These projections

will likely alter the habitats occupied by certain

riparian formations less adapted to drought or peak

floods potentially leading to a decrease in species

diversity and unbalanced distribution of ages in the

remaining (Rivaes et al. 2013), threatening the long-

term sustainability of their populations (McCauley

et al. 2013). A combined study of ecological and

evolutionary strategies that would enable species

adaptation to climate change is mandatory for future

research (Klausmeyer and Shaw 2009). The identifi-

cation of local climatic refugia or patches of core

habitat on the local scale even in regionally unfavour-

able areas (Lepais et al. 2013) represents an additional

option to focus management resources, since their

potential to maintain relict populations will also

enable conservation of seed sources from local

provenances into the future (Hampe and Jump 2011).

Given the ecologic (Roy et al. 2007) and economical

(Claessens et al. 2010) importance of A. glutinosa, and

242 Plant Ecol (2014) 215:233–245

123

the potential for rapid changes in the distribution of

this species, the identification of those areas mostly at

risk and the adequate management of high priority

alder populations will become progressively more

important over coming years, as will be necessary the

development of appropriate monitoring and manage-

ment strategies.

Acknowledgments This work was supported by the IWRM

Era-Net Funding Initiative through the RIPFLOW Project (ERA-

IWRM/0001/2008). Portuguese Ministry for Science and

Technology through Fundacao para a Ciencia e a Tecnologia-

FCT funded post-doctoral research Grants for Patricia Marıa

Rodrıguez-Gonzalez (SFRH/BPD/47140/2008) and Filipe

Campelo (SFRH/BPD/47822/2008). Rui Rivaes benefited from

a PhD Grant sponsored by Universidade Tecnica de Lisboa. The

authors especially thank Mario Tavares from the Portuguese

National Institute of Biological Resources (INRB) for logistics

support. We would like to thank Aguas do Algarve S.A. and

Imobiente Lda. for giving us permission to access and to collect

the sample trees in the dam area of Odelouca. Logistica Florestal

provided chainsaw operators for tree felling. We are grateful to

Mario Santinho for his help during fieldwork.

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