PHYSIOLOGICAL ECOLOGY - ORIGINAL PAPER
Root traits explain different foraging strategies
between resprouting life histories
Susana Paula • Juli G. Pausas
Received: 4 May 2010 / Accepted: 29 September 2010
 Springer-Verlag 2010
Abstract Drought and fire are prevalent disturbances in
Mediterranean ecosystems. Plant species able to regrow
after severe disturbances (i.e. resprouter life history) have
higher allocation to roots and higher water potential during
the dry season than coexisting non-resprouting species.
However, seedlings of non-resprouters have a higher sur-
vival rate after summer drought. We predict that, to coun-
teract their shallow-rooting systems and to maximize
seedling survival, non-resprouters have root traits that confer
higher efficiency in soil resource acquisition than resprou-
ters. We tested this prediction in seedlings of less than
1.5 months old. We select 13 coexisting woody species
(including both resprouters and non-resprouters), grew them
in a common garden and measured the following root traits:
length, surface, average diameter, root tissue density (RTD),
specific root length (SRL), surface:volume ratio (SVR),
specific tip density (STD), tip distribution in depth, internal
links ratio (ILR), and degree of branching. These root traits
were compared between the two resprouting life histories
using both standard cross-species and phylogenetic-
informed analysis. Non-resprouters showed higher SRL and
longer, thinner and more branched laterals, especially in the
upper soil layers. The external links (i.e. the most absorptive
root region) were also more abundant, longer, thinner and
with higher SVR for non-resprouters. The results were
supported by the phylogenetic-informed analysis for the root
traits most strongly related to soil resource acquisition (SRL,
SVR and branching pattern). The seedling root structure of
non-resprouters species allows them to more efficiently
explore the upper soil layer, whereas seedling roots of
resprouters will permit both carbon storage and deep soil
penetration.
Keywords Drought  Fire  Mediterranean-type
ecosystems  Root branching  Root morphology
Introduction
Resource availability and disturbances have been regarded
as the major factors driving plant functioning (Grime 1979;
Westoby 1998; Lavorel and Garnier 2002), and traits
associated with these two factors define the range of
strategies for plant coexistence (Ackerly 2004). In Medi-
terranean conditions, the topsoil water content during the
dry season is drastically reduced, sometimes to less than
1% (Lossaint and Rapp 1978; Puigdefa´bregas et al. 1996;
Martı´nez-Vilalta et al. 2003; Padilla and Pugnaire 2007),
which is very close to the permanent wilting point esti-
mated for xerophytes (Larcher 1995). Consequently, plant
traits related to water uptake are of paramount importance
for explaining plant persistence in Mediterranean-type
ecosystems (Valladares et al. 2004). Moreover, the pro-
ductivity and aridity levels of Mediterranean ecosystems
provide dry fuel loads that promote recurrent fires during
Communicated by Fernando Valladares.
Electronic supplementary material The online version of this
article (doi:10.1007/s00442-010-1806-y) contains supplementary
material, which is available to authorized users.
S. Paula
CEAM Centro de Estudios Ambientales del Mediterra´neo,
Charles R. Darwin 14, Parc Tecnolo`gic, 46980 Paterna,
Vale`ncia, Spain
J. G. Pausas (&)
CIDE Centro de Investigaciones sobre Desertificacio´n (CSIC),
Camı´ de la Marjal s/n Apartado Oficial, 46470 Albal,
Vale`ncia, Spain
e-mail: juli.g.pausas@uv.es
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Oecologia
DOI 10.1007/s00442-010-1806-y

the dry season (Pausas 2004; Pausas and Bradstock 2007).
There are two main mechanisms for post-fire persistence at
population level coexisting in Mediterranean-type ecosys-
tems: (1) the regeneration of the above-ground biomass
after being 100% scorched (i.e. resprouting), and (2) the
recruitment of new individuals from a fire-resistant seed
bank (Pausas et al. 2004). Each of these mechanisms is
strongly associated with vegetative and reproductive
functional traits, and define two contrasted life histories
(Keeley and Zedler 1978; Pausas et al. 2004; Pausas and
Verdu´ 2005): resprouters and non-resprouters.
Resprouting species need to allocate more resources to
below-ground organs, where energetic reserves are stored
to sustain regrowth (e.g., Bowen and Pate 1993; Schutz
et al. 2009). Consequently, they show lower shoot:root
ratio than coexisting non-resprouting species (Pate et al.
1990; Bell et al. 1996; Verdaguer and Ojeda 2002; Silva
and Rego 2004; Schwilk and Ackerly 2005); this allows
resprouters access to more reliable deep water throughout
the year (Hellmers et al. 1955; Davis et al. 1998; Bell et al.
1996; Silva et al. 2002; Ackerly 2003; Guerrero-Campo
et al. 2006). In contrast, non-resprouting species are sub-
jected to seasonal changes in water availability because of
their smaller and shallower roots. In fact, the decreasing
water potential of non-resprouters during the dry season is
seldom observed in resprouting species (Davis et al. 1998;
Clemente et al. 2005; Gratani and Varone 2004; Jacobsen
et al. 2007; Pratt et al. 2007a). As a consequence of
exposure to stronger seasonality, non-resprouters have
drought resistance mechanisms. At leaf level, they have
higher water use efficiency and leaf mass area ratio
(Ackerly 2003; Knox and Clarke 2005; Paula and Pausas
2006; Pratt et al. 2007a). For roots and stems, the low
vulnerability to cavitation shown by non-resprouters has
been described as a mechanism for water stress tolerance in
both adults (Davis et al. 1998; Jacobsen et al. 2007; Pratt
et al. 2007a) and seedlings (Pratt et al. 2008). Higher water
stress tolerance at the seedling stage is specially relevant in
species in which population persistence relies exclusively
on seedling recruitment (non-resprouters) and explains
their higher survival rates under summer drought (Keeley
and Zedler 1978; Zammit and Westoby 1987; Frazer and
Davis 1988; Davis et al. 1998; Enright and Goldblum 1999;
Pratt et al. 2008). Furthermore, seedlings of non-resprou-
ters show greater water transport efficiency (Pratt et al.
2010) allowing for faster growth and earlier maturity
(Pausas et al. 2004). The lack of evidence relating water
stress resistance and rooting depth in seedlings (Frazer and
Davis 1988; Pratt et al. 2008) suggests that the correlation
between the hydraulic architecture and the life history
constitute a functional syndrome appearing early in plant
development and not as a consequence of differences in
water availability at the seedling stage.
Root structure is strongly correlated with physiological
traits responsible of the plant’s water status (Herna´ndez
et al. 2010), and it has been suggested as a promising
candidate for explaining the differences in hydraulic
architecture between life histories in seedlings (Pratt et al.
2010). One of the most relevant root traits related with soil
exploration and resource uptake is the specific root length
(SRL; the root length achieved per unit of root biomass
invested), which in turn depends on root diameter and/or
tissue density (Wright and Westoby 1999; Nicotra et al.
2002). Roots with high SRL have a high surface:volume
ratio (SVR) for the same carbon investment, and this
maximizes the root–soil interface and hence the root
absorption potential (Larcher 1995). Moreover, thin roots
with high SRL offer less resistance to the radial flow of
water, thus increasing radial conductivity (Huang and
Eissenstat 2000). In addition, plants with high SRL tend to
show higher root hydraulic conductance per leaf unit sur-
face area (Pema´n et al. 2006) or per stem cross-section area
(Herna´ndez et al. 2010). Consequently, plants with high
SRL (considering either the whole root system or only fine
roots) show high uptake rates of water (Eissenstat 1991),
nitrogen (Reich et al. 1998) and phosphorus (Comas et al.
2002).
Intensively branched roots, which have abundant root
tips, are highly efficient for water transport because of their
low overall distance from the tips to the root crown (Fitter
1986). Tips are the root parts with the highest absorptive
capacity due to the presence of root hairs and non-lignified
tissues, whereas the main functions of older roots are
anchorage, storage and transport (Fahn 1985; Wells and
Eissenstat 2003; Guo et al. 2008; Valenzuela-Estrada et al.
2008). Consequently, the number of tips per unit of root
biomass (i.e. specific root tip density; STD hereafter) is a
relative measure of allocation to the most absorptive tis-
sues, which is particularly relevant in woody plants.
Our hypothesis is that, to counteract their lower root
allocation and maximize seedling survival, non-resprouting
species have root traits conferring higher efficiency in soil
resource acquisition than coexisting resprouters. Specifi-
cally, we predict that, in comparison to the root system of
resprouters, the root system of non-resprouters should
have: (1) longer and thinner roots and higher surface area
per unit of root biomass (i.e. higher SRL and SVR values)
and/or (2) more tips (per unit of root biomass) and higher
branching. To test our predictions, we grew seedlings of
several Mediterranean woody species in a common garden,
measured their root traits, and compared them between
resprouting abilities. We used a common garden approach
to minimize environmental heterogeneity that could affect
root structure (Goss 1977; Padilla et al. 2007). Since root
traits are strongly affected by the species’ phylogenetic
affiliation (Fitter and Stickland 1991; Nicotra et al. 2002;
Oecologia
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