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Restoration interventions produce opposite and non-additive benefits on tree establishment in degraded forest clearings

Abstract

Abstract The natural regeneration of forests is declining in human modified landscapes and overcoming ecological barriers to seedling establishment is paramount to its restoration. This study focus on two common forest regeneration barriers: excessive sun exposure and low-quality soils. A degraded clearing with eroded and compacted soils within a disturbed oak forest in Mexico was chosen, and 20 experimental plots in a randomized factorial block design were set up to test seedling performance in artificial shade and in forest topsoil that was transferred from a nearby remnant forest, as well as a combination of both. We sowed 400 acorns from two oak species (Quercus eduardii and Q. viminea) and monitored the emerging seedlings for 63 months. Our results confirm different survival and growth rates between species, ontogenetic stages, and environmental micro-conditions. The effect of artificial shade on seedling performance was positive in weathered soil but negative or neutral in transferred forest soil. Restoration interventions did not have additive benefits; seedling performance was improved by both restoration interventions applied separately though was not further enhanced when both actions were combined. Both species had different mechanisms to cope with water stress, which resulted in different photosynthetic rates under full sun. Trade-offs resulted in different life stages that were more enhanced by different restoration strategies; survival and growth was most enhanced by applying artificial shade or transferring forest topsoil respectively. Restoration precisionists may prioritize seedling survival in harsh conditions and growth in less severe degraded sites or apply interventions sequentially over time.
SETBACKS AND SURPRISES
Restoration interventions produce opposite and
non-additive benets on tree establishment
in degraded forest clearings
Maximino B. Rivas Rivas1, David Douterlungne2,3 , Lorena G
omez Aparicio4,
Ernesto I. Badano1, Jorge Alberto Flores Cano5
The natural regeneration of forests is declining in human-modied landscapes and overcoming ecological barriers to the seed-
ling establishment is paramount to its restoration. This study focus on two common forest regeneration barriers: excessive sun
exposure and low-quality soils. A degraded clearing with eroded and compacted soils within a disturbed oak forest in Mexico
was chosen, and 20 experimental plots in a randomized factorial block design were set up to test seedling performance in the
articial shade and in forest topsoil that was transferred from a nearby remnant forest, as well as a combination of both. We
sowed 400 acorns from two oak species (Quercus eduardii and Q. viminea) and monitored the emerging seedlings for 63 months.
Our results conrm different survival and growth rates between species, ontogenetic stages, and environmental micro-conditions.
The effect of articial shade on seedling performance was positive in weathered soil but negative or neutral in transferred forest
soil. Restoration interventions did not have additive benets; seedling performance was improved by both restoration interventions
applied separately though was not further enhanced when both actions were combined. Both species had different mechanisms to
cope with water stress, which resulted in different photosynthetic rates under full sun. Trade-offs resulted in different life stages
that were more enhanced by different restoration strategies; survival and growth were most enhanced by applying articial shade
or transferring forest topsoil, respectively. Restoration practitioners may prioritize seedling survival in harsh conditions and
growth in less severe degraded sites or apply interventions sequentially over time.
Key words: conicting life stages, Forest regeneration, shade, topsoil translocation, Quercus
Implications for Practice
Restoration intervention to enhance seedling establish-
ment rates can have opposing effects according to spe-
cies, seedling life-stage, and micro-environmental
conditions.
Combining different restoration interventions does not
necessarily produce additional improvements for seed-
ling establishment.
The emergence and survival of oak seedlings in a
degraded clearing were more increased by articial shade
than by forest topsoil transference.
Seedlings grew faster in transferred forest topsoil but suf-
fered higher mortality rates.
Identifying interactions between different barriers to the
seedling establishment is important for understanding
tree regeneration dynamics.
Introduction
Forest cover decreased by 185 million hectares globally
between 2000 and 2010 (FAO 2015), and many of the remaining
forests are fragmented and degraded (Hansen et al. 2013). One
and a half billion people, 74% of whom live in poverty, depend
on degraded land for subsistence and are forced to use sub-
optimal farming and land management practices that further
degrade the landscape (IPBES 2018). These forests have a
severely modied structure, function and plant diversity
(Chazdon et al. 2009) and are often reduced to scattered frag-
ments immersed in a mosaic matrix with patches of different
land uses (Taubert et al. 2018). Restoring impacted patches in
human-modied landscapes (HML) is key to sustaining forest
biodiversity and ecosystem functioning (Chazdon et al. 2016;
Author contributions: MBRR, DD conceived and designed the research and wrote the
rst draft of the manuscript; DD administrated funding; all authors contributed to
editing and guiding the manuscript.
1
Department of Environmental Sciences, Instituto Potosino de Investigaci
on Cientíca
y Tecnol
ogica A.C. (IPICyT), Camino a la Presa San José No. 2055. Col. Lomas 4ta
Secci
on, C.P. 78216. San Luis Potosí, S.L.P., Mexico
2
Department of Environmental Sciences, CONACYT Research FellowInstituto
Potosino de Investigaci
on Cientíca y Tecnol
ogica A.C. (IPICyT), Camino a la Presa
San José 2055. Col. Lomas 4ta secci
on CP. 78216. San Luis Potosí S.L.P., Mexico
3
Address correspondence to D. Douterlungne, email david.d@ipicyt.edu.mx
4
Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Av. Reina
Mercedes 10, E-41012, Sevilla, Spain
5
Facultad de Agronomía y Veterinaria, Universidad Aut
onoma de San Luis Potosí,
Km. 14.5 Carretera San Luis-Matehuala, Apartado Postal 32, Soledad de Graciano
S
anchez, C.P. 78321, San Luis Potosí, S.L.P., Mexico
© 2021 Society for Ecological Restoration.
doi: 10.1111/rec.13539
Supporting information at:
http://onlinelibrary.wiley.com/doi/10.1111/rec.13539/suppinfo
Restoration Ecology 1of9
Arroyo-Rodríguez et al. 2020), which in turn is essential for the
wellbeing of rural populations (Aronson & Alexander 2013;
Brancalion et al. 2013).
Managing and restoring forest ecosystems in landscapes,
such as these is challenging as succession may be arrested and
current environmental conditions may differ from the niche
requirements of the local climax vegetation (Arroyo-Rodríguez
et al. 2017). In particular, germination and the establishment of
tree seedlings can be severely limited by both above- and
belowground factors (G
omez-Aparicio et al. 2005; Badano
et al. 2015). Aboveground, high light levels in clearings cause
photo-inhibition in shade-tolerant seedlings due to the inability
of their photosynthetic apparatus to dissipate the excess light
energy. Seedlings exposed to high levels of solar radiation often
suffer increased mortality and/or deformed growth (Lambers
et al. 2008). In addition, low soil and atmospheric moisture in
full sun microsites are often critical limiting factors for plant
growth to which seedlings respond with functional adaptations,
such as thickening their leaves to reduce foliar transpiration
(Lambers et al. 2008). Natural or articial shade provided by
nurse plants or shade cloths is known to improve germination
and the overall seedling performance of tree species that
are intolerant to drought and full sun exposure (Badano
et al. 2009, 2011). A common restoration technique in such
sites is the planting of seedlings in the articial or natural
shade (Rey-Benayas et al. 2005; Badano et al. 2011; Gonz
alez-
Salvatierra et al. 2013).
Furthermore, belowground factors in human-made clearings
also challenge plant growth. Vegetative nutrient uptake in lands
previously used for agriculture or cattle breeding is often ham-
pered due to depleted and compacted soils with few nutrients,
low water retention capacity, and impoverished microbial com-
munities (Foley et al. 2005). A restoration intervention that is
frequently applied in sites that are completely deprived of their
soilsuch as abandoned minesconsists of transferring topsoil
layers from healthy ecosystems to the target sites. This type of
transfer implies introducing soil nutrients, organic matter,
microbial communities, and plant propagules from the donor
site (Rivera et al. 2014; Douterlungne et al. 2018).
In eld conditions, above- and belowground degrading fac-
tors interact in complex ways with other micro-environmental
conditions and form a complex interaction of multiple barriers
whose impact on forest regeneration is still poorly understood
(Kabeya et al. 2003; Osone et al. 2008; Arosa et al. 2015).
Therefore, restoration interventions that aim to tackle an individ-
ual barrier may not always be successful in enhancing tree estab-
lishment. In addition, tree species pass through different life
stages from germination to adult tree (Schupp 1995). Previous
studies suggest that habitat requirements vary across the differ-
ent stages (Rousset & Lepart 2000; Leverkus et al. 2016). This
process, known as conicting life stages,challenges the
design of restoration strategies as germination, survival, and
growth may require different restoration interventions. In partic-
ular, the transition from seed to seedling represents a bottleneck
for spontaneous regeneration (Pérez-Ramos et al. 2012).
Oak forests are a common dominant climax system in the north-
ern hemisphere and tropical mountainous regions. These forests
stand out for their functionality and diversity (Nixon 2006). They
provide a habitat for a vast number of epiphytic and understory
plants, while acorns serve as an important food source for most
forest-dwelling granivores and regulate populations of higher pred-
ators (McShea 2000). However, many oak forests in HML suffer a
regeneration decit that undermines their long-term persistence
(Urbieta et al. 2011; Pérez-Ramos et al. 2012; Ib
añez et al. 2017;
Perea et al. 2017).
Several strategies have been tested with varying degrees of
success to improve oak seedling establishment in impacted land-
scapes, including transplanting seedlings beneath nurse shrubs
(Badano et al. 2016; Rivas-Rivas et al. 2017), articial shade
structures (Gonz
alez-Salvatierra et al. 2013), or transferring
top soil from nearby healthy systems (Douterlungne et al.
2018). Although seedling establishment in eld conditions is
mostly hindered in the long term by the interaction of several
barriers, restoration studies generally focus on short periods
and a single stressor. Hence, little information is available
regarding how the impact of certain barriers on tree regeneration
varies across different life stages or how these barriers interact
with other environmental conditions.
In this study, we assessed how topsoil translocation and arti-
cial shade, and a combination of these as restoration interven-
tions, may enhance oak seedling establishment in tropical
HML. We used 63 weeks monitoring period to address the fol-
lowing questions: (1) Is oak seedling establishment in an HML
more enhanced by improving poor soil conditions or by reduc-
ing full sun exposure? (2) Does combining two restoration inter-
ventions enhance oak seedling establishment more than when
each intervention is applied separately? (3) Does the outcome
of a particular restoration intervention changes according to
seedling life stage and species?
Methods
Study Area
The study took place in a disturbed oak forest located in the state
of San Luis Potosí, Central Mexico (2154046.400Nand
10021037.900W, 1,773 m asl). The disturbance consists of freely
browsing cattle, the extraction of non-timber products, and clear-
ing sites for agricultural use. The resulting landscape is a mosaic
matrix of degraded patches with bare ground immersed in pri-
mary forest remnants. The mean annual temperature is 16.3C
and annual precipitation averages 732.9 mm with a rainy season
between June and November, followed by a dry season with less
than 20 mm per month (Fern
andez-Eguiarte et al. 2012). Forest
soils are shallow lithosols covered by a humus-rich topsoil of
approximately 1015 cm deep (Vargas-M
arquez 1984) and a lit-
ter layer up to 1 m deep. Local dominant oak tree species in forest
parches include Quercus eduardii Trel., Q. viminea Trel. and
Q. resinosa Liebm. Our experimental site is located in a clearing
with a 1015slope facing North and contains compacted weath-
ered soil without organic matter and high rainwater run-off. This
soil, locally known as Tepetate,is a common result of pro-
longed agricultural use on hillsides and frequently remains for
decades with little recolonizing vegetation.
Restoration Ecology2of9
Interacting barriers for seedling establishment
Experimental Design
We followed a randomized block design by placing 20 circular
experimental units of 0.64 m
2
each, which we fenced with
90-cm-tall wire mesh (13 mm opening) to exclude small herbi-
vores and granivores. Each experimental unit was divided into
10 equal pie sections where we randomly located one acorn
from each of the two focal oak species in each section, ending
up with 20 acorns per experimental unit or 400 seeds over the
whole experimental area. One of the following restoration inter-
ventions was applied within each experimental unit: (1) articial
shade; (2) forest topsoil transference; (3) combined forest top-
soil transference +articial shade; and (4) control (hereafter
abbreviated as shade,”“soil,”“shade +soiland control,
respectively). Each treatment included ve replicates (blocks),
and shaded experimental units were covered with 50% shade-
cloth. The forest soil had higher nutrient availability than the
degraded soil (Table 1). Forest topsoil transference treatment
consisted of removing the upper 10 cm at ve different sites
(approximately 5 m
2
each) from the adjacent forest and mixing
thoroughly to homogenize the substrate. The forest topsoil
included three different layers: (1) forest litter or dried whole
leaves; (2) decomposing litter; and (3) mineral soil particles with
decomposed organic matter. We maintained these three layers
by removing and mixing each layer separately and adding them
in approximately the same proportions as in the donor site. The
experimental units receiving topsoil were previously excavated
to a depth of 10 cm; this depth was chosen based upon the min-
imum amount of transferred topsoil necessary to enrich the
donor site with sufcient soil microbial activity and nutrients
(Rivera et al. 2014). The upper 10 cm of soil in all experimental
units were mechanically disturbed with a pickaxe to standardize
compaction and aeration.
Species Selection and Acorn Management
We selected Q. eduardii Trel. and Q. viminea Trel. based upon
local abundance and presence of acorns during the experimental
setup. Both species are endemic to Mexico and belong to the
Lobatae section (Sab
as-Rosales et al. 2015). Both are sub-
deciduous species associated with igneous and sedimentary
soils and are considered typical of intermediate successional
stages. Between July and August 2015, we collected acorns
beneath the canopies of a minimum of ve parent trees for each
species. The acorns were disinfected using a 10% chlorine solu-
tion and stored at 4C to delay their germination. Two days
before sowing, we applied the buoyancy test to discard non-
viable acorns (Gribko & Jones 1995; Morina et al. 2017). Viable
acorns were pre-hydrated for 2448 hours in water at room tem-
perature to standardize relative water content in all acorns and
reduce experimental bias. We planted the acorns at 2 cm depth
in all experimental units on September 4, 2015.
Soil Analyses
For each experimental treatment, we collected ve 20 cm soil
cores of 100 g each from which we retained a 400 g compound
sample. These samples were taken to the laboratory, where we
determined soil texture and pH using the Bouyoucos hydrome-
ter method and electrometric procedures, respectively. We
quantied soil organic matter content with the Walkley and
Black protocol (Salehi et al. 2011), while the ammonium ace-
tate/silver thiourea method was used to assess exchangeable
cations. Finally, we determined the soil content of nitrogen
(NH
3
and NO
4+
separately) and total phosphorus using
colorimetric methods (Pansu & Gautheyrou 2006).
Evaluation of Seedling Performance and Environmental
Conditions
Emergence, survival, and growth were monitored biweekly dur-
ing the rst 2 months after the experimental setup, then monthly,
bimonthly, and quarterly during the rst, second, and third
growing years, respectively. Seedlings were registered as dead
when aerial organs had completely wilted and snapped upon
touching, while seedlings that resprouted afterward were regis-
tered as alive during the whole experiment. Seedling height
was recorded as the maximum vertical distance between the soil
and the highest shoot apex. Basal stem diameter was registered
at 1 cm from ground level. As the soil level presented small
oscillations after rain events, we marked basal measuring points
with liquid corrector ink. Reductions in height or diameter were
common due to the partial wilting of seedlings during hot and
dry months.
We registered several variables to quantify plant stress. In
February 2019, we randomly selected three surviving seedlings
with at least three complete and mature leaves in each experi-
mental unit. We registered chlorophyll uorescence to estimate
the effective quantum yield of photosystem II (Φ
PSII
) with a
chlorophyll uorometer (opti-sciences) on sunny days between
11:00 and 13:00 hours. In May month of the same year, we
Table 1. Physicochemical properties of forest and weathered soil. P, phosphor; NH
4
, ammonium; NO
3
, ammonium nitrates; Na, sodium; K, potassium; Ca,
calcium; Mg, magnesium.
Exchangeable bases Cation exchange capacity
Soil sample
Soil
moisture (%)
Organic
matter (%)
pH
(mg kg
1
)P
NH
4
(mg kg
1
)NO
3
Na
(mg kg
1
)
K
(mg kg
1
)
Ca
(mg kg
1
)
Mg
(mg kg
1
)
NH
4
(mg kg
1
)
cmol
(NH
4
/kg)
Forest soil 10.4 8 7.11 18.3 3.6 4.8 39.7 107.8 700.4 121 1753.2 9.7
Weathered
soil
3.5 2.2 5.05 2.3 1.7 0.4 12.4 77 96 40.5 534.3 3
Restoration Ecology 3of9
Interacting barriers for seedling establishment
harvested those leaves and stored them in hermetically sealed
plastic bags placed in ice to prevent water loss. The specic leaf
area (SLA) was then recorded at a maximum of 3 hours after har-
vesting with an LI-COR, LI-3000C portable area meter. SLA
changes with environmental variables (Dwyer et al. 2014) and
correlates closely with the plants relative growth rate (Osone
et al. 2008). Therefore, SLA is considered as an important trait
to indicate the tness of species in their environment, especially
for saplings growth under high light such as in our experimental
site (Sterck et al. 2006; Poorter et al. 2009). Percent water
content (PWC) was used as a surrogate of the water status of
seedlings in the eld like a determinant of metabolic activity
and leaf survival (Sinclair & Ludlow 1985; Ogburn &
Edwards 2012), it correlates negatively with water stress and
the water potential of the xylem before dawn (Ψpd) (Chirino
et al. 2011). This variable was calculated based upon biomass
loss: PWC =(Fb Db)/Fb where Fb is fresh biomass and Db
is dry biomass. Leaves were dried in plant presses placed into
a ventilated stove at 60C until reaching constant biomass
(about 72 hours).
As for environmental conditions (Figs. S1S3), we registered
volumetric soil water content in each experimental unit with a
time-domain reectometer probe (Field Scout TDR 300, Spectrum
Technologies) at 7.6 cm soil depth. Soil moisture values were aver-
aged per experimental unit based upon three random point measure-
ments taken around noon during 18 monitoring events. Average
atmospheric humidity and temperature were registered each
60 minutes with minimum two data-loggers per treatment (HOBO
U23, ONSET Computer Corporation, U.S.A.) at 100 cm height.
Statistical Analyses
We estimated emergence and survival functions using nonpara-
metric stepwise KaplanMeier curves (Kaplan & Meier 1958)
and compared treatments with Cox Proportional hazards
models. Overall model signicance was evaluated with likeli-
hood ratio tests or nonparametric log-rank tests based upon
chi-squared statistics (Therneau & Grambsch 2010). Post hoc
pairwise testing of survival curves was applied with Bonferroni
correction to evaluate signicant differences between each pos-
sible pair of treatments.
Height and diameter were compared between restoration
treatments and species using mixed- effects regressions with
repeated measurements. Mixed models were fully factorial with
shade and soil as well as their interaction as xed terms. As for
the random terms, we started with nesting block in time and then
dened the minimum adequate models using likelihood ratio
tests as described in Zuur et al. (2009). We used the same mixed
model approach to model the stress variables (ΦPSII, PWC, and
SLA) between treatments and species, although without the time
variable as these variables were registered without repeated
measurements. We used the relative parameter coefcients to
deduce the direction and size of each modeled effect (Grace &
Bollen 2005). In addition, we also ranked the four experimental
treatments according to their contribution to seedling perfor-
mance. We therefore additionally modeled the same data with
mixed-effects ANOVA and applied post hoc pairwise testing.
The resulting ANOVA pvalues and post hoc pairwise combina-
tions are included in gure panels where possible. All model
assumptions were visually checked with quantilquantil and
residual plots (Crawley 2013). All statistical analyses were car-
ried out using R version 3.6.2 (R Core Team 2020). We run sur-
vival and mixed models with customized scripts based upon the
survival (Therneau 2020) and nlme (Pinheiro et al. 2020) pack-
age, respectively.
Results
Emergence and Survival
All restoration interventions signicantly improved emergence
rates, but this effect varied among species (Fig. 1, Table S1).
While Quercus viminea did not perform differently between
restoration treatments, Q. eduardii emerged more under the
shade treatment. For both species, combining forest soil trans-
fer and articial shade was less effective for increasing
emergence rates than each treatment separately. Without dif-
ferentiating between treatments, Q. viminea recorded a higher
emergence rate than Q. eduardii (proportional hazard ratio:
1.439 0.19, p=0.05).
Survival probability for all treatments decreased gradually
during the rst months of evaluation, dropping severely 1 year
after establishment and stabilizing after 2 years. During the rst
year of evaluation, no differences were recorded in the survival
probability between restoration treatments for any species. Mor-
tality peaked when temperature and relative humidity reached
their respective annual maximums (38C) and minimums
(2%). After 2 years of evaluation, higher survival rates were
recorded for Q. eduardii (Hazard ratio: 1.748 0.12,
p< 0.001) and survival probabilities diverged signicantly
between treatments (Fig. 1, Table S1). Seedlings in the shade
treatment had the highest survival probability; 60.65% for
Q. eduardii and 40.92% for Q. viminea. Seedling response of
both species to adding articial shade depended on the type of
soil, doubling its survival rate in native weathered soil but
remaining consistent in transferred forest soil (Fig. 1).
Growth and Functional Responses
Seedling growth differed signicantly between treatments and
species (Fig. 2). Sixty-three months after establishment,
Q. eduardii had signicantly thicker and taller stems than
Q. viminea in all treatments (repeated measures ANOVA of
diameter and height respectively: F
1,4,129
=201.1, p< 0.001;
F
1,4,176
=201.1, p< 0.001), except in the shade +soil sites
where both species grew equally tall. Transferring forest soil
increased seedling diameter growth with 49% while applying
articial shade reduced it with 22% (Table S3). First-year
growth rates were not affected by restoration interventions.
The leaf water content percentage was not signicantly
affected by either shade, soil treatment, or a combination of
these for either of the species (Fig. 3, Table S3). The lowest
SLA for both species and photosynthetic efciency for
Q. eduardii were recorded in seedlings growing in the control
Restoration Ecology4of9
Interacting barriers for seedling establishment
treatment. As for inter-specic comparisons (Table S4),
Q. viminea had lower SLA in the shade and soil transference
treatment while Q. eduardii recorded higher water content in
all restoration interventions but not in the combined treatment
(shade +transferred soil). The same species also yielded higher
photosynthetic efciency in the soil +shade treatment.
p << 0.001 b
a
d
c
p << 0.001
a
a
c
b
p << 0.001
b
a
c
c
p << 0.001
a
a
b
c
Q. eduardii Q. viminea
Diameter Height
50 100 150 200 250 50 100 150 200 250
1.0
1.5
2.0
2.5
3.0
0
50
100
150
200
Weeks since seedling emerged
Growth (mm)
control
shade
soil
soil + shade
Figure 2. Basal diameter and total height growth curves of two 55-month-old oak species in an eroded clearing with different levels of shade and substrate. Each
panel represents a different model and treatments that do not share letters are signicantly different according to pairwise testing based upon mixed-effects
ANOVA model, from which their pvalue is included in each panel (see Table S2 for complete model results).
ab
b
ab
a
NS
a
b
a
a
a
b
ab
ab
Emergence Survival
Q. eduardii Q. viminea
10.0 12.5 15.0 17.5 20.0 0 100 200
0.25
0.50
0.75
1.00
0.25
0.50
0.75
1.00
Weeks since sowing
Probability (%)
control
shade
soil
soil + shade
p < 0.001
p = 0.024
p = 0.007
22.5
Figure 1. KaplanMeier curves for two 55-month-old Quercus species in an eroded clearing with different levels of shade and substrate. Each panel represents a
different model and curves that do not share letters are signicantly different according to pairwise testing with Bonferroni correction. pValues in panels
correspond to likelihood ratio tests of the Cox proportional hazards models (see Table S1 for complete model results).
Restoration Ecology 5of9
Interacting barriers for seedling establishment
Discussion
All tested restoration treatments improved seedling perfor-
mance; however, their effects varied according to ontogenic
stage, micro-environment, and species.
Restoration Outcomes Varied between Life Stages
The effectiveness of our environmental manipulations to enhance
seedling performance varied over time and produced antagonist
effects between different life-stages. Moreover, transferring forest
soil improved emergence of Quercus viminea during its rst year,
it reduced survival during its second year. While rst-year growth
rates were not sensitive to restoration interventions, subsequent
growth was affected particularly by top soil transference.
A tree goes through various ontogenetic stagesfrom germi-
nation to death by senescenceand at each stage faces different
barriers and demands different resources from its micro-
environment. These conicts in habitat requirements across life
stages are common among many plant species (Schupp 1995)
but are especially pronounced in the Quercus genus (Leverkus
et al. 2016). This dynamic sensitivity over time to certain
stressors is due to changing ecology and habitat requirements
during growth (Espelta et al. 1995; Alvarez-Aquino &
Williams-Linera 2012). Oak acorns consist of fattened cotyle-
dons stuffed with carbohydrates that serve as an energy source
during the rst year of seedling growth. At this early stage, less
dependence on the environment and therefore less sensitivity to
soil quality is expected (G
omez-Aparicio et al. 2008; Montes-
hern
andez & L
opez-barrera 2013). However, from the second
year of life, seedlings depend more on external resources and
hence modify their responses to restoration interventions. This
may explain why our restoration interventions created differ-
ences in seedling responses after their rst year of growth, or
why a single restoration practice can generate opposite effects
during the early and latter stages of the seedlings life.
Our data reveal a conict between survival and growth. Trade-
offs exist as seedlings favor their growth under optimal conditions
or avoid mortality in harsh environments (Freschet et al. 2010; de
la Riva et al. 2014; Moles et al. 2014). Compared to the control
treatment in our experiment, adding shade improved survival
while growth was more beneted by soil transfer.
In our experiment, as we expected faster growth in transferred
topsoil and higher survival below the articial shade, we
believed the best micro-environmental conditions were created
when combining both restoration actions. However, the units
with combined treatment did not result in the best seedling
establishment rates. Seedlings growing in the richest soils did
indeed invest more resources in growth and yielded higher pho-
tosynthetic efciency. This, however, came at a cost of
increased mortality compared to the seedlings growing in
weathered soil. Furthermore, photosynthetic efciency was
increased either by adding shade or transferring topsoil but
was not further enhanced when both actions were combined.
NS
p = 0.001
a a ab b
p = 0.005
a b ab b
NS
p = 0.038
a b ab ab
p < 0.001
abbab
Q. viminea Q. eduardii
%cm2/g (Fm'−F)/Fm
control shade soil soil + shade control shade soil soil + shade
0.15
0.20
0.25
0.30
0.35
0.40
0.05
0.06
0.07
0.08
0.09
0.10
0.2
0.4
0.6
ɸ PSII SLA PWC
Figure 3. Water content percentage (PWC) in leaves; specic leaf area (SLA), and chlorophyll uorescence ([Fm0F]/Fm0) for two 55-month-old Quercus
seedlings in an eroded clearing with different levels of shade and substrate. Each panel represents a different model and treatments that do not share letters are
signicantly different according to pairwise testing based upon mixed effects ANOVA model, from which itspvalue their included in each panel (see Table S3
for complete model results).
Restoration Ecology6of9
Interacting barriers for seedling establishment
Restoration Outcomes Varied According
to Micro-Environmental Conditions
Seedlings responded differently to the same restoration interven-
tion according to the micro-environmental conditions where they
were grown. In our experiment, the effect of shading on seedling
emergence and survival depends on the soil quality; this being
positive in degraded soil but negative or neutral in forest soil.
Similar antagonist interactions have been reported for other resto-
ration interventions: Q. eduardíi acorn emergence rates correlate
positively with litter presence in clearings but negatively in forests
(Douterlungne et al. 2018); litter cover improved the acorn germi-
nation in grasslands with gradual transitions into the forest but not
in sharply edged grasslands (L
opez-Barrera et al. 2006).
Generally, seedlings search to tackle the most stressful barrier
for growth and/or survival. These barriers change with different
micro-sites and habitats. For example, (G
omez-Aparicio
et al. 2008) observed a shift in the most critical regeneration bar-
rier for some oaks in the Mediterranean: excess light in dry
places and temporary excess moisture in more humid places.
Plant species can adapt according to these most critical barriers;
for instance, the same oak species can be deciduous or evergreen
according to the amount of available water (Aguilar-Romero
et al. 2017). Therefore, the success of a particular restoration
intervention to enhance seedling establishment may change
according to whether critical stressors are being tackled or not.
Furthermore, restoration interventions, such as adding shade
or introducing forest soil brings along a cascade of micro-
environmental changes. In our study site, introducing top-soil
reduced moisture and temperature in a more effective way than
adding articial shade, which may not be the case in more arid
regions. The impact of a certain environmental stressor or resto-
ration intervention changes according to this interaction with
other abiotic characteristics that form the regeneration niche
(Rousset & Lepart 2000). It is this interaction that allows us to
predict the performance of a seedling, rather than the isolated
effect of a single variable (Plath et al. 2011; Dong et al. 2012).
Results from studies focusing on a single barrier in a single site
should therefore be interpreted with caution.
Restoration Ability Varied between Species
In this study, both species present different strategies to deal
with water stress under the control treatment. While
Q. viminea develops thicker and smaller leaves to reduce the
proportion of foliar area to its biomass (lower SLA),
Q. eduardii presents leaves with denser pubescence and a
waxy cuticle. This last strategy is probably more efcient in
dealing with drought stress, which allows to obtain higher pho-
tosynthetic rates and hence faster growth under full sun expo-
sure. This concurs with the natural habitat preferences of
both species; Q. eduardii grows naturally in poorer soils and
more arid environments than Q. viminea (Castillo-Lara
et al. 2008; Sab
as-Rosales et al. 2015).
Overall, the differences in oak seedling responses to restora-
tion interventions are not surprising given the enormous phe-
notypic genus plasticity (Nixon 2006). This allows different
oak species to overcome different barriers for forest succession
by performing optimally under distinct resource gradients,
such as sun exposure (Quero et al. 2008; Li et al. 2018), litter
(L
opez-Barrera et al. 2006; Pérez-Ruiz et al. 2018), moisture
(Poulos et al. 2007; Leiva et al. 2018), nutrients (Bakker
et al. 2000), or microbiota (Sapp et al. 2019). Restoration inter-
ventions such as applying articial shade or transferring forest
topsoil alters those environmental variables and most likely
create different regeneration niches. Although little is known
regarding the natural regeneration niches of Quercus species,
this information is crucial to select species from the local spe-
cies pool that best perform in the degraded conditions of the
target site to be restored.
Lessons for Oak Forest Restoration in HML
Our data demonstrate a triple source of heterogeneity. First, an
individual tree seedling changes its response to a certain interven-
tion as it passes from one life stage to another. Second, different
oak species respond differently to a particular restoration inter-
vention. This effect may be amplied when using bigger species
pools, as the oak genus in the tropics includes many different spe-
cies, many ofwhich have high intra-specic genetic diversity and
morphologic plasticity. Finally, different restoration interventions
create different micro-habitats.This adds upwith the natural envi-
ronmental heterogeneity in HML that are often mosaic conglom-
erations of patches with diverse micro-environments due to
contrasting land-use histories (Vandermeer & Perfecto 2007).
This triple heterogeneity makes it difcult to predict the outcome
of restoration plantings or draw robust conclusions from restora-
tion trials. We, therefore, recommend monitoring periods of at
least 3 years and that restoration interventions are rested across
species in different environmental settings.
This study detected trade-offs between survival and growth,
with the former being more enhanced by providing articial
shade and the latter by improving soil conditions. Trade-offs
are difcult to handle in restoration plantations and force practi-
tioners to enhance seedling survival at the cost of growth or vice
versa. Our data suggest to prioritize survival by providing arti-
cial shade in severely damaged systems. On the other hand, in
sites with more moderate damage, improving soil conditions
will most likely reduce the time and costs it takes for saplings
to provide signicant tree cover and unleash spontaneous suc-
cession. Alternatively, practitioners might apply environmental
manipulations sequentially over time; shading seedlings for
the rst 2 years and enriching soil conditions once the seedling
had enough time to develop a robust root system.
On the other hand, combining simultaneous interventions did
not produce additional benets. Seedlings receiving both arti-
cial shade and forest soil transference were less likely to survive
and did not yield higher photosynthetic rates and SLA than seed-
lings where only one intervention was applied. The costs of
large-scale restoration plantings may be reduced by identifying
rst the most critical barriers for forest regeneration in the target
site and testing the efciency of several restoration interventions
under eld conditions with different land use histories.
Although the lack of consistency in the response of seedlings
in particular intervention challenges the design of sound
Restoration Ecology 7of9
Interacting barriers for seedling establishment
restoration strategies in oak forests, it also offers advantages.
Restoration strategies in HML can mimic this process by intro-
ducing large amounts of acorns of different species in different
patches of the landscape, thereby increasing the probability that
some seeds will encounter their regeneration niches. This may
be particularly suited to tropical oak species of which the basic
reproductive ecology remains relatively unknown.
Acknowledgments
This work was supported by the Secretary of Public Education
(SEP) and the National Council for Science and Technology
(CONACyT; grants CB-2015-01-257738 to DD and fellowship
no. 574853 to MBRR). The authors would also like to thank
Juan Pablo Rodas Ortíz, Jorge G
amez Rocha, Alejandro Mala-
gamba Rumbio, Marlen Rangel V
azquez and Rosaura Alfaro
García for eld assistance.
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Supporting Information
The following information may be found in the online version of this article:
Figure S1. Signicant differences of average volumetric soil water content values.
Figure S2. Average atmospheric humidity at 100 cm height.
Figure S3. Average temperature at 100 cm height.
Table S1. Hazard ratios (SE) of Cox proportional hazards regression.
Table S2. Left-hand side of vertical gray line.
Table S3. Left hand side of vertical gray line.
Table S4. Mixed effect regression analyses evaluating inter-specic differences.
Coordinating Editor: Louise Egerton-Warburton Received: 6 April, 2021; First decision: 26 May, 2021; Revised: 3 August, 2021;
Accepted: 25 August, 2021
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Interacting barriers for seedling establishment
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Seedling establishment in degraded Oak forests is often hampered by harsh soil conditions, which may take decades to recover. Translocating the top soil from old-growth healthy forests to severely impaired sites can improve environmental conditions and eventually trigger self-repairing forest succession. We tested the potential of this strategy to enhance the seedling establishment of three oak species (Quercus eduardii Trel., Quercus viminea Trel. and Quercus resinosa Liebm.) in a fragmented seasonally dry oak forest with severely weathered soils in Mexico. We transferred old-growth forest topsoil with and without leaf litter to a degraded clearing. To separate habitat from soil effects, we also moved topsoil from the clearing into the old-growth forest. The effects of soil translocation on seedling establishment varied according to life-stage (acorn, seedling, and young sapling), season (rainy vs dry) and site (clearing vs forest). In the clearing, transferred forest topsoil covered with leaf litter yielded the maximum germination probability rates, which were 7 ± 1% higher than in native weathered soil. Once seedlings emerged, survival probability decreased in the transferred soil in both sites, i.e. the weathered clearing soil in the forest habitat, as well as the forest soil in the clearing. Furthermore, transferring forest soil and leaf litter enhanced initial seedling growth in the clearing, increasing growth rates by 60 ± 5% compared to native weathered soil. Increased soil moisture due to soil translocation enhanced seedling establishment in the clearing, but decreased germination and survival rates in the forest. Our results suggest a dynamic water stress mechanism: (1) lack of moisture in soils with poor water retention capacity during the dry season; and (2) water excess during the rainy season in more mesic soil habitats. Given the elevated cost of translocating topsoil and the damage this causes at donor-sites, we recommend considering this intervention only for sites with reduced water retention capacity, prolonged dry seasons and slow soil formation.
Article
The ecological forces determining where within a landscape plants recruit and grow has been termed proximal habitat choice. Habitat choice is imposed first by a heterogeneous pattern of seed dispersal across the patches that make up the landscape and second by environmental variation that favors plant survival in some patches more than in others. Seed-seedling conflicts can occur during both of these phases of habitat choice if conditions or traits that are favorable for seeds are unfavorable for seedlings. During the dispersal phase, smaller seeds may have a greater probability of dispersal than larger seeds, and thus a greater probability of escape from predation, but they contain fewer reserves for support of the establishing seedling. After dispersal, environmental characteristics of a given patch type that lead to disproportionately high seed survival may lead to disproportionately low seedling survival. Considering three hypothetical landscapes, each composed of five patch types, I demonstrate that seed-seedling conflicts can have a major impact on both the overall quantity of recruitment at the landscape level and on the distribution of recruitment among patches. Available empirical evidence suggests these conflicts may be widespread in natural systems. Given their potential importance and extent, seed-seedling conflicts may play a previously unrecognized role in habitat choice.
Article
The main aim of this study is to assess the effect of moderate to low level of cotyledon damage (simulated weevils infection) on holm-oak seedling growth and physiological performance under conditions of soil water stress, a recurrent constraint in Mediterranean and other seasonally dry environment. Three levels of artificial damage were applied to the acorns (no damage NoD, low damage LD, and medium damage MD), and the germination, emergence and early seedling growth under controlled conditions were studied during ca. 1.5 months. On the other hand drought effect on seedling growth, leaf gas-exchange, PSII efficiency, photosynthetic pigments and electron transport energy fluxes was analyzed in a set of older seedlings (i.e., 6.5 months old) that also derived from treated acorns and were exposed to two irrigation treatments (well water WW and water stress WS) for 1.5 months. The results showed that LD and MD acorns germinated earlier than NoD ones but final seedling emergence was lowest in the MD treatment. Cotyledons exhibited increased level of necrotic tissue as physical damage (drilling) increased while seedling biomass and size-related traits tended to decrease. Under WS conditions seedlings derived from LD and MD exhibited higher decrease in above and belowground biomass, as well as on net photosynthetic rate (AN), stomatal conductance (gs), intercellular CO2 concentration (Ci) and PSII efficiency than those derived from NoD. These differences were much less conspicuous under WW treatment where all traits reached higher values. In view of the interactive effect of drought and acorn damage it is concluded that under natural conditions acorn infection by weevils and other insects may represent a highest limitation to holm-oak seedling recruitment than previously considered. In addition this limitation may become more important in the future whether warming and drought increase.