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Negative effects of temperature and atmospheric depositions on the seed viability of common juniper (Juniperus communis)

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Background and AimsEnvironmental change is increasingly impacting ecosystems worldwide. However, our knowledge about the interacting effects of various drivers of global change on sexual reproduction of plants, one of their key mechanisms to cope with change, is limited. This study examines populations of poorly regenerating and threatened common juniper (Juniperus communis) to determine the influence of four drivers of global change (rising temperatures, nitrogen deposition, potentially acidifying deposition and altering precipitation patterns) on two key developmental phases during sexual reproduction, gametogenesis and fertilization (seed phase two, SP2) and embryo development (seed phase three, SP3), and on the ripening time of seeds.Methods In 42 populations throughout the distribution range of common juniper in Europe, 11 943 seeds of two developmental phases were sampled. Seed viability was determined using seed dissection and related to accumulated temperature (expressed as growing degree-days), nitrogen and potentially acidifying deposition (nitrogen plus sulfur), and precipitation data.Key ResultsPrecipitation had no influence on the viability of the seeds or on the ripening time. Increasing temperatures had a negative impact on the viability of SP2 and SP3 seeds and decreased the ripening time. Potentially acidifying depositions negatively influenced SP3 seed viability, while enhanced nitrogen deposition led to lower ripening times.Conclusions Higher temperatures and atmospheric deposition affected SP3 seeds more than SP2 seeds. However, this is possibly a delayed effect as juniper seeds develop practically independently, due to the absence of vascular communication with the parent plant from shortly after fertilization. It is proposed that the failure of natural regeneration in many European juniper populations might be attributed to climate warming as well as enhanced atmospheric deposition of nitrogen and sulfur.
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Negative effects of temperature and atmospheric depositions on the seed viability
of common juniper (Juniperus communis)
R. Gruwez1,*, P. De Frenne1,2, A. De Schrijver1, O. Leroux3, P. Vangansbeke1,4 and K. Verheyen1
1
Forest and Nature Lab, Ghent University, Geraardsbergsesteenweg 267, BE-9090 Melle-Gontrode, Belgium,
2
Forest Ecology and
Conservation Group, Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK,
3
Pteridology Lab, Ghent University, K.L. Ledeganckstraat 35, BE-9000 Ghent, Belgium and
4
Flemish Instute of Technological
Research (VITO), Boeretang 200, BE-2400 Mol, Belgium
* For correspondience. E-mail Robert.Gruwez@UGent.be
Received: 15 July 2013 Returned for revision: 11 September 2013 Accepted: 8 October 2013 Published electronically: 26 November 2013
Background and Aims Environmental change is increasingly impacting ecosystems worldwide. However, our
knowledge about the interacting effects of various drivers of global change on sexual reproduction of plants, one
of their key mechanisms to cope with change, is limited. This study examines populations of poorly regenerating
and threatened common juniper (Juniperus communis) to determine the influence of four drivers of global change
(rising temperatures, nitrogen deposition, potentially acidifying deposition and altering precipitation patterns) on
two key developmental phases during sexual reproduction, gametogenesis and fertilization (seed phase two, SP2)
and embryo development (seed phase three, SP3), and on the ripening time of seeds.
Methods In 42 populations throughout the distribution range of common juniper in Europe, 11 943 seeds of two
developmental phases weresampled. Seed viability was determined using seed dissection and related to accumulated
temperature (expressed as growing degree-days), nitrogen and potentially acidifying deposition (nitrogen plus
sulfur), and precipitation data.
Key Results Precipitation had no influence on the viabilityof the seeds or on the ripening time. Increasing tempera-
tures had a negative impact on the viability of SP2 and SP3 seeds and decreased the ripening time. Potentially acid-
ifying depositions negatively influenced SP3 seed viability, while enhanced nitrogen deposition led to lower ripening
times.
Conclusions Higher temperatures and atmospheric deposition affected SP3 seeds more than SP2 seeds. However,
this is possibly a delayed effect as juniper seeds develop practically independently, due to the absence of vascular
communication with the parent plant from shortly after fertilization. It is proposed that the failure of natural regen-
eration in many Europeanjuniper populations might be attributed to climate warming as well as enhanced atmospher-
ic deposition of nitrogen and sulfur.
Key words: Juniperus communis, juniper, seed viability, ripening time, climate change, increasing temperature,
nitrogen deposition, acidifying deposition.
INTRODUCTION
The early life history stages of plants, including seed production,
are among the most important processes that drive plant commu-
nity structure (HilleRisLambers et al., 2009;Linkies et al.,
2010). Sexual reproduction aids plants to adapt to changing
environments and to colonize previously unoccupied habitats
(Fenner and Thompson, 2005). Worldwide, environmental con-
ditions and ecosystems are undergoing rapid change (Millennium
Ecosystem Assessment, 2005),and the effects of thedrivers of this
global change (e.g. climate change, nitrogen deposition, habitat
fragmentation and invasive species) will increase in the coming
decades (Rands et al., 2010). Hence, the role of sexual reproduc-
tion in the adaptation of organisms to changing environments
might become more important. However, sexual reproduction
itself is also affected by global change. Several studies have inves-
tigated the influence of different drivers of global changeon sexual
reproduction of plants, including warming (Pen
˜uelas et al.,2004;
De Frenneet al.,2011;Koivuranta et al.,2012), elevated CO
2
con-
centrations (Thurig et al., 2003), nitrogen deposition (Callahan
et al.,2008) and drought (Demirtas et al.,2010). Fewer studies
have investigated the integrated effect of different drivers on
sexual reproduction (Hovenden et al.,2008;HilleRisLambers
et al., 2009;Verheyen et al., 2009;Li et al.,2011). Even less is
known about the different processes acting during subsequent
phases of the sexual reproductive cycle of plants (but see Owens
et al.,2001;Hedhly, 2011). For example, Hedhly et al. (2009)
underlined the importance of studying the sensitive stages (e.g.
fertilization and embryogenesis) independently in order to obtain
a better understanding of the effectof temperature on sexualrepro-
duction. Here we follow such an approach in the coniferous shrub
common juniper (Juniperus communis L.) to assess the effects
of various drivers of global change across its distribution range.
Juniperus communis has a relatively long sexual reproduction
cycle (2 3 years) with clearly distinguishable phases (Gruwez
et al.,2012) and it is widely distributed across much of the northern
hemisphere (Adams, 2008). Populationsof comm onjuniper are de-
clining throughout several European regions, including the north-
western European lowlands [e.g. Belgium (Frankard, 2004;
Adriaenssens et al., 2006), The Netherlands (Oostermeijer and
De Knegt, 2004), northern and western Germany (Hu
¨ppe, 1995),
and England (Clifton et al.,1997)], and the Mediterranean
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Annals of Botany 113: 489–500, 2014
doi:10.1093/aob/mct272, available online at www.aob.oxfordjournals.org
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mountain regions (Garcı
´aet al., 1999). In contrast, the species is
still abundant and exhibits good regeneration in other regions
[e.g. in the Alps, Scandinavia and Poland(Falinski, 1980;Rose
´n,
1995;Rose
´n and Bakker, 2005)]. Nevertheless, due to their threa-
tened status in several regions in Europe, J. communis communities
are listed in Annex I of the EU Habitat Directive (code 5130).
Verheyen et al. (2005) identified habitat destruction, habitat
degradation and limited sexual reproduction as the most import-
ant causes for this decline. In addition, a triangular relationship
between the fraction of recently recruited individuals and the
percentage of viable seeds in a population has been identified
(Verheyen et al., 2009). Hence, a low percentage of viable seeds
results in negligible recruitment, while in the case of a high per-
centage of viable seeds other factors such as herbivory, summer
drought and the absence of suitable microsites for germination
can explain the differences in recruitment between populations
(Ward, 1973,1982;Fitter and Jennings, 1975;Gilbert, 1980;
Garcı
´a, 2001). Seed viability showed large inter-regional as
well as intraregional variation across Europe (Verheyen et al.,
2009). In addition, Verheyen et al. (2009) found a negative rela-
tionship between seed viability on the one hand and increasing
temperature (expressed as mean annual growing degree-days
above 0 8C) and enhanced nitrogen deposition on the other hand.
In combination with climate warming, changing precipitation
patterns are often put forward as important drivers of sexual re-
production in plants (e.g. Owens, 1995;Walck et al., 2011).
Although Verheyen et al. (2009) found no relationship between
seed viability of ripe common juniper seeds and precipitation,
there can still be an influence during other phases of sexual repro-
duction. To date, landscape fragmentation has not led to genetic
impoverishment of common juniper in north-western Europe
(Vanden Broeck et al., 2011); thus, loss of genetic diversity is un-
likely to be a cause of low seed viability.
The most critical phase of pre-dispersal seed development in
common juniper occurs during embryo development (seed
phase three; see Gruwez et al., 2012). However, it remains
unclear whether the reasons for the failure of embryo develop-
ment occur in this phase or in the previous phase of the growth
of the pollen tube, gametogenesis, fertilization and early
embryo development (seed phase two; see Gruwez et al.,
2012), as different processes during seed development can regu-
late each other (Fig. 1). Two processes that need to be successful
to allow fertilization are pollen tube growth and female gameto-
phyte development (Fig. 1D, E). A prerequisite for pollen tube
growth is that pollination supplies healthy pollen (Fig. 1A).
There also seems to be an interaction between the pollen tube
and the female gametophyte (Fig. 1B, C). In some species, a
normal development of the ovule is promoted by the pollen or
pollen tube that triggers the production of hormones such as
auxins, gibberellins and cytokinins (Fernando et al., 2005;
Owens et al., 2005). However, many gymnosperms show
normal development of the female gametophyte until shortly
after the period of fertilization, even without pollen (Owens
and Blake, 1986;Owens, 1995;Owens and Morris, 1998).
Growth of the pollen tube, on the other hand, often requires the
presence of a healthy female gametophyte (e.g. Takaso and
Owens, 1996;Fernando et al., 1997;Drews and Koltunow,
2011), probably because it provides specific secretions
(Fernando et al., 2005) (Fig. 1B). During the pre-fertilization
stage, the female gametophyte not only forms the archegonia
and egg cells but also prepares, for instance, for seed reserve
storage (Owens et al., 2008). Thus, the female gametophyte in
gymnosperms accumulates nutrients before fertilization (Vuosku
et al., 2009) and, at the moment of fertilization, the megagameto-
phytes have almost reached their full development and there is prac-
tically no vascular communication between the seeds and the
ovuliferous scales. Therefore, in general, the seeds are autonomous
after fertilization (Owens and Blake, 1986;Owens, 1991)andthe
megagametophyte nourishes the developing embryo (Durzan and
Chalupa, 1968;Vuosku et al., 2009). Thus, the development of
the female gametophyte not only directly influences the fertilization
(Fig. 1E) and indirectly influences the growth of the pollen tube
(Fig. 1B), but anomalies during this phasecanalsoleadtonutrition-
al problems during embryo development (Fig. 1G).
In common juniper, an additional complexity is that seeds can
ripen in 2 years or in 3 years. In the lattercas e, fertilizationis post-
poned for 1 year. A lag between pollination and fertilization is
found in different conifers (e.g. different Pinus species; Singh,
1978), but the reasons remain unclear. It appears that the
pollen tube enters dormancy while the female gametophyte is
slowly developing. Shortly before fertilization, the pollen tube
revives due to unknown cues (Williams, 2009). Willson and
Burley (1983) suggested that delayed fertilization increases the
time for selection of male gametophytes and female archegonia,
Pollination Growth of pollen tube
Seed phase 2 Seed phase 3
Development of female gametophyte
G
Fertilization Embryo development
F
A
BC
D
E
FIG. 1. Schematic of the relationships between the key processes during the seed development of Juniperus communis (solid arrows for important relationships,
dotted arrows for less important relationships). See text for a detailed explanation.
Gruwez et al. — Negative effects of global change on the seed viability of juniper490
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but they also mentioned the possibility that short reproductive
seasons force plants to spread pollination and fertilization over
1 year (Willson and Burley, 1983). However, there is still no con-
sensus. In common juniper, the pattern of seed ripening can be
dichotomized, with some seeds requiring a time interval of a
few months and others a full year. These two strategies may
appear within the same shrub (Gruwez et al., 2012). To our
knowledge, this dual strategy is absent in other conifers. In add-
ition, a complex relationship between the ripening time of the
seeds of common juniper and seed viability appears to exist.
Most seeds ripening in 3 years already have low viability
shortly after fertilization, whereas the viability of seeds ripening
in 2 years decreased mostly during embryo development
(Gruwez et al., 2012).
In the present study, we sampled the hitherto spatially widest
spread of populations (to our knowledge) of common juniper and
collected seeds of two different development phases (shortly
after fertilization and at the end of embryo ripening). By sam-
pling in 42 populations throughout Europe ( from Sweden to
Spain and from Ireland to Poland), we are able to take advantage
of the wide climatic and deposition gradients (De Frenne et al.,
2013) in this area. We examined the influence of four drivers
of global change (increasing temperature, nitrogen deposition,
potentially acidifying depositions and altering precipitation pat-
terns) on the seed viability of common juniper after both seed de-
velopment phases and on the ripening time. The aim of the
present study is therefore to test the following hypotheses: (1)
that the influence of drivers of global change on seed viability
is more pronounced after seed phase two, which indicates that
this phase is more vulnerable and (2) that these drivers are deter-
minants of which ripening time strategy occurs in seed.
MATERIALS AND METHODS
Species studied
Juniperus communis is a gymnosperm and one of the most wide-
spread plant species, with a geographic distribution covering
most of the northern hemisphere (Adams, 2008). It is a dioecious,
wind-pollinated coniferous shrub or tree. The females annually
produce fleshy, spherical, berry-like cones of approx. 6.5mm
in diameter that take 2 or 3 years to ripen (Ottley, 1909;Garcı
´a
et al., 2000;Thomas et al., 2007;Ward, 2010). Sexual reproduc-
tion starts with the cone initiation in autumn or early winter
(Singh, 1978), with the female strobili usually containing three
ovules (Thomas et al., 2007). As common juniper has a dual
seed ripening strategy, both a 2 year and a 3 year cycle can
occur (Fig. 1; Gruwez et al., 2012). In a 2 year cycle, pollination
takes place in the following spring and fertilization follows in the
summer of the same year. After fertilization, embryo develop-
ment starts and, by the end of the summer of the second year,
the seeds are ready for dispersal. In a 3 year cycle, fertilization
is postponed by 1 year and only takes place in the summer of
the second year, so seeds are ripe for dispersal by the end of
the summer of the third year (Ottley, 1909;Garcı
´aet al., 2000;
Thomas et al., 2007;Ward, 2010;Gruwez et al., 2012). A
detailed description of the seed and cone development is avail-
able in Gruwez et al. (2012). We here refer to seeds from the de-
velopmental phase shortly after fertilization as seed phase two
seeds (SP2 seeds), while seeds that have a ripe embryo are re-
ferred to as seed phase three seeds (SP3 seeds; Gruwez et al.,
2012).
Population, shrub and seed characteristics and sampling
Seeds of 42 populations across the species’ distribution range
in Europe (Fig. 2A; Supplementary Data Table S1, Fig.S1) were
sampled in autumn of 2008 and 2010 (eight and 34 populations,
respectively). Populations consisted of at least 30 individual
shrubs growing in unshaded conditions (i.e. not below other
tree species). In each population, 3– 8 (with a median of five)
cone-bearing shrubs were randomly selected. Per shrub, three
branches were randomly selected, of which on average 28.7
(+9.4 s.d.) SP2 seeds and 23.2(+9.9 s.d.) SP3 seeds were
sampled.
Different characteristics were measured and estimated on
three different levels: population, shrub and seed. The age of
the seeds was deduced from the age of the woody branches on
which the cones (containing the seeds) were growing (the
cones are always 1 year younger than the wood). The age of
the wood can be determined by counting the growing shoot inter-
nodes that are separated by the annual bud scars. By taking the
seed phase and the age of the seed into account, we then calcu-
lated the ripening time of the seeds (an SP2 seed of 1 year old
or an SP3 seed of 2 years old has a ripening time of 2 years, an
SP2 seed of 2 years old or an SP3 seed of 3 yearsold has a ripening
time of 3 years). For every seed, the number of growing degree-
days above 0 8C base temperature (GDD
.08C
; cf. Hall et al.,
2002) was calculated for three important processes during seed
development: pollination, fertilization and embryo develop-
ment. Depending on the collection date, seed phase and the
ripening time, data of different years and seasons were used
(Supplementary Data Table S2). Daily minimum and maximum
temperatures of each population were obtained from the nearest
weather stations (see Supplementary Data Table S1) and used to
calculate the GDD
.08C
. When the population and the weather
station had different altitudes, a mean adiabatic lapse rate of
5.5Kkm
21
(Ko
¨rner, 2007) was applied. The GDD
.08C
ranged
between 257.6 and 1633.8, with an average of 979.5
(+245.6 s.d.) for the spring of pollination, between 775.7 and
2164.1 with an average of 1554.8(+243.8 s.d.) for the
summer of fertilization and between 1217.9 and 5074.7 with
an average of 3344.8(+786.7 s.d.) for the year of embryo devel-
opment (Fig. 2A).
Nitrogen and sulfur deposition data were obtained from the
European Monitoring and valuation Programme database
(EMEP; http://www.emep.int). The EMEP is the ‘Co-operative
Programme for Monitoring and Evaluation of the Long-range
Transmission of Air pollutants in Europe’ and provides scientific
information on the emission, transport and deposition of air
pollutants. Here, data for 2008 were used: total (wet +dry)
inorganic nitrogen (NH
x
+NO
y
) depositions expressed as
kg ha
21
year
21
and potentially acidifying (NH
x
+NO
y
+SO
x
)
depositions expressed as keq ha
21
year
21
in 50 ×50 km grid
cells covering Europe. Nitrogen depositions ranged from 1.84 to
36.05 kg ha
21
year
21
with an average of 12.21 kg ha
21
year
21
(+6.9 s.d.). Potentially acidifying depositions ranged from 0.20
to 3.03 keq ha
21
year
21
with an average of 1.17 keq ha
21
year
21
(+0.60 s.d.) (Fig. 2B).
Gruwez et al. — Negative effects of global change on the seed viability of juniper 491
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Next, the annual amount of precipitation in the year preceding
the time of sampling was calculated per population using the
monthly precipitation data from Climatic Research Unit
(CRU) time-series data sets (Harris et al., 2013). Yearly precipi-
tation ranged from 467.9 to 2280.8 mm year
21
with an average of
858.9 mm year
21
(+301.1 s.d.).
A
D
B
C
E
FIG. 2. The locations and characteristics of the 42 sampled European common juniper (Juniperus communis) populations. For each map, the size of the dots is a
relative measure for the GDD
.08C
during embryo development (A), the amount of potentially acidifying deposition (N +S; keq ha
21
year
21
) (B), the percentage
of viable SP2 (C) and the percentage of viable SP3 seeds (D) per population; and the percentage seeds that ripen in 3 years instead of 2 years (E).
Gruwez et al. — Negative effects of global change on the seed viability of juniper492
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Correlations between temperature variables, atmospheric
depositions and annual precipitation were low (Supplementary
Data Table S3).
Finally, for each population, we estimated two soil character-
istics in different classes: texture of the first 50 cm (sandy,
sandy loam, loamy or clayey) and bedrock type (calcareous vs.
non-calcareous).
At the shrub level, three characteristics, namely proportion of
needle loss, cone density and plant height, were estimated.
Different classes of needle loss (,20, ,40 and 40 %) were
used as an indicator for the health of each shrub. Cone density
was sub-divided into three classes: low (the cones appear scat-
tered and it is difficult to find any), normal (the cones appear scat-
tered, but they are rather abundant) or dense (large clusters of
cones are abundant). Finally, the height of each shrub was mea-
sured and classified into five different height classes (,0.5, ,1,
,2, ,3 and 3m).
Seed analyses
The viability of all sampled seeds was assessed by means of
stereoscopic observations of dissected seeds (6609 seeds for
SP2 and 5333 seeds for SP3). Seeds that had no visible signs of
anomalies were considered to have the potential to develop to
the next phase and are further referred to as ‘viable seeds’.
Although this method generates an overestimation of the real
seed viability, Adriaenssens (2006) stated that there is a clear cor-
relation (R¼0.681 and P,0.01) with the results of more
precise methods such as a tetrazolium test (Miller, 2004).
Viable SP2 seeds presented a megagametophyte and nucellus
consisting of green-white and moist tissue, not completely
filling the space within the seed coat (Gruwez et al., 2012).
Viable SP3 seeds consisted of an embryo and megagametophyte
with a smooth, white and moist surface. In this phase, almost all
space within the seed coat is filled (Gruwez et al., 2012). In both
SP2 and SP3, seeds were occasionally damaged by mites [e.g.
Trisetacus quadrisetus (Acarina, Eriophyiidae)] or by the seed
predator chalcid Megastigmus bipunctatus [Hymenoptera,
Torymidae; see Roques and Skrzypczynska (2003) for a
review of the seed-infesting chalcids of the genus Juniperus].
The content of seeds attacked by mites is completely distorted
and, mostly, the mites are still present. Damage by M. bipunctatus
could be recognized by the granular content, an exit hole or the
presence of larvae. For both seed phases, seeds were scored on
the basis of viability (non-viable or viable), presence of mites and
M. bipunctatus (absent or present) and the ripening time (2 or 3
years). Mean infection rates with mites and M. bipunctatus were cal-
culated for each shrub and population.
Data analysis
To study the relationships between the seed viability of SP2
seeds (viable or not), SP3 seeds (viable or not) and the ripening
time (2 or 3 years; seed-level data throughout) on the one hand,
and the climatic, environmental, soil, shrub and seed (ripening
time) variables (fixed-effect terms) on the other hand, general-
ized linear mixed modelling with binomial distributions was
applied, using the glmmML function of the glmmML library
and the lmer function of the lme4 library in R 2.15.1
(R Development Core Team, 2012). Ripening time was only
included in the models concerning the viability of SP2 and SP3
seeds. Populations were treated as clusters within the glmmML
function and as random effects within the lmer function. In a
first step, all variables were entered in the model on a one-by-one
basis. Per dependent variable (viability of SP2 and SP3 seeds and
ripening time), variables with a significance level of 0.1 were
selected for multivariate modelling. Autocorrelation between
the selected variables was checked by calculating the variance
inflation factor (Quinn and Keough, 2002). In the case of autocor-
relation (notablybetween GDD
.08C
during pollination,GDD
.08C
during fertilization and GDD
.08C
during embryo development,
and between nitrogen deposition and potentially acidifying
depositions), only the most significant variables were selected.
Subsequently, all possible models for the three dependent
variables (i.e. built by each combination of the selected
fixed-effects terms, giving 384 models in total ) were compared
using the Akaike’s information criterion, adjusted for sample
size (AIC
c
)(Hurvich and Tsai, 1989). The DAIC
c
of a model
was then calculated as the difference between the AIC
c
of the
model with the best fit and the AIC
c
of that model. Models
with DAIC
c
4 were considered equivalent (Bolker, 2008). To
determine the relative importance of the explanatory variables,
the sum of Akaike weights of the set of all top models (DAIC
c
4) in which the variable appeared (Burnham and Anderson,
2002) was used. The Aikake weight reflects the weight of evi-
dence in support of a particular model relative to the entire
model set, and varies from 0 (no support) to 1 (complete support).
For each explanatory variable, the relative importance was calcu-
lated by summing the Aikake weights of the models containing
the variable. Finally, the averaged parameters of the top models
were calculated using the model averaging function based on the
AIC
c
of the MuMin package in R.
Finally, to visualize the effects of temperature,nitrogen depos-
ition and potentially acidifying depositions on seed viability and
ripening time, we calculated the proportion of viable SP2 and
S3 seeds and the proportion of seeds that ripened in 3 years per
population. A similar procedure was followed for shrub height,
cone density and needle loss, where the proportion per class
was calculated.
RESULTS
As expected, seed viability declined between seed phase two and
three (Fig. 2). The average percentage of viable SP2 seeds per
population was 38.2%(+18.6 s.d.) with a minimum of 2.3%
and a maximum of 73.8 %. For SP3 seeds, the average was
10.9% (+14.6 % s.d.) with a minimum of 0 % and a max-
imum of 58.2 %. The seed viability exhibits a large variability
for both SP2 seeds and SP3 seeds. For example, 12 populations
(in Belgium, France, Germany, Italy, The Netherlands, Spain
and the UK) had extremely low percentages (,1 %) of viable
SP3 seeds. Conversely, populations with higher percentages of
viable SP2 seeds (.40 %) were situated in Scandinavia, on the
axis of eastern Germany towards north-eastern Italy, on the
axis of north-central Spain towards south-eastern France, in
Ireland and in the south-west of the UK (Fig. 2C). After SP3,
most of the Scandinavian populations still had relatively high
percentages of viable seeds (.20 %), together with three popu-
lations in southern and central Germany and Austria and the Irish
population (Fig. 2D).
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Infection rates with mites and M. bipunctatus were relatively
low for populations (mean 8.3 and 3.1 %, respectively), although
infection rates of individual shrubs can be significant (e.g. 93.3
and 76.9 %, respectively). In only one population, more than
half of the seeds were infected with mites (53.4 %), while
M. bipunctatus infection rates always stayed below 20 %.
Most of the seeds ripened in 2 years (64.5 %). Fourteen popu-
lations had .90 % of their seeds ripening in 2 years and for nine
populations this percentage dropped below 10 %. Seeds with a 3
year ripening time were mainly found in Scandinavia, but popu-
lations with high percentages were also present in Spain and
south-eastern France (Fig. 2E).
Selection of the variables for multivariate modelling led to dif-
ferent results for the viability of SP2 and SP3 seeds and ripening
time. For the viability of SP2 seeds, the factors precipitation, mite
infection rate, type of bedrock, soil texture, needle loss and ripen-
ing time did not have a significance level lower than 0.1. These
variables were therefore considered as not important and were
excluded from the model selection procedure. In a similar way,
precipitation, mite and M. bipunctatus infection rate, type of
bedrock, soil texture and needle loss were excluded for SP3
seeds, and precipitation, mite infection rate and soil texture for
ripening time. In addition, autocorrelation occurred between
the temperature variables, and between the atmospheric depos-
ition variables, resulting in a selection (on the basis of the
factor with the highest significance level) of GDD
.08C
during
pollination and potentially acidifying deposition for SP2 seeds;
of GDD
.08C
during embryo development and potentially acid-
ifying deposition for SP3 seeds; and of GDD
.08C
in the year
before sampling and nitrogen deposition for ripening time.
The most important variables affecting the viability of SP2
seeds were temperature (GDD
.08C
during pollination), infection
rate with M. bipunctatus on a population level and shrub height,
which all had a negative influence (Table 1, Figs 3A, 4A).
Potentially acidifying deposition had only a marginally negative
influence (Table 1, Fig. 3B). The ripening time strategy for a
given seed had no influence on the viability of SP2 seeds.
The patterns were slightly different for SP3 seeds (Table 2).
Here both potentially acidifying depositions and temperature
(GDD
.08C
during embryo development) had a strong negative
influence on seed viability (Figs 3C, D). In addition, their inter-
action was also important and indicated that the negative influ-
ence of temperature was more pronounced in populations with
a lower potentially acidifying deposition. In addition, shrub
height and cone density had an important negative and positive
influence, respectively (Fig. 4D, E). Seeds that ripened in 3
years had a slightly greater chance of being viable than seeds
that ripened in 2 years, but this effect was less pronounced
(Table 2).
Ripening time was mostly determined by nitrogen deposition,
the bedrock type, cone density, shrub height and needle loss
(Table 3, Figs 3F, 4G– I). Seeds originating from populations
with a higher nitrogen deposition or growing on soil with a cal-
careous bedrock more often had a ripening time of 2 years.
Shrubs with a greater cone density had more seeds that ripened
in 2 years, and vice versa for taller shrubs or those with a larger
needle loss. Higher temperatures (GDD
.08C
during embryo de-
velopment) led to shorter ripening times, but this effect was
less pronounced (Fig. 3E). The interaction between temperature
and nitrogen deposition was of minor importance.
DISCUSSION
The aim of this study was to achieve a better understanding of the
influence of four drivers of global change (increasing tempera-
tures, enhanced nitrogen, potentially acidification deposition
and altering precipitation patterns) on the viability and ripening
time of common juniper seeds (Juniperus communis). We
focused on two key seed developmental phases, i.e. growth of
the pollen tube, megagametogenesis, fertilization and early
embryo development (SP2) and ripening of the embryo (SP3),
that were identified as crucial for the sexual reproductive cycle
of this species (Gruwez et al., 2012). Both needle loss and
shrub height (as a rough proxy for age, Breek, 1978;Forbes
and Proctor, 1986) can be seen as a measure of senescence.
Cone density, on the other hand, relates to the vitality of the
shrub. This can explain the relationships between cone density,
shrub height and seed viability. Precipitation was shown to
have no influence. In the following sections, we focus on the im-
portant effects of temperature and enhanced atmospheric deposi-
tions on seed viability of common juniper.
Temperature effects
We showed that increasing temperatures have a negative influ-
ence on seed viability of both SP2 and SP3 seeds of common
TABLE 1. Model selection statistics for the analysis of the effects of GDD
.08C
during the spring of pollination, potentially acidifying
deposition, their interaction, infection rate with M. bipunctatus, cone density and shrub height on the viability of SP2 seed
Intercept
Growing degree-days
(GDD) pollination
Potentially acidifying
deposition (PAD) GDD:PAD
Infection rate with
M. bipunctatus
Cone
density
Shrub
height d.f. DAICc Weight
3.50 –3.09 ×10
23
–11.9+80 0
.48
3.55 –3.02 ×10
23
–0.0979 – 12.1+91
.85 0.19
3.40 –3.12 ×10
23
–11.7++10 1.92 0.18
3.96 –3.41 ×10
23
–0.447 3.27 ×10
24
–12.4+10 3.72 0.08
3.45 –3.06 ×10
23
–0.0951 – 11.9++11 3.78 0.07
Importance 1.00 0.34 0.07 1.00 0.26 1.00 – –
+, a factorial variable is included in the model.
DAICc, difference in values of the corrected Akaike Information Criterion between a model and the best model; weight, Akaike weight indicating the relative
support for the model; importance, the relative importance of the explanatory variables based on the sum of the Akaike weights of the models in which the
variables appear.
Gruwez et al. — Negative effects of global change on the seed viability of juniper494
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juniper and promote a ripening time of 2 years. Different patterns
can be seen between the two studied developmental phases. For
the viability of the SP2 seeds, the GDD
.08C
during springtime
were most important, while, for the SP3 seeds, only the
GDD
.08C
during embryo development had a significantly nega-
tive influence.
Our results differ from what is found in other studies on con-
ifers where a positive relationship between higher temperatures
and seed vi ability was revealed (e.g . Desplandand Houle, 1997;
Noland et al., 2006;Meunier et al., 2007). However, the latter
studies were often performed at the northern distribution
range limits, whereas our study included common juniper
populations from a wider geographical area. Low temperatures
and late frosts during pollination are often mentioned as
reasons for failing pollination and ovule abortion during
further seed development (e.g. Owens, 1995;Thomas et al.,
0·6
SP2
AC E
BD F
SP3 Ripening time
0·6 1·0
0·8
0·6
0·4
0·2
0
0·5
0·4
0·3
0·2
0·1
0
0·4
0·2
0
0·6
0·4
0·2
0·6 1·0
0·8
0·6
0·4
0·2
0
0·4
0·5
0·3
0·2
0·1
0
0
0·5 1·0 1·5 2·0 2·5 3·0
Potentially acidifying deposition
(keq ha–1 year–1)
0·5 1·0 1·5 2·0 2·5 3·0 10 20 30
Potentially acidifying deposition
(keq ha–1 year–1)
Nitrogen deposition
(kg N ha–1 year–1)
Proportion viable SP2-seeds
Proportion viable SP3-seeds
Proportion seeds that ripen in 3 years
500 1000 1500 2000 3000 4000 5000
GDD>0°C during the spring of pollination GDD>0°C during embryo development
2000 3000 4000 5000
GDD>0°C during year before sampling
Proportion viable SP2-seeds
Proportion viable SP3-seeds
Proportion seeds that ripen in 3 years
FIG. 3. Relationships between accumulated temperature (GDD
.08C
during the spring of pollination for seed phase two, GDD
.08C
during embryo development for
seed phase three and GDD
.08C
during the year beforesampling for the ripening time) (A, C, E), potentially acidifying deposition (keq ha
21
year
21
) for seed phase two
and three, and nitrogendeposition (kg N ha
21
year
21
) for ripening time (B, D, F) on the one hand, and viability of SP2seeds (left column), viability of SP3 seeds (middle
column) and the seed ripening time (right column). A smoothing spline is fitted to the continuous data.
TABLE 2. Model selection statistics for the analysis of the effects of GDD
.08C
during embryo development, potentially acidifying
deposition, their interaction, cone density, shrub height and ripening time on the viability of SP3 seeds
Intercept
Growing degree-days (GDD)
embryo development
Potentially acidifying
deposition (PAD) GDD:PAD
Cone
density
Shrub
height
Ripening
time d.f. DAICc Weight
4.70 –2.07 ×10
23
–6.95 1.72 ×10
23
+++12 0 0.65
5.15 –2.16 ×10
23
–7.18 1.77 ×10
23
++ 11 1.20 0.36
Importance 1 1 1 1 1 0.65 – –
+, a factorial variable is included in the model.
DAICc, difference in values of the corrected Akaike Information Criterion between a model and the best model; weight, Akaike weight indicating the relative
support for the model; importance, the relative importance of the explanatory variables based on the sum of the Akaike weights of the models in which the
variables appear.
Gruwez et al. — Negative effects of global change on the seed viability of juniper 495
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2007). Therefore, a lackof pollination cannot explain the nega-
tive relationship between seed viability and the temperature
during the spring.
During SP2, there are two processes (the development of the
female gametophyte and growth of the pollen tube) that can
help to explain the negative effects of temperature on seed viabil-
ity (Fig. 1).
First, higher temperatures can induce abnormalities in the
female gametophyte (Franz and Jolliff, 1989;Kozai et al.,
2004) or other female structures (Saini et al., 1983;Hedhly
et al., 2003,2004,2005), which can lead to abortion of the
seed. Secondly, little is known about the direct effects of
higher temperatures on the viability of the germinating pollen
(but see Young et al., 2004;Steinacher and Wagner, 2012).
However, several studies hypothesized that the ovule and
female gametophyte might be important regulators of pollen
tube growth (e.g. Gifford and Foster, 1989;Takaso and Owens,
1996;Fernando et al., 2005;Drews and Koltunow, 2011).
Thus, through influencing the female gametophyte, increased
temperatures can have an indirect effect.
In addition, due to their separate influences on the pollen
tube and female gametophyte, high temperatures also have
100 AD G
BE H
CF I
SP2 SP3 Ripening time
80
60
40
20
012345
Shrub height class
12345
Shrub height class
12345
Shrub height class
Percentage viable SP2-seeds
100
80
60
40
20
0123
Cone density class
Needle loss class Needle loss class Needle loss class
123
Cone density class
123
123 123 123
Cone density class
Percentage viable SP2-seeds
100
80
60
40
20
0
Percentage viable SP2-seeds
100
80
60
40
20
0
Percentage viable SP3-seeds
100
80
60
40
20
0
Percentage viable SP3-seeds
100
80
60
40
20
0
Percentage viable SP3-seeds
100
80
60
40
20
0
100
80
60
40
20
0
Percentage seeds that ripen
in 3 years
Percentage seeds that ripen
in 3 years
100
80
60
40
20
0
Percentage seeds that ripen
in 3 years
FIG. 4 . Relationships between shrub height (A, D, G), cone density (B, E, H) and needle loss (C, F, I) on the one hand, and viability of SP2 seeds (left column), viability
of SP3 seeds (middle column) and the seed ripening time (right column). Shrub height classes: 1, ,0.5m;2,,1m;3,,2m;4,,3m;5,3 m; needle loss classes:
1, ,20 %; 2, ,40 %; 3, 40 %; cone density classes: 1, low; 2, normal; 3, dense. Values are means and error bars represent the 95 % confidence interval.
Gruwez et al. — Negative effects of global change on the seed viability of juniper496
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detrimental effects on the male–female synchrony in the pre-
ferilization phases (Zinn et al., 2010;Hedhly, 2011).
Hence, both mechanisms, i.e. the negative influence of higher
temperatures on the viability of the female gametophyte and the
different effects on the growth speed of both female gametophyte
and pollen tube, may lead to unviable SP2 seeds.
Higher temperatures during the spring of the pollination and
the summer of the fertilization seem to have no influence on via-
bility of SP3 seeds. Perhaps cones with aborted seeds have been
shed by the third year, which can mask these effects. On the other
hand, GDD
.08C
during embryo development had a negative in-
fluence on seed viability. Possibly, higher temperatures may
disrupt the meristimatic activity of the female gametophyte
with accumulation of resources such as lipids, starch and proteins
(Singh, 1978;Owens et al., 2008) and the nutrition and growth of
the embryo. Owens et al. (2001) and Cross et al. (2003), for in-
stance, found a higher rate of abortion in Picea abies and
Linum usitatissimum, respectively, under higher temperatures
during embryo development. An indirect negative effect of tem-
perature on the viability of SP3 seeds due to malfunctions during
the pre-fertilization development of the female gametophyte
could not be detected, as GDD
.08C
during that period had no sig-
nificant effects.
Warmer temperatures during the last year before sampling (for
SP2 and SP3 seeds) led to shorter ripening times. The influence
of temperature on ripening time can be explained by an altered
development of the male and female gametophytes and their
interactions. As common juniper can be considered a cold-
adapted species (cf. its relatively northerly distribution range
and the assumption of its survival in Central Europe during the
last glacial maximum; Michalczyk et al., 2010), there is a prob-
ability that the mechanism of delayed fertilization to overcome
shorter reproduction seasons has developed in this species
(Willson and Burley, 1983). Longer reproduction seasons due
to higher temperatures can reduce the need for such mechanisms,
leading to a higher chance of shorter ripening times.
To further our understanding of the role of higher temperature
in the described processes, research on a biochemical level is
needed.
Effects of nitrogen and potentially acidifying deposition
Acidifying depositions appear to have negative impacts on
seed viability after SP3. We can assume that nitrogen deposition
has a similar effect as both variables were highly correlated. This
effect was almost absent after seed phase two. In addition, the
effects of temperature and potentially acidifying depositions
had a significant interaction after seed phase three: in populations
with low potentially acidifying depositions, the negative effect of
temperature was pronounced, while the effect was slightly
reversed in populations with high depositions. Seeds sampled
from individuals growing in areas with high nitrogen depositions
also ripened more in 2 years instead of 3 years.
Our results agree with those of different studies demonstrating
that nitrogen (e.g.Ve rgeer et al.,2003;Li etal.,2011) or poten tial-
ly acidifying depositions (Wertheimand Craker, 1987;Feret et al.,
1990;Munzuroglu et al., 2003;Vergeer et al., 2003)negatively
affect plant performance in terms of seed quality. However,
other studies have shown that nitrogen depositions can also in-
crease seed quality (e.g. Drenovsky and Richards, 2005).
Nitrogen and potentially acidifying depositions can influence
seed viability in a direct way by creating nutrient imbalances and
causing decreased uptake and leaching of cations including K
+
,
Ca
2+
and Mg
2+
in the plant (Bobbink et al., 1992;Krupa, 2003),
leading to nutritional deficiencies (e.g. Pearson and Stewart,
1993). As for the influence of temperature, the biochemical
mechanisms behind the effects on seed viability need more re-
search. For example, Ca
2+
plays a role in the control of conifer
pollen tube growth (Fernando et al., 2005), and detoxificationpro-
ducts such as arginine, needed in case of a higher uptake of NH
4
+
and NH
3
through canopy exchange (Krupa, 2003), can have dis-
turbing effects (Durzan and Chalupa, 1968;Durzan, 2002).
Nitrogen and potentially acidifying depositions can also indir-
ectly influence plant performance as they cause a reduction of
mycorrhizae associations in several species (Malcova
´et al.,
1999;Krupa, 2003). For common juniper, symbiosis with
mycorrhiza [especially with arbuscular mycorrhiza (Thomas
et al. (2007)) can be important; Bakker (1988) suggested a pos-
sible relationship between the presence of mycorrhiza and the
viability of J. communis shrubs.
TABLE 3. Model selection statistics for the analysis of the effects of GDD
.08C
during the year before sampling, nitrogen deposition,
their interaction the, bedrock type, cone density, shrub height and needle loss on the ripening time of the seeds
Intercept
Growing degree-days
(GDD) year before
sampling
Nitrogen
deposition GDD:ND
Bedrock
type
Infection rate with
M. bipunctatus
Cone
density
Shrub
height
Needle
loss d.f. DAICc Weight
6.18 –2.29 ×10
23
–0.553 1.06 ×10
24
+15.8+++15 0 0.22
2.14 –1.20 ×10
23
–0.156 +17.5+++14 0.11 0.21
3.17 –1.47 ×10
23
–0.132 23.0+++13 1.08 0.13
8.24 –2.69 ×10
23
–0.714 1.43 ×10
24
+ +++14 1.15 0.13
7.27 –2.56 ×10
23
–0.518 1.03 ×10
24
20.0+++14 1.22 0.12
–1.91 –0.188 +19.6+++13 1.64 0.10
2.84 –1.21 ×10
23
–0.184 + +++13 2.67 0.06
–1.15 –0.218 + +++12 3.99 0.03
Importance 0.87 1 0.47 1 0.78 1 1 1 – –
+, a factorial variable is included in the model.
DAICc, difference in values of the corrected Akaike Information Criterion between a model and the best model; weight, Akaike weight indicating the relative
support for the model; importance, the relative importance of the explanatory variables based on the sum of the Akaike weights of the models in which the
variables appear.
Gruwez et al. — Negative effects of global change on the seed viability of juniper 497
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Our results show an effect of potentially acidifying deposi-
tions only after seed phase three. One would expect a larger
effect after seed phase two since, as in most conifers, seeds are
largely autonomous shortly after fertilization. However, it is pos-
sible that anomalies during seed phase two (e.g. a badly devel-
oped megagametophyte due to nutrient deficits) only lead to
seed abortion during seed phase three, when the megagameto-
phyte nourishes the developing embryo. Similarly, nutrient
imbalances and signalling disturbance can also alter the ripening
time of the seed.
The effect of ripening time on seed viability was absent after
seed phase two and of much less importance than the effect of po-
tentially acidifying depositions and temperature after seed phase
three. Thus, there is no clear evidence that the negative effects of
increased temperatures, nitrogen depositions and potentially
acidifying depositions on seed viability are acting through
changed ripening duration of the seeds.
The negative influences of temperature, nitrogen deposition
and potentially acidifying deposition on the viability of both
SP2 and SP3 seeds of common juniper indicate that these
drivers of global change affect different key processes of the
sexual reproductive cycle of J. communis including pollen tube
growth, megagametogenesis and embryo development. Thus,
the failure of natural regeneration in many European juniper
populations might be attributed to climate warming as well as
high atmospheric deposition of nitrogen and sulfur.
SUPPLEME NTARY DATA
Supplementary data are available online at www.aob.oxford-
journals.org and consist of the following. Table S1: additional in-
formation for the sampled populations. Table S2: detail of the
seasons that were taken into account for calculation the
GDD
.08C
of the spring of pollination, the summer of fertilization
and the year of embryo development for SP2 seeds with a ripen-
ing time of 3 years and 2 years, and for SP3 seeds with a ripening
time of 3 years and 2 years. Table S3: Pearson’s correlation
between three environmental variables. Figure S1: location and
population number of the sampled juniper populations.
ACKNOWLEDGEMENTS
We are grateful to Natalia Filipowicz, Bernard Pre
´vosto, Fiona
Cooper, Cristina Blandino, Anna Shevtsova, Ge
´rald Berger,
Lena Ward, Daniel Garcı
´a, Eje Rose
´n, Massimo Nepi, Stefan
Mayr, Aure
´lien Jamoneau, Guilaume Decocq, Inga Michalczyk,
Dieter Michalczyk, Jake Alexander, Annette Kolb, Dirk, Lutz
Eckstein, Tobias Donath, Sara Cousins, Marc Deconchat, Bente
Graae, Jo
¨rg Brunet, Chris Melhuish, Chris Ford, Wolfgang
Petrick, Thilo Heinken, Ana Isabel Gar
´a-Cervigo
´n Morales,
Jose
´Miguel Olano Mendoza, Adria
´n Escudero, Georges
Kunstler and Gnesotto Massimiliano for their help with the seed
sampling, and to Luc Willems for help with the processing of
the seeds. This paper was written while R.G. was funded by the
Special Research Fund of Ghent University (BOF). P.D.F. and
A.D.S. held a post-doctoral fellowship from the Research
Foundation-Flanders (FWO). O.L. was funded by IRC. P.V.
held a scholarship from the Flemish Institute for Technological
Research (VITO).
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... Despite the ecological plasticity of Juniperus communis [11,13], in many European countries, researchers observe the decline in its populations [18,19]. Among the threatened populations are those in the Czech Republic [20], some regions of England and Ireland [21,22], the Netherlands, and Belgium [23]. ...
... Among the threatened populations are those in the Czech Republic [20], some regions of England and Ireland [21,22], the Netherlands, and Belgium [23]. The decline and recovery of Juniperus communis are influenced by the wide range of biotic, abiotic, and anthropogenic factors, such as land use changes, climate change, and increased pressure by forest management [13,18,19,[22][23][24][25]). In Lithuanian populations, only 15 to 34% of Juniperus communis individuals can be evaluated as healthy [25][26][27]. ...
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Although common juniper (Juniperus communis L.) is a widely spread species and important for the forest biodiversity and economy in many European countries, it remains one of the least studied coniferous species. This research is the first attempt to evaluate the factors affecting the increment of Juniperus communis in Lithuanian populations. The aim of this article is to evaluate the patterns of radial increment in Juniperus communis and to identify the key factors influencing the increment. We collected stem discs from 160 junipers in 8 stands distributed in the different regions of Lithuania and performed the tree-ring analysis. All studied junipers expressed a pronounced eccentricity of the stem. The results of our study revealed four patterns of Juniperus communis’ radial increment, which are strongly dependent on the granulometric properties of the soil and hydrologic conditions. The effect of climatic conditions on the Juniperus communis increment was strongly dependent on the terrain; however, most of the junipers had a positive reaction to the temperatures in April, July, and August and to the precipitation in February.
... This abrupt rise would have initiated major biological responses [92,106], including rapid movement through initial Holocene successional communities [107] to the establishment of closed woodland in the warmer southerly areas, where their respective temperature tolerances would have allowed birch to outcompete and thus quickly suppress the light-demanding Juniperus [108]. Warmer temperatures inhibit Juniperus dispersal and seed viability [109], giving Betula a competitive advantage [110]. This would not have occurred at the northern end of the transect where temperature would have been lower [59,62], accounting for the spatial difference in the abundance of juniper and birch, the main shrub/woodland components. ...
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... These studies contrast with what we observed in Phragmites, where Phragmites from more nutrient polluted regions (Northeast & Midwest) were less sensitive to local nitrogen levels than those from the historically less-polluted Southeast. Several experimental studies have shown that nitrogen fertilization decreased seed viability in Succisa pratensis (Vergeer et al. 2003), Juniperus communis (Gruwez et al. 2014), and a variety of subarctic plants (Milbau et al. 2017). Nitrate can increase seed viability (Ronnenberg et al. 2011;Baskin and Baskin 2014), but studies in other grass species have generally found no effect on seed viability (Wagner et al. 2001;Torres et al. 2009Tullos & Cadenasso 2016. ...
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Seedling recruitment is an important mode of establishment utilized by many invasive plants. In widespread invasive plants, regional variation in the rates of seedling recruitment can contribute to differences in invasion intensity across regions. In this study, we examined regional variation in reproductive traits and seedling performance in a cosmopolitan invasive wetland grass, Phragmites australis . We tested whether nitrogen levels and regions with different histories and intensities of invasion would affect reproductive traits and seedling performance. We sampled invasive Phragmites inflorescences from 34 populations across three regions in North America: The Northeast (old, most intense invasion), the Midwest (recent, intense invasion), and Southeast (recent, sparse invasion). We hypothesized that Northeast Phragmites populations would have the highest reproductive output and seedling performance, and that populations experiencing high nitrogen pollution would have higher reproductive output and seedling performance under high nitrogen conditions. We found that populations in the Northeast had the highest inflorescence mass, as expected. We also found that despite sparse distribution of Phragmites in the Southeast, populations from the Southeast displayed a high potential for sexual reproduction. However, increasing watershed-level nitrogen (kg/km ² ) decreased percent seed germination in Southeastern populations, suggesting that Southeastern populations are sensitive to rising nitrogen levels. While elevated nitrogen improved seedling performance through increased belowground growth in Southeastern Phragmites seedlings, elevated nitrogen decreased belowground growth in Midwestern seedlings. These results suggest that the southeastern region of North America may be primed to become an emergent invasion front of Phragmites , warranting more research into the possible management of Phragmites spread in the region.
... In general, Juniperus species, including Juniperus excelsa, present a high proportion of empty seeds (Juan et al., 2006;Bonner, 2008;Gruwez et al., 2014;Pinna et al., 2014). This is probably due either to sub-optimal climatic conditions (Hedhly et al., 2009;Verheyen et al., 2009), which affect pollination, or due to inbreeding depression amongst the fragmented populations (García & Zamora, 2003;Castilleja-Sánchez et al., 2016). ...
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... When it comes to embryo development, higher temperature can sometimes inhibit embryo development, as in the case of Aciphyllya glacialis (Hoyle et al. 2014). Elevated temperatures have also been associated with a decrease in seed viability, as suggested for Acacia lasiocalyx and Juniperus communis (Gruwez et al. 2014(Gruwez et al. , 2016Cochrane 2017a). On the other hand, higher temperatures can lead to increased seed viability in species living in cold areas; this is exemplified by some conifers, such as Picea mariana, whose embryos matured faster under higher temperature (Sirois et al. 1999), and by the tropical tree Trichilia emetica (Sershen et al. 2014). ...
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Article
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For the study of the ionomic parameters of Juniperus communis needles, fourteen sites covering most of the territory of Lithuania and belonging to distinct habitats (coastal brown dunes covered with natural Scots pine forests (G), Juniperus communis scrubs (F), transition mires and quaking bogs (D), subcontinental moss Scots pine forests (G), and xero-thermophile fringes) were selected. Concentrations of macro-, micro-, and non-essential elements were analyzed in current-year needles, sampled in September. According to the concentrations of elements in J. communis needles, the differences between the most contrasting populations were as follows: up to 2-fold for Mg, N, K, Ca, and Zn; 2- to 7-fold for P, Na, Fe, Cu, Al, Cr, Ni, and Pb; and 26- to 31-fold for Mn and Cd. The concentrations of Cd, Cr, and Ni in needles of J. communis did not reach levels harmful for conifers. When compared to all other habitats (B, F, G, and E), the populations from transition mires and quaking bogs (D) had significantly lower concentrations of main nutritional elements N (12176 µg/g d. m.), P (1054 µg/g d. m.), and K (2916 µg/g d. m.). In Juniperus communis scrubs (F), a habitat protected by EUNIS, the concentration of K in the needles was highest, while Zn and Cu concentrations were the lowest. Principal component (PC) analyses using concentrations of 15 elements as variables for the discrimination of populations or habitats allowed authors to distinguish F and B habitats from the E habitat (PC1) and F and D habitats from the G habitat (PC2). Discriminating between populations, the most important variables were concentrations of P, N, Mg, Ca, Cu, and K. Discriminating between habitats, the important variables were concentrations of N and P.
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To examine the effect of the temperature on the development of reproductive organs, potted plants of five year old 'Hakuho' peach were exposed to constant temperatures of 15°C, 20°C, 25°C, 30°C, and natural conditions. The rate of flower and leaf bud burst, and flowering were recorded every day. The characteristics of reproductive organs in each treatment were examined by measuring flower size, pollen germinabitily, pollen tube elongation, development of embryo sacs, and fruit set. Percentage of flower bud bursting at 30°C was about 80% within 3 d after the onset of the treatment, while it took 18 d to reach the same percentage in the control. Flower bud break preceded leaf bud break in all treatments. Flowering was earliest at 30°C, and the period from bud burst to flowering was as short as 3-4 d. Flower sizes were significantly decreased with increasing temperature. The pollen germination was negatively affected by higher temperature, but the pollen tube elongation in the pistils was faster at higher temperatures. On the other hand, the development of the embryo sac at high temperature was considerably less satisfactory than that at lower temperature and under field conditions. High temperatures also significantly reduced the percentages of fruit set. The results suggested that the high temperature above 25°C interferes with the normal development of reproductive organs especially embryo sac, and causes poor fruit set in 'Hakuho' peach.
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What determines the number and size of the seeds produced by a plant? How often should it reproduce them? How often should a plant produce them? Why and how are seeds dispersed, and what are the implications for the diversity and composition of vegetation? These are just some of the questions tackled in this wide-ranging review of the role of seeds in the ecology of plants. The authors bring together information on the ecological aspects of seed biology, starting with a consideration of reproductive strategies in seed plants and progressing through the life cycle, covering seed maturation, dispersal, storage in the soil, dormancy, germination, seedling establishment, and regeneration in the field. The text encompasses a wide range of concepts of general relevance to plant ecology, reflecting the central role that the study of seed ecology has played in elucidating many fundamental aspects of plant community function.
Book
1. Introduction 2. Estimation 3. Hypothesis testing 4. Graphical exploration of data 5. Correlation and regression 6. Multiple regression and correlation 7. Design and power analysis 8. Comparing groups or treatments - analysis of variance 9. Multifactor analysis of variance 10. Randomized blocks and simple repeated measures: unreplicated two-factor designs 11. Split plot and repeated measures designs: partly nested anovas 12. Analysis of covariance 13. Generalized linear models and logistic regression 14. Analyzing frequencies 15. Introduction to multivariate analyses 16. Multivariate analysis of variance and discriminant analysis 17. Principal components and correspondence analysis 18. Multidimensional scaling and cluster analysis 19. Presentation of results.
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(1) The life-span of juniper, Juniperus communis communts L. appears to be about 100 years in southern England on the chalk; whereas in the north of England exceptional individuals reach over 200 years. (2) Longevity may be related to growth rate; slower growing junipers can live longer, and the life-span can be correlated with the growth rate in the early years. Variability of growth rates makes comparison of trunk girths of specimens from different sites very unreliable as a basis for estimating age. (3) Seed production in older junipers is reduced. Sex ratios are often not 1.1, and past history may be a factor in explaining sex ratios of present-day populations. (4) Juniper populations are often roughly even-aged, and in these cases study of the age and expected longevity of the bushes allows for prediction of the ultimate life-span of such populations in the absence of regeneration. This is relevant to the management of juniper on nature reserves.