ORIGINAL PAPER

Broadleaf seedling responses to warmer temperatures ‘‘chilled’’by late frost that favors conifers

Nicholas Fisichelli • Torsten Vor • Christian Ammer

Received: 29 November 2012 / Revised: 17 January 2014 / Accepted: 21 January 2014

� Springer-Verlag Berlin Heidelberg 2014

Abstract Climate change includes not only shifts in

mean conditions but also changes in the frequency and

timing of extreme weather events. Tree seedlings, as the

potential future overstory, are responding to the selective

pressures of both mean and extreme conditions. We

investigated how increases in mean temperature and the

occurrence of late spring frosts affect emergence, devel-

opment, growth, and survival of 13 native and non-native

broadleaf and conifer tree species common in central

Europe. Three temperature levels (ambient, ?3, and

?6 �C) and three spring frost treatments (control, late, and

very late) were applied. Development responses of first-

year seedlings to warmer temperatures were similar in

direction and magnitude for broadleaf and conifer species.

Stem size also increased with rising mean temperature for

most species, though broadleaf species had maximal height

advantage over conifer species in the warmest treatment.

Sensitivity to frost differed sharply between the broadleaf

and conifer groups. Broadleaf survival and stem length

exhibited strong reductions due to frost events while

conifer species only showed minor decreases in survival.

Importantly, more rapid development and earlier leaf-out

in response to warmer temperatures were associated with

increased mortality from frost for broadleaf species but

decreased mortality for conifer species. This research

suggests that compositional shifts in the direction of spe-

cies favored by increasing mean temperatures may be

slowed by extreme events, and thus, the occurrence and

impacts of such weather events must be acknowledged and

incorporated into research and forest planning.

Keywords Broadleaf seedling � Climate change � Conifer

seedling � Extreme weather events � Phenology � Spring

frost � Survival

Introduction

Forest management in the face of multiple global change

agents must apply flexible approaches to foster healthy and

productive forests (Millar et al. 2007; Bolte et al. 2009;

Sohn et al. 2013). Diversifying monospecific stands,

notably conifer stands expected to be threatened by

droughts and more virulent pests, is one approach to dif-

fusing risk (Ammer et al. 2008; Knoke et al. 2008; Kolling

et al. 2009; Overbeck and Schmidt 2012). However,

determining which species may be most successful under

future climatic conditions is not clear. There are not only

uncertainties in the sensitivity of various species to

changing climate (for European beech, see, e.g., Leuschner

et al. 2001; Rennenberg et al. 2004; Ammer et al. 2005),

but also uncertainties in the magnitude of mean tempera-

ture increases and shifts in the seasonal timing and fre-

quency of extreme events (Jentsch et al. 2007). For

example, increasing mean temperatures and a longer

growing season are likely to favor species best able to

Communicated by G. Brazaitis.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10342-014-0786-6) contains supplementarymaterial, which is available to authorized users.

N. Fisichelli (&) � T. Vor � C. Ammer

Department of Silviculture and Forest Ecology of the Temperate

Zones, Georg-August-Universitat Gottingen, Busgenweg 1,

37077 Gottingen, Germany

e-mail: nfisichelli@gmail.com

N. Fisichelli

Natural Resource Stewardship and Science, U.S. National Park

Service, Fort Collins, CO, USA

123

Eur J Forest Res

DOI 10.1007/s10342-014-0786-6

maximize productivity under the changed conditions,

whereas increased climate variability such as late spring

frost events may select for species with more conservative

growth strategies (Hufkens et al. 2012). Research is needed

to understand how co-occurring broadleaf and conifer tree

species respond to changes in climate means and extremes

at the earliest stages of development and thus which spe-

cies may thrive under future conditions.

Spring average temperatures are increasing in many

regions; however, this does not necessarily mean that late

spring frost dates are retreating at the same rate or that the

risk of frost damage is decreasing (Meehl et al. 2000; Gu

et al. 2008; Inouye 2008). Changes in the frequency and

timing of late spring frosts will depend as much on changes

in variance as in climate means (Rigby and Porporato

2008). For example, a 1 �C change in the standard devia-

tion of the temperature distribution will influence the fre-

quency of late spring frosts more than a 1 �C change in

mean temperature (Meehl et al. 2000). Recent late spring

frost events in eastern North America have impacted for-

ests across large regions (Gu et al. 2008; Augspurger 2009;

Hufkens et al. 2012). Interspecific differences in growth

strategies and susceptibility to damage resulted in shifts in

competitive dynamics and an advantage for species less

impacted by spring frost (Hufkens et al. 2012). In European

forests, the potential ecological importance of late spring

frosts is exemplified by Fagus sylvatica, which due to late

spring frost events is precluded from areas with otherwise

sufficiently high growing season temperatures (Peters

1992).

Development responses to warming in spring may alter

risk of frost damage. Plant species face a trade-off between

maximizing growing season length and protecting against

frost damage (Saxe et al. 2001). Investments in cold tol-

erance, for example, by conifer species, reduce growth

rates, and frost avoidance in the form of late-onset spring

growth may confer a competitive advantage to neighboring

stems that emerged at an earlier time (Hannerz et al. 1999;

Loehle 1998). Conversely, early-onset growth of frost-

sensitive tissue, such as by some broadleaf species, could

lead to greater frost damage (Cannell and Smith 1986;

Inouye 2000). However, more rapid development beyond

the most frost-sensitive stages, especially in a warmer

world, could reduce risk of frost damage for some species

(Coursolle et al. 1998; Kreyling et al. 2012).

In this study, we examined how potential future climatic

conditions, including warmer temperatures and late spring

frost events, impact first-year seedling emergence, devel-

opment, growth, and survival of tree species commonly

grown in central Europe. We hypothesized that warming

temperatures would lead to earlier emergence, more rapid

development, and increased growth of seedlings and that

responses would be greater for broadleaf than conifer

species. Conversely, we hypothesized that late spring frost

events would favor conifer species over broadleaf species,

due to higher survival rates. Furthermore, we expected that

the combination of increased temperatures and very late

frost would lead to the greatest impacts on plant perfor-

mance. These data will inform managers on how future

variations in climate may impact first-year seedling per-

formance and potentially the direction and rate of forest

change.

Methods

A growth chamber experiment was conducted in the spring

and summer of 2012 at Georg-August-Universitat Gottin-

gen, Germany, and included a fully crossed two-way fac-

torial design with temperature (three levels: ambient, ?3,

and ?6 �C) and frost (three levels: control, late, and very

late) treatments. Seeds from 22 tree species commonly

found growing in central Europe were collected in the fall

of 2011 in central and northern Germany (Lower Saxony)

and processed and cold stratified (generally at 3 �C for

60–90 days) by a professional nursery. Seeds were planted

in 5-l plastic pots (17 9 17 9 17 cm) filled with 2,000 g

of potting material (‘‘Einheitserde SP VM’’ peat, clay, and

sand mix, pH = 5.8, nitrogen concentration 0.2 %). Of the

original 22 tree species, only 13 had sufficient emergence

rates ([*7 %) to permit analyses (Table 1). This included

most of the common native and non-native broadleaf and

conifer species present in central European forests. The

number of replicate pots per warming treatment was gen-

erally five (range 4–9), though the number of seeds and

pots per species varied with seed availability and seed size

(e.g., 882 seeds in 18 pots for Picea abies and 432 seeds in

27 pots for Fagus sylvatica; see Table 1).

The experiment was conducted within climate-con-

trolled growth chambers (BBC, Brown Boveri-York,

Hamburg, Germany). Temperature levels (day/night: 15/8,

18/11, and 21/14 �C) were based on late spring/early

summer values (Gottingen, Germany 1970–2000) and

potential temperatures by the end of the twenty-first cen-

tury (EEA 2012). All growth chambers began with a day/

night temperature of 10/6 �C, and temperatures were

increased incrementally over 14 days to reach experiment

levels. The first day that maximum treatment temperatures

were reached was considered day 1 of the experiment. Pots

were watered two to three times per week to field capacity,

with frequency increasing with rising temperatures.

Humidity in all chambers was kept at 60 % during the day

and 75 % at night. Light availability within the chambers

was similar to moderately open forest understory condi-

tions (PAR * 150 lmols/m2/s), and day length began with

12 h and increased to 16 h. As only three growth chambers

Eur J Forest Res

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were available for the study, pot location within chamber

was randomized weekly and pots were rotated among

chambers every 2 weeks to account for any within- or

among-chamber-treatment effects. Two replications of the

late spring frost treatment occurred on days 27 and 28 and

two replicates of the very late frost on days 46 and 47. Pots

receiving the frost treatment were moved to a frost cham-

ber in the evening and cooled at a rate of 3 �C per hour,

held at -5 �C for 2 h, and then warmed again at a rate of

3 �C per hour. Pots were packed in loose potting soil to

insulate the roots from freezing, and temperatures 2 cm

below the soil surface remained above 0 �C during all frost

treatments.

Pots were surveyed twice per week to determine the

percentage of seedlings emerging (emergence is defined as

the epicotyl breaking the soil surface) and development

stage (emerging, 1st leaf fully expanded). For conifers, the

first leaf fully expanded stage was reached when the first

true needles were [1 cm in length. Survival of all stems

was monitored for 19 days after each frost treatment. Total

stem length was measured on day 62.

Seedling responses to experimental treatments and

interactions were analyzed with linear mixed-effects

models and pot as a random effect (i.e., random intercept to

account for autocorrelation of stems within the same pot) in

R (v. 2.12; R Development Core Team 2008). Emergence

day, leaf-out day, and stem length responses were assessed

with linear mixed-effects models and a Gaussian error

distribution using the ‘‘nlme’’ package (Pinheiro et al.

2009). As the first frost was not applied until after the

fastest-developing species in the ?6 �C treatment level had

leafed out, emergence and leaf-out analyses only included

the temperature treatment. Comparisons of factor levels

(Tukey’s test) were carried out using the ‘‘multcomp’’

package (Hothorn et al. 2008). The percentage of seedlings

emerging and survival (of aboveground tissue) post-frost

were assessed with generalized linear mixed-effects mod-

els and a binomial error distribution using the ‘‘lme4’’

package (Bates et al. 2011). Likelihood ratio tests were

utilized to formally compare emergence percentage and

survival models and test whether temperature and frost

improved model performance over simpler models with

each variable individually removed (Crawley 2007). Sur-

vival post-frost was also compared among development

stages. All figures shown include the same eight species,

four broadleaves and four conifers, which had the largest

sample sizes and are representative of responses for each

functional group.

Results

Emergence

The number of species responding to warming treatments

increased with development stage (Table 2). The percent-

age of seedlings emerging varied with temperature treat-

ment for five out of 13 species (see Electronic

Supplementary Material, Online Resource 1 for all pair-

wise comparisons). Acer pseudoplatanus was the only

species to exhibit a decrease in the percentage of seedlings

emerging with increasing temperature, from 58 ± 2 %

(mean ± se) at ?6 �C to 73 ± 2 % at ambient temperature

(z = -2.86, p = 0.01). The only other broadleaf species

with an emergence percentage shift was Juglans regia,

where the ?6 �C treatment emergence was 69 ± 8 % and

ambient temperature emergence was 40 ± 3 % (z = 2.71,

p = 0.02). Three conifer species exhibited increased

emergence with warming treatments. For Abies alba,

emergence in the ?3 and ?6 �C treatments (both

9 ± 3 %) was significantly higher than under ambient

temperature (3 ± 0.5 %; z = 2.82, p = 0.01; z = 2.70,

p = 0.02, respectively). Similar effects were found for

Picea abies, with the ?3 and ?6 �C treatments (70 ± 3

and 75 ± 4 %, respectively) having higher emergence

rates than with ambient conditions (53 ± 3 %; z = 3.46,

p = 0.01; z = 4.43, p = 0.001, respectively). Finally, for

Table 1 Broadleaf and conifer tree species commonly found in

central European forests and included in this study

Species Seeds/

pot

Pots Total

seeds

Emergence

(%)

Native

range

Broadleaf species

Acer

pseudoplatanus

25 15 375 65.1 Europe

Fagus sylvatica 16 27 432 68.1 Europe

Juglans regia 9 15 135 57.0 Europe

Quercus

petraea

6 12 72 40.3 Europe

Quercus robur 9 15 135 37.8 Europe

Robinia

pseudoacacia

36 15 540 18.7 Eastern

North

America

Conifer species

Abies alba 49 15 735 7.1 Europe

Abies grandis 25 15 375 14.7 Western

North

America

Larix decidua 49 15 735 40.1 Europe

Larix

kaempferi

49 15 735 65.0 Japan

Picea abies 49 18 882 65.6 Europe

Pinus sylvestris 49 15 735 87.9 Europe

Pseudotsuga

menziesii

49 15 735 11.7 Western

North

America

Eur J Forest Res

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Pseudotsuga menziesii, more seedlings emerged in the

?6 �C treatment (19 ± 3 %) than under ambient temper-

ature (5 ± 1 %, z = 4.45, p = 0.002).

The amount of time required for emergence (emergence

day) decreased with increasing temperature for nine out of

13 species, and no species showed a later emergence date at

a higher temperature (Table 2, Online Resource 2). Fur-

thermore, trends were similar among early- and late-

emerging species, with three out of four earliest and three

out of four latest species exhibiting significant responses to

temperature. For the earliest species, Robinia pseudoacacia,

seedlings in the ?6 �C treatment (day 1 ± 0.5; mean ± se)

emerged significantly earlier than in the ?3 �C treatment

(day 6 ± 0.3; z = -3.46, p = 0.002) and ambient treatment

(day 9 ± 2; z = -5.08, p \ 0.0001). Pinus sylvestris stems

in the ambient treatment emerged on average on day

10.9 ± 0.8, ?3 �C on day 8.1 ± 0.8, and ?6 �C on day

5.7 ± 0.5, with all three treatments significantly different

from one another (p \ 0.02). For Fagus sylvatica, seedlings

emerged at similar times in the ?3 and ?6 �C treatments

(days 9 ± 0.5 and 8 ± 0.8, respectively) and both were

significantly earlier than under ambient conditions (day

13 ± 0.7, p \ 0.0001 in both comparisons).

Late-emerging species included the three largest seeded,

hypogeous species, Juglans regia, Quercus petraea, and

Quercus robur, and the conifer Pseudotsuga menziesii. For J.

regia, emergence was significantly later in the ambient

treatment (day 65 ± 9) than in ?3 �C (day 40 ± 2; z =

-3.98, p = 0.0002) and ?6 �C treatments (day 30 ± 3;

z = -5.58, p \ 0.0001). Stems in the ?6 �C treatment

emerged over 19 days earlier than under ambient tempera-

ture for both Q. robur and P. menziesii (p value \0.02 for

both species). Quercus petraea emerged on average on day

56 ± 5, the earliest Q. robur stems (in the ?6 �C treatment)

on day 46 ± 3, and the earliest P. menziesii stems (?6 �C

treatment) on day 61 ± 1. Thus, these three species

emerged, on average, after the very late frost treatment.

Leaf-out

The date of first leaf fully expanded (leaf-out day) shifted

to an earlier time with heating for all species (Table 2;

Fig. 1, the eight species shown in figures had the largest

samples and were representative of variation in responses

for each functional group). Warming of ?6 �C resulted in

significantly reduced leaf-out time compared with ambient

for all 13 species (all p values\0.01) (Online Resource 3);

for example, reductions in development time for broadleaf

species included 14.1 ± 2 days for A. pseudoplatanus

(z = -6.74, p \ 0.0001), 19 ± 2 days for F. sylvatica

(z = -8.45, p \ 0.0001), 28.5 ± 4 days for J. regia

(z = -7.21, p \ 0.0001), and 32 ± 2 days for R. pseudo-

acacia (z = -13.70, p \ 0.0001) (Fig. 1a–d). Similar

responses were found for conifer species, with the ?6 �C

warming causing leaf-out to be earlier than in the ambient

treatment by 19 ± 6 days for Abies grandis (z = -3.44,

p = 0.002), 17 ± 2 days for Larix decidua (z = -6.98,

p \ 0.0001), 22 ± 2 days for P. abies (z = -7.21,

Table 2 ANOVA results of seedling emergence percentage, emergence day, and leaf-out day responses to the fixed effect of temperature (3

levels: ambient, ?3, and ?6 �C)

Species Response: Emergence (%) Emergence day Leaf-out day

den df Trend v2 p Trend F p Trend F p

Acer pseudoplatanus 12 2 8.40 0.01 0 2.76 0.14 / 26.30 <0.0001

Fagus sylvatica 24 0 0.24 0.89 / 17.01 <0.0001 / 39.13 <0.0001

Juglans regia 12 1 8.15 0.02 / 15.95 0.0004 / 26.52 0.0001

Quercus petraea 9 0 4.39 0.11 0 2.26 0.16 / 7.10 0.02

Quercus robur 12 0 1.08 0.58 / 6.89 0.01 / 15.86 0.0006

Robinia pseudoacacia 12 0 0.10 0.95 / 13.44 0.0009 / 95.05 <0.0001

Abies alba 12 1 8.94 0.01 0 2.30 0.14 / 5.59 0.04

Abies grandis 10 0 1.96 0.38 3.93 0.05 / 7.31 0.01

Larix decidua 12 0 5.40 0.07 0 2.28 0.14 / 26.42 <0.0001

Larix kaempferi 12 0 3.52 0.17 / 31.13 <0.0001 / 154.20 <0.0001

Picea abies 15 1 19.80 <0.0001 / 19.83 0.0001 / 57.23 <0.0001

Pinus sylvestris 12 0 3.19 0.20 / 17.54 0.0003 / 242.41 <0.0001

Pseudotsuga menziesii 12 1 15.47 0.000 / 5.74 0.02 / 6.82 0.01

Symbols -/? denote decreases/increases in emergence percentage with increasing temperature; / denotes earlier emergence/leaf-out with

increasing temperature. ‘‘den df’’ is denominator degrees of freedom. Emergence day and leaf-out day responses are from linear mixed-effects

models

Values in bold are significant at p \ 0.05

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p \ 0.0001), and 23 ± 1 days for P. sylvestris (z =

-21.74, p \ 0.0001) (Fig. 1e–h). Temperature differences

of 3 �C caused significant shifts (p \ 0.05) in leaf-out day

for eight out of 13 species when comparing ambient and

?3 �C treatments and also eight out of 13 species when

comparing ?3 and ?6 �C treatments (Online Resource 3).

Growth and survival

Emergence and development responses to temperature treat-

ments shown above were generally similar across broadleaf

and conifer groups, whereas survival and growth responses to

temperature and frost treatments differed more strongly

between these functional groups. Survival of aboveground

tissue varied significantly with temperature for one species

and with frost treatment for eight species (Table 3; Fig. 2).

Similar to the reduction in emergence, A. pseudoplatanus

exhibited a small, though significant reduction in survival with

increasing temperature. Mean survival in the ?3 �C

(86 ± 7 %) and ?6 �C treatments (86 ± 7 %) was lower

than the ambient treatment (97 ± 3 %).

In response to frost, all four broadleaf species had

strongly reduced survival, with the very late event gen-

erally resulting in the greatest mortality (Fig. 2a–d).

Survival for 19 days after the very late frost varied from a

high of 61 ± 9 % for A. pseudoplatanus to a low of

8.5 ± 5 % for J. regia. Conversely, survival was gener-

ally much higher for conifers than for broadleaf species

Fig. 1 Leaf-out day responses to mean temperature for four broadleaf (a–d) and four conifer (e–h) tree species. See Table 2 for ANOVA test

output. Means and standard errors based on pot-level data

Table 3 ANOVA results of

seedling survival responses to

the fixed effects of temperature

and frost

Analyses were run using

generalized linear mixed-effects

models, a binomial error

distribution, and pot as a

random effect. Temperature by

frost interaction was not

significant (see text).

Differences in post-frost

survival by development stage

(emerging vs. leafed-out) were

also tested. Empty cells indicate

insufficient sample sizes, such

as for Q. petraea, Q. robur, and

P. menziesii, which primarily

emerged after frost treatments

Values in bold are significant at

p \ 0.05

Species Survival (prop) Temperature Frost Post-frost survival by

development stage

v2 p v2 p v2 p

Acer pseudoplatanus 0.86 12.45 0.002 68.13 <0.0001 29.14 <0.0001

Fagus sylvatica 0.63 2.73 0.26 176.0 <0.0001 0.84 0.36

Juglans regia 0.62 0.13 0.94 71.99 <0.0001 8.22 0.004

Quercus petraea 1.00

Quercus robur 0.95

Robinia pseudoacacia 0.72 3.82 0.15 55.05 <0.0001 0.04 0.85

Abies alba 0.97

Abies grandis 0.83 4.89 0.09 15.59 0.0004 1.81 0.18

Larix decidua 0.96 0.01 0.99 7.68 0.02 7.10 0.008

Larix kaempferi 0.95 0.01 0.99 9.68 0.008 10.83 0.001

Picea abies 0.95 2.26 0.32 135.3 <0.0001 1.70 0.19

Pinus sylvestris 0.98 1.40 0.50 3.87 0.14 19.02 <0.0001

Pseudotsuga menziesii 1.00

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even though likelihood ratio tests indicated significant

survival responses to frost for several conifers (Fig. 2e–

h). For example, survival after frost events was greater

than 95 % for P. sylvestris, and only one conifer, A.

grandis, had fewer than 88 % of stems survive a frost.

Temperature by frost interactions did not indicate strong

effects on survival. The three broadleaf species with

sufficient samples in each interacting temperature by frost

level did not exhibit significant responses (A. pseudo-

platanus: v2 = 4.08, p = 0.40; F. sylvatica: v2 = 4.29,

p = 0.37; R. pseudoacacia: v2 = 6.31, p = 0.18), and

mortality was too low among the conifer species to reveal

strong interactions.

Post-frost survival by development stage showed

opposing trends between the broadleaf and conifer groups

(Table 3; Fig. 3). For broadleaf species, emerging stems

had higher survival after frost than leafed-out stems while

the trend for conifer species indicated lower mortality risk

for leafed-out individuals compared with emerging stems.

Thus, stems responding to warmer temperatures by devel-

oping more rapidly had lower post-frost survival for

broadleaf species and higher survival for conifers.

Stem length of plants that survived to day 62 of the

experiment varied with temperature and frost treatments

for multiple species (Table 4; Fig. 4, Online Resource 4).

Both broadleaf (4 of 6) and conifer (4 of 7) species showed

Fig. 2 Survival responses to frost treatments for four broadleaf (a-d) and four conifer (e-h) tree species. Survival monitored for 19 days after

frost treatments. See Table 3 for ANOVA test output. Means and standard errors based on pot-level data

Fig. 3 Survival responses to frost by development stage for four broadleaf (a-d) and four conifer (e-h) tree species. Survival monitored for 19

days after frost treatments. See Table 3 for ANOVA test output. Means and standard errors based on pot-level data

Eur J Forest Res

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significantly greater size (p \ 0.05) with increased tem-

perature. For A. pseudoplatanus, F. sylvatica, and J. regia,

a ?6 �C warming significantly increased stem length by

40–60 % over the ambient treatment (Fig. 4a–c). Broadleaf

R. pseudoacacia had the largest increase in stem length

with a ?6 �C warming, almost 500 % (Fig. 4d, note the

y-axis scale). When significant, stem length differences due

to a ?6 �C warming for conifer species were similar to the

first three broadleaf species above, with increases of

25–128 % (Fig. 4e–h).

Unlike warming, frost treatments had much larger

impacts on stem lengths of broadleaf than conifer species

(Table 4; Fig. 4, Online Resource 4). Frost caused stem

length decreases of up to 80 % for broadleaf species, while

no conifer species exhibited a difference in stem length by

frost treatment. Thus, size advantage for broadleaf species

over conifers was greatest under the combination of the

warmest temperatures and lack of frost occurrence. High

mortality and subsequent small sample sizes at the pot level

reduced the ability to detect temperature by frost interac-

tions, although stem-level data suggest a trend toward very

late frosts resulting in greater decreases in size at warmer

temperatures (e.g., F. sylvatica and R. pseudoacacia,

Fig. 4b, d).

Discussion

Our results show that increased mean temperatures and late

frost events impact emergence, development, growth, and

Table 4 ANOVA results of

seedling stem length responses

to the fixed effects of

temperature, frost, and the

interaction

Analyses were run using linear

mixed-effects models, a

Gaussian error distribution, and

pot as a random effect. Empty

cells indicate sample sizes that

were too small to carry out

statistical tests. ‘‘den df’’ is

denominator degrees of freedom

Values in bold are significant at

p \ 0.05

Species n den df Temperature Frost Temp 9 frost

F p F p F p

Acer pseudoplatanus 207 6 11.42 0.009 5.94 0.04 1.37 0.35

Fagus sylvatica 189 15 6.01 0.01 11.74 0.0009 1.55 0.24

Juglans regia 55 8 14.17 0.002 23.10 0.0005

Quercus petraea 18 2 2.29 0.30 0.63 0.61

Quercus robur 31 3 3.35 0.17 1.05 0.45

Robinia pseudoacacia 66 4 29.03 0.004 6.04 0.06 3.67 0.12

Abies alba 42 4 1.62 0.31 1.20 0.39 4.47 0.09

Abies grandis 46 5 0.55 0.61 0.47 0.65 3.12 0.12

Larix decidua 176 6 26.56 0.001 3.09 0.12 0.95 0.49

Larix kaempferi 209 6 48.53 0.0002 0.11 0.89 0.88 0.53

Picea abies 228 9 60.07 <0.0001 2.08 0.18 2.83 0.09

Pinus sylvestris 193 6 36.94 0.0004 0.02 0.98 1.80 0.25

Pseudotsuga menziesii 25 5 4.17 0.09 0.80 0.50

Fig. 4 Stem length responses to temperature and frost treatments for four broadleaf (a–d) and four conifer (e–h) tree species. Note the different

y-axis scaling for (d) R. pseudoacacia. See Table 4 for ANOVA test output. Means and standard errors based on stem-level data

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survival of tree seedlings at early stages of development.

Emergence and leaf-out responses to warmer temperatures

were generally similar in direction and magnitude for first-

year broadleaf and conifer seedlings. Both groups also

increased size with temperature, though height advantage

of broadleaf species over conifers increased with temper-

ature. Sensitivity to spring frost differed sharply between

these two functional groups, with broadleaf survival and

stem length exhibiting strong reductions due to frost events

and conifer species showing only minor decreases in sur-

vival. Furthermore, more rapid development in response to

warmer temperatures was associated with increased mor-

tality from frost for broadleaf species but decreased mor-

tality for conifer species. This research indicates that the

magnitude of warming and frequency and timing of future

frost events may in part determine the relative performance

of broadleaf and conifer seedlings in central European

forests.

Seedling establishment, growth, and ascension into lar-

ger size classes are bottleneck phases of population growth

(Walck et al. 2011), and small differences in relative per-

formance may be sufficient to tip competitive dynamics in

favor of species or provenances better adapted to current

climatic conditions. Frost-tolerant conifers were unable to

keep pace with the growth rates of broadleaf species,

especially under the warmest mean temperatures (Loehle

1998). In addition to obvious physiological differences

between functional groups, there was also wide variation in

emergence responses within the broadleaf group that could

shift competitive dynamics (Hufkens et al. 2012). The three

broadleaf species with the largest seeds, J. regia, Q. pet-

raea, and Q. robur, on average emerged late, and thus,

many individuals avoided frost damage. In contrast, the

small-seeded R. pseudoacacia emerged very early and

grew very rapidly in the warmest conditions; however, this

aggressive growth strategy was heavily penalized by cli-

mate variability, with large decreases in stem size and

survival after frost. Though not examined here, genetic

diversity within species, such as from multiple prove-

nances, may also result in intraspecific differences in

responses to climate change (Kreyling et al. 2012).

Our experiment looked at responses to means and

extremes in a single year, and multiple extreme events (or

the lack of such events) over multiple years would likely

have compounding effects and result in greater fitness

differences between species. Extreme weather events such

as late frosts can also impact older tree regeneration as well

as overstory trees and overall ecosystem productivity. For

example, broadleaf saplings typically flush their leaves

earlier than overstory trees and produce a large portion of

their photosynthetic carbon gain during this period of high

light availability, and stems forced to refoliate after a frost

will miss this high-light window and may show greater

mortality than was found for first-year seedlings in this

study (Augspurger 2009). Additionally, this research

assessed aboveground vegetative tissue, and frost is typi-

cally more damaging to reproductive tissue (Sakai and

Weiser 1973) and can cause widespread reproductive

failure for a species in a given year (Inouye 2000), illus-

trating that frosts can also impact the relative numbers of

seeds and seedlings in subsequent years after reproduction.

Other manifestations of increased climatic variability

will also impact tree species. Similar to frosts during the

growing season, warm temperature spells during the dor-

mant season can stress broadleaf and conifer trees and lead

to widespread regional forest declines (Bourque et al. 2005;

Lazarus et al. 2006). Increased temperature variability has

been linked to summer heat waves in Europe (Schar et al.

2004), and the combination of late spring frosts and sum-

mer droughts could result in major declines in productivity

and higher mortality for many tree species (Gu et al. 2008).

A single late frost event, by itself, can reduce gross annual

ecosystem productivity by 10 % or more for the subsequent

growing season (Hufkens et al. 2012).

Climate change will also interact with many other fac-

tors to determine the relative success of tree species (Fis-

ichelli et al. 2013). For example, earthworms may interact

with warming temperatures to exacerbate drought condi-

tions (Eisenhauer et al. 2012), while browse pressure by

deer is likely to inhibit growth responses to warming

temperatures (Fisichelli et al. 2012). Increased atmospheric

CO2 concentrations, such as the levels predicted by the end

of the century, lead to heightened frost sensitivity, so

similar frost events under future atmospheric conditions

may result in greater damage and ecosystem productivity

losses (Lutze et al. 2002; Gu et al. 2008). Frost can also

interact with other factors such as browse pressure to

modify growth and mortality (Buckley et al. 1998).

Key attributes close to nature forestry such as mixing

tree species, reliance on natural regeneration, and keeping

shelter or retention trees for decades (Grassi et al. 2003,

Pommerening and Murphy 2004) may help to decrease the

risk of stand loss due to extreme events. First, as shown in

this study, tree species respond differently to such events,

supporting the idea of mixtures being more resistant to

disturbances than monocultures (Pretzsch 2003; Griess

et al. 2012). Second, natural selective pressures at these

early stages seem to foster adaptation to changed climate

conditions (Bilela et al. 2012). Third, silviculture practices

such as retaining overstory trees for their insulating effects

can reduce occurrence and impact of extreme events and

encourage the growth of tree species better adapted to a

warmer world (Buckley et al. 1998).

Understanding which tree species will be most viable

under likely future conditions requires detailed ecophysi-

ological knowledge of species-level responses (Kimball

Eur J Forest Res

123

et al. 2010; Walck et al. 2011) as well as fine temporal and

spatial scale predictions of climatic conditions. Given the

multiple global change factors that must be taken into

account and imprecise forecasts of future conditions, forest

managers must hedge their bets and make decisions that

will be robust under the broadest swath of potential future

scenarios (Lawler 2009; Kolling et al. 2009). Composi-

tional shifts toward species favored by increasing mean

temperatures are likely to be slowed by extreme events,

and thus, the occurrence and impacts of extreme events

must be acknowledged and incorporated into research and

forest planning.

Acknowledgments Financial support was provided by the U.S.

Fulbright Program. Thanks to M. Unger and H. Coners for laboratory

assistance.

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