Plant phenological responses to a long t

Year

Day of year

Year

Day of year 180

Year

Fig. 2 Mean day of year of leaf bud break (a), floral anthesis (b), and leaf senescence (c) for each treatment and study year. C = control, ES = extended season, and ESW = extended season + warming. Error bars represent standard error of mean. Solid trend line repre- sents control (C), small hashed line represents early snow removal (ES), and large hashed line represents early snow removal + soil warming (ESW). No flowering data were collected in 1999, 2001, or 2002.

4526 R . K H O R S A N D R O S A et al. (Fig. 1c). Leaf senescence occurred a mean of 8 days

thaw, and snow-free status of plot) significantly pre- earlier in the experimental treatment plots than in the

dicted the probability of bud break (Table S1). Within control plots, but timing did not differ between the

these explanatory variables, the highest probability of treatment plots. A downward trend was detected

bud break (indicated by a high odds ratio) was associ- between year and DOY, that is, senescence occurred

ated with Polygonum bistorta, the snow removal and earlier in the later years of the project. Negative slopes

warming treatments, soil moisture and timing of snow for the control and treatments suggest a 4-day advance

melt. However, when the analysis was separated by in onset of leaf senescence for the control and 5-day

year, species (specifically Polygonum bistorta) and air advance for the experimental treatments with each

temperature were consistently the best predictors additional study year (Fig. 2c). Year accurately pre-

across all years (Table 1). Photoperiod, depth of thaw, dicted DOY of senescence for the control and experi-

and treatment were also good predictors, although less

mental treatments (C: F 1,3229 = 219.31, P < 0.001; ES:

so than species and air temperature.

F 1,4156 = 366.21, P < 0.001; ESW: F 1,4340 = 404.25,

P < 0.001). Growth form (F 3,9314 = 427.53, P < 0.001) Flowering. When all years were analyzed together, the and the interaction between growth form and treatment

following independent variables were associated with a ( F 6,9314 = 10.26, P < 0.001) also affected the timing of

high probability of flowering: year, species, treatment, leaf senescence. In other words, leaf senescence

air temperature, photoperiod, and depth of thaw. Soil occurred significantly later in the control plots com-

moisture and date of snow melt were not significant pared to the experimental plots in every single growth

predictors in the model. The highest probability of form. Each pairwise comparison among the four

anthesis was associated with Eriophorum vaginatum, air growth forms was also significantly different, with

temperature, and photoperiod (Table S2). On a year-to- evergreen shrubs and graminoids browning up to

year basis, Eriophorum vaginatum, air temperature, and

3 weeks before deciduous shrubs and the forb. depth of thaw were consistently associated with flower- ing, making them the best predictors of flowering

Species-specific responses. Phenological responses to (Table 2). We also found a significant relationship treatment were species-specific. The highest proportion

between flowering frequency and thawing degree days of bud break was recorded in Polygonum bistorta while

for all species (Spearman’s rank correlation = 0.72, the highest proportion of flowering occurred in Eriopho-

P < 0.001).

rum vaginatum. Species significantly affected timing of greening ( F 5,36102 = 288.14, P < 0.001),

Leaf senescence. When all years were analyzed together, ( F 7,2367 = 284.91, P < 0.001), and leaf senescence

flowering

year, species, treatment, air temperature, photoperiod, ( F 7,11707 = 53.44, P < 0.001). The mean day of bud

depth of thaw, and snow-free status of plot significantly break, flowering, and leaf senescence differed signifi-

predicted timing of leaf senescence (Table S3). Of the cantly among experimental treatments and controls for

significant explanatory variables, air temperature, all species except Cassiope tetragona. In general, C. te-

depth of thaw, and year best predicted leaf browning, tragona showed no response to either experimental

(indicated by a high odds ratio). Soil moisture was not treatment. In contrast, Betula nana, Salix pulchra, and

significant. On a year-to-year basis, air temperature, Vaccinium vitis-idaea were highly responsive to both

photoperiod, and depth of thaw most consistently pre- treatments (Fig. 1a–c). The duration of flowering dif-

dicted senescence; these three variables were significant fered significantly between Eriophorum vaginatum and

in 100% of the models (Table 3). Soil moisture, treat-

ment, and snow-free status of plot were significant pre- Duration of flowering did not differ significantly

each of the other species ( F 7,16 = 13.01, P < 0.001).

dictors of leaf senescence for fewer than half of the between any other species. Not only did treatment and

study years.

species affect the timing of each phenological variable, the interaction between species and treatment was also

significant (greening: F 10,36102 = 2.42, P = 0.007; anthe- Delayed effects of air temperature on phenology

sis:

F 14,2367 = 2.46, P = 0.002;

leaf senescence:

We found a significant relationship between air temper-

F 14,11707 = 4.65, P < 0.001). ature of previous years and the frequency of bud break of all species combined; 1-year time lag ( F 1,610 = 137.39, P < 0.001), 2-year time lag (F 1,610 = 175.96, P < 0.001),

Abiotic variables as determinants of phenology and 3-year time lag ( F 1,610 = 156.30, P < 0.001). Each of

Bud break. When all years were pooled together, each the six species was responsive to historic air tempera- of the independent variables (year, species, treatment,

ture. Previous years’ temperature also significantly pre- air temperature, photoperiod, soil moisture, depth of

dicted frequency of flowering across all species; 1-year

C H A N G I N G P H E N O L O G Y O F T U N D R A P L A N T S 4527 Table 1 Best predictors of leaf bud break, separated by year. Odds ratio and P-values are indicated for each predictor variable:

Species ( PB = Polygonum bistorta), air temperature, photoperiod, depth of thaw, and treatment (ES = extended season, ESW = extended season + warming)

Year Species – PB

ESW 1997

Air temp.

Photoperiod

Depth of thaw

ES

1.43, NS 0.76, NS 1998

0.93, NS 0.98, NS 2003

0.75, NS 0.99, NS

Table 2 Best predictors of flowering, separated by year. Table 4 Relationship between 1-year, 2-year, and 3-year time Odds ratio and P-values are indicated for each predictor vari-

lags in air temperature (°C) and frequency of flowering in each able: Species ( EV = Eriophorum vaginatum), air temperature,

species; where BN = Betula nana, CB = Carex bigellowii, and depth of thaw

CT = Cassiope tetragona, EV = Eriophorum vaginatum, LP = Le- Year

Species – EV dum palustre, PB = Polygonum bistorta, SP = Salix pulchra, and Vaccinium vitis-idea. Results are from linear regressions VVI = 1995

Air temp.

Depth of thaw

2-year time-lag 3-year time-lag 1997

1-year time-lag

F = 1.72 NS F = 2.46 NS 1998

F = 1.61 NS

F = 1.42 NS F = 1.84 NS 2000

CB F = 0.98 NS

F = 1.00 NS F = 0.99 NS 2003

F = 1.93 NS

EV F = 16.75**

F = 4.79* F = 9.77**

LP

F = 8.96**

F = 5.64* F = 4.79*

F = 7.12* F = 7.28** Table 3 Best predictors of leaf senescence, separated by year.

PB

F = 7.98**

F = 0.004 NS F = 0.00 NS Odds ratio and P-values are indicated for each predictor vari-

SP

F = 0.46 NS

F = 27.34** F = 23.38** able: air temperature, photoperiod, and depth of thaw

VVI

F = 35.56**

Df values for all categories is 64, 1. P-values <0.05 are indi- Year

cated by *, P-values <0.01 are indicated by **. 1995

Air temp.

Photoperiod

Depth of thaw

Our results clearly show that early snow removal 1999

induces earlier leaf bud break, senescence, and floral 2000

anthesis relative to the controls. Previous ITEX results 2001

also reported earlier leaf burst and flowering in season- 2002

long-warmed plots (Arft et al., 1999). However, our 2003

findings show that although earlier loss of snow cover caused earlier onset of phenophases, the total period of activity did not increase because senescence was also

time lag ( F 1,524 = 17.31, P < 0.001), 2-year time lag accelerated. These results contrast Arft et al. (1999), ( F 1,524 = 18.44, P < 0.001), and 3-year time lag

which reported delayed senescence in response to ( F 1,526 = 15.54, P < 0.001), were all significant. How-

warming of air, resulting in longer overall periods of ever, when analyzed alone, not each species showed a

plant activity. Thus, our study suggests that species significant response to air temperature carryover

which do not respond immediately to favorable envi- effects. This pattern was consistent for 1-, 2-, and 3-year

ronmental conditions will be at a disadvantage relative time lags (Table 4). Eriophorum vaginatum, Ledum palus-

to phenologically plastic species. Our findings corrobo- tre, Polygonum bistorta, and Vaccinium vitis-idaea consis-

rate a growing number of studies showing that plant tently responded to air temperature up to 3 years prior

growth at high latitudes may begin earlier but may not to actual flowering, while Betula nana, Carex bigellowii,

necessarily last longer. In fact, warming temperatures Cassiope tetragona, and Salix pulchra showed no

may cause the growing season to shorten (Post et al., response.

2001; Linderholm, 2006; Shutova et al., 2006). Previous

4528 R . K H O R S A N D R O S A et al. work in our plots found that season duration did not

actually address how delayed responses in flowering increase physiological activity in response to the

and greening vary across a range of species. manipulation (Oberbauer et al., 1998; Starr et al., 2000).

The timing of phenophases with respect to climate Høye et al. (2013) found an inverse correlation between

will play a key role in species resiliency and interspeci- duration of flowering and temperature, suggesting that

fic competition. In tussock tundra, earlier snow melt as the summers get warmer in the Arctic, the flowering

may affect early greening and flowering species such as season will shorten. A shorter flowering season in the

E. vaginatum and S. pulchra more than late greening Arctic has been linked to decreases in floral resources

V. vitis-idaea and B. nana. and visitation rates (Potts et al., 2010).

and flowering species such as

Earlier flowering species are more dependent on timing Species variation is an important factor to consider

of snow melt than late-flowering species (Dunne et al., when evaluating the phenological and physiological

2003; Kudo et al., 2008; Wipf, 2010). Abundance of spe- responses of tundra communities to climate change

cies with early leaf expansion was higher in early snow (Starr et al., 2008; Cooper et al., 2011). Our study shows

melt plots than late snow melt plots in alpine areas of that species do not respond uniformly to an extended

Colorado (Galen & Stanton, 1995). Molau (1993) snow-free period and soil warming. In contrast to the

hypothesized that late-bloomers could be short-term other seven species, Cassiope tetragona exhibited no

‘winners’ under climate change. The probability of suc- response to either treatment. Molau (1997) also found lit-

cessful pollen transfer and seed germination would be tle response of

C. tetragona to warming treatments. higher for these individuals because they could take Therefore, we could classify

advantage of the end of the growing season. While ear- Polygonum bistorta (Starr et al., 2000), as periodic species,

C. tetragona, and possibly

lier flowering species have a longer timespan to set fruit or those which have a genetically fixed growth strategy.

and disperse their seeds, they can potentially lose all Highly responsive species such as Salix pulchra and

their reproductive output because of early-season frost, Vaccinium vitis-idaea fit the classification of aperiodic, or

a typical outcome of warming (Inouye, 2008). Although plastic, species (Sørensen, 1941). Such species can adapt

it still remains unclear if plastic growth strategies in their growth strategy to changing environmental condi-

response to early snow melt will ultimately be advanta- tions and consequently may out-compete species with

geous for a species or not, it underlines the possibility nonplastic growth strategies (Lechowicz, 1995).

that phenotypic acclimation to warming may be more Our data corroborate the idea that present plant

important for specific individuals and populations than growth directly reflects past environmental conditions.

general macro-evolutionary adaptations (Totland and Many species in the Arctic produce bud primordia

Alatalo, 2002). Furthermore, phenotypic adaptation will underground, sometimes up to several years prior to

have direct effects on other biotic interactions. Variation flowering, as an evolutionary adaptation to a short

among early-flowering individuals and late-flowering growing season (Sørensen, 1941; Billings & Mooney,

individuals can alter the length of the flowering season, 1968). Diggle (1997) showed that in the alpine species,

imposing immediate effects on population dynamics Polygonum viviparum, the maximum reproductive out-

and plant–pollinator interactions (Høye et al., 2013). put of each inflorescence is already determined 1-year

In addition to the varying responses of species to prior to actual maturation. Moreover, the development

treatment, we also found the contribution of each spe- of each leaf and inflorescence, from initiation to func-

cies to differ in each of the regression models. Although tional and structural maturity, requires 4 years. Not

species, in general, significantly predicted bud break only may underground buds take longer to develop,

and flowering, the likelihood of bud break and flower- but they also may be susceptible to abiotic conditions

ing was an order of magnitude higher in P. bistorta and prior to the season of observation. In other words, the

E. vaginatum, respectively. One interpretation is that effect of air temperature on plant growth may not man-

such high odds ratios simply reflect the high frequency ifest itself until several years later (Arft et al., 1999). Our

of these two species and their life histories. Rates of results imply that time lags in air temperature do not

growth (both vegetative and reproductive) and regen- affect flowering in all species in the same way. The non-

eration tend to be higher in herbaceous than woody plastic response in

plants (Bazzaz, 1979). Thus, we must consider relative what we would expect from a periodic species which

C. tetragona to air temperature is

abundance of these species when interpreting the cannot respond to current, nor past, abiotic conditions.

E. vaginatum and P. bistorta may In contrast, we would expect species such as Eriopho-

results. Alternatively,

be more predictable than other species and do well in a rum vaginatum, which develop preformed buds, to be

more tightly controlled environment. In contrast to bud highly sensitive to past environmental conditions.

break and flowering, we did not detect a species-speci- Although it is implied in the literature that bud forma-

fic or growth form-specific pattern with respect to leaf tion is susceptible to past abiotic conditions, few studies

senescence, suggesting that new leaves of all species

C H A N G I N G P H E N O L O G Y O F T U N D R A P L A N T S 4529 are equally likely to senesce at the end of the season.

predicted vegetative phenology for the majority of Oberbauer et al. (2013) found senescence of all growth

study years, but not for flowering. These results make forms to occur at similar thaw degree day values. It is

intuitive sense; an increase in hours of light is a key also important to point out that the most abundant

trigger for plants to begin vegetative processes, while a species will not necessarily be more resilient to changes

decrease in hours of light is a key trigger for plants to in the growing season. Our results suggest that

prepare for winter (H abjørg, 1972). Photoperiod is at a

E. vaginatum will be at a competitive disadvantage to maximal constant during peak flowering (June/July), deciduous shrubs.

however. Photoperiod may play an important role in While plant phenology is dependent upon many abi-

the timing of early- or late-bloomers, but has a negligi- otic factors, our study suggests that air temperature is

ble effect for the majority of flowering individuals. Our the key determinant of the onset of vegetative and

results agree with other studies suggesting that snow reproductive phenology in the tundra. Temperature

cover and depth of thaw may be especially important significantly predicted each of the three phenophases,

in the early season (when greening occurs), while pho- both when years were pooled and analyzed separately.

toperiod and genetic constraints become increasingly The strong correlation between thaw degree days and

important in the late-season (associated with senes- flowering further highlights the critical role air temper-

cence) (Shaver & Kummerow, 1992; Oberbauer et al., ature plays in phenology. Surface air temperature is

1998; Van Wijk et al., 2003; Estiarte & Pe nuelas, 2015). ~ one of the most useful climate change variables as it

While early snow melt allows plants to get a ‘jump- accounts for changes in the surface energy budget and

start’ on growth, it also exposes them to early-season atmospheric circulation (Serreze et al., 2000). Air tem-

low temperatures, damaging frost, and drier conditions perature is disproportionately important as it dictates,

(Wookey & Robinson, 1997; Sturm et al., 2005). Soil in part, depth of thaw, with indirect effects on other

warming likely aggravated drying effects in our study, abiotic variables including water and nutrient availabil-

probably explaining why we did not observe a differ- ity. There is ample evidence demonstrating that tem-

ence in phenology between the two experimental treat- perature determines many phenophases, in general

ments. Drier tundra organic soils are highly insulative, (Badeck et al., 2004) and particularly in arctic and

reducing thermal transfer from the soil surface to dee- alpine species (Dunne et al., 2003; Huelber et al., 2006;

per layers (Hinkel et al., 2001); as a result, the warmed Euskirchen et al., 2014). Timing of bud break in Betula

plots had slightly shallower depth of thaw than the nana and Salix pulchra was found to be a function of air

extended season plots. Although a lengthened snow- temperature (Pop et al., 2000). Air temperature was the

free period offers plants the opportunity for a longer strongest predictor of the commencement of photosyn-

period of potential growth, it can also lead to water thesis in an evergreen boreal forest (Tanja et al., 2003).

stress. A lack of water obstructs effective nitrogen With the exception of air temperature, environmental

assimilation (Kramer & Boyer, 1995) and prevents variables such as snow melt, thaw, and photoperiod

plants from taking advantage of a longer growing sea- exert different degrees of importance at different peri-

son. Other studies have attributed delayed reproduc- ods in the growing season. Date of snow melt was the

tive phenology (Dorji et al., 2013) and declines in flower most relevant for bud break, which suggests that plants

production (de Valpine and Harte, 2001) to soil drying are limited by snow cover early in the season, when the

caused by soil warming.

majority of growth occurs. These results corroborate Growth form affects snow accumulation and has a the strong, positive linear relationship we found

consequential ripple effect through the landscape between timing of snow melt and bud break. Other

(Sturm et al., 2001b, 2005). Furthermore, different plant studies have also found bud break of evergreen and

functional types with different life histories will deciduous species to be dependent on timing of snow

respond heterogeneously to climate change, potentially melt (Shaver & Kummerow, 1992; Shevtsova et al.,

introducing asynchronies into plant–plant and plant– 1997). Earlier snow melt since the 1950s is well docu-

animal interactions (Dunne et al., 2003; Roy et al., 2004; mented in the Arctic and is predicted to be one of the

Post & Forchhammer, 2008; Høye et al., 2013). In our primary consequences of climate change (Foster, 1989;

study, evergreen shrubs were the least responsive to Aurela et al., 2004; Post et al., 2009). Thus, we predict

treatment, while deciduous shrubs and graminoids earlier bud break in the tundra as the timing of snow

were the most responsive, corroborating previous melt advances.

studies (Molau, 1997; Dormann & Woodin, 2002). Soil thaw also explained leaf bud break in our mod-

Woody, deciduous shrubs have a competitive advan- els, consistent with other studies. Soil thaw accurately

tage over other growth forms as a result of their physi- predicted bud break of

cal architecture, ability to uptake nutrients, and Wijk et al., 2003). In our plots, photoperiod significantly

B. nana 3 years in a row (Van

production of rapidly decomposing litter (Shaver et al.,

4530 R . K H O R S A N D R O S A et al. 1996). Evergreen shrubs tend to be slow growing and

increased season length. Perhaps plants need addi- rely heavily on internal cycling of nitrogen, while

tional nutrients to be able to take advantage of a longer deciduous shrubs are characterized by rapid growth

growing season. Natali et al. (2012) point to N limita- and can access soil-available nitrogen (Aerts, 1995).

tion as the primary explanation why ecosystem-level Starr et al. (2008) demonstrated that photosynthetic

net primary productivity did not increase despite rates (directly affecting and affected by phenology) in

experimental lengthening of the growing season. Fertil- our plots were highest for deciduous shrubs and lowest

ization effects have been shown to have a greater influ- for evergreen shrubs. Also, deciduous shrubs must

ence on productivity in the Arctic than warming effects ‘take a chance’ and break buds before other plant func-

(Chapin et al., 1995; Dormann & Woodin, 2002; Van tional types (Billings & Mooney, 1968), monopolizing

Wijk et al., 2004; but see Larigauderie & Kummerow, resources and increasing recruitment probability. In

1991). Eriophorum vaginatum appears to be more limited our study, deciduous shrubs senesced later than ever-

by nutrients than photosynthesis in the Alaskan tussock greens and graminoids, suggesting that deciduous

tundra (Tissue & Oechel, 1987). Growth in Ledum and shrubs are best suited to take advantage of an extended

Eriophorum was highly constrained by nutrients in the growing season. These results support growing evi-

late-season (Chapin & Shaver, 1996). Earlier phenology dence of deciduous shrub expansion in the tundra

may cause a feedback mechanism by which nutrient (Sturm et al., 2001b; Stow et al., 2004; Tape et al., 2006;

limitation is further exacerbated, thereby limiting pro- Walker et al., 2006). We are not the first to predict a

ductivity (Kremers et al., 2015). Our results provide evi- decline in evergreen shrubs including

dence that an earlier onset of the growing season alone (Grime, 1979; Billings & Peterson, 1992; Molau, 1997;

C. tetragona

will not result in increased growth. These findings con- Buizer et al., 2012) and a consequential reduction in

trast with satellite data that indicate an increase in tun- species diversity (Walker et al., 2006).

dra plant growth (Myneni et al., 1997; Tucker et al., As expected, temporal variation was significant

2001), implying the role of other factors beyond among years. Anomalous weather events explain, to an

changes in timing of snow melt. Late-season nutrient extent, seasonal phenology. In alpine communities, 15–

supply and plants’ ability to access nutrients may be 40% of among-year variation in phytomass was attribu-

key factors determining ecosystem productivity. Limi- ted to interannual climate variation (Walker et al.,

tations in growth will, in turn, cause limitations in 1994). The dynamic interaction between abiotic factors

carbon sequestration, making the tundra potentially a and interannual variation also may explain nonlinear

larger source than sink of carbon (Starr & Oberbauer, phenological responses to climate (Iler et al., 2013). In

our study, 1999 was marked by unusually early snow melt, warm spring conditions, and an extended dry

Acknowledgements

period. Other seemingly random events such as the complete absence of flowering in S. pulchra in 1996

This work is based, in part, on funding from National Science

make generalizing temporal patterns difficult.

Foundation grants OPP-9321626, 9615845, 9907185, and 0856710.

Although our results suggest a unidirectional, down- Logistical support by the staff of the Institute of Arctic Biology

Toolik Field Station is greatly appreciated. Kevin R. T. Whelan,

ward trend in onset of phenology, we interpret these

Carlo Calandriello, Esperanza Rodriguez, Brook Shamblin, Car-

results with caution. Further work is crucial so we can

rie Beeler, Michael Rasser, and Tara Madsen provided much

describe with more certainty the relationship between

appreciated field assistance. The work benefited greatly from

timing of phenophases and year. Nevertheless, our

statistical advice by Dr. Jianbin Zhu.

results add to a growing body of evidence demonstrat- ing earlier onset of phenology at northern latitudes

References

(Zhou et al., 2001; Badeck et al., 2004; Post et al., 2009; Aerts R (1995) The advantages of being evergreen. Bock Trends in Ecology and Evolution, 10, et al., 2014).

Finally, our work highlights the possibility that

Arft AM, Walker MD, Gurevitch J et al. (1999) Responses of tundra plants to experi-

advanced snow melt and phenology will not necessar-

mental warming: meta-analysis of the International Tundra Experiment. Ecological

ily be accompanied by a net increase in productivity. Monographs, 69, 491–511.

Aurela M, Laurila T, Tuovinen JP (2004) The timing of snow melt controls the annual

While greening began significantly earlier in the treat-

CO 2 balance in a subarctic fen. Geophysical Research Letters, 31, L16119.

ment plots, the total duration of activity did not

Badeck FW, Bondeau A, B €ottcher K, Doktor D, Lucht W, Schaber J, Sitch S (2004) Re-

sponses of spring phenology to climate change. increase, suggesting that an earlier start to the growing New Phytologist, 162, 295–309.

Bazzaz FA (1979) The physiological ecology of plant succession. Annual Review of

season, in and of itself, is not enough to increase pro-

Ecology and Systematics, 10, 351–371.

ductivity. Our phenological observations are consistent

Beaubien EJ, Freeland HJ (2000) Spring phenology trends in Alberta, Canada: links to

ocean temperature. with finding of La Puma International Journal of Biometeorology, 44, 53–59. et al. (2007), who reported no

Billings WD (1987) Constraints to plant growth, reproduction, and establishment in

increase in net ecosystem productivity at Toolik despite

arctic environments. Arctic and Alpine Research, 19, 357–365.

C H A N G I N G P H E N O L O G Y O F T U N D R A P L A N T S 4531

Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biological Høye T, Post E, Schmidt NM, Trøjelsgaard K, Forchhammer MC (2013) Shorter flow- Reviews, 43, 481–529.

ering seasons and declining abundance of flower visitors in a warmer Arctic. Na- Billings WD, Peterson KM (1992) Some possible effects of climatic warming on arctic

ture Climate Change, 3, 759–763.

tundra ecosystems of the Alaskan North Slope. In: Global Warming and Biological Huelber K, Gottfried M, Pauli H, Reiter K, Winkler M, Grabherr G (2006) Phenologi- Diversity (eds Peters RL, Lovejoy TE), pp. 233–243. Yale University Press, New

cal responses of snowbed species to snow removal dates in the central Alps: impli- Haven.

cations for climate warming. Arctic, Antarctic, and Alpine Research, 38, 99–103. Bliss LC, Matveyeva NV (1992) Circumpolar vegetation. In: Arctic Ecosystems in a

Hughes L (2000) Biological consequences of global warming: is the signal already Changing Climate: An Ecophysiological Perspective (eds Chapin FS III, Jeffries RL,

apparent? Trends in Ecology and Evolution, 15, 56–61. Reynolds JF, Shaver GR, Svoboda J), pp. 59–86. Academic Press, San Diego.

Iler AM, Høye TT, Inouye DW, Schmidt NM (2013) Nonlinear flowering responses to Bock A, Sparks TH, Estrella N (2014) Changes in first flowering dates and flowering

climate: are species approaching their limits of phenological change? Philosophical duration of 232 plant species on the island of Guernsey. Global Change Biology, 20,

Transactions of the Royal Society B, 368, 20120489. 3508–3519.

Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral Bonan GB, Chapin FS III, Thompson SL (1995) Boreal forest and tundra ecosystems as

abundance of montane wildflowers. Ecology, 89, 353–362. components of the climate system. Climate Change, 29, 145–167.

Intergovernmental Panel on Climate Change (IPCC) (2014) Climate Change 2013: The Buizer B, Weijers S, van Bodegom PM et al. (2012) Range shifts and global warming:

Physical Science Basis: Working group I contribution to the fifth assessment report of the ecological responses of Empetrum nigrum L. to experimental warming at its north-

Intergovernmental Panel on Climate Change. Cambridge University Press, Cam- ern (high Arctic) and southern (Atlantic) geographical range margin. Environmen-

bridge, UK.

tal Research Letters, 7, 025501. Jia GS, Epstein HE, Walker DA (2003) Greening of Arctic Alaska, 1981–2001. Geophysi- Chapin FS III, Shaver GR (1996) Physiological and growth responses of arctic plants

cal Research Letters, 30, 2067.

to a field experiment simulating climatic change. Ecology, 77, 822–840. Kramer PJ, Boyer JS (1995) Water Relations of Plants and Soils. Academic Press, San Chapin FS III, Shaver GR, Giblin AE, Nadelhoffer KJ (1995) Responses of arctic tun-

Diego, CA.

dra to experimental and observed changes in climate. Ecology, 76, 694–711. Kremers KS, Hollister RD, Oberbauer SF (2015) Diminished response of arctic plants Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant

to warming over time. PLoS ONE, 10, e0116586. phenology in response to global change. Trends in Ecology and Evolution, 22, 357–

Kudo G, Ida TY, Tani T (2008) Linkages between phenology, pollination, photosyn- 365.

thesis, and reproduction in deciduous forest understory plants. Ecology, 89, 321– Cooper EJ, Dullinger S, Semenchuka P (2011) Late snowmelt delays plant develop-

ment and results in lower reproductive success in the High Arctic. Plant Science, La Puma IP, Philippi TE, Oberbauer SF (2007) Relating NDVI to ecosystem CO 2 180, 157–167.

exchange patterns in response to season length and soil warming manipulations Diggle PK (1997) Extreme preformation in alpine Polygonum viviparum: an architec-

in arctic Alaska. Remote Sensing of Environment, 109, 225–236. tural and developmental analysis. American Journal of Botany, 84, 154–169.

Larigauderie A, Kummerow J (1991) The sensitivity of phenological events to changes Dorji T, Totland Ø, Moe SR, Hopping KA, Pan J, Klein JA (2013) Plant functional

in nutrient availability for several plant growth forms in the Arctic. Holarctic Ecol- traits mediate reproductive phenology and success in response to experimental

ogy, 14, 38–44.

warming and snow addition in Tibet. Global Change Biology, 19, 459–472. Lechowicz MJ (1995) Seasonality of flowering and fruiting in temperate forest trees. Dormann CF, Woodin SJ (2002) Climate change in the Arctic: using plant functional

Canadian Journal of Botany, 73, 175–182.

types in a meta-analysis of field experiments. Functional Ecology, 16, 4–17. Linderholm HW (2006) Growing season changes in the last century. Agricultural and Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology

Forest Meteorology, 137, 1–14.

responses to climate change: integrating experimental and gradient methods. Eco- Maxwell B (1992) Arctic climate: potential for change under global warming. In: Arc- logical Monographs, 73, 69–86.

tic Ecosystems in a Changing Climate: An Ecophysiological Perspective (eds Chapin FS Ernakovich JG, Hopping KA, Berdanier AB, Simpson RT, Kachergis EJ, Steltzer H,

III, Jeffries RL, Reynolds JF, Shaver GR, Svoboda J), pp. 11–31. Academic Press, Wallenstein MD (2014) Predicted responses of arctic and alpine ecosystems to

San Diego, CA.

altered seasonality under climate change. Global Change Biology, 20, 3256–3269. McCarty JP (2001) Ecological consequences of recent climate change. Conservation Estiarte M, Pe nuelas J (2015) Alteration of the phenology of leaf senescence and fall in ~

Biology, 15, 320–331.

winter deciduous species by climate change: effects on nutrient proficiency. Global McKane RB, Rastetter EB, Shaver GR, Nadelhoffer KJ, Giblin AE, Laundre JA, Chapin Change Biology, 21, 1005–1017.

FS III (1997) Climatic effects on tundra carbon storage inferred from experimental Eugster W, McFadden JP, Chapin FS III (2005) Differences in surface roughness,

data and a model. Ecology, 78, 1170–1187.

energy, and CO 2 fluxes in two moist tundra vegetation types, Kuparuk watershed, Menzel A, Fabian P (1999) Growing season extended in Europe. Nature, 397, 659. Alaska, U.S.A. Arctic, Antarctic, and Alpine Research, 37, 61–67.

Molau U (1993) Relationships between flowering phenology and life-history strate- Euskirchen ES, McGuire AD, Chapin FS III, Yi S, Thompson CC (2014) Changes in

gies in tundra plants. Arctic and Alpine Research, 25, 391–402. vegetation in northern Alaska under scenarios of climate change, 2003–2100: impli-

Molau U (1997) Responses to natural climatic variation and experimental warming in cations for climate feedbacks. Ecological Applications, 19, 1022–1043.

two tundra plant species with contrasting life forms: Cassiope tetragona and Ranun- Fahnestock JT, Povirk KL, Welker JM (2000) Ecological significance of litter redistri-

culus nivalis. Global Change Biology, 3 (Suppl. 1), 97–107. bution by wind and snow in Arctic landscapes. Ecography, 23, 623–631.

Molau U, Mølgaard P (1996) ITEX Manual. Danish Polar Center, Copenhagen, Denmark. Foster JL (1989) The significance of the date of snow disappearance on the arctic tun-

Molau U, Nordenh €all U, Eriksen B (2005) Onset of flowering and climate variability dra as a possible indicator of climate change. Arctic and Alpine Research, 21, 60–70.

in an alpine landscape: a 10-year study from Swedish Lapland. American Journal of Frei A, Robinson DA, Hughes MG (1999) North American snow extent: 1900–1994. In-

Botany, 92, 422–431.

ternational Journal of Climatology, 19, 1517–1534. Myers-Smith IH, Forbes BC, Wilmking M et al. (2011) Shrub expansion in tundra Galen C, Stanton ML (1995) Responses of snowbed plant species to changes in grow-

ecosystems: dynamics, impacts and research priorities. Environmental Research Let- ing-season length. Ecology, 76, 1546–1557.

ters, 6, 6045509.

Grime JP (1979) Plant Strategies and Vegetation Processes. Wiley and Sons, New York. Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant H abjørg A (1972) Effects of photoperiod and temperature on growth and develop-

growth in the northern high latitudes from 1981 to 1991. Nature, 386, 698–702. ment of three latitudinal and three altitudinal populations of Betula pubescens Ehrh.

Natali SM, Schuur EAG, Rubin R (2012) Increased plant productivity in Alaskan tun- Norges Landbrukshøgsk Meld, 51, 1–27.

dra as a result of experimental warming of soil and permafrost. Journal of Ecology, Higuera PE, Brubaker LB, Anderson PM, Brown TA, Kennedy AT, Sheng HUF (2008)

Frequent fires in ancient shrub tundra: implications of paleorecords for arctic envi- Oberbauer SF, Starr G (2002) The role of anthocyanins for photosynthesis of Alaskan ronmental change. PLoS ONE, 3, e0001744.

arctic evergreens during snowmelt. Advances in Botanical Research, 37, 129–145. Hinkel KM, Paetzold F, Nelson FE, Bockheim JG (2001) Patterns of soil temperature

Oberbauer SF, Tenhunen JD, Reynolds JF (1991) Environmental effects on CO 2 efflux and moisture in the active layer and upper permafrost at Barrow, Alaska: 1993–

from water track and tussock tundra in arctic Alaska, USA. Arctic, Antarctic, and 1999. Global and Planetary Change, 29, 293–309.

Alpine Research, 23, 162–169.

Hollister RD, Webber PJ, Tweedie CE (2005) The response of Alaskan arctic tundra to Oberbauer SF, Starr G, Pop EW (1998) Effects of extended growing season and soil experimental warming: differences between short- and long-term responses. Global

warming on carbon dioxide and methane exchange of tussock tundra in Alaska. Change Biology, 11, 525–536.

Journal of Geophysical Research, 103, 29075–29082.

4532 R . K H O R S A N D R O S A et al.

Oberbauer SF, Elmendorf SC, Troxler TG et al. (2013) Phenological response of tundra Sturm M, Schimel J, Michaelson G et al. (2005) Winter biological processes could help plants to background climate variation tested using the International Tundra

convert arctic tundra to shrubland. BioScience, 55, 16–26. Experiment. Philosophical Transactions of the Royal Society B, 368, 20120481.

Tanja S, Berninger F, Vesala T et al. (2003) Air temperature triggers the recovery of O’Brien JJ, Oberbauer SF (2001) An inexpensive, portable method for measuring soil

evergreen boreal forest photosynthesis in spring. Global Change Biology, 9, 1410– moisture. Soil Science Society of America Journal, 65, 1081–1083.

1426.

Overpeck J, Hughen K, Hardy D et al. (1997) Arctic environmental change of the last Tape K, Sturm M, Racinez C (2006) The evidence for shrub expansion in Northern four centuries. Science, 278, 1251–1256.

Alaska and the Pan-Arctic. Global Change Biology, 12, 686–702. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts

Tissue DT, Oechel WC (1987) Response of Eriophorum vaginatum to elevated CO 2 and across natural systems. Nature, 421, 37–42.

temperature in the Alaskan tussock tundra. Ecology, 68, 401–410. Pop EW, Oberbauer SF, Starr G (2000) Predicting vegetative bud break in two arctic

Totland O, Alatalo JM (2002) Effects of temperature and date of snowmelt on growth, deciduous shrub species, Salix pulchra and Betula nana. Oecologia, 124, 176–184.

reproduction, and flowering phenology in the arctic/alpine herb, Ranunculus gla- Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an

cialis. Oecologia, 133, 168–175.

arctic herbivore through trophic mismatch. Philosophical Transactions of the Royal Tucker CJ, Slayback DA, Pinzon JE, Los SO, Myneni RB, Taylor MG (2001) Higher Society B, 363, 2369–2375.

northern latitude normalized difference vegetation index and growing season Post E, Forchhammer MC, Stenseth NC, Callaghan TV (2001) The timing of life-his-

trends from 1982 to 1999. International Journal of Biometeorology, 45, 184–190. tory events in a changing climate. Proceedings of the Royal Society B-Biological

de Valpine P, Harte J (2001) Plant responses to experimental warming in a montane Sciences, 268, 15–23.

meadow. Ecology, 82, 637–648.

Post E, Forchhammer MC, Bret-Harte MS et al. (2009) Ecological dynamics across the Van Wijk MT, Williams M, Laundre JA, Shaver GR (2003) Interannual variability of Arctic associated with recent climate change. Science, 325, 1355–1358.

plant phenology in tussock tundra: modelling interactions of plant productivity, Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Glo-

plant phenology, snowmelt and soil thaw. Global Change Biology, 9, 743–758. bal pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution,

Van Wijk MT, Clemmensen KE, Shaver GR et al. (2004) Long-term ecosystem level 25, 345–353.

experiments at Toolik Lake, Alaska, and at Abisko, Northern Sweden: generaliza- Roy BA, G usewell S, Harte J (2004) Response of plant pathogens and herbivores to a €

tions and differences in ecosystem and plant type responses to global change. Glo- warming experiment. Ecology, 85, 2570–2581.

bal Change Biology, 10, 105–123.

Rumpf SB, Semenchuk PR, Dullinger S, Coope EJ (2014) Idiosyncratic responses to Walker MD, Webber PJ, Arnold EH, Ebert-May D (1994) Effects of inter-annual climate high Arctic plants to changing snow regimes. PLOS One, 9, e86281.

variation on aboveground phytomass in alpine vegetation. Ecology, 75, 393–408. Serreze MC, Walsh JE, Chapin FS III et al. (2000) Observational evidence of recent

Walker MD, Wahren CH, Hollister RD et al. (2006) Plant community responses to change in the northern high-latitude environment. Climatic Change, 46, 159–207.

experimental warming across the tundra biome. Proceedings of the National Academy Shaver GR, Kummerow J (1992) Phenology, resource allocation, and growth of arctic

of Sciences, 103, 1342–1346.

vascular plants. In: Arctic Ecosystems in a Changing Climate: An Ecophysiological Per- Walther GR, Post E, Convey P et al. (2002) Ecological responses to recent climate spective (eds Chapin FS III, Jefferies RL, Reynolds JF et al.), pp. 191–212. Academic

change. Nature, 416, 389–395.

Press, New York. Webber PJ, Walker MD (1991) The International Tundra Experiment (ITEX): resolu- Shaver GR, Giblin AE, Nadelhoffer KJ, Rastetter EB (1996) Plant functional types

tion. Arctic and Alpine Research, 23, 124.

and ecosystem change in arctic tundras. In: Plant Functional Types (eds Smith T, Wipf S (2010) Phenology, growth, and fecundity of eight subarctic tundra species in Woodward I, Shugart H), pp. 152–172. Cambridge University Press, Cambridge,

response to snowmelt manipulations. Plant Ecology, 207, 53–66. UK.

Wipf S, Rixen C (2010) A review of snow manipulation experiments in Arctic and Shevtsova A, Haukioja E, Ojala A (1997) Growth responses of subarctic dwarf shrubs,

alpine tundra ecosystems. Polar Research, 29, 95–109. Empetrum nigrum and Vaccinium vitis-idaea, to manipulated environmental condi-

Wookey PA, Robinson CH (1997) Interpreting environmental manipulation experi- tions and species removal. Oikos, 78, 440–458.

ments in arctic ecosystems: are ‘disturbance’ responses properly accounted for? In: Shutova E, Wielgolaski FE, Karlsen SR et al. (2006) Growing seasons of Nordic moun-

Disturbance and Recovery in Arctic Lands (ed. Crawford RMM), pp. 115–134. Kluwer, tain birch in northernmost Europe as indicated by long-term field studies and

Dordrecht, the Netherlands.

analyses of satellite images. International Journal of Biometeorology, 51, 155–166. Wu X, Liu H (2013) Consistent shifts in spring vegetation green-up date across tem- Sørensen T (1941) Temperature relations and phenology of the northern Greenland

perate biomes in China, 1982–2006. Global Change Biology, 19, 870–880. flowering plants. Meddar Gronland, 125, 1–305.

Zar JH (1984) Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ. Starr G, Oberbauer SF (2003) Photosynthesis of arctic evergreens under snow: impli-

Zhou L, Tucker CJ, Kaufman RK, Slayback D, Shabanov N, Myneni RB (2001) Varia- cations for tundra ecosystem carbon balance. Ecology, 84, 1415–1420.

tions in northern activity inferred from satellite data of vegetation index during Starr G, Oberbauer SF, Pop EW (2000) Effects of extended growing season and soil

1981 to 1999. Journal of Geophysical Research, 106, 20069–20083. warming on phenology and physiology of Polygonum bistorta. Global Change Biol- ogy, 6, 357–369.

Starr G, Oberbauer SF, Ahlquist LH (2008) The photosynthetic response of Alaskan tundra plants to increased season length and soil warming. Arctic, Antarctic, and Alpine Research, 40, 181–191.

Supporting Information

Stone RS, Dutton EG, Harris JM, Longenecker D (2002) Earlier spring snowmelt in northern Alaska as an indicator of climate change. Journal of Geophysical Research-

Additional Supporting Information may be found in the

Atmospheres, 107, 1–13.

online version of this article:

Stow DA, Hope A, McGuire D (2004) Remote sensing of vegetation and land-cover change in arctic tundra ecosystems. Remote Sensing of Environment, 89, 281–308. Sturm M, Racine CR, Tape K (2001a) Increasing shrub abundance in the Arctic. Na-

Table S1. Results of binary logistic regression for leaf bud

break for 1997–2003.

ture, 411, 546–547.

Sturm M, Mcfadden JP, Liston GE, Chapin FS III, Racine CH, Holmgren J (2001b)

Table S2. Logistic regression results for flowering.

Snow–shrub interactions in arctic tundra: a hypothesis with climatic implications.

Table S3. Logistic regression results for leaf senescence.

Journal of Climate, 14, 336–344.