沙漠研究 19-1, 137 - 140 (2009 )Journal of Arid Land Studies“Desert Technology IX ”
Refereed Paper

Environmental Factors Controlling Leaf Emergence in Caragana microphylla,a Deciduous Shrub of the Mongolian Steppe
Yoshihiro YAMADA*1, Yasuto YAMAGUCHI2, Jamsran UNDARMAA3, Muneto HIROBE1, Ken YOSHIKAWA1
Abstract: We examined the effect of temperature and rainfall on the timing of leaf emergencein Caragana microphylla, a representative deciduous shrub found in the Mongolian steppe overa three-year period. Two peaks of leaf emergence were identified, the first of which appeared
to be induced by temperature, while the second was controlled by rainfall.
Keywords: Caragana, Phenology, Pulse-response, Unpredictable rain, Steppe

1. Introduction
Plants growing in arid regions exhibit morphological, physiological, and phenological adaptations to
avoid water deficits. Coincident leaf emergence at the beginning of the rainy season is a typicalphenological adaptation in the Mediterranean regioin (Gill and Mahall, 1986) and in dry tropical forests(Williams et al., 1997; de Bie et al., 1998; Borchert et al., 2002). In such regions with distinct wet anddry seasons, the trees are able to set their leaves about one month prior to the beginning of the rainy season(Singh and Kushwaha, 2005; Elliott et al., 2006) based on changes in the photoperiod (Nilsen and Muller,1981). However, in many regions, rainfall is unpredictable, and occurs occasionally or in pulses, suchthat the timing and amount of rain per year can vary widely (Noy-Meir, 1973). Therefore, desert plants
set their leaves only after significant rainfall (Beatley, 1974).
In the Mongolian steppe, the timing and intensity of rainfall are variable and unpredictable. Rainfalls mostly during the summer without a distinct rainy season. The vegetation in the Mongolian steppe
consists primarily of grasses, but shrubs are also common. Caragana microphylla (Fabaceae) is a
representative deciduous shrub of the Mongolian steppe, found in the sandy grasslands of northern andeastern Mongolia, and which dominates some parts of the steppe. Its thick woody roots penetrate deeply
into the soil (> 1 m), while its more abundant fine roots are found 5-10 cm below the soil surface (YamadaY., personal observation).
The phenology of the grasses in the steppe has already been clarified in terms of emergence andgrowth, which are depend on the amount of rainfall in the spring (Kondoh et al., 2005); however, no
phenological studies on shrubs have been reported. Shrub phenology may differ from that of herbaceous
plants in the same habitat (Hoffmann et al., 2005; Campanella and Bertiller, 2008). We therefore
surveyed the leaf and shoot phenology of C. microphylla and clarified its relationship with unpredictable
rainfall and temperature.
2. Materials and Methods
This study was conducted near Mandalgobi City in Mongolia (45˚47'N, 106˚11'E). The mean annual
temperature at Mandalgobi City was 2 ˚C while the mean annual precipitation was 150 mm. Thevegetation Mongolia may be divided into distinct categories from north to south, according to the amountof precipitation, namely, taiga, steppe, semi-desert, and desert. Mandalgobi City, which is located at thesouthern end of the steppe, is bounded by a semi-desert region. The main species of the steppes areGraminaceae, e.g., Stipa krylovii and Cleistogenes squarrosa. The soil at the site is sandy (Sasaki et al.,2008), with an accumulation of calcium carbonate about 40 cm below the surface (Yamada Y., personalobservation). Water sources on the surface, such as rivers or lakes, are absent around the site.
Climate data, including the average maximum and minimum temperatures and the daily amount ofrainfall, were obtained from the National Climatic Data Center (2007).
Five patches of C. microphylla were selected in a fenced area protected from livestock grazing. In1Graduate School of Environmental Science, Okayama University, 1-1-1 Tsushima-Naka, Okayama, JapanOkayama Prefectural Environmental Conservation Corporation, 665-1 Uchio, Okayama, Japan3Center for Ecosystem Studies, Mongolian State University of Agriculture, 53 Zaisan, Ulanbaatar, Mongolia
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each patch, five (in 2005) or two (in 2006and 2007) terminal branches (targetbranches) were selected. The number ofleaves on each target branch was measured
about once a week.

Number of leaves

5040302010

3. Results and Discussion
05/1 5/15 5/29 6/12 6/26 7/10 7/24 8/7 8/21 9/4 9/18
Over a three year period, most of thebranches showed two periods of intensive
2005
2006
2007
leaf emergence during the growing season;
however, the timing differed (Fig. 1).
Turkey’s test was used to identify peakFig. 1. Seasonal change in the number of leaves on eachperiods of leaf emergence (Fig. 2). Intarget branch (average±SD). The number of leaves on
2005, the first peak was from 22 May to 21
each target branch was averaged per patch, thenJune, while the second peak was from 28
averaged for each date.
July to 8 August. In 2006, the first peak
was from 5 to 9 June, while the second peak was from 1 to 16 July. In 2007, the first peak was from 17
May to 22 June, while the second peak was from 2 to 28 July.
Because the Mongolian steppe has extremely cold winters and dry summers, the limiting factor forleaf emergence in C. microphylla could be temperature and/or rainfall. We analyzed the temperature in
the region using 21-day running averages to avoid effects of short-term changes in the environment(Lieberman, 1982; Jolly et al., 2005). In each year, the first peak of leaf emergence began when the21-day running average was around 3 ˚C (Fig. 3). However, the amount of rainfall before the first peak ofleaf emergence differed among the three years, especially between 2005 and 2007. The monthly
precipitation in May was 16 mm in 2005, but was only 3 mm in 2006 and 4 mm in 2007. Thus, theamount of rainfall prior to leaf emergence may not be a major factor in controlling the first peak of leaf
emergence.
No relationships between the second peak of leaf emergence and temperature was identified (Fig. 4);
however, it coincided with the first heavy rain (> 10 mm day-1) during the growing season in 2005 and2006 (Fig. 4). The second peak of leaf emergence appeared to begin prior to the first heavy rain in 2006
(Fig. 4), but this may have been due to the observation interval (observation dates: 1 and 10 July; first2005

number of newly emerged
leaves (number/day)

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survey datesurvey dateFig. 2. Number of newly emerged leaves. Different letters indicate significant differences according to Turkey’stest (p<0.05).
2006

5/1 5/8 5/15 5/22 5/29 6/5 6/12 6/19 6/26
date
daily rainfall
minimum temperature (21-day running average)

5/1 5/8 5/15 5/22 5/29 6/5 6/12 6/19 6/26
date
daily rainfall
minimum temperature (21-day running average)

15
129
6
30-3-6

14
12
1086
4
20

rainfall (mm)2007
1412108
6
4
20

temperature
(℃)

15
129
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30-3-6

rainfall (mm)temperature(℃)

14
12
108
6
4
20

rainfall (mm)temperature(℃)

2005
15
1296
30-3-6

5/1 5/8 5/15 5/22 5/29 6/5 6/12 6/19 6/26
datedaily rainfall
minimum temperature (21-day running average)

Fig. 3. Twenty-one-day running averages of the minimum temperature and daily rainfall. Shadowed boxes
indicate the beginning of leaf emergence in each year.

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15

15

10

10

5

500
6/1

rainfall

6/15

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7/13 7/27
date

8/10

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average temperature (21-day running average)

25
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6/15 6/29 7/13 7/27 8/10 8/24
date

daily rainfall
average temperature (21-day running average)

25
20
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50
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rainfall (mm)20temperature(℃)

202520151050rainfall (mm)25temperature(℃)

2006

25rainfall (mm)temperature (℃)

2005

2007

6/15 6/29 7/13 7/27 8/10 8/24
date

daily rainfall
average temperature (21-day running average)

Fig. 4. Twenty-one-day running averages of the average temperature and daily rainfall. Shadowed boxes
indicate the second peak of leaf emergence in each year.

heavy rainfall: 8 July). In 2007, although there was no heavy rain (> 10 mm day-1) before the second
peak of leaf emergence, successive periods of light rain (each about 2-3 mm day-1) occurred before thesecond peak of leaf emergence that amounted to almost 10 mm per week (Fig. 4).
Previous studies indicate that a threshold amount of rain is required to induce leaf emergence (Beatley,1974; Reynolds et al., 1999). For example, in the Mojave Desert, leaf emergence in shrubs occurred after
25 mm of rain (Beatley, 1974). However, the response of plants to rainfall events in a temperate steppe
has not been analyzed. Thus, the threshold amount of rain required to induce leaf emergence in theMongolian steppe is unknown. Our data suggested that the threshold is about 10 mm in a week, but
further study is needed.
Coincident leaf emergence with a rise in temperature is common in humid temperate regions,especially at high latitudes (Fenner, 1998), and coincident leaf emergence with rainfall is common in arid
regions (Noy-Meir, 1973; Beatley, 1974). However, this is the first observation of a plant that responds totwo environmental factors at different times.
A study period of three years is inadequate to detect the triggers of leaf emergence in the steppe.
Also, we were unable to investigate the generality of the leaf emergence traits for C. microphylla (i.e.,
whether it is common to other shrubs in the Mongolian steppe, or to plants in other regions), because of therarity of phenological studies of shrubs in temperate arid regions.
4. Conclusions
Leaf emergence in C.microphylla occurs in two peaks. The first-time peak of leaf emergenceappeared to be induced by temperature while the second was controlled by rainfall.
5. Acknowledgements
This study was supported by the Yakumo Foundation for Environmental Science; the Global
Environment Research Fund (G-071); the Ministry of Environment; Japan, and by a Grant-in-Aid for
Scientific Research (17405001) from the Ministry of Education, Culture, Sports, Science, and Technology,Japan.
References
Beatley J.C. (1974): Phenological events and their environmental triggers in Mojave desert ecosystems. Ecology, 55: 856-863.
Borchert R., Rivera G., Hagnauer W. (2002): Modification of vegetative phenology in a tropical semi-deciduous forest by abnormal
drought and rain. Biotropica, 34: 27-39.
Campanella M.V., Bertiller M.B. (2008): Plant phenology, leaf traits and leaf litterfall of contrasting life forms in the arid PatagonianMonte, Argentina. Journal of Vegetation Science, 19: 75-85.
de Bie S., Ketner P., Paasse M., Geerling C. (1998): Woody plant phenology in the West African savanna. Journal of Biogeography,
25: 883-900.
Elliott S., Baker P.J., Borchert R. (2006): Leaf flushing during the dry season: the paradox of Asian monsoon forests. Global Ecology
and Biogeography, 15: 248-257.
Fenner M. (1998): The phenology of growth and reproduction in plants. Perspectives in Plant Ecology, Evolution and Systematics, 1:78-91.
Gill D.S., Mahall B.E. (1986): Quantitative phenology and water relations of an evergreen and a deciduous Chaparral shrub.
Ecological Monographs, 56: 127-143.
Hoffmann W.A., de Silva E.R.J., Machado G.C., Bucci S.J., Scholz F.G., Goldstein G., Meinzer F.C. (2005): Seasonal leaf dynamics
across a tree density gradient in a Brazilian savanna. Oecologia, 145: 307-316.
Jolly W.M., Running S.W. (2004): Effects of precipitation and soil water potential on drought deciduous phenology in the Kalahari.

140

Global Change Biology, 10: 303-308.
Kondoh A., Kaihatsu I., Hirata M., Dorgorsurren A. (2005): Interannual variation of phenology and biomass in Mongolian herbaceousvegetation. Journal of Arid Land Studies, 14: 209-218.
Lieberman D. (1982): Seasonality and phenology in a dry tropical forest in Ghana. Journal of Ecology, 70: 791-806.
National Climatic Data Center (2007): Global Summary of the Day, http://cdo.ncdc.noaa.gov/CDO/redirector
Nilsen E. T., Muller W.H. (1981): Phenology of the drought-deciduous shrub Lotus scoparius: Climatic controls and adaptivesignificance. Ecological Monographs, 51: 323-341.
Noy-Meir I. (1973): Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics, 4: 25-41.
Reynolds J.F., Virginia R.A., Kemp P.R., de Soyza A.G., Tremmel D.C. (1999): Impact of drought on desert shrubs: Effects ofseasonality and degree of resource island development. Ecological Monographs, 69: 69-106.
Sasaki T., Okayasu T., Shirato Y., Undarmaa J., Okubo S., Takeuchi K. (2008): Can edaphic factors demonstrate landscape-scaledifferences in vegetation responses to grazing? Plant Ecology, 194: 51-66.
Singh K.P., Kushwaha C.P. (2005): Emerging paradigms of tree phenology in dry tropics. Current Science, 89: 964-975.
Williams R.J., Myers B.A., Muller W.J., Duff G.A., Eamus D. (1997): Leaf phenology of woody species in a north Australian tropicalsavanna. Ecology, 78: 2542-2558.