No Job Name Colonization of the polar willow Salix polaris on the early stage of succession after glacier retreat in the High Arctic, Ny-Ålesund, Svalbardpor_170 385..390 Takayuki Nakatsubo,1 Masaaki Fujiyoshi,2 Shinpei Yoshitake,3 Hiroshi Koizumi4 & Masaki Uchida5 1 Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, 739-8521, Japan 2 School of Humanities and Culture, Tokai University, Kitakaname 1117, Hiratsuka, 259-1292, Japan 3 Graduate School of Advanced Science and Engineering, Waseda University, 2-2, Wakamatsucho, Shinjuku-ku, Tokyo, 162-8480, Japan 4 Faculty of Education and Integrated Arts and Sciences, Waseda University, 2-2, Wakamatsucho, Shinjuku-ku, Tokyo, 162-8480, Japan 5 National Institute of Polar Research, 10-3, Midori-cho, Tachikawa City, Tokyo 190-8518, Japan Abstract The polar willow (Salix polaris), predominant in the late successional stage in deglaciated areas of Ny-Ålesund, Svalbard, is rarely found in the early stage, when purple saxifrage (Saxifraga oppositifolia) dominates. To elucidate the pattern and the mechanism of successional change from the Saxifraga stage to the Salix stage, we examined the distribution pattern, size structure and habitat conditions of a colonizing Salix population in the seral stage where Salix was invading Saxifraga-dominated sites. The present distribution pattern and aerial photographs taken in the past suggest that Salix colonization at this site com- menced within the last 70 years. We found 115 Salix individuals (22 male, 13 female and 80 unknown) in a 30 m ¥ 30 m quadrat on the seral stage. Although the largest individual had a size of 2000 cm2 (length ¥ maximum width), the majority (84%) of individuals were smaller than 100 cm2. The seedling size distribution, as inferred from the leaf scar number, indicated that annual recruitment was slight. Of the individuals observed about 75% had colonized bare ground; only four individuals grew within Saxifraga colonies. No significant difference was found in soil characteristics (water content, and carbon and nitrogen concentrations) between the seral stage and the earlier stage prior to colonization by Salix. These results suggest that difficulties in seed production, germination and/or seedling establishment of Salix, rather than soil formation by preceding species (Saxifraga), limits the early-stage coloniza- tion by Salix. Keywords Glacier retreat; High Arctic; population structure; Salix polaris; succession; Svalbard. Correspondence Takayuki Nakatsubo, Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, 739-8521, Japan. E-mail: kuyakat@hiroshima-u.ac.jp doi:10.1111/j.1751-8369.2010.00170.x Glacier retreat is occurring widely in the Arctic, including the High Arctic (Green 2005; Kohler et al. 2007). Some evidence suggests that many glaciers in western Svalbard are losing mass at an increasing rate (Kohler et al. 2007). Glacier retreat provides new habitats for plant coloniza- tion, where organic matter accumulates. Information related to colonization rates of plants, especially domi- nant species, and their limiting factors is critically important for predicting how ecosystems in deglaciated areas will respond to future climate change. In a deglaciated area in Ny-Ålesund, Svalbard, purple saxifrage (Saxifraga oppositifolia L.) colonizes bare ground as early as a few years after deglaciation (Kume et al. 1999). Several traits enable this species to be the first colonizer in the area: high fecundity, the ability to form adventitious roots from shoot fragments (Kume et al. 1999) and low leaf nitrogen content, which might facili- tate their establishment on nutrient-poor substrates (Muraoka et al. 2008). In addition, Saxifraga oppositifolia is known to have two growth forms—prostrate and semi- erect—that are adapted to maximize growth in different habitat conditions (Crawford et al. 1995). In contrast, the polar willow (Salix polaris Wahlenb.), a dwarf shrub with creeping subterranean shoots or Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd 385 mailto:kuyakat@hiroshima-u.ac.jp occurring in a moss carpet, predominates in the late suc- cessional stage, but it is rarely found in the early stage, where Saxifraga oppositifolia dominates (Kume et al. 1999; Nakatsubo et al. 1998; Nakatsubo et al. 2005; Muraoka et al. 2008). This species has high leaf photosynthetic capacity, and plays a crucial role in carbon sequestration in the deglaciated ground (Muraoka et al. 2002). Muraoka et al. (2008) estimated that the contribution of Salix polaris is as high as 12 times that of the pioneer plant Saxifraga oppositifolia. Therefore, invasion by Salix polaris during the early stage is important not only in terms of community structure but also for carbon sequestration in this area. To date, however, the pattern and the mecha- nism of the successional change from the Saxifraga stage to the Salix stage have been undocumented. This study specifically examined the seral stage–– between the early and the late successional stages–– during which Salix polaris colonizes Saxifraga-dominated sites. We examined the distribution pattern, size structure and habitat conditions of colonizing Salix populations in the seral stage to study the colonization rate of Salix and its limiting factor(s). Materials and methods The study site was situated in the glacier foreland of Austre Brøggerbreen, near Ny-Ålesund, on the fjord Kongsfjorden in Svalbard (78.5°N, 11.5°E). In the Kongs- fjorden area, the retreat rates of glaciers ending on land are reportedly about 10–20 m per year (Svendsen et al. 2002). The rate of retreat of Austre Brøggerbreen deter- mined in our field study agrees with these values: the recession was about 30 m between 2003 and 2005, and about 60 m between 2003 and 2008. The annual mean air temperature and precipitation in this area between 2001 and 2008 were, respectively, -4.2°C and 433 mm. The ground begins to be free of snow in early July; snow begins to accumulate in mid-September. Several authors have studied the vegetation and suc- cession pattern in the glacier foreland of Austre Brøggerbreen (Nakatsubo et al. 2005; Ohtsuka et al. 2006), and of a neighbouring glacier (Hodkinson et al. 2003). Saxifraga oppositifolia is the most common pioneer plant in the newly deglaciated moraines of Austre Brøggerbreen, although it also occurs in later stages. Late stages are dominated by various species, including mosses, such as Sanionia uncinata (Hedw.) Loeske and Aulacomnium turgidum (Wahlenb.) Schwaegr., and vascu- lar plants, such as Saxifraga oppositifolia, Salix polaris, Dryas octopetala L. and Luzula confusa Lindeb. The early stage (Saxifraga stage) and the later stages of succession are divided spatially by the floodplain (Fig. 1). A recent study (Nakatsubo et al. 2008) showed that part of the later stage had developed on a raised beach deposit. Although Salix was rare in the early stage, colonization of scattered individuals of Salix was observed in the old part (near the floodplain) of the early stage. This stage is hereafter designated as the “seral stage”. Early in August 2008, a 30 m ¥ 30 m quadrat (quadrat A) was set in the seral stage. The distance between quadrat A and the front of the Austre Brøggerbreen glacier was about 1 km. For comparison, another 30 m ¥ 30 m quadrat (quadrat B), within which no Salix was observed, was set in the upper (more recently deglaciated) site of the deglaciated area. 1000 m A B 1977 1936 FP FP 2008 Fig. 1 Satellite image showing the study site in the glacier foreland of Austre Brøggerbreen, near Ny-Ålesund, Svalbard. Locations of the two quadrats (A and B), the glacier front terminus in 1936 and 1977, and the floodplain (FP) are also shown; they were determined using aerial photo- graphs from the Norwegian Polar Institute. Colonization of polar willow after glacier retreat T. Nakatsubo et al. Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd386 The two quadrats were situated in the middle of the two lateral moraines (west and east ridges) of Austre Brøgger- breen (Fig. 1). The respective vegetation coverage ratios (mainly Saxifraga oppositifolia) of quadrats A and B were about 3 and <1%, respectively. Accurate positions of these quadrats were determined using a portable GPS receiver (Trimble GeoXT GPS unit; Trimble Navigation, CA, USA) and a satellite image (Advanced Land Observ- ing Satellite multi-spectral Advanced Visible Near Infrared 2 sensor image, acquired on 31 July 2008). Aerial photographs from the Norwegian Polar Institute were used to demarcate successive changes visually at the glacier front terminus in 1936 and 1977. The quadrats were subdivided into 5 m ¥ 5 m subquad- rats, and the size, sex and position of each Salix plant within the subquadrat was recorded. Because the Salix colony shape varied widely, the length (L) and the maximum width (W) of the ground covered by each colony was measured: L ¥ W was used as the plant size index. A preliminary study indicated that there was a highly significant relationship between the index (L ¥ W) and the colony size (area) determined from photographs with an image scanner (r = 0.99; P < 0.001). The sex of each (male, female or unknown) was determined according to inflorescence. Seed production in female inflorescences of the current (2008) and previous year (2007) were also recorded. Individuals smaller than 1 cm2 were recorded as “seedlings”. To determine the seedling age, we collected all seedlings and counted leaf scars under a binocular microscope. At that time, the presence of mycorrhiza was also recorded. We examined the relation of Salix polaris to Saxifraga oppositifolia colonies. Each Salix individual was classified into one of the following three categories based on its position relative to Saxifraga: (1) Salix colony growing within the Saxifraga colony; (2) Salix colony growing close to Saxifraga (with at least one branch of the two species crossed); (3) Salix colony colonizing bare ground. To examine the study site soil characteristics, soil samples of the 0–3 cm layer were collected from 18 ran- domly selected subquadrats in each quadrat. Fresh weights of these samples were measured to obtain their water contents later. They were freeze-dried and brought back to Japan. The total carbon and nitrogen contents of the soil were measured using a CN analyser (Sumigraph NC-22; Sumika Chemical Analysis Co., Tokyo, Japan). Results and discussion Colonization of Salix polaris on the seral stage was observed only within 200 m of the riverbank. Although five isolated individuals of Salix were found between the two quadrats (A and B), we were unable to find any Salix individual between quadrat B and the glacier front. The aerial photograph taken in 1936 showed that the glacier front was near the riverbank; the study site was covered entirely by the glacier at that time. By 1977, when another photograph was taken, the site was left exposed by the glacier (Fig. 1). Although the site might have been subjected to disturbances after deglaciation, these data suggest that colonization of Salix commenced within the last 70 years. This rapidity of colonization is faster than some late successional species in other glacier forelands, e.g., Betula nana in a glacier foreland in main- land Norway (Whittaker 1993). However, although Saxifraga oppositifolia invaded near to the glacier front, Salix colonization was limited to the older part of the moraine, which suggests that the Salix invasion speed is insufficient to keep up with the recession speed, which was estimated as about 10–20 m annually (Svendsen et al. 2002). This pattern of colonization of Salix polaris and Saxifraga oppositifolia in our study site is somewhat different from that reported for the neighbouring glacier, Midre Lovén- breeen (Hodkinson et al. 2003), where isolated small seedlings of Salix were found in a pioneer site of as young as 2 years (Hodkinson et al. 2003). However, successional changes in frequency of occurrence and in ground cover were slower in Salix than in Saxifraga (Hodkinson et al. 2003: figs. 2, 3), which also suggests a limited ability of Salix to colonize pioneer sites. In quadrat A we found 115 Salix individuals (22 male, 13 female and 80 unknown, including seedlings), although the total coverage of Salix was less than 1%. The largest individual was 2000 cm2 (L ¥ W), but most (84%) of the individuals were smaller than 100 cm2 (Fig. 2a). The size structure of the colonizing population (Fig. 2a) resembles an inverted J-shaped size distribution: a popu- lation structure with a relatively constant juvenile supply (Mori et al. 2006). However, the fraction of individuals larger than 100 cm2 was very small, and the size distri- bution of the large individuals is discontinuous. Moreover, analysis of leaf scars revealed that the age of the small individuals classified as seedlings varied widely, ranging from less than 5 years to greater than 20 years (Figs. 2b, 3). Half of the seedlings had more than five leaf scars. Because most seedlings had two or three green leaves, it is estimated that most seedlings were older than several years. These results indicate that annual recruit- ment was quite limited: not more than 10 individuals in the 30 m ¥ 30 m quadrat. Regarding propagation by seeds, vegetative propaga- tion might play some role in Salix colonization. Reportedly, Salix polaris can form roots from shoot frag- ments, but this capability is rather limited compared with Colonization of polar willow after glacier retreatT. Nakatsubo et al. Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd 387 that of Saxifraga oppositifolia with its prostrate growth form, which has high rhizogenesis ability and which spreads vegetatively by shoot fragments (Kume et al. 1999). Apparently, the short above-ground part of Salix is unsuitable for propagation by shoot fragments. In fact, we were unable to find any rooted fragments of Salix in our study site. This difference in vegetative propagation might partly explain why Salix is rare in the early stage, and why Saxifraga oppositifolia dominates. Several factors might explain the small annual recruit- ment of Salix polaris at this study site. Seed availability can be a limiting factor of plant colonization in this area. Cooper et al. (2004), who examined the composition and density of soil seed banks in Svalbard, reported that Salix polaris is common in vegetation, but was a poor germi- nator in seed bank trials. At our study site, seven of the 13 females failed to bear seeds in 2008 (Table 1), suggesting the difficulty in seed set in this area. Additionally, we were unable to find even a single seedling around some female plants (Table 2), which suggests limited germina- tion and/or high seedling mortality in the field. Slow initial growth rate, as indicated by the analysis of leaf scars (Figs 2b, 3), might also contribute to the slow colo- nization of Salix at this site. It has been suggested that facilitation, the process by which colonizing species improve the environment for later successional species, is among the major succes- sional mechanisms in severe environments (Chapin et al. Fig. 2 Size distribution of the Salix polaris population at the study site. (a) The size distri- bution of Salix individuals found in quadrat A (n = 115). Sizes are expressed as the product of the length (L) and the maximum width (W) of the colony. (b) The size distribution of seed- lings based on the number of leaf scars, excluding cotyledons. 0 20 40 60 80 100 120 -9 9 1 0 0 -1 9 9 2 0 0 -2 9 9 3 0 0 -3 9 9 4 0 0 -4 9 9 5 0 0 -5 9 9 6 0 0 -6 9 9 7 0 0 -7 9 9 8 0 0 -8 9 9 9 0 0 - Size class (cm2 ) N u m b e r o f p la n ts Female Male Unknown (a) 0 2 4 6 8 10 12 0-4 5-8 9-12 13-16 17-20 21-24 25< Number of leaf scars + green leaves N u m b e r o f se e d lin g s (b) 10 mm C S C S M S S C C M M M M S Fig. 3 Salix seedlings of different ages: S, leaf scar; C, cotyledon or its leaf scar; M, mycorrhizal roots. Colonization of polar willow after glacier retreat T. Nakatsubo et al. Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd388 1994). If this applies to our study site, it is expected that the late successional species (Salix) colonizes sites where the early successional species (Saxifraga) has already been established. Our results did not support this hypothesis: about 75% of Salix individuals had colonized bare ground, although only four individuals grew within Saxi- fraga colonies (Table 2). This difference indicates that the presence of the preceding species is unimportant, at least for the initial stage of Salix colonization. Furthermore, no significant difference was found in soil characteristics (water content, and carbon and nitrogen concentrations) between the seral stage (quadrat A) and the Saxifraga stage (quadrat B) (Student’s t-test, P > 0.05) (Table 3). We also examined the correlation between soil characteristics (water content, and carbon and nitrogen concentrations) and the number of Salix individuals in the subquadrats of quadrat A. The relation was not found to be significant (n = 18, P > 0.05). Therefore, it is unlikely that coloniza- tion of Salix was limited by soil development in our study site. Another factor that might have affected the coloniza- tion of Salix is the presence of mycorrhizal fungi. Reportedly, colonization of mycorrhizal fungi facilitates subsequent seedling establishment of Salix species in a successional volcanic desert (Nara & Hogetsu 2004). At this study site, all Salix seedlings had ecotomycorrhiza. It is likely that whether the seedling was able to form a mycorrhizal association determined the survival of the seedling. This hypothesis should be tested through future study, including culture experiments. To conclude, Salix polaris is a later colonizer of the deglaciated area than the pioneer Saxifraga oppositifolia. However, the presence of the preceding species— Saxifraga—is not a prerequisite of Salix colonization. The slight annual recruitment, which might be explained by low seed availability, difficulties in germination and/or seedling establishment, has limited the colonization rate of Salix at this study site. The colonization rate is insuffi- cient to keep up with the speed of the glacier’s recession. The loss of the glacier in this region has accelerated in recent years, in response to climate change (Nuth et al. 2007). Therefore, it is unlikely that Salix will make an important contribution to carbon sequestration in newly exposed sites unless future climate change considerably raises its colonization rate. Acknowledgements The authors wish to thank Dr Kenlo Nishida Nasahara of the University of Tsukuba and the Japan Aerospace Exploration Agency for operating the advanced land observing “Daichi” satellite. This study was supported by a Grant-in-Aid for Scientific Research by the Japan Society for the Promotion of Science. References Chapin F.S. III, Walker L.R., Fastie C.L. & Sharman L.C. 1994. Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecological Monographs 64, 149–175. Cooper E.J., Alsos I.G., Hagen D., Smith F.M., Coulson S.J. & Hodkinson I.D. 2004. Plant recruitment in the High Arctic: seed bank and seedling emergence on Svalbard. Journal of Vegetation Science 15, 115–224. Crawford R.M.M., Chapman H.M. & Smith L.C. 1995. Adaptation to variation in growing season length in Arctic population of Saxifraga oppositifolia L. Botanical Journal of Scotland 47, 177–192. Green A.M. 2005. A time constant for hemispheric glacier mass balance. Journal of Glaciology 51, 353–362. Table 1 Seed production of each female Salix polaris plant. Individual females Seed production Presence of seedlings around the femalea2007 2008 1 + + + 2 + + + 3 + + + 4 + - + 5 + - + 6 + - - 7 + + - 8 - - + 9 + + - 10 + + + 11 - - + 12 + - - 13 + - - a Distance from the female to each seedling was less than 1 m. Table 2 Colonizing site of Salix polaris in relation to Saxifraga oppositi- folia within the 30 m ¥ 30 m quadrat. Colonizing site Number of Salix individuals Within a Saxifraga colony 4 Close to Saxifragaa 25 Bare ground 86 a With at least one branch of the two species crossed. Table 3 Some soil characteristics of the two 30 m ¥ 30 m quadrats. Mean values of soil samples (0–3 cm depth) collected from 18 randomly selected subquadrats (5 m ¥ 5 m) are shown with the SD. Soil characteristics Quadrat A Quadrat B Water contenta 0.15 � 0.06 0.15 � 0.06 Carbon concentration (%) 0.56 � 0.21 0.48 � 0.17 Nitrogen concentration (%) 0.03 � 0.01 0.03 � 0.01 a Water content = (fresh weight – dry weight)/dry weight. Colonization of polar willow after glacier retreatT. Nakatsubo et al. Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd 389 Hodkinson I.D., Coulson S.J. & Webb N.R. 2003. Community assembly along proglacial chronosequences in the High Arctic: vegetation and soil development in north-west Svalbard. Journal of Ecology 91, 651–663. Kohler J., James T.D., Murray T., Nuth C., Brandt O., Barrand N.E., Aas H.F. & Luckman A. 2007. Acceleration in thinning rate on western Svalbard glaciers. Geophysical Research Letters 34, L18502, doi: 10.1029/2007GL030681. Kume A., Nakatsubo T., Bekku Y. & Masuzawa T. 1999. Ecological significance of different growth forms of purple saxifrage, Saxifraga oppositifolia L., in the High Arctic, Ny-Ålesund, Svalbard. Arctic, Antarctic, and Alpine Research 31, 27–33. Mori A., Osono T., Iwasaki S., Uchida M. and Kanda H. 2006. Initial recruitment and establishment of vascular plants in relation to topographical variation in microsite conditions on a recently-deglaciated moraine on Ellesmere Island, High Arctic Canada. Polar Bioscience 19, 85–95. Muraoka H., Noda H., Uchida M., Ohtsuka T., Koizumi H. & Nakatsubo T. 2008. Photosynthetic characteristics and biomass distribution of the dominant vascular plant species in a High Arctic tundra ecosystem, Ny-Ålesund, Svalbard: implications for their role in ecosystem carbon gain. Journal of Plant Research 121, 137–145. Muraoka H., Uchida M., Mishio M., Nakatsubo T., Kanda H. & Koizumi H. 2002. Leaf photosynthetic characteristics and net primary production of the polar willow (Salix polaris) in a High Arctic polar semi-desert, Ny-Ålesund, Svalbard. Canadian Journal of Botany 80, 1193–1202. Nakatsubo T., Bekku Y., Kume A. & Koizumi H. 1998. Respiration of the belowground parts of vascular plants: its contribution to total soil respiration on a successional glacier foreland in Ny-Ålesund, Svalbard. Polar Research 17, 53–59. Nakatsubo T., Bekku Y.S., Uchida M., Muraoka H., Kume A., Ohtsuka T., Masuzawa T., Kanda H. & Koizumi H. 2005. Ecosystem development and carbon cycle on a glacier foreland in the High Arctic, Ny-Ålesund, Svalbard. Journal of Plant Research 118, 173–179. Nakatsubo T., Yoshitake S., Uchida M., Uchida M., Shibata Y. & Koizumi H. 2008. Organic carbon and microbial biomass in a raised beach deposit under terrestrial vegetation in the High Arctic, Ny-Ålesund, Svalbard. Polar Research 27, 23–27. Nara K. & Hogetsu T. 2004. Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85, 1700–1707. Nuth C., Kohler J., Aas H.F., Brandt O. & Hagen J.O. 2007. Glacier geometry and elevation changes on Svalbard (1936–90): a baseline dataset. Annals of Glaciology 46, 106–116. Ohtsuka T., Adachi M., Uchida M. & Nakatsubo T. 2006. Relationships between vegetation types and soil properties along a topographical gradient on the northern coast of the Brøgger Peninsula, Svalbard. Polar Bioscience 19, 63–72. Svendsen H., Beszczynska-Møller A., Hagen J.O., Lefauconnier B., Tverberg V., Gerland S., Ørbæk J.B., Bischof K., Papucci C., Zajaczkowski M., Azzolini R., Bruland O., Wiencke C., Winther J.-G. & Dallmann W. 2002. The physical environment of Kongsfjorden– Krossfjorden, an Arctic fjord system in Svalbard. Polar Research 21, 133–166. Whittaker R.J. 1993. Plant population patterns in a glacier foreland succession: pioneer herbs and later-colonizing shrubs. Ecography 16, 117–136. Colonization of polar willow after glacier retreat T. Nakatsubo et al. Polar Research 29 2010 385–390 © 2010 the authors, journal compilation © 2010 Blackwell Publishing Ltd390