ECOGRAPHY 27: 311 /322, 2004
Seed dispersal and seedling establishment of Rhus trichocarpa promoted by a crow (Corvus macrorhynchos) on a volcano in Japan Hideo Nishi and Shiro Tsuyuzaki
Nishi, H. and Tsuyuzaki, S. 2004. Seed dispersal and seedling establishment of Rhus trichocarpa promoted by a crow (Corvus macrorhynchos ) on a volcano in Japan. / Ecography 27: 311 /322. The interaction between frugivorous birds and trees producing bird-dispersed seeds in devastated areas has been considered to be weak, owing to the paucity of avifauna and/ or food resources for birds. Here, we present evidence that strong interactions between birds and plants may promote the enlargement of tree distribution on harsh environments. The summit of Mount Koma, northern Japan, was denuded by the 1929 volcanic eruption. Vegetation cover gradually decreases from the bottom (secondary forest) to the top (bareground) of the mountain. We recorded 48 bird species in the four seasons of 2001, along a 5-km line transect on the southwestern slope of the mountain. Birds faeces collected along the transect contained seeds of more than 14 plant taxa. Five of the 14 taxa were bird-dispersal tree species (Rhus trichocarpa , Sorbus commixta , Prunus ssiori , Prunus maximowiczii and Prunus sargentii ) and were established in the summit area. Most faeces were derived from Corvus spp. (mostly C . macrorhynchos ) and Turdus naumanni . In particular, the seeds of R . trichocarpa were found mostly from the faeces of Corvus spp. and the seeds of Gaultheria miqueriana , a shrub species, were only from T. naumanni . Rhus trichocarpa retained fruits on the canopy at all times of the year, and crows could feed on them even when food resources were poor in winter. Rhus trichocarpa seedlings established well near rock at higher elevation, while they occurred mostly under the larch canopy of larches at lower elevation. Crows mostly utilized tree canopies and rocks as perches in respective habitats. Therefore, seedlings should be abundant in specific habitats at different elevations. Size-class distribution of seedlings suggested that seedling mortality was lower at higher elevation where open sites were more abundant. These findings indicate that strong mutual advantages for C. macrorhynchos and R . trichocarpa on denuded areas play an important role on revegetation. H. Nishi and S. Tsuyuzaki (correspondence:
[email protected]), Graduate School of Environmental Earth Sci., Hokkaido Univ., Sapporo 060-0080, Japan.
In early succession on terrestrial volcanoes, long-distance seed dispersal is common. However, wind appears to be the most important dispersal agent (Tsuyuzaki and del Moral 1995, Haruki and Tsuyuzaki 2001), with animal-dispersal including bird-dispersal contributing little to revegetation on debris avalanches (Nakashizuka et al. 1993). One reason for the low amount of animal dispersal is that animal species richness and abundance are low in the early stages of succession, owing to the paucity of food resources (Brown and Southwood 1987).
For example, after the 1980 catastrophic eruption on Mount St. Helens, Washington, USA, bird recolonization took many years (Manuwal et al. 1987). Therefore, seed dispersal by birds has been little mentioned in studies of the early stages of volcanic succession. While plant colonization on newly-emerged oceanic islands is mostly via long-dispersal agents such as water (sea current), birds, bats and wind (Fridriksson and Magnusson 1992, Partomihardjo et al. 1992, Shanahan et al. 2001).
Accepted 19 November 2003 Copyright # ECOGRAPHY 2004 ISSN 0906-7590 ECOGRAPHY 27:3 (2004)
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To predict plant community dynamics, seedling establishment patterns must be understood, in particular, on severe and/or infertile environments (Maruta 1983, Yura 1988) because seedlings may be often more sensitive than adults to the environments (Silvertown and Lovett Doust 1993). For seedling establishment, microhabitats are critical in primary succession (Titus and del Moral 1998). Seed germination of pioneer species is also influenced by micro-environments such as temperature, moisture and topography (Baskin and Baskin 1998). Vegetation on the summit area of Mount Koma, northern Japan, was completely destroyed by the 1929 volcanic eruption which produced 0.38 km3 ash and 0.14 km3 pumice, and the resulting mudflows destroyed most vegetation on the slopes (Yoshii 1932). To this date, the vegetation cover is sparse on the summit. A winddispersed, locally introduced tree Larix kaempferi is abundant on the slopes (Kondo and Tsuyuzaki 1999), while bird-dispersal trees, in particular, R . trichocarpa , also are established there. To clarify why and how birddispersal tree species could establish even in the harsh environments, we first studied what bird species acted as seed vectors and what plant species were dispersed by birds? Fruiting phenology is synchronized with seasonal changes in bird populations (Loiselle and Blake 1991). Therefore, to detect relationships between birds and fruiting plants, we monitored fruiting phenology on bird-dispersal tree species. Finally, we determined if the seedlings of those species survived and established in the dispersed area.
Study area and methods Mount Koma is an active andesite stratovolcano located in a southwestern part of Hokkaido Island, Japan (42804?N, 140842?E, 1131 m in altitude) (Fig. 1). The summit has a 2-km wide horseshoe-shaped caldera opening to the east. After the 1929 large one day eruption, the volcano did not erupt again until 1942 when a medium eruption was recorded. A few smallscaled phreatic explosions occurred during 1996 and 2000, but they did not affect the ecosystems in the study area (Uesaka and Tsuyuzaki, in press). The ground surface mostly was covered with pumice on the slopes (Yoshii 1932), and boulders were sparsely distributed. There is a trail up to the top of the mountain on the southwestern slope. The trail is paved from the base up to 370 m, and then is unpaved up to the top. Since government permission was required to enter the mountain owing to the recent eruptions, human impact was minimal during the surveyed period. The climate is warm-cool temperate. The mean annual temperature is 11.68C (maximum/24.68C in August, and minimum/ /6.98C in January) at Mori Climatological Observatory 9 km from Mount Koma (10 m in altitude), and the mean annual precipitation is 973 mm (Anon. 1963 /1994). The vegetation on Mount Koma has not attained any climax due to the eruptions (Kondo and Tsuyuzaki 1999). The upper limit of forest line before the 1929 eruption extended to 900 /800 m, and now the treeline is depressed and ragged. Lichens and mosses are common
Fig. 1. Study area. A: Location of Mount Koma on Hokkaido Island, Japan. B: Study area. Polygon shown by thick solid lines is an area for line transect. The boundaries of vegetation determined by TWINSPAN are represented by thick solid lines within the polygon. BG (Bareground): 685 /890 m, LB (Larix kaempferi and Betula ermanii ): 500 /685 m, PB (Populus sieboldii and Betula platyphylla var. japonica ): 345 / 500 m, SF (Secondary forest): 245 /345 m.
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at high elevation, and Salix reinii and G. miqueliana occur in scattered patches. A secondary forest has developed on the mountain B/350 m, and it is assumed to be a major seed source for most species, including bird-dispersal species. The forest floor is mostly covered with herbaceous plants, but dwarf bamboos, Sasa spp., which are common in natural forests in Hokkaido (Hino 1993), were not observed.
storing, were determined by the field observations and references (Karasawa 1978, Higuchi 1991, Ueda 1992). ANOVA and Scheffe´’s test were used for identifying differences in distribution pattern between the bird species. All statistical analyses were conducted by StatView ver. 5.0.1 (Anon. 1999), except for TWINSPAN. ANOVA and post hoc tests were performed by default setting without data transformation.
Altitudinal distribution of vegetation
Seed transportation by birds
Fifty-five 20/20 m plots were established at 245 /880 m to obtain elevational distribution patterns of vegetation. In each plot, the taxa, height and diameter at breast height were recorded of all individual plants /1.3 m in height. TWINSPAN (two-way indicator species analysis) cluster analysis was conducted based on the number of trees, using PC-ORD ver. 4.27 (Anon. 2002a). Based on TWINSPAN, we divided into four elevational zones of plant communities; BG/bareground (890 /685 m), LB /Larix kaempferi and Betula ermanii (685 /500 m), PB /Populus sieboldii and Betula platyphylla var. japonica (500 /345 m), and SF /secondary forest (345 / 245 m) (Fig. 1).
Faeces containing seeds were collected from an area in 5 m wide along the line transect during May and December 2001. Bird species that dropped faeces were identified by the characteristics of faeces, e.g., size, shape and color, using voucher faeces collected when we directly observed birds dropping faeces. Seeds in the faeces were identified by comparing them with seeds collected from the study area and seed germination tests. Ten ingested seeds were placed on five-layered filter papers moistened with distilled water in 9-cm-diameter Petri dishes at 25oC/5oC (12h:12h) with continuous light. Number of seeds in each faeces was counted, except for G. miqueliana . Due to a large number of fine seeds for G. miqueliana , seed germination test using five faeces was used to estimate the number of seeds. The five faeces were directly placed on filter papers, as described above. After 30 days, the emerged seedlings were counted and used as seed number (average seedlings per faeces / 1849/30, mean with standard deviation). To investigate the seed viability of R . trichocarpa after ingestion by birds, we cut fifty seeds and the albumen; seeds with white and/or hard embryos were considered as viable (Tsuyuzaki and Goto 2001).
Bird distribution A 5-km line transect was set up along a trail to conduct bird census (Bibby et al. 2000) (Fig. 1). The census was conducted at 2-week intervals in the snow-free period (April /December 2001), and 1-month intervals in winter (January /March 2002). The sampling was not carried out under rain and/or snow conditions. Two days were used for each census. We started the observation at sunrise from 225 m in elevation walking at ca 1.5 km/h and finished at 950 m the first day. We walked the opposite direction in the following day. The observation ranges were 50 m between 225 m and 450 m in elevation, and 100 m over 450 m in elevation, depending on the visibility. Whenever we observed any birds, species, number of individuals, and locations were recorded. The locations were recorded on latitude, longitude and altitude by a GPS receiver. To evaluate altitudinal distribution patterns of birds, the altitudinal range between 225 and 950 m was divided into 29 classes. Based on the density of each bird species in each class, TWINSPAN cluster analysis was conducted. Species observed only in one class were not used for the analysis. Species richness and individual number were averaged in each cluster group determined by TWINSPAN. The mean among the groups was compared by ANOVA, and Scheffe´’s test was applied for the multiple comparison when a significant difference was obtained by ANOVA. For widespread bird species, feeding habit types, i.e., fruit-swallowing and foodECOGRAPHY 27:3 (2004)
Phenology of fruit storage on crown Five individuals on each bird-dispersal woody species were marked in the study area. The presence or absence of fruits on canopies was recorded at 2-week intervals in 2001. The beginning of fruit production was when the first individual produced fruits. The retention of fruits on the crowns was recorded until all individuals released fruits. Rhus trichocarpa developed canopy seedbank, i.e., fruits held on trees throughout year. On this species, lastyear fruits were recorded separately from current fruits.
Seedling distribution of trees producing birddispersed seeds A belt transect (2000 m long and 50 m wide) was set up on the left side of the bird census line in LB and BG (Fig. 1). To avoid the effect of the trial, area within 5 m of the trial was not used. Seedlings (range: 0 /1.3 m high) of 313
bird-dispersal tree species with a potential maximum height /1.3 m were counted and recorded their height, location and microhabitat. To evaluate seedling establishment patterns, microhabitats were divided into four categories: under-larch (area under the canopy of L . kaempferi ), near-rock (area within 1 m from a boudler/50 cm in diameter), patch (shrub patch of Salix reinii and/or G. miqueliana /50 cm in diameter) and bareground. The relative dominance of each microhabitat was measured by ten 100 m lines on both sides of the line transect for bird census in LB and BG. Seedling densities among microhabitats in LB and BG were examined by x2-test, assumed as uniform distribution. Rhus seedlings were sampled and age was determined by counting the number of whorls and/or year rings on LB and BG. The origin of plants, i.e., seedling or sprouting, was confirmed by digging where seedlings crowded. Relationships between seedling age (x, yr) and height (y, cm) were fitted to log-transformed linear regressions lny//0.76lnx/1.16; r2 /0.296 (n /26, pB/0.01) on LB, and lny /1.06lnx/0.48; r2 /0.447 (n /34, pB/0.05) on BG. Analysis of covariance indicated that there was no significant difference between the slopes of the two fitted lines, suggesting that the height-class relationships could be surrogate to investigate age-class relationships between LB and BG. Therefore, establishment patterns of seedlings were compared between LB and BG based on height-class distribution. Two classes were defined, i.e., 0 /10 cm and /10 cm. Approximate age of stems with 10 cm in height was 5 yr.
Soil temperature Temperatures 0.5 cm below the ground surface were measured every 1 hr from July to September, 2002, by seven automatic thermometers. Thermometers were established in open site and under the canopy at 800, 600 and 450 m, and under the canopy at 350 m. Here, open site meant the ground surface is not covered with vascular plants, and bareground and near-rock were included into open site. Mean soil temperature and range of daily fluctuation (maximum / minimum in a day) were compared between elevations and microhabitats by ANOVA and Scheffe’s post hoc test.
Results Distribution pattern of plant communities TWINSPAN recognized four plant community types along the elevational gradient (Fig. 1). BG was dominated by L . kaempferi and was distributed at the highest elevation, although the average stem density was nine per 20 /20 m plot and nearly all stems were B/3 m in 314
height. Therefore, trees were not major plant community components, and most ground surface directly received solar radiation. LB was distinguished by the dominance of L . kaempferi and Betula ermanii . The stem density was still low, i.e., 20 stems per plot, and average tree height was 2.6 m. In BG and LB, the cover of vascular plants was poor. PB was represented by the dominance of P. sieboldii and B. platyphylla var. japonica distributed mostly at middle elevation. The average stem density was 78, and maximum stem height was 10.5 m. SF was the secondary forest, which had a crown height of 15 /20 m, with various deciduous trees, e.g., Quercus mongolica var. grosseserata , Prunus ssiori and Acer japonicum . All plots in SF were distributed at the lowest elevation. There was no elevational overlap of plant communities between PB and SF that were distributed in lower elevation, while the boundaries between the other groups were somewhat overlapped. The centers of overlapped areas were used as boundaries between plant communities for further analyses.
Distribution pattern of birds In total, 48 bird species were recorded, and 34 were observed in two or more elevational classes (Table 1). TWINSPAN distinguished four clustering groups. Classes were divided into two groups, and each group was divided into two subgroups. The first and second subgroups were separated from the third and fourth subgroups by the high frequency of Emberiza spodocephala . The first and second subgroups, which were divided by the presence/absence of Parus ater, had only four and six classes, respectively. The difference between the first and second subgroups was due to low species richness, and thus the elevational distributions of the two subgroups overlapped. However, the distribution of the other clustering groups did not overlap in elevations. Therefore, the first and second subgroups were merged to investigate the altitudinal distribution of birds, and three elevational zones of bird distribution were distinguished (hereafter, H /high, M /middle and L /low zones). The distribution of H was roughly consistent with BG, M was overlaid on LB and PB, and that of L was on SF. Most bird species were observed in L with high frequency, and bird species richness decreased with increasing elevation (Table 1). The most common species in L were Turdus naumanni and Corvus macrorhynchos, and these two species also were observed in H. Alauda arvensis and Anthus hodgsoni frequently were observed in H, and Alauda arvensis was common in H and M. Of species occurring in all elevational zones with high frequency, four species, P. ater, C. macrorhynchos, T. naumanni and Sitta europaea , are well-known to disperse seeds by fruit-swallowing or food-storing. The ECOGRAPHY 27:3 (2004)
Table 1. Bird species observed on the southwestern slope of Mount Koma during May 2001 and April 2002. Bird communities classified by TWINSPAN, based on individual number of birds (ha 1 hour1) in 29 elevational classes are shown. 34 species ]/two elevation classes were used. Mean density of bird (ha 1 hour1) per plot are represented. /, no individual observed. For mean species richness and total number of birds, the same letters indicate no significant difference at p B/0.05 (Scheffe’s test). Cluster code Number of classes Vegetation Altitude (m)
High 10 BG-LB 675 /950
Middle 9 LB-PB 450 /675
Low 10 PB-SF 225 /450
Total mean 29
Species* Turdus naumanni Anthus hodgsoni Corvus macrorhynchos Emberiza cioides Parus ater Parus major Sitta europaea Eophona personata Garrulus glandarius Zoothera dauma Alauda arvensis Emberiza spodocephala Parus palustris Carduelis sinica Cettia diphone Aegithalos caudatus Hypsipetes amaurotis Dendrocopos major Pyrrhula pyrrhula Lanius bucephalus Zosterops japonicus Turdus chrysolaus Sphenurus sieboldii Erithacus akahige Parus varius Luscinia cyane Dendrocopos kizuki Corvus corone Streptopelia orientalis Ficedula narcissina Urosphena squameiceps Coccothraustes coccothraustes Uragus sibiricus Cuculus canorus Mean species richness (plot 1) Mean total number of birds (ha 11 hr 1)
0.24 1.43 0.26 0.08 0.49 0.03 0.13 0.04 0.04 0.04 1.82 / / / / / / / / / / / / / / / / / / / / / / / 3.50 4.61
1.60 1.60 0.81 0.69 0.52 0.24 0.20 0.02 0.29 0.03 0.20 1.13 0.55 0.40 0.14 0.06 0.02 0.06 0.04 0.10 0.04 0.04 0.02 0.02 0.02 0.01 / / / / / / / 0.03 11.78 8.89
2.38 0.49 1.26 0.58 0.31 0.88 0.40 0.60 0.17 0.02 / 1.08 1.17 0.69 0.28 0.30 0.24 0.16 0.17 0.03 0.04 0.01 0.02 0.02 0.01 0.01 0.33 0.26 0.23 0.17 0.09 0.04 0.02 / 22.10 12.48
1.41 1.17 0.78 0.45 0.44 0.39 0.24 0.22 0.17 0.03 0.68 0.74 0.57 0.36 0.14 0.12 0.09 0.07 0.07 0.04 0.02 0.02 0.01 0.01 0.01 0.01 0.11 0.09 0.08 0.06 0.03 0.01 0.01 0.01 12.48 8.66
a a
b b
c b
225 /950
Others: Milvus migrans, Picus canus, Motacilla cinerea , Motacilla grandis, Troglodytes troglodytes, Tarsiger cyanurus, Turdus obscurus, Locustella lanceolata , Phylloscopus coronatus, Regulus regulus, Emberiza fucata , Emberiza variabilis, Carduelis flannea , Sturnus cineraceus. Nomenclature follows the Anon. (2000b).
abundance of T. naumanni was significantly higher in PB and lower in BG (Fig. 2). Corvus macrorhynchos decreased abundance with increasing elevation. Parus ater and S. europaea showed no significant differences in individual numbers between all plant community types, probably due to low individual numbers. In the highest elevational zone, BG, individual numbers were not significantly different between the four species, suggesting that all of these species had a similar potential to carry seeds to high elevations. The other frugivorous birds had low density and/or were not observed in BG.
Relationship between phenology of fruits and birds Fourteen woody species producing bird-dispersed fruits were recorded (Fig. 3). All of those species produced ECOGRAPHY 27:3 (2004)
fruits in autumn, except Prunus sargentii and P. maximowiczii which produced fruits during spring and summer. Rhus trichocarpa maintained an aerial seedbank throughout year. Fruits of R . trichocarpa had a small amount of pulp, ranged from 2.3 /4.2 mm in diameter and were dry soon after ripening, while those of the other trees had fleshy pulp. The number of individuals of frugivorous birds exhibited seasonal fluctuations, and the highest peak was recorded by T. naumanni in late fall, i.e., October (Fig. 4). Due mostly to this peak, T. naumanni showed the highest total number of individuals during the survey period, however, this species was not abundant in the other seasons. Most of the individuals of Corvus spp. belonged to C. macrorhynchos (Table 1), and seasonal fluctuation of numbers was rather stable (Fig. 4). Even in winter, Corvus spp. stayed in the region. In fact, field 315
Fig. 2. Appearance frequency of Turdus naumanni , Corvus macrorhynchos, Parus ater and Sitta europaea on four elevational zones. The same letters indicate non-significant difference at pB/0.05 (Scheffe´’s test). Error bars are 0.1 SD of the mean. N.S., not significant.
observations confirmed that a few Corvus individuals stayed throughout year. Most of the other species showed a peak in fall. There were 623 faeces collected from the study area. Few bird-regurgitated pellets were found in the study area, and none included seeds. Therefore, the effects of regurgitation on seed dispersal were insignificant. Of the faeces collected, 72% and 23% were derived from T. naumanni , and Corvus spp., respectively (Table 2). Total number of seeds in the faeces was 14346. The faeces of T. naumanni and Corvus spp. contained 12079 (84.2% of total) and 2066 (14.4%) seeds, respectively. The total number of seeds extracted from Turdus and Corvus explained 98.6% of total seeds, indicating that those two species were major seed dispersers.
More than 14 plant species were extracted from dropped faeces, and 13 species were identified (Table 2). Tree taxa were R . trichocarpa , Magnolia obovata and Prunus spp. There were three species of Prunus (P. ssiori , P. sargentii and P. maximowiczii ) growing in the study area. All G. miqueliana seeds that ripened mostly in October (Fig. 5) were obtained from Turdus faeces, and accounted for 79% of the seeds detected from Turdus, suggesting that Turdus was a major seed disperser for G. miqueliana . Seeds of Celastrus orbiculatus, a vine, were the most abundant in T. naumanni faeces in November, but they also were common in the faeces of Corvus spp. and other species. About 97% of the R . trichocarpa seeds and 77% of the Prunus spp.
Fig. 3. Periods of ripened fruits stayed on canopies. Black columns indicate the terms of ripened fruits borne in 2001 and hatched columns show those in 2000.
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Fig. 4. Seasonal variation of frugivorous bird abundance. Others include 23 frugivorous birds (Streptopelia orientalis, Sphenurus sieboldii , Dendrocopos major, Hypsipetes amaurotis, Zoothera dauma , Turdus chrysolaus, Turdus obscurus, Cettia diphone, Parus palustris, Parus ater, Parus varius, Parus major, Sitta europaea , Zosterops japonicus, Emberiza spodocephala , Carduelis sinica , Carduelis flammea , Uragus sibiricus, Pyrrhula phrrhula , Eophona personata , Coccothraustes coccothraustes, Sturnus cineraceus, and Garrulus glandarius ).
seeds were obtained from the faeces of Corvus spp. Viability of R . trichocarpa seeds was 74%. In contrast to the two dominant plant species in the faeces that showed sharp peaks of seed dispersal duration, R . trichocarpa seeds were obtained from Corvus faeces throughout snow-free periods. We could not collect faeces in snow season owing to snow cover and did not observe crows fed on Rhus fruits directly. However, Corvus spp. were observed even in winter (Fig. 4), and R . trichocarpa retained fruits on the crown (Fig. 3). Also, we collected the faces of crows containing Rhus seeds soon after the snow thaws. Those findings indicated that Corvus could feed on R . trichocarpa fruits throughout year.
Fig. 5. Seasonal variation of number of seeds in the faeces of the two common bird taxa and others. See also Table 3.
Elevational distribution of faeces and seedlings Total number of collected faeces decreased with increasing elevation (Fig. 6), and this pattern was roughly
Table 2. Number of seeds on each seed plant taxa in bird faeces collected. Numbers of faeces that contained seeds are shown in parentheses. /, no faeces observed. *, estimated by germination test. Plant species
Gaultheria miqueliana Celastrus orbiculatus Rhus trichocarpa Aralia elata Vitis coignetiae Viburnum dilatatum Elaeagnus umbellata Magnolia obovata Schisandra chinensis Actinidia arguta Prunus spp. Rubus sp. Liliaceae sp. Unidentified Total
ECOGRAPHY 27:3 (2004)
Life form
Shrub Vine Tree Shrub Vine Shrub Shrub Tree Vine Vine Tree Shrub Herb
Bird species Turdus naumanni
Corvus spp.
Others
Total
9568* (52) 2075 (301) 7 (3) 202 (17) 46 (14) 35 (20) 35 (11) / 12 (10) 8 (1) / / 16 (9) 75 (13) 12079 (451)
/ 970 482 / / 8 / 29 4 1 10 382 / 180 2066
/ 103 9 8 12 / 2 / / / 3 / 2 62 201
9568 3148 498 210 58 43 37 29 16 9 13 382 18 317 14346
(78) (48) (3) (3) (3) (1) (4) (1) (2) (143)
(15) (3) (1) (1) (1)
(1) (2) (5) (29)
(52) (394) (54) (18) (15) (23) (12) (3) (13) (2) (5) (1) (11) (20) (623)
317
Effects of microhabitat and elevation on seedling establishment The relative dominance of microhabitats was significantly different between LB and BG (Table 3). Bareground, patch and under-larch showed similar relative dominance and near-rock was least in LB, while bareground was predominant and under-larch was lower in BG. Near-rock was less in both LB and BG, although the relative dominance was higher in BG. For R . trichocarpa in LB and BG, respectively, seedling densities were significantly different among microhabitats (Table 3). The most favorable sites for seedling emergence and/or establishment were different between LB and BG, i.e., the density was the highest under the larch canopy in LB and near rock in BG. Seedling density on near-rock in BG showed the highest seedling density, and that under the canopy in LB was slightly lower. Those two microhabitats showed more than seven times higher densities than the other microhabitats. Patch microhabitat showed the lowest seedling densities in LB and BG. Therefore, under-larch was the most favorable microhabitat for the establishment of R . trichocarpa seedlings in the overall areas. Additionally, near-rock is the most important site for seedling establishment of R . trichocarpa in bareground located at higher elevation. Maximum and minimum soil temperatures were recorded in the open site (Table 4). Maximum soil temperature was 44.68C, at 600 m, and the minimum was 5.68C, at 800 m. Mean soil temperature was higher and fluctuated more in the open site than under the larch canopy at each elevation. Mean soil temperature under the canopy in the lowest elevation was not significantly different from that on open site in the highest elevation, although the range of daily fluctuations differed between open site and under the canopy, regardless of elevational differences. These results indicated that, in BG, the range of soil temperature fluctuation in open site was greater
Fig. 6. Density of faeces in the four plant community types, SF/secondary forest, PB/Populus maximowiczii and Betula platyphylla var. japonica forest, LB/sparse Larix kaempferi and Betula ermanii forest, and BG/bareground.
consistent with the pattern of number of birds observed (Table 1). Turdus faeces decreased drastically with increasing elevation, and they were not collected from LB and BG. Corvus faeces also decreased in number with increasing elevation, but the decrease was more gradual. Seedlings of five bird-dispersal tree species, R . trichocarpa , Sorbus commixta , Prunus ssiori , P. sargentii and P. maximowiczii , established in LB and BG, and the density decreased with increasing elevation, as well as number of faces. Total seedling density was approximately 555.0 ha1, and most of them were R . trichocarpa with 802.1 ha1 and 98.2 ha1 on LB and BG, respectively. Stem density of S. commixta seedlings was 89.7 ha1 on LB and 8.9 ha1 on BG, although no seeds were collected from any bird faeces (Table 2). Seedling density of Prunus spp. was 29.9 ha 1 on LB, while there were no Prunus seedlings on BG.
Table 3. Relative abundance of microhabitats and Rhus trichocarpa seedling density (ha 1) on each microhabitat in two plant communities, LB (Larix kaempferi and Betula ermanii ) and BG (bareground). Relative abundance of microhabitats was significantly different between LB and BG, and seedling density was significantly different among microhabitats in each plant community at p B/0.001 (x2-test). Microhabitat
Plant community type LB
Under-larch Near-rock Patch Bareground Total
318
BG
Seedling density (ha 1)
Relative abundance of microhabitat
Seedling density (ha 1)
Relative abundance of microhabitat
2854.3 278.7 67.1 143.5 802.1
25.3% 0.2% 34.9% 39.6% 100.0%
413.4 2923.4 51.7 66.3 98.2
3.6% 0.8% 18.5% 77.1% 100.0%
ECOGRAPHY 27:3 (2004)
Table 4. Soil temperature at 0.5 cm below the soil surface during July 4 and September 24 in 2002. For soil temperatures of maximum and minimum, observed dates are shown in parentheses. Mean soil temperature and mean daily fluctuation of soil temperature are shown by mean with S. D. The same letters indicate non-significant difference at p B/0.05 (Scheffe’s test). Soil temperature (oC)
Elevation (m) 350
Maximum Minimum Mean Daily fluctuation range
450
600
800
Under-larch
Open site
Under-larch Open site
Under-larch
Open site
25.5 (Jul 25) 8.2 (Sep 24) 16.69/2.9 cf 4.99/2.8 b
38.8 (Jul 26) 8.6 (Sep 14) 19.49/5.1 e 10.59/6.0 a
31.0 (Sep 5) 8.9 (Sep 24) 17.59/3.5 a 6.59/4.2 b
29.7 (Jul 26) 7.3 (Sep 24) 16.49/3.6 b 6.19/3.6 b
40.8 (Jul 25) 29.3 (Sep 15) 5.6 (Jul 22/24) 6.5 (Sep 24) 17.59/5.8 15.99/3.8 a b 11.99/7.4 6.99/4.7 a b
than that under the canopy and soil temperature should exceed 458C.
Height-class distribution on Rhus trichocarpa Root excavations confirmed that nearly all Rhus stems were derived from seedling. Rhus trichocarpa stemsB/10 cm in height showed higher seedling densities (621.5 ha 1) than seedlings ]/10 (179.5 ha1) on LB, while stems ]/10 cm were more abundant (60.0 ha1), than stems B/10 cm (38.2 ha1) on BG. In the class of stem height B/10 cm, seedling density at BG was ca 20 times higher than at BG. These results suggested that the number of emerged seedlings was higher at LB than at BG but seedling mortality was higher at LB. In contrast, seedling emergence was lower but the seedling mortality was lower at BG. Therefore, BG was likely to be more preferable for the seedling establishment of R . trichocarpa .
44.6 (Jul 26) 6.2 (Sep 14) 18.69/6.2 d 13.29/8.3 a
Under-larch
USA, 10 yr after the 1980 eruption (Frenzen and Crisafulli 1990). Corvus macrorhynchos was often observed on the summit of Mount Koma, even in winter season, while C. corone was infrequent. Corvus macrorhynchos prefers living in various habitats, e.g., forests, agricultural areas and residential areas from lowland to highland in central and south-eastern Hokkaido, while C. corone inhabits mostly agricultural and residential areas B/400 m (Higuchi 1979, Fujimaki 1998). Difference in observed frequencies between C. macrorhynchos and C. corone can be accounted for differences in habitat preferences, and therefore, of the two Corvus species, the major seed disperser was C. macrorhynchos rather than C. corone on the mountain. Based on the collected faeces, Corvus spp. often fed on R . trichocarpa seeds and T. naumanni mostly fed on G. miqueliana seeds. It is well-known that C. macrorhynchos and C. corone normally eat carrion but they are omnivorous (Madge and Burn 2001). Corvus species is apt to prefer dry-fruits such as Rhus, while species in Turdidae feed mostly on fleshy fruits (Ueda 1992).
Discussion Behavioral characteristics of dominant frugivorous birds
Relationships between phenology of fruit storage on crown and birds
On Mount Koma, two Corvus species, C. macrorhynchos and C. corone, were observed. Corvus macrorhynchos and C. corone are widespread in Japan and their areas of distribution overlap (Anon. 2000, Madge and Burn 2001). Corvus species tend to appear in disturbed areas such as volcanoes. For example, on a volcanic island, Anak Krakatau, Indonesia, C. macrorhynchos was found within decade after the volcanic activities (Zann and Darjono 1992). On Surtsey Island, Iceland, newly-emerged in 1963 from the ocean, C. corax was first seen in 1965 (Fridriksson and Magnusson 1992). Corvus corax was found in the most heavily-disturbed areas on Mount St. Helens,
Of the trees with bird-dispersed seeds on Mount Koma, only R . trichocarpa developed an aerial seedbank. Corvus spp. utilized R . trichocarpa fruits when of other trees were gone. Trees with specialized seed dispersers in winter have long fruiting duration (Howe and Estabrook 1977, Herrera 1982). Corvus macrorhynchos was likely to feed on R . trichocarpa fruits throughout year. The other birds could not disperse seeds by fruit-swallowing. Corvus macrorhynchos must be a specific seed disperser for R . trichocarpa on Mount Koma. In contrast to the relationship between R . trichocarpa and C. macrorhynchos, T. naumanni is an opportunistic
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disperser for G. miqueliana seeds. In fall, G. miqueliana produced fleshy fruits that contain numerous seeds. Gaultheria miqueliana fruits were great food resources for T. naumanni , and thus the immigration timing of T. naumanni was synchronized with the duration of the fruit production.
Significance of seeds dispersed by frugivorous birds The establishment of seedlings under the canopy of parental plants is inappropriate for R . trichocarpa because it is a shade-intolerant tree and has high mortality by shading, competition and/or predation (Howe and Smallwood 1982). Neotropic early successional trees have longer fruiting duration than climax forest trees, and long-time storage of seeds and fruits on the crown increases the probability that seeds reach forest gaps (Rathcke and Lacey 1985). The interaction between aerial fruit storage on R . trichocarpa and feeding by C. macrorhyncos should increase the probability of long-distance seed dispersal. Flying distance of larger birds including Corvus is generally superior to that of smaller birds. Furthermore, retention time of ingestion, i.e., recovery of the last viable seed, for large birds is longer than that of small birds (Vernon 1968, Howe and Kerckhove 1980). An interval between seed ingested by C. cryptoleucus and the last viable seed recovered from faeces was 14 h for R . glabra (Vernon 1968). The data suggest that seed dispersal by Corvus promotes longer-distance dispersal of seeds, although the number of seeds carried by crows decreased with increase in distance from seed sources. Impermeable hard seed or fruit coat often delays seed germination (Baskin and Baskin 1998). Rhus trichocarpa seeds also is impermeable. In such seeds, various pretreatments, such as acid and mechanical scarification, that are imitations of conditions to seeds digested by mammals and birds, release physical seed dormancy. However, a preliminarily seed germination experiment suggested that the effects of seed ingestion by crows on seed germination influenced little for R . trichocarpa (Nishi, unpubl.). Turdus naumanni is a middle-sized bird, and behavioral characteristics are the opposite to those of C. macrorhynchos. Turdus seems to contribute the establishment of G. miqueliana within a habitat, and not to contribute to enlargement of distribution.
Effects of microhabitats on seed germination and establishment for R . trichocarpa For R . trichocarpa , under-larch showed the highest seedling density at lower elevation and relatively higher density at higher elevation. The crows often used larch as 320
perch, and thus the seedlings could be accumulated below. Perches facilitate succession by increasing the diversity of seed deposition (McDonnell and Stiles 1983, McClanahan and Wolfe 1987, Guevara and Laborde 1993). In a Mediterranean region, the highest density of Rhus spp. seeds was observed under the canopy of isolated trees that are favorable perching places for the seed dispersers (Debussche and Isenmann 1994). Light quality and quantity had no effects on seed germination for R . javanica (Washitani and Takenaka 1986). Since the effects of low light intensity on seed germination rate for R . trichocarpa were weak under the larch canopy, seedling density could be high because of high seed colonization. In higher elevation, near-rock microhabitat showed the highest seedling density. Large rocks were distributed more at higher elevation, and density of larch decreased greatly. The large rocks are likely to be surrogate to larch trees at lower elevation for C. macrorhynchos, i.e., the crow used large rocks as perch. On Mount Koma, the range of daily temperature fluctuation on the ground surface was /108C on open site, including near-rock, at all elevations and occasionally exceeded 458C. Seed dormancy broken by temperature fluctuation has been known for numerous species (Baskin and Baskin 1998), and R . javanica showed high seed germination rate after heat treatment at /48oC (Washitani and Takenaka 1986). On open site including near-rock, soil temperature fluctuated greatly; therefore, near-rock could show the highest seedling density even though the seed supply was lower in higher elevation.
Seedling establishment pattern on R. trichocarpa The height-class distribution of R . trichocarpa seedlings indicated that seedling mortality was lower in higher elevation, and vice versa. Even though the number of seeds immigrated from seed source was lower in higher elevation, therefore, seedling density was the highest on near-rock in BG. Rhus trichocarpa establishes in the early stages of xeric succession (Tsujimura and Hara 1995), suggesting that one of the safe sites is open site. In LB where most seedlings established under the larch canopy, seedlings did not grow well and showed higher mortality, indicating that near-rock is the best safe site for R . trichocarpa and seedling regeneration is not expected under the larch canopy. In conclusion, mutual advantages between a crow C. macrorhynchos and R . trichocarpa were detected. The major determinants of the interaction were that: 1) aerial seedbank on R . trichocarpa , 2) behavioral characteristics of C. macrorhynchos, and 3) near-rock safe site for seedling establishment of R . trichocarpa . For the other plants producing bird-dispersed seeds, the mechanisms ECOGRAPHY 27:3 (2004)
of seed dispersal by birds were not clearly detected, due to low seedling density, except for the relationship between T. naumanni and G. miqueliana . However, weak relationships between bird-dispersal tree species and the other frugivorus bird species also imply that the relatively-strong interactions between C. macrorhynchos and R . trichocarpa .
Acknowledgements / Special thanks are due to J. H. Titus, M. Akasaka, S. Uesaka, A. Hase, H. Kimura, and all members in Regional Ecosystems Lab., GSEES, HU, for assistance in providing valuable ideas and cooperation. K. Nakanishi, Public Office of Mori Town, and Y. Iwaya, Forest Administration of Oshima Province, gave research permission. We thank T. Kohyama and G. Kudo for useful comments. Miyuki Nakajima gave us great peace of mind when we wrote this paper.
References Anon. 1963 /1994. ‘‘Maximun monthly wind direction on mori Climatological Observatory.’’ / Japan Meteorological Agency, Tokyo. Anon. 1999. Using StatView, 3rd ed. / SAS Inst., Cary. Anon. 2002a. PC-Ord. ver. 4.27. / MjM Software Design, Gleneden Beach. Anon. (ed). 2002b. Check-list of Japanese birds, 6th ed. / Ornithological Society of Japan, Obihiro. Baskin, C. C. and Baskin, J. M. 1998. Seeds: ecology, biogeography, and evolution of dormancy and germination. / Academic Press Bibby, C. J. et al. 2000. Bird census techniques, 2nd ed. / Academic Press. Brown, V. K. and Southwood, T. R. E. 1987. Secondary succession: patterns and strategies. / In: Gray, A. J., Crawley, M. J. and Edwards, P. J. (eds), Colonization, succession and stability. Blackwell Scientific Publ., pp. 315 /317. Debussche, M. and Isenmann, P. 1994. Bird-dispersed seed rain and seedling establishment in patchy Mediterranean vegetation. / Oikos 69: 414 /426. Frenzen, P. M. and Crisafulli, C. M. 1990. Mount St. Helens ten years later: past lessons and future promise. / Northwest Sci. 64: 263 /267. Fridriksson, S. and Magnusson, B. 1992. Development of the ecosystem on Surtsey with reference to Anak Krakatau. / GeoJournal 28: 287 /291. Fujimaki, Y. 1998. Distribution and abundance of carrion and jungle crow in central and south-eastern Hokkaido. / Strix 16: 47 /54, in Japanese with English summary. Guevara, S. and Laborde, J. 1993. Monitoring seed dispersal at isolated standing trees in tropical pastures: consequences for local species availability. / Vegetatio 107/108: 319 / 338. Haruki, M. and Tsuyuzaki, S. 2001. Woody plant establishment during the early stage of volcano succession on Mount Usu, northern Japan. / Ecol. Res. 16: 451 /457. Herrera, C. M. 1982. Seasonal variation in the quality of fruits and diffuse coevolution between plants and avian dispersers. / Ecology 63: 773 /785. Higuchi, H. 1979. Habitat segregation between the jungle and carrion crows, Corvus macrorhynchos and C. corone, in Japan. / Jpn. J. Ecol. 29: 353 /358. Higuchi, H. 1991. Long-distance seed dispersal by birds. / Study Spec. Biol. 15: 15 /18, in Japanese. Hino, T. 1993. Bird fauna and its distributions in Hokkaido. / In: Higashi, S., Osawa, A. and Kanagawa, K. (eds), ECOGRAPHY 27:3 (2004)
Biodiversity and ecology in the northernmost Japan. Hokkaido Univ. Press, pp. 89 /102. Howe, H. F. and Estabrook, G. F. 1977. On intraspecific competition for avian dispersers in tropical trees. / Am. Nat. 111: 817 /832. Howe, H. F. and Smallwood, J. 1982. Ecology of seed dispersal. / Annu. Rev. Ecol. Syst. 13: 201 /228. Howe, H. F. and Kerckhove, G. A. V. 1980. Nutmeg dispersal by tropical birds. / Science 210: 925 /927. Karasawa, K. 1978. Relationships between fruit-eating birds and seed dispersal in urbanized areas. / Tori 27: 1 /20, in Japanese with English summary. Kondo, T. and Tsuyuzaki, S. 1999. Natural regeneration patterns of the introduced larch, Larix kaempferi (Pinaceae), on the volcano Mount Koma, Northern Japan. / Diver. Distr. 5: 223 /233. Loiselle, B. A. and Blake, J. G. 1991. Temporal variation in birds and fruits along an elevational gradient in Costa Rica. / Ecology 72: 180 /193. Madge, S. and Burn, H. 2001. Crows and jays. / Princeton Univ. Press. Manuwal, D. A. et al. 1987. Summer birds on the upper subalpine zone of Mount Adams, Mount Rainier, and Mount St. Helens, Washington. / Northwest Sci. 61: 82 / 92. Maruta, E. 1983. Growth and survival of current-year seedlings of Polygonum cuspidatum at the upper distribution limit on Mt. Fuji. / Oecologia 60: 316 /320. McClanahan, T. R. and Wolfe, R. W. 1987. Dispersal of ornithochorous seeds from forest edges in central Florida. / Vegetatio 71: 107 /112. McDonnell, M. J. and Stiles, E. W. 1983. The structural complexity of old field vegetation and the recruitment of bird dispersed plant species. / Oecologia 56: 109 / 116. Nakashizuka, T. et al. 1993. Seed dispersal and vegetation development on a debris avalanche on the Ontake volcano, Central Japan. / J. Veg. Sci. 4: 537 /542. Partomihardjo, T., Mirmanto, E. and Whittaker, R. J. 1992. Anak Krakatau’s vegetation and flora circa 1991, with observation on a decade of development and change. / GeoJournal 28: 233 /248. Rathcke, B. and Lacey, E. P. 1985. Phenological patterns of terrestrial plants. / Annu. Rev. Ecol. Syst. 16: 179 /214. Shanahan, M. et al. 2001. Colonization of an island volcano, Long Island, Papua New Guinea, and an emergent island, Motmot, in its caldera lake. V. Colonization by figs (Ficus spp.), their dispersers and pollinators. / J. Biogeogr. 28: 1365 /1377. Silvertown, J. W. and Lovett Doust, J. L. 1993. Introduction to plant population biology. / Blackwell. Titus, J. H. and del Moral, R. 1998. Seedling establishment in different microhabitats on Mount St. Helens, Washington, USA. / Plant Ecol. 134: 13 /26. Tsujimura, A. and Hara, K. 1995. The pattern of species association in a successional forest on Mt. Bandai. / Ecol. Rev. Sendai 23: 101 /110. Tsuyuzaki, S. and del Moral, R. 1995. Species attributes in early primary succession. / J. Veg. Sci. 6: 517 /522. Tsuyuzaki, S. and Goto, M. 2001. Persistence of seedbank under thick volcanic deposits twenty years after eruptions of Mount Usu, Hokkaido Island, Japan. / Amer. J. Bot. 88: 1813 /1817. Ueda, K. 1992. Unexpected fancy of unexpected birds / Who eats inconspicuous dry-fruits? / Biological Sci., Tokyo 44: 81 /88, in Japanese. Uesaka, S. and Tsuyuzaki, S. (in press). Differential establishment and survival of species in deciduous and evergreen shrub patches and on bare ground, Mt. Koma, Hokkaido, Japan. / Plant Ecol. Vernon, W. P. 1968. Long-distance dispersal of seeds by retention digestive tract of birds. / Science 160: 321 /322.
321
Washitani, I. and Takenaka, A. 1986. Safe sites’ for the seed germination of Rhus javanica : a characterization by response to temperature and light. / Ecol. Res. 1: 71 / 82. Yoshii, Y. 1932. Revegetation of volcano Komagatake after the great eruption in 1929. / Bot. Mag. Tokyo 46: 208 /216.
322
Yura, H. 1988. Comparative ecophysiology of Larix kaempferi (Lamb.) Carr. and Abies veitchii Lindl. 1. Seedling establishment on bare ground on Mt. Fuji. / Ecol. Res. 3: 67 /73. Zann, R. A. and Darjono 1992. The birds of Anak Krakatau: the assembly of an avian community. / GeoJournal 28: 261 /270.
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