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Collembolan community dynamics during deciduous forests regeneration in Japan
ARTICLE IN PRESS Pedobiologia 50 (2006) 117—126
www.elsevier.de/pedobi
PROCEEDINGS OF THE XITH INTERNATIONAL COLLOQUIUM ON APTERYGOTA, ROUEN, FRANCE, 2004
Collembolan community dynamics during deciduous forests regeneration in Japan Motohiro Hasegawa, Kenji Fukuyama, Shun’ichi Makino, Isamu Okochi, Hideaki Goto, Takeo Mizoguchi, Tadashi Sakata, Hiroshi Tanaka Kiso Experimental Station, Forestry and Forest Products Research Institute, 5473 Kisofukushima, Kisogun, Nagano 397-0001, Japan Received 10 May 2005; accepted 2 December 2005
KEYWORDS Collembola; Secondary succession; Feeding group; Soil environment; Vegetation structure
Summary The structure and feeding group composition of collembolan communities were studied in secondary deciduous forests of different ages to investigate the collembolan community response to environmental changes associated with forest cycles. The study was carried out at eight sites forming a chronosequence (1, 4, 12, 24, 51, 54, 71 and 128 years after clear cutting) of deciduous forest stands in northern Ibaraki (Japan). Total collembolan density and species richness was low at the 1-year-old site, and there was little difference in density among sites over 4 years of age. The density of sucking feeders was especially low at the 1-year-old site. Species richness of trees of a diameter at breast height (DBH)o5 cm positively correlated with the density of fungal feeders. Species richness of total Collembolans and of sucking feeders correlated positively with the water content of the organic layer. Ordination of the collembolan community with Canonical Correspondence Analysis suggested that species richness of larger trees (DBH X 5 cm) contributed to the differences in species composition of fungal feeders and sucking feeders. We conclude that total abundance and species richness of collembolans recovered within 4 years after clear-cutting, but species composition of fungal feeders and sucking feeders took longer to recover. & 2006 Elsevier GmbH. All rights reserved.
Introduction Changes in the structure of soil animal communities during the succession of forest have been Corresponding author. Fax: +81 264 22 2542.
E-mail address: [email protected] (M. Hasegawa).
studied in several taxa from the viewpoint of the conservation of biodiversity or ecosystem functions (Fukuyama and Ito 1992; Scheu and Schulz 1996; Horwood and Butt 2000; Yeates et al. 2000; Rusek 2001; Zaitsev et al. 2002). Research on sites of serial stands (‘chronosequences’) offers the opportunity to examine long-term changes in forest
0031-4056/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2005.12.003
ARTICLE IN PRESS 118 succession. Collembolans are one of the dominant groups of the soil fauna (Petersen and Luxton 1982), and may have a significant function in decomposition and nutrient cycling in forest ecosystems (Verhoef and Brussaard 1990; Filser 1995). Collembolan communities are structured by a number of factors, such as soil fertility (Ha( gvar 1982), humus type (Cassagne et al. 2003), water content (Verhoef 1981) and biological factors (Addison et al. 2003b; Ha( gvar 1982). These soil and plant factors have been related with the community structure of soil arthropods to explain their successional changes (Zaitsev et al. 2002; Chauvat et al. 2003). The mass and water content of the forest floor have often been cited as important determinants in collembolan community structure (Takeda 1987). In addition, pH, EC and organic matter of the top soil have been related with invertebrate communities (Ha( gvar 1982; Zaitsev et al. 2002). Changes in plant communities structures were also the main cause of the differences in soil arthropods (Ha( gvar 1982; Rusek 2001). The activity of microorganisms in the sites might influence the collembolan communities. Soil respiration could be an index for the activity microorganisms. Zaitsev et al. (2002) and Chauvat et al. (2003) tried to relate changes in arthropods with CO2 emission of forest floor. Feeding habits of collembola are different between species. Some collembolan species grazed fungi directly and responded to the fungal condition and some species recycled the humus materials (Hasegawa and Takeda 1995). The condition of microorganisms or humus materials may change in relation to changes in plant communities (Scheu 1990; Cassagne et al. 2003). Thus it is useful to relate changes in feeding groups with environmental changes, in order to explain successional changes in microarthropods (Zaitsev et al. 2002; Addison et al. 2003b; Chauvat et al. 2003). In previous studies, successional changes in collembolan communities were studied mainly in coniferous forests (Seta ¨la ¨ and Marshall 1994; Shaw and Usher 1996; Addison et al. 2003a,b; Chauvat et al. 2003). The present study, however, was conducted in a chronosequence of deciduous broad-leaved forests, in which the changing pattern of the collembolan community is expected to differ from that of a coniferous forest chronosequence. The aims of this study were to determine: (1) how the collembolan community responds to environmental changes (soil environment, soil respiration and vegetation structure) associated with successional changes of deciduous broadleaved forests and (2) whether different feeding groups of collembolans show different responses.
M. Hasegawa et al. Table 1.
Size and type of the forest studied
Age
Size (ha)
Type of forest
1
5
4 12 24 51 54 71 128
2.5 4 8 10 15 19 100
Cutover land just after clearcutting Shrub forest Young secondary forest Young secondary forest Old secondary forest Old secondary forest Old secondary forest Old natural (perhaps) forest
Age refers to years after clear-cutting. No records of clear-cut
Materials and methods Study site The study area (Ogawa) is located at the southern edge of the Abukuma Mountains, in northern Ibaraki, central Japan (approximately 361560 N, 1401350 E, 580–800 m a.s.l.). The mean annual air temperature is 10.7 1C, and the mean annual precipitation is approximately 1900 mm. This area includes natural deciduous forests and planted forests of two conifer species, Cryptomeria japonica and Chamaecypress obtusa. In this study, only deciduous forests were investigated. Some parts of the forests in this area have been subjected to human activities such as burning, cattle grazing and clear-cutting for fuel wood (Nakashizuka and Matsumoto 2002). In the deciduous forests the dominant large trees are Quercus serrata, Quercus mongolica and Fagus crenata (Table 1) (for further information, see Inoue 2003). A chronosequence containing eight stands of different ages after clear-cutting was investigated (1, 4, 12, 24, 51, 54, 71 and X 128 years). All eight stands were located within a 4 6 km area.
Sampling of collembolans Forest floor was sampled, in April, August and November 2002. At each site, an 8 8 m plot was set up and divided into eight subplots (2 4 m). Forest floor was collected by a soil core (125 ml, 5 cm depth, 25 cm2 area) from each subplot. The depth of the soil core was enough to collect most collembolans in the study sites, because litter layers of the study sites were very thin (1–2 cm), and most collembolans occurred in the litter layer and the upper mineral soil layer. A total of 192 samples (8 sites 8 subplots 3 dates) were
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests collected. Density and species richness of total collembolans at each site on each date were obtained from eight samples. Collembolans were extracted with Tullgren funnels at a constant temperature of 35 1C for 72 h. Feeding groups for collembolan species were identified by the analysis of gut contents, following Takeda and Ichimura (1983) and Hasegawa and Takeda (1995). Species were grouped into ‘‘fungal feeder’’ which selectively feed on fungal hyphae or spores, ‘‘detritus feeder’’ which feed on humus and fungal material, and ‘‘sucking feeder’’ which possess sucker-type mouthparts and have fluid gut contents.
Soil chemistry and respiration analysis Samples for chemical parameters and respiration analyses were taken in July 2003. In each site forest floor was collected from five plots of a 25 25 cm area, weighed, air-dried at 40 1C for 72 h, and reweighed in order to determine forest floor mass. The standard errors of five replicates were 8–15% of average values, indicating that this method was adequate to evaluate the weight of forest floor. Although it might be ideal to take forest floor samples for pH, electric conductivity (EC) and soil respiration analysis as in the sample of collembolans, these soil parameters in forest floor were often very unstable and seemed not to reflect to successional changes in sites. Therefore, we estimated these parameters for the top soil as parameters which indirectly reflect the conditions in forest floor. After removing the organic layer, a core of 100 ml of the top 5 cm of soil was collected from each of the five plots for soil chemical analysis. For soil pH and EC analysis, 5 g of fresh soil was immersed and mixed in 25 ml of 0.1 M KCl solution (for pH) or deionized water (for EC). Soil pH was measured with a glass electrode (HM14P, DKK-Toa Corp., Tokyo, Japan) and soil EC was measured with a conductivity cell electrode (SC82, Yokogawa Electric Corp., Tokyo, Japan). Soil organic matter was determined by mass loss on ignition after burning in an electric furnace (1000 1C, for 1 h). Soil samples for soil respiration measurements were collected from 0 to 4 cm depth of surface soil using a 400 ml cylindrical sampler with five replicates at each site. The samples were sieved through 2 mm mesh to remove roots and coarse organic particles. Samples of about 40 g were then pre-incubated in sealed, 650 ml containers at 15 1C for 2 days. After pre-incubation the CO2 concentrations in the container were measured at 0, 2.5 and
119 5 h at 15 1C using an infrared gas analyzer (ZFP9, Fuji Electric Co., Japan).
Forest characteristics We established a line transect (10 100 m) at each site from September 2000 to October 2003. All trees and vines of at least 2 m in height and at least 5 cm in diameter at breast height (DBH) were counted and their DBH was measured in forty 5 5 m quadrats along a 100 m line. The frequency of trees smaller than 5 cm in DBH in the 40 quadrates was also determined. Forest floor vegetation with a height of less than 2 m (forest floor plants) was estimated following the Braun–Blanquet method for 1 1 m in 5 5 m quadrat.
Statistical analysis We examined differences in the abundance and species diversity of collembolans among the eight stands for each of three dates (April, August and November) with ANOVA using SYSTAT 5.2.1 for Mac (SYSTAT INC., Evanston, USA). Because replicated samplings were only made from subplots of a single site, they were ‘pseudoreplicated’ with respect to stand age (Hurlbert 1984). However, we believe that individual sites represented different age classes of forests since the sites were relatively close to each other thereby avoiding differences caused by geographic and climatic variations. Tukey’s minimum significant difference test was used for comparisons of means. Before statistical tests, population data were transformed using logarithmic transformation, log10 ðx þ 1Þ. Spearman rank correlation coefficients between collembolan abundance or community index and environmental variables were calculated using SYSTAT 5.2.1 for Mac (SYSTAT INC., Evanston, USA). Canonical correspondence analysis (CCA) was performed with Canoco for Windows, Version 4.5 (ter Braak and Smilauer 2002). Here, it was used to relate environmental variables in each site to the species composition of collembolans. In CCA, only those species with a total count of at least three individuals were used. Population data were transformed using logarithmic transformation, log10 ðx þ 1Þ. Environmental variables were tested using forward selection of variables with Monte Carlo test using 499 unrestricted permutations (Po0.05). In order to investigate the effects of plant community species composition on the collembolan community, Spearman rank correlation coefficients between the scores of the first axis of the collembolan
ARTICLE IN PRESS 120 group ordination and that of the plant community group ordination were calculated. The plant community was divided into three groups, i.e., trees with DBH X 5 cm, trees with DBHo5 cm and forest floor plants. For the ordination, Detrended Correspondence Analysis (DCA) was performed with Canoco for Windows, Version 4.5 (ter Braak and Smilauer 2002). In DCA of trees with DBH X 5 cm the 1-year-old site and the 4-year-old site were excluded because there were no trees of these size classes. Likewise, in the DCA of forest floor plants, the 1-year-old site was excluded. In DCA, species with at least three individuals in total were used, and population data were transformed using logarithmic transformation, log10(x+1).
Results Density and species richness of collembolans The densities of collembolans ranged from 12,000 to 53,000 ind m2 (Fig. 1). They were slightly lower at the 1-year-old site than those at the other sites on all dates. In August the density at the 1-year-old site was significantly lower than that at the 4, 12 and 24-year-old site. A total of 87 collembolan species was found. Species richness was also slightly lower at the 1-year-old site than that at the other sites (Fig. 2). In August and November, average species richness was significantly lower at the 1-year-old site than that at most of the other sites. Detritus feeders were dominant both in density and species richness (70–87% in density and 47–57% in species richness) while sucking feeders had the lowest values (Fig. 3). The density and species richness of detritus feeders at the 1-year-old site tended to be lower than the other sites. The density of fungal feeders at the 1-year-old site also tended to be lower than that at the other sites. It increased at the 4-year-old site but gradually decreased after 4 years. Species richness of fungal feeders was similar at all sites. Sucking feeders tended to have a very low density and species richness at the 1-year-old site. Significant differences of density and species richness for these feeding groups were found between the 1-year-old site and some sites in August and November.
Correlation between collembolans and environmental variables Since seasonal changes in collembolan community structure were small, data on collembolan
M. Hasegawa et al. communities of the three sampling dates were pooled. The pooled data were used for Spearman rank correlation, DCA and CCA to relate them to environmental variables. Most of the variables of plant community did not significantly correlate with indices of collembolan community. Significantly positive correlation was only found between species richness of trees with DBHo5 cm and fungal feeder density (r s ¼ 0:755, Po0.05). In the variables of soil environments (Table 2), water content positively correlated with total species richness (r s ¼ 0:756, Po0.05) and sucking feeder species richness (r s ¼ 0:723, Po0.05), and forest floor mass negatively correlated with fungal feeder density (rs ¼ 0:731, Po0.05). The CCA analysis of detritus feeders selected no environmental variables in the forward selection process, and then detritus feeders were excluded from further analysis. Eigenvalues of the first two axes and their cumulative percentage in CCA were respectively as follows for total collembolans, 0.12%, 0.14% and 43.9%, fungal feeders, 0.20%, 0.20% and 55.9%, and sucking feeders, 0.42%, 0.30% and 53.6%. The eigenvalues and cumulative percentage variance showed that sucking and fungal feeders were relatively well classified, while total collembolans were not. In these three analyses, species richness of trees with DBH X 5 cm was selected as a factor related to the species composition of collembolans. In the analysis for sucking feeders, the forest age was also selected as a significant factor (Fig. 4a–c). Scores of the first axis of sucking feeders in the DCA ordination significantly (Po0.05) correlated with those of trees with DBH X 5 cm (r s ¼ 0:886).
Discussion The density and species richness of total collembolans was low at the 1-year-old site as compared with those at the older sites but not always significantly and not at all sampling times. A decrease in the density of microarthropods after clear-cutting has been reported by some studies (Vlug and Borden 1973; Seastedt and Crossley 1981; Bird and Chatarpaul 1986). The removal of canopy leads to harsh environmental conditions on the forest floor (Abbott et al. 1980). Abbott et al. (1980) showed that clearcutting caused a reduction in oribatid mite density and suggested that the reduction was due to changes in the temperature and humidity of the forest floor rather than to food availability in the litter. Our study also showed that the water content of forest floor organic matter at the 1-year-old site was lower than
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests
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70000 Apr. '02
10000
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a
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ab
10000
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Nov. '02
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1000 1
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Age
Fig. 1. Density of total collembolans of forest sites of different age after clear-cutting. Bars indicate standard errors; different letters indicate significant differences at Po0.05.
ARTICLE IN PRESS 122
M. Hasegawa et al. Average species richness per core
50
Total species richness
Apr. '02
40
30
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0 50
Aug. '02
Species richness
40
30 c bc
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a 10
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Age
Fig. 2. Species richness of total collembolans of forest sites of different age after clear-cutting. Bars indicate standard errors; different letters indicate significant differences at Po0.05.
that at the other sites (Table 2). This may be a cause of the low abundance of collembolan fauna at the youngest site.
The density and species richness of collembolans at the 4-year-old site suggested that collembolans recover quickly after clear-cutting (Fig. 1). In
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests
123 Detritus feeders
(a)
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Average density per core
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Species richness
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Fig. 3. Density (a) and species richness (b) of feeding groups of collembolans of forest sites of different age after clearcutting. For density (a), averages of data on three sampling dates are given. For species richness (b), totals of data on three sampling dates are given.
comparison with previous studies conducted in Canadian and European coniferous forests (Addison et al. 2003a,b; Zaitsev et al. 2002; Chauvat et al. 2003), this study showed a faster recovery of collembolan community in terms of total density and species richness. This might be attributed to the faster recovery in deciduous plant communities. In our study area shrub or small tree species, such as Rubus spp. or Salix spp., immediately invaded after clear-cutting and some tree species (for example, Quercus serrata) regenerated from
stumps by sprouting. Development of these young secondary forests might soon ameliorate the high temperature and/or low moisture environments that are experienced after clear-cutting. Total collembolan density did not significantly correlate with any soil environmental variables, but the density of fungal feeders negatively correlated with forest floor mass. In contrast, in previous studies positive correlations were observed between forest floor mass and density of collembolans were found (Petersen and Luxton 1982; Takeda
ARTICLE IN PRESS 124
M. Hasegawa et al.
Table 2. Forest floor mass and gravimetric water content, soil respiration in the top 4 cm soil, pH (KCl), EC and organic matter (loss on ignition) in the top 5 cm mineral soil of the forest studied Age
Forest floor mass (g m2)
Forest floor water Soil respiration content (%) (mg CO2 m2 s1)
pH (KCl) (1:5)
EC (dS m1)
Organic matter (%)
1 4 12 24 51 54 71 128
514 394 407 471 657 597 633 669
63 242 192 171 246 232 123 211
3.5 3.6 3.8 4.3 3.6 3.5 3.5 4.0
2.8 2.8 1.2 1.4 1.6 2.4 1.8 1.0
52.8 30.4 31.5 42.1 29.6 34.9 28.1 26.8
16.1 20.1 16.2 17.3 18.6 22.1 15.6 25.6
1987). In the present study, differences in the forest floor mass were relatively small (Table 2), and might not reflect the habitat and food availability for collembolans. Species richness of trees with DBHo5 cm positively correlated with that of fungal feeding collembolans suggesting that small tree species dominant in early successional stages of deciduous broad-leaved forests might be favoured by fungal feeders. The litter of such tree species tends to decompose faster than late successional tree species due to its relatively high nitrogen concentration and low lignin content (Osono and Takeda 2005a,b). Possibly, fungal feeders were abundant at the sites with little forest floor due to high fungal activity in early successional tree species litter (Takeda 1987). Forest floor water content did not correlate with species richness of either detritus feeders or fungal feeders, but it positively correlated with species richness of total collembolans and of sucking feeders. Sucking feeders take up organic matter or bacteria through water in the soil (Singh 1969; Adams and Salmon 1972). Therefore, low water content might limit their diversity. Detritus feeders were the most dominant group in this study, and did not show any significant correlation with soil and plant variables. Compared with the other groups, detritus feeders are food and habitat generalists rather than specialists and this may explain their weak response to changes in the plant community structure. Plant species richness did not correlate with species richness of collembolans. The effect of plant species richness of forests on soil microarthropods has been investigated using litterbags with single and mixed species litter (Kaneko and Salamanca 1999; Hansen and Coleman 1998). Kaneko and Salamanca (1999) suggested that microarthropod abundance and oribatid mite diversity were higher in mixed (2 or 3 species)
litter than in single species litter. Hansen and Coleman (1998) also suggested that oribatid mite species richness in mixed litter is significantly higher than that in the single species litter, but they found no differences in oribatid diversity between the mixed litter of three and seven species. Relationships between plant species richness and soil arthropod performance also have been investigated in grassland ecosystems (Koricheva et al. 2000; Hedlund et al. 2003). In an experiment conducted in plots with varying numbers (4–15) of plant species, Hedlund et al. (2003) showed that the numbers of collembolan and mites were not influenced by plant biomass production or plant species numbers. Likewise, Salamon et al. (2004) failed to find any correlation between species richness or functional group of plant and total diversity of collembolans in their experiment conducted in a series of plots with up to 32 plant species in a grassland community. These results indicate that the number of plant species influences the density and/or diversity of soil microarthropods only in simple systems with low numbers of plant species as investigated by Kaneko and Salamanca (1999). The effect of plant species richness on arthropod diversity disappears or becomes redundant in ecosystems with larger numbers of plant species as also found in the present study. In contrast to the diversity of collembolans, plant community structures correlated with the collembolan species composition. In CCA analysis for total collembolans, fungal feeders and sucking feeders, the species richness of trees with DBH X 5 cm was related to the species composition of collembolans (Fig. 4). DCA scores of sucking feeders significantly correlated with the scores of DCA in trees with DBH X 5 cm. These results suggest that the species compositions of some collembolan feeding groups are associated with the diversity or species
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests (a)
1.0 1
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128 Species richness (DBH 5cm)
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-0.6 -1.5 (b)
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Cer sp.1
Acknowledgements
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Cer den 54 24
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Species richness (DBH 5cm)
Pter
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Species richness (DBH 5cm) 71
Forest age
24 Pseud 3 54 12
forests recovered from clear-cutting faster than those reported in coniferous forests in Canada and Europe. This might be attributed to fast recovery of the deciduous forest plants in an early phase of secondary succession than of conifers. Species composition of detritus feeders (dominating the collembolan community) showed a weak response to soil and plant variables. In contrast, the species composition of fungal feeders and sucking feeders was more closely associated with the changes in plant communities, and took longer to recover. If collembolans are to be used as biological indicators for forest management, it is recommended to investigate not only total density and species richness but also community structure and functional composition.
128 51 Tomo
Hyp
125
We would like to thank the staff of the Insect Ecology Laboratory and the Kiso Experimental Station at the Forestry and Forest Products Research Institute for their help and guidance in the field research and laboratory analysis. Also, we thank Mrs. S. Sebayashi for her help in sorting the soil fauna. This study was supported by research grant #200004 of the Forestry and Forest Products Research Institute.
Supero 3 51
Frie
References
Pseud 4 128
-0.6 -0.4
Supero1 1 4
1.0
Fig. 4. CCA ordination plots for total collembolans (a), fungal feeders (b) and sucking feeders (c). Diamonds show the positions of communities with forest age indicated by numerals. Crosses show the positions of the main species. Significant environmental variables are shown by arrows. Cer sp.1; Ceratophysella sp.1, Hyp; Hypogastrura sp.1, Pter; Pteronychella spatiosa Uchida and Tamura, 1968, Cer den; Ceratophysella denisana (Yosii, 1956), Tomo; Tomocerus varius Folsom, 1899, Frie; Friesea japonica Yosii, 1954, Pseud 4; Pseudachorhutes sp.4, Supero 3; Superodontella sp.3, Pseud 3; Pseudachorhutes sp.3, Supero 1; Superodontella sp.1.
composition of large trees, though the mechanisms underlying the association is unknown. In conclusion, this study showed that abundance and species richness of Collembolans in deciduous
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M. Hasegawa et al. Petersen, H., Luxton, M., 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 288–388. Rusek, J., 2001. Microhabitats of Collembola (Insecta: Entognatha) in beech and spruce forests and their influence on biodiversity. Eur. J. Soil Biol. 37, 237–244. Salamon, J.A., Schaefer, M., Alphei, J., Schmid, B., Scheu, S., 2004. Effects of plant diversity on Collembola in an experimental grassland ecosystem. Oikos 106, 51–60. Scheu, S., 1990. Changes in microbial nutrient status during secondary succession and its modification by earthworms. Oecologia 84, 351–358. Scheu, S., Schulz, E., 1996. Secondary succession, soil formation and development of a diverse community of oribatida and saprophagous soil macro-invertebrates. Biodiv. Cons. 5, 235–250. Seastedt, T.R., Crossley Jr., D.A., 1981. Microarthropod response following cable logging and clear-cutting in the Southern Apparachians. Ecology 62, 126–135. Seta ¨la ¨, H., Marshall, V.G., 1994. Stumps as a habitat for Collembola during succession from clear-cuts to oldgrowth Douglas-fir forests. Pedobiologia 38, 307–326. Shaw, P.J.A., Usher, M.B., 1996. Edaphic Collembola of Lodgepole pine Pinus contorta plantation in Cumbria, UK. Eur. J. Soil Biol. 32, 89–97. Singh, S.B., 1969. Preliminary observations on the food preference of certain Collembola (Insecta). Rev. Ecol. Biol. Sol 4, 461–467. Takeda, H., 1987. Dynamics and maintenance of collembolan community structure in a forest soil ecosystem. Res. Popul. Ecol. 29, 291–346. Takeda, H., Ichimura, T., 1983. Feeding attributes of four species of Collembola in a pine forest soil. Pedobiologia 25, 373–381. ter Braak, C. J. F., Smilauer, P., 2002. CANOCO Reference Manual and Canodraw for Windows User’s Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, USA. Verhoef, H.A., 1981. Water balance in Collembola and its relation to habitat selection; water content, haemolymph osmotic pressure and transpiration during an instar. J. Insect Physiol. 27, 755–760. Verhoef, H., Brussaard, L., 1990. Decomposition and nitrogen mineralization in natural and agro-ecosystems: the contribution of soil animals. Biogeochemistry 11, 175–211. Vlug, H., Borden, J.H., 1973. Soil Acari and Collembola Populations affected by logging and slash burning in a coastal British Columbia Coniferous forest. Environ. Entomol. 2, 1016–1023. Yeates, G.W., Hawke, M.F., Rijkse, W.C., 2000. Changes in soil fauna and soil conditions under Pinus radiata agroforestry regimes during a 25-year tree rotation. Biol. Fertil. Soils 31, 391–406. Zaitsev, A.S., Chauvat, M., Pflug, A., Wolters, V., 2002. Oribatid mite diversity and community dynamics in a spruce chronosequence. Soil Biol. Biochem. 34, 1919–1927.
www.elsevier.de/pedobi
PROCEEDINGS OF THE XITH INTERNATIONAL COLLOQUIUM ON APTERYGOTA, ROUEN, FRANCE, 2004
Collembolan community dynamics during deciduous forests regeneration in Japan Motohiro Hasegawa, Kenji Fukuyama, Shun’ichi Makino, Isamu Okochi, Hideaki Goto, Takeo Mizoguchi, Tadashi Sakata, Hiroshi Tanaka Kiso Experimental Station, Forestry and Forest Products Research Institute, 5473 Kisofukushima, Kisogun, Nagano 397-0001, Japan Received 10 May 2005; accepted 2 December 2005
KEYWORDS Collembola; Secondary succession; Feeding group; Soil environment; Vegetation structure
Summary The structure and feeding group composition of collembolan communities were studied in secondary deciduous forests of different ages to investigate the collembolan community response to environmental changes associated with forest cycles. The study was carried out at eight sites forming a chronosequence (1, 4, 12, 24, 51, 54, 71 and 128 years after clear cutting) of deciduous forest stands in northern Ibaraki (Japan). Total collembolan density and species richness was low at the 1-year-old site, and there was little difference in density among sites over 4 years of age. The density of sucking feeders was especially low at the 1-year-old site. Species richness of trees of a diameter at breast height (DBH)o5 cm positively correlated with the density of fungal feeders. Species richness of total Collembolans and of sucking feeders correlated positively with the water content of the organic layer. Ordination of the collembolan community with Canonical Correspondence Analysis suggested that species richness of larger trees (DBH X 5 cm) contributed to the differences in species composition of fungal feeders and sucking feeders. We conclude that total abundance and species richness of collembolans recovered within 4 years after clear-cutting, but species composition of fungal feeders and sucking feeders took longer to recover. & 2006 Elsevier GmbH. All rights reserved.
Introduction Changes in the structure of soil animal communities during the succession of forest have been Corresponding author. Fax: +81 264 22 2542.
E-mail address: [email protected] (M. Hasegawa).
studied in several taxa from the viewpoint of the conservation of biodiversity or ecosystem functions (Fukuyama and Ito 1992; Scheu and Schulz 1996; Horwood and Butt 2000; Yeates et al. 2000; Rusek 2001; Zaitsev et al. 2002). Research on sites of serial stands (‘chronosequences’) offers the opportunity to examine long-term changes in forest
0031-4056/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2005.12.003
ARTICLE IN PRESS 118 succession. Collembolans are one of the dominant groups of the soil fauna (Petersen and Luxton 1982), and may have a significant function in decomposition and nutrient cycling in forest ecosystems (Verhoef and Brussaard 1990; Filser 1995). Collembolan communities are structured by a number of factors, such as soil fertility (Ha( gvar 1982), humus type (Cassagne et al. 2003), water content (Verhoef 1981) and biological factors (Addison et al. 2003b; Ha( gvar 1982). These soil and plant factors have been related with the community structure of soil arthropods to explain their successional changes (Zaitsev et al. 2002; Chauvat et al. 2003). The mass and water content of the forest floor have often been cited as important determinants in collembolan community structure (Takeda 1987). In addition, pH, EC and organic matter of the top soil have been related with invertebrate communities (Ha( gvar 1982; Zaitsev et al. 2002). Changes in plant communities structures were also the main cause of the differences in soil arthropods (Ha( gvar 1982; Rusek 2001). The activity of microorganisms in the sites might influence the collembolan communities. Soil respiration could be an index for the activity microorganisms. Zaitsev et al. (2002) and Chauvat et al. (2003) tried to relate changes in arthropods with CO2 emission of forest floor. Feeding habits of collembola are different between species. Some collembolan species grazed fungi directly and responded to the fungal condition and some species recycled the humus materials (Hasegawa and Takeda 1995). The condition of microorganisms or humus materials may change in relation to changes in plant communities (Scheu 1990; Cassagne et al. 2003). Thus it is useful to relate changes in feeding groups with environmental changes, in order to explain successional changes in microarthropods (Zaitsev et al. 2002; Addison et al. 2003b; Chauvat et al. 2003). In previous studies, successional changes in collembolan communities were studied mainly in coniferous forests (Seta ¨la ¨ and Marshall 1994; Shaw and Usher 1996; Addison et al. 2003a,b; Chauvat et al. 2003). The present study, however, was conducted in a chronosequence of deciduous broad-leaved forests, in which the changing pattern of the collembolan community is expected to differ from that of a coniferous forest chronosequence. The aims of this study were to determine: (1) how the collembolan community responds to environmental changes (soil environment, soil respiration and vegetation structure) associated with successional changes of deciduous broadleaved forests and (2) whether different feeding groups of collembolans show different responses.
M. Hasegawa et al. Table 1.
Size and type of the forest studied
Age
Size (ha)
Type of forest
1
5
4 12 24 51 54 71 128
2.5 4 8 10 15 19 100
Cutover land just after clearcutting Shrub forest Young secondary forest Young secondary forest Old secondary forest Old secondary forest Old secondary forest Old natural (perhaps) forest
Age refers to years after clear-cutting. No records of clear-cut
Materials and methods Study site The study area (Ogawa) is located at the southern edge of the Abukuma Mountains, in northern Ibaraki, central Japan (approximately 361560 N, 1401350 E, 580–800 m a.s.l.). The mean annual air temperature is 10.7 1C, and the mean annual precipitation is approximately 1900 mm. This area includes natural deciduous forests and planted forests of two conifer species, Cryptomeria japonica and Chamaecypress obtusa. In this study, only deciduous forests were investigated. Some parts of the forests in this area have been subjected to human activities such as burning, cattle grazing and clear-cutting for fuel wood (Nakashizuka and Matsumoto 2002). In the deciduous forests the dominant large trees are Quercus serrata, Quercus mongolica and Fagus crenata (Table 1) (for further information, see Inoue 2003). A chronosequence containing eight stands of different ages after clear-cutting was investigated (1, 4, 12, 24, 51, 54, 71 and X 128 years). All eight stands were located within a 4 6 km area.
Sampling of collembolans Forest floor was sampled, in April, August and November 2002. At each site, an 8 8 m plot was set up and divided into eight subplots (2 4 m). Forest floor was collected by a soil core (125 ml, 5 cm depth, 25 cm2 area) from each subplot. The depth of the soil core was enough to collect most collembolans in the study sites, because litter layers of the study sites were very thin (1–2 cm), and most collembolans occurred in the litter layer and the upper mineral soil layer. A total of 192 samples (8 sites 8 subplots 3 dates) were
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests collected. Density and species richness of total collembolans at each site on each date were obtained from eight samples. Collembolans were extracted with Tullgren funnels at a constant temperature of 35 1C for 72 h. Feeding groups for collembolan species were identified by the analysis of gut contents, following Takeda and Ichimura (1983) and Hasegawa and Takeda (1995). Species were grouped into ‘‘fungal feeder’’ which selectively feed on fungal hyphae or spores, ‘‘detritus feeder’’ which feed on humus and fungal material, and ‘‘sucking feeder’’ which possess sucker-type mouthparts and have fluid gut contents.
Soil chemistry and respiration analysis Samples for chemical parameters and respiration analyses were taken in July 2003. In each site forest floor was collected from five plots of a 25 25 cm area, weighed, air-dried at 40 1C for 72 h, and reweighed in order to determine forest floor mass. The standard errors of five replicates were 8–15% of average values, indicating that this method was adequate to evaluate the weight of forest floor. Although it might be ideal to take forest floor samples for pH, electric conductivity (EC) and soil respiration analysis as in the sample of collembolans, these soil parameters in forest floor were often very unstable and seemed not to reflect to successional changes in sites. Therefore, we estimated these parameters for the top soil as parameters which indirectly reflect the conditions in forest floor. After removing the organic layer, a core of 100 ml of the top 5 cm of soil was collected from each of the five plots for soil chemical analysis. For soil pH and EC analysis, 5 g of fresh soil was immersed and mixed in 25 ml of 0.1 M KCl solution (for pH) or deionized water (for EC). Soil pH was measured with a glass electrode (HM14P, DKK-Toa Corp., Tokyo, Japan) and soil EC was measured with a conductivity cell electrode (SC82, Yokogawa Electric Corp., Tokyo, Japan). Soil organic matter was determined by mass loss on ignition after burning in an electric furnace (1000 1C, for 1 h). Soil samples for soil respiration measurements were collected from 0 to 4 cm depth of surface soil using a 400 ml cylindrical sampler with five replicates at each site. The samples were sieved through 2 mm mesh to remove roots and coarse organic particles. Samples of about 40 g were then pre-incubated in sealed, 650 ml containers at 15 1C for 2 days. After pre-incubation the CO2 concentrations in the container were measured at 0, 2.5 and
119 5 h at 15 1C using an infrared gas analyzer (ZFP9, Fuji Electric Co., Japan).
Forest characteristics We established a line transect (10 100 m) at each site from September 2000 to October 2003. All trees and vines of at least 2 m in height and at least 5 cm in diameter at breast height (DBH) were counted and their DBH was measured in forty 5 5 m quadrats along a 100 m line. The frequency of trees smaller than 5 cm in DBH in the 40 quadrates was also determined. Forest floor vegetation with a height of less than 2 m (forest floor plants) was estimated following the Braun–Blanquet method for 1 1 m in 5 5 m quadrat.
Statistical analysis We examined differences in the abundance and species diversity of collembolans among the eight stands for each of three dates (April, August and November) with ANOVA using SYSTAT 5.2.1 for Mac (SYSTAT INC., Evanston, USA). Because replicated samplings were only made from subplots of a single site, they were ‘pseudoreplicated’ with respect to stand age (Hurlbert 1984). However, we believe that individual sites represented different age classes of forests since the sites were relatively close to each other thereby avoiding differences caused by geographic and climatic variations. Tukey’s minimum significant difference test was used for comparisons of means. Before statistical tests, population data were transformed using logarithmic transformation, log10 ðx þ 1Þ. Spearman rank correlation coefficients between collembolan abundance or community index and environmental variables were calculated using SYSTAT 5.2.1 for Mac (SYSTAT INC., Evanston, USA). Canonical correspondence analysis (CCA) was performed with Canoco for Windows, Version 4.5 (ter Braak and Smilauer 2002). Here, it was used to relate environmental variables in each site to the species composition of collembolans. In CCA, only those species with a total count of at least three individuals were used. Population data were transformed using logarithmic transformation, log10 ðx þ 1Þ. Environmental variables were tested using forward selection of variables with Monte Carlo test using 499 unrestricted permutations (Po0.05). In order to investigate the effects of plant community species composition on the collembolan community, Spearman rank correlation coefficients between the scores of the first axis of the collembolan
ARTICLE IN PRESS 120 group ordination and that of the plant community group ordination were calculated. The plant community was divided into three groups, i.e., trees with DBH X 5 cm, trees with DBHo5 cm and forest floor plants. For the ordination, Detrended Correspondence Analysis (DCA) was performed with Canoco for Windows, Version 4.5 (ter Braak and Smilauer 2002). In DCA of trees with DBH X 5 cm the 1-year-old site and the 4-year-old site were excluded because there were no trees of these size classes. Likewise, in the DCA of forest floor plants, the 1-year-old site was excluded. In DCA, species with at least three individuals in total were used, and population data were transformed using logarithmic transformation, log10(x+1).
Results Density and species richness of collembolans The densities of collembolans ranged from 12,000 to 53,000 ind m2 (Fig. 1). They were slightly lower at the 1-year-old site than those at the other sites on all dates. In August the density at the 1-year-old site was significantly lower than that at the 4, 12 and 24-year-old site. A total of 87 collembolan species was found. Species richness was also slightly lower at the 1-year-old site than that at the other sites (Fig. 2). In August and November, average species richness was significantly lower at the 1-year-old site than that at most of the other sites. Detritus feeders were dominant both in density and species richness (70–87% in density and 47–57% in species richness) while sucking feeders had the lowest values (Fig. 3). The density and species richness of detritus feeders at the 1-year-old site tended to be lower than the other sites. The density of fungal feeders at the 1-year-old site also tended to be lower than that at the other sites. It increased at the 4-year-old site but gradually decreased after 4 years. Species richness of fungal feeders was similar at all sites. Sucking feeders tended to have a very low density and species richness at the 1-year-old site. Significant differences of density and species richness for these feeding groups were found between the 1-year-old site and some sites in August and November.
Correlation between collembolans and environmental variables Since seasonal changes in collembolan community structure were small, data on collembolan
M. Hasegawa et al. communities of the three sampling dates were pooled. The pooled data were used for Spearman rank correlation, DCA and CCA to relate them to environmental variables. Most of the variables of plant community did not significantly correlate with indices of collembolan community. Significantly positive correlation was only found between species richness of trees with DBHo5 cm and fungal feeder density (r s ¼ 0:755, Po0.05). In the variables of soil environments (Table 2), water content positively correlated with total species richness (r s ¼ 0:756, Po0.05) and sucking feeder species richness (r s ¼ 0:723, Po0.05), and forest floor mass negatively correlated with fungal feeder density (rs ¼ 0:731, Po0.05). The CCA analysis of detritus feeders selected no environmental variables in the forward selection process, and then detritus feeders were excluded from further analysis. Eigenvalues of the first two axes and their cumulative percentage in CCA were respectively as follows for total collembolans, 0.12%, 0.14% and 43.9%, fungal feeders, 0.20%, 0.20% and 55.9%, and sucking feeders, 0.42%, 0.30% and 53.6%. The eigenvalues and cumulative percentage variance showed that sucking and fungal feeders were relatively well classified, while total collembolans were not. In these three analyses, species richness of trees with DBH X 5 cm was selected as a factor related to the species composition of collembolans. In the analysis for sucking feeders, the forest age was also selected as a significant factor (Fig. 4a–c). Scores of the first axis of sucking feeders in the DCA ordination significantly (Po0.05) correlated with those of trees with DBH X 5 cm (r s ¼ 0:886).
Discussion The density and species richness of total collembolans was low at the 1-year-old site as compared with those at the older sites but not always significantly and not at all sampling times. A decrease in the density of microarthropods after clear-cutting has been reported by some studies (Vlug and Borden 1973; Seastedt and Crossley 1981; Bird and Chatarpaul 1986). The removal of canopy leads to harsh environmental conditions on the forest floor (Abbott et al. 1980). Abbott et al. (1980) showed that clearcutting caused a reduction in oribatid mite density and suggested that the reduction was due to changes in the temperature and humidity of the forest floor rather than to food availability in the litter. Our study also showed that the water content of forest floor organic matter at the 1-year-old site was lower than
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests
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70000 Apr. '02
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ab
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Fig. 1. Density of total collembolans of forest sites of different age after clear-cutting. Bars indicate standard errors; different letters indicate significant differences at Po0.05.
ARTICLE IN PRESS 122
M. Hasegawa et al. Average species richness per core
50
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Apr. '02
40
30
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30 c bc
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Fig. 2. Species richness of total collembolans of forest sites of different age after clear-cutting. Bars indicate standard errors; different letters indicate significant differences at Po0.05.
that at the other sites (Table 2). This may be a cause of the low abundance of collembolan fauna at the youngest site.
The density and species richness of collembolans at the 4-year-old site suggested that collembolans recover quickly after clear-cutting (Fig. 1). In
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests
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Fig. 3. Density (a) and species richness (b) of feeding groups of collembolans of forest sites of different age after clearcutting. For density (a), averages of data on three sampling dates are given. For species richness (b), totals of data on three sampling dates are given.
comparison with previous studies conducted in Canadian and European coniferous forests (Addison et al. 2003a,b; Zaitsev et al. 2002; Chauvat et al. 2003), this study showed a faster recovery of collembolan community in terms of total density and species richness. This might be attributed to the faster recovery in deciduous plant communities. In our study area shrub or small tree species, such as Rubus spp. or Salix spp., immediately invaded after clear-cutting and some tree species (for example, Quercus serrata) regenerated from
stumps by sprouting. Development of these young secondary forests might soon ameliorate the high temperature and/or low moisture environments that are experienced after clear-cutting. Total collembolan density did not significantly correlate with any soil environmental variables, but the density of fungal feeders negatively correlated with forest floor mass. In contrast, in previous studies positive correlations were observed between forest floor mass and density of collembolans were found (Petersen and Luxton 1982; Takeda
ARTICLE IN PRESS 124
M. Hasegawa et al.
Table 2. Forest floor mass and gravimetric water content, soil respiration in the top 4 cm soil, pH (KCl), EC and organic matter (loss on ignition) in the top 5 cm mineral soil of the forest studied Age
Forest floor mass (g m2)
Forest floor water Soil respiration content (%) (mg CO2 m2 s1)
pH (KCl) (1:5)
EC (dS m1)
Organic matter (%)
1 4 12 24 51 54 71 128
514 394 407 471 657 597 633 669
63 242 192 171 246 232 123 211
3.5 3.6 3.8 4.3 3.6 3.5 3.5 4.0
2.8 2.8 1.2 1.4 1.6 2.4 1.8 1.0
52.8 30.4 31.5 42.1 29.6 34.9 28.1 26.8
16.1 20.1 16.2 17.3 18.6 22.1 15.6 25.6
1987). In the present study, differences in the forest floor mass were relatively small (Table 2), and might not reflect the habitat and food availability for collembolans. Species richness of trees with DBHo5 cm positively correlated with that of fungal feeding collembolans suggesting that small tree species dominant in early successional stages of deciduous broad-leaved forests might be favoured by fungal feeders. The litter of such tree species tends to decompose faster than late successional tree species due to its relatively high nitrogen concentration and low lignin content (Osono and Takeda 2005a,b). Possibly, fungal feeders were abundant at the sites with little forest floor due to high fungal activity in early successional tree species litter (Takeda 1987). Forest floor water content did not correlate with species richness of either detritus feeders or fungal feeders, but it positively correlated with species richness of total collembolans and of sucking feeders. Sucking feeders take up organic matter or bacteria through water in the soil (Singh 1969; Adams and Salmon 1972). Therefore, low water content might limit their diversity. Detritus feeders were the most dominant group in this study, and did not show any significant correlation with soil and plant variables. Compared with the other groups, detritus feeders are food and habitat generalists rather than specialists and this may explain their weak response to changes in the plant community structure. Plant species richness did not correlate with species richness of collembolans. The effect of plant species richness of forests on soil microarthropods has been investigated using litterbags with single and mixed species litter (Kaneko and Salamanca 1999; Hansen and Coleman 1998). Kaneko and Salamanca (1999) suggested that microarthropod abundance and oribatid mite diversity were higher in mixed (2 or 3 species)
litter than in single species litter. Hansen and Coleman (1998) also suggested that oribatid mite species richness in mixed litter is significantly higher than that in the single species litter, but they found no differences in oribatid diversity between the mixed litter of three and seven species. Relationships between plant species richness and soil arthropod performance also have been investigated in grassland ecosystems (Koricheva et al. 2000; Hedlund et al. 2003). In an experiment conducted in plots with varying numbers (4–15) of plant species, Hedlund et al. (2003) showed that the numbers of collembolan and mites were not influenced by plant biomass production or plant species numbers. Likewise, Salamon et al. (2004) failed to find any correlation between species richness or functional group of plant and total diversity of collembolans in their experiment conducted in a series of plots with up to 32 plant species in a grassland community. These results indicate that the number of plant species influences the density and/or diversity of soil microarthropods only in simple systems with low numbers of plant species as investigated by Kaneko and Salamanca (1999). The effect of plant species richness on arthropod diversity disappears or becomes redundant in ecosystems with larger numbers of plant species as also found in the present study. In contrast to the diversity of collembolans, plant community structures correlated with the collembolan species composition. In CCA analysis for total collembolans, fungal feeders and sucking feeders, the species richness of trees with DBH X 5 cm was related to the species composition of collembolans (Fig. 4). DCA scores of sucking feeders significantly correlated with the scores of DCA in trees with DBH X 5 cm. These results suggest that the species compositions of some collembolan feeding groups are associated with the diversity or species
ARTICLE IN PRESS Collembolan community dynamics in deciduous forests (a)
1.0 1
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forests recovered from clear-cutting faster than those reported in coniferous forests in Canada and Europe. This might be attributed to fast recovery of the deciduous forest plants in an early phase of secondary succession than of conifers. Species composition of detritus feeders (dominating the collembolan community) showed a weak response to soil and plant variables. In contrast, the species composition of fungal feeders and sucking feeders was more closely associated with the changes in plant communities, and took longer to recover. If collembolans are to be used as biological indicators for forest management, it is recommended to investigate not only total density and species richness but also community structure and functional composition.
128 51 Tomo
Hyp
125
We would like to thank the staff of the Insect Ecology Laboratory and the Kiso Experimental Station at the Forestry and Forest Products Research Institute for their help and guidance in the field research and laboratory analysis. Also, we thank Mrs. S. Sebayashi for her help in sorting the soil fauna. This study was supported by research grant #200004 of the Forestry and Forest Products Research Institute.
Supero 3 51
Frie
References
Pseud 4 128
-0.6 -0.4
Supero1 1 4
1.0
Fig. 4. CCA ordination plots for total collembolans (a), fungal feeders (b) and sucking feeders (c). Diamonds show the positions of communities with forest age indicated by numerals. Crosses show the positions of the main species. Significant environmental variables are shown by arrows. Cer sp.1; Ceratophysella sp.1, Hyp; Hypogastrura sp.1, Pter; Pteronychella spatiosa Uchida and Tamura, 1968, Cer den; Ceratophysella denisana (Yosii, 1956), Tomo; Tomocerus varius Folsom, 1899, Frie; Friesea japonica Yosii, 1954, Pseud 4; Pseudachorhutes sp.4, Supero 3; Superodontella sp.3, Pseud 3; Pseudachorhutes sp.3, Supero 1; Superodontella sp.1.
composition of large trees, though the mechanisms underlying the association is unknown. In conclusion, this study showed that abundance and species richness of Collembolans in deciduous
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