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Seasonal distribution of Xenylla brevispina (Collembola) in the canopy and soil habitat of a Cryptomeria japonica plantation
ARTICLE IN PRESS Pedobiologia 50 (2006) 235—242
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Seasonal distribution of Xenylla brevispina (Collembola) in the canopy and soil habitat of a Cryptomeria japonica plantation Tomohiro Yoshida, Naoki Hijii Laboratory of Forest Protection, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan Received 9 September 2005; accepted 17 December 2005
KEYWORDS Collembola; Cryptomeria japonica plantation; Forest canopy; Life cycle; Vertical migration; Xenylla brevispina
Summary We investigated the life cycle and habitat use of an arboreal collembolan species, Xenylla brevispina, in the canopy and soil of a conifer (Cryptomeria japonica D. Don) plantation. The adaptive significance of migration between arboreal and soil habitats in the maintenance of its population in relation to the vertical structure of the forest is discussed. We sampled dead branches with foliage in the canopy (canopy litter) and on the forest-floor (soil litter). X. brevispina had one generation a year throughout the 3 years of the study. The mean densities of X. brevispina were similar in the canopy litter (0.06 to 14.57 g1 dry weight) and the soil litter (0.44 to 18.99 g1 dry weight). Seasonal patterns of density and relative abundance indicate that individuals of X. brevispina in the canopy were closely associated with those in the soil. These results suggest that vertical migration between the canopy and the soil might be a strategy allowing X. brevispina to be a predominant collembolan species in this forest. & 2006 Elsevier GmbH. All rights reserved.
Introduction In terrestrial ecosystems, producer and decomposer subsystems are established between aboveand below-ground components, and the importance of simultaneous analysis of both components has Corresponding author. Tel.: +81 52 789 4181;
fax: +81 52 789 5518. E-mail address: [email protected] (T. Yoshida).
increasingly been recognized in clarifying the patterns and processes of ecosystem function (Wardle, 2002; Wardle et al., 2004). In the aboveground component of forest ecosystems, numerous and varied detritivorous and fungivorous microarthropods are found on dead foliage and branches, bark, suspended soils and epiphytes (Andre´, 1983, 1984; Nadkarni and Longino, 1990; Paoletti et al., 1991; Prinzing and Wirtz, 1997; Walter and BehanPelletier, 1999; Winchester et al., 1999; Yoshida
0031-4056/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2005.12.002
ARTICLE IN PRESS 236 and Hijii, 2005a). The abundance and diversity of such microarthropods in arboreal habitats imply that a decomposer subsystem is also formed in the canopy, and that the microarthropods may determine the structure and function of detrital food webs (Hijii, 1989; Nadkarni and Longino, 1990; Yoshida and Hijii, 2005a) and may also play important roles in regulating rates of decomposition and nutrient cycling and in maintaining the biodiversity of forest ecosystems (Wardle et al., 2003; Fonte and Schowalter, 2004). Collembolans that utilize plant litter as food and habitat resources (Takeda, 1987, 1995) live in both arboreal and soil habitats in forests (Bowden et al., 1976; Hijii, 1989; Rogers and Kitching, 1998; Yoshida and Hijii, 2005a, b), and some species are known to migrate seasonally between both habitats (Bowden et al., 1976; Von Allmen and Zettel, 1982; Leinaas, 1983; Hisamatsu and Matsunaga, 1994; Ichisawa, 2001; Yoshida and Hijii, 2005b). Driving forces for the migration of collembolans could be the search for ideal microclimates (Usher, 1970; Hijii, 1987; Hopkin, 1997) or available food resources (Hassel et al., 1986; Prinzing and Woas, 2003). Variability of environmental conditions such as temperature and humidity in arboreal habitats may be greater than that in the soil, and this situation should be less favorable for the reproduction of collembolans than edaphic environments (Nicolai, 1986; Prinzing and Wirtz, 1997). For example, some arboreal collembolan species hatch in the soil because of poor resistance of their eggs to desiccation aboveground (Von Allmen and Zettel, 1982; Hisamatsu and Matsunaga, 1994). An arboreal collembolan species, Xenylla brevispina Kinoshita is dominant in the canopy of Japanese conifer forests (Uchida and Kojima, 1966; Yoshida and Hijii, 2005b). Itoh (1991) revealed that this species deposited about 60 eggs per batch on average in the litter at the soil surface. Because egg hatch did not occur at all below 70% relative humidity in a culture experiment, and relative humidity in the canopy is mostly lower than 70% during the daytime, the survival rate of eggs of this species would be much lower in the canopy. This species hatches in the soil in spring, moves upward into the canopy for growth during summer and moves down to the soil for overwintering (Itoh, 1991). Thus, X. brevispina does not complete its life cycles only in the canopy and migrates between both habitats, and may have maintained large populations in forests by efficiently utilizing the vertical structure of the forest from the canopy to the soil. Clarification of the life history and population dynamics of X. brevispina in both habitats would
T. Yoshida, N. Hijii help us to better understand the adaptive significance of making their way into arboreal habitats in collembolans that originated in the soil. Such studies should extend to the community structure of canopy arthropods, including the predators that prey on collembolans. These approaches require quantification of collembolan abundances, and resources that are available to them simultaneously, in both the canopy and soil. A previous study of the life cycles of X. brevispina (Itoh, 1991) did not use the same method to quantify both population dynamics and resource suitability in the canopy and soil and, therefore, did not examine spatiotemporal associations between canopy and soil assemblages of this species. In this study, we investigated the life cycle of X. brevispina and seasonal changes in its population density and size distribution in a plantation of Japanese cedar (Cryptomeria japonica D. Don), which retains a large amount of litter in the canopy (Yoshida and Hijii, 2005b). We discuss the adaptive significance of migration between the canopy and soil for maintenance of its population in relation to the vertical structure of the forest.
Materials and methods Study sites The study was carried out in a 33-year-old (as of 2003) plantation of Japanese cedar in the Experimental Forest of Nagoya University in central Japan (351110 N, 1371330 E; 980–1000 m asl). Details of the study site were presented in Yoshida and Hijii (2005b). Annual rainfall in this site averaged 2137 mm (2001–2004). The mean air and soil (at 5 cm depth) temperatures over the study period were 10.8 and 12.5 1C, respectively. The degree of seasonal fluctuation in air and soil temperatures was expressed in terms of monthly range of temperatures, defined as a maximum of mean daily temperatures minus a minimum of mean daily temperatures in each month. In mature C. japonica plantations, there was constantly a large amount of dead branches with foliage that remained attached to the trunk in the lower parts of the canopy. We defined them as ‘‘canopy litter’’, and the litter on the forest floor as ‘‘soil litter’’. There was no canopy litter on the trees below 6 m above the ground, because of lack of branches due to a pruning operation long past. Small amounts of mosses and lichens grew in patches on the branches and trunks, but there was no accumulation of leaves of any other species in the canopy at our site.
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat
Microarthropod sampling in canopy litter and soil litter We carried out monthly canopy litter surveys from May 2001 to April 2004. Litter was sampled from the soil stratum about 1 week after the canopy sampling, but only in the period May 2003 to April 2004. In the canopy, we sampled dead leaves (defined as dead leaves and foliage shoots with a diameter of less than 5 mm) as the canopy litter, by clipping dead branches from each tree after climbing a ladder set against the trunk. Litter samples were collected in polyethylene bags (400 mm wide, 600 mm deep, 0.05 mm thick) that were sealed with string for transport to the laboratory. We randomly selected five (from May 2001 to April 2003) or four (from May 2003 to April 2004) sample trees in this forest, and collected one litter sample from the lower part of the canopy of each tree at a height of about 6–9 m, giving a total of five samples (May 2001 to April 2003) or at 1 m intervals at heights of 7–17 m, giving a total of 30 to 39 samples (May 2003 to April 2004) on each sampling occasion. In the soil, we randomly established ten 25 25 cm quadrats on the forest floor within a radius of about 1 m from the bases of trees that were not used for canopy sampling on any of the sampling dates. We sampled the litter from each quadrat to a depth of 3 cm below the litter surface (the ‘‘soil litter’’), except in December and January when the ground was frozen. We used five of the ten litter samples for microarthropod extraction. We extracted microarthropods from both the canopy litter and soil litter samples by using Tullgren funnels for 6 days, and then preserved them in 60% ethanol. We identified collembolans to the species level under an optical microscope ( 100, 400) and counted them. Body lengths of X. brevispina were measured to the nearest 0.01 mm and grouped in 0.05-mm-size classes. After extraction of the microarthropods, including collembolans, we dried all litter samples in a convection oven (85 1C, 48 h) and weighed them. We expressed the densities of collembolans collected from the canopy litter or the soil litter as the number of individuals per unit dry weight of litter (g–1 dry weight) (Yoshida and Hijii, 2005b).
237 soil litter on any of the sampling occasions from May 2003 to April 2004 (t-test, Po0:01). Lengths ranged from 0.26 mm (min) to 1.81 mm (max) for canopy individuals, and from 0.20 mm to 1.58 mm for soil individuals (Fig. 1). Large individuals occurred among the canopy individuals from May to July, whereas juveniles were found exclusively in late July and in August. Thereafter, size distributions in the canopy were similar among all months until the following early May. In contrast, juveniles of soil individuals occurred from July to October, and although the overall seasonal trend in size distribution was similar to that of canopy individuals, the duration of their recruitment period appeared longer. Growth curves for canopy individuals of X. brevispina indicated that this species had at least four annual generations during the study period (Fig. 2). In the canopy, juveniles appeared in July, maintained a relatively constant size until next March and, thereafter, grew rapidly. In the soil, juveniles also appeared in July, and grew gradually from July to August in the next year. The mean body size of individuals in the canopy decreased from June to July or August.
Seasonal changes in density and relative abundance The seasonal densities of X. brevispina were similar between the canopy litter (0.0670.08 to 14.5777.18 [mean7SD] g1 dry weight) and the soil litter (0.4470.25 to 18.9976.86 g–1 dry weight) (Fig. 3). The density of canopy individuals did not exceed 10 g1 dry weight throughout 2001 to 2004, except in August 2003, and this increase occurred several weeks later than that of the soil individuals. The density of the soil individuals increased markedly from July to August 2003 and peaked at about 20 g–1 dry weight. The relative abundance of X. brevispina continuously accounted for more than 50% of all collembolans in the canopy litter, but varied greatly from 5% to 67% in the soil litter (Fig. 4). The proportion in the canopy decreased in July and in winter, whereas that in the soil increased in those seasons, suggesting that the abundances of X. brevispina in both the canopy and soil were closely related due to migration.
Results Discussion Seasonal changes in size distribution The body lengths of Xenylla brevispina in the canopy litter were significantly larger than those in
At this study site, X. brevispina had one generation a year throughout the 3 years of the study. This species probably laid eggs from July to October in
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Fig. 1. Seasonal changes in body length distribution within populations of Xenylla brevispina in the canopy litter and soil litter in the Cryptomeria japonica plantation. N indicates the number of individuals measured.
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat
Body length [mm]
2.0
(a)
1.0
0.0
M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M AM 2001 2002 2003 2004
Body length [mm]
2.0
(b)
1.0
0.0
M J J A S O N D J F M AM 2003 2004
Fig. 2. Growth curves of Xenylla brevispina in the canopy litter and soil litter in the Cryptomeria japonica plantation. Vertical lines indicate 71SD.
Mean number of individuals per litter mass [g-1 dry wt]
30
20
10
0
M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M AM 2001 2002 2003 2004
Fig. 3. Seasonal changes in densities of Xenylla brevispina in the canopy litter (solid circles) and soil litter (open circles) in the Cryptomeria japonica plantation. Vertical lines indicate 71SD.
the soil, maintained its small size during the overwintering period, and then grew rapidly starting in March; the large individuals then died after June. By October, this cohort had disappeared from both the canopy and soil. A life cycle of X. brevispina similar to this has been reported from canopy and soil in a temperate pine (Pinus densiflora) forest in Japan (Itoh, 1991), but the period of recruitment in both canopy and soil habitats began later in our study, possibly because of a lower soil temperature at our study site. The seasonal patterns of density and relative abundance suggest that individuals of X. brevispina in both the canopy and soil were closely associated. The population dynamics of this species likely encompass breeding in the soil and seasonal vertical migration between habitats, as in summer, the density in the canopy increased several weeks later than the increase in density in the soil. We
239 interpreted the data to mean that the relative abundance of this species in the canopy decreased in July because of death of the previous generation in the canopy, and then increased in August because of recruitment of the new generation from the soil. In winter, the decrease in the relative abundance in the canopy and the increase in the soil occured simultaneously. This may have occurred because X. brevispina in the canopy moved down to the soil (Itoh, 1991) and some collembolan species other than X. brevispina in the soil migrated deep into the soil to avoid the decline in temperature (Tamura et al., 1969; Usher, 1970; Hijii, 1987); or because X. brevispina did not move upward into the canopy but stayed in the soil litter. Seasonal patterns of size distribution of X. brevispina were similar between the canopy and soil, but the duration of recruitment in the canopy was shorter than in the soil. This result suggests that there are some barriers, such as drought and distance, to juveniles of X. brevispina moving from the soil into the canopy. Collembolans are known to move upward into the canopy during the rainy season (Bowden et al., 1976; Bauer, 1979) but, as our study suggests, in dry season juveniles would not move upward, and only older individuals with higher tolerance to drought (e.g. Leinaas and Sømme, 1984; Leinaas and Fjellberg, 1985) would colonize arboreal habitats. Similarities in densities of X. brevispina in canopy and soil litter suggest that both litter habitats share resources essential for this species. At this site, the density of all collembolans is significantly higher in the soil than in the canopy, because most collembolans other than X. brevispina live exclusively in soil (Yoshida and Hijii, 2005b). Microclimatic variability as indicated by mean monthly range of temperatures over the study period was greater in the canopy (9.4 1C) than in the soil (5.3 1C), and canopy litter may be a resource and a habitat less available to collembolans, other than X. brevispina. Since X. brevispina apparently has a high tolerance to desiccation and moves about actively (Itoh, 1991), the dominance of this species in the canopy could result from this species tolerating such larger variations in microclimate than other species. Alternatively, X. brevispina could utilize resources in the canopy less available to other species. On exposed habitats such as rocks and tree trunks, collembolans are likely have strategies for coping with drought (Leinaas and Sømme, 1984; Prinzing, 1997; Prinzing and Wirtz, 1997). Leinaas and Fjellberg (1985) reported that two collembolan species had different strategies for utilizing lichens
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Fig. 4. Seasonal changes in the relative abundance of Xenylla brevispina in (a) the canopy litter and (b) the soil litter in the Cryptomeria japonica plantation.
on exposed habitats: (1) a physiological adaptation to resist severe environmental conditions (staying strategy) and (2) an escape from such conditions by moving within or between habitats (migration strategy), X. brevispina may have the latter strategy. Our results suggest that X. brevispina is a species that can take advantage of the three-dimensional structure of the forest. Individuals in the canopy and those in the soil can, respectively, be considered as sink and source, because egg hatch apparently occurs in the soil, and individuals then disperse into the canopy. The density of all collembolans per unit litter mass was significantly larger in the soil than in the canopy (Yoshida and Hijii, 2005b) and, thus, competitions among them and/or with other detritivorous and fungivorous microarthropods may be stronger in the soil than in the canopy. Colonization by individuals born in the soil (source) into the canopy (sink) may have helped X. brevispina to avoid competition with other microarthropods in the soil, to expand its carrying capacity, and thus to become a predominant collembolan species in this forest. Presence of X. brevispina into the canopy also implies that this species influences the community
structures of arboreal arthropods. In the canopy of this forest, hunting spiders have frequently been observed to prey on collembolans. Collembolans are potential food resources for predators such as spiders (Wise, 1993, 2004), and those that migrate into the canopy from the soil could, therefore, be a subsidized food resource for arboreal predators (Winchester, 1997; Halaj et al., 2000) referred to as a ‘‘detrital infusion’’ (Polis and Strong, 1996). To better understand the functional roles of collembolans in food web and decomposition processes in both canopy and soil, further investigations are required on the ecological linkages between canopy and soil and dispersal of collembolans between these habitats (Bowden et al., 1976; Itoh, 1991; Ichisawa, 2001).
Acknowledgments We are grateful to Drs. R. Itoh and M.K. Hasegawa of Showa University, and to Dr. M.T. Hasegawa of the Forestry and Forest Products Research Institute, Kiso Experimental Station, for their useful suggestions on this manuscript. We
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat thank Messrs. Y. Imaizumi and N. Yamaguchi and all the members of the Laboratory of Forest Protection, Nagoya University, for their helpful suggestions and support. This study was supported in part by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (no. 10660142).
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241 to lichen habitats on alpine rocks. Oikos 43, 197–206. Leinaas, H.P., Fjellberg, A., 1985. Habitat structure and life history strategies of two partly sympatric and closely related, lichen feeding collembolan species. Oikos 44, 448–458. Nadkarni, N.M., Longino, J.T., 1990. Invertebrates in canopy and ground organic matter in a neotropical montane forest, Costa Rica. Biotropica 22, 286–289. Nicolai, V., 1986. The bark of trees: thermal properties, microclimate and fauna. Oecologia 69, 148–160. Paoletti, M.G., Taylor, R.A.J., Stinner, B.R., Stinner, D.H., Benzing, D.H., 1991. Diversity of soil fauna in the canopy and forest floor of a Venezuelan cloud forest. J. Trop. Ecol. 7, 373–383. Polis, G.A., Strong, D.R., 1996. Food web complexity and community dynamics. Am. Nat. 147, 813–846. Prinzing, A., 1997. Spatial and temporal use of microhabitats as a key strategy for the colonization of tree bark by Entomobrya nivalis L. (Collembola: Entomobryidae). In: Stork, N.E., Adis, J., Didham, R.K. (Eds.), Canopy Arthropods. Chapman and Hall, London, pp. 453–476. Prinzing, A., Wirtz, H.-P., 1997. The epiphytic lichen, Evernia prunastri L., as a habitat for arthropods: shelter from desiccation, food-limitation and indirect mutualism. In: Stork, N.E., Adis, J., Didham, R.K. (Eds.), Canopy Arthropods. Chapman and Hall, London, pp. 477–494. Prinzing, A., Woas, S., 2003. Habitat use and stratification of Collembola and oribatid mites. In: Basset, Y., Novotny, V., Miller, S.E., Kitching, R.L. (Eds.), Arthropods of Tropical Forests. Cambridge University Press, Cambridge, pp. 271–281. Rogers, D.J., Kitching, R.L., 1998. Vertical stratification of rainforest collembolan (Collembola: Insecta) assemblages: description of ecological patterns and hypotheses concerning their generation. Ecography 21, 392–400. Takeda, H., 1987. Dynamics and maintenance of collembolan community structure in a forest soil system. Res. Popul. Ecol. 29, 291–346. Takeda, H., 1995. Templates for the organization of collembolan communities. In: Edwards, C.A., Abe, T., Striganova, B.R. (Eds.), Structure and Function of Soil Communities. Kyoto University Press, Kyoto, pp. 5–20. Tamura, H., Nakamura, Y., Yamauchi, K., Fujikawa, T., 1969. An ecological survey of soil fauna in Hidaka– Monbetsu, southern Hokkaido. J. Fac. Sci., Hokkaido Univ. Ser. VI Zool. 17, 17–57. Uchida, H., Kojima, K., 1966. On the Collembola obtained by the aircraft chemical application. Kontyu 34, 317–326 (in Japanese with English summary). Usher, M.B., 1970. Seasonal and vertical distribution of a population of soil arthropods: Collembola. Pedobiologia 10, 224–236. Von Allmen, H., Zettel, J., 1982. Populationsbiologische Untersuchungen zur Art Entomobrya nivalis (Collembola). Rev. Suisse Zool. 89, 919–926.
ARTICLE IN PRESS 242 Walter, D.E., Behan-Pelletier, V., 1999. Mites in forest canopies: filling the size distribution shortfall? Ann. Rev. Entomol. 44, 1–19. Wardle, D.A., 2002. Communities and Ecosystems. Linking the Aboveground and Belowground Components. Princeton University Press, Princeton. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Seta ¨la ¨, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633. Wardle, D.A., Yeates, G.W., Barker, G.M., Bellingham, P.J., Bonner, K.I., Williamson, W.M., 2003. Island biology and ecosystem functioning in epiphytic soil communities. Science 301, 1717–1720. Winchester, N.N., 1997. The arboreal superhighway: arthropods and landscape dynamics. Can. Entomol. 129, 595–599.
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Seasonal distribution of Xenylla brevispina (Collembola) in the canopy and soil habitat of a Cryptomeria japonica plantation Tomohiro Yoshida, Naoki Hijii Laboratory of Forest Protection, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan Received 9 September 2005; accepted 17 December 2005
KEYWORDS Collembola; Cryptomeria japonica plantation; Forest canopy; Life cycle; Vertical migration; Xenylla brevispina
Summary We investigated the life cycle and habitat use of an arboreal collembolan species, Xenylla brevispina, in the canopy and soil of a conifer (Cryptomeria japonica D. Don) plantation. The adaptive significance of migration between arboreal and soil habitats in the maintenance of its population in relation to the vertical structure of the forest is discussed. We sampled dead branches with foliage in the canopy (canopy litter) and on the forest-floor (soil litter). X. brevispina had one generation a year throughout the 3 years of the study. The mean densities of X. brevispina were similar in the canopy litter (0.06 to 14.57 g1 dry weight) and the soil litter (0.44 to 18.99 g1 dry weight). Seasonal patterns of density and relative abundance indicate that individuals of X. brevispina in the canopy were closely associated with those in the soil. These results suggest that vertical migration between the canopy and the soil might be a strategy allowing X. brevispina to be a predominant collembolan species in this forest. & 2006 Elsevier GmbH. All rights reserved.
Introduction In terrestrial ecosystems, producer and decomposer subsystems are established between aboveand below-ground components, and the importance of simultaneous analysis of both components has Corresponding author. Tel.: +81 52 789 4181;
fax: +81 52 789 5518. E-mail address: [email protected] (T. Yoshida).
increasingly been recognized in clarifying the patterns and processes of ecosystem function (Wardle, 2002; Wardle et al., 2004). In the aboveground component of forest ecosystems, numerous and varied detritivorous and fungivorous microarthropods are found on dead foliage and branches, bark, suspended soils and epiphytes (Andre´, 1983, 1984; Nadkarni and Longino, 1990; Paoletti et al., 1991; Prinzing and Wirtz, 1997; Walter and BehanPelletier, 1999; Winchester et al., 1999; Yoshida
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ARTICLE IN PRESS 236 and Hijii, 2005a). The abundance and diversity of such microarthropods in arboreal habitats imply that a decomposer subsystem is also formed in the canopy, and that the microarthropods may determine the structure and function of detrital food webs (Hijii, 1989; Nadkarni and Longino, 1990; Yoshida and Hijii, 2005a) and may also play important roles in regulating rates of decomposition and nutrient cycling and in maintaining the biodiversity of forest ecosystems (Wardle et al., 2003; Fonte and Schowalter, 2004). Collembolans that utilize plant litter as food and habitat resources (Takeda, 1987, 1995) live in both arboreal and soil habitats in forests (Bowden et al., 1976; Hijii, 1989; Rogers and Kitching, 1998; Yoshida and Hijii, 2005a, b), and some species are known to migrate seasonally between both habitats (Bowden et al., 1976; Von Allmen and Zettel, 1982; Leinaas, 1983; Hisamatsu and Matsunaga, 1994; Ichisawa, 2001; Yoshida and Hijii, 2005b). Driving forces for the migration of collembolans could be the search for ideal microclimates (Usher, 1970; Hijii, 1987; Hopkin, 1997) or available food resources (Hassel et al., 1986; Prinzing and Woas, 2003). Variability of environmental conditions such as temperature and humidity in arboreal habitats may be greater than that in the soil, and this situation should be less favorable for the reproduction of collembolans than edaphic environments (Nicolai, 1986; Prinzing and Wirtz, 1997). For example, some arboreal collembolan species hatch in the soil because of poor resistance of their eggs to desiccation aboveground (Von Allmen and Zettel, 1982; Hisamatsu and Matsunaga, 1994). An arboreal collembolan species, Xenylla brevispina Kinoshita is dominant in the canopy of Japanese conifer forests (Uchida and Kojima, 1966; Yoshida and Hijii, 2005b). Itoh (1991) revealed that this species deposited about 60 eggs per batch on average in the litter at the soil surface. Because egg hatch did not occur at all below 70% relative humidity in a culture experiment, and relative humidity in the canopy is mostly lower than 70% during the daytime, the survival rate of eggs of this species would be much lower in the canopy. This species hatches in the soil in spring, moves upward into the canopy for growth during summer and moves down to the soil for overwintering (Itoh, 1991). Thus, X. brevispina does not complete its life cycles only in the canopy and migrates between both habitats, and may have maintained large populations in forests by efficiently utilizing the vertical structure of the forest from the canopy to the soil. Clarification of the life history and population dynamics of X. brevispina in both habitats would
T. Yoshida, N. Hijii help us to better understand the adaptive significance of making their way into arboreal habitats in collembolans that originated in the soil. Such studies should extend to the community structure of canopy arthropods, including the predators that prey on collembolans. These approaches require quantification of collembolan abundances, and resources that are available to them simultaneously, in both the canopy and soil. A previous study of the life cycles of X. brevispina (Itoh, 1991) did not use the same method to quantify both population dynamics and resource suitability in the canopy and soil and, therefore, did not examine spatiotemporal associations between canopy and soil assemblages of this species. In this study, we investigated the life cycle of X. brevispina and seasonal changes in its population density and size distribution in a plantation of Japanese cedar (Cryptomeria japonica D. Don), which retains a large amount of litter in the canopy (Yoshida and Hijii, 2005b). We discuss the adaptive significance of migration between the canopy and soil for maintenance of its population in relation to the vertical structure of the forest.
Materials and methods Study sites The study was carried out in a 33-year-old (as of 2003) plantation of Japanese cedar in the Experimental Forest of Nagoya University in central Japan (351110 N, 1371330 E; 980–1000 m asl). Details of the study site were presented in Yoshida and Hijii (2005b). Annual rainfall in this site averaged 2137 mm (2001–2004). The mean air and soil (at 5 cm depth) temperatures over the study period were 10.8 and 12.5 1C, respectively. The degree of seasonal fluctuation in air and soil temperatures was expressed in terms of monthly range of temperatures, defined as a maximum of mean daily temperatures minus a minimum of mean daily temperatures in each month. In mature C. japonica plantations, there was constantly a large amount of dead branches with foliage that remained attached to the trunk in the lower parts of the canopy. We defined them as ‘‘canopy litter’’, and the litter on the forest floor as ‘‘soil litter’’. There was no canopy litter on the trees below 6 m above the ground, because of lack of branches due to a pruning operation long past. Small amounts of mosses and lichens grew in patches on the branches and trunks, but there was no accumulation of leaves of any other species in the canopy at our site.
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat
Microarthropod sampling in canopy litter and soil litter We carried out monthly canopy litter surveys from May 2001 to April 2004. Litter was sampled from the soil stratum about 1 week after the canopy sampling, but only in the period May 2003 to April 2004. In the canopy, we sampled dead leaves (defined as dead leaves and foliage shoots with a diameter of less than 5 mm) as the canopy litter, by clipping dead branches from each tree after climbing a ladder set against the trunk. Litter samples were collected in polyethylene bags (400 mm wide, 600 mm deep, 0.05 mm thick) that were sealed with string for transport to the laboratory. We randomly selected five (from May 2001 to April 2003) or four (from May 2003 to April 2004) sample trees in this forest, and collected one litter sample from the lower part of the canopy of each tree at a height of about 6–9 m, giving a total of five samples (May 2001 to April 2003) or at 1 m intervals at heights of 7–17 m, giving a total of 30 to 39 samples (May 2003 to April 2004) on each sampling occasion. In the soil, we randomly established ten 25 25 cm quadrats on the forest floor within a radius of about 1 m from the bases of trees that were not used for canopy sampling on any of the sampling dates. We sampled the litter from each quadrat to a depth of 3 cm below the litter surface (the ‘‘soil litter’’), except in December and January when the ground was frozen. We used five of the ten litter samples for microarthropod extraction. We extracted microarthropods from both the canopy litter and soil litter samples by using Tullgren funnels for 6 days, and then preserved them in 60% ethanol. We identified collembolans to the species level under an optical microscope ( 100, 400) and counted them. Body lengths of X. brevispina were measured to the nearest 0.01 mm and grouped in 0.05-mm-size classes. After extraction of the microarthropods, including collembolans, we dried all litter samples in a convection oven (85 1C, 48 h) and weighed them. We expressed the densities of collembolans collected from the canopy litter or the soil litter as the number of individuals per unit dry weight of litter (g–1 dry weight) (Yoshida and Hijii, 2005b).
237 soil litter on any of the sampling occasions from May 2003 to April 2004 (t-test, Po0:01). Lengths ranged from 0.26 mm (min) to 1.81 mm (max) for canopy individuals, and from 0.20 mm to 1.58 mm for soil individuals (Fig. 1). Large individuals occurred among the canopy individuals from May to July, whereas juveniles were found exclusively in late July and in August. Thereafter, size distributions in the canopy were similar among all months until the following early May. In contrast, juveniles of soil individuals occurred from July to October, and although the overall seasonal trend in size distribution was similar to that of canopy individuals, the duration of their recruitment period appeared longer. Growth curves for canopy individuals of X. brevispina indicated that this species had at least four annual generations during the study period (Fig. 2). In the canopy, juveniles appeared in July, maintained a relatively constant size until next March and, thereafter, grew rapidly. In the soil, juveniles also appeared in July, and grew gradually from July to August in the next year. The mean body size of individuals in the canopy decreased from June to July or August.
Seasonal changes in density and relative abundance The seasonal densities of X. brevispina were similar between the canopy litter (0.0670.08 to 14.5777.18 [mean7SD] g1 dry weight) and the soil litter (0.4470.25 to 18.9976.86 g–1 dry weight) (Fig. 3). The density of canopy individuals did not exceed 10 g1 dry weight throughout 2001 to 2004, except in August 2003, and this increase occurred several weeks later than that of the soil individuals. The density of the soil individuals increased markedly from July to August 2003 and peaked at about 20 g–1 dry weight. The relative abundance of X. brevispina continuously accounted for more than 50% of all collembolans in the canopy litter, but varied greatly from 5% to 67% in the soil litter (Fig. 4). The proportion in the canopy decreased in July and in winter, whereas that in the soil increased in those seasons, suggesting that the abundances of X. brevispina in both the canopy and soil were closely related due to migration.
Results Discussion Seasonal changes in size distribution The body lengths of Xenylla brevispina in the canopy litter were significantly larger than those in
At this study site, X. brevispina had one generation a year throughout the 3 years of the study. This species probably laid eggs from July to October in
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Fig. 1. Seasonal changes in body length distribution within populations of Xenylla brevispina in the canopy litter and soil litter in the Cryptomeria japonica plantation. N indicates the number of individuals measured.
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat
Body length [mm]
2.0
(a)
1.0
0.0
M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M AM 2001 2002 2003 2004
Body length [mm]
2.0
(b)
1.0
0.0
M J J A S O N D J F M AM 2003 2004
Fig. 2. Growth curves of Xenylla brevispina in the canopy litter and soil litter in the Cryptomeria japonica plantation. Vertical lines indicate 71SD.
Mean number of individuals per litter mass [g-1 dry wt]
30
20
10
0
M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M AM 2001 2002 2003 2004
Fig. 3. Seasonal changes in densities of Xenylla brevispina in the canopy litter (solid circles) and soil litter (open circles) in the Cryptomeria japonica plantation. Vertical lines indicate 71SD.
the soil, maintained its small size during the overwintering period, and then grew rapidly starting in March; the large individuals then died after June. By October, this cohort had disappeared from both the canopy and soil. A life cycle of X. brevispina similar to this has been reported from canopy and soil in a temperate pine (Pinus densiflora) forest in Japan (Itoh, 1991), but the period of recruitment in both canopy and soil habitats began later in our study, possibly because of a lower soil temperature at our study site. The seasonal patterns of density and relative abundance suggest that individuals of X. brevispina in both the canopy and soil were closely associated. The population dynamics of this species likely encompass breeding in the soil and seasonal vertical migration between habitats, as in summer, the density in the canopy increased several weeks later than the increase in density in the soil. We
239 interpreted the data to mean that the relative abundance of this species in the canopy decreased in July because of death of the previous generation in the canopy, and then increased in August because of recruitment of the new generation from the soil. In winter, the decrease in the relative abundance in the canopy and the increase in the soil occured simultaneously. This may have occurred because X. brevispina in the canopy moved down to the soil (Itoh, 1991) and some collembolan species other than X. brevispina in the soil migrated deep into the soil to avoid the decline in temperature (Tamura et al., 1969; Usher, 1970; Hijii, 1987); or because X. brevispina did not move upward into the canopy but stayed in the soil litter. Seasonal patterns of size distribution of X. brevispina were similar between the canopy and soil, but the duration of recruitment in the canopy was shorter than in the soil. This result suggests that there are some barriers, such as drought and distance, to juveniles of X. brevispina moving from the soil into the canopy. Collembolans are known to move upward into the canopy during the rainy season (Bowden et al., 1976; Bauer, 1979) but, as our study suggests, in dry season juveniles would not move upward, and only older individuals with higher tolerance to drought (e.g. Leinaas and Sømme, 1984; Leinaas and Fjellberg, 1985) would colonize arboreal habitats. Similarities in densities of X. brevispina in canopy and soil litter suggest that both litter habitats share resources essential for this species. At this site, the density of all collembolans is significantly higher in the soil than in the canopy, because most collembolans other than X. brevispina live exclusively in soil (Yoshida and Hijii, 2005b). Microclimatic variability as indicated by mean monthly range of temperatures over the study period was greater in the canopy (9.4 1C) than in the soil (5.3 1C), and canopy litter may be a resource and a habitat less available to collembolans, other than X. brevispina. Since X. brevispina apparently has a high tolerance to desiccation and moves about actively (Itoh, 1991), the dominance of this species in the canopy could result from this species tolerating such larger variations in microclimate than other species. Alternatively, X. brevispina could utilize resources in the canopy less available to other species. On exposed habitats such as rocks and tree trunks, collembolans are likely have strategies for coping with drought (Leinaas and Sømme, 1984; Prinzing, 1997; Prinzing and Wirtz, 1997). Leinaas and Fjellberg (1985) reported that two collembolan species had different strategies for utilizing lichens
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Fig. 4. Seasonal changes in the relative abundance of Xenylla brevispina in (a) the canopy litter and (b) the soil litter in the Cryptomeria japonica plantation.
on exposed habitats: (1) a physiological adaptation to resist severe environmental conditions (staying strategy) and (2) an escape from such conditions by moving within or between habitats (migration strategy), X. brevispina may have the latter strategy. Our results suggest that X. brevispina is a species that can take advantage of the three-dimensional structure of the forest. Individuals in the canopy and those in the soil can, respectively, be considered as sink and source, because egg hatch apparently occurs in the soil, and individuals then disperse into the canopy. The density of all collembolans per unit litter mass was significantly larger in the soil than in the canopy (Yoshida and Hijii, 2005b) and, thus, competitions among them and/or with other detritivorous and fungivorous microarthropods may be stronger in the soil than in the canopy. Colonization by individuals born in the soil (source) into the canopy (sink) may have helped X. brevispina to avoid competition with other microarthropods in the soil, to expand its carrying capacity, and thus to become a predominant collembolan species in this forest. Presence of X. brevispina into the canopy also implies that this species influences the community
structures of arboreal arthropods. In the canopy of this forest, hunting spiders have frequently been observed to prey on collembolans. Collembolans are potential food resources for predators such as spiders (Wise, 1993, 2004), and those that migrate into the canopy from the soil could, therefore, be a subsidized food resource for arboreal predators (Winchester, 1997; Halaj et al., 2000) referred to as a ‘‘detrital infusion’’ (Polis and Strong, 1996). To better understand the functional roles of collembolans in food web and decomposition processes in both canopy and soil, further investigations are required on the ecological linkages between canopy and soil and dispersal of collembolans between these habitats (Bowden et al., 1976; Itoh, 1991; Ichisawa, 2001).
Acknowledgments We are grateful to Drs. R. Itoh and M.K. Hasegawa of Showa University, and to Dr. M.T. Hasegawa of the Forestry and Forest Products Research Institute, Kiso Experimental Station, for their useful suggestions on this manuscript. We
ARTICLE IN PRESS Xenylla brevispina in canopy and soil habitat thank Messrs. Y. Imaizumi and N. Yamaguchi and all the members of the Laboratory of Forest Protection, Nagoya University, for their helpful suggestions and support. This study was supported in part by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (no. 10660142).
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