Patch structure and ramet demography of the clonal tree, Asimina triloba, under gap and closed-canopy
Naomi HosakaÆNaoki KachiÆHiroshi KudohÆ Josef F. StueferÆDennis F. Whigham
Received: 29 October 2006 / Accepted: 18 October 2007 / Published online: 3 November 2007 ÓSpringer Science+Business Media B.V. 2007
Abstract Clonal understory trees develop into patches of interconnected and genetically identical ramets that have the potential to persist for decades or centuries. These patches develop beneath forest canopies that are structurally heterogeneous in space and time. Canopy heterogeneity, in turn, is respon- sible for the highly variable understory light environment that is typically associated with decid- uous forests. We investigated what aspects of patch
structure (density, size structure, and reproductive frequency of ramets) of the clonal understory tree, Asimina triloba, were correlated with forest canopy conditions. Specifically, we compared A. triloba patches located beneath closed canopies and canopy gaps. We also conducted a three-year demographic study of individual ramets within patches distributed across a light gradient. The closed canopy-gap comparison demonstrated that the patches of A. triloba had a higher frequency of large and flowering ramets in gaps compared to closed-canopy stands, but total ramet density was lower in gaps than in closed canopy stands. In the demographic study, individual ramet growth was positively correlated with light availability, although the pattern was not consis- tent for all years. Neither ramet recruitment nor mortality was correlated with light conditions. Our results indicate that the structure ofA. triloba patches was influenced by canopy condition, but does not necessarily depend on the responses of ramets to current light conditions. The lack of differences in ramet recruitment and mortality under varying canopy condi- tions is likely to be a primary reason for the long-term expansion and persistence of the patches. The primary benefit of a positive growth response to increasing light is the transition of relatively small ramets into flowering ramets within a short period of time.
Keywords Clonal growth Forest dynamics Forest understoryLight availability
Root sproutingSexual reproduction N. Hosaka (&)
Biodiversity Division, National Institute for Agro- Environmental Sciences, Tsukuba, Ibaraki 305-8604, Japan
e-mail: [email protected] N. Kachi
Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan
e-mail: [email protected] H. Kudoh
Department of Biology, Graduate School of Science, Kobe University, Nada-ku, Kobe 657-8501, Japan e-mail: [email protected]
J. F. Stuefer
Department of Ecology, Radboud University Nijmegen, Toernooiveld 1, 6525ED Nijmegen, The Netherlands e-mail: [email protected]
D. F. Whigham
Smithsonian Environmental Research Center, Edgewater, MA 21037, USA
e-mail: [email protected] DOI 10.1007/s11258-007-9372-z
Introduction
Forest canopies are structurally heterogeneous result- ing in an equally heterogeneous light environment on the forest floor (e.g., Brown and Parker 1994). The greatest contrast in light conditions in the forest understory is typically associated with areas beneath closed-canopies and areas beneath canopy gaps. Less than 10% of full daylight typically reaches the forest floor under a closed canopy in hardwood forests, while considerably higher amounts of light reach the ground level beneath canopy gaps (Schnitzler and Closset 2003; Beaudet et al. 2004). The appearance and closure of canopy gaps in forests adds a temporal component to variations in the light environment beneath the canopy. The average rate of gap open- ings, for example, has been estimated as much as 0.4%–1.3% of total area per year in temperate hardwood forests (McCarthy 2001; Henbo et al.
2004; Busing2005). Even small gap openings caused by death of a large branch or a single canopy tree generally increase light availability for understory plants but they are followed by gap closure within a decade (Beaudet et al. 2004). One consequence of temporally varying canopy structure is that under- story plants, especially long-lived species, experience a wide range of light environments during their lifetime and can vary their growth and reproduction (e.g., Kudoh et al.1999).
Many understory perennials are clonal and pro- duce patches of genetically identical offspring (ramets) that are connected horizontally (Kawano 1985; Klimesˇ et al. 1997; Whigham 2004). The production of patches of genetically identical indi- viduals often results in a reduction in the probability of death of genetic individuals (Eriksson and Jerling 1990; Eriksson 1993; Cain and Damman 1997).
Clonal understory trees, for example, have been shown to survive for decades or centuries (Cook 1983; Popp and Reinartz 1988; Kowarik 1995).
During the long lifespan of clonal understory trees, processes that influence patch development are likely to be influenced by the light conditions that individ- ual ramets experience, which in turn will vary temporally in responses to changing canopy conditions.
For example, shoot growth and sexual reproduc- tion of individual ramets of clonal plants are known to respond to the changes of light environments
(Ashmun and Pitelka1985; Popp and Reinartz1988;
Kowarik 1995; Wijesinghe and Whigham 1997;
Moola and Mallik 1998; Li et al.2001; Saitoh et al.
2002). These light-dependent responses of individual ramets may cause differences in some aspects of the clonal patch structure, such as size distribution of ramets and frequency of reproductive ramets. In contrast, recruitment and mortality of individual ramets have been reported to be less sensitive to light environments (Cain and Damman1997; Li et al.
2001; Levin and Feller 2004). Even shade-intolerant clonal trees such as Ailanthus altissima are able to persist in low-light habitats by continuing to produce ramets (Kowarik 1995). These conservative responses of ramets to light may cause only small differences in some aspects of patch structure, such as density and area of the clonal patches, between gap and closed-canopy stands of forests.
In this study, we examined patch structure and ramet dynamics of the understorey tree, Asimina triloba (L.) Dunal in habitats with varying light conditions. The goals of the study were, first, to determine which aspects of patch structures differ between the closed-canopy (low light) and gap (high light) conditions. The second goal was to quantify differences in within-patch dynamics of ramets in varying light conditions. We specifically addressed the following questions: (1) Does ramet density, size distribution, and the ratio of reproductive ramets to vegetative ramets differ between patches in closed- canopy and gap conditions? (2) Do differences in patch characteristics correspond with individual ramet performance (i.e., recruitment, mortality, growth, and sexual reproduction) under heteroge- neous light conditions?
Methods
Plant material and study sites
Asimina triloba (Annonaceae) is common under- growth of hardwood forests in the eastern North America and is distributed from northern Florida to southern Ontario (Kral 1960). A. triloba annually produces offspring ramets that arise on the horizontal root system of the parent plant (Karizumi1979). The size of ramets ranges from less than 0.3 m to more than 10 m in height (Larimore et al. 2003). Only
ramets that have a basal stem diameter of more than 18 mm produce flowers at the leaf axils of their current-year shoots (Willson and Schemske 1980).
Based on the number of tree rings at the ground level, ramets ofA. trilobahave ability to survive for at least 34 years (N. Hosaka, personal observation).A. triloba patches begin as a series of ramet generations originating from a single seed or groups of seeds;
patches thus may be composed of a single or multiple genotype. Patches of A. triloba occur in closed- canopy forest as well as in canopy gaps (Battaglia et al.1999).
We examinedA. trilobain hardwood forests in the Coastal Plain of Maryland, USA. Three study areas were selected in 50–100-year-old forests. One study area was the 1072-ha Patuxent Wildlife Research Center (PX site) (39°800N, 76°850W). At PX, we examined patches ofA.trilobain a floodplain forest that had developed on abandoned agricultural fields (Hotchkiss and Stewart1947).A trilobapatches in a floodplain forest were also examined at the Flag Pond Nature Park (FP site) (38°450N, 76°450W), a 132 ha area preserve operated as a county park (Maryland Department of Natural Resources 2003). The third study area was the 1133-ha Smithsonian Environ- mental Research Center (SI site) (38°530N, 76°330W), a research reserve including mature deciduous forests and successional forests that had developed on abandoned agricultural fields (Levine and Feller 2004). The forests at the three sites were dominated by Liriodendron tulipifera L., Fagus grandifolia Ehrh., Quercus alba L., Q. rubra L., and Acer rubrumL. The canopy height was typically 25–35 m at all sites.
Patch-level comparison
The structure ofA. trilobapatches was examined in a pair of forest stands at each of the three study sites.
One member of each pair was located in an area with no recent canopy disturbances, hereafter referred to as the closed-canopy stand. The other member of each pair was located beneath canopy gaps, referred to as the gap stand. In 2003, we established a 2,000 m2-rectangular plot in each stand. Each plot, centered on a spatially continuous group ofA. triloba patches, was subdivided into twenty 10910 m subquadrats. In all plots, A. triloba patches were
often intermingled without distinctive boundaries;
therefore we characterized the patch structure per area bases rather than per patch bases. The numbers of reproductive and vegetative ramets were counted in each subquadrat. To estimate ramet-size distribu- tions, we measured the basal diameters at 3 cm above the ground in the end of the 2004-growing season (late September to early October) for 15% of the total number of ramets in the plot.
To quantify canopy conditions, we measured the diameter of all canopy trees (DBH, in cm) in each subquadrat and converted the diameter data to total basal area (TBA, in cm2) per plot. Photosynthetically active radiation (PAR, in lmol/m2/s) was measured in the centre of each subquadrat using a point quantum sensor (LI-190SA or LI-190SB, LICOR, Lincoln, USA) set at the height of the tallestA. triloba ramet (3–15 m) using a tall telescopic pole. Relative PARs were calculated against reference PARs. At the SI site, reference PAR was measured at the top of a 50-m high canopy tower. At the FP and PX sites, reference PAR was measured in open areas adjacent to the study plots. All measurements were taken when the sky was overcast during August and September 2004.
Ramet-level comparison
The demography of individual ramets along a light gradient was measured over a three-year period (2001–2004) at the SI site. We chose nineA. triloba patches that had clear boundaries and were located in areas of the forest with different light conditions.
Each patch had a single large reproductive ramet (a putative parent plant) and a number of smaller ramets (5–64 small ramets per patch). The sizes of individual patches ranged from 3.3 to 32.7 m2in 2001.
All individual ramets in the nine patches were tagged in June 2001 and annually censused between July and September of 2001, 2002, 2003, and 2004.
For each ramet, we measured stem height and basal diameter at 3 cm above the ground and counted the numbers of branches (current-year shoots) and flower buds. A ramet was regarded as dead if all above- ground parts were missing or if the ramet had no leaves during the growing season. Mortality rate was calculated as the number of dead ramets divided by the total number of ramets recorded in the previous
year. New ramets, which had been recruited in the patches were distinguished from seedlings by exam- ining connections to the horizontal root system through careful hand excavation, and were measured in the same manner as the older ramets. Ramet recruitment rate was calculated as the number of new ramets divided by the total number of ramets recorded in the previous year. For each ramet, a relative growth rate (RGR) was calculated as the difference in ln- transformed ramet diameter at two censuses divided by the time difference between those censuses.
The light environments of the nine patches were evaluated by analyzing hemispherical canopy photo- graphs. The photographs were taken with a digital camera (CoolPix 960, Nikon, Tokyo, Japan) equipped with a fish-eye lens (FC-E8, Nikon, Tokyo, Japan) that was horizontally mounted over the tallest ramet in each patch. All photographs were taken while the sky was overcast in August 2002, and then analyzed with a software program, Hemiview 2.1 (Delta-T Devices, Cambridge, UK). In the software, diffuse light transmission was calculated as ISF that repre- sented the proportion of PAR transmitted through the canopy. No large-scale qualitative change of canopy structure was observed above the nine patches during the study period; thus the data collected in 2002 was representative of the diffuse light transmission during the three-year study period (2001–2004).
Statistical analysis
All data were analyzed using the SAS System for Windows (v8, SAS Institute Inc., Cary, USA).
Wilcoxon rank-sum tests were performed to test differences between closed-canopy and gap stands in the properties of forest canopies (the number, mean diameter at breast height, and total basal area of the canopy trees), the relative PARs of understories, and the abundance of A. triloba (the frequency of reproductive and vegetative ramets and the ratio of reproductive ramets) (PROC NPAR1WAY).
Kolmogorov–Smirnov two-sample tests were used to test differences in ramet size distribution between the closed-canopy and gap stands for each site (PROC NPAR1WAY). The probability levels of the above tests (P\0.05) were set at the site-wise level by the sequential Bonferroni method. Pearson corre- lation coefficients were calculated between diffuse
light transmission and parameters of ramet demogra- phy (the recruitment rate, mortality rate, diameter RGR, height growth, branch number increment, and flower bud production) for the periods of 2001–2002, 2002–2003, and 2003–2004, separately (PROC CORR). Pearson correlation coefficients were also calculated between the initial patch size in 2001 (total number of ramets) and the above-mentioned param- eters of ramet demography for the periods of 2001–
2002, 2002–2003, and 2003–2004, separately (PROC CORR). The probability levels of the tests on ramet demography (P\0.05) were set at the parameter- wise level by the sequential Bonferroni method.
Results
Patch-level comparisons
The densities of canopy trees were significantly higher in the closed-canopy plots for FP and PX sites (Table 1). No statistical differences in mean DBH were detected between the closed-canopy and gap plots for any of the sites, even though the means were always greater in gap sites (Table 1). Total basal area of the canopy trees was generally higher in the closed canopy plots, but statistical differences were not detected across the three sites (Table 1). Relative PARs were significantly higher in the gap plots for the FP and SI sites but not for the PX site (Table1).
The total number of ramets per plot varied between 506 and 7924 ramets and ramets were present in all 20 subquadrats at the FP site. In contrast, ramets were not present in some of the subquadrats at the SI and PX sites (Table1). At the FP site, a significantly greater number of reproductive ramets, a lower number of vegetative ramets, and fewer total ramets were found in the gap plot (Table 1). At the SI and PX sites, the numbers of ramets did not differ significantly between the plots for either reproductive or vegetative ramets (Table 1). The mean number of flowering ramets was relatively low in all plots, ranging from 0.06 to 15.4% of the total number of ramets (Table1). The ratio of flowering to vegetative ramets was generally higher in the gap plots, but a statistical difference was detected only at the FP site (Table1).
The size distribution of A. triloba ramets was skewed toward larger size classes in the gap plots at
Table1Forestcanopyconditions(thenumber,meandiameteratbreastheight,andtotalbasalareaofthecanopytrees),relativePARs,andclonalpatchstructureofAsimina triloba(thenumberofsubquadratswithA.trilobaramets,thenumbersofreproductiveandvegetativeramets,totalrametdensity,andtheratioofreproductiveramets)inthegap andclosed-canopystandsatthethreestudysites(FP,SI,andPX)inMaryland,USA VariablesFPSIPX GapClosed-canopyZGapClosed-canopyZGapClosed-canopyZ Forestcanopycondition #Canopytrees/100m2a 4.1(0.5)8.5(0.9)-3.6***8.7(0.8)8.4(0.6)-0.013.8(0.7)6.1(0.7)-2.5* MeanDBH(cm)a25.7(2.4)21.7(2.3)1.420.1(1.3)19.3(1.1)0.2323.9(2.9)21.6(2.9)0.6 TBA(cm2)a3699(606)5647(684)-1.94080(486)5034(538)-1.23559(1086)3728(664)-0.8 RelativePAR(%)a 17.19(1.43)5.36(1.00)4.6***13.00(2.43)2.82(0.41)4.9***12.06(3.30)7.84(1.34)0.6 PatchstructureofA.triloba SubquadratswithA.triloba20201982018 #Reproductiveramets/100m2b 13.2(1.2)1.9(0.9)4.8***1.3(0.4)0.4(0.4)-1.43.1(0.7)2.7(0.8)-0.3 #Vegetativeramets/100m2b 236.8(24.3)394.0(44.9)-2.7***71.4(17.2)95.4(68.0)-1.422.3(4.2)49.8(11.9)1.3 Totalrametdensity/100m2b250.0(24.1)395.9(45.0)-2.5*72.7(17.6)95.8(68.4)-1.525.3(4.2)52.5(11.9)1.2 %Reproductiveramets/100m2b6.6(1.3)0.5(0.2)5.1***2.3(1.3)0.06(0.06)-1.615.4(4.4)7.1(2.7)-1.0 Means(standarderrors)werecalculatedfortheforeststandsbasedoneitherathevaluesobtainedfromall10910msubquadratsintheplot(n=20)orbthevaluesobtainedfrom subquadratswhereA.trilobawaspresent(n=8–20).Asterisksindicatestatisticallysignificantdifferencesbetweengapandclosed-canopystandswithineachstudysite(*,**, and***forP\0.05,0.01,and0.001,Wilcoxonrank-sumtestsfollowedbysequentialBonferronicorrection)
all three sites (Fig.1). The size distributions differed significantly between the plots at the PF and SI sites (Kolmogorov–Smirnov two-sample tests; D= 0.31 and 0.27; P\0.0001 and \0.0001, respectively) while a statistical significance was not detected at the PX site (D= 0.076, p = 0.934). Minimum ramet sizes were similar between the two types of plots
within the study sites, but the maximum ramet sizes were greater in the gap plots (99, 51, and 141 mm in basal stem diameter for FP, SI, and PX sites, respectively) compared to closed-canopy plots (38, 18, and 116 mm in diameter for FP, SI, and PX sites, respectively).
Ramet-level comparison
Ramet recruitment was annually observed in the nine patches at the SI site and the total number of ramets increased through the three-year study period. Most of the new ramets that appeared in the patches (173 of 182 in total) survived until the end of the 2004- growing season. Ramet mortality rate was low (mean across the nine patches=0.03, 0.04, and 0.001 for 2001–2002, 2002–2003, and 2003–2004 periods, respectively) compared with ramet recruitment rate (0.31, 0.28, and 0.14 for 2001–2002, 2002–2003, and 2003–2004, respectively). Neither the mortality rate nor the recruitment rate showed significant correla- tions with light conditions of the patches (Table2, Fig.2a). There were also no significant correlations between ramet recruitment rates and the initial size of the patches (Table2). Only ramet mortality rates during the period 2002–2003 showed positive corre- lations with the initial size of the patches (Table2).
On the other hand, parameters related to ramet growth varied with light conditions. The mean values of RGR, absolute height growth, and increment in the number of branches were all positively correlated with diffuse light transmission during the period 2001–2002 (Table 2, Fig.2b). The number of flower buds produced by the reproductive ramets in 2002 and 2004 also showed positive correlation with diffuse light transmission (Table2). Correlations between these parameters and diffuse light transmis- sion were not significant for the rest of the study period. No significant correlations between the same parameters of ramet growth and initial patch size were detected for the entire study period (Table 2).
Discussion
Approximately 31% of North American tree species are known to produce root sprouts and their functions have been studied in relation to recovery from injury Fig. 1 Comparison of ramet size structure ofAsimina triloba
between gap (open bars) and closed-canopy (hatched bars) stands at the (a) FP, (b) SI, and (c) PX sites. The value of thex- axis represents the lower limit of each size class in basal stem diameter of ramets. The result of Kolmogorov–Smirnov two sample test is shown in each plate with *** (\0.0001) or ns ([0.05) ofP-value
(Del Tredici 2001). However, as observed in A. triloba, root suckering is rather common mode of new ramet production among clonal trees (Klimesˇova´ and Klimesˇ 2004). They tend to form clonal patches that persist for more than decades (Cook 1983; Popp and Reinartz 1988; Kowarik 1995). During the long period of time thatA. triloba patches develop beneath forest canopies, they are likely to be influenced by factors associated with changes in the structure of the forest canopy. Our data clearly demonstrate that differences in patch charac- teristics were associated with the forest canopy conditions, with statistically significant differences in several measured characteristics between closed- canopy and gap stands. Some of these differences can be explained by differences in the light regimes of gap and non-gap stands, but others did not necessarily correspond with the light environments.
At the FP and SI sites, ramet-size distribution was skewed toward larger sizes in the gap stands where relative PARs were significantly greater than those in the closed-canopy stands. Similar patterns have been reported for other clonal understory trees (Huffman 1997; Pancer-Koteja et al. 1998; Kanno and Seiwa 2004). High light condition is expected to enhance individual ramet growth and cause a shift in size distribution toward larger sizes. In our demographic study, ramet growth was positively correlated with the light availability, although the dependency was not necessarily strong during the three-year study period.
Previous experimental studies on clonal plant species have also shown that shoot growth of ramets are enhanced in response to the change of light from closed-canopy to gap levels (Ashmun and Pitelka1985;
Table 2 Correlation coefficients (r) calculated for demographic parameters ofA. trilobaramets against light conditions (diffuse light transmission) and patch size (initial number of ramets) for nine patches at the SI site
Variable Diffuse light transmission Initial number of ramets
2002 2003 2004 2002 2003 2004
Recruitment rate 0.58 0.65 -0.13 -0.02 -0.13 0.14
Mortality rate -0.27 -0.14 – 0.70 0.78* –
Diameter RGR 0.79* 0.39 0.61 -0.14 -0.20 -0.12
Height growth 0.89** 0.68 0.32 -0.09 -0.22 -0.26
Branch inclement 0.90** 0.75 0.37 -0.19 -0.17 -0.12
Flower bud production 0.82** – 0.67 -0.02 – 0.11
Asterisks indicate significant correlations (* and ** forP\0.05 and 0.01, Pearson correlation followed by sequential Bonferroni correction). Mortality rate during 2003–2004 was not calculated because only one ramet had died in this period. The number of flower buds was not recorded in 2003
Fig. 2 (a) The recruitment rate of ramets and (b) the mean relative growth rate in basal stem diameter for the nine patches at the SI site along a gradient light availability in diffuse light transmission. Different symbols represent different years: 2002 (circle), 2003 (triangle), and 2004 (diamond)
Wijesinghe and Whigham 1997; Moola and Mallik 1998; Li et al. 2001; Saitoh et al. 2002). Greater shoot growth of individual ramets may contribute to the higher ratio of reproductive ramets of A. triloba under gap conditions by increasing the number of ramets that exceed the reproductive threshold.
Indeed, the presence of size threshold for reproduc- tion has been reported in A. trilobaramets (Willson and Shemske1980). Reduced sexual reproduction in clonal herbs, shrubs, and understory trees is fre- quently observed in low light environments (Ashmun and Pitelka1984; Kowarik 1995; Moola and Mallik 1998; Li et al. 2001; Levin and Feller 2004; Kanno and Seiwa 2004), but this may simply reflect the effects of the small size and poor vigor of ramets that could result from light limitation in closed-canopy stands (Hartnett1990).
All aspects of clonal patch structures ofA. triloba were not necessarily explained by current light regimes. Total ramet density tended to be higher in closed-canopy compared to gap patches, and the difference was statistically significant at the FP site.
This can not be readily explained by the results of ramet demography in which mortality and recruit- ment rates showed no correlations with light environments. Several other studies also reported that recruitment and mortality of ramets were incon- sistent with light environments (Cain and Damman 1997; Li et al. 2001; Levin and Feller 2004). In clonal woody and even herbaceous species, it has been reported that belowground parts of ramets responded slowly or did not respond at all to short- term changes of light (Wijesinghe and Whigham 1997; Moola and Malik 1998; Li et al. 2001; Saitoh et al. 2002). Although light is one of the most prominent differences when environments were com- pared between gap and closed-canopy within the forests (Montgomery and Chazdon 2001; Nicotra et al. 1999), other factors, such as soil moisture, nutrients, and temperature, provide heterogeneous conditions in a forest (Guo et al.2002,2004; Ga´lhidy et al.2006). These factors are known to be common growth regulators of root buds (Peterson 1975;
Klimesˇ and Klimesˇova´ 1999; Frey et al.2003), and may explain ramet demography of A. triloba, and possibly other root-suckering clonal trees, which are likely to have distinctive root functions and ramet regulations from those non-root-sprouting plants (Guerrero-campo et al.2006).
We observed differences in patch structures of A. triloba among the three study sites, although we did not explicitly analyze the variation between the sites. Past history of the forests, such as land-use before forest development and the extent of damages caused by stochastic disturbances, may have influ- enced the structure of A. triloba patches. For example, large storms or hurricanes, can simulta- neously damage canopy trees and understorey vegetation (Webb 1989; Pascarella1998). This type of large-scale disturbance may result in a positive correlation between forest structure and abundance of A. triloba. Indeed, in an old-growth forest of South Carolina, Battaglia et al. (1999) found that ramet density ofA. trilobawas lower in the area with severe damage of canopy trees after the hurricane Hugo. The pattern is consistent with the positive association between canopy cover and total ramet density found in our study. In the past 50 years, two hurricanes have struck our study sites (National Climatic Data Center 2007). Especially for the long-lived clonal woody plants, including A. triloba, rare large-scale distur- bances may considerably modify the developmental process and the structure of clonal patches.
Our results showed that the sexual reproduction of A. trilobalocalize in space, and probably in time, to gap stands where light resource is abundant. This localized sexual reproduction does not seem to restrict the spatial distribution of A. triloba within forests. Fleshy fruits of A. triloba are dispersed by small mammals (Cypher and Cypher 1999) and seedlings are distributed widely within forests (Battaglia et al. 1999). Seeds of A. triloba are sensitive to desiccation throughout the germination process (Finneseth et al. 1998; Pomper et al. 2002), therefore closed canopy conditions may provide safe sites for seedling establishments. In our study, we observed high recruitment rate of ramets (24.4% on average) far exceeding the mortality rate (2.4% on average). These results clearly demonstrate that the patches ofA. trilobaare able to increase the number of ramets even under closed-canopy conditions once they are established. Augspurger et al. (2005) also reported that A. triloba express high photosynthesis even under fully closed forest canopy. This ability to persist and accumulate resources in low light condi- tions has been demonstrated in other understory plants, including a clonal understory herb (Noda et al.
2004), a bamboo (Lei and Koike1998), an understory
palm in a tropical rain forest (Mendoza and Franco 1998), and the non-native Ailanthus altissima in a West Virginia deciduous forest (Kowarik1995). The advantages of increased ramet density under a range of light conditions assure long-term persistence (Cook 1983; Damman and Cain 1998; Jo´nsdo´ttir et al.2000) as well as continuous increases in stored resources that allow the patches to respond rapidly to increases in light following canopy gap opening.
Considering the patch structure and ramet dynam- ics under different canopy conditions, we speculate thatA. trilobaadopts a ‘sit-and-wait’ strategy, which is characterized by spontaneous clonal growth and localized reproduction in short-time optimal condi- tions (Hosaka et al. 2005). Although this type of strategy seems to be rather common among other clonal understory herbs and trees inhabiting old- growth hardwood forests (Ashmun and Pitelka1984;
Kudoh et al. 1999; Kanno and Seiwa 2004), it has been demonstrated in only a few clonal woody species growing in the understory of forest canopies (Popp and Reinartz 1988; Kowarik 1995). The physiological characteristics of clonal understory woody species especially needs further examination as the degree of resource sharing between sibling ramets or between parent-offspring ramets remains unknown.
Acknowledgments This research was supported by a Pre- doctoral Fellowship to Naomi Hosaka from the Smithsonian Environmental Research Center. We thank Takashi Tani and Jun-ichirou Suzuki for constructive comments on earlier versions of the manuscript; Geoffrey G. Parker, Catherine E.
Lovelock, and Ilka C. Feller for technical support for the field measurements; Dwight Williams and Richard S.
Hammerschlag for the guidance in the study sites. We are very grateful to Jay O’Neill, Sara Go´mez, Laura Dietrich, Dawn Miller, and Reginald Reid for invaluable field assistance.
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