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. 2006 Jul;98(1):219–226. doi: 10.1093/aob/mcl091

Shoot Development and Extension of Quercus serrata Saplings in Response to Insect Damage and Nutrient Conditions

ERI MIZUMACHI 1,*, AKIRA MORI 1,2, NAOYA OSAWA 1, REIKO AKIYAMA 1, NAOKO TOKUCHI 3
PMCID: PMC2803554  PMID: 16709576

Abstract

• Background and Aims Plants have the ability to compensate for damage caused by herbivores. This is important to plant growth, because a plant cannot always avoid damage, even if it has developed defence mechanisms against herbivores. In previous work, we elucidated the herbivory-induced compensatory response of Quercus (at both the individual shoot and whole sapling levels) in both low- and high-nutrient conditions throughout one growing season. In this study, we determine how the compensatory growth of Quercus serrata saplings is achieved at different nutrient levels.

• Methods Quercus serrata saplings were grown under controlled conditions. Length, number of leaves and percentage of leaf area lost on all extension units (EUs) were measured.

• Key Results Both the probability of flushing and the length of subsequent EUs significantly increased with an increase in the length of the parent EU. The probability of flushing increased with an increase in leaf damage of the parent EU, but the length of subsequent EUs decreased. This indicates that EU growth is fundamentally regulated at the individual EU level. The probabilities of a second and third flush were significantly higher in plants in high-nutrient soil than those in low-nutrient soil. The subsequent EUs of damaged saplings were also significantly longer at high-nutrient conditions.

• Conclusions An increase in the probability of flushes in response to herbivore damage is important for damaged saplings to produce new EUs; further, shortening the length of EUs helps to effectively reproduce foliage lost by herbivory. The probability of flushing also varied according to soil nutrient levels, suggesting that the compensatory growth of individual EUs in response to local damage levels is affected by the nutrients available to the whole sapling.

Keywords: Quercus serrata, extension units, compensation, soil fertility, herbivore, sapling, rhythmic growth, flush, leaf damage

INTRODUCTION

Plants have several different compensatory responses to herbivore damage. They may enhance leaf-level photosynthetic activity, increase their relative growth rate or activate the growth of meristems (e.g. Rosenthal and Kotanen, 1994; Strauss and Agrawal, 1999; Tiffin, 2000; Nykänen and Koricheva, 2004). Such compensatory responses are affected by abiotic and biotic factors such as water availability, soil nutrients and competition among plants (e.g. Maschinski and Whitham, 1989; Rosenthal and Kotanen, 1994; Strauss and Agrawel, 1999). Among these factors, soil nutrient availability is important for understanding compensatory responses, because nutrient levels determine biomass production and shoot growth patterns (e.g. Harmer, 1989; Berger and Glatzel, 2001) as well as foliage quality (e.g. Forkner and Hunter, 2000; Berger and Glatzel, 2001). A change in foliage quality could influence a herbivore's ovipositing and feeding preferences (Lower et al., 2003). Soil nutrient availability is therefore expected to influence the compensatory response of a plant by both modifying its growth and changing the intensity of herbivore attack.

Many studies have evaluated the effects of soil nutrient availability on compensatory responses of herbaceous plants to herbivore damage (e.g. Maschinski and Whitham, 1989; Meyer, 2000). However, for woody plants, information on their herbivory-induced responses at different nutrient availabilities has been limited, mainly due to the difficulty in estimating compensatory responses through their long life spans. Hawkes and Sullivan (2001) showed that there are qualitative differences between herbaceous plants and woody plants in response to herbivory. Therefore, it is important to elucidate the possible effects of nutrient condition on herbivory-induced compensatory responses in woody plants.

Woody plants form complex branching structures by repeatedly producing shoot units (White, 1979). These units act semi-autonomously; resources within an individual plant may be restricted to local use (Watson, 1986; Sprugel et al., 1991). Several studies have investigated resource autonomy by documenting the responses of plants to artificial defoliation (Tuomi et al., 1988; Haukioja et al., 1990; Honkanen and Haukioja, 1994; Honkanen et al., 1999). These studies showed that herbivory-induced responses of plant units such as ramets or branches could also be local, which suggests that plant modularity is a fundamental factor in the way that woody plants respond to herbivore damage. Identifying the responses of woody plants to herbivore damage based on each plant unit would further enhance our knowledge about plant–herbivore interaction.

Quercus saplings show rhythmic growth, i.e. they produce several growth flushes per growing season (e.g. Borchert, 1975). The number of flushes varies according to environmental factors, including soil nutrient availability (Hanson et al., 1986; Collet and Frochot, 1996; Charr et al., 1997a, b). The portion of a shoot that elongates during one flush is regarded as a unit of the whole plant and is termed an extension unit or growth unit (hereafter represented by EU for extension unit). Several studies have used EUs for various analyses (e.g. Charr et al., 1997a, b; Heuret et al., 2003; Mizumachi et al., 2004). Many studies have suggested that the properties of EUs produced during subsequent higher flushes in Quercus are influenced by both abiotic and biotic factors of parent shoots produced earlier in the season (e.g. Harmer, 1989; Charr et al., 1997b). These characteristics of rhythmic growth of Quercus saplings may play an important role for its compensative growth patterns.

We previously demonstrated that Quercus serrata saplings could fully compensate for herbivore damage by changing their shoot growth pattern, i.e. herbivore-damaged saplings could achieve shoot production nearly equivalent to that of undamaged saplings within one growing season at whole sapling level (Mizumachi et al., 2004). We also showed that these responses might increase under conditions of high nutrient availability, even when the intensity of herbivory is severe (Mizumachi et al., 2004). However, we could not show how each individual EU responds to herbivore damage and soil nutrient availability. It is also important to quantify the responses of individual EUs because individual EUs are expected to act semi-autonomously.

In this study, we analysed the responses of daughter EUs in relation to parent EUs to examine in detail the responses of EUs to various levels of herbivore damage and soil nutrient availability in Q. serrata. The objective of this study is to determine how the compensatory growth of Q. serrata saplings is achieved from the viewpoint of plant modularity.

MATERIALS AND METHODS

Experimental plants

In December 2001, a group of 120 Q. serrata Thunb. Ex Murray saplings were acquired from Kutsuki Village Forest Association. The roots of each plant were washed to remove any remnants of soil, and then each sapling was transplanted into plastic pots (44 cm in diameter, 24 cm in depth) containing 500 cm3 of kamuma soil (pumice) at the bottom; the remainder of each pot was filled with sand. The saplings were grown in two plastic greenhouses at the Kitashirakawa Experimental Station of Kyoto University in Kyoto (35·02 °N, 135·47 °E), Japan. Average annual temperature is 15·9 °C (Field Science Education and Research Center, Kyoto University). The temperature and the light conditions in these greenhouses were not manipulated. All saplings were watered to saturation for 10 min daily by an automatic sprinkler (Sprinkler Thinker DC-1, Irrigation Control Equipment, Galcon®). Bud-break at the first flush occurred in early April 2002. The mean sapling heights were then 43·4 ± 0·4 cm (mean ± s.e.). Sapling height did not differ significantly among the treatments (Scheffé's range test, P > 0·05). During the growing season, most of the saplings had more than one flush. The bud-break at the last flush occurred in early October 2002.

Experimental design

The experiment tested Q. serrata sapling responses to herbivore damage and soil fertility. The experiment was conducted in two plastic greenhouses (House 1, 10 × 7·5 m, 4 m in height; House 2, 9·5 × 4·4 m, 3·5 m in height). These two greenhouses were built on the same site and the distance between these two greenhouses was within 25 m. We have treated the data of the two greenhouses equally for analyses. Nylon mesh (1 mm × 1 mm) divided each plastic greenhouse into two separate blocks; a herbivore-damaged and a herbivore-undamaged block. The three non-boundary sides of the herbivore-damaged blocks were made of 20 mm × 20 mm nylon mesh to allow insect herbivores free access to the plants. Therefore, the saplings in these blocks were damaged naturally by insect herbivores. The leaf damage at this experimental station was caused mainly by generalist insect herbivores such as the larvae of Lepidoptera (families: Oecophoridae, Timyridae, Noctuidae, Geometridae, Lymantriidae and Arctiidae), Hymenoptera (family Tenthredinidae), and adult Coleoptera in the families Attelabidae and Scarabaeidae (H. Ishii and N. Osawa, unpubl. data). In the herbivore-undamaged blocks, the three non-boundary sides were made of 1 mm × 1 mm mesh to exclude insect herbivores. This mesh size effectively reduced herbivore damage (leaf area loss in undamaged blocks was <3 %), although a few insect invasions did occur. For that reason, we checked all saplings in the herbivore-undamaged blocks every 2 d to remove any invasive insects. The saplings in each block were assigned to different fertilization treatments (low- and high-nutrient soil), and the pots were arranged in random order with respect to the fertilization treatments. Fertilizer was applied as 25 : 5 : 20 (N : P : K) (Peters Professional, HYPONeX JAPAN®) every 2 weeks from April to November 2002. The concentration of fertilizer was adjusted to the two levels of soil fertility: half of the saplings in each block were grown under low soil fertility (20 kg N ha−1 year−1) and half were grown under high soil fertility (200 kg N ha−1 year−1). Tokuchi et al. (1999) showed that the annual fluxes of inorganic nitrogen in a temperate forest in Japan are approx. 20 kg N ha−1 year−1 at the plot of relatively low nutrient availability and these values could vary greatly with topographic conditions. Therefore, the level of low soil fertility was decided by the value, and, for high soil fertility level, we increased the level by ten. The Q. serrata saplings were randomly assigned to four treatments (i.e. low and high soil fertility in damaged blocks, and low and high soil fertility in undamaged blocks); 40 saplings were submitted to each treatment.

Measurements

Quercus saplings may flush several times during one growing season. An EU is defined as the portion of a shoot that elongates during one flush. The EUs formed during the first flush in April were defined as ‘the first EUs’. The EUs formed subsequent to the first EUs were defined as ‘the second EUs’. Similarly, any subsequent EUs were defined as ‘the third EUs’, ‘the fourth EUs’ and ‘the fifth EUs’.

A two-dimensional diagram was drawn to illustrate the branching structure of each sapling when new shoots elongated during the growing season. Each EU was numbered on the diagram, so it was possible to determine which parent EUs produced subsequent daughter EUs. For each EU, we measured its length and number of leaves after elongation. Leaves of the EUs had finished growing between early May and early October 2002. At the same time, all leaves of the EUs were roughly categorized into one of seven classes based on leaf damage, which was determined visually by estimating the percentage of leaf area loss. We estimated and classified area loss for each leaf using the following percentages for each leaf damage class: 0, 0 %; 1, 2·5 %; 2, 15 %; 3, 30 %; 4, 62·5 %; 5, 87·5 %; 6, 100 %. Leaf damage (D) for each EU was calculated as an average value of these percentages.

Data analysis

The lengths of the first EU (L1st), the second EU (L2nd) and the third EU (L3rd) were analysed by two-way analysis of variance (ANOVA) with two between-subjects factors (herbivore damage and soil fertility). Student's t-test was performed for comparison among four treatments. The length of EUs was log transformed. The length of the fourth EU and the fifth EU was not tested, because there was not an adequate number of EUs to test in these flush stages (Table 2). The leaf damage of EUs (D1st, D2nd, D3rd, D4th and D5th) was analysed with Wilcoxon rank sum test under low and high soil fertility.

Logistic regression analyses were performed separately for herbivore-damaged and undamaged saplings. For the damaged saplings, the probability of a subsequent flush was regressed by two numerical factors (length and leaf damage of parent EU) and one categorical factor (soil fertility). For the undamaged saplings, the probability of a subsequent flush was regressed on one numerical factor (length of parent EU) and one categorical factor (soil fertility).

Multiple regression analyses were performed separately for the herbivore-damaged and the undamaged saplings. For the damaged saplings, the length of daughter EU was regressed on two numerical factors (length and leaf damage of parent EU) and one categorical factor (soil fertility). For the undamaged saplings, the length of daughter EU was regressed on one numerical factor (length of parent EU) and one categorical factor (soil fertility). The relationship between the fourth and fifth EUs was not tested, because the undamaged saplings had few fifth EUs (Table 2). In this multiple regression, we treated the apical EU produced on the parent EU as a daughter EU. The length and the leaf damage of EU were log and arcsine transformed, respectively.

The relationships between leaf number and length of individual EUs was assessed by linear regressions of the form ln y = a + b ln x, where x is the length of an EU and y is the leaf number of the EU, and a and b are specific parameters determined from reduced major axis (RMA) regression (Niklas, 1994). The regression was performed for each flush stage and each treatment. The relationship at the fourth EUs in undamaged saplings under low soil fertility was not tested, because there were not enough EUs to test in this category (Table 1). The test was performed with the (S)MATR program version 1.0 (Falster et al., 2003). All statistical analyses except for the RMA regressions were performed with JMP version 5.1.1 (SAS Institute, 2004).

Table 1.

The results of two-way ANOVA comparing the length of EUs

d.f. F P
1st EU
    Herbivore damage 1 1·433 0·2315
    Soil fertility 1 0·759 0·3839
    Interaction 1 9·062 0·0027
    Error 1495
2nd EU
    Herbivore damage 1 66·344 <0·0001
    Soil fertility 1 1·083 0·2984
    Interaction 1 5·098 0·0243
    Error 631
3rd EU
    Herbivore damage 1 51·230 <0·0001
    Soil fertility 1 4·070 0·0445
    Interaction 1 1·290 0·2569
    Error 314
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The lengths of EUs were log transformed.

RESULTS

The basic data of EUs

Soil fertility significantly affected the leaf damage of the second EU (D2nd) (Table 2), while soil fertility did not affect D1st, D3rd, D4th and D5th (Table 2).

Table 2.

Number, mean length (± s.e.) and mean leaf area loss (±s.e.) of EUs produced each flush in Q. serrata saplings subjected to herbivore damage at various soil nutrient levels

Damaged block
 Undamaged block
Low High Low High
1st EU
    Number 342 366 421 373
    Length (mm) 61·1 ± 2·5a 55·3 ± 2·6b 54·7 ± 2·0ab 62·8 ± 2·4a
    Leaf damage (%) 15·5 ± 1·1a 17·5 ± 1·2a – –
2nd EU
    Number 167 211 63 201
    Length (mm) 47·8 ± 3·1c 65·7 ± 3·8b 97·8 ± 6·4a 97·5 ± 4·5a
    Leaf damage (%) 14·5 ± 1·8b 23·0 ± 2·1a – –
3rd EU
    Number 66 151 22 81
    Length (mm) 68·8 ± 7·0c 89·9 ± 5·7b 133·1 ± 9·1a 176·9 ± 10·9a
    Leaf damage (%) 40·6 ± 4·0a 46·4 ± 2·6a – –
4th EU
    Number 31 122 1 27
    Length (mm) 68·0 ± 8·5 83·6 ± 5·7 203·0 212·7 ± 19·7
    Leaf damage (%) 42·5 ± 5·1a 51·3 ± 2·8a – –
5th EU
    Number 7 40 – 1
    Length (mm) 32·4 ± 8·5 77·8 ± 11·1 – 138·2
    Leaf damage (%) 64·0 ± 11·7a 52·8 ± 5·5a – –
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The different letters for length are significantly different by Student's t-test (P < 0·05).

The different letters for damage are significantly different by Wilcoxon rank sum test (P < 0·05).

Herbivore damage did not affect the length of the first EU (L1st), while herbivore damage significantly affected L2nd and L3rd (Table 1). L2nd and L3rd in damaged saplings were significantly shorter than those in undamaged saplings (Table 2). Soil fertility affected L3rd, but did not affect L1st and L2nd (Table 1). Multiple comparisons showed that, for the damaged saplings, L2nd and L3rd under high soil fertility were longer than those under low soil fertility (Table 2).

The probability of subsequent flushes

In the logistic regression analyses of the damaged saplings, the three independent variables had significant effects on the probabilities of second and third flushes (Table 3). The probability of a second flush significantly increased with increasing L1st and D1st, and when soil fertility (FS) was high (Table 3). Similarly, the probabilities of third and fourth flushes significantly increased with increasing L2nd and L3rd and leaf damage of the second (D2nd) and third (D3rd) EUs (Table 3). The probability of a third flush increased when FS was high, but the probability of a fourth flush did not (Table 3). In the logistic regression analyses of the undamaged saplings, the two independent variables also had significant effects on the probability of a second flush (Table 3). The probability of a second flush increased with increasing L1st and FS (Table 3). The probability of a third flush was significantly influenced by L2nd but not by FS (Table 3). Neither L3rd nor FS significantly affected the probability of a fourth flush (Table 3).

Table 3.

The results of logistic regression analysis for the probability of subsequent flush vs. length (L) and leaf damage (D) of parent EU, and soil fertility (FS)

Treatment Flush stage Independent variables B s.e. Wald χ2 Exp(B)
Damaged 2nd L1st 0·017 0·002 69·348**** 1·017
D1st 2·365 0·387 37·443**** 10·644
FS 0·193 0·085 5·207* 1·213
Constant −1·546 0·156 98·090****
3rd L2nd 0·022 0·003 50·274**** 1·022
D2nd 1·547 0·450 11·825*** 4·697
FS 0·326 0·122 7·178** 1·385
Constant −1·682 0·223 57·280****
4th L3rd 0·011 0·003 13·804*** 1·011
D3rd 2·242 0·522 18·449**** 9·412
FS 0·296 0·172 2·972+ 1·344
Constant −1·913 0·347 30·450****
Undamaged 2nd L1st 0·032 0·003 141·671**** 1·033
FS 0·826 0·105 61·435**** 2·284
Constant −3·233 0·223 209·960****
3rd L2nd 0·024 0·003 53·149**** 1·024
FS −0·025 0·174 0·021 –
Constant −3·112 0·396 61·630****
4th L3rd 0·003 0·003 1·069 –
FS 0·968 0·531 3·325+ 2·633
Constant −2·427 0·666 13·280***
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Significant levels: +P < 0·1; *P < 0·05; **P < 0·01; ***P < 0·001; ****P < 0·0001.

B, regression coefficients; Exp(B), odds of an event occurring.

The properties of EUs

For the damaged saplings, L2nd, L3rd and L4th significantly increased with increasing L1st, L2nd and L3rd, respectively (Table 4). Also, L2nd, L3rd and L4th significantly decreased with increasing D1st, D2nd and D3rd, respectively (Table 4). The average L2nd in high soil fertility was longer than that in low soil fertility, but L3rd and L4th were not affected by FS (Table 4). For the undamaged saplings, L2nd and L3rd significantly increased with increasing L1st and L2nd, respectively, while FS did not significantly affect L2nd or L3rd (Table 4).

Table 4.

The results of multiple regression analyses for length of subsequent EUs vs. length (LP) and leaf damage (DP) of parent EUs, and soil fertility (FS)

β
Treatment Dependent variables n F r2 LP DP FS
Damaged L2nd 319 95·378 0·476**** 0·637**** −0·229**** 0·173****
L3rd 171 38·254 0·407**** 0·599**** −0·208*** −0·030
L4th 109 19·752 0·361**** 0·522**** −0·260** 0·078
Undamaged L2nd 213 60·136 0·364**** 0·601**** – −0·021
L3rd 92 13·054 0·227**** 0·492**** – −0·061
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Significant levels: **P < 0·01; ***P < 0·001; ****P < 0·0001.

β, the standardized coefficient.

Variables were arcsine or log transformed.

In 15 out of 16 categories, log-transformed length (ln L) and log-transformed leaf number (ln N) were significantly linearly correlated (Fig. 1). Furthermore, in 14 out of 16 categories, the slopes of the regressions were significantly smaller than one, indicating that the relationships between L and N described convex curves (Fig. 1). Therefore, these results showed that the shorter EUs displayed a greater number of leaves per unit of EU length than did longer EUs.

Fig. 1.

Fig. 1.

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Relationships between leaf number (y) and length (x) of EUs. Results of the RMA regressions are shown in each diagram. The regression represents an allometric relationship; ln y = a + bln x. Significant levels: **P < 0·01, ****P < 0·0001.

DISCUSSION

Effects of soil fertility on leaf damage

The extent of leaf damage in second EUs was more severe at high soil fertility than at low soil fertility, although soil fertility did not affect the extent of leaf damage at the other flush stages (Table 2). The species of insect and the quantity of available leaves for insects existing at that time might relate to whether soil fertility affected the extent of leaf damage or not.

Compensative growth responses

The probability of subsequent flushes had significantly increased with increasing leaf damage of the parent EU (Table 3). This suggests that herbivore-damaged Q. serrata saplings produce more growth flushes, which increase the number of higher EUs within damaged saplings, as observed in our previous work (Mizumachi et al., 2004). Defoliation can cause mortality in oak trees (Staley, 1965; Wright et al., 1989; Byington et al., 1994). Juvenile woody plants in particular allocate a large fraction of their biomass to leaves (Poorter and Nagel, 2000). Therefore, it is crucial for damaged saplings to reproduce new EUs that can compensate for photosynthetic organs lost to herbivore damage.

Several studies have shown that artificial defoliation can affect the length of subsequently produced shoots (Heichel and Turner, 1984; Charr et al., 1997b). This response is expected to be closely associated with the compensatory production of foliage. Our previous study showed that herbivore damage reduces the length of subsequently produced EUs (Mizumachi et al., 2004). In this study, we showed the reduction in length of second EUs and third EUs (Tables 1 and 2) and we also showed that the reduced length of subsequent EUs was intimately related to the intensity of herbivore damage to parent EUs (Table 4). From the viewpoint of biomass allocation, photosynthetic tissue comprises a greater proportion of total EU biomass in shorter EUs (e.g. Niinemets and Kull, 1995; Mori and Takeda, 2004). Furthermore, shorter EUs had a greater number of leaves per unit EU length than did longer EUs in this study (Fig. 1). Therefore, EUs shorten according to the intensity of herbivore damage, thereby reducing the structural investment in shoot stems as supportive non-photosynthetic tissue. Accordingly, Q. serrata saplings under herbivore pressure can effectively allocate more resources to photosynthetic tissues, and thus achieve compensatory reproduction of their foliage, by enhancing the production of shorter EUs (Mizumachi et al., 2004).

The intensity of herbivore damage to parent EUs was related not only to the length of their daughter EUs but also to the probability of subsequent flushes (Tables 3 and 4, respectively), indicating that the production of EUs in response to herbivore damage is fundamentally regulated at the individual EU level. Several studies that have investigated the responses of plant units to artificial defoliation (e.g. Tuomi et al., 1988; Honkanen and Haukioja, 1994; Ruohomäki et al., 1997) have shown that damaging the foliage of a branch alters the quantity and quality of foliage only within that branch. In this study, we showed that each daughter EU responded according to the intensity of herbivore damage to its parent EU. This result suggests that each EU acts autonomously. Given that the intensity of herbivory damage is spatially and temporally heterogeneous within a tree crown (Yamasaki and Kikuzawa, 2003), it may be strategically effective for each EU within the crown to respond to its respective localized leaf damage. Moreover, the probability of subsequent flushes and the length of subsequent EUs significantly increased with the length of their parent EUs (Tables 3 and 4, respectively). Similarly, Karlsson et al. (1996) reported that in Betula spp., the length of parent shoots produced during previous years was positively correlated with subsequent shoot characteristics such as length, bud number and internode length. These results suggest that each shoot growth is mainly determined by the condition of local resources, which generally depends on the resource acquisition and availability of parent shoots. Therefore, the present study indicates that, for Quercus saplings, the parent EUs play a major role in determining the growth response of subsequent EUs against herbivore damage during the growing season. Alaoui-Sossé et al. (1996) demonstrated that the elongation of subsequent EUs produced during a given flush in Q. robur generally depended on the photosynthate of the first EUs, demonstrating the importance of parent EUs for the growth of subsequent EUs in Quercus saplings.

Effects of soil fertility on EU growth

Our results showed that, for damaged saplings, the probabilities of second and third flushes were significantly higher for plants growing in high-fertility soil than those raised in low-fertility soil (Table 3). High soil fertility stimulates the flushing of a greater number of buds on actively growing shoots and produces plants with more branches, compared with those at low soil fertility (Harmer, 1989). Therefore, high soil fertility increases plant biomass production, the number of leaves and leaf area (e.g. Berger and Glatzel, 2001). These responses to nutrient availability might affect herbivory-induced compensatory responses. Although several studies on woody plants have investigated the responses to both defoliation and resource availability, most of these studies analysed mainly foliage quality, based on characteristics such as phenolic and nitrogen concentrations and biomass allocation (e.g. Hunter and Schultz, 1995; Ruohomäki et al., 1996; Mutikainen et al., 2000; Hikosaka et al., 2005). Few studies have investigated compensatory growth responses at the individual or shoot level. Plants cannot always avoid herbivore damage, even when they have developed defence mechanisms against herbivores (Haukioja and Koricheva, 2000; Lehtilä, 2000). Therefore, an ability to compensate for herbivore damage is important for plant survival and performance. In our previous study, the compensatory growth responses of Quercus saplings to nutrient availability were investigated (Mizumachi et al., 2004). The number and total length of EUs produced in Quercus saplings during one growing season were greater when raised in high-nutrient conditions than in low-nutrient conditions (Mizumachi et al., 2004), as was the intensity of insect damage according to time (Table 2). These results suggest that saplings growing in high-fertility soil might show more compensatory shoot growth than those growing in low-fertility soil. The present study further clarified how Q. serrata saplings responded in a compensatory manner to soil fertility. In Salix planifolia ssp. planifolia cuttings, the relative growth rates of shoots responding to simulated leaf herbivory were dependent upon nutrient availability (Houle, 1999). In Quercus saplings, shoot elongation occurs rhythmically, i.e. elongations take place in bursts separated by distinct rest periods (e.g. Borchert, 1975). Therefore, the enhanced probability of subsequent flushes according to soil fertility is an important response by Q. serrata saplings to compensate for herbivory during the growing season.

Given sufficient resources for EUs, increasing the lengths of subsequent EUs is essential for saplings to acquire the space and the resultant resources for future growth (Yagi and Kikuzawa, 1999) and bud production (Harmer, 1992). The length of second EUs in damaged saplings was significantly longer in plants growing in high-fertility soil than in those raised in low-fertility soil (Tables 2 and 4). This suggests that the EU growth of Q. serrata saplings in response to herbivory is profoundly affected by soil fertility. However, saplings both in low- and high-fertility soil could show the compensatory responses at each EU level according to their nutrient availability, reflecting the fact that the production of shorter EUs is an effective response to recovery from herbivory (Mizumachi et al., 2004). In conclusion, according to soil nutrient availability, Q. serrata has a significant plasticity to show growth responses at an individual EU level and thereby can achieve compensatory growth at whole sapling level.

Acknowledgments

We thank the members of the Kitashirakawa Experimental Station, Field Science Education and Research Center, Kyoto University, for their support in this experiment. We also thank Professor H. Takeda, Mr H. Ishii, Dr K. Kawamura and Dr T. Hishi, Kyoto University, for their helpful advice and encouragement, and all of the members of the Laboratory of Forest Ecology, Kyoto University, for engaging us in useful discussions. This study was supported in part by a Grant-in-Aid for Science Research (no. 13306012, to N.O.) and a Grant-in-Aid for the 21st Century COE Program for Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. This study was also supported by JSPS Research Fellowships for Young Scientists (no. 17·2313, to E.M.).

LITERATURE CITED

  1. Alaoui-Sossé B, Ricaud S, Barnola P, Dizengremel P. 1996. Rhythmic growth and carbon allocation in Quercus robur. Sucrose metabolizing enzymes in leaves. Physiologia Plantarum 96: 667–673. [Google Scholar]
  2. Berger TW, Glatzel G. 2001. Response of Quercus petraea seedlings to nitrogen fertilization. Forest Ecology and Management 149: 1–14. [Google Scholar]
  3. Borchert R. 1975. Endogenous shoot growth rhythms and indeterminate shoot growth in oak. Physiologia Plantarum 35: 152–157. [Google Scholar]
  4. Byington TS, Gottschalk KW, McGraw JB. 1994. Within-population variation in response of red oak seedlings to herbivory by gypsy moth larvae. American Midland Naturalist 132: 328–339. [Google Scholar]
  5. Chaar H, Colin F, Collet C. 1997a. Effects of environmental factors on the shoot development of Quercus petraea seedlings. A methodological approach. Forest Ecology and Management 97: 119–131. [Google Scholar]
  6. Chaar H, Colin F, Leborgne G. 1997b. Artificial defoliation, decapitation of the terminal bud, and removal of the apical tip of the shoot in sessile oak seedlings and consequences on subsequent growth. Canadian Journal of Forest Research 27: 1614–1621. [Google Scholar]
  7. Collet C, Frochot H. 1996. Effects of interspecific competition on periodic shoot elongation in oak seedlings. Canadian Journal of Forest Research 26: 1934–1942. [Google Scholar]
  8. Falster DS, Warton DI, Wright IJ. 2003. Standardised major axis testes and routines. Version 1.0. http:\\www.bio.mq.edu.au\ecology\SMATR
  9. Forkner RE, Hunter MD. 2000. What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81: 1588–1600. [Google Scholar]
  10. Hanson PJ, Dickson RE, Isebrands JG, Crow TR, Dixon RK. 1986. A morphological index of Quercus seedling ontogeny for use in studies of physiology and growth. Tree Physiology 2: 273–281. [DOI] [PubMed] [Google Scholar]
  11. Harmer R. 1989. The effect of mineral nutrients on growth, flushing, apical dominance and branching in Quercus petraea (Matt.) Liebl. Forestry 62: 383–395. [Google Scholar]
  12. Harmer R. 1992. Relationships between shoot length, bud number and branch production in Quercus petraea (Matt.) Liebl. Forestry 65: 61–72. [Google Scholar]
  13. Haukioja E, Koricheva J. 2000. Tolerance to herbivory in woody vs. herbivorous plants. Evolutionary Ecology 14: 551–562. [Google Scholar]
  14. Haukioja E, Ruohomäki K, Senn J, Suomela J, Walls M. 1990. Consequences of herbivory in the mountain birch (Betula pubescens ssp tortuosa): importance of the functional organization of the tree. Oecologia 82: 238–247. [DOI] [PubMed] [Google Scholar]
  15. Hawkes CV, Sullivan JJ. 2001. The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82: 2045–2058. [Google Scholar]
  16. Heichel GH, Turner NC. 1984. Branch growth and leaf numbers of red maple (Acer rubrum L.) and red oak (Quercus rubra L.): response to defoliation. Oecologia 62: 1–6. [DOI] [PubMed] [Google Scholar]
  17. Heuret P, Guédon Y, Guérard N, Barthélémy D. 2003. Analysing branching pattern in plantations of young red oak trees (Quercus rubra L., Fagaceae). Annals of Botany 91: 479–492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hikosaka K, Takashima T, Kabaya D, Hirose T, Kamata N. 2005. Biomass allocation and leaf chemical defence in defoliated seedlings of Quercus serrata with respect to carbon–nitrogen balance. Annals of Botany 95: 1025–1032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Honkanen T, Haukioja E. 1994. Why does a branch suffer more after branch-wide than after tree-wide defoliation? Oikos 71: 441–450. [Google Scholar]
  20. Honkanen T, Haukioja E, Kitunen V. 1999. Responses of Pinus sylvestris branches to simulated herbivory are modified by tree sink/source dynamics and by external resources. Functional Ecology 13: 126–140. [Google Scholar]
  21. Houle G. 1999. Nutrient availability and plant gender influences on the short-term compensatory responses of Salix planifolia ssp. planifolia to simulated leaf herbivory. Canadian Journal of Forest Research 29: 1841–1846. [Google Scholar]
  22. Hunter MD, Schultz JC. 1995. Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology 76: 1226–1232. [Google Scholar]
  23. Karlsson PS, Olsson L, Hellström K. 1996. Trade-offs among investments in different long-shoot functions—variation among mountain birch individuals. Journal of Ecology 84: 915–921. [Google Scholar]
  24. Lehtilä K. 2000. Modelling compensatory regrowth with bud dormancy and gradual activation of buds. Evolutionary Ecology 14: 315–330. [Google Scholar]
  25. Lower SS, Kirshenbaum S, Orians CM. 2003. Preference and performance of a willow-feeding leaf beetle: soil nutrient and flooding effects on host quality. Oecologia 136: 402–411. [DOI] [PubMed] [Google Scholar]
  26. Maschinski J, Whitham TG. 1989. The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. American Naturalist 134: 1–19. [Google Scholar]
  27. Meyer GA. 2000. Interactive effects of soil fertility and herbivory on Brassica nigra. Oikos 88: 433–441. [Google Scholar]
  28. Mizumachi E, Osawa N, Akiyama R, Tokuchi N. 2004. The effects of herbivory and soil fertility on the growth patterns of Quercus serrata and Q. crispula saplings at the shoot and individual levels. Population Ecology 46: 203–211. [Google Scholar]
  29. Mori A, Takeda H. 2004. Functional relationships between crown morphology and within-crown characteristics of understory saplings of three co-dominating conifers in a subalpine forest in central Japan. Tree Physiology 24: 661–670. [DOI] [PubMed] [Google Scholar]
  30. Mutikainen P, Walls M, Ovaska J, Keinänen M, Julkunen-Tiitto R, Vapaavuori E. 2000. Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81: 49–65. [Google Scholar]
  31. Niinemets Ü, Kull O. 1995. Effects of light availability and tree size on the architecture of assimilative surface in the canopy of Picea abies: variation in shoot structure. Tree Physiology 15: 791–798. [DOI] [PubMed] [Google Scholar]
  32. Niklas KJ. 1994. Plant allometry: the scaling of form and process. Chicago, IL: University of Chicago Press.
  33. Nykänen H, Koricheva J. 2004. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104: 247–268. [Google Scholar]
  34. Poorter H, Nagel O. 2000. The role of biomass allocation in the growth responses of plants to different levels of light, CO2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology 27: 595–607. [Google Scholar]
  35. Rosenthal JP, Kotanen PM. 1994. Terrestrial plant tolerance to herbivory. Trends in Ecology and Evolution 9: 145–148. [DOI] [PubMed] [Google Scholar]
  36. Ruohomäki K, Chapin III FS, Haukioja E, Neuvonen S, Suomela J. 1996. Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 77: 2302–2311. [Google Scholar]
  37. Ruohomäki K, Haukioja E, Repka S, Lehtilä K. 1997. Leaf value: effects of damage to individual leaves on growth and reproduction of mountain birch shoots. Ecology 78: 2105–2117. [Google Scholar]
  38. SAS Institute. 2004. JMP Statistical Discovery Software (ver. 5.1.1). Cary, NC: SAS Institute Inc.
  39. Sprugel DG, Hinckley TM, Schaap W. 1991. The theory and practice of branch autonomy. Annual Review of Ecology and Systematics 22: 309–334. [Google Scholar]
  40. Staley JM. 1965. Decline and mortality of red and scarlet oaks. Forest Science 11: 2–17. [Google Scholar]
  41. Strauss SY, Agrawal AA. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution 14: 179–185. [DOI] [PubMed] [Google Scholar]
  42. Tiffin P. 2000. Mechanisms of tolerance to herbivore damage: what do we know? Evolutionary Ecology 14: 523–536. [Google Scholar]
  43. Tokuchi N, Takeda H, Yoshida K, Iwatsubo G. 1999. Topographical variations in a plant–soil system along a slope on Mt. Ryuoh, Japan. Ecological Research 14: 361–369. [Google Scholar]
  44. Tuomi J, Niemelä P, Rousi M, Sirén S, Vuorisalo T. 1988. Induced accumulation of foliage phenols in mountain birch: branch response to defoliation? American Naturalist 132: 602–608. [Google Scholar]
  45. Watson MA. 1986. Integrated physiological units in plants. Trends in Ecology and Evolution 1: 119–123. [DOI] [PubMed] [Google Scholar]
  46. White J. 1979. The plant as a metapopulation. Annual Review of Ecology and Systematics 10: 109–145. [Google Scholar]
  47. Wright SL, Hall RW, Peacock JW. 1989. Effect of simulated insect damage on growth and survival of northern red oak (Quercus rubra L.) seedlings. Environmental Entomology 18: 235–239. [Google Scholar]
  48. Yagi T, Kikuzawa K. 1999. Patterns in size-related variations in current-year shoot structure in eight deciduous tree species. Journal of Plant Research 112: 343–352. [Google Scholar]
  49. Yamasaki M, Kikuzawa K. 2003. Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata. Oecologia 137: 226–232. [DOI] [PubMed] [Google Scholar]

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