Marian J. GIERTYCH*, Piotr KAROLEWSKI, Jacek OLEKSYN
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland;
*e-mail: giertych@man.poznan.pl (corresponding author)
EARLYSEASON DEFOLIATION OF SORBUS AUCUPARIA L. AND ACER PLATANOIDES L. CAN INDUCE DEFENSE MECHANISMS
AGAINST THE SPIDER MITE TETRANYCHUS URTICAE KOCH
ABSTRACT: Artificial defoliation is often used in studies of induced defense reactions of plants to damage by arthropods. However, little is known about the role of various external fac- tors that may determine the nature of inducible defenses. Here we tested whether light level un- der which plants grow could affect the natural invasion of two-spotted spider mite (Tetranychus urticae Koch) with a broad range of host plants.
For this study we used two host species that differ widely in shade tolerance: shade-adapted Norway maple (Acer platanoides L.) and sun-adapted Eu- ropean mountain ash (Sorbus aucuparia L.). The purpose of this study was to explore mite inva- sion and to test whether prior simulated defo- liation, light conditions and host species differ- ences in secondary defense metabolites (soluble phenolics) play a role in the pattern of invasion.
One-year-old maple and ash seedlings growing in pots were placed into two shade houses that pro- duced a treatment with 5% light transmittance, and the second group of seedlings was placed in full sunlight. The experiment was carried out in a location chronically affected by spider mite pres- ence. The defoliation was performed in mid-May by manual removal of 0 (control), 25, 50, 75 and 100% of leaves. Natural two-spotted spider mite invasion took place in mid-July and was observed only on seedlings growing in the shade. Mites were found on leaves of almost all seedlings. How- ever, the intensity of feeding damage to leaves was related to the level of earlier defoliation. Control
and slightly to moderately (25–50%) defoliated seedlings of both species were most affected by spider mites. Mite feeding behavior was directly linked to changes in concentration of leaf carbon and phenolic compounds. Carbon content was positively correlated with the percent of seedlings damaged by spider mites in both tree species (R2>
0.80; P <0.05). The highest concentration of phe- nolic compounds was observed in leaves of seed- lings subjected to 50 and 75% defoliation.
Our results indicated that two-spotted spider mites preferred plants grown in a shade environ- ment and within these plants favored leaves which are high in carbon and low in phenolic com- pounds. Both plant species were able to survive early season leaf damage inflicted by spider mites.
Inducible phenolic compounds were among de- fensive secondary metabolites contributing to low spider mite success in plants recovering from artificial spring defoliation.
KEY WORDS: herbivore mite, chemical composition, Arachnida, Acari, Tetranychidae
1. INTRODUCTION
Plant-herbivore interaction has been studied extensively during the last several decades. The important parts of these stud- ies are defense reactions of plants, which are well summarized by Haw ke s and Su l l iv an Regular research paper
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(2001), Kor i ch e v a (2002), Ny k än e n and Kor i ch e v a (2004), and Kor i ch e v a et al.
(2004). However, very little information is available regarding physical, nutritional and allelochemical traits affecting the strength of constitutive and induced resistance against mites in woody plants. Constitutive resistance is considered to be more costly to achieve in comparison with induced defenses which al- low plants to save resources when herbivores are absent (Bro dy and Kar b an 1992, Kar- b an and B a l dw i n 1997, Ag r aw a l 2005).
Different forms of induced resistance take variable lengths of time to become effective and are divided into rapid induced resistance and delayed induced resistance categories (Hau k i oj a 1990). Delayed induced re- sponses refer to defense reactions against the next generation of insect herbivores (B au r et al. 1991, Kait an i e m i et al. 1998) or other insect species that attack later in the growing season (Hu nte r and S chu lt z 1995, Tre - w h e l l a et al. 1997).
Simulated defoliation of trees is often used in studies of induced defense reactions to herbivory (O l e k s y n et al. 1998, D ol ch and Ts ch ar nt ke 2000, Ts ch ar nt ke et al. 2001, Ste ve ns and L i n d rot h 2005, Va l k am a et al. 2005). There is little infor- mation about potential interaction between light conditions and induced defenses caused by the simulated defoliation (Ru oh om ä k i et al. 1996, Mut i k ai n e n et al. 2000). Studies of induced defense responses by host plants are usually restricted to the determination of defense metabolite levels or determination of herbivore performance under laboratory conditions. According to the carbon-nu- trient balance hypothesis, shade limits the production of carbon-based defense me- tabolites. Whereas defoliation induces plants to produce secondary compounds (defense metabolites) and physical defenses that may further affect growth processes.
Depending on their degree of shade tol- erance, plants may express different mor- phological, physiological and defense traits under low light conditions. The two host spe- cies used in our studies differ widely in shade tolerance. Norway maple (Acer platanoides L.) is considered to be shade-adapted and European mountain ash (Sorbus aucuparia L.) is sun-adapted (E l l e nb e rg et al. 1991).
Based on earlier reports of C ol e y (1987), Ho o ge ste ge r and Kar l ss on (1992), and Fre it a s and B e r t i - F i l h o (1994), we hy- pothesized that chemical defenses will be restricted in defoliated plants because they will rebuild their leaves in order to provide assimilates necessary to sustain plant growth and vitality; this effect would be more pro- nounced for plants growing in the shade, es- pecially for sun-adapted mountain ash. The objective of the present study was to exam- ine the role of a few external factors that may determine the nature of inducible defenses against two-spotted spider mite (Tetranychus urticae Koch) – a polyphagous, parenchyma cell feeding mite found on over 1000 host plant species from 129 families (Mi ge on and D or ke l d 2006). We asked specifically:
(1) To what extent do light conditions and early season defoliation affect two-spotted spider mite establishment on two host spe- cies that differ in shade tolerance? (2) Do induced responses following early-season damage to trees play a role in plant resistance to mites?
2. MATERIAL AND METHODS 2.1. Cultivation of seedlings
One-year-old Norway maple (Acer plat- anoides L.) and European mountain ash (Sorbus aucuparia L.) seedlings were grown individually in pots filled with a 1:1 ratio (v/
v) mixture of forest soil and peat with addi- tion of Osmocote® fertilizer, which has con- trolled release over a period of 5–6 months.
At the beginning of growing season (April 2006) the 140 maple and 160 ash seedlings were randomly divided into two groups. The first group was placed into two replicated shade houses covered with polypropylene shade cloththatproduced a treatment with 5% light transmittance. The second group of seedlings was placed in two blocks with full sunlight. The distance between all treatments and blocks has not exceeded 10 m. The ex- periment was carried out at the experimental field of the Institute of Dendrology in Kórnik, Poland (52°14’N; 17°05’E; 75 m altitude) that was chronically affected by spider mite pres- ence. The seedlings were randomly assigned to the defoliation treatment. The defoliation
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was accomplished in May 16–18th 2006 by manual removal of the leaves. For each seed- ling, all leaves were counted and the desired percent of foliage was removed, and five defoliation treatments were established: 0 (control), 25, 50, 75 and 100% of leaves re- moved. New leaves appeared 1–2 weeks after defoliation. The seedlings were watered as necessary. Temperatures and relative humid- ity inside the tents and on the full sunlight plots were recorded using Hobo Data Log- gers (Onset, Computer Corp., USA).
2.2. Two-spotted spider mite invasion Two-spotted spider mite (Tetranychus urticae Koch) natural invasion took place in mid-July and was observed only on seedlings growing in the shade. The intensity of feed- ing was assessed in late July by counting seed- lings with withered leaves. The invasion was observed mainly on older, primary leaves al- though later it spread to younger, secondary leaves. In early August primary flush leaves from each seedling were collected for mor- phological and chemical analyses (except the 100% defoliated treatment where were col- lected new leaves).
2.3. Morphological and chemical analyses One leaf from each plant was collected for morphological and chemical analyses.
The projected leaf area was determined using an image analysis system and the WinFOLIA Pro Software (Regent Instruments
,
Inc., Que- bec, Canada). Specific leaf area (SLA, defined as the projected leaf area divided by leaf dry mass, cm2g–1) was calculated for undamaged leaves. The leaves were oven dried (65°C for 48 h), powdered in a Mikro-Feinmühle Cu- latti mill (IKA Labortechnik Staufen, Ger- many) and stored in plastic boxes.For chemical analyses data are means of two replicates from composite samples of the individual seedlings sampled in each treat- ment in each block. Nitrogen and carbon concentration in the leaves were measured using the Elemental Combustion System CHNS-0 (Constech Analytical Technologies Inc., Valentia, USA). The concentration of phenolic compounds (TPh) was measured colorimetrically using Folin and Ciocalteu’s Phenol Reagent (SIGMA F-9252), following the method of Joh ns on and S ch a a l (1957) as modified by Singleton and Rossi (1965).
The content of total phenols was expressed in μmol of chlorogenic acid g–1 dry mass. To- tal soluble carbohydrates and starch concen- trations were determined by a modification of the method described by Hans e n and Møl l e r (1975) and Hai ss i g and D i ck s on (1979). Sugars were extracted from oven- dried (65°C, 48 h) tissue powder in metha- nol-chloroform-water, and tissue residuals were used for starch content determination.
Fig 1. Percent of shade grown Sorbus aucuparia and Acer platanoides seedlings damaged by spider mites across defoliation treatments. The vertical lines represent ±1 standard error of the mean.
0 20 40 60 80 100
0 25 50 75 100
So r b u s
Defoliation treatment
% of seedlings damaged by spider mite
0 20 40 60 80 100
0 25 50 75 100
A c e r
Defoliation treatment
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2.4. Statistical analyses
Analysis of variance (ANOVA) was used to assess the influence of species and defo- liation treatment on leaf TPh, N and C con- centration. Data are means of two composite
samples (with equal numbers of individual plant in each sample). Blocks were used as replication for chemical analyses. The cor- relation analyses were used to establish re- lationships between the leaf TPh, N and C concentration and the percent of seedlings 0
100 200 300 400
0 25 50 75 100 Specific leaf area (cm2 g-1 )
S o r b u s
0 100 200 300 400
0 25 50 75 100
A c e r
30 35 40 45 50
0 25 50 75 100
Leaf carbon (%)
30 35 40 45 50
0 25 50 75 100
0 1 2 3 4
0 25 50 75 100
Leaf nitrogen (%)
Defoliation treatment
0 1 2 3 4
0 25 50 75 100 Defoliation treatment
Fig. 2. Specific leaf area (SLA, cm2g–1), carbon (% DM) and nitrogen (% DM) concentrations in leaves of Sorbus aucuparia and Acer platanoides growing in shade (dark) and full light (white). The vertical lines represent ±1 standard error of the mean.
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damaged by two-spotted spider mite. The χ2 test was used to analyze the preferences of spider mite to leaves from different defolia- tion treatment. All analyses were conducted with JMP software (JMP, Version 5.1.2 SAS Institute Inc., Cary, NC, USA).
3. RESULTS
Spider mite invasion was observed on both tree species, shade-adapted Norway maple and sun-adapted European mountain ash, but only on seedlings growing in the shade. Shade houses affected also both the thermal condition (mean temperature of July was 24.5°C in the full light vs. 21.2°C in the shade) and relative humidity (51% in the full light vs. 83% in the shade).
Mites appeared on leaves of almost all seedlings, but intensity of feeding (number of seedlings with withered leaves) was sig- nificantly related to the level of earlier defo- liation (χ2 – 20.3; P <0.001 for maple and χ2 – 25.0; P <0.001 for ash). The mites preferred seedlings grown in shade and those with the lowest level of defoliation (0–50%). Seed- lings with higher early-spring defoliation (75–100%) were attacked with lower inten- sity (Fig. 1).
The light conditions and defoliation al- tered SLA. In both species SLA was more than twice as high in the shade-grown seed- lings (131 vs. 323 cm2g–1, Fig. 2). The influ- ence of defoliation on SLA was also greater for shade-grown seedlings, particularly ash seedlings (Fig. 2; Table 1). Nitrogen concen- tration was not related to defoliation, how- ever it was related to species and light condi- tions (Fig. 2; Table 1). Carbon concentration in leaves was significantly affected by the light and defoliation treatments. Leaves from the full light treatment exhibited a higher carbon concentration. In shade conditions the highest C concentration was observed in leaves from seedlings of the control and lowest level of defoliation, and the lowest in seedlings totally defoliated in early spring (Fig. 2; Table 1). Carbon concentration was significantly correlated with the percent of seedlings damaged by two-spotted spider mite in both species (R2 = 0.80; P <0.05 for maple and R2 = 0.86; P <0.05 for ash). The
concentration of phenolic compounds var- Table 1. Summary of ANOVA results for specific leaf area (SLA), carbon, nitrogen, phenolic compounds and soluble carbohydrates by species, light and defolia- tion treatment. P <0.05 are given in bold. Source of SLACarbonNitrogen Phenolic compoundsSoluble carbohydrates variation d.f.d.f. errorFPFP FP FP FP Species (S)1208.010.01030.370.551916.330.000628.03<0.00010.250.6237 Light (L)120509.85<0.0001337.91<0.0001546.57<0.0001816.4<0.0001232.19<0.0001 Defoliation 4203.400.02833.370.02921.110.38120.510.72950.61410.6580 (D) S × L1200.090.762121.870.000135.60<0.00010.800.38072.220.1528 S × D4205.800.00290.560.69272.460.07893.560.02401,500.2445 L × D4202.840.05152.180.10841.560.22363.860.01750.760.5676 S × L ×D4203.410.02780.780.55141.520.23242.980.04401.950.1464
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ied with light conditions and with the level of defoliation. Full light leaves had a greater than four-fold higher concentration of phe- nolics (Fig. 3). Under shade conditions the highest concentration of soluble phenolics was observed in the leaves of seedlings with 50 and 75% leaves removed (Fig. 2; Table 1).
All leaves from 100% treatment originated from the secondary flush and were younger by ca. 45 days. Therefore, their concentration of N was higher and C and TPh lower than those observed in older leaves from control and slightly defoliated seedlings. Soluble car- bohydrate concentrations were three-fold higher in leaves from plants grown in full sun, and there was no effect of defoliation.
The level of starch was below the threshold of detection.
4. DISCUSSION
Two-spotted spider mite usually is de- scribed as a greenhouse pest (v an d e Vr i e et al. 1972) but it also occurs in field-grown plants (v an d e n B o om et al. 2003). In our experiment spider mite was observed only under low light conditions of shade houses that were characterized by an average tem- perature 3.3°C lower and significantly higher relative humidity (83% in shade vs. 51% in full-light). Therefore, our findings contradict earlier reports that T. urticae prefer hot and dry environments (D u s o et al. 2004). Spider mites do not infest all plants to the same de- gree because of differences in nutritive and toxic constituents (v an d e n B o om et al.
2003). Our study confirmed that two-spot- 0
100 200 300 400 500 600 700
0 25 50 75 100
So r b us
0 100 200 300 400 500 600 700
0 25 50 75 100
Acer
0 2 4 6 8 10
0 25 50 75 100 0
2 4 6 8 10
0 25 50 75 100 Defoliation treatment Defoliation treatment
Fig. 3. Phenolic compounds (μMg–1DM) and soluble carbohydrates (% DM) concentrations in leaves of Sorbus aucuparia and Acer platanoides growing in shade (dark) and full light (white). The vertical lines represent ±1 standard error of the mean.
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ted spider mites prefers older leaves (Kar- b an and T h a l e r 1999), but only for the case of Sorbus leaves. Acer and Sorbus differ in their strategy of leaf development. Acer leaves develop only in spring in our experi- ment all leaves were in fully developed before the manual defoliation. New leaves appeared only after the 100% defoliation treatment.
In Sorbus new leaves develop along with the growth of the stem until the terminal bud appears in mid-summer. Reactions of both tree species to two-spotted spider mite in- festation were similar except for differences caused by leaf development strategy. Results of our experiments indicated that coloniza- tion by two-spotted spider mite may be also affected by intraspecific differences in leaf C and N, and secondary metabolite concentra- tion related to the light condition and prior defoliation history. Higher vulnerability of plants growing in shade to herbivore dam- age is in agreement with observations of Mai or an a (1981), although L ou d a et al.
(1987) show that for herbaceous forbs the sun exposed plants are often more damaged, and Han n a et al. (1996) also found that the spider mite Tetranychus pacificus occurred in greater densities on exposed compared with shaded leaves of Vitis vinifera.
The occurrence of spider mites only in shade house grown S. aucuparia and A. plat- anoides was most likely related to chemical composition and structure of leaves (SLA) than to temperature or humidity conditions.
Plants growing in the shade differ in many traits from those growing in full sunlight.
Shade leaves have higher SLA (Fig. 1; Table 1, R e i ch et al. 1999), lower levels of pheno- lics (Fig. 2, Table 1, C h a c ón and A r m e sto 2006, C ron i n and L o d ge 2003, Gi e r t yc h 2001), higher nitrogen concentrations (Fig.
1, Table 1, R e i ch et al. 1995, B ar a z a et al.
2004, Po or te r and B onge rs 2006), and be- cause of that shade leaves are generally more attractive for herbivores (He n r i k ss on et al.
2003).
The reaction of trees to defoliation or light limitation may depend on their shade- tolerance (C ol e y 1987). In our experiment sun-adapted Sorbus aucuparia and shade- adapted Acer platanoides behaved similarly under shade conditions. However, concen- tration of phenolic compounds in Acer leaves
from shade was higher and also defoliation increased (except in 100% defoliated plants) the level of phenolics. The abilities to defense in the shade condition are probably higher in the case of Acer in comparison with Sorbus.
We expected that defoliated plants growing in shade would allocate carbon mostly for rebuilding their assimilation apparatus and less for expensive chemical defense. We also expected that chemical defenses would be especially impaired when the sun-adapted species was grown in shade. However, the pattern of spider mite invasion during the defoliation experiment showed that, through changes in leaf metabolism, the seedlings can defend their leaves even under very shady conditions. Control and lightly defoliated seedlings were most affected by spider mites while more heavily defoliated seedlings were attacked later and with lower intensity. The effect of early-season defoliation and shade condition on defense chemistry was mani- fested by 25–62% and 34–47% increases in the concentration of phenolic compounds in Sorbus and Acer, respectively (Fig. 3). The leaves of extensively defoliated seedlings of both species had higher concentrations of phenolic compounds, except for the totally defoliated plants where all leaves from sec- ondary flush were ca. 45 days younger. Young leaves have often less phenolics (G owd a and Pa l o 2003, Gi e r t ych et al. 1999, but see L okv am i Ku rs ar 2005). Leaves origi- nating from a secondary flush after defolia- tion have different chemical and structural characteristics (Ku h aj e k et al. 2006, L ok - v am and Ku rs ar 2005), and it is likely that for this reason they were avoided by spider mites. The appearance of herbivores is often connected with changes in metabolite lev- els during leaf development (B a z z a z et al.
1987, Kau s e et al. 1999). In that case we can talk about delayed induced resistance. Phe- nolic compounds are one of the most impor- tant defense metabolites which increase after herbivore damage (O l e k s y n et al. 1998, Ny k än e n and Kor i ch e v a 2004, C h a c ón and A r me sto 2006) and they are often take part both in delayed induced and constitutive defense (Ru oh om ä k i et al. 1996, C or n e - l i ss e n and Fe r n an d e s 2001, Ts ch ar nt ke et al. 2001, Ag re l l et al. 2003, Ste ve ns and L i n d rot h 2005). It is likely that the relation-
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ship between leaf phenolics and resistance to T. urticae observed in our study was related to reduction in mite growth and development due to inactivation of their digestive enzymes by phenolics (Lu c z y ns k i et al. 1990, B e n - n e tt and Wa l l s g rove 1994).
The higher attractiveness of control and lightly defoliated leaves to spider mites may be connected to their higher carbon con- centration, since carbon-based compounds, such as carbohydrates and lipids have a major impact on herbivore performance (R au b e n h e i m e r and Si mp s on 2004).
In our experiment defoliation did not al- ter the carbohydrate concentration (Fig. 3;
Table 1) but carbon-based nutrients may have positive effects on herbivore perfor- mance (Aw m a ck and L e at h e r 2002).
Lower concentrations of leaf carbon in seedlings defoliated early in the season was not surprising, because it is likely that re- duction in foliar area created carbohydrate constraints for development of remaining leaves. Meta-analyses have shown that the concentration of carbohydrates decreased in damaged plants (Ny k än e n and Ko - r i ch e v a 2004). However, regardless of whether nutrients or secondary metabolites determine the choice of feeding location for mites, carbon concentration may also affect insect performance (Aw m a ck and L e at h e r 2002). This was confirmed by correlations between level of damage and carbon concentration in foliage in both tree species examined. The lack of differences of nitrogen between defoliation treatments supports the conclusions of meta-analy- sis of Ny k än e n and Kor i ch e v a (2004) that nitrogen concentrations of deciduous species did not change after damages. It is likely that the chemical defense in both tree species is not based on nitrogen.
5. CONCLUSIONS
Early-season defoliation under shade conditions stimulated defense reactions of Sorbus and Acer seedlings and reduced dam- age inflicted by the two-spotted spider mite (Tetranychus urticae). Spider mites occurred only on the leaves of seedlings grown in a shade environment and within these plants choose those with low concentrations of
phenolic compounds and high concentra- tions of carbon. Both plant species were able to survive early season leaf damage inflicted by mites. Inducible secondary metabolites (soluble phenolics) were among factors con- tributing to low two-spotted spider mite suc- cess in plants recovering from early-season artificial defoliation.
ACKNOWLEDGEMENTS: We gratefully thank dr Wojciech Magowski for help in the iden- tification of spider mite. We also thank Alicja Bu- kowska, Ewa Cupryjak and Łucja Mądra for their help with the chemical analysis. We are grateful to Lee Frelich for language correction of final ver- sion of the manuscript. This study was supported by the Ministry of Sciences and Higher Educa- tion, Poland (grant no. 2PO4F 06427)
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Received after revising March 2008
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