J. Appl. Ent. 115 (1993), 233-239 0 1993 Verlag Paul Parey, Hamburg und Berlin ISSN 0931-2048

Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture, Wadenswil, and Swiss Federal Institute of Technology ETH, Department of Plant ScienceslPhytomedicine,

Zurich, Switzerland

Photosynthesis and transpiration of “Riesling x Sylvaner” grapevine leaves as affected by European red mite

(Panonychus ulmi Koch) (Acari, Tetranychidae) feeding By M. P. CANDOLFI, B. WERMELINGER and E. F. BOLLER

Abstract

The effects of feeding damage by the European red mite, Panonychus ulmi on the gas exchange of grapevine leaves (Vitis vinifera L.) were investigated. At mite infestation levels up to 3500 mite-days per leaf (corresponding to a peak density of 60 miteslleaf), plants infested with P. ulmi showed no decrease in the photos nthetic rate. The same infestation level reduced transpiration only by 8.7 %. Stomata1 and mesophyi conductance were not affected by P. ulmi feeding. The results obtained in this investigation lead to the conclusion that the empirically defined economic injury level for P. ulmi of 2-5 mites per leaf, actually used by the viticulturists in Central Europe, is far too low.

1 Introduction

Panonychus ulmi is considered to be an important pest on grapevine in the northern part of the European grape production area. This mite species is reported to cause serious crop damage resulting in lower yield and fruit quality.

However, the relationship between P. ulmi feeding damage and grape productivity was mostly studied on a non-quantitative base, lacking exact information on the mite popula- tion density during the vegetation period (ENGLERT 1979; SCHROPP et al. 1982; BORGO 1988; KAST 1989). The economic injury levels of 2-5 miteslleaf (BAILLOD et al. 1979; BOLLER and REMUND 1983; SCHRUFT et al. 1990) in use for acaricide treatment decisions are therefore based on empirical estimations rather than on quantitative data. In contrast to other crops (see review by RILLING and DURING 1990), little is known on the impact of P. ulmi on grapevine physiology. RILLING and DURING (1990) found a decline of the leaf chlorophyll content and a decrease of photosynthesis, stomata1 conductance and transpira- tion with increasing degree of leaf discoloration due to mite feeding. As proposed by RILLING and DURING (1990), leaf discoloration estimation can be successfully used as a rapid screening test to assess mite tolerance of grapevine in breeding programs but it does not account for spacial or temporal variability of the plants and, therefore, this method is not suited to define economic injury levels.

In this study, the effect of P. ulmi population density on the gas exchange rates of grapevine leaves was examined with the aim of quantifying the physiological response of the plant to mite feeding. The influence of P. ulmi on yield, fruit quality and plant growth of different grape varieties will be presented elsewhere.

2 Material and methods

The experiment was conducted at Stafa (Switzerland) in 1988, on mature field-grown, 23-year-old Riesling x Sylvaner” grapevines grafted on SO 4. The plants were trained to double Guyot with a

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234 M. P. Candolf, B. Werrnelinger and E . F. Boller

spacing of 1.70 x 1.20 m. All the shoots were topped to 12 nodes. The P. ulmi population density and gas exchange rates were measured on the gfh main leaf from the base, located opposite of the first cluster (the 2nd leaf was sampled on 25. 5. 88, at the 3-leaf-stage) on a representative shoot arising from the middle of the cane. The number of mobile P. ulmi was counted on both the upper and lower leaf surface in a non-destructive way by using a magnification lens. Mite load was expressed in mite-days per leaf' (HOYT et al. 1979). The gas exchange measurements were performed on 20 plants naturally infested with mites and on 10 mite-free control plants seven times during the growing season (25.5. 88, stage' 09-12/22. 6. 88, 23-25/24. 6. 88, 23-25/8. 7.88, 31/19. 7. 88, 31-33/8. 8. 88, 35/22. 9. 88, 37). In order to keep the control plants free of mites, they were sprayed three times during the growing season with the acaricide Tetradifon (Remanex, Burri) at 0.2 %, a pesticide that has shown no influence on the gas exchange rate of grapevine leaves (CANDOLFI et al. 1992). All other cultural practices (fertilisation, weed control, disease control and green pruning) were the same for all the treatments. Except for the measurments conducted on a cloudy day (22. 6 . 89), where the influence of environmental conditions on the impact of mite feeding damage on photosynthesis was tested, the other measurements were carried out under fully light-saturated conditions (> 1200 pmol m-'s-') between 9.00 and 11.30 h (2 h maximum measurement time per day).

Gas exchange measurements were performed using a portable infrared gas analyser system LCA-2 from ADC (Analytical Development Co. Ltd., England). Net photosynthesis (A, pmol COz m-',s?), transpiration (E, mmol H 2 0 m-2s-1), stomatal conductance to COz transfer (gs, mmol COz m- s ) and intercellular C02 partial pressures (pi, Pa) were calculated using the built-in equations of the program version 3.3 of the data-logger DL2 (Analytical Development Co. Ltd., England). Mesophyll conductance to COz transfer (gm, mmol COz m-'s-') was computed using the values recorded by the data-logger for pi and A as follows:

where: A = net photosynthesis, intercellular C02 partial pressures, pc = C02 partial pressure at site of carboxilation, rm = mesopgyi resistance, g, = mesophyll conductance. Assuming that the C 0 2 partial pressure at the site of carboxilation (pc) is zero, the carboxilation resistance is implemented in the estimate of the mesophyll resistance r, (JARVIS 1971).

Statistical analysis: the relationships between mite feeding damage (mite-days per leaf) and the gas exchange parameters were tested with regression analysis. To account for random variation in gas exchange due to different environmental conditions, leaf age, and source-sink relationshi s at different phenological stages (KRIEDEMANN et al. 1970; KRIEDEMANN 1977; SHULTZ 1989), the i t a plotted in fig. 1 were expressed as percentage of the control (mean of the control = 1) for each measurement.

3 Results and discussion

Photosynthesis, stomatal conductance, mesophyll conductance and intercellular COZ partial pressure were no t affected by P. ulmi feeding damage at infestation levels up t o 3500 mite-days per leaf (fig. 1). Transpiration was slightly reduced (8.7% reduction at 3500 mite-days per leaf, value predicted by the regression function) but even if the regression is significant, only 3.8 % of the variation can be explained by this function (R2 = 0.038).

Analysing the photosynthesis data separately for each measurement day, we note that o n six ou t of seven sampling dates the photosynthetic rate was independent of mite feeding (fig. 2). During viraison (8. 8. 88, phenological stage that marks the onset of fruit ripening) a P. ulmi infestation showed even an increase in the photosynthetic performance of the leaves (fig. 2f). A t this physiologically important stage, the grapevine leaves increase their photosynthetic rate due t o a higher sink demand (SCHULTZ 1989; CANDOLFI-VASCON- CELOS and KOBLET 1991) and have also shown t o be less sensitive t o two spotted spider mite (Tetrunychus uuticue) feeding (CANDOLFI et al. 1992). In contrast t o apple (AVERY and BRIGGS 1968) or lima bean (MARTENS and TRUMBLE 1987), grapevine leaves do not have the ability t o regenerate the tissue destroyed by mite (RILLING and DURING 1990). However, grapevine seems t o possess the ability t o tolerate European red mite infestation by raising

' One mite-day corresponds to one mite feeding for one day. - EICHHORN and LORENZ (1977).

Phenological stages as described by

Photosynthesis and transpiration of grapevine leaves as affected by P. ulmi feeding 235

0

1.5-

9s l -

0.5 -

0

y = 1.015 - 8.612E-6 X

R2 = 0.002, p = 0.50 - .. . *

* . ..

y = 0.979 - 2.914E-5 X

0

1.5-

Pi 1 -

0.5-

0

the photosynthesis of the individual cells left intact by the mites; in fact, as already mentioned, no decline in the assimilation rate was measured even when feeding damage symptoms were fairly visible.

y = 1.05-1.155E-5X

R2 = 0.007, p = 0.21

236 M . P. Candolf, B. Wermelinger and E. F. Boller

R2 = 0,001 ; p = 0.906 ' O ? . . 15:

"7 a 15: .

10-

5: 5-

e R2 = 0.001 ; p = 0.870 . . t

4 . *.: f .. . I

15-

1 0 - i

5: 7

"1 d R2 = 0.039 ; p = 0.298

.* . 0- . ..

10- I- H .. .*.... : . 0 @ . . 5:

' # * @ 8 .

0' I " " " " ' " * " " ' " ' 0 500 1000 1500 2000

20 7 203 c R2 = 0.004 : p = 0.749

15: 15-

10-

. $ 8 10: 1 *. 8. . .

.@ . 5: 5:

0- I " " ' ' " ' I ' ' ' ' ' 0-

Mite-days per leaf

Fig. 2. Relationship between Panonychus ulmi feeding damage (mite-daydeaf) and rate of photosyn- thesis (A) of "Riesling x Sylvaner" grapevine leaves at different measurement dates: a = 25. 5. 88, phenological stage 09-12; b = 22. 6. 88, 23-25; c = 24. 6. 88, 23-25; d = 8. 7. 88, 31; e = 19. 7. 88, 31-33; f = 8. 8. 88, 35; g = 22. 9. 88, 37. Note: the x-axis scale varies with measurement date

R2 = 0.023 ; p = 0.425 . 9

. . * . * ~ 8 ' ! i @ * *. . . . . ' . , , ' n . ' ' " ' . . . ' ' ' " I " . ' "'.L1

Different light and temperature conditions seem to have no influence on the response of grapevine leaves to mite feeding. In fact the results obtained on a cloudy day (22. 6 . 88;

Photosynthesis and transpiration of grapevine leaves as affected by P. ulmi feeding 237

temperature = 23.4"C and light = 477 pmol m-*s-') and on a sunny day (24. 6. 88; temperature = 24.5 "C and light = 1423 pmol m-'s-') did not differ (fig. 2b, 2c).

RILLING and DURING (1990) reported a decline of net assimilation, stomata1 conduct- ance and transpiration as leaf discoloration, induced by P. ulmi feeding, increased. A direct comparison, however, is difficult because they did not relate cumulative mite-days with discoloration level but used instead the size of the population on a given sampling date.

Experiments conducted with P. ulmi on almond, peach and apple showed that P. ulmi reduced gas exchange processes. Almond leaves seem to react very sensitively to mite feeding: 320 mite-days reduced photosynthesis by 10.2 % (YOUNGMAN 1984). On green- house-grown apple an accumulation of 2000 mite-days caused a reduction of net assimila- tion between 3 0 % and 5 0 % depending on the level of nitrogen fertilisation, while transpiration rate was reduced by 12 % at the high nitrogen level (CAMPBELL and MARINI 1990). On field-grown apple 3056 mite-days reduced photosynthesis by 17 % and transpi- ration by 12 % (CAMPBELL et al. 1990). Peach leaves reacted less sensitively to European red mite feeding than apple leaves: for a 45 % reduction in peach photosynthesis, 2900 mite-days were required while only 1750 mite-days were required for a similar reduction in apple (MOBLEY and MARINI 1990). Comparing these findings with ours it appears that the grapevine is probably more tolerant to mite feeding than other plant species. Results similar to ours were reported by HARE and YOUNGMAN (1987) and by HARE et al. (1989) with P. citri McGregor on orange. They did not find any influence of this mite species on gas exchange up to infestation levels of 2800 mite-days.

At mite infestation levels of 3500 mite-days per leaf, grapevine leaves infested with T. urticue showed an average reduction of 30 % in the photosynthetic activity and a 23.8 YO reduction in the transpiration rate (CANDOLFI et al. 1992). The same infestation level of P. ulmi failed to affect the photosynthetic rate and reduced transpiration only by 8.7 Yo (fig. 1). These comparisons show that T. urticue is a much more harmful pest to the grapevine than P. ulmi. This is in agreement with MOBLEY and MARINI (1990). They found on apple that, at the same mite-load, the photosynthesis reduction caused by T. urticue feeding was twofold that of P. ulmi. However, the impact of the two spider mite species on peach was similar (MOBLEY and MARINI 1990). YOUNGMAN et al. (1986) found that the feeding of Tetrunychus species caused a two times lower photosynthetic rate on almond leaves than that of the genus Punonychus. They attributed the different impact of the mite genera to the different physiological and metabolic requirements of the mites. Punonychus has a lower reproductive potential and lower reproductive rate than Tetrunychus which results in lower daily energy and amino acid needs and probably a lower feeding rate. Another explanation not discussed by YOUNGMAN et al. (1986) could be a difference in the salivary secretions of the two mite genera. It is known that the saliva of T. urticue consists of serous, mucous and ion-rich secretions but there is no information available on the exact chemical composition (MOTHES and SEITZ 1981, 1982). It is unknown whether P. ulmi also secrets saliva during feeding.

The results obtained in this investigation lead to the conclusion that the empirically defined economic injury level for P. ulmi of 2-5 mites per leaf, actually used by the viticulturists in central Europe (cf. Introduction), is far too low. O u r data show that the damage boundary for P. ulmi on grapevine is certainly higher than 3500 mite-days per leaf (corresponding to a peak density of 60 mitedeaf), mite-load that still did not impair the photosynthetic performance of the leaves. In parallel studies, we failed to observe a negative effect on plant vigour, yield and fruit quality even at much higher mite infestation levels (CANDOLFI 1991; CANDOLFI et a]. 1992).

238 M . P. Candolfi, B . Wermelinger and E. F. Boller

Acknowledgements

We would like to thank Dr. M. C. CANDOLFI-VASCONCELOS, Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture, CH-8820 Widenswil, Switzerland, for the technical assistance and critical review of the manuscript.

Zusammenfassung

Zur Auswirkung von Suugschaden der Obstbaumspinnrnilbe, Panonychus ulmiKoch (Acari, Tetranycbidue) auf Pbotosynthese und Transpiration von Blattern der Weinrebe (Riesling x Sylvuner)

Die Auswirkungen von Saugschaden der Obstbaumspinnmilbe (Panonychus ulmi) auf den Gasaus- tausch von Blattern der Weinrebe (Vitis vinifera L.) wurden untersucht. Bei einer P. ulmi-Belastung bis zu 3500 Milbentagen pro Blatt (Populationsspitze von 60 Milben pro Blatt) wurde die Photosyn- these nicht beeinflufit. Die Transpirationsrate wurde bei dieser Belastung nur um 8.7% reduziert. Die stomataren und mesophyllaren Leitfahigkeiten wurden nicht beeintrachtigt. Als Schlufifolgerung ergibt sich, dad die gegenwartig angewendete empirische Schadenschwelle von 2-5 Milben pro Blatt vie1 zu niedrig angesetzt ist.

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757-761.

Authors' addresses: Dr. M. P. CANDOLFI (for correspondence), Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture, CH-8820 Wadenswil; Dr. B. WERMELINGER, Swiss Federal Institute for Forest, Snow and Landscape Research, CH-8903 Birmensdorf; Dr. E. F. BOLLER, Swiss Federal Research Station for Fruit-Growing, Viticulture and Horticulture, CH-8820 Wadenswil, Switzerland