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Published online 1 September 2007
Published in Crop Sci 47:2047-2057 (2007)
© 2007 Crop Science Society of America
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CROP PHYSIOLOGY & METABOLISM

Photosynthetic Response of Cotton to Spider Mite Damage: Interaction with Light and Compensatory Mechanisms

A. A. Reddalla, L. J. Wilsona,*, P. C. Greggb and V. O. Sadrasc

a CSIRO Plant Industry and Cotton Catchment Communities CRC, Locked Bag 59, Narrabri NSW 2390, Australia
b The Univ. of New England and Cotton Catchment Communities CRC, Armidale NSW 2351, Australia
c South Australian Research and Development Institute–School of Agriculture, Food & Wine, The Univ. of Adelaide, Waite Campus, Australia

* Corresponding author (lewis.wilson{at}csiro.au).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We investigated the photosynthetic responses of cotton (Gossypium hirsutum L.) leaves to two-spotted spider mite (Tetranychus urticae K.) damage. Light-response curves of mite-infested (+M) and uninfested (– M) leaves diverged as mite populations increased. At 17 adult female mites per leaf, photosynthetic rate of +M leaves at photosynthetic photon flux density of about 1600 µmol m–2 s–1 was halved from 31 µmol CO2 m–2 s–1 in –M to 16 µmol CO2 m–2 s–1 in +M but there was no effect on either respiration or apparent maximum quantum yield. This has important implications when comparing the response to mites of individual leaves versus canopies. In the field (i) photosynthesis declined with crop age, but the rate of decline was faster in mite-infested leaves, and (ii) mite damage progressed downward in the canopy and from basal to distal leaf positions. We found no evidence of within-leaf (i.e., basal vs. distal section) or within-plant (top vs. mid or bottom leaf) increases in photosynthesis in compensation for mite damage, except for a minor enhancement of photosynthesis in bottom leaves of mite-infested crops due to greater light penetration in canopies severely defoliated by mite damage.

Abbreviations: DAS, days after sowing • +M, mite treatment (plants artificially infested with mites) • –M, control treatment (no mites) • PPFD, photosynthetic photon flux density

Photosynthetic Response of Cotton to Spider Mite Damage: Interaction with Light and Compensatory Mechanisms

A. A. Reddalla, L. J. Wilsona,*, P. C. Greggb and V. O. Sadrasc

a CSIRO Plant Industry and Cotton Catchment Communities CRC, Locked Bag 59, Narrabri NSW 2390, Australia
b The Univ. of New England and Cotton Catchment Communities CRC, Armidale NSW 2351, Australia
c South Australian Research and Development Institute–School of Agriculture, Food & Wine, The Univ. of Adelaide, Waite Campus, Australia

* Corresponding author (lewis.wilson{at}csiro.au).

We investigated the photosynthetic responses of cotton (Gossypium hirsutum L.) leaves to two-spotted spider mite (Tetranychus urticae K.) damage. Light-response curves of mite-infested (+M) and uninfested (– M) leaves diverged as mite populations increased. At 17 adult female mites per leaf, photosynthetic rate of +M leaves at photosynthetic photon flux density of about 1600 µmol m–2 s–1 was halved from 31 µmol CO2 m–2 s–1 in –M to 16 µmol CO2 m–2 s–1 in +M but there was no effect on either respiration or apparent maximum quantum yield. This has important implications when comparing the response to mites of individual leaves versus canopies. In the field (i) photosynthesis declined with crop age, but the rate of decline was faster in mite-infested leaves, and (ii) mite damage progressed downward in the canopy and from basal to distal leaf positions. We found no evidence of within-leaf (i.e., basal vs. distal section) or within-plant (top vs. mid or bottom leaf) increases in photosynthesis in compensation for mite damage, except for a minor enhancement of photosynthesis in bottom leaves of mite-infested crops due to greater light penetration in canopies severely defoliated by mite damage.

Abbreviations: DAS, days after sowing • +M, mite treatment (plants artificially infested with mites) • –M, control treatment (no mites) • PPFD, photosynthetic photon flux density


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The two-spotted spider mite (Tetranychus urticae K.) is an important secondary pest of cotton in Australia, with potential to cause severe reductions in lint and oil yield and in lint quality (Sadras and Wilson, 1996; Wilson, 1993; Wilson et al., 1991). Mites are known to reduce photosynthetic rate in a number of plant species including almonds [Prunus dulcis (Mill.) D.A. Webb.], oranges [Citrus sinensis (L.) Osbeck], tomato (Solanum lycopersicum L.), and cotton (Gossypium hirsutum L.) (Bondada et al., 1995; Hare et al., 1989; Royalty and Perring, 1989; Youngman and Barnes, 1986). In cotton, photosynthetic responses to mites have been researched from cytological (Bondada et al., 1995) to whole-canopy levels (Sadras and Wilson, 1997a). Most studies of mite effects on leaf-level photosynthesis, however, measured light-saturated photosynthetic rate. Understanding the effect of mites in partially shaded leaves is important because: (i) most leaves in the crop canopy are exposed to below-saturation light intensity, and (ii) in typical irrigated cotton crops in Australia, mites initially concentrate in nodes 3 to 5 below the main plant apex, but as populations build they move down to nodes 5–15 below the terminal (Wilson and Morton, 1993).

Equation [1] relates net photosynthetic rate (Pnet) and light incident at the leaf surface (Q):

Formula 1[1]
where R, the gas exchange rate at Q = 0, is taken as a measure of dark respiration, b is a fitted parameter, related to curvature, which multiplied by Pmax gives an estimate of the apparent maximum quantum yield, and Pmax is the light-saturated photosynthetic rate (Constable and Rawson, 1980; Connor et al., 1993; Peek et al., 2002). Elucidating the mechanisms of mite effects on leaf photosynthesis in terms of the parameters of the light-response curve is essential to link leaf and canopy photosynthetic responses. Reduction in Pmax would be more important in young, well-lit leaves at the top of the canopy, whereas reduced apparent maximum quantum yield would be more important in leaves which are under a prevalent nonsaturating regime. Putative increase of respiration in mite-damaged leaves is particularly important for the low-lit "overdraft" layer of the canopy, where leaves are predominantly below their compensation point (Thomas and Sadras, 2001).

There are also knowledge gaps in relation to compensatory photosynthesis in mite-infested cotton. The relationship between radiation-use efficiency and intensity of mite infestation found by Sadras and Wilson (1997a) suggested some degree of compensation for mite damage. Nowak and Caldwell (1984) indicate that within-plant compensation occurs in herbivore-infested plants when the photosynthetic rate of undamaged leaves or undamaged portions of damaged leaves increases in relation to foliage of the same age on uninfested plants. These compensatory responses to herbivory may be mediated by one or more of the following processes: (i) changes in assimilate transport or use that overcome inhibition caused by accumulation of assimilate in leaves, (ii) reduction in leaf area which may improve water availability to undamaged leaves, (iii) increased chlorophyll content of remaining or new leaves, (iv) increased cytokinin level that could enhance CO2 fixation and delay senescence of undamaged leaves (Trumble et al., 1993). There is also evidence for other mechanisms of increased crop photosynthesis in response to herbivory that involve changes in canopy structure and light distribution (Sadras, 1996; Holman and Oosterhuis, 1999). In comparison to undamaged controls, Sadras (1996) found a 20 to 27% increase in radiation-use efficiency of well-fertilized, low density cotton crops where reproductive structures were manually removed to simulate damage by Helicoverpa spp. More recently, Holman and Oosterhuis (1999) confirmed this response in a study where increased photosynthesis was measured in mid canopy leaves (node 8 below terminal) or whole canopies in response to loss of flower buds, which triggered a changed canopy structure allowing a better light distribution. Some studies have shown no evidence of compensatory photosynthesis; for instance, Lei and Wilson (2004) found that the photosynthetic rate of cotton seedlings damaged by thrips was no different from undamaged plants and therefore could not explain the compensatory growth that occurred in damaged plants.

However, spider mites are mesophyll feeders, and their mode of action is fundamentally different from that of the herbivores investigated in the previous studies, which were predominantly defoliators or cause shedding of reproductive structures. Reddall et al. (2004) found no evidence of increased photosynthetic rate in undamaged portions of mite-infested leaves in the upper canopy, but the possibility of compensation in lower leaves was not reported. Spider mite damage can result in reduced leaf size, internode length, and plant height, and if damage is severe, loss of upper leaves (Reddall, 2000). This could alter the canopy structure, changing the light environment, and allowing more light to mid and lower canopy leaves, resulting in elevated photosynthetic rate of those leaves compared with similar aged leaves on undamaged plants.

The aims of this study were to (i) quantify the effect of mites on the parameters of the light-response curve of photosynthesis (Exp. 1), (ii) characterize the spatial and temporal patterns of mite effects on photosynthesis, and (iii) seek evidence for compensatory photosynthesis by comparison of rates in basal (preferred by mites) and distal leaf sections, and in leaves at two to three positions in the canopy (Exp. 2 and 3). This information will be valuable in understanding how mite damage at the leaf level translates to effects at the canopy level, especially taking into account the possibility of compensatory photosynthesis which has received little attention in cotton–arthropod studies. In future, this information will also assist efforts to model the effects of mites on cotton growth, yield, and fiber quality via effects on radiation use efficiency (Sadras and Wilson, 1997b), which may be valuable in pest management decisions for mite control.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All experiments were done at the Australian Cotton Research Institute, Narrabri (30°S, 150°E), NSW, Australia.

Experiment 1: Light-Response Curves of Mite-Damaged Leaves
Cotton cv. Nucotn 37 was grown in 10-L pots filled with top-soil from a cracking gray clay Vertisol. Three seeds were sown per pot, on 7 Dec. 1998, and were later thinned to one seedling per pot. Forty pots were arranged in the open in 10 rows spaced 0.4 m apart from the pot perimeters, with 0.6 m between each pot within each row, yielding a density of 5 plants m–2. Plants were well fertilized and fully watered with an automated dripper system.

The pots were assigned randomly to one of two treatments: control, no mites (–M) or plants artificially infested with mites (+M). The +M treatment was established 70 d after sowing (DAS), when four adult female mites were placed on the first fully expanded mainstem leaf from the top of the plant (L1 leaf). This leaf position, usually the fourth node from the top, is most likely to contain the highest mite density in naturally infested cotton (Wilson and Morton, 1993). A fine brush was used to transfer each mite individually from mite-infested cotton seedlings, reared in a glasshouse, to the plants. The mite population of each plant was assessed weekly by counting the number of adult female mites on the L1 leaves. Adult female mites provide a good surrogate for the total mite population (Carey, 1983). Full details and justification of mite sampling procedures are given in Wilson and Morton (1993). Acaricide (Agrimec [18 g L–1 abamectin, Syngenta Crop Protection Australia, Sydney, Australia] applied at 0.09 g ai abamectin L–1) was sprayed when necessary to control mites in the –M plants.

Photosynthesis was measured at 65, 81, and 94 DAS, on clear, sunny days between 1030 and 1530 h. Four plants were randomly selected from each treatment and gas exchange and photosynthetic photon flux density (PPFD) measurements were taken from the basal section of an L1 leaf from each plant using the Li-Cor, LI-6400 (Lincoln, NE) portable photosynthesis system with a clear leaf chamber covering an area of 6 cm2 which was clamped onto the leaf, as described by Reddall et al. (2004). Photosynthetic rate was measured in leaves exposed to full sunlight (PPFD > 1600 µmol m–2 s–1) and in leaves shaded with a combination of black tulle, black shade cloth, and heavy duty black plastic reducing average PPFD to 1307, 950, 675, 379, 21, and 0 µmol m–2 s–1. Shading material was mounted on 50 by 50 cm steel frames placed over the target leaf. To allow stomata to adjust to the shaded conditions each incremental level of shade was maintained for 20 min before the measurements were made, beginning with full sunlight and working progressively to the lowest PPFD (Petersen et al., 1991).

Experiments 2 and 3: Temporal and Spatial Patterns of Photosynthesis and Compensation
The effect of mite damage on the photosynthetic rate of leaves of differing age and position in the canopy profile was investigated in field crops over two seasons (Season 1, 1996–1997; Season 2, 1997–1998). The experiments have been described by Reddall et al.(2004). Briefly, Nucotn 37 cotton crops were grown during two seasons under high input crop agronomy. There were two mite treatments, –M, control (no mites), and +M, crops artificially infested with mites, in a randomized block design with four replications (eight plots). The cotton was sown on beds 1 m apart at about 12 plants m2 and each plot was eight rows by 18 m (Season 1) and eight rows by 15 m (Season 2). Details of mite infestation methods and management are in Wilson (1993). Briefly, mites were mass reared on cotton seedlings in a glasshouse then transferred to the +M plots at a density of about five infested seedlings per meter to initiate a field infestation. The exact number of mites transferred per plant or square meter was not assessed; this is unnecessary as the number of mites established per leaf was recorded during each experiment (see below). As the mites can be transferred from plot to plot on clothing and by air currents there was always the risk of contamination of –M plots with mites, and a selective acaricide (Agrimec applied at 5.4 g ai abamectin ha–1) was used to control these unwanted infestations as needed.

Measurements of mite abundance, photosynthetic rate, PPFD, and relative chlorophyll content were made on a weekly basis. In Season 1, we measured these parameters on leaves in three positions: L1, defined as before; L2, at the 14th node from the base of the plant, and L3 at the 10th node from the base. Positions L1 and L2 were sampled in the second season. Data for L1 leaves were partially discussed in Reddall (2000). This provided a leaf near the top of the plant, which is the preferred feeding position of mites (Wilson and Morton, 1993), and also in the mid (L2) and lower (L3) canopy where mites are less abundant and where some within-plant compensation for mite damage to upper leaves (e.g., L1) could occur. The position of the L1 leaf measured remained constant relative to the plant terminal but was at a progressively higher node position in relation to the cotyledons as the season progressed. Because the leaf that occupied this position changed from week to week the fate of particular leaves over time was not studied. Instead, a new plant was tagged in each plot each week (i.e., mite numbers, relative chlorophyll content, and gas exchange were measured on three leaves [L1– L3] in Season 1, or two leaves [L1 and L2] in Season 2 on each of four plants per plot, the following week similar measurements were made on four new plants in that plot and so on). On each measurement date the number of adult female mites was counted on the underside of each leaf measured.

Measurements of gas exchange and relative chlorophyll content were taken from the basal (near the junction with the petiole) and distal leaf portions (near the leaf edge farthest from the petiole junction) of each leaf as described in Reddall et al. (2004) to assess within-leaf compensation. At each position gas exchange variables were measured with the LI-6400 portable photosynthesis system with a clear leaf chamber covering an area of 6 cm2. Measurements were taken within the period of 3 h either side of solar noon using ambient light when the PPFD reaching the adaxial leaf surface of the L1 leaves was greater than 1600 µmol m–2 s–1. Chamber conditions used ambient CO2, the chamber temperature was set to 2°C below ambient to allow for slight heating when the chamber is clamped on the leaf (usually between 25 and 35°C) and relative humidity was controlled to between 60 and 70% using air flow rate and moisture scrubbers. While measurements were being taken, the L1 leaves were held perpendicular to the sun, while L2 and L3 leaves were measured in their natural position at the ambient light level, which was often considerably less than that of the L1 leaves. This was done to estimate the effects of mites on leaves in the light environment in which they were functioning, which meant that L2 and L3 leaves would often be functioning at a lower level than L1 leaves due to less light. This approach also avoided long acclimation times (>30 min) required if the L2 or L3 leaves had been exposed to higher light levels to estimate their maximum photosynthetic capacity. Photosynthetic rates were measured approximately 2 min after the chamber was placed over the leaf to allow stabilization of readings. PPFD was measured at the same time as photosynthesis using the sensor on the LI-6400. For both the gas exchange parameters and PPFD, each measurement was the average of five consecutive readings, taken sequentially at 2-s intervals. Leaf relative chlorophyll content was measured using a SPAD 501 chlorophyll meter (Minolta, Osaka, Japan), which has been tested in a number of plant species, including cotton (Wood et al., 1992).

Relative chlorophyll content was measured in basal and distal portions (average of five separate measurements) of the same mite-infested and control leaves used for photosynthesis measurements. Data was analyzed and presented in SPAD units.

Statistical Analyses
Genstat 8 (Payne et al., 2005) was used for all statistical analysis except the fitting of the light curves for Experiment 1. Effect of mite treatments (+M vs. –M) on all response variables was assessed with analysis of variance. Nonlinear regression in S-PLUS (Insightful Corporation, 2001) was used to fit and compare nonlinear curves (Eq. [1]) for data from Experiment 1.


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Light-Response Curves of Mite-Damaged Leaves
Once established, mite colonies grew exponentially to an average of 17 adult female mites per leaf at L1 whereas acaricide treatment controlled mites effectively in controls (Fig. 1 ). The photosynthetic response to PPFD was not significantly different between +M and –M treatments at 65 DAS, before mite addition, and at 85 DAS when mite populations in infested plants averaged four adult female mites per leaf (Fig. 2 ). At 94 DAS, when mites in +M leaves averaged 17 adult female mites per leaf, the light curves of the +M and –M plants diverged substantially. This was tested by fitting a general nonlinear model of Eq. [1] to all data (+M and –M), then adding a separate term for each treatment for each parameter (Pmax, R, and b) and testing if this significantly improved the fit of the model. The analysis indicated that the fitted parameters Pmax and b were significantly different between the +M and –M treatments (P < 0.001 in both cases) while R was not (Fig. 2). The apparent maximum quantum yield (Pmaxb) was the same for both treatments (0.04 mol CO2 mol–1). At 94 DAS the photosynthetic rate of +M leaves was significantly less than that of –M leaves, for a given PPFD level. Estimated Pmax in +M treatments was 50% lower than in –M treatments.


Figure 1
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  		Figure 1. Number of adult female T. urticae per leaf for L1 leaves in mite-infested and control plants grown in pots in the field. Error bars 2 SEM, and are not shown when smaller than the symbol.

 

Figure 2
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  		Figure 2. Relationship between net photosynthesis and photosynthetic photon flux density (PPFD) for mite-infested (+M) and control (–M) leaves of cotton plants grown in pots in the field. Effect of mite treatment for each PPFD level is ns = not significant; ** P < 0.01; *** P < 0.001. Boxes show parameters (mean ± SE) of the light-response curve (Eq. [1]), i.e., light-saturated photosynthesis (Pmax, µmol CO2 m–2 s–1), respiration (R, µmol CO2 m–2 s–1), and a fitted parameter of curvature [b, (µmol m–2 s–1) –1]. DAS, days after sowing.

 
Temporal and Spatial Patterns of Photosynthesis and Compensation
Acaricide treatments were effective in controlling mites in the –M treatment (data not shown). Once established, mite colonies tended to grow exponentially in +M crops (Fig. 3 ). Start of rapid colony growth and peak numbers both were delayed in the bottom of the canopy compared with the top (e.g., compare L2–L3 to L1).


Figure 3
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  		Figure 3. Number of adult female T. urticae in top (L1), medium (L2), and low (L3) canopy positions of mite-infested crops during two seasons. Error bars are 2 SEM and are not shown when smaller than the symbol. DAS, days after sowing.

 
Figures 4 and 5 show the dynamics of leaf photosynthesis accounting for variation in leaf position in the canopy, and for basal and distal leaf sections. Photosynthesis declined with crop age in all leaves. The rate of decline, however, was faster in mite-infested leaves, particularly in Season 1. Mite effects were first detected in apical leaves, and progressed downward in the canopy. Within leaves, photosynthetic reduction attributable to mites was detected first, and was more pronounced, in basal leaf positions, where mites prefer to establish and feed. Late in Season 1, the photosynthetic rate of leaves at the bottom of the canopy (L3) was significantly greater in +M crops than in controls. This was associated with defoliation of the upper section of the canopy (Reddall, 2000) and consequent increase in PPFD incident at the bottom of mite-damaged crops (Fig. 6 ). Mites reduced the relative chlorophyll content of cotton leaves in both seasons but only in the basal positions where colonies were established (Fig. 7 , 8 ). Late in Season 2, bottom leaves of mite-infested crops had greater relative chlorophyll content than leaves in control crops.


Figure 4
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  		Figure 4. Net photosynthetic rate of leaves in top (L1), medium (L2), and low (L3) canopy positions in Season 1. Measurements were taken in basal and distal leaf sections. Error bars are 2 SEM and asterisks indicate mite effects: *P < 0.05; **P < 0.01; ***P < 0.001.

 

Figure 5
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  		Figure 5. Net photosynthetic rate of leaves in top (L1), and medium (L2) canopy positions in Season 2. Measurements were taken in basal and distal leaf sections. Error bars are 2 SEM and asterisks indicate mite effects: *P < 0.05; **P < 0.01.

 

Figure 6
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  		Figure 6. Dynamics of photosynthetic photon flux density (PPFD) incident at the leaf surface for leaves in mid (L2) and bottom (L3) canopy positions in mite-infested (+M) and uninfested controls (–M) in Season 1. Measurements were taken in basal and distal leaf sections. Error bars 2 SEM, and asterisks indicate significance on mite effects: *P < 0.05, **P < 0.01, ***P < 0.001.

 

Figure 7
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  		Figure 7. Relative chlorophyll content of leaves in top (L1), medium (L2), and low (L3) canopy positions of mite-infested (+M) and control (–M) crops in Season 1. Measurements were taken in basal and distal leaf sections. Error bars are 2 SEM and asterisks indicate mite effects: *P < 0.05, **P < 0.01, ***P < 0.001. See "Methods" for an explanation of SPAD units.

 

Figure 8
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  		Figure 8. Relative chlorophyll content of leaves in top (L1), medium (L2), and low (L3) canopy positions of mite-infested (+M) and control (–M) crops in Season 2. Measurements were taken in basal and distal leaf sections. Error bars are 2 SEM and asterisks indicate mite effects: *P < 0.05, **P < 0.01. See "Methods" for an explanation of SPAD units.

 

   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
A Mitscherlich-type model provided physiologically adequate descriptions of the response of net photosynthesis to irradiance, and captured important changes in leaf performance in response to mites. All three parameters of the curve obtained from our pot-grown plants agreed closely with those reported for irrigated cotton crops (Milroy and Bange, 2003). The main effect of mites was to reduce light-saturated photosynthesis, with no effects on either respiration or apparent maximum quantum yield. The lack of mite effects on leaf photosynthesis at low light intensity, i.e., PPFD below 400 µmol m–2 s–1, may be related to their feeding habit, where damage is initially caused on the abaxial leaf surface, within the spongy mesophyll layer (Welter, 1989). Evans et al. (1993) has shown that there is a gradient in light absorption, and hence photosynthetic capacity, through Eucalyptus leaves which affects the shape of the light-response curves. It is possible that at low light levels, most light is being absorbed by the undamaged adaxial layers (epidermis and palisade cells) of mite-damaged leaves, hence there is little or no effect on photosynthesis compared with undamaged leaves. As light levels increase and there is greater penetration of light through the leaf, the effect of mite damage to spongy mesophyll means these cells, in damaged areas, are less active than similar cells on undamaged leaves.

The lack of photosynthetic response to mites under low light may have implications for partially shaded leaves in the canopy profile, and is important for scaling-up growth calculations from leaf to canopy. The level of light at which mite damage results in a reduction in photosynthesis, however, may be variable as light-response curves may differ at different canopy positions (Campbell et al., 1992), with lower/older and very young cotton leaves higher in the canopy reaching light saturation at lower irradiance than fully expanded leaves in the upper mid canopy (Constable and Rawson, 1980).

As both the leaf and mite populations were included in the LiCor 6400 chamber in all experiments we calculated the likely CO2 contribution of the mites to see if it could significantly affect photosynthesis calculations. Estimates of the respiration rate (nL O2 µg live weight–1 h–1) of mite adults, nymphs, and eggs of T. cinnabarinus Boisduval, which is closely related to T. urticae, were obtained from Thurling (1980). These were converted to micromoles of CO2 per microgram live weight per hour, then to micromoles of CO2 per mite stage per hour. The peak density of adult female mites at 94 DAS was about 17 mites leaf–1. Using the stable age distribution found by Carey (1983) we calculated the number of mite nymphs and eggs expected for a population of 17 female mites (males are not abundant), then multiplied this up to a square meter assuming an average fully expanded cotton leaf has an area of about 70 cm2 (Wilson, 1994). This provided an estimate of micromoles of CO2 for each mite stage per square meter per hour, which was then divided by 3600 to provide CO2 production in micromoles of CO2 for each mite stage per square meter per second. This was totaled across mite stages to yield a value of 0.0026 µmol CO2 m–2 s–1 which is about 1/10,000th of the CO2 (31 µmol CO2 m–2 s–1) exchanged by control leaves at 94 DAS (e.g., 0.0026/31), so the contribution of mite respiration to the results was trivial, at a density of 17 adult mites leaf–1 in the light response experiment, or even at the peak of 60 adult females leaf–1 at L1 in Season 2.

Wilson (1993) and Wilson and Morton (1993) characterized mite distribution in canopy profiles and individual leaves through the crop cycle for typical irrigated cotton crops in Australia. At the canopy level, colonies are usually established around the fourth node from the top (L1 in this paper), and move downward later in the season. At the level of individual leaves, colonies are first established in basal leaf sections, where they are relatively protected under the thicker boundary layer associated with thicker leaf veins. The spatial and temporal dynamics of leaf photosynthesis in our field experiments (Fig. 4 and 5) reflected the combined effect of crop ontogeny and mite dynamics. Photosynthesis declined with crop age, but the rate of decline was generally faster in mite-infested leaves, particularly the L1 leaves in the upper canopy. The "wave" of mite damage, as reflected in reduced photosynthesis and relative chlorophyll content, progressed downward in the canopy and from basal to distal leaf positions. Though mites reduced photosynthesis in lower leaves (L1 and L2) the effect of lower light intensity, due to shading was probably the most limiting factor, especially for L3 leaves. Temporal and spatial patterns in photosynthesis thus closely reflected the temporal and spatial distribution of mites in both the canopy profile and within leaf sections and also leaf position, with L2 and L3 leaves having lower photosynthesis than L1 leaves due to less light.

The response of canopy radiation use efficiency (i.e., biomass per unit intercepted radiation) to mite infestation reported by Sadras and Wilson (1997a) had two phases. Little or no response for infestations below about 20 adult females per leaf, measured at L1, followed by a sharp reduction in canopy radiation use efficiency for more intense infestations. Here we measured photosynthetic rate in basal and distal leaf sections, and in leaves from upper (L1), middle (L2), and lower (L3) sections of the profile. These direct measurements revealed no compensatory photosynthesis in the early stages of infestation. Distal leaf sections had similar relative chlorophyll concentration and similar photosynthetic rates in +M and –M plants. For most of the growing season, the photosynthetic rate of undamaged leaves in damaged plants (leaves L2 and L3) was similar to that in their uninfested counterparts. These results therefore indicate that the stability of crop photosynthesis reported by Sadras and Wilson (1997a) for the early stages of mite infestation is not due to within-plant or within-leaf increases in photosynthesis in undamaged areas. Instead it is likely that at low levels of mite damage a relatively small proportion of the crop leaves are affected—hence reduction in photosynthesis, though significant on the leaves affected, is not significant when viewed at the crop level. As mite populations increase they spread not only to lower main-stem leaves but also to secondary leaves on both vegetative and fruiting branches (Carey, 1982). Hence, it is likely that an increasing mite population leads to damage on an increasing proportion of leaves, and to a larger effect on crop photosynthesis.

Compensatory photosynthesis was found at the crop level in advanced stages of mite infestation, when upper portions of the crop (e.g., L1 and young and fully expanded leaves in this zone of the canopy) were severely damaged, causing rapid leaf senescence. This allowed for greater PPFD incidence in and regreening of bottom leaves, which accounted for their increased photosynthetic rate. Seventy-five percent of the variation in the rate of photosynthesis of bottom leaves in +M and –M plants was explained by variation in PPFD (data not shown). The contribution of this compensatory mechanism to whole-plant C economy is likely to be negligible, as the photosynthetic rate of leaves at the bottom of the canopy was very small. The regreening at the bottom of the open canopy following severe mite infestation, however, may be important in other systems, such as perennials that could therefore initiate active regrowth.


   ACKNOWLEDGMENTS
 
We thank Greg Constable and Tom Lei (CSIRO) for valuable comments on an early draft of this manuscript and Bob Forrester (CSIRO), Bruce McCorkell, and Steve Harden (New South Wales Department of Primary Industries) for assistance with statistical analysis. This research formed a portion of a Ph.D. dissertation submitted to the University of New England, Armidale, Australia. The Cotton Research and Development Corporation provided substantial funding for this project (grant no. CSP60C).


   NOTES
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 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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Received for publication November 8, 2006.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 





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