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CROP PHYSIOLOGY & METABOLISM

Cotton Photosynthesis and Carbon Partitioning in Response to Floral Bud Loss Due to Insect Damage

^a Northeast Res. Stn., Louisiana State Univ. Agric. Center, St. Joseph, LA 71366 USA
^b Dep. of Agronomy, Univ. of Arkansas, Fayetteville, AR 72701 USA

mholman{at}agctr.lsu.edu

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
To understand better cotton (Gossypium hirsutum L.) plant compensation for early-season floral bud (square) loss due to insect damage, a field study was conducted in 1994 and 1995 at Marianna, AR. The control treatment was protected by insecticide applications, while tarnished plant bugs (Lygus lineolaris Palisot de Beauvois) and bollworms (Helicoverpa zea Boddie) were released in the plots of the other treatment three times before flowering. Square abscission at the first sympodial fruiting position was 5 and 33% for the control and infested plants, respectively, and yield was reduced 21% by insect infestation. Insect treatment resulted in 4% more light penetration through the canopy, which may have contributed to the 17% increase in photosynthesis of the eighth main-stem leaf from the terminal leaf as compared with the control plants. Canopy photosynthesis recorded 4 wk after the initiation of flowering was 21% higher in the infested plants. CO₂ labeling showed infestation also resulted in more ¹⁴C recovered in the terminal node (terminal leaf plus main stem above the terminal leaf) and less remaining in the branch at the same node as the source leaf, which corresponded to an increase in plant height, although node number was not affected. Since our insect-induced abscission treatments had similar effects as manual fruit removal treatments reported by others, future studies seem justified in using either approach. Early fruit loss in the U.S. Mid-south results in changes in carbon exchange and allocation, but poor late-season growing conditions often prevent yield compensation.

Abbreviations: CER, CO₂ exchange rate • RUE, radiation-use efficiency • NAWF, nodes above white flower • DPM, disintegrations per minute • HVI, high volume instrument • DAP, days after planting

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
KEY INSECT PESTS of cotton have been shown to feed preferentially on flower buds (squares) and young bolls (Hearn and Fitt, 1992; Williams et al., 1987). Investigation of cotton plant responses to herbivory are complicated by the indeterminate, perennial growth habit of cotton. Numerous studies have examined the effect of square loss on cotton yield with responses ranging from slight yield increases to dramatic decreases (for a review, see Sadras, 1995). In describing individual plant compensation to square loss, Sadras (1995) defined four types of responses as distinguished in previous work (Hearn and Room, 1979; Kletter and Wallach, 1982; Brook et al., 1992). One is passive and instantaneous, in that squares are damaged that would shed physiologically anyway. A second is passive and time dependent, whereby squares that would abscise for reasons other than insect damage are instead retained, replacing those lost to insect damage. A third type is active and instantaneous, where resources (carbon, water, and minerals) that would have been partitioned to the damaged squares are partitioned to undamaged ones (leading to larger fruit). The fourth is active and time dependent, where the loss of squares leads to prolonged vegetative growth thus creating additional fruiting forms. These plant responses are not mutually exclusive, and, in many cases, no single response hypothesis can be used to explain observed field responses.

Plant responses as defined by Sadras (1995) are based mainly on the complexities of plant carbon partitioning and the dynamics of resource allocation, which are complex and not well understood. Brook et al. (1992) suggested that early insect damage to squares could extend the period of canopy expansion with a concomitant increase in light interception and growth in crops with incomplete canopy closure. Although leaf area is a major variable affecting the ability of the plant to gain carbon, other factors such as a greater leaf nitrogen content that may increase photosynthetic rate per unit area could also be important (Sinclair and Horie, 1989). Sadras (1996) recently reported that removal of fruiting structures did not affect radiation-use efficiency (RUE) when plant population was high and nitrogen supply was low. However, with a high nitrogen supply and low plant population, manually induced fruit loss resulted in 20 to 27% higher RUE than in the control, which was more related to changes in plant structure than to variation in leaf nitrogen (Sadras, 1996). However, the timing of square and boll removal reported by Sadras (1996) was from 57 to 85 d after planting (DAP); it remains to be seen whether square removal at an earlier date results in a similar physiological response. Active and time dependent plant responses to square loss, such as the changes in plant architecture reported by Sadras (1996), it would seem should be sensitive to the length of the effective growing season and the environmental conditions during that growing season. It is not known whether the growing season and environmental conditions in the Mid-South region of the U.S. cotton belt are adequate for the plant responses reported from Australia by Sadras (1996). In the U.S. mid-south, Pettigrew et al. (1993) reported that manual removal of squares did not affect CO₂ exchange rate (CER) of the upper-most fully expanded leaf, crop growth rate, or net assimilation rate of cotton plants during three periods following square removal. However, the crop growth rates and net assimilation rates (Pettigrew et al., 1993) did not include root dry weights.

Most of the aforementioned experiments made the assumption that manual removal of squares was sufficiently similar to actual pest damage to justify its use in establishing treatments (Brook et al., 1992; Dale, 1959; Sadras, 1995, 1996). While this approach greatly simplifies treatment establishment, it fails to address the possibility that a number of effects associated with insect feeding could possibly alter plant response, such as release of toxins or natural plant hormones by insects, remobilization of resources from damaged squares before abscission, altered balance of endogenous hormones by the plant in response to the damage, induced antibiosis by the plant against the feeding arthropod, and insect preference for a square at one position over another (Burden et al., 1989; Stewart and Sterling, 1989; Tugwell et al., 1976). Therefore, this study was designed to observe the effect of early-season square loss from insect feeding on cotton plant growth, photosynthesis, and carbon partitioning in the U.S. mid-south in an attempt to better explain plant resource allocation following early square loss.

	Materials and methods

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In 1994 and 1995, a field study was conducted at the Cotton Branch Experiment Station in Marianna, AR, on a Loring silt loam (thermic Typic Fragiuadalf). The cotton cultivar Deltapine 51 was planted on 10 May 1994 and 16 May 1995. The experiment design was a randomized complete block with two treatments and three replications. Plot size was four rows 15 m long, spaced 0.9 m apart with two or four row skips between plots. However, only 6 m from the middle portion of the two middle rows of each plot was treated with the remainder left to act as a border, in an attempt to limit insect movement down the row into an adjoining plot. Plots were thinned to a uniform plant density of eight plants per meter of row after emergence. Furrow irrigation was applied as needed each year in order to avoid limiting plant response from the treatments. Crop management decisions were based on the standard practices recommended by the Arkansas Cooperative Extension Service (Bonner, 1994).

Treatments
To limit insect damage, lambda-cyhalothrin ([1(S*),3(Z)]-(±)-cyano-(3-phenoxyphenyl)methyl-3-(2-chloro-3,3,3-trifluoro-1-propenyl)-2,2-dimethylcyclopropanecarboxylate) was applied to the control treatment with a CO₂ backpack sprayer at 0.028 kg ai/ha at first visible square, late squaring, and first bloom. Dates of application were 39, 46, and 53 DAP in 1994 and 40, 47, and 54 DAP in 1995. The other treatment (insect infested) was established by releasing tarnished plant bugs and bollworms into the appropriate plots.

One tarnished plant bug nymph was released onto the main-stem of every other plant once weekly for three weeks beginning the week following first visible square (40, 47, 54 DAP in 1994 and 41, 48, and 55 DAP in 1995). The afternoon before insects were released, tarnished plant bug nymphs were collected with a sweep net from wild hosts and placed in buckets with either sprouted potato (Solanum tuberosum L.) or common bean (Phaseolus vulgaris L.), and placed in an air-conditioned room for the night. The following morning before 0900 h, the nymphs were transferred onto cotton plants with a paper straw approximately 3 to 6 cm long. The paper straws had one end plugged with bridal vail to prevent insect passage through the straw when negative air pressure was applied. Pressure was applied by placing the straw into the tip of a glass tube with a piece of flexible rubber tubing attached to the end creating a modified aspirator. The nymphs were then aspirated into the end of a straw and while pressure was applied to keep them inside, the applicator placed a finger over the end of the straw trapping the nymph inside. The straw was then withdrawn from the glass tube and taped to the base of the plant stem, open end up, thus allowing the nymph to escape onto the plant.

In addition to the tarnished plant bugs, one bollworm was released onto every other plant once each year (55 and 56 DAP, in 1994 and 1995, respectively). Bollworm larvae (1–2 instars) were obtained from a population maintained at the University of Arkansas (Biocontrol Laboratory, Fayetteville, AR). Larvae were hand-placed on the highest, visible, first position square. All plots were sprayed with lambda-cyhalothrin (0.039 kg ai/ha) at 62 and 63 DAP in 1994 and 1995, respectively.

Measurements
First position square counts, plant height, and number of main-stem nodes (above the cotyledonary node) were taken immediately before first flower in both years. The number of nodes above white flower (NAWF) were recorded according to Bourland et al. (1992) in order to document treatment effects on crop maturity. Counts of NAWF were taken twice weekly beginning at first flower and continuing for approximately 5 wk.

In 1995, single leaf CER measurements were taken at 91 DAP with a LI-6200 portable photosynthesis system (LI-COR Inc., Lincoln, NE) on the fourth and the eighth main-stem leaves from the terminal leaf (three undisturbed leaves at each position per plot). Canopy photosynthesis was taken once during peak flowering at 64 and 73 DAP, in 1994 and 1995, respectively, and again late in the fruiting period at 92 and 93 DAP in 1994 and 1995, respectively. Measurements were taken with a LI-6200 portable photosynthesis system attached to a clear plastic cube (1 by 1 by 1 m) with an open base that could be placed over 1 m of crop row for gas exchange measurements (Wullschleger and Oosterhuiset, 1990b). All readings were made between 1230 and 1430 h on cloudless days when ambient photosynthetic photon flux density exceeded 1700 µmol m^-2 s^-1. Light penetration through the canopy was measured (95 and 91 DAP in 1994 and 1995, respectively) by recording the amount of photosynthetically active radiation (PAR) immediately above and below the canopy (I_o and I, respectively) with an LI-191B line quantum sensor (LI-COR Inc.). The sensor was inserted perpendicularly into the rows at ground level. Measurements were made between 1200 and 1330 h with 4 sub-samples per plot. Instantaneous light extinction coefficients (k) were calculated as the ratio between ln (I/I_o) and leaf area index (LAI). Plants from 1 m of row per plot were harvested (95 and 91 DAP in 1994 and 1995, respectively) for leaf area [determined with a LI-3100 leaf area meter (LI-COR Inc.)] and dry weight determination.

Three plants from each treatment were randomly chosen for short exposure to ¹⁴CO₂ to investigate changes in carbon translocation within the plant. Procedures were adapted from Ashley (1972). At 95 and 91 DAP in 1994 and 1995, respectively, the upper-most, fully expanded main-stem leaf from each plant was covered with a plastic bag (1 L) tightly sealed to the petiole with plastic tape. An open vial was attached to the inside of the bag, and a septum cap was also attached to the side of the bag. The vial contained 1.5 mL of 0.0003 M NaH¹⁴CO₃ (specific activity 2.1 x 10⁹ Bq mmol^-1) into which 4 mL of 2.5 M lactic acid was injected through the septum into the vial, thus releasing ¹⁴CO₂ into the bag. The bags were kept in place for 15 min and removed. The plants were harvested 3 d later, and separated into component parts of interest [branch three nodes below the source, branch on node below the source, terminal node (terminal leaf plus the main stem above the terminal leaf), and the source branch). Plant material was dried in a forced-draft oven to constant weight at 60°C, ground, a sub-sample combusted in a sample oxidizer (R. J. Harvey Instrument Corp., Hillsdale, NJ), and carbon was trapped in a carbo-trap, scintillation cocktail mixture. The disintegrations per minute (DPM) of each sample were counted with a Packard Tri-Carb 4530 liquid scintillation spectrophotometer (Packard Instrument Co., Downers Grove, IL) for 10 min or 10000 counts (which ever came first).

Yield was determined at final harvest during the first to second week of October in each year. Open bolls from two 1-m lengths of row were hand harvested from each plot. One randomly selected sample from the harvested seed cotton of each plot was ginned to determine lint percentage and fiber samples were analyzed for quality by HVI (Louisiana State University, Cotton Fiber Laboratory, Baton Rouge, LA.). Immediately prior to harvest, the fruiting positions of 10 plants per plot were mapped using COTMAP, a modified whole plant mapping program developed by Bourland and Watson (1990) to record plant structure and fruiting pattern at the end of each season.

Statistical Analysis
All data were statistically analyzed with the General Linear Model (GLM) procedures in the SAS statistical program (SAS Institute, 1990). Treatment means were not averaged across years in some cases because of significant year x treatment interaction. Treatment means were separated by Fisher's protected LSD at P 0.05.

	Results

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Averaged across years, the insect infestation resulted in 33% square abscission at the first sympodial fruiting position by first flower compared with only 5% first-position square abscission for the control (Table 1) . Plant height and number of sympodia were not affected by the treatments by first flower in either year (data not shown). However, at final harvest plant height was significantly increased in the infested treatment, although number of sympodia was not affected (Table 1). Treatment effects on NAWF were similar each year of the study with values declining at a slower rate in the infested treatment than in the control, thus the infested plants reached 5.0 an average of 7 d later than the plants in the control treatment (Table 1).

View larger version (23K): [in this window] [in a new window]   Fig. 1 Recovery of 14C from plant parts of infested and uninfected (control) cotton plants in 1994 and 1995, expressed as the percentage of the recovered 14C. Terminal node includes the leaf at the terminal node and the main stem above the terminal node. Bars with the same letter within the same plant part and same year are not significantly different (P > 0.05)

View larger version (15K): [in this window] [in a new window]   Fig. 2 Fruit production from sympodial branches (first, second, and outer positions from the main stem), monopodial branches, and extra-axillary positions in infested (damaged) and uninfested (control) cotton plants. Bars at each plant position with the same letter are not significantly different (P > 0.05)

	Discussion

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

Aboveground plant dry weight per unit area was unaffected by square loss (data not shown); however, root dry weight of the plants was not measured. Eaton and Rigler (1945) found that debudded plants had up to twice the root mass of undisturbed control plants. It is also possible that greater boll weight in the control plants offset gains in vegetative dry weight of the infested plants. Pettigrew et al. (1993) reported that in Mississippi early square loss did not affect crop growth rate or net assimilation rate; however, they also failed to take root growth into account. Sadras (1996) reported that under favorable growing conditions (low plant density, e.g., 5 plants m^-1, and high nitrogen), manual removal of fruit resulted in 1.6 times more dry matter production, which included the tap root. However, under unfavorable conditions (high plant density, e.g., 12.5 plants m^-1, and low nitrogen), fruit removal did not affect dry matter production. Although plants in this study received the recommended amount of nitrogen fertilizer, competition of the plant population of 8 plants m^-1 may have limited plant response to fruit loss.

In 1994, 24 d after the last insect release, the plants in the infested treatment exhibited a lower rate of canopy CER; however, this effect was not observed in 1995. Therefore, no explanation for the lower CER in the infested plants at the early measurement date in 1994 is offered. In contrast, canopy CER at later dates in both years was higher for the infested plants. This confirms the observations of Sadras (1996) that fruit loss increased seasonal RUE in cotton under good but not poor growing conditions. Sadras (1996) concluded that the increase in RUE with damage was more closely associated to changes in canopy structure than to changes in leaf nitrogen.

Sadras (1996) reported that bud removal resulted in longer internodes, more internodes, and branches that were more vertical than in the damaged plants which likely contributed to better light distribution and enhanced RUE. Our results also suggest that increased light penetration associated with high early square loss contributed to higher CER at lower leaf positions in the canopy (Table 2), which likely contributed to increased canopy CER late in the season.

Plants with less early fruit translocated more carbon to the terminal node, while the plants with more fruit allocated a greater proportion of carbon to sinks within the fruiting branch (Fig. 1a, 1b). Several researchers (Ashley, 1972; Constable and Rawson, 1982; Wullschleger and Oosterhuis, 1990a) have investigated the dynamics of carbon production, utilization, and translocation within cotton plants with a normally developing boll load. Constable and Rawson (1982) demonstrated that main-stem leaves export a large amount of carbon to developing sinks (vegetative and reproductive) at other nodes. Wullschleger and Oosterhuis (1990a) reported that substantial carbon translocation from leaves outside the main-stem node was necessary to support boll growth at several of the nodes examined. Therefore, without a large boll load, as is the case with high early square loss, there is a large amount of available carbon for allocation to the various vegetative sinks on the plant. the increase in carbon available to the terminal node also corresponds well with the observed trend toward greater height with increased early fruit loss, although sympodial node number was not affected (Table 3). This increase in vegetative growth was similar to the results of Jones et al. (1996) and Pettigrew et al. (1992) that showed a reduction in the late-season reproductive to vegetative ratio after removal of early fruit, indicative of a shift in dry matter partitioning.

Contribution to overall yield from the first fruiting position was decreased with early insect infestation and contribution from the second and outer positions was increased. Jones et al. (1996) also reported a shift in boll location to upper and outer positions with early flower removal, although in contrast to the current study yield was not affected. Only a certain amount of yield compensation from retention of outer (2) sympodial positions can be expected in any given environment. Therefore, cotton plant response to increasing levels of early square loss will often be limited at some point by the environment.

Although the present study and Sadras (1996) reported that increased canopy photosynthesis was associated with increased light penetration, the yield from the current study was still depressed by square loss. The fact that the current study did not record a difference in sympodia could indicate that growth was limited late in the season. It appears that the duration of favorable growing conditions is an important factor related to compensatory growth and may help to explain differences in yield response to square loss in different environments. In addition, as the results from this study are similar to that reported for plants that received manual removal of squares (Sadras, 1996), it seems that the use of either manual removal or insect-induce square removal is suitable for future physiological studies.Statistical Analysis Systems Institute Inc 1990; Wullschleger Oosterhuis 1990

	ACKNOWLEDGMENTS

 
This research was funded in part by Cotton Incorporated. The authors also appreciate the many contributions of Phil Tugwell.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Manuscript no. LSU99-79-0081.

Received for publication July 30, 1998.

	REFERENCES

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• Constable G.A., Rawson H.M. Distribution of ¹⁴C label from cotton leaves: consequences of changed water and nitrogen status. Aust. J. Plant Physiol. 1982;9:735-747.
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