Influence of Cover Crop and Intercrop Systems on Bemisia argentifolli ...

PEST MANAGEMENT

Influence of Cover Crop and Intercrop Systems on Bemisia argentifolli (Hemiptera: Aleyrodidae) Infestation and Associated Squash Silverleaf Disorder in Zucchini ROSHAN MANANDHAR,1 CERRUTI R. R. HOOKS,2,3

AND

MARK G. WRIGHT1

Environ. Entomol. 38(2): 442Ð449 (2009)

ABSTRACT Field experiments were conducted to evaluate the effects of cover cropping and intercropping on population densities of silverleaf whiteßy, Bemisia argentifolli Bellow and Perring, and the incidence of squash silverleaf disorder (SSL) in zucchini, Cucurbita pepo L., in Oahu, HI. Two cover crops, buckwheat (BW), Fagopyrum esculentum Moench, and white clover (WC), Trifolium repens L., or sunn hemp (SH), Crotolaria juncea L., and an intercropped vegetable, okra, Abelmonchus esculentus L., were evaluated during the 2003, 2005, and 2006 growing seasons, respectively. Population densities of whiteßies and SSL severity varied during the three Þeld experiments. In 2003, the severity of SSL and percentage of leaves displaying symptoms were signiÞcantly lower on zucchini plants in WC than BW plots throughout the cropsÕ growth cycle. Additionally, the percentage of leaves per plant displaying SSL symptoms was signiÞcantly greater in bare-ground (BG) compared with the pooled BW and WC treatments on each inspection date. In 2005, zucchini intercropped with okra had lower numbers of adult whiteßies and resulted in signiÞcantly lower severity of SSL than pooled BW and WC treatments. During 2006, zucchini grown with SH had signiÞcantly lower numbers of all whiteßy stages (i.e., egg, immature, and adult) and less SSL severity symptoms than BW. Despite these differences in whiteßy numbers and SSL severity, marketable yields were not signiÞcantly lower in BW compared with WC or SH treatment plots during the study. The mechanisms underlying these results and the feasibility of using cover crops and intercrops to manage B. argentifolli and SSL are discussed. KEY WORDS Bemisia argentifolii, phytotoxemia, squash, intercropping, living mulch

Whiteßies (Hemiptera; Aleyrodidae) can be severe pests of cucurbit crops and are capable of inducing phytotoxemias (Costa et al. 1993a, Hooks et al. 1998). Phytotoxemia is deÞned as an adverse, often delayed reaction of plants to toxins introduced during insect feeding. The silverleaf whiteßy (Bemisia argentifolii Bellows and Perring) is a severe pest of several agricultural crops throughout the world and is responsible for the phytotoxemia known as squash silverleaf disorder (SSL) (Hooks et al. 1998). Feeding by immature stages causes this phytotoxemia, and symptom severity is dependent on the number of immature whiteßies per unit of leaf area (Yokomi et al. 1990, Costa et al. 1993b). If whiteßy populations become high enough to cause signiÞcant leaf silvering, there is reduction in photosynthesis (Burger et al. 1988) and plant growth, resulting in severe yield losses in squash Þelds (Costa et al. 1994). In addition to SSL, whiteßy feeding can cause a reduction in plant vigor (Byrne and Bellows 1991, McAuslane et al. 2004) and irregular fruit rip1 Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, Honolulu, HI. 2 Department of Entomology, University of Maryland, College Park, MD. 3 Corresponding author, e-mail: [email protected].

ening (Cohen et al. 1992). Whiteßies are also responsible for transmitting plant viruses to healthy plants (Brown and Bird 1992, Wisler et al. 1998, Gibson et al. 2004, Hilje and Stansly 2008). In Hawaii, B. argentifolli is an important zucchini (Cucurbita pepo L.) pest because it induces SSL (Costa et al. 1993a, Hooks et al. 1998). Attempts to manage B. argentifolli with the use of insecticides are not always successful, and overdependence on insecticides has resulted in resistant populations to selected classes of insecticides (Omer et al. 1993, Crowder et al. 2006). Insecticide failures in managing whiteßies in cucurbits and a recent trend toward more sustainable production practices and organic farming in Hawaii have caused a need for alternative pest management strategies. Using cultural-control techniques, such as intercropping or growing one or more nonhost plant species within the same Þeld as the cash crop, with other pest suppression methods have the potential to reduce whiteßy numbers and their associated phytotoxemias. The use of reßective mulches as a cultural management practice to control silverleaf whiteßy in cucurbits has been well studied (Costa et al. 1994, Summers and Stapleton 2002, Summers et al. 2004). Although

0046-225X/09/0442Ð0449$04.00/0 䉷 2009 Entomological Society of America

April 2009

MANANDHAR ET AL.: COVER CROP AND INTERCROP SYSTEMS IN ZUCCHINI

studies have shown that whiteßy densities are reduced in mixed cropping systems (Smith 1976, Gold et al. 1989) and crops interplanted with cover crops (Hooks et al. 1998, Frank and Liburd 2005, Hilje and Stansly 2008), use of these tactics to manage SSL has received limited research attention. Thus, the purpose of this study was to determine whether companion plants in the form of cover crop and intercrop systems could be used effectively to reduce whiteßy numbers and the occurrence of SSL in zucchini plantings. Materials and Methods Treatments and Experimental Design. Field experiments were conducted on the island of Oahu at the University of HawaiiÕs Poamoho Research Station in Wailua in 2003 and at Aloun Farms in Ewa in 2005 and 2006. Zucchini (variety Spineless Beauty; Syngenta Seeds, Golden Valley, MN) was used as the main crop. Two cover crops, buckwheat (BW), Fagopyrum esculentum Moench (Peaceful Valley Farm Supply, Grass Valley, CA), and white clover (WC), Trifolium repens L. (variety New Zealand; Peaceful Valley Farm Supply), were evaluated during 2003, and also an intercropped vegetable, okra, Abelmonchus esculentus L. (variety Dwarf Green Long; Crossman Seeds, East Rochestar, NY), was added as a treatment in 2005. In 2006, the white clover failed to germinate properly, and after numerous attempts to reseed it failed, it was replaced with sunn hemp (SH), Crotolaria juncea L. (variety Tropic Sunn; USDAÐNRCS). Zucchini monoculture bare-ground (BG) was used as a check treatment. Buckwheat was chosen because it was found to be an effective companion plant in reducing the occurrence of nonpersistently aphid-transmitted viruses and SSL in an earlier study conducted by Hooks et al. (1998). However, buckwheat is a shortlived annual that senesced early during the zucchini growth cycle. One of our hypotheses was that overall pest suppression would have been greater if we used a cover crop that persisted throughout the growth cycle of the cash crop. White clover, sunn hemp, and okra (vegetable intercrop) were chosen because of their potential to provide other production beneÞts (e.g., soil fertility, additional farm income) in addition to their ability to persist the entire crop cycle. Furthermore, okra and sunn hemp are tall relative to zucchini and may act as physical barrier to whiteßy colonization. The experiment was set up in a randomized complete block design with each treatment replicated four times. Each plot measured 13.2 by 13.2 m. Zucchini plantlets were transplanted in between rows of companion plants in diculture plots. Ten rows of zucchini transplants were interplanted so that each row was surrounded on either side by a row of companion plants. The intra- and inter-row spacing was 1.2 m, and each plot contained 110 zucchini plants. Bare-ground plots contained a total of 11 rows of zucchini plants, and each plot was separated by a minimum of 7 m. Crop Planting. White clover was sown at ⬇47 g/row on 31 March 2003 and 17 March 2005. The seeds were

443

sown by hand into an ⬇8-cm-wide furrow. One week before zucchini planting, a motor-operated weed eater was used to clear ⬇1-m rows in each clover plot. Afterward, a motorized hand tiller was used to cultivate ⬇90-cm-wide rows for zucchini plantings. Buckwheat seeds were broadcasted uniformly in the plots and covered using a garden rake. The seeds were broadcasted on 18 September 2003, 8 Ð9 September, and 14 August in 2003, 2005, and 2006, respectively. Per plot seeding rates were 1.8 kg in 2003 and 2005 and 2.7 kg in 2006, respectively. Greenhouse grown okra seedlings were transplanted on 20 June (intrarow spacing of 60 cm) and 31 May (intrarow spacing of 1 m) in 2005 and 2006, respectively. Sunn hemp seeds were sown at 48 g/row on 1 June 2006. The seeds were sown by hand into an ⬇8-cm-wide furrow. Sunn hemp rows were clipped to a height of ⬇80 cm on 24 July, 14 and 31 August, and 20 September to reduce possible competition through shading of the zucchini plants. Twelve to 14-d-old greenhouse grown zucchini plantlets were transplanted into treatment plots on 13 October 2003 and 12 September 2005 at Poamoho Agricultural Research Station in Wailua and 4 Ð5 September, 2006 at Aloun Farms in Ewa, HI. Okra was pruned on two occasions to mimic a common cultural practice used when growing this crop. Border and plot areas were kept weed free by spot treating with glyphosate (Roundup; Monsanto, St. Louis, MO) and hand weeding, respectively. Rows of sudan grass (Sorghum bicolor variety sudanese Moench) planted around the experimental site were sprayed with GF 120 NF Naturalyte fruitßy bait (GF 120; Dow AgroScience, Indianapolis, IN) weekly to manage melon ßy populations. Bacillus thurigiensis variety kurtaski (Crymax; Certis, Columbia, MD) was sprayed on zucchini plants at a rate of 1.2 g/liter of water using a hand pumped knapsack sprayer to manage pickleworms, Diaphania nitidalis (Stoll), during the 2005 and 2006 trials. Additionally, Spinosad (Success; Dow AgroScience) was also sprayed on zucchini plants at the rate of 2.2 ml/liter of water to manage pickleworms at Aloun Farms, 1 wk before zucchini harvest. During both years, zucchini plants were fertilized with urea at the rate of 25 g/plot. Whitefly Samples. On each sampling date, 20 zucchini plants were randomly selected in each treatment plot for counting adult whiteßies. Whiteßies on the underside of leaves were counted after gently turning over the most recently mature leaf of each randomly selected zucchini plant (Simmons 1994, Hooks et al. 1998). When whiteßy densities were high (⬎50 per leaf), counts were taken from half of the leaf and multiplied by two to estimate whole leaf total. Sampling of whiteßy adults was conducted weekly from 14 to 49, 9 to 44, and 7 to 42 d after planting (DAP) in 2003, 2005, and 2006, respectively. To estimate the number of whiteßy eggs and immature stages (nymphs and pupae), a cork borer was used to remove a 3.14-cm2 circular disc sample from zucchini leaves of 15 randomly selected plants per plot (Smith et al. 2000). The leaf samples were partitioned according to plant stratum (upper, n ⫽ 5; medium, n ⫽

5; lower, n ⫽ 5 leaves). Disc samples were collected from the area halfway between the leaf tip and petiole and halfway between the leaf margin and mid vein. Leaf discs were placed in a plastic bag and transported to the laboratory in a chilled cooler. All whiteßy eggs and immature stages found on the abaxial leaf surface were recorded using a dissecting microscope. Leaf disc sampling was conducted weekly 23Ð 44, 17Ð 43, and 28 Ð 46 DAP in 2003, 2005, and 2006, respectively. Squash Silverleaf Evaluation. During each inspection date, SSL symptoms were recorded from all plants in three randomly selected interior rows of each treatment plot. Silverleaf severity symptoms were rated on the new leaf growth on a scale of 0 Ð5 (0 ⫽ no silvering to 5 ⫽ 95Ð100% leaf silvering) (Paris et al. 1987, Hooks et al. 1998). Plants were rated for squash silverleaf symptoms at 10-d intervals at 16 Ð36, 10 Ð30, and 16 Ð37 DAP in 2003, 2005, and 2006, respectively. Additionally, in 2003, the percentage of leaves per zucchini plant displaying silverleaf symptoms were determine in each treatment by randomly sampling 10 plants per plot. The total number of leaves on each plant displaying silverleaf symptoms was divided by the total number of leaves per plant to calculate silverleaf percentages. Yield. Harvested squash fruit were graded as marketable and unmarketable. Unmarketable fruits were further categorized as cull (irregular shaped fruit), virus (fruit displaying viral symptoms), fruit ßy (fruit containing injury mark from a female fruit ßy sting), and pickleworm (fruit into which larva had bored). The fruit weight by category was summed to obtain total fruit weight per plot. Harvesting discontinued when the percentage of zucchini plants inßicted by aphid-transmitted nonpersistent viruses reached ⬇85% in each treatment plot. To estimate okra yield, four neighboring plants were selected from Þve alternating rows (n ⫽ 20) excluding border rows. Marketable-sized fruits were harvested from 26 July to 28 September in 2005 and 12 July to 10 September in 2006. Yield data from the 20 plants/plot were used to estimate mean yields per hectare. Statistical Analysis. Data from arthropod counts and silverleaf ratings were analyzed by using mixed model analysis of variance (ANOVA; PROC MIXED; SAS Institute 2002). The model was constructed to examine the main effect of treatment by date, and block was designated as a random factor. Within the model, the following preplanned orthogonal contrasts were conducted: diculture (zucchini ⫹ intercrop and zucchini ⫹ cover crops) versus monoculture (zucchini bareground); (zucchini ⫹ intercrop) versus (zucchini ⫹ cover crops); and (zucchini ⫹ buckwheat) versus (zucchini ⫹ clover or sunn hemp). All data for arthropod counts were log10(x ⫹ 1) transformed to stabilize variances. Reported means are from nontransformed data. Differences among treatment were considered signiÞcant if P ⬍ 0.05. Results Foliar Counts. During 2003, adult whiteßy numbers from whole leaf counts were similar among treatments

Mean no. of adult whiteflies per leaf

ENVIRONMENTAL ENTOMOLOGY

Vol. 38, no. 2

2.4

Bare-ground Buckwheat White clover

2.2 2.0

** b

1.8 1.6

b

1.4 1.2 1.0 0.8 0.6 0.4

14

21

28

35

42

Days after Planting

Fig. 1. Mean numbers of adult whiteßies per zucchini leaf counted in treatment habitats in 2003. Bare-ground represents zucchini monoculture, and buckwheat and white clover represent zucchini interplanted with buckwheat and white clover, respectively. **Counts were signiÞcantly higher in diculture than monoculture; bcounts are signiÞcantly higher in buckwheat than white clover treatment (P ⬍ 0.05).

on two of the Þve sample dates (Fig. 1; P ⬎ 0.05). However, at 21 DAP, counts were signiÞcantly lower on zucchini plants in BG compared with pooled WC and BW (F1,6 ⫽ 7.4; P ⫽ 0.0075). On the Þnal two sampling dates (35 and 42 DAP), whiteßy counts were also signiÞcantly lower on zucchini plants in WC compared with BW plots (F1,6 ⫽ 11.1; P ⫽ 0.001 and F1,6 ⫽ 9.5; P ⫽ 0.002, respectively). Similar to 2003, population density of adult whiteßies was generally low during the 2005 study. SigniÞcantly higher numbers of adult whiteßies were found in pooled WC and BW compared with okra on the last three sampling dates from 30 to 44 DAP (F1,9 ⫽ 9.96 Ð12.5; P ⬍ 0.0116; Fig. 2). Adult whiteßy density was highest (⬇11.0 per leaf) during the 2006 study. The mean density in pooled diculture treatments (BW ⫹ SH ⫹ okra) was significantly greater than BG treatment on 14 and 28 DAP


444

4

3

Bare-ground Buckwheat White clover Okra

cc

cc

2

cc

1

0 9

16

23

30

37

44

Days after planting

Fig. 2. Mean number of adult whiteßies per zucchini leaf counted in different treatment habitats in 2005. Bare-ground represents zucchini monoculture, and buckwheat and white clover represent zucchini interplanted with buckwheat and white clover cover crops, respectively. Okra represents zucchini intercropped with okra. cc, cover crops signiÞcantly greater than intercrop.


35 30

Bare-ground Buckwheat Okra Sunn hemp

25 20

b

**, b ** , b

15 10

i, b

5 0 7

14

21

28

35

42

Days after planting

Mean no. of immature whitefly/leaf disc


April 2009

0.5 0.4

445

*

Bare-ground Buckwheat Clover Okra

0.3 0.2

*

0.1 0.0 17

23

30

37

43

Days after planting

Fig. 5. Mean numbers of immature whiteßies found per zucchini leaf disc in treatment habitats in 2005. Bare-ground represents zucchini monoculture; buckwheat and white clover represent zucchini interplanted with buckwheat and white clover cover crops, respectively. Okra represents zucchini intercropped with okra. *Monoculture signiÞcantly greater than diculture treatments (P ⬍ 0.05).

(Fig. 3; F1,9 ⫽ 5.95; P ⫽ 0.0374 and F1,9 ⫽ 18.4; P ⫽ 0.002, respectively). Whiteßy numbers were higher in the okra-intercropped than pooled cover crop treatments during the initial sampling date (F1,9 ⫽ 9.3; P ⫽ 0.0139). There was also signiÞcantly higher number of whiteßies in BW compared with SH treatment from early to midseason (F1,9 ⫽ 11.1Ð 40.1; P ⬍ 0.0087; Fig. 3). Eggs and Immature Whitefly Counts. During 2003, whiteßy egg counts per leaf disc sample were similar among treatments on most sampling dates (Fig. 4; P ⬎ 0.05). Only during the initial sampling period were there signiÞcantly different whiteßy egg counts among treatments. On this date, fewer eggs were counted on leaf disc samples collected in BG compared with pooled BW and WC treatments and in WC than in BW (F1,6 ⫽ 5.0; P ⫽ 0.027 and F1,6 ⫽ 10.1; P ⫽

0.002, respectively). However, no differences were detected among treatments in immature whiteßy counts in 2003 (data not shown). Numbers of whiteßy eggs (⬇0.6 per leaf disc) and immature stages (⬇0.07 per leaf disc) were low during the 2005 study. Mean numbers of whiteßy eggs were similar among treatments and did not signiÞcantly differ on any sampling date (data not shown). However, numbers of immature whiteßy stages were signiÞcantly higher in BG contrasted with pooled diculture treatments (BW ⫹ WC ⫹ okra) during the last two sampling dates (37 and 43 DAP; F1,9 ⫽ 12.64; P ⫽ 0.006 and F1,9 ⫽ 8.00; P ⫽ 0.0198, respectively; Fig. 5). During the 2006 study, counts were signiÞcantly higher in BW contrasted with the SH treatment from 23 to 37 DAP (F1,9 ⫽ 5.3Ð14.2; P ⬍ 0.047; Fig. 6A). Number of immature stages was also signiÞcantly higher in BW contrasted to SH during that period (F1,9 ⫽ 5.6 Ð22.2; P ⬍ 0.041; Fig. 6B). Silverleaf Evaluation. In 2003, the percentage of leaves displaying SSL was signiÞcantly greater in BG compared with pooled BW and WC treatments and BW compared with WC treatment on each inspection date (F1,6 ⫽ 7.1Ð27.15; P ⬍ 0.0372 and F1,6 ⫽ 8.3Ð 8.6; P ⬍ 0.028, respectively; Table 1). Similarly, SSL severity was signiÞcantly greater in BW than WC on each inspection date (F1,6 ⫽ 7.05Ð212; P ⬍ 0.0085; Table 2). SSL severity was signiÞcantly greater in bare-ground compared with the pooled diculture treatments only during the initial inspection (16 DAP; F1,6 ⫽ 212; P ⬍ 0.0001; Table 2). Zucchini plants in BG plots could not be rated for SSL at the Þnal inspection date (46 DAP) because of the high occurrence and symptom severity of aphid-borne nonpersistent viruses. In 2005, SSL symptoms were not observed on the Þrst sampling date (10 DAP). However, severity symptoms were signiÞcantly lower in zucchini intercropped with okra contrasted to WC and BW on 20 and 30 DAP (F1,9 ⫽ 23.2; P ⫽ 0.001 and F1,9 ⫽ 18.3; P ⫽

Mean no. of whitefly eggs/leaf disc

Fig. 3. Mean numbers of adult whiteßies per zucchini leaf found in different habitats in 2006. Bare-ground represents zucchini monoculture; buckwheat and white clover represent zucchini interplanted with buckwheat and white clover cover crops, respectively. Okra represents zucchini intercropped with okra. **Dicultures signiÞcantly greater than monoculture; iintercrop signiÞcantly greater than cover crops; bbuckwheat signiÞcantly greater than sunn hemp.

1.0


* *, b

0.8 0.6 0.4 0.2 0.0

23

30 37 Days after planting

44

Fig. 4. Mean numbers of whiteßy eggs per zucchini leaf disc counted in treatment habitats in 2003. Bare-ground represents zucchini monoculture, and buckwheat and white clover represent zucchini interplanted with buckwheat and white clover, respectively. **Counts were signiÞcantly higher in diculture than monoculture; bcounts are signiÞcantly higher in buckwheat than white clover treatment (P ⬍ 0.05).

Mean no of immature whitefly/leaf disc Mean no. of whitefly eggs/leaf disc

446


70 A

b

Bare-ground Buckwheat Sunn hemp Okra

60 50 b 40

Table 2. Mean rating ⴞ SE of SSL symptoms on zucchini foliage in three treatment habitats during 2003 Treatmentsa

b


30 20

a b

10

Vol. 38, no. 2

c

Days after planting 16 db,c

26 db

36 db

46 db

3.51 ⫾ 0.13 2.20 ⫾ 0.15 0.65 ⫾ 0.09

1.28 ⫾ 0.09 1.53 ⫾ 0.09 0.99 ⫾ 0.02

0.87 ⫾ 0.03 1.05 ⫾ 0.03 0.85 ⫾ 0.03

Ñ 1.07 ⫾ 0.04 0.95 ⫾ 0.02

Each treatment is grown with zucchini. Bare-ground signiÞcantly greater than dicultures. Buckwheat signiÞcantly greater than white clover.

0 B

pared with the okra treatment plots (F1,9 ⫽ 54.43; P ⬍ 0.0001; Fig. 7B). In 2006, marketable fruit yields were greatly reduced by the presence of melon ßies that infested 38.2% of the harvested fruits and no difference existed among treatments (P ⬎ 0.05, data not shown).

b 30

b

20 b

Discussion

10

0.002, respectively; Table 3). Silverleaf severity symptoms were signiÞcantly lower in BG contrasted to the pooled diculture treatments (BW ⫹ WC ⫹ okra) on the Þnal inspection date (30 DAP: F1,9 ⫽ 7.3; P ⫽ 0.021). During the 2006 study, mean SSL severity symptoms were highest on zucchini plants in BW plots and were signiÞcantly higher in BW contrasted with SH plots on each sampling date (F1,9 ⫽ 5.9 Ð20.9; P ⬍ 0.0379; Table 4). Fruit Yield. Marketable fruit yield varied from year to year and was highest during the 2003 study (Fig. 7). During that year, marketable fruit yield was signiÞcantly greater in BW and WC than in BG plots (F1,6 ⫽ 7.4, P ⫽ 0.03; Fig. 7A). During 2005, mean marketable yields were signiÞcantly greater in BW and WC com-

Field experiments were conducted to determine the impact of using cover crops and an intercrop system on densities of B. argentifolii and associated SSL disorder in zucchini. Zucchini plants grown with buckwheat generally had higher whiteßy counts than those grown with white clover, sunn hemp or okra. Similarly, the severity of SSL was also commonly greater on zucchini plants grown with buckwheat compared with these habitats. Despite these differences, marketable yields were not signiÞcantly lower in buckwheat plots. The overall impact of cover crop and intercrop systems on populations of whiteßy and SSL differed according to planting system. For example, in 2003, adult whiteßy counts were generally greater on zucchini plants in buckwheat than in white clover plots. During the 2005 trial, zucchini intercropped with okra had lower adult whiteßy counts and signiÞcantly less SSL severity symptoms compared with zucchini grown with white clover and buckwheat. In the 2006 study, whiteßy populations were high compared with previous studies and zucchini grown with sunn hemp generally had signiÞcantly lower numbers of all whiteßy stages (i.e., egg, immature and adult) than zucchini grown with buckwheat. Zucchini grown with sunn hemp also contained the lowest SSL severity ratings among all treatments throughout the sampling period.

Table 1. Mean percentage ⴞ SE of leaves displaying SSL symptoms on zucchini plants in three treatment habitats during 2003

Table 3. Mean rating ⴞ SE of SSL symptoms on zucchini foliage in three treatment habitats during 2005

0 23

30

37

46

Days after planting

Fig. 6. Mean numbers of (A) eggs and (B) immature whiteßies per zucchini leaf disc in treatment habitats in 2006. Bare-ground represents zucchini monoculture; buckwheat and sunn hemp represent zucchini interplanted with buckwheat and sunn hemp, respectively; and okra represents zucchini intercropped with okra. bBuckwheat signiÞcantly greater than sunn hemp.

Treatmentsa Bare-ground Buckwheat White clover

Days after planting 21 db,c

28 db,c

35 db,c

92.85 ⫾ 1.43 77.52 ⫾ 3.22 60.50 ⫾ 3.09

96.18 ⫾ 0.98 92.29 ⫾ 2.60 85.54 ⫾ 1.27

99.65 ⫾ 0.20 97.21 ⫾ 2.50 95.24 ⫾ 0.71

Treatmentsa Bare-ground Buckwheat White clover Okra

Days after planting 10 d

20 db

30 db,c

0 0 0 0

0.60 ⫾ 0.07 1.42 ⫾ 0.13 1.51 ⫾ 0.15 0.13 ⫾ 0.04

0.22 ⫾ 0.04 0.76 ⫾ 0.06 1.08 ⫾ 0.10 0.16 ⫾ 0.04

a

Each treatment was grown with zucchini. SSL in bare-ground is signiÞcantly greater than diculture treatments. c SSL in buckwheat is signiÞcantly greater than white clover treatment. b

a

Each treatment is grown with zucchini. Cover crop treatments are signiÞcantly greater than okra intercrop. c Dicultures signiÞcantly greater than monoculture. b

April 2009


Table 4. Mean rating ⫾ SE of silverleaf severity symptoms on zucchini foliage in three treatment habitats during 2006 Treatmentsa Bare-ground Buckwheat Okra Sunn hemp a b

Days after planting 16 db

26 db

37 db

3.99 ⫾ 0.10 4.00 ⫾ 0.16 3.21 ⫾ 0.15 2.36 ⫾ 0.13

2.50 ⫾ 0.14 3.54 ⫾ 0.16 2.40 ⫾ 0.12 1.59 ⫾ 0.12

1.25 ⫾ 0.09 2.74 ⫾ 0.14 1.32 ⫾ 0.10 0.89 ⫾ 0.11

Each treatment is grown with zucchini. Buckwheat is signiÞcantly greater than sunn hemp.

During each year, mean SSL severity ratings declined over time in all treatment plots. This is attributable to two factors. Firstly, as the season progressed, there was a high incidence of aphid-borne nonpersistent viruses (NPVs) among zucchini plants (Manandhar 2007, Hooks and Wright 2008). Leaves that are mottled and deformed because of virus infection often display minimal silverleaf symptoms (Hooks et al. 1998). Bare-ground treatments had the highest incidence of NPVs (Manandhar 2007, Hooks and Wright 2008). This may have resulted in SSL severity symptoms being underestimated to a greater extent in BG 8000 7000 6000

Marketable Fruit fly Virus Cull Pickle worm

**

A

**

5000

Mean zucchini yield (Kg/ ha)

4000 3000 2000 1000 0

Bare-ground

Buckwheat

White clover

3000

B

cc 2500 2000

cc

1500 1000 500 0 Bare-ground Buckwheat White clover

Okra

Fig. 7. Mean zucchini fruit yield from different treatments habitats in 2003 (A) and 2005 (B). Bare-ground represents zucchini monoculture; buckwheat, white clover, and sunn hemp represent zucchini interplanted with buckwheat, white clover, and sunn hemp cover crop, respectively; and okra represents zucchini intercropped with okra. Fruit ßy and pickle worm represents fruit ßy and pickle worm infested fruit. Virus represents fruit displaying viral symptoms and cull represents misshaped fruit not caused by insects. **Marketable yields signiÞcantly greater in (buckwheat ⫹ white clover) versus bare-ground treatment; ccmarketable yields signiÞcantly greater in (buckwheat ⫹ white clover) versus okra.

447

plots. Secondly, SSL severity is depended on the number of immature whiteßies per leaf area (Costa et al. 1993b). Thus, as zucchini plants continued to mature and the amount of leaf area increased, greater number of immature whiteßies would need to be present to maintain similar SSL severity symptoms. Differences in zucchini plant size among treatments may also explain why SSL severity symptoms were not consistently correlated with immature whiteßy densities. For example, in 2003, although immature whiteßy densities were similar among treatments, SSL severity symptoms were lowest in white clover plots. Correspondingly, zucchini leaf area and canopy measurements were greatest in white clover plots (C.R.R.H., unpublished data). In 2006, zucchini plants were signiÞcantly larger in SH than in BW plots (Manandhar 2007). Although, competition with the buckwheat could have contributed to plants being smaller in BW, we hypothesized that the high severity of silver leaf was the main cause of smaller zucchini plants in BW plots. Severe silvering in squash Þelds causes considerable reductions in plant growth and associated yield reductions (Costa et al. 1994). Symptom severity of SSL was highest in 2006 and greatest among plants in BW plots. During this period, immature whiteßy numbers were also greatest in buckwheat plots. Thus, it is possible that SSL contributed to reduced growth of zucchini plants in BW plots. Zucchini in SH were generally larger than plants in other treatment plots. Sunn hemp, which was clipped before planting the zucchini, likely increased soil nutrients and sheltered zucchini plants from wind, allowing increased crop growth. This would have allowed zucchini plants in these plots to sustain higher whiteßy counts before being impacted by SSL. However, in the case of SH, this increased growth may have been detrimental to Þnal marketable yields. Although zucchini plants were noticeably larger and greener in SH plots, there was a delay in the initial harvest period; this presumably occurred because the excess nitrogen from the decomposing sunn hemp, boost zucchini plant growth but delayed ßowering and fruit production. This delay in fruit maturity allowed more time for plants in these plots to become infected with viruses. In addition to insects, cucurbit crops in Hawaii may incur damages from avian pests. Farmers in Hawaii have reported losing 80 Ð100% of their crop to bird damage (Koopman and Pitt 2007). Bulbul birds, Pycnonotus sp., which were frequently found at the Poamoho study site, are especially injurious to vegetable crops. During the 2005 experiment, zucchini yield was severely reduced in plots with okra. These reductions were mostly attributed to damages caused by bulbul birds, which fed on the growing axils of zucchini plants. Fourteen percent of the zucchini plants in okra plots were heavily damaged by birds. Bulbuls may have restricted themselves to feeding on zucchini plants in okra plots because they could perch on the okra stems before ßying down to zucchini plants. The architecture of the other plants grown at the site may have been less favorable to serve as “launch” sites. In 2006, in the absence of bulbul birds,

448


zucchini yields in okra plots were similar to other treatments. During the 2006 experiment, melon ßies, Dacus cucurbitae, were the most problematic pests at the study site. A standard control procedure include weekly applications of a liquid protein bait (GF 120 Naturalyte fruitßy bait; Dow AgroScience) to sudan grass borders serving as a melon ßy trap crop. However, beneÞts of this management tactic were nulliÞed because high numbers of melon ßies were migrating from large untreated cucurbit crops surrounding the study area. Additionally, rain that occurred during the fruiting period may have washed the GF 120 sprays off the sudan border, reducing their efÞcacy. Findings from this study suggest that cover crop and intercrop systems may not always be practical in alleviating yield reductions in zucchini plantings associated with whiteßy populations and that not all intercropping systems will have similar impact on whiteßies and the occurrence of SSL. Both whiteßy densities and SSL symptoms were sometimes greatest in BW plots. It was noted through casual observations that buckwheat served as a whiteßy host, and this may have contributed to zucchini plants in these habitats having higher whiteßy numbers. Additionally, buckwheat is a short-term annual that started to senesce shortly after zucchini planting. Thus, whiteßies may have moved from the buckwheat over to the neighboring zucchini plants. However, Hooks et al. (1998) found mean SSL severity symptoms were lowest on zucchini in buckwheat treatments on all sampling dates compared with bare-ground and zucchini grown with yellow mustard, Sinapis alba. Furthermore, they found numbers of whiteßy adults were also signiÞcantly lower on zucchini plants grown with buckwheat compared with bare-ground habitats. In Florida, Frank and Liburd (2005) also found a reduction in whiteßy densities in zucchini grown with buckwheat compared with monoculture habitats. However, because of the inconsistencies associated with buckwheat among studies, it may not be an ideal companion plant in areas with high whiteßy populations. Conversely, if the main concern is NPVs, buckwheat may be a more favorable companion plant because it has been shown to signiÞcantly reduce the occurrence of NPVs in zucchini (Hooks et al. 1998, Manandhar 2007, Hooks and Wright 2008). Individuals who are interested in using this cultural method to manage whiteßies should consider other factors such as (1) added farm expense or inconveniences, especially if there is only minimum whiteßy suppression; (2) additional production beneÞts, for example, an advantage of using an intercrop is the potential economic return from another marketable plant. Additionally, legumes are nitrogen Þxers, and thus can be potentially used to offset the rising cost of synthetic fertilizer; and (3) potential to mitigate or enhance other crop pests that may be found at the Þeld site. During this study, whiteßy, melon ßy, avian pests, and aphid borne NPVs inßuenced Þnal zucchini yields at some period during the study. Thus, any companion plant chosen to help manage whiteßy and its associ-

Vol. 38, no. 2

ated silverleaf disorder should not create conditions more inviting to these pests. Although only evaluated in 2006, sunn hemp showed great promise as a companion plant. In addition to it potential to help manage insect pests, sunn hemp possesses nematicidal properties when incorporated into the soil (Wang et al. 2003) and may supply a natural source of nitrogen (Balkcom and Reeves 2005). Current experiments are aimed at evaluating sunn hempÕs ability to simultaneously manage above and below ground crop pests and enhance soil fertility in other vegetable plantings.

Acknowledgments The authors thank R. Pandey, D. Kabasawa, and the crew at the Poamoho Research Station for assisting in Þeld work. We also thank the owner, managers, and crew team at Aloun Farms for logistic and Þeld support in conducting the experiment. This project was supported by a USDA/CSREES Special Grant for Tropical and Subtropical Agriculture Research (T-STAR), 2002-34135-12791, and a Western Region integrated pest management grant (Project 2004-05060).

References Cited Balkcom, K. S., and D. W. Reeves. 2005. Sunn-Hemp utilized as a legume cover crop for corn production. Agron. J. 97: 26 Ð31. Brown, J. K., and J. Bird. 1992. Whiteßy-transmitted geminiviruses and associated disorders in the Americas and the Caribbean Basin. Plant Dis. 76: 220 Ð225. Burger, Y., A. Schwartz, and H. S. Paris. 1988. Physiology and anatomical features of the silvering disorder of Cucurbita. J. Hort. Sci. 63: 635Ð 640. Byrne, D. N., and T. S. Bellows, Jr. 1991. Whiteßy biology. Annu. Rev. Entomol. 40: 511Ð534. Cohen, S., J. E. Duffus, and H. Y. Liu. 1992. A new Bemisia tabaci biotype in the southwestern United states and its role in silverleaf of squash and transmission of lettuce infectious yellow. Phytopathology 82: 86 Ð90. Costa, H. S., M. W. Johnson, D. E. Ullman, A. D. Omer, and B. E. Tabashnik. 1993a. Sweetpotato whiteßy (Homoptera: Aleyrodidae): Analysis of biotypes and distribution in Hawaii. Environ. Entomol. 22: 16 Ð20. Costa, H. S., D. E. Ullman, M. W. Johnson, and B. E. Tabashnik. 1993b. Squash silverleaf symptoms induced by immature, but not adult, Bemisia tabaci. Phytopathology 83: 763Ð766. Costa, H. S., M. W. Johnson, and D. E. Ullman. 1994. Row covers effect on sweetpotato whiteßy (Homoptera: Aleyrodidae) densities, incidence of silverleaf, and crop yield in zucchini. J. Econ. Entomol. 87: 1616 Ð1621. Crowder, D. W., Y. Carrie`re, B. E. Tabashnik, P. C. Ellsworth, and T. J. Dennehy. 2006. Modeling evolution of resistance to Pyriproxyfen by the sweetpotato whiteßy (Homoptera: Aleyrodidae). J. Econ. Entomol. 99: 1396 Ð 1406. Frank, D. L., and O. E. Liburd. 2005. Effects of living and synthetic mulch on the population dynamics of whiteßies and aphids, their associated natural enemies, and insecttransmitted plant diseases in zucchini. Environ. Entomol. 34: 857Ð 865. Gibson, R. W., V. Aritua, E. Byamukama, I. Mpembe, and J. Kayongo. 2004. Control strategies for sweet potato virus in Africa. Vir. Res. 100: 115Ð122.

April 2009


Gold, C. S., M. A. Altieri, and A. C. Bellotti. 1989. Effects of intercrop competition and differential herbivore numbers on cassava growth and yields. Agric. Ecosys. Environ. 26: 131Ð146. Hilje, L., and P. A. Stansly. 2008. Living ground covers for management of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) and tomato yellow mottle virus (ToYMoV) in Costa Rica. Crop Protect. 27: 10 Ð16. Hooks, C.R.R., and M. G. Wright. 2008. Use of a living and dying mulch as barrier plants to protect zucchini from insect caused viruses and phytotoxemias. CTAHR Coop. Ext. Serv. Insect. Plant Dis., PD-36 Jan 2008. University of Hawaii, Honolulu, HI. Hooks, C.R.R., H. R. Valenzuela, and J. Defrank. 1998. Incidence of pests and arthropod natural enemies in zucchini grown with living mulches. Agric. Ecosys. Environ. 69: 217Ð231. Koopman, M. E., and W. C. Pitt. 2007. Crop diversiÞcation leads to diverse bird problems in Hawaii agriculture. Human Wildlife Conßicts 1: 235Ð243. Manandhar, R. 2007. Cultural management of insect pests: using barrier crops to protect against insect inßicted plant impairments. MS thesis, University of Hawaii at Manoa, Honolulu, HI. McAuslane, H., J. J. Chen, R. B. Carle, and J. Schmalstig. 2004. Inßuence of Bemisia argentifolli (Homoptera: Aleyrodidae) infestation and squash silverleaf disorder on zucchini seedling growth. J. Econ. Entomol. 97: 1096 Ð 1105. Omer, A. D., M. W. Johnson, B. E. Tabashnik, H. S. Costa, and D. E. Ullman. 1993. Sweetpotato whiteßy resistance to insecticide in Hawaii: intra-island variation is related to insecticide use. Entomol. Exp. Appl. 67: 173Ð182. Paris, H. S., H. Nerson, and Y. Burger. 1987. Leaf silvering of Cucurbita. Can. J. Plant Sci. 67: 593Ð598.

449

SAS Institute. 2002. Statistics, version 9.1. SAS Institute, Cary, NC. Simmons, A. V. 1994. Oviposition on vegetable by Bemisia tabaci (Homoptera: Aleyrodidae): temporal and leaf surface factor. Environ. Entomol. 23: 381Ð389. Smith, J. G. 1976. Inßuence of crop background on aphids and other phytophagous insects on brussels sprouts. Ann. Appl. Biol. 83: 1Ð13. Smith, H. A., R. L. Koenig, H. J. McAuslane, and R. McSorley. 2000. Effect of silver reßective mulch and a summer squash trap crop on densities of immature Bemisia argentifollii (Homoptera: Aleyrodidae) on organic bean. J. Econ. Entomol. 93: 726 Ð731. Summers, C. G., and J. J. Stapleton. 2002. Use of UV reßective mulch to delay the colonization and reduce the severity of Bemisia argentifollii (Homoptera: Aleyrodidae) infestations in cucurbits. Crop Protect. 21: 921Ð928. Summers, C. G., J. P. Mitchell, and J. J. Stapleton. 2004. Management of aphid-borne viruses and Bemisia argentifollii (Homoptera:Aleyrodidae) in zucchini squash by using UV reßective plastic and wheat straw mulches. Environ. Entomol. 33: 1447Ð1457. Wang, K.-H., R. McSorley, and R. N. Gallaher. 2003. Effect of Crotalaria juncea amendment on nematode communities in soil with different agricultural histories. J. Nematol. 35: 294 Ð301. Wisler, G. C., J. E. Duffus, H.-Y., Liu, and R. H. Li. 1998. Ecology and epidemiology of whiteßy-transmitted closteroviruses. Plant Dis. 82: 270 Ð280. Yokomi, R. K., K. A. Hoelmer, and L. S. Osborne. 1990. Relationships between the sweetpotato whiteßy and the squash silverleaf disorder. Phytopathology 80: 895Ð900. Received 31 July 2008; accepted 9 November 2008.