Arthropod pest and natural enemy abundance under second-level versus first-level integrated pest management practices in apple orchards: a 4-year study

ELSEVIER Agriculture, Ecosystem and Environment 57 (1996) 35-47

Agriculture Ecosystems & Enwronment

Arthropod pest and natural enemy abundance under second-level versus first-level integrated pest management practices in apple

orchards: a 4-year study

Ronald J. Prokopy *, Jennifer L. Mason, Margaret Christie, Starker E. Wright Department of Entomology, University of Massachusetts, Amherst MA 01003, USA

Accepted 20 October 1995

Abstract

The authors conceive of second-level integrated pest management (IPM) in apple orchards as involving integration of multiple management tactics across all classes of pests. From 1991-1994, a second-level IPM pilot project was carried out in six commercial Massachusetts apple orchard blocks (2-4 ha) in which pest and natural enemy populations and injuries to fruit were compared with those in adjacent blocks receiving first-level IPM practices (considered to be integration of tactics within a single class of pests). The approach to second-level IPM was use of chemically based tactics for arthropod, disease and weed control during the first part of the growing season (up to mid-June for arthropods) and thereafter use of only biologically based tactics (cultural, behavioral and biological control methods). This article deals with findings on arthropod management. As expected, total injury to fruit by insects causing damage before mid-June did not differ between second-level (4.7%) and first-level (4.8%) IPM blocks. Total injury to fruit by insects active after mid-June averaged about the same (0.5%) in both types of blocks in 1991 and 1992, but in 1993 and 1994 it averaged more in second-level blocks (4.8%) than first-level blocks (1.9%). This was particularly true for Grapholitha prunivora Walker and leafrollers and less so for Cydia pomonella (L.) and Rhagoletis pomonella (Walsh). Among foliar pest arthropods and their natural enemies, populations of aphids and aphid predators and populations of spider mites and mite predators averaged about the same in both types of blocks. Populations of leafminers averaged lower and parasitoids of leafminers averaged greater in second-level blocks. Populations of leafhoppers averaged greater in second-level blocks. Pesticide use against fruit-damaging insects averaged 37% less in second-level than in first-level blocks, but against foliar-damaging arthropods, it was not less. Some refinements of second-level IPM tactics for arthropod control are needed before second-level IPM practices can be recommended broadly to commercial growers in New England as an economical and reliable alternative to first-level IPM.

Keywords: Integrated pest management; Apple

1. Introduction

As described by Dover (1985), ideally integrated pest management (IPM) ought to optimize pest con-

* Corresponding author.

trol in an ecologically and economical ly sound manner, emphasize coordinated use of multiple tactics to assure stable crop production, and maintain pest damage below injurious levels while minimizing hazards to humans, animals, plants and the environment. During the past 3 decades or so in which researchers, extension personnel, private consultants

0167-8809/96/$15.00 © 1996 Elsevier Science B.V. All rights reserved SSDI 0167-8809(95)00657-5

36 R.J. Prokopy et a l . / Agriculture, Ecosystem and Environment 57 (1996) 35-47

and farmers have gained experience with application of these ideals in IPM programs across a wide range of crops, numerous benefits as well as several constraints associated with IPM have emerged (Corbet, 1981; Miller, 1983; Wearing, 1988; Rajotte, 1993; Zalom, 1993). Benefits often include reduction in amount and cost of chemically based (pesticidal) control measures and improvement in crop yield or quality. Constraints usually are expressed as being of a social, institutional, educational or technical nature. Technical constraints become particularly challeng- ing as practitioners move from chemically based toward biologically based forms of IPM (Frisbie and Smith, 1991).

As an aid for measuring progress toward achiev- ing an ideal program of IPM for apple orchards, Prokopy (1993, Prokopy (1994) proposed that progress be viewed in the form of taking a series of steps, analogous to climbing steps of a ladder. The first step up the ladder (equivalent to first-level IPM) involves integrating use of chemically based and biologically based management tactics within a single class of pests, such as arthropods, diseases, weeds or vertebrates. The second step (equivalent to second-level IPM) integrates multiple management tactics across all classes of pests. Third-level IPM emphasizes integration of pest management approaches with the entire system of crop production on a farm. Fourth-level IPM involves social, cultural and political realms. Progress under first-level IPM for apple orchards has been reported for Australia (Be wer et al., 1993), Europe (references in Blom- me~ ;, 1994) and North America (references in Prckopy and Croft, 1994). Guidelines for integrated production of apples in Europe corresponding to second-level (and even third-level) IPM practices are given in Dickler and Schafermeyer (1990). Progress by some European apple growers in production and marketing of high quality fruit under second- or third-level IPM is described by Oberhofer (199t) and Cross (1996). Implementation of second- or third-level IPM practices in North American apple orchards is in a state of early development.

From 1991-1994, a second-level IPM pilot project was conducted in blocks of trees at several commercial apple orchards in Massachusetts. The evolution of concepts and practices leading up to initiation of this pilot project, together with a subset

of findings for 1993, are given in Prokopy et al. (1994). The predominant approach to second-level IPM involved use of chemically based tactics for arthropod, disease and weed control during the first part of the growing season (up to mid-June) and thereafter use of biologically based tactics. It was believed that relying to the greatest extent possible on biologically based tactics during the second part of the growing season would maximize the potential for build-up of beneficial natural enemies of arthropod pests, reduce selection pressure on pests to develop resistance to pesticides and minimize the amount of pesticide residue on the fruit at harvest. The objective was to compare pest and natural enemy populations and injuries to fruit in second-level IPM blocks with those in adjacent first-level IPM blocks that were under chemically based management throughout the growing season. Here, all 4 years of findings for arthropods are presented. Find- ings on disease, weed and vertebrate pest management are planned for future articles.

2. Materials and methods

In each of six commercial orchards, one second- level IPM pilot project block and one first-level IPM block were established, each ~ 2-4 ha. Nearly all blocks were bordered on two sides by woods, on one side by an open field and on one side by apple trees under first-level IPM management. Both types of blocks consisted primarily of 'Mclntosh', 'Cortland', 'Red Delicious' and 'Empire' cultivars on M.26 or M.7 rootstock. Crop load in each block varied from medium to heavy during the 4 years of study.

In Massachusetts, principal fruit-damaging arthropod pests on apple trees active from bud break until mid-June include tarnished plant bug, Lygus lineo- Iaris (Palisot de Beauvois), European apple sawfly Hoplocampa testudinea (Klug), plum curculio, Conotrachelus nenuphar (Herbst), green fruitworms, Orthosia spp. , and first generations of San Jos~ scale, Quadraspidiotus perniciosis (Comstock), redbanded leafroller, Argyrotaenia velutinana (Walker), obliquebanded leafroller, Choristoneura rosaceana (Harris), lesser appleworm, Grapholitha prunivora Walker, and codling moth, Cydia pomonella (L.). Principal foliar-damaging arthropods active in or-

R.1. Prokopy et a l . / Agriculture, Ecosystem and Enoironment 57 (1996) 35-47 37

chards during this time include first generations of European red mite, Panonychus ulmi (Koch), Phyl- lonorycter lea/miners, and white apple lea/hopper, Typhlocyba pomaria McAtee.

Because no effective biologically based control methods have been developed for several of these pests, particularly tarnished plant bug, European apple sawfly, plum curculio and green fruitworms, the authors felt obliged to rely upon chemically based methods of control up to mid-June (none of these four pests causes injury after mid-June). Determina- tion of need and timing of pesticide application against arthropod pests active up to mid-June was based on monitoring pest abundance. The monitoring methods used, described in Prokopy et al. (1994), were employed in both second- and first-level IPM blocks. Pesticides used to treat either type of block in which an arthropod pest exceeded an action threshold (Prokopy et al., 1991) included diflubenzuron (experimental use permit) against lea/miners in second-level blocks, oxamyl or methomyl against lea/miners in first-level blocks, endosulfan against lea/hoppers and phosmet or azinphosmethyl against all other insects. Horticultural oil was applied pre- bloom to all blocks against overwintering European red mite eggs and overwintering San Jos~ scale as a preventative treatment.

In Massachusetts, principal fruit-damaging arthropod pests on apple trees active from mid-June to harvest include apple maggot, Rhagoletis pomonella (Walsh), and summer generations of codling moth, lesser appleworm, lea/rollers and San Jos~ scale. Principal foliar-damaging arthropods include apple aphids, Aphis pomi DeGeer, spirea aphids, Aphis spiraecola Patch, woolly apple aphids, Erisoma lanigerum (Hausmann), rose lea/hoppers, Edward- siana rosae (L.), potato lea/hoppers, Empoasca fabae (Harris), two-spotted spider mites, Tetranychus ur- ticae (Koch), and summer generations of European red mites, lea/miners and white apple lea/hoppers.

In second-level IPM blocks, 8-cm red spherical sticky-coated traps were used (Tangletrap TM) to control apple maggot. Each trap was baited with a polyethylene vial containing the synthetic fruit attractant butyl hexanoate (release rate = 500/zg h- l )

and one semi-permeable membrane containing the synthetic food attractant ammonium acetate (Consep Membranes Inc., Bend, OR). In late June, traps were

placed 5 m apart on perimeter apple trees to intercept adults entering orchard blocks from neighboring abandoned trees up to 2 km away. The authors chose this perimeter-tree approach to trap deployment because their prior experience suggested that the vast majority of apple maggot flies infesting Mas- sachusetts orchards originated from neighboring unsprayed apple trees and not within the orchard itself. To minimize within-orchard origin and emergence of apple maggot flies, it was requested at the outset that fallen apples in each second-level block be removed by growers at weekly intervals. None of the cooper- ating growers was able to carry out this recommen- dation, however. Traps were cleaned and the sticky- coating renewed (if needed) every 2 weeks until harvest. For controlling summer generations of codling moth and lesser appleworm, all unsprayed apple and pear trees (primary hosts of these pests) within 100 m of the orchard block perimeter were cut down to discourage females of these pests from entering the block (Prokopy et al., 1990). None of the first-level IPM blocks was close enough to be affected by this practice. No direct action was planned against lea/rollers, San Jos~ scale, or foliar pests because it was anticipated that these pests would be held below injurious levels by natural enemies build- ing up in the absence of insecticide or acaricide use after mid-June.

In first-level IPM blocks, arthropod pests active after mid-June were monitored and treated by growers with pesticide based on recommended thresholds (Prokopy et al., 1991) or the grower's own criteria for need to treat. Pesticides used for treating first- level IPM blocks after mid-June included: phosmet, azinphosmethyl or chlorpyrifos against apple maggot, codling moth, lesser appleworm or lea/rollers; horticultural oil, hexakis or propargite against mites; methomyl against lea/miners and endosulfan against leaf hoppers.

To estimate the amount of insect-injured fruit in each block at harvest, 10 fruit on each of 20 interior trees of each principal cultivar and 10 fruit on each of 10 perimeter-row trees were examined (average number of fruit sampled per block = 700). To estimate the abundance of fotiar-feeding pests and predators of pests in each block, every other week from petal fall to harvest, 10 fruit cluster leaves and 10 shoot terminals on each of 20 interior trees were


examined. Samples of fruit and foliage from interior trees were taken in an X pattern across the block. In each case, the proportion of fruit or leaves with or without the characteristic injury or arthropod in question was recorded (the only exception was leafminers, where the number of mines per leaf was counted). Leaves containing leafminer larvae were brought to the laboratory to determine the proportion of miners parasitized by hymenopterous larvae. Finally, to monitor penetration of apple maggot flies into the interior of second-level and first-level blocks, one unbaited sticky red sphere trap was hung about 5 m inward from each comer of each block. In addition, four such traps were hung near the center of each block.

Student's t-test at the P = 0.05 level of signifi- cance was used to compare mean levels of fruit injury and arthropod pest and natural enemy populations in second-level and first-level IPM blocks. Separate comparisons were made for each year as well as across all 4 years combined. In the case of foliar pest and natural enemy populations, mean population levels per block per year were calculated by taking the percentage of sampled leaves or shoots containing the arthropod in question for each sam- pling date from its first to last appearance in samples and averaging these mean percentages across all samples. In addition, for each block, the percentage sampled leaves or shoots containing the arthropod in

question when it was at its peak population for the year was determined. In no case was there any discrepancy between a mean population index and a peak population index in terms of pattern of significant difference between second- and first-level blocks. Data are presented in terms of mean rather than peak population levels.

3. Results

Table 1 shows the mean dosage equivalents of pesticide used in second-level and first-level IPM blocks for each of the 4 years of the study. Amounts of pesticide applied against fruit-damaging insects before mid-June averaged the same (2.4 dosage equivalents) in both types of blocks; after mid-June, however, first-level blocks were the only blocks to receive pesticide against such insects (average of 1.4 dosage equivalents). Against foliar-damaging arthropods, amounts of pesticide used before mid-June averaged slightly greater in second-level than first- level blocks (2.5 vs. 1.9 dosage equivalents). Of these amounts, 1.5 dosage equivalents in each type of block were in the form of pre-bloom horticultural oil sprays against overwintering European red mite eggs; 0.5 dosage equivalents in second-level blocks were mistakenly applied by growers against leafminers when leafminer populations were still below

Table 1 Mean dosage equivalents a of pesticide used against fruit and foliar pests in six second-level and six first-level IPM blocks

Year IPM level Fruit insects Foliar arthropods b

Before mid-June After mid-June

Before mid-June After mid-June M LM LH A M LM LH A

1991 ~ d 2.0 0.0 1.9 1.0 0.I 0 0.5 0.0 0.2 0 1st 2.1 1.0 1.7 0.2 0.1 0 0.8 0.2 0.2 0

1992 ~ d 2.4 0.0 0.9 1.1 0.2 0 0.0 0.0 0.0 0 1st 2.2 2.0 1.1 0.4 0.0 0 0.1 0.0 0.0 0

1993 2nd 2.7 0.0 1.8 0.3 0.0 0 0.4 0.0 0.2 0 1st 2.2 1.0 1.4 0.0 0.0 0 0.6 0.0 0.2 0

1994 ~ d 2.6 0.0 1.6 0.3 0.3 0 0.0 0.0 0.3 0 1st 2.9 1.7 1.6 0.7 0.3 0 0.3 0.0 0.4 0

Avemge ~ d 2.4 0.0 1.6 0.7 0.2 0 0.2 0.0 0.2 0 1st 2.4 1.4 1.5 0.3 0.1 0 0.5 0.1 0.2 0

a Dosage equivalent = actual amount of pesticide applied per hectare per application relative to amount recommended per application in the 1991 New England Apple Pest Management Guide b M, mites; LM, leafminers; LH, leafhoppers; A, aphids.

RJ. Prokopy et al.// Agriculture, Ecosystem and Environment 57 (1996) 35-47 39

threshold levels. After mid-June, amounts of pesticide used against foliar-damaging arthropods averaged 0.4 dosage equivalents in second-level blocks (in the form of emergency treatments of propargite against European red mites and insecticidal soap against rose leafhoppers) and 0.8 dosage equivalents in first-level blocks.

Combined injury on harvest fruit samples by insects causing damage up to mid-June (plant bugs, sawfly, plum curculio, fruitworms) averaged essentially the same (2.0 vs. 1.9%) for second-level and first-level blocks. Except for sawfly in 1994, there were no significant differences between block types in injury levels caused by any of these pests, either within a single year or across all 4 years (Fig. 1). The majority of injury in both types of blocks was caused by tarnished plant bug.

Combined injury on harvest fruit samples by insects initiating damage after mid-June (codling moth, lesser appleworm, leafrollers, apple maggot and San Jos6 scale) averaged somewhat greater for second- level than first-level blocks (2.6 vs. 1.2%). Except for lesser appleworm and leafrollers in 1994 and lesser appleworm across all 4 years, there were no significant differences between block types in injury levels caused by any of these pests (Fig. 2). No fruit injury by San Jos~ scale was found in any block in any year. Of concern was the increase in codling moth, lesser appleworm, leafroller and apple maggot injury to fruit in second-level blocks during the last 2 years compared with the first 2 years (Fig. 2). To illustrate, average injury levels in second-level blocks for 1991 and 1992 combined versus 1993 and 1994 combined were 0.0 vs. 0.3% for codling moth, 0.0

Tarnished Plant Bug

3.5

3

2.5

2

1.5

1

0.5

0

91 92 93 94 AV

Year

4

3.5

3

2.5

2

1.5

1

0.5

0

3.5

3

2.5

2

1.5

1

0.5

0

European Apple Sawfly

91 92 93 94 AV

Year

Plum Curcu l i o 4

0 , , '

91 92 93 94 AV

Year

Green Fruit Worm

91 92 93 94 AV

Year

Fig. I. Percent injury ( ± SE) to fruit in harvest samples by insects causing damage before mid-June (1991-1994). In the case of tarnished plant bug, 70% of the fruit injured exhibited injury (dimples) too slight to cause reduction in grade. Therefore, we report here only the 30% that received injury sufficient to cause downgrading. Black bars = second-level IPM blocks; gray bars = first-level IPM blocks. * denotes a significant difference between second-level and first-level blocks.

40 R.J. Prokopy et al. // Agriculture, Ecosystem and Enoironment 57 (1996) 35-47

vs. 1.4% for lesser appleworm, 0.2 vs. 1.2% for leafrollers and 0.2 vs. 2.1% for apple maggot. Except for apple maggot, there was no such marked trend toward increased injury from the first 2 years compared with the last 2 years in first-level blocks (Fig. 2). For apple maggot, captures on unbaited red sphere monitoring traps averaged 16.9 vs. 12.3 per trap in second-level versus first-level blocks across all 4 years (a significant difference), suggesting some difference between block types in number of flies pene- trating the block interior. On average, 5901 apple maggot flies per block per year were intercepted on perimeter-tree baited red spheres in second-level blocks, indicating high population pressure.

Among foliar pests, there were no significant differences between second- and first-level blocks, either within any year or across all years, in mean population levels of apple aphids and spirea aphids

(combined), woolly apple aphids, European red mites or two-spotted spider mites (Fig. 3). On the other hand, each year leafminers averaged numerically fewer in second-level than in first-level blocks, with significant differences in 1991 and 1993 and across all 4 years (Fig. 4). White apple leafhoppers were significantly more abundant in second-level than in first-level blocks in 1991 but not thereafter nor across all 4 years (Fig. 4). Rose leafhoppers were significantly more abundant in second-level than in first- level blocks during both years in which they were sampled (1993 and 1994) (Fig. 4). Potato leafhoppers were significantly more abundant in second-level than in first-level blocks in 1992 and 1994 and across all 4 years (Fig. 4).

Among natural enemies of foliar pests, predators of aphids were very abundant in both types of blocks, with no significant differences between block types

3.5

3

2.5

• _~ 2

N 1.5

1

0.5

0

Codling Moth

91 92 93 94 AV

Year

4

3.5

3

2.5

• _~ 2

N 1.5

1

0.5

0

Lesser Apple Worm

91 92 93 94 AV

Year

4

3.5

3

2.5

2

1.5

1

0.5

0

Leaf rollers

91 92 93 94 AV

Year

Apple Maggot Fly

91 92 93 94 AV

Year

3.5

3

2.5

2

1.5

1

0.5

0

Fig. 2. Same as Fig. 1 except d a m a g e was caused b y insects act ive af ter mid-June. There was no injury in any b lock caused b y San Jos~

scale.

RJ. Prokopy et a l . / Agriculture, Ecosystem and Environment 57 (1996) 35-47 41

either within or across years (Fig. 5). For each block type, - 73% of observed aphid predators were larvae of Aphidoletes aphidimyza (Rondani). Nearly all of the remainder were larvae of Syrphus spp. For each year in which they were sampled (1993 and 1994), parasitoids of second-generation leafminer larvae were significantly more abundant in second- level than in first-level blocks (Fig. 5). For each block type, ~ 70% of parasitized leafminer larvae were parasitized by larvae of Sympiesis marylanden- sis Girault. Most of the remainder were parasitized by larvae of Pholetesor ornigis (Weed). Although phytoseiid mite predators were numerically less abundant in second-level than in first-level blocks in 1992, 1993 and 1994 and stigmaeid mite predators were numerically more abundant in second-level than in first-level blocks in 1991, 1992 and 1994, there were no significant differences between block types

in abundance of either type of predator, either within or across years (Fig. 5). Of the several hundred mite predators identified to species, all phytoseiids were Amblyseius fallacis (Garman) and nearly all stig- maeids were Zetzellia mali (Ewing).

4. Discussion

Up to mid-June, second-level IPM blocks in this 4-year pilot project were treated with pesticide against fruit-damaging insects and foliar-damaging arthropods to essentially the same extent as first-level IPM blocks. Thereafter, behavioral, cultural and biological control tactics were substituted completely for pesticide use against fruit-damaging insects and largely so against foliar-damaging arthropods. As expected, the extent of injury to fruit by insects

_-== 2

i

60 55

50

45

40 35

30

25

20 15

10 5

0

App le & Spirea Aphids

92 93 94 AV

Year

60 55

~ 45

~ 4o ~ as 2 30 ~- 2s ® 20

~ 10

5

0

Woo l l y A p p l e A p h i d s

t 91 92 93 94 AV

Year

European Red Mites 60 . . . . .

55 . . . . .

50'~ - . . . . . .

45 ~

=e 35 _= _= 30

2O

15

10

5

0

91 92 93 94 AV

Year

60 Two Spotted Mites

55 - -

50

45

40

35

30 . . . . .

25 - - -

20 . . . . . . .

15 . . . .

10

0 - - - i - I - - i

91 92 93 94 AV

Year

Fig . 3. M e a n popu la t ion l eve l s ( + S E ) o f fo l i a r a r th ropod pes t s in s econd - l eve l I P M b l o c k s ( b l a c k ba r s ) and f i r s t - l eve l I P M b l o c k s ( g r a y

ba r s ) ( 1 9 9 1 - 1 9 9 4 ) . * d e n o t e s a s i g n i f i c a n t d i f f e r e n c e b e t w e e n s ec ond - and f i r s t - l eve l b locks .

42 RJ. Prokopy et al. / Agriculture, Ecosystem and Environment 57 (1996) 35-47

causing damage before mid-June did not differ between second- and first-level blocks. Injury to fruit caused by insects active after mid-June was about the same in both types of blocks during the first 2 years of the project but was somewhat greater in second-level than first-level blocks during the last 2 years. Comparative abundance of foliar pests and their natural enemies in each block type varied according to species.

Many tree fruit researchers have predicted that grower implementation of more advanced levels of IPM may be accompanied by increased amounts of pest injury to fruit as pesticide use is reduced or eliminated. Results of 3- or 4-year studies in which practices equivalent to those of second- or third-level IPM were applied in California or Washington apple orchards support this prediction (Caprile et al., 1994; Vossen et al., 1994; Knight, 1995). Likewise, findings here are consistent with this prediction.

For codling moth, the amount of injury increase above that which occurred in first-level IPM blocks was only slight, even during the 4th year, when it reached a marginally acceptable level of 0.3%. But data trends suggest that if second-level IPM practices were to be employed continuously for 5 or more years, control of second-generation codling moth solely via management of the habitat adjacent to orchards, as practiced here, might not be sufficient to prevent economically important fruit injury. Alterna- tives, such as orchard treatment with mating disruption pheromone or biological control agents (eg. virus, bacteria, parasitoids), might be required in addition (van der Geest and Evenhuis, 1991; Howell et al., 1992; Caprile et al., 1994; Vossen et al., 1994; Knight, 1995).

For lesser appleworm, fruit injury in second-level blocks rose sharply and substantially in the 4th year, reaching an unacceptable level of 2.4% (compared

g

I 6

Z

60

55

50

45

40

35

30

25

20

15

10

5

0

Leafminers

91 92 93 94 AV

Year

60

55

5O

45

40 tO

~ 35 w 30 ~ 25

~ 20 N 15

10 5

0

White Apple Leafhoppers

91 92 93 94 AV

Year

m

8 >

60

Rose Leafhoppers

55

50

45

40

35

30

25

20

15

5

0

93 94 AV

Year

60

55

5O

~ 40 ~ 35 2 30

~- 2s ~ 20

N 10 5 0

Potato Leafhoppers

92 93 94 AV

Year

Fig. 4. S a m e as Fig. 3.

R.J. Prokopy et al. /Agriculture, Ecosystem and Environment 57 (1996) 35-47 43

with only 0.2% in first-level blocks) and suggesting that management of the habitat adjacent to orchards might be less reliable for control of second-generation lesser appleworms than second-generation codling moths. The host range of lesser appleworm is broader than that of codling moth (Chapman and Lienk, 1971). Thus, populations of lesser appleworm may have built up on host species which were not

removed from within 100 m of borders of second- level blocks. Much less is known about the biology and management of lesser appleworm than codling moth. Presently, there appear to exist few proven pesticidal alternatives for effective lesser appleworm control, although mating disruption via pheromone treatment may be a future possibility (Pfeiffer and Killian, 1988).

Leafrotler injury in second-level blocks reached an unacceptable level of 1.1% by the 4th year (compared with 0.1% in first-level blocks). The vast majority of such injury was caused by obliquebanded leafrollers and redbanded leafrollers. No overt measures were taken to control leafrollers in second-level blocks. In view of this fact and the much greater economic problems caused by leafrollers in other locales, both nearby (Agnello, 1992) and more distant (Pfeiffer et al., 1993), it is perhaps comforting that leafroller injury in second-level blocks rose to no greater heights than it did. Use of pheromone to disrupt leafroller mating (Agnello, 1992; Pfeiffer et al., 1993; Blommers, 1994) could be a viable alternative to pesticides for leafroller control should leafroller populations in Massachusetts orchards practicing

6O

55

~ 5o

40 ~ as £ 30 ~- 2s ~ ao

~ 15 N 10

5 0

91

Aphid Predators

92 93 94

Year

AV

60

55

50

45

40

35

30

25

20

15

10

5

0

2nd Generation Leafminer Parasitoids

93 94 AV

Year

Phytoseiid Mite Predators 10

9

8

m ~ 5 g 4 3 ~ 3

2

1

0

Stigmaeiid Mite Predators

91 92 93 94 AV 91 92 93 94 AV

Year Year

Fig. 5. Mean population levels ( + SE) of natural enemies of arthropod pests in second-level IPM blocks (black bars) and first-level IPM blocks (gray bars) (1991-1994). * denotes a significant difference between second- and first-level blocks.


second-level IPM reach levels that economically jus- tify such treatment.

Injury by apple maggot in second-level blocks reached 3.0% of sampled fruit by the 4th year. Although this amount of injury is unacceptable for most commercial growers, two factors modify inter- pretation of the extent of injury severity. First, apple maggot injury in pesticide-treated first-level IPM blocks likewise was exceptionally great (2.1%) during 1994. Secondly, an average of more than 12500 apple maggot flies was captured on perimeter-tree interception traps in second-level blocks in 1994, indicating extremely high fly population pressure. Conditions that were ideal for large build-up of apple maggot pupae beneath wild hosts during late summer of 1993, coupled with ideal conditions for overwintering of pupae thereafter, undoubtedly contributed strongly to the exceptional 1994 fly populations. Furthermore, it has been established that sticky red sphere traps lose about 25% of their fly capturing potential each week they are not cleaned of apple maggot flies and other insects (Duan and Prokopy, 1995). The trap servicing schedule did not permit cleaning more often than every 2 weeks, which must have allowed at least some proportion of alighting flies to escape from traps and move into the interior of blocks (possibly accounting for the average 37% greater number of flies captured on unbaited monitoring traps in second-level compared with first-level blocks). To overcome this disadvantage of sticky red spheres and to overcome the messiness associated with preparing and employing such spheres, development of pesticide-treated red spheres as an alternative is being pursued (Duan and Prokopy, 1995).

With respect to foliar pests and their natural enemies, it was gratifying but not surprising that neither apple or spirea aphids nor foliar populations of woolly apple aphids reached damaging numbers in any second-level blocks in any year. In fact, the same was true for first-level blocks. Substantial populations of aphid predators in both types of blocks provided excellent biocontrol. Two factors contributed to this favorable outcome. First, the time of Aphidoletes and Syrphus aphid predator peak activ- ity in orchards coincided closely with that of build- ing and peak pest aphid populations (mid-June to mid-July), a period during which even first-level IPM blocks normally receive little insecticide. Sec-

ondly, A. aphidimyza (to a lesser extent Syrphus spp.) is somewhat tolerant of both phosmet and azinphosmethyl (Croft, 1990), the most commonly used insecticides during June and July in Mas- sachusetts orchards practicing first-level IPM.

Disappointingly, populations of pest mites were not significantly lower and populations of predatory mites were not significantly greater in second-level than in first-level blocks. Indeed, in both types of blocks occasional post-bloom intervention with acaricide was required (Table 1) when pest mites exceeded threshold levels following pre-bloom treatment with horticultural oil. At least two factors may have contributed to the lack of a reliable level of predator control of pest mites in second-level blocks. First, of the two predaceous mite species found in second- and first-level blocks, A. fallacis is believed to be much more capable than Z. mali of providing effective biocontrol of moderate to high pest mite populations (Santos, 1976; Clemens and Harmsen, 1992; Croft, 1994; Nyrop et al., 1994; Hardman et al., 1995). However, A. fallacis appears to suffer high mortality during New York and Massachusetts winters (Nyrop, 1993; Hu et al., 1995), and for this and possibly also other reasons, was not found in samples from any block in any year until July, too late to have affected pest mite populations that reached damaging numbers before July. Secondly, even though both A. fallacis and Z. mali have developed considerable resistance to organophosphate insecticides of the type used in orchards involved here (Croft, 1990), they and other species of predaceous mites are known to be affected adversely by the fungicides benomyl, mancozeb or metiram (Baynon and Penman, 1987; Hagley and Biggs, 1989; Ioriatti et al., 1992; Hardman et al., 1995). All three of these materials were used in two or more spray applications to both second- and first-level blocks (principally during May and June) each year of this pilot project. They may have been a principal con- straining factor on predaceous mite build-up in both types of blocks (Cooley et al., 1995).

Advantages of second-level over first-level IPM practices in regard to foliar pest management were perhaps best exemplified by the significantly greater abundance of second-generation leafminer parasitoids in second-level than first-level blocks. Such parasitoids may have been a principal factor account-

R.J. Prokopy et a l . / Agriculture, Ecosystem and Environment 57 (1996) 35-47 45

ing for numerically lower levels of leafminer populations in second-level blocks each of the 4 years as well as for the fact that in no second-level block did second- or third-generation leafminer larvae (present in July or August) require intervention with pesticide (Table 1). Even so, the amount of parasitism of first-generation leafminer larvae (present in May and June) was no different between block types (R.G. Van Driesche, J. Mason and R.J. Prokopy, unpublished data), undoubtedly reflecting high parasitoid susceptibility to organophosphate insecticides (Pree et al., 1994) applied before mid-June to both types of blocks. Immigration of leafminer parasitoid adults from nearby wild host plants (Maier, 1994; Van Driesche et al., 1994) into second-level blocks after mid-June and their subsequent survival there in the absence of insecticide may largely account for the higher levels of second-generation leafminer parasitism observed in these blocks. Knight (1995) found greater levels of parasitism of leafminer larvae in blocks that received mating disruption pheromone for codling moth control compared with convention- ally sprayed blocks.

Perhaps the greatest shortcoming of second-level practices used here, with respect to arthropod foliar pest management, involves the significant build-up of leafhoppers after mid-June in second-level compared with first-level blocks. After the 1st year, white apple leafhoppers were not a problem in this regard. However, rose leafhoppers and potato leafhoppers were problems in second-level blocks each year in which they were sampled, sometimes requiring intervention with pesticide treatment (Ta- ble 1). First-generation rose leafhopper nymphs develop almost exclusively on rose bushes growing outside of orchards, with adults then immigrating into orchards from mid-June to mid-July and producing a second and third generation of nymphs in orchards during summer (Day and Hogmire, 1993; Straub and Jentsch, 1994). Similarly, potato leafhopper adults originating from far-distant sources (southern states of the USA) immigrate into orchards from mid-June onward, producing one or more generations of nymphs before moving to other plants. Conceivably, immigration of rose leafhoppers could be reduced to tolerable levels by removing rose bushes within yet undetermined distances from orchard borders. Nonetheless, some other currently

unavailable biologically based approach will have to be developed for managing potato leafhoppers if Massachusetts growers practicing second-level IPM are to cope with this pest in the absence of insecticide use after mid-June.

As reported in detail elsewhere (Prokopy et al., 1995), in second-level blocks there was variation among cultivars in the amount of fruit injury caused by insects active after mid-June and in abundance of foliar pests. Thus, codling moth and apple maggot inflicted more damage on 'Red Delicious' than on 'Cortland' or 'Mclntosh'. Lesser appleworm was particularly injurious to 'Cortland'. Leafroller was greater on 'Cortland' and 'Red Delicious' than on 'Mclntosh'. Mites, leafminers and leafhoppers were most abundant on 'Red Delicious'. This suggests that with respect to management of fruit- and foliar- damaging arthropods, orchard blocks composed pre- dominantly of cultivars such as 'Mclntosh' may reap maximum benefit with minimum disadvantage from employment of second-level IPM practices. Such may not be the case, however, for blocks comprising largely 'Cortland' or 'Red Delicious'.

As in this study on apple pest management, studies on the management of pests of other crops where biologically based approaches to pest control have been substantially or completely substituted for pesticidal approaches (e.g. Trumble and Alvarado- Rodriguez, 1993) likewise have indicated benefits. These include greater environmental health and food safety, build-up of certain beneficial organisms and reduced potential for development of pest resistance to pesticides. At the same time, however, there may be shortcomings in terms of increased levels of damage by some pests. To what extent might such potential benefits and shortcomings affect grower willingness to adopt advanced approaches to IPM?

In northeastern North America, many apple growers have gained considerable economic advantage by engaging in chemically based first-level IPM practices compared with non-IPM practices (Prokopy et al., 1980; Hull et al., 1983; Bostanian and Coulombe, 1986; Hardman et ai., 1987; Kovach and Tette, 1988; Agnello et al., 1994). However, costs associated with engaging in second-level IPM may exceed those of first-level IPM and be a disincentive to grower adoption of second-level IPM. For example, in this study, the expenses of biologically based

46 R.J. Prokopy et al . / Agriculture, Ecosystem and Environment 57 (1996) 35-47

methods for controlling fruit-damaging insects active after mid-June, coupled with losses of revenue result- ing from greater damage to fruit by insects con- trolled in this manner, resulted in about $US 260 ha- I lower net profit for second-level than first-level IPM blocks (Acquaye et al., 1996). Hopefully, sub- stitution of pesticide-treated spheres (Duan and Prokopy, 1995) for sticky spheres to control apple maggot (and consequent substantial savings in cost of labor to employ spheres) could negate much of the current economic disadvantage of second-level IPM practices. As discussed by McDonald and Glynn (1994), economic considerations actually may turn out to be less of a concern in apple grower adoption of second- or third-level IPM practices than other factors. These authors suggest that in northeastern North America, apple growers might be motivated to adopt more advanced IPM practices largely out of environmental concerns and associated social and psychological rewards. The authors concur with this assessment.

Acknowledgements

This work was sponsored by the Massachusetts Society for Promoting Agriculture, the Northeast Regional USDA Competitive IPM Grants Program, State/Federal IPM funds, and the Northeast Re- gional Sustainable Agriculture Research and Educa- tional Program. Thanks are extended to Roy Van Driesche for examining leafminers for evidence of parasitism and identification of parasitoids to species and Xingping Hu for identifying mite predators to species.

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