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"'1: ”H’IfiIIII'Ir | 1 1 ‘ I11I11..ff,.~1I.1,1111'1 1113111111111111 .I" I1 II1" "I 'K 11' III III": I 11'III'IHIIIII1 HUI“ I11H "'1111‘II1I 1‘111'111 1'1'I'11II'I111111111I I"'111 I1I1L"'11I"I1IJ'IIII'III «0—»... I" ‘ 'In.‘11lf'"\‘ 1“ I" "'1 1" 1 ‘1" 1‘ I 1. I. 1, “far: mllfllmlullflul‘flllllfllil 193 00103 5470 , I" Afiaig 0‘23 Stvfl - ”14"?” Ur‘ all; 2, it i!- :fiiafi' r ‘ ‘- This is to certify that the dissertation entitled BIOLOGICAL STUDIES ON APHIDOLETES APHIDIMYZA (RONDANI) (DIPTERA:CECIDOMYIIDAE) AND ITS USE IN BIOLOGICAL CONTROL OF THE APPLE APHID APHIS POMI DEGEER (HOMOPTERA:APHIDIDAE) presented by JOSEPH GRANT MORSE has been accepted towards fulfillment of the requirements for Ph . D . degree in Entomology 4/th Glad/5b Major profi/V or Date 9/10/87 MS U is an Affirmative Action/Equal Opportunity Institution 0~1277 l P RETURNING MATERIALS: 1V1£31_J Place in book drop to lJBRARJES remove this checkout from .—3-. your record. FINES will be charged if book is returned after the date stamped below. BIOLOGICAL STUDIES ON APHIDOLETES APHIDIMYZA (RONDANI) (DIPTERAzCECIDOMYIIDAE) AND ITS USE IN BIOLOGICAL CONTROL OF THE APPLE APHID APHIS POMI DEGEER (HOMOPTERA:APHIDIDAE) BY Joseph Grant Morse A DISSERTATION Submitted'to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Department of Entomology 1981 ABSTRACT BIOLOGICAL STUDIES ON APHIDOLETES APHIDIMYZA (RONDANI) (DIPTERA:CECIDOMYIIDAE) AND ITS USE IN BIOLOGICAL CONTROL OF THE APPLE APHID APHIS POMI DEGEER (HOMOPTERAzAPHIDIDAE) BY Joseph Grant Morse Aphidoletes aphidimyza is a larval predator which appears to show considerable promise in biological control of the apple aphid in Michigan commercial apple orchards. In addition, this cecidomyiid has potential as an aphid predator on a variety of agricultural crops, limited only by the suscep- tibility of the midge to dessication under conditions of low humidity. A simulation model of apple aphid development and repro- duction during summer months was first constructed from literature data using the heat unit.concept with lower and upper developmental thresholds of 37 and 95°F. respectively. Model output was compared with field sleeve cage data. Laboratory experiments on basic features of cecidomyiid biology were conducted to determine: (1) egg and larval developmental thresholds and developmental periods (larvae provided with excess aphids), (2) larval functional response to aphid density, (3) adult female longevity and fecundity under Optimal conditions and (4) search and oviposition behavior of females. Field experiments in commercial orchards Joseph Grant Morse were performed to investigate: (l) the timing and form of cecidomyiid pupal emergence from overwintering sites in the soil, (2) the use of aphid infested trap plants in monitoring adult occurance in both commercial and natural environments and (3) levels of cecidomyiid predation using terminal sleeve cages. Data from the apple aphid model and field and laboratory experiments were combined to form a predation simulation model. Larvae appear to kill up to 45 apple aphids per cecidomyiid in commercial orchards. Future research is needed on adult female search and oviposition behavior. Since larval mobility is limited, female behavior "regulates” the impact of cecidomyiid pre- dation. Additional priorities in future research to further refine the predation simulation model are presented. ACKNOWLEDGEMENTS I wish to express my deep appreciation to my advisor, Dr. Brian Croft, whose guidance, enthusiasm and editorial suggestions were invaluable in completion of this work. I also wish to extend my thanks to the members of my guidance committee, Drs. Erik Goodman, Gus Howitt, Gary Simmons and Fred Stehr for their suggestions and assistance throughout my Ph.D. program. In addition, Drs. Jim Bath, Ring Carde, James Miller, Dean Haynes and Mark Whalon provided assis- tance during several stages of my program. I also wish to thank Debra Cadotte, John Gilmore, Duane Jokinen, Joe Klein, Robert Kriegel, Matt Michels, Karen Strickler, Jose Velarde, Steve wagner and Leslie warner for their helpful input to various portions of this project. I reserve my special thanks and appreciation for my wife Nancy who provided encouragement throughout my program in addition to typing the final manuscript. ii TABLE OF CONTENTS LIST OF TABLES . . . . . . . . . . . . . LIST OF FIGURES . . . . . . . . . . . . I. II. III. INTRODUCTION 0 O O O O O O O .7 O 0 GENERAL COMMENTS ON MATERIALS AND METHODS A. LABORATORY EXPERIMENTS . . . . 1. Greenhouse Aphid Colonies . 2. Laboratory Cecidomyiid Colony 3. Hygrothermograph Records . . 4. Adult Cecidomyiid Aspirator 5. Environmental'Chambers . . . B. FIELD EXPERIMENTS . . . . . . . 1. Field Research Sites . . . . .. Klein 1979, 1980 . . . . b. Graham 1990 . . . . . . . 2. Emergence Cages . . . . . . 3. Sleeve Cages . . . . . . . . APPLE APHID SIMULATION A. INTRODUCTION . . . . . . . . . 1. Prevalence and Host Plants . 2. Life Cycle on Apple . ... . 3. Economic Importance on Apple iii Page vii ix mmmm 10 10 11 ll 11 ll l3 14 15 15 15 17 TABLE OF CONTENTS (cont.) B. C. D. OBJECTIVES AND METHODOLOGY . . . . . . . . 1. 2. 3. .Objectives . . . . . . . . . . . . . . . Use of the Heat Unit Concept . . . . . . Methodology . . . . . . . . . . . . . . LITERATURE REVIEW AND ANALYSIS . . . . . . 1. 2. 3. Determination of Thermal Developmental ThreShOIdS O O O O I O O O O O O I O O O a. Lower Threshold . . . . . . . . . . . b. Upper Threshold . . . . . . . . . . . Nymph Deve10pmental Period . . . . . . . Adult Fecundity and Survivorship . . . . APPLE APHID SIMULATION . . . . . . . . . . l. 2. 3. 4. 5. Simulation Structure . . . . . . . . . . Nymph Developmental Model . . . . . . . Adult Survivorship and Fecundity MOdel . Model Improvement Using Field Sleeve cage Data 0 O I O O O O O O O O O O O O a. Relative Duration of Nymphal Instars. b. Effect of Aphid Density . . . . . . . c. Effect of Tree Nutrient Status . . . Simulatioanesults . . . . . . . . . . . IV. CECIDOMYIID EXPERIMENTS A. B. INTRODUCTION 0 O O O O O O O O O O O O O O l. 2. Taxonomy and Worldwide Use in Biological contrOI O O O O I O O O O O O O O O O 0 Life Cycle . . . . . . . . . . . . . . . OBJECTIVES AND METHODOLOGY . . . . . . . . iv Page 19 19 19 20 22 22 22 26 27 27 34 34 34 38 41 46 46 47 49 56 56 58 62 TABLE OF CONTENTS (cont.). VI. C. LABORATORY EXPERIMENTS . . . . . . . . . . D. 1. 2. 3. 4. 5. Cecidomyiid Egg Development . . . . . . Larval Development With Excess Food . . Larval Functional Response . . . . . . . Adult Female Fecundity and Longevity . . Female Search and Oviposition . . . . . FIELD EXPERIMNTS O O O O O O O O O O O C O l. 4. Adult Emergence from Overwintering Sites a. Klein's Orchard 1979 . . . . . . . . b. Testing Emergence Cage Design . . . . c. Fall Seeding of Field Emergence Cages d. 1980 Emergence Cages . . . . . . . . Trap Plants Placed in a Non-Commercial setting 0 O O O C I O O I O O O i O O O 0 Summary of Early Season Cecidomyiid Appearance . . . . . . . . . . . . . . . Commercial Orchard Trap Plants Compared with Direct Larval Sampling . . . . . . CECIDOMYIID PREDATION SIMULATION A. B. C. OBJECTIVES AND METHODOLOGY . 3 . . . . . . SIMULATION STRUCTURE . . . . . . . . . . . l. 2. Egg Stage . . . . . . . . . . . . . . . Larval Stage . . . . . . . . . . . . . . SIMUMTION RESULTS 0 O O O O O O O O O O 0 DISCUSSION AND CONCLUSIONS A. APHID SIWMTION O O O C O O O O O O O O O B. EXPERIMENTS ON CECIDOMYIID BIOLOGY . . . . C. PREDATION SIMULATION . . . . . . . . . . . V Page 63 63 66 75 85 86 94 94 94 95 97 97 99 106 106 113 114 114 117 124 131 133 135 TABLE OF CONTENTS (cont.) VII. APPENDIX A. B. C. D. SIZE AND WEIGHT COMPARISONS FOR A, PISUM, E. PERSICM MD A. POMI C O O O O C O O O COMPUTER PROGRAM LISTING . . . . . . . . 1. Program Term . . . . . . . . . . . . . 2. Subroutine DEGD . . . . . . . . . . . 3. Subroutine DELAY . . . . . . . . . . . 4. Other Subroutines . . . . . . . . . . FIELD TEMPERATURE DATA . . . . . . . . . SPRAY RECORDS FOR GRAHAM STATION 1980 . . VI II C LIST OF REFERENCES 0 O O O O O O O O O O O 0 vi Page 136 138 138 145 147 148 152 157 159 TABLE 1. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. LIST OF TABLES Major Arthr0pod Pests Occurring in Apple orChardS Of MiChigan o o o o o o o o o o o o 0 1980-81 Cecidomyiid Colony . . . . . . . . . . Types of Damage Caused by A, pomi on Apple . . Coefficient of Variation Determination of Base Temperature . . . . . . . . . . . . . . . Heat Units Calculated for Nymph Developmental PeriOd O O O O O O O O O O O O O O O O O O O 0 Nymph Developmental Period Arranged by Month Of Birth 0 O O O O O O O O O O O O O O O O O 0 Adult Aphid Longevity . . . . . . . . . . . . Adult Aphid Fecundity . . . . . . . . . . . . Adult Survivorship and Fecundity Parameters . Simulated Effect of Aphid Density and Tree Nutrient Status on Aphid Fecundity . . . . . . Sleeve Cage and Simulation Data for Graham Station 1980 O O O O O O O O I O O I O I O O 0 Comparisons of Simulation Model Output and Sleeve Cage Data . . . . . . . . . . . . . . . worldwide Reports of the Use Of A, aphidimyza in Biological Control . . . . . . . . . . . . Literature Data on Cecidomyiid Egg Hatch.. . . Experimental Egg Hatch Data . . . . . . . . . Experimental Conditions and.Probit Analysis for the Cecidomyiid Egg Hatch Experiment . . . . . Heat Units and Standard Deviations for Literature and Experimental Data on Cecidomyiid Egg Hatch . vii Page 18 25 28 30 31 33 42 48 50 54 57 64 65 67 69 LIST OF TABLES (cont.) TABLE 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. 37. Literature Data on Larval Development with Excess Food Supplied . . . . . . . . . . . . . Experimental Developmental Data . . . . . . . Experimental Conditions and Probit Analysis for Larval Development . . . . . . . . . . . . Functional Response Data . . . . . . . . . . . Fecundity and L8ngevity of 22 Female Cecido- inids at 23.33 C. O O O O O O I O O O O O I O Fecundity and L8ngevity of 31 Female Cecido- inids at 16 I 39 C O I O O O O O I O O O O O O O Cecidomyiid Search and Oviposition Data . . . Klein 1979 Emergence Cage Data . . . . . . . . Testing Emergence Cage Design . . . . . . . . Klein 1980 Emergence Cage Data . . . . . . . . Graham 1980 Emergence Cage Data 1980 Rose Lake Trap Plant Data . . . . . . . . First Appearance of Cecidomyiids in the Spring Trap Plant and Terminal Sampling Data from Graham Station 19 80 O O O O O O O O O O O I 0 Simulated Effect of Aphid Density on the Speed of Larval Development . . . . . . . . . . . . Simulated Cecidomyiid Predation . . . . . . . Predation Data for Sleeve Cages Compared with Simulation Model Output . . . . . . . . . . . Size and weight Measurements for 3 Aphid Species Field Temperature Data . . . . . . . . . . . . Spray Records for Graham Station 1980 . . . . viii Page 71 72 73 78 87 88 92 96 .99 100 101 104 107 109 119 121 125 137 153 158 FIGURE 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. LIST OF FIGURES Graham Station Block 12 . . . . . . . . . . . Life Cycle of the Apple Aphid . . . . . . . . Sine Wave Simulation of Diurnal Temperatures. Aphid Developmental Rate Versus Mean Tenlperature O O O O O O O O O O O O O O O O 0 Black Box Model of Aphid Simulation . . . . . Flowchart of Aphid Simulation . . . . . . . . Conceptual Diagram of Nymph Distributed-Delay Deve10pmenta1 Model . . . . . . . . . . . . . Aphid Nymph Development . . . . . . . . . . . Conceptual Diagram of Adult Discrete-Delay Developmental Model . . . . . . . . . . . . . Aphid Adult Survivorship . . . . . . . . . . Aphid Fe cundi ty 0 O O O O O O O O O O O O O O Sleeve Cage Data Compared with Simulation MOdel output 0 O O O O O O O I O O O O I O O Cecidomyiid Life Cycle . . . . . . . . . . . Cecidomyiid Egg Developmental Rate . . . . . Maximal Larval Developmental Rate . . . . . . Second Instar Functional Response . . . . . . Third Instar Functional Response . . . . . . Cecidomyiid Fecundity at Two Temperatures . . Cumulative Adult Emergence from Orchard Over- wintering Sites . . . . . . . . . . . . . . . ix Page 12 16 21 23 35 36 37 39 40 43 44 55 59 68 74 83 84 90 102 LIST OF FIGURES (cont.) FIGURE 20. 21. 22. 23. 24. 25. 26. 27. 1980 Rose Lake Trap Plants . . . . . . . . . . Trap Plant and Terminal Sampling Data from Graham Station 1980 . . . . . . . . . . . . . . Black Box Model of Aphid/Cecidomyiid Simulation . . . . . . . . . . . . . . . . . . Cecidomyiid Egg Discrete Delay Developmental MOde 1 O O O O O O O O O O O I O O I O C O O O O O Cecidomyiid Larval Discrete Delay Developmental Model . . . . . . . . . . . . . . Reduction in Predation Due to Competition:CFACT Sleeve Cage Data Compared with Simulation~ Model Output (with Predation) . . . . . . . . . Comparison of Observed and Simulated Predation. Page 105 111 115 116 118 123 129 130 I. INTRODUCTION The major insect and mite pests of Michigan commercial apple orchards may be classified into 3 categories: direct key pests, secondary (indirect) pests and sporadic pests (both direct and indirect) (Croft 1975a, Brunner and Howitt 1981, see Table 1). Direct pests cause direct damage to apple (i.e. to the fruit itself). The very low tolerance for fruit damage and infestation at harvest dictates that direct pests be held to very low levels in commercial apple orchards. Indirect pests of apple feed on leaves or woody portions of the tree and because of their indirect action may be tol- erated at low to moderate levels. Because of this higher economic threshold for indirect pests, natural enemies of these species may often play important roles in commercial apple orchards. Sporadic pests are those species rarely found at economic levels in commercial apple orchards al- though they may occasionally appear and influence pest man- agement decisions. For the past 15 to 20 years, direct key pest control has relied heavily on the use of broadspectrum organOphosphate (O-P) insecticides (Croft 1979). To date no direct key pest has developed resistance to O-Ps (Croft 1981). Although.im- proved monitoring and prediction techniques for direct key pests (eg. Thompson et al. 1974, Riedl and Croft 1978, welch et al. 1978) may assist in reducing unnecessary sprays, control of direct key pests of apple will most likely con- tinue to depend on insecticide applications. 1 TABLE 1. Major Arthropod Pests Occurring in Apple Orchards of Michigan (adapted from Croft 1975a, Brunner and Howitt 1981) DIRECT KEY PESTS codling moth - Laspeyresia pomonella L. plum curculio - Conotrachelus nenuphar Herbst apple maggot - Rhagoletis pomonella Walsh oriental fruit moth - Grapholitha molesta Busck red-banded leafroller - Argyrotaenia velutinana Walker SECONDARY PESTS APHIDS apple aphid - Aphis pomi DeGeer rosy apple aphid - Dysaphis plantaginea (Passerini) wooly apple aphid - Erisoma lanigerum (Hausmann) MITES European red mite - Panonychus ulmi (Koch) two-spotted spider mite - Tetranychus urticae Koch apple rust mite - Aculus schlechtendali (Nalepa) SCALES San Jose scale - Quadraspidiotus perniciosus (Comstock) oystershell scale - Lepidosaphes ulmi (L.) European fruit Lecanium scale - Lecanium corni (Bch.) OTHERS oblique-banded leafroller - Choristoneura rosaceana Harris white apple leafhopper - Typhlocyba pomaria MacAtee tentiform leafminer - Phyllonorycter blancardella (F.) tarnished plant bug - Lygus lineolaris (P.de B.) SPORADIC PESTS fruit tree leafroller - Archips argyrospilus Walker tufted apple budmoth - Platynota idaeusalis Walker variegated leafroller - Platynota flavedana Clemens green fruitworms - F. Noctuidae eyespotted bud moth - Spilonota ocellana Denis lesser appleworm - Grapholitha prunivora Walsh - apple curculio - Tachypterellus guadrigibbus (Say) The history of the response of secondary pests and their associated natural enemies to O-Ps applied for direct key pest control may be divided into 3 phases (Croft and Hoyt 1978, Croft 1979). Initially both secondary pests and natural enemies were controlled to very low levels by O-Ps (Phase I). Quite rapidly several secondary pests (especially mites and aphids, see Figure l in Croft 1980) developed resistance to O-Ps and caused severe problems in apple because of the absence of their natural enemies (Phase II). O-Ps continued to be used for control of direct key pests and after a period of years (Phase III), several natural enemies of secondary pests developed resistance (especially mite predators, Croft and Brown 1975, Croft 1977). With the appearance of resistant natural enemies, the potential for integrated pest management (IPM) programs for secondary pest control has increased. Croft (1975b) has developed an IPM program for apple pest mites in Michigan utilizing the O-P resistant predatory mite Amblyseius fallacis. Suitable predator-prey ratios are maintained within the context of direct pest control through the con- servation of mite predators with selective pesticides and proper cultural practices. Within the past decade a cecidomyiid predator of aphids, Aphidoletes aphidimyza (Rondani), has become more common in commercial apple orchards (Adams 1977, Adams and Prokopy 1980). Warner (1981) has shown that O-P tolerant/resistant strains of this species are present in Michigan orchards where they show.considerable promise as biological control agents of the apple aphid, Aphis pomi. This study was undertaken to investigate the possi- bility of utilizing this predator in an IPM program for aphid control similar to that already developed for phytophagous mites. The objectives of this project were threefold: (1) To accumulate and organize existing bio- logical data on the apple aphid (A. pomi) so that a simulation model of aphid development and repro- duction could be developed (Section III), (2) To gather basic biological data on the cecidomyiid predator A. aphidimyza through literature review and laboratory and field experiments (Section IV), (3) To combine aphid and cecidomyiid biological data into a predation simulation model which could serve to (Section V): (a) Evaluate the impact of cecidomyiid predation in apple aphid control and (b) Orient future research on aphid-cecidomyiid population dynamics. II. GENERAL COMMENTS ON MATERIALS AND METHODS A. LABORATORY EXPERIMENTS 1. Greenhouse Aphid Colonies Greenhouse adapted pea aphids [Acyrthosiphon pisum (Harris)] and green peach aphids [Myzus persicae (Sulzer)] were used in many of the laboratory and field experiments as hosts for A, aphidimyza (both aphid colonies had been reared in MSU greenhouses for at least 3 years and were of unknown origin). Both species were reared in isolated 40x45x60 cm. screen covered cages in a greenhouse room attached to the Pesticide Research Center on the MSU campus. Pea aphids were chosen as the primary food source for the laboratory cecidomyiid colony because of their large size, rapid reproduction and ease of manipulation. They were reared on fava bean plants (Yigig £333 L., purchased from W. Atlee Burpee Co., Clinton, IA, listed as long pod fava beans) grown in 14 cm. diameter clay pots with 5-15 bean plants per pot. Green peach aphids were used in the larval functional response experiment because they were closer in size to apple aphids (see Section IV-C-3). These aphids were reared on turnip (Brassica rapa L., purple top, white globe - NorthrOp King seeds Minneapolis, MN) and jimsonweed (Datora stramoniom L., seeds collected from wild plants from the Lansing area courtesy of Lynn Oates) plants potted in 10.5 cm. diameter plastic pots. 6 2. Laboratory Cecidomyiid Colony A laboratory A, aphidimyza colony was maintained in room B10 of the Pesticide Research Center at MSU for use in lab- oratory and field experiments. Room temperature and relative humidity averaged 25.15°c. (range 23.3-27.1) and 45% (25-100) as measured using a hygrothermograph. Two or four 60 watt 2.4 m. flourescent lamps (suspended 10 cm. above each cage) provided an artificial light source with a 16:8 light/dark cycle (on 4am-8pm). A single 25 watt light bulb (on 6pm- 6am) was suspended 5-8 m. above the rearing cages to provide light for adult mating and oviposition (studies by Mansour 1976 indicate maximal oviposition at low light intensities with few eggs laid in unilluminated cages) and to allow for observation of adults after 8pm. ‘ The initial laboratory cecidomyiid colony (1979-80 colony) was started with approximately 200 larvae (mostly 2nd rd and 3 instars) collected on July 6, 1979 from apple aphid and rosy apple aphid colonies at the MSU Graham Horticulture Research Station near Grand Rapids, MI. In order to increase the colony size, approximately 300 eggs were collected from the Rose Lake Wildlife Station near Lansing, MI (using aphid infested trap plants to attract ovipositing females) on August 28, 1980 and were added to the eggs from the initial colony. This 1979-80 colony (made up of individuals collected from both sources) was carried through 18 distinct generations (from egg to first egg of the next generation) until the colony was discarded in May 1980 to make space available for the 1980-81 colony. Individuals from the 1979-80 colony were util- ized in the (l) cecidomyiid egg development experiment (Section IV-C-l), (2) emergence cage testing experiment (Section IV-D-l) and (3) diapause seeding experiment (Section IV-D-l), with the remainder of the experiments utilizing the 1980-81 colony. The 1980-81 colony was composed of eggs and larvae col- lected on four dates from the Graham Research Station. Approx- imately 85 larvae were collected on July 28, 1980 and another 300 on July 31. Approximately 600 and 250 eggs were collected on August 28-31 and September 1-4 respectively. The 1980-81 colony was carried through 15 distinct generations with 500- 2500 adults produced per generation. Each generation consisted of 3-7 cages containing cecidomyiids reared from eggs laid over a 2-5 day period (see Table 2). Eggs for each cage were pro- duced by adults from 2-4 cages of the previous generation (for example cage A eggs usually resulted from cages A and B of the previous generation; B from A,B,C; etc.). Each cage held up to 12 clay pots (14 cm. in diameter), each pot containing 5-15 fava bean plants infested with pea aphids. Silica sand or vermiculite was spread on the base of each cage to provide pupation sites for mature larvae. The cages were placed in water filled trays to provide isolation. As adult cecidomyiids appeared in a cage, 2-6 aphid infested pots (when possible young plants each 5 cm. tall were used so that a healthy aphid pOpulation would be supported for as long as possible; each pot was initially infested with approximately 100 pea aphids) were introduced into the cage for predator egg collection (if possible, colonies were worked with from 8am-noon TABLE 2. 1980—81 Cecidomyiid Colony Date Eggs Date Eggs Generation Cage Laid Generation Cage Laid l A 8/12-8/14 9 A 1/12-1/13 B 8/15-8/16 B 1/14-1/17 C 8/17-8/22 C 1/18-1/19 - D 1/20-1/21 2 A 8/27/8/29 E 1/22-1/23 B 8/30-9/2 F 1/24-1/26 C 9/3-9/4 D 9/5-9/7 10 A 1/27-1/29 B 1/30-2/1 3 A 9/12-9/17 C 2/2-2/4 B 9/18-9/21 D 2/5-2/6 C 9/22-9/23 E 2/7-2/8 D 9/24-9/26 F 2/9-2/11 4 A 10/2-10/6 11 A 2/15-2/16 B 10/7-10/9 B 2/17-2/20 C 10/10-10/12 C 2/21-2/23 D 10/13-10/15 D 2/24-2/25 E 2/26-2/27 5 A 10/23-10/25 F 2/28-3/1 B 10/26-10/28 C 10/29—10/30 12 A 3/6-3/9 D 10/31-11/2 B 3/10-3/12 E 11/3-11/5 C 3/13-3/16 F 11/6-11/9 D 3/17-3/18 E 3/19-3/20 6 A 11/10-11/15 F 3/21—3/22 B 11/16-11/18 G 3/23-3/24 C 11/19-11/20 D ll/21-ll/22 13 A 3/29-3/30 E 11/23-11/26 B 3/31-4/1 ' C 4/2-4/3 7 A 11/30-12/3 D 4/4-4/5 B 12/4-12/9 E 4/6-4/7 C 12/10-12/11 F 4/8-4/11 D 12/12-12/14 E 12/15-12/17 14 A 4/14-4/17 v B 4/18-4/19 8 A 12/19-12/25 C 4/20-4/22 B 12/26-12/28 D 4/23-4/25 C 12/29-12/30 E 4/26-4/27 D 12/31-1/2 F 4/28-5/1 E l/3-1/4 F 1/5-1/7 15 A 5/2-5/5 B 5/6-5/8 while adults were inactive; later in the afternoon adults became more active, and thus were more likely to escape from the cage). After several nights of oviposition, adults were removed from the plants (by tapping or blowing) and the pots were placed in a new cage. Aphid abundance was carefully monitored especially during periods of peak larval feeding and aphids were removed or added as necessary. After all larvae had drOpped into the soil to pupate (about half pupated in the soil in the pots with the remainder in the sand on the cage floor) the bean stems were cut and removed and the pots stacked in the back of the cage to provide room for later intro- duction of plants for egg collection. The removal of the old stems insured that eggs would be laid on only the new plants. Frequent watering (a minimum of every 2 days) was essen- tial for maintenance of a healthy cecidomyiid colony in order to provide adequate plant growth for the aphids, high humidity conditions for the larvae and adequate soil moisture for the pupating cecidomyiids (sand on the cage floor and soil in the pots was watered after removal of the stems to maintain moisture levels for the pupae: the vermiculite and sand aided in water retention). 3. Hygrothermograph Records Temperature and relative humidity records were maintained for several laboratory and field experiments. Hygrothermographs used were Bendix Model 549 and weather Measure Corp. Model 3311 using 1 week strip charts. Both models recorded degrees Fahrenheit and were calibrated weekly using a thermometer 10 (t 10F.) and dial hygrometer (* 5%). Estimates of constant temperature in laboratory exper-. iments were calculated by averaging hourly hygrothermograph readings. Simulations of field conditions utilized daily maximum and minimum (from noon of the previous day to noon of the given day) temperatures (see Section VII-C for maximum and minimum temperatures for various field sites). 4. Adult Cecidomyiid Aspirator Adult cecidomyiids are extremely fragile but are quite easy to collect if handled gently in morning hours (6am-2pm) when they are fairly inactive. An oversized aspirator was constructed using 1.5 cm. diameter plastic tubing which when combined with a very gentle aspiration pressure resulted in acceptable adult mortality ((10%). 5. Environmental Chambers Several Sears Coldspot refrigerators which had been modified using the methods of Platner et al. (1973) were utilized in constant temperature laboratory experiments. Interior dimensions were 45x45x72 cm. with illumination provided by a single 15 watt fluorescent lamp set on a 16:8 light-dark schedule (on 4am-8pm). Since plants were isolated (mainly from ants) by small water-filled trays, the humidity bath was discarded. A hygrothermograph was placed in the refrigerator to monitor temperature and relative humidity. 11 B. FIELD EXPERIMENTS 1. Field Research Sites a. Klein 1979,1980 Two apple orchard blocks were used in several field experiments in 1979 and 1980. The first was a commercial block near Sparta, MI owned and operated by Joe Klein. The second block was part of the MSU Graham Horticulture Re- search Station located just west of Grand Rapids, MI. The southeast block of Klein's orchard (12239 Fruit Ridge Rd., at the corner of Fruit Ridge and 13 Mile Rd.) was used in 1979 and 1980 to monitor cecidomyiid emergence fnunoverwintering sites in the soil (Section IV-D-l). This block was chosen because large cecidomyiid populations were observed during July and early August of 1978 and 1979. The block consisted of approximately 415 standard sized trees of McIntosh, Jonathan, Spy and Banana varieties. b. Graham 1980 Block 12 of the Graham Station was used in 1980 for a number of experiments. The Graham Station is a 3-3/4 acre research station containing apple, pear, cherry, plum and peach trees for horticultural research. Block 12 consists of 60 standard sized trees planted on seedling rootstock with Virginia Crab interstock. The block was planted in 1951 with a 8.5 m. tree spacing on the diagonal and contains 17 Jonathan, 18 Red Delicious, l6 McIntosh and 9 Red Rome trees (see Block 12 Map - Figure l). The block is surrounded to the north by an open field, to the east by 12 FIGURE 1. Graham Station Block 12 (60 trees) .Wou POE I I / q I ’I I O [I . (I ’/ N \ \ \ \ ~ ~ B x ‘\ “ a “ 4 ‘~ 2 i 8 ‘x ‘\ \ o ‘ 0 Q q g \\ \ \ \‘\ ‘\ ‘\ 3 \\ 7 ‘\5 “. 3 ‘s 1 \ 0 g \. g ‘0‘ m9 3 \ \ “ \‘ \\ \\‘ \‘ \“ . \ l \\ \6 ‘3 ‘2. \ . V . \ x \ \‘ \ \ \\ ‘ \ \ x m —. )0 I I I I N I , (I ,( I! ’I I ’I & 'I I I I N > f a Inqouoa ,oa L I’ on I (a ’I ’0 1. t— I I I I 0 t I ’ I I I (I I I I «L I I s: ‘ f \ ‘\ ‘\ B \\ \\a \‘ 8- 3 \3 , ~g : 0‘ 0“ x ‘. . ‘ ' ‘ s \ g 2 ‘\ \\\ 2 \\ \\ 1 \ g . \\% \. \g‘ M5 \ \ “ \ \ \ _ s \ F I I I ’d I I ’I .L I/ .5 I I .5 13 Block 10 and 11 (similar in structure to 12), to the south by a block of mixed variety apple trees and to the west by a block of young mixed variety trees (transplanted in 1978). Pruning during the dormant season was performed to remove shoot growth in the inner portions and base of the tree. Weak and non-bearing limbs were also removed. Section VII-D contains the spray record for Block 12 and other apple trees on the Graham Station (see Figure l for fungicide treatment rows A-D). ' 2. Emergence Cages Cone shaped emergence cages were used in 1979 and 1980 to trap cecidomyiid adults emerging from overwintering sites in the soil. The cages had a base diameter of 76 cm. and thus covered an area of .46 m2. The cages were constructed of wire mesh screening with Openings 1.6xl.6 mm. The cone was 66 cm. in height with an apex opening 11 cm. in diameter. A collection chamber was constructed from a jello mold 21 cm. in diameter and 6 cm. high. The inside lip of the mold was shortened to a height of 3 cm. The collection chamber was fit tightly over the emergence cone apex, filled with 2-5 cm. of a 1:2 ethylene glycol/water mixture and covered with a piece of plastic wrap (polyethylene) secured by a rubber band. Cecidomyiid larvae released into the cage in the laboratory were observed to fly upwards into the collection chamber where they eventually contacted the ethylene glycol and were captured (see results of laboratory tests on emergence cage trap efficiency, Section IV-D-l). l4 3. Sleeve Cages Sleeve cages were constructed to enclose aphid and cecidomyiid infested apple terminals. The sleeves were built of white nylon parachute cloth (100% nylon, .88 oz./square yard, purchased from Army Surplus) and were approximately 50 cm. in length with a diameter of 20 cm. One end was sewn shut and the other end was slipped over the terminal and secured with a string. The sleeve cages were tested using a Lamda Instruments Corp. LI-185 Quantum/Radiometer/Photometer (courtesy of Dr. Jim Flore) which showed light penetration reduced by the nylon cloth 21.08%. Temperatures and relative humidities inside the sleeve cages were estimated by enclosing a hygrothermograph with 3 apple terminals inside a specially constructed oversized sleeve cage (see Section VII-C). III. APPLE APHID SIMULATION A. INTRODUCTION 1. Prevalence and Host Plants The apple aphid (Aphis pomi DeGeer) is of EurOpean origin and was first reported damaging young apple trees in the eastern United States in 1849 (Matheson 1919). It presently occurs throughout the apple growing areas of the United States and Canada as well as in Europe and Asia (Baker and Turner 1916, Brunner and Howitt 1981). Patch (1923) lists 5 species of plants in the rose family (Rosaceae) upon which overwintering eggs are laid including apple (Malus sylvestris Mill.) and pear (Pyrus japonica Thunb.). Both Patch (1923) and Evenhuis (1963) indicate they believe the majority of overwintering eggs are laid on trees other than apple. Patch (1923) also lists 49 species of plants in 24 different families upon which summer generations of the apple aphid have been observed. The majority of reports of large summer populations deal with apple and to a lesser extent pear although Fluckiger et al. (1978) have observed high levels on hawthorn (Crataegus monogyna). 2. Life Cycle on Apple The life cycle of the apple aphid is depicted in Figure 2. The aphid overwinters as a diploid egg laid on the bark of water sprouts and terminals that have grown the previous season (Peterson 1918). Eggs hatch in mid-April to early May and give rise to the fundatrix or stem mother. The stem 15 16 FIGURE 2. Life Cycle of the Apple Aphid VERWINTERING EGGS STEM ' [ MOTHERS J ‘ ........................ B. r :o . - : :a OVIPARAE I .0 (Egg Produclng Forms . , N ' :A * ’ u IF! : {I :v I I I 1 P :9 ‘ ‘ : H " :A GYNOPARAE : S :P ‘80! Produclng Forms) : (H * t , H I F) I - ---------- _, :5." : . :u E r l ‘ 9% i Q=Iscum>rnaH 1 ADULTS J ET L-------------"-.---.Emisntml-.Pmmsm--_:g POPULATION OUTSIDE ORCHARD 17 mother is the first of a large number of summer parthen- ogenic generations. Three morphological forms of summer parthenogenic females are observed on apple. The majority of the 2nd generation (the offspring of the stem mothers) and lesser prOportions of succeeding summer generations are composed of alate (winged) viviparous females which serve as the major means of population dispersal. Factors known to increase the ratio of alatae/apterae (wingless) aphids in other aphid species include high aphid density, poor host plant condition, ancestry and temperature/photo- period (Lees 1966). The apterae (wingless viviparous females) are the most abundant form in the 3rd and following summer generations under uncrowded conditions. A relatively small number of aphids in each of the summer generations is ob- served to be of an intermediate form (Baker and Turner 1916, Matheson 1919). During August to September the sexual forms are produced which mate and lay the overwintering eggs. 3. Economic Importance on Apple Table 3 lists the problems associated with large apple. aphid populations on apple (adapted from Adams 1977). The greatest impact is on young trees where large populations may reduce growth and development. Apple aphids are rarely a severe problem on mature trees with standard rootstocks (Madsen et al. 1975, Brunner and Howitt 1981) although large continuous populations can cause economic damage due to deposition of honeydew on the fruit which provides an excellent medium for the growth of sooty mold fungus. 18 TABLE 3. Problems Associated with Large A. pomi Populations on Apple (adapted in part from Adams 1977) Feeding on fruits. Leaf curling. Stunting of terminal growth, reduction of fruit size by large populations (Brunner and Howitt 1981). Possible transmission of organism causing fireblight, Erwinia amylovora (Oatman and Legner 1961, Cutright 1963, Plurad et al. 1965). Later work by Plurad et a1. 1967 have questioned A. pomi's role as a fireblight vector. Honeydew may serve as primary food source for adult apple maggot, Rhagoletis pomonella (Neilson and Wood 1966, Boush et al. 1969). Excretion of honeydew with subsequent growth of sooty mold fungus (Fumago vagans Fries) on fruits and foliage. Overall effect on tree quality caused by nutrient with- drawal (poorly quantified). 19 B. OBJECTIVE AND METHODOLOGY 1. Objectives The objective of Section III was to develop a simulation model of apple aphid development and reproduction during summer months (June 1 - August 31) on a single apple terminal. This simulation was then coupled with the cecidomyiid de- velopment and predation simulation of Section V. 2. Use of the Heat Unit Concept For a review of this concept see Davidson (1944), Andrewartha and Birch (1973) and Campbell et al. (1974). Since insects are poikilothermic animals, develOpment would be expected to proceed as some function of accumulated heat units. A simple assumption proposed by Oettingen (1879) is a linear relationship between rate of development (inverse of developmental time if at constant temperature) and temper- ature. Several studies since have shown the actual.relati0n- ship to be curvilinear (Janisch 1925, Davidson 1944), the departure from linearity being most pronounced at the extremes of temperature. The types of errors introduced by assuming the linear relationship are discussed in Arnold (1959), Campbell et a1. (1974) and Gutierrez and Wang (1977). The majority of biological data accumulated in this thesis is expressed using heat unit accumulations above a theoretical developmental threshold (with the linear re- lationship assumption) as the independent variable. Daily field temperature fluctuations are assumed to approximate a modified 3-point sine wave (Baskerville and Emin 1969, 20 Allen 1976, see Subroutine DEGD in Section VII-B-2) fit to daily maximum and minimum temperatures. Figure 3 depicts an example of a heat unit calculation using the 3-point sine wave on a hypothetical day with a maximum temperature of 100°F. and minimums of 400 and 30°F. (minimum that morning and the night following, respectively). Heat units are calcu- lated by integrating under the sine wave below an upper de- velopmental threshold of 95°F. and above a lower threshold of 37°F. (note that the Fahreheit scale is used because both climatological records and hygrothermograph charts are scaled in 0F.). 3. Methodology The majority of model parameters for the aphid section were estimated from analysis of literature data (Section III- C). The output of the simulation model constructed using these parameters was then compared with data obtained from 34 sleeve cages placed on aphid infested terminals at Graham Station during the summer of 1980. Additional model parameters (which were unavailable from literature sources) were then estimated by "tuning" the simulation model with the aphid sleeve cage data. Model structure, estimated model parameters and simulation results are presented in Section III-D. 21 FIGURE 3. Sine wave Simulation of Diurnal Temperatures 1 . 0'55‘5'15 """" ' THRESH. am - 3 E 507 16.19 4.1 ‘ E \\\// Ed'v’vié'fi‘fii'fié's'fiom \ 25: TIME OF DAY IN RADIANS (o, 21=TIME OF MIN.;11 = MAX.) EQUATIONS: AMP- (MAX-MIN)/2 TBARP (MAX+MIN)/2 TEMP(X)- AMP*SIN(X-PI/2)+TBAR PMTERS‘ First Half Day Second Half Maximum Temperature (°F.) 100 100 Minimum Temperature (°F.) 40 30 AMP ’ 30 35 TBAR 70 65 Calculated Heat Units 16.19 14.19 Lower Threshold- 37°F. Upper Threshold- 95°F. 22 C. LITERATURE REVIEW AND ANALYSIS 1. Determination of Thermal Developmental Thresholds a. Lower Threshold Lathrop (1923) measured development times (from date of birth to date first young produced) for 20 aphids held in sleeve cages on apple terminals at Corvallis, OR during the summer of 1920. He also calculated the mean temperature over the developmental period of each aphid (the average of 1/2 hour temperature readings on a recording thermometer). He plotted average temperature versus days to develop (Figure 8 in his paper) and estimated the lower developmental threshold to be 41°F. (5°C.) using a hyperbolic relationship between average temperature and days. Lathrop's original data (as they appear in Table 5 of his paper, see Table 5 of this paper) are reanalyzed using linear regression (Figure 4). In Figure 4, the inverse of days to develop is plotted versus mean temperature, resulting in a r2 value of .70 and a theoretical develOpmental threshold of 37.2°F. (using the x-intercept method of Arnold 1959). Note that this linear regression method is more accurate but mathe- matically equivalent to Lathrop's hyperbolic curve method.l 1Equivalence may be seen as follows: Linear Regression: l/D = mT + c D days to develop T average temperature c -x-intercept l/Dm = T + c/m D = (l/m)/(T + C/m) . Lathrop's Hyperbolic Equation: x = a/(y-b); x = days to develop y = average temperature b = his threshold These are equivalent with 1/m = a,b = -c/m 23 FIGURE 4. Aphid Developmental Rate Versus Mean Temperature (Data from Lathrop 1923) 0‘” U V U U U — Linear Regression w/ all 20 Aphids ° Jar ---- L. a. without 19"1 Aphid .. 1 4 2 Data Points It 2 2.031- eg 0 o O 2. .4» 3 v=-.140395+.004007x, . 112:. 7994 E .04. 19*" Aphid — I g Y: -.150592+.004046x g 112: .7001 302-» 10 >' (O O 50 65 ' 60 9 36.53 Mean Temperature (°F.) 24 Lathrop noted that aphid no. 19 was reared on mature th foliage which retarded its development (see 19 aphid in Figure 4). This data point was deleted from the data set and a new linear regression performed resulting in an r2 value of .80 and a theoretical deve10pmental threshold of 36.5°F. A second method of calculating the base temperature is the lowest coefficient of variation method (Arnold 1959). Heat unit summations are calculated for a data set using various base temperatures and the one giving the least varia- tion is chosen as the lower theoretical deve10pmental threshold. These two methods are equivalent when using the sgmg_temperature profile (Arnold 1959), although the x-intercept method is quicker and has the advantage of indicating any departures from the assumed linear relationship between temperature and developmental rate. The lowest coefficient of variation method was also used in analysis of Lathrop's (1923) 19 aphids. Daily maximum and minimum temperatures (from Table 2 of his paper) were used with Subroutine DEGD (see Section VII-B-2, daily temperature fluctuations were assumed to be in the form of a sine wave fit to daily maximum and minimums) to calculate heat unit sums over the develOpmental period for each aphid. Sums are listed in Table 4 and include 1/2 of the heat units on the day the aphid was born and none of the heat units on the day first young were produced. As can be seen from Table 4, this method indicates 42°F. as the best lower developmental threshold versus 37°F. using the x-intercept method. 25 TABLE 4. Coefficient of Variation Determination of Base Temperature Lower Upper Mean Heat Units Standard Coefficient Threshold Threshold for 19 aphids Deviation of Variation (OF.) (OF.) (R) (Sx) (Sx/R) 36 95 260.458 46.468 .178 37 95- 248.684 42.396 .170 38 95 237.416 39.477 .166 39 95 226.184 36.528 .162 40 95 215.153 33.949 .158 41 95 204.353 31.725 .155 42 95 193.784 29.893 1121 43 95 183.447 28.470 .155 44 95 123.353 27.373 .158 26 Most studies to date using a heat unit calculation for the apple aphid (Lathrop 1923, 1928, westigard and Madsen 1965, Specht 1970, 1972, Jokinen 1980) have used Lathrop's (1923) 41°F. (5°C.) threshold. Since more accurate temperature data was used in the x-intercept method (1/2 hour temperature readings versus daily maximum and minimums) I have chosen to use the 37°F. lower theoretical developmental threshold. Certainly more data (calculations are based on 19 aphids reared at a single site) is needed to resolve this question. Note that the accuracy of the lower threshold is of importance only when the range of temperature fluctuations frequently crosses 'the threshold (during early and late season). b. Upper Threshold LeRoux (1959) noted 48 and 95% reductions in two apple aphid populations sampled after a 3-day exposure to temperatures averaging 90°F. in Rougemont, Quebec. Madsen et al. (1975) observed that prolonged high temperatures (up to 110°F.) caused considerable apple aphid mortality in a California orchard. Based on observations over a 3-year period at Watsonville, CA, Westigard and Madsen (1965) stated that temperatures below 90°F. had no appreciable effect on apple aphid p0pulations but that prolonged exposure to temperatures above 95°F. caused aphid mortality. Based on these reports an upper developmental threshold of 95°F. with a horizontal cutoff was used (Baskerville and Emin 1968, see Figure 3). Since daily summer temperatures in Michigan rarely average 95°F. or greater (based on climato- logical records) aphid mortality from high temperatures was assumed to be negligible. 27 2. Nymph Developmental Period Many factors influence the rate of nymph development including temperature, humidity, tree nutrient status and aphid density. For the purposes of the aphid simulation, nymph development was modeled on the basis of heat unit accumulations for the months of June-August. The effects of poor tree nutrient status and high aphid density were modeled by reducing aphid fecundity using scalar functions (see Section III-D-4). Data for estimation of nymph developmental parameters comes from aphid cage studies from Ithaca, NY (Matheson 1919) and Corvallis, OR (Lathrop 1923). Table 5 contains heat unit totals (over the nymph developmental period) for this data calculated using Subroutine DEGD (Section VII-B-l). Table 6 summarizes the data organized by the month of birth. For the 119 aphids born June 1 - August 31 the mean developmental period t 63.98 HU (Heat Units t standard deviation with was 272.19 thresholds 37,95; see Figure 8 for a comparison of literature data from Table 6 and the results of the simulation model). 3. Adult Fecundity and Survival Model parameters for adult fecundity and survival were obtained through analysis of the life histories of 39 aphids (generations 2-8 in Reproduction Chart 1 of his paper, apterous females only) reared by Matheson (1919) at Ithaca, NY during the summer of 1915. Adult longevity (in terms of heat units) was first calculated and is displayed in Table 7. Adults l+ lived an average of 655.79 154.35 heat units (see 28 TABLE 5. HEAT UNITS CALCULATED FOR NYMPH DEVELOPMENTAL PERIOD A. Data for 60 aphids reared at Ithaca, NY in 1915 by Matheson (1919). Temperature data from 0.3. Weather Service, Climatological Data 1915 for Ithaca, NY. Gener- Date Gener- Date ation Born Heat Unitsl ation Born Heat Units 1 4/25 3* 031.7) 7 7/14 3*(306.8) 4/26 319.1 7/14 344.3 4/28 227.1 7/16 .268.8 2 5/14 445.8 8 7/21 396.3 5/14 310.3 7/24 265.0 5/17 419.5 9 7/29 591.6 5/17 441.5 8/1 438.0 3 ~6/1 455.5 8/2 2*(397.8) 6/3 6*(408.8) 8/3 368.0 6/3 311.1 10 8/15 3*(255.0) 4 6/11 358.0 8/15 288.6 6/12 350.3 8/17 287.5 6/12 294.1 11 8/23 319.3 6/13 263.8 8/23 250.8 6/14 265.5 8/24 3*(317.0) 6/14 229.0 8/24 283.7 5 6/24 2*(303.0) 12 8/29 348.0 6/24 329.8 13 9/4 464.0 6/25 282.2 9/5 389.8 6/25 309.0 9/5 ' 460.8 6 7/4 313.2 9/6 357.5 7/4 276.6 9/6 397.5 7/4 351.6 B. Data for 72 aphids reared at Corvallis, OR in 1919 by Lathrop (1923). Temperature data from 0.8. Weather Service, Climatological Data 1919 for Albany, OR (near Corvallis). Aphid Date Aphid Date Number Born Heat Units Number Born Heat Units 1 3/31 383.6 10 6/10 275.8 2 4/29 301.6 11 6/12 270.2 3 5/17 292.9 12 6/13 229.0 4 6/2 277.7 13 6/17 274.0 5 6/3 276.5 14 6/18 250.2 6 6/4 250.0 15 6/20 239.0 7 6/5 250.3 16 6/21 239.3 8 6/6 256.3 17 6/22 . 240.3 9 6/9 268.0 18 6/23 219.3 lHeat units totals (37,95)calcu1ated using Subroutine DEGD include % of the day of birth and none on the day first young were produced. Multiple data points indicated as n*(H) (n aphids, with H heat units over the developmental period). 29 TABLE 5 (cont.) B. Corvallis, OR 1919 (cont.) Aphid Number 19 20 21 22 23 24 25 26 27 28 29 30 31 32 Date Born 6/24 6/25 6/26 6/27 6/28 6/29 6/30 7/1 7/2 7/3 7/4 7/6 7/7 7/8 7/9 7/11 7/12 7/13 7/14 7/16 7/29 7/30 7/31 8/3 8/4 8/7 8/8 Heat Units 253.0 272.8 275.5 255.7 268.0 217.2 267.7 275.6 270.9 242.6 269.7 257.7 306.3 331.5 268.8 268.8 322.1 296.1 219.1 252.2 269.8 272.3 278.5 214.1 379.0 293.7 292.0 Aphid Number 46 47 48 49 50 51 52 53 54 55 Date Born 8/11 8/12 8/13 8/14 8/16 8/19 8/20 8/21 8/23 8/24 8/25 8/26 8/27 8/28 8/29 8/30 8/31 9/1 9/2 9/3 9/5 9/6 9/8 9/10 9/11 9/13 9/16 Heat Units 231.0 240.8 214.8 287.0 244.3 268.0 293.6 257.8 253.5 283.1 293.0 266.5 278.0 317.3 306.3 516.2 284.0 300.0 280.0 332.8 315.5 294.5 308.2 265.8 298.5 368.1 314.3 C. Data for 20 aphids reared at Corvallis, OR in 1920 by Lathrop (1923). Temperature data from Lathrop (1923, see Section III-C-l-a). Aphid Number O‘DQOUIwaH H Date Born 3/28 5/3 5/13 5/16 5/31 6/2 6/9 6/14 6/17 6/21 Heat Units 351.2 195.6 273.1 262.8 243.5 279.8 243.1 250.8 194.3 184.5 Aphid Number 11 12 13 14 15 16 17 18 19 20 Date Born 6/27 6/30 7/7 7/9 7/18 7/28 8/12 8/20 8/20 8/23 Heat Units 230.5 231.8 274.0 223.5 250.8 228.3 305.0 299.3 482.4 203.1 2 219th aphid reared on mature foliage was deleted in av- erage developmental period calculation (see Section III-C-l-a). TABLE 6. Arranged by Month of Birth Nymph Developmental Period 30 Month Born March-April May June July August September Site & Year Itha Alba Corv Itha Alba Corv Itha Alba Corv Itha Alba Corv Itha Alba Corv Itha Alba Corv 1915 1919 1920 1915 1919 1920 1915 1919 1920 1915 1919 1920 1915 1919 1920 1915 1919 1920 Number l—‘NU‘I 1Sites and data sources were: Ithaca, NY, Albany, OR, Corvallis, OR, 1915 - Matheson (1919) 1919 - Lathrop (1923) 1920 - Lathrop (1923) Developmental Period (Heat Units) Me an 322.2 320.6 286.4 293.8 297.9 343.2 Standard Deviation 45.3 92.3 63.9 67.5 62.3 61.8 31 TABLE 7. Adult Aphid Longevity Heat units over the adult life are calculated for the 39 aphids in generations 2-8 (apterous females only) from the data of Matheson (1919) Generation Day lStYoung Day Died Heat Units(37,95)l 2 6/9 7/9 845.5 6/9 7/12 936.0 6/10 7/2 626.1 6/4 6/19 452.1 6/4 6/20 479.0 3 6/15 7/5 578.7 6/18 7/6 503.8 6/18 7/2 383.6 6/18 7/13 706.8 6/18 7/16 818.1 6/18 7/17 854.8 6/18 7/17 854.8 6/18 7/4 448.3 4 6/25 7/20 783.3 6/24 7/18 738.0 6/22 7/19 810.0 6/22 7/18 774.5 . 6/24 7/14 591.3 6/22 7/22 889.5 6/22 7/9 466.2 5 7/5 7/21 515.0 7/5 7/22 539.8 7/5 7/26 675.8 7/6 7/19 433.5 7/6 7/29 746.0 6 7/15 8/6 755.8 7/14 8/1 630.5 7/16 8/1 555.5 7/19 8/10 734.8 7/15 7/27 410.0 7 7/24 8/14 726.7 7/24 8/7 497.5 7/24 8/9 561.5 7/25 8/16 761.0 7/25 8/8 492.3 8 8/1 8/22 675.8 8/2 8/25 737.3 8/8 9/6 852.2 8/7 9/1 734.5 65578 i 154.4 Range 383.6 - 436.0 lHeat units include 8 of the amount on the day of death and all of the heat on the first day young were produced. 32 Figuré 10 for a comparison of simulation model output and literature data from Table 7). Adult fecundity was estimated by calculating cumulative fecundity of the 39 aphids based on a heat unit scale (Table 8). Average fecundity for Matheson's (1919) 39 aphids was 60.72 offspring per female (see Figure 11 for comparison of simulation model output and literature data from Table 8). 33 TABLE 8. Adult Aphid Fecundity1 Cumulative Aphids Cumulative Young Heat Units (37,95) Born to 39 Females Per Female 0- 20 137 3.51 20- 40 184 4.72 40- 60 313 8.03 60- 80 417 10.69 80-100 513 13.15 100-120 623 15.97 120-140 722 18.51 140-160 840 21.54 160-180 943 24.18 180-200 1035 26.54 200-220 1129 28.95 220-240 1217 31.21 240-260 1307 33.51 260-280 1410 36.15 280-300 1503 38.54 300-320 1624 41.64 320-340 1713 43.92 340-360 1822 46.72 360-380 1904 48.82 380-400 1974 50.62 400-420 2056 52.72 420-440 2093 53.67 440-460 2133 54.69 460-480 2194 56.26 480-500 2236 57.33 500-520 2248 57.64 520-540 2275 58.33 540-560 2304' 59.08 560-580 2313 59.31 580-600 2326 59.64 600-620 2343 60.08 620-640 2346 60.15 640-660 2352 60.31 660-680 2357 60.44 680-700 2361 60.54 700-720 2366 60.67 720-740 2366 60.67 740-760 2367 60.69 760-780 2367 60.69 .780-800 2367 60.69 800-820 2368 60.72 lData based on cumulative fecundity of 39 females (Matheson 1919) calculated on a heat unit scale. 34 D. APPLE APHID SIMULATION 1. Simulation Structure Figure 5 presents a black box model of the single- terminal aphid simulation. Aphids were classified into 3 categories: (1) the number of lSt + an instar nymphs = AP(1), (2) the number of 3rd + 4th instars = AP(2) and the number of adults = AP(3) (both apterae and alatae). Future aphid numbers were predicted on the basis of heat units accumulated. Figure 6 depicts a flowchart of the simulation. Nymphs and.adults were aged and fecundity computed using a time step of 5 heat units with output printed every 8 day. The following 2 sections describe the nymph and adult developmental models respectively. 2. Nymph Developmental Model Nymph development was modeled using a distributed delay developmental model (Manetsch 1976, see conceptual diagram in Figure 7). The advantage of using the distri- buted delay over a discrete delay (such as the one used for adult development - see Figure 9) is that variability in nymph maturation times was introduced. The distributed delay is characterized by two parameters: (1) DEL - the mean delay time in heat units (set to 272.19, see Section III-C-Z) and (2) K - the number of substages in the delay process. The variability in nymph maturation times is related to K and DEL by the equation Sx2 = DELZ/K (where Sx2 is the 35 FIGURE 5. Black Box Model of Aphid Simulation Time Initial Month, Interval Day (DAYS) (IMNTH, IDAY) Initial Aphid Single Terminal Final Aphid Numbers Numbers-AP(1), Aphid Simulation AP(1),AP(2),AP(3) AP(2) ,AP(3) Daily Maximum, Minimum Temperatures MAX (I,J), MIN (I,J) Explanation 2: Variables: AP(1) - Number of 1st, 2nd instar apple aphids AP(2) - Number of 3rd, 4th instar apple aphids AP(3) - Number of adult aphids DAYS - Time interval in half day units IMNTH - Month simulation starts on (6-8 i.e. June-August) IDAY - Day simulation starts on (1-31) MAX (I,J) - Maximum temperature on month a I, day = J MIN (I,J) - Minimum temperature on month ll L; I, day 36 FIGURE 6. Flowchart of Aphid Simulation 7 READ INITIAL NUMBER OF APHIDS, STARTING TIME, DURATION OF SIMULATION ‘ 1 I T=T+ . 5 l.— - (nus) AD MAXIMUM, MINIMUM TEMPERATURES] FOR THIS HALF DAY , {r _ [COMPUTE HEAT UNITS] 1 DFACT TER EECUNDITN TER FECUNDITY CCORDING TO .q1COMPUTE FECUNDITY CCORDING TO REE NUTRIENT (ADD BELOW) . HID DENSITY e I IAGE SURVIVING ADULTSI L [AGE SURVIVING NYMPHfl ADD YOUNG BORN ’ .(COMPUTE ABOVE — OUTPUT APHIDSI PRESENT , IJ 37 FIGURE 7. Conceptual Diagram of Nymph Distributed Delay Developmental Model (After Manetsch 1976) M M M XNY(1) RNY(l)—O °°'—9RNY(19)-¢--ORNY(20) DEL = 272.19 K = 20 PLR = .00038 DT = 5 RNY(i,T+DT) = RNY(i,T) + A *(R(i-1,T) - B*R(i,T)) A = K*DT/DEL B = 1 + PLR*DEL/K AN(i) = RNY(i)*DEL/K 6 AP(1) =JEIAN(i) i=1 20 AP(2) =2:IAN(i) i=7 Explanation of Variables and Parameters: XNY(1) - input rate variable into nymph stage XNY(Z) - output rate variable out of nymph stage = RNY(20) RNY(i) - array Of K intermediate rates, the outputs of the K substages Of the delay process AN(i) - storage in the ith substage M - mortality (set by PLR) DEL - mean delay for nymph development (in heat units) K - number of substages in the delay process PLR - proportional loss rate (PLR = .00038 results in average mortality Of 10% over the nymph stage) T - time expressed in heat units DT - time increment in heat units AP(1) - total first and second instar aphids AP(2) - total third and fourth instar aphids 38 \ square of the standard deviation). Using the data Of Section III-C-Z, K was set to 20 (K = 272.192/63.982 = 18.10; each instar was initially assumed to be Of equal duration: K was set to 20 so that each instar was repre- sented by 5 substages). Figure 8 compares developmental times for the literature data from Table 5 with the output Of the distributed delay model using the above parameters. NO literature data was found on nymph mortality rates. Nymph mortality in the present simulation was set to 10% distributed evenly over the nymph developmental period. A time step Of heat units was chosen for the aphid simulation (nymph and adult development and fecundity were updated every 5 heat units). This time step was large enough to prevent excessive computer costs while small enough to avoid numerical instability (the distributed delay fails to conserve flow if DT 3 75!- - < :2 . 5| —- Model Output 050* Literature Data : From Table 7 I 2 Ill 2 251- In a. O J FIGURE 11. 44 Aphid Fecundity Cumulative fecundity per female for 39 females from Table 7 is compared with output of the discrete delay simulation model with FEC(i) as given in Table 8. i 42‘ CUMULATIVE YOUNG/ FEMALE AA A. A‘AAAAAA ——- Model Output Literature Data _ From Table 7 L HEAT UNITS [37, 95] 45 inside an oversized sleeve cage (see Section VIIro—Z) for the dates of 7/14 to 9/03. A comparison of temperatures for these dates inside the sleeve cage versus the normal hygrothermograph records indicated that daily maximum and minimum temperatures inside the sleeves were elevated by an average of 2.56 and .29°F. respectively (see Section VII-C-Z). Thus sleeve cage simulations for dates on which sleeve cage temperature records were not available (6/Ol to 7/13) were driven by the normal Graham Station temperature records with 3 and 0 degrees added to maximum and minimum daily temperatures respectively. The output of the simulation model as described to present agreed only fairly well with sleeve cage data. Three main areas of disagreement were as follows: (1) Although the total number of aphids predicted was fairly accurate, the numbers of l8t and 2nd instar nymphs (AP(1)) was too high while the number of 3rd and 4th instar nymphs (AP(2)) was too low. (2) While the number of aphids predicted at low densities was fairly accurate, the number pre- dicted at high aphid densities was too high. (3) Prediction early in the season was somewhat low. As the season progressed prediction was increasingly high. The disagreement of simulation output with sleeve cage data was not surprising in view of the many simplistic assumptions made in model construction. The following 3 46 sections describe modifications to the basic model made in order to more accurately simulate factors influencing aphid population dynamics. A major objective of this simulation (and modifications) was to maintain biological realism. a. Relative Duration of Nymphal Instars To this point, nymph development was modeled as con- sisting of 20 equally spaced substages (K = 20) with each of the four instars represented by S successive substages (see Section III-DeZL This assumption was based on Baker and Turner's (1916) statement that for summer generations of apterous forms of the apple aphid (reared at Vienna, VA) the average duration of the nymphal instar was 7—8 days, the time being equally divided between the four stages. De- velopment of alates was observed to be similar except that two extra days were spent in the fourth instar. In order to mimic sleeve cage data, instars were reas- lSt 2nd signed as follows: and instars - substages 1-6; 3rd and 4th instars - substages 7-20. Note that as far as aphid development is concerned assignment of instars is unimportant. b. Effect of Aphid Density Evidence exists (Way 1973) for an optimum colony size‘ in aphid populations. Small aggregations presumably benefit because group feeding may improve the nutritional status of the plant at the feeding site. As colony size increases beyond a relatively small optimum level, the multiplication rate of the colony dramatically decreases. 47 Aphid caging studies from which model parameters were derived (see Section III—C-2,3) were performed under low aphid density conditions (individual aphids were confined on separate apple terminals). Thus developmental and fecundity parameters were assumed to be close to optimal levels. Table 10 lists the adjustment for aphid density made in the aphid simulation. Aphid fecundity was reduced by the parameter DFACT (Qensity Eéggor) as the aphid density rose above 100 aphids/terminal. No adjuStment in aphid developmental times or mortality rates was made in relation to density. c. Effect of Tree Nutrient Status Very little usable data exists on the relationship between tree nutrient status and aphid population dynamics.. In arriving at a submodel of the effect of tree nutrient status, several literature data sets were utilized quali- tatively to derive the form of the effect. Baker and Turner (1916) measured apterae fecundity at Vienna, VA of aphids reproducing before July 6 (2617 HU using a tree developmental threshold of 41°F. - Ashcroft et al. 1977) at 55.4 young/ female and for aphids reproducing July 6 - Sept. 10 (2617- 4647 HU) at 30.9 young/female (a reduction of 56%). Jokinen (1980) measured the pattern of apple leaf primordia decline over the season at Graham Station for 1977 (for trees in similar condition as those used for sleeve cages in the present study). He noted a very rapid decline starting at approximately 1100 HU and continuing to approx- 48 TABLE 10. Simulated Effect of Aphid Density and Tree Nutrient Status on Aphid Fecundity FECUNDITY EQUATION: APHIDS BORN = BORN * DFACT * TFACT where BORN = # aphids born in absence of density and nutritional factors APHID DE SITY = APTOT Qgégg 0 - 100 1.0 100 - 1000 1.0 - .75 * (LOGlo(APTOT) - 2.0) > 1000 .25 9333 Heat Units (41)2 w 6/1 - 7/4 748.8 - 1500 1.33 7/5 - 7/20 1500 - 2000 .9 7/21 - 8/6 2000 - 2500 .6 8/7 - 8/24 2500 - 3000 .5 8/25 - 8/31 3000 - 3209.7 .4 1Total number of aphids on the terminal. 2Tree heat units above a threshold of 41°F. calculated for Graham Station 1980 using Subroutine DEGD. 3Fecundity data calculated from Table 7 was for females fecund 6/4-8/30. Thus fecundity factor during period of optimal tree nutrient status (6/1-7/4) was elevated above unity. 49 imately 2200 EU (Figure 2C in his paper). He also noted that aphids are observed to distribute themselves in close association with active plant growing sites (Kennedy et al. 1950, Kennedy 1958). I Table 10 lists the adjustment made to aphid fecundity in response to changing tree nutrient status through the season (parameter TFACT-gree Egggor; again no adjustments were made to developmental or survivorship parameters). Heat units listed for various dates are for Graham Station 1980 (using a tree developmental threshold of 41°F.). Early in the season (6/1—7/4), nutrient availability was assumed to be at optimum levels and TFACT was set to 1.3 (greater than unity since model fecundity data was derived from aphids reared June 1 - August 31, see Section III-C). TFACT was reduced as shown in Table 10 as the season progressed. 5. Simulation Results Table 11 lists sleeve cage data and the results of sleeve cage simulations. Simulation output was classified as accurate if predicted population levels were within i l/3 of actual counts (see Table 12 footnote for the equation used). Table 12 summarizes the accuracy of the simulation. Total aphid pOpulation levels were classified as accurate in 19 of the simulations, high in 10 and low in the remaining 5. Figure 12 graphically presents the data of Tables 11 and 12. 50 TABLE 11. Sleeve Cage and Simulation Data -for Graham Station 1980 Sleeve I & II III & IV Cage Instars Instars Adults Total Aphids Number Dates AP(1) AP(2) AP(3) APTOTZ 1 6/16 2:00 131 34 31 196 6/24 4:30 399 384 81 864 Simulation 328.3A 441.2A 89.0A 858.5A 2 6/16 2:00 6 4 15 25 6/24 5:00 135 147 9 291 Simulation 105.2A 179.2A 15.7H 300.1A 3 6/16 2:00 2 0 V 1 3 6/24 5:00 8 l6 8 32 Simulation 10.0A 11.6A 12.6H 22.9A 4 6/16 2:00 3 l 1 5 6/24 5:00 25 35 3 63 Simulation 24.4A 21.8L 2.5A 48.6A 5 6/16 2:00 0 0 3 3 6/24 5:30 18 19 3 40 Simulation 17.1A 31.0H 2.0L 50.2A 6 7/2 1:00 175 148 26 349 7/6 2:15 306 327 102 735 Simulation 372.9H 347.2A 102.4A 822.4A 7 7/2 1:00 33 29 6 68 7/6 2:30 80 61 19 160 Simulation 150.0H 92.3H 20.7A 263.0H 8 7/2 1:00 67 84 13 164 7/6 3:00 124 247 35 406 Simulation 289.2H 195.2A 56.8H 541.3H 9 7/2 2:00 147 197 17 361 7/6 3:30 208 324 66 598 Simulation 426.7H 351.2A 123.9H 901.7H 1Sleeve cages were placed around aphid infested ter- minals on the first date after removing all natural enemies. On the second date, sleeve cages were removed and aphid population counted. Simulation output rounded to one decimal place. AP(1) + AP(2) + AP(3) may not add up to APTOT. 3Results of aphid simulation initialized with aphid numbers from first date. Model results were compared with observed population levels and classified as high (H), accurate (A) or low (L) - see Table 12. Thus 51 TABLE 11. (cont.) Sleeve I & II III & IV Cage Instars Instars Adults Total Aphids Number Dates AP(1) AP(2) AP(3) APTOT 10 7/2 2:30 1 0 1 2 7/6 .3:30 4 10 0 14 Simulation 5.7H 4.2L 0.7H 10.6A 11 7/2 2:30 175 295 47 517 7/6 3:30 231 617 160 1008 Simulation 523.9H 465.4L 200.5H 1189.8H 12 7/2 3:00 51 71 12 134 7/6 4:00 354 159 38 551 Simulation 265.9H 169.2A 48.7H 483.8A 13 7/2 4:00 86 119 21 226 7/6 5:30. 263 267 72 602 Simulation 354.0H 254.4A 82.3A 690.7A 14 7/2 4:30 80 48 13 141 7/6 5:30 152 173 13 338 Simulation 209.6H 168.1A 36.4H 414.1H 15 7/14 1:00 93 80 13 186 7/19 4:00 630 343 80 1053 Simulation 319.7L 382.6A 96.4A 798.7A 16 7/16 3:00 25 31 2 58 7/21 4:00 142 126 22 290 Simulation 162.3A 142.7A 28.8H 333.9A 17 7/16 3:00 55 60 21 136 7/21 4:00 253 301 48 602 Simulation 251.6A 292.1A 66.9H 610.6A 18 7/16 3:00 67 30 6 103 7/21 4:00 61 123 40 224 Simulation 162.0H 180.7H 34.3A 377.0H 19 7/16 4:00 39 57 3 99 7/21 4:30 297 308 39 644 Simulation 235.3A 223.1L 51.9H 510.0A 20 7/16 4:00 27 15 4 46 7/21 4:30 139 117 21 277 Simulation 105.1A 100.9A 17.2A 223.1A 21 7/16 4:00 59 39 25 123 7/21 4:30 229 342 46 617 Simulation 205.5A' 263.6A 52.5A 521.6A 52 TABLE 11. (cont.) Sleeve I & II III & IV Cage Instars Instars Adults Total Aphids Number Dates AP(1) AP(2) AP(3) APTOT 22 7/16 4:30 121 67 15 203 7/21 5:00 250 508 93 851 Simulation 258.3A 318.3L 74.9A 651.5A 23 7/28 3:00 19 37 8 64 7/31 1:00 104 56 16 176 Simulation 106.3A 46.5L 23.3H 176.2A 24 7/28 3:30 7 5 4 16 7/31 1:30 15 9 5 29 Simulation 25.0H 12.1H 5.5H 42.6H 25 7/28 3:30 13 23 8 44 7/31 1:30 52 35 9 96 Simulation 79.7H 32.1A 17.0H 128.7H 26 7/28 3:45 21 16 5 42 7/31 1:30 37 25 6 68 Simulation 54.9H 32.0H 11.3H 98.2H 27 7/28 4:00 18 31 2 51 7/31 1:30 52 47 7 106 Simulation 79.2H 37.4L 15.7H 132.3H 28 7/28 4:00 84 93 16 193 7/31 2:00 180 177 45 402 Simulation 185.9A 137.9L 55.3H 379.1A 29 8/11 11:30 5 9 4 18 8/14 2:00 31 24 6 61 Simulation 26.9A 11.7L 7.1H 45.8L 30 8/11 11:15 9 9 l 19 8/14 2:00 12 16 5 33 Simulation 19.4 13.5 4.7 37.7 8/18 11:30 43 20 5 68 Simulation 46.1A 36.0H 9.9H 92.0H 31 8/11 1:30 20 54 7 81 8/14 2:00 60 86 22 168 Simulation 106.2. 53.7 29.0 188.9 8/18 11:30 285 182 40 507 Simulation 170.3L 170.0A 54.1H 394.4A 32 8/11 11:30 0 7 0 7 8/14 2:00 2 5 2 9 Simulation 12.3 4.4 3.0 19.7 8/18 11:30 18 16 6 40 Simulation 31.0H 20.4H 6.1A 57.5H 53 TABLE 11. (cont.) Sleeve I & II III & IV Cage Instars Instars Adults Total Aphids Number Dates AP(1) AP(2) AP(3) APTOT 33 8/11 11:30 14 34 8 56 8/14 2:30 59 60 17 136 Simulation 81.2 36.7 21.2 139.2 8/18 11:30 172 114 45 331 Simulation 129.5A 128.9A 36.3A 294.6A 34 8/11 12:00 4 4 2 10 8/14 3:00 14 9 2 25 Simulation 12.7 6.8 3.4 22.9 8/18 11:30 39 26 5 70 Simulation 23.8L 21.6A 5.3A 50.6A 54 TABLE 12. Comparison of Simulation Model Output and Sleeve Cage Data Accuracy2 I & II Instars III & IV Instars Adults Total Category AP(1) AP(2) AP(3) Aphids H 15 7 20 12 L 3 9 1 l A 16 18 13 21 l34 sleeve cages were simulated. Results list the number of sleeve cage simulations falling into each accuracy category. 211 (High) - (PF-AF)/(AF-AI) >1/3 A (Accurate) - [AF-PFI/(AF-AI)(l/3 L (Low) - (AF-PF)/(AF-AI) >1/3 ‘ _ where AF final sleeve cage populations PF final simulation prediction AI initial sleeve cage population 55 § § (lOldV) BZIS NOLLV‘IndOd OIHdV . mmmaazugo m>mm o.» mm ow , 1a.. _ Alma m o E E ES 8 . < 63¢ mmam .NH mmome IV. CECIDOMYIID EXPERIMENTS A. INTRODUCTION 1. Taxonomy and WOrldwide Use in Biological Control Several recent taxonomic studies (Harris 1966,.1973, Nijveldt 1969, Gagne 1971, 1973) have helped to clarify classification of aphidophagous Cecidomyiidae. Harris (1973) reports that there are 5 species which feed exclusively on aphids and are the only Cecidomyiidae definitely known to do so. Aphidoletes aphidimyza (Rondani) is by far the most common and widespead of these species with a host range of at least 61 aphid species. A. urticariae (Kieffer) is behaviorally and morphologically quite similar to A. aphidimyza but appears to be less common with perhaps a more northerly distribution. Both A. abietis (Kieffer) and A. thompsoni M3hn are fairly uncommon and are reported feeding only on adelgids. Monobremia subterranea (Kieffer) is a rare species reported to feed on root aphids. Within the past decade, a great deal of interest has been shown worldwide in the use of A. aphidimyza. Table 13 presents a partial list (only one reference is included for each country or state) of research reports dealing with the possible use of this species in biological control programs for aphids in glasshouses and on field crops and fruit trees. Within Finland, this species has been used commercially since 1978 for glasshouse control of aphids on vegetables and ornamental plants (Markkula and Tiittanen 1980). 56 57 TABLE 13. Worldwide Reports of the Use of A. aphidimyza in Biological Control Aphid Control in Glasshouses USSR West Germany Finland Denmark Czechoslovakia Aphid Control on Field Crops Italy England Egypt Netherlands Rumania Chile USSR Aphid Control on Fruit Trees Israel France Bulgaria Lebanon U.S. Poland Reference Asyakin 1973 El Titi 1974a Markkula and Tiittanen 1977 Hansen 1980 Havelka 1980b Roberti 1946 Dunn 1949 Azab et al. 1965a Nijveldt 1969 Constantinescu 1972 Apablaza and Tiska 1973 Narjikulov and Umarov 1975 Nijveldt 1957 Coutin 1974 Pelov 1977 Talhouk 1977 Adams and Prokopy 1980(Mass.), Jokinen 1980(MI). Olszak 1979 58 2. Life Cycle The biology of A. aphidimyza has been reviewed by several authors (Azab et al. 1965b, Harris 1973, Markkula et al. 1979, Adams and Prokopy 1980). The following account includes observations from laboratory rearing cages as described in Section II-A-Z (entrained to artificial light on 4am-8pm). Figure 13 presents a diagram of the cecidomyiid life cycle. Adult midges emerge from pupal sites in the soil with peak emergence occurring in late afternoon hours (4-8pm). Adults are nocturnal and hide during daylight hours in dim protected areas. During the first night of adult life mating occurs and very few eggs are laid. Females live up to 16 days in captivity and lay ca. 150 eggs (see Section IV-C-4). Males do not live as long as females (a maximum of 9 nights was observed at 23.330C.). Adults appear to feed on aphid honeydew and its presence increases both longevity and fertility (Wilbert 1977, Kuo 1977). The species is monogenic (Sell 1976) with males apparently having no effect on the sex of their progeny. The ratio of arrheno- genic to thelygenic females as well as the ratio of females to males appears to be close to 1:1 (Sell 1976, Linskii 1977). The majority of oviposition occurs at late evening hours (6-12pm) under laboratory conditions. Eggs are laid singly or in clusters of up to 40 and are sometimes laid directly on the aphids. Females are able to locate aphid colonies even at quite low aphid densities (E1 Titi 1974b, see Section IV-C-S) and appear to lay eggs only in close 59 FIGURE 13. Cecidomyiid Life Cycle ‘ Ad 11 ‘ , Overwlnterlng) Emgrgence Puple ln Sell” From Sell Summer Pupat 10!! In Sell ’1 s ' t I ti ‘1 I “Q 1. . ] Adult ’ searching 81 Oviposition - 60. proximity to aphids (El Titi 1973). Increasing levels of aphids and honeydew serve as ”releasing mechanisms” which promote increased oviposition (E1 Titi 1974b). Eggs are .3 mm. long, orange, and are barely visible with the naked eye. Hatching occurs in 2-3 days (see Section IV-C-l) and it is generally agreed that there are 3 larval instars although some reports have indicated 4 (Azab et al. 1965b, El-Gayer 1976). First instar larvae locate aphid prey from short distances, probably using a sense of smell (Wilbert 1973,1974). In addition females appear to orient their eggs toward nearby aphids (Wilbert 1972). Recently hatched larvae lived an average of 5.3 hours without food and traveled an average of 49 mm. before dying (Wilbert 1972). Larvae usually attack their prey by piercing a leg joint with their mandibles (Solinas 1968) and paralyze the aphid through the injection of a salivary enzyme (Mayr 1975). The enzyme also serves to liquify the gut contents which are withdrawn after a period of time. Handling times vary from 30-60 minutes, decreasing with increasing aphid density (Azab et al. 1965b). The shrivelled bodies_ of the aphids generally remain attached to the plant, indicating that the aphids were overcome before their stylets were retracted from the plant tissues (Harris 1973). Reports of the number of aphids killed by cecidomyiid larvae vary greatly with the aphid species and experimental conditions. Uygun (1971) reports a minimum requirement of 61 7 Myzus persicae (Sulzer) for larval develOpment. The number of aphids killed during larval development greatly influences fecundity levels of adult females (Uygun 1971). Mature larvae drop into the soil to construct small silk coccoons within the tOp 3 cm. (Roberti 1946). Occasionally coccoons may be spun on plant leaves within a cluster of dead aphids. Cecidomyiids overwinter as pupae in the soil with emergence occurring during late May and early June (see Section IV-D-l). 62 B. OBJECTIVES AND METHODOLOGY The objectives of this section were to gather basic experimental data on several diverse features of cecido- myiid biology as they affect aphid predation. Section C presents laboratory experiments on egg and larval develop- mental periods, larval functional response and adult female search and oviposition. Section D lists field experiments on adult emergence from overwintering sites, the use of aphid infested trap plants in monitoring adult cecidomyiids and a comparison of direct terminal samples with trap plant samples in a commercial apple orchard. Section V presents the cecidomyiid computer simulation which was constructed. utilizing much of the biological data gathered in Section IV. 63 C. LABORATORY EXPERIMENTS 1. Cecidomyiid Egg Development Uygun (1971) calculated mean egg hatch for a laboratory colony from GSttingen, West Germany to be 2.5 days at 21°C. Havelka (1980a) measured constant temperature egg develOpment in a laboratory population of A. aphidimyza collected originally form Leningrad, USSR (see Table 14). This data is analyzed and compared to experimental data in Table 17. In order to compare egg development for a Michigan cecidomyiid colony with the above data, jimsonweed plants (these plants were chosen because they were easier to observe under a microscope without disturbing the eggs) infested with green peach aphids were left for 2 hours in a laboratory cecidomyiid colony containing a large adult population. The plants were removed, checked for the absence of adults and a map was made of all eggs deposited. The plants were held at constant temperatures and were checked at approximately 2 hour intervals over the duration of egg hatch (preliminary experiments had indicated the interval for expected first hatch). During observations each plant was removed from the environmental chamber for approximately 5 minutes (with room temperature 23.3-25.l°C.). Cumulative percent hatch versus time (for both experimental and literature data) was fit to a cumulative normal distribution using the MSU Entomology department computer program BNPGPROBIT which estimated time and standard deviation to 50% hatch. Table 15 lists experimental data for egg hatch at 5 64 TABLE 14. Literature Data on Cecidomyiid Egg Hatch1 Probit Equation Mean y = percent Days Laboratory hatch in to Tsmperature Days Post Percent probits 50% Standard ( C.) Oviposition Hatch x = days Hatch Deviation 15 4.75 23.1 y=3.2940x 4.9753 .3036 -11.3886 5.00 53.5 5.13 68.1 5.25 82.4 20 2.37 6.2 y=7.9581x 2.5600 .1257 -15.3726 2.50 33.1 2.75 93.3 25 1.58 28.2 y=7.9027x 1.6543 .1265 -8.0731 1.83 90.7 1.87 96.1 1.92 100.02 1Data from Havelka (1980a) analyzed by this author using BNPGPROBIT. 2This data point deleted in analysis. 65 TABLE 15. Experimental Cecidomyiid Egg Hatch Data (see Table 16 for experimental conditions of experiments A-D) Hours Post Percent Hours Post Percent Oviposition Hatch Oviposition Hatch EXP.A 208.50 1.5 EXP.C 48.25 27.17 225.75 16.7 50.50 62.60 227.25 22.7 52.25 84.25 229.75 29.5 231.25 36.4 232.75 43.9 EXP.D 34.25 48.80 234.25 47.0 35.75 60.24. 257.00 90.9 37.75 81.33 258.50 91.7 40.50 90.36 260.00 92.4 43.75 96.39 274.00 94.7 49.00 96.99 276.00 97.7 279.00 99.2 EXP.B 73.75 18.18 76.25 36.36 77.75 57.95 79.00 64.77 80.50 73.86 82.00 77.27 83.50 80.68 66 constant temperatures with the experimental conditions and probit analysis listed in Table 16. The inverse of estimated days to 50% hatch versus temperature is plotted in Figure 14 for both literature and experimental data (using the x- intercept method of Arnold 1959). Linear regression was performed on the data giving a theoretical developmental threshold (x-intercept) of 10.48°C. (51°F.) and a develop- mental period (inverse of the slope) of 25.49 heat units (45.88 °F.-HU). Table 17 lists heat units and standard deviations above the 10.48°C. base (HU10.48) calculated for each data point. More data is needed to accurately determine egg mortality rates. Mortality at intermediate temperatures appears to be in the range of 10-15% with higher levels indicated at either of the two extremes (Table 16). 2. Larval Development With Excess Food Some disagreement has existed over the number of larval instars of A. aphidimyza. Azab et al. (1965b) reported that "larval stages...are very difficult to separate" and that "it seems...there are” four instars. El-Gayer (1976) and Adams (1977) also assume 4 larval instars. Roberti (1946) states that there are 3 larval instars and Harris (1973) and Markkula and Tiittanen (1977) agree that this is most likely the case. My own observations and those of Warner (unpublished) indicate that there are 3 larval instars. Several authors have measured larval developmental 67 . h.Hm 1 1 1 mm.o vm vmloe he 1w.om ha.Hm h.mm moan. «mmm.a mamm.+xmvma.n> vm.mm mma mmlmm om 1¢.wm ha.mm H.m~ mmoa. mmho.m mmno.ma1xmmov.u> mh.mm mmN omlwo me 1m.m~ ha.vN h.mH mmmm. eov~.m mmom.m1xmmma.u> om.mm mm mm1mh mm 1m.ma m>.ba H.mH . vmah. mmmm.m mmmo.m1xmmmo.u> mm.~m cam OOHIOh Hm 1m.~a mm.ma Anamov nouns mom musoznx noun: ou>umnno mmcmm cums uwcmm sum: :0wumfi>mo on when «muwnoum cw usmo mmvm mo vamufioflEdm A.Uou74MEmB pnmocmum noun: unmoummum lumm HmnEsz u>wumHum ecu Hom.mwmaamc¢ awnoum can mcowuflocoo anacoEHummxm .ma wands coaumsvm ufinoum ucuEwuomxm noun: mmm owfiheooflomo umnsmao HmucmE locuw>cm umnsmso Houses 1coufl>cm cam Boom ca mmmo Hmnamno amazes 1couw>sm umnsmso Housofi Iconfl>sm < mcoflu Hausa 1Hocoo lummxm HmucmE lummxm 68 FIGURE 14. Cecidomyiid Egg Developmental Rate -7' A Uygun 1971 0 Havelka 1980 ‘ I O U I EXperlmental Data 75 in DEVELOPMENTAL RATE [DAYS TO 50% HATCH)" a l Y' '.41120+ . 03923X .2 Hz : .9772 I j .1. q o ' . .1- l 4 0 1O 15 2O 25 30 TEMP. l°CJ 69 TABLE 17. Heat Units and Standard Deviations for Literature and Experimental Data on Cecidomyiid Egg Hatch Mean Estimated Standard HU 10.48°C. Standard Temp. 50% Hatch Deviation (degrei- Deviation2 Source (0C.) (Days) (Days) days) (Heat Uhits) Uygun 1971 21 2.5 — 26.2988 - Havelka 1980a 15 4.9753 .3036 22.4860 1.3720 20 2.5600- .1257 24.3699 1.1961 25 1.6543 .1265 24.0189 1.8373 Experimental 13.89 9.9966 .7124 34.0736 2.4282 Data 17.78 3.2404 .2266 23.6472 1.6533 24.17 2.0725 .1033 28.3653 1.4131 29.17 1.3584 .3103 25.3838 ‘5.7125 Means 26.0805 2.2304 1HUI .48 = (Mean Temp. - 10.48) x (days to estimated 50% hatch9. 2Standard Deviation (Heat Units) = (Mean Temp. - 10.48) x (Standard Deviation in days). 70 rates of cecidomyiids provided with excess food (see Table 18) and their data are compared with experimental data in Figure 15. . The objectives of this section were to compare larval developmental rates (with excess food) of a Michigan cecidomyiid p0pulation with the above data. Cecidomyiid eggs which had been collected over a .4 hour interval were held at room temperature (approx. 25°C.) and were checked once per hour during the duration of egg hatch. Newly hatched larvae (which had not yet fed on any aphids) were transferred to a pea aphid infested fava bean stem using a camel hair brush. Plants were held in environmental chambers (or at room temperature) and were checked every 2-4 hours for completion of larval development (this in- volved removal from the environmental chamber to room temperature for approximately 5 minutes; the larval stage was ”completed" when larvae dropped from the aphid infested leaf onto a petri dish containing moist sand for pupation). The data for these experiments are presented in Tables 19 and 20. Results are compared with literature data in Figure 15. Linear regression was fit to the 3 main data sets (Uygun 1971, Havelka 1980a, Experimental Data) with theoretical developmental threshold of 4.80, 5.27, and 8.10°C indicated respectively. The data displayed in Figure 15 is for cecidomyiid populations collected from widely separated geographical regions reared using different experimental techniques and 71 magma .BHmommwmzm Hospsm was» >9 mausmocummosw omuaamcm mm3.AmommHv oxam>mm no open used News. eeaa.m ede~.mnxeeee.~u» mm Hmmm.a mamm.w mhm~.1xmmmh.n> om seam.a emem.ea meee.auxmeee.u> ma 1 o.m 1 pm 1 m.m 1 am 1 h.@ 1 ma 1 mm.m 1 m.n~ Ammmov Amweov mmdoux 4muwnonm A.Uov coaumw>mn .>ma mom cw .>oo mu» .9509 oumocmum ooumsaumm cowumsum uwnoum mmmum>¢ .uxosm unwow> musowoz ..moom mmnmm mwsm< lumuaeme mmoflmumm was»: .mmmm unnecsm mfinm¢ mmmD .pmnmswsmq mamEHmw ummz .cmmcfluuww ummmm .meo muflommm mmum osnma omma meam>mm Huma com»: mead .Hm um Dana cwmuum oaassoeaomo mo :wmfluo QOHQOW ”UGO omwammsm Doom mmmoxm nuwz usufimo~u>mo Hm>umq so mama musumuoqu .mH mqmda TABLE 19. 72 Experimental Larval Developmental Data (Excess Food) Experiment Experiment Experiment Experiment Experiment Hours Post Hatch A 82.50 90.50 94.25 98.75 102.50 113.50 B 56.00 63.00 66.00 70.00 75.75 C 175.75 186.00 198.00 209.75 221.50 D 81.00 85.00 89.00 94.25 100.75 114.00 E 56.00 * 60.00 64.00 67.50 71.75 76.00 91.25 Percent Develop. 3.77 54.72 73.58 77.36 81.13 96.23 4.17 50.00 62.50 70.83 83.33 11.76 29.41 62.75 72.55 96.08 6.98 18.60 46.51 65.12 72.09 97.67 2.20 13.19 39.56 63.74 78.02 85.71 98.90 73 eem~.e eemm.me mmmu0>m smasmao IIIIII. 1IIIIII. m.mm amuscho mmoo.n mmam.om vmmm. moem.~ mmmm.m1x~haa.u> Hm 1h.m~ Hm.mm 1Hw>cm m cam Boom . m.m~ ca Hema.h mmov.oo made. mamm.m mmq~.e1x~mmo.u> me 1m.m~ a~.mm mmmu o Hmanno m.>H Hmuccho woem.m mmmm.wm nmmm. ~m~a.m mmom.o1xoamo.uw. Hm 1o.ma mm.wH 1HH>sm o umanno w.vm Hmuccho omoa.m Hmha.mm mumm. mmm>.~ mHHv.mnxm>~H.u> em 1o.om hm.mm 1HH>cm m cam Boom H.5N ca vmea.h hmmm.mm home. mmom.m mmma.e1xommo.u> mm 1m.mm ma.mm ummo d Aomv Amado AmNmov .>uo mom musosuxumuflnoum um>umq mmcmm smmz ucuBco ucmBfl nodumw>un Imuumuov :oHumw>mo ou mama a“ .>m© w u» mo A.oov.mBmB luw>cm lummxm pumocmum UOoH.mDm pumpcmum cmumBaumm coHumsvm panoum HmnBsz HmucmB awnmmxm ustmon>oa Hm>umq new mwmhamcd panoum paw mcofluflocou Hmucmbuwmxm .om Manda DEVELOPMENTAL RATE (DAYS To 50% DEV. l" .3F- 50 74 FIGURE 15. Maximal Larval Developmental Rate (Excess Food Supplied) U I V I V I ' Uygun 1971 . I . ' e 4 Havelka 1980 " Experimental Data 8 ' zoata Points Y=-.12398 +.01531x R2=.9768 « v = -.O7356 +.01534x R2=.9815 ,7 . q . j , . Y=-.O5213+.00989X 82 =.9999 r a 4.8 ~ 10 .15 20 25 30 5.3 a. TEMP l°c.l 75 aphid prey species. Thus the disagreement in larval devel- Opment rates is not surprising. Probably the most important Variable in this type of experiment (given differences in the cecidomyiid populations collected from different areas) is the availability of the prey species to the cecidomyiids. In this author's experiment an excess number of pea aphids (which are a comparatively large species of aphid) were provided,thus allowing for a maximal rate of development (the cecidomyiids appeared to have no problem attacking the large pea aphids; this assumes no significant nutritional differences between the aphid species). For the Michigan cecidomyiid population, a developmental threshold of 8.10°C. (46.580F.) and developmental period of 65.54 (117.57 °F.-HU) heat units Was indicated. 3. Larval Functional Response Reports of the number of aphids killed by cecidomyiid larvae over their developmental period have ranged from 5.2 M1325 persicae reported by Nijveldt (1966) to 60-80 ApAis gossypii reported by Roberti (1946). The objective of this section was to estimate the number of A. pgmi_that would be killed under different aphid densities and temperature conditions. Green peach aphids (A. persicae) reared on jimsonweed (see Section II-A-l) were used as apple aphid substitutes for the following laboratory experiments. The data in Table 35 in Section VII-A indicate that these two species are quite similar in size although green peach aphids have 5 immature 76 instars whereas the apple aphid has 4. Young jimsonweed plants having trifoliet leaves with an average area of 9.9 cm.2 (measured using a Lambda Instruments Corp. LI-300 Portable Area Meter) were used in the experiments. Two of the leaves were trimmed from the plant shortly before the start of the experiment so that the experimental arena was confined to the 9.9 cm.2 area (aphids normally stayed on the underside of the leaf, cecidomyiids were not observed to search on the other side of the leaf or the stem). Shortly after hatch, a single cecidomyiid was transferred to the leaf arena. Since aphid levels did fluctuate somewhat (due to reproduction), the number of aphids was counted once - at a time which the larval developmental experiments (previous section) had indicated was 2/3 of the normal larval period. Previous experiments had in- dicated that the majority of aphids were killed by the 3rd larval stage (which was assumed to begin at approximately this time) and thus the number of aphids were counted at the 2/3 time interval instead of at the beginning of the experiment. Post experimental analysis indicated that 24.28% of the aphids were killed prior to the 2/3 time interval and that the number of aphids killed by the young instars showed little correlation with aphid density (see Figure 16). In order to include any dead aphids which fell off the leaf, a large petri dish rimmed with tanglefoot was placed be- low the leaf (a hole was cut for the stem and then taped up). very few dead aphids were found in the petri dish - confirming the observation that most aphids are killed before they can 77 remove their stylets from the leaf. HoweVer, dead aphids were observed to stick to the mature larvae and as many as 29 aphids were carried off the leaf as the cecidomyiids dropped to the petri dish to pupate. The total number of aphids killed (of each aphid life stage) was recorded at 3 overall mean temperatures of 16.79, 24.51 and 29.87°c. and is listed in Table 21. The total number nd rd of aphids killed by both the 2 and 3 instar larvae was first plotted separately for the 3 experimental temperatures. Since rd instar the data for the 3 temperatures appeared similar (for 3 larvae, data for the 3 temperatures fit the curve shown in Figure 17 with mean square relative errors of .101, .083 and .081 re- spectively), it was pooled in the following account. Uygun st (1971) has reported that 1 instar larvae kill only one aphid. Thus the number of aphids killed up to the 2/3 time interval nd instar larvae. This 2nd (minus 1) was attributed to the 2 instar functional response (aphids killed at the 2/3 time inter- val minus 1, versus aphids assumed to be present midway through the interval = alive at the 2/3 time interval plus 1/2 of those killed over that interval) is displayed in Figure 16. The line drawn is the relation used in the simulation model of Section V. As mentioned earlier, the number of aphids killed by the 2nd instars did not seem to be greatly affected by aphid density. The remaining number of aphids killed was attributed to the 3rd instars. Figure 17 presents this functional response data (aphids killed after the 2/3 time interval versus aphids assumed to be present midway through the 78 TABLE 21. Functional Response Data A. Overall Mean of l6.79°C.(Exp.l-3) Experiment 1: Mean Temperature l6.78°C. (Range 15.6-17.9); N = 7: Aphids Counted After 131.75 hours Appids Counted Aphids Killed Cecid. Number Alive Dead Total £_ AA AAA} £2. E. Ag. A; 2233; l 68 18 86 10 24 12 3 - 2 -, 51 2 24 ll 35 3 10 7 3 1 1 - 25 3 23 9 32 1 l4 6 4 - - l 26 4 9 ll 20 1 5 3 l l - - ll 5 36 7 43 2 6 6 4 4 l - 23 6 18 9 27 1 12 9 2 2 - - 26 7 18 15 33 2 10 8 5 4 2 - 31 Experiment 2: Mean Temperature 16.74°C.(Range 15.7-18.7); N = 6; Aphids Counted After 126.5 hours Aphids Counted Aphids Killed Cecid. Number Alive Dead Total £’ LE. _ll £!_ 2, ES. él.$2£21 l 138 14 152 2 30 6 5 3 l l 48 2 111 7 118 l 29 12 2 2 - - 46 3 22 7 29 2 7 1 - - l - ll 4 28 7 35 - 6 3 3 3 l - 16 5 23 4 ‘27 1 1 7 1 1 - 1 12 6 70 12 82 - 18 13 2 l - 2 36 Experiment 3: Mean Temperature 16.82°C.(Range 15.6-18.1); N = 10; Aphids Counted After 136.5 hours Aphids Counted Aphids Killed Number Alive Dead Total A II II ;y_ 2' Ag_ AA_Total 1 62 13 75 - 18 9 5 3 2 - 37 79 TABLE 21. (cont.) Experiment 3. (cont.) Aphids Counted Aphids Killed Cecid. Number Alive Dead Total 5 {5' III A!_ Z] 59. Al Total 2 12 11 23 - 11 4 2 1 1 - l9 3 182 4 186 - 15 ll - l l l 29 4 103 11 114 2 l4 9 2 1 l - 29 5 28 12 40 - 17 8 l l - l 28 6 140 9 149 - 13 20 6 2 - - 41 7 73 14 87 1 ll 14 9 3 l 4 39 8 93 7 100 - 18 9 5 l l l 35 9 35 7 42 - 12 ll 6 1 2 2 34 10 74 5 79 2 18 10 2 l l - 34 B. Overall Mean of 24.6l°C.(Exp. 4-5) Experiment 4: Mean Temperature 24.33°C.(Range 21.7-26.7) N = 26; Aphids Counted After 62.00 hours Aphids Counted Aphids Killed Cecid. - Number Alive Dead Total A ‘AE’ III 3!. V_ Ag. AA_Total 1 52 8 60 14 20 4 4 2 3 - 47 2 84 7 91 5 22 14 4 5 1 - 51 3 27 4 31 2 9 3 4 6 2 - 26 4 40 8 48 9 8 5 6 6 2 - 36 5 92 4 96 - 10 11 8 6 l - 36 6 73 6 79 10 15 8 1 ' 1 3 - 38 7 61 5 66 1 10 6 4 4 l - 26 8 95 7 102 12 18 8 6 4 2 - 50 9 56 6 62 2 7 3 7 4 1 - 24 80 TABLE 21. (cont.) Experiment 4.(cont.) Aphids Counted Aphids Killed Cecid. n_umber MMM 111123112. 39.21.12.221 10 115 9 124 3 12 15 10 l l - 42 11 31 7 38 2 13 8 3 - l - 27 12 152 8 160 3 14 13 7 7 1 - 45 13 49 7 56 3 9 10 8 4 2 - 36 14 125 8 133 8 21 10 4 3 1 - 47 15 46 6 52 6 7 4 5 3 - - 25 16 75 13 88 10 8 10 8 9 2 - 47 17 26 7 33 4 10 10 2 3 3 - 32 18 66 6 72 3 21 8 S 1 l - 39 19 19 6 25 2 3 6 5 4 - - 20 20 33 7 40 3 9 7 9 5 - 4 33 21 61 7 68 4 8 6 3 2 l - 24 22 219 7 226 - 19 13 2 1 1 - 36 23 85 4 89 - 18 10 6 4 3 - 41 24 42 8 50 5 8 9 4 2 l - 29 25 109 6 115 2 21 8 4 3 l - 39 26 14 6 20 2 5 5 4 3 ' - - 19 Experiment 5: Mean Temperature 25.12°C. (Range 23.3-26.4) N = 14; Aphids Counted After 66.5 hours Aphids Counted Aphids Killed Cecid. . Number Alive Dead Total A. A; III £2, V. 59. Al Total 1 94 9 103 15 13 16 5 4 4 - 57 2 ‘ 35 6 41 4 3 4 3 3 1 1 l9 3 109 7 116 16 24 5 1 - - - 46 81 TABLE 21. (cont.) Experiment 5.(cont.) Aphids Counted Aphids Killed Cecid. Number QLEXE Dead Total ‘3 ;5_ Ag_ ;y_ E. Ag_ él.22£§l 4 96 12- 108 20 25 9 l 2 - - 57 5 171 2 173 18 18 4 3 8 2 - 53 6 51 5 56 9 4 4 1 l 3 - 22 7 52 4 56 2 9 11 2 2 2 - 28 8 55 5 60 7 12 11 3 2 6 - 41 9 12 3 15 2 5 6 - l - - 14 10 61 5 66 9 20 7 5 3 6 - 50 11 360 4 364 1 15 19 3 2 - - 40 12 88 5 93 4 27 12 4 1 - - 48 13 185 8 193 2 29 16 4 2 2 l 56 14 282 10 292 2 19 15 6 5 1 - 48 0. Overall Mean of 29.87°c.(8§g.6-9) Experiment 6: Mean Temperature 29.620C.(Range 26.9-30.8) N = 9; Aphids Counted After 47.00 hours Aphids Counted Aphids Killed Cecid. Number Alive Dead Total 1’ A; III 1!, !_ AA, A; Total 1 56 14 70 - 12 13 4 2 l - 32 2 103 15 118 - 11 19 4 2 1 - 37 3 69 10 79 _ 1 9 12 4 4 - - 30 4 128 10 138 2 18 11 5 3 2 - 41 5 178 10 188 - 16 16 3 4 2 - 41 6 336 5 341 2 11 19 4 l l 1 39 7 58 15 73 - 14 16 5 4 2 - 41 82 TABLE 21. (cont.) Experiment 6.(cont.) Aphids Counted Aphids Killed Cecid. Number Alive Dead Total A A; III £2. !_ 59. AA_Total 8 . 41 15 56 l 18 14 5 l - - 39 9 68 9 77 - 10 5 5 5 4 - 29 Experiment 7: Mean Temperature 29.42°C.(Range 28.4-32.1) N = 5; Aphids Counted After 47.00 hours Aphids Counted Aphids Killed Cecid. Number Alive Dead Total A A; III 1!. V_ AQ| Al Total 1 193 7 200 1 18 17 4 l l - 42 2 71 14 85 3 18 15 4 1 - -‘ 41 3 102 8 110 - 5 l3 8 3 1 - 30 4 59 7 66 - 12 2 5 10 5 - 34 5 5 10 15 - 3 8 l 2 - - l4 Experiment 8: Mean Temperature 29.6l°C.(Range 27.4-30.7) N = 2: Aphids Counted After 46.25 hours Aphids Counted Aphids Killed Cecid. . Number Alive Dead Total 1_ A; III £2. V__ AA {AA Total 1 82 3 85 - 11 8 8 1 2 - 30 2 278 14 292 - 38 12 8 4 1 - 63 0 Experiment 9: Mean Temperature 30.86 C.(Range 30.2-31.9) N = 5; Aphids Counted After 46.25 hours Aphids Counted Aphids Killed Cecid. Number Alive Dead Total 1 A; III £y_ y_ BE. A; Total 1 29 16 45 3 4 9 4 5 2 - 27 2 226 15 241 - 18 16 5 2 1 1 43 3 380 11 391 - 22 14 4 9 4 - 53 163 13 176 l 12 18 9 4 2 - 46 5 21 14 35 1 12 ll 1 - 29 83 hzmmmza mo—Ia< com . cow e8 o8 o . 1.1. o a ' e o eee e .0” ee 0 fi a... e e en..1_w e e e e e... I‘ll Q IIKIEI3IlIIIIRIlINIlEIEIBINLIIIIIBDNIIIlBIhrlIIBLPIJ1IEI&WUMJWIILP5NIMIMPl1flfib e e e e e ee AuF . . . A O O O O t O 0 dose? . . .. . . . .9 .0853. dance? . uncommom Hmcowuoasm HmumsH pcoomw .mH mmDUHh 0311M SCIlHdV 84 oov ._<>mm._.z_ 1023...: >559! hzmwmma wa.:&< he. as 8. vudo "momcm mm<=0w z a . OOPm-‘N I . e .oomhamw. o _ .. C I. e e 1+1 0 e. I I d a D b L b r D uncommmm Hmsowuossm HmumcH pawns .ha mmDon 03TH)! SOIHdV 85 interval = alive at the 2/3 time interval minus 1/2 killed over the last interval) for the 3rd instars which was fit to a Michaelis-Menton saturation curve (Lehninger 1970, using a computer program courtesy of Dr. Erik Goodman, Dept. of Electrical Engineering and Systems Science, MSU). The curve has a y-asymptote of 41 aphids killed per cecidomyiid. 4. Adult Female Fecundity and Longevity The objective of this section was to measure fecundity and longevity of cecidomyiid females under assumed optimal conditions. El Titi (1973) has demonstrated that females respond to aphid aggregations, laying more eggs when presented with higher aphid densities. In this study, recently emerged females which had been provided with excess food as larvae were confined with 2 males on single fava bean plants (grown in plastic pots) infested with a minimum of 300 (300-400, average 350) pea aphids (see Section II-A-l for description of materials, this number of aphids resulted in fairly dense colonies which were assumed to be optimal in "releasing" oviposition - see E1 Titi 1974b). Adults were confined to each plant using plastic cylinders 9 cm. in diameter and 21 cm. tall. One end of the chamber was capped with a plastic petri dish while the other end was pushed into the dirt surrounding the plant. Four to five 2 cm. diameter holes were cut in the cylinders and covered with screening to allow air circulation. Plants were changed daily at midday with the adults transferred to new plants. Since adults were inactive during 86 the day this was accomplished with little disturbance of the females. The number of eggs deposited on each plant was counted using a microscope. The experiment was performed at room temperature (23.33°C.) and in an environmental chamber set at 16.39°C. (see Section II-A-S). Tables 22 and 23 list daily fecundity and longevity of 22 and 31 females for the two temperatures. Figure 18 shows daily fecundity (per female alive at the start) for the two data sets. Total fecundity per female was slightly higher (163.41 to 150.55 eggs per female) at the higher temperature while longevity was somewhat less (7.41 versus 10.68 days). 5. Female Search and Oviposition E1 Titi (1973) has shown that cecidomyiid females respond to aphid aggregation, laying more eggs with in- creasing density. In addition he showed qualitatively‘ (El Titi 1974a) that females could find aphid colonies under low density conditions (one plant in 75 infested). In this section, the quantitative effect of low aphid density on female oviposition was studied. Cecidomyiid females which were provided with excess food as larvae were confined their first night of adult life with excess males and several fava bean plants heavily infested with pea aphids. At 6:00pm (lab colonies were entrained to light on 4am-8pm, these experiments were per- formed during winter months) on the second night of adult life, 10-30 females were released into a 4.1x3.4x2.9 m. 87 .msHGMOB mom3oHH0m on» pump UGDOM mm3 mHmBmm map was» muumowpcwnu He.mwa o.o h~.o vm.o Hm.o m>.N mv.m mm.m Nm.h mN.mH hm.- mm.m~ mo.mm oo.mm mH.o o H mmmm o w mma I I mom I I m I. 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N O Na ma Oa Oa ON ON ON on Om am am am am ®>aa4a 8. hOOv a Na mw OO Oh boa NON OOO Oev oac OOv mOO FOO NNoa O Bdm haa I I I I I I I GO m Oa N MN ha NO O am «Oa I I I I I I I QON ON O ON OM OM OO O Om OO I I I I I I I I DO O oa ON m aO O ON MON I 0v O oa O Na «a aN ON aN ON vm mv hm O ON Nma I I I I I I GO O aa O ON vN Na .OO O 5N ONa I I I I I I QN O O ON 5 ON O . «O O ON Oma I I I I I CO v O Oa va Na ON mm Na O ON Ov I I I I I I I I I DO a O ON Oa O «N amuOB Oa ea ma Na aa oa O O b O O O m N a HmQBsz .anwo when ease< «0 Damez A.ucooe.m~ mamas 90 Cecidomyiid Fecundity at Two Temperatures FIGURE 18. Ru 11 s ‘ _ . a _ c Q a Av nu s a0 nu \Ll 1mm 3 3 \I 3 .O IIIIID 2 1 .‘v\\\. H a \1 u a. I r I “““ ..\\ L5 IIIHHHHHUIE (ITIIIIII IIIIIIIIIIIIIIIIIIIIIIIII . (Id .....r w A .a. . IN 1.....I a an o hmfirm h< u>3< m4<2mu cum 0.: «Own NIGHTS OF ADULT LIFE 91 greenhouse room containing 1-100 fava bean plants with plants infested with pea aphids as shown in Table 24. The number of eggs deposited on infested plants was determined the following morning. In addition to the females released into the room, 10 females were confined to single fava bean plants identical to those used in Section IV-C-4. These controls were used to monitor variability in the laboratory colony and green- house room environment since individual experiments were performed at approximately 10 day intervals to insure that females released for the previous experiment had died. Temperature within the room fluctuated within the range of 15.6 and 23.9°C. over the duration of the experiment (6pm-8am) for all 6 experiments. The results of the experiments shown in Table 24 indicate that: (1) Control fecundity (range 30.3-34.9 at temperatures fluctuating between 15.6-23.9OC.) was similar to that observed in the lab fecundity experiments (previous section) at 16.39 and 23.33°C. (32.97 and 39.00 respectively for the 2nd night of adult life). (2) With 10 infested plants alone in the room, fe- cundity was reduced somewhat over that of the controls although this effect was less at the higher aphid density (21.7 at a density of 150-250 aphids/ plant, 31.7 at 500-700/p1ant and an average of 92 .nao>ma Nuancoomm museum uo: can muamBmm som3uon aOauauomBoo uonu musmsa ou pmoscou mm3 Ummmmamu mmamBmm mo HonBDZm .muouam noun o>mm mamsam so NaaMDOa>aooa Uuoamcoo muamBmm oa mom ommum>¢ .ucmam\mpanmm OOeIoom u :Oauomm msoa>uum ecu mo am>oa msu um Omummmsa aaoq muCMam mu:Mam HmnBsz Bonn aOauoso OmumomcH moaoBum soaum momcH Omumuwcaca poummmcH ucuBaHmmxm Imm ucmouom mamBmh Hum mOOm mo HonBsz mo HonBsz mo umnBsz muma scauamoma>o pom noummm OaamBOanoU .eN mqmda (3) 93 32.95 with controls at 300-400/p1ant). This re- duction might be caused by the escape of some fe- males from the room (every effort was made to in- sure against this) or more likely by a reduction caused by searching (10 plants in a 4.04x107 cm.3 room versus 1 plant in the 1.34x103 cm.3 confine- ment cylinder). The presence of additional uninfested plants also reduced fecundity levels with the effect less noticeable at the higher aphid density (at 10 and 1% of the plants infested, reductions were 67.7 and 53.6% at the moderate aphid density and 83.0 and 63.4% at high density repectively). 94 D. FIELD EXPERIMENTS 1. Adult Emergence From Overwintering Sites Adams (1977), working in a Massachussettes orchard, placed 10 emergence cages beneath apple terminals which had harbored A. Aphidimyza colonies the previous fall and caught 4 adults on June 11, 1976. This "late" appearance of A. Aphidimyza agreed with his egg sampling data and he concluded that ”owing to a lack of biological synchrony between predator and prey”, (the apple aphid appears and builds up somewhat earlier), "Aphidoletes is unable to prevent early season aphid damage." Jokinen (1980) placed 10 emergence cages at the base of apple trees at the Graham Station in 1977. His trap catch was quite high (eg. 110 A. aphidimyza caught 5/18-5/25) and this author questions whether all of the specimens were A. aphidimyza. In the author's emergence cages at Graham Station, a great number of other Cecidomyiidae of similar appearance were captured. The objective of this section was to characterize the season-long pattern of cecidomyiid emergence from overwinter- ing sites in the soil. a. Klein's Orchard 1979 Forty emergence cages (see Section II-B-2 for a description of cage design) were placed in Klein's orchard (field research sites are described in Section II-B-l) on April 1 and monitored weekly until August 13. Nine trees were chosen randomly with 4 emergence cages placed beneath 95 each tree. Four cages were placed outside the canopy of one tree. All cages were covered with a single layer of cheese- cloth to prevent escape of adults from the cages. Terminals above the cages containing aphids or cecidomyiids were pruned so that emergence records represented adults emerging from overwintering sites. All specimens resembling A. aphidimyza were placed in alcohol, removed to the laboratory and examined under a microsc0pe for positive identification. Genitalia off all male specimens believed to be A. aphidimyza were examined and compared with the drawings of Harris (1966). Table 25 presents the data for the 1979 Klein emerg- ence cages. A total of 31 A. aphidimyza adults were captured (8 males, 23 females). No adults were caught in the 4 cages outside the canopy of the one tree. This data is compared with following emergence cage data from 1980 in Figure 19. The data is plotted using a lower heat unit threshold of 41°F. since pupal developmental data by Havelka (1980), analyzed independently by this author, indicated a lower pupal developmental threshold of 41.20F. b. Testinngmergence Cage Design The low trap catch obServed during the summer of 1979 prompted laboratory testing of emergence cage trap efficiency during the following winter. Adult cecidomyiids were aspir- ated from laboratory colonies (recently emerged adults were used) and released into an emergence cage set up in a green- house room (time of release was 11 am - 7 pm since peak 96 TABLE 25. Klein 1979 Emergence Cage Data Cumulative Cumulative 2322. Heat Units(41'95) .J!1 _g_ 3233; % of Total 4/1 158.6 0 0 0 0.0 6/7 1459.1 0 0 0 0.0 6/15 1719.9 4 2 6 19.4 6/22 1909.9 1 7 14 45.2 6/29 2100.1 2 8 25 80.6 7/6 2290.9 2 28 90.3 7/16 2592.6 1 29 93.5 7/23 2780.1 0 1 30 96.8 7/30 2995.1 0 0 30 96.8 8/13 3390.1 _Q_. _l_. ‘ 31 100.0 Totals 8 23 97 eclosion observed in laboratory colonies was over this time period). The number of adults killed in the aspira- tion process (measured as the number of dead cecidomyiids still in the aspirator) and numbers caught were counted after 48 hours. Two cage designs were tested - with and without a single layer of cheesecloth covering the exterior of the cage. Table 26 presents the data for the laboratory testing of the emergence cage design. The results indicate a recapture rate of approximately 75% with little difference observed when the cheesecloth was removed. c. Fall Seeding of Field Emergence Cages An attempt was made to artificially increase the number of cecidomyiids overwintering in the soil beneath 3 emergence cages at the two trap sites for 1979-80. Laboratory colonies were taken to the field sites and placed in emerg- ence cages on August 25, September 27 and October 4, 1979. The colonies were checked and new aphid infested plants introduced approximately every 2 weeks. Cecidomyiid larvae were observed as late as November 2. Emergence cages were left in place throughout the winter to mark the position of the pupae for monitoring during the spring and summer of 1980. d. 1980 Emergence Cages Twenty emergence cages were monitored every 3 to 7 days at both field sites (Klein 1980, Graham 1980) from May 4 to September 8. Methods were similar to 1979 except that the cheesecloth covering the exterior of the cages 98 am.me wmqmm ee.me ss.me ee.ee ~e.as ma.me amumm me.ae ae.ee ee.ee es.es wwsmaoumum ousummo m N aOa aN hN Om mm OO In In &0 [\I G M Oa Aomoc_umnBsz I cummoauu HonBszO\u:Osmo HonBozN mason OO Houmm Houmuammm ca Omen umnBDZa Hmm menace ImaI me as mm Oh ee\e~\m ee\a\m em\e\m ee\e~\~ em\aa\~ nanoommuno nua3 Omum>oo mOmo mo acauuuxm .m was IMNI em mm Hm Om Damsno uuoBsz O N Hem menses IMOI on me am we nanoumoono usonuaz oODU .« coma anonasz commoamm umnBsz ee\ea\~ eexaxm ee\em\a ee\e~\e ee\ma\a aOaum>uomno mo usas Eaeena ee\a~\m Emeena ee\e\m soon we eexmxm Eaeeue em\m~\~ Ememum em\ea\~ Eameum em\ea\~ Eneeuee em\em\a Eneenfla ee\e~\a suemnm ee\ee\e Eaeena ee\ea\a ommoaom mo oBaB :Oamoo mOmU mocmOumBm mcaumme .ON mnmdfi 99 was removed. Emergence from seeded cages represents the sum of natural and seeded populations. Data for 1980 emergence cages are presented in Tables 27 and 28. In 1980, 288 adults were captured, 30.6% of which were male and 48.3% were from the 6 seeded cages. Cumulative percent emergence for 1979 and 1980 is plotted in Figure 19 on a heat unit scale using a 41°F. lower thres- hold. 1979 and 1980 data are in some disagreement when compared on a heat unit scale (Figure 19), although data for the two sites in 1980 do seem to agree quite well. It is quite possible that some unexplained phenomenon (perhaps soil moisture) triggers spring cecidomyiid emergence. It is also likely that air temperatures don't accurately mimic the pattern of soil temperature fluctuations to which the diapausing pupae are exposed. Of interest is the bimodal form of emergence observed in 1980 with very little emergence from 1400-2300 heat units. It is possible that 1979 monitoring was discontinued prematurely (Aug. 13 versus Sept. 8 in 1980) which resulted in a failure to observe a late season peak in 1979. 2. Trap Plants Placed in a Non-Commercial Setting During the summers of 1978 and 1979, field observations and scout reports had indicated that cecidomyiid larvae seemed to appear in many different crops whenever appre- ciable aphid populations appeared. Earlier work by Jokinen (1980) had indicated that fairly large populations over- winter in some commercial apple orchards. In addition, 100 TABLE 27. Klein 1980 Emergence Cage Data Cumulative Heat Units Seeded_gages Naturalrgages Percent Date (41,95) Agigs Females Males Females of Tota1(95) 5/4 261.0 0 0 0 0 0.0 6/2 766.0 0 0 0 0 0.0 6/5 828.0 0 0 0 2 2.1 6/8 896.2 0 0 0 0 2.1 6/13 962.0 0 0 1 3 6.3 6/16 1033.2 0 0 0 3 9.5 6/20 1108.0 0 0 0 1 10.5 6/24 1214.7 1 3 0 9 24.2 6/28 1343.7 0 2 1 2 29.5 7/2 1445.2 0 0 0 7 36.8 7/6 1553.5 0 0 0 1 37.9 7/11 1704.5 0 0 0 1 39:0 7/19 1968.2 0 0 0 1 40.0 7/25 2151.7 0 0 1 0 41.1 7/31 2323.7 1 l 1 1 45.2 8/7 2537.5 1 2 0 4 52.6 8/14 2735.0 1 1 3 10 68.4 8/21 2935.7 0 1 4 4 77.9 8/28 3147.0 1 2 0 5 86.3 9/4 3353.0 4 4 0 3 97.9 9/8 3462.7 _9_ _A_ _Q_ _A_ 100.0 Totals 9 17 ll 58 101 TABLE 28. Graham 1980 Emergence CageData Cumulative Heat Units Seeded Cages Natural Cages Percent Date (41,95) Males Females Males Females of Total(l93) 5/4 256.6 0 0 0 0 0.0 5/26 600.3 0 0 0 0 0.0 6/2 766.8 2 3 0 0 2.6 6/5 830.3 7 3 0 0 7.8 6/8 896.8 3 2 l 0 10.9 6/13 961.3 4 7 0 0 16.6 6/16 1033.8 0 l 1 1 18.1 5/20 1096.7 3 2 0 1 21.2 6/24 1187.7 9 1 28.5 6/28 1317.4 7 0 32.1 7/2 1415.4 0 0 0 32.1 7/6 1517.9 0 l 0 32.6 7/11 1665.4 0 0 0 32.6 7/19 1923.2 1 1 1 34.2 7/25 2109.7 0 1 34.7 7/31 2275.4 2 3 40.9 8/7 2493.4 3 2 52.9 8/14 2688.4 1 1 63.2 8/21 2875.9 3 11 76.7 8/28 3079.2 6 11 89.6 9/4 3292.7 1 5 96.9 9/8 3399.2 _2_ __2_ L _l_0_0_.g Totals 102 _OO._.O_ $.52: ._.o pumnouo Bouu OOOw . . 5:283 3...... _— ..oo .82 E235 ..--.. 82. 2.5. III. .8 BONBOHBNS IN 3383:! SMIVTDWHO ONO? 2:3. I . . . LS. mocoOumBm uaso¢ m>aumasBsU .Oa OODOHO 103 aphid infested plants left at several abandoned orchard sites had indicated that cecidomyiid females could be attracted to the plants and would deposit eggs close to the aphid colonies. The objective of this section was to investigate the qualitative abundance of cecidomyiids in a natural setting, remote from any commercial apple orchards. The Rose Lake Wildlife Research and Game Area, located northeast of Lansing, MI was chosen for this experiment. No known commercial apple orchards were present within a distance of 10 miles. Four clay pots, each containing 3 fava bean plants infested with approximately 650 (range * 200) pea aphids, were placed in locations separated by approximately 300 m. Plants were placed in water filled trays (to eliminate ants) on the ground and were replaced with fresh plants every 2-7 days. The plants were cut into sections and examined under a microscope for the presence of cecidomyiid and syrphid eggs (several different species of syrphids were observed). Results are listed in Table 29 and plotted in Figure 20. An astounding number of eggs were captured in late June, July and early August. Data from Section IV-C-4 have indicated that laboratory fecundity under optimal conditions for 2 nights was 72.09 eggs/female (nights 2 and 3, Table 22). Thus eggs trapped 8/18-8/19 represent a minimum of 21.6 females (and probably a good deal more). This data indicate that cecidomyiid levels in this natural setting TABLE 29. 104 1980 Rose Lake Trap Plants Data1 Dates Plants Left in Field 5/5-5/8 5/13-5/15 5/19-5/22 5/27-5/30 5/30-6/3 6/3-6/6 6/6-6/8 6/8-6/15 6/15-6/17 6/17-6/21 6/21-6/25 6/25-6/29 6/29-7/1 7/1-7/4 7/4-7/9 7/9-7/12 7/12-7/15 7/15-7/18 7/18-7/21 7/21-7/24 7/24-7/29 7/29-8/1 8/1-8/5 8/5-8/8 8/8-8/12 8/12-8/15 8/18-8/19 8/19-8/23 8/23-8/26 8/26-8/30 8/30-9/2 9/2-9/5 9/5-9/8 9/8-9/11 1Eggs are the total deposited on 4 pots each con- taining 3 fava bean plants. Each pot was infested with approximately 650 pea aphids. Cecidomyiid Syrphid Eggs Eggs 0 10 0 0 0 216 12 160 44 89 160 63 13 455 602 138 16 33 6 29 92 48 466 28 75 111 217 51 116 41 520 34 766 10 916 26 419 6 562 6 849 15 981 46 1185 3 728 3 1798 54 913 25 1560 39 501 13 2631 1 1708 6 1381 0 324 10 124 42 131 16 105 musoam mums oxmq whom OOOH N .ON mmeHm F SiNVWd (NHL 8003 NO .LHOIN 83d ("‘11 $993 SOVHBAV b 106 are quite high and/or cecidomyiid females are extremely good at locating aphid colonies (see Section IV-C-S). 3. Summary of Early Season Cecidomyiid Appearance Data on early season cecidomyiid appearance was obtained from several sources: (1) Emergence cages were placed in favorable orchard sites (Section IV-D-l), (2) Aphid infested trap plants were placed in a remote wildlife area (Section IV-D-2) and (3) Michigan field scouts were asked to report any cecidomyiids spotted during the spring of 1979 and 1980. Data on early season appearance and heat units since Jan. 1 (using a 41°F. lower threshold) are listed in Table. 30. Several factors complicate prediction of first appear- ance of cecidomyiids based on a heat unit concept. Cecid- omyiid larvae construct a cocoon at a depth of about 2 cm. (Markkula and Tiittanen 1977) and thus air temperature may not accurately represent soil temperature to which the pupae are exposed. Secondly, relatively few cecidomyiids overwinter in the orchard and thus data using emergence cages is based on a small smaple size. In addition, other factors such as soil moisture levels may influence over- winter emergence. 4. Commercial Orchard Trap Plants Compared With Direct LarvaI'Sampllng Trap plants were also placed in Block 12 of the Graham Station during the summer of 1980. Direct terminal samples of aphid and cecidomyiid populations were performed for correlation with trap plant catch. The objective was to 107 TABLE 30. First Appearance of Cecidomyiids in the Spring Heat Data Units 1 Source Date Location (41L95) Comments Adams 1977 6/11/76 Belchertown, 1350.5 10 emergence MA cages 4 0 caught on 6/11 Jokinen 1980 5/7/77 Graham Station 510.1 10 emergence Grand Rapids,MI cages This Report 6/7/79 Klein Orchard 1719.9 40 emergence Sparta,MI cages 6/5/80 Klein Orchard 828.0 20 emergence Sparta,MI cages with 3 "seeded" cages 6/2/80 Graham Station 766.8 20 emergence Grand Rapids,MI cages with 3 "seeded" cages 5/28/80 Rose Lake,near 630.2 4 aphid Lansing,MI infestsd trap plants 5/22/80 Washtenaw Co., 539.6 observation MI of larvae in rosy apple 3 aphid colony 1All observations are adults caught in emergence cages except where noted. 2Twelve eggs were collected from trap plants left in the field 5/27-5/29. Night of oviposition was assumed to be. 5/29 because of the stage of egg development. Latest date of emergence was set as 5/28 (first eggs are usually laid the 2nd night of adult life). 3Late instar larvae were reported from a commercial orchard by field scout Robert Kriegel on 5/30. Assuming a late 2nd instar larvae, date of emergence was calculated to be at least as early as 5/22. 108 determine whether trap plants could be used to monitor early season cecidomyiid populations before high apple aphid populations outcompeted the trap plants. Four trap pots (identical to those used in Section IV- D-2) were suspended at head height in trees chosen at random from Block 12. New plants were placed in the orchard every 3-5 days and predators collected were counted using a lab microsc0pe. Terminal samples were taken by choosing 10 trees randomly from Block 12 (see block map in Section II-B-l-b) and counting the number of aphids and predators on each of 10 watersprouts located within the inner 1/2 diameter of each tree. Predator eggs were included in the totals when observed. Syrphid, chrysopid and hemerobiid eggs were fairly easy to see but cecidomyiid eggs were rarely observed although lab inspection (using a microscope) of leaves indicated they were present. Table 31 lists the data for both trap plant and term- inal sample observations for each date. Figure 21 compares the pattern of cecidomyiid eggs trapped and the number of aphids sampled from the terminals with the emergence cage data of Section IV-D-l. It was hoped that the cecid- omyiid trap plants would indicate early season appearance of cecidomyiid females. Data from the Graham 1980 emergence cages showed initial overwinter emergence during 5/26-6/2 with 28.5% of the cecidomyiids emerged by 6/24. In view of the low number of aphids present during this time, it is 109 .as goosm on tessaan nausea we pass sssu now oIsss> nosuoum mmmm .Oeussoo uoc mes coac3 Aeneasooocusdv aem momOacamsa msaso use .OOO eecaacoueBeO ..OUO eeOaOOmmucU esea Oe>uemco msoueeeum secuo I! .seeasenoxsa one saaaseueoom no user was an cesaBueueO we Aseeoeov msueeuaec .m use .OOO macOsosO cemaez HeOacsa mscmshw eue3 eeaoemm soneB ecu coaueum secesu ue OOOa mo HeBBsm ecu Onassc Oeseucsooce meacmsmm ecu “Om . .N\O co ceceu meamBem momeB O\OIN\O .e.a I ce>aO euec umuau ecu How eue meamBem ..eesu Hem Oeuoemmca maecaeueu oa cuaz eeesu ca :0 Aceumemsa mascaBueu no my muoemca no sech: aeuou eue meaOBemN .vsecoso ecu ca Ocsc muceam menu O :0 oeuamomeo mOOe mo senBss aeuou ese muenBDZa lace seaeaa laacasaa ae sas exaIsm\a laces laseaa seaeeaae mm mm smxaIaaxa mosava laces lavas seacaeaa as e a~\aIa~\a .sna ees\ax case case .aecasaa e as aaxaImaxa nossuso saxa canvas saaesa Aeaemaaas ea as amxaIas\a Asmese lessen Aeaeaaaa me ass as\aIes\a .sna ees\am Aaaeae lava Assessae so mas es\aIss\a soscuso a\a saacam cave caeeeaae aa am ssxaIe\a lava asea saaeemes mas ss exaIaxa .sna ees\ax lava love laaeaea sss as ~\aIa~\e noseuso a~\e lava sees saaemsa em a a~\eIs~\e .ses love lavaas as e a~\eIe~\e lees lace sacea am a e~\eIes\e .sna ees\ax mossee love love cases see as e eseras\e eossuse ssxe lace lees leeas a e as\eIa\e case case sees aa a a\eIa\e mosses lave sees lace mos am e a\eIa\e aflalussm humane. message .mem. a amassed haau naan Ilhmem mcacmuhm .oeo muceam . meueo M960 UWHHh CO mmdmemm MHCMHQ WMHB N a eaas nosenum Ensnnu sous nuns massasnm snsssuus can Dense anus .sm memes 110 .eee love love a\a mmlses .sce Asea sseeaa mos e eaa a\aIe\a sees lace levees e eee e\aIs\a ssea Aaeaes Assemae as mass sxaIaa\a love lava lacsas am amen a~\aIm~\a menses .sna ees\a» .eossvs .ses Assam Aenease ma ases maxaIs~\a tossese as\a Ases cascaa lasesmms a has s~\aIas\a malaee.molsvs sses lava Bandeau mes.aom am sass as\aIes\a lace lavas Aeeemass use as eaa asxaIss\a .snm eesxax solace savas lavas leaveeaa mom ea eam ss\aIa\a :osruse axe caaeae Aaacasa saavmeaes sa es a\aIa\a nxmumm unease masseusw ammm nesrma neruo name name sums , escausm .omo mucmsa mwuma eueo umuam co eeamBem muceam mesa ..usooe .sa memes 111 ....n. mm #95:»? >15... mza. ><2 .e an ..«Im...» R a. = a mu ‘1 ...-----.{-I. -I. . o O as Mm I .. .. x. n .4 I .. Lma ..Vw . a . , i .1 .. swears. .... m . E . .. . .. «1O u. a _ u . . son .a on. . . . z w .INI V I u . . . V4.0 a a . _ .. u .. mo screen m .n ... n . sma n . . . .. H u . .. a. . ... m m . .. . .. 8:9... 2.28 .— u m r m ... u .. tonne... eoam .II. 1.8% r . a N ooF u. ... “ ... 3.95...» 35.50... 2ca< ...I. O a u .. u .. 833 .0 35225 I .... I .- m a. . O81 18 . a .. a... a _— a .. .. .... ... .. omP I. n p p P p p [- p p I n p P h" n n p b b p b p p p p p L *8? eaas sosunum statue some nuns massesmm snssEues can sense anus .sa assess 112 surprising that so few eggs were collected on the trap plants. It is possible that the sprays applied on 6/11 and 6/25 reduced trap plant egg deposition. As aphid levels increased (after July 1), trap plant catch remained low although larvae became prevalent as demonstrated by the terminal samples. It was expected that competition from apple aphids would reduce trap plant catch during this period. Also as expected, large trap plant catch began once the orchard apple aphid population had "crashed” in late season (after Aug. 10). V. CECIDOMYIID PREDATION SIMULATION A. OBJECTIVES AND METHODOLOGY The objective of this section was to combine the aphid development and reproduction simulation of Section III with the biological data on cecidomyiid development and predation in Section IV into a simulation of cecidomyiid predation on a single apple terminal. The components of the predation simulation are listed in Section V-B and the output of the simulation is compared with aphid/cecidomyiid sleeve cage data in Section V-C. 113 114 B. SIMULATION STRUCTURE Figure 22 presents a black box model of the aphid/ cecidomyiid single terminal simulation (see Figure 5 for further description of the aphid portion of the simulation). Input to the simulation included the initial number of aphids and cecidomyiids present on the terminal, the duration of the simulation and the temperature profile (daily maximum and minimums) over the period of the simulation. Output included the final number of aphids and cecidomyiids (cecidomyiid larvae which have completed their development on the terminal are converted to pupae) on the terminal and the number of aphids killed by the cecidomyiids. Lines 4560-6520 of the computer program listing in Section VII-B contain the cecidomyiid portion of the simulation. 1. EggAStage Linear regression performed on literature and exper- imental data (see Figure 14, Section IV-C-l) indicated an egg developmental threshold of 51°F. and a developmental period (inverse of the slope x 9/5) of 45.88 heat units (OF.-HU). Since the variability in the egg develOpmental period was fairly small (see standard deviation in Table 17) the egg stage was modeled using a discrete delay (Manetsch and Park 1977) developmental model as shown in Figure 23. The egg stage was divided into 9 equal substages, each of 5 heat units (above the 51°F. developmental threshold) in duration. For the purposes of the sleeve cage simulations, egg mortality (failure to hatch = EMORT) was set to zero since sleeve cage 115 FIGURE 22. Black Box Model of Aphid/Cecidomyiid Simulation Initial Month, Day, Time - IMNTH, IDAY, ITIMIN Inital Number of Aphids - AP(i), i=1,3 Initial Number of Cecidomyiids - CEGG(i),i=l,9;CLARV(i),i=1,33 Duration of Simulation - DAYS Daily Maximum, Minimum Temperature - MAX(I,J),MIN(I,J) Aphid/Cecidomyiid Single Terminal Simulation 1 Final Aphid Numbers - AP(i),i=1,3 Final Cecidomyiid Numbers - CLARV(i),i=l,33;CTPUP Aphids Killed - APKILD Explanation of Variables Not Defined in Figure 5: ITIMIN - Time of day simulation starts on (1=early morning, 2=noon) CEGG(i) - Number of cecidomyiid eggs in each substage CLARV(i) - Number of cecidomyiid larvae in each substage CTPUP - Total number of cecidomyiid pupae APKILD - Total aphids killed by the cecidomyiids 116 FIGURE 23. Cecidomyiid Egg Discrete Delay. Developmental Model CETOL CEGG(i):i=1,2,...9 EQUATIONS: CEGG(i+1,T+DT) = CEGG(i,T) i=1,2,...8 CETOL(T+DT) = CEGG(9,T)*(1 - EMORT) DT = 5 EMORT = 0 Definition of Variables: CEGG(i) - Number of cecidomyiid eggs in the ith substage. CETOL - Number of recently hatched eggs which are trans- ferred to the larval stage. DT - Time step (5 heat units above a developmental threshold of 51°F.). EMORT - Egg mortality (failure to hatch); Since only surviving cecidomyiids.were counted in the sleeve cages, this was set to 0 for this simulation. 117 data is reported in terms of the number of 2nd instar larvae present in each sleeve. 2. Larval Staga Linear regression on experimental data (see Figure 15, Section IV-C-2) indicated a larval developmental threshold of 46.58°F. and a developmental period of 117.57 heat units. Since data for the 2 literature data Sets (Uygun 1971 - 40.64OF., Havelka 1980 - 41.54OF.) indicated lower develop- mental thresholds, the experimental threshold was rounded downwards and a 46°F. threshold was used. The larval stage was also simulated using a discrete delay developmental model as shown in Figure 24. The 3 larval instars were divided into 7, 13 and 13 substages respectively. The number of aphids present on the terminal was assumed to affect the speed of larval development as shown in Table 32 (also see equations in Figure 24). First instar larvae molt to the second instar after killing and feeding on a single aphid (Uygun 1971). The proportion of lSt substage cecidomyiids which successfully attacked their first aphid was represented by the variable ClFIND. In the sleeve cage simulations ClFIND was set to unity since only surviving cecidomyiids were counted. The duration of the lSt instar was 35 heat units (above the 46°F. threshold) regardless of aphid density. The durations of both the 2nd and 3rd larval stages varied from 35 to 65 heat units, increasing with decreasing aphid density as controlled by the variable FRFIND. Under 118 FIGURE 24. Cecidomyiid Larval Discrete Delay Developmental Model lst INSTAR: CLARV(i),i=1,2,...7 znd INSTAR: CLARV(i),i=8,9...20 ( n'nllllllllllm I PR PR PR' PR PR PR 3rd INSTAR: CLARV(i),i=21,22,...33 IIII-EEEEEIIM P' PR PR PR PR PR EQUATIONS: CLARV(1,T) = CETOL(T) CLARV(2,T+DT) = CLARV(1,T)*C1FIND CLARV(i+l,T+DT) = CLARV(i,T) for i = 2,3,...7 CLARV(i+l,T+DT) = CLARV(i,T)*(l-FRFIND) 1-8 10 18, ": .... I CLARV(i+2,T+DT) = CLARV(i,T)*FRFIND+CLARV(i+l,T) 21'23"'°31 CLARV(21,T+DT) = CLARV(20,T) CLTOP(T+DT) = CLARV(33,T) ' ClFIND = 1 (only surviving cecidomyiids were counted in sleeve cages) DT = 5 Heat units above a 46°F. threshold PR - Predation (see Table 33) FRFIND - see Table 32 119 TABLE 32. Simulated Effect of Aphid Density on the Speed of Larval Development Agggg FRFIND 0- 10 0.00 10- 20 0.10 20- 30 0.35 30- 50 0.65 504100‘ 0.90 > 100 1.00 APTOT - Total number of aphids present on the terminal. FRFIND - Fraction of 2nd and 3rd instar cecid- omyiids which are advanced "quickly" due to adequate availability of prey. Duration of Stage in Heat Units Quick Development Slow Development Life Stage (FRFIND=1.00) (FRFIND=0.00) 1St Instar 35 35 2nd Instar 35 65 3rd Instar 35 65 Total 105 165 120 high aphid density conditions, cedidomyiids passed directly from one feeding stage to the next (feeding stages denoted by PR; eg. from stage 10 to 12). If fewer aphids were pre- sent, larvae spent time in an intermediate substage (eg.ll) searching for prey. Mature larvae from substage 33 were transferred to the pupal stage (CLTOP). Predation was simulated as shown in Table 33 (also see Figure 24). First instar larvae killed a single aphid while in the 2nd substage. As mentioned, predation by 2nd and 3rd instar larvae was attributed to 6 feeding substages in each stage (denoted by PR in Figure 24). The relative proportion of aphids killed by each feeding substage was set by the array CSUBKL(i) (see Table 33, e4;.2nd instar larvae in the final feeding substage killed six times as many aphids as those in the initial feeding substage). The number of aphids which would be killed by each larval stage (APKZ for 2nd instar larvae, APK3 for 3rd) was first computed as a function of the number of aphids present, using the functional response data of Figures 16 and 17 (Section IV-C-3). This level was then multiplied by the pro- portion of aphids killed by each substage (CSUBKL(i)) in order to obtain the number of aphids killed by the substage. Note that the total number of aphids killed over a given stage (the sum of aphids killed by each of the 6 feeding sub- stages) would not necessarily equal the level given by the functional response curves since aphid levels would vary over the duration of the stage. TABLE 33. 121 Simulated Cecidomyiid Predation A. Aphids Killed by Bach Feeding Substage Feeding Instar Substage Aphids Killed Per Cecidomyiid 1 2 1 2 10 APKZ * CSUBKL(l) 12 APK2 * CSUBKL(Z) 14 APKZ * CSUBKL(B) 16 APKZ * CSUBKL(4) 18 APKZ * CSUBKL(S) 20 APKZ * CSUBKL(G) 3 23 APK3 * CSUBKL(l) 25 VAPK3 * CSUBKL(Z) 27 APK3 * CSUBKL(B) 29 APK3 * CSUBKL(4) 31‘ APK3 * CSUBKL(S) 33 APK3 * CSUBKL(G) B. Relative PrOportion of Aphids Killed by Each Feeding Substage i CSUBKL(i) CSUBKL(i)/.05 1 .05 1 2 .1 , 2 3 .15 3 4 .2 4 5 .2 4 6 .3 6 C. Functional Response Equations Derived from Figures 16 and 17 APTOT APKZ (see Figure 16) 0- 5 0 5-15 APTOT/15.*7.561 15 7.56 APK3 = (4l.*(APTOT-S))/(20+APTOT-5) (see Figure 17) APK3 = 0 if APTOT 5 1The number of aphids killed by 2nd instar larvae showed little correlation with aphid density above 15 aphids/ter- miaal (see Figurelfi). The average number of aphids killed by 2D instar larvae in the laboratory functional response ex- periment (Table 21) was 7.56 aphids. 122 Functional response data was calculated for a single cecidomyiid confined on an aphid infested leaf (Section IV-C-3). The effect of competition between cecidomyiids was simulated using the variable CFACT as shown in Figure 25. The ratio (RAT) of the number of aphids that would be killed in the absence of competition (i.e. the number of cecido- myiids on the terminal multiplied by the number that would be killed by a single cecidomyiid) divided by the number of aphids present (APTOT) was first computed. CFACT represents the proportional reduction in the number of aphids killed (as a function of this ratio) due to competition. The number of aphids killed during each model iteration was computed as a function of the total number of aphids present on the terminal regardless of life stage. Aphids were then removed (i.e. killed) in proportion to the numbers present on the terminal in each life stage (i.e. if 10% of the aphids were killed, 10% of each life stage was removed). Thus cecidomyiids were not assumed to preferentially attack one life stage over another. 123 h0h¢<\zo_h_hma200Fault; nm._.:x main: V . . a. . .. - ... v n N. «J w. 225.525 m5 2. 33 550 ..... .... m 02_Iomwmam Hmwuwcfi Ha cowuowomnm cofiumasaam Hmcwm mm cofiumHsmom ammo m>mmam Hmcwm H mm oumn3 m\NA :«kfimsoazimmums .. :55 a m\N vAHaam¢.m¢Vx o.mm H mm m «N am _ cone mN\m m «.5m «H.5m m.N m.mN . m.mN :oNumNnaNm o.mv mm v NN as omum exp o.mm H mm N m an acne mN\m v N.mN Am.» a. m.N «.5 coNumasaNm m.mN «N N N NH omum o\N m.» w mN N NN m mean mN\m m H.mm mm.oo m.m o.¢N N.mm :oNumasaNm m.mm me m NN ma cmum o\N o.mN N om N mN NH mvum mN\m N >.q¢ mAm.N¢N H.0N «.ma «.mNN :oNumHsst o.mm can we SNN NoN omum exp o.Nm N Nm N AN NN omnm meo N Nomxma; .NoNumm .chomo soam< “mama ANema ANema mmuma umbesz HafiuacH HmwuflcH muasom mumumcH mumumcH mmmu >H a HHH NH 5 H m>mmNm usmuso Hmcoz nodumaseflm nuw3 Umummaou mommu m>wmam How mama coflumcoum .vm mqmH.« HHH HH O H m>mmHm H.ucooO .«m mqmae 127 0.00 AO.OH O.N O.« O.OH coHuOHsaHO 0.0« «O O OH OH OOOHH OH\O 0.0H « OO O O« OH OOuNH HH\O ON O.«« OO.OOH O.NH 0.00 O.NO aoHuOHsaHO 0.0« OOH OH O« «O OOOO OH\O O.OO O OHH O OO OO OOOO «H\O OH O.ON 40.0 «. O.N 0.0 coHuOHseHO «.OO NN O O HH OHuO OH\O N.OH O HO « HN OO OOuO «H\O OH 0.0« OO.OOH H.HH O.HO H.OO coHumHssHm O.NO OOH OH OO OO OHuO OH\O O.ON O «O « H« OO OOuO «HxO OH 0.0« O«.OON N.OH O.«O «.OHH coHuOHseHO 0.0« OOH OH O« HO OHuO OH\O O.NO H NO H OO HO OO"« «H\O OH O.«« OO.OHH 0.0 N.H« H.OO coHumHseHO 0.0« OOH HH OO «O OHuO OH\O O.ON O O«H O OO NO OO.« «H\O OH 0.0« «O.OOH N.OH O.O« «.NO :oHuOHssHO N.O« OOH «N N« OOH OOOO OH\O O.ON O OOH OH «O OO OO"« «HxO «H omxma oHuOm .OoHomo eoOOO HOOOO ANOm4 AHOOO mmumo Hunssz HOHOHOH HOHuHaH OOHOOO OHOOOOH OumumcH mOOo >H O HHH HH O H m>mmHO H.u:ooO .«O mHmaa 128 N.¢N. m.HN o.mH o.mH m.o~ m.a Dmxmd owumm HmwuHGH HO.O OO N OO m0.0 H O ON .mvHomo OOOOO HOHOHOH O. H.O O HH H OH O. O.H O H H OH HOOOO ANOOO muascd mumumcH >H O HHH m.v «H ma m.m o m AHOma mumumcH HH a H coHumHssOm O«"HH OH\O OHOH HH\O :oHuOHOeHO OOOHH OH\O OOuNH HH\O mmuma mm Hm Hmnfisz wmmo m>wmam H.u:ooO .«O mummy 129 FIGURE 26. Sleeve Cage Data Compared with Simulation Model Output (with Predation) I r A I 600 KEY: 5007‘ A ACURACY RATING“ FINAL POP [flSIMULATION 400% _ INITIAL POP. - H . 3300i- — + E .L A A, g 0 1' ()ZKIDP } L, p. ' o "‘ A A z “(A O ‘3? l A 1(“3? ‘, -7 I! “ 1 II [:1 1 E] '- A I}: m [I] L ‘ $17 20 SLEEVE CAGE NO 130 ..ooo\%_c..a<. Sam 2 25. ,OO-. 8 T OO Oh Om" ON Or j T .. 23802000 25 \3 33:0 5:225?! . . 33 3:38.395 .. _ OOOO 2.33 . iIF . .- b I p b - ~ :oOumomum omumHsEOm 0cm pm>ummno Mo comOHmmEou .ON mmslo l k PIMWOPIoeo / PPIII>I SPIudv VI. DISCUSSION AND CONCLUSIONS A. APHID SIMULATION Reanalysis of Lathrop's (1923) aphid developmental data indicated a 37°F. developmental threshold in contrast to the 41°F. threshold used commonly by other authors (Lathrop 1923, 1928, Westigard and Madsen 1965, Specht 1970, 1972, Jokinen 1980). In addition, the upper develOpmental threshold was tentatively set at 95°F. Additional data to support or refute these thresholds (particularly the upper threshold) would be useful. Grouping data on nymph developmental periods by the month of birth revealed an interesting relationship. Mean developmental periods of aphids born early in the season (March-April 322.2, May - 320.6) were somewhat higher than periods during mid-season (June - 286.4, July - 293.8, August - 297.9). The September mean (343.2) was more in the range of the early season means. This relationship may have been due to the use of a lower developmental threshold which was too low (use of a low lower threshold results in heat summations which decrease as the mean temperature increases - Arnold 1959). Use of a higher developmental threshold (41°F.) resulted in better agreement between early and mid-season developmental periods but resulted in a late season (September) period that was still high in comparison. A second factor which may have caused slower development in early and late season is the in- fluence of tree nutrient status. Especially in late ' 131 132 season, reduced nutrient availability may have slowed aphid development. The aphid simulation presented in Section III was fairly successful in predicting short-term (3-7 days) population trends of aphids confined to a single apple terminal. The effects of tree nutrient status and aphid density on population dynamics were crudely mimicked using the equations presented in Table 10. Mbre accurate simulation of population trends over longer time periods will depend on more accurate data on the effect of these factors. The effects of pesticides applied for control of other apple pest species is an additional factor which limits the feasibility of long-term aphid simulations. Data on the effect of sub-lethal pesticide doses on aphid development and reproduction would be especially useful. 133 B. EXPERIMENTS ON CECIDOMYIID BIOLOGY Laboratory experiments on basic features of cecidomyiid biology provided useful data for the simulation model of Section V. Additional data on female search and oviposition behavior would be quite useful in extending the simulation beyond its present scope. This aspect of cecidomyiid be- havior appears especially significant in view of the limited dispersal abilities of cecidomyiid larvae (Wilbert 1972). Cecidomyiid females appear functionally equivalent.to many insect parasitoids. Females search for aphid colonies and the number of eggs laid increases with increasing aphid density (El Titi 1974b). Larvae are essentially at the mercy of the environment in which they were placed as eggs. Thus female search and oviposition behavior "regulates" subsequent predation by the larvae. Field experimental data indicated some rather useful and surprising features of cecidomyiid biology. Emergence from overwintering sites appears to start in early June and continues throughout the season. This "late” appearance of cecidomyiids (aphids appear somewhat earlier), necessitates early season aphid control by alternative means. Emergence distributed over the summer is most likely a survival mechanism evolved in re- sponse to the ephemeral nature of most aphid populations (of which the apple aphid is an exception) and to the possibility of exploitation of a number of aphid species. In general, aphids are an r-adapted species, well suited to capitalize on a flush of growth on a host plant, and then disperse to a new 134 host. Continuous emergence of cecidomyiids over the season insures that at least some of the predators will survive to perpetuate the species. Aphid infested trap plants appear to be a good qualitative tool to sample for the presence of adult cecidomyiids. Trap plant catch from the Rose Lake area and other non-commercial sites indicated that large pop- ulations are present outside of commercial apple orchards. Trap plants were not shown to be useful in predicting early season appearance of cecidomyiids at Graham Station during 1980. Perhaps insecticide sprays applied during this period reduced trap plant egg deposition. Additional research is needed to develop an efficient sampling method for cecid- omyiids present at low densities (direct larval samples are laborious and useful only at moderate cecidomyiid densities). 135 C. PREDATION SIMULATION The objectives of this section were only partially met. The predation simulation of Section V was fairly successful in predicting the number of aphids killed by cecidomyiid larvae at different aphid densities. Eval- uation of the impact of cecidomyiid predation on orchard aphid control, however, requires additional data on long- term aphid population dynamics, the sub-lethal effects of pesticides on aphid development and reproduction and exten- sion of the cecidomyiid portion of the simulation model to include between-generation phenomena. Adequate data are available on cecidomyiid pupal developmental rates (Havelka 1980) and the effect of pesticides on cecidomyiid life stages (warner 1981). Thus the major limitation to extending the cecidomyiid simulation is the need for additional data on female search and oviposition behavior. It is this aspect of cecidomyiid biology - aphid host location and egg deposition by the female, whichdetermines the impact of cecidomyiid predation. Further research in this area would greatly improve our understanding of this species which shows so much promise as a biological control agent of aphids on a wide variety of agricultural crops. VI I . APPENDIX A. SIZE AND WEIGHT COMPARISONS FOR I}: PISUM, fl- PERSICAE AND A. POMI Aphid length (excluding cornicles) and width were measured using a microscope eyepiece micrometer (100 divisions/ cm.). weight was estimated by weighing 50-100 aphids (recently killed using ethyl acetate) using a Mettler H31AR balance (1 .0001 g.; courtesy Dr. Jim Miller). Pea aphids [Acyrthosiphon pisum (Harris)] were collected from a colony reared on fava beans (Yigig_§gg§ L.). Apple aphids (A, pomi) were collected from apple terminals on July 28, 1980 from an abandoned orchard on the MSU campus. Green peach aphids [Myggg persicae (Sulzer)] were collected from a laboratory colony reared on jimsonweed (Datura stramonium L.). Table 35 lists size and weight measurements for each species. Pea aphids are much larger than the other two species. Green peach aphids are very similar in size and weight to apple aphids and thus were assumed equivalent in the cecidomyiid larvae functional response experiment of Section IV-C-3. 136 137 TABLE 35. Size and weight Measurement for 3 Aphid Species Length1 Width1 Average Weight Species Instar (cm.) _(gm;) (mg.) A. pisum 1 .11i.01 .osi.01 .13 2 .14i.oz .06i.01 .26 3 .19i.02 .09:.o1 .71 4 .251.01 .12i.01 1.42 Apterae .33i.01 .Isi.01 2.64 Alatae .251.01 .091.01 2.85 g. persicae 1 .051.01 .03i.01 .02 2 ..071.01 .041.01 .03 3 .09i.01 .osi.01 .07 4 .121.01 .06:.01 .12 5 .14i.o1 .07i.o1 .18 Apterae .15i.o1 .loi.01 .32 Alatae .13i.ol .063.01 ' .21 A. pomi 1 .051.01 .o3i.01 .03 2 .09i.01 .osi.o1 .04 3 .11i.01 .oei.o1 ‘.14 4 .13i.o1 .07i.01 .25 Apterae .16i.01 .lOi.01 .34 Alatae .151.01 .073.01 .22 1Length and width measurements are average 1 1/2 range; i.e. .33-.01 corresponds to an observed range of .32-.34 138 B. COMPUTER PROGRAM LISTING Section VII—B contains a listing of the computer program used for the aphid simulation of Section III and the cecido- myiid predation simulation of Section V. The program is written in FORTRAN IV for the MSU Cyber 750. 1. Program Term This is the main program which interfaces with sub- routines DEGD, DELAY, INITIAL, CONVERT and OUTPT. Daily maximum and minimum temperatures are read from an input file attached locally as TAPE1 (Section VII-C contains some of the weather data contained in TAPE1). 100=C******************************************************** 120= PROGRAM TERM(INPUT=65,0UTPUT=65,TAPEl) 140=C******************************************************** 160=C . 180=C THIS PROGRAM SIMULATES A SINGLE APPLE TERMINAL 200=C ATTACH WEATHER DATA AS TAPE1 220=C CATALOGED As EWPGJMTERM 240=C 260= COMMON /ALL/RNY(20),K,DEL,XNY(2),AP(3), 280= +APTOT,ISTART,TOTHU(4),ITIMIN,AA(18),CSTART,APDIE, 300: +CEGG(9),CLARV(33),CTEGG,CTLARV(3),CTPUP,TCEC, 320= +TAPKLD,TBORN 340=C 360= DIMENSION MAX(5,31),MIN(5,31),IDPM(12),ITHRLO(4), 380= +ITHRHI(3),DD(3),FEC(18),SURV(17),THEAT(3),NITT(3), 390= +CSUBKL(6) 400=C 420= DATA DEL/292.19/ 440= DATA K/20/ . 460= DATA SURV/7*1.0,.95,.8947368,.8823529,.8666667, 480: +.8461538,.8181818,.7777778,.7142857,.6,.3333333/ 500= DATA FEC/l.39,7*.625,.3863158,.4305882,.l746667, 520= +.1538462,.0818182,.l,.0257l43,.036,2*0.0/ 540=C FEC(1)=1.39(NOT .625) COMPENSATES FOR lST STAGE 560=C ADULTS NOT LEFT THERE FOR FULL 50 HU‘ 580= DATA PLR/.00038/ 600=C PLR=.00038 GIVES 10 PERCENT MORTALITY OVER NYMPH STAGE 620= DATA ITHRLO,ITHRHI/37,Sl,46,3*95/ 640= DATA IDPM/31,28,31,30,3l,30,31,31,30,31,30,31/ 700= DATA CSUBKL/.05,.1,.15,.2,.2,.3/ 720=C 139 740=C***** CONTROL SECTION 760= 780=2 920= 940=C 960= 980= 1000=8 1020=C 1060= 1260= 1280=C IREP=0 ISTART=1 ‘ IF(ISTART.NE.1)GO TO 8 ITIMIN=1 MEANS SIMULATION STARTS IN THE MORNING PRINT *," ENTER MONTH,DAY,TIME (10R2) SIM STARTS ON..." READ *,IMNTH,IDAY,ITIMIN CONTINUE ' ITIM=ITIMIN IF(IREP.EQ.1)GO TO 40 1300=C***** READ WEATHER DATA FROM TAPE1 1320=C 1360= 1380= 1400= l420=4 1440=C 1460=5 1480-10 1500= 1520= 1540=15 1560= 1580= 1600=C 1620=20 1640=25 1660= 1680= 1700=30 1720=35 1780=C REWIND 1 PRINT *," ENTER SITE,YEAR TO RUN SIMULATION FOR..." READ 4,SRUN,IYRRUN ' FORMAT(A4,1X,I4) READ(1,10) IYR,SITE FORMAT(1X,I4,1X,A4). IF(IYR.EQ.IYRRUN.AND.SITE.EQ.SRUN) GO TO 20 READ(1,15) FORMAT(23(/)) IF(EOF(1).NE.0)PRINT *," END WEATHER FILE ENCOUNTERED" GO To 5 READ(1,25) FORMAT(7(/)) DO 30 I=5,9 READ(1,35) (MAX(I,J),J=1,31) READ(1,35) (MIN(I,J),J=1,31) FORMAT(4X,3113) 1800=C***** INITIALIZATIONS 1820=C 1840=40 1880a 19003 2580=C 2600= 2700= 2720= 2730= 2735= 2740= 2750= 2760= 2780= 2820= 2830=52 2831= CONTINUE PRINT *," ENTER DAYS,OUTFR..." READ *,DAYS,OUTFR CESURV=1.0 IF(ISTART.EQ.0)GO TO 50 CALL INITIAL CTPUP=0. APDIE=0. CALL CONVERT CSTART=TCEC IF(ITIMIN.EQ.1)ITIM=0 IF(ITIMIN.EQ.2)ITIM=1 DO 52 I=l,4 TOTHU‘I)=0. TAPKLD=0. 2840= 2860= 2880=C 2900= 2920= 2940= 2980= 3020= 3040= 3060= 3080=44 3100= 3120= 3140= 3160=50 3180=C 3200= 140 TBORN=0. CALL OUTPT(IMNTH,IDAY,ITIM) OUT=.0001 CETOL=CLTOP=0. APKILD=0. BORN=0. APDIE=0. NTHR=3 DO 44 I=1,4 THEAT(I)=0. IADAP=0 DT=5. CELAID=0. CONTINUE NIT=DAYS/.5+.0001 3220=c********** 3240= DO 200 IDUM=1,NIT 3260=C********** 3280=C 3300=C 3320=C 3340=C 3360=C 3380= 34008 3420=C 3440860 3460= 3480= 3500= 35208 3540= 3560865 3580=C 3600= 3640= 3660= 3680= 3700= 3720= 3740= 3760= 3780=70 3800=C 39808 4000= 4060=89 4080=C 4180= 4200= 4210= 4220= OVERALL TIME STEP IS 1/2 DAY; WITHIN EACH HALF DAY EACH STAGE IS UPDATED SEPARATELY DUE TO DIFFERENT DEVELOPMENTAL THRESHOLDS ITIM=ITIM+1 IF(ITIM.EQ.3)ITIM=1 IF(ITIM.EQ.2)GO TO 65 IF(ISTART.EQ.1)GO TO 65 IDAY=IDAY+1 IF(IDAY.LE.IDPM(IMNTH)) GO TO 65 IDAY=1 IMNTH=IMNTH+1 CONTINUE ISTART=0 IMN=IMNTH IDY=IDAY IF(ITIM.EQ.1)GO TO 70 IDY=IDAY+1 IF(IDAY.NE.IDPM(IMNTH))GO TO 70 IMN=IMNTH+1 IDY=1 CONTINUE MX=MAX(IMNTH,IDAY) MN=MIN(IMN,IDY) CONTINUE DO 90 JTHR=1,NTHR CALL DEGD(MX,MN,ITHRLO(JTHR),0,ITHRHI(JTHR), +DD(JTHR)) THEAT(JTHR)=THEAT(JTHR)+DD(JTHR)*.5 4240= 4260= 4280= 4300=90 4320=91 4340=C 4360= 4380= 4400= 4420= 4440= 4460=C*** 4480= 4500= 4520=C*** 4540=C 141 TOTHU(JTHR)=TOTHU(JTHR)+DD(JTHR)*.5 NITT(JTHR)=THEAT(JTHR)/DT THEAT(JTHR)=THEAT(JTHR)-(NITT(JTHR)*DT) CONTINUE CONTINUE ITCEG=ITCLA=ITAP=O NITMAx=NITT(1) IF(NITMAX.LT.NITT(2))NITMAx=NITT(2) IP(NITMAx.LT.NITT(3))NITMAx=NITT(3) IF(NITMAX.LT.1)GO TO 161 D0 160 ITERA=1,NITMAX CALL CONVERT 4560=C*****CECIDOMYIID SECTION 4580=C 4940=C* 4960= 4980= 5020=C 5040=C* 5050=C 5060= 5080= 5100= 5120= 5140= 5160= 5180= 5200= 5220= 5240= 5260= 5280=79 5300=C 5320=C* 5360= 5380= 5390= 5400= 5410=80 5420= 5500=C 5520=C* 5550= 5560= 5570= 5580-81 5590= 5620=C 5640=C* UPDATE LARVAE ITCLA=ITCLA+1 IF(ITCLA.GT.NITT(3))GO TO 84 DETERMINE DELAY IN DEVELOPMENT DUE TO SEARCHING FOR APHIDS FRFIND=1. IF(APTOT.GE.100.)GO TO 79 FRFIND=.9 IF(APTOT.GE.50.)GO TO 79 FRFIND=.65 IF(APTOT.GE.30.)GO TO 79 FRFIND=.35 IF(APTOT.GE.20.)GO TO 79 FRFIND=.1 sIF(APTOT.GE.10.)GO TO 79 FRFIND=0. CONTINUE 3RD INSTARS (CLARV(21-33)) CTPUP=CTPUP+CLARV(33) DO 80 I=l,6 ISUB=35-I*2 CLARV(ISUB)=CLARV(ISUB-2)*FRFIND+CLARV(ISUB-l) CLARV(ISUB-l)=CLARV(ISUB-2)*(l.-FRFIND) CLARV(21)=CLARV(20) 2D INSTARS (CLARV(8-20)) DO 81 I=1,6 ISUB=22-I*2 CLARV(ISUB=CLARV(ISUB-2)*FRFIND+CLARV(ISUB-l) CLARV(ISUB-l)=CLARV(ISUB-2)*(l.-FRFIND) CLARV(8)=CLARV(7) lST INSTAR (CLARV(1-7)) 5680= 5700= 5720= 5740= 5760=86 5800= 5820= 5840= 5860=C 5880=C* 5890= 5895= 5900= 5905= 5910= 5915=82 5920= 5925= 5926= 5935: 5940= 5945= 5950= 5955=C 5960=C 5970=C 5975= S976= 5977= 5978= 5979: 5980= 5981= 5982= 5983= 5984= 5985= 5986= 6025=802 6030= 6035=84 6320=C 6340=C* 6380= 6400= 6420= 6440= 6460= 6480=93 6500= 6520=94 6540=C 142 CLARV(1)=CLARV(1)+CETOL CETOL=0. DO 86 I=1,5 ISUB=8-I CLARV(ISUB)=CLARV(ISUB-1) ClFIND=l. CLARV(2)=CLARV(1)*C1FIND CLARV(1)=0. COMPUTE NUMBER OF APHIDS KILLED CPRZEQ=CPR3EQ=0. DO 82 I=l,6 ISUBl=2*I+8 CPRZEQ=CPR2EQ+CLARV(ISUBl)*CSUBKL(I) ISUBZ=2*I+21 CPR3EQ=CPR3EQ+CLARV(ISUBZ)*CSUBKL(I) APK2=7.56 ~ IF(APTOT.LT.15.)APK2=APTOT/15.*7.56 AI(APTOT.LT.5.)APK2=0. APK3=(41.*(APTOT-5.))/(20.+APTOT-5.) IF(APTOT.LT.5.)APK3=0. TKILD=CLARV(2)+CPR2EQ*APK2+CPR3EQ*APK3 RAT=TKILD/APTOT - REDUCE APHIDS KILLED DUE TO COMPETITION BETWEEN CECIDS CFACT=1. IF(TCEC.LE.1.)GO TO 802 IF(RAT.LE..5)GO To 802 CFACT=l.-.05*(RAT-.5)/.25 IF(RAT.LE..75)GO TO 802 CFACT=.95-.15*(RAT-.75)/.25 IF(RAT.LE.1.)GO T0 802 CFACTé.8-.18*(RAT-l.)/.5 IF(RAT.LE.1.5)GO TO 802 CFACT=.62-.12*(RAT-l.5)/.5 IF(RAT.LE.2.)GO TO 802 CFACT=l./RAT CONTINUE APKILD=CFACT*TKILD CONTINUE UPDATE EGGS ITCEG=ITCEG+1 IF(ITCEG.GT.NITT(2))GO TO 94 CETOL=CETOL+CEGG(9)*CESURV DO 93 I=1,4 ISUB=lO-I CEGG(ISUB)=CEGG(ISUB-l) CEGG(1)=0. CONTINUE 6560=C*****APHID SECTION - ALL ON SAME THRESHOLD (37) 6580=C 66008 66208 66408C 6760=C 6770=C 68208 68608 68808 69008 69208 69408100 69608C 69808C 70008 70208 70608 70808 71008 71208 71408 71608 71808 72008 72208 72408 72608101 72808C 73008C* 73408 73608102 73808 74008106 74208C 74408C* 74708 75008 75208800 75408 75608801 75808808 76208 76408C 76608C* 76708C 77608 77808 78008 78208 78408 78608 78808108 79008 143 ITAP8ITAP+1 IF(ITAP.GT.NITT(3))GO TO 118 REDUCE FECUNDITY BY DFACT; 0-100 DFACT81.; 100-1000 DFACT8 1.-.25; GT.1000 DFACT8.25 DFACT81. IF(APTOT.LE.100.)GO TO 100 DFACT8.25 IF(APTOT.GT.1000.)GO TO 100 DFACT8l.-.7S*(ALOG10(APTOT)-2.) CONTINUE REDUCE FECUNDITY BY TFACT BY DATE IF(ITAP.GT.1)GO TO 101 TFACT81.3 IF(IMNTH.LE.6)G0 TO 101 IF(IMNTH.EQ.7.AND.IDAY.LE.4)GO TO 101 TFACT8.9 IF(IMNTH.EQ.7.AND.IDAY.LE.20)GO TO 101 TFACT8.6 IF(IMNTH.EQ.7)GO TO 101 IF(IMNTH.EQ.8.AND.IDAY.LE.6)GO TO 101 TFACT8.5 IF(IMNTH.EQ.8.AND.IDAY.LE.24)GO TO 101 TFACT8.4 CONTINUE APHID FECUNDITY (ADD LATER) DO 102 ISUB81,18 BORN8BORN+AA(ISUB)*FEC(ISUB) BORN8BORN*DFACT*TFACT CONTINUE ‘ APHIDS KILLED BY CECIDS HERE IF(APKILD.LT..0001)GO TO 808 D0 800 I81,18 AA(I)8AA(I)§(1.-APKILD/APTOT) DO 801 I81,20 RNY(I)8RNY(I)*(l.-APKILD/APTOT) TAPKLD8TAPKLD+APKILD APKILD80. UPDATE ADULT APHIDS WITH MORTALITY (DISCRETE EVERY 50 HU) IADAP8IADAP+1 IF(IADAP.NE.10)GO TO 110 IADAP80 APDIE8APDIE+AA(18) DO 108 I81,l7 ISUB818-I AA(ISUB+1)8AA(ISUB)*SURV(ISUB) AA(1)80. 144 7920:110 CONTINUE 7940=C 7960=C* UPDATE APHID NYMPHS 8020= CALL DELAY(XNY(1),XNY(2),RNY(1),PLR,DEL,DT,K) 8030=C NOTE XNY(Z) CHANGED TO AMOUNT IN DELAY 8031= AA(l)=AA(1)+XNY(2) 8040=ll7 CONTINUE 8080= RNY(l)=RNY(1)+BORN*K/DEL 8100: TBORN=TBORN+BORN 8120= BORN80. 8140=118 CONTINUE 8160=C 8200=C*** 8220=160 CONTINUE 8240=C*** 8260=161 CONTINUE 8280=C 8300=C* DETERMINE IF TIME FOR OUTPUT 8340= OUT=OUT+.5 8360= IF(OUT.LT.OUTFR)GO TO 200 8380= CALL CONVERT 8400= OUT8.0001 8420: CALL OUTPT(IMNTH,IDAY,ITIM) 84408C 86203C********** 86408200 CONTINUE 8660=C********** 8680=C 8700=C* RERUNS 8720: PRINT 240 8740:240 PORMAT(/."WISH TO CONTINUE THIS RUN (YORN)...") 87608260 FORMAT(A1) ' 88008 IF(ANS.EQ.1HY)GO T0 40 88208C 88408 PRINT*,"WISH To START A NEW RUN FROM SAME SITE?..." 8860: READ 260,ANS 8880= IF(ANS.EQ.1HN)GO TO 270 8900= IREP=1 8920: GO TO 2 8940:270 CONTINUE 8960=C 89808 END 145 2. Subroutine DEGD This subroutine calculates heat units in a day using a sine wave temperature profile based on daily maximum and minimum temperatures (adapted from Baskerville and Emin 1968, Allen 1976). When used with a 3 point sine wave (in which the two minimums may be different, see Figure 3), the subroutine was called twice a day with DD (degree-days) halved (see lines 4180-4300 in Program TERM). 11120=C ************************************************* 11140= SUBROUTINE DEGD (MAX,MIN,K1,K2,K3,DD) 11160=C **********************************.*************** 11300=C 11320: DATA PI/3.14159/ 11360=C**** NO UPPER THRESHOLD CUTS MADE 11380=C 11400=C* NO HEAT, MAX BELOW Kl 11420= TBAR=(MAx+MIN)/2. 11440= AMP=(MAx-MIN)/2. 11460: DD=0. ll480= IF(MAX.LE.K1)RETURN 11500=C 11520=C* CASE A, No CUTS, UPPER.GT.MAx AND MIN.GT.K1 11540: DD=TBAR-Kl ‘ 11560= IF(K3.GE.MAX.AND.MIN.GE.K1)RETURN 11580= IF(K2.GE.MAX.AND.MIN.GE.K1)RETURN 11600=C ' 11620=C* CASE B, CUT AT BOTTOM, UPPER.GE.MAx AND K1.GT.MIN 11640: IF(K3.EQ.0.AND.MAX.GT.K2) GO To 100 11660= IF(K2.EQ.0.AND.MAX.GT.K3)GO TO 10 11680= TH1=ASIN((FLOAT(Kl)-TBAR)/AMP) 11700= DD=(AMP*COS(TH1)+(TBAR-K1)*(PI/2.-TH1))/PI 11720= RETURN ll740=C ll760=C**** HORIZONTAL CUTOFF (K3) 11780=C 118008C* CASE C1, CUT TOP, MAX.GT.K3 AND MIN.GT.K1 11820810 TH28ASIN((FLOAT(K3)7TBAR)/AMP) 11840= IF(K1.GT.MIN)GO TO 20 118608 DD=((K3-Kl)*(PI/2.-TH2)+(TBAR-Kl)* 11870: +(TH2+PI/2.)-AMP*COS(TH2))/PI 11900= RETURN 11920=C 119408C* CASE C2, CUT AT TOP AND BOTTOM, MAX.GT.K3, K1.GT.MIN 146 11960=20 THl=ASIN((FLOAT(K1)-TBAR)/AMP) 11980= DD=(AMP*(COS(THl)-COS(TH2))+(K3-Kl)*(PI/2.-TH2)- 12000= +(K1—TBAR)*(TH2-TH1))/PI 12020: RETURN 12040=C 12060=C****VERTICAL CUTOFF (K2) 12080=C 12100=C* CASE Dl, CUT TOP, MAX.GT.KZ AND MIN. GT.K1 12120=100 TH2+ASIN((FLOAT(K2)-TBAR)/AMP) 12140= IF(K1.GT.MIN)GO To 110 12160= DD=((TH2+PI/2.)*(TBAR-Kl)-AMP*COS(TH2)))/PI 12180= RETURN 12200=C 12220=C* CASE D2, CUT AT TOP AND BOTTOM, MAX.GT.KZ, K1.GT.MIN 122408110 TH1+ASIN((FLOAT(K1)-TBAR)/AMP) 12260= DD=((TH2-TH1)*(TBAR-Kl)+AMP*(COS(THl)-COS(TH2)))/PI 12280= RETURN , 12300= END 123208C 147 3. Subroutine DELAY This subroutine implements the distributed delay model of aphid nymph development (modified from Manetsch 1976). 10630=C****************************************************** 106408 SUBROUTINE DELAY(VIN,VOUT,R,PLR,DEL,DT,K) 10650=C****************************************************** 106608C 106908 107008 107408C 107608 107808 108008 108208C 108408 108608C 108808 109008C 109208 109408 109608 10980810 11000820 110208C 110408 110608 110808C 111008C DIMENSION R(1) FK8FLOAT(K) B81.+PLR*DEL/FK IDT81.+2.*DT*FK/DEL*AMAX1(B,0.) A8FK*DT/(DEL*FLOAT(IDT)) KM18K-1 VOUT8R(K)*A*B*DEL/K DO 20 J81,IDT DO 10 IC=1,KMl I8K-IC+1 R(I)=R(I)+A*(R(I-1)-B*R(I)) R(1)=R(l)+A*(VIN-B*R(l)) RETURN- END 148 4. Other Subroutines These 3 subroutines interface with Program TERM. Subroutine INITIAL initializes aphids and cecidomyiids at the beginning of each simulation. The aphid simulation of Section III is run with 0 cecidomyiids. Subroutine CONVERT converts the number of aphids and cecidomyiids in each sub- stage into their respective stage totals. Subroutine OUTPT prints the output data (output time, heat units and numbers in each life stage for the two species) for each simulation. 12340=C ***********t************************************* 123608 SUBROUTINE INITIAL . 123808C ************************************************* 124008C ' 124208 COMMON /ALL/RNY(20),K,DEL,XNY(2),AP(3), 124408 +APTOT,ISTART,TOTHU(4),ITIMIN,AA(18),CSTART,APDIE 124608 +CEGG(9),CLARV(33),CTEGG,CTLARV(3),CTPUP,TCEC, 124708 +TAPKLD,TBORN 124808C 125008 DIMENSION APHIN(3) 125208C 125808C*****APHID SECTION 126008C ' 126208 ISU31286 126608' PRINT *," ENTER INITIAL APHIDS(1-2,3-4,AD-AL)..." 126808 READ*,(APHIN(I),I81,3) 127008C ~ 127208201 INYDIS82 127408 IADDIS83 128408C 128608C FIRST SET ALL TO ZERO 128808 DO 2 I81,20 1290082 RNY(I)80. 129208 DO 3 I81,18 1294083 AA(I)=0. 129608 XNY(1)=XNY(2)80. 129808C 130008C*** NYMPHS 13020=C PUT IN BEGINNING OF NYMPH STAGE 130408 IF(INYDIS.NE.1)GO TO 20 130608 RNY(l)=APHIN(1)*K/DEL 130808 RNY(ISUB12+1)=APHIN(2)*K/DEL 131008 GO TO 50 13120820 CONTINUE 131408C 131608C 131808 132008 132208 13240830 132608 132808 13300831 133208C 133408C*** 133608C 13380850 134008 134208 134408 13460825 134808C 135008C 135208 135408 135608 13580841 136008 13620840 136408C 136608C 136808 137008 13720860 13740870 1376O8C 149 DISTRIBUTE EVENLY APHIN(1)8APHIN(1)/ISUBlZ*K/DEL APHIN(Z)8APHIN(2)/(20.-ISU312)*K/DEL DO 30 ISUB81,ISUB12 RNY(ISUB)8APHIN(1) IIN8ISUB12+1 DO 31 ISUB8IIN,20 RNY(ISUB)8APHIN(2) ADULTS PUT IN BEGINNING OF ADULT STAGE CONTINUE IF(IADDIS.NE.1)GO TO 25 AA(1)=APHIN(3) GO To 70 CONTINUE PUT IN FRONT END OF ADULT STAGE IF(IADDIS.NE.2)GO TO 40 APHIN(3)=APHIN(3)/5. DO 41 ISUB81,5 AA(ISUB)=APHIN(3) GO TO 70 CONTINUE DISTRIBUTE EVENLY APHIN(3)=APHIN(3)/18. DO 60 ISUB81,18 AA(ISUB)8APHIN(3) CONTINUE 137808C*****CECID SECTION 138008C 138208C 138408 13860890 138808 13900801 139208C 139408100 139508 139558 139608 140208 140308 140408 140608105 140808 140908120 141208C 141808 142008 OK- FIRST SET ALL TO ZERO DO 90 181,9 CEGG(I)=0. DO 91 I81,33 CLARV(I)=0. PRINT*," ENTER CEC- IMORE,ISTAGE,ISUB,IAMT-" READ*,IMORE,IST,ISUB,AMT IF(IMORE.EQ.2)GO TO 120 IF(IST.EQ.2)GO TO 105 CEGG(ISUB)=AMT IF(IMORE.EQ.0)GO TO 120 GO TO 100 CLARV(ISUB)=AMT IF(IMORE.EQ.1) GO TO 100 CONTINUE RETURN END 150 9020=C******************************************************* 90408 SUBROUTINE CONVERT 9050=C******************************************************* 90808C 91008 COMMON /ALL/RNY(20),K,DEL,XNY(2),AP(3), 91208 +APTOT,ISTART,TOTHU(4),ITIMIN,AA(18),CSTART,APDIE 91408 +CEGG(9),CLARV(33),CTEGG,CTLARV(3),CTPUP,TCEC, 91508 +TAPKLD,TBORN 91608C - 92208C*****APHID SECTION 92408 AP(1)8AP(2)80. 92608 DO 10 ISUB81,6 9280810 AP(1)8AP(1)+RNY(ISUB) 93008 AP(1)8AP(1)*DEL/K 93208C 93408 DO 20 ISUB87,20 9360820 AP(2)8AP(2)+RNY(ISUB) 93808 AP(2)8AP(2)*DEL/K‘ 94008C 94208 AP(3)=0. 94408 DO 30 ISUB81,18 9460830 AP(3)=AP(3)+AA(ISUB) 94808C 95008 APTOT8AP(1)+AP(2)+AP(3) 95208C 95408C*****CECID SECTION 95608 CTEGG80. 95808 DO 40 181,9 9600840 CTEGG8CTEGG+CEGG(I) 96208C 96408 DO 45 I81,3 9660845 CTLARV(I)80. 96808 DO 46 I8l,7 9700846 CTLARV(1)8CTLARV(1)+CLARV(I) 97208 DO 57 188,20 9740847 CTLARV(2)=CTLARV(2)+CLARV(I) 97608 DO 48 I821,33 9780848 CTLARV(3)8CTLARV(3)+CLARV(I) 98008C 98108. TCEC8CTEGG+CTLARV(1)+CTLARV(2)+CTLARV(3)+CTPUP 9811=C 98608 RETURN 98808 END 99008C 151 9920=C******************************************************* 99408 SUBROUTINE OUTPT(IMNTH,IDAY,ITIM) 9960=C******************************************************* 9980=C 100008 100208 100408 100508 100608C 100908 100958 101008 101058C 101208 101258 10130=1 101358 101408 1014582 101508 1015584 1016085 101618 -10165810 101708C 101958 10200820 102508C 105008 105208 105408C COMMON /ALL/RNY(20),K,DEL,XNY(2),AP(3), +APTOT,ISTART,TOTHU(4),ITIMIN,AA(18),CSTART,APDIE, +CEGG(9),CLARV(33),CTEGG,CTLARV(3),CTPUP,TCEC, +TAPKLD,TBORN TIMDY8”E". IF(ITIM.EQ.0)TIMDY8"M" IF(ITIM.EQ.1)TIMDY8"N" IF(ISTART.NE.1)GO To 4 PRINT 1 FORMAT(/,7X,"TOTHU(1)",4X,"1-2",9X,"3-4", +7X,"ADULTS",6X,"TOTAL",7X,"TOT CEC") PRINT 2 - FORMAT(7X,"TOTHU(3)",4X,"EGGS",7X,"LARV1", +6x,"LARv2",7x,"LARV3",7x,"PUPAE",/) CONTINUE , PRINT 10,IMNTH,IDAY,TIMDY,TOTHU(1), +(AP(I),I=1,3),APTOT,TCEC FORMAT(1X,IZ,"/",IZ,A1,F6.1,5E12.5) PRINT 20,TOTHU(3),CTEGG,(CTLARV(I),I81,3),CTPUP FORMAT(7X,F6.1,5E12.5) RETURN END 152 C. FIELD TEMPERATURE DATA Hygrothermograph temperature records (daily maximum and minimums) taken by this author are reported in this section for field research sites at the Klein Orchard and the MSU Graham Horticultural Research Station (see Section II-B-l for description of sites, Section II-A-3 for hygrothermograph methods). Hygrothermographs (except for the sleeve cage hygrothermograph) were enclosed in white painted shelters (the bases were built with metal screening to expose the hygrothermographs to the air) placed on posts approximately 1.5 m. above the ground. The hygrothermograph used to monitor conditions inside the sleeve cages was placed (without the shelter) on a post 1.5 m. above the ground midway between the trunk and drip line of an apple tree. Three apple terminals together with the hygrothermograph were enclosed inside a specially con- structed oversized sleeve cage secured at the base of the terminals with a string (see Section II-B-3 for description of sleeve cages). A comparison of temperatures for the sheltered hygro- thermograph vs. the sleeve cage enclosed hygrothermograph showed that daily maximums and minimums were elevated inside the sleeves by 2.56 i 1.56 (mean 3 standard deviation, range 4. -l to 9, n=51) and .29 - .94°F. (range -2 to 2, n=51) respectively. 153 TABLE 36. Field Temperature Data A. Temperature Data for Klein's Orchard 19791 Temperature Record (OF.)2 53 59 62 64 70 56 64 71 62 62 50 56 42 50 42 38 30 32 33 40 53 34 36 47 56 42 35 34 24 36 65 68 78 70 69 62 65 65 56 66 62 60 63 75 62 76 33 43 55 57 39 42 36 50 44 41 42 44 46 36 48 53 84 71 71 79 80 80 72 62 67 56 72 74 76 73 76 84 77 81 81 82 84 85 86 73 70 75 79 77 78 76 75 60 56 48 48 49 54 56 62 64 66 53 51 61 49 52 64 83 77 78 80 83 83 84 86 78 76 79 83 81 83 83 83 59 52 47 52 53 55 61 63 69 70 S7 58 65 55 65 65 1Data for 7/11-8/13 and the maximum for 7/10 were obtained from the Peach Ridge recording station (near Sparta,MIL 2The first two numbers in each row are the month (eg. 3=March) and the maximum (=1) or minimum (=2). 154 TABLE 36. (cont.) B. Temperature 42 24 46 24 65 39 70 44 82 66 72 51 37 43 19 24 62 50 42 23 70 58 41 53 72 70 52 42 80 80 58 64 77 67 62 63 75 64 Data for Klein's Orchard 19803 Temperature Record (OF.) 37 43 20 25 44 64 38 38 79 64 47 50 72 76 55 57 82 79 48 59 82 79 59 64 79 52 37 43 20 25 48 65 36 47 80 72 47 50 73 60 47 57 77 85 58 70 82 84 54 56 83 61 38 44 20 26 58 75 36 40 78 73 55 49 69 73 50 80 90 64 70 77 86 66 68 78 55 38 44 21 26 65 69 38 44 66 43 43 74 75 59 52 76 73 53 68 81 79 65 72 79 59 38 45 21 26 60 79 48 54 50 82 36 45 75 80 59 60 85 78 58 64 82 81 67 62 78 56 39 46 21 27 58 56 50 40 48 80 36 50 60 85 43 61 84 78 70 56 80 67 54 88 58 39 46 22 27 40 40 36 28 55 79 35 62 63 85 51 64 80 78 60 52 83 81 67 54 39 47 22 27 36 50 33 30 64 77 42 58 58 84 37 66 84 81 57 64 71 74 64 63 40 47 22 28 41 54 35 36 62 75 50 44 68 84 34 88 68 63 66 72 83 60 65 40 48 23 28 41 52 34 42 68 76 45 46 74 77 42 61 80 72 68 65 79 84 56 64 41 48 23 29 44 52 27 57 78 49 52 77 81 57 56 83 80 60 66 69 82 52 67 41 49 23 29 34 53 32 43 57 75 37 .60 78 73 62 63 89 80 64 63 81 84 67 65 42 49 24 29 40 56 30 61 76 40 61 62 71 59 55 83' 75 72 55 78 78 57 66 3Data for March are Normals from the Peach Ridge Data from 8/09 to 8/13 and 8/14 minimum are also from this station. recording station (near Sparta, MI). 44 30 72 59 82 66 70 66 155 TABLE 36. (cont.) C. Temperature 42 24 43 21 66 41 65 41 83 67 70 48 37 43 19 24 56 51 38 20 71 58 41 52 ‘75 68 52 37 80 80 59 62 78 65 62 59 75 65 Data for Graham Station 19804 Temperature Record (OF.) 37 43 20 25 41 63 35 34 89 73 42 50 70 73 59 50 82 79 45 57 80 77 60 62 80 52 37 43 20 25 44 76 32 38 84 72 43 49 71 62 47 56 74 87 54 66 85 84 54 53 84 62 4Data for March 38 44 20 26 52 79 30 38 89 75 51 50 70 71 50 42 79 92 64 72 78 87 67 66 79 52 are Graham Station Normals. 38 44 21 26 62 71 38 43 67 80 39 42 78 76 60 46 75 76 51 68 83 80 62 71 78 56 38 45 21 26 60 83 47 56 51 82 36 42 75 80 50 43 86 79 56 65 83 79 67 59 78 55 39 46 21 27 60 58 52 41 51 80 37 48 64 85 42 58 84 79 70 55 82 81 67 51 85 56 39 46 22 27 39 38 36 28 51 78 37 62 64 85 48 60 80 79 59 52 80 80 63 52 39 47 22 27 35 49 32 30 55 75 32 54 58 85 32 63 84 82 55 56 72 76 66 60 40 47 22 28 41 53 34 31 67 77 40 42 67 85 31 63 86 69 61 66 71 84 64 61 40 48 23 28 41 56 33 42 69 76' 46 44 77 78 40 60 78 73 65 64 75 85 58 63 41 48 23 29 44 56 26 40 59 82 50 80 80 55 57 83 79 59 65 68 87 50 68 41 49’ 23 29 36 54 31 44 58 78 36 60 79 75 62 59 89 80 63 58 82 87 63 67 42 49 24 29 39 57 30 45 63 88 36 58 62 71 60 52 85 75 72 52 75 80 54 66 40 30 72 59 85 65 71 64 156 TABLE 36. (cont.) D. Temperature Data for Graham Station Sleeve Cages 19805 Temperature Record (OF.) 71--------------88 86 83 80 89 93 75 82 86 88 87 71 73 81 83 77 87 72--------------71 66 62 57 66 72 67 65 55 52 58 66 65 65 58 53 65 8 1 87 77 84 89 79 85 84 85 86 74 74 80 70 82 79 74 66 82 86 87 82 82 83 85 77 87 88 90 90 84 73 8 2 65 63 60 53 65 61 66 67 64 67 64 58 52 64 56 49 60 62 54 66 71 59 51 52 61 62 63 67 68 68 66 5Readings for July start on 7/15. 157 D. SPRAY RECORDS FOR GRAHAM STATION 1980 Sprays were applied using a Bean 447 air-blast sprayer. Amounts are lbs./lOO gallons (dilute) with approximately 350 gallons applied per acre. A - D are four fungicide treatments for Block 12 (see orchard map in Section II-B-l-b.) with applications applied on both sides of a treatment row and outside of both guard rows (see diagram below). Table 37 lists spray-applications and dates. CGA 64251 is an experimental fungicide similar to.BAYCOR. The C treat- ment on August 4 was accidently made at a double rate of l 1b./100 gal. guthion (azinphosmethyl). Guard row 1 Treatment row :1: Guard row i Treatment row 1 158 TABLE 37. Spray Records for Graham Station 1980 Treatment Rate Date Block(s) Row(s)l Compound (/100 gal. dilute) 4/22 All All Cyprex %# All All Oil 2 gal. 4/29 10-12 A Dikar 2# 10-12 B CGA64251 2.5 oz. 10-12 C Captan 2# 10-12 D Baycor 6 oz. Rest All Cyprex %# 5/6 All All Thiodan SOWP 1# All All 'Fungicides as 4/29 5/14 10-12 A-C Fungicides as 4/29 10-12 D Baycor 4 oz. Rest All Fungicides as 4/29 6/4 All All Fungicides as 5/14 6/11 A11 A11 Guthion SOWP 8# 10-12 A Dikar 1%# 10-12 B CGA64251 2.5 oz. 10-12 C Captan 1%# 10-12 D Baycor 2.5 oz. Rest All Cyprex 3/8# 6/25 All All Guthion SOWP %# 10-12 A-C Fungicides as 6/11 10-12 D Baycor 4 oz. 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