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Predaceous arthropods of the sweetpotato whitefly, Bemisia tabaci (Gennadius), on tomatoes in Florida

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Title:
Predaceous arthropods of the sweetpotato whitefly, Bemisia tabaci (Gennadius), on tomatoes in Florida
Creator:
Dean, David Ed, 1947-
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Language:
English
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xvi, 231 leaves : ill., photos ; 29 cm.

Subjects

Subjects / Keywords:
Eggs ( jstor )
Instars ( jstor )
Lacewings ( jstor )
Larvae ( jstor )
Natural enemies ( jstor )
Pests ( jstor )
Predation ( jstor )
Predators ( jstor )
Species ( jstor )
Tomatoes ( jstor )
Dissertations, Academic -- Entomology and Nematology -- UF
Entomology and Nematology thesis Ph.D ( lcsh )
City of Gainesville ( local )
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bibliography ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1994.
Bibliography:
Includes bibliographical references (leaves 201-229).
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by David Ed Dean.

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PREDACEOUS ARTHROPODS OF THE SWEETPOTATO WHITEFLY,
BEMISIA TABACI (GENNADIUS), ON
TOMATOES IN FLORIDA
















BY

DAVID ED DEAN


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY



UNIVERSITY OF FLORIDA

1994















ACKNOWLEDGMENTS


Much of the time and effort that went into this program was contributed by someone other than myself. Unfortunately, space will not permit an exhaustive list. Certainly a large commitment has come from my major advisor, Dr. D. J. Schuster. Among other things, he has been a generous and patient mentor, a constant encouragement, a good example, a great fishing guide, and a trusted friend. I am fortunate to have had the opportunity to know him.

My time spent on coursework in Gainesville was directed by Dr. C. S. Barfield who has served as cochairman on the advisory committee. Like Dr. Schuster, he also has taken an interest in my personal welfare, as well as my academic preparation. Along with good academic counsel, he gave me full access to his laboratory and office space while on campus. I benefited from his instruction in the classroom and had the opportunity to assist him with two international IPM courses. I am grateful for the opportunity to know him as an instructor and friend.

Dr. F. D. Bennett served on my committee until his

retirement in 1993. He was a great encouragement and source of valuable information on biological control. It was a privilege to have had the opportunity to know him and draw









from his experience in the field. Dr. J. B. Jones generously gave me bench space and access to equipment in his laboratory. Upon Dr. Bennett's retirement, Dr. Jones agreed to fill his place on the committee. I am very grateful for his generosity and for his counsel concerning antibody techniques. Dr. L. S. Osborne has been a source of information concerning biological control of whiteflies and was a major influence in the decision to investigate the predation of whiteflies. Dr. J. A. Bartz has always encouraged me and given a good balance to all the entomologists on the committee. I want to thank each of these individuals for the time invested in committee meetings and reading of manuscripts.

Dr. J. E. Polston has also donated laboratory space and Dr. G. M. Danyluck gave direction for electrophoresis and protein work. Dr. J. H. Frank gave many hours to personally tutor me through his course in biological control. Dr. J. R. McLaughlin loaned a 'D vac' for insect sampling. Dr. R. D. Oetting sent greenhouse whiteflies. Dr. P. J. Walgenbach sent potato aphids. Dr. D. G. Boucias assisted in the concentration and quantification of whitefly protein.

Identification of insects important to this study was provided by Drs. T. J. Henry (Hemiptera), R. D. Gordon (Coccinellidae), R. J. Gagn6 and N. E. Woodley (Diptera) of the Systematic Entomology Laboratory, Agriculture Research Service, USDA and by Drs. M. C. Thomas (Coleoptera) and L. A. Stange of the Entomology Section of the Division of Plant


iii









Industries, Florida Department of Agriculture. Dr. J. H. Frank, University of Florida, identified the staphylinids.

Mr. M. Maedgen of Biofac insectary in Mathis, TX has generously supplied the green lacewings for this research. Mr. Fred Adams of the USDA insectaries in Gainesville gave me noctuid larvae and eggs for rearing lacewings. Mr. C. Liewald gave 30 hibiscus plants for rearing whiteflies. B. Mr. S. Wood assisted me faithfully as a part-time technician for two years. Mrs. L. Green was a tremendous help at the hybridoma lab. Mrs. M. Litchfield helped with long distance registration and department records each semester. To each of these individuals mentioned, I would like to express my sincere gratitude for their selfless generosity.

Lastly, my family has sacrificed time and finances

during the time I have spent in graduate school. They have endured two moves, spent countless hours waiting for me while I checked on experiments at night and weekends, helped me find articles in the library, moved insect traps, and brought me 'neat bugs'. My wife has had to keep me going many times, proof papers, remind me of deadlines and important dates, and pay most of the bills. Words alone are inadequate to express what their support has meant to me. So, I will just have to make some time to demonstrate my gratefulness.















TABLE OF CONTENTS

page
ACKNOWLEDGMENTS ........................................... ii

TABLE OF CONTENTS .........................................v

LIST OF TABLES ............................................viii

LIST OF FIGURES ........................................... x

ABSTRACT .................................................. xiv

CHAPTER I. INTRODUCTION AND LITERATURE REVIEW ............ 1

Introduction .........................................1
Literature Review .................................... 3
History of The Sweetpotato Whitefly ............. 3
Whiteflies ......................................5
Biological Control of Whiteflies ................ 6
Natural enemies ............................ 6
Predators of whiteflies. .................... 9
Predation and Prey Populations .................. 10
Models of predation ........................ 13
Population regulation and predators ........ 15
Sampling Predators .............................. 18
Evaluation of Predation ......................... 19
Prey preference ............................ 20
Prey suitability for development ........... 22
Detecting Predation in the Field. ................24
Augmentation of Predators .......................25
The Use of Chemicals to Manipulate Predators .... 26
Attractants and predators. .................. 27
Screening Predators for Pesticide Tolerance ..... 28

CHAPTER II. PREDATION OF THE SWEETPOTATO WHITEFLY ON FIELD TOMATOES ............................................54

Introduction .........................................54
Methods and Procedures ...............................56
Statistical Treatment ........................... 63
Results and Discussion ............................... 64
Predator Survey ................................. 64
Archnida ................................... 68
Insecta .................................... 70










Population Dynamics ...........................
Conclusions ........................................


.. 83
.. 129


CHAPTER III. PREY PREFERENCE AND SUITABILITY OF PREY FOR GREEN LACEWINGS ....................................... 132


Introduction ........................
Materials and Methods ...............
Preference .....................
Preference models .........
Prey Suitability ...............
Development and Mortality.
Fecundity .................
Maximum consumption.......
Statistical analysis ...........
Preference ................
Prey suitability ..........
Results .............................
Preference .....................
Prey Handling .............
Prey Suitability ...............
Development ...............
Mortality .................
Fecundity .................
Maximum consumption....... Conclusion and Discussion ...........


132 134 134 135 137 137 137 138 138 138 139 140 140 145 148 148 150 151 151 151


CHAPTER IV. ATTRACTION AND ARRESTMENT OF ADULT LACEWINGS .......................................


Introduction ..................................
Materials and Methods ....................
Olfactometer .............................
Attractant Bioassays ................
Statistical Analysis for Olfactomete
Field trials .............................
Sampling method .....................
Statistical analysis of Field Data.. Results .......................................
Olfactometer assays ......................
Field Trials .............................
Lacewing attraction and oviposition.
Effects of Attractant on Other
Arthropods ..........................
Conclusion and Discussion .....................


.......... 158


....... 158
....... 160
....... 160
....... 162
r...... 163
....... 164
....... 165
....... 168
....... 169
....... 169
....... 172
....... 172

....... 177
....... 182


r










CHAPTER V. SUMMARY AND CONCLUSIONS ....................... 184

Introduction ......................................... 184
General Discussion ................................... 185
Predator Survey ................................. 185
Predator Manipulation ........................... 187
Attractants ................................ 196
Introduced Predators ............................ 199

REFERENCES ................................................ 201

BIOGRAPHICAL SKETCH .......................................230


vii















LIST OF TABLES


Table page

1.1. Predators of Whiteflies ............................ 30

2.1. Predaceous arthropods observed feeding on
Bemisia tabaci in the laboratory or field .......... 65

2.2. Seasonal incidence of orders of arthropods and
related prey collected with the whitefly, Bemisia tabaci, on unsprayed tomatoes in
Bradenton, FL . .....................................89

2.3. Seasonal abundance of selected predator taxa
collected during the survey of the fauna
associated with Bemisia tabaci on unsprayed
tomatoes in Bradenton, FL . .........................96

2.4. Correlation coefficients (r2) for combinations of
prevalent whitefly (WF) predators and the
whitefly predator complex with alternative prey
present on insecticide free tomatoes at
Bradenton, FL . ....................................125

2.5. Association coefficients for various whitefly
(WF) predators and common prey found on
unsprayed tomatoes in Bradenton, FL . ..............127

3.1. Means (�SE) of prey consumption by larvae of two
lacewing species at a standard density of 30
prey and a standard time of 30 minutes . ...........141

3.2. Relative preference of each larval instar of _.
cubana (Cc) and -. rufilabris (Cr) larvae for M.
euphorbiae and nymphs of a. tabaci ................ 143

3.3. Development of -. rufilabris and _. cubana, on
three different prey diets consisting of M.
euphorbiae, and B. tabaci alone and combined
(A/W) . ............................................149


viii









4.1. Responses of the lacewings, Q. r1filgris (Cr)
and -. cubana (Cc) to various compounds and
products in an olfactometer in the laboratory. ....170

4.2. Mean number of arthropods collected in vacuum
samples taken from tomato plots sprayed with an artificial honeydew and unsprayed control plots,
spring 1992 . ......................................178

4.3. Mean number of arthropods collected in vacuum
samples taken from tomato plots sprayed with an artificial honeydew and unsprayed control plots,
fall 1992 . ........................................179

4.4 Mean number of arthropods collected in vacuum
samples taken from squash plots sprayed with an
artificial honeydew and from unsprayed control
plots, summer 1993 . ...............................180















LIST OF FIGURES


Figure page

2.1. Cylindrical drop trap ..............................59

2.2. Collection of arthropods ...........................60

2.3. Mechanical timer ...................................61

2.4. Mean number of whitefly adults per plant and
immature lifestages per leaf sample, on
unsprayed tomatoes at Bradenton, FL, fall 1991 .....84

2.5. Mean number of whitefly adults per plant and
immature lifestages per cm2 leaf sample, on unsprayed tomatoes at Bradenton, FL, spring
1992 ...............................................85

2.6. Mean number of whitefly adults per tomato plant
and immature lifestages per cm2 leaf sample, on
unsprayed tomatoes at Bradenton, FL, fall 1992 .....86

2.7. Mean number of whitefly adults per plant and
immature lifestages per cm2 leaf sample, on unsprayed tomatoes at Bradenton, FL, spring
1993 ...............................................87

2.8. Mean plant height, mean number of predators of
the immature lifestages of the whitefly, mean number of B. tabaci nymphs and eggs per cm2 of leaf, and mean number of spiders on unsprayed
tomatoes at Bradenton, Fl, spring 1992 . ............92

2.9. Mean plant height, mean number of predators of
the immature lifestages of the whitefly, mean number of B. tabaci nymphs and eggs per cm2 of leaf, and mean number of spiders on unsprayed
tomatoes at Bradenton, Fl, fall 1992 . ..............93

2.10. Mean plant height, mean number of predators of
the immature lifestages of the whitefly, mean number of B. tabaci nymphs and eggs per cm2 of









leaf, and mean number of spiders on unsprayed
tomatoes at Bradenton, Fl, spring 1993 . ............94

2.11. Mean numbers of Orius insidiosus and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1991 . ..........................99

2.12. Mean numbers of Ceraeochrysa cubana and selected
alternative prey on tomatoes at Bradenton, FL,
fall 1991 . ........................................100

2.13. Mean numbers of Ge~cis punctiZpes and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1991 . .........................101

2.14. Mean numbers of Orius insidiosus and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1992 . .......................102

2.15. Mean numbers of Ceraeochrysa cubana and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1992 . .......................103

2.16. Mean numbers of Geo coris unctie and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1992 . .......................104

2.17. Mean numbers of hemerobiid larvae and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1992 . .......................105

2.18. Mean numbers of coccinellid larvae and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1992 . .......................106

2.19. Mean numbers of Orius insidiosus and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1992 . .........................107

2.20. Mean numbers of Ceraeochrysa cubana and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1992 . .........................108

2.21. Mean numbers of Cardiastethus assimilis and
selected alternative prey on unsprayed tomatoes
at Bradenton, FL, fall 1992 . ......................109









2.22. Mean numbers of LChrysoperla externa and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1992 . .........................110

2.23. Mean numbers of coccinellid larvae and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, fall 1992 . .........................111

2.24. Mean numbers of Orius insidiosus and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1993 . .......................112

2.25. Mean numbers of Ceraeochrysa cubana and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1993 . .......................113

2.26. Mean numbers of Geocoris punctipes and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1993 . .......................114

2.27. Mean numbers of Cardiastethus assimilis and
selected alternative prey on unsprayed tomatoes
at Bradenton, FL, spring 1993 . ....................115

2.28. Mean numbers of hemerobiid larvae and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1993 . .......................116

2.29. Mean numbers of coccinellid larvae and selected
alternative prey on unsprayed tomatoes at
Bradenton, FL, spring 1993 . .......................117

2.30. Mean numbers of Q. insidiosus and Thysanoptera
per tomato plant, spring 1992.(N=6) data
transformed log(10(Y+1)) and Log Log (10Y)
respectively ......................................119

2.31. Mean numbers of Q. insidious and adult
whiteflies per tomato plant, spring 1992.(N=6)
data transformed log(10(Y+1)) ..................... 120

3.1. The mean number of prey consumed at each instar
by larvae of -. cubana (Cc) and -. rufilabris
(Cr) in a mixed prey environment (with �SE) and
one half of the mean number consumed in the
single prey tests (without �SE). All
observations were conducted at a standard
density of 30 prey for 30 minutes . ................142


xii









3.2. Mean (�SE) of the probability of selection of M.
euphorbiae vs a. tabaci nymphs by each larval
instar of C. cubana (Cc) and -. rufilabris (Cr)
(N=16) (Manly 1972) . ..............................146

3.3. Percentage of time spent handling prey for each
instar of -. cubana (Cc) and _. rufilabris (Cr)
in a mixed prey environment of M. euphorbiae and
B. tabaci nymphs at a standard density of 30
prey for 30 minutes (N=16) . .......................147

3.4. Mean (�SE) maximum prey consumed by third instar
larvae of C. rufilabris and _. cubana of M.
euphorbiae and nymphs of the whitefly B. tabaci
(N=8) ............................................152

4.1. Vacuum sampler ....................................167

4.2. The mean (�SE) number of oviposition sites and
eggs of lacewings in tomato plots sprayed with an artificial honeydew and in unsprayed plots,
spring 1992 . ......................................173

4.3 The mean (�SE) number of oviposition sites and
eggs of lacewings in tomato plots sprayed with an artificial honeydew and in unsprayed plots,
fall 1992 . ........................................174

4.4. Mean (�SE) number of oviposition sites and eggs
of lacewings in squash plots sprayed with
artificial honeydew and in unsprayed plots,
summer 1993 . ......................................175

5.1. The exponential relationship of leaf area to
plant height in the phenology of tomato cv
'Duke', at Bradenton, FL, 1983 (from Marlowe et
al. 1983) . ........................................191

5.2. Mean number of adult whiteflies per tomato plant
and mean plant height (cm), spring 1992 (N=6). ....192

5.3. Mean number of adult whiteflies per tomato plant
and mean plant height (cm), spring 1993 (N=6). ....193

5.4. Mean number of adult whiteflies on tomato plants
fall 1991 (N=6) . ..................................194

5.5. Mean number of adult whiteflies per tomato plant
and mean plant height (cm), fall 1992 (N=6) . ......195


xiii















Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy


PREDACEOUS ARTHROPODS OF THE SWEETPOTATO WHITEFLY,
BEMISIA TABACI (GENNADIUS), ON TOMATOES IN FLORIDA

By

David Ed Dean

August, 1994




Chairman: Dr. D. J. Schuster Co-chairman: Dr. C. S. Barfield Major Department: Entomology and Nematology


Field and laboratory studies were undertaken to

ascertain the extent of arthropod predation of Bemisia tabaci (Gennadius) (recently transferred to the new species, B. argentifolii Bellows & Perring) on tomatoes in Florida. The suitability of the whitefly as prey and olfactory response to attractants and food supplements were investigated for selected predators.

Observations made in the laboratory and in the field

revealed that a least 19 species of arthropods feed on one or more lifestages of D. tabaci. Field populations of the whitefly and predaceous arthropods were monitored for two years on tomatoes using a whole plant sampling method. An


xiv









anthocorid, Orius insidiosus (Say), and a chrysopid, Ceraeochrysa cubana (Hagen), were found to be the most abundant predators. The suitability of an alternative prey, the potato aphid, Macrosiphum euphorbiae (Thomas), for the commercially available lacewing, ChrysoperI rufilabris Burmeister, and the native lacewing, Q. cubana, were tested. Both predator species were able to complete normal development on whiteflies alone. 2. cubana larvae preferred B. tabaci over M. euphorbiae in two different models for testing preference. -. rufilabris preferred the aphid in the third instar in only one of the two preference models.

The adult stage of the two lacewing species also were

tested in the laboratory for attraction to various compounds and products with an olfactometer. Of the compounds tested, an 'artificial honeydew' and L-tryptophane were found to be highly attractive to -. rufilabris, but less attractive to �. cubana. The 'artificial honeydew' also was tested in the field for increasing the presence and oviposition of chrysopids on tomatoes and squash in the field. _. cubana oviposited more on tomatoes sprayed with the 'artificial honeydew' although significant effects were difficult to detect.

Although various predator species appear to be

responding to the abundance of whiteflies in the field, the populations of this pest currently are not being regulated by predators. Continued studies are needed to investigate ways to manipulate predator populations such that they synchronize









with whitefly populations. Introduction of exotic predators or augmentation of endemic ones should be investigated.














CHAPTER I
INTRODUCTION AND LITERATURE REVIEW


Introduction


In 1986, greenhouses in Central Florida began experiencing a dramatic increase in populations of whiteflies. These whitefly populations were much larger than had been experienced previously and they did not respond to control measures. The new pest was identified as the "sweetpotato whitefly", Bemisia tabaci (Gennadius), although it had not been considered a serious pest in Florida before this time. The spread of this whitefly among poinsettia nurseries was so rapid and widespread that it could not be contained. By the following season, this aggressive whitefly pest had spread out-of-doors and was attacking field tomatoes in Central Florida. In the ten years since the initial outbreak, the sweetpotato whitefly has become a major pest responsible for multimillion dollar losses each year across the southern United States from Florida to California.

The advancement of the sweetpotato whitefly to this new elevated pest status has resulted in an effort to gain information about its biology and factors leading toward a reduction in agricultural losses. For many years this polyphagous whitefly was known by various synonyms around the









world because of morphological differences that are associated with development on different host plants and not true genetic differences. However, researchers have recently proposed that the whitefly responsible for the current outbreak is the new species, a. argentifolii Bellows & Perring (Bellows et al. 1994). This proposal is made on the basis of numerous dissimilarities between the organism known before the 1986 outbreak and the current whitefly pest. In view of the sudden and extensive damage done by this new pest, there can be no argument that the feeding behavior and reproductive potential are very different from the whitefly present in Florida before 1986. While those disposed to systematics vascillate over the nomenclature of this new pest-race, biotype, strain, or species,--much is still not known about the biology and ecology of this new pest. For the remainder of this paper and until there is greater consensus as to the taxonomic status of this new whitefly pest it shall be refered to as the "sweetpotato whitefly", E. tabaci.

The focus of this research has been to determine what

naturally occurring predaceous arthropods attack a. tabaci in Florida and to derive possible strategies for manipulating them for more effective reduction of whitefly populations. Information of the endemic predaceous enemies of whiteflies in Florida is limited primarily to citrus pests. A knowledge of the native predaceous fauna associated with whiteflies on vegetable crops is necessary for attempting to discover









methods to enhance predation in the field. Therefore, it was decided that a faunal survey on horticulture crops was an essential prerequisite. In addition, preliminary investigations of some possible biological control agents of the whitefly were done in conjunction with the field survey. Prey preference and olfactory response of two lacewing species, Chrysoperla rufilabris (Burmeister) and Ceraeochrysa cubana (Hagen) were studied. !. rufilabris is available as a commercial biological control agent and it was observed that

-. cubana was frequently associated with whiteflies on tomatoes in the field.


Literature Review



History of The Sweetpotato Whitefly


The whitefly outbreak that occurred in the Florida greenhouse industry in 1986 and in field tomatoes the following year has resulted in an importance pest for Florida agriculture (Schuster & Price 1987). First reported in Florida by Quaintence (1900), the sweetpotato whitefly, Bemisia tabaci (Gennadius), was not a pest until the recent outbreak. Watson (1914), reported that Aleuro tabaci (a. tabaci) occasionally attack tomatoes in Florida. Some controversy has existed over the taxonomic status of the species currently causing extensive damage in the southern US (Perring et al. 1993a, 1993b, Gawel & Bartlett 1993, Campbell 1993, Costa et al. 1993, Costa & Brown 1991).









The whitefly problem in Florida is compounded by the association of large populations with several new viral diseases (Kring et al. 1991), as well as, fruit and plant disorders of unknown etiology (Schuster et al. 1990, 1991, Brown & Costa 1992). The "sweetpotato whitefly" is a vector of new plant viruses that can cause severe damage to horticultural crops throughout Florida and the Caribbean region (Brown & Nelson 1988, Brown & Poulos 1990; Brown et al. 1990, Brown & Bird 1992).

Subsequent outbreaks of this whitefly pest have caused widespread losses in the southwestern US (Perring et al. 1991, Cohen et al. 1992, Perring et al. 1993) and elsewhere in the Caribbean (D. J. Schuster, personal communication). The "sweetpotato whitefly" has long been a serious pest in other parts of the world, particularly where cotton is grown. The quantity of insecticides used on cotton is implicated as the cause of whitefly outbreaks in such places as the Sudan (Eveleens 1983) and Turkey (Stam & Tune 1983). According to Stam and Elmosa (1990), the interference of natural enemies by pesticide use has contributed to whitefly outbreaks in these areas. Heavy pesticide use associated with the production of cotton also has resulted in the development of resistance in many whitefly populations (Abdeldaffie et al. 1987, Prabhaker et al. 1985).














Whiteflies are considered to be tropical pests and have been referred to as "the aphids of the tropics" (Mound & Halsey 1978). They can cause plant damage by rapidly developing large populations that siphon sap from plant tissue and excrete the extracted liquid in the form of honeydew. This sugary material is deposited on the leaves of plants where the carbohydrates provide an excellent medium for formation of sooty mold that, in turn, can reduce plant photosynthesis (Lopez-Avila 1986b).

Of the more than 1156 species of whiteflies, only a relatively few are economically important (Mound & Halsey 1978). Only four species are serious pests of annual field and vegetable crops (Byrne et al, 1990): Aleurodes proletella

(L.), Trialeurodes abutilonea (Haldeman), Trialeurodes vaporariorum Westwood, and B. tabaci. Traits common to most of the whiteflies just mentioned are polyphagy and high rates of reproduction.

Direct feeding damage can be detrimental to certain

crops, such as cucurbits. However, disease transmission is the greatest threat. Although a single whitefly is not as efficient as a vector of a virus as a winged aphid, the larger numbers of whiteflies can more than compensate, making them a serious vector (J. A. Bartz, personal communication). D. tabaci is the most important whitefly









vector (Mound & Halsey 1978), vectoring 25 or more viral diseases (Costa 1976) and able to transmit more than one virus simultaneously (Varma 1963). B. tabaci has been discovered to be the only whitefly vector of geminiviruses (Duffus 1987).


Biological Control of Whiteflies


Natural enemies

The natural enemies which are important to biological control can be placed into three catagories: pathogens, parasites, and predators. Viruses, bacteria, fungi, protozoa, and nematodes can be important pathogens in the regulation of insect numbers. Parasites (parasitoids) of insects are smaller than their host and parasitic in the immature stages, developing within or on a single host. Predators are usually larger than their host. Most often the predator is carnivorious in the immature and adult stage, feeding on many hosts during the course of its development (van den Bosh et al. 1982). There are examples from each of these groups which have exhibited various degrees of success in controling whitefly populations. Various fungi attack whiteflies. Early uses of Aegerita, Aschersonia, and Fusarium were made against whiteflies found on citrus in Florida (Watson, 1914). A strain of Paecilomyces fumosoroseus found in Florida has been released against E. tabaci (Osborne et al. 1990) and is proving effective in greenhouses.









Gerling (1990) reviewed the natural enemies of

whiteflies. Among the parasitoids listed, three families of Hymenoptera containing six genera are known to attack whiteflies. These are Amitus from the family Platygasteridae, Azotus, Cales, Encarsia, and Eretmocerus from the family Aphelinidae, and Euderomphale from the family Eulophidae. An example of successful biological control by a parasitoid in Florida is the citrus blackfly, Aleurocanthus wogJlumi Ashby (Dowell et al. 1979). Although extensive research is being conducted on many of the parasitoid species in these groups, information on predator fauna is said to be lacking (Greathead & Bennett 1981; Gerling 1986, 1990; Osborne, 1990). Gerling (1990) lists four insect orders and two arachnid orders which contain almost all of the known predators of whiteflies. These are Coleoptera, Hemiptera, Diptera, Neuroptera, Acarina, and Aranea.

The relatively long period that whiteflies remain in sessile stages makes them vulnerable to pathogens, parasitoids, and predators. Although investigators have searched for ways to control the whitefly, efforts to locate and release parasitoids as biological control agents against this pest have not resulted in significant reductions in field populations (F. D. Bennett, personal communication). Greathead and Bennett (1981) point out that B. tabaci was a problem in cotton before the use of synthetic insecticides and therefore suggest that it is unlikely that natural enemies can be used for successfull management. However,









these authors also recommened minimizing pesticide applications and surveying and evaluating natural enemies, especially in Asian areas of suspected whitefly origin. Gerling (1986) suggested some reasons for the variable insect parasitoid efficiency in attacking a. tabaci. Foremost is the improper timing and selection of the pesticides being used. He also suggested that the rapid development of whitefly populations will require improvements in the performance of endemic natural enemies or the introduction of exotic species.

Some reasons for a lack of knowledge about predators of whiteflies are evident. First, most of the successes in biological control have been with parasitoids (Gerling 1986). Secondly, realistic mathematical modeling is simpler for parasitoids (Hassell 1978). Thirdly, the fact that predation is much more difficult to detect and quantify than parasitism has contributed to the sparseness of information of predators (Whitcomb & Godfrey 1991). For example, predators are not collected as easily as are parasitoids. Many stages of predators are small and cryptic. Some are nocturnal. Accurate detection of predation in the field becomes a major obstacle in evaluating predation since little or no evidence of feeding activity is left for study.

Even in the event of the successful introduction of a

parasitoid, predators may still play an important role in the regulation of whitefly populations. At lower pest densities, predators may constitute a major component of stability.









DeBach (1951) suggested that predators act as a balance by feeding on whatever prey is the most abundant. Some authors believe that the aggregation of predators can stabilize population equilibrium levels (Hassell 1978, O'neal 1984, Alomar 1990, Gerling 1992). This has been suggested by Stam and Elmosa, (1990) in their study of the natural enemies of ,. tabaci on cotton in Syria. There is also some evidence that generalist predators may have been responsible for the maintenance of a low equilibrium of the viburnum whitefly, Aleurotrachelus jelinekii, during a lengthy study of its population dynamics in England (Southwood & Reader 1988, Southwood et al. 1989).

Predators of whiteflies

Mound and Halsey (1978) include a systematic list of the natural enemies of Aleyrodidae in their catalogue Whiteflies of the World. A list of natural enemies of 8. tabaci was given by Greathead and Bennett (1981) and updated by LopezAvila (1986a). The number of predator species reported to attack whiteflies is varied and growing. Approximately 159 species of arthropod predators, from 10 orders and 35 families, have been compiled from the existing literature (Table 1.1). The largest group represented is Coccinellidae, followed by Chrysopidae, Miridae, and Phytoseiidae. An asterisk denotes those found in Florida, which were found to attack E. tabaci during this study.

Perhaps the most commonly observed and reported predator of B. tabaci has been the green lacewing, Chrysoierla carnea









(Stephens) (Or & Gerling 1985, Butler & Henneberry 1988, Abdelrahman 1986). These authors report that this species is found in the field in association with the whitefly and has been maintained successfully on a diet of whiteflies (Butler & Henneberry 1988, Kapadia & Puri 1992b).


Predation and Prey Populations


The biology and general impact of predators are

discussed by Hagen et al. (1976). These authors discuss the "sterile" environments of modern monocultures indicating that the absence of suitable refugia to permit survival of predators during dormant periods inhibits predation. In some cases, only the ability to migrate to other habitats and polyphagy is said to enable predators to survive modern agriculture.

Contrasts between predators and parasitiods are made by Hassell (1978) and Sabelis (1992) outlines some of the important differences. For example, while parasitoids are always smaller in size than their host, predators tend to be more successful in capturing prey which are smaller than themselves. Only the adult female parasitoid searches for hosts, as opposed to predators, where often both genders of all stages attack prey. Parasitoid females may deposit one or more eggs per host and complete their development in that single host. In contrast, predators usually require more than one prey to produce one egg.









Another important difference between parasitoids and predators is how each responds to changes in prey density. Predation is basically a density dependent process (Horn 1988) that is to say that the size of the predator population is dependent on the density of the prey. There are two catagories of predator responses to prey density. The first is a numerical response, in which the predator increases in density, through aggregation and/or reproduction, in response to increases in the prey density. The second is a functional response, in which the rate of predator attack is a function of the prey density. This concept was first introduced by Holling (1959). Sabelis (1992) notes that since the parasitoid assimilates its food as a larva, it spends most of its time as an adult in searching for hosts. The predator, on the other hand, often spends much of its life not only in searching for food, but in food handling and digestion. The rate at which predators can convert food becomes the most important factor controlling the rate at which prey are attacked. Thus, the numerical response of predators to changes in prey density will result in more delay than that of parasitoids and their functional response will level off earlier than parasitoids because of satiation of appetite. Another factor to consider is that many predators may switch to alternate prey when it is abundant or even rely on other food sources such as fungi, pollen, nectar, or plant products.









Kuno (1987) points out that the state of prey regulation by predators in a natural ecosystem is quite fragile. Depending upon the availability of food resources, predators are said to shift between a state of being regulators and nonregulators. Food resources, therefore, govern the dynamics of prey populations.

The fact that the stability found in heterogeneous

natural ecosystems is lacking in the ephemeral agroecosystem can be advantageous for biological pest control. Although long term stability in an agricultural system is not possible, the system can be replenished with intentionally selected "able" predators from time to time. Murdoch et al. (1985) presented cases which support Kuno's (1987) position concerning the potential effectiveness of polyphagous predators in short term cropping systems. These authors argued that the conventional requisites for a successful biological control agent including host specificity, synchrony with the pest, rapid reproduction in response to host population increases, numerically low host requirement for life cycle completion, and high searching ability, are not necessarily applicable for effective biological control in an ephemeral situation. Rather, local extinction of the pest and polyphagy are said to be compatible with control in such circumstances.

O'Neil (1984, 1987) found that the functional and

numerical response of predators to velvetbean caterpillars in soybeans was constant over time. The potential impact of









predators was greatest when prey density was low. Searching behavior was found to be the greatest factor influencing predation rather than functional response. Predators adjusted their search effort to changes in leaf area of the host plant such that the rate of predation remains constant despite increases in the leaf area throughout plant phenology.

Models of predation

Although theory has been greatly expanded through

complex ecological models in recent years, simple models can still provide useful understanding of real biological systems (Murdoch 1990). The complexity of the various interactions of predation in the field continues to be achieved by first visualizing the simple single predator-single prey components of interactions and then adding to them the different factors that affect them (Hassell 1978)

Many different models of predation theory have been used to describe the predator and prey dynamics built on the earliest models of Lotka (1925), Volterra (1928), and Nicholson and Bailey (1935). These early models were strictly linear. Later, nonlinear functional predator responses to increases in prey were introduced and elaborated upon by Holling (1959a, 1959b, 1961, 1965). Three different categories of general functional responses of predators to prey densities were described. Type I is a linear response assuming increased predator attacks as prey density increases. A type II response is also linear, but at a









decreasing rate resulting in an asymptotic leveling off of the number of attacks to some constant level despite increases in prey density. This is the most common type of response seen among laboratory tests of predators. A type III response is a sigmoidal relationship of predator to prey density. A predator with type III response can discern prey density and adjust the amount of effort expended to attack prey with increases in density until leveling off at some point, as in the type II response.

The models just mentioned have seen extensive

modification resulting in a diverse growth of modeling. For example, the optimal foraging theory developed by Stephens and Krebs (1986). A general multiple predator and multiple prey model is offered by Gutierrez et al. (1981). Recently, Berryman (1992) presented a departure from the conventional predator-prey model of population theory, which suggests that ratio-dependence, rather than density dependence, is responsible for the functional response of predators to their prey.

Modeling pest population dynamics requires exacting

experimentation and an understanding of ecology (Baumgartner et al. 1981). Each attempt to model must make assumptions concerning searching behavior and prey dispersion that are often difficult to measure in the field. With the added complexity of incorporating such elements as "switching" in preference to the more abundant prey (Murdoch 1969) and the inter specific competition among multiple predators (DeBach









1974), the usefulness of theoretical modeling becomes controversial. Ridgway and Vinson (1976) believe that reliable computer modeling of the functional responses of predators to prey is defective given the difficulties associated with identifying all the biological variables and the time lag effects which are involved in predator-prey models. Recently, there has been considerable controversy over the appropriate methods of insect population analysis in intensive field studies.

Population regulation and predators

Waage and Mills (1992) define biological control as the use of living organisms as agents of pest control (i.e. regulation of pest populations with living organisms). The question of population regulation by natural enemies becomes a fundamental issue to the question of biological control and has become the subject of much debate. As a result, the ecological literature abounds with theoritical discussion of the subject of predator-prey systems and models of the role of natural enemies in population regulation.

Key factor analysis is a simple correlation-regression method used to assess the factors that cause major fluctuations in population sizes (Kuno 1991a). This method of analysis has been recommended by Southwood (1978) as a method for detecting density dependence in insect ecology. However, concern has been expressed in using the mechanism of density dependence in key factor analysis to determine the causes of animal population regulation (Wolda 1989, Hassell









1985, Hassell et al. 1987, Mountford 1988, Stiling 1988). The concern is about the difficulty of detecting densitydependent factors in population fluctuations of natural enemies from estimates of the mean population size per generation. The fluctuations from the mean of a population can be misinterpreted because the within-generation instar mortality is not always sufficient for detecting density dependence. Density dependence tests cannot be expected to provide useful information determined when it is not known if a given population is at, above, or below equilibrium. Rather, says Wolda (1989), "stabilization tests may provide a more useful alternative", as suggested by Reddingius and Den Boer (1989). However, Kuno (1991b) noted these authors' objections and made reasonable proposals for a balanced approach to the problem. He suggested that, although spurious density dependence may arise from purely statistical causes, conventional regression analysis can be used. The overall density dependence is determined by calculating the adjusted slope from Bartlett's (1953, 1955) correction for time-series. If the overall density dependence is significant, the contributions of the individual stages can then be analyzed by comparing the b values for their regression on densities of the corresponding stages. The variance in the density among the different stages should then be compared to see at which stage density dependent stabilization might be occurring (Kuno 1973).









In the summary of his recent book, Natural Enemies, Crawley (1992a) concludes that there is still not enough solid evidence that natural enemies can be relied upon to regulate populations of prey. The author emphasizes that, for population regulation to occur, "the percentage of prey population killed by natural enemies must increase as prey population density rises" (i.e. the attack rate must be density-dependent). He points out that the predator prey interactions often are affected by such an array of factors and different trophic levels that, at best, they are asymmetrical (i.e. each species is not influencing each other in a regular or predictably equal way). Murdock (1994) addresses the problem of detecting population regulation when he states that there are unsolved statistical problems when looking for density dependence from the time series of a single population. He suggests studying the mechanisms of regulation for a population directly.

Hassell (1978) accepts that understanding and explaining the dynamics of animal populations is a prodigious undertaking. Population ecology, even with its increasingly sophisticated methods, is said to have a difficult time differentiating predator-prey interactions in the field. Some predators have little observable effects on their prey populations, whereas others apparently maintain their prey at low levels. Between these two extremes, there are many examples of cyclic oscillations between the predator/prey









populations and of cases where outbreaks occur in what appear to be regulated prey populations.


Sampling Predators


Whitcomb and Godfrey (1991) recognize the numerical and functional responses of predators to prey populations as a fundamental necessity for a thorough investigation of predation. These authors insist that laboratory tests should not form the basis of research when trying to determine the role that a predator plays in controlling a pest. Rather, they stress that field investigation is what is important to determine the function of the principal predators in an agroecosystem. The sampling methods are said to be of prime importance.

Guidelines are given for the step-by-step survey of predators in the field and evaluation of the interactions that may occur by Whitcomb and Godfrey (1991). They also stress the importance of the proper identification of the predators associated with the particular crop and pest. Southwood (1978) provides a comprehensive review and theory of sampling insect populations. McDonald et al. (1989) also has edited a useful book on methods for estimating and analyzing insect populations.

The detection and evaluation of predator populations is difficult at best. Most arthropod predators are cryptic and some may feed infrequently. Interspecific interactions in the field are therefore difficult to ascertain. Direct









observations can be made, but are difficult to perform without creating disturbances which bias the predation record. A combination of sampling methods is recommended for making a comprehensive survey of predator species (Southwood 1978). He suggested techniques for obtaining absolute density estimates by sampling a unit of habitat. The chamber or cylinder method should theoretically give the best absolute counts of pest numbers (Whitcomb & Godfrey 1991). Sampling at various times of the day to allow for different diel activities also is recommended (Dumas et al. 1962, Suderland & Chambers 1983).


Evaluation of Predation


Quantitative evaluation of the efficiency of predators on pest populations in the field is difficult to achieve. Since no single technique is suitable for all situations, a combination of methods is often necessary to gather reliable information about predation in the field (Grant & Shepard 1985). Various criteria and methods of assessing the value of natural enemies of economic pests in agricultural production are covered by different authors (Suderland & Chambers 1983, Huffaker & Kennett 1969, DeBach et al. 1976).

Predator density and consumption rate can be useful in estimating the effect of the predators on pest populations. Exclusion studies which are designed to control factors of mortality are a method used to measure consumption rates on a defined area of host plants. For example, screen field cages









have been used to isolate predators and prey to estimate prey consumption (Lingren et al. 1968, van den Bosch 1969, Frazier et al. 1981).

Prey preference

The question of prey preference in polyphagous predators may be more important than is generally realized. It has been noted that polyphagous predators often demonstrate preference for specific prey (Hassell 1978, Crawley 1992). Also, apparent prey preference might be misleading. The suitability of a particular prey for longevity or reproduction should also be considered (Hodek 1993). Given the number of alternative prey often available to a generalist predator in the agroecosystem, preference and the suitability of prey for proper development are important issues in determining the potential of predators as biological control agents for a specific pest.

There have been few attempts to determine preference for lacewing species. The lacewing, Chrysopa oculata Say, was tested for preference on a variety of prey by Lavallee and Shaw (1969). Each of the three instars of the lacewing were presented equal numbers of the following prey: pea aphid, alfalfa weevil, leaf hopper, and plant bug nymphs. Aphids were found to be the prey fed upon most often, while the leaf hoppers and mirids were practically ignored. Boyd (1970) found that the preference of Chrysoperla carnea (Stephens) varied for each instar. Presented Heliothis eggs and larvae, cotton aphids, and spider mites, the first instar lacewing









larvae preyed most frequently on cotton aphids, the second instar on cotton aphids and Heliothis larvae equally, and the third instar on Heliothis larvae. Hydorn's (1971) study of the food preferences of Q. rufilabris was actually a comparison of development and fecundity on a wide assortment of prey. More recently, handling time and preference was measured on _. rufilabris by Nordlund and Morrison (1990). When observed at five minute intervals for one hour, the lacewing larvae were observed to be feeding more often on Heliothis virescens (F.) larvae than i. virescens eggs or aphids. The total count of each prey consumed in a mixed prey environment was compared for preference determination and no attempt was made to formulate a prey selection index. No other criterion was used for measurement of preference, nor was any consideration given for the difference in the time required to handle large prey as opposed to small prey.

Some of the preference models that are currently

available were used in this study. The whitefly nymph and aphid used as prey in this study presented very different characteristics to the potential predator. Macrosiphum euphorbiae (Thomas) is a large species of aphid and a. tabaci nymphs are minute, flattened, sessile scales, found on the underside of leaves. The difference in size and mobility of each prey causes doubt that reliable estimates of preference can be attained by simply comparing the total numbers of each prey consumed.









Prey suitability for development

The rate and quality of development of most generalist predators are influenced by prey. Chrysopa ateralis (Ceraeochrysa cubana) (Hagen) was found to develop at different rates on different prey associated with citrus (Muma 1957). The lacewing developed more slowly on a diet of the cloudy-winged whitefly, Dialeurodes citrifoliii (Morgan) than on a diet of the six spotted spider mite, Florida red scale, citrus red mite or the purple scale. Hydorn (1971) found significant differences in the rate of development, weight, and mortality of the larvae of _. rufilabris reared on different prey consisting different species of aphids, mites, Drosophila, eggs and larvae of the potato tuberworm Phthorimaea operculella (Zeller), and the whitefly Dialeurodes citri (Ashmead). Generally, _. rufilabris was found to perform best on a prey of the aphids, Myzua persicae (Sulzer), Acyrthosiphon piam (Harris), Aphis craccivora Koch and the eggs of Galleria sp. Although mortality of lacewings fed on the whitefly, 12. citri, was the lowest of any other prey, development time through the pupa stage was long, 26.8 days at 22.50C. Putman (1937) found a mean larval-pupal development time for Q. rufilabris to be 24.9 days at 22.5�30C when fed eggs and larvae of the moth Grapholita molest (Busck). Burke and Martin (1956) observed that 16.9 days was required for the same lacewing species to complete developmant on a diet of cotton aphids, Ahis osyii









(Glover) ( mean maximum temperature 300C and mean minimum 250C). Kapadia (1992b) found the total days of instar development of Q. carnea to be longer on a diet of B. tabaci, than on a diet of Aphis aoyii (Glover) or Rhopalosiphum maidis Fit. However, the survival rate was 100% on the whitefly compared to 90% and 56% for the respective aphids. This survival rate agrees with that of Hydorn (1971) for -. rufilabris on 12. citri.

Temperature will greatly affect the development rate of insects (Honek & Kocourek 1988). Butler and Ritchie (1970) examined the development rates of -. carnea at constant and fluctuating temperatures while holding the diet of Sitotroga cerealella (Oliver) eggs constant. The mean development time for this species was 27.7 days at a constant temperature of 200C and 19.4 days at 250C.

The development of Q. carnea at different prey densities has been reported recently by Zheing et al. (1993). Development of the first two instars was slightly longer on a sub optimal or limited diet. However, the third instar was found to be a very efficient converter of food. It was able to compensate for a limited diet received during the first two instars and to complete proper development when supplied with sufficient food.

Tauber and Tauber (1983) compared -. rufilabris and 1. carnea ontogeny under the influence of humidity. They concluded that relative humidity was a factor determining the geographical distribution and thus their respective potential









as biological control agents. C. rufilabris had a mean preimaginal development period of 26.4 days at 55% RH and 24.2 days at 75% RH, with temperature constant at 22.2 � 20C.


Detecting Predation in the Field


Direct observation and gut analysis are recommended as methods for determining what prey predators are using for food in the field (Suderland 1988). He reviews the different quantitative and qualitative methods for detecting predation in the field, including: direct observation, field cages, recovery of labeled prey, electrophoresis, single radial immunodiffusion, rocket immunoelectrophoresis, and enzymelinked immunosorbent assay. The use of electrophoresis is reviewed by Menken and Ulenberge (1987) and quantitative methods for assessment of predation rates of arthropods is covered by Fitzgerald et al. (1986). A serological method of immunoassay of insect predators is described by Schoof et al. (1986). The use of serology to evaluate predator and their prey is reviewed by Boreham and Ohiagu (1978).

Recently, a new serological method for identification of predator stomach contents has been developed which proves to be as sensitive and as accurate as the ELISA method (Stuart & Greenstone 1990). This immunodot assay shows great promise for field work. With the advent of technology to increase antibody specificity, new possibilities exist for the identification of exotic predators in the field (Lentz & Greenstone 1988, Greenstone 1989, Greenstone & Morgan 1989).









Antisera specific to a narrow range of antigens can be produced by this method. Specific antibodies are produced through cloning and then screened against all possible prey species in the system to eliminate those which cross react with the target prey.

Isozyme patterns were shown to be species specific for three species of whiteflies by Prabhaker et al. (1987) and for E. tabaci, Dialeurodes kirkaldyi (Kotinsky), Dialeurodes citri (Ashmead), and I. vaporariorum (Westwood) by Wool et al. (1989). This would indicate that each species has unique proteins that can be used for specific antibody production; however, variation in electrophoretic banding patterns among populations of B. tabaci were also reported by Costa and Brown (1990). Recently, a monoclonal antibody for the eggs of the sweetpotato whitefly, B. tabaci, has been developed to detect predation (Hagler et al. 1993).


Augmentation of Predators


Inundative releases of natural enemies are generally for the purpose of immediate suppression of pests and can be seen as a type of biological insecticide (Gerling 1992). Addition of predators to an agroecosystem by augmentative releases can demonstrate their impact on agricultural systems. Studies on the release of predators have primarily been limited to Chrysoperla carnea (Stephens), different coccinellids, Geooris, Nabis, and phytoseiid mites (Hagen et al. 1976). Augmentation of predators as a mean of biological control is









treated specifically by Ridgway and Vinson (1976) who suggest that the primary benefit from augmentation of natural enemies is to overcome the time lag in the numerical response of the predator to the pest population increase. The question of when and how many predators to release depends on many factors. A knowledge of the different components of the ecosystem is necessary. Information about how the predator and prey interact in time and space and if the predator shows preference, becomes important.


The Use of Chemicals to Manipulate Predators


Various semiochemicals, pheromones, allomones,

kairomones, synomones, and apneumones can potentially be useful tools in the manipulation of both insect pests and their natural enemies (Nordlund et al. 1981). Kairomones are chemical signals released by a prey species that benefit the predator species in host location. The importance and possible applications of kairomones in the augmentation of natural enemies are covered by Vinson (1977), Greany and Hagen (1981), and Gross (1981). Although most predator-prey models make the assumption that host encounters are random, it is now known that many arthropod predators make significant use of allelochemicals to locate prey and prey habitat. Cases are well documented where both habitat location and long distance detection of individual prey are chemically mediated. Searching, therefore, appears to be more systematic and in many cases employs a combination of









host stimuli for the location and acceptance of prey. There are various sources of host kairomones, including: frass, mandibular gland secretions, host sex pheromones, scales, and exoskeletal hydrocarbons. Different examples of kairomone prey finding from different families of insects are reviewed by Greany and Hagen (1981). They suggest that many generalist predators respond to more common biochemicals, while specialist predators may respond to more exclusive cues.

Attractants and predators

Allelochemicals have been suggested as a way to

aggregate natural predators in a field or retaining predators in a desired location during augmentative releases (Gross 1981). An "artificial honeydew" was used to increase the presence of the predator _. carnea and to increase oviposition in the field (Hagen et al. 1971). The amino acid tryptophan was found to be the source of attraction to the females of this species increased attraction when added to artificial honeydew (Hagen et al. 1976). Since tryptophan is not volatile, various products from the hydrolysis and oxidation of this amino acid were also tested for their attractiveness by Van Emden and Hagen (1976).

Green lacewings have also been reported to be attracted to other naturally occurring compounds including: methyl eugenol (Suda & Cunningham 1970), terpinyl acetate (Caltagirone 1969), monoterpene alcohols (Sakan et al. 1970), and caryophyllene (Flint et al. 1979). Although Van Emden









and Hagen (1976) reported indolyacetaldehyde and tryptamine as being highly attractive, this was not confirmed in y-tube olfactometer tests by Dean and Satasook (1983). The latter authors also could not confirm the attractiveness of caryophyllene in the y-tube experiments with Q. carnea.

Hagen and Tassan (1970) had shown the effectiveness of spraying "artificial honeydews" for the attraction and increased oviposition of chrysopids; however, various other field trials have shown different degrees of attractiveness (Ben Saad & Bishop 1976, Tassan et al. 1979, Liber & Niccoli 1988). One field study indicated that oviposition of lacewings was increased on cabbage intercropped with a sorghum-sudan hybrid, when sprayed with "artificial honeydew". Yet, no effect was noted on cabbage looper populations (Wellik and Slosser 1983). Nichols and Neel (1977) foun that levels of the coccinellid Coleomegilla maculata (Degeer) increased in corn sprayed with "artifical honeydew".


Screening Predators for Pesticide Tolerance


Predators are thought to play an important role in the reduction and regulation of natural populations of whiteflies; however, pesticide applications have been responsible for the destruction of polyphagous predators and their prey. In cases where prolonged heavy applications have been made, the results has been severe pest outbreaks (Gerling 1990). The intense use of synthetic organic









insecticides and the associated reduction in natural enemies was specifically cited as causing a control crisis on cotton and tomatoes in the Sudan (Greathead & Bennett 1981). In light of these reports, predators should be screened for sensitivity to pesticides. The response of natural enemies to insecticides has been reviewed by Croft and Brown (1975). Lacewing species have been tested for various compounds (Lawrence 1974, Lawrence et al. 1973, Grafton-Cardwell & Hoy 1985). The lacewing, -. carnea, has been shown to tolerate some insecticides at field rates (Pree et al. 1989).









Table 1.1. Predators of Whiteflies


Taxa


Location, Host, Reference


Archnida

Acarina


* Phytoseiidae




Amblyseius aleyrodis
(El Badry)

Amblyseius chilensis
Dosse

Amblyseius aossici
(El Badry)
[Euseius cossipi]

* Amblyseius hibisci (Chant) = Euseius
hibisci (Chant)

Amblyseius limonicus
(Garman and
McGregor)

Amblyseius rubini
Swirsiki & Amitai

Amblyseius swirski
(Athias-Henriot)

Euseius aleyrodis (El
Badry)

* Euseius hibisci
(Chant)


Florida, 2. citri, D.
citrifoli, (Muma 1971) Sudan, a. tabaci,
(Abdelrahman 1986)

Sudan, a. tabaci, (El Badry
1967,1968; Gameel 1971)c

Israel, B. tabaci, (Swirski
et al. 1970)

Egypt, B. tabani, (AbdelGawaad et al. 1990)


Israel, B. tabaci,
et al. 1970)


Israel, E. tabaci,
& Doriza 1968)


Israel, B. tabaci,
1966)c

Israel, a. tabaci,
1966)c


(Swirski (Swirski


(Teich (Teich


Sudan, B. tabaci, (El Badry
1967, 1968; Gameel 1971)

Israel, a. tabaci, (Swirski
et al. 1970)
California, D. tabaci,
(Meyerdirk & Coudriet
1985)









Table 1.1 -- continued


Location, Host, Reference


Euseius scutalis
(Athias-Henriot)
(Chant)=rubini




Typhlodromus athiasae
Porath & Swirski

Typhlodromus
medanicus El Badry


Typhlodromus
occidentalis
Nesbitt


Typhlodromus
sudanicus El Badry


Israel, B. tabaci, (Teich
1966; Swirsiki et al.
1967a)c; E. myricae, (Wysoki & Cohen 1983)
Jordan, a. tabaci, (Meyerdirk
& Coudriet 1986)

Israel, D. tabaci, (Swirski
et al., 1967b)c

Sudan, a. tabaci, (El Badry
1967)c


Israel, B. tabaci,
& Doriza 1969)c


(Swirski


Sudan, a. tabaci, (El Badry
1967, Gameel 1971)c


Stigmaeidae


Agistemua exsertus
Gonzales


Egypt, a. tabaci,
et al. 1976)c


* Araneae


Florida, D. citri, (Morrill
& Back 1912), A. woalumi,
(Cherry & Dowell 1979) England, A. jelinekii,
(Southwood & Reader 1988) Egypt, a. tabaci, (Darwish &
Farghal 1990)


Araneidae


* Gasterocantha
eliPsoides
(Walckenaer)
Leucauge venusta
(Walckenaer)


Florida, A. kWoglumi, (Cherry
& Dowell 1979)


Florida, A. Woalumi, (Cherry
& Dowell 1979)


Taxa


(Soliman









Table 1.1 -- continued

Taxa

Meta seagmentata


Episininae


Location, Host, Reference England, A. jelinekii,
(Southwood & Reader 1988) India, B. tabaci, (Kapadia &
Puri 1989)


Linyphiidae

Linyhia triangularis England, A. jelinekii,
(Clerck) (Southwood & Reader 1988) Lyssomanidae


* Lyssomanes viridis
(Walckenaer)

Theridiidae


* Coleosoma acutiventer
(Keyserling)

* Theridula opulenta
(Walckenaer) Insecta

Coleoptera

* Coccinellidae








Axinoscymnus beneficus
Kamiya


Florida, A. Woluimi, (Cherry
& Dowell 1979)

India, D. tabaci, (Kapadia &
Puri, 1989)

Florida, B. tabaci, (Bennett
unpub.)

Florida, ]. tabaci, (Dean &
Schuster unpub.)





India, R. eueniae, (Rao
1958)a
Florida, A. Woalumi, (Cherry
& Dowell 1979) Sudan, E. tabaci,
(Abdelrahman 1986)
Nicaragua, B. tuberculata,
(Caballero 1993)

Japan, A. spiniferus,
(Kamiya 1963)
Java, A. disperses, (Kajita
et al. 1991)








Table 1.1 -- continued


Location, Host, Reference


* Azy luteipes Mulsant


Brumoides suturalis
(F.)





Brumus sp.= Brumoides




Catana parcesetosa
(Sicard)
= Seranoium
Parcesetosa Sicard



Chilocorus
bipustulatus L.

* Chilocorus stigma
(Say)
= Q. bivulnerus
Muls.

Clitostethus arcuatus
(Rossi)









Coccinella novemnotata
Herbst


Florida, A. Wog lumi, (Cherry
& Dowell 1979)

India, B. tabaci, (Rahman
1940)c; (Husian & Trehan
1933c
Pakistan, ]. tabaci, (CIBC
1983)c; A. barodensis,
(Inayatullah 1984)

India, E. tabaci, (Husian &
Trehan 1933c; Thompson &
Simmionds 1964a; Reddy et
al. 1985)

Pakistan, E. tabaci, R.
hancocki, Aleurocanthus sp., A. barodensis and Dialeurodes sp., (CIBC
1983c, Inayatullah 1984,
Shah et al 1986)

Morocco, A. floccosus,
(Abbassi 1980)

Florida, D. citri (Morrill &
Back 1912)a; Aleyrodidae,
(Muma 1961); A. WoQlumi,
(Cherry & Dowell 1979)

Italy, A. iproletella,
(Silvestri, 1934)a France, a. phillyreae,
(Thompson & Simmionds
1964)a
Russia, 2. citri, (Agekyan
1977)
Iraq, T. lubia, (Anon 1977) Germany, A. proletella,
(Bathon & Pietrzik 1986)

Louisiana, I. abutilQnea,
(Watve & Clower 1976)


Taxa









Table 1.1 -- continued


Location, Host, Reference


Coccinella repanda
Thunberg



Coccinella septempunctata L.





Coccinella undecimpunctata (L. Coelophora inecualis
F.

Coelophora pupillata
(Swartz)

Coleomegilla sp.


Coleomegilla cubensis


* Coleomegilla maculata
(DeGreer)








Coleomegilla maculata lenagi Timberlake Genus Cryptognatha Mulsant


Pacific Region, N. beraii,
(Kirkaldy 1907) Hawaii, a. hibisci,
(Kirkaldy 1907)

Japan, T. vaporariorum,
(Kajita 1980)
Pakistan, B. tabaci, (CIBC
1983)c
Egypt, a. tabaci, (Darwish &
Farghal 1990)

Egypt, a. tabaci, (AbdelGawaad et al. 1990)

Java, A. dispersus, (Kajita
1991)

Hawaii, A. dispersus,
(Kumashiro et al. 1983)

Dominican Rep. ]. tabaci,
(Reyes et al. 1989)

Dominican Rep., ]. tabaci,
(Alvarez et al. 1993)

Illinois, T. abutiloneus,
(Dysart 1966)
Brazil, ]. tabaci, (Link &
Costa 1980)
El Salvador, a. t.abaci,
(Escobar 1983, Serrano et
al.1993)
Florida, B. tabaci, (Dean &
Schuster unpub.)

Louisiana, 2. abutiloneus.
(Watve & Clower 1976)

SE Asia, A. WoQalumi, A.
spiniferus (Clausen &
Berry 1932)
Sumatra, A. Wo1~lumi,
(Thompson & Simmionds 1964)


Taxa









Table 1.1 -- continued


Location, Host, Reference


Cryptognatha
flavicepa (Crotch)




Cryptoonatha nodiceps
Marshall

* Cryptolamus
montrouzieri
Mulsant


Cycloneda sp.


* Cycloneda sanuinea
(L.)













* Genus Delphastus


India, A. spiniferus, Q.
Citri, (Silvestri 1927)a Panama, A. WQQlumi,
(Thompson & Simmionds
1964)a

Guyana, A. cocois, (Thompson
& Simmionds 1964)a

Florida, A. Woolumi, (Cherry
& Dowell 1979)
Hawaii, A. di.spersus,
(Kumashiro et al. 1983)

Dominican Rep., B. tabaci,
(Reyes et al. 1989)

Florida, D. citri, (Morrill
& Back 1912); A. Woglumi,
(Cherry & Dowell 1979);
2. tabaci, (Dean &
Schuster unpub.)
Brazil, B. tabaci, (Link &
Costa 1980)
Colombia, D. tabaci,
(Caballero 1993)
Dominican Rep., a. tabaci,
(Alvarez et al. 1993) El Salvador, a. tabaci,
(Escobar 1983, Serrano et
al. 1993)

Japan, A.spiniferus,
(Thompson & Simmionds
1964)a
USA, P. kelloggi, T.
floridensis, 2. citri, 2.
citrifolii, (Gordon 1985) Colombia, A. malangae,
(Caballero 1993)
El Salvador, A. woalumi,
(Quezada 1978; Serrano et
al.1993)


Taxa









Table 1.1 -- continued


Location, Host, Reference


Delphastus catalinae
Horn






Delphastus diversipes
(Champion)


* Delphastus pallidus
LeConte










* Delphastu pusillus
LeConte
















(Germar)Eriopis connexa
(Germar)


Jamaica, A. wolumi,
(Thompson & Simmionds
1964)
USA, D. citri, D.
citrifolii, P. kelloci,
(Thompson & Simmionds
1964)a

Jamaica, A. wolumi, M.
cardini, (Thompson &
Simmionds 1964)

USA, T1. floridensis,
(Thompson & Simmionds
1964)a
Florida, D. citri, D.
citrifolii, A. floccosus,
(Muma et al. 1961); A.
Wolumi, (Cherry & Dowell
1979)
Dominican Rep., T.
vaporariorum, (Alvarez et
al. 1993)

USA, T. packardi, (Britton
1907)a
Florida, D. citri, D.
citrifolii, A. floccosus,
(Muma et al. 1961); A.
Woolumi, (Cherry & Dowell 1979); B. tabaci, Florida,
(Osborne et al. 1990;
Hoelmer et al. 1993)
Mexico, A. Woalumi, (Smith
et al. 1964
Louisiana, 2. abutiloneus,
(Watve & Clower 1976)
Colombia, A. socialist, 2. variabili, (Gold & Altieri 1989)

Brazil, B. tabaci, (Link & Costa 1980)


Taxa









Table 1.1 -- continued


Location, Host, Reference


Exoplectra sp.


Harmonia dimidiata
(Fabricius)

Harmonia sedecimnotata F.

Hippodamia convergens
Guerin-Menaville







Hveraspis albicollis
Gorham


Hycerascis calderana
Gorham


Leia conformis
(Boisduval)

* Leis dimidiata
Mulsant This is
Harmonia dimidiata
(F.)

Lindorus lophanthaee
Blaisdale


Menochilus sp.


West Indies, A. cocois,
(Thompson & Simmionds
1964)a
Pakistan, E. tabaci, (CIBC
1983)c

Java, A. dispersus, (Kajita
et al. 1991)

Louisiana, 2. abutiloneus,
(Watve & Clower 1976)
Dominican Rep., a. tabaci,
(Reyes et al. 1989), (Alvarez et al. 1993) El Salvador B. tabaci,
(Escobar 1983; Serrano et
al.1993)

Panama, A. Woolumi,
(Thompson & Simmionds
1964)a

Panama, A. Wolumi,
(Thompson & Simmionds
1964)a

USA, A. o lumi, (Thompson &
Simmionds 1964)a

Florida, established in Florida (Gordon 1985); E. tabaci, (Gerling 1986)


Morocco, A. floccosus,
(Abbassi 1980)

India, . phillyreae, (Rao 1958)a


Taxa








Table 1.1 -- continued


Location, Host, Reference


Menochilus
sexmaculatus (F.)





Mesochilis
parcesetosa

Microweisea castanea
Mulsant


Genus Neihaspis Casey




* Nehaspis oculatus
(Blatchley)
= Nephaspis
corhami Casey.
= Nephascis
amnicola Wingo




Nephaspis picturata
Gordon

Olla abdominalis
(Say)

* Olla v-nigrum
(Mulsant)



Oenopia sauzeti
Mulsant


India, R. eugeniae, (Rao
1958) a
Pakistan, a. tabaci, (CIBC
1983)c
Java, A. dispersus, (Kajita
et al. 1991)

B. tabaci, (Gerling 1986)


Panama, A. Woolumi,
(Thompson & Simmionds
1964)a

USA, A. dispersusi, A.
cocois, (Gordon 1985) Nicaragua, A. cocois,
(Caballero 1993)

Florida, D. citri, 2.
citrifolii, A. floccosus,
(Muma et al. 1961); A.
Woalumi, (Cherry & Dowell
1979)
Hawaii,
Honduras,
Trinidad, A. dispersus
(Kumashiro et al. 1983)

Argentina, Paraleyrodes
spp., (Teran 1989)

Louisiana, 2. abutilonea,
(Watve & Clower 1976)

Colombia, Aleyrodinae,
(Caballero 1993)
Florida, B. tabaci, (Dean & Schuster unpub.)

Pakistan, A. barodens's,
(Inayatullah 1984)


Taxa








Table 1.1 -- continued


Location, Host, Reference


* Genus Scymnus

















Scymnillodes aeneus
Sicard


Scymnillodes
cyanescens Sicard


* Scymnillodes
subtroicus Casey

Scymnus coloratus
Gorham


Scmnus gorhami Weise



Scymnus hornai Gorham



Scymnus nubilus
Mulsant


SE Asia, A. (Clausen & Berry
1932)
India, . tabaci, (Rahman
(1940)c; ER. eugeniae,
(Rao 1958)a
Florida, 12. citri, D.
citrifolii, P. perseae,
(Muma 1961)
Pakistan, A. barodensis,
(Inayatullah 1984)
Egypt, a. tabaci, (Darwish &
Farghal 1990)
Colombia, 2. citirfolii,
(Caballero 1993); B.
tabaci, El Salvador,
(Escobar, 1983; Serrano
et al. 1993)

Jamaica, A. iWoalumi,
(Thompson & Simmionds
1964) a

Jamaica, A. WoiQlumi,
(Thompson & Simmionds
1964) a

Florida, Citrus,
Aleyrodidae, (Muma 1961)

Panama, A. WoLlumi,
(Thompson & Simmionds
1964)a

Panama, A. Wolumi,
(Thompson & Simmionds
1964) a

Panama, A. Woclumi,
(Thompson & Simmionds
1964)a

Pakistan, A. barodensi,
(Inayatullah 1984)


Taxa








Table 1.1 -- continued


Location, Host, Reference


Scymnus smithianus
Silvestri

Scymnus syriacus
Mars.

Scymnus thoracicus
(F.)


Scymnus pallidivestis
Mulsant

* Scymnus punctatus
Melsheimer

Serengium cinctum


Serenaium
parcesetosum
Sicard




Genus Zilus Mulsant


Verania cardoni Weise


SE Asia, A. WoQglumi,
(Clausen & Berry 1932)

Egypt, a. tabaci, (Hafez et
al. 1979)

Panama, A. Woglumi,
(Thompson & Simmionds
1964)a

Egypt, S. phillyreae,
(Priesner & Hosny 1940)a

Florida, D. citri, (Morrill
& Back 1912)a

Nigeria, B. tabaci, (Gerling
1986)b

India, 2. citri, (Timoteyeva
& Nhuan 1978); A.
barodensis, (Shah et al.
1986); B. tabaci,
(Kapadia & Puri 1989,
1992)

USA, A. Wolumi, (Gordon
1985)

India, D, citri, (Woglum
1911)a


Melyridae


Collops vittatus Say


Arizona, a. tabaCi, (Hagler
& Naranjo 1993)


Taxa








Table 1.1 -- continued


Taxa


Location, Host, Reference


Nitidulidae


Cybocephalus sp.


Java, Aleurocanthus (Causen
& Berry 1932); A.Woglumi,
(Thompson & Simmionds 1964)a; A. dispersus,
(Kajita et al. 1991)
Indonesia, Aleurocanthus
spp., A. destructor,
(Kalshoven 1981)
India, ]. tabaci, (Kapadia &
Puri 1989)


Staphylinidae


Paederus alfierii


Egypt, Z. tabaci, (Darwish &
Farghal 1990)


Dermaptera


* Labiduridae
Labidura riparia
(Pallas) Diptera

* Anthomiidae


Cecidomyiidae


Cleodipllosis
aleyrodici Felt




Lestodiplosis sp.


Egypt, a. tabaci, (Darwish &
Farghal 1990)
Florida, a. tabaci, (Dean &
Schuster unpub.)


Florida, (Osborne et al.
1990)

El Salvador, I. abutilonea,
(Serrano et al.1993)

Australia, A ,chaientios,
(Fulmek 1943)a
Panama, L. aiganteus
(Thompson & Simmonds
1964)a

USA, Aleurode sp., (Barnes
1930)a









Table 1.1 -- continued


Location, Host, Reference


Phaenobremi
aphidivora
Rubsqmen
[Aphidoletes
aphidimyza]

* Dolichopodidae


* Genus Condylostylus






* Condylostylus chrysoprasi Walker


Egypt, B. tabaci, Moshtohor,
(Abdel-Gawaad et al.
1990)



Florida, D. tabaci, (Dean &
Schuster unpub.)

Florida, Aleyrodidae, (Muma
1961)
El Salvador, E. tabaci,
(Serrano 1978, Ardon et
al. 1992, Serrano et
al.1993)

Florida, A. woolumi, (Muma
et al. 1961, Buren &
Whitcomb 1979, Cherry &
Dowell 1979)


Drosophilidae


Acletoxemus sp.



Acletoxenus formosusw)
(Loew)


Sumatra, A. wolaumi,
(Thompson & Simmonds
1964)a

Crete, B. tabaci, T.
vaporariorum, (Kirk et
al. 1993)
Portugal, A. proletella,
(Silvestri 1934)a
England, A. ielinekii,
(Southwood & Reader 1988) Italy, A. jelinekii,
(Frauenfeld 1866)a; S.
phillyreae, (Thompson
1950)a
France a. philyree,
(Thompson & Simmonds
1964)a


Taxa









Table 1.1 -- continued


Location, Host, Reference


Acletoxenus indica
Malloch


SE Asia, A. wolgumi,
(Clausen & Berry 1932)a Java, A. wolgumi, (Thompson
& Simmonds 1964)a


Empididae


Drapetis sp.


DrapeCollartis hesuieri
Collart


Israel, a. tabaci, (Sussman
1988)

Zaire, E. tabaci, (Mayne &
Ghesquiere 1934)a


Muscidae


Coenosia solita
Walker

Syrphidae


Genus Alloorapta


* Allograpta oblicua
(Say)






* Baccha sp.




Baccha clavata F.


Baccha parvicornis
Loew


USA, Aleyrodes sp., (Fulmek
1943)a

England, A. jelinekii,
(Southwood & Reader 1988)

Colombia, Aleyrodine,
(Caballero 1993)

Florida, Aleurodidae, (Weems
1971); B. tabaci, (Dean &
Schuster unpub.)
Hawaii, A. disperse s,
(Kumashiro et al. 1983) Mexico, A. spiraeodes, B.
tabaci, (Ruiz 1993)

Brazil, A. destructor,
(Costa Lima, 1968)
Florida, h. tabaci, (Dean &
Schuster unpub.)

Cuba, M. cardini, (Thompson
& Simmonds 1964)

Cuba, M. cardini, (Thompson
& Simmonds 1964)


Taxa









Table 1.1 -- continued


Taxa


* Baccha lugens Loew.


*Ocyptamus
paravicornis
(Loew)
Syrphus corollae [Eupeodes
corollae]
Genus Toxomerus


Paraaus (Paragus) serratus (Fab.)


Location, Host, Reference Florida, Aleyrodidae, (Muma
1961)

Florida, a. tabaci, (Bennett
unpub.)

Egypt, B. tabaci, Assiut,
(Darwish & Farghal 1990) Colombia, Aleyrodine,
(Caballero 1993)

Java, A. dispersus, (Kajita
et al. 1991)


Hemiptera


Anthocoridae
AnthocoQris nemorum
(L.)

* Cardiastethus
assimilis (Reuter)

Orius spp.






Orius albidipennis
(Reuter)

* Oriu insidious
(Say)





Orius majusculus
Reuter


Sweden, T. vaporariorum,
(Ekbom 1981)

Florida, a. tabaci, (Dean &
Schuster unpub.)

Italy, 1. vaporariorum,
(Arzone 1976)
Japan, 1. vaporariorum,
(Nakazawa & Hayashi 1977) Egypt, B. tabaci, (Hafez et
al. 1979; )

Sudan, a. tabaci,
(Abdelrahman 1986)

Illinois, y. abutilonea,
(Dysart 1966)
Louisiana, T. abutilonea,
(Watve & Clower 1976)
Florida, E. tabaci, (Dean &
Schuster unpub.)

Italy, T. vaporariorum,
(Arzone 1976)









Table 1.1 -- continued


Location, Host, Reference


Orius ni�.age (Wolff) Orius sauteri Poppius


Italy, T. vaporariorum,
(Arzone 1976)

Japan, 2. vaporariorum,
(Kajita 1982)


Berytidae


* Jalysus wickhami Van
Duzee


Florida, a. tAbaci, (Dean &
Schuster unpub.)


Lygaeidae


Geocoris sp.




Geocoris ochropterus
Fieber

Geocoris pallens Stal



* Geocoris unctipes
(Say)



Miridae




Campylomma spp.


Camplomma
diversicornis
(Reuter)


Egypt, B. tabaci, (Darwish &
Farghal 1990)
Honduras, B. tabaci,
(Caballero 1993)

India, B. tabaci, (Kapadia &
Puri 1989, 1991)

Oregon,
Washington, A. spiraeodes
(Landis et al. 1958)

Illinois, T. abutilonea,
(Dysart 1966)
Florida, B. tabaci, (Dean &
Schuster unpub.)

Florida, 12. citri, (Merrill
& Back 1912)
Dominican Rep., B. tabaci,
(Caballero 1993)

Japan, 1. vaDorariorum,
(Kajita 1980, 1984)

Iraq, 1. lubia, (Anon.
1977); T. Desmodii,
(Anon. 1978)
Syria, B. tabaci, (Beingolea
1980, Stam 1983)


Taxa





Table 1.1 -- continued

Taxa

Camovlomma nicolasi
Reuter

Campyloneura vircula
(Herrick-Schaffer)

Cyrtopeltis modesta
(Distant)
= Encytatus modesta

Cyrtopeltis tenuis
Reuter



Deraeocoris sp.


Deraeocoris
delaaranoei (Puton)

Deraeocoris pallens
Reuter

Deraeocoris pattens
Reuter

Deraeocoris
punctulatus (Fallen)

Deraeocoris serenus
Dgl. Sc.)

Dicvphu5 tamaninii
Wagner

Macrolophus
caliainosus (Wagner)


Macrolophus costalis
Fiet


Location, Host, Reference

India, a. tabaci, (Kapadia &
Puri 1989)

England, A. jelinekii,
(Southwood & Reader 1988)

Dominican Republic, a.
tabaci, (Serra, 1992)


Japan, 1. vaporariorum,
(Kajita 1978)
Dominican Republic, a.
tabaci, (Serra, 1992)

India, B. tabaci, (Kapadia &
Puri 1989)

Turkey, (Yayla 1986)


Israel, . tabaci, (Susman
1988)

Turkey, 2. vaporariorum,
(Soylu 1980)

Syria, a. tabaci, (Stam
1983)

Italy, T. vaporariorum,
(Arzone 1976)

Spain, 2. vaporariorum,
(Gabarra et al. 1988)

Crete, a. tabaci, 2.
vaporariorum, (Kirk et
al. 1993)

Russia, I. vaporariorum,
(Khristova et al. 1974)b





Table 1.1 -- continued

Taxa

Phytocoris sp.


Spanogonicus
albofasciatus
(Reuter)

Nabidae

Nabis spp.


Nabis ferus (L.)


Reduviidae

Coranus spiniscutis
Reuter

Harpactor costalis
Stal

Rhinocorus iracundus
(Poda)

* Sinea diadema
(Fabricius)

Neuroptera

* Coniopterygidae
* Coniotery vicina
Hagen

Conwentzia sp.


Conwentzia psociformis
(Curtis)


Location, Host, Reference Egypt, B. tabaci, (Darwish &
Farghal 1990)

Arizona, T. abutiloneus,
(Butler 1967)




Louisiana, _. abutiloneus,
(Watve & Clower 1976) Illinois, T. abutiloneus,
(Dysart 1966)



Egypt, B. tabaci, (Hafez et
al. 1979)

Egypt, B. tabaci, (Hafez et
al. 1979)

Hawaii, Aley~rodes sp.,
(Kirkaldy 1907)

Florida, a. tabaci, (Dean &
Schuster unpub.)




Florida, . citrifnil,
(Muma 1967)

California, 1. vaporariorum,
(Gerling 1967)

England, A. ielinekii,
(Southwood & Reader 1988)








Table 1.1 -- continued


Location, Host. Reference


* Chrysopidae





































Anisochrysa
flavifrons (Brauer)

Brinckochrysa
scelestes (Banks)


Panama,
Jamaica,
Malaya, A. wolumi,
(Thompson & Simmonds
1964)a;
California, 1. vaporariorum,
(Gerling 1967)
India, a. tabaci, 2.
riicini, (Thompson &
Simmonds 1964)a
Egypt, a. tabaci, (El Helaly
et al. 1971)c
Louisiana, T. abutilonea,
(Watve & Clower 1976)
Florida, D. citri, (Morrill
& Back), A. woulumi,
(Cherry & Dowell 1979)
Brazil, a. tabaci, (Link &
Costa 1980)
India, B. tabaci, (B.
tabaci, (Thomas 1932c;
Husain & Trehan, 1933c;
Reddy et al., 1985; Kapadia & Puri 1989)
Dominican Rep., a. tabaci,
(Reyes et al. 1989); (Alvarez et al. 1993)
Java, A. disperses, (Kajita
et al. 1991)
El Salvador, A. woalumi,
(Quezada 1978, Serrano et
al.1993)
Panama, Aleyrodidae,
(Zachrisson & Poveda
1993)

Morroco, B. tabaci, (Mimeur
1946)c

India, B. tabaci, (Roshman
1940, Nasir 1947)c


Taxa





Table 1.1 -- continued

Taxa

* Ceraeochrsysa cincta
(Schneider)



* Ceraeochrsysa cubana
(Hagen) = Chrysopa
cubana Hagen

Chrysoa comanche
Banks

Chrysopa cymbele
Banks

Chrysona formosa
Brauer

Chrysona flava
(Scopoli)

Chrysopa lacciperda
Kimmins

Chrysova oculata Say


Chrysopa scelestes
Banks

Chrysopa ne1 L.


Location, Host, Reference

Argentina, citrus aleyrodids
(GonzAlez 1987)
Florida, M. Griseus, Mason
et al. 1991)

Florida, A. floccosus, (Muma
1961); . tabaci, (Dean &
Schuster unpub.)

Hawaii, A. dispersus,
(Kumashiro et al. 1983)

India, B. tabaci, (Nasir
1947)c

Morocco, B. tabaci, (Mimeur
1946)c

Morocco, B. tabaci, (Mimeur
1946)c

India, B. tabaci, (Kapadia &
Puri 1989)

Illinois, T. abutiloneus,
(Dysart 1966)

India, a. tabaci, (Nasir
1947)a

Bulgaria, T. vaporariorum,
(Babrikova 1979)b









Table 1.1 -- continued


Location, Host, Reference


Chrysoperla carnea
(Stephens)
= Chrysova carnea











Chrysoperla
plorabunda (Fitch)

* Chrysoperla
rufilabris
(Burmeister)
= Chrysona rufilabris


* Chrysoerla external
(Hagen)
= Chrysopa externa
Hagen




Mallada boninensis
(Okamoto)

Hemerobidae


* Micromus aposticus
(Walker)
* Micromus subanticus
(Walker)


Egypt, B. tabaci, (Hafez et
al. 1979, Darwish &
Farghal 1990, AbdelGawaad et al. 1990)
Pakistan, . tabaci, (CIBC
1983)c, . barodensis,
(Inayatullah 1984)
Israel, B. tabaci, (Or &
Gerling 1985) Sudan, a. tabaci,
(Abdelrahman 1986)
India, D. tabaci, (Kapadia &
Puri 1989)

Arizona, ]. tabaci, Butler &
Henneberry 1988)

Canada, 1. vaporariorum,
(Thompson & Simmonds
1964) a
Florida B. tabaci, (Dean &
Schuster unpub.)

Argentina, citrus alyrodids,
(GonzAlez 1987)
Colombia, Aleyrodinae, L.
gicanteus, (Caballero
1993)
Florida, a. tabaci, (Dean &
Schuster unpub.)

India, a. tabaci, (Kapadia &
Puri 1989)

Louisiana, _. abutiloneus,
(Watve & Clower 1976)

Florida, a. tabaci, (Dean &
Schuster unpub.)

Florida, B. tabaci, (Dean &
Schuster unpub.)


Taxa









Table 1.1 -- continued


Taxa


Mantispidae Thysanoptera


Phlaeothripidae


* Aleurodothrips
fasciatus Franklin
[fasciapennis]


Ha-plothrips merrilli
Watson
[Karnyothrips]

Karnyothrips sp.


Location, Host, Reference


Honduras, Aleuroglandulus
sp. (Caballero 1993)


India, a. tabaci, (Kapadia &
Puri 1989)

Florida, 2. citri, (Morrill &
Back 1912), Aleyrodidae,
(Selhime et al. 1953, Muma
1961)

Puerto Rico, A. floccosus,
(Fulmek 1943)


Worldwide, Aleurodidae,
(Palmer et al. 1989)


Thripidae


* Franklinothrips
vespiformis
(Crawford)




Sericothrips
trifasciatus
(Ashmead)


Hymenoptera

Ceraphronidae


AphonogrQmus fumipennis


Cuba
Florida
Texas
Nicaragua Brazil, Aleurodidae,
(Moulton 1932)c

Mississippi, A. gossii,
(Ashmead 1894)a
Hawaii, T. abutiloneus,
(Kirkaldy 1907)a


B. tabaci, (Gerling 1986)


Formicidae


Iridomyrmex ancepsr)
(Roger)


Java, A. dispersus, (Kajita
et al. 1991)









Table 1.1 -- continued


Taxa


Location, Host, Reference


Lepidoptera

Noctuidae


Coccidiphaga scitula
(Rambur)


Nigeria, D. africana, (Mound
1965)a


Pyralididae


Crvyptoblabes
anidiella
(Milliere)


India, A. wonlumi, (Thompson
& Simmonds 1964)a
Malaya, Aleurocanthus sp.
(Clausen 1940)


Tortricidae


Clepsis consimilana
(Hubner)


England, a. immaculatus
(Caballero 1993)


a As cited in (Mound & Halsey 1978) b As cited in (Ekbom 1981) c As cited in (Cock 1986) d As cited in (Gerling 1990) e As cited in (Serrano et al. 1992) e As cited in (Hilje & Arboleda 1993)

* predators found in Florida
** full names of whitefly hosts listed below


Aleurocanthus s~iiferus (Quaintance) Aleurocanthus wolumi Ashby Aleurodes ~aovii (Fitch) Aleurodicus cocois (Curtis) Aleurodicus destructor Mackie Aleurodicus dispersus Russell Aleurolobus barodensis (Maskell) Aleurothrixus flocosus (Maskell) Aleurotrachelus socialist Bondar Aleurotrachelus elinekii (Frauenfeld) Aleurycerus chaientios Fulmek Aleurv.cus chacentios Nomen nudum Alerode proletella (Linnaeus) Aleyrodes; spiraeodes Quaintance


Spiny whitefly Citrus blackfly


Coconut whitefly Spiralling whitefly Sugarcane whitefly Wooly whitefly

Viburnum whitefly


Iris whitefly







Table 1.1. -- continued


Bemisia argentifolia Bellows & Perring Silverleaf whitefly Bemisia tabaci Gennadius Sweetpotato whitefly Dialeurodes citrifolii (Morgan) Dialeurodes citri (Ashmead) Dialeurolonga africana (Newstead) Lecanoideus aianteus (Quaintance & Baker) Metaleurodicus cardini (Back) Metaleurodicus griseus
[Aleurodicus griseus Dozier] Neomaskellia bergii (Signoret) Parabemisia myricae Kuwana Paraleyrodes perseae (Quaintance) Pelius kelloagi (Bemis) Rusostigma eugeniae (Maskell) Singhius hibisci (Kotinsky) Siphoninus immaculatus (Heeger) Siphoninus phillvreae (Haliday) Trialeurodes abutiloneus (Haldeman) Bandedwing whitefly Trialeurodes floridensis (Quaintance) Trialeurodes rara Singh
= T. desmodii Corbett and _. lubia El Khidir & Khalifa Trialeurodes ricini (Misra)
[possibly = 2. Lara]
Trialeurodes vaporariorum (Westwood) Greenhouse whitefly Trialeurodes variabilis (Quantiance)















CHAPTER II
PREDATION OF THE SWEETPOTATO WHITEFLY ON FIELD TOMATOES



Introduction

Since the 1986 outbreak of the "sweetpotato whitefly" in Florida greenhouses, large numbers of this pest have been present on vegetable crops, including field tomatoes. The feeding and honeydew damage, normally associated with high whitefly populations, can become quite pronounced on tomatoes. In addition, when young fruit are attacked, they later fail to ripen uniformly resulting in a condition called "irregular ripening" (Schuster et al. 1990). The viruses transmitted by this species are perhaps the most important threat to Florida tomato production (Kring et al. 1991).

Certain lifestages of the whitefly make it particularly vulnerable to predation and parasitism. While the winged adults are active flyers, the four nymphal stages and the pupae are sessile. Eggs are deposited on a small stalk on the underside of tomato leaves. The first instar (crawler) has fully developed legs, yet it migrates but a few millimeters after eclosing before it settles at a particular location to feed (Mound 1978). For the remainder of development, it is an immobile, translucent scale feeding on









the underside of the leaf. These immature life stages are vulnerable to attack by numerous natural enemies.

Little has been reported concerning predators of

whiteflies in Florida. The earliest mention concerns the citrus whitefly, Dialeurodes citri (Ashmead), and the cloudywing whitefly, Dialeurodes citrifolii (Morgan), (Morrill & Back 1912). Muma et al. (1961) gave an extensive survey of the natural enemies of the citrus whitefly in Florida. Predator induced mortality was also included in the evaluation of biological control of the citrus blackfly in Southern Florida (Dowell et al. 1979); however, no mention of predaceous species was made. The nearest reports of predation in the U. S. are in Dysart's (1966) study of the natural enemies of the bandedwing whitefly in Illinios and Watve and Clower's (1976) study of the same pest on cotton and soybean in Louisiana.

The first step in studying predation in the

agroecosystem is to determine what predator species in a particular crop will attack the pest of interest (Whitcomb & Godfrey 1991). Since little information exists concerning the predacious species attacking the sweetpotato whitefly in Florida, this investigation was undertaken to learn what predators exist and what potential contribution they might make toward the biological control of this new pest. Pest and natural enemy populations of arthropods were surveyed over the entire spring and fall seasons of Florida tomato









production using an absolute sampling method (Southwood 1978), which was non destructive.


Methods and Procedures


Field survey. Sampling of populations of whiteflies and related predators was begun the fall of 1991 and conducted through the spring of 1993, spanning two years of two tomato crops each. Survey plots were situated on the edge of fields near border vegetation or fallow land and were buffered from normally sprayed plots by at least eight 48 in. spaced rows. Pesticide applications were limited to Bravo 720, for the control of fungal pathogens and Bacillus thuringiensis var. kurstuki, (Javelin WG), for the control of southern armyworm larvae, LSpodoptera eridani. (Cramer).

Sampling began with transplants of tomato cv. 'Sunny' and continued through final harvest for each crop. Plots consisted of six 30.5 m rows spaced 1.5 m apart. Plants were spaced 45.7 cm apart on raised soil beds covered with plastic film and supported with stakes (Kelbert et al. 1966). Plants that were to be sampled were separated by ten plants and were numbered in each row. A randomization table was used to select the sampling sequence of three plants per day that were taken twice each week throughout the growing season. One plant was sampled at each of three different times on each sample date (10:30 am, 3:30 pm, 10:30 pm), in order to avoid possible diel feeding cycles of predators (Dumas 1962).









Sampling in the plots was accomplished with a whole

plant drop trap (Fig. 2.1). The device consisted of a clear fiberglass cylinder, 0.95 m diameter and 1.22 m high, which was suspended over the plant to be sampled by a portable tripod. The top of the cylinder was fitted with a screen so that air could escape as it fell over the plant. The trap was positioned over the plant to be sampled for a minimum of 2 hrs. prior to the designated sampling time. This was done to allow for the normal dispersion of insects among tomato plants prior to the sample time and to diminish perturbation of the fauna that was present prior to sampling. In the event of rain, the trap could often be left in place until sufficient drying occurred to allow for the removal of arthropods.

The tripod was secured with three nylon lines and metal stakes to avoid falling in the event of high wind gusts or storms. The height of the tripod was 3.15 m that allowed sufficient height above the plant stakes for positioning the trap and allowed at least 0.5 m clearance above a late season plant height (1 m - 1.2 m). The trap could be triggered remotely with either a manual trip line (10 m) or an automatic timer to avoid disturbances of predator behavior caused by human activity. The clear cylinder and tripod of the trap created minimal shading and were not in contact with the plant. Wire guides on the tripod legs, passing through eyelet's on the sides of the cylinder, assured that the cylinder fell perpendicular to the raised bed and made









uniform contact with the plastic mulch surface. The falling cylinder formed a crease in the soil beneath the plastic mulch that helped assure that no arthropods escaped capture. Clear plastic windows and openings secured with organdy sleeves were provided on each side of the drop cylinder. The windows allowed physical access to the entire plant from either row. (Fig. 2.2).

To collect each sample, the base of the cylinder was

first inspected to assure that there was a complete seal with the plastic mulch. Then, a cardboard disk was placed over the top of the screened cylinder. Thus enclosed, the plant and cylinder were sprayed thoroughly with a synthetic pyrethroid, PT 2100 Resmethrin (Whitmire Research Laboratories Inc., St. Louis, MO). A minimum of one full minute was allowed for the insecticide spray to subdue the arthropods. The arthropods were then collected from the interior of the cylinder, the plastic mulch, and the plant with a portable DC hand vacuum (BioQuip Products, Gardena, CA). The plant was shaken vigorously and dislodged arthropods were vacuumed. After this procedure was completed, the cylinder was raised and the plant and plastic mulch was again inspected for any remaining arthropods.

During the fall of 1992 and the spring of 1993, many of the night samples were made with the aid of a mechanical timer (Fig. 2.3). At the designated time, the timer activated a 24 volt DC solenoid that released a lever that held the cylinder in place. When the mechanical timer was to

















































Figure 2.1. Cylindrical drop trap

-Ln









































Figure 2.2. Collection of arthropods




























































Figure 2.3. Mechanical timer









be used, the drop trap was positioned on the plant to be sampled the afternoon of the sample date. Extra care was taken to assure that the surface of the plastic mulch around the plant was smooth so that a uniform seal would take place. The next morning the arthropods were extracted from the plant following the routine procedure.

Vacuum samples were taken to the laboratory and kept at 4oC for sorting into groups for storage and identification. Specimens were either pinned, stored in 70% ethanol, or stored at -700C for serological assays at a later date. Some of the specimens were identified at the state museum in Gainesville, Florida and others were sent to the Taxonomic Service Unit of the USDA/ARS in Beltsville, Maryland for authoritative identification. Voucher specimens will be deposited at the state museum in Gainesville, Florida.

Immature whiteflies. Leaf samples were take from each plant to monitor the number of immature whiteflies. The upper leaves were used for consistency in monitoring the immature whiteflies. In the fall of 1991, only the terminal leaflet of the 7th leaf from the growing tip was taken; however, this proved to yield very low counts. Therefore, for the remaining seasons the terminal leaflet from the 7th, 8th, and 9th leaf from the terminal bud was sampled. Eggs and all stages of whitefly nymphs were recorded and leaf area was measured to determine the number of whiteflies per cm2.











Statistical Treatment


The use of log correlation was proposed for the analysis of paired data by Legendre & Legendre (1979) and was used by Gabarra et al. (1988) to analyze the association of populations of the mirid Dicyhus tamaninii Wagner with those of Trialeurodes vaporariorum Westwood. Adjustments made for the time lag between predator and prey populations allowed for closer correlation.

An attempt was made to identify some of the

relationships between field populations of the different prey found on tomatoes as well as selected predators. The Pearson product-moment correlation was applied to measure these relationships (SAS Institute 1989). This correlation coefficient is to be applied to a bivariate normal distribution; however, the bivariate normal distribution is not common (Steel & Torrie 1980). When the survey data were found to lack normality, an attempt was made to transform it using square root and logarithmic transformations. Normality of the distributions was tested using the Shapiro-Wilk's W test (Shapiro & Wilk 1965). The probabilities given for the data by this test were not considered to be normal (P <

0.05). Therefore, the correlation analysis was not performed.

When data cannot be transformed, Southwood (1978)

suggests some coefficients of association that can be used









without making assumptions about the respective distributions. A method which was chosen for the whitefly predator data is
ai = 2 A + B 0.5
a[A + B

where J = the number of individuals of species A and B in samples where both are found present and A and B equal the total of individuals of species A and B, respectively, in all samples. This method gives a proportion of individuals occurring together throughout the sampling period. Values range from -1 representing no association and +1 representing complete association.


Results and Discussion



Predator Survey


The predaceous arthropods observed feeding on the sweetpotato whitefly on tomatoes in the field or in the laboratory or both are listed in Table 2.1. Of the 39 predaceous species reported to feed on whiteflies in Florida, 19 species were found on tomatoes. The observations made during this survey are in close agreement with the findings of both Dysart (1966) and Watve & Clower (1976), with the exception that very few nabids and no Delphastis pusillus LeConte were observed in this survey. In addition to the reported new findings, there are numerous other species that probably will be found to feed on some stage of the whitefly. Numerous Diptera, Dolichopodidae, Empididae, and some









Table 2.1.


Predaceous arthropods observed feeding on Bemisia tabaci in the laboratory or field.


Predator Whitefly Life Observation Stage Taxon Stagea Siteb Egg Nymph Adult


Araneae

Theridiidae


Theridula opulenta
(Walckenaer)*


A F,L


Coleoptera

Coccinellidae


Coleomegilla maculata
fusilabris (Mulsant) Cycloneda sanauinea
sanuinea Casey
Hippodamia convergens
Guerin
o la -nigrum
(Mulsant)


A, L A, L A, L A, L


Dermaptera


Labiduridae
Labidura riparia
(Pallas) Diptera

Dolichopodidae


Ukn. spp.


Syrphidae


Al10aracta obliqua
(Say)
Baccha spp.


N A N A N A N A









Table 2.1. -- continued


Predator Whitefly Life Observation Stage


Stage Site Egg Nymph Adult


Taxon

Hemiptera

Anthocoridae

Cardiastethus
assimilis (Reuter)*
Orius insidiosus (Say)

Berytidae

Jalysus wickhami Van
Duzee*

Lygeadae

Geocoris punctivpis
(Say)

Reduviidae
Sinea diadema
(Fabricius) *

Neuroptera

Chrysopidae

Ceraeochrysa cubana
(Hagen) *
Chrysoperla externa
(Hagen) *
Chrysoperla rufilabris
(Burmeister)

Hemerobiidae

Micromus posticus
(Walker) *
Micromus subanticus
(Walker)*


F,L F,L


F,L


N A


A,N A,N A, N A,N



N






L

L

L




L

L


F,L

L

L




L

L






67


Table 2.1. -- continued a A = adult, N = nymph, L = larva, E = egg b F = field, L = lab
* first report of predation on Bemisia tabaci









Drosophilidae were observed throughout the season; however, most of them are still awaiting species identification and their feeding habits need to be confirmed. Some infrequent species that were collected may also feed on whiteflies. Most are probably "tourist insects" passing through the sampling area.

Archnida

Acarina. Although a number of phytosiid species are

found in Florida, very few predaceous mites were encountered in either the leaf samples or whole plant samples. This taxa was not sampled for in a manner specific for a survey of mites. Muma et al. (1971), estimated that the eighty-six species that they listed for Florida represent only half of the species existing in the state. Of the species present in Florida, only Euseius hibisci (Chant) has been reported as a predator of a. tabaci (Table 1.1). However, this species was not identified among the mites collected during this survey. A ubiquitous omnivorious species, Typhlodromalus perearinus Muma was collected on a single occasion.

Although, Muma (1971) reported on predaceous mites of citrus, the biology and habitat are little known for many species in the state. Muma and Denmark (1970) noted that whitefly crawlers and scale insects serve as alternative food for some species. Therefore, the potential exists for other whitefly predators to be found among the predaceous mites of Florida and they should be investigated further.









Araneae. Among the many spiders seen with whiteflies in their webs during this study, the most obvious predator of whiteflies observed was the small species, _. Opulent, which strings silk lines across the underside of a single tomato leaf. Late in the season, adult whiteflies were consistantly seen in these webs with up to 20 - 30 per leaf. The remainder of the spiders collected in this survey still await identification. There may still be found hunting spiders that will feed on whitefly nymphs, as well as insect eggs, such as, salticids (Whitcomb & Bell 1964) or Chiracanthium inclusum (Hentz), which was found to feed on eggs of Anticarsia aemmatalis Hubner by using radioactive labeled prey in the field (Buschman et al. 1977). Whiteflies would appear to make a small meal for most spiders. However, Southwood and Reader (1988), found that spiders were the main predators of Aleurotrachelus jelinekii (Frauenf.) on Viburnum bushes in England. Predation was limited to adult whiteflies for these two web spinners, Linyphia triangualris Clerck and Meta segementata (Mort.).

Spiders deserve a treatment apart from that of the class Insecta. All spiders are predaceous and most can prey on almost any insect (euryphagous). They are ubiquitous and remain at fairly constant numbers in all kinds of habitats regardless of insect densities (Riechart 1974). Although spiders do not exhibit a functional response to changes in populations of prey, they can contribute to the stability of prey populations. Through the consistent presence of sheer









numbers, the diverse spider complex can reduce pest numbers (Riechert & Lockley 1984). This may fill a somewhat unique ecological position from that of insect predators and one that needs further study. There are cases where spiders can be an effective agent in maintaining stability in the agroecosystem (Mansour et al. 1983). Riechert (1990) attempted to demonstrate prey control by the assemblage of spiders found in an agroecosystem. It was concluded that the collective spider fauna may serve as a buffer by limiting the potential exponential growth of pest populations (Riechart 1992). Wise (1993), in his review of the ecology of spiders, concludes that spiders may very well exert considerable density-independent mortality on insect pest populations; however, more evidence is needed from well-designed field studies.

Insecta

Coleoptera. As a group, Coccinellidae has the greatest number of reported whitefly predators (Table 1.1). Although Gordon (1985) recognizes primarily three host groups for coccinellid species, scale insects, mites, and aphids, he asserts that when preferred food is not available, many species are known to feed on other insects. The ladybeetles listed in Table 2.1 of this survey are classified primarily as aphid feeders. Nevertheless, coccinellid adults have been shown to be attracted to an artificial honeydew (Nichols & Neel 1977). Recently, both adults and larvae were shown to be arrested by and to feed on honeydew (Heidari & Copland









1993). Apparently, they also will feed on whitefly nymphs when they encounter them while feeding on honeydew and while searching areas of honeydew deposition.

The small coccinellids, Delphastus pusillus LeConte and Nephaspia oculatus Casey, are whitefly predators that are found in Florida (Table 1.1). They were conspicuously absent from our survey samples on tomatoes. They are species most often found in arboreal habitats (Osborne, personal comm.), although D. pusillus will feed on B. tabaci when released on herbaceous plants (Heinz et al. 1994). In view of the extensive records of coccinellids that attack whiteflies (Table 1.1), this group presents potential for further investigation and trial introductions.

Staphylinids were the only other predaceous beetles that were found to any extent during this survey. Tinolthus longicornis Stephens, T. acummus Erichson, and Atheta coriania (Krantz) were found on the foliage late in the season, but were not observed feeding. A. coriania was previously reported on tomatoes by Miller and Williams (1983). Only one report of whitefly predation by staphilinids exists, and that was from Egypt (Table 1.1). Two species, Discoxenua sp. and Oxv iadonica Sharp, are reported feeding on armored scales on citrus in Japan (Nakao 1962). It is very likely that among this large group of predaceous insects, which exhibit such diverse feeding habits and are known to feed on other homopterous insects, those will be found which feed on whitefly nymphs.









Dermaptera. The cosmopolitan species L abidura riparia (Pallas) was seen regularly after mid season. Apparently, some time is necessary for them to colonize the soil beneath the plastic mulch on the raised tomato beds after fumigation occurs just prior to planting. A single report of predation of 2. tabaci exists from Egypt (Table 1.1). However, Dean and Schuster (1958) reported that this species also feeds on scales and crawlers of the Rhodes-Grass Scale Antonina raminis (Mask.) in Texas. In Florida, these predators were found to be active in the foliage at night and early morning and were credited with the greatest amount of predation of lepidopterous larvae and eggs occurring in Florida soybeans (Buschman et al. 1977). Likewise, L. riparia was found to demonstrate a functional response to increases in noctuid prey in South Carolina (Price & Shepard 1978). During this study nymphs of this species were maintained for two weeks on leaves infested with B. tabaci. However, they did not complete development on this diet.

Diptera. A number of dipteran species occur in Florida that are reported as predators of whiteflies (Table 1.1). Members of the group, Cecidomyiidae, were not found preying on whiteflies during this survey. Mound and Halsey (1978) expressed doubts about the early records of this group as predators of aleyrodids. Harris (1990), indicates that the only species of Diptera known to feed on armored scales are cecidomyiids, but that evidence is sparse and records are









infrequent. This is a group that needs additional study to ascertain feeding habits and hosts.

Adult dolichopodids were seen throughout the season in the field. A number of species were reported in a predator survey done in Florida soybeans (Neal 1974). They are easily disturbed and their rapid and frequent flight behavior makes them difficult to observe feeding on prey as small as whiteflies. They were not observed on the underside of tomato leaves where the immature stages of the whitefly develop, but generally are found on the upper side of tomato leaves. Condylostylus species have been reported feeding on citrus whitefly adults (Table 1.1). Members of this genus may have been feeding on whiteflies but, at the time of this writing, collected specimens are awaiting authoritative identification.

Among the Drosophilidae, members of the genus

Acletoxemus are known to feed on whiteflies (Table 1.1). The species observed during this survey were associated with ripe and rotten fruit and not observed to feed on whiteflies. Ashburner (1981), gives examples of entomophagous Drosophilidae

All members of the family Empididae are said to be

predaceous on small insects and mites and are abundant in moist places (Curran 1934, Borror et al. 1981). Thus far, they have not been seen feeding on whiteflies in the field; no observations were made in the laboratory with whiteflies. This group also needs further study.









Adults of the family Syrphidae frequently were found hovering about tomato plants in the field. The predaceous larvae of A1arata obliqua (Say) were found on tomatoes and what appears to be Baccha clavata Fabricius or another Baccha sp. Some specimens that were collected in the field and allowed to complete development on whiteflies in the laboratory still await identification to species. Larvae were most often found associated with aphids, although whiteflies were also present. There are various reports of predation on whiteflies (see Table 1.1).

Hemiptera. This order contains the most species of predators found attacking whiteflies in this survey. Anthocorids appear to be an important predator of the whitefly on tomato in Florida. Oriusn insidiosus (Say) was the most consistent and abundant predator associated with the whitefly throughout each of the tomato seasons. Both nymphs and adults feed on eggs, larvae, and pupae of the whitefly. Nymphs were regularly seen on the undersides of tomato leaves infested with whitefly nymphs and eggs. Nymphs were able to complete development on a sole diet of whitefly nymphs. There are wide reports of Orius sp attacking whiteflies (Table 1.1).

The anthocorid Cardiastethus assimilis (Reuter), was also found in association with whiteflies on tomatoes. Nymphs maintained on whitefly diet in the laboratory were also able to complete development. There is very little reported in the literature concerning this genus of









anthocorid. Although the numbers of C. assimilis encountered did not approach those of 2. insidiosus, this species demonstrated an equal capacity to capture and consume whiteflies.

Another species that was occasionally collected was

Lasiochilus allidulus Reuter; however, it was not observed feeding on whiteflies. Q2. insidiosus, . assimilis, and L. piallidulus were the most common anthocorids found in Florida soybeans by Neal (1974). Confirming that these species are adapted to agroecosystems in Florida. A few solitary specimens were collected, such as Xylocorias alactinus (Fieber), which were most likely transient.

The stilt bug, Jalysus wickhami Van Duzee, mistakenly referred to as Jalysus spinosus (Wheeler & Henry 1981, Wheeler 1986), has been reported as a pest of tomatoes (Phipps 1924). This stilt bug was reported to cause blossom drop in tomatoes as a result of feeding in blossom buds and on the fruit stem. Elsey and Stinner (1971), found that, when fed tobacco alone, 100% mortality occurred. Further investigation proved that this species is omnivorous, requiring insect prey to develop and reproduce normally; therefore, it was released in tobacco to control lepidopteran eggs. This species was found to feed readily on whitefly nymphs and there was also no apparent damage caused to tomatoes. However, it was only seen late in the season of the spring tomato crops and the numbers were never great enough to exert much impact on whitefly populations.









Another berytid, Metacanthus tenellus Stal, was more abundant in the late spring tomato crops than J. wickhami. Specimens were held for observation with whitefly nymphs and were not found to be predaceous.

A lygaeid, (Say), was found at times during the seasonl surveys and fed on whitefly nymphs when brought into the laboratory. However, they were never very numerous in the field. Cohen and Byrne (1992) found that G. ounCtipes was an active predator of E. tabaci in the laboratory.

The family of hemipterans known as plant bugs, Miridae, are carnivorous secondarily, occasionally acquiring nutrients from sources other than plants (Henry & Wheeler 1988; Cohen 1990). A number of mirids are reported to feed on whiteflies (Table 1.1).

The most abundant mirid found on tomato was the tomato bug, Cyrtopeltis modesta (Distant). At times, this species can be a pest of tomatoes by girdling stems while feeding (Tanada & Holdaway 1954). Such feeding damage was observed during this survey; however, the damage was slight and did not appear to cause weakening or breaking of stems and blossom drop as has been reported. Predation by Q. modesta was first noted on corn earworm eggs and larvae by Rosewell and Smith (1930). Illingsworth (1937), while studying this mirid as a pest on tomatoes, also found that it fed upon aphids, mealybugs, and lepidopteran eggs and caterpillars. Parrella and Bethke (1982) investigated the use of Q. modesta as a biological control agent against the leaf miner









Liriomyza sativae Blanchard on tomatoes. They found that no nymphs completed development when given tomato stem cuttings alone but, 100% completed development when given lepidopteran eggs and tomato cuttings.

During this survey, _. modesta was held on tomato leaves infested with whitefly nymphs. Just as Illingworth (1937) reported, the mirids were found to be "decidedly wary and not at all gregarious". They are easily disturbed and continue to move rapidly with brief pauses. They were not observed to feed on whitefly nymphs . They appeared to remain primarily on the stems and did not seek out whitefly nymphs on the undersides of leaves. Although, they did puncture whitefly nymphs while probing the tomato leaves during confinement, longer term studies on plants need to be done to determine the extent of predation. Their size, behavior, and green coloring made them difficult to observe on tomato plants; therefore, they were not observed feeding on whiteflies in the field.

Other mirids identified thus far in this survey are

Ceratocapsus punctulatus Reuter and Jobertus chrysolectrus Distant. It is suggested that species of Ceratocapsus are primarily predaceous (Wheeler & Henry 1978, Henry & Wheeler 1988) from feeding observations of homopterans. J. chrysolectrus, is a Neotropical species recently discovered in South Florida (Henry & Wheeler 1982). These authors state that it has been found on eggplant and squash infested with leaf hoppers and suggest that it is at least partially









predaceous. It was collected on tomato and squash during this survey. Feeding trials have not been conducted on these species, as yet; however, it is likely that they will both be found to feed on whitefly nymphs.

Another mirid, Spanogonicus albofasciatus (Reuter), has been found preying on noctuid eggs in Florida soybeans. This species was reported to feed on the bandedwing whitefly in cotton by Butler (1967). Although this might eventually prove to be an additional mirid whitefly predator occuring in Florida, it was not encountered in this survey. However, Halticus bractatus Say was regularly seen on tomatoes in these studies and previously has been reported as a predator of velvetbean caterpillar eggs in soybeans (Buschman et al. 1977). Although Ji. bractatus was not observed as such during this survey, it is possible that this mirid will be found to be a predator of whitefly eggs or nymphs. Deraeocoris nubulosus (Uhler) was found to be a significant predator of noctuid eggs in cotton and soybeans in the southeast US (Snodgrass, 1991). This mirid should be observed for predation on whiteflies as well.

The Miridae of Florida are not very well know (Henry &

Wheeler 1982). Hagler and Naranjo (1993), with the aid of an immunoassay specific for sweetpotato whitefly eggs, recently discovered that Lyaus hesperus Kight was the most abundant whitefly predator on cotton in Arizona. Such assays may reveal a number of unsuspected predators among Florida's poorly known mirids.









Encounters with nabids were infrequent and they were not observed to feed on whiteflies in the field. The most abundant nabid found in this survey was Nabis ca~siformis Germar. It is listed among the most common species occurring in row crops in the Southeastern US. (Elvin & Sloderbeck 1984). Ekbom (1981) reported that feeding trials with Nabis sp. on whitefly nymphs indicated that only 8% of these predators were able to complete development. Only three reports of whitefly predation by nabids are presently known to exist (Table 1.1), although there are numerous reports of predation on leafhoppers, aphids, lygus bugs, mirids, early instar lepidopterans and lepidopteran eggs (Neal 1974).

All life stages of Reduviidae are considered to be

predaceous (Froeschner 1988). Among the larger reduviids, only Sinea diadema (Fabricius) was encountered with any regularity in this study. Nymphs of this species fed on whitefly nymphs and adults in the laboratory. This has not been confirmed in the field, although, it would be reasonable to assume that the apterous nymphs of this aggressive group of predators would feed on smaller prey and eggs until they could develop sufficient size and mobility to successfully attack larger prey. Neal (1974), observed adults of this species feeding on velvetbean caterpillars, Mexican bean beetle larvae, a nabid, a soybean looper, and an adult green cloverworm in soybeans in Florida.

Late in the spring seasons, Empicoris sp. were found to be quite common in the tomato field. Little is known of the









feeding habits of this species and the group currently needs revision (T. J. Henry, personal communication). This small species and another reduviid, a Barce sp., were occasionally collected. Both are very delicate and are easily damaged when collected. When brought into the laboratory, specimens would not feed at all and died within a few days. Both of these species are highly cryptic. Since they were only abundant late in the season, when the tomato plants were large and densely foliated, it has not been possible to confirm their prey.

Neuroptera. Coniopterygidae were not encountered in the tomato plots. Members of this family of predators are known to prey on whiteflies (Table 1.1). However, they may be mainly of arboreal habitats in Florida (Killington 1936, Muma 1967, Stange 1981). This family has been poorly studied (Drea 1990) and further investigation could reveal useful information related to whiteflies.

Ceraeochrysa cubana (Hagen) was the most abundant

chrysopid found feeding on whiteflies during this survey. This trash bearing species has been reported from various habitats and hosts in Florida (Muma 1961, Buschman et al. 1977, Neal 1974) and, recently, on cotton in Brazil (Gravena & Cunha 1991). Formerly known as Chryso-a cubana Hagen, Adams (1982) recently revised the group, placing this species in the current genus. He reported that this is the most abundant neotropical chrysopid genus. Muma (1959) reported this as the most common green lacewing found on citrus in









Florida. He also conducted feeding trials with this lacewing on various prey associated with citrus in Florida (Muma 1957). Other members of this genus have been reported in Florida. Ceraeochrysa cinta (Schneider) was reported feeding on the whitefly Metaleurodicus rises [Aleurodious ariseus Dozier] (Mason et al. 1991) and on the mealy bug Plotococcus eugeniae (Minter) (Eisner & Silberglied 1988). -. valida (Banks) and Q. sanchezi (Naves) were reported on armored scales in citrus (Muma 1959, Muma et al. 1961)

The next most abundant green lacewing collected in this survey was Chrysoerla externa (Hagen). This is also a common species in the neotropical region ranging from Florida to Argentina (Gonzalez 1987). It has been evaluated and summarized recently for potential as a biological control agent in tropical and temperate regions of Central and South America (Albuquerque et al. 1994). Chrysoperla rfilabris Burmeister and Chrysopodes collars (Hagen) were rarely encountered. The larvae of all of these species feed voraciously on whitefly nymphs in the laboratory. -. rufilabris is available from commercial insectaries for augmentative releases.

The hemerobiids, MicromUs posticus (Walker) and M.

subantius (Walker), were found on aphids late in the spring seasons. When brought into the laboratory, they fed on whiteflies and could complete development on whitefly nymphs. The adult brown lacewings fed on the same sugar and yeast diet that was used to maintain adult green lacewings. Drea









(1990), states that the importance of members of this family as predators of aphids are underestimated and like many Neuroptera more study needs to be done on specific prey.

Thysanoptera. The flower thrips Frankliniella tritici (Fitch) and E. occidentalis (Pergande) were common in the samples collected. The black hunter, Leptothrips mali (Fitch), was frequently found associated with the flower thrips; however, no thrips were observed feeding on whiteflies. However, authoritative identifications and gut assays may reveal some thrips predation in the future. The predacious thrips Aleurodothrips fasciapennis Franklin and Haplothrips merrilli Watson reported on Florida citrus were absent from the samples taken in tomatoes (Table 1.1).

Hymenoptera. There were no wasps or ants that were

found to be predacious on whiteflies. Formicidae were also not found to interfere with predators as has been reported in some cases (Dreistadt et al. 1986; Tedders et al. 1990). Unlike the finding of Neal (1974) and McDaniel and Sterling (1979), the imported fire ant Sol invicta Buren was not abundant in this survey. The reason that members of Formicidae were seldom encountered may be due to the plowing and fumigation of the soil that is practiced prior to each planting of a tomato crop on the research station.











Population Dynamics


Whiteflies. The weekly means of adult whiteflies and immature life stages for the four seasons surveyed are represented in Figures 2.4 through 2.7. Each season displayed some distinct characteristics in the population dynamics of the whiteflies. There was also no difference (ChiSquare = 0.559, df = 2, P < 0.05) found in the mean number of whiteflies found at the different diel sampling times (Wilcoxon rank sums, SAS Institute 1989, 282-284). During the spring crops, the weekly mean populations of whitefly adults remained below 50 per plant until the 7th or 8th week building rapidly the last 4 to 5 weeks. The whitefly sample means for the spring 1992 were very large, 3 to 3.5 times greater than in other seasons. The spring of 1992 had a maximum mean number of 970 adults per plant at the 12th week, while the spring of 1993 had a maximum mean of only 250. This amounted to 3.9 times more adults and 4.9 times more immatures. While studying the bionomics of three species of whiteflies on cotton in California, Gerling (1967), saw large differences in abundance from year to year. However, a reason was not found for these large fluctuations.

Although, the fall seasons had smaller whitefly

populations than either spring crop, populations began to increase earlier and reach their peak earlier than in the spring. In each fall season, the whitefly adults peaked













3.5

00 H 3 II
z
4
2.5


n 2 +1


.. 1.5






0.5


0-


1 2 3 4 5 6 7 8 9 Week (26 Sep. - 19 DEC, 1991) Figure 2.4. Mean number of whitefly adults per plant and immature life
on unsprayed tomatoes at Bradenton, FL, fall 1991.


10 11


stages per leaf,




Full Text

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PREDACEOUS ARTHROPODS OF THE SWEETPOTATO WHITEFLY, BEMISIA TABACI (GENNADIUS) , ON TOMATOES IN FLORIDA BY DAVID ED DEAN A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 1994

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ACKNOWLEDGMENT S Much of the time and effort that went into this program was contributed by someone other than myself. Unfortunately, space will not permit an exhaustive list. Certainly a large commitment has come from my major advisor. Dr. D. J. Schuster. Among other things, he has been a generous and patient mentor, a constant encouragement, a good example, a great fishing guide, and a trusted friend. I am fortunate to have had the opportunity to know him. My time spent on coursework in Gainesville was directed by Dr. C. S. Bar field who has served as cochairman on the advisory committee. Like Dr. Schuster, he also has taken an interest in my personal welfare, as well as my academic preparation. Along with good academic counsel, he gave me full access to his laboratory and office space while on campus. I benefited from his instruction in the classroom and had the opportunity to assist him with two international IPM courses. I am grateful for the opportunity to know him as an instructor and friend. Dr. F. D. Bennett served on my committee until his retirement in 1993. He was a great encouragement and source of valuable information on biological control. It was a privilege to have had the opportunity to know him and draw ii

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from his experience in the field. Dr. J. B. Jones generously gave me bench space and access to equipment in his laboratory. Upon Dr. Bennett's retirement. Dr. Jones agreed to fill his place on the committee. I am very grateful for his generosity and for his counsel concerning antibody techniques. Dr. L. S. Osborne has been a source of information concerning biological control of whiteflies and was a major influence in the decision to investigate the predation of whiteflies. Dr. J. A. Bartz has always encouraged me and given a good balance to all the entomologists on the committee. I want to thank each of these individuals for the time invested in committee meetings and reading of manuscripts. Dr. J. E. Polston has also donated laboratory space and Dr. G. M. Danyluck gave direction for electrophoresis and protein work. Dr. J. H. Frank gave many hours to personally tutor me through his course in biological control. Dr. J. R. McLaughlin loaned a 'D vac' for insect sampling. Dr. R. D. Getting sent greenhouse whiteflies. Dr. P. J. Walgenbach sent potato aphids. Dr. D. G. Boucias assisted in the concentration and quantification of whitefly protein. Identification of insects important to this study was provided by Drs. T. J. Henry (Hemiptera) , R. D. Gordon (Coccinellidae) , R. J. Gagne and N. E. Woodley (Diptera) of the Systematic Entomology Laboratory, Agriculture Research Service, USDA and by Drs. M. C. Thomas (Coleoptera) and L. A. Stange of the Entomology Section of the Division of Plant iii

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Industries, Florida Department of Agriculture. Dr. J. H. Frank, University of Florida, identified the staphylinids . Mr. M. Maedgen of Biofac insectary in Mathis, TX has generously supplied the green lacewings for this research. Mr. Fred Adams of the USDA insectaries in Gainesville gave me noctuid larvae and eggs for rearing lacewings. Mr. C. Liewald gave 30 hibiscus plants for rearing whiteflies. B. Mr. S. Wood assisted me faithfully as a part-time technician for two years. Mrs. L. Green was a tremendous help at the hybridoma lab. Mrs. M. Litchfield helped with long distance registration and department records each semester. To each of these individuals mentioned, I would like to express my sincere gratitude for their selfless generosity. Lastly, my family has sacrificed time and finances during the time I have spent in graduate school. They have endured two moves, spent countless hours waiting for me while I checked on experiments at night and weekends, helped me find articles in the library, moved insect traps, and brought me 'neat bugs'. My wife has had to keep me going many times, proof papers, remind me of deadlines and important dates, and pay most of the bills. Words alone are inadequate to express what their support has meant to me. So, I will just have to make some time to demonstrate my gratefulness. iv

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TABLE OF CONTENTS page ACKNOWLEDGMENTS ii TABLE OF CONTENTS V LIST OF TABLES viii LIST OF FIGURES x ABSTRACT xiv CHAPTER I. INTRODUCTION AND LITERATURE REVIEW 1 Introduction 1 Literature Review 3 History of The Sweetpotato Whitefly 3 Whiteflies 5 Biological Control of Whiteflies 6 Natural enemies 6 Predators of whiteflies 9 Predation and Prey Populations 10 Models of predation 13 Population regulation and predators 15 Sampling Predators 18 Evaluation of Predation 19 Prey preference 20 Prey suitability for development 22 Detecting Predation in the Field 24 Augmentation of Predators 25 The Use of Chemicals to Manipulate Predators .... 26 Attractants and predators 27 Screening Predators for Pesticide Tolerance 28 CHAPTER II. PREDATION OF THE SWEETPOTATO WHITEFLY ON FIELD TOMATOES 54 Introduction 54 Methods and Procedures 56 Statistical Treatment 63 Results and Discussion 64 Predator Survey 64 Archnida 68 Insecta 70 V

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Population Dynamics 83 Conclusions 129 CHAPTER III. PREY PREFERENCE AND SUITABILITY OF PREY FOR GREEN LACEWINGS 132 Introduction 132 Materials and Methods 134 Preference 134 Preference models 135 Prey Suitability 137 Development and Mortality 137 Fecundity 137 Maximum consumption 138 Statistical analysis 138 Preference 138 Prey suitability 139 Results 140 Preference 140 Prey Handling 145 Prey Suitability 148 Development 148 Mortality 150 Fecundity 151 Maximum consumption 151 Conclusion and Discussion 151 CHAPTER IV. ATTRACTION AND ARRESTMENT OF ADULT LACEWINGS 158 Introduction 158 Materials and Methods 160 Olfactometer 160 Attract ant Bioassays 162 Statistical Analysis for Olfactometer 163 Field trials 164 Sampling method 165 Statistical analysis of Field Data 168 Results 169 Olfactometer assays 169 Field Trials 172 Lacewing attraction and oviposition 172 Effects of Attractant on Other Arthropods 177 Conclusion and Discussion 182 vi

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CPIAPTER V. SUMMARY AND CONCLUSIONS 184 Introduction 184 General Discussion 185 Predator Survey 185 Predator Manipulation 187 Attractants 196 Introduced Predators 199 REFERENCES 201 BIOGRAPHICAL SKETCH 230 vii

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LIST OF TABLES Table page 1.1. Predators of Whiteflies 30 2.1. Predaceous arthropods observed feeding on Bemisia tabaci in the laboratory or field 65 2.2. Seasonal incidence of orders of arthropods and related prey collected with the whitefly, Bemisia tabaci , on unsprayed tomatoes in Bradenton, FL 89 2.3. Seasonal abundance of selected predator taxa collected during the survey of the fauna associated with Bemisia tabaci on unsprayed tomatoes in Bradenton, FL 96 2.4. Correlation coefficients (r^) for combinations of prevalent whitefly (WF) predators and the whitefly predator complex with alternative prey present on insecticide free tomatoes at Bradenton, FL 125 2.5. Association coefficients for various whitefly (WF) predators and common prey found on unsprayed tomatoes in Bradenton, FL 127 3.1. Means (±SE) of prey consumption by larvae of two lacewing species at a standard density of 30 prey and a standard time of 30 minutes 141 3.2. Relative preference of each larval instar of £. CUbana (Cc) and £. rufilabris (Cr) larvae for M. euphorbiae and nymphs of E. tabaci 143 3.3. Development of Q. rufilabris and Q. cubana ,, on three different prey diets consisting of M. euphorbiae f and B. tabaci alone and combined (A/W) 149 viii

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4.1. Responses of the lacewings, £. rufilabris (Cr) and cubana (Cc) to various compounds and products in an olfactometer in the laboratory 170 4.2. Mean number of arthropods collected in vacuum samples taken from tomato plots sprayed with an artificial honeydew and unsprayed control plots, spring 1992 178 4.3. Mean number of arthropods collected in vacuum samples taken from tomato plots sprayed with an artificial honeydew and unsprayed control plots, fall 1992 179 4.4 Mean number of arthropods collected in vacuum samples taken from squash plots sprayed with an artificial honeydew and from unsprayed control plots, summer 1993 180 ix

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LIST OF FIGURES Figure P^ge 2.1. Cylindrical drop trap 59 2.2. Collection of arthropods 60 2.3. Mechanical timer 61 2.4. Mean number of whitefly adults per plant and immature lifestages per leaf sample, on unsprayed tomatoes at Bradenton, FL, fall 1991 84 2.5. Mean number of whitefly adults per plant and immature lifestages per cm^ leaf sample, on unsprayed tomatoes at Bradenton, FL, spring 1992 85 2.6. Mean number of whitefly adults per tomato plant and immature lifestages per cm^ leaf sample, on unsprayed tomatoes at Bradenton, FL, fall 1992 86 2.7. Mean number of whitefly adults per plant and immature lifestages per cm^ leaf sample, on unsprayed tomatoes at Bradenton, FL, spring 1993 87 2.8. Mean plant height, mean number of predators of the immature lifestages of the whitefly, mean number of B. t abaci nymphs and eggs per cm^ of leaf, and mean number of spiders on unsprayed tomatoes at Bradenton, Fl, spring 1992 92 2.9. Mean plant height, mean number of predators of the immature lifestages of the whitefly, mean number of B. tabaci nymphs and eggs per cm^ of leaf, and mean number of spiders on unsprayed tomatoes at Bradenton, Fl, fall 1992 93 2.10. Mean plant height, mean number of predators of the immature lifestages of the whitefly, mean number of B. tabaci nymphs and eggs per cm^ of X

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leaf, and mean number of spiders on unsprayed tomatoes at Bradenton, Fl, spring 1993 94 2.11. Mean numbers of Orius insidiosus and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1991 99 2.12. Mean numbers of Ceraeochrysa cubana and selected alternative prey on tomatoes at Bradenton, FL, fall 1991 100 2.13. Mean numbers of Geocoris punctipes and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1991 101 2.14. Mean numbers of Orius insidiosus and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1992 102 2.15. Mean numbers of Ceraeochrysa cubana and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1992 103 2.16. Mean numbers of Geocoris punctipes and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1992 104 2.17. Mean numbers of hemerobiid larvae and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1992 105 2.18. Mean numbers of coccinellid larvae and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1992 106 2.19. Mean numbers of Orius insidiosus and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1992 107 2.20. Mean numbers of Ceraeochrysa cubana and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1992 108 2.21. Mean numbers of Cardiastethus assimills and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1992 109 xi

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2.22. Mean numbers of Chrysoperla externa and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1992 110 2.23. Mean numbers of coccinellid larvae and selected alternative prey on unsprayed tomatoes at Bradenton, FL, fall 1992 Ill 2.24. Mean numbers of Orius insidiosus and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 112 2.25. Mean numbers of Ceraeochrysa cubana and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 113 2.26. Mean numbers of Geocoris punctipes and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 114 2.27. Mean numbers of Cardiastethus assimilis and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 115 2.28. Mean numbers of hemerobiid larvae and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 116 2.29. Mean numbers of coccinellid larvae and selected alternative prey on unsprayed tomatoes at Bradenton, FL, spring 1993 117 2.30. Mean numbers of Q. insidiosus and Thysanoptera per tomato plant, spring 1992. (N=6) data transformed log(10(Y+l)) and Log Log (lOY) respectively 119 2.31. Mean numbers of Q. insidiosus and adult whiteflies per tomato plant, spring 1992. (N=6) data transformed log(10(Y+l)) 120 3.1. The mean number of prey consumed at each instar by larvae of £. cubana (Cc) and £. rufllahri s (Cr) in a mixed prey environment (with ±SE) and one half of the mean number consumed in the single prey tests (without ±SE) . All observations were conducted at a standard density of 30 prey for 30 minutes 142 xii

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3.2. Mean (±SE) of the probability of selection of M. enphnrbiae vs £. Jiaiiaci nymphs by each larval instar of £. cubana (Cc) and rufilabris (Cr) (N=16) (Manly 1972) 146 3.3. Percentage of time spent handling prey for each instar of Q. cubana (Cc) and Q.. rufilabris (Cr) in a mixed prey environment of euphorbiae and B. tabaci nymphs at a standard density of 30 prey for 30 minutes (N=16) 147 3.4. Mean (±SE) maximum prey consumed by third instar larvae of rufilabris and £. cubana of M. euphorbiae and nymphs of the whitefly E. tabaci (N=8) 152 4.1. Vacuum sampler 167 4.2. The mean (±SE) number of oviposition sites and eggs of lacewings in tomato plots sprayed with an artificial honeydew and in unsprayed plots, spring 1992 173 4.3 The mean (±SE) number of oviposition sites and eggs of lacewings in tomato plots sprayed with an artificial honeydew and in unsprayed plots, fall 1992 174 4.4. Mean (±SE) number of oviposition sites and eggs of lacewings in squash plots sprayed with artificial honeydew and in unsprayed plots, summer 1993 175 5.1. The exponential relationship of leaf area to plant height in the phenology of tomato cv 'Duke', at Bradenton, FL, 1983 (from Marlowe et al. 1983) 191 5.2. Mean number of adult whiteflies per tomato plant and mean plant height (cm), spring 1992 (N=6) 192 5.3. Mean number of adult whiteflies per tomato plant and mean plant height (cm), spring 1993 (N=6) 193 5.4. Mean number of adult whiteflies on tomato plants fall 1991 (N=6) 194 5.5. Mean number of adult whiteflies per tomato plant and mean plant height (cm), fall 1992 (N=6) 195 xiii

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Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy PREDACEOUS ARTHROPODS OF THE SWEETPOTATO WHITEFLY, BEMISIA l^EACI (GENNADIUS) , ON TOMATOES IN FLORIDA By David Ed Dean August, 1994 Chairman: Dr. D. J. Schuster Co-chairman: Dr. C. S. Barfield Major Department: Entomology and Nematology Field and laboratory studies were undertaken to ascertain the extent of arthropod predation of Bemisia t abaci (Gennadius) (recently transferred to the new species, B. arqentifolii Bellows & Perring) on tomatoes in Florida. The suitability of the whitefly as prey and olfactory response to attractants and food supplements were investigated for selected predators. Observations made in the laboratory and in the field revealed that a least 19 species of arthropods feed on one or more lifestages of B. t abaci . Field populations of the whitefly and predaceous arthropods were monitored for two years on tomatoes using a whole plant sampling method. An xiv

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anthocorid, £iriiis insidlosus (Say) , and a chrysopid, Ceraeochrysa cubana (Hagen) , were found to be the most abundant predators. The suitability of an alternative prey, the potato aphid, Macrosiphum euphorbiae (Thomas) , for the commercially available lacewing, Chrysoperla ruf ilabris Burmeister, and the native lacewing, C cubana ^ were tested. Both predator species were able to complete normal development on whiteflies alone. £, cubana larvae preferred £. tabaci over M. euphorbiae in two different models for testing preference. £. ruf ilabris preferred the aphid in the third instar in only one of the two preference models. The adult stage of the two lacewing species also were tested in the laboratory for attraction to various compounds and products with an olfactometer. Of the compounds tested, an 'artificial honeydew' and L-tryptophane were found to be highly attractive to £. rufilahri s ^ but less attractive to £. cubana. The 'artificial honeydew' also was tested in the field for increasing the presence and oviposition of chrysopids on tomatoes and squash in the field. cubana oviposited more on tomatoes sprayed with the 'artificial honeydew' although significant effects were difficult to detect . Although various predator species appear to be responding to the abundance of whiteflies in the field, the populations of this pest currently are not being regulated by predators. Continued studies are needed to investigate ways to manipulate predator populations such that they synchronize XV

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with whitefly populations. Introduction of exotic predators or augmentation of endemic ones should be investigated. xvi

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CHAPTER I INTRODUCTION AND LITERATUI^ REVIEW Introduction In 1986, greenhouses in Central Florida began experiencing a dramatic increase in populations of whiteflies. These whitefly populations were much larger than had been experienced previously and they did not respond to control measures. The new pest was identified as the "sweetpotato whitefly", Bemisia tabaci (Gennadius) , although it had not been considered a serious pest in Florida before this time. The spread of this whitefly among poinsettia nurseries was so rapid and widespread that it could not be contained. By the following season, this aggressive whitefly pest had spread out-of-doors and was attacking field tomatoes in Central Florida. In the ten years since the initial outbreak, the sweetpotato whitefly has become a major pest responsible for multimillion dollar losses each year across the southern United States from Florida to California. The advancement of the sweetpotato whitefly to this new elevated pest status has resulted in an effort to gain information about its biology and factors leading toward a reduction in agricultural losses. For many years this polyphagous whitefly was known by various synonyms around the 1

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world because of morphological differences that are associated with development on different host plants and not true genetic differences. However, researchers have recently proposed that the whitefly responsible for the current outbreak is the new species, 3.argentifolii Bellows & Perring (Bellows et al . 1994). This proposal is made on the basis of numerous dissimilarities between the organism known before the 1986 outbreak and the current whitefly pest. In view of the sudden and extensive damage done by this new pest, there can be no argument that the feeding behavior and reproductive potential are very different from the whitefly present in Florida before 1986. While those disposed to systematics vascillate over the nomenclature of this new pest — race, biotype, strain, or species, — much is still not known about the biology and ecology of this new pest. For the remainder of this paper and until there is greater consensus as to the taxonomic status of this new whitefly pest it shall be refered to as the "sweetpotato whitefly", £. tabaci. The focus of this research has been to determine what naturally occurring predaceous arthropods attack B. tabaci in Florida and to derive possible strategies for manipulating them for more effective reduction of whitefly populations. Information of the endemic predaceous enemies of whiteflies in Florida is limited primarily to citrus pests. A knowledge of the native predaceous fauna associated with whiteflies on vegetable crops is necessary for attempting to discover

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methods to enhance predation in the field. Therefore, it was decided that a faunal survey on horticulture crops was an essential prerequisite. In addition, preliminary investigations of some possible biological control agents of the whitefly were done in conjunction with the field survey. Prey preference and olfactory response of two lacewing species, Chrysoperla ruf ilabris (Burmeister) and Ceraeochrysa cubana (Hagen) were studied. C. ruf ilabris is available as a commercial biological control agent and it was observed that cubana was frequently associated with whiteflies on tomatoes in the field. Literatu re Review History of The Sweetpotato Whitefly The whitefly outbreak that occurred in the Florida greenhouse industry in 1986 and in field tomatoes the following year has resulted in an importance pest for Florida agriculture (Schuster & Price 1987) . First reported in Florida by Quaintence (1900), the sweetpotato whitefly, Bemisia t abaci (Gennadius) , was not a pest until the recent outbreak. Watson (1914), reported that Aleurodes tabaci (£. t abaci) occasionally attack tomatoes in Florida. Some controversy has existed over the taxonomic status of the species currently causing extensive damage in the southern US (Perring et al. 1993a, 1993b, Gawel & Bartlett 1993, Campbell 1993, Costa et al . 1993, Costa & Brown 1991).

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The whitefly problem in Florida is compounded by the association of large populations with several new viral diseases (Kring et al. 1991), as well as, fruit and plant disorders of unknown etiology (Schuster et al. 1990, 1991, Brown & Costa 1992) . The "sweetpotato whitefly" is a vector of new plant viruses that can cause severe damage to horticultural crops throughout Florida and the Caribbean region (Brown & Nelson 1988, Brown & Poulos 1990; Brown et al. 1990, Brown & Bird 1992) . Subsequent outbreaks of this whitefly pest have caused widespread losses in the southwestern US (Perring et al. 1991, Cohen et al. 1992, Perring et al . 1993) and elsewhere in the Caribbean (D. J. Schuster, personal communication). The "sweetpotato whitefly" has long been a serious pest in other parts of the world, particularly where cotton is grown. The quantity of insecticides used on cotton is implicated as the cause of whitefly outbreaks in such places as the Sudan (Eveleens 1983) and Turkey (Stam & Tune 1983) . According to Stam and Elmosa (1990), the interference of natural enemies by pesticide use has contributed to whitefly outbreaks in these areas. Heavy pesticide use associated with the production of cotton also has resulted in the development of resistance in many whitefly populations (Abdeldaffie et al. 1987, Prabhaker et al . 1985).

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Whitef lies Whiteflies are considered to be tropical pests and have been referred to as "the aphids of the tropics" (Mound & Halsey 1978) . They can cause plant damage by rapidly developing large populations that siphon sap from plant tissue and excrete the extracted liquid in the form of honeydew. This sugary material is deposited on the leaves of plants where the carbohydrates provide an excellent medium for formation of sooty mold that, in turn, can reduce plant photosynthesis (Lopez-Avila 1986b) . Of the more than 1156 species of whiteflies, only a relatively few are economically important (Mound & Halsey 1978) . Only four species are serious pests of annual field and vegetable crops (Byrne et al, 1990) : Aleurodes proletella (L.), Trialeurodes abutilonea (Haldeman) , Trialeurodes vaporariorum Westwood, and h. tabacl . Traits common to most of the whiteflies just mentioned are polyphagy and high rates of reproduction. Direct feeding damage can be detrimental to certain crops, such as cucurbits. However, disease transmission is the greatest threat. Although a single whitefly is not as efficient as a vector of a virus as a winged aphid, the larger numbers of whiteflies can more than compensate, making them a serious vector (J, A. Bartz, personal communication) . £. t abaci is the most important whitefly

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vector (Mound & Halsey 1978) , vectoring 25 or more viral diseases (Costa 1976) and able to transmit more than one virus simultaneously (Varma 1963) . B. t abaci has been discovered to be the only whitefly vector of geminiviruses (Duffus 1987) . Biological Control of Whiteflies Natural enemies The natural enemies which are important to biological control can be placed into three catagories: pathogens, parasites, and predators. Viruses, bacteria, fungi, protozoa, and nematodes can be important pathogens in the regulation of insect numbers. Parasites (parasitoids) of insects are smaller than their host and parasitic in the immature stages, developing within or on a single host. Predators are usually larger than their host. Most often the predator is carnivorious in the immature and adult stage, feeding on many hosts during the course of its development (van den Bosh et al. 1982). There are examples from each of these groups which have exhibited various degrees of success in controling whitefly populations. Various fungi attack whiteflies. Early uses of Aegerita , Aschersonia , and Fusarium were made against whiteflies found on citrus in Florida (Watson, 1914) , A strain of Paecilomyces fumosoroseus found in Florida has been released against E. t abaci (Osborne et al . 1990) and is proving effective in greenhouses .

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Gerling (1990) reviewed the natural enemies of whiteflies. Among the parasitoids listed, three families of Hymenoptera containing six genera are known to attack whiteflies. These are Amitus from the family Platygasteridae, Azotus , Gales , Encarsia , and Eretmocerus from the family Aphelinidae, and Euderomphale from the family Eulophidae. An example of successful biological control by a parasitoid in Florida is the citrus blackfly, Aleurocanthus woglumi Ashby (Dowell et al. 197 9) , Although extensive research is being conducted on many of the parasitoid species in these groups, information on predator fauna is said to be lacking (Greathead & Bennett 1981; Gerling 1986, 1990; Osborne, 1990) , Gerling (1990) lists four insect orders and two arachnid orders which contain almost all of the known predators of whiteflies. These are Coleoptera, Hemiptera, Diptera, Neuroptera, Acarina, and Aranea. The relatively long period that whiteflies remain in sessile stages makes them vulnerable to pathogens, parasitoids, and predators. Although investigators have searched for ways to control the whitefly, efforts to locate and release parasitoids as biological control agents against this pest have not resulted in significant reductions in field populations (F. D. Bennett, personal communication). Greathead and Bennett (1981) point out that B. tabar.i was a problem in cotton before the use of synthetic insecticides and therefore suggest that it is unlikely that natural enemies can be used for successfull management. However,

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8 these authors also reconunened minimizing pesticide applications and surveying and evaluating natural enemies, especially in Asian areas of suspected whitefly origin. Gerling (1986) suggested some reasons for the variable insect parasitoid efficiency in attacking £. tabaci . Foremost is the improper timing and selection of the pesticides being used. He also suggested that the rapid development of whitefly populations will require improvements in the performance of endemic natural enemies or the introduction of exotic species. Some reasons for a lack of knowledge about predators of whiteflies are evident. First, most of the successes in biological control have been with parasitoids (Gerling 1986) . Secondly, realistic mathematical modeling is simpler for parasitoids (Hassell 1978) . Thirdly, the fact that predation is much more difficult to detect and quantify than parasitism has contributed to the sparseness of information of predators (Whitcomb & Godfrey 1991) . For example, predators are not collected as easily as are parasitoids. Many stages of predators are small and cryptic. Some are nocturnal. Accurate detection of predation in the field becomes a major obstacle in evaluating predation since little or no evidence of feeding activity is left for study. Even in the event of the successful introduction of a parasitoid, predators may still play an important role in the regulation of whitefly populations. At lower pest densities, predators may constitute a major component of stability.

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DeBach (1951) suggested that predators act as a balance by feeding on whatever prey is the most abundant . Some authors believe that the aggregation of predators can stabilize population equilibrium levels (Hassell 1978, O'neal 1984, Alomar 1990, Gerling 1992) . This has been suggested by Stam and Elmosa, (1990) in their study of the natural enemies of E. t abaci on cotton in Syria. There is also some evidence that generalist predators may have been responsible for the maintenance of a low equilibrium of the viburnum whitefly, Aleurotrachelus jelinekii , during a lengthy study of its population dynamics in England (Southwood & Reader 1988, Southwood et al. 1989). Predators of whi teflies Mound and Halsey (1978) include a systematic list of the natural enemies of Aleyrodidae in their catalogue Whiteflies of the World. A list of natural enemies of E. tabaci was given by Greathead and Bennett (1981) and updated by LopezAvila (198 6a) . The number of predator species reported to attack whiteflies is varied and growing. Approximately 159 species of arthropod predators, from 10 orders and 35 families, have been compiled from the existing literature (Table 1.1). The largest group represented is Coccinellidae, followed by Chrysopidae, Miridae, and Phytoseiidae . An asterisk denotes those found in Florida, which were found to attack £. tabaci during this study. Perhaps the most commonly observed and reported predator of E. tabaci has been the green lacewing, Chrysoperl a carnea

PAGE 26

10 (Stephens) (Or & Gerling 1985, Butler & Henneberry 1988, Abdelrahman 1986) . These authors report that this species is found in the field in association with the whitefly and has been maintained successfully on a diet of whiteflies (Butler & Henneberry 1988, Kapadia & Puri 1992b) . Predation and Prey Populations The biology and general impact of predators are discussed by Hagen et al. (1976). These authors discuss the "sterile" environments of modern monocultures indicating that the absence of suitable refugia to permit survival of predators during dormant periods inhibits predation. In some cases, only the ability to migrate to other habitats and polyphagy is said to enable predators to survive modern agriculture. Contrasts between predators and parasitiods are made by Hassell (1978) and Sabelis (1992) outlines some of the important differences. For example, while parasitoids are always smaller in size than their host, predators tend to be more successful in capturing prey which are smaller than themselves. Only the adult female parasitoid searches for hosts, as opposed to predators, where often both genders of all stages attack prey. Parasitoid females may deposit one or more eggs per host and complete their development in that single host. In contrast, predators usually require more than one prey to produce one egg.

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Another important difference between paras itoids and predators is how each responds to changes in prey density. Predation is basically a density dependent process (Horn 1988) that is to say that the size of the predator population is dependent on the density of the prey. There are two catagories of predator responses to prey density. The first is a numerical response, in which the predator increases in density, through aggregation and/or reproduction, in response to increases in the prey density. The second is a functional response, in which the rate of predator attack is a function of the prey density. This concept was first introduced by Rolling (1959) . Sabelis (1992) notes that since the parasitoid assimilates its food as a larva, it spends most of its time as an adult in searching for hosts. The predator, on the other hand, often spends much of its life not only in searching for food, but in food handling and digestion. The rate at which predators can convert food becomes the most important factor controlling the rate at which prey are attacked. Thus, the numerical response of predators to changes in prey density will result in more delay than that of parasitoids and their functional response will level off earlier than parasitoids because of satiation of appetite. Another factor to consider is that many predators may switch to alternate prey when it is abundant or even rely on other food sources such as fungi, pollen, nectar, or plant products .

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12 Kuno (1987) points out that the state of prey regulation by predators in a natural ecosystem is quite fragile. Depending upon the availability of food resources, predators are said to shift between a state of being regulators and nonregulators . Food resources, therefore, govern the dynamics of prey populations. The fact that the stability found in heterogeneous natural ecosystems is lacking in the ephemeral agroecosystem can be advantageous for biological pest control. Although long term stability in an agricultural system is not possible, the system can be replenished with intentionally selected "able" predators from time to time. Murdoch et al. (1985) presented cases which support Kuno's (1987) position concerning the potential effectiveness of polyphagous predators in short term cropping systems. These authors argued that the conventional requisites for a successful biological control agent including host specificity, synchrony with the pest, rapid reproduction in response to host population increases, numerically low host requirement for life cycle completion, and high searching ability, are not necessarily applicable for effective biological control in an ephemeral situation. Rather, local extinction of the pest and polyphagy are said to be compatible with control in such circumstances. O'Neil (1984, 1987) found that the functional and numerical response of predators to velvetbean caterpillars in soybeans was constant over time. The potential impact of

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13 predators was greatest when prey density was low. Searching behavior was found to be the greatest factor influencing predation rather than functional response. Predators adjusted their search effort to changes in leaf area of the host plant such that the rate of predation remains constant despite increases in the leaf area throughout plant phenology. Models of predation Although theory has been greatly expanded through complex ecological models in recent years, simple models can still provide useful understanding of real biological systems (Murdoch 1990) . The complexity of the various interactions of predation in the field continues to be achieved by first visualizing the simple single predator-single prey components of interactions and then adding to them the different factors that affect them (Hassell 1978) Many different models of predation theory have been used to describe the predator and prey dynamics built on the earliest models of Lotka (1925), Volterra (1928), and Nicholson and Bailey (1935) . These early models were strictly linear. Later, nonlinear functional predator responses to increases in prey were introduced and elaborated upon by Holling (1959a, 1959b, 1961, 1965) . Three different categories of general functional responses of predators to prey densities were described. Type I is a linear response assuming increased predator attacks as prey density increases. A type II response is also linear, but at a

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14 decreasing rate resulting in an asymptotic leveling off of the number of attacks to some constant level despite increases in prey density. This is the most common type of response seen among laboratory tests of predators. A type III response is a sigmoidal relationship of predator to prey density. A predator with type III response can discern prey density and adjust the amount of effort expended to attack prey with increases in density until leveling off at some point, as in the type II response. The models just mentioned have seen extensive modification resulting in a diverse growth of modeling. For example, the optimal foraging theory developed by Stephens and Krebs (1986) . A general multiple predator and multiple prey model is offered by Gutierrez et al . (1981). Recently, Berryman (1992) presented a departure from the conventional predator-prey model of population theory, which suggests that ratio-dependence, rather than density dependence, is responsible for the functional response of predators to their prey. Modeling pest population dynamics requires exacting experimentation and an understanding of ecology (Baumgartner et al. 1981) . Each attempt to model must make assumptions concerning searching behavior and prey dispersion that are often difficult to measure in the field. With the added complexity of incorporating such elements as "switching" in preference to the more abundant prey (Murdoch 1969) and the inter specific competition among multiple predators (DeBach

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1974), the usefulness of theoretical modeling becomes controversial. Ridgway and Vinson (1976) believe that reliable computer modeling of the functional responses of predators to prey is defective given the difficulties associated with identifying all the biological variables and the time lag effects which are involved in predator-prey models. Recently, there has been considerable controversy over the appropriate methods of insect population analysis in intensive field studies. Population regulation and predatnr.q Waage and Mills (1992) define biological control as the use of living organisms as agents of pest control (i.e. regulation of pest populations with living organisms) . The question of population regulation by natural enemies becomes a fundamental issue to the question of biological control and has become the subject of much debate. As a result, the ecological literature abounds with theoritical discussion of the subject of predator-prey systems and models of the role of natural enemies in population regulation. Key factor analysis is a simple correlation-regression method used to assess the factors that cause major fluctuations in population sizes (Kuno 1991a) . This method of analysis has been recommended by Southwood (1978) as a method for detecting density dependence in insect ecology. However, concern has been expressed in using the mechanism of density dependence in key factor analysis to determine the causes of animal population regulation (Wolda 1989, Hassell

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16 1985, Hassell et al. 1987, Mountford 1988, Stiling 1988). The concern is about the difficulty of detecting densitydependent factors in population fluctuations of natural enemies from estimates of the mean population size per generation. The fluctuations from the mean of a population can be misinterpreted because the within-generation instar mortality is not always sufficient for detecting density dependence. Density dependence tests cannot be expected to provide useful information determined when it is not known if a given population is at, above, or below equilibrium. Rather, says Wolda (1989), "stabilization tests may provide a more useful alternative", as suggested by Reddingius and Den Boer (1989) . However, Kuno (1991b) noted these authors' objections and made reasonable proposals for a balanced approach to the problem. He suggested that, although spurious density dependence may arise from purely statistical causes, conventional regression analysis can be used. The overall density dependence is determined by calculating the adjusted slope from Bartlett's (1953, 1955) correction for time-series. If the overall density dependence is significant, the contributions of the individual stages can then be analyzed by comparing the b values for their regression on densities of the corresponding stages. The variance in the density among the different stages should then be compared to see at which stage density dependent stabilization might be occurring (Kuno 1973) .

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17 In the summary of his recent book, Natural Enemies , Crawley (1992a) concludes that there is still not enough solid evidence that natural enemies can be relied upon to regulate populations of prey. The author emphasizes that, for population regulation to occur, "the percentage of prey population killed by natural enemies must increase as prey population density rises" (i.e. the attack rate must be density-dependent) . He points out that the predator prey interactions often are affected by such an array of factors and different trophic levels that, at best, they are asymmetrical (i.e. each species is not influencing each other in a regular or predictably equal way) . Murdock (1994) addresses the problem of detecting population regulation when he states that there are unsolved statistical problems when looking for density dependence from the time series of a single population. He suggests studying the mechanisms of regulation for a population directly. Hassell (1978) accepts that understanding and explaining the dynamics of animal populations is a prodigious undertaking. Population ecology, even with its increasingly sophisticated methods, is said to have a difficult time differentiating predator-prey interactions in the field. Some predators have little observable effects on their prey populations, whereas others apparently maintain their prey at low levels. Between these two extremes, there are many examples of cyclic oscillations between the predator/prey

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18 populations and of cases where outbreaks occur in what appear to be regulated prey populations. Samplin g Predators Whitcomb and Godfrey (1991) recognize the numerical and functional responses of predators to prey populations as a fundamental necessity for a thorough investigation of predation. These authors insist that laboratory tests should not form the basis of research when trying to determine the role that a predator plays in controlling a pest. Rather, they stress that field investigation is what is important to determine the function of the principal predators in an agroecosystem. The sampling methods are said to be of prime importance . Guidelines are given for the step-by-step survey of predators in the field and evaluation of the interactions that may occur by Whitcomb and Godfrey (1991) . They also stress the importance of the proper identification of the predators associated with the particular crop and pest. Southwood (1978) provides a comprehensive review and theory of sampling insect populations. McDonald et al. (1989) also has edited a useful book on methods for estimating and analyzing insect populations. The detection and evaluation of predator populations is difficult at best. Most arthropod predators are cryptic and some may feed infrequently. Interspecific interactions in the field are therefore difficult to ascertain. Direct

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19 observations can be made, but are difficult to perform without creating disturbances which bias the predation record. A combination of sampling methods is recommended for making a comprehensive survey of predator species (Southwood 1978) . He suggested techniques for obtaining absolute density estimates by sampling a unit of habitat. The chamber or cylinder method should theoretically give the best absolute counts of pest numbers (Whitcomb & Godfrey 1991) . Sampling at various times of the day to allow for different diel activities also is recommended (Dumas et al . 1962, Suderland & Chambers 1983) . Evaluation of Predation Quantitative evaluation of the efficiency of predators on pest populations in the field is difficult to achieve. Since no single technique is suitable for all situations, a combination of methods is often necessary to gather reliable information about predation in the field (Grant & Shepard 1985) . Various criteria and methods of assessing the value of natural enemies of economic pests in agricultural production are covered by different authors (Suderland & Chambers 1983, Huffaker & Kennett 1969, DeBach et al. 1976). Predator density and consumption rate can be useful in estimating the effect of the predators on pest populations. Exclusion studies which are designed to control factors of mortality are a method used to measure consumption rates on a defined area of host plants. For example, screen field cages

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have been used to isolate predators and prey to estimate prey consumption (Lingren et al. 1968, van den Bosch 1969, Frazier et al. 1981) . Prey preference The question of prey preference in polyphagous predators may be more important than is generally realized. It has been noted that polyphagous predators often demonstrate preference for specific prey (Hassell 1978, Crawley 1992) . Also, apparent prey preference might be misleading. The suitability of a particular prey for longevity or reproduction should also be considered (Hodek 1993) . Given the number of alternative prey often available to a generalist predator in the agroecosystem, preference and the suitability of prey for proper development are important issues in determining the potential of predators as biological control agents for a specific pest. There have been few attempts to determine preference for lacewing species. The lacewing, Chrysopa oculata Say, was tested for preference on a variety of prey by Lavallee and Shaw (1969) . Each of the three instars of the lacewing were presented equal numbers of the following prey: pea aphid, alfalfa weevil, leaf hopper, and plant bug nymphs. Aphids were found to be the prey fed upon most often, while the leaf hoppers and mirids were practically ignored. Boyd (1970) found that the preference of Chrysnperl a carnea (Stephens) varied for each instar. Presented He Hot hi s eggs and larvae, cotton aphids, and spider mites, the first instar lacewing

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21 larvae preyed most frequently on cotton aphids, the second instar on cotton aphids and Hellothis larvae equally, and the third instar on Heliothis larvae. Hydorn's (1971) study of the food preferences of C. ruf ilabris was actually a comparison of development and fecundity on a wide assortment of prey. More recently, handling time and preference was measured on £. rufilabris by Nordlund and Morrison (1990) . When observed at five minute intervals for one hour, the lacewing larvae were observed to be feeding more often on Heliothis virescens (F.) larvae than R. virescens eggs or aphids. The total count of each prey consumed in a mixed prey environment was compared for preference determination and no attempt was made to formulate a prey selection index. No other criterion was used for measurement of preference, nor was any consideration given for the difference in the time required to handle large prey as opposed to small prey. Some of the preference models that are currently available were used in this study. The whitefly nymph and aphid used as prey in this study presented very different characteristics to the potential predator. Macrosiphum euphorbiae (Thomas) is a large species of aphid and £. tabaci nymphs are minute, flattened, sessile scales, found on the underside of leaves. The difference in size and mobility of each prey causes doubt that reliable estimates of preference can be attained by simply comparing the total numbers of each prey consumed.

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22 Prey suitability for development The rate and quality of development of most generalist predators are influenced by prey. Chrysopa lateralis ( Ceraeochrysa cubana ) (Hagen) was found to develop at different rates on different prey associated with citrus (Muma 1957) . The lacewing developed more slowly on a diet of the cloudy-winged whitefly, Dialeurodes citrifolii (Morgan) than on a diet of the six spotted spider mite, Florida red scale, citrus red mite or the purple scale. Hydorn (1971) found significant differences in the rate of development, weight, and mortality of the larvae of Q. rufilabris reared on different prey consisting different species of aphids, mites, Drosophila f eggs and larvae of the potato tuberworm Fhthorimaea operculella (Zeller) , and the whitefly Dialeurgdes citri (Ashmead) . Generally, C. rufilabris was found to perform best on a prey of the aphids, Myzus persicae (Sulzer) , Acyrthoaiphon pisnm (Harris) , AeMs craccivnra Koch and the eggs of Galleria sp. Although mortality of lacewings fed on the whitefly, D. ciixi, was the lowest of any other prey, development time through the pupa stage was long, 26.8 days at 22.5°C. Putman (1937) found a mean larval-pupal development time for rufilahri s to be 24.9 days at 22.5±3°C when fed eggs and larvae of the moth GraphoH ta molesta (Busck) . Burke and Martin (1956) observed that 16.9 days was required for the same lacewing species to complete developmant on a diet of cotton aphids. Aphis aossypi i

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23 (Glover) ( mean maximum temperature 30°C and mean minimum 25°C) . Kapadia (1992b) found the total days of instar development of £. carnea to be longer on a diet of B.. t abaci ^ than on a diet of Aphis gossypii (Glover) or Rhopalosiphum maidis Fit. However, the survival rate was 100% on the whitefly compared to 90% and 56% for the respective aphids. This survival rate agrees with that of Hydorn (1971) for £. rufilabrls on iliixi. Temperature will greatly affect the development rate of insects (Honek & Kocourek 1988) . Butler and Ritchie (1970) examined the development rates of £. carnea at constant and fluctuating temperatures while holding the diet of Sitotroga cerealella (Oliver) eggs constant. The mean development time for this species was 27.7 days at a constant temperature of 20°C and 19.4 days at 25°C. The development of £. carnea at different prey densities has been reported recently by Zheing et al . (1993). Development of the first two instars was slightly longer on a sub optimal or limited diet. However, the third instar was found to be a very efficient converter of food. It was able to compensate for a limited diet received during the first two instars and to complete proper development when supplied with sufficient food. Tauber and Tauber (1983) compared Q. rufilabri s and £. carnea ontogeny under the influence of humidity. They concluded that relative humidity was a factor determining the geographical distribution and thus their respective potential

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24 as biological control agents. Q. ruf ilabris had a mean preimaginal development period of 2 6.4 days at 55% RH and 24.2 days at 75% RH, with temperature constant at 22.2 ± 2°C. Detecting Predation in the Field Direct observation and gut analysis are recommended as methods for determining what prey predators are using for food in the field (Suderland 1988) . He reviews the different quantitative and qualitative methods for detecting predation in the field, including: direct observation, field cages, recovery of labeled prey, electrophoresis, single radial immunodiffusion, rocket Immunoelectrophoresis, and enzymelinked immunosorbent assay. The use of electrophoresis is reviewed by Menken and Ulenberge (1987) and quantitative methods for assessment of predation rates of arthropods is covered by Fitzgerald et al . (1986) . A serological method of immunoassay of insect predators is described by Schoof et al . (1986) . The use of serology to evaluate predator and their prey is reviewed by Boreham and Ohiagu (1978) . Recently, a new serological method for identification of predator stomach contents has been developed which proves to be as sensitive and as accurate as the ELISA method (Stuart & Greenstone 1990) . This immunodot assay shows great promise for field work. With the advent of technology to increase antibody specificity, new possibilities exist for the identification of exotic predators in the field (Lentz & Greenstone 1988, Greenstone 1989, Greenstone & Morgan 1989) .

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25 Antisera specific to a narrow range of antigens can be produced by this method. Specific antibodies are produced through cloning and then screened against all possible prey species in the system to eliminate those which cross react with the target prey. Isozyme patterns were shown to be species specific for three species of whiteflies by Prabhaker et al. (1987) and for B. t abaci, Dialeurodes kirkaldyl (Kotinsky) , Dialeurodes ilitri (Ashmead) , and 1. vaporariorum (Westwood) by Wool et al. (1989) . This would indicate that each species has unique proteins that can be used for specific antibody production; however, variation in electrophoretic banding patterns among populations of £. tabaci were also reported by Costa and Brown (1990) . Recently, a monoclonal antibody for the eggs of the sweetpotato whitefly, £. tabaci , has been developed to detect predation (Hagler et al. 1993) . Augmentation nf Predators Inundative releases of natural enemies are generally for the purpose of immediate suppression of pests and can be seen as a type of biological insecticide (Gerling 1992) . Addition of predators to an agroecosystem by augmentative releases can demonstrate their impact on agricultural systems. Studies on the release of predators have primarily been limited to Chrysoperl a carnea (Stephens) , different coccinellids, Geocorif?/ Nabis, and phytoseiid mites (Hagen et al. 1976). Augmentation of predators as a mean of biological control is

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26 treated specifically by Ridgway and Vinson (1976) who suggest that the primary benefit from augmentation of natural enemies is to overcome the time lag in the numerical response of the predator to the pest population increase. The question of when and how many predators to release depends on many factors. A knowledge of the different components of the ecosystem is necessary. Information about how the predator and prey interact in time and space and if the predator shows preference, becomes important. The Use of Chemicals to Manipulate Predators Various semiochemicals, pheromones, allomones, kairomones, synomones, and apneumones can potentially be useful tools in the manipulation of both insect pests and their natural enemies (Nordlund et al. 1981). Kairomones are chemical signals released by a prey species that benefit the predator species in host location. The importance and possible applications of kairomones in the augmentation of natural enemies are covered by Vinson (1977), Greany and Hagen (1981), and Gross (1981). Although most predator-prey models make the assumption that host encounters are random, it is now known that many arthropod predators make significant use of allelochemicals to locate prey and prey habitat. Cases are well documented where both habitat location and long distance detection of individual prey are chemically mediated. Searching, therefore, appears to be more systematic and in many cases employs a combination of

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27 host stimuli for the location and acceptance of prey. There are various sources of host kairomones, including: frass, mandibular gland secretions, host sex pheromones, scales, and exoskeletal hydrocarbons. Different examples of kairomone prey finding from different families of insects are reviewed by Greany and Hagen (1981) . They suggest that many generalist predators respond to more common biochemicals, while specialist predators may respond to more exclusive cues . Attractants an d predators Allelochemicals have been suggested as a way to aggregate natural predators in a field or retaining predators in a desired location during augmentative releases (Gross 1981) . An "artificial honeydew" was used to increase the presence of the predator C. carnea and to increase oviposition in the field (Hagen et al . 1971) . The amino acid tryptophan was found to be the source of attraction to the females of this species increased attraction when added to artificial honeydew (Hagen et al . 1976). Since tryptophan is not volatile, various products from the hydrolysis and oxidation of this amino acid were also tested for their attractiveness by Van Emden and Hagen (1976) . Green lacewings have also been reported to be attracted to other naturally occurring compounds including: methyl eugenol (Suda & Cunningham 1970), terpinyl acetate (Caltagirone 1969), monoterpene alcohols (Sakan et al . 1970), and caryophyllene (Flint et al. 1979). Although Van Emden

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28 and Hagen (1976) reported indolyacetaldehyde and tryptamine as being highly attractive, this was not confirmed in y-tube olfactometer tests by Dean and Satasook (1983) . The latter authors also could not confirm the attractiveness of caryophyllene in the y-tube experiments with £. carnea . Hagen and Tassan (1970) had shown the effectiveness of spraying "artificial honeydews" for the attraction and increased oviposition of chrysopids; however, various other field trials have shown different degrees of attractiveness (Ben Saad & Bishop 1976, Tassan et al. 1979, Liber & Niccoli 1988) . One field study indicated that oviposition of lacewings was increased on cabbage intercropped with a sorghum-sudan hybrid, when sprayed with "artificial honeydew". Yet, no effect was noted on cabbage looper populations (Wellik and Slosser 1983) . Nichols and Neel (1977) foun that levels of the coccinellid Coleomegi 1 1 a maculata (Degeer) increased in corn sprayed with "artifical honeydew" . Screening Predators for P esticide Tolerance Predators are thought to play an important role in the reduction and regulation of natural populations of whiteflies; however, pesticide applications have been responsible for the destruction of polyphagous predators and their prey. In cases where prolonged heavy applications have been made, the results has been severe pest outbreaks (Gerling 1990) . The intense use of synthetic organic

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insecticides and the associated reduction in natural enemies was specifically cited as causing a control crisis on cotton and tomatoes in the Sudan (Greathead & Bennett 1981) . In light of these reports, predators should be screened for sensitivity to pesticides. The response of natural enemies to insecticides has been reviewed by Croft and Brown (1975) . Lacewing species have been tested for various compounds (Lawrence 1974, Lawrence et al. 1973, Grafton-Cardwell & Hoy 1985) . The lacewing, £. carnea , has been shown to tolerate some insecticides at field rates (Free et al. 1989).

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Table 1.1. Predators of Whiteflies 30 Taxa Location^ Host, Reference Archnida Acarina * Phytoseiidae Florida, citri . n. citrifQli/ (Muma 1971) Sudan, fi. t abaci, (Abdelrahman 1986) Ainblvselus aleyrodls (El Badry) Sudan, E. t abaci . (El Badry 1967, 1968; Gameel 1971) <= Amblyseius chilensis Dosse Israel, £. tabaci ^ (Swirski et al. 1970) Amblyseius gossipi (El Badry) FEuseius aossipH Egypt, E. t abaci, (AbdelGawaad et al. 1990) * Amblyseius hibisci (Chant) = Euseius hibisci (Chant) Israel, B. t abaci , (Swirski et al. 1970) Amblyseius limonicus (Carman and McGregor) Israel, B. tabaci , (Swirski & Doriza 1968) Amblyseius rubini Swirsiki & Amitai Israel, £. t abaci , (Teich 1966) c Amblyseius swirski (Athias-Henriot) Euseius aleyrodi s (El Badry) * EuseiT:s hibisci (Chant) Israel, B. tabaci , (Teich 1966) c Sudan, t abaci . (El Badry 1967, 1968; Gameel 1971) Israel, B. t abaci , (Swirski et al. 1970) California, E. tabaci . (Meyerdirk & Coudriet 1985)

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Table 1.1 — continued 31 Taxa Location^ Host, Reference Euseius scutalis (Athias-Henriot) (Chant) = rubini Israel, R. tabaci , (Teich 1966; Swirsiki et al. 1967a) £. myricae ^ (Wysoki & Cohen 1983) Jordan, fi. tabacl ^ (Meyerdirk & Coudriet 1986) Typhlodromus athiasae Porath & Swirski Typhlodromus medanicus El Badry Israel, £. tabaci ^ (Swirski et al., 1967b) c Sudan, £. t abaci . (El Badry 1967) c Typhlodromus occidentalis Nesbitt Israel, £. t abaci , (Swirski & Doriza 1969) ^ Typhlodromus sudanicus El Badry Stigmaeidae Aaistemus exsertus Gonzales Araneae Sudan, t abaci . (El Badry 1967, Gameel 1971) c Egypt, B. tabaci , (Soliman et al. 1976) c Florida, R. iiiixi, (Morrill & Back 1912), A. woglumi , (Cherry & Dowell 1979) England, A. -ielinekii ^ (Southwood & Reader 1988) Egypt, £. tabacl . (Darwish & Farghal 1990) Araneidae * Gasterocantha elipsoides (Walckenaer) Florida, A. Woolumi , (Cherry & Dowell 1979) * Leucaugp! yenusta (Walckenaer) Florida, A. Woglumi , (Cherry & Dowell 197 9)

PAGE 48

Table 1.1 — continued 32 Taxa Location, Host, Reference Met a segmept^ta Episininae England, hjelinekii . (Southwood & Reader 1988) India, E. t abaci ^ (Kapadia & Puri 1989) Linyphiidae Linyphia triangulacis (Clerck) Lyssomanidae * Lyssomanes viridis (Walckenaer) Theridiidae * Coleosoma acuti venter (Keyserling) * Theridula opulenta (Walckenaer) England, A. jelinekii , (Southwood & Reader 1988) Florida, AWoalumir (Cherry & Dowell 1979) India, B, t abaci ^ (Kapadia & Puri, 1989) Florida, B. tabaci , (Bennett unpub . ) Florida, £. t abaci . (Dean & Schuster unpub.) Insecta Coleoptera * Coccinellidae India, E. eugeniae , (Rao 1958) a Florida, A. Woglumi , (Cherry & Dowell 1979) Sudan, B. t abaci ^ (Abdelrahman 1986) Nicaragua, tuberculata . (Caballero 1993) Axinoscymn^.S beneficus Japan, A. spinifernS r Kamiya (Kamiya 1963) Java, A. dispersuS f (Kajita et al. 1991)

PAGE 49

Table 1.1 — continued 33 Taxa Location, Host, Reference * Azya luteipes Mulsant Florida, ^. & Dowell Woalumi. 1979) (Cherry Brumoides suturalis (F.) Erumua sp.= Brumnide.q Catana parceseto.sa (Sicard) = Serangium parcesetosa Sicard Chilocorus bipustulatns L. * Chilocoru.s stigma (Say) = £. bivulnerus Muls . ClitQSt.ethiaff arcuatns (Rossi) India, fi. t abaci , (Rahman 1940) c; (Husian & Trehan 1933C Pakistan, h. tabaci , (CIBC 1983) C; ^, barodensis . (Inayatullah 1984) India, B. t abaci , (Husian & Trehan 1933C; Thompson & Simmionds 19 64 a; Reddy et al. 1985) Pakistan, £. tabaci , B. hancocki/ Aleurocanthus sp., A. barodensis and Dialeurodes sp., (CIBC 1983^, Inayatullah 1984, Shah et al 1986) Morocco, A. f loccosuS f (Abbassi 1980) Florida, R. citri (Morrill & Back 1912) a; Aleyrodidae, (Muma 1961); h. Woalumi , (Cherry & Dowell 1979) Italy, A. pro let el la, (Silvestri, 1934) a France, ^. phillyreae r (Thompson & Simmionds 1964) a Russia, citri , (Agekyan 1977) Iraq, T. lubia . (Anon 1977) Germany, A. proletella , (Bathon & Pietrzik 1986) Coccinel 1 a noveTnnntaf-;^ Louisiana, 1. abnti 1 nnpa , Herbst (Watve & Clower 1976)

PAGE 50

Table 1.1 — continued Taxa Location, Host, Reference Coccinella repanda Pacific Reaion, N. berqii, Thunberg (Kirkaldy 1907) Hawaii, S. hibisci, (Kirkaldy 1907) Coccinella Jaoan, T. vaporariorum. septempunctata L. (Kajita 1980) Pakistan, B. tabaci. fCIBC 1983) c EavDt, B. tabaci. (Darwish & r argnax ±yyu) Cocci nel 1 a Egypt, fi. tabaci , (AbdeluiiuecimpuncLaca (Li.) ijawaaa et ax. xyyu) Coelophora inecfualis Java. A. dispersus, (Kajita I. • 1 Q Q 1 ^ X y yx ) CoeloDhora pupillata Hawaii. A. dispersn.q, \ O WclL U Z ^ (Kumasnxro et ax. xybJ) Coleomeailla sp. Dominican Rep. B. tabaci, (Reyes et al. 1989) Coleomeailla cubensis Dominican Rep., E. t^h^ox, (Alvarez et al . 1993) * Coleomeailla maculata Illinois, T. abutiloneus. (DeGreer) (Dysart 1966) E>i.clZ_L±, D . LdlJciCl (IjlnK: ftf Costa 1980) El Salvador, E. tabaci , (CiSCooar xyoo, Serrano et al.l993) Florida, B. tabaci, (Dean & Schuster unpub.) Coleomeailla macnlat-a Louisiana. T. abut i 1 nnen.q . lenai Timber] akp (Watve & Glower 1976) Genus Cryptoanatha SB Asia, A. Woalumi, A. Mulsant spiniferus fClan.qpn K. Berry 1932) Sumatra. A. Woalumi, (Thompson & Simmionds 1964)

PAGE 51

Table 1.1 — continued 35 Taxa Location, Host, Reference Cr ypt ognat ha f lavlceps (Crotch) Cryptognatha nodiceps Marshall * Crypto lamus montrouzieri Mulsant Cycloneda sp. * Cycloneda sanguinea (L.) Genus Delphastus India, spiniferus . Q.. £itri, (Silvestri 1927) a Panama, A. Woglumi , (Thompson & Simmionds 1964) a Guyana, A. cocoiS f (Thompson & Simmionds 1964) a Florida, A. Woglumi . (Cherry & Dowell 1979) Hawaii, A. dispersus ^ (Kumashiro et al. 1983) Dominican Rep., £. tabaci ^ (Reyes et al. 1989) Florida, D.. citri ^ (Morrill & Back 1912); A. Woalumi . (Cherry & Dowell 1979); E. t abaci. (Dean & Schuster unpub.) Brazil, tabaci , (Link & Costa 1980) Colombia, £. t^h^Qx, (Caballero 1993) Dominican Rep., £. tabaci ^ (Alvarez et al. 1993) El Salvador, tabaci , (Escobar 1983, Serrano et al. 1993) Japan, A. spiniferus ^ (Thompson & Simmionds 1964) a USA, £. kelloaai . T. floridensis. jQ. citri . Q_. citri foT i i , (Gordon 1985) Colombia, A. malangae , (Caballero 1993) El Salvador, Awoalumi ^ (Quezada 1978; Serrano et al.l993)

PAGE 52

36 Table 1.1 — continued Taxa Location^ Host, Reference Delphastus catalinae Horn Jamaica, A, woglumi ^ (Thompson & Simmionds 1964) USA, D. riitri, citrifolii . (Thompson & 1964)a n. P. kelloaai. Simmionds Delphastus dlversipes (Champion) Delphastus paiildus LeConte Delphastus pusiiius LeConte Jamaica, A. woalumi ^ M. cardini . (Thompson & Simmionds 1964) USA, l. floridensis , (Thompson & Simmionds 1964) a Florida, D. citri ^ D. citrifolii, h. flocnnsusr (Muma et al . 1961) ; A. Woglumi f (Cherry & Dowell 1979) Dominican Rep., T. vaporariorum ^ (Alvarez et al. 1993) USA, l. Packard 1 , (Britton 1907)a Florida, D. citri , n. citrifolii , A. fioccosus ^ (Muma et al. 1961) ; A. Woalumi , (Cherry & Dowell 1979); B. t abaci . Florida, (Osborne et al, 1990; Hoelmer et al . 1993) Mexico, A. Woalumi , (Smith et al. 1964 Louisiana, 1. abutlloneu.g , (Watve & Clower 1976) Colombia, A. socialis . T. variabilis ^ (Gold & Altieri 1989) Eriopis connexa (Germar) Brazil, E. t abaci , (Link & Costa 1980)

PAGE 53

Table 1.1 — continued Taxa Location^ Host, Reference Exoplectra sp. Harmonia dimidiata (Fabricius) West Indies, ^. cocois ^ (Thompson & Simmionds 1964)3 Pakistan, E. tabaci . (CIBC 1983)C Harmonia sedecimnotata F. Java, A. dispersus ^ (Kajita et al. 1991) Hippodamia convergens Guerin-Menaville Louisiana, 1. abutiloneus , (Watve & Glower 197 6) Dominican Rep., £. tabaci , (Reyes et al. 1989) , (Alvarez et al. 1993) El Salvador B. tabaci ^ (Escobar 1983; Serrano et al.l993) Hyperaspis albicollis Gorham Panama, Woglumi ^ (Thompson & Simmionds 1964)3 Hyperaspis calderana Gorham Leis conformis (Boisduval) * Lela dimidiata Mulsant This is Harmonia dimidiata (F.) Panama, ^. Woalumi, (Thompson & Simmionds 1964)3 USA, A. Woalumi f (Thompson & Simmionds 1964)3 Florida, established in Florida (Gordon 1985); £. tabaci . (Gerling 1986) Lindoru.S lophanthap Blaisdale MenochiluR sp. Morocco, A. floccnsus . (Abbassi 1980) India, ^. phillyreae . (Rao 1958)3

PAGE 54

38 Table 1.1 — continued Taxa Location^ Host, Reference Menochllus sexmaculatus (F. ) India, R. eugenlae . (Rao 1958) a Pakistan, B.. t^hsLOl, (CIBC 1983)C Java, A. dispersuS f (Kajita et al. 1991) Mesochllis parcesetosa B. tabaci , (Gerling 1986) Microweisea castanea Mulsant Panama, A. Woglumi , (Thompson & Simmionds 1964)^ Genus Nephaspis Casey Nephaspis oculatus (Blatchley) = Nephaspi s aorhami Casey. = Nephaspi s amnicola Wingo Nephaspis picturata Gordon QllA abdominal i .q (Say) 011a v-niarum (Mulsant) USA, h. dispersus ^ A. cocois , (Gordon 1985) Nicaragua, A. cocoiS f (Caballero 1993) Florida, D. citri , D. citrifQlii, A. floccosus, (Muma et al. 1961) ; A. Woglumi , (Cherry & Dowell 1979) Hawaii, Honduras, Trinidad, A. dispersus (Kumashiro et al. 1983) Argentina, Paraleyrodes spp., (Teran 1989) Louisiana, 1. abuti Innea , (Watve & Glower 1976) Colombia, Aleyrodinae, (Caballero 1993) Florida, B. tabaci , (Dean & Schuster unpub.) Qenopia sauzet-i Mulsant Pakistan, Abarodpn.qi (Inayatullah 1984)

PAGE 55

39 Table 1.1 — continued Taxa Location, Host^ Reference Genus Scynmus SE Asia, (Clausen & Berry 1932) India, B.. t abaci , (Rahman (1940) C; B. euaeniae . (Rao 1958) a Florida, R. citri, n. citrifolii, £. perseae ^ (Muma 1961) Pakistan, h. barodensis. (Inayatullah 1984) Egypt, B. t abaci. (Darwish & Farghal 1990) Colombia, H. citi rfnl i i , (Caballero 1993); R. tabaci f El Salvador, (Escobar, 1983; Serrano et al. 1993) Scymnillodef? aeneus Sicard Jamaica, A. Woglumi , (Thompson & Simmionds 1964) a Scymni 1 1 ndp.q cyanescens Sicard Jamaica, A. Woglumi , (Thompson & Simmionds 1964) a * Scvmnill nde.q subtropi cus Casey Florida, Citrus, Aleyrodidae, (Muma 1961) Scvmnus coloratus Gorham Panama, AWoglumi , (Thompson & Simmionds 1964) a Scymnus aorhami Weise Panama, A. Woglumi , (Thompson & Simmionds 1964) a Scymnus horni Gorham Panama, AWoalumi |. (Thompson & Simmionds 1964) a Scymnu.s nubiiu.c; Mulsant Pakistan, A. baroden.qi .g , (Inayatullah 1984)

PAGE 56

Table 1.1 — continued Taxa Location, Host, Reference Scymnus smithianus Silvestri Scymnus syrlacus Mars . Scymnus thoracicus (F.) Scynmus pallidivestis Mulsant * Scymnus Punctatn.q Melsheimer Serengium cinctum Serenalum parcesetosnm Sicard Genus Zilus Mulsant Verania cardoni Weise Melyridae Col lops vittal-us Say SE Asia, ^. Woglumi f (Clausen & Berry 1932) Egypt, B.. t abaci , (Hafez et al. 1979) Panama, Woglumi f (Thompson & Simmionds 1964) a Egypt, ^. phillyreae^ (Priesner & Hosny 1940) a Florida, H. qILlI, (Morrill & Back 1912) a Nigeria, B. t abaci , (Gerling 1986)b India, Hcitri c (Timoteyeva & Nhuan 1978) ; A. barodens-i s^ (Shah et al. 1986); E. tabaci , (Kapadia & Purl 1989, 1992) USA, A. Wolguml f (Gordon 1985) India, citri , (Woglum 1911) a Arizona, B. t abaci , (Hagler & Naranjo 1993)

PAGE 57

Table 1,1 — continued Taxa Location, Host/ Reference Nitidulidae Cybocephaln.^ sp. Staphylinidae Paederus alf ierii Dermaptera * Labiduridae Labidura riparia (Pallas) Diptera * Anthomiidae Cecidomyiidae Cleodipllosis alevrodici Felt Java, Aleurocanthns (Causen & Berry 1932); A. Woalumi . (Thompson & Siininionds 1964) a; A. dispersuS f (Kajita et al. 1991) Indonesia, Alf^nrncanthns spp., A. destructor, (Kalshoven 1981) India, B. t abaci ^ (Kapadia & Puri 1989) Egypt, B. t abaci . (Darwish & Farghal 1990) Egypt, £. t abaci , (Darwish & Farghal 1990) Florida, E. t abaci , (Dean & Schuster unpub.) Florida, (Osborne et al. 1990) El Salvador, J. abutilonea , (Serrano et al.l993) Australia, h chaaientios , (Fulmek 1943) a Panama, L. aiganteus (Thompson & Simmonds 1964) a Lestodi plosis sp. USA, Aleurodes sp., (Barnes 1930)3

PAGE 58

Table 1.1 — continued 42 Taxa Location, Host, Reference Phaenobremla aphidivora Rubsqmen F Aphidoletes aphidimyza l Dolichopodidae Genus Condyl n.qtyl n.q * CondvlostyluR chrysoprasi Walker Drosophilidae Acletoxemus sp. Acletoxenus formosus (Loew) Egypt, B. t abaci ^ Moshtohor, (Abdel-Gawaad et al. 1990) Florida, B. t abaci ^ Schuster unpub.) (Dean & Florida, Aleyrodidae, (Muma 1961) El Salvador, £. t abaci . (Serrano 1978, Ardon et al, 1992, Serrano et al.l993) Florida, A. woglumi , (Muma et al. 1961, Buren & Whit comb 1979, Cherry & Dowell 1979) Sumatra, A. wolaumi . (Thompson & Simmonds 1964) a Crete, B. t abaci , T. vaporariorum , (Kirk et al. 1993) Portugal, A. Proletel la . (Silvestri 1934) a England, A. ielinekii , (Southwood & Reader 1988) Italy, A. iel ineki i . (Frauenfeld 1866) a; ^. phillyreae . (Thompson 1950) a France 2.. phillyreap , (Thompson & Simmonds 1964) a

PAGE 59

Table 1.1 — continued 43 Taxa Location, Host, Reference Acletoxenus indica Malloch Empididae Drapetis sp. Drapeti s ahesquiere-j Collart Muscidae SE Asia, wolgumi f (Clausen & Berry 1932) a Java, A. wolgumi ^ (Thompson & Simmonds 1964)^ Israel, t abaci . (Sussman 1988) Zaire, £. t abaci , (Mayne & Ghesquiere 1934) a Coenosia solita Walker Syrphidae Genus Alloarapta * Alloarapta obliqua (Say) Baccha sp. Baccha clavata F, USA, Aleyrodes sp . , (Fulmek 1943) a England, A. ielinekii f (Southwood & Reader 1988) Colombia, Aleyrodine, (Caballero 1993) Florida, Aleurodidae, (Weems 1971); £. t abaci , (Dean & Schuster unpub.) Hawaii, A. dispersus , (Kumashiro et al. 1983) Mexico, A. spiraeodeS f tabaci , (Ruiz 1993) Brazil, A. destructor. (Costa Lima, 1968) Florida, B. t abaci . (Dean & Schuster unpub.) Cuba, M. cardlni , (Thompson & Simmonds 1964) Baccha parvicorni s Loew Cuba, M. cardini f (Thompson & Simmonds 1964)

PAGE 60

44 Table 1.1 — continued Taxa Location, Host, Reference * Baccha lugens Loew. * Ocyptamus paravicornis (Loew) Syrphus corollae T Eupeodes corollae l Genus Toxomerus Florida, Aleyrodidae, (Muma 1961) Florida, R. t abaci ^ (Bennett unpub . ) Egypt, £. t abaci . Assiut, (Darwish & Farghal 1990) Colombia, Aleyrodine, (Caballero 1993) Paraaus ( Paragus ) serratus (Fab.) Java, hdispersuS f (Kajita et al. 1991) Hemiptera Anthocoridae Anthocoris nemorum (L.) Sweden, T. vaporariorum , (Ekbom 1981) * Cardi astethi]<^ assimilis (Reuter) Orius spp. £2riliS albidipenni s (Reuter) * Orius insidiosus (Say) Florida, E. t abaci , (Dean & Schuster unpub.) Italy, T. vaporariorum , (Arzone 1976) Japan, 1. vaporariorumf (Nakazawa & Hayashi 1977) Egypt, B. t abaci f (Hafez et al. 1979; ) Sudan, fi. t abaci , (Abdelrahman 1986) Illinois, T. abutilonea , (Dysart 1966) Louisiana, i;. abutilonea , (Watve & Glower 1976) Florida, £. t abaci , (Dean & Schuster unpub.) Orius maiusculus Reuter Italy, T. vaporarioruiTi f (Arzone 1976)

PAGE 61

Table 1.1 — continued Taxa Location^ Host, Reference Orius niger (Wolff) Italy, X. vaporariorum , (Arzone 197 6) £iriiis sauteri Poppius Japan, H. vaporariorum , (Kajita 1982) Berytidae * Jalysu.S wickhami Van Duzee Lygaeidae Geocoris sp. Geocoris ochroptems Fieber Geocoris pallens Stal * Geocoris punctipes (Say) Miridae Campylomma spp. Campy 1 ottittir diversicorni s (Reuter) Florida, B. tabaci , (Dean & Schuster unpub.) Egypt, B. t abaci f (Darwish & Farghal 1990) Honduras, £. tabaci ^ (Caballero 1993) India, B. t abaci , (Kapadia & Puri 1989, 1991) Oregon, Washington, ^. spiraeodes (Landis et al. 1958) Illinois, 1. abuti]nnea r (Dysart 1966) Florida, B. tabaci , (Dean & Schuster unpub.) Florida, citri, (Merrill & Back 1912) Dominican Rep., B. tabaci , (Caballero 1993) Japan, j;. vaporariorum ^ (Kajita 1980, 1984) Iraq, 1. luiiia, (Anon. 1977) ; T. Desmodii . (Anon. 1978) Syria, Btabaci . (Beingolea 1980, Stam 1983)

PAGE 62

Table 1.1 — continued 46 Taxa Location, Host, Reference Campylomma nicolasi Reuter Campylcneurf^ virani a (Herrick-Schaf fer) Cvrtopeltis modesta (Distant) = Engytatu.S modesta Cvrtopeltis tenuis Reuter Deraeocori s sp. Deraeocoris delaarangei (Puton) Deraenrnri q pal 1 enq Reuter Deraeocor-i s pattens Reuter Deraencnri .q punctui atn<^ (Fallen) Deraeocoris serenus Dgl. Sc.) Dicyphus tamanini i Wagner Macrolophiis caliai nn.qn.c; (Wagner) Macrolophiis costalis Fiet India, t abaci . (Kapadia & Puri 1989) England, A. -ielinekii , (Southwood & Reader 1988) Dominican Republic, £. Lah^Ql, (Serra, 1992) Japan, J. vaporariorum ,. (Kajita 1978) Dominican Republic, B. t abaci , (Serra, 1992) India, R. taiiaci, (Kapadia & Puri 1989) Turkey, (Yayla 1986) Israel, E. tabaci , (Susman 1988) Turkey, 1. vaporarinrnmr (Soylu 1980) Syria, £. tabani, (Stam 1983) Italy, T. vaporariorum r (Arzone 1976) Spain, X. vaporari nrnm, (Gabarra et al . 1988) Crete, B. t abaci , l. vapnrari nru^r (Kirk et al. 1993) Russia, T. vaporariorum ^ (Khristova et al. 1974)t>

PAGE 63

47 Table 1.1 — continued Taxa Location^ Host, Reference Phytocoris sp. Spanogonicus albofasciatus (Reuter) Egypt, £. t abaci ^ (Darwish & Farghal 1990) Arizona, H. abutiloneus , (Butler 1967) Nabidae Nab is spp, Nab is ferus (L.) Reduviidae Louisiana, 1. abutiloneuSf (Watve & Glower 1976) Illinois, X. abutiloneuS f (Dysart 1966) Coranus spiniscutis Reuter Egypt, B. t abaci , (Hafez et al. 1979) Harpactor costal i s Stal Rhinocorus iracundus (Poda) * Sinea diadema (Fabricius) Neuroptera Egypt, B.. Lsh^Ql, (Hafez et al. 1979) Hawaii, Aleyrodes sp., (Kirkaldy 1907) Florida, fi. tabaci , (Dean & Schuster unpub . ) * Coniopterygidae * Conioptery?^ vici n;^ Hagen Conwentzia sp. Florida, R. citrifol i i . (Muma 1967) California, 1. vaporariornnir (Gerling 1967) Conwentzia psociformi .q England, A. ielineki i , (Curtis) (Southwood & Reader 1988)

PAGE 64

Table 1.1 — continued Taxa Location, Host, Reference Chrysopidae Panama, Jamaica, Malaya, A. woglumi^ (Thompson & Simmonds 1964) a; California, T. vaporariorum f. (Gerling 1967) India, t abaci , J, riicini ^ (Thompson & Simmonds 1964) a Egypt, B. t abaci , (El Helaly et al. 1971)c Louisiana, 1. abutilonea^ (Watve & Glower 1976) Florida, Hcitri , (Morrill & Back) , A. woalumi ^ (Cherry & Dowell 1979) Brazil, E. t abaci , (Link & Costa 1980) India, S. t abaci , (B. tabaci . (Thomas 1932C; Husain & Trehan, 1933C; Reddy et al., 1985; Kapadia & Puri 1989) Dominican Rep., E. tabaci , (Reyes et al. 1989) ; (Alvarez et al . 1993) Java, A. dispersus , (Kajita et al. 1991) El Salvador, Awoglumi , (Quezada 1978, Serrano et al.l993) Panama, Aleyrodidae, (Zachrisson & Poveda 1993) AnisQchrysa Morroco, B. tabaci . (Mimeur f lavif rons (Brauer) 1946) c Brinckochrypa India, £. tabaci , (Roshman SCelggtes (Banks) 1940, Nasir 1947) c

PAGE 65

49 Table 1.1 — continued Taxa Location, Host^ Reference * Ceraeochrsys^ cincta (Schneider) Argentina, citrus aleyrodids (Gonz^ilez 1987) Florida, MGriseus , Mason et al. 1991) * Ceraeochrsysa cubana (Hagen) = Chrysopa cubana Hagen Florida, hf loccosus ^ (Muma 1961); £. t abaci . (Dean & Schuster unpub.) Chrysopa comanche Hawaii. A. dispersus. Banks (Kumashiro et al . 1983) Chrysopa cymbele India. B. tabaci, (Nasir Banks 1947) c Chrysopa formosa Morocco. B. t abaci ^ (Mimeur Brauer 1946) c Chrvsopa flava Morocco^ B. t abaci, (Mimeur (Scopoli) 1946) c Chrysopa lacciperda India. B. t abaci, (Kapadia Kimmins Puri 1989) Chrysopa oculata Say Illinois, T. abutiloneus, (Dysart 1966) Chrysopa scelestes India. B. tabaci, (Nasir Banks 1947) a Chrysopa perla L. Bulgaria, I. vaporariorum ^ (Babrikova 197 9)*^

PAGE 66

Table 1.1 — continued Taxa Location, Host, Reference Chrysoperla carnea (Stephens) = Chrysopa carnea Chrysoperla plorabunda (Fitch) * Chrysoperla rufilabris (Burmeister) = Chrysopa ruf nahri s * Chrysoperla externa (Hagen) = Chrysopa externa Hagen Mallada boninensi s (Okamoto) Hemerobidae * Micromus posticus (Walker) * Micromus subanticus (Walker) Egypt, fi. t abaci . (Hafez et al. 1979, Darwish & Farghal 1990, AbdelGawaad et al. 1990) Pakistan, £. t abaci . (CIBC 1983) c, ^. barodensis. (Inayatullah 1984) Israel, £. t abaci . (Or & Gerling 1985) Sudan, fi. t abaci. (Abdelrahman 1986) India, B, t abaci . (Kapadia & Puri 1989) Arizona, £. t abaci ^ Butler & Henneberry 1988) Canada, X. vaporarioruni f (Thompson & Simmonds 1964) a Florida £. t abaci , (Dean & Schuster unpub.) Argentina, citrus alyrodids, (Gonzalez 1987) Colombia, Aleyrodinae, L. aiaanteus ^ (Caballero 1993) Florida, £. t abaci , (Dean & Schuster unpub.) India, B. t abaci , (Kapadia & Puri 1989) Louisiana, 1. abutiloneus ^ (Watve & Clower 1976) Florida, E. tabaci . Schuster unpub.) (Dean & Florida, B. tabaci , (Dean & Schuster unpub . )

PAGE 67

51 Table 1.1 — continued Taxa Location^ Host, Reference Mantispidae Thysanoptera Phlaeothripidae * Aleurod othrips fasclatus Franklin r fasciapennis i HaplQthrip.S merrin i Watson rKarnyothrlpsI Karnyothrips sp. Thripidae * Franklinothrips vespif ormis (Crawford) Sericothrip.q trifasnia1-ii.q (Ashmead) Hymenoptera Ceraphronidae Aphonoomus fumipennis Formicidae Iridomyrme?^ anceps (Roger) Honduras, Aleuroalandulus sp. (Caballero 1993) India, £. t abaci ^ (Kapadia & Puri 1989) Florida, H. cltnL, (Morrill & Back 1912), Aleyrodidae, (Selhime et al. 1953, Muma 1961) Puerto Rico, A. f loccosn.q^ (Fulmek 1943) Worldwide, Aleurodidae, (Palmer et al. 1989) Cuba Florida Texas Nicaragua Brazil, Aleurodidae, (Moulton 1932) c Mississippi, A. aossypii ^ (Ashmead 18 94) a Hawaii, 1. abutil onpn.c; ^ (Kirkaldy 1907) a B. tabaci , (Gerling 1986) Java, A. dispersii.q, (Kajita et al. 1991)

PAGE 68

Table 1.1 — continued Taxa Location, Host^ Reference Lepidoptera Noctuidae Coccidiphaga scitula (Rambur) Pyralididae Nigeria, U.africana ^ (Mound 1965) a CrvptobTahe.q anidiella (Milliere) India, A. woglumi , (Thompson & Simmonds 1964)^ Malaya, Alenror.ant-hii.c; sp. (Clausen 1940) Tortricidae Clepsif? consimil ana (Hubner) England, ^. immacut atn.q (Caballero 1993) ^ As cited in (Mound & Halsey 1978) ^ As cited in (Ekbom 1981) c As cited in (Cock 1986) ^ As cited in (Gerling 1990) e As cited in (Serrano et al . 1992) ® As cited in (Hilje & Arboleda 1993) * predators found in Florida ** full names of whitefly hosts listed below Aleurocanthu? soini fprn.q (Quaintance) Aleuronanthnq woalumi Ashby Aleurode8 aossypi i (Fitch) Aleurndi nn.q cocois (Curtis) Aleurodi cn.q destructor Mackie Aleurodicu.q dispersus Russell Aleurol 0bil,s barodpn.<^i s (Maskell) Aleurothri flocn.g;n.c; (Maskell) Aleurotrfachehjff soci ai i .q Bondar Algyrptr^^chglys ielineki i (Frauenfeld) Aleyryr-erus chaaient i n.c; Fulmek Algyrygys chaaenti ns Nomen nudum AleyrodP.S proletPl (Linnaeus) Aleyrodfiff spiraenH^.g Quaintance Spiny whitefly Citrus blackfly Coconut whitefly Spiralling whitefly Sugarcane whitefly Wooly whitefly Viburnum whitefly Iris whitefly

PAGE 69

Table 1.1. — continued Bemisia argentifolia Bellows & Perring Silverleaf whitefly Bemisia t abaci Gennadius Sweetpotato whitefly Dialeurodes cltrif olii (Morgan) Dialeurodes citri (Ashmead) Dialeurolonga afrlcana (Newstead) Lecanoideus gjganteus (Quaintance & Baker) Metaleurodicus cardini (Back) Metaleurodlcus grlseus [ Aleurodicus griseus Dozier] Neomaskellia bergii (Signoret) Parabemisia myricae Kuwana Paraleyrodes perseae (Quaintance) Pelius kelloggi (Bemis) Rusostiama eugeniae (Maskell) Singhius hibisci (Kotinsky) Siphoninus immaculatus (Heeger) Siphoninus phillyreae (Haliday) Trialeurodes abutiloneus (Haldeman) Bandedwing whitefly Trialeurodes floridensis (Quaintance) Trialeurodes rara Singh = T. desmodii Corbett and 1. lubia El Khidir & Khalifa Trialeurodes ricini (Misra) [possibly = z. xara] Trialeurodes vaporariorum (Westwood) Greenhouse whitefly Trialeurodes variabilis (Quantiance)

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CHAPTER II PREDATION OF THE SWEETPOTATO WHITEFLY ON FIELD TOMATOES Introduction Since the 1986 outbreak of the "sweetpotato whltefly" In Florida greenhouses, large numbers of this pest have been present on vegetable crops, including field tomatoes. The feeding and honeydew damage, normally associated with high whitefly populations, can become quite pronounced on tomatoes. In addition, when young fruit are attacked, they later fail to ripen uniformly resulting in a condition called "irregular ripening" (Schuster et al. 1990). The viruses transmitted by this species are perhaps the most important threat to Florida tomato production (Kring et al . 1991). Certain lifestages of the whitefly make it particularly vulnerable to predation and parasitism. While the winged adults are active flyers, the four nymphal stages and the pupae are sessile. Eggs are deposited on a small stalk on the underside of tomato leaves. The first instar (crawler) has fully developed legs, yet it migrates but a few millimeters after eclosing before it settles at a particular location to feed (Mound 1978) . For the remainder of development, it is an immobile, translucent scale feeding on 54

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55 the underside of the leaf. These immature life stages are vulnerable to attack by numerous natural enemies . Little has been reported concerning predators of whiteflies in Florida. The earliest mention concerns the citrus whitefly, Dialeurodes iiitri (Ashmead) , and the cloudywing whitefly, Dialeurodes citrifolii (Morgan) , (Morrill & Back 1912) . Muma et al . (1961) gave an extensive survey of the natural enemies of the citrus whitefly in Florida. Predator induced mortality was also included in the evaluation of biological control of the citrus blackfly in Southern Florida (Dowell et al. 1979); however, no mention of predaceous species was made. The nearest reports of predation in the U. S. are in Dysart ' s (1966) study of the natural enemies of the bandedwing whitefly in Illinios and Watve and Glower's (197 6) study of the same pest on cotton and soybean in Louisiana. The first step in studying predation in the agroecosystem is to determine what predator species in a particular crop will attack the pest of interest (Whitcomb & Godfrey 1991) . Since little information exists concerning the predacious species attacking the sweetpotato whitefly in Florida, this investigation was undertaken to learn what predators exist and what potential contribution they might make toward the biological control of this new pest. Pest and natural enemy populations of arthropods were surveyed over the entire spring and fall seasons of Florida tomato

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56 production using an absolute sampling method (Southwood 1978), which was non destructive. Methods and Procedures Field survey . Sampling of populations of whiteflies and related predators was begun the fall of 1991 and conducted through the spring of 1993, spanning two years of two tomato crops each. Survey plots were situated on the edge of fields near border vegetation or fallow land and were buffered from normally sprayed plots by at least eight 48 in. spaced rows. Pesticide applications were limited to Bravo 720, for the control of fungal pathogens and Bacillus thuringiensi f> var. kurstnki . (javelin WG) , for the control of southern armyworm larvae, Spodoptera eridania (Cramer) . Sampling began with transplants of tomato cv. 'Sunny' and continued through final harvest for each crop. Plots consisted of six 30,5 m rows spaced 1.5 m apart. Plants were spaced 45.7 cm apart on raised soil beds covered with plastic film and supported with stakes (Kelbert et al. 1966). Plants that were to be sampled were separated by ten plants and were numbered in each row. A randomization table was used to select the sampling sequence of three plants per day that were taken twice each week throughout the growing season. One plant was sampled at each of three different times on each sample date (10:30 am, 3:30 pm, 10:30 pm) , in order to avoid possible diel feeding cycles of predators (Dumas 1962) .

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57 Sampling in the plots was accomplished with a whole plant drop trap (Fig. 2.1). The device consisted of a clear fiberglass cylinder, 0 . 95 m diameter and 1.22 m high, which was suspended over the plant to be sampled by a portable tripod. The top of the cylinder was fitted with a screen so that air could escape as it fell over the plant. The trap was positioned over the plant to be sampled for a minimum of 2 hrs. prior to the designated sampling time. This was done to allow for the normal dispersion of insects among tomato plants prior to the sample time and to diminish perturbation of the fauna that was present prior to sampling. In the event of rain, the trap could often be left in place until sufficient drying occurred to allow for the removal of arthropods . The tripod was secured with three nylon lines and metal stakes to avoid falling in the event of high wind gusts or storms. The height of the tripod was 3.15 m that allowed sufficient height above the plant stakes for positioning the trap and allowed at least 0.5 m clearance above a late season plant height (1 m 1.2 m) . The trap could be triggered remotely with either a manual trip line (10 m) or an automatic timer to avoid disturbances of predator behavior caused by human activity. The clear cylinder and tripod of the trap created minimal shading and were not in contact with the plant. Wire guides on the tripod legs, passing through eyelet's on the sides of the cylinder, assured that the cylinder fell perpendicular to the raised bed and made

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58 uniform contact with the plastic mulch surface. The falling cylinder formed a crease in the soil beneath the plastic mulch that helped assure that no arthropods escaped capture. Clear plastic windows and openings secured with organdy sleeves were provided on each side of the drop cylinder. The windows allowed physical access to the entire plant from either row. (Fig. 2.2). To collect each sample, the base of the cylinder was first inspected to assure that there was a complete seal with the plastic mulch. Then, a cardboard disk was placed over the top of the screened cylinder. Thus enclosed, the plant and cylinder were sprayed thoroughly with a synthetic pyrethroid, PT 2100 Resmethrin (Whitmire Research Laboratories Inc., St. Louis, MO). A minimum of one full minute was allowed for the insecticide spray to subdue the arthropods. The arthropods were then collected from the interior of the cylinder, the plastic mulch, and the plant with a portable DC hand vacuum (BioQuip Products, Gardena, CA) . The plant was shaken vigorously and dislodged arthropods were vacuumed. After this procedure was completed, the cylinder was raised and the plant and plastic mulch was again inspected for any remaining arthropods. During the fall of 1992 and the spring of 1993, many of the night samples were made with the aid of a mechanical timer (Fig. 2.3). At the designated time, the timer activated a 24 volt DC solenoid that released a lever that held the cylinder in place. When the mechanical timer was to

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59

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60

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Figure 2.3. Mechanical timer

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62 be used, the drop trap was positioned on the plant to be sampled the afternoon of the sample date. Extra care was taken to assure that the surface of the plastic mulch around the plant was smooth so that a uniform seal would take place. The next morning the arthropods were extracted from the plant following the routine procedure. Vacuum samples were taken to the laboratory and kept at 4°C for sorting into groups for storage and identification. Specimens were either pinned, stored in 70% ethanol, or stored at -70°C for serological assays at a later date. Some of the specimens were identified at the state museum in Gainesville, Florida and others were sent to the Taxonomic Service Unit of the USDA/ARS in Beltsville, Maryland for authoritative identification. Voucher specimens will be deposited at the state museum in Gainesville, Florida. Immature whitef 1 i es . Leaf samples were take from each plant to monitor the number of immature whiteflies. The upper leaves were used for consistency in monitoring the immature whiteflies. In the fall of 1991, only the terminal leaflet of the 7th leaf from the growing tip was taken; however, this proved to yield very low counts. Therefore, for the remaining seasons the terminal leaflet from the 7th, 8th, and 9th leaf from the terminal bud was sampled. Eggs and all stages of whitefly nymphs were recorded and leaf area was measured to determine the number of whiteflies per cm^.

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63 statistical Trf^atment The use of log correlation was proposed for the analysis of paired data by Legendre & Legendre (197 9) and was used by Gabarra et al. (1988) to analyze the association of populations of the mirid Dicyphus tamaninii Wagner with those of Trialeurodes vaporariorum Westwood. Adjustments made for the time lag between predator and prey populations allowed for closer correlation. An attempt was made to identify some of the relationships between field populations of the different prey found on tomatoes as well as selected predators. The Pearson product -moment correlation was applied to measure these relationships (SAS Institute 1989) . This correlation coefficient is to be applied to a bivariate normal distribution; however, the bivariate normal distribution is not common (Steel & Torrie 1980) . When the survey data were found to lack normality, an attempt was made to transform it using square root and logarithmic transformations. Normality of the distributions was tested using the Shapiro-Wilk ' s W test (Shapiro & Wilk 1965) . The probabilities given for the data by this test were not considered to be normal (P < 0.05). Therefore, the correlation analysis was not performed. When data cannot be transformed, Southwood (1978) suggests some coefficients of association that can be used

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64 without making assumptions about the respective distributions. A method which was chosen for the whitefly predator data is lai = 2 where J = the number of individuals of species A and B in samples where both are found present and A and B equal the total of individuals of species A and B, respectively, in all samples. This method gives a proportion of individuals occurring together throughout the sampling period. Values range from -1 representing no association and +1 representing complete association. Results and Pi Rnnssi nn Predator Survey The predaceous arthropods observed feeding on the sweetpotato whitefly on tomatoes in the field or in the laboratory or both are listed in Table 2.1. Of the 39 predaceous species reported to feed on whiteflies in Florida, 19 species were found on tomatoes. The observations made during this survey are in close agreement with the findings of both Dysart (1966) and Watve & Glower (1976), with the exception that very few nabids and no Delphasti pusillus LeConte were observed in this survey. In addition to the reported new findings, there are numerous other species that probably will be found to feed on some stage of the whitefly. Numerous Diptera, Dolichopodidae, Empididae, and some

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65 Table 2.1. Predaceous arthropods observed feeding on Bemisia t abaci in the laboratory or field. Predator Whitefly Life Observation Stage Taxon Staged Site^ Egg Nymph Adult Araneae Theridiidae Theridnl a opulent a (Walckenaer) * A F,L A Coleoptera Coccinellidae Coleomegil la maculata fusilabris (Mulsant) Cycloneda sanguinea sanauinea Casey Hippodami a convergens Guerin QUA v-nigrum (Mulsant) Dermaptera Labiduridae LabiduCf^ ripari a (Pallas) N L N Diptera Dolichopodidae Ukn. spp. A L A Syrphidae A,L L N A A,L L N A A,L L N A A,L L N A Allograpti^^ obi iqua (Say) L Baccha spp. l N N

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Table 2.1. — continued 66 Predator Observation Whitefly Life Stage Taxon Stage Site Egg Nymph Adult Hemiptera Anthocoridae Cardiastethus assimilis (Reuter) * nniiiS insidiosn.q (Say) Berytidae Jalysus wickhami Van Duzee* Lygeadae Geocoris punctipls (Say) Reduviidae Silifia diadems (Fabricius) * Neuroptera Chrysopidae Ceraeochrysq cubana (Hagen) * Chrvsoperl r externa (Hagen) * Chrv.snppria rufnabri.<=! (Burmeister) Hemerobiidae Micromus posticus (Walker) * Micronms suhantirn<; (Walker) * A,N A,N A,N A,N N F,L F,L E N A E N A N N N L F,L E N L L E N L L E N L L E N L L E N

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Table 2.1. — continued ^ A = adult, N = nymph, L = larva, E = egg b F = field, L = lab * first report of predation on Bemisla tabaci

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68 Drosophilidae were observed throughout the season; however, most of them are still awaiting species identification and their feeding habits need to be confirmed. Some infrequent species that were collected may also feed on whiteflies. Most are probably "tourist insects" passing through the sampling area. Archnida Acarina . Although a number of phytosiid species are found in Florida, very few predaceous mites were encountered in either the leaf samples or whole plant samples. This taxa was not sampled for in a manner specific for a survey of mites. Muma et al. (1971), estimated that the eighty-six species that they listed for Florida represent only half of the species existing in the state. Of the species present in Florida, only Euseius hibisci (Chant) has been reported as a predator of R. t abaci (Table 1.1) . However, this species was not identified among the mites collected during this survey. A ubiquitous omnivorious species, Typhlodromal i]s perearinus Muma was collected on a single occasion. Although, Muma (1971) reported on predaceous mites of citrus, the biology and habitat are little known for many species in the state, Muma and Denmark (1970) noted that whitefly crawlers and scale insects serve as alternative food for some species. Therefore, the potential exists for other whitefly predators to be found among the predaceous mites of Florida and they should be investigated further.

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Araneae . Among the many spiders seen with whiteflies in their webs during this study, the most obvious predator of whiteflies observed was the small species, J. opulenta . which strings silk lines across the underside of a single tomato leaf. Late in the season, adult whiteflies were consistantly seen in these webs with up to 20 30 per leaf. The remainder of the spiders collected in this survey still await identification. There may still be found hunting spiders that will feed on whitefly nymphs, as well as insect eggs, such as, salticids (Whitcomb & Bell 1964) or Chlracanthlum inclusum (Hentz) , which was found to feed on eggs of Anticarsia gemmatalis Hubner by using radioactive labeled prey in the field (Buschman et al. 1977) . Whiteflies would appear to make a small meal for most spiders. However, Southwood and Reader (1988), found that spiders were the main predators of Aleurotrachelus ielinekii (Frauenf.) on Viburnum bushes in England. Predation was limited to adult whiteflies for these two web spinners, Linyphia triangualris Clerck and Met a seaementata (Mort . ) . Spiders deserve a treatment apart from that of the class Insecta. All spiders are predaceous and most can prey on almost any insect (euryphagous) . They are ubiquitous and remain at fairly constant numbers in all kinds of habitats regardless of insect densities (Riechart 1974) . Although spiders do not exhibit a functional response to changes in populations of prey, they can contribute to the stability of prey populations. Through the consistent presence of sheer

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70 numbers, the diverse spider complex can reduce pest numbers (Riechert & Lockley 1984) . This may fill a somewhat unique ecological position from that of insect predators and one that needs further study. There are cases where spiders can be an effective agent in maintaining stability in the agroecosystem (Mansour et al, 1983). Riechert (1990) attempted to demonstrate prey control by the assemblage of spiders found in an agroecosystem. It was concluded that the collective spider fauna may serve as a buffer by limiting the potential exponential growth of pest populations (Riechart 1992). Wise (1993), in his review of the ecology of spiders, concludes that spiders may very well exert considerable density-independent mortality on insect pest populations; however, more evidence is needed from well-designed field studies . Insecta Coleoptera . As a group, Coccinellidae has the greatest number of reported whitefly predators (Table 1.1). Although Gordon (1985) recognizes primarily three host groups for coccinellid species, scale insects, mites, and aphids, he asserts that when preferred food is not available, many species are known to feed on other insects. The ladybeetles listed in Table 2.1 of this survey are classified primarily as aphid feeders. Nevertheless, coccinellid adults have been shown to be attracted to an artificial honeydew (Nichols & Neel 1977) . Recently, both adults and larvae were shown to be arrested by and to feed on honeydew (Heidari & Copland

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: 71 1993) . Apparently, they also will feed on whitefly nymphs when they encounter them while feeding on honeydew and while searching areas of honeydew deposition. The small coccinellids, Delphastus pusillus LeConte and Nephaspis oculatus Casey, are whitefly predators that are found in Florida (Table 1.1). They were conspicuously absent from our survey samples on tomatoes . They are species most often found in arboreal habitats (Osborne, personal comm.), although C pusillus will feed on B. t abaci when released on herbaceous plants (Heinz et al. 1994) . In view of the extensive records of coccinellids that attack whiteflies (Table 1.1), this group presents potential for further investigation and trial introductions. Staphylinids were the only other predaceous beetles that were found to any extent during this survey. Tinolthus longicornis Stephens, Z. acummus Erichson, and At he t a coriania (Krantz) were found on the foliage late in the season, but were not observed feeding. A. coriania was previously reported on tomatoes by Miller and Williams (1983) . Only one report of whitefly predation by staphilinids exists, and that was from Egypt (Table 1.1). Two species, Discoxenus sp. and Oxypoda japonica Sharp, are reported feeding on armored scales on citrus in Japan (Nakao 1962) . It is very likely that among this large group of predaceous insects, which exhibit such diverse feeding habits and are known to feed on other homopterous insects, those will be found which feed on whitefly nymphs.

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72 Dermaptera . The cosmopolitan species Labidura riparia (Pallas) was seen regularly after mid season. Apparently, some time is necessary for them to colonize the soil beneath the plastic mulch on the raised tomato beds after fumigation occurs just prior to planting. A single report of predation of E. t abaci exists from Egypt (Table 1.1) . However, Dean and Schuster (1958) reported that this species also feeds on scales and crawlers of the Rhodes-Grass Scale Antonina graminis (Mask.) in Texas. In Florida, these predators were found to be active in the foliage at night and early morning and were credited with the greatest amount of predation of lepidopterous larvae and eggs occurring in Florida soybeans (Buschman et al . 1977) . Likewise, Lriparia was found to demonstrate a functional response to increases in noctuid prey in South Carolina (Price & Shepard 1978) . During this study nymphs of this species were maintained for two weeks on leaves infested with B. t abaci . However, they did not complete development on this diet. Diptera . A number of dipteran species occur in Florida that are reported as predators of whiteflies (Table 1.1). Members of the group, Cecidomyiidae, were not found preying on whiteflies during this survey. Mound and Halsey (1978) expressed doubts about the early records of this group as predators of aleyrodids . Harris (1990), indicates that the only species of Diptera known to feed on armored scales are cecidomyiids, but that evidence is sparse and records are

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73 infrequent. This is a group that needs additional study to ascertain feeding habits and hosts. Adult dolichopodids were seen throughout the season in the field. A number of species were reported in a predator survey done in Florida soybeans (Neal 1974) . They are easily disturbed and their rapid and frequent flight behavior makes them difficult to observe feeding on prey as small as whiteflies. They were not observed on the underside of tomato leaves where the immature stages of the whitefly develop, but generally are found on the upper side of tomato leaves. Condylostylus species have been reported feeding on citrus whitefly adults (Table 1.1). Members of this genus may have been feeding on whiteflies but, at the time of this writing, collected specimens are awaiting authoritative identification . Among the Drosophilidae, members of the genus Acletoxemus are known to feed on whiteflies (Table 1.1). The species observed during this survey were associated with ripe and rotten fruit and not observed to feed on whiteflies. Ashburner (1981) , gives examples of entomophagous Drosophilidae All members of the family Empididae are said to be predaceous on small insects and mites and are abundant in moist places (Curran 1934, Borror et al . 1981) . Thus far, they have not been seen feeding on whiteflies in the field; no observations were made in the laboratory with whiteflies. This group also needs further study.

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74 Adults of the family Syrphidae frequently were found hovering about tomato plants in the field. The predaceous larvae of Allograpta obliqua (Say) were found on tomatoes and what appears to be Baccha clavata Fabricius or another Baccha sp. Some specimens that were collected in the field and allowed to complete development on whiteflies in the laboratory still await identification to species. Larvae were most often found associated with aphids, although whiteflies were also present. There are various reports of predation on whiteflies (see Table 1.1), Hemiptera . This order contains the most species of predators found attacking whiteflies in this survey. Anthocorids appear to be an important predator of the whitefly on tomato in Florida. Qrlus insidiosus (Say) was the most consistent and abundant predator associated with the whitefly throughout each of the tomato seasons. Both nymphs and adults feed on eggs, larvae, and pupae of the whitefly. Nymphs were regularly seen on the undersides of tomato leaves infested with whitefly nymphs and eggs. Nymphs were able to complete development on a sole diet of whitefly nymphs. There are wide reports of Qrlns. sp attacking whiteflies (Table 1.1) . The anthocorid Cardi a.ql-pl-hnc: assimi 1 i s (Reuter) , was also found in association with whiteflies on tomatoes. Nymphs maintained on whitefly diet in the laboratory were also able to complete development. There is very little reported in the literature concerning this genus of

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75 anthocorid. Although the numbers of £. assimilis encountered did not approach those of Q. insidlosuS f this species demonstrated an equal capacity to capture and consume whitef lies . Another species that was occasionally collected was Lasiochilus pallidulus Reuter; however, it was not observed feeding on whiteflies. Q.. insidiosus , £. assimilis ^ and L. pallidulus were the most common anthocorids found in Florida soybeans by Neal (1974) . Confirming that these species are adapted to agroecosystems in Florida. A few solitary specimens were collected, such as Xylocoris galactinus (Fieber) , which were most likely transient. The stilt bug, Jalysus wlckhami Van Duzee, mistakenly referred to as Jalysus spinosus (Wheeler & Henry 1981, Wheeler 1986) , has been reported as a pest of tomatoes (Phipps 1924) . This stilt bug was reported to cause blossom drop in tomatoes as a result of feeding in blossom buds and on the fruit stem. Elsey and Stinner (1971), found that, when fed tobacco alone, 100% mortality occurred. Further investigation proved that this species is omnivorous, requiring insect prey to develop and reproduce normally; therefore, it was released in tobacco to control lepidopteran eggs. This species was found to feed readily on whitef ly nymphs and there was also no apparent damage caused to tomatoes. However, it was only seen late in the season of the spring tomato crops and the numbers were never great enough to exert much impact on whitef ly populations.

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76 Another berytid, Metacanthus tenellus Stal, was more abundant in the late spring tomato crops than J. wickhami . Specimens were held for observation with whitefly nymphs and were not found to be predaceous . A lygaeid, (Say) , was found at times during the seasonl surveys and fed on whitefly nymphs when brought into the laboratory. However, they were never very numerous in the field. Cohen and Byrne (1992) found that G. punctip es was an active predator of B. t abaci in the laboratory. The family of hemipterans known as plant bugs, Miridae, are carnivorous secondarily, occasionally acquiring nutrients from sources other than plants (Henry & Wheeler 1988; Cohen 1990) . A number of mirids are reported to feed on whiteflies (Table 1.1) . The most abundant mirid found on tomato was the tomato bug, CyrtQpelti modesta (Distant) . At times, this species can be a pest of tomatoes by girdling stems while feeding (Tanada & Holdaway 1954) . Such feeding damage was observed during this survey; however, the damage was slight and did not appear to cause weakening or breaking of stems and blossom drop as has been reported. Predation by £. modest a was first noted on corn earworm eggs and larvae by Rosewell and Smith (1930). Illingsworth (1937), while studying this mirid as a pest on tomatoes, also found that it fed upon aphids, mealybugs, and lepidopteran eggs and caterpillars. Parrella and Bethke (1982) investigated the use of modesta as a biological control agent against the leaf miner

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77 Liriomyza sativae Blanchard on tomatoes . They found that no nymphs completed development when given tomato stem cuttings alone but, 100% completed development when given lepidopteran eggs and tomato cuttings. During this survey, Q. modesta was held on tomato leaves infested with whitefly nymphs. Just as Illingworth (1937) reported, the mirids were found to be "decidedly wary and not at all gregarious". They are easily disturbed and continue to move rapidly with brief pauses. They were not observed to feed on whitefly nymphs . They appeared to remain primarily on the stems and did not seek out whitefly nymphs on the undersides of leaves. Although, they did puncture whitefly nymphs while probing the tomato leaves during confinement, longer term studies on plants need to be done to determine the extent of predation. Their size, behavior, and green coloring made them difficult to observe on tomato plants; therefore, they were not observed feeding on whiteflies in the field. Other mirids identified thus far in this survey are CeratQCcap,'^U,=! punctnl Reuter and Jobertus chrysol ent rii.c; Distant. It is suggested that species of Ceratocapsus are primarily predaceous (Wheeler & Henry 1978, Henry & Wheeler 1988) from feeding observations of homopterans. J. chrysolectrus, is a Neotropical species recently discovered in South Florida (Henry & Wheeler 1982) . These authors state that it has been found on eggplant and squash infested with leaf hoppers and suggest that it is at least partially

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78 predaceous . It was collected on tomato and squash during this survey. Feeding trials have not been conducted on these species, as yet; however, it is likely that they will both be found to feed on whitefly nymphs. Another mirid, Spanoaonicus albof asciatus (Reuter) , has been found preying on noctuid eggs in Florida soybeans. This species was reported to feed on the bandedwing whitefly in cotton by Butler (1967) . Although this might eventually prove to be an additional mirid whitefly predator occuring in Florida, it was not encountered in this survey. However, Halticus bract at us Say was regularly seen on tomatoes in these studies and previously has been reported as a predator of velvetbean caterpillar eggs in soybeans (Buschman et al . 1977) . Although fl. bractatus was not observed as such during this survey, it is possible that this mirid will be found to be a predator of whitefly eggs or nymphs. Deraeocoris nubulQSUS (Uhler) was found to be a significant predator of noctuid eggs in cotton and soybeans in the southeast US (Snodgrass, 1991) . This mirid should be observed for predation on whiteflies as well. The Miridae of Florida are not very well know (Henry & Wheeler 1982). Hagler and Naranjo (1993), with the aid of an immunoassay specific for sweetpotato whitefly eggs, recently discovered that Lygus hespern.q Kight was the most abundant whitefly predator on cotton in Arizona. Such assays may reveal a number of unsuspected predators among Florida's poorly known mirids.

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79 Encounters with nabids were infrequent and they were not observed to feed on whiteflies in the field. The most abundant nabid found in this survey was Nab is capsiformis Germar. It is listed among the most common species occurring in row crops in the Southeastern US. (Elvin & Sloderbeck 1984) . Ekbom (1981) reported that feeding trials with Nabis sp. on whitefly nymphs indicated that only 8% of these predators were able to complete development . Only three reports of whitefly predation by nabids are presently known to exist (Table 1.1), although there are numerous reports of predation on leafhoppers, aphids, lygus bugs, mirids, early instar lepidopterans and lepidopteran eggs (Neal 1974) . All life stages of Reduviidae are considered to be predaceous (Froeschner 1988) . Among the larger reduviids, only Sinea diadema (Fabricius) was encountered with any regularity in this study. Nymphs of this species fed on whitefly nymphs and adults in the laboratory. This has not been confirmed in the field, although, it would be reasonable to assume that the apterous nymphs of this aggressive group of predators would feed on smaller prey and eggs until they could develop sufficient size and mobility to successfully attack larger prey. Neal (1974), observed adults of this species feeding on velvetbean caterpillars, Mexican bean beetle larvae, a nabid, a soybean looper, and an adult green cloverworm in soybeans in Florida. Late in the spring seasons, Empicoris sp. were found to be quite common in the tomato field. Little is known of the

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80 feeding habits of this species and the group currently needs revision (T. J. Henry, personal communication) . This small species and another reduviid, a Barce sp., were occasionally collected. Both are very delicate and are easily damaged when collected. When brought into the laboratory, specimens would not feed at all and died within a few days. Both of these species are highly cryptic. Since they were only abundant late in the season, when the tomato plants were large and densely foliated, it has not been possible to confirm their prey. Neuroptera . Coniopterygidae were not encountered in the tomato plots. Members of this family of predators are known to prey on whiteflies (Table 1.1). However, they may be mainly of arboreal habitats in Florida (Killington 1936, Muma 1967, Stange 1981) . This family has been poorly studied (Drea 1990) and further investigation could reveal useful information related to whiteflies. Ceraeochry.sa cubana (Hagen) was the most abundant chrysopid found feeding on whiteflies during this survey. This trash bearing species has been reported from various habitats and hosts in Florida (Muma 1961, Buschman et al. 1977, Neal 1974) and, recently, on cotton in Brazil (Gravena & Cunha 1991) . Formerly known as Chrysopa cubana Hagen, Adams (1982) recently revised the group, placing this species in the current genus. He reported that this is the most abundant neotropical chrysopid genus. Muma (195 9) reported this as the most common green lacewing found on citrus in

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81 Florida. He also conducted feeding trials with this lacewing on various prey associated with citrus in Florida (Muma 1957) . Other members of this genus have been reported in Florida. Ceraeochrysa cinta (Schneider) was reported feeding on the whitefly Metaleurodicus griseus r Aleurodious griseus Dozier] (Mason et al . 1991) and on the mealy bug Plotococcus eugenlae (Minter) (Eisner & Silberglied 1988) . £. valida (Banks) and £. sanchezi (Naves) were reported on armored scales in citrus (Muma 1959, Muma et al. 1961) The next most abundant green lacewing collected in this survey was Chrysoperla externa (Hagen) . This is also a common species in the neotropical region ranging from Florida to Argentina (Gonzalez 1987) . It has been evaluated and summarized recently for potential as a biological control agent in tropical and temperate regions of Central and South America (Albuquerque et al . 1994). Chrysoperla rufilabris Burmeister and Chrysopodes collaris (Hagen) were rarely encountered. The larvae of all of these species feed voraciously on whitefly nymphs in the laboratory. rufilabris is available from commercial insectaries for augmentative releases. The hemerobiids, Micrnmn.q post i ens (Walker) and M. SUbanticus (Walker) , were found on aphids late in the spring seasons. When brought into the laboratory, they fed on whiteflies and could complete development on whitefly nymphs. The adult brown lacewings fed on the same sugar and yeast diet that was used to maintain adult green lacewings. Drea

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(1990) , states that the importance of members of this family as predators of aphids are underestimated and like many Neuroptera more study needs to be done on specific prey. Thysanoptera. The flower thrips Frankliniella tritici (Fitch) and £. occidentalis (Pergande) were common in the samples collected. The black hunter, Leptothrips mali (Fitch) , was frequently found associated with the flower thrips; however, no thrips were observed feeding on whiteflies. However, authoritative identifications and gut assays may reveal some thrips predation in the future. The predacious thrips Aleurodothrips fasciapennis Franklin and HaplQthrips merrilli Watson reported on Florida citrus were absent from the samples taken in tomatoes (Table 1.1). Hymenoptera . There were no wasps or ants that were found to be predacious on whiteflies. Formicidae were also not found to interfere with predators as has been reported in some cases (Dreistadt et al. 1986; Tedders et al . 1990). Unlike the finding of Neal (1974) and McDaniel and Sterling (1979), the imported fire ant Solenopsi s invicta Buren was not abundant in this survey. The reason that members of Formicidae were seldom encountered may be due to the plowing and fumigation of the soil that is practiced prior to each planting of a tomato crop on the research station.

PAGE 99

83 Population Dynamics Whitef lies . The weekly means of adult whiteflies and immature life stages for the four seasons surveyed are represented in Figures 2.4 through 2.7. Each season displayed some distinct characteristics in the population dynamics of the whiteflies. There was also no difference (ChiSquare = 0.559, df = 2, P < 0.05) found in the mean number of whiteflies found at the different diel sampling times (Wilcoxon rank sums, SAS Institute 1989, 282-284) . During the spring crops, the weekly mean populations of whitefly adults remained below 50 per plant until the 7th or 8th week building rapidly the last 4 to 5 weeks. The whitefly sample means for the spring 1992 were very large, 3 to 3.5 times greater than in other seasons. The spring of 1992 had a maximum mean number of 970 adults per plant at the 12th week, while the spring of 1993 had a maximum mean of only 250. This amounted to 3.9 times more adults and 4.9 times more immatures . While studying the bionomics of three species of whiteflies on cotton in California, Gerling (1967), saw large differences in abundance from year to year. However, a reason was not found for these large fluctuations. Although, the fall seasons had smaller whitefly populations than either spring crop, populations began to increase earlier and reach their peak earlier than in the spring. In each fall season, the whitefly adults peaked

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(9=N) ^UTSjd I (as+) s:}inpH m. unaw 4J s cr> e CTi -H d ^ 1 c m 4-1 CJ p [£1 c Q CTi a iH M c 1 0) o p to G a 0) (1) -p •o cn CM m >i V (0 y. 0) 4-1 CO dj (U (U S 4-) O -H P (0 e o 4-1 4-) O X! mbe ray 3 a G ns; C m 0) c s o (8T=N) (3S+) uiuiT ueaw CM
PAGE 102

86

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between 140 and 160 per plant at about the 9th or 10th week. During the fall of 1992, the mean adult population fluctuated, while the immature life stages remained constant and below 1 per cm^. Only during the fall of 1992, did the number of immature stages not correlate well with changes in the adults. Arthropod orders . In Table 2.2, the total number of arthropods collected is given for each order each season of the survey. As was shown above for whiteflies, the general arthropod fauna was much more abundant in the spring crops than in the fall, particularly in 1992. Because the length of sampling time varied slightly with each season, sample means are used to make comparisons between seasons. Overall, the total means did not vary that greatly between the two fall seasons and between the two spring seasons; however, extreme seasonal fluctuations can be seen among many groups. For example, in the spring 1992 season, an influx of thrips early in the season was several magnitudes larger than was seen any other season during the survey. Also, greater numbers of Psocoptera and Coleoptera were trapped during the spring of 1993. There were also large numbers of southern armyworm and tomato pinworm larvae that occurred during this season. Large numbers of parasitic wasps developed on the lepidopteran larvae present at the time. The coleopterans were primarily lathridiids, or the minute brown scavenger beetle, and psocopterans, which are primarily detritus and fungus feeders (Borrer & De Long 1981) .

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0) p si +J •H > T3 i -u C 0) m -d (U m 4-) nJ c iH -H <1) »-i CO i 4-) <0 (0 CO G o CO C ^^ o 0) T) M -ro c a: x; o (t 4J o (t c -H 0) CO T3 r^ -H e o d c ffl -H f-i >1 rO rH C m O X> in r~ CM CTl in cr> o c» CTs ID oo CM rH rH CM rH CM in LO oo rH LO rH CM rH in rH LO O rro O rH CJ^ ^ 00 CM 00 rU3 CX> rH CM LO 00 o rH 00 00 00 O '=1' 00 oo 00 CM rH <^ CM rH t~~ in oo rH 00 CM T-H CM 00 in rrH 00 rH r• O CM ^ 00 in rCM rvo oo O o CTl C» CO CM o cy> 00 cr> O in o o 00 00 00 OO rH o CM IT) cx> O rys) 00 «3 CM 00 CM CTl rH 00 O 00 LO oo 00 VD in in CM LO 00 U) O lO rH o CM oo CM CM oo LO 00 CM rH in rH o 1^ rH CM CTi rH CM o 00 in cr> CM rr-CTl ro rCO ^ o iH O in r CM CM 00 in CM rH rH 00 CM 00 VD oo CM o 00 <-i rH VD rH o CM CM 00 in 00 o CJ^ CM O rH r~ -H 4J m Q) o Ti T3 0) 4J u O 03 XI -H cc 03 a Q 4-1 03 T) s-H CU o x; 03 03 rH rH rH pa Eh O o o < O < o 03 03 M M 03 0) CU h 4J 4-) i CU 03 ^4 0) 4-1 a >g 4-) -H o sh a g g 1 -G C o CO OJ CU CO

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90 (0 u 0) M O a) CO a; p li c M-l te X) -H (1) xi T3 CO c >H (0 •0 O Q) c C (CJ -H a CO J-> c T3 o -rH c CO ph 0) m m m ot an 0) 4-> ^ M P •-{ na M 0) X) o ^ 0) CO -P +j m 0 CO Q) -H CO m (1) er CO -p p CO G 0 0) G -p o -H 0 o o xi c -0 >1 Q) -p T3 c d tw (U 0) Q) CO 3 4-) O C -H G -H -H P c 0) O M (J 1 an m >i als 1 0) -p •H 0 -p p (N a, jC 0) Eh o * Eh * 4:3 *

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Planthf^ight . The height of the tomato plants was recorded for each sample during the last three seasons of the survey in an attempt to determine what relationships might exist between populations of arthropods and changes in plant phenology (Figs. 2.8, 2.9, and 2.10). Adult whiteflies increased exponentially over time during the two spring seasons (R ^ = 0.96 and 0.93, 1992 and 1993 respectively) and correlated well with plant growth (r = 0.9 and 0.87, 1992 and 1993 respectively; P < 0.001). The increase in spiders also correlated well with increases in plant height (r = 0.9, 0.94, and 0.87, 1992 spring and fall and 1993 spring, respectively) , and was highly significant each season, P < 0.001. The best fit for spiders was nonlinear and revealed an exponential increase occurred for a period of time each tomato season {R ^ = 0.87, 0.93, 0.81, 1992 spring and fall and 1993 spring, respectively) . The increase in a whitefly predator complex made up of combined counts of anthocorids, lygaeids, coccinellids, chrysopids, and hemerobiids, also were correlated significantly with plant growth for the successive crops during this survey (r = 0.88, 0.7, and 0.7, P < 0.05, spring and fall and 1993 spring, respectively) .

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92 (uiD) :m5Taii :;uB-[d ub8w uio / suiuiT pue q.uexd / saoq-Hpaad ueaw 0) u

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93 o CM o o o I o o I o -H O CD (U c •a (13 0) Cn S-l ^( < • 1 cn x: 4-) c m i T — 1 — I — [ — I — I — r CNI U5 ' ' ' 1 ' ' 1^ CM O C T3 C u/ ' *u 1 1 (d i 0) c O 4-1 a M to u e 4-1 o o 4-1 S-i 4-J T3 i CQl (0 D S-l C i-l a CO C c (0 OJ 3 6 C c uio / suiuiT pu^ :iuHX<3 / sjco:iHpa:rci ueaw 4-1 x: CP -H OJ x: 4J c to a c to 0) t a ^ (0 U-I (U ij-i 4-1 O •r4 x: s-l
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94 (uio) q.t[5Taii q.uHxd ueaw o CM o o i-H _i L. o oo o o o ^ CM I I I I I I I I I 1 0) (0 0) -H C m o 1^ CM W 0) 4-1 M <4-l 0) M P e e H 0) 4-) 4-1 O CO u o p to T3 0) a 4-1 o u (U XI c c 0 e 4-) -H (U P C (0 iH G (0 UIO / sunuT puH :;uBic3 / sjo:;Hpaac3 unaw CN 0) tn H o CM e u u 0) a CO CP Cn 0) XJ c m CO a >i u CO c p pal u X) 6 c G 0) 4-) -H a o +j c (U T3 (0 M m p CO 0) o +J (tS e o p o 0) m a CO c c o CO u Q> XJ -H a CO o 0) c m 0) e • 4-1 C CTl o m ^ 4->

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Predators . Seasonal incidence of predators which have indicated a possible relationship with whiteflies are shown in Table 2.3. Again, because the length of the sampling period varied slightly each season, comparisons of populations must be made by the use of sample means. As has already been indicated for whiteflies and arthropods, in general, a greater number of predators were present in the spring crops than in the fall. The combined means indicate that during the spring of 1992, there was large number of predaceous arthropods present. No explanation can be given for the higher numbers of spiders which were present in the fall of 1992. Hemerobiids were only found in the spring crops . The only predators present with any consistency each season of this survey were Q. insidiosus , £. i^uhana and dolichopodids. The extent of whitefly predation by Dolichopodidae does not appear to be very great at this point and species have not yet been determined (Table 1.1). Q. insidiosus was the most abundant predator during the survey. The greatest numbers were seen in the spring seasons and a large population was present in the spring of 1992 which was greater than 3 times the mean number present in the spring of 1993. Fall numbers of Q.. insidiosus were proportionately low, with only 2 to 3 percent of the mean number which were present in the spring of 1992 collected in the fall of 1991 and 1992, and only 6 to 10 percent of those present in the

PAGE 112

<0 Xi 4J • m o >i C 0) o > -p u c 0) to X5 03 0) m +j c &i H G CO 0) o -p (0 •d e 1 o Q^ >i CO (d c 4J >^ c o o 4J (0 "O u ^ p T5 0) +J -H O cc o Eh K C o m EH '3" LT) CD 00 CM C30 CM o IT) CM O 00 G m r~ CTl 00 OO iH O V£) CM O O O o o o o CX) VD O >H O O O O CTl (» CTi CM OO LT) O CM O O CO CX) IT) ^ ^ H C» iH O LO • • • • o o o o CM CM CM ro CTi 00 ^ ,H fO VD IT) rH O ^ O O O O CM 00 00 CM CM CM O rH O O O O O O CT) r-l ro o CM o o o o LO 00 rH iH CM lO ro OO iH CO V. (T. cc ^3 r O CO rH CO CU CJ G c O CO (T3 c G (TJ (TJ o O (TJ 0 -H H g CO u U P O • * Ul a o cji u U u cu (TJ (TJ n G -H (TJ to -H >H (TJI £1 G (TJ >H (U a, £1 p O 3 >C CO cj^ cu >1 g U Ul Ul 00 00 CM UO 00 rH O CM O O O O 00 00 LO rH CM O 00 CM rH LO CM O OO cu (TJ -a -H T) -H &> O O O Q

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a •H M &. CN (0 CN CD c -H a CO (0 -p o Eh C o 0) (T3 -H a g • • • Cn • 0) 2] SI c/^ >i a IS 4-) ;2: CO 0) o •H a >i CO o O CM CM o 00 n CM o o o CM CM CM • rH o o o o O O O cy^ rm CM IT) in tc -K CO to -P o Eh CO d) o H Q 1 CO CO -H >i &> (0 M ,-H CO fO -* •1— ' (J tri \\j \V \iJ r* 1 1 -M H f-\ \J Ip d) CO O iH U m (0 (0 d) 4-) O
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spring of 1993. There was no statistical difference found between the weekly mean number of Q.. cubana present each season (chi-square = 2.29, df =3, P = 0.5) (Wilcoxon Rank Sums, SAS Institute 1989, 282-284) . During each season, increases in populations were seen for different groups of predaceous arthropods which appear to correspond to changes in whitefly populations. By graphing the concurrent populations of various alternative prey, comparisons can be made between a range of possible predator response combinations for the season. The population dynamics of the predator and possible prey alternatives can be partially evaluated in this way. Graphical representations of the population of the most abundant predator species and alternative prey for each season of the survey are presented in Figures 2.11 through 2.29. The prey presented are combined whitefly immature stages, aphids, thrips, and lepidopteran larvae, although at times collembola and psocoptera were abundant as an alternative prey. The predators represented are those that were present in sufficient numbers to graph for that particular season.

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100 Predators/ Plant uD IT) ID IT) in in

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101 oooooooooo llllllllllllllllllllllllllllllllllllllllllll Predators / Plant CTlOOr-VOLD'^fOCM rHOOOOOOOO o o I 1 1 1 ' I " " I ' " ' I " LO O LO O CM CM iH iH (yioor-ir)'^fOCMrH C o >i -H 4-1 (0 CO o p m E o p T) (U >i m CO c

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102 Predators / Plant oooooooooo iiiiliiiil mil mil I mil mill iilii I ill II iliiii I I I I I I I I I I I I I I I I I 11 I I I I I I I I M I 1 1 I OOOOOOOOOO tOOlOOlOOLOOLO o O O o iH CO nliiiilii o o o o o o o r-'XlLO'^OOCNiHO 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 VD IT) ^ OO CN i Eh c o >1 0) M (X > -P G 0) p . -H CM T3 ^ 0) P O 0) iH 0) CO ) O00<^'^C\IO00<^'^CMO CM ,H rH .H i-H

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103 00 >X) '3' CN OD ^ CN Predators / Plant 00 >X) CM CO CN CNirHr-HiHfHiHOOOOO 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 M 1 1 1 [ r 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 oooooooooo LO o LO o in o T ^ m n CN CM LD O LO 00 IX) CM 00 >X> ^ CN CMrHiHiHrHi-IOOOOO " ' I ' " I " ' I " ' ' " ' I " 'I " 'I " ' I " 'I ' " oor~>x)ir)'ToocMiHO CNiH
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104 Predators (Ticx)r-'X)Lo^ooc\itHo / Plant oooooooooo LOOLOOLOOLOOlT) X)LO^OOCMrHO I M 1 1 1 1 1 1| I M 1 1 1 1 n| 1 1 1 1 1 1 J 1 1| 1 1 1 1 1 1 1 1 1| I oooooooooo LOomotnoiooLO crioor^ix>LO'=rrocN>Ho iiii|iiii|iijj|iiii|iiii|iin|iiii|iiii|i CT^OOt^^OLO^mCNtHO r"||"i"'i"'i' O OO >X> CNJ CNJ rH rH

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105 ^ Predators / Plant I mini ill I I I li I I ill II I I I I I ill mill III I II I I II ! I l| I I I I I I I I I I J I I I I I I I I I I I I I I I r I I I I I I I I I I I I oooooooooo LOoinoLooiooio iHcr»oor~->x)Ln"^oocMiHo lllliiliiiiliiiiliml.ml.mlimlmil, cTioor-voiDTrocNjiHo 'I" " "I" "I " "I"" I " "I " "I " " — oooooooooo LOOLOotnoLnoLO X! C 0) (0 > u 03 I mil I I I li I III ... .1. .1 il , , , , I, , III ,, , ,1 ,, T-t o G o p ^ C Xi X) ^ XI m O »^ 4-1 S 1 0) 0) •H C

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106 Predators / Plant (NrHiHiHiHt-HOOOOO 'i""i""r"'i""l""l""l""l""l oooooooooo LOoinoLooLOOLO CNItH^rHrHiHOOOOO ' I " ' I " I " ' * ' ' ' * " ' I " ' I I " ' * M 0) a o >i a> u a> > -H 4J n) C U V ^ c m o X! 0) -H t3 u c •H 4J o ^ O CO o CO -9 n o 4-) g o 0) >1 (0 s <^ (0 CO cr^oor~v£>LO^oo
PAGE 123

107 Predators / Plant LO ID IT) ID ID in oooooooo ^rooocsicsii-HrH

PAGE 124

108 Predators / Plant (x> run CO CM ooooooooo ooooooooo

PAGE 125

109 Predators ID IT) IT) LO LD Ln^^nrO(\jcM.HtHo OOOOOOOOOOO I ill ll.l III ill ll.l. .. .1. ,1, , , , I , , , , / Plant m in in IT) IT) lO^^POnC\|CNJ>Hoor-u)in'3*ncNiHO in in in in in Ln^^oom(N(Ni.HrHo OOOOOOOOOOO M 0) >i 0) M a > H -P (0 c d i (0 a CO c c o

PAGE 126

110 IT) LO IT) ID ^ 00 OO eg CVJ IT) O Predators / Plan^ ^ IT) ^ ^ 00 00 CM CM in ID .-I o ooooooooooo lllllllllllllllllllllllllllllllllllllllllll ID lO ID ID ID'^^OOOOCMCMrH ID O OOOOOOOOOOO ooooooooooo ll|llll|IUI|llll|llll|llll|llll|IIM OCTlOOr-UJlD^OOCMr LD LD ID LD ID LO'^^OOOOCNCMi 0) M a > -H 4-> (tJ C U 0) U iH 03 T3 0) . O ^ S C a X a; (t rJQ) D. O K > c l4-( o w C C s c o 4-) c 0) a m >-i CQ j-> CO o to o p 0) >1 M c ^3 CM CM CM Q) Cn -H b4

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112 Predators / Plant 00 D "^j" CM O ' " I ' ' ' I " ' ' " ' I ' ' ' ' " I ' I ' I " I " O IT) O n CN CM T3 Q) 4-) O O u >1 0) M > -H m G . 4-) r-l •d 0) 4-1 u c (0 o c -H o M-l O 3 C c 0) CM CM 0) ^4 H C rH 0. 0) w 0) CO h:i C O 4-) C
PAGE 129

113 in Predators / Plant LT) ID 00 CN CN o O O O o o o o o CM O 00 CNJ tH I I I I I I I I I I I I I I I I I M I I I I I I I I I I I I I I I I rH1 0) a . 00 > cr^ H M 4-1 «3 tn (1) P rH m 0) M c m c (0 u 4-1 O W (U 6 c G 0) s in CN 0) M c -H CO o 0) c o 4-> c m m p g O 4J > u O X) ^ >1 c G O T! Q) P O O o

PAGE 130

114 r~ VD LO CO CM iH Predators

PAGE 131

115 Predators ^ P^ant rH rH 00 U3 ^ CM o ryn ' 1 ' -pp-i ' 1 ' -q-n rrp-rr O o O O O o O CN o 00 CM iH ^ CN O 00 I I I I i I I I J I M I I I I I I i I J I I I I I I I I I I I I _ VO'^CNItHOOVD'^OgO l|llll|llll{llll|llll|llll|llll|llll|llll|||M omoLDomoiooLoo o o o o >1 0) a > 4-) CJ^ •"^ C -H 0) CO 4-1 U ^ 0) ^ H Ci, 0) w ^ (0 c m p w
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116 IT) IT) LD Predators / Plap^t IT) 00 CN CN rH rI I I I I I I I I I I I I I I I I I i I I I I I I I I I I I j I I I I I I I I I I I I I I I I I OOOOOOOOO VO^CNOCX) 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 t-HiHiHt— I OOOO 00 CM CM H

PAGE 133

Predators / r LT) T 00 CN iH " ' I " ' I ' " I " ' I " ' I " ' I " ' I " ' ooooooooo <^ LO ^ ro CM 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 C0>>D'^CMrHCD>^^C\|O tHiHi— IrH OOOO u . 0) cr. > .H -H G 0) c •H o o c (V CM CM 0) 3 -H G <1) 0) o 0) G S ^ 0) 0) 4J (U fO nJ CO 0) o "J ^ P T) 0) O ^ O M CO 3 " C ^ o C o O u

PAGE 134

118 Fall 1991 . In the fall of 1991, a slightly bimodal response to some unknown factor (s) occurred in each prey population represented. Although the numbers of punctipes were very low, the populations also were bimodal and appeared to be related to prey dynamics (Fig. 2.13) . Q.. insidiosus and cubana populations each showed a close relationship to whitefly numbers, particularly late in the season (Fig. 2.11 and 2.12) . Spring 1992 . During the spring of 1992, it was first thought that the increase in the Q.. insidiosus population might have been in response to the large thrips immigration that occurred early in the season. The populations of the two species were found to be negatively correlated (Fig 2.30); however, the numbers of thrips were actually diminishing prior to the first appearance of the predator, which occurred at the 6th week (Fig 2.14). The thrips were essentially gone before Q.. insidiosus numbers dramatically increased, beginning in the 9th week. Perhaps this seasonal flight of thrips to tomatoes is in response to tomato pollen. Clearly thrips were not supporting the continued increase of Q.. insidiosus to the end of the season. This increase was correlated significantly with a corresponding increase in whiteflies (Fig. 2.31). An initial response of Q. cubana also may have occurred for the thrips population between weeks 4 and 5 but then later switched to aphids between weeks

PAGE 135

Fir--" 119

PAGE 136

120

PAGE 137

9 and 12, only to end with a dramatic numerical response to whiteflies and/or lepidopterans between weeks 13 and 14 (Fig. 2.15) . The practice of switching in polyphagous predators is well documented and is a very practical mechanism for survival in an environment where prey populations can rapidly fluctuate between abundance and local extinction (Murdoch 1969, Lawton et al . 1974, Bazin et al . 1974). This feeding behavior would appear to be occurring on a routine basis with many of the polyphagous predators found feeding on whiteflies in this system. Populations of punctipes made an initial response to aphids in weeks 10 and 11; however, the aphid population declined at this time and continued to remain low while Q. punctipes made a final increase which corresponded to whiteflies and/or lepidopterans (Fig 2.16). The hemerobiids clearly had a strong response to aphids which lagged one week behind the aphids on weeks 10 and 11. The last increase of this group of predators which occurred between week 13 and 14 was in response to whiteflies and/or lepidopterans (Fig. 2,17), Coccinellid were responding to aphids between week 6 and 7 and again between week 10 and 11 (Fig, 2.18). The last and largest response between week 13 and 14 might have been to whiteflies since Coccinellids are not generally known to develop on Lepidoptera or thrips. Fall 199?. In the fall of 1992, predator population fluctuations were more difficult to interpret. Q. insidiosns

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122 populations followed the classic predator prey counter oscillations for the changes in thrips populations; however, it could have just as easily preyed on whiteflies, lepidopterans and aphids during this time (Fig. 2.19). C cubana was apparently responding to aphids primarily weeks 5 through 12, but, could also have been responding to whiteflies, lepidopterans and thrips as well (Fig. 2.20). An erratic predator prey response was seen in £. assimiliS f the only season that it was abundant (Fig. 2.21). The first peak in population could have been in response to Lepidoptera in weeks 4 to 5; although, later prey could have been any of the alternatives that are presented. Another anthocorid which was abundant this season was Q.. externa (Fig. 2.22) . It was responding to an increase in whiteflies early in the season, weeks 2 and 3, well before the aphids and other prey were present in any number. Although it is not clear which prey dominated the diet later in the season, this early response might prove to be a desirable trait for early release survival of this predator against whiteflies. Coccinellid larvae clearly were responding aphid populations (Fig. 2.23). Whitefly immatures were present in low numbers early in the season; yet, the coccinellid' s first apperance followed the classic delayed response of a predator to aphids beginning in week 8. Though lady beetles can survive on alternative prey, the species encountered in this survey are recognized as aphid predators. Therefore, only

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123 whiteflies and aphids were compared in the graphical representations of populations. Spring 1993. In the spring of 1993, Q.. insidiOSUS populations started responding to thrips and/or aphids in the 5th week and switched to whiteflies in the 10th week (Fig. 2.24) . There was no relationship seen between Cuban a and any prey except whitefly nymphs (Fig. 2.25). punctipes numbers were low during this season. The last and greatest response seen in this species for the season, weeks 10 and 11, could have only been with whiteflies or Lepodoptera (Fig. 2.26). The aphids and thrips were not present to evoke a response in £. punctipes at the time. The anthocorid, £. assimiliSf also showed a similar response pattern week 8 through 12 (Fig. 2.27). Its presence could only have been to whiteflies or Lepidoptera. The two Micromus species of hemerobiid larvae indicated the greatest response to aphids at week 6 and 7 (Fig 2.28). Various coccinellid larvae encounterd during this season were present prior to an aphid build up (week 6) and the population oscillations do not correspond well with aphids (Fig. 2.29). However, the numbers were low and the coccinellids were not observed feeding on whiteflies in the field. Predator-prey correlatinn. Some of the most abundant alternative prey that were found on tomatoes each season are aphids, thrips, Lepidoptera eggs and larvae, and psocoptera. The few statistically valid linear correlations that could be made after transforming the data for whitefly predators and

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124 alternative prey groups for each season of the survey are shown in Table 2.4. During both spring crops the correlation of Q. insidiosus with the numbers of Lepidoptera larvae and whitefly adults present were significant (F < 0.05). In the spring of 1993, the Lepidoptera were almost totally southern army worms and to some extent tomato pinworm larvae. This predator also was positively correlated (P < 0.05) with whitefly immatures in the fall of 1992 and spring of 1993 and negatively correlated (P < 0.001) with thrips. The second anthocorid in sufficient numbers to make any correlation was £. assimilis ; however, this species occurred in sufficient numbers to analyze only during the fall of 1992. The strongest correlation found was with Thysanoptera; however, it was not found to be significant at P < 0.05. Among the neuropterans, the only member encountered in sufficient numbers on which to perform correlation analyses was £. cubana . Although no significant correlation was seen for the fall 1992, significant correlation (P < 0.05) was seen with whitefly adults and immatures during the spring of 1993. The number of each species of anthocorids, chrysopids, hemerobiids, coccinellids, nabids and Geocoris sp., which are known predators of whiteflies, were totaled each week and the numbers correlated with the various categories of prey which were present during each season. The total number of

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125 Table 2.4. Correlation coeffecients (r^) for combinations of prevalent whitefly (WF) predators and the whitefly pedator complex with alternative prey present on insecticide free tomatoes at Bradenton, FL. (J. insiQc assim o. cuoana iosus ills c rccj. . complex Fall 1991 WF adult WF immature Aphididae Thysanoptera ijcpj-UUpL.tr I. d Psocoptera 0.799* 0.682* 0.617* 0.441 n (^9 u . 0.321 WF adult WF immature Aphididae Thysanoptera Spring 1992 0.899** 0.541* -0.939** u . o o ^ 0.906** 0.816** -0.616* U . D / 1 Fall 1992 WF adult WF immature Aphididae Thysanoptera LeoidoDtera Psocoptera -0.408* 0.268 0.057 0.504* 0.127 0.089 -0.425 0.01 0.365 -0.1366 0.465 0.139 -0.185 -0.231 0.019 0.736* 0.326 0.673* 0.842** U . O 0 0.187 WF adult WF immature Aphididae Thysanoptera Lepidoptera Spring 1993 0.839* 0.812* 0.703* 0.718* 0.263 -0.075 0.238 -0.296 0.881** -0.602 0.616* 0.589* 0.824** 0.619* 0.49 *Values significant at the P < 0.05 **Values significant at P < 0.001

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predators was significantly correlated with whitefly adult and aphids for every season. Predator numbers were negatively correlated with the number of thrips in the spring of 1992 and positively correlated in the fall of 1992 and spring of 1992. Positive correlations were obtained with the numbers of whitefly immatures in the fall of 1991 and spring of 1993. Psocoptera, although at times present in large numbers, were not correlated with the above group of predators . Association coefficients . The results of the association coefficients can be seen in Table 2.5. These figures must be interpreted as the association between species throughout the entire season. Thus, while some species might have shown a brief but strong numerical response to increases in the pest population, because they were not present with the pest throughout the season, they have a low association coefficient. Those predaceous species which are present with the pest very early in the season and remain throughout the season will have a high coefficient, although they may have not been able to keep up with the growth of the pest population numerically. This coefficient might be helpful to identify those species which may respond earliest to low prey densities and which persist throughout the season rather than those species which respond only to pest populations after they have increased to potentially damaging levels. These coefficients indicate that Q. insldiosus was present

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o o d c m CO u o Q) M Cl, WF) ' >1 .H 4-4 H M O CO a) o w 4-) -p 03 c 0) o -H p u -H •d m 0) M-l >i 0) m o o &. CO c C o •H p o -H u T3 o G CO CO o < 4-1 CO M O 4J d 0) u 4-1 0) +J -rH 0) c (CJ •H (0 > 0) c •H u o u X) -H o > 0) (13 e -^ i O (C3 o ^ m o u i u CO G 0) O rH CO H iH H O O I I I I •«3< VD O CN C\J O O rH O O I I I I 00 00 VD o o o o o I I I I I oo ro 00 00 VD o o o o o I I 00 o iH cr> rO tH o o o -p cu p (CS J-) a g CO CO o e n a, o n -H -H -H O -H 4d n o a Cu a 41! CO 0) S <; Eh Oi CM »H II CO 2 O O O O CTl O rH rH rH O I I I I I CM OO 00 CM o o o o o I I I CO Q) M 3 -p (C3 CO -H -rH -H fr. ax: !S !< Eh CM cr> 00 (0 (0 0) H-> o -H cx 0)

PAGE 144

CJD O (Ti O CTi O • • • • O O rH O I 1^ O O O O
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129 along with whiteflies, aphids, psocids, and Lepidoptera during both spring seasons. The highest association was with aphids, although in the spring of 1993, there were high associations with Thysanoptera, Psocoptera and Lepidoptera larvae . Q. punctipes indicated a high association with whiteflies and Lepidoptera larvae only in the spring of 1992. £. cubana , hemerobiids and coccinellids did not indicate any high associations, with any prey over the entire survey. The Araneae, on the other hand, because they were present from the earliest days each season generally showed strong association with all groups of prey throughout the survey. Conclusions A large complex of predaceous fauna was found to attack whiteflies on tomatoes in West-Central Florida. This fauna will most likely be expanded with time to include additional species, some of which are awaiting authoritative identification. At certain times, some predator species may be responding numerically to whitefly populations; however, these responses are not soon enough or great enough to reduce whitefly populations. There were specific instances during this survey, when £. punctipes, £. asslmllis , and externa responded to whitefly populations. However, of the predators discovered in this survey, Q. insidiosu.q and £. ^miiana appear to be the most numerically responsive to whitefly populations. They also display an association with

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130 whiteflies which begins with low density populations early in the seasonal colonization of the tomato fields and continues throughout the remainder of the season. Although the other predators mentioned may have potential as natural enemies of whiteflies, both of these species should be studied further for their impact on whitefly populations and as potential biological control agents. Spring and fall crops are markedly different in both the numbers of whiteflies present and in the predator species present. The lower numbers of whiteflies that occur in the fall cropping seasons could possibly lead to some degree of population regulation, if predator numbers could be manipulated and maintained in the system before whitefly colonization. Conservation of predators by sequential planting, however, is not feasible, since the avoidance of viruliferous whiteflies is vital to the prevention of the diseases vectored by the whitefly. The Araneae as a group of predators deserve special attention. Only recently has the role of these predators in temporary agroecosystems begun to be studied and understood in part. As a complex, they undoubtedly make some contribution to the final equation by virtue of the fact that they are ubiquitous predators which are the first to colonize tomato fields each season. Spiders by their very nature require supporting structures for web construction. And if they are not the "sit and wait" strategists, then prey capture techniques of active hunters require vegetation for

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131 insects in which to stalk prey. As the crop enters its vegetative growth phase the spider numbers have been shown to increase exponentially. However, the exact role that these predaceous arthropods have in a given agroecosystem remains to be defined. A reliable, gut content assay would aid greatly both to determine qualitatively and quantitatively what specific predaceous arthropods are present and to monitor their feeding behavior over the season. To date, there is not an effective method known for quantitatively measuring the amount of prey taken by a predator in the field. Using predation estimates for predators confined on prey in laboratory feeding trials to extrapolate field consumption rates is at best dubious. Given the complexities of the searching environment and multitrophic interactions presented to a predator in the field, better methods of determining predator feeding rates and behavior in the field are needed.

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CHAPTER III PREY PREFERENCE AND SUITABILITY OF PREY FOR GREEN LACEWINGS Introduction ' , \ The whitefly, Bemisia t abaci (Gennadius) , recently proposed as a new species, £. argentlf olll (Bellows and Perrlng) , by Bellows et al . (1994), has plagued horticultural and field crops in the southern United States in recent years. Costs to the agricultural industry in control measures and crop losses are estimated to be in the millions of dollars (Perring et al . 1993b). Damage can include, direct yield losses and reduced fruit quality. Much damage is the result of honeydew and the sooty mold, plant disorders (Hoelmer et al. 1990, Schuster et al. 1990, Schuster et al. 1991, Costa et al. 1993), and virus transmission (Costa 1976, Duffus et al 1986, Kring et al . 1991). Biological control programs for different whitefly species have met success in the past (Dowell et al 1979, Bellows et al. 1992). Given the record of this species for the development of resistance to pesticides (Eveleens 1983, Prabhaker et al . 1985, Abdeldaffie et al . 1987), biological control must be an important component of future control programs . 132

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133 Two species of lacewings, Chrysoperla ruf ilabris Burmeister and Ceraeochrysa cubana (Hagen) , were among the chrysopids associated with whiteflies and aphids in a survey of predators on tomatoes in Florida, (see Chapter 2) . Breene et al. (1992) found that larvae of £. ruf ilabris were able to control B.t abaci when caged on infested hibiscus plants in a greenhouse. A generalist predator in the field is often presented with numerous alternative prey options. Information is needed on the preference and suitability of prey which are commonly available in the field. Nordlund and Morrison (1990) in a study on cotton, found that the larvae of ruf ilabris feed on greater numbers of the larvae of Heliothis virescens (F.) than on E. virescens eggs or the cotton aphid. Aphis gossypii (F.) . Numerous species of prey were evaluated for their effects on the development and fecundity of rufilabris by Hydorn (1971) . Mortality was found to be the lowest on Dialurodes citri (Ashmend) ; however, development time was one of the longest of the prey tested. Differences were found in the development of C cubana on various prey associated with citrus, scales, mites, and whitefly (Muma 1957) . Here again, development time was longest on the cloudywinged whitefly ( Dialeurodes citrifolii (Morgan) . The objective of this study was to determine if £. rufilabris and £. cubana exhibited preference for prey which are commonly associated with tomatoes, fi. t abaci and

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134 Macroslphum euphorblae (Thomas) , and if each prey was suitable for normal predator development and fecundity. Materials and Methods Preference ruf ilabris was obtained from a commercial insectary (Biofac, Mathis, TX) and adults and eggs of cubana were collected at GCREC Bradenton, FL and maintained in a temperature controlled room. The larvae of both species for all tests were reared singly in disposable petri dishes on a diet of velvetbean caterpillar larvae and eggs, Anticarsia aemmatalis (Hubner) , as well as nymphs and adults of the potato aphid and nymphs of £. t abaci . The lacewings were reared and maintained at 23° to 2 9°C and a 14L:10D photoperiod. Adult lacewings were given water and a 1:1:1 ratio of yeast ( Saccharomyces cerevisiae (Delecta Yeast Flakes, Schiff Bio-Food Products, Moonachie, NJ) ) , sugar, and water. A 10 cm diameter disposable plastic petri dish was use as a search arena for each timed feeding preference observation. The inside of the lip of the petri dishes were coated with Fluon to prevent escape of the larvae during observation. Predation was evaluated for each prey separately and for the two prey species mixed. For the whitefly tests, a 20 mm diameter leaf disk was cut from an infested hibiscus plant and placed in the center of the

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135 arena. The number of third and fourth instar nymphs of E. tabacl on each leaf disk was adjusted to 30 by removing excess scales with a probe. For the aphid tests, U. euphorbiae of mixed sizes were transferred with a camel hair brush into a paper can and 30 were placed in the arena just prior to each observation. The same procedure was used to combine the two prey for the mixed prey tests using a density of 30 prey for each species. Food was denied lacewing larvae approximately 12 to 20 hours prior to each observation. A lacewing larva was placed in the center of the petri dish, and the number of seconds were recorded for each of the following modes of behavior: searching, feeding, and resting. In the case of mixed prey, the prey type attacked was noted as well. A minimum of 16 replications were conducted for each instar of both species of lacewings using a single larva for each observation. Each larva was tested only once during a given instar and each was observed for 30 minutes using a dissecting microscope with low intensity light. Prefere nce models Rapport 's model . Rapport and Turner's (1970) preference model was used to calculate a preference coefficient (p i and P2) for each lacewing larva for each prey being tested. This was accomplished by first estimating the mean number of each prey species, }ii and ^2, which is consumed during a specified time period at a standard density. In the case where no preference is exercised between two species in mixed culture, the number of prey consumed would be half that consumed of

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136 each prey in the single prey environment. The preference coefficients are calculated in the following manner: 2^1* 2^l2* where represents the mean number of prey type 1 consumed in the mixed prey culture and Ha* the mean of mixed prey type 2. = the mean number of prey type 1 consumed in a single prey environment; ^2 = the mean number of prey type 2 consumed in a single prey environment. Manly 's model . A model, originally developed by Manly et al. (1972) and further developed by Manly (1974), Chesson (1978), and Manly (1980), also was used to estimate preference in this study. A probabilistic model, it estimates the proportion of each class of prey in the diet of a predator if all kinds of prey are available at the same density. It also allows for the depletion of prey during the time that the observations are being made using an approximate moment estimator ^i, which is given by: ln( (n_^ r_^) /n^) Jii = ~i / j = l,...,k X In ( (n • -r.) /n.) j -1 where and are the number of individuals of prey i and j present in the environment at the start of the experiment; and rj are the number of prey i and j remaining at the end of the experiment and k is the number of species present.

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137 Prey Suitability In each of the following experiments, investigations of the suitability of B. t abaci and euphorbiae as prey for the lacewings C. cubana and £. ruf ilabris were carried out under the same temperature and lighting conditions described in the prey preference tests. Methods of rearing the lacewings in each test were the same except where noted. Development and Mortality Lacewings were reared on single diets of £. tabaci and M. euphorbiae , and on these two prey mixed. Lacewing eggs were placed in 10 cm petri dishes with Fluon coated sides. Every 24 hours, each lacewing was observed for mortality and ecdysis and prey density was adjusted to 30. To prevent the possibility of inducing mortality by removing pupae for weighing, pupal weights were obtained by obtaining the difference of the weight of the petri dish containing the pupa within one day of pupation and the weight after eclosion of the adult. Fecundity The gender of adult reared on each diet regimen was determined upon eclosion. Females were paired with males from the colony and pairs were placed in individual pint paper cans (Neptune Paper Prod., NJ) with oviposition liners made of construction paper and provided the same food as the colony. The liners were changed and the lacewings received

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fresh diet on alternate days. The number of eggs were recorded and totaled for the first 20 days of oviposit ion. Maximum consumption Consumption of either the two prey species, B. tabaci and M. euphorbiae f was recorded for the third instar of each of the lacewing species . Individual larvae were given excess prey on a daily basis beginning at the second molt. The number of uneaten prey were counted each day and suffecient fresh prey were added to maintain an excess. The prey consumption for each larva was summed for the period of time between ecdysis and pupation. Statistical analysis Preference A two tailed sign test (Conover 1981) was used to test for preference among the lacewing instars. The relative preferences calculated for each observation (Rapport and Turner, 1970) were classified as a positive (+) , a negative (-) , or a tie (0). The null hypothesis for a two tailed test would be: Hq: P(Xj < Y_i ) = P(Xi > ) Ha: Either P{X^ < ) < P (X^ > ) or P(X^ < Y_i ) > P{X^ > Y^ ) For the preference test of Manly et al. (1972), the total iS values for the individual predators observed can be regarded as a sample from a normal distribution (Chesson, 1983) . Therefore, a standard t test was used to test the

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139 null hypothesis that no preference was observed between the lacewing instars for the two types of prey Hq: = ^2 ^ ^-^ and Ej^: ^ ^2Prey suitability Development and fecundity . An ANOVA was used to test if the means were equal. Bartlett's test was used to check if the variances were equal across all levels. If this test indicated the variance was not homogeneous, then the Welch Anova, was used to test the equality of means. Where the ANOVA indicated that the means were not equal, the means were separated using the Tukey-Kramer HSD multiple comparison test. All statistical tests were done with a statistical computer package (SAS Institute 198 9) . The level of significance used throughout was P = 0.05. Mortality . The variables for this factor were treated as nominal values. A bivariate response was used with one of two values assigned to each observation. A nominal value of j (1) was used for death and a value of (0) was assigned for survival of the predator on each diet. The Pearson and the Likelihood Ratio chi-square tests were used to test the hypothesis that the mortality response was the same for each of the lacewing 's diets (SAS Institute 1989) . Maximum predation . A t test was used to test the hypothesis that the means of whitefly and aphid consumption for each species of lacewing were equal at P = 0.05. Prior to the analysis, distributions were tested for normality and

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140 the variances were tested for equality with Bartlett's test (SAS Institute 1989) . Results Preference The mean number of prey consumed by each predator for each prey species in both the single and the mixed prey environment are given in Table 3.1. Comparisons between the two species in the mixed prey environment seem to indicate that the species are not similar in their feeding behavior, with each instar of £. cubana consuming more whiteflies than £. ruf ilabris and £. ruf llabris consuming more aphids than £. cubana . As would be expected, both species exhibited the greatest potential for prey consumption in the third instar. If no preference is exhibited, the expected number of prey consumed in the mixed prey environment would be half the number of each prey consumed in the single prey environment. A comparison can be made in Fig. 3.1, where the number of prey consumed in the mixed prey tests are compared to half the number of prey consumed in the single prey tests. These comparisons suggest that £. cubana demonstrates a preference for whiteflies in the first instar and £. rufilabris a preference for aphids in the third instar. Rapport and Turner's model . The individual preference for each observation is shown as the individual relative preference in Table 3.2. The relative preference is taken as

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141 u c (0 p m m a> -H o I m 0< c -H IS 0) • o w (tJ 4-1 O O ^ (0 O 0) e -H 4-) H ° ^ Oh & W CO "5 " S 0) >i M ?> a o c CO CO o p CO -H a CO (cj a CM CM CN o o o o o o -H -H -H -H -H -H VO CM ^ CTi CM ^ O CO O CN in CO 00 cTi in o o O O 1 O T3 (U i 0) -H rH E -P 0) >i -M C 1— 1 -iH O 4-1 Q) en -H Ti c -H -H X! 0) 3 CO CO JQ G O O O 4-1 O C O U CO 0) -H CO 4-1 M -H 4-) 0) x: -H g (0 s C 4-1 4-1 O O XI H H 4J (U
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142 00 o u O U i Mi m U 4-t CO c w H o ex o O U 1 o 00 o o ' ' I ' o o o o I ' ' I I o o ^ CM O oo <-! >H rH (as+) pauinsuoo AajcJ ueaw T" o CM o u o o 0) X! 4J •4-1 O 73 c o (0 G (0 P o w C/3 -H p -H o u (0 p CO <0 > (0 O >1 X) n e CO c o o 9. M p c 0) g a o -H > c cu >1 cu M a cu (T3 o o o ip rH >1 • Cu o w 00 CO -H 4-1 O P >i o 4J Xi -H 4J CO •H C ^ 0) T) CO -d 4-) CO 0) t3 4-) c (d >i jj CO a 0) i -H 0) P ^ (0 CO (1) -3 oo a > c
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143 V. \X r•rG Id o <1 •. c -H r (13 ^ -2 u nil o M-l O to w 4-1 CO C e -H >i > c M (0 rH 0) (0 •H O 0) o 0 o p 0) 0) o 0) M 0) O m •4-1 0) 0) > 0) > m -H rH 0) u OS 0) XI m (D O C 0) -H P (0 rH 0) T3 -H > -H G (0 4-) o -p W3 IT) 00 CM CTi IT) CO CN V£> CO O 00 IT) VO ^ lo 00 o o r•=r I .H oj CN ro CN 00 ^ CN CN o ro o ,H I I I I I CN 00 O ^ iH 00 CN iH O X> ^ 1^ 00 CN I I O 00 o rH I I r~ ".D 00 00 00 CN H C O -H Xi D O ^1 0) N SI Mh O u o to MH Q) Q) U O • to > -H -p > to -H rH J-) 1 X! rH -H u rO M tU to C -P U • H mi c c to to 4J CO O 3 a, rH a. (0 to > DS i > Xi -H -P rH -H 0) CO T3 O o a s >1 (U X! • 41! d) -P -O O Q) C Cn 4-) 0) C to M -H U OJ CO -H 4-1 D X) CU C M * -H a<

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144 the difference of p i and P2 • When px = P2 = lno preference is indicated. Thus, the table represents an index of preference, with the values closest to zero showing the least preference. Since the aphid M. euphorbiae was designated as prey 1 and t abaci was designated as prey 2, the positive preference coefficients indicate a higher preference for aphids and negative values indicate preference for whiteflies. An assessment of preference can be seen by summing the relative preference values observed for the individual observations in each instar of each lacewing species (Table 3.2). The value of -44.6 for first instar £. cubana indicates a strong preference for the whitefly, whereas, the value of 27.8 for the third instar of ([;. rufilabris indicates a strong preference for the aphid. The sums of relative preferences for the individual observations of second and third instars of £. cubana and the first instar of £ rufilabris are near 0 and therefore little or no preference is indicated. The sign test which was applied to the number of positive (+) and negative (-) responses of relative preference for each observation indicates which overall responses of each instar of each species were different from 0 at the P = 0.05 level of significance. The null hypothesis, Hq: P (X^ < ) = P (X^ > ) , was rejected for the first instar of £. cubana and for the second and third instar of £. rufil
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145 Manly 's model . ^ values (Manly et al . , 1972) were found for the 16 replications of each lacewing instar on each prey species (Fig. 3.2) . The mean IS values for each of the three instars of Q.. cubana on £. t abaci (0.91, 0.82, and 0.82 respectively) and for £. rufilabris (0.59, 0.56, and 0.49 respectively) indicate a strong preference for t abaci , by each instar of the lacewing £. cubana and no preference between the whitefly and aphid prey by £. rufilabris . A student ' s t test was used to compare the mean B values for each species. The results were highly significant for Q, cubana (t = 16.6, df = 32, P <0.001; t = 10.5, df = 30, P <0.001; t = 10.7, df = 32, P <0.001 for instars 1, 2, and 3 respectively) , confirming that all instars prefer the whitefly and that £. rufilabris indicates no preference in any instar (t = 1.2, df = 30, P >0.05; t = 0.9, df = 30, P >0.05; t = 0.2, df = 32, P >0.05 for instars 1, 2, and 3 respectively) . Prey Handling The percentage of time spent searching, feeding, and resting during the mixed prey preference tests is shown in Fig. 3.3. Although little difference is seen between the first instar of each species of lacewing, more time was spent searching and less time feeding in each instar of Q, cubana . In the last two instars, £ cubana spent approximately twice as much time searching as did rufilabris . The most obvious reason for this behavior is that £ cubana consumed approximately twice the number of whiteflies than £.

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146 >1 rH <4-l 0) p -H -H «----?Sv-^ 1 iiliiiii^ 00 O o M -P w c CO I I I I I I I I I I I I I I I I I I J I I I I I I I I I I lcri (0 -H ^ CM o si O Q 0) 21 m o c o -H p u 1 4-1 -H -iH to ^ o a (U x: -p O (0 3 T3 M CO M CO -H CN to (U u en -H CM O >i 0) c 03 >i S X! CO — ~ e II

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147 c -H 4-) V) 0) G -H 0) c -H O U (T5 i (1) G G 4-) G 0) w (1) e H J-1 o a) (0 4J G (U o 0) 00 CO 0) M Cn -H G m • i o 0) U •H a > G o 0} CO >i 4-1 (1) o a >i -p n -H CO ><; G 0) e T3 m T3 M G H T3 G OJ P o CO (0 P i >^ G H CJ (0 o ^ G «3 p

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148 ruf ilabrls did in the mixed prey test and approximately half the number of aphids (Fig. 3.1). euphorbiae has a large body size in relation to a single whitefly nymph; therefore, it requires a longer time to completely ingest than a whitefly nymph. £. ruf ilabris spent more time feeding on aphids and less time searching for whiteflies than Q cubana . Although the 2nd and 3rd instar larvae of each species can consume a single whitefly nymph in a short time, more prey encounters entail greater time spent locating prey, cleaning mandibles between encounters, and returning to already consumed prey than the equivalent time spent feeding on a single aphid. Prey Suitability Development The development times on the three different prey regimes are summarized in Table 3.3. Generally, both species of lacewings appear to develop at a slower rate on an all aphid diet and fastest on a mixed diet. This suggests that together the two prey supplied greater nutrition than either species alone; however, as was seen in the preference tests, each species consumed a greater amount of both prey in the mixed prey situation (Fig, 3.1). The increased consumption may contribute to a shorter development time on the mixed prey diet. Although the same facilities and procedures were used for each species of lacewing, the observations on the two

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149 m +J 0) •H •o >i • -P ^ 0) X) u 4-1 m -H (1) T3 C o (1) c o V 03 a • Wi -a T3 G (d C -1 S (1) o Q O CO (0 E-" (0 0) en nJ -P w u m 0) a -H W >i CO T) M-l O W C/3 +1 c 0) -P •H .H # (0 4-) M O E 4-> c o -H w o o w 0) (0 m 4-1 -H •H >i 0) X) O O r~ O IT) o O O +1 -H +1 +1 <^ CM CM HH K * tc K •K 03 03 03 03 03 OS o ^ o ^ o +1 -H +1 -H x: 4-1 p -H & OS X! u 4J G i X! x: -c M O 4-> O rH CO 4-1 <1) O -P 4J 4-1 I C -U (D C M e V (U 3 in 4-1 iH O 4-1 O • -rH O O d 0! V >1 +J -H — G 03 CO CO U G Cn -H 03 G 4-1 (U -H -H S > G H 0) 1 CO P >i 4J (U G o CU a; 0) u 3 CU 4h Eh 0) 4-> d e V 0) CU OS lO X) cn CO o G p 03 0) o G x: CU -p A P CU G >i 4h (U XI 4-1 e -H •d -d o 0) G iH •H >i CU o IS .H > fH 0) P rH u G •d O 03 03 4-1 •-\ O 4h -H O 4h 4h O H rH G CU .H CO Cn > O 0) -H CU O -h CO o OS CU CU u o G CO m m -H (U 03 >i CO G 03 CO C -H CU CU S p -P -H OS & ^H O 4h CO OS X)

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150 species were conducted almost a year apart. Therefore, it may not be valid to compare the two data sets. However, it can be observed from differences in the data that the two lacewing species responded differently. The mean total days of development were found to be different on all diets (F = 272.1, df = 19, P <0.001;.F = 434.9, df = 19, P <0.001; F = 412, df = 20, P <0.001; on aphid only, whitefly only and mixed diets respectively (Welch's ANOVA, SAS Institute 1989, pp 288) . The mean time of pupal development was not different for the diets within a species of lacewing (P >0.05), but was very different between the species, being 9.2 days for £. ruf ilabrls ^ and 13.8 days for C. cubana (F = 167, df = 51, P <0.001 (Welch's ANOVA, SAS Institute 1989, pp 288) . The mean pupal weights for £. cubana were not different on each diet, but for Q,. ruf ilabris were higher on the whitefly only diet than on either the aphid or the mixed diet (Table 3.3) . Pupal weights of the two species on the whitefly only diet were significantly different (Z = -4.3, P <0.001) (Wilcoxon rank sums, SAS Institute 1989, 282-284) . Mortality No difference was found in the mortality for £. ruf ilabris on any of the three diets (Pearson chi-square = 0.025, P >0.05) (Table 3.3). However, for £. i^liiiana, 21.7% mortality on the aphid diet and 0% on whiteflies supports the conclusion that the whiteflies sre a more suitable prey for this lacewing.

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151 Fecundity The fecundity for £. cubana on the three different diets was not found different at the P = 0.05 level of significance (F = 0.486, df = 2, P = 0.622) (ANOVA, SAS Institute 1989). The mean number of eggs (± SE) deposited over the 20 day post eclosion and breeding period was 204 ± 38 for the mixed diet (N = 10), 166 ± 32 for the whitefly diet (N = 7), and 161 ± 38 for the aphid diet (N = 7) . The fecundity for £. ruf ilabrls is not reported. Maximum consumption Maximum consumption of prey for the third instar of each lacewing species was found to be different for both prey types (whitefly diet T = 5 . 95, df = 14, F <0.001; aphid T = 4.32, df = 10, F <0.05) (Fig. 3.4). C. rufilabrls consumed twice the number of whiteflies and a third more aphids than £. cubana . Conclusion and Discussion Some fundamental difference and similarities were observed in the feeding habits of the two lacewing species used in these experiments. £. ruf ilabris is a larger lacewing with a shorter average development time and a larger consumption capacity than Q. cubana . Both lacewings generally appear to develop more rapidly on a mixed diet than on a single diet; however, both species can develop adequately on whiteflies alone. Both species consume many

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152 2500 2000G o •H +J §^1500 d CO G o o >1 G 1000I I Whiteflies Aphids 500 C. rufilabris C. cubana Lacewing species Figure 3.4. Mean (±SE) maximum prey consumed by third instar larvae of Q,. rufilabris and Q.. cubana of M. euphorbi and nymphs of the whitefly, B. t abaci (N = 8) .

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153 more whiteflies than aphids, yet both do not exhibit equal preference for whiteflies. The results of these experiments demonstrate the differences in approach to the question of preference. Rapport and Turner's (1970) model seems to follow an intuitive approach for testing and establishing food preference. The model of Manly et al. (1972) relies on the ratio of prey in the environment and the prey consumed for an indication of preference, which is expressed as a probability estimate of what the next prey choice will be. Though both models show similar trends in preference, the results are markedly different. Rapport's method indicates strong preference for whiteflies in the first instar of £. cubana and preference for aphids by the second and third instars of £. ruf ilabris . In contrast. Manly ' s method indicates strong preference for whiteflies by Q. cubana and no preference between the prey by £. ruf ilabris . However, both tests indicate a significant degree of preference on the part of £. cubana for fi. t abaci and no preference for this whitefly on the part of £ ruf ilabris . In the mixed prey situation, £ cubana fed on more whiteflies than Q. ruf ilabris and spent approximately twice as much time searching as did Q. ruf Ilabris . £. rufilabris spent less time searching for whiteflies and more time feeding on aphids. This may be related to prey quality as a factor in prey preference as noted by Crawley, "The reason that a predator might turn down a prey species is that by

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154 feeding on an inferior prey it would lose the opportunity to find and feed from a superior prey" (Crawley 1992b, p. 45). This would intuitively lead one to conclude that £. cubana preferred the whitefly and £. ruf ilabris the aphid. Therefore, based on the indications of preference found to be in agreement between the two preference models and on searching behavior, it is concluded that cubana prefers R. t abaci over M. euphorbiae and that C rufilabris does not exhibit a strong preference for either prey. Crawley (1992a) is correct in his estimation of the difficulties associated with an unbiased determination of preference. Perhaps polyphagy needs to be redefined to include levels of specialization or degrees of polyphagy. Certainly, varying degrees of preference can be seen in polyphagous or general feeders. Apparently, some generalist feeders can survive on a wide range of prey, yet, search non randomly for a preferred prey. There may also be evidence for genetic differences in preference and foraging habits within populations of a species. Tauber and Tauber (1987), in their study on feeding preference of Chrysopa quadripunctata Burmeister and C slossonae Banks, concluded that prey specificity may be a derived trait in Chrysopidae. Rapport and Turners model, indicated that £. cubana and £. rufilabri.S can display preference differences among instars. The same or smaller body size is known to be an important factor in the foraging behavior of many predators (Sabelis 1992) . Therefore, it is apparent that in early

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155 instars, a predator may not be able to attack larger prey successfully. First instar larvae of lacewings are very small and fragile, however, a well fed third instar is larger and more robust and is capable of attacking adult aphids and larger prey with success. Predators theoretically will maximize efficiency of prey intake while minimizing the effort required to attack it successfully (Crawley & Krebs 1992) . The question becomes, can the predator distinguish size or strength of a particular prey? If so, it is reasonable to conclude that the early instars of lacewings would be optimizing food consumption by the reward of success in attacking the sessile whitefly nymphs more frequently than occasionally loosing the larger mobile aphids. As the larvae increase in size, the number of whitefly nymphs required to sustain them results in less efficient predation than the larger aphid meal. An observation, which Rapport and Turner (1970) also observed in their empirical data, was that, in the mixed prey environment, predators consumed more prey than in the single prey situation. The most obvious explanation for this behavior would be the higher density of prey which is doubled in the mixed prey arena (30 pi and 30 P2) . Also, many predators, in an excess of prey, have been observed to demonstrate a feeding frenzy resulting in an increased attack rate often coupled with incomplete consumption of prey. This may help to explain the functional response of predators to an increase in prey density which allows them to become more

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156 efficient predators up to some point of satiation or prey depletion or local extinction. Dukas and Ellner (1993) presented a model to examine the way predators should divide attention among different prey types. This model assumes the optimal foraging theory that predators will tend to maximize their rate of energy intake. They predict that when encountering conspicuous prey, the predators will divide their attacks among the different prey. Learning to recognize and handle prey is said to be a function of density. At the higher density of prey found in the mixed lacewing test, as opposed to the single prey tests, the probability of successful prey capture must have increased noticeably, resulting in greater prey consumption in the mixed prey environment. In the field, there are normally multiple alternative prey available at a given time. At times, there may be an abundance of different prey from which the predator can select an optimal diet for proper development. This, again, assumes that it can detect and distinguish between these desired qualities of prey. In conclusion, there is a degree of preference that is being demonstrated on the part of these lacewing species. From the results of these tests and the rather high incidence of £. cubana in sweetpotato whitefly infested tomatoes (see Chap. 2), it appears that this species may be selective in its' attack of whiteflies. More work is needed to establish actual feeding behavior in the complex field environment and possible kairomone attraction for prey location. Useful

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157 information on the biology and rearing methods of this species has been gained during this study. £. ruf ilabris has potential as a biological control agent since it can feed on large numbers of the sweetpotato whitefly and since it will develop and reproduce normally on this prey.

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CHAPTER IV ATTRACTION AND ARRESTMENT OF ADULT LACEWINGS Introduction Predator-prey population cycles, which are coupled in a density-dependent fashion, oscillate out of phase with one another, such that the numerical response of the predator often lags behind increases in the prey population (Horn 1988) . Such delays in the ephemeral agroecosystem can prevent predators from having an impact on pest numbers before crop losses occur. Murdock (1985) , suggests that a build up of a general predator prior to pest increases might be the "best" predator (Murdock 1973) . The establishment of predators can be accomplished more effectively when importation is done in conjunction with an attractant (Greany and Hagen 1981) . An effective attractant could be useful in the enhancement or manipulation of predators by aggregating endemic natural enemies to a desired location or by limiting the dispersal of predators released for the purpose of augmentation (Gross 1981) . Different lacewing species were found to be associated with the sweetpotato whitefly, Bemisia t abaci Gennadius, in insecticide free tomato plots in Florida (see Chap. 2) . Two species, Chrvsoperla rufilabris Burmeister and Ceraeochrysa 158

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159 I cubana Say, were observed to feed on eggs and nymphs of E. t abaci in the field and in the laboratory (see Chap 3) . £. cubana f preferred Et abaci over the potato aphid, Macrosiphum euphorbiae (Thomas) , in laboratory feeding trials. In the field, lacewing and other general predator populations did not increase in numbers until R. t abaci numbers had increased to high levels (see Chap. 2) . Methods that allow for the manipulation of lacewings and other predators, such that they are present prior to pest migration into annual crops, may hold promise for enhancing biological control of the sweetpotato whitefly. The adults of some species of Chrysopidae are known to feed on pollen, nectar, and honeydew, while the larval stages alone are predaceous (Hagen 1950, Sundby 1967, Canard et al . 1984) . Chemoreception of volatile breakdown products of tryptophan in aphid honeydew has been found to attract the adult of the lacewing Chrysoperla carnea Stephens to the aphid infested plant (Hagen et al. 1976). The topic is reviewed by Hagen (1986) . Kairomones, in the form of "artificial honeydew" made by mixing yeast products and sugar, have been used to attract the lacewing carnea | \ (Hagen et al. 1970, 1971). However, different attempts to i i show attraction with the yeast protein hydrolysates have been ; inconsistent (Dean and Satasook 1983, Wellik and Slosser 1983, Liber and Niccoli 1988, Ben Saad and Bishop 1976) The yeasts Saccharomyces cerevlsiae . ^. fraailis and Kluyreromyces fragilis have been used to produce artificial

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160 diet for adult lacewings (Hagen 1986) . fraailis produced on cheese whey was found to be as effective of an attractant as the enzymatic protein hydrolysate of ^. cerevisiae and not as phytotoxic when applied to cotton (Hagen 1986) . ^. f ragilis plus its whey substrate was found to be as effective as the hydrolysated yeast, ^. cerevisiae (Hagen et al. 1971) . Also whey, a dairy by-product formed in the manufacture of cheese, is high in protein and contains sufficient tryptophan needed for the attraction of lacewings (K. M. Daane, personal communication) The following chemicals also are reported to be attractive to lacewing species: methyl eugenol (Suda and Cunningham 1957) , yeast products and sugar (Hagen and Tassan 1966), terpinyl acetate (Caltagirone 1969), tryptophan (Hagen et al. 1971), caryophyllene (Flint et al. 1979), and eugenol (Wilkinson et al. 1980) . This objective of this study was to test the attraction of C. rufilabris and C. cubana so that they can be used more effectively as biological control agents of B. tabaci. Materials and Mpthndq Olfactometer Initially, attraction attempts were not succesful using an olfactometer by Vet (1983) . It was determined that the size and design of the olfactometer were not compatible with the flight behavior necessary for the lacewing adults to

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161 demonstrate attraction. Therefore, an olfactometer was constructed for the assays. Aluminum flashing material and plastic counter top were used to form a cylindar 1.1 m long and 0.58 m diameter. A modified ventilation fan ,20 cm diameter, was used to draw air through the olfactometer and exhaust it to the exterior of the room housing the olfactometer. The air intake end of the cylinder was covered by a screen and held two 10.5 x 20 cm PVC tubing sections. These were used as ports into which the different volatiles were placed and where the responding individual lacewings were trapped. One tube was used as a treatment port and the other as a control port. These ports were positioned 6 cm apart and parallel to each other at the center of the screen opening, A second screen circle of nylon extending to within 8 cm of the perimeter of the olfactometer cylinder surrounded the ports. This assured even and equal air flow through the ports by reducing the air flow immediately surrounding the ports. The port tubes extended 3 cm into the holding chamber of the olfactometer. The interior opening of each port held a removable screen funnel trap with an opening 2 cm in diameter and fitted with a section of clear plastic tubing that extended 6 cm. into the inside of the port. A removable screen cover at the exterior opening of each port completed the collection chamber used to hold the different attractants and trap the lacewings. Air flow was regulated by means of a rheostat on the fan and set at a low steady volume of 34 cm/sec at the

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162 treatment and control ports. Air flow was measured with a mechanical anemometer. In order to facilitate cleaning between different attractants, the two port cylinders were fitted with removable vinyl liners and plastic bait supports. Attractant Bioassays The £. ruf ilabris used in the experiments was supplied by Biofac insectary, Mathis, Texas and the cubana was maintained in a colony established from adults and eggs collected in the field at the Gulf Coast Research and Education Center, Bradenton, Florida. The adults were maintained on a diet of sugar, yeast (5. cerevislae) , (Delecta Yeast Flakes, Schiff Bio-Food Products, Moonachie, NJ) and water, in a 1:1:1 ratio. The larvae were fed a mixture of eggs and larvae of the velvetbean caterpillar, Anticarsia gemmatalis Hubner. The lacewings were maintained on a 5% sucrose solution from the time of eclosion until they were tested. Each lacewing was only tested once. Approximately 12 lacewing adults of the same age were placed in the olfactometer and were allowed to respond overnight to the different attractants. The temperature during the olfactometer test was maintained at 22-26°C and a 14L:10D photoperiod. Insects were removed from the port traps and the olfactometer using a modified portable hand insect vacuum (BioQuip Products, Gardena, CA) . The number and the sex of those responding were recorded and then they were added to the colony. The attractant port liners and bait holders were washed between

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163 each test with warm soapy water, rinsed with 70% ethanol and then allowed to air dry. The compounds were tested at the following concentrations: caryophyllene, a series of four dilutions ranging from 1.25 ^ll/ml H2O to 100%; methyl eugenol 100%; terpinyl acetate, 2.6 |ig/ml H2O; and L-tryptophan, 1 mg/3 ml H2O hydrolized with 1 normal NaOH or 1 mg with four drops of 5% H2O2. An artificial honeydew consisting of the same diet used for adult colony maintenance was also tested (1:1:1, sugar, yeast, water) . The yeast used in this product is 5.. cerevisiae and contained 6 mg tryptophan per gram of the yeast product. In addition, a commercial attractant product, Pred Feed I, P.M., (Custom Chemicides, Fresno, CA) , was tested at the recommended rate of 0.06 g/ml of water. When a solvent was used in the treatment, it also was included at the same concentration in the control port. Statistical Analysis fo r Olfactometer ^ « A sign-test of the binomial distribution procedure used by Dwumfour (1992) was followed for the statistical analysis of responses. Those insects caught in the treatment port were considered as a positive response designated (+) and those caught in the control port were considered a negative response and scored with (-) sign. Those not responding to either port were not included in the analyses. The attraction rate (AR) was calculated as follows: ( + )/(( + ) + (-))

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164 on the basis of the assumption that the probability of a positive response is greater than 50%. The AR was calculated for each gender separately in each replication. The AR values for each gender were then averaged for each treatment and the variance calculated. A probability level of 5% for determining significance was chosen from a table of the binomial distribution. Field trials During the spring and fall of 1992, a study was conducted at a commercial organic farm on Pine Island, Florida. The plots were set in oblong blocks of sequentially planted tomatoes that were bordered by eggplant, squash, or tomatoes separated by a single row of sugarcane used as a windbreak. During the summer of 1993, studies were conducted on squash at two commercial tomato farms located in Manatee and Hillsborough counties. Small plots of squash were set in the corners of large tomato fields and were not treated with insecticides . At the organic farm sites, the plots contained approximately 232 m^ and consisted of 12 rows of 15 m lengths with 1.2 m row spacing. Each replication consisted of a treatment plot and a control plot, which were in the same rows 46 m apart. During the summer of 1993, plots of were made from six beds of double-row squash with the same dimensions as that were used in tomatoes. In all plots and at all locations, the directional location of the treatment

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165 and control plots were alternated, north to south or east to west, in case prevailing winds had an effect on the downwind attraction of lacewings. Alternate rows of each treatment plot were sprayed weekly using a handheld COa-powered sprayer that was operated at 28 psi and delivered 10 gallons per acre. In the spring of 1992, a mixture of 0.23 kg powdered dairy whey product containing 12.6% protein, (Le-Pro SW420, Leprino Foods, Denver, CO), 0.23 kg yeast 2,. cerevisiae containing 6 mg tryptophan per gram, 0.45 kg sugar, and 3.785 L water was sprayed at the rate of 4.5 kg per acre at all test locations. This rate is necessary to provide sufficient residue on the plants of approximately the same consistency of natural honeydew (Hagen 1971) . The whey was eliminated from the formula and one 0.45 kg of yeast was substituted for the 0.23 kg of whey and yeast in the fall of 1992 and in the spring of 1993. At the organic sites, sprays were not begun until the plants had attained approximately 30 cm in height and continued until harvest. Squash plots were sprayed weekly beginning the second week after emergence through harvest. Sampling method The first season on the organic farm an older model Dvac (Dietrick 1961) was used to sample insects; however, it proved to be cumbersome in the rows of tomatoes and was unreliable mechanically. In the fall of 1992, a simpler and lighter vacuum was constructed from a five gallon plastic paint bucket adapted to fit on gasoline yard blower (PB-1010,

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166 Echo, Inc., Lake Zurich, IL) (Fig. 4.1). An organdy net was fitted into the bucket to collect arthropods. This device proved to be reliable for vacuum sampling of arthropods and was easy to handle without damaging the tomato plants. The vacuum device is small, weighs only 6 kg and can be disassembled for easy storage and transport. The cost for the blower was ca. $100.00. The modifications required for the suction of arthropods from plants was made from readily available materials. Four groups of three plants each were sampled from each plot for a total of twelve plants per plot at all locations. Plants to be sampled were selected by randomization of the rows and the plant order within each 50 foot row. The plants were vacuumed using a consistent method that was not destructive to the tomato plants. The row side of the plant was vacuumed from the bottom to the top by bumping the plant three times with the lip of the collection device, once on the bottom foliage, again in the mid foliage, and lastly on the upper foliage of the plant. Although tests have shown that the most efficient method for sampling with the D-vac is a vertical approach on the plant (Turnbull & Nicholls 1966, Shepard et al. 1972), this is not possible with tomatoes that are supported by four foot stakes and which rapidly become too large to completely cover with the net. Insects were collected in a seperate organdy net that was fitted into the

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168 insect vacuum for each sample location. The insects were transported in these nets to the laboratory for counts of whiteflies, predators, and other tomato pests. After taking the vacuum sample, the plant was inspected for lacewing oviposition sites. The number of eggs was recorded and labeled with a string indicating the number of eggs and the date in the event that the plant again fell within the randomization of plants to be sampled. A visual inspection was made of plants that had been sprayed for evidence of phytotoxicity during throughout the sampling process . Statistical analysis of Field Data A t-test was planned to compare each treatment and control plot for lacewing attraction using pooled sample data of the number of oviposition sites and total ova for each field location. The incidence of lacewing eggs was rare and was not normally distributed. Such data can often be transformed using + 0.5, when values are under 10 and zeros are present (Steel and Torrie 1980) . However, a test for normality (Shapiro & Wilk 1965), often indicated that the transformed data did not conform to a normal distribution. Therefore, the Wilcoxon rank score was used to test for differences in the mean lacewing eggs for treatment and control plots (Wilcoxon rank sum, SAS Institute 1989, 282284) . The same procedure was followed for the occurrence of other insect groups collected in the vacuum samples in the sprayed vs unsprayed plots.

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169 Results Olfactom eter assays The greatest response for all compounds and products that evoked a response was shown by Q. ruf ilabris with an AR of 0.97 {Table 4.1). £. cubana did not respond in very high numbers to any compound or product tested. No significant AR value was seen except for females to L-tryptophan. The variability among most tests was high suggesting that more replications need to be done where attraction may be in question. The lowest variability was found in the tests on caryophyllene which indicates a consistent low response and for the yeast sugar mixture with £. ruf ilabris indicating a consistently high attraction rate. The overall response was generally the greatest for the females of each species. They accounted for 62% of the response for £. ruf ilabris and 59% for £. cubana . The strongest lure among those tested was the yeastsugar artificial diet (Table 4.1). No difference was seen between responses of males and females of C. ruf ilabris (mean AR 0.97 ± 0.08 SD) . L-tryptophan that had been hydrolyzed with NaOH was the second strongest compound tested with a mean AR for male and female £. ruf ilabris of 0.64 and 0.76, respectively The females of C. cubana also indicated a strong preference for this compound with a mean AR of 0.75. The only other compounds found to be attractive were terpinyl

PAGE 186

Q CO (0 0) o o 2: CO 0) CO c o CO 0) CO r~LD ro o o o •=T m r-t o 00 rH 00 IT) rrM ^ O O O U U U S S S X o o o o (0 (X5 (0 2 2 2 S C o o p I G G (C5 m 0 o p -p >i >i u u -p -P 1 I 00 1 >1 p P -p -p Xi Xi a, (X (X a, >. >i >i >i o o H M u u >i >i +J 4J 1 1 p -p 1 1 u u m m 1-1 hi o o ^H M O O u u u o X S X X o o o o (0 (C3 (15 (tJ S 2 2 S i >i >i >i M W M M (0 nj fO 03 O O O O 00 o o rH ro to o o o o o VD CTi LO O O rH CM O O O O O CM 00 O rH rH O rH O 00 OO '3' M M O O U U (J O O O O O CM CM CM CM s m s rr; o o o o G G G C
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171 o (Ti oo n in 00 LO iH o o o o 4J *J 4-) (1) 0) J-) 4J CX5 00 00 00 o o IT) tn O O O O rr~ r~ 00 >X> O <-l ^; -H 0 a< +J 4J +J 4-1 1 +J (0 >i (fl o Cn CO 0) CO G G iH T3 0 (0 c c •H 0 (0 P Ti 0) (0 -H E d > c -(m Q) 0) u g Di c > 4-) 0) -H (0 -H T3 (1) jj 4-1 ^1 -H >i X) O Jj CO p 0 -H -p > (U -H -H 4-1 X) 3) o (fl f— +J \ 4-1 X 1) T3 0 0 d) 0) (l5 jj > iH u 0) 4-1 (0 j_) +' > >i o -r-j 0) -* — ' CO iH o jj -d (0 H (0 KM 0) •s i> jj m CO (0 CO "d (H ,—1 0 0) tC J2 G u (0 a) 0) sn T) II Di cu 4J +j •H a; 0 CO > u CO d) 1— 1 ^ ^ -H 0) 4-1 0 CO J-> M 1 1 — ' O c (0 0) »— « CO 0 0 p n) o -H -H G 0 t— ' p X) -H CO fl) jj as G ^ J to 0 •H 4-1 4-1 o 4-1 -H 0 rH 0 -P r-* i-l Oh -P 0) CO r\ \J c: c (U CO II 1 /—V M x> p •H 1 1 UJ 0) P t \ rH •a 0 cy fU 0 rH -H 0 0 c 0 (0 -p CO > Q) tH d) (0 4J (0 X( 0 0 d

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172 acetate and Pred Feed. Each compound showed some attraction for the females of £. ruf ilabrls only (mean AR rates of 0.72 and 0.73 respectively). Caryophyllene did not indicate attraction for either species at the concentrations used and was not tested further. Dean and Satasook (1983) used a Y-tube olfactometer to test Chrysoperla carnea (Steph.) and could not confirm the findings of Flint et al. (1979), that caryophyllene was attractive to that species in the laboratory or in the field. In initial olfactometer tests with caryophyllene, cotton balls were used as evaporation wicks for the volatile compound. Degradation of the cellulose by 1 N NaOH, which was used to hydrolyze the tryptophan, may have resulted in the formation of some basic sugars that were attractive to lacewings of both species. If so, it would explain some high counts in the controls for that test. There was no attraction to NaOH alone, after the cotton wick was discontinued. Further investigations of the basic and complex sugars found in honeydews for attraction of these species are anticipated. Field Trials Lacewin g attraction and oviposition Mean weekly samples of oviposition sites and total lacewing eggs at each location revealed few differences between the control and sprayed plots (Figures 4.2, 4.3, and 4.4). Although there were isolated oviposition sites with

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173 3 (0 4-) 0) c ^1 o Eh o m -P 0) C O W M H O O o a a w CO -H -rH Cn Cn > > &i o o u T T ^ CO CM aiduips / J9C[uinN uesw 1^ to o Oi o to e o 0) -P >i •H -P c 0) O P e o -p 4-1 O G -H a CO CO to c o u o CO en Cn a) T3 G m to i (0 a, to a :3 c H a c (tj n 0) c o (0 -H > o 4-1 O U 4-1 -H U (tJ c 5 ^ -H C (0 0) e Eh CM a> u 3 H CC4 tu >, (XJ M a CO to p o CM

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174

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175 Ovipos. Treat. [ I Ovipos • Cont • Eggs Treat. Eggs Cont . Figure 4.4. Plot Mean (±SE) number of oviposition sites and eggs of green lacewings in squash plots sprayed with artificial honeydew and in unsprayed plots, summer 1992.

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176 numerous eggs present, generally, oviposit ion sites were rarely encountered. High variability, highly skewed distributions and unequal variances made statistical differences difficult to detect. £. cubana deposits eggs in groups, often forming a string of as many as 7 to 15 eggs per oviposition site. Apparently, the females congregated on the tomato plants that were attractive, resulting in a highly aggregated distribution. Despite the low incidence of differences found at individual sampling dates for each location during the Spring and Fall of 1992, the mean per sample occurrence of oviposition sites and the total number of eggs at most locations was generally higher in the treatment plots than the control plots (Figs. 4.2 and 4.3). Nevertheless, the pooled weekly samples for each location were not found to be significantly different when analyzed at the P <0.05 level. Only in plot C, in the spring of 1992, was a borderline difference found for mean oviposition sites per sample and for mean number of eggs per sample (P >0.0516, and 0.0557, respectively) . In plot A, during the fall of 1992, the mean number of eggs and oviposition sites was greater in the sprayed plots than in the control plots at the P <0.05 level. The plots were sequential plantings of tomatoes with A being the first plot sampled in the season and D the latest plot sampled (Figures 4.2 and 4.3). More oviposition sites and eggs were observed early in the fall experiment and late in the spring experiment, suggesting that populations of

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lacewings may have declined in the colder months. However, there were also grower related cultural and chemical practices that may have influenced populations, as well. In the squash trials during the summer 1993, more lacewing eggs were found in the control plots than in the sprayed plots at one location (B) and no lacewing activity was found in the other location (A) (Figure 4.4) . The explanation for the absence of lacewings in plot A cannot be attributed to the presence of insecticides alone for there should have been a severe reduction in the numbers of other arthropods present, as well. However, most groups are present in relatively equal abundance in both plots as shown in the vacuum samples of each plot (Table 4.4) . There was no statistical difference in treatment vs control plots found at the P <0.05 level of significance for location B. Effects of Attractant o n Other Arthropods The tomato and squash plants were sampled with a vacuum sampler for a comparison of the possible effects of the artificial food spray as an attractant for arthropods other than chrysopids . The mean number per sample for each plot each season is given in Tables 4.2, 4.3 and 4.4. Predaceous species were not abundant in these samples. The berytid found in the spring of 1992, was not the predaceous species, Jalysus wickhami Van Duzee, but rather, Metacanthus tenellus Stal. The mirid, Cyrtopeltis modest a (Say), was common on tomatoes in the spring of 1992. Collembola, of the family Entomobridae, brown scavenger

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180 Table 4.4. Mean number of arthropods collected in vacuum samples taken from squash plots sprayed with an artificial honeydew and from unsprayed control plots. Summer 1993. Block A Block B XX XX Taxa Spray Cont. N Spray Cont. Araneae 1 c 1 b U / U , 4 1 o U c . O U . J Anthocoridae 16 0 0 0 .0 12 0 .0 0 .0 Aphidae 16 0 4 0 .4 12 0 .0 0 0 B. tabaci ^ 16 2171 .6 4293 .9 12 1366 .9 2485 .4 Berytidae 16 0 0 0 0 12 0 .0 0 0 Chrysopidae 16 1 1 0 4 12 0 .0 0 0 Cicadellidae 16 0 1 0 1 12 0 .0 0 0 Coccinellidae 16 0 0 0 0 12 0 .0 0 0 Collembola 16 0 1 0 2 12 0 .8 0 3 C. punctulatus 16 0 2 0 4 12 0 .2 0 1 Diptera 16 18 2 21 1 12 25 2 46 6 G. punctipus 16 0 1 0 3 12 0 1 0. 0 H. bractatus 16 0, 0 0 0 12 0 0 0, 0 Hymenoptera 16 2. 3 2 3 12 3. 2 3. 8 Lathridiidae 16 2. 6 3 3 12 0. 5 0. 9 Psocoptera 16 0, 2 0. 1 12 0. 0 0. 1 Thysanoptera 16 0. 1 0, 3 12 0 2 0. 3 a Each sample consists of three plants, b adult whiteflies

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181 beetles of the family Labridiidae, and psocoptera were common in both seasons . Numerous Diptera were present including Liriomyza spp. leafminers; however, they were not abundant. Various parasitic wasps were generally present, including, Encarsia spp. and Eretmocerous spp., which attack the sweetpotato whitefly. There was no significant difference between sprayed and unsprayed plots during any of the seasons studied for the attraction of other arthropods. The only instance in which a significant difference was found was for the mirid £. modesta and hymenopteran wasps in plot B, during the Spring of 1992. During the summer of 1993, the t abaci populations in control plots were nearly double those of treated plots (Table 4.4), although the differences were not significant at P <0.05. It is possible that the stickiness of the artificial spray or some other undetermined factor was repellent to the adult whiteflies in the treated plots. The severity of whiteflies on squash is evident in the large total number of adults in the vacuum samples. The excess whitefly adults in the control plots may have generated a greater amount of honeydew that had greater attraction for the lacewings than the artificial honeydew. This would explain the greater number of lacewings in the control plots. Hagen et al. (197 6) found that natural honeydew from heavy aphid infestations was more attractive to the lacewing £. carnea, than the artificial honeydew sprayed on alfalfa.

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182 Cnnclnsion an d p-iscussion The olfactometer test indicated variability in responses. Although the mean attraction of the lacewings was low and attraction difficult to detect, the overall numbers of positive responses to certain compounds or products were higher than the control . In agreement with previous findings, more females were attracted than males. In the olfactometer test Q.. ruf ilabris was attracted to the yeast spray, while £. cubana was not so strongly attracted. The majority of lacewing eggs observed in the field trials were probably £. cubana . This species of lacewing was found to be the most common in insecticide free tomatoes (see Chap. 2) . cubana oviposits clusters of eggs in a single file while £. ruf ilabris oviposits eggs singly. Another species of lacewing commonly observed on tomatoes, Chrysoperla externa (Hagen) , also deposits eggs singly. The field attraction study of the lacewings is encouraging but not very conclusive. The incidence of lacewings was low in all plots. This is most likely due to the absence of lacewings in the habitat. Although there was little statistical evidence of increased oviposition, there was a general trend for greater numbers of both oviposition sites and total eggs in treated plots. Although £. cubana was probably the most common species observed in the field, it was not greatly responsive to the yeast and sugar attractant in the olfactometer studies. In contrast, Q..

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ruf ilabris which was highly attracted to the yeast and sugar in the olfactometer, was rarely observed in the field. Further studies are planned using these spray attractants to retain and increase oviposition of Q. ruf ilabris adults released in the field.

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CHAPTER V SUMMARY AND CONCLUSIONS Introduction The issue of population regulation has emerged as a question of foremost concern in considering the possibilities of exploiting generalist predators for biological control of the sweetpotato whitefly. Predaceous arthropods were found to be common in Florida field tomatoes. One species has been found to exhibit preference for the sweetpotato whitefly in the laboratory. Others apparently are demonstrating a numerical response to whitefly populations in the field. The predator complex, as a whole, appears to be reducing the number of whiteflies. Nevertheless, during this survey, field populations of whiteflies appeared to be regulated by the availability of their food resource rather than natural enemies. When humidity and temperature are optimal, entomogenous fungi may significantly reduce whitefly populations . Given the extremely high reproduction rate of this new pest, predators alone, either individually or as a complex, have not responded in such a way as to effectively reduce whitefly populations such that economic damage is prevented on tomatoes in the field. In addition, the factor of disease 184

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185 transmission by this pest, causes it to be a particularly challenging opponent for biological control. This chapter is devoted to an evaluation of some of the findings of this study and to considerations of possible approaches for continued research in biological control of the sweetpotato whitef ly . General Discussion Predator Survey Although this survey of predaceous arthropods on tomatoes was as thorough and comprehensive as time would permit, additional seasons of monitoring could reveal seasonal variations in the species makeup of the predaceous fauna. Furthermore, the predator fauna undoubtedly differs in different cultivated and non cultivated habitats. Predators respond to their prey and their prey responds to many factors that influence their resources, ie. resource availability, plant nutrition, seasonal weather patterns, abundance of competitors, and so on. The population level for a given time is a single measurement that is the combined result of many biological processes (Reddingius and den Boer 1989) . However, this two year study, which encompassed four distinct growing seasons, revealed that the surveys were very similar both years. The greatest difference was found between the fall and spring populations each year. For

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186 instance, no brown lacewings (Hemerobiidae) were seen either fall season, but were present in both spring seasons. Over all there were few extraordinary findings in the survey. To date, 19 predator species have been observed and identified from this survey. More are expected to be confirmed and identified with time. Many species that are predaceous on whiteflies appear to be arboreal in their habitat. Therefore, these predators were not encountered in the ephemeral annual crop environment. A reliable predator gut assay perhaps would reveal additional occasional or facultative predators feeding on whiteflies. Although the information about any additional predaceous species gained from such an assay would be of interest, the ability to monitor the extent of predation in the field by each species would be an even greater aid for the accurate evaluation of the rate and extent of predation for a given species in the field. The families of predators encountered in the survey were similar to and, in some cases, identical to those that have been found attacking whiteflies on annual crops in other parts of the country (Dysart 1966, Watve & Glower 1976) . Three species were common to each survey: Coleomegilla maculata, GeoCQcis punctipus , and Orius insidiosus . Of these three, only Q.. insidiosus appeared to exhibit a strong response to whitefly numbers. During the spring of 1992, a strong numerical response correlated well with whitefly increases (see Chap 2) . That response culminated with a

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187 decline in the whitefly population. However, the decline in whitefly numbers also coincided with the characteristic resource depletion which occurs at the end of the season. As determinant tomato plants achieve maturity, they rapidly desiccate. There is a dramatic decrease in whitefly numbers near the end of the period of senescence in tomatoes (Fig 5.1) . A factor of equal importance to the response of a predator to increases in the whitefly population is the presence of a predator early in the season while whitefly densities are still very low. Such an attribute may be desirable when considering ways to manipulate predator populations such that their presence can have a greater impact on pest populations before economic losses occur. The capacity to locate prey at low density and to survive in a scarce prey habitat may prove to be of much greater significance than failure of predators to regulate whitefly populations at high densities. Predator Manipulation The fact that the natural complex of predator fauna is not regulating whitefly populations in the tomato monoculture has been apparent from the onset of this whitefly outbreak. What has not been known is which predaceous species are present throughout the various cropping seasons, what times of the growing season do they first appear, and to what extent do they prey upon whiteflies. This survey has

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188 provided answers for the first two questions. Investigation now needed to learn more about the feeding habits of the different species of whitefly predators encountered. With information about the field response of these predators to whiteflies, more can be done to investigate what manipulations might be possible to ensure their earlier presence in the field and to initiate an earlier response to increases in whitefly populations. Thus, while there is currently a failure of predators to regulate the whitefly population in this agroecosystem, it may still be possible to alter the lagging predatory responses to better synchronize with increases in whitefly populations. In the case of tomato production, as in many crops, early season avoidance of the whitefly is crucial to yield. If virus incidence can be delayed until flowering and fruiting has progressed sufficiently, then the fruit set and the vegetative growth necessary to achieve potential yield has been achieved by the plant. After this point, whiteflies, and the viruses that they transmit, would have little effect on yield or fruit quality (J. W. Scott, personal communication) . A possible objective for biological control, therefore, would be to ensure an adequate predator presence prior to an early or mid-season buildup of whiteflies. Those predators that have early responses and are able to maintain themselves at low prey densities would be the best candidates.

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189 Using data from a growth and development study that had been conducted at GCREC Bradenton research station on tomato cv 'Duke' (Marlowe et al . 1983), it was found that there was a high correlation with seasonal changes in plant height and leaf area (r = 0.9, P < 0.05) for week 4 through week 11 of the growth curves (Figure 5.3) . The seasonal growth curve for height of tomato cvs 'Sunny' (from this study) and 'Duke' was also highly correlated (r = 0.98, 0.98, 0.95, spring and fall 1992 and spring 1993, P < 0.001) which indicates that their growth pattern is nearly the same. The plant height for cv 'Sunny' also correlated well with increases in leaf area for cv 'Duke' (r = 0.94, 0.93, 0.94, spring and fall 1992 and spring 1993, P < 0.001). Thus, the leaf area data from cv 'Duke' can be used to give an estimate of the changes in leaf area for cv 'Sunny' that was grown for this survey. Increases in whitefly populations during this survey appear to be due to a continual colonization by immigrating whiteflies. Immigration started early in the season, and each spring was followed by a period of mid to late season exponential increase in whitefly populations (Figs. 5.1 & 5.2) (also chap 2). This rapid whitefly population increase follows a 3 to 4 week period of rapid increase in vegetative growth that occurs between week 5 and week 9 and ends just before the plant reaches its maximum height of between 100 and 130 cm. At this time the leaf area presented to the pest as a resource was increasing exponentially and the mean daily temperature was optimal for whitefly development. As these

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190 locally produced generations of whiteflies completed development, they began augmenting the numbers of steadily immigrating whiteflies. This explains the rapid whitefly buildup that was seen at this time each spring season. In the fall crops, summer whitefly populations colonized tomatoes early in the season but never reached the numbers as seen in the spring (Fig. 5.4, 5.5) . The most plausible late season winter temperatures do not permit rapid whitefly development . During the period in which tomato leaf area expands rapidly, resources and protection are provided for the whiteflies. Such increases mean that the potential predator is presented with an increasingly complex and ever expanding search area. Including both sides of a leaf, the total searching area that would be presented to a predator is twice the leaf area. In cv 'Duke', the search area increases from less than 1 m^ per plant up through week 5 then up to more than 12.6 m^ per plant at week 12. The average leaf area per tomato plant, with 4.5 ft between rows and 2 ft spacing between plants in rows, would amount to 21,268.17 m^ of leaf area per hectare of tomatoes (565,312 ft^ / acre). This represents 5.2 6 hectares of search area per hectare of tomatoes (12.98 acres per acre of tomatoes). It has been shown that a generalist predator's per capita predation rate is most affected by leaf area (O'Neil & Wiedenmann 1987, O'Neal & Stimac 1988) . These authors studied a group of predators associated with soybeans in Florida and Illinois

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196 and found that prey density and plant search area are related. As a plant passes through the vegetative stage of development, the leaf area changes result in an expanding search area for the predator. Predators were found to increase the amount of area searched as the plant leaf area increased and the density of prey decreased. When prey density increased, predators reduced the area searched. A constant predation rate over time resulted, rather than the predicted increased rate of predation as proposed in the functional response model of predation theory (Holling 1959a) . Therefore, during rapid growth phases of a plant, the prey density in terms of leaf area can be decreasing, although the prey population per plant is increasing. For predators, increases in the number of prey per plant may constitute little change in pest density and rates of predation due to increased time spent in searching an ever expanding area for prey. In short, prey density can change in two rather independent manners over time: through changes in prey numbers and through changes in the leaf area of the plant that affect the search area of the predator. Attractants Local extinctions of both pest and predator populations in the ephemeral tomato crop were observed over the course of a season. Since long-term stability is not a realistic option in a short term agroecosystem, the factors that are responsible for driving the pest to the point of being at or near local extinction are worthy of consideration. In the

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197 preceding section, it has been reasoned that predation is most critical for pest population suppression early in the season when prey density is low and the tomato plant is in a vegetative growth phase. Ways are needed to manipulate the abundance and synchronization of predators with pest populations early in the season. Among the recognized methods of manipulation is the mass rearing of natural enemies for timely releases to augment naturally occurring populations. However, predators released before prey colonization might result in dispersal of individuals through emigration to new habitats in search of prey. To compensate for sparse prey situations early in the season, attractants and food supplements might prove to be a viable method for retaining predators in the desired location and helping to sustain them in times of scarce resources (Chap. 4) . The ability to subsist at low prey densities would also be a necessary attribute for the success of early field releases. Polyphagy in general predators is a positive attribute that can allow the survival of predators in low prey situations. Alternative prey can thus sustain the polyphagous predator, where the specialist would have to emigrate or face starvation. The ability to switch to a more abundant alternative prey, may also prove to be a desirable feeding trait. This behavior has been observed in numerous polyphagous predators (Chap. 3) . It may allow early releases of predators to subsist on alternative prey when the pest is

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198 at low density and then switch to the pest should the pest population increase. Among the lacewings encountered in this survey, Ceraeochrysa cubana (Hagen) , was found to be present early in the season during this survey, however, the numerical response was never sufficient to mount an effective reduction of the whitefly population. This species was found to have a preference for the sweetpotato whitefly over the potato aphid, in laboratory studies (Chap. 3) . In addition, field applications of adult food supplement indicated that this species was frequently attracted to tomato plots. This species also has been successfully maintained in colony for two years. It can be reared on the same diet as that used for rearing Chrysoperla ruf llabris Burmeister, using slightly modified procedures (Chap. 3) . Therefore, £. cubana would be considered as a candidate worthy of further investigation for mass rearing methods, early field releases and attraction studies . The capacity for Chrysoperla carnea Stephens to develop slowly on sub optimal diets in the first two instars and yet develop into a normally fecund adult if presented adequate prey in the third instar was reported by Zheng et al. (1993) . This characteristic was observed in £. cubana as well (Chap. 3) . This is an additional adaptive trait that would make £. cubana desirable as a biological control agent to be used for release prior to a pest population buildup and survive for periods of limited prey.

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199 Orius insldiosus Say is another predator that was present relatively early in the season during this survey. Preference, development and attraction studies may prove this species to be another candidate worthy of early release field studies. In other studies, Orius species were shown to complete develop on the white fly, Trialeurodes vaporariorum (Westwood) , (Ekbom 1981, Kajita 1982). Recently, Q.. tristicolor White has been shown to respond to the alarm pheromone of the western flower thrips as a kairomone for finding prey (Teerling et al . 1993) . These authors also suggest the use of a kairomone for early attraction and retention of anthocorids in crop protection. This predator is able to survive during periods of low prey on alternative prey and will also supplement diet by feeding on plants (Kiman & Yeargan 1985) . Introduced Predators A thorough review of the literature indicated that the list of predaceous enemies of the whitefly has expanded from that of Mound and Halsey's (1978) . Among this list there exist numerous exotic predators that might prove to be adaptable to the local environment and successfully reduce whitefly populations. Additional surveys in suspected origins of the whitefly may reveal other potential species for introduction. An aspect of conservation and augmentation of natural enemies that will need to be considered for each species

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200 studied is the impact of their natural enemies. The possibility exists that introduced species might escape some of their natural enemies in a new environment enabling them to successfully reduce pest populations. Conversely, introduced species need to be evaluated for potential negative impact on native natural enemies and plants. There remains much work to be done on specific predator species as potential control agents for the sweetpotato whitefly. Given the environmental constraints and the ability of this whitefly to develop resistance to insecticides, biological control remains a viable alternative for continued research on control of this important pest.

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201 REFERENCES Abbassi, M. 1980. Recherche sur deux homopteres fixes des citrus, Aonidlella aurantii Mask. (Homoptera: Diaspididae) et Aleurothrixus f loccosus Mask. (Homoptera: Aleyrodidae) . Cah. Rec. Agron. : 77-157 . Abdeldaffie, E. Y. A., E. A. Elhag, & N. H. Y. Bashir. 1987. Resistance in the cotton whitefly, Bemisia Tabaci (Genn) to insecticide. Trop. Pest Mgt . 33:283-286. Abdel Gawaad, A. A., A. M. El Sayed, F. F. Shalaby, & M. R. Abo EL Ghar. 1990. Natural enemies of Bemisia tabaci Genn. and their role in suppressing the population density of the pest. Agri. Res. Rev, 68:185-195. Abdelrahman, A. A. 1986. The potential of natural enemies of the cotton whitefly in Sudan Gezira. Insect Sci . Applic. 7:69-73. Adams, P. A. 1982. Ceraeochrysa , a new genus of Chrysopinae (Neuroptera) (Studies in the new world Chrysopidae, part 2) . Neur. Int. 2: 69-75. Albuquerque, G. S., C. A. Tauber, & N. J. Tauber. 1994. Chrysoperla externa (Neuroptera: Chrysopidae) life history and potential for biological control in Central and South America. Bio. Cont . 4:8-13. Alomar, 0. 1990. Mirid bugs: another strategy for IPM on Mediterranean vegeteble crops. lOBC/WPRS Bull. 15:6-9. Alvarez, P., L. Alfonseca, A. Abud, A. Villar, R. Rowland, E. Marcano, J. Borbon, & L. Garrido. 1993. Las moscas blancas in La Republica Dominicana, pp. 34-37. In L. Hilje & 0. Arboleda [eds.]. Las Moscas Blancas (Homoptera: Aleyrodidae) en America Central Y El Caribe. Serie Tecnica, Informe Tecnico No. 205. CATIE, Turrialba, Costa Rica. Anon. 1977. Two new predators of the whitefly in Iraq. PANS 23:210.

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202 Ardon, M. L., R. A. Cuellar, & J. I. Henriquez . 1992. Reconocimento de Enemigos Naturales y Hospederos de Moscas Blancas (Homoptera: Aleyrodidae) en Tres Zonas de la Cuenca del Lago de lopango. Inginero Agronimo Thesis, Universidad de El Salvador. Arzone, A. 1976. Indagini su Tri aleurodes vaporariorum ed Encarsia tricolor in pien aria. Inf. tore fitopatol 26:510. Ashburner, M. 1981. Entomophagous and other bizarre Drosophilidae. Genetics Bio. Drosophila 3a:395-429. Babrikova, T. 1979. Study of the biology of Chrysopa pa£LL^. Rasteniev"dnii Nauki 16:95-100. Barnes, H. F. 1930. Gall midges (Cecidomyiidae) as enemies of the Tingidae, Psyllidae, Aleyrodidae and Coccidae. Bull. Entomol. Res. 21:319-329. Bartlett, M. S. 1953. Approximate confidence intervals II. More than one unknown parameter. Biometrika 40:306-317. Bartlett, M. S. 1955. Approximate confidence intervals III. A bias correction. Biometrika 42:201-204. Bathon, H., & J. Pietrzik, 1986. Zur nahrungsaufnahme des Bogen-Marienkaefers Clitostethus arcuatus (Rossi) (Col.: Coccinellidae) , einem Vertilger des Kohlmottenlaus, Aleurodes proletella Linne (Horn.: Aleyrodidae) . J. Appl. Entomol. 102:321-326. Baumgaertner, J. U., B. D. Frazier, N. Gilbert, B. Gill, A. P. Gutierrez, P. M. Ives, V. Nealis, D. A. Raworth, & C. G. Summers. 1981. Coccinellids (Coleoptera) and aphids (Hemiptera) . Can. Entomol. 113:975-1048. Bazin, M. J., V. Rapa, & P. T. Saunders. 1974. The integration of theory and experiment in the study of predator-prey dynamics, pp. 159-164. In M. B. Usher & M. H. Williamson [eds.]. Ecological Stability. Chapman and Hall, London. Beingolea, 0. G. 1980. Cotton protection through integrated control. Consultancy report TCP/SYR/001 FAO, Rome. Bellows, T. S., T. D. Paine, J. R. Gould, L. G. Bezark, & J. C. Ball. 1992. Biological control of ash whitefly: a success in progress. Calif. Agri . 46:24-28.

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228 Volterra, V. 1928. Variations and fluctuations of the number of individuals in animal species living together. Translated In R. N. Chapman, 1931. Animal Ecology. Arno, New York. Waage, J. K., & N. J. Mills. 1992. Biological control, pp. 412-430. In M. J. Crawley, [Ed.], Natural Enemies: The Population Biology of Predators, Parasites and Diseases. Blackwell Scientific Publications, Oxford. Watson, J. R. 1914. Tomato insects, Agri . Exp. Sta. Bull. 125 Univ. FL, Gainesville. Watve, C. M., & D. F. Clower. 1976. Natural enemies of the bandedwing whitefly in Louisiana. Environ. Entomol. 5(6) :1075-1078. Welch, B. L. 1951. On the comparison of several mean values: an alternative approach. Biometrika 38:330-336. Wellik, M. J., & J. E. Slosser. 1983. The Tex. Agri. Exp. St., PR 4137: Manipulation of lacewings (Neuroptera: Chrysopidae) on cabbage. Tex. A&M Univ. System, College Station . Wheeler, A. G. 1977. Studies of the arthropod fauna of alfalfa. VII. predaceous insects. Can. Entomol. 109:423427. Wheeler, A. G., Jr. 1986. A new host association for the stilt bug Jalysus spinosus (Heteroptera : Berytidae) . Entomological News 97(2):63-65. Wheeler, A. G., Jr., & T. J. Henery. 1981. Jalysus spinosus and J. wickhami : Taxonomic clarification, review of host plants and distribution, and keys to adults and 5th instars. Ann. Entomol. Soc. Am. 74:606-615. Whitcomb, W. H., & K. Bell. 1964. Predaceous insects, spiders, and mites of Arkansas cotton fields. Bulletin, 690. Univ. of Ark., Fayetteville . Whitcomb, W. H., & K. E. Godfrey. 1991. The use of predators in insect control, pp. 215-241. In D. Pimentel [ed.]. Handbook of Pest Management in Agriculture, Vol. 2. CRC Press, Boca Raton, FL.

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229 Wolda, H. 1989. The equilibirum concept and density dependence tests. What does it all mean? Oecologia 81:430432. Wool, D., D. Gerling, B. L. Nolt, L. M. Constantino, A. C. Bellotti, & F. J. Morales. 1989. The use of electrophoresis for identification of adult whiteflies (Homoptera, Aleyrodidae) in Israel and Colombia. J. Appl. Entomol. 107:344-350. Wysoki, M., & M. Cohen. 1983. Mites of the family Phytoseiidae (Acarina: Mesotigmata) as predators of the Japanese bayberry whitefly, Parabemisia myricae Kuwana (Hom. : Aleyrodidae). Agronomie 3:823-825. Yayla, A. 1986. A new benificial heteroptera (Miridae: Deraeocorine) in olive groves in Turkey. Olivae 14:12-13. Zachrisson, B., & J. Poveda. 1993. Las moscas blancas in Panama, pp. 64-66. In L. Hilje & 0. Arboleda [eds.]. Las Moscas Blancas (Homoptera: Aleyrodidae) en America Central y El Caribe. Serie Tecnica, Informe Tecnico No. 205. CATIE, Turrialba, Costa Rica. Zheng, Y., K. S. Hagen, K. M. Daane, & T. E. Mittler. 1993. Influence of larval dietary supply on the food consumption, food utilization efficiency, growth and development of the lacewing Chrysoperla carnea . Entomol. Exp. Appl. 67:1-7.

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BIOGRAPHICAL SKETCH David Ed Dean was born in Pecos, Texas, on October 13, 1947. He spent most of his early years in West Texas where his father, Ed Dean, was involved in various advisory positions in agriculture. He assisted his father in the release of biological control agents for cotton bollworm, as a boy, never thinking that he would one day prepare for a career in that area. In 1960, his family moved to Lubbock, Texas were he remained until he graduated from Coronado High School in 1966. Upon graduation he received a scholarship from the American Broadcasting Company to attend the American Academy of Dramatic Arts in New York City. Following a year and a half in New York, David entered a four year enlistment in the Marine Corps, which included a tour of duty in Vietnam as a radio operator. Upon his discharge from the service, he entered Sul Ross State University at Alpine, Texas. He graduated from there in 1975 with a Bachelor of Science degree in Animal Health and worked for Longfellow Cattle Company. David married Karen Guckert on December 28, 1973. They have two sons, Samuel David born November 27, 1975 and Jeremy Matthew born February 16, 1977. After marriage, David worked in various church related jobs which included four years of

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volunteer conununity service and construction in Mexico and South America. In 1987 David enrolled in Texas Tech University to pursue a Master of Agriculture degree. Upon completion of the program at Texas Tech, he began a PhD at the University of Florida in the department of Entomology and Nematology. He is currently a member of the Entomological Society of America, the Florida Entomological Society, the International Organization for Biological Control, and the Southeastern Biological Control Working Group.

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I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doct/r^ of Pl^ilosophy. J. "Schu^er,* Chairman Professor of Entomology and Nematology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree c Doctor of P hilosophy .\ C. S. Barf; eld/ /Cochairman Professor cx£ Entomology and Nematology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of PhMosophy. Bartz Associate Professor of Plant Pathology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy. ! b\ V nes (y Associate Professor of Plant Pathology I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctfcr of PhiLasophy. mo 6 L. S. Osborne Associate Professor of Entomology and Nematology

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This dissertation was submitted to the Graduate Faculty of the College of Agriculture and to the Graduate School and was accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy. August, 1994 _ Dean, 'College of Agriculture i,*^ollege of Agric Dean, Graduate School