-1-
A COMPARATIVE STUDY OF FOUR SPECIES OF Encarsia (HYMENOPTERA:
APHELINIDAE) AS POTENTIAL CONTROL AGENTS FOR Bemisia tabaci (GENNADIUS) (HOMOPTERA: ALEYRODIDAE)
By
ARISTOBULO LOPEZ AVILA Mo.
A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College of Science and Technology
Dept. of Pure and Applied Biology Imperial College Field Station Silwood Park Ascot, Berkshire May 1988 -2-
ABSTRACT
Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) is a serious pest of some important crops in tropical and subtropical regions of the world. The aim of this work was to study some fundamental components of the host-parasitoid interrelationship between it and four species of parasitoids of the genus Encarsia
(Hymenoptera: Aphelinidae) in order to estimate their potential for the control of the pest.
The study was conducted in the laboratory under enviromentally controlled conditions and quarantine regulations.
Some aspects of the biology and morphology of the whitefly and the effect of different host plants on its development were explored in the first phase of the study. The life cycle and survival of the immature stages of B. tabaci were influenced by the host plant on which it developed.
A comparative study of aspects of biology, morphology and ecology of the four parasitoid species was conducted. Important differences were found between species in life cycle duration, adult longevity, fecundity, sex ratio, and rates of growth of the population.
The four species of Encarsia exhibited a Holling type II functional response. The rate of attack of the parasitoids varied with the host stage exposed, increasing from the earlier to the intermediate instars and then decreasing in the pupal stage. The time spent handling the different host stages showed little variation between the four nymphal instars, but was significantly different in the pupal stage, within parasitoid species.
The calculated value of handling time in the four species was far higher than the actual observed time spent parasitizing a host. -3-
Differences in number of hosts parasitized between stages within parasitoid species were interpreted as an expression of host preference for the stages more efficiently parasitized. The second, third and fourth nymphal instars were the most efficiently parasitized.
The four species of Encarsia exhibited a predatory behaviour characterized by the host-feeding and host-mutilation habits of the females. Results suggested a particular strategy of the these parasitoids when they allocate their feeding and oviposition bouts, using more intensively the youngest and oldest host stages for feeding and the intermediate ones for oviposition. Results also suggested that the predatory behaviour is a significant contributor to the total host mortality and therefore has an important effect in the depression of the host population.
Finally, the host plant of the whitefly was shown to have a significant effect on levels of parasitism by two of the parasitoid species.
The species Encarsia cibeensis Lopez-Avila and E. adrianae Lopez-Avila were described in the course of this investigation. -4-
ACKNOWLEDGEMENTS
I am deeply indebted to many people for their help in the course of this work. Foremost among these are my supervisor Dr. J. K. Waage and my advisor Dr. D. J. Greathead for their guidance and encouragement throughout the duration of this study. Sincere thanks are also due to Professor M. P. Hassell, and Drs. T. Ludlow, M. J. Crawley, H. C. J. Godfray, M. J. W. Cock for their advice in different topics of this work.
I wish to express my deep gratitude to Mrs. A. H. Greathead for her inexhaustible patience reading and correcting the typescript.
I am very grateful for the friendship and occasional helping hand given to me by menbers of CIBC at Silwood Park especially Dr. D. J. O'Donnell, Mr. C. Speed, Mr. T. Cross and members of the Munro Lab. and Insect Ecology group at Silwood Park, Sivasubramaniam Raveendranath (Ravi), Carlos Garcia, and Mike Hochberg deserve special mention.
I would also like to thank to Dr. I. A. Mohyuddin at CIBC
Pakistan and Professor D. Gerling at Tel Aviv University who forwarded field material to establish the cultures at Silwood Park, Mr. D. J. Girling for finding literature through the computer data bank at CIE.
I wish to acknowledge the helping hand given to me by members of the Imperial College staff especially Mr. R. Webb and Mr. C. Merryman in the Glasshouses.
My sincere thanks to Dr. D. J. Greathead for the use of the CIBC facilities at Silwood Park.
For the finacial assistance I am indebted to the Instituto Colombiano Agropecuario and the Colombian people.
Finally, I wish to thank all my friends and the Silwood Park community for making my stay in England a rewarding and unforgettable experience. -5-
TABLE OF CONTENTS
Page
ABSTRACT 2
ACKNOWLEDGEMENTS 4
TABLE OF CONTENTS 5
LIST OF FIGURES 9
LIST OF TABLES 11
CHAPTER 1 INTRODUCTION 14
1.1 Bemisia tabaci as a pest 14
1.2 Biological control 16
1.3 Parasitoids as biological control agents 19
1.4 Characteristics of an effective natural enemy 23
1.5 Aims of this study 24
CHAPTER 2 LIFE HISTORY AND MORPHOLOGY OF THE HOST Bemisia tabaci 26
2.1 Review o f literature 26
2. 1. 1 Taxonomy 26
2. 1. 2 Biology 29
2. 1. 3 Distribution and host plants 30
2. 1. 4 Economic importance 30
2. 1. 5 Natural enemies 38
2. 1. 5. 1 The recorded species 38
2. 1. 5. 2 Encarsia lutea 42
2. 1. 5. 3 Eretmocerus mundus 44
2.2 Biology and morphology of Bemisia tabaci 45
2. 2. 1 Materials and methods 45
2. 2. 2 Results and discussion 50
2. 2. 2. 1 Life cycle and morphology 50
2. 2. 2. 2 Fecundity and preoviposition period 65 -6-
Page
2.2.2.3 Parthenogenesis and sex ratio 66
2.3 Life cycle on five host plant species 67
2.3.1 Matarials and methods 67
2.3.2 Results and discussion 68
CHAPTER 3 COMPARATIVE BIOLOGY, MORPHOLOGY AND ECOLOGY OF THE PARASITOID SPECIES 72
3. 1 Review of literature 72
3.1.1 Encarsia formosa 72
3.1.2 Encarsia deserti 78
3.1.3 Encarsia cibeensis and Encarsia adrianae 79
3. 2 Life history and morphology 79
3.2.1 Materials and methods 80
3.2.2 Results and discussion 84
3. 3 Effect of the host stage on parasitism and development of the parasitoid species 105
3.3.1 Materials and methods 107
3.3.2 Results and discussion 108
3. 4 Adult longevity 118
3.4.1 Materials and methods 120
3.4.2 Results and discussion 121
3. 5 Oviposition, mating and feeding behaviour 122
3.5.1 Materials and methods 126
3.5.2 Results and discussion 128
3. 6 Fecundity 140
3.6.1 Materials and methods 141
3.6.2 Results and discussion 143
3. 7 Sex ratio 152
3.7.1 Materials and methods 155 -7-
Page
3.7.2 Results and discussion 157
3.8 Rate of growth of the populations of the parasitoids 161
3.8.1 Introduction 161
3.8.2 Results and discussion 163
CHAPTER 4 EFFECT OF THE HOST DENSITY ON LEVELS OF PARASITISM AND OTHER FACTORS AFFECTING EFFICIENCY 166
4.1 Comparative functional responses 166
4.1.1 Review of literature 166
4.1.1.1 Type I Functional Response 167
4.1.1.2 Type II Functional Response 170
4.1.1.3 Type III Functional Response 172
4.1.1.4. The domed type of functional response curve 175
4.1.1.5 Estimating parameter values 176
4.1.2 Materials and methods 179
4.1.3 Results and discussion 181
4.2 Overall host mortality 219
4.2.1 Introduction 219
4.2.2 Materials and methods 222
4.2.3 Results and discussion 222
4.3 Survival of the parasitoid progeny 227
4.3.1 Introduction 227
4.3.2 Materials and methods 228
4.3.3 Results and discussion 228
CHAPTER 5 EFFECT OF THE HOST PLANT ON LEVELS OF PARASITISM 231
5.1 Introduction 231
5.2 Materials and methods 233
5.3 Results and discussion 234 -8-
Page
CHAPTER 6 GENERAL DISCUSSION AND CONCLUSIONS 237
APPENDIX 1 Two new species of Encarsia Foerster (Hymenoptera: Aphelinidae from Pakistan, associated with the cotton whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) 249
APPENDIX 2 Experimental results of effect of host density on levels of parasitism 255
APPENDIX 3 Mean number of hosts parasitized by four species of Encarsia on five stages and six densities of Bemisia tabaci 268
APPENDIX 4 Life and fertility tables and rate of growth of the populations of four species of Encarsia 270
APPENDIX 5 Partial derivatives of the functions with respect to the parameters a' and Th 274
BIBLIOGRAPHY 275 -9-
LIST OF FIGURES
Figure Page
1. The presently recorded distribution of Bemisia tabaci. 31
2. Rearing cage. 48
3. Cylindrical cage. 48
4. Bemisia tabaci egg. 62
5. Bemisia tabaci first nymphal instar. 62
6. Bemisia tabaci pupal stage. 62
7. Bemisia tabaci vasiform orifice. 62
8. Survival curves of immature stages of Bemisia tabaci. 71
9. Leaf cage and its position on a plant. 81
10. Encarsia adrianae egg. 86
11. Encarsia adrianae third larval instar. 90
12. Pupal cases. 94
13. Developmental duration of four species of Encarsia. 102
14. Relationship between parasitism and the stage of host exposed to parasitoid. 110
15. Effect of the host stage on the developmental duration of the parasitoids. 116
16. Survival curves for Encarsia formosa, E. deserti E. cibcensis and E. adrianae. 124
17. Encarsia adrianae female in oviposition posture. 129
18. Proportion of time invested by Encarsia formosa, E. deserti, E. cibcensis and E. adrianae in ovipositing and other activities during the first hour in a host patch. 133
19. Encarsia formosa superparasitism - three eggs in fourth nymphal instar of Bemisia tabaci. 135 - 10 -
Figure Page
20. Ovaries of Encarsia formosa and E. ciboensis. 146
21. Encarsia formosa number of ovarioles. 148
22. Number of mature eggs per wasp of Encarsia formosa, E. deserti, E. ciboensis and E. adrianae. 150
23. Mean number of mature eggs in ovarioles of Encarsia cibcensis and E. adrianae. 153
24. Sex ratio in cultures of Encarsia deserti, E. cibeensis and E. adrianae. 159
25. Curves representing the three types of functional responses. 173
26. 'Test leaf' and setup of functional response experiment. 182
27. Parasitism of Bemisia tabaci by Encarsia formosa, number of hosts parasitized versus host density. 185
28. Parasitism of Bemisia tabaci by Encarsia deserti, number of hosts parasitized versus host density. 187
29. Parasitism of Bemisia tabaci by Encarsia cibcensis, number of hosts parasitized versus host density. 189
30. Parasitism of Bemisia tabaci by Encarsia adrianae, number of hosts parasitized versus host density. 191
31. Parasitism of Bemisia tabaci by four species of Encarsia, number of hosts parasitized versus host density and host stage. 193
32. Functional response curves of Encarsia formosa. 198
33. Functional response curves of Encarsia deserti. 200
34. Functional response curves of Encarsia cibcensis. 202
35. Functional response curves of Encarsia adrianae. 2011
36. Age specific fertility (m ) of Encarsia formosa and E. adrianae. x 272 - 11 -
LIST OF TABLES
Table Page
1. Synonyms of Bemisia tabaci (Gennadius 1889). 28
2. Worldwide distribution of Bemisia tabaci. 32
3. Ranking of families of Bemisia tabaci host plants. 36
1. Some crops on which Bemisia tabaci is a serious pest. 37
5. Hymenoptera parasitoids recorded from Bemisia tabaci. 39
6. Predators recorded attacking Bemisia tabaci. 41
7. Duration of the cycle and size of the immature stages of Bemisia tabaci on detached bean leaves. 52
8. Duration of the life cycle and mortality of Bemisia tabaci on five different host plants. 69
9. Developmental duration and size of the immature stages of Encarsia cibcensis. 100
10. Developmental duration and size of the immature stages of Encarsia adrianae. 101
11. Developmental duration of four species of Encarsia. 104
12. Percentages of parasitism and superparasitism of Encarsia cibcensis and Encarsia adrianae on Bemisia tabaci. 106
13. Mean percentages of parasitism of four species of Encarsia on five different stages of Bemisia tabaci. 109
14. Developmental duration of Encarsia formosa females from eggs laid in different host stages. 114
15. Developmental duration of Encarsia deserti females from eggs laid in different host stages. 114
16. Developmental duration of Encarsia cibcensis females from eggs laid in different host stages. 115
17. Developmental duration of Encarsia adrianae females from eggs laid in different host stages. 115
18. Comparison of total developmental duration of four species of Encarsia from eggs laid in five different stages of Bemisia tabaci. 119 - 12 -
Table Page
19. Adult longevity of four species of Encarsia. 123
20. Oviposition of female eggs by four species of Encarsia in Bemisia tabaci. 131
21. Time spent by Encarsia deserti, E. cibcensis and E. adrianae depositing male eggs. 136
22. Mean number of ovarioles of Encarsia formosa, E. deserti, E. cibcensis and E. adrianae. 145
23. Number of eggs per female of Encarsia formosa, E. deserts, E. cibeensis and E. adrianae. 149
24. Sex ratio in cultures of Encarsia deserti, E. cibcensis and E. adrianae. 158
25. Parameters of the growth of the population of four species of Encarsia developing in third nymphal instar of Bemisia tabaci. 164
26a. Non-linear estimated parameters of the 'disc equation'. 206
26b. Non-linear estimated parameters of the 'random attack equation'. 207
27. Observed and calculated handling time (Th) for four species of Encarsia parasitizing third instar nymphs of Bemisia tabaci. 209
28. Percentages of parasitism by Encarsia formosa on five stages and six densities of Bemisia tabaci. 214
29. Percentages of parasitism by Encarsia deserti on five stages and six densities of Bemisia tabaci. 215
30. Percentages of parasitism by Enearsia eibeensis on five stages and six densities of Bemisia tabaci. 216
31. Percentages of parasitism by Encarsia adrianae on five stages and six densities of Bemisia tabaci. 217
32. Percentages of parasitism by four species of Encarsia on six densities of Bemisia tabaci. 218
33. Mortality of Bemisia tabaci caused by four species of Encarsia in five host stages. 224 - 13 -
Table Page
34. Percentages of mortality of Bemisia tabaci due to four species of Encarsia. 226
35. Progeny produced and percentages of survival per female of four species of Enearsia. 230
36. Mean number of Bemisia tabaci nymphs parasitized by four species on four different host plants. 236 - 14 -
CHAPTER 1
INTRODUCTION
1.1 Bemisia tabaci as a pest
Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) known as cotton whitefly, tobacco whitefly or sweet potato whitefly (Hafez et
al. 1983a, Horowitz, Podoler & Gerling 1984, Gerling, Motro &
Horowitz 1980, Gerling & Horowitz 1984) has been reported in some
cases as a sporadic pest and in other cases as a very serious pest throughout the tropical and subtropical regions of the world on a wide range of host plants. More than 500 species of plants in 74
families have been recorded as hosts of B. tabaci (Mound & Halsey
1978, Mound 1983, Greathead 1986a).
B. tabaci, like most of the sucking insects, causes direct
damage by withdrawing the sap of the plants and indirect damage as a
vector of virus diseases. This second aspect is perhaps the most important since it has been reported as vector of virus diseases such
as mosaics, leaf-curl, vein-clearing and yellowing on crops of
economic importance including cotton (Gossypium spp. ) (Golding 1938,
Dickson, Johnson & Laird 1954, Pollar 1955, Giha & Nour 1969), tobacco (Nicotiana tabacum) (Hemsingh & Samuel 1942, Hill 1984),
tomatoes (Lycopersicon esculentum) (Cohen & Nitzang 1966, Berling &
Dahan 1983, Castellani et al. 1982), cassava (Manihot esculenta)
(Golding 1935, Chant 1958, Bock 1983, Githunguri et al. 1984), beans - 15 -
(Phaseolus vulgaris) (Costa 1965, Grupo Paulista de Fitopatologia
1983, Gamez 1971, Chagas et al. 1984), sweet potato (Ipomea batatas)
(Loebenstein & Harpaz 1960), pigeon pea (Ca anus ca an) (Bisht &
Banerjee 1965), cucurbits (Cucurbita maxima, C. moschata, C. pepo)
(Harpaz & Cohen 1965, Cohen et al. 1983, Dodds et al. 1984). In all it is the vector of more than 25 different diseases (Costa 1976) and thus is the most important species of whitefly reported as a vector of plant diseases considered to be due to virus infection.
The cotton whitefly has affected world agriculture for a long time but due to the severity and intensity of outbreaks in recent years it has become the main pest of some crops in some countries, for example cotton in Israel (Gerling et al. 1980).
Furthermore, as well as the virus diseases it transmits, B. tabaci causes very serious indirect damage on cotton because of the abundant secretion of honeydew on to the cotton lint and the black sooty moulds that develop on it, which interfere with the spinning process and reduce lint quality (Horowitz, Podoler & Gerling 1984).
Since its first description in 1889 as Aleurodes tabaci
Gennadius (Mound & Halsey 1978), numerous synonyms have been published (Russell 1958, Hidalgo et al. 1975, Mound & Halsey 1978), due to the diversity of host plants. As an added complication, whitefly species are identified from the structure of their pupal cases and the pupal cases of many species are variable, particularly those that are polyphagous such as B. tabaci (Mound 1963,1983).
In spite of the importance of B. tabaci as a pest of many crops, knowledge of its biology, ecology and natural enemies is - 16 -
incomplete and very little work has been done, except on cotton in which several studies have been made (Greathead & Bennett 1981).
1.2 Biological control
Since one of the very first definitions of biological control
given by Smith in 1919 as "the use of all natural organic checks,
bacterial and fungal diseases as well as parasitic and predatory
insects to control insect pests", biological control of pests has
been defined in at least 30 different ways (van Lenteren 1986).
Van den Bosch, Messenger & Gutierrez (1982) discussed the
definition of the term "biological control" and concluded that while
some people hold a broad view of biological control that embraces
such factors as host resistance, autosterilization and genetic manipulation of species, the most appropiate, simple, traditional and
neatly delimited definition is given by DeBach (1964) as "the action
of parasites, predators and pathogens in maintaining another
organism's density at a lower average than would occur in their
absence".
The introduction and permanent establishment of exotic species
for the long term suppression of pests is conveniently referred to as
"classical biological control" to distinguish it from other
applications of biotic agents in pest control which either involve
periodic releases of native or exotic agents or are concerned with
manipulations intended to enhance the impact of natural enemies
already present in the crop environment" (Greathead 1986b). - 17 -
In van Lenteren's (1980) opinion biological pest control is considered to be an art by many scientists, although several efforts have been made to transfer it to the realm of science. A number of researchers (the scientists) defend a more scientific basis of pest control, others (the artists) do not mind too much about theoretical considerations, because they think that this scientific basis is still too small and they develop biological pest control mainly by trial-and-error methods.
Waage & Hassell (1982) examine the present facts on biological control and state that the use of parasitoids remains largely an art,
aided by past experience of success and failure. They add that a more fundamental approach, involving basic research and theory, has not yet contributed significantly to practical biological control.
The year 1888 has been taken as the start of serious attempts at biological control with the well known case of the introduction of
the coccinellid beetle Rodolia cardinalis (Mulsant) from Australia
into California for control of the cottony cushion scale, Icerya purchasi Maskell. In spite of this success, the first successful
introduction of a parasitoid did not take place until 1906 when Italy
imported Encarsia berlesi (Howard) from the USA for the control of
the mulberry scale, Pseudaulacaspis pentagona Targioni-Tozzetti
(Greathead 1986). Since then there have been many attempts at pest
control by the "classical biological control method", some of them ending in successful establishments but others having little success,
and maybe most resulting in failure. - 18 -
According to the most recent information (Waage & Greathead
1988) the CAB International Institute of Biological Control (CIBC) has collected records of 1063 successful establishments of 563 species of insects against some 294 pest insects in 168 countries, of these about 40% of cases achieved a substantial success. Greathead
(1986) observes that failures are difficult to document and analyse; he estimates that 570 parasitoid species have been released in classical biological control attempts on 2110 occasions.
Van Lenteren (1980) states the usual course of work in a biological control project as follows: 'The taxonomic and noxious status of the target organism are defined and the available information about the pest is collected and evaluated. A reasonably broad inventory of natural enemies including pertinent ecological details should be completed before detailed studies begin. After a first selection of candidate species the following characteristics of a natural enemy are commonly studied prior to introduction (Zwolfer,
Ghani & Rao 1976): (1) reproductive capacity and impact on host, (2) adaptation to different climates, (3) searching ability, (4) host selection, (5) synchronization (6) genetics'.
Many applied entomologists are of the opinion that pre-introduction evaluation is impossible and unreliable. Other workers state that basic research is, or may become, very important for pre-introduction evaluation (Vet & van Lenteren 1981). - 19 -
1.3 Parasitoids as biological control agents.
The term "parasitoid" was first used by Reuter in 1913 to describe a group of insects that develop as larvae on the tissues of other arthropods, which they ultimately kill (Waage & Hassell 1982).
Doutt (1959), in a'review of the biology of parasitic Hymenoptera, stated that although there may be justification for using the term
"parasitoid" it does not seem to have gained widespread usage, and it has been adopted by few authorities in this field or it has been used interchangeably with "parasite" (van den Bosch, Messenger & Gutierrez
1982). However during the last decade it has gained widespread usage
(Waage & Hassell 1982, Hassell & Waage 1984, Waage & Greathead 1988) and it has been adopted recently by the CIBC in its publications.
The parasitoid life style is summarised by Waage & Hassell
(1982); adult females forage actively for hosts, depositing eggs
through an ovipositor either in, on or near their hosts. Upon hatching, the larvae locate and begin feeding on host tissues and
pass through several developmental stages either within the host as
endoparasitoids, or on the host as ectoparasitoids. Solitary parasitoids develop singly in hosts, while gregarious parasitoids may develop in groups from eggs laid during one or more ovipositions.
Parasitoids differ from true parasites in that they almost
invariably kill their host as they complete their development, and
from predators in that only one host (prey) is required for the
parasitoid for its complete development. - 20 -
Many categorizations and a considerable terminology have been proposed which try to explain and categorize different ways in which parasitoids express their relationship with the host, differences in host range, kinds of hosts, and nature of the parasitoid development.
Van den Bosch, Messenger & Gutierrez (1982) defined the following categories of parasitoid:
Primary parasite. This occurs when a species of parasitoid develops in or upon nonparasitic hosts. These hosts may be phytophagous, saprophagous, coprophilous, polleniferous, fungiferous or predatory but in no case are they themselves parasitoids.
Hyperparasite. A hyperparasite is a parasitoid that develops on another parasitoid. There may be more than one level of hyperparasi-
tism in this kind of relationship (secondary parasitoids, tertiary parasitoids).
Endoparasitism. Parasitoids that develop within the host's body
(internally) are called endoparasites. Two categories occur:
solitary endoparasite where only a single larva completes its
development in a given host or gregarious endoparasite where several
to many larvae develop to maturity in a single host.
Ectoparasitism. This occurs when a parasitoid develops externally on
the host. As with endoparasites there are solitary or gregarious
ectoparasites.
Multiple parasitism. It is a situation in which more than one
parasitod species occur simultaneously within or upon a single host. - 21 -
In most cases one of these species overcomes the others, surviving to maturity.
Superparasitism. It is the phenomenon in which more individuals than
the number that can develop, of a given parasitoid species, occur in a single host.
Cleptoparasitism. This phenomenon occurs when a parasitoid attacks hosts that are already parasitized by another species. It differs
from hyperparasitism because it does not parasitize the previously
occurring parasitoid. The relationship between the two species is competitive, usually with success of the second species.
Adelphoparasitism. This remarkable phenomenon occurs when a species
is parasitic on itself, as in the case of certain aphelinid species in which males develop as parasitoids of females of their own
species.
This phenomenon, in which males of a parasitoid species have
different host relationships from the females was first identified and described by Flanders in 1937 (Doutt, Annecke & Tremblay 1976)
and has been referred to in many different ways since then (Flanders
1959, Zinna 1961,1962, Fernere 1965), but more recently the denomination "heteronomous hyperparasitoid" has been introduced by
Walter (1983) and a new classification is proposed by him to explain this phenomenon in Aphelinidae. In this family those species whose males always develop on conspecifics of either sex are called
"obligate autoparasitoids", those whose males are parasitic on
individuals of other species or their own species are "facultative - 22 - autoparasitoids", while "alloparasitoids" are those whose males always develop on parasitoid species other than their own.
Haeselbarth (1979) divided parasitoids into two groups on the
basis of whether they develop in a growing or non-growing host. The
former are called "koinophytic parasitoids" and the latter
"idiophytic parasitoids".
Askew & Shaw (1986) prefer to employ the terms "koinobionts" and "idiobionts" for the same categories, and define them as follows:
Koinobionts
Koinobionts include most endoparasitoids of larval and adult
insects, some groups of specialized ectoparasitoids of mobile hosts
and almost all groups of obligatory secondary parasitoids. The
parasitized host continues to be mobile and able to defend itself;
larval hosts are often not killed until they have prepared cryptic
pupation retreats. The host may not live very long after parasitism,
but the fundamental point is that the koinobiont parasitoid benefits
from the continued life of its host.
Idiobionts
Idiobionts include the many ectoparasitoids which permanently
paralyze or kill the host before the egg hatches; egg parasitoids and
pupal endoparasitoids. The host is consumed in the location and
state it is in when attacked. Many idiobiont parasitoids can
function as facultative secondary parasitoids. - 23 -
1.4 Characteristics of an effective natural enemy
There are many factors that can influence the host-parasitoid relationship and determine the amount of parasitization, and thus the success of a biological control programme. Vet, van Lenteren & Woets
(1980) state that the size and growth of both the host and parasitoid population are determined by: (1) abiotic factors such as temperature, humidity and light, (2) biotic factors such as host-plant species and host-plant conditions, (3) biological characteristics of the parasitoid species themselves.
Waage & Hassell (1982) considering the criteria that an effective natural enemy should possess, state that factors such as parasitoid foraging behaviour, fecundity, larval survival and sex ratio are important in influencing the depression of host population and/or the stability of host-parasitoid interactions after depression.
According to Huffaker, Messenger & DeBach (1971) four main characteristics are relevant to the efficiency of a natural enemy
(parasitoid or predator). They are (1) its adaptability to the varying physical conditions of the environment, (2) its searching capacity, including its general mobility, (3) its power of increase relative to that of its host and its capacity for parasitizing hosts,
(4) other intrinsic factors such as synchronization with hosts, host specificity, ability to survive host free periods and special behaviour traits that alter its performance in relationship to the density or dispersion of its host and own population. - 24 -
1.5 Aims of this study
This work is an attempt to learn which of four parasitoid species should be recommended for further field trials in order to improve the biological control of the cotton whitefly, B. tabaci, in various parts of the world, on the various crops on which this insect is an economic pest.
A comparative study of some of the fundamental components of a host-parasitoid interrelationship of four species of parasitoids in the genus Encarsia attacking B. tabaci has been conducted in order to estimate their potential for control of the pest.
An extensive review of literature on the parasitoid and host species under study was conducted. This concentrated on the host B. tabaci and the parasitoid E. formosa Gahan, which is well known as a successful biological control agent of the greenhouse whitefly
(Trialeurodes vaporariorum (Westwood)). The other parasitoids are very poorly known. Encarsia deserti Gerling & Rivnay is a recently described species, originating in the southwestern USA (Gerling &
Rivnay 1984), and E. cibeensis Lopez-Avila and E. adrianae
Lopez-Avila are new species from Pakistan, described during the development of the present work.
The biology and morphology of the cotton whitefly were studied under controlled conditions and the life cycle was worked out on five different host plants. - 25 -
A comparative study of biology and ecology of the four species of parasitoids was conducted, including life history, host susceptibility and host suitability, life cycle duration on different host stages, adult longevity, oviposition behaviour, fecundity and sex ratio.
The functional response is the classical method of investigating how a natural enemy responds to changes in the density of its host (prey). It was first defined by Solomon (1949) and extensively studied by Holling (1959a, 1959b). Since then the functional response has been widely studied and discussed by a number of workers. Some of these studies are reviewed and discussed in
Chapter 4.
The functional response studies were made on all four species, on five different host stages. The differences resulting from these experiments are analyzed as difference in efficiency of the parasitoid species.
Messenger, Wilson & Whitten (1976) stated that is desirable that a biological control agent should be able to attack the host on all of its important host plant species. This requires that the natural enemy should frequent all such species and be able to develop on hosts that use any of them for food. This aspect was investigated in this study for the four parasitoid species. The efficiency of the parasitoid species against B. tabaci was evaluated on three crop plants of which B. tabaci is a serious pest, and one weed common throughout the tropics. - 26 -
CHAPTER 2
LIFE HISTORY AND MORPHOLOGY OF THE HOST Bemisia tabaci
2.1 Review of literature
2.1.1 Taxonomy
Bemisia tabaci (Gennadius) belongs to the subfamily
Aleyrodinae, family Aleyrodidae, superfamily Aleyrodoidea, which is placed either in the suborder Homoptera of the order Hemiptera
(Richards & Davies 1977, Woodward, Evans & Eastop 1970) or in the suborder Sternorrhycha, order Homoptera (Borror & Delong 1964).
Mound & Halsey (1978) provide a catalogue of the Aleyrodidae (over
1,100 species) with much information on host plants and natural enemies.
While there are keys for classification of the aleyrodids at the generic and subfamilial level based on adult morphology (Hidalgo et al. 1975), the majority of whitefly species cannot be identified by morphological characters of the adult. The genera and species are defined on the structure of the fourth nymphal instar, the so-called
"pupal case" (Mound & Halsey 1978). Unfortunately polyphagous whitefly species, such as Trialeurodes vaporariorum (Westwood) and B. tabaci, vary in the appearance of their pupal cases depending on the form of the host plant cuticle on which they develop (Mound 1963,
Russell 1948). Mound (1963) raised offspring of a single virgin -27- female of B. tabaci on different species of plants, and demonstrated that two of these forms, from tobacco and cassava, differ significantly in shape as well as in size. He suggested that these variants are induced phenotypically by morphological characters of the host plant leaves, such as cuticle irregularity and hairiness.
It is essential to understand the significance of these morphological forms, particularly where whitefly species are vectors of diseases between crops or between crop and reservoir host plants.
B. tabaci was first described as Aleurodes tabaci from tobacco in Greece (Gennadius 1889), but host-correlated morphological variation and host-plant diversity has led to a large number of synonyms. Takahashi (1936) and Russell (1958) synonymized several described species of Bemisia with B. tabaci, and Mound & Halsey
(1978) list the synonyms given in Table 1.
Hidalgo et al. (1975) listed Bemisia hancocki Corbett as a synonym of B. tabaci but these can be separated using the key given by Mound (1965c) in his study of aleyrodids from West Africa which recognizes only these two species of Bemisia from that area.
Leon (pers. comm. cited in Hidalgo et al. 1975) suggests that
B. tabaci may be indigenous to Africa, but Mound (1965c, 1983) suggests that it originated in the Oriental Region where related species occur, and that it was introduced and dispersed from India into America and Africa by man. - 28 -
Table 1. Synonyms of Bemisia tabaci (Gennadius 1889) (from Mound & Halsey 1978)
Species Type locality
Aleurodes tabaci Gennadius 1889 Greece
A. inconspicua Quaintance 1900 USA (Florida)
Bemisia achyranthes Singh 1931 India B. bahiana Bondar 1928 Brazil
B. costa-limai Bondar 1928 Brazil
B. emiliae Corbett 1926 Sri Lanka
B. goldingi Corbett 1935 Nigeria
B. gossypiperda Misra & Lamba 1929 India, Pakistan
B. gossypiperda var.
mosaicivectura Ghesqui&re 1934 Zaire B. hibisci Takahashi 1933 Taiwan
B. inconspicua Quaintance 1900 USA (Florida) B. longispina Priesner & Hosny 1934 Egypt
B. lonicerae Takahashi 1957 Japan
B. manihotis Frappa 1938 Madagascar
B. minima Danzing 1964 USSR (Georgia)
B. minuscula Danzing 1964 USSR (Georgia)
B. nigeriensis Corbett 1935 Nigeria
B. rhodesiaensis Corbett 1935 Nigeria
B. signata Bandar 1928 Brazil
B. vayssierei Frappa 1939 Madagascar - 29 -
2.1.2 Biology
Many studies on the life cycle and morphology of B. tabaci have been carried out under different climatic conditions, on different host plants (particularly cotton), and also under different names.
One of the first studies was conducted by Misra & Lamba in 1929, on
"B. gossypiperda. " More recently Avidov (1956), Azab, Megahed &
El-Mirsawi (1970a, 1970b, 1972) and El-Helaly, El-Shazli & El-Gayar
(1971a, 1971b) carried out more complete and detailed studies on biology and morphology of B. tabaci.
The immature stages of whiteflies are usually called larvae and most workers on B. tabaci employ this term, but because of the incomplete metamorphosis which this insect undergoes, it seems to be more appropriate to call them nymphs, which is the term used here.
Azab, Megahed & El-Mirsawi (1970a, 1972), El-Helaly, El-Shazli
& El-Gayar (1971a 1971b) and Sharaf & Batta (1985) recognized four immature stages of B. tabaci between the egg and adult emergence.
They call the first three larval instars, and the fourth the pupal stage. Gerling & Foltyn (1987) subdivided the fourth stage into three substages, the same as recognized by van Lenteren et al. (1976) and Nechols & Tauber (1977) in Trialeurodes vaporariorum. They call the first "early 4th", the second "transitional" or "prepupa" and the third "pharate adult" or "pupal stage". Only two stages are recognized in this study, between the third nymphal instar and the adult emergence of B. tabaci which are described below in this
Chapter. - 30 -
2.1.3 Distribution and host plants
Distribution
B. tabaci is widespread throughout the tropical and subtropical regions of the world on a wide range of host plants. The distribution map (Figure 1) (CIE 1986) shows the world-wide distribution of the cotton whitefly (Table 2).
Host plants
B. tabaci has been reported as an extremely polyphagous species. The very wide range of host plants listed by Greathead
(1986a) includes 506 plant names representing 74 families, an increase over the list in Mound & Halsey (1978) of some 200 names and
12 families (Table 3).
2.1.4 Economic importance
As mentioned in Chapter 1, B. tabaci causes direct damage by piercing and sucking the foliage, and indirect damage as a vector of virus diseases. Both the adult and nymphal stages cause direct damage by withdrawing sap from the plant. High populations feeding on the foliage may affect the plant physiological processes, weakening growth, and causing dwarfing. Chiorotic spots appear at
feeding sites on leaf surfaces, causing leaf wilting and leaf shedding. As a consequence of foliage damage, the development of the -
Co rn
U
+-1 U
09 6 4)
44 O
O
.o
v]
N
0 C) 4)
Q) m
Laý a m w - 32 -
Table 2.11ordwide distribution of Bemisia tabaci (after CIE 1986)
Region Country References
EIROPE Cyprus Cyprus 1977,1979,1980,1981 France BMNH(1981, Provence) Greece Mound& Halsey 1978 Italy Iaccarino 1981, Patti & Rapisarda 1981, Viggiani & Battaglia 1983 Portugal Gentry 1965 Sicily Rapisarda & Patti 1983, Russo 1942 Spain Mound & Halsey 1978 Turkey Dancer 1979,1984, $engonca1982, Tunc et al. 1983, Turban et al. 1983, Uygun & Ozgur 1980 [United Kingdom] The record of Mound& Halsey (1978) has been omitted as this was based on an accidental introduction into Kent and no permanentcolony has been establised
USSR Azerbaijan SSR Moskovetz 1941 Georgian SSR Danzing 1964
AFRICA Angola Mound& Halsey 1978 Pagalu Mound& Halsey 1978 Cameroun Mound& Halsey 1978 Cape Verde Is. Lobo-Lima & Klein-Koch 1981 Central African Republic Mound & Halsey 1978 Chad Bink 1973, Bink-Moenen1983, Lourens, van der Laan & Brader 1972 Congo Matile-Ferrero 1978, Nkouka, Onore & Fabres 1981 Egypt Abdel Fattah, Sharaf & El Sebae 1983, Awadallah, Tawfik & Shalaby 1980 (Giza), El Nawawyet al. 1983, Hafez et al. 1983a, 1983b, 1983c (Upper & Lower Egypt), Khalil, Watson& Guirguis 1983 (Kafr E1-Shiekh), Shaheen1983 (Ismailia), Shanab & Awad-Allah 1982 Ethiopia Gentry 1965, Mound& Halsey 1978 Gambia King 1980, Mound& Halsey 1978 Ghana Forsyth 1966, Mound& Halsey 1978 Ivory Coast Delattre 1961, Mound& Halsey 1978 Kenya Bock 1983, De Bruijn & Guthrie 1982, Githunguri, Ndong'a & Ammadalo1984, Self 1981 Libya Gentry 1965, Viggiani 1982 Madagascar Appert 1967, Paulson & Kumashiro1985 Malawi Mound& Halsey 1978, Sauti 1982,1984 Mauritius Mound& Halsey 1978 Morocco Brander 1981 Mozambique BMNH(Lourenco Marques), Mound & Halsey 1978 Nigeria Van Rheenen 1973, Vetten & Allen 1983 Reunion Russell & Etienne 1985 Rwanda Mulindangabo& Blrandano 1984 Senegal Thewys, Herve & Larroque 1979 Sierra Leone Mound& Halsey 1978 Somalia Castellani, Nur & Mohamed1982, Skaf 1968 - 33 -
Cont. Table 2
Region Country References
AFRICA
South Africa Hill 1968 (Transvaal), 1969 Sudan Bindra 1983, Bindra & Rahman 1983, Dittrich & Ernst 1983,1985, Heijne & Peregrine 1984, Khalifa & Gameel 1983, Kisha 1984, Sidding 1984, von Arx, Baungartner & Delucchl 1983,1984, etc. Tanzania Mound& Halsey 1978 Togo Dengel 1981, Reckhaus1979 Tunisia BMNH(1980, Hanmamet) Uganda Mound& Halsey 1978 Zaire Mound& Halsey 1978 Zimbabwe BMNH(1935, Umtali; 1953, Salisbury; 1980, Chisumbanje)
ASIA
Afganistan Gentry 1965 Burma BMNH(1984, Rangoon), Crowe1985 China Chou 1949 (Chekiang, Fukien, Kwangtung, Shensi, Szechwan),Mound & Halsey 1978 India Anon. 1936 (Bihar, Andhra Pradesh), BMNH(1965, Madhya Pradesh), Butani & Jotwani 1983 (Delhi), Chavan1983 (West Bengal), Chhabra& Kooner 1981 (Punjab), Gangwar & Sachan 1981 (Meghalaya), Gupta & Singh 1983 (Uttar Pradesh), Lal & Pillai 1982 (Kerala), Muniyappa 1983 (Karnataka), Murugesan& Chelliah 1981 (Tamil Nadu), Patel & Patel 1966 (Gujarat), Patil & Pokharker 1979 (Maharashta), Satyavir 1983 (Rajasthan), Sinha & Chakrabarti 1982 (Haryana), Yein 1981 (Assam) Indonesia BMNH(1985, Sulawesi), Martin 1985 (Java), Mound& Halsey 1978 (Sumatra) Iran Habibi 1975, Monsef & Kashkooli 1978 Iraq El-Serwiy, El-Haidari & Saad1984, Rizk & Ahmed1981 Israel Berlinger & Dahan 1983, Berlinger, Dahan & Cohen1983, Gerling 1983, Gerling & Horowitz 1984, Horowitz, Podoler & Gerling 1984, Israel 1983,1984,1985 Japan Kobatake, Osaki & Inouye 1981 (Honshu), Takahashi 1955 (Shikoku) Jordan Ohnesorge 1981, Ohnesorge, Sharaf & Allawi 1980, Sharaf 1982,1984, Sharaf, Al-Musa & Nazer 1984a, 1984b Lebanon Gentry 1965 Malaysia Corbett 1935 (Malaya), Martin 1985 (Sarawak), Parker, Booth & Bellotti 1978 (Selangor) Oman BMNH(1976, Rumais, Nizwar) Pakistan Baloch & Soomro 1980 (Sind Province), Habib & Mohyuddin 1981 (Rawalpindi), Shafee & Rizri 1982 (Charsadda) Philippines Deang1969, Paulson & Kumashiro 1985 Saudi Arabia Abu Yaman1971, BMNH(1968, Riyadh) South Yemen Mound& Halsey 1978 (Aden) Sri Lanka Shivanathan 1983 Syria FAO1966 Taiwan Chang1969, Chou1949 Thailand Mabbett 1979,1980,1983, Nachapong& Mabbett 1979, Wangboonkong1981 - 34 -
Cant. Table 2
Region Country References
AUSTRALASIAAM PACIFIC ISLANDS
Australia BMNH(1962, Western Australia; 1981, Queensland; 1982, NewSouth Wales), Mound & Halsey 1978 Caroline Is. Mound& Halsey 1978 Fiji Paulson & Kumashiro 1985 Hawaii Paulson & Kumashiro1985 (Oahu) Mariana Is. Paulson & Kumashiro1985 PapuaNew Guinea Martin 1985 (Buso, Lae, Lasaranga Is., NewBritain) SolomonIs. BMNH(1977, Guadalcanal) Tuvalu BMNH(1976, Funafuti, Makin, S. Tarawa) Western Samoa BMNH(1977, Upolu, Manua)
(ERICA, NORTH
USA Arizona Butler & Henneberry 1984, Butler, Henneberry & Natwick 1985, Butler & Wilson 1984 California Butler & Henneberry 1984, Butler, Henneberry & Natwick 1985, Butler & Wilson 1984, Duffus & Flock 1982, Natwick & Zalom 1984 (District of Columbia), Russell 1975 Florida Russell 1975 Georgia Russell 1975 Maryland Russell 1975 Texas Russell 1975 Mexico Espinosa 1972, Leon 1976 (Chiapas), Leon & Sifuentes 1973
AMERICA,CENTRAL AND CARIBBEAN
Barbados Bennett & Alam 1985, BMNH(1920,1921), Paulson & Kumashiro 1985 Costa Rica BMNH(1983, N. Heredia Province) Cuba Blanco & Bencomo1978,1981 Dominican Republic BMNH(1979,San Juan) El Salvador Granillo, Anaya & Diaz 1974, Meiners et al. 1973 Guatemala Gamez 1971 Honduras Howell 1978 Jamaica BMNH(1965, Kingston), Paulson & Kumashiro 1985 Nicaragua Falcon 1971, Laboucheix 1973 Panama BMNH(1983, Darien Province), Gamez1971 Puerto Rico Bird & Sanchez1971, Bird, Sanchez& Vakili 1973
AMERICA,SOUTH
Argentina BMNH(1943, Chaco), Paulson & Kumashiro1985 Brazil Barradas & Chagas1982 (Sao Paulo), Barreto, Silva & Teixeira 1980 (Rio Grande do Sul), Bortoli & Giacomini 1981, d'Araujo e Silva et al. 1968 (Bahia, Santa Catarina, Sao Paulo), Santis 1981 Colombia Hohmann,Schoonhoven & Cardona1980, Posadaet al. 1976 Venezuela Guagllami 1967 - 35 -
reproductive structure is affected, ultimately causing heavy losses.
In general it is thought that the direct damage is not very serious and few studies have been carried out on this aspect. Mound (1965b) dem'cstrated a serious reduction in cotton yield, due to a decreased number of bolls contributing to the yield and to a decline in the weight of seed and lint per boll resulting from general weakening of the plant. Damage apparent before harvest included reduced growth, and some leaf shedding.
In addition, however, B. tabaci causes very serious indirect damage to some crops by the excretion of honeydew in all stages, especially the later nymphal instars and adult stage. The accumulation of honeydew on the plant results in the development of sooty moulds, reducing photosynthesis and other physiological processes. On cotton, because of the abundant secretion of honeydew on to the cotton lint and the black sooty moulds that develop on it, the lint quality is seriously reduced. This, according to Horowitz,
Podoler & Gerling (1984), is the most serious economic damage caused by B. tabaci to cotton.
Although B. tabaci is recognised as an important pest, there is strikingly little quantitative data on the damage it causes, or even economic thresholds. Table 4 summarizes some reports of the importance of B. tabaci as a pest on some important crops others than cotton. - 36 -
Table 3. Ranking of families of Bemisia tabaci host
plants (after Greathead 1986a)
Family No of No of species
species in family
Leguminosae 96 12,000
Compositae 56 13,000
Malvaceae 35 1,000
Solanaceae 33 2,000
Euphorbiaceae 32 2,000
Convolvulaceae 20 1,650 Cucurbitaceae 17 640
Labiatae 16 3,500
Verbenaceae 16 3,000 Cruciferae 15 3,200 Amaranthaceae 12 850
Rosaceae 12 2,000
Moraceae 10 1,400
Oleaceae 8 600 Gramineae 8 10,000
Capparidaceae 7 650
Chenopodiaceae 6 400
T1liaceae 6 450
Umbelliferae 5 2,850
3 families 4
9 families 3
15 families 2 28 families 1 - 37 -
Table 4. Some crops on which Beuisia tabaci is a serious pest (other than cotton)
Crop Occurrence References
Aubergine (Solanum melongena) Egypt Herakly & El-Ezz 1970 Beans (Phaseolus vulgaris) Central America Gamez 1971 Colombia Hohmann, Schoonhoven & Cardona 1980 Cabbage (Brassica oleracea) Micronesian Islands Esaki 1940 Cassava (Manihot esculenta) Malawi Sauti 1982 India Nair & Nambiar 1984 Rwanda Mulindangabo & Birandano 1984 Africa Herren & Bennett 1984 Kenya Bock 1984, Githunguri, Ndong'a & Amadalo 1984 Nigeria Chant 1958, Golding 1936 Chili (Capsicum frutescens) Sri Lanka Fernando & Peiris 1957 Cowpea (Vigna unguiculata) Nigeria Anno-Nyako et al. 1983 Faba beans (Vicia faba) Egypt Herakly & El-Ezz 1970 Greenhouses Turkey Uygan & Ozgur 1980 [enaf (Hibiscus cannabinus) Nigeria Donnelly 1966 Lettuce (Lactuca sativa) USA Duffus, Larsen & Liu 1986 Mung bean (Vigna radiata) India Agrawal et al. 1979 (V. mungo) India Dhuri & Singh 1985, Dhuri, Singh & Singh 1984 Okra (Hibiscus esculentus) India Dhamdhere, Bahadur & Misra 1985, Diwakar, Rajput & D'Souza 1986 Passion fruit (Passiflora edulls) Kenya Ondieki 1975 Potato (Solanun tuberosum) Egypt Herakly & El-Ezz 1970 Soybean (Glycine max) Philippines Rodrigo 1947 Egypt Shaheen 1977 Turkey Turham et al. 1983 Squash (Cucurbita pepo) Iraq Rizk & Ahmed 1981 Egypt Herakly & El-Ezz 1970 USA Nameth, Laemmlen & Dodds 1985 Sweet potato (Ipomoea batatas) USA Berger 1921 East Africa Sheffield 1957,1958 Israel Loebenstein & Harpaz 1960 Tomato (Lycopersicon esculentum) Israel Berlinger, Dahan & Shevach-Urkin 1983, Berlinger, Dahan & Cohen 1983 Somalia Castellani, Nur & Mohamed1984 Cyprus Cyprus Agricultural Institute 1986 Venezuela Debrot, Herold & Dao 1983 Brazil Flores, Silberschmidt & Kramer 1960 Egypt Shaheen 1977 Tobacco (Nicotiana tabacum) Malawi Smee 1933 Zimbabwe Chorley 1943-44 Rhodesia Jack 1936, Mossop 1932, Chorley 1939, 1943-44 South Africa Hill 1968 India Pruthi & Samuel 1942 - 38 -
2.1.5 Natural enemies
As indicated by Greathead & Bennett (1981) knowledge of natural
enemies of B. tabaci is extremely scanty. Due to the severity and
intensity of B. tabaci outbreaks during the last 10 years, the number
and scope of studies on its natural enemies have increased in some
places world-wide in recent years. The most relevant information is
summarized by Cock (1986).
2.1.5.1 The recorded species
The following catalogue of natural enemy records is an update
of the summary provided by Greathead & Bennett (1981). The natural
enemies are listed in Table 5 (parasitoids) and Table 6 (predators).
Most of these records are from cotton and almost all the parasitoids
belong to the family Aphelinidae (Hymenoptera). The single records
of an encyrtid and a ceraphronid are probably errors, so that all
true records of parasitoids are Aphelinidae. The principal genera
are Encarsia (= Prospaltella) and Eretmocerus. The genera
Prospaltella and Aspidiotiphagus were synonymized with Encarsia
(Viggiani & Mazzone 1979); under the old definitions Enearsia spp.
and Prospaltella spp. were exclusively parasitoids of whiteflies,
while Aspidiotiphagus spp. were associated with diaspidid scales.
Eretmocerus spp. are also exclusively parasitoids of whiteflies.
Species of these genera are often host specific (Gerling 1972)
The older records of predators are of Chrysopidae and
Coccinellidae, which are highly polyphagous, but it has not been - 39 -
Table S. Hymenopteraparasitolds recorded from Beeisia tabaci
Parasitoid species Locality References
Aphelinidae
Aphelosomasp. Pakistan Ahmad& Muzaffar 1977 Encarsia sp. Egypt Azab, Megahed & El-Mirsawi 1970c, Khalifa & (= Prospaltella sp. ) El-Khidir 1965 Jordan Elmosa1979, Sharaf 1982,1984 Pakistan Ahmad& Muzaffar 1977 Sudan Abdelrahnan 1986, Cowland 1934, Fulmek 1943, Shires, Murray & Sading 1983 Turkey Elmosa1979 E. aspidioticola (Mercet) Turkey Elmosa1979 E. sp. ?aurantii (Howard) Pakistan Ahmad& Muzaffar 1947 a E. desantisi We Santis) Brazil Santis 1981, Viggiani 1985 E. deserti Gerling & Rivnay Israel Gerling & Rivnay 1984 E. shafeei Hayat India Lal 1980,1983, Nair & Nambiar 1983 (= E. flava Shafee) Pakistan CIBC Pakistan Station 1983 Than E. fornosa California Gerling 1967 Jordan Elmosa1979 E. lutea (Masi) Israel Gerling 1972,1984, Gerling, Motro & Horowitz 1980, Horowitz, Motro & Gerling 1980, Wool, Gerling & Cohen1984 Italy Viggiani & Mazzone1980 Pakistan CIBC Pakistan Station 1983 Sudan Abdelrahman1986, Gameel1969 E. meritoria Gahan California Gerling 1967 E. mineoi Viggiani Libya Viggiani 1982 E. mohyuddini Shafee & Rizvi Pakistan Shafee & Rizvi 1984 E. partenopea Masi Egypt Priesner & Hosny 1940 Morocco Mimeur1946 E. smithi (Silvestri) India Pruthi & Samuel1942, Samuel1951
E. sublutea Silvestri Kenya, Malawi, & Zimbabwe Gerling 1985 Pakistgn Mohyuddinpers. comm.1986 Hawaii Gerling 1985 E. tabacivora We Santls)a Brazil Santis 1981, Viggiani 1985 E. sp. nr. tricolor Foerster Pakistan CIBC Pakistan Station 1983
Eretmocerus sp. Egypt Azab, Megahed & El-Mirsawi 1970c, El-Helaly, El-Shazli & El-Gayar 1971a Italy Viggiani & Battaglia 1983 Pakistan Ahmad& Muzaffar 1977 Sudan Joyce 1955, Shires, Murray & Sading 1983 E. aligarhensis Khan & Shafee Pakistan CIBC Pakistan Station 1983 E. californicus Howard California Gerling 1966 - 40 -
Cant. Table 5
Parasitold species Locality References
Aphelinidae
E. corni Haldeman Egypt Priesner & Hosny 1940 India Hayat 1972 Pakistan CIBCPakistan Station 1983 E. "diversicillatus Silvestri"C Egypt Khalifa & El Khidir 1965 Sudan Aldelrahman 1986, Cowland1934, Fulmek 1943 E. haldemani Howard California Gerling 1966,1967, Natwick & Zalom 1984 E. mundusMercet Kenya, Malawi, (= massi Silvestri) & Zimbabwe Gerling 1985 Egypt El-Helaly, El-Shazli & El-Gayar 1971a, Hafez et al. 1983a, 1983b, 1983c, Tawfik et al. 1983 India Hayat 1972, Pruthi 1941, Pruthi & Samuel 1942, Samuel1951 Israel Avidov 1956, Gerling 1972,1984, Foltyn & Gerling 1984, Gerling, Motro & Horowitz 1980, Horowitz, Motro & Gerling 1980, Wool, Gerling & Cohen1984 E. mundus Italy Tremblay 1959 Jordan Elmosa 1979, Sharaf 1982,1984, Sharaf & Batta 1985 Pakistan Ahmad& Muzaffar 1977, CIBC Pakistan Station 1983 Sudan Abdelrahman1986, Gameel1969 Syria Greathead & Bennett 1981 Turkey Elmosa 1979 USSR Mound& Halsey 1978 Pteroptrix bemisiae Masid India Pruthi & Samuel 1942, Samuel 1951
Encyrtidae
Adelencyrtus moderatus (Howard) (= femoralis Compere & Annecke) Pakistan Ahmad & Muzaffar 1977
Ceraphronidae
Aphanogmusfumipennis Thomsone Zaire Mound& Halsey 1978
a Encarsia bicolor de Santis E. bemisiae de Santis were renamedby Viggiani (1985) b and In lit. as E. transvena (Timberlake) ä Possible misidentification, needs confirmation It has not been possible to trace this name e Probably an error as this is normally a parasitoid of cecidomyild larvae, although once reared from a thrips (Dessert & Bournier 1971) - 41 -
Table 6. Predators recorded attacking Bemisia tabaci
Predator species Locality References
Neuroptera: Chrysopidae
Anisochrysa flavifrons (Brauer) Morocco Mimeur 1946 Brinckochrysa scelestes (Banks) India Nasir 1947, Rahman194 0 Chrysopa sp. Egypt El-Helaly, El'Shazli & El-Gayar 1971a India Thomas 1932, Husain & Trehan 1933 Brazil Link & Costa 1981 C. cymbele Banks India Nasir 1947 C. flava (Scopoll) Morocco Mimeur 1946 C. formosa Brauer Morocco Mimeur 1946 Chrysoperla carnea (Stephens) Israel Israel 1985 Pakistan CIBC Pakistan Station 1983 Sudan Abdelrahman 1986 Hemiptera: Anthocoridae
Orius albidipennis (Reuter) Sudan Abdelrahman 1986
Coleoptera : Coccinellidae
Brumoides suturalls (F. ) India Rahman 1940, Thomas 1932 Pakistan CIBC Pakistan Station 1983 Brumus sp. India Husain & Trehan 1933 Catana parcesetosa (Sicard) Pakistan CIBC Pakistan Station 1983 Coccinella septempunctata L. Pakistan CIBC Pakistan Station 1983 Coleomegilla maculata (DeGeer) Brazil Link & Costa 1981 Cycloneda sanguinea (L. ) Brazil Link & Costa 1981 Eriopis connexa (German) Brazil Link & Costa 1981 Harmonia dimidiata (F. ) Pakistan CIBC Pakistan Station 1983 Menochilus sexmaculatus (F. ) Pakistan CIBC Pakistan Station 1983 Scymnus sp. India Rahman1940
Acarina: Phytoseiidae
Amblyseius aleyrodis El Badry Sudan El Badry 1967,1968, Gameel 1971 A. chilenensis Dosse Israel Swirski, Amitai & Dorzia 1970 A. limonicus Garman & McGregor Israel Swirski & Dorzia 1968 A. swirskii Athias-Henriot Israel Teich 1966 Euselus hibisci (Chant) California Meyerdick & Coudrlet 1985 Israel Swirski, Amitai & Dorzia 1970 E. scutalis (Athias-Henriot) California Meyerdick & Coudriet 1986 (- A. rubini Swirski & Amitai) Israel Teich 1966 Typhlodromus athiasae Parath & Swirski Israel Swirski, Amitai & Dorzia 1970 T. medanicus El Badry Sudan El Badry 1967 T. occidentalis Nesbitt Israel Swirskl & Dorzia 1969 T. sudanicus El Badry Sudan El Badry 1967, Gameel 1971
Acarina: Stigmaeidae
Agistemus exertus Gonzalez Egypt Soliman et al. 1976
Acarina: Tarsonemidae
Polyphagotarsonemus latus Banks* India Gupta & Chaudhry 1972
* This is most probably an error as P. latus is a phytophagous species. _42_ shown whether whitefly are preferred or incidental prey. The predatory mites are mostly more recently recorded and some are being evaluated. Meyerdick & Coudriet (1985,1986) have conducted laboratory evaluations of Euseius hibisci (Chant) and E. scutalis
(Athias-Henriot) as biological control agents of B. tabaci.
One pathogen has been recorded attacking B. tabaci: a fungus,
Paecilomyces farinosus (Dickson & Fries) Brown & Smith, in India
(Balakrishnan & Nene 1980, Nene 1973). P. farinosus is recorded from a wide range of arthropod hosts.
Detailed information on biology, ecology and behaviour of parasitoids attacking B. tabaci is available only for the following two species.
2.1.5.2 Encarsia lutea (Masi 1910)
Taxonomy, origin and distribution
Encarsia lutea (Hymenoptera: Aphelinidae) was described as
Prospaltella lutes from two female specimens reared from a
"cochenille" on Cistus salvifolius collected at Portici, Italy (Masi
1910). Mercet (cited in Fernere 1965) described the male from one specimen collected in Spain. It has since been redescribed by
Gomes-Menor (1944), Ferriere (1965) and Viggiani & Mazzone (1980).
E. lutea is the type-species of a group of Encarsia spp. characterized by a peculiar structure of the male antennae (Viggiani
& Mazzone 1980). It also has been reported from places other than the Mediterranean Region (Table 5) - 43 -
Bionomics
Some aspects of biology and ecology of E. lutea have been studied. Gerling, Foltyn & Horowitz (in Israel 1982, p. 293) and
Foltyn & Gerling (in Israel 1984, p. 142) found that E. lutea preferred the third and fourth instar of B. tabaci for oviposition; the first and second instars were not used under normal circumstances. Developmental duration for females at 250C was 17 days and for males 15 days. Their observations also showed that E. lutea will lay more than once on the same host even when other unparasitized hosts are available.
Gerling & Foltyn (1987) studied host preferences and intraspecific and interspecific host discrimination of E. lutea.
They found that no oviposition occurred in first instar, whereas second instar nymphs as well as late fourth instar (pupae) had occasional eggs in them. The third instar was parasitized to a substantial degree and the first two stages of fourth instar showed highest parasitism. But from their experiments they were unable to conclude clearly about intra- and inter-specific host discrimination.
Gerling, Motro & Horowitz (1980) found that E. lutea and
Eretmocerus mundus were the only important natural enemies of B. tabaci in cotton fields on the costal plain of Israel, but they also found that the percentage of parasitism did not rise with increases in the population of the whitefly. Horowitz, Motro & Gerling (1981) made similar observations during the summers of 1977 and 1978. - 44 -
2.1.5.3 Eretmocerus mundus Mercet
Taxonomy, origin and distribution
Eretmocerus mundus was described by Mercet (1931) from specimens from Italy and Spain on a species of Aleurodes infesting aubergine. Ferriere (1965) synonymizes E. corni Masi with E. mundus and gives the distribution as: Algeria, Italy, Spain, and the whole
Mediterranean Region. Viggiani & Battaglia (1983) reported that E. mundus is very active parasitoid on B. tabaci in the Palaeartic
Region. It has also been reported in Egypt, Greece, Illinois (USA),
Sudan and places given in Table 5.
Bionomios
Foltyn & Gerling (1985), Gameel (1969), Hafez et al. (1983b,
1983c), Sharaf (1982), Sharaf & Batta (1985) and Tawfik et al. (1983) have studied aspects of the biology of E. mundus. The eggs are laid under all four whitefly nymphal instars, but not the pupa; second or third instar nymphs are preferred. When ovipositing, the female stands at an angle of 90°C to the host with wings raised and inserts the ovipositor under the host. The egg is laid close to the insertion point of the whitefly's proboscis into the leaf. After oviposition, the female apparently marks the host while drumming on it with her hind legs. She distinguishes already parasitized hosts from unparasitized ones and refrains from laying by former.
Discrimination is accomplished after antennal drumming only. Hence, in most cases only one egg is deposited per host. In the few cases - 45 - when two eggs were deposited, only the second egg hatched and accordingly in all cases one parasitoid adult emerged from each host pupa. Under laboratory conditions at 18°C, a mated female deposits about 15 eggs throughout its life, whereas at 30°C a mated female deposits 48 eggs and an unmated female 42 eggs. At 300C the total developmental period takes 18 days, whereas it takes 20.5 days at
25°C, 26 days at 19°C and 35 days at 12°C. Both males and females can copulate within a few hours of emergence. Parthenogenetic reproduction gives both males and females. The percentage of females in progeny of mated females averaged 81.1%, whereas female progeny of virgin females averaged only 36%. Adult parasitoids live for a maximum of 5 days at ambient conditions (mean temp. 25.6°C) when provided with water and honey.
The egg hatches only under the fourth instar or the pupa.
After hatching the first instar parasitoid larva bores into the host and develops internally. The parasitized nymph becomes swollen, and the pupa becomes brownish and is smaller than unparasitized pupae.
Pupation is within the host pupa and the adult wasp emerges through a semi-circular hole at the antero-dorsal part of the host.
2.2 Biology and morphology of Bemisia tabaci
2.2.1 Materials and methods
All insect cultures and experiments were carried out in envircnentally controlled conditions, in the quarantine unit of CIBC at Silwood Park, Ascot. The conditions were: temperature (T°) of 25
8 + 1°C, relative humidity (R. H. ) 75 +5%, photoperiod of 16: hours -u6-
ca. light: dark (L: D) by fluorescent tubesA3.500 lux.
The stock culture of B. tabaci was obtained from May & Baker;
where the insect, which originated from Sudan, is kept on tobacco.
At Silwood Park the whitefly, as well as the parasitoid
cultures, were maintained on bean plants (Phaseolus vulgaris) in
acrylic (perspex) cages with forced ventilation of the type devised
by Scopes et al. (1975) and modified by CIBC as shown in Figure 2.
The cage consists of an inverted five sided perspex box (45 x 45 x 45
cm), with two 10 cm diameter holes out in the rear wall to admit air
from a ventilation system, and two frontal openings, one rectangular
20 x 40 cm fitted with a door fixed with eight screws and one rubber
strip around the opening, the other opening circular 13 cm in
diameter, fitted with a cloth sleeve which permits handling and
watering the plants. The rear holes and the door were covered with
polyester mesh sufficiently fine to prevent insects entering or
leaving the cage.
The cages were placed open side down in plastic trays 55 x 55
cm, 5 cm high sides, the bottom lined with a sheet of capillary
matting.
The trays containing the cages with the cultures were placed in
racks fitted with ventilation system in the quarantine unit.
Two to four pots (9 cm high x 14 cm diameter) were kept per
cage each one containing three to five bean plants. Pots were
replaced as required.
+ May & Baker Ltd, Mfg. Chemists, Rainham Rd. Sth, Dagenham, Essex. -u7-
Cylindrical cages were used for studies on biology and life cycle of the whitefly on different host plants, and also for keeping the plants for experiments with parasitoids as is described later.
Cylindrical cages were made using Watkins & Doncaster cages which were modified as shown in Figure 3 in order to improve ventilation of the plants inside the cage.
Leaf cages, as described in Chapter 3, were used to confine individual whiteflies in some studies such as adult longevity, fecundity and preoviposition period.
Stereoscopic microscope, biological compound microscope (Kyowa
Optical), magnifying glasses and a basic dissecting equipment were used as required for different observations in behavioural and morphological description of the species.
The life cycle of B. tabaci was worked out on detached bean leaves as follows: bean plants were confined in oviposition (rearing) cages for 12 hours. After the oviposition period adult whiteflies were removed by spraying the plants with soapy water. Sprigs with two or three trifoliate leaves were cut, leaflets were marked and the eggs on each of them were counted. Each sprig was dipped in a glass tube (8 x 2.5 cm) filled with water and was fixed in place by means of a plug of high density foam. The glass tubes were kept in cylindrical cages. Observations were made daily, different stages counted and changes recorded.
For morphological description of the immature stages, specimens were sampled from leaflets on sprigs labelled for morphological - 48 -
Figure 2. Rearing cage; a, perspex cage; b, plastic tray; c, sheet of capillary matting; d, ventilation holes; e, airline with T-junctions; f, door; g, cloth sleeve; h, plants infested with whitefly.
Figure 3. Cylindrical cage; a, base, 23 cm diameter x 10 cm high; b, transparent plastic cylinder, 23 cm diameter x 30 cm high; c, ventilation holes, 10 cm diameter; d, experimental plant; (the top and ventilation holes were covered with polyester mesh). - 49 -
2
3 - 50 - studies. Nymphal stages were mounted directly in Berlese's fluid, pupae and pupal cases were prepared as follows: (1) maceration in potassium hydroxide (caustic potash) 10% in a staining block keeping the specimens immersed for 24 hours at room temperature, (2) washing the specimens in ten baths of distilled water to remove the caustic potash, (3) dehydration in several baths of alcohol in ascending concentrations (30,50 and 70%), for three minutes each, (4) staining in acid fuchsin for 24 hours, (5) clearing the specimens in clove oil for ten minutes, (6) mounting the specimens in Berlese's fluid.
Adults were examined as fresh specimens either dry or in alcohol
(70%).
2.2.2 Results and discussion
2.2.2.1 Lyfe cycle and morphology
Identification of the whitefly was confirmed by D. J. Williams of the C. A. B. International Institute of Entomology (CIE) as Bemisia tabaci (Gennadius).
Life cycle
Life cycle duration is the time from oviposition of the egg to the emergence of the new adult insect, also called developmental duration. It has been measured for B. tabaci in many ways: in laboratory or field conditions (El-Helaly, El-Shazli & El-Gayar
1971b, Azab, Megahed & El-Mirsawi 1971), under fixed or fluctuating - 51 - temperatures (Butler, Henneberry & Clayton 1983) or at different pH values (Berlinger, Magal & Benzioni 1983). Developmental duration has been measured also separately for the egg, for each nymphal instar, and for all immature stages together. However there is little information on the influence of the host plant on the developmental duration of B. tabaci, the only study recorded so far is by Coudriet et al. (1985).
Russell (1975) observed that, in different studies, the reported life cycle of B. tabaci varies considerably and is correlated with the climatic and host conditions. Azab, Megahed &
El-Mirsawi (1971) stated that the duration of life cycle varied from
14 to 75 days under field conditions in Egypt. The life cycle was shortest in summer (June-September) at 14-20 days (mean 16.4 days) and longest in winter (December-March) at 74-75 days (mean 74.6 days).
Results in the present study (Table 7) show a developmental duration for B. tabaci from oviposition to adult emergence of 22.28 +
0.21 days. Differences in total developmental duration on different host plants as well as separately for each of the immature stages are discussed below in section 2.4.
The egg
The egg is oval, sub-elliptical in shape, tapering towards its distal end and is provided at one side of its base with a stalk which serves to attach it to the leaf (Figure u). The dimensions (mean + - 52 -
'O N ON co MN In O -4 .4ON Y d O OOOOO E +ý W +ý N O OOOOO m U*i n V- +1 +ý +ý+I+I+I+) OM L. Ix -10 v co Let o %C c. er - rn v t` NS O .yNN ýY M E E o 00o Cl o i-ý W C) a) O N d- u9 rý %0 NMO O ONNNO +ý d O OOOOO i0 Ln EN t N O OOOOO E +ý +1+ý+1+ý+1 N N IX . -ý 1- t[) C. NO = 0. r 'r t0 %o co %0 O 'E N NM 1a 1O I. d I- O OOOOO O
dN c N to On 1- co to Ny 1n at mmNM r Na
C co %o 1- %D O. N N N O OOONO AC N 'O O OOOOO O C 0! O v T +1 +1+1+1+1+1 +1 4' 9 Ix A N OO to Of 1- co O 1[f 1-. 1ý N P. to N L .C u a+ tý M .+NN of N v ýp N L d a. .C G c 1. IA th %C UM N N a+ O OO Oý Cý Oý ON CC pp do. E .. 06 o LL rOp g0 L oO da 'a .0 to -&-p ýe c i) N i. ) N N Fý .. OS Nc d OJ cYcY r YY u CL ++ c1 u rý Ol L N0LL i0 01 C. I- uY7G a) w to v1 E +ý dLO7 4- I- 41 0' >. V- N +, Y- CL Y a N W = a f- - 53 - s. e. ) are: length 0.211 + 0.005 mm; breadth at the broadest part
0.096 + 0.002 mm; length of the stalk 0.024 + 0.003 mm. Eggs are almost always laid on the lower surface of the leaves, sometimes in small circular or semicircular groups produced by the female rotating about her feeding stylets whilst laying eggs (a characteristic of the subfamily Aleyrodinae (Mound 1983)).
The newly-laid egg has a shiny chorion, which is smooth, whitish-yellow and covered with a mealy powder. Before hatching it becomes light brown, the distal tip turns dark brown with two small red spots which correspond to the eyes of the nymph, and two yellow spots appear on the base of the egg which are the mycetomes of the nymph. Both the eyes and the mycetomes are easily visible through the chorion.
Observations on the hatching process confirm the description given by Azab, Megahed & El-Mirsawi (1971). At the time of hatching a crack appears longitudinally on one side of the egg and the cephalic end of the nymph emerges. The emerging nymph bends itself towards the leaf surface until it can grip it; the legs, as they emerge, are used to push away from the egg-shell. This process is assisted by bending and alternate contraction and expansion of the abdomen. The empty egg-shell is left on the leaf surface, maintaining its upright position and shape.
Several workers have stated that the incubation period varies mainly with the temperature and relative humidity. Avidov (1956) found that eggs are not affected by the air humidity as they are attached to the leaf; but it was found in this study that when the - 54 - leaf withers and dies, the eggs collapse even when they are about to hatch.
Azab, Megahed & El-Mirsawi (1971), rearing B. tabaci on sweet potato under field conditions in Egypt, found that the incubation period varied from three to 29 days for the periods June-September and December-January with daily mean temperatures (DMT) of 28.4°C and
14.3°C respectively. In their analysis they found a negative and highly significant correlation between DMT and the incubation period.
They also found a positive effect of RH on the incubation period.
Results on this study show that under constant conditions of
25°C, RH 75% and L: D 16: 8, the duration of the egg was 7.52 + 0.06 days on bean leaves. Similar results were obtained by Butler,
Henneberry & Clayton (1983) on cotton plants at constant temperature of 250C; they found anincubation period of 7.6 + 0.7 days. Sharaf &
Batta (1985) found an incubation period of 6.4 + 0.1 days on tomato plants at 25°C, RH 42-57% and L: D 12: 12. El-Helaly, El-Shazli &
El-Gayar (1971b) found incubation periods of 10.7 + 0.9,7.1 + 0.6, and 5.9 + 0.7 days at saturation humidity and 22.3 + 2.0,28.0 + 1.0 and 31.0 + 1.0°C respectively.
First nymphal instar
The first nymphal instar is also called the crawler, because of its habit of crawling on the leaf surface from eclosion until it finds a suitable place to settle down and start feeding. It is oval in shape and measures 0.267 + 0.007 mm long and 0.144 + 0.010 mm - 55 - broad at the broadest part. The dorsal surface is convex and the ventral surface flat. The colour is whitish-green and on each side of the abdominal cavity there is a yellow spot mycetome, which is quite apparent through the integument. Figure 5 shows the most apparent morphological characters of the first nymphal instar.
In the morphological descriptions given by Azab, Megahed &
El-Mirsawi (1970a) and El-Helaly, El-Shazli & El-Gayar (1971a) there are sixteen pairs of marginal setae of variable lengths. There are three pairs in the cephalic region, five pairs in the thoracic region, and eight pairs in the abdominal region. The anal pair is the longest. Dorsally, there are three pairs of microsetae: the
first is cephalic, the second is on abdominal segment one and the third on the abdominal segment eight. Ventrally there are also three pairs of microsetae. The small eyes are on each side of the cephalic region, situated antero-ventrally and contracted in the middle or completely divided, and are apparent as small inconspicuous red spots. Antennae are three-segmented and end in a fine spine.
Legs on the first instar are well developed and
four-segmented. The coxa is small and thick and bears one spine on the inner side; the trochanter is inconspicuous; the femur is longer than the coxa and as long as the tibia which is slender and bears a large and curved spine in the middle of its outer side. The tarsus is unisegmented and ends in two small claws.
The mouth parts are situated at the level of the front pair of
legs and comprise two pairs of stylets which correspond to the mandibles and the maxillae. The vasiform orifice (a large dorsal - 56 - opening on the last abdominal segment characteristic of whiteflies) is semi-circular and elongated; the lingula (a process within the vasiform orifice on which the honey-dew collects) is finger-shaped, has two setae and projects beyond the operculum.
The duration of the first and other nymphal instars varies and is correlated with the temperature as was stated by Azab, Megahed &
El-Mirsawi (1971). Under their study conditions, which were close to ambient conditions they found that the duration of the first instar varied from 2 to 6 days. Sharaf & Batta (1985) stated that the duration of the first instar was 2.8 + 0.2 days at 25°C, and 9.0 +
0.7 days at 14°C.
Duration of the first nymphal instar in this study was 3.70 +
0.08 days, lasting the longest time of the four nymphal instars
(Table 7).
Second nymphal instar
The body is oval in shape as in the first instar, measuring
0.365 + 0.026 mm long and 0.218 + 0.012 mm at the broadest part (at
the level of the thorax). The margin is crenulated and the marginal setae present in the first instar are missing here except the
antero-lateral, postero-lateral and caudal pairs. Azab, Megahed &
El-Mirsawi (1970b) mentioned only two pairs of marginal setae in the second instar. - 57 -
There are also three pairs of dorsal microsetae, the first are cephalic the second are situated on the abdominal segment one and the third on the abdominal segment eight on each side of, and anterior to, the vasiform orifice. El-Helaly, El-Shazli & El-Gayar (1971a) stated that there is one more pair of dorsal microsetae on the mesothorax, and two pairs of ventral microsetae, the first cephalic, situated near to the base of the mouth parts, and the second on the abdominal segment eight, situated at the same level as the dorsal pair. There are three pairs of spiracles, two pairs on the thorax and the third on abdominal segment eight.
The eyes are small, inconspicuous, and not divided as in the first instar. The antennae are atrophied, two-segmented and directed backwards. The legs are also atrophied, two-segmented, conical without setae, and end in a disc-like sucker. The mouth parts are more developed than in the first instar. The vasiform orifice is triangular, the operculum is semicircular and the lingula is long, thick, and armed with two prominent setae. The colour of the body is greenish-yellow and the mycetomes which are visible through the integument are orange-yellow.
Duration of this nymp,al instar was 1.70 + 0.06 days, which is the shortest duration of all immature stages. Similar results have been found by other workers under different laboratory and field conditions. Azab, Megahed & El-Mirsawi (1971) found the duration of this instar to vary from one to five days. Sharaf & Butler (1985) °C, reported 7.0 + 0.4 days at 14 and 2.8 + 0.1 at 25°C. - 58 -
Third nymphal instar
The body is oval, elongate with a crenulated margin, measuring
0.489 + 0.022 mm long and 0.295 + 0.018 mm broad at the level of the thorax. The third instar bears the same setae as the second instar.
There is a slight constriction of the margin at the cephalic region.
The eyes are circular, small and inconspicuous. The antennae are atrophied and directed towards the median line of the body, they look like hooks, due to the setaceous third segment bent back on the second.
The mouth"parts, as in the previous instars, are situated at the level of the front pair of legs and consist of four long stylets, but at the base there is a trapezoidal structure which is more elongate in this instar than in the two preceding ones. The legs are unsegmented, atrophied and end in a disc-like sucker. The vasiform orifice is triangular and the lingula is long and projects beyond the operculum.
The colour of the third instar is greenish-yellow and, as in the second instar, the mycetomes are orange-yellow and conspicuous.
Azab, Megahed & El-Mirsawi (1972) found that the duration of the third instar varied from two to seven days under their study conditions. They also found a negative correlation between the temperature and the duration of this instar with a variation of 0.38 day per 1°C. - 59 -
The third instar duratio; z was 2.26 + 0.075 days in this study.
Sharaf & Batta (1985) recorded a duration of 3.0 ± 0.4 days at 25°C, meanwhile El-Helaly, Ibrahim & Rawash (1977) recorded a duration of
2.00 days for the third instar under laboratory conditions of 28°C,
RH 80-90% and L: D 16: 8 hrs.
Fourth nymphal instar
Two entities are readily recognizable in the development of B. tabaci. between the third moult and adult emergence. They are referred to here as the fourth nymphal instar and the pupal stage.
The description given here for the fourth instar is comparable to those given by previous workers for the early, or freshly formed pupa.
The fourth nymphal instar is large, elliptical with the cephalic region semicircular, thin and flat with the margin crenulated and sometimes deeply indented due to the leaf hairs. It is 0.662 + 0.023 mm long and 0.440 + 0.003 mm broad. The marginal setae are as for the second and third instars, the anal pair being the most conspicuous. The dorsal setae are quite conspicuous, but vary in number from one to seven. Mound (1963) stated that when the insect develops on glabrous leaves, it has fewer setae than when it develops on hirsute leaves. When a full set of seven pairs of setae is present, its distribution is: two pairs on the cephalic region, two pairs in the thoracic region and three pairs on the abdominal region. In this instar, there is a series of dorsal and bilateral structures including tubercules, pores, porettes and ridges which - 60 - become more evident in the pupal stage.
The eyes are still small in size and apparent as two small, inconspicuous red spots. The legs are short, curved and unsegmented.
The vasiform orifice is triangular and elongated. The lingula, with a pair of setae, projects beyond the operculum towards the caudal margin. The colour of the fourth nymphal instar is greenish-yellow and the mycetomes are elongated and yellow.
Under the conditions of this study the fourth instar lasted
2.79 + 0.164 days. Sharaf & Batta (1985) recorded a duration of 4.7
+ 0.3 days at 25°C for the stage they called 4th larval instar which corresponds to the fourth nymphal instar and the pupal stage together, and El-Helaly, Ibrahim & Rawash (1977), under conditions noted for third nymphal instar, recorded for the same stage (pupa) a duration of 6.73 days. Furthermore they divided the duration of the pupal stage into two periods: the first half of the stage and the second half of the stage and recorded duration of 3.43 days 3.64 days respectively.
Pupal stage
There is no moult between the fourth nymphal instar and the pupal stage, as recognized here, but some morphological characters are quite different. The body is elliptical with the cephalic region semicircular. The dorsal surface is convex and the thoracic and abdominal segments apparent. It is 0.70 mm long and 0.376 + 0.022 mm broad at the broadest part, the mesothorax. - 61 -
The marginal and dorsal setae are as for the fourth nymphal instar, but the marginal ones are inconspicuous except the anal pair which is the most obvious of all. When the full set of seven pairs of dorsal setae is present they are arranged as in Figure 6, two pairs on the cephalic region, two pairs on the thoracic region and three pairs on the abdominal region. Ventrally, there is a pair of microsetae on the abdominal segment 8. The effect of degree of pubescence of the host plant on the number and distribution of dorsal setae in the pupal stage has been studied in detail by Mound (1963),
Azab, Megahed & El-Mirsawi (1970b) and Harakly (1974).
Pores and porettes are present in the pupal stage but they are only visible with careful staining of the pupal cases. The inverted
T-shaped fracture line of ecdysis is visible. Thoracic tracheal
folds are present in the pupa and extend between the first pair of spiracles and the body margin. TYfre are four pairs of spiracles: two thoracic and two abdominal.
The vasiform orifice is triangular as in the fourth instar and
the lingula extends beyond the operculum towards the caudal furrow, which appears only in the pupal stage. The surface of the lingula is
covered with minute microspines and is armed distally with a pair of
prominet setae. The anal (caudal) pair of setae is more than half the length of the caudal furrow (Mound 1965c) (Fugure 7).
The eyes look like two red spots constricted in the middle and are quite conspicuous, which is a distintive character of the pupal
stage. The body colour changes from geenish in the fourth instar to yellowish in this stage and the mycetomes become less apparent. - 62 -
Figure 4. Bemisia tabaci egg ready to hatch: a, longitudinal hatching line; b, nymph eye; c, nymph mycetome; d, egg stalk.
Figure 5. Bemisia tabaci first nymphal instar: D. V. dorsal view; V. V.
ventral view; a, cephalic-marginal seta; b, cephalic-dorsal
microseta; c, eye; d, thoracic-marginal seta; e, abdominal- dorsal microseta; f, abdominal-marginal seta; g, abdominal-
dorsal microseta; h, vasiform orifice; i, caudal seta; j,
anterocephalic ventral microseta; k, cephalic-ventral
microseta; 1, antenna; m, fore-leg; n, spiracle; o, mandibular and maxillary stylets; p, meso-leg; q, hind-leg; r, abdominal- ventral microseta; s, operculum; t, lingula.
Figure 6. Bemisia tabaci pupal stage: D. V. dorsal view; V. V. ventral view; a, 1st cephalic seta; b, eye; c, 2nd cephalic seta; d, 1st thoracic spiracle; e, 1st thoracic seta; f, 2nd thoracic spiracle; g, inverted T-shaped line of ecdysis; h, 2nd thoracic seta; i, 1st abdominal seta; j, abdominal segmentation; k, 3rd-4th abdominal seta; 1,8th abdominal seta; m, lingula; n, caudal furrow; o, caudal (anal) seta; p, thoracic-tracheal fold; q, fore-leg; r, meso-leg; s, hind-leg; t, mandibular and maxillary stylets; u, 1st abdominal spiracle; v, 8th abdominal- ventral microseta; w, 8th abdominal spiracle.
Figure 7. Bemisia tabaci vasiform orifice: 1,8th abdominal seta; m, lingula; n, caudal furrow; o, caudal (anal) seta; v, 8th abdominal ventral microseta; w, spiracle; x, vasiform orifice; r y, operculum.
IhL - 63 -
D. V. V. V.
ý - -1
Y ýý - III
--c %
r _, 4
1 5
D. V. I V. V.
b
ý -- " ýý>, -p d. -q ý f. _.. . ý. f 9- h. ---t
--U k-.
- -w
0--_
61 7 - 64 -
Pruthi & Samuel (1941) and Mound (1963) stated that there is a sexual dimorphism among pupae of B. tabaci; the sexes can be distinguished by size, with females produced from large pupae and males from small pupae. However Azab, Megahed & El-Mirsawi (1970a) found that male and female pupae were of similar size.
Duration of the pupal stage in this study was 4.67 + 0.09 days.
The Adult
The newly emerged adult is soft, and whitish-yellow in colour,
but after a few hours the colour changes to completely white, due to
the deposition of wax on the body and wings. The body measures from
vertex to tip of the genitalia 0.96 mm in the female and 0.82 mm in
the male, and from vertex to tip of the wings 1.30 mm in females and
1.15 mm in males. The head is more or less conical, broadest at
level of the antennae and narrow towards the mouth parts. The
antennae are long, filiform and seven-segmented. The mouth marts are of the typical piercing and sucking type.
The compound eyes are red and comprize one optical mass which
is crossed on the surface by a triangular strip-like cuticular
projection which is covered with white wax.
The adult has two pairs of wings covered with white waxy
powder; their venation is reduced. The legs are slender, the hind
pair longest. The abdomen is spindle-shaped with the vasiform
orifice dorsal, near to the apex. The male is generally smaller and - 65 - more slender than the female and they also differ in the external genitalia. The ovipositor consists of two pairs of sharply pointed lobes and, when at rest, is bent dorsally towards the vasiform orifice. The male genitalia, consisting of an aedeagus and a pair of curved claspers, is permanently extended.
Azab, Megahed & El-Mirsawi (1970a) and Gupta (1972) describe and discuss the external morphology of the adult male and female of
B. tabaci in more detail.
From data obtained over one year in Egypt Azab, Megahed &
El-Mirsawi (1971) found that in the male longevity varied from two to
17 days, while in females it varied from eight to 60 days. Butler,
Henneberry & Clayton (1983) found that at 26.7 and 32.20C males lived an average of 7.6 and 11.7 days and females an average of 8.0 and
10.4 days respectively. Sharaf & Batta (1985) stated that at 25°C females live from one to 29 days (mean 111.8) while males live from two to 19 days (mean 8.9). Under the standard laboratory conditions of this study, it was found that the longevity varied from five to 15 days (8.66 + 0.83 days) for males and five to 32 days (19.75 + 1.93 days) for females.
2.2.2.2 Fecundity and preoviposition period
Fecundity was studied on eight mated females. It was found that the number of eggs per female varied from 37 to 192 with a mean of 96.87. The average number of eggs laid per day was 6.36 with a maximum of 22. These findings show higher fecundity than the average - 66 - of 28 to 43 eggs per female reported by Husain & Trehan (1933) or 72 to 88 reported by Butler, Henneberry & Clayton (1983) or 76.0 reported by Sharaf & Batta (1985); but lower fecundity than the Azab,
Megahed & El-Mirsawi (1971) report of 48 to 394 eggs per female with a mean of 161 eggs per female. Sharaf & Batta found no significant differences in the fecundity of B. tabaci at temperatures of 14°C and
25°C despite more eggs being laid at the latter temperature. They also found preoviposition periods of 4.9 and 3.6 days for the two temperatures. In the fecundity experiments in the present work, 60% of the whitefly females started oviposition within 24 hours of emergence, 80% within 48 hours and 100% within the three first days of life.
On the other hand, Gerling, Horowitz & Baumgartner (in Israel
1985) report that there are indications' that repeated insecticide applications have created an insecticide-resistant, highly fecund
(300 eggs/female) strain of B. tabaci in Sudan.
2.2.2.3 Parthenogenesis and sex ratio
Results in this study corroborate previous findings by Azab,
Megahed & El-Mirsawi (1971), Husain & Trehan (1933), Mound (1983) and Sharaf & Batta (1985) that virgin females of B. tabaci lay eggs which give rise only to males.
The sex ratio was determined in samples taken from culture cages where B. tabaci had been reared on bean plants for more than ten generations at 25°C it was 1: 2.15 (male: female) - 67 -
Sharaf & Batta (1985) found that a decrease in temperature from
250C to 14°C caused a remarkable increase in the number of adult females. The sex ratios were: 1: 1.8 and 1: 3.1 (male: female) respectively at those temperatures.
2.3 Life cycle on five host plant species
The life cycle of B. tabaci was worked out on five different species of host plants, in order to investigate the influence of the host plant species on the developmental duration of the whitefly.
2.3.1 Materials and methods
The experiments were carried out under the controlled conditions described in Section 2.2.1.
Plants of the five species in Table 8 were grown from seeds in soil in individual plastic pots in the greenhouse. Test plants previously cleaned of any insect or mites were exposed to B. tabaci in the rearing cages for a period of 12 hours. Thereafter, adult whiteflies were removed as described above. True leaves were selected on each plant and marked with leaf labels. Cotyledonal and un-needed leaves were trimmed. Five to 20 leaves were used per species of host plant. Eggs on test leaves were counted and thereafter observed daily, different stages counted and changes - 68 - recorded, until adult emergence. The plants were kept in individual cylindrical cages. Emerged whiteflies, as well as the empty pupal skins were counted and removed daily until the last adult emerged.
Plants were discarded three days after emergence ceased.
The mortality during the different stages was recorded on the five host plants. The mortality of each stage was recorded as the difference between the number of individuals that came into the stage and the number that proceeded to the successive stage as a proportion of the original egg number.
Data were analyzed by the analysis of variance and by the least significant difference (LSD) for means separation.
2.3.2 Results and discussion
Results in this study show that the time required for B. tabaci
to complete development from egg to adult was influenced by the host
plant on which the whitefly was reared. Developmental duration from
oviposition to adult emergence as well as for each immature stage on
five different host plants was recorded as shown in Table 8. The duration of the egg stage showed small variation among host plants,
from 6.14 days on bean to 7.67 days on cotton. The first nymphal
instar had a mean duration of 3.27 days on bean, lasting from the 6th
day to the 9th day after oviposition whereas on cotton this instar
had a mean duration of 6.42 days from the 7th day to the 14th day
after oviposition. The time spent reaching the third instar, which
is considered, for other whitefly species as the most suitable stage - 69 -
ö ö P. ö -4 -4u ~co 8 - - i . - ö ö ö ö ö ö ö - .. ' C +I +I +I +I +I +I +I +I C dL V f-. t0 N N N rr M bN- N LC) Y.
Gý en -r C7% T b U[ IL) ýf 1W C C b p ö ö ö ö co ö ° ö 9 9 . e CD ö ö ö CD ö un o, N N 4J o + +I +I +I +I +I +I +I N a 4 CD in In tc co in o i M .ý M.4 M Cý M ýf 'a n F- n U) ý"ý N - N N M r-+ N N L O GJ . 4* C-i co 14 (11 (%j N LO CD CA co O 0, O O CC) GD co G! C CJ L U N b w 4-A N d L Ö co co N cli V^ O .+ . -+ y . ý 4- d aý ö ö ö ö ö ö ö ro CD '. N + +I +I +I +I +I +I +I ,F I 41C C) to CD b N co Oý 1n N N- N' CC J %C LO M M M cV u9 N N Ln
'I CC %0 0% M %D lA IA Äb 0 C) %C to %Q %o %0 O %1 N T L .0 Ö Ö Ö Ö co - CD .C- I b N - Lp Cl O O O Cl O O Llf 4- b o- +1 +I +I +I +I +I +I +I N M ~ Ö Ö N U Q M 4. ) f' ') OO +O b O to IC CV M N `r N M 4O J F I- oQ In M to N b E NC7% N -to 14%C N N fV N CV N /V C +1 O 5 u7 W r- N U a u et to to ar T LO co 9' üz O O O r+ .r N N H C O O O O O O O O i ar V- +i +I +i +I +I +I +I +I H N C < CA co C .-v C0 M aT N O d .+ m ýO M - N M at .r Y lV ý-1 L 7 oN f\ b N U) U[ to %0 t) 1 1 CN 4)I- .Nd G
L L V- b Ä O . IO CI 41 In 4+ N Cr T N C N C O0 w C T r T + - +ý U +) d L q L N ý L L. W Q d L O L Id 6 ;, 9 > v-O yý CA (1) w N W V- N 41 Y- G C N }. ' Cl +j . -. C ýO D !2 - 70 - for attack by their parasitoids (Gerling 1966b, 1966c, Nechols &
Tauber 1977a, Vet et al. 1980), varied from 11.30 days on bean to
16.77 on cotton and it had a maximum mean duration of 3.69 days on lantana (Lantana camara).
The minimum mean developmental duration was 21.5 days in bean and the maximum was 25.38 days on lantana. Coudriet et al. (1985) found that at 26.7 + 1°C development was completed in 30% less time on lettuce, cucumber, aubergine, and squash than on broccoli or carrot.
Survival
Figure 8 shows the survival curves for the immature stages on five host plants. The first nymphal instar exhibited the highest mortality on the five host plants. This could be explained by the disappearance of the crawlers which failed to settle and left the leaf.
The total mortality during the immature stages varied from
14.28% on bean to 56.09% on cotton (Table 8), this difference being significant. This could be explained by the fact that the stock culture had been kept on bean plants for some time (ca. ten generations). Furthermore the shortest developmental duration and the lowest mortality of B. tabaci on bean plants in these experiments, suggest the development of a specific B. tabaci strain adapted to the host plant, in a relatively short time. - 71 -
J Q
N MR
STAGE
Figure 8. Survival curves of immature stages of Bemisia tabaci on five different hosts under laboratory conditions. -72-
CHAPTER 3
COMPARATIVE BIOLOGY, MORPHOLOGYAND ECOLOGYOF THE PARASITOID SPECIES
3.1 Review of literature
The parasitoid species selected for the present study were:
Encarsia formosa, obtained from Glasshouse Crops Research Institute
(GCRI) (England), E. deserti from Israel, E. cibcensis and E. adrianae from Pakistan.
3.1.1 Enoarsia formosa Gahan
Origin and distribution
Encarsia formosa which is the most important biological control agent of the greenhouse whitefly Trialeurodes vaporariorum was described by Gahan (1924) from specimens collected in Idaho (USA).
The place of origin of E. formosa is unknown; Vet, van Lenteren &
Woets (1980) suggest that from the bionomics of the insect it has a tropical or subtropical origin, and that its origin must be the same as that of its main host. Russell (1948) suggests that T. vaporariorum is indigenous to the western and southwestern part of
North America.
E. Formosa has been reported as a parasitoid of T. vaporariorum in Europe, Australia, New Zealand, Canada and throughout most of the - 73 -
U. S. A. (Vet, van Lenteren & Woets 1980) and as a parasitoid of B. tabaci only in California (Gerling 1967) and Jordan (Elmosa 1979).
Biology, morphology and ecology
Various studies have been carried out on the biology, behaviour and ecology of E. formosa since the first in 1927, by Speyer (1927).
It also has been used commercially for many years to control the glasshouse whitefly but with some interruptions due to the development and introduction of synthetic organic pesticides.
According to Parr et al. (1976) no precise method for using the parasitoid was devised during the first periods: "growers merely hung up tomato leaves infested with parasitized whitefly scales when whitefly infestations appeared in the glasshouses".
During the last 10 years different methods of using E. formosa to control the glasshouse whitefly have been evaluated commercially and many studies on biology, ecology and behaviour have been conducted mainly by two research groups, one at the GCRI working on biology and the other one at the Agricultural University of
Wageningen, The Netherlands, working on ecology and behaviour. No studies have so far been conducted with E. formosa parasitizing B. tabaci.
Vet, van Lenteren & Woets (1980) review and summarize the biology and morphology of E. formosa: the adult female wasp is approximately 0.6 mm long; the colour pattern is quite distinctive: the head and thorax are dark brown to black; the abdomen is uniformly shining yellow and provided with a conspicuous ovipositor which - 74 -
extends beyond the extremity of the body. Towards the posterior end
of the abdomen on each side of the ovipositor there is a pair of
tubercles each bearing three hairs, two long and one relatively
short. The antennae are eight-jointed 0.5 mm long and light brown.
The wings are hyaline, covered regularly with short hairs and fringed
with long hairs. The male is conspicuously larger, has larger
antennae and a dark brown abdomen (more details in Fernere 1965,
Gahan 1924, Speyer 1927)
The parasitoid's life cycle consists of an egg stage, three
larval stages, a pupa and the adult stage. Nechols & Tauber (1977a)
give a development time of 16 to 22 days and state that the period of
egg and larval develcnent decreased as progressively older whitefly
stages were attacked. About 10 days after parasitization the
whitefly pupa turns black. After this blackening the larval stage of
E. formosa lasts two more days (32°C). The pupal stage averaged 7
days.
E. formosa is known to be uniparental, although males occur
rarely (Gerling 1966a). A few males were observed by Speyer (1927)
who mentioned that they occurred after a cool period. Burnett (pers.
comm. cited in Gerling 1966a) suggests that males are produced when
the parasitoid population reaches its peak of abundance. Gerling
(1966a) conducted experiments verifiying the theory that the males
develop parasitically on females.
Van Lenteren et al. (1976a, 1976b, 1980), Nell et al. (1976),
Nechols & Tauber (1977a, 1977b), the 2 and studied and analyzed
oviposition behaviour of the parasitoid, with aspects of host - 75 - selection, host discrimination and host feeding. The information is summarized by van Lenteren (1980) as follows:
1. Host-searching by E. formosa on leaves is random
2. The number of hosts parasitized per unit of time is entirely dependent on the walking speed of the parasitoid (which is strongly influenced by the structure of the leaf surface) and the number and size of the host present.
3. The third and fourth instar nymphs and the prepupae are selected for oviposition. Host selection is performed while drumming and turning on the host (antennal test) and/or while adopting oviposition posture, moving and standing still (oviposition test).
4. Host feeding occurs in all stages. Hosts used for feeding will never be parasitized and feeding was never observed in parasitized hosts.
5. E. formosa is able to distinguish parasitized from unparasitized hosts by antennal and/or ovipositional test.
6. When (almost) all suitable hosts on a leaf part are parasitized, the wasp leaves the site; thus both host selection and host discrimination contribute to dispersal.
7. The best period for introduction of E. formosa in a greenhouse will be at a time that a large part of the whitefly population is in the third or fourth nymphal stage. - 76 -
8. In mass-rearings there should be a large number of third and fourth nymphal stages of whitefly present at the time of emergence of wasps.
With regard to the number of eggs that each E. formosa female can lay Parr et al. (1976) report an average of about 50. As many as
350 eggs have been recorded from single, isolated females kept in the laboratory at 25°C and 16 h daylight (Biggerstaff pers. comm. cited in Parr et al. 1976). Scheewe (pers. comm. cited in Vet, van
Lenteren & Woets 1980) recorded 151 and 120 eggs from two females.
Vet (1980) and Vet & van Lenteren (1981) found that E. formosa laid an average of 165.6 eggs during 20 days at 17°C ; at the end of that period the wasps were still capable of laying eggs, so the total fecundity was not measured. Arakawa (1982) found the total mean fecundity to be about 450 eggs at 25 + 10C and about 20 eggs were deposited daily until the 15th day after emergence, after which a rapid decrease occurred.
Kajita & van Lenteren (1982), van Vianen & van Lenteren (1982,
1986a, 1986b) and van Lenteren et al. (1987) have studied the oogenesis and oviposition dynamics and genetic and environmental factors influencing body size, life span, number of ovarioles, and fecundity of E. formosa. Some of the most relevant findings are:
1. The overall rate of oogenesis is positively correlated with temperature and negatively correlated with the number of eggs already present in the ovarioles. Storage capacity is limited to about 2 mature oocytes per ovariole. - 77 -
2. After a few days with no possibility of ovipositing, more eggs are resorbed than are newly produced, but mature oocytes are
still present after a month without oviposition opportunities at
20°C.
3. The number of oocytes present in the ovary increases
proportionally to the number of ovarioles.
4. The number of ovarioles varies between five and 16 and is mainly influenced by environmental factors. Inheritance did not seem
to be involved, and selection for four generations failed to produce
a strain with a higher average number of ovarioles than the F1
generation.
5. Oviposition by E. formosa reaches a maximum at 25°C and
stops below 12°C or above X10°C. The rate of oogenesis is not the
limiting factor for oviposition at low temperature regimes.
6. When isolated without the possibility of parasitizing or
feeding on a host, E. formosa has a longer life span and more oocytes
per ovariole when honey is provided as food than when no food is
available. The life span with honey as a diet is longer than with
several other diets, but shorter than that of wasps that had
parasitization and host-feeding possibilities.
7. The host-plant species on which the whitefly develop affects
the lifespan of the parasitoids. - 78 -
Some controversy still persists in relation to the size of the wasp and its lifespan, van Vianen & van Lenteren (1982) found that larger animals have a longer life span, but van Lenteren et al.
(1987) found no relation between the size of the parasitoid and its life span.
3.1.2 Encarsia deserti Gerling & Rivnay
Origin and distribution
The very first reports of this species, as "E. formosa (desert form)" come from the Coachella and Imperial valley of Southern
California as well as from Yuma County, Arizona (USA) (Gerling 1967).
Gerling found that this parasitoid was slightly different from the
"conventional" E. formosa with lighter head and thorax than E. formosa, and its larvae do not cause melanization of Trialeurodes vaporariorum pupae.
During 1981-83 the "desert form" was introduced and established in Israel for the control of Bemisia tabaci, and later it was described as a new species at the Tel Aviv University, from descendants of the material received from the type locality, Poston,
Arizona (Gerling & Rivnay 1984)
Biology, morphology and ecology
Very little is known about these aspects of E. deserti. The -79- taxonomic description is given by Gerling & Rivnay (1984) and some biological characteristics are mentioned.
The hosts of E. deserti in the field are B. tabaci and
Aleurocybotus occiduus Russel (Gerling 1967) and in the laboratory it has also been reared on T. vaporariorum.
E. deserti is biparental. It reproduces as a facultative heteronomus hyperparasitoid. The males develop as hyperparasitoids on individuals of their own species or other Encarsia species. In contrast to E. formosa, no female progeny are produced by unmated females (Gerling & Rivnay 1984).
3.1.3 Enearsia cibeensis and Encarsia adrianae
As stated in Chapter 1 E. cibeensis and E. adrianae are new species described during the development of the present study. They were introduced into UK and established in culture on B. tabaci under quarantine regulation at CIBC, Silwood Park. The initial material was collected at Rawalpindi, Pakistan, from B. tabaci on Lantana camara during April and May 1985 (Lopez-Avila 1987). The taxonomic description of these two species is given in the Appendix 1
3.2 Life history and morphology
The life cycles and morphological descriptions of the four parasitoid species were worked out. E. adrianae and E. ciboensis were - 80 -
studied in more detail than the other two species. Various studies
have been carried out for E. formosa on these aspects and E. deserti is currently under study in Israel.
3.2.1 Materials and methods
All the studies on biology of the parasitoid species were
conducted in the quarantine unit under the controlled conditions
described in Chapter 2.
Stock cultures of the four parasitoid species were established
on B. tabaci on bean plants in rearing cages.
Leaf cages were used for life history studies, made with
polystyrene hinged boxes X31 from Stewart Plastic Boxes and
Containers Ltd. The cage consisted of a box of dimensions 83x57x16
mm in which two 30 mm diameter holes were cut in the lid and one in
the base, to allow circulation of air. These holes were covered with
polyester mesh sufficiently fine to prevent insects entering or
leaving the cage. A slot was out in the side wall of the base and
lined with plastic foam, to fit around the petiole of a leaf. The
cage was supported by a galvanized wire support fixed on a tray by
plastic tape. One leaf attached to the plant was inserted into the
cage with the petiole passing through the slot in the wall as shown
in Figure 9. - 81 -
Figure 9. Leaf cage and its position on a plant. - 82 -
Bean plants were heavily infested with B. tabaci according to the method described before. These plants were kept in cylindrical
cages until day 12 after oviposition then were set up on a tray and
leaves having whitefly nymphs (third instar) were confined in leaf cages.
Adults of the parasitoid species were obtained from the stock cultures by collecting leaves with parasitized whitefly pupae and keeping them in butter dishes. Adults were collected every 24 hours and placed in glass vials. They were fed with very small droplets of honey smeared on the walls of the vial. Females were kept with
abundant males, at least a proportion of 1: 1, except for E. formosa.
These females were assumed to be all mated after 24 hours.
Mated females were taken from the vials with a miniaspirator
made with a glass pasteur pipette (145 mm) and a plastic tube,
chilled in the refrigerator for one minute and then introduced into
the leaf cages. After 24 hours wasps were removed and the plants
taken back into the cylindrical cages.
The number of hosts per leaf was 300 to 500, the number of
wasps per leaf cage was 25 to 30, and the number of leaves per
parasitoid species was 10 to 12. The leaf cages were divided into two groups, one for the female life cycle and the second one to study
the male life cycle.
Female life cycle
Random samples of 20 whitefly nymphs (or pupae), were taken
daily from each test leaf (replicate) and dissected in saline - 83 - solution (0.1%) under a dissecting microscope. The number of hosts parasitized, parasitoid stage and parasitoid size as well as morphological description were recorded. After eight days following oviposition all the whitefly pupae parasitized per leaf were recorded and removed daily by cutting one small piece of leaf around each one using a scalpel, and kept singly in gelatine capsules until adult emergence.
Male life cycle
Mature female larvae (third instar) or prepupae of the same species were used as host for male development. Six to eight days after the first parasitism, hyperparasitism was allowed in the same way as described above for primary parasitism. Samples of ten parasitized whitefly pupae were taken per replicate (leaf) daily and similar procedures to those decribed for female life cycle were followed.
The above procedure was followed with E. adrianae and E. cibeensis. In addition to these studies, general developmental duration was determined for the four parasitoid species. The number of days from oviposition to pupation and from pupation to adult emergence were recorded.
Morphological descriptions of the immature stages as well as adult insects were made during these experiments. Both adults and immature stages were examined directly in saline solution or after mounting on slides in Berlese's fluid. In the latter case specimens were mounted directly or after clearing and staining. Glacial acetic - 84 - acid was used for clearing and acid fuchsin for staining.
The measurements were made on fresh specimens in saline solution under a stereomicroscope with a micrometric eyepiece (Kyowa optical). Specimens were measured as follows: adult length from vertex to tip of the abdomen, when breadth is given it was measured at the thorax level between tegulae; egg measured from tip to tip and at the broadest part; larval length from head to tip of the tail and breadth at the thorax level. The duration of the egg stage was determined for E. adrianae and E. cibcensis for both female and male.
The size of the egg was measured 24 hours after oviposition in all four species and for E. adrianae three days after oviposition also.
3.2.2 Results and discussion
Adult specimens of the four species of parasitoids were deposited in the Britsh Museum (Natural History).
The development of the four species of parasitoids studied here consists of the egg stage, three larval instars, a prepupal substage a pupal stage and the imago. The four species are 'facultative autoparasitoids'. Females develop as primary parasitoids on nymphal stages of the whitefly and males develop as hyperparasitoids of immature stages of females of their own or other Encarsia species. E. formosa is a uniparental species and the other three are biparental species. These aspects were investigated and are discussed later in this Chapter. - 85 -
Immature stages of the four species of Encarsia studied here are morphologically similar but differ in aspects such as size, developmental duration and some effects of the parasitoid development on the host appearence. Taking into account these aspects, a general morphological description of the immature stages is given here for the four parasitoid species, emphasising those aspects of the life cycle in which they differ.
The egg
The egg is laid within the body fluid of the host, where it floats freely (Figure 10). It is oval in shape, rounded at the anterior end and pointed at the posterior end. Embryonic development is apparent the day after oviposition, and the first instar larva is visible, through the chorion, during the last day of incubation.
Duration of the egg stage was longer for females than for males irrespective of the species in which it was recorded, and was shorter in E. cibeensis than in E. adrianae (Tables 9& 10).
The size of the egg of the four species showed small variation, being 0.127 x 0.047 mm in E. Formosa, 0.123 x 0.047 mm in E. deserti,
0.118 x 0.040 mm in E. cibeensis, and 0.133 x 0.050 mm in E. adrianae. It was also found that the egg enlarges during embryonic development in the four species of parasitoids; the enlargement was measured in eggs of E. adrianae and was from 0.133 x 0.05 mm to 0.222 x 0.110 mm during the three days of incubation. - 86 -
.;ýý_ ý.
Figure 10. Encarsia adrianae; egg in fourth nymphal instar of Bemisia tabaci. -87-
The larva
The larval development of Encarsia species studied here closely resembles the larval development of Encarsia pergandiella
Howard, described by Gerling (1966b). It has three larval instars which differ mainly in size, developmental duration and some morphological characteristics between female and male.
The larva is dilated at the anterior end and tapers towards the posterior end and has 13 body segments in each of the three instars.
First larval instar
First instar larvae can be found floating freely within the host from the third to the sixth day after egg deposition.
The cephalic segment possesses several oral appendages of which the mandibles are the most apparent and are triangular in shape and bear a solerotized tooth.
The cuticle is transparent and the internal organs such as oesophagus and gut are visible through it. Segment 13 is a tail.
First instar larvae of the male differ from those of the female in their external appearance. The female larva has a smooth appearance whereas the male larva has a serrate appearance due to each segment being conspicuously wider around the middle than around the intersegmental joints. - 88 -
Gerling (1966b) found that the development of the first instar of E. pergandiella male takes place within the egg chorion and it
starts to moult into the second instar before leaving the egg. In contrast, in the present study it was found that the first instar of
the male larva hatches and lasts for one to two days before moulting into the second instar.
Second larval instar
The second larval instar has a mean duration of about one and a half days and can be found from the third to the eighth day after oviposition depending upon the species and the sex (Tables 9& 10).
The tail is shorter than in the first instar and the cuticle and the cephalic appendages are like those of the first instar.
The second instar larva of the male loses the serrate appearance of the first instar and its surface becomes smooth. It is similar to the second instar larva of the female.
Third larval instar
The third larval instar develops in one and a half to three days and can be found from the sixth to the tenth day after oviposition. It has 13 body segments as-in the preceding instars but has not a tail. The cuticle is transparent and the internal organs such as oesophagus, gut and ileo-labial glands and tracheal system are visible through it. - 89 -
The ileo-labial glands are similar to those described by
Gerling (1966b) for E. pergandiella, resemble the same kind of glands
described by Zinna (1961,1962) for Coccophagus bivittatus Compere and Coccophagoides similis (Masi).
The third instar starts in a semiliquid environment and ends in a nearly dry one. It has a tracheal system which comprises two main
tracheal trunks and five pairs of well developed funnel-shaped spiracles located on thoracic segments two and three and abdominal
segments two, three and seven, this is different from the nine pairs of spiracles observed by Gerling (1966b) for E. pergandiella.
The third instar larva of the female and the male are morphologically similar, but at the end of the instar they are in different surroundings. When the female larva has finished consuming the contents of the whitefly host, it settles down in the empty whitefly pupal case and is ready to cast its meconium (Figure 11a).
On the other hand when the male larva has finished consuming the host within the whitefly case it is surrounded by the dorsal integument
(cocoon) and meconium of the female if the development took place in a female pupa as in Figure 11b, but if the host was a female larva only a few traces of it can be eventually found.
At the end of third instar the larva casts its meconium which consists of six to eight pellets which are discharged alternately on each side of the host puparium. The larva changes its shape, becoming shorter and wider until the pupal form is completely differentiated. - 90 -
Figure 11. Encarsia adrianae; a, late third larval instar 9 (stained with acid fuchsin) in an empty case of the whitefly; b, late third larval instar (j' developed in a conspecific female pupa, notice the outer whitefly pupal case (transparent), and the female pupal cocoon (black) and meconium (yellow). - 91 -
I
ý`ý
a
10
b - 92 -
This process takes from a few hours to one day and is known as the prepupal stage.
The pupa
Because of some morphological differences in the pupation process among the four species of parasitoids two groups are considered for morphological description.
E. formosa and E. deserti pupate in a similar way. They do not cause melanization of the B. tabaci puparium as the former does in T. vaporariorum (Speyer 1927), so the pupa of the parasitoid is quite apparent through the pupal skin of the whitefly. The pupa normally lies face downward with the head towards the anterior end of the whitefly case. The head is dark and the eyes and the antennae are quite visible. The thorax which is also dark bears the wingfolds.
The abdomen is yellow and notal sclerites are fully differentiated, appendicular segments and outlines of the ovipositor and hairs on the wings are clearly visible. The whole body occupies most of the cavity of the whitefly case. On the third to fourth day all externally visible organs and coloration are as in the adult, and the female pupa can be distinguished from the male pupa, the whole body of the latter being dark brown (see adult description).
At the last day of pupal'stage, the full-grown adult turns over on its axis and chews a hole in the dorsum of the host puparium through which the adult emerges. In most cases the exit hole is made in the anterodorsum but in some cases it is out through the operculum or even laterally. After adult emergence the whitefly case remains - 93 - transparent with the parasitoid's meconium within at each side
(Figure 12a).
Neither E. adrianae nor E. cibcensis causes melanization of the B. tabaci puparium which remains transparent during the pupal stage of the parasitoid, but the pupa of these parasitoid species is covered by a pupal cocoon which is made by the late third instar larva with material probably originating in the ileo-labial glands.
The pupal cocoon is black in colour hiding the pupal structures.
Pupal development and morphology are as described above.
It was found that when a female of either E. adrianae or E. cibeensis emerges, the remaining whitefly case is transparent containing the parasitoid meconium on each side and the parasitoid pupal cocoon which is plicated by the emerging wasp to the posterior end of the whitefly case (Figure 12c). But when a male emerges, two kinds of case can be produced, if the male develops from an egg laid in a second or third instar larva (female), the case is quite similar to the female's, as in Figure 12c; but if the male develops from an egg laid in a prepupa or pupa (female) the remaining case is as in
Figure 12b, and three pupal exuviae can be distinguished: the outer which is transparent and belongs to the whitefly, the middle one is black, belongs to the pupa of the female and has an exit-hole similar to the one in the whitefly case, and finally the inner one which is the male's exuvium, is black and is plicated by the emerging male to the posterior end of the female's case.
These findings suggest that in these species when hyperparasitism takes place in the larval stage of the female, male development prevents female pupation. - 94 -
Figure 12. Pupal cases; a, this type of case is produced by emerging Encarsia
formosa and E. deserti of both sexes; b, E. cibcensis and E. adrianae
males produce this type of case only when hyperparasitism takes place
in females in prepupa or pupa stages; c, this type of case is
produced by females of E. cibcensis and E. adrianae as well as by
males when hyperparasitism takes place in females in larval stage. - 95 -
The adult
E. Formosa. The adult female is approximately 0.6 mm long. The mean length of 50 specimens was 0.58 + 0.009 mm; the head and thorax
are dark brown to black; the abdomen is uniformly bright yellow and
shining provided with a conspicuous ovipositor which extends beyond
the extremity of the body. Towards the posterior end of the abdomen
on each side of the ovipositor there is a pair of tubercles each bearing three hairs, two long and one relativaly short. The wings are hyaline, covered with small hairs; the tips and trailing edges of the wings are fringed with long hairs. When the adult is at rest, the wings are held straight back over the body. The antennae are
eight-jointed and 0.5 mm long and yellow and the legs are also yellow.
Speyer (1927) stated that the male is conspicuously larger than
the female, but data from the present work do not confirm this
information. The mean length of 20 male specimens was 0.498 + 0.008 mm; Gahan (1924) gave the same size (0.6 mm) for both male and
female. The male can be distinguished from the female by the colour pattern: the whole body including the abdomen is dark brown to black, legs and antennae are light brown and the wings are hyaline opalescent covered with small hairs.
E. deserti. The adult female is about 0.5 mm long. The mean length of 30 specimens was 0.514 + 0.004 mm; the head and thorax are
light brown; the gaster is pale yellow; legs are pale and as in E.
Formosa the mid tarsus is four-segmented and fore and hind tarsi are - 96 - five-segmented. Other morphological characters are also similar to
E. formosa. The antennae are eight-segmented, with flagellum filiform, consisting of four funicular and two club segments. In general appearance the female is pale and smaller than the female of
E. formosa.
The adult male is smaller than the female. The mean length of
30 specimens was 0.436 + 0.005 mm. The whole body including the gaster is brown, antennae and legs light brown to yellow. The male is similar to the male of E. formosa.
Adults of both sexes reared on B. tabaci in the present research were smaller than the size reported by Gerling & Rivnay
(1984) from the same host.
E. cibcensis. The female is 0.57 + 0.01 mm and the colour pattern of this species in both female and male is completely different from the other three species. Body, antennae and legs bright yellow; eyes and ocelli red. Flagellum six-segmented with both funicle and club apparently three-segmented. Fore wing hyaline with a very distinctive setal pattern. All tarsi five-segmented.
The male differs from the female mainly in the structure of the antennae and the colour. The mean length of the body of 15 speoimens was 0.55 + 0.01 mm. Antennae, legs, head and body in ventral view yellow; pronotum, axillae and gaster in dorsal view dark brown (see
Appendix 1 for full details). - 97 -
E. adrianae. The adult female is approximately 0.7 mm long.
Mean length of 30 specimens was 0.66 + 0.01 mm. The head and thorax are bright brown to ochre, the abdomen is uniformly bright yellow to whitish, as long as the thorax with a conspicuous ovipositor which extends beyond the extremity of the body. The abdomen has a pair of tubercles on the posterior end on each side of the ovipositor, each bearing three hairs. The wings are hyaline covered with small hairs and the tips and posterior edges are fringed with long hairs. The antennae and legs are yellowish brown. The antennae are eight-jointed; the filiform flagellum consists of four funicular and two club segments. All tarsi are five-segmented.
The male is slightly shorter than the female (0.62 + 0.01 mm, n= 17). The whole body is dark brown to black, and antennae and legs are light brown. The wings are hyaline opalescent and covered with small hairs. The male is similar in colour pattern to males of E. deserti and E. formosa but can be distinguished by the number of segments in the mid tarsus, four in the latter species and five in E. adrianae. (see Appendix 1 for full details of morphology).
E. formosa is known to be uniparental bisexual, males occur but are rare (Gerling 1966a). A few males were observed by Speyer
(1927), who mentioned that they occurred after a cool period.
Burnett (pers. comm. cited in Gerling 1966a) suggested that males are produced when the parasitoid population reaches its peak of abundance. In the present work it was found that some males are produced when the population of the parasitoid is very high and the proportion of parasitism is also high. Gerling (1966a) conducted experiments verifying the theory that the males develop parasitically - 98 - on females. Copulation was never observed in this species.
E. ciboensis, E. adrianae and E. deserti are biparental heteronomus hyperparasitoid species. This was stated for the first two and corroborated for the last species during the present work.
When unparasitized third instar whitefly nymphs were exposed for 24 hours to virgin females, no progeny were produced, when the same experiment was conducted with mated females the progeny were only females. When previously parasitized whitefly nymphs were exposed to mated parasitoid females, both sexes were obtained in the progeny.
These observations were widely corroborated during life cycle experiments.
Contrary to E. fomosa, males were abundant in the stock cultures of E. deserti, E. cibeensis and E. adrianae and copulation was frequently observed in vials.
In samples taken from cultures it was found that in each generation females start to emerge approximately three days before males. The same observation was made on the initial field collected material from Pakistan and Israel.
It was also found that males of the biparental species (E. deserti, E. cibeensis and E. adrianae) develop on conspecific females as well as on females of the other species including E. formosa which allows these species to be classed as 'facultative autoparasitoids'. - 99 -
Developmental duration
Tables 9 and 10 detail the developmental duration of immature stages of both sexes of E. cibcensis and E. adrianae, Table 11 gives the developmental duration of the four species, from oviposition to pupation and to adult emergence. These results are shown in graphic form in Figure 13. In all cases males developed faster than females and E. cibcensis developed faster than the other three species, followed by E. deserti and E. adrianae. The developmental duration of E. formosa was longest, but not significantly different from that of E. adrianae.
Regarding a short developmental period as an important attribute of a good natural enemy, these results suggest that E. cibcensis is a promising species for control. of B. tabaci because of its short developmental period compared with other species in this work.
For E. formosa ovipositing in third instar nymphs of
Trialeurodes vaporariorum Nechols & Tauber (1977) report a developmental duration of 9.53 + 0.97 days from oviposition to pupation (egg + larva) and 17.04 + days from oviposition to adult emergence (total) at 25 + 2°C and 16: 8 L: D. The values obtained in present study were 9.75 + 0.05 days and 15.96 + 0.05 days.
Superparasitism
Percentages of parasitism and superparasitism were recorded from the sampling in the experiments on life history of E. cibeensis - 100 -
O N et to at lV M N of 1A of O OO OO OO OO OO OO OO OO OO OO OO L N OO OO O OO O Cl OO 41
Ix+1 +1+1 +1+1 +1+1 +1+1 +1 +1 +1+1 i O -T O1 N to .4 In In N üY 1, In Ö ^ N ÖÖ Ö . -i -i N -i N lV N OO OO OO OO OO OO
N
N C 0) OO in .+ 1. of in N. in 0 NN N NN OO OO O O -. O -. u Y d OO OO OO OO OO OO U ýN OO OO OO OO OO OO a +I +ý+1 +ý+1 +ý+1 +ý+1 ++ý +ý+1 a) Ix co in I- N. O In in in of ON at N pe ä Ln -: U) 1V C) LC U) in ÖO Öö ÖO Ö uu OO OÖ CD uir- 0 O C in n MO N in to O in O MO . N N N N et N N -4 . -r .r . -4 . -1 QJ I a U,N 0 Q1 ++ -W lV t[1 e'', in in N. in fS 1ý el' M N- 7 Co OO mN t en LO V in itf 1. in ro 4
aý o cl C! N. in %D V' OD M -. N of in in N +a J N O O ON ON 99 O .. W (D O OO OO OO OO OO O oO 1s _ ui +I N Ä * +I+I +1+1 +1+1 +1+I +1+1 +1+1 IX d t' it) lV OM to in O1 co . CO N. N 00 N .4 1L) O O! Ili in in 10 N U1 .+ 0! N -. at N in q1t in to 1. in .r 0% Cp ~ O O ++ in N in in M -Y N NO in f to IX 00 o NM M KA i r at 9O .+ C 7 N .ý .r -4 - .r -- OO M O 10 Q b ý-1 LV 7O C m Oý ýp O% M 1.- Oh .r nM .. r at Np CN M at .r K) - CO r+ in tP 1S {[1 N G
O CN N Lý M U. i U. Z U. 2 I. L. S U. X M gL rd' d i i C ýO 1 b O d +ý 41 W Oý N C N 40 C r C r Y b ro 7 4O v1 O i O. L i L N G! C4 0) t c I ä WJ 4- ýn a ro 0. a) N 41 - 101 -
N %0 MM tr 1- M of !hN -e 4r OO OO OO CD, O O OO tu OO OO OO cOO OO c OO = O jI OO O LI +I+I + G OO O N OO .O NN NN MN oO oO OO OO OO Oo
w
aý i N sf fh eY O CO M M N. N N. 4 40' 90 OO -I . -I O- .4 lV ýO OO 90 N G) OO OO OO 99 OO 99 to m #A OO OO OO OO OO OO L a +ý +1+ý +1+1 +1+1 +1+1 +ý+1 +1+1 40 NX M Co NN N CO t[) N. M N. UU to r1 M . -a "r tff N. M - N. N. N C N .r NN MM U) IL) In 4t IC) K) W OO ý0 OO OO OO OO OO
N C N O MO Co O N of In NO O U) Ol
U) N O L +1 et et to 44) Co %0 O" CO lV ON O 1L) 7 .+
i OO NM et a 40 %0 N. N. 0 N. C,C) H Nb q d 0) tO t i1 Cl O NM of eh O. M O at O to ON NN -i O !9O N 4J . -! -! - -! 0 O OO OO OO O CI OÖ 0O O d + 'O * +1+1 +ý+1 +1+1 +ý+ý +1+ý +1+ý C X O Co rO O et O'. IA to of N. N 47 N +1 V ON Oet c4 O4 at 03 NN lff . -+ "i 0) MN In M t0 1!! C'. N. C'. Co m t C 78gO N O O C ++ O Co .4N O'. of O' -+ %D N- N OS L X ON ON 00 N. N CO N OD MM r C ++ C Mf N N- N N NN OO %0 O b o- 00 00 C ^ b 0 Np N N CO U) C') f4 %0 03 1A ýd G r J-1q t1 C to O N y LL3: LL: E LLx LLx LLx LLm 6 O ýF CJ G L N i R1 L C m 43 O O 4+ Y N C N C C p Y Y a L 7 O i4 C ' O N iC Un O O. C d tm G CL )O r A C» (0 4- N i4 d W -i d2- Fý is - 102 -
Figure 13. Developmental duration of four species of Encarsia from eggs laid on third nymphal instar of Bemisia tabaci; numbers in bars are the number of observations. The hatched histograms show the mean duration of immature stages of both sexes of E. cibcensis and E. adrianae.
116ý - 103 -
16
938 63
14
58 455 i0 o a 12 a, 171
69 `0 10 Co n n CL CL a w 54 947 _ a CL a 6 ä I- z w 458 - o a 0 83 w 0
" 10 4 m - > " rn c
rn 2
Eformosa E. desert' E. cfbcensis ¬adrlanae - 104 -
Table 11. Developmental duration of four species of Encarsia, when ovipositing on third instar of Bemisia tabaci (Temp = 25 + 10C; R. H. = 75 + 5%; L: D = 16: 8)
Mean duration in days from ovipisition to
Species pupation adult emergence (egg + larva) (egg + larva + pupa) Sex n x + s. e. n x+ s. e.
E. formosa F 947 9.75 + 0.05 938 15.96 + 0.05a
E. deserti F 458 7.57 + 0.06 455 13.37 + 0.05b M 93 6.81 + 0.10 69 10.86 + 0.15b
E. cibeensis F 157 7.71 + 0.05 171 11.57 + 0.05c M 49 5.58 + 0.05 54+ 9.62 + 0.120
E. adrianae F 64 9.45 + 0.10 63 15.77 + 0.20a M 87 8.82 + 0.04 58 13.22 + 0.16a
Means followed by different letters are significantly different (P<0.01, LSD test, separate for sexes) - 105 - and E. adrianae, where the number of parasitoids and hosts per leaf were standarized as described in Section 3.2.1. The results are given in Table 12. They show higher percentages of parasitism by E. adrianae than E. cibcensis both as primary parasitoids (female) and hyperparasitoids (males).
Results also show that E. adrianae superparasitized secondary hosts (its own female larvae) more (31.00%) than primary hosts
(4.58%). A very low level of superparasitism by E. cibcensis was observed.
A maximum of three eggs of E. adrianae per host was recorded in primary hosts, whereas in secondary hosts up to eight eggs (male) were found in a single host. It was also found that those eggs have a normal embryonic development and first instar larvae hatched normally, but there was never more than one second or third instar larva found in a single host.
3.3 Effect of the host stage on parasitism and development of the
parasitoid species.
Doutt (1964) stated four phases in the process of parasitoid selection behaviour: (1) host habitat finding, (2) host finding, (3) host acceptance and (4) host suitability. The first two are regarded as steps in 'ecological selection' the third as 'psychological selection' and fourth as 'physiological selection'. He gives an account of each one of these sequential steps, which the parasitoids - 106 -
Table 12. Percentages of parasitism and superparasitism of Encarsia cibcensis and E. adrianae on Bemisia tabaci
(temp. = 25 + 1°C; R. H. = 75 +5%; L: D = 16: 8)
Species Sex % parasitism % superparasitism n x+s. e. x+s. e.
E. cibeensis F 30 29.83 + 2.50 0.17a b M 18 33.33 ± 6.05 ---
E. adrianae F 24 42.70 + 2.02 4.58 + 0.99 M 20 49.00 + 3.62 31.00 + 5.27 n number of samples a superparasitism was observed only on one sample b no superparasitism was observed - 107 - must overcome in order to use successfully a host resource.
Experiments in the present work were conducted investigating
host acceptance and host suitability by the four species of
parasitoids with the following objectives: (1) to determine which
nymphal stages of B. tabaci are accepted for oviposition and which
ones are suitable for larval development, pupation and adult
emergence by each one of the four parasitoid species and (2) to
determine the influence of the host stage in which oviposition occurs
on the developmental duration of the parasitoids.
3.3.1 Materials and methods
The experiments were conducted under the conditions already
described. The whitefly stages tested were: first instar (sessile),
second instar, third instar, fourth instar and pupa. Hosts of each
one of the five stages were exposed in leaf cages for 244 hours to a
mated female in the same way as described in the life cycle
experiments (section 3.2.1) the density of the host in each stage
varied from four to 128 individuals per leaf and there were six in functional replicates in each experiment (Data from experiments responses, section u. 1.2).
The following information was recorded from the experiments: 1.
number of hosts parasitized in each stage, as the number of hosts on
which pupation of the parasitoids took place, 2. number of days from
oviposition to pupation and to emergence of the adults.
Data on parasitism were analysed as a binomial distribution
(parasitized versus unparasitized hosts) by the analysis of deviance - 108 - by GLIM system (Royal Statistical Society 1977). Mean differences between host stages and parasitoid species were compared using the standard error of the differences in a t-test.
3.3.2 Results and discussion
Host acceptance and suitability
All the B. tabaci immature stages tested were successfully attacked by the four species of parasitoid. However the percentage of parasitism varied with the host stage exposed and the species of parasitoid as shown in Table 13 and Figure 14. The third instar had the highest percentage of parasitism, this was significantly different (P<0.01; t-test) from the other stages. There was no significant difference in percentage of parasitism between second and fourth nymphal instars, whereas the first instar was significantly different from them and from the pupal stage, the latter being the least parasitized. Further analysis of differences in parasitism among species are discussed on Chapter 4.
Egg development takes place in all five host stages tested.
Hatching occurs in second, third, fourth nymphal instars and pupal stage and larval development occurs in the same stages, but at different rates (see next Section). Pupation and adult emergence occur in the fourth nymphal instar and pupal stage of the host.
The results in this study differ from those of other workers working with E. formosa as a parasitoid of T. vaporariorum, who have stated - 109 -
w C N *49 u to v N N N.0 M r.0 - Oý N tt tD N - 1- 10 y N N f. co t. . -4 N +1 +1 +1 +1 +1 +1 C Ix I, V M %C N d N N. -4 M M S. G! CO YY N 00 - V- N N M N N W "
C) N N G w N O tý C C C to U IC m In U, 00 10 N CO A ap i O Oý OD N Oý } O
N ýp i0 ý-+ t0 . u9 N N O LN N M at M - N V IC d Up WI O C M Wp C V- J OJ O I. r 0) . N 0 m 4- C ie2 e0 ie to 12 .+ .4- C) N O N OO +1 U of M N rý N +1 c+W G' V N 1n CO 7y N N - CO r 4., C ib Co Wý - b V T U T r (3 C a1 i+ U .O V L U .0 A R! U M T Eo U .. 4 to Pof CO to N M 01 f+f In OO N }I d N C M 1ý N O. '0 C% I. - +1 b b W - L LN N GJ aM b G/ O r on IO rl E N Nd o a Ie a a U i. E O to N M N w Cv L lb O R N N + L a O V- M O CO et Oý 1-. N V- N et of et 10 N W- 4d T u W1 mv Lb M u N +ý n G go NC N CN L 6! L 'O N L # E r L r0 L IO # X0
61 ib 14 41 UI C) G N C N C I 0 N U C r C r N ww p1 r r 0 M N A 41 v s41 +1 CC -41ýn N O L L 1O IX 10 to L 1.) 7 C. NW C) .43 r U L O 7 6E I N V.. 0 14 4- d a O M F- S 41 41 - 110 -
wI m m ý co U2 X:
P44 00 110 4
4) m yO C) O Ob 4) L w 4-3 9) 'O L 4)) 0 ýtl aý +0"i Wý i0. Am V-3 m 9bm0 C co m m 3 ca Ü . 04 2 p, U C. OV wl +' ý v 03 43 LO 01 s C13 ý, 'OC 4) . r- w - 111 -
at ob o0 in 0 of ý P1 N
0to n
L d
m
W. ýy 0 w PN co
N
2
a
W 0
ti {ý { ti" '} '''ý" ý{ x " ' H :. 1L" 7: ' .' 1 }1 "L ® 0
C N
0)
xee Ne
03Z I. ISVHVd ISOH JO 3DViN33U3d - 112 - that only some the immature stages of the whitefly are parasitized
(Speyer 1927, Burnett 1964, Gerling 1966a), or that only some stages could be successfully parasitized. Gould et al. (1975) stated that only third instar whiteflies could be successfully attacked by E. formosa, while Nell et al. (1976) stated that when first and second nymphal instars are parasitized, host and parasitoid die prematurely, and when eggs are laid in pupae, parasitoids are not produced and whitefly adults emerge from such pupae. But findings in this work are in accordance with those of Nechols & Tauber (1977a) who found that all stages including first instar and pharate adult (late pupa stage) were accepted for oviposition (susceptible) and parasitoid adults were obtained from eggs laid in all stages.
In conclusion, in this investigation parasitism of all four species of parasitoids in the five stages of B. tabaci tested resulted ultimately in the completion of the parasitoid's life cycle.
Encarsia spp. are koinobiont parasitoids, since for the four species of parasitod studied, the whitefly nymph continued its development after being parasitized irrespective of the instar in which parasitism took place.
Effect of host stage on parasitoid development
Tables 14 to 17 and Figure 15 show the developmental duration of females of the four species of parasitoids, when eggs are laid in five different host stages. Duration from egg deposition to pupation - 113 -
(egg + larva) and to adult emergence (total) as well as for pupal stage are given.
For the four species these results show that the rate of development increased as eggs were laid in later stages and significant differences were found for each species (Tables 14-17).
Developmental duration of egg + larva was significantly faster when eggs were laid in third and fourth nymphal instars and pupal stage than when laid in first and second instars. Similar differences were found in the total duration of the developmental period (life cycle).
However the duration of the pupal stage remains more or less constant for each species.
These differences in the rate of development of females from eggs laid in different host stages could contribute in explaining the sex allocation strategy of these 'heteronomus hyperparasitoid' species, since, if the female has the choice of laying eggs in different host stages in the same patch, which could be possible under field conditions, the later developing females (from eggs laid in earlier host stages) can be used as secondary hosts by the faster ones for laying male eggs.
On the other hand a comparision of the total developmental duration of the four species of parasitoids from eggs laid in the five different host stages (Table 18) shows that there are significant differences (P<0.01) in the developmental duration among species, being shortest in E. eibeensis and longest in E. adrianae and E. formosa. As already discussed, the shorter developmental period of E. cibcensis suggests this species could be a promising natural enemy for control of B. tabaci. - 114 -
Table 14. Developmental duration of Encarsia formosa females, from eggs laid in different host stages (Temp = 25 ± 1°C; R. H. = 75 + 5%; L: D = 16: 8)
Mean duration (days) egg + larva pupa adult emergence Stage exposed to parasitoid n x+ s. e. R n z+ s. e.
first instar 217 13.50 + 0.07a 5.75 183 19.28 + 0.09a
second instar 286 11.86 + 0.10b 5.03 270 16.89 + 0.11b
third instar 306 9.38 + 0.080 6.20 284 15.58 + 0.07o
fourth instar 293 9.54 + 0.12c 5.94 254 15.48 + 0.12c
pupa 65 9.37 + 0.13c 6.04 57 15.77 + 0.17c
Means in columns followed by different letters are significantly different (P<0.01, LSD test)
Table 15. Developmental duration of Encarsia deserti females, from eggs laid in different host stages (Temp = 25 + 1°C; R. H. = 75 + 5%; L: D : 16: 8)
Mean duration (days) egg + larva pupa adult emergence Stage exposed to parasitoid n x + s. e. X n x + s. e.
first instar 126 10.11 + 0.17a 5.44 76 15.55 + 0.15a
second instar 130 10.10 + 0.11a 2.42 112 12.52 + 0.17be
third instar 197 7.37 + 0.07b 5.59 147 12.96 + 0.13b
fourth instar 172 7.22 + 0.13bo 5.08 128 12.30 + 0.13c
pupa 114 7.04 + 0.040 5.05 81 12.09 + 0.08o
Means in columns followed by different letters are significantly different (P<0.01, LSD test) - 115 -
Table 16. Developmental duration of Encarsia cibcensis females, from eggs laid in different host stages ( Temp. = 25 + 1OC; R. H. = 75 + 5%; L: D = 16: 8)
Mean duration (days) egg + larva pupa adul t emergence Stage exposed to parasitoid n x + s. e. R n x + s. e.
first instar 112 10.82 + 0.15a 3.77 108 14.56 + 0.18a
second instar 106 8.04 + 0.11b 4.01 101 12.05 + 0.16b
third instar 128 7.54 + 0.09c 3.69 127 11.23 + 0.100
fourth instar 130 7.14 + 0.06d 3.88 128 11.02 + 0.090
pupa 87 6.80 + 0.13e 3.28 75 10.08 + 0.16d
Means in columns followed by different letters are significantly different (P<0.01, LSD test)
Table 17. Developmental duration of Encarsia adrianae females, from eggs laid in different host stages (Temp. = 25 ± 1OC; R. H. : 75 + 5%; L: D = 16: 8)
Mean duration (days) egg + larva pupa adu lt emergence Stage exposed to parasitoid n x + s. e. X n x + s. e.
first instar 201 14.09 + 0.14a 5.27 181 19.36 + 0.19a
second instar 270 11.18 + 0.11b 7.16 249 18.34 + 0.22b
third instar 322 9.20 + 0.06o 7.12 311 16.32 + 0.120
fourth instar 215 8.44 + 0.14d 6.44 200 14.88 + 0.16d
pupa 79 8.23 + 0.21d 6.66 77 14.83 ± 0.19d
Means in columns followed by different letters are significantly different (P<0.01, LSD test) - 116 -
a) to 4, +4 o 4) o
o ö
4.1 b tu 9) 12) f- to »a :j tu g.
ý fl' yo tti aQ 4) Ei a 4'
4) a) oý 4) o
ö
+' o0 U) w oö U) .cy 4) °) mg) 4 4) IciU) ai U) 4" s) 10 o30 Ü 0)
A-4 ö `)
cri
hL - 117 -
Nrýrýr
° a
M p b 4 N C C C N N ri C
V T p C wi N N N
ednd N enJeI +BBe
rý a a + e C 4 C uII ü
V Wý ö e C O e W
V ednd eAJeI + BBa Q F-
Q
w W aä 4 a F-
O N « H N äZ
of O 9O WI 2 Q N rf C N
O BBa ednd enjeI + b N Q K Q a O ^ b ý n 10 7 6
m e t N N f OI h O b V O b e E N 19 ol uil N N
ednd ^ eAJel + BBe ä
O tl IC ONO tl pN Nrrw. rr (SAVO) 3 WI1 1 N3 WdO13A3O - 118 -
3.4 Adult longevity
Flanders (1950) used the chronological relation between the
maturation of the egg and its deposition for grouping the species of
parasitoid Hymenoptera in two categories: (1) Pro-ovigenic species in
which egg maturation is completed before oviposition begins, and the
ripe eggs stored in either the ovary or the oviducts, this could
happen before parasitoid emergence, so that females emerge with
their full complement I of mature or nearly mature eggs which they
deposit usually within a few days after emergence. Such females are
short-lived and feed little if at all. (2) Synovigenic species in
which females emerge with few or no mature eggs, and the oogenesis process is not completed before oviposition begins but is more or
less continuous throughout the life of the female. The females of
those species are long-lived, and oogenesis depends upon female
feeding. Thus, the life time fecundity or 'functional longevity' of a parasitoid will depend upon its longevity and the kind of food it can obtain for survival and production of eggs. Further, in the
absence of food resources, many parasitoids can resorb eggs, thereby trading fecundity for longevity (Waage & Hassell 1982).
It has been also suggested (Jones 1986) that the shorter life span of ovipositing females is due to a considerable amount of their energy reserves being apportioned to actual host location and oviposition.
Encarsia spp. fall into the synovigenic category, so differences in adult longevity among species might make differences - 119 -
se v r
b i0 ýO A i0 ^ +1 01 N N MD 01 G! .r N ý.r .r Ln .r to d Q G O O O O O N ro 'A E L +I +I +I +I +I +I .J 0 C to -r co M N L= 'O IX M M M co co N W dd ag: NO Cl r N J LV A U ""ý N C O W+ O w a u U v c V Ln Co lp O 0% b ON H U . -ý .+ r+ Cl .4 a C N d UI O O O O O 11 CIO u r C u +I +I +I +I +I +I a) wa U Ix to 11l M N CO GL E LO O N O Cl d NN 14., WI if N .ý º+ O N. Lv N - - N N V Or 41" 31 u 4. 'e oa C A r0 U U V C4 U .0 0 ßf1 1. M M co rb Y bN L. N O O O O 0 C Lr W OI I- + + + +I +I + N Ix 1Lf N ýO O 0% ^ co U! ref Oý eý'f O E) A I. 4J V- WI !n N N N N 'O Co . -ý "-a H .ý rr d N EN 6d W O 4' N I- yN ro .0 a N RI O1 0% fý N 1, 4' ro U O O O - - C N W Ay O N O O O O O E W OO +I +I +I +I +I +I w O V- '4- IX co as co co 1. ' Ww N 1O to at fý Or WI O4 %0 K1 u uA C co .O 0 "" N "C r> na C) Lr i0 y 11 O G I EcO 0 O V 'r' J L {. W L of L . vO 4o ++ ro ++ N 41 VI 41 N N C N C O U C T C T ý T T i0 C t C
N N O L L 10 L U 7 G N d 41 T U .C O 7 C a N M. N i+ V- G .o O N F- S z - 120 - in the life time fecundity and ultimately in the capacity of the species for controlling the host.
The adult longevity of E. formosa, E. deserti, E. cibcensis and
E. adrianae was studied for females as well as males of the biparental species, for wasps kept without host contact. Information on adult longevity of ovipositing females of E. formosa and E. adrianae was obtained from experiments on fecundity.
3. u. 1 Materials and methods
Adults were obtained from stock cultures as described in the life history and morphology studies.
Wasps were kept in cylindrical glass vials (55 x 25 mm) closed with a plastic cap in which a small hole (5 mm diameter) was bored.
They were fed with very tiny droplets of honey which was smeared on
the walls of the tube through the hole in the cap, with a dissecting needle, every other day; the hole in the cap was plugged with a small cork.
Mortality was recorded daily from the first day until last wasp
in the vial died. Six replicates, with a different number of wasps in each one, were laid out for each species and sex.
Wasps killed by sticking on the honey droplets were not counted for the analysis. - 121 -
The method of keeping wasps with host is described in fecundity experiments (Section 3.6.1)
One experiment was conducted to find out how long the wasps survive without food; 300 female wasps (3 replicates) of each species were kept in glass vials as described above, but without any food.
Data were analyzed by the analysis of variance and least significant difference for means separation.
3.2 Results and discussion
The results of the longevity studies which are given in Table
19 and represented as survivorship curves in Figure 16 show that longevity of E. cibeensis females (17.41 days) was considerably shorter than the longevity of the other species. E. adrianae was the
longest lived species (23.5 days). There were no significant differences in longevity between E. formosa and E. deserti.
In all cases males lived a shorter time than females of their own species and significant differences were found in the adult
longevity of males between species (Table 19).
The results also show that females of species that were allowed
to feed and oviposit on hosts lived a considerably shorter time than
females kept without host contact. Similar results were found by Vet
& van Lenteren (1981) for females of E. formosa, E. pergandiella
and Encarsia sp. near meritoria Gahan feeding and ovipositing on - 122 -
T. vaporariorum at temperatures below 20°C, but the contrary is reported by van Lenteren et al. (1987). They found that E. formosa lives longer when it is able to parasitize than when it is isolated on artifical diets throughout its life span at 200C and they concluded that the differences in their findings are due to temperature differences. However findings in the present work (at
250C) disagree with that conclusion.
Most of the wasps kept without food died within 24 hours of the beginning of the experiment (E. formosa 90%, E. deserti 64%,. K. cibcensis 94% and E. adrianae 80%) and all of them within 48 hours.
The extremely short life span (24 h) of females kept without any food and the differences in longevity between females kept without oviposition opportunities and ovipositing females, suggest that few energy reserves can be traded from fecundity to longevity and a considerable amount of energy reserve is spent in the process of host searching and ovipositing, in the studied species.
Taking into account differences in longevity between species,
E. adrianae has an advantage over the other three species, and E. cibeensis is at considerable disadvantage, as good biological control agents.
3.5 Oviposition, mating and feeding behaviour
Oviposition and feeding behaviour as well as other behavioural aspects have been studied in detail for E. formosa on T. - 123 -
Table 19. Adult longevity. of four species of Encarsia kept in vials and fed with honey (Temp. = 25 + 1°C; R. H. = 75 + 5%; L: D = 16: 8)
Species Sex No. of x + s. e. range wasps (days) (days)
E. formosa F 216 21.62 + 0.34b 7- 34 Ft 7 18.71 + 2.63 12 - 32 E. deserti F 185 22.64 + 0.39b 11 - 37 M 106 18.32 + 0.29a 5- 24
E. eibeensis F 121 17.41 + 0.42o 7- 26 M 73 9.25 + 0.33c 3- 15 E. adrianae F 166 23.50 + 0.35a 14 - 32 M 117 17.05 + 0.35b 7- 23 F' 9 15.22 + 1.13 9- 21
Means followed by different letters are significantly different (P<0.01; LSD test, separate for sexes) * wasps kept with host (ovipositing females) - 124 -
w1 X:
'V co
U 4) U m 0 W 4) 0 i, Q) 93 U 4) Q,
c0 ei Og a) aý 0,
43 . -1 m 2 4-4 0 m a m d1 0 w ri a; co
c2
ýo I - 125 -
mi 11 0 o" ID I)
mi o 8i O+ O+'b O+'b O+' D ! '7 .y NC O E U N O_ . 'OW UN WI wl WI WI
o
N
(0
O3 N
W `' U dam' JA-- 0; Z .Ö , - W 0 cc 0 w 2 W 1001* Q W F- LL N cr ' - 1/ W / / 2 i'i d '- I-
0
i
qp
C2 o ao erv öööÖö
ONIAIAdfS NOIlHOdOUd - 126 -
vaporariorum. Van Lenteren, Nell & Sevenster (1980) using a digital
tape-recorder specially developed for this kind of study, constructed
a series of detailed diagrams and stated a sequence of behavioural
components. Gerling & Foltyn (1987) conducted studies on oviposition
behaviour of E. lutea on B. tabaci. Through direct observation they
found a series of behavioural components similar to those described by van Lentern, Nell & Sevenster (1980).
A comparative study of some aspects of mating, oviposition, and feeding behaviour sequences was worked out for the four species of
parasitoid, in order to get information that could contribute to clarifying differences in the parasitoids' efficiency.
3.5.1 Materials and methods
All experiments were conducted at 25 + 10C by direct and continuous observations under stereomicroscope and time was measured with a stop watch. Young females (24-48 h old) were used in the
They experiments. were kept for 24 hours in glass vials with males
(biparental species) in order to assure copulation before the oviposition experiments. The hosts used were third and fourth instar
B. tabaci nymphs of for primary parasitism and female mature larvae and pupae of their own species or in some cases different species, for hyperparasitism (male eggs).
The arena for these experiments consisted of a small Petri dish (35 mm diameter). A hole (10 mm diameter) was out in the lid and covered with polyester mesh, to allow ventilation and avoid - 127 - condensation during the time of the experiment. The bottom of the
Petri dish was lined with a disc of filter paper. A disc of bean leaf, 30 mm diameter with hosts in the appropiate stage, was cut and set in the Petri dish. The host density was fixed at 30 individuals per disc. One female was released into the dish and the whole unit taken to the stereomicroscope for observation.
The movements of the wasp were followed and each time it adopted an oviposition posture on the host the time was registered and the position of the host marked on a map of the leaf disc. All marked hosts were dissected after the observation and checked whether oviposition had occurred or not. When no egg was found the time of that observation was not taken in account for calculation of ovipositing time.
Some preliminary observations with E. formosa showed that a batch of eggs is laid during the first hour of contact of the wasp with a host patch and after that oviposition activity declines considerably. One wasp laid ten eggs during the first hour and only two during the next hour so experiments for oviposition of female eggs were limited to one hour's duration.
For observation on courtship and mating behaviour, young wasps
(24-48 h old) were confined in couples or small groups of both sexes in small glass tubes with droplets of honey on the walls. Duration of the componets was recorded on at least ten observations. - 128 -
3.5.2 Results and discussion
Oviposition behaviour
The behavioural components and its sequence on parasitism
(oviposition) of females of the four species of parasitoids were
similar to those described for E. formosa (van Lenteren et al. 1976a,
1976b, van Lenteren, Nell & Sevenster 1980, Nell et al. 1976) and for
E. lutea by Gerling & Foltyn (1987). They include antennal drumming
while walking, standing still, encountering the host, examining the
host by drumming and walking on it, adopting an oviposition posture
(Figure 17), preening and host feeding. This suggests a similar
general pattern of these behavioural components and similar sequence
for the species of this genus. However some differences were found mainly in the time invested in the different activities.
Ovipositing female eggs
Results of number of contacts of the wasp with new hosts, number of eggs deposited and mean time spent ovipositing, are given
in Table 20. They show that there is little difference in the mean
time spent by the different species in depositing one female egg (4-5
min), but the mean number of eggs deposited during the first hour of
the wasp's time in a host patch varied from 3.3 eggs by E. cibcensis
to 7.7 eggs by E. formosa.
Regarding the number of hosts thrust with the ovipositor, the
four species showed that in at least one of each five of those
contacts no egg was laid, neither was host-feeding observed. - 129 -
**F-+iý- - ab * -, -
ý __
n: ^a, 4% . -"- ---- ý'-. ýý ,, fS
^ýr
Noe
Figure 17. Encarsia adrianae; female in oviposition posture on a third nymphal
instar of Bemisia tabaci. - 130 -
A comparison of the proportion of the first hour spent per species in real oviposition activity in a host patch is given in
Figure 18, and shows that E. formosa invests 59.6% of its first hour in the host patch in ovipositing activity whereas E. ciboensis invests only 22.9%; this is about half of the time invested by the other species in the same activity.
Superparasitism while depositing females eggs was recorded in all four species during these experiments, but at a very low level; one E. formosa superparasitized on two occasions, two eggs in one host and three in other (Figure 19); two E. deserti superparasitized once each; one E. cibeensis superparasitized once; and one E. adrianae superparasitized three different hosts.
Ovipositing male eggs
Results of these experiments are given in Table 21. They show that for the three biparental species tested, the time spent depositing male eggs in a female larva (about 6 min) is much less than the time spent ovipositing in a female pupa (16-20 min); whereas the former is little more than the time spent depositing female eggs
(4-5 min, Table 20). These differences can be explained by the physical resistance of the host's covers that have to be bored by the ovipositor of the wasp in order to deposit the egg. When a female egg is deposited, only the soft cuticle of the whitefly nymph has to be bored; when a male egg is deposited in a female larva, two covers have to be bored, first the whitefly cuticle, which could be dry but not very hard, and then the skin of the female larva, which is soft; - 131
a 0 4 N 1_ O -t O a} Co N Co cm to at %0 a . -1 b O O O O O L .r O A d 10 +ý tI +ý +ý +ý +I to 1. %D O 1ý 4Y In d L. -: IA th l0 W lY t M .: b et %0 to 1A M I- UY W O WI
L 7 N to N O at %O M t
d. ) N L
w t-, t0 Oh t0 rl d
O . -ý .r M O N M N
L O O O O O +ý +ý +ý +ý I +ý V fý Kf Co O% Co O" 1" In p 1 1[! u Y 1 V 1 M In R Q c .o W
0 M Co M N O ý-a to in 1 T M E ao
m ýo
a 'r N TN ý OI to 1 cr 'V O
NJ L A UN 1, P. CO O CO M N N M N N c In W O O O O O p Y- O Mf d M N CO 1ý N M N O In dN d p M of M at u i NI CL N Ld 7 yN 01 00 1A LL"! 1[f N Q! t0 00 O.c ++7
C > +ý oE CN Co 1ý LL'J !h {p NN 41 a -r C1 N Nv W O CL o) wn r p) E > cu r; 1l N N Ln lp .. y Q O a v M 1ý 1ý c0 N E 4J lA C V A IS O O O O O cm r- CC v Nr O ++ N at l0 Co O r. O% 10 O N 10 UY CQ lt cp AN O 'd at eT 10 +) O r 4) et t0 M et C0G N ON T0 E NZ i u do O - rý 10 T 10 Ny GA 1[f O ++ E X. C N ob _ O cm Or WI dJ LN
W) 4 Ch Ob O Co ule M O" OON
LL CD VI N mm +I N EE C Ix CL CC- a ý^ ý"ý NM et Lfl to b a ýe oE H 3z amu - 132 - and finally when a male egg is deposited in a female pupa, three covers have to be bored, two dry and very hard which are the whitefly cuticle (exuvium) and the female's pupal cocoon, and finally the pupa skin (see morphological description of the pupa, Section 3.2.2).
These results suggest that females should prefer the female larva to the pupa for deposition of male eggs. No further studies were conducted in this area in the present work. However they are needed not only for these species but for the whole genus Encarsia.
Some observations were made on hyperparasitism by E. formosa females released in an arena with E. adrianae pupae as hosts. The wasps spent long periods on the hosts in ovipositing posture (8-30 min) but after that they fed on the host fluids and no eggs were found.
Courtship and mating behaviour
Viggianni & Battaglia (1983) reviewed the facts on courtship and mating behaviour in Aphelinidae and stated that there is remarkable variation in the phases of sexual behaviour among species, going from one simple pattern exhibited by species such as Encarsia pergandiella, which includes antennal contact, mounting, copulation and dismounting, to a complex pattern including antennal contact, mounting, postmounting antennation, copulation, dismounting, remounting, postcopulatory courtship and final dismounting. The latter pattern has been observed in Enearsia asterobemisiae Viggiani
& Mazzone, which shows a very particular postcopulatory courtship lasting 25 - 30 min (Viggiani 1984). s
i I - 133
0ä yý
'0 bo (a
WI c
CO E09Ö ,44.3 4ý L. b0
44 4.3 H
0^ F3 4)
C U
C n' N V1 49 N 4) W , -1
8 M4 9) 4) 4-3 U) °ý 00 LL U -4 .0 m 1) s. - 134 -
0) Ol 0 4) L L 'ýfi W N 0 N N L -0 0 wi WI ,
Co
i.
I- O da +"00 Z
(1) N N 0 N N 0 C E N L U 0 (- .0. r4 (0 U
In WI wi r-.
N - 135 -
i
1
#sIiI
Figure 19. Encarsia formosa superparasitism; three eggs (a, b, e, ) in a fourth
nymphal instar of Bemisia tabaci. - 136 -
0 cd 8 bO " M C.- .ým N Ln co vo O N mo oa cV +1 +1 +I a ++ c 9) 8 f d J1 M ti 4S. %.0 mý 'o ö «t N c ap ca e WI o ti m
C) v (D ca cd 02 Co M m ý ýD lfl ,i 92 0 '- m Go 0 N N t. u Go +1 +1 +I o +4 a)a a) 154 0 to .,. l ä U ON Ul 0 +J.c Lr - U 1 wl o; Z In WI l 4) 0. Q M L. In r r a) Q. t- 02 a0u va x «1 ..a m m cd cý O M s. > G) a0 .ý t) «1 O 03 0 M ýý- -4 +1 +1 +1 O S. ik Ln "- .0 Co9 aý Ln m mm LC a co 4N a) ýc 0 Q) II aa wl Co 92 0. aim -ýo IIn A3 0
f«, cd OO Cd WI cd ° ` ä. ac 02 . - 137 -
Different patterns of courtship and mating behaviour were
exhibited by the four species studied in the present work, and were
as follows:
E. formosa showed no mating behaviour at all. Despite females
being confined with males in couples and small groups and observed
for long periods (up to 3 h), neither females nor males took any
interest at all in copulation.
E. deserti showed the simplest sequence of events in the mating
patterns of the three species, including encountering the mate by
antennal contact, mounting, postmount antennation, copulation,
dismounting. The whole process takes an average time of 11 see. No
regular and persistent antennal contact prior to mounting was
observed in this species. Copulation was observed as soon as the
wasps found each other and after a very brief postmount antennation.
When several males find a female, there is a contest among them
crowding on the top of the female trying to copulate without any
previous antennal contact, that contest lasts until one of them
succeeds, then they all disperse.
E. cibcensis. This species exhibited the most complex mating
pattern of the three biparental species, including encounter by antennal contact, premount antennation, mounting, postmount antennation, copulation, dismounting.
The premount antennation seems to be an important phase in the
precopulatory courtship of this species, as no copulation take place - 138 -
before it. It consists of a relatively long lasting antennal
contact, during which the male rubs the inner side of its third
funicular segment against the outer side of the female's antennal
club. The inner side of the third funicular segment of the male
antenna is a particularly sensitive area covered by set of papillary
sensilla (see Appendix 1 Figure 17). This phase lasts 45 see on
average after which the male mounts the female and a very short
antennation takes place before copulation which lasts on average 9
sec.
E. adrianae. The courtship and mating behaviour of this species
includes encounter by antennal contact, mounting, postmount
antennation, copulation and dismounting. The postmount antennation
resembles very much the phase decribed by Viggiani (1984) for E.
asterobemisiae. The male mounts on the cephalic region of the female
and rubs the apex of the female's antennae with its antennal clubs,
then a full contact of the antennae with an intense rubbing takes
place, which lasts on average 18 sec, followed by the proper
copulation which takes about 15 see.
As suggested by Viggiani (1984) a detailed study of the
courtship and mating patterns can provide parameters for
"discrimination of sibling species and for a sound grouping of allied
species". In fact it was useful during the present work for discrimination between E. formosa and E. deserti.
Feeding behaviour
Adults of parasitic Hymenoptera feed on different sources of - 139 - carbohydrate and proteins such as honeydew, plant fluids, host body fluids (Rosen & DeBach 1979, Bartlett 1964).
The habit of some aphelinids of feeding on the host fluids, inflicting a wound in the host body, has been regarded as a predatory habit that in some species can be a factor of host mortality that affects the host population to the same or even greater degree than the parasitism itself (Viggiani 1984).
A detailed account of the host feeding behaviour of E. formosa is given by van Lenteren, Nell & Sevenster (1980). They were able to distinguish host feeding behaviour from oviposition behaviour at an early stage by the type and duration of the movements of the abdomen when the wasp inserts its ovipositor in the host.
All the four species of parasitoid studied here, fed on bee's honey, honeydew from whitefly and host body fluids.
The host feeding behaviour was observed during the experiments on oviposition behaviour of the four parasitoid species.
E. formosa showed a very regular host feeding habit. As stated above, the wasps used in these experiments were kept for 24-48 hours after emergence, feeding on honey; when those wasps were confined with hosts (third and fourth instar nymphs) they started to oviposit and did not feed until they had parasitized seven or eight hosts
(about one hour). This habit was observed very regularly in E. formosa. Whereas when E. formosa adults were confined with larvae or pupae of E. adrianae they fed on all the hosts into which they -14o- inserted the ovipositor.
The other species, E. deserti, E. cibeensis and E. adrianae, showed a very erratic behaviour in the host feeding frequency; some wasps started host feeding on the first host they contacted within the first five minutes of confinement and fed on different hosts during the first hour, whereas others spent long periods of time without any host feeding.
However the sequence of events during the host feeding phase was similar for the four species including 'encountering the host',
'drumming on the host', 'turning 18001, 'adopting oviposition posture', 'piercing the host skin', 'turning to search for the hole', and 'feeding' on the fluids oozing from the wound. Those hosts may be used for host-feeding by the same wasp or a conspecific during several short periods (20 sec) or a relatively long one which can take up to 15 minutes until the host is nearly empty.
3.6 Fecundity
Number of ovarioles, number of eggs, oogenesis and oviposition
As mentioned in the review of literature of the present
Chapter, several studies have been conducted regarding oogenesis, oviposition, dynamic, genetic and enviromental factors influencing body size, number of ovarioles and fecundity of E. formosa as a parasitoid of T. vaporariorum. - 141 -
Some experiments were worked out in order to compare some characteristics of fecundity, number of ovarioles and oogenesis of the four species studied.
3.6.1 Materials and methods
Stock cultures and environmental conditions were as described for previous experiments.
Number of ovarioles and mature eggs
The experiment was initiated with a large number (about 300) of wasps of each species maintained without oviposition opportunities in glass vials, fed with honey from emergence. Batches of 30 wasps of each group were removed and dissected at 1,2,5,10 and 20 day
intervals after emergence. The numbers of eggs as well as the numbers of ovarioles were counted. All full size eggs (see morphology section) were assumed to be mature. A batch of 30 wasps of each species taken directly from cages of the stock culture, as well as a batch of E. formosa emerged from T. vaporariorum, were examined.
Number of hosts parasitized
One experiment was conducted with E. formosa and E. adrianae, giving the wasps the opportunity to oviposit during the whole life span. They were kept from emergence to death in continuous contact with suitable hosts. - 142 -
The experiment was initiated with 15 wasps of each of the two species selected. They were maintained in leaf cages on bean plants with enough third instar nymphs of B. tabaci and transferred into new arenas (on new plants) every three days. The parasitized hosts (in each arena) were counted after eight to 12 days, when all parasitoids were in prepupa or pupa stage. When leaves dropped before the end of the register period, they were put in a leaf cage of which the bottom was covered with a wet foam pad (spontex) and kept in that way. Only those data from wasps that were observed until natural death were taken into account for analysis. Partial data from wasps that died prematurely (by accident i. e. sticking on honeydew) or disappeared during the experiment, were excluded.
Oogenesis and oviposition
The rates of oogenesis and egg deposition were studied in E. cibeensis and E. adrianae. Young mated female wasps were used in this experiment. Groups of five wasps were kept in leaf cages with abundant third and fourth instar nymphs of B. tabaci on bean plants.
These groups were removed and dissected at 0,1,2,4,6 and 8 hour intervals. The numbers of mature eggs in ovarioles were counted, also the number of parasitized hosts was determined by counting parasitoid pupae, eight to 12 days later. Each group had three replicates, so that, 15 wasps per species were dissected at each interval.
A second experiment was conducted with E. adrianae. Groups of ten wasps were kept in the same way as described above; they were - 143 -
48 removed and dissected at 0,1,2,4,8,12,24 and hours intervals. Each group had three replicates.
3.6.2 Results and discussion
Number of ovarioles and mature eggs
Van Vianen & van Lenteren (1982,1986) disagree with Copland's
Encarsia, (1976) conclusion, based on a few dissected specimens of
Aphelinidae Aphelinus and Coccophagus, that "probably all species of
have ovaries comprising three ovarioles". They found a variable
number of ovarioles in E. formosa and demonstrated a positive
correlation between body size (width of the head) and number of
ovarioles.
Results of this work in Table 22 show a variation of number of
ovarioles in E. formosa (Figure 20a) from six to 17, a small
variation in E. deserti from six to eight, and all the specimens of (Figure E. cibeensis and E. adrianae had invariably six ovarioles
20b). Furthermore, there was a significant difference between number
B. of ovarioles of E. formosa reared on T. vaporariorum and reared on is tabaci, as shown in Figure 21. It is assumed that this difference
due to differences in body size of the wasps, which at the same time
is a result of differences in host body size.
Numbers of mature eggs of wasps kept without oviposition
(not opportunities (Table 23) showed that there is a small increase
two days significant) in the number of eggs per wasp during the first - 144 - of isolation, and that number stays more or less constant until the fifth day in the four species, and until the tenth day in E. deserti and E. adrianae. After that period a gradual decrease in the number of mature eggs takes place, as shown in Figure 22. Resorption of eggs was observed in the four parasitoid species and some eggs appeared partially resorbed during the time that the wasps were kept isolated. Figure 22 also shows a considerable difference in the initial number of eggs in ovaries between E. formosa and the other three species. After 20 days of isolation resorption was almost complete in the four species and the mean number of eggs per wasp was close to zero.
Analysis of the number of mature eggs in wasps from culture cages compared to isolated wasps (same species) showed a significant difference between means, except for E. Formosa (see Table 23 and bars in Figure 22). This suggests a possible increase in the rate of oogenesis in wasps that have been in contact with hosts for some time.
Number of hosts parasitized
Data from seven E. formosa and nine E. adrianae were obtained in this experiment. The longevity of these wasps is given in Table
19. During its whole life span E. formosa parasitized an average of
141.28 hosts (range 47-257) whereas E. adrianae parasitized an average of 70.88 hosts (9-153). These results suggest that the former species has almost twice as much real fecundity as the latter.
Nevertheless more experiments are needed on this aspect to produce more reliable information, mainly for the new species. Life and fertility tables were constructed with data of these experiments and rates of growth of the population were calculated (see Section 3.8) - 145 -
Table 22. Mean number of ovarioles of Encarsia Formosa, E. deserti, E. cibeensis and E. adrianae in females reared on Bemisia tabaci (Temp. = 25+1°C; R. H. = 75 + 5%; L: D = 16: 8)
Species Host n Mean + s. e. Range
E. formosa T. vaporariorum k0* 13.05 + 0.27 10 - 17 B. tabaci 210 8.50 + 0.07 6- 14
E. deserti B. tabaci 210 6.11 + 0.03 6-8
E. ciboensis B. tabaci 210 6
6 E. adrianae B. tabaci 210 ----
n= number of females examined * batch of females emerged from Trialeurodes vaporariorum - 146 -
tj
i
i
5
Figure 20. Ovaries; a, Enearsia Formosa, notice the different number of in (5: 7); b, E. ovarioles each ovary - cibeensis, all examined specimens had six ovarioles (3: 3).
bý - 147 -
ý. ti. . -d
VAb .l1
a
J
"
0,
b
ýýý YI ýý
. `ý 1 .ý- - 148 -
160
155 on B. tabaci ® on L vaoorariorurn 150
145 U) a co 140
30 LL 0
25 w m M 20 z 15
10
5
n
6789 10 11 12 13 14 15 16 17
NUMBER OF OVARIOLES
Figure 21. Encarsia formosa number of ovarioles; wasps reared on Trialeurodes vaporariorum and on Bemisia tabaci. - 149 -
41 CL Ya,
d i W OA Ot 1- 1- to N co N wC 1111111
CL a. N at OO 10 CL Ab -IV aO N 10
'O aa .0 .0uv to et 1. .r 1- N .r en M WIN .rm C Co OOOOOOO +1 +1 +1 +1 +1 +1 +1 +1 M r- r- OO1. O bJ Ix O 11 O: N 04 01 OO . -. to IL1 1n 1A NOO WIC N
b yý n co CO co of .N at N t»d 'r C 1111111 NS 0 10 C CL O to UC N u
m 9n UI . .0 Ci uC lO -4 to st P. Ot M et C3 NNNN N WI d J uil+ý OOOOOOO N wN N +1 +1 +1 +1 +1 +1 +1 O +ý MOMOc, Ln P. P. at O+ dE Ix .+O t0 u, 1t C, N v ýJ In an 1n NNO at to a 17 v 41 C +)
WIO ac O d wý to 1- ON co in th N .L ar a d NN CA 1I1IIII .Jo v- OO l 0r +1 L M at MMNOM E Lý L 0 °C W 41 >, ýO N N C +a Ai ua .0au 4o oc t0 to NO T= .4O 'sf a ýI N N . -ý .r CV N . -4 N It7 rU 7r Lr N OOOOOO A= Lw u or +1 +1 +1 +1 +1 +1 +1 +1 L. CD W yý IX 1.1. - OO T- O br eh tO O 01 1ý 00 Q1 LN ý. T 0 O +ý at In %O Q. 4! AL yC i RJ r A VI N Ei I. N L. ýO O et co to tf to O 10 w v- n ai .+N- .4N O +J CL 11111111 7 Ql IO 'O CJ p ai ýi CO in co 'd' OO CO Cl CL ° O E N dJ Y" C Ld T O I-ý L Oh N W 10 i0 .0 U D yO r, CO M M ßt9 O E V- G a ýO M N M N -W In o 4. WI d wL N O O O O O O O O Op L V- O +1 +1 +1 +1 +1 +1 +1 ar a d0 1ý P7 fr O M O O 7c ° Ix J2 9 M In 1ý .r aF u+- v E d "r - - to N O .r M Z u .93 0 o0 . - 4-A - NN0 O O O O O O O O d V- G M M M M M M M ad. WN Z 10 N M ++ E
W oN-. IC! Lo0 N ý- Eu A L N 4- CN NoC Un om dV- ý -N N NLC p" VI Ea.. 3 WI C *ý E F- ar ro Q .w co s - 150 -
ýw böý
W1 öä
Ö3
Öä ý'
ä s°, 3 z'
U) w
U)
O D, 9 a Co ö
cýc
ý wl 3 Nep
v OI p tC ,
m pUO
Z "-f c6 ZOO yCi - 151 -
V
V
ýo N
.
i
..
I E" U_ o"- Iý Fu" N WIII I rý uil u+l lC V 01i. 8 6c4 W U Z W
acc W 2 W
m W H
Q
., W to 2 I-
I a
I
r4 d 0 'A
O
NO OD to VN O
dSVM LI3d S003 AO ä38WfN - 152 -
Oogenesis and oviposition
The results (Figure 23) show for E. eibcensis and E. adrianae that the number of mature eggs per wasp in ovarioles declines gradually from the beginning of the oviposition period until the wasp almost runs out of eggs after eight hours. Meanwhile the mean number
of parasitized hosts (laid eggs) increases gradually during the same
period. But the second experiment with E. adrianae lasting 48 hours
showed that after 12 hours the pattern changes and the number of mature eggs in ovarioles starts to increase, reaching a mean of about
12 eggs per wasp which is suggested as the mean of the egg storage capacity of this species. These results confirm an increase in the
rate of oogenesis in wasps that have been in contact with hosts for
some time, which may be attributed to the effect of host-feeding as has been demonstrated for other parasitoid species (see Jervis & Kidd
1986). On the other hand, the average number of eggs laid per female
remains almost constant, irrespective of the duration of the oviposition period (8,12,24,18 h) suggesting that wasps were
limited in their oviposition activity by factors other than the availability of eggs (i. e. mutual interference).
3.7 Sex ratio
Many hypotheses (Flanders 1959, Zinna 1961,1962, Williams
1977, Charnov 1982, Waage 1982, Hassell, Waage & May 1983, Avilla &
Albajes 1984, Donaldson 1985, Hunter 1986 (Mimeograph)) have been
proposed and explored empirically as well as theoretically,
attempting to explain how sex allocation takes place in parasitic - 153 -
s
>ý
3
C O w,d i tJca &)0 a)8 I: 4.4 4jS ý ö Q, m co O Oi m "d . c c aý S. cc ö ca 4
Mo ö 0 O a O 0 Ö 4 S O r. N 0 G c b c'ý
td O Q) Ö .C 9 C J., x: C N O B Co CO Co Co Co +ý v --r O v v v 1. W %ý
O +' N 0 c0 i i 0 O 0) co
(13 .0 SID C a> C 43 ca r-4 L 4 19 .4 cOÖ 9 L. U co 43) 10 Ä ý' ccc y 4) ail ci
N - 154 -
rrWý, r,
0 I.
S. . . .
t v
.` N -
(0
O 1 c O_
Co ca a ec z O V Co
. Co uil uil tC O 1
1 O
A I,
1 N
;'
0 N0 CO to le N r r. d SV M d3d SDE)3 d0 U39 WI1N - 155 -
Hymenoptera in general, and in particular for species which deposit
female eggs and male eggs in different types of host, being the 'heteronomous hyperparasitoid' species, maybe one of the most
representative cases. Sex ratio in these species has been claimed to
be adaptive and related to the availability, relative abundance, and
frequency of encounters of one or another type of host; genetic factors have been claimed to be involved in the mechanism of sex
allocation also.
The aim of the present experiment was to get information about
the sex ratio of the species involved in this work in laboratory
conditions and find out if there are differences in sex ratio among
those species, rather than answer the questions of how and why the
sex allocation works in those species.
As mentioned before E. formosa is a uniparental species and
males are rare in cultures, so only the biparental species were
included in the experiments.
3.7.1 Materials and methods
New cultures of the three biparental species were initiated in
the environmentally controlled conditions unit. Two pots containing
four bean plants, each infested with an abundant population of nymphs
B. of tabaci in third and fourth instar were set up in rearing cages
(Figure 2). New plants were introduced into cages when required.
Young adults of both sexes of the parasitoid species were obtained from the stock cultures and kept for 24-48 hours in glass - 156 - vials as described in Section 3.2.1.
A population of 100 couples of each species was released into its respective rearing cage. These adults (as many as it was possible to find) were removed from the cages seven to eight days later.
Sex ratio was determined in the new cultures by sampling the parasitoid population in pupal and adult stages.
Samples were taken at five day intervals, starting the pupal sampling ten days after the release date and the adult sampling five days later; 50 pupae and 50 adults were taken at random in each sample. Adults were sampled with a miniaspirator from the underside of the leaves; the sex ratio was recorded and the wasps released back into the cage immediately. As many adults were observed on the walls of the cages, trying to migrate, a second adult sampling was conducted from the walls of the cage of E. adrianae culture. Pupae were sampled by cutting a small piece of the leaf around each one and keeping them individually in gelatin capsules until adult emergence.
The sex of the emerging adult was recorded and the wasp released in its respective cage.
The sampling was carried out for about two months, so that, depending on the developmental duration of the species involved, there were at least three generations of the parasitoids during the sampling time. - 157 -
3. T. 2 Results and dicussion
Results are given in Table 24 and represented in Figure 24.
They show first of all that the information obtained varied according to the stage sampled.
Sampling of adults on the underside of the leaf showed an almost 100% female-biased sex ratio in the three species. In contrast, observation of the adults of the three species walking on the walls of the cages, confirmed by the sampling of E. adrianae
(Table 24), showed that males concentrate on the walls of the cages, trying to emigrate rather than staying with females in the host patches. This could be because the females were already mated. On the other hand, adults obtained from pupal sampling showed a more steady cyclical sex ratio, but female biased in most cases.
Taking into account previous findings for development time of both sexes, host stage and host type, these results suggest that sex
in E. deserti E. E. ratio , cibeensis and adrianae changes in relation to the available type of host; males in cultures are produced mainly by females parasitizing their daughters rather than their sisters; males tend to disperse more than females which show a tendency to stay on the underside of the leaves; there is little difference in the pattern of sex ratio among the species studied. - 158 -
d bC MO 10 wr O A OO O 1ý O NOO L C 01 0 Cl eF eO at N b .a 1l ON In 00 .r
W
o rn %0 00 A_ 000 .i o0 o CO S LO NNoN 1 Iý r- %0 CO 49 Y ýQ N ý-r Co. dM u CL ao o0 c .ý 0ovo ýc o0 to u o"o N NM Co LO 41 WIC 1,2, 10 L 41 +
4 C Ln a+ to .4o0 no . -. o-o0 00 a) Wp ýo Le .ý in .q.. to .4 v un CO Ln A
to a 12; N d to t. 1 -I O N Cl .+ Cl tl' OO u OO C- U, !V .r !V- 1n U, w W 0 4JN Ln O E N W O MO v L MO MOO d C 1 7d O "O "O I- 'r et 1 O a' . -1 ý.r M .rN r E rý en G Y E 4J N CN b rr CO OO et OO 1 O 1O OL M 1 O 1O MON dN rd 8 .r 1 .r In ON "r 10 4 N qC N Lr ýo X to M Oi O aw N O IC O1 bO 1 N, "O ob N 1O P-4 N co cl 1 ++ u 1N r. 1f) C% Nr d dd
q +7 0 4a E ýe d O M 1ý LO w V- C O NO CO O1 a) d - "O "O "O1 OO N 1l, N .41 oq 1' 00 ON N CI Id 10 jc Ny dL 41 N 61 Ol NI
to 3 rý
CN o- E 10 n= a7 n 7O un ++ =v =v =vv a LE Q. m a Io am ro W N 1p C dy
N Y Q) ++bE a 4 N IC N iý C C N d L y 10 OI d r N u Y CN d a1 Y v Nr a n v u do N7 f- N -Q E ýo WI W' W A 49 - 159 -
witCa (tl 0 0) E m C a)
U W. . ý WI i. U +1 4-1
U NU VV
to
ýý H
cd WC o9 4ý4. ) U
co
0 94 4r U US a) CC
O U Co pp N Co
Ub cU
N - 160 -
n .o, 1L
"L
0
1'11
ie
ýL
d1 m MEMEMEM, V 1 w f }LL } l. L " y .:: "fl. "ý":: '. LPL " ý.ý. In
ca '' z ": ': " LL". ý:: L: ". .L J a a .rý WI y ý.
1 "L': N M
N1 DI1
Iý:: ý }: tiýrtiý: ":ti j"'.rL": ýSLLiL ý: :, Lti ". UJ "": 'ý: ' ""L. fL
N
"" ý'::: :: L y. ".. ": ""L" "": ýL Lgg '. '. '. " .
eeeoeOOOeee O00n 10 N ýº IN
(eIew8: 1 % OIiVF! X3S - 161 -
3.8 Rate of growth of the populations of the parasitoids
3.8.1 Introduction
Birch (1948) describes the intrinsic rate of natural increase (r) as a fundamental parameter which an ecologist may wish to establish for an insect population. He defines it as the rate of increase per head under specified physical conditions, in an unlimited environment where the effects of increasing density do not need to be considered.
The intrinsic rate of increase is of value as a means of describing the growth potential of a population under given climatic and food conditions (Messenger 1964), and it is an important parameter in inductive strategic and management models for insect pest populations (Southwood 1978).
The value of the intrinsic rate of increase has also been used in some cases to compare related species (Orphanides & Gonzales 1971,
Raveendranath 1987).
The calculation of the intrinsic rate of natural increase is based on life and fertility tables which are used to calculate the two main components of r, the 'net reproductive rate' (Ro) and the 'mean length of a generation' (T). Ro describes the number of times that a population will multiply per generation and T is the cohort generation time (Birch 1948). Southwood (1978) defines the intrinsic rate of natural growth as the maximum value of ý population growth - 162 - that is possible for the species under the given physical and biotic environment, and denotes it as rm, which may be calculated from the following equation:
1i e-rmx 1m xxx where: x= the pivotal age in days
lx = the age specific survival (the number females surviving at the beginning of the age class x, as a fraction of an initial population of one)
mx = age specific fertility (progeny x interval x proportion of females)
rm = the intrinsic rate of natural increase
The rates of growth of the population of Encarsia formosa, E. deserti, E. cibcensis and E. adrianae were calculated from life and fertility tables (Appendix 4) which were constructed for the four species of parasitoids, with mean values of the different parameters obtained from studies on the biology of the species (Chapter 3), and also for E. formosa and E. adrianae with experimental data. Details of the calculation of the parameters are given in Appendix 4. They were calculated for the species developing in the third nymphal instar of Bemisia tabaci. The difference between the thelytokous reproductive strategy of E. formosa and the arrhenotokous strategy of the other three species was taken into account by using the sex ratio of the species when calculating the 'age specific fertility' (mx) in fertility tables. Mortality during the pupal stage (Table 35) was considered as mortality of immature stages, in calculation of lx.
Because age specific adult fecundity data were not available for E. cibcensis and E. deserts, and because data for E. adrianae and E. formosa showed no consistent patterns which could be used to - 163 -
approximate patterns, for the other species, a simplifying assumption
was made that daily fecundity was constant. In reality it is not for
E. adrianae and E. formosa (see Appendix 4b, mx), and difference in
daily patterns of egg production which could affect rm are therefore
not incorporated. However, by treating all species in this way, it
is hoped that this source of error in comparison of species is
minimized. rm was calculated using a computer program based on the
formula given above.
3.8.2 Results and discussion
The calculated and estimated values of the intrinsic rate of
increase of the four species of Encarsia in Table 25 show the
following trends: rm of E. formosa calculated from direct
experimental data was higher than that estimated using the average
values of the biological parameters. This may be explained by the
trend in the pattern of age specific fertility (mx), which in the
former case was calculated using data of host parasitized per
interval (fecundity), whereas in the latter case it was estimated based on the mean number of progeny produced per female (live births) and considered constant during the generation time. In the case of of E. adrianae the difference was very little, which may be also explained as being due to its pattern of age specific fertility (mx)
(see Tables and Figure 36 in Appendix 4).
Despite considerable differences between E. formosa and other species, in fertility and reproductive strategy, the intrinsic rate - 164 -
Table 25. The intrinsic rate of increase (r ) of the population of four species of Encarsia cfveloping in third nymphal instar of Bemisia tabaci (Temp. = 25 + 1°C; R. H. = 75 + 5%; L: D = 16: 8)
r m Species (A) (B)
E. formosa 0.237 0.209
E. deserti ----- 0.192
E. cibeensis ----- 0.223
E. adrianae 0.198 0.196
(A) calculated from experimental data. (B) estimated using average values of biological parameters. - 165 -
of natural increase of all species differs very little. These findings confirm Lewontin's (1965) theory about the effect of development period on the intrinsic rate of increase. He stated that the intrinsic rate of increase of a population is influenced as much by small absolute change in developmental rate, of the order of 10%, as it is by large increase in fertility, of the order of 100%. In fact, E. ciboensis showed the highest value of intrinsic rate of increase despite being the species with the lowest fertility (as much as twice as low as that of E. formosa). This is due to the effect of its developmental period which confers to this species the shortest generation time compared with the others.
There were no replicates for rm value. However values in Table
25 were obtained from average values of biological parameters from a considerable number of replicates (see Appendix 4a and the respective
Tables in text).
In conclusion, the results indicated that the value of the intrinsic rate of natural increase of parasitoids (rm) did not differ greatly between species, and suggeted that they have a similar population growth under the same environmental conditions and in the same host stage. - 166 -
CHAPTER 4
EFFECT OF HOST DENSITY ON LEVELS OF PARASITISM AND OTHER FACTORS
AFFECTING EFFICIENCY
4.1 Comparative functional responses
Estimations of functional responses have become an important means of investigating the efficiency of natural enemies under controlled conditions, as they describe the response of the natural enemy to changes in density of its host; they are also useful to compare efficiency between species by means of comparison of the functional response curves and their parameters.
4.1.1 Review of literature
The terms 'functional response' and 'numerical response' were introduced by Solomon (1949) to describe basic components of the relationship between a natural enemy and its 'victim'. He defined functional response as the relationship between the number of hosts
(prey) attacked per natural enemy (parasitoid or predator) and host density, and numerical response as the relationship between the number of natural enemies and host density.
Holling (1959a) examined previous results of laboratory experiments on relationships between host density and its predator
(parasitoid), (DeBach & Smith 1941, Ullyett 1949, Burnett 1951) and - 167 -
his own results, and recognised three distinct types of curve
describing the functional response (Figure 25): type I where the number of prey killed per predator is directly proportional to prey density, so that the rising phase of the curve is a straight line to a plateau; type II where the number of prey attacked per predator
increases very rapidly with initial increase in prey density and thereafter increases more slowly approaching a certain fixed level, the curve shows a continually decreasing rate; and type III where the rate of attack at first increases with increase of prey density and then decreases so that the functional response curve is S-shaped.
These three types of functional responses are discussed in detail by
Hassell (1978).
Mathematical models have been proposed since early in the century in an attempt to describe host-parasitoid or prey-predator relationships (Thompson 1924, Volterra 1926, Nicholson 1933,
Nicholson & Bailey 1935). Some of them will be examined here, since functional responses are implicit in them, with assumptions which sometimes may or may not have any biological validity, such as that parasitoids do not run out of eggs, or that predators do not become satiated, or that parasitoids and predators oviposit or search at random.
4.1.1.1 Type I functional response
Type I functional response occurs when the number of prey killed per predator is directly proportional to prey density, or a parasitoid attacks hosts in direct proportion to their abundance.
This behaviour tends to cease abruptly due to any physiological - 168 - constraint, for instance the predator is satiated or the parasitoid runs out of eggs, giving rise to the plateau (Figure 25a). This type of response, according to Rolling (1959a), was postulated by Ricker
(1941) for certain fish preying on sockeye salmon. These responses are typical of aquatic filter-feeding invertebrates that waft in plankton in direct proportion to its surrounding abundance (Hassell
1978).
Nicholson & Bailey (1935) proposed a model to explain the parasitoid searching behaviour which made two important assumptions:
(1) The number of encounters with hosts, Ne, by Pt parasitoids is in direct proportion to host density Nt, thus
Ne =a Nt Pt, (1)
where the constant a may be viewed as the proportion of the total number hosts encountered by the parasitoid during its lifetime.
Nicholson assumed a to be a species specific characteristic, which he called 'area of discovery' of the parasitoid and Rogers (1972) called
'area of search'.
(2) The number of encounters, Ne, is distributed randomly among the available hosts.
The probability of a particular host not being attacked is given by the zero term (p0) of the Poisson distribution, namely
Po = exp (- Ne/Nt ) - 169 -
A general model for predation or parasitism is provided by the
following equation:
Na = Nt [1- exp (- Ne/Nt )]. (2)
in which according to Rogers (1972), Thompson (1924) and Nicholson &
Bailey (1935), differ in the form of the exponent of the equation.
Thompson suggests that the parasitoid is limited by its fecundity and
makes the exponent dependent on it, whereas Nicholson & Bailey assume
that the limiting factor is the parasitoid's searching capacity and
make the exponent dependent on it.
From (1) equation Ne / Nt =a Pt and by substituting in
equation (2) Nicholson & Bailey predict the actual number of hosts
parasitized.
Na = Nt L1- exp (-a Pt )] (3)
Assuming a constant time T available for search Hassell (1978)
describes the linear response (type I) by the equation
Ne/Pt = a' T Nt (II)
Ne where is the number of encounters with the host and at is the
instantaneous search rate. The combination a'T is identical to
Nicholson's area of discovery a in equation (1). - 170 -
By substituting a in equation (3) with its equivalent a'T, the equation for a linear response in terms of number of host actually parasitized becomes:
Na = Nt [1- exp (- a' T Pt)l (5)
4.1.1.2 Type II functional response
Rolling (1959a) stated that type II functional response occurs when the number of prey attacked per predator increases very rapidly with an initial increase in prey density, but at decreasing rate towards an upper asymptote (Figure 25b).
It was Holling (1959b) who first pointed out the essential biological difference that distinguishes type I from type II functional response: equation (5) assumes a constant searching time
(T), but parasitoids and predators spend time on a series of activities other than searching, such as handling the host or quelling, killing and eating a prey and then cleaning and resting, which reduce the actual time available for search. These activities are collectively called " handling time" (Th)"
If, Th is constant per prey encountered for a particular parasitoid or predator and Tt is the total time during which the parasitoid searches for a host, the actual searching time Ts is determined by the number of hosts encountered and is given by:
Ts = Tt - Th (Ne/Pt) i6) - 171 -
Substituting for T the actual searching time Ts in equation (4) and rearranging (Pt= 1)
at Tt Nt N e (7) (1+ a' Th Nt) which is the Holling's 'disc equation' (Holling 1959b, equation 4).
From the disc equation (7) and Nicholson & Bailey's equation
(3) Rogers (1972) obtained the 'random attack equations' for both parasitoids and predators:
a' Tp Na = Nt L1- exp {-tt }] (for parasitoids) (8) (1+ at Th Nt
which expresses the functional response for a single parasitoid in terms of number of hosts attacked rather than encounters.
L1- {- (for Na = Nt exp a' Pt (Tt - Th (Na/Pt))}7 predators) (9)
The two equations differ because a parasitized host remains exposed to further encounters by foraging parasitoids, and in a re-encounter the parasitoid spends the same time handling the host as in the first encounter. Also predators consume the prey, so prey density changes during the predator-prey interaction. Consequently, altogether more time is spent in handling by a parasitoid than by an equivalent predator (see Hassell 1978 for full details and examples).
More recently, Arditi (1983) modified the classical 'disc model' for type II functional response, to describe parasitoids that are able to discriminate between unparasitized and parasitized hosts. - 172 -
In his model he introduces different handling times for each type of host.
Arditi's model makes the following assumptions: (1) searching parasitoids move randomly in a constant environment and encounter hosts at a rate a; (2) the parasitoids always discriminate between unparasitized (healthy) and parasitized (infested) hosts; (3) the encounter of a healthy host reduces the searching time by an amount
Th; (4) the encounter of a parasitized host reduces the searching time by an amount Tp; (5) no other factors influence the activity of the parasitoids.
With these assumptions, Arditi's model for (Np), the number of hosts parasitized during the time interval T, is given by
PT (T T)N] Chpp)}-a[ - Np N{1- exp (10) 1+aTpN where N is the number of hosts and P the number of parasitoids, and
Th and Tp represent different handling times for unparasitized and parasitized hosts respectively.
In Arditi's model, Rogers's 'random parasitoid equation' and
(for 'random predator equation' become special cases when Tp = Th non-discriminating parasitoids) and Tp =0 (for predators).
4.1.1.3 Type III functional response
Type III functional response (Figure 25c) was stated and demonstrated by Holling (1959a) in his study of small mammals 173 - -
a
w 2
W G Y W V Y Q F- C) h- Q H F-. b Q z _0 F- Ic w 0 m d 0 Ic z d
C
HOST DENSITY (Nt)
Figure 25. Curves representing the three types of functional responses; a, type I; b, type II; a, type III (after Rolling 1959a). - 174 - feeding on sawfly cocoons. Since then it has been assumed that type
III functional responses were typical of vertebrate predators, while type II responses were characteristic of invertebrates (predators and parasitoids). But van Lenteren & Bakker (1976), Hassell, Lawton &
Beddington (1977) and Hassell (1978) changed that concept by giving evidence that sigmoid responses are also common among arthropod parasitoids and predators. Furthermore, they suggest that type III responses may be much more common than was supposed previously. They argue that the normal practice of carrying out experiments in artificial laboratory systems may have produced a distorted picture of the full range of behaviour which invertebrate predators are capable of showing, confusing the interpretation of the results.
According to Hassell, Lawton & Beddington (1977) and Hassell
(1978) the importance of distinguishing between type II and type III responses rests on their supposedly very different contributions to stability. They state that type II functional responses cannot contribute to stability of a predator-prey interaction, whereas sigmoid functional responses can, since they are density dependent up to some threshold prey density.
At least three different phenomena can induce type III functional responses (Jones 1986): an increase of at with Nt, an increase of T with Nt or a decrease of Th with Nt. See Murdoch &
Oaten (1975), Hassell, Lawton & Beddington (1977) and Hassell (1978) for models and full details on sigmoid responses. - 175 -
i. 1.1.4 The domed type of functional response curve
A different type of functional response has been obtained in
some works, the 'dome-shape' curve. It was first reported by Welty
(1934, cited in Rolling 1961). He observed that goldfish consumed
fewer Daphnia sp. when the prey were present as a dense swarm than
when they were less dense, Welty attributed this decline to a
confusion effect, presuming that several prey in the immediate field
of vision of the predator offered conflicting stimuli that blocked
the feeding response. A similar effect was observed by Morris (pers.
comm., cited in Holling 1961) when the pentatomid predator Podisus
maculiventris (Say) attacked larvae of the fall-webworm Hyphantria
cunea (Drury), and he attributed this to the continual disturbance of
the predator by large numbers of active prey. A similar effect was
observed by Utida (Mori & Chant 1966) in host-parasitoid interactions
in experimental populations of the azuki bean weevil, Callosobruchus
chinensis (L. ), and the parasitoid Heterospilus prosopidis Viereck.
Holling (1961) concluded that if the confusion or disturbance
component works in the prey-predator interaction, then a domed type
of functional response might be expected. In fact Mori & Chant
(1966) observed a domed curve as an effect of disturbance of the
predatorPhytoseiulus persimilis Athias-Henriot at high densities of
the prey Tetranychus urticae (Koch). They found that the number of prey consumed diminished significantly at higher prey densities after a maximum consumption at lower densities. They attributed this result to the fact that frequently a prey may be abandoned before it
is killed, due to disturbance of the predator by other prey. They also found that the number of captures abandoned because of - 176 - interference increased with increasing prey density, and reported significant differences in abandonment between the different prey densities. Despite this Takafuji & Chant (1976) argued that the decline in number of prey consumed should be due to the predator increasingly preying on the newly laid eggs at the higher adult prey densities.
Fernando & Hassell (1980) carried out two series of functional response experiments using the same species as Mori & Chant (1966) and similar densities but various stages of the predator as well as the prey. They found that the functional responses were mostly of a typical type II form, with three exceptions: one that showed a type I response and two that seem better described by type III functional response. No domed functional response curve was found in their experiments.
4.1.1.5 Estimating parameter values
Many attempts have been made to achieve a proper definition for the parameter a or at. It has been called 'area of discovery'
(Nicholson 1933), 'area of search' (Rogers 1972), 'instantaneous search rate' (Hassell 1978), and it represents the searching efficiency of an individual parasitoid or predator (Waage & Hassell
1982). Searching efficiency is fully discussed by Hassell (1982), from both theoretical and applied points of view.
'Handling time' (Th) has not been discussed as widely as searching efficiency, but its importance has been generally accepted - 177 - and it is often included in different models, as the portion of the total time spent on handling the host or quelling, killing and eating the prey and then perhaps cleaning and resting (Hassell 1978, Waage &
Hassell 1982).
Arditi (1983) introduced Tp as a third parameter, in his unified model of functional responses, to describe the time spent by a discriminating parasitoid handling a previously parasitized host.
The functional response equations can be rearranged to estimate the values of the attack coefficient (a') and handling time (Th).
Rogers (1972) suggests the use of a linear regression of transformed data to estimate the values of attack coefficient and handling time, while Hassell (1978) suggests the use of a standard nonlinear least squares regression technique applied directly to untransformed data.
(1983) But Livdahl & Stiven question the statistical validity of the traditional linearization of the disc equation suggested by Holling
(1959b) and by Rogers (1972). With respect to the least squares method, they argue that the biological significance of the
(see coefficients Livdahl & Stiven 1983, equation (4]) is not clear,
the and meaningful parameters a' and Th emerge only as combinations of these coefficients. They also argue that because each coefficient is an estimate, the construction of confidence intervals about the estimated a' and Th values is a difficult task. They observe the general absence of confidence intervals for at and Th in the functional response literature.
Livdahl & Stiven (1983) suggest the use of a linear transformation (Lineweaver-Burk plot, based on the Henri-Michaelis - 178 -
Menten model) different from the one suggested by Holling (1959b) and
Rogers (1972). However, Williams & Juliano (1985) believe that the use of linearizations of the disc equation, especially the one advocated by Livdahl & Stiven (1983) produce highly variable and/or biased results. They conclude that non-linear least squares regression and a nonparametric technique produce more precise and less biased parameter estimates.
Houck & Straus (1985), in a comparative study of functional responses, review existing experimental and statistical procedures with reference to Holling's generalized model of functional response.
They describe: (1) a general experimental design compatible with
Holling's model, (2) a maximum likelihood method for fitting the model, (3) several available methods for statistical comparison of sets of functional response curves, and (4) an exploratory graphical method for examining patterns of variation among larger numbers of samples.
The functional responses are used in the present work as a method to study and evaluate the effect of changes in whitefly density (host density) on levels of parasitism by the four species of
Encarsia being studied, and overall to compare differences in efficiency of the parasitoids attacking different types of host (host instars). - 179 -
4.1.2 Materials and methods
The experiments were carried out under the laboratory conditions described in Chapter 2.
The stock cultures of Bemisia tabaci as well as of the parasitoids were kept on bean plants as described in previous
Chapters. Leaf cages as described in Section 3.2.1 were used for these studies.
The different numbers of hosts (nymphs) required were obtained on the 'test leaf', which was the terminal leaflet (foliole) of a trifoliate bean plant leaf, by exposing uninfested and previoyly cleaned plants to whitefly in rearing cages for 12 hours, so as to get a population of uniform age and stage on the leaf (see Section 2.
3.1 for B. tabaci developmental duration). Thereafter, adult whiteflies were removed by spraying the plants with soapy water. The required number of whitefly nymphs in the instar desired were then obtained by removing the excess and the other stages, using fine forceps. Each leaf was divided into one distal, one middle and two proximal sectors, which were delimited by the main veins as shown in
Figure 26a and all the nymphs on the proximal and distal sectors were also removed; in this way a more or less uniform size searching area was obtained.
Adult mated females of the parasitoids were obtained as described in Section 3.2.1.
The constant conditions of trials were: the environment, the number of parasitoids searching (one wasp per arena = 'test leaf'), -180- the age and stage of the wasps (24-48 h old mated females), exposure time (24 h) and the area of searching (middle sector of the leaf = 18 2). cm
Based on preliminary trials in the present study and in literature (Perera 1982, Sharaff & Batta 1985) the following host densities were tested: four, eight, 16,32,64 and 128 nymphs per leaf. Each density was replicated six times. Control treatments were included for the five host stages, whitefly immature stages were kept in the same way as the other treatments, the same densities and number of replicates but without parasitoids. The five immature stages of B. tabaci described in Chapter 2 were tested separately.
The species of parasitoids tested were: Encarsia formosa, E. deserti,
E. cibeensis and E. adrianae.
Although, 'host experience' has been shown to be of considerable importance in the foraging efficiency of some parasitoids (Samson-Boshuizen, van Lenteren & Bakker 1974 cited in
Jones 1986) and suggested for Encarsia by Fransen & van Montfort
(1987), Gerling & Foltyn (1987) and Waage (pers. comm. ), the wasps in the present experiments were not given prior 'host experience' in order to standarize them; by being sure that all of them had the full fecund capacity (see oviposition and fecundity sections 3.5 and 3.
6) it was assumed that the exposure time was enough to give the wasps the opportunity to get experience in searching, handling and parasitizing the host.
The test leaves were prepared as described above. The mated female wasps were taken from the vials with a miniaspirator and - 181 -
immobilized by chilling in the refrigerator for one minute, and then
introduced into a leaf cage, the 'test leaf', attached to the plant,
was fitted in the cage. Wasps were removed after 24 hours and the
plants kept in cylindrical cages. The whole setup of the experiment
is shown in Figure 26b.
The number of parasitized hosts was recorded 10 to 13 days
after exposure, and wasp and whitefly adult emergence was recorded as
well.
The results were computer analysed in three ways (1) data were
examined in an exploratory graphical method by a Statgraphics System
(Statgraphics 1986), (2) as functional response using a non-linear
squares program and curves fitted using the "random attack equation"
for parasitoids (Rogers 1972) (3) by using the GLIM program (3.11
Royal Statistical Society, London, 1977) to carry out an analysis of
deviance.
4.1.3 Results and discussion
The raw data of the experiments are given in Appendix 2.
Figures 27-30 show a graphical analysis by plotting the mean
number of hosts parasitized (Appendix 3) for each of the five stages against the host density and for the four species of parasitoid.
They show in general that second, third and fourth nymphal instars are the most parasitiszed and first nymphal instar and pupal stage
the least parasitized. In most cases, within each stage, the number - 182 -
Figure 26. a, 'Test leaf' (d, distal sector, m, middle sector, p, proximal sectors); b, setup of functional response experiment. - 183 -
a
b - 184 - of hosts parasitized increased as host density increased from four to
128, in a way that suggests a type II functional response, in a few cases that trend was not maintained when density increased from 64 to
128 hosts; the number of hosts parasitized diminished at the higher host density, suggesting a domed curve of the functional response in the cases of E. formosa parasitizing third nymphal instar (Figure
270) and E. adrianae parasitizing first instar (Figure 30a).
The maximum mean numbers of hosts parasitized were found at host densities between 32 and 128, in the four species of parasitoids
(Appendix 3), and varied between the third and fourth instars of the host, 13.8 third instar nymphs being parasitized by E. adrianae, 12.8 by E. formosa and 7.5 fourth instar nymphs by E. deserti and 5.2 by
E. cibcensis. These means are related to the daily maximum fecundity of the four species of parasitoids (see Section 3.6.2).
Tables 28-31 record the mean percentages of hosts parasitized by each species of Encarsia on the five host stages and six different host densities. These data show a continually decreasing rate as host density increase from four to 128 individuals.
The mean numbers of hosts parasitized in each of five host stages and six densities by four species of Encarsia are displayed graphically in Figure 31. They show clearly maximum numbers of hosts parasitized on host stages two, three and four, and that the least parasitized was the pupal stage. Differences between species are also clearly shown in the Figure. - 185 -
C) C) 4.3 +) m 91 0 OC m w >o 0>
ON... s. 4r Ooy oHO C. C) a
a) °. C) co O
CO N U ýa 0 Wo
,DX cm Z M Co 4) W .a tu a) t. i
.HUv CO
+I vd 41 Ik o) W >s C) C) CNCL. C)
03 a) in O Cu cu +ý C. C) S. Cu Cu Cu O CL. a y) .C o) ti N a, bo H W - 186 -
a 0 t a M
0 N aN a a
0 0 0 0 a a } F J 0 0M 0 "s Z
0 a 0 0 of W 0 I a 0
0 aN N
II11111111 1J: t !0 I! IIIIIIIIIIIII Q ID lY o0 19 0 QN0DA0 14 11 14 14
0 0 0 i r I a a 0 0 0 N N a MN
0 0 0 0 0 0 a } h 0 0 QM " I as Z m 0 0 0 0 0 0 cl- t a 0 f 0 I 0 0 2 I h t I c 0 hI a a 0 I N n F
iupIIIV1 I1 iI13t11p IIIIIIIIIIIII1 I-1 13 QN00A0QN0 l0 0 inq 14no0no
aezxixavarv_ aJ -4 ýo ýaawnn+ - 187 -
a) a) 4) o vý 0 0 a) > a) w o> w ON
Oow C
Lam. HO c, C) a QJ 4.4
aý 02 cý ao
CO U C) O WU +-1
""I x-I N O Mj 42 . pOx cu 4. 41 O o O Cli ýý "-I pOj Ov rl 0 Ei . a, +ý v
14 vii w> Q) O4
6OOO ONOa, +1 O
a) 02 Co cd c0 40
«1 ce O 4) L1.0. M 92
N N L. v
M [LI - 188 -
0 0 r 4 a 0 0N N
0 0 0 0 a a } 1- 0 OH 0 00 s Z 0 0 0 0 0F 0 a 0 t I a 0 0 t t
0 i 0 I N i N
VIIIIIII1III II Ip ittitt11111IY LU 10 N00a0 DN00ND "1 "I .4a
0 0 0 t t
-o C 0N N -N M a _ ..1 0 0 -o 0 -o 0 a } º- F 0M 0H -o I C -m en Z zW W 0 0 0 0 0 0F 0h 0 0 a a e 0 0 I I F i 0 D e t t
o 0 0 N! N N i IIIIIIIIIIIII I--, IQ ttI1IItII11 11 rI pLlIIIIIIIIII "r 1I10 in N00 11 0 in N00A0 o! o .4Mnaa. VI 11 14
oazz l: svb+v.. d MJ I-4 . Io owmmwnW - 189 -
v) om 0 m to Z. cu a) 41 .c of o yN .ý .0ýN
ÖI
a .,
°1 q Co a) N wA
0N0. a tu °) ,4 m 0] 0) 0 t' 4 0 o tu w ml Co rf a ý "- .os. "
U) Coca Co A-4 (n o
ý r- !C M 02 " CO 13 +i wvv o .d .ýv 4) b aN 14 0 -m 07 4) ,N N
4-3 tu 0 u) L. 4-3 fr M Z. 0 °c s A. ,
N 4)
00 CTr - 190 -
0 0 r f
D 0 N N
0 0 0 0 a a }
QM H 0 I e 2 Id 0 0 0 DI i a º- 0a i I i D 0 Vi t i 0 0 N i a i i
U i1111111111I1 0 VI1U[III!! III10 mN00A0 0N0NA0 .4M .4 14
0 0 0 rM
n 0 N 0N a a
0 10 0 0 a a a f0 F 0 0M S Iq co tjt 2 m a to 0 a t0 0 Df q a I- i I S U 0 Z 'f N I
I- m D 0 N 1N N N l.
IIIIIIIIIIIIII 1I 01IIIIIIIIII11YIIp II LV DN0Dm0DNNDND qNNN Al 0 N .4N .4
O7ZS1ISVMV.. 1 MliOM . 1O UIMMINMN - 191 -
02 4.3 43 ° o .. 0 4)s° .O o. ,> LwON 'O Z. , > cd o
ca L N n1 il "ý w L Co t. Co 43 a) ei ao ° co
LO Co 41 N O C %O OkM x tu 4M %d 4) +3 o m ai .i03 CO v m HO +' 4) 00 ,x o) 6ý v 7s O OO +3 8OOO NOL 02 3 4-4 O ý0 a) ca LLO d tu O 4) aaC v) 0 M m 00 +-I W - 192 - Q 0 f a 14 0 0 N n a 0 0 0 M0 a I- 0 0 D 0m 2 W 0 0 a D 0E 1 1 I 0 F I 1 0 a t I 0 0 N N U1I1t 1E 1tt -r lLp IIIIIIIIIIi i'r-i ii in naoAo DN00A0 11 14 1 .1 C 0 U f r r N D 0 N CN Mn w 0 0 U D U 0 a Y F 0 0 UM D 0 ea C z u a 0 a 0D of c a 0 t a t e 0 0 0 t I i i i 0 0 U i N N N i 11 111II1IIIII i^I 101 11 IIIIIIIi 'i' jii0 111111IIIIIIII1a DNmON0 Il No0N0 nN00m0 .1 14 VI .4 aaz tiz svaWv.. i W. Luc3 H , 10 lwaBwnr4 - 193 - 1v 14 a, m U) a c a) m s. iä 0, w a, 4) U C5 0) i aý 4-3 +-I 0 4r O O b O C N O cd v U U, m cd adl v, 43 `° 03 a, 4) a) m 0 . tom 4) b L] a) c . cd .a w äm Nýp l'Q aý rl V U 0 O ti-1 N v . -1 4) m 0 W 0) 00 aý O b 4.3 a aý m 0 +-1 92 aý 4) m a> 0 w A 4) w m a 0 19 M m +ýiW - 194 - LD W W N ü rs 0 Co O F- = W N cc O w Z z a, w wr WI -0 w t2 F b 44 O+ a5ý \Aosco N05ý ý\o4 4n w, W of W N Co ti en CO O 0 S Co 0 cc I 0 W U. U WI Ui 4zZ tD r R4 'n in C13Z 111 SV8 Vd $, LSOH dO H3evm - 195 - Searching efficiency, a', and handling time, Th, for the four species of parasitoids were estimated using a non-linear least- squares computer program and the curves fitted using the 'disc equation' (Holling 1959b) and the 'random attack equation' for parasitoids (Rogers 1972). a' Tt Ne =tt (disc equation) 1+ a' Th Nt a' Tp Na = Nt [1- exp {-tt} (1+ a' Th Nt ) (random attack equation) Where: Ne = number of hosts encountered per parasitoid Na = number of hosts parasitized Pt = number of parasitoids searching Nt = Host density a' = searching efficiency Th = handling time Tt = total time With: Pt =1 (one wasp) Tt =1 (24 h tonst) Na = dependent variable Nt = independent variable Non-linear regression algorithms require the partial derivatives of the functions with respect to the parameters a' and Th. They are given in Appendix 5 for both equations. - 196 - The results are displayed in Figures 32 to 35 and the estimated parameters from both equations are given in Tables 26a and 26b. In most cases curves fitted very well with the observed results except in the case of E. formosa attacking the third nymphal instar, where the mean number of hosts parasitized decreased at the highest host density. As suggested before, a dome type of functional response seems to describe better the data in this case, but as this result was not consistent in other stages or species, and given the confidence intervals (see s. e. of the mean indicated in the Figure) it was attributed to experimental error. Nevertheless, it is important to point out that the 'domed curve' of functional response has been suggested for parasitoids of Homoptera (Waage pers. comm. ) in this type of experiment, and attributed mainly to the increasing amount of honeydew present in the arena (leaf) with increasing host density. As a result the wasp spends more time in cleaning and preening her body and the parasitism decreases. The curves overall show that the number of host parasitized per parasitoid increases rapidly with initial increase in host density but with a continually decreasing rate, with upper asymptote different for host stages and parasitoid species. They are of the typical shape of the type II of functional response and as stated above they provided a good description of the data. The curves in Figures 32 to 35 were drawn using the random attack equation (except Figure 32c), but they were the same using the disc equation. In the case of E. formosa parasitizing third nymphal instar there was not convergence with the attack equation so that curve was drawn using the disc equation. - 197 - The estimated values of handling time (Tables 26a and 26b) were the same from the two equations, whereas the values of searching efficiency were different, and larger, when estimated with the attack equation. Also the confidence intervals for searching efficiency were larger with the attack equation than with the disc equation. Due to the very large confidence intervals for a' estimated by the attack equation no differences were found in this parameter between stages within parasitoid species, whereas results suggested some differences when the parameters were estimated using the disc equation. The absence of confidence intervals for a' and Th in the functional response literature when nonlinear regression is used is notorious, as has been pointed out by Livdahl & Stiven (1983) who attributed it to the statistical difficulties in the construction of confidence intervals. The estimates of the parameters a' and Th in Tables 26a and 26b show the following general trends: the searching efficiency parameter increased from the first and second to the third and fourth nymphal instars and then decreased in the pupal stage. There was little variation in the values of handling time between the nymphal stages, whereas the time spent handling the pupal stage was significantly larger in three of the four parasitoid species. The estimated values of handling time differ considerably from the actual (observed) time spent parasitizing a host, for example the estimated handling times of four species parasitizing the third nymphal instar of the host, shown in Table 27, were considerably higher than the observed (see also Section 3.5.2) being about 18 - 198 - O J: 2 Cu c:0 +O-ý L. O H 'O 'C w - 0 -f . to O' 4) N m .N O 4.3 j O (0 e 10 Z. v 0 a) r. m Z 41 ca ct 4) ä '_' 44 Cu s0. > Cu tu Cu (D c: 0 4a tu Co o CU M 9 CU > .r ,c 92 9, cu v m -43 V C: d 'ý Oä 4-1 r-1 i) rl : N O t+ w 4) 0) ^ .0 "-" > G i. « Cu O L. C7N 0 o. 4r l> (D 9. 0 Cu O> 0 N V 0 "- C. cd O Vl - v C +ý O O 0 O R « +1 ýd ýj a X O O O O E L Cu w Ä .ö 40., a) N tr1 a) 00 +-1 W 4- 199 - m in v+ x a. r a. N O u") n CS) to U) U ru # + #t A L- CD CO VN im ID `S NO N ; O m uD. Ln #as +r N N O O m F- N U, U) z W i. K +k D i .Y. 7. " * 4. m CD I- in Cl) O 40 Ln S U) N M N m 0 0m to c cu m CD CD nr cu O m td vN O 00 to c cu O © m U) u') ni cu O m O m .r .r U) U n n m m u) u, un N unN # *\ý a. m m M CO CD N OW tD n- NO N CD C4 QN m GD to CN O a3ZI. ISVUVd S. SOH d0 a38Wf1N - 200 - ö c 0 m 43 4. cd co cv - 03 0' 0 cu 4) -j e. f (1 X .o N C, ýt w '4 +3 Z. 41 tu -4 Q) tu °l @ 'O 0 N L. c V ä r rr 4) Co 4) m cu 'a a c4 M 0 0) ä 2 L- K, a) cC -n o C vy 10 0 y O W .C 43 ä O N 0 a) ti 9 w 4) 'p 7 aý z. om £ Ö C) t .,, L , O 43 0. i vý o) . v aý c v T+ s. ýn O b . 4) .4 Co -4 ° c 4) 0 4) v .i O .. i N 4) 0) a in . x 0 +i 0 r. EI Z. tu n MC. fr 00 1 W - 201- cm un u, N u-) n m U7 U7 a) CD LD C' N CD W co -Nm m U7 in " Ln u, +r ax N N M F- N U") Z n n W F- Ul in N 0 {# 'N #* U7 S Cu OmM mm CO QNM (D QN to Q Nm (D QN O m U, Ui ". N Y+L " Ln + +1. +k N N O O © N N N O m 0 N Ti N Ow CO VNm Co fD QN©M tD ýT N OD ID VNm N C\j a3Z1IISV2Vd SISOH d0 d38Wf1N - 202 - ý ý0 4S U f ob to clj., m Ei 0 m ä °' o s. (L) Ei m c "' c U U b N . -1 W w ce 3 i 4). Ö O b O a ' U O 4 V U cd +ý O ro b ä ä 0 ö CU 02 L= 0 j2 90 v4) C ö r: ö u o pý tio ý' to -t O CU O b +1 4.) cr C Lg. ' m 0 M L 00 -203- m ui x Ntn .. r lf'1 n U) ###i ßt4 UI U N m m CO tD QNm CD tD QNm N 0 0 Ui N ## ** Ln * '04 N Cu N } r .r f- u) Ul U1 Z W m m F- U) Ln N O Ln IP1 N N +k k #t k xa ý xr ý m m m CO to QNmM fD V Cu m O W to v NmW tD -N © m in in N N i Y. Mx +k .r ru O m m m U-) U'1 n n m m uý un 44 c cuun Cuui 41k* *I x xa m m N CD CO of NDW ID Q Cu m m w to Q NOw tD 7 Cu C r. r. N ... ý. - a3ZIiISV 1Vd SISOH H3SWf N -AO - 204 - O R! 0 U 06 4 O O a 4 o ný O 0 0 ns a) o) v o c > co 'i « ä o ö , c W o ö v " 4) to ; L» 03 N c. ei L, ýI v " 0 0 vý aý 0 M 90 CU o G Ü V) 0 . -1 Co EI 0 .0 - 90 0 O 4) O O -41 43 4 C) O 4.3 C i. ý MLA m fr CO G4 - 205 - CD u) * ý" a * un m m un M # # " ## U) U N CS] m OD CD Q N m W ID CN m U) N N O 0 H_ N U7 n z W m U7 f- t N # 0 # # #4 Lf9 2 N 'Q CD NLr) ## " iºýk+i m Q" m CD Q N CO m ID QN OD CD 'W N CD W to Co N CN CD U7 c Ln Ln iº ? "i. * a" ýº " 4. N N i. N m m U") Ui N 4. *"*i. ri i. Y. I. CS) 0 U7 N Ui (ýt N V [rU k# 1ýt + # +401. ýF 'h it "* # -" " N CD m m CO Q N CD to vN m a) to QNmW to QNO a3ZIlwSb8dd S. SOH dO H39Wf1N - 206 - Table 26a. Non-linear estimated parameters of the 'disc equation' (Rolling 1959b) of Figures 30 to 33. a'* searching efficiency, Th** handling time. The sum of squared residuals (SSR) are also given Species a' Th SSR Stage z + s. e. R + s. e. E. formosa first instar 0.443 + 0.136 0.072 + 0.012 330.18 second instar 1.311 + 0.385 0.083 + 0.008 383.54 third instar 1.740 + 0.555 0.081 + 0.008 336.71 fourth instar 1.353 + 0.389 0.082 + 0.008 279.04 pupa 0.260 + 0.180 0.355 + 0.088 86.56 E. deserti first instar 0.300 + 0.119 0.138 + 0.027 163.44 second instar 0.395 + 0.213 0.150 + 0.035 266.97 third instar 1.250 + 0.346 0.134 + 0.010 88.19 + fourth instar 1.454 0.857 0.165 + 0.022 226.47 pupa 0.308 + 0.137 0.163 + 0.033 156.57 E. cibcensis first instar 0.533 + 0.269 0.214 + 0.035 126.44 second instar 0.482 + 0.339 0.217 + 0.051 236.61 third instar 1.511 7 1.045 0.235 + 0.031 118.66 fourth instar 1.003 + 0.745 0.214 + 0.039 227.21 pupa 0.265 + 0.844 0.342 + 0.059 96.37 E. adrianae first instar 0.645 + 0.333 0.144 + 0.026 293.32 + second instar 0.826 + 0.253 0.078 0.009 342.00 third instar 1.050 + 0.246 0.068 + 0.006 264.22 + fourth instar 1.331 + 0.409 0.122 0.010 132.31 pupa 0.249 + 0.104 0.228 + 0.041 72.81 * (a') in units of cm2/h (test leaf = 18 cm2/24h) ** (Th) as a fraction of the total time (24h) - 207 - Table 26b. Non-linear estimated parameters of the 'random attack equation' (Rogers 1972) of Figures 30 to 33. a'* - searching efficiency, Th** - handling time. The sum of squared residuals (SSR) are also given Species at Th SSR Stage R s. e. R s. e. E. formosa first instar 0.581 + 0.237 0.072 + 0.012 330.09 second instar 9.809 + 0.385 0.085 + 0.008 277.86 third instar fourth instar 8.684 + 18.930 0.084 + 0.008 279.04 pupa 0.299 + 0.241 0.355 + 0.088 86.56 E. deserti first instar 0.355 + 0.167 0.138 + 0.027 163.45 second instar 0.498 + 0.340 0.155 + 0.035 266.95 third instar 4.706 + 5.303 0.135 + 0.011 88.00 fourth instar 11.454 + 54.220 0.163 + 0.023 225.00 pupa 0.366 + 0.193 0.166 + 0.033 156.00 E. cibcensis first instar 0.746 + 0.533 0.214 + 0.053 126.36 second instar 0.643 + 0.607 0.217 + 0.051 236.69 third instar 11.511 + 0.049 0.237 + 0.001 118.65 fourth instar 2.229 + 3.816 0.214 + 0.039 227.14 pupa 2.051 + 3.856 0.343 + 0.058 96.24 E. adrianae first instar 0.996 + 0.813 0.145 + 0.027 293.05 second lnstar 1.513 + 0.892 0.078 + 0.010 342.92 third instar 2.601 + 1.678 0.069 + 0.006 266.14 fourth instar 6.688 + 11.425 0.124 + 0.021 132.23 pupa 0.286 + 0.138 0.228 + 0.041 72.80 * (a') in units of cm2/h (test leaf 2 18 cm2/24 h) ** (Th) as a fraction of the total time (24 h) ***--- there was not convergence in this case (see text) - 208 - times higher in E. adrianae and over 70 times in E. cibcensis. Differences between the empirical and estimated values of handling time have been explained as being due to the estimated handling time including periods of non-searching activity, induced by factors such as egg depletion (Hassell 1978). In the present case any other activity on which the wasp spent time, other than the mere act of handling the hosts while ovipositing, e. g. feeding, preening, resting and walking, and rejections of hosts already parasitized or physiologically unsuitable, were excluded from the observed handling time and were included in the estimated value. If it is assumed from the disc equation that T/Th defines the maximum number of hosts that can be parasitized and a' determines how rapidly the curve approaches the upper asymptote, and taking into account information gathered from the biological studies, the following general conclusions can be drawn from analysis of the functional response curves and the estimated parameters: The maximum numbers of hosts parasitized are reached at densities of 32 and 64 hosts per unit of area ('test leaf') with a mean of hosts parasitized that varies with the species of parasitoid, and is apparently related to the daily maximum fecundity of the species. Analysis of the functional response curves and values of searching efficiency (despite the confidence intervals from the attack equation) suggested E. formosa and E. eibeensis, and particularly the latter, as the species with the best searching - 209 - Table 27. Observed and calculated handling time (Th) for four species of Encarsia parasitizing third instar nymphs of Bemisia tabaci (when laying female eggs, Tn in minutes) Handling time Species observed calculated n x ± s. e. ± s. e. E. formosa 43 4.99 + 0.54a 116.64 ± 11.52c E. deserti 32 4.01 + 0.28b 192.96 + 14.40b E. eibeensis 15 4.58 + 0.23ab 338.40 + 44.64a E. adrianae 32 5.44 + 0.68a 97.92 + 8.64c n= number of observations * Handling time calculated with the 'disc equation'; values with 'attack equation" were the same Means followed by different letters are significantly different (P<0.01; LSD test) - 210 - efficiency, since the curves reach the 'plateau' at the lowest host densities. Values of handling time indicated that E. adrianae and E. formosa have the potential for attacking a higher number of hosts per unit of time than the other two species, as many as twice or thrice that of E. deserti and E. cibcensis respectively The fact that some stages are more efficiently attacked than others, within parasitoid species, may be interpreted as an expression of host preference for the stages where the curve reaches the upper asymptote at higher levels. The higher value of handling time shown by the four species handling the pupal stage may be explained by either the physical resistance of the cuticle of the pupa to the ovipositor or by a relative physiological unsuitability of the pupa for parasitoid development. The cuticle (skin) of the pupa is dry and harder than the cuticle of the nymphal stages, which makes it more difficult for the female to insert the ovipositor in the pupa (see Section 3.5. 2. ). Results in the present work show that the four nymphal instars and the pupal stage are parasitized by the four species of parasitoids. However the youngest instars and the pupa are less used for parasitism than the third and fourth nymphal instars. Finally, data were analysed as a binomial distribution (parasitized hosts versus unparasitized hosts) using the GLIM programme (Royal Statistical Society 1977) to carry out an analysis of variance (deviance) in order to find out the statistical - 211 - differences in data already graphically analysed. The analysis was performed separately for each species to compare levels of parasitism between stages and densities (Tables 28-31), and on all data together to compare levels of parasitism between species (Table 32). It was considered an 'F-distribution' and when a significant 'F' value was obtained a t-test was used for individual comparisons between means, using the estimated values and the standard error of the differences. The comparison between levels of parasitism in different host stages by E. Formosa, E. deserti and E. adrianae show significant differences (analysis of deviance Tables 28,29,31) whereas they were not significantly different in the case of E. cibcensis (Table 30). Results of these analyses also show significant differences between species. The highest percentage of parasitism was produced by E. formosa and the lowest by E. cibeensis (Table 32). Tables 28 - 32 also show means of parasitism for stages and species calculated in two ways, unweighted (directly) and weighted by GLIM. The unweighted means give equal 'weight' to each value (percentage) in the six different host densities. GLIM however weighted the values according to the number of hosts at risk, and this was far higher in the high density treatments where the proportion parasitized was lower, so that the weighted mean proportion from the GLIM analysis was lower than unweighted means as shown in the Tables. It has been suggested by Fransen & Montfort (1987) that lack of - 212 - differences between numbers of whitefly nymphs of different instars parasitized by E. formosa can be due to the use of wasps which had no previous experience with the different host stages. Results in the present study do not confirm this suggestion but rather show the opposite, that inexperienced E. formosa, E. deserti and E. adrianae showed preference for some of the host stages. The precise biological significance of the functional response parameters, the way they are estimated, as well as statistical comparisons of sets of functional response curves, have been discussed and questioned and different methods proposed, as mentioned in the review of literature in the present Chapter. The aim here has been to use the variation in values of these parameters and curves, calculated and fitted by one of those methods, to try to explain differences in efficiency of the species of parasitoids studied, rather than look into the statistical difficulties of their analysis and interpretation. With this in mind, the following conclusions can be reached: 1. Differences in mean number of hosts parasitized between stages within parasitoid species may be interpreted as an expression of host preference for the stages more efficiently parasitized. Results suggested host preference for the third and fourth nymphal instars. 2. Type II functional response provided a good description of the data for the four species of Encarsia attacking five immature stages of B. tabaci. - 213 - 3. The values of searching efficiency tend to be higher for the intermediate stages of host than for the younger and older stages. The reverse is the tendency for values of handling time. 4. Statistical analysis confirmed the conclusions suggested by graphical analysis and stated significant differences in parasitism between parasitoid species. - 214 - Table 28. Percentage of parasitism by Encarsia formosa on five stages and six densities of Bemisia tabaci (Temp. - 25 + 1"C; R.H. a 75 + 5%; L: D 16: 8) Host density Stage 48 16 32 64 128 mean+ s. e. mean* first instar 41.67 22.92 27.08 28.12 12.24 8.98 23.50 + 1.98 14.35b second instar 66.67 60.42 58.33 29.17 17.97 7.81 40.06 + 4.15 18.91a third instar 79.17 81.25 53.13 38.02 20.05 6.90 46.42 + 5.09 20.67a fourth Instar 83.33 77.08 50.00 30.21 14.58 9.63 44.14 + 5.22 19.37a pupa 16.67 16.67 8.33 8.85 2.60 2.21 9.21 + 1.07 4.27c mean 57.55 51.63 39.36 26.88 13.49 7.12 * Weighted mean calculated by GLIM. Means followed by different letter are significantly different (P< 01, t-test) (figures . are meanof six replicates). Analysis of Deviance by GLIM source M. dev. mean F-ratio deviance dev. Stage 4 255.0 63.75 31.44** Dens. 5 808.4 161.68 79.64** Dens. x Stage 20 77.0 3.85 1.89 Residual 150 305.6 2.03 Total 179 1446.0 ** (N 01) . - 215 - Table 29. Percentage of parasitism by Encarsia deserts on five stages and six densities of Beeisia tabaci (Temp. = 25 + 1%; R.H. 75 + 5%; L: D - 16: 8) Host density Stage 48 16 32 64 128 mean+ s. e. mean* first instar 16.67 18.75 22.92 13.03 7.03 5.07 13.91 + 1.15 8.27c second instar 37.50 20.83 17.71 15.63 8.33 4.16 17.36 + 2.89 8.59cb third instar 70.83 52.08 38.54 17.19 10.94 5.59 32.53 + 4.29 13.03a fourth instar 66.67 47.92 35.42 14.06 11.72 3.51 29.88 + 4.07 11.37ab pupa 33.33 22.92 20.83 7.81 8.59 4.03 16.25 + 1.88 7.80c mean 45.00 32.50 27.08 13.54 9.32 4.47 * Weighted mean calculated by GLIM. Means followed by different letter are significantly different (P< t-test) (figures . 01, are meanof six replicates). Analysis of deviance by GLIM source M. dev. mean F-ratio deviance dev. Stage 4 34.1 8.53 4.87** Dens. 5 476.3 95.26 54.87** Dens. x Stage 20 44.7 2.24 1.21 Residual 150 264.0 1.76 Total 179 819.1 ** (P< . 01) - 216 - Table 30. Percentage of parasitism by Encarsia cibcensis on five stages and six densities of Bemisia tabaci (Temp. = 25 +1C; R. H. 75 + 5%; L: D a 16:8) Host density Stage 48 16 32 64 128 mean+ s. e. mean* first instar 20.83 27.08 22.92 12.50 5.73 3.38 15.41 + 1.61 7.40ab second instar 33.33 35.42 18.75 7.29 5.47 3.65 17.32 + 2.37 7.014 third Instar 58.33 43.75 23.96 9.89 5.20 4.04 24.20 + 3.74 8.46a fourth instar 53.33 29.17 23.96 14.06 8.07 2.73 22.72 + 3.33 8.59a pupa 29.17 27.08 18.75 10.94 4.17 1.56 15.28 + 1.94 5.75b mean 40.00 32.49 21.67 10.94 5.73 3.07 * Weighted mean calculated by GLIM. Means followed by different letter are significantly different (P< (figures . 01. t-test) are meanof six replicates). Analysis of deviance by GLIM source M. dev. mean F-ratio deviance dev. Stage 4 12.2 3.05 1.26 Dens. 5 483.1 96.62 40.09** Dens. x stage 20 26.7 1.33 0.55 Residual 150 362.1 2.41 Total 179 884.1 "* (P< 01) . - 217 - Table 31. Percentage of parasitism by Encarsia adrianae on five stages and six densities of Bemisia tabaci (Temp. = 25 +1C; R.H. " 75 + 5%; L: D " 16: 8) Host density Stage 48 16 32 64 128 mean+ s. e. mean* first Instar 33.33 33.33 27.08 17.19 11.46 3.91 21.05 + 2.03 10.38c second instar 66.67 68.75 36.46 26.04 15.10 8.85 36.98 + 4.27 17.19ab third instar 87.49 77.08 44.79 30.21 19.01 10.55 44.86 + 5.23 20.70a fourth instar 70.83 66.67 35.42 20.83 11.20 6.38 35.22 + 4.63 14.22b pupa 25.00 18.75 14.58 10.94 5.73 2.86 12.98 + 2.16 6.21d mean 56.66 52.92 31.67 21.04 12.50 6.51 * Weighted mean calculated by GLIM. Means followed by different letter are significantly different (P< 01, t-test) (figures . are mean of six replicates). Analysis of deviance by GLIM source M. dev. mean F-ratio deviance dev. Stage 4 172.8 43.20 29.19** Dens. 5 694.7 138.94 93.87** Dens. x stage 20 28.8 1.44 0.97 Residual 150 222.7 1.48 Total 179 1119.0 ** (P< 01) . - 218 - Table 32. Percentage of parasitism by four species of Encarsia on six densities of Banisia tabaci (Temp. - 25 + 1°C; R.H. 75 + 5%; L: 0 16:8) Host density Species 4 8 16 32 64 128 mean+ s. e. mean* E. formosa 57.55 51.63 39.36 26.88 13.49 7.12 32.67 + 3.72 15.50a E. deserts 45.00 32.50 27.08 13.54 9.32 4.47 21.99 + 2.83 9.83c E. cibcensis 40.00 32.49 21.67 10.94 5.73 3.07 18.98 + 2.74 7.45d E. adrianae 56.66 52.92 31.67 21.04 12.50 6.51 30.21 + 3.81 13.74b * Weighted mean calculated by GLIM. Means followed by different letter are significantly different (P< 01, t-test). . - 219 - 4.2 Overall host mortality 4.2.1 Introduction Some groups of parasitoids cause host mortality through factors other than parasitism itself, which may have a significant influence on the dynamics of the host-parasitoid relationship. One of the most important of these factors is 'host-feeding' behaviour. Jervis & Kidd (1986) review and discuss the nature and diversity of host-feeding behaviour in hymenopteran parasitoids, based on information from literature. They state that this important characteristic of parasitoids has been largely ignored or neglected by workers on this field, particularly when models have been proposed to explain parasitoid foraging behaviour. Jervis & Kidd (1986) list more than 140 species, belonging to 17 hymenopteran families showing a host-feeding behaviour. They define four main types of host-feeding behaviour (1) concurrent, where the female parasitoid uses the same host individual for both feeding and oviposition, (2) non-concurrent, where different host individuals are used for feeding and oviposition (these two categories are not mutually exclusive), (3) destructive, where the host dies as a result of the parasitoid feeding and (4) non-destructive, where the host survives the feeding encounter. Non-destructive feeding may be either concurrent or non-concurrent, whereas destructive feeding is usually non-concurrent. - 220 - Another habit of some parasitoids that may kill a number of hosts, is known as 'host-mutilation'. This term was first used by Flanders (1935) to describe the repeated puncturing of a host by a parasitoid without any attempt to oviposit or ingest body fluids. Bartlett (1964) defined host-mutilation as frustrated host-feeding in which the host does not bleed freely. It might also occur as a result of a frustrated attempt to oviposit in an unsuitable host. Nell et al. (1976) defined rejection after 'ovipositorial test' as a component of the normal oviposition behaviour sequence of Encarsia formosa on its natural host Trialeurodes vaporariorum. The importance of this habit and its impact on the host population has not yet been completly investigated. Van Lenteren, Nell & Sevenster-van der Lelie (1980) found that the percentage of rejections of different stages of T. vaporariorum after ovipositorial test by E. formosa varies strongly, being rare in first and second nymphal instars and relatively more frequent in the other instars. It has been found for some parasitoid species that host-feeding can have an effect on host population reduction as great as, or greater than the parasitism habit, for instance DeBach (1943) reported that adult females of Metaphycus helvolus (Compere) (Hymenoptera: Encyrtidae) kill the black scale Saissetia oleae (Bernard) (Homoptera: Coccidae) by parasitism, by mutilation and by host-feeding. He reported that about one-quarter of mortality in field tests was by parasitism, and the rest mainly by host-feeding. Mortality due to host-feeding was also related to the size of the host, decreasing from small to medium size scales, and increasing - 221 - with large size scales. Another example is given by DeBach & Sundby (1963) who reported a larger number of scales killed by Aphytis fisheri DeBach (Hymenoptera: Aphelinidae) by host-feeding than the number killed by parasitism. Burnett (1962) and Nechols & Tauber (1977a) studied mortality in T. vaporariorum caused by E. formosa and found significant differences between the percentages of mortality due to parasitism and total mortality. Nell et al. (1976) pointed out that host-feeding never occurred in parasitized hosts, and hosts used for feeding were never parasitized afterwards. Furthermore, all the immature stages of the whitefly were used for host-feeding, but third and fourth nymphal instars and 'prepupa' were less used than the second instar and the pupa. Burnett (1962) found that the percentage of T. vaporariorum nymphs that died unparasitized increased with increasing E. Formosa density and decreased with increasing size of the host instar. Nechols & Tauber (1977a), considering only mortality resulting from causes other than parasitism in the same host-parasitoid relation- ship, found that percentages of host mortality decreased as host age (size) increased from the first to the 'early' fourth instar, and were significantly greater in the first instar than in any of the rest. The present section deals with the total mortality of Bemisia tabaci immature stages, caused by E. Formosa, E. deserti, E. cibcensis and E. adrianae, resulting not only from successful - 222 - parasitism but also from other causes (e. g. 'host-feeding', 'ovipositorial test', other unexplained deaths) that can be attributed to the action of the parasitoid foraging behaviour. 4.2.2 Materials and methods The overall mortality of B. tabaci due to the four species of parasitoids was calculated using data obtained from the experiments on 'functional responses' (Appendix 2). Total mortality is given by the number of hosts parasitized (Na) plus the number of hosts killed by other causes (Nhd), and percentage of mortality was calculated from this number and the total number of hosts exposed to the parasitoids. Percentages of mortality due to parasitism were calculated as well. As mentioned in Section 4.1.2 a control treatment was included to record the unexposed whitefly mortality. Data were analysed using analysis of variance (ANOVA), and means separated by the least significant difference (LSD) test. 11.2.3 Results and discussion Taking into account results from feeding and oviposition behaviour of the species of Encarsia studied (Section 3.5.2) and following Jervis & Kidd's (1986) classification of host feeding behaviour in hymenopteran parasitoids, E. Formosa, E. deserti, E. cibeensis and E. adrianae may be classified as non-concurrent - 223 - destructive host-feeding, and killing host by ovipositor piercing either with feeding or without feeding or oviposition. Results given in Tables 33 and 34 show conclusively that mortality in unexposed host treatment (control Table 33) for all five whitefly stages was considerably less than in the whitefly exposed to any of the parasitoid species. Percentages of host mortality show the following trends: in the control treatment, the first instar nymphs showed significantly higher mortality than any of other stages which were not significan- tly different from each other and showed a mean percentage of mortality similar to that recorded earlier in the present work (Table 8,14.28 + 3.18%) in the study of B. tabaci biology on bean plants. There were no significant differences in the overall mortality (i. e. parasitism plus other mortality) between host stages within parasitoid species for E. deserti and E. eibeensis whereas total mortality was significantly less in the pupal stage than in the preceding stages when the whitefly was exposed to E. Formosa and E. adrianae. The lack of significant difference in overall mortality between most stages of host attacked within each parasitoid species, suggests that the overall activity of the wasps killing hosts is more or less constant during a given amount of time, irrespective of the host stage, compared with the differences found in percentages of parasitism between host stages, this suggests that in stages where levels of parasitism are less, total mortality is compensated by an - 224 - a w " a a a A ýO O N o M N N N L C O +1 +1 f1 f1 f1 M f N N A M a: H a Ö N A MAI N 'D N f 1(1 f N _ qL O fI fI "I fI +I 9 9 N P IO f UO ad WI N M f M a a a e A w u N f : n f f f f M O N "O M 'O CD O 1ý O f M U1 N N N O O O 19 S. Y N f0 1. O 1: Ö Ö C S a b M Oý 4 N M M Y f M N 1. M U p Wý N N U UI N O IC f N f f M K f1 fI "I fI +I f M 1- M 1ý a. U' M N f M f M M M f O .+ N w Y O Y 40 N O A 01 Y N N - - - M N Y N O a i N a CI ß+N1 - CI V i Y H N f " N v m fý ýý "ý "1 +1 C v a v YI a J w N Wý N INý1 N O MI L Y 'e V W = " S na A" N" Me 0 f N f " f ry 0 VmV Y M N 'O f P r" "4 Y N OO N 1. vi Y f f t f M Dn te M4 Y eY iC e Y" UVYN O " 1. 'O " VL ä°J S. ÖÖ Y M A f M ýL f N - - N NM !N NC VVV u "1 YLL VO OM ÖY "L CIIUI. 19 YCM O N S. N N n1 L"Y iY G O fý f1 f1 f1 +1 KM º Y9 f 1 N »LY V "F C ä f :g 4: °' OaVV Zb" WI CYML e +1 M N M N VS "N N i++1 f YI N M M1 N » "g a^ s O' OVYp M N A b YC ýE A M b YI b N M NYY-f eý LrrO ºONr O"VLM» 4 r"r6 9 A A V L L M A Y Y "LYYY A »YNNLO NOD M N M M M N C 6 T r f(O0V Y C OOOO «NN N p Y M C DL Y r L MNNMM ' D 4D ýF N M ý 6 ftOYO - 225 - increase in mortality due to other factors (e. g. host feeding and ovipositorial test). The differences between total mortality and mortality caused by parasitism (host parasitized) were so great in all cases that statistical test is not necessary. These differences are shown for each parasitoid and each host stage in Table 33 (columns C). The percentages of mortality decreased from the less preferred to the most preferred stages for parasitism which suggests a preference for host-feeding (inverse to preference for parasitism) on first and second nymphal instars and pupal stage. This seems likely to contribute to the explanation of the parasitoid's problem of how to allocate its feeding and oviposition bouts in field conditions where all stages of the host can be found in the same patch. Table 34 shows the percentages of total mortality of B. tabaci caused by the four species of parasitoids as well as mortality in unexposed populations; total percentages of parasitism for each species are also given. Overall host mortality caused by E. formosa was significantly greater than that caused by any of the other three species and there was no significant difference between them. Results in this section and observations from parasitoid biology (Section 3.5.2), indicate that host-feeding behaviour may be considered as an important factor of host mortality after parasitism in these four species of Encarsia, and that this habit affects the host stages in an inverse way to parasitism, and its effect on host population dynamics should be investigated in more detail. - 226 - Table 34. Percentages of mortality of Bemisia tabaci due to four species of Encarsia -R. (Temp. = 25 +1 H. _ 75 + 5%; L: D = 16: 8) % overall % host % mortality Species mortality parasitized other than parasitism E. formosa 55.4 + 5.1a 32.7 + 3.7a 22.7 E. deserti 41.5 + 4.6b 21.9 + 2.8c 19.6 E. cibcensis 38.1 + 4.6b 18.9 + 2.7d 19.2 E. adrianae 44.3 + Z. 7b 30.2 + 3.8b 14.1 Control 15.1 + 2.4c ------ (x + s. e. ) six replicates, six densities and five stages (n = 180) Means in columns followed by different letters are significantly different (P<. 01; LSD test) - 227 - Z" 3 Survival of the parasitoid progeny " 3.1 Introduction "In seeking natural enemies, and parasitoids in particular, for use in biological control programmes, high searching efficiency is only one ingredient for a successful agent, and could be completely negated if the parasitoid progeny themselves suffer high levels of mortality" Hassell (1982). Any mortality factor affecting the parasitoid progeny will have the effect equivalent to reducing searching efficiency and hence affect the 'overall parasitoid performance' (Hassell & Moran 1976) Clearly there are many factors affecting the survival of parasitoid progeny under field conditions, biotic factors such as natural enemies (hyperparasitoids, predators, diseases) and abiotio factors such as climatic conditions. It has been found that the success or failure of most biological control programmes has been due to the identification or disregard of some of those important factors, Hassell & Moran (1976) cited some examples. Identification of those factors and detailed studies of their effects can be conducted only under natural conditions. On the other hand intrinsic factors in the host-parasitoid relationship such as the host's defensive system may affect parasitoid progeny as much as the mentioned mortality factors (Bouletreau 1986). Such factors may be studied in more detail and their effects better measured under laboratory conditions. - 228 - The present section deals with mortality of parasitoid progeny during the pupal stage, and measures successful parasitism as the number of adults produced per female. 4.3.2 Material and methods The number of wasps emerging was recorded in the functional response experiments as well as the number of parasitoids dying during the pupal stage (Appendix 2 Npe, Npd). These data were used in the analysis of survival of the parasitoid progeny. It is clear that this progeny is the result of a female laying only female eggs during a limited amount of time (24 h) rather over than the parasitoid lifetime. Only data from third and fourth host nymphal instars (preferred stages) were analysed. Percentage of survival was calculated based on the number of wasps emerged related to number of hosts parasitized. 3.3 " Results and discussion Table 35 shows the average number of wasps produced per female of each of the four species of parasitoid during a fixed period of 24 h ovipositing on third and fourth nymphal instars of B. tabaci. Statistical analysis showed significant differences in the number of progeny produced by the species, E. formosa and E. adrianae having a greater number of descendants than E. deserti and E. cibeensis. - 229 - Percentages of survival (Table 35) show that E. cibeensis and E. adrianae suffered less mortality than E. formosa and E. deserti during the pupal stage. This suggests a better adaptation of the two former species to their natural host B. tabaci, than E. formosa and E. deserti which came originally from different hosts in the field. In these experiments all the progeny were females and potentially capable of attacking hosts and laying eggs, but this is not expected to happen under natural conditions. The fact that species are 'heteronomus hyperparasitoids' is very important in an assessment of their 'overall performance' in host depression. E. formosa is a uniparental species and, as was stated earlier, males are rare under normal conditions, but the other three species are biparentals, and sex ratio and the way males develop (hyperparasitically on their own females) are crucial factors that should be taken into account in any comparison between these species. - 230 - Table 35. Progeny produced and percentage of survival per female of four species of Encarsia parasitizing third and fourth nymphal instars of Bemisia tabaci, during an exposure time of 24 h (Temp. = 25 + 10C; R. H. = 75 + 5%; L: D = 16: 8) Species Host Progeny % parasitized produced survival n x + s. e. x+s. e. E. formosa 72 8.40 + 0.47 7.54 + 0.45a 89.76 E. deserti 72 5.13 + 0.19 4.58 + 0.28b 89.27 E. cibeensis 72 3.58 + 0.12 3.58 + 0.27o 100 E. adrianae 72 7.47 + 0.40 7.17 + 0.48a 95.72 n= number of females Means followed by different letter are significantly different (P<. 01; LSD test) - 231 - CHAPTER 5 EFFECT OF THE HOST PLANT ON LEVELS OF PARASITISM 5.1 Introduction Of the plants attacked by Bemisia tabaci, cotton is the crop in to which by far the greatest effort has been put in studying the host-plant relationship, and perhaps the only one in which plant resistance has been studied to a significant degree, although varieties of several other crops such as tomato (Berlinger, Dahan & Shevach-Urkin 1983), beans (Gamez 1971), potato (Abdel-Salam et al. 1972), cassava (Lal & Hrishi 1981) and soyabean (Mansour, Gouhar & Guirguis 1974, Rossetto et al. 1977) have been screened for incidence of B. tabaci. It is generally agreed that hairy varieties of cotton and other crop plants are more heavily attacked by B. tabaci than the glabrous varieties. This has been attributed to factors such as more sheltered conditions in the hairy leaved varieties and a greater willingness of adults to fly from glabrous leaved plants, as well as differences in the action of predators or parasitoids and competition from other pests between the two types of plant (Mound 1965, Sippell, Bindra & Khalifa 1983). On the other hand, it has been reported that in tomatoes glandular leaf hairs trap and kill many adults of the whitefly, especially ovipositing females, with high numbers of adults being trapped and killed on hairy varieties and none being trapped on the glabrous varieties (Kisha 1984). - 232 - It has also been suggested that the host searching efficiency of parasitoids of aleyrodids is reduced on hairy host plants. Studies have been conducted in attempts to prove this and some other related hypotheses in the relationship of Encarsia formosa with its host Trialeurodes vaporariorum (van Lenteren et al. 1967,1977, Hulspas-Jodaan & van Lenteren 1978, Lizhao-Hua et al. 1987). It has been stated that the host-searching behaviour of E. formosa on a leaf is random (van Lenteren et al. 1976); differences have been found in the control of T. vaporariorumwith E. formosa on various greenhouse crops, sudeess being reported for such crops as tomatoes and paprika, but failure for others, such as cucumber (Parr & Stacey 1975, Woets 1978). The failure has been attributed to different factors, all related to the structure of the leaf of the host plant (van Lenteren et al. 1977). Hulspas-Jordaan & van Lenteren (1978) found significant differences in walking speed of the wasps on leaves of hairy and hairless plants, the walking speed being inversely proportional to the leaf hairiness. Findings of Lizhao-Hua et al. (1987) confirm previous results on the relationship between walking speed of E. formosa and leaf hairiness in two cultivars of cucumber, but they found no significant differences in the percentages of host contacted between the two types of leaf, also the walking pattern of the wasp did not differ on the two types of leaves. The present experiments were set up in an attempt to find out whether or not there are differences in the levels of parasitism of B. tabaci by the four species of parasitoids studied here: (1) - 233 - between parasitoid species on each of four host plants and (2) between host plants by each of four parasitoid species. 5.2 Materials and methods The host plants tested were three crop plants, beans, tomatoes and cotton, on which B. tabaci is a serious pest, and lantana (Lantana camara), a common weed throughout the tropics and frequent host of the whitefly.. The host and the parasitoids obtained from stock cultures were kept under the enviromental conditions described in Section 2.2.1. The required number of whitefly nymphs was obtained on the leaves of the different host plants as described on Section u. 2. 'Leaf cages' were used to confine the wasps with the host (see Figure 26). The experiments were conducted in the same way as experiments in Chapter 4. About 60 third and fourth instar whitefly nymphs were exposed to a young mated female (except E. formosa) in each arena for 24 h, and replicated 12 times on each of the four host plants. This density was chosen based on results of the functional response experiments. The number of hosts parasitized was recorded 10 to 14 days after exposure. - 234 - Data were analysed by an one-way ANOVA, and means separated using the LSD test. 5.3 Results and discussion Results are shown in Table 35; they indicate that despite some numerical differences, there are few statistical differences between species in levels of parasitism on each of the four host plants. E. formosa was the species with the highest levels of parasitism in the four different host plants, and was significantly different from the other three species on cotton, tomato and lantana, but not on bean plants where it was not significantly different from E. adrianae (LSD in columns in Table 36). In the comparison of levels of parasitism between host plants within each parasitoid species (Table 36), E. cibcensis and E. adrianae showed no significant differences. E. Formosa and E. deserti presented significantly greater numbers of parasitized nymphs of the whitefly when the host plant was cotton, whereas the levels of parasitism were not significantly different on the other three species of host plant. Differences in levels of parasitism between parasitoid species on the same species of host plant seem to be due to biological characteristics of the parasitoid species, fecundity may be the main one. - 235 - The general lack of significant differences between levels of parasitism on different host plants within each parasitoid species, despite clear differences in leaf shape and hairiness (e. g. between bean and tomato leaves), suggests that under these controlled conditions the host plant has low influence on the levels of parasitism of these species. It is clear that influence could be distorted by the experimental conditions, due to the wasps' being arrested on the host plant leaves for a relatively long period (24 h) which does not occur in nature where the wasps can freely fly away after landing on an unacceptable leaf. However differences between the mean number of nymphs of B. tabaci parasitized by each parasitoid species on different host-plants, in some cases as much as twice from one plant to other, suggest that the species behave differently on different host-plants under laboratory conditions, which indicates the importance of taken in consideration the host-plant of the whitefly when working in laboratory conditions with these species. - 236 - a w 0 4) c0 A cu cd co v v v v ..-I Pý a cdoo f11 M [ t- ON v co ON O 4.3 a 'c co C) N O O 0 4., u co +1 +1 +I +1 0 .. ] l- M M !- 02 M a) DC ýD N Lf1 Lfl 0 4) aß C) !Z ma a Ln C) 4.3 C) +1 A . -1 vcu vt1 vcd vai V! O o t- a as w cd 4 p a '. D ON .-.0 00 u 0 W 1.n wC) 0 oa .o 4.) N "- ' "- b aßä O +1 +I +1 +1 v N U rl CC) M N N .NU O a) : C' .. -10 Co ý 0 U1 ý C of N OC +I N a Ul% w N 4-& O N D Cu Cu ri O L, II v.0 v v v a Cd J3 wo 9s +-1 - 00.0 co 0 01 00 _-:r y) w 4) a) NC o ý" 0 O +4 Q) 0.4 v 43 Cu O C) G) llým +3 C Q O L. G) Cd ý. O to 4) N U " r4 "" 43 L V) p L M-4 43 N wi 0 4) +4 V U 44 V U cc p, 4r OX H a) +Iýýfd+A12 WI WI WI WI v 2 Q) c" - 237 - CHAPTER 6 GENERAL DISCUSSION AND CONCLUSIONS The cotton whitefly Bemisia tabaci is considered a serious problem in the production of food and fibre throughout the tropical and subtropical regions of the world. Its importance as a pest is enhanced by its wide distribution and the diversity of cultivated, weed and wild plants attacked. Worldwide distribution and some crops on which B. tabaci is a serious pest are given in Tables 2 and 4. The importance of B. tabaci as an economic pest has increased considerably in some countries such as India, Pakistan, Sudan, Israel and USA (California) during the last decade. Several explanations have been suggested (Butler, Henneberry & Hutchison 1986), including development of resistance to insecticides, reduction of competition as a result of the control of other pests, increase of whitefly fecundity and egg viability as a result of the effect of insecticides on the physiology of the plants, and reduction of the impact of natural mortality factors, mainly the action of parasitoids and predators. The role of natural enemies in the control of B. tabaei has been discussed widely; natural enemies have sometimes been considered to contribute significantly to the depression of the pest population, other times their effect has been considered to be insignificant. - 238 - Up to 28 species of parasitoids and 29 species of predators (Tables 5 and 6) have been reported attacking B. tabaci worldwide. Among the former, Encarsia lutea and Eretmocerus mundus have been studied in some detail. Encarsia formosa is one of the most intensively studied whitefly parasitoids, but all the studies have been conducted on its relationship with its natural host Trialeurodes vaporariorum. As stated by Ohnesorge (1984), only a thorough study of the life history, ecology, behaviour and pest-parasitoid interactions can reveal the causes of failure of biologic.,, -a1 control attempts and indicate the possibilities for more efficient biological control of B. tabaci. Waage & Hassell (1982), in a review of parasitoids as biological control agents, stated that theoretical studies have identified by mathematical modelling searching efficiency, fecundity, larval survival, sex ratio, and interference and spatial heterogeneity as key contributors to the depression of host equilibria and/or to the stability of the interactions. These considerations were basically taken into account in the present study in an attempt to identify, and gain knowledge of species of parasitoids as potential control agents for B. tabaci. The first phase of this study was concerned with the biology and morphology of the cotton whitefly and its life cycle on five different host plants, under controlled conditions. It showed that - 239 - five well defined immature stages can be recognized between egg and adult emergence of B. tabaci. They were called: first, second, third and fourth nymphal instars and pupal stage. No 'transitional' or 'prepupal' stages were recognized. The host plant was shown to have significant influence on the developmental duration of the different whitefly immature stages, as well as on the total duration of the life cycle. It seems that the differences are mainly due to a physiological interaction between the host plant and the whitefly immature stages. Significant differences were also found in the survival of the immature stages on different host plants. Mortality of the immature stages on lantana and cotton was three and a half to four times higher than on bean plants, on which the immature stages suffered the lowest mortality of the five host plants tested. It is clear that these differences are very important in field conditions and should be taken into account when working with different crops and planning a population management method for B. tabaci. From a theoretical point of view, the host plant on which the whitefly develops should be considered when formulating predictive life table models. These considerations are also very important, and perhaps more relevant, when working under laboratory conditions and planning experiments including other live organisms (different trophic levels of biophages) and in particular when working with parasitoids. For example, selecting the host plant on which the insect develops faster and less mortality occurs. - 240 - A general conclusion of this phase of the work is that the biology of the pest and the host plant on which the insect develops, and their interactions, should be taken into consideration and determined under specific conditions when basic studies of parasitoids are undertaken. The second phase of this investigation deals with comparative studies on biology and morphology of the selected parasitoid species as well as their interrelation with the whitefly. Field searches for B. tabaci parasitoids were conducted in Pakistan and Israel, and parasitized whitefly nymphs were sent to Silwood Park (Ascot, England) where adults of different species of parasitoids were obtained, screened and reared for at least one generation before being discarded or accepted for the investigation. The following parasitoid species were reared from Pakistan (Rawalpindi), Encarsia lutea, Encarsia sp. A, Encarsia sp. B, Encarsia sp. C, Eretmocerus mundus; from Israel, Encarsia lutea, E. deserti and Eretmocerus mundus. Following the screening of the species, Encarsia sp. A and Encarsia sp. B and E. deserti were selected for this study, and E. formosa, obtained from GCRI in England, was included. Encarsia species A and B were described as E. eiboensis and E. adrianae (Appendix 1). - 241 - The four species of parasitoids are 'facultative autoparasi- toids', E. formosa is uniparental (thelytokous), and the other three species are biparental (arrhenotokous), this being perhaps one of the most important characteristics that confers certain advantage to E. formosa compared with the others, as a biological control agent. The general characteristics of development were similar for the four species of parasitoids, consisting of the egg stage, three larval instars, a prepupal substage, a pupal stage and the adult. Some morphological differences were found during the larval stages, as well in the pupal stage, between males and females, and the pupal cases left after adult emergence allow separation of pupae of E. formosa and E. deserti from pupae of E. cibeensis and E. adrianae, and, in some particular cases, to tell whether the emergent female (see Section 3.2.2 Figure 12). wasp was a or a male , The developmental duration E. formosa and E. adrianae was significantly longer than that of the other two species, and that of E. cibeensis was the shortest. Findings in this investigation showed, for the four species of parasitoids, that all nymphal stages and the pupa of B. tabaci were successfully parasitized, but the rate of development increased as eggs were laid in later stages and the total duration of the developmental period was significantly shorter when eggs were laid in third and fourth nymphal instars and pupal stage than in first and second nymphal instars. - 242 - Considering the developmental period to be specific, and a short one to be a good biological characteristic, the short developmental period of E. cibcensis may be regarded as a good trait, since it confers to this species the shortest 'mean length of a generation' (T) which contributes to increase in the intrinsic rate of growth of the population (Section 3.8). Adult longevity also seems a specific characteristic, and in synovigenic species such as Encarsia spp. a longer longevity means a longer 'life time fecundity', which may be a desirable biological characteristic, since combined with a high fecundity it contributes to the increase of the 'net reproductive rate' (Ro). The results of this study showed significant differences in longevity between species (Table 19). E. adrianae was the longest lived species and E. cibeensis the shortest. There was no significant difference in longevity between E. Formosa and E. deserti, which may be due to the fact that they are very closely related species (Gerling 1967). The results from fecundity studies (Section 3.6.2) corroborate previous findings by van Vianen & van Lenteren (1982, 1986b) on the number of ovarioles of E. formosa, which this study showed to vary from six to 17. Results suggested a positive correlation between the number of ovarioles and number of mature eggs as well as the body size of the wasp. E. deserti also showed a variable number of ovarioles, but with a very small variation, from six to eight, whereas E. cibcensis and E. adrianae showed a fixed number of six ovarioles. This character might give certain - 243 - biological advantages to the former two species, and in particular to E. formosa. Fecundity, oogenesis, and oviposition behaviour studies showed that E. formosa has a greater fecundity than the other three species. Very low levels of superparasitism by the four species while depositing female eggs suggest avoidance of superparasitism, this may be explained by females being able to distinguish primary parasitized hosts from unparasitized hosts. However, relatively high levels of superparasitism by E. adrianae while depositing male eggs (Table 12) suggest that this ability changes, and that wasps are not able to discriminate between secondary parasitized and unparasitized hosts. Batches of eggs are laid daily in a relatively short time, and long periods are spent resting, preening, walking and feeding, possibly while a new batch of eggs is being prepared. Long periods of isolation of females produce a gradual decrease in the number of mature eggs in ovarioles, whereas contact with the host might produce a gradual increase in egg production, to its maximum. This suggests that host-feeding has a very important effect on egg production. Comparing the thelytokous reproductive strategy of E. formosa to the arrhenotokous strategy of the other three species, E. formosa has theoretically the advantages of not having to produce males, and that a single individual can colonize a local habitat; whereas E. deserts, E. cibeensis, and E. adrianae have to produce males according to a specific strategy, and at least one couple is necesary to initiate a local colonization. Although not exhaustive, studies on sex ratio were conducted in the present investigation, results from some experiments (Section 3.7) showed for the biparental - 244 - species a fluctuating cyclical female biased sex ratio in cultures, suggesting that sex ratio changes in relation to the available type of host, increasing the proportion of males with the availability of secondary hosts. Two theories are suggested from results of this investigation, in relation to the sex allocation strategy of the three biparental species in field conditions. First, that the species take advantage of the differential rate of development of females from eggs laid in different stages of development of the host. According to this theory females develop faster from eggs laid in later host stages, and lay male eggs in their younger sisters (or cousins) which are still developing from eggs laid in young nymphal stages in the same host patch. The second theory, suggested by the experiments on sex ratio, supposes that males are produced by females hyperparasitizing their daughters (or nieces), by spending long periods (several days) in the same host patches, or coming back to them some time after the first parasitism, when secondary hosts are available for hyperparasitism. Regarding all biological studies of the four species of parasitoid, in the present investigation a general conclusion is that each species shows a combination of different values for its biological traits, e. g. whereas E. formosa showed the highest fecundity but the longest developmental period, E. oibeensis showed the opposite values, the shortest developmental period and the lowest fecundity, and E. adrianae showed advantage in adult longevity over the other three species. However it is clear that values of these biological characters can vary with the insect host, the stage of the - 245 - host and environmental conditions. Studies on the effect of the host stage and host density on levels of parasitism showed that second, third and fourth nymphal instars of B. tabaci are more efficiently attacked by E. formosa and E. adrianae, and third and fourth instars by E. deserti and E. cibcensis. The higher parasitism in these stages may be interpreted as a preference of the parasitoids for them. Analysis of the estimated parameters in the functional response studies showed in general a similar pattern for the four species of parasitoids, characterized by a shorter handling time on the preferred host stages (third and fourth nymphal instars) than on the less preferred stages, and the longest estimated handling time for the pupal stage. Fransen & Montford (1987) found the same handling time for E. 'formosa parasitizing four different stages of Trialeurodes vaporariorum and concluded that differences in functional response in that particular case cannot be attributed to this parameter. Higher estimated searching efficiency was also found for these parasitoids parasitizing third and fourth nymphal instars than the first and second nymphal instars and pupal stage. The parameters were estimated from experiments with a relatively short period of exposure (24 h) and the estimated handling time comprises time spent in other activities (walking, searching, feeding, preening and resting); results from direct observation showed real handling time as much as 70 times shorter than the estimated. Thus, differences in estimated handling time between host stages within parasitoid species are likely to be due to differences - 246 - in time spent in other activities rather than in real handling time. Longer estimated handling time in the less preferred stages may be attributed to time spent in searching and handling hosts that are rejected without parasitism, due to a possibly physiological unsuitability or physical resistance to the ovipositor penetration. Differences in estimated handling time between species of parasitoids parasitizing the same host stage may be attributed to biological traits (e. g. egg limitation = longer periods resting) rather than to actual handling time. This was confirmed by the very little variation in values of the real handling time (Table 27) between parasitoid species. The highest value for searching efficiency was obtained for E. cibeensis parasitizing the third nymphal instar, and suggests that this species could be more efficient than the others at low host densities. " Despite the 'predatory habit' (host-feeding and host- mutilation) of some parasitoids that has been mentioned since early this century (Howard 1910), and suggested as an important factor in host mortality (Johnston 1915), its role as a contributor to the depression of host populations has been largely ignored by workers on hymenopteran parasitoids, particularly in theoretical models (Jervis & Kidd 1986). The predatory habit seems to have particular importance in Aphelinidae species such as Encarsia spp. Mortality of immature stages of B. tabaoi attributable to predation by the four species of Encarsia was recorded and evaluated - 247 - during the present study. Results showed that total mortality in the treatments was in all cases much greater than mortality caused by parasitism (Table 32), and suggested that differences may be attributed to the host-feeding habit of the females of all four species of parasitoids. Thus, the predatory behaviour of Encarsia spp. is a significant contributor to the total host mortality, and therefore has an important effect in the depression of the host population. Results also suggested that these parasitoids have a particular strategy when they allocate their feeding and oviposition bouts, using more intensively the youngest and oldest host stages (first, and second nymphal instars and pupal stage) for feeding, and the intermediate ones (third and fourth nymphal instars) for parasitism. This strategy and behaviour should be taken into consideration when formulating models on overall efficiency of these parasitoid species. Percentage mortality in the pupal stage of E. formosa and E. deserti was greater than in E. adrianae, there was almost no pupal mortality in E. cibeensis. These differences were explained as a better adaptation of E. cibeensis and E. adrianae to B. tabaci, but much more investigation is necessary on this aspect, including mortality of the progeny during the egg and larval stages as well as in both sexes. Despite the advantage of E. formosa in fecundity and its thelytokous reproductive strategy, the lack of significant difference found in the rate of natural increase of the population of the four species of parasitoids, suggests that the other three species, and particularly the two new species, have the same potential growth of - 248 - their population which makes them promising biological control agents of the whitefly. Finally, the host plant was shown to have a significant effect on levels of parasitism by E. formosa and E. deserti but not by E. cibcensis and E. adrianae. In general, the mean number of hosts parasitized on different host plants suggested some differences in the efficiency of attack of the parasitoids on them. It was suggested from these experiments that the main effect of the host plant could be distorted by the experimental conditions. Based on all the biological characteristics of the species of Encarsia studied and evaluated in this investigation, and considering that the species showed a combination of values in the parameters measured, and taking into account that recent evolutionary theory has shown that much of the variability in traits and pattern of the parasitoids is adapt Ave (Waage & Hassell 1982), this study suggests that E. cibeensis and E. adrianae are promising agents for the control of Bemisia tabaci, and that studies should continue on these two species, particularly the latter. They should be evaluated in field experiments. - 249- APPENDIX 1 Bull. ent. Res. 77,425-430 425 Published 1987 Two new species of Encarsia Foerster (Hymenoptera: Aphelinidae) from Pakistan, associated with the cotton whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) A. LOPEZ-AVILAs Imperial College, Silwood Park, Ascot, Berks, SL5 7PY, UK Abstract The aphelinids Encarsia adrianae sp. n. and E. cibcensis sp. n. are described from material in culture ex Bemisia tabaci (Gennadius) on beans at the C"A"B International Institute of Biological Control, Ascot, UK. They are descendants of material collected in Rawalpindi, Pakistan, from B. tabaci on Lantana camara. Introduction Bemisia tabaci (Gennadius) is an important whitefly pest of tropical field crops (Lopez-Avila & Cock, 1986). It supports a large complex of parasitoids, all of the family Aphelinidae (Hymenoptera), the principal genera being Encarsia and Eretmocerus. Two new species of Encarsia are described from Pakistan, near the supposed centre of origin of B. tabaci ; they are currently under study as potential control agents of this pest at the C"A"B International Institute of Biological Control (CIBC), Silwood Park, Ascot, UK. Encarsia adrianae sp. n. Female. Length 0.52-0.76 mm (. ± s.e. = 0.66 ± 0.010 mm, na 30, holotype 0.75 mm). Head and thorax light brown to ochre; abdomen uniformly bright yellow to whitish; antennae and legs yellow; eyes yellow and ocelli reddish. Head: width 0.28 mm; ocelli forming an isosceles triangle; distance between posterior ocelli about equal to distance between posterior ocellus and eye (0.043 mm); posterior ocellar line present and dark in colour. Frontovertex with fine setae and finely transversely lineolate-reticulate. Eyes finely setose (Fig. 1); maxillary and labial palpi one-segmented; long funicle four- mandibles with three teeth. Antenna (Fig. 2) with pedicel as as F2; segmented with Fl distinctly shorter than F2 (15:20), F2, F3 and F4 equal in length (20); club two-segmented as long as the scape with the basal segment as long as F4 and the apical segment longer than the basal (25:20). Segments of flagellum with 2-4 linear sensilla except Fl which has two papillary sensilla on the distal end, one dorsal and one ventral and no linear sensilla (Fig. 3); other flagellar segments with one papillary sensillum on the distal-dorsal side, except the apical segment which has the sensillum pre-apical. Papillary sensilla clavate in shape (Fig. 4). * The author is working temporarily in UK. His permanent address is: Instituto Colombiano Agropecuario, A. A. 151123Eldorado, Bogotd. Colombia. - 250 - Cont. Appendix 1 426 A. LOPEZ-AVILA j ;} ý r'. 1: ý,ý , ý. t. .,, ^ý+ý ý+` ,rte ýý (ý it ý`ý Lý 8ý 9; 2, 9; 3. first Figs 1-9. -Encarsia adrianae sp. n.; 1, head and thorax, antenna, and second funicular segments (Fl, F2); 4, papillary sensillum; 5, forewing; 6, strigil of the foreleg; 7, mid-tibial spur and basitarsus; 8, ovipositor; 9, antenna, d. Thorax (Fig. 1): mesoscutum with five pairs (4 +2+2+ 2) of setae, parapsis with four small setae, each axilla with one seta, scutellum with two pairs of setae and each tegula with one seta. Mesoscutum, scutellum and axillae reticulate, with polygonal cells and parapsis lineolate; mesoscutum trapezoidal and scutellum ellipsoidal. Metanotum and propodeum arcuated and transversely striated with two setae near each spiracle. Forewing (Fig. 5): 2.5 times as long as broad, with a row of very short setae on the costal cell; submarginal vein with two setae and marginal vein with seven setae; disc area uniformly setose: longest cilia of marginal fringe about one-quarter of width of disc. I lind wing nine times as long as wide, with longest cilia of marginal fringe slightly longer than wing width. Tarsi five-segmented; foretibial spur as in other species. arcuate and forming a strigil with an oblique row of spines on the inner aspect of the basitarsus (Fig. 6); mid-tibial spur (Fig. 7) slightly more than one-third as long as the corresponding basitarsus (10:27). - 251 - Cont. Appendix 1 ENCARS(A SPP. ATTACKING BEMISfA TABACI 427 Gaster ovate, longer than thorax (30:25); abdominal tergites II and III reticulate laterally and dark in colour; tergites III-VII reticulate laterally, bearing 2-4 strong setae on the reticulated area; tergite VIII bearing the spiracles on sides, with a small dark area around each one, and two setae between them. Ovipositor apparently originating between abdominal segments VI and VII, slightly shorter than mid-tibia (70:74) and extending beyond the apex of the gaster by about 0.038 mm (Fig. 8). Male. Length 0.57-0.66 mm (z ± s.e. = 0.62 ± 0.01 mm, n= 17). Similar to female except in body colour, structure of antenna and sex characters. Body dark brown with pronotum, axillae, tegulae, front part of mesoscutum, coxae and gaster largely dark brown to black; head, legs and antennae light brown, eyes red. Mesoscutum with four pairs of setae (4 +2+ 2). Antenna (Fig. 9) with six flagellar segments, the sixth partially fused with the fifth, funicular segments approximately equal in length, bearing 3-6 linear sensilla on each flagellar segment. including Fl, and one papillary sensillum in a dorso-distal aspect of each flagellar segment: club two-segmented with apical segment shorter than basal segment (19:23). Copulatory organ apparently originating between sixth and seventh abdominal segments, slightly longer than the middle tibia (68: 62). Material examined. Holotype 9 and 69 paratypes on a slide, mounted in Berlese fluid. Further paratypes, 9 9,3 d' on a second slide mounted in Berlese fluid. Deposited in the British Museum (Natural History) (BMNH). This species was described from specimens in culture ex B. tabaci on beans at CIBC, Silwood Park, Ascot, UK. They are descendants of material collected by Dr A. I. Mohyuddin at Rawalpindi, Pakistan, from B. tabaci on Lantana camara (iv. 1985). E. adrianae belongs to the coryli group (Viggiani, 1981). Morphologically it is very near to E. coryli Viggiani (G. Viggiani, pers. comm. ), but differs from the description given by Viggiani (1981) in the colour pattern of both sexes and the number of setae on the female mesoscutum. Specimens of this species were determined in 1986 by Dr G. Viggiani (Institute of Agricultural Entomology, University of Naples, Italy) as an undescribed species. E. adrianae is biparental. and males develop as hyperparasitoids of immature females of their own species or other Encarsia species, such as E. formosa Gahan, E. deserti Gerling & Rivnay and E. cibcensis sp. n. (heteronomous hyperparasitoids (Walter, 1983)). The species is named in memory of the author's beloved niece, who passed away at the age of 17, while this species was being described. Encarsia cibcensis sp. n. Female. Length 0.52-0.68 mm (z ± s.e. = 0.57 ± 0.01 mm, n- 20, holotype 0.60 mm). Body, antennae and legs bright yellow; eyes and ocelli red in colour, Head: Eyes finely setose. Mandibles well developed with three teeth, maxillary palpi and labial palpi one-segmented. Ocelli very close to each other, distance between posterior ocellus and eye about eight times the distance between posterior ocelli; posterior ocellar line present but not very conspicuous. Antennal radicle slightly less than three times as long as wide (14:5), scape slightly longer than four times the width in the widest part (33:8); pedicel as long as F2 and longitudinally lineolate (Fig. 10); funicle three-segmented, Fl distinctly shorter than F2 (8: 14) and as long as wide; F2 distinctly shorter than F3 (14:20); club apparently three-segmented, with the basal segment as long as F3 and apical segment slightly longer than the basal (23:20), bearing one papillary sensillum in a dorso-distal position on each segment. Funicular segments Fl, F2 and F3 (Fig. 10) bearing one, two and three papillary sensilla, respectively; flagellar segments bearing 1-3 linear sensilla, except Fl has none. The papillary sensilla clavate in shape. Thorax: (Fig. 11) mesoscutum with eight setae (4 +2+ 2), scutellum with two pairs (2 + 2) of setae, parapsis with two setae, axillae and tegulae with one seta on each. Mesoscutum, scutum and axillae reticulate with polygonal cells and parapsis lineolate. Forewing (Fig. 12) 3.3 times as long as broad with a row of short setae on the costal cell: - 252 - Cont. Appendix 1 428 nI OPE?-AVII A submarginal and marginal veins hearing two and seven long setae, respectively: disc setose with two glabrous areas in the anterior and posterior margin as in figure: longest cilia of marginal fringe slightly longer than half width of disc. I lind wine ten times as long it,, wirk, with longest cilia of marginal fringe twice as long as width of wing. 'I arsi tie e-segmented: forelegs with strigil consisting of an arcuate, bifid tibial spur and an oblique rovN of shines on inner aspect of the basitarsus (Fig. 13): mid-tibial spur two-thirds as long, as the corresponding basitarsus (Fig. 14). Gaster ovate. longer than thorax (115: 71)), tergites III-VI reticulate on sides. hearing one seta on the reticulated area, seventh tergite hearing four strong setae. and eighth tercite bearing the spiracles and two strong setae between them. Ovipositor apharentls originating between abdominal segments VI and V11. sliehtls exsertcd, longer than mididflc tibia ('7: 6(1). ý`. lý% ýF . IU. d Fie, I-P, --tcauNia ih, ois o sI, n, Qntr[n; tC. : ýII]II )III it ; iitJ It uh ,' dorsal ttrtý. 7: 12. lurr%ktnc: 13. Strl, `il of the Iurrlci, outer %irt%; 14. rnul-tibial %I ui Mid h. uu. u u 15. tunic! c. d; 16, third funicular segment (F3), outer side. 17, third tunliul: u segment, Inner side, I?, papillary sensillum, i. Male. Ditfers from the female mainly in structure of the antennae and eoluut. Rods length 0.50-0.611 nom (k = s. e. = (I. 55 i (1.1101)nun. II =- I5). Antenna( scape somewhat less than four tines a, long as sidle 129:, Sl. hearing a %rnu: ii row of 4-5 setae: pedicel as in female: funicle ttit ee se mented. 1,1 slight Is loneci than wide ( 13: 10) and bearing tour linear sensilla, three hahill: u\ sensilla on the rnnet si k ant( F2 in numerous setae (Fig. 15): similar size and shape to 1I but hearrne mu (meat srn, ill, i on the outer side and a series of six papillary sensilla on the inner stir: I. (little r1r`Itnius in this species. the biggest segment of the antenna. sontessh: tt harrel-shapedl. heartnc deer linear (Fig. l0). immer h\ sensilla on the outer side the side cosc, rd .4ýr os it papillarn - 253 - Cont. Appendix 1 F. VCARSIA SPP ATT'AC'KING P(; MISIA 'T'ARA(/ 421) sensilla (21-23 sensilla) (Fig. 17): club apparently three-segmented but not well defined, with the basal segment twice as long as wide, apical segment smaller than the basal one, all club segments bearing 3-5 linear sensilla. All flagellar segments covered by numerous setae. The papillary sensilla on the inner side of the male antenna are different in shape from those on the female antenna. they are curved (Fig. 18). Colour: antennae, legs, head and body in ventral view yellows: pronotum, axillae and garter in dorsal view dark brown: mesoscutum yellow with the anterior region dark brown: parapsis and scutellum entirely yellow: metanotum and propodeum yellow in the middle and dark brown on the sides: eyes and ocelli red. Copulatory organ typical for the genus and apparently originating in the eighth abdominal segment and shorter than the middle tibia (511:60). Material examined. Holotype Y and 4Y paratypes, on it slide, mounted in Berlesc fluid. Further paratvpes: 8 d' on a second slide, also mounted in Berlese fluid. Deposited in the BMNH. This species was described from males and females from culture ex 11. tabaci on beans at CIBC, Silwood Park, Ascot, UK. They are descendants of material collected by Dr A. I. Mohvuddin at Rawalpindi, Pakistan. from B. tabaci on L. samara (iv. 1985). E. cibcensis belongs to the lutea group (Viggiani & Mauone, 1979). Specimens of this species were determined by Dr B. R. Subba Rao (C-A. 13 International Institute of Entomology, London (CIE)) as an undescribed species. The species differs from F. lutea (Masi) and E. asterohemisiae Viggiani & Mazzone mainly in body coloration in both sexes, setal pattern on the disc and the conformation of the male antenna (Viggiani & Mazzone, 1980: Viggiani, 1981). E. cihcensi. s is biparental. and males develop as hyperparasitoids of immature female stages of their own species or other Encarsia species, such as F. f rniosu. E. desern and 1:. adrianae (heteronomous hvperparasitoids (Walter, 1983)). The new species is named for the C"A"B Institute of Biological Control (('IRC). Comments. Previous papers describing Encarsia species do not mention the papillary sensilla described herein for both species. The sensilla are particularly evident on the male antennae of E. cihcensi. s. The author believes this is the same sensorial complex which Viggiani (1980) described from the antennae of some species of Encarsia of the linen group, and that these structures will he important new elements in the hiosvstematics of this genus. as mentioned by Viggiani (198(t). This sensorial complex is important to precopulatorv courtship behaviour. Acknowledgements The author is grateful to Dr I. A. Mohvuddin (CIBC, Rawalpindi, Pakistan) who forwarded the initial material to establish the cultures Silwood Park, Dr I. K. Waage, at . Dr M. J. W. Cock, Mrs A. II. Greathead (CIBC, Silwood Park), Dr H. R. Subba Rao (CIE), T. Williams and S. Raveendranath (Imperial College, Silwuod Park) for reading the manuscript and providing comments, Dr G. Viggiani (Institute of Agricultural Entomology, University of Naples) for determining one of the species, R. Ilartle\ College, (Imperial South Kensington) for his help with the scanning election microscopy, the Instituto Colombiano Agropecuario for financial support and CIRC for use of the facilities at Silwood Park. References LOPE7-AV! A. & COCA, M. J. W. (1980). Economic damage. LA. --hp iI ' lot ('oik, NI \1 ' (Ed. ). Bemisia literature .1 tahati--a some on the cotton wwhuetIN %kith in ; utn Gated bibliograph%. Ascot. UK, (' A 13 International -121 pp. Institute ,I Jiloioi iul (ontml VtGGIANI, G. Nuoxi (19811). compiesoi seas oriali solle anlehne di !n ar trl oast (11c111 Aphetinidae). (. Lab. Em. Filippo Silvestri 37, -Bo! agr. _'7-311. - 254 - Cont. Appendix 1 430 A. LOPEZ"AVILA VIGGIANI, G. (1981). Afelinidi parassiti di Asterobemisia avellanae (Signoret) (Ilomoptera Aleyrodidae), con descrizione di una nuova specie.-Boll. Lab. Ent. agr. Filippo Silvestri 38, 67-72. VIGGIANI, G. & MAZZONE, P. (1979). Contributi alla conoscenza morfo-biologica delle specie del Encarsia Foerster-Prospaltella complesso Ashmead (Hym. Aphclinidac). -Boll. Lab. Ent. agr. Filippo Silvestri 36.42-50. VIGGIANI,G. & MAZZONE,P. (1980). Le specie paleartiche di Encarsia del gruppo lurea Masi (Ilym. Aphelinidae), con descrizione di due nuove specie.-Boll. Lab. Ent. agr. Filippo Silvestri 37, 51-57. WALTER,G. H. (1983). Divergent male ontogenies in Aphelinidae (Ilymenoptera: Chalcidoidea): a simplified classification and suggested evolutionary sequence.-Biol. J. Linnean Soc. Lond. 19,63-82. (Received 10 November 1986) © C"A"B International, 1987 255 APPENDIX2 Experimental results of effect of host density on levels of parasitism (Data from functional response experiments) Key: Re = Replicate Nt = Host density Nhe = Number of hosts (whiteflies) emerged Nhd = Number of hosts dead from causes other than parasitism Na = Number of hosts parasitized Npe = Number of parasitoids (wasps) emerged Npd = Number of parasitoid pupae failing to emerge a. Encarsia formosa First instar Second instar He Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 0 0 4 3 1 4 1 0 3 3 0 8 1 4 3 3 0 8 1 1 6 4 2 16 7 3 6 6 0 16 9 2 5 4 1 32 8 12 12 11 1 32 18 4 10 9 1 64 26 33 5 5 0 64 54 2 8 8 0 128 70 40 18 17 1 128 112 7 9 9 0 2 4 0 3 1 1 0 2 4 0 1 3 3 0 8 1 3 4 4 0 8 0 2 6 6 0 16 0 7 9 9 0 16 1 0 15 15 0 32 4 18 10 10 0 32 17 9 6 6 0 64 28 29 7 4 3 64 35 16 13 13 0 128 98 18 12 11 1 128 117 7 4 4 0 3 4 0 4 0 0 0 3 4 1 2 1 1 0 8 2 6 2 2 0 8 3 0 1 1 0 16 5 9 2 0 2 16 4 0 12 12 0 32 10 11 11 10 1 32 17 3 12 10 2 64 31 25 8 6 2 64 41 10 13 12 1 128 88 27 13 13 0 128 102 16 10 9 1 4 4 0 4 0 0 0 4 4 0 2 2 2 0 8 1 5 2 1 1 8 2 2 4 4 0 16 4 11 1 0 1 16 4 6 6 6 0 32 7 20 5 4 1 32 15 5 12 12 0 64 33 18 13 9 4 64 43 7 14 12 2 128 112 10 6 4 2 128 108 8 12 12 0 5 4 0 0 4 3 1 5 4 0 0 4 4 0 8 3 5 0 0 0 8 1 3 4 4 0 16 4 4 8 7 1 16 2 5 9 8 1 32 14 10 8 7 1 32 7 16 9 6 3 64 6 55 3 3 0 64 46 9 9 9 0 128 81 38 9 4 5 128 73 39 16 16 0 6 4 0 3 1 1 0 6 4 0 1 3 3 0 8 7 1 0 0 0 8 0 0 8 8 0 16 4 12 0 0 0 16 4 3 9 9 0 32 13 11 8 8 0 32 21 4 7 7 0 64 40 13 11 10 1 64 45 7 12 10 2 128 88 29 11 9 2 128 102 17 9 9 0 - 256 - Cont. Appendix 2a Third instar Fourth instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 0 0 4 4 0 4 0 0 4 4 0 8 1 0 7 7 0 8 1 1 6 4 2 16 6 2 8 8 0 16 8 2 6 5 1 32 15 3 14 12 2 32 20 5 7 6 1 64 51 4 9 8 1 64 52 3 9 8 1 128 107 11 10 8 2 128 113 2 13 11 2 2 4 0 0 4 4 0 2 4 0 2 2 1 1 8 0 1 7 7 0 8 1 3 4 4 0 16 3 4 9 9 0 16 2 6 8 8 0 32 19 2 11 11 0 32 18 5 9 7 2 64 36 16 12 10 2 64 45 6 13 10 3 128 108 10 10 10 0 128 96 23 9 9 0 3 4 1 0 3 3 0 3 4 1 0 3 3 0 8 0 2 6 5 1 8 0 1 7 7 0 16 1 5 10 10 0 16 7 6 3 1 2 32 2 11 19 17 2 32 21 2 9 7 2 64 38 12 14 13 1 64 51 4 9 9 0 128 66 55 7 6 1 128 108 9 11 9 2 4 4 0 0 4 4 0 4 4 0 0 4 4 0 8 0 3 5 4 1 8 1 0 7 7 0 16 1 2 13 12 1 16 4 6 6 4 2 32 6 13 13 13 0 32 27 0 5 3 2 64 37 11 16 16 0 64 38 18 8 8 0 128 111 11 6 4 0 128 100 20 8 6 2 5 4 2 0 2 2 0 5 4 0 0 4 3 1 8 0 0 8 8 0 8 1 2 5 4 1 16 9 12 5 5 0 16 4 0 12 10 2 32 20 4 8 7 1 32 20 0 12 11 1 64 43 13 8 6 2 64 40 16 8 7 1 128 102 15 11 10 1 128 91 23 14 13 1 6 4 1 1 2 2 0 6 4 0 1 3 3 0 8 1 1 6 6 0 8 0 0 8 8 0 16 8 2 6 5 1 16 3 0 13 10 3 32 23 1 8 8 0 32 10 6 16 13 3 64 45 1 18 17 1 64 52 3 9 8 1 128 105 14 9 8 1 128 102 7 19 19 0 - 257 - Cont. Appendix 2a b. Fhcarsia deserti pupa First ins tar He Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 2 1 1 1 0 1 4 4 0 0 0 0 8 3 2 3 2 1 8 2 4 2 1 1 16 10 4 2 2 0 16 8 3 5 3 3 32 26 4 2 2 0 32 28 3 1 1 0 64 48 14 2 1 1 64 58 4 2 2 0 128 112 14 2 2 0 128 116 4 8 6 2 2 4 3 0 1 1 0 2 4 1 3 0 0 0 8 6 1 1 1 0 8 2 5 1 1 0 16 8 8 0 0 0 16 13 1 2 1 1 32 23 6 3 3 0 32 10 18 4 2 2 64 58 6 0 0 0 64 52 9 3 1 2 128 116 6 6 5 1 128 81 37 10 6 4 3 4 1 3 0 0 0 3 4 0 2 2 2 0 8 3 4 1 1 0 8 5 2 1 1 0 16 9 3 4 3 1 16 8 2 6 4 2 32 22 8 2 2 0 32 24 6 4 4 0 64 56 7 1 1 0 64 44 12 8 4 4 128 115 9 4 4 0 128 104 19 5 4 1 4 4 2 2 0 0 0 4 4 1 3 0 0 0 8 5 3 0 0 0 8 5 1 2 0 2 16 9 6 1 1 0 16 12 1 3 2 1 32 30 2 0 0 0 32 15 10 7 7 0 64 39 20 5 5 0 64 50 9 5 4 1 128 114 11 3 3 0 128 128 24 2 2 0 5 4 3 1 0 0 0 5 4 0 3 1 1 0 8 2 5 1 1 0 8 5 2 1 0 1 16 10 5 1 1 0 16 5 7 4 4 0 32 21 5 6 5 1 32 23 9 0 0 0 64 52 12 0 0 0 64 51 8 5 4 1 128 110 16 2 2 0 128 101 17 10 7 3 6 4 2 0 2 2 0 6 4 1 2 1 1 0 8 5 1 2 2 0 8 4 2 2 2 0 16 12 4 0 0 o 16 8 6 2 0 2 32 22 6 4 1 3 32 8 15 9 7 2 64 59 3 2 2 0 64 50 10 4 4 0 128 108 20 0 0 0 128 99 25 4 2 2 - 258 - Cont. Appendix 2b Second instar Third instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 4 0 0 0 0 4 1 0 3 3 0 8 0 4+ 4+ 4 0 8 3 3 2 2 0 16 12 1 3 3 0 16 5 5 6 6 0 32 19 13 0 0 0 32 24 5 3 2 1 614 58 5 1 1 0 64 44 12 8 7 1 8 128 109 16 3 3 0 128 119 0 7 1 2 4 0 2 2 2 0 2 4 2 0 2 2 0 8 4 2 2 2 0 8 0 4 4 4 0 16 13 0 3 1 2 16 10 0 6 4 2 32 21 0 11 11 0 32 18 9 5 5 0 64 49 6 9 9 0 64 52 6 6 4 2 128 102 17 9 6 3 128 104 16 8 8 0 3 4 0 2 2 1 1 3 4 1 0 3 3 0 8 3 5 0 0 0 8 3 0 5 3 2 16 3 10 3 2 1 16 9 1 6 5 1 32 16 12 4 44 0 32 25 2 5 5 0 64 58 3 3 3 0 64 51 8 5 5 0 128 99 26 3 3 0 128 105 13 10 10 0 4 4 0 1 3 3 0 4 4 1 1 2 2 0 8 5 3 0 0 0 8 3 0 5 4 1 16 10 0 6 4 2 16 8 1 7 5 2 32 23 6 3 3 0 32 16 8 8 8 0 64 55 7 2 2 0 64 54 0 10 9 1 128 121 7 1 1 0 128 109 12 7 7 0 5 4 0 3 1 0 1 5 4 0 0 4 4 0 8 6 1 1 0 1 8 1 3 4 4 0 16 14 2 0 0 0 16 8 0 8 7 1 32 17 10 5 5 0 32 25 0 7 5 2 64 41 11 12 9 3 64 52 2 5 4 1 128 120 1 7 7 0 128 103 22 3 3 0 6 4 0 3 1 1 0 6 4 1 0 3 3 0 8 0 5 3 3 0 8 3 0 5 5 0 16 9 5 2 1 1 16 12 0 4 3 1 32 17 8 7 6 1 32 22 5 5 3 2 64 50 9 5 5 0 64 47 9 8 8 0 128 116 3 9 7 2 128 96 25 7 5 2 - 259 - Cont. Appendix 2b Fourth instar Pupa Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 0 0 4 4 0 1 4 2 1 1 0 1 8 0 4 4 4 0 8 1 4 3 3 0 16 5 8 3 2 2 16 5 7 4 2 2 32 24 6 2 2 0 32 30 2 0 0 0 64 46 4 14 14 0 64 54 1 9 8 1 128 110 11 7 7 0 128 124 4 0 0 0 2 4 1 2 1 1 0 2 4 4 0 0 0 0 8 4 1 3 3 0 8 7 1 0 0 0 16 5 7 4 3 1 16 8 5 3 2 1 32 20 9 3 3 0 32 22 9 1 1 0 64 37 22 5 5 0 64 54 9 1 1 0 128 108 12 8 8 0 128 123 0 6 6 0 3 4 1 0 3 3 0 3 4 0 3 1 0 1 8 0 3 5 4 1 8 3 2 3 3 0 16 7 1 8 8 0 16 4 7 5 1 4 32 25 2 5 5 0 32 28 3 1 1 0 64 48 8 8 7 1 64 49 8 7 6 1 128 80 44 4 1 3 128 108 16 4 3 1 4 4 1 0 3 3 0 4 1 0 3 3 0 8 3 0 5 5 0 8 5 2 1 1 0 16 9 3 4 4 0 16 6 6 4 4 0 32 14 12 6 6 0 32 28 0 4 1 3 64 53 3 8 4 4 64 27 29 8 7 1 128 120 4 4 4 0 128 114 10 4 2 2 5 4 2 0 2 2 0 5 4 2 0 2 1 1 8 1 1 6 4 2 8 3 3 2 2 0 16 10 0 6 6 0 16 11 2 3 3 0 32 11 18 3 2 1 32 22 5 5 5 0 64 56 4 4 4 0 64 53 6 3 3 0 128 107 21 0 0 0 128 114 6 8 7 1 6 4 1 0 3 3 0 6 4 3 0 1 1 0 8 7 1 0 0 0 8 5 1 2 2 0 16 4 3 9 9 0 16 7 8 1 1 0 32 23 1 8 8 0 32 17 11 4 3 1 64 51 7 6 4 2 64 59 0 5 5 0 128 110 14 4 4 0 128 115 4 9 6 3 - 260 - Cont. Appendix 2 c. Encarsia cibcensis First instar Second instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 3 1 0 0 0 4 3 1 0 0 0 8 6 2 0 0 0 8 3 2 3 3 0 16 5 9 2 2 0 16 13 2 1 1 0 32 15 8 9 9 0 32 18 8 6 5 1 64 49 10 5 5 0 64 54 8 2 2 0 128 85 39 4 4 0 128 108 11 9 8 1 2 4 0 2 2 1 1 2 4 0 2 2 2 0 8 4 2 2 1 1 8 5 3 0 0 0 16 3 6 7 7 0 16 10 0 6 6 0 32 16 14 2 1 1 32 27 3 2 2 0 64 32 26 6 6 0 64 40 22 2 2 0 128 110 14 4 4 0 128 78 48 2 2 0 3 4 1 2 1 1 0 3 4 0 3 1 1 0 8 7 0 1 1 0 8 8 0 0 0 0 16 10 2 4 4 0 16 10 1 5 5 0 32 13 15 4 4 0 32 30 2 0 0 0 64 43 20 1 1 0 64 31 29 4 4 0 128 103 18 7 7 0 128 116 4 8 8 0 4 4 2 0 2 2 0 4 4 0 2 2 2 0 8 2 3 3 3 0 8 0 2 6 6 0 16 1 11 4 4 0 16 13 3 0 0 0 32 17 12 3 3 0 32 30 2 0 0 0 64 49 10 5 5 0 64 54 7 3 3 0 128 105 19 4 4 0 128 109 11 8 8 0 5 4 3 1 0 0 0 5 4 4 0 0 0 0 8 1 0 7 7 0 8 5 3 0 0 0 16 3 11 2 2 0 16 12 3 1 1 0 32 23 5 4 4 0 32 28 4 0 0 0 64 55 7 2 2 0 64 59 1 4 4 0 128 78 47 3 3 0 128 119 9 0 0 0 6 4 4 0 0 0 0 6 4 1 0 3 3 0 8 2 6 0 0 0 8 0 0 8 8 0 16 9 4 3 3 0 16 8 3 5 5 0 32 12 18 2 2 0 32 22 4 6 6 0 64 47 14 3 3 0 64 59 0 6 6 0 128 121 3 4 3 1 128 121 7 1 1 0 - 261 - Cont. Appendix 2c Third instar Fourth instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 0 0 4 4 0 4 1 0 3 3 0 8 2 1 5 5 0 8 4 4 0 0 0 16 6 6 4 4 0 16 13 3 0 0 0 32 19 7 6 6 0 32 18 6 8 8 0 64 42 16 6 6 0 64 54 6 4 4 0 128 110 14 4 4 0 128 119 7 2 2 0 2 4 4 0 0 0 0 2 4 2 0 2 2 0 8 3 2 3 3 0 8 5 3 0 0 0 16 7 5 4 4 0 16 10 1 5 5 0 32 26 2 4 4 0 32 25 5 2 2 0 64 45 15 4 4 0 64 56 4 4 4 0 128 114 7 7 7 0 128 107 16 5 5 0 3 4 1 0 3 3 0 3 4 3 0 1 1 0 8 2 2 4 4 0 8 3 0 5 5 0 16 12 3 1 1 0 16 7 4 5 5 0 32 28 1 3 3 0 32 23 4 5 5 0 64 42 18 4 4 0 64 55 8 1 1 0 128 114 11 3 3 0 128 112 12 4 4 0 4 4 0 2 2 2 0 4 4 1 1 2 2 0 8 4 2 2 2 0 8 4 4 0 0 0 16 9 5 2 2 0 16 8 3 5 5 0 32 20 7 5 5 0 32 27 1 4 4 0 64 54 7 3 3 0 64 59 0 5 5 0 128 114 9 5 5 0 128 126 2 0 0 0 5 4 2 0 2 2 0 5 4 2 0 2 2 0 8 1 1 6 6 0 8 3 1 4 4 0 16 4 5 7 7 0 16 13 3 0 0 0 32 31 1 0 0 0 32 24 0 8 8 0 64 55 7 2 2 1 64 53 3 8 8 0 128 113 10 5 5 0 128 120 1 7 7 0 6 4 0 1 3 3 0 6 4 0 0 4 4 0 8 5 2 1 1 0 8 3 0 5 5 0 16 5 6 5 5 0 16 8 0 8 8 0 32 26 5 1 1 0 32 32 0 0 0 0 64 52 11 1 1 0 64 55 0 9 9 0 128 93 29 7 7 0 128 116 9 3 3 0 - 262 - Cont. Appendix 2c d. Encarsia adrianae pupa First instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 1 4 2 1 1 1 0 1 4 3 1 0 0 0 8 4 3 1 1 0 8 3 0 5 5 0 16 14 0 2 1 1 16 4 5 7 7 0 32 27 2 3 3 0 32 26 3 3 2 1 64 55 7 2 2 0 64 34 13 17 16 1 128 116 10 2 2 0 128 106 18 4 4 0 2 4 0 3 1 1 0 2 4 0 2 2 2 0 8 6 0 2 2 0 8 2 2 4 4 0 16 11 3 2 2 0 16 9 0 8 7 1 32 22 7 3 2 1 32 22 6 4 4 0 64 46 15 3 3 0 64 51 11 2 1 1 128 120 6 2 2 0 128 112 10 6 6 0 3 4 4 0 0 0 0 3 4 2 1 1 1 0 8 3 3 2 2 0 8 5 1 2 2 0 16 2 6 8 3 5 16 15 1 0 0 0 32 18 8 6 6 0 32 25 1 6 6 0 64 47 16 1 1 0 64 52 8 4 4 0 128 108 19 1 1 0 128 115 13 0 0 0 4 4 2 0 2 2 0 4 4 0 1 3 2 1 8 3 0 5 4 1 8 3 4 1 1 0 16 12 2 2 2 0 16 11 1 4 4 0 32 19 9 4 4 0 32 24 3 5 5 0 64 45 18 1 1 0 64 53 5 6 6 0 128 107 20 1 1 0 128 93 25 10 10 0 5 4 3 0 1 1 0 5 4 3 1 0 0 0 8 5 2 1 1 0 8 4 1 3 3 0 16 9 3 4 3 1 16 10 3 3 3 0 32 24 4 4 2 2 32 19 5 8 8 0 64 52 7 5 5 0 64 50 7 7 6 1 128 97 27 4 4 0 128 101 22 5 2 3 6 4 2 0 2 2 0 6 4 0 2 2 2 0 8 5 1 2 2 0 8 5 2 1 1 0 16 14 2 0 0 0 16 10 2 4 3 1 32 25 6 1 1 0 32 20 5 7 5 2 64 40 20 4 4 0 64 45 11 8 6 2 128 114 12 2 2 0 128 106 17 5 2 3 - 263 - Cont. Appendix 2d Second instar Third instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 0 1 3 3 0 4 0 1 3 3 0 8 3 0 5 5 0 8 0 3 5 5 0 16 4 3 9 9 0 16 4 5 7 7 0 32 18 6 8 6 2 32 16 9 7 7 0 64 41 17 10 8 2 64 54 4 6 6 0 128 108 11 9 6 3 128 88 30 10 9 1 2 4 2 1 1 1 0 2 4 0 0 4 4 0 8 3 1 4 4 0 8 0 3 5 5 0 16 6 4 6 6 0 16 9 2 5 4 1 32 20 6 6 4 2 32 21 5 6 5 1 64 41 5 18 18 0 64 42 12 10 10 0 128 104 14 10 10 0 128 78 32 18 18 0 3 4 o 0 4 4 0 3 4 0 0 4 4 0 8 0 1 7 5 2 8 0 0 8 8 0 16 10 1 5 5 0 16 4 5 7 4 3 32 14 10 8 8 0 32 13 8 11 11 0 64 50 6 8 8 0 64 33 9 22 22 0 128 73 49 6 6 0 128 66 48 14 13 1 4 4 0 0 4 0 u 4 1 0 3 3 0 .4 8 0 0 8 7 1 8 1 0 7 7 0 16 10 0 6 6 0 16 10 0 6 6 0 32 22 4 6 6 0 32 24 2 6 6 0 64 54 0 15 13 2 64 52 2 10 10 0 128 108 5 15 15 0 128 87 29 12 11 1 5 4 2 0 2 0 0 5 4 0 0 4 4 0 8 3 1 4 0 4 8 2 0 6 5 1 16 10 1 5 3 3 16 4 0 12 11 1 32 17 3 12 11 1 32 13 5 14 14 0 64 45 13 6 6 0 64 40 7 17 16 1 128 107 5 16 14 2 128 110 4 14 11 3 6 4 0 1 3 3 0 6 4 2 0 2 2 0 8 3 0 5 5 0 8 2 0 6 6 0 16 10 2 4 3 1 16 10 0 6 6 0 32 19 3 10 10 0 32 18 0 14 14 0 64 24 35 5 5 0 64 50 0 18 17 1 128 112 0 18 17 1 128 98 17 13 13 0 - 264 - Cont. Appendix 2d Fourth instar Pupa Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 1 4 2 0 2 2 0 1 41 1 1 2 2 0 8 2 2 4 3 1 8 4 2 2 2 0 16 5 7 4 4 0 16 9 5 2 2 0 32 25 4+ 3 3 0 32 22 7 3 3 0 64 53 4 7 7 0 64 56 6 2 2 0 128 98 23 7 6 1 128 114 10 4 3 1 2 4 0 1 3 3 0 2 4 4 0 0 0 0 8 2 1 5 5 0 8 5 1 2 2 0 16 10 0 6 6 0 16 9 3 4 4 0 32 17 7 8 8 0 32 24 4 4 4 0 64 53 7 4 3 1 64 53 5 6 5 0 128 109 15 4 4 0 128 110 10 8 8 0 3 4 1 0 3 3 0 3 4 3 1 0 0 0 8 1 1 6 6 0 8 6 2 0 0 0 16 11 0 5 5 0 16 14 2 0 0 0 32 20 4 8 6 2 32 26 6 0 0 0 64 38 22 4 4 0 64 56 8 2 2 0 128 112 6 10 9 1 128 108 18 2 2 0 4 4 2 0 2 2 0 4 4 2 0 2 2 0 8 1 1 6 6 0 8 2 4 2 2 0 16 5 5 6 6 0 16 13 0 3 3 0 32 19 6 7 7 0 32 28 0 4 4 0 64 48 4 12 11 1 64 58 2 4 4 0 128 78 42 8 8 0 128 116 9 3 3 0 5 4 0 0 4 4 0 5 4 4 0 0 0 0 8 1 3 4 4 0 8 7 1 0 0 0 16 8 2 6 6 0 16 10 3 3 3 0 32 24 0 8 8 0 32 30 0 2 2 0 64 51 5 8 8 0 64 59 0 5 4 1 128 99 16 13 13 0 128 97 28 3 3 0 6 4 0 1 3 3 0 6 4 2 1 1 1 0 8 1 0 7 7 0 8 5 2 1 1 0 16 6 3 7 7 0 16 12 3 1 1 0 32 14 12 6 6 0 32 26 2 4 4 0 64 42 14 8 7 1 64 60 1 3 3 0 128 102 19 7 7 0 128 102 24 2 2 0 - 265 - Cont. Appendix 2 e. Control First instar Second instar Npd Re Nt Nhe Nhd Na Npe Npd Re Nt. Nhe Nhd Na Npe 4 4 0--- 4 3 1--- 8 4 4--- 8 7 1--- 16 11 5--- 16 13 3--- 32 26 6--- 32 27 5--- 64 55 9--- 64 60 4--- 128 123 1--- 128 114 14 --- 2 4 2 2--- 2 4 3 1--- 8 7 1--- 8 5 3--- 4--- 16 13 3--- 16 12 32 27 5--- 32 30 2--- 64 64 0--- 64 52 12 --- 128 115 13 128 110 18 ------4 3 4 1 3--- 3 4 0--- 8 7 1--- 8 5 3--- 4--- 16 14 2--- 16 12 32 27 5--- 32 29 3--- 64 57 7--- 64 59 5--- 128 121 7--- 128 96 32 --- 4 4 3 1--- 4 4 3 1--- 8 6 2--- 8 7 1--- 16 12 4--- 16 13 3--- 32 28 4--- 32 27 5--- 64 63 1--- 64 59 6--- 128 113 15 128 105 23 ------4 5 4 2 2--- 5 4 0--- 8 6 2--- 8 5 3--- 4--- 16 15 1--- 16 11 32 19 13 32 31 1------64 51 13 64 43 21 ------128 116 12 --- 128 93 35 --- 6 4 1 3--- 6 4 4 0--- 8 6 2--- 8 8 0--- 16 13 3--- 16 14 2--- 32 32 0--- 32 30 2--- 64 45 19 64 53 11 ------128 108 20 128 99 29 ------266 - Cont. Appendix 2e Third star Fourth instar Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 4 1 3--- 1 4 4 0--- 8 7 1--- 8 8 0--- 16 15 1--- 16 16 0--- 32 27 5--- 32 22 10 --- 64 64 0--- 64 56 8--- 128 123 1--- 128 112 16 --- 2 u 4 0--- 2 4 3 1--- 8 8 0--- 8 8 0- -- 16 16 0--- 16 15 1--- 32 25 7--- 32 22 10 --- 64 55 9--- 64 45 19 --- 128 111 17 128 114 14 ------ 3 4 3 1--- 3 4 4 0--- 8 8 0--- 8 5 3--- 16 14 2--- 16 13 3--- 32 29 3--- 32 32 0--- 64 60 4--- 64 56 8--- 128 122 6--- 128 119 9--- 4 4 4 0--- 4 4 3 1--- 8 5 3--- 8 8 0--- 16 15 1--- 16 16 0--- 32 29 3--- 32 31 1--- 64 64 0--- 64 64 0--- 128 119 9--- 128 117 11 --- 5 4 4 0--- 5 4 3 1--- 8 6 2--- 8 6 2--- 16 15 1--- 16 11 5--- 32 24 8--- 32 31 1--- 64 63 1--- 64 57 7--- 128 106 22 128 117 11 ------ 6 4 2 2--- 6 4 4 0--- 8 7 1--- 8 8 0--- 16 14 2--- 16 15 1--- 32 28 4--- 32 31 1--- 64 60 4--- 64 47 17 --- 128 121 7--- 128 118 10 --- - 267 - Cont. Appendix 2e Pupa Re Nt Nhe Nhd Na Npe Npd Re Nt Nhe Nhd Na Npe Npd 1 4 3 1--- 44 3 1--- 8 8 0--- 8 8 0--- 16 14 2--- 16 16 0--- 32 26 6--- 32 29 3--- 64 58 6--- 64 59 5--- 128 125 3--- 128 91 37 --- 2 4 2 2--- 54 4 0--- 8 5 3--- 8 8 0--- 16 15 1--- 16 16 0--- 32 29 3--- 32 25 7--- 64+ 64+ 0--- 64 59 6--- 128 128 0--- 128 81 47 --- 3 4+ 3 1--- 64 3 1--- 8 8 0--- 8 6 2--- 16 16 0--- 16 14 2--- 32 29 3--- 32 28 4--- 64 59 5--- 64 48 16 --- 128 128 0--- 128 113 15 --- - 268 - APPENDIX3 Meannumber of hosts parasitized by four species of Encarsia on five stages and six densities of Benisia tabaci (x + s. e. figures are meanof six replicates) a. Encarsia formosa Host density Stage 48 16 32 64 128 first instar 1.67 + 0.76 1.83 + 0.65 4.33 + 1.56 9.00 + 1.03 7.83 + 1.51 11.50 + 1.64 second instar 2.67 + 0.42 4.83 + 0.98 9.33 + 1.52 9.33 + 1.02 11.50 + 0.99 10.00 + 1.61 third instar 3.17 + 0.40 6.50 + 0.43 8.50 + 1.18 12.17 + 1.70 12.83 + 1.60 8.83 + 0.79 fourth instar 3.33 + 0.33 6.16 + 0.60 8.00 + 1.57 9.67 + 1.58 9.33 + 0.76 12.33 + 1.62 pupa 0.67 + 0.33 1.33 + 0.42 1.33 + 0.61 2.83 + 0.83 1.67 + 0.76 2.83 + 0.83 b. Encarsia deserti Host density Stage 48 16 32 64 128 first instar 0.67 + 0.33 1.50 + 0.22 3.67 + 0.67 4.17 + 1.40 4.50 + 0.85 6.50 + 1.36 second instar 1.50 + 0.43 1.67 + 0.67 2.83 + 0.79 5.00 + 1.52 5.33 + 1.73 5.33 + 1.40 third instar 2.83 + 0.31 4.17 + 0.48 6.17 + 0.54 5.55 + 0.72 7.00 + 0.82 7.17 + 0.95 fourth instar 2.66 + 0.42 3.83 + 0.87 5.67 + 0.99 4.50 + 0.92 7.50 + 1.45 4.50 + 1.15 pupa 1.33 + 0.42 1.83 + 0.48 3.33 + 0.56 2.50 + 0.85 5.50 + 1.26 5.17 + 1.33 - 269 - Cont. Appendix 3 c. Encarsia cibcensis Host density Stage 48 16 32 64 128 first instar 0.83 + 0.40 2.17 + 1.08 3.67 + 0.76 4.00 + 1.06 3.67 + 0.80 4.33 + 0.56 second instar 1.33 + 0.49 2.83 + 1.42 3.00 + 1.06 2.33 + 1.20 4.50 + 0.88 4.67 + 1.67 third instar 2.33 + 0.55 3.50 + 0.76 3.83 + 0.87 3.16 + 0.95 3.33 + 0.71 5.16 + 0.65 fourth instar 2.33 + 0.42 2.33 + 1.05 3.83 + 1.30 4.50 + 1.31 5.17 + 1.19 3.50 + 0.99 pupa 1.67 + 0.31 2.17 + 0.60 3.00 + 1.13 3.50 + 0.67 2.57 + 0.57 2.00 + 0.44 d. Encarsia adrianae Host density Stage 48 16 32 64 128 first instar 1.33 + 0.40 2.67 + 1.08 4.33 + 0.76 5.50 + 1.06 7.33 + 0.80 5.00 + 0.56 second instar 2.67 + 0.49 5.50 + 1.42 5.83 + 1.06 8.33 + 1.20 10.33 + 0.88 12.33 + 1.67 third instar 3.50 + 0.55 6.17 + 0.76 7.17 + 0.87 9.67 + 0.95 13.83 + 0.71 13.50 + 0.65 fourth instar 2.83 + 0.42 5.33 + 1.05 5.67 + 1.30 6.67 + 1.31 7.17 + 1.19 8.17 + 0.99 pupa 0.83 + 0.31 1.67 + 0.60 2.17 + 1.13 2.83 + 0.67 3.67 + 0.57 3.67 + 0.44 - 270 - APPENDIX 4 Life and fertility tables and rate of growth of the population of four species of Encarsia a. average values of biological parameters (from tables in the text) E. formosa E. deserti E. ciboensis E. adrianae Developmental period (Table 11) 15.96 13.37 11.57 15.77 $ of survival 89.76 89.27 100 95.72 Adult longevity (Table 19) 21.62 22.64 17.41 23.50 Hosts parasitized (Table 35) 8.40 5.13 3.58 7.47 Progeny (Table 35) 7.54 4.58 3.58 7.17 Sex ratio (9 prop. ) (Table 24) 1.00 0.78 0.85 0.74 - 271 - Cont. Appendix 4 b. Life and fertility tables for Encarsia formosa and E. adrianae constructed using experimental data (Birch 1948, Southwood 1978) E. formosa E. adrianae x lX mX 1X mX 0- 16 0.90 immature 0.96 immature stages stages 17 0.90 10.64 0.96 3.82 18 0.90 10.64 0.96 3.82 19 0.90 10.64 0.96 3.82 20 0.90 16.31 0.96 4.97 21 0.90 16.31 0.96 4.97 22 0.90 16.31 0.96 4.97 23 0.90 3.86 0.85 4.92 24 0.90 3.86 0.85 4.92 25 0.90 3.86 0.85 4.92 26 0.64 6.73 0.85 5.33 27 0.61 6.73 0.85 5.33 28 0.6k 6.73 0.85 5.33 29 0.51 9.08 0.42 6.08 30 0.51 9.08 0.42 6.08 31 0.51 9.08 0.42 6.08 32 0.26 6.17 0.42 2.08 33 0.26 6.17 0.42 2.08 34 0.26 6.17 0.42 2.08 35 0.13 4.67 0.11 1.67 36 0.13 4.67 0.11 1.67 37 0.13 4.67 0.11 1.67 38 0.13 2.67 ------39 0.13 2.67 ------40 0.13 2.67 ------ E. formosa: E. adrianae: rm = 0.237 rm = 0.198 - 272 - Cont. Appendix 4 o. 18 E. formosa 16 14 12 10 8 6 x 4 }2 J F Q W 2468 10 12 14 16 18 20 22 24 U. 16 U LL 14 U W CL V) 12 w c7 < 10 8 5 4 2 2468 10 12 14 16 18 20 22 DAYS Figure 36. Age specific fertility (m ) of Encarsia formosa and E. adrianae; continuous line from experimental datä, dashed line estimated. The developmental period of 16 days for both species is not included. - 273 - Cont. Appendix 4 d. Life and fertility tables constructed using average values of the biological parameters from studies in biology of the four species of Encarsia E. formosa E. deserti E. cibcensis E. adrianae x lx 1x 1x 1x 0- 12 immature immature immature immature stages stages stages stages 13 ------1.00 ------14 ------1.00 ------15 ----- 0.89 1.00 ------16 ----- 0.89 1.00 17 0.90 0.89 1.00 0.96 18 0.90 0.89 1.00 0.96 19 0.90 0.89 1.00 0.96 20 0.90 0.89 0.96 0.96 21 0.90 0.89 0.96 0.96 22 0.90 0.89 0.92 0.96 23 0.90 0.89 0.92 0.96 24 0.89 0.88 0.88 0.96 25 0.89 0.88 0.88 0.96 26 0.89 0.88 0.71 0.96 27 0.89 0.88 0.71 0.96 28 0.89 0.85 0.55 0.96 29 0.89 0.85 0.55 0.96 30 0.85 0.83 0.41 0.95 31 0.85 0.83 0.41 0.95 32 0.73 0.70 0.27 0.91 33 0.73 0.70 0.27 0.91 34 0.61 0.48 0.17 0.84 35 0.61 0.48 0.17 0.84 36 0.50 0.36 0.06 0.72 37 0.50 0.36 ----- 0.72 38 0.43 0.29 ----- 0.56 39 0.43 0.29 ----- 0.56 40 0.30 0.19 ----- 0.44 41 0.30 0.19 ----- 0.44 42 0.14 0.10 ----- 0.29 43 0.14 0.10 ----- 0.29 44 0.08 0.05 ----- 0.07 45 0.08 0.05 ----- 0.07 46 0.02 0.03 ----- 0.02 47 0.02 0.03 ----- 48 0.02 0.02 ------49 ---- 0.02 ------50 ----- 0.01 ------ m 7.54 3.57 3.07 5.53 x r 0.209 0.192 0.223 0.196 m * age specific fertility estimated constant during the generation time. - 274 - APPENDIX 5 Partial derivatives of the functions with respect to the parameters a' and Th 1. 'Disc equation' (Holling 1959b) a' Tt Nt Ne = 1+ a' Th Nt Ne Nt a' (1 + a' Th Nt)2 % 2 Ne -(a' Nt) S Th (1 + a' Th Nt)2 2. 'Random attack equation' (Rogers 1972) Tt a' t Na }) =N[1- t1+ exp{ - a' Th Nt pt 1 Tt =1 S Na - at Nt }[ a' Th Nt (1 + a' Th Nt)-2 gal exp{ 1+ a' Th Nt -11 - (1 + a' Th N0 Na - a' }C a'2 Nt+ Th N )-2 -N t1+ exp{ tt a' Th a' Th Nt - 275 - BIBLIOGRAPHY ABDEL FATTAH, S. A. S., SHARAF,I. M. F. & EL SEBAE, A. (1983) Performance of flucythrinate (Cybolt) against a wide spectrum of agricultural pests in Egypt. Arab Journal of Plant Protection 1 (2), 74-78. ABDELRAHMAN,A. A. (1986) The potential of natural enemies of the cotton whitefly in Sudan Gezira. Insect Science and its Application 7, 69-73. ABU YAMAN, I. R. (1971) Outbreaks and records. FAO Plant Protection Bulletin 19 (6), 140-141. AGRAWAL, H. S., GUPTA, N. R. & VISHWAKARMA,S. (1979) Chemical control of yellow mosaic of moong. Pesticides 13 (5), 44-47. AHMAD, R. & MUZAFFAR, N. (1977) Studies on cotton pests and their natural enemies with reference to effects of three insecticides of different persistencies. Agriculture Pakistan 28,193-203. ANNO-NYAKO. F. O., VETTEN, H. J., ALLEN, D. J. & THOTTAPPILLY, G. (1983) The relation between cowpea golden mosaic and its vector Bemisia tabaci. Annals of Applied Biology 102,319-323. ANON. (1963) Pests & diseases number. Plant Protection Bulletin, New Delhi 11 (1-4) (1959), 70 pp. APPERT, J. (1967) Notes techniques sur les insects nuisibles aux cultures malagasy. Suite. Agronomie tropicale, Nogent-sur-Marne 22,504-552. ARAKAWA, R. (1982) Reproductive capacity and amount of host-feeding of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) Zeitschrift für Angewandte Entomologie 93,175-182. ARDITI, R. (1983) A unified model of the functional response of predators and parasitoids. Journal of Animal Ecology 52,293-303. von ARX, R., BATIIGÄRTNER, J. & DELUCCHI, V. (1983a) Developmental biology of Bemisia tabaci (Genn. ) (Sternorrhyncha, Aleyrodidae) on cotton at constant temperatures. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 56,389-399. von ARX, R., BAUMGÄRTNER,J. & DELUCCHI, V. (1983b) A model to simulate the population dynamics of Bemisia tabaci Genn. (Ster., Aleyrodidae) on cotton in the Sudan Gezira. Zeitschrift fUr Angewandte Ehtomologie 96,341-363. von ARX, R., BATJMGÄRTNER,J. & DELUCCHI, V. (1984) Sampling of Bemisia tabaci (Gern. ) (Sternorryncha: Aleyrodidae) in Sudanese cotton fields. Journal of Economic Entomology 77,1130-1136. ASKEW, R. R. & SHAW, M. R. (1986) Parasitoid communities: their size, structure and development. In Insect parasitoids (ed. J. Waage & D. Greathead), pp. 225-264. London; Academic Press. AVIDOV, Z. (1956) Bionomics of the tobacco whitefly (Bemisia tabaci Gennad. ) in Israel. Ktavim 7 (1), 25-41. - 276 - AVILLA, J. & ALBALES, R. (1984) The influence of female age and host size on the sex ratio of the parasitoid Opius concolor. Entomologia Experimentalis et Applicata 35,43-48. AWADALLAH, K. T., TAWFIK, M. F. S. & SHALABY, F. (1980) Insect fauna of the bind-weed, Convolvulus arvensis L., in Giza, Egypt. Bulletin of the Entomological Society of Egypt 60 (1976), 15-24. AZAB, A. K., MEGAHED,M. M. & EL-MIRSAWI, H. D. (1970a) Studies on Bemisia tabaci (Genn. ) (Hemiptera-Homoptera: Aleyrodidae). Bulletin de la Societe Entomologique d'Egypte 53 (1969), 339-352. AZAB, A. K., MEGAHED,M. M. & EL-MIRSAWI, H. D. (1970b) Effect of degree of pubescence of host-plant on the number and distribution of dorsal spines in pupa of Bemisia tabaci (Gern. ) (Hemiptera-Homoptera). Bulletin de la Societd Entomologique d'Egypte 53 (1969), 352-357 AZAB, A. K., MEGABED,M. M. & EL-MIRSAWI, H. D. (1970o) Parasitism of Bemisia tabaci (Genn. ) in U. A. R. (Hemiptera-Homoptera: Aleyrodidae). Bulletin de la Societ' Entomologique d'Egypte 53 (1969), 439-441. AZAB, A. K., MEGAHED,M. M. & EL-MIRSAWI, D. H. (1971) On the biology of Bemisia tabaci (Genn. ) (Hemiptera-Homoptera: Aleyrodidae) Bulletin de la Soeietd Entomologque d'Egypte 55 (1971), 305-315. GALA RISHNAN, S. & NENE, Y. L. (1980) A note on the mode of penetration of the fungus Paecilomyces farinosus (Dickson Ex. Fries) Brown and Smith into the whitefly Bemisia tabaci Gennadius. Science and Culture 46 (6), 231-232. BALOCH, A. A. & SOOMRO,B. A. (1980) Preliminary studies on plant profile and population dynamics of insect pests of cotton. Turkiye Bitki Koruma Dergisi 4 (4), 203-217. BARRADAS,M. H. & CHAGAS,C. M. (1982) Mosaic dourado de Vigna luteola (Jacq. ) Betharn, leguminosa da vegetacao espontanea. Arquivos do instituto Biologico, Sao Paulo 49,85-88. BARRETO, B. A., SILVA, T. L. da. & TEIXEIRA, R. M. de C. (1980) Ocorrencia de 'mosca branca' Bemisia tabaci (Gennadius, 1889) (Homoptera; Aleyrodidae) em feijoeiro (Phaseolus vulgaris L. ) no estado do Rio Grande do sul. Agronomia Sulriograndense 16 (2), 363-365. BARTL.ETT, B. R. (1964) Patterns in the host-feeding habit of adult Hymenoptera. Annals of the Entomological Society of America 57, 344-350. BENNETT, F. D. & ALAM, M. M. (1965) An annotated check-list of the insects and allied terrestrial arthropods of Barbados. Barbados; Caribbean Agricultural Research and Development Institute. 81 pp. BERGER, E. W. (1921) Natural enemies of scale insects and whiteflies in Florida. Quarterly Bulletin Florida State Plant Board, Gainesville (3), 141-154. ,5 - 277 - BERLINGER, M. J. & DAHAN, R. (1983) Integrated control of the tobacco whitefly Bemisia tabaci in greenhouse tomatoes in Israel. In 10th International Congress of Plant Protection 1983. Volume 3. Proceedings of a conference held at Brighton, England, 20-25 November, 1983. Plant protection for human welfare. Croydon, UK; British Crop Protection Council. p. 1109. BERLINGER, M. J., DAHAN, R. & COHEN, S. (1983) Greenhouse tomato pests and their control in Israel. Bulletin SROP6,7-11. BERLINGER, M. J., DAHAN, R. & SHEVACHURKIN, E. (1983) Breeding for resistance to whiteflies in tomatoes - in relation to integrated pest control in greenhouses. Bulletin SROP6 (3), 172-176. BERLINGER, M. J., MAGAL, Z. & BENZIONI, A. (1983) The importance of pH in food selection by the tobacco whitefly, Bemisia tabaei. Phytoparasitica 11,151-160. BINDRA, O. S. (1983) Insect resistance in cotton in Sudan. In Durable resistance in crops (ed. F. Lamberti, J. M. Waller, & N. A. van der Graaf), pp. 227-229. New York; USA; Plenum Press. BINDRA, O. S. & RAHMAN, A. A. A. (1983) Cotton integrated-pest-control in Sudan. In 10th International Congress of Plant Protection 1983. Volume 3. Proceedings of a Conference held at Brighton, England, 20-25 November, 1983. Plant protection for human welfare. Croydon, UK; British Crop Protection Council. p. 937. BINK, F. A. (1973) Nouvelle contribution a l'etude de la mosaique du contonnier au Tchad. I. Symptomes, transmission par Bemisia tabaei (Genn. ); II. - Observations sur B. tabaci, III. - Autres maladies virales sur cotoniers et plantes voisines. Coton et Fibres Tropicales 28,365-378. BINK-MOENEN, R. M. (1983) Revision of the African whiteflies (Aleyrodidae) mainly based on a collection from Tchad. Amsterdam Netherlands; Nederlandse Entomologische Vereniging. 210 pp. BIRCH, L. C. (1948) The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology 17,15-26. BIRD, J. & SANCHEZ,J. (1971) Whitefly-trasnmitted viruses in Puerto Rico. Journal of Agriculture of the University of Puerto Rico 55,1461-1467. BIRD, J., SANCHEZ, J. & VAKILI, N. G. (1973) Golden yellow mosaic of beans (Phaseolus vu arcs) in Puerto Rico. Phytopathology 63,1435. BISHT, N. S. & BANERJEE, A. K. (1965) Occurrence of two new diseases in Uttar Pradesh. Labdev Journal of Science and Technology 3 (4) 271-272. BLANCO SANCHEZ, N. & BENCOMO, I. (1978) Afluencia de la mosca blanca (Bemisia tabaci), vector del virus del mosaico dorado, en plantaciones de frijol. Ciencias de la Agricultura 2,39-46. BLANCO SANCHEZ, N. & BENCCMOPEREZ, I. (1981) Presencia del virus del mosaico dorado del frijol (BGMV) en Cuba. Ciencias de la Agricultura 9,118. - 278 - BOCK, K. R. (1983) Epidemiology of cassava mosaic disease in Kenya. In Plant virus epidemiology. The spread and control of insect-borne virus (ed. R. T. Plumb & J. M. Thresh), pp 337-347 Oxford, United Kingdom; Blackwell Scientific Publications. van den BOCH, R., MESSENGER,P. S. & GUTIERREZ, A. P. (1982) An introduction to biological control. New York and London; Plenum press. BORROR, D. J. & DeLONG, D. M. (1964) An introduction to the study of insects. New York; Rinehart & Winston. 819 pp. BORTOLI, S. A. de, GIACOMINI, P. L. (1981) Acao de alguns inseotioidas granulados sistemicos sobre Bemisisa tabaci (Genradius, 1889) (Homoptera-Aleyrodidae) e Empoasca kraemeri Ross and Moore, 1957 (Homoptera-Cicadellidae) e seus efeitos na productidade do feijoeiro (Phaseolus vulgaris L. ). Anais da Sociedade Entomologica do Brasil 10,97-104. BOULETREAU,M. (1986) The genetic and coevolutionary interactions between parasitoids and their hosts. In Insect parasitoids (ed. J. Waage & D. Greathead), pp. 169-200. London; Academic Press. BRADER, L. (1981) Resistance horizontale aux ravageurs et maladies des vegetaux. Rome, Italy; FAO. 10 pp. BURNETT, T. (1962) An effect of parasite attack on host mortality as exemplified by Encarsia formosa and Trialeurodes vaporariorum. Canadian Entomology 94 (7), 673-679. BURNETT, T. (1951) Effects of temperature and host density on the rate of increase of an insect parasite. American Naturalist 85,337-357. BUTANI, D. K. & JOTWANI, M. G. (1983) Insects as limiting factors in vegetable production. Pesticides 17 (9), 6-13. BUTLER, G. D., HENNEBERRY, T. J. & CLAYTON, T. E. (1983) Bemisia tabaoi (Homoptera; Aleyrodidae): development, oviposition, and longevity in relation to temperature. Annals of the Entomological Sooiety of America 76,310-313. BUTLER, G. D. & FENNEBERRY,T. J. (1984) Bemisia tabaci; effect of cotton leaf pubescence on abundance. Southwestern Entomologist 9 (1), 91-94. BUTLER, G. D., HENNEBERRY,T. J. & NATWICK, E. T. (1985) Bemisia tabaci: 1982 and 1983 populations in Arizona and California cotton fields. Southwestern Entomologist 10 (1), 20-45. BUTLER, G. D., HENNEBERRY,T. J. & HUTCHISON, W.D. (1986) Biology, sampling and population dynamics of Bemisia tabaci. Agricultural Zoology Reviews 1,167-195. BUTLER, G. D. & WI SON, F. D. (1984) Activity of adult whiteflies (Homoptera: Aleyrodidae) within plantings of different cotton strains and cutivars as determined by sticky-trap catches. Journal of Economic Entomology 77,1137-1140. - 279 - CIE (1986) Distribution maps of pests. Series A (Agriculture). Map no 284 June 1986 (revised) Bemisia tabaci (Gennadius). London, UK; C. A. B. International Institute of Entomology. CASTELLANI, E., NUR, A. M. & MOHAMED,M. I. (1982) L'arricoiamento fogliare del pomodoro in Somalia. Annali della Facolta di Scienze Agrarie della Universita degli Studi di Torino 12 (1979-1982), 145-161. CHAGAS, C. M., VICENTE, M. & BARRADAS, M. M. ( 1981) Maeroptilium erythroloma (Mart. ex Benth. ) Urb. Leguminosae-possivel reservatorio do virus do mosaico dourado do feijoeiro (VMDF)Arquivos do Instituto Biologico, Sao Paulo 48,113-116. CHANG, Y. C. (1969) Host plant and morphological variation of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) in Taiwan. Plant Protection Bulletin, Taiwan 11 (1), 23-32. CHANT, S. R. (1958) Studies on the transmission of cassava mosaic virus by Bemisia spp. (Aleyrodidae). Annals of Applied Biology 46,210-215. CHARNOV,E. L. (1982) The theory of sex allocation. Princeton; University Press. CHAVAN, V. M. (1983) Efficacy of systemic insecticides for the control of Bemisia tabaci Genn., a vector of a leaf-curl of cigar-wrapper tobacco. [tobacco leaf curl virus]. Indian Journal of Agricultural Sciences 53,585-589. CHHABRA, K. S. & KOONER, B. S. (1981) Field resistance in black gram, Vigna mungo L. against insect-pest complex and yellow mosaic virus. Indian Journal of Entomology 43,288-293. CHORLEY, J. R. (1939) Report of the Division of Entomology for the year ending 31st December, 1938. Rhodesia Agricultural Journal 36, 598-622. CHORLEY, J. K. (1943-44) Report(s) of the Acting Chief Entomologist for the year(s) 1942 [and] 1943.16 pp. 17 pp., typescript. CHOU, I. (1959) Listo de la konataj Aleurodoj "Homoptero" en cinio. Entomologia et Ars, Entomologia Sinica 3 (4), 18 pp. CIBC PAKISTAN STATION (1983) Studies on potential biological control agents of whiteflies in Pakistan. March 1979-February 1982. Unpublished Report. Rawalpindi, Pakistan, CIBC Pakistan Station. 88 pp. COCK, M. J. W. (1986) Possibilities for classical biological control. In Bemisia tabaci a literature survey on the cotton whitefly with an annotated bibliography. (ed. M. J. W. Cock), pp. 63-72. UK, C. A. B. International Institute of Biological Control. COHEN, S., DUFGUS, J. E., LARSEN, R. C., LIU, H. Y. & FLOCK, R. A. (1983) Purification, serology, and vector relationships of squash leaf curl virus a whitefly-transmitted geminivirus. Phytopathology, 73, 1669-1673. COHEN,S. & NITZANY, F. E. (1966) Transmission and host range of the tomato yellow leaf curl virus. Phytopathology 56,1127-1131. - 280 - COPLAND, M. J. W. (1976) Female reproductive system of the Aphelinidae (Hymenoptera: Chalcidoidea). International Journal of Insect Morphology and Ecology 5 (3), 156-166. CORBETT, G. H. (1935a) On new Aleurodidae (Hem. ) Annals and Magazine of Natural History 16,240-252. CORBETT, G. H. (1935b) Malayan Aleurodidae. Journal of the Federated Malay States Museums 17,722-852. COSTA, A. S. (1965) Three whitefly-transmitted virus diseases of beans in Säo Paulo, Brazil. FAO Plant Protection Bulletin 13 (6), 121-130, COSTA, A. S. (1976) Whitefly-transmitted plant diseases. Annual Review of Phytopathology 14,429-449. COUDRIET, D. L., PRABHAKER,N., KISHARA, A. N. & MEYERDIRK, D. E. (1985) Variation on development rate on different hosts and overwintering of the sweet potato whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Environmental Entomology 14,516-519. LOWLAND,J. W. (1943) Gezira Entomological Section, G. A. R. S. Final report on experimental work, 1933-33. Repost. Gezira Agricultural Reserach Service, Anglo Egyptian Sudan 1933,107-125. CROWE, T. J. (1985) Field crop pests in Burma. An annotated list. Rangoon, Burma; Office of the FAO Representative. 65 pp. CYPRUS(1977) Annual Report for 1976. Report. Cyprus Agricultural Research Institute, 40-47. CYPRUS (1979) Annual Report for 1978. Report. Cyprus Agricultural Research Institute, 148-50. CYPRUS (1980) Annual Report for 1979. Report Cyprus Agricultural Research Institute, 33-35,36-39. CYPRUS (1981) Annual Report for 1980. Report Cyprus Agricultural Research Institute, 34-37. d'ARAUJO e SILVA, A. G., GONCALVES, C. R., GALVAO, D. M., GONCALVES, A. J. L., GOMEZ, J., SILVA, M. do N. & SIM NI, L. de. (1968) Quarto catalogo dos insetos gue vivem nas plantas do Brasil seus parasitos e predatores. Parte II 1 Tomo. Rio de Janeiro, Brazil; Ministeriode A- gricultura. pp. 117-118. DAZING, E. M. (1964) The whiteflies (HomDptera, Aleyrodidae) of Caucasus. Entomologicheskoe Obozrenie 43,633-646. [In Russian; English translation in Entomological Review 43,325-330] (1969) DEANG, R. T. An annotated list of insect pests of vegetables in the Philippines. Philippine Entomologist 1,313-333. DEBACH, P. (1943) The importance of host-feeding by adult parasites in the reduction of host population. Journal of Economic Entomology 36, 647-658. - 281 - DEBACH, P. (1964) Biological control of insect pests and weeds. London; Chapman and Hall. DEBACH, P. & SMITH, H. S. (1941) The effect of host density on the rate of reproduction of entomophagous parasites. Journal of Economic Entomology 34,741-745. DEBACH,P. & SUNDBY,R. A. (1963) Competitive displacement between ecological homologues. Hilgardia 34,105-166. DEBROT, C. E., HEROLD,F. & DAO, F. (1963) Nota preliminar sobre un "mosaico amarillento" del tomate en Venezuela. Agronomia Tropical 13,33-41. DELATTRE, R. (1961) Studies on the infestation and pesticide treatment of cotton in Africa. Outline of the work of the I. R. C. T. Phytiatrie-phytopharmacie 10, (1), 13-26. DENGEL, H. J. (1961) Untersuchungen fiber das Auftreten der Imagines von Bemisia tabaei (Genn. ) auf verschiedenen Manioksorten. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 88,355-366 DHURI, A. V. & SINGH, K. M. (1963) Pest complex and succession of insect pests in black gram Vigna mungo (L. ) Hepper. Indian Journal of Entomology 45,396-401. DICKSON, R. C., JOHNSON,M. Mc. D. & LAIRD, E. F. (1954) Leaf crumple, a virus disease of cotton. Phytopathology 44,479-480. (1979) DIOGER, J. Progress made in integrated control of cotton pests with special emphasis on its practicability and economic interest. In ) Russ, K., Berger, H. (eds. Proceedings. International symposium of IOBC/WPRS on Integrated control in agriculture and forestry. Vienna, 8th-12th October 1979. Vienna, Austria; International Organization of Biological Control. pp. 211-213. DINGER, J. (1984) Ege bblgesinde pamuk zararhlarina karsi integre mUcadele imkanlarinin arastirilmasi. Bitki Korurna bülteni 24 (1), 15-32. DITRICH, V. & ERNST, G. H. (1983) The resistance pattern in whiteflies of Sudanese cotton. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 4 (1/3), 96-97. DIETRICH, V., HASSAN, S. O. & ERNEST, G. H. (1985) Sudanese cotton and the whitefly: a case study of the emergence of a new primary pest. Crop Protection. 4,161-176. DODDS, J. A., LEE, J. G., NANETH, S. T. & LAEMMLEN, F. F. (1981) Aphid and whitefly-transmitted cucubit viruses in Imperial county, California. Phytopathology 74,221-225. DONALSON, J. S. (1985) Sex ratios of Coecophagus atratus (Hymenoptera: Aphelinidae) in relation to host availability. Unpublishished MSo Thesis Rhodes University. DONNELLY, J. (1966) Insect pest on kenaf. Nigerian Entomological Magazine 1 (1), 8-9. - 282 - DUFFUS, J. & DOLLET, M. (1981) Beet pseudo-yellow virus, transmitted by the greenhouse whitefly (Trialeurodes vaporariorum). Phytopathology 55, 450-453. (1959) DOUTT, R. L. The biology of parasitic Hymenoptera. Annual Review of Entomology 4,161-182. DOUTT, R. L. (1964) Biological characteristics of entomophagous adults. In Biological control of insect pests and weeds. (ed. P. DeBach), pp. 141-167. London; Chapman and Hall. DOUTT, R. L., ANNECKE, D. P. & TRE4BLAY, E. (1976) Biology and host relationships of parasitoids. In Theory and practice of biological control(ed. C. B. Huffaker & P. S. Mesenger), pp. 143-168. New York; Academic Press. DUFFUS, J. E., LARSEN, R. C. & LIU, H. Y. (1986) Lettuce infectious yellow virus -a new type of whitefly-transmitted virus. Phytopathology 76, 97-100. EL BADRY, E. A. (1967) Three new species of phytoseiid mites preying on the cotton whitefly Bemisia tabaci in the Sudan (Acarina: Phytoseiidae). Entomologist 100,106-111. EL BADRY, E. A. (1968) Biological studies on Amblyseius aleyrodis a predator of the cotton whitefly. Entomophaga 13,323-329. EL-HELALY, M. S., EL-SHAZLI, A. Y. & EL-GAYAR, F. H. (1971a) Morphological studies on immature stages of Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) Zeitschrift für Angewandte Entomologie, 68, 403-408. EL-RELAY, M. S., EL-SHAZLI, A. Y. & EL-GAYAR, F. H. (1971b) Biological studies on Bemisia tabaci Genn. (Homopt., Aleyrodidae) in Egypt. Zeitschrift für Angewandte Entomologie 69,48-55. EL-HELALY, M. S., IBRAHIM, E. G. & RAWSH,I. A. (1976) Photoperiodism of the whitefly Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). Zeitschrift für Angewandte Entomologie 83,393-397 EL-NAWAWY, A. S., ABD-EL-RAHMAN, I., ASHRY, M. A., HOSNY, A. & BELAL, A. (1983) Effect of mixtures of a foliar fertilizer and each of several insecticides on sucking pests and their predators in cotton field. Mededelingen van de Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 48 (1), 117-127. EL-SERWIIY, S., EL-HAIDARI, H. & SAAD, A. (1984) [Population density of the whitefly Bemisia tabaci (Genradius), (Homoptera: Aleyrodidae) on fall cucumber in Iraq. ] Journal of Agriculture and Water Resources Research 3 (2), 78-87. (Arabic), 135 (English) ELMOSA, N. (1979) FAO/UNEP Near East inter-country program for the development and application of integrated pest control in cotton growing. 1979 report. Working paper AGP:IPC/WP/II of 9th Session FAO/UNEP panel of Experts on Integrated Pest Control. Wad-Medani, Sudan. December 1979 (multigraph). - 283 - ESAKI, T. (1940) A preliminary report on the entomological survey of the Micronesian Islands under the Japanese Mandate, with special reference to the insects of economic importance. 6th Pacific Science Congress 1939 4,407-J415. -Proceedings ESPINOSA, P. (1972) Estudios preliminares para el control de la mosca blanca Bemisia tabaci (Genn. ) del algodonero. In Seventh National Congress of Entomology, 13-16 October 1970, Mexico, D. F. Agricultural entomology: cotton(ed. G. Halffter) Folia Entomologica Mexicana 23/24,25. FALCON, L. A. (1971) Progreso del control integrado en el algodon de Nicaragua. Revista Peruana de Entomologia 14,376-378. FAO (1966) Plant Pest and Disease Situation Near East Regional Report 20,7. FERNANDO, H. E. & PEIRIS, J. W.L. (1975) Investigations on the chilli leaf-curl complex and its control. Tropical Agriculturist 113, 305-323. FERNANDO,M. J. P. & HASSELL, M. P. (1980) Predatory-prey responses in an acarine system. Researches on Population Ecology 22,301-322. FERRIERE, C. (1965) Hymenoptera Aphelinidae d'Europe et du bassin Mediterraneen. Paris; Masson. FLANDERS, S. E. (1935) An apparent correlation between the feeding habits of certain pteromalids and the conditions of their ovarian follicles (Pteromalidae, Hymenoptera). Annals of the Entomological Society of America 28 (4), 438-414. FLANDERS, S. E. (1950) Regulation of ovulation and egg disposal in the parasitic Hymenoptera. Canadian Entomologist 82,134-140. FLANDERS, S. E. (1959) Differential host relations of the sexes in parasitic Hymenoptera. Entomologia Experimentalis et Applicata 2,125-142. FLORES, E., SILBERSCHMIDT, K. &K AMER, M. (1960) Observacoes de "clorose infecciosa" das malvaceas em tomateiros do campo. 26 (4), 65-69. _Biologico FOLTYN, S. & GERLING, D. (1985) The parasitoids of the aleyrodid Bemisia tabaci in Israel: development, host preference and discrimination of the aphelinid wasp Eretmocerus mundus. Entomologia Experimentalis et Applicata 38,255-260. FORSYTH, J. (1966) Agricultural insects of Ghana. A list of insects recorded in Ghana on field crops and stored produce with their host plants, damage caused, locality, parasites and predators where known, together with references to the literature for Ghana and neighbouring coutries covering the period 1910-1960. Accra, Ghana; Ghana University Press. 163 pp. FRANSEN. J. & MONFORT,M. J. (1987) Functional response and host preference of Encarsia formosa Gahan (Hym. Aphelinidae), a parasitoid of greenhouse whitefly T. vaporariorum (Westwood) (Hom., Aleyrodidae). Zeitschrift für Angewandte Entomologie 103,55-69. - 284 - FULNEX, L. (19+3) Wirtsindex der Aleyrodiden-und Cocaiden-Parasiten. Entomologische Beihefte aus Berlin-Dahlem 10,100 pp. GAHAN, A. B. (1924) Some new parasitic Hymenoptera with notes on several described forms. Proceedings the U. S. National Hiseum 65,1-23. GAMEEL, 0.1. (1969) Studies on whitefly parasites Encarsia lutea Masi and Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae). Revue de Zoologie et Botanique Africaines 79,65-77. GAMEZ, R. (1971) Los virus del frijol en Centro America. I. Transmision por moscas blancas (Bemisia tabaci Gen. ) y plantas hospedantes del virus del mosaico dorado. Thrrialba 21,22-27 GANGWAR, S. K. & SACHAN, J. N. (1981) Seasonal incidence and control of insect pests of brinjal with special reference to shoot and fruit borer, Leucinodes orbonbalis Guen. in Meghalaya. Journal of Research, Assam Agricultural University 2 (2), 187-192. GENNADIUS (1889) Disease of tobacco plantations in the Trikonia. The aleurodid of tobacco. Ellenike Georgia 5,1-3. (in Greek]. GENTRY, J. W. (1965) Crop insects of northeast Africa-southwest Asia. Agriculture Handbook, United States Department of Agriculture 273, 210 pp. GERLING, D. (1966a) Biological studies on IIzcarsia formosa (Hymenoptera: Aphelinidae). Annals of the Entomological Society of America 59, 142-143. GERLING, D. (1966b) Studies with whitefly parasites of southern California I. Encarsia pergandiella Howard (Hymenoptera: Aphelinidae) Canadian Entomologist 98,707-724. GERLING, D. (1966c) Studies with whitefly parasites of southern California. II. Eretmocerus californicus Howard (Hymenoptera: Aphelinidae). Canadian Entomologist 98,1316-1329. GERLING, D. (1967) Bionomics of the white fly-parasite complex associated with cotton in southern California (Homoptera: Aleurodidae; Hymenoptera: Aphelinidae) Annals of the Entomological Society of America 60,1306-1321. GERLING, D. (1972) Notes on three species of Eretmocerus Haldeman occurring in Israel with a description of a new species. Entomologische Berichten 32,156-161. GERLING, D. (1983) Factors affecting the establishment of Bemisia tabaci on cotton in Israel. In 10th International Congress of Plant Protection 1983. Volume 3. Proceedings of a Conference held at Brighton, England, 20-25 November, 1983. Plant protection for human welfare. Croydon, UK; British Crop Protection Council. p. 959. GERLING, D. (1984) The overwintering mode of Bemisia tabaoi and its parasitoids in Israel. Phytoparasitiea 12,109-118. GERLING, D. (1985) Parasitoids attacking Bemisia tabaci (Hom.: Aleyrodidae) in eastern Africa. Entomophaga 30,163-165. - 285 - GERLING, D. & FOLTYN, (1987) S. Development and host preference of Enoarsia lutea (Masi) and interspecific host discrimination with Eretmocerus (Mercet) (Hymenoptera, mundus Aphelinidae) parasitoids of Bemisia tabaci (Gennadius) (Homoptera, Aleyrodidae). Journal of Applied Entomology 103,1425-1133. GERLING, D. & HOROWITZ, R. (1984) Yellow traps for evaluating the population levels and dispersal patterns of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 77,753-759. GERLING, D., MOTRO,U. & HOROWITZ,R. (1979) Dynamics of Bemisia tabaci and its in parasites Israel cotton fields. Abstracts of Papers, 9th International Congress of Crop Protection, Washington DC, 5-11 August, 1979. GERLING,D., MTRO, U. & HOROWITZ,R. (1980) Dynamics of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) attacking cotton in the coastal 70,213-219. plain of Israel. Bulletin of Entomological Research (Hym.: GERLING, D. & RIVNAY, T. (1984) A new species of ncarsia (Hom.: Aleyrodidae). Aphelinidae) parasitizing Bemisia tabaci Entomophaga 29 (4), 439-44+4. GIHA, O. H. & NOUR, M. A. (1969) Epidemiology of cotton leafcurl virus in the Sudan. Cotton Growing Review 46,105-118. GITHUNGURI, C. H., NDONG'A, M. F. 0. & AMADALO, B. A. (1984) Cassava production and constraints in Kenya. In Integrated pest management in of cassava green mite. Proceedings of a regional training workshop East Africa (ed. A. H. Greathead, R. H. Markham, R. J. Murphy, S. T. Murphy, I. A. D. Robertson) Ascot, United Kingdom; Commonwealth Institute of Biological Control. pp. 75-79. GOLDING, F. D. (1935) A probable vector of cassava mosaic in Southern Nigeria. Tropical Agriculture, Trinidad 12,215. GOLDING, F. D. (1936) Bemisia nigeriensis Corb., a vector of cassava mosaic in Southern Nigeria. Tropical Agriculture Trinidad 13,182-186. GOLDIN, F. D. (1938) Notes on the insect pests of cotton in Nigeria. Empire Cotton Growing Review 15,224-227. GCMEZ--MENOR,J. (1944) Aleirodidos de interes agricola. Instituto Nacional de Investigacion Agricola, Espafia Trabajos 133,36 p. GOULD, H. J., PARR, W.J., WOODVILLE,H. C. & SNIONDS, S. P. (1975) Biological control of glasshouse whitefly (Trialeurodes vaporariorum) on cucumbers. Entomophaga 20 (3), 285-292. GRANILLO, C. R., ANAYA, M. & DIAZ, A. (1974) Virus desease of sweet pepper in El Salvador Phytopathology 64,768. (1986a) GREATHEAD, A. H. Host plants. In Bemisia tabaci a literature survey on the cotton whitefly with an annotated bibliography (ed. M. J. W. Cook), pp. 17-25 Ascot UK; C. A. B. International Institute of Biological Control. - 286 - GREATHEAD, D. J. (1986b) Parasitoids in classical biological control. In Insect parasitoids (ed. J. Waage & D. Greathead), pp. 290-318. London; Academic Press. G[REATHEAD], D. J. & B[ENNETT], F. D. (1981) Possibilities for the use of biotic agents in the control of the whitefly, Bemisia tabaoi. Biocontrol News and Information 2,7-13. GREATHEAD, D. J. & WAAGE,J. K. (1983) Opportunities for biological control of agricultural pests in developing countries. World Bank Technical Paper Number 11,34 pp. GRUPOPAULISTA DE FITOPATOLOGIA. (1983) Paulist Phytopathological Group. VI Paulist Phytopathology Congress, 24 to 26 January 1983, IAA/PLANALSUCAR- Coordenadoria Regional Sul Araras- SP. Summ Phytopathologica 9 (1/2), 3-97. GUAGLIUMI, P. (1967) Insetti e aracnidi delle piante comuni del Venezuela segnalati nel periodo 1938-1963. Relazioni e Monografie Agrarie Subtropicali e Tropicali Firenze (Nuova Serie) 86,391 pp. GUPTA, P. C. (1972) External morphology of Bemisia gossypiperda (M. & L. ) a vector of plant virus disease (Homoptera: Aleyrodidae). Zoologische Beitrage 18,1-23. GUPTA, P. C. & CHAUDHRY,H. S. (1972) New record of Hemitarsonemus latus Bank (Tarsonemidae) as a predator of Bemisia gossypiperda M. & L. Indian Journal of Entanology 33 (1971), 476. GUPTA, P. K. & SINGH, J. (1983) Effect of systemic granular insecticides on whitefly population and yellow-mosaic infection in greengram. Indian Journal of Agricultural Sciences 53,737-742. HABIB, R. & MOHYUDDIN,A. I. (1981) Possibilities of biocontrol of some pests of cotton in Pakistan. Biologia 27 (1), 107-113. HABIBI, J. (19750 The cotton whitefly Bemisia tabaci Gen. Bioecology and methods of control. Entomologie et Phytopathologie Appliquees 38, 13-36. HAESELBARTH,E. (1979) Zur Parasitierung der Puppen von Forloule (Panolis flammea Schiff) Kiefernspanner (Bupalus piniarius L. ) und Heidelbeerspanner (Boarmia bistortata Goeze) in baygerischen kierfernwaldern. Zeitschrift für Angewandte Entomologie 87,311-322. HAFEZ, M., TAWFIK, M. F. S., AWADALLAH,K. T. & SARHAN, A. A. (1983a) Natural enemies of cotton whitefly, Bemisia tabaci (Gern. ), in the world and in Egypt. Bulletin de la Societd Entomologique d' Egypte 62 (1978/1979), 9-13. HAFEZ, M., TAWFIK, M. F. S., AWADALLAH,K. T. & SARHAN,A. A. (1983b) Studies on Eretmocerus mundus Mercet, a parasite of the cotton whitefly, Bemisisa tabaci (Genn. ) in Egypt (Hymenoptera: Aphelinidae). Bulletin de la Societe Entomologique d' Egypte 62 (1978/1979), 15-22. HAFEZ, M., TAWFIK, M. F. S., AWADALLAH,K. T. & SARHAN,A. A. (1983o) Impact of the parasite, Eretmocerus mundus Mercet on populations of the cotton whitefly, Bemisia tabaci (Genn. ), in Egypt. Bulletin de la Societe Entomologique d' Egypte 62 (1978/1979), 23-32. - 287 - HARAKLY, F. A. (1974) Variation in pupae of Bemisia tabaci (Gennadius) bred on different hosts (Homoptera: Aleyrodidae). Bulletin de la Societ6 Entomologique de'Egypte 57,407-412. HARPAZ, I. & COHEN,S. (1965) Semipersistent relationship between cucumber vein yellowing virus (CVYV) and its vector, the tobacco whitefly (Bemisia tabaci Gennadius). Phytopathologische Zeitschrift 54 240-248. HASSELL, M. P. (1978) The dynamics of arthropod predator-prey systems. Monographs in population biology 13. Princeton; Princeton University Press. HASSELL, M. P. (1980) The dynamics of competition and predation. Studies in biology no. 72. Southampton; Camelot Press. HASSELL, M. P. (1982) What is searching efficiency. Annals of Applied Biology 101,170-175. HASSELL, M. P. & MORAN, V. C. (1976) Equilibrium levels and biological control. Journal of the Entomological Society of South Africa 39, 357-366. HASSELL, M. P., LAWTON, J. H. & BEDDINGTON, J. R. (1977) Sigmoid functional responses in invertebrate predators and parasitoids. Journal of Animal Ecology 46,246-262. HASSELL, M. P. & WAAGE,J. K. (1984) Host-parasitoid population interactions. Annual Review of Entomology 29,89-114. HASSELL, M. P., WAAGE,J. K. & MAY, R. M. (1983) Variable parasitoid sex ratios and their effect on host-parasitoid dynamics. Journal of Animal Ecology 52,889-904. HAYAT, M. (1972) The species of Eretmocerus Haldeman, 1850 (Hymenoptera: Aphelinidae) from India. Entomophaga 17,99-106. HEIJNE, C. G. & PARAEGRINE, D. J. (1984) The effects of ULV spray characteristics on the activity of amitraz against the cotton whitefly, Bemisia tabaci (Gennadius). In 1984 British Crop Protection Conference. Pests and Diseseas. Proceedings of a conference held at Brighton Metropole, England, November 19-22,1984. Volume 3. Croydon, United Kingdom; British Crop Protection Council. pp. 975-979. HEIMSINGH PRUTHI & SAMUEL[C. IC.] (1942) Entomological investigations on the leaf-curl disease of tobacco in northern India. Indian Journal of Agricultural Science 12,35-57. HERAKLY, F. A. & EL-EZZ, A. A. (1970) The cotton whitefly, Bernisia tabaci (Gern. ), infesting cucurbits, in U. A. R. Agricultural Research Review 48,110-118. - 288 - HERREN,H. R. & BENNETT, F. D. (1984) Cassava pests, their spread and control. In Hawksworth, D. L. (ed. ) Advancing agricultural production in Africa. Proceedin s of CAB's First Scientific Conference, Arusha, Tanzania, 12-18 February 1984. Farnham Royal, Slough, UK;_ Commonwealth Agricultural Bureaux. pp. 110-114. HIDALGO SALVATIERRA, 0., LEON QUANTt G., LINDO ESPINOZA, 0. & VAUGHAN RODRIGUEZ, M. (1975) Informe de la Mision de Estudio de la Mosca Blanca. Banco Nacional de Nicaragua, Comision Nacional del Algodon & Ministerio de Agricultura y Ganaderia, Managua Nicaragua. 120 pp. HILL, B. G. (1968) Ocurrence of Bemisia tabaci (Genn. ) in the field and its relation to the leaf curl disease of tobacco. South African Journal of Agricultural Science 11 (3) 583-594. HOHMANN,C. L., van SCHOONHOVEN,A. & CARDONA.C. (1980) Manejo de plagas del frijol (Phaseolus vulgaris Linneaus, 1753) a traves de la utilizacion de sistemas de diversificacion del cultivo con malezas asociado a resistencia varietal. Anais da Sociedade Ehtomologica do Brasil 9,143-153. HOLLING, C. S. (1959a) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Canadian Entomologist 91,293-320. HOLLING, C. S. (1959b) Some characteristics of simple types of predation and parasitism. Canadian Entomologist 91,385-398. HOLLINGO C. S. (1961) Principles of insect predation. Annual Review of Entomology 6,163-182. HOROWITZ, A. R., MOTRO, U. & GERLING, D. (1979) Natural mortality of the tobacco whitefly (Bemisia tabaci) in Israel cotton fields. [Abstract]. In Proceedings InterTational Symposium of IOBC/WPRSon Integrated Control in Agriculture and Forestry, Vienna, 8th-12th October 1979 (ed. K. Russ, H. Berger). Vienna, Austria; International Organization for Biological Control. p. 503. HOROWITZ,A. R., PODOLER,H. & GERLINGt D. (1984) Life table analysis of the tobacco whitefly Bemisia tabaci (Gennadius) in cotton fields in Israel. Acta Oecologica, Oecologia Applicata 5 (3), 221-233. HOUCH, M. A. & STRAUSS, R. E. (1985) The comparative study of functional responses: experimental design and statistical interpretation. Canadian Entomologist 11T, 61T-629. HOWARDtL. O. (1910) On the habit with certain chalcidoidea of feeding at puncture holes made by the ovipositor. Journal of Economic Entomology 3 (3)p 25T-260. HOWELL, N. H., (1978) Notas sobre el manejo de las plagas del agodon en Honduras, C. A. su ecologia y su control. Ceiba 22 (1), 29-33. HUFFAKERt C. B. t MESSENGER0P. S. & DEBACH, P. (1971) The natural enemy component in natural control and the theory of biological control. In Biological (ed. C. B. Huffaker) 16-67. New York: Plenum control. , pp. Press. - 289 - HUNTER, M. S. (1986) Sex ratio and egg distribution of an autoparasitoid Encarsia pergandiella (Hymenoptera: Aphelinidae) on greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Mimeograph unpublished. HUSAIN, M. A. & TREHAN, K. N. (1933) Observations on the life-history, bionomics and control of the white fly on cotton (Bemisia gossypiperda M. & L. ). Indian Journal of Agricultural Science 3 (5), 701-753. IACCARINO, F. M. (1981) Aleirodidi nuovi o poco noti per 1'Italia. Bolletino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici 38,143-157. _ ISRAEL (1982) Abstracts of papers presented at a meeting on whiteflies in field crops and vegetables, May 20,1982, Gilat Regional Experimental Station, Israel. Phytoparasitica 10,293- 298. ISRAEL (1983) Abstracts of papers presented at the 2nd meeting on whiteflies in field crops and vegetables. January 17,1983 Rehovot, Israel. Phytoparasitica 11,63-67. ISRAEL (1984) Abstracts of papers presented at the 3rd meeting on whiteflies in field crops and vegetables, February 7,1984, Tel Aviv, Israel. Phytoparasitica 12,139-143. ISRAEL, (1985) Abstracts of papers presented at the 4th meeting on whiteflies in field crops, vegetables and orchards. February 11,1985, Bet Dagan, Israel. Phytoparasitica 13,73-79. JACKSON, G. V. H. (1980) Diseases and pests of taro. Noumea, New Caledonia; South Pacific Commission. 52 pp. JERVIS, M. A. & KIDD, N. A. C. (1986) Host-feeding strategies in hymenopteran parasitoids. Biological Reviews 61,395-434. JOHNSTON,F. A. (1915) Asparagus beetle egg parasite. Journal of Agricultural Research 4,303-313. JONES, T. H. (1986) Patterns of parasitism by Trybliographa rapae (Westwood) a cynipid parasitoid of the cabbage root fly. Unpublished Ph. D. thesis University of London. JOYCE, R. J. V. (1955) Cotton spraying in Sudan Gezira. I. Yield increase from spraying and spraying methods. II. Entomological problems arising from spraying. FAO Plant Protection Bulletin 3,86-92,97-103" KAJITA, H. & van LENTEREN, J. C. (1982) The parasite-host relationship between &carsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). XIII. Effect of low temperatures on egg maturation of Encarsia formosa. Journal of Applied Entomology 93,430-1439. KHALIFA, A. & EL-KHIDIR, E. (1965) Biological study on Trialeurodes lubia and Bemisia tabaci (Aleyrodidae). Bulletin de la Societd Entomologigue d' Egypte 48 (1964), 115-129. - 290 - KHALIFA, H. & GAMEEL, 0.1. (1983) Breeding cotton cultivars resistant to whitefly (Bemisia tabaci(Genn. ))In Durable resistance in crops (ed. F. Lamberti, J. M. Waller, N. A. van der Graaf), pp. 231-236. New York, USA; Plenum Press. KHALIL, F. A., WATSON,W. M. & GUIRGUIS, M. W. (1983) Evaluation of Dimilin and its combinations with different insecticides against some cotton pests in Egypt. Bulletin of the Entomological Society of Egypt (Economic) 1978-79 (13), 71-76. KING, W. J. (1980) Cotton in the Gambia (report on the cotton Development Project 1975-78). Miscellaneous Report, Overseas Development Administration 51,18 pp. KISHA, J. S. A. (1984) Whitefly, Bemisia tabaci, infestations on tomato varieties and a wild Lycopersicon species. Annals of Applied Biology 104 (Supplement, Tests of Agrochemicals and Oultivars, 5), 124-125. KOBATAKE, H., OSAKI, T. & INOUYE, T. (1981) [Ecology and control of yellow dwarf disease of tomato caused by tobaco leaf curl virus. ] Proceedings of the Kansas Plant Protection Society 23,8-14. [In Japanese with English summary. ] LABOUCHEIX,J. (1973) Recherche et production cotonieres au Nicaragua. Bilan de cinq annees de lutte phytosanitaire. Coton et Fibres Tropicales 28,323-335. LAL, S. S. (1980) A note on Prospaltella flava Shafee, an aphelinid parasitoid of Bemisia tabaci (Gennadius). Madras Agricultural Journal 67,557-558. LAL, S. S. & PILLAI, K. S. (1982) Ecological studies on whitefly, Bemisia tabaci (Gennadius), infesting cassava in Kerala. Ehtomon 7 (1), 101-102. van LENTEREN, J. C. (1980) Evaluation of natural enemies: does art have to become science? Netherlands Journal of Zoology 30,369-386. van LENTEREN, J. C. (1986) Parasitoids in the greenhouse: successes with seasonal inoculative release systems. In Insect parasitoids (ed. J. Waage & D. Greathead), pp. 341-374. London; Academic Press. van LENTEREN, J. C. & BAKKER, K. (1976) Functional responses in invertebrates. Netherlands Journal of Zoology 26,567-572. van LENTEREN,J. C., EGGENKAMP-ROTTEVEELMANSVELD, M. H. & ELLENBROEK,F. J. M. (1976) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). V. Population dynamics of Trialeurodes vaporariorum and Encarsia formosa in a glasshouse. Bulletin SROPWPRS 14,125-137. van LENTEREN, J. C., HELL, H. W. & SEVENSTER-vander LELIE, L. A. (1980) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). IV. Ovipositional behaviour of the parasite with aspects of host selection host discrimination and host feeding. Zeitschrift für Angewandte Entomologie 89,442-454. - 291 - van LENTEREN, J. C., NELL, H. W., SEVENSTER-vander LELIE, L. A. & WOETS, J. (1976a) The parasite-host relationship between Enoarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) I. Host finding by the parasite. Entomologia Experimentalis et Applicata 20,123-130. van LENTEREN, J. C., NELL, H. W., SEVENSTER-van der LELIE, L. A. & WOETS, J. (1976b) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). III. Discrimination between parasitized and unparasitized hosts by the parasite. Zeitschrift für Angewandte Entomologie 81,377-380. van LENTEREN, J. C., van VIANEN, A., GAST, H. F. & KORTENHOFF,A. (1987) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). XVI. Food effects on ooogenesis, oviposition, life-span and fecundity of Encarsia formosa and other hymenopterous parasites. Zeitschrift für Angewandte Entomologie 103,69-84. van LENTEREN, J. C., WOETS, J., POEL, N. van der, van BOXTEL, W., van der MERENDONK,S., van der KAMP, R., NELL, H. & SEVENSTER-vander LELIE, L. (1977) Biological control of the greenhouse whitefly Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) by Encarsia formosa Gahan (Hymenoptera: Aphelinidae) in Holland, an example of successful ecological research. Proceedings of the International Symposium on Crop Protection. Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 42,1333-1342. (1976) LEON, E. D. de Control quimico de plagas del algodonero en la regidn del Soconusco, Chiapas. Agricultura Tecnica en Mexico 3,447-451. (1073) LEON, F. de & SIFUENTES, A. J. A. Control quimico de la mosquita blanca en algodonero en la regiön del Soconusco, this. Agricultura T&nica en Mexico 3 (7), 270-273. LEWONTIN, R. C. (1965) Selection for colonizing ability. In The genetics of colonizing species (ed. H. G. Baker & G. L. Stebbins), London; Academic Press. LINK, D. & COSTA, E. C. (1980) Ocurrencia de inimigos da mosca branca. Bemisia tabaci (Gennadius 1889), na cultura da soja. Revista do Ciencias Rurais 10 (2), 111-113. LIVDAHL, T. P. & STIVEN, A. E. (1983) Statistical difficulties in the analysis of predator functional response data. Canadian Entomologist 115, 1365-1370. LOBO-LIMA, M. L. & KLEIN-KOCH, C. (1981) Schwerpunkte in der intergrierten Bekampfung von Schadarthropoden auf den Kapverdischen Inseln (W Afrika). Mitteilungen der Deutschen Gesellshaft für Allgemeine und Angewandte Entomologie 3,60-65. LOEBENSTEIN, G. & HARPAZ, I. (1960) Virus diseases of sweet potatoes in Israel. Phytopathology 50,100-104. - 292 - LOPEZ-AVILA, A. (1987) Two new species of Encarsia Foerster (Hymenoptera: Aphelinidae) from Pakistan, associated with the cotton whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 77 (3), 425-430. LOURENS,J. H., VAN DER LAAN, P. A. & BRADER, L. (1972) Contribution h lldtude d1une Imosaiquel du cotonier au Tchad; distribution dans un champ; Aleurodidae communs; essais de transmission de cotonier par les Aleurodidae. Coton et Fibres Tropicales 27,225-230. MABBETT, T. H. (1979) Review of the economic insect pests of cotton in Thailand. Description, infestation and control. Bankok, Thailand; Cotton Pests Research Branch, Department of Agriculture. 80 pp. MABBETT, T. [H. 1 (1980) Management of four major cotton pests in Thailand. World Crops 32 (4), 101-104. MABBETT, T. [H. ] (1983) Pin-point your cotton pests. Part 2: distribution on the plant and in the field., World Crops 35 (4), 133-134. MARTIN, J. H. (1985) The whitefly of New Guinea (Homoptera: Aleyrodidae). Bulletin of the British Museum (Natural History) Entomology Series 50 (3), 303-351. L. (1910) Contribuzioni dei italiani. MASI I alla conoscenza calcididi Bolletino del Laboratorio di Zoologia Generale e Agraria Portici 4, 3-37. MATILDE-FERRERO,D. (1978) Cassava mealybug in the People's Republic of Congo. In Proceedings of the International Workshop on the cassava mealybug Phenacocus manihoti Mat. -Ferr. (Pseudococcidae) held at INERA - Mlvuazi, Bas-Zaire (ed. K. F. Nwanze, & K. Leuschner), pp. 29-46. Nigeria; International Institute for Tropical Agriculture. MERCET, R. G. (1931) Notas sobre afelinidos (Hym. Chalc) (4) (Eretmocerus, Espaflola de Entomologia T, 395-410. Coccophagus . EOS, Revista MEINERS, J. P., LAWSON, R. H., SMITH, F. F. & DIAZ, A. J. (19T3) Mechanical transmission of a whitefly-borne disease agent of beans in El Salvador. [Abstract. ] Phytopathology 63,803-804. MESSENGER, P. S. (1964) Use of life tables in a bioclimatic study of an experimental aphid-braconid wasp host-parasite system. Ecology 45, 119-131. MESSENGERtP. S., WILSON, F. & WHITTEN, M. J. (1976) Variation# fitness and adaptability of natural enemies. In Theory and practice of biological control (ed. C. B. Huffaker & P. S. Messenger), pp. 209-231. New York; Academic Press. MEYERDIRK,D. E. & COUDRIET, D. L. (1985) Predation and developmental studies of Euseius hibisci (Chant) (Acarina: Phytoseiidae) feeding on Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Ehviromental Entomology 14,24-27. MEYERDIRK, D. E. & COUDRIET, D. L. (1986) Evaluation of two biotypes of Euseius scutalis (Acari: Phytoseiidae) as predators of Bemisia tabaci (HomoptJa: Aleyrodidae) Journal of Economic Entomology 79,659'-663. - 293 - MIMEUR, J. M. (1946) Aleurodidae du Moroc (ire note). Bulletin de la Societe des sciences naturalles et physiques du Maroc 24 (1944), 87-89. MISRA, C. S., LANBA K. S. (1929) The cotton whitefly (Bemisia gossypiperda, n. sp. ). Bulletin of the Agricultural Research Institute, Pusa 196,7 pp. MONSEF, A. A. & KASHKOOLI, A. (1978) Die Baumwollweissfliege Bemisia tabaci Gen. in der Provinz Fars und die Kontrolle. Entomologie et Phytopathologie Appliquees 46 (1/2), 66-77. MORI, H. & CHANT, D. A. (1966) The influence of prey density relative humidity and starvation on the predacious behaviour of Phytosiulus persimilis Athias-Henriot (Acarina: Phytoseiidae). Canadian Journal of Zoology 44,483-491. MOSKOVETZ, S. N. (1941) Virus disease of cotton and its control. In Plant virus diseases and their control. Transactions of the conference on plant virus diseases, Moscow, 4-7/II 1940. Moscow; Institut Mikrobiologie Akademie Nauk SSSR. pp. 173-190. MOSSOP, M. C. (1932) Cultural methods and tobacco whitefly in Southern Rhodesia. Rhodesian Agricultural Journal 29,869-872. MOUND, L. A. (1962) Studies on the olfaction and colour sensitivity of Bemisia tabaci (Gern. ) (Homoptera, Aleyrodidae). Entomologia Experimentalis et Applicata 5,99-104. MOUND, L. A. (1963) Host-correlated variation in Bemisia tabaci (Genradius) (Homoptera: Aleyrodidae). Proceedings of the Royal Entomological Society of London (A) 38,171-180. MOUND, L. A. (1965a) Effect of leaf hair on cotton whitefly populations in the Sudan Gezira. Empire Cotton Growing Review 42,33-40. MOUND,L. A. (1965b) Effect of the whitefly (Bemisia tabaci) on cotton in the Sudan Gezira. Empire Cotton Growing Review 42,290-294. MOUND, L. A. (19650) An introduction to the Aleyrodidae of western Africa (Hem. ). Bulletin of the British Museum (N. H. ) Entomology 17,140-142. MOUND, L. A. (1983a) Biology and identity of whitefly vectors of plant pathogens. In Plant virus epidemiology. The spread and control of insect-borne viruses Oxford, United Kingdom; Blackwell Scientific Publications. pp. 305-313. MOUND, L. A. & HALSEY, S. M. (1978) Whitefly of the world. London and Chichester John Wiley British Museum (Natural History) 340pp MULINDANGABO,J. & BIRANDANO,B. (1984) Some problems of cassava production in Rwanda. In Integrated pest management of cassava green mite. Proceedings of a regional training workshop in east Africa ( ed. A. H. Greathead, R. H. Markham, R. J. Murphy, S. T. Murphy, I. A. D. Robertson), pp. 95-100. Ascot, United Kingdom; Commonwealth Institute of Biological Control. - 294 - MUNIYAPPA, V. (1983) Epidemiology of yellow mosaic disease of horsegram (Macrotyloma uniflorum) in southern India. In Plant virus epidemiology. The spread and control of insect-borne viruses (ed. R. T. Plumb, & J. M. 7hresh), pp. 331-335. Oxford, 1b1ted Kingdom; Blackwell Scientific Publications. MURUGESAN,S. & CHELLIAH, S. (1981) Efficacy of insecticides in the control of Bemisia tabaci (Genn. ), a vector of the yellow-mosaic virus disease on greengram. Indian Journal of Agricultural Sciences 51, 583-584. MURDOCH, W.W. & OATEN, A. (1975) Predation and population stability. Advances in Ecological Research 9,2-131. NACHAPONG,M. & MABBETT, T. (1979) A survey of some wild hosts of Bemisia - tabaci Genn. around cotton fields in Thailand. Thai Journal of Agriculiural Sciencie 12,217-222. NAIR, R.G. & NAMBIAR,T. A. (1984) India, Central Tuber Crops Research Institute. Annual progress report 1983. (For the period January- December 1983) Trivandrum, India; Central Tuber Crops Research Institute. 140 pp. NASIR, M.M. (194Ta) Chrysopa eymbele Banks and its two varieties. Indian Journal of Entomology 8,119-120. NASIR, M.M. (19471b)Biology of Chrysopascelestes Banks. Indian Journal of Entomology9,177-192. NATWICK,E. G. & ZALOHOF. G. (1984) Surveying sweetpotato whitefly in the Imperial valley. California Agriculture 38 (3/4), 11. NECHOLS,J. R. & TAUBER,M. J. (1977a) Age-specific interaction between the greenhousewhitefly and Encarsia formosa. Influence of host on the parasite's oviposition and development. Enviromental Entomology 6, 143-149. NECHOLS,J. R. & TAUBER,M. J. (1977b) Age-specific interaction between the greenhousewhitefly and Encarsia formosa. Influence of the parasite on host development. Environmental Entomology6,207-210. NELLt H.W., SENSTERvan der LELIE, L. A., WOETS,L. & van LENTEREN,J. C. (1976) The parasite-host relationship between Encarsia formosa (Hymenoptera:Aphelinidae) and Trialeurodes vaporaýiorum (Homoptera: Aleyrodidae) II. Selection of host stages for oviposition and feeding by the parasite. Zeitschrift fur AngewandteEntomologie 81,372-376. NENE,Y. L. (1973) Note on a fungus parasite of Bemisia tabaci Genn. a vector of several plant viruses. Indian Journal of Agricultural Sciences 43, 514-516. NICHOLSON,A. J. (1933) The balance of animal population. Journal of Animal Ecology 2,131-178. NICHOLSON,A.J. & BAILEY,V. A. (1935) The balance of animal ecology, Part 1. Proceedingsof the Zoological Society of London3,551-598. - 295 - NKOUKA, N., ONORE, G. & FABRES, G. (1981) Elements d'un inventaire de l'entomofaune phytophage du manioc en vue de 1' identification des insectes vecteurs de la bacteriose vasculaire. Cahiers ORSTOM,Serie Biologie 44,9-10. OHNESORGE, B. (1984) Bemisia tabaci ecology and control. Proceedings of a Symposium on Bemisia tabaci ecology and control 17th International Congress of Entomology, (ed. F. R. G. Chnesorge & D. Gerling) 19-23 August 1984, Hamburg. OHNESORGE, (1970) E. R. Parasitization of whiteflies on strawberry plants in southern California. Journal of Economic Entomology 63,1377-1378. OHNESORGE, E. R., SHARAF, N. & ALLWI, T. (1980) Population studies on the tobacco whitefly Bemisia tabaci Genn. (Homoptera; Aleyrodidae) during the winter season. I. The spatial distribution on some host plants. Zeitschrift fur Angewandte Entomologie 90,226-232. ONDIEK, J. J. (1975) Diseases and pests of passionfruit in Kenya. Acta Horticulturae 49,291-293. ORPHANIDES, G. M. & GONZALES, D. (1971) Fertility and life tables with Trichogramma pretiosum and Trichogramma retorridum (Hym. Trichogrammatidae). Annals of the Entomological Society of America 64,824-834. PARR, W.J., GOULD, H. J., JESSOP, N. H. & LUDLAM, F. A. B. (1976) Progress towards a biological control programme for glasshouse whitefly (Trialeurodes vaporariorum) on tomatoes. Annals of Applied Biology 83,349-363. PARKER, B. L., BOOTH, R. H. & BELLOTI, A. C. (1978) Bemisia tabaci identified on Manihot esculenta in Malaysia. Malaysian Applied Biology 7 (1), 85-86. PATEL, V. C. & PATEL, H. K. (1966) Inter-relationship between whitefly (Bemisia tabaci Genn. ) population and the incidence of leaf curl in bidi tobacco (Nicotiana tabacum L. ) in relation to different planting dates. Indian Journal of Entomology 28,339-344. PATI, I. & RAPISARDA, C. (1981) Reperti morfo-biologici sugli aleirodidi nocivi alle piante coltivate in Italia. Bolletino di Zoologia Agraria e di Bachicoltura 16,135-190. PATIL, S. P. & POKHARKAR,R. N. (1979) Some new records of insect pests infesting cruciferous vegetable crops in Maharashtra State. Journal of Maharashtra Agricultural Universities 4 (2), 222-223. PAULSON,G. S. & KUMASHIRO,B. R. (1985) Hawaiian Aleyrodidae. Proceedings of the Hawaiian Entomological Society 25,103-124. PERERA, C. R. (1982) Some effects of insecticide deposit patterns on the parasitism of Trialeurodes vaporariorum by Encarsia formosa. Annals of Applied Biology 101,239-244. (1955) POLLARD, D. G. Feeding habits of the cotton whitefly, Bemisia tabaci (Genn. ) (Homoptera: Aleyrodidae). Annals of Applied Biology. 43, 664-671. - 296 - POSADA, O. L., POLANIA, Z. I., AREVALO, S. I., SALDARRIAGA,V. A., GARCIA, R. F. & CARDENAS,M. R. (1976) Lista de insectos dafiinos y otras plagas en Colombia. Tercera Edicion. Boletin Tecnico. Instituto Colombiano Agropecuario ICA Programa de Entomologia 43,484 pp. PRIESNER, H. & HOSNY, M. (1934) Contribution to a knowledge of whiteflies (Aleurodidae) of Egypt (II). Bulletin Ministry of Agriculture Fgypt Technical Scientific Service. PRUTHI, H. S. & SAMUEL, C. K. (1941) Entomological investigations on the leaf-curl disease of tobacco in northern India. IV. Transmission of the disease by whitefly (Bemisia from some new alternate hosts. Indian Journal of Agricultural_gossypiperda) Science 11,387-409. PRUTHI, H. & SAMUEL, C. K. (1942) Entomological investigations on the leaf-curl disease of tobacco in northern India. V. Biology and population of the whitefly vector (Bemisia tabaci Gen. ) in relation to the incidence of the disease. Indian Journal of Agricultural Science 12,35-57. QUAINTANCE, A. L. (1900) Contribution towards a monograph of the American Aleurodidae. Technical Series. Bureau of Entomology, United States Department of Agriculture 8,9-64. RAHMAN, K. A. (1940) Short notes and exhibits. Indian Journal of Entomology 2,243. (1983) RAPISARDA, C. & PATTI, I. Stato attuale delle conoscenze sulla composizione dell'aleirofauna siciliana. In Atti 13 congresso Nazionale Italiano di Entomolgia. Istituto di Fhtomologia Agraria e Apicoltura, Universita di Torino. pp. 327-332. RAVEENDRANATH,S. (1987) Biology and behaviour of Telenomus spp. (Hymenoptera: Scelionidae) egg parasitoids attacking Spodoptera spp. (Lepidoptera: Noctuidae). Unpublished Ph. D. thesis. University of London. RECKHAUS, P. (1979) A virus disease of white yam (Dioscorea rotundata) in Togo. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 86, 763-766. REUTER, O. M. (1913) Lebensgewohnheiten und Instinkte der Insekten. Berlin; Friedlander. RICHARDS, O. W. & DAVIES, R. G. (1977) Imms' general textbook of entomology. Tenth edition. London and New York; Chapman & Hall. 1354 pp. RIZK, G. N. & ARMED, K. G. (1981) Population dynamics of some insect pests attacking squash plants, Cucurbita pepo L. in Iraq. Research Bulletin, Faculty of Agriculture, Ain Shams University 1653,8[+ 51 pp. RODRIGO,P. A. (1947) Soybean culture in the Philippines. Philippine Journal of Agriculture 13,1-22. (1972) ROGERS, D. J. Random search and insect population models. Journal of Animal Ecology 41,369-383. + RICKER, W. E. (1941) The consumption of young sockeye salmon by predaceous fish. Journal of the Fisheries Research Board of Canada 5: 293-313. - 297 - ROSEN, D. & DEBACH, P. (1979) Species of Aphytis of the world. The Hague, Boston, London; W. Junk. ROYALSTATISTICAL SOCIETY (1977) The GLIM System Release 3.11 RUSSELL, L. M. (1948) The North American species of whiteflies of the genus Trialeurodes. Miscellaneus Publications. United States Department of Agriculture 635,85 pp. RUSSELL, L. M. (1958) Synonyms of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Bulletin of the Brooklyn Entomological Society 52 (5), 122-123. RUSSELL, L. M. (1975) Collections of records of Bemisia tabaci (Gennadius) in the United States (Hemiptera: Homoptera: Aleyrodidae). Cooperative Economic Insect Report 25 (12), 229-230. RUSSELL, L. M. & ETIENNE, J. (1985) A list of Aleyrodidae of the Island of Reunion. Proceedings of the Entomological Society of Washington 87, 202-206. RUSSO, G. (1942) I parasiti animali dannosi alle coltivazioni di cotone. Ricerche ed osservazioni eseguite in Italia nel 1941. Annali della Facolta di Agraria della Universita di Pisa (N. S. ) 5,436-480. SAMUEL, C. K. (1951) Parasites and parasitism of the whitefly, Bemisia tabaci (Gern. ) vector of tobacco leaf-curl in northen India. Indian Journal of Entomology 12 (1950), 248-250. SANTIS, L. de (1981) Sobre dos especies de Encarsia (Hymenoptera, Aphelinidae) del Brasil parasitoides de Benisia tabaei (Homoptera: Aleyrodidae). Revista Prasileira de Entomologia 25,37-39. SATYAVIR (1983) Efficacy of some important insecticides in the control of Bemisia tabaci (Gern. ) a vector of the yellow mosaic disease on mothbean. Indian Journal of Plant Protection 11 (1/2), 31-33. SAUTI, R. F. N. (1982) Malawi. In ' Ds in eastern Africa. Proceedings of workshop held at Kigali, Rwanda, 23-27 November Ottawa, Canada; International Development Research Centre. pp. 1 SAUTI, R. F. N. (1984) Distribution, utilization and production constraints of cassava in Malawi. In Integrated pest management of cassava green mite. Proceedings of a regional training worshop on East Africa, 30 April -4 May 1984 (ed. A. H. Greathead, R. H. Markham, R. J. Murphy, S. T. Murphy & I. A. D. Robertson), pp. 81-86. Ascot, United Kingdom; Commonwealth Institute of Biological Control. SCOPES, N. E., RANDALL, R. E. & BIGGERSTAFF, S. M. (1975) Constant temperature, ventilated perspex cage for rearing phytophagous insects. Glasshouse Crops Research Institute, Littlehampton, Sussex. Reprinted from Laboratory Practice, pp. 33-34. SEIF, A. A. (1981a) Seasonal fluctuation of adult population of the whitefly, Bemisia tabaci, on cassava. Insect Science and its Application 1, 363-364. - 298 - SEIF, A. A. (1981b) Transmission of cassava mosaic virus by Bemisia tabaci. Plant Disease 65,606-607. §ENGONCA, C. (1975) Beitrag zum epidemischen Auftreten der Tabakmottenshildlaus, Bemisia tabaci Genn., an Baumwollpflanzen in Sudanatolien (Homoptera: Aleyrodidae). Anzeiger fOr Schddlingskunde, Pflanzenschutz, Umweltschutz 48 (9)0 140-142. SHARE, S. A. & RIZVI, S. (1982) A new species of Encarsia Foerster (Hymenoptera: Aphelinidae) from Pakistan. Journal of EnFomological Research 6,157-158. SHAHEEN, A. H. (1977a) Survey of pests attacking tomato in Egypt with some ecological notes. Agricultural Research Review 55 (1), 49-57. SHAHEENpA. H. (1977b) Survey of pests attacking soybean plants in Egypt with some ecological notes. Agricultural Research Review 55 Mp 59-65. SHAHEEN,A. H. (1983) Some ecological aspects of the whitefly, Bemisia tabaci Gem., om tomato. Bulletin de la Societ4- Entomologique dlEgypte 62 (1978/79), 83-87. SHANAB, L. M. & BWAD-ALLAH, S. S. (1982) Studies on the whitefly (Bemisia tabaci Gem. ) infesting tomato at Mansoura District, Egypt. Acta Phytopýthologica Academiae Scientiarum Hingariae 17 (1/2), 147-155. SHARAF, N. (1984) Ecology and control of the sweetpotato, whitefly (Bemisia tabaci. Genn., Homoptera: Aleyrodidae) in Jordan. 11 (7), 45-56. -Dirasat SHARAF, N., AL-MUSA, A. & NAZERj 1. (1984) The impact of three irrigation methods on the whitefly (Bemisia tabaci Genn. ) population and the incidence of tomato yellow leaf curl disease in Jordan. Dirasat 11 (7), 109-117. SHARAF, N. & BATTA, Y. (1985) Effect of some factors on the relationship between the whitefly Bemisia tabaci Gem. (Homptera: Aleyrodidae) and the parasitoid Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae). Zeitschrift ffir Angewandte Entomologie 99,267-276. SHARAF, N. S. (1982) Parasitization of the tobacco whitefly Bemisia tabaci Gem., (Hom., Aleyrodidae) on Lantana camara L. in the Jordan Valley. Zeitschrift fiAr Angewandte Entomologie 94,263-271. SHARAF, N. S., AL-MUSA, A. M. & NAZER, I. K. (1984) Control of the tomato yellow leaf curl virus in Jordan. I. Effect of two irrigation regimes alone or in combination with pirimiphos-methyl on whitefly (Bemisia tabaci Genn. ) population and the incidence of tomato yellow leaf curl virus. Zeitschrift fUr Pflazenkrankheiten und Pflanzenschutz 91, 404-410. SHEFFIELD, F. M.L. (1957) Virus disease of sweet potato in East Africa. I. Identification of the viruses and their insect vectors. Phytopathology 47,582-590. SHEFFIELD, F. M.L. (1958) Virus disease of sweet potato in East Africa. II. Transmission to alternative hosts. Phytopathology 48,1-16. - 299 - SHIRES, S., MURRAY,A. & SADIG, S. (1983) Stickiness in cotton: progress in solving the problem. Shell Agriculture May, 1-2. SHIVANATHAN, P. (1983) The epidemiology of three diseases caused by whitefly-borne pathogens. In Plant virus epidemiology. The spread and control of insect-borne viruses (ed. R. T. Plumb & J. M. Thresh), pp. 323-330. Oxford, United Kingdom; Blackwell Scientific Publications. SIDDING, S. A. (1984) Shambat Research Station. Entomology Section. In Annual report of the Gezira Research Station and substations, Sudan, Sudan; Ministry Agriculture Irrigation. . of and pp. SINHA, S. N. & CHAKRABARTI,A. K. (1982) Studies on control on the control of yellow vein mosaid in okra seed. Vegetable Science 9 (1), 64-69. SMEE, C. (1933) Report of the Entomologist. Report. Department of Agriculture, Nyasaland 1932,48-52. SMITH, H. S. (1919) On some phases of insect control by the biology method. Journal of Economic Entomology 12,288-292. SOLIMAN, Z. R., SHEHATA, K. K. & GOMAA, E. A. (1976) on the food range and economic importance of the predatory mite Agistemus exsertus Gonz. (Atari, Prostigmata). Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz 49 (6), 87-90. SOLOMON, M. E. (1949) The natural control of animal population. Journal of Animal Ecology 18,1-35. SOUTHWOOD,T. R. E. (1978) Ecological methods with particular reference to the study of insect population. 2nd edition. Chapman and Hall. pp. 367-375. SPEYER, E. R. (1927) An important parasite of the greenhouse whitefly. Bulletin of Entomological Reserach 17,301-308. STATGRAPHICS (1986) Statistical graphics system. Statistical Graphics Corporation. SWIRSKI, E., AMITAI, S. & DORZIA, N. (1967) Laboratory studies on the feeding development and reproduction of the predaceous mite Amblyseius rubini Swirski and Amitai and Amblyseius swirski Athias (Acarina: Phytoseiidae) on various kinds of food substances. Israel Journal of Agricultural Research 17,101-119. SWIRSKI, E., AMITAI, S. & DORZIA, N. (1970) Laboratory studies on feeding habits, post-embryonic survival and oviposition of the predaceous mites Amblyseius chilenensis Dosse and Amblyseius hibisci Chant (Aoarina: Phytoseiidae) on various kinds of food substances. Entomophaga 15,93-106. SWIRSKI, E. & DORZIA, N. (1968) Studies on the feeding, development and oviposition of the predaceous mite Amblyseius limonicus Garman and McGregor (Acarina: Phytoseiidae) on various kinds of food substances. Israel Journal of Agricultural Research 18,71-75. - 300 - TAKAHASHI, R. (1936) Some Aleyrodidae, Aphididae, Coccidae (Homoptera), and Thysanoptera from Micronesia. Tenthredo 1 (2), 109-120. TAKAHASHI, R. (1955) Bemisia and Acanthobemisia of Japan (Aleyrodidae, Homoptera). Kontyu 23 (1), 1-5. TEICH, Y. (1966) Mites of the family Phytoseiidae as predators of the tobacco whitefly, Bemisia tabaci Gennadius. Israel Journal of Agricultural Research 16,141-142. THEWYS, G., HERVE, J. J. & LARROQUE, M. (1979) Bilan de deux anndes d'experimentation de la decamethrine sur cotonier en milieu paysan au Senegal. In Congres sur la lutte contre les insectes en milieu tropical. Chambre de Commerce et d'Industrie de Marseille, 13-14 Mars 1979. Compte rendu des travaux. Marseilles, France; Chambre de Commerce et d' Industrie. pp. 115-126. THOMAS, R. (1923) Periodic failure of the Punjab-American cotton crop. Agriculture and Live-stock in India 2 (3), 243-274. TREMBLAY, E. (1959) Osservazione sulla simbiosi endocellulare de alcuni Aleyrodidae (Bemisia tabaci Gennad. Aleurobolus olivinus Silv. Trialeurodes vaporariorum West. ) Bolletino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici 17,210-246. TURHAN, N., TUNg, A., BELLI, A., KISMIR, A. & KISAKÜREK, N. (1983) cukurova'da soya (Glycine max L. ) 'da böeek ve akar faunasinin tesbiti üzerinde calismalar. Bitki Koruma B01teni 23 (3), 148-169. TWAFIK, M. F. S., AWADALLAH,K. T., HAFEZ, M. & SARHAN, A. A. (1983) Biology of the aphelinid parasite Eretmocerus mundus Mereet. Bulletin de la Societe Entomologique d'Egypte 62 (1978/1979), 33-48. ULLYETT, G. C. (1949) Distribution of progeny by Chelonus texanus Cress. (Hymenoptera: Braconidae) Canadian Entomologist 81,25-44. UYGUN, N. & ÖZGÜR, F. (1980) Icel ve Adana illeri sera sebze zararlilarini saptanm, asi, endosülfan Rooktablet ve primicarb'in Myzus persicae (Sulz. ) 'ye etkileri. Turkiye Bitki Koruma Dergisi 4 (3), 185-192. [With German summary. ] van VIANEN, A. & van LENTEREN,J. C. (1986b) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). XV. Oogenesis and oviposition of Encarsia formosa. Zeitschrift for Angewandte Entomologie 102, 130-139. van VIANEN, A. & van LENTEREN, J. C. (1982) Increasing the number of ovarioles of Encarsia Formosa a possibility to improve the parasite for biological control of the greenhouse whitefly Trialeurodes vaporariorum? Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 47 (2), 523-531. van VIANEN, A. & van LEUTEREN, J. C. (1986a) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). XIV. Genetic and environmental factors influencing body-size and number of ovarioles of Encarsia formosa Zeitschrift für Angewandte Entomologie 101,321-331. - 301 - VARLEY, G. C., GRALMELL, G. R. & HASSELL, M. P. (1973) Insect population ecology. Oxford; Blackwell Scientific Publications. VET, L. E. M. (1980) Laboratory studies on three Encarsia spp. and one Eretmocerus sp. (Hym.: Aphelinidae) parasites of the greenhouse whitefly Trialeurodes vaporariorum (Westw. ) to assess their efficiency as biological control. Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 45 (3), 555-561. VET, L. E. M. & van LENTEREN, J. C. (1981) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). X. A comparision of three Encarsia spp. and one Eretmocerus sp. to estimate their potentialities in controlling whitefly on tomatoes in greenhouses with a low temperature regime. Zeitschrift für Angewandte Entomologie 91,327-348. ) VET, L. E. M., van LENTEREN, J. C. & WOETS, J. (1980) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). IX. A review of the biological control of the greenhouse whitefly with suggestion for future research. Zeitschrift für Angewandte Entomologie 90,26-51. VETTEN, H. J. & ALLEN, D. J. (1983) Effects of environment and host on vector biology and incidence of two whitefly-spread diseases of legumes in Nigeria. Annals of Applied Biology 102,119-227. VIGGIANI, G. (1982) New species and host records of African aphelinids (Researches on Hymenoptera Chalcidoidea LXX). Journal of the Entomological Society of Southern Africa 45 (1), 27-32. VIGGIANI, G. (1984) Bionomics of the Aphelinidae. Annual Review of Entomology 29,257-76. VIGGIANI, G. & BATTAGLIA, D. (1983a) Le specie italiani del genere Eretmocerus Hald. (Hymenoptera; Aphelinidae). Bolletino del Laboratorio di Entomologia Agraria 'Filippo Silvestri', Portici40, 97-101. VIGGIANI, G. & BATTAGLIA, D. (1983b) Courtship and mating behaviour in some Aphelinidae Bolletino del Laboratorio de Entomologia Agraria 'Filippo Silvestri$, Portici 40,102-105. VIGGIANI, G. & MAZZONE, P. (1980) Le specie paleartiche di Encarsia del grupo lutea Iasi (Hym. Aphelinidae), con descrizione di due nuove specie. Bolletino del Laboratorio di Entomologia Agraria 'Filippo Sivestri', Portici 37,51-57. VOLTERRA, V. (1926) Variazioni e fluttuazioni del numero d'individui in specie animali conviventi. Mem Accad. Lincci ser 6 (3), 31-112. WAAGE, J. K. (1982) Sib-mating and sex ratio strategies in soelionid wasps. Ecological Entomology 7,103-112. - 302 - WAAGE, J. K. & GREATHEAD,D. J. (1988) Biological control: challenges and opportunities. In Biological control of pests, pathogens and weeds: developments and prospects. (ed. R. K. S. Wood & M. J. Way). Philosophical Transactions of the Royal Society of London B 318, 111-128. WAAGE,J. K. & HASSELL, M. P. (1982) Parasitoids as biological control agents- a fundamental approach. Parasitology 84,241-268. WALTER, G. H. (1983) Divergent male ontogenies in Aphelinidae (Hymenoptera: Chalcidoidea); a simplified classification and a suggested evolutionary sequence. Biological Journal of the Linnean Society 19 (1), 63-82. WANGBOOKONG,S. (1981) Chemical control of cotton insects pests in Thailand. Tropical Pest Management 27,195-500. WILLIAMS, F. M. & JULIANO, S. A. (1985) Further difficulties in the analysis of functional response experiments and a resolution. Canadian Entomologist 117,631-640. WILLIAMS, J. R. (1977) Some features of sex linked hyperparasitism in Aphelinidae (Hymenoptera) Ehtomophaga 22,345-350. WILLIS, J. C. (1973) (Eighth Edition revised by H. K. Airy Shaw) A dictionary of the flowering plants and ferns. London, U. K.; Cambridge University Press. 1245 + lxvi pp. WOODWARD,T. E., EVANS, J. W. & EASTHOP,V. F. (1970) Hemiptera. In The insects of Australia, Commonwealth Scientific and Industrial Research Organization (CSIRO), pp. 387-457. Melborne, Australia University Press. YEIN, B. R. (1981) Relative efficacy of certain insecticides against cotton pests. Journal of Research, Assam Agricultural University 2 (2), 196-201. ZINNA, G. (1961) Ricerche sugli insetti entomofagi. II. Specializzazioni entomoparassitica negli Aphelinidae: Studio morfologico, etologico e fisiologico del Coccophagus' bivittatus Compere nuovo parassita del Coccus hesperidum L. per l'Italia. Bolletino del Laboratorio di Entomologia agraria 'Filippo Silvestri', Portici 19,301-358. ZINNA, G. (1962) Ricerche sugli insetti entomofagi. III. Specializzazioni entomoparassitica negli Aphelinidae: Interdipendenze biocenotiche tradue specie associate. Studio morfologico, etologico e fisiologico del Coccophagoides similis (Masi) e Azotus matritensis Mercet. Bolletino del Laboratorio di E tomologia agraria 'Filippo Silvestri', Portici 20,73-182. ZWÖLFER, H., GHANI, M. A. & RAO, V. P. (1976) Foreign exploration and importation of natural enemies. In Theory and Practice of biological (ed. control C. B. Huffaker & P. S. Messenger), pp. 189-207. New York; Academia Press.