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Biological control of the citrus blackfly (Aleurocanthus woglumi Ashby) by Prospaltella opulenta Silv. in central-western Venezuela

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Title:
Biological control of the citrus blackfly (Aleurocanthus woglumi Ashby) by Prospaltella opulenta Silv. in central-western Venezuela with a review of the pest's invasion of the Western Hemisphere and suppression by introduced parasites
Added title page title:
Aleurocanthus woglumi
Added title page title:
Prospaltella opulenta
Creator:
Chavez Torres, Hugo A., 1945-
Publication Date:
Language:
English
Physical Description:
xiii, 118 leaves : ill. ; 28 cm.

Subjects

Subjects / Keywords:
Adult insects ( jstor )
Eggs ( jstor )
Female animals ( jstor )
Infestation ( jstor )
Instars ( jstor )
Nymphs ( jstor )
Orchards ( jstor )
Parasite hosts ( jstor )
Parasites ( jstor )
Pupae ( jstor )
Citrus black fly -- Venezuela ( lcsh )
Citrus black fly -- Biological control ( lcsh )
Dissertations, Academic -- Entomology and Nematology -- UF
Entomology and Nematology thesis Ph. D
Genre:
bibliography ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis--University of Florida.
Bibliography:
Bibliography: leaves 109-117.
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Hugo A. Chavez Torres.

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University of Florida
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University of Florida
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BIOLOGICAL CO: TROL OF THE CITRUS BLACKFLY (ALEUROCANITHUS WIOGLiMI
ASHBY) BY PRUSPALTELLA OPULENTA SILV. IN CENTR' L-W ESTFRW VEiNEZUELA
WIH A RPEVIEI OF THE PEST'S INVASION OF THE WESTERN HEMlISPHERE
AND SUPPRESSION BY INTRODUCED PARASITES








BY


HUGO A. CHAVEZ TORRES


A DISS' NATION P.F Vh-D TO Tfi GRADUATF COUNCIL OF THE
U IVERSITY OF FLORIDlA iN PARTIAL FULFILLMENT OF THE
REQUIREENTS FOP? THE DEGREE OF
DOCTOR OF PHILOS PH"'


UNIVERSITY OF FLORIDA


1930
















Dedicated


to


My Parents Alejandro and Basilisa

My Wife Maria Ines

My Son Luis Alejandro

My Daughters Maria Sofia and Monica Maria

The Universidad Centro Occidental Lisandro Alvarado

My Students














ACKNOWLEDGEMENTS


I am deeply indebted to the Chairman of my graduate committee,

Dr. Reece Sailer, for his suggestions, guidance, assistance and

advice throughout this study.

Special thanks are extended to Dr. Donald E. Short, Dr. James L.

Nation, Dr. Jerry L. Stimac, and Dr. Francis W. Zettler who served as

members of the author's supervisory committee for critical review of

the first draft of the dissertation.

I am personally grateful to Mr. A. Martinez (Hacienda Santa Lucia),

Juconasa Industries (Apoliro Experimental Orchard), and Mr. G. Gascon
(Gloria de Lara) whose valuable collaboration helped greatly to make

possible this study, and to the team of Entomology of the Escuela de

Agronomia (UCOLA) for its valuable collaboration, encouragement and

support.

I wish to express my gratitude to Ing. Agr. Hector Ochoa Z.,

Rector of the Universidad Centro Occidental Lisandro Alvarado, to

Ings. Agrs. Orlando Molina and Omar Gimenez, Directors of the Escuela

de Agronomia, to Consejo Asesor de Investigaciones y Servicios,

whose support made this study possible, to ings. Agrs. Francis

Geraud, Nancy de Martinez and Jorge Teran for their cooperation in

obtaining stock of Prospaltella opulenta for purposes of this study

and to Ing. Agr. Liz de Rodriguez for her assistance and guidance in

the statistical analysis.








I wish also to remember Dr. hilledge Murphy, former member of
the supervisory committee and professor of the University of Florida,

now deceased.
I extend my sincerest appreciation to my wife, Maria Ines, for

her support and enthusiasm during the time of the study.

Finally, I am deeply indebted to Dr. Jose M. Osorio, professor

of the Escuela de Agronomia (UCOLA) who introduced me to entomology

and through his teaching, general guidance and assistance encouraged

me to seek a career in this field.















TABLE OF CONTENTS

CHAPTER PAGE

ACKNOWLEDGEMENTS ....... .................... iii

LIST OF TABLES ....................vi

LIST OF FIGURES ........ .................. ..viii

ABSTRACT ........ ....................... ... xi

INTRODUCTION .......... ...................... 1

II A REVIEW OF LITERATURE .......... ............ 3

Taxonomic Position, Synonymy and Common Names 3
Origin and Distribution ....... .............. 4
Biology ................. .............. 10
Life History ......... .... ........... ... 13
Host Plants .... ..... ................ ... 16
Damage or Injury ..... ............... ... 18
Diological Control in the Western Hemisphere 18
Countries of the Western Hemisphere Where Natural
Enemies Have Been Introduced for Control of
Citrus Blackfly .... ............ ..... ... 25

III BIOLOGICAL CONTROL OF CITRUS BLACKFLY IN THE CENTRAL-
WESTERN REGION OF VENEZUELA ... ............. ....36

Materials and Methods .... ............... ... 37
Host Plants ........ ................. 37
Locations ...... ........ ... ........ 37
Sampling Procedure .... .............. ....38
Count .. ... .................... 38
Mortality Factors.. .... ............ ... 39
Statistical Analysis ....... ........... 39
Parasite ..................39
Results ............................... .....40
Hacienda Santa Lucia ...... ............. 40
Apoliro Experinental Orchard ........... ....61
Gloria de Lara Citrus Orchard .... ........ 79
Statistical Analysis ...... ............. 97
Discussion ............................ ...105

LITERATURE CITED ....................109

BIOGRAPHICAL SKETCH ...... .................. ...118














LIST OF TABLES


TABLE PAGE

1 PERCENT HEALTHY AND DEAD NYMPHAS OF A. WOGLUMI ON 60
SAMPLED LEAVES PER DATE LOCALITY: YARITAGUA
(HACIENDA "SANTA LUCIA") ... ............ .... 48

2 SUMMARY OF MONTHLY DATA RELATING TO TEMPERATURE,
RELATIVE HUMIDITY, RAINFALL AND EVAPORATION FOR
"APOLIRO" AND "SANTA LUCIA" ORCHARDS ............. 51

3 EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED
LEAVES PER DATE LOCALITY: YARITAGUA (HACIENDA
"SANTA LUCIA") ............ ..... ....55

4 PERCENT PARASITISM OF DISSECTED LIVE FORMS OF
A. WOGLUMI ON 60 LEAVES PER SAMPLE
LOCALITY: YARITAGUA (HACIENDA "SANTA LUCIA") . 58

5 PERCENT HEALTHY AND DEAD NYMPHS OF A. WOGLUMI ON 60
SAMPLED LEAVES PER DATE LOCALITY: CABUDARE
("APOLIRO" EXPERIMENTAL ORCHARD) .............. ....70

6 EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED
LEAVES PER DATE LOCALITY: CABUDARE ("APOLIRO"
EXPERIMENTAL ORCHARD) ...... .............. .... 72

7 PERCENT PARASITISM OF DISSECTED LIVE FORMS OF
A. WOGLUMI ON 60 LEAVES PER SAMPLE LOCALITY:
CABUDARE ("APOLIRO" EXPERIMENTAL ORCHARD) ... ...... 77

8 EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED
LEAVES PER DATE LOCALITY:SAiRARE ("GLORIA DE
LARA" CITRUS ORCHARD) .......... ............. 84

9 SUMMARY OF MONTHLY DATA RELATING TO RAINFALL FOR
"GLORIA DE LARA" CITRUS ORCHARD ............. .... 86

10 PERCENT HEALTHY AND DEAD NYMPHS OF A. WOGLUMI ON 60
SAMPLED LEAVES PER DATE LOCALITY: SARARE
("GLORIA DE LARA" CITRUS ORCHARD) ..... .......... 90

11 PERCENT PARASITISM OF DISSECTED LIVE FORMS OF A.
WOGLUHI ON 60 LEAVES PER SAMPLE LOCALITY:-
SARARE ("GLORIA DE LARA" CITRUS ORCHARD) .......... 95










12 CORRELATION COEFFICIENTS FOR SQUARE CENTIMETER AND
TOTAL LEAF COUNTS FOR EACH VARIABLE STUDIED AT
HACIENDA SANTA LUCIA ........ ................. 98

13 CORRELATION COEFFICIENTS FOR SQUARE CENTIMETER AND
TOTAL LEAF COUNTS FOR EACH VARIABLE STUDIED AT
APOLIRO EXPERIMENTAL ORCHARD ................ ....99

14 CORRELATION COEFFICIENTS FOR SQUARE CENTIMETER AND
TOTAL LEAF COUNTS FOR EACH VARIABLE STUDIED AT
GLORIA DE LARA CITRUS ORCHARD .... ............ 100

15 PREDICTION EQUATION INCLUDING THE LINEAR AND QUADRATIC
EFFECT OF THE COUNT PER SQUARE CENTIMETER AND R2
VALUES FOR HACIENDA SANTA LUCIA ............. l.. 101

16 PREDICTION EQUATION INCLUDING THE LINEAR AND QUADRATIC
EFFECT OF THE COUNT PER SQUARE CENTIMETER AND R2
VALUES FOR APOLIRO EXPERIMENTAL ORCHARD ... ....... 102

17 REGRESSION COEFFICIENTS, STANDARD ERROR AND PROBABILITY
>Itl FOR EGGS, NYIIPHAL (FIRST, SECOND, AND THIRD
INSTAR) AND PUPAE FOR HACIENDA SANTA LUCIA.. .... 103

18 REGRESSION COEFFICIENTS, STANDARD ERROR AND PROBABILITY
>Itl FOR EGGS, NYMPHAL (FIRST, SECOND, AND THIRD
INSTAR) AND PUPAE FOR APOLIRO EXPERIMENTAL ORCHARD. 104


TABLE


PAGE














LIST OF FIGURES


FIGURE PAGE

I Map showing the countries and dates where the citrus
blackfly has been reported in the Western
Hemisphere ........ ...................... 7
2 Places where P. opulenta has been released in Venezuela
and where A. woglumi was first observed ... ....... 34

3 Hacienda Santa Lucia, Yaritagua. ............... ..41

4 Egg and adult populations of A. woqglumi observed on
leaves of C. sinensis var. "California" at Hacienda
Santa Lucia, Yaritagua ...... ................ 42

5 First, second, and third nymphal instars of A. wogiumi
observed on leaves of C. sinensis var. "California"
at Hacienda Santa Lucik, Yrtagua. .............. 43

6 Total, healthy, and dead first nymphal instar popula-
tions of A. woglumi observed on leaves of C.
sinensis var. "California" at Hacienda Santa
Lucia, Yaritagua ........ .................. 45

7 Total, healthy, and dead second nymphal instar popula-
tions of A. woglumi observed on leaves of C.
sinensis var. "California" at Hacienda Santa
Lucia, Yaritagua ...... ................... 46

8 Total, healthy, and dead third nymphal instar popula-
tions of A. woqlumi observed on leaves of C.
sinensis var. "California" at Hacienda Santa
Lucia, Yaritagua ...... ................... 47

9 Average monthly temperature, relative humidity,
rainfall, and evaporation (shadow) for Santa Lucia
and Apoliro Citrus Orchards ."...... ..... 50

10 Total, healthy, dead, and parasitized pupa populations
of A. woglumi observed on leaves of C. sinensis var.
"California" at Hacienda Santa Lucia, Yaritagua 54

I1 Percent healthy and parasitized (with hole) pupae and
percent dissected parasitism of A. woglumi observed
on leaves of C. sinensis var. "California" at
Hacienda Santa Luca, Yaritagua .... ........... 57
viii








FIGURE


PAGE


12 Apoliro Experimental Orchard, Cabudare ..... ....... 62

13 Egg and adult populations of A. woqlumi observed on
leaves of C. sinensis var. "Pineapple" at Apoliro
Experimental Orchrd, Cabudare ..... ........... 63

14 First, second, and third nymphal instars of A. woglumi
observed on leaves of C. sinensis var. "Pineapple"
at Apoliro Exprimental Orchard, Cabudare ... ...... 64

15 Total, healthy, and dead first nymphal instar
populations ofA. woqlumi observed on leaves of
C. sinensis var. "Pineapple" at Apoliro Experi-
mental Orchard, Cabudare ...... ............. 66

16 Total, healthy, and dead second nymphal instar
populations of A. woglumi observed on leaves of
C. sinensis var. "Pineapple" at Apoliro Experi-
mental Orchard, Cabudare ...... ............. 68

17 Total, healthy, and dead third nymphal instar
populations of A. woglumi observed on leaves of
C. sinensis var. "Pineapple" at Apoliro Experi-
mental Orchard, Cabudare ..... ............... 69

18 Total, healthy, dead, and parasitized pupa popula-
tions of A. woglumi observed on leaves of
C. sinensis var. "Pineapple" at Apoliro Experi-
mental Orchard, Cabudare ..... ............. 75

19 Percent healthy and parasitized (with hole) pupae
and percent dissected parasitism of A. woglumi
observed on leaves of C. sinensis var.
"Pineapple" at Apoliro Experimental Orchard,
Cabudare ...... ..................... .... 76

20 Glorida de Lara, Sarare ......... .... ..... .... 80

21 Egg and adult populations of A. woglumi observed on
leaves of C. sinensis var. "Valencia" at Gloria
de Lara,.Sarare ........ .................. 82

22 First, second, and third nymphal instars of
A. woglumi observed on leaves of C. sinensis var.
"Valencia" at Glorida de Lara, Sarare ........... 83

23 Total, healthy, and dead first nymphal instar
populations of A. woglumi observed on leaves of
C. sinensis var. "Valencia" at Gloria de Lara,
Sarare ...... ....................... 87








FIGURE


24 Total, healthy, and dead second nymphal instar
populations of A. woqlumi- observed on leaves of
C. sinensis var. "Valencia" at Gloria de Lara,
Sarare ....... .. ........................ 88

25 Total, healthy, and dead third nymphal instar
populations of A. woql_umi observed on leaves of
C. sinensis var. "Valencia" at Gloria de Lara,
Sarare. ... ... ...................... 89

26 Total, healthy, dead, and parasitized pupa popula-
tions of A. woglumi observed on leaves of
C. sinensis var. "Valencia" at Gloria de Lara,
Sarare ........ ........................ 92
27 Percent healthy and parasitized (with hole) pupae and
percent dissected parasitism of A. woglumi observed
on leaves of C. sinensis var. "Valencia" at
Gloria de Lara, Sarare .... ................ ...94


PAGE














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

BIOLOGICAL CONTROL OF THE CITRUS BLACKFLY (ALEUROCANIHUS WOGLUMI
ASHBY) BY PROSPALTELLA OPULENTA SILV. JN CENTRAL-WESTERN VENEZUELA
WITH A REVIEW OF THE PEST'S INVASION OF THE WESTERN HEMISPHERE
AND SUPPRESSION BY INTRODUCED PARASITES

By

Hugo A. Chavez Torres

June 1980

Chairman: R. I. Sailer
Major Department: Entomology and Nematology
The citrus blackfly, Aleurocanthus woglumi Ashby, is assumed to

be a native of India, India and Pakistan, South Asia, Southern China, and

Asia. Specimens were first received by USDA, Entomology, in 1910

from Maxwell-Lefroy in India. The first report of A. wo lumi in the

Western Hemisphere was made by Ashby in Jamaica in 1915. From here

the citrus blackfly invaded other countries and now is widely dis-

tributed in the Western Hemisphere.

The introduction of the natural enemies from Asia to the Western

Hemisphere can be divided into 2 stages. The first stage began in

1930, with shipment of Eretmocerus serius from Malaya to Cuba, where

it was successfully established and controlled the citrus blackfly.

This parasite was later introduced into other countries of the

Hemisphere. The second stage began in 1949, with the shipment of

parjisitized material from India and Pakistan to Mexico. Of the








species of parasites received in Mexico, Amitus hesperidum,

Prospaltella opulenta, and P. clypealis proved to be the most ef-

fective in the control of tile pest and were later introduced into

other countries of the Hemisphere.

After being found and eradicated by means of chemical applica-

tions from Florida (1937) and Texas (1955), the citrus blackfly

reinvaded Texas in 1967 and Florida in 1976. It proved unfeasible,

if not impossible, to eradicate these infestations, and both are now

effectively controlled by parasites. Parasites have provided highly

satisfactory control in all infested countries where they have been

introduced. When earlier control seemed to break down (Jamaica),

the situation was corrected by introduction of a second species of

parasite. In Mexico, where adverse climatic or cultural factors

cause sporadic local outbreaks, control is reestablished by reintro-

ducing parasites from localities where they are abundant.

In Venezuela, A. woglumi was first found in 1967 at San Antonio

del Tachira and was first observed in Barquisimeto in 1968. By 1974,

the citrus blackfly was widespread through all the country. The

first shipment of Prospaltela opulenta from Mexico was received in

1975. Additional shipments were received in June 1976, and positive

evidence of establishment was obtained between June and September.

Beginning November 11, 1976, egg, nymphal, pupal and adult stages of

the citrus hackfly were sampled at 3 citrus grove locations. The

sample procedure included standardized leaf counts for the immature

stages. Adult populations were determined by visual counts. Leaf

samples included square centimeter counts and were compared with

whole leai counts in an effort to establish reliability of the less








laborious square inch method showing high correlation coefficients.

Mortality factors were identified in the field as well as in the leaf

samples; however, the combined effect of these observed and suspected

mortality factors did not prevent the increase of citrus blackfly

populations when more favorable conditions returned. After the release

of P. opulenta the number of dead citrus blackflies increased as an

effect of parasite host feeding as well as by stinging activity of

the female parasite that fails to result in parasite development.

Scales sp., a native parasite, probably played an important role as a

host of the male P. opulenta which develops as secondary parasite and

thus hastened the establishment and colonization of P. opulenta. As

the introduced parasite increased to a level having a measurable

effect on the host population, Cales sp. was displaced as a parasite

of A. woglumi. The increase of the P. opulenta population was

followed and its impact on the host population established. Complete

biological control was achieved in 18 months after P. opulenta was

released in the Central-Western region of Venezuela.


xiii













CHAPTER I
INTRODUCTION

Citrus is second only to apples in world trade. They belong to

six genera, namely, Fortunella, Eremocitrus, Clymenia, Poncirus,

Microcitrus and Citrus, but from an economic point of view, only

Fortunella, Poncirus and Citrus are important (Chapot, 1975). Fortunella

(kumquats), Poncirus (trifoliate orange) and Citrus (shaddock, mandarin,

sour orange, sweet orange, lime, citron, lemon, and other types of fruits

including natural hybrids) are native to a very large asiatic area. The

grapefruit is an exception. It (C. paradisi Macfadyen) appeared, prob-

ably as a hybrid, in Barbados (West Indies). The 2 main species of

Fortunellaare native to Southern China and the genus Poncirus to

Central and Northern China. The mandarin (C. reticulata Blanco) is

believed to be native to Indochina and Southern China, the lime

(C. aurantifolia Swingle) to the East Indian Archipelago, the shaddock

(C. grandisOsbeck) to the East Indian Archipelago, the citron (C.

medica L.) to Southern China and India. The origin of lemon (C. limon

Burmann) is totally unknown, the sweet orange (C. sinensis Osbeck)

probably originated in Indochina and Southern China, and the sour

orange (C. aurantium L.) is possible indigenous to India (Chapot, 1975).

Citrus crops are grown in a belt between 40' north and 400 south

latitude, high elevations excepted. In the equatorial part of this

belt (15' north and south) constant high temperature induces several

crops a year, poor coloration of fruit and fast development of pests.





2

Subtropical, temperate and mediterranean types of climates character-

ized by low humidity, a cold winter and considerable daily change of

temperature ind-luces good color, tastier flesh and uniform ripening of

the crop. Beyond the 400 latitude, the problem of recurrent freezes

can to a certain extent be alleviated by choice of particular scion

and rootstock varieties.

Semitropical Florida, Brazil and Japan fall between these 2 zones

and have intermediate characteristics (Chapot, 1975).

Citrus fruits are marketed not only as table fruit, but as

processed products in the form of beverage flavor bases, frozen con-

centrates, chilled pasteurized juice, canned single-strength juice,

lime and lemonades, canned segment, salads, cosmetics, perfumes, dye-

stuffs and many others (Kesterson and Braddock, 1975).

The production of citrus fruit (sweet orange) in Venezuela for

1978 was 262.690 metric tons harvested from 27.806 Ha (Fomento

Agropecuario, 1980).

The most important groups of citrus pests worldwide are fruit

flies, scale insects, mites and whiteflies (including citrus blackfly).















CHAPTER II
A REVIEW OF LITERATURE

Taxonomic Position, Synonymy and Common Names


Aleurocanthus wogumi Ashby is a member of the homopterous family

Aleyrodidae. Because of the appearance of the adult stage, it is com-

monly referred to as the citrus blackfly. It was first described by

S. F. Ashyby (Ashby, 1915). There has been no recent taxonofric treat-

ment of the family, and the most definitive work remains that of

Quaintance and Baker (1913-14). They noted that "unfortunately" the

pupal stage -as the life form most readily used in identificationr and

classification of species. Pupae continue to be the most readily iden-

tified. The genus Aleurocanthus is widely distributed throughout the

tropical to lower temperate regions and includes the species listed

below which are currently treated as valid members of the genus and are

potentially serious pests of citrus (Quaintance and Baker, 1916).

A. citricolus (Newstead)

A. citriperdus Quaintance and Baker

A. woglumi Ashby

A. spiniferus (Quaintance)

Other members of this family commonly encountered often as

serious pests on citrus are (Quaintance and Baker, 1916):

Alourolobus marlatti (Quai.ntance)

Aleurothrixus floccosus (Miaskell)


3








Aleurothrixus howardi (Quaintance)

Aleurothrixus por teri Quaintance and Baker

Bemisia giffardi (Kotinsky)

Dialeurodes citri (Ashmead)

Dialeurodes citrifolii (Morgan)

Paraleyrodes perseae (Quaintance)

Trialeurodes floridensis (Quaintance)

Trialeurodes vitrinellus (Cockerell)

Tetraleurodes mori (Quaintance)

Tetraleurodes mori var. arizonensis (Cockerell)

Synonymous and common names for A. woglumi Ashby are the following:

Synonymous:

Aleurocanthus woglumi (Quaintance) (Ashby, 1915)

A. punjabensis Corbett (1935a)

A. woglumi var. formosana Takahashi (1935)

Common names:

Mosca prieta, citrus blackfly, blackfly, black

scale (in Jamaica), blue fly, citrus bluefly

(in Bahamas). The most used common names are

Mosca prieta and citrus blackfly.


Origin and Distribution

The citrus blackfly has been treated as a native of India (Ashby,

1915; Dietz and Zetek, 1920; Wolcott, 1933; Weems, 1962), India and

Pakistan (Osorio et al., 1972), South Asia (Jimenez, 1963; Smith et al.,

1964; Enkerlin, 1976), Southern China (Clausen and Berry, 1932), Asia








(Russell, 1962; Howard and Neel, 1977; Dowell and Fitzpatrick, 1978;

Dowell et al., 1979; Dowell, 1979a).

The citrus blackfly was first received by the U. S. Dept. of

Agriculture, Bureau of Entomology, in 1910 from Maxwell-Lefroy in

India and subsequently from George Compere in the Philippine Islands

and R. S. Woglum in India and Ceylon. The citrus blackfly is now

widely distributed in most of the citrus growing areas:

Africa

Kenya (Wheatley, 1964; Hill, 1975)

South Africa: Durban (Bosman, 1959; Russell, 1962; Bedford

and Thomas, 1965).

Seychelle Islands (Russell, 1962; Browne, 1968)

Asia

Aden (Knorr et al., 1961; Russell, 1962; Gentry, 1965)

Bangladesh (Alam et al., 1965)

Burma (Clausen and Berry, 1932)

Ceylon (Srilanka) (Quaintance and Baker, 1916; Russell, 1962)

China

Canton: Wangtung (Wu, 1935)

Southern China (Clausen and Berry, 1932; Weems, 1962)

India

Surat, Ahmadabad: Gujarat (Smith et al., 1964)

Andra Pradesh (State), Assam (State), Bihar (State), Delhi,

Mad'hya Pradesh (State) (Anonymous, 1959).

Calcutta: Benial (Smith et al., 1964)

Sikkim (Quaintance and Baker, 1916; Dietz and Zetek, 1920)








Nagpur: Maharashtra (Quaintance and Baker, 1916; Dietz

and Zetek, 1920)
Bombay: Maharashtra (Husain and Kahn, 1945)

Poona: Maharaslhtra (Smith et al., 1964)

Mysore: Mysore (Smith et al., 1964)

Cuttack: Orissa (Smith et al., 1964)

Madras: Tamil Nadu (Smith et al., 1964)

Kalimpong: West Bengal (Quaintance and Baker, 1916)

Dehra Dun, Saharampur: Uttar Pradesh (Smith et al., 1964)

Indochina (Clausen and Berry, 1932; Weems, 1962)

Indonesia (Dutch East Indies, Weems, 1962)

Java, Sumatra (Clausen and Berry, 1932; Russell,1962)

Iran (Kiriukhin, 1947; Gentry, 1965)

Korea (Muller, 1956)

Malaya: Kuala Lanpur, Malacca, Serdang, Selangor (Clausen and

Berry, 1932; Corbett, 1935b; Clausen, 1936; Russell,

1962; Weems, 1962)

Philippines: Manila (Quaintance and Baker, 1916; Pratt, 1958;

Russell, 1962; Weems, 1962)

Pakistan: Sind (Abbas et al., 1955; Russell, 1962)

Oman (Watts and Alam, 1973; Simmonds, 1975)

Singapore (Silvestri, 1926; Russell, 1962)

Thailand (Siam): Bangkok (Clausen and Berry, 1932; Takahashi,

1942; Weems, 1962)

Turkey (Anonymrous, 1968)

Central Arerica and West Indies (Fig. 1)

Bahahas (Quaintance and Baker, 1916; Newell, 1918; Wolcott, 1933;

Richardson, 1948; Russell, 1962; Weems, 1962)































Figure ZI. ap shoin the~ coutresan dte her th cirs icfl a




benreported in the Western Hemisphere.








Bermuda (Russell, 1962)
Barbados (Bennett and van Whervin, 1965; Pschorn-Walcher and

Bennett, 1967)

Costa Rica (Zetek, 1919; Wolcott, 1933; Russell, 1962; Osorio

et al., 1972)

Cuba (Quaintance and Baker, 1916; Anonimo, 1917; Hutson, 1917;

Bruner, 1931; Berry and McGough, 1932; Wolcott, 1933;

Bruner et al., 1945; Osorio, 1946; Bruner, 1954;

Osorio et al., 1972)

Canal Zone (Dietz and Zetek, 1920; Wolcott, 1933)

Dominica (Russell, 1962)

El Salvador (McGuire and Crandall, 1967; Quezada, 1974)

Guatemala (McGuire and Crandall, 1967)

Haiti (Dozier, 1932, 1933; Wolcott, 1933; Russell, 1962, Weems,

1962)

Honduras (McGuire and Crandall, 1967)

Jamaica (Ashby, 1915; Quaintance and Baker, 1916; Wolcott, 1933)

Nicaragua (Russell, 1962; McGuire and Crandall, 1967)

Republic of Panama (Dietz and Zetek, 1920; Wolcott, 1933;

Russell, 1962; Osorio et al., 1972)

Taboga Island (Dietz and Zetek, 1920)

San Andres Island (Republic of Colombia) (Zetek, 1919)

North America (Fig. 1)

Mexico

El Dorado: Sinaloa (Baker and Dampf, 1937)

Aguas Calientes, Baja California, Colima, Campeche,

Chihuahua, Durango, Guanajato, Guerrero, Hidalgo, Jalisco,








Morelos, Michoacan, Nayarit, Nuevo Leon, Oaxuco, Puebla,

Sonora, San Luis Potosi, Tamaulipas, Zacatecas (Jimenez,

1963; Mateos, 1963; Smith et al., 1964; Carrillo et

al., 1966; Jimenez, 1968).

Coahuila, Mexico D.F., Queretaro,Simalca, Uruapan,

Vera Cruz (Russell, 1962)

U.S.A.

Florida

Key West (Brown, 1937; Brown, 1939; Newell and Brown,

1939) (Eradicated)

Broward County (Anonymous, 1976a; Cherry et al., 1978)

Palm Beach County (Anonymous, 1976b; Cherry et al., 1978)

Dade County (Cherry et al., 1978)

Texas (Smith et al., 1964; Enkerlin, 1976; Ketner and Rosier,

1978)
Texas (Again after eradication; Hart et al., 1973; Ketner

and Rosier, 1978)

South America (Fig. 1)

Colombia (Russell, 1962; Weems, 1962; Angeles et al., 1967;

Angeles et al., 1968; Bustillo, 1970; Posada and

Garcia, 1976)
Ecuador (Yust and Cevallos, 1954-55; Russell, 1962; Jimenez,

1963; Bennet and van Whervin, 1965; Osorio et al.,

1972; Clausen, 1978)


Venezuela
Valera: Trujillo State, San Antonio: Tachira State

(Angeles et al., 1967; Angeles et al., 1968)








Lara, Aragua, Monay: Trujillo (Osorio, 1970)

Tachira, Merida, Zulia, Carabobo, Miranda and Dto. Federal

(Angeles et al., 1971)

Yaracuy, Portuguesa, Falcon, Barinas (Osorio et al., 1972)

Anzoategui, Guarico, Cojedes (Angeles et al., 1974)

Atlantic Ocean Island

Azores (Russell, 1962)


Biology

Species of the genus Aleurocanthus, in common with all Aleyrodidae,

are characterized by a mode of development that appears to be gradual

in some respects but may be considered as of an intermediate type

(Quaintance and Baker, 1913), as nymphs undergo a form of metamorphosis

corresponding closely to that known as holometabolous. In consequence,

the life stages are generally referred to as egg, nymph, pupa and adult

(J. H. Corstock, 1967). The first description of the life history of

citrus blackfly was published by S. F. Ashby in a report in the Bulletin

of the Department of Agriculture, Jamaica, August 1915. Quaintance

and Baker, June 1916, published the first technical description of

Aleurocanthus woqlumi, although they did not describe the first, second

or third nymphal instars of the insect. Other authors have further

described and/or photographed all stages.(Dietz and Zetek, 1920; Berry

and McGouch, 1932; Ebeling, 1950; Islas, 1951; Jimenez, 1963; Smith

et al., 1964; Osorio, 1970; Osorio et al., 1972; and Martinez and

Angeles, 1973). Many of these as well as later articles repeat

noterial in earlier references and add little new information. The

following descriptions relating to A. woglumi Ashby are basically those








published by Dietz and Zetek (1920) and prepared by Dr. A. C. Baker

and Miss Margaret L. Moles of the Bureau of Entomology and Islas (1951).

Egg stage: Very minute about 0.203 am. by 0.08 rm., elliptical

in shape, curved, attached to the leaf of the host plant by a short

stalk or pedicel situated near its posterior end. The eggs are nor-

mally laid in a spiral. When first laid the egg is yellowish white

with reticulations on the corion, but it soon turns light brown to

blackish as the embryo develops.

First nymphal instar: Elongate-ovate in shape, about 0.150 mm.

by 0.304 m., dusky in color, with reddish eye spot, short antennae,

and rather short legs. On each side of a pronounced median ridge, two

long dorsal spines and numerous shorter spines.

Second nynphal instar: More ovate and convex than the first stage

and measuring apprluxinately 0.200 mm. by 0.400 mm., with eye spots and

vasiform orifice quite prominent. Color dull black with patches of

dull green. At least 10 long spines distributed symmetrically on each

side of the mesa line.

Third nymphal instar: Ovate, more convex and much larger than the

second stage, averaging 0.740 mm. by 0.870 rm; body shiny black with a

more or less hemispherical dull green spot on anterior part of the

dorsum, covering greater part of thorax and anterior part of the

abdomen, spines are stouter with at least 13 spines symmetrically dis-

tributed on each side of dorsal line. In this instar sexes can be

distinguished, the males being smaller than the female.

Fourth instar or p a: Regularly elliptical to ovate in shape,

averaging 0.89 mm. by 1.50 mi. Sexes readily distinguished, the female

pupae being conspicuously larger than males, the former averaging








1.25 mm. and the latter 1.00 mm. in length. The pupa is convex with

the dorsum considerably arched or rounded; the median ridge high, but

not markedly distinct from the dorsal area, except near the caudal

portion of the abdomen and at the vasiform orifice, which is elevated

into a more or less prominent tubercle. Color shiny black with at

least 15 spines on either side of the dorsal mesal line. These vary

considerably in length, but the caudal pair is nearly always the long-

est. Margin of the pupal case dentate, teeth large and bluntly rounded.

Spaces bet,;,een teeth not acute, but often quadrate. A space of 0.1 mm.

is occupied by 6 or 7 teeth. On this feature alone the pupal case is

easily separdble from those of the other species. The pupa has a

marginal band of white waxy secretion, males usually secreting notice-

ably more than females. The cottony lateral wax fringe sometimes

extends mesad, irregularly covering the submarginal area, but the

secretion is usually absent dorsally.

Adult staie: When the adult emerges, the head, thorax, and

abdomen is a bright brick-red in color, with front of head (vertex)

pale yellow, anrtennae and legs whitish, and eyes a deep red or reddish

brown. Later the head, thorax, wings (with the exception of the color-

less or whitish areas), and legs dusky pale, suture of thorax smoky;

the entire abdomen remains a brick-red color and the antennae more

or less whitish, tinged with pale yellow. 'Eyes become a deep reddish

brown. The insects become covered with heavy pulverulence so that they

have a general slaty blue appearance. When the insects are at rest,

the colorless spot on the wings form what appears to be a white band

across the middle of the abdomen.- Adult females average 1.66 m. and

males 1.33 nun. in length. Adult males resemble the females but








are smaller and the more slender abdomens bear a pair of terminal

claspers.
A more complete technical description can be found in Dietz

and Zetek, 1920, pages 39-42.

All nymphal instars except the first are scale-like, and appressed

to the leaves. The first instar is a crawler that inserts its mouth-

parts into the leaf along the minor veination and usually becomes

stationary within ca. 15 minutes after emergence. However, on more

mature leaves a nymph may continue its search for a favorable feeding

station for as long as 24 hours after hatching (Sanchez et al., 1977)

(45 to 60 minutes, Islas, 1951). Dowell et al. (1978) found that a

small portion (0.2-0.3%) of first instar A. woglumi is mobile for 2-4

hours and will crawl up to 25-30 am. Earlier-Dietz and Zetek (1920)

observed crawlers to move a maximum distance of 38 mm. from the egg

spiral (5 to 10 mm., Islas, 1951). Islas (1951) states that the time

required for a crawler to settle depends upon the maturity of the

leaf. He also observed a 2 day old crawler moving from one site to

another on the same leaf. On new leaves the mobility time is reduced.


Life History

In the laboratory egg laying begins approximately 18 hours after

emergence of adults and may continue for as long as 4 (or more) days

in adults of unknown history brought in on young citrus shoots (Dietz

and Zetck, 1920); however, Sanchez et al. (1977) found egg deposition

to cease after 3 days when females were confined in a cage. It has been

observed that females will lay eggs-near the pupal cases from which they

have emerged. Copulation takes place on the young growth where both








sexes congregate to obtain food and to insure fertilization of the

females. Mating has been observed between individuals whose color

would indicate that they were not more than 12 hours old (Dietz and

Zetek, 1920). The females oviposit usually in a spiral pattern on the

underside of leaves on the same day mating takes place. Males are

polygamous, but no multiple mating of the females has been observed

(Sanchez et al., 1977). However, Dietz and Zetek (1920) observed a

male that mated with the same female 3 times in 20 minutes. Islas

(1951) observed that the elapsed time between 2 matings of a couple was

60 seconds. In laying eggs the female usually starts at what becomes

the center of the spiral. Each female oviposits from 35 to 50 eggs per

spiral (50 eggs per spiral, Ashby, 1915) and more than one spiral is

laid per female; thus a single female may lay considerably more than

100 eggs in her lifetime (Dietz and Zetek, 1920; Jimenez, 1963 and

Smith et al., 1964). According to Sanchez et al. (1977) the usual num-

ber of eggs per spiral ranged from ca. 20-40 and each female blackfly

was observed to deposit an average of 61 eggs during the first 3 days

of life. Females lived as long as 13 days. It may be assumed that the

life of the adults is at least a week and that it may be as long as

.12 days (Dietz and Zetek, 1920) (1 to 14 days, Berry and McGough, 1932).

Jimenez (1963) and Smith et al. (1964) stated that mating takes place

soon after emergence, and oviposition occurs several days later.

Hatching occurs in from 9 to 40 days according to the weather (9

to 25 days, Jimenez, 1963; and Smith et al., 1964) (HI to 20 days,

Dietz and Zetek, 1920) (12 to 40 days, Berry and McGough, 1932) (14

days, Ashby, 1915; and Sanchez et al., 1977) (15 to 29 days, Osorio

et al., 1972).








The first molt occurs in from 6 to 43 day'; (Brry ann WGough,

1932) (7 to'f6 days, Dietz and Zetek, 1920) (Q to R7 days, Jimenez,

1963; and Smith et al., 1961) (9.5 days, Satchni et al., 1977 and 10

days, Ashby, 1915) (7 to 11 days, Islas, 1951). The second molt occurs

in from 4 to 30 days (U[rry and McGough, 1932) (3 to 13 days, Dietz

and Zetek, 1920) (7 to 16 days, Jimenez, 1963; and Smith et al., 1964)

(7 days, Sanchez et al., 1977; and 8 days, Ashby, 1915) (5 to 11 days,

Islas, 1951). The third molt occurs in from 7 to 31 days (Berry and

McGough, 1932) (8 to 14 days, Dietz and Zetek, 1920; Islas, 1951) (7

to 22 days, Jimenez, 1963; and Smith et al., 1964) (9.5 days, Sanchez

et al., 1977; and 11 days, Ashby, 1915) before becoming a pupa. Pupal

molt occurs in from 16 to 89 days (16 to 48 days, Dietz and Zetek, 1920)

(18 to 89 days, Berry and McGough, 1932) (21 to 45 days, Jimenez, 1963;

and Smith et al., 1964) (22 days, Sanchez et al., 1977; and Ashby, 1915)

(22 to 35 days, Islas, 1951). The period between molts seems to be

determined by temperature and according to Berry and McGough (1932),

developmental periods of each stage doubles with a temperature reduc-

tion of 4.440C (80F) to 6.66C (12'F). The life cycle from egg to

adult may, therefore, rangc from 42 to 233 days (1.4 to 7.77 months),

a great variation being noted even among eggs laid on the same leaf on

the same day but in different egg spirals (45 to 113 days, Dietz and

Zetek, 1920) (54 to.144 days, Berry and McGough, 1932) (60 to 120 days,

Jimenez, 1963; and Smith et al., 1964) (62 days, Sanchez et al., 1977;

and 63 days, Ashby, 1915) (45 to 127 days, Islas, 1915). Dowell and
Fitzpatrick (1978) working with thermal units found that the life cycle

varies from 66.8 days at 28.40C to 156 days at 20"C.








On the basis of the maximum and minimum times for the completion

of the life cycle from egg to adult there is the possibility of from

three to six generations per year with all degrees of generation

overlapping even from the same colony of individuals.

Morrill (1903) was the first to note parthenogenesis in this

family, and Morrill and Back (1911) further established the phenomenon

in D. citri. Parthenogenesis occurs in A. woglumi (Dietz and Zetek,

1920) when unfertilized eggs hatch and the nymphs develop into adult

males, a condition known as arrhenotoky.


Host Plants

The citrus blackfly is a highly polyphagous insect and will ovi-

posit on at least 160 plant species in 60 families (Dietz and Zetek,

1920; Shaw, 1950a; Anonimo, 1952; Angeles et al., 1972; Hill, 1975;

Howard and Neel, 1977; Steinberg et al., 1978; Howard, 1979; Dowell and

Steinberg, 1979; Dowell et al., 1979). There is, howevever, little

relation between the number of plant species on which eggs have been

found and the number on which immature stages can develop. Plant at-

tractiveness appears innate and is unrelated to the frequency with

which the plant occurs in the environment. Dowell et al. (1979) found

that mango (Mangifera indica L.: Anacardiaceae), pink trumpet

(Ta.bbujia pallida (Lindley) Miers: Bignoniaceae) and kumquat

(For tunella sp: Rutaceae) are as attractive as Citrus (Rutaceae) to

ovipositing A. woglunmi at low densities. They found that citrus black-

fly adults appear to be attracted to plant material reflecting light in

the 500-600 rim. range. This indicates that blackfly females do not

oviposit on plants at random but appear to actively seek "preferred"








host plants. On the other hand, the number of host species utilized for

oviposition and development is a function of the size of the citrus

blackfly population (Jimenez, 1963; Smith et al., 1964; Howard and

Neel, 1977; Dowell et al., 1979). Dowell (1979a) states that dis-

persal from the leaf upon which the insect develops occurs if the leaf

is unacceptable for feeding or after oviposition and that host dis-

crimination occurs only after the females makes physical contact with
the plant. In its area of origin the citrus blackfly has been reported

only from Citrus spp.; however, in the Western Hemisphere the number

of "preferred" host plants on which A. woglumi is reported to oviposit

and develop is remarkably large. Dowell and Steinberg (1979) tested

23 plant species for development and survival of immature citrus

blackfly and found that survival was not closely related to either plant

family or plant species and that number of degree-days required for

completion of the insect's life cycle did not vary significantly among

the plants. Survivorship of A. woglumi on lemon is significantly

higher than that on orange, lime, tangerine and tangelo which are not

significantly different from each other, while survivorship on grape-

fruit is significantly lower (Dowell et al., 1978). Three factors inter-

act to determine the importance of any host plant. Females must fre-

quently Oviposit upon the plant, substantial numbers of nymphs must

complete development, and the plant must be commonly found in the en-

virohment (Dowell and Steinberg, 1979). Clausen found during two

years of observation in seven asiatic countries that citrus was vir-

tually the sole host of citrus blackfly (Clausen and Berry, 1932).

However, noncitrus host plants are important as aids to dispersal of

A. wogILumi .









Dalmqe or Injjry

Damage caused by the citrus blackfly results from feeding, par-

ticularly on new growth of the host plants and from excretion of honey-

dew on which sooty-mold fungus develops (Ashby, 1915; Dietz and Zetek,

1920; Berry and McGough, 1932; Russell, 1962; Jimenez, 1963; Smith et

al., 1964; Angeles et al., 1971; Osorio et al., 1972; Hart et al.,

1976; and Cherry et al., 1978). Badly infested leaves wither and drop

off as a result of injury caused by extraction of the cell sap. Such

defoliation weakens the tree, interferes with its normal development

and fruiting, and makes it unsightly (Clausen and Berry, 1932; Berry

and McGough, 1932; Russell, 1962; Jimenez, 1963; Osorio et al., 1972;

Enkerlin, 1976). Hart et al. (1976) state that damage to citrus

foliage caused by A. woglumi is of two types: feeding injury which

results in dauiage to cells of the lower epidermis, due to thickening

of the cell wall, loss of cellular contents and the appearance of

chlorotic areas on leaves, and the physiological damage caused by a

sooty-mold fungus (Capnodium citri Berk. and Desm.) that develops on

the honey-dew excreted by the developing insect. Sooty-mold deposits

reduce the photosynthesis and respiration of the affected plant. In

Mexico there i, admits a complete crop failure when heavy infestation

of the citrus blackfly lasts longer than one year (Jimenez, 1963;

Smith et al., 1964; and Enkerlin, 1976).


Biological Control in the Western Hemisphere

Introduction of natural enemies from Asia for control of the citrus

blackfly in Western Hemisphere countries can be divided into 2 stages.









The first, in 1930, began with the shipment of Eretmocerus serius Silv.

from Malaya. In 3 consignments of natural enemies forwarded from

Malaya during 1930 and 1931 ProsaItela divergens Silv., P. smithi

Silv., Cybocephalus sp., Catana clauseni Chapin (Cr ptognatha sp.),

ScXmnus smithianus Silv., Scymnuss. near pallidicollis Mulsant,

and Acletoxenus indica Malloch were present in varying numbers (Clausen

and Berry, 1932; Bruner, 1954).

Of the natural enemies listed above, E. serius, C. clauseni and

S. smithianus were established in Cuba. Scymnus smithianus was ap-

parently not well adapted to Cuban conditions. Catana clauseni demon-

strated ability to suppress heavy citrus blackfly infestations but

became inactive in low or moderate infestations and failed to prevent

resurgence to high levels. This predator was also released in the

Bahama Islands to supplement the activity of E. serius. Of the species

successfully established in Cuba during the first period only E. serius

proved useful. Commercial control of the citrus blackfly was quickly

obtained throughout Cuba. This parasite was later introduced into

other countries of the Western Hemisphere (Clausen and Berry, 1932;

Bruner, 1954).
The second stage of natural enemies importation began in November

1949 with shipment of parasitized material from India and Pakistan to

Mexico. Shipments were terminated in April 1950. Amitus hesperidum

Silv., Lncarsia nerceti Silv., Eretmocerus serius, Prospaltella

cl_y~pe1is, P. divecjlens, P. oPulenta, P. smithi, Prospaltela sp. (near

citrofila Silv.),Catana parcesetosa (Sicard), and Acletoxenus indica

were included in the shipments received during this period (Jimenez,

1963; Smith et al., 1964).








Amitus hesperidum, P. oLulenta and P. clypealis proved to be the

most effective species in the control of the pest in Mexico (Jimenez,

1963; Smith et al., 1964).

A more comprehensive discussion of the natural enemies and of

their introduction into the countries of the Western Hemisphere known

to be infested with citrus blackfly follows.

Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae)

Amitus hesperidum is biparental in reproduction with a sex ratio

1:1. There is 1 generation for each generation of the host.

The female is proovigenic, and as an adult lives from 3 to 6

days under favorable conditions. According to Dowell (1979b), A.

hesperidum lived an average of 2 days without food or water, 2.3 days

with water only and 4.1 days with 1:1 mixture of honey:water.

Mating occurs readily, the male having emerged from the host a

few days ahead of the female. Oviposition by A. hesperidum occurs in

the 3 nymphal instars of citrus blackfly, with an apparent preference

for the first. Thirty eggs, presumably nonpolyembryonic, may be

deposited in rapid succession. One to 3 eggs are deposited in a

single host, each egg being placed in the host's midgut. Female host

pupae commonly produce 2 and occasionally 3 parasites, whereas male

host pupae produce only 1. Host pupae usually enlarge perceptibly,

and this occurs while A. hesperidum is still in the minute first

larval instar. The parasite larva completes its development only after

the host attains an advanced stage. The emergence holes of the adult

parasites are usually in the side of the vacated host rather than on

its ends (Jiimenz, 1963; Smith et al., 1964; Flanders, 1969).








Eretmocerus serius Silvestri (Hymenuptera: Aphelinidae)

The first shipment of E. serius Sii. from Malaya to Cuba was made

in March 1930 (Bruner, 1931; Clausen and Berry, 1932). This parasite

was responsible for the first example of successful use of parasites

for control of citrus blackfly in the Western Hemisphere (Clausen and

Berry, 1932; Bruner et al., 1945; Osorio, 1946; Shaw, 1950b; Bruner,

1954). This proovigenic species reproduces biparentally. The life

cycle of the male is normally about 2 days shorter than of the female.

The sex ratio is about 1 male to 1.99 females. Mating takes place

on the foliage very shortly after emergence, and oviposition may

ensue the same day. Oviposition continues over a period of 7 to 10

days. It completes development as an endoparasite, but the first 2

larval instars are ectoparasitic. Oviposition may take place in any

instar of the host from the first nymphal stage to pupa but is

believed to prefer the second nymphal instar. Irrespective of the

stage in t.hich the eggs are laid, adults emerge from the host pupae.

The complete cycle requires approximately 4 weeks; consequently,

the parasite is able to develop 2 generations to each host generation.

The female lays the egg on the leaf surface beneath the second nymphal

instar, almost invariably in the area near the line dividing the thorax

and abdomen. First and second larval instars feed externally, and

although a certain amount of feeding takes place, this is considered a

resting period, and the second molt is delayed until after penetration

of the pupa of the host, following which development is rapid. The

penetration is also usually effected in the area where the egg was

placed and the entry hole is surrounded by a light brownish area that

contrasts markedly with the normal black coloration of the integment.









The female does not exercise any discrimination in choice of host, and

as many as 8 first and second larval instars have been found be-

neath a singl- host individual. Only 1 of these, however, can attain

maturity. The body contents of the host are entirely consumed, and

no solid meconium is cast by the larva. The adult parasite cuts a

circular emergence hole through the dorsal integument of the anterior

end of the host body (Clausen and Berry, 1932; Smith, 1945; Osorio

et al., 1972).

Prospaltella clypealis Silvestri (Hymenoptera: Aphelinidae)

This species reproduces biparentally at the rate of 2 generations

to 1 of its host (Flanders, 1969); however, Jimenez (1963) and Smith

et al. (1964) state that it may be parthenogenetic, as mating was

rarely observed.

This species is an endoparasite of citrus blackfly. The sex

ratio of P. clypealis is approximately 1 to 7, with females predomi-

nating. Oviposition takes place in the 3 nymphal arid pupal stages of

the host, with a preference for the second instar. If oviposition

takes place in the first nymphal instar, the egg is carried over into

the second before hatching. The haploid (male) egg is deposited on the

surface of the fully fed larva or pupae of a primary parasite of citrus

blackfly. The hatched larva acts as a secondary ectoparasite feeding

on developing females of its own species or 1 of like habits. Female

eggs are deposited directly into the host body on the underside of

the leaf. Male eggs are deposited by thrusting the ovipositor into

the host body through the upper surface of the leaf (Jimenez, 1963;

Smith et al., 1964; Flanders, 1969).








Flanders (1969) states that P. clypealis is synovigenic in

reproduction with relative long-lived females (2 months at room tem-

perature if fed honey). Fertilized (diploid) eggs may be deposited in

the same host generation from which the female emerged. Mated females

oviposit as secondary, as well as primary, parasites depending on

whether a haploid or diploid egg is to be laid. As with many

synovigenic species the female adults host-feed and have been ob-

served to feed on the body fluids of first nymphal instars.

The body of the blackfly contracts somewhat in size when parasit-

ized by Prospaltella. A host pupa from which P. clypealis has issued

shows a very small emergence hole and contains a rose-colored meconium

(Jimenez, 1963; Smith et al., 1964; Flanders, 1969).

Prospaltella opulent Silvestri (Hymenoptera: Aphelinidae)

This species reproduces biparentally (Flanders, 1969). Jimenez

(1963) and Smith et al. (1964) state that the life history of this

species is similar to that of P. clypealis.

Prospaltella opulenta is an endoparasite of citrus blackfly.

This species reproduces at the rate of 1 generation to 1 of its host.

The sex ratio is about 1 to 7.3, with female predominating. According
to Flanders (1969), the male of P. opulenta is -n endoparasite develop-

ing as a secondary parasite of citrus blackfly through either its own

species or 1 of like habits. Should such hosts of males be scarce

as many as 100,000 adults of P. 2pulenta may be collected in the field

without finding a male.

Oviposition occurs in all larval instars and the pupal stage, but

the second instar is preferred. The haploid (male) egg is deposited

within the host body of fully fed female larvae and pupae of








conspecifics and other primary parasites of citrus blackfly. Emergence

of P. opulenta from a host pupa is indicated by a hole slightly larger

than that made by P. clypealis and by a yellow meconium (Jimenez, 1963;

Smith et al., 1964; Flanders, 1969).

Flanders (1969) states that P. opuleita is synovigenic with

relatively lonQ-lived females (4 to 6 weeks). After the first day of

adult life ovigenesis progresses at a rate that produces 8 to 10

mature eggs a day.

Prospaltella smithi Silvestri (Hymenoptera: Aphelinidae)

This species is bisexual but reproduces uniparentally (Deutero-

tokous), as an endoparasite of the host pupa at the rate of 1 to

2 generations of each host generation. Mating has not been observed

although the reported sex ratio of males to females is I to 4. The

female is synov-genic with an adult life of about I month. She

deposits diploid (female) eggs inside the Malpighian tubules of the

host's pupa and late larval instar. Egg incubation period is about 3

days, but the first larval instar remains dormant until its host

pupates. The haploid (male) egg develops inside the prepupa or pupa of

either its own or some other parasite species, the male being a true

secondary parasite of the citrus blackfly (Jimenez, 1963; Smith et al.,

1964; Flanders, 1969).

Clausen and Berry (1932) state that oviposition by P. smithi takes

place largely in the first larval stage of the host, though females

have frequently been observed to attack the later larval stages.

Silvestri (1927) provides a complete description of the adult stages

of the most important parasites of A. wogIumi.








Countries of the Western Hemisphere Where Natural Enemies
Have Been Introduced for Control of Citrus Blackfly

The introduction and establishment of important natural enemies of

the citrus blackfly from Malaya, India and Pakistan in Cuba and Mexico,

and the further colonization and establishment of these natural enemies

in other infested countries of the Western Hemisphere, is one of the

outstanding successes of biological control (Fig. 1).

Cuba: Several natural enemies were sent to Cuba in 1930. They
were Eretmocerus serius which multiplied to such an extent that it was

possible to make liberations throughout that island and quickly obtain

economic control. At the same time colonies were shipped from Cuba and

the species was established in other countries. Prospaltella divergens

was sent from Malaya, but no progeny developed in Cuba. Prospaltella

smithi: A considerable number of this species were included in the ship-

ments from Malaya to Cuba, but development of the parasite in the Wardian

cages en route was very unsatisfactory. Cybocephalus sp. was a predator

of Aleyrodidae, but no reproduction took place en route. Catana

clauseni (Cryptognatha sp.) was well established at several localities

in Cuba, and according to Bruner (1954) this species was still present

thru May 1933 when he, Berry and Boucle collected 1,000 individuals to

be sent to Bahamas. Scymnus smithianus, a coccinellid, was also es-

tablished in Cuba. Scymnus sp. near Lallidicollis was found attacking

Aleurocanthus, but in no instance did reproduction occur. Acletoxenus

indica a predacious drosophilid was received, but attempts to effect

colonization failed (Clausen and Berry, 1932).

Bruner (1931) stated that of the natural enemies imported,

E. serius appeared most promising. Subsequently this parasite








increased very rapidly at all sites, and commercial control was usually

attained in groves 8 to 12 months after release (Bruner et al., 1945;

Osorio, 1946; Shaw, 1950; Burner, 1954; Clausen, 1978). In 1945,

Bruner and Boucle stated that during more than 14 years following

introduction of E. serius, full control had been consistent throughout

the island. Although little information is available concerning the

present status of control in Cuba, there is reason to believe that at

least some local outbreaks of the citrus blackfly have occurred.

Reasons for such outbreaks are conjectural but possibly a result of

host resistance to E. serius or adverse factors of climate. In any

event, Sailer (i976a) learned that P. opulenta was shipped to Cuba from

Mexico in September 1976.

Panama (including Canal Zone): According to Clausen and Berry

(1932), James Zetek, in charge of the Bureau of Entomology Laboratory

at Balboa, Canal Zone, rendered valuable assistance in the preparation

for the second trip to Malaya, 1930, and was responsible for the

colonization and establishment of Eretmocerus serius in Panama. They

add that colonies of E. serius were also sent from Cuba to the Canal

Zone, the Bahamas and Haiti. Clausen (1978) also states that this

parasite was introduced from Cuba into the Panama Canal Zone, Haiti

and the Bahamas Islands in 1931. Zetek in official correspondence

informed Shaw (1950b) that E. serius effected commercial control of the

citrus blackfly in Panama.

Haiti: Dozier (1932) states that after repeated attempts to rear

out a native parasite of A. woglumi in Haiti, negotiations were under-

taken with the U. S. Bureau of Entonology and the Cuban Department of

Agriculture to obtain a supply of E. serius from Cuba. Two shipments








were received in July and August 1931. The parasites were observed to

start ovipositing immediately in several different stages of the citrus

blackfly, and Dozier expressed the hope and expectation that the in-

troduction would prove as highly successful in Haiti as in Cuba.

Dozier left Haiti in 1932, and there are no later reports of progress

of the parasite.

Sailer (1976b) states that in Haiti he, together with 3 other

Florida entomologists, visited 3 locations where there was an ap-

preciable amount of citrus and made several intermediate stops and

examined dooryard citrus. No citrus blackfly was seen, and he was

assured by Ministry of Agriculture people that the pest did not occur

in Haiti. Earlier, in 1952 Miss Louise Russell, Aleyrodid specialist

for the Systematic Entomology Laboratory, U.S.D.A., visited Haiti and

was unable to find citrus blackfly (personal communication). If in

fact the citrus blackfly has disappeared from Haiti, reasons for the

disappearance should be investigated.

Bahama Islands: Clausen (1978) states that following the success

of E. serius in Cuba, this parasite was introduced into the Bahama

Islands in 1931. Observations by C. P. Clausen in 1937 indicated that

the citrus blackfly was still abundant in places even though a high

population of the parasite was present at the time. A coccinellid,

Catana clauseni, previously introduced from Malaya into Cuba, was

released at Nassau in the hope that it would supplement Eretmocerus in

controlling infestations. It is not known whether or not the beetle

became established (Richardson, 1948). The citrus blackfly is now well

under control at Bahama Islands (Richardson, 1948; Clausen, 1978).








Jamaica: In April 1932 a consignment of E. serius was sent from

Cuba to Jamaica (Edwards, 1932). According to van Whervin (1968),

A. woglumi was under complete control over practically the whole island

by 1934. In 1936, recol.onization of the parasite was undertaken in

some areas where E. serius appeared to have disappeared. During the

1950's recolonizations were again necessary. Because of the reduced

effectiveness of E. serius during the 1950's and early 1960's it was

suggested in 1964 that P. opulenta should be introduced from Mexico in

an effort to achieve a higher level of control. Stock of P. opulenta

was imported in September and October 1964. Successful colonization

followed, and within less than 2 years this species dispersed throughout

the island and almost completely replaced the previously established

E. serius. There has been no recurrence of citrus blackfly infesta-

tion since introduction of P. opulenta (van Whervin, 1968; Bennett,

1971; Clausen, 1978).

Costa Rica: Eretmocerus serius was introduced into Costa Rica

from Cuba in 1.933-34. Commercial control followed introduction of the

parasite (Clausen, 1948).

Mexico: Attempts to introduce the parasite E. serius from Costa

Rica in 1936 and from the Panama Canal Zone in 1938 were unsuccessful.

A further attempt was made in 1943 by United States and Mexican

authorities to move this parasite from the Panama Canal Zone into

Mexico (Smith, 1945). The parasite became established in at least 3

places; however, with the exception of restricted areas of persisting

high humidity, it was unable to bring the citrus blackfly under satis-

factory control on the west coast of Mexico (Shaw, 1950b;Jimenez,

1963; Smith et al., 1964).








Smith sent the first shipment of natural enemies of the A. woglumi

from Malaya to Mexico in 1948. A few adults of P. divergens and

P. Smithi emerged from the air shipment. These were released in the

field but failed to become established. From November 1949 to April

1950, shipments of parasitized material were made to Mexico from India

and Pakistan. Jimenez (1963) and Smith et al. (1964) give a list of the

various species of natural enemies of the citrus blackfly that emerged

from these shipments and were released in infested citrus groves. Three

3f these parasites, Amitus hesperidum, Prospaltella clypealis and

P. opulenta have become dominant in controlling the citrus blackfly in

Mexico. The native predator Delphastus pusillus is useful in reducing

heavy infestations, but it cannot be depended on to effect satisfactory

control in the absence of parasites.

Prospaltella smithi appeared to b.c the most promising of the

imported parasites during the early stages of the program. It proved

to be dominant over Eretmocerus but was in turn superseded by P.

opulenta, P. clypealis and A. hesperidum. While both species have

persisted in Mexico, they are seldom present in detectable numbers

(Smith, 1958; Jimenez, 1963; Smith et al., 1964).

Smith (1958), Jimenez (1963), Smith et al. (1964) and Flanders

(1969) studied the interrelations and the competition between the

natural enemies of the citrus blackfly in Mexico.

The most effective of the imported parasites were P. optulenta,

P. !clyealis and A. hesperidum. The former is adapted to a wider range

of climate than the other two and is much more effective in the hot dry

regions of the country, whereas the second is best adapted to humid

conditions. Amitus hesperidum is especially effective when released








in heavy infestations, but its numbers are reduced when in competition

with either of the 2 ProspjItella (Clausen, 1978).

According to Jimenez (1971), P. o]puleinta and A. hesperidum are

now the most effective parasites for the control of A. woglumi and

P. clypealis, P. smithi and E. serius are of little importance as

factors responsible for control of the citrus blackfly in Mexico.

No commercial damage has been reported in recent years from any area

of Mexico; however, it has been necessary periodically to recolonize

certain areas. This is accomplished by moving parasites from areas

where they are abundant to areas where they have disappeared because of

climatic irregularities, drift of insecticides applied to crops near

citrus groves, or for reasons not well understood (Smith, 1958; Jimenez,

1963; Smith et al., 1964; Anonimo, 1964; Jimenez, 1970; Jimenez, 1971;

Enkerlin, 1976).

Barbados: According to Bennett and van Whervin (1966), adults of

E. serius and leaves bearing parasitized citrus blackflies were col-

lected in Jamaica by Bennett during June 1964. The adults and those

subsequently emerging from the infested leaves were released on heavily

attacked trees in several areas in Barbados. Establishment was attained

and extensive spread was noted. Arrangements were made to obtain ship-

ments of P. opulenta from Miexico in late 1964 and early 1965. This

species also became established, and the citrus blackfly was quickly

reduced to nonpest status (Bennett and van v hervin, 1966; Pschorn-

Walcher and Bennett, 1967; Bennett, 1971).

Ecuador: Aitus hesperidum was imported into Ecuador in 1955 and

is reported to be established. The effectiveness of this parasite has

not been reported (Clausen, 1978).








El Salvador: Small shiprients of P. opulenta from northern Mexico

and Barbados were secured in 1970, but there was no evidence of the

establishment of the released parasite. In July 1971, P. opulenta was

brought from Mexico and the parasite was soon well established. Another

shipment of parasites from Mexico was secured in April 1972.

Aleurocanthus woglumi is under biological control in El Salvador

(Quezada, 1974), except in citrus groves near or surrounded by cotton

fields (Sailer, personal communication).

U.S.A.: The citrus blackfly appeared the first time in Key West

Island, Florida, in 1934. This infestation was successfully eradicated

in 1937 as a result of a spray program (Newell and Brown, 1939). The

second infestation of citrus blackfly, A. woglumi, was found in Texas

in 1955. Chemical applications were made and eradication was achieved

by 1956 (Cavin, 1976; Ketner and Rosier, 1978).

According to George Cavin (1976), in 1966, Hurricane Beulah came

up from the Yucatan Peninsula into Mexico. Within 6 to 7 months after

the hurricane, they began finding the citrus blackfly in citrus groves,

and in 1967 an infestation was well established in the lower Rio Grande

Valley of Texas. Subsequent eradication efforts failed.

By 1971 the infestation included Brownsville, and other areas of

the lower Rio Grande Valley have since beer, invaded (Cavin, 1976;

Ketner and Rosier, 197;).
.In 19, an area of Brownsville was set aside for integrated con-

trol. Prs ltella opulenta from Mexico was released, and the

parasites became established. The success of the biological control

program is evidenced by the absence of documented production losses

in commercial groves due to citrus blackfly infestations during the

1976 and 1977 crop years (Ketner and Rosier, 1978).








In January 1976, Aleurocanthus woqlumi was discovered in Fort

Lauderdale, Florida. Immediate action was taken by Florida State and

Federal Regulatory agencies to contain the infestation through imposi-

tion of quarantine measures. This was quickly followed by a program

designed to eradicate the infestation. Initially, plans for introduc-

tion of parasites were made with the view that they might reduce the

population of citrus blackfly and facilitate eradication. During April

1976 and continuing through the summer, shipments, which included 3

species of parasites, were sent to Fort Lauderdale. These were

provided by the U.S.D.A. Laboratory at General Teran, Mexico, where

the 3 species were in culture. Of the 3 species, A. hesperidum,

P. opulenta and P. clypealis, A. hesperidum was released in largest

numbers and was responsible for reduction of the population to about

3% of the prerelease level. At this point P. opulenta, which was

released at the same time but in much smaller numbers, began to in-

crease and by the end of 1979 was the dominant parasite in the infested

area. The third species, P. clypealis, was released in very small

numbers and has not been recovered (Hart et al., 1978; Dowell, 1979b;

Dowell et al., 1979; Dowell et al., 1980).

Dowell et al. (1979) state that for the period of May 1977-

December 1978, citrus blackfly was under complete biological control

in southern Florida due to the combined action of A. hesperidum and

P. ojulenta.

Venezuela: The first report of Aleurocanthus w oglumi in Venezuela

was made by Angeles et al. (1967) from specimens collected in Cucuta

(Colombia) and San Antonio del Tachira (Venezuela) on leaves of

Citrus sinensis and identified by Louise Russell of the U. S. Department








of Agriculture (Fig. 2). Specimens closely resembling those identified

by Russell were collected in 1965 at Valera, Trujillo State (Venezuela).

Osorio (1970) and Osorio et al. (1972) state that the citrus

blackfly first came to the attention of the Department of Entomology

of the Universidad Centro Occidental in 1968. It seems that A. woglumi

has been established in Barquisimeto (Lara State) since 1966 or 1967,

and that its introduction was possibly through Colombia from Ecuador

or Central America. It might also have been inadvertently introduced

directly from some country of the Western Hemisphere where the citrus

blackfly was already established.

Later, Angeles et al. (1971), Osorio et al. (1972), Angeles et al.

(1972), Martinez and Angeles (1973), Angeles et al. (1974) contributed

substantially to the knowledge of the distribution, biology, host

plant, native enemies (parasites, predators and fungus diseases), and

control. Osorio et al. (1972) suggested importation of natural enemies

as the only solution to suppression of the pest.

In October 1975, a team consisting of entomologists of the U.C.V.

(Facultad de Agronomia), C.E.N.I.A.P. and FUSAGRI who had previously

been trained by the Division de Control Biologico de la Direccion

General de Sanidad Vegetal de Mexico and subventioned by the CONICIT

and the Direccion de Sanidad Vegetal del M.A.C., received the first

shipments of parasites from Mexico. These parasites, Prospaltella

oputlenta, were released in Aragua and Yaracuy States but no establish-

ment was obtained. Approximately 120,000 adult P. opulenta were

included in the shipment, and failure to establish may have been due

to their being held at the customhouse for 2 days during which

average mortality was 50%. After processing through quarantine,






































Figure 2. Places where P. opulenta has been released in Venezuela and where
A. wogluni was first observed.








only 20,000 parasites were available for release in the field. The

releases coincided with the season of heavy rain when the citrus

blackfly populations normally declined due to fungus diseases (Geraud

et al., 1977; Geraud, 1979).

A second series of parasites shipments was received in June 1976.
These parasites (40,000 approx.) were released directly in the field in

Aragua, Carabobo and Yaracuy States. According to Geraud et al. (1977)

and Geraud (1979), positive evidence of establishment between June and

September of the same year was found.














CHAPTER III
BIOLOGICAL CONTROL OF CITRUS BLACKFLY IN THE
CENTRAL-WESTERN REGION OF VENEZUELA


Lara State encompasses 4 markedly different regions, the foothills
of the Andes Mountains on the south and the Coastal Range on the north.

The western part is semiarid and the eastern area is typical of the

Venezuelan Llanos. As a consequence, there are a variety of climatic

conditions that contribute to a diversity of crops and animal breed-

ing that makes Lara State one of the most important agricultural

areas in Venezuela and an important market center for agricultural

and livestock products. Although citrus is not as important as other

crops, it constitutes one of the most important fruit processing in-

dustries. Juconasa is located at Cabudare city (Lara State) where

most of the citrus fruit harvested in the central and central-western

regions are processed as frozen concentrates and chilled pasteurized

juice. In addition, dooryard citrus is very common in residential

areas of the highly urbanized cities as well as in farmsteads in

rural areas. These trees were generally infested throughout the state

and provided additional justification for the introduction of P.

opulenta from Carabobo State (Venezuela), where by 1976 it could be

easily obtained.








Materials and Methods


Host Plants

Citrus trees were selected in accord with the importance of the

commercial variety. Three varieties were sampled: "California" in

Santa Lucia orchard, "Pineapple" in Apoliro orchard and "Valencia" in

Glorida de Lara orchard. Al'i the citrus trees sampled were about 12

years old.


Locations

Citrus blackfly populations were sampled every 2 weeks at 3 loca-

tions, the first being located in the Hacienda Santa Lucia (Yaritagua:

Yaracuy State). This citrus grove occupied an area of 7,884 m2 and

contained 259 trees. It is located in a sugarcane farm, and it is not

managed in a manner similar to commercial groves. These trees re-

ceived no pesticide treatments but may have received some drift from

treatments applied to the nearby sugarcane; however, such treatments

are seldom applied on this particular farm.

The other 2 locations were the Apoliro Experimental Orchard

(Juconasa Industries) in which the study area was 119,280 m2 with

2,635 citrus trees located close to Cabudare city (Lara State), and

the Glorida de Lara in which the study area was 78,800 m2 with 2,045

citrus trees, located close to Sarare city (Lara State) (Fig. 2).

Both are managed as commercial groves, and much of the land surrounding

the study groves is also planted to citrus.

In all 3 of the study groves no pesticides were applied during

the period of study.








Sampling Procedure

Five citrus trees were sampled in each location. Each tree was

divided in 4 quadrants: north, south, east and west; in each quadrant

a new, middle, and old leaf was taken and placed separately in a previ-

ously labeled small plastic bag. Samples from different trees were held

separately, and the same trees were sampled throughout the period of

observation.

One sample was taken each 2 weeks from each tree from November 1976

through November 1977 (see solid line in the figures 4-27). Additional

samples were taken during January, February, April and June 1978 and

February 1979 from the "Apoliro" and "Santa Lucia" citrus groves and

during January, February and June 1978 and March 1979 from the "Gloria

de Lara" citrus grove (see dashed line in the-figures 4-27).

A "new leaf" was the third leaf of the new flush, or, in the
absence of new flush, the "new leaf" was the second leaf of the last

"flush" season. The middle leaf was either the third or fifth leaf

of the last "flush." Old leaves were taken from leaves of the past
year's growth. Branches from which leaves were taken were selected at

random within each quadrant and height range of between 1.50 m. to

2.0 m. as previously used by Chavez (1974).


Count

Each leaf was placed under stereoscopic microscope Olympus (lOx)

for the purpose of counting numbers of eggs, nymphs (first, second and

third instar), pupae and exuviae. A lOx power magnification was used

as this is the normal magnification .of a good hand magnifier used for
assessing the pest in the field.
Adults were counted in the field at the time leaf samples were taken.








All samples were counted on tle asis of 2 square centimeters

in the center of the leaf. Rill leaf counts were also made of the

same leaves as a check on reliability of the 2 square centimeter counts.


Mortal ity Factors

Insofar as possible, causes of mortality were identified in the

field as well as in the leaf samples collected for count of immature

stages. Insects were identified by comparison with identified ref-

erence specimens in the Entomological Museum of the Universidad Centro

Occidental Lisandro Alvarado, Escuela de Agronomia, as well as with

specimens in possession of ing Agr. Nancy de Martinez (CENIAP--Maracay).

Identifications were confirmed by specialists of the U.S.A. and Israel

(Martinez, 1978).


Statistical Analysis

Data from the 2 square centimeter counts were subjected to simple

correlation analysis as well as a regression analysis including the

linear and quadratic effect as required for establishing a prediction

equation based on the value of r for each citrus orchard separately.


Parasite'

Specimens of Prospaltella opulenta were collected in the "La

Segoviana" citrus orchard (Guigue: Carabobo State) (Fig. 2) on

April 22, 1977, with a double chamber aspirator. Approximately 100

parasites were placed in vial, each of which contained a piece of

filter paper saturated with a 1:1 mixture of honey and water. The

parasites were collected in the morning and hand carried to expedite








delivery and insure maximum survival. Parasites were received in the

afternoon, immediately carried to the field and released directly on

the underside of leaf surfaces in heavily infested trees by uncapping

and inverting the vials.

Two hundred parasites were released at "Santa Lucia" and 800 at

"Apoliro." One hundred parasites were released on each tree, and no

release trees were used for subsequent leaf samples. This was to

insure no interference with the establishment and colonization of the

small number of P. opulenta released.

First and second nymphal instars of citrus blackfly, the preferred

instar for parasitism by P. opulenta, were abundant at the release

sites at the time of release. The average mortality of adult parasites

shipped ranged between 1 and 3%.

Evaluation of the parasites were made by counting the pupae with

parasite holes and by dissection of puoae and third instars to deter-

mine whether parasite larvae or pupae were present.


Results

Hacienda Santa Lucia


This citrus grove contained 259 trees in an area of 7,884 m2
(Fig. 3) and received no pesticide treatments, but some drift of

pesticide could have reached the trees from the surrounding areas

where the pesticides were applied to control sugarcane pests.

Figures 4 and 5 show the population trends of citrus blackflies at

Santa Lucia citrus grove. Figure 4 shows clearly the 5 generations

of A. woglumi through a year of study from November 1976 to November



























A Ife
U .Sh.sLl -i.,ti
C110. "'Af z is


17
,.

Ni











---A- 1 -T -






F _..+-.- hi1 r T- -L~k_4 ,
.. ,.fJ__ I i '- -r ----- -


-' l ,--; : :-;i : - t + -L- L


~~... ..... ....... .


I,


. J


TO YARJTACUA.............. .

.cTrcc -occ__T.A n EWAY --------


- .. .. IC t I,*I*
IC Ba.QUI.I-,'aET tI F" ST, ",JCA
Y A -,O ?.tl+,It9A
1 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ 1l I-- -A 1 m+('+


Figure 3. Hacienda Santa Lucia, Yaritagua.


I,







I.

I.


F.'















F.


!
-|









7000-
6000-
5000- EGGS
4000 -- ADULTS

3000O

2000- ,I




S800 .
> 700

o0 5030-
S400-
< pA
300
I oII




0
z 200-


oo
-
IL .

o0-



io I
Z o-00



40 I
@-I
30- I


20-



0-




Figure 4. Egg and adult populations of A. ywoqiumi obser ved
on leaves of C. sinensis var. "California" at Eaci-enda anta Lucia,
Yaritagua. (F-or expla nation of dashed line, see page 38.)






43






2000 -" o NI
;I 'Nil
6LN il
(ftlea'.1y)


900-'"
800 -


600-- .


5i400 .
--I'
o / I
( 00 -




o4200-
0 -
ILL

80 -
70-

60--P


40-- .

.30-


20-
-~ I I










to-j
!~ I





40- r I-TTl---

NovD J F M A M J J A S 0 N D J F M A M J
197G :977 1978
released -TIME




Figure 5. First, second, and third nymphal instars of
A. wolumi observed on leaves of C. sinensis var. "California"
at Hacienda Santa Lucia, Yaritagua. TFor explanation of dashed
line, see page 38.)







1977. Those generations were the first in December, the second at
the end of February and early March, the third in June, the fourth

at the end of July and early August, and the fifth in October. Figure 5

shows the peaks of each of the nymphal instars and the shift from 1

nymphal instar to the next.
Figures 6, 7, and 8 show the population trends of each nymphal

instar and the number of total, healthy and dead individuals for each

sample date. As is evident from the data preceding release of P.

optulenta on April 22, 1977, the mortality factors (biotic and abiotic)

did not prevent resurgence of citrus blackfly population despite a

decline that occurred in December 1976 when samples showed 100% mor-

tality of first instars, 95% of seconds and 70% of the third stage

(Table 1). Dead individuals of all developmental stages had the ap-

pearance of individuals killed by fumigation or by some sprays.

However, individuals that are victims of sucking predators and

parasite host feeding as well as those "stung" by female parasites

but not successfully parasitized have this same appearance. This has

been referred to as unexplained mortality (Morrill and Back, 1912;

Chavez, 1974; Sailer, personal communication; Dowell, personal

communication). During this time, precipitation was low (Fig. 9 and

Table 2); however, relative humidity was comparatively high (76%)

and the leaves were regularly covered by morning dew which favored the

development of fungus diseases (Aegerita webberi Faw. and'Aschersonia

aleyrodis Webber). Several adults were observed to be trapped in dew

drops. Other natural enemies found in higher numbers during December

were Mantispilla sp. near viridis Walk (Neuroptera: Mantispidae) and

Nodita sp. (Neuroptera: Chrysopidae) and the most important were















N I
I TOTAL
6 HEALTHY

1000- DHEALT
900->0DA
000
700-
600-
500-I



4o300 I
40
o. Ii ,I

200- -

o H


o i

60-
z 50- $



40- l









Nco. Z J F VA I JA SO 0 jF .,I A MJ J
1976 1977 1978
I? O~i~l4O TIME


Figure 6. Total, healthy, and dead first nymphal instar
populations of A. woglumi observed' on leaves of C. sinensis var.
"California" at Hacienda Santa Lucia, Yaritagua. (For an
explanation of dashed line, see page 38.)






46







2000 -





1000-
900- Nil
800-
700- 9 TOTAL
600 HEALTHY
0 DEAD
500-

V)400 _
w
S300/ I

j \


0




100- .l

70 0 01
w 70 70-
o-

z 50- 1

40-

30-


20 1

I
..10, I



0 T -t'f T-'y~rr rrnrr~i
Nov D J F M A M J J A S 0 N D J F M A M J
1976 1977 1978
F' OQ'f'rto TI ME




Figure 7. Total, healthy, and dead second nymphal instar
populations of A. woglumi observed-on leaves of C. sinensis var.
"California" at Hacienda Santa Lucia, Yaritagua. (For an
explanation of dashed line, see page 38.)
















1000-
900-- NIII
800-
700- TOTAL
600- HEALTHY
500- DEAD
>w 400-

-1 300' t'
0
. o ii



I ;; I I
IV 200--




z 00

o 80- I I
cr 70 I
C3 60 -

:3 50- *I
40 I

i i
3o I



20-

AIO

1-r-TT-T -nr--- r TrTTrTr-1-r rTg -iT~r
NovD JFMA 'J J A S 0 N D J F M A M j
1976/ 1977 TIME 19W8

released


Figure 8. Total, healthy, and dead third nymphal instar
populations of A. wojluini observed on leaves of C. sinensis var.
"California at Hacienda Santa Lucia, Yaritagua. (For an
explanation of dashed line, see page 38.)












TABLE 1

PERCENT HEALTHY AND DEAD NYMPHS OF A. WOGLUMI ON 60 SAMPLED LEAVES PER DATE
LOCALITY: YARITAGUA (HACIENDA "SANTA LUCIA")


____ h Nymph II INymph III % Infested Infestation
Date Total / Healthy % Dead Total % Healthy %Dcw ; Total % Healthy % Dead Leaves Index2
11/11/76 889 100.00 0.00 276 100.00 0.00 172 100.00 0.00 48.33 90.55

11/13/76 477 65.20 34.80 216 63.43 36.57 100 52.00 48.00 28.33 32.27
12/'C2/76 120 0.00 100.00 57 5.26 94.74 134 30.60 69.40 26.67 15.25
12/16/76 38 94.74 5.26 66 3.03 96.97 33 21.21 78.79 33.33 29.93 4
12/30/75 236 83.90 16.10 116 74.14 f.5.86 50 50.00 50.00 35.00 42.95
01/13/177 64 100.00 0.00 9 100.00 0.0t0 38 7.89 92.11 26.67 10.27
01/27/77 250 97.20 2.80 82 90.24 9.76 103 82.52 17.48 23.33 21.33
02/I]/77 239 100.03 0.00 122 100.00 0.00 88 90.91 9.09 25.00 15.70
0212'5/77 250 100.00 0.00 171 88.30 11.70 106 82.08 17.92 33.33 17.70
03,/10/77 183 100.C0 0.00 61 100.00 0.00 146 94.52 5.48 40.00 54.55
03'24177 704 100.00 0.00 57 100.00 0.00 15 100.00 0.00 35.00 54.33
04/11/77 1515 100.00 0.00 233 100.00 0.00 84 100.00 0.00 40.00 69.17
04/21/77 1359 98.90 1.10, 414 98.31 1.69 325 97.54 2.46 45.00 47.42
05/05/77 1213 100.00 0.00 612 100.00 0.00 325 88.62 11.38 51.67 50.48
05/19/77 j 451 100.00 0.00 138 95.65 4.35 175 74.29 25.71 48.33 43.20
06/02/77 660 100.00 0.00 150 100.00 0.00 55 51.00 49.00 63.33 116.32
06/16/71 1585 100.00 0.00 376 88.03 11.97 201 85.07 14.93 68.33 125.18
06/30/77 2199 90.86 9.14 1281 88.99 11.01 620 83.06 16.94 75.00 98.53














TABLE 1--Continued


iT
Nymiph I Nymph II Nymph III % Infested Infestation
Date To:. % Healthy % Dead Total % Healthy % Dead Total % Healthy % Dead LeavesI Index2

07/14/77 168 99.23 0.77 1079 82.85 17.15 884 67.08 32.92 58.33 80.85
07/23/77 637 100.00 0.00 378 80.16 19.84 477 40.04 59.96 63.33 72.95
103/11/77 673 98.51 1.49 265 87.55 12.45 266 41.73 58.27 53.33 125.23
08/25/77 2224 99.91 0.09 201 91.04 8.95 183 26.23 73.77 60.00 112.08
09/C8/77 1352 98.00 2.00 716 71.65 28.35 331 18.43 81.57 61.67 61.43
09/22/77 1308 94.27 5.73 545 49.91 50.09. 600 46.00 54.00 56.67 52.97
i0/36/77 415 84.52 15.42 196 11.73 88.27 112 43.75 56.25 41.67 34.92
10/20/77 580 86.38 13.62 307 73.94 26.06 197 27.92 72.08. 38.33 56.12
111/03/77 1083 85.78 14.22 420 61.43 38.57 331 43.50 56.50 33.33 47.20
11/17/77 610 92.13 7.87 434 68.20 3-1.80 432 62.50 37.50 41.67 29.75
01/12/78 520 95.19 4.81 213 34.74 65.26 358 5.59 94.41 51.67 69.97
02/20/78 995 96.58 3.42 271 60.15 39.85 353 53.26 46.74 63.33 39.48
04/13/78 743 94.48 5.52 475 64.63 35.37 686 75.95 24.05 48.33 44.00
06/15/78 0 0.00 0.00 0 0.00 0.00 0 0.00 0.00 20.00 1.17
02/22/79 0 0.00 0.00 0 0.00 0.00 0 0.00 0.00 0.00 0.00


1The % of infested

% Infested Leaves


leaves does not include leaves where
N leaves with live forms
60


only adults were found.


21nfestation Index = (Eggs + NI + NIl + NIII + Pupae) live forms
No of sampled leaves 60



















200-






100-
90-
80-
7 0 R H.


50-



OMax.



20N. 0TMieai



J0-
Evopor

Rain to
0 ... "T T -T-1--T I
Nov D J FM A M J J ASOND JFMAMJJ A SOND JF
19,76 1977 1978 1979




Figure 9. Average monthly temperature, relative humidity,
rainfall, and evaporation (shadow) for Santa Lucia and Apoliro
Citrus Orchards.








TABLE 2

SUMMARY OF MONTHLY DATA RELATING TO TEMPERATURE, RELATIVE HUMIDITY, RAINFALL
AND EVAPORATION FOR "APOLIRO" AND "SANTA LUCIA" ORCHARDS*


Nov. 76 Dec. 76 Jan. 77 Feb. 77 Mar. 77 ApI. 77 May 77 Jun. 77 Jul. 77

Rainfall (m.m.)
(Precipitation) 6.3 9.9 0.0 0.0 0.0 12.2 81.0 157.7 205.5

Mean Maximum 31.4 30.7 31.9 32.7 32.1 32.3 29.9 29.0 29.0
0

3 Mean Minimum 18.0 17.5 16.9 17.0 18.0 19.4 20.2 20.2 19.3
-W
E I Mean 24.9 24.2 24.4 24.9 24.8 24.4 25.0 24.4 24.3


Mean Relative
Humidity Daily (%) 77 76 70 70 68 76 81 85 37


Mean Evaporation
Daily (m.m.)(shadow) 1.9 1.6 3.9 4.4 4.2 4.9 2.7 1.6 1.6


*Data available from Agro-Meteorological Station, C.A. Central "Rio Turbio"







TABLE 2--Extended


Aug. 77 Sep. 77 Oct. 77 INov. 77 Jan. 78 Feb. 78 Apl. 78 Jun. 78 Feb. 79

Rainfall (m.m.)
(Precipitation) 111.2 43.0 33.5 32.9 2.8 0.0 121.0 225.0 1.0

U Mean Maximum 29.6 30.1 31.2 31.1 31.8 33.1 30.0 28.7 32.0
0

4- Mean Minimum 19.5 19.5 19.6 19.0 16.7 17.6 20.8 20.2 16.7

E Mean 24.5 25.3 26.3 25.6 23.8 25.4 25.4 24.6 24.4


Mean Relative
Humidity Daily %) 84 84 83 80 79 78 88 91 65

Mean Evaporation
Daily (m.m.)(shadow) 1.9 2.4 2.7 2.2 4.9 5.5 2.7 1.9 4.3








coccinellids of the genus Delphastus which were found as larvae and

adults and observed to feed on all stages of A. woglumi. Three species

of Delphastus were identified: D. pusillus (Lec.), Delphastus s.p. near

argentinicus Nunenmacher, and Delphastus sp. (Coleoptera: Coccinellidae).

However, the combined effect of these observed and suspected mortality

factors did not prevent a subsequent increase of the citrus blackfly

populations to even higher peaks when more favorable conditions returned.

Figure 10 and Table 3 show the population trends of the citrus-

blackfly pupae and the number of total, healthy, dead and parasitized

(with exit hole of the parasite) individuals per sample date.

Figure 11 and Table 4 show the percentage of parasitism in

dissected live forms (nymphs III and pupae) of citrus blackfly per

sample. These live forms were third nymphal instars and pupae counted

as "healthy" and dissected in order to more accurately measure the

percent parasitism of the field population. Dissections were made from

February 1977 to the end of the study.
From the data it is evident that prior to release of the parasite,

P. opulenta, the citrus blackfly was subject to high levels of unex-

plained mortality. For example, on January 13, 1977, only 9.71% of the

pupae were alive, and by January 27, this had declined to 3.39% with
42.37% of the pupae showing emergence holes of Cales sp. (Hymenoptera:

Aphelinidae). Still later on March 10, 1977, 25.71% of the pupae were

found by dissection to be parasitized by Cales sp. However, the effects
of this mortality failed to prevent resurgence of the citrus blackfly to

the even higher level observed June 16, immediately before P. opulenta

increased sufficiently to have a measurable effect on the host popula-

tion.
















IUVQ- 9 PUPA
900- I o TOTAL
800- 6 HEALTHY
700--_ o DEAD
600- A PARASITIZED
500- (With Hole)
400- I


C300- Iil l
w
-J 200 l l
/ T\!



D !,t
.:-, 1i~ 4II I iI*
oo-I

o60- 1

uj 50- I l\
11W 1 \\\'

40-
30- "1 A \\ '



20 1

10-
1"T7 7,r 'i 1 T17T7



NovD JF FJ ASONDJ F MAM J JA SON D J F
1976 197.7 1978 1979
P :. or'uento T I ME
rele sed



Figure 10. Total, healthy, dead, and parasitized pupa
populations of A. woqlumi observed on leaves of C. sinensis
var. "California" at Hacienda Santa Lucia, Yaritagua.
(For an explanation of dashed line, see page 38.)








TABLE 3
EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED LEAVES PER DATE
LOCALITY: YARITAGUA (HACIENDA "SANTA LUCIA")

Pupae % Infested Infestation
Date Eggs Total % Healthy % Dead % Parasitized Adults Leaves Index 2
(with holes)
11/11/76 3741 355 100.00 0.00 0.00 3 48.33 90.55
11/18/76 1365 193 36.79 61.14 2.07 2 28.33 32.27
12/02/76 813 215 27.44 64.19 8.37 44 26.67 15.25
12/16/76 1639 240 46.67 25.00 28.33 245 33.33 29.93
12/30/76 2079 325 58.15 39.69 2.15 53 35.00 42.95
01/13/77 530 103 9.71 90.29 0.00 59 26.67 10.27
01/27/77 876 59 3.39 54.24 42.37 1 23.33 21.33
02/11/77 388 133 84.96 11.28 3.76 0 25.00 15.70
02/25/77 346 256 89.06 7.42 3.52 139 33.33 17.70
03/10/77 2691 221 88.24 8.60 3.17 70 40.00 54.55
03/24/77 2364 142 84.51 14.79 0.70 125 35.00 54.33
04/11/77 2272 46 100.00 0.00 0.00 103 40.00 69.17
04/21/77 683 217 43.32 56.68 0.00 17 45.00" 47.42
05/05/77 838 139 56.12 43.17 0.72 13 51.67 50.48
05/19/77 1294 695 84.17 15.83 0.00 156 48.33 43.20
06/02/77 5721 562 73.31 26.69 0.00 423 63.33 116.32
06/16/77 5389 100 35.00 65.00 0.00 252 68.33 125.18
06/30/77 2203 134 41.79 56.72 1.49 92 75.00 98.53







TABLE 3--Continued


Pupae % Infested Infestation
Date Eggs Total % Healthy % Dead % Parasitized Adults LeavesI Index2
...._... (with holes) ....
07/14/77 1335 606 58.42 41.58 0.00 56 58.33 80.85
07/28/77 2551 1019 68.20 31.80 0.00 304 63.33 72.95
03/11/77 6169 647 52.40 47.45 0.15 310 53.33 125.23
08/25/77 4176 315 30.48 63.81 5.71 36 60.00 112.08
09/08/77 1522 712 37.22 62.50 0.28 3 61.67 61.43
09/22/77 1233 940 17.45 80.85 1.70 55 56.67 52.97
10/06/77 1503 536 31.53 63.06 5.41 113 41.67 34.92
10/20/77 2579 404 1.24 96.29 2.48 43 38.33 56.12
11/03/77 1416 429 19.81 79.02 1.17 21 33.33 47.20
11/17/77 469 553 34.00 60.40 5.61 0 41.67 29.75
01/12/78 3464 573 25.31 72.43 2.27 125 51.67 69.97
02/20/78 952 299 35.12 54.18 10.70 26 63.33 39.48
04/13/78 707 985 40.91 28.22 30.86 27 48.33 44.00
06/15/78 0 132 53.03 0.00 46.97 0 20.00 1.17
02/22/79 0 0 0.00 0.00 0.00 0 0.00 0.00


1The % of infested leaves

% Infested Leaves = No 1


does not include leaves where only adults were found.
eaves with live forms


21nfestation Index = {Egs + NI + NIl + NIll + Pupae) live forms
No of sampled leaves 60





















DISSECTED PARASITISM
PARASITIZED PUPAE
(With K1':e
HEALTHY PUPAE


50- /


/0-I\ \



4 i'

7\




Nov D J F M AM j J A S 0 N D J F MA M J J A SOND J F
IS76 1977 rIM 13" e 19? 9
P. opi.~r to







Figure 11. Percent healthy and parasitized (with hole)
pupae and percent dissected parasitism of A. woglumi observed
on leaves of C. sinensis var. "California" at Hacienda Santa
Lucia, Yaritagua. Foran explanation of dashed line, see
page 38.)










TABLE 4

PERCENT PARASITISM OF DISSECTED LIVE FORMS OF A. WOGLUMI ON 60 LEAVES PER SAMPLE
LOCALITY: YARITAGUA (HACIENDA "SANTA LUCIA")


Infected Infestation Dissected Parasitism % of Parasites Adult Observed Field
12 1 1_ en ___ Cae__Ppu
Date LeavesI Index N III Pupa % Parasitism % Healthy Cales sp. P. opulenta Gales sp. P. opulenta
i02/11/77 25.00 15.70 3 62 0.00 100.00 0.00 0.00 1 0
02/25/77 33.33 17.70 0 43 0.00 100.00 0.00 0.00 0 0
103/10/77 40.00 54. 55 12 58 25.71 74.29 25.71 0.00 0 0
03/24/77 35.00 1 54.33 3 95 13.27 36.73 13.27 0.00 0 0
04/1/77 40.00 6Q.17 17 40 3.00 100.00 0.00 0.00 0 0
04/21/77 45.00 47.42 30 70 3.00 97.00 3.00 0.00 0 0
release date 04/22/77
I05/35/771 51.67 50.48 61 56 0.00 100.00 0.00 0.00 0 0
057119/17 48.33 43.20 0 100 6.00 94.00 6.00 0.00 3 0
06/02/77 53.33 116.32 0 101 4.95 95.05 4.95 0.00 1 0
06/16/77 68.33 125.18 69 33 0.00 100.00 0.00 0.00 2 0
06/3o/77 75.00 98.53 43 57 0.00 100.00 0.00 0.00 0 0
107/14/77 58.3 80.85 12 88 0.00 100.00 0.00 0.00 0 0
07123/77 63.33 72.95 5 99 0.00 100.00 0.00 0.00 0 0
08/11/77 53.33 125.23 21 79 1.00 99.00 1.00 0.00 0 0
08/25/77 60.00 112.08 20 48 10.29 89.71 10.29 0.00 0 0
09/08/77 61.67 61.43 10 90 23.00 77.00 21.00 2.00 0 0
09/22/77 56.67 52.97 37 73 6.36 93.64 6.36 0.00 0 0














TABLE 4--Con tinued


% Infested Infestation Dissected Parasitism % of Parasites Adult Observed Field
Date Leaves Tndex2 N III Pupa % Parasitism % Healthy Cales sp. P. opulenta Cales sp. P. opuienta

10/06/77 41.67 34.92 0 100 0.00 100.00 0.00 0.00 0 0
10/20/77 38.33 56.12 55 5 3.33 96.67 3.33 0.00 0 0
11/03/77 33.33 47.20 32 85 0.00 100.00 0.00 0.00 0 0
i'/17/77 41.67 29.75 57 43 9.00 91.00 9.00 0.00 1 0
01/12/78 51.67 69.97 6 94 0.00 100.00 0.00 0.00 0 1
02/20/73 63.33 39.48 15 85 4.00 96.00 4.00 0.00 2 4
04/13/78 48.33 44.00 0 100 16.00 84.00 7.00 9.00 1 0
05/15/73 20.00 1.17 0 70 44.29 55.71 0.00 44.29 0 5
02/22/79 0.00 0.00 0 0 0.00 0.00 0.00 0.00 0 0


The % of infested

% Infested Leaves


leaves does not include leaves
NG leaves with live forms


where only adults were found.


2Infestation Index = (Eggs + NI + NIl + NIII + Pupae) live forms
N0 of sampled leaves 60








There is also a significant change in the relation of mortality
of immature stages of the citrus blackfly and total population numbers

following the release of 200 P. opulenta on 2 different trees (Fig. 3,
inoculated trees) of this grove. Prior to release there was no cor-

relation between number of dead individuals and total numbers of the

populations sampled. Following release of P. opulenta there was an

abrupt shift to a direct relation between the number of dead individuals
and the total number present resulting in coinciding peaks for the 2

categories (Figs. 6, 7, 8, and 10).

The first detection of the released parasite was made on Sep-

tember 8, 1977, when 2% of the citrus blackflies included in the samples

were parasitized by P. opulenta. The first adult parasite was seen in

the field on January 12, 1978 (Table 4). However, parasitized pupae

(with exit hole of the parasite) started to increase after August 1977,

and peaked in April 1978 (Table 3). Parasitism as found by dissection

varied but was generally low until February 1978, when it started to

increase and reached a peak on June 1978, with 44.29%. At this time,

P. opulenta was found to have almost completely displaced the only

native parasite (Cales 5R.) present in earlier samples. On this date,
the parasitized pupae (with exit hole of the parasite) reached the

highest percentage (Table 3 and Fig. 11), and all other stages of citrus

blackfly declined to 0.
In February 1979, complete biological control had been achieved,

and by December 1979, it was impossible to find any sign of A. woglumi

in this citrus grove.
Other natural enemies observed as mortality factors were yellow

aschersonia (Aschersonia 9oldiana Sacc. and Ellis); the jumping spiders








(Attidae); the coccinellid predators Azyasp., Scymnus sR. and

Cycloneda sanguinea L.; an anthocorid predator (Hemiptera: Anthrocoridae);

the assassin bug (Zelus sp.) and the tettigoniid predator Phlugis teres

DeGeer.

Apoliro Experimental Orchard

This citrus grove contained 2,635 trees in an area of 119,280 m2

(Fig. 12), and all trees received the last pesticide treatment (1 1.

Endrin + 3 kg. foliar fertilizer/400 Is. water) on November10, 1976,

but 2 of the sample trees did not receive this application. All

pesticide treatments were suspended from this date. This farm was

managed as a commercial grove with a good irrigation system, periodic

application (prior to November 10, 1976) of insecticides and fertilizer.

Figures 13 and 14 show the population trends of citrus blackflies

at Apoliro citrus grove. Figure 13 shows clearly the 5 generations of

A. woglumi through the year of study from November 1976 to November

1977. Those generations were the first in November, the second in

February, the third at the end of April and early May, the fourth in

July, and the fifth in October. Figure 14 shows the peaks of each of

the nymphal instars and the shift from 1 nymphal stage to the next

and occurred regularly every other sample date.
Figures 15, 16, and 17 show the population trends of each nymphal

instar and the number of total, healthy and dead individuals for each

sample date. As is evident from the data preceding release of P.

opulenta on April 22, 1977, the mortality factors (biotic and abiotic)
did not exert any substantial control on the populations of any stage

of A. wogumi (Tables 5 and 6). However, the highest percentages of











... ..... -----------...

......... 'f "



















.. . -, ,
C11"US ".IE S "-. -' .. S I- L- -L ---











INCC '-AI D CA3',CAPL T (,TC -PP,.AVE Cl:,
0- SAAK L IRFC ,nYL: S.* *l





Figure 12. Apoliro Experimental Orchard, Cabudare.






63


9000-
7000- o EGGS
ADULTS
5000 1


5000 N



U) I
uI I

LJ I000- I

0 800-
(0
600-

0-
zI
o 400-'I

I?


o 200-
w
a: I
MI
z 100-

80-
_"I / 'II I




40 I
30-


20--~

10 y ii
T o- rP1 rrr r~YF~-T~Ii




Nov! J F I AIM J S 0 N D J F M A M J J
1971 I I7 7" TIME 1973
P Oou,,!~la releos' J

Figure 13. Egg and adult populations of A. woglumi observed
on leaves of C. sinensis var. "Pineapple" at Apoliro Experimental
Orchard, Cabudare. (For an explanation of dashed line, see page 38.)





64


4000-
3000- o N I
oNII
0N 11
AN III
2000- (Heal"hy)






14 ~
700-] I
o500-
I I! '. i i
-L) It f '

300 i


I I i i 1



o -. !1II
10I
)90






4o--- ,
30-







t0'11 1971 T I M



Figure 14. First, second, and third nymphal instars of
A. woglumi observed on leaves of C. sinensis var.-"Pineapple" at
Apoliro"Experimental Orchard, Cabudare. (For an explanation of
dashed line, see page 38.)





























Figure 15. Total, healthy, and dead first nymphal instar
populations of A. woglumi observed on leaves of C. sinensis var.
"Pineapple" at Apoliro Experimental Orchard, Cabudare.
(For an explanation of dashed line, see page 38.)






66







4000 N I

3000 TOTAL
6 HEALTHY
0 DEAD
2000_ A





1000
900-
800-
700-
600-
>I
< 500-




ti
Id I
-: 400- i
0

30-


C)







70-

60-
4 Ii





.20-
10k
80 -A I |!






t
50 -i11




4030-t





NovO F IA M J J A S 0 N D J F tm A 41 J J A 3 0 Ni 0. J F
1976 ,ci;,sn, ree.s~ 1977 TIME 1978 1979































Figure 16. Total, healthy, and dead second nymphal instar
populations of A. woylumi observed on leaves of C. sinensis var.
"Pineapple" at Apoliro Experimental Orchard, Cabudare. (For an
explanation of dashed line, see page 38.)










2000


1000
900
800


u) 700
w
> 600
500
0
0 400

300

D
200

z
IL
0
Ad
m) 100

Z 80
70
60
50


NovD J F M AfM J J A S 0 N D J F M A M J
1976 reesed 1977 1978
TIME
















NIII
TOTAL
HEALTHY
DEAD


S'1 *|' 1"
NovD J F 'i A M J J A
1976 1977
relea ed


Figure
populations
"Pineapple"
explanation


i



C D J F M A M j J A S 0 N D J F
TiME 1978 1979


* Total, healthy, and dead third nymphal instar
A. woglumi observed on leaves of C. sinensis var.
Apoliro Experimental Orchard, Cabudare. (For an
dashed line, see page 38.)


2000











TABLE 5

PERCENT HEALTHY AND DEAD NYMPHS OF A. WOGLUMI ON 60 SAMPLEDLEAVES PER DATE
LOCALITY: CABUDARE ("APOLIRO" EXPERIMENTAL ORCHARD)


-F Nymph I Nymph II Nymph III Infested Infestation

Date ITotal %" Healthy % Dead Total % Healthy % lead Total % Healthy % Dead Leaves Index2
11/11/76 165 71.52 28.48 137 37.96 62.04 233 30.90 69.10 40.00 30.90
11/13/76 I 101 81.19 18.81 33 36.36 6-.64 38 42.11 57.89 43.33 29.22
12/02/76 298 95.64 4.36 78 47.44 52.56 252 78.57 21.43 45.00 51.15

12/16/76 1574 99.49 0.51 754 94.83 5.J7 900 90.22 9.78 58.33 129.42
12/30/76 694 97.55 2.45 1453 86.17 13.83 926 92.66 7.34 53.33 88.60
C!/13/77 377 97.88 2.12 481 90.85 9.15 633 87.05 12.95 45.00 43.73
01/27/77 303 97.69 2.31 165 95.15 4.15 301 88.37 11.63 50.00 36.88
02/11/77 134 10.0.00 0.00 170 97.65 2.35 243 90.95 9.05 60.00 84.10
02/25/77 1097 99.27 0.73 200 84.00 16.00 339 91.45 8.55 78.33 150.67
03/10/77 1879 100.00 0.00 481 100.00 0.00 196 83.16 16.84 75.00 141.08
03/24/77 1770 100.00 0.00 606 100.00 0.00 208 96.63 3.37 71.67 72.08
04/11/77 2045 100.00 0.00 1258 99.36 0.64 1502 95.87 4.13 73.33 143.32
04/21/77 716 97.77 2.23 365 87.67 12.33 526 66.92 33.08 85.00 88.08
release date 04/22/77
05/05/77 654 100.00 0.00 242 80.99 19.01 173 41.04 58.96 81.67 172.95
05/19/77 4036 100.00 0.00 411 90.51 9.49 143 22.38 77.62. 91.67 194.43
05/02/77 2959 100.00 0.00 584 94.86 5.14 345 56.23 43.77 71.67 121.38
05,/11/77 1732 99.65 0.35 1000 86.70 13.30 984 73.17 26.83 66.67 79.32
06/30/77 913 M00.00 0.00 578 96.19 3.81 572 75.52 24.48 70.00 79.15
I _ _ _ _ _ _ _ _ _ _ _ _ _














TABLE 5--Continued


e I Nyph I Nymph II Nymph III % Infested Infestation I
Date Total % Healthy % Ded Total % Healthy % Dead Total % Healthy % Dead Leaves Index2

07/14/77 685 100.00 0.00 234 58.85 46.15 368 25.00 75.00 85.00 131.08
07/2S/77 3293 97.85 2.15 528 69.13 30.87 336 13.10 86.90 80.00 172.33
08/11/77 2590 97.30 2.70 1378 79.68 20.32 615 52.20 47.80 83.33 142.20
08/25/77 2440 99.14 0.86 1246 65.81 34.19 1181 62.91 37.09 73.33 85.80
09/08/77 1130 100.00 0.00 1005 65.97 34.03 751 33.02 66.98 71.67 56.07
09/22/77 1858 97.15 2.85 837 62.96 37.04 745 31.95 68.05 85.00 94.33
110/06/77 1160 100.00 0.00 319 58.93 41.07 223 7.62 92.38 78.33 54.55
10/20/77 917 97.27 2.73 485 82.06 17.94 309 37.54 62.46 78.33 67.73
11/03/77 1880 95.64 4.36 617 55.75 44.25 510 25.69 74.31 81.67 61.55
11/17/77 1018 88.61 11.39 699 57.37 42.63 756 50.00 50.00 60.00 42.68
01/12/78 944 91.74 8.26 580 62.24 37.76 688 60.32 39.68 68.33 60.83
02/20/78 1104 99.00 1.00 454 66.30 33.70 361 33.52 66.48 90.00 126.20
04/13/78 1118 88.01 11.99 536 69.96 30.04 487 47.43 52.57 70.00 74.58
06/15/78 0 0.00 0.00 0 0.00 0.00 0 0.00 0.00 16.67 0.90
02/22/79 3 100.00 0.00 0 0.00 0.00 11 100.00 0.00 21.67 0.30


IThe Z of infested leaves does not include leaves where only adults were found.


% Infested Leaves

21nfestation Index


No leaves with live forms
60
_ (Eggs + NI + Nil + NIII + Pupae)
No of sampled leaves


live forms
60







TABLE 6


EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED LEAVES PER DATE
LOCALITY: CABUDARE ("APOLIRO" EXPERIMENTAL ORCHARD)


Pupae % Infested Infestation
Date Eggs Total % Healthy % Dead % Parasitized Adults Leaves1 Index2
_(with holes)
11/11/76 1370 385 62.86 30.91 6.23 185 40.00 30.90
11/18/76 1339 609 49.92 48.11 1.97 155 43.33 29.22
12/02/76 2520 113 25.66 72.57 1.77 114 45.00 51.15
12/16/76 4469 320 63.44 30.94 5.62 74 58.33 129.42
12/30/76 2055 576 82.29 14.41 3.30 9 53.33 88.60
01/13/77 811 571 79.86 19.61 0.53 44 45.00 43.73
01/27/77 633 1016 84.74 15.26 0.00 89 50.00 36.88
02/11/77 3573 1040 86.73 12.12 1.15 255 60.00 84.10
02/25/77 6273 1292 92.88 6.04 1.08 427 78.33 150.67
03/10/77 5570 391 95.14 4.86 0.00 59 75.00 141.08
03/24/77 1521 241 94.19 3.73 2.08 6 71.67 72.08
04/11/77 3142 948 76.16 23.63 0.21 76 73.33 143.32
04/21/77 3055 1077 79.67 19.96 0.37 55 85.00 88.08
05/05/77 8291 1421 81.98 17.87 0.15 311 81.67 172.95
05/19/77 6967 394 53.05 46.70 0.25 172 91.67 194.43
06/02/77 3499 325 23.69 74.46 1.85 31 71.67 121.38
06/16/77 1058 707 54.88 44.84 0.28 24 66.67 79.32
06/30/77 1907 1293 72.78 27.07 0.15 156 70.00 79.15







TABLE 6--Continued


Pupae % Infested Infestation
Date Eggs Total % Healthy % Dead % Parasitized Adults Leaves1 Index2
(with holes)
07/14/77 6718 641 38.07 61.15 0.78 273 85.00 131.08
07/28/77 6410 716 38.63 60.84 0.53 123 80.00 172.33
08/11/77 4501 580 15.86 82.93 1.21 151 83.33 142.20
08/25/77 870 1105 26.79 73.03 0.18 30 73.33 85.80
09/08/77 774 1243 44.17 55.83 0.00 38 71.67 56.07
09/22/77 2914 993 17.72 82.18 0.10 28 85.00 94.33
10/06/77 1183 1146 63.26 36.21 0.53 16 78.33 54.55
10/20/77 2417 711 33.90 66.10 0.00 72 78.33 67.73
11/03/77 1278 674 21.07 78.49 0.44 17 81.67 61.55
11/17/77 663 519 41.81 55.68 2.51 36 60.00 42.68
01/12/78 1416 936 63.25 36.54 0.21 92 68.33 60.83
02/20/78 5707 643 54.43 44.32 1.25 146 90.00 126.20
04/13/78 583 1088 36.95 50.18 12.87 46 70.00 74.58
06/15/78 0 263 20.53 0.00 79.47 0 16.67 0.90
02/22/79 0 103 3.88 58.25 37.86 0 21.67 0.30


IThe % of


infested leaves does not include leaves where only adults were found.


% Infested Leaves


No leaves with live forms


21nfestation Index = (Eggs + NI + NIl + NIII + Pupae) live forms
N of sampled leaves 60








dead first, second and third nymphal instars were in November 1976,
as a consequence of the insecticide treatment (Table 5). This could

also be the reason for the high percentage of dead pupae found on

December 2, 1976 (Table 6). During this time, precipitation was low

(Fig. 9 and Table 2); however, relative humidity was comparatively high

(76%) and the leaves were regularly covered by morning dew which favored

the development of Aegerita webberi, the only fungus pathogen present

in this grove during the study. Other natural enemies found in highest

number during November and December were Scymnus sp., Delphastus spp.,

Nodita sp., and Mantispilla sp. The combined effects of these observed

and suspected mortality factors did not prevent the citrus blackfly

populations from increasing to higher levels.
Figure 18 and Table 6 show the population trends of the citrus

blackfly pupae and the number of total, healthy, dead, and parasitized

(with exit hole of the parasite) individuals per each sample date.

Figure 19 and Table 7 show the percentage of parasitism in

dissected "healthy" live forms (nymphs III and pupae) of citrus

blackfly per sample.
From the data it is evident that prior to release of the parasite,

P. opulenta, the citrus blackfly, though subject to high levels of

Unexplained mortality, was able to maintain a population able to erupt

at frequent intervals to very high levels.
Following release of 100 P. opulenta on each of 8 different trees
(Fig. 12, inoculated trees), the number of dead citrus blackfly in-

creased and peaked at times coinciding with the peaks of immature
instars of A. woglumi (Figs. 15, 16,. 17, and 18). It should also be

noted that percentages of dead citrus blackflies increased as














PUPAE
TOTAL
6 HEALTHY
o DEAD
A PARASITIZEO
S i(With Hole)









1'\
ilN, \


2000




1000
900
800
700
600
),)500
w
'400
-J
0300

C')
-J 200
0
z




IX 80

'60
Z


\


/


Nov O J F M A M J
1976

re/ecse8


J A
1977


S 0 N D J F M A M J J A S 0 11 0 J F
1970 1979
T I ME


Figure 18. Total, healthy, dead, and parasitized pupa popula-
tions of A. woqlumi observed on leaves of C. sinensis var.
"Pineapple" at Apoliro Experimental Orchard, Cabudare.
(For an explanation of dashed line, see page 38.)


1'
II'




I
I
I
I
I
I
I
I,


I


I

I
I
I

I
1
I
I-


















110 0 DISSECTED PARASITISM
P PARASITIZED PUPAE
(With Hole)
100 6 HEALTHY PUPAE


90


80


70-
z\ I
WI


Ir I f





30-


20- j1

Io"




NovD J F A MJ J A S 0 N D J F M A M J J A S 0 N D J F
1976 t 1977 TIME1 1978 19T9
P o teMto
ADULTS GBSERVED ON FIELD







Figure 19. Percent healthy and parasitized (with hole) pupae
and percent dissected parasitism of A. woglumi observed on leaves
of C. sinensis var. "Pineapple" at Apoliro Experimental Orchard,
Cabudare. (For an explanation of dashed line, see page 38.)











TABLE 7

PERCENT PARASITISM OF DISSECTED LIVE FORMS OF A. WOGLUMI ON 60 LEAVES PER SAvIPLE
LOCALITY: CABUDARE ("APOLIRO" EXPERIMENTAL ORCHARD)


Infested Infestation Dissected Parasitismi % of Parasites Adults Observed Field
,Date LeavesI Index2 N II1 Pupa % Parasitism % Healthy Cales s. P. opulenta Cales sp. P. opulenta
T--
!02/i!/77 60.00 1 84.10 -- 95 0.00 100.00 0.00 0.00 0 0
02/25/71 78.33 150.67 -- 85 10.59 89.41 10.59 0.00 0 0
03/10/77 75.00 141.08 16 80 16.67 83.33 16.67 0.00 0 0
03/2-/77 71.67 72.08 19 94 5.31 94.69 5.31 0.00 2 0
U/111/77 73.33 143.32 5 95 18.00 82.00 18.00 0.00 2 0
04/21/77 35.00 88.08 1 99 0.00 100.00 0.00 0.00 2 0
: release date 04/22/77
05/05/77 81.67 172.95 -- 100 1.00 99.00 1.00 0.00 2. 0
05/19/77 91.67 194.43 -- 100 0.00 100.00 0.00 0.00 3 0
0/02/77 71.67 121.38 -- 57 19.30 80.70 19.30 0.00 4 0
06/16/77 66.67 I 79.32 -- 100 10.00 90.00 10.00 0.00 2 0
06/330/77 70,00 79.15 5 95 0.00 100.00 0.00 0.00 2 0
07/14/77 85.00 131.08 2 98 0.00 100.00 0.00 0.00 2 0
07/28/77 80.00 172.33 -- 100 10.00 90.00 10.00 0.00 1 0
08/11/77 83.33 142.20 34 66 11.00 89.00 11.00 0.00 0 0
03/25/77 73.33 85.80 5 95 0.00 100.00 0.00 0.00 1 0
09/08/77 71.67 56.07 7 93 O.Go 100.00 0.00 0.00 0 0
09/22/77 85.00 94.33 44 56 0.00 100.00 0.00 0.00. 0 0
10/06/77 78.33 54.55 -- 103 3.00 97.00 3.00 0.00 1 0













TABLE.7--Continued


7 Z Infested Infestation Dissected j Parasitism % of Parasites Adults Observed Field
Date Leaves' Index2 N III Pupa % Parasitiim % Healthy Cales sp. P. opulenta Cales sp. P. opulenta
'40/20/77 78.33 67.73 29 67 5.00 95.00 5.00 0.00 0 0
11/03/77 81.67 61.55 15 93 0.00 100.00 0.00 0.00 3
11/1/7/77 60.00 42.68 -- 100 0.00 100.00 0.00 0.00 2 0
011'12178 68.33 60.83 36 64 0.00 100.00 0.00 0.00 6 0
02/20/7a 90.00 126.20 -- 100 0.00 100.00 0.00 0.00 12 8
1 04/11378 70.00 74.58 3 89 18.48 81.52 7.61 10.87 6 5
,O&/15/78 16.67 0.90 -- 54 I11.11 88.89 0.00 11.11 2 11
o/22/79 21.67 030 11 4 0.00 lO.00 0.00 0.00 4 2


IThe % of infested
% Infested Leaves


leaves does not include leaves where only
NO leaves with live forms
60


adults were found.


21nfestation Index = (Egs + NI + NIl + NIII + Pupae)*. live forms
N0 of sampled leaves 60








P. puTlenta increased sufficiently to have a measurable effect on the
host populations (Tables 5 and 6).

Although adult parasites were first seen in the field on
February 20, 1978, the first evidence of presence of P. opulenta in

the leaf samples was observed on April 13, 1978, when 10.87% of the

citrus blackfly pupae were parasitized by P. opulenta (Table 7).
Parasitized pupae (with exit hole of the parasite) increased steadily

and peaked in June 1978 with 79.47% when P. opulenta was found to

have almost completely displaced the only native parasite (Cales sp.)

(Tables 6 and 7). On this date, June 1978, all other stages of citrus

blackfly declined to 0.
By February 1979, only 3 first nymphal instars, 11 third nymphal

instars and 4 pupae were found and complete biological control had

been achieved.

Other natural enemies observed as mortality factors were

the coccinellid predator Cycloneda sanguinea; the assassin bug

(Zelus sR.) and a spider web in which 34 adult citrus blackflies were

observed to be trapped.

Gloria de Lara Citrus Orchard

This citrus grove contained 2,045 trees in an area of 78,800 m2

(Fig. 20) and was supposed to receive normal commercial management.

However, because of management changes by the owner and uncertainties
caused by the agricultural reform of the government, there was a

shortage of workers and a succession of administrators responsible

for the grove. As a result, cultural practices including irrigation,

fertilization and application of pesticides were neglected or applied




















',1e I
.. . ... : .' .' ..

T, ..









GL:J 01 LR
". .. 7,"." / ", '** ,2 ".. '.,-<"/ -

-F ig e Glor, d /,/ ,, !




:..;/.., 4//.,
.
*- ."I; /-.1" .'

f it,' J -e ?*,O / -.._
1 1/, / 1 /II
0 ..,. v.T' '4/ -'




I 1rRULS OHC.A D
; IIGLCP!A 0i L.ARA
'I S A R t.E.
I DSTRI'O PL AVE .NO
.... I ....... 01(5. ,,tU h '

Figure 20. Gloria de Lara, Sarare.








capriciously. The parasite, P. opulenta, was not released in this

citrus grove.
Figures 21 and 22 show trend of citrus blackfly populations at

Glorida de Lara citrus grove. Figure 21 clearly shows 5 generations of

A. woglumi during the year of study from November 1976 to November 1977.

Those generations were the first in December, the second at the end

of February and early March, the third in June, the fourth in August,

and the fifth in October which was present only in the egg stage

probably because of high pupal mortality caused by fungus diseases

(A. webberi, A. aleyrodis, and A. goldiana) during the period from

August 25, 1977, to November 3, 1977 (Table 8), when the pupae popula-

tions declined to 0. During this time, high precipitation (Table 9)

favored the development of fungus diseases. Fungus diseases were the

principal mortality factor on this farm throughout the study period and

probably results from the generally high rainfall of this area

(Table 9). However, fungi did not prevent resurgence of citrus black-

fly pupae, and on February 20, 1978, the percentage of healthy pupae

was 67.33% (Table 8). Figure 22 shows the peaks of each of the nymphal

instars and the shift from 1 nymphal instar to the next.

Figures 23, 24, and 25 show the population trends of each nymphal

instar and the number of total, healthy and dead individuals for each

sample date. Table 10 shows the percentage of healthy and dead nymphs

of A. woluii.
Figure 26 and Table 8 show the population trend of the citrus

blackfly pupae and the number of total, healthy, dead and parasitized

(with exit hole of the parasite) individuals per sample date.










9000

7000

5000


3000




CO
w

UJ 1O00
_J
o 800

600
,)

o 400


020
C>
z

m
I,
o 200
ii

:D
z
100
80

60


30


o EGGS
ADULTS

















I '






I
I
I

tI
I

I
l '



I I
I I





NovD JF MAMJ J A S ON D JF I'm A M Jt
1976 1977 TIME !973 Julenta
Found


Figure 21. Egg and adult populations of A. woglumi observed
on leaves of C. sinensis var. "Valencia" at Glorida de Lara,
Sarare. (For an explanation of dashed line, see page 38.)














oNI
*Nil

(Heolthy)


5000-


2000-




1000-
, 800-
w

wj600
I -
0


-J


>200 -
3

..
0
100-
LL5
m
: 80-
z


/ -Ie
/


A -





JoyD J iM AM J JAOrJFA JJAO DF
376 1977 T I ME 1979 1979
j>PfL111rXJ F,-Lfld


Figure 22.
woglumi observed
de Lara, Sarare.


First, second, and third nymphal instars of A.
on leaves of C. sinensis var. "Valencia" at Gloria
(For an expla-nation of dashed line, see page 38.)


' '


60-


40-

50-


20-


I'.








TABLE 8


.EGGS, PUPAE AND ADULTS OF A. WOGLUMI ON 60 SAMPLED LEAVES PER DATE
LOCALITY: SARARE "GLORIA DE LARA" CITRUS ORCHARD)


- t 1~


_________ Pupae ________


% Healthy


% Dead


% Parasitized
(with holes)


Adults


% Infested
LeavesI


L 4. A 4. 4 4 +


96.65
58.74
33.05
35.99
35.05
98.92
81 .22
70.41
67.67
89.41
90.78
89.25
78.33
74.66
69.55
47.57
25.76
23.91


2.90
41.26
66.10
59.52
28.87
1.08
16.40
28.40
32.14
8.19
8.51
9.95
21.67
25.15
30.12
52.43
74.24
76.09


0.45
0.00
0.85
4.50
36.08
0.00
2.38
1.19
0.19
2.40
0.71
0.80
0.00
0.20
0.33
0.00
0.00
0.00


. .


9
20
206
26
10
11
2
27
113
32
11
0
17
29
84
701
179
77


41 .67
26.67
38.33
35.00
51.67
40.00
38.33
38.33
46.67
46.67
61.67
48.33
46.67
55.0
53.33
55.00
68.33
65.00


Infestation
Index2


52.15
12.23
25.50
39.02
52.18
35.85
24.70
32.80
47.60
66.82
63.52
56.90
41.63
28.72
33.03
68.48
81.28
67.37


Da te


Eggs


Total


11/11/76
11/18/76
12/02/76
12/16/76
12/30/76
01/13/77
01/27/77
02/11/77
02/25/77
03/10/77
03/24/77
04/11/77
04/21/77
05/05/77
05/19/77
06/02/77
06/16/77
06/30/77


1944
401
1347
1792
1750
492
340
1110
1783
2230
1276
438
481
718
711
3400
3098
1035


448
269
351
298
97
649
378
419
532
1001
282
623
960
509
601
370
66
230








TABLE 8--Continued


______ Ppae
% Infested Infestation
Date Eggs Total % Healthy % Dead % Parasitized Adults Leaves2 Index1
(with holes)

07/14/77 314 647 48.84 51.16 0.00 4 68.33 62.75
07/28/77 1268 1087 71.76 28.24 0.00 72 75.00 57.00
08/11/77 8605 1053 72.65 27.35 0.00 142 95.00 177.43
08/25/77 2718 455 7.91 92.09 0.00 170 73.33 77.82
09/08/77 634 508 1.77 98.23 0.00 4 76.67 75.47
09/22/77 34 524 26.91 73.09 0.00 1 58.33 25.82
10/06/77 129 285 28.42 71.58 0.00 1 48.33 17.78
10/20/77 190 418 1.44 97.61 0.96 1 48.33 18.27
11/03/77 20 388 0.00 100.00 0.00 0 15.00 5.52
11/17/77 74 264 6.82 92.80 0.38 0 25.00 9.37
01/12/78 66 96 13.54 86.46 0.00 0 23.33 8.7.3
02/20/78 413 339 66.67 33.04 0.29 5 38.33 15.48
06/15/78 0 101 67.33 0.00 32.67 0 13.33 1.13
03/27/79 0 220 0.00 67.73 32.27 0 13.33 0.97


1The % of infested leaves does not include leaves where only adults were found.


% Infested Leaves
21nfestation Index


N leaves


with live forms


60
- (Eggs + NI + Nil + NIII + Pupae) live forms
N0 of sampled leaves 60












TABLE 9

SUMMARY OF MONTHLY DATA RELATING TO RAINFALL FOR "GLORIA DE LARA" CITRUS ORCHARD*


6.0


Aug. 7?


316.7


Oct. 77


Rainfall (m.m.) 223.4 220.8 265.4 239.2 282.8 198.8 103.7 0.0 8.5

(Precipitation) Feb. 78 Mar. 78 Apl. 78 i May 78 Jun. 78 Jul. 78 Aug. 78 Sep. 78 Oct. 78


289.7


314.0


142.2


158.4


245.4


0.0


165.9


*Data available from Experimental Station of Araure (Ecology Seccion)


Jun. 77


Nov .


May 77


Jul 77


Sep. 77


Dec.


Jan. 78






87






3000-

N 1
2000- TOTAL
6 HEALTHY
0 DEAD



1000-
900-
800-
W700-,

< 600-
w
-J 500-
0
( 400-

j 300i


"- 200 j I




x I
00-

S80-
70- 4
60-
50-
I
40-

30I
i I
I I

20- I I

10- 1




Nov[ JF ,M J J J A SONDJ FAJtJ A SON 0 JFM
1976 1977 TIME 1978 1979
P V.mIfloG FounJ

Figure 23. Total, healthy, and dead first nymphal instar
populations of A. woglumi observed on leaves of C. sinensis var.
"Valencia" at Gloria de Lara, Sarare. (For an explanation of
dashed line, see page 38.)




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