UNIVERSITI PUTRA MALAYSIA BIOLOGY AND PREDATORY POTENTIAL OF GREEN LACEWING

(APERTOCHRYSA SP.)

MOHAMMED A. ALI HUSSAIN

FP 2010 36

BIOLOGY AND PREDATORY POTENTIAL OF GREEN LACEWING(APERTOCHRYSA SP.)

BY

MOHAMMED A. ALI HUSSAIN

Thesis Submitted to the School of Graduate Studies, Universiti PutraMalaysia in Fulfillment of Requirements of the Degree of

Doctor of Philosophy

June 2010

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DEDICATION

I dedicate this thesis to my parents, my wife Layla S. Hashim, my daughter Sara, and mysons Habib, Ahmed, Yassir, Bashir for their patience during my study in Malaysia,

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Abstract of thesis presented to the Senate ofUniversiti Putra Malaysia in fulfilment ofthe requirement for the degree of Doctor of Philosophy.

BIOLOGY AND PREDATORY POTENTIAL OF GREEN LACE"VING(APERTOCHRYSA SP.)

By

MOHAMMED A. ALI HUSSAIN

June 2010

Chairman: Professor Dzolkhifli Omar, PhD

Faculty: Agriculture

The green lacewings being active polyphagous predatos, can be mass reared in the

laboratory and used for classical, inundative and augmentative release against crops

pests. The green lacewings are also resistant to wide range of pesticide and one of the

most important biological control agents in integrated pest management.

The studie were conducted at University Putra Malaysia (UPM), to establish the

laboratory culture of Apertochrysa sp. The studies comprised of the following new and

original contIibutions: 1- Identified the important species of green lacewing and

surveyed the OCCUlTenceof Apertochrysa sp. in field and within the plants 2- Studied the

effect of temperature and type of prey on survival and development time of immature

stages 3- Established nest of life table studies 4- Determined axon of the functional

responses 5- Studied the effect of storage on eggs and pupae, and 6- Determined the

effect of insecticides on different stages of Apertochrysa sp.

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A total of 43 local plants were surveyed and only 18 plants were found with eggs of

Apertochrysa sp. The citrus trees showed the highest number of eggs of Apertochrysa

sp. recorded, 65.84% (4 eggs/ plant). The Telenomus sp. was highly affecting the eggs of

Apertochrysa sp. and the highest parasitism was recorded on the eggs collected from

com plants (14%), while the parasitism was 9.2% on eggs collected from citrus trees.

No significant differences between the heights (0-1 m, 1-2 m and 2-3 m) above the

ground on occurrence of eggs, but the east side recorded 79.8% of laid eggs, which

seemed to be more attractive to the females of Apertochrysa sp. for oviposition. In sweet

com,100% of eggs were found on the height of 1-2 m above the ground, and no

significant differences on the number of eggs laid between the east and west side of the

plant. The number of eggs of Apertochrysa sp. was found to be significantly different on

the lower and upper surface of the citrus and com leaf. At 60 days after planting of

sweet com the number of eggs of Apertochrysa sp. was found to be the highest.

The larval developmental times of Apertochrysa sp. at15°C, 20°C, 25°C, and 28±3°C

(laboratory condition) were 50.54, 41.9, 11.3, and 15.7 days respectively, and the total

developmental times from egg to adult were 88.36, 68.8, 29.5 and 33.3 days

respectively. The Apertochrysa sp. was successfully cultured and complete it's life cycle

on Corcyra cephalonica eggs, Rapolasiphum maidis, Aleurodicus disperses Russell and

Aleurocanthus woglumi Ashby and the total developmental times were 29.5, 25.4, 22.8

and 30 days respectively.

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The survivorship (Ix) of Apertochrysa sp. for three different cohorts indicates to high

mortality occurring during eggs, larvae (particularly 2nd instal') and pupae. The intrinsic

rate of natural increase (r) was 0.02 (females / female / day) with mean generation time

(T) was 40.6 days. The net reproductive rate (RO) of the population was 2.3. The

population double time (DT) was within 14.8 clays.

The highest number of aphids, R. maidis, was consumed by the third instar larva (42.95

aphids/ larva), followed by second instar (36 aphids/ larva), then the first instar (31.14

aphids/ larva). While the eggs of C. cephalonica were consumed by first, second and

third instar of larvae of Apertochrysa sp. are 68.4, 232.1, 494.6 eggs/larva respectively.

The longest storage period of eggs of Apertochrysa sp. was 9.49 days at 15°C followed

by 7.31 days at 20°C. While the pupae following 20 days of storage at 20°C showed the

lowest mortalitv (16.2%) with good percentage of good quality adults produced

(67.52%). However the pupae stored at 15°C for 40 days gave 100% disability.

The four insecticides (carbaryl, cypermethrin, azadirachtin, and imidacloprid) tested on

eggs of Apertochrysa sp. in the laboratory showed slightly harmful effect with eggs

mortality ranged from 43.33% to 63.33%.

When the insecticides were treated on the third instars larvae, the mortality at 72h was

less than 13.33% and all insecticides were categorized as harmless. The effect based on

successful pupation was categorized as harmless also for carbaryl (7% mortality),

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cypermethrin (l0% mortality), azadirachitin (23.15% mortality) and imidacloprid

(25.92% mortality).

Based on the successful molt to adults of the treated third instars larvae, cypermethrin ,

azadirachitin and imidacloprid were harmless while carbaryl was harmful. The

insecticides when treated on pupae showed harmless effect (mortality .:s 20%), however,

when the effect was based on the successful molting to adults from the treated pupae,

azadirachitin (10% mortality) was harmless, slightly harmful for cypermethrin (50%

mortality) and imidacloprid (56.7% mortality) and harmful for carbaryl (100%

mortality).

All four insecticides recorded harmful effect (100% mortality) when treated on the

adults of Apertochrysa sp. within 72h.

The newly recorded green lacewing Apertochrysa sp. is an important predator in

Malaysian agro-ecosystem environment. High tolerance to insecticides, high potential on

different insect pest and successfully mass culture of Apertochrysa sp. in laboratory

make it a good biological control agent can be used to control different lepidopteran and

homopteran pests.

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Abstrak tesis yang elikemukakan kepaela Senat Universiti Putra Malaysia sebagaimemenuhi keperluan untuk ijazah Doktor Falsafah

BIOLOGI DAN POTENSI PEMANGSA GREEN LACEWING(APERTOCHRYSA SP.)

Oleh

MOHAMMED A. ALI HUSSAIN

June 2010

Pengerusi: Professor Dzolkhifli Omar, PhD

Fakulti: Pertanian

'Green lacewing' sebagai pemangsa polyphagous aktif, boleh diternak secara besar-

besaran elalam makmal elan boleh eligunakan untuk gerak gempur klasik bagi menentang

haiwan perosak. Green lacewings juga mempunyai tahap ketahanan yang tinggi bagi

kebanyakan racun serangga elan merupakan satu agen kawalan biologi yang am at

penting elalam pengurusan haiwan perosak.

Kajian ini dilakukan eli Universiti Putra Malaysia (UPM), untuk menyeeliakan kultur

makmal Apertochrysa sp. Kajian tersebut meliputi mengenalpasti 1- Spesis penting

'green lacewing' elan meninjau kewujuelan Apertochrysa sp. eli lapangan elan elalam

tumbuhan-tumbuhan. 2- Kesan suhu elan jenis mangsa terhaelap jangka kehielupan elan

tempoh perkembangan tahap belum matang 3- Kajian jaelual jangka hayat 4- Rangkaian

fungsi tinelakbalas 5- Kesan penyimpanan terhadap telur dan pupa, dan 6- Kesan racun

serangga ke atas Apertochrysa sp. pada peringkat yang berlainan.

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Daripada 43 tumbuhan tempatan yang dikaj i selidik hanya 18 tumbuhan mempunyai

telur Apertochrysa sp. Pokok limau menunjukkan bilangan telur Apertochrysa sp. yang

tertinggi, 65.84% (4 telur/ tumbuhan). Telenomus sp. memberi kesan yang tinggi keatas

telur Apertochrysa sp. dan kesan parasitisma yang tinggi direkodkan pada telur yang di

kumpul dari pokok jagung (14%), manakala kesan parastisma pada telur yang dikumpul

dari pokok limau, 9.2%.

Tiada perbezaan ketara antara ketinggian dari paras tanah (0-1 m, 1-2 m dan 2-3 m)

dengan kehadiran telur, tetapi bahagian sebelah timur tumbuhan melaporkan 79.8% telur

seolah lebih menarik bagi Apertochrysa sp. betina untuk proses oviposisi. Pada pokok

jagung manis, 100% telur dijumpai pada ketinggian 1-2 m dari paras tanah, dan tiada

pcrbezaan ketara antara bilangan telur yang dijumpai pad a bahagian sebelah timur atau

barat, Bilangan telur Apertochrysa sp. yang dijumpai pada permukaan atas dan bawah

daun menunjukkan perbezaan yang ketara bagi kedua-dua pokok limau dan jagung.

Bilangan telur Apertochrysa sp. yang paling tinggi dijurnpai pada hari ke-60 selepas

penanaman pokokjagung manis.

Tempoh pertumbuhan larva Apertochrysa sp. pada suhu 15DC, 20DC, 25DC, dan 28DC

dengan ±3DC (keadaan makmal) masing-rnasing adalah 50.54, 41.9, 11.3, dan 15.7 hari,

manakala jumlah tempoh pertumbuhan dari peringkat telur ke dewasa adalah 88.4, 68.8,

29.5 dan 33.3 hari. Apertochrysa sp. telah berjaya dikulturkan dan menyempurnakan

kitaran hidup dengan telur Corcyra cephalonica, Rapolasiphum maidis, Aleurodicus

disperses Russell dan Aleurocanthus woglumi Ashby. Jumlah tempoh pertumbuhannya

rnasing-masing adalah 29.5,25.4,22.8 dan 30 hari.

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langka hidup (Ix) Apertochrysa sp. bagi tiga kelompok yang berlainan menunjukkan

angka kematian yang tinggi semasa peringkat telur, larva (khususnya instal' ke-2) dan

pupa. Kadar pertambahan semulajadi (r) adalah 0.02 (betina / betina / hari) dengan

purata tempoh penghasilan (T) 40.6 hari. Jurnlah kadar pembiakan purata (RO) bagi

populasi tersebut adalah 2.3 hari. Tempoh bagi mengganda dua (DT) populasi adalah

14.8 hari.

Bilangan tertinggi aphid, R. maidis, yang dimakan berlaku pada peringkat larva instar

ke-3 (42.95 aphid/ larva), diikuti dengan peringkat instar ke-2 (36 aphid/ larva),

kemudian peringkat instar pertama (31.14 aphid/ larva). Bilangan telur C. cephalonica

yang telah dimakan pada peringkat larva instar pertama, ke-2 dan ke-3 Apertochrysa sp.

adalah masing-masing sebanyak 68.4, 232.1,494.6 telurllarva.

Tempoh penyirnpanan telur Apertochrysa sp. yang paling lama adalah 9.49 hari pada

15De diikuti dengan 7.31 hari pada 20De, manakala pupa yang telah disimpan untuk 20

hari pada 20De menunjukkan angka kematian yang paling rendah (16.2%) dengan

menghasilkan peratusan dewasa berkualiti tinggi yang baik (67.52%).

Walaubagaimanapun, pupa yang disimpan pad a suhu 15De selama 40 hari menghasilkan

100% kecacatan.

Empat jenis racun serangga (carbaryl, cypermethrin, azadirachtin, dan imidacloprid)

yang telah diuji ke atas telur Apertochrysa sp. dalam makmal menunjukkan kesan yang

agak berbahaya di mana julat angka kematian telur adalah dalam lingkungan 43.33%

hingga 63.33%. Apabila racun serangga tersebut digunakan ke atas peringkat larva instar

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ke-3, angka kernatian pada jam ke-72 adalah kurang daripada 13.33% dan semua racun

serangga dikategorikan sebagai tidak berbahaya. Berdasarkan kesan-kesan racun

serangga terhadap kejayaan proses menjadi pupa, carbaryl (angka kematian 7%),

cypermethrin (angka kematian 10%), azadirachitin (angka kematian 23.15%) dan

imidaclopricl (angka kematian 25.92%) telah dikategorikan sebagai tidak berbahaya.

Berdasarkan kejayaan proses menjadi dewasa daripada larva instar ke-3 yang diracuni,

cypermethrin, azadirachitin dan imidacloprid adalah tidak berbahaya sementara carbaryl

adalah berbahaya. Racun serangga yang digunakan ke atas pupa menunjukkan kesan

yang ticlak berbahaya (angka kematian :s 20%). Namun begitu, berdasarkan kesan

terhaclap kejayaan proses menjadi dewasa daripada pupa yang diracuni, azadirachitin

(angka kematian 10%) aclalah tidak berbahaya, cypermethrin (angka kematian 50%) clan

imidacloprid (angka kematian 56.7%) adalah sedikit berbahaya dan carbaryl (angka

kematian 100%) adalah berbahaya.

Keempat-empat jenis racun serangga mencatatkan kesan berbahaya (angka kematian

100%) apabila cligunakan ke atas Apertochrysa sp. dewasa dalam tempoh 72 jam.

Green lacewing Apertochrysa sp.yang terbaru di rekodkan adalah pemangsa yang

penting dalam persekitaran agro-ekosistem Malaysia. Apertochrysa sp. mernpunyai

toleransi yang tinggi terhadap racun serangga, berpotensi tinggi terhadap serangga

perosak yang lain clan berjaya di kultur secara besar besaran di makmal. Ciri cm 1111

membolehkannya berfungsi sebagai agen kawalan biologi dan cligunakan untuk

mengawal berbagai perosak lepidopteran dan homopteran.

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ACKNOWLEDEMENTS

I wish to express my deep appreciation to member of my supervisory committee,

Professor Dr. Dzolkhifli Omar (Chairman), Professor Yusof Ibrahim and Associate

Professor Dr. Rohani Ibrahim, for being supportive to my ideas, and for being a source

of inspiration as a professional and as a human being. Special more thanks to my

supervisor Professor Dr. Dzolkhifli Omar for his help during difficult times, guidance,

critical discussions and encouragement in the preparation of this thesis.

I am also grateful to Professor Dr. Rita Mohmud Awang, Department of Plant

Protection, Faculty of Agriculture, UPM for advising me the first two semester of my

study.

My sincerely thank to Professor Dr. Ahmad Said Sajap, Faculty of forestry, UPM, for

the value information he gave to me which helped me starting my project.

Special thanks to all members of the Entomological Laboratory, Department of Plant

Protection, Faculty of Agriculture, UPM, particularly Mr. Mohammed Zaki, Mr.

Selvaragan, Mr. Manan Tikon. Mr. Hishamuddin Zainuddin and Mr. larkasi Sarbini for

their assistance.

The assistant and helps of Mr. Abdul-Rahman, field 2, Siti, and Mr.Sahrir, field 10 are

kindly acknowledged.

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I gratefully acknowledge to my friends and fellow graduate students in Plant protection

Department, especially the Toxicology and Entomology laboratory and particularly to

San San Win and Raga Mohammed for their cooperative and helps during my study.

Deepest thanks to Iraqi Agriculture Minster Professor Dr. Ali Al- Bahadily for helping

me to get the permission to complete my study in Malaysia.

I would like sincerely to thanks and grateful my brother Dr. Nejim alasdi and his wife

Dr. Zahra for all helps and kindly and I will never forget their beautiful children when

they award me special feeling make me more patient when I miss my family.

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This thesis submitted to the Senate of Universiti Putra Malaysia and has been acceptedas fulfilment of the requirement for the degree of Doctor of Philosophy. The members ofthe Supervisory Committee are as follows:

Dzolkhifli Omar, PhDProfessor / Insect ToxicologyFaculty of AgricultureUniversity Putra Malaysia(Chairman)

Yusof Ibrahim, PhDProfessor / Agricultural Entomology

Faculty of AgricultureUniversity Putra Malaysia(Member)

Rohani Ibrahim, PhDAssociate Professor / Insect TaxonomyFaculty of AgricultureUniversity Putra Malaysia(Member)

HASANAHProfessor and DeanSchool of Graduate StudiesUniversiti Putra Malaysia

Date: ~ 5 JUL 2010

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I certify that a Thesis Examination Committee has met on 24 May 2010 to conductthe final examination of Mohammed Abid Ali Hussain on his thesis entitled"Biology and Predatory Potential of Green Lacewing (Apertochrysa sp.)" inaccordance with the Universities and University Colleges Act 1971 andthe Constitution of the Universiti Putra Malaysia [P.U.(A) 106] 15 March 1998.The Committee recommends that the student be awarded the Doctor of Philosophy.

Members of the Thesis Examination Committee were as follows:

Zainal Abidin Mior Ahmad, PhDAssociate ProfessorFaculty of AgricultureUniversiti Putra Malaysia(Chairman)

Ahmad Said Sajap, PhDProfessorFaculty of ForestryUniversiti Putra Malaysia(Intemal Examiner)

Nur Azura Adam, PhDSenior LecturerFaculty of AgricultureUniversiti Putra Malaysia(Intemal Examiner)

Muhammad Ashfaq, PhDProfessor and DeanDepartment of EntomologyFaculty of AgricultureUniversity of AgricultureFaisalabadPakistan(Extemal Examiner)

J

KIM HUAT, PhDProfessor an Deputy DeanSchool of Graduate StudiesUniversiti Putra Malaysia

Date: 24 June 2010

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DECLARA TION

I declare that the thesis is my original work except for quotation and citation which havebeen duly acknowledged. I also declare that it has not been previously, and is notconcurrently submitted for any other degree at University Putra Malaysia or at any otherinstitution.

MOHAMMED A. ALI HUSSAIN

Date: 1 March 2010

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TABLE OF CONTENTS

DEDICATIONABSTRACTABSTRAKAKNO'WLEDGEMENTSAPPROVALDECLARA TIONLIST OF TABLESLIST OF FIGURESLIST OF PLATES

CHAPTER

1 INTRODUCTION

2 LITERATURE REVIEW2.1 Importance of green lacewings2.2 Life cycle of green lacewings2.3 Distribution of green iacewings2.4 Scientific classification of green lacewings2.5 Taxonomy of green lacewings2.6 The rearing of green lacewings

2.6.1 Natural preys of green lacewings2.6.2 DietsMass rearing and commercially of green lacewingsNatural enemies on green lacewingsThe effect of pesticides on green lacewingsApertochrysa sp.Malaysian green lacewing

2.72.82.92.102.11

3 FJELD SURVEY OF THE GREEN LACE\YINGS3.1 Introduction3.2 Materials and Methods

3.2.1 Study site3.2.2 Survey methods3.2.3 Identification of collected specimens3.2.4 The parasitism of Telenonius sp. on the eggs

of Apertochrysa sp. collected from citrus treesand com plants.

3.2.5 Survey the occurrence of Apertochrysa sp. onvarious plants

3.2.6 The occurrence of Apertochrysa sp. withinthe com field

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3.2.7 The oviposition placement of Apertochrysa sp. 47

3.2.8 The effect of plant's age on the oviposition of 49Apertochrysa sp.

3.3 Results and Discussions 493.3.1 Survey methods 493.3.2 The specimen's identification 503.3.3 The occurrence of green lacewing on various 50

Plants3.3.4 The parasitism of Telenomus sp. on the eggs 56

of Apertochrysa sp. in citrus trees and cornplants fields

3.3.5 The occurrence of Apertochrysa sp. eggs 58within the com field

3.3.6 The oviposional preference of Apertochrysa 61sp. within the plant

3.3.7 The effect of plant's age on the oviposition of 67Apertochrysa sp.

3.4 Conclusions 69

4 EFFECTS OF TEMPERATURE AND PREY ON 71SURVIVAL, DEVELOPMENT, AND SEX RATIOOF APERTOCHRYSA SP.4.1 Introduction 714.2 Materials and Methods 74

4.2.1 Rearing of Corcyra cephalonica 744.2.2 Rearing of Apertochrysa sp. 744.2.3 Effect of temperature on preimagenal 77

developments, survival and sex ratio ofApertochrysa sp.

4.2.4 Effect of prey on preimagenal developments, 78survival and sex ratio of Apertochiysa sp.

4.2.5 Data analysis 784.3 Results and Discussions 79

4.3.1 Effect of temperature on preimagenal 79developments, survival and sex ratio ofApertochrysa sp.

4.3.2 Effect of prey on preimagenal developments, 84survival and sex ratio of Apertochrysa sp.

4.4 Conclusions 87

5 LIFE TABLE AND POPULATION PARAMETERS 89OF A PER TOCHR YSA SP. (NEUROPTERA:CHRYSOPIDAE) REARED ON THE RICE MOTHC. CEPHALONICA (STAINTON) (LEPIDOPTERA:PYRALIDAE)

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5.1 Introduction5.2 Materials and Methods

5.2.1 Rearing of C. cephalonica5.2.2 Life table experiments in laboratory

5.3 Results and Discussions5.3.1 Mortality of immature5.3.2 Age-specific survival life table5.3.3 Age-specific fertility Schedule

5.4 Conclusion

6 FUNCTIONAL RESPONSES OF APERTOCHRYSASP.ON APHID RAPOLASIPHUM Jl1AIDIS. ANDEGGS OF CORCYRA CEPHALONICA ATLABORATORY CONDITION6.1 Introduction6.2 Materials and Methods

6.2.1 The predator Apertochrysa sp.6.2.2 The preys Rhopalosiphum maidis and

Corcyra cephalonica6.2.3 Predation6.2.4 Data analysis

6.3 Results and Discussions6.3.1 The predation on the aphid R. maidis6.3.2 The predation on the eggs of C.cephalonica

6.4 Conclusions

7 EFFECTS OF THE STORAGE OF EGGS ANDPUPAE OF APER TOCHR YSA SP. AND POST-STORAGE EFFECTS ON PUPAE7.1 Introduction7.2 Materials and Methods

7.2.1 Storage of eggs and pupae7.2.2 Data analysis

7.3 Results and Discussions7.3.1 Storage of eggs7.3.2 Storage of pupae

7.4 Conclusions

8 SUSCEPTIBILITY OF EGG, PUPA, LARVA ANDi- DULT OF APERTOCHRYSA SP. TOAZADIRACHTIN, CVPERMETHRIN,IMIDACLOPRID AND CARBARYL UNDERLABORATORY CONDITION8.1 Introduction8.2 Materials and Methods

8.2.1 Apertochrysa sp.

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8.2.2 Insecticides 1358.2.3 Methodology 1358.2.4 Statistical analysis 137

8.3 Results and Discussions 1388.3.1 Effects of insecticides on eggs of 138

Apertochrysa sp.8.3.2 Effects insecticides on pupae of 139

Apertochrysa sp.8.3.3 Effects insecticides on larvae of 140

Apertochrysa sp.8.3.4 Effects of insecticides on adults of 143

Apertochrysa sp.8.4 Conclusions 148

9 CONCLUSIONS AND RECOMMENDATIONS FOR 149FUTURE RESEARCH

REFERENCES 153BIODATA OF THE STUDENT 176LIST OF PUBLICATIONS 177

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