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1145313293 01411 3017
3 LIERARY

Michigan State
University

 

 

 

 

 

 

 

This is to certify that the

dissertation entitled
Ecology and behavior of Diadegma insulare
(Cresson), a biological control agent of
diamondback moth, Plutella xylostella (L.)

 

presented by

Idris Bin Abd-Ghani

has been accepted towards fulfillment
of the requirements for

 

 

Ph . D . degree in EntomologL

Wye/gal

Major prétéssor

 

Date June 26, 1995

MS U is an Affirmative Action/Equal Opportunity Institution 0-12771

 

PLACENRETURN Boxmmwomhchockomflunmm
TO AVOID FINES Mum on or baton date duo.

DATE DUE DATE DUE DATE DUE

      

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

ECOLOGY AND BEHAVIOR OF DIADEGMA INSULARE
(CRESSON), A BIOLOGICAL CONTROL AGENT OF
DIAMONDBACK MOTH, PLUTELLA XYLOSTELLA (L.)

By

Idris Bin Abd. Ghani

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Entomology

1995

Dim 1'4
PIuIc‘Ha {VIII
diimondbacl
studies were
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by 2100 h. ;
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“The of “mm:

ABSTRACT
ECOLOGY AND BEHAVIOR OF DIADEGMA INSULARE
(CRESSON), A BIOLOGICAL CONTROL AGENT OF
DIAMONDBACK MOTH, PLUTELLA XYLOSTELLA (L.)
By

Idris Bin Abd. Ghani

Diadegma insulare (Cresson) is an important parasitoid of diamondback moth,
Plutella xylostella L., in North and Central America. In the United States and Canada,
diamondback moth parasitism by D. insulare is nearly always > 75%. Field and laboratory
studies were conducted to assess the ecology and behavior of D. insulare. D. insular-e lived
longer with high fecundity when fed on flowers of Brassica kaber (D.C) Wheeler,
Barbarea vulgaris R. Br. and Daucus carota L. than on the other flowers. Flower's
morphological characters, corolla length and openings. were positively correlate with
longevity and fecundity of the parasitoid. D. insulare showed nine nectar-collecting
behaviors that depended on the accessibility of the flower's nectar. Diurnal foraging
activity of D. insulare females was influenced by temperature, light intensity and wind
speed while male foraging activity was affected by temperature and light intensity. Activity
generally began between 0800 and 1000 h, peaked between 1100 and 1300 h and stopped
by 2100 h. Plant density did not affect D. insulare parasitism rate, sex ratio or foraging
activity, but severely affected diamondback moth population. Parasitism of diamondback
moth larvae occurred in all habitats except in the middle of the woodland. Percent
parasitism was very high in most crop habitats and non-crop habitats (where D. carom is
the major plant present). Diamondback moth laid more eggs on the Brassica crops varieties
than on the wild Brassicaceae. Percent egg hatch was similar regardless of the host plant
offered. Percent of diamondback moth larval survival was also higher on the cultivated
than on wild Brassicaceae. There was no larval survival on B. vulgaris. Developmental

time of unparasitized and parasitized diamondback moth larvae was similarly affected by

 

Wh19151plants.
Campc’sfrt’ R. E
varieties than 1
field. the abunl
the host plants
Michigan did '
parent/rd N
many alternata
influenced h}
10. design Bra.

dependence 3

the host plants. Percent parasitism was lowest on Berteroa incana L. DC, Lepidium
campestre R. Br. and Erysimum cheiranthoides L., but generally higher on cultivated
varieties than on wild brassicas (except B. kaber and Brassica nigra L. Koch). In the
field, the abundance of D. insulare and its parasitism rate were not significantly affected by
the host plants (Brassica crops varieties). Although the lepidopterous insects collected in
Michigan did not appear to be alternate hosts of D. insulare, I found that D. insulare
parasitized two gelechiids that do not occur in Michigan. In nature, D. insular-e could have
many alternate hosts other than the plutellids, its major insect hosts, but this could be
influenced by their length of exposure for parasitism. Information from my study will help
to design Brassica crop agroecosystems that would favor D. insulare, reduce pesticide

dependence and improve diamondback moth management.

Copyright by
Idris Bin Abd-Ghani
1995

DEDICATION

This dissertation is dedicated to my wife, Norhayati Abd.Mukti,
without whose courage, understanding, patience and support none

of it would have been possible

I v. Ni 1
ptdcncc and er
my guidance Ct
George Ayers :
(Department of
identification. [
l‘nh'crsity} for
Adriatic Area. 5
Georgia) for 511;
and field cxpcn:
Wild flowers as 1
tnh‘t‘fSlly A gm
School Dissertat
Ih'ttncial sum)

home for the Ids

 

ACKNOWLEDGMENTS

I wish to express. my sincere thanks to Dr. Edward J. Grafius for his support,
patience and encouragement throughout this process. I also wish to thank the members of
my guidance committee: Dr. James Miller, Dr. Douglas Landis, Dr, James Kells, Dr.
George Ayers and Dr. Suzanne Thiem. Special thanks go to Dr. S. Stephenson
(Department of Botany and Plant Pathology, Michigan State University) for weed
identification, Dr. Anthony Shelton (New York Agriculture Experiment Station, Cornell
University) for twice donating cultures of diamondback moth, Dr. D. K. Weaver (South
Atlantic Area, Stored-Product Insects Research and Development Laboratory, Savannah,
Georgia) for supplying S. cerealella. Beth Bishop and Dr. Walter Pet for help in laboratory
and field experiments, Dr. Lan‘y Dyer and Dr. Paul Marino for cage design and ideas about
wild flowers as nectar sources. The Michigan Vegetable Council, Michigan State
University Agriculture Experiment Station and the Michigan State University Graduate
School Dissertation Completion Fellowship Program are gratefully acknowledged for their
financial support. Finally, to the faculty and staff of the Department of Entomology, my

home for the last few years, I wish to acknowledge my gratitude.

vi

LIST OF TAB
LIST OF FIG!
GENERAL I..\"
GEXTRAL M}
CHAPTER 1. V

I
t”
I:
inil’ttducz
Didii‘fidi\
Results ,1

Concluxi.
CHAPTER 2. .‘t
(l

m

Abxtmct

IDITQdUC.

 

Ihwnflt
RQMQC

COnCiUS

CHAPTER 3. I
'I

L

Ahmad

 

InLi-Itduk.

TABLE OF CONTENTS

LIST OF TABLES . . . . . . . . x
LIST OF FIGURES . . . . . . . . xii
GENERAL INTRODUCTION . . . . '. . 1
GENERAL MATERIALS AND METHODS . . . . 12

CHAPTER 1. Wildflowers as nectar sources for Diadegma insulare
(Cresson) (Hymenoptera: Ichneumonidae), a parasitoid
of diamondback moth, Plutella nylosrella (L. )(Lepidoptera:

Plutellidae). . . 16
Abstract . . . . . . . . 17
Introduction . . . . . . . . 1 8
Materials and Methods . . . . . . 19
Results and Discussion . . . . . . 23
Conclusions . . . . . . . . 37

CHAPTER 2. Nectar-collecting behavior of Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of diamondback

moth, Plutella xylostella (L.)(Lepidoptera: Plutellidae). . 39
Abstract . . . . . . . . 40
Introduction . . . . . . . . 41
Materials and Methods . . . . . . 42
Results and Discussion . . . . . . 45
Conclusions . . . . . . . . 56

CHAPTER 3. Diurnal foraging activity of Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of the diamondback

moth (Lepidoptera: Plutellidae). in the field . . . 57
Abstract . . . . . . . . 58
Introduction . . . . . . . . 59

vii

Materi‘
Resulu
Conclu

CHAPTER 4.

Ahslfilt‘
Intrudm
Material
Results .
Conclus

CHAPTER 5. I
I

T!
Abstract
Intmdu-ct
Matt‘tiuls
Results :11

Conclusir

 

 

Materials and Methods
Results and Discussion
Conclusions
CHAPTER 4. Effects of plant density on diamondback moth (Lepidoptera:
Plutellidae) and its parasitoid, Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae) . .
Abstract
Introduction
Materials and Methods
Results and Discussion
Conclusions
CHAPTER 5. Influence of habitats on the parasitism of diamondback moth,
Plutella xylostella (L. )(Lepidoptera: Plutellidae), by Diadegma
insulare (Cresson)(Hymenoptera: Ichneumonidae)
Abstract
Introduction
Materials and Methods
Results and Discussion

Conclusions

CHAPTER 6. Effects of wild and cultivated host plants on oviposition,

survival and development of diamondback moth (Lepidoptera:

Plutellidae) and its parasitoid, Diadegma insulae (Cresson)
(Hymenoptera: Ichneumonidae) . .

Abstract

Introduction

Materials and Methods
Results and Discussion

Conclusions

CHAPTER 7. Alternate hosts of Diadegma insulare (Cresson)(Hymenoptera:

Ichneum onidae), a parasitoid of diamondback moth
(Lepidoptera: Plutellidae): A preliminary search

Abstract

viii

60
63
75

76
77
78
79
81
91

92
93
94
95
98
l 10

112
113
114
115
121
136

137
138

Introduet
Materials
ResuIts a
Conclusii
OVERALL CO.‘
LIST OF REI-‘E
APPENDIX I
APPENDIX 1.1
APPENDIX 2

Evidenee
PIute/la .1‘

A
I n

M

 

 

Introduction . . . . . . . . 140

Materials and Methods . . . . . . 143

Results and Discussion . . . . . . 147

Conclusions . . . . . . . . 158

OVERALL CONCLUSIONS . . . . . . 159

LIST OF REFERENCES . . . . . . . 170

APPENDIX 1 . . . . . . . . 193

APPENDIX 1.1 . . . . . . -. . 194

APPENDIX 2 . . . . . . . . 195
Evidence of pre-imaginal overwintering of diamondback moth,

Plutella xylostella (L.)(Lepidoptera: Plutellidae) in Michigan . . 195

Abstract . . . . . . . 195

Introduction . . . . . . . 196

Materials and Methods . . . . . 197

Result and Discussion . . . . . 198

Conclusions . . . . . . . 203

References cited . . . . . . 204

ix

l. \V
Chapter ((‘
0.1

r

TahIe 1.

TubIe 2.

Chapter 2. \I'
I
m

TahIe I.

TahIe 2.

Chapter 3. D

(I
n

Table ].

ChaPter 4. ‘
P
(I
TabIc ].

 

Table 2.

 

LIST OF TABLES

Chapter 1. Wildflowers as nectar sources for Diadegma insulare
(Cresson) (Hymenoptera: Ichneumonidae), a parasitoid

of diamondback moth, Plate/la xylosrella (L.)(Lepidoptera:
Plutellidae).

Table 1. Species, common names, and families of wildflowers
used for the study

Table 2. Corolla length and opening diameter of wildflowers .

Chapter 2. Nectar-collecting behavior of Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of diamondback
moth, Plate/Ia xylosrella (L.)(Lepidoptera: Plutellidae).

Table 1. Species, common names, and families of flowers
used for this study, and mean longevity and fecundity
of D. insulare when fed on these flowers

Table 2. Nectar-collectin g behaviors of D. insulare females
observed in choice test with various flowers .

Chapter 3. Diurnal foraging activity of Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of the diamondback
moth (Lepidoptera: Plutellidae), in the field

Table 1. Multiple conelation statistics for Diadegma insulare
foraging activity .

Chapter 4. Effects of plant density on diamondback moth (Lepidoptera:
Plutellidae) and its parasitoid, Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae)

Table 1. ANOVA for effects of plant density, time of day and

canopy height on the temperature (0C) within the
broccoli canopy

Table 2. ANOVA for effects of plant density, time of day and
canopy height on the relative humidity (%) within the
broccoli canopy

20
33

43

46

67

88

90

APPEndix 2 I

Chapter 5. 1
1

Table 1.
Table 2.

Chapter 6.

-"‘ GIU‘ (A .—

Tahle I.

Tahle 2,

Chapter 7, 15

Table 1_

Table 2.

Table 3.

 

Table 4.

Table l.

 

 

 

Chapter 5. Influence of habitats on the parasitism of diamondback moth,
Plutella xylostella (L.)(Lepidoptera: Plutellidae), by Diadegma
insulare (Cresson)(Hymenoptera: Ichneumonidae)

Table 1. Number of D. insulare caught in various habitats from

12 to 18 August 1993 . . . . . 105
Table 2. Number of D. insulare caught in various habitats from

14 to 20 August 1994 . . . . . 105

Chapter 6. Effects of wild and cultivated host plants on oviposition,
survival and development of diamondback moth (Lepidoptera:
Plutellidae) and its parasitoid, Diadegma insulae (Cresson)
(Hymenoptera: Ichneumonidae)

Table 1. Species and common names of host plants used in the

study . . . . . . . 117
Table 2. Effect of host foods on percent parasitism, developmental

time of parasitized diamondback moth third instar, and

sex ratio of D. insulare . . . . 128

Chapter 7. Alternate hosts of Diadegma insulare (Cresson)(Hymenoptera:
Ichneumonidae), a parasitoid of diamondback moth (Lepidoptera:
Plutellidae): A preliminary search

Table 1. Insect larvae collected from the wild Brassicaceae
during the summer of 1993 and 1994 . . 149
Table 2. Lepidoptera larvae collected from the broccoli field In the
summers of 1993 and 1994, and percent parasitism by
Diadegma insulare. . . . . 150
Table 3. Percent parasitism of Phthorimaea operculella (Zeller) by

Diadegma insulare (Cresson), the male to female sex ratio
of D. insulare and percent parasitism of Plutella
xylostella (L. ) by D. insulare produced from P.

operculella. . . . 152
Table 4. Tortricids of apple orchard exposed for parasitism by
Diadegma insulare (Cresson). . . . v 154

Appendix 2 Evidence of preirnaginal overwintering of diamondback moth,
Plutella xylostella (L.)(Lepidoptera: Plutellidae) in Michigan

Table 1. Diamondback moth larvae or pupae or first instar
counted from weeds and detached weed leaves. . 199

xi

Chapter I. I
t
p.

Figure I

Figure 3_

FIgUrc 4

Figure 5.

 

 

 

LIST OF FIGURES

Chapter 1. Wildflowers as nectar sources for Diadegma insulare
(Cresson) (Hymenoptera: Ichneumonidae), a parasitoid
of diamondback moth, Plate/Ia xylostella (L.)(Lepidoptera:
Plutellidae).

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Longevity of D. insulare females fed on various
wildflowers as nectar sources. (G.H) indicates the
results from experiment conducted on plants brought
into the greenhouse for study. Columns with different
letters are significantly different (Fisher's Protected
LSD, P < 0.05) . .

Longevity of D. insulare females fed on various
wildflowers during June through September 1993.

Total fecundity per lifetime of D. insulare females fed on

various wildflowers as nectar sources. (G.H) indicates the

results from experiment conducted on plants brought
into the greenhouse for study. Columns with different
letters are significantly different (Fisher's Protected
LSD, P < 0.05). . . . .

Total fecundity of D. insulare females fed with various
wildflowers during June through September 1993.

Fecundity pattern (beginning on day 3 after emergence
from pupae) of D. insulare females fed on various
wildflowers as nectar sources.

Frequency of oviposition behavior made by D. insulare
females, fed on various flowers or honey+water, during

the first 20 min of exposure to diamondback moth larvae.

Columns with different letters are significantly different
(Fisher's Protected LSD, P < 0.05). .

The relationship between longevity (A) or fecundity (B)
and the frequency of ovipositional behavior made by

D. insulare females within the fusst minute of exposure
to host larvae. .

Longevity of D. insulare females in relation to corolla
length (A) and opening (B) of wildflowers.

xii

24

27

29

31

32

34

Figure

Chapter 2.

Figure L

Figure 3

Figure 4

Figarc 5.

ChaPter 3. D
(I

n

[:1qu ]

FISUW 2.

Figure 3.

 

 

Figure 9.

The relationship of fecundity of D. insulare females to
the corolla length (A) and Opening (B) of wildflowers.

Chapter 2. Nectar-collecting behavior of Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of diamondback
moth, Plutella xylosrella (L.)(Lepidoptera: Plutellidae)

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Number of visits (A) and time spent per visit (B) to
flowers by D. insulare in 30 min in choice test
experiment. Bars with different letters are significantly
different (Fisher's Protected LSD, P < 0.05).

Number of visits (A) and time spent per visit (B) to
corolla base by D. insulare in 30 min in choice test
experiment. Bars with different letters are significantly
different (Fisher's Protected LSD, P < 0.05).

Time spent per visit to flowers by D. insulare
females at different visit number in choice test
experiment. [Visit number = first, second, third,
fourth, fifth and sixth; visit to that flower species].

Number of visitors (D. insulare females) per flower
species per 30 sec in no-choice experiment. Bars

with different letters are significantly different (Fisher's
Protected LSD, P < 0.05).

Time spent per visit at the upper (A) and lower (B) one
third of corolla made by D. insulare in choice test
experiment. Bars with different letters are significantly
different (Fisher's Protected LSD, P < 0.05) .

Chapter 3. Diurnal foraging activity of Diadegnm insulare (Cresson)
(Hymenoptera: Ichneumonidae), a parasitoid of the diamondback
moth (Lepidoptera: Plutellidae), in the field

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Diurnal pattemss of D. insulare caught in the sticky traps
on 11 (A) and 13 (B) September 1993. .

Diurnal patterns of D. insulare caught in the sticky traps
(top), light Intensity and temperature (middle), and wind

speed (bottom) on 14 August (A to C) and 18 August
(D to F) 1993.

Diurnal pattems of D. insulare caught in the sticky traps
(top), light Intensity and temperature (middle), and wind
speed (bottom) on 22 August (A to C) and 5 September

(D to F) 1993.

Relationship between the number of D. insulare males
and females caught in the same traps.

xiii

36

49

50

53

53

54

64

65

66

71

Figure 1

Figure (

Chapter 4. l
l
1

Figure I
Figure 2

Figure 3,

Figure 5.

Chapter 5.

in r

FigUrc l

 

 

Figure 5.

Figure 6.

Comparison of the percent of the total day's D. insulare
caught on the sticky traps versus direct or visual
observations (males plus females). . . . 72

Relationship of D. insulare caught per sticky trap with

different numbers of host per plant. Effect of host

density (diamondback moth larvae) on D. insulare

activity. . . . . . . 74

Chapter 4. Effects of plant density on diamondback moth (Lepidoptera:
Plutellidae) and its parasitoid, Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae)

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Number of diamondback moth large larvae (A) and
pupae (B), and D. insulare pupae (C) in three different
broccoli densities (0.3, 0.6 and 0.9 m between plants). 83

Total D. insulare males plus females caught per plant
in three different broccoli planting densities (0.3, 0.6
and 0.9 m between plants). . . . . 87

Percent parasitism of field (A) and laboratory-reared

(B) diamondback moth larvae by D. insulare in the upper
versus lower broccoli canopy in the three different

broccoli planting denssities (0.3, 0.6 and 0.9 In between
plants). . . . . . . 89

Temperature (0C) in the upper (A) versus lower (B)
broccoli canopy planted in three different plant densities
(0.3, 0.6, and 0.9 m between plants). . . 88

Relative humidity (%) in the upper versus lower
broccoli canopy planted in three different plant densities
(0.3, 0.6, and 0.9 m between plants). . . 90

Chapter 5. Influence of habitats on the parasitism of diamondback moth,
Plutella xylostella (L.)(Lepidoptera: Plutellidae), by Diadegma
insulare (Cresson)(Hymenoptera: Ichneumonidae)

Figure 1.

Figure 2.

Location of habitats at Michigan State University research
farm used for study (a, apple; af, alfalfa; b, beans; c, corn;
t, tomato; w, woodland; wa, weedy areas). Letters with _",
'_',_ 'and'_ indicate the habitats were used only during
1992 and 1993,1992 to 1994,1993 and 1994,

respectively. . . . . 96

Percent parasitism of diamondback moth larvae by

D. insulare in various habitats on 10-11 August 1992.

In corn field treatment was placed + 30 m from the field

edge. Bars with different letters are significantly

different (Fisher's Protected LSD, P < 0.05). . 100

xiv

Figure 3

Figure 4

Figure 5

Figure 6

Chapter 6.

”Cup”

Fl{lure I.

Figure 2

 

 

 

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Percent parasitism of diamondback moth larvae by

D. insulare in various habitats on 23-24 July (A),

15-16 August (B) and 13-14 September 1993 (C).

In corn field treatment was placed + 30 m from the field
edge. Bars with different letters are significantly
different (Fisher's Protected LSD, P < 0.05)..

Percent parasitism of diamondback moth larvae by

D. insulare in various habitats on 12-13 August 1994.
In corn field treatment was placed + 30 m from the field
edge. Bars with different letters are significantly
different (Fisher's Protected LSD, P < 0.05).

Percent parasitism of diamondback moth larvae as
affected by the interaction between habitat and
month in 1993 (A) and year (B).

Relationshipbetween percent parasitism of diamondback
moth larvae by D. insulare and the distance from
the field edge. .

Chapter 6. Effects of wild and cultivated host plants on oviposition, survival
and development of diamondback moth (Lepidoptera: Plutellidae)
and its parasitoid, Diadegma insulae (Cresson)(Hymenoptera:
Ichneumonidae)

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Numbers of eggs laid by diamondback moth females on
Brassica plants in choice (A) and no-choice (B) test. Bars
with different letters are significantly different (Fisher's
Protected LSD, P < 0.05). .

Numbers of eggs laid by diamondback moth on the field
and greenhouse leaves of Brassica crops (A) and wild
species (B) of Brassicaceae.

Percent of larval survival from hatching through
second (A) and third through fourth (B) instars, and
developmental time of diamondback moth larvae
from hatch to pupation (C) when larvae were fed on
various plants in no-choice test. Bars with different
letters are significantly different (Fishers's Protected
LSD, P < 0.05). . . . .

Relationship between developmental time of parasitized

and unparasitized diamondback moth larvae fed on
various host plants.

XV

101

102

103

103

122

124

126

130

Figure 5

Appendix 2 l
I

Figure I

 

 

 

Figure 5.

Distribution patterns of diamondback moth small
(first - second instars)(A) and large larvae (third -
fourth instars)(B), total larvae counts (C), and percent
parasitism of the diamondback moth larvae by

D. insulare (D) on different cultivated brassicas crop.
Bars with different letters are significantly different
(Fishers's Protected LSD, P < 0.05).

Appendix 2 Evidence of preimaginal overwintering of diamondback moth,
Plutella xylostella (L.)(Lepidoptera: Plutellidae) in Michigan

Figure 1.

Average daily air (A) and soil (above debris or sod
surface)(B) temperature, numbers of days snowing or
below freezing (C) and the degree-days accumulation
(D) for October to December 1992 and January to May
1993 (Michigan State University Horticulture Farm,
1.5 km southeast of Collins Road Entomology Fram).

xvi

132

200

GENERAL INTRODUCTION

Th
on plants I
With mu.\L
and tropic
1962). 31
such as A
St‘llr‘tux‘ QC
middle 01
IRObertsi

L
lengm 01'
lchctieic
[here are
and Adult
apparent]

1982‘ YL‘

GENERAL INTRODUCTION

The diamondback moth, Plutella xylostella (L.), is an oligophagous insect and feeds
on plants that contain mustard glucosides (Thorsteinson 1953). Important economic crops
with mustard glucosides are members of the family Brassicaceaegrown both in temperate
and tropical regions. Diamondback moth was first recorded as a pest in 1746 (Harcourt
1962). Since then there have been many accounts of its importance. In some countries
such as Argentina, Australia, New Zealand and South Africa, diamondback moth caused
serious economic losses to Brassica crops well before 1930 (Muggeridae 1930). In the
middle of 1930's the moth was recorded as a pest of brassicas in many parts of the world
(Robertson 1939).

Levels of diamondback moth infestation vary with locality, conducive environment,
length of growing season, number of acres of brassicaceous crops grown and frequency of
insecticide application (Lim 1986, Yamada & Koshihara 1978, Sun et al. 1978). Although
there are evidences of pre-imaginal overwintering (Honda 1992, Dosdall 1994, Appendix 2)
and adult hibernation (T alekar & Shelton 1993), it is generally accepted that DBM
apparently does not survive in the severe winter weather (Harcourt 1986, Smith & Sears
1982, Yoshio 1987, Theobald 1926). In the northern United States, Harcourt (1986)
suggested that annual infestations arise from adults that disperse from winter breeding sites
in the southern United States and are carried northward in the spring, usually in the last half
of May, by favorable winds and are favored by high temperature and low rainfall. Similme
in Japan, this insect migrates from southwestern islands, some of which are warm
subtropical, to the cooler temperate climate of Honshu and Hokaido (Honda 1992). Similar

migrations probably occur in other parts of the world such as New Zealand, Australia,

 

South Africa.
diamondbacl
migration of
EurOpe with
indicate that .
cover distant
and high 3111'.

Com:
the most pop
Chemical int
esfem'alerate
mCmOml'Il. '.

Parathiun) it;

 

Maggam 3; 1
I992. Fahrm|
Whamc on c
diamolldbacj
mommend,
Malaysia's \.
effecfively (

3
South Africa, and southern parts of Chile and Argentina. Chu (1986) estimated that
diamondback moth can fly continuously for several days as far as 3,000 km. Mass
migration of diamondback moth is also reported from Finland to England and other part of
Europe with distances over 3,680 km (French 1967, Lokki et al. 1978). These studies also
indicate that diamondback moth adults can remain in continuous flight for several days and
cover distances of 1000 km per day, but how the moths survive at such low temperatures
and high altitude is not known.

Control of diamondback moth by conventional chemical pesticides has so far been
the most popular method practiced by the majority of farmers throughout the world.
Chemical insecticides, including pyrethroids (cyperrnethrin, deltamethrin, pennetlrrin and
esfenvalerate), insect growth regulators (chlorofluazuron), carbamates (carbaryl and
methomyl), and organophosphates (metamidophos, dictrophos, triazophos and methyl
parathion) are commonly used (Liu et al. 1982a & b, Ho et al. 1983, Perng et al. 1988,
Maggaro & Edelson 1990, Cheng et al. 1992, Leibee & Savage 1992, Shelton & Wyman
1992, Fahmi & Miyata 1992, Fauziah et al. 1992). This unilateral approach and over
reliance on chemicals has resulted in the development of insecticide resistance by
diamondback moth (Ooi 1986). For example, in spite of spraying at higher than the
recommended rates and changing insecticides to replace the ineffective ones, 70% of
Malaysia's vegetable growers were still unsuccessful in controlling diamondback moth
effectively (Lim 1974). It is not surprising that 30% of the production cost is used to buy
insecticides (Lim 1974).

Resistance of diamondback moth to DDT and BHC was reported during the late
19503 (Henderson 1957). Organophosphates (OP) and carbarmates were used as
alternative insecticides and again resistance problems arose (Ho 1965). Pyretlrroids were
used extensively to replace or alternate with the above-mentioned insecticides.
Diamondback moth also developed resistance to pyrethroids, (Sun et al. 1978, Georghiou
1981, Miyata et al. 1982, Chen & Sun 1986, Tabashnik et al. 1987).

T
problem.
(Elliot er
dialinon
cyperme
diamond
resistant
kinds ()1
found th
01. resist.

Diamon

4

Tactical reliance on new products to combat resistance, far from resolving the
problem, has rendered the genetics and biochemical basis of the trait increasingly complex
(Elliot et al. 1987). Liu et al. (1982a & b) found that diamondback moth resistance to
diazinon (OP) showed significant cross-resistance to the pyrethroids such as pennethrin,
cypermethrin, deltamethrin and esfenvalerate. Fahmy & Miyata (1992) reported that
diamondback moth resistance to insect growth regulators (IGR) gives broad spectrum cross-
resistance to various types of insecticides. The occurrence of multiple resistance to many
kinds of insecticides has also been reported by Liu et al. (1982b) and Cheng (1988). They
found that this phenomenon was probably due to the presence of non-metabolic mechanisms
of resistance in addition to the microsomal functional oxidase (mfo) enzymes.
Diamondback moth also has been reported to be capable of developing resistance faster to
most toxic insecticides like synthetic pyrethroids than less toxic insecticides like carbarmate
(Cheng 1988). This resistance resulted primarily from reduction in cuticular penetration,
increase in detoxification and insensitivity of the site of action.

Different approaches have been tried to overcome the resistance developed by
diamondback moth to chemical insecticides. For instance, microsomal oxidase inhibitors
such as piperonyl butoxide and DDT-dehydrochlorinase inhibitors have been added as
synergist but results were unsatisfactory (Liu et al. 1982a & b). Next, a microbial
insecticide, Bacillus thuringiensis Berliner var. kurstaki, was used as an alternative method.
However, resistance to B. thuringiensis developed, even to the genetically improved strains,
within two to three years after its introduction in the field (Tabashnik et al. 1990, Jansson
1992). Tabashnik et al. (1991) reported that resistance to B. thuringiensis is more persistent
than resistance to chemical pesticides like esfenvalerate. Schwartz et al. (1991) found that
the resistance is physiologically based because resistant and susceptible larvae did not avoid
feeding on B. thuringiensis treated leaves. The inability of mixtures or rotations of B.
thuringiensis toxins to retard evolution of resistance and speed-up restoration of

susceptibility in the absence of treatments was also pointed out by Tabashnik et al. (1992).

The only 101
fewer ad \‘Cf
because 8. I
required for

Bee;
insects that .-
compatihle '
find ways tr"-
Soares and (
endotoxin to
genetically (
61:11. 1983,).
such as Dip,
Parasitoid 1,,
”’“ri’lsientri
homozyg,-,U
Risistam 1‘“
example, if
non‘u'anSgg

polalmso ‘I

 

6fndomxi'
(F'Xl‘epldtf;
1992). I

In SI

   
 

emlimnmer'
1

factors (Ha.

5
The only long term advantage of B. thuringiensr's over chemical pesticides is that it has
fewer adverse effects on the predators and parasitoids of diamondback moth. This is
because B. rhuringiensis must be ingested to be effective and specific gut conditions are
required for toxicity (Fast & Donaghue 1971).

Because it is safe to the environment and beneficial insects, has no cross-resistant to
insects that are resistant to conventional insecticides (Soares & Quick 1992), and is
compatible with other control methods (Iman et al. 1986, Kao & Tzeng 1992) studies to
find ways to increase 8. thuringiensis effectiveness have been intensified. For example,
Soares and Quick (1992) reported that a new B. thuringiensis product (MVP), a 6 -
endotoxin toxin of B. thuringiensis bioencapsulated within a killed cell preparation of a
genetically engineered of another bacterium (Pseudomonas)(Feitelson et al. 1990, Kronstad
et al. 1983), performs five to six times better than the older B. thuringiensis formulations
such as Dipel or Javelin. However, recent studies indicated that B. thuringiensis kills the
parasitoid larvae within its host larvae (Idris & Grafius 1993c). Very recently, B.
thuringiensis-transgenic Brassica crops have been developed and are reported to kill only
homozygous and heterozygous susceptible larvae (Shelton & Tang 1994), indicating
resistant problems will not be resolved except with intelligent use of this new method. For
example, if B. thuringiensis—transgenic cabbage is used then it should be interplanted with
non-transgenic plant as suggested by Ferro (1993) in planting B. thuringiensis-transgenic
potatoes. The transgenic B. thurt'ngiensis lines of cotton were reported not to express the
5 -endotoxin at levels sufficient to have a relatively large influence on Helicoverpa virescens
(F.)(Lepidoptera: Noctuidae) behavior, growth, survival or plant damage (Benedict et al.
1992).

In spite of the wide adaptability of diamondback moth towards different
environments and insecticides, it appears to be held in check in some regions. For instance,
in Canada, diamondback moth outbreaks do occur when populations fail to be held by biotic

factors (Harcourt 1960). Marsh (1917), reported that diamondback moth is normally

repressed 1‘.
absent or in
Ox'e
parts of the
important. .
pupae. respt
of the gamer
dominate vvl
moth. The c
contribute li
diamondhac
al. 1992. WI
5111).. most 0:
1993),

In R
and Second;1
010419ng 31
1968‘ Hater)
1986). Dian

COIesia and

 

 

6
repressed by parasitoids and may become a serious pest only where the natural enemies are

absent or ineffective (Lim et al. 1986).

Over 90 species of parasitoids of diamondback moth have been recorded in various
parts of the world (Goodwin 1979). However, only about 60 of them appear to be
important. Among these; 6, 38, and 13 species attack diamondback moth eggs, larvae and
pupae, respectively (Lim 1986). Despite this range of parasitoid species, larval parasitoids
of the genera Diadegma and Micropliris, Coresia (= ApantalesXBraconidae) tend to
dominate wherever they occur and are very important mortality factors for diamondback
moth. The egg parasitoids belonging to the genera Trichogramma and Trichogrammatoidae
contribute little to natural control even though research to find strains that prefer
diamondback moth's eggs in the field have been increased quite recently (Keinmeesuka et
al. 1992, Wiihrer & Hassan 1993, Klemm et a1. 1992, Vasquez 1994). A few Diadromus
spp., most of which are pupal parasitoids, also exert significant control (Talekar & Shelton
1993).

In Romania alone, over 15 species of lchneumonidae and Braconidae act as primary
and secondary parasitoids of diamondback moth (Mustata 1992). In North America,
Diadegma spp. and M. plutellae (Muesback) are dominant (Marsh 1917, Pimental 1961 &
1968, Harcourt 1963a & b, Oatrnan & Platner 1969, Putnam 1968 & 1973, Lasota & Kok
1986). Diadegma and Diadromus species dominate in Europe (Hardy 1938), Africa (Ullyett
1947, Abbas 1988) and New Zealand (Hardy 1938, Todd 1959). In Russia, Diadegma.
Cotesia and Diadromus spp. appear dominant (Kopvillem 1960a & b). Cotesia is an
important genus in Asia and other tropical regions because Diadegma are less adapted to h0t
conditions (Chang 1974, Wang et al. 1972, Ooi 1986, Sastrosiswojo & Sastrodiharjo
1986, Talekar & Yang 1989, Yang et al. 1993).

Diadegma spp. are more competitive than the other diamondback moth parasitoids
because they have excellent searching capacity, high fecundity, synchronize with the

development of their host and are capable of avoiding superparasitism or multiple parasitism

 

(Harcourt l9
Brassica en
the genera D

1988, Talek.
I

Bolter 8; La:
factors for d
moth by D. l

(_Biever er al

 

diamondbae
diamondbae
PUPUIthion r
199”. diam.
beCame the
(SEBUDSIW
“one with
incofl‘fmt
in a Signii
Taiwan it
end of 111.
1989). l

PrOvjch

7
(Harcourt 1986, Bolter & Laing 1983, Wage 1983). Diadegma presence and abundance in
Brassica crop agroecosystems were reported by Harcourt (1986) and Mustata (1992). Of
the genera Diadegma, D. semiclausum (= eucerophaga)(Hellen)(Santoso 1979, Abbas
1988, Talekar & Chang 1989) and D. insulare (Cresson) (Harcourt 1969, Putnam 1973,
Bolter & Laing 1983, Lasota & Kok 1986, Idris 1991) are the most important mortality
factors for diamondback moth larval populations. For instance, parasitism of diamondback
moth by D. insulare was between 74 an 90 % in Washington and Oregon, United States
(Biever et al. 1992). In southern Ontario, Canada, D. insulare parasitizes as high as 75% of
diamondback moth larvae (Harcourt 1969). In Indonesia, D. semiclausum, an introduced
diamondback moth parasitoid from New Zealand, effectively suppressed diamondback moth
population with > 80% parasitism in some areas (Sastrosiswojo & Sastrodiharjo 1986). In
1990, diamondback moth was effectively controlled by D. senu'clausum and this parasitoid
became the most important biocontrol agent of diamondback moth in Indonesia
(Sastrosiswojo & Setiawati 1992). In the Cameron Highlands, Malaysia, D. semiclausum
along with Cotesia plutellae (Kurdjumov) and Diadromus collaris (Gravenhost) were
incorporated into the integrated diamondback moth management program package resulting
in a significant reduction in diamondback moth infestation (Ooi 1992). Studies. conducted in
Taiwan indicated that D. semiclausum parasitizes > 70% within one season, and towards the
end of that season diamondback moths could not be found in the field (T alekar & Yang
1989). D. semiclausum now occurs throughout the highland areas of Central Taiwan and
provides substantial savings in diamondback moth control (T alekar 1992).

Parasitism rate of diamondback moth by Diadegma spp. varies with time, locations
or regions, the dynamic and/or relation between each species, and its host population
density (Mustata 1992, Biever et al. 1992, Wage 1983, Goodwin 1979). For instance,
parasitism of diamondback moth by D. insulare is always high (>75%) in North America
(Harcourt 1986,1dris & Grafius 1993b, Biever et al. 1992), but it varies greatly (1.5 to
70%) in South America and Caribbean Islands (Alarm 1992). Generally, Diadegma spp. are

el'l'ectivt
tempera
produce
in Hi ghi
En glanr
parasiti:
Sastrod

by the r

pesticitl
insectic
(Idris d
1192\6 ).
$08111 it
of dim

18 3130

8
effective in areas with temperature range between 15 and 250C (T alekar & Yang 1991). At
temperature approaching 30°C, parasitism drops sharply and more male progeny are
produced (Yang et al. 1993). Therefore, in the tropical region Diadegma spp. are effective
in Highland areas and inferior to Cotesia spp. in the lowland areas (T alekar 1992). In
England, Waage (1983) found that although D. semiclausum aggregate in the field, its
parasitism rate is independent of the host density. In Indonesia, Sastrosiswojo &
Sastrodiharjo (1986) reported that the percentage parasitism of D. semiclausum is affected
by the present of surrounding vegetation.

There is evidence that diamondback moth's parasitoids can develop resistant to
pesticides applied in the field. In Michigan, diamondback moth parasitism by D. insulare in
insecticide treated plots was not significantly different from parasitism in the untreated plots
(Idris & Grafius 1993b). In Indonesia, Iman et al. (1986), Sastrosiswojo & Sastrodiharjo
(1986), Santoso (1979), and Ooi (1986) also reported that D. semiclausum and C. plutellae
seem to adapt to an environment of frequent pesticide application and their rate of parasitism
of diamondback moth is not adversely affected. The female to male sex ratio of C. plurellae
is also not altered if the pesticides are used judiciously (Ooi 1986).

In Taiwan, parasitism of diamondback moth by D. semiclausum and C. plutellae
was no different whether the cabbages were grown in monoculture where no pesticides
were used or in a mixed culture with non-brassicaceous crops, all of which were sprayed
frequently with pesticide (T alekar & Yang 1989 & 1993). They also observed that D.
semiclausum hovered over the insecticide treated Brassica crops but did not land. In
Hawaii, parasitism o diamondback moth larvae was higher in Brassica-tomato plots than
plots planted with brassicas crops alone which indirectly indicates that tomato plants had no
long-range effect on parasitism activity of C. plate/lac (Bach & Tabashnik 1990).

In the laboratory, C. plutellae and D. semiclausum were susceptible to malatlrion
and methyl parathion, but they were as tolerant as diamondback moth larvae to fenvalerate

(Chiang & Sun 1991). Fenvalerate is extremely toxic to D. insulare adults in the United

  
 

States (Idris t

plate/lac wax

insulare (ldri
Although D.
199331,. the p

killed Ildns e

 

Ian'ae are. Ies
the non-purl.
3Pl‘ilrt‘nt acti
severely aft;
than for [he
Hig
Parasitoidc
the ICXS Sci
MIT-lame
R‘SiStach
HOWCVer
diam 0nd;
brassicas
either lhr
Nymp r
iILSe'clici

eCOD'Om

1% m;

9
States (Idris & Grafius 1993a). In another study, LC95 value increased 2-fold after C.
plutellae was exposed to fenitrothion for 8 months (Ke et al. 1991). However, the pupae of
D. semiclausum and C. plutellae (T alekar & Yang 1991, Kao & Tzeng 1992) and D.
insulare (Idris & Grafius 1993c) were more tolerant to chemical insecticides than the adults.
Although D. insulare pupae and adults are not killed by B. thuringiensis (Idris & Grafius
1993a), the parasitoid larvae within the B. thuringiensis intoxicated host larvae are indirectly
killed (Idris & Grafius 1993c). Idris (1991) also found that parasitized diamondback moth
larvae are less sensitive to most insecticides commonly used in brassicas crops fields than
the non-parasitized diamondback moth larvae. Although acylurea (teflubenzuron) had no
apparent activity against adult males of D. semiclausum and C. plutellae, females were
seveme affected by this lGR as the percent parasitism was significantly lower the treated
than for the untreated individuals (Furlong & Wright 1993).

High rates of mortality achieved by D. insulare and other diamondback moth larval
parasitoids, their increasing adaptability in fields that are frequently treated with pesticides.
the less sensitive of their immature stages toward pesticides, and are not affected by plants
interplanted with Brassica crop indicate there is a potential for using them in insecticide
resistance management within an integrated diamondback moth management program.
However, for the future, insecticides will remain a powerful and essential tool in integrated
diamondback moth management. This is because high price short term crops, such as
brassicas, need a very effective control method. However, their use must be minimized
either through careful use or if other tactics fail to accomplish pest control effort (Binns &
Nyrop 1992). Shelton et al., (1982) and Lumaban & Ross (1975) recommended that
insecticides should be applied only during critical periods of crop growth or based on
economic threshold level (ETL) of pest and crop damage.

A prime strategy for controlling diamondback moth is to build a broader ecological
base that would make possible integration of various management techniques with more

emphasis on the conservation and maximum use of naturally occurring beneficial insects

   

(Tahzbhnik e:
toward any h
However. tht
important if \
(Haynes et all
introduced p.
response to t]
0i. pest L‘\'t\l\
[sing
reduce the in

D. semiclaus

 

1PM packagt
diamt‘tndhuct
brassiea Cft‘tf
iml‘ik‘t of Di
be SC‘K‘I‘Ch' ]
ParasitoidS (
spraying Cm
Chemical Co
pest‘parasiu

(3 pafim [C
Way ‘0 Prou
instanCc‘ lht
BL, as a {O(

rated E

10
(T abashnik et al. '1991). Natural enemies could decrease the rate of herbivore adaptation
toward any kind of selection pressure like pesticides exerted on them (Gould et al. 1991).
However, the techniques and philosophies of using natural enemies like D. insulare are very
important if we want to avoid pest evolving to develop resistance as it occurs on pesticides
(Haynes et al. 1980). A rapid resistance deve10ped by house fly, Musca domestica. L., to its
introduced parasite, Nosonia vitripennis (Pimental and Stone 1968) and the Australia rabbit
response to the released of viral disease, Myxomatosis (Ratcliffe 1959). are two examples
of pest evolving resistant to the biocontrol agents.

Using diamondback moth parasitoids as a control method has been emphasized to
reduce the insecticide resistance problem in certain countries. In certain parts of Indonesia,
D. semiclausum has been successfully used as biological agent for diamondback moth. An
1PM package, based on ETL which takes into account the percentage parasitism of
diamondback moth by D. semiclausum was superior over prophylactic control practiced by
brassica crops farmers in Malaysia (Loke et al. 1992, Ooi 1992). However, the potential
impact of Diadegma spp. like D. insulare on diamondback moth population dynamics will
be severely limited by pesticides, especially in areas of high pest density as occurred on
parasitoids of the cereal leaf beetle (Haynes & Gage 1981). The frequencies of pesticide
spraying could be reduced to spot treatments with successful integration of biological and
chemical control technologies (Grossman 1990, Gould et al. 1991). Manipulating plant-
pest-parasitoid interactions in crop ecosystem is another better alternative (Gould 1991).
The parasitoid management technique of growing beneficials in the field (refuges) is the best
way to protect biocontrol agents in heavily sprayed cropping system (Grossman 1990). For
instance, the potential of using wild Brassica such as yellow rocket, Barbarea vulgaris R.
Br., as a food source and refuge for D. insulare was suggested to be included in an

integrated DBM management (Idris & Grafius 1994).

T0 Ct
parasitoid 31‘
in natural ee
must be mad
some of the -.
population 1:
lnt‘onnation
agroecosyst.

diumondhut

H-1;

2;
H-3.
H-4.

 

———————-'l'—

 

11

To combat pests via parasitoids one must know precisely the activity of the
parasitoid and predators which limit pest populations. It is important that our interventions
in natural ecosystems be done on the basis of thorough biocenotic data. Our intervention
must be made in a way that it does not affect the beneficial fauna. In my study I examined
some of the ecological factors and behavior or activity of D. insulare that may affect its
population abundance and role as a biological control agent of diamondback moth.
Information from this study could help us to have an idea of how to design Brassica crop
agroecosystems that would favor D. insulare. reduce pesticide use and improve

diamondback moth management.
HYPOTHESES

H-l: Wildflowers, nectar-collecting behavior of D. insulare and host plants are
determinant factors in population abundance and role of D. insulare as a
biological control agent of diamondback moth.

H-2: D. insulare parasitism rate is habitat-dependent.

H-3:, Diurnal host foraging behavior of D. insulare varies with weather factors.

H-4: D. insulare has other hosts for overwintering that affect its population

abundance in the field
OBJECTIVES

1. To find wildflowers that serve as nectar sources for D. insulare.

2. To study the nectar-collecting behavior of D. insulare

3. To study the D. insulare foraging activity as affected by weather factors.

4. To study the effect of plant density on the populations of diamondback moth and

D. insulare

12
5. To investigate the influence of habitats on the parasitism of diamondback moth
by D. insulare
6. To study the effects of host plants on oviposition, survival and development of
diamondback moth and D. insulare

7. To search for alternate hosts of D. insular-e

GENERAL MATERIALS AND METHODS

13

Cm 1.
side
[lira
End -
“CR

PMS]

14

GENERAL MATERIALS AND METHODS

Sources of insects

Diamondback moth eggs (Geneva strain) were donated by Anthony Shelton, Cornell
University. The eggs were put on fresh cauliflower leaves (grown in the greenhouse) in
plastic pans (sterilized with clorox), with 3 x 6 cm screen lids, and kept in the growth
chamber at 25 : 2°C, R. H i 60 and a photo period of 16:8 (LzD). The hatched larvae were
fed with new fresh broccoli leaves every day until pupation. Plastic pans were changed
every other day to protect larvae from diseases. Pupae were collected and kept in Peui
dishes at 50C or used for further rearing. In 1994, new diamondback moth colony of
Geneva strain were donated by Anthony Shelton. This is because the previous colony had
become infected by microsporidia disease.

D. insulare pupae were randomly collected from insecticide-free Brassica napus
(canola) field at Michigan State University Research Farm in late May, each year. This is
because, B. napus was planted as both early and late season crop while the other Brassica
crops were planted late in the season. Pupae were brought back to laboratory for rearing.

Diamondback moth rearing

Oviposition cages were made of clear plastic tubes cut from 2 liter drink bottles (15
cm long x 12 cm diameter) and the cup. Screen lid (3 cm diameter) was constructed on each
side of the plastic for ventilation. One end of the tubes was capped with a plastic plug, with
three quarters of the plug cut out and the opening covered with an organdy cloth. The other
end was attached to cup (with lid) by masking tape. Two holes (1.5 cm diam) on the lid
were made and one half from the bottom of the cup was cut out prior to attachment of the

plastic tube.

A 3m;
soaked in it a
cup of the tag
towel prm’idt
The food and

Aft-pr:
Oviposition t
(LID). A sin
substrate. Tl
depressions,
were erttshet
oviposition,
0r kal M St

D. insul.
A St
Cauliflower
Cauliflower
diamondhm
Placed insic
insular? pu
l’Llulare 8d
dental Wick
d [0 facilim
dlan’tttndha
“Mme“,
0f f“male I

pamlloid l

15

A small glass vial filled with diluted honey (10%) with portion of tissue paper
soaked in it, and paper towel were inserted through either hole of the cut cup lid. The cut
cup of the cage was put in other three quater water filled cup. Water absorbed by a paper
towel provided water and honey served as food source for the diamondback moth adults.
The food and water were changed every day.

Approximately 100 diamondback moth pupae were placed in one oviposition cage.
Oviposition cages were kept at room temperature (22 3: 30C) and a photo period of 16:8
(LzD). A single aluminum foil strip, 2.5 cm x 7.5 cm. was provided as an oviposition
substrate. The foil strip will be crumpled to create suitable ovipositional ridges and
depressions, then smoothed to a flat surface. The fresh leaves of broccoli or cauliflower
were crushed using hammer and then rubbed over the surface of the foil to increase the
oviposition. Eggs were collected from the oviposition cages and used to start a new colony
or kept at 5°C for future rearing.

D. insulare rearing

A 500 ml plastic container nearly filled with water was used to hold the middle age
cauliflower leaves. Holes were made in the cup cover and stems of four to six middles-aged
cauliflower leaves were inserted into cup through the hole. The leaves were inoculated with
diamondback moth third and early fourth instars. The cup and inoculated leaves were
placed inside a 50 x 40 x 40 cm ovipositional cage (22 i 30C, 16L:8D photo period). D.
insulare pupae (ca. 100 per cages) were placed inside the cage for adult emergence. D.
insulare adults were fed with honey+water (10% honey) solution distributed on cotton
dental wicks. The emerged males and females were kept in a cage without host larvae for 2
d to facilitate mating which is less frequent in the laboratory than in the field. Parasitized
diamondback moth were collected about 24 h later and transferred to a plastic pan for
experimental use or reared as above until pupation, for future rearing. To get high numbers
of female I used only diamondback moth early fourth instars as hosts and kept both sexes of

parasitoid together more than 4 d before used for parasitism.

CHAPTER

(Cresson

l

CHAPTER 1

Wildflowers as Nectar Sources for Diadegma insulare
(Cresson)(Hymenoptera: Ichneumonidae), a Parasitoid of Diamondback
Moth, Plutella xylostella (L.)(Lepidoptera: Plutellidae)

l6

17

ABSTRACT

The effects of wildflowers 0n the longevity and fecundity of Diadegma insulare
(Cresson), one of the major parasitoid of diamondback moth in North America, Plutella
xylostella L., were studied in the field. Wildflowers provided nectar sources for D.
insulare. Longevity and fecundity of the parasitoid female varied with wildflower species
and the morphological characteristics of the flower. Several flowers, including Brassica
kaber (D.C.) Wheeler, Barbarea vulgaris R. Br., and Daucus carota L., supplied nectar and
resulted in D. insulare longevity and fecundity equal to when honey+water was supplied as
food. Others, including Elysimum cher'ramhoides L. and Thlaspi arvense 11..., were not
significantly better than no food at all. Chenopodium. album L. and Sonchus arvensis L.
did not provide available nectar, however, adult parasitoids fed on honeydew excreted by
Aphisfabae (Scopli) feeding on the plants. Fecundity of D. insulare generally peaked 6 to
15 d after adult emergence. An increase in longevity and fecundity was correlated with
flower corolla opening diameter but not with corolla length. Except on B. vulgaris,
longevity and fecundity of D. insulare fed on flowers brought into the greenhouse versus in
the field were not significantly different. Shading also increased longevity and fecundity of
D. insulare. The oviposition behavior within the first minute of exposure to diamondback
moth larvae was highly conelated with longevity and total fecundity of D. insulare, which
we considered indices of food quality. Seasonal manipulation of the diversity and
distribution of wildflowers in the cabbage field and adjacent habitats, as well as providing
shade for D. insulare, could increase D. insulare effectiveness in management of

diamondback moth.

Diurlr‘gr
diamondback n
l956t Success
management h;
Sastrodiharjo l
thought to inllu
treated and um
insulare parasi'
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rePOTIed by Va
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Cowgl“ et al. (
insulare may b

m

18

INTRODUCTION

Diadegma spp. (Hymenoptera: Ichneumonidae) are major mortality factors of the
diamondback moth, Flute/la xylosrella L. (Lepidoptera: Plutellidae)(Ooi 1992, Harcourt
1986). Success in using Diadegma semiclausum (Hellen) in integrated diamondback moth
management has been reported in Malaysia and Indonesia (Ooi 1992, Sastrosiswojo &
Sastrodiharjo 1986). In Michigan, the presence of wildflowers surrounding the field was
thought to influence the DBM parasitism rate by Diadegma insulare (Cresson) in pesticide
treated and untreated plots (Idris & Grafius 1993b). Zhao et al. (1992) found that D.
insulare parasitism of diamondback moth was higher in the brassicas crops fields adjacent
to nectar-producing plants than in the fields that were not surrounded by nectar-producing
plants. In England. Diadegma sp.was observed feeding on the flowers of weeds (Filton &
Walker 1992). The importance of wildflowers as food sources for adult parasitoids was
reported by Van Emden (1963a & b, 1965a & b), Wolcott (1942), Leius (1967), Keven
(1973) and Kopvillem (1960). Syme (1975) reported that the fecundity of Hyssopus
thymus Girault (Hymenoptera: Eulophidae) females fed on various flowers was
comparable to that of honey-fed females in most cases, and in some cases was significantly
greater. The selective use of floral resources by the parasitoid, Episyrphus balteatus
(Degeer)(Diptera: Syrphidae), on farmland in the United Kingdom was reported by
Cowgill et al. (1993). An understanding of the relative importance of wildflowers to D.
insulare may be important if we want to enhance its role and effectiveness in diamondback

moth management.

longe
insult.
phnu
orho
long:

long:

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(mt t
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3V3

19
The objectives of this study were: (1) to assess the effects of wildflowers on the
longevity and fecundity of D. insulare, (2) to compare the longevity and fecundity of D.
insulare fed on greehouse versus outdoor wildflowers or fed of plants+aphids versus
plants-aphids, (3) to determine oviposition behavior of D. insulare fed on different flowers
or honey+water, (4) to assess the effects of shading versus full exposure to sunlight on the
longevity and fecundity of D. insulare, and (5) to correlate flower structure with D. insulure

longevity and fecundity

MATERIALS AND METHODS

Food sources. Flowers of eight Brassicaceous weeds, five non-Brassicaceae (2,
Asteraceae; one for Polygonaceae, Chenopodiaceae and Umbelliferae, respectively), and
onecultivated Brassica crop (canola, Brassica napus L.) were used as the nectar sources
for the parasitoid (Table l). Brassicaceous weeds were emphasized because they are
common in and near Brassica crops fields. They are also potential hosts for diamondback
moth larvae and are tolerant to many herbicides used in brassicas crops.

Sources of insects. I used F13-20 of diamondback moth (Geneva strain) donated by
Anthony Shelton, Cornell University in January, 1990. Diamondback moth were reared in
the laboratory by feeding the larvae with live plants (broccoli leaves grown in the
greenhouse)(see also general materials and methods). I used 132-3 field collected D.
insulare which were reared in the laboratory out of the above diamondback moth strain.

Site of study. This study was conducted at the Michigan State University Research
Farm during May, June, July, August and September 1993, using wildflower species

available during each period.

Long
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20

Longevity and fecundity. I enclosed the flowers and D. insulare. in a cylindrical

screen cage (20 cm high & 10 cm diam) with circular Styrofoam board covering the top and

bottom of the cage, and one small slit at the side of the screen for introducing insects. I cut

a 5 cm slit from the edge to the center of the bottom foam for the flowers stem. Each cage

Table 1. Species, common names, and families of wildflowers used for the study

 

Species

Common name' Family

 

Barbarea vulgaris R. Br.

Berteroa incana (L.) DC.

Brassica kaber (D.C) Wheeler
Brassica napus L.

Capsella bursa-pastaris (L.) Medic
Erysr'mum cher'ranthor'des L.
Lepidium campestre (L.) R. Br.
Thlaspi arvense L.

Chrysanthemum leucamhemum L.

Sonchus arvensis L.
Rumex crispus L.
Chenopodium album L.

Daucus carota L.

yellow rocket Brassicaceae
hoary alyssum "
wild mustard
canola
shepherd's purse
wormseed mustard "
field pepperweed
field pennycress "
oxeye daisy Asteraceae

perennial sowthistle "

curly dock Polygonaceae
common lambsquarters Chenopodiaceae
wild carrot Umbelliferae

 

was tied on to a wooden stake erected close to individual flowering weeds (four spikes or

two umbles per cages). I moved the cage to a new flower when the flower began to wilt

(usually every 3 to 5 d) and the honey+water treatment was changed every 4 days. Each

treatment (= flower species) was replicated eight times.

cag

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21

One male-female pair of D. insulare (1 (1 old and not yet fed) was released into the
cage using an aspirator inserted through a slit on the side of the screen. The opening was
plugged with a cotton wick. To make sure a female was mated the male was kept in the
cage for 3 d.

For control treatments, we put glass vials (21 x 70 mm) filled with honey+water
(10% honey, v/v) in place of the flower, water alone or no food or water. I rolled a piece
of tissue paper which was dipped into the vial of honey+water or water. The top of the vial
was covered by the paper to avoid excessive evaporation. The vial was inserted through a
hole in the bottom foam.

Four wild Brassicaceae (B. vulgaris, T. arvense and E. cheiranthoides) and one
Umbelliferae (Daucus carota L.) were brought into the greenhouse and transplanted them in
pots for comparisons study with other food sources in the field in May and August The
testjon these nectar-producing plants were conducted using the cage and insects and at the
same time as before.

In September, many of Chenopodium album L. and Sonchus arvensis L. were
naturally infested by aphids, Aphisfabae (Scopli). For this study I inserted two branches
of the plants+aphids or plants-aphids in place of the flower into the cage as before. Other
treatments used for comparisons were water, no food or water and honey+water.

Daucus carota, which grows near the edge of forest (sides that protect the flowers
from intense sun light in the afternoon were selected) was used in this study. Flower and
insect were put in cage as before. Like in the greenhouse study, I used data of D. carota
that exposed fully to sun light (unshaded) and other food sources in the above study for a
comparison in July and August (the hottest moths in the summer).

I had only four replicates for B. kaber, B. incana and D. carota in June and
September studies. These weeds were less abundant in early and end of the season but
they were the only weeds that present throughout summer. This allows me to study the

seasonal effect of food sources to the D. insulare longevity and fecundity. The

 

crper

ll't‘llll

Ton

l'ttll

ins.

22

experimental set up was similar as before and honey+water was used as the control
treatment.

Survival of the D. insulare females was recorded daily to measure the longevity.
To measure fecundity I took the adult female parasitoid from the cage every 3 d and
released it into a 400 ml transparent plastic container with a screen lid with 30 third instar
diamondback moth larvae for 3 h before putting it back into the cage. My previous field
experience indicated that no more than 25-27 third diamondback moth would be attacked
and superparasitism would not occur (unpublished data). The presumably parasitized
diamondback moth larvae were reared in the laboratory at 25 i 2°C, 50-70% relative
humidity and a photoperiod of 16: 8 (LzD) h until pupation, when the number of D.
insulare and diamondback moth pupae were recorded. I did not dissect the parasitized host
larvae for D. insulare eggs for fecundity measurement because there were no eggs
encapsulated (Bolter & Laing 1983). In addition, dissecting host larvae for parasitoid egg
was a laborious work and time consuming. Fecundity was calculated as the sum of all D.
insulare pupae produced by a female D. insulare during her life (30 host larvae offered
every 3 d).

Oviposition behavior. _On day 9, in the August study, I also randomly selected four
of the eight replicates for D. carora, B. kaber, B. incana and honey+water treatment from
the above study (= 4 replicate per food sources) and recorded oviposition behavior (any
attack on host made by the parasitoid that ended with inserting its ovipositor into host
body) of D. insulare females, fed on these food sources, within 1 min, 5 min and 20 min
of exposure to diamondback moth larvae. The observation was made from 1100 to 1450 h
during when the females are active (unpublished data). Because of day-time constraint to
monitor observation behavior I conducted separate observation (also in August) for D.
insulare fed on B. napus. C. bursa-pastoris, Tarvense and honey+water. B. napus, C.
bursa—pastoris, and Tarvense were not used in the above study (longevity and fecundity)

because of difficulty in getting eight replicates for the whole period of study in August.

 

ttt

fe

CE

23
Result from honey+water treatment (control) was used to determine if the treatments of the
two observations are comparable and analyzed together.

- Relationship between flower structure with D. insulare longevity and
fecundity. The corolla length and diameter of the Opening for a sample of 10 flowers for
each species per replicate were measured. Measurements were made from 1100 to 1300 h
when flower corolla were fully open. I used the longevity and fecundity data from the
above study to relate it with the corolla length and diameter of the opening.

Longevity and fecundity of D. insulare, ovipositional behavior of D. insulare fed on
different food sources, and the corolla length and opening diameter of flowers were
analyzed using l-way ANOVA, while means were separated using Fisher's Protected LSD
test (Abacus Concepts, SuperAnova 1991). The oviposition behavior of D. insulare
females fed honey+water in two observation was analyzed by paired student t - test
(MSTAT, Eisensmith & Russell 1989). Longevity and fecundity of D. insulare fed on
flowers Species tested in the greenhouse versus in the field, shaded versus unshaded and
plants+aphids or plants-aphids treatments were analyzed together with the other treatments
(= food sources). Relationships between longevity and fecundity and the length and
Opening diameter of flower corolla, the opening and length of the corolla, and ovipositional
behavior of D. insulare within 1 min of exposure to host larvae were analyzed using

regression analysis (Abacus Concepts, SuperAnova 1991).
RESULTS AND DISCUSSION

Longevity. In May, longevity of D. insulare females was significantly affected by
food source or flower species (F = 93.6; (if = 11,77; P < 0.05). For instance, D. insulare
longevity was significantly higher when fed on B. vulgaris than on the other wildflowers,
or water or without food (Fisher's Protected LSD, P < 0.05)(Fig. 1 A). In June,

parasitoid longevity was also significantly higher when fed with B. vulgaris than with the

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24

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insulare females fed on
into the greenhouse for study. Columns with different

ficantly different (Fisher's I’LSD, P < 0.05).

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25
other wildflowers, including Rumex crispus L. and Chrysanthemum leucanthemum L.
(Fisher's PLSD, P < 0.05)(Fig. l B). However, longevity of D. insulare on B. vulgaris
in June was significantly shorter than on honey+water. In July D. carata and B. kaber had
similar impacts on the longevity of D. insulare, comparable to honey+water (Fisher's
PLSD, P > 0.05)(Fig. 1 C). Although D. insulare longevity on B. incana was shorter than
on B. kaber it supported D. insulare better than C. album and S. arvensis In August,
longevity of D. insulare was higher when fed on B. kaber than on the other flowers or on
the honey+water (Fisher's PLSD, P < 0.05)(Fig. l D).

In September, C. album and S. anrensis, offered additional food sources for D.
insulare because they were harboring bean aphids, Aphisfabae (Scopli), which apparently
provided honeydew for D. insulare (aphids were not present on these plants in June, July
or August). This was clearly indicated by my September results where D. insulare lived
longer on C. album and S. arvensis+aphids than on these plants-aphids (Fisher's PLSD, P
< 0.05)( Fig. l E). Longevity of Pholetesor ornigis (Weed) (Hymenoptera: Braconidae)
adults also increased when they were provided with aphid honeydew (Hagley & Barber
1992). However, longevity of D. insulare fed on these two weeds+aphids was
significantly less than with honey+water. Honeydew from A. fabea, the apparent food
source, may not have certain sugars or essential amino acids or they may be present in
insufficient quantity compared to floral nectar (Baker & Baker 1983, Baker et al. 1978,
Saleh & Salama 1971, Lamb 1959).

There was an increase in longevity of D. insulare from early to mid season when B.
kaber and B. incana were used as food sources but not with D. carota or honey+water
(Fig. 2). From August to September D. insulare longevity was reduced when fed on B.
incana or D. carota flower nectar but not on B. kaber. This could be due to a change in
food quantity or quality (sugar'and amino acid content) of the flowers' nectar. However,
values can not be compared statistically because they were different experiments, including

possible differences in temperature, humidity and solar radiation. Lingren & Lukefahr

26
(1977) reported that for Campaletis sonorensis (Cameron)(Hymenoptera: Ichneumonidae),
a parasitoid of tobacco budworm, Heliothis virescens (F.), longevity is affected by the
quantity of extrafloral nectar produced by the cotton plant, which declines in the late
season. These weeds emerge early in the season; flowering start in June, peak in July and
August, decline in September but continues until frost (Buchholtz et al. 1981). There is no

study on the temporal population trends of D. insulare in the field but its parasitism rate is

also peak in July and August (Harcourt 1986).

 

25 1
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20 W """" B. kaber

 

 

 

 

 

 

 

 

 

 

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75.75 l

as 10.

be

'3 5

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‘°=° 0

June July August September

Figure 2. Longevity of D. insulare females fed on various
wildflowers during June through September 1993

Fecundity. Total fecundity of D. insulare in May and June was significantly higher
when B. vulgaris flowers or honey+water was used as food, compared with other foods
offered (Fisher's PLSD, P < 0.05)(Fig. 3 A). In May and June, total fecundity of D.

insulare fed on B. vulgaris was significantly lower than when it fed on honey+water

(Fisher's PLSD. P < 0.05)(Fig. 3 A & B).

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or.
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ficantly different (Fisher's

rgnr

Total fecundity per lifetime of D.

Figure 3.
females fed on various wildflowers as nectar sources.

th different letters are 5

PLSD, P< 0.05).

(G.H) indicates the results from experiment conducted on
wr

plants brought into the greenhouse for study.

28

In July, parasitoid feeding on B. kaber, D. carota or honey+water resulted in
higher fecundity than on other food sources (Fisher's PLSD, P < 0.05)(Fig. 3 C).
Although B. incana was not as beneficial for D. insulare fecundity as B: kaber, it still
offered better food than the non-brassicas wildflowers, S. arvensr's and C. album.

In August, total fecundity of D. insulare was significantly higher when fed on B.
kaber than on the other flowers or honey+water (Fisher's PLSD, P < 0.05)(Fig. 3 D).
Interestingly, longevity and total fecundity of D. insulare fed on B. kaber were significantly
higher than when fed with honey+water in August (Fig. 2 & 3 D). This suggests that B.
kaber is a better food for D. insulare than honey+water.
Fecundity of D. insulare fed on C. album or S. arvensis+aphids was significantly higher
than these weeds-aphids (Fisher's PLSD, P < 0.05)(Fig. 3 E). However, this fecundity
was very much lower than with honey+water.

In each month, total fecundity was zero when only water or no food was given to
D. insulare (Fig. 3 A - E). However, in laboratory observations after 6 to 10 h of
exposure to host larvae. unfed 1 (1 old D. insulare females did parasitize diamondback moth
larvae (unpublished data). D. insular-e without food or water, exposed to host larvae for 2
to 3 d before they died, parasitized at least 9 to 18 diamondback moth larvae, respectively
(unpublished data). This suggests that D. insulare is a pro-ovigenic insect; food is not
necessary for D. insulare egg maturation (as in mosquitoes) or for successful parasitism
(Jervis l993). Food, however, is necessary for D. insulare to live longer which indirectly
increases fecundity. In addition, energy acquired from food helped the D. insulare, within
a given time, to parasitizes more host larvae than if it was not given food at all or just
water.

D. insulare fecundity tended to gradually increase from early to mid season when
B. kaber or D. carom was used as food sources but not with B incana (Fig. 4). However,

given the size of standard errors, increase may not be significant.

 

l0

ht

29
Fecundity patterns over the life of individual D. insulare were generally similar if
food was sufficient to prevent early death. B. vulgaris in June; B. kaber, D. carota or
honey+water in August; or C. album + aphids in September are shown as examples (Fig.
5). Fecundity was low on day 3 and peaked from day 6 to 15. On C. album+aphids (a
moderately good food source), fecundity peaked on day 6 and declined thereafter.
Inexperience or physiological development of D. insulare females may account for lower

fecundity on day 3.

  

‘2'

+ B. incana

-------o B. kaber

' " o- ' D. carom
+ honey + water

  
    
 

H
U!
6

    
    

female (:tSE.)
é

(ll
9

Total fecundity per D. insulare

9

June July August September

Figure 4. Total fecundity of D. insulare females fed with various
wildflowers during June through September 1993

Longevity of D. insulare females was significantly shorter when fed on the B.
vulgaris and D. carota flowers in the greenhouse than in the field (Fisher's PLSD, P <
0.05)(Fig. 1 A & D). However, this was not true when E. cheiranthoides, T. arvense and
honey+water were used as food sources for the parasitoid (Fig. 1 A). Unlike longevity,

fecundity of D. insulare fed on B. vulgaris and D. carota flowers in the greenhouse was not

 

signifiea
(Fisher's

S
(Fig. l(
and Aug

t‘ttrr‘tlu I

30
significantly different from fecundity of parasitoid fed on these flowers in the field
(Fisher's PLSD. P > 0.05)(Fig. 3 A & D).
Shading significantly increased longevity of D. insulare fed on D. carota in July
(Fig. l C) and in August (Fig. 1 D). Like longevity, total fecundity of D. insulare in July
and August were significantly higher when fed on the shaded than on the unshaded D.

carom and several other food sources (Fisher's PLSD, P < 0.05)(Fig. 3 C & D).

 

 

' B. vrrlgaris

B. kaber

D. carom

C. album + aphid

' honey + water

 

 

 

 

 

 

 

 

 

 

 

 

.0-...-,.,. ,
036912151821242730

Age (days) of D. insulare

Fecundity of D. insulare female (iS.E.)

Figure 5. Fecundity pattern (beginning on day 3 after emergence
from pupae) of D. insulare females fed on various wildflowers as
nectar sources.

Oviposition behavior. The frequency of oviposition made by D. insulare fed
honey+water in two separate observations was not significantly different (paired t - test. (if
= 3, P > 0.05). Therefore, the treatments from the two observations were comparable.

The frequency of ovipositional behavior made by D. insulare, within 1 min of exposure to

 

the I
will

we

the

31
the larvae, was higher when they were fed on D. carota, B. kaber or honey+water than
when fed on other food sources (Fig. 6). Longevity and fecundity of D. insulare, which
we consider as indices of food quality, were strongly correlated with thefrequency of
individual parasitoids initiating oviposition behavior within the first minute of exposure to

the host (r = 0.91 and 0.87, Fig. 7 A & B).

 

 

 

 

 

 

 

 

    

 

 

 

 

 

 

 

 

 

 

 

 

 

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Food sources

Figure 6. Frequency of oviposition behavior made by

D. insulare females, fed on various wildflowers or honey+water,
during the first 20 min of exposure to diamondback larvae.
Columns with different letters are significantly different (Fisher's
Protected LSD,P < 0.05).

32

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   
 
 

 

 

 

 

 

 

 

 

20
r (A)
honey+water
16 ‘1
‘ D. carota
12 $’ B. kaber
B. uapus
1 . o
_ ........ C. bursa-pastorrs .
E 8
g T; ”"9"“ /Bi.ncana = 0.81X - 1.24, r = 0.91
g 4 ' ' - = 255.67, n = 56, P = 0.001
Q. ll 1 l l 1
v 0
3 a 0 5 10 15 20 25
= o
:3 T4 Longevity (days) of D. insulare females
8 8
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3 E
c... 6—
° 20
>~o
g . (B)
Sr 16 .
L“ .C. bursa-pastorrs D. carota
\
12 B. napus B. kaber -
. \ I honey+water
8 I
‘ / .
4 . B. incaua IY = 4.72 + 0.06X; r =0.87;
< T. arvense F = 14.83; n = 56;"P = 0.01
0 l l l l
0 40 80 120 160 200

Total fecundity of D. insulare females

Figure 7. The relationship between longevity (A) or
fecundity (B) and the frequency of ovipositional behavior
made by D. insulare females within the first minute of
exposure to host larvae.

ullll<plllll

33
Relationship of flower characters to D. insulare longevity and fecundity.
Corolla lengths and Opening diameters were significantly different among flower species (F
= 38.2; (if = 8, 56; P = 0.0001 and F = 46.2; df = 8, 56; P = 0.0001 for the corolla lengths
and opening diameters. respectively). The corolla lengths of B. vulgaris, B. napus and B.
kaber were significantly longer than corolla lengths of the other flowers, especially D.

carom (Fisher's PLSD. P < 0.05) (Table 2). In contrast. the corolla opening of D. carom

Table 2. Corolla length and Opening diameter of wildflowers

 

 

Species Corolla length Corolla opening width
(mm 1- S.E) (mm i S.E)
Daucus carota L. 0.53 i 0.02a 6.02 i 0.3lh
Brassica kaber (D.C) Wheeler 4.31 i 0.13d 5.50 i- 0.20g
Brassica napus L. 4.81 i 0.09d 3.83 i 0.03f
Barbarea vulgaris R Br. 4.44 i- 0] Id 2.80 i 0.03e
Berteroa incana (L.) DC. 2.48 i 0.50c 2.06 i 0.03d
Capsella bursa-pastoris (L.) Medic 2.46 i 0.03bc 1.67 i 0.03e
Thiaspi arvense L. 1.71 i 0.08b 1.20 i 0.02b
Erysimum cheiramhoides L. 2.62 i 0.03e 1.00 i 0.20b
Lepidium campestre (L.) R. Br. 1.55 i 0.04b 0.52 i 0.02a

 

In column means with the same letter are not significantly different (Fisher's Protected
LSD, P > 0.05).

was significantly wider than those of the other flowers; L campestre had the narrowest
corolla opening (Fisher's PLSD, P < 0.05)(T able 2). Regression analysis indicated that
14.4% (F = 11.75, P = 0.001) and 59.5% (F = 102.82. P = 0.001) of variation in the
longevity of D. insulare could be explained by the corolla length and opening diameter.
respectively (Fig. 8 A & B). There was a significant positive correlation between D.

insulare longevity and corolla length even though a negative correlation was expected, if a

34

 

 

 

 

 

 

 

 

 

 

 

 

 

     
  

 

 

     

 

30 ~
Y=5.67+1.48X,r=0.38 . (A)
. F=ll.75,n=72,P=0.001
m B. kaber h
"5 2° 3'11 -
. ans
El §D. carota B. incana 8
'Es‘ - //‘,
E 10 "/ѤӤ7 . B 9
‘93 T. arvense C. bursa pastons . napus
a.) L campestre Q o E. clzeiranthoides
S 0 a . . .
§ 0 1 2 3 4
"f Corolla length (mm)
Q
(4.4
O 30 _ k
70‘ Y = 4.05 + 2.17x. r = 0.77, B kaber (B )
g? F: 102.82, n = 72, P = 0.001 -
'U l B. vulgaris ¥
V 20
>~.
H
‘g B. incana §
(D D. carota
g) 10 +11 campestre B. napus
O C. bursa pastoris
r—l T. arvense

   
 

 

 

 

E. cheiranthoides

I I I I

0 1 2 3 4 5 6

Corolla opening (mm)

Figure 8. Longevity of D. insulare females in relation
to corolla length (A) and opening (B) of wildflowers.

 

35
narrow corolla limited access to nectar by D. insulare (Fig. 8 A & B). This positive
correlation is probably due tO the high conelation between length and opening
except for D. carota (r = 0.79; F = 108.98; df = 1, 62; n = 72; P = 0.001) rather than any
factor resulting in increased longevity with longer corollas. For D. carota the corolla
Opening is large enough that length did not influence longevity. B. kaber petals are
separated down to the base Of the corolla providing easy access of the parasitoid tO the
nectaries. in spite Of its length.

There was no significant relationship between the corolla'length and the fecundity
Of D. insulare (r = 0.37, F = 1.09. P = 0.33)(Fig. 9 A). However, corolla Opening
explained 75% Of the variation in D. insulare fecundity (r = 0.87, F = 21.01. P = 0.003.
Fig. 9 B).

Subsequent to these studies I looked at the effect of Scrophularia nodosa L.
(Scrophulariaceae) on the longevity and fecundity Of D. insulare following similar
procedure as above. It has a very wide corolla and is known to produce high amounts Of
nectar (Ayers et al. 1987). D. insulare fed on S. nodosa lived 25.3 i 2.5 d (n = 10) and
parasitized 170.3 i 18.5 diamondback moth larvae (unpublished data). These were
somewhat similar when the parasitoid were fed on B. kaber, the better fOOd sources for D.
insulare in my study.

There are also other factors affecting access to nectar besides corolla length and
Opening. The separation Of the sepals and petals in B. kaber flowers exposes the basal part
Of the flower where nectar is located even for newly Opened flowers. Thickness Of the
petals and sepals at the base Of the corolla and sepals attached at the base, covering the
bottom half Of the corolla may also be important. I Observed D. insulare apparently
chewing or sucking at the base Of B. vulgaris and B. napus flowers to get nectar. In some

cases, a hole in the base Of a petal was visible after D. insulare chewing.

36

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

200 v = 26.08 + 14.13x, r= 0.37, (A)

‘ _ F=1.09,n=72,p=0.33 B. kaber }
m 150 1
{/5 i D. carota B. vulgan's i
+| 100
2 B. incana
g i B. napus
,3 50 / i C. bursa pastoris

. T. meme
3 L cam stre ‘3‘ E. cbeiranthoides
VS 0 pet I 4 I ' '
a 0 1 2 3 4 5
«’3 Corolla length (mm)
Q
“5 200
g» [ Y: 24.-76x 3.,01r= 0.,87 (B)
,H ‘ F: 21.,01 n: 72,p= 0.003 13: kaber
6
g 150
8 ‘ B. vulgaris /{
‘4—4
73 100 B . D. carota
H Q .mcaaa 1
a 50 Llcampestre ;B. napus

‘L/fil bursa-paston's
0 w Echeiranthoides
0 1 2 3 4 5 6

Corolla opening (mm)

Figure 9. The relationship Of fecundity Of D. insulare
females to the corolla length (A) and opening (B) Of
wildflowers.

37
In the field and the laboratory, 1 also Observed squeezing or kicking behavior Of D.
insulare on the petals or sepals Of C. bursa-pastoris and T. arvense flowers (narrow and
short corollas with soft thin petals and sepals). D. insulare appeared to be trying to reach
the nectar at the base Of the corolla. I did not Observe this behavior on D. carota flowers

perhaps because they are wider and have shorter corollas.
C O N CL US [ON S

Overall, results Of my study indicate that D. insulare longevity and fecundity are
dependent on the availability and accessibility Of food (nectar) sources in and around the
field. The accessibility Of the nectar correlates with flower characters. Although the width
Of the corolla Opening has a strong effect on both longevity and fecundity. it did not explain
all the Observed variation between wildflower species as food sources. Nectar quality and
extrafloral nectar are probably important (Baker & Baker 1983) but I did not measure it. C.
album and S. arvensis which did not have accessible nectar could indirectly provide food
sources by harboring aphids which produce honeydew for the parasitoid.

Although D. insulare also used flowers Of non-brassicas weeds. D. insulare may
have coevolved with the diamondback moth to associate with the Brassicaceae weeds.
However, Herrera (1993) found that evolution for adapting to Other ecological factors are
far more important determinants Of fitness (longevity and fecundity) Of the hawk moth.
Macroglossum stellatarum L. (Lemdoptera: Sphingidae), than selection of floral
morphology or phenotype. It is also possible that certain Brassica species like B. kaber
may have evolved to have floral structures that attract D. insulare or Other parasitoids.
Flowers with accessible nectar might help increase parasitism Of diamondback moth. In
Michigan, B. kaber, which supported the highest longevity and fecundity Of D. insulare, is

most commonly infested by diamondback moth, 80—90% Of which are parasitized

38
(unpublished data). Further study needs to be done on the parasitism rate Of diamondback
moth by D. insulare when these plants are used as fOOd sources.

B. vulgaris, and B. kaber and D. carom, which are abundant in weedy areas and
idle field in Michigan during early and middle tO late season, respectively. could influence
effectiveness Of D. insulare as a biocontrol agent Of diamondback moth. The distribution
of these weeds could be manipulated in brassicas cropping systems tO favor D. insular-e.
In addition. providing refuge (shading) for D. insulare is important for enhancing the
effectiveness and role Of this parasitoid in integrated diamondback moth management.
Other nectar-producing plants may be even more suitable, providing more or better quality
nectar or nectar over a longer period Of time (e.g., Pycnanthemem pilosum Nutt. and
Scrophularia nodosa L.. Ayers et al. 1987). Design Of crop management systems
including management Of natural enemy fOOd sources will become more important as we

try to integrate biological control with production Of high value vegetable crops.

CHAPTER 2

Nectar-collecting Behavior of Diadegma insulare (Cresson)(Hymennoptera:
Ichneumonidae), a Parasitoid of Diamondback Moth, Plutella xylostella
(L.)(Lepidoptera: Plutellidae)

39

40

ABSTRACT

I Observed nine nectar-collecting behaviors of Diadegma insulare (Cresson), a
major parasitoid of diamondback moth, Plutella xylostella (L.). The most striking
behavior, on Barbarea vulgaris R. Br. and Brassica napus L. flowers, involved chewing at
the base of the corolla and creating holes that probably released the floral nectar. D.
insulare apparently is not a pollen feeder as the anthers of flowers were never approached.
D. insulare visited more frequently and spent longer times on flower species supporting
longer life and fecundity (B. vulgaris, Brassica kaber (D.C) Wheeler. B. napus and Daucus
carota L. Times spent per visit number to each flower specis were significantly affected by
flower species and were significantly influenced by visit numbers by flower species
interaction. The times spent by D. insulare on the more rewarding species, B. kaber and
B. vulgaris increased with numbers of visits but declined between the fifth and sixth visits.
This pattern was not true for poor nectar sources. Berteroa incana L. (DC) and
Elysimumcheiranthoides L. This suggests that D. insulare, after experience, was able tO
positively correlate nectar rewards with the flower characters. Flower color was not a
factor influencing parasitoid choice to visit flowers. D. insulare spent significantly longer
time at the upper one third Of D. carom corolla and at the lower one third Of B. kaber and B.
vulgaris corollas than other flowers. Behavioral flexibility Of D. insulare to flower
characters and its nectar-collecting behaviors should be manipulated for increased impact Of

this parasitoid in diamondback moth control program.

41

INTRODUCTION

Diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), is the major
pest of Brassicaceae crops worldwide. Pesticide resistance problems have forced growers
to increase the frequency and rate of sprays. This leads to excessive use of pesticides that
destroys the pest's natural biocontrol agents in Brassica crop agroecosystems (Lim et al.
1986).

The abundance of Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae) in
the field and its role as major diamondback moth parasitoid was reported by Harcourt
(1986). Pesticides continue to be the major means for controlling pests, but these are
detrimental to D. insulare (Lingren et al. 1972,1dris & Grafius 1993a & b). However,
judicious use of pesticides with good Brassica crop agroecosystem management could
increase role of Diadegma in the field (Ooi 1992, Srinivasan & Krishna Moorthy 1991).

D. insulare live longer and are more fecund when fed on Brassica kaber (DC.)
Wheeler, Barbarea vulgaris R. Br. or Daucus carota L., wildflowers commonly found in
and around crop fields in North America (Buchholtz et al. 1981). Earlier studies indicated
that the presence Of wildflowers in the field increases the effectiveness of other parasitoids
(van Emden 1963 a & b. Leius 1967, Kopvillem 1960, Keven 1973, Syme 1975, Zhao et
al. 1992). D. insulare effectiveness could be increased by providing suitable wildflower
nectar sources in or around the fields.

Floral structures, the corolla length and opening diameter of wildflowers affect
longevity and fecundity of D. insulare. (Chapter 1). They may also influence the behavior
of D. insulare in collecting nectar (Chapter 1). Different behavior of bumble bees, Bombus

spp., on various flowers was observed more than 100 years ago by Charles Darwin

42

(Guiterman 1959). Darwin reported that individual bees made holes near to the nectaries of
long tubular flowers by biting through the corolla with their mandibles or piercing them
with their tongues. The specialist bumble bee, B. consobrinus Dhalb, is more efficient
than generalist species in acquiring flower-handling skills on their specialty plants by
probing in the vicinity of the nectary and quickly locating the nectar even without previous
experiences (Laverty & Plowright 1988).

The Objectives of my study were to (l) characterize nectar-collecting behaviors of
D. insulare on various flowers that are used as food sources, (2) quantify the number of
visits or visitors and times spend on flowers Offered to D. insulare. (3) evaluate flower
color choice, and (4) look at the possible learning ability of D. insulare to select more

rewarding flowers in maximizing their nectar-collecting effort
MATERIALS AND METHODS

Flowers used in my studies were common weed species and one Brassica crop
plant (Table l). I selected these weeds because they support a wide range in longevity and
fecundity of D. insulare adults (Chapter 1)(T able 1).

Choice tests. Stalks of three flowers of each species were inserted through holes in
the lid of a 300 ml plastic container almost filled with sucrose solution (0.5 g/ml). The
flower species were randomly arranged in a circle about 4.0 cm from the center of the
cover. A second 300 ml container, with 1.5 cm diam screened holes in the side, was put
upside down on the first container and fastened with tape, creating a testing arena. The
arena was put under white inflorescence light (Philips; FI‘2T12/CWN HG, 160Watt, 44 cm
above arenas), at 25 :l: 2°C and 50—70% relative humidity. I randomly arranged the arenas
parallel to the light.

An unfed female D. insulare (1 (1 Old) was put in a freezer for 3 min for easy

handling and released in the center of the testing arena through a hole in the upper

43

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44
container. I used cotton to plug the hole. Females were allowed to acclimate for about 2 h
in the arena before observation.

The nectar-collecting behaviors of D. insulare; the numbers of visits and time spent
per visit per flower type, the numbers of visits and time spent at the base of corollas were
recorded using an audio tape recorder for 30 min per observation session. These
observations were repeated five times with new plants and insects each time.

To evaluate possible learning ability of D. insulare I used 8. vulgaris, B. kaber, B.
incana and E. cheiramhoides flowers, testing arenas were set up‘as before (five arenas =
replications, one D. insulare and four flower species per replicate). Females were allowed
to acclimate to the testing arena as before. Times spent per visit for six visits for each D.
insulare female and flower species were recorded using an audio tape recorder.

No-Choice tests. Freshly emerged adult D. insulare females were released into
cages (30 per 30 x 30 x 20 cm screen cage. one D. insulare per cage. six cages =
neplications) 1 d before the experiment to acclimate them to the cage environment. The
cages were put under white inflorescent light as before. but the distance of the top of the
cages to the light bulb was 20 cm. No food was given to the parasitoids before the
experiment because I desired quick responses to the introduced flowers (previous
observations indicated that D. insulare can survive up to 2 d without food). Environmental
conditions were same as in the choice tests.

I inserted stalks of flowers of each species into glass vials (21 x 70 mm, 3 flowers
per vial) filled with sucrose solution (0.5 g/ml). To prevent D. insulare from reaching the
sucrose I used cotton to cover the vial mouth. D. insulare were observed feeding at this
location. Six vials with flowers of a single species were put in the middle of each cage.

Fifteen minutes after introduction of the flowers I recorded the numbers of
individual D. insulare visiting the flowers using audio tape recorder in 30 see. I then took

out the flowers with vials.

45

I introduced new flower species (randomly selected, excluding the species that just
tested) with vials in the another cage for the next observation. After the sixth cage I
returned to the first cage and repeated this process five times (= five replicates per species).
The numbers of visiting D. insulare per flower species per observation were recorded.

In choice and no—choice tests (above) D. insulare females visited and fed at the
bases of the flower corollas of some species. To quantify the visit times of D. insulare at
the upper and lower parts of corollas I used a set up similar to the choice test experiment.
However, I used one flower species per test arena. Isubdivided°the corolla into upper,
middle and lower one thirds. Treatments were replicated five times (five D. insular-e
females per flower species) with new flowers each replication.

The number of visits and time spent per visit on flowers and on upper or lower one
third of flowers per flower species, and comparisons of total visitors per 30 sec for each
flower species were analyzed using 1-way ANOVA; and means were compared using
Fisher's Protected LSD test. The time spent per visit number per flower species was
analyzed using 2-way ANOVA (Abacus Concept. Super ANOVA 1991). I used
correlation analysis to test the strength of relationships between time spent per visit with

visit numbers (Abacus Concept, Super ANOVA 1991)

RESULTS AND DISCUSSION

Choice tests. Charagterizatign of nectar-gallegting behaviors. I observed at least

nine distinct nectar-collecting behaviors of D. insulare (Table 2, Fig. l & 2). This indicates
that there is behavioral flexibility of D. insulare in collecting floral nectar. Most of these
behaviors have been reported for bumble bees (Guiterrnan 1959) but most have not been
reported for parasitoids, especially the ichneumonids (Jervis et al. 1993). Therefore, this is

the first report that an ichneumonid can behave like the bumble bee in trying to leach the

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47
floral nectar sources. However, unlike the bumblebees, D. insulare females were never
seen feeding on anthers.

D. insulare tried to get in the corolla through the corolla opening on all flower
species. However, they only entered the corolla of Berteroa incana (L.) DC., Thlaspi
arvence L, Capsella bursa-pastoris (L.) Medic and Daucus carota L. flowers (Table l).
Kicking (using both front and hind legs) the soft, separated sepal or petal, was observed on
B. incana, Etysimum cheiranthoides L., T. arvense or C. bursa-pastoris. D. insulare did
not try to enter the corolla tubes of Brassica kaber (D.C) Wheeler flowers because the
corolla base has a wide separation between the sepals or petals, and between the sepals and
petals; to reach the nectar at base of the corolla, D. insulare could easily enter from the side.
After examining the upper and lower corolla of E. cheiranthoides flower several times D.
insulare finally uied to enter corolla tube from the upper section. However, sepals and
petals of E. cheiranthoides are attached to form a corolla tube, and given the narrow corolla
opening D. insulare could not enter the tube or reach the nectar.

D. insulare easily entered the wide, shallow corolla of D. carota. D. insulare circled
the corolla bases of all other flower species offered, indicating a high affinity to get close to
the actual food source. D. insulare appeared to suck or chew at the corolla base of Brassica
vulgaris R. Br. and Brassica napus L. flowers and these were subsequently found to have
holes that probably released the floral nectar. Apparently, D. insulare used its mandibles to
make the holes to reach the nectar, as does the bumble bee (Guitennan 1959). Bentley &
Elias (1983) and Keven & Baker (1984) reported that insects with mandibulate mouthpart
often feed on discal or bowl-shaped flowers. D. insulare used these holes to suck nectar
each time they visited the corolla base although sometimes they also tried to make new
holes. This behavior appears similar regardless of D. insulare flower foraging experience.
Laverty & Plowright (1988) also reported that with no previous foraging experience.
workers of the specialist bumblebee, B. consobrinus, began probing in the vicinity of the

nectary and quickly located the nectar.

48

W. The numbers of visits
and time spent per flower per visit were significantly different among flower species (F =
36.6, 54.2; df = 7, 28; P = 0.001; n = 40)(Fig. 1 A & B). D. insulare made significantly
more visits to B. vulgaris and B. kaber than to the other flower species (Fisher's Protected
LSD, P < 0.05). They spent longer times per visit on B. napus, B. vulgaris, B. kaber and
D. carota than on the other flower species (FPLSD, Fig. 1 B). This suggests that visiting
these flowers is more rewarding or beneficial (Fig. l A & B); D. insulare generally
preferred flowers that support long life and high fecundity (Table l).

The number of visits made by D. insular? to B. vulgaris, B. napus, B. kaber, E.
cheiranthoides and D. carota were significantly higher than to T. arvense, C. bursa-
pastoris or B. incana (FPLSD, P < 0.05)(Fig. l A). The times spent per visit were also
significantly longer on the B. vulgaris, B. napus, B. kaber and D. carom than on the E.
cheiranthoides, T. arvense, C. bursa-pastoris and B. incana (FPLSD, P < 0.05)(Fig. 1 B).
There was only E. cheiranthoides flower attracted many insects but short visits.

The numbers of visits to the corolla bases were significantly higher on B. vulgaris.
B. napus and B. kaber than on the other flower species (FPLSD, P < 0.05)(Fig. 2A).
Although D. insulare visited the base of T. arvense, C. bursa—pastoris and B. incana
flowers. the numbers of visits to the bases of these flower species were not significantly
different from zero (FPLSD, P > 0.05). D. insulare did not visit the base of D. carom
corolla because its corolla tube is extremely short and widely open. The times spent per
visit at the base of corollas were significantly different among the flower species (F = 31.8;
df = 7, 28; P = 0.007; n = 40)(Fig. 2 B). Again, E. cheiranthoides attracted a moderate
numbers of visits, but visits were very short

D. insulare spent significantly shorter times per visit at the flowers and at the
corolla bases of B. kaber than at flowers of B. vulgaris or B. napus (FPLSD, P <
0.05)(Fig. l & 2 B). Probably, D. insulare takes extra time to chew and make holes at the

B. vulgaris and B. napus corolla base before sucking nectar. The intriguing question was

49

 

 

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D. insulare in 30 min in choice test experiment. Bars with different letters are

significantly different (Fisher

50

(A) Number of visits to corolla base

 

Visits per D. insulare in
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different letters are significantly different (Fisher's Protected LSD, P < 0.05).

51
why D. insulare selected B. vulgaris in the presence of B. kaber where nectar is more
easily accessable. I do not think that D. insulare was attracted to B. vulgaris more than to
B. kaber because number of visits was similar. D. insulare used in my study were hungry,
and this might prompt feeding attempts on whatever flower is first encountered in the
testing arena. If true, longer time per visit would not necessarily mean the flower is good
or prefened by the parasitoids. On the hand, E. cheiramhoides was apparently attractive
(moderate number of visits) but not desirable (short time per visit); E. cheiramhoides is a
poor nectar sources, based on longevity and fecundity (Table l).'

Elower color choice. No color preference was apparent. There was no significant
difference in the number of visits to E. cheiranthoides, B. napus (yellow) or D. carom
(white) flowers made by D. insulare (FPLSD, P > 0.05)(Fig. lA)(Table 1). However, the
number of visit to E. cheiramhoides and D. carom differed significantly from the numbers
of visits to T. atvense, C. bursa-pastoris or B. incana (all are white). However, what
appear to be white flowers to us may be reflecting some insect-attractive color at the center
of the corolla which serves as an indicator for the presence of nectar and attracting the
parasitoids (Matthew & Matthew 1978).

'0 ir'l a. rut .. iii 0 o '1. : '0 u- w. .' 9‘ r'n‘ C wi '.0,wrin
flowers. The times spent on B. vulgaris or B. kaber increased from first to fifth visits and
decreased between fifth and sixth visits, possibly indicating satiation of the parasitoid. The
times spent per visit by D. insulare to B. vulgaris and B. kaber were positively correlated
with the number of times the D. insulare individual had visited that flower (visit numbers)(r
= 0.42 & 0.38; F = 6.1 & 4.8; df = 1, 28; P < 0.05; n = 10)(Fig. 3). In contrast, the
times spent per visit by the D. insulare to B. incana and E. cheiranthoides decreased with
the visit number. The times spent by D. insulare per visit to B. incana or E. cheiranthoides
were negatively correlated with the visit numbers (r = 0.64 & 0.77; F = 20.3 & 39.8; (if =

1, 28; P < 0.05; n = 10). The time spent per visit was also significantly influenced by the

52
interaction between flower species and visit number (2—way ANOVA, F = 5.1; df = 15, 96;
P < 0.01; n = 20).

No-choice tests.

 

The numbers of visitors (2 D. insulare females) per observation were significantly different
among flower species (F = 80.9; (if = 5, 15; P = 0.001; n = 30; FPLSD)(Fig. 4). Like the
choice test (Fig. 1A), there were significantly more visitors (D. insulare females) to B.
kaber, B. vulgaris and D. carom than to the other flowers (FPLSD, P < 0.05)(Fi g. 4); there
were fewer visitors to E. cheiranthoides flowers than to any other species. In the choice
tests. E. cheiranthoides was visited often although D. insulare spent very little time on this
flower. Apparently D. insulare could not distinguish between E. cheiranthoides and other
attractive flowers, before landing. In contrast. in the no choice test, few visits were made
to E. cheiranthoides, reflecting the poor quality or quantity of its nectar (Table 1).

Numbers of visitors to C. bursa pastoris and B. incana were higher in this no choice test
than in the choice tests. Results will also be different in nature as the diversity and
abundance of wildflowers vary with habitat or landscape. In the field, like my no choice
tests, some flower types are visited more frequently or have more visitors than would be
expected, based on their respective abundance (Jervis et al. 1993).

The visit times in the upper one third of the flower's corolla were significantly
different among flower species (F = 44.3; (if = 3, 12; P = 0.001; n : 20)(Fig. 5A). D.
insulare made longer visits to the upper one third of D. carom corollas than to the upper one
third of B. vulgaris, B. kaber or E. cheiramhoides (FPLSD, P < 0.05). This is because D.
carom has a very short wide corolla tube. Longer visits were made to the lower one third
of B. vulgaris and B. kaber corollas than to the lower one third of E. cheiranthoides or D.
carom corolla (FPLSD, P < 0.05)(Fig. SB). Although the corolla tube of B. kaber is
widely open as D. carom corolla (Chapter 1), D. insulare visited longer to the lower one
third than to the upper one third of B. kaber corolla; the nectar source is readily accessible

between the separated sepals and petals.

53

 

.1:

.2 3m

> B.vngaris
him 250 - “"0" [Haber
a”) 200 . am...

E :1 150 ‘ ~~n-~ mama.
a.) 8' 100

$69 50

‘5’ 0

"E: 1 2 3 4 5 6

Visit number

Figure 3. Time spent per visit to flowers by D. insulare females at different
visit number in choice test experiment. [Visit number = first, second, third,
fourth, fifth and siXth; visit to that flower species].

 

 

 

 

 

Vrsrtors per 30 see.
i S.E.M.

'~.
{3%

 

B. vulgaris

B kaber

E. cheiranthoides
C. bursa-paston's
B. mcana

D. carota

Figure 4. Number of visitors (D. insulare females) per flower
species per 30 sec in no-choice test experiment. Bars with different
letters are significantly different (Fisher's Protected LSD, P < 0.05).

54

 

 

 

 

 

 

 

    

 

 

(A) Upper one third of corolla

300 .

250 I

200 .

rso ‘

100
2. 4
m.
m - e. a s
it E. s 33:
g i °° E e:
8.
a O
8. (B) Lower one tlurd of corolla
3 300
E 250
9“ 200

150

100

50 a
0

B. kaber

D. carota

E
3
:5

E. cheiranthoides

Figure 5. Time spent per visit at the upper (A) and lower (B) one third of
corolla made by D. insulare in no-choice test experiment. Bars with different letters
are significantly different (Fisher's Protected LSD, P < 0.05).

55
I did not measure the number of visits and time Spent on the middle one third of the
corolla of all flower species. However, I observed D. insulare used this portion only to
move from upper one third to the lower one third of all flower species.

Elgwer color choice. Results of no-choice tests showed a trend similar to the
choice tests (Fig. 1 & 4). The number of visit to D. carota was as high as to B. vulgaris.
and D. carota attracted significantly more visits than B. incana (Fig.4). Thus, color again
appeared not to be a factor affecting D. insulare behavior in flower choice (B. vulgaris and
E. cheiranthoides is yellow but D. carota, T. awense. C. bar'sa-pbstoris and B. incana are
white)(Table 1).

Jervis et al. (1993) believed that ichneumonids. being relatively large insects
compared to braconids, and mostly lacking elongated mouth parts are largely excluded
from using the nectar of (a) plants whose flowers or florets have narrow, tubular corollas.
e.g. Asteraceae and Leguminosae; and (b) plants that have relatively wide corollas. but
have their nectars well concealed. e.g. Convolaceae. They also suspected that wasps were
feeding either partly or entirely at the extra floral nectaries of the plants. However. they
failed to discuss why certain flowers like B. vulgaris or B. kaber attracted parasitoids in the
field. B. vulgaris, for example. has sepals that stick together at the corolla base. but the
sepals are thin enough to allow D. insulare to chew, making hole and sucking the nectar.

Behavioral flexibility of D. insulare in relation to flower characters and nectar-
collecting behaviors should be manipulated for better utilization of this parasitoid in an
integrated diamondback moth management program. My results suggest that B. vulgaris.
B. kaber or D. carota can be integrated in Brassica cropping systems. They can be planted
around the field or in patches or within the field. Russian researchers found that if rapid-
flowering mustards are sown with brassica crops. parasitism of cabbage white butterfly
larvae (Piert's spp.) by a braconid. Cotesia ( = Apantales) glomeratus L. increased from

10% to 60% (National Academy of Science 1969). C. glomerams is known to feed on

 

{Oi

let
“C
Br
Ga

er

or
kn
flu
in]

Ex

an.

56
nectar from mustard flowers and. like D. insulare. females live longer and lay more eggs

when these flowers are available.

CONCLUSIONS

Planting or leaving weeds around or within the vicinity of the field ecosystem may
also harbor pests. but these can provide alternate hosts for the parasitoids. In place of
weeds, we also can harvest only part of the Brassica crop. the remainder being allowed to
flower. or intersow two Brassica crops. Wild brassicas such as B. incana or C. bursa-
pastoris can be interplanted with brassicas crops. These Brassica spp. can also serve as
food sources even though they are not as good as B. kaber or other wild flowers (Chapter
1).

Results of my study may be applicable to the temperate region since flowers that 1
tested are adapted to this climate. In the tropic or sub-tropical growing regions other
flowers could better serve as nectar sources. Through a literature search and by examining
Brassicaceae from all over the world planted at Michigan State University's Beal Botanical
Garden I suggest that the Indian mustard. Brassica juncea L.(Czern), that is abundant in the
tropics, could serve as an excellent food sources. equal to B. kaber for other diamondback
moth parasitoids such as Diadegma semiclausum (Hellen)(Hymenoptera: Ichneumonidae)
or Cotesia plutellae (Kurdjumov)(l—Iymenoptera: Braconidae). Flower characters of B.
kaber and B. juncea are very similar. however. detailed studies need to be done on B.
juncea and other flower species. B. juncea is now also being used as the most effective
trap crop for diamondback moth in India (Srinivasan & Krishna Moorthy 1991 & 1992).
Evaluating seasonality of flowering to provide floral resources throughout the season
(Ayers et al. 1987) will also be important in using flowers to increase activity of D. insulare

and other parasitoids.

 

CHAI’

Drum;

IChnI

CHAPTER 3

Diurnal Foraging Activity of Diadegma insulare (Cresson)(Hymenoptera:
Ichneumonidae), a Parasitoid of the Diamondback Moth (Lepidoptera:
Plutellidae), in the Field

57

58

ABSTRACT

I studied the diurnal foraging activity of Diadegma insulare (Cresson) at the Collins
Road Entomology Research Field Michigan State University during the summer of 1992
and 1993. Foraging activity was measured using sticky traps placed within the broccoli
canopy and by direct or visual observation. Foraging activity of D. insular-e males was
positively correlated with light intensity. while female's activity was positively correlated
with light intensity. temperature and wind speed. Relative humidity, percent cloud cover
and time of day did not influence D. insulare catch. There was no significant difference
between male and female catch. The patterns of males and females foraging activity at
different times of day were significantly different from a uniform distribution except on 14
and 22 August 1993 for males and 14 August for females. Activity generally began
between 0800 and 1000 h, peaked between 1100 to 1300 h and stopped by 2100 h. There
was no significant correlation between the numbers of males and females caught on the
same trap, suggesting that an increase in numbers of females does not attract more males.
Males were caught more than females in September of both years. suggesting that males
were more abundant or more active at the end of the season. The patterns of percent of the
total day's catch of D. insulare male plus female catch at different times of the day in sticky
traps were generally not different from visual observations. The numbers of D. insulare
caught were positively conelated with the numbers of diamondback moth larvae per plant.
This information could be useful for developing a model that can predict the peak diumal
activity of D. insulare in the field which would help with decisions on whether pesticides

should be sprayed.

59

INTRODUCTION

Diadegma insulate (Cresson)(Hymenoptera: Ichneumonidae) is an important
parasitoid of the diamondback moth. Plate/la xylosrella L. (Lepidoptera: Plutellidae).
(Harcourt 1969 & 1986. Bolter & Laing 1983. Biever et al. 1992. Putnam 1968. Lasota &
Kok 1986. Idris & Gratius 1993b). This parasitoid is native to central America (Carlson
1979, Wage & Cherry 1992). However. Carlson (1979) reported that D. insulare can be
found as far as the Hawaiian Islands, and Argentina and Canada in South and North
America respectively. It parasitizes Hellula undalis (F.)(Pyralidae) and Plurella armoricae
(Busck)(Plutellidae)(Carlson 1979). but diamondback moth is its major host (Harcourt
1960 &1963). D. insulare is abundant in the field and parasitizes 50-80% of diamondback
moth larvae in the field (Harcourt 1986).

Presently. insecticide treatment decisions for diamondback moth control in brassica
crop fields are based on counts of larvae or damage to the leaves (Sastrosiswojo &~
Sastrodiharjo 1986. Palis 1983. Shelton et al. 1982. Stewart & Sear 1988). Even though
the need for conserving beneficial arthropods is commonly recognized, explicit instructions
cannot be given for sampling and using their numbers in decision making until their
behavior, population dynamics. and parasitoid-pest-host relationships are understood to a
greater degree.

Many laboratory studies of D. insulare have been conducted (Putnam 1968 &
1973. Bolter & Laing 1983. Harcourt 1963. Idris & Grafius 1993a & b). but information
on this parasitoid's foraging behavior in the field is scant. Thus. my effort was made to
learn some of this parasitoid's diurnal foraging activity and to determine if its foraging

pattern is limited by weather factors or host numbers.

60
The objectives of this study were to: (1) determine diurnal foraging activity of
D. insulare; (2) study the relationship between weather factors and D. insulare's foraging
activity; (3) determine attraction between sexes in the field; (4) compare the diurnal patterns
of parasitoids caught by the sticky traps with direct or visual observation; and (5) compare

the numbers of hosts per plant with the numbers of D. insulare caught on the sticky traps.

MATERIALS AND METHODS

This study was conducted in 1992 and 1993 at the Michigan State University Collins
Road Entomology Field. In 1992. the experimental plot contained 20 rows of broccoli
transplanted on 14-15 July, 0.6 m between plants. 1.5 m between rows. and 40 plants per
row. I used 20:20:20 transplant fertilizer and kept the plot free of weeds manually.

On 28 and 30 August 1992. ten yellow sticky traps and 10 white sticky traps
(PheroconTM 1C trap - bottoms; Trece lnc.. Salinas. California) were used to determined
which color attracted more D. insulare. Because these traps have one-sided sticky coating
material, each trap was folded in half to make a two-sided trap with sticky side out and placed
upright on a 40 cm stake in the middle portion of the canopy. Broccoli leaves were trimmed
as needed to make sure there were no broccoli leaves sticking to the traps. I found that there
was no difference in numbers of parasitoids caught by the two colors and types of the traps.
White sticky traps did not attract aphids or flies and its sticky coating material did not melt as
readily during hot weather as on yellow sticky traps. Parasitoid identification and counting
was also easier on white traps. therefore. I used white sticky traps in subsequent

observations in 1992 and 1993.

61
D. insulare diurnal foraging activity, it's relationship to weather factors,
and attraction between sexes. On 11 and 13 September 1992, we placed 20 white
sticky traps within the canopy of randomly selected broccoli plants at about 0630 h (Eastern
Daylight Savings Time. EDT). D. insulare in the traps were sexed, counted and removed at
2 h intervals from 0800 to 2200 h.

In 1993, I planted 30 rows of broccoli and used 14 rows of each side of the plot for
the study using sticky traps on one side and direct visual observation on the other, leaving
two rows in the middle as buffer. On 14, 18 and 22 August, and 5 September, I conducted
similar experiments and recorded the number of D. insulare caught at different times of the
day (1 h interval), the temperature and relative humidity (Taylor Hygrometer, UCA,
Thermometer corp., CA), sunlight intensity (Quantum Sense Meter; Li-COR, lnc.. Lincoln,
NE), wind speed (Turbo Meter; Davis Instruments, Hayward, CA) and cloud cover every
20 min from 0630 to 2200 h. Cloud cover was visually rated as sunny, partly sunny (<
50% cloud cover), partly cloudy (> 50% cloud cover). cloudy or fog.

The numbers of D. insulare males and females. and males plus females caught at
different times of the day. and the patterns of males versus females catch were analyzed
using X2 to determine if activity varied during the day (using the average of the day's catch
as expected value. actual catch as the observed). I used multiple regression analysis to
determine the relationship between D. insulare activity (trap catch) and weather factors
(Abacus Concepts. SuperAnova 1991). Correlation analysis was used to test the hypothesis
that more males were caught on traps with high counts of females (Abacus Concepts,
SuperAnova 1991). A paired student'sr —test was used to compare the total numbers of each
sex caught per day (MSTAT, Eisensmith 1989).

Diurnal patterns of D. insulare caught by sticky traps versus direct or
visual observation. Direct visual observations of D. insulare were made every hour,
while walking along rows of broccoli and capturing with a sweep net all D. insulare seen on

the same day as observations on the sticky traps (The number and turning angle of its zig-

62

zag flight pattern is less frequent and small. respectively. and this can be easily
distinguished from flight pattern of other ichneumonids or braconids that normally observed
in broccoli field) along 35 m of row. Observations of two adjacent rows were made
simultaneously for an effective sampling unit of 70 m of row at each sampling. Captured
parasitoids were identified. sexed. counted. and released. To compare the patterns of D.
insulare caught on sticky traps with visually observations 1 transformed the D. insulare catch
and observations hourly data to the percentage of the total day's catch or observation at each
sample interval. then analyzed using X2 as above.

Relationship between the numbers of hosts per plant with numbers of
D. insulare caught in the sticky traps. On 25 August 1993. I conducted an
experiment to study the relationship between the numbers of diamondback moth larvae per
plant with the number of D. insulare caught per trap. I randomly selected 3 broccoli rows
(each row = block) and eight plants (each plant = replicate) per block in the experimental
plot described above. Diamondback moth larvae from these plants were removed by hand.
I placed laboratory-reared third instar diamondback moth on these plants (0, 3 or 6 per
plant. randomly assigned within blocks) and let the larvae acclimate to the host plant for 24
h. On 26 August 1993. each plant was sampled to ensure it had the correct number of .
diamondback moth larvae as assigned and added new larvae where needed. At 1000 h I
randomly placed sticky traps next to each treatment's plant. The numbers and sex of D.
insulare caught per trap were recorded hourly from 1100 to 1700 h and D. insulare were
removed as before. The numbers of D. insulare males and females caught per treatment
were compared with diamondback moth density using regression analysis (Abacus

Concepts. SuperAnova 1991).

63
RESULTS AND DISCUSSION

D. insulare diurnal foraging activity. Females began foraging between 1000 and
1200 h on 11 September and between 0800 and 1000 h on 13 September 1992 that is 1-2 h
later than the males (Fig. l A & B). Male foraging peaked at a similar time regardless of the
temperature. but female foraging peaked earlier on warmer days (1000-1200 h) than on
cooler days (1400;1600 h). Female and male activity ceased at the same time on both days.

The patterns of males and females caught on the sticky traps at different times of the
day were significantly different from uniform distributions (2’2: 28.5. 20.3 for males and
females respectively; df = 7; P < 0.05) (Fig. 1A & B). The numbers of D. insulare (males
plus females) caught at different times of the day were also significantly different from a
uniform distribution on 11 September (12 = 25.8. df = 7. P < 0.05), but not on 13
September (2'2: 9.6; df = 6; P > 0.05). The diurnal patterns of male catch were
significantly different from the patterns of female catch at different time on both days (2’2:
35.5, 17.3; df = 7; P < 0.05).

In 1993. females foraging began between 0900 h and 1100 h, 1-2 h later than the
males, peaked between 1000 and 1300 h and ceased between 1900 and 2100 h (Fig. 2 and 3
A & C). Female Microplitis croceipes Cresson (Hymenoptera: Braconidae). a parasitoid of
Helicorverpa spp.. also begin foraging 1 h later than the males (Powel & King 1984).
Except on 18 August. female foraging ceased at the same time as males. The activity of
males plus females peaked at the same time as for females alone.

The diurnal patterns of males catch differed significantly from a uniform distribution
on 18 August and 5 September 1993 (2'2: 51.2 & 47.2; (if = 15; P < 0.05). However.
diurnal patterns of female catch differed significantly from a uniform distribution on all dates
(12: 26.1. 24.3, 27.0 & 33.3; df = 15; P < 0.05). Male plus female diurnal catch pattern
was also significantly different from a uniform distribution (12: 27.43. 57.6. 33.9 & 68.5;

(if = 15; P < 0.05). Male plus female diurnal catch pattern was also significantly different

D. insulare caught. per trap

0.2

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64

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Figure 1. Diurnal patterns of D. insulare caught in the sticky traps
on 11(A) and 13 (B) September 1993.

18 August 1993

14 August 1993

65

 

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Figure 2. Diurnal

temperature (middle)

D. insulare in the sticky traps (top). light intensity and

, and wrnd speed (bottom) on 14 August (A to C) and 18 August (D to F) 1993.

patterns of

66

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Figure 3. Diurnal patterns of D. insulare in the sticky traps (top), light intensity and
temperature (middle), and wrnd speed (bottom) on 22 August (A to C) and 5 September (D to F) 1993.

Collection interval (EDT)

67

from a uniform distribution (2’2: 27.43, 57.6, 33.9 & 68.5; df = 15; P < 0.05). In contrast
to 1992, there was no significant difference between male and female catch patterns (2’2:
15.7. 9.8, 6.6, 18.5; (if = 15, P > 0.05) (Fig. 2, 3 A & C). The total male catch per day
did not differ from female catch in August of both years (paired t-test; df = 15; P < 0.05) but
was significantly higher than the females catch in September in both years (paired t-test, df
= 15, P > 0.05)(Fig. 2 & 3). This suggests that more male offspring were produced at the
end of the cropping season. Low host larvae quality as a result of reduced food plant
quality at the end of the season may shift the parasitoid sex ratio. toward more males (Fox et
al. 1990. Harcourt 1986).

Relationship between diurnal foraging activity with weather factors.
Light intensity was significantly correlated with male, female and male plus female diurnal
foraging patterns (Table 1). Temperature and wind speed were significantly correlated with

only female foraging pattern, after stepwise elimination regression. Weather factors

Table 1. Multiple Correlation Statistics for Diadegma insulare foraging activity

 

Males“ Femalesb (Males + Females)C

Factors d.f

 

 

F P F P F P

 

 

Light intensity 1.54 15.49 0.0002 23.01 0.001 17.98 0.001

 

Temperatured " 0.22 0.64 12.33 0.001 1.01 0.32
Wind speedd " 0.78 0.38 6.12 0.016 1.45 0.23
a, r = 0.55; F = 4.97; df= 1, 54, P = 0.0009
b, r = 0.63; F = 7.39; df= 1. 54; P = 0.0001

68
explained 31.3, 40.3 and 39.8% of the variation in the male, female and male plus female
catch patterns. Relative humidity and cloud cover were not correlated with male. female or
male plus female catch on the sticky traps.

Light intensity was relatively higher on 18 and 22 August and 5 September 1993.
especially between 1000 and 1500 h, than on 14 August 1993 (< 1000 llEm'zs'l, micro
Einsteins per m2 per sec, throughout the day)(Fig. 2 B. E & 3 B, E). However, D. insulare
catch patterns on 14 and 22 August were similar (Fig. 2 & 3A). This indicates that factors
other than light intensity affected foraging activity patterns of D.'insulare. The diurnal
foraging patterns of D. insular-e males and females are shown by the lower D. insulare catch
in the morning and afternoon when light intensity is low, but peaked in the mid-day when
light intensity is peaked. Partly cloudy weather may lowered light intensity between 1300
and 1500 h on 5 September (Fig. 3 E).

Temperature was > 20°C throughout the day of 14 August and < 20°C on 5
September 1993 (Fig. 2 B). On August 18 and 22, temperature was lower
than 20°C before 0800 h, between 22 and 32°C in the mid-day and above 24°C in late
afternoon hours (Fig. 2 E & 3 B). However, more D. insulare males and females were
caught on 5 September than on 14 and 22 August. This suggests that temperatures > 25°C
do not increase D. insulare foraging activity. In the laboratory, the optimum temperature for
D. insulare and Diadegma semiclausum (Hellen)(Hymenoptera: Ichneumonidae), another
major parasitoid of diamondback moth. parasitism activity is 25-28°C (Bolter & Laing
1983, Talekar & Yang 1991). Females seemed more sensitive to low temperature than the
males because low temperature in the morning delayed the start of females foraging activity
1-2 h especially on 5 September compared to males. Low temperature may reduce the
numbers of active females and ,peak foraging activity as indicated on 11 September 1992
(Fig. l A). Bolter & Laing (1983) reported that 15°C is the minimum temperature for

females D. insulare to actively parasitizing the host.

69

Light intensity was always around 500 ttEm‘ZS'l. and temperature varied from
below 12°C to around 22°C between 0630 and 0700 h. On the sunny morning of 18
August, when temperature and light intensity were above 15°C and 500 ttEm’Zs".
respectively, males and females begin foraging 1 h earlier than on 14 (foggy morning) and
22 August (sunny). There was inconsistency of peak foraging time for both sexes even
though the temperature and light intensity were high (Fig. 2 & 3 A. B, D. E). There was a
drastic decline in the patterns of D. insulare males and female's activity 1-2 h after reaching
their peaks. However. the foraging activities increased again between 1500 to 1900 h
regardless of increase or decrease in temperature and decrease in light intensity (Fig. 2 & 3
A, B, D, E). Regardless of the afternoon temperature, foraging activity ceased when light
intensity lower than 500 ttEm'ZS'l. This suggests that foraging ceased because of poor
visibility in the late afternoon hours. D. semiclausum female used its visual perception for
finding suitable host for egg laying (Talekar & Yang 1991). Males of Campoletis
sonorensis (Cameron)(Hymenoptera: Braconidae). a parasitoid of Helicoverpa spp.. also
need adequate visual cues to locate females (McAuslane et al. 1990b). There were no D.
insulare males captured during this period or collection interval, suggesting that good
visibility prompted males to start foraging.

Wind speed was always lower than 4.0 m/s (14.8 km/h), but was correlated with the
diurnal patterns of D. insulare female foraging activity (r = 0.63; F = 6.12; df = 1, 54; P =
0.01)(Fig. 2, 3 C & F). On 18 August, wind speed was lower than the wind speed on 5
September 1993, but the total females caught were not different on both days. This
indicates that D. insulare may a have low wind speed threshold for its diurnal foraging
activity. However, low wind speed threshold may have a detrimental impact on D. insulare
foraging activity and parasitism rate during gusty winds. For example, On 11 September
1992, gusting wind (> 15 m per 8) may be the factor that significantly reduced the number
of females caught. Keller (1990) reported that the oviposition rate of Cotesia rubecula

(Marshall)(Hymenoptera: Braconidae) was reduced the increasing wind speed. Wind

70
gusting above 4.4 m per 5 also inhibits S. mesollana (Géhin) (Diptera: Cecidomyiidae)
flying to the wheat head to lay eggs (Pivnick 1993). Wind is important to carry sex
pheromone released by D. insulare females that invokes males to find mates. Chemical
signals released by female wasp that carried a long distance by wind was studied in detail by
LeMs et al. (1971) and Eller et a1. (1984).

Attraction between sexes. The numbers of males were not significantly correlated
with the numbers of females caught on the same traps on 14 and 18 August and 5
September (r = 0.05. 0.23. 0.19; F = 0.09. 2.55. 1.69; P = 0.77. 0.12, 0.20)(Fig. 4 A, B
& D). On 22 August, however, the number of males caught was negatively correlated with
the numbers of females caught on the same traps (Fig. 4 C). This suggests that more
females did not attract more males. There may be several reasons for this. First. females
may not release sex pheromones during host foraging and are therefore not attractive to
males. Second. females may call males by releasing pheromones while resting on a
substrate and waiting for the males to come to her; hence female catch would be low, male
catch would be high. Third, there may be intraspecific interference or competition between
the males.

Diurnal patterns of D. insulare caught in sticky traps versus direct or
visual observation. The patterns for percent of total day‘s catch of D. insulare males
plus females on the sticky traps and visually observed at different time of the day were
significantly different from a uniform distribution (12: 28.8, 25.6 & 30.1, on 14, 18 and
22 August, respectively; df = 14, P < 0.05)(Fig. 5 A to C). Both sticky traps and direct
visual observation counts indicated a similar time of peak parasitoid foraging activity on
each day. There was no significant difference between the percent of total D. insulare males
plus females caught on the sticky traps and those of visually observed at different time of the
day on 14, 18 and 22 August 1993 (12: 18.05, 19.4, 8.9; (if = 14. P > 0.05)(Fig. 5 A to
C). This indicates that sticky traps are as good as visual observation for monitoring

foraging activity of D. insulare. Parasitoids may be recounted during visual observation

Males per traps

71

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

3 A. 14 August 1993
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Females per trap

Figure 4. Relationship between the number of D. insulare

males and females caught on the same traps.

72

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Figure 5. Comparison of the percent of the total day's

D. insulare caught on the sticky traps versus direct or visual

observations (males plus females).

73

because I released them from the sweep net after they were counted. However, using sticky
traps means higher cost than visual observation and sticky traps do not give any direct
information about D. insulare activity. Sticky traps may be more applicable to large brassica
crop fields in developed countries where labor cost to hire people for field scouting is high.
In contrast. the visual observation method may be better suited for small brassica crop
growers especially in developing countries where the cost of labor is low and the price of
sticky traps is high. Although I found that using sticky traps took less time than visual
observation in counting D. insulare per unit time, sticky traps may only be suitable for
brassicas crops that have a similar leaf canopy to broccoli. I also observed that the flight
behavior of D. insulare is quite similar to another ichneumonid, Diadromus substilicomis
(Gravenhorst), a pupa] parasitoid of diamondback moth, in the cultivated brassica field.
Otherwise we could monitor D. insulare visually without using a sweep net to verify
identification.

Relationship between the numbers of hosts per plant and the numbers of
D. insulare caught on the sticky traps. There was a significant correlation between
the numbers of males and females, and males plus females caught per trap per 6 h and the
numbers of host larvae per plant (Fig. 6 A to C). This suggests that D. insulare tend to
aggregate, select and forage preferentially on plants with higher host's density. Similar
results were also reported for D. semiclausum and Diadegma fenestralis (Holmgren)
(Hymenoptera: Ichneumonidae)(Waage 1983). Aggregation of parasitoids may reduce the
effectiveness of parasitism because of mutual interference among females (Harcourt 1986)

and handling time on the host (Holling 1959).

74

 

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Numbers of larvae per. plant

Figure 6. Relationship of D. insulare caught per'sticky
trap with different numbers of host per plant. Effect of host
density (diamondback moth larvae) on D. insulare activity.

75
CONCLUSIONS

Pesticides continue to be an important tool for combating pests. However, D.
insulare is highly sensitive to pesticide spraying (Idris & Grafius 1993a). Results of my
study indicate that weather factors (light intensity, temperature and wind speeds) influenced
the patterns of D. insulare diumal foraging activity. This information could be useful in
developing a model that can predict the peak diurnal activity of D. insulare in the field. In
addition, a checklist of numbers of D. insulare per unit catches 6r observation could be
derived. This could help with decisions on whether pesticides should be sprayed. In
addition, it could reduce the pesticides' effect on D. insulare and other natural enemies of
diamondback moth and other Brassica crop pests in the field. In Malaysia, the numbers of
D. semiclausum pupae have been used as important information before decision to spray
pesticides is made in the integrated diamondback moth management program (Ooi 1992).

Both the sticky trap and visual observation are useful methods to monitor D. insulare
activity in the field. However, their practicality will depend on the farm size, the cost of
labor for scouting work and the price of the sticky trap. Further study is. needed to improve
diamondback moth integrated management programs especially for the numbers of host per
plant that influence diurnal foraging activity of the parasitoid. Weather factors and diurnal
foraging activity of parasitoid information are useful for insecticide ueatment decisions to

control crop pests and could improve pest management program.

CHAPTER 4

Effects of Plant Density on Diamondback Moth (Lepidoptera: Plutellidae)
and Its Parasitoid, Diadegma insulare (Cresson)(Hymenoptera:

Ichneumonidae)

76

77

ABSTRACT

Effects of plant density (broccoli, Brassica oleracea L. var. italica) on diamondback
moth, Plutella xylostella L., and its parasitoid, Diadegma insulare (Cresson) were studied
at the Collins Road Entomology Research Field, Michigan State University, in the summer
of 1993. Mean numbers of diamondback moth small larvae (first and second instars) were
not significantly different across the densities of broccoli planted (0.3 x 0.3 m, 0.6 x 0.6 m
and 0.9 x 0.9 m between plants) and sampling dates. However, mean numbers of large
diamondback moth larvae (third and fourth instars) and pupae and D. insulare pupae were
significantly influenced by plant density and sampling date. Percent parasitism by D.
insulare was not significantly affected by plant density. but was significantly affected by
date (range = 35 to 95%, mean > 75%). Percent of D. insular-e that were females (versus
males) and numbers of D. insulare caught on sticky traps were not significantly influenced
by plant density or date. Percent parasitism of diamondback moth larvae by D. insulare
was significantly higher in the upper one third of the plant canopy than in the lower one
third of the canopy. Temperature within the canopy was significantly influenced by plant
density, canopy height and time of the day. Temperature and relative humidity (RH)
were generally lower in the lower one third of the canopy than in the upper one third
canopy. The interaction between plant density and canopy height also influenced the R H.
within the broccoli canopy. Because plant density had no adverse affect on D. insulare
parasitism and suppressed diamondback moth population (influenced the number of small
larvae to reach 3rd or fourth instars), plant density for optimal yield and quality should be

emphasized in an integrated management program of diamondback moth.

78

INTRODUCTION

The "resource concentration hypothesis" suggests that specialist insect herbivores
should be more abundant where their food plants are concentrated (Root 1973). Many
insect parasitoids must locate certain plants to find suitable insect hosts (Vinson 1985). By
analogy with the resource concentration hypothesis for herbivores, specialist parasitoids
may be more likely to find, or less likely to leave, concentrated patches of their prey's food
plants (Sheehan 1986).

Concentration of host-plant resources involves at least five interdependent variables:
patch size; plant density; distance between patches; plant diversity (i.e., presence of non-
host plants); and plant quality (Kareiva 1983). However, the response of insects
colonizing different host plant concentrations or patches can vary (Macguire 1983, Sheehan
& Shelton 1989). For example, larvae of diamondback moth, Plutella xylostella
(L.)(Lepidoptera: Plutellidae), were more abundant on collards in large than in smaller
patches while larvae of imported cabbageworm. Pieris rapae (L.)(Lepidoptera: Pieridae),
were more abundant in smaller than in larger patches (Maguire 1983). In another study,
Cromartie (1975) reported that the numbers of diamondback moth and imported
cabbageworrn per plant were not significantly different regardless of numbers of plants per
patch.

The effects of plant density or spacing within a patch can be very useful in
integrated pest management programs (Dent 1991). An increase in plant density may
reduce pest numbers (A'Brook, 1964 & 1968; Farrell 1976; Tukahirwa & Coaker 1982)
but not in all cases (Mayse 1978, Troxclair & Boethel 1984). Lower insect numbers in

dense plantings may be caused by host plant condition and quality (Farrell 1976, Fox et al.

79

1990), excess vegetation acting as a deterrent (Delobel 1981), changes in the
microenvironment unfavorable to the pest or favoring its natural enemies, and the crop's
attractiveness (Coaker 1987). Parasitoids respond directly to plant properties (Shepard &
Dahlman 1988, Martin et al. 1990, Turling et al. 1990), and reduced herbivore mortality
from the action of natural enemies on poorer quality plants has been documented (Damman
1987). Plant quality, altered by treating collard plants with high or low N-fertilizer, did not
affect diamondback moth ovipositional preferences (Fox & Eisenbach 1992), but indirectly
affected parasitism rate and sex ratio of its major parasitoid, Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae)(Harcourt 1986, Fox et al. 1990). Fox & Eisenbach
(1992) reported that D. insulare spent less time to begin host searching or searched more
frequently on hosts that fed on high quality plant (high N-fertilized) than low quality plant
(low N-fertilized).

Habitat types or preferences of parasitoids may also be different from those of their
prey (Nordlund et al. 1988). The importance of spatial scale in the relation of parasitism to
local host density was discussed in detail by Wadle & Murdoch (1988).

The objectives of this study were to investigate the effects of plant density on (1)
diamondback moth numbers, (2) diamondback moth parasitism by D. insulare, (3) percent
of D. insulare that are female, (4) foraging activity of D. insulare, (5) parasitism rate at
different canopy heights and (6) plant canopy microclimate (temperature and relative

humidity).
MATERIALS AND METHODS

Experiments were conducted at the Collins Road Entomology Field, Michigan State
University, in the summer of 1993. I tested three different plant spacings; high (0.3 m
between plants), medium (0.6 m between plants) and low (0.9 m between plants), as

treatments in a 0.5 ha field. There were twelve 15 x 15 m plots with treatments (four

80
replications of each) arranged in a randomized complete block design. Broccoli (Brassica
oleracea L. var. italica. 'Green Comet') was transplanted on 25—28 June. Transplant
fertilizer 20:20:20 was applied immediately after planting. Plots were treated with
glyphosate (1.12 kg active ingredient/ha, Monsanto, Kansas City, Missouri) 3 wk before
transplanting and weeds were manually removed weekly after planting.

Diamondback moth population, percent parasitism and percent D.
insulare females. Ten percent of the plants (120 in high, 60 in medium, 10 in low
density) were randomly sampled weekly a long the transect, beginning July 21; numbers of
small diamondback moth larvae (first - second instar), large larvae (third - fourth instar)
and pupae; and D. insulare pupae were recorded. Second to fourth instars of diamondback
moth and D. insulare pupae were collected from the plants every other week beginning 24
July and reared in the laboratory to measure the percent of D. insulare females versus males
emerged. Plants where I collected D. insulare pupae and diamondback moth larvae were
marked and not used for other data collection.

Foraging activity of D. insulare. D. insulare foraging activity was measured by
randomly selecting four broccoli plants per replicate per ueatrnent. White sticky traps
(PheroconTM 1C trap-bottoms, Trece lnc.. Salinas, CA) were folded in half, sticky side
out, and attached to wooden stakes with binder clips at 15 cm height within the broccoli
canopy (six per plot). Traps were placed within the broccoli canopy at 0700 h on 7 and 22
August. D. insulare caught were recorded, sexed and removed every 3 h until 2000 h,
when D. insulare activity ceases (Chapter 3).

Parasitism within canopy. Five plants were randomly selected from each plot on
18 and 23 August to compare the parasitism rate at top versus bottom canopy levels. The
broccoli plant was divided into three equal sections; upper, middle, and lower. On 18
August, I collected diamondback moth second and third instars from upper and lower
sections, and reared them in the laboratory until pupation as before. Numbers of

diamondback moth and D. insular-e pupae formed were recorded. On 23 August, all larvae

81
on these plants were removed by hand and replaced with 10 laboratory-reared diamondback
moth larvae (second and third instars). Larvae were collected 24 h after release and reared
as above to measure percent parasitism.

Canopy microclimate. I used wet bulb dry bulb hygrometers (Taylor Products,
Fletcher, NC.) to measure relative humidity (RH) and temperature within the canopy on
18 August Four broccoli plants per replicate per treatments were randomly selected. Plant
canopy was divided into three sections as before. Hygrometers were placed on the leaf
stalk within upper or lower sections. Temperature and R. H weie recorded every 20 min
from 1000 until 1800 b.

Data for number of small and large larvae, diamondback moth pupae and D.
insulare pupae were transformed using Log (1 + X); while percent parasitism data were
transformed using arcsim/i before analysis using 2-way ANOVA (density x
date)(Abacus Concept, SuperAnova 1991). Percent D. insulare females and parasitism
(arcsin sf): transformed) at upper and lower canopy among treatments were also analyzed
by 2-way ANOVA. Three-way ANOVA were used to analyze the effects of plant density,
time of day and plant canopy position on relative humidity and temperature within plant
canopy. Numbers of D. insulare adults caught on sticky traps were analyzed using l-way
ANOVA. Where ANOVAs determined significant treatment effects, means were separated

using Fisher's Protected LSD (Abacus Concept. SuperAnova 1991).

RESULTS AND DISCUSSION

Diamondback moth population, percent parasitism and percent D.
insulare females There were no significant differences in the mean numbers of small
larvae per plant among plant densities (F = 2.5; df = 2 & 54; P > 0.05), across the dates ( F
= 1.7, df = 5 & 54, P > 0.05) and the interaction between these two factors was not

significant (F = 1.4, df = 10 & 54, P > 0.05). Therefore, diamondback moths may have

   

 

82

laid eggs randomly in the plots which produced similar numbers of early instar. This
suggests that the contrast between plant and soil background that occurred among the plant
densities over the dates did not influence optomotor landing responses of adult
diamondback moth females as reported for Aphis craccivora (Koch)(A'Brook 1968).
Broccoli plants in the high density plots matured earlier. becoming less suitable for growth
of small diamondback moth larva (Eigenbrode & Shelton 1990a), than the plants in the low
density plots. Heavy rainfall may also affect small diamondback moth larvae, washing
them from the leaves (Wakisaka et al. 1992), or increasing disease incidence (Wilding
1986). The upward leaf orientation in high density plots (0.3 m between plants) may also
increase the impact of rainfall on small larvae compared with its impact in low density plots
(0.9 m between plants).

Plant density (F = 19.9, (if = 2 & 54, P < 0.05) and date (F = 14.4, (if = 5 & 54,
P <0.05) significantly affected numbers of large larvae per plant. The mean numbers of
large larvae per plant were generally lower in the low plant density than in the other two
plant densities throughout the sampling period (Fig. I A). This agrees with the resource
concentration hypothesis (Root 1973). However, Pimental (1985) reported that herbivores
per plant surface were five time more abundant in sparse and dispersed plantings than in the
dense planting. On most dates, numbers of large larvae are similar in the high and medium
plant densities plots. Numbers of large larvae were lower in the early season (July) than in
later of the season especially for the medium and high plant density (Fig. l A). Regardless
of plant density, numbers of large larvae were highest on 6 August than on the other dates.
There was a significant density and date interaction for numbers of large larvae collected
per plant (F = 2.7, (if = 10 & 54, P < 0.05).

Plant leaf quality is one of the factors that determines the abundance of
diamondback moth populations in the late season because of its direct effects on early larval

survivorship (Harcourt 1986). However, my August data showed that large larvae were

Larvae per plant i S.E.M

Pupae per plant i S.E.M

0.0

0.4

0.0

83

A. Large diamondback moth larvae

 

 

 

 

 

 

 

B. Diamondback moth pupae

 

1.6

 

1.2

 

0.8

 

0.4

 

 

 

 

 

1.6

 

 

1.2

 

 

High density

 

 

 

0.8

 

 

      

 

 

21 26 6 13 21 27

|<—-— August ———>I

Figure I. Number of diamondback moth large larvae (A) and pupae (B), and

D. insulare pupae (C) in three different broccoli densities (0.3, 0.6 and 0.9 m
between plants).

84
more abundant in the high and medium plant densities than in the low plant density
(expected to have better quality leaf due to less competition between plants).

Plant density did not significantly influence the mean numbers of diamondback
moth pupae per plant (F = 2.5, (if = 2 & 54, P > 0.05). However, mean numbers of
diamondback moth pupae were significantly different among dates (F = 5.4, df = 5 & 54.
P < 0.05). Mean numbers of diamondback moth pupae per plant were significantly
influenced by the plant density and date interaction (F = 2.6, df = 10 & 54, P < 0.05)(Fig.
l B). Numbers of pupae collected across the dates showed a similar trend to large larvae
(Fig. l A & B). I expected higher numbers of pupae in the low densities than in the high
plant density plots. This is because of better plant quality in low density than in the high
density (higher competition for growth between plants in the high than in low density) may
allow more larvae to reach the pupal stage in the low density planting. However, heavy
rainfall may have increased disease incidence (Wilding 1986) and loss to predators and
parasitoids perhaps allowed fewer larvae to successfully reach the pupal stage (Wakisaka et
al. 1992, Harcourt 1986) in the low densities plots.

Plant density (F = 15.7, df = 2 & 54, P < 0.05) and date (F = 13.9, df = 5 & 54, P
< 0.05) significantly affected the mean numbers of D. insulare pupae per plant. Mean
numbers of D. insulare pupae per plant were also significantly affected by the date by plant
density interaction (F = 3.1, df = 10 & 54, P < 0.05)(Fig. l C). Except on 6 August,
numbers of D. insulare pupae were higher in the medium or high densities than in the low
plant density (Fig. 1 C); this trend was similar to both numbers of diamondback moth large
larvae and pupae per plant (Fig. 1 A to C).

Regardless of sampling date or plant density, there were more D. insular-e pupae
than diamondback moth pupae (up to a 4 fold difference). This indicates that D. insulare is
one of the most important natural enemies of diamondback moth agreeing with previous
reports (Harcourt 1986, Idris & Grafius 1993, Biever et a1. 1992). Mean percent

parasitism ranged between 35 and 95%. averaging > 75% in all plots. However, percent

85
parasitism was not significantly affected by plant density (F = 1.3; df = 2 & 54; P > 0.05)
or sampling date (F = 1.6, df = 5 & 54, P > 0.05). In contrast. Fox et al. (1990) reported
that parasitism rate declined as the season progressed because plants became older
(provided low quality food to the host larvae) which may have more adverse effects on D.
insulare larvae than on its host larvae. Talekar & Yang (1993) reported that Diadegma
semiclausum (Hellcn)(= eucerophagaXHyrnenoptera: Ichneumonidae) parasitism rate
increased as the brassicas crops grew older or was not affected by plant age.

Percent of D. insulare females (versus males) from field‘collected larvae and pupae
ranged from 15 to 55% (i = 30.6% i 12.4)(range for plant density x dates) but was not
significantly different among plant densities (F = 1.0, df = 2 & 36, P > 0.05) or among
sampling dates (F = 1.9, df = 3 & 36, P > 0.05). Fox et al. (1990) and Harcourt (1986)
showed that plant quality resulting from low N-fertilized plants or increased plant age
contributed to a male bias sex ratio of D. insulare. In my study both plant density and date
affect plant growth and maturity. but did not consistently affect proportion of female D.
insulare.

Foraging activity of D. insulare. The mean numbers of male or female D.
insulare caught per trap per day were not significantly different among plant densities
(male: F = 2.3, df = 2 & 18, P > 0.05; femalezF = 1.9, df = 2 & 18, P > 0.05) or sampling
dates (males: F = 0.18, df = 2 & 18; P > 0.05; females: F = 1.0. df = 2 & 18, P > 0.05).
This suggests that D. insulare are abundant and visited the host's habitat regardless of the
numbers of hosts per plant (there were fewer diamondback moth larvae in lower than in the
higher plant density plots, Fig. 1 A). Brassica plants with zero hosts are still visited by D.
insulare (Chapter 3) and D. semiclausum (Waage 1983).

The mean total males plus females caught were significantly different among plant
densities (Fig. 2)(F = 3.7, df = 2 & 18, P < 0.05) but not between dates (F = 0.02, df = l
& 18, P > 0.05). Mean total catch was significantly higher in medium and high than in the

low density planting (FPLSD, P < 0.05) where diamondback moth larvae were also less

 

   

86
abundant. Regardless of plant density, the patterns of D. insulare caught in 3 h intervals
per day were not different (2'2 = 2.4, df = 8, P > 0.05); they were active from 1100 to
2000 h (Chapter 3). 7

Parasitism within canopy. Percent parasitism of diamondback moth larvae within
the upper or lower one third of the canopy were not significantly different among plant
densities (F = 0.2, df = 2 & 18, P > 0.05). However, percent parasitism diamondback
was significantly higher in the upper one third than in the lower one third of the canopy for
all plant densities (F = 4.5, df = l & 18. P < 0.05; FPLSD, P >'0.05)(Fig. 3 A).
Although parasitism of the larvae in the upper was higher than in the lower canopy for each
plant density, percent parasitism on the lower canopy was also very high (79.8-83.6%).
D. insulare females appear to have excellent host searching capacity (Lasota & Kok 1986),
and parasitism is not severely affected by plant density. Percent parasitism of laboratory-
reared diamondback moth larvae was not significantly different across plant densities (F =
1.7; df = 2 &18; P > 0.05) or height within canopy (F = 0.9, df = l &18; P > 0.05)(Fig. 3
B). There was no significant interaction between plant density and canopy height to
influence percent parasitism of the field (F = 0.4, df = 2 &18, P > 0.05) or laboratory-
reared diamondback moth larvae (F = 0.3, df = 2 &18, P > 0.05).

Canopy microclimate. The temperature within the canopy was significantly
influenced by plant density, time of day and canopy height and the interaction among these
factors (Table l). Regardless of plant density and canopy levels, temperature was above

20-25°C for most of the day except between 1000 and 1100 h (Fig. 4 A & B).
Temperature was higher in the upper one third canopy of low density plants than in the
upper one third canopy of medium or high density plant between 1200 and 1500 h (Fig. 4
A). Conversely, temperature was lower in the lower one third of low density planting than
in the lower one third canopy of the other two plant densities (Fig. 4 B). The daily

temperature never exceeded 30°C; the upper threshold temperature for D. insulare is 35°C

87

 

 

 

 

 

E- 4 , D. insulare males + females

US

+1 3 Li
E‘ 2

a . V

"5

a 1 ‘

'53

g 0 B j T

 

 

 

Low Medium High

Plant density
Figure 2. TotalD. insulare males plus females caught per

plant in three different broccoli planting densities (0.3, 0.6 and
0.9 m between plants).

 

951 (A) Field larvae

90

 

 

85

 

 

 

80

 

75

 

 

 

70 . .
Upper Lower

 

95 . (B) Laboratory-reared larvae __,_ High gensity

90 ’ """ Medium "
t '_A'— Low "

 

 

 

 

 

 

Percent parasitism (i S. E)

85

 

 

80

d

 

 

75

 

 

 

70 . .
Upper Lower

Canopy height

Figure 3. Percent parasitism of field (A) and laboratory-reared (B)
diamondback moth larvae byD. insulare in the upper versus lower

broccoli canopy in the three different broccoli planting densities
(0.3, 0.6 and 0.9 m between plants).

88
(Bolter & Laing 1983). The moderate temperatures partly explains why the average percent

parasitism was > 75% in all plant densities.

Table 1. ANOVA for effects of plant density, time of day and canopy height on the
temperature (0C) within the broccoli canopy

 

 

Sources df F — value P - value
im 1 ff
Plant density 2 8. 8 0.001
Time of day 7 87. 1 0.0001
Canopy height 1 26.1 0.0001
lateraetionrifects

Density it time 14 3.6 0.0001
Density x canopy 2 20.0 0.0001
Time x canopy 7 21.8 0.0001
Density x time x canopy 14 2.2 0.0107
Error 144 - -

 

Mean relative humidity (R. H.) within the canopy of broccoli was significantly
influenced by plant density, time of the day, canopy height and by the interaction between
plant density and canopy heights (Table 2). Mean R.H. in the uppet one third of canopy
was lower than in the lower one third of the canopy for all plant densities, and it was higher
in the lower one third canopy in low density than in the lower canopy of the medium or
higher density broccoli (Fig. 5). Microclimate may be important, however D. insulare's

diurnal activity was not affected by RH. in open field (Chapter 3).

89

 

 

 

 

 

 

““0"" Low dens'ty
_0_ Medium density
15 ""6"" High density

 

 

 

 

 

 

 

10

1000-1100 "
1100-1200 ‘
1200-1300 ‘
1300-1400 ‘
1400-1500 ‘
1500-1600 ‘
1600-1700 ‘
1700-1800 ‘

 

 

Temperature (0C) i S.E.M

 

 

 

 

 

10

1000-1100‘
1100-1200 ‘
1200-1300‘
1300-1400‘
1400-1500‘
1500-1600‘
1600-1700‘
1700-1800“

C.)
a

g
E.
35:
5'
5.
a
2

E.

Figure 4. Temperature (0C) in the upper (A) versus lower (B)
broccoli canOpy planted in three different plant densities (0.3, 0.6, and
0.9 m between plants).

90

Table 2. ANOVA for effect of plant density, time of day and canopy height on the
relative humidity (%) within the broccoli canopy

 

 

 

 

 

 

 

 

 
 

 

 

 

 

 

 

 

 

 

 

 

Sources df F - value P - value
Simnleeffws
Plant density 2 30.8 0.0001
Time of day 7 217.5 0.0001
Canopy height 1 394.9 0.0001
mm
Density x time 14 1.5 0.1300
Density x canopy 2 40.7 0.0001
Time x canopy 7 0.8 0.5754
Density x time x canopy 14 0.7 0.7909
Error 144 - -
A
Q
8 68
a K . " 'A ‘ ‘ High density
... 66 "-1-" Medium density
"" ‘ —0— Low density
0: 64
5 2 62
.1: m .
cu CD 60
> .
.5 +| 58
E 4
c» 56 ' fl
m UPPCI‘ Lower

Canopy height

Figure 5. Relative humidity (%) in the upper versus lower broccoli

canOpy planted in three different plant densities (0.3, 0.6 and 0.9 m
between plants)

91
The influence of interactions among plant density, time of the day and canopy

height on temperature and RH. may have direct or indirect effects on percent parasitism of
diamondback moth by D. insulare and the survivorship of diamondback moth larvae (Fig.
3 A, 4 & 5) as well as the functional and numerical response of other diamondback moth
natural enemies. For example, percent parasitism of diamondback moth larvae was higher
in the lower one third than in the upper one third of broccoli canopy in all plant densities
(Fig. 3 A). Low temperature and high R.H. in the lower canopy (Fig. 4 & 5) may favor
the action of natural enemies, especially diseases (fungal, viruses and microsporidium), on
both unparasitized and parasitized diamondback moth larvae. Other factors, such as low

diamondback moth larval populations and leaf quality, are also involved.

CONCLUSIONS

Further study on the effects of plant density on diamondback moth populations
and parasitism by D. insulare under different field locations and setting are necessary
before recommendation of plant density can be made. However, because D. insulare
parasitism rate, abundance of adults and sex ratio are not seriously affected by plant
density, plant densities that suppress diamondback moth populations and produce optimal

yield and quality should be emphasized.

CHAPTER 5

Influence of Habitats on the Parasitism of Diamondback Moth, Plutella
xylostella (L.) (Lepidoptera: Plutellidae), by Diadegma insulare

(Cresson)(Hymenoptera: Ichneumonidae)

92

93

ABSTRACT

Influence of habitats on the percent parasitism of diamondback moth larvae, Plate/la
xylostella L., by Diadegma insulare (Cresson) and its presence in habitats were studied at
the Michigan State University Research Farm during the summer of 1992 through 1994.
Percent parasitism was measured by placing broccoli plants infested with third instar
diamondback moth in crop and non-crop habitats for 26 to 28 h. Numbers of D. insulare
caught on the sticky traps placed in habitats were used to measure its presence in the
respective habitats. Percent parasitism was significantly different among the habitats.
although parasitism occuned in all habitats except in the center of the woodland. This
suggests that D. insulare is very mobile and effective searcher. Percent parasitism was
very high (> 40% to 60%) in most crop and non-crop habitats, however, it was
significantly influenced by the interaction between habitats and dates (months and years) of
observations conducted. The percent parasitism of diamondback moth larvae decreased as
the distance of treatments in the corn field from the field edge increased, suggesting that the
corn field is not a primary habitat for D. insulare. Numbers of D. insulare caught on the
sticky traps was significantly lower in habitats without D. carota, Brassica kaber L., B.
nigra L. or Raphanus raphanistrum L. than in habitats that have these weeds (nectar
sources for D. insulare). This indicates that D. insulare preferred habitats that can provide
food sources or suitable hosts or both. The present monoculture of brassica crops could be
modified into intercropping or polyculture systems without negatively affecting the impact

of D. insulare in diamondback moth management program.

94

INTRODUCTION

Gould & Stinner (1984) defined habitat as the physical area encompassing the
resources that support the existence of an individual insect or insect population for a
specific time. They define habitat heterogeneity as the environment being composed of
significantly different parts within a particular landscape. Habitats can influence the
population size and disuibution size of the pest and its parasitoids (Cromartie 1975a & b,
Hawkin & Sheehan 1994). Vinson (1985) outlined that habitat preference and the potential
of host community location within the habitat are two of the nine steps necessary for
successful parasitism. He also suggested that the interactions between the host's habitat
and the parasitoid are depend on the active behavioral and physiological aspects of the
parasitoid. A study conducted by Landis & Haas (1992) indicates that the microclimate of
habitats, particularly in warm years, influences the movement and behavior of Eriborus
terebrans (Gravenhost)(Hymenoptera: Ichneumonidae), a parasitoid of European corn
borer, Ostrinia nubilalis (Hiibner)(l.epidoptera: Pyralidae). Dyer & Landis (1993) and Sato
& Ohsaki (1987) reported that the effects of habitat on parasitoid activity varied as the
season progressed. Types of vegetation within or between habitats also affected parasitism
by Cotesia (= Apantales) glomeratus L. (Sato & Ohsaki 1987).

The effects of habitat heterogeneity on the predator-prey dynamics are subject to
specific dispersal behavior of the predator and prey (Kareiva 1987). Landis & Haas (1992)
reported that the effectiveness of E. terebrans is influenced by the local landscape mosaic,
including proximity of particular crops or other non-crops with the host habitats. The
structures of landscape also influence the spatial distribution of adult food resources for this

wasp (Landis 1993). Non-host plants in the heterogeneous habitat of polyculture

95
agroecosystems can affect the movement of herbivores and their natural enemies (Sheehan
1986, Andow 1988, Lawrence & Bach 1989). The specialist parasitoids might be less
abundant in the structurally complex polyculture than in structurally simple monocultures;
chemical cues used in host finding will be disrupted and parasitoids will be less able to find
hosts, therefore, they are more effective in less diverse agroecosystems (Sheehan 1986,
Andow & Prokrym 1990).

Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae), the major parasitoid
of diamondback moth, used nectar sources from certain wildflOWers that grew in different
habitats (Idris & Grafius 1995a). Differential temperature in habitats may affect D.
insulare's fecundity, longevity and day-time foraging activity which indirectly determines
the parasitism rate (Chapter 1). In addition, suitable habitats near the insecticide-treated
field could provide refuge for D. insulare.

The objectives of this study were to (l) assess the presence or absence of D.
insulare in different habitats. and (2) find out the influence of habitats on the percent

parasitism of diamondback moth by D. insulare.

MATERIALS AND METHODS

The study was conducted at the Michigan State University Research Farm, East
Lansing, Michigan, during the summers of 1992 through 1994. The habitats used were;
beans (Phaseolus vulgaris L., Pisum sativum L. and Glysine max (L.) Merill), tomato
(Lycorpersicon esculentus Mill), com (Zea maize L.)and alfalfa (Madicago sativa L.)
fields, apple (Malus domestica Borkh) orchard, weedy areas, and at the center and edge of
woodland (Fig. 1). I did not use all these habitats in every observation because they were

not always available.

96

 

 

 

 

 

 

 

 

 

 

 

Forest Road b
SWinC '\v'
, College [:1 Research
C0111“ .. Road
Road C .
at‘
7' . 1‘ Beef Cattle Research
a
wa Bennett Road
496 Entomological 'at‘ . I
Research .. . . .. C. . .
wa w t w wa"
n30 1 o I r o
c b a t af"
" Ia!
t
Botany &Plant
\ Pathology Field
Lab. b"
Jolly Road
To Detroit ___)
Jral Research wa"
't la!
Cwl
N
Scale in meters
:2:

l o 225 550

‘g

Figure 1. Location of habitats at Michigan State University Research Farm
selected for the study (a, apple; af, alfalfa; b, beans; c, com; t, tomato; w, woodland;

wa, weedy areas). Letters with _ , _ , _ , and '_ indicate that the habitats were
used only during 1992 and 1993, 1992 to 1994, 1993 and 1994, respectively.

97

Greenhouse grown broccoli plants, Brassica oleracea var. italica (L.) cav. 'Green
Comet' raised in pot were used for the study. At two months old each broccoli plant was
infested with ten second or third stadium diamondback moth larvae. Infested plants were
kept in the greenhouse for 18 to 20 h before placing in various habitats. I added new
diamondback moth larvae for plants that had less than 10 larvae per plant after setting out
the plants.

Weedy areas used in 1992 had > 50% Daucus carota L. but only two replicates of
weedy areas used in 1993 had a similar density of D. carota as in 1992. Weedy areas were
not used as tested habitat in 1994 because there were only two small weedy areas available.

Influence of Habitat on Percent Parasitism. Amgng Habitats. I placed 20
infested broccoli plants in each habitat (five pots of broccoli plant per replicates = 50 larvae)
between 1000 and 1200 h. Each treaunent (habitat) was replicated four times. The next
day between 1400 and 1600 h plants and larvae were collected. I randomly selected 20
larvae per replicate. Larvae were placed in a 14.5 cm diam Petri dish with 3 cm diam
screen lid on the cover (20 larvae per dish per replicate) and brought to the laboratory.
Larvae were fed broccoli leaves grown in the greenhouse and kept at 25 i 2°C,
photoperiod 16: 8 h L : D until pupation. The numbers of D. insulare and diamondback
moth pupae formed were recorded. 1 did not dissect the diamondback moth larvae because
D. insulare eggs are encapsulated and survival of D. insulare larvae is always high (Chapter
1, Bolter & Laing 1983).

Within the same habitat Qf non-hast plant (99m). To determine within field
influence on the parasitism of diamondback moth larvae I conducted a similar experiment
on the same corn fields as before on 13-14 August 1994. However, I placed the treatments
inside the com field at 50, 100, 200 and 500 m from the field edge.

Percent parasitism of diamondback moth by D. insulare was calculated as the total
number of D. insulare pupae divided by the total number of diamondback moth plus D.

insulare pupae x 100 (Idris & Grafius 19930). The percent parasitism (transformed using

98

arcsin J)? ) among habitats, at different distances from corn field edge, and at different
habitats versus months or years were analyzed by l-way and 2-way ANOVA,
respectively. Fisher's Protected LSD (Abacus Concepts, SuperAnova 1991) was used to
separate means when main effects were significant (no significant interaction between
factors).

The presence of D. insulare in habitats. I used 40 white sticky traps
(PheroconTM 1C trap - bottom; Trece lnc.. Salinas, CA) per habitat (10 traps per replicate,
10 m between traps) to assess the presence of D. insulare within. the habitats. Each trap
was folded in half to make a two-sided trap with sticky side out. Traps were placed upright
on a 40 cm stake in; weedy areas, middle of alfalfa fields, and within the canopy of tomato,
Brassica kaber L., B.nigra L. and Raphanus raphanistrum L.; along the edge and center of
the woodland; or hung on apple tree branches, and corn leaves (50 m into the field). Trap
height varied with habitat but ranged from 20 to 80 cm from the ground except for apple
orchard (depending on the height of the apple tree). D. insulare trapped were recorded
every day between 1800 and 1900 h for a week. I removed D. insulare from the traps
every day. Numbers of D. insulare caught per trap per day in various habitats were
analyzed using 1-way ANOVA and means were separated as above. Data were

transformed using Log (1 + x) before analysis.

RESULTS AND DISCUSSION

Influence of habitats on the percent parasitism. W. Percent
parasitism was significantly different among habitats in all years (0—89%), and was high (>
40-60%) in most habitats regardless of the sampling dates and years (Fig. 2 to 4).

In 1992, percent parasitism ranged from 55% (bean) to 89% (tomato)(Fig. 2).
Except at the woodland edge, parasitism was significantly higher in the tomato than in the

other habitats (79%)(Fisher's PLSD, P < 0.05). In 1993, parasitism ranged from 3%

 

99
(woodland edge) to 87% (com)(Fig. 3). Except in the alfalfa fields, parasitism in the other

crop habitats was considerably higher (70-87%)(Fig. 3) and comparable to with 85-93% in
a nearby broccoli field (unpublished data). The apple orchard, the only crop habitats used
in the three sampling dates in 1993, had consistently high rates of parasitism (76-81%).
Parasitism in the non-crop habitats (woodland edge and weedy areas) was low except on
15-16 August 1993 when parasitism at woodland edge was as high as in the crop habitats.
On 12-13 August 1994, percent parasitism was significantly higher in the corn field (80%)
than in the other habitats (0-40%)(Fisher's PLSD, P < 0.05)(Fig. 4). There was no
parasitism recorded in the center of the woodland.

The percent parasitism of diamondback moth larvae was significantly affected by
the interaction between habitats and dates (month: F = 24.4, (if = 2 & 8, P = 0.001; year:
14.4, df = 4 & 27, P = 0.001)(Fig. 5 A & B). Parasitism at the woodland edge was
significantly lower in September than in July and August 1993 (Fisher's PLSD, P <
0.001)(Fig. 5 A). In 1994, parasitism was higher in the corn field than in the other habitats
(Fig. 5 B).

Within the same habitat Qf nan-hast plant (99m 1. There was a significant
correlation between percent parasitism of diamondback moth larvae and the distance from
the field edge (r = 0.86, F = 40.9, df = 1 & 14, P < 0.001)(Fig. 6). Distance from the
field edge explained 74.5% of the variation in the percent parasitism of diamondback moth
larvae; decreased as the distances of the ueatments from the edge into the corn field

increased.

 

 

 

 

 

 

 

 

E 10-11 August 1992
m 100
.5. .
o- A 80
gas 60-
.35! 40-
=

c

o

S-r

c

D-r

‘3
Tomato
Corn
Apple

Weedy areas

Figure 2. Percent parasitism of diamondback moth larvae by D.
insulare in various habitats on 10-11 August 1992. In corn field treatment
was placed i 30 m from the field edge. Bars with different letters are
significantly different (Fisher's Protected LSD, P < 0.05).

101

A. 23-24 July 1993

 

 

 

 

 

 

Percent parasitism (iS.E)

 

Woodland

Figure 3. Percent parasitism of diamondback moth larvae
by D. insulare in various habitats on 23-24 July (A), 15-16 August
(B) and 13-14 September 1993 (C). In the corn field treatment
was placed i 30 m from the field edge. Bars with different letters are
significantly different (Fisher's Protected LSD, P < 0.05).

Percent parasitism (i S. E)

102

12-13 August 1994
100

80
60
40
20

C

 

Apple
Alfalfa
Corn

Woodland edge
Woodland center

Figure 4. Percent parasitism of diamondback moth larvae by D.
insulare in various habitats on 12-13 August 1994. In corn field treatment
was placed 1 30 m from the field edge. Bars with different letters are
significantly different (Fisher's Protected LSD, P < 0.05).

103

A. Habitats x month

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

100‘
mjfli a
m ‘I I.’ °\.‘. —0— APP“
m. . ---- mm...
m 40‘ i-
+l
20 ~.\
1 .‘
E 0 . . l
'2; July August September
‘2‘ B. Habitats x year
a 100
5 .
E 80* r ....... -I~. \9
m "\ r_°_ IPPiC
60 ". “W" woodlandedge ]
A \R —0— itsidecomfield
40 ' “ (30 m from field edge)
1 .‘ '
20 . . fi
91 92 93 94 95

Figure 5. Percent parasitism of diamondback moth larvae
as affected by the interaction between habitat and months in
1993 (A) and years (B). -

 

 

l ................. .Y=63-7"U3X-F=4‘19-. .. ....................
80 o r=0.86,df=1&14,1’<0.001

a\\
0 100 200 300 400 500 600
D'stant fromcornfreld edge (m)

 

 

-3

 

 

 

 

 

Percent parasitism
:l: S.E
3

Figure 6. Relationship of percent parasitism of
diamondback moth larvae by D. insulare and the distance
from the field edge.

104
The presence of D. insulare in habitats. The numbers of D. insulare caught per
trap per day on the sticky traps were significantly different among the habitats in both years
(1993: F = 4.1, df = 9 & 27, P < 0.05; 1994: F = 10.6; df = 5 & 15, P < 0.05)(Table l &
2).

In 1993, numbers of D. insulare caught were significantly higher in traps placed at
the woodland edge that had 50 to 70% Daucus carota L. than in traps placed with
Asteraceae plus A gropyron repens (L.) Beauv, in the alfalfa, weedy areas or apple habitats
(FPLSD, P < 0.05)(Table 1). There was a significantly difference between the numbers
of D. insulare caught on traps placed in weedy areas and along the woodland edge where
D. carota were the majority of plants present (FPLSD, P < 0.05). There were no D.
insulare caught along the woodland edge where A. repens was > 90% of the plants
present, and in the weedy areas where Compositae plus grasses or A. repens were the
dominant weed present. In 1994, numbers of D. insulare caught were significantly lower
in the tomato and corn fields than in habitats primarily with B. kaber, B. nigra and R.
raphanistrum (Fisher's PLSD, P > 0.05). There were no D. insulare caught in the traps
placed in the center of the woodland. This indicates that D. insulare is more abundant or
prefers habitats that can provide them food sources or alternate hosts. In crop habitats, the
numbers of D. insulare caught were somewhat higher in traps placed in the tomato and corn
fields than in traps placed in the alfalfa field or apple orchard (Table l & 2).

As a kionobiont parasitoid (host larvae continue to develop after oviposition and are
only killed in the late instar as oppose to idiobiont parasitoids which paralyze or kill the
host larvae or pupae, respectively, after oviposition) D. insulare may have a restricted host
range in a simple habitat within a particular landscape (Askew & Shaw 1986). Therefore,
it has to be very mobile in heterogeneous habitats to find its alternate hosts. This explains
why the parasitism of diamondback moth larvae occurred in all habitats except in the center

of the woodland (Fig. 2 & 4).

105

Table 1. Number of D. insulare caught in various habitats from 12 to 18 August 1993

 

 

Habitats Number of D. insulare caught
per trap per day (i S.E)“

Woodland edge

50 to 70 % Daucus carota L. 0.40 i 0.16c

Asteraceae + Agropyron repens (L. ) Beauv 0.05 i 0.28ab

> 90% A. repens 0a

no weed but shrubs ' 0.15 :t 0.05b
Apple 0.08 :1: 0.053b
Weedy areas

50 to 70 % D. carota 0.18 i 0.05b

50 to 70 % Asteraceae weeds 0.03 i- 0.03ab

Asteraceae + grasses 0a

> 90% A. repens 0a
Alfalfa 0.05 i 0.03ab

 

a In column means with same letter are not significantly different (Fisher's Protected LSD,
P > 0.05)

Table 2. Number of D. insulare caught in various habitats from 14 to 20 August 1994

 

 

Habitats Number of D. insulare caught
' per trap per day (i S.E)“

Woodland center 0a

Tomato 0.15 :l: 0.05a
Corn 0.14 i 0.08a
50 to 80% Brassica nigra (L.) (Black mustard) 1.60 i: 0.19b
50 to 70% Raphanus raphanistrum L. (wild radish) 1.50 i 0.14b
50 to 70% Brassica kaber L. (wild mustard) 1.83 i 0.17b

 

a In column means with same letter are not significantly different (Fisher's Protected LSD,
P > 0.05)

106

In August 1992, parasitism was higher when larvae were placed in tomato than in
alfalfa and corn, and apple habitats (Fig. 2). On 23-24 July 1993. however, percent
parasitism in tomato was not different with alfalfa and apple habitats (Fig. 3 A). On 15- 16
August, percent parasitism was similar across all habitats (70 to 90%) except in the weedy
areas (30%)(Fig. 3B). This suggests that D. insulare were more abundant in habitats other
than the weedy areas. On 12-13 August 1994, percent parasitism in the apple orchard and
along the woodland edge is somewhat lower than the parasitism in these habitats in the
same month of 1992 and 1993 (Figs. 2. 3 A & B, 4 ). This is probably due to lack of
visual cues for D. insulare to locate its host or they were less active in the cloudy day (low
light intensity) on the 12-13 August The numbers D. insulare caught on the sticky traps
were also positively conelated with the light intensity (Chapter 3). Diadegma semiclausum
(Hellen)(Hymenoptera: Ichneumonidae), another important larval parasitoid of
diamondback moth, uses its visual perception for finding a suitable host for egg laying
(T alekar & Yang 1991). Campoletis sonorensis (Cameron)(Hymenoptera:
Ichneumonidae). a parasitoid of Heliothis virescens (F.)(Lepidoptera: Noctuidae). also
used visual cues to associate the host plant cotton, Gossypium hirsutum L., with the
location of its host larvae, frass and damaged leaf (McAuslane et al. 1991).

The effect of very low light intensity in the center of the woodland on D. insulare's
response to the visual cues may partly explains why there was no parasitism when
diamondback moth larvae were placed in the center of the woodland but 40 to 79%
parasitism along the woodland edge (Fig. 4). Other factors including temperature, relative
humidity, wind and odors may also involve. This result also indicates that woodland
center was not a preferred habitat for D. insulare. In Indonesia, however, Hymenoptera
parasitica were found more inside than along the woodland edge (Noyes 1989).

The percent parasitism in corn, tomato, bean, and apple habitats was consistently
high (55 to 80%) for all sampling dates except in apple on 12-13 August 1994, compared
with alfalfa (10 to 40%), woodland edge (3 to 80%) and weedy areas (20-69%) where

107
parasitism was highly variable (Fig. 2, 3 A to C & 4). This suggests that the former crop
habitats are preferred by D. insulare. Probably, they are the better habitat for optimum
parasitism and other D. insulare activity such as food finding. There may be altemate hosts
for D. insulare in one or more of the other "preferred crop habitats". Other diamondback
moth parasitoids, D. semiclausum and Diadegma fenestrale (Holrngren) (Hymenoptera:
Ichneumonidae). use some tortricids of apples as their alternate host for overwintering
(Hardy 1938). The parasitism of diamondback moth larvae in these crops may also depend
on the D. insulare entering the habitat after the placement of the larvae.

Parasitism in the woodland edge was highly variable at least in part because of the
variability in this habitat. In August 1992 and 1993 when parasitism was high, D. carota,
one of the best wildflowers for nectar for D. insulare females (Chapter 1), was at peak
flowering. In contrast, in July or September 1993, D. carota had just begun to flower or
started to decline. In August 1994, however, D. carota was less abundant than in 1992 and
1993. The low number of D. insulare present, as indicated by the numbers of parasitoids
caught on the sticky traps (Table 1), in woodland edge with few or no D. carota and
dependency on the D. insulare entering this area after diamondback moth larvae was
introduced may explain why the parasitism was low. A cloudy day on the sampling date
may also have caused caused lower parasitism in August 1994 than in 1992 or 1993, partly
sunny or sunny days. The presence of shrubs in the woodland edge, which likely has
fewer D. insulare than in the woodland edge with D. carota (T able 1), will further reduce
the light intensity, disrupt D. insulare visual cues and parasitism rate during the cloudy day.

Parasitism in weedy areas was also highly variable probably due to habitat
variability. The weedy areas used for study in August 1992 (Fig. 2) had 50 to 70% D.
carota . In July and August 1993, only one replicate had a density of D. carota similar to
August 1992 (Fig. 2, 3 A & B). The other replicates had no D. carota but Asteraceae
weeds+grasses, Asteraceae weeds+A. repen s or primarily A. repens. Percent parasitism

was higher in August 1992 than on July and August 1993, indicating that diamondback

108
moth larvae placed in weedy areas with D. carota were parasitized more by D. insulare than
in the weedy areas with less or no D. carota. (Fig. 2, 3 A & B). In July and August 1993,
percent parasitism ranged from 10% in the replicate with A. repens to 75% in replicate with
50 to 70 % D. carota. This variability is shown by the high standard error of the mean for
percent parasitism (Fig. 3 A & B). The numbers of D. insulare caught on the sticky traps
placed among the weedy areas differed significantly (Table 1). This explains why the
parasitism is highly variable and very low in areas with primarily Asteraceae+grasses or A.
repens. Besides no food or less food available in the latter areas there also may be no
alternate hosts of D. insulare.

Variability in environmental factors, especially light intensity and temperature, and
habitats' compositions per unit time (months and years) determine the D. insulare activity
and its parasitism rate (Fig. 5 A & B). Fluctuation in day temperature, light intensity and
wind speed influenced the diurnal foraging activity of D. insulare (Chapter 3). The
changes in value of particular habitats for D. insulare over time, habitat's composition, the
presence of wildflowers and overshadows vegetation affected parasitism rate. Apantales
glomeratus 1L. (Hymenoptera: Braconidae) responds similarly to D. insulare; A. glomeratus
female host habitat location is disrupted by overshadowing vegetation on the host plant
causing low parasitism of Pierr's rapae L. (Sato & Ohsaki 1987). These results suggest that
certain habitats are suitable for D. insulare parasitism activity. However, their suitability is
subject to the interaction between those particular habitats and the environmental
conditions.

The distance of treatments from the corn field edge into the field significantly
influenced the parasitism rate (Fig. 6). Parasitism by D. insulare significantly decreased as
the distance of ueatments from the corn field edge increased. This indicates that com field
is not a prefened habitat for D. insulare. Probably, there was no alternate host for D.
insulare in the corn field, but. its presence may be associated with food finding activity or

temporary stay during the hotter time of the day. The need of shelter is also indicated by

' 109
the higher numbers of D. insulare caught along the woodland edge than in the weedy areas
even though both habitats had high percent of D. carota present (Table 1). In another
study, F1 generation of Eriborus terebrans (Gravenhost)(Hymenoptera: Ichneumonidae). a
parasitoid of the European corn borer, has no preference between the edge and in the
middle of corn field (Dyer & Landis 1993).

D. insulare was present in many habitat types even though parasitism may not
occur. and it is actively mobile in the heterogeneous habitats. In view of this fact, there
will be a potential for manipulation of present Brassica crop field design or planting
Brassica crops in polyculture system without affecting the role of D. insrrlare as a
biocontrol agent of diamondback moth.

Results of these study showed that tomato plants had no adverse effect on D.
insulare parasitism rate. The parasitism rate of diamondback moth by Cotesia pluteIIae
(Kurdjumov) (Hymenoptera: Braconidae), another important larval parasitoid of
diamondback moth, was also not affected by the presence of tomato plants in Brassica
crops field in Hawaii (Bach & Tabashnik 1990). However, tomato plants are reported to
adversely affect the long range host finding by adult diamondback moth, probably due to
the volatile compounds emitted by the tomato plants (Buranday & Raros 1975). This
indirectly reduces the numbers of larvae and pupae per plant especially during the first 60 d
after Brassica crops are transplanted to the field (T alekar et al. 1986). Therefore, tomato
plants can be interplanted with Brassica crops.

Polyculture systems restrict natural enemies movement and they could become less
effective biocontrol agents (Sheehan 1986. Andow & Prokrym 1990). However, Talekar
& Yang (1991) reported that the parasitism rate of diamondback moth larvae by D.
semiclausum in Brassica planted in polyculture (soybean, eggplant, com, sweet potato.
garden pea, tomato, garlic, okra and Brassica crops) was not different from parasitism in
the monoculture Brassica crops. Result of my study also showed that com, bean, and

apple habitats have the potential to be interplanted with Brassica crops in polyculture

110
systems. The com and apple habitats could also provide refuges for D. insulare during the
hottest time in the day.

Horn (1987) reported that parasitism of diamondback moth larvae by D. r'nsulare is
lower in the non-tilled than in the tilled (weed-free) Brassica crop field. However, the
presence of D. carota within any habitat can harbor D. insulare (Table 1), serves as nectar
source (Chapter 1), and increases parasitism rate (Fig. 2 to 4). Results also indicate that
the Brassicaceae weeds (B. kaber, B. nigra and R. raphanistrum) attract high numbers of
D. insular-e (Table 2). B. kaber and D. carota can be excellent nectar sources for D.
insulare (Chapter 1). As such, these weeds could be interplanted within Brassica crop
fields in a patch, between Brassica crop rows or around the field. Wild Brassica, Brassica
nigra L. (Indian mustard), planted in one row per 15 rows of Brassica crops has been used
as a trap crop in integrated diamondback moth management in India (Srinivasan & Krishna
Moorthy 1991). The techniques of interplanting wild Brassicaceae or other non—
Brassicaceae with Brassica crops may depend on the size of the field. I suggest that if the
Brassica field is >10 ha then a patch or into-row planting of wild Brassicaceae or other non-
Brassr'ca plants with the Brassica crop may favor parasitoid activity. D. insulare and
probably other parasitoids of diamondback moth may be more abundant at the field edge
that normally provide plenty of food to the parasitoid than in the interior field. However,
the effect of field edge and size to the D. insulare population abundance, activity and

parasitism rate need to be studied.
CONCLUSIONS
The integration of factors that could optimize the impact of D. insulare to conuol

diamondback moth should be emphasized in the Brassica crops ecosystem management.

However, it could only be achieved with intelligent modification of the current field

111

agroecosystem and/or field setting within any particular landscape. By doing so, the

impact of other biocontrol agents on diamondback moth could also be increased.

CHAPTER 6

Effects of Wild and Cultivated Host Plants on Oviposition, Survival and
Development of Diamondback Moth (Lepidoptera: Plutellidae) and Its

Parasitoid, Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae)

112

113

ABSTRACT

I studied the effects of wild and cultivated host plants on diamondback moth,
Plutella xylostella L., oviposition, egg hatch, larval survival, infestation level, parasitism
rate by Diadegma insulare (Cresson), and the developmental tim'e and sex ratio of D.
insulare. Egg laying was highest on the cultivated varieties, especially broccoli, and lowest
on wild spp., especially Berteroa incana L. DC. and Erysimum cheiranthoides L. Egg
laying was generally higher on leaves of cultivated Brassica plants from the field than on
leaves from the greenhouse. The reverse was true for leaves of wild species. Percent egg
hatch was not significantly different among host plants. Percent diamondback moth larval
survival was generally higher on the cultivated varieties than on wild species and there was
no survival on Barbarea vulgaris R. Br. Developmental time of diamondback moth larvae
was generally longer on the wild spp. than on the cultivated varieties. Percent parasitism
by D. insulare was lowest on B. incana, Lepidium campestre R. Br. and E.
cheiranthoides. Percent parasitism was higher when diamondback moth larvae fed on B.
kaber than on the cultivated varieties. Parasitized diamondback moth larvae fed E.
cheiranthoides, T. arvense and B. incana took significantly longer to develop to D. insulare
pupae than when fed on the other Brassica varieties or species. Diamondback moth
infestation and percent parasitism in the field were higher on broccoli than on the other
crops. The distribution of D. insulare females was not significantly different among the
crops. The presence of wild Brassicaceae, especially B. vulgaris and B. kaber, in the field
could reduce diamondback moth populations, the impact of D. insulare, and increase the

success of diamondback moth management programs.

114

INTRODUCTION

Diamondback moth. Plutella xylostella L.(Lepidoptera: Plutellidae), is an important
pest of Brassica crops worldwide. Diamondback moth is also found on many wild
Brassicaceae (Marsh 1917, Thorsteinson 1953, Harcourt 1986). 'It is a multivoltine insect
with 4 to 17 generations per year in temperate and tropical regions, respectively (Harcourt
1986, Chelliah & Srinivasan 1986). The abundance of host plants and the action of its
natural enemies are two keys biotic factors that regulate diamondback moth populations
(Harcourt 1986, Fox et al. 1990, Ooi 1992).

The volatile compounds released by host and non-host plants attract or deter
diamondback moth oviposition (Palaniswamy & Gillott 1986, Dover 1986, Reed et al.
1989, Raddiff & Chapman 1966). Extracts of a wild Brassica sp., Elysimum
cheiranrhoides L., also deterred oviposition by Pierr's rapae L. (Lepidoptera: Peiridae)
(Dirnosk & Renwick 1991). Diamondback moth larval survival can be affected by toxic
substances, lack of feeding stimulant in the host, and the morphological characteristics of
the host plants' leaves (Eigenbrode & Shelton 1992, Hough-Goldstein & Hahn 1992,
Gupta & Thorsteinson 1960a & b). Some of these compounds have been isolated and
identified from several host and non-host plants (Cole 1976, Reed et al. 1989, Pivnick et
al. 1994).

Tumlinson et al. (1993) reported that, besides recognizing odors from their host,
parasitic wasps and flies also learn to identify compounds released by the plant on which
the hosts feed. Eucelatoria bryani Sabrosky (Diptera: Tachinidae), a parasitoid of
Helicoverpa spp., responds only to fresh plant tissues and not to the extracts tested (Martin

et al. 1989). Volatile compounds released by plants affect host location and parasitism rate

115
by the braconid wasps Microplitis croceipes Cresson, Cotesia marginiventris Cresson,
Macrocentrus grandii Goidarich and Cotesia glomerata L. (Steinberg et al. 1992, Udayagiri
& Jones 1992, Turlings et al. 1990, McCall et al. 1993). Host plants also indirectly affect
parasitoid development (McDougall et al. 1988, Ritter & Johnson 1991, McCucheon et al.
1991, Bentz & Barbosa 1990, Werren et al. 1992, Bloem & Duffey 1990, Riggin et al.
1992, Campos et al. 1990), flight behavior (McAuslane et al. 1990a) and movement
(Keller 1987).

As a specialist parasitoid we expect Diadegma insulare (Cresson)(Hymenoptera:
Ichneumonidae) to rely more on host related cues than do generalist parasitoids. If so, its
parasitism may occur only when diamondback moth larvae are feeding on certain plants or
plant materials. Diaeretiella rapae M'Intosh, a specialist parasitoid of aphids, is attracted to
collard leaves and allylisothiocyanate (mustard oil) found in the collard leaves (Read et al.
1970). To the best of our knowledge there are no studies about the effects of host plant
species on the interaction between diamondback moth and D. insulare. This tritropic
interaction is important to be understood for more effective integrated diamondback moth
management.

The objectives of this study were to find out the effects of several cultivated and
wild Brassicaceae on (1) diamondback moth oviposition, percent egg hatch, larval survival,
and developmental time; (2) parasitism rate. developmental time of parasitized larvae and
the sex ratio of D. insulare and; (3) in the field, the level of diamondback moth infestation

in the field, disuibution of D. insulare and percent parasitism.

MATERIALS AND METHODS

Insects and Food Plant sources. The diamondback moths used were strain, G88

F97 (provided by Anthony Shelton, Cornell University, New York Agriculture Experiment

Station, Geneva). It has been reared in the laboratory on broccoli, Brassica oleracea L. l

116

used a laboratory colony (F10) of D. insulare collected from the Michigan State University
Collins Road Entomology Research Field in 1993 for parasitism experiments.

Host plants used were five cultivated varieties and nine wild Brassicaceae (Table 1).
The leaves of wild Brassicaceae were collected from the Michigan State University
Research Farm and other places on the Michigan State University campus. To maintain the
freshness of the detached leaves they were put in clear zip lock plastic bags and kept inside
a cooler with ice, returned to the laboratory and kept in refrigerator. The host plants were
also raised in the greenhouse for an experiment to compare the effect of field and
greenhouse plants on diamondback moth oviposition.

Diamondback moth studies. Qumsitioh. WW. Choice
tests were used to study oviposition by diamondback moth on field collected leaves from
various hosts and compare oviposition on leaves from field and greenhouse plants. I used
14.5 cm diam Petri dishes with an 8.0 cm diam screen opening in the lid. To study
oviposition on different field collected leaves, 1 cut 2 cm2 of the leaf and randomly put
them on moist filter paper around the edge inside the Petri dish ( 1.0 cm from the dish edge
and 4.5 cm from the center, and 1.5 cm between the leaves). To compare oviposition on
leaves collected from field and greenhouse plants, 2 cm2 pieces of each were placed
opposite to each other, 4.0 cm from the center of the Peui dish.

One 2 (1 old mated diamondback moth female was released at the center of dish.
For easy handling the individual moth was put inside a glass vial (21 x 70 mm) plugged
with cotton wick and put in the freezer for 3 min before release. The dishes were randomly
placed 60 cm under white florescent light (Philipm, FI‘2T12/CW/VHG, 160 Watt) and
kept at 25 i 2°C. Treatments were replicates four times. Eggs laid were recorded after 4 h
of oviposition.

I followed similar procedures of choice test for no-choice tests except three leaf
pieces of a single host species were put around the edge of each Petri dish, 4.0 cm from the

dish center.

117

Table 1. Species and common names of host plants used in the study

 

Species

Common names

 

g :ttltivated
Brassica oleracea L. var. italica cv. Green Comet
B. oleracea L. var. acephala cv. Nagoya Mix
B. oleracea L. var. bonytis cv. Early snowball "A"
B. oleracea L. var. capitata cv. Early Great Dutch
B. oleracea L. var. capitata cv. Ruby Ball
B. napus L.
Wild
B. kaber D. C. Wheeler
B. nigra L. Koch
Berteroa incana L. DC.
Erysimum cheiranthoides L.
Capsella bursa-pastoris (L.) Medic
Barbarea vulgaris R. Br.
Lepidium campestre (L.) R. Br.
Raphanus raphanistrum L.
Thlaspi arvense L.

Broccoli
Flowering kale
Cauliflower
Green cabbage
Red cabbage
Canola

Wild mustard
Black mustard
Hoary alyssum
Worrnseed mustard
Shepard's purse
Yellow rocket
Field pepperweed
Wild radish

Field pennycress

 

l 18
W. I took 50 eggs per replicate per plant species or variety from

choice and no-choice test to measure the percent egg hatch. The eggs laid on a particular
plant species or variety were placed on a new fresh leaf of the same plant in a similar Petri
dish as before. More than one leaf was used if necessary to have at least 5 cm2 per dish.
Leaves were replaced with fresh ones after 12 to 15 h. Leaves and eggs were kept in the
growth chamber (23 i 2°C. 50 - 75% relative humidity (RH) and a photo period 16 : 8 h
(L: D) h for 4 d and the numbers of eggs hatched were recorded.

Bereent larva survival and develepmental time t9 papatie'n. Diamondback moth
eggs were collected from each host plant (100 eggs per variety or species) and reared
following the no-choice test above except I put three to five diamondback moth females per
dish to get more eggs and larvae. I randomly selected 40 newly hatched first instars (ten
per replicate) to study larval survival from hatch through second and third through fourth
instars. The surviving second instars were used for accessing the survivorship from third
through fourth instars. Five newly hatched first instars were used to study the
developmental time from hatch through pupation (= five replicates, one larvae per replicate
per host plant). Larvae for each experiment were placed in a similar type of Petri dish as
above and kept as above. Larvae were fed with leaf of the respective host-plants and leaves
were replaced with fresh ones as above. Treatments (host plant + larvae) were kept as
before. Numbers of surviving larvae at the end of second and fourth instars, and the time
(day) of pupae formed were recorded.

Diadegma insulare studies. W. A clear plastic container (12.0 cm
and 8.0 cm diam top and bottom, respectively, and 10.0 cm high with 5.0 cm diam screen
Opening lid on top and two 1.5 cm screened openings on the sides of the container) was
used. One cross cut was made on one side of the container for easy release and taking out
the parasitoid. A 2 cm2 piece of damaged leaf and 30-33 diamondback moth early third
instars were put together in one plastic container. A mated and experienced 3 (1 old D.

insulare female was released into the container using an aspirator and placed under white

119
inflorescent light (as in Chapter 2) at 25 :t 3°C for parasitism by D. insulare for 3 h after
which the parasitoid was removed. Parasitized larvae were fed with leaves of the
respective host plant until pupation. The number of D. insulare pupae and diamondback
moth pupae formed were recorded.

WWW. To study the developmental time of
parasitized larvae I used similar methods as for parasitism but only five early third instar
from each host plant were exposed to D. insulare females (to make sure all larvae are
parasitized). One larva. parasitized or unparasitized, was put inside the modified 14.5 cm
diam Petri dish and fed as above until pupation. Time (day) of pupation of each parasitized
and unparasitized larvae was recorded and treatments (= five larvae per treatment) were
replicated four times.

fl he sea rage at D, insalgre, I randomly selected seven D. insulare pupae per
replicate from the above experiment and put them in plastic container (= 35 pupae per host
plant per container) and kept as before until adult emergence. D. insulare sexes were
recorded on the day of emergence.

Numbers of eggs laid, percent egg hatch and larva survival from hatch to second
and third to fourth instars, developmental times of unparasitized and parasitized larvae, and
percent parasitism were analyzed using 1-way ANOVA and means were separated by
Fisher's Protected LSD (Abacus Concept, SuperAnova 1991). The numbers of eggs laid
on leaves collected from field and greenhouse were analyzed by 2-way ANOVA and
whenever the main effects were significant means were separated as before (Abacus
Concept, SuperAnova 1991). The sex ratio was analyzed using X2 and the lowest sex ratio
as the expected value. The relationship between developmental time of parasitized and
unparasitized larvae for each host plant was analyzed using regression analysis (Abacus

Concept, SuperAnova 1991).

120

Field studies on diamondback moth infestation, parasitism rate and
distribution of D. insulare adults. This experiment was conducted at the Michigan
State University Collins Road Entomology Research Field in the summer of 1994. Plots
were 7.0 x 7.0 m with 1.5 m between plots and 0.6 m between plants (100 plants per
plots). Plots were arranged as a randomized block design with four replicates per
treatment. The treatments were cultivated varieties of Brassica; kale, red cabbage, green
cabbage, cauliflower and broccoli (Table l). Transplant fertilizer 16:16:16 was broadcast
before transplanting. Two month-old plants were hand-transplanted on 14 and 15 July

1994. To keep plots free from any pesticide treatment weeds were hand-pulled and hoed

weekly.
Diamendhaek math lamae ahd D, t'nsalgre pupae. The numbers of diamondback

moth small larvae (first and second instars) and large larvae (third and fourth instars), and
D. insulare pupae were sampled on randomly chosen plants (10 per replicate) on 15 and 25
August and 3 September.

Bespeptparasitism. I collected five second to fourth diamondback moth instars per
replicate from non-sampled plants. to measure parasitism. Larvae were brought to
laboratory, fed on the same host leaves collected from the same plots and kept as above
until pupation.

WWW. To assess the distribution of D. insulare adults
in the experimental plots I walked along the rows of each replicate and caught the
parasitoids using a sweep net, hourly (1100 to 1600 h, EDT) on 17 and 25 August. D.
insulare adults caught were identified, sexed, recorded and released.

Percent parasitism was calculated as the number of D. insulare pupae divided by the
total numbers of D. insulare + diamondback moth pupae x 100 (Idris & Grafius 1993b).
Data were transformed using log(1 + x)(for numbers of larvae) or arcsin w/K (for percent
parasitism) before analysis. Numbers of small and large larvae, and D. insulare adults

caught, and percent parasitism were analyzed using 2-way ANOVA and, whenever mains

121

effects were significant and interaction between factors was not significant, means were

separated by Fisher's Protected LSD (Abacus Concept, SuperAnova 1991).

RESULTS AND DISCUSSION

Diamondback moth studies. Qvipesition. The numbers of eggs laid per host were
significantly different among the host plants both in choice tests (F = 14. 23; df = 10, 30; P
< 0.05) and no-choice tests (F = 9.81; df = 11, 33; P < 0.05)(Fig. 1A & B). In choice
tests, diamondback moths laid significantly more eggs on broccoli than on the other host
plants except canola (FPLSD, P < 0.05)(Fig. 1A). Numbers of eggs laid on canola
(cultivated) were not significantly different from numbers on B. kaber, L. campestre or T.
arvense (wild)(FPLSD, P < 0.05). In no—choice tests, there were no significantly
differences in numbers of eggs laid on broccoli. canola. cauliflower, B. kaber, B. nigra or
T. arvense. Diamondback moths laid significantly fewer eggs on E. cheiranthoides and B.
incana than on the other wild species (FPLSD, P < 0.05)(Fig. 1B). The genus Brassica
included both the most preferred and least prefened host plants for diamondback moth in
the choice tests and plants with the lowest and highest egg laying, in the no-choice test.

Glucosinolates (mustard oils), commonly found in Brassicaceae plants, are the
major oviposition stimulant for diamondback moth (Reed et al. 1989). Upon hydrolysis,
glucosinolates give rise to different isothiocyanates depending on the Brassicaceae spp. or
varieties. Different glucosinolates or similar glucosinolates with different concentrations
have been identified in host (Brassicaceae) and nonhost plants (Cole 1976, Wallbank &
Wheatley 1976). Recently, certain volatiles that are not a kind of glucosinolates from B.
juncea and B. napus were found to be important in host-plant finding by diamondback
moth (Pivnick et a1. 1994). These secondary chemicals may explain the differences in
preference and in the number of eggs laid by diamondback moth among the host plants in

my study. For example, numbers of eggs laid were always highest on broccoli both in

                      

usumefieeaefi .m

.m

.3333; .m
Mohegan .4
ESEEEE U

329:: g

122

A. Choice test

Em? .m
e33 .m
32:6

505050
”2211

mm H a v .2 case .3 wwwm

       

 

; m§§=2§9 .m
385 .m
Sanguine .x
2.53:; .m
2.85:3 .4

“tenaeré .9

choice test

.No

B

 

 

m w w w w 0
mfifiavbaufifiasnmwwm

Figure 1. Numbers of eggs laid by diamondback moth females on Brassica
plants in choice (A) and no-choice (B) test. Bars with different letters are

significantly different (Fisher's Protected LSD, P < 0.05).

123
choice or no-choice situations (Fig. 1 A & B), indicating it has chemicals that attracted
diamondback moth to lay more eggs than on the other host plants.

Diamondback moth laid fewer eggs on B. vulgaris than on B. nigra, T. arvense, L~
campestre or C. bursa-pastoris in choice tests, but, in no-choice tests the numbers of eggs
laid on these species were not significantly different (Fig. 1 A & B). In no-choice tests,
which simulate early spring situations where B. vulgaris is more abundant than other
species, B. vulgarr's is very acceptable for oviposition (Fig. l B)(Reed et al. 1989).
Diamondback moth do not discriminate between different types bf glucosinolates (Reed et
a1. 1989). B. incana or E. cheiranthoides may have lower concentration of glucosinolates
and other water-soluble compounds (Renwick & Radke 1988) that attract fewer moths to
lay eggs (Fig. l A & B). B. incana and E. cheiranthoides may also have oviposition
deterrents which may outweigh the attractants. Similarly, deterrents (cardenolides) appear
to outweigh the attractants (glucosinolates) for oviposition by P. rapae on E. cher'ranthoides
(Renwick & Radke 1987, Renwick et al. 1989).

The numbers of diamondback moth eggs laid were significantly different among
host plants (F = 24.5. df = 10 & 66, P < 0.05), but not between host plant leaf collection
(field versus greenhouse)(F = 0.13. df = 1 & 66, P > 0.05). Numbers of diamondback
moth eggs were significantly affected by the interactions between the host plants and their
leaf collection (F = 6.7, (if = 10 & 66, P < 0.05)(Fig. 2 A & B). Diamondback moth laid
more eggs on the field leaves than on the greenhouse leaves of the Brassica crop varieties,
except for canola (FPLSD, P < 0.05)(Fig. 2 A). In contrast, eggs were laid more on the
greenhouse leaves of wild species except for B. kaber. This may due to chemicals or
physical structures of a particular host plant (Gupta & Thorsteinson 1960b).

EereenLegghateh. Percent egg hatch was not significantly different among host
plants (F = 1.73; df = 14, 42; P > 0.05). However, in a previous study percent egg hatch
was significantly lower on B. vulgaris than on T. arvense, C. bursa-pastoris or broccoli

(Idris & Grafius 1994). This contrasting result may due to the difference in diamondback

Eggs per female i S.E

50

20

50

10

124

 

I

 

 

 

""*‘ " Broccoli
—°"— Cauliflower

- — D "' ‘ Green cabbage
Red cabbage

' Kale

Canola

 

 

 

 

 

 

Field Greenhouse

B. Wild species

 

ll

 

 

—°— B. kaber

 

"""" Tianense
—0_ B. vulgar-is
""0"" B. incana

“'_'— E. cheimnthor‘des

 

 

 

 

 

 

 

 

 

1

Field Greenhouse

Leaves

Figure 2. Numbers of eggs laid by diamondback moth on
field and greenhouse leaves of Brassica crops cultivars (A) and
Wild specres (B).

125
moth strain and method used. In this study, leaves were provided better aeration through a
screened Opening on the top of the Petri dish as compared with no screen in the study
conducted by Idris & Grafius (1994). In the field, however, percent egg hatch may be
affected by the density of the plants per unit area. In dense plant populations there may be
higher concentration of plant volatiles within the canopy that could be lethal to the
deve10ping eggs as indicated by the detached leaf experiment in Petri dishes (Idris &
Grafius 1994).

Pereent larva surviva l and developmental time to papatien. Percent of diamondback
moth larva surviving from hatch through second instar (F = 31.96; df = 14, 42; P < 0.001)
and third through fourth instars (F = 23.71; df = 14, 42; P < 0.001), and larval
developmental time from hatch to pupation (F = 14.82; df = 13, 39; P < 0.001) were
significantly different among the host plants (Fig. 3 A, B & C). Percent survival from
hatch through second instar was highest when larvae were fed on the cauliflower, but not
significantly different from survival on broccoli or kale (FPLSD, P > 0.05)(Fig. 3 A).
Survival rate was lower on red cabbage than on the other Brassica crop varieties (Fig. 3 A
& B). Generally, larval survival rate was higher when fed on the Brassica crop varieties
than on the wild species. Of the nine wild species tested, larval survival was lowest when
fed on B. vulgaris and B. incana (Fig. 3 A & B).

An autolysis of 79 Brassicaceae and two related species indicated that 4—
methylthiobutyl thiocyanate and 2-Hydroxy—2-phenylpropionitrile are found only in B.
incana and B. vulgaris, respectively (Cole 1976). These two compounds may be toxic or
feeding inhibitors to diamondback moth larvae. Thorsteinson (1953) reported that
diamondback moth larvae do not feed on leaves containing allyl isothiocyanate. I observed
that small larvae refused to feed and larger larvae initiated fewer feeding sites on B.
vulgaris before they died. In contrast, 52% of diamondback moth larvae (reared from field
collected populations) survived from hatch through second and 13% survived from third

through fourth instars when fed on B. vulgaris (Idris & Grafius 1994). This suggests

126

A. Percent survival (hatch through woond instar)

 

 

 

 

.2.m.w .I_.

 

B. Percent survival (third through fourth irstars)

 

_aztsm 282$

 

C. Developmental time (hatch to pupation)

 

 

Edd H
333 2:: 355225

 

Figure 3. Percent of larval survival from hatching through second

(A) and third through fourth (B) instars, and developmental time of
diamondback moth larvae from hatch to pupation (C) when larvae were fed

on various plants in no-choice test Bars with different letters are

significantly different (Fisher's Protected LSD, P < 0.05).

127

some field diamondback moth populations may be resistant to toxic compounds found in
B. vulgaris. In the current study I used diamondback moth (New York strain) that are
susceptible to most pesticides used to control diamondback moth. Whether resistance to B.
vulgaris is caused by the same mechanism as resistance to pesticides is not known.

There was no significantly difference in developmental time for diamondback moth
larvae fed on all Brassica crop varieties and three wild species (B. kaber, B. nigra and R.
raphanistrum)(FPLSD, P > 0.05)(Fig. 3 C). Similar results were reported when
diamondback moth larvae fed on other Brassicaceae crops (brocColi, cauliflower and
common cabbage)(AVRDC, 1987). Developmental time was significantly longer for larvae
fed on L campestre than on the Brassica crop varieties and other wild species (FPLSD, P
< 0.05)(Fig. 3 A & B). However, Idris & Grafius (1994) found that developmental times
of field collected diamondback moth larvae fed on wild species (T. arvense and C. bursa-
pastoris) were not different from those fed on the broccoli. L. campestre may have an
antifeedent that affected both the larva survival rate and developmental time. An antifeedent
prolonged developmental time of P. rapae larvae to pupation (Hough-Goldstein & Hann
1992). In contrast, B. incana, which severely reduced larval survival rate showed similar
effects as the other wild species on larval developmental time (Fig. 3 C).

D. insulare studies. Eereept parasitism. Parasitism of diamondback moth by D.
insulare ranged from 0 to 91.5% and was significantly different among host plants (F =
13.9, df = 12 & 36; P < 0.001)(T able 2). Parasitism of diamondback moth larvae fed on
B. kaber and B. nigra was as high as when diamondback moth larvae were fed on the
Brassica crop varieties; it was lowest when B. incana, L campestre or E. cheiranthoides
were used as food for the larvae. These differences might be even larger in the field
because diamondback moth larvae are exposed longer to parasitism in the field due to
longer developmental time, especially when fed on L. campesrre (Fig. 3C).

No parasitism occurred when C. bursa-pastoris was used as food for the

diamondback moth larvae. 1 observed that D. insulare females did not initiate searching

128

Table 2. Effect of host foods on percent parasitism, developmental time of

parasitized diamondback moth third instar, and sex ratio of D. insular-e

 

Percent parasitism

Developmental time

Female to Male

 

Brassica species (i S.E.) (days i S.E.) sex ratio
(female:male)1

Brassica kaber 91.5 i 3.8g 13.0 i 0.33 l : 2.5
Broccoli 90.8 i 2.21‘g 13.0 i 0.4a l : 2.3
Cauliflower 89.5 i 6.5fg 12.8 i 0.5a 1 : 3.3
Canola 87.3 i 5.6efg 12.9 i 0.5a 1 : 3.3
Kale 83.3 i 2.2defg 13.8 i 0.3a l : 3.1
B. nigra 81.3 i 4.9defg 13.1 i 0.5a 1 : 2.7
Red cabbage 79.5 i 3.4dcf 13.5 i 0.5a I : 3.6
Green cabbage 76.5 i 56ch 13.5 i 0.3a 1 : 3.4
R. raphanistrum 72.8 i 4.9cd 13.9 i 0.5a 1 : 3.8
E. cheiranthoides 65.5 i 5.2bc 15.8 i 0.3b l : 5.0
T. arvense 65.0 i 6.5bc 16.3 i' 0.3b 1 : 4.8
B. incana 55.0 i 6.5b 16.0 i 0.6b l : 7.5
L campestre _ 39.3 i 3.9a 20.3 i 2.2c l : 4.7
C. buma-pastorisz 0.0 - -

B. vulgaris3 -

 

1 The variation in D. insulare sex ratio was significantly different (X2 = 23.6, df = 12, P <

0.05)

2 Parasitism did not occur in 3 h exposure of the diamondback moth larvae to D. insulare

3 No diamondback moth larvae survived on B. vulgaris

129

behavior for diamondback moth larvae when C. bursa-pastoris was used to feed the
larvae. I also noticed that there was a delay in showing searching and oviposition behavior
by D. insulare when diamondback moth larvae were fed on L. campestre. Udayagiri &
Jones (1992) reported that Marocenrrus grandii Goidarich, a parasitoid of European corn
borer, showed host searching behavior only to European corn borer fed on certain plants.
In nature, D. insulare may also expected to respond differently with parasitoids' age,
previous experience and host plant morphology as reported for other parasitoids (Steinberg
et a1. 1992. McCall et al. 1993. Keller 1987). Although I was nor able to record parasitism
when diamondback moth larvae fed on B. vulgaris. I suspect parasitism could occur in

the field because some field-collected diamondback moth larvae survived on B. vulgaris in
another study (Idris & Grafius 1994).

Develepmental time. Time to develop to D. insulare pupa by the parasitized third
instar of diamondback moth was significantly longer on E. cheiranthoides, T. arvense and
B. incana than on the Brassica crop varieties and three other wild species (B. kaber, B.
nigra and R. rapham'strum (F = 19.7, df = 12 & 36, P = 0.001)(Table 2). There was a
positive correlation between time taken by parasitized and unparasitized larvae to form D.
insulare and diamondback moth pupae (Fig. 4). This indicates that the effects of food
plants on developmental time to pupation are similar for parasitized and unparasitized
diamondback moth larvae. McCutcheon et al. (1991) reported that pre-imaginal
development of Cotesr'a marginiventrr’s Cresson (Hymenoptera: Braconidae), a parasitoid of
soybean looper, Pseudolupsia includens Walker (Lepidoptera: Noctuidae), was severely
affected by the resistant line of soybeans (McCutcheon et al. 1991). However, effects of
host plants may be subject to the host insect's stage at the time of parasitism because
different host's stages may be affected differently. For Helicoverpa zea (Boddie) larvae.
the variation in host sterol composition in larvae affects the growth and development of its
parasitoid, Microplitis demoliror Wilkinson (Hymenoptera: Braconidae) (Ritter & Johnson

1991). Developmental time of Eriborus terebrans (Gravemhost) to pupation is affected by

Developmental time (days) of parasitized

diamondback moth larvae

22

18

14

10

130

 

 

Y = 4.37 + 0.82X; r = 0.79; F : 81.9;
df=l,50;n=52;p=0.001 .

 

 

 

 

 

 

 

 

I ‘ I ' I ' I ' I ' I

10 12 14 16 18 20 22

Developmental time (days) of
unparasitized diamondback moth larvae

Figure 4. Relationship between developmental time of parasitized

and unparasitizeed diamondback moth larvae fed on various host plants.

ll

 

 

 

 

 

 

 

 

131

a- tertienyl, one of the secondary chemicals that affect European corn borer larval
development (McDougall et al. 1988).

Q, insular-a sex Latip. Female to male sex ratio of D. insulare ranged from 1: 2.3 to
l: 7.5 and was significantly different among the host plants (Table 2). There were more
females produced when diamondback moth larvae were fed on the cultivated varieties than
on the wild species except for B. kaber. B. m’gra and R. mphanisrrum. Female to male
sex ratio of D. insulare fed on broccoli was between 1: 1.7 to 1: 2.5 (Idris & Grafius
1993b) agreeing with my present result (Table 2). In another study, higher proportions of
female D. insulare emerged from diamondback moth larvae fed on leaves of high N-
fertilized than on the low N-fertilized collards (Fox et al. 1990). Percent female
Comperrr'ella bifacr'area Howard (Hymenoptera: Encyctidae) produced was 45% and 84%
when its host reared on valencia orange (C itrus sinensr's Osbeck) and yucca (Yucca

filipendula Baker) plants, respectively (Smith 1957).

Field studies. Level of diamondback moth infestation in the field,
distribution of D. insulare and parasitism. The numbers of small larvae (F = 3.9,
df = 4 & 45, P <, 0.05), large larvae (F = 9.3, (if = 4 & 45, P < 0.05) and total larval
counts per plant (F = 9.3. df = 4 & 45. P < 0.05) were significantly different among crops
(Brassica cultivars). Numbers of small larvae on broccoli and green cabbage were
significantly higher than on cauliflower, kale or red cabbage (FPLSD, P < 0.05)(Fig. 5 A).
There were significantly more large larvae and total larvae on broccoli than on the other
crops (FPLSD, P < 0.05)(Fig. 5 A, B & C). My results disagree with the report of Lasota
& Kok (1986) where numbers of larvae on kale were as high as on broccoli or cauliflower.
This contrasting result may due to the difference of Brassica cultivars used as reported by
Lin et al. (1983) and Eigenbrode et al. (1990). Although diamondback moth in the field
study were not reared on broccoli (unlike the laboratory strain), broccoli was the most

common Brassica crop at this site for the past ten years.

 

 

 

 

 

 

 

 

CTotal larvae

Larvae per plant i S.E.M.

 

 

Kale

Percent parasitism i S.E.M.
c 8 8 8 8

E
U
E?
a

Green cabbage
Red cabbage

Figure 5. Distribution patterns of diamondback moth small (first—
second instars)(A) and large larvae (third-fourth instars)(B), total larvae
counts (C), and percent parasitism of the diamondback moth larvae by
Dinsulare (D) on different Brassica crops. Bars with different letters

are significantly different (Fisher's Protected LSD, P < 0.05).

133

Numbers of small larvae per plant on three different dates were not significantly
different (F = 0.3, df = 2 &45. P = 0.560). However, numbers of large larvae (F = 7.6,
df= df = 2 & 45, P = 0.001) and total larvae (F = 4.0, df = 2 & 45. P = 0.001) were
significantly different among the dates and were higher on 25 August and 3 September than
on 7 July. A similar trend was also shown by the numbers of small larvae although
differences were not significant.

The interaction between Brassica variety and sampling date did not influence the
numbers of small larvae (F = 0.8, (if = 8 & 45, P = 0.453), large larvae (F = 1.7. df = 8 &
45, P = 0.635) or total larvae (F = 0.3. df = 4 & 45, P = 0.731) per plant.

Percent parasitism of diamondback moth by D. insulare was significantly affected
by crop (F = 2.7, df = 4 & 45, P = 0.021) and sampling dates (F = 4.2. df = 2 & 45, P =
0.006) but not by the interaction between these two factors (F = 0.2, df = 8 & 45, P =
0.673). Parasitism rate was significantly higher on broccoli (87%) than on green (53%) or
red (63%) cabbage (FPLSD, P < 0.05)(Fig. 5 D). In contrast, parasitism of diamondback
moth by Diadegma semiclausum (Hellen) (Hymenoptera: Ichneumonidae) was highest on
cabbage, followed by Chinese cabbage, cauliflower and broccoli (Talekar & Yang 1991).
Percent parasitism of diamondback moth by D. insulare (= insularis) on Abbott and Cobb #
five Brassica cultivars was significantly higher even though the diamondback moth
infestation was higher on other cultivars (Lasota & Kok 1986). My results showed that
this was not necessarily true because the total larval count on kale was lower than on the
broccoli, but the parasitism rate on these two varieties was similar (Fig. 5 C & D). This
suggests D. insulare is a good host searcher regardless of plant's leaf structure (kale leaves
are much more curly than broccoli leaves). Percent parasitism over the dates showed
similar trend as for the numbers of large diamondback moth larvae or total larvae.

Numbers of D. insulare males, females and total catch per trap were not
significantly different among crops (F = 1.1, males; 1.4, female; 1.7. total; df = 4 & 30, P
= 0.432) or sampling dates (F = 2.9, males; 0.9, female; 2.5. total; df = l & 30. P =

134
0.353). The interaction between crops and sampling dates did not significantly influence
the numbers of D. insulare males, females or total (males plus females) caught per trap (F =
0.2,male; 0.1, female; 0.1, total; df = 4 & 30; P = 0.647). This indicates that the
parasitoid was evenly distributed in field and apparently not affected by the volatiles
released by the different crops. Diadegma may aggregate on plants with higher host
numbers (Waage 1983. Chapter 3). However. in this study. numbers of D. insulate
females caught per trap in broccoli were not significantly different from catch in the other
crops even though the total larvae counts were significantly higher on the broccoli than on
the other crops (Fig. 5 C). This may due to the low diamondback moth larval population
density in the field during my study.

Results of my field study indicate that choosing the right Brassica cultivar could
suppress diamondback moth infestation. Although percent parasitism was always higher
on broccoli than some of the other crops. broccoli also supported high number of
diamondback moth larvae (Fig. 5). Low numbers of diamondback moth larvae on red
cabbage supported my laboratory results which indicate the low numbers of larvae
surviving to pupation on red cabbage (Fig. 3 A & B; Fig. 5). Low percent parasitism
appears to be a disadvantage of selecting red cabbage for planting.

Use of wild Brassica spp. in diamondback moth management. Results of
my laboratory study and a previous report (Idris & Grafius 1994) suggest that an
augmentation of B. vulgaris could reduce diamondback moth infestation early in the
season. B. vulgaris seeds can be sown in the field or nearby before winter. They
germinate in late April in the northern US. and the plants will be abundant in May and
early June before planting of mid-to late-season Brassica crops. My no—choice test results,
which may simulate an early spring situation, indicated that diamondback moth laid as
many eggs on B. vulgaris as on the cultivated crops. cauliflower and canola but no larvae
survived to second instar. Any larvae that might survive on B. vulgaris may be parasitized

by D. insulare or sprayed with selective pesticide such as Bacillus thuringiensis var.

135
kurstaki Berliner without disrupting biological control of D. insulare. Alternatively, B.
vulgaris could be killed by cultivation or herbicides before diamondback moth larvae
mature. These tactics will reduce diamondback moth populations before the cropping
season begins. Besides acting as a trap crop for diamondback moth, B. vulgaris also
serves as excellent nectar source for D. insulare adults (Chapter 1). The presence of B.
vulgaris may attract high numbers of D. insulare to stay longer around the field and
increase parasitism rate. B. vulgaris could also act as refuge for diamondback moths
susceptible to insecticides and aid in insecticide-resistance management of diamondback
moth.

L campestre and B. incana significantly prolonged larva development and caused
high mortality to diamondback moth larvae. They could be intersown before winter or
sown in May next to B. vulgaris. These weeds could be used as a trap crop after B.
vulgaris is gone in June. Although B. incana and L campestre are early season weeds like
B. vulgaris, they grow and continue flowering throughout the summer. Their flowers can
provide an additional food source for D. insulare adults (Chapter 1).

Diamondback moth oviposition is higher on Brassica hirta L. than on canola
(Palaniswamy & Gillott 1986). In contrast, my results indicate that egg laying on B.
kaber, closely related to B. hirta, and canola were not different. In addition. B. kaber was
as good as the Brassica crop varieties for both diamondback moth development and D.
insulare parasitism. In the United States, B. kaber is considered to be a troublesome weed
(Buchholtz et al. 1981). B. kaber, however, is an excellent nectar source for D. insular-e
(Chapter 1). It grows throughout the summer season, and can easily be killed by
herbicides normally used in Brassica fields (Buchholtz et al. 1981). In addition, the
presence of B. kaber throughout planting season could be important near fields frequently
treated with pesticide because it could provide refuge for the susceptible diamondback moth
populations and hosts for D. insulare. This can slow down resistance build up, reduce

pesticide use and maintain the presence of parasitoids in the field. Therefore, I have no

136
doubt that there will be more benefit than risk when B. kaber is used in diamondback moth
management program. B. kaber can be grown outside the field or in patches within the
field. Brassica juncea (L.) Czern.. is currently used as a trap crop in a diamondback moth

management program in India (Srinivasan & Krisna Moorthy 1991).

CONCLUSIONS

It is important for us to understand the triu'ophic interaction between brassicaceous
plants, diamondback moth and its parasitoids. especially D. insulare. This will enable us to
effectively combine the effects of host plant, varieties or cultivar selection and planting of
wild brassicaceous species, and use D. insulare to suppress diamondback moth populations
and reduce pesticide dependence. Adoption of this type of integrated system will be more
difficult than selecting a new cultivar or using a new pesticide. Demonstration and

acceptance by leading growers will be required for larger scale adoption.

 

CHAPTER 7

Alternate Hosts of Diadegma insulare (Cresson)(Hymenoptera:
Ichneumonidae), a Parasitoid of Diamondback Moth (Lepidoptera:
Plutellidae): A Preliminary Search

137

 

138

ABSTRACT

Diamondback moth parasitism in the field in Michigan is high throughout the year
and in a variety of habitats, in spite of low diamondback moth populations. This suggests
that an alternate host may be involved. If so. it could perhaps be used to increase numbers
and effectiveness of D. insular-e in managing diamondback moth. I conducted a
preliminary search for alternate hosts of Diadegma insulare (Cresson) at the Michigan State
University Research Farm and three other locations near the campus area in the spring and
summer of 1993 and 1994. Potential alternate host larvae and pupae were collected from;
wild brassicas and brassicas crops, apple (Ma/us domestica L.) orchards, ornamental
honeylocust tree (Gleditsia triacanthos L.), and corn (Zea mays L.) for further laboratory
observation. I also used laboratory reared Phthorimaea operculella (Zeller) and Sitotroga
cerealella (Oliver)(1_epidoptera: Gelechiidae) to see if D. insulare will parasitize these
gelechiids. None of the Lepidoptera studied seemed to be important alternate hosts of D.
insulare. However, the samples were small and few plants, except for Brassicaceae, were
inspected for the alternate hosts. Surprisingly, D. insulare parasitized Plutella porrectella
L., but neither host pupae nor parasitoid pupae were formed. P. operculella and S.
cerealella were also parasitized by D. insulare. Percent parasitism of P. operculella ranged
from 0-34.3% depending on the host instars parasitized. There were only two male D.
insulare emerged from > 1000 S. cerealella larvae exposed for parasitism. This is the first
report that D. insulare can parasitize P. operculella or S. cerealella. In contrast to the
parasitized P. xylostella larvae, the development of these two gelechiids larvae was greatly
shortened by parasitism. This suggests that D. insulare may have other hosts in nature

because of the flexible ability to control its host development. Since microlepidopterans,

 

139
especially gelechiids and tortricids larvae are usually concealed within the webbed leaf or
fruit, the temporal window (length of exposure for parasitism) of each host and the
searching ability of D. insulare could partly determine the level of parasitism. Steps to

speed up searching for the alternates host of D. insulare are discussed.

 

140

INTRODUCTION

Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae) is the new world
species of the genus Diadegma and is recorded from southern Canada south to Venezuela
and west to Hawaii (Carlson 1979). In Canada and United States, D. insulare is the major
parasitoid of the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae) and
often parasitizes > 80% of the host larvae (Harcourt 1986, Idris & Grafius 1993). D.
insulare populations are abundant in Brassica crop fields (Harcourt 1986) and other crop
fields (Chapter 5). For example, percent parasitism of diamondback moth larvae placed in
crops such as tomatoes, corn or apples for 24-26 h was as high as parasitism in broccoli
(Chapter 5).

Diamondback moth cannot survive the winter weather in Canada (Smith & Sears
1982), but may overwinter in Michigan (Idris & Grafius 1995b). Diamondback moth
infestation in early season Brassica crops may be caused by populations migrating from the
southern States of United State in the mid-May each year (Smith & Sears 1982, Harcourt
1962), by overwintering (Idris 1995) or brought with Brassica transplants from the
southern United States. No one seems to have considered that some of its parasitoids
might also be migratory. Putnam (1978) found that D. insulare does not survive the winter
in Saskatchewan, Canada, but the other diamondback moth parasitoid, Microplitis plutellae
(Muesback)(Hymenoptera: Braconidae) does. However, D. insulare is more abundant than
M. plutellae. Recently, traps used to monitor the migration of potato leaf hopper from the
southern United State accidentally caught diamondback moth but no D. insulare or other

Hymenoptera (Rahardja, personal communication).

 

141

It is not known how Diadegma species associated with diamondback moth in the
temperate zones overwinter. However, the most common method of overwintering in
ichneumonids is diapause of the full-grown larva within its own cocoon (which may be
within some host remains, such as a pupa)(Fitton & Walker 1992). In multivoltine
Ichneumonidae, sometimes only a proportion of the late summer generation enters
diapause, the remainder survive or perish, depending on weather. In many cropping
situations Diadegma cocoons might be destroyed during winter plowing but wild
Brassicaceae or crops left undisturbed could possibly harbor a large enough overwintering
population to explain the sometimes high rate of parasitism of the spring generations of
diamondback moth in the spring (Fitton & Walker 1992). In Michigan, we observed adults
of D. insulare female searching or visiting the wild Brassica, Erysinms cheiranthoides L.,
as early as 17 May 1993 (Appendix 2).

Because diamondback moth can overwinter as an adult some workers have
suggested that Diadegma must overwinter in association with another overwintering insect
Data in the literature suggests that many Diadegma species have wide host ranges. For
example, Hardy (1938) reported that, in addition to diamondback moth, D. semiclausum (=
eucerophaga)(Hellen) and Diadegma fenestrale (Holrngren) attack 8 and 24 species of
Lepidoptera, respectively, none of them in the family Plutellidae. He also described D.
fenestrale as very polyphagous because it also attacked one coleopteran.

Diadegma species that have more than one host often have some common factor
linking the hosts. For example, Diadegma chrysosrictos (Gmelin) parasitizes a small
number of pyralid moths that live in a narrowly defined niche (Horstmann & Shaw 1984).
D. Chrysostictos is suspected to alternate between a micro and a macro-lepidopteran feeding
on the same plant (Fitton & Shaw, 1992). However, reports of Horstrnann & Shaw
(1984) and Dijkerrnan (1990) indicate that Diadegma are relatively host-specific where the

primary host is a microlepidoptera.

 

142

Other than diamondback moth, two macrolepidoptera, Trichoplusia ni (Hiibner)
and soybean looper, Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae), are
parasitized by D. insularis and D. plutellae (Harding (1976); both are synonymised to D.
insulare (Azizad A. A. & M. Fitton, Natural History Museum, University of London,
personal communication). These noctuids, however, were not listed as the alternate hosts
of D. insulare (Carlson 1979). D. insulare is also reported to parasitize two
microlepidoptera. Hellula undalis (F.)(Pyralidae) and Plutella armoricacae Busck
(Plutellidae)(Carlson 1979). Hellula are tropical and subtropical species (Heppner 1987)
and are not potential altemate hosts for D. insulare in Michigan. In contrast, P.
armoricacae is recorded from Michigan (Department of Entomology Museum, Michigan
State University), but its host plant, the horseradish (also Brassicaceae), is rare.
Therefore, it also is probably not associated with the D. insulare abundance and high
parasitism rate of diamondback moth in the early spring each year.

I have a strong belief that D. insulare must have alternate hosts in Michigan and
other northern states of the United States. First its parasitism rate is high throughout the
year and in a variety of habitats. Second, D. insulare is not a good migratory insect
compared to its primary host, the diamondback moth (Putnam 1978, Smith & Sears 1982).
Third, D. insulare was found in the field as early as the 17 May 1993 (Appendix 2).

The objectives of my study were to search for altemate hosts of D. insulare from
the (1) insects associated with cultivated and wild Brassicaceae, (2) Lepidopteran found in
Brassica crop fields, (3) remains in the spring of the previously year's broccoli cr0p, and

(4) insects associated with nonhost plants of diamondback moth.

 

143
MATERIALS AND METHODS

Insects associated wild Brassicaceae. Wild Brassicaceae (50-100 plants per
species per year) was collected from April through August of 1993 and 1994 from
Michigan State University research farms. East Lansing, Michigan, and three locations
adjacent to campus (Table 1). Each plant was pulled by hand and put on white paper
placed on the ground. I shook each plant over the paper for about 3 min and collected all
insect larvae and pupae. Thorough inspection was made of the flowers because larvae may
feed and hide in between the florets (Marsh 1917). Larvae and pupae were brought to the
laboratory for rearing.

Leaves of each plant were randomly selected and detached, brought to the
laboratory and placed in 10 x 7 x 5 cm rearing pans (3 x 4 cm lid on top) at 25 i 2°C and
photoperiod of 16:8 (LzD) h. To keep the leaves fresh for few days I put wet paper towel
inside the bottom of the pan before putting in the leaves. The numbers of newly hatched
larvae were recorded for 10 d.

Field collected pupae were reared as above until adults emergence. Field collected
and laboratory-reared larvae were divided into two groups to be used in separate
observations. For group 1, larvae were put in the rearing pan as before and fed with leaves
of the same plant species from which they were collected. Larvae of group 2 were exposed
to parasitism by D. insulare as described in Chapter 1. larvae from both groups were
reared until pupation as before and I recorded the types and numbers of pupae formed. 1
also dissected the prepupae of Plutella porrectella L. and diamondback moth (n = 20 per
insect species) from group 2 to determine the presence of D. insulare larvae. This was
done because I wanted to know why there were no parasitoid or Plutella porrectella L.

pupae formed from the parasitized P. porrectella larvae.

144
In the summer of 1993 and 1994, I also put white sticky traps (PheroconTM 1C -
bottoms, Trece, lnc.. Salinas, CA) within patches of the Dame's rocket, Hesperis
matronalis (L.). since it is reported as the main host plant for P. porrectella (L.)(Smith &
Sears 1984). The traps were hung on the stems (10-20 cm below the highest level of the
plants). D. insulare adults and other Lepidoptera caught on the traps were recorded and
removed every day.

Lepidoptera larvae in the broccoli field. I collected all Lepidoptera larvae found
in the broccoli field in the summer of 1993 and 1994 (Table 2). 'Larvae were subdivided
into two groups and were subjected to separate observations as before.

Cultivated broccoli remains. On 28 April 1994, I set up six cages (180 x 165 x
165 cm high) in my 1993 broccoli experimental plots at the Michigan State University
Collins Road Entomology Research Field . On 3 May, I pulled up the partially rotten
broccoli remains and put 50-70 of them in each cage. To monitor adult D. insulare or other
potential hosts I hung white sticky traps. 0.5 m from the ground on wooden stakes in the
cages. On 7 May, six potted broccoli plants from the greenhouse, infested with
diamondback moth second and third instars, were placed inside each cage. larvae were
collected weekly, brought to the laboratory and reared as before until pupation. The
infested potted broccoli plants were replaced weekly and larval collection and rearing were
continued until the end of June. Numbers of D. insulare adults or other Lepidoptera caught
on the traps, numbers and types of pupae formed were recorded.

Insects associated with nonhost plants of the diamondback moth. Estate
.0; 110.1 '1 0' r’. n r .' . llr ‘ mo r : ' 1‘1; hii 1' . Iconducted these
experiments in the laboratory. One month old greenhouse raised potted potato plants were
put in 45 x 40 x 40 cm cages (two per cage).
In the first experiment, P. operculella eggs from laboratory culture were put on the
potato leaves in the cages. After most eggs hatched we released several 6 (1 old-

experienced D. insulare females into the cages for 3-4 (1 to parasitized the first instar of P.

145
operculella. I put a cotton wick wetted with honey+water (10% honey) in the cages as
food for the parasitoids.

In the second experiment, I put P. operculella eggs in a 14.5 cm diam Petri dish
until hatch. Second, third and fourth instar P. operculella were collected accordingly, and
were released on the potted potato plants for parasitism as before.

After 4 (1 access by D. insulate the P. operculella larvae were collected from the
leaves. stems and the tubers of the potted potato plants, put in 10 x 7 x 5 cm rearing pans
half filled with potato tubers and kept at 25 i 2°C and a photoperiod of 16:8 (LzD) h until
pupation. The numbers of P. operculella and D. insulare pupae formed were recorded
every day until all larvae pupated. I recorded the developmental time for each instar to form
P. operculella or parasitoid pupae, and sexes of adults D. insulare emerged. Because each
instar of P. operculella was exposed to parasitism separately 1 just recorded the day of the
first five P. operculella or D. insulare pupae formed from the respective larval group (first.
second. third or fourth instars) to measure the developmental time for parasitized versus
unparasitized larvae.

In the third experiment, Icross—checked the occurrence of parasitism on
diamondback moth by D. insulare produced from P. operculella. To do this, 30 third instar
diamondback moth were exposed to one D. insulare female (reared from P. operculella) as
described in Chapter 1 except the exposure time was increased from 3 h to 4 d. The
presumably parasitized P. xylostella larvae were reared as before until pupation. Numbers
of D. insulare and diamondback moth pupae formed were recorded.

All experiments were replicated four times. Percent parasitism was calculated as
described in chapter 4 and analyzed by 1-way ANOVA (Abacus Concept, SuperAnova
1991). The differential in sex ratio of D. insulare produced from parasitized instars of P.
operculella was calculated using X2 (l : 3.2 D. insulare sex ratio from cross-checked

experiment was used as the expected value)

146

u or 1-1 0 u r orr I u' ' ,m' lg '_onr L: m o 9 : .° P mlro .‘ . Fourty
first instar 0. nubilalis (donated by Dr. Douglas A. Landis. Department of Entomology,
Michigan Sate University) were divided in two groups (five larvae per group per replicate).
Group 1 was tested as a first instar. Group 2 larvae were fed on artificial diet (also donated
by Dr. Landis) until they became second instar and then tested. Larvae of each group were
exposed for parasitism by D. insulare as before. After D. insulare exposure, larvae were
fed with fresh artificial diet every 3 d and reared to determine parasitism.

In August 1994, larvae of 0. nubilalis were collected from a corn field at the
Entomology Researh Field, brought to laboratory and reared as before to determine if D.
insulare parasitism had occuned.

Ipstrieids in Apple Qrehard. I conducted two separate studies. In the first study, I
collected 1000-1100 apples from the Entomology Research Field and Trevor Nicchols Fruit
Research Station, Fenville, Michigan, in July through September 1994. In the laboratory
the fruit were carefully cut to look for tortricid larvae or pupae. All parasitoid pupae
collected were kept as before and reared to parasitoid emergence. I also collected apple
leaves and shoots, and put them in a rearing pan as before, to get fresh first or second
instar tortricids for similar observations. The collected larvae were separated by species. .
Regardless of the larvae stages or if they were naturally parasitized in the field, I exposed
them for parasitism by D. insulare as before. I supplied larvae with a thin slice of apple
fruit on the second day of exposure. The presumably parasitized larvae were fed with a
fresh apple slice every 4 d and reared. The types and numbers of pupae formed were
recorded.

For the second study, larvae were collected from leaves, shoots, and 500 apple
fruits from the field as before. but reared without exposing them to D. insulare for
parasitism. Larvae were grouped by species, fed apple fruit, and reared as before until

pupation. I recorded the types and numbers of pupae formed.

147

an” moi 9 in r l mu ”!'.11V1‘ 'rrrru:. ‘lhrract' . S.
cerealella (donated by Dr. D. K. Weaver, South Atlantic Area Stored-Product Insects
Research and Development laboratory, Georgia, USA) was used for the study. A folded
black paper stapled at both ends (6 cm x 2 cm) was put in 400 m1 plastic container
(designed as described in chapter 1) for oviposition. Ten pairs of S. cerealella were
released in the container for 2 d, after which they were taken out leaving the eggs on the
black paper. After all the eggs hatched, I released five 6 (1 old and experienced D. insular-e
females into the container for 4 d to parasitize the first instar of S. cerealella. I provided
only enough corn kemals during parasitism period to keep the larvae alive. I_added more
com kernels 4 (1 later when D. insulare were removed. Presumably parasitized larvae were
reared until adult emergence. The numbers of S. ccrealella and D. insulare pupae formed.
and the emerged adults of both insects (starting 10 d after eggs hatched) were recorded.

Percent parasitism was calculated as before.

Mi 0 .w wr‘mH urII' 'rI'M rik .rl :olli . M i.-rwih
WWW Larvae of H. anisocentra were

collected from 250-300 C. triacanthos around the campus and the nursery field of Forestry
Department. Michigan State University, Michigan in June and July 1994. Larvae were
brought to laboratory, reared by feeding them with G. triacanthos leaves and flowers, and

kept as before until pupation. The numbers of pupae formed were recorded.
RESULTS AND DISCUSSION

Insect associated with wild Brassicaceae. I found diamondback moth larvae
on all wild Brassicaceae except Neslia paniculata L. (Table 1). Imported cabbagewonn
larvae, Pieris rapae L (Lepidoptera: Pieridae), were collected from Barbarea vulgaris R.
Br. , Brassica kaber (DC) Wheeler, Raphanus raphanistrum L. and Sisymbrium officinale

(L.) Scop. Cabbage looper, Trichoplusia m' L. (Iepidoptera: Noctuidae), was found from

148

B. vulgaris, R. raphanistrum and Hesperis matronalis (L.). Other than Lepidoptera larvae,
syrphid species (Diptera: Syrphidae) and lady beetle species (Coleoptera: Coccinellidae)
were also collected. There were no D. insulare pupae formed from Lepidotera other than
diamondback moth larvae collected in 1993 and 1994 in both larval groups tested. In the
laboratory, 1 found mostly P. xylostella and five 0. nubilalis larvae from field collected
detached Brassica leaves. None of the 0. nubilalr's larvae were parasitized by D. insulare.

Most third and fourth instars of the P. porrectella collected in May 1993 (78.6%, n
= 155) and June 1994 (93.7%, n = 180) successfully formed moth pupae. Regardless of
larvae group tested, there were no D. insular-e or other parasitoid pupae formed. In
Ontario, Canada. Smith & Sears (1984) reported that P. porrectella was not parasitized by
D. insulare but by ltoplcctis conquisitor (Say)(Hymenoptera: Ichneumonidae). The
external appearance of parasitized P. porrectella and P. xylostella larvae look similar at the
prepupa stage. During pupal stage, parasitized P. xylostella formed a parasitoid pupa while
parasitized P. porrectella's body shrunk, failed to produced a cocoon and died, not forming
either host or parasitoid pupa. Dissection of the larvae exposed to D. insulare indicated that
there were no D. insulare larvae from the P. porrectella but z 92% of parasitized P.
xylostella contained D. insulare larvae. I also observed that D. insulare females were
actively searching for P. porrectella larvae and ovipositing; behavior similar to what I
usually see when the parasitoid is exposed to P. xylosrella larvae. This indicates that the
parasitoid eggs failed to survive in the host body. Physiological development of P.
porrectella parasitized larvae was probably affected by a polydnavirus injected with the
eggs during oviposition. The influence of ichneumonid parasitoids polynavirus on host
physiology is common. For example, polynavirus of Eriborus (= Diadegma) terebrans
(Gravenhost) is responsible for parasitism success of this parasitoid on European corn

borer, 0. nubilalis (Stoltz et al. 1981).

Table l. Insect larvae collected from the wild Brassicaceae during the summer of 1993

149

 

 

 

and 1994
Larvae“
Weed Species Common Name
Lepidoptera Diptera Coleoptera
Barbarea vulgaris R. Br. Yellow rocket ICW, DBM. CL S LB
Berteroa incana (L.) DC Hoary alyssum DBM ' N LB
Brassica nigra (L.) Koch Black mustard DBM S LB
Brassica kaber (DC) Wheeler Wild mustard DBM, ICW, UL* S LB
Capsella bursa-pastoris Shepher's purse DBM N N
(L.) Medic

Erysimum. Wormseed mustard DBM N N

cheiramhoides (L.)
Lepidium campestre Field pappervvecd DBM S LB

(L.) R. Br.
Lepidium densiflorum Greenflower DBM S LB
(Schard) pepperweed
Lepidium virginicum L. Virginia pepperweed DBM N N
Neslia paniculata Ball mustard N N LB
(L.) Desv.

Raphanus raphanistrum L. Wild radish DB M, ICW, CL S LB
Sisymbrium altissimum L. Tumble mustard DBM N LB
Sisymbrium ofi‘icinale Hedge mustard DBM, ICW S N

(L.) Scop.
Thlaspi arvense L. Field pennycress DBM S LB
Hesperis matronalis (L.) Dame's rocket PP, DBM*, S N

UML, CL

 

a ICW, imported cabbage worm; DBM, diamondback moth (Plutella xylostella L.); UL,

unidentified microlepidopteran; PP, P. porrecrela L.; CL, Cabbage looper; UML,

unidentified macrolepidopteran; S, syrphid larvae; N, none; LB, lady beetle; * .less than

five collected.

150

Three D. insulare, ten P. porrectella, and three P. rapae adults were caught on the
sticky traps placed within H. matronalis patches but there were no P. xylostella adults.
The presence of D. insulare was not surprising because it attacked both P. xylostella and P.
porrectella larvae in the laboratory.

Lepidoptera larvae found within the broccoli field. Except for diamondback
moth larvae, none of the other field collected Lepidoptera larvae (from both larval groups
tested) were parasitized by D. insulare (Table 2). In the laboratory, D. insulare females
were not observed attacking Lepidoptera larvae Other than diamOndback moth and P.
porrectella larvae. This suggests that. at least in Michigan, common insects that regularly

or occasionally feed on Brassica plants are not altemate hosts Of D. insulare.

Table 2. Lepidoptera larvae collected from the broccoli field in the summer of 1993
and 1994, and percent parasitism by Diadegma insulate

 

 

Insect species Common name Approximate Percent
or family numbers collected parasitism

Plutella xylostella L. Diamondback moth 100 100
Pieris rapae L. imported cabbagewonn 70 0“
Trichoplusia ni L. Cabbage looper 30 0”
Tortricidae - 10 0”
Lymantridae (unknown sp.) - 20 0”
Arctiidae ( " ) - r0 0“- ’7
Noctuidae( " ) - 8 0a' b
Unidentified

microlepidopteranc - - -

macrolepidopteran - 4 0b

 

a There was no parasitism even though all different larval stages were exposed for
parasitism by D. insulare.

b Only late instars were exposed for parasitism and were fed broccoli leaves.

c Died because of food source problem

15 1

Cultivated broccoli remains. There were no diamondback moth or D. insulare
adults caught on the sticky traps placed inside the cages until the end Of June in 1993 or
1994, indicating D. insulare is not using diamondback moth as a host to overwinter.
However, three M. plutellae adults (one female) were caught from one of the six cages. A
total of 20 pupae of a M. plutellae were produced from diamondback moth larvae exposed
for parasitism in the field cages and of these, ten M. plutellae adults emerged.

Insects associated with nonhost plants of the diamondback moth. Estate
tuber meth, P. upergulellg. Parasitism was as high as 34% and ivas significantly lower on
the later instars than on the earlier instars of P. operculella (FPLSD, P < 0.05)(T able 3). In
contrast, percent parasitism of P. xylostella larvae by D. insulare is higher on the second
and third instars than on the first or fourth instars (Bolter & Laing 1983, Harcourt 1960).
Larger P. operculella larvae spend less time outside the plant (tuber, stem or leaf) than the
smaller larvae (Metcalf & Metcalf 1951). Therefore, larger larvae have a shorter exposure
time for parasitism to occur than the smaller larvae. Results of cross-checked parasitism
showed that D. insulare produced from P. operculella parasitized 88.9% of diamondback
moth larvae (Table 3). This is similar to parasitism rate by D. insulare originating from P.
xylostella (Bolter & Laing 1983).

Regardless of the P. operculella instars parasitized, the male to female sex ratios of
D. insulare from P. operculella were not significantly different from the sex ratios of D.
insulare produced from cross-check parasitism; the sex ratio from cross-check parasitism
is similar to the sex ratio of D. insulare originated from diamondback moth (Idris & Grafius
1993b, Chapter 6). Therefore, in a potato-Brassica intercropping, D. insulare originating
from a potato field infested with P. operculella could parasitize as high a proportion of
diamondback moth in the Brassica crop field as D. insulare from the Brassica crop field
itself. The foreseeable limitation is that there would be less D. insulare produced from the
potato field than from the Brassica crops field. However, the availability of P. operculella

as an alternate host Of D. insulare may allow us, if necessary, to use pesticides to

 

152

Table 3. Percent parasitism of Phthorimaea operculella (Zeller) by Diadegma
insulare (Cresson), the male to female sex ratio of D. insulare and percent parasitism of
Plutella xylostella (L.) by D. insulare produced from P. operculella

 

Instar of P. operculella
Observation Cross—check parasitism

First Second Third Fourth (third instar P. .xjvlostella)

 

 

Percentparasitism 34.3c 25.3b 8.8a 0a . 88.91
Thesexratioz 5.4:1 4.5:1 3.5:1 - 3.2:1

 

Same letters in the row are not significantly different (Fisher's Protected LSD, P > 0.05)

1 Mean of four replicates

The male to female sex ratio was not significantly different (12, P > 0.05)

control diamondback moth; D. insulare from the potato field could kill diamondback moth
larvae in the Brassica field that escaped from pesticide treatment. This can indirectly slow
down insecticide-resistance development

Surprisingly, the time taken for parasitized P. operculella larvae to form D. insulare
pupae was approximately 14 d, 4 to 6 d shorter than the time taken by unparasitized larvae
to form P. operculella pupae. In contrast, time taken by unparasitized diamondback moth
larvae to form diamondback moth pupae is 2 to 3 d shorter than time taken by the
parasitized larvae to form D. insulare pupae (Idris & Grafius 1993c). This indicates that D.
insulare larvae within the parasitized P. operculella larvae may be able to control the
physiological development of the host to synchronize with its developmental time.
Parasitized P. operculella larvae were also observed to pupate more openly or without full
cover of frass on the outside of potato tubers compared with healthy pupae. These two
intriguing behaviors; the D. insulare larvae within the parasitized P. operculella larvae and

pupating behavior of the parasitized P. operculella larvae may have some biological

153
significance to control pests especially with the help of advanced biotechnology
knowledge.

WW3. In the field, I did not find L6pidoptera larvae or
pupae other than 0. nubilalis. In the laboratory, no parasitism occurred on 0. nubilalis
larvae. D. insulare females did not approach the European corn borer larvae even with the
frass around. This was not surprised me because the significant reduction in percent
parasitism of the diamondback moth was reduced with distance from the edge of a corn
field indicating that com does not harbor alternate host of D. insulare (Chapter 4).

Although D. insulare parasitizes H. undalis (Carlson 1979), my results indicate that
this parasitoid parasitizes only certain pyralid(s) that feeds on certain plants. Another

species of pyralid, H. rogatalis (Hulst), that feeds on Portulacaceae and Amaranthaceae

 

with Brassicaceae as its main food plant (Heppner 1987), may act an alternate host of D.
insulare. However, H. undalis and H. rogatalis are not reported to occur in Michigan.
There were no pyralids found from cultivated or wild Brassicaceae in my study. Searching
for pyralids on Portulacaceae and Amaranthaceae plants should be initiated.

W. No D. insulare emerged from five different types of
tortricid pupae collected in the field or exposed for parasitism in the laboratory. There were
only one first and two second instars of Grapholita molesta (Busck), the oriental fruit
moth, collected from apple fruit that I put in the rearing pan. A total of 60 of the six
tortricid larvae, all in third or later instar, were collected from the apple leaves, shoots and
fruits in the field (Table 4). None of these tortricids were parasitized by D. insulare.

My results and other studies (N. 1‘. Mills, University of California Berkeley,
personal communication) confirmed that codling moth, Cydia pomonella (L.), is not an
alternate host of D. insulare. Three other Diadegma (= Horogenous) species are reported to
parasitize G. molesta but they are not important parasitoids (Allen 1962). However, P.
xylostella larvae placed in an apple orchard for 28 h were parasitized by D. insulare

(Chapter 5). Therefore, there is a possibility that D. insulare use tortricids, like 0. molesta

154

Table 4. Tortricids of apple orchard exposed for parasitism by Diadegma
insulare (Cresson)

 

 

Scientific names Common name
Cydia pomonella (L.) Codling moth
Grapholita molesta (Busck) Oriental fruit moth
Archips argyrospila (Walker) Fruittree leafroller
Charistoneura rosaceana (Harris) Oliquebanded leafroller
Plarynota idaeusalis (Walker) Tufted apple budmoth
Platynota flavedana (Walker) Variegated leafroller

 

 

and Platynota idaeusalis (Walker), as alternate hosts to overwinter (Beddingger et al.
1994). However, I had only three small larvae (in nature, this is the only possible stages
that are expose to parasitism by Diadegma spp.) of G. molesta and used laboratory-reared
D. insulare. This study should be repeated by using more G. molesta small larvae which
may need special laboratory rearing and expose them to field collected D. insulare.

Closely related species to D. insulare, D. fenestrales (also parasitizes P. xylostella
larvae, Hardy 1938, Fitton & Walker 1992) and Diadegma interruptum pterophorae
(Ahmead) parasitize tortricids of apple in Oregon and in Alaska, respectively (Carlson
1979). In Michigan, there are 47 species of microlepidoptera in apple orchards, and of
these, 27 species are tortricids (Strickler & Whalon 1985). High numbers of tortricids in
apple orchards increases the possibility that at least one of them could be an alternate host
of D. insulare. However, further research is needed, including exposing as many small
larvae of tortricids as possible to D. insulare, in the laboratory. In the field, collection of
the tortricid larvae in the early spring and at the end of the summer may increase the

possibility to get overwintered parasitized tortricid larvae.

ll

155

W. There were only two D. insulare males
produced from >1000 first instar S. cerealella exposed for parasitism. The D. insulare

adults emerged 6-9 d earlier than the S. cerealella adults. The developmental time for
unparasitized larvae of S. cerealella is between 20 and 24 d (Metcalf & Metcalf 1951). This
suggests that D. insulare larvae could alter host larval physiology to suit its life cycle or
larval development

In Egypt, D. semiclausum is reported to emerged from S. cerealella infesting stored
grains (Ahmad Musa, personal communication). However, there was no S. cereallella
collected from stored grain in a Michigan study (Russell 1980), indicating it is not common I
in Michigan. In the field, I did not get this moth form wheat or corn, but ichneumonid
(probably Diadegma sp.) searching for hosts on the wheat head were observed.

Mimosa webwgm, H, gm'sgaggna'g. I was able to get only three larvae (one third
and two fourth instars) of H. aniscocentra from G. triacanthos trees sampled in May 1994.
They were found from the flowers. I failed to find them from J une onward. However,
none of the three larvae were parasitized by D. insulare. I also found four pupae within
webbed leaves. N o D. insulare adults emerged from these pupae. However, Diadegma
spp. are reported as the primary parasitoids of H. aniscocentra (Peacock , see Miller et al.
1987). This moth is probably not an important alternate host of D. insulare. A
combination of increased parasitism from other parasitoids, heavy rains, and cold winter is
perhaps reduce the local H. aniscocentra populations nearly to zero (E. R. Hart. ,
Entomology Department, Iowa State University, personal communication). This also
explains why I was unable to collect enough larvae for my study.

Other pluttelids, feeding on non-brassicaceous plants that occur in Michigan are
Plutella amzoraciae Busck (Museum of Department Entomology, Michigan State
University) and Ypsolopha dentiferella (F.)(Profant 1991). These are unlikely hosts for
overwintering D. insulare adults in Michigan because their host plants are very rare.

Plutellid close relatives, yponomeutids, have three species reported in Michigan (Profant

 

156

1991). D. insulare may also use them as alternate hosts, but further study is needed. In
the Netherlands, Dijkennan (1990) reported that Diadegma armillata (Gravenhorst)
parasitizes six species of Yponomeutidae. 9

Results of my preliminary search indicate that none of the Lepidoptera collected are
the alternate hosts of D. insulare. Although P. operculella and S. cerealella cannot
overwinter in Michigan and probably in other northern states of the United States and
Canada, to my best knowledge, this is the first report that D. insulare parasitizes these two
gelechiids. Therefore, I added two more species to the current list of Lepidoptera that can r
be the alternate hosts of D. insulare (Carlson 1979).

My results and from previous records (Carlson 1979) indicate that D. insulare is

not a true specialist parasitoid. Besides diamondback moth as its major host (Harcourt

 

1986), D. insulare may have many alternate hosts other than plutellids. This would be
facilitated by the ability of the D. insulare larvae to influence the physiological development
of its host larva either by delaying or speeding up the parasitized host larvae entering
prepupa stages when D. insular-e comes out and pupates outside the host. Although
delaying the host development is a common phenomenon for the endoparasites, forcing the
host to pupate one to two weeks earlier is unusual. D. insulare's influence on parasitized
larvae to pupate more openly (P. porrectella and P. operculella) is also interesting. The
second argument is that most plutellids may have evolved some kind of defensive
mechanism, due to long association between the two insects, such as behavior to avoid an
attack from D. insulare or an immune system to succumb the parasitoid eggs. P.
porrectella has some type of defensive mechanism against D. insulare parasitism.
Differential ability to encapsulate eggs of Diadegma spp. by P. xylostella are reported in
Australia and England (Goodwin 1979, Fitton & Walker 1992, Hardy 1938). Another
example is reported by Dijkerman (1990) where six species of Yponomeutidae, a close
related family of Plutellidae, have differential ability to encapsulate the eggs of theirs

parasitoid, D. armillata. He speculated that species showing high encapsulation rates are

 

157
those that have diverged early in the evolution of the genus, whereas the more recently
evolved species showed an intermediate percentage or were not able to encapsulate eggs of
their parasitoids. Therefore, P. xylostella and D. insulare may have become associated
quite recently.

P. xylostella larvae are easily accessible for parasitism by D. insulare. In contrast,
the potential of other insect's larva to become an alternate host is depend on their length of
exposure for possible parasitism by D. insulare. This is because many Lepidoptera larvae
are concealed or protected from the reach of a parasitoid like D. insulare. For example, the
length of exposure for parasitism of S. cerealella and P. operculella is about 1 d after
hatch. P. opercullella may also be exposed sometime during latter larval stages.

In Michigan and other northern states of the United States and Canada, the question
of what insect species act as the alternate hosts of D. insulare is still widely open.
However, I suggest that a search for D. insulare's alternate hosts should be concentrated on
the three microlepidopteran families; Pyralidae, Gelechiidae and Tortricidae. Thorough
search of microlepidopterans associated with Brassica plants might also increase the
chances to find the alternate hosts of D. insulare. Some ichneumonid parasitoids of apple
tortricids parasitize unrelated Lepidoptera in the same orchard, if its primary hosts are less
abundant (Brunner et al. 1981). The microlepidopterans. especially the pyralids, gelechiids
and tortricids, on crops or plants other than Brassicaceae should be collected as many as
possible or tested for parasitism in the laboratory. Laboratory rearing of the insects
collected could really help the process of host searching but it may be laborious. Dissecting
adult females late in the season to examine the condition of the ovarioles and fat body
should also be conducted. If the abdomen of the females is full of active ovarioles, with
mature eggs present, and the condition of fat body is normal then the parasitoid most
probably overwinters as larvae within the host larvae (N. J. Mills, personal

communication).

 

158
CONCLUSIONS

Result of this study could narrow down the areas, plants or habitats as well as the
insect family to be searched for D. insulare alternate hosts in the future study. Identification
of an alternate host will speed up the integration of factors responsible for D. insulare
overwintering population into the total diamondback management program. For example.
we could intercrop the host food plant of D. insulare 's alternate host within Brassica crop
agroecosystem. This could increase the parasitism efficiency of D. insulare because it does
not need to do much travel and spend longer time to find its alternate host.

I still believe that an alternate host or hosts are responsibles for D. insulare
abundance and high parasitism of diamondback moth larvae in many different habitats, in
spite of low diamondback moth populations. Identification of the alternate hosts would

provide objectives for design of pest management system for increased level and stability of

parasitism.

 

 

OVERALL CONCLUSIONS

159

 

160

OVERALL CONCLUSIONS

At least four developing countries; Malaysia, Indonesia, Taiwan and Guatemala,
report success of controlling diamondback moth using parasitoids in their Brassica growing
areas (Idris et al. 1995). The evolution and implementation of abiological control-
integrated pest management (BC-1PM) system for Brassica crop, a 24 year case history,
was discussed by Biever et al. (1994). In Guatemala, Biever et al. (1994) report the
success of a biological control-integrated pest management program (BC-1PM) to manage
lepidopteran insect pests using biological control agents (Bacillus thuringiansis var.
Kurstakj), pest population monitoring, and early-season inoculative releases of beneficial
agents; these have replaced the routine application of chemical insecticides to control
diamondback moth and other brassicas crop pests. In this BC-IPM system D. insulare and
C. plutellae are used as diamondback moth's parasitoids. They did not mention which of
these two parasitoids gives more impact on the diamondback moth population. In
Caribbean islands, parasitism of diamondback moth larvae by D. insulare is higher than by
C. plutellae (Alam 1992) and the impact of D. insulare could be increased by knowing
some of its ecological needs and behavior or activity in the field.

Results of my studies indicate that wildflowers; B. kaber and B. vulgaris
(Brassicaceae) and D. carota (Umbelliferae), supply nectar that results in high D. insulare
longevity and fecundity (Chapter 1). The increase in longevity and fecundity was strongly
correlate with flower corolla Opening diameters but not with corolla length. However, the
width of corolla opening only explained 45% of the observed variation among wildflowers
as food sources. The separation among the petals, and between sepals and petals increases

the nectar accessibility for D. insulare on flowers that have narrow corolla openings.

 

161
Nectar quality is also probably important (Baker & Baker 1983, Kidd & Jervis 1989) but I
did not measure it. High numbers of D. insulare caught in weedy areas and at woodland
edge with > 50% D. carota (Chapter 5) indicate that D. carota has high quality nectar that
attracts the parasitoid. D. insulare's nectar collecting behaviors including chewing at the
base of the corolla to access nectar (first recorded here)(Chapter 2) could be another cause
of the variation in the relation between corolla width and D. insulare longevity.

Food source availability determines the impact of natural enemies or failure of insect
biocontrol programs (Kidd & Jervis 1989). The role of wildflowers in the vicinity of crOp
field in reducing insect pests has been demonstrated (Leuis 1960. National Academy of
Science 1969, Van Emdan 1963a & b). In southern Ontario, Canada, B. vulgaris and
other wild Brassicaceae are abundant around the field in early spring (Harcourt 1986). B.
kaber and D. carota also are abundant in Michigan and the northern states of United States
(Buchholtz et al. 1981). As I have discussed above, B. kaber, B. vulgaris and D. carota,
increased longevity and fecundity, and this may explain why D. insulare is abundant
(Harcourt 1986. Chapter 4) and percent parasitism is always high in the field (Chapters 4 &
6). However, the current trend of farming systems, eliminating or causing these weeds to
be sparsely distributed away from the field, disrupts the host foraging process of natural
enemies, especially the specialist parasitoids (Wickers et al. 1994), Although some
parasitoids, such as D. insulare are very mobile in heterogeneous habitats (Chapter 5), their
parasitism efficiency may be seveme affected. When food or wildflowers are available in
the vicinity of the host. this disruption would be minimized and parasitism efficiency
increased (Wéickers & Swaans 1993, Wickers et al. 1994). Therefore, field release of D.
insulare may not be needed. This overcomes the problem of mass-rearing of D. insulare
for use in field release programs (Adam 1994).

B. kaber can be planted in patches or rows within or near to cabbage fields. In
India, the Indian mustard, B. juncea (L.) Czem., planted in one row per 15 rows of

cabbage was found to be the most promising for successful management of diamondback

 

ll

162
moth and the leafwebber, Crocidolomia binomlis Zeller (Lepidoptera: Pyralidae)(Srinivasan
& Krishna Moorthy 1991). In U. S, however, B. kaber is considered as a troublesome
weed (Buchholtz et al. 1981). In addition. reduction in crop related or unrelated weeds has
been especially recommended as a pest control strategy earlier and has been adopted by
many growers (van Emden & Williams 1973). These contradictory recommendations
might confuse the farmers and make them wary in allowing weeds to be present around the
field even though this may only involve maintaining weed populations in the headlands or
hedgerows. Besides acting as food source for D. insulare, B. kaber also provides a refuge r
for insecticidesusceptible diamondback moth, has no adverse effect on the D. insulare sex

ratio, could reduce the numbers of eggs laid and slow down insecticide-resistant build up

 

by diamondback moth. Reports from other studies also partly support my argument. L
Thomas et al. (1992) reported that creating of "island" habitats. (e.g., planting B. kaber in '
patches within the Brassica field), in farmland can manipulate populations of beneficial
arthropods, increasing predator densities and species composition which increases the
stability and enhances biocontrol within the agro-ecosystem. The presence of weeds in a
crop can also influence the contrast between the crop plant and its background (Smith
1969). If the pattern can be broken upwitlr weeds then the contrast is reduced and the
number of diamondback moth or other pests could also be reduced and at the same time the
crop environment made more attractive to the natural enemies. All the above reasons
obviously could outweigh the risk that may incur to the growers due to inclusion of B.
kaber in cabbage ecosystem. However, the question is how to convince the growers? This
is where an effective extension method(s) or workers are very important to ensure the
success of this approach.
D. carota flower is the only non-brassicaceae weed tested that significantly prolong
D. insulare life with high fecundity (Chapter 1). Another Umbelliferae, Aegopodium
podagraria L., a ground—elder is also known to be frequently visited by various parasitoid

species (Kevan 1973). A. podagraria‘s exposed nectaries provide accessible nectar to

163
nectar feeders with short mouth parts (Leius 1960) like D. insulare, although D. insulare is
also able to reach nectar by chewing at the flower base (Chapter 1). Although longevity
and fecundity of D. insulare are significantly lower when fed on D. carota than on B.
kaber, there are three advantages of choosing D. carota over B. kaber. First, it is not an
alternate host plant for diamondback moth and grows in non-cultivated fields (Buchholtz et
al. 1981). Second, D. carota is more easily controlled in a Brassica crops with herbicides
or cultivation than the other Brassicaceae weeds. Third, it is an Umbelliferae, therefore, it
will not pose any cross-fertilization risk with the Brassica crops' as does B. kaber or other
non-crop Brassicaceae. Cross-fertilization will hamper the seed production industry like
canola seed. If the Brassica crops planted are a herbicide-resistant variety then the gene for
resistant could be passed to the non-crop Brassica like B. kaber. The consequences of the
wild beet populations for breeding, seed production and release of herbicide—resistant
transgenic sugar beets was discussed by Boudry et al. (1993). Therefore, D. carota or
other weeds that have similar characters should also be considered in designing Brassica
crop ecosystem. Since D. carota is a biennial (first year, producing rosette of finely
divided leaves and fleshy taproot weed and second year, bloom and dies) it needs to be
planted one year ahead of Brassica crop planting. Subsequent planting may not be
necessary because in the field it produces a lot of seeds.

Although I was not able to record parasitism of diamondback moth larvae by D.
insulare when B. vulgaris was used as host food source (Chapter 6), results of my study
and a report by Idris & Grafius (1994) indicate that B. vulgaris has potential to be used in
insecticide resistant management. Methods of planting and manipulation of this weed were
discussed in Chapter 6.

Honeydew of bean aphids, A. fabea, on C. album increased longevity and
fecundity of D. insulare when compared with parasitoids that were not given any food or
just water (Chapter 1). Although honeydew is rich in the amino acid, tryptophan (Hagen &

Tassan 1972), it may not be as important food source for D. insulare as floral nectar

 

164
because it lacks food finding cues. Wiickers et al. (1994) reported that Cotesia rebecula L.
(Hymenoptera: Ichneumonidae), a parasitoid of imported cabbageworrn, Pien's rapae
(Lepidoptera: Pieridae) neither responds to honeydew nor to volatiles of aphid infested
leaves; they concluded that finding honeydew is a random process. However, leaving
weeds or plants that can provide aphid honeydew outside the field could provide an extra
food source for D. insular-e. The spraying of L-tryptophan solution in olive orchards
increases the numbers of the green lacewing Chrysoperla camea L. in this tree canopy
(McEwen et al. 1994).

Pesticides continue as important tools to combat pests. However, in integrated
pest management it is generally accepted that only selective pesticides should be used and
only if there are no other effective control methods available. Pesticide applications should
also be based on economic threshold levels (ETL) that vary with pest, location and
marketability of the cabbage (Shelton et al. 1982, Doman et al. 1994, Stewart & Sear
1988). The impact of D. insulare on diamondback moth population would be severely
reduced with the wrong timing of pesticide spraying. Idris & Grafius (1993a) found that
all pesticides except Bacillus thuringiensis Berliner var. Kursarki were highly toxic to D.
insulare. My results suggest that pesticides should not be applied between 1100 and 1300
h (Chapter 3) when D. insulare populations are most actively foraging. Effectiveness of
pesticides may be reduced if sprayed early in the morning because leaves are wet with dew
that dilutes the spray droplets. Therefore, the more appropriate time for spraying is in the
late afternoon or evening. This practice could avoid killing of D. insulare as a result of
direct impact of the pesticide sprayed, particularly if there are no refuges outside the field as
discussed in Chapter 1. If B. thuringeinsis is used, its effectiveness could be optimized
because the exposure time of the toxin to ultra violet (UV) light would be shortened.
However, the time range when the parasitoid population is abundant in the field may vary
with day and location (region) of the B. thuringiensis fields, and for different parasitoid

species. This prediction needs further research because diurnal foraging activity of D.

 

165
insulare, especially the females, is also significantly influenced by weather factors (light,
temperature and wind speed)(Chapter 3).

Percent parasitism of diamondback moth larvae is significantly affected by habitats
(Chapter 5). Differential characteristics of the habitats (crops) used and the presence of
food sources in the vicinity of the crop may be the most important factors influencing the
parasitism rate. Host searching efficiency by specialist parasitoids, like D. insulare may be
more reduced in certain habitats (Sheehan 1986). and in most cases efficiency is affected by
the types ofcrop planted (Booij & Noorlander 1992). I did not directly measure the host
searching efficiency of D. insulare. However, percent parasitism in the crop habitats
studied is consistently high (55 to > 80%) indicating searching efficiency of D. insulare
may not be seveme affected. Similar results were observed at the woodland edge and in
weedy areas with > 50% D. carota (Chapter 5). The high mobility of D. insulare in
heterogeneous habitats indicates that D. insulare has a narrow host ranges per habitat or
actively searching for food sources. Parasitism occurred on two gelechiids, P. operculella
and S. cerealella in my research, although they cannot survive winter or are not common in
Michigan, indicating that D. insulare is perhaps able to use insects other than plutellids as
alternate hosts (Chapter 7). This may also explain why this parasitoid is actively mobile in
such diverse habitat. Percent parasitism was also not severely affected by Brassica
varieties or cultivars planted and plant density (= spacing)(Chapter 4). This suggests that
plant density and improved cultivars that produce high yield and quality should be
emphasized in planning for brassicas crops planting.

The above discussion indicates that Brassica crops could be planted in polyculture
or intercropping systems without disrupting the impact of D. insulare in the field. It could
be done as one or the combination of the following suggestions.

1. Brassica crop(s) could be interplanted with tomato because tomatoes have

no adverse effect on parasitism rate of D. insulare (Chapter 5) or C. plutellae, (Bach

 

166
& Tabashnik 1990) . In addition, tomato plants repel diamondback moth adults and
reduce oviposition (Bach & Tabashnik 1990, Burandy & Raros 1975).

2. Brassica fields should be designed so that they are surrounded or are
very close to corn, bean or alfalfa fields. and apple orchard. Although these
crops apparently do not have alternate hosts of D. insulare, they could provide
refuges for the parasitoid when the Brassica crops field is sprayed with pesticide.
Com-soybean intercropping provides shade, reduced wind speed, alternate foods,
and higher humidity and lower temperatures for soybean 'natural enemies (T onhasca
1993).

3. Planting a few rows of small trees, that simulate a woodland edge, on the
west side of the field could be beneficial. Besides providing shelter for D. insulare
during hot days it also could protect the B. thuringiensis toxin. if applied, from
the exposure to the intense UV light in the afternoon hours (Beegle et al. 1981).
Trees, such as basswood species that provided a very significant food source of
nectar for honey bees (Ayers & Batchtell 1995) and probably for D. insulare, can
be used for the above purposes.

4. Wildflowers should be planted, as suggested above, before we plant
Brassica crops. It could be a year ahead for D. carota, or in the fall for B. vulgaris
and B. kaber. Therefore, parasitoids can be retained or stay longer in or around the
field (Hagen et al. 1984). and the impact of D. insulare and other natural enemies
on diamondback moth could be enhanced. The availability of food sources for the
natural enemies in and around the field can overcome the need for mass releases of
biocontrol agents (Wackers & Swaan 1993). Certain wildflowers, such as B.
juncea, can serve as a trap crop because diamondback moth prefers to oviposit on
this weed rather than on the Brassica crops (Srinivasan & Krishna Moorthy 1991).

Weeds also can act as a point of spore dissemination for insect pathogen because

 

167
insects infected with Entomopthora spp. usually will climb to top of weed canopy
before die (Haynes et al., 1980).

5. Planting selected Brassica crops cultivars that reduce diamondback moth
oviposition and larval survival (Chapter 6)(Stoner 1990, Eigenbrode & Shelton
1990 & 1992) but still allow parasitism by D. insulare (Chapter 6, Lasota & Kok
1986) is also important. In addition. planting of crops or weeds with more
extended production of nectar sources close to Brassica crop field would increase
the retention of D. insular-e in the field (Wiicker & Swaah 1993). Some species of
Scrophulariaceae (figwort family) might be especially useful for extended nectar

production (Ayers et al. 1987 & 1991).

Intercropping is probably more easily accepted by farmers in the developing
countries because it has been a common cultural practice for them where two or more crops
and/or wild plants are grown simultaneously. sometime unintentionally, in the same field
(Perrin & Phillips 1978). In more intensive farming, in the developed countries,
intercropping seems to be inappropriate because of the difficulties with management and
harvesting, particularly where specialized machinery is used. Herbicide use also
complicates intercropping. In my opinion the second crop in an intercropping system could
be treated as the less important crop and grown purely to attract pests away from the
primary crop or to change the environment to promote the activity of natural enemies. In
cotton/sesame intercropping using row strips of sesame constituting 5% of the total
acreage, both these objectives were achieved (Pair et al. 1982). The’sesame was highly
attractive to Heliothis species from the seedling stage through the senescence and attracted
an otherwise obscure parasitoid species, Campoletis sonorensis. This species, attracted

only in the presence of sesame, parasitized large numbers of Heliothis species (Pair et al.

1982).

 

168
Although all the above suggestions would enhance the impact of D. insulare as an
important biocontrol agent in integrated diamondback moth management, I personally think
that its impact could be optimized if further study in the following areas are conducted.

1. It is important to identify of the stimuli and mechanism involved in food
detection by D. insulare. The relative suitability of food sources is not determined
only by its availability and quality but also by their detectability. Floral fragrances
and visual stimuli determine detectability of floral nectar by C. rubecula (Wiickers
1994).

2. We should continue a thorough search for alternate hosts of D. insulare
(Chapter 7). It is crucial to find altemate host because we can mix the plant(s) that

found to act as host plant for D. insulare's alternate hosts in Brassica polyculture or

 

intercropping system.

3. Effects of the interaction between different patch sizes with plant density
on both diamondback moth population dynamics and parasitism by D. insulare are
important. Until my research, only the effect of different patch sizes on the
diamondback population abundance has been studied (Pimental 1985). There is no
study on the effect of either plant density or patch sizes on D. insulare population
dynamics.

4. Since intercropping seems possible to use in managing diamondback
moth population and D. insulare. study should also be conducted on the impact of
this practice on other diamondback moth natural enemies. especially egg and pupal
parasitoids. This is important because D. insulare can only kill diamondback
moth's larvae. Effects on other pest and beneficial insects should be studied.

Zhao et al. (1992) suggested that effects of intercropping with nectar producing

plants will be different for different pest and beneficial species.

169
5. Developing a model. based on the weather information, D. insulare's
diurnal foraging activity and pesticide residue activity. to predict the best time for

pesticide spraying could also help integrate pesticides and biological control.

Much research remains to be done before an optimal diamondback moth
management system can be designed. However, these studies on parasitoid ecology and
behavior and parasitoid-diamondback moth-host plant tritropic interactions will increase our
ability to effectively use D. insular-e in a system to manage diamOndback moth. Similar
studies on other parasitoid—pest-host plant systems could improve management of these
pests as well. Only by accepting and studying pest management in a multicrop or regional

perspective can we design systems optimal for long term sustainable management.

ll

 

 

 

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170

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induced variation in Brassica nigra. Entomol. Exp. Appl. 27: 223-232.

 

192

Workman, R. G., R. B. Chalfant, & D. J. Schuster. 1981. Management of
the cabbage looper (Trichoplusia m) and diamondback moth (Plutella xylostella) on

cabbage by using 2 damage tresholds and insecicide treatments. J. Econ. Entomol.
73: 757-758.

Wiihrer, B. G. & S. A. Hassan. 1993. Selection of effective species/strains of
Trichogramma (Hym., Trichogrammatidae) to control the diamondback moth
Plutella xylostella L. (Lep., Plutellidae). J. Appl. Entomol. 116: 80 ~89.

Yamada, H. T., & T. Koshihara. 1987. A simple mass rearing method of
diamondback moth. Plant Protection 28: 253-256.

Yang, J-C Y-I. CHU, & N. S. Talekar. 1993. Biological studies of Diadegma
semiclausum (Hym., Ichneumonidae), a parasite of diamondback moth.
Entomophaga 38: 579- 586.

Yoshio, M. 1987. Simultaneous trap catches of the oriental armyworm and

diamondback moth during the early flight season at Morioko, Japan. Jpn. Appl.
Entomol. 2001. 31: 138-143.

Zhao, J. Z, G. S. Ayers, E. J. Grafius, & F. W. Stehr. 1992. Effects of
neighboring nectar-producing plants on populations of pest Lepidoptera and their
parasitoids in broccoli plantings. Great Lakes Entomol. 25: 253-258.

 

 

ll

 

 

APPENDIX

 

 

 

193

APPENDIX 1

Record of Deposition of Voucher Specimens*

The specimens listed on the following sheet(s) have been deposited in
the named museum(s) as samples of those species or other taxa which were
used in this research. Voucher recognition labels bearing the Voucher
No. have been attached or included in fluid-preserved specimens.

1995-3

Voucher No.:

 

Title of thesis or dissertation (or other research projects):
Ecology and Behavior of Diadegma insulare (Cresson), a

Biological Control Agent of Diamondback Moth, Plutella xylostella (L.)

Museum(s) where deposited and abbreviations for table on following sheets:
Entomology Museum, Michigan State University (MSU)

Other Museums:

None

Investigator's Name (3) (typed)
Idris Bin Abd. Ghani

Department of’Entomology
Michigan State University
Date June 30, 199;

*Reference: Yoshimoto, C. M. 1978. Voucher Specimens for Entomology in
North America. Bull. Entomol. Soc. Amer. 24:141-42.

Deposit as follows:

Original: Include as Appendix 1 in ribbon copy of thesis or
dissertation.

Copies: Included as Appendix 1 in copies of thesis or dissertation.
Museum(s) files.
Research project files.

This form is available from and the Voucher No. is assigned by the Curator,
Michigan State University Entomology Museum.

 

Pages

1

_—

194

APPENDIX 1.1
of

1

Voucher Specimen Data

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APPENDIX 2

Evidence of Pre-imaginal Overwintering of Diamondback Moth, Plutella
xylostella (L.)(Plutellidae) in Michigan

 

ll

 

 

195

Evidence of Pre-imaginal Overwintering of Diamondback moth, Plutella

xylostella (L.)(Lepidoptera: Plutellidae) in Michigan

ABSTRACT

I investigated the possibility of overwintering diamondback moth, Plutella
xylostella L., at the Michigan State University Research Field. I inspected 550 to 600 (50-
70 of each species every 5 (1) early spring season weeds; Barbarea vulgaris R. Br., Thalpsi
arvense L. and Capsella bursa-pastoris (L.) Medic, for diamondback moth eggs, larvae and
pupae on 10, 15, 20 and 25 May 1993. One diamondback moth third and 24 fourth instars
were found but no eggs. On 25 May, however, three first instars were found. In the
laboratory, I recorded more first instar from detached weed leaves collected on 20 and 25
May than in direct field inspection. This suggests an oviposition occurred sometime in
Mid-May, and egg hatch was delayed or that mortality of early instars was higher in the
field than in the laboratory. Four pupae were also collected on 20 and 25 May, indicating
they originated from the overwintering late instars of diamondback moth. Plant debris or
sod may protect the overwintering larvae because the temperature in the debris is higher
than the air temperature. 1 suggest further research on overwintering site of diamondback
moth and D. insulare should be conducted although Diadegma insulare (Cresson) pupae

and parasitized diamondback moth larvae were not found in our investigation.

 

196

INTRODUCTION

Diamondback moth, Plutella .rylostella L., is a major Brassica crops pest
worldwide. In Michigan, it commonly occurs at relatively low population densities, rarely
reaching outbreak levels. This is probably due to the abundance of Diadegma insulare
(Cresson)(Hymenoptera: Ichneumonidae), a larval parasitoid, that regulates diamondback
moth populations. Parasitism rates of 70-100 percent were reported in the US (Biever et
al. 1992, Idris & Grafius 1993) and Canada (Harcourt 1986).

Diamondback moth is believed not to overwinter in Canada. For example, in
southem Ontario, Smith & Sears (1982) found that no diamondback moth life stages
survived winter conditions in the field, or simulated winter conditions in the laboratory.
Populations are thought to die out completely each year to be replaced in spring by migrants
from the south (Philip and Mengersen 1989). Recent observations indicated that pre-
imaginal stages of diamondback moth may successfully overwinter in Alberta, and that
volunteer canola plants provided an early larval food source (Dosdall 1994).

In United States, diamondback moth adults apparently overwinter beneath crop
debris in Colorado (Marsh 1917) and New York (Harcourt 1957). In upper midwestem
States (Michigan, Wisconsin and Minnesota), diamondback moth populations are not
thought to overwinter but early infestations often occur near Brassica crops debris,
indicating that overwintering of adults in protected areas is possible (Mahr et al. 1993).

The objectives of my study were to determine whether diamondback moth

overwinters in Michigan, and to identify possible overwintering life stages.

 

197
MATERIALS AND METHODS

In early spring 1993, three weed species, Barbarea vulgaris R. Br., Thalspi arvense

 

 

 

L. and Capsella bursa-pastoris (L.) Medic were abundant in the previous season broccoli
experimental field at the Michigan State University Collins Road Entomology Research
Farm and other areas at the Michigan State University Farm. On 10, 15, 20 and 25 May, I
selected the above weeds randomly from any patches they grew. The plants were pulled
out of the ground and inspected for the presence of diamondback moth larvae or pupae by
placing individual weeds on white paper placed on the ground. The number of larvae and
pupae found on each weed species were recorded separately. I reared larvae in 25 x 15 x

10 cm covered rearing pans in the laboratory at 25 1: 20C and photoperiod of 16:8 (L:D) h

 

until pupation, to evaluate parasitism.

To determine the presence of diamondback moth eggs I randomly selected and
detached leaves from each plant. Detached leaves (by species) were kept in the laboratory
as described above and checked daily for 5 d for egg hatch.

Overwintering of adult diamondback moth was evaluated by setting up five cages
(180 x 165 x 165 cm) in and near our experimental field previously planted with
broccoliprevious broccoli field in early April 1993. I pulled up broccoli plant residue by
hand and put the remains of 5070 plants in each cage. To catch the emerged diamondback
moth adults I hung white sticky trap (PheroconTM 1C - bottom; Trece lnc.. Salinas, CA) on
a wood stake. Sticky traps were inspected for diamondback moth adult emergence every
other day. I also put five potted broccoli plants in each cage for the emerged adults to lay
eggs. The presence of diamondback moth's eggs or larvae on broccoli leaves was checked
using a 10x magnifying glass once every 3 d. Traps and the presence of eggs or larvae
were monitored until end of May 1993.

The Michigan State University Climatological Resources Center (Dr. Jeff

Andresen) provided air and soil temperature data Degree-days (dd) accumulation above

ll

 

198

7.30C, developmental threshold for diamondback moth (Butts & McEwen 1981), was
calculated following Zalom et al. (1983).

RESULTS AND DISCUSSION

I found 24 fourth instar diamondback moths from the three early spring season
weeds (Table 1). They were found on the first sample data, 10 May. One late third instar
was also found on B. vulgaris on 10 May. Most larvae and eggs were found on B.
vulgaris. There were no eggs collected before 20 May (based on the larvae from detached
leaves collected on this date, Table 1). I did not find any diamondback moth first or second

instars before 25 May. On 25 May. however, three first instars were recorded from B.

 

vulgaris. On the same day we found three pupae from B. vulgaris and one from C. bursa-
pastoris. There were 11 and 23 diamondback moth first instars recorded from the detached
leaves collected on 20 and 25 May, respectivey. No Diadegma insulare (Cresson)
(Hymenoptera: Ichneumonidae) or other parasitoids pupae were recorded from weeds
inspected in the field or reared from diamondback moth fourth instars. There were no
diamondback moth adults caught by the sticky traps in the field cages. I did not find
diamondback moth eggs or larvae on leaves of potted broccoli pots placed inside the cages.
The average daily maximum air temperature and soil temperature above sod or
debris surface was relatively similar (Fig. 1 A & B). However, the minimum temperature
above debris was warmer than the air temperature. In December 1992, and from January
to March 1993, the air and soil temperature were much lower than 73°C, but the numbers
of days below freezing were higher (28 > 20 d) than in the other months of both years
(Fig. l A to C). In February 1993. when average temperature was the lowest. it snowed
for 17 d (Fig. 1 C), causing accumulation of snow above the ground. The total degree-

days (dd) above 73°C was 45.8 dd from December 1992 to January through March 1993.

199

Table 1. Diamondback moth larvae or pupae or first instar counted from weeds and
detached weed leaves

 

 

 

 

 

 

Diamondback Moth
Weed species Dates Larvae‘I
Pupaeb First instar from
1st 2nd 3rd 4th detached leavcsC
Barbarea 10 May 0 0 1 2 0 0
vulgar-is R. Br. 15 May 0 0 0 3 0 0
20 May 0 0 0 6 1 l 1
25 May 3 0 0 4 2 23
Thalspi arvense L. 10 May 0 0 0 l 0 0
15 May 0 0 0 0 0 0
20 May 0 0 0 l 0 3
25 May 0 0 0 2 0 6
Capsella 10 May 0 0 0 0 0 0
bursa-pastoris (L.) 15 May 0 0 0 l 0 0
Medic 20 May 0 0 0 0 0 2
25 May 0 0 0 l l 8
Total 3 0 0 2 4 4 5 3

 

a No parasitoid pupae formed from field collected larvae that were reared in laboratory
17 No parasitoid pupae were found

C First diamondback moth instar originated from eggs laid on weed leaves that were

detached and brought to laboratory on the stated date

200

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201
but it was 217 dd from October through December 1992 to January through April 1993
(Fig. l D).

The above results clearly indicate overwintering of DBM larvae is occuring in
Michigan. Overwintering is supported by the fact that first, there were no eggs or first and
second (early) instars found until long after the third or fourth (late) instars (Table 1). The
diamondback moth late instars are reported to have very low super cooling points
(-14.3"C), suggesting that some of them can tolerate below sub-freezing temperature
(Hayakawa et al. 1988). Higher temperature in or below the debris than above the debris
surface and higher accumulation of snow in February than in the other months (Fig. 1C)
were also likely protecting the diamondback moth larvae. Diamondback moth larvae may
have begun to enter diapause in November 1992 when weeds were dead (no food
available). and the minimum and maximum air temperature were less than 7.30C (Fig. 1
A). The successful overwintering larvae may have continued development in late April
1993, when early season weeds flourished (food became abundance) and temperature was
moderate (Fig. l A).

Secondly, the developmental period of diamondback moth larvae from hatch to the
third or fourth instars found in this study required 110 or 170 dd above 73°C (Butts &
McEwen 1981). Butts & McEwen (1981) reported that the second. third and fourth instars
required 70, 60 or 40 dd to become third, fourth or pupae respectively. In England, Hardy
(1938) reported that developmental period of the diamondback moth larvae (from batch to
pupation) was over two months at 10°C. At above 73°C. the degree-days accumulated in
late April was 80.2 dd and in May was 422.8 dd (0C)(Fig. l D). Degree-day accumulation
required by diamondback moth to complete one generation is 293 dd (0C)(Butts &
McEwen 1981). According to these heat unit accumulation we would expect diamondback
moth first and second instars to overwinter successfully. In the laboratory, however, I
observed these two larval stages survived for only a week when placed in empty 15.0 cm

diam Petri dishes and kept at 4°C, while the third and fourth instars survived over two

 

202
months (unpublished data). This suggests that the diamondback moth third and fourth
instars were the one that successfully overwintering. At the time of sampling,
overwintered third or fourth instars should have been in the fourth or pupated. However, I
found only four pupae on 20 and 25 May, perhaps due to predation. The development of
diamondback moth third and fourth instars may be prolonged because the weed leaves or
flower buds are not the best food for this insect (personal observation). Otherwise these
late instars should have been pupating at the time of sampling (based on the accumulated
degree-days, Fig. 1 D and Butts & McEwen 1981).

Thirdly, diamondback moth pupae may overwinter within or under the debris.
They can also tolerate super-cooling down to -19.2°C (Hayakawa et al. 1988). However,
at above 73°C, the development from pupae to adult would require 100 dd (Butts &
McEwen 1981). Mortality of an egg is 100% at below 10°C (Hardy 1938)(the maximum
air temperature between mid-October 1992 to week three of April 1993 was lower than
10°C, Fig. 1 A) or if exposed to chilling temperature for 60 (1 (Honda 1992). This
suggests that our field collected larvae did not originate from adults emerged from any
overwintering diamondback moth's pupae.

Fourth, in my field cage study, there were no diamondback moth eggs observed or
adults caught even though they were monitored until the end of May. This suggests that
adult moths did not overwinter in Michigan. Similarly, in Alberta, Canada, diamondback
moth adults were first caught by the emergence traps on 26 May, indicating adults may
originate from the successful overwintering larvae (Dosdall 1994).

Fifth, in southem Ontario, Canada. where temperature is similar to Mid-Michigan
area, diamondback moth adults arrive from the southern United States around mid-May
(Harcourt 1986). This tends to agree with my result that showed there were considerable
numbers of first instars recorded from the detached leaves collected on the 20 and 25 May,
suggesting an oviposition began in Mid-May, 1993 (Table 1). If oviposition occurred, the

developmental time from egg hatch to third or fourth instars would require 23 d at 20°C

 

203
(Salinas 1986). Therefore, it is impossible that larvae collected in this study were the
offspring of these migrants.

Six, the average daily maximum air temperature was lower then 7°C in March 1993
(Fig. l A), and no oviposition observed at this temperature (Hardy 1938). Oviposition by
the successful overwintered diamondback moth adults could occur in late April when the
average daily maximum air temperature was at 12°C, but it would require 13 d for egg to
hatch (Hardy 1938). If this happened then the diamondback moth first instars should have
been in the field and collected on 10 May (my first sampling date). On this date, however,
only third and fourth instars were found (T able 1). Therefore, if any diamondback moth
adults successfully pass the winter they could not be the source for the larvae that I
collected.

D. insulare females may not be that active in late fall especially in October or
November. Therefore, less diamondback moth larvae were parasitized and of these only
few or none survive the winter (none in my collection). I did observe D. insulare adults
foraging for host on 25 May. They may have originated from overwintering cocoons since
D. insulare is apparently not as good a migrant as diamondback moth adults (Putnam

1978).
CONCLUSIONS

This is the first evidence of pre-imaginal diamondback moth successfully
overwintering in Michigan and other states in the northern U.S. However, the numbers of
successful overwintering individuals may be significantly reduced in colder winters.

This result indicates the importance of proper treatment on the previous Brassica
crops field for managing diamondback moth. Tilling of field before planting is a common
practice that may indirectly destroy overwintering diamondback moth, D. insulare pupae or

parasitized larvae although no D. insulare pupae or parasitized larvae were found in this

 

204

study. Further research on overwintering sites for diamondback moth and D. insular-e
should conducted. For example, by carrying out several tillages or other practices on the

previous field that may reduce diamondback moth but increase D. insulare survival.

REFERENCES CITED

Biever, K. D. , R. L. Chauvin, G. L. Reed, & R. C. Wilson. 1992.
Seasonal occurrence and abundance of lepidopterous pests and associated

parasitoids on collards in the northwestern United States. J. Entomol. Sci. 27: 5-
18.

Butts, R. A. & F. L. McEwen. 1981. Seasonal populations of the diamondback
moth Plutella xylostella (Lepidoptera: Plutellidae) in relation to day-degree
accumulation. Can. Entomol. 113: 127-131.

Dosdall, L. M. 1994. Evidence for successful overwintering of diamondback moth,
Plutella xylostella (L.) (Lepidoptera: Plutellidae), in Alberta. Can. Entomol. 126:
183-185.

Hardy, J. E. 1938. Plutella maculipennis, Curt., its natural and biological control in
England. Bull. Entomol. Res. 29: 343-373.

Harcourt, D. G. 1986. Population dynamics of the diamondback moth in southern
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Griggs (eds.). Proceeding of the First International Workshop. Asian
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1985.

Harcourt, D.G. 1957. Biology of the diamondback moth, Plutella maculipennis
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Entomol. 89: 554-564.

Hayakawa, H., H. Tsutsui, & C. Goto. 1988. A survey of overwintering of the
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Honda, K. 1992. Hibernation and migration of diamondback moth in northern Japan.
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Idris A. B. & E. Grafius. 1993. Field studies on the impact of pesticides on the
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by Diadegma insulare (Cresson)(Hymenoptera: Ichneumonidae). J. Econ.
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Mahr, S. E. R., D. L. Mahr, & J. A. Wyman. 1993. Biological control of insect
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Marsh, 0. H. 1917. The life history of Plutella maculipennis, the diamondback moth.
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Salinas, P. D. 1986. Studies on diamondback moth in Venezuela with reference to
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Coperative Extension, University of California, Berkeley. Leaflet 21373. 10 pp.

 

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